Maternal obesity accelerates fetal pancreatic β-cell but not α-cell development in sheep: Prenatal consequences

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 297, Issue 3, 2009, Pages

  Ford, Stephen P ^a   Zhang, Liren ^a   Zhu, Meijun ^a   Miller, Myrna M ^a   Smith, Derek T ^a   Hess, Bret W ^a   Moss, Gary E ^a   Nathanielsz, Peter W ^a,b   Nijland, Mark J ^a,b  

^a UNIVERSITY OF WYOMING   (United States)

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

Author keywords

Fetal growth; Pancreatic function; Sheep

Indexed keywords

GLUCOSE; HYDROCORTISONE; INSULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CALORIC INTAKE; CONTROLLED STUDY; CROWN RUMP LENGTH; EWE; FEMALE; FETUS; FETUS DEVELOPMENT; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; HYDROCORTISONE BLOOD LEVEL; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; MALE; NONHUMAN; OBESITY; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; SHEEP;

ANIMALS; ANIMALS, NEWBORN; BLOOD GLUCOSE; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; FEMALE; FETAL DEVELOPMENT; FETUS; GESTATIONAL AGE; GLUCAGON-SECRETING CELLS; HYDROCORTISONE; INSULIN; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; MITOSIS; OBESITY; PANCREAS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SHEEP; UP-REGULATION;

EID: 69249110098     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00072.2009     Document Type: Article

References (46)

1. Aagaard-Tillery KM, Grove K, Bishop J, Ke X, Fu Q, McKnight R, Lane RH. Developmental origins of disease and determinants of chromatin structure: maternal diet modifies the primate fetal epigenome. J Mol Endocrinol 41: 91-102, 2004.
2. Aldoretta PW, Carver TD, Hay WW Jr. Maturation of glucose-stimulated insulin secretion in fetal sheep. Biol Neonate 73: 375-386, 1998.
3. +-ATPase. J Physiol 586: 5013-5022, 2008.
4. Armitage JA, Khan IY, Taylor PD, Nathanielsz PW, Poston L. 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, 2004.
5. Armitage JA, Taylor PD, Poston L. Experimental models of developmental programming: consequences of exposure to an energy rich diet during development. J Physiol 565: 3-8, 2005.
6. 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.
7. Breant B, Gesina E, Blondeau B. Nutrition, glucocorticoids and pancreas development. Horm Res 65, Suppl 3: 98-104, 2006.
8. Callaway LK, Prins JB, Chang AM, McIntyre HD. The prevalence and impact of overweight and obesity in an Australian obstetric population. Med J Aust 184: 56-59, 2006.
9. Carver TD, Anderson SM, Aldoretta PW, Hay WW Jr. Effect of low-level basal plus marked "pulsatile" hyperglycemia on insulin secretion in fetal sheep. Am J Physiol Endocrinol Metab 271: E865-E871, 1996.
10. Catalano PM, Thomas A, Huston-Presley L, Amini SB. Increased fetal adiposity: a very sensitive marker of abnormal in utero development. Am J Obstet Gynecol 189: 1698-1704, 2003.
11. Cripps RL, Martin-Gronert MS, Archer Zoe A, Hales CN, Mercer JG, Ozanne SE. Programming of hypothalamic neuropeptide gene expression in rats by maternal dietary protein content during pregnancy and lactation. Clin Sci (Lond) 117: 85-93, 2009.
12. Dahri S, Reusens B, Remacle C, Hoet JJ. Nutritional influences on pancreatic development and potential links with non-insulin-dependent diabetes (Abstract). Proc Nutr Soc 54: 345-356. 1995.
13. Fowden AL. Endocrine regulation of fetal growth. Reprod Fertil Dev 7: 351-363, 1995.
14. Fowden AL, Comline RS. The effects of pancreatectomy on the sheep fetus in utero. Q J Exp Physiol 69: 319-330, 1984.
15. Fowden AL, Forhead AJ. The role of hormones in intrauterine development. In: Fetal Origins Of Cardiovascular And Like Disease, edited by Barker DJP. New York: Decker, 2000, p. 199-228.
16. Fowden AL, Hill DJ. Intra-uterine programming of the endocrine pancreas. Br Med Bull 60: 123-142, 2001.
17. Fowden AL, Hughes P, Comline RS. The effects of insulin on the growth rate of the sheep fetus during late gestation. Q J Exp Physiol 74: 703-714, 1989.
18. Freinkel N. Banting Lecture 1980: Of pregnancy and progeny. Diabetes 29: 1023-1035, 1980.
19. Gluckman PD, Liggins GC. Regulation of fetal growth. In: Fetal Physiology and Medicine: The Basis of Perinatology, edited by Beard RW and Nathanielsz PW. London: Butterworth, 1984, p. 511-557.
20. Hales CN, Barker DJ. The thrifty phenotype hypothesis. Br Med Bull 60: 5-20, 2001.
21. Hennige AM, Fritsche A, Strack V, Weigert C, Mischak H, Borboni P, Renn W, Haring HU, Kellerer M. PKC zeta enhances insulin-like growth factor 1-dependent mitogenic activity in the rat clonal beta cell line RIN 1046-38. Biochem Biophys Res Commun 290: 85-90, 2002.
22. Hill DJ, Hogg J, Petrik J, Arany E, Han VK. Cellular distribution and ontogeny of insulin-like growth factors (IGFs) and IGF binding protein messenger RNAs and peptides in developing rat pancreas. J Endocrinol 160: 305-317, 1999.
23. Kervran A, Guillaume M, Jost A. The endocrine pancreas of the fetus from diabetic pregnant rat. Diabetologia 15: 387-393, 1978.
24. Limesand SW, Jensen J, Hutton JC, Hay WW Jr. Diminished β-cell replication contributes to reduced β-cell mass in fetal sheep with intrauterine growth restriction. Am J Physiol Regul Integr Comp Physiol 288: R1297-R1305, 2005.
25. Lobelo F. Fetal programming and risk of metabolic syndrome: prevention efforts for high-risk populations. Pediatrics 116: 519, 2005.
26. Manikkam M, Thompson RC, Herkimer C, Welch KB, Flak J, Karsch FJ, Padmanabhan V. Developmental programming: impact of prenatal testosterone excess on pre- and postnatal gonadotropin regulation in sheep. Biol Reprod 78: 648-660, 2008.
27. McDonald TJ, Nathanielsz PW. Bilateral destruction of the fetal paraventricular nuclei prolongs gestation in sheep. Am J Obstet Gynecol 1991: 764-771, 1991.
28. Mercier J, Pomar C, Marcoux M, Goulet F, Theriault M, Castonguay FW. The use of dual-energy X-ray absorptiometry to estimate the dissected composition of lamb carcasses. Meat Sci 73: 249-257, 2006.
29. Milner RDG. Endocrine control of fetal growth? In: Perinatal Nutrition, edited by Lindblad BS. London: Academic, 1988, p. 45-62.
30. Nathanielsz PW. Comparative studies on the initiation of labor. Eur J Obstet Gynaecol Reprod Biol 78: 127-132, 1998.
31. National Center for Health Statistics. Prevalence of overweight and obesity among adults: United States 1999-2002. (Online at http://www.cdc.gov/nchs/products/pubs/pubd/hestats/obese/obse99.htm), 2007.
32. National Research Council. Nutrient Requirements of Sheep. (6th Edition). Washington, DC: National Academy, 1985.
33. Nohr EA, Bech BH, Davies MJ, Frydenberg M, Henriksen TB, Olsen J. Prepregnancy obesity and fetal death: a study within the Danish National Birth Cohort. Obstet Gynecol 106: 250-259, 2005.
34. Pearce KL, Ferguson M, Gardner G, Smith N, Greef J, Pethick DW. Dual X-ray absorptiometry accurately predicts carcass composition from live sheep and chemical composition of live and dead sheep. Meat Sci 81: 285-293, 2009.
35. Pederson J. Weight and length at birth of infants of diabetic mothers. Acta Endocrinol 6: 330-342, 1954.
36. Pettitt DJ, Aleck KA, Baird HR, Carraher MJ, Bennett PH, Knowler WC. Congenital susceptibility to NIDDM. Role of intrauterine environment. Diabetes 37: 622-628, 199.
37. Reusens B, Remacle C. Programming of the endocrine pancreas by the early nutritional environment. Intl J Biochem Cell Biol 38: 913-922, 2006.
38. Rozance PJ, Limesand SW, Barry JS, Brown LD, Thorn SR, LoTurco D, Regnault TRH, Friedman JE, Hay WW Jr. Chronic late-gestation hypoglycemia upregulates hepatic PEPCK associated with increased PGC1α mRNA and phosphorylated CREB in fetal sheep. Am J Physiol Endocrinol Metab 294: E365-E370, 2008.
39. 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.
40. Snoeck A, Remacle C, Reusens B, Hoet JJ. Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate 57: 107-118, 1990.
41. Stanger BZ, Tanaka AJ, Melton DA. Organ size is limited by the number of embryonic progenitor cells in the pancreas but not the liver. Nature 445: 886-891, 2007.
42. Vonnahme KA, Hess BW, Hansen TR, McCormick RJ, Rule DC, Moss GE, Murdoch WJ, Nijland MJ, Skinner DC, Nathanielsz PW, Ford SP. Maternal undernutrition from early- to mid-gestation leads to growth retardation, cardiac ventricular hypertrophy, and increased liver weight in the fetal sheep. Biol Reprod 69: 133-140, 2003.
43. Wei JN, Sung FC, Li CY, Chang CH, Lin RS, Lin CC, Chiang CC, Chuang LM. Low birth weight and high birth weight infants are both at an increased risk to have type 2 diabetes among schoolchildren in Taiwan. Diabetes Care 26: 343-348, 2003.
44. 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 signaling pathways are down regulated and skeletal muscle development impaired in fetuses of obese, over-nourished sheep. J Physiol 586: 2651-2664, 2008.
45. Zhu MJ, Ford SP, Means WJ, Hess BW, Nathanielsz PW, Du M. Maternal nutrient restriction affects properties of skeletal muscle in offspring. J Physiol 575: 241-250, 2006.
46. Soto N, Bazaes RA, Pena V, Salazar T, Avila A, Iniguez G, Ong KK, Dunger DB, Mericq MV. Insulin sensitivity and secretion are related to catch-up growth in small-for-gestational-age infants at age 1 year: results from a prospective cohort. J Clin Endocrinol Metab 88: 3645-3650, 2003.