Cysteine-rich secretory proteins are not exclusively expressed in the male reproductive tract

Developmental Dynamics

Volumn 237, Issue 11, 2008, Pages 3313-3323

  Reddy, Thulasimala ^a   Gibbs, Gerard M ^a   Merriner, D Jo ^a   Kerr, Jeffrey B ^a   O'Bryan, Moira K ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE RICH SECRETORY PROTEIN; MESSENGER RNA; SECRETORY PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; CONTROLLED STUDY; FEMALE; MALE; MALE GENITAL SYSTEM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

ANIMALS; EXOCRINE GLANDS; FEMALE; GENE EXPRESSION REGULATION; GENITALIA, FEMALE; GENITALIA, MALE; MALE; MEMBRANE GLYCOPROTEINS; MICE; ORGAN SPECIFICITY; SPLEEN; THYMUS GLAND;

MAMMALIA; MURINAE; REPTILIA;

EID: 55549129634     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21738     Document Type: Article

References (66)

1. Bjartell A, Johansson R, Bjork T, Gadaleanu V, Lundwall A, Lilja H, Kjeldsen L, Udby L. 2006. Immunohistochemical detection of cysteine-rich secretory protein 3 in tissue and in serum from men with cancer or benign enlargement of the prostate gland. Prostate 66:591-603.
2. Bjartell AS, Al-Ahmadie H, Serio AM, Eastham JA, Eggener SE, Fine SW, Udby L, Gerald WL, Vickers AJ, Lilja H, Reuter VE, Scardino PT. 2007. Association of cysteine-rich secretory protein 3 and beta-microseminoprotein with outcome after radical prostatectomy. Clin Cancer Res 13:4130-4138.
3. Brooks DE. 1982. Purification of rat epididymal proteins "D' and "E', demonstration of shared immunological determinants, and identification of regional synthesis and secretion. Int J Androl 5:513-524.
4. Brown RL, Haley TL, West KA, Crabb JW. 1999. Pseudechetoxin: a peptide blocker of cyclic nucleotide-gated ion channels. Proc Natl Acad Sci USA 96:754-759.
5. Burnett LA, Boyles S, Spencer C, Bieber AL, Chandler DE. 2008. Xenopus tropicalis allurin: Expression, purification, and characterization of a sperm chemoattractant that exhibits cross-species activity. Dev Biol 316:408-416.
6. Busso D, Cohen DJ, Maldera JA, Dematteis A, Cuasnicu PS. 2007. A novel function for CRISP1 in rodent fertilization: involvement in sperm-zona pellucida interaction. Biol Reprod 77:848-854.
7. Charest NJ, Petrusz P, Ordronneau P, Joseph DR, Wilson EM, French FS. 1989. Developmental expression of an androgen-regulated epididymal protein. Endocrinology 125:942-947.
8. Chentoufi AA, Palumbo M, Polychronakos C. 2004. Proinsulin expression by Hassall's corpuscles in the mouse thymus. Diabetes 53:354-359.
9. Cohen DJ, Ellerman DA, Cuasnicu PS. 2000. Mammalian sperm-egg fusion: evidence that epididymal protein DE plays a role in mouse gamete fusion. Biol Reprod 63:462-468.
10. Dauplais M, Lecoq A, Song J, Cotton J, Jamin N, Gilquin B, Roumestand C, Vita C, de Medeiros CL, Rowan EG, Harvey AL, Menez A. 1997. On the convergent evolution of animal toxins. Conservation of a diad of functional residues in potassium channel-blocking toxins with unrelated structures. J Biol Chem 272:4302-4309.
11. Durham WJ, Wehrens XH, Sood S, Hamilton SL. 2007. Diseases associated with altered ryanodine receptor activity. Subcell Biochem 45:273-321.
12. Ellerman DA, Cohen DJ, Da Ros VG, Morgenfeld MM, Busso D, Cuasnicu PS. 2006. Sperm protein "DE" mediates gamete fusion through an evolutionarily conserved site of the CRISP family. Dev Biol 297:228-237.
13. Foster JA, Gerton GL. 1996. Autoantigen 1 of the guinea pig sperm acrosome is the homologue of mouse Tpx-1 and human TPX1 and is a member of the cysteine-rich secretory protein (CRISP) family. Mol Reprod Dev 44:221-229.
14. Gibbs GM, O'Bryan MK. 2007. Cysteine rich secretory proteins in reproduction and venom. Soc Reprod Fertil Suppl 65:261-267.
15. 2+ signaling. J Biol Chem 281:4156-4163.
16. Gibbs GM, Bianco DM, Jamsai D, Herlihy A, Ristevski S, Aitken RJ, Kretser DM, O'Bryan MK. 2007. Cysteine-rich secretory protein 2 binds to mitogen-activated protein kinase kinase kinase 11 in mouse sperm. Biol Reprod 77:108-114.
17. Guo M, Teng M, Niu L, Liu Q, Huang Q, Hao Q. 2005. Crystal structure of cysteine-rich secretory protein stecrisp reveals the cysteine-rich domain has a K+-channel inhibitor-like fold. J Biol Chem 280:12405-12412.
18. Haendler B, Kratzschmar J, Theuring F, Schleuning WD. 1993. Transcripts for cysteine-rich secretory protein-1 (CRISP-1; DE/AEG) and the novel related CRISP-3 are expressed under androgen control in the mouse salivary gland. Endocrinology 133:192-198.
19. Haendler B, Habenicht UF, Schwidetzky U, Schuttke I, Schleuning WD. 1997. Differential androgen regulation of the murine genes for cysteine-rich secretory proteins (CRISP). Eur J Biochem 250:440-446.
20. Haendler B, Toda I, Sullivan DA, Schleuning WD. 1999. Expression of transcripts for cysteine-rich secretory proteins (CRISPs) in the murine lacrimal gland. J Cell Physiol 178:371-378.
21. Hardy DM, Huang TT Jr, Driscoll WJ, Tung KK, Wild GC. 1988. Purification and characterization of the primary acrosomal autoantigen of guinea pig epididymal spermatozoa. Biol Reprod 38:423-437.
22. Harper CV, Barratt CL, Publicover SJ. 2004. 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 279:46315-46325.
23. Henriksen A, King TP, Mirza O, Monsalve RI, Meno K, Ipsen H, Larsen JN, Gajhede M, Spangfort MD. 2001. Major venom allergen of yellow jackets, Ves v 5: structural characterization of a pathogenesis-related protein superfamily. Proteins 45:438-448.
24. Ito N, Mita M, Takahashi Y, Matsushima A, Watanabe YG, Hirano S, Odani S. 2007. Novel cysteine-rich secretory protein in the buccal gland secretion of the parasitic lamprey, Lethenteron japonicum. Biochem Biophys Res Commun 358:35-40.
25. Jalkanen J, Huhtaniemi I, Poutanen M. 2005. Mouse cysteine-rich secretory protein 4 (CRISP4): a member of the crisp family exclusively expressed in the epididymis in an androgen-dependent manner. Biol Reprod 72:1268-1274.
26. Jamsai D, Bianco DM, Smith SJ, Merriner DJ, Niranjan B, Gibbs GM, O'Bryan MK. 2008a. Characterization of gametogenetin 1 (GGN1) and its potential role in male fertility through the interaction with the ion channel regulator, cysteine-rich secretory protein 2 (CRISP2) in the sperm tail. Reproduction 135:751-759.
27. Jamsai D, Bianco DM, Smith SJ, Merriner DJ, Niranjan B, Gibbs GM, O'Bryan MK. 2008b. Polymorphisms in the human cysteine-rich secretory protein 2 (CRISP2) gene in Australian men. Hum Reprod 23:2151-2159.
28. Kasahara M, Gutknecht J, Brew K, Spurr N, Goodfellow PN. 1989. Cloning and mapping of a testis-specific gene with sequence similarity to a sperm-coating glycoprotein gene. Genomics 5:527-534.
29. King TP, Sobotka AK, Alagon A, Kochoumian L, Lichtenstein LM. 1978. Protein allergens of white-faced hornet, yellow hornet, and yellow jacket venoms. Biochemistry 17:5165-5174.
30. Kjeldsen L, Cowland JB, Johnsen AH, Borregaard N. 1996. SGP28, a novel matrix glycoprotein in specific granules of human neutrophils with similarity to a human testis-specific gene product and a rodent sperm-coating glycoprotein. FEBS Lett 380:246-250.
31. Kosari F, Asmann YW, Cheville JC, Vasmatzis G. 2002. Cysteine-rich secretory protein-3: a potential biomarker for prostate cancer. Cancer Epidemiol Biomarkers Prev 11:1419-1426.
32. Kratzschmar J, Haendler B, Eberspaecher U, Roosterman D, Donner P, Schleuning WD. 1996. The human cysteine-rich secretory protein (CRISP) family. Primary structure and tissue distribution of CRISP-1, CRISP-2 and CRISP-3. Eur J Biochem 236:827-836.
33. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
34. Laine M, Porola P, Udby L, Kjeldsen L, Cowland JB, Borregaard N, Hietanen J, Stahle M, Pihakari A, Konttinen YT. 2007. Low salivary dehydroepiandrosterone and androgen-regulated cysteine-rich secretory protein 3 levels in Sjogren's syndrome. Arthritis Rheum 56:2575-2584.
35. Liao Q, Kleeff J, Xiao Y, Guweidhi A, Schambony A, Topfer-Petersen E, Zimmermann A, Buchler MW, Friess H. 2003. Preferential expression of cystein-rich secretory protein-3 (CRISP-3) in chronic pancreatitis. Histol Histopathol 18:425-433.
36. Lu G, Villalba M, Coscia MR, Hoffman DR, King TP. 1993. Sequence analysis and antigenic cross-reactivity of a venom allergen, antigen 5, from hornets, wasps, and yellow jackets. J Immunol 150:2823-2830.
37. Maeda T, Nishida J, Nakanishi Y. 1999. Expression pattern, subcellular localization and structure-function relationship of rat Tpx-1, a spermatogenic cell adhesion molecule responsible for association with Sertoli cells. Dev Growth Differ 41:715-722.
38. Marquez B, Ignotz G, Suarez SS. 2007. Contributions of extracellular and intracellular Ca2+ to regulation of sperm motility: Release of intracellular stores can hyperactivate CatSper1 and CatSper2 null sperm. Dev Biol 303:214-221.
39. Milne TJ, Abbenante G, Tyndall JD, Halliday J, Lewis RJ. 2003. Isolation and characterization of a cone snail protease with homology to CRISP proteins of the pathogenesis-related protein superfamily. J Biol Chem 278:31105-31110.
40. Miosga T, Schaaff-Gerstenschlager I, Chalwatzis N, Baur A, Boles E, Fournier C, Schmitt S, Velten C, Wilhelm N, Zimmermann FK. 1995. Sequence analysis of a 33.1 kb fragment from the left arm of Saccharomyces cerevisiae chromosome X, including putative proteins with leucine zippers, a fungal Zn(II)2-Cys6 binuclear cluster domain and a putative alpha 2-SCB-alpha 2 binding site. Yeast 11:681-689.
41. Morrissette J, Kratzschmar J, Haendler B, el-Hayek R, Mochca-Morales J, Martin BM, Patel JR, Moss RL, Schleuning WD, Coronado R, Possani LD. 1995. Primary structure and properties of helothermine, a peptide toxin that blocks ryanodine receptors. Biophys J 68:2280-2288.
42. Moyle M, Foster DL, McGrath DE, Brown SM, Laroche Y, De Meutter J, Stanssens P, Bogowitz CA, Fried VA, Ely JA, et al. 1994. A hookworm glycoprotein that inhibits neutrophil function is a ligand of the integrin CD11b/CD18. J Biol Chem 269:10008-10015.
43. Murphy EV, Zhang Y, Zhu W, Biggs J. 1995. The human glioma pathogenesis-related protein is structurally related to plant pathogenesis-related proteins and its gene is expressed specifically in brain tumors. Gene 159:131-135.
44. Niderman T, Genetet I, Bruyere T, Gees R, Stintzi A, Legrand M, Fritig B, Mosinger E. 1995. Pathogenesis-related PR-1 proteins are antifungal. Isolation and characterization of three 14-kilodalton proteins of tomato and of a basic PR-1 of tobacco with inhibitory activity against Phytophthora infestans. Plant Physiol 108:17-27.
45. Nixon B, MacIntyre DA, Mitchell LA, Gibbs GM, O'Bryan M, Aitken RJ. 2006. The identification of mouse sperm-surface-associated proteins and characterization of their ability to act as decapacitation factors. Biol Reprod 74:275-287.
46. Nolan MA, Wu L, Bang HJ, Jelinsky SA, Roberts KP, Turner TT, Kopf GS, Johnston DS. 2006. Identification of rat cysteine-rich secretory protein 4 (Crisp4) as the ortholog to human CRISP1 and mouse Crisp4. Biol Reprod 74:984-991.
47. O'Bryan MK, Loveland KL, Herszfeld D, McFarlane JR, Hearn MT, de Kretser DM. 1998. Identification of a rat testis-specific gene encoding a potential rat outer dense fibre protein. Mol Reprod Dev 50:313-322.
48. O'Bryan MK, Sebire K, Meinhardt A, Edgar K, Keah HH, Hearn MT, de Kretser DM. 2001. Tpx-1 is a component of the outer dense fibers and acrosome of rat spermatozoa. Mol Reprod Dev 58:116-125.
49. Olson JH, Xiang X, Ziegert T, Kittelson A, Rawls A, Bieber AL, Chandler DE. 2001. Allurin, a 21-kDa sperm chemoattractant from Xenopus egg jelly, is related to mammalian sperm-binding proteins. Proc Natl Acad Sci USA 98:11205-11210.
50. Pfisterer P, Konig H, Hess J, Lipowsky G, Haendler B, Schleuning WD, Wirth T. 1996. CRISP-3, a protein with homology to plant defense proteins, is expressed in mouse B cells under the control of Oct2. Mol Cell Biol 16:6160-6168.
51. Pfitzner UM, Goodman HM. 1987. Isolation and characterization of cDNA clones encoding pathogenesis-related proteins from tobacco mosaic virus infected tobacco plants. Nucleic Acids Res 15:4449-4465.
52. Roberts KP, Wamstad JA, Ensrud KM, Hamilton DW. 2003. Inhibition of capacitation-associated tyrosine phosphorylation signaling in rat sperm by epididymal protein Crisp-1. Biol Reprod 69:572-581.
53. Rochwerger L, Cuasnicu PS. 1992. Redistribution of a rat sperm epididymal glycoprotein after in vitro and in vivo capacitation. Mol Reprod Dev 31:34-41.
54. Schreiber MC, Karlo JC, Kovalick GE. 1997. A novel cDNA from Drosophila encoding a protein with similarity to mammalian cysteine-rich secretory proteins, wasp venom antigen 5, and plant group 1 pathogenesis-related proteins. Gene 191:135-141.
55. Schuren FH, Asgeirsdottir SA, Kothe EM, Scheer JM, Wessels JG. 1993. The Sc7/Sc14 gene family of Schizophyllum commune codes for extracellular proteins specifically expressed during fruit-body formation. J Gen Microbiol 139:2083-2090.
56. Shikamoto Y, Suto K, Yamazaki Y, Morita T, Mizuno H. 2005. Crystal structure of a CRISP family Ca2+ -channel blocker derived from snake venom. J Mol Biol 350:735-743.
57. Sullivan R, Frenette G, Girouard J. 2007. Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit. Asian J Androl 9:483-491.
58. Tapinos NI, Polihronis M, Thyphronitis G, Moutsopoulos HM. 2002. Characterization of the cysteine-rich secretory protein 3 gene as an early-transcribed gene with a putative role in the pathophysiology of Sjogren's syndrome. Arthritis Rheum 46:215-222.
59. Thimon V, Calvo E, Koukoui O, Legare C, Sullivan R. 2008. Effects of vasectomy on gene expression profiling along the human epididymis. Biol Reprod.
60. Udby L, Bjartell A, Malm J, Egesten A, Lundwall A, Cowland JB, Borregaard N, Kjeldsen L. 2005. Characterization and localization of cysteine-rich secretory protein 3 (CRISP-3) in the human male reproductive tract. J Androl 26:333-342.
61. Wang J, Shen B, Guo M, Lou X, Duan Y, Cheng XP, Teng M, Niu L, Liu Q, Huang Q, Hao Q. 2005. Blocking effect and crystal structure of natrin toxin, a cysteine-rich secretory protein from Naja atra venom that targets the BKCa channel. Biochemistry 44:10145-10152.
62. Warren R, Molday RS. 2002. Regulation of the rod photoreceptor cyclic nucleotide-gated channel. Adv Exp Med Biol 514:205-223.
63. Xiang X, Burnett L, Rawls A, Bieber A, Chandler D. 2004. The sperm chemoattractant "allurin" is expressed and secreted from the Xenopus oviduct in a hormone-regulated manner. Dev Biol 275:343-355.
64. Yamakawa T, Miyata S, Ogawa N, Koshikawa N, Yasumitsu H, Kanamori T, Miyazaki K. 1998. cDNA cloning of a novel trypsin inhibitor with similarity to pathogenesis-related proteins, and its frequent expression in human brain cancer cells. Biochim Biophys Acta 1395:202-208.
65. Yamazaki Y, Brown RL, Morita T. 2002a. Purification and cloning of toxins from elapid venoms that target cyclic nucleotide-gated ion channels. Biochemistry 41:11331-11337.
66. Yamazaki Y, Koike H, Sugiyama Y, Motoyoshi K, Wada T, Hishinuma S, Mita M, Morita T. 2002b. Cloning and characterization of novel snake venom proteins that block smooth muscle contraction. Eur J Biochem 269:2708-2715.