Maternal obesity and overnutrition alter fetal growth rate and cotyledonary vascularity and angiogenic factor expression in the ewe

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 299, Issue 1, 2010, Pages

  Ma, Yan ^a   Zhu, Mei J ^a   Zhang, Liren ^a   Hein, Sarah M ^a   Nathanielsz, Peter W ^a,b   Ford, Stephen P ^a  

^a UNIVERSITY OF WYOMING   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Angiogenesis; Cotyledonary vasculature; Pregnancy; Sheep

Indexed keywords

ANGIOPOIETIN 1; ANGIOPOIETIN 2; FIBROBLAST GROWTH FACTOR 2; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; PLACENTAL GROWTH FACTOR; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIOLE; ARTERY DIAMETER; ARTICLE; BLOOD FLOW VELOCITY; BODY WEIGHT; CONTROLLED STUDY; CROWN RUMP LENGTH; EWE; FEMALE; FETUS; FETUS GROWTH; FETUS WEIGHT; GENE EXPRESSION; GESTATIONAL AGE; GROWTH RATE; MATERNAL NUTRITION; NONHUMAN; OBESITY; OVERNUTRITION; PLACENTA CIRCULATION; PLACENTA DEVELOPMENT; PLACENTA WEIGHT; PRIORITY JOURNAL; PROTEIN EXPRESSION; WEIGHT GAIN;

ANGIOGENESIS INDUCING AGENTS; ANGIOPOIETIN-1; ANIMALS; BLOOD VESSELS; DIET; FEMALE; FETAL DEVELOPMENT; FETAL WEIGHT; FETUS; FIBROBLAST GROWTH FACTOR 2; OBESITY; OVERNUTRITION; PLACENTA; PREGNANCY; RNA, MESSENGER; SHEEP; UTERUS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 77954422346     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00498.2009     Document Type: Article

References (54)

1. Anthony RV, Limesand SW, Jeckel KM. Transcriptional regulation in the placenta during normal and compromised fetal growth. Biochem Soc Trans 29: 42-28, 2001.
2. Aron EA, Anthony RV. Angiogenesis. In: Fetal and Neonatal Physiology (3rd ed.), edited by Polin RA, Fox WW, and Abman SH. Philidelphia: Saunders WB Company, 2003, p. 79-84.
3. Babaei S, Teichert-Kuliszewska K, Monge JC, Mohamed F, Bendeck MP, Stewart DJ. Role of nitric oxide in the angiogenic response in vitro to basic fibroblast growth factor. Circ Res 82: 1007-1015, 1998. (Pubitemid 28225941)
4. Barry JS, Anthony RV. The pregnant sheep as a model for human pregnancy. Theriogenology 69: 55-67, 2008.
5. Bassingthwaighte JB, Goresky CA. Modeling in the analysis of solute and water exchange in the microvasculature. In: Handbook of Physiology. The Cardiovascular System. Micrcirculation. Bethesda MD: Am. Physiol. Soc., 1984, set. 2, vol. IV, pt. 1, chapt 13, p. 549-626.
6. Bio-Rad Laboratories. Real-Time PCR Applications Guide. Hercules, CA: Bio-Rad, 2006.
7. Boney CM, Verma A, Tucker R, Vohr BR. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics 115: e290-e296, 2005.
8. Borowicz PP, Arnold DR, Johnson ML, Grazul-Bilska AT, Redmer DA, Reynolds LP. Placental growth throughout the last two thirds of pregnancy in sheep: vascular development and angiogenic factor expression. Biol Reprod 76: 259-267, 2007.
9. Catalano PM, Presley L, Minium J, Hauguel-de Mouzon S. Fetuses of obese mothers develop insulin resistance in utero. Diabetes Care 32: 1076-1080, 2009.
10. Challis JR, Lockwood CJ, Myatt L, Norman JE, Strauss JF, 3rd, Petraglia F. Inflammation and pregnancy. Reprod Sci 16: 206-215, 2009.
11. National Research Council. Nutrient Requirements of Sheep. Washington DC: National Academic Press 1985.
12. Ericsson A, Hamark B, Powell TL, Jansson T. Glucose transporter isoform 4 is expressed in the syncytiotrophoblast of first trimester human placenta. Hum Reprod 20: 521-530, 2005.
13. Ferrell CL. Placental regulation of fetal growth. In: Animal Growth Regulation, edited by Campion DR, Hausman GJ and Martin RJ. New York: Plenum, 1989, p. 1-19.
14. Ford SP, Hess BW, Schwope MM, Nijland MJ, Gilbert JS, Vonnahme KA, Means WJ, Han H, Nathanielsz PW. Maternal undernutrition during early to mid-gestation in the ewe results in altered growth, adiposity, and glucose tolerance in male offspring. J Anim Sci 85: 1285-1294, 2007.
15. Ford SP, Zhang L, Zhu M, Miller MM, Smith DT, Hess BW, Moss GE, Nathanielsz PW, Nijland MJ. Maternal obesity accelerates fetal pancreatic β cell but not α cell development in the sheep: prenatal and postnatal consequences. Am J Physiol Regul Integr Comp Physiol 297: R835-R843, 2009.
16. Fowden AL, Forhead AJ. Effects of pituitary hormone deficiency on growth and glucose metabolism of the sheep fetus. Endocrinology 148: 4812-4820, 2007.
17. Gassmann M, Manini A, Stallmach T, Saam B, Kuhn G, Grenacher B, Bogdanova AY, Vogel J. Abortion in mice with excessive erythrocytosis is due to impaired arteriogenesis of the uterine arcade. Biol Reprod 78: 1049-1057, 2008.
18. Harding JE, Evans PC, Gluckman PD. Maternal growth hormone treatment increases placental diffusion capacity but not fetal or placental growth in sheep. Endocrinology 138: 5352-5358, 1997.
19. Hood JD, Meininger CJ, Ziche M, Granger HJ. VEGF upregulates eNOS message, protein, and NO production in human endothelial cells. Am J Physiol Heart Circ Physiol 274: H1054-H1058, 1998. (Pubitemid 128734103)
20. Jansson N, Greenwood SL, Johansson BR, Powell TL, Jansson T. Leptin stimulates the activity of the system A amino acid transporter in human placental villous fragments. J Clin Endocrinol Metab 88: 1205-1211, 2003.
21. Jansson T, Cetin I, Powell TL, Desoye G, Radaelli T, Ericsson A, Sibley CP. Placental transport and metabolism in fetal overgrowth - a workshop report. Placenta 27 Suppl A: S109-S113, 2006.
22. Johnson ML, Grazul-Bilska AT, Redmer DA, Reynolds LP. Effects of estradiol-17β on expression of mRNA for seven angiogenic factors and their receptors in the endometrium of ovariectomized (OVX) ewes. Endocrine 30: 333-342, 2006.
23. Lang U, Baker RS, Khoury J, Clark KE. Effects of chronic reduction in uterine blood flow on fetal and placental growth in the sheep. Am J Physiol Regul Integr Comp Physiol 279: R53-R59, 2000. (Pubitemid 30625416)
24. Limesand SW, Rozance PJ, Smith D, Hay WW Jr. Increased insulin sensitivity and maintenance of glucose utilization rates in fetal sheep with placental insufficiency and intrauterine growth restriction. Am J Physiol Endocrinol Metab 293: E1716-E1725, 2007.
25. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408, 2001.
26. Lopez-Andreo M, Lugo L, Garrido-Pertierra A, Prieto MI, Puyet A. Identification and quantitation of species in complex DNA mixtures by real-time polymerase chain reaction. Anal Biochem 339: 73-82, 2005.
27. Melbin J, Detweiler DK. The cardiovascular system and blood flow. In: Duke's Physiology of Domestic Animals (11th ed.), edited by Swenson MJ and Reece WO. New York: Cornell University Press, 1993, p. 64-89.
28. Mingrone G, Manco M, Mora ME, Guidone C, Iaconelli A, Gniuli D, Leccesi L, Chiellini C, Ghirlanda G. Influence of maternal obesity on insulin sensitivity and secretion in offspring. Diabetes Care 31: 1872-1876, 2008.
29. Molina RD, Meschia G, Wilkening RB. Uterine blood flow, oxygen and glucose uptakes at mid-gestation in the sheep. Proc Soc Exp Biol Med 195: 379-385, 1990.
30. National Center for Health Statistics. Health, United States, With Chartbook on Trends in the Health of Americans. Hyattsville, MD: National Center for Health Statistics 2007, p. 88-292.
31. Pedersen J. The Pregnant Diabetic and Her Newborn: Problems and Management. Baltimore: Williams & Wilkens, 1967.
32. Recabarren SE, Padmanabhan V, Codner E, Lobos A, Duran C, Vidal M, Foster DL, Sir-Petermann T. Postnatal developmental consequences of altered insulin sensitivity in female sheep treated prenatally with testosterone. Am J Physiol Endocrinol Metab 289: E801-E806, 2005.
33. Redmer DA, Aitken RP, Milne JS, Reynolds LP, Wallace JM. Influence of maternal nutrition on messenger RNA expression of placental angiogenic factors and their receptors at midgestation in adolescent sheep. Biol Reprod 72: 1004-1009, 2005.
34. Redmer DA, Luther JS, Milne JS, Aitken RP, Johnson ML, Borowicz PP, Borowicz MA, Reynolds LP, Wallace JM. Fetoplacental growth and vascular development in overnourished adolescent sheep at day 50, 90 and 130 of gestation. Reproduction 137: 749-757, 2009.
35. Reynolds LP, Borowicz PP, Vonnahme KA, Johnson ML, Grazul-Bilska AT, Wallace JM, Caton JS, Redmer DA. Animal models of placental angiogenesis. Placenta 26: 689-708, 2005.
36. Reynolds LP, Ferrell CL. Transplacental clearance and blood flows of bovine gravid uterus at several stages of gestation. Am J Physiol Regul Integr Comp Physiol 253: R735-R739, 1987.
37. Reynolds LP, Kirsch JD, Kraft KC, Redmer DA. Time-course of the uterine response to estradiol-17β in ovariectomized ewes: expression of angiogenic factors. Biol Reprod 59: 613-650, 1998.
38. Reynolds LP, Redmer DA. Angiogenesis in the placenta. Biol Reprod 64: 1033-1040, 2001.
39. Reynolds LP, Redmer DA. Utero-placental vascular development and placental function. J Anim Sci 73: 1839-1851, 1995.
40. Sanson DW, West TR, Tatman WR, Riley ML, Judkins MB, Moss GE. Relationship of body composition of mature ewes with condition score and body weight. J Anim Sci 71: 1112-1116, 1993.
41. Shih SC, Claffey KP. Regulation of human vascular endothelial growth factor mRNA stability in hypoxia by heterogeneous nuclear ribonucleoprotein L. J Biol Chem 274: 1359-1365, 1999.
42. Simon MP, Tournaire R, Pouyssegur J. The angiopoietin-2 gene of endothelial cells is up-regulated in hypoxia by a HIF binding site located in its first intron and by the central factors GATA-2 and Ets-1. J Cell Physiol 217: 809-818, 2008.
43. Smith JJ, Kampine JP. Circulatory Physiology-The Essentials (3rd ed.). Baltimore: Williams & Wilkins, 1990, 345 p.
44. Stegeman JHJ. Placental development in the sheep and its regulation to fetal development. Bijdragen Tot De Dierkunde 44: 4-72, 1974.
45. Vatnick I, Schoknecht PA, Darrigrand R, Bell AW. Growth and metabolism of the placenta after unilateral fetectomy in twin pregnant ewes. J Dev Physiol 15: 351-356, 1991.
46. Wallace J, Bourke D, Da Silva P, Aitken R. Nutrient partitioning during adolescent pregnancy. Reproduction 122: 347-357, 2001.
47. Wallace JM, Aitken RP, Milne JS, Hay WW, Jr. Nutritionally mediated placental growth restriction in the growing adolescent: consequences for the fetus. Biol Reprod 71: 1055-1062, 2004.
48. Wallace JM, Bourke DA, Aitken RP, Leitch N, Hay WW, Jr. Blood flows and nutrient uptakes in growth-restricted pregnancies induced by overnourishing adolescent sheep. Am J Physiol Regul Integr Comp Physiol 282: R1027-R1036, 2002.
49. Wallace JM, Luther JS, Milne JS, Aitken RP, Redmer DA, Reynolds LP, Hay WW, Jr. Nutritional modulation of adolescent pregnancy outcome - a review Placenta 27 Suppl A: S61-S68, 2006.
50. Weibel ER. Point counting methods. J Microsc 95: 373-378, 1972.
51. Whitaker RC. Predicting preschooler obesity at birth: the role of maternal obesity in early pregnancy. Pediatrics 114: e29-e36, 2004.
52. Zhu MJ. Down-regulation of growth signaling pathways linked to a reduced cotyledonary vascularity in placentomes of over-nourished, obese pregnant ewes. Placenta 30: 405-410, 2009.
53. Zhu MJ, Du M, Hess BW, Nathanielsz PW, Ford SP. 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, 2007.
54. Zhu MJ, Han B, Tong J, Ma C, Kimzey JM, Underwood KR, Xiao Y, Hess BW, Ford SP, Nathanielsz PW, Du M. AMP-activated protein kinase signalling pathways are down regulated and skeletal muscle development impaired in fetuses of obese, over-nourished sheep. J Physiol 586: 2651-2664, 2008.