Cysteine-rich secretory protein 4 is an inhibitor of transient receptor potential M8 with a role in establishing sperm function

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 17, 2011, Pages 7034-7039

  Gibbs, Gerard M ^a   Orta, Gerardo ^b   Reddy, Thulasimala ^a   Koppers, Adam J ^a   Martínez López, Pablo ^b   De La Vega Beltràn, José Luis ^b   Lo, Jennifer C Y ^a   Veldhuis, Nicholas ^c   Jamsai, Duangporn ^a   McIntyre, Peter ^c   Darszon, Alberto ^b   O'Bryan, Moira K ^a  

^a MONASH UNIVERSITY   (Australia)

^b INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Antigen 5; Cysteine rich secretory proteins; Epididymal maturation; Fertility; Pathogenesis related 1

Indexed keywords

CYSTEINE RICH SECRETORY PROTEIN; CYSTEINE RICH SECRETORY PROTEIN 2; CYSTEINE RICH SECRETORY PROTEIN 4; ION CHANNEL; PROGESTERONE; PROTEIN; RYANODINE RECEPTOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL M8; UNCLASSIFIED DRUG;

ACROSOME REACTION; ANIMAL CELL; ARTICLE; CELL ASSAY; CHO CELL; ELECTROPHYSIOLOGY; EPIDIDYMIS; FEMALE; HOMEOSTASIS; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; SPERM;

ACROSOME REACTION; ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; HUMANS; MALE; MICE; MICE, KNOCKOUT; PROGESTERONE; PROGESTINS; SEMINAL PLASMA PROTEINS; SPERMATOZOA; TRPM CATION CHANNELS;

MAMMALIA; MUS; REPTILIA;

EID: 79955569953     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1015935108     Document Type: Article

References (57)

1. Baker HWG (2008) Clinical management of male infertility. Endocrinology of Male Reproduction, ed. McLachlan RI (MDText.com, Inc., S. Darmouth). Available at http://www.endotext.org/male/index.htm.
2. Yanagimachi R (1994) The Physiology of Reproduction, eds Knobil E, Neill JD (Raven Press, Ltd., New York), pp 189-317.
3. Aitken RJ, et al. (2007) Proteomic changes inmammalian spermatozoa duringepididymal maturation. Asian J Androl 9:554-564. (Pubitemid 47046163)
4. Cornwall GA (2009) New insights into epididymal biology and function. Hum Reprod Update 15:213-227.
5. Salicioni AM, et al. (2007) Signalling pathways involved in sperm capacitation. Soc Reprod Fertil Suppl 65:245-259.
6. Darszon A, et al. (2007) Ion channels in sperm motility and capacitation. Soc Reprod Fertil Suppl 65:229-244.
7. 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. (Pubitemid 40547992)
8. Nolan MA, et al. (2006) Identification of rat cysteine-rich secretory protein 4 (Crisp4) as the ortholog to human CRISP1 and mouse Crisp4. Biol Reprod 74:984-991.
9. Gibbs GM, Roelants K, O'Bryan MK (2008) The CAP superfamily: Cysteine-rich secretory proteins, antigen 5, and pathogenesis-related 1 proteins-roles in reproduction, cancer, and immune defense. Endocr Rev 29:865-897.
10. Gibbs GM, et al. (2006) The cysteine-rich secretory protein domain of Tpx-1 is related to ion channel toxins and regulates ryanodine receptor Ca2+ signaling. J Biol Chem 281:4156-4163. (Pubitemid 43847843)
11. Guo M, et al. (2005) Crystal structure of the cysteine-rich secretory protein stecrisp reveals that the cysteine-rich domain has a K+ channel inhibitor-like fold. J Biol Chem 280:12405-12412.
12. Yamazaki Y, Morita T (2004) Structure and function of snake venom cysteine-rich secretory proteins. Toxicon 44:227-231. (Pubitemid 39078338)
13. Gibbs GM, O'Bryan MK (2007) Cysteine rich secretory proteins in reproduction and venom. Soc Reprod Fertil Suppl 65:261-267.
14. Koppers AJ, Reddy T, O'Bryan MK (2011) The role of cysteine-rich secretory proteins in male fertility. Asian J Androl 13(1):111-117.
15. 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. (Pubitemid 26171185)
16. 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. (Pubitemid 30026668)
17. O'Bryan MK, et al. (2001) Tpx-1 is a component of the outer dense fibers and acrosome of rat spermatozoa. Mol Reprod Dev 58:116-125.
18. Eberspaecher U, et al. (1995) Mouse androgen-dependent epididymal glycoprotein CRISP-1 (DE/AEG): Isolation, biochemical characterization, and expression in recombinant form. Mol Reprod Dev 42(2):157-172.
19. Krätzschmar J, et al. (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.
20. 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. (Pubitemid 35340379)
21. Bjartell A, et al. (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.
22. Esposito G, et al. (2004) Mice deficient for soluble adenylyl cyclase are infertile because of a severe sperm-motility defect. Proc Natl Acad Sci USA 101:2993-2998. (Pubitemid 38332002)
23. Suarez SS (2008) Control of hyperactivation in sperm. Hum Reprod Update 14: 647-657.
24. Florman HM (1994) Sequential focal and global elevations of sperm intracellular Ca2+ are initiated by the zona pellucida during acrosomal exocytosis. Dev Biol 165(1): 152-164.
25. De Blas GA, et al. (2009) TRPM8, a versatile channel in human sperm. PLoS ONE 4: e6095.
26. Brauchi S, Orio P, Latorre R (2004) Clues to understanding cold sensation: Thermodynamics and electrophysiological analysis of the cold receptor TRPM8. Proc Natl Acad Sci USA 101: 15494-15499. (Pubitemid 39441569)
27. Martínez-López P, et al. (2011) TRPM8 in mouse sperm detects temperature changes and may influence the acrosome reaction. J Cell Physiol 226:1620-1631.
28. Martínez-López P, et al. (2009) Mouse sperm K+ currents stimulated by pH and cAMP possibly coded by Slo3 channels. Biochem Biophys Res Commun 381:204-209.
29. Jungnickel MK, Marrero H, Birnbaumer L, Lémos JR, Florman HM (2001) Trp2 regulates entry of Ca2+ into mouse sperm triggered by egg ZP3. Nat Cell Biol 3:499-502. (Pubitemid 32422086)
30. Treviño CL, Serrano CJ, Beltrán C, Felix R, Darszon A (2001) Identification of mouse trp homologs and lipid rafts from spermatogenic cells and sperm. FEBS Lett 509(1): 119-125. (Pubitemid 33153093)
31. Dragoni I, Guida E, McIntyre P (2006) The cold and menthol receptor TRPM8 contains a functionally important double cysteine motif. J Biol Chem 281:37353-37360. (Pubitemid 46042039)
32. Behrendt HJ, Germann T, Gillen C, Hatt H, Jostock R (2004) Characterization of the mouse cold-menthol receptor TRPM8 and vanilloid receptor type-1 VR1 using a fluorometric imaging plate reader (FLIPR) assay. Br J Pharmacol 141:737-745. (Pubitemid 38453266)
33. Reddy T, Gibbs GM, Merriner DJ, Kerr JB, O'Bryan MK (2008) Cysteine-rich secretory proteins are not exclusively expressed in the male reproductive tract. Dev Dyn 237: 3313-3323.
34. Levine N, Marsh DJ (1971) Micropuncture studies of the electrochemical aspects of fluid and electrolyte transport in individual seminiferous tubules, the epididymis and the vas deferens in rats. J Physiol 213:557-570.
35. Vijayaraghavan S, Hoskins DD (1990) Changes in the mitochondrial calcium influx and efflux properties are responsible for the decline in sperm calcium during epididymal maturation. Mol Reprod Dev 25(2):184-194.
36. Ecroyd H, Asquith KL, Jones RC, Aitken RJ (2004) The development of signal transduction pathways during epididymal maturation is calcium dependent. Dev Biol 268(1):53-63. (Pubitemid 38367849)
37. Naono-Nakayama R, Sunakawa N, Ikeda T, Nishimori T (2010) Differential effects of substance P or hemokinin-1 on transient receptor potential channels, TRPV1, TRPA1 and TRPM8, in the rat. Neuropeptides 44(1):57-61.
38. Peier AM, et al. (2002) A TRP channel that senses cold stimuli and menthol. Cell 108: 705-715. (Pubitemid 34241429)
39. Dhaka A, et al. (2007) TRPM8 is required for cold sensation in mice. Neuron 54: 371-378. (Pubitemid 46659806)
40. Bautista DM, et al. (2007) The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448:204-208. (Pubitemid 47067367)
41. Staaf S, Franck MC, Marmigere F, Mattsson JP, Ernfors P (2010) Dynamic expression of the TRPM subgroup of ion channels in developing mouse sensory neurons. Gene Expr Patterns 10(1):65-74.
42. Tsavaler L, Shapero MH, Morkowski S, Laus R (2001) Trp-p8, a novel prostate-specific gene, is up-regulated in prostate cancer and other malignancies and shares high homology with transient receptor potential calcium channel proteins. Cancer Res 61: 3760-3769. (Pubitemid 32694990)
43. Liu B, Qin F (2005) Functional control of cold- and menthol-sensitive TRPM8 ion channels by phosphatidylinositol 4,5-bisphosphate. J Neurosci 25:1674-1681. (Pubitemid 40279272)
44. Daniels RL, Takashima Y, McKemy DD (2009) Activity of the neuronal cold sensor TRPM8 is regulated by phospholipase C via the phospholipid phosphoinositol 4,5-bisphosphate. J Biol Chem 284:1570-1582.
45. Gordon-Shaag A, Zagotta WN, Gordon SE (2008) Mechanism of Ca(2+)-dependent desensitization in TRP channels. Channels (Austin) 2(2):125-129.
46. Premkumar LS, Raisinghani M, Pingle SC, Long C, Pimentel F (2005) Downregulation of transient receptor potential melastatin 8 by protein kinase C-mediated dephosphorylation. J Neurosci 25:11322-11329. (Pubitemid 43083706)
47. Abe J, Hosokawa H, Sawada Y, Matsumura K, Kobayashi S (2006) Ca2+-dependent PKC activation mediates menthol-induced desensitization of transient receptor potential M8. Neurosci Lett 397(1-2):140-144. (Pubitemid 43340475)
48. Wang J, et al. (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. (Pubitemid 41076809)
49. Da Ros VG, et al. (2008) Impaired sperm fertilizing ability in mice lacking Cysteine-Rlch Secretory Protein 1 (CRISP1). Dev Biol 320(1):12-18.
50. Berridge MJ, Bootman MD, Lipp P (1998) Calcium-aA life and death signal. Nature 395:645-648.
51. Roderick HL, Cook SJ (2008) Ca2+ signalling checkpoints in cancer: remodelling Ca2+ for cancer cell proliferation and survival. Nat Rev Cancer 8:361-375. (Pubitemid 351589702)
52. Kaczorowski GJ, McManus OB, Priest BT, Garcia ML (2008) Ion channels as drug targets: The next GPCRs. J Gen Physiol 131:399-405. (Pubitemid 351620096)
53. Kirichok Y, Navarro B, Clapham DE (2006) Whole-cell patch-clamp measurements of spermatozoa reveal an alkaline-activated Ca2+ channel. Nature 439:737-740. (Pubitemid 43237621)
54. Beltrán C, Darszon A, Labarca P, Liévano A (1994) A high-conductance voltage-dependent multistate Ca2+ channel found in sea urchin and mouse spermatozoa. FEBS Lett 338(1):23-26.
55. Cowin PA, et al. (2010) Vinclozolin exposure in utero induces postpubertal prostatitis and reduces sperm production via a reversible hormone-regulated mechanism. Endocrinology 151:783-792.
56. Cotton L, et al. (2006) FGFR-1 [corrected] signaling is involved in spermiogenesis and sperm capacitation. J Cell Sci 119(1):75-84. (Pubitemid 43169300)
57. Borg CL, Wolski KM, Gibbs GM, O'Bryan MK (2010) Phenotyping male infertility in the mouse: how to get the most out of a 'non-performer'. Hum Reprod Update 16: 205-224.