Glucose homeostasis in prediabetic NOD and lymphocyte-deficient NODscid mice during gestation

Review of Diabetic Studies

Volumn 7, Issue 1, 2010, Pages 36-44

  Coulaud, J ^a   Durant, S ^b   Homo Delarche, Françoise ^a  

^a Groupe Hospitalier Pitié Salpêtrière   (France)

^b INSERM   (France)

Author keywords

Corticosterone; Gestation; Glucagon; Insulin resistance; Islet neogenesis; Macrophage; NOD mouse; NODscid mice; T1D; Type 1 diabetes

Indexed keywords

CORTICOSTERONE; GLUCAGON; GLUCOSE; INSULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD GLUCOSE MONITORING; CELL ACTIVITY; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DISEASE ACTIVITY; DRUG EFFECT; FEMALE; GLUCAGON BLOOD LEVEL; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE TEST; INSULIN BLOOD LEVEL; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RESISTANCE; MATING; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; PANCREAS ISLET BETA CELL; PREGNANCY; PREVALENCE; PUERPERIUM; SCID MOUSE; ANIMAL; BLOOD; C57BL MOUSE; CHEMISTRY; HOMEOSTASIS; IMMUNOLOGY; IMPAIRED GLUCOSE TOLERANCE; LYMPHOCYTE; MOUSE MUTANT; PANCREAS; PANCREAS ISLET; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY DIABETES MELLITUS;

ANIMALS; BLOOD GLUCOSE; CORTICOSTERONE; DIABETES MELLITUS, TYPE 1; FEMALE; GLUCAGON; GLUCOSE TOLERANCE TEST; HOMEOSTASIS; INSULIN; INSULIN RESISTANCE; ISLETS OF LANGERHANS; LYMPHOCYTES; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, SCID; PANCREAS; PREDIABETIC STATE; PREGNANCY; PREGNANCY IN DIABETICS;

EID: 77953300820     PISSN: 16136071     EISSN: 16140575     Source Type: Journal    
DOI: 10.1900/RDS.2010.7.36     Document Type: Article

References (68)

1. Homo-Delarche F. Neuroendocrine immuno-ontogeny of the pathogenesis of autoimmune disease in the nonobese diabetic (NOD) mouse. Ilar J 2004. 45:237-258.
2. Amrani A, Durant S, Throsby M, Coulaud J, Dardenne M, Homo-Delarche F. Glucose homeostasis in the nonobese diabetic mouse at the prediabetic stage. Endocrinology 1998. 139:1115-1124.
3. Rosmalen JG, Leenen PJ, Pelegri C, Drexhage HA, Homo-Delarche F. Islet abnormalities in the pathogenesis of autoimmune diabetes. Trends Endocrinol Metab 2002. 13:209-214.
4. Homo-Delarche F, Boitard C. Autoimmune diabetes: the role of the islets of Langerhans. Immunol Today 1996. 17:456-460.
5. Pelegri C, Rosmalen JG, Durant S, Throsby M, Alves V, Coulaud J, Esling A, Pleau JM, Drexhage HA, Homo-Delarche F. Islet endocrine-cell behavior from birth onward in mice with the nonobese diabetic genetic background. Mol Med 2001. 7:311-319. (Pubitemid 33701981)
6. Charre S, Rosmalen JG, Pelegri C, Alves V, Leenen PJ, Drexhage HA, Homo-Delarche F. Abnormalities in dendritic cell and macrophage accumulation in the pancreas of nonobese diabetic (NOD) mice during the early neonatal period. Histol Histopathol 2002. 17:393-401. (Pubitemid 34411197)
7. Throsby M, Coulaud J, Durant S, Homo-Delarche F. Increased transcriptional preproinsulin II beta-cell activity in neonatal nonobese diabetic mice: in situ hybridization analysis. Rev Diabet Stud 2005. 2:75-83.
8. Melnik BC. Permanent impairment of insulin resistance from pregnancy to adulthood: the primary basic risk factor of chronic Western diseases. Med Hypotheses 2009. 73:670-681.
9. Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 2008. 359:61-73.
10. Le Clair C, Abbi T, Sandhu H, Tappia PS. Impact of maternal undernutrition on diabetes and cardiovascular disease risk in adult offspring. Can J Physiol Pharmacol 2009. 87:161-179.
11. Palinski W, Nicolaides E, Liguori A, Napoli C. Influence of Maternal Dysmetabolic Conditions During Pregnancy on Cardiovascular Disease. J Cardiovasc Transl Res 2009. 2:277-285.
12. Amrani A, Chaouloff F, Mormede P, Dardenne M, Homo-Delarche F. Glucose, insulin, and open field responses to immobilization in nonobese diabetic (NOD) mice. Physiol Behav 1994. 56:241-246.
13. Rosmalen JG, Pigmans MJ, Kersseboom R, Drexhage HA, Leenen PJ, Homo-Delarche F. Sex steroids influence pancreatic islet hypertrophy and subsequent autoimmune infiltration in nonobese diabetic (NOD) and NODscid mice. Lab Invest 2001. 81:231-239. (Pubitemid 32176387)
14. Leturque A, Burnol AF, Ferre P, Girard J. Pregnancy-induced insulin resistance in the rat: assessment by glucose clamp technique. Am J Physiol 1984. 246:E25-31.
15. Nolan CJ, Proietto J. The feto-placental glucose steal phenomenon is a major cause of maternal metabolic adaptation during late pregnancy in the rat. Diabetologia 1994. 37:976-984.
16. Nieuwenhuizen AG, Schuiling GA, Moes H, Koiter TR. Role of increased insulin demand in the adaptation of the endocrine pancreas to pregnancy. Acta Physiol Scand 1997. 159:303-312. (Pubitemid 27193338)
17. Lauenborg J, Hansen T, Jensen DM, Vestergaard H, Molsted-Pedersen L, Hornnes P, Locht H, Pedersen O, Damm P. Increasing incidence of diabetes after gestational diabetes: a long-term follow-up in a Danish population. Diabetes Care 2004. 27:1194-1199.
18. Smirnakis KV, Martinez A, Blatman KH, Wolf M, Ecker JL, Thadhani R. Early pregnancy insulin resistance and subsequent gestational diabetes mellitus. Diabetes Care 2005. 28:1207-1208.
19. Aerts L, Holemans K, Van Assche FA. Maternal diabetes during pregnancy: consequences for the offspring. Diabetes Metab Rev 1990. 6:147-167.
20. Tamas G, Kerenyi Z. Gestational diabetes: current aspects on pathogenesis and treatment. Exp Clin Endocrinol Diabetes 2001. 109 Suppl 2:S400-411.
21. Boloker J, Gertz SJ, Simmons RA. Gestational diabetes leads to the development of diabetes in adulthood in the rat. Diabetes 2002. 51:1499-1506. (Pubitemid 34826617)
22. Aaen K, Rygaard J, Josefsen K, Petersen H, Brogren CH, Horn T, Buschard K. Dependence of antigen expression on functional state of beta-cells. Diabetes 1990. 39:697-701. (Pubitemid 20218968)
23. Buschard K. The functional state of the beta cells in the pathogenesis of insulin-dependent diabetes mellitus. Autoimmunity 1991. 10:65-69.
24. Bjork E, Kampe O, Karlsson FA, Pipeleers DG, Andersson A, Hellerstrom C, Eizirik DL. Glucose regulation of the autoantigen GAD65 in human pancreatic islets. J Clin Endocrinol Metab 1992. 75:1574-1576.
25. Leslie RD, Taylor R, Pozzilli P. The role of insulin resistance in the natural history of type 1 diabetes. Diabet Med 1997. 14:327-331.
26. Wilkin TJ. The accelerator hypothesis: weight gain as the missing link between Type I and Type II diabetes. Diabetologia 2001. 44:914-922.
27. Greenbaum CJ. Insulin resistance in type 1 diabetes. Diabetes Metab Res Rev 2002. 18:192-200.
28. Fourlanos S, Narendran P, Byrnes GB, Colman PG, Harrison LC. Insulin resistance is a risk factor for progression to type 1 diabetes. Diabetologia 2004. 47:1661-1667.
29. Tsai EB, Sherry NA, Palmer JP, Herold KC. The rise and fall of insulin secretion in type 1 diabetes mellitus. Diabetologia 2006. 49:261-270.
30. Xu P, Cuthbertson D, Greenbaum C, Palmer JP, Krischer JP. Role of insulin resistance in predicting progression to type 1 diabetes. Diabetes Care 2007. 30:2314-2320.
31. O'Reilly LA, Gu D, Sarvetnick N, Edlund H, Phillips JM, Fulford T, Cooke A. alpha-Cell neogenesis in an animal model of IDDM. Diabetes 1997. 46:599-606. (Pubitemid 27143375)
32. Suarez-Pinzon WL, Power RF, Yan Y, Wasserfall C, Atkinson M, Rabinovitch A. Combination therapy with glucagon-like peptide-1 and gastrin restores normoglycemia in diabetic NOD mice. Diabetes 2008. 57:3281-3288.
33. Hornnes PJ. On the decrease of glucose tolerance in pregnancy. A review. Diabete Metab 1985. 11:310-315. (Pubitemid 16194169)
34. Beis C, Grigorakis SI, Philippou G, Alevizaki M, Anastasiou E. Lack of suppression of plasma glucagon levels in late pregnancy persists postpartum only in women with previous gestational diabetes mellitus. Acta Diabetol 2005. 42:31-35.
35. Greenbaum CJ, Havel PJ, Taborsky GJ, Jr., Klaff LJ. Intra-islet insulin permits glucose to directly suppress pancreatic A cell function. J Clin Invest 1991. 88:767-773.
36. Dumonteil E, Magnan C, Ritz-Laser B, Meda P, Dussoix P, Gilbert M, Ktorza A, Philippe J. Insulin, but not glucose lowering corrects the hyperglucagonemia and increased proglucagon messenger ribonucleic acid levels observed in insulinopenic diabetes. Endocrinology 1998. 139:4540-4546.
37. Kaneko K, Shirotani T, Araki E, Matsumoto K, Taguchi T, Motoshima H, Yoshizato K, Kishikawa H, Shichiri M. Insulin inhibits glucagon secretion by the activation of PI3-kinase in In-R1-G9 cells. Diabetes Res Clin Pract 1999. 44:83-92.
38. Laube H, Fussganger RD, Maier V, Pfeiffer EF. Hyperglucagonemia of the isolated perfused pancreas of diabetic mice (db-db). Diabetologia 1973. 9:400-402.
39. Leiter EH, Coleman DL, Eppig JJ. Endocrine pancreatic cells of postnatal "diabetes" (db) mice in cell culture. In Vitro 1979. 15:507-521.
40. Vecchio D, Luyckx A, Zahnd GR, Renold AE. Insulin release induced by glucagon in organ cultures of fetal rat pancreas. Metabolism 1966. 15:577-581.
41. Kawai K, Yokota C, Ohashi S, Watanabe Y, Yamashita K. Evidence that glucagon stimulates insulin secretion through its own receptor in rats. Diabetologia 1995. 38:274-276.
42. Heindorff H, Almdal T, Vilstrup H. The in vivo effect of interleukin-1 beta on urea synthesis is mediated by glucocorticoids in rats. Eur J Clin Invest 1994. 24:388-392. (Pubitemid 2091427)
43. Wogensen LD, Kolb-Bachofen V, Christensen P, Dinarello CA, Mandrup-Poulsen T, Martin S, Nerup J. Functional and morphological effects of interleukin-1 beta on the perfused rat pancreas. Diabetologia 1990. 33:15-23.
44. Zumsteg U, Reimers JI, Pociot F, Morch L, Helqvist S, Brendel M, Alejandro R, Mandrup-Poulsen T, Dinarello CA, Nerup J. Differential interleukin-1 receptor antagonism on pancreatic beta and alpha cells. Studies in rodent and human islets and in normal rats. Diabetologia 1993. 36:759-766. (Pubitemid 23218645)
45. Ellingsgaard H, Ehses JA, Hammar EB, Van Lommel L, Quintens R, Martens G, Kerr-Conte J, Pattou F, Berney T, Pipeleers D, Halban PA, Schuit FC, Donath MY. Interleukin-6 regulates pancreatic alpha-cell mass expansion. Proc Natl Acad Sci U S A 2008. 105:13163-13168.
46. Mendelson CR. Minireview: fetal-maternal hormonal signaling in pregnancy and labor. Mol Endocrinol 2009. 23:947-954.
47. Saravia-Fernandez F, Faveeuw C, Blasquez-Bulant C, Tappaz M, Throsby M, Pelletier G, Vaudry H, Dardenne M, Homo-Delarche F. Localization of gamma-aminobutyric acid and glutamic acid decarboxylase in the pancreas of the nonobese diabetic mouse. Endocrinology 1996. 137:3497-3506. (Pubitemid 26250204)
48. Saravia F, Homo-Delarche F. Is innervation an early target in autoimmune diabetes? Trends Immunol 2003. 24:574-579.
49. Winer S, Tsui H, Lau A, Song A, Li X, Cheung RK, Sampson A, Afifiyan F, Elford A, Jackowski G, Becker DJ, Santamaria P, Ohashi P, Dosch HM. Autoimmune islet destruction in spontaneous type 1 diabetes is not beta-cell exclusive. Nat Med 2003. 9:198-205.
50. Lindsay JR, Nieman LK. The hypothalamic-pituitary-adrenal axis in pregnancy: challenges in disease detection and treatment. Endocr Rev 2005. 26:775-799.
51. Mastorakos G, Ilias I. Maternal and fetal hypothalamic-pituitary-adrenal axes during pregnancy and postpartum. Ann N Y Acad Sci 2003. 997:136-149.
52. Thompson A, Arany EJ, Hill DJ, Yang K. Glucocorticoid receptor expression is altered in pancreatic beta cells of the non-obese diabetic mouse during postnatal development. Metabolism 2002. 51:765-768.
53. Harizi H, Homo-Delarche F, Amrani A, Coulaud J, Mormede P. Marked genetic differences in the regulation of blood glucose under immune and restraint stress in mice reveals a wide range of corticosensitivity. J Neuroimmunol 2007. 189:59-68.
54. Beauquis J, Homo-Delarche F, Giroix MH, Ehses J, Coulaud J, Roig P, Portha B, De Nicola AF, Saravia F. Hippocampal neurovascular and hypothalamic-pituitary-adrenal axis alterations in spontaneously type 2 diabetic GK rats. Exp Neurol 2008. 222:125-134.
55. Gaillard RC, Daneva T, Hadid R, Muller K, Spinedi E. The hypothalamo-pituitary-adrenal axis of athymic Swiss nude mice. The implications of T lymphocytes in the ACTH release from immune cells. Ann N Y Acad Sci 1998. 840:480-490. (Pubitemid 128714712)
56. Atkinson MA, Leiter EH. The NOD mouse model of type 1 diabetes: as good as it gets? Nat Med 1999. 5:601-604.
57. Zeidler A, Tosco C, Kumar D, Slavin B, Parker J. Spontaneous hyperglycemia and impaired glucose tolerance in athymic nude BALB/c mice. Diabetes 1982. 31:821-825. (Pubitemid 12062873)
58. Zeidler A, Shargill NS, Chan TM. Peripheral insulin insensitivity in the hyperglycemic athymic nude mouse: similarity to noninsulin-dependent diabetes mellitus. Proc Soc Exp Biol Med 1991. 196:457-460.
59. Feuerer M, Herrero L, Cipolletta D, Naaz A, Wong J, Nayer A, Lee J, Goldfine AB, Benoist C, Shoelson S, Mathis D. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat Med 2009. 15:930-939.
60. Winer S, Chan Y, Paltser G, Truong D, Tsui H, Bahrami J, Dorfman R, Wang Y, Zielenski J, Mastronardi F, Maezawa Y, Drucker DJ, Engleman E, Winer D, Dosch HM. Normalization of obesity-associated insulin resistance through immunotherapy. Nat Med 2009. 15:921-929.
61. Chaparro RJ, Konigshofer Y, Beilhack GF, Shizuru JA, McDevitt HO, Chien YH. Nonobese diabetic mice express aspects of both type 1 and type 2 diabetes. Proc Natl Acad Sci U S A 2006. 103:12475-12480.
62. Kagohashi Y, Udagawa J, Abiru N, Kobayashi M, Moriyama K, Otani H. Maternal factors in a model of type 1 diabetes differentially affect the development of insulitis and overt diabetes in offspring. Diabetes 2005. 54:2026-2031.
63. Wilson SS, DeLuca D. NOD fetal thymus organ culture: an in vitro model for the development of T cells involved in IDDM. J Autoimmun 1997. 10:461-472.
64. Geutskens SB, Homo-Delarche F, Pleau JM, Durant S, Drexhage HA, Savino W. Extracellular matrix distribution and islet morphology in the early postnatal pancreas: anomalies in the non-obese diabetic mouse. Cell Tissue Res 2004. 318:579-589.
65. Senecat O, Martignat L, Elmansour A, Charbonnel B, Sai P. Diabetes enhancement and increased islet antigen expression following neonatal injections of glucose and arginine in non-obese diabetic mice. Metabolism 1994. 43:1410-1418.
66. Saravia-Fernandez F, Durant S, el Hasnaoui A, Dardenne M, Homo-Delarche F. Environmental and experimental procedures leading to variations in the incidence of diabetes in the nonobese diabetic (NOD) mouse. Autoimmunity 1996. 24:113-121.
67. Dahlquist G, Kallen B. Early neonatal events and the disease incidence in nonobese diabetic mice. Pediatr Res 1997. 42:489-491. (Pubitemid 27411155)
68. Washburn LR, Dang H, Tian J, Kaufman DL. The postnatal maternal environment influences diabetes development in nonobese diabetic mice. J Autoimmun 2007. 28:19-23.