Animal models for small for gestational age and fetal programing of adult disease

Hormone Research

Volumn 68, Issue 3, 2007, Pages 113-123

  Vuguin, Patricia M ^a,b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b CHILDREN S HOSPITAL AT MONTEFIORE   (United States)

Author keywords

Animal models; Caloric restriction; Intrauterine growth restriction; Protein restriction; Small for gestational age; Uterine ligation

Indexed keywords

GLUCOCORTICOID;

ADULT DISEASE; ANATOMY; ARTERY LIGATION; ARTIFICIAL EMBOLISM; CALORIC RESTRICTION; EMBRYOLOGY; ENDOCRINE SYSTEM; FETUS DEVELOPMENT; FETUS GROWTH; GENETICS; HYPOXIA; INTRAUTERINE GROWTH RETARDATION; IRON DEFICIENCY; LIGATION; MAMMAL; MATERNAL DIABETES MELLITUS; NONHUMAN; NUTRITION; OVERNUTRITION; PATHOPHYSIOLOGY; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN RESTRICTION; SHORT SURVEY; SMALL FOR DATE INFANT; STRESS; UMBILICAL ARTERY; UTERUS;

ANIMALS; ANOXIA; CALORIC RESTRICTION; CARDIOVASCULAR DISEASES; DISEASE MODELS, ANIMAL; FEMALE; FETAL GROWTH RETARDATION; GLUCOCORTICOIDS; GUINEA PIGS; HUMANS; INFANT, NEWBORN; INFANT, SMALL FOR GESTATIONAL AGE; KIDNEY DISEASES; LIGATION; MICE; PREGNANCY; PREGNANCY IN DIABETICS; PROTEIN DEFICIENCY; RATS; SHEEP; STRESS; SWINE; UTERUS;

EID: 34547865037     PISSN: 03010163     EISSN: None     Source Type: Journal    
DOI: 10.1159/000100545     Document Type: Short Survey

References (124)

1. Ludwig DS, Ebbeling CB: Type 2 diabetes mellitus in children: primary care and public health considerations. JAMA 2001;286:1427-1430.
2. Bertram C, Hanson MA: Animals models and programming of the metabolic syndrome. Br Med Bull 2001;60:103-121.
3. Ozanne SE: Metabolic programming in animals. Br Med Bull 2001;60:143-152.
4. Vuguin P: Animals models for assessing the consequences of intrauterine growth retardation on subsequent glucose metabolism of the offspring: a review. J Matern Fetal Neonatal Med 2002;254-257.
5. Gluckman PD, Cutfield W, Hofman P, Hanson MA: The fetal, neonatal, and infant environments-the long-term consequences for disease risk. Early Hum Dev 2005;81:51-59.
6. Gluckman PD, Hanson MA: Maternal constraint of fetal growth and its consequences. Semin Fetal Neonatal Med 2004;9:419-425.
7. Hales CN, Ozanne SE: For debate: fetal and early postnatal growth restriction lead to diabetes, the metabolic syndrome and renal failure. Diabetologia 2003;46:1013-1019.
8. Hales CN: Early programming of glucose metabolism, insulin action and longevity. Adv Exp Med Biol 2000;478:57-64.
9. Hales C, Barker D, Clark P, Cox L, Fall C, Osmond C: Fetal and infant growth and impaired glucose tolerance at age 64 years. Br Med 1991;303:1019-1022.
10. Rich-Edwards J, Colditz G, Stampfer M, et al: Birthweight and the risk for type 2 diabetes mellitus in adult women. Ann Intern Med 1999;130:278-284.
11. Drake AJ, Walker BR: The intergenerational effects of fetal programming: non-genomic mechanisms for the inheritance of low birth weight and cardiovascular risk. J Endocrinol 2004;180:1-16.
12. Lucas A, Morley R: Birthweight ratio. Arch Dis Child 1991;66:1099.
13. Singhal A, Lucas A: Early origins of cardiovascular disease: is there a unifying hypothesis? Lancet 2004;363:1642-1645.
14. Singhal A, Cole TJ, Lucas A: Early nutrition in preterm infants and later blood pressure: two cohorts after randomised trials. Lancet 2001;357:413-419.
15. Singhal A, Cole TJ, Fewtrell M, Lucas A: Breastmilk feeding and lipoprotein profile in adolescents born preterm: follow-up of a prospective randomised study. Lancet 2004;363:1571-1578.
16. Srinivasan M, Laychock SG, Hill D, Patel M: Neonatal nutrition: metabolic programming of pancreatic islets and obesity. Exp Biol Med 2003;228:15-23.
17. Beierle EA, Chen MK, Hartwich JE, et al: Artificial rearing of mouse pups: development of a mouse pup in a cup model. Pediatr Res 2004;56:250-255.
18. Singhal A, Fewtrell M, Cole TJ, Lucas A: Low nutrient intake and early growth for later insulin resistance in adolescents born preterm. Lancet 2003;361:1089-1097.
19. Petry CJ, Ozanne SE, Hales CN: Programming of intermediary metabolism. Mol Cell Endocrinol 2001;185:81-91.
20. Wigglesworth JS: Experimental growth retardation in the foetal rat. J Pathol Bacteriol 1964;88:1-13.
21. Younoszai MK, Peloso J, Haworth JC: Fetal growth retardation in rats exposed to cigarette smoke during pregnancy. Am J Obstet Gynecol 1969;104:1207-1213.
22. Hill DE, Myers RE, Holt AB, Scott RE, Cheek DB: Fetal growth retardation produced by experimental placental insufficiency in the rhesus monkey. II. Chemical composition of the brain, liver, muscle and carcass. Biol Neonate 1971;19:68-82.
23. Anthony RV, Scheaffer AN, Wright CD, Regnault TR: Ruminant models of prenatal growth restriction. Reprod Suppl 2003;61:183-194.
24. Villar J, Belizan JM: The timing factor in the pathophysiology of the intrauterine growth retardation syndrome. Obstet Gynecol Surv 1982;37:499-506.
25. Ergaz Z, Avgil M, Ornoy A: Intrauterine growth restriction-etiology and consequences: what do we know about the human situation and experimental animal models? Reprod Toxicol 2005;20:301-322.
26. Gardner JD, Brower GL, Janicki JS: Effects of dietary phytoestrogens on cardiac remodeling secondary to chronic volume overload in female rats. J Appl Physiol 2005;99:1378-1383.
27. Mahn K, Borras C, Knock GA, et al: Dietary soy isoflavone induced increases in antioxidant and eNOS gene expression lead to improved endothelial function and reduced blood pressure in vivo. FASEB J 2005;19:1755-1757.
28. Garofano A, Czernichow P, Breant B: In utero undernutrition impairs rat beta-cell development. Diabetologia 1997;40:1231-1234.
29. Garofano A, Czernichow P, Breant B: Postnatal somatic growth and insulin contents in moderate or severe intrauterine growth retardation in the rat. Biol Neonate 1998;73:89-98.
30. Garofano A, Czernichow P, Breant B: Age-dependent inability of the endocrine pancreas to adapt to pregnancy: a long-term consequence of perinatal malnutrition in the rat. Endocrinology 1999;140:4208-4213.
31. Jimenez-Chillaron JC, Hernandez-Valencia M, Reamer C, et al: Beta-cell secretory dysfunction in the pathogenesis of low birth weight-associated diabetes: a murine model. Diabetes 2005;54:702-711.
32. Ozaki T, Nishina H, Hanson MA, Poston L: Dietary restriction in pregnant rats causes gender-related hypertension and vascular dysfunction in offspring. J Physiol 2001;530:141-152.
33. Vickers MH, Breier BH, Cutfield WS, Hofman PL, Gluckman PD: Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab 2000;279:E83-E87.
34. Han HC, Austin KJ, Nathanielsz PW, Ford SP, Nijland MJ, Hansen TR: Maternal nutrient restriction alters gene expression in the ovine fetal heart. J Physiol 2004;558:111-121.
35. Vonnahme KA, Hess BW, Hansen TR, et al: Maternal undernutrition from early- to midgestation leads to growth retardation, cardiac ventricular hypertrophy, and increased liver weight in the fetal sheep. Biol Reprod 2003;69:133-140.
36. Edwards LJ, McMillen IC: Periconceptional nutrition programs development of the cardiovascular system in the fetal sheep. Am J Physiol Regul Integr Comp Physiol 2002;283:R669-R679.
37. Hawkins P, Steyn C, McGarrigle HH, et al: Cardiovascular and hypothalamic-pituitary-adrenal axis development in late gestation fetal sheep and young lambs following modest maternal nutrient restriction in early gestation. Reprod Fertil Dev 2000;12:443-456.
38. Ozaki T, Hawkins P, Nishina H, Steyn C, Poston L, Hanson MA: Effects of undernutrition in early pregnancy on systemic small artery function in late-gestation fetal sheep. Am J Obstet Gynecol 2000;183:1301-1307.
39. Kind KL, Clifton PM, Grant PA, et al: Effect of maternal feed restriction during pregnancy on glucose tolerance in the adult guinea pig. Am J Physiol Regul Integr Comp Physiol 2003;284:R140-R152.
40. Snoeck A, Remacle C, Reusens B, Hoet J: Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate 1990;57:107-118.
41. Munoz G, Bongiorni-Malave I: Influence of dietary protein restriction on ovulation, fertilization rates and pre-implantation embryonic development in mice. J Exp Zool 1979;210:253-257.
42. Young M, Widdowson EM: The influence of diets deficient in energy, or in protein, on conceptus weight, and the placental transfer of a non-metabolisable amino acid in the guinea pig. Biol Neonate 1975;27:184-191.
43. Fernandez-Twinn DS, Ozanne SE, Ekizoglou S, et al: The maternal endocrine environment in the low-protein model of intrauterine growth restriction. Br J Nutr 2003;90:815-822.
44. Langley SC, Jackson AA: Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low protein diets. Clin Sci (Lond) 1994;86:217-222; discussion 121.
45. Nishina H, Green LR, McGarrigle HH, Noakes DE, Poston L, Hanson MA: Effect of nutritional restriction in early pregnancy on isolated femoral artery function in mid-gestation fetal sheep. J Physiol 2003;553:637-647.
46. Lucas A, Baker BA, Desai M, Hales CN: Nutrition in pregnant or lactating rats programs lipid metabolism in the offspring. Br J Nutr 1996;76:605-612.
47. Ozanne SE, Wang CL, Dorling MW, Petry CJ: Dissection of the metabolic actions of insulin in adipocytes from early growth-retarded male rats. J Endocrinol 1998;162:313-319.
48. Jackson AA, Dunn RL, Marchand MC, Langley-Evans SC: Increased systolic blood pressure in rats induced by a maternal lowprotein diet is reversed by dietary supplementation with glycine. Clin Sci (Lond) 2002;103:633-639.
49. Brawley L, Torrens C, Anthony FW, et al: Glycine rectifies vascular dysfunction induced by dietary protein imbalance during pregnancy. J Physiol 2004;554:497-504.
50. Contreras RJ, Wong DL, Henderson R, Curtis KS, Smith JC: High dietary NaCl early in development enhances mean arterial pressure of adult rats. Physiol Behav 2000;71:173-181.
51. Scholl TO, Hediger ML: Anemia and iron-deficiency anemia: compilation of data on pregnancy outcome. Am J Clin Nutr 1994;59:492S-500S; discussion 500S-501S.
52. Gambling L, Andersen HS, Czopek A, Wojciak R, Krejpcio Z, McArdle HJ: Effect of timing of iron supplementation on maternal and neonatal growth and iron status of iron-deficient pregnant rats. J Physiol 2004;561:195-203.
53. McCance DR, Pettitt DJ, Hanson RL, Jacobsson LT, Knowler WC, Bennett PH: Birth weight and non-insulin dependent diabetes: thrifty genotype, thrifty phenotype, or surviving small baby genotype? BMJ 1994;308:942-945.
54. Ray JG, Vermeulen MJ, Shapiro JL, Kenshole AB: Maternal and neonatal outcomes in pregestational and gestational diabetes mellitus, and the influence of maternal obesity and weight gain: the DEPOSIT study. Diabetes Endocrine Pregnancy Outcome Study in Toronto. QJM 2001;94:347-356.
55. Kirchengast S, Hartmann B, Schweppe KW, Husslein P: Impact of maternal body build characteristics on newborn size in two different European populations. Hum Biol 1998;70:761-774.
56. Wallace JM, Luther JS, Milne JS, et al: Nutritional modulation of adolescent pregnancy outcome - a review. Placenta 2006;27(suppl A):S61-S68.
57. Simmons R, Gounis A, Bangalore S, Ogata E: Intrauterine growth retardation: Fetal glucose transport is diminished in lung but spared in brain. Pediatr Res 1991;31:59-63.
58. Ogata E, Bussey M, Finley S: Altered gas exchange, limited glucose, branched chain amino acids, and hypoinsulinism retard fetal growth in the rat. Metabolism 1986;35:970-977.
59. Vuguin P, Raab E, Liu B, Barzilai N, Simmons R: Hepatic insulin resistance precedes the development of diabetes in a model of intrauterine growth retardation. Diabetes 2004;53:2617-2622.
60. Aalinkeel R, Srinivasan M, Kalhan SC, Laychock SG, Patel MS: A dietary intervention (high carbohydrate) during the neonatal period causes islet dysfunction in rats. Am J Physiol 1999;277:E1061-E1069.
61. Duncan JR, Cock ML, Loeliger M, Louey S, Harding R, Rees SM: Effects of exposure to chronic placental insufficiency on the postnatal brain and retina in sheep. J Neuropathol Exp Neurol 2004;63:1131-1143.
62. Louey S, Cock ML, Stevenson KM, Harding R: Placental insufficiency and fetal growth restriction lead to postnatal hypotension and altered postnatal growth in sheep. Pediatr Res 2000;48:808-814.
63. Creasy RK, Barrett CT, de Swiet M, Kahanpaa KV, Rudolph AM: Experimental intrauterine growth retardation in the sheep. Am J Obstet Gynecol 1972;112:566-573.
64. Gagnon R, Challis J, Johnston L, Fraher Fetal endocrine responses to chronic placental embolization in the late-gestation ovine fetus. Am J Obstet Gynecol 1994;170:929-938.
65. Trudinger BJ, Stevens D, Connelly A, et al: Umbilical artery flow velocity waveforms and placental resistance: the effects of embolization of the umbilical circulation. Am Obstet Gynecol 1987;157:1443-1448.
66. Charlton V, Johengen M: Fetal intravenous nutritional supplementation ameliorates the development of embolization-induced growth retardation in sheep. Pediatr Res 1987;22:55-61.
67. Jones CT, Gu W, Harding JE, Price DA, Parer JT: Studies on the growth of the fetal sheep. Effects of surgical reduction in placental size, or experimental manipulation of uterine blood flow on plasma sulphation promoting activity and on the concentration insulin-like growth factors I and II. J Dev Physiol 1988;10:179-189.
68. Robinson JS, Kingston EJ, Jones CT, Thorburn GD: Studies on experimental growth retardation in sheep. The effect of removal a endometrial caruncles on fetal size and metabolism. J Dev Physiol 1979;1:379-398.
69. Butler TG, Schwartz J, McMillen IC: Differential effects of the early and late intrauterine environment on corticotrophic cell development. J Clin Invest 2002;110:783-791.
70. Supramaniam VG, Jenkin G, Loose J, Wallace EM, Miller SL: Chronic fetal hypoxia increases activin A concentrations in the latepregnant sheep. BJOG 2006;113:102-109.
71. Lafeber HN, Rolph TP, Jones CT: Studies on the growth of the fetal guinea pig. The effects of ligation of the uterine artery on organ growth and development. J Dev Physiol 1984;6:441-459.
72. Jones CT, Lafeber HN, Roebuck MM: Studies on the growth of the fetal guinea pig. Changes in plasma hormone concentration during normal and abnormal growth. J Dev Physiol 1984;6:461-472.
73. Carter AM, Kingston MJ, Han KK, Mazzuca DM, Nygard K, Han VK: Altered expression of IGFs and IGF-binding proteins during intrauterine growth restriction in guinea pigs. J Endocrinol 2005;184:179-189.
74. Huang ST, Vo KC, Lyell DJ, et al: Developmental response to hypoxia. FASEB J 2004;18:1348-1365.
75. Tapanainen PJ, Bang P, Wilson K, Unterman TG, Vreman HJ, Rosenfeld RG: Maternal hypoxia as a model for intrauterine growth retardation: effects on insulin-like growth factors and their binding proteins. Pediatr Res 1994;36:152-158.
76. Nyirenda MJ, Lindsay RS, Kenyon CJ, Burchell A, Seckl JR: Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. J Clin Invest 1998;101:2174-2181.
77. Newnham JP, Moss TJ: Antenatal glucocorticoids and growth: single versus multiple doses in animal and human studies. Semin Neonatol 2001;6:285-292.
78. Newnham JP: Is prenatal glucocorticoid administration another origin of adult disease? Clin Exp Pharmacol Physiol 2001;28:957-961.
79. Moss TJ, Sloboda DM, Gurrin LC, Harding R, Challis JR, Newnham JP: Programming effects in sheep of prenatal growth restriction and glucocorticoid exposure. Am J Physiol Regul Integr Comp Physiol 2001;281:R960-R970.
80. Johnson JW, Mitzner W, London WT, Palmer AE, Scott R: Betamethasone and the rhesus fetus: multisystemic effects. Am J Obstet Gynecol 1979;133:677-684.
81. Reinisch JM, Simon NG, Karow WG, Gandelman R: Prenatal exposure to prednisone in humans and animals retards intrauterine growth. Science 1978;202:436-438.
82. Collaborative Group on Antenatal Steroid Therapy: Effects of antenatal dexamethasone administration in the infant: long-term follow-up. J Pediatr 1984;104:259-267.
83. Bloom SL, Sheffield JS, McIntire DD, Leveno KJ: Antenatal dexamethasone and decreased birth weight. Obstet Gynecol 2001;97:485-490.
84. French NP, Hagan R, Evans SF, Godfrey M, Newnham JP: Repeated antenatal corticosteroids: size at birth and subsequent development. Am J Obstet Gynecol 1999;180:114-121.
85. Rodriguez-Pinilla E, Prieto-Merino D, Dequino G, Mejias C, Fernandez P, Maryinez-Frias M; Grupo del ECEMC: Antenatal exposure to corticosteroids for fetal lung maturation and its repercussion on weight, length and head circumference in the newborn infant (Spanish). Med Clin 2006;127:361-367.
86. Murphy DJ, Caukwell S, Joels LA, Wardle P: Cohort study of the neonatal outcome of twin pregnancies that were treated with prophylactic or rescue antenatal corticosteroids. Am J Obstet Gynecol 2002;187:483-488.
87. Abbasi S, Hirsch D, Davis J, et al: Effect of single versus multiple courses of antenatal corticosteroids on maternal and neonatal outcome. Am J Obstet Gynecol 2000;182:1243-1249.
88. Pratt L, Magness RR, Phernetton T, Hendricks SK, Abbott DH, Bird IM: Repeated use of betamethasone in rabbits: effects of treatment variation on adrenal suppression, pulmonary maturation, and pregnancy outcome. Am J Obstet Gynecol 1999;180:995-1005.
89. Dodic M, McAlinden AT, Jefferies AJ, et al: Differential effects of prenatal exposure to dexamethasone or cortisol on circulatory control mechanisms mediated by angiotensin II in the central nervous system of adult sheep. J Physiol 2006;571:651-660.
90. McArthur S, Siddique ZL, Christian HC, et al: Perinatal glucocorticoid treatment disrupts the hypothalamo-lactotroph axis in adult female, but not male, rats. Endocrinology 2006;147:1904-1915.
91. Jobe AH, Newnham JP, Moss TJ, Ikegami M: Differential effects of maternal betamethasone and cortisol on lung maturation and growth in fetal sheep. Am J Obstet Gynecol 2003;188:22-28.
92. Moritz KM, Boon WM, Wintour EM: Glucocorticoid programming of adult disease. Cell Tissue Res 2005;322:81-88.
93. Dodic M, Hantzis V, Duncan J, et al: Programming effects of short prenatal exposure to cortisol. FASEB J 2002;16:1017-1026.
94. Dodic M, Abouantoun T, O'Connor A, Wintour EM, Moritz KM: Programming effects of short prenatal exposure to dexamethasone in sheep. Hypertension 2002;40:729-734.
95. Dodic M, May CN, Wintour EM, Coghlan JP: An early prenatal exposure to excess glucocorticoid leads to hypertensive offspring in sheep. Clin Sci (Lond) 1998;94:149-155.
96. Ortiz LA, Quan A, Zarzar F, Weinberg A, Baum M: Prenatal dexamethasone programs hypertension and renal injury in the rat. Hypertension 2003;41:328-334.
97. McDonald TJ, Franko KL, Brown JM, Jenkins SL, Nathanielsz PW, Nijland MJ: Betamethasone in the last week of pregnancy causes fetal growth retardation but not adult hypertension in rats. J Soc Gynecol Investig 2003;10:469-473.
98. Piffer RC, Pereira OC: Reproductive aspects in female rats exposed prenatally to hydrocortisone. Comp Biochem Physiol C Toxicol Pharmacol 2004;139:11-16.
99. Manikkam M, Crespi EJ, Doop DD, et al: Fetal programming: prenatal testosterone excess leads to fetal growth retardation and postnatal catch-up growth in sheep. Endocrinology 2004;145:790-798.
100. Canavan JP, Goldspink DF: Maternal diabetes in rats. II. Effects on fetal growth and protein turnover. Diabetes 1988;37:1671-1677.
101. Eriksson UJ, Lewis NJ, Freinkel N: Growth retardation during early organogenesis in embryos of experimentally diabetic rats. Diabetes 1984;33:281-284.
102. Eriksson UJ, Jansson L: Diabetes in pregnancy: decreased placental blood flow and disturbed fetal development in the rat. Pediatr Res 1984;18:735-738.
103. Eriksson UJ: Diabetes in pregnancy: retarded fetal growth, congenital malformations and feto-maternal concentrations of zinc, copper and manganese in the rat. J Nutr 1984;114:477-484.
104. Holemans K, Aerts L, Van Assche FA: Fetal growth restriction and consequences for the offspring in animal models. J Soc Gynecol Investig 2003;10:392-399.
105. Lesage J, Del-Favero F, Leonhardt M, et al: Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat. J Endocrinol 2004;181:291-296.
106. Thureen PJ, Trembler KA, Meschia G, Makowski EL, Wilkening RB: Placental glucose transport in heat-induced fetal growth retardation. Am J Physiol 1992;263:R578-R585.
107. Rasco JF, Hood RD: Differential effect of restraint procedure on incidence of restraint-stress-induced rib fusion in CD-1 mice. Toxicol Lett 1994;71:177-182.
108. Rasco JF, Hood RD: Effects of maternal restraint stress and sodium arsenate in mice. Reprod Toxicol 1994;8:49-54.
109. Ponnappa BC, Rubin E: Modeling alcohol's effects on organs in animal models. Alcohol Res Health 2000;24:93-104.
110. Nitzan M, Orloff S, Chrzanowska BL, Schulman JD: Intrauterine growth retardation in renal insufficiency: an experimental model in the rat. Am J Obstet Gynecol 1979;133:40-43.
111. Ishimoto H, Natori M, Tanaka M, Miyazaki T, Kobayashi T, Yoshimura Y: Role of oxygen-derived free radicals in free growth retardation induced by ischemia-reperfusion in rats. Am J Physiol 1997;272:H701-H705.
112. Pickard MR, Leonard AJ, Ogilvie LM, et al: Maternal hypothyroidism in the rat influences placental and liver glycogen stores: fetal growth retardation near term is unrelated to maternal and placental glucose metabolic compromise. J Endocrinol 2003;176:247-255.
113. Li RY, Tsutsui Y: Growth retardation and microcephaly induced in mice by placental infection with murine cytomegalovirus. Teratology 2000;62:79-85.
114. 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 1989;74:703-714.
115. Hensen K, Braem C, Declercq J, et al: Targeted disruption of the murine Plag1 protooncogene causes growth retardation and reduced fertility. Dev Growth Differ 2004;46:459-470.
116. Tamemoto H, Kadowaki T, Tobe K, et al: Insulin resistance and growth retardation in mice lacking insulin receptor substrate-1. Nature 1994;372:182-186.
117. Sibley CP, Turner MA, Cetin I, et al: Placental phenotypes of intrauterine growth. Pediatr Res 2005;58:827-832.
118. Vuguin PM, Kedees MH, Cui L, et al: Ablation of the glucagon receptor gene increases fetal lethality, and produces alterations in islet development and maturation. Endocrinology 2006;147:3995-4006.
119. Ivanova M, Dobrzycka KM, Jiang S, et al: Scaffold attachment factor B1 functions in development, growth, and reproduction. Mol Cell Biol 2005;25:2995-3006.
120. Collins LL, Lee YF, Heinlein CA, et al: Growth retardation and abnormal maternal behavior in mice lacking testicular orphan nuclear receptor 4. Proc Natl Acad Sci USA 2004;101:15058-15063.
121. Hansen TV, Hammer NA, Nielsen J, et al: Dwarfism and impaired gut development in insulin-like growth factor II mRNA-binding protein 1-deficient mice. Mol Cell Biol 2004;24:4448-4464.
122. Lupu F, Terwilliger JD, Lee K, Segre GV, Efstratiadis A: Roles of growth hormone and insulin-like growth factor 1 in mouse postnatal growth. Dev Biol 2001;229:141-162.
123. Nakae J, Kido Y, Accili D: Distinct and overlapping functions of insulin and IGF-I receptors. Endocr Rev 2001;22:818-835.
124. Crossey PA, Pillai CC, Miell JP: Altered placental development and intrauterine growth restriction in IGF binding protein-1 transgenic mice. J Clin Invest 2002;110:411-418.