CABS1 is a novel calcium-binding protein specifically expressed in elongate spermatids of mice

Biology of Reproduction

Volumn 80, Issue 6, 2009, Pages 1293-1304

  Kawashima, Akihiro ^a   Osman, Boran A H ^b   Takashima, Minoru ^b   Kikuchi, Akihiko ^b   Kohchi, Sae ^a   Satoh, Emiko ^b   Tamba, Michiko ^b   Matsuda, Manabu ^b   Okamura, Naomichi ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Busulfan; Calcium; Signal transduction; Sperm maturation; Spermatogenesis

Indexed keywords

ACID PROTEIN; BUSULFAN; CALCIUM BINDING PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; CALCIUM BINDING; CELL CYCLE; CONTROLLED STUDY; EPIDIDYMIS; FLAGELLUM; MALE; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; SEMINIFEROUS TUBULE EPITHELIUM; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; SPERMATOZOON MATURATION; TESTIS; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; BUSULFAN; CALCIUM; CALCIUM-BINDING PROTEINS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; MALE; MICE; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SPERM TAIL; SPERMATIDS; SPERMATOGENESIS; TESTIS;

MUS;

EID: 66149112026     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.108.073866     Document Type: Article

References (74)

1. Sharpe RM. Regulation of spermatogenesis. In: Knobil E, Neill JD (eds.), The Physiology of Reproduction, vol.1, 2nd ed. New York: Raven Press; 1994:1363-1434.
2. Russell LD, Ettlin RA, Sinha Hikim AP, Clegg ED. Mammalian spermatogenesis. In: Russell LD, Ettlin RA, Sinha Hikim AP, Clegg ED (eds.), Histological and Histopathological Evaluation of the Testis, 1st ed. Clearwater, FL: Cache River Press; 1990:1-40.
3. Weinbauer GF, Wessels J. 'Paracrine' control of spermatogenesis. Andrologia 1999; 31:249-262.
4. Willison K, Ashworth A. Mammalian spermatogenic gene expression. Trends Genet 1987; 3:351-355.
5. Hecht NB. Molecular mechanisms of male germ cell differentiation. Bioessays 1998; 20:555-561. (Pubitemid 28362301)
6. Jegou B, Pineau C, Dupair A. Paracrine control of testis function. In: Wang C (ed.), Male Reproductive Function (Endocrine Updates). Boston: Kluwer Academic Publishers; 1999:41-64.
7. Tanaka H, Nozaki M, Yomogida K, Nishimune Y. Cloning and characterization of male germ-cell-specific genes. In: Rommerts FFG, Teerds KJ (eds.), Testicular Tangrams. Berlin: Springer Verlag; 2002:53-73.
8. Eddy EM. Male germ cell gene expression. Recent Prog Horm Res 2002; 57:103-128.
9. Brinster RL, Avarbock MR. Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci U S A 1994; 91:11303-11307. (Pubitemid 24356332)
10. Brinster RL, Zimmermann JW. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci U S A 1994; 91:11298-11302. (Pubitemid 24356331)
11. Ogawa T, Dobrinski I, Brinster RL. Recipient preparation is critical for spermatogonial transplantation in the rat. Tissue Cell 1999; 31:461-472. (Pubitemid 29531288)
12. Brinster CJ, Ryu BY, Avarbock MR, Karagenc L, Brinster RL, Orwig KE. Restoration of fertility by germ cell transplantation requires effective recipient preparation. Biol Reprod 2003; 69:412-420. (Pubitemid 36885943)
13. Honaramooz A, Behboodi E, Hausler CL, Blash S, Ayres S, Azuma C, Echelard Y, Dobrinski I. Depletion of endogenous germ cells in male pigs and goats in preparation for germ cell transplantation. J Androl 2005; 26:698-705. (Pubitemid 41476628)
14. Buggia I, Locatelli F, Regazzi MB, Zecca M. Busulfan. Ann Pharmacother 1994; 28:1055-1062.
15. Haddad S, Carvalho TL, Anselmo-Franci JA, Petenusci SO, Favaretto AL. Ultrasound stimulation of rat testes damaged by busulfan. Ultrasound Med Biol 1997; 23:1421-1425. (Pubitemid 27506344)
16. Choi YJ, Ok DW, Kwon DN, Chung JI, Kim HC, Yeo SM, Kim T, Seo HG, Kim JH. Murine male germ cell apoptosis induced by busulfan treatment correlates with loss of c-kit-expression in a Fas/FasL- and p53- independent manner. FEBS Lett 2004; 575:41-51. (Pubitemid 39237679)
17. Kanatsu-Shinohara M, Toyokuni S, Morimoto T, Matsui S, Honjo T, Shinohara T. Functional assessment of self-renewal activity of male germline stem cells following cytotoxic damage and serial transplantation. Biol Reprod 2003; 68:1801-1807. (Pubitemid 36519788)
18. Jiahao S, Zuomin ZH, Jianmin L. Preparation of human testicular cDNA microarray and initial research of gene expression library related to spermatogenesis. In: Chan HS (ed.), Epithelial Cell Biology - A Primer. Beijing: Press of Military Medical Science; 2000:274-277.
19. Noguchi J, Hikono H, Sato S, Watanabe G, Taya K, Sasamoto S, Hasegawa Y. Ontogeny of inhibin secretion in the rat testis: secretion of inhibin-related proteins from fetal Leydig cells and of bioactive inhibin from Sertoli cells. J Endocrinol 1997; 155:27-34. (Pubitemid 27428302)
20. Campbell KP, MacLennan DH, Jorgensen AO. Staining of the Ca2+-binding proteins, calsequestrin, calmodulin, troponin C, and S-100, with the cationic carbocyanine dye "Stains-all". J Biol Chem 1983; 258:11267-11273.
21. Charuk JH, Pirraglia CA, Reithmeier RA. Interaction of ruthenium red with Ca2(+)-binding proteins. Anal Biochem 1990; 188:123-131. (Pubitemid 20215886)
22. Caday CG, Steiner RF. The interaction of calmodulin with the carbocyanine dye (Stains-all). J Biol Chem 1985; 260:5985-5990. (Pubitemid 15072499)
23. Nakamura M, Moriya M, Baba T, Michikawa Y, Yamanobe T, Arai K, Okinaga S, Kobayashi T. An endoplasmic reticulum protein, calreticulin, is transported into the acrosome of rat sperm. Exp Cell Res 1993; 205:101-110. (Pubitemid 23192108)
24. Huo R, Zhu YF, Ma X, Lin M, Zhou ZM, Sha JH. Differential expression of glucose-regulated protein 78 during spermatogenesis. Cell Tissue Res 2004; 316:359-367. (Pubitemid 38824002)
25. Aumuller G, Seitz J. Immunocytochemical localization of actin and tubulin in rat testis and spermatozoa. Histochemistry 1988; 89:261-267. (Pubitemid 18146945)
26. Lopez-Fernandez LA, del Mazo J. The cytosolic aldehyde dehydrogenase gene (Aldh1) is developmentally expressed in Leydig cells. FEBS Lett 1997; 407:225-229. (Pubitemid 27199497)
27. Gelly JL, Richoux JP, Grignon G. Immunolocalization of albumin and transferrin in germ cells and Sertoli cells during rat gonadal morphogenesis and postnatal development of the testis. Cell Tissue Res 1994; 276:347-351. (Pubitemid 24125481)
28. Zhu LJ, Zong SD, Phillips DM, Moo-Young AJ, Bardin CW. Changes in the distribution of intermediate filaments in rat Sertoli cells during the seminiferous epithelium cycle and postnatal development. Anat Rec 1997; 248:391-405. (Pubitemid 27280146)
29. Kobayashi T, Kaneko T, Iuchi Y, Matsuki S, Takahashi M, Sasagawa I, Nakada T, Fujii J. Localization and physiological implication of aldose reductase and sorbitol dehydrogenase in reproductive tracts and spermatozoa of male rats. J Androl 2002; 23:674-683.
30. Asquith KL, Harman AJ, McLaughlin EA, Nixon B, Aitken RJ. Localization and significance of molecular chaperones, heat shock protein 1, and tumor rejection antigen gp96 in the male reproductive tract and during capacitation and acrosome reaction. Biol Reprod 2005; 72:328-337. (Pubitemid 40129708)
31. Welch JE, O'Rand MG. Characterization of a sperm-specific nuclear autoantigenic protein. II. Expression and localization in the testis. Biol Reprod 1990; 43:569-578.
32. Tsuchida J, Nishina Y, Wakabayashi N, Nozaki M, Sakai Y, Nishimune Y. Molecular cloning and characterization of meichroacidin (male meiotic metaphase chromosome-associated acidic protein). Dev Biol 1998; 197:67-76. (Pubitemid 28224228)
33. Wu XQ, Lefrancois S, Morales CR, Hecht NB. Protein-protein interactions between the testis brain RNA-binding protein and the transitional endoplasmic reticulum ATPase, a cytoskeletal gamma actin and Trax in male germ cells and the brain. Biochemistry 1999; 38:11261-11270. (Pubitemid 129516702)
34. Gold B, Fujimoto H, Kramer JM, Erickson RP, Hecht NB. Haploid accumulation and translational control of phosphoglycerate kinase-2 messenger RNA during mouse spermatogenesis. Dev Biol 1983; 98:392-399.
35. Moriya M, Ochiai M, Yuasa HJ, Suzuki N, Yazawa M. Identification of Ca2+-dependent calmodulin-binding proteins in rat spermatogenic cells as complexes of the heat-shock proteins. Mol Reprod Dev 2004; 69:316-324. (Pubitemid 39315014)
36. Ohtani H, Wakui H, Ishino T, Komatsuda A, Miura AB. An isoform of protein disulfide isomerase is expressed in the developing acrosome of spermatids during rat spermiogenesis and is transported into the nucleus of mature spermatids and epididymal spermatozoa. Histochemistry 1993; 100:423-429. (Pubitemid 24049311)
37. O'Shaughnessy PJ, Murphy L. Cytochrome P-450 17 alpha-hydroxylase protein and mRNA in the testis of the testicular feminized (Tfm) mouse. J Mol Endocrinol 1993; 11:77-82. (Pubitemid 23297953)
38. Srivastava RA, Bhasin N, Srivastava N. Apolipoprotein E gene expression in various tissues of mouse and regulation by estrogen. Biochem Mol Biol Int 1996; 38:91-101. (Pubitemid 26340465)
39. Huang SY, Tam MF, Hsu YT, Lin JH, Chen HH, Chuang CK, Chen MY, King YT, Lee WC. Developmental changes of heat-shock proteins in porcine testis by a proteomic analysis. Theriogenology 2005; 64:1940-1955.
40. Sha J, Zhou Z, Li J, Yin L, Yang H, Hu G, Luo M, Chan HC, Zhou K. Spermatogenesis study group. Identification of testis development and spermatogenesis-related genes in human and mouse testes using cDNA arrays. Mol Hum Reprod 2002; 8:511-517.
41. Kawasaki K, Weiss KM. Mineralized tissue and vertebrate evolution: the secretory calcium-binding phosphoprotein gene cluster. Proc Natl Acad Sci U S A 2003; 100:4060-4065. (Pubitemid 36418157)
42. Benton L, Shan LX, Hardy MP. Differentiation of adult Leydig cells. J Steroid Biochem Mol Biol 1995; 53:61-68.
43. O'Shaughnessy PJ, Willerton L, Baker PJ. Changes in Leydig cell gene expression during development in the mouse. Biol Reprod 2002; 66:966-975. (Pubitemid 34263116)
44. Thomas K, Del Mazo J, Eversole P, Bellve A, Hiraoka Y, Li SS, Simon M. Developmental regulation of expression of the lactate dehydrogenase (LDH) multigene family during mouse spermatogenesis. Development 1990; 109:483-493. (Pubitemid 20205586)
45. Kashiwabara S, Arai Y, Kodaira K, Baba T. Acrosin biosynthesis in meiotic and postmeiotic spermatogenic cells. Biochem Biophys Res Commun 1990; 173:240-245.
46. Van der Hoorn FA, Tarnasky HA, Nordeen SK. A new rat gene RT7 is specifically expressed during spermatogenesis. Dev Biol 1990; 142:147-154. (Pubitemid 20375973)
47. Coucouvanis EC, Jones PP. Changes in protooncogene expression correlated with general and sex-specific differentiation in murine primordial germ cells. Mech Dev 1993; 42:49-58.
48. Mali P, Kaipia A, Kangasniemi M, Toppari J, Sandberg M, Hecht NB, Parvinen M. Stage-specific expression of nucleoprotein mRNAs during rat and mouse spermiogenesis. Reprod Fertil Dev 1989; 1:369-382. (Pubitemid 20121836)
49. Kurth BE, Klotz K, Flickinger CJ, Herr JC. Localization of sperm antigen SP-10 during the six stages of the cycle of the seminiferous epithelium in man. Biol Reprod 1991; 44:814-821.
50. Kido T, Lau YF. The rat Tspy is preferentially expressed in elongated spermatids and interacts with the core histones. Biochem Biophys Res Commun 2006; 350:56-67. (Pubitemid 44466573)
51. Zheng H, Stratton CJ, Morozumi K, Jin J, Yanagimachi R, Yan W. Lack of Spem1 causes aberrant cytoplasm removal, sperm deformation, and male infertility. Proc Natl Acad Sci U S A 2007; 104:6852-6857. (Pubitemid 47175590)
52. Iida H, Doiguchi M, Yamashita H, Sugimachi S, Ichinose J, Mori T, Shibata Y. Spermatid-specific expression of Iba1, an ionized calcium binding adapter molecule-1, in rat testis. Biol Reprod 2001; 64:1138-1146. (Pubitemid 32239184)
53. Walensky LD, Snyder SH. Inositol 1,4,5-trisphosphate receptors selectively localized to the acrosomes of mammalian sperm. J Cell Biol 1995; 130:857-869.
54. Harper CV, Barratt CL, Publicover SJ. Stimulation of human spermatozoa with progesterone gradients to simulate approach to the oocyte. Induction of [Ca(2+)](i) oscillations and cyclical transitions in flagellar beating. J Biol Chem 2004; 279:46315-46325.
55. Harper C, Wootton L, Michelangeli F, Lefievre L, Barratt C, Publicover S. Secretory pathway Ca(2+)-ATPase (SPCA1) Ca(2)+ pumps, not SERCAs, regulate complex [Ca(2+)](i) signals in human spermatozoa. J Cell Sci 2005; 118:1673-1685.
56. Lawson C, Dorval V, Goupil S, Leclerc P. Identification and localisation of SERCA 2 isoforms in mammalian sperm. Mol Hum Reprod 2007; 13:307-316. (Pubitemid 47061641)
57. Publicover S, Harper CV, Barratt C. [Ca2+]i signalling in sperm-making the most of what you've got. Nat Cell Biol 2007; 9:235-242.
58. Qi H, Moran MM, Navarro B, Chong JA, Krapivinsky G, Krapivinsky L, Kirichok Y, Ramsey IS, Quill TA, Clapham DE. All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility. Proc Natl Acad Sci U S A 2007; 104:1219-1223.
59. Darszon A, Acevedo JJ, Galindo BE, Hernandez-Gonzalez EO, Nishigaki T, Trevino CL, Wood C, Beltran C. Sperm channel diversity and functional multiplicity. Reproduction 2006; 131:977-988. (Pubitemid 43904971)
60. Schuh K, Cartwright EJ, Jankevics E, Bundschu K, Liebermann J, Williams JC, Armesilla AL, Emerson M, Oceandy D, Knobeloch KP, Neyses L. Plasma membrane Ca2+ ATPase 4 is required for sperm motility and male fertility. J Biol Chem 2004; 279:28220-28226. (Pubitemid 38900098)
61. Wennemuth G, Babcock DF, Hille B. Calcium clearance mechanisms of mouse sperm. J Gen Physiol 2003; 122:115-128. (Pubitemid 36859135)
62. Okunade GW, Miller ML, Pyne GJ, Sutliff RL, O'Connor KT, Neumann JC, Andringa A, Miller DA, Prasad V, Doetschman T, Paul RJ, Shull GE. Targeted ablation of plasma membrane Ca2+-ATPase (PMCA) 1 and 4 indicates a major housekeeping function for PMCA1 and a critical role in hyperactivated sperm motility and male fertility for PMCA4. J Biol Chem 2004; 279:337:42-50. (Pubitemid 39063023)
63. Naaby-Hansen S, Wolkowicz MJ, Klotz K, Bush LA, Westbrook VA, Shibahara H, Shetty J, Coonrod SA, Reddi PP, Shannon J, Kinter M, Sherman NE, et al. Co-localization of the inositol 1,4,5-trisphosphate receptor and calreticulin in the equatorial segment and in membrane bounded vesicles in the cytoplasmic droplet of human spermatozoa. Mol Hum Reprod 2001; 7:923-933.
64. 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. (Pubitemid 34163983)
65. 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. (Pubitemid 350159471)
66. Scott BT, Simmerman HK, Collins JH, Nadal-Ginard B, Jones LR. Complete amino acid sequence of canine cardiac calsequestrin deduced by cDNA cloning. J Biol Chem 1988; 263:958-964. (Pubitemid 18163154)
67. Sharma Y, Rao CM, Rao SC, Gopala Krishna A, Somasundaram T, Balasubramanian D. Binding site conformation dictates the color of the dye Stains-all. J Biol Chem 1989; 264:20923-20927.
68. Serrano L, Wandosell F, Diez JC, Avila J. The combined use of limited proteolysis and differential peptide staining for protein characterization. J Biochem Biophys Methods 1986; 12:281-287. (Pubitemid 16100373)
69. Sharma Y, Balasubramanian D. Stains-all is a dye that probes the conformational features of calcium binding proteins. In: Heizmann CW (ed.), Novel Calcium-Binding Proteins. Berlin: Springer-Verlag; 1991:51-61.
70. Caday CG, Lambooy PK, Steiner RF. The interaction of Ca2+-binding proteins with the carbocyanine dye stains-all. Biopolymers 1986; 25:1579-1595.
71. Sharma Y, Rao CM, Narasu ML, Rao SC, Somasundaram T, Gopalakrishna A, Balasubramanian D. Calcium ion binding to delta- and to beta-crystallins. The presence of the "EF-hand" motif in delta-crystallin that aids in calcium ion binding. J Biol Chem 1989; 264:12794-12799.
72. Yuasa K, Maeshima M. Purification, properties, and molecular cloning of a novel Ca(2+)-binding protein in radish vacuoles. Plant Physiol 2000; 124:1069-1078.
73. Graceffa P, Jancso A, Mabuchi K. Modification of acidic residues normalizes sodium sulfate-polyacrylamide gel electrophoresis of caldesmon and other proteins that migrate anomalously. Arch Biochem Biophys 1992; 297:46-51.
74. Alves VS, Pimenta DC, Sattlegger E, Castilho BA. Biophysical characterization of Gir2, a highly acidic protein of Saccharomyces cerevisiae with anomalous electrophoretic behavior. Biochem Biophys Res Commun 2004; 314:229-234. (Pubitemid 38058392)