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Carbonyl stress and detoxification ability in the male genital tract and testis of rats

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Abstract

Carbonyl compounds, which are naturally produced and augmented under oxidative stress, have deleterious effects on the reproductive system. The aldo-keto reductase (AKR) family of enzymes catalyze the reductive detoxification of various carbonyl compounds in an NADPH-dependent manner. To elucidate involvement of AKR in detoxification of endogenously produced carbonyls in the male reproductive system, we investigated the differential expression and tissue localization of aldehyde reductase (ALR) and protein adducts produced by reaction with lipid peroxidation products. A strong immunoreactivity to an anti-ALR antibody was observed in the epithelia of the epididymis, vas deferens, seminal vesicle, and prostate gland. Virtually the same cells were stained with a monoclonal antibody (mAb) 5F6, raised against an acrolein-modified protein. In the testis, however, mAb5F6 specifically stained the nuclei of somatic cells and less differentiated spermatogenic cells. While acrolein inactivated glutathione reductase, an enzyme involved in recycling oxidized glutathione, AKR activity was affected at the high concentration only. The colocalization of lipid peroxidation products and AKR in the epithelia of the male genital tract indicates that these tissues are exposed to oxidative stress and possess a protective system coordinately.

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References

  • Baynes JW, Thorpe SR (1999) Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes 48:1–9

    CAS  PubMed  Google Scholar 

  • Fujii J, Takahashi M, Hamaoka R, Kawasaki Y, Miyazawa N, Taniguchi N (1999) Physiological relevance of aldehyde reductase and aldose reductase gene expression. Adv Exp Med Biol 463:419–426

    CAS  PubMed  Google Scholar 

  • Fujii T, Hamaoka R, Fujii J, Taniguchi N (2000) Redox capacity of cells affects inactivation of glutathione reductase by nitrosative stress. Arch Biochem Biophys 378:123–130

    Article  CAS  PubMed  Google Scholar 

  • Fujii J, Iuchi Y, Matsuki S, Ishii T (2003) Cooperative function of antioxidant and redox systems against oxidative stress in male reproductive tissues. Asian J Androl 5:231–242

    CAS  PubMed  Google Scholar 

  • Grimes SR Jr, Henderson N (1984) Hyperacetylation of histone H4 in rat testis spermatids. Exp Cell Res 152:91–97

    CAS  PubMed  Google Scholar 

  • Halliwell B, Gutteridge JMC (1999) In: Free radical biology and medicine, 3rd edn. Clarendon, Oxford

  • Iuchi Y, Kobayashi T, Kaneko T, Takahara M, Ogino T, Fujii J (2001) The expression of a Y-box protein, YB2/RYB-a, precedes protamine 2 during spermatogenesis in rodents. Mol Hum Reprod 7:1023–1031

    Article  CAS  PubMed  Google Scholar 

  • Jez JM, Bennett MJ, Schlegel BP, Lewis M, Penning TM (1997) Comparative anatomy of the aldo-keto reductase superfamily. Biochem J 326:625–636

    CAS  PubMed  Google Scholar 

  • Kaneko T, Iuchi Y, Kawachiya S, Fujii T, Saito H, Kurachi H, Fujii J (2001) Alteration of glutathione reductase expression in the female reproductive organs during the estrous cycle. Biol Reprod 65:1410–1416

    CAS  PubMed  Google Scholar 

  • Kaneko T, Iuchi Y, Kobayashi T, Fujii T, Saito H, Kurachi H, FujiiJ (2002) Expression of glutathione reductase in the male reproductive system of rats supports the enzymatic basis of glutathione function in spermatogenesis. Eur J Biochem 269:1570–1578

    Article  CAS  PubMed  Google Scholar 

  • Kaneko T, Iuchi Y, Takahashi M, Fujii J (2003) Colocalization of polyol-metabolizing enzymes and immunological detection of fructated proteins in the female reproductive system of the rat. Histochem Cell Biol 119:309–315

    CAS  PubMed  Google Scholar 

  • Kehrer JP, Biswal SS (2000) The molecular effects of acrolein. Toxicol Sci 57:6–15

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi T, Kaneko T, Iuchi Y, Matsuki S, Takahashi M, Sasagawa I, Nakada T, Fujii J (2002) Localization and physiological implication of aldose reductase and sorbitol dehydrogenase in male reproductive systems, accessory glands, and spermatozoa of rats. J Androl 23:674–683

    Google Scholar 

  • Kolb NS, Hunsaker LA, Vander Jagt DL (1994) Aldose reductase-catalyzed reduction of acrolein: implications in cyclophosphamide toxicity. Mol Pharmacol 45:797–801

    CAS  PubMed  Google Scholar 

  • Lefrancois-Martinez AM, Tournaire C, Martinez A, Berger M, Daoudal S, Tritsch D, Veyssiere G, Jean C (1999) Product of side-chain cleavage of cholesterol, isocaproaldehyde, is an endogenous specific substrate of mouse vas deferens protein, an aldose reductase-like protein in adrenocortical cells. J Biol Chem 274:32875–32880

    Article  CAS  PubMed  Google Scholar 

  • Ludvigson MA, Sorenson RL (1980) Immunohistochemical localization of aldose reductase. I. Enzyme purification and antibody preparation: localization in peripheral nerve, artery, and testis. Diabetes 29:438–449

    CAS  PubMed  Google Scholar 

  • Ludvigson MA, Waites GM, Hamilton DW (1982) Immunocytochemical evidence for the specific localization of aldose reductase in rat Sertoli cells. Biol Reprod 26:311–317

    CAS  PubMed  Google Scholar 

  • Meistrich ML, Trostle-Weige PK, Lin R, Bhatnagar YM, Allis CD (1992) Highly acetylated H4 is associated with histone displacement in rat spermatids. Mol Reprod Dev 31:170–181

    CAS  PubMed  Google Scholar 

  • Nishi N, Shoji H, Miyanaka H, Nakamura T (2000) Androgen-regulated expression of a novel member of the aldo-keto reductase superfamily in regrowing rat prostate. Endocrinology 141:3194–3199

    CAS  PubMed  Google Scholar 

  • Oya T, Hattori N, Mizuno Y, Miyata S, Maeda S, Osawa T, Uchida K (1999) Methylglyoxal modification of protein. Chemical and immunochemical characterization of methylglyoxal-arginine adducts. J Biol Chem 274:18492–18502

    CAS  PubMed  Google Scholar 

  • Stadtman ER (2001) Protein oxidation in aging and age-related diseases. Ann N Y Acad Sci 928:22–38

    CAS  PubMed  Google Scholar 

  • Takahashi M, Fujii J, Teshima T, Suzuki K, Shiba T, Taniguchi N (1993) Identity of a major 3-deoxyglucosone-reducing enzyme with aldehyde reductase in rat liver established by amino acid sequencing and cDNA expression. Gene 127:249–253

    Article  CAS  PubMed  Google Scholar 

  • Takahashi M, Fujii J, Miyoshi E, Hoshi A, Taniguchi N (1995) Elevation of aldose reductase gene expression in rat primary hepatoma and hepatoma cell lines. Implication of cytotoxic aldehydes. Int J Cancer 62:749–754

    CAS  PubMed  Google Scholar 

  • Takahashi M, Hoshi A, Fujii J, Miyoshi E, Kasahara T, Suzuki K, Aozasa K, Taniguchi N (1996) Induction of aldose reductase gene expression in LEC rats during the development of the hereditary hepatitis and hepatoma. Jpn J Cancer Res 87:337–341

    Google Scholar 

  • Uchida K (2000) Role of reactive aldehyde in cardiovascular diseases. Free Radic Biol Med 28:1685–1696

    Article  CAS  PubMed  Google Scholar 

  • Uchida K, Kanematsu M, Sakai K, Matsuda T, Hattori N, Mizuno Y, Suzuki D, Miyata T, Noguchi N, Niki E, Osawa T (1998) Protein-bound acrolein: potential markers for oxidative stress. Proc Natl Acad Sci U S A 95:4882–4887

    Article  CAS  PubMed  Google Scholar 

  • Vander Jagt DL, Robinson B, Taylor KK, Hunsaker LA (1992) Reduction of trioses by NADPH-dependent aldo-keto reductases: aldose reductase, methylglyoxal, and diabetic complications. J Biol Chem 267:4364–4369

    PubMed  Google Scholar 

  • Vander Jagt DL, Kolb NS, Vander Jagt TJ, Chino J, Martinez FJ, Hunsaker LA, Royer RE (1995) Substrate specificity of human aldose reductase: identification of 4-hydroxynonenal as an endogenous substrate. Biochim Biophys Acta 1249:117–126

    PubMed  Google Scholar 

  • Vander Jagt DL, Hunsaker LA, Vander Jagt TJ, Gomez MS, Gonzales DM, Deck LM, Royer RE (1997) Inactivation of glutathione reductase by 4-hydroxynonenal and other endogenous aldehydes. Biochem Pharmacol 53:1133–1140

    Article  PubMed  Google Scholar 

  • Warren JC, Murdock GL, Ma Y, Goodman SR, Zimmer WE (1993) Molecular cloning of testicular 20 alpha-hydroxysteroid dehydrogenase: identity with aldose reductase. Biochemistry 32:1401–1406

    CAS  PubMed  Google Scholar 

  • Wermuth B, Monder C (1983) Aldose and aldehyde reductase exhibit isocorticosteroid reductase activity. Eur J Biochem 131:423–426

    CAS  PubMed  Google Scholar 

  • Yabe-Nishimura C (1998) Aldose reductase in glucose toxicity: a potential target for the prevention of diabetic complications. Pharmacol Rev 50:21–33

    CAS  PubMed  Google Scholar 

  • Yamada S, Kumazawa S, Ishii T, Nakayama T, Itakura K, Shibata N, Kobayashi M, Sakai K, Osawa T, Uchida K (2001) Immunochemical detection of a lipofuscin-like fluorophore derived from malondialdehyde and lysine. J Lipid Res 42:1187–1196

    CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported, in part, by the 21st Century COE Program and Grant-in-Aid for Young Scientists (B) (number 14770797) and JSPS Fellows (number 13007321) from the Japan Society for the Promotion of Science (JSPS).

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Authors and Affiliations

  1. Department of Biochemistry, Yamagata University School of Medicine, 2-2-2 Iidanishi, 990-9585, Yamagata, Japan

    Yoshihito Iuchi, Tomoko Kaneko, Shingo Matsuki, Tatsuya Ishii, Yoshitaka Ikeda & Junichi Fujii

  2. Laboratory of Food and Biodynamics, Graduate School of Bioagricultural Science, Nagoya University, 464-8601, Nagoya, Japan

    Koji Uchida

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  1. Yoshihito Iuchi
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  2. Tomoko Kaneko
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  3. Shingo Matsuki
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  4. Tatsuya Ishii
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  5. Yoshitaka Ikeda
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  6. Koji Uchida
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  7. Junichi Fujii
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Correspondence to Junichi Fujii.

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Iuchi, Y., Kaneko, T., Matsuki, S. et al. Carbonyl stress and detoxification ability in the male genital tract and testis of rats. Histochem Cell Biol 121, 123–130 (2004). https://doi.org/10.1007/s00418-003-0607-3

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