Skip to main content
SpringerLink
Log in

LPS-induced transient testicular dysfunction accompanied by apoptosis of testicular germ cells in mice

  • ORIGINAL PAPER
  • Published:
Medical Molecular Morphology Aims and scope Submit manuscript

Abstract

The aim of this study was to clarify effects of inflammation on spermatogenesis in LPS-administered mice. ICR mice were treated by intraperitoneal injection for 7 days with either physiological saline (control) or 0.1 mg lipopolysaccharide (LPS)/kg body weight/day. Control mice were killed at 24 h after the last injection and the LPS-treated group after 24 h or 1, 3, or 5 weeks. Sperm concentration and motility in the cauda epididymis were examined as well as immunohistochemical localization of Fas and FasL and germ cell apoptosis. Sperm concentration and motility markedly fluctuated in LPS-treated mice. Increase of apoptotic cells was common in all post-LPS treatment groups, with a peak at 24 h after LPS injection. In contrast to the lack of Fas immunoreactivity in control testes, LPS-treated groups demonstrated Fas in many germ cells, especially in spermatocytes and spermatids. Immunoreactivity for FasL, on the other hand, was positive for some Sertoli cells, Leydig cells, and germ cells in both control and LPS-treated groups at all time points. The results suggest that the Fas/FasL system mediates apoptosis of germ cells in LPS-treated mice testes. LPS-administered mice thus provide a good experimental model for the study of transient disruption of spermatogenesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. S Bhasin DM Kretser HWG Baker (1994) ArticleTitleClinical review 64: pathophysiology and natural history of male infertility J Clin Endocrinol Metab 79 1525–1529 Occurrence Handle7989450 Occurrence Handle10.1210/jc.79.6.1525 Occurrence Handle1:CAS:528:DyaK2MXislWitrs%3D

    Article  PubMed  CAS  Google Scholar 

  2. AM Jequier (2000) Male infertility (a guide for the clinician) Blackwell London 112–135

    Google Scholar 

  3. MK O'Bryan S Schlatt DJ Phillips DM Kretser MP Hedger (2000) ArticleTitleBacterial lipopolysaccharide-induced inflammation compromises testicular function at multiple levels in vivo Endocrinology 141 238–246 Occurrence Handle10614644 Occurrence Handle10.1210/en.141.1.238

    Article  PubMed  Google Scholar 

  4. JFR Kerr AH Wyllie AR Currie (1972) ArticleTitleApoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics Br J Cancer 26 239–257 Occurrence Handle4561027 Occurrence Handle1:STN:280:CSyD3crgslU%3D

    PubMed  CAS  Google Scholar 

  5. Y Gavrieli Y Sherman SA Ben-Sasson (1992) ArticleTitleIdentification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation J Cell Biol 119 493–501 Occurrence Handle1400587 Occurrence Handle10.1083/jcb.119.3.493 Occurrence Handle1:CAS:528:DyaK38XmtVyhsbs%3D

    Article  PubMed  CAS  Google Scholar 

  6. Y Otsuki (2004) ArticleTitleTissue specificity of apoptotic signal transduction Med Electron Microsc 37 163–169 Occurrence Handle15449109

    PubMed  Google Scholar 

  7. T Koji (2001) ArticleTitleMale germ cell death in mouse testis: possible involvement of Fas and Fas ligand Med Electron Microsc 34 213–222 Occurrence Handle11956994 Occurrence Handle10.1007/s007950100018 Occurrence Handle1:CAS:528:DC%2BD38XksFyrs7Y%3D

    Article  PubMed  CAS  Google Scholar 

  8. L Seethalakshmi M Menon RK Malhotra DA Diamond (1987) ArticleTitleEffect of cyclosporine a on male reproduction in rats J Urol 138 991–995 Occurrence Handle3656581 Occurrence Handle1:CAS:528:DyaL2sXmt1yksro%3D

    PubMed  CAS  Google Scholar 

  9. N Hakuno T Koji T Yano N Kobayashi O Tsutsumi Y Taketani PK Nakane (1996) ArticleTitleFas/APO-1/CD95 system as a mediator of granulosa cell apoptosis in ovarian follicle atresia Endocrinology 137 1938–1948 Occurrence Handle8612534 Occurrence Handle10.1210/en.137.5.1938 Occurrence Handle1:CAS:528:DyaK28XisFCqsL4%3D

    Article  PubMed  CAS  Google Scholar 

  10. T Koji N Kobayashi Y Nakanishi A Yoshii S Hashimoto Y Shibata N Anjiki R Yamamoto A Aoki T Ueda S Kanazawa PK Nakane (1994) ArticleTitleImmunohistochemical localization of Fas antigen paraffin sections with rabbit antibodies against human synthemic Fas peptides Acta Histochem Cytochem 27 459–463 Occurrence Handle1:CAS:528:DyaK2MXksFanurY%3D

    CAS  Google Scholar 

  11. T Remer K Pietrzik H Wieland L Tiefenauer (1987) ArticleTitleDehydroepiandrosterone-sulphate secretion and state of adrenal function in the rat. Investigation of basic endocrine aspects in the well-fed state after dexamethasone, ACTH, metyrapone, hCG treatment J Clin Biochem Nutr 2 141–152 Occurrence Handle1:CAS:528:DyaL2sXlt1OgtLw%3D

    CAS  Google Scholar 

  12. EF Oakberg (1956) ArticleTitleA description of spermatogenesis in the mouse and its use in analysis of the cycle of seminiferous epithelium and germ cell renewal Am J Anat 99 391–413 Occurrence Handle13402725 Occurrence Handle10.1002/aja.1000990303 Occurrence Handle1:STN:280:CyiD2cfps1E%3D

    Article  PubMed  CAS  Google Scholar 

  13. C Huckins (1978) ArticleTitleThe morphology and kinetics of spermatogonial degeneration in normal adult rats: an analysis using a simplified classification of germinal epithelium Anat Rec 190 905–926 Occurrence Handle637327 Occurrence Handle10.1002/ar.1091900410 Occurrence Handle1:STN:280:CSeC2c3ntlE%3D

    Article  PubMed  CAS  Google Scholar 

  14. L Johnson CS Petty WB Neaves (1983) ArticleTitleFurther quantification of human spermatogenesis: germ cell loss during postprophase of meiosis and its relationship to daily sperm production Biol Reprod 29 207–215 Occurrence Handle6615966 Occurrence Handle10.1095/biolreprod29.1.207 Occurrence Handle1:STN:280:BiuD3c%2Fnt1c%3D

    Article  PubMed  CAS  Google Scholar 

  15. Y Yin WC DeWolf A Morgentalar (1998) ArticleTitleExpression of cryptorchidism induces testicular germ cell apoptosis by p53-dependent and -independent pathways in mice Biol Reprod 58 492–496 Occurrence Handle9475406 Occurrence Handle10.1095/biolreprod58.2.492 Occurrence Handle1:CAS:528:DyaK1cXot1SrtQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  16. K Henriksen H Hakovirta M Parvinen (1995) ArticleTitleIn-situ quantification of stage-specific apoptosis in the rat seminiferous epithelium: effects of short-term experimental cryptorchidism Int J Androl 18 256–262 Occurrence Handle8567096 Occurrence Handle1:STN:280:BymC38fmvVE%3D

    PubMed  CAS  Google Scholar 

  17. T Shikone H Billig AJW Hsueh (1994) ArticleTitleExpression induced cryptochidism increases apoptosis in rat testis Biol Reprod 51 865–872 Occurrence Handle7849188 Occurrence Handle10.1095/biolreprod51.5.865 Occurrence Handle1:CAS:528:DyaK2cXmsFejsrc%3D

    Article  PubMed  CAS  Google Scholar 

  18. T Koji Y Hishikawa H Ando Y Nakanishi N Kobayashi (2001) ArticleTitleExpression of Fas and Fas ligand in normal and ischemia-reperfusion testes: involvement of the Fas system in the induction of germ cell apoptosis in the damaged mouse testis Biol Reprod 64 946–954 Occurrence Handle11207212 Occurrence Handle10.1095/biolreprod64.3.946 Occurrence Handle1:CAS:528:DC%2BD3MXhsVKjt7w%3D

    Article  PubMed  CAS  Google Scholar 

  19. TT Turner KS Tung H Tomomasa LW Wilson (1997) ArticleTitleAcute testicular ischemia results in germ cell-specific apoptosis in the rat Biol Reprod 57 1267–1274 Occurrence Handle9408230 Occurrence Handle10.1095/biolreprod57.6.1267 Occurrence Handle1:CAS:528:DyaK2sXnvVWgsL4%3D

    Article  PubMed  CAS  Google Scholar 

  20. JJ Lysiak SD Turner TT Turner (2000) ArticleTitleMolecular pathway of germ cell apoptosis following ischemia/reperfusion of the rat testis Biol Reprod 63 1465–1472 Occurrence Handle11058553 Occurrence Handle10.1095/biolreprod63.5.1465 Occurrence Handle1:CAS:528:DC%2BD3cXnslCktb4%3D

    Article  PubMed  CAS  Google Scholar 

  21. APS Hikim C Wang A Leung RS Swerdloff (1995) ArticleTitleInvolvement of apoptosis in the induction of germ cell degeneration in adult rats after gonadotropin-releasing hormone antagonist treatment Endocrinology 136 2770–2775 Occurrence Handle7750502 Occurrence Handle10.1210/en.136.6.2770 Occurrence Handle1:CAS:528:DyaK2MXlslGgu78%3D

    Article  PubMed  CAS  Google Scholar 

  22. H Billig I Furuta C River J Tapanainen M Parvinen AJW Hsueh (1995) ArticleTitleApoptosis in testis germ cells: developmental changes in gonadotropin dependence and localization to selective tubule stages Endocrinology 136 5–12 Occurrence Handle7828558 Occurrence Handle10.1210/en.136.1.5 Occurrence Handle1:CAS:528:DyaK2MXjt1Knsbw%3D

    Article  PubMed  CAS  Google Scholar 

  23. JH Richburg A Nanez LR Williams ME Embree K Boekelheide (2000) ArticleTitleSensitivity of testicular germ cells to toxicant-induced apoptosis in gld mice that express a nonfunctional form of Fas ligand Endocrinology 141 787–793 Occurrence Handle10650961 Occurrence Handle10.1210/en.141.2.787 Occurrence Handle1:CAS:528:DC%2BD3cXmvFCrtw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  24. J Lee JH Richburg SC Younkin K Boekelheide (1997) ArticleTitleThe Fas system is a key regulator of germ cell apoptosis in the testis Endocrinology 138 2081–2088 Occurrence Handle9112408 Occurrence Handle10.1210/en.138.5.2081 Occurrence Handle1:CAS:528:DyaK2sXislCgs74%3D

    Article  PubMed  CAS  Google Scholar 

  25. S Nandi PP Banerjee B Zirkin (1999) ArticleTitleGerm cell apoptosis in the testes of Sprague Dawley rats following testosterone withdrawal by ethane 1,2-dimethanesulfonate administration: relationship to Fas Biol Reprod 61 70–75 Occurrence Handle10377033 Occurrence Handle10.1095/biolreprod61.1.70 Occurrence Handle1:CAS:528:DyaK1MXktFKgtbs%3D

    Article  PubMed  CAS  Google Scholar 

  26. D Nonclercq D Reverse G Toubeau JF Beckers J Sulon G Laurent J Zanen JA Heuson-Stiennon (1996) ArticleTitleIn situ demonstration of germinal cell apoptosis during diethylstilbestrol-induced testis regression in adult male Syrian hamsters Biol Reprod 55 1368–1376 Occurrence Handle8949895 Occurrence Handle10.1095/biolreprod55.6.1368 Occurrence Handle1:CAS:528:DyaK2sXkvFWitA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  27. L Cai BF Hales B Robaire (1997) ArticleTitleInduction of apoptosis in the germ cells of adult male rats after exposure cyclophosphamide Biol Reprod 56 1490–1497 Occurrence Handle9166702 Occurrence Handle10.1095/biolreprod56.6.1490 Occurrence Handle1:CAS:528:DyaK2sXjtlKgsbo%3D

    Article  PubMed  CAS  Google Scholar 

  28. H Masuda S Fujihira H Ueno M Kagawa Y Katsuoka H Mori (2003) ArticleTitleUltrastructural study on cytotoxic effects of cyclosporine A in spermatogenesis in rats Med Electron Microsc 36 183–191 Occurrence Handle14505063 Occurrence Handle10.1007/s00795-003-0213-4 Occurrence Handle1:CAS:528:DC%2BD3sXntl2hsLs%3D

    Article  PubMed  CAS  Google Scholar 

  29. S Nagata P Golstein (1995) ArticleTitleThe Fas death factor Science 267 1449–1456 Occurrence Handle7533326 Occurrence Handle10.1126/science.7533326 Occurrence Handle1:CAS:528:DyaK2MXktlClt7w%3D

    Article  PubMed  CAS  Google Scholar 

  30. R Watanabe-Fukunaga CI Brannan N Itoh S Yonehara NG Copeland NA Jenkin S Nagata (1992) ArticleTitleThe cDNA structure, expression, and chromosomal assignment of the mouse Fas antigen J Immunol 148 1274–1279 Occurrence Handle1371136 Occurrence Handle1:CAS:528:DyaK3sXht1amtrk%3D

    PubMed  CAS  Google Scholar 

  31. T Suda T Takahashi P Golstein S Nagata (1993) ArticleTitleMolecular cloning and expression of the Fas ligand, a novel member of the tumor necrosis factor family Cell 75 1169–1178 Occurrence Handle7505205 Occurrence Handle10.1016/0092-8674(93)90326-L Occurrence Handle1:CAS:528:DyaK2cXhtlWrurY%3D

    Article  PubMed  CAS  Google Scholar 

  32. K Henriksen H Hakovirta M Parvinen (1995) ArticleTitleTestosterone inhibits and induces apoptosis in rat seminiferous tubules in a stage-specific manner: in situ quantification in squash preparations after administration of ethane dimethane sulphonate Endocrinology 136 3285–3291 Occurrence Handle7628362 Occurrence Handle10.1210/en.136.8.3285 Occurrence Handle1:CAS:528:DyaK2MXntFKnsb8%3D

    Article  PubMed  CAS  Google Scholar 

  33. L Troiano MF Fustini E Lovato A Frasoldati W Malorni M Capri E Grassilli P Marrama C Franceschi (1994) ArticleTitleApoptosis and spermatogenesis: evidence from an in vivo model of testosterone withdrawal in the adult rat Biochem Biophys Res Commun 202 1315–1321 Occurrence Handle8060308 Occurrence Handle10.1006/bbrc.1994.2074 Occurrence Handle1:CAS:528:DyaK2cXlsV2gs7k%3D

    Article  PubMed  CAS  Google Scholar 

  34. JS Tapanainen JL Tilly KK Vihko AJW Hsueh (1993) ArticleTitleHormonal control of apoptotic cell death in the testis: gonadotropins and androgens as testicular cell survival factors Mol Endocrinol 7 643–650 Occurrence Handle8316250 Occurrence Handle10.1210/me.7.5.643 Occurrence Handle1:CAS:528:DyaK3sXksVWgtrs%3D

    Article  PubMed  CAS  Google Scholar 

  35. A Bartke (1995) ArticleTitleApoptosis of male germ cells, a generalized or a cell type-specific phenomenon? Endocrinology 136 3–4 Occurrence Handle7828545 Occurrence Handle10.1210/en.136.1.3 Occurrence Handle1:CAS:528:DyaK2MXjt1Knsb8%3D

    Article  PubMed  CAS  Google Scholar 

  36. B Jegou C Cudicini E Gomez JP Stephan (1995) ArticleTitleInterleukin-1, interleukin-6 and the germ cell-Sertoli cell cross-talk Reprod Fertil Dev 7 723–730 Occurrence Handle8711209 Occurrence Handle10.1071/RD9950723 Occurrence Handle1:CAS:528:DyaK28Xht1ClsrY%3D

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Obstetrics and Gynecology, Saitama Medical School, 38 Morohongo, Moroyama, Iruma-gun, Saitama, Japan

    Takeshi Kajihara, Ryugo Okagaki & Osamu Ishihara

Authors
  1. Takeshi Kajihara
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ryugo Okagaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Osamu Ishihara
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Takeshi Kajihara.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kajihara, T., Okagaki, R. & Ishihara, O. LPS-induced transient testicular dysfunction accompanied by apoptosis of testicular germ cells in mice. Med Mol Morphol 39, 203–208 (2006). https://doi.org/10.1007/s00795-006-0334-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00795-006-0334-7

Key words

Search

Navigation