Retardation of fetal dendritic development induced by gestational hyperglycemia is associated with brain insulin/IGF-I signals

International Journal of Developmental Neuroscience

Volumn 37, Issue , 2014, Pages 15-20

  Jing, Yu Hong ^a   Song, Yan Feng ^a   Yao, Ya Ming ^a   Yin, Jie ^a   Wang, De gui ^a   Gao, Li Ping ^a  

^a LANZHOU UNIVERSITY   (China)

Author keywords

Dendritic spine; Fetal brain development; Gestational hyperglycemia; Insulin IGF I

Indexed keywords

INSULIN; INSULIN RECEPTOR; MESSENGER RNA; SODIUM CHLORIDE; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; STREPTOZOCIN; SYNAPTOPHYSIN; GLUCOSE BLOOD LEVEL;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN DEVELOPMENT; BRAIN LEVEL; CONTROLLED STUDY; DENDRITIC SPINE; DISEASE ASSOCIATION; EMBRYO DEVELOPMENT; FEMALE; FETUS; FETUS DEVELOPMENT; GESTATIONAL AGE; HYPERGLYCEMIA; INTRAUTERINE GROWTH RETARDATION; MALE; NONHUMAN; PLACENTAL TRANSFER; PREGNANCY COMPLICATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; AGE; ANIMAL; BRAIN; CHEMICALLY INDUCED; COMPLICATION; DENDRITE; DRUG EFFECTS; EMBRYOLOGY; FETAL GROWTH RETARDATION; FETOMATERNAL TRANSFUSION; GENETICS; GLUCOSE BLOOD LEVEL; METABOLISM; NERVE CELL; NONPARAMETRIC TEST; PATHOLOGY; PHYSIOLOGY; PREGNANCY; SILVER STAINING; TIME; ULTRASTRUCTURE; WISTAR RAT;

AGE FACTORS; ANIMALS; BLOOD GLUCOSE; BRAIN; DENDRITES; FEMALE; FETAL GROWTH RETARDATION; FETUS; HYPERGLYCEMIA; INSULIN; INSULIN-LIKE GROWTH FACTOR I; MALE; MATERNAL-FETAL EXCHANGE; NEURONS; PREGNANCY; RATS; RATS, WISTAR; RNA, MESSENGER; SIGNAL TRANSDUCTION; SILVER STAINING; STATISTICS, NONPARAMETRIC; STREPTOZOCIN; TIME FACTORS;

EID: 84903701413     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2014.06.004     Document Type: Article

References (46)

1. Brinciotti M., Napoli A., Mittica A., Bitterman O., Matricardi M. Cortical evoked potentials in children of diabetic mothers. Exp. Diabetes Res. 2011, 2011:640535.
2. Bruning J.C., Gautam D., Burks D.J., Gillette J., Schubert M., Orban P.C., Klein R., Krone W., Muller-Wieland D., Kahn C.R. Role of brain insulin receptor in control of body weight and reproduction. Science 2000, 289:2122-2125.
3. Camarero G., Avendano C., Fernandez-Moreno C., Villar A., Contreras J., de Pablo F., Pichel J.G., Varela-Nieto I. Delayed inner ear maturation and neuronal loss in postnatal Igf-1-deficient mice. J. Neurosci. 2001, 21:7630-7641.
4. Clausen T.D., Mortensen E.L., Schmidt L., Mathiesen E.R., Hansen T., Jensen D.M., Damm P. Cognitive function in adult offspring of women with gestational diabetes - the role of glucose and other factors. PLoS ONE 2013, 8:e67107.
5. Clausen T.D., Mortensen E.L., Schmidt L., Mathiesen E.R., Hansen T., Jensen D.M., Holm S., Poulsen L., From M., Damm P. Cognitive function in adult offspring of women with Type 1 diabetes. Diabet. Med. 2011, 28:838-844.
6. Coetzee E.J. Pregnancy and diabetes scenario around the world: Africa. Int. J. Gynaecol. Obstet. 2009, 104(Suppl. 1):S39-S41.
7. Cole G.M., Frautschy S.A. The role of insulin and neurotrophic factor signaling in brain aging and Alzheimer's Disease. Exp. Gerontol. 2007, 42:10-21.
8. D'Ercole A.J., Ye P., O'Kusky J.R. Mutant mouse models of insulin-like growth factor actions in the central nervous system. Neuropeptides 2002, 36:209-220.
9. Dabelea D., Snell-Bergeon J.K., Hartsfield C.L., Bischoff K.J., Hamman R.F., McDuffie R.S. Increasing prevalence of gestational diabetes mellitus (GDM) over time and by birth cohort: Kaiser Permanente of Colorado GDM Screening Program. Diabetes Care 2005, 28:579-584.
10. Damm P. Future risk of diabetes in mother and child after gestational diabetes mellitus. Int. J. Gynaecol. Obstet. 2009, 104(Suppl. 1):S25-S26.
11. Dionne G., Boivin M., Seguin J.R., Perusse D., Tremblay R.E. Gestational diabetes hinders language development in offspring. Pediatrics 2008, 122:e1073-e1079.
12. Dornhorst A., Paterson C.M., Nicholls J.S., Wadsworth J., Chiu D.C., Elkeles R.S., Johnston D.G., Beard R.W. High prevalence of gestational diabetes in women from ethnic minority groups. Diabet. Med. 1992, 9:820-825.
13. Entingh-Pearsall A., Kahn C.R. Differential roles of the insulin and insulin-like growth factor-I (IGF-I) receptors in response to insulin and IGF-I. J. Biol. Chem. 2004, 279:38016-38024.
14. Farquhar J.W. Diabetes and the fetus: questions which need answers. Can. Med. Assoc. J. 1971, 105:289-292.
15. Fernandes de Abreu D.A., Caballero A., Fardel P., Stroustrup N., Chen Z., Lee K., Keyes W.D., Nash Z.M., Lopez-Moyado I.F., Vaggi F., Cornils A., Regenass M., Neagu A., Ostojic I., Liu C., Cho Y., Sifoglu D., Shen Y., Fontana W., Lu H., Csikasz-Nagy A., Murphy C.T., Antebi A., Blanc E., Apfeld J., Zhang Y., Alcedo J., Ch'ng Q. An insulin-to-insulin regulatory network orchestrates phenotypic specificity in development and physiology. PLoS Genet. 2014, 10:e1004225.
16. Freude S., Leeser U., Muller M., Hettich M.M., Udelhoven M., Schilbach K., Tobe K., Kadowaki T., Kohler C., Schroder H., Krone W., Bruning J.C., Schubert M. IRS-2 branch of IGF-1 receptor signaling is essential for appropriate timing of myelination. J. Neurochem. 2008, 107:907-917.
17. Hansen-Pupp I., Hovel H., Lofqvist C., Hellstrom-Westas L., Fellman V., Huppi P.S., Hellstrom A., Ley D. Circulatory insulin-like growth factor-I and brain volumes in relation to neurodevelopmental outcome in very preterm infants. Pediatr. Res. 2013, 74:564-569.
18. Hartling L., Dryden D.M., Guthrie A., Muise M., Vandermeer B., Donovan L. Diagnostic thresholds for gestational diabetes and their impact on pregnancy outcomes: a systematic review. Diabet. Med. 2014, 31:319-331.
19. Hay W.W. Recent observations on the regulation of fetal metabolism by glucose. J. Physiol. 2006, 572:17-24.
20. Hodge R.D., D'Ercole A.J., O'Kusky J.R. Insulin-like growth factor-I (IGF-I) inhibits neuronal apoptosis in the developing cerebral cortex in vivo. Int. J. Dev. Neurosci. 2007, 25:233-241.
21. Jin Y.M., Zhao S.Z., Zhang Z.L., Chen Y., Cheng X., Chuai M., Liu G.S., Lee K.K., Yang X. High glucose level induces cardiovascular dysplasia during early embryo development. Exp. Clin. Endocrinol. Diabetes 2013, 121:448-454.
22. Karakash S.D., Einstein F.H. Diabetes in pregnancy: glycemia control guidelines and rationale. Curr. Opin. Endocrinol. Diabetes Obes. 2011, 18:99-103.
23. Kruse M.S., Barutta J., Vega M.C., Coirini H. Down regulation of the proliferation and apoptotic pathways in the embryonic brain of diabetic rats. Cell. Mol. Neurobiol. 2012, 32:1031-1037.
24. Lacroix M., Battista M.C., Doyon M., Menard J., Ardilouze J.L., Perron P., Hivert M.F. Lower adiponectin levels at first trimester of pregnancy are associated with increased insulin resistance and higher risk of developing gestational diabetes mellitus. Diabetes Care 2013, 36:1577-1583.
25. Le Roith D., Zick Y. Recent advances in our understanding of insulin action and insulin resistance. Diabetes Care 2001, 24:588-597.
26. Li Y., Komuro Y., Fahrion J.K., Hu T., Ohno N., Fenner K.B., Wooton J., Raoult E., Galas L., Vaudry D., Komuro H. Light stimuli control neuronal migration by altering of insulin-like growth factor 1 (IGF-1) signaling. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:2630-2635.
27. Liu D., Zhang H., Gu W., Liu Y., Zhang M. Neuroprotective effects of ginsenoside Rb1 on high glucose-induced neurotoxicity in primary cultured rat hippocampal neurons. PLoS ONE 2013, 8:e79399.
28. Luo S.J., Yang H.X. Roles of advanced glycation end products and its receptor on the fetal brain injury in pregnant rats with gestational diabetes mellitus. Zhonghua Fu Chan Ke Za Zhi 2012, 47:364-367.
29. Lupien S.B., Bluhm E.J., Ishii D.N. Systemic insulin-like growth factor-I administration prevents cognitive impairment in diabetic rats, and brain IGF regulates learning/memory in normal adult rats. J. Neurosci. Res. 2003, 74:512-523.
30. Ma R.C., Chan J.C. Pregnancy and diabetes scenario around the world: China. Int. J. Gynaecol. Obstet. 2009, 104(Suppl. 1):S42-S45.
31. Maric-Bilkan C., Symonds M., Ozanne S., Alexander B.T. Impact of maternal obesity and diabetes on long-term health of the offspring. Exp. Diabetes Res. 2011, 2011:163438.
32. Nold J.L., Georgieff M.K. Infants of diabetic mothers. Pediatr. Clin. North Am. 2004, 51:619-637. viii.
33. Park S., Kim da S., Kang S., Moon N.R. beta-Amyloid-induced cognitive dysfunction impairs glucose homeostasis by increasing insulin resistance and decreasing beta-cell mass in non-diabetic and diabetic rats. Metabolism 2013, 62:1749-1760.
34. Phelan S.A., Ito M., Loeken M.R. Neural tube defects in embryos of diabetic mice: role of the Pax-3 gene and apoptosis. Diabetes 1997, 46:1189-1197.
35. Plum L., Schubert M., Bruning J.C. The role of insulin receptor signaling in the brain. Trends Endocrinol. Metab. 2005, 16:59-65.
36. Rivera E.J., Goldin A., Fulmer N., Tavares R., Wands J.R., de la Monte S.M. Insulin and insulin-like growth factor expression and function deteriorate with progression of Alzheimer's disease: link to brain reductions in acetylcholine. J. Alzheimers Dis. 2005, 8:247-268.
37. Russo V.C., Gluckman P.D., Feldman E.L., Werther G.A. The insulin-like growth factor system and its pleiotropic functions in brain. Endocr. Rev. 2005, 26:916-943.
38. Schubert M., Gautam D., Surjo D., Ueki K., Baudler S., Schubert D., Kondo T., Alber J., Galldiks N., Kustermann E., Arndt S., Jacobs A.H., Krone W., Kahn C.R., Bruning J.C. Role for neuronal insulin resistance in neurodegenerative diseases. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:3100-3105.
39. Seshiah V., Balaji V., Balaji M.S., Paneerselvam A., Kapur A. Pregnancy and diabetes scenario around the world: India. Int. J. Gynaecol. Obstet. 2009, 104(Suppl. 1):S35-S38.
40. Stenninger E., Flink R., Eriksson B., Sahlen C. Long-term neurological dysfunction and neonatal hypoglycaemia after diabetic pregnancy. Arch. Dis. Child. Fetal Neonatal Ed. 1998, 79:F174-F179.
41. 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.
42. Walker S.P., Ugoni A.M., Lim R., Lappas M. Inverse relationship between gestational weight gain and glucose uptake in human placenta from female foetuses. Pediatr. Obes. 2013.
43. Werner H., Leroith D. Insulin and insulin-like growth factor receptors in the brain: physiological and pathological aspects. Eur. Neuropsychopharmacol. 2014.
44. Yessoufou A., Moutairou K. Maternal diabetes in pregnancy: early and long-term outcomes on the offspring and the concept of "metabolic memory". Exp. Diabetes Res. 2011, 2011:218598.
45. Zabihi S., Loeken M.R. Understanding diabetic teratogenesis: where are we now and where are we going?. Birth Defects Res. A: Clin. Mol. Teratol. 2010, 88:779-790.
46. Zhou Y., Luo Y., Dai J. Axonal and dendritic changes are associated with diabetic encephalopathy in rats: an important risk factor for Alzheimer's disease. J. Alzheimers Dis. 2013, 34:937-947.