Fascin 1 is an actin filament-bundling protein that regulates ectoplasmic specialization dynamics in the rat testis

American Journal of Physiology - Endocrinology and Metabolism

Volumn 307, Issue 9, 2014, Pages E738-E753

  Gungor Ordueri, N Ece ^a   Celik Ozenci, Ciler ^b   Cheng, C Yan ^a  

^a POPULATION COUNCIL   (United States)

^b AKDENIZ UNIVERSITY   (Turkey)

Author keywords

Blood testis barrier; Ectoplasmic specialization; F actin; Fascin 1; Seminiferous epithelial cycle; Spermatid polarity; Spermatogenesis; Testis

Indexed keywords

EPS8 PROTEIN; FASCIN; FASCIN 1; PALLADIN PROTEIN; PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; 1-(2,4-DICHLOROBENZYL)INDAZOLE-3-CARBOHYDRAZIDE; ACTIN BINDING PROTEIN; EPS8 PROTEIN, RAT; FASCIN-1 PROTEIN, RAT; HYDRAZINE DERIVATIVE; INDAZOLE DERIVATIVE; MALE CONTRACEPTIVE AGENT; PALADIN PROTEIN, RAT; PHOSPHOPROTEIN PHOSPHATASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD TESTIS BARRIER; CELL ADHESION; CELL MEMBRANE; CELL POLARITY; CELL SPECIFICITY; CONTROLLED STUDY; DOWN REGULATION; GENE SILENCING; IN VITRO STUDY; MALE; NONHUMAN; PROTEIN EXPRESSION; RAT; SEMINIFEROUS TUBULE EPITHELIUM; SERTOLI CELL; SPERMATID; TESTIS; ACTIN FILAMENT; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CYTOLOGY; CYTOPLASM; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROTEIN TRANSPORT; SPERMATOGENESIS; SPRAGUE DAWLEY RAT; TIGHT JUNCTION; ULTRASTRUCTURE;

ACTIN CYTOSKELETON; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BLOOD-TESTIS BARRIER; CELL POLARITY; CELLS, CULTURED; CONTRACEPTIVE AGENTS, MALE; CYTOPLASM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE SILENCING; HYDRAZINES; INDAZOLES; MALE; MICROFILAMENT PROTEINS; PHOSPHOPROTEIN PHOSPHATASES; PROTEIN TRANSPORT; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; SERTOLI CELLS; SPERMATIDS; SPERMATOGENESIS; TESTIS; TIGHT JUNCTIONS;

EID: 84908362283     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00113.2014     Document Type: Article

References (75)

1. Adams JC. Roles of fascin in cell adhesion and motility. Curr Opin Cell Biol 16: 590-596, 2004.
2. Amann RP, Howards SS. Daily spermatozoal production and epididymal spermatozoal reserves of the human male. J Urol 124: 211-215, 1980.
3. Aravindan GR, Pineau C, Bardin CW, Cheng CY. Ability of trypsin in mimicking germ cell factors that affect Sertoli cell secretory function. J Cell Physiol 168: 123-133, 1996.
4. Assémat E, Bazellières E, Pallesi-Pocachard E, Le Bivic A, Massey- Harroche D Polarity complex proteins. Biochim Biophys Acta 1778: 614-630, 2008.
5. Auharek SA, Franca LR. Postnatal testis development, Sertoli cell proliferation and number of different spermatogonial types in C57BL/6J mice made transiently hypo- and hyperthyroidic during the neonatal period. J Anat 216: 577-588, 2010.
6. Cao D, Ji H, Ronnett BM. Expression of mesothelin, fascin, and prostate stem cell antigen in primary ovarian mucinous tumors and their utility in differentiating primary ovarian mucinous tumors from metastatic pancreatic mucinous carcinomas in the ovary. Int J Gynecol Pathol 24: 67-72, 2005.
7. Cheng CY, Lie PP, Wong EW, Mruk DD. Focal adhesion kinase and actin regulatory/binding proteins that modulate F-actin organization at the tissue barrier: Lesson from the testis. Tissue Barriers 1: e24252, 2013.
8. Cheng CY, Lie PP, Wong EW, Mruk DD, Silvestrini B. Adjudin disrupts spermatogenesis via the action of some unlikely partners: Eps8, Arp2/3 complex, drebrin E, PAR6 and 14-3-3. Spermatogenesis 1: 291- 297, 2011.
9. Cheng CY, Mruk DD. Cell junction dynamics in the testis: Sertoli-germ cell interactions and male contraceptive development. Physiol Rev 82: 825-874, 2002.
10. Cheng CY, Mruk DD. A local autocrine axis in the testes that regulates spermatogenesis. Nat Rev Endocrinol 6: 380-395, 2010.
11. Cheng CY, Mruk DD, Silvestrini B, Bonanomi M, Wong CH, Siu MK, Lee NP, Mo MY. AF-2364 [1-(2,4-dichlorobenzyl)-1H-indazole-3-carbohydrazide] is a potential male contraceptive: a review of recent data. Contraception 72: 251-261, 2005.
12. Cheng CY, Silvestrini B, Grima J, Mo MY, Zhu LJ, Johansson E, Saso L, Leone MG, Palmery M, Mruk DD. Two new male contraceptives exert their effects by depleting germ cells prematurely from the testis. Biol Reprod 65: 449-461, 2001.
13. Cheng CY, Wong EW, Lie PP, Li MW, Su L, Siu ER, Yan HH, Mannu J, Mathur PP, Bonanomi M, Silvestrini B, Mruk DD. Environmental toxicants and male reproductive function. Spermatogenesis 1: 2-13, 2011.
14. Chin YR, Toker A. Akt isoform-specific signaling in breast cancer. Uncovering an anti-migratory role of palladin. Cell Adh Migr 5: 211-214, 2011.
15. Clermont Y, Morales C, Hermo L. Endocytic activities of Sertoli cells in the rat. Ann NY Acad Sci 513: 1-15, 1987.
16. Edwards RA, Bryan J. Fascins, a family of actin bundling proteins. Cell Motil Cytoskeleton 32: 1-9, 1995.
17. Goldenring JR. A central role for vesicle trafficking in epithelial neoplasia: intracellular highways to carcinogenesis. Nat Rev Cancer 13: 813- 820, 2013.
18. Goldstein B, Macara IG. The PAR proteins: fundamental players in animal cell polarization. Dev Cell 13: 609-622, 2007.
19. Hashimoto Y, Kim DJ, Adams JC. The roles of fascins in health and disease. J Pathol 224: 289-300, 2011.
20. Hess RA, Schaeffer DJ, Eroschenko VP, Keen JE. Frequency of the stages of the cycle of the seminiferous epithelium in the rat. Biol Reprod 43: 517-524, 1990.
21. Hinck L, Näthke I. Changes in cell and tissue organization in cancer of the breast and colon. Curr Opin Cell Biol 26: 87-95, 2014.
22. Humbert PO, Dow LE, Russell SM. The Scribble and Par complexes in polarity and migration: friends or foes? Trends Cell Biol 16: 622-630, 2006.
23. Iden S, Collard JG. Crosstalk between small GTPases and polarity proteins in cell polarization. Nat Rev Mol Cell Biol 9: 846-859, 2008.
24. Jayo A, Parsons M. Fascin: a key regulator of cytoskeletal dynamics. Int J Biochem Cell Biol 42: 1614-1617, 2010.
25. Johnson L, Petty CS, Neaves WB. A comparative study of daily sperm production and testicular composition in humans and rats. Biol Reprod 22: 1233-1243, 1980.
26. Kierszenbaum AL, Rivkin E, Tres LL. Molecular biology of sperm head shaping. Soc Reprod Fertil Suppl 65: 33-43, 2007.
27. Kierszenbaum AL, Tres LL. The acrosome-acroplaxome-manchette complex and the shaping of the spermatid head. Arch Histol Cytol 67: 271-284, 2004.
28. Lee M, Vasioukhin V. Cell polarity and cancer-cell and tissue polarity as a non-canonical tumor suppressor. J Cell Sci 121: 1141-1150, 2008.
29. Lie PP, Chan AY, Mruk DD, Lee WM, Cheng CY. Restricted Arp3 expression in the testis prevents blood-testis barrier disruption during junction restructuring at spermatogenesis. Proc Natl Acad Sci USA 107: 11411-11416, 2010.
30. Lie PP, Mruk DD, Lee WM, Cheng CY. 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, 2009.
31. 397 exhibit antagonistic effects on blood-testis barrier dynamics in the rat. Proc Natl Acad Sci USA 109: 12562- 12567, 2012.
32. Lin-Jones J, Burnside B. Retina-specific protein fascin 2 is an actin cross-linker associated with actin bundles in photoreceptor inner segments and calycal processes. Invest Ohpthalmol Vis Sci 48: 1380-1388, 2007.
33. Lou E, Fujisawa S, Morozov A, Barlas A, Romin Y, Dogan Y, Gholami S, Moreira AL, Manova-Todorova K, Moore MA. Tunneling nanotubes provide a unique conduit for intercellular transfer of cellular contents in human malignant pleural mesothelioma. PLoS One 7: e33093, 2012.
34. Mok KW, Mruk DD, Lee WM, Cheng CY. Rictor/mTORC2 regulates blood-testis barrier dynamics via its effects on gap junction communications and actin filament network. FASEB J 27: 1137-1152, 2013.
35. Mok KW, Mruk DD, Lee WM, Cheng CY. 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, 2012.
36. Mruk DD, Cheng CY. Cell-cell interactions at the ectoplasmic specialization in the testis. Trends Endocrinol Metab 15: 439-447, 2004.
37. Mruk DD, Cheng CY. Enhanced chemiluminescence (ECL) for routine immunoblotting. An inexpensive alternative to commercially available kits. Spermatogenesis 1: 121-122, 2011.
38. Mruk DD, Cheng CY. An in vitro system to study Sertoli cell blood-testis barrier dynamics. Methods Mol Biol 763: 237-252, 2011.
39. Mruk DD, Cheng CY. 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.
40. Noatynska A, Tavernier N, Gotta M, Pintard L. Coordinating cell polarity and cell cycle progression: what can we learn from flies and worms? Open Biol 3: 130083, 2013.
41. Parvinen M. Regulation of the seminiferous epithelium. Endocr Rev 3: 404-417, 1982.
42. Pineau C, Syed V, Bardin CW, Jegou B, Cheng CY. Germ cell conditioned medium contains multiple factors that modulate the secretion of testin, clusterin, and transferrin by Sertoli cells. J Androl 14: 87-98, 1993.
43. Qian X, Mruk DD, Cheng YH, Cheng CY. Actin cross-linking protein palladin and spermatogenesis. Spermatogenesis 3: e23473, 2013.
44. Qian X, Mruk DD, Wong EW, Lie PP, Cheng CY. Palladin is a regulator of actin filament bundles at the ectoplasmic specialization in the rat testis. Endocrinology 154: 1907-1920, 2013.
45. Robaire B. Advancing towards a male contraceptive: a novel approach from an unexpected direction. Trends Pharmacol Sci 24: 326-328, 2003.
46. Ross R, Ross XL, Schwing J, Langin T, Reske-Kunz AB. The actinbundling protein fascin is involved in the formation of dendritc processes in maturing epidermal Langerhans cells. J Immunol 160: 3776-3782, 1998.
47. Russell L. Observations on rat Sertoli ectoplasmic ('junctional') specializations in their association with germ cells of the rat testis. Tissue Cell 9: 475-498, 1977.
48. Russell LD. 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 155: 259-279, 1979.
49. Russell LD, Peterson RN. Sertoli cell junctions: morphological and functional correlates. Int Rev Cytol 94: 177-211, 1985.
50. Russell LD, Saxena NK, Weber JE. Intratesticular injection as a method to assess the potential toxicity of various agents to study mechanisms of normal spermatogenesis. Gamete Res 17: 43-56, 1987.
51. Saishin Y, Ishikawa R, Ugawa S, Guo W, Ueda T, Morimura H, Kohama K, Shimizu H, Tano Y, Shimada S. Retinal fascin: functional nature, subcellular distribution, and chromosomal localization. Invest Ohpthalmol Vis Sci 41: 2087-2095, 2000.
52. Saishin Y, Shimada S, Morimura H, Sato K, Ishimoto I, Tano Y, Tohyama M. Isolation of a cDNA encoding a photoreceptor cell-specific actin-bundling protein: retinal fascin. FEBS Lett 414: 381-386, 1997.
53. Saishin Y, Shimada S, Morimura H, Sato K, Ishimoto I, Tano Y, Tohyama M. Isolation of a cDNA encoding a photoreceptor cell-specific actin-bundling protein: retinal fascin. FEBS Lett 414: 381-386, 1997.
54. Siu MK, Wong CH, Lee WM, Cheng CY. 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.
55. Sonego M, Gajendra S, Parsons M, Ma Y, Hobbs C, Zentar MP, Williams G, Machesky LM, Doherty P, Lalli G. Fascin regulates the migration of subventricular zone-derived neuroblasts in the postnatal brain. J Neurosci 33: 12171-12185, 2013.
56. Su WH, Wong EW, Mruk DD, Cheng CY. The Scribble/Lgl/Dlg polarity protein complex is a regulator of blood-testis barrier dynamics and spermatid polarity during spermatogenesis. Endocrinology 153: 6041- 6053, 2012.
57. Tubb B, Mulholland DJ, Volg AW, Lan Z, Niederberger C, Cooney A, Bryan J. Testis fascin (FSCN3): a novel paralog of the actin-bundling protein fascin expressed specifically in the elongate spermatid head. Exp Cell Res 275: 92-109, 2002.
58. Tubb BE, Bardien-Kruger S, Kashork CD, Shaffer LG, Ramagli LS, Xu J, Siciliano MJ, Breyan J. Characterization of human retinal fascin gene (FSCN2) at 17q25: close physical linkage of fascin and cytoplasmic actin genes. Genomics 65: 146-156, 2000.
59. Vogl A. Distribution and function of organized concentrations of actin filaments in mammalian spermatogenic cells and Sertoli cells. Int Rev Cytol 119: 1-56, 1989.
60. Vogl AW, Vaid KS, Guttman JA. The Sertoli cell cytoskeleton. Adv Exp Med Biol 636: 186-211, 2008.
61. 397 regulates spermatid adhesion in the rat testis via its effects on F-actin organization at the ectoplasmic specialization. Am J Physiol Endocrinol Metab 305: E687-E699, 2013.
62. Wan HT, Mruk DD, Wong CK, Cheng CY. Perfluorooctanesulfonate (PFOS) perturbs male rat Sertoli cell blood-testis barrier function by affecting F-actin organization via p-FAK-Tyr(407): an in vitro study. Endocrinology 155: 249-262, 2014.
63. Wolski KM, Mruk DD, Cameron DF. The Sertoli-spermatid junctional complex adhesion strength is affected in vitro by adjudin. J Androl 27: 790-794, 2006.
64. Wong EW, Cheng CY. Polarity proteins and cell-cell interactions in the testis. Int Rev Cell Mol Biol 278: 309-353, 2009.
65. Wong EW, Mruk DD, Lee WM, Cheng CY. Par3/Par6 polarity complex coordinates apical ectoplasmic specialization and blood-testis barrier restructuring during spermatogenesis. Proc Natl Acad Sci USA 105: 9657- 9662, 2008.
66. Wong EW, Mruk DD, Lee WM, Cheng CY. Regulation of blood-testis barrier dynamics by TGF-beta3 is a Cdc42-dependent protein trafficking event. Proc Natl Acad Sci USA 107: 11399-11404, 2010.
67. Wong EW, Sun S, Li MW, Lee WM, Cheng CY. 14-3-3 protein regulates cell adhesion in the seminiferous epithelium of rat testes. Endocrinology 150: 4713-4723, 2009.
68. Xiao X, Mruk DD, Cheng CY. 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, 2013.
69. Xiao X, Mruk DD, Lee WM, Cheng CY. 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, 2011.
70. Yamakita Y, Matsumura F, Yamashiro S. Fascin 1 is dispensable for mouse development but is favorable for neonatal survival. Cell Motil Cytoskeleton 66: 524-534, 2009.
71. Yamashiro-Matsumura S, Matsumura F. Intracellular localization of the 55-kD actin-bundling protein in cultured cells: spatial relationships with actin, alpha-actinin, tropomyosin, and fimbrin. J Cell Biol 103: 631-640, 1986.
72. Yan HH, Cheng CY. Blood-testis barrier dynamics are regulated by an engagement/disengagement mechanism between tight and adherens junctions via peripheral adaptors. Proc Natl Acad Sci USA 102: 11722-11727, 2005.
73. Yan HH, Cheng CY. Laminin alpha 3 forms a complex with beta3 and gamma3 chains that serves as the ligand for alpha 6beta1-integrin at the apical ectoplasmic specialization in adult rat testes. J Biol Chem 281: 17286-17303, 2006.
74. Yan HH, Mruk DD, Lee WM, Cheng CY. Ectoplasmic specialization: a friend or a foe of spermatogenesis? Bioessays 29: 36-48, 2007.
75. Zwain IH, Cheng CY. Rat seminiferous tubular culture medium contains a biological factor that inhibits Leydig cell steroidogenesis: its purification and mechanism of action. Mol Cell Endocrinol 104: 213-227, 1994.