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Mammalian Genome

, Volume 15, Issue 6, pp 433–451 | Cite as

Mouse testis transcriptome revealed using serial analysis of gene expression

  • Junjie Yao
  • Takuya Chiba
  • Jun Sakai
  • Kunitaka Hirose
  • Mikio Yamamoto
  • Akiyuki Hada
  • Kazunao Kuramoto
  • Keiichi Higuchi
  • Masayuki Mori
Article

Abstract

We applied serial analysis of gene expression (SAGE) to the mouse testis to reveal the global gene expression profile and to identify senescence-dependent changes in that profile. A total of 61,929 SAGE tags, including 19,323 unique tags, were obtained from 3- and 29-month-old BDF1 mice and 14-month-old SAMP1 mice. Genes highly expressed in the testis included those associated with spermatogenesis, protein metabolism, energy metabolism, growth and differentiation, and signal transduction. Testes from old mice of both strains appeared atrophied. Morphological examination of aged testes revealed extremely thin seminiferous epithelia and significantly decreased numbers of spermatids and spermatocytes. Despite the physical deterioration, no gross changes in the gene expression profile were apparent in the testes of old BDF1 mice. However, in 14-month-old SAMP1 mice, protamine 2 gene transcription was approximately 50% lower than in BDF1 mice. This reduction may be associated with the oligozoospermia and early decline in reproductive performance of SAMP1 mice. Our SAGE results are the first quantitative gene expression profile of the mouse testis and provide a reliable transcriptome reference for this organ.

Notes

Acknowledgments

This work was supported in part by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (11680819) and from the Japan Health Foundation for the Prevention of Chronic Diseases and the Improvement of QOL of Patients.

References

  1. Bodyak, N, Kang, PM, Hiromura, M, Sulijoadikusumo, I, Horikoshi, N, Khrapko, K, Usheva, A 2002Gene expression profiling of the aging mouse cardiac myocytesNucleic Acids Res3037883794CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bronikowski, AM, Carter, PA, Morgan, TJ, Garland, T,Jr, Ung, N, Pugh, TD, Weindruch, R, Prolla, TA 2003Lifelong voluntary exercise in the mouse prevents age-related alterations in gene expression in the heartPhysiol Genomics127172CrossRefGoogle Scholar
  3. Cao, SX, Dhahbi, JM, Mote, PL, Spindler, SR 2001Genomic profiling of short- and long-term caloric restriction effects in the liver of aging miceProc Natl Acad Sci USA981063010635CrossRefPubMedGoogle Scholar
  4. Chen, H, Centola, M, Altschul, SF, Metzger, H 1998Characterization of gene expression in resting and activated mast cellsJ Exp Med18816571668CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cho, C, Willis, WD, Goulding, EH, Jung-Ha, H, Choi, Y-C, Hecht, NB, Eddy, EM 2001Haploinsufficiency of protamine-1 or -2 causes infertility in miceNat Genet288286PubMedGoogle Scholar
  6. Eddy, EM, O’Brien, DA 1998Gene expression during mammalian meiosisHandel, MA eds. Meiosis and GametogenesisAcademic PressLondon141200Google Scholar
  7. Eddy, EM, Welch, JE, O’Brien, DA 1993Gene expression during spermatogenesisKrester, DM eds. Cellular and Molecular Mechanisms in Male ReproductionAcademic PressLondon181232Google Scholar
  8. Fujii, T, Tamura, K, Masai, K, Tanaka, H, Nishimune, Y, Nojima, H 2002Use of stepwise subtraction to comprehensively isolate mouse genes whose transcription is up-regulated during spermatogenesisEMBO Report.367372CrossRefGoogle Scholar
  9. Gu, W, Kwon, Y, Oko, R, Hermo, L, Hecht, NB 1995Poly (A) binding protein is bound to both stored and polysomal mRNAs in the mammalian testisMol Reprod Dev40273285CrossRefPubMedGoogle Scholar
  10. Hecht, NB 1998Molecular mechanisms of male germ cell differentiationBioEssays20555561CrossRefPubMedGoogle Scholar
  11. Heidaran, MA, Showman, RM, Kistler, WS 1998A cytochemical study of the transcriptional and translational regulation of nuclear transition protein 1 (TP1), a major chromosomal protein of mammalian spermatidsJ Cell Biol10614271433CrossRefGoogle Scholar
  12. Higuchi, K, Hosokawa, M, Takeda, T 1999Senescence-accelerated mouseMethods Enzymol309674686CrossRefPubMedGoogle Scholar
  13. Jiang, CH, Tsien, JZ, Schultz, PG, Hu, Y 2001The effects of aging on gene expression in the hypothalamus and cortex of miceProc Natl Acad Sci USA9819301934CrossRefPubMedGoogle Scholar
  14. Kim, GH, Wright, WW 1997A comparison of the effects of testicular maturation and aging on the stage-specific expression of CP-2/cathepsin L messenger ribonucleic acid by Sertoli cells of the Brown Norway ratBiol Reprod5714671477CrossRefPubMedGoogle Scholar
  15. Kleene, KC, Distel, RJ, Hecht, NB 1984Translational regulation and deadenylation of a protamine mRNA during spermiogenesis in the mouseDev Biol1057179CrossRefPubMedGoogle Scholar
  16. Kleene, KC, Wang, MY, Cutler, M, Hall, C, Shih, D 1994Developmental expression of poly(A) binding protein mRNAs during spermatogenesis in the mouseMol Reprod Dev39355364CrossRefPubMedGoogle Scholar
  17. Lee, CK, Klopp, RG, Weindruch, R, Prolla, TA 1999Gene expression profile of aging and its retardation by caloric restrictionScience28513901393CrossRefPubMedGoogle Scholar
  18. Lee, CK, Weindruch, R, Prolla, TA 2000Gene-expression profile of the ageing brain in miceNat Genet25294297CrossRefPubMedGoogle Scholar
  19. Miyamoto, H, Manabe, N, Akiyama, Y, Mitani, Y, Sugimoto, M, Sato, E 1994Quantitative studies on spermatogenesis in the senescence accelerated mouseTakeda, T eds. The SAM Model of SenescenceElsevier ScienceAmsterdam275278Google Scholar
  20. O’Shaughnessy, PJ, Fleming, L, Baker, PJ, Jackson, G, Johnston, H 2003Identification of developmentally regulated genes in the somatic cells of the mouse testis using serial analysis of gene expressionBiol Reprod69797808CrossRefPubMedGoogle Scholar
  21. Ryo, A, Kondoh, N, Wakatsuki, T, Hada, A, Yamamoto, N, Yamamoto, M 2000A modified serial analysis of gene expression that generates longer sequence tags by nonpalindromic cohesive linker ligationAnal Biochem277160162CrossRefPubMedGoogle Scholar
  22. Schultz, N, Hamra, FK, Garbers, DL 2003A multitude of genes expressed solely in meiotic or postmeiotic spermatogenic cells offers a myriad of contraceptive targetsProc Natl Acad Sci USA1001220112206CrossRefPubMedGoogle Scholar
  23. Syed, V, Hecht, NB 2001Selective loss of Sertoli cell and germ cell function leads to a disruption in Sertoli cell-germ cell communication during aging in the Brown Norway ratBiol Reprod64107112CrossRefPubMedGoogle Scholar
  24. Tanemura, K, Kurohmaru, M, Kuramoto, K, Hayashi, Y 1993Age-related morphological changes in the testis of the BDF1 mouseJ Vet Med Sci55703710CrossRefPubMedGoogle Scholar
  25. Velculescu, VE, Zhang, L, Vogelstein, B, Kinzler, KW 1995Serial analysis of gene expressionScience270484487CrossRefPubMedGoogle Scholar
  26. Wreford, NG, Rajendra Kumar, T, Matzuk, MM, Kretser, DM 2001Analysis of the testicular phenotype of the follicle-stimulating hormone beta-subunit knockout and the activin type II receptor knockout mice by stereological analysisEndocrinology14229162920CrossRefPubMedGoogle Scholar
  27. Yamamoto, M, Wakatsuki, T, Hada, A, Ryo, A 2001Use of serial analysis of gene expression (SAGE) technologyJ Immunol Methods2504566CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Junjie Yao
    • 1
  • Takuya Chiba
    • 2
  • Jun Sakai
    • 3
  • Kunitaka Hirose
    • 3
  • Mikio Yamamoto
    • 4
  • Akiyuki Hada
    • 4
  • Kazunao Kuramoto
    • 5
  • Keiichi Higuchi
    • 1
  • Masayuki Mori
    • 1
  1. 1.Department of Aging BiologyInstitute on Aging and Adaptation, Shinshu University Graduate School of MedicineMatsumotoJapan
  2. 2.Department of Pathology 1Nagasaki University School of Medicine, 1-12-4 SakamotoNagasakiJapan
  3. 3.Biomedical Research LaboratoriesKureha Chemical Industry CO., LTD., 3-26-2 HyakuninchoShinjuku-kuJapan
  4. 4.Department of Biochemistry IINational Defense Medical College, 3-2 NamikiTokorozawaJapan
  5. 5.Department of Laboratory Animal ScienceTokyo Metropolitan Institute of Gerontology, 35-2 Sakae-choItabashi-kuJapan

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