Interleukin-6 disrupts blood-testis barrier through inhibiting protein degradation or activating phosphorylated ERK in Sertoli cells

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Zhang, Huijuan ^a   Yin, Yimeng ^a   Wang, Guishuan ^a   Liu, Zhimin ^a   Liu, Lin ^a   Sun, Fei ^a,b  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL; ARTICLE; BLOOD TESTIS BARRIER; CELL CULTURE; ENZYME ACTIVATION; MALE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; RAT; SERTOLI CELL; SIGNAL TRANSDUCTION; WISTAR RAT;

ANIMALS; BLOOD-TESTIS BARRIER; CELLS, CULTURED; ENZYME ACTIVATION; INTERLEUKIN-6; MALE; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RATS; RATS, WISTAR; SERTOLI CELLS;

EID: 84897640618     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep04260     Document Type: Article

References (50)

1. Dym, M. & Fawcett, D. W. The blood-testis barrier in the rat and the physiological compartmentation of the seminiferous epithelium. Biol Reprod 3, 308-326 (1970).
2. Mruk, D. D. & Cheng, C. Y. 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 (2004). (Pubitemid 39362296)
3. Kopera, I. A., Bilinska, B., Cheng, C. Y. & Mruk, D. D. Sertoli-germ cell junctions in the testis: a review of recent data. Philos Trans R Soc Lond B Biol Sci 365, 1593-1605 (2010).
4. Mruk, D. D. & Cheng, C. Y. Tight junctions in the testis: new perspectives. Philos Trans R Soc Lond B Biol Sci 365, 1621-1635 (2010).
5. Lui, W. Y. & Lee, W. M. Mechanisms of reorganization of cell-cell junctions in the testis. Front Biosci 13, 6775-6786 (2008).
6. Xia, W., Wong, E. W., Mruk, D. D. & Cheng, C. Y. TGF-beta3 and TNFalpha perturb blood-testis barrier (BTB) dynamics by accelerating the clathrinmediated endocytosis of integral membrane proteins: a new concept of BTB regulation during spermatogenesis. Dev Biol 327, 48-61 (2009).
7. Xia, W., Mruk, D. D., Lee, W. M. & Cheng, C. Y. Differential interactions between transforming growth factor-beta3/TbetaR1, TAB1, and CD2AP disrupt bloodtestis barrier and Sertoli-germ cell adhesion. J Biol Chem 281, 16799-16813 (2006).
8. Li, M.W. et al. Tumor necrosis factor {alpha} 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 (2006). (Pubitemid 44288369)
9. Lui, W. Y., Lee, W. M. & Cheng, C. Y. Transforming growth factor beta3 regulates the dynamics of Sertoli cell tight junctions via the p38 mitogen-activated protein kinase pathway. Biol Reprod 68, 1597-1612 (2003). (Pubitemid 36519763)
10. Lie, P. P., Cheng, C. Y. & Mruk, D. D. Interleukin-1alpha is a regulator of the blood-testis barrier. FASEB J 25, 1244-1253 (2011).
11. Perez, C. V. et al. Loss of occludin expression and impairment of blood-testis barrier permeability in rats with autoimmune orchitis: effect of interleukin 6 on Sertoli cell tight junctions. Biol Reprod 87, 122 (2012).
12. Bryniarski, K., Szczepanik, M., Ptak, M. & Ptak, W. Modulation of testicular macrophage activity by collagenase. Folia Histochem Cytobiol 43, 37-41 (2005). (Pubitemid 40347641)
13. Kern, S., Robertson, S. A., Mau, V. J. & Maddocks, S. Cytokine secretion by macrophages in the rat testis. Biol Reprod 53, 1407-1416 (1995).
14. Boockfor, F. R., Wang, D., Lin, T., Nagpal, M. L. & Spangelo, B. L. Interleukin-6 secretion from rat Leydig cells in culture. Endocrinology 134, 2150-2155 (1994). (Pubitemid 24142956)
15. Cudicini, C., Kercret, H., Touzalin, A. M., Ballet, F. & Jegou, B. Vectorial production of interleukin 1 and interleukin 6 by rat Sertoli cells cultured in a dual culture compartment system. Endocrinology 138, 2863-2870 (1997). (Pubitemid 27258518)
16. Rival, C., Theas, M. S., Guazzone, V. A. & Lustig, L. Interleukin-6 and IL-6 receptor cell expression in testis of rats with autoimmune orchitis. J Reprod Immunol 70, 43-58 (2006). (Pubitemid 43669097)
17. Potashnik, H. et al. Interleukin-6 expression during normal maturation of the mouse testis. Eur Cytokine Netw 16, 161-165 (2005). (Pubitemid 46638765)
18. Hakovirta, H., Syed, V., Jegou, B. & Parvinen, M. Function of interleukin-6 as an inhibitor of meiotic DNA synthesis in the rat seminiferous epithelium. Mol Cell Endocrinol 108, 193-198 (1995).
19. Boockfor, F. R. & Schwarz, L. K. Effects of interleukin-6, interleukin-2, and tumor necrosis factor alpha on transferrin release from Sertoli cells in culture. Endocrinology 129, 256-262 (1991).
20. Okuma, Y. et al. Regulation of activin A and inhibin B secretion by inflammatory mediators in adult rat Sertoli cell cultures. J Endocrinol 187, 125-134 (2005). (Pubitemid 41556408)
21. Lampiao, F. & du Plessis, S. S. TNF-alpha and IL-6 affect human sperm function by elevating nitric oxide production. Reprod Biomed Online 17, 628-631 (2008).
22. Syed, V. et al. Residual bodies activate Sertoli cell interleukin-1 alpha (IL-1 alpha) release, which triggers IL-6 production by an autocrine mechanism, through the lipoxygenase pathway. Endocrinology 136, 3070-3078 (1995).
23. Cudicini, C. et al. Human Leydig cells and Sertoli cells are producers of interleukins-1 and -6. J Clin Endocrinol Metab 82, 1426-1433 (1997). (Pubitemid 27200413)
24. Stephan, J. P., Syed, V. & Jegou, B. Regulation of Sertoli cell IL-1 and IL-6 production in vitro. Mol Cell Endocrinol 134, 109-118 (1997). (Pubitemid 27510877)
25. Li, R. et al. Expression of IL-1alpha, IL-6, TGF-beta, FasL and ZNF265 during sertoli cell infection by ureaplasma urealyticum. Cell Mol Immunol 6, 215-221, doi:10.1038/cmi.2009.29 (2009).
26. Siu, M. K., Wong, C. H., Lee, W. M. & Cheng, C. Y. Sertoli-germ cell anchoring junction dynamics in the testis are regulated by an interplay of lipid and protein kinases. J Biol Chem 280, 25029-25047 (2005). (Pubitemid 40934595)
27. Hirano, T., Nakajima, K. & Hibi, M. Signaling mechanisms through gp130: a model of the cytokine system. Cytokine Growth Factor Rev 8, 241-252 (1997). (Pubitemid 28202436)
28. Mihara, M., Hashizume, M., Yoshida, H., Suzuki, M. & Shiina, M. IL-6/IL-6 receptor system and its role in physiological and pathological conditions. Clin Sci (Lond) 122, 143-159 (2012).
29. Cheng, C. Y. & Mruk, D. D. A local autocrine axis in the testes that regulates spermatogenesis. Nat Rev Endocrinol 6, 380-395 (2010).
30. Cheng, C. Y. & Mruk, D. D. An intracellular trafficking pathway in the seminiferous epithelium regulating spermatogenesis: a biochemical and molecular perspective. Crit Rev Biochem Mol Biol 44, 245-263 (2009).
31. Pelletier, R. M. & Byers, S. W. The blood-testis barrier and Sertoli cell junctions: structural considerations. Microsc Res Tech 20, 3-33 (1992).
32. Ogawa, Y. et al. Cadmium exposure increases susceptibility to testicular autoimmunity in mice. J Appl Toxicol (2012).
33. Wu, H. et al. Cytokines produced by microwave-radiated Sertoli cells interfere with spermatogenesis in rat testis. Andrologia 44 Suppl 1, 590-599 (2012).
34. Bialas, M. et al. The role of IL-6, IL-10, TNF-alpha and its receptors TNFR1 and TNFR2 in the local regulatory system of normal and impaired human spermatogenesis. Am J Reprod Immunol 62, 51-59 (2009).
35. Yamaguchi, K., Ishikawa, T., Kondo, Y. & Fujisawa, M. Cisplatin regulates Sertoli cell expression of transferrin and interleukins. Mol Cell Endocrinol 283, 68-75 (2008).
36. Schuppe, H. C. et al. Chronic orchitis: a neglected cause of male infertility? Andrologia 40, 84-91 (2008).
37. Jacobo, P., Guazzone, V. A., Theas, M. S. & Lustig, L. Testicular autoimmunity. Autoimmun Rev 10, 201-204 (2011).
38. Li, F. Y. & Li, Y. Interleukin-6, desmosome and tight junction protein expression levels in reflux esophagitis-affected mucosa. World J Gastroentero 15, 3621-3630 (2009).
39. Suzuki, T., Yoshinaga, N. & Tanabe, S. Interleukin-6 (IL-6) regulates claudin-2 expression and tight junction permeability in intestinal epithelium. J Biol Chem 286, 31263-31271 (2011).
40. Lui, W. Y., Lee, W. M. & Cheng, C. Y. Rho GTPases and spermatogenesis. Biochim Biophys Acta 1593, 121-129 (2003). (Pubitemid 36173480)
41. Siu, M. K. & Cheng, C. Y. Dynamic cross-talk between cells and the extracellular matrix in the testis. Bioessays 26, 978-992 (2004). (Pubitemid 39273071)
42. Wong, C. H. & Cheng, C. Y. Mitogen-activated protein kinases, adherens junction dynamics, and spermatogenesis: a review of recent data. Dev Biol 286, 1-15 (2005). (Pubitemid 41394043)
43. Chen, M. et al. Effect of heat stress on expression of junction-associated molecules and upstream factors androgen receptor and Wilms' tumor 1 in monkey sertoli cells. Endocrinology 149, 4871-4882 (2008).
44. MICHELA, GALDIERI, ELIO, ZIPARO, FIORETTA, PALOMBI, MARIO, A. RUSSO & STEFANINI, M. Pure Sertoli Cell Cultures: A New Model for the Study of Somatic-Germ Cell Interactions. Journal of Andrology 2, 249-254 (1981).
45. Byers, S. W., Hadley, M. A., Djakiew, D. & Dym, M. Growth and characterization of polarized monolayers of epididymal epithelial cells and Sertoli cells in dual environment culture chambers. J Androl 7, 59-68 (1986). (Pubitemid 16132311)
46. Chung, S. S., Lee, W. M. & Cheng, C. Y. Study on the formation of specialized inter-Sertoli cell junctions in vitro. J Cell Physiol 181, 258-272 (1999). (Pubitemid 29463641)
47. Yan, H. H., Mruk, D. D., Lee, W.M. & Cheng, C. Y. 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 (2008). (Pubitemid 351811471)
48. Lui, W. Y., Lee, W. M. & Cheng, C. Y. Transforming growth factor-beta3 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 (2001). (Pubitemid 32405944)
49. Josephine Grima, Connie C. S. Wong, Li-ji Zhu, Shu-dong Zong & Cheng, C. Y. Testin Secreted by Sertoli Cells Is Associated with the Cell Surface, and Its Expression Correlates with the Disruption of Sertoli-Germ Cell Junctions but Not the Inter-Sertoli Tight Junction. J. Biol. Chem 273, 21040-21053 (1998). (Pubitemid 28385389)
50. Yao, G. et al. MicroRNA-224 is involved in transforming growth factor-betamediated mouse granulosa cell proliferation and granulosa cell function by targeting Smad4. Mol Endocrinol 24, 540-551 (2010).