Catalase prevents maternal diabetes-induced perinatal programming via the Nrf2-HO-1 defense system

Diabetes

Volumn 61, Issue 10, 2012, Pages 2565-2574

  Chang, Shiao Ying ^a   Chen, Yun Wen ^a   Zhao, Xin Ping ^a   Chenier, Isabelle ^a   Tran, Stella ^a   Sauvé, Alexandre ^a   Ingelfinger, Julie R ^b   Zhang, Shao Ling ^a  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; GREEN FLUORESCENT PROTEIN; HEME OXYGENASE 1; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; FEMALE; GENE ACTIVITY; GENE EXPRESSION; GLOMERULUS FILTRATION; HYPERTENSION; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CELL; KIDNEY DISEASE; KIDNEY INJURY; KIDNEY PROXIMAL TUBULE; MALE; MATERNAL DIABETES MELLITUS; MOUSE; NONHUMAN; PERINATAL DEVELOPMENT; PRENATAL PERIOD; PRIORITY JOURNAL; PROGENY; SYSTOLIC BLOOD PRESSURE;

ANIMALS; CATALASE; DIABETES MELLITUS, EXPERIMENTAL; FEMALE; HEME OXYGENASE-1; HYPERTENSION; KIDNEY DISEASES; MALE; MICE; MICE, TRANSGENIC; NF-E2-RELATED FACTOR 2; REACTIVE OXYGEN SPECIES;

EID: 84866613749     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db12-0248     Document Type: Article

References (50)

1. Simeoni U, Barker DJ. Offspring of diabetic pregnancy: long-term outcomes. Semin Fetal Neonatal Med 2009;14:119-124
2. Simeoni U, Ligi I, Buffat C, Boubred F. Adverse consequences of accelerated neonatal growth: cardiovascular and renal issues. Pediatr Nephrol 2011;26: 493-508
3. Ingelfinger JR. Pathogenesis of perinatal programming. Curr Opin Nephrol Hypertens 2004;13:459-464 (Pubitemid 38901626)
4. Plagemann A. Maternal diabetes and perinatal programming. Early Hum Dev 2011;87:743-747
5. Kanwar YS, Nayak B, Lin S, et al. Hyperglycemia: its imminent effects on mammalian nephrogenesis. Pediatr Nephrol 2005;20:858-866 (Pubitemid 40909252)
6. Kanwar YS, Akagi S, Nayak B, et al. Renal-specific oxidoreductase biphasic expression under high glucose ambience during fetal versus neonatal development. Kidney Int 2005;68:1670-1683 (Pubitemid 43169912)
7. Ornoy A. Embryonic oxidative stress as a mechanism of teratogenesis with special emphasis on diabetic embryopathy. Reprod Toxicol 2007;24:31-41 (Pubitemid 47042350)
8. Auten RL, Davis JM. Oxygen toxicity and reactive oxygen species: the devil is in the details. Pediatr Res 2009;66:121-127
9. Davis JM, Auten RL. Maturation of the antioxidant system and the effects on preterm birth. Semin Fetal Neonatal Med 2010;15:191-195
10. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001;414:813-820 (Pubitemid 34000785)
11. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes 2005;54:1615-1625 (Pubitemid 40770750)
12. Grabenbauer M, Fahimi HD, Baumgart E. Detection of peroxisomal proteins and their mRNAs in serial sections of fetal and newborn mouse organs. J Histochem Cytochem 2001;49:155-164 (Pubitemid 32113378)
13. Johkura K, Usuda N, Liang Y, Nakazawa A. Immunohistochemical localization of peroxisomal enzymes in developing rat kidney tissues. J Histochem Cytochem 1998;46:1161-1173 (Pubitemid 28445290)
14. Oberley TD, Oberley LW, Slattery AF, Lauchner LJ, Elwell JH. Immunohistochemical localization of antioxidant enzymes in adult Syrian hamster tissues and during kidney development. Am J Pathol 1990;137:199-214 (Pubitemid 20229602)
15. Brown MR, Miller FJ Jr, Li WG, et al. Overexpression of human catalase inhibits proliferation and promotes apoptosis in vascular smooth muscle cells. Circ Res 1999;85:524-533 (Pubitemid 29431953)
16. Yoo JH, Erzurum SC, Hay JG, Lemarchand P, Crystal RG. Vulnerability of the human airway epithelium to hyperoxia. Constitutive expression of the catalase gene in human bronchial epithelial cells despite oxidant stress. J Clin Invest 1994;93:297-302
17. de Haan JB, Stefanovic N, Nikolic-Paterson D, et al. Kidney expression of glutathione peroxidase-1 is not protective against streptozotocin-induced diabetic nephropathy. Am J Physiol Renal Physiol 2005;289:F544-F551 (Pubitemid 41208469)
18. Lee JM, Li J, Johnson DA, et al. Nrf2, a multi-organ protector? FASEB J 2005;19:1061-1066 (Pubitemid 40946431)
19. Moi P, Chan K, Asunis I, Cao A, Kan YW. Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region. Proc Natl Acad Sci USA 1994;91:9926-9930 (Pubitemid 24311921)
20. Shin DH, Park HM, Jung KA, et al. The NRF2-heme oxygenase-1 system modulates cyclosporin A-induced epithelial-mesenchymal transition and renal fibrosis. Free Radic Biol Med 2010;48:1051-1063
21. Jiang T, Huang Z, Lin Y, Zhang Z, Fang D, Zhang DD. The protective role of Nrf2 in streptozotocin-induced diabetic nephropathy. Diabetes 2010;59: 850-860
22. Wu QQ, Wang Y, Senitko M, et al. Bardoxolone methyl (BARD) ameliorates ischemic AKI and increases expression of protective genes Nrf2, PPARg, and HO-1. Am J Physiol Renal Physiol 2011;300:F1180-F1192
23. Kim HJ, Vaziri ND. Contribution of impaired Nrf2-Keap1 pathway to oxidative stress and inflammation in chronic renal failure. Am J Physiol Renal Physiol 2010;298:F662-F671
24. Kim HJ, Sato T, Rodríguez-Iturbe B, Vaziri ND. Role of intrarenal angiotensin system activation, oxidative stress, inflammation, and impaired nuclear factor-erythroid-2-related factor 2 activity in the progression of focal glomerulosclerosis. J Pharmacol Exp Ther 2011;337:583-590
25. Hosick PA, Stec DE. Heme oxygenase, a novel target for the treatment of hypertension and obesity? Am J Physiol Regul Integr Comp Physiol 2012; 302:R207-R214
26. Chen YW, Chenier I, Chang SY, Tran S, Ingelfinger JR, Zhang SL. High glucose promotes nascent nephron apoptosis via NF-kappaB and p53 pathways. Am J Physiol Renal Physiol 2011;300:F147-F156
27. Tran S, Chen YW, Chenier I, et al. Maternal diabetes modulates renal morphogenesis in offspring. J Am Soc Nephrol 2008;19:943-952
28. Zhang SL, Chen YW, Tran S, Chenier I, Hébert MJ, Ingelfinger JR. Reactive oxygen species in the presence of high glucose alter ureteric bud morphogenesis. J Am Soc Nephrol 2007;18:2105-2115 (Pubitemid 47041076)
29. Chen YW, Chenier I, Tran S, Scotcher M, Chang SY, Zhang SL. Maternal diabetes programs hypertension and kidney injury in offspring. Pediatr Nephrol 2010;25:1319-1329
30. Srinivas S, Goldberg MR, Watanabe T, D'Agati V, al-Awqati Q, Costantini F. Expression of green fluorescent protein in the ureteric bud of transgenic mice: a new tool for the analysis of ureteric bud morphogenesis. Dev Genet 1999;24:241-251 (Pubitemid 29211788)
31. Watanabe T, Costantini F. Real-time analysis of ureteric bud branching morphogenesis in vitro. Dev Biol 2004;271:98-108 (Pubitemid 38757778)
32. Brezniceanu ML, Liu F, Wei CC, et al. Catalase overexpression attenuates angiotensinogen expression and apoptosis in diabetic mice. Kidney Int 2007;71:912-923 (Pubitemid 46663797)
33. Brezniceanu ML, Liu F, Wei CC, et al. Attenuation of interstitial fibrosis and tubular apoptosis in db/db transgenic mice overexpressing catalase in renal proximal tubular cells. Diabetes 2008;57:451-459
34. Godin N, Liu F, Lau GJ, et al. Catalase overexpression prevents hypertension and tubular apoptosis in angiotensinogen transgenic mice. Kidney Int 2010;77:1086-1097
35. Bammann BL, Coulam CB, Jiang NS. Total and free testosterone during pregnancy. Am J Obstet Gynecol 1980;137:293-298 (Pubitemid 10068713)
36. Carlsen SM, Jacobsen G, Romundstad P. Maternal testosterone levels during pregnancy are associated with offspring size at birth. Eur J Endocrinol 2006;155:365-370 (Pubitemid 44269454)
37. Castracane VD, Stewart DR, Gimpel T, Overstreet JW, Lasley BL. Maternal serum androgens in human pregnancy: early increases within the cycle of conception. Hum Reprod 1998;13:460-464
38. Jeremy SD. Winter: sexual differentiation. In Endocrinology and Metabolism. 2nd ed. Felig P, Baxter JD, Broadus AE, Frohman LA, Eds. New York, McGraw-Hill Book Company, 1987, p. 996
39. Barkley MS, Michael SD, Geschwind II, Bradford GE. Plasma testosterone during pregnancy in the mouse. Endocrinology 1977;100:1472-1475 (Pubitemid 8094072)
40. Chang SY, Chen YW, Chenier I, Tran SleM, Zhang SL. Angiotensin II type II receptor deficiency accelerates the development of nephropathy in type I diabetes via oxidative stress and ACE2. Exp Diabetes Res 2011; 2011:521076
41. Qi Z, Fujita H, Jin J, et al. Characterization of susceptibility of inbred mouse strains to diabetic nephropathy. Diabetes 2005;54:2628-2637 (Pubitemid 41233584)
42. Weibel ER. Numerical density: shape and size of particles. In Stereological Methods Volume 2 Theoretical Foundations. Weibel ER, Ed. London, Academic Press, 1980, p. 149-152
43. Bertram JF. Counting in the kidney. Kidney Int 2001;59:792-796 (Pubitemid 32157946)
44. Brezniceanu ML, Wei CC, Zhang SL, et al. Transforming growth factor-beta 1 stimulates angiotensinogen gene expression in kidney proximal tubular cells. Kidney Int 2006;69:1977-1985
45. Zhang SL, Moini B, Ingelfinger JR. Angiotensin II increases Pax-2 expression in fetal kidney cells via the AT2 receptor. J Am Soc Nephrol 2004;15:1452-1465 (Pubitemid 38679670)
46. Karacay O, Sepici-Dincel A, Karcaaltincaba D, et al. A quantitative evaluation of total antioxidant status and oxidative stress markers in preeclampsia and gestational diabetic patients in 24-36 weeks of gestation. Diabetes Res Clin Pract 2010;89:231-238
47. Vaughan MR, Quaggin SE. How do mesangial and endothelial cells form the glomerular tuft? J Am Soc Nephrol 2008;19:24-33
48. Kang SJ, You A, Kwak MK. Suppression of Nrf2 signaling by angiotensin II in murine renal epithelial cells. Arch Pharm Res 2011;34:829-836
49. Yoh K, Itoh K, Enomoto A, et al. Nrf2-deficient female mice develop lupus-like autoimmune nephritis. Kidney Int 2001;60:1343-1353 (Pubitemid 32960028)
50. Yoh K, Hirayama A, Ishizaki K, et al. Hyperglycemia induces oxidative and nitrosative stress and increases renal functional impairment in Nrf2-deficient mice. Genes Cells 2008;13:1159-1170