2011 and 2012 Early Careers Achievement Awards: Placental programming: How the maternal environment can impact placental function

Journal of Animal Science

Volumn 91, Issue 6, 2013, Pages 2467-2480

  Vonnahme, K A ^a   Lemley, C O ^a   Shukla, P ^b   O'Rourke, S T ^b  

^a NORTH DAKOTA STATE UNIVERSITY   (United States)

^b MISSISSIPPI STATE UNIVERSITY   (United States)

Author keywords

Maternal nutrition; Placenta; Umbilical blood flow; Uterine blood flow

Indexed keywords

ANIMAL; ANIMAL FOOD; ARTICLE; CATTLE; DOMESTIC SHEEP; FEMALE; FETUS; FETUS DEVELOPMENT; HEMODYNAMICS; MAMMAL; MATERNAL NUTRITION; PHYSIOLOGY; PLACENTA; PREGNANCY; PRENATAL DEVELOPMENT; SWINE; UMBILICAL CORD; UTERUS; VASCULARIZATION;

ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; CATTLE; FEMALE; FETAL DEVELOPMENT; FETUS; HEMODYNAMICS; MAMMALS; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; PLACENTA; PREGNANCY; SHEEP, DOMESTIC; SUS SCROFA; UMBILICAL CORD; UTERUS;

EID: 84882630417     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2012-5929     Document Type: Article

References (108)

1. Adamson, S. L., R. J. Morrow, S. B. Bull, and B. L. Langille. 1989. Vasomotor responses of the umbilical circulation in fetal sheep. Am. J. Physiol. 256:R1056-R1062.
2. Ahokas, R. A., S. L. Reynolds, G. D. Anderson, and J. Lipshitz. 1984. Maternal organ distribution of cardiac output in the diet-restricted pregnant rat. J. Nutr. 114:2262-2268.
3. Belkacemi, L., D. M. Nelson, M. Desai, and M. G. Ross. 2010. Maternal undernutrition influences placental-fetal development. Biol. Reprod. 83:325-331.
4. Bergaya, S., P. Meneton, M. Bloch-Faure, E. Mathieu, F. Alhenc-Gelas, B. I. Levy, and C. M. Boulanger. 2001. Decreased flow-dependent dilation in carotid arteries of tissue kallikrein-knockout mice. Circ. Res. 88:593-599.
5. Bhoola, K. D., C. D. Figueroa, and K. Worthy. 1992. Bioregulation of kinins: Kallikreins, kininogens, and kininases. Pharmacol. Rev. 44:1-80.
6. Björkman, N. 1965. Fine structure of the ovine placentome. J. Anat. 99:283-297.
7. Borowicz, P. P., D. R. Arnold, M. L. Johnson, A. T. Grazul-Bilska, D. A. Redmer, and L. P. Reynolds. 2007. Placental growth throughout the last two-thirds of pregnancy in sheep: Vascular development and angiogenic factor expression. Biol. Reprod. 76:259-267.
8. Bottari, S. P., M. de Gasparo, U. M. Steckelings, and N. R. Levens. 1993. Angiotensin II receptor subtypes: Characterization, signaling mechanisms, and possible physiological implications. Front. Neuroendocrinol. 14:123-171.
9. Burrell, J. H., and E. R. Lumbers. 1997. Angiotensin receptor subtypes in the uterine artery during ovine pregnancy. Eur. J. Pharmacol. 330:257-267.
10. Camacho, L. E., L. A. Lekatz, M. L. Van Emon, C. S. Schauer, K. R. Maddock Carlin, and K. A. Vonnahme. 2010. Effects of maternal metabolizable protein supplementation in late gestation on uterine and umbilical blood flows in sheep. J. Anim. Sci. 88 (E. Suppl. 2):106 (Abstr.).
11. Camacho, L. E., A. M. Meyer, T. L. Neville, C. J. Hammer, D. A. Redmer, L. P. Reynolds, J. S. Caton, and K. A. Vonnahme. 2012. Neonatal hormone changes and growth in lambs born to dams receiving differing nutritional intakes and selenium supplementation during gestation. Reproduction 144:23-35.
12. Carr, D. J., R. P. Aitken, J. S. Milne, A. L. David, and J. M. Wallace. 2012. Fetoplacental biometry and umbilical artery Doppler velocimetry in the overnourished adolescent model of fetal growth restriction. Am. J. Obstet. Gynecol. 207:141.e6-15.
13. Chandler, K. D., B. J. Leury, A. R. Bird, and A. W. Bell. 1985. Effects of undernutrition and exercise during late pregnancy on uterine, fetal, and uteroplacental metabolism in the ewe. Br. J. Nutr. 53:625-635.
14. Clark, K. E., G. L. Irion, and C. E. Mack. 1990. Differential responses of uterine and umbilical vasculatures to angiotensin II and norepinephrine. Am. J. Physiol. 259:H197-H203.
15. Cox, B. E., M. A. Ipson, P. W. Shaul, K. E. Kamm, and C. R. Rosenfeld. 1993. Myometrial angiotensin II receptor subtypes change during ovine pregnancy. J. Clin. Invest. 92:2240-2248.
16. Cox, B. E., and C. R. Rosenfeld. 1999. Ontogeny of vascular angiotensin II receptor subtype expression in ovine development. Pediatr. Res. 45:414-424.
17. Dantzer V. 1984. Scanning electron microscopy of exposed surfaces of the porcine placenta. Acta Anat. (Basel). 118:96-106.
18. Dudley, D. T., R. L. Panek, T. C. Major, G. H. Lu, R. F. Bruns, B. A. Klinkefus, J. C. Hodges, and R. E. Weishaar. 1990. Subclasses of angiotensin II binding sites and their functional significance. Mol. Pharmacol. 38:370-377.
19. Feletou, M., and P. M. Vanhoutte. 2006. Endothelium-derived hyperpolarizing factor: Where are we now? Arterioscler. Thromb. Vasc. Biol. 26:1215-1225.
20. Feron, O., and J. L. Balligand. 2006. Caveolins and the regulation of endothelial nitric oxide synthase in the heart. Cardiovasc. Res. 69:788-797.
21. Ferrario, C. M., and S. N. Iyer. 1998. Angiotensin-(1-7): A bioactive fragment of the renin-angiotensin system. Regul. Pept. 78:13-18.
22. Foote, W. C., A. L. Pope, C. R. Earl, A. B. Chapman, and L. E. Casida. 1958. Reproduction in the yearling ewe as affected by breed and sequence of feeding levels: II. Effects on fetal development. J. Anim. Sci. 18:463-474.
23. Ford, S. P. 1995. Control of blood flow to the gravid uterus of domestic livestock species. J. Anim. Sci. 73:1852-1860.
24. Ford, S. P. 1999. Cotyledonary placenta. In: E. Knobil and J. D. Neil, editors, Encyclopedia of reproduction. Academic Press, San Diego, CA. p. 730-738.
25. Ford, S. P., and S. L. Stice. 1985. Effects of the ovary and conceptus on uterine blood flow in the pig. J. Reprod. Fert. Suppl. 33:83-90.
26. Fowden, A. L., A. J. Forhead, P. M. Caon, and G. J. Burton. 2008. The placenta and intrauterine programming. J. Neuroendocrinol. 20:439-450.
27. Fowden, A. L., D. A. Giussani, and A. J. Forhead. 2006. Intrauterine programming of physiology systems: Causes and consequences. Physiology 21:29-37.
28. Funston, R. N., D. L. Larson, and K. A. Vonnahme. 2010. Impacts of maternal nutrition on conceptus growth and offspring performance: Implications for beef cattle production. J. Anim. Sci. 88(E.-Suppl.):E205-E215.
29. Funston, R. N., A. F. Summers, and A. J. Roberts. 2012. Alpharma Beef Cattle Nutrition Symposium: Implications of nutritional management for beef cow-calf systems. J. Anim. Sci. 90:2301-2307.
30. Garris, D. R., G. J. Kasperek, S. V. Overton, and G. R. Alligood Jr. 1985. Effects of exercise on fetal-placental growth and uteroplacental blood flow in the rat. Biol. Neonate 47:223-229.
31. Godfrey, K. M., and D. J. Barker. 2000. Fetal nutrition and adult disease. Am. J. Clin. Nutr. 71:1344S-1352S.
32. Grazul-Bilska, A. T., J. S. Caton, W. Arndt, K. Burchill, C. Thorson, E. Borowczyk, J. J. Bilski, D. A. Redmer, L. P. Reynolds, and K. A. Vonnahme. 2009. Cellular proliferation and vascularization in ovine fetal ovaries: Effects of undernutrition and selenium in maternal diet. Reproduction 137:699-707.
33. Hammer, C. J., J. F. Thorson, A. M. Meyer, D. A. Redmer, J. S. Luther, T. L. Neville, J. J. Reed, L. P. Reynolds, J. S. Caton, and K. A. Vonnahme. 2011. Effects of maternal selenium supply and plane of nutrition during gestation on passive transfer of immunity and health in neonatal lambs. J. Anim. Sci. 89:3690-3698.
34. Harris, E. K., E. P. Berg, E. L. Berg, and K. A. Vonnahme. 2013. Effect of maternal activity during gestation on maternal behavior, fetal growth, umbilical blood flow, and farrowing characteristics in pigs. J. Anim. Sci. 91:734-744.
35. Heasman, L., L. Clarke, K. Firth, T. Stephenson, and M. E. Symonds. 1998. Influence of restricted maternal nutrition in early to mid gestation on placental and fetal development at term in sheep. Pediatr. Res. 44:546-551.
36. Houghton, P. E., M. F. Mottola, J. H. Plust, and C. L. Schachter. 2000. Effect of maternal exercise on fetal and placental glycogen storage in the mature rat. Can. J. Appl. Physiol. 25:443-452.
37. Ignarro, L. J., R. E. Byrns, G. M. Buga, and K. S. Wood. 1987. Endothelium-derived relaxing factor from pulmonary artery and vein possesses pharmacologic and chemical properties identical to those of nitric oxide radical. Circ. Res. 61:866-879.
38. Inagami, T., D. F. Duo, and Y. Kitami. 1994. Molecular biology of angiotensin II receptors: An overview. J. Hypertens. Suppl. 12:S83-S94.
39. Isla, M., and D. C. Dyer. 1990. Characterization of alpha-adrenoceptors in the late pregnant ovine uterine artery. Eur. J. Pharmacol. 178:321-331.
40. Jansson, T. 1988. Responsiveness to norepinephrine of the vessels supplying the placenta of growth-retarded fetuses. Am. J. Obstet. Gynecol. 158:1233-1237.
41. Jansson, T., and T. L. Powell. 2007. Role of the placenta in fetal programming: Underlying mechanisms and potential interventional approaches. Clin. Sci. 113:1-13.
42. Knight, J. W., F. W. Bazer, W. W. Thatcher, D. E. Franke, and H. D. Wallace. 1977. Conceptus development in intact and unilaterally hysterectomized-ovariectomized gilts: Interrelations among hormonal status, placental development, fetal fluids and fetal growth. J. Anim. Sci. 44:620-637.
43. Koukoulas, I., T. Mustafa, R. Douglas-Denton, and E. M. Wintour. 2002. Angiotensin II receptor (type 1 and 2) expression peaks when placental growth is maximal in sheep. Am. J. Physiol. 283:R972-R982.
44. Lammers, P. J., M. S. Honeyman, J. W. Mabry, and J. D. Harmon. 2007. Performance of gestating sows in bedded hoop barns and confinement stalls. J. Anim. Sci. 85:1311-1317.
45. Larson, D. M., J. L. Martin, D. C. Adams, and R. N. Funston. 2009. Winter grazing system and supplementation during late gestation influence performance of beef cows and steer progeny. J. Anim. Sci. 87:1147-1155.
46. Lekatz, L. A., J. S. Caton, J. B. Taylor, L. P. Reynolds, D. A. Redmer, and K. A. Vonnahme. 2011a. Maternal selenium supplementation and timing of nutrient restriction in pregnant sheep: Impacts on maternal endocrine status and placental characteristics. J. Anim. Sci. 88:955-971.
47. Lekatz, L.A., J. S. Luther, J. S. Caton, and K.A. Vonnahme. 2013. Impacts of maternal nutritional plane on umbilical artery hemodynamics, fetal, and placentome growth in sheep. Anim. Reprod. (In press.)
48. Lekatz, L. A., A. Reyaz, M. S. Sane, F. Yao, S. T. O'Rourke, C. Schwartz, M. L. Van Emon, C. S. Schauer, K. M. Carlin, C. O. Lemley, and K. A. Vonnahme. 2012. Influence of metabolizable protein supplementation during late gestation on vasoreactivity of maternal placental arteries in sheep. J. Anim. Sci. 90 (Suppl. 3):473 (Abstr.).
49. Lekatz, L. A., M. L. Van Emon, P. K. Shukla, S. T. O'Rourke, C. S. Schauer, K. M. Carlin, and K. A. Vonnahme. 2010. Influence of metabolizable protein supplementation during late gestation on vasoreactivity of maternal and fetal placental arteries in sheep. J. Anim. Sci. 88(E. Suppl. 2):869-870.
50. Lekatz, L. A., G. Wu, J. S. Caton, J. B. Taylor, L. P. Reynolds, D. A. Redmer, and K. A. Vonnahme. 2011b. Maternal selenium supplementation and timing of nutrient restriction in pregnant sheep: Impacts on nutrient availability to the fetus. J. Anim. Sci. 89:59-76.
51. Lemley, C. O., L. E. Camacho, A. M. Meyer, M. Kapphahn, J. S. Caton, and K. A. Vonnahme. 2013. Dietary melatonin supplementation alters fetal amino acids consumption during intrauterine growth restriction in ewes. Animal. (In press.)
52. Lemley, C. O., A. M. Meyer, L. E. Camacho, T. L. Neville, P. Shukla, S. T. O'Rourke, J. S. Caton, and K. A. Vonnahme. 2011. Umbilical cord blood flow following melatonin supplementation in adequately fed or nutrient restricted ewes. Biol. Reprod. 85:458.
53. Lotgering, F. K., R. D. Gilbert, and L. D. Longo. 1983a. Exercise responses in pregnant sheep: Blood gases, temperatures, and fetal cardiovascular system. J. Appl. Physiol. 55:842-850.
54. Lotgering, F. K., R. D. Gilbert, and L. D. Longo. 1983b. Exercise responses in pregnant sheep: Oxygen consumption, uterine blood flow, and blood volume. J. Appl. Physiol. 55:834-841.
55. Ma, X., M. W. Chapleau, C. A. Whiteis, F. M. Abboud, and K. Bielefeldt. 2001. Angiotensin selectively activates a subpopulation of postganglionic sympathetic neurons in mice. Circ. Res. 88:787-793.
56. Mackanjee, H. R., P. W. Shaul, R. R. Magness, and C. R. Rosenfeld. 1991. Angiotensin II vascular smooth muscle receptors are not down-regulated in near-term pregnant sheep. Am. J. Obstet. Gynecol. 165:1641-1648.
57. Madeddu, P., C. Emanueli, and S. El-Dahr. 2007. Mechanisms of disease: The tissue kallikrein-kinin system in hypertension and vascular remodeling. Nat. Clin. Pract. Nephrol. 3:208-221.
58. Martin, J. L., K. A. Vonnahme, D. C. Adams, G. P. Lardy, and R. N. Funston. 2007. Effects of dam nutrition on growth and reproductive performance of heifer calves. J. Anim. Sci. 85:841-847.
59. McMullen, J. R., K. J. Gibson, E. R. Lumbers, J. H. Burrell, and J. Wu. 1999. Interactions between AT1 and AT2 receptors in uterine arteries from pregnant ewes. Eur. J. Pharmacol. 378:195-202.
60. McMullen, S., J. C. Osgerby, J. S. Milne, J. M. Wallace, and D. C. Wathes. 2005. The effects of acute nutrient restriction in the mid-gestational ewe on maternal and fetal nutrient status, the expression of placental growth factors and fetal growth. Placenta 26:25-33.
61. McMurray, R. G., M. F. Mottola, L. A. Wolfe, R. Artal, L. Millar, and J. M. Pivarnik. 1993. Recent advances in understanding maternal and fetal responses to exercise. Med. Sci. Sports Exerc. 25:1305-1321.
62. Meyer, A. M., J. J. Reed, T. L. Neville, J. B. Taylor, C. J. Hammer, L. P. Reynolds, D. A. Redmer, K. A. Vonnahme, and J. S. Caton. 2010. Effects of nutritional plane and selenium supply during gestation on ewe and neonatal offspring performance, body composition, and serum selenium. J. Anim. Sci. 88:1786-1800.
63. Morrison, J. L. 2008. Sheep models of intrauterine growth restriction: Fetal adaptations and consequences. Clin. Exp. Pharmacol. Physiol. 35:730-43.
64. Myatt, L. 2006. Placental adaptive responses and fetal programming. J. Physiol. 572:25-30.
65. Neville, T. L., J. S. Caton, C. J. Hammer, J. J. Reed, J. S. Luther, J. B. Taylor, D. A. Redmer, L. P. Reynolds, and K. A. Vonnahme. 2010. Ovine offspring growth and diet digestibility are influenced by maternal selenium supplementation and nutritional intake during pregnancy despite a common postnatal diet. J. Anim. Sci. 88:3645-3656.
66. Nielsen, A. H., H. Winther, V. Dantzer, and K. Poulsen. 1996. High densities of angiotensin II subtype 2 (AT2) receptors in the porcine placenta and fetal membranes. Placenta 17:147-153.
67. Nishimura, H. 2001. Angiotensin receptors-Evolutionary overview and perspectives. Comp. Biochem. Physiol. Part A 128:11-30.
68. NRC, 2007. Nutrient requirements of small ruminants. Washington DC: National Academy Press.
69. Regnault, T. R. H., H. L. Galan, T. A. Parker, and R. V. Anthony. 2002. Placental development in normal and compromised pregnancies-A review. Placenta 23:S119-S129.
70. Reyaz, A., F. Yao, M. S. Sane, L. E. Camacho, C. O. Lemley, K. C. Swanson, S. T. O'Rourke, and K. A. Vonnahme. 2012. Nutrient restriction during early pregnancy alters cotyledonary arterial vascular reactivity in response to bradykinin in beef cows. J. Anim. Sci. 90(Suppl. 3):323 (Abstr.).
71. Reynolds, L. P., P. Borowicz, K. A. Vonnahme, M. L. Johnson, A. T. Grazul-Bilska, J. M. Wallace, J. S Caton, and D. A. Redmer. 2005. Animal models of placental angiogenesis. Placenta 26:689-708.
72. Reynolds, L. P., J. S. Caton, D. A. Redmer, A. T. Grazul-Bilska, K. A. Vonnahme, P. P. Borowicz, J. S. Luther, J. M. Wallace, G. Wu, and T. E. Spencer. 2006. Evidence for altered placental blood flow and vascularity in compromised pregnancies. J. Physiol. 572:51-58.
73. Reynolds, L. P., C. L. Ferrell, D. A. Robertson, and J. Klindt. 1990. Growth hormone, insulin and glucose concentrations in bovine fetal and maternal plasmas at several stages of gestation. J. Anim. Sci. 68:725-733.
74. Reynolds, L. P., and D. A. Redmer. 1995. Utero-placental vascular development and placental function. J. Anim. Sci. 73:1839-1851.
75. Ribeiro, C. A., and T. A. Macedo. 1986. Pharmacological characterization of the postsynaptic alpha-adrenoceptors in human uterine artery. J. Pharm. Pharmacol. 38:600-605.
76. Richter, H. G., J. A. Hansell, S. Raut, and D. A. Giussani. 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.
77. Robinson, J., S. Chidzanja, K. Kind, F Lok, P. Owens, and J. Owen. 1995. Placental control of fetal growth. Reprod. Fertil. Dev. 7:333-344.
78. Rosenfeld, C. R. 1984. Consideration of the uteroplacental circulation in intrauterine growth. Semin. Perinatol. 8:42-51.
79. Rosenfeld, C. R. 2001. Mechanisms regulating angiotensin II responsiveness by the uteroplacental circulation. Am. J. Physiol. 281:R1025-R1040.
80. Rosenfeld, C. R., and D. E. Fixler. 1977. Cardiovascular changes and heart disease in pregnancy. In: J. T. Willerson and C. A. Saunders, editors, Clinical cardiology, the science and practice of clinical medicine (vol. 3). Grune and Stratton, New York, NY. p. 477-482.
81. Rosenfeld, C. R., A. Gresores, T. A. Roy, and R. R. Magness. 1995. Comparison of ANG II in fetal and pregnant sheep: Metabolic clearance and vascular sensitivity. Am. J. Phys. 268:E237-E247.
82. Sampaio, W. O., A. A. Nascimento, and R. A. Santos. 2003. Systemic and regional hemodynamic effects of angiotensin-(1-7) in rats. Am. J. Physiol. 284:H1985-H1994.
83. Satterfield, M. C., F. W. Bazer, T. E. Spencer, and G. Wu. 2010. Sildenafil citrate treatment enhances amino acid availability in the conceptus and fetal growth in an ovine model of intrauterine growth restriction. J. Nutr. 140:251-258.
84. Sauer, J. J. 1987. Adrenergic control of blood flow through fetal and maternal components of the bovine placentome. MS Thesis. Iowa State University, Ames, IA.
85. Sauer, J. J., D. E. Van Orden, D. B. Farley, and S. P. Ford. 1989. Changing adrenergic sensitivity of the caruncular arterial vasculature supplying the bovine placentome. J. Anim. Sci. 67:3003-3010.
86. Schauser, K. H., A. H. Nielsen, H. Winther, V. Dantzer, and K. Poulsen. 1998. Autoradiographic localization and characterization of angiotensin II receptors in the bovine placenta and fetal membranes. Biol. Reprod. 59:684-692.
87. Shnider, S. M., R. G. Wright, G. Levinson, M. F. Roizen, K. L. Wallis, S. J. Rolbin, and J. B. Craft. 1979. Uterine blood flow and plasma norepinephrine changes during maternal stress in the pregnant ewe. Anesthesiology 50:524-527.
88. Stalker, L. A., D. C. Adams, T. J. Klopfenstein, D. M. Feuz, and R. N. Funston. 2006. Effects of pre-and postpartum nutrition on reproduction in spring calving cows and calf feedlot performance. J. Anim. Sci. 84:2582-2589.
89. Stegeman, J. H. J. 1974. Placental development in the sheep and its relation to fetal development. Bijdragen tot de dierkunde 44:3-72.
90. Swanson, T. J., C. J. Hammer, J. S. Luther, D. B. Carlson, J. B. Taylor, D. A. Redmer, T. L. Neville, J. J. Reed, L. P. Reynolds, J. S. Caton, and K. A. Vonnahme. 2008. Effects of plane of nutrition and selenium supplementation on colostrum quality and mammary development in pregnant ewe lambs. J. Anim. Sci. 86:2415-2423.
91. Torres-Farfan, C., F. J. Valenzuela, M. Mondaca, G. J. Valenzuela, B. Krause, E. A. Herreral, R. Riquelme, A. J. Llanos, and M. Seron-Ferre. 2008. Evidence of a role for melatonin in fetal sheep physiology: Direct actions of melatonin on fetal cerebral artery, brown adipose tissue and adrenal gland. J. Physiol. 586:4017-4027.
92. Vandenbosche, R. C., and J. T. Kirchner. 1998. Intrauterine growth retardation. Am. Fam. Physician 58:1384-1390.
93. Vonnahme, K. A. 2012. Effects of fetal programming on skeletal muscle growth. In: Proc. Am. Meat Science Assoc. 65th Annual Reciprocal Meat Conference, Fargo, ND. p. 58-60.
94. Vonnahme, K. A., W. J. Arndt, M. L. Johnson, P. P. Borowicz, and L. P. Reynolds. 2008. Effect of morphology on placentome size, vascularity, and vasoreactivity in late pregnant sheep. Biol. Reprod. 79:976-982.
95. Vonnahme, K. A., and S. P. Ford. 2004. Placental vascular endothelial growth factor receptor system mRNA expression in pigs selected for placental efficiency. J. Physiol. 554:194-201.
96. Vonnahme, K. A., J. S. Luther, L. P. Reynolds, C. J. Hammer, D. B. Carlson, D. A. Redmer, and J. S. Caton. 2010. Impacts of maternal selenium and nutritional level on growth, adiposity, and glucose tolerance in female offspring in sheep. Domest. Anim. Endocrinol. 39:240-248.
97. Vonnahme, K. A., M. E. Wilson, and S. P. Ford. 2001. Relationship between placental vascular endothelial growth factor expression and placental/endometrial vascularity in the pig. Biol. Reprod. 64:1821-1825.
98. Vonnahme, K. A., M. J. Zhu, P. P. Borowicz, T. W. Geary, B. W. Hess, L. P. Reynolds, J. S. Caton, W. J. Means, and S. P. Ford. 2007. Effect of early gestational undernutrition on angiogenic factor expression and vascularity in the bovine placentome. J. Anim. Sci. 85:2464-2472.
99. Vosatka, R. J., P. M. Hassoun, and K. B. Harvey-Wilkes. 1998. Dietary L-arginine prevents fetal growth restriction in rats. Am. J. Obstet. Gynecol. 178:242-246.
100. Wallace, J. M, D. A. Bourke, and R. P. Aitken. 1999. Nutrition and fetal growth: Paradoxical effects in the overnourished adolescent sheep. J. Reprod. Fertil. Suppl. 54:385-399.
101. Wallace, J. M., D. A. Bourke, R. P. Aitken, N. Leitch, and W. W. Hay Jr. 2002. Blood flows and nutrient uptakes in growth-restricted pregnancies induced by overnourishing adolescent sheep. Am. J. Physiol. 282:R1027-R1036.
102. Wallace, L. R. 1948a. The growth of lambs before and after birth in relation to the level of nutrition. J. Agric. Sci. 38:243-300.
103. Wallace, L. R. 1948b. The growth of lambs before and after birth in relation to the level of nutrition. J. Agric. Sci. 38:367-398.
104. Walther, T., A. Menrad, H. D. Orzechowski, G. Siemeister, M. Paul, and M. Schirner. 2003. Differential regulation of in vivo angiogenesis by angiotensin II receptors. FASEB J. 17:2061-2067.
105. Wiemer, G., B. A. Scholkens, A. Wagner, H. Heitsch, and W. Linz. 1993. The possible role of angiotensin II subtype AT2 receptors in endothelial cells and isolated ischemic rat hearts. J. Hypertens. Suppl. 11:S234-S235.
106. Wu, G., F. W. Bazer, J. M. Wallace, and T. E. Spencer. 2006. Intrauterine growth retardation: Implications for the animal sciences. J. Anim. Sci. 84:2316-2337.
107. Yoshimura, T., R. R. Magness, and C. R. Rosenfeld. 1990. Angiotensin II and alpha-agonist. I. Responses of ovine fetoplacental vasculature. Am. J. Physiol. 259:H464-H472.
108. Zhu, M. J., M. Du, B. W. Hess, W. J. Means, P. W. Nathanielsz, and S. P. Ford. 2007. Maternal nutrient restriction upregulates growth signaling pathway in the cotyledonary artery of cow placentomes. Placenta 28:361-368.