Skip to main content

Inflammatory Networks in the Control of Spermatogenesis

Chronic Inflammation in an Immunologically Privileged Tissue?

  • Chapter
Molecular Mechanisms in Spermatogenesis

Part of the book series: Advances in Experimental Medicine and Biology ((volume 636))

Abstract

Spermatogenesis is a complex, organized process involving intimate interactions between the developing germ cells and supporting Sertoli cells. The process is also highly regulated. Studies suggest that regulation in the seminiferous epithelium involves molecules normally associated with either immune or inflammatory processes; in particular, interleukin 1a (IL1a), IL6, tumor necrosis factor (TNFa), activin A and nitric oxide (NO). While there is considerable evidence that these inflammatory mediators have effects on spermatogonial and spermatocyte development as well as critical supportive functions of the Sertoli cells, which are undoubtedly of considerable importance during testicular inflammation, there remains some skepticism regarding the significance of these molecules with respect to normal testicular function. Nonetheless, it is evident that expression of these regulators varies across the cycle of the seminiferous epithelium in a consistent manner, with major changes in production coinciding with key events within the cycle. This review summarizes the evidence supporting the hypothesis that inflammatory cytokines play a role in normal testicular spermatogenesis, as well as in the etiology of inflammation induced sub-fertility. The balance of data leads to the striking conclusion that the cycle of the seminiferous epithelium resembles a chronic inflammatory event. This appears to be a somewhat paradoxical assertion, since the testis is an immunologically privileged tissue based on its well-established ability to support grafts with minimal rejection responses. However, it may be argued that local immunoregulatory mechanisms, which confer protection from immunity on both transplanted tissues and the developing spermatogenic cells, are equally necessary to prevent local inflammation responses associated with the spermatogenic process from activating the adaptive immune response.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Clermont Y, Leblond CP. Spermiogenesis of man, monkey, ram and other mammals as shown by the periodic acid-Schiff technique. Am J Anat 1955; 96:229–253.

    Article  CAS  PubMed  Google Scholar 

  2. Clermont Y, Harvey SC. Duration of the cycle of the seminiferous epithelium of normal, hypophysectomized and hypophysectomized-hormone treated albino rats. Endocrinology 1965; 76:80–89.

    Article  CAS  PubMed  Google Scholar 

  3. Oakberg EF. Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am J Anat 1956; 99:507–516.

    Article  CAS  PubMed  Google Scholar 

  4. Clermont Y. Kinetics of spermatogenesis in mammals: Seminiferous epithelium cycle and spermatogonial renewal. Physiol Rev 1972; 52:198–236.

    CAS  PubMed  Google Scholar 

  5. Syed V, Söder O, Arver S et al. Ontogeny and cellular origin of an interleukin-1-like factor in the reproductive tract of the male rat. Int J Androl 1988; 11:437–447.

    Article  CAS  PubMed  Google Scholar 

  6. Gérard N, Syed V, Bardin W et al. Sertoli cells are the site of interleukin-1α synthesis in rat testis. Mol Cell Endocrinol 1991; 82:R13–16.

    Article  PubMed  Google Scholar 

  7. Okuda Y, Sun XR, Morris PL. Interleukin-6 (IL-6) mRNAs expressed in Leyding and Sertoli cells are regulated by cytokines, gonadotropins and neuropeptides Endocrine 1994; 2:617–624.

    CAS  Google Scholar 

  8. Cudicini C, Kercret H, Touzalin AM et al. Vectorial production of interleukin 1 and interleukin 6 by rat Sertoli cells cultured in a dual culture compartment system. Endocrinology 1997; 138:2863–2870.

    Article  CAS  PubMed  Google Scholar 

  9. O’Bryan MK, Schlatt S, Gerdprasert O et al. Inducible nitric oxide synthase in the rat testis: Evidence for potential roles in both normal function and inflammation-mediated infertility. Biol Reprod 2000; 63:1285–1293.

    Article  PubMed  Google Scholar 

  10. Head JR, Billingham RE. Immune privilege in the testis. II. Evaluation of potential local factors. Transplantation 1985; 40:269–275.

    Article  CAS  PubMed  Google Scholar 

  11. Ferguson J, Scothorne RJ. Extended survival of pancreatic islet allografts in the testis of guinea-pigs. J Anat 1977; 124:1–8.

    CAS  PubMed  Google Scholar 

  12. Sanberg PR, Borlongan CV, Saporta S et al. Testis-derived Sertoli cells survive and provide localized immunoprotection for xenografts in rat brain. Nat Biotechnol 1996; 14:1692–1695.

    Article  CAS  PubMed  Google Scholar 

  13. Korbutt GS, Elliott JF, Rajotte RV. Cotransplantation of allogeneic islets with allogeneic testicular cell aggregates allows long-term graft survival without systemic immunosuppression. Diabetes 1997; 46:317–322.

    Article  CAS  PubMed  Google Scholar 

  14. Gerdprasert O, O’Bryan MK, Muir JA et al. The response of testicular leukocytes to lipopolysaccharide-induced inflammation: Further evidence for heterogeneity of the testicular macrophage population. Cell Tiss Res 2002; 308:277–285.

    Article  CAS  Google Scholar 

  15. O’Bryan MK, Gerdprasert O, Nikolic-Paterson DJ et al. Cytokine profiles in the testes of rats treated with lipopolysaccharide reveal localized suppression of inflammatory responses. Am J Physiol—Reg Int Comp Physiol 2005; 288:R1744–1755.

    Google Scholar 

  16. Hayes R, Chalmers SA, Nikolic-Paterson DJ et al. Secretion of bioactive interleukin 1 by rat testicular macrophages in vitro. J Androl 1996; 17:41–49.

    CAS  PubMed  Google Scholar 

  17. Kern S, Robertson SA, Mau VJ et al. Cytokine secretion by macrophages in the rat testis. Biol Reprod 1995; 53:1407–1416.

    Article  CAS  PubMed  Google Scholar 

  18. Kern S, Maddocks S. Indomethacin blocks the immunosuppressive activity of rat testicular macrophages cultured in vitro. J Reprod Immunol 1995; 28:189–201.

    Article  CAS  PubMed  Google Scholar 

  19. Bryniarski K, Szczepanik M, Maresz K et al. Subpopulations of mouse testicular macrophages and their immunoregulatory function. Am J Reprod Immunol 2004; 52:27–35.

    Article  PubMed  Google Scholar 

  20. Hedger MP. Macrophages and the immune responsiveness of the testis. J Reprod Immunol 2002; 57:19–34.

    Article  CAS  PubMed  Google Scholar 

  21. Mantovani A, Sica A, Locati M. Macrophage polarization comes of age. Immunity 2005; 23:344–346.

    Article  CAS  PubMed  Google Scholar 

  22. Wang J, Wreford NG, Lan HY et al. Leukocyte populations of the adult rat testis following removal of the Leydig cells by treatment with ethane dimethane sulfonate and subcutaneous testosterone implants. Biol Reprod 1994; 51:551–561.

    Article  CAS  PubMed  Google Scholar 

  23. Pöllänen P, Maddocks S. Macrophages, lymphocytes and MHC II antigen in the ram and the rat testis. J Reprod Fertil 1988; 82:437–445.

    PubMed  Google Scholar 

  24. Pöllänen P, Niemi M. Immunohistochemical identification of macrophages, lymphoid cells and HLA antigens in the human testis. Int J Androl 1987; 10:37–42.

    Article  PubMed  Google Scholar 

  25. Hendry WF, Morgan H, Stedronska J. The clinical significance of antisperm antibodies in male subfertility. Br J Urol 1977; 49:757–762.

    Article  CAS  PubMed  Google Scholar 

  26. Pattinson HA, Mortimer D. Prevalence of sperm surface antibodies in the male partners of infertile couples as determined by immunobead screening. Fertil Steril 1987; 48:466–469.

    CAS  PubMed  Google Scholar 

  27. Rosenberg HF, Gallin JI. Inflammation. In: Paul WE, ed. Fundamental Immunology. 5th ed. Philadelphia: Lippincott, Williams and Wilkins, 2003:1151–1169.

    Google Scholar 

  28. Syed V, Stéphan JP, Gérard N et al. Residual bodies activate Sertoli cell interleukin-1α (IL-1α) release, which triggers IL-6 production by an autocrine mechanism, through the lipoxygenase pathway. Endocrinology 1995; 136:3070–3078.

    Article  CAS  PubMed  Google Scholar 

  29. Stéphan JP, Syed V, Jégou B. Regulation of Sertoli cell IL-1 and IL-6 production in vitro. Mol Cell Endocrinol 1997; 134:109–118.

    Article  PubMed  Google Scholar 

  30. Okuma Y, O’Connor AE, Muir JA et al. Regulation of activin A and inhibin B secretion by inflammatory mediators in adult rat Sertoli cell cultures. J Endocrinol 2005; 187:125–134.

    Article  CAS  PubMed  Google Scholar 

  31. Gérard N, Syed V, Jégou B. Lipopolysaccharide, latex beads and residual bodies are potent activators of Sertoli cell interleukin-1a production. Biochem Biophys Res Commun 1992; 185:154–161.

    Article  PubMed  Google Scholar 

  32. Okuma Y, O’Connor AE, Hayashi T et al. Regulated production of activin A and inhibin B throughout the cycle of the seminiferous epithelium in the rat. J Endocrinol 2006; 190:331–340.

    Article  CAS  PubMed  Google Scholar 

  33. Dejucq N, Lienard MO, Guillaume E et al. Expression of interferons-α and −γ in testicular interstitial tissue and spermatogonia of the rat. Endocrinology 1998; 139:3081–3087.

    Article  CAS  PubMed  Google Scholar 

  34. Guo H, Calkins JH, Sigel MM et al. Interleukin-2 is a potent inhibitor of Leydig cell steroidogenesis. Endocrinology 1990; 127:1234–1239.

    Article  CAS  PubMed  Google Scholar 

  35. Strand ML, Wahlgren A, Svechnikov K et al. Interleukin-18 is expressed in rat testis and may promote germ cell growth. Mol, Cell Endocrinol 2005; 240:64–73.

    Article  CAS  Google Scholar 

  36. Ishikawa T, Morris PL. A multistep kinase-based sertoli cell autocrine-amplifying loop regulates prostaglandins, their receptors, and cytokines. Endocrinology 2006; 147:1706–1716.

    Article  CAS  PubMed  Google Scholar 

  37. Teerds KJ, Dorrington JH. Localization of transforming growth factor β1 and β2 during testicular development in the rat. Biol Reprod 1993; 48:40–45.

    Article  CAS  PubMed  Google Scholar 

  38. Mullaney BP, Skinner MK. Transforming growth factor-β (β1, β2, and β3) gene expression and action during pubertal development of the seminiferous tubule: Potential role at the onset of spermatogenesis. Mol Endocrinol 1993; 7:67–76.

    Article  CAS  PubMed  Google Scholar 

  39. Dinarello CA. Proinflammatory cytokines. Chest 2000; 118:503–508.

    Article  CAS  PubMed  Google Scholar 

  40. Dinarello CA. Biologic basis for interleukin-1 in disease. Blood 1996; 87:2095–2147.

    CAS  PubMed  Google Scholar 

  41. Medzhitov R, Preston-Hurlburt P, Kopp E et al. MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol Cell 1998; 2:253–258.

    Article  CAS  PubMed  Google Scholar 

  42. Wesche H, Henzel WJ, Shillinglaw W et al. MyD88: An adapter that recruits IRAK to the IL-1 receptor complex. Immunity 1997; 7:837–847.

    Article  CAS  PubMed  Google Scholar 

  43. Hazuda DJ, Lee JC, Young PR. The kinetics of interleukin 1 secretion from activated monocytes: Differences between interleukin 1a and interleukin 1b. J Biol Chem 1988; 263:8473–8479.

    CAS  PubMed  Google Scholar 

  44. Black RA, Kronheim SR, Cantrell M et al. Generation of biologically active interleukin-1β by proteolytic cleavage of the inactive precursor. J Biol Chem 1988; 263:9437–9442.

    CAS  PubMed  Google Scholar 

  45. Watanabe N, Kobayashi Y. Selective release of a processed form of interleukin 1α. Cytokine 1994; 6:597–601.

    Article  CAS  PubMed  Google Scholar 

  46. Thornberry NA, Molineaux SM. Interleukin-1β converting enzyme: A novel cysteine protease required for IL-1β production and implicated in programmed cell death. Prot Sci 1995; 4:3–12.

    CAS  Google Scholar 

  47. Rubartelli A, Bajetto A, Allavena G et al. Post-translational regulation of interleukin 1β secretion. Cytokine 1993; 5:117–124.

    Article  CAS  PubMed  Google Scholar 

  48. Arend WP. Interleukin-1 receptor antagonist. Adv Immunol 1993; 54:167–227.

    Article  CAS  PubMed  Google Scholar 

  49. Jonsson CK, Zetterström RH, Holst M et al. Constitutive expression of interleukin-1α messenger ribonucleic acid in rat Sertoli cells is dependent upon interaction with germ cells. Endocrinology 1999; 140:3755–3761.

    Article  CAS  PubMed  Google Scholar 

  50. Jonsson CK, Setchell BP, Martinelle N et al. Endotoxin-induced interleukin 1 expression in testicular macrophages is accompanied by downregulation of the constitutive expression in Sertoli cells. Cytokine 2001; 14:283–288.

    Article  CAS  PubMed  Google Scholar 

  51. Gomez E, Morel G, Cavalier A et al. Type I and type II interleukin-1 receptor expression in rat, mouse, and human testes. Biol Reprod 1997; 56:1513–1526.

    Article  CAS  PubMed  Google Scholar 

  52. Pöllänen P, Söder O, Parvinen M. Interleukin-1α stimulation of spermatogonial proliferation in vivo. Reprod Fertil Dev 1989; 1:85–87.

    Article  PubMed  Google Scholar 

  53. Söder O, Syed V, Callard GV et al. Production and secretion of an interleukin-1-like factor is stage-dependent and correlates with spermatogonial DNA synthesis in the rat seminiferous epithelium. Int J Androl 1991; 14:223–231.

    Article  PubMed  Google Scholar 

  54. Hakovirta H, Pentitilä TL, Pöllänen P et al. Interleukin-1 bioactivity and DNA synthesis in X-irradiated rat testes. Int J Androl 1993; 16:159–164.

    Article  CAS  PubMed  Google Scholar 

  55. Parvinen M, Söder O, Mali P et al. In vitro stimulation of stage-specific deoxyribonucleic acid synthesis in rat seminiferous tubule segments by interleukin-1α. Endocrinology 1991; 129:1614–1620.

    Article  CAS  PubMed  Google Scholar 

  56. Hoeben E, Van Damme J, Put W et al. Cytokines derived from activated human mononuclear cells markedly stimulate transferrin secretion by cultured Sertoli cells. Endocrinology 1996; 137:514–521.

    Article  CAS  PubMed  Google Scholar 

  57. Nehar D, Mauduit C, Boussouar F et al. Interleukin 1α stimulates lactate dehydrogenase A expression and lactate production in cultured porcine Sertoli cells. Biol Reprod 1998; 59:1425–1432.

    Article  CAS  PubMed  Google Scholar 

  58. Sultana T, Svechnikov K, Weber G et al. Molecular cloning and expression of a functionally different alternative splice variant of prointerleukin-1α from the rat testis. Endocrinology 2000; 141:4413–4418.

    Article  CAS  PubMed  Google Scholar 

  59. Svechnikov KV, Sultana T, Söder O. Age-dependent stimulation of Leydig cell steroidogenesis by interleukin-1 isoforms. Mol Cell Endocrinol 2001; 182:193–201.

    Article  CAS  PubMed  Google Scholar 

  60. Huleihel M, Lunenfeld E, Blindman A et al. Over expression of interleukin-1α, interleukin-1β and interleukin-1 receptor antagonist in testicular tissues from sexually immature mice as compared to adult mice. Eur Cyto Netw 2003; 14:27–33.

    CAS  Google Scholar 

  61. Haugen TB, Landmark BF, Josefsen GM et al. The mature form of interleukin-1 α is constitutively expressed in immature male germ cells from rat. Mol Cell Endocrinol 1994; 105:R19–23.

    Article  CAS  PubMed  Google Scholar 

  62. Lin T, Wang D, Nagpal ML. Human chorionic gonadotropin induces interleukin-1 gene expression in rat Leydig cells in vivo. Mol Cell Endocrinol 1993; 95:139–145.

    Article  CAS  PubMed  Google Scholar 

  63. Rozwadowska N, Fiszer D, Kurpisz M. Interleukin-1 system in testis—Quantitative analysis. Expression of immunomodulatory genes in male gonad. Adv Exp Biol Med 2001; 495:177–180.

    CAS  Google Scholar 

  64. Zeyse D, Lunenfeld E, Beck M et al. Interleukin-1 receptor antagonist is produced by Sertoli cells in vitro. Endocrinology 2000; 141:1521–1527.

    Article  CAS  PubMed  Google Scholar 

  65. Xiong Y, Hales DB. Immune-endocrine interactions in the mouse testis: Cytokine-mediated inhibition of Leydig cell steroidogenesis. Endocrine 1994; 2:223–228.

    CAS  Google Scholar 

  66. Hales DB. Interleukin-1 inhibits Leydig cell steroidogenesis primarily by decreasing 17α-hydroxylase/C17–20 lyase cytochrome P450 expression. Endocrinology 1992; 131:2165–2172.

    Article  CAS  PubMed  Google Scholar 

  67. Xiong Y, Hales DB. Differential effects of tumor necrosis factor-α and interleukin-1 on 3β-hydroxysteroid dehydrogenase/D5 → D4 isomerase expression in mouse Leydig cells. Endocrine 1997; 7:295–301.

    Article  CAS  PubMed  Google Scholar 

  68. Lin T, Wang D, Stocco DM. Interleukin-1 inhibits Leydig cell steroidogenesis without affecting steroidogenic acute regulatory protein messenger ribonucleic acid or protein levels. J Endocrinol 1998; 156:461–467.

    Article  CAS  PubMed  Google Scholar 

  69. Heinrich PC, Behrmann I, Haan S et al. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 2003; 374:1–20.

    Article  CAS  PubMed  Google Scholar 

  70. Tilg H, Dinarello CA, Mier JW. IL-6 and APPs: Anti-inflammatory and immunosuppressive mediators. Immunol Today 1997; 18:428–432.

    Article  CAS  PubMed  Google Scholar 

  71. Cudicini C, Lejeune H, Gomez E et al. Human Leydig cells and Sertoli cells are producers of interleukins-1 and-6. J Clin Endocrinol Metab 1997; 82:1426–1433.

    Article  CAS  PubMed  Google Scholar 

  72. Okuda Y, Bardin CW, Hodgskin LR et al. Interleukins-1α and-1β regulate interleukin-6 expression in Leydig and Sertoli cells. Recent Prog Horm Res 1995; 50:367–372.

    CAS  PubMed  Google Scholar 

  73. Hakovirta H, Syed V, Jégou B et al. Function of interleukin-6 as an inhibitor of meiotic DNA synthesis in the rat seminiferous epithelium. Mol Cell Endocrinol 1995; 108:193–198.

    Article  CAS  PubMed  Google Scholar 

  74. Fujisawa M, Okuda Y, Fujioka H et al. Expression and regulation of gp130 messenger ribonucleic acid in cultured immature rat Sertoli cells. Endocr Res 2002; 28:1–8.

    Article  CAS  PubMed  Google Scholar 

  75. Boockfor FR, Schwarz LK. Effects of interleukin-6, interleukin-2, and tumor necrosis factor alpha on transferrin release from Sertoli cells in culture. Endocrinology 1991; 129:256–262.

    Article  CAS  PubMed  Google Scholar 

  76. Hoeben E, Wuyts A, Proost P et al. Identification of IL-6 as one of the important cytokines responsible for the ability of mononuclear cells to stimulate Sertoli cell functions. Mol Cell Endocrinol 1997; 132:149–160.

    Article  CAS  PubMed  Google Scholar 

  77. Jenab S, Morris PL. Interleukin-6 regulation of κ opioid receptor gene expression in primary Sertoli cells. Endocrine 2000; 13:11–15.

    Article  CAS  PubMed  Google Scholar 

  78. Rival C, Theas MS, Guazzone VA et al. Interleukin-6 and IL-6 receptor cell expression in testis of rats with autoimmune orchitis. J Reprod Immunol 2006; 70:43–58.

    Article  CAS  PubMed  Google Scholar 

  79. Li L, Itoh M, Ablake M et al. Prevention of murine experimental autoimmune orchitis by recombinant human interleukin-6. Clin Immunol 2002; 102:135–137.

    Article  CAS  PubMed  Google Scholar 

  80. Spooner CE, Markowitz NP, Sarvolatz LD. The role of tumor necrosis factor in sepsis. Clin Immunol Immunopath 1992; 62:S11–S17.

    Article  CAS  Google Scholar 

  81. Cerami A. Inflammatory cytokines. Clin Immunol Immunopath 1992; 62:S3–S10.

    Article  CAS  Google Scholar 

  82. Hsu H, Shu HB, Pan MG et al. TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell 1996; 84:299–308.

    Article  CAS  PubMed  Google Scholar 

  83. Mak T, Yeh WC. Signaling for survival and apoptosis in the immune system. Arthritis Res 2002; 4:S243–S252.

    Article  PubMed  Google Scholar 

  84. De SK, Chen HL, Pace JL et al. Expression of tumor necrosis factor-α in mouse spermatogenic cells. Endocrinology 1993; 133:389–396.

    Article  CAS  PubMed  Google Scholar 

  85. Mauduit C, Besset V, Caussanel V et al. Tumor necrosis factor a receptor p55 is under hormonal (follicle-stimulating hormone) control in testicular Sertoli cells. Biochem Biophys Res Commun 1996; 224:631–637.

    Article  CAS  PubMed  Google Scholar 

  86. Moore C, Hutson JC. Physiological relevance of tumor necrosis factor in mediating macrophage-Leydig cell interactions. Endocrinology 1994; 134:63–69.

    Article  CAS  PubMed  Google Scholar 

  87. Xiong Y, Hales DB. Expression, regulation, and production of tumor necrosis factor-α in mouse testicular interstitial macrophages in vitro. Endocrinology 1993; 133:2568–2573.

    Article  CAS  PubMed  Google Scholar 

  88. Pentikäinen V, Erkkilä K, Suomalainen L et al. TNFα down-regulates the Fas ligand and inhibits germ cell apoptosis in the human testis. J Clin Endocrinol Metab 2001; 86:4480–4488.

    Article  PubMed  Google Scholar 

  89. Suominen JS, Wang Y, Kaipia A et al. Tumor necrosis factor-alpha (TNF-α) promotes cell survival during spermatogenesis, and this effect can be blocked by infliximab, a TNF-α antagonist. Eur J Endocrinol 2004; 151:629–640.

    Article  CAS  PubMed  Google Scholar 

  90. Siu MK, Lee WM, Cheng CY. The interplay of collagen IV, tumor necrosis factor-α, gelatinase B (matrix metalloprotease-9), and tissue inhibitor of metalloproteases-1 in the basal lamina regulates Sertoli cell-tight junction dynamics in the rat testis. Endocrinology 2003; 144:371–387.

    Article  CAS  PubMed  Google Scholar 

  91. Le Magueresse-Battistoni B, Pernod G, Kolodié L et al. Tumor necrosis factor-α regulates plasminogen activator inhibitor-1 in rat testicular peritubular cells. Endocrinology 1997; 138:1097–1105.

    Article  PubMed  Google Scholar 

  92. Nehar D, Mauduit C, Boussouar F et al. Tumor necrosis factor-α-stimulated lactate production is linked to lactate dehydrogenase A expression and activity increase in porcine cultured Sertoli cells. Endocrinology 1997; 138:1964–1971.

    Article  CAS  PubMed  Google Scholar 

  93. Riera MF, Meroni SB, Gómez GE et al. Regulation of lactate production by FSH, IL1β, and TNFα in rat Sertoli cells. Gen Comp Endocrinol 2001; 122:88–97.

    Article  CAS  PubMed  Google Scholar 

  94. Mauduit C, Jaspar JM, Poncelet E et al. Tumor necrosis factor-α antagonizes follicle-stimulating hormone action in cultured Sertoli cells. Endocrinology 1993; 133:69–76.

    Article  CAS  PubMed  Google Scholar 

  95. Delfino FJ, Boustead JN, Fix C et al. NF-κB and TNF-α stimulate androgen receptor expression in Sertoli cells. Mol Cell Endocrinol 2003; 201:1–12.

    Article  CAS  PubMed  Google Scholar 

  96. Yule TD, Tung KS. Experimental autoimmune orchitis induced by testis and sperm antigen-specific T cell clones: An important pathogenic cytokine is tumor necrosis factor. Endocrinology 1993; 133:1098–1107.

    Article  CAS  PubMed  Google Scholar 

  97. Suescun MO, Rival C, Theas MS et al. Involvement of tumor necrosis factor-α in the pathogenesis of autoimmune orchitis in rats. Biol Reprod 2003; 68:2114–2121.

    Article  CAS  PubMed  Google Scholar 

  98. Riccioli A, Starace D, D’Alessio A et al. TNF-α and IFN-γ regulate expression and function of the Fas system in the seminiferous epithelium. J Immunol 2000; 165:743–749.

    CAS  PubMed  Google Scholar 

  99. Riccioli A, Filippini A, De Cesaris P et al. Inflammatory mediators increase surface expression of integrin ligands, adhesion to lymphocytes, and secretion of interleukin 6 in mouse Sertoli cells. Proc Natl Acad Sci USA 1995; 92:5808–5812.

    Article  CAS  PubMed  Google Scholar 

  100. Hong CY, Park JH, Ahn RS et al. Molecular mechanism of suppression of testicular steroidogenesis by proinflammatory cytokine tumor necrosis factor α. Mol Cell Biol 2004; 24:2593–2604.

    Article  CAS  PubMed  Google Scholar 

  101. Mauduit C, Hartmann DJ, Chauvin MA et al. Tumor necrosis factor α inhibits gonadotropin action in cultured porcine Leydig cells: Site(s) of action. Endocrinology 1991; 129:2933–2940.

    Article  CAS  PubMed  Google Scholar 

  102. Li X, Youngblood GL, Payne AH et al. Tumor necrosis factor-α inhibition of 17α-hydroxylase/C17–20 lyase gene (Cyp17) expression. Endocrinology 1995; 136:3519–3526.

    Article  CAS  PubMed  Google Scholar 

  103. Xiong Y, Hales DB. The role of tumor necrosis factor-α in the regulation of mouse Leydig cell steroidogenesis. Endocrinology 1993; 132:2438–2444.

    Article  CAS  PubMed  Google Scholar 

  104. Mauduit C, Gasnier F, Rey C et al. Tumor necrosis factor-α inhibits leydig cell steroidogenesis through a decrease in steroidogenic acute regulatory protein expression. Endocrinology 1998; 139:2863–2868.

    Article  CAS  PubMed  Google Scholar 

  105. Morales V, Santana P, Diaz R et al. Intratesticular delivery of tumor necrosis factor-α and ceramide directly abrogates steroidogenic acute regulatory protein expression and Leydig cell steroidogenesis in adult rats. Endocrinology 2003; 144:4763–4772.

    Article  CAS  PubMed  Google Scholar 

  106. Phillips DJ. The activin/inhibin family. In: Thomson AW, Lotze MT, eds. The Cytokine Handbook, Vol 2. 4th ed. Amsterdam: Academic Press, 2003:1153–1177.

    Google Scholar 

  107. de Kretser DM, Hedger MP, Loveland KL et al. Inhibins, activins and follistatin in reproduction. Human Reprod Update 2002; 8:529–541.

    Article  Google Scholar 

  108. Yu J, Dolter KE. Production of activin A and its roles in inflammation and hematopoiesis. Cytokines Cell Mol Ther 1997; 3:169–177.

    CAS  PubMed  Google Scholar 

  109. Phillips DJ, Jones KL, Scheerlinck JY et al. Evidence for activin A and follistatin involvement in the systemic inflammatory response. Mol Cell Endocrinol 2001; 180:155–162.

    Article  CAS  PubMed  Google Scholar 

  110. Hedger MP, Phillips DJ, de Kretser DM. Divergent cell-specific effects of activin-A on thymocyte proliferation stimulated by phytohemagglutinin, and interleukin 1β or interleukin 6 in vitro. Cytokine 2000; 12:595–602.

    Article  CAS  PubMed  Google Scholar 

  111. Hedger MP, Drummond AE, Robertson DM et al. Inhibin and activin regulate [3H]thymidine uptake by rat thymocytes and 3T3 cells in vitro. Mol Cell Endocrinol 1989; 61:133–138.

    Article  CAS  PubMed  Google Scholar 

  112. Okuma Y, Saito K, O’Connor AE et al. Reciprocal regulation of activin A and inhibin B by interleukin-1 (IL-1) and follicle-stimulating hormone (FSH) in rat Sertoli cells in vitro. J Endocrinol 2005; 185:99–110.

    Article  CAS  PubMed  Google Scholar 

  113. Yoshida E, Tanimoto K, Murakami K et al. Isolation and characterization of 5′-regulatory region of mouse activin βA subunit gene. Biochem Mol Biol Int 1998; 44:325–332.

    CAS  PubMed  Google Scholar 

  114. Tanimoto K, Yoshida E, Mita S et al. Human activin βA gene: Identification of novel 5′ exon, functional promoter, and enhancers. J Biol Chem 1996; 271:32760–32769.

    Article  CAS  PubMed  Google Scholar 

  115. Ardekani AM, Romanelli JC, Mayo KE. Structure of the rat inhibin and activin βA gene and regulation in an ovarian granulosa cell line. Endocrinology 1998; 139:3271–3279.

    Article  CAS  PubMed  Google Scholar 

  116. Bilezikjian LM, Corrigan AZ, Blount AL et al. Regulation and actions of Smad7 in the modulation of activin, inhibin, and transforming growth factor-β signaling in anterior pituitary cells. Endocrinology 2001; 142:1065–1072.

    Article  CAS  PubMed  Google Scholar 

  117. Chen X, Weisberg E, Fridmacher V et al. Smad4 and FAST-1 in the assembly of activin-responsive factor. Nature 1997; 389:85–89.

    Article  CAS  PubMed  Google Scholar 

  118. Ethier JF, Findlay JK. Roles of activin and its signal transduction mechanisms in reproductive tissues. Reproduction 2001; 121:667–675.

    Article  CAS  PubMed  Google Scholar 

  119. Mellor SL, Ball EM, O’Connor AE et al. Activin βC-subunit heterodimers provide a new mechanism of regulating activin levels in the prostate. Endocrinology 2003; 144:4410–4419.

    Article  CAS  PubMed  Google Scholar 

  120. Mather JP, Roberts PE, Krummen LA. Follistatin modulates activin activity in a cell-and tissue-specific manner. Endocrinology 1993; 132:2732–2734.

    Article  CAS  PubMed  Google Scholar 

  121. Nakamura T, Takio K, Eto Y et al. Activin-binding protein from rat ovary is follistatin. Science 1990; 247:836–838.

    Article  CAS  PubMed  Google Scholar 

  122. Buzzard JJ, Loveland KL, O’Bryan MK et al. Changes in circulating and testicular levels of inhibin A and B and activin A during postnatal development in the rat. Endocrinology 2004; 145:3532–3541.

    Article  CAS  PubMed  Google Scholar 

  123. Kaipia A, Penttila TL, Shimasaki S et al. Expression of inhibin βA and βB, follistatin and activin-A receptor messenger ribonucleic acids in the rat seminiferous epithelium. Endocrinology 1992; 131:2703–2710.

    Article  CAS  PubMed  Google Scholar 

  124. de Winter JP, Vanderstichele HM, Verhoeven G et al. Peritubular myoid cells from immature rat testes secrete activin-A and express activin receptor type II in vitro. Endocrinology 1994; 135:759–767.

    Article  PubMed  Google Scholar 

  125. Knight PG, Muttukrishna S, Groome NP. Development and application of a two-site enzyme immunoassay for the determination of ‘total’ activin-A concentrations in serum and follicular fluid. J Endocrinol 1996; 148:267–279.

    Article  CAS  PubMed  Google Scholar 

  126. Groome NP, Tsigou A, Cranfield M et al. Enzyme immunoassays for inhibins, activins and follistatins. Mol Cell Endocrinol 2001; 180:73–77.

    Article  CAS  PubMed  Google Scholar 

  127. Meinhardt A, O’Bryan MK, McFarlane JR et al. Localization of follistatin in the rat testis. J Reprod Fertil 1998; 112:233–241.

    Article  CAS  PubMed  Google Scholar 

  128. Hakovirta H, Kaipia A, Söder O et al. Effects of activin-A, inhibin-A, and transforming growth factor-β1 on stage-specific deoxyribonucleic acid synthesis during rat seminiferous epithelial cycle. Endocrinology 1993; 133:1664–1668.

    Article  CAS  PubMed  Google Scholar 

  129. Mather JP, Attie KM, Woodruff TK et al. Activin stimulates spermatogonial proliferation in germ-Sertoli cell cocultures from immature rat testis. Endocrinology 1990; 127:3206–3214.

    Article  CAS  PubMed  Google Scholar 

  130. Meehan T, Schlatt S, O’Bryan MK et al. Regulation of germ cell and Sertoli cell development by activin, follistatin, and FSH. Dev Biol 2000; 220:225–237.

    Article  CAS  PubMed  Google Scholar 

  131. Boitani C, Stefanini M, Fragale A et al. Activin stimulates Sertoli cell proliferation in a defined period of rat testis development. Endocrinology 1995; 136:5438–5444.

    Article  CAS  PubMed  Google Scholar 

  132. Meinhardt A, McFarlane JR, Seitz J et al. Activin maintains the condensed type of mitochondria in germ cells. Mol Cell Endocrinol 2000; 168:111–117.

    Article  CAS  PubMed  Google Scholar 

  133. Chen YG, Lui HM, Lin SL et al. Regulation of cell proliferation, apoptosis, and carcinogenesis by activin. Exp Biol Med 2002; 227:75–87.

    CAS  Google Scholar 

  134. de Kretser DM, Hedger MP, Phillips DJ. Activin A and follistatin: Their role in the acute phase reaction and inflammation. J Endocrinol 1999; 161:195–198.

    Article  PubMed  Google Scholar 

  135. Illingworth PJ, Groome NP, Byrd W et al. Inhibin-B: A likely candidate for the physiologically important form of inhibin in men. J Clin Endocrinol Metab 1996; 81:1321–1325.

    Article  CAS  PubMed  Google Scholar 

  136. Clifton RJ, O’Donnell L, Robertson DM. Pachytene spermatocytes in coculture inhibit rat Sertoli cell synthesis of inhibin βB-subunit and inhibin B but not the inhibin α-subunit. J Endocrinol 2002; 172:565–574.

    Article  CAS  PubMed  Google Scholar 

  137. Stuehr DJ. Structure-function aspects in the nitric oxide synthases. Ann Rev Pharmacol Toxicol 1997; 37:339–359.

    Article  CAS  Google Scholar 

  138. Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: Structure, function and inhibition. Biochem J 2001; 357:593–615.

    Article  CAS  PubMed  Google Scholar 

  139. Davis KL, Martin E, Turko IV et al. Novel effects of nitric oxide. Ann Rev Pharmacol Toxicol 2001; 41:203–236.

    Article  CAS  Google Scholar 

  140. Droge W. Free radicals in the physiological control of cell function. Physiol Rev 2002; 82:47–95.

    CAS  PubMed  Google Scholar 

  141. Schmidt HH, Walter U. NO at work. Cell 1994; 78:919–925.

    Article  CAS  PubMed  Google Scholar 

  142. Nathan C, Xie QW. Nitric oxide synthases: Roles, tolls, and controls. Cell 1994; 78:915–918.

    Article  CAS  PubMed  Google Scholar 

  143. Lee NP, Cheng CY. Nitric oxide/nitric oxide synthase, spermatogenesis, and tight junction dynamics. Biol Reprod 2004; 70:267–276.

    Article  CAS  PubMed  Google Scholar 

  144. Brenman JE, Xia H, Chao DS et al. Regulation of neuronal nitric oxide synthase through alternative transcripts. Dev Neurosci 1997; 19:224–231.

    Article  CAS  PubMed  Google Scholar 

  145. Wang Y, Goligorsky MS, Lin M et al. A novel, testis-specific mRNA transcript encoding an NH2-terminal truncated nitric-oxide synthase. J Biol Chem 1997; 272:11392–11401.

    Article  CAS  PubMed  Google Scholar 

  146. Wang Y, Newton DC, Miller TL et al. An alternative promoter of the human neuronal nitric oxide synthase gene is expressed specifically in Leydig cells. Am J Pathol 2002; 160:369–380.

    CAS  PubMed  Google Scholar 

  147. Herman M, Rivier C. Activation of a neural brain-testicular pathway rapidly lowers Leydig cell levels of the steroidogenic acute regulatory protein and the peripheral-type benzodiazepine receptor while increasing levels of neuronal nitric oxide synthase. Endocrinology 2006; 147:624–633.

    Article  CAS  PubMed  Google Scholar 

  148. Kostic TS, Andric SA, Maric D et al. Inhibitory effects of stress-activated nitric oxide on antioxidant enzymes and testicular steroidogenesis. J Steroid Biochem Molec Biol 2000; 75:299–306.

    Article  CAS  PubMed  Google Scholar 

  149. Sharma AC, Sam IInd AD, Lee LY et al. Effect of NG-nitro-L-arginine methyl ester on testicular blood flow and serum steroid hormones during sepsis. Shock 1998; 9:416–421.

    Article  CAS  PubMed  Google Scholar 

  150. Welch C, Watson ME, Poth M et al. Evidence to suggest nitric oxide is an interstitial regulator of Leydig cell steroidogenesis. Metabolism 1995; 44:234–238.

    Article  CAS  PubMed  Google Scholar 

  151. Del Punta K, Charreau EH, Pignataro OP. Nitric oxide inhibits Leydig cell steroidogenesis. Endocrinology 1996; 137:5337–5343.

    Article  PubMed  Google Scholar 

  152. Lee NP, Cheng CY. Regulation of Sertoli cell tight junction dynamics in the rat testis via the nitric oxide synthase/soluble guanylate cyclase/3′,5′-cyclic guanosine monophosphate/protein kinase G signaling pathway: An in vitro study. Endocrinology 2003; 144:3114–3129.

    Article  CAS  PubMed  Google Scholar 

  153. Lue Y, Sinha Hikim AP, Wang C et al. Functional role of inducible nitric oxide synthase in the induction of male germ cell apoptosis, regulation of sperm number, and determination of testes size: Evidence from null mutant mice. Endocrinology 2003; 144:3092–3100.

    Article  CAS  PubMed  Google Scholar 

  154. Shiraishi K, Naito K, Yoshida K. Nitric oxide promotes germ cell necrosis in the delayed phase after experimental testicular torsion of rat. Biol Reprod 2001; 65:514–521.

    Article  CAS  PubMed  Google Scholar 

  155. Lissbrant E, Löfmark U, Collin O et al. Is nitric oxide involved in the regulation of the rat testicular vasculature? Biol Reprod 1997; 56:1221–1227.

    Article  CAS  PubMed  Google Scholar 

  156. Chang H, Lau AL, Matzuk MM. Studying TGF-β superfamily signaling by knockouts and knockins. Mol Cell Endocrinol 2001; 180:39–46.

    Article  CAS  PubMed  Google Scholar 

  157. Cohen PE, Pollard JW. Normal sexual function in male mice lacking a functional type I interleukin-1 (IL-1) receptor. Endocrinology 1998; 139:815–818.

    Article  CAS  PubMed  Google Scholar 

  158. Pasparakis M, Alexopoulou L, Episkopou V et al. Immune and inflammatory responses in TNFα-deficient mice: A critical requirement for TNFα in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response. J Exp Med 1996; 184:1397–1411.

    Article  CAS  PubMed  Google Scholar 

  159. Morales-Montor J, Baig S, Mitchell R et al. Immunoendocrine interactions during chronic cysticercosis determine male mouse feminization: Role of IL-6. J Immunol 2001; 167:4527–4533.

    CAS  PubMed  Google Scholar 

  160. Granholm T, Fröysa B, Lundström C et al. Cytokine responsiveness in germfree and conventional NMRI mice. Cytokine 1992; 4:545–550.

    Article  CAS  PubMed  Google Scholar 

  161. Granholm T, Fröysa B, Midtvedt T et al. Ontogeny of lymphocyte activating factors in conventional and germfree rats. Reg Immunol 1992; 4:209–215.

    CAS  PubMed  Google Scholar 

  162. Kangasniemi M, Kaipia A, Mali P et al. Modulation of basal and FSH-dependent cyclic AMP production in rat seminiferous tubules staged by an improved transillumination technique. Anat Rec 1990; 227:62–76.

    Article  CAS  PubMed  Google Scholar 

  163. Kangasniemi M, Kaipia A, Toppari J et al. Cellular regulation of follicle-stimulating hormone (FSH) binding in rat seminiferous tubules. J Androl 1990; 11:336–343.

    CAS  PubMed  Google Scholar 

  164. Delfino F, Walker WH. Stage-specific nuclear expression of NF-κB in mammalian testis. Mol Endocrinol 1998; 12:1696–1707.

    Article  CAS  PubMed  Google Scholar 

  165. Kluger MJ, Kozak W, Leon LR et al. The use of knockout mice to understand the role of cytokines in fever. Clin Exp Pharmacol Physiol 1998; 25:141–144.

    Article  CAS  PubMed  Google Scholar 

  166. Born TL, Smith DE, Garka KE et al. Identification and characterization of two members of a novel class of the interleukin-1 receptor (IL-1R) family: Delineation of a new class of IL-1R-related proteins based on signaling. J Biol Chem 2000; 275:29946–29954.

    Article  CAS  PubMed  Google Scholar 

  167. Andre R, Moggs JG, Kimber I et al. Gene regulation by IL-1β independent of IL-1R1 in the mouse brain. Glia 2006; 53:477–483.

    Article  PubMed  Google Scholar 

  168. Cohen PE, Chisholm O, Arceci RJ et al. Absence of colony-stimulating factor-1 in osteopetrotic (csfmop/csfmop) mice results in male fertility defects. Biol Reprod 1996; 55:310–317.

    Article  CAS  PubMed  Google Scholar 

  169. Hedger MP, Hales DB. Immunophysiology of the male reproductive tract. In: Neill JD, ed. Knobil and Neill’s Physiology of Reproduction, Vol 1. 3rd ed. Amsterdam: Elsevier, 2006:1195–1286.

    Google Scholar 

  170. Cutolo M, Balleari E, Giusti M et al. Sex hormone status of male patients with rheumatoid arthritis: Evidence of low serum concentrations of testosterone at baseline and after human chorionic gonadotropin stimulation. Arthritis Rheum 1988; 31:1314–1317.

    Article  CAS  PubMed  Google Scholar 

  171. Buch JP, Havlovec SK. Variation in sperm penetration assay related to viral illness. Fertil Steril 1991; 55:844–846.

    CAS  PubMed  Google Scholar 

  172. Adamopoulos DA, Lawrence DM, Vassilopoulos P et al. Pituitary-testicular interrelationships in mumps orchitis and other viral infections. Br Med J 1978; 1:1177–1180.

    Article  CAS  PubMed  Google Scholar 

  173. O’Bryan MK, Schlatt S, Phillips DJ et al. Bacterial lipopolysaccharide-induced inflammation compromises testicular function at multiple levels in vivo. Endocrinology 2000; 141:238–246.

    Article  PubMed  Google Scholar 

  174. Tulassay Z, Viczián M, Böjthe L et al. Quantitative histological studies on the injury of spermatogenesis induced by endotoxin in rats. J Reprod Fertil 1970; 22:161–164.

    Article  CAS  PubMed  Google Scholar 

  175. Bosmann HB, Hales KH, Li X et al. Acute in vivo inhibition of testosterone by endotoxin parallels loss of steroidogenic acute regulatory (StAR) protein in Leydig cells. Endocrinology 1996; 137:4522–4525.

    Article  CAS  PubMed  Google Scholar 

  176. Clemens JW, Bruot BC. Testicular dysfunction in the adjuvant-induced arthritic rat. J Androl 1989; 10:419–424.

    CAS  PubMed  Google Scholar 

  177. Wallgren M, Kindahl H, Larsson K. Clinical, endocrinological and spermatological studies after endotoxin in the ram. Zentralbl Veterinarmed [A] 1989; 36:90–103.

    CAS  Google Scholar 

  178. Wallgren M, Kindahl H, Rodriguez-Martinez H. Alterations in testicular function after endotoxin injection in the boar. Int J Androl 1993; 16:235–243.

    Article  CAS  PubMed  Google Scholar 

  179. Baker HW. Reproductive effects of nontesticular illness. Endocrinol Metab Clin North Am 1998; 27:831–850.

    Article  CAS  PubMed  Google Scholar 

  180. Hedger M, Klug J, Fröhlich S et al. Regulatory cytokine expression and interstitial fluid formation in the normal and inflamed rat testis are under Leydig cell control. J Androl 2005; 26:379–386.

    Article  CAS  PubMed  Google Scholar 

  181. Hales KH, Diemer T, Ginde S et al. Diametric effects of bacterial endotoxin lipopolysaccharide on adrenal and Leydig cell steroidogenic acute regulatory protein. Endocrinology 2000; 141:4000–4012.

    Article  CAS  PubMed  Google Scholar 

  182. Turner TT, Tung KS, Tomomasa H et al. Acute testicular ischemia results in germ cell-specific apoptosis in the rat. Biol Reprod 1997; 57:1267–1274.

    Article  CAS  PubMed  Google Scholar 

  183. Hales DB, Diemer T, Hales KH. Role of cytokines in testicular function. Endocrine 1999; 10:201–217.

    Article  CAS  PubMed  Google Scholar 

  184. Gow RM, O’Bryan MK, Canny BJ et al. Differential effects of dexamethasone treatment on lipopolysaccharide-induced testicular inflammation and reproductive hormone inhibition in adult rats. J Endocrinol 2001; 168:193–201.

    Article  CAS  PubMed  Google Scholar 

  185. Sharpe RM, Donachie K, Cooper I. Re-evaluation of the intratesticular level of testosterone required for quantitative maintenance of spermatogenesis in the rat. J Endocrinol 1988; 117:19–26.

    Article  CAS  PubMed  Google Scholar 

  186. Cunningham GR, Huckins C. Persistence of complete spermatogenesis in the presence of low intratesticular concentrations of testosterone. Endocrinology 1979; 105:177–186.

    Article  CAS  PubMed  Google Scholar 

  187. Liew SH, Meachem SJ, Hedger MP. A stereological analysis of the response of spermatogenesis to an acute inflammatory episode in adult rats. J Androl 2007; 28, (in press).

    Google Scholar 

  188. Tjioe DY, Steinberger E. A quantitative study of the effect of ischaemia on the germinal epithelium of rat testes. J Reprod Fertil 1970; 21:489–494.

    Article  CAS  PubMed  Google Scholar 

  189. Meachem SJ, McLachlan RI, Stanton PG et al. FSH immunoneutralization acutely impairs spermatogonial development in normal adult rats. J Androl 1999; 20:756–762, (discussion 755).

    CAS  PubMed  Google Scholar 

  190. O’Donnell L, McLachlan RI, Wreford NG et al. Testosterone promotes the conversion of round spermatids between stages VII and VIII of the rat spermatogenic cycle. Endocrinology 1994; 135:2608–2614.

    Article  PubMed  Google Scholar 

  191. Heckert LL, Griswold MD. Expression of follicle-stimulating hormone receptor mRNA in rat testes and Sertoli cells. Mol Endocrinol 1991; 5:670–677.

    Article  CAS  PubMed  Google Scholar 

  192. Schindler R, Clark BD, Dinarello CA. Dissociation between interleukin-1b mRNA and protein synthesis in human peripheral blood mononuclear cells. J Biol Chem 1990; 265:10232–10237.

    CAS  PubMed  Google Scholar 

  193. Lord PC, Wilmoth LM, Mizel SB et al. Expression of interleukin-1a and b genes by human blood polymorphonuclear leukocytes. J Clin Invest 1991; 87:1312–1321.

    Article  CAS  PubMed  Google Scholar 

  194. Herzyk DJ, Allen JN, Marsh CB et al. Macrophage and monocyte IL-1β regulation differs at multiple sites: Messenger RNA expression, translation, and post-translational processing. J Immunol 1992; 149:3052–3058.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Moira K. O’Bryan .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Landes Bioscience and Springer Science+Business Media

About this chapter

Cite this chapter

O’Bryan, M.K., Hedger, M.P. (2009). Inflammatory Networks in the Control of Spermatogenesis. In: Cheng, C.Y. (eds) Molecular Mechanisms in Spermatogenesis. Advances in Experimental Medicine and Biology, vol 636. Springer, New York, NY. https://doi.org/10.1007/978-0-387-09597-4_6

Download citation

Publish with us

Policies and ethics