N-WASP Is Required for Structural Integrity of the Blood-Testis Barrier

PLoS Genetics

Volumn 10, Issue 6, 2014, Pages

  Xiao, Xiang ^a   Mruk, Dolores D ^a   Tang, Elizabeth I ^a   Massarwa, R'ada ^b   Mok, Ka Wai ^a   Li, Nan ^a   Wong, Chris K C ^c   Lee, Will M ^d   Snapper, Scott B ^e   Shilo, Ben Zion ^b   Schejter, Eyal D ^b   Cheng, C Yan ^a  

^a POPULATION COUNCIL   (United States)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c HONG KONG BAPTIST UNIVERSITY   (Hong Kong)

^d UNIVERSITY OF HONG KONG   (Hong Kong)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CELL PROTEIN; FAK PROTEIN; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; TYROSINE; UNCLASSIFIED DRUG; ACTIN RELATED PROTEIN 2-3 COMPLEX; WASL PROTEIN, MOUSE;

ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD TESTIS BARRIER; CELL MATURATION; CONTROLLED STUDY; GENE DISRUPTION; GERM CELL; MALE; MEIOSIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SEMINIFEROUS TUBULE; SERTOLI CELL; SPERMATOGENESIS; ANIMAL; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; SEMINIFEROUS TUBULE EPITHELIUM; SPERMATID; SPERMATOCYTE; TESTIS;

ACTIN-RELATED PROTEIN 2-3 COMPLEX; ACTINS; ANIMALS; BLOOD-TESTIS BARRIER; MALE; MICE; SEMINIFEROUS EPITHELIUM; SERTOLI CELLS; SPERMATIDS; SPERMATOCYTES; SPERMATOGENESIS; TESTIS; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

EID: 84903434710     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004447     Document Type: Article

References (52)

1. de Kretser DM, Kerr JB (1988) The cytology of the testis. In: Knobil E, Neill JB, Ewing LL, Greenwald GS, Markert CL, et al., editors. The Physiology of Reproduction Vol 1. New York: Raven Press. pp. 837-932.
2. Cheng CY, Mruk DD, (2012) The blood-testis barrier and its implication in male contraception. Pharmacol Rev 64: 16-64.
3. Franca LR, Auharek SA, Hess RA, Dufour JM, Hinton BT, (2012) Blood-tissue barriers: Morphofunctional and immunological aspects of the blood-testis and blood-epididymal barriers. Adv Exp Med Biol 763: 237-259.
4. Vogl AW, Vaid KS, Guttman JA, (2008) The Sertoli cell cytoskeleton. Adv Exp Med Biol 636: 186-211.
5. Russell LD, Peterson RN, (1985) Sertoli cell junctions: morphological and functional correlates. Int Rev Cytol 94: 177-211.
6. Cheng CY, Mruk DD, (2010) A local autocrine axis in the testes that regulates spermatogenesis. Nature Rev Endocrinol 6: 380-395.
7. Wang CQF, Cheng CY, (2007) A seamless trespass: germ cell migration across the seminiferous epithelium during spermatogenesis. J Cell Biol 178: 549-556.
8. Russell LD, (1977) Movement of spermatocytes from the basal to the adluminal compartment of the rat testis. Am J Anat 148: 313-328.
9. Cheng CY, Lie PPY, Mok KW, Cheng YH, Wong EWP, et al. (2011) Interactions of laminin β3 fragment with β1-integrin receptor: a revisit of the apical ES-BTB-hemidesmosome functional axis in the testis. Spermatogenesis 1: 174-185.
10. 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.
11. Kurisu S, Takenawa T, (2009) The WASP and WAVE family proteins. Genome Biol 10: 226.221-226.229.
12. Padrick SB, Rosen MK, (2010) Physical mechanisms of signal integration by WASP family proteins. Annu Rev Biochem 79: 707-735.
13. Burianek LE, Soderling SH, (2013) Under lock and key: Spatiotemporal regulation of WASP family proteins coordinates separate dynamic cellular processes. Semin Cell Dev Biol 24: 258-266.
14. Cheng CY, Mruk DD, (2011) Regulation of spermiogenesis, spermiation and blood-testis barrier dynamics: novel insights from studies on Eps8 and Arp3. Biochem J 435: 553-562.
15. Rotkopf S, Hamberg Y, Aigaki T, Snapper SB, Shilo BZ, et al. (2011) The WASp-based actin polymerization machinery is required in somatic support cells for spermatid maturation and release. Development 138: 2729-2739.
16. Cotta-de-Almeida V, Westerberg L, Maillard MH, Onaldi D, Wachtel H, et al. (2007) Wiskott Aldrich syndrome protein (WASP) and N-WASP are critical for T cell development. Proc Natl Acad Sci USA 104: 15424-15429.
17. Bitgood MJ, Shen L, McMahon AP, (1996) Sertoli cell signaling by Desert hedgehog regulates the male germline. Curr Biol 6: 298-304.
18. Jaegle M, Ghazvini M, Mandemakers W, Piirsoo M, Driegen S, et al. (2003) The POU proteins Brn-2 and Oct-6 share important functions in Schwann cell development. Genes Dev 17: 1380-1391.
19. Lindeboom F, Gillemans N, Karis A, Jaegle M, Meijer D, et al. (2003) A tissue-specific knockout reveals that Gata1 is not essential for Sertoli cell function in the mouse. Nucleic Acids Res 31: 5405-5412.
20. Koch M, Olson P, Albus A, Jin W, Hunter D, et al. (1999) Characterization and expression of the laminin γ3 chain: a novel, non-basement membrane-associated, laminin chain. J Cell Biol 145: 605-618.
21. Yan HHN, Cheng CY, (2006) 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 281: 17286-17303.
22. Oatley JM, Brinster RL, (2006) Spermatogonial stem cells. Methods Enzymol 419: 259-282.
23. van Bragt MP, Roepers-Gajadien HL, Korver CM, Bogerd J, Okuda A, et al. (2008) Expression of the pluripotency marker UTF1 is restricted to a subpopulation of early A spermatogonia in rat testis. Reproduction 136: 33-40.
24. Sharpe RM, McKinnell C, Kivlin C, Fisher JS, (2003) Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 125: 769-784.
25. Li MWM, Xia W, Mruk DD, Wang CQF, Yan HHY, et al. (2006) TNFα 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.
26. Mok KW, Mruk DD, Lee WM, Cheng CY, (2012) Spermatogonial stem cells alone are not sufficient to re-initiate spermatogenesis in the rat testis following adjudin-induced infertility. Int J Androl 35: 86-101.
27. Cyr DG, (2011) Connexins and pannexins: Coordinating cellular communication in the testis and epididymis. Spermatogenesis 1: 325-338.
28. Li MWM, Mruk DD, Cheng CY, (2012) Gap junctions and blood-tissue barriers. Adv Exp Med Biol 763: 260-280.
29. Morrow CMK, Mruk DD, Cheng CY, Hess RA, (2010) Claudin and occludin expression and function in the seminiferous epithelium. Philos Trans R Soc Lond B Biol Sci 365: 1679-1696.
30. Siu ER, Wong EWP, Mruk DD, Porto CS, Cheng CY, (2009) Focal adhesion kinase is a blood-testis barrier regulator. Proc Natl Acad Sci USA 106: 9298-9303.
31. Cummins PM, (2012) Occludin: one protein, many forms. Mol Cell Biol 32: 242-250.
32. Lee NPY, Mruk DD, Lee WM, Cheng CY, (2003) Is the cadherin/catenin complex a functional unit of cell-cell-actin-based adherens junctions (AJ) in the rat testis? Biol Reprod 68: 489-508.
33. Wang CQF, Mruk DD, Lee WM, Cheng CY, (2007) Coxsackie and adenovirus receptor (CAR) is a product of Sertoli and germ cells in rat testes which is localized at the Sertoli-Sertoli and Sertoli-germ cell interface. Exp Cell Res 313: 1373-1392.
34. Ozaki-Kuroda K, Nakanishi H, Ohta H, Tanaka H, Kurihara H, et al. (2002) Nectin couples cell-cell adhesion and the actin scaffold at heterotypic testicular junctions. Curr Biol 12: 1145-1150.
35. Palombi F, Salanova M, Tarone G, Farini D, Stefanini M, (1992) Distribution of b1 integrin subunit in rat seminiferous epithelium. Biol Reprod 47: 1173-1182.
36. Siu MKY, Cheng CY, (2004) 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 70: 945-964.
37. Xiao X, Cheng CY, Mruk DD, (2013) Intercellular adhesion molecule-2 is involved in apical ectoplasmic specialization dynamics during spermatogenesis in the rat. J Endocr 216: 73-86.
38. Poukkula M, Kremneva E, Seerlachius M, Lappalainen P, (2011) Actin-depolymerizating factor homology domain: a conserved fold performing diverse roles in cytoskeletal dynamics. Cytoskeleton 68: 471-490.
39. Li MWM, Xiao X, Mruk DD, Lam YL, Lee WM, et al. (2011) Actin binding protein drebrin E is involved in junction dynamics during spermatogenesis. Spermatogenesis 1: 123-136.
40. Arold ST, (2011) How focal adhesion kinase achieves regulation by linking ligand binding, localization and action. Curr Opin Struct Biol 21: 808-813.
41. Lie PPY, Mruk DD, Mok KW, Su L, Lee WM, et al. (2012) Focal adhesion kinase-Tyr407 and-Tyr397 exhibit antagonistic effects on blood-testis barrier dynamics in the rat. Proc Natl Acad Sci USA 109: 12562-12567.
42. Siu MKY, Mruk DD, Lee WM, Cheng CY, (2003) Adhering junction dynamics in the testis are regulated by an interplay of β1-integrin and focal adhesion complex (FAC)-associated proteins. Endocrinology 144: 2141-2163.
43. Cheng CY, Lie PPY, Wong EWP, Mruk DD, (2013) Focal adhesion kinase and actin regulatory/binding proteins that modulate F-actin organization at the tissue barrier. Lession from the testis. Tissue Barriers 1: e24252 (DOI:10.4161/tisb.24252).
44. Monastyrska I, He C, Geng J, Hoppe AD, Li Z, et al. (2008) Arp2 links autophagic machinery with the actin cytoskeleton. Mol Biol Cell 19: 1962-1975.
45. Shivas JM, Skop AR, (2012) Arp2/3 mediates early endosome dynamics necessary for the maintenance of PAR asymmetry in Caenorhabditis elegans. Mol Biol Cell 23: 1917-1927.
46. Yamamoto T, Mochida J, Kadota J, Takeda MB, E., Tanaka K, (2010) Initial polarized bud growth by endocytic recycling in the absence of actin cable-dependent vesicle transport in yeast. Mol Biol Cell 21: 1237-1252.
47. Jaegle M, Ghazvini M, Mandemakers W, Piirsoo M, Driegen S, et al. (2003) The POU proteins Brn-2 and Oct-6 share important functions in Schwann cell development. Genes Dev 17: 1380-1391.
48. Snapper SB, Takeshima F, Anton I, Liu CH, Thomas SM, et al. (2001) N-WASP deficiency reveals distinct pathways for cell surface projections and microbial actin-based motility. Nature Cell Biol 3: 897-904.
49. Xiao X, Mruk DD, Lee WM, Cheng CY, (2011) 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 43: 651-665.
50. Mruk DD, Cheng CY, (2011) Enhanced chemiluminescence (ECL) for routine immunoblotting. An inexpensive alternative to commercially available kits. Spermatogenesis 1: 121-122.
51. Xiao X, Mruk DD, Cheng CY, (2013) 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 304: E145-E159.
52. 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.