Advancements and challenges in generating accurate animal models of gestational diabetes mellitus

American Journal of Physiology - Endocrinology and Metabolism

Volumn 305, Issue 11, 2013, Pages

  Pasek, Raymond C ^b   Gannon, Maureen ^a,b,c  

^a Tennessee Valley Healthcare System   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

cell; Gestational diabetes mellitus; Glucosestimulated insulin secretion; Hyperplasia; Hypertrophy; Pregnancy

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; INSULIN; JANUS KINASE 2; LEPTIN RECEPTOR; METHIONINE; MIXED LINEAGE LEUKEMIA 2 PROTEIN; MIXED LINEAGE LEUKEMIA PROTEIN; NUCLEAR FACTOR; PROLACTIN RECEPTOR; PROTEIN BCL 6; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; SEROTONIN; SEROTONIN 2B RECEPTOR; SEROTONIN UPTAKE INHIBITOR; STAT5 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXD3; TRANSCRIPTION FACTOR FOXM1; TRYPTOPHAN HYDROXYLASE; TRYPTOPHAN HYDROXYLASE 2; UNCLASSIFIED DRUG;

ALLOXAN DIABETES MELLITUS; ANIMAL MODEL; BODY WEIGHT; CELL PROLIFERATION; DIABETOGENESIS; DISEASE MODEL; ENVIRONMENTAL FACTOR; ETHNICITY; FAMILY HISTORY; GENE INACTIVATION; GENE OVEREXPRESSION; GENETIC MANIPULATION; GENETIC MODEL; GENETIC SUSCEPTIBILITY; GLUCOSE HOMEOSTASIS; HEREDITY; HUMAN; HYPERGLYCEMIA; HYPOGLYCEMIA; INSULIN RELEASE; LIPID DIET; MACROSOMIA; NEONATAL RESPIRATORY DISTRESS SYNDROME; NEWBORN DISEASE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PANCREAS ISLET BETA CELL; PANCREAS RESECTION; PREGNANCY; PREGNANCY COMPLICATION; PREGNANCY DIABETES MELLITUS; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SEROTONIN RELEASE; STREPTOZOCIN DIABETES; TRANSGENE; WELLBEING;

Β-CELL; GESTATIONAL DIABETES MELLITUS; GLUCOSE-STIMULATED INSULIN SECRETION; HYPERPLASIA; HYPERTROPHY; PREGNANCY;

ADULT; ANIMAL EXPERIMENTATION; ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES, GESTATIONAL; FEMALE; HUMANS; PANCREATECTOMY; PREGNANCY; RODENTIA;

EID: 84888874213     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00425.2013     Document Type: Review

References (114)

1. Aerts L, Van Assche FA. Ultrastructural evaluation of B-cell recruitment in virgin and pregnant offspring of diabetic mothers. Diabetes Res Clin Pract 41: 9-14, 1998.
2. Arison RN, Ciaccio EI, Glitzer MS, Cassaro JA, Pruss MP. Light and electron microscopy of lesions in rats rendered diabetic with streptozotocin. Diabetes 16: 51-56, 1967.
3. Association AD. Gestational diabetes mellitus. Diabetes Care 27: s88-s90, 2004.
4. Brelje TC, Stout LE, Bhagroo NV, Sorenson RL. Distinctive roles for prolactin and growth hormone in the activation of signal transducer and activator of transcription 5 in pancreatic islets of langerhans. Endocrinology 145: 4162-4175, 2004.
5. Bruckmann G, Wertheimer E. Alloxan studies: the action of alloxan homologues and related compounds. J Biol Chem 168: 241-256, 1947.
6. Butler AE, Cao-Minh L, Galasso R, Rizza RA, Corradin A, Cobelli C, Butler PC. Adaptive changes in pancreatic beta cell fractional area and beta cell turnover in human pregnancy. Diabetologia 53: 2167-2176, 2010.
7. Cardinal JW, Allan DJ, Cameron DP. Differential metabolite accumulation may be the cause of strain differences in sensitivity to streptozotocin-induced beta cell death in inbred mice. Endocrinology 139: 2885-2891, 1998.
8. Carlson AJ, Drennan FM. The control of pancreatic diabetes in pregnancy by the passage of the internal secretion of the pancreas of the fetus to the blood of the mother. Am J Physiol 28: 391-395, 1911.
9. Chen H, Charlat O, Tartaglia LA, Woolf EA, Weng X, Ellis SJ, Lakey ND, Culpepper J, Moore KJ, Breitbart RE, Duyk GM, Tepper RI, Morgenstern JP. Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice. Cell 84: 491-495, 1996.
10. Cheung NW, Byth K. Population health significance of gestational diabetes. Diabetes care 26: 2005-2009, 2003.
11. Cohen G, Heikkila RE. The generation of hydrogen peroxide, superoxide radical, and hydroxyl radical by 6-hydroxydopamine, dialuric acid, and related cytotoxic agents. J Biol Chem 249: 2447-2452, 1974.
12. Cuthbert FP, Ivy AC, Isaacs BL, Gray J. The relation of pregnancy and lactation to the extirpation diabetes in the dog. Am J Physiol 115: 480-496, 1936.
13. Cypryk K, Szymczak W, Czupryniak L, Sobczak M, Lewinski A. Gestational diabetes mellitus-an analysis of risk factors. Endokrynol Pol 59: 393-397, 2008.
14. da Silva Xavier G, Mondragon A, Sun G, Chen L, McGinty JA, French PM, Rutter GA. Abnormal glucose tolerance and insulin secretion in pancreas-specific Tcf7l2-null mice. Diabetologia 55: 2667-2676, 2012.
15. Demirci C, Ernst S, Alvarez-Perez JC, Rosa T, Valle S, Shridhar V, Casinelli GP, Alonso LC, Vasavada RC, Garcia-Ocana A. Loss of HGF/c-Met signaling in pancreatic beta-cells leads to incomplete maternal beta-cell adaptation and gestational diabetes mellitus. Diabetes 61: 1143-1152, 2012.
16. Diamond MP, Moley KH, Pellicer A, Vaughn WK, DeCherney AH. Effects of streptozotocin-and alloxan-induced diabetes mellitus on mouse follicular and early embryo development. J Reprod Fertil 86: 1-10, 1989.
17. Dickinson JE, Meyer BA, Brath PC, Chmielowiec S, Walsh SW, Parisi VM, Palmer SM. Placental thromboxane and prostacyclin production in an ovine diabetic model. Am J Obstet Gynecol 163: 1831-1835, 1990.
18. Dickinson JE, Meyer BA, Chmielowiec S, Palmer SM. Streptozocininduced diabetes mellitus in the pregnant ewe. Am J Obstet Gynecol 165: 1673-1677, 1991.
19. Dooley SL, Metzger BE, Cho NH. Gestational diabetes-mellitus-influence of race on disease prevalence and perinatal outcome in a United-States population. Diabetes 40: 25-29, 1991.
20. Dunn JS, Sheehan HL, McLetchie NGB. Necrosis of islets of Langerhans produced experimentally. Lancet 241: 484-487, 1943.
21. Ezekwe MO, Ezekwe EI, Sen DK, Ogolla F. Effects of maternal streptozotocin-diabetes on fetal growth, energy reserves and body composition of newborn pigs. J Anim Sci 59: 974-980, 1984.
22. 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 sheep: prenatal consequences. Am J Physiol Regul Integr Comp Physiol 297: R835-R843, 2009.
23. Frias JL, Frias JP, Frias PA, Martinez-Frias ML. Infrequently studied congenital anomalies as clues to the diagnosis of maternal diabetes mellitus. Am J Med Genet A 143A: 2904-2909, 2007.
24. Fujinaka Y, Takane K, Yamashita H, Vasavada RC. Lactogens promote beta cell survival through JAK2/STAT5 activation and Bcl-XL upregulation. J Biol Chem 282: 30707-30717, 2007.
25. Gauguier D, Bihoreau MT, Ktorza A, Berthault MF, Picon L. Inheritance of diabetes mellitus as consequence of gestational hyperglycemia in rats. Diabetes 39: 734-739, 1990.
26. Gewolb IH, Barrett C, Wilson CM, Warshaw JB. Delay in pulmonary glycogen degradation in fetuses of streptozotocin diabetic rats. Pediatr Res 16: 869-873, 1982.
27. Giachini FR, Carriel V, Capelo LP, Tostes RC, Carvalho MH, Fortes ZB, Zorn TM, San Martin S. Maternal diabetes affects specific extracellular matrix components during placentation. J Anat 212: 31-41, 2008.
28. Gillman J, Gilbert C, Epstein E, Allan JC. Endocrine control of blood sugar, lipaemia, and ketonaemia in diabetic baboons. Br Med J 2: 1260-1263, 1958.
29. Gilmartin AB, Ural SH, Repke JT. Gestational diabetes mellitus. Rev Obstet Gynecol 1: 129-134, 2008.
30. Gloyn AL, Siddiqui J, Ellard S. Mutations in the genes encoding the pancreatic beta-cell KATP channel subunits Kir6.2 (KCNJ11) and SUR1 (ABCC8) in diabetes mellitus and hyperinsulinism. Hum Mutat 27: 220-231, 2006.
31. Gorus FK, Malaisse WJ, Pipeleers DG. Selective uptake of alloxan by pancreatic B-cells. Biochem J 208: 513-515, 1982.
32. Griffiths M. The mechanism of the hypoglycemic action of alloxan. Aust J Exp Biol Med Sci 26: 339-346, 1948.
33. Gupta RK, Gao N, Gorski RK, White P, Hardy OT, Rafiq K, Brestelli JE, Chen G, Stoeckert CJ Jr, Kaestner KH. Expansion of adult beta-cell mass in response to increased metabolic demand is dependent on HNF-4alpha. Genes Dev 21: 756-769, 2007.
34. Gupta RK, Vatamaniuk MZ, Lee CS, Flaschen RC, Fulmer JT, Matschinsky FM, Duncan SA, Kaestner KH. The MODY1 gene HNF-4alpha regulates selected genes involved in insulin secretion. J Clin Invest 115: 1006-1015, 2005.
35. Harder T, Franke K, Kohlhoff R, Plagemann A. Maternal and paternal family history of diabetes in women with gestational diabetes or insulindependent diabetes mellitus type I. Gynecol Obstet Invest 51: 160-164, 2001.
36. Higashide S, Inoue K, Minote H, Tobe T, Mori C, Shiota K. Expression of epidermal growth factor receptor after partial pancreatectomy in adult rats: an immunohistochemical study. Nihon Geka Hokan 61: 311-319, 1992.
37. Hoftiezer V, Carpenter AM. Comparison of streptozotocin and alloxaninduced diabetes in the rat, including volumetric quantitation of the pancreatic islets. Diabetologia 9: 178-184, 1973.
38. Holemans K, Caluwaerts S, Poston L, Van Assche FA. Diet-induced obesity in the rat: a model for gestational diabetes mellitus. Am J Obstet Gynecol 190: 858-865, 2004.
39. Huang C, Snider F, Cross JC. Prolactin receptor is required for normal glucose homeostasis and modulation of beta-cell mass during pregnancy. Endocrinology 150: 1618-1626, 2009.
40. Hummel KP, Dickie MM, Coleman DL. Diabetes, a new mutation in the mouse. Science 153: 1127-1128, 1966.
41. Jarrett IG, Potter BJ, Packham A. Effects of pancreatectomy in the sheep. Aust J Exp Biol Med Sci 34: 133-141, 1956.
42. Jawerbaum A, Catafau JR, Gonzales ET, Rodriguez RR, Gelpi E, Gomez G, Gimeno AL, Gimeno MA. Eicosanoid production by uterine strips and by embryos obtained from diabetic pregnant rats. Prostaglandins 45: 487-495, 1993.
43. Johansson M, Mattsson G, Andersson A, Jansson L, Carlsson PO. Islet endothelial cells and pancreatic beta-cell proliferation: studies in vitro and during pregnancy in adult rats. Endocrinology 147: 2315-2324, 2006.
44. Jones N, Harrison GA. Genetically determined obesity and sterility in the mouse. Proc Soc Study Fertil 9: 51-64, 1957.
45. Karnik SK, Chen H, McLean GW, Heit JJ, Gu X, Zhang AY, Fontaine M, Yen MH, Kim SK. Menin controls growth of pancreatic beta-cells in pregnant mice and promotes gestational diabetes mellitus. Science 318: 806-809, 2007.
46. Karnik SK, Hughes CM, Gu X, Rozenblatt-Rosen O, McLean GW, Xiong Y, Meyerson M, Kim SK. Menin regulates pancreatic islet growth by promoting histone methylation and expression of genes encoding p27Kip1 and p18INK4c. Proc Natl Acad Sci USA 102: 14659-14664, 2005.
47. Kato R, Onoda K, Takanaka A. Species difference in drug metabolism by liver microsomes in alloxan diabetic or fasted animals. II. The substrate interaction with cytochrome P-450 in drug oxidation. Jpn J Pharmacol 20: 554-561, 1970.
48. Kaufmann RC, Amankwah KS, Dunaway G, Maroun L, Arbuthnot J, Roddick JW Jr. An animal model of gestational diabetes. Am J Obstet Gynecol 141: 479-482, 1981.
49. Kelly PA, Bachelot A, Kedzia C, Hennighausen L, Ormandy CJ, Kopchick JJ, Binart N. The role of prolactin and growth hormone in mammary gland development. Mol Cell Endocrinol 197: 127-131, 2002.
50. Kemnitz JW, Eisele SG, Lindsay KA, Engle MJ, Perelman RH, Farrell PM. Changes in food intake during menstrual cycles and pregnancy of normal and diabetic rhesus monkeys. Diabetologia 26: 60-64, 1984.
51. Kilpatrick DC. Mannan-binding lectin: clinical significance and applications. Biochim Biophys Acta 1572: 401-413, 2002.
52. Kim H, Toyofuku Y, Lynn FC, Chak E, Uchida T, Mizukami H, Fujitani Y, Kawamori R, Miyatsuka T, Kosaka Y, Yang K, Honig G, van der Hart M, Kishimoto N, Wang J, Yagihashi S, Tecott LH, Watada H, German MS. Serotonin regulates pancreatic beta cell mass during pregnancy. Nat Med 16: 804-808, 2010.
53. Kim SY, England L, Sappenfield W, Wilson HG, Bish CL, Salihu HM, Sharma AJ. Racial/ethnic differences in the percentage of gestational diabetes mellitus cases attributable to overweight and obesity, Florida, 2004-2007. Prev Chronic Dis 9: E88, 2012.
54. Kivimaki M, Hamer M, Batty GD, Geddes JR, Tabak AG, Pentti J, Virtanen M, Vahtera J. Antidepressant medication use, weight gain, and risk of type 2 diabetes: a population-based study. Diabetes Care 33: 2611-2616, 2010.
55. Kobayashi K, Kobayashi N, Okitsu T, Yong C, Fukazawa T, Ikeda H, Kosaka Y, Narushima M, Arata T, Tanaka N. Development of a porcine model of type 1 diabetes by total pancreatectomy and establishment of a glucose tolerance evaluation method. Artif Organs 28: 1035-1042, 2004.
56. Le TN, Elsea SH, Romero R, Chaiworapongsa T, Francis GL. Prolactin receptor gene polymorphisms are associated with gestational diabetes. Genet Test Mol Biomarkers 17: 567-571, 2013.
57. Lenich CM, Chobanian AV, Brecher P, Zannis VI. Effect of dietary cholesterol and alloxan-diabetes on tissue cholesterol and apolipoprotein E mRNA levels in the rabbit. J Lipid Res 32: 431-438, 1991.
58. Lenzen S, Panten U. Alloxan: history and mechanism of action. Diabetologia 31: 337-342, 1988.
59. Liang C, DeCourcy K, Prater MR. High-saturated-fat diet induces gestational diabetes and placental vasculopathy in C57BL/6 mice. Metabolism 59: 943-950, 2010.
60. Long H, Cundy T. Establishing consensus in the diagnosis of gestational diabetes following HAPO: where do we stand? Curr Diabetes Reports 13: 43-50, 2013.
61. Lopez-Soldado I, Herrera E. Different diabetogenic response to moderate doses of streptozotocin in pregnant rats, and its long-term consequences in the offspring. Exp Diabes Res 4: 107-118, 2003.
62. Markowitz J, Soskin S. Pancreatic diabetes and pregnancy. Am J Physiol 79: 553-558, 1927.
63. Martin ME, Garcia AM, Blanco L, Herrera E, Salinas M. Effect of streptozotocin diabetes on polysomal aggregation and protein synthesis rate in the liver of pregnant rats and their offspring. Biosci Rep 15: 15-20, 1995.
64. Megia A, Gallart L, Fernandez-Real JM, Vendrell J, Simon I, Gutierrez C, Richart C. Mannose-binding lectin gene polymorphisms are associated with gestational diabetes mellitus. J Clin Endocrinol Metab 89: 5081-5087, 2004.
65. Metzger BE, Coustan DR. Summary and recommendations of the Fourth International Workshop-Conference on Gestational Diabetes Mellitus. The Organizing Committee. Diabetes Care 21, Suppl 2: B161-B167, 1998.
66. Metzger BE, Gabbe SG, Persson B, Buchanan TA, Catalano PA, Damm P, Dyer AR, Leiva A, Hod M, Kitzmiler JL, Lowe LP, McIntyre HD, Oats JJ, Omori Y, Schmidt MI. International association of diabetes and pregnancy study groups recommendations on the diagnosis and classification of hyperglycemia in pregnancy. Diabetes Care 33: 676-682, 2010.
67. Miodovnik M, Mimouni F, Berk M, Clark KE. Alloxan-induced diabetes mellitus in the pregnant ewe: metabolic and cardiovascular effects on the mother and her fetus. Am J Obstet Gynecol 160: 1239-1244, 1989.
68. Miura A, Yamagata K, Kakei M, Hatakeyama H, Takahashi N, Fukui K, Nammo T, Yoneda K, Inoue Y, Sladek FM, Magnuson MA, Kasai H, Miyagawa J, Gonzalez FJ, Shimomura I. Hepatocyte nuclear factor-4alpha is essential for glucose-stimulated insulin secretion by pancreatic beta-cells. J Biol Chem 281: 5246-5257, 2006.
69. Moehn S, Pencharz PB, Ball RO. Lessons learned regarding symptoms of tryptophan deficiency and excess from animal requirement studies. J Nutr 142: 2231S-2235S, 2012.
70. Moore MC, Menon R, Coate KC, Gannon M, Smith MS, Farmer B, Williams PE. Diet-induced impaired glucose tolerance and gestational diabetes in the dog. J Appl Physiol 110: 458-467, 2011.
71. Morisset J, Morisset S, Lauzon K, Cote S, Laine J, Bourassa J, Lessard M, Echave V. Pancreatic inflammation, apoptosis, and growth: sequential events after partial pancreatectomy in pigs. Pancreas 21: 321-324, 2000.
72. Murata M, Takahashi A, Saito I, Kawanishi S. Site-specific DNA methylation and apoptosis: induction by diabetogenic streptozotocin. Biochem Pharmacol 57: 881-887, 1999.
73. Nebigil CG, Choi DS, Dierich A, Hickel P, Le Meur M, Messaddeq N, Launay JM, Maroteaux L. Serotonin 2B receptor is required for heart development. Proc Natl Acad Sci USA 97: 9508-9513, 2000.
74. O'Sullivan JB, Mahan CM, Charles D, Dandrow RV. Screening criteria for high-risk gestational diabetic patients. Am J Obstet Gynecol 116: 895-900, 1973.
75. Pan A, Sun Q, Okereke OI, Rexrode KM, Rubin RR, Lucas M, Willett WC, Manson JE, Hu FB. Use of antidepressant medication and risk of type 2 diabetes: results from three cohorts of US adults. Diabetologia 55: 63-72, 2012.
76. Pang K, Mukonoweshuro C, Wong GG. Beta cells arise from glucose transporter type 2 (Glut2)-expressing epithelial cells of the developing rat pancreas. Proc Natl Acad Sci USA 91: 9559-9563, 1994.
77. Parsons JA, Bartke A, Sorenson RL. Number and size of islets of Langerhans in pregnant, human growth hormone-expressing transgenic, and pituitary dwarf mice: effect of lactogenic hormones. Endocrinology 136: 2013-2021, 1995.
78. Parsons JA, Brelje TC, Sorenson RL. Adaptation of islets of Langerhans to pregnancy: increased islet cell proliferation and insulin secretion correlates with the onset of placental lactogen secretion. Endocrinology 130: 1459-1466, 1992.
79. Perera HK, Caldwell ME, Hayes-Patterson D, Teng L, Peshavaria M, Jetton TL, Labosky PA. Expression and shifting subcellular localization of the transcription factor, Foxd3, in embryonic and adult pancreas. Gene Expr Patterns 6: 971-977, 2006.
80. Perkins JM, Dunn JP, Jagasia SM. Perspectives in gestational diabetes mellitus: a review of screening, diagnosis, and treatment. Clin Diabetes 25: 57-62, 2007.
81. Phelps RL, Metzger BE, Freinkel N. Carbohydrate metabolism in pregnancy. XVII. Diurnal profiles of plasma glucose, insulin, free fatty acids, triglycerides, cholesterol, and individual amino acids in late normal pregnancy. Am J Obstet Gynecol 140: 730-736, 1981.
82. Plank JL, Frist AY, LeGrone AW, Magnuson MA, Labosky PA. Loss of Foxd3 results in decreased beta-cell proliferation and glucose intolerance during pregnancy. Endocrinology 152: 4589-4600, 2011.
83. Ramsay TG, Wolverton CK, Steele NC. Alteration in IGF-I mRNA content of fetal swine tissues in response to maternal diabetes. Am J Physiol Regul Integr Comp Physiol 267: R1391-R1396, 1994.
84. Reynolds WA, Chez RA, Bhuyan BK, Neil GL. Placental transfer of streptozotocin in the rhesus monkey. Diabetes 23: 777-782, 1974.
85. Rieck S, Kaestner KH. Expansion of beta-cell mass in response to pregnancy. Trends Endocrinol Metab 21: 151-158, 2010.
86. Robitaille J, Grant AM. The genetics of gestational diabetes mellitus: evidence for relationship with type 2 diabetes mellitus. Genet Med 10: 240-250, 2008.
87. Rossini AA, Williams RM, Appel MC, Like AA. Sex differences in the multiple-dose streptozotocin model of diabetes. Endocrinology 103: 1518-1520, 1978.
88. Ryan EA, Tobin BW, Tang J, Finegood DT. A new model for the study of mild diabetes during pregnancy. Syngeneic islet-transplanted STZinduced diabetic rats. Diabetes 42: 316-323, 1993.
89. Savitz DA, Janevic TM, Engel SM, Kaufman JS, Herring AH. Ethnicity and gestational diabetes in New York City, 1995-2003. Br J Obstet Gynaecol 115: 969-978, 2008.
90. Schein PS, Loftus S. Streptozotocin: depression of mouse liver pyridine nucleotides. Cancer Res 28: 1501-1506, 1968.
91. Schein PS, O'Connell MJ, Blom J, Hubbard S, Magrath IT, Bergevin P, Wiernik PH, Ziegler JL, DeVita VT. Clinical antitumor activity and toxicity of streptozotocin (NSC-85998). Cancer 34: 993-1000, 1974.
92. Schnedl WJ, Ferber S, Johnson JH, Newgard CB. STZ transport and cytotoxicity. Specific enhancement in GLUT2-expressing cells. Diabetes 43: 1326-1333, 1994.
93. Schraenen A, Lemaire K, de Faudeur G, Hendrickx N, Granvik M, Van Lommel L, Mallet J, Vodjdani G, Gilon P, Binart N, in't Veld P, Schuit F. Placental lactogens induce serotonin biosynthesis in a subset of mouse beta cells during pregnancy. Diabetologia 53: 2589-2599, 2010.
94. Segar EM, Norris AW, Yao JR, Hu S, Koppenhafer SL, Roghair RD, Segar JL, Scholz TD. Programming of growth, insulin resistance and vascular dysfunction in offspring of late gestation diabetic rats. Clin Sci (Lond) 117: 129-138, 2009.
95. Shaat N, Ekelund M, Lernmark A, Ivarsson S, Almgren P, Berntorp K, Groop L. Association of the E23K polymorphism in the KCNJ11 gene with gestational diabetes mellitus. Diabetologia 48: 2544-2551, 2005.
96. Shaat N, Karlsson E, Lernmark A, Ivarsson S, Lynch K, Parikh H, Almgren P, Berntorp K, Groop L. Common variants in MODY genes increase the risk of gestational diabetes mellitus. Diabetologia 49: 1545-1551, 2006.
97. Shaat N, Lernmark A, Karlsson E, Ivarsson S, Parikh H, Berntorp K, Groop L. A variant in the transcription factor 7-like 2 (TCF7L2) gene is associated with an increased risk of gestational diabetes mellitus. Diabetologia 50: 972-979, 2007.
98. Sharma A, Zangen DH, Reitz P, Taneja M, Lissauer ME, Miller CP, Weir GC, Habener JF, Bonner-Weir S. The homeodomain protein IDX-1 increases after an early burst of proliferation during pancreatic regeneration. Diabetes 48: 507-513, 1999.
99. Sivan E, Boden G. Free fatty acids, insulin resistance, and pregnancy. Curr Diabetes Reports 3: 319-322, 2003.
100. Szkudelski T. The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiol Res 50: 537-546, 2001.
101. Tein MS, Breen SA, Loveday BE, Devlin H, Balment RJ, Boyd RD, Sibley CP, Garland HO. Bone mineral density and composition in rat pregnancy: effects of streptozotocin-induced diabetes mellitus and insulin replacement. Exp Physiol 83: 165-174, 1998.
102. Tsai MY, Schallinger LE, Josephson MW, Brown DM. Disturbance of pulmonary prostaglandin metabolism in fetuses of alloxan-diabetic rabbits. Biochim Biophys Acta 712: 395-399, 1982.
103. Van Assche FA, Aerts L, De Prins F. A morphological study of the endocrine pancreas in human pregnancy. Br J Obstet Gynaecol 85: 818-820, 1978.
104. Vercheval M, De Hertogh R, Pampfer S, Vanderheyden I, Michiels B, De Bernardi P, De Meyer R. Experimental diabetes impairs rat embryo development during the preimplantation period. Diabetologia 33: 187-191, 1990.
105. Waguri M, Yamamoto K, Miyagawa JI, Tochino Y, Yamamori K, Kajimoto Y, Nakajima H, Watada H, Yoshiuchi I, Itoh N, Imagawa A, Namba M, Kuwajima M, Yamasaki Y, Hanafusa T, Matsuzawa Y. Demonstration of two different processes of beta-cell regeneration in a new diabetic mouse model induced by selective perfusion of alloxan. Diabetes 46: 1281-1290, 1997.
106. Wang RN, Bouwens L, Kloppel G. Beta-cell growth in adolescent and adult rats treated with streptozotocin during the neonatal period. Diabetologia 39: 548-557, 1996.
107. Watanabe RM, Allayee H, Xiang AH, Trigo E, Hartiala J, Lawrence JM, Buchanan TA. Transcription factor 7-like 2 (TCF7L2) is associated with gestational diabetes mellitus and interacts with adiposity to alter insulin secretion in Mexican Americans. Diabetes 56: 1481-1485, 2007.
108. Weinhaus AJ, Stout LE, Bhagroo NV, Brelje TC, Sorenson RL. Regulation of glucokinase in pancreatic islets by prolactin: a mechanism for increasing glucose-stimulated insulin secretion during pregnancy. J Endocrinol 193: 367-381, 2007.
109. Yamagata K, Furuta H, Oda N, Kaisaki PJ, Menzel S, Cox NJ, Fajans SS, Signorini S, Stoffel M, Bell GI. Mutations in the hepatocyte nuclear factor-4alpha gene in maturity-onset diabetes of the young (MODY1). Nature 384: 458-460, 1996.
110. Yamashita H, Shao J, Ishizuka T, Klepcyk PJ, Muhlenkamp P, Qiao L, Hoggard N, Friedman JE. Leptin administration prevents spontaneous gestational diabetes in heterozygous Lepr(db/+) mice: effects on placental leptin and fetal growth. Endocrinology 142: 2888-2897, 2001.
111. Yamashita H, Shao J, Qiao L, Pagliassotti M, Friedman JE. Effect of spontaneous gestational diabetes on fetal and postnatal hepatic insulin resistance in Lepr(db/+) mice. Pediatr Res 53: 411-418, 2003.
112. Zabihi S, Wentzel P, Eriksson UJ. Maternal blood glucose levels determine the severity of diabetic embryopathy in mice with different expression of copper-zinc superoxide dismutase (CuZnSOD). Toxicol Sci 105: 166-172, 2008.
113. Zhang H, Ackermann AM, Gusarova GA, Lowe D, Feng X, Kopsombut UG, Costa RH, Gannon M. The FoxM1 transcription factor is required to maintain pancreatic beta-cell mass. Mol Endocrinol 20: 1853-1866, 2006.
114. Zhang H, Zhang J, Pope CF, Crawford LA, Vasavada RC, Jagasia SM, Gannon M. Gestational diabetes mellitus resulting from impaired beta-cell compensation in the absence of FoxM1, a novel downstream effector of placental lactogen. Diabetes 59: 143-152, 2010.