Role of non-receptor protein tyrosine kinases in spermatid transport during spermatogenesis

Seminars in Cell and Developmental Biology

Volumn 30, Issue , 2014, Pages 65-74

  Wan, H T ^a   Mruk, Dolores D ^a   Tang, Elizabeth I ^a   Xiao, Xiang ^a   Cheng, Yan Ho ^b   Wong, Elissa W P ^a   Wong, Chris K C ^c   Cheng, C Yan ^a  

^a POPULATION COUNCIL   (United States)

^b RICHMOND UNIVERSITY MEDICAL CENTER   (United States)

^c HONG KONG BAPTIST UNIVERSITY   (Hong Kong)

Author keywords

Blood testis barrier; C Src; C Yes; Cell adhesion; FAK; Seminiferous epithelial cycle; Spermatogenesis; Spermiation; Spermiogenesis; Testis

Indexed keywords

ACTIN; CYTOPLASM PROTEIN; FOCAL ADHESION KINASE; NON RECEPTOR PROTEIN TYROSINE KINASE; PHOSPHOTRANSFERASE; PROTEIN KINASE YES; PROTEIN TYROSINE KINASE; TYROSINE; UNCLASSIFIED DRUG;

ACTIN FILAMENT; CELL MEMBRANE; CYTOSKELETON; HUMAN; INFERTILITY; INTRACELLULAR TRANSPORT; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SERTOLI CELL; SPERMATID; SPERMATOGENESIS; ANIMAL; BLOOD TESTIS BARRIER; CYTOLOGY; ENZYMOLOGY; MALE; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; SEMINIFEROUS TUBULE EPITHELIUM; SIGNAL TRANSDUCTION; SPERMATOZOON MIGRATION;

EUKARYOTA;

ANIMALS; BLOOD-TESTIS BARRIER; HUMANS; MALE; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-TYROSINE KINASES; SEMINIFEROUS EPITHELIUM; SERTOLI CELLS; SIGNAL TRANSDUCTION; SPERM TRANSPORT; SPERMATIDS; SPERMATOGENESIS;

EID: 84901633273     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2014.04.013     Document Type: Review

References (117)

1. Sharpe R.M. Regulation of spermatogenesis. The physiology of reproduction 1994, 1363-1434. Raven Press, New York. E. Knobil, J.D. Neill (Eds.).
2. de Kretser D.M., Kerr J.B. The cytology of the testis. The physiology of reproduction 1988, vol. 1:837-932. Raven Press, New York.
3. O'Donnell L., Robertson K.M., Jones M.E., Simpson E.R. Estrogen and spermatogenesis. Endocr Rev 2001, 22:289-318.
4. Carreau S., Hess R.A. Oestrogens and spermatogenesis. Philos Trans R Soc Lond B: Biol Sci 2010, 365:1517-1535.
5. Verhoeven G., Willems A., Denolet E., Swinnen J.V., De Gendt K. Androgens and spermatogenesis: lessons from transgenic mouse models. Philos Trans R Soc Lond B: Biol Sci 2010, 365:1537-1556.
6. Ge R.S., Chen G., Hardy M.P. The role of the Leydig cell in spermatogenic function. Adv Exp Med Biol 2008, 636:255-269.
7. Smith L.B., Walker W.H. The regulation of spermatogenesis by androgens. Semin Cell Dev Biol 2014, 30:2-13.
8. Carreau S., Wolczynski S., Galeraud-Denis I. Aromatase, estrogens and human male reproduction. Philos Trans R Soc Lond B: Biol Sci 2010, 365:1571-1579.
9. Ferlin A., Selice R., Carraro U., Foresta C. Testicular function and bone metabolism - beyond testosterone. Nat Rev Endocrinol 2013, 9:548-554.
10. Carreau S. Estrogen roles in spermatogenesis. Immun Endocr Metab Agents Med Chem 2008, 8:59-65.
11. McLachlan R.I., O'Donnell L., Meachem S.J., Stanton P.G., De Kretser D.M., Pratis K., et al. Identification of specific sites of hormonal regulation in spermatogenesis in rats, monkeys, and man. Recent Prog Horm Res 2002, 57:149-179.
12. Wang R.S., Yeh S., Tzeng C.R., Chang C. Androgen receptor roles in spermatogenesis and fertility: lessons from testicular cell-specific androgen receptor knockout mice. Endocr Rev 2009, 30:119-132.
13. Schlatt S., Ehmcke J. Regulation of spermatogenesis: an evolutionary biologist's perspective. Semin Cell Dev Biol 2014, PMID: 24685618 [in press]. 10.1016/j.semcdb.2014.03.007.
14. de Rooij D.G. The spermatogonial stem cell niche. Microsc Res Tech 2009, 72:580-585.
15. Cheng C.Y.E. Biology and regulation of blood-tissue barriers 2012, 1-361. Landes Bioscience/Springer Science+Business Media, LLC, Austin, TX.
16. Cheng C.Y., Mruk D.D. The blood-testis barrier and its implication in male contraception. Pharmacol Rev 2012, 64:16-64.
17. Franca L.R., Auharek S.A., Hess R.A., Dufour J.M., Hinton B.T. Blood-tissue barriers: morphofunctional and immunological aspects of the blood-testis and blood-epididymal barriers. Adv Exp Med Biol 2012, 763:237-259.
18. Pelletier R.M. The blood-testis barrier: the junctional permeability, the proteins and the lipids. Prog Histochem Cytochem 2011, 46:49-127.
19. Cheng C.Y., Mruk D.D. Cell junction dynamics in the testis: Sertoli-germ cell interactions and male contraceptive development. Physiol Rev 2002, 82:825-874.
20. 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 2004, 25:747-806.
21. Ivanov A.I. Structure and regulation of intestinal epithelial tight junctions. Adv Exp Med Biol 2012, 763:132-148.
22. Turner J.R. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 2009, 9:799-809.
23. Campbell M., Humphries P. The blood-retina barrier: tight junctions and barrier modulation. Adv Exp Med Biol 2012, 763:70-84.
24. Easton A.S. Regulation of permeability across the blood-brain barrier. Adv Exp Med Biol 2012, 763:1-19.
25. Russell L.D., Peterson R.N. Sertoli cell junctions: morphological and functional correlates. Int Rev Cytol 1985, 94:177-211.
26. Vogl A.W., Vaid K.S., Guttman J.A. The Sertoli cell cytoskeleton. Adv Exp Med Biol 2008, 636:186-211.
27. Enders G. Sertoli-Sertoli and Sertoli-germ cell communications. The Sertoli cell 1993, 447-460. Cache River Press, Clearwater. L. Russell, M. Griswold (Eds.).
28. Byers S., Pelletier R.M., Suarez-Quain C. Sertoli cell junctions and the seminiferous epithelium barrier. The Sertoli cell 1993, 431-446. Cache River Press, Clearwater. L.D. Russell, M.D. Griswold (Eds.).
29. Mruk D.D., Cheng C.Y. Desmosomes in the testis. Moving into an unchartered territory. Spermatogenesis 2011, 1:47-51.
30. Lie P.P.Y., Cheng C.Y., Mruk D.D. The biology of the desmosome-like junction: a versatile anchoring junction and signal transducer in the seminiferous epithelium. Int Rev Cell Mol Biol 2011, 286:223-269.
31. Cheng C.Y., Wong E.W.P., Lie P.P.Y., Li M.W.M., Mruk D.D., Yan H.H.N., et al. Regulation of blood-testis barrier dynamics by desmosome, gap junction, hemidesmosome and polarity proteins: an unexpected turn of events. Spermatogenesis 2011, 1:105-115.
32. Russell L.D. Movement of spermatocytes from the basal to the adluminal compartment of the rat testis. Am J Anat 1977, 148:313-328.
33. Smith B.E., Braun R.E. Germ cell migration across Sertoli cell tight junctions. Science 2012, 338:798-802.
34. Yan H.H.N., 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 2008, 22:1945-1959.
35. Mruk D.D., Cheng C.Y. Delivering non-hormonal contraceptives to men: advances and obstacles. Trends Biotechnol 2008, 26:90-99.
36. Cheng Y.H., Wong E.W.P., Cheng C.Y. Cancer/testis (CT) antigens, carcinogenesis and spermatogenesis. Spermatogenesis 2011, 1:209-220.
37. Su W.H., Mruk D.D., Cheng C.Y. Regulation of actin dynamics and protein trafficking during spermatogenesis - insights into a complex process. Crit Rev Biochem Mol Biol 2013, 48:153-172.
38. Cheng C.Y., Mruk D.D. A local autocrine axis in the testes that regulates spermatogenesis. Nat Rev Endocrinol 2010, 6:380-395.
39. Cheng C.Y., Wong E.W.P., Yan H.H.N., Mruk D.D. Regulation of spermatogenesis in the microenvironment of the seminiferous epithelium: new insights and advances. Mol Cell Endocrinol 2010, 315:49-56.
40. 397 exhibit antagonistic effects on blood-testis barrier dynamics in the rat. Proc Natl Acad Sci USA 2012, 109:12562-12567.
41. Xiao X., Mruk D.D., Lee W.M., Cheng C.Y. c-Yes regulates cell adhesion at the blood-testis barrier and the apical ectoplasmic specialization in the seminiferous epithelium of rat testes. Int J Biochem Cell Biol 2011, 43:651-665.
42. Xiao X., Mruk D.D., Cheng C.Y. c-Yes regulates cell adhesion at the apical ectoplasmic specialization-blood-testis barrier axis via its effects on protein recruitment and distribution. Am J Physiol Endocrinol Metab 2013, 304:E145-E159.
43. Xiao X., Mruk D.D., Cheng F.L., Cheng C.Y. c-Src and c-Yes are two unlikely partners of spermatogenesis and their roles in blood-testis barrier dynamics. Adv Exp Med Biol 2012, 763:295-317.
44. Vogl A.W., Young J.S., Du M. New insights into roles of tubulobulbar complexes in sperm release and turnover of blood-testis barrier. Int Rev Cell Mol Biol 2013, 303:319-355.
45. Russell L.D. Spermatid-Sertoli tubulobulbar complexes as devices for elimination of cytoplasm from the head region in late spermatids of the rat. Anat Rec 1979, 194:233-246.
46. Russell L.D. Observations on rat Sertoli ectoplasmic ('junctional') specializations in their association with germ cells of the rat testis. Tissue Cell 1977, 9:475-498.
47. Li S.Y.T., Mruk D.D., Cheng C.Y. Focal adhesion kinase is a regulator of F-actin dynamics. New insights from studies in the testis. Spermatogenesis 2013, 3:e25385. PMID: 24381802, PMCID: PMC3861170. 10.4161/spermatogenesis.25385.
48. 397 regulates spermatid adhesion in the rat testis via its effects on F-actin organization at the ectoplasmic specialization. Am J Physiol Endocrinol Metab 2013, 305:E687-E699.
49. Wong C.H., Xia W., Lee N.P.Y., Mruk D.D., Lee W.M., Cheng C.Y. Regulation of ectoplasmic specialization dynamics in the seminiferous epithelium by focal adhesion-associated proteins in testosterone-suppressed rat testes. Endocrinology 2005, 146:1192-1204.
50. Siu M.K.Y., Mruk D.D., Lee W.M., Cheng C.Y. Adhering junction dynamics in the testis are regulated by an interplay of β1-integrin and focal adhesion complex (FAC)-associated proteins. Endocrinology 2003, 144:2141-2163.
51. Yan H.H.N., Mruk D.D., Wong E.W.P., Lee W.M., Cheng C.Y. An autocrine axis in the testis that coordinates spermiation and blood-testis barrier restructuring during spermatogenesis. Proc Natl Acad Sci USA 2008, 105:8950-8955.
52. Su L., Mruk D.D., Lie P.P.Y., Silvestrini B., Cheng C.Y. A peptide derived from laminin-γ3 reversibly impairs spermatogenesis in rats. Nat Commun 2012, 3:1185. 10.1038/ncomms2171.
53. 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 2009, 44:245-263.
54. Kowalczyke A.P., Green K.J. Structure, function, and regulation of desmosomes. Prog Mol Biol Transl Sci 2013, 116:95-118.
55. O'Donnell L., O'Bryan M.K. Microtubules and spermatogenesis. Semin Cell Dev Biol 2014, 30:45-54.
56. Tang E.I., Mruk D.D., Cheng C.Y. MAP/microtubule affinity-regulating kinases, microtubule dynamics, and spermatogenesis. J Endocrinol 2013, 217:R13-R23.
57. Kierszenbaum A.L., Rivkin E., Ters L.L. Acroplaxome, an F-actin-keratin-containing plate, anchors the acrosome to the nucleus during shaping of the spermatid head. Mol Biol Cell 2003, 14:4628-4640.
58. Kierszenbaum A.L., Rivkin E., Tres L.L. Molecular biology of sperm head shaping. Soc Reprod Fertil Suppl 2007, 65:33-43.
59. Kierszenbaum A.L., Tres L.L. The acrosome-acroplaxome-manchette complex and the shaping of the spermatid head. Arch Histol Cytol 2004, 67:271-284.
60. Franke W., Grund C., Schmid E. Intermediate-sized filaments present in Sertoli cells are of the vimentin type. Eur J Cell Biol 1979, 19:269-275.
61. Aumuller G., Steinbruck M., Krause W., Wagner H.J. Distribution of vimentin-type intermediate filaments in Sertoli cells of the human testis, normal and pathologic. Anat Embryol 1988, 178:129-136.
62. Vogl A.W. Distribution and function of organized concentrations of actin filaments in mammalian spermatogenic cells and Sertoli cells. Int Rev Cytol 1989, 119:1-56.
63. Lie P.P.Y., Mruk D.D., Lee W.M., Cheng C.Y. Cytoskeletal dynamics and spermatogenesis. Philos Trans R Soc Lond B: Biol Sci 2010, 365:1581-1592.
64. Russell L.D., Goh J.C., Rashed R.M.A., Vogl A.W. The consequences of actin disruption at Sertoli ectoplasmic specialization sites facing spermatids after in vivo exposure of rat testis to cytochalasin D. Biol Reprod 1988, 39:105-118.
65. Fawcett D. Ultrastructure and function of the Sertoli cell. Handbook of physiology 1975, 21-25. American Physiological Society, Washington, DC. D. Hamilton, R. Greep (Eds.).
66. Russell L.D. Observations on the inter-relationships of Sertoli cells at the level of the blood-testis barrier: evidence for formation and resorption of Sertoli-Sertoli tubulobulbar complexes during the spermatogenic cycle of the rat. Am J Anat 1979, 155:259-279.
67. Kierszenbaum A.L. Mammalian spermatogenesis in vivo and in vitro: a partnership of spermatogenic and somatic cell lineages. Endocr Rev 1994, 15:116-134.
68. Kierszenbaum A.L. Keratins: unraveling the coordinated construction of scaffolds in spermatogenic cells. Mol Reprod Dev 2002, 61:1-2.
69. Amlani S., Vogl A. Changes in the distribution of microtubules and intermediate filaments in mammalian Sertoli cells during spermatogenesis. Anat Rec 1988, 220:143-160.
70. Aumuller G., Schulze C., Viebahn C. Intermediate filaments in Sertoli cells. Microsc Res Tech 1992, 20:50-72.
71. Tanaka H., Iguchi N., de Carvalho C., Tadokoro Y., Yomogida K., Nishimune Y. Novel actin-like proteins T-ACTIN 1 and T-ACTIN 2 are differentially expressed ifn the cytoplasm and nucleus of mouse haploid germ cells. Biol Reprod 2003, 69:475-482.
72. Coulombe P.A., Wong P. Cytoplasmic intermediate filaments revealed as dynamic and multipurpose scaffolds. Nat Cell Biol 2004, 6:699-706.
73. Toivola D.M., Tao G.Z., Habtezion A., Liao J., Omary M.B. Cellular integrity plus: organelle-related and protein-targeting functions of intermediate filaments. Trends Cell Biol 2005, 15:608-617.
74. Tang E.I., Xiao X., Mruk D.D., Qian X.J., Mok K.W., Jenardhanan P., et al. Microtubule affinity-regulated kinase 4 (MARK4) is a component of the ectoplasmic specialization in the rat testis. Spermatogenesis 2012, 2:117-126.
75. Vogl A. Changes in the distribution of microtubules in rat Sertoli cells during spermatogenesis. Anat Rec 1988, 222:34-41.
76. Palombi F., Salanova M., Tarone G., Farini D., Stefanini M. Distribution of β1 integrin subunit in rat seminiferous epithelium. Biol Reprod 1992, 47:1173-1182.
77. Salanova M., Stefanini M., De Curtis I., Palombi F. Integrin receptor α6β1 is localized at specific sites of cell-to-cell contact in rat seminiferous epithelium. Biol Reprod 1995, 52:79-87.
78. Ozaki-Kuroda K., Nakanishi H., Ohta H., Tanaka H., Kurihara H., Mueller S., et al. Nectin couples cell-cell adhesion and the actin scaffold at heterotypic testicular junctions. Curr Biol 2002, 12:1145-1150.
79. Siu M.K.Y., Wong C.H., Xia W., Mruk D.D., Lee W.M., Cheng C.Y. The β1-integrin-p-FAK-p130Cas-DOCK180-RhoA-vinculin is a novel regulatory protein complex at the apical ectoplasmic specialization in adult rat testes. Spermatogenesis 2011, 1:73-86.
80. Gliki G., Ebnet K., Aurrand-Lions M., Imhof B.A., Adams R.H. Spermatid differentiation requires the assembly of a cell polarity complex downstream of junctional adhesion molecule-C. Nature 2004, 431:320-324.
81. Lee N.P.Y., Mruk D.D., Lee W.M., Cheng C.Y. Is the cadherin/catenin complex a functional unit of cell-cell-actin-based adherens junctions (AJ) in the rat testis. Biol Reprod 2003, 68:489-508.
82. Lie P.P.Y., Mruk D.D., Lee W.M., Cheng C.Y. 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 2009, 23:2555-2567.
83. Qian X., Mruk D.D., Wong E.W.P., Lie P.P.Y., Cheng C.Y. Palladin is a regulator of actin filament bundles at the ectoplasmic specialization in the rat testis. Endocrinology 2013, 154:1907-1920.
84. Lie P.P.Y., Chan A.Y.N., Mruk D.D., Lee W.M., Cheng C.Y. Restricted Arp3 expression in the testis prevents blood-testis barrier disruption during junction restructuring at spermatogenesis. Proc Natl Acad Sci USA 2010, 107:11411-11416.
85. Su W.H., Mruk D.D., Lie P.P.Y., Lui W.Y., Cheng C.Y. Filamin A is a regulator of blood-testis barrier assembly during postnatal development in the rat testis. Endocrinology 2012, 153:5023-5035.
86. Serrels B., Serrels A., Brunton V.G., Holt M., McLean G.W., Gray C.H., et al. Focal adhesion kinase controls actin assembly via a FERM-mediated interaction with the Arp2/3 complex. Nat Cell Biol 2007, 9:1046-1056.
87. Tang H., Li A., Bi J., Veltman D.M., Zech T., Spence H.J., et al. Loss of Scar/WAVE complex promotes N-WASP- and FAK-dependent invasion. Curr Biol 2013, 23:107-117.
88. Hubbard S.R., Till J.H. Protein tyrosine kinase structure and function. Annu Rev Biochem 2000, 69:373-398.
89. Goupil S., La Salle S., Trasler J.M., Bordeleau L.J., Leclerc P. Developmental expression of Src-related tyrosine kinases in the mouse testis. J Androl 2011, 32:95-110.
90. Hall J.E., Fu W., Schaller M.D. Focal adhesion kinase: exploring FAK structure to gain insight into function. Int Rev Cell Mol Biol 2011, 288:185-225.
91. Siu E.R., Wong E.W.P., Mruk D.D., Sze K.L., Porto C.S., Cheng C.Y. An occludin-focal adhesion kinase protein complex at the blood-testis barrier: a study using the cadmium model. Endocrinology 2009, 150:3336-3344.
92. Broussard J.A., Webb D.J., Kaverina I. Asymmetric focal adhesion disassembly in motile cells. Curr Opin Cell Biol 2008, 20:85-90.
93. Boutros T., Chevet E., Metrakos P. Mitogen-activated protein (MAP) kinase/MAP kinase phosphatase regulation: roles in cell growth, death, and cancer. Pharmacol Rev 2008, 60:261-310.
94. Cheng C.Y., Mruk D.D. Regulation of blood-testis barrier dynamics by focal adhesion kinase (FAK). An unexpected turn of events. Cell Cycle 2009, 8:3493-3499.
95. Beardsley A., Robertson D.M., O'Donnell L. A complex containing α6β1-integrin and phosphorylated focal adhesion kinase between Sertoli cells and elongated spermatids during spermatid release from the seminiferous epithelium. J Endocrinol 2006, 190:759-770.
96. Siu M.K.Y., 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 2005, 280:25029-25047.
97. Siu E.R., Wong E.W.P., Mruk D.D., Porto C.S., Cheng C.Y. Focal adhesion kinase is a blood-testis barrier regulator. Proc Natl Acad Sci USA 2009, 106:9298-9303.
98. Cheng C.Y., Wong E.W.P., Lie P.P.Y., Li M.W.M., Su L., Siu E.R., et al. Environmental toxicants and male reproductive function. Spermatogenesis 2011, 1:2-13.
99. Wong E.W.P., Mruk D.D., Lee W.M., Cheng C.Y. Par3/Par6 polarity complex coordinates apical ectoplasmic specialization and blood-testis barrier restructuring during spermatogenesis. Proc Natl Acad Sci USA 2008, 105:9657-9662.
100. Chen Y.M., Lee N.P.Y., Mruk D.D., Lee W.M., Cheng C.Y. Fer kinase/Fer T and adherens junction dynamics in the testis: an in vitro and in vivo study. Biol Reprod 2003, 69:656-672.
101. Mruk D.D., Silvestrini B., Cheng C.Y. Anchoring junctions as drug targets: role in contraceptive development. Pharmacol Rev 2008, 60:146-180.
102. Mitra S.K., Schlaepfer D.D. Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr Opin Cell Biol 2006, 18:516-523.
103. Thomas S., Brugge J. Cellular functions regulated by Src family kinases. Annu Rev Cell Dev Biol 1997, 13:513-609.
104. Frame M.C. Newest findings on the oldest oncogene: how activated src does it. J Cell Sci 2004, 117:989-998.
105. Bolos V., Gasent J.M., Lopez-Tarruella S., Grande E. The dual kinase complex FAK-Src as a promising therapeutic target in cancer. Onco Targets Ther 2010, 3:83-97.
106. Wang W., Wine R.N., Chapin R.E. Rat testicular Src: normal distribution and involvement in ethylene glycol monomethyl ether-induced apoptosis. Toxicol Appl Pharmacol 2000, 163:125-134.
107. Wine R., Chapin R. Adhesion and signaling proteins spatiotemporally associated with spermiation in the rat. J Androl 1999, 20:198-213.
108. Lee N.P.Y., Cheng C.Y. Protein kinases and adherens junction dynamics in the seminiferous epithelium of the rat testis. J Cell Physiol 2005, 202:344-360.
109. Yan H.H.N., Cheng C.Y. Laminin α3 forms a complex with β3 and γ3 chains that serves as the ligand for α6β1-integrin at the apical ectoplasmic specialization in adult rat testes. J Biol Chem 2006, 281:17286-17303.
110. Wong E.W.P., Cheng C.Y. NC1 domain of collagen α3(IV) derived from the basement membrane regulates Sertoli cell blood-testis barrier dynamics. Spermatogenesis 2013, 3:e25465. [PMID: 23885308; PMCID: PMC3710226]. 10.4161/spmg.25465.
111. Siu M.K.Y., Lee W.M., Cheng C.Y. The interplay of collagen IV, tumor necrosis factor-α, gelatinase B (matrix metalloprotease-9), and tissue inhibitor of metalloprotease-1 in the basal lamina regulates Sertoli cell-tight junction dynamics in the rat testis. Endocrinology 2003, 144:371-387.
112. Li M.W.M., Mruk D.D., Lee W.M., Cheng C.Y. Cytokines and junction restructuring events during spermatogenesis in the testis: an emerging concept of regulation. Cytokine Growth Factor Rev 2009, 20:329-338.
113. Xia W., Mruk D.D., Lee W.M., Cheng C.Y. Cytokines and junction restructuring during spermatogenesis - a lesson to learn from the testis. Cytokine Growth Factor Rev 2005, 16:469-493.
114. Lui W.Y., Cheng C.Y. Regulation of cell junction dynamics by cytokines in the testis - a molecular and biochemical perspective. Cytokine Growth Factor Rev 2007, 18:299-311.
115. Su W.H., Mruk D.D., Cheng C.Y. Filamin A: a regulator of blood-testis barrier assembly during post-natal development. Spermatogenesis 2012, 2:73-78.
116. Li M.W.M., Xiao X., Mruk D.D., Lam Y.L., Lee W.M., Lui W.Y., et al. Actin binding protein drebrin E is involved in junction dynamics during spermatogenesis. Spermatogenesis 2011, 1:123-136.
117. Siu M.K.Y., Cheng C.Y. Interactions of proteases, protease inhibitors, and the β1 integrin/laminin γ3 protein complex in the regulation of ectoplasmic specialization dynamics in the rat testis. Biol Reprod 2004, 70:945-964.