Placental phenotype and resource allocation to fetal growth are modified by the timing and degree of hypoxia during mouse pregnancy

Journal of Physiology

Volumn 594, Issue 5, 2016, Pages 1341-1356

  Higgins, J S ^a   Vaughan, O R ^a   Fernandez de Liger, E ^a   Fowden, A L ^a   Sferruzzi Perri, A N ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 2 METHYLPROPIONIC ACID; CARBON 14 METHYLAMINOISOBUTYRIC ACID; INSULIN; LEPTIN; OXYGEN; SOMATOMEDIN B; UNCLASSIFIED DRUG; GLUCOSE BLOOD LEVEL;

AMINO ACID TRANSPORT; ANIMAL EXPERIMENT; ARTICLE; BLOOD VOLUME; CONTROLLED STUDY; DISEASE SEVERITY; ENVIRONMENTAL EXPOSURE; FEMALE; FETUS GROWTH; GENE; GENE EXPRESSION; GESTATION PERIOD; GLUCOSE TRANSPORT; HORMONE BLOOD LEVEL; HYPOPHAGIA; HYPOXIA; IGF2 GENE; MOUSE; NONHUMAN; NUTRIENT AVAILABILITY; PHENOTYPE; PLACENTA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ADAPTATION; ANIMAL; C57BL MOUSE; COMPLICATION; FETAL GROWTH RETARDATION; FETUS HYPOXIA; GENETICS; GLUCOSE BLOOD LEVEL; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PREGNANCY; SECOND MESSENGER;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BLOOD GLUCOSE; FEMALE; FETAL GROWTH RETARDATION; FETAL HYPOXIA; INSULIN; INSULIN-LIKE GROWTH FACTOR II; MICE; MICE, INBRED C57BL; OXYGEN; PHENOTYPE; PLACENTA; PREGNANCY; SECOND MESSENGER SYSTEMS;

EID: 84959294504     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP271057     Document Type: Article

References (79)

1. Ali KZM, Burton GJ, Morad N & Ali ME (1996). Does hypercapillarization influence the branching pattern of terminal villi in the human placenta at high altitude?Placenta 17, 677-682.
2. Bacon BJ, Gilbert RD, Kaufmann P, Smith AD, Trevino FT & Longo LD (1984). Placental anatomy and diffusing capacity in guinea pigs following long-term maternal hypoxia. Placenta 5, 475-487.
3. Burton GJ & Fowden AL (2012). Review: the placenta and developmental programming: balancing fetal nutrient demands with maternal resource allocation. Placenta 33, S23-S27.
4. Burton GJ & Fowden AL (2015). The placenta: a multifaceted, transient organ. Philos Trans R Soc Lond B Biol Sci 370, 20140066.
5. Cetin I (2003). Placental transport of amino acids in normal and growth-restricted pregnancies. Eur J Obstet Gynecol Reprod Biol 110(Suppl 1), S50-S54.
6. Coan PM, Ferguson-Smith AC & Burton GJ (2004). Developmental dynamics of the definitive mouse placenta assessed by stereology. Biol Reprod 70, 1806-1813.
7. Coan PM, Fowden AL, Constancia M, Ferguson-Smith AC, Burton GJ & Sibley CP (2008). Disproportional effects of Igf2 knockout on placental morphology and diffusional exchange characteristics in the mouse. J Physiol 586, 5023-5032.
8. Coan PM, Vaughan OR, McCarthy J, Mactier C, Burton GJ, Constancia M & Fowden AL (2011). Dietary composition programmes placental phenotype in mice. J Physiol 589, 3659-3670.
9. Coan PM, Vaughan OR, Sekita Y, Finn SL, Constancia M, Burton GJ & Fowden AL (2010). Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice. J Physiol 588, 527-538.
10. Constancia M, Angiolini E, Sandovici I, Smith P, Smith R, Kelsey G, Dean W, Ferguson-Smith A, Sibley CP, Reik W & Fowden A (2005). Adaptation of nutrient supply to fetal demand in the mouse involves interaction between the Igf2 gene and placental transporter systems. Proc Natl Acad Sci USA 102, 19219-19224.
11. Cramer S, Beveridge M, Kilberg M & Novak D (2002). Physiological importance of system A-mediated amino acid transport to rat fetal development. Am J Physiol Cell Physiol 282, C153-C160.
12. Cuffe JS, Walton SL, Singh RR, Spiers JG, Bielefeldt-Ohmann H, Wilkinson L, Little MH & Moritz KM (2014). 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.
13. Diaz P, Powell TL & Jansson T (2014). The role of placental nutrient sensing in maternal-fetal resource allocation. Biol Reprod 91, 82.
14. Dwyer CM & Stickland NC (1992). The effects of maternal undernutrition on maternal and fetal serum insulin-like growth factors, thyroid hormones and cortisol in the guinea pig. J Dev Physiol 18, 303-313.
15. Efeyan A, Comb WC & Sabatini DM (2015). Nutrient-sensing mechanisms and pathways. Nature 517, 302-310.
16. Feldser D, Agani F, Iyer NV, Pak B, Ferreira G & Semenza GL (1999). Reciprocal positive regulation of hypoxia-inducible factor 1alpha and insulin-like growth factor 2. Cancer Res 59, 3915-3918.
17. Fernandez-Twinn DS, Ozanne SE, Ekizoglou S, Doherty C, James L, Gusterson B & Hales CN (2003). The maternal endocrine environment in the low-protein model of intra-uterine growth restriction.Br J Nutr 90, 815-822.
18. Fowden AL, Sferruzzi-Perri AN, Coan PM, Constancia M & Burton GJ (2009). Placental efficiency and adaptation: endocrine regulation. Journal of Physiology 587, 3459-3472.
19. Fowden AL, Ward JW, Wooding FP, Forhead AJ & Constancia M (2006). Programming placental nutrient transport capacity. J Physiol 572, 5-15.
20. Ganguly A, Collis L & Devaskar SU (2012). Placental glucose and amino acid transport in calorie-restricted wild-type and Glut3 null heterozygous mice. Endocrinology 153, 3995-4007.
21. Gheorghe CP, Mohan S, Oberg KC & Longo LD (2007). Gene expression patterns in the hypoxic murine placenta: a role in epigenesis?Reprod Sci 14, 223-233.
22. Giussani DA & Davidge ST (2013). Developmental programming of cardiovascular disease by prenatal hypoxia. J Dev Orig Hlth Dis 4, 328-337.
23. Giussani DA, Phillips PS, Anstee S & Barker DJ (2001). Effects of altitude versus economic status on birth weight and body shape at birth. Pediatr Res 49, 490-494.
24. Glazier JD, Cetin I, Perugino G, Ronzoni S, Grey AM, Mahendran D, Marconi AM, Pardi G & Sibley CP (1997). Association between the activity of the system A amino acid transporter in the microvillous plasma membrane of the human placenta and severity of fetal compromise in intrauterine growth restriction. Pediatr Res 42, 514-519.
25. Hutter D, Kingdom J & Jaeggi E (2010). Causes and mechanisms of intrauterine hypoxia and its impact on the fetal cardiovascular system: a review. Int J Pediatr 401323, 19.
26. Hvizdosova-Klescova A, Uhlik J, Malina M, Vulterinova H, Novotny T & Vajner L (2013). Remodeling of fetoplacental arteries in rats due to chronic hypoxia. Exp Toxicol Pathol 65, 97-103.
27. Illsley NP, Caniggia I & Zamudio S (2010). Placental metabolic reprogramming: do changes in the mix of energy-generating substrates modulate fetal growth?Int J Dev Biol 54, 409-419.
28. Jacobs R, Robinson JS, Owens JA, Falconer J & Webster ME (1988). The effect of prolonged hypobaric hypoxia on growth of fetal sheep. J Dev Physiol 10, 97-112.
29. Jansson N, Greenwood SL, Johansson BR, Powell TL & Jansson T (2003). Leptin stimulates the activity of the system A amino acid transporter in human placental villous fragments. J Clin Endocrinol Metab 88, 1205-1211.
30. Jansson N, Pettersson J, Haafiz A, Ericsson A, Palmberg I, Tranberg M, Ganapathy V, Powell TL & Jansson T (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.
31. Jansson T, Scholtbach V & Powell TL (1998). Placental transport of leucine and lysine is reduced in intrauterine growth restriction. Pediatr Res 44, 532-537.
32. Jansson T, Ylven K, Wennergren M & Powell TL (2002). Glucose transport and system A activity in syncytiotrophoblast microvillous and basal plasma membranes in intrauterine growth restriction. Placenta 23, 392-399.
33. Jones HN, Woollett LA, Barbour N, Prasad PD, Powell TL & 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.
34. Kavitha JV, Rosario FJ, Nijland MJ, McDonald TJ, Wu G, Kanai Y, Powell TL, Nathanielsz PW & Jansson T (2014). Down-regulation of placental mTOR, insulin/IGF-I signaling, and nutrient transporters in response to maternal nutrient restriction in the baboon. FASEB J 28, 1294-1305.
35. King V, Hibbert N, Seckl JR, Norman JE & Drake AJ (2013). The effects of an obesogenic diet during pregnancy on fetal growth and placental gene expression are gestation dependent. Placenta 34, 1087-1090.
36. Kleppa MJ, Erlenwein SV, Darashchonak N, von Kaisenberg CS & von Versen-Hoynck F (2014). Hypoxia and the anticoagulants dalteparin and acetylsalicylic acid affect human placental amino acid transport. PLoS ONE 9, e99217.
37. Krebs C, Macara LM, Leiser R, Bowman AW, Greer IA & Kingdom JC (1996). Intrauterine growth restriction with absent end-diastolic flow velocity in the umbilical artery is associated with maldevelopment of the placental terminal villous tree. Am J Obstet Gynecol 175, 1534-1542.
38. Lager S, Samulesson AM, Taylor PD, Poston L, Powell TL & Jansson T (2014). Diet-induced obesity in mice reduces placental efficiency and inhibits placental mTOR signaling. Physiol Rep 2, e00242.
39. Lueder FL, Kim SB, Buroker CA, Bangalore SA & Ogata ES (1995). Chronic maternal hypoxia retards fetal growth and increases glucose utilization of select fetal tissues in the rat. Metabolism 44, 532-537.
40. Ma Y, Zhu MJ, Uthlaut AB, Nijland MJ, Nathanielsz PW, Hess BW & Ford SP (2011). Upregulation of growth signaling and nutrient transporters in cotyledons of early to mid-gestational nutrient restricted ewes. Placenta 32, 255-263.
41. Malandro MS, Beveridge MJ, Kilberg MS & Novak DA (1996). Effect of low-protein diet-induced intrauterine growth retardation on rat placental amino acid transport. Am J Physiol Cell Physiol 271, C295-C303.
42. Mayhew TM (1998). Thinning of the intervascular tissue layers of the human placenta is an adaptive response to passive diffusion in vivo and may help to predict the origins of fetal hypoxia. Eur J Obstet Gynecol Reprod Biol 81, 101-109.
43. McMillen IC & Robinson JS. (2005). Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 85, 571-633.
44. Mogami H, Yura S, Itoh H, Kawamura M, Fujii T, Suzuki A, Aoe S, Ogawa Y, Sagawa N, Konishi I & Fujii S (2009). Isocaloric high-protein diet as well as branched-chain amino acids supplemented diet partially alleviates adverse consequences of maternal undernutrition on fetal growth. Growth HormIGF Res 19, 478-485.
45. Moore LG, Charles SM & Julian CG (2011). Humans at high altitude: hypoxia and fetal growth. Respir Physiol Neurobiol 178, 181-190.
46. Myatt L (2006). Placental adaptive responses and fetal programming. J Physiol 572, 25-30.
47. Nelson DM, Smith SD, Furesz TC, Sadovsky Y, Ganapathy V, Parvin CA & Smith CH (2003). Hypoxia reduces expression and function of system A amino acid transporters in cultured term human trophoblasts. Am J Physiol Cell Physiol 284, C310-C315.
48. Parraguez VH, Atlagich M, Diaz R, Bruzzone ME, Behn C & Raggi LA (2005). Effect of hypobaric hypoxia on lamb intrauterine growth: comparison between high- and low-altitude native ewes. Reprod Fert Develop 17, 497-505.
49. Parraguez VH, Atlagich M, Diaz R, Cepeda R, Gonzalez C, De los Reyes M, Bruzzone ME, Behn C & Raggi LA (2006). Ovine placenta at high altitudes: comparison of animals with different times of adaptation to hypoxic environment. Anim Reprod Sci 95, 151-157.
50. Penninga L & Longo LD (1998). Ovine placentome morphology: effect of high altitude, long-term hypoxia. Placenta 19, 187-193.
51. Postigo L, Heredia G, Illsley NP, Torricos T, Dolan C, Echalar L, Tellez W, Maldonado I, Brimacombe M, Balanza E, Vargas E & Zamudio S (2009). Where the O2 goes to: preservation of human fetal oxygen delivery and consumption at high altitude. J Physiol 587, 693-708.
52. Rosario FJ, Jansson N, Kanai Y, Prasad PD, Powell TL & 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.
53. Rosso P (1977). Maternal-fetal exchange during protein malnutrition in the rat. Placental transfer of glucose and a nonmetabolizable glucose analog. J Nutr 107, 20006-20010.
54. Saker F, Voora DM, Mahajan SD, Kilic I, Ismail-Beigi F & Kalhan SC (1999). Effect of reduced inspired oxygen on fetal growth and maternal glucose metabolism in rat pregnancy. Metabolism 48, 738-744.
55. Schmittgen TD & Livak KJ (2008). Analyzing real-time PCR data by the comparative C-T method. Nat Protoc 3, 1101-1108.
56. Sferruzzi-Perri AN, Owens JA, Pringle KG & Roberts CT (2010). The neglected role of insulin-like growth factors in the maternal circulation regulating fetal growth. J Physiol 589, 7-20.
57. Sferruzzi-Perri AN, Vaughan OR, Coan PM, Suciu MC, Darbyshire R, Constancia M, Burton GJ & Fowden AL (2011). Placental-specific Igf2 deficiency alters developmental adaptations to undernutrition in mice. Endocrinology 152, 3202-3212.
58. Sferruzzi-Perri AN, Vaughan OR, Forhead AJ & Fowden AL (2013a). Hormonal and nutritional drivers of intrauterine growth. Curr Opin Clin Nutr Metab Care 16, 298-309.
59. Sferruzzi-Perri AN, Vaughan OR, Haro M, Cooper WN, Musial B, Charalambous M, Pestana D, Ayyar S, Ferguson-Smith AC, Burton GJ, Constancia M & Fowden AL (2013b). An obesogenic diet during mouse pregnancy modifies maternal nutrient partitioning and the fetal growth trajectory. FASEB 27, 3928-3937.
60. Sibley CP, Coan PM, Ferguson-Smith AC, Dean W, Hughes J, Smith P, Reik W, Burton GJ, Fowden AL & Constância M (2004). Placental-specific insulin-like growth factor 2 (Igf2) regulates the diffusional exchange characteristics of the mouse placenta. Proc Natl Acad Sci USA 101, 8204-8208.
61. Skeffington KL, Higgins JS, Mahmoud AD, Evans AM, Sferruzzi-Perri AN, Fowden AL, Yung HW, Burton GJ, Giussani DA & Moore LG (2016). Hypoxia, AMPK activation and uterine artery vasoreactivity. J Physiol 594, 1357-1369.
62. Soria R, Julian CG, Vargas E, Moore LG & Giussani DA (2013). Graduated effects of high-altitude hypoxia and highland ancestry on birth size. Pediatr Res 74, 633-638.
63. Storz JF, Sabatino SJ, Hoffmann FG, Gering EJ, Moriyama H, Ferrand N, Monteiro B & Nachman MW (2007). The molecular basis of high-altitude adaptation in deer mice. Plos Genet 3, e45.
64. Tissot van Patot M, Grilli A, Chapman P, Broad E, Tyson W, Heller DS, Zwerdlinger L & Zamudio S (2003). Remodelling of uteroplacental arteries is decreased in high altitude placentae. Placenta 24, 326-335.
65. Tissot van Patot MC, Murray AJ, Beckey V, Cindrova-Davies T, Johns J, Zwerdlinger L, Jauniaux E, Burton GJ & Serkova NJ (2010). Human placental metabolic adaptation to chronic hypoxia, high altitude: hypoxic preconditioning. Am J Physiol Regul Integr Comp Physiol 298, R166-R172.
66. Vadlakonda L, Dash A, Pasupuleti M, Anil Kumar K & Reddanna P (2013). The paradox of Akt-mTOR interactions. Front Oncol 3, 165.
67. Vaughan OR, Fisher HM, Dionelis KN, Jefferies EC, Higgins JS, Musial B, Sferruzzi-Perri AN & Fowden AL (2015). Corticosterone alters materno-fetal glucose partitioning and insulin signalling in pregnant mice. J Physiol 593, 1307-1321.
68. Vaughan OR, Sferruzzi-Perri AN, Coan PM & Fowden AL (2012a). Environmental regulation of placental phenotype: implications for fetal growth. Reprod Fertil Dev 24, 80-96.
69. Vaughan OR, Sferruzzi-Perri AN & Fowden AL (2012b). Maternal corticosterone regulates nutrient allocation to fetal growth in mice. J Physiol 590, 5529-5540.
70. West JB (2002). Highest permanent human habitation. High Alt Med Biol 3, 401-407.
71. Woodall SM, Breier BH, Johnston BM & Gluckman PD (1996). A model of intrauterine growth retardation caused by chronic maternal undernutrition in the rat: effects on the somatotrophic axis and postnatal growth. J Neuroendocrinol 150, 231-242.
72. Yang Z-Z, Tschopp O, Hemmings-Mieszczak M, Feng J, Brodbeck D, Perentes E & Hemmings BA (2003). Protein kinase Balpha/Akt1 regulates placental development and fetal growth. J Biol Chem 278, 32124-32131.
73. Yung H-w, Calabrese S, Hynx D, Hemmings BA, Cetin I, Charnock-Jones DS & Burton GJ (2008). Evidence of placental translation inhibition and endoplasmic reticulum stress in the etiology of human intrauterine growth restriction. Am J Pathol 173, 451-462.
74. Yung HW, Cox M, Tissot van Patot M & Burton GJ (2012). Evidence of endoplasmic reticulum stress and protein synthesis inhibition in the placenta of non-native women at high altitude. FASEB J 26, 1970-1981.
75. Zamudio S (2003). The placenta at high altitude. High Alt Med Biol 4, 171-191.
76. Zhang S, Regnault TR, Barker PL, Botting KJ, McMillen IC, McMillan CM, Roberts CT & Morrison JL (2015). Placental adaptations in growth restriction. Nutrients 7, 360-389.
77. Zhou J, Xiao D, Hu Y, Wang Z, Paradis A, Mata-Greenwood E & Zhang L (2013). Gestational hypoxia induces preeclampsia-like symptoms via heightened endothelin-1 signaling in pregnant rats. Hypertension 62, 599-607.
78. Zhu MJ, Du M, Hess BW, Nathanielsz PW & Ford SP (2007). Periconceptional nutrient restriction in the ewe alters MAPK/ERK1/2 and PI3K/Akt growth signaling pathways and vascularity in the placentome. Placenta 28, 1192-1199.
79. Zhu MJ, Du M, Nijland MJ, Nathanielsz PW, Hess BW, Moss GE & Ford SP (2009). Down-regulation of growth signaling pathways linked to a reduced cotyledonary vascularity in placentomes of over-nourished, obese pregnant ewes. Placenta 30, 405-410.