Loss of R2D2 proteins ROPN1 and ROPN1L causes defects in murine sperm motility, phosphorylation, and fibrous sheath integrity

Biology of Reproduction

Volumn 88, Issue 2, 2013, Pages

  Fiedler, Sarah E ^a   Dudiki, Tejasvi ^b   Vijayaraghavan, Srinivasan ^b   Carr, Daniel W ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b KENT STATE UNIVERSITY   (United States)

Author keywords

AKAP; Fibrous sheath; OmniBank; PKA; ROPN1; Sperm

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; PROTEIN; ROPN1 PROTEIN; ROPN1L PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CALCIUM SIGNALING; CILIARY MOTILITY; CONTROLLED STUDY; DIMERIZATION; FLAGELLUM; GENE INACTIVATION; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MALE; MALE FERTILITY; MALE INFERTILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SEMINIFEROUS TUBULE; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOZOON; SPERMATOZOON CAPACITATION; SPERMATOZOON MOTILITY; TESTIS;

A KINASE ANCHOR PROTEINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AXONEME; CYCLIC AMP-DEPENDENT PROTEIN KINASES; INFERTILITY, MALE; MALE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MODELS, ANIMAL; PHOSPHORYLATION; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; SPERM CAPACITATION; SPERM MOTILITY; SPERM TAIL; TYROSINE;

MURINAE; MUS;

EID: 84877038864     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.105262     Document Type: Article

References (51)

1. Remenyi A, Good MC, Lim WA. Docking interactions in protein kinase and phosphatase networks. Curr Opin Struct Biol 2006; 16:676-685.
2. Carr DW, Stofko-Hahn RE, Fraser ID, Bishop SM, Acott TS, Brennan RG, Scott JD. Interaction of the regulatory subunit (RII) of cAMP-dependent protein kinase with RII-anchoring proteins occurs through an amphipathic helix binding motif. J Biol Chem 1991; 266:14188-14192. 3. Bhattacharyya RP, Remenyi A, Yeh BJ, Lim WA. Domains, motifs, and scaffolds: the role of modular interactions in the evolution and wiring of cell signaling circuits. Annu Rev Biochem 2006; 75:655-680.
3. Bhattacharyya RP, Remenyi A, Yeh BJ, Lim WA. Domains, motifs, and scaffolds: the role of modular interactions in the evolution and wiring of cell signaling circuits. Annu Rev Biochem 2006; 75:655-680
4. Carr DW, Fujita A, Stentz CL, Liberty GA, Olson GE, Narumiya S. Identification of sperm-specific proteins that interact with A-kinase anchoring proteins in a manner similar to the type II regulatory subunit of PKA. J Biol Chem 2001; 276:17332-17338.
5. Eddy EM, Toshimori K, O'Brien DA. Fibrous sheath of mammalian spermatozoa. Microsc Res Tech 2003; 61:103-115.
6. Newell AE, Fiedler SE, Ruan JM, Pan J, Wang PJ, Deininger J, Corless CL, Carr DW. Protein kinase A RII-like (R2D2) proteins exhibit differential localization and AKAP interaction. Cell Motil Cytoskeleton 2008; 65:539-552.
7. Eddy EM. The scaffold role of the fibrous sheath. Soc Reprod Fertil Suppl 2007; 65:45-62.
8. Krisfalusi M, Miki K, Magyar PL, O'Brien DA. Multiple glycolytic enzymes are tightly bound to the fibrous sheath of mouse spermatozoa. Biol Reprod 2006; 75:270-278.
9. Miki K, Qu W, Goulding EH, Willis WD, Bunch DO, Strader LF, Perreault SD, Eddy EM, O'Brien DA. Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility. Proc Natl Acad Sci U S A 2004; 101:16501-16506.
10. Miki K, Willis WD, Brown PR, Goulding EH, Fulcher KD, Eddy EM. Targeted disruption of the Akap4 gene causes defects in sperm flagellum and motility. Dev Biol 2002; 248:331-342.
11. Oakberg EF. A description of spermiogenesis in the mouse and its use in analysis of the cycle of the seminiferous epithelium and germ cell renewal. Am J Anat 1956; 99:391-413.
12. Olson GE, Hamilton DW, Fawcett DW. Isolation and characterization of the fibrous sheath of rat epididymal spermatozoa. Biol Reprod 1976; 14:517-530.
13. Brown PR, Miki K, Harper DB, Eddy EM. A-kinase anchoring protein 4 binding proteins in the fibrous sheath of the sperm flagellum. Biol Reprod 2003; 68:2241-2248.
14. Fiedler SE, Bajpai M, Carr DW. Identification and characterization of RHOA-interacting proteins in bovine spermatozoa. Biol Reprod 2008; 78:184-192.
15. Fujita A, Nakamura K, Kato T, Watanabe N, Ishizaki T, Kimura K, Mizoguchi A, Narumiya S. Ropporin, a sperm-specific binding protein of rhophilin, that is localized in the fibrous sheath of sperm flagella. J Cell Sci 2000; 113(pt 1):103-112.
16. Burton KA, McKnight GS. PKA, germ cells, and fertility. Physiology (Bethesda) 2007; 22:40-46.
17. Carr DW, Hausken ZE, Fraser ID, Stofko-Hahn RE, Scott JD. Association of the type II cAMP-dependent protein kinase with a human thyroid RII-anchoring protein. Cloning and characterization of the RII-binding domain. J Biol Chem 1992; 267:13376-13382.
18. Vijayaraghavan S, Goueli SA, Davey MP, Carr DW. Protein kinase A-anchoring inhibitor peptides arrest mammalian sperm motility. J Biol Chem 1997; 272:4747-4752.
19. Harrison RA. Rapid PKA-catalysed phosphorylation of boar sperm proteins induced by the capacitating agent bicarbonate. Mol Reprod Dev 2004; 67:337-352.
20. Burton KA, Treash-Osio B, Muller CH, Dunphy EL, McKnight GS. Deletion of type IIalpha regulatory subunit delocalizes protein kinase A in mouse sperm without affecting motility or fertilization. J Biol Chem 1999; 274:24131-24136.
21. Hsu HC, Lee YL, Cheng TS, Howng SL, Chang LK, Lu PJ, Hong YR. Characterization of two non-testis-specific CABYR variants that bind to GSK3beta with a proline-rich extensin-like domain. Biochem Biophys Res Commun 2005; 329:1108-1117.
22. Chiriva-Internati M, Yu Y, Mirandola L, Jenkins MR, Chapman C, Cannon M, Cobos E, Kast WM. Cancer testis antigen vaccination affords long-term protection in a murine model of ovarian cancer. PLoS One 2010; 5:e10471.
23. Frayne J, Hall L. A re-evaluation of sperm protein 17 (Sp17) indicates a regulatory role in an A-kinase anchoring protein complex, rather than a unique role in sperm-zona pellucida binding. Reproduction 2002; 124:767-774.
24. Grizzi F, Chiriva-Internati M, Franceschini B, Bumm K, Colombo P, Ciccarelli M, Donetti E, Gagliano N, Hermonat PL, Bright RK, Gioia M, Dioguardi N, et al. Sperm protein 17 is expressed in human somatic ciliated epithelia. J Histochem Cytochem 2004; 52:549-554.
25. Grizzi F, Chiriva-Internati M, Franceschini B, Hermonat PL, Soda G, Lim SH, Dioguardi N. Immunolocalization of sperm protein 17 in human testis and ejaculated spermatozoa. J Histochem Cytochem 2003; 51:1245-1248. 26. Huang Z, Somanath PR, Chakrabarti R, Eddy EM, Vijayaraghavan S. Changes in intracellular distribution and activity of protein phosphatase PP1gamma2 and its regulating proteins in spermatozoa lacking AKAP4. Biol Reprod 2005; 72:384-392.
26. Huang Z, Somanath PR, Chakrabarti R, Eddy EM, Vijayaraghavan S. Changes in intracellular distribution and activity of protein phosphatase PP1gamma2 and its regulating proteins in spermatozoa lacking AKAP4 Biol Reprod 2005; 72:384-392
27. Lea IA, Widgren EE, O'Rand MG. Association of sperm protein 17 with A-kinase anchoring protein 3 in flagella. Reprod Biol Endocrinol 2004; 2:57.
28. Li Z, Li W, Meklat F, Wang Z, Zhang J, Zhang Y, Lim SH. A yeast two-hybrid system using Sp17 identified Ropporin as a novel cancer-testis antigen in hematologic malignancies. Int J Cancer 2007; 121:1507-1511. 29. Richardson RT, Yamasaki N, O'Rand MG. Sequence of a rabbit sperm zona pellucida binding protein and localization during the acrosome reaction. Dev Biol 1994; 165:688-701.
29. Richardson RT, Yamasaki N, O'Rand MG. Sequence of a rabbit sperm zona pellucida binding protein and localization during the acrosome reaction Dev Biol 1994; 165:688-701
30. Li YF, He W, Jha KN, Klotz K, Kim YH, Mandal A, Pulido S, Digilio L, Flickinger CJ, Herr JC. FSCB, a novel protein kinase A-phosphorylated calcium-binding protein, is a CABYR-binding partner involved in late steps of fibrous sheath biogenesis. J Biol Chem 2007; 282:34104-34119. 31. Li YF, He W, Kim YH, Mandal A, Digilio L, Klotz K, Flickinger CJ, Herr JC. CABYR isoforms expressed in late steps of spermiogenesis bind with AKAPs and ropporin in mouse sperm fibrous sheath. Reprod Biol Endocrinol 2010; 8:101.
31. Li YF, He W, Kim YH, Mandal A, Digilio L, Klotz K, Flickinger CJ, Herr JC CABYR isoforms expressed in late steps of spermiogenesis bind with AKAPs and ropporin in mouse sperm fibrous sheath Reprod Biol Endocrinol 2010; 8:101
32. Naaby-Hansen S, Mandal A, Wolkowicz MJ, Sen B, Westbrook VA, Shetty J, Coonrod SA, Klotz KL, Kim YH, Bush LA, Flickinger CJ, Herr JC. CABYR, a novel calcium-binding tyrosine phosphorylation-regulated fibrous sheath protein involved in capacitation. Dev Biol 2002; 242:236-254.
33. Fiedler SE, Sisson JH, Wyatt TA, Pavlik JA, Gambling TM, Carson JL, Carr DW. Loss of ASP but not ROPN1 reduces mammalian ciliary motility. Cytoskeleton (Hoboken) 2012; 69:22-32.
34. Zambrowicz BP, Friedrich GA, Buxton EC, Lilleberg SL, Person C, Sands AT. Disruption and sequence identification of 2,000 genes in mouse embryonic stem cells. Nature 1998; 392:608-611.
35. Kaneto M, Krisfalusi M, Eddy EM, O'Brien DA, Miki K. Bicarbonate-induced phosphorylation of p270 protein in mouse sperm by cAMP-dependent protein kinase. Mol Reprod Dev 2008; 75:1045-1053.
36. Mammalian Reproductive Genetics [Internet]. Seattle, WA, and Bar Harbor, ME: Department of Genome Sciences, University of Washington and The Jackson Laboratory. http://mrg.genetics.washington.edu/. Accessed 3 August 2007.
37. Lefievre L, Jha KN, de Lamirande E, Visconti PE, Gagnon C. Activation of protein kinase A during human sperm capacitation and acrosome reaction. J Androl 2002; 23:709-716.
38. Liu SL, Ni B, Wang XW, Huo WQ, Zhang J, Tian ZQ, Huang ZM, Tian Y, Tang J, Zheng YH, Jin FS, Li YF. FSCB phosphorylation in mouse spermatozoa capacitation. BMB Rep 2011; 44:541-546.
39. Li YF, He W, Mandal A, Kim YH, Digilio L, Klotz K, Flickinger CJ, Herr JC. CABYR binds to AKAP3 and Ropporin in the human sperm fibrous sheath. Asian J Androl 2011; 13:266-274.
40. Mandal A, Naaby-Hansen S, Wolkowicz MJ, Klotz K, Shetty J, Retief JD, Coonrod SA, Kinter M, Sherman N, Cesar F, Flickinger CJ, Herr JC. FSP95, a testis-specific 95-kilodalton fibrous sheath antigen that undergoes tyrosine phosphorylation in capacitated human spermatozoa. Biol Reprod 1999; 61:1184-1197.
41. Aitken RJ, Nixon B, Lin M, Koppers AJ, Lee YH, Baker MA. Proteomic changes in mammalian spermatozoa during epididymal maturation. Asian J Androl 2007; 9:554-564.
42. Ecroyd H, Asquith KL, Jones RC, Aitken RJ. The development of signal transduction pathways during epididymal maturation is calcium dependent. Dev Biol 2004; 268:53-63.
43. Lewis B, Aitken RJ. Impact of epididymal maturation on the tyrosine phosphorylation patterns exhibited by rat spermatozoa. Biol Reprod 2001; 64:1545-1556.
44. Lin M, Lee YH, Xu W, Baker MA, Aitken RJ. Ontogeny of tyrosine phosphorylation-signaling pathways during spermatogenesis and epididymal maturation in the mouse. Biol Reprod 2006; 75:588-597.
45. Vijayaraghavan S, Stephens DT, Trautman K, Smith GD, Khatra B, da Cruz e Silva EF, Greengard P. Sperm motility development in the epididymis is associated with decreased glycogen synthase kinase-3 and protein phosphatase 1 activity. Biol Reprod 1996; 54:709-718.
46. Visconti PE, Bailey JL, Moore GD, Pan D, Olds-Clarke P, Kopf GS. Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation.Development 1995; 121:1129-1137.
47. Furusawa M, Taira T, Iguchi-Ariga SM, Ariga H. AMY-1 interacts with SAKAP84 and AKAP95 in the cytoplasm and the nucleus, respectively, and inhibits cAMP-dependent protein kinase activity by preventing binding of its catalytic subunit to A-kinase-anchoring protein (AKAP) complex. J Biol Chem 2002; 277:50885-50892.
48. Baccetti B, Collodel G, Estenoz M, Manca D, Moretti E, Piomboni P. Gene deletions in an infertile man with sperm fibrous sheath dysplasia. Hum Reprod 2005; 20:2790-2794.
49. Baccetti B, Collodel G, Gambera L, Moretti E, Serafini F, Piomboni P. Fluorescence in situ hybridization and molecular studies in infertile men with dysplasia of the fibrous sheath. Fertil Steril 2005; 84:123-129.
50. Matzuk MM, Lamb DJ. The biology of infertility: research advances and clinical challenges. Nat Med 2008; 14:1197-1213.
51. Turner RM, Musse MP, Mandal A, Klotz K, Jayes FC, Herr JC, Gerton GL, Moss SB, Chemes HE. Molecular genetic analysis of two human sperm fibrous sheath proteins, AKAP4 and AKAP3, in men with dysplasia of the fibrous sheath. J Androl 2001; 22:302-315.