Poor maternal nutrition leads to alterations in oxidative stress, antioxidant defense capacity, and markers of fibrosis in rat islets: Potential underlying mechanisms for development of the diabetic phenotype in later life

FASEB Journal

Volumn 24, Issue 8, 2010, Pages 2762-2771

  Tarry Adkins, Jane L ^a   Chen, Jian Hua ^a   Jones, Richard H ^a   Smith, Noel H ^a   Ozanne, Susan E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Fibrosis; Hyperglycemia; Type 2 diabetes

Indexed keywords

ANGIOTENSIN RECEPTOR; CHOLESTEROL; COLLAGEN TYPE 1; COLLAGEN TYPE 3; CONNECTIVE TISSUE GROWTH FACTOR; COPPER ZINC SUPEROXIDE DISMUTASE; FATTY ACID; GLUCOSE; HEME OXYGENASE 1; HIGH DENSITY LIPOPROTEIN; INSULIN; INTERLEUKIN 6; LOW DENSITY LIPOPROTEIN; MANGANESE SUPEROXIDE DISMUTASE; PEROXIREDOXIN 1; PEROXIREDOXIN 2; PEROXIREDOXIN 3; TRANSFORMING GROWTH FACTOR BETA1; TRIACYLGLYCEROL; XANTHINE OXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHOLESTEROL BLOOD LEVEL; CYSTIC FIBROSIS; DIETARY INTAKE; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL MODEL; EXPERIMENTAL RAT; FATTY ACID BLOOD LEVEL; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; INSULIN BLOOD LEVEL; LIPID PEROXIDATION; LIPOPROTEIN BLOOD LEVEL; MALE; MATERNAL NUTRITION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET; PHENOTYPE; PRIORITY JOURNAL; PROGENY; PROTEIN RESTRICTION; RAT; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION; URINALYSIS;

ANIMALS; ANTIOXIDANTS; DIABETES MELLITUS, TYPE 2; FEMALE; FIBROSIS; ISLETS OF LANGERHANS; MALE; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; OXIDATIVE STRESS; PHENOTYPE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS;

ANIMALIA; RATTUS;

EID: 77955794377     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-156075     Document Type: Article

References (57)

1. Hales, C. N., Barker, D. J., Clark, P. M., Cox, L. J., Fall, C., Osmond, C., and Winter, P. J. (1991) Fetal and infant growth and impaired glucose intolerance at age 64. BMJ 26, 1019-1022
2. Ravelli, A. C., van der Meulen, J. H., Michels, J. P., Osmond, C., Barker, D. J., Hales, C. N., and Bleker, O. P. (1998) Glucose tolerance in adults after prenatal exposure to famine. Lancet 351, 173-177
3. Ong, K. K., Petry, C. J., Emmett, P. M., Sandhu, M. S., Kiess, W., Hales, C. N., Ness, A. R., and Dungar, D. B. (2004) ALSPAC study team. Insulin sensitivity and secretion in normal children related to size at birth, postnatal growth and plasma insulin-like growth factor-I levels. Diabetologia 47, 1064-1070
4. Barker, D. J., Hales, C. N., Fall, C. H., Osmond, C., Phipps, K., and Clark, P. M. (1993) Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36, 62-67
5. Lithell, H. O., McKeigue, P. M., Berglund, L., Mohsen, R., Lithell, U. B., and Leon, D. A. (1996) Relation of size at birth to non-insulin dependent diabetes and insulin concentrations in men aged 50-60 years. BMJ 312, 406-410
6. Poulsen, P., Vaag, A. A., Kyvik, K. K., Moller-Jensen, D., and Beck-Neilsen, H. (1997) Low birth weight is associated with NIDDM in discordant monozygotic and dizygotic twin pairs. Diabetologia 40, 439-446
7. Bo, S., Cavelli-Perin, P., Scaglione, L., Ciccone, G., and Pagano, G. (2000) Low birth weight and metabolic abnormalities in twins with increased susceptibility to Type 2 diabetes mellitus. Diabet. Med. 5, 365-370
8. Grunnet, L., Vielworth, S., Vaag, A. A., and Poulsen, P. (2007) Birth weight is nongenetically associated with glucose intolerance in elderly twins, independent of adult obesity. J. Int. Med. 262, 96-103
9. McMillen, C., and Robinson, J. (2005) Developmental origins of the metabolic syndrome: Prediction, plasticity and programming. Am. Physiol. J. 85, 571-633
10. Dahri, S., Snoeck, A., Reusens-Billen, B., Remacle, C., and Hoet, J. J. (1991) Islet function in offspring of mothers on a low protein diet during gestation. Diabetes 40, 115-120
11. Petrik, J., Reusens, B., Arany, E., Remacle, C., Coelho, C., Hoet, J. J., and Hill, D. J. (1999) A low protein diet alters the balance of islet cell replication and apoptosis in the fetal and neonatal rat and is associated with a reduced pancreatic expression of insulin-like growth factor II. Endocrinology 140, 4861-4873
12. Ozanne, S. E., Jensen, C. B., Tingey, K. T., Storgaard, H., Madsbad, S., and Vaag, A. A. (2005) Low birth weight is associated with specific changes in muscle insulin signalling protein expression. Diabetologia 48, 547-552
13. Ozanne, S. E., Olsen, G. E., Hansen, L. L., Tingey, K. T., Nave, B. T., Wang, C. L., Harthil, K., Petry, C. J., Buckley, A., and Mosthaf-Seedorff, L. (2003) Early growth restriction leads to down regulation of protein kinase C zeta and insulin resistance in skeletal muscle. J. Endocrinol. 177, 235-242
14. Petry, C. J., Ozanne, S. E., Wang, C. L., and Hales, C. N. (2000) Effects of early low protein restriction and adult obesity on rat pancreatic hormone content and glucose tolerance. Horm. Metab. Res. 32, 233-239
15. Shepherd, P. R., Crowther, N. J., Desai, M., Hales, C. N., and Ozanne, S. E. (1997) Altered adipocyte properties in the offspring of protein malnourished rats. Br. J. Nutr. 78, 121-129
16. Hales, C. N., Desai, M., Ozanne, S. E., and Crowther, N. J. (1996) Fishing in the stream of diabetes: from measuring insulin to the control of fetal organogenesis. Biochem. Soc. Trans. 24, 341-350
17. Petry, C. J., Dorling, M. W., Pawlak, D. B., and Ozanne, S. E. (2001) Diabetes in old male offspring fed a reduced protein diet. Int. J. Exp. Diabetes Res. 2, 139-143
18. Garafano, A., Czernichow, P., and Breant, B. (1999) Effect of ageing on beta-cell mass and function in rats malnourished during the perinatal period. Diabetologia 42, 711-718
19. Valko, V., Leibfritz, D., Moncol, J., Cronin, M. T. D., Mazur, M., and Telser, J. (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39, 44-84
20. Newsholme, P., Morgan, D., Rebelato, E., Oliveira-Emilio, H. C., Procopio, R., Curi, R., and Caripenelli, A. (2009) Insights into the critical role of NADPH oxidase(s) in the normal and dysregulated pancreatic beta cell. Diabetologia 52, 2489-2498
21. Newsholme, P., Haber, E. P., Hirabara, S. M., Rebelato, E. L. O., Procopio, J., Morgan, D., Oliveira-Emilio, H. C., Carpinelli, A. R., and Curi, R. (2007) Diabetes associated cell stress and dysfunction: role of mitochondrial and non-mitochondrial ROS production and activity. J. Physiol. 581, 9-24
22. Lenzen, S., Drinkgern, J., and Tiedge, M. (1996) Low antioxidant enzyme gene expression in pancreatic islets compared with other various mouse tissues. Free Rad. Biol. Med. 20, 464-466
23. Masamune, M., Watanabe, T., Kikuta, K., Satoh, K., and Shimosegawa, T. (2008) NADPH oxidase plays a crucial role in the activation of pancreatic stellate cells. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G99-G108
24. Tanioka, H., Mizushima., T., Shirahige, A., Matusushita, K., Ochi, K., Ichimura, M., Matsumura, N., Shinji, T., Tanimoto, M., and Koide, N. (2006) Xanthine oxidase-derived free radicals directly activate rat pancreatic stellate cells. J. Gastroenterol. Hepatol. 21, 537-544
25. Hong, O. K., Lee, S. H., Rhee, M., Ko, S. H., Cho, J. H., Choi, Y. H., Song, K. H., Son, H. Y., and Yoon, K. H. (2007) Hyperglycemia and hyperinsulinemia have additive effects on activation and proliferation of pancreatic stellate cells: possible explanation of islet-specific fibrosis in type 2 diabetes mellitus. J. Cell Biol. 101, 665-675
26. Snoeck, A., Remacle, C., Reusens, B., and Hoet, J. J. (1990) Effect of low protein during pregnancy on the fetal rat pancreas. Biol. Neonate 57, 107-118
27. Tarry-Adkins, J. L., Chen, J. H., Smith, N. H., Jones, R. H., Cherif, C., and Ozanne, S. E. (2009) Poor maternal nutrition followed by accelerated growth leads to telomere shortening and increased markers of cell senescence in rat islets. FASEB J. 23, 1521-1528
28. Armitage, J. A., Khan, I. Y., Taylor, P. D., Nathanielsz, P. W., and Poston, L. (2004) Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals? J. Physiol. 561.2, 355-377
29. Evans, J. L., Goldfine, I. D., Maddux, B. A., and Grodsky, G. M. (2003) Are oxidative stress-activated signalling pathways mediators of insulin resistance and beta cell dysfunction? Diabetes 52, 1-8.
30. Grankvist, K., Marklund, S. L., and Taljedal, I. B. (1981) CuZn-superoxide dismutase, Mn-superoxide dismutase, catalase and glutathione peroxidase in pancreatic islets and other tissues in the mouse. Biochem. J. 173, 83-91
31. Azevedo-Martin, A. K., Lortz, S., Lenzen, S., Curi, R., Eizirik, D. L., and Tiedge, M. (2003) Improvement of the mitochondrial antioxidant status prevents cytokine-induced nuclear kappaB activation in insulin producing cells. Diabetes 52, 93-101
32. Chen, H., Li, X., and Epstein, P. N. (2005) MnSOD and catalase transgenes demonstrate that protection of islets from oxidative stress does not alter cytotoxicity. Diabetes 54, 1437-1446
33. Pileggi, A., Molano, R. D., Berney, T., Cattan, P., Vizzardelli, C., Oliver, R., Fraker, C., Ricordi, C., Pastori, R. L., Bach, F. H., and Inverardi, L. (2001) Heme oxygenase-1 induction in islet cells results in protection from apoptosis and improved in vivo function after transplantation, Diabetes 50, 1983-1991
34. Li, Y. X., Li, G., Dong, W. P., Lu, D. R., and Tam, J. M. (2006) Protection of human islets from induction of apoptosis and improved islet function with HO-1 transduction. Chin. Med. J. (Engl.) 119, 1639-1645
35. Ye, J., and Laychock, S. G. (1998) A protective role for heme oxygenase expression in pancreatic islets exposed to interleukin 1 β. Endocrinology 139, 4155-4163
36. Won, K. C., Moon, J. S., Eun, M. J., Yoon, J. S., Chun, K. A., Cho, I. H., Kim, Y. W., and Lee, H. W. (2006) A protective role for heme oxygenase-1 in INS1 cells and rat islets that are exposed to high glucose conditions. J. Korean Med. Sci. 21, 418-424
37. Kajimoto, Y., and Kaneto, H. (2004) Role of oxidative stress in pancreatic β-cell dysfunction. Ann. N. Y. Acad. Sci. 1011, 168-176
38. Brand, M. D., Affourtit, C., Esteves, T. C., Green, K., Lambert, A. J., Miwa, S., Pakay, J. L., and Parker, N. (2004) Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Rad. Biol. Med. 37, 755-767
39. Guichard, C., Moreau, R., Pessayre, D., Epperson, T. K., and Krauss, H. K. (2008) NOX family NADPH oxidases in liver and pancreatic islets: a role in the metabolic syndrome and diabetes? Biochem. Soc. Trans. 36, 920-929
40. Bedard, K., and Krause, H. K. (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87, 245-313
41. Nakamaya, M., Inoguchi, T., Sonta, T., Maeda, Y., Sasaki, S., Saswada, F., Tsubouchi, H., Sonanda, N., Kobayashi, K., Sumimoto, H., and Nawata, H. (2005) Increased expression of NAD(P)H oxidase in islets of animal models of type 2 diabetes and its improvement by an AT1 receptor antagonist. Biochem. Biophys. Res. Commun. 332, 927-933
42. Morgan, D., Oliveira-Emilio, H. R., Keane, D., Hirata, A. E., Santos da Rocha, M., Bordin, S., Curi, R., Newsolme, P., and Carpinelli, A. R. (2007) Glucose, palmitate, and pro-inflammatory cytokines modulate and activity of a phagocyte-like NADPH oxidase in rat pancreatic cells and a clonal beta cell line. Diabetologia 50, 359-369
43. Manae, A., Raicu, M., and Simionescu, M. (2005) Expression of functionally phagocyte-type NAD(P)H oxidase in pericytes: effect of angiotensin II and high glucose. Biol. Cell 97, 723-734
44. Karawitz-Biniska, A., Suzin, A., and Sieroszewski, P. (2008) Evaluation of oxidative stress in pregnant women with intrauterine growth retardation. Med. Sci. Monit. 8, CR211-CR216
45. Simmons, R. A., Suponitsky-Kroter, I., and Selak, M. A. (2005) Progressive accumulation of mitochondrial DNA mutations and decline in mitochondrial function lead to β-cell function. J. Biol. Chem. 31, 28785-28791
46. Apte, M. V., Haber, P. S., Darby, S. J., Rodgers, S. C., McCaughan, G. W., Korsten, M. A., Pirola, R. C., and Wilson, J. S. (1999) Pancreatic stellate cells are activated by proinflammatory cytokines: Implications for pancreatic fibrogenesis. Gut 43, 128-133
47. Nagashio, Y., Asaumi, H., Watanabe, S., Nomiyama, Y., Taguchi, M., Tashiro, M., Sugaya, T., and Otsuki, M. (2004) Angiotensin II type I receptor interaction is an important regulator for the development of pancreatic fibrosis in mice. Am. J. Gastrointest. Liver Physiol. 287, G170-G177
48. Chu, K-Y., Lau, T., Carlsson, P., and Leung, P. (2006) Angiotensin II type I receptor blockade improves β-cell function and glucose tolerance in a mouse model of type 2 diabetes. Diabetes 55, 367-374
49. Shao, J., Iwashita, N., Du, H., Wang, Y., Wang, Y., Zhao, M., Wang, J., Watada, H., and Kawamori, R. (2007) Angiotensin II receptor blocker provides pancreatic β-cell protection independent of blood pressure lowering in diabetic db/db mice. Acta Pharmacol. Sin. 28, 246-257
50. Leung, K. K., and Leung, P. S. (2008) Effects of hyperglycemia on angiotensin II receptor type I expression on insulin secretion in an INS-1E pancreatic beta-cell line. J. Pancreas 9, 290-299
51. Wenzel, P., Schulz, E., Oelze, M., Muller, J., Schuhmacher, S., Alhamdani, M. S., Debrezion, J., Hortmann, M., Reifenburg, K., Fleming, I., Munzel, T., and Daiber, A. (2008) AT1- receptor blockade by telmisartan upregulates GTP-cyclohydrolase I and protects eNOS in diabetic rats. Free Rad. Biol. Med. 45, 619-626
52. Hong, O. K., Lee, S.-H., Rhee, M., Ko, S-H., Cho, J-H., Choi, Y-H., Song, K-H., Son, H-Y., and Yoon, K-H. (2007) Hyperglyemia and hyperinsulinemia have additive effects on activation and proliferation of pancreatic stellate cells: possible explanation of islet-specific fibrosis seen in type 2 diabetes mellitus. J. Biochem. Chem. 101, 665-675
53. Karger, A., Fitzner, B., Brock, P., Sparmann, G., Emmrich, J., Liebe, S., and Jaster, R. (2008) Molecular insights into connective tissue growth factor action in rat pancreatic stellate cells. Cell Signal 20, 1865-1872
54. Bonnefont-Rousselot, D., Bastard, J. P., Jaudon, M. C., and Delattre, J. (2000) Consequences of the diabetic status on the oxidant/antioxidant balance. Diabetes. Metab. (Paris) 26, 162-166
55. Shimizu, K., Ogawa, F., Akiyama, Y., Murio, E., Yoshizaki, A., Iwata, Y., Komura, K., Bae, S., and Sato, S. (2008) Increased serum levels of N(epilson)-(hexanoyl)lysine, a new marker of oxidative stress, in systemic sclerosis. J. Rhematol. 35, 2214-2219
56. Memisogullari, R., Taysi, S., Bakan, E., and Capoglu, I. (2003) Antioxidant status and lipid peroxidation in type II diabetes mellitus. Cell Biochem. Funct. 21, 291-296
57. Lodivici, M., Bigagli, E., Bardini, G., and Rotella, C. M. (2009) Lipoperoxidation and antioxidant capacity in patients with poorly controlled type 2 diabetes. Toxicol. Ind. Health 25, 337-341