Functional characterization of a mouse testicular olfactory receptor and its role in chemosensing and in regulation of sperm motility

Journal of Cell Science

Volumn 117, Issue 24, 2004, Pages 5835-5845

  Fukuda, Nanaho ^a   Yomogida, Kentaro ^b   Okabe, Masaru ^b   Touhara, Kazushige ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

Calcium; Chemotaxis; Odorant; Olfactory receptor; Sperm; Testis

Indexed keywords

CALCIUM; CYCLIC AMP DERIVATIVE; G PROTEIN COUPLED RECEPTOR; LIGAND;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CHEMORECEPTOR; CHEMOSENSITIVITY; CHEMOTAXIS; CONTROLLED STUDY; DEVELOPMENTAL STAGE; FERTILIZATION; FLAGELLUM; GERM CELL; IN SITU HYBRIDIZATION; MOUSE; NONHUMAN; OLFACTORY EPITHELIUM; OLFACTORY RECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOZOON; SPERMATOZOON MIGRATION; SPERMATOZOON MOTILITY; TESTIS; TRANSGENIC MOUSE;

ANIMALS; CALCIUM; CELL LINE; CELL MOVEMENT; CHEMOTAXIS; CYCLIC AMP; DOSE-RESPONSE RELATIONSHIP, DRUG; FERTILIZATION; FLAGELLA; GERM CELLS; HUMANS; IN SITU HYBRIDIZATION; MALE; MICE; MICE, TRANSGENIC; MODELS, CHEMICAL; OLFACTORY RECEPTOR NEURONS; RECEPTORS, ODORANT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPERM MOTILITY; SPERM-OVUM INTERACTIONS; SPERMATIDS; SPERMATOZOA; TESTIS; TIME FACTORS; TISSUE DISTRIBUTION;

ANIMALIA; MUS MUSCULUS;

EID: 12344307640     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01507     Document Type: Article

References (51)

1. Araneda, R. C., Kini, A. D. and Firestein, S. (2000). The molecular receptive range of an odorant receptor. Nat. Neurosci. 3, 1248-1255.
2. Asai, H., Kasai, H., Matsuda, Y., Yamazaki, N., Nagawa, F., Sakano, H. and Tsuboi, A. (1996). Genomic structure and transcription of a murine odorant receptor gene: differential initiation of transcription in the olfactory and testicular cells. Biochem. Biophys. Res. Commun. 221, 240-247.
3. Baldi, E., Luconi, M., Bonaccorsi, L. and Forti, G. (2002). Signal transduction pathways in human spermatozoa. J. Reprod. Immunol. 53, 121-131.
4. Cohen-Dayag, A., Ralt, D., Tur-Kaspa, I., Manor, M., Makler, A., Dor, J., Mashiach, S. and Eisenbach, M. (1994). Sequential acquisition of chemotactic responsiveness by human spermatozoa. Biol. Reprod. 50, 786-790.
5. Cohen-Dayag, A., Tur-Kaspa, I., Dor, J., Mashiach, S. and Eisenbach, M. (1995). Sperm capacitation in humans is transient and correlates with chemotactic responsiveness to follicular factors. Proc. Natl. Acad. Sci. USA 92, 11039-11043.
6. Darszon, A., Beltran, C., Felix, R., Nishigaki, T. and Trevino, C. L. (2001). Ion transport in sperm signaling. Dev. Biol. 240, 1-14.
7. Dawson, T. M., Arriza, J. L., Jaworsky, D. E., Borisy, F. F., Attramadal, H., Lefkowitz, R. J. and Ronnett, G. V. (1993). Beta-adrenergic receptor kinase-2 and beta-arrestin-2 as mediators of odorant-induced desensitization. Science 259, 825-829.
8. Defer, N., Marinx, O., Poyard, M., Lienard, M. O., Jegou, B. and Hanoune, J. (1998). The olfactory adynylyl cylase type 3 is expressed in male germ cells. FEBS Lett. 424, 216-220.
9. Drabent, B., Bode, C., Bramlage, B. and Doenecke, D. (1996). Expression of the mouse testicular histone gene Hlt during spermatogenesis. Histochem. Cell Biol. 106, 247-251.
10. Eisenbach, M. (1999). Sperm chemotaxis. Rev. Reprod. 4, 56-66.
11. Eisenbach, M. and Tur-Kaspa, I. (1999). Do human eggs attract spermatozoa? BioEssays 21, 203-210.
12. Firestein, S. (2001). How the olfactory system makes sense of scents. Nature 413, 211-218.
13. Gautier-Courteille, C., Salanova, M. and Conti, M. (1998). The olfactory adenylyl cyclase III is expressed in rat germ cells during spermiogenesis. Endocrinology 139, 2588-2599.
14. Gibbons, B. H. and Gibbons, I. R. (1980). Calcium-induced quiescence in reactivated sea urchin sperm. J. Cell Biol. 84, 13-27.
15. Izumi, H., Marian, T., Inaba, K., Oka, Y. and Morisawa, M. (1999). Membrane hyperpolarization by sperm-activating and -attracting factor increases cAMP level and activates sperm motility in the ascidian Ciona intestinalis. Dev. Biol. 213, 246-256.
16. Jaiswal, B. S., Tur-Kaspa, I., Dor, J., Mashiach, S. and Eisenbach, M. (1999). Human sperm chemotaxis: is progesterone a chemoattractant? Biol. Reprod. 60, 1314-1319.
17. Kajiya, K., Inaki, K., Tanaka, M., Haga, T., Kataoka, H. and Touhara, K. (2001). Molecular bases of odor discrimination: reconstitution of olfactory receptors that recognize overlapping sets of odorants. J. Neurosci. 21, 6018-6025.
18. Katada, S., Nakagawa, T., Kataoka, H. and Touhara, K. (2003). Odorant response assays for a heterologously expressed olfactory receptor. Biochem. Biophys. Res. Commun. 305, 964-969.
19. Kaupp, U. B., Solzin, J., Hildebrand, E., Brown, J. E., Helbig, A., Hagen, V., Beyermann, M., Pampaloni, F. and Weyand, I. (2003). The signal flow and motor response controling chemotaxis of sea urchin sperm. Nat. Cell Biol. 5, 109-117.
20. Kirkman-Brown, J. C., Sutton, K. A. and Florman, H. M. (2003). How to attract a sperm. Nat. Cell Biol. 5, 93-96.
21. Lindemann, C. B. and Goltz, J. S. (1988). Calcium regulation of flagellar curvature and swimming pattern in Triton X-100-extracted rat sperm. Cell Motil. Cytoskeleton 10, 420-431.
22. Mali, P., Kaipia, A., Kangasniemi, M., Toppari, J., Sandberg, M., Hecht, N. B. and Parvinen, M. (1989). Stage-specific expression of nucleoprotein mRNAs during rat and mouse spermiogenesis. Reprod. Fertil. Dev. 1, 369-382.
23. Malnic, B., Hirono, J., Sato, T. and Buck, L. B. (1999). Combinatorial receptor codes for odors. Cell 96, 713-723.
24. Mombaerts, P. (1999). Seven-transmembrane proteins as odorant and chemosensory receptors. Science 286, 707-711.
25. Noce, T., Okamoto-Ito, S. and Tsunekawa, N. (2001). Vasa homolog genes in mammalian germ cell development. Cell Struct. Funct. 26, 131-136.
26. Oliveira, R. G., Tomasi, L., Rovasio, R. A. and Giojalas, L. C. (1999). Increased velocity and induction of chemotactic response in mouse spermatozoa by follicular and oviductal fluids. J. Reprod. Fertil. 115, 23-27.
27. Parmentier, M., Libert, F., Schurmans, S., Schiffmann, S., Lefort, A., Eggerickx, D., Ledent, C., Mollereau, C., Gerard, C., Perret, J. et al. (1992). Expression of members of the putative olfactory receptor gene family in mammalian germ cells. Nature 355, 453-455.
28. Ralt, D., Manor, M., Cohen-Dayag, A., Tur-Kaspa, I., Ben-Shlomo, I., Makler, A., Yuli, I., Dor, J., Blumberg, S., Mashiach, S. et al. (1994). Chemotaxis and chemokinesis of human spermatozoa to follicular factors. Biol. Reprod. 50, 774-785.
29. Russell, L. D. (1990). Histological and Histopathological Evaluation of the Testis, pp. 119-161. Clearwater, FL: Cache River Press.
30. Spehr, M., Gisselmann, G., Poplawski, A., Riffell, J. A., Wetzel, C. H., Zimmer, R. K. and Hatt, H. (2003). Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science 299, 2054-2058.
31. Spehr, M., Schwane, K., Riffell, J. A., Barbour, J., Zimmer, R. K., Neuhaus, E. M. and Hatt, H. (2004). Particulate adenylate cyclase plays a key role in human sperm olfactory receptor-mediated chemotaxis. J. Biol. Chem. 279, 40194-40203.
32. Suarez, S. S. and Ho, H. C. (2003). Hyperactivated motility in sperm. Reprod. Domest. Anim. 38, 119-124.
33. Tatsura, H., Nagao, H., Tamada, A., Sasaki, S., Kohri, K. and Mori, K. (2001). Developing germ cells in mouse testis express pheromone receptors. FEBS Lett. 488, 139-144.
34. Touhara, K. (2001). Functional cloning and reconstitution of vertebrate odorant receptors. Life Sci. 68, 2199-2206.
35. Touhara, K. (2002). Odor discrimination by G protein-coupled olfactory receptors. Microsc. Res. Tech. 58, 135-141.
36. Touhara, K., Sengoku, S., Inaki, K., Tsuboi, A., Hirono, J., Sato, T., Sakano, H. and Haga, T. (1999). Functional identification and reconstitution of an odorant receptor in single olfactory neurons. Proc. Natl. Acad. Sci. USA 96, 4040-4045.
37. Toyoda, Y., Yokoyama, M. and Hoshi, T. (1971). Studies on the fertilization of ruouse eggs in vitro. I. In vitro fertilization of eggs by fresh epididymal sperm. Jpn. J. Anim. Reprod. 16, 147-151.
38. Vanderhaeghen, P., Schurmans, S., Vassart, G. and Parmentier, M. (1993). Olfactory receptors are displayed on dog mature sperm cells. J. Cell Biol. 123, 1441-1452.
39. Vanderhaeghen, P., Schurmans, S., Vassart, G. and Parmentier, M. (1997). Specific repertoire of olfactory receptor genes in the male germ cells of several mammalian species. Genomics 39 239-246.
40. Walensky, L. D., Roskams, A. J., Lefkowitz, R. J., Snyder, S. H. and Ronnett, G. V. (1995). Odorant receptors and desensitization proteins colocalize in mammalian sperm. Mol. Med. 1, 130-141.
41. Walensky, L. D., Ruat, M., Bakin, R. E., Blackshaw, S., Ronnett, G. V. and Snyder, S. H. (1998). Two novel odorant receptor families expressed in spermatids undergo 5′-splicing. J. Biol. Chem. 273, 9378-9387.
42. Ward, G. E., Brokaw, C. J., Garbers, A L. and Vacquier, V. D. (1985). Chemotaxis of Arbacia punctulata spermatozoa to resact, a peptide from the egg jelly layer. J. Cell Biol. 101 2324-2329.
43. 2+-binding protein (calmegin) specifically expressed during male meiotic germ cell development. J. Biol. Chem. 269 7744-7749.
44. Watanabe, D., Okabe, M., Hamajima, N., Morita, T., Nishina, Y. and Nishimune, Y. (1995). Characterization of the testis-specific gene 'calmegin' promoter sequence and its activity defined by transgenic mouse experiments. FEBS Lett. 368, 509-512.
45. 2+ into mouse sperm. J. Biol. Chem. 275, 21210-21217.
46. Weyand, I., Godde, M., Frings, S., Weiner, J., Muller, F., Altenhofen, W., Hatt, H. and Kaupp, U. B. (1994). Cloning and functional expression of a cyclic-nucleotide-gated channel from mammalian sperm. Nature 368, 859-863.
47. 2+ entry into sperm. J. Cell Biol. 142, 473-484.
48. Yoshida, M., Inaba, K. and Morisawa, M. (1993). Sperm chemotaxis during the process of fertilization in the ascidians Ciona savignyi and Ciona intestinalis. Dev. Biol. 157, 497-506.
49. Yoshida, M., Murata, M., Inaba, K. and Morisawa, M. (2002). A chemoattractant for ascidian spermatozoa is a sulfated steroid. Proc. Natl. Acad. Sci. USA 99, 14831-14836.
50. Zhang, X. and Firestein, S. (2002). The olfactory receptor gene superfamily of the mouse. Nat. Neurosci. 5, 124-133.
51. Zhao, H., Ivic, L., Otaki, J. M., Hashimoto, M., Mikoshiba, K. and Firestein, S. (1998). Functional expression of a mammalian odorant receptor. Science 279, 237-242.