Skip to main content

Advertisement

SpringerLink
Log in

The biology of interleukin-1: emerging concepts in the regulation of the actin cytoskeleton and cell junction dynamics

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Interleukin (IL)-1 is a proinflammatory cytokine with important roles in innate immunity, as well as in normal tissue homeostasis. Interestingly, recent studies have also shown IL-1 to function in the dynamics of the actin cytoskeleton and cell junctions. For example, treatment of different epithelia with IL-1α often results in the restructuring of the actin network and cell junctions, thereby leading to junction disassembly. In this review, we highlight new and interesting findings that show IL-1 to be a critical player of restructuring events in the seminiferous epithelium of the testis during 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.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Dinarello CA (2009) Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol 27:519–550

    PubMed  CAS  Google Scholar 

  2. Dinarello CA (2006) Interleukin 1 and interleukin 18 as mediators of inflammation and the aging process. Am J Clin Nutr 83:447S–455S

    PubMed  CAS  Google Scholar 

  3. Lomedico PT, Gubler U, Hellmann CP, Dukovich M, Giri JG, Pan YE, Collier K, Semionow R, Chua AO, Mizel SB (1984) Cloning and expression of murine interleukin-1 cDNA in Escherichia coli. Nature 312:458–462

    PubMed  CAS  Google Scholar 

  4. Auron PE, Webb AC, Rosenwasser LJ, Mucci SF, Rich A, Wolff SM, Dinarello CA (1984) Nucleotide sequence of human monocyte interleukin 1 precursor cDNA. Proc Natl Acad Sci USA 81:7907–7911

    PubMed  CAS  Google Scholar 

  5. Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK, Zurawski G, Moshrefi M, Qin J, Li X, Gorman DM, Bazan JF, Kastelein RA (2005) IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23:479–490

    PubMed  CAS  Google Scholar 

  6. Dinarello CA (2005) Blocking IL-1 in systemic inflammation. J Exp Med 201:1355–1359

    PubMed  CAS  Google Scholar 

  7. Hoffman HM, Rosengren S, Boyle DL, Cho JY, Nayar J, Mueller JL, Anderson JP, Wanderer AA, Firestein GS (2004) Prevention of cold-associated acute inflammation in familial cold autoinflammatory syndrome by interleukin-1 receptor antagonist. Lancet 364:1779–1785

    PubMed  CAS  Google Scholar 

  8. Maier JA, Voulalas P, Roeder D, Maciag T (1990) Extension of the life-span of human endothelial cells by an interleukin-1α antisense oligomer. Science 249:1570–1574

    PubMed  CAS  Google Scholar 

  9. Corradi A, Franzi AT, Rubartelli A (1995) Synthesis and secretion of interleukin-1α and interleukin-1 receptor antagonist during differentiation of cultured keratinocytes. Exp Cell Res 217:355–362

    PubMed  CAS  Google Scholar 

  10. Walsh SV, Hopkins AM, Nusrat A (2000) Modulation of tight junction structure and function by cytokines. Adv Drug Deliv Rev 41:303–313

    PubMed  CAS  Google Scholar 

  11. Harhaj NS, Antonetti DA (2004) Regulation of tight junctions and loss of barrier function in pathophysiology. Int J Biochem Cell Biol 36:1206–1237

    PubMed  CAS  Google Scholar 

  12. Sarkar O, Mathur PP, Cheng CY, Mruk DD (2008) Interleukin 1α (IL1A) is a novel regulator of the blood–testis barrier in the rat. Biol Reprod 78:445–454

    PubMed  CAS  Google Scholar 

  13. Lie PPY, Cheng CY, Mruk DD (2011) Interleukin-1α is a regulator of the blood–testis barrier. FASEB J 25:1244–1253

    PubMed  CAS  Google Scholar 

  14. March CJ, Mosley B, Larsen A, Cerretti DP, Braedt G, Price V, Gillis S, Henney CS, Kronheim SR, Grabstein K, Conlon PJ, Hopp TP, Cosman D (1985) Cloning, sequence and expression of two distinct human interleukin-1 complementary DNAs. Nature 315:641–647

    PubMed  CAS  Google Scholar 

  15. Dinarello CA (1997) Interleukin-1. Cytokine Growth Factor Rev 8:253–265

    PubMed  CAS  Google Scholar 

  16. Dinarello CA (1996) Biologic basis for interleukin-1 in disease. Blood 87:2095–2147

    PubMed  CAS  Google Scholar 

  17. Mosley B, Urdal DL, Prickett KS, Larsen A, Cosman D, Conlon PJ, Gillis S, Dower SK (1987) The interleukin-1 receptor binds the human interleukin-1α precursor but not the interleukin-1β precursor. J Biol Chem 262:2941–2944

    PubMed  CAS  Google Scholar 

  18. Kobayashi Y, Yamamoto K, Saido T, Kawasaki H, Oppenheim JJ, Matsushima K (1990) Identification of calcium-activated neutral protease as a processing enzyme of human interleukin 1α. Proc Natl Acad Sci USA 87:5548–5552

    PubMed  CAS  Google Scholar 

  19. Thornberry NA, Bull HG, Calaycay JR, Chapman KT, Howard AD, Kostura MJ, Miller DK, Molineaux SM, Weidner JR, Aunins J et al (1992) A novel heterodimeric cysteine protease is required for interleukin-1β processing in monocytes. Nature 356:768–774

    PubMed  CAS  Google Scholar 

  20. Kuida K, Lippke JA, Ku G, Harding MW, Livingston DJ, Su MS, Flavell RA (1995) Altered cytokine export and apoptosis in mice deficient in interleukin-1β converting enzyme. Science 267:2000–2003

    PubMed  CAS  Google Scholar 

  21. Li P, Allen H, Banerjee S, Franklin S, Herzog L, Johnston C, McDowell J, Paskind M, Rodman L, Salfeld J, Towne E, Tracey D, Wardwell S, Wei FY, Wong W, Kamen R, Seshadri T (1995) Mice deficient in IL-1β-converting enzyme are defective in production of mature IL-1β and resistant to endotoxic shock. Cell 80:401–411

    PubMed  CAS  Google Scholar 

  22. Rubartelli A, Cozzolino F, Talio M, Sitia R (1990) A novel secretory pathway for interleukin-1β, a protein lacking a signal sequence. EMBO J 9:1503–1510

    PubMed  CAS  Google Scholar 

  23. Martinon F, Burns K, Tschopp J (2002) The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-β. Mol Cell 10:417–426

    PubMed  CAS  Google Scholar 

  24. Martinon F, Mayor A, Tschopp J (2009) The inflammasomes: guardians of the body. Annu Rev Immunol 27:229–265

    PubMed  CAS  Google Scholar 

  25. Ferrari D, Pizzirani C, Adinolfi E, Lemoli RM, Curti A, Idzko M, Panther E, Di Virgilio F (2006) The P2X7 receptor: a key player in IL-1 processing and release. J Immunol 176:3877–3883

    PubMed  CAS  Google Scholar 

  26. Mariathasan S, Monack DM (2007) Inflammasome adaptors and sensors: intracellular regulators of infection and inflammation. Nat Rev Immunol 7:31–40

    PubMed  CAS  Google Scholar 

  27. Martinon F, Tschopp J (2007) Inflammatory caspases and inflammasomes: master switches of inflammation. Cell Death Differ 14:10–22

    PubMed  CAS  Google Scholar 

  28. Skaper SD, Debetto P, Giusti P (2010) The P2X7 purinergic receptor: from physiology to neurological disorders. FASEB J 24:337–345

    PubMed  CAS  Google Scholar 

  29. Khakh BS, North RA (2006) P2X receptors as cell-surface ATP sensors in health and disease. Nature 442:527–532

    PubMed  CAS  Google Scholar 

  30. Solle M, Labasi J, Perregaux DG, Stam E, Petrushova N, Koller BH, Griffiths RJ, Gabel CA (2001) Altered cytokine production in mice lacking P2X7 receptors. J Biol Chem 276:125–132

    PubMed  CAS  Google Scholar 

  31. Humphreys BD, Rice J, Kertesy SB, Dubyak GR (2000) Stress-activated protein kinase/JNK activation and apoptotic induction by the macrophage P2X7 nucleotide receptor. J Biol Chem 275:26792–26798

    PubMed  CAS  Google Scholar 

  32. Aga M, Johnson CJ, Hart AP, Guadarrama AG, Suresh M, Svaren J, Bertics PJ, Darien BJ (2002) Modulation of monocyte signaling and pore formation in response to agonists of the nucleotide receptor P2X7. J Leukoc Biol 72:222–232

    PubMed  CAS  Google Scholar 

  33. Potucek YD, Crain JM, Watters JJ (2006) Purinergic receptors modulate MAP kinases and transcription factors that control microglial inflammatory gene expression. Neurochem Int 49:204–214

    PubMed  CAS  Google Scholar 

  34. Andrei C, Margiocco P, Poggi A, Lotti LV, Torrisi MR, Rubartelli A (2004) Phospholipases C and A2 control lysosome-mediated IL-1β secretion: implications for inflammatory processes. Proc Natl Acad Sci USA 101:9745–9750

    PubMed  CAS  Google Scholar 

  35. MacKenzie A, Wilson HL, Kiss-Toth E, Dower SK, North RA, Surprenant A (2001) Rapid secretion of interleukin-1β by microvesicle shedding. Immunity 8:825–835

    Google Scholar 

  36. Chen C, Kono H, Golenbock D, Reed G, Akira S, Rock KL (2007) Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat Med 13:851–856

    PubMed  CAS  Google Scholar 

  37. Dinarello CA (1994) The interleukin-1 family: 10 years of discovery. FASEB J 8:1314–1325

    PubMed  CAS  Google Scholar 

  38. Gustafsson K, Sultana T, Zetterstrom CK, Setchell BP, Siddiqui A, Weber G, Soder O (2002) Production and secretion of interleukin-1α proteins by rat testis. Biochem Biophys Res Commun 297:492–497

    PubMed  CAS  Google Scholar 

  39. O’Neill LAJ (2008) The interleukin-1 receptor/Toll-like receptor superfamily: 10 years of progress. Immunol Rev 226:10–18

    PubMed  Google Scholar 

  40. Colotta F, Re F, Muzio M, Bertini R, Polentarutti N, Sironi M, Giri JG, Dower SK, Sims JE, Mantovani A (1993) Interleukin-1 type II receptor: a decoy target for IL-1 that is regulated by IL-4. Science 261:472–475

    PubMed  CAS  Google Scholar 

  41. Mantovani A, Locati M, Polentarutti N, Vecchi A, Garlanda C (2004) Extracellular and intracellular decoys in the tuning of inflammatory cytokines and Toll-like receptors: the new entry TIR8/SIGIRR. J Leukoc Biol 75:738–742

    PubMed  CAS  Google Scholar 

  42. Greenfeder SA, Nunes P, Kwee L, Labow M, Chizzonite RA, Ju G (1995) Molecular cloning and characterization of a second subunit of the interleukin 1 receptor complex. J Biol Chem 270:13757–13765

    PubMed  CAS  Google Scholar 

  43. Lang D, Knop J, Wesche H, Raffetseder U, Kurrle R, Boraschi D, Martin MU (1998) The type II IL-1 receptor interacts with the IL-1 receptor accessory protein: a novel mechanism of regulation of IL-1 responsiveness. J Immunol 161:6871–6877

    PubMed  CAS  Google Scholar 

  44. Dunne A, O’Neill LAJ (2003) The interleukin-1 receptor/Toll-like receptor superfamily: signal transduction during inflammation and host defense. Sci STKE 171:re3–re17

    Google Scholar 

  45. Burns K, Martinon F, Esslinger C, Pahl H, Schneider P, Bodmer JL, Di Marco F, French L, Tschopp J (1998) MyD88, an adaptor protein involved in interleukin-1 signaling. J Biol Chem 273:12203–12209

    PubMed  CAS  Google Scholar 

  46. Wesche H, Henzel WJ, Shillinglaw W, Li S, Cao Z (1997) MyD88: an adaptor that recruits IRAK to the IL-1 receptor complex. Immunity 7:837–847

    PubMed  CAS  Google Scholar 

  47. Wang Z, Wesche H, Stevens T, Walker N, Yeh WC (2009) IRAK-4 inhibitors for inflammation. Curr Top Med Chem 9:724–737

    PubMed  CAS  Google Scholar 

  48. Gottipati S, Rao NL, Fung-Leung WP (2008) IRAK1: a critical signaling mediator of innate immunity. Cell Signal 20:269–276

    PubMed  CAS  Google Scholar 

  49. Janssens S, Beyaert R (2003) Functional diversity and regulation of different interleukin-1 receptor-associated kinase (IRAK) family members. Mol Cell 11:293–302

    PubMed  CAS  Google Scholar 

  50. Suzuki N, Suzuki S, Yeh WC (2002) IRAK-4 as the central TIR signaling mediator in innate immunity. Trends Immunol 23:503–506

    PubMed  CAS  Google Scholar 

  51. Barton GM, Medzhitov R (2003) Toll-like receptor signaling pathways. Science 300:1524–2525

    PubMed  CAS  Google Scholar 

  52. Kawaguchi Y, Nishimagi E, Tochimoto A, Kawamoto M, Katsumata Y, Soejima M, Kanno T, Kamatani N, Hara M (2006) Intracellular IL-1α-binding proteins contribute to biological functions of endogenous IL-1α in system sclerosis fibroblasts. Proc Natl Acad Sci USA 103:14501–14506

    PubMed  CAS  Google Scholar 

  53. Maier JAM, Statuto M, Ragnotti G (1994) Endogenous interleukin 1α must be transported to the nucleus to exert its activity in human endothelial cells. Mol Cell Biol 14:1845–1851

    PubMed  CAS  Google Scholar 

  54. Wessendorf JHM, Garfinkel S, Zhan X, Brown S, Maciag T (1993) Identification of a nuclear localization sequence within the structure of the human interleukin-1α precursor. J Biol Chem 268:22100–22104

    PubMed  CAS  Google Scholar 

  55. Hu B, Wang S, Zhang Y, Feghali CA, Dingman JR, Wright TM (2003) A nuclear target for interleukin-1α: interaction with the growth suppressor necdin modulates proliferation and collagen expression. Proc Natl Acad Sci USA 100:10008–10013

    PubMed  CAS  Google Scholar 

  56. Luheshi NM, Rothwell NJ, Brough D (2009) The dynamics and mechanisms of interleukin-1α and β nuclear import. Traffic 10:16–25

    PubMed  CAS  Google Scholar 

  57. Fadeel B, Grzybowska E (2009) HAX-1: a multifunctional protein with emerging roles in human disease. Biochim Biophys Acta 1790:1139–1148

    PubMed  CAS  Google Scholar 

  58. Yin HL, Morioka H, Towle CA, Vidal M, Watanabe T, Weissbach L (2001) Evidence that HAX-1 is an interleukin-1α N-terminal binding protein. Cytokine 15:122–137

    PubMed  CAS  Google Scholar 

  59. Kawaguchi Y, McCarthy SA, Watkins SC, Wright TM (2004) Autocrine activation by interleukin 1α induces the fibrogenic phenotype of systemic sclerosis fibroblasts. J Rheumatol 31:1946–1954

    PubMed  CAS  Google Scholar 

  60. Campos SB, Ashworth SL, Wean S, Hosford M, Sandoval RM, Hallett MA, Atkinson SJ, Molitoris BA (2009) Cytokine-induced F-actin reorganization in endothelial cells involves RhoA activation. Am J Physiol Renal Physiol 296:F487–F495

    PubMed  CAS  Google Scholar 

  61. Nilsson M, Husmark J, Bjorkman U, Ericson LE (1998) Cytokines and thyroid epithelial integrity: interleukin-1α induces dissociation of the junctional complex and paracellular leakage in filter-cultured human thyrocytes. J Clin Endocrinol Metab 83:945–952

    PubMed  CAS  Google Scholar 

  62. Al-Sadi RM, Ma TY (2007) IL-1β causes an increase in intestinal epithelial tight junction permeability. J Immunol 178:4641–4649

    PubMed  CAS  Google Scholar 

  63. Quagliarello VJ, Wispelwey B, Long WJ, Scheld WM (1991) Recombinant human interleukin-1 induces meningitis and blood–brain barrier injury in the rat. J Clin Invest 87:1360–1366

    PubMed  CAS  Google Scholar 

  64. Singh R, Wang B, Shirvaikar A, Khan S, Kamat S, Schelling JR, Konieczkowski M, Sedor JR (1999) The IL-1 receptor and Rho directly associate to drive cell activation and inflammation. J Clin Invest 103:1561–1570

    PubMed  CAS  Google Scholar 

  65. Ridley AJ (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 16:522–529

    PubMed  CAS  Google Scholar 

  66. Heasman SJ, Ridley AJ (2008) Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 9:690–701

    PubMed  CAS  Google Scholar 

  67. Burridge K, Wennerberg K (2004) Rho and Rac take center stage. Cell 116:167–179

    PubMed  CAS  Google Scholar 

  68. Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247–269

    PubMed  CAS  Google Scholar 

  69. Bishop AL, Hall A (2000) Rho GTPases and their effector proteins. Biochem J 348:241–255

    PubMed  CAS  Google Scholar 

  70. Barth BM, Stewart-Smeets S, Kuhn TB (2009) Proinflammatory cytokines provoke oxidative damage to actin in neuronal cells mediated by Rac1 and NADPH oxidase. Mol Cell Neurosci 41:274–285

    PubMed  CAS  Google Scholar 

  71. Ridley AJ, Hall A (1992) The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70:389–399

    PubMed  CAS  Google Scholar 

  72. Quarnstrom EE, Page RC, Gillis S, Dower SK (1988) Binding, internalization, and intracellular localization of interleukin-1β in human diploid fibroblasts. J Biol Chem 263:8261–8269

    Google Scholar 

  73. Wang Q, Downey GP, Herrera-Abreu MT, Kapus A, McCulloch CA (2005) SHP-2 modulates interleukin-1-induced Ca2+ flux and ERK activation via phosphorylation of phospholipase Cγ1. J Biol Chem 280:8397–8406

    PubMed  CAS  Google Scholar 

  74. Ganter MT, Roux J, Miyazawa B, Howard M, Frank JA, Su G, Sheppard D, Violette SM, Weinreb PH, Horan GS, Matthay MA, Pittet J (2008) Interleukin-1β causes acute lung injury via αvβ5 and αvβ6 integrin-dependent mechanisms. Circ Res 102:804–812

    PubMed  CAS  Google Scholar 

  75. Summers L, Kangwantas K, Nguyen L, Kielty C, Pinteaux E (2010) Adhesion to the extracellular matrix is required for interleukin-1β actions leading to reactive phenotype in rat astrocytes. Mol Cell Neurosci 44:272–281

    PubMed  CAS  Google Scholar 

  76. Novakofski K, Boehm A, Fortier L (2009) The small GTPase Rho mediates articular chondrocyte phenotype and morphology in response to interleukin-1α and insulin-like growth factor-I. J Orth Res 27:58–64

    CAS  Google Scholar 

  77. Chrzanowska-Wodnicka M, Burridge K (1996) Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J Cell Biol 133:1403–1415

    PubMed  CAS  Google Scholar 

  78. Pittet J, Griffiths MJD, Geiser T, Kaminski N, Dalton SL, Huang X, Brown LAS, Gotwals PJ, Koteliansky VE, Matthay MA, Sheppard D (2001) TGF-β is a critical mediator of acute lung injury. J Clin Invest 107:1537–1544

    PubMed  CAS  Google Scholar 

  79. Lui WY, Lee WM, Cheng CY (2003) Transforming growth factor-β3 regulates the dynamics of Sertoli cell tight junctions via the p38 mitogen-activated protein kinase pathway. Biol Reprod 68:1597–1612

    PubMed  CAS  Google Scholar 

  80. Baker RG, Hayden MS, Ghosh S (2011) NF-κB, inflammation and metabolic disease. Cell Metab 13:11–22

    PubMed  CAS  Google Scholar 

  81. Schneider G, Kramer OH (2011) NF-κB/p53 crosstalk—a promising new therapeutic target. Biochim Biophys Acta 1815:90–103

    PubMed  CAS  Google Scholar 

  82. Tak PP, Firestein GS (2001) NF-κB: a key role in inflammatory diseases. J Clin Invest 107:7–11

    PubMed  CAS  Google Scholar 

  83. Aggarwai BB (2004) Nuclear factor-κB: the enemy within. Cancer Cell 6:203–208

    Google Scholar 

  84. Al-Sadi R, Ye D, Said HM, Ma TY (2010) IL-1β-induced increase in intestinal epithelial tight junction permeability is mediated by MEKK-1 activation of canonical NF-κB pathway. Am J Pathol 177:2310–2322

    PubMed  CAS  Google Scholar 

  85. Al-Sadi R, Ye D, Dokladny K, Ma TY (2008) Mechanism of IL-1β-induced increase in intestinal epithelial tight junction permeability. J Immunol 180:5653–5661

    PubMed  CAS  Google Scholar 

  86. Kamm KE, Stull JT (2001) Dedicated myosin light chain kinases with diverse cellular functions. J Biol Chem 276:4527–4530

    PubMed  CAS  Google Scholar 

  87. Shen Q, Rigor RR, Pivetti CD, Wu MH, Yuan SY (2010) Myosin light chain kinase in microvascular endothelial barrier function. Cardiovasc Res 87:272–280

    PubMed  CAS  Google Scholar 

  88. Ivanov AI, Parkos CA, Nusrat A (2010) Cytoskeletal regulation of epithelial barrier function during inflammation. Am J Pathol 177:512–524

    PubMed  CAS  Google Scholar 

  89. Kumar S, Millis JT, Baglioni C (1992) Expression of interleukin 1-inducible genes and production of interleukin 1 by aging human fibroblasts. Proc Natl Acad Sci USA 89:4683–4687

    PubMed  CAS  Google Scholar 

  90. Dewberry RM, Crossman DC, Francis SE (2003) Interleukin-1 receptor antagonist (IL-1RN) genotype modulates the replicative capacity of human endothelial cells. Circ Res 92:1285–1287

    PubMed  CAS  Google Scholar 

  91. Maas-Szabowski N, Fusenig NE (1996) Interleukin-1-induced growth factor expression in postmitotic and resting fibroblasts. J Invest Dermatol 107:849–855

    PubMed  CAS  Google Scholar 

  92. Barland CO, Zettersten E, Brown BS, Ye J, Elias PM, Ghadially R (2004) Imiquimod-induced interleukin-1α stimulation improves barrier homeostasis in aged murine epidermis. J Invest Dermatol 122:330–336

    PubMed  CAS  Google Scholar 

  93. Ye J, Garg A, Calhoun C, Feingold KR, Elias PM, Ghadially R (2002) Alterations in cytokine regulation in aged epidermis: implications for permeability barrier homeostasis and inflammation. I. IL-1 gene family. Exp Dermatol 11:209–216

    PubMed  CAS  Google Scholar 

  94. Clermont Y (1972) Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol Rev 52:198–235

    PubMed  CAS  Google Scholar 

  95. Lie PPY, Cheng CY, Mruk DD (2011) The biology of the desmosome-like junction: a versatile anchoring junction and signal transducer in the seminiferous epithelium. Int Rev Cell Mol Biol 286:223–269

    PubMed  CAS  Google Scholar 

  96. Wong EWP, Cheng CY (2009) Polarity proteins and cell–cell interactions in the testis. Int Rev Cell Mol Biol 278:309–353

    PubMed  Google Scholar 

  97. Bardin CW, Cheng CY, Musto NA, Gunsalus GL (1988) The Sertoli cell. In: Knobil E, Neill JD, Ewing LL, Greenwald GS, Markert CL, Pfaff DW (eds) The physiology of reproduction, vol 1. Raven Press, New York, pp 933–974

    Google Scholar 

  98. Mruk DD, Cheng CY (2004) Sertoli–Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev 25:747–806

    PubMed  CAS  Google Scholar 

  99. Cheng CY, Mruk DD (2002) Cell junction dynamics in the testis: Sertoli–germ cell interactions and male contraceptive development. Physiol Rev 82:825–874

    PubMed  CAS  Google Scholar 

  100. Russell LD (1977) Movement of spermatocytes from the basal to the adluminal compartment of the rat testis. Am J Anat 148:313–328

    PubMed  CAS  Google Scholar 

  101. Parvinen M (1982) Regulation of the seminiferous epithelium. Endocr Rev 3:404–417

    PubMed  CAS  Google Scholar 

  102. Cheng CY, Mruk DD (2009) An intracellular trafficking pathway in the seminiferous epithelium regulating spermatogenesis: a biochemical and molecular perspective. Crit Rev Biochem Mol Biol 44:245–263

    PubMed  CAS  Google Scholar 

  103. Lie PPY, Cheng CY, Mruk DD (2009) Coordinating cellular events during spermatogenesis: a biochemical model. Trends Biochem Sci 34:366–373

    PubMed  CAS  Google Scholar 

  104. Cheng CY, Mruk DD (2010) A local autocrine axis in the testes that regulates spermatogenesis. Nat Rev Endocrinol 6:380–395

    PubMed  CAS  Google Scholar 

  105. O'Donnell L, Nicholls OK, O'Bryan MK, McLachlan RI, Stanton PG (2011) Spermiation: the process of sperm release. Spermatogenesis 1:14–35

    PubMed  Google Scholar 

  106. Li MWM, Mruk DD, Lee WM, Cheng CY (2009) Cytokines and junction restructuring events during spermatogenesis in the testis: an emerging concept of regulation. Cytokine Growth Factor Rev 20:329–338

    PubMed  CAS  Google Scholar 

  107. Jonsson CK, Zetterstrom RH, Holst M, Parvinen M, Soder O (1999) Constitutive expression of interleukin-1α messenger ribonucleic acid in rat Sertoli cells is dependent upon interaction with germ cells. Endocrinology 140:3755–3761

    PubMed  CAS  Google Scholar 

  108. Gerard N, Syed V, Bardin W, Genetet N, Jegou B (1991) Sertoli cells are the site of interleukin-1α synthesis in rat testis. Mol Cell Endocrinol 82:R13–R16

    PubMed  CAS  Google Scholar 

  109. Haugen TB, Landmark BF, Josefsen GM, Hansson V, Hogset A (1994) The mature form of interleukin-1α is constitutively expressed in immature male germ cells from rat. Mol Cell Endocrinol 105:R19–R23

    PubMed  CAS  Google Scholar 

  110. Zeyse D, Lunenfeld E, Beck M, Prinsloo I, Huleihel M (2000) Interleukin-1 receptor antagonist is produced by Sertoli cells in vitro. Endocrinology 141:1521–1527

    PubMed  CAS  Google Scholar 

  111. Rozwadowska N, Fiszer D, Jedrzejczak P, Kosicki W, Kurpisz M (2007) Interleukin-1 superfamily genes expression in normal or impaired human spermatogenesis. Genes Immun 8:100–107

    PubMed  CAS  Google Scholar 

  112. Gomez E, Morel G, Cavalier A, Lienard M, Haour F, Courtens J, Jegou B (1997) Type I and type II interleukin-1 receptor expression in rat, mouse and human testes. Biol Reprod 56:1513–1526

    PubMed  CAS  Google Scholar 

  113. Sultana T, Svechnikov K, Weber G, Soder O (2000) Molecular cloning and expression of a functionally different alternative splice variant of pro-interleukin-1α from the rat testis. Endocrinology 141:4413–4418

    PubMed  CAS  Google Scholar 

  114. Janitz M, Fiszer D, Lukaszyk A, Skorupski W, Kurpisz M (1995) Analysis of mRNA expression for interleukin-1 genes on human testicular cells. Immunol Lett 48:139–143

    PubMed  CAS  Google Scholar 

  115. Syed V, Stephan J, Gerard N, Legrand A, Parvinen M, Bardin CW, Jegou B (1995) Residual bodies activate Sertoli cell interleukin-1α (IL-1α) release, which triggers IL-6 production by an autocrine mechanism, through the lipoxygenase pathway. Endocrinology 136:3070–3078

    PubMed  CAS  Google Scholar 

  116. Wahab-Wahlgren A, Holst M, Ayele D, Sultana T, Parvinen M, Gustafsson K, Granholm T, Soder O (2000) Constitutive production of interleukin-1α mRNA and protein in the developing rat testis. Int J Androl 23:360–365

    PubMed  CAS  Google Scholar 

  117. Gerard N, Syed V, Jegou B (1992) Lipopolysaccharide, latex beads and residual bodies are potent activators of Sertoli cell interleukin-1α production. Biochem Biophys Res Commun 185:154–161

    PubMed  CAS  Google Scholar 

  118. Petersen C, Boitani C, Froysa B, Soder O (2002) Interleukin-1 is a potent growth factor for immature rat Sertoli cells. Mol Cell Endocrinol 186:37–47

    PubMed  CAS  Google Scholar 

  119. Petersen C, Svechnikov K, Froysa B, Soder O (2005) The p38 MAPK pathway mediates interleukin-1-induced Sertoli cell proliferation. Cytokine 32:51–59

    PubMed  CAS  Google Scholar 

  120. Pollanen P, Soder O, Parvinen M (1989) Interleukin-1α stimulation of spermatogonial proliferation in vivo. Reprod Fertil Dev 1:85–87

    PubMed  CAS  Google Scholar 

  121. Okuma Y, Saito K, O’Connor AE, Phillips DJ, de Kretser DM, Hedger MP (2005) 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 185:99–110

    PubMed  CAS  Google Scholar 

  122. Colon E, Svechnikov KV, Carlsson-Skwirut C, Bang P, Soder O (2005) Stimulation of steroidogenesis in immature rat Leydig cells evoked by interleukin-1α is potentiated by growth hormone and insulin-like growth factors. Endocrinology 146:221–230

    PubMed  CAS  Google Scholar 

  123. Bornstein SR, Rutkowski H, Vrezas I (2004) Cytokines and steroidogenesis. Mol Cell Endocrinol 215:135–141

    PubMed  CAS  Google Scholar 

  124. Calkins JH, Sigel MM, Nankin HR, Lin T (1988) Interleukin-1 inhibits Leydig cell steroidogenesis in primary culture. Endocrinology 123:1605–1610

    PubMed  CAS  Google Scholar 

  125. Lui WY, Lee WM, Cheng CY (2001) Transforming growth factor-β3 perturbs the inter-Sertoli tight junction permeability barrier in vitro possibly mediated via its effects on occludin, zonula occludens-1, and claudin-11. Endocrinology 142:1865–1877

    PubMed  CAS  Google Scholar 

  126. Li MWM, Xia W, Mruk DD, Wang CQF, Yan HHN, Siu MKY, Lui WY, Lee WM, Cheng CY (2006) Tumor necrosis factor α reversibly disrupts the blood–testis barrier and impairs Sertoli–germ cell adhesion in the seminiferous epithelium of adult rat testes. J Endocrinol 190:313–329

    PubMed  CAS  Google Scholar 

  127. Lie PPY, Mruk DD, Lee WM, Cheng CY (2009) Epidermal growth factor receptor pathway substrate 8 (Eps8) is a novel regulator of cell adhesion and the blood–testis barrier integrity in the seminiferous epithelium. FASEB J 23:2555–2567

    PubMed  CAS  Google Scholar 

  128. Lie PPY, Chan AYN, Mruk DD, Lee WM, Cheng CY (2010) Restricted Arp3 expression in the testis prevents blood–testis barrier disruption during junction restructuring at spermatogenesis. Proc Natl Acad Sci USA 107:11411–11416

    PubMed  CAS  Google Scholar 

  129. Goley ED, Welch MD (2006) The ARP2/3 complex: an actin nucleator comes of age. Nat Rev Mol Cell Biol 7:713–726

    PubMed  CAS  Google Scholar 

  130. Disanza A, Carlier MF, Stradal TEB, Didry D, Frittoli E, Confalonieri S, Croce A, Wehland J, Di Fiore PP, Scita G (2004) Eps8 controls actin-based motility by capping the barbed ends of actin filaments. Nat Cell Biol 6:1180–1188

    PubMed  CAS  Google Scholar 

  131. Disanza A, Mantoani S, Hertzog M, Gerboth S, Frittoli E, Steffen A, Berhoerster K, Kreienkamp H, Milanesi F, Di Fiore PP, Ciliberto A, Stradal TEB, Scita G (2006) Regulation of cell shape by Cdc42 is mediated by the synergic actin-bundling activity of the Eps8-IRSp53 complex. Nat Cell Biol 8:1337–1347

    PubMed  CAS  Google Scholar 

  132. Lie PPY, Mruk DD, Lee WM, Cheng CY (2010) Cytoskeletal dynamics and spermatogenesis. Philos Trans R Soc Lond B Biol Sci 365:1581–1592

    PubMed  CAS  Google Scholar 

  133. Vogl AW, Vaid KS, Guttman J (2008) The Sertoli cell cytoskeleton. In: Cheng CY (ed) Molecular mechanisms in spermatogenesis. Landes Bioscience/Springer Science + Business Media LLC, Austin, pp 186–221

    Google Scholar 

  134. Mruk DD, Silvestrini B, Cheng CY (2008) Anchoring junctions as drug targets: role in contraceptive development. Pharmacol Rev 60:146–180

    PubMed  CAS  Google Scholar 

  135. Yan HHN, Mruk DD, Lee WM, Cheng CY (2008) Blood–testis barrier dynamics are regulated by testosterone and cytokines via their differential effects on the kinetics of protein endocytosis and recycling in Sertoli cells. FASEB J 22:1945–1959

    PubMed  CAS  Google Scholar 

  136. Su L, Mruk DD, Lee WM, Cheng CY (2010) Differential effects of testosterone and TGF-β3 on endocytic vesicle-mediated protein trafficking events at the blood–testis barrier. Exp Cell Res 316:2945–2960

    PubMed  CAS  Google Scholar 

  137. Russell LD (1979) Further observations on tubulobulbar complexes formed by late spermatids and Sertoli cells in rat testis. Anat Rec 194:213–232

    PubMed  CAS  Google Scholar 

  138. Guttman J, Takai Y, Vogl AW (2004) Evidence that tubulobulbar complexes in the seminiferous epithelium are involved with internalization of adhesion junctions. Biol Reprod 71:548–559

    PubMed  CAS  Google Scholar 

  139. Vaid KS, Guttman JA, Babyak N, Deng W, McNiven MA, Mochizuki N, Finlay BB, Vogl AW (2007) The role of dynamin 3 in the testis. J Cell Physiol 210:644–654

    PubMed  CAS  Google Scholar 

  140. Young JS, Guttman JA, Vaid KS, Vogl AW (2009) Cortactin (CTTN), N-WASP (WASL), and clathrin (CLTC) are present at podosome-like tubulobulbar complexes in the rat testis. Biol Reprod 80:153–161

    PubMed  CAS  Google Scholar 

  141. Chapin RE, Wine RN, Harris MW, Borchers CH, Haseman JK (2001) Structure and control of a cell–cell adhesion complex associated with spermiation in rat seminiferous epithelium. J Androl 22:1030–1052

    PubMed  CAS  Google Scholar 

  142. Guttman JA, Obinata T, Shima J, Griswold M, Vogl AW (2004) Non-muscle cofilin is a component of tubulobulbar complexes in the testis. Biol Reprod 70:805–812

    PubMed  CAS  Google Scholar 

  143. Kaksonen M, Toret CP, Drubin DG (2006) Harnessing actin dynamics for clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 7:404–414

    PubMed  CAS  Google Scholar 

  144. Xia W, Wong EWP, Mruk DD, Cheng CY (2009) TGF-β3 and TNFα perturb blood–testis barrier (BTB) dynamics by accelerating the clathrin-mediated endocytosis of integral membrane proteins: a new concept of BTB regulation during spermatogenesis. Dev Biol 327:48–61

    PubMed  CAS  Google Scholar 

  145. Siu MKY, Lee WM, Cheng CY (2003) 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 144:371–387

    PubMed  CAS  Google Scholar 

  146. Xia W, Cheng CY (2005) TGF-β3 regulates anchoring junction dynamics in the seminiferous epithelium of the rat testis via the Ras/ERK signaling pathway: an in vivo study. Dev Biol 280:321–343

    PubMed  CAS  Google Scholar 

  147. Xia W, Mruk DD, Lee WM, Cheng CY (2006) Differential interactions between transforming growth factor-β3/TβR1, TAB 1, and CD2AP disrupt blood–testis barrier and Sertoli–germ cell adhesion. J Biol Chem 281:16799–16813

    PubMed  CAS  Google Scholar 

  148. Wang Y, Lui WY (2009) Opposite effects of interleukin-1α and transforming growth factor-β2 induce stage-specific regulation of junctional adhesion molecule-B gene in Sertoli cells. Endocrinology 150:2404–2412

    PubMed  CAS  Google Scholar 

  149. Horai R, Asano M, Sudo K, Kanuka H, Suzuki M, Nishihara M, Takahashi M, Iwakura Y (1998) Production of mice deficient in genes for interleukin (IL)-1α, Il-1β, IL-1α/β and IL-1 receptor antagonist shows that IL-1β is crucial in turpentine-induced fever development and glucocorticoid secretion. J Exp Med 187:1463–1475

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Research in the authors’ laboratory is supported by NICHD, NIH (R03 HD061401 to D.D.M.; R01 HD056034, R01 HD056034-02S1 and U54 HD029990 Project 5 to C.Y.C.).

Author information

Authors and Affiliations

  1. Center for Biomedical Research, Population Council, 1230 York Avenue, New York, NY, 10065, USA

    Pearl P. Y. Lie, C. Yan Cheng & Dolores D. Mruk

Authors
  1. Pearl P. Y. Lie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. Yan Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dolores D. Mruk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dolores D. Mruk.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lie, P.P.Y., Cheng, C.Y. & Mruk, D.D. The biology of interleukin-1: emerging concepts in the regulation of the actin cytoskeleton and cell junction dynamics. Cell. Mol. Life Sci. 69, 487–500 (2012). https://doi.org/10.1007/s00018-011-0760-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-011-0760-0

Keywords

Search

Navigation