RAB13 participates in ectoplasmic specialization dynamics in the rat testis

Biology of Reproduction

Volumn 80, Issue 3, 2009, Pages 590-601

  Mruk, Dolores D ^a   Lau, Ann S N ^a  

^a POPULATION COUNCIL   (United States)

Author keywords

Cell junctions; Ectoplasmic specialization; Germ cell; Rab13; RAM13; Sertoli cells; Testis

Indexed keywords

ACTIN BINDING PROTEIN; ESPIN; RAB PROTEIN; RAB13 PROTEIN; UNCLASSIFIED DRUG; VINCULIN;

ANIMAL CELL; ARTICLE; BLOOD TESTIS BARRIER; CELL JUNCTION; CELL MEMBRANE; CONTROLLED STUDY; CYTOSKELETON; IMMUNOBLOTTING; IMMUNODETECTION; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEMINIFEROUS TUBULE EPITHELIUM; SERTOLI CELL; SPERMATOCYTE; SPERMATOGENESIS; TESTIS; TIGHT JUNCTION;

ANIMALS; CELLS, CULTURED; CYTOSKELETON; DNA, COMPLEMENTARY; GTP PHOSPHOHYDROLASES; HYDRAZINES; INDAZOLES; INTERCELLULAR JUNCTIONS; MALE; MICROFILAMENT PROTEINS; MOLECULAR SEQUENCE DATA; RAB GTP-BINDING PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; SEMINIFEROUS EPITHELIUM; SERTOLI CELLS; SPERMATOCYTES; TESTIS; VINCULIN;

RATTUS;

EID: 62149121636     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.108.071647     Document Type: Article

References (102)

1. Heiskala M, Peterson PA, Yang Y. The roles of claudin superfamily proteins in paracellular transport. Traffic 2001; 2:92-98.
2. Furuse M, Tsukita S. Claudins in occluding junctions of humans and flies. Trends Cell Biol 2006; 16:181-188.
3. Van Itallie CM, Anderson JM. Claudins and epithelial paracellular transport. Annu Rev Physiol 2006; 68:403-429.
4. Balda MS, Matter K. Transmembrane proteins of tight junctions. Semin Cell Dev Biol 2000; 11:281-289.
5. Tsukita S, Furuse M, Itoh M. Structural and signalling molecules come together at tight junctions. Curr Opin Ceil Biol 1999; 11:628-633.
6. Ebnet K, Suzuki A, Ohno S, Vestweber D. Junctional adhesion molecules (JAMs): more molecules with dual functions? J Cell Sci 2004; 117:19-29.
7. Bazzoni G. The JAM family of junctional adhesion molecules. Curr Opin Cell Biol 2003; 15:525-530.
8. Coyne CB, Bergelson JM. CAR: a virus receptor within the tight junction. Adv Drag Deliv Rev 2005; 57:869-882.
9. Gonzalez-Mariscal L, Betanzos A, Avila-Flores A. MAGUK proteins: structure and role in the tight junction. Semin Cell Dev Biol 2000; 11: 315-324.
10. Chen YH, Lu Q, Goodenough DA, Jeansonne B. Nonreceptor tyrosine kinase c-yes interacts with occludin during tight junction formation in canine kidney epithelial cells. Mol Biol Cell 2002; 13:1227-1237.
11. Mitic LL, Anderson JM. Molecular architecture of tight junctions. Annu Rev Physiol 1998; 60:121-142.
12. Clarke H, Marano CW, Peralta-Soler A, Mullin JM. Modification of tight junction function by protein kinase C isoforms. Adv Drug Deliv Rev 2000;41:283-301.
13. Weber E, Berta G, Tousson A, St. John P, Green MW, Gopalokrishnan U, Jilling T, Sorscher EJ, Elton TS, Abrahamson DR, Kirk KL. Expression and polarized targeting of Rab3 isoform in epithelial cells. J Cell Biol 1994; 125:583-594.
14. Zahraoui A, Joberty G, Arpin M, Fontaine JJ, Hellio R, Tavitian A, Louvard D. A small Rab GTPase is distributed in cytoplasmic vesicles in non polarized cells but colocalizes with the tight junction marker ZO-1 in polarized epithelial cells. J Cell Biol 1994; 124:101-115.
15. Sheth B, Fontaine JJ, Ponza E, McCallum A, Page A, Citi S, Louvard D, Zahraoui A, Fleming TP. Differentiation of the epithelial apical junctional complex during mouse preimplantation development: a role for Rab13 in the early maturation of the tight junction. Mech Dev 2000; 97:93-104.
16. Yamamoto Y, Nishimura N, Morimoto S, Kitamura H, Manabe S, Kanayama H, Kagawa S, Sasaki T. Distinct roles of Rab3B and Rab13 in the polarized transport of apical, basolateral, and tight junctional membrane proteins to the plasma membrane. Biochem Biophys Res Commun 2003; 308:270-275.
17. Schimmoller F, Simon I, Pfeffer SR. Rab GTPases, directors of vesicle docking. J Biol Chem 1998; 273:22161-22164.
18. Collins RN, Brennwald P. Rab. In: Hall A (ed.), GTPases. New York: Oxford University Press; 2000:137-175.
19. Takai Y, Sasaki T, Matozaki T. Small GTP-binding proteins. Physiol Rev 2001; 81:153-208.
20. Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001; 2:107-117.
21. Pfeffer SR. Unsolved mysteries in membrane traffic. Annu Rev Biochem 2007; 76:629-645.
22. Lu H, Bilder D. Endocytic control of epithelial polarity and proliferation in Drosophila, Nat Cell Biol 2005; 7:1232-1239.
23. Snider MD. A role for Rab7 GTPase in growth factor-regulated cell nutrition and apoptosis. Mol Cell 2003; 12:796-797.
24. Murray RZ, Kay JG, Sangermani DG, Stow JL. A role for the phagosome in cytokine secretion. Science 2005; 310:1492-1495.
25. Miaczynska M, Christoforidis S, Giner A, Shevchenko A, Uttenweiler-Joseph S, Habermann B, Wilm M, Parton RG, Zerial M. APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 2004; 116:445-456.
26. Morimoto S, Nishimura N, Terai T, Manabe S, Yamamoto Y, Shinahara W, Miyake H, Tashiro S, Shimada M, Sasaki T. Rab13 mediates the continuous endocytic recycling of occludin to the cell surface. J Biol Chem 2005; 280:2220-2228.
27. Lau ASN, Mruk DD. Rab8B GTPase and junction dynamics in the testis. Endocrinology 2003; 144:1549-1563.
28. Mruk DD, Lau ASN, Sarkar O, Xia W. Rab4A GTPase-catenin interactions are involved in cell junction dynamics in the testis. J Androl 2007; 28:742-754.
29. Beaver BV, Reed W, Leary S, McKiernan B, Bain F, Schultz R, Bennett BT, Pascoe P, Shull E, Cork LC, Francis-Floyd R, Amass KD, et al. 2000 Report of the American Veterinary Medical Association Panel in Euthanasia. J Am Vet Med Assoc 2001; 218:669-696.
30. Mruk DD, Siu MKY, Conway AM, Lee NPY, Lau ASN, Cheng CY. Role of tissue inhibitor of rnetalloproteases-1 in junction dynamics in the testis. J Androl 2003; 24:510-523.
31. Cheng CY, Mather JP, Byer AL, Bardin CW. Identification of hormonally responsive proteins in primary Sertoli cell culture medium by anion-exchange high performance liquid chromatography. Endocrinology 1986; 118:480-488.
32. Galdieri M, Ziparo E, Palombi F, Russo MA, Stefanini M. Pure Sertoli cell cultures: a new model for the study of somatic-germ cell interactions. J Androl 1981; 5:249-259.
33. 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 1996; 168:123-133.
34. Aravindan GR, Mruk D, Lee WM, Cheng CY. Identification, isolation, and characterization of a 41-kilodalton protein from rat germ cellconditioned medium exhibiting concentration-dependent dual biological activities. Endocrinology 1997; 138:3259-3268.
35. Sarkar O, Xia W, Mruk DD. Adjudin-mediated junction restructuring in the seminiferous epithelium leads to displacement of soluble guanylate cyclase from adherens junctions. J Cell Physiol 2006; 208:175-187.
36. Lee NPY, Mruk DD, Conway AM, Cheng CY. Zyxin, axin, and Wiskott-Aldrich syndrome protein are adaptors that link the cadherin/catenin protein complex to the cytoskeleton at adherens junctions in the seminiferous epithelium of the rat testis. J Androl 2004; 25:200-215.
37. Grima J, Zhu LJ, Zong SD, Catterali JF, Bardin CW, Cheng CY. Rat testin is a newly identified component of the junctional complexes in various tissues whose mRNA is predominantly expressed in the testis and ovary. Biol Reprod 1995; 52:340-355.
38. Moroi S, Saitou M, Fujimoto K, Sakakibara A, Furuse M, Yoshida O, Tsukita S. Occludin is concentrated at tight junctions of mouse/rat but not human/guinea pig Sertoli cell testes. Am J Physiol 1998; 274:0708-C1717.
39. Baillie AH, Griffiths K. 3β-Hydroxysteroid dehydrogenase activity in the mouse Leydig cell. J Endocrinol 1964; 29:9-17.
40. Palombi F, Di Carlo C. Alkaline phosphatase is a marker for myoid cells in cultures of rat peritubular and tubular tissue. Biol Reprod 1988; 39: 1101-1109.
41. Richardson LL, Kleinman HK, Dym M. Basement membrane gene expression by Sertoli and peritubular myoid cells in vitro in the rat. Biol Reprod 1995; 52:320-330.
42. Skinner MK, Tung PS, Fritz IB. Cooperativity between Sertoli cells and testicular peritubular cells in the production and deposition of extracellular matrix components. J Cell Biol 1985; 100:1941-1947.
43. Mruk D, Zhu LJ, Silvestrini B, Lee WM, Cheng CY. Interactions of proteases and protease inhibitors in Sertoli-germ cell cocultures preceding the formation of specialized Sertoli-germ cell junctions in vitro. J Androl 1997; 18:612-622.
44. Mruk D, Cheng CY. Sertolin is a novel gene marker of cell-cell interactions in the rat testis. J Biol Chem 1999; 274:27056-27068.
45. Cheng CY, Chen CL, Feng ZM, Marshall A, Bardin CW. Rat clusterin isolated from primary Sertoli cell enriched culture medium is sulfated glycoprotein-2 (SGP-2). Biochem Biophys Res Commun 1988; 155: 398-404.
46. 2-macroglobulin messenger ribonucleic acid expression to acute inflammation in the testis is different from the response in the liver and brain. Biol Reprod 1994; 50:1287-1296.
47. Chavrier P, Gorvel JP, Stelzer E, Simons K, Gruenberg J, Zerial M. Hypervariable C-terminal domain of Rab protein acts as a targeting signal. Nature 1991; 353:769-772.
48. Weeke B. Crossed Immunoelectrophoresis. In: Axelsen NH, Kroll J, Weeke B (eds.), A Manual of Quantitative Immunoelectrophoresis. Methods and Applications. Oslo, Norway: Universititesforlaget Oslo; 1975: 47.
49. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680-685.
50. Sarkar O, Mathur PP, Cheng CY, Mruk DD. Interleukin-1α (IL1A) is a novel regulator of the blood-testis barrier in the rat. Biol Reprod 2008; 78:445-454.
51. Cheng CY, Grima J, Stahler MS, Lockshin RA, Bardin CW. Testins are two structurally related Sertoli cell proteins whose secretion is tightly coupled to the presence of germ cells. J Biol Chem 1989; 264:21386-21393.
52. Cheng CY, Bardin CW. Identification of two testosterone-responsive testicular proteins in Sertoli cell-enriched culture medium whose secretion is suppressed by cells of the intact seminiferous tubule. J Biol Chem 1987; 262:12768-12779.
53. Vitale R, Fawcett DW, Dym M. The normal development of the bloodtestis barrier and the effects of clomiphene and estrogen treatment Anat Rec 1973; 176:333-344.
54. Gilula NB, Fawcett DW. The Sertoli cell occluding junctions and gap junctions in mature and developing mammalian testis. Dev Biol 1976; 59:142-168.
55. Russell LD, Bartke A, Goh JC. Postnatal development of the Sertoli cell barrier, tubular lumen, and cytoskeleton of Sertoli and myoid cells in the rat, and their relationship to tubular fluid secretion and flow. Am J Anat 1989; 184:179-189.
56. Cheng CY, Silvestrini B, Grima J, Mo MY, Zhu LJ, Johansson E, Saso L, Leone MG, Palmery M, Mruk D. Two new male contraceptives exert their effects by depleting germ cells prematurely from the testis. Biol Reprod 2001; 65:449-461.
57. Grima J, Silvestrini B, Cheng CY. Reversible inhibition of spermatogenesis in rats using a new male contraceptive, 1-(2,4-dichlorobenzyl)- indazole-3-carbohydrazide. Biol Reprod 2001; 64:1500-1508.
58. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72:248-254.
59. Cheng CY, Mathur PP, Grima J. Structural analysis of clusterin and its subunits in ram rete testis fluid. Biochemistry 1988; 27:4079-4088.
60. Page M, Thorpe R. Purification of IgG by precipitation with sodium sulfate or ammonium sulfate. In: Walker JM (ed.), The Protein Protocols Handbook. Totowa, NJ: Humana Press; 2001:983-984.
61. Page M, Thorpe R. Purification of IgG using DEAE-Sepharose chromatography. In: Walker JM (ed.), The Protein Protocols Handbook. Totowa, NJ: Humana Press; 2001:987-988.
62. Kohler K, Louvard D, Zahraoui A. Rab13 regulates PKA signaling during tight junction assembly. J Cell Biol 2004; 165:175-180.
63. 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 2004; 25:747-806.
64. Xia W, Wong CH, Lee NP, Lee WM, Cheng CY. Disruption of Sertoligerm cell adhesion function in the seminiferous epithelium of the rat testis can be limited to adherens junctions without affecting the bloodtestis barrier integrity: an in vivo study using an androgen suppression model. J Cell Physiol 2005; 205:141-157.
65. Wong CH, Mruk DD, Lee WM, Cheng CY. Targeted and reversible disruption of the blood-testis barrier by an FSH mutant-occludin peptide conjugate. FASEB J 2007; 21:438-448.
66. Chung SS, Lee WM, Cheng CY. Study on the formation of specialized inter-Sertoli cell junctions in vitro. J Cell Physiol 1999; 181:258-272.
67. Chung NPY, Cheng CY. Ts cadmium chloride-induced inter-Sertoli tight junction permeability barrier disruption a suitable in vitro model to study the events of junction disassembly during spermatogenesis in the rat testis? Endocrinology 2001; 142:1878-1888.
68. Wong CCS, Chung SSW, Grima J, Zhu LJ, Mruk D, Lee WM, Cheng CY. Changes in the expression of junctional and nonjunctional complex component genes when inter-Sertoli tight junctions are formed in vitro. J Androl 2000; 21:227-237.
69. Chung SS, Mo MY, Silvestrini B, Lee WM, Cheng CY. Rat testicular N-cadherin: its complementary deoxyribonucleic acid cloning and regulation. Endocrinology 1998; 139:1853-1862.
70. Grove BD, Pfeiffer DC, Allen S, Vogl AW. Immunofluorescence localization of vinculin in ectoplasmic ("junctional") specializations of rat Sertoli cells. Am J Anat 1990; 188:44-56.
71. Pfeiffer DC, Vogl AW. Evidence that vinculin is co-distributed with actin bundles in ectoplasmic ("junctional") specializations of mammalian Sertoli cells. Anat Rec 1991; 231:89-100.
72. Battles JR, Wierda A, Zheng L. Identification and characterization of espin, an actin-binding protein localized to the F-actin-rich junctional plaques of Sertoli cell ectoplasmic specializations. J Cell Sci 1996; 109: 1229-1239.
73. Chen YM, Lee NPY, Mruk DD, Lee WM, Cheng CY. Fer kinase/Fer T and adherens junction dynamics in the testis; an in vitro and in vivo study. Biol Reprod 2003; 69:656-672.
74. Boekelheide K. Sertoli cell toxicants. In: Russell LD, Griswold MD (eds.), The Sertoli Cell. Clearwater, FL: Cache River Press; 1993:551-575.
75. Russell LD, Goh JC, Rashed RMA, Vogl AW. 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.
76. De Martino C, Malcorni W, Bellocci M, Floridi A, Marcante ML. Effects of AF1312 TS and lonidamine on mammalian testis. A morphological study. Chemotherapy 1981; 27(suppl 2):27-42.
77. Silvestrini B, Palazzo G, De Gregorio M. Lonidamine and related compounds. Prog Med Chem 1984; 21:110-135.
78. Jockusch BM, Isenberg G. Interaction of α-actinin and vinculin with actin: opposite effects on filament network formation. Proc Natl Acad Sci USA 1981;78:3005-3009.
79. Chen B, Li A, Wang D, Wang M, Zheng L, Battles JR. Espin contains an additional actin-binding site in its N-terminus and is a major actinbundling protein of the Sertoli cell-spermatid ectoplasmic specialization junctional plaque. Mol Biol Cell 1999; 10:4327-4339.
80. Dym M, Fawcett DW. The blood-testis barrier in the rat and the physiological compartmentation of the seminiferous epithelium. Biol Reprod 1970; 3:308-326.
81. Setchell BP, Waites GMB. The blood-testis barrier. In: Hamilton DW, Greep RO (eds.), The Handbook of Physiology. Baltimore: Williams and Wilkins; 1975:143-172.
82. Russell LD. Observations on rat Sertoli ectoplasmic ('junctional') specializations in their association with germ cells of the rat testis. Tissue Cell 1977; 9:475-498.
83. Vogl AW, Pfeiffer DC, Redenbach DM, Grove BD. Sertoli cell cytoskeleton. In: Russell LD, Griswold MD (eds.), The Sertoli Cell. Clearwater, FL: Cache River Press; 1993:39-86.
84. Mruk DD, Silvestrini B, Cheng CY. Anchoring junctions as drug targets: role in contraceptive development. Pharmacol Rev 2008; 60:146-180.
85. Yan HH, Mruk DD, Lee WM, Cheng CY. Ectoplasmic specialization: a friend or foe of spermatogenesis'? BioEssays 2007; 29:36-48.
86. Russell LD, Clermont Y. Anchoring device between Sertoli cells and late spermatids in rat seminiferous tubules. Anat Rec 1976; 185:259-278.
87. Russell LD. Further observations on tubulobulbar complexes formed by late spermatids and Sertoli cells in the rat testis. Anat Rec 1979; 194: 213-232.
88. 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 1979; 155:259-279.
89. Russell LD. Morphological and functional evidence for Sertoli-germ cell relationships. In: Russell LD, Griswold MD (eds.), The Sertoli Cell. Clearwater, FL: Cache River Press; 1993:365-390.
90. Tida H, Yoshinaga Y, Tanaka S, Toshimori K, Mori T. Tdentification of Rab3A GTPase as an acrosome-associated small GTP-binding protein in rat sperm. Dev Biol 1999; 211:144-155.
91. Yunes R, Michaut M, Tomes C, Mayorga LS. Rab3A triggers the acrosome reaction in permeabilized human spermatozoa. Biol Reprod 2000; 62:1084-1089.
92. Belmonte SA, Lopez CI, Roggero CM, De Blas GA, Tomes CN, Mayorga LS. Cholesterol content regulates acrosomal exocytosis by enhancing Rab3A plasma membrane association. Dev Biol 2005; 285: 393-408.
93. Mountjoy JR, Xu W, McLeod D, Hyndman D, Oko R. RAB2A: a major subacrosomal protein of bovine spermatozoa implicated in acrosomal biogenesis. Biol Reprod 2008; 79:223-232.
94. Russell LD. Movement of spermatocytes from the basal to the adluminal compartment of the rat testis. Am J Anat 1977; 148:313-328.
95. Byers S, Hadley MA, Djakiew D, Dym M. Growth and characterization of epididymal epithelial cells and Sertoli cells in dual environment culture chambers. J Androl 1986; 7:59-68.
96. 2macroglobulin, and testins: biosynthesis and differential regulation by germ cells. Mol Cell Endocrinol 1992; 89:127-140.
97. Janecki A, Jakubowiak A, Steinberger A. Regulation of transepithelial electrical resistance in two-compartment Sertoli cell cultures: in vitro model of the blood-testis barrier. Endocrinology 1991: 129:1489-1496.
98. Lee NPY, Mruk D, Lee WM, Cheng CY. Is the cadherin/catenin complex a functional unit of cell-cell-actin-based adherens junctions (AD in the rat testis? Biol Reprod 2003; 68:489-508.
99. Mruk DD, Wong CH, Silvestrini B, Cheng CY. A male contraceptive targeting germ cell adhesion. Nat Med 2006; 12:1323-1328.
100. Mruk DD, Cheng CY. Cell-cell interactions at the ectoplasmic specialization in the testis. Trends Endocrinol Metab 2004; 15:439-447.
101. Cheng CY, Mruk DD. Cell junction dynamics in the testis: Sertoli-gerrn cell interactions and male contraceptive development. Physiol Rev 2002; 82:825-874.
102. Siu MKY, Mruk DD, Lee WM, Cheng CY. Adhering junction dynamics in the testis are regulated by an interplay of β1 integrin and focal adhesion complex-associated proteins. Endocrinology 2003; 144:2141-2163.