Gender-dimorphic regulation of liver proteins in Streptozotocin-induced diabetic rats

Biotechnology and Bioprocess Engineering

Volumn 19, Issue 1, 2014, Pages 93-107

  Chaudhari, Harmesh N ^a   Yun, Jong Won ^a  

^a Daegu University   (South Korea)

Author keywords

2 DE; gender differences; liver proteome; sterptozotocin; type 1 diabetes mellitus

Indexed keywords

AMINO ACIDS; ELECTROPHORESIS; PROTEINS; RATS;

2-DE; BLOOD GLUCOSE LEVEL; DIFFERENTIAL REGULATION; GENDER DIFFERENCES; PROTEOMIC ANALYSIS; STERPTOZOTOCIN; TWO-DIMENSIONAL GEL ELECTROPHORESIS (2-DE); TYPE 1 DIABETES MELLITUS;

SOCIAL SCIENCES;

DOPACHROME TAUTOMERASE; EARLY PREGNANCY FACTOR; ESTRADIOL; INSULIN; LIVER PROTEIN; METHIONINE; TESTOSTERONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; CITRIC ACID CYCLE; CONTROLLED STUDY; DISEASE PREDISPOSITION; DISEASE SEVERITY; FEMALE; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE; INSULIN RELEASE; LIPID METABOLISM; LIVER HISTOLOGY; LIVER INJURY; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; ORAL GLUCOSE TOLERANCE TEST; PATHOPHYSIOLOGY; PHENOTYPE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEOMICS; RAT; REGULATORY MECHANISM; SEX DIFFERENCE; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; STRESS; TWO DIMENSIONAL GEL ELECTROPHORESIS; WESTERN BLOTTING;

EID: 84896929113     PISSN: 12268372     EISSN: 19763816     Source Type: Journal    
DOI: 10.1007/s12257-013-0612-x     Document Type: Article

References (65)

1. WHO report (2012) http://www.who.int/mediacentre/factsheets/fs312/en/
2. Atkinson, M. A., J. Bluestone, G. Eisenbarth, M. Hebrok, K. Herold, D. Accili, M. Pietropaolo, P. Arvan, M. Herrath, D Markel, and C. Rhodes (2011) How does type 1 diabetes develop? The notion of homicide or â-cell suicide revisited. Diabetes 60: 1370-1379.
3. Report of the Expert Committee on Diagnosis and Classification of Diabetes Mellitus (1997) Expert committee on the diagnosis and classification of diabetes mellitus. Diab. Care 20: 1183-1197.
4. Gale, E. A. and K. Gillespie (2001) Diabetes and gender. Diabetol. 44: 3-15. (Pubitemid 32141879)
5. Legato, M. J., A. Gelzer, R. Goland, S. Ebner, S. Rajan, V. Villagra, and M. Kosowski (2006) Gender-specific care of the patient with diabetes: Review and recommendations. Gend. Med. 3: 131-158. (Pubitemid 44069479)
6. Zillikens, M. C., M. Yazdanpanah, L. Pardo, F. Rivadeneira, Y. Aulchenko, B. Oostra, A. Uitterlinden, H. Pols, and C. Van Duijn (2008) Sex-specific genetic effects influence variation in body composition. Diabetol. 51: 2233-2241.
7. King, H., R. Aubert, and W. Herman (1998) Global burden of diabetes, 1995-2025: Prevalence, numerical estimates, and projections. Diab. Care 21: 1414-1431. (Pubitemid 28405191)
8. Auryan, S. and R. Itamar (2008) Gender-specific care of diabetes mellitus: Particular considerations in the management of diabetic women. Diab. Obes. Metab. 10: 1135-1156.
9. Kumar, K. M. P. (1996) Gender difference in diabetes mellitus. Int. J. Diab. Dev. Count. 16: 103-104.
10. 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)
11. Perreault, L., M. Yong, S. Agogo-Jack, E. Horton, D. Marrero, J. Crandall, and E. Barrett-Connor (2008) Sex differences in diabetes risk and the effect of intensive lifestyle modification in the diabetes prevention program. Diab.s Care 31: 1416-1421.
12. Satav, J. G. and S. Katyare (2004) Effect of Streptozotocin induced diabetes on oxidative energy metabolism in rat liver. Ind. J. Clin. Biochem. 19: 23-31.
13. Sajad, H. M., R. Abdui-Baqui, M. Bhagat, and S. Abdul-Wahid (2008) Biochemical and histomorphological study of streptozotocin induced diabetes mellitus in rabbits. Pak. J. Nutrit. 7: 359-364.
14. Roy, A. and B. Chatterjee (1983) Sexual dimorphism in the liver. Ann. Rev. Physiol. 45: 37-50.
15. 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.
16. Sparre T., M. Larsen, P. Heding, A. Karlsen, O. 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)
17. Scott, E. M., A. Carter, and J. Findlay (2005) The application of proteomics to diabetes. Diab. Vasc. Dis. Res. 2: 54-60. (Pubitemid 40826996)
18. Korc, M. (2003) Diabetes mellitus in the era of proteomics. Mol. Cell Proteom. 2: 399-404.
19. Sundsten, T. and H. Ortsater (2009) Proteomics in diabetes research. Mol. Cell Endocrinol. 297: 93-103.
20. Sattar, N. and D. Hodgkin (2012) Biomarkers for diabetes prediction, pathogenesis or pharmacotherapy guidance? Past, present and future possibilities. Diabet. Med. 29: 5-13.
21. Jiang, Y. L., Y. Ning, X. Ma, Y. Liu, Y. Wang, Z. Zhang, C. Shan, Y. Xu, L. Yin, and Y. Yang (2011) Alteration of the proteome profile of the pancreas in diabetic rats induced by Streptozotocin. Int. J. Mol. Med. 28: 153-160.
22. Zhi, W., S. Purohit, C. Carey, M. Wang, and J. She (2010) Proteomic technologies for the discovery of Type 1 diabetes biomarkers. J. Diab. Sci. Technol. 4: 993-1002.
23. Johnson, D. T., R. Harris, S. French, A. Aponte, and R. Balaban (2009) Proteomic changes associated with diabetes in the BB-DP rat. Am. J. Physiol. Endocrinol. Metab. 296: 422-432.
24. 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.
25. Wang, X., J. Choi, J. Joo, D. Kim, T. Oh., D. Choi, and J. Yun (2011) Differential expression of liver proteins between obesityprone and obesity-resistant rats in response to high fat diet. Br. J. Nutrit. 106: 612-626.
26. Wang, X., J. Choi, T. Oh, D. Choi, R. Mukherjee, H. Liu, and J. Yun (2012) Comparative hepatic proteome analysis between lean and obese rats fed a high fat diet reveals existence of gender differences. Proteomics 12: 284-299.
27. Choi, M., J. Choi, H. Chaudhari, K. Aseer, R. Mukherjee, and J. Yun (2013) Gender-dimorphic regulation of skeletal muscle proteins in streptozotocin-induced diabetic rats. Cell Physiol. Biochem. 31: 408-420.
28. Shevchenko, A., M. Wilm, O. Vorm, and M. Man (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68: 850-858.
29. Khor, V. K., R. Dhir, X. Yin, R. Ahima, and W. Song (2010) Estrogen sulfotransferase regulates body fat and glucose homeostasis in female mice. Am. J. Physiol. Endocrinol. Metab. 299: 657-664.
30. Song, W. C., Y. Qian, and A. Li (1998) Estrogen sulfotransferase expression in the human liver: Marked interindividual variation and lack of gender specificity. J. Pharmacol. Exp. Ther. 284: 1197-1202. (Pubitemid 28130851)
31. Khor, V. K., M. Tong, Y. Qian, and W. Song (2008) Gender-specific expression and mechanism of regulation of estrogen sulfotransferase in adipose tissues of the mouse. Endocrinol. 149: 5440-5448.
32. Bass, N. M., J. Manning, R. Ockner, J. Gordon, S. Seetharam, and D. Alpers (1985) Regulation of the biosynthesis of two distinct fatty acid-binding proteins in rat liver and intestine. Influences of sex difference and of clofibrate. J. Biol. Chem. 260: 1432-1436. (Pubitemid 15144156)
33. Veerkamp, J. H. (1995) Fatty acid transport and fatty acid-binding proteins. Proc. Nutr. Soc. 54: 23-37.
34. Gossett, R. E., A. Frolov, J. Roths, W. Behnke, A. Kier, and F. Schroeder (1996) Acyl-CoA binding proteins: Multiplicity and function. Lipids 31: 895-918. (Pubitemid 26313708)
35. May, C. L., T. Pineau, K. Bigot, C. Kohl, J. Girard, and J. Pégorier (2000) Reduced hepatic fatty acid oxidation in fasting PPARα null mice is due to impaired mitochondrial hydroxymethylglutaryl-CoA synthase gene expression. FEBS Lett. 475: 163-166. (Pubitemid 30408445)
36. Williamson, D. H., M. Bates, and H. Krebs (1968) Activity and intracellular distribution of enzymes of ketone-body. Biochem. J. 108: 353-361.
37. Harris, I. R., H. Hoppner, W. Siefken, A. Farrell, and K. Wittern (2000) Regulation of HMG CoA synthase and HMG CoA reductase by insulin and epidermal growth factor in HaCaT Keratinocytes. J. Invest. Dermatol. 114: 83-87. (Pubitemid 30195977)
38. Boquist, L., I. Ericsson, R. Lorentzon, and L. Nelson (1985) Alterations in mitochondrial aconitase activity and respiration, and in concentration of citrate in some organs of mice with experimental or genetic diabetes. FEBS Lett. 183: 173-176. (Pubitemid 15090148)
39. Kil, I. S., J. Lee, A. Shin, and J. Park (2004) Glycation-induced inactivation of NADP+-dependent isocitrate dehydrogenase: Implications for diabetes and aging. Free Radic. Biol. Med. 37: 1765-1778. (Pubitemid 39441061)
40. Jo, S. H., M. Son, H. Koh, S. Lee, I. Song, Y. Kim, Y. Lee, K. Jeong, W. Kim, J. Park, B. Song, and T. Huh (2001) Control of mitochondrial redox balance and cellular defense against oxidative damage by mitochondrial NADP+-dependent isocitrate dehydrogenase. J. Biol. Chem. 276: 16168-16176.
41. Kakkar, R., S. 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. Hamdena, K., S. Carreaub, M. Boujbihaa, S. Lajmic, D. Aloulouc, D. Kchaoud, and A. Elfeki (2008) Hyperglycaemia, stress oxidant, liver dysfunction and histological changes in diabetic male rat pancreas and liver: Protective effect of 17 β-estradiol. Steroids 73: 495-501.
43. Lei, X. G. and M. Vatamaniuk (2011) Two tales of antioxidant enzymes on beta cells and diabetes. Antioxid. Redox Sig. 14: 489-503.
44. Cho, S. Y., J. Park, E. Park, M. Choi, M. Lee, S. Jeon, M. Jang, M. Kim, and Y. Park (2002) Alternation of hepatic antioxidant enzyme activities and lipid profile in Streptozotocin-induced diabetic rats by supplementation of dandelion water extract. Clin. Chim. Acta 317: 109-117. (Pubitemid 34114025)
45. Yilmaz, H. R., E. Uz, N. Yucel, I. Altuntas, and N. Ozcelik (2004) Protective effect of caffeic acid phenethyl ester (CAPE) on lipid peroxidation and antioxidant enzymes in diabetic rat liver. J. Biochem. Mol. Toxicol. 18: 234-238. (Pubitemid 39341509)
46. Rodrigues, G. R., F. Di Naso, M. Porawski, E. Marcolin, N. Kretzmann, A. Ferraz, M. Richter, C. Marroni, and N. Marroni (2012) Treatment with aqueous extract from Croton cajucara Benth reduces hepatic oxidative stress in Streptozotocin-diabetic rats. J. Biomed. Biotechnol. doi: 10.1155/2012/902351.
47. Saxena, A. K., P. Srivastava, R. Kale, and N. Baquer (1993) Impaired antioxidant status in diabetic rat liver: Effect of vanadate. Biochem. Pharmacol. 45: 539-542. (Pubitemid 23064556)
48. Sanders, R. A., F. Rauscher, and J. Watkins (2001) Effects of quercetin on antioxidant defense in streptozotocin induced diabetic rats. J. Biochem. Mol. Tox. 15: 143-149. (Pubitemid 32514748)
49. Prabakaran, D. and N. Ashok kumar (2013) Protective effect of esculetin on hyperglycemia-mediated oxidative damage in the hepatic and renal tissues of experimental diabetic rats. Biochimie. 95: 366-373.
50. Maritim, A. C., R. Sanders, and J. Watkins III (2003) Diabetes, oxidative stress, and antioxidants: A review. J. Biochem. Mol. Toxic. 7: 24-38. (Pubitemid 36410972)
51. Bast, A., G. Wolf, I. Oberbaumer, and R. Walther (2002) Oxidative and nitrosative stress induces peroxiredoxins in pancreatic beta cells. Diabetol. 45: 867-876.
52. Hwang, H. J., S. Kim, Y. Baek, S. Lee, H. Hwang, S. Kumar, M. Rahman, and J. Yun (2008) Differential expression of liver proteins in Streptozotocin- induced diabetic rats in response to hypoglycemic mushroom polysaccharides. Kor. J. Chem. Eng. 25: 308-322.
53. Wood, Z. A., E. Schröder, J. Harris, and L. Poole (2003) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28: 32-40. (Pubitemid 36051004)
54. Raza, H., M. Robin, J. Fang, and N. Avadhani (2002) Multiple isoforms of mitochondrial glutathione S-transferases and their differential induction under oxidative stress. Biochem. J. 366: 45-55. (Pubitemid 34971802)
55. Sun, H. D., Y. Ru, D. Zhang, S. Yin, L. Yin, Y. Xie, Y. Guan, and S. Liu (2012) Proteomic analysis of glutathione S-transferase isoforms in mouse liver mitochondria. World J. Gastroenterol. 18: 3435-3442.
56. Sindhu, R. K., J. Koo, C. Roberts, and N. Vaziri (2004) Dysregulation of hepatic superoxide dismutase, catalase and glutathione peroxidase in diabetes: Response to insulin and antioxidant therapies. Clin. Exp. Hypertns. 26: 43-53. (Pubitemid 38248221)
57. Miller, A. L. (2003) The Methionine-homocysteine cycle and its effects on cognitive diseases. Altern. Med. Rev. 8: 7-19.
58. Lee, A. S. (2001) The glucose-regulated proteins: Stress induction and clinical applications. Trends Biochem. Sci. 26: 504-510.
59. Yu, Z. F., H. Luo, W. Fu, and M. Mattson (1999) The endoplasmic reticulum stress-responsive protein GRP78 protects neurons against excitotoxicity and apoptosis: Suppression of oxidative stress and stabilization of calcium homeostasis. Exp. Neurol. 155: 302-314. (Pubitemid 29124724)
60. Szántó I., P. Gergely, Z. Marcsek, T. Bányá sz, J. Somogyi, and P. Csermely (1994) Changes of the 78 kDa glucose-regulated protein (grp78) in livers of diabetic rats. Acta Physiol. Hung. 83: 333-342.
61. Hartman, D. J., N. Hoogenraad, R. Condron, and P. Høj (1992) Identification of a mammalian 10-kDa heat shock protein, a mitochondrial chaperonin 10 homologue essential for assisted folding of trimeric ornithine transcarbamoylase in vitro. Proc. Natl. Acad. Sci. 89: 3394-3398.
62. Johnson, B. J., T. Le, C. Dobbin, T. Banovic, C. Howard, F. Flores, D. Vanags, D. Naylor, G. Hill, and A. Suhrbier (2005) Heat shock protein 10 inhibits lipopolysaccharide-induced inflammatory mediator production. J. Biol. Chem. 280: 4037-4047. (Pubitemid 40288567)
63. Takizawa, S., T. Endo, X. Wanjia, S. Tanaka, M. Takahashi, and T. Kobayashi (2009) HSP 10 is a new autoantigen in both autoimmune pancreatitis and fulminant type 1 diabetes. Biochem. Biophys. Res. Commun. 386: 192-196.
64. Merk, M., R. Mitchell, S. Endres, and R. Bucala (2012) D-dopachrome tautomerase (D-DT or MIF-2): Doubling the MIF cytokine family. Cytokine 59: 10-17.
65. Sugimoto, H., M. Taniguchi, A. Nakagawa, I. Tanaka, M. Suzuki, and J. Nishihira (1999) Crystal structure of human D-Dopachrome tautomerase, a homologue of macrophage migration inhibitory factor, at 1.54 Å resolution. Biochem. 38: 3268-3279.