T3 fails to restore mitochondrial thiol redox status altered by experimental hypothyroidism in rat testis

General and Comparative Endocrinology

Volumn 169, Issue 1, 2010, Pages 39-47

  Chattopadhyay, Sutapa ^a   Choudhury, Supragyanshree ^a   Roy, Anita ^a   Chainy, Gagan B N ^a   Samanta, Luna ^a  

^a UTKAL UNIVERSITY   (India)

Author keywords

Antioxidant defenses; Hypothyroidism; Mitochondria; Oxidative stress; Spermatogenesis; State III respiration; State IV respiration; Sub mitochondrial particles; Testis; Thyroid hormone

Indexed keywords

LIOTHYRONINE;

ANIMAL; ARTICLE; DRUG EFFECT; HYPOTHYROIDISM; MALE; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PATHOPHYSIOLOGY; RAT; TESTIS; WISTAR RAT;

ANIMALS; HYPOTHYROIDISM; MALE; MITOCHONDRIA; OXIDATION-REDUCTION; OXIDATIVE STRESS; RATS; RATS, WISTAR; TESTIS; TRIIODOTHYRONINE;

EID: 77956619995     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2010.07.014     Document Type: Article

References (64)

1. Ahmed A.F., Whelan J., Jequier A.M., Cummins J.M. Torsion-induced injury in rat testes does not affect mitochondrial respiration or the accumulation of mitochondrial mutations. Int. J. Androl. 2000, 23:347-356.
2. Andreyev A.Y., Kushnareva Y.E., Starkov A.A. Mitochondrial metabolism of reactive oxygen species. Biochemistry (Moscow) 2005, 70:200-214.
3. Aust S.D., Morehouse L.A., Thomas C.E. Role of metals in oxygen radical reactions. J. Free Radic. Biol. Med. 1985, 1:3-25.
4. Canale D., Agostini M., Giorgilli G., Caglieresi C., Scartabelli G., Nardini V., Jannini E.A., Martino E., Pinchera A., Macchia E. Thyroid hormone receptors in neonatal, prepubertal and adult rat testis. J. Androl. 2001, 22:284-288.
5. Carmagnol F., Sinet P.M., Jerome H. Selenium-dependent and non-selenium-dependent glutathione peroxidases in human tissue extracts. Biochim. Biophys. Acta 1983, 759:49-57.
6. Chance B., Seis H., Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 1979, 59:527-605.
7. 3 on rat heart superoxide dismutase, catalase and lipid peroxidation. Indian J. Exp. Biol. 2003, 41:846-849.
8. Chattopadhyay S., Sahoo D.K., Roy A., Samanta L., Chainy G.B.N. Thiol redox status critically influences mitochondrial response to thyroid hormone-induced hepatic oxidative injury: a temporal analysis. Cell Biochem. Funct. 2010, 28:126-134.
9. Chattopadhyay S., Sahoo D.K., Subudhi U., Chainy G.B.N. Differential expression profiles of antioxidant enzymes and glutathione redox status in hyperthyroid rats: a temporal analysis. Comp. Biochem. Physiol. C 2007, 146:383-391.
10. Choudhury S., Chainy G.B.N., Mishro M.M. Experimentally induced hypo- and hyper-thyroidism influence on the antioxidant defence system in adult rat testis. Andrologia 2003, 35:131-140.
11. Das K., Samanta L., Chainy G.B.N. A modified spectrophotometric assay of superoxide dismutase using nitrite formation of superoxide radicals. Indian J. Biochem. Biophys. 2000, 37:201-204.
12. de Haan J.B., Bladier C., Griffiths P., Kelner M., O'Shea R.D., Cheung N.S., Bronson R.T., Silvestro M.J., Wild S., Zheng S.S., Beart P.M., Hertzog P.J., Kola I. Mice with a homozygous null mutation for the most abundant glutathione peroxidase, GPx1, show increased susceptibility to the oxidative stress-inducing agents paraquat and hydrogen peroxide. J. Biol. Chem. 1998, 273:22528-22536.
13. Faraone-Mennella M.R., Ferone A., Marino L., Cardone A., Comitato R., Venditti P., Di Meo S., Farina B. Poly(ADP-ribosyl)lation of proteins and germ cell development in hyperthyroid testis. Mol. Cell Biochem. 2009, 323:119-129.
14. Fernandez V., Tapia G., Varela P., Castillo I., Mora C., Moya F., Orellana M., Videla L.A. Redox up-regulated expression of rat liver manganese superoxide dismutase and Bcl-2 by thyroid hormone is associated with inhibitor of κB-α phosphorylation and nuclear factor-κB activation. J. Endocrinol. 2005, 186:539-547.
15. Fernandez V., Videla L.A. Hepatic glutathione biosynthetic capacity in hyperthyroid rats. Toxicol. Lett. 1996, 89:85-89.
16. Folgero T., Bertheussen K., Lindal S., Torbergsen T., Oian P. Mitochondrial disease and reduced sperm motility. Hum. Reprod. 1993, 8:1863-1868.
17. Francavilla S., Cordeschi G., Properzi G., Di Cicco L., Jannini E.A., Palmero S., Fugassa E., Loras B., D'Armiento M. Effect of thyroid hormone on the pre- and post-natal development of the rat testis. J. Endocrinol. 1991, 129:35-42.
18. Franco M.C., Arciuch V.G.A., Peralta J.G., Galli S., Levisman D., Lopez L.M., Romorini L., Poderoso J.J., Carreras M.C. Hypothyroid phenotype is contributed by mitochondrial complex I inactivation due to translocated neuronal nitric oxide synthase. J. Biol. Chem. 2006, 281:4779-4786.
19. Gomez Dumm C.L., Cortizo A.M., Gagliardino J.J. Morphological and functional changes in several endocrine glands induced by hypothyroidism in the rat. Acta Anatomica 1985, 124:81-87.
20. Griffith O.W. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 1980, 106:207-212.
21. Guerrero A., Pamplona R., Portero-Otin M., Barja G., Lopez-Torres M. Effect of thyroid status on lipid composition and peroxidation in the mouse liver. Free Radic. Biol. Med. 1999, 26:73-80.
22. 1-ATP synthase in rat liver. J. Bioenerg. Biomembr. 1998, 30:269-276.
23. Habig W.H., Pabst M.J., Jakoby W.B. Glutathione S-transferases. J. Biol. Chem. 1974, 249:713-739.
24. Hearn A.S., Fan L., Lepock J.R., Luba J.P., Greenleaf W.B., Cabelli D.E., Tainer J.A., Nick H.S., Silverman D.N. Amino acid substitution at the dimeric interface of human manganese superoxide dismutase. J. Biol. Chem. 2004, 279:5861-5866.
25. Holsberger D.R., Cooke P.S. Understanding the role of thyroid hormone in Sertoli cell development: a mechanistic hypothesis. Cell Tissue Res. 2005, 322:133-140.
26. Imai H., Suzuki K., Ishizaka K., Ichinose S., Oshima H., Okayasu I., Emoto K., Umeda M., Nakagawa Y. Failure of the expression of phospholipid hydroperoxide glutathione peroxidase in the spermatozoa of human infertile males. Biol. Reprod. 2001, 64:674-683.
27. Jannini E.A., Ulisse S., D'Armiento M. Thyroid hormone and male gonadal function. Endocr. Rev. 1995, 16:443-459.
28. Knapen M.F.C.M., Zusterzeel P.L.M., Peters W.H.M., Steegers E.A.P. Glutathione and glutathione-related enzymes in reproduction. A review. Eur. J. Obstet. Gynecol. Reprod. Biol. 1999, 82:171-184.
29. Kowaltowski A.J., Vercesi A.E. Mitochondrial damage induced by conditions of oxidative stress. Free Radic. Biol. Med. 1999, 26:463-471.
30. Lebovitz R.M., Zhang H., Voge l.H., Cartwright J., Dionne L., Lu N., Huang S., Matzuk M.M. Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc. Natl. Acad. Sci. USA 1996, 93:9782-9787.
31. Levine R.L., Garland D., Oliver C.N., Amici A., Climent I., Lenz A.G., Ahn B.W., Shaltiel S., Stadtman E.R. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 1990, 186:464-478.
32. Lotscher H., Winterhalter K.H., Carafoli E., Richter C. Hydroperoxide-induced loss of pyridine nucleotides and release of calcium from rat liver mitochondria. J. Biol. Chem. 1980, 256:9325-9330.
33. Maran R.R., Aruldhas M.M. Adverse effects of neonatal hypothyroidism on Wistar rat spermatogenesis. Endocr. Res. 2002, 28:141-154.
34. Marjani A., Mansourian A.R., Ghaemi E.O., Ahmadi A., Khori V. Lipid perpxidation in the serum of hypothyroid patients (In Gorgan-South east of Caspian Sea). Asian J. Cell Biol. 2008, 3:47-50.
35. Martensson J., Meister A. Glutathione deficiency decreases tissue ascorbate levels in newborn rats: ascorbate spares glutathione and protects. Proc. Natl. Acad. Sci. USA 1991, 88:4656-4660.
36. Massey V., Williams C.H. On the reaction mechanism of yeast glutathione reductase. J. Biol. Chem. 1965, 240:4470-4481.
37. Mendis-Handagama S.M., Siril Ariyaratne H.B. Leydig cells, thyroid hormones and steroidogenesis. Indian J. Exp. Biol. 2005, 43:939-962.
38. Mitsui A., Ohta T. Photooxidative consumption and photoreductive formation of ascorbic acid in green leaves. Plant Cell Physiol. 1961, 2:31-44.
39. Moreno M., Lanni A., Lombardi A., Goglia F. How the thyroid controls metabolism in the rat: different roles for triiodothyronine and diiodothyronines. J. Physiol. 1997, 505:529-538.
40. Ohkawa H., Ohishi N., Yagi K. Assay for lipid peroxides in animal tissue by thiobarbituric acid reaction. Anal. Biochem. 1979, 95:351-358.
41. Olsvik P.A., Kristensen T., Waagbo R., Rosseland B.O., Tollefsen K.E., Baeverfjord G., Berntssen M.H.G. MRNA expression of antioxidant enzymes (SOD, CAT and GSH-Px) and lipid peroxidative stress in liver of Atlantic salmon (Salmo salar) exposed to hyperoxic water during smoltification. Comp. Biochem. Physiol. 2005, 141:314-323.
42. Paglia D.E., Valentine W.N. Studies on quantitative characterization of erythrocyte glutathione peroxidase. J. Lab. Clin. Med. 1967, 70:158-169.
43. Pamplona R., Portero-Otin M., Ruiz C., Bellmunt M.J., Requena J.R., Thorpe S.R., Baynes J.W., Romero M., Lopez-Torres M., Barja G. Thyroid status modulates glycoxidative and lipoxidative modification of tissue proteins. Free Radic. Biol. Med. 1999, 27:901-910.
44. Pick E., Keisari Y. Superoxide anion and hydrogen peroxide production by chemically elicited peritoneal macrophages-induction by multiple nonphagocytic stimuli. Cell Immunol. 1981, 59:301-318.
45. Robb G.W., Amann R.P., Killian G.J. Daily sperm production and epididymal sperm reserves of pubertal and adult rats. J. Reprod. Fertil. 1978, 54:103-107.
46. Rosenblum E., Gavaler J.S., Van Thiel D.H. Lipid peroxidation: a mechanism for ethanol-associated testicular injury in rats. Endocrinology 1985, 116:311-318.
47. Sahoo D.K., Roy A., Bhanja S., Chainy G.B.N. Experimental hyperthyroidism-induced oxidative stress and impairment of antioxidant defence system in rat testis. Indian J. Exp. Biol. 2005, 43:1058-1067.
48. Sahoo D.K., Roy A., Bhanja S., Chainy G.B.N. Hypothyroidism impairs antioxidant defence system and testicular physiology during development and maturation. Gen. Comp. Endocrinol. 2008, 156:63-70.
49. 3 treatment on glutathione redox pool and its metabolizing enzymes in mitochondrial and post-mitochondrial fractions of adult rat testes. Indian J. Exp. Biol. 2007, 45:338-346.
50. Sakai Y., Yamashina S., Furudate S. Developmental delay and unstable state of the testes in the rdw rat with congenital hypothyroidism. Dev. Growth Diff. 2004, 46:327-334.
51. Samanta L., Chainy G.B.N. Comparison of hexachlorocyclohexane-induced oxidative stress in the testis of immature and adult rats. Comp. Biochem. Physiol. 1997, 118C:319-327.
52. Schoolwerth A.C., LaNoue K.F. The role of microcompartmentation in the regulation of glutamate metabolism by rat kidney mitochondria. J. Biol. Chem. 1980, 255:3403-3411.
53. Sedlak J., Lindsay R.H. Estimation of total, protein-bound and non-protein sulfydryl groups in tissue with Ellman's reagent. Anal. Biochem. 1968, 25:192-205.
54. Sies H. Glutathione and its role in cellular functions. Free Radic. Biol. Med. 1999, 27:916-921.
55. Tahmaz L., Gokalp A., Kibar Y., Kocak I., Yalcin O., Ozercan Y. Effect of hypothyroidism on the testes in mature rats and treatment with levothyroxine and zinc. Andrologia 2000, 32:85-89.
56. Tas S., Dirican M., Sarandol E., Serdar Z. The effect of taurine supplementation on oxidative stress in experimental hypothyroidism. Cell Biochem. Funct. 2006, 24:153-158.
57. Tietze F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione; applications to mammalian blood and other tissue. Anal. Biochem. 1969, 27:502-522.
58. Venkatesh S., Deecaraman M., Kumar R., Shamsi M.B., Dada R. Role of reactive oxygen species in the pathogenesis of mitochondrial DNA (mtDNA) mutations in male fertility. Indian J. Med. Res. 2009, 129:127-137.
59. Wajner S.M., Wagner M.S., Melo R.C., Parreira G.G., Chiarini-Garcia H., Bianco A.C., Fekete C., Sanchez E., Lechan R.M., Maia A.L. Type 2 iodothyronine deiodinase is highly expressed in germ cells of adult rat testis. J. Endocrinol. 2007, 194:47-54.
60. Winkler B.S., Orselli S.M., Rex T.S. The redox couple between glutathione and ascorbic acid: a chemical and physiological perspective. Free Radic. Biol. Med. 1994, 17:333-349.
61. Wrutniak-Cabello C., Casa F., Cabello G. Thyroid hormone action in mitochondria. J. Mol. Endocrinol. 2001, 26:67-77.
62. Wudarczyk J., Debska G., Lenartowicz E. Relation between the activities reducing disulfides and the protection against membrane permeability transition in rat liver mitochondria. Arch. Biochem. Biophys. 1996, 327:215-221.
63. Yilmaz S., Ozan S., Benzer F., Canatan H. Oxidative damage and antioxidant enzyme activities in experimental hypothyroidism. Cell Biochem. Funct. 2003, 21:325-330.
64. Zamoner A., Barreto K.P., Filho D.W., Sell F., Woehl V.M., Guma F.C.R., Pessoa-Pureur R., Silva F.R.M.B. Propylthiouracil-induced congenital hypothyroidism upregulates vimentin phosphorylation and depletes antioxidant defenses in immature rat testis. J. Mol. Endocrinol. 2008, 40:125-135.