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Science 28 March 2003:
Vol. 299. no. 5615, pp. 2054 - 2058
DOI: 10.1126/science.1080376

Reports

Identification of a Testicular Odorant Receptor Mediating Human Sperm Chemotaxis

Marc Spehr,1 Günter Gisselmann,1 Alexandra Poplawski,1 Jeffrey A. Riffell,2 Christian H. Wetzel,1 Richard K. Zimmer,23 Hanns Hatt1*

Although it has been known for some time that olfactory receptors (ORs) reside in spermatozoa, the function of these ORs is unknown. Here, we identified, cloned, and functionally expressed a previously undescribed human testicular OR, hOR17-4. With the use of ratiofluorometric imaging, Ca2+ signals were induced by a small subset of applied chemical stimuli, establishing the molecular receptive fields for the recombinantly expressed receptor in human embryonic kidney (HEK) 293 cells and the native receptor in human spermatozoa. Bourgeonal was a powerful agonist for both recombinant and native receptor types, as well as a strong chemoattractant in subsequent behavioral bioassays. In contrast, undecanal was a potent OR antagonist to bourgeonal and related compounds. Taken together, these results indicate that hOR17-4 functions in human sperm chemotaxis and may be a critical component of the fertilization process.

1 Department of Cell Physiology, Ruhr University Bochum, 150 University Street, D-44780 Bochum, Germany.
2 Department of Biology,
3 Neurosciences Program and Brain Research Institute, University of California, 621 Young Drive South, Los Angeles, CA 90095, USA.
*   To whom correspondence should be addressed. E-mail: hanns.hatt{at}ruhr-uni-bochum.de


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Dual Activities of Odorants on Olfactory and Nuclear Hormone Receptors.
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Molecular Tuning of Odorant Receptors and Its Implication for Odor Signal Processing.
J. Reisert and D. Restrepo (2009)
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
Endogenous signaling pathways and chemical communication between sperm and egg.
P. J. Krug, J. A. Riffell, and R. K. Zimmer (2009)
J. Exp. Biol. 212, 1092-1100
   Abstract »    Full Text »    PDF »
A Signature of Evolutionary Constraint on a Subset of Ectopically Expressed Olfactory Receptor Genes.
O. De la Cruz, R. Blekhman, X. Zhang, D. Nicolae, S. Firestein, and Y. Gilad (2009)
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   Abstract »    Full Text »    PDF »
Functional expression of the olfactory signaling system in the kidney.
J. L. Pluznick, D.-J. Zou, X. Zhang, Q. Yan, D. J. Rodriguez-Gil, C. Eisner, E. Wells, C. A. Greer, T. Wang, S. Firestein, et al. (2009)
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   Abstract »    Full Text »    PDF »
Progestin Signaling through an Olfactory G Protein and Membrane Progestin Receptor-{alpha} in Atlantic Croaker Sperm: Potential Role in Induction of Sperm Hypermotility.
C. Tubbs and P. Thomas (2009)
Endocrinology 150, 473-484
   Abstract »    Full Text »    PDF »
Detection of Olfactory Receptor Transcripts in Bird Testes.
S. S. Steiger, A. E. Fidler, and B. Kempenaers (2008)
J. Hered. 99, 624-628
   Abstract »    Full Text »    PDF »
Control of hyperactivation in sperm.
S. S. Suarez (2008)
Hum. Reprod. Update 14, 647-657
   Abstract »    Full Text »    PDF »
Efficient cell-free production of olfactory receptors: Detergent optimization, structure, and ligand binding analyses.
L. Kaiser, J. Graveland-Bikker, D. Steuerwald, M. Vanberghem, K. Herlihy, and S. Zhang (2008)
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   Abstract »    Full Text »    PDF »
Control of feeding behavior in C. elegans by human G protein-coupled receptors permits screening for agonist-expressing bacteria.
M. S. Teng, P. Shadbolt, A. G. Fraser, G. Jansen, and J. McCafferty (2008)
PNAS 105, 14826-14831
   Abstract »    Full Text »    PDF »
Relationships Between Molecular Structure and Perceived Odor Quality of Ligands for a Human Olfactory Receptor.
G. Sanz, T. Thomas-Danguin, E. H. Hamdani, C. Le Poupon, L. Briand, J.-C. Pernollet, E. Guichard, and A. Tromelin (2008)
Chem Senses 33, 639-653
   Abstract »    Full Text »    PDF »
Functional Analysis of a Subset of Canine Olfactory Receptor Genes.
N. Benbernou, S. Tacher, S. Robin, M. Rakotomanga, F. Senger, and F. Galibert (2007)
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   Abstract »    Full Text »    PDF »
Microarray Analyses of Newborn Mouse Ovaries Lacking Nobox.
Y. Choi, Y. Qin, M. F. Berger, D. J. Ballow, M. L. Bulyk, and A. Rajkovic (2007)
Biol Reprod 77, 312-319
   Abstract »    Full Text »    PDF »
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H. M. Florman, M. K. Jungnickel, and K. A. Sutton (2007)
PNAS 104, 11123-11124
   Full Text »    PDF »
Sex and the nose: human pheromonal responses.
M. F Bhutta (2007)
J R Soc Med 100, 268-274
   Abstract »    Full Text »    PDF »
Synergism of Accessory Factors in Functional Expression of Mammalian Odorant Receptors.
H. Zhuang and H. Matsunami (2007)
J. Biol. Chem. 282, 15284-15293
   Abstract »    Full Text »    PDF »
Sperm binding to the zona pellucida is not sufficient to induce acrosome exocytosis.
B. Baibakov, L. Gauthier, P. Talbot, T. L. Rankin, and J. Dean (2007)
Development 134, 933-943
   Abstract »    Full Text »    PDF »
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Y.-H. Huang, C.-C. Wei, Y.-H. Su, B.-T. Wu, Y.-Y. Ciou, C.-F. Tu, T. G. Cooper, C.-H. Yeung, S.-T. Chu, M.-T. Tsai, et al. (2006)
Endocrinology 147, 4792-4800
   Abstract »    Full Text »    PDF »
beta-Arrestin2-Mediated Internalization of Mammalian Odorant Receptors.
A. Mashukova, M. Spehr, H. Hatt, and E. M. Neuhaus (2006)
J. Neurosci. 26, 9902-9912
   Abstract »    Full Text »    PDF »
Receptors in Spermatozoa: Are They Real?.
R. K. Naz and R. Sellamuthu (2006)
J Androl 27, 627-636
   Full Text »    PDF »
Novel function of {beta}-arrestin2 in the nucleus of mature spermatozoa.
E. M. Neuhaus, A. Mashukova, J. Barbour, D. Wolters, and H. Hatt (2006)
J. Cell Sci. 119, 3047-3056
   Abstract »    Full Text »    PDF »
Ric-8B promotes functional expression of odorant receptors.
L. E. C. Von Dannecker, A. F. Mercadante, and B. Malnic (2006)
PNAS 103, 9310-9314
   Abstract »    Full Text »    PDF »
A Specific Heat Shock Protein Enhances the Expression of Mammalian Olfactory Receptor Proteins.
E. M. Neuhaus, A. Mashukova, W. Zhang, J. Barbour, and H. Hatt (2006)
Chem Senses 31, 445-452
   Abstract »    Full Text »    PDF »
Calcium signalling in human spermatozoa: a specialized 'toolkit' of channels, transporters and stores.
C. Jimenez-Gonzalez, F. Michelangeli, C.V. Harper, C.L.R. Barratt, and S.J. Publicover (2006)
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   Abstract »    Full Text »    PDF »
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S. M. Schuh, A. E. Carlson, G. S. McKnight, M. Conti, B. Hille, and D. F. Babcock (2006)
Biol Reprod 74, 492-500
   Abstract »    Full Text »    PDF »
Sperm transport in the female reproductive tract.
S.S. Suarez and A. A. Pacey (2006)
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   Abstract »    Full Text »    PDF »
Developmental expression patterns of testicular olfactory receptor genes during mouse spermatogenesis.
N. Fukuda and K. Touhara (2006)
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   Abstract »    Full Text »    PDF »
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M. Bajpai, S. E. Fiedler, Z. Huang, S. Vijayaraghavan, G. E. Olson, G. Livera, M. Conti, and D. W. Carr (2006)
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   Abstract »    Full Text »    PDF »
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C. V. Harper and S. J. Publicover (2005)
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   Abstract »    Full Text »    PDF »
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M. Kosinski, K. McDonald, J. Schwartz, I. Yamamoto, and D. Greenstein (2005)
Development 132, 3357-3369
   Abstract »    Full Text »    PDF »
Real-time analysis of the role of Ca2+ in flagellar movement and motility in single sea urchin sperm.
C. D. Wood, T. Nishigaki, T. Furuta, S. A. Baba, and A. Darszon (2005)
J. Cell Biol. 169, 725-731
   Abstract »    Full Text »    PDF »
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G. Livera, F. Xie, M. A. Garcia, B. Jaiswal, J. Chen, E. Law, D. R. Storm, and M. Conti (2005)
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   Abstract »    Full Text »    PDF »
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E. Shirokova, K. Schmiedeberg, P. Bedner, H. Niessen, K. Willecke, J.-D. Raguse, W. Meyerhof, and D. Krautwurst (2005)
J. Biol. Chem. 280, 11807-11815
   Abstract »    Full Text »    PDF »
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F. Sun, A. Bahat, A. Gakamsky, E. Girsh, N. Katz, L. C. Giojalas, I. Tur-Kaspa, and M. Eisenbach (2005)
Hum. Reprod. 20, 761-767
   Abstract »    Full Text »    PDF »
Identification of a nematode chemosensory gene family.
N. Chen, S. Pai, Z. Zhao, A. Mah, R. Newbury, R. C. Johnsen, Z. Altun, D. G. Moerman, D. L. Baillie, and L. D. Stein (2005)
PNAS 102, 146-151
   Abstract »    Full Text »    PDF »
Comparison of Odorant Specificity of Two Human Olfactory Receptors from Different Phylogenetic Classes and Evidence for Antagonism.
G. Sanz, C. Schlegel, J.-C. Pernollet, and L. Briand (2005)
Chem Senses 30, 69-80
   Abstract »    Full Text »    PDF »
Functional characterization of a mouse testicular olfactory receptor and its role in chemosensing and in regulation of sperm motility.
N. Fukuda, K. Yomogida, M. Okabe, and K. Touhara (2004)
J. Cell Sci. 117, 5835-5845
   Abstract »    Full Text »    PDF »
An Odorant Derivative as an Antagonist for an Olfactory Receptor.
Y. Oka, A. Nakamura, H. Watanabe, and K. Touhara (2004)
Chem Senses 29, 815-822
   Abstract »    Full Text »    PDF »
Stimulation of Human Spermatozoa with Progesterone Gradients to Simulate Approach to the Oocyte: INDUCTION OF [Ca2+]i OSCILLATIONS AND CYCLICAL TRANSITIONS IN FLAGELLAR BEATING.
C. V. Harper, C. L. R. Barratt, and S. J. Publicover (2004)
J. Biol. Chem. 279, 46315-46325
   Abstract »    Full Text »    PDF »
High-throughput microarray detection of olfactory receptor gene expression in the mouse.
X. Zhang, M. Rogers, H. Tian, X. Zhang, D.-J. Zou, J. Liu, M. Ma, G. M. Shepherd, and S. J. Firestein (2004)
PNAS 101, 14168-14173
   Abstract »    Full Text »    PDF »
Particulate Adenylate Cyclase Plays a Key Role in Human Sperm Olfactory Receptor-mediated Chemotaxis.
M. Spehr, K. Schwane, J. A. Riffell, J. Barbour, R. K. Zimmer, E. M. Neuhaus, and H. Hatt (2004)
J. Biol. Chem. 279, 40194-40203
   Abstract »    Full Text »    PDF »
Towards Understanding the Molecular Mechanism of Sperm Chemotaxis.
M. Eisenbach (2004)
J. Gen. Physiol. 124, 105-108
   Full Text »    PDF »
Olfactory Receptor Neuron Profiling using Sandalwood Odorants.
S. Bieri, K. Monastyrskaia, and B. Schilling (2004)
Chem Senses 29, 483-487
   Abstract »    Full Text »    PDF »
Control of Male Gametophyte Development.
S. McCormick (2004)
PLANT CELL 16, S142-S153
   Full Text »    PDF »
Paracrine regulation of mammalian oocyte maturation and male germ cell survival.
K. Kawamura, J. Kumagai, S. Sudo, S.-Y. Chun, M. Pisarska, H. Morita, J. Toppari, P. Fu, J. D. Wade, R. A. D. Bathgate, et al. (2004)
PNAS 101, 7323-7328
   Abstract »    Full Text »    PDF »
Evolution and Comparative Genomics of Odorant- and Pheromone-Associated Genes in Rodents.
R. D. Emes, S. A. Beatson, C. P. Ponting, and L. Goodstadt (2004)
Genome Res. 14, 591-602
   Abstract »    Full Text »    PDF »
A pharmacological profile of the aldehyde receptor repertoire in rat olfactory epithelium.
R. C. Araneda, Z. Peterlin, X. Zhang, A. Chesler, and S. Firestein (2004)
J. Physiol. 555, 743-756
   Abstract »    Full Text »    PDF »
The human olfactory receptor gene family.
B. Malnic, P. A. Godfrey, and L. B. Buck (2004)
PNAS 101, 2584-2589
   Abstract »    Full Text »    PDF »
The mouse olfactory receptor gene family.
P. A. Godfrey, B. Malnic, and L. B. Buck (2004)
PNAS 101, 2156-2161
   Abstract »    Full Text »    PDF »
Expression of fractalkine in the Fallopian tube and of CX3CR1 in sperm.
Q. Zhang, K. Shimoya, K. Temma, T. Kimura, T. Tsujie, M. Shioji, K. Wasada, O. Fukui, S. Hayashi, T. Kanagawa, et al. (2004)
Hum. Reprod. 19, 409-414
   Abstract »    Full Text »    PDF »
First messenger regulation of capacitation via G protein-coupled mechanisms: a tale of serendipity and discovery.
L. R. Fraser, S. A. Adeoya-Osiguwa, and R. W. Baxendale (2003)
Mol. Hum. Reprod. 9, 739-748
   Abstract »    Full Text »    PDF »
Understanding the chemistry of chemical communication: Are we there yet?.
J. Meinwald (2003)
PNAS 100, 14514-14516
   Full Text »
Evolution of olfactory receptor genes in the human genome.
Y. Niimura and M. Nei (2003)
PNAS 100, 12235-12240
   Abstract »    Full Text »    PDF »
SNIFFING SPERM.
H. Merzendorfer (2003)
J. Exp. Biol. 206, 2528
   Full Text »    PDF »



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