Protection of testis through antioxidant action of Mallotus roxburghianus in alloxan-induced diabetic rat model

Journal of Ethnopharmacology

Volumn 176, Issue , 2015, Pages 268-280

  Roy, Vikas Kumar ^a   Chenkual, Lalramdinthara ^a   Gurusubramanian, Guruswami ^a  

^a MIZORAM UNIVERSITY   (India)

Author keywords

Acutetoxicity; Antioxidantdefense; GC MS; Mallotus roxburghianus; Oxidativestress; PCNAexpression; Testicularhistopathology

Indexed keywords

AGENTS ACTING ON THE GENITAL SYSTEM; ALANINE AMINOTRANSFERASE; ALLOXAN; ANTIOXIDANT; ASPARTATE AMINOTRANSFERASE; BERGENIN; BETULIC ACID; CATALASE; CYCLINE; ESTER; EUPHORBIA EXTRACT; FATTY ACID; GLIBENCLAMIDE; GLUCOSE; GLUTATHIONE; GLUTATHIONE TRANSFERASE; MALLOTUS ROXBURGHIANUS EXTRACT; MALONALDEHYDE; PHENOL DERIVATIVE; PROTEIN; RICINOLEIC ACID; SUPEROXIDE DISMUTASE; TERPENE; TESTOSTERONE; UNCLASSIFIED DRUG; ANTIDIABETIC AGENT; PLANT EXTRACT;

ACUTE TOXICITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CELL PROLIFERATION; CHEMICAL COMPOSITION; CONTROLLED STUDY; DIABETES CONTROL; DIABETES MELLITUS; ENZYME ACTIVITY; GERM CELL; GLUCOSE BLOOD LEVEL; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; LD50; LIPID PEROXIDATION; MALE; MALLOTUS; MALLOTUS ROXBURGHIANUS; MASS FRAGMENTOGRAPHY; NONHUMAN; OXIDATIVE STRESS; PHYTOCHEMISTRY; PLANT LEAF; RAT; SEMINIFEROUS TUBULE; SPERMATOCYTE; STEROIDOGENESIS; TESTIS DISEASE; TESTIS WEIGHT; TESTOSTERONE BLOOD LEVEL; ANIMAL; BLOOD; DIABETES MELLITUS, EXPERIMENTAL; DRUG EFFECTS; KIDNEY; LIVER; MALLOTUS PHILIPPINENSIS; METABOLISM; ORGAN SIZE; PATHOLOGY; PHYTOTHERAPY; TESTIS; WISTAR RAT;

ANIMALS; ANTIOXIDANTS; CATALASE; DIABETES MELLITUS, EXPERIMENTAL; GLUTATHIONE; GLUTATHIONE TRANSFERASE; HYPOGLYCEMIC AGENTS; KIDNEY; LIVER; MALE; MALLOTUS PLANT; ORGAN SIZE; PHYTOTHERAPY; PLANT EXTRACTS; PLANT LEAVES; PROLIFERATING CELL NUCLEAR ANTIGEN; RATS, WISTAR; SUPEROXIDE DISMUTASE; TESTIS; TESTOSTERONE;

EID: 84946914908     PISSN: 03788741     EISSN: 18727573     Source Type: Journal    
DOI: 10.1016/j.jep.2015.11.006     Document Type: Article

References (76)

1. H. Aebi Catalase in vitro Methods Enzymol. 105 1984 121 126
2. A. Agarwal, S. Gupta, and S. Sikka The role of free radicals and antioxidants in reproduction Curr. Opin. Obstet. Gynecol. 18 2006 325 332
3. B. Altay, S. Cetinkalp, B. Doganavs Argil, M. Hekimgil, and B. Semerci Streptozotocin-induced diabetic effects on spermatogenesis with proliferative cell nuclear antigen immunostaining of adult rat testis Fertil. Steril. 80 2003 828 831
4. M.G. Alves, A.D. Martins, J.E. Cavaco, S. Socorro, and P.F. Oliveira Diabetes, insulin-mediated glucose metabolism and Sertoli/blood-testis barrier function Tissue Barriers 1 2 2013 1 10
5. K. Asada, M. Takahashi, and M. Nagate Assay and inhibitors of spinach superoxide dismutase Agric. Biol. Chem. 38 1974 471 473
6. H. Aybek, Z. Aybek, S. Rota, N. Sen, and M. Akbulut The effects of diabetes mellitus, age, and vitamin E on testicular oxidative stress Fertil. Steril. 90 2008 755 760
7. J. Ballester, M.C. Munoz, J. Dominguez, T. Rigau, J.J. Guinovart, and J.E. Rodriguez-Gil Insulin-dependent diabetes affects testicular function by FSH- and LH-linked mechanisms J. Androl. 25 2004 706 719
8. J.D. Bancroft, and M.N. Gamble Theory and Practice of Histological Techniques 5th edition 2002 Churchill-Livingstone Edinburgh, London 175
9. J.W. Baynes, and S.R. Thorpe Role of oxidative stress in diabetic complications: a new perspective on an old paradigm Diabetes 48 1999 1 9
10. J. Blasiak, M. Arabski, R. Krupa, K. Wozniak, M. Zadrozny, J. Kasznicki, M. Zurawska, and J. Drezewoski DNA damage and repair in type 2 diabetes mellitus Mutat. Res. 554 1-2 2004 297 304
11. L. Cai, S. Chen, T. Evans, D.X. Deng, K. Mukherjee, and S. Chakrabarti Apoptotic germ-cell death and testicular damage in experimental diabetes: prevention by endothelin antagonism Urol. Res. 28 2000 342 347
12. D.F. Cameron, F.T. Murray, and D.D. Drylie Interstitial compartment pathology and spermatogenic disruption in testes from impotent diabetic men Anat. Rec. 213 1985 53 62
13. M. Cheesbrough Medical Laboratory Manual for Tropical Countries 2 1991 479
14. A. Elgawish, M. Glomb, M. Friedlander, and V.M. Monnier Involvement of hydrogen peroxide in collagen cross linking by high glucose in vitro and in vivo J. Biol. Chem. 271 1996 12964 12971
15. U.F. Ezuruike, and J.M. Prieto The use of plants in the traditional management of diabetes in Nigeria: pharmacological and toxicological considerations J. Ethnopharmacol. 155 2014 857 924
16. J.B. Farrell, A. Deshmukh, and A.A. Baghaie Low testosterone and the association with type 2 diabetes Diabetes Educ. 34 2008 799 806
17. J. Fujii, Y. Iuchi, S. Matsuki, and T. Ishii Cooperative function of antioxidant and redox systems against oxidative stress in male reproductive tissues Asian J. Androl. 5 2003 231 242
18. A.G. Gornall, G.S. Bardwill, and M.M. David Determination of serum proteins by means of the biuret reaction J. Biol. Chem. 177 1949 751 766
19. E. Guneli, K. Tugyan, H. Ozturk, M. Gumustekin, S. Cilaker, and N. Uysal Effect of melatonin on testicular damage in streptozotocin-induced diabetes rats Eur. Surg. Res. 40 4 2008 354 360
20. G. Gurusubramanian, and V.K. Roy Expression of visfatin in alloxan-induced diabetic rat testis Acta Histochem. 116 2014 1462 1468
21. W.H. Habig, M.J. Pabst, and W.B. Jakoby The first enzymatic step in mercapturic acid formation J. Biol. Chem. 249 22 1974 7130 7139
22. O. Hammer, D.A.T. Harper, and P.D. Ryan PAST: palaeontological statistics software package for education and data analysis (version 1.86b) Palaeontol. Electron. 4 1 2001 9
23. J.E. Hilaly, Z.H. Israili, and B. Lyouss Acute and chronic toxicological studies of Ajuva Iva in experimental animals J. Ethnopharmacol. 91 2004 43 50
24. S.M. Hsu, L. Raine, and H. Fanger Use of avidin-biotin-peroxidase complex (ABC) in immunperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures J. Histochem. Cytochem. 29 1981 577 580
25. R. Hunt, R.T. Dean, and S.P. Wolff Hydroxyl radical production and autoxidative glycosylation Biochem. J. 256 1988 205 212
26. International Diabetes Federation, 2014. IDF Diabetes Atlas UPDATE 2014, 6th edition. Brussels, Belgium: International Diabetes Federation. (http://www.idf.org/diabetesatlas).
27. M.J. Kang, M.K. Kim, A. Terhune, J.K. Park, Y.H. Kim, and G.Y. Koh Cytoplasmic localization of cyclin D3 in seminiferous tubules during testicular development Exp. Cell Res. 234 1997 27 36
28. M. Kanter, C. Aktas, and M. Erboga Protective effects of quercetin against apoptosis and oxidative stress in streptozotocin-induced diabetic rat testis Food Chem. Toxicol. 50 2012 719 725
29. M. Kanter, C. Aktas, and M. Erboga Curcumin attenuates testicular damage, apoptotic germ cell death, and oxidative stress in streptozotocin-induced diabetic rats Mol. Nutr. Food Res. 57 2013 1578 1585
30. J. Karimi, M.T. Goodarzi, H. Tavilani, I. Khodadadi, and I. Amiri Relationship between advanced glycation end products and increased lipid peroxidation in semen of diabetic men Diabetes Res. Clin. Pract. 91 2011 61 66
31. A. Khaki, F. Fathiazad, M. Nouri, A.F. Khaki, N.A. Maleki, H.J. Khamnei, and P. Ahmadi Beneficial effects of quercetin on sperm parameters in streptozotocin-induced diabetic male rats Phytother. Res. 24 2010 1285 1291
32. M. Khan, R.A. Qureshi, M. Hussain, K. Mehmood, and R.A. Khan Hexane soluble extract of Mallotus philippensis (Lam.) Muell. Arg. root possesses anti-leukaemic activity Chem. Cent. J. 7 2013 157
33. H.S. Kim, H.K. Lim, M.W. Chung, and Y.C. Kim Antihepatotoxic activity of bergenin, the major constituent of Mallotus japonicus, on carbon tetrachloride-intoxicated J. Ethnopharmacol. 69 2000 79 83
34. P.O. Koh, and M.O. Kim Ethanol exposure decreases cell proliferation and increases apoptosis in rat testes J. Vet.-Med. Sci. 68 2006 1013 1017
35. R. Kumar, D.K. Patel, S.K. Prasad, D. Laloo, S. Krishnamurthy, and S. Hemalatha Type 2 antidiabetic activity of bergenin from the roots of Caesalpinia digyna Rottler Fitoterapia 83 2012 395 401
36. H. Lalhlenmawia, C.T. Kumarappan, B.B. Bhattacharjee, and S.C. Mandal Antidiabetic activity of Mallotus roxburghianus leaves in diabetic rats induced by streptozocin Pharmacologyonline 3 2007 244 254
37. H. Lalhlenmawia, S.C. Mandal, V. Lalremruata, T.C. Lalhriatpuii, and Zothanpuia In vitro antioxidant activity study of traditionally used plant Mallotus roxburghianus Muell Int. J. Res. Pharm. Sci. 3 1 2013 93 104
38. N. Lameire, W. Van Biesen, and R. Vanholder Acute renal failure The Lancet 365 2005 417 430
39. T.A. Loomis, and A.W. Hayes Loomis's Essentials of Toxicology 4th ed. 1996 Academic Press California 208 245
40. S. La Vignera, R. Condorelli, E. Vicari, R. D'Agata, and A.E. Calogero Diabetes mellitus and sperm parameters J. Androl. 33 2012 145 153
41. J.T. Litchfield Jr.; and F. Wilcoxon A simplified method of evaluating dose-effect experiments J. Pharmacol. Exp. Ther. 96 1949 99 113
42. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J. Biol. Chem. 193 1951 265 275
43. C. Mallidis, I. Agbaje, N. McClure, and S. Kliesch The influence of diabetes mellitus on male reproductive function: a poorly investigated aspect of male infertility Der Urologe 50 2011 33 37
44. M.F. Moghaddam, F.B.H. Ahmad, and A. Samzadeh-Kermani Biological activity of betulinic acid: a review Pharmacol. Pharm. 3 2012 119 123
45. M. Mohasseb, S. Ebied, M.A. Yehia, and N. Hussein Testicular oxidative damage and role of combined antioxidant supplementation in experimental diabetic rats J. Physiol. Biochem. 67 2011 185 194
46. S. Morgenstern, G. Kessler, J. Auebach, R. Flor, and B. Klein An automated p-nitrophenylphosphate serum alkaline phosphatase procedure for the auto-analyser Clin. Chem. 11 1965 876 888
47. C.J. Mullarkey, D. Edelstein, and M. Brownlee Free radical generation by early glycation products: a mechanism for accelerated atherogenesis in diabetes Biochem. Biophys. Res. Commun. 173 1990 932 939
48. J.T. Mukinda, and P.F.K. Eagles Acute and sub-chronic oral toxicity profiles of the aqueous extract of Polygala fruticosa in female mice and rats J. Ethnopharmacol. 128 2010 236 240
49. F. Nielsen, B.B. Mikkelsen, J.B. Nielsen, H.R. Andersen, and P. Grandjean Plasma malondialdehyde as biomarker for oxidative stress: reference interval and effects of life-style factors Clin. Chem. 43 1997 1209 1214
50. J.W. Nowicke, and M. Takahashi Pollen morphology, exine structure, and systematics of Acaphyloideae (Euphorbiaceae) Rev. Paleobotany Palynol. 121 2002 231 336
51. OECD Guideline for the Testing of Chemicals, 2001. OECD/OCDE 420. Acute oral toxicity - Fixed dose procedure. pp. 1-14.
52. H. Ohkawa, H. Oshini, and K. Yagi Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction Anal. Biochem. 95 1979 351 358
53. C. Palmeira, D. Santos, R. Seica, A.J. Moreno, and M. Santos Enhanced mitochondrial testicular antioxidant capacity in Goto-Kakizaki diabetic rats: role of coenzyme Q Am. J. Physiol. Cell Physiol. 281 2001 1023 1028
54. L. Piconi, L. Quagliaro, and A. Ceriello Oxidative stress in diabetes Clin. Chem. Lab. Med. 41 2003 1144 1149
55. M.F. Rahman, M.K. Siddiqui, and K. Jamil Effects of Vepacide (Azadirachta indica) on aspartate and alanine aminotransferase profiles in a subchronic study with rats Hum. Exp. Toxicol. 20 2001 243 249
56. I. Rahman, A. Kode, and S.K. Biswas Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method Nat. Protoc. 1 6 2007 3159 3165
57. V.S. Rana, M.S.M. Rawat, G. Pant, and A. Nagatsu Chemical constituents of antioxidant activity of Mallotus roxburghianus leaves Chem. Biodivers. 2 2005 792 798
58. S. Reitman, and S. Frankel A colorimetric method for the determination of serum glutamic oxalacetic and pyruvic transaminases Am. J. Clin. Pathol. 28 1957 58 59
59. G. Ricci, A. Catizone, R. Esposito, F.A. Pisanti, M.T. Vietri, and M. Galdieri Diabetic rat testes: morphological and functional alterations Andrologia 41 2009 361 368
60. C. Riviere, T.H.V. Nguyen, H.Q. Tran, G. Chataigne, H.N. Nguyen, B. Dejaegher, C. Tistaert, N.K.T. Thi, Y. Vander Heyden, V.M. Chau, and J. Quetin-Leclercq Mallotus species from Vietnamese mountainous areas: phytochemistry and pharmacological activities Phytochem. Rev. 9 2010 217
61. M. Salama, M. Tsuji, M. Tamura, and S. Kagawa Impact of aging and diabetes mellitus on the expression of the proliferating cell nuclear antigen in rat testicular tissue Arch. Androl. 40 1998 95 107
62. F.A.R. Sawiress, M.S. Ziada, W.S.F. Bebawy, and H.A. Amer Effect of ginseng extract supplementation on testicular functions in diabetic rats Endocr. Regul. 45 2011 139 148
63. P. Sharma, J. Parmar, P. Sharma, P. Verma, and P.K. Goyal Radiation induced testicular injury and its amelioration by Tinospora cordifolia (an Indian medicinal plant) extract Evid. Based Complement. Altern. Med. 2011 2011 9 643847 10.1155/2011/643847 Hindawi Publishing Corporation
64. K.K. Shivji, M.K. Kenny, and R.D. Wood Proliferating cell nuclear antigen is required for DNA excision repair Cell 69 2 1992 367 374
65. B. Shrilatha, and Muralidhara Early oxidative stress in testis and epididymal sperm in streptozotocin-induced diabetic mice: its progression and genotoxic consequences Reprod. Toxicol. 23 2007 578 587
66. K. Steger, I. Aleithe, H. Behre, and M. Bergman The proliferation of spermatogonia in normal and pathological human seminiferous epithelium: an immunohistochemical study using monoclonal antibodies against Ki-67 protein and proliferating cell nuclear antigen Mol. Hum. Reprod. 4 1998 227 233
67. T. Szkudelski, K. Kandulska, and M. Okulicz Alloxan in vivo does not only exert deleterious effects on pancreatic B cells Physiol. Res. 47 1998 343 346
68. X.Y. Tang, Q. Zhang, D.Z. Dai, H.J. Ying, Q.J. Wang, and Y. Dai Effects of strontium fructose 1,6-diphosphate on expression of apoptosis-related genes and oxidative stress in testes of diabetic rats Int. J. Urol. 15 3 2008 251 256
69. M. Valko, D. Leibfritz, J. Moncol, M.T.D. Cronin, M. Mazur, and J. Telser Free radicals and antioxidant in normal physiological function and human disease Int. J. Biochem. Cell Biol. 39 2007 44 84
70. WHO, 2000. General Guidelines for Methodologies on Research and Evaluation of Traditional Medicine. p. 80.
71. WHO, 2008. Traditional medicine. (http://www.who.int/mediacentre/factsheets/fs134/en/).
72. WHO World Health Organization WHO Traditional Medicine Strategy 2014-2023 2013 WHO Press Geneva, Switzerland
73. J.R. Williamson, K. Chang, K.S. Hasan, Y. Ido, T. Kawamura, J.R. Nyengaard, M. van den Enden, C. Kilo, and R.G. Tilton Hyperglycemic pseudohypoxia and diabetic complications Diabetes 42 1993 801 813
74. S.P. Wolff Diabetes mellitus and free radicals. Free radicals, transition metals and oxidative stress in the aetiology of diabetes mellitus and complications Br. Med. Bull. 49 1993 642 652
75. S.D. Yan, A.M. Schmidt, G.M. Anderson, J. Zhang, J. Brett, Y.S. Zou, D. Pinsky, and D. Stern Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptor/binding proteins J. Biol. Chem. 269 1994 9889 9897
76. L. Zeng, X.T. Kong, J.W. Su, T.L. Xia, Y.Q. Na, and Y.L. Guo Evaluation of germ-cell kinetics in infertile patients with proliferating cell nuclear antigen proliferating index Asian J. Androl. 3 2001 63 66