The programming power of the placenta

Frontiers in Physiology

Volumn 7, Issue MAR, 2016, Pages

  Sferruzzi Perri, Amanda N ^a   Camm, Emily J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Fetus; Maternal environment; Nutrient transport; Placenta; Pregnancy; Programming

Indexed keywords

BRAIN SIZE; CATCH UP GROWTH; ENVIRONMENTAL FACTOR; FETUS GROWTH; FETUS WEIGHT; HUMAN; KIDNEY STRUCTURE; MATERNAL WELFARE; NONHUMAN; PHENOTYPE; PHYSIOLOGICAL PROCESS; PLACENTA WEIGHT; PLACENTAL TRANSFER; PROGENY; REVIEW;

EID: 84964599265     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2016.00033     Document Type: Review

References (255)

1. Ahokas, R. A., Anderson, G. D., and Lipshitz, J. (1983). Effect of dietary restriction, during the last week only or throughout gestation, on cardiac output and uteroplacental blood flow in pregnant rats. J. Nutr. 113, 1766-1776.
2. Ahokas, R. A., Lahaye, E. B., Anderson, G. D., and Lipshitz, J. (1981). Effect of maternal dietary restriction on fetal growth and placental transfer of alpha-amino isobutyric acid in rats. J. Nutr. 111, 2052-2058.
3. Ain, R., Dai, G., Dunmore, J. H., Godwin, A. R., and Soares, M. J. (2004). A prolactin family paralog regulates reproductive adaptations to a physiological stressor. Proc. Natl. Acad. Sci. USA. 101, 16543-16548. doi: 10.1073/pnas.0406185101
4. Alam, S. M., Konno, T., Dai, G., Lu, L., Wang, D., Dunmore, J. H., et al. (2007). A uterine decidual cell cytokine ensures pregnancy-dependent adaptations to a physiological stressor. Development 134, 407-415. doi: 10.1242/dev.02743
5. Alexander, B. T., Kassab, S. E., Miller, M. T., Abram, S. R., Reckelhoff, J. F., Bennett, W. A., et al. (2001). Reduced uterine perfusion pressure during pregnancy in the rat is associated with increases in arterial pressure and changes in renal nitric oxide. Hypertension 37, 1191-1195. doi: 10.1161/01.HYP.37.4.1191
6. Almeida, S. S., Tonkiss, J., and Galler, J. R. (1996). Prenatal protein malnutrition affects exploratory behavior of female rats in the elevated plus-maze test. Physiol. Behav. 60, 675-680. doi: 10.1016/S0031-9384(96)80047-3
7. Alves, M. B., Dalle Molle, R., Desai, M., Ross, M. G., and Silveira, P. P. (2015). Increased palatable food intake and response to food cues in intrauterine growth-restricted rats are related to tyrosine hydroxylase content in the orbitofrontal cortex and nucleus accumbens. Behav. Brain Res. 287, 73-81. doi: 10.1016/j.bbr.2015.03.019
8. Alzamendi, A., Del Zotto, H., Castrogiovanni, D., Romero, J., Giovambattista, A., and Spinedi, E. (2012). Oral metformin treatment prevents enhanced insulin demand and placental dysfunction in the pregnant rat fed a fructose-rich diet. ISRN Endocrinol. 2012, 757913. doi: 10.5402/2012/757913
9. Anevska, K., Gallo, L. A., Tran, M., Jefferies, A. J., Wark, J. D., Wlodek, M. E., et al. (2015). Pregnant growth restricted female rats have bone gains during late gestation which contributes to second generation adolescent and adult offspring having normal bone health. Bone 74, 199-207. doi: 10.1016/j.bone.2015.01.018
10. Armitage, J. A., Khan, I. Y., Taylor, P. D., Nathanielsz, P. W., and Poston, L. (2004). Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals? J. Physiol. 561, 355-377. doi: 10.1113/jphysiol.2004.072009
11. Bacon, B. J., Gilbert, R. D., Kaufmann, P., Smith, A. D., Trevino, F. T., and Longo, L. D. (1984). Placental anatomy and diffusing capacity in guinea pigs following long-term maternal hypoxia. Placenta 5, 475-487. doi: 10.1016/S0143-4004(84)80002-8
12. Barker, D. J. (2004a). The developmental origins of adult disease. J. Am. Coll. Nutr. 23, 588S-595S. doi: 10.1080/07315724.2004.10719428
13. Barker, D. J. (2004b). The developmental origins of well-being. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359, 1359-1366. doi: 10.1098/rstb.2004.1518
14. Barker, D. J. (2004c). Developmental origins of adult health and disease. J. Epidemiol. Comm. Health 58, 114-115. doi: 10.1136/jech.58.2.114
15. Barker, D. J., Gelow, J., Thornburg, K., Osmond, C., Kajantie, E., and Eriksson, J. G. (2010b). The early origins of chronic heart failure: impaired placental growth and initiation of insulin resistance in childhood. Eur. J. Heart Fail. 12, 819-825. doi: 10.1093/eurjhf/hfq069
16. Barker, D. J., Hales, C. N., Fall, C. H., Osmond, C., Phipps, K., and Clark, P. M. (1993). Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36, 62-67. doi: 10.1007/BF00399095
17. Barker, D. J., Larsen, G., Osmond, C., Thornburg, K. L., Kajantie, E., and Eriksson, J. G. (2012). The placental origins of sudden cardiac death. Int. J. Epidemiol. 41, 1394-1399. doi: 10.1093/ije/dys116
18. Barker, D. J., and Osmond, C. (1986). Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1, 1077-1081. doi: 10.1016/S0140-6736(86)91340-1
19. Barker, D. J., Osmond, C., Forsen, T. J., Thornburg, K. L., Kajantie, E., and Eriksson, J. G. (2013c). Foetal and childhood growth and asthma in adult life. Acta Paediatr. 102, 732-738. doi: 10.1111/apa.12257
20. Barker, D. J., Osmond, C., Thornburg, K. L., Kajantie, E., and Eriksson, J. G. (2011). The lifespan of men and the shape of their placental surface at birth. Placenta 32, 783-787. doi: 10.1016/j.placenta.2011.07.031
21. Barker, D. J., Osmond, C., Thornburg, K. L., Kajantie, E., and Eriksson, J. G. (2013a). The shape of the placental surface at birth and colorectal cancer in later life. Am. J. Hum. Biol. 25, 566-568. doi: 10.1002/ajhb.22409
22. Barker, D. J., Osmond, C., Thornburg, K. L., Kajantie, E., and Eriksson, J. G. (2013b). The intrauterine origins of Hodgkin's lymphoma. Cancer Epidemiol. 37, 321-323. doi: 10.1016/j.canep.2013.01.004
23. Barker, D. J., Thornburg, K. L., Osmond, C., Kajantie, E., and Eriksson, J. G. (2010a). The surface area of the placenta and hypertension in the offspring in later life. Int. J. Dev. Biol. 54, 525-530. doi: 10.1387/ijdb.082760db
24. Barker, D. J., Thornburg, K. L., Osmond, C., Kajantie, E., and Eriksson, J. G. (2010c). The prenatal origins of lung cancer. II. The placenta. Am. J. Hum. Biol. 22, 512-516. doi: 10.1002/ajhb.21041
25. Barker, D. J., Winter, P. D., Osmond, C., Margetts, B., and Simmonds, S. J. (1989). Weight in infancy and death from ischaemic heart disease. Lancet 2, 577-580. doi: 10.1016/S0140-6736(89)90710-1
26. Belkacemi, L., Desai, M., Nelson, D. M., and Ross, M. G. (2011b). Altered mitochondrial apoptotic pathway in placentas from undernourished rat gestations. Am. J. Physiol. Regul. Integr. Comp. Physiol. 301, R1599-R1615. doi: 10.1152/ajpregu.00100.2011
27. Belkacemi, L., Jelks, A., Chen, C. H., Ross, M. G., and Desai, M. (2011a). Altered placental development in undernourished rats: role of maternal glucocorticoids. Reprod. Biol. Endocrinol. 9, 105. doi: 10.1186/1477-7827-9-105
28. Bellisario, V., Panetta, P., Balsevich, G., Baumann, V., Noble, J., Raggi, C., et al. (2015a). Maternal high-fat diet acts as a stressor increasing maternal glucocorticoids' signaling to the fetus and disrupting maternal behavior and brain activation in C57BL/6J mice. Psychoneuroendocrinology 60, 138-150. doi: 10.1016/j.psyneuen.2015.06.012
29. Bellisario, V., Panetta, P., Balsevich, G., Baumann, V., Noble, J., Raggi, C., et al. (2015b). High-fat diet during pregnancy acts as a stressor increasing maternal glucocorticoids' signaling to the fetus and disrupting maternal behavior in a mouse model. Psychoneuroendocrinology 61, 10-10. doi: 10.1016/j.psyneuen.2015.07.414
30. Black, M. J., Siebel, A. L., Gezmish, O., Moritz, K. M., and Wlodek, M. E. (2012). Normal lactational environment restores cardiomyocyte number after uteroplacental insufficiency: implications for the preterm neonate. Am. J. Physiol. Regul. Integr. Comp. Physiol. 302, R1101-R1110. doi: 10.1152/ajpregu.00030.2012
31. Blesson, C. S., Sathishkumar, K., Chinnathambi, V., and Yallampalli, C. (2014). Gestational protein restriction impairs insulin-regulated glucose transport mechanisms in gastrocnemius muscles of adult male offspring. Endocrinology 155, 3036-3046. doi: 10.1210/en.2014-1094
32. Brawley, L., Itoh, S., Torrens, C., Barker, A., Bertram, C., Poston, L., et al. (2003). Dietary protein restriction in pregnancy induces hypertension and vascular defects in rat male offspring. Pediatr. Res. 54, 83-90. doi: 10.1203/01.PDR.0000065731.00639.02
33. Breton, C., Lukaszewski, M. A., Risold, P. Y., Enache, M., Guillemot, J., Riviere, G., et al. (2009). Maternal prenatal undernutrition alters the response of POMC neurons to energy status variation in adult male rat offspring. Am. J. Physiol. Endocrinol. Metab. 296, E462-E472. doi: 10.1152/ajpendo.90740.2008
34. Burdge, G. C., Slater-Jefferies, J., Torrens, C., Phillips, E. S., Hanson, M. A., and Lillycrop, K. A. (2007). Dietary protein restriction of pregnant rats in the F0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. Br. J. Nutr. 97, 435-439. doi: 10.1017/S0007114507352392
35. Caminos, J. E., Bravo, S. B., Gonzalez, C. R., Garces, M. F., Cepeda, L. A., Gonzalez, A. C., et al. (2008). Food-intake-regulating-neuropeptides are expressed and regulated through pregnancy and following food restriction in rat placenta. Reprod. Biol. Endocrinol. 6, 14. doi: 10.1186/1477-7827-6-14
36. Camm, E. J., Hansell, J. A., Kane, A. D., Herrera, E. A., Lewis, C., Wong, S., et al. (2010). Partial contributions of developmental hypoxia and undernutrition to prenatal alterations in somatic growth and cardiovascular structure and function. Am. J. Obstet. Gynecol. 203, 495.e24-495.e34. doi: 10.1016/j.ajog.2010.06.046
37. Camm, E. J., Martin-Gronert, M. S., Wright, N. L., Hansell, J. A., Ozanne, S. E., and Giussani, D. A. (2011). Prenatal hypoxia independent of undernutrition promotes molecular markers of insulin resistance in adult offspring. FASEB J. 25, 420-427. doi: 10.1096/fj.10-158188
38. Carter, A. M., Kingston, M. J., Han, K. K., Mazzuca, D. M., Nygard, K., and Han, V. K. (2005). Altered expression of IGFs and IGF-binding proteins during intrauterine growth restriction in guinea pigs. J. Endocrinol. 184, 179-189. doi: 10.1677/joe.1.05781
39. Chakraborty, D., Rumi, M. A., Konno, T., and Soares, M. J. (2011). Natural killer cells direct hemochorial placentation by regulating hypoxia-inducible factor dependent trophoblast lineage decisions. Proc. Natl. Acad. Sci. U.S.A. 108, 16295-16300. doi: 10.1073/pnas.1109478108
40. Chen, P. Y., Ganguly, A., Rubbi, L., Orozco, L. D., Morselli, M., Ashraf, D., et al. (2013). Intrauterine calorie restriction affects placental DNA methylation and gene expression. Physiol. Genomics 45, 565-576. doi: 10.1152/physiolgenomics.00034.2013
41. Clayton, Z. E., Vickers, M. H., Bernal, A., Yap, C., and Sloboda, D. M. (2015). Early life exposure to fructose alters maternal, fetal and neonatal hepatic gene expression and leads to sex-dependent changes in lipid metabolism in rat offspring. PLoS ONE 10:e0141962. doi: 10.1371/journal.pone.0141962
42. Cleal, J., and Lewis, R. (2008). The Mechanisms and Regulation of Placental Amino Acid Transport to the Human Foetus. J. Neuroendocrinol. 20, 419-426. doi: 10.1111/j.1365-2826.2008.01662.x
43. Clifton, V. L. (2010). Review: sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta 31(Suppl.), S33-S39. doi: 10.1016/j.placenta.2009.11.010
44. Coan, P. M., Vaughan, O. R., McCarthy, J., Mactier, C., Burton, G. J., Constancia, M., et al. (2011). Dietary composition programmes placental phenotype in mice. J. Physiol. 589, 3659-3670. doi: 10.1113/jphysiol.2011.208629
45. Coan, P. M., Vaughan, O. R., Sekita, Y., Finn, S. L., Constancia, M., Burton, G. J., et al. (2010). Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice. J. Physiol. 588, 527-538. doi: 10.1113/jphysiol.2009.181214
46. Connor, K. L., Vickers, M. H., Beltrand, J., Meaney, M. J., and Sloboda, D. M. (2012). Nature, nurture or nutrition? Impact of maternal nutrition on maternal care, offspring development and reproductive function. J. Physiol. 590, 2167-2180. doi: 10.1113/jphysiol.2011.223305
47. Connor, K. L., Vickers, M. H., Cupido, C., Sirimanne, E., and Sloboda, D. M. (2010). Maternal high fat diet during critical windows of development alters adrenal cortical and medullary enzyme expression in adult male rat offspring. J. Dev. Orig. Health Dis. 1, 245-254. doi: 10.1017/S2040174410000346
48. Coupe, B., Dutriez-Casteloot, I., Breton, C., Lefevre, F., Mairesse, J., Dickes-Coopman, A., et al. (2009). Perinatal undernutrition modifies cell proliferation and brain-derived neurotrophic factor levels during critical time-windows for hypothalamic and hippocampal development in the male rat. J. Neuroendocrinol. 21, 40-48. doi: 10.1111/j.1365-2826.2008.01806.x
49. Cramer, S., Beveridge, M., Kilberg, M., and Novak, D. (2002). Physiological importance of system A-mediated amino acid transport to rat fetal development. Am. J. Physiol. Cell Physiol. 282, C153-C160.
50. Crowe, C., Dandekar, P., Fox, M., Dhingra, K., Bennet, L., and Hanson, M. A. (1995). The effects of anaemia on heart, placenta and body weight, and blood pressure in fetal and neonatal rats. J. Physiol. 488 (Pt 2), 515-519. doi: 10.1113/jphysiol.1995.sp020986
51. Cuffe, J. S., Walton, S. L., Singh, R. R., Spiers, J. G., Bielefeldt-Ohmann, H., Wilkinson, L., et al. (2014a). Mid-to late term hypoxia in the mouse alters placental morphology, glucocorticoid regulatory pathways and nutrient transporters in a sex-specific manner. J. Physiol. 592, 3127-3141. doi: 10.1113/jphysiol.2014.272856
52. Cuffe, J. S., Walton, S. L., Steane, S. E., Singh, R. R., Simmons, D. G., and Moritz, K. M. (2014b). The effects of gestational age and maternal hypoxia on the placental renin angiotensin system in the mouse. Placenta 35, 953-961. doi: 10.1016/j.placenta.2014.09.004
53. Dahlhoff, M., Pfister, S., Blutke, A., Rozman, J., Klingenspor, M., Deutsch, M. J., et al. (2014). Peri-conceptional obesogenic exposure induces sex-specific programming of disease susceptibilities in adult mouse offspring. Biochim. Biophys. Acta 1842, 304-317. doi: 10.1016/j.bbadis.2013.11.021
54. Das, U. G., Sadiq, H. F., Soares, M. J., Hay, W. W. Jr., and Devaskar, S. U. (1998). Time-dependent physiological regulation of rodent and ovine placental glucose transporter (GLUT-1) protein. Am. J. Physiol. 274, R339-R347.
55. Delahaye, F., Breton, C., Risold, P. Y., Enache, M., Dutriez-Casteloot, I., Laborie, C., et al. (2008). Maternal perinatal undernutrition drastically reduces postnatal leptin surge and affects the development of arcuate nucleus proopiomelanocortin neurons in neonatal male rat pups. Endocrinology 149, 470-475. doi: 10.1210/en.2007-1263
56. Delahaye, F., Lukaszewski, M. A., Wattez, J. S., Cisse, O., Dutriez-Casteloot, I., Fajardy, I., et al. (2010). Maternal perinatal undernutrition programs a "brown-like" phenotype of gonadal white fat in male rat at weaning. Am. J. Physiol. Regul. Integr. Comp. Physiol. 299, R101-R110. doi: 10.1152/ajpregu.00604.2009
57. de Rooij, S. R., Wouters, H., Yonker, J. E., Painter, R. C., and Roseboom, T. J. (2010). Prenatal undernutrition and cognitive function in late adulthood. Proc. Natl. Acad. Sci. U.S.A. 107, 16881-16886. doi: 10.1073/pnas.1009459107
58. Desai, M., Gayle, D., Babu, J., and Ross, M. G. (2005a). Programmed obesity in intrauterine growth-restricted newborns: modulation by newborn nutrition. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R91-R96. doi: 10.1152/ajpregu.00340.2004
59. Desai, M., Gayle, D., Babu, J., and Ross, M. G. (2005b). Permanent reduction in heart and kidney organ growth in offspring of undernourished rat dams. Am. J. Obstet. Gynecol. 193, 1224-1232. doi: 10.1016/j.ajog.2005.05.041
60. Desai, M., Gayle, D., Babu, J., and Ross, M. G. (2007b). The timing of nutrient restriction during rat pregnancy/lactation alters metabolic syndrome phenotype. Am. J. Obstet. Gynecol. 196, 555e1-7. doi: 10.1016/j.ajog.2006.11.036
61. Desai, M., Gayle, D., Han, G., and Ross, M. G. (2007a). Programmed hyperphagia due to reduced anorexigenic mechanisms in intrauterine growth-restricted offspring. Reproductive sciences 14, 329-337. doi: 10.1177/1933719107303983
62. Desai, M., Guang, H., Ferelli, M., Kallichanda, N., and Lane, R. H. (2008). Programmed upregulation of adipogenic transcription factors in intrauterine growth-restricted offspring. Reprod. Sci. 15, 785-796. doi: 10.1177/1933719108318597
63. Doherty, C. B., Lewis, R. M., Sharkey, A., and Burton, G. J. (2003). Placental composition and surface area but not vascularization are altered by maternal protein restriction in the rat. Placenta 24, 34-38. doi: 10.1053/plac.2002.0858
64. Dudley, K. J., Sloboda, D. M., Connor, K. L., Beltrand, J., and Vickers, M. H. (2011). Offspring of mothers fed a high fat diet display hepatic cell cycle inhibition and associated changes in gene expression and DNA methylation. PLoS ONE 6:e21662. doi: 10.1371/journal.pone.0021662
65. Duttaroy, A. K. (2009). Transport of fatty acids across the human placenta: a review. Prog. Lipid Res. 48, 52-61. doi: 10.1016/j.plipres.2008.11.001
66. Elmes, M. J., Gardner, D. S., and Langley-Evans, S. (2007). C., Fetal exposure to a maternal low-protein diet is associated with altered left ventricular pressure response to ischaemia-reperfusion injury. Br. J. Nutr. 98, 93-100. doi: 10.1017/S000711450769182X
67. Elmes, M. J., McMullen, S., Gardner, D. S., and Langley-Evans, S. C. (2008). Prenatal diet determines susceptibility to cardiac ischaemia-reperfusion injury following treatment with diethylmaleic acid and N-acetylcysteine. Life Sci. 82, 149-155. doi: 10.1016/j.lfs.2007.10.022
68. Fowden, A. L., Forhead, A. J., Coan, P. M., and Burton, G. J. (2008). The placenta and intrauterine programming. J. Neuroendocrinol. 20, 439-450. doi: 10.1111/j.1365-2826.2008.01663.x
69. Fowden, A. L., and Moore, T. (2012). Maternal-fetal resource allocation: co-operation and conflict. Placenta 33(Suppl. 2), e11-e15. doi: 10.1016/j.placenta.2012.05.002
70. Fowden, A. L., Sferruzzi-Perri, A. N., Coan, P. M., Constancia, M., and Burton, G. J. (2009). Placental efficiency and adaptation: endocrine regulation. J. Physiol. 587, 3459-3472. doi: 10.1113/jphysiol.2009.173013
71. Fowden, A. L., Ward, J. W., Wooding, F. P., Forhead, A. J., and Constancia, M. (2006). Programming placental nutrient transport capacity. J. Physiol. 572, 5-15. doi: 10.1113/jphysiol.2005.104141
72. Franko, K. L., Forhead, A. J., and Fowden, A. L. (2009). Effects of maternal dietary manipulation during different periods of pregnancy on hepatic glucogenic capacity in fetal and pregnant rats near term. Nutr. Metab. Cardiovasc. Dis. 19, 555-562. doi: 10.1016/j.numecd.2008.11.001
73. Fukami, T., Sun, X., Li, T., Desai, M., and Ross, M. G. (2012). Mechanism of programmed obesity in intrauterine fetal growth restricted offspring: paradoxically enhanced appetite stimulation in fed and fasting states. Reprod. Sci. 19, 423-430. doi: 10.1177/1933719111424448
74. Gabory, A., Ferry, L., Fajardy, I., Jouneau, L., Gothie, J. D., Vige, A., et al. (2012). Maternal diets trigger sex-specific divergent trajectories of gene expression and epigenetic systems in mouse placenta. PLoS ONE 7:e47986. doi: 10.1371/journal.pone.0047986
75. Gaccioli, F., White, V., Capobianco, E., Powell, T. L., Jawerbaum, A., and Jansson, T. (2013). Maternal overweight induced by a diet with high content of saturated fat activates placental mTOR and eIF2alpha signaling and increases fetal growth in rats. Biol. Reprod. 89, 96. doi: 10.1095/biolreprod.113.109702
76. Gallo, L. A., Tran, M., Moritz, K. M., Jefferies, A. J., and Wlodek, M. E. (2012b). Pregnancy in aged rats that were born small: cardiorenal and metabolic adaptations and second-generation fetal growth. FASEB J. 26, 4337-4347. doi: 10.1096/fj.12-210401
77. Gallo, L. A., Tran, M., Moritz, K. M., Mazzuca, M. Q., Parry, L. J., Westcott, K. T., et al. (2012a). Cardio-renal and metabolic adaptations during pregnancy in female rats born small: implications for maternal health and second generation fetal growth. J. Physiol. 590, 617-630. doi: 10.1113/jphysiol.2011.219147
78. Gallou-Kabani, C., Gabory, A., Tost, J., Karimi, M., Mayeur, S., Lesage, J., et al. (2010). Sex-and diet-specific changes of imprinted gene expression and DNA methylation in mouse placenta under a high-fat diet. PLoS ONE 5:e14398. doi: 10.1371/journal.pone.0014398
79. Ganguly, A., Collis, L., and Devaskar, S. U. (2012). Placental glucose and amino acid transport in calorie-restricted wild-type and Glut3 null heterozygous mice. Endocrinology 153, 3995-4007. doi: 10.1210/en.2011-1973
80. Gao, H., Sathishkumar, K. R., Yallampalli, U., Balakrishnan, M., Li, X., Wu, G., et al. (2012b). Maternal protein restriction regulates IGF2 system in placental labyrinth. Front. Biosci. (Elite Ed). 4, 1434-1450. doi: 10.2741/E472
81. Gao, H., Yallampalli, U., and Yallampalli, C. (2012a). Gestational protein restriction reduces expression of Hsd17b2 in rat placental labyrinth. Biol. Reprod. 87, 68. doi: 10.1095/biolreprod.112.100479
82. Gao, H., Yallampalli, U., and Yallampalli, C. (2013). Gestational protein restriction affects trophoblast differentiation. Front. Biosci. (Elite Ed). 5, 591-601. doi: 10.2741/E641
83. George, E. M., Garrett, M. R., and Granger, J. P. (2014). Placental ischemia induces changes in gene expression in chorionic tissue. Mamm. Genome 25, 253-261. doi: 10.1007/s00335-014-9505-3
84. Gheorghe, C. P., Goyal, R., Holweger, J. D., and Longo, L. D. (2009). Placental gene expression responses to maternal protein restriction in the mouse. Placenta 30, 411-417. doi: 10.1016/j.placenta.2009.03.002
85. Gheorghe, C. P., Mohan, S., Oberg, K. C., and Longo, L. D. (2007). Gene expression patterns in the hypoxic murine placenta: a role in epigenesis? Reprod. Sci. 14, 223-233. doi: 10.1177/1933719107302860
86. Ghilardi, N., Ziegler, S., Wiestner, A., Stoffel, R., Heim, M. H., and Skoda, R. C. (1996). Defective STAT signaling by the leptin receptor in diabetic mice. Proc. Natl. Acad. Sci. U.S.A. 93, 6231-6235. doi: 10.1073/pnas.93.13.6231
87. Gilbert, M., and Leturque, A. (1982). Fetal weight and its relationship to placental blood flow and placental weight in experimental intrauterine growth retardation in the rat. J. Dev. Physiol. 4, 237-246.
88. Gilbert, R. D., Cummings, L. A., Juchau, M. R., and Longo, L. D. (1979). Placental diffusing capacity and fetal development in exercising or hypoxic guinea pigs. J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 46, 828-834.
89. Giussani, D. A., Camm, E. J., Niu, Y., Richter, H. G., Blanco, C. E., Gottschalk, R., et al. (2012). Developmental programming of cardiovascular dysfunction by prenatal hypoxia and oxidative stress. PLoS ONE 7:e31017. doi: 10.1371/journal.pone.0031017
90. Giussani, D. A., Niu, Y., Herrera, E. A., Richter, H. G., Camm, E. J., Thakor, A. S., et al. (2014). Heart disease link to fetal hypoxia and oxidative stress. Adv. Exp. Med. Biol. 814, 77-87. doi: 10.1007/978-1-4939-1031-1_7
91. Gray, C., Long, S., Green, C., Gardiner, S. M., Craigon, J., and Gardner, D. S. (2013). Maternal fructose and/or salt intake and reproductive outcome in the rat: effects on growth, fertility, sex ratio, and birth order. Biol. Reprod. 89, 51. doi: 10.1095/biolreprod.113.109595
92. Hanson, M. A., and Gluckman, P. D. (2008). Developmental origins of health and disease: new insights. Basic Clin. Pharmacol. Toxicol. 102, 90-93. doi: 10.1111/j.1742-7843.2007.00186.x
93. Harper, J. L., Caesar, G. A., Pennington, K. A., Davis, J. W., and Schulz, L. C. (2015). Placental changes caused by food restriction during early pregnancy in mice are reversible. Reprod. Suppl. 150, 165-172. doi: 10.1530/REP-15-0010
94. Hay, W. W. Jr. (1995). Regulation of placental metabolism by glucose supply. Reprod. Fertil. Dev. 7, 365-375. doi: 10.1071/RD9950365
95. Hayes, E. K., Lechowicz, A., Petrik, J. J., Storozhuk, Y., Paez-Parent, S., Dai, Q., et al. (2012). Adverse fetal and neonatal outcomes associated with a life-long high fat diet: role of altered development of the placental vasculature. PLoS ONE 7:e33370. doi: 10.1371/journal.pone.0033370
96. Hayes, E. K., Tessier, D. R., Percival, M. E., Holloway, A. C., Petrik, J. J., Gruslin, A., et al. (2014). Trophoblast invasion and blood vessel remodeling are altered in a rat model of lifelong maternal obesity. Reprod. Sci. 21, 648-657. doi: 10.1177/1933719113508815
97. Henry, T. Q., Mansano, R. Z., Nast, C. C., Lakshmanan, J., Abdallah, M., Abdel-Hakeem, A. K., et al. (2010). GDNF and MAPK-ERK pathway signaling is reduced during nephrogenesis following maternal under-nutrition. J. Dev. Orig. Health Dis. 1, 67-74. doi: 10.1017/S2040174409990134
98. Higgins, J. S., Vaughan, O. R., de Liger, E. F., Fowden, A. L., and Sferruzzi-Perri, A. N. (2015). Placental phenotype and resource allocation to fetal growth are modified by the timing and degree of hypoxia during mouse pregnancy. J. Physiol. doi: 10.1113/JP271057. [Epub ahead of print].
99. Ho-Chen, J. K., Ain, R., Alt, A. R., Wood, J. G., Gonzalez, N. C., and Soares, M. J. (2006). Hypobaric hypoxia as a tool to study pregnancy-dependent responses at the maternal-fetal interface. Methods Mol. Med. 122, 427-434.
100. Hoile, S. P., Lillycrop, K. A., Thomas, N. A., Hanson, M. A., and Burdge, G. C. (2011). Dietary protein restriction during F0 pregnancy in rats induces transgenerational changes in the hepatic transcriptome in female offspring. PLoS ONE 6:e21668. doi: 10.1371/journal.pone.0021668
101. Holemans, K., Caluwaerts, S., Poston, L., and Van Assche, F. A. (2004). Diet-induced obesity in the rat: a model for gestational diabetes mellitus. Am. J. Obstet. Gynecol. 190, 858-865. doi: 10.1016/j.ajog.2003.09.025
102. Howie, G. J., Sloboda, D. M., Kamal, T., and Vickers, M. H. (2009). Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J. Physiol. 587, 905-915. doi: 10.1113/jphysiol.2008.163477
103. Howie, G. J., Sloboda, D. M., Reynolds, C. M., and Vickers, M. H. (2013). Timing of maternal exposure to a high fat diet and development of obesity and hyperinsulinemia in male rat offspring: same metabolic phenotype, different developmental pathways? J. Nutr. Metab. 2013, 517384. doi: 10.1155/2013/517384
104. Hutter, D., Kingdom, J., and Jaeggi, E. (2010). Causes and mechanisms of intrauterine hypoxia and its impact on the fetal cardiovascular system: a review. Int. J. Pediatr. 2010, 401323. doi: 10.1155/2010/401323
105. Hvizdosova-Klescova, A., Uhlik, J., Malina, M., Vulterinova, H., Novotny, T., and Vajner, L. (2013). Remodeling of fetoplacental arteries in rats due to chronic hypoxia. Exp. Toxicol. Pathol. 65, 97-103. doi: 10.1016/j.etp.2011.06.006
106. Igosheva, N., Abramov, A. Y., Poston, L., Eckert, J. J., Fleming, T. P., Duchen, M. R., et al. (2010). Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS ONE 5:e10074. doi: 10.1371/journal.pone.0010074
107. Intapad, S., Warrington, J. P., Spradley, F. T., Palei, A. C., Drummond, H. A., Ryan, M. J., et al. (2014). Reduced uterine perfusion pressure induces hypertension in the pregnant mouse. Am. J. Physiol. Regul. Integr. Comp. Physiol. 307, R1353-R1357. doi: 10.1152/ajpregu.00268.2014
108. Itoh, S., Brawley, L., Wheeler, T., Anthony, F. W., Poston, L., and Hanson, M. A. (2002). Vasodilation to vascular endothelial growth factor in the uterine artery of the pregnant rat is blunted by low dietary protein intake. Pediatr. Res. 51, 485-491. doi: 10.1203/00006450-200204000-00014
109. Jansson, N., Pettersson, J., Haafiz, A., Ericsson, A., Palmberg, I., Tranberg, M., et al. (2006). Down-regulation of placental transport of amino acids precede the development of intrauterine growth restriction in rats fed a low protein diet. J. Physiol. 576, 935-946. doi: 10.1113/jphysiol.2003.550004
110. Jansson, T., and Powell, T. L. (2006). IFPA 2005 Award in Placentology Lecture. Human placental transport in altered fetal growth: does the placenta function as a nutrient sensor?-a review. Placenta 27(Suppl. A), S91-S97. doi: 10.1016/j.placenta.2005.11.010
111. Jones, H. N., Woollett, L. A., Barbour, N., Prasad, P. D., Powell, T. L., and Jansson, T. (2008). High-fat diet before and during pregnancy causes marked up-regulation of placental nutrient transport and fetal overgrowth in C57/BL6 mice. FASEB J. 23, 271-278. doi: 10.1096/fj.08-116889
112. Jungheim, E. S., Schoeller, E. L., Marquard, K. L., Louden, E. D., Schaffer, J. E., and Moley, K. H. (2010). Diet-induced obesity model: abnormal oocytes and persistent growth abnormalities in the offspring. Endocrinology 151, 4039-4046. doi: 10.1210/en.2010-0098
113. Kane, A. D., Herrera, E. A., Camm, E. J., and Giussani, D. A. (2013). Vitamin C prevents intrauterine programming of in vivo cardiovascular dysfunction in the rat. Circul. J. 77, 2604-2611. doi: 10.1253/circj.CJ-13-0311
114. Keesey, R. E., and Hirvonen, M. D. (1997). Body weight set-points: determination and adjustment. J. Nutr. 127, 1875S-1883S.
115. Khorram, N. M., Magee, T. R., Wang, C., Desai, M., Ross, M., and Khorram, O. (2011). Maternal undernutrition programs offspring adrenal expression of steroidogenic enzymes. Reprod. Sci. 18, 931-940. doi: 10.1177/1933719111404613
116. Khorram, O., Han, G., Bagherpour, R., Magee, T. R., Desai, M., Ross, M. G., et al. (2010). Effect of maternal undernutrition on vascular expression of micro and messenger RNA in newborn and aging offspring. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298, R1366-R1374. doi: 10.1152/ajpregu.00704.2009
117. Khorram, O., Keen-Rinehart, E., Chuang, T. D., Ross, M. G., and Desai, M. (2015). Maternal undernutrition induces premature reproductive senescence in adult female rat offspring. Fertil. Steril. 103, 291-8 e2. doi: 10.1016/j.fertnstert.2014.09.026
118. Khorram, O., Khorram, N., Momeni, M., Han, G., Halem, J., Desai, M., et al. (2007b). Maternal undernutrition inhibits angiogenesis in the offspring: a potential mechanism of programmed hypertension. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R745-R753. doi: 10.1152/ajpregu.00131.2007
119. Khorram, O., Momeni, M., Desai, M., and Ross, M. G. (2007a). Nutrient restriction in utero induces remodeling of the vascular extracellular matrix in rat offspring. Reprod. Sci. 14, 73-80. doi: 10.1177/1933719106298215
120. Kim, D. W., Young, S. L., Grattan, D. R., and Jasoni, C. L. (2014). Obesity during pregnancy disrupts placental morphology, cell proliferation, and inflammation in a sex-specific manner across gestation in the mouse. Biol. Reprod. 90, 130. doi: 10.1095/biolreprod.113.117259
121. Kind, K. L., Clifton, P. M., Grant, P. A., Owens, P. C., Sohlstrom, A., Roberts, C. T., et al. (2003). Effect of maternal feed restriction during pregnancy on glucose tolerance in the adult guinea pig. Am. J. Physiol. Regul. Integr. Comp. Physiol. 284, R140-R152. doi: 10.1152/ajpregu.00587.2001
122. Kind, K. L., Clifton, P. M., Katsman, A. I., Tsiounis, M., Robinson, J. S., and Owens, J. A. (1999). Restricted fetal growth and the response to dietary cholesterol in the guinea pig. Am. J. Physiol. 277, R1675-R1682.
123. Kind, K. L., Roberts, C. T., Sohlstrom, A. I., Katsman, A., Clifton, P. M., Robinson, J. S., et al. (2005). Chronic maternal feed restriction impairs growth but increases adiposity of the fetal guinea pig. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R119-R126. doi: 10.1152/ajpregu.00360.2004
124. Kind, K. L., Simonetta, G., Clifton, P. M., Robinson, J. S., and Owens, J. A. (2002). Effect of maternal feed restriction on blood pressure in the adult guinea pig. Exp. Physiol. 87, 469-477. doi: 10.1111/j.1469-445X.2002.tb00060.x
125. King, V., Hibbert, N., Seckl, J. R., Norman, J. E., and Drake, A. J. (2013). The effects of an obesogenic diet during pregnancy on fetal growth and placental gene expression are gestation dependent. Placenta 34, 1087-1090. doi: 10.1016/j.placenta.2013.09.006
126. Kwong, W. Y., Miller, D. J., Ursell, E., Wild, A. E., Wilkins, A. P., Osmond, C., et al. (2006). Imprinted gene expression in the rat embryo-fetal axis is altered in response to periconceptional maternal low protein diet. Reprod. Suppl. 132, 265-277. doi: 10.1530/rep.1.01038
127. Kwong, W. Y., Wild, A. E., Roberts, P., Willis, A. C., and Fleming, T. P. (2000). Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development 127, 4195-4202.
128. Laborie, C., Molendi-Coste, O., Breton, C., Montel, V., Vandenbulcke, F., Grumolato, L., et al. (2011). Maternal perinatal undernutrition has long-term consequences on morphology, function and gene expression of the adrenal medulla in the adult male rat. J. Neuroendocrinol. 23, 711-724. doi: 10.1111/j.1365-2826.2011.02159.x
129. Lager, S., and Powell, T. L. (2012). Regulation of nutrient transport across the placenta. J. Pregnancy 2012, 179827. doi: 10.1155/2012/179827
130. Lager, S., Samulesson, A. M., Taylor, P. D., Poston, L., Powell, T. L., and Jansson, T. (2014). Diet-induced obesity in mice reduces placental efficiency and inhibits placental mTOR signaling. Physiol. Rep. 2, e00242. doi: 10.1002/phy2.242
131. Lauritz, B., Siebel, A. L., Guille, V., Jefferies, A. J., and Wlodek, M. E. (2012). Growth restriction alters adult spatial memory and sensorimotor gating in a sex-specific manner. J. Dev. Orig. Health Dis. 3, 59-68. doi: 10.1017/S2040174411000729
132. Leonhardt, M., Lesage, J., Croix, D., Dutriez-Casteloot, I., Beauvillain, J. C., and Dupouy, J. P. (2003). Effects of perinatal maternal food restriction on pituitary-gonadal axis and plasma leptin level in rat pup at birth and weaning and on timing of puberty. Biol. Reprod. 68, 390-400. doi: 10.1095/biolreprod.102.003269
133. Leonhardt, M., Lesage, J., Dufourny, L., Dickes-Coopman, A., Montel, V., and Dupouy, J. P. (2002). Perinatal maternal food restriction induces alterations in hypothalamo-pituitary-adrenal axis activity and in plasma corticosterone-binding globulin capacity of weaning rat pups. Neuroendocrinology 75, 45-54. doi: 10.1159/000048220
134. Lesage, J., Blondeau, B., Grino, M., Breant, B., and Dupouy, J. P. (2001). Maternal undernutrition during late gestation induces fetal overexposure to glucocorticoids and intrauterine growth retardation, and disturbs the hypothalamo-pituitary adrenal axis in the newborn rat. Endocrinology 142, 1692-1702. doi: 10.1210/en.142.5.1692
135. Lesage, J., Dufourny, L., Laborie, C., Bernet, F., Blondeau, B., Avril, I., et al. (2002b). Perinatal malnutrition programs sympathoadrenal and hypothalamic-pituitary-adrenal axis responsiveness to restraint stress in adult male rats. J. Neuroendocrinol. 14, 135-143. doi: 10.1046/j.0007-1331.2001.00753.x
136. Lesage, J., Hahn, D., Leonhardt, M., Blondeau, B., Breant, B., and Dupouy, J. P. (2002a). Maternal undernutrition during late gestation-induced intrauterine growth restriction in the rat is associated with impaired placental GLUT3 expression, but does not correlate with endogenous corticosterone levels. J. Endocrinol. 174, 37-43. doi: 10.1677/joe.0.1740037
137. Lewis, R. M., Doherty, C. B., James, L. A., Burton, G. J., and Hales, C. N. (2001a). Effects of maternal iron restriction on placental vascularization in the rat. Placenta 22, 534-539. doi: 10.1053/plac.2001.0679
138. Lewis, R. M., Forhead, A. J., Petry, C. J., Ozanne, S. E., and Hales, C. N. (2002). Long-term programming of blood pressure by maternal dietary iron restriction in the rat. Br. J. Nutr. 88, 283-290. doi: 10.1079/BJN2002656
139. Lewis, R. M., James, L. A., Zhang, J., Byrne, C. D., and Hales, C. N. (2001b). Effects of maternal iron restriction in the rat on hypoxia-induced gene expression and fetal metabolite levels. Br. J. Nutr. 85, 193-201. doi: 10.1079/BJN2000247
140. Lewis, R. M., Petry, C. J., Ozanne, S. E., and Hales, C. N. (2001c). Effects of maternal iron restriction in the rat on blood pressure, glucose tolerance, and serum lipids in the 3-month-old offspring. Metab. Clin. Exp. 50, 562-567. doi: 10.1053/meta.2001.22516
141. Li, H. P., Chen, X., and Li, M. Q. (2013). Gestational diabetes induces chronic hypoxia stress and excessive inflammatory response in murine placenta. Int. J. Clin. Exp. Pathol. 6, 650-659.
142. Liang, C., DeCourcy, K., and Prater, M. R. (2010). High-saturated-fat diet induces gestational diabetes and placental vasculopathy in C57BL/6 mice. Metab. Clin. Exp. 59, 943-950. doi: 10.1016/j.metabol.2009.10.015
143. Liang, C., Oest, M. E., Jones, J. C., and Prater, M. R. (2009a). Gestational high saturated fat diet alters C57BL/6 mouse perinatal skeletal formation. Birth Defects Res. B Dev. Reprod. Toxicol. 86, 362-369. doi: 10.1002/bdrb.20204
144. Liang, C., Oest, M. E., and Prater, M. R. (2009b). Intrauterine exposure to high saturated fat diet elevates risk of adult-onset chronic diseases in C57BL/6 mice. Birth Defects Res. B Dev. Reprod. Toxicol. 86, 377-384. doi: 10.1002/bdrb.20206
145. Lillycrop, K. A., and Burdge, G. C. (2011). Epigenetic changes in early life and future risk of obesity. Int. J. Obes. 35, 72-83. doi: 10.1038/ijo.2010.122
146. Lillycrop, K. A., Phillips, E. S., Jackson, A. A., Hanson, M. A., and Burdge, G. C. (2005). Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J. Nutr. 135, 1382-1386.
147. Lillycrop, K. A., Phillips, E. S., Torrens, C., Hanson, M. A., Jackson, A. A., and Burdge, G. C. (2008). Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPAR alpha promoter of the offspring. Br. J. Nutr. 100, 278-282. doi: 10.1017/S0007114507894438
148. Lillycrop, K. A., Slater-Jefferies, J. L., Hanson, M. A., Godfrey, K. M., Jackson, A. A., and Burdge, G. C. (2007). Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications. Br. J. Nutr. 97, 1064-1073. doi: 10.1017/S000711450769196X
149. Lin, Y., Han, X. F., Fang, Z. F., Che, L. Q., Nelson, J., Yan, T. H., et al. (2011). Beneficial effects of dietary fibre supplementation of a high-fat diet on fetal development in rats. Br. J. Nutr. 106, 510-518. doi: 10.1017/S0007114511000614
150. Lineker, C., Kerr, P. M., Nguyen, P., Bloor, I., Astbury, S., Patel, N., et al. (2015). High fructose consumption in pregnancy alters the perinatal environment without increasing metabolic disease in the offspring. Reprod. Fertil. Dev. doi: 10.1071/RD15119. [Epub ahead of print].
151. Liu, X., Lin, Y., Tian, B., Miao, J., Xi, C., and Liu, C. (2014). Maternal protein restriction alters VEGF signaling and decreases pulmonary alveolar in fetal rats. Int. J. Clin. Exp. Pathol. 7, 3101-3111.
152. Lueder, F. L., Kim, S. B., Buroker, C. A., Bangalore, S. A., and Ogata, E. S. (1995). Chronic maternal hypoxia retards fetal growth and increases glucose utilization of select fetal tissues in the rat. Metab. Clin. Exp. 44, 532-537. doi: 10.1016/0026-0495(95)90063-2
153. Lukaszewski, M. A., Butruille, L., Moitrot, E., Montel, V., Dickes-Coopman, A., Lesage, J., et al. (2013). The hypothalamic POMC mRNA expression is upregulated in prenatally undernourished male rat offspring under high-fat diet. Peptides 43, 146-154. doi: 10.1016/j.peptides.2013.03.013
154. Lukaszewski, M. A., Mayeur, S., Fajardy, I., Delahaye, F., Dutriez-Casteloot, I., Montel, V., et al. (2011). Maternal prenatal undernutrition programs adipose tissue gene expression in adult male rat offspring under high-fat diet. Am. J. Physiol. Endocrinol. Metab. 301, E548-E559. doi: 10.1152/ajpendo.00011.2011
155. Luzzo, K. M., Wang, Q., Purcell, S. H., Chi, M., Jimenez, P. T., Grindler, N., et al. (2012). High fat diet induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation/brain defects. PLoS ONE 7:e49217. doi: 10.1371/journal.pone.0049217
156. Magee, T. R., Han, G., Cherian, B., Khorram, O., Ross, M. G., and Desai, M. (2008). Down-regulation of transcription factor peroxisome proliferator-activated receptor in programmed hepatic lipid dysregulation and inflammation in intrauterine growth-restricted offspring. Am. J. Obstet. Gynecol. 199, 271 e1-5. doi: 10.1016/j.ajog.2008.05.022
157. Malandro, M. S., Beveridge, M. J., Kilberg, M. S., and Novak, D. A. (1996a). Effect of low-protein diet-induced intrauterine growth retardation on rat placental amino acid transport. Am. J. Physiol. 271, C295-303.
158. Malandro, M. S., Beveridge, M. J., Novak, D. A., and Kilberg, M. S. (1996b). Rat placental amino acid transport after protein-deprivation-induced intrauterine growth retardation. Biochem. Soc. Trans. 24, 839-843.
159. Mark, P. J., Sisala, C., Connor, K., Patel, R., Lewis, J. L., Vickers, M., et al. (2011). A maternal high-fat diet in rat pregnancy reduces growth of the fetus and the placental junctional zone, but not placental labyrinth zone growth. J. Dev. Orig. Hlth. Dis. 2, 63-70. doi: 10.1017/S2040174410000681
160. Master, J. S., Zimanyi, M. A., Yin, K. V., Moritz, K. M., Gallo, L. A., Tran, M., et al. (2014). Transgenerational left ventricular hypertrophy and hypertension in offspring after uteroplacental insufficiency in male rats. Clin. Exp. Pharmacol. Physiol. 41, 884-890. doi: 10.1111/1440-1681.12303
161. Matheson, H., Veerbeek, J. H., Charnock-Jones, D. S., Burton, G. J., and Yung, H. W. (2015). Morphological and molecular changes in the murine placenta exposed to normobaric hypoxia throughout pregnancy. J. Physiol. doi: 10.1113/JP271073. [Epub ahead of print].
162. Mayeur, S., Lancel, S., Theys, N., Lukaszewski, M. A., Duban, S., Bastide, B., et al. (2012). Maternal calorie restriction modulates placental mitochondrial biogenesis and bioenergetic efficiency: involvement in feto-placental growth defects in rats. Am. J. Physiol. Endocrinol. Metab. 304, E14-E22. doi: 10.1152/ajpendo.00332.2012
163. Mazzuca, M. Q., Tare, M., Parkington, H. C., Dragomir, N. M., Parry, L. J., and Wlodek, M. E. (2012). Uteroplacental insufficiency programmes vascular dysfunction in non-pregnant rats: compensatory adaptations in pregnancy. J. Physiol. 590, 3375-3388. doi: 10.1113/jphysiol.2012.230011
164. Mazzuca, M. Q., Wlodek, M. E., Dragomir, N. M., Parkington, H. C., and Tare, M. (2010). Uteroplacental insufficiency programs regional vascular dysfunction and alters arterial stiffness in female offspring. J. Physiol. 588, 1997-2010. doi: 10.1113/jphysiol.2010.187849
165. Mazzucco, M. B., Fornes, D., Capobianco, E., Higa, R., Jawerbaum, A., and White, V. (2016). Maternal saturated-fat-rich diet promotes leptin resistance in fetal liver lipid catabolism and programs lipid homeostasis impairments in the liver of rat offspring. J. Nutr Biochem. 27, 61-69. doi: 10.1016/j.jnutbio.2015.08.019
166. Mazzucco, M. B., Higa, R., Capobianco, E., Kurtz, M., Jawerbaum, A., and White, V. (2013). Saturated fat-rich diet increases fetal lipids and modulates LPL and leptin receptor expression in rat placentas. J. Endocrinol. 217, 303-315. doi: 10.1530/JOE-13-0021
167. McMillen, I. C., and Robinson, J. S. (2005). Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol. Rev. 85, 571-633. doi: 10.1152/physrev.00053.2003
168. Minge, C. E., Bennett, B. D., Norman, R. J., and Robker, R. L. (2008). Peroxisome Proliferator-Activated Receptor-{gamma} Agonist Rosiglitazone Reverses the Adverse Effects of Diet-Induced Obesity on Oocyte Quality. Endocrinology 149, 2646-2656. doi: 10.1210/en.2007-1570
169. Mitchell, M., Schulz, S. L., Armstrong, D. T., and Lane, M. (2009). Metabolic and mitochondrial dysfunction in early mouse embryos following maternal dietary protein intervention. Biol. Reprod. 80, 622-630. doi: 10.1095/biolreprod.108.072595
170. Moraes, C., Rebelato, H. J., Amaral, M. E., Resende, T. M., Silva, E. V., Esquisatto, M. A., et al. (2014). Effect of maternal protein restriction on liver metabolism in rat offspring. J. Physiol. Sci. 64, 347-355. doi: 10.1007/s12576-014-0325-8
171. Moritz, K. M., Mazzuca, M. Q., Siebel, A. L., Mibus, A., Arena, D., Tare, M., et al. (2009). Uteroplacental insufficiency causes a nephron deficit, modest renal insufficiency but no hypertension with ageing in female rats. J. Physiol. 587, 2635-2646. doi: 10.1113/jphysiol.2009.170407
172. Mukai, Y., Kumazawa, M., and Sato, S. (2013). Fructose intake during pregnancy up-regulates the expression of maternal and fetal hepatic sterol regulatory element-binding protein-1c in rats. Endocrine 44, 79-86. doi: 10.1007/s12020-012-9815-8
173. O'Dowd, R., Kent, J. C., Moseley, J. M., and Wlodek, M. E. (2008). Effects of uteroplacental insufficiency and reducing litter size on maternal mammary function and postnatal offspring growth. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R539-R548. doi: 10.1152/ajpregu.00628.2007
174. Ojeda, N. B., Grigore, D., Robertson, E. B., and Alexander, B. T. (2007). Estrogen protects against increased blood pressure in postpubertal female growth restricted offspring. Hypertension 50, 679-685. doi: 10.1161/HYPERTENSIONAHA.107.091785
175. Ojeda, N. B., Intapad, S., and Alexander, B. T. (2014). Sex differences in the developmental programming of hypertension. Acta Physiol. (Oxf). 210, 307-316. doi: 10.1111/apha.12206
176. Qiao, L., Guo, Z., Bosco, C., Guidotti, S., Wang, Y., Wang, M., et al. (2015). Maternal high fat feeding increases placenta lipoprotein lipase activity by reducing sirt1 expression in mice. Diabetes 64, 3111-3120. doi: 10.2337/db14-1627
177. Qiao, L., Yoo, H. S., Madon, A., Kinney, B., Hay, W. W. Jr., and Shao, J. (2012). Adiponectin enhances mouse fetal fat deposition. Diabetes 61, 3199-3207. doi: 10.2337/db12-0055
178. Rebelato, H. J., Esquisatto, M. A., Moraes, C., Amaral, M. E., and Catisti, R. (2013). Gestational protein restriction induces alterations in placental morphology and mitochondrial function in rats during late pregnancy. J. Mol. Histol. 44, 629-637. doi: 10.1007/s10735-013-9522-7
179. Rebholz, S. L., Burke, K. T., Yang, Q., Tso, P., and Woollett, L. A. (2011). Dietary fat impacts fetal growth and metabolism: uptake of chylomicron remnant core lipids by the placenta. Am. J. Physiol. Endocrinol. Metab. 301, E416-E425. doi: 10.1152/ajpendo.00619.2010
180. Rees, S., Harding, R., and Walker, D. (2008). An adverse intrauterine environment: implications for injury and altered development of the brain. Intern. J. Dev. Neurosci. 26, 3-11. doi: 10.1016/j.ijdevneu.2007.08.020
181. Reid, G. J., Lane, R. H., Flozak, A. S., and Simmons, R. A. (1999). Placental expression of glucose transporter proteins 1 and 3 in growth-restricted fetal rats. Am. J. Obstet. Gynecol. 180, 1017-1023. doi: 10.1016/S0002-9378(99)70675-7
182. Reynolds, C. M., Vickers, M. H., Harrison, C. J., Segovia, S. A., and Gray, C. (2015). Maternal high fat and/or salt consumption induces sex-specific inflammatory and nutrient transport in the rat placenta. Physiol. Rep. 3:e12399. doi: 10.14814/phy2.12399
183. Richter, H. G., Camm, E. J., Modi, B. N., Naeem, F., Cross, C. M., Cindrova-Davies, T., et al. (2012). Ascorbate prevents placental oxidative stress and enhances birth weight in hypoxic pregnancy in rats. J. Physiol. 590, 1377-1387. doi: 10.1113/jphysiol.2011.226340
184. Richter, H. G., Hansell, J. A., Raut, S., and Giussani, D. A. (2009). Melatonin improves placental efficiency and birth weight and increases the placental expression of antioxidant enzymes in undernourished pregnancy. J. Pineal Res. 46, 357-364. doi: 10.1111/j.1600-079X.2009.00671.x
185. Riviere, G., Michaud, A., Breton, C., VanCamp, G., Laborie, C., Enache, M., et al. (2005). Angiotensin-converting enzyme 2 (ACE2) and ACE activities display tissue-specific sensitivity to undernutrition-programmed hypertension in the adult rat. Hypertension 46, 1169-1174. doi: 10.1161/01.HYP.0000185148.27901.fe
186. Roberts, C. T., Sohlstrom, A., Kind, K. L., Earl, R. A., Khong, T. Y., Robinson, J. S., et al. (2001). Maternal food restriction reduces the exchange surface area and increases the barrier thickness of the placenta in the guinea-pig. Placenta 22, 177-185. doi: 10.1053/plac.2000.0602
187. Rodford, J. L., Torrens, C., Siow, R. C., Mann, G. E., Hanson, M. A., and Clough, G. F. (2008). Endothelial dysfunction and reduced antioxidant protection in an animal model of the developmental origins of cardiovascular disease. J. Physiol. 586, 4709-4720. doi: 10.1113/jphysiol.2008.156976
188. Romano, T., Hryciw, D. H., Westcott, K. T., and Wlodek, M. E. (2015). Puberty onset is delayed following uteroplacental insufficiency and occurs earlier with improved lactation and growth for pups born small. Reprod. Fertil. Dev. doi: 10.1071/RD15151. [Epub ahead of print].
189. Romano, T., Wark, J. D., and Wlodek, M. E. (2014). Developmental programming of bone deficits in growth-restricted offspring. Reprod. Fertil. Dev. doi: 10.1071/RD13388. [Epub ahead of print].
190. Rosario, F. J., Jansson, N., Kanai, Y., Prasad, P. D., Powell, T. L., and Jansson, T. (2011). Maternal protein restriction in the rat inhibits placental insulin, mTOR, and STAT3 signaling and down-regulates placental amino acid transporters. Endocrinology 152, 1119-1129. doi: 10.1210/en.2010-1153
191. Rosario, G. X., Konno, T., and Soares, M. J. (2008). Maternal hypoxia activates endovascular trophoblast cell invasion. Dev. Biol. 314, 362-375. doi: 10.1016/j.ydbio.2007.12.007
192. Rosso, P. (1977a). Maternal-fetal exchange during protein malnutrition in the rat. Placental transfer of glucose and a nonmetabolizable glucose analog. J. Nutr. 107, 20006-20010.
193. Rosso, P. (1977b). Maternal-fetal exchange during protein malnutrition in the rat. Placental transfer of alpha-amino isobutyric acid. J. Nutr. 107, 2002-2005.
194. Rueda-Clausen, C. F., Stanley, J. L., Thambiraj, D. F., Poudel, R., Davidge, S. T., and Baker, P. N. (2014). Effect of prenatal hypoxia in transgenic mouse models of preeclampsia and fetal growth restriction. Reprod. Sci. 21, 492-502. doi: 10.1177/1933719113503401
195. Rutland, C. S., Latunde-Dada, A. O., Thorpe, A., Plant, R., Langley-Evans, S., and Leach, L. (2007). Effect of gestational nutrition on vascular integrity in the murine placenta. Placenta 28, 734-742. doi: 10.1016/j.placenta.2006.07.001
196. Sasson, I. E., Vitins, A. P., Mainigi, M. A., Moley, K. H., and Simmons, R. A. (2015). Pre-gestational vs gestational exposure to maternal obesity differentially programs the offspring in mice. Diabetologia 58, 615-624. doi: 10.1007/s00125-014-3466-7
197. Sathishkumar, K., Balakrishnan, M. P., and Yallampalli, C. (2015). Enhanced mesenteric arterial responsiveness to angiotensin II is androgen receptor-dependent in prenatally protein-restricted adult female rat offspring. Biol. Reprod. 92, 55. doi: 10.1095/biolreprod.114.126482
198. Sathishkumar, K., Elkins, R., Yallampalli, U., and Yallampalli, C. (2009). Protein restriction during pregnancy induces hypertension and impairs endothelium-dependent vascular function in adult female offspring. J. Vasc. Res. 46, 229-239. doi: 10.1159/000166390
199. Sathishkumar, K., Elkins, R., Yallampalli, U., and Yallampalli, C. (2012). Protein restriction during pregnancy induces hypertension in adult female rat offspring-influence of oestradiol. Br. J. Nutr. 107, 665-673. doi: 10.1017/S0007114511003448
200. Schlitt, J. M., and Schulz, L. C. (2012). The source of leptin, but not leptin depletion in response to food restriction, changes during early pregnancy in mice. Endocrine 41, 227-235. doi: 10.1007/s12020-011-9548-0
201. Schulz, L. C., Schlitt, J. M., Caesar, G., and Pennington, K. A. (2012). Leptin and the placental response to maternal food restriction during early pregnancy in mice. Biol. Reprod. 87, 120. doi: 10.1095/biolreprod.112.103218
202. Sebaai, N., Lesage, J., Alaoui, A., Dupouy, J. P., and Deloof, S. (2002b). Effects of dehydration on endocrine regulation of the electrolyte and fluid balance and atrial natriuretic peptide-binding sites in perinatally malnourished adult male rats. Eur. J. Endocrinol. 147, 835-848. doi: 10.1530/eje.0.1470835
203. Sebaai, N., Lesage, J., Breton, C., Vieau, D., and Deloof, S. (2004). Perinatal food deprivation induces marked alterations of the hypothalamo-pituitary-adrenal axis in 8-month-old male rats both under basal conditions and after a dehydration period. Neuroendocrinology 79, 163-173. doi: 10.1159/000078098
204. Sebaai, N., Lesage, J., Vieau, D., Alaoui, A., Dupouy, J. P., and Deloof, S. (2002a). Altered control of the hypothalamo-pituitary-adrenal axis in adult male rats exposed perinatally to food deprivation and/or dehydration. Neuroendocrinology 76, 243-253. doi: 10.1159/000065947
205. Sferruzzi-Perri, A. N., Vaughan, O. R., Coan, P. M., Suciu, M. C., Darbyshire, R., Constancia, M., et al. (2011). Placental-specific Igf2 deficiency alters developmental adaptations to undernutrition in mice. Endocrinology 152, 3202-3212. doi: 10.1210/en.2011-0240
206. Sferruzzi-Perri, A. N., Vaughan, O. R., Haro, M., Cooper, W. N., Musial, B., Charalambous, M., et al. (2013). An obesogenic diet during mouse pregnancy modifies maternal nutrient partitioning and the fetal growth trajectory. FASEB 27, 3928-3937. doi: 10.1096/fj.13-234823
207. Sibley, C., Glazier, J., and D'souza, S. (1997). Placental transporter activity and expression in relation to fetal growth. Exp. Physiol. 82, 389-402. doi: 10.1113/expphysiol.1997.sp004034
208. Siebel, A. L., Gallo, L. A., Guan, T. C., Owens, J. A., and Wlodek, M. E. (2010). Cross-fostering and improved lactation ameliorates deficits in endocrine pancreatic morphology in growth-restricted adult male rat offspring. J. Dev. Orig. Health Dis. 1, 234-244. doi: 10.1017/S2040174410000383
209. Siebel, A. L., Mibus, A., De Blasio, M. J., Westcott, K. T., Morris, M. J., Prior, L., et al. (2008). Improved lactational nutrition and postnatal growth ameliorates impairment of glucose tolerance by uteroplacental insufficiency in male rat offspring. Endocrinology 149, 3067-3076. doi: 10.1210/en.2008-0128
210. Skeffington, K. L., Higgins, J. S., Mahmoud, A. D., Evans, A. M., Sferruzzi-Perri, A. N., Fowden, A. L., et al. (2015). Hypoxia, AMPK activation and uterine artery vasoreactivity. J. Physiol. doi: 10.1113/JP270995. [Epub ahead of print].
211. Slater-Jefferies, J. L., Lillycrop, K. A., Townsend, P. A., Torrens, C., Hoile, S. P., Hanson, M. A., et al. (2011). Feeding a protein-restricted diet during pregnancy induces altered epigenetic regulation of peroxisomal proliferator-activated receptor-alpha in the heart of the offspring. J. Dev. Orig. Health Dis. 2, 250-255. doi: 10.1017/S2040174410000425
212. Sloboda, D. M., Howie, G. J., Pleasants, A., Gluckman, P. D., and Vickers, M. H. (2009). Pre-and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat. PLoS ONE 4:e6744. doi: 10.1371/journal.pone.0006744
213. Smart, J. L., Dobbing, J., Adlard, B. P., Lynch, A., and Sands, J. (1973). Vulnerability of developing brain: relative effects of growth restriction during the fetal and suckling periods on behavior and brain composition of adult rats. J. Nutr. 103, 1327-1338.
214. Smith, T., Sloboda, D. M., Saffery, R., Joo, E., and Vickers, M. H. (2014). Maternal nutritional history modulates the hepatic IGF-IGFBP axis in adult male rat offspring. Endocrine 46, 70-82. doi: 10.1007/s12020-013-0034-8
215. Sohlstrom, A., Fernberg, P., Owens, J. A., and Owens, P. C. (2001). Maternal nutrition affects the ability of treatment with IGF-I and IGF-II to increase growth of the placenta and fetus, in guinea pigs. Growth Horm. IGF Res. 11, 392-398. doi: 10.1054/ghir.2001.0253
216. Sohlstrom, A., Katsman, A., Kind, K. L., Grant, P. A., Owens, P. C., Robinson, J. S., et al. (1998a). Effects of acute and chronic food restriction on the insulin-like growth factor axis in the guinea pig. J. Endocrinol. 157, 107-114.
217. Sohlstrom, A., Katsman, A., Kind, K. L., Roberts, C. T., Owens, P. C., Robinson, J. S., et al. (1998b). Food restriction alters pregnancy-associated changes in IGF and IGFBP in the guinea pig. Am. J. Physiol. 274, E410-E416.
218. Soo, P. S., Hiscock, J., Botting, K. J., Roberts, C. T., Davey, A. K., and Morrison, J. L. (2012). Maternal undernutrition reduces P-glycoprotein in guinea pig placenta and developing brain in late gestation. Reprod. Toxicol. 33, 374-381. doi: 10.1016/j.reprotox.2012.01.013
219. Strakovsky, R. S., Zhou, D., and Pan, Y. X. (2010). A low-protein diet during gestation in rats activates the placental mammalian amino acid response pathway and programs the growth capacity of offspring. J. Nutr. 140, 2116-2120. doi: 10.3945/jn.110.127803
220. Sun, C., Velazquez, M. A., Marfy-Smith, S., Sheth, B., Cox, A., Johnston, D. A., et al. (2014). Mouse early extra-embryonic lineages activate compensatory endocytosis in response to poor maternal nutrition. Development 141, 1140-1150. doi: 10.1242/dev.103952
221. Susser, E., and St Clair, D. (2013). Prenatal famine and adult mental illness: interpreting concordant and discordant results from the Dutch and Chinese Famines. Soc. Sci. Med. 97, 325-330. doi: 10.1016/j.socscimed.2013.02.049
222. Tafti, S. A., Nast, C. C., Desai, M., Amaya, K. E., Ross, M. G., and Magee, T. R. (2011). Maternal undernutrition upregulates apoptosis in offspring nephrogenesis. J. Dev. Orig. Health Dis. 2, 226-235. doi: 10.1017/S2040174411000262
223. Tare, M., Parkington, H. C., Bubb, K. J., and Wlodek, M. E. (2012). Uteroplacental insufficiency and lactational environment separately influence arterial stiffness and vascular function in adult male rats. Hypertension 60, 378-386. doi: 10.1161/HYPERTENSIONAHA.112.190876
224. Tarry-Adkins, J. L., Chen, J. H., Smith, N. S., Jones, R. H., Cherif, H., and Ozanne, S. E. (2009). Poor maternal nutrition followed by accelerated postnatal growth leads to telomere shortening and increased markers of cell senescence in rat islets. FASEB J. 23, 1521-1528. doi: 10.1096/fj.08-122796
225. Taylor, P. D., Khan, I. Y., Lakasing, L., Dekou, V., O'Brien-Coker, I., Mallet, A. I., et al. (2003). Uterine artery function in pregnant rats fed a diet supplemented with animal lard. Exp. Physiol. 88, 389-398. doi: 10.1113/eph8802495
226. Tissot van Patot, M. C., Murray, A. J., Beckey, V., Cindrova-Davies, T., Johns, J., Zwerdlinger, L., et al. (2010). Human placental metabolic adaptation to chronic hypoxia, high altitude: hypoxic preconditioning. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298, R166-R172. doi: 10.1152/ajpregu.00383.2009
227. Torrens, C., Brawley, L., Anthony, F. W., Dance, C. S., Dunn, R., Jackson, A. A., et al. (2006). Folate supplementation during pregnancy improves offspring cardiovascular dysfunction induced by protein restriction. Hypertension 47, 982-987. doi: 10.1161/01.HYP.0000215580.43711.d1
228. Torrens, C., Poston, L., and Hanson, M. A. (2008). Transmission of raised blood pressure and endothelial dysfunction to the F2 generation induced by maternal protein restriction in the F0, in the absence of dietary challenge in the F1 generation. Br. J. Nutr. 100, 760-766. doi: 10.1017/S0007114508921747
229. Tran, M., Gallo, L. A., Wadley, G. D., Jefferies, A. J., Moritz, K. M., and Wlodek, M. E. (2012). Effect of pregnancy for females born small on later life metabolic disease risk. PLoS ONE 7:e45188. doi: 10.1371/annotation/0a0f4d8b-8ec3-4d62-8d0b-1917716beaa0
230. Tran, M., Young, M. E., Jefferies, A. J., Hryciw, D. H., Ward, M. M., Fletcher, E. L., et al. (2015). Uteroplacental insufficiency leads to hypertension, but not glucose intolerance or impaired skeletal muscle mitochondrial biogenesis, in 12-month-old rats. Physiol. Rep. 3:e12556. doi: 10.14814/phy2.12556
231. Turner, A. J., and Trudinger, B. J. (2009). A modification of the uterine artery restriction technique in the guinea pig fetus produces asymmetrical ultrasound growth. Placenta 30, 236-240. doi: 10.1016/j.placenta.2008.11.023
232. van Abeelen, A. F., de Rooij, S. R., Osmond, C., Painter, R. C., Veenendaal, M. V., Bossuyt, P. M., et al. (2011). The sex-specific effects of famine on the association between placental size and later hypertension. Placenta 32, 694-698. doi: 10.1016/j.placenta.2011.06.012
233. Varma, D. R., and Ramakrishnan, R. (1991). Effects of protein-calorie malnutrition on transplacental kinetics of aminoisobutyric-acid in rats. Placenta 12, 277-284. doi: 10.1016/0143-4004(91)90009-5
234. Vaughan, O. R., Fisher, H. M., Dionelis, K. N., Jefferies, E. C., Higgins, J. S., Musial, B., et al. (2015a). Corticosterone alters materno-fetal glucose partitioning and insulin signalling in pregnant mice. J. Physiol. 593, 1307-1321. doi: 10.1113/jphysiol.2014.287177
235. Vaughan, O. R., Phillips, H. M., Everden, A. J., Sferruzzi-Perri, A. N., and Fowden, A. L. (2015b). Dexamethasone treatment of pregnant F0 mice leads to parent of origin-specific changes in placental function of the F2 generation. Reprod. Fertil. Dev. doi: 10.1071/RD14285. [Epub ahead of print].
236. Vaughan, O. R., Sferruzzi-Perri, A. N., Coan, P. M., and Fowden, A. L. (2012a). Environmental regulation of placental phenotype: implications for fetal growth. Reprod. Fertil. Dev. 24, 80-96. doi: 10.1071/RD11909
237. Vaughan, O. R., Sferruzzi-Perri, A. N., Coan, P. M., and Fowden, A. L. (2013). Adaptations in placental phenotype depend on route and timing of maternal dexamethasone administration in mice. Biol. Reprod. 89, 1-12. doi: 10.1095/biolreprod.113.109678
238. Vaughan, O. R., Sferruzzi-Perri, A. N., and Fowden, A. L. (2012b). Maternal corticosterone regulates nutrient allocation to fetal growth in mice. J. Physiol. 590, 5529-5540. doi: 10.1113/jphysiol.2012.239426
239. Vickers, M. H., Breier, B. H., Cutfield, W. S., Hofman, P. L., and Gluckman, P. D. (2000). Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am. J. Physiol. Endocrinol. Metab. 279, E83-E87.
240. Vickers, M. H., Clayton, Z. E., Yap, C., and Sloboda, D. M. (2011). Maternal fructose intake during pregnancy and lactation alters placental growth and leads to sex-specific changes in fetal and neonatal endocrine function. Endocrinology 152, 1378-1387. doi: 10.1210/en.2010-1093
241. Vieau, D., Sebaai, N., Leonhardt, M., Dutriez-Casteloot, I., Molendi-Coste, O., Laborie, C., et al. (2007). HPA axis programming by maternal undernutrition in the male rat offspring. Psychoneuroendocrinology 32 (Suppl. 1), S16-S20. doi: 10.1016/j.psyneuen.2007.03.014
242. Vieira-Filho, L. D., Lara, L. S., Silva, P. A., Luzardo, R., Einicker-Lamas, M., Cardoso, H. D., et al. (2009). Placental oxidative stress in malnourished rats and changes in kidney proximal tubule sodium ATPases in offspring. Clin. Exp. Pharmacol. Physiol. 36, 1157-1163. doi: 10.1111/j.1440-1681.2009.05212.x
243. Wadley, G. D., McConell, G. K., McConell, G. K., Siebel, A. L., Westcott, K. T., and Wlodek, M. E. (2013). Growth restriction in the rat alters expression of metabolic genes during postnatal cardiac development in a sex-specific manner. Physiol. Genomics 45, 99-105. doi: 10.1152/physiolgenomics.00095.2012
244. Wadley, G. D., Siebel, A. L., Cooney, G. J., McConell, G. K., Wlodek, M. E., and Owens, J. A. (2008). Uteroplacental insufficiency and reducing litter size alters skeletal muscle mitochondrial biogenesis in a sex-specific manner in the adult rat. Am. J. Physiol. Endocrinol. Metab. 294, E861-E869. doi: 10.1152/ajpendo.00037.2008
245. Wakefield, S. L., Lane, M., and Mitchell, M. (2011). Impaired mitochondrial function in the preimplantation embryo perturbs fetal and placental development in the mouse. Biol. Reprod. 84, 572-580. doi: 10.1095/biolreprod.110.087262
246. Walton, S. L., Singh, R. R., Tan, T., Paravicini, T. M., and Moritz, K. M. (2015). Late gestational hypoxia and a postnatal high salt diet programs endothelial dysfunction and arterial stiffness in adult mouse offspring. J. Physiol. doi: 10.1113/JP271067. [Epub ahead of print].
247. Wang, C., Li, H., Luo, C., Li, Y., Zhang, Y., Yun, D., et al. (2015). The effect of maternal obesity on the expression and functionality of placental P-glycoprotein: implications in the individualized transplacental digoxin treatment for fetal heart failure. Placenta 36, 1138-1147. doi: 10.1016/j.placenta.2015.08.007
248. Watkins, A. J., Lucas, E. S., Marfy-Smith, S., Bates, N., Kimber, S. J., and Fleming, T. P. (2015). Maternal nutrition modifies trophoblast giant cell phenotype and fetal growth in mice. Reprod. Suppl. 149, 563-575. doi: 10.1530/REP-14-0667
249. Watkins, A. J., Ursell, E., Panton, R., Papenbrock, T., Hollis, L., Cunningham, C., et al. (2008). Adaptive responses by mouse early embryos to maternal diet protect fetal growth but predispose to adult onset disease. Biol. Reprod. 78, 299-306. doi: 10.1095/biolreprod.107.064220
250. Wattez, J. S., Delahaye, F., Barella, L. F., Dickes-Coopman, A., Montel, V., Breton, C., et al. (2014). Short-and long-term effects of maternal perinatal undernutrition are lowered by cross-fostering during lactation in the male rat. J. Dev. Orig. Health Dis. 5, 109-120. doi: 10.1017/S2040174413000548
251. Wlodek, M. E., Mibus, A., Tan, A., Siebel, A. L., Owens, J. A., and Moritz, K. M. (2007). Normal lactational environment restores nephron endowment and prevents hypertension after placental restriction in the rat. J. Am. Soc. Nephrol. 18, 1688-1696. doi: 10.1681/ASN.2007010015
252. Wlodek, M. E., Westcott, K., Siebel, A. L., Owens, J. A., and Moritz, K. M. (2008). Growth restriction before or after birth reduces nephron number and increases blood pressure in male rats. Kidney Int. 74, 187-195. doi: 10.1038/ki.2008.153
253. Wlodek, M. E., Westcott, K. T., O'Dowd, R., Serruto, A., Wassef, L., Moritz, K. M., et al. (2005). Uteroplacental restriction in the rat impairs fetal growth in association with alterations in placental growth factors including PTHrP. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R1620-R1627. doi: 10.1152/ajpregu.00789.2004
254. Wu, L. L., Russell, D. L., Wong, S. L., Chen, M., Tsai, T. S., St John, J. C., et al. (2015). Mitochondrial dysfunction in oocytes of obese mothers: transmission to offspring and reversal by pharmacological endoplasmic reticulum stress inhibitors. Development 142, 681-691. doi: 10.1242/dev.114850
255. Zamudio, S. (2003). The placenta at high altitude. High Alt. Med. Biol. 4, 171-191. doi: 10.1089/152702903322022785