Gender-dependent expression of pancreatic proteins in streptozotocin- induced diabetic rats

Biotechnology and Bioprocess Engineering

Volumn 18, Issue 6, 2013, Pages 1122-1134

  Aseer, Kanikkai Raja ^a   Yun, Jong Won ^a  

^a Daegu University   (South Korea)

Author keywords

2 DE; diabetes; gender dimorphism; pancreas proteome; streptozotocin

Indexed keywords

2-DE; AMINO ACID SYNTHESIS; BLOOD GLUCOSE LEVEL; DIFFERENTIAL REGULATION; GENDER DIMORPHISM; PROTEOMIC APPROACHES; REGULATION PATTERN; STREPTOZOTOCIN;

AMINO ACIDS; BIOCHEMISTRY; INSULIN; MEDICAL PROBLEMS; PROTEINS; RATS; SOCIAL SCIENCES;

BIOSYNTHESIS;

ADENOSINE KINASE; ALDEHYDE DEHYDROGENASE FAMILY 7 MEMBER A1 PROTEIN; ALPHA AMYLASE PANCREAS ISOENZYME; AMINO ACID; ANTIOXIDANT; ATP SYNTHASE SUBUNIT ALPHA PROTEIN; CHAPERONIN CONTAINING TCP1; CITRIC ACID; DIHYDROLIPOAMIDE DEHYDROGENASE; ESTRADIOL; EUKARYOTIC TRANSLATION ELONGATION FACTOR 1 DELTA PROTEIN; GLUCOSE; GLUTAMATE DEHYDROGENASE; GLUTAMYL AMINOPEPTIDASE; GLUTATHIONE TRANSFERASE P1; GLYCINE AMIDINOTRANSFERASE; HEMOGLOBIN A2; INSULIN; MEDIUM CHAIN SPECIFIC ACYL COA DEHYDROGENASE; METHYLCROTONOYL COENZYME A CARBOXYLASE; PANCREATIC LIPASE RELATED PROTEIN 1; PANCREATIC PROTEIN; PEROXIREDOXIN 6; PORPHOBILINOGEN SYNTHASE; PROTEIN; STREPTOZOCIN; TESTOSTERONE; TRYPSIN 1 PROTEIN; UNCLASSIFIED DRUG; UNINDEXED DRUG; WEE1 LIKE PROTEIN KINASE;

AMINO ACID SYNTHESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DAMAGE; CELL REGENERATION; CELL STRESS; CITRIC ACID CYCLE; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE PREDISPOSITION; DRUG INDUCED DISEASE; FEMALE; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE; GLYCOLYSIS; HORMONE BLOOD LEVEL; INSULIN BLOOD LEVEL; INSULIN RELEASE; INSULIN SYNTHESIS; INTRACELLULAR SIGNALING; LIPID METABOLISM; MALE; MASS SPECTROMETRY; NONHUMAN; PANCREAS; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION; RAT; SEX DIFFERENCE; TWO DIMENSIONAL GEL ELECTROPHORESIS;

EID: 84892656772     PISSN: 12268372     EISSN: 19763816     Source Type: Journal    
DOI: 10.1007/s12257-013-0324-2     Document Type: Article

References (63)

1. Szalat, A. and I. Raz (2008) Gender-specific care of diabetes mellitus: Particular considerations in the management of diabetic women. Diabetes Obes. Metab. 10: 1135-1156.
2. King, H., R. E. Aubert, and W. H. Herman (1998) Global burden of diabetes 1995-2025: Prevalence, numerical estimates, and projections. Diabetes Care 21: 1414-1431. (Pubitemid 28405191)
3. Macedo, C. S., S. M. Capelletti, M. C. S. Mercadante, C. R. Padovani, and C. T. Spadella (2002) Role of metabolic control on diabetic nephropathy. Acta Cir. Bras. 17: 370-376.
4. Wandell, P. E. and A. C Carlsson (2013) Time trends and gender differences in incidence and prevalence of type 1 diabetes in Sweden. Curr. Diabetes. Rev. 9: 342-349.
5. Wells, C. C., S. Riazi, R. W. Mankhey, F. Bhatti, http://0-www. sciencedirect.com.precise.petronas.com.my/science/article/pii/ S155085790580052X-aff1 C. Ecelbarger, and C. Maric (2005) Diabetic nephropathy is associated with decreased circulating estradiol levels and imbalance in the expression of renal estrogen receptors. Gend. Med. 2: 227-237. (Pubitemid 43192759)
6. Le May, C., K. Chu, M. Hu, C. S. Ortega, E. R. Simpson, K. S. Korach, M. J. Tsai, and F. Mauvais-Jarvis (2006) Estrogens protect pancreatic beta-cells from apoptosis and prevent insulin-deficient diabetes mellitus in mice. Proc. Natl. Acad. Sci. USA. 103: 9232-9237. (Pubitemid 43902561)
7. Vital, P., E. Larrieta, and M. Hiriart (2006) Sexual dimorphism in insulin sensitivity and susceptibility to develop diabetes in rats. J. Endocrinol. 190: 425-432. (Pubitemid 44307818)
8. Kim, S. W., H. J. Hwang, H. M. Kim, M. C. Lee, M. Shik Lee, J. W. Choi, and J. W. Yun (2006) Effect of fungal polysaccharides on the modulation of plasma proteins in streptozotocin-induced diabetic rats. Proteomics. 6: 5291-5302. (Pubitemid 44547167)
9. Kim, S. W., H. J. Hwang, E. J. Cho, J. Y. Oh, Y. M. Baek, J. W. Choi, and J. W. Yun (2006) Time-dependent plasma protein changes in streptozotocin- induced diabetic rats before and after fungal polysaccharide treatments. J. Proteome Res. 5: 2966-2976. (Pubitemid 44749215)
10. Kim, S. W., H. J. Hwang, Y. M. Baek, S. H. Lee, H. S. Hwang, and J. W. Yun (2008) Proteomic and transcriptomic analysis for streptozotocin-induced diabetic rat pancreas in response to fungal polysaccharide treatments. Proteomics. 8: 2344-2361. (Pubitemid 351898038)
11. Ahmed, M. (2010) Proteomics and islet research. Adv. Exp. Med. Biol. 654: 363-390.
12. Sparre, T., M. R. Larsen, P. E. Heding, A. E. Karlsen, O. N. Jensen, and F. Pociot (2005) Unraveling the pathogenesis of type 1 diabetes with proteomics: Present and future directions. Mol. Cell Proteomics. 4: 441-457. (Pubitemid 40590564)
13. Andersen, H. U., S. J. Fey, P. M. Larsen, A. Nawrocki, K. R. Hej naes, T. Mandrup-Poulsen, and J. Nerup (1997) Interleukin-1beta induced changes in the protein expression of rat islets: A computerized database. Electrophoresis. 18: 2091-2103. (Pubitemid 27501270)
14. Christensen, U. B., P. M. Larsen, S. J. Fey, H. U. Andersen, A. Nawrocki, T. Sparre, T. Mandrup-Poulsen, and J. Nerup (2000) Islet protein expression changes during diabetes development in islet syngrafts in BB-DP rats and during rejection of BB-DP islet allografts. Autoimmunity. 32: 1-15. (Pubitemid 30636037)
15. Larsen, P. M., S. J. Fey, M. R. Larsen, A. Nawrocki, H. U. Andersen, H. Kahler, C. Heilmann, M. C. Voss, P. Roepstorff, F. Pociot, A. E. Karlsen, and J. Nerup (2001) Proteome analysis of interleukin-1 beta-induced changes in protein expression in rat islets of Langerhans. Diabetes. 50: 105610-105663.
16. Sparre, T., U. B. Christensen, P. Mose Larsen, S. J. Fey, K. Wrzesinski, P. Roepstorff, T. Mandrup-Poulsen, F. Pociot, A. E. Karlsen, and J. Nerup (2002) IL-1beta induced protein changes in diabetes prone BB rat islets of Langerhans identified by proteome analysis. Diabetol. 45: 1550-1561. (Pubitemid 35352049)
17. Xie, X., S. Li, S. Liu, Y. Lu, P. Shen, and J. Ji (2008) Proteomic analysis of mouse islets after multiple low-dose streptozotocin injection. Biochim. Biophys. Acta 1784: 276-284.
18. Zhi, W., S. Purohit, C. Carey, M. Wang, and J. X. She (2010) Proteomic technologiesfor the discovery of type 1 diabetes biomarkers. J. Diabetes Sci. Technol. 4: 993-1002.
19. Jiang, Y. L., Y. Ning, X. L. Ma, Y. Y. Liu, Y. Wang, Z. Zhang, C. X. Shan, Y. D. Xu, L. M. Yin, and Y. Q. Yang (2011) Alteration of the proteome profile of the pancreas in diabetic rats induced by streptozotocin. Int. J. Mol. Med. 28: 153-160.
20. Yang, M., W. Liu, C. Y. Wang, T. Liu, F. Zhou, J. Tao, Y. Wang, and M. T. Li (2006) Proteomic analysis of differential protein expression in early process of pancreatic regeneration in pancreatectomized rats. Acta Pharmacol. Sin. 27: 568-578.
21. Resjo, S., K. Berger, M. Fex, and O. Hansson (2008) Proteomic studies in animal models of diabetes. Proteomics Clin. Appl. 2: 654-669. (Pubitemid 351772022)
22. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
23. Choi, J. W., X. Wang, J. I. Joo, D. H. Kim, T. S. Oh, D. K. Choi, and J. W. Yun (2010) Plasma proteome analysis in diet-induced obesity-prone and obesity-resistant rats. Proteomics. 10: 4386-4400.
24. Shevchenko, A., M. Wilm, O. Vorm, and M. Mann (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68: 850-858. (Pubitemid 26101214)
25. Rodriguez-Cuenca, S., E. Pujol, R. Justo, M. Frontera, J. Oliver, M. Gianotti, and P. Roca (2002) Sex-dependent thermogenesis, differences in mitochondrial morphology and function, and adrenergic response in brown adipose tissue. J. Biol. Chem. 277: 42958-42963. (Pubitemid 35285674)
26. Justo, R., J. Boada, M. Frontera, J. Oliver, J. Bermudez, and M. Gianotti (2005) Gender dimorphism in rat liver mitochondrial oxidative metabolism and biogenesis. Am. J. Physiol. Cell Physiol. 289: 372-378. (Pubitemid 41008883)
27. Zhang, D., J. Christianson, Z. X. Liu, L. Tian, C. S. Choi, S. Neschen, J. Dong, P. A. Wood, and G. I. Shulman (2010) Resistance to high-fat diet-induced obesity and insulin resistance in mice with very long-chain acyl CoA dehydrogenase deficiency. Cell. Metab. 11: 402-411.
28. Ashmarina, L. I., N. Rusnak, H. M. Miziorko, and G. A. Mitchell (1994) 3-Hydroxy-3-methylglutaryl-CoA lyase is present in mouse and human liver peroxisomes. J. Biol. Chem. 269: 31929-31932. (Pubitemid 24379569)
29. Sowers, M., C. Gonzalez Villalpando, M. P Stern, C. Fox, and B. D. Mitchell (1995) Relationships between physical activity, insulin levels and lipids in non-diabetic low income residents of Mexico City: The Mexico city diabetes study. Arch. Med. Res. 26: 133-140.
30. Adrogue, H. J., H. Wilson, A. E. III. Boyd, W. N. Suki, and knoyan (1982) Plasma acid base patterns in diabetic ketoacidosis. N. Engl. J. Med. 307: 1603-1610. (Pubitemid 13250419)
31. Wang, Z., L. Jiang, C. Huang, Z. Li, L. Chen, L. Gou, P. Chen, A. Tong, M. Tang, F. Gao, J. Shen, Y. Zhang, J. Bai, M. Zhou, D. Miao, and Q. Chen (2008) Comparative proteomics approach to screening of potential diagnostic and therapeutic targets for oral squamous cell carcinoma. Mol. Cell Proteomics. 7: 1639-1650.
32. Qiu, Y., T. Mao, Y. Zhang, M. Shao, J. You, Q. Ding, Y. Chen, D. Wu, D. Xie, X. Lin, X. Gao, R. J. Kaufman, W. Li, and Y. Liu (2010) A crucial role for RACK1 in the regulation of glucosestimulated IRE1alpha activation in pancreatic beta cells. Sci. Signal. 3: ra7.
33. Lipson, K. L., S. G. Fonseca, S. Ishigaki, L. X. Nguyen, E. Foss, R. Bortell, A. A. Rossini, and F. Urano (2006) Regulation of insulin biosynthesis in pancreatic beta cells by an endoplasmic reticulum-resident protein kinase IRE1. Cell Metab. 4: 245-254. (Pubitemid 44283955)
34. Anastasi, E., E. Ponte, R. Gradini, A. Bulotta, P. Sale, C. Tiberti, H. Okamoto, F. Dotta, and U. Di Mario (1999) Expression of Reg and cytokeratin 20 during ductal cell differentiation and proliferation in a mouse model of autoimmune diabetes. Eur. J. Endocrinol. 141: 644-652. (Pubitemid 30064766)
35. De Reggi, M. and B. Gharib (2001) Protein-X, pancreatic stone-, pancreatic thread-, reg-protein, P19, lithostathine, and now what? Characterization, structural analysis and putative function(s) of the major nonenzymatic protein of pancreatic secretions. Curr. Protein Pept. Sci. 2: 19-42. (Pubitemid 32409757)
36. Okamoto, H. (1999) The Reg gene family and Reg proteins: With special attention to the regeneration of pancreatic beta-cells. J. Hepatobiliary Pancreat. Surg. 6: 254-262.
37. Ohno, T., C. Ishii, N. Kato, Y. Ito, M. Shimizu, S. Tomono, K. Murata, and S. Kawazu (1995) Increased expression of a regenerating (reg) gene protein in neonatal rat pancreas treated with streptozotocin. Endocr. J. 42: 649-653.
38. Christofilis, M. A., J. Carrere, C. Atlan-Gepner, C. Zevaco-Mattei, C. Thivolet, N. Baeza, C. Figarella, and B. Vialettes (1999) Serum reg protein level is not related to the beta cell destruction/regeneration process during early phases of diabetogenesis in type I diabetes. Eur. J. Endocrinol. 141: 368-373. (Pubitemid 29529490)
39. Qiu, L., E. O. List, and J. J. Kopchick (2005) Differentially expressed proteins in the pancreas of diet-induced diabetic mice. Mol. Cell Proteomics. 4: 1311-1318. (Pubitemid 41448718)
40. Watanabe, T., Y. Yonemura, H. Yonekura, Y. Suzuki, H. Miyashita, K. Sugiyama, S. Moriizumi, M. Unno, O. Tanaka, and H. Kondo (1994) Pancreatic beta-cell replication and amelioration of surgical diabetes by Reg protein. Proc. Natl. Acad. Sci. U S A. 91: 3589-3592. (Pubitemid 24139475)
41. Kakkar, R., S. V. Mantha, J. Radhi, K. Prasad, and J. Kalra (1998) Increased oxidative stress in rat liver and pancreas during progression of streptozotocin-induced diabetes. Clin. Sci. 94: 623-632. (Pubitemid 28269062)
42. Kaneto, H., N. Katakami, M. Matsuhisa, and T. A. Matsuoka (2010) Role of reactive oxygen species in the progression of type 2 diabetes and atherosclerosis. Mediators Inflamm. 2010: 453892.
43. Strehlow, K., S. Rotter, S. Wassmann, O. Adam, C. Grohe, K. Laufs, M. Bohm, and G. Nickenig (2003) Modulation of antioxidant enzyme expression and function by estrogen. Circ Res. 93: 170-177. (Pubitemid 36919705)
44. Halliwell, B. (1994) Free radicals, antioxidants, and human disease: Curiosity, cause, or consequence? Lancet. 344: 721-724. (Pubitemid 24281426)
45. Liochev, S. I. and I. Fridovich (1994) The role of O2. - in the production of HO.:In vitro and in vivo. Free Radic. Biol. Med. 16: 29-33.
46. Lenzen, S., J. Drinkgern, and M. Tiedge (1996) Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues. Free Radic. Biol. Med. 20: 463-466. (Pubitemid 26077870)
47. Ketterer, B. (1998) Glutathione S-transferases and prevention of cellular free radical damage. Free Radic. Res. 28: 647-658. (Pubitemid 28454257)
48. Kim, S. K., K. J. Woodcroft, and R. F. Novak (2003) Insulin and glucagon regulation of glutathione S-transferase expression in primary cultured rat hepatocytes. J. Pharmacol. Exp. Ther. 305: 353-361. (Pubitemid 36373871)
49. Fatma, N., P. Singh, B. Chhunchha., E. Kubo, T. Shinohara, B. Bhargavan, and D. P. Singh (2011) Deficiency of Prdx6 in lens epithelial cells induces ER stress response-mediated impaired homeostasis and apoptosis. Am. J. Physiol. Cell Physiol. 301: 954-967.
50. Nair, S., D. Yadav, and C. S. Pitchumoni (2000) Association of diabetic ketoacidosis and acute pancreatitis: Observations in 100 consecutive episodes of DKA. Am. J. Gastroenterol. 95: 2795-2800.
51. Hardt, P. D., A. Killinger, J. Nalop, H. Schnell-Kretschmer, T. Zekorn, and H. U. Klor (2002) Chronic pancreatitis and diabetes mellitus. A retrospective analysis of 156 ERCP investigations in patients with insulin-dependent and non-insulin-dependent diabetes mellitus. Pancreatol. 2: 30-33. (Pubitemid 34639099)
52. Vantyghem, M. C., S. Haye, M. Balduyck, C. Hober, P. M. Degand, and J. Lefebvre (1999) Changes in serum amylase, lipase and leukocyte elastase during diabetic ketoacidosis and poorly controlled diabetes. Acta Diabetol. 36: 39-44.
53. Jennens, M. L. and M. E. Lowe (1995) Rat GP-3 is a pancreatic lipase with kinetic properties that differ from colipase-dependent pancreatic lipase. J. Lipid Res. 36: 2374-2382.
54. Lowe, M. E., M. H. Kaplan, L. Jackson-Grusby, D. D'Agostino, and M. J. Grusby (1998) Decreased neonatal dietary fat absorption and T cell cytotoxicity in pancreatic lipase-related protein 2-deficient mice. J. Biol. Chem. 273: 31215-31221. (Pubitemid 28533136)
55. Rippe, C., K. Berger, J. Mei, M. E. Lowe, and C. Erlanson-Albertsson (2003) Effect of long-term high-fat feeding on the expression of pancreatic lipases and adipose tissue uncoupling proteins in mice. Pancreas. 26: e36-42.
56. Rosendahl, J., H. Witt, R. Szmola, E. Bhatia, B. Ozsvari, O. Landt, H. U. Schulz, T. M. Gress, R. Pfutzer, M. Lohr, P. Kovacs, M. Bluher, M. Stumvoll, G. Choudhuri, P. Hegyi, R. H. te Morsche, J. P. Drenth, K. Truninger, M. Macek, G. Puhl, U. Witt, H. Schmidt, C. Buning, J. Ockenga, A. Kage, D. A. Groneberg, R. Nickel, T. Berg, B. Wiedenmann, H. Bodeker, V. Keim, J. Mossner, N. Teich, and M. Sahin-Toth (2008) Chymotrypsin C (CTRC) variants that diminish activity or secretion are associated with chronic pancreatitis. Nat. Genet. 40: 78-82.
57. Szabo, A. and M. Sahin-Toth (2012) Increased activation of hereditary pancreatitis-associated human cationic trypsinogen mutants in presence of chymotrypsin C. J. Biol. Chem. 287: 20701-20710.
58. Rebours, V., P. Levy, and P. Ruszniewski (2012) An overview of hereditary pancreatitis. Dig. Liver Dis. 44: 8-15.
59. Saluja, A. K., L. Bhagat, H. S. Lee, M. Bhatia, J. L. Frossard, and M. L. Steer (1999) Secretagogue-induced digestive enzyme activation and cell injury in rat pancreatic acini. Am. J. Physiol. 276: 835-842.
60. Hartl, F. U. (1996) Molecular chaperones in cellular protein folding. Nature 381: 571-579. (Pubitemid 26177472)
61. Quintana, F. J., A. Rotem, P. Carmi, and I. R Cohen (2000) Vaccination with empty plasmid DNA or CpG oligonucleotide inhibits diabetes in non-obese diabetic mice: Modulation of spontaneous 60-kDa heat shock protein autoimmunity. J. Immunol. 165: 6148-6155.
62. Tessari, P., L. Puricelli, E. Iori, G. Arrigoni, M. Vedovato, P. James, A. Coracina, and R. Millioni (2007) Altered chaperone and protein turnover regulators expression in cultured skin fibroblasts from type 1 diabetes mellitus with nephropathy. J. Proteome Res. 6: 976-986. (Pubitemid 46480462)
63. Pullen, T. J., A. M. Khan, G. Barton, S. A. Butcher, G. Sun, and G. A. Rutter (2010) Identification of genes selectively disallowed in the pancreatic islet. Islets. 2: 89-95.