Human sperm thermotaxis is mediated by phospholipase C and inositol trisphosphate receptor Ca2+ channel

Biology of Reproduction

Volumn 82, Issue 3, 2010, Pages 606-616

  Bahat, Anat ^a   Eisenbach, Michael ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Sperm chemotaxis motility and transport; Sperm thermotaxis

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 2 AMINOETHOXYDIPHENYLBORANE; CALCIUM; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; PHOSPHOLIPASE C; POTASSIUM CHANNEL; VOLTAGE GATED CALCIUM CHANNEL; 1,2 BIS(2 AMINOPHENOXY)ETHANE N,N,N',N' TETRAACETIC ACID ACETOXYMETHYL ESTER; 1,2-BIS(2-AMINOPHENOXY)ETHANE N,N,N',N'-TETRAACETIC ACID ACETOXYMETHYL ESTER; CALCIMYCIN; CALCIUM CHANNEL; CHELATING AGENT; DRUG DERIVATIVE; EGTAZIC ACID; IONOPHORE;

ACROSOME; ARTICLE; CALCIUM CELL LEVEL; CHEMOTAXIS; HUMAN; PRIORITY JOURNAL; SEMEN ANALYSIS; SPERMATOZOON MOTILITY; THERMOREGULATION; BIOLOGICAL MODEL; CALCIUM SIGNALING; CELL MOTION; CELL SEPARATION; CYTOLOGY; DRUG EFFECT; GENETIC PROCEDURES; INSTRUMENTATION; MALE; METABOLISM; METHODOLOGY; PHYSIOLOGY; SPERMATOZOON; SPERMATOZOON CAPACITATION; TEMPERATURE;

ORYCTOLAGUS CUNICULUS; SUIDAE;

BIOSENSING TECHNIQUES; CALCIMYCIN; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL MOVEMENT; CELL SEPARATION; CHELATING AGENTS; EGTAZIC ACID; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; IONOPHORES; MALE; MODELS, BIOLOGICAL; SEMEN ANALYSIS; SPERM CAPACITATION; SPERMATOZOA; TEMPERATURE; TYPE C PHOSPHOLIPASES;

EID: 77953108762     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.109.080127     Document Type: Article

References (99)

1. Eisenbach M, Giojalas LC. Sperm guidance in mammals - an unpaved road to the egg. Nat Rev Mol Cell Biol 2006; 7:276-285.
2. Miller RL. Sperm chemo-orientation in the metazoa. In: Metz CB, Monroy A (eds.), Biology of Fertilization, vol. 2. New York: Academic Press; 1985:275-337.
3. Cosson MP. Sperm chemotaxis. In: Gagnon C (ed.), Controls of Sperm Motility: Biological and Clinical Aspects. Boca Raton: CRC Press; 1990:103-135.
4. Hildebrand E, Kaupp UB. Sperm chemotaxis: a primer. Ann N Y Acad Sci 2005; 1061:221-225.
5. Bahat A, Tur-Kaspa I, Gakamsky A, Giojalas LC, Breitbart H, Eisenbach M. Thermotaxis of mammalian sperm cells: A potential navigation mechanism in the female genital tract. Nat Med 2003; 9:149-150. (Pubitemid 36227702)
6. David A, Vilensky A, Nathan H. Temperature changes in the different parts of the rabbit's oviduct. Int J Gynaecol Obstet 1972; 10:52-56.
7. Hunter RHF, Nichol R. A preovulatory temperature gradient between the isthmus and the ampulla of pig oviducts during the phase of sperm storage. J Reprod Fertil 1986; 77:599-606. (Pubitemid 16075417)
8. Bahat A, Eisenbach M, Tur-Kaspa I. Periovulatory increase in temperature difference within the rabbit oviduct. Hum. Reprod 2005; 20:2118-2121. (Pubitemid 41418493)
9. Bahat A, Eisenbach M. Sperm thermotaxis. Mol Cell Endocrinol 2006; 252:115-119.
10. Fabro G, Rovasio RA, Civalero S, Frenkel A, Caplan SR, Eisenbach M, Giojalas LC. Chemotaxis of capacitated rabbit spermatozoa to follicular fluid revealed by a novel directionality-based assay. Biol Reprod 2002; 67:1565-1571. (Pubitemid 35204933)
11. Cohen-Dayag A, Ralt D, Tur-Kaspa I, Manor M, Makler A, Dor J, Mashiach S, Eisenbach M. Sequential acquisition of chemotactic responsiveness by human spermatozoa. Biol Reprod 1994; 50:786-790. (Pubitemid 24085218)
12. Cohen-Dayag A, Tur-Kaspa I, Dor J, Mashiach S, Eisenbach M. Sperm capacitation in humans is transient and correlates with chemotactic responsiveness to follicular factors. Proc Natl Acad Sci U S A 1995; 92:11039-11043.
13. Teves ME, Barbano F, Guidobaldi HA, Sanchez R, Miska W, Giojalas LC. Progesterone at the picomolar range is a chemoattractant for mammalian spermatozoa. Fertil Steril 2006; 86:745-749. (Pubitemid 44306995)
14. Oren-Benaroya R, Orvieto R, Gakamsky A, Pinchasov M, Eisenbach M. The sperm chemoattractant secreted from human cumulus cells is progesterone. Hum Reprod 2008; 23:2339-2345.
15. Guidobaldi HA, Teves ME, Unates DR, Anastasia A, Giojalas LC. Progesterone from the cumulus cells is the sperm chemoattractant secreted by the rabbit oocyte cumulus complex. PLoS ONE 2008; 3:e3040.
16. Sun F, Bahat A, Gakamsky A, Girsh E, Katz N, Giojalas LC, Tur-Kaspa I, Eisenbach M. Human sperm chemotaxis: both the oocyte and its surrounding cumulus cells secrete sperm chemoattractants. Hum Reprod 2005; 20:761-767. (Pubitemid 40425506)
17. Imae Y. Molecular mechanism of thermosensing in bacteria. In: Eisenbach M, Balaban M (eds.), Sensing and Response in Microorganisms. Amsterdam: Elsevier; 1985:73-81.
18. Nara T, Kawagishi I, Nishiyama S, Homma M, Imae Y. Modulation of the thermosensing profile of the Escherichia coli aspartate receptor tar by covalent modification of its methyl-accepting sites. J Biol Chem 1996; 271:17932-17936. (Pubitemid 26250774)
19. Nara T, Lee L, Imae Y. Thermosensing ability of Trg and Tap chemoreceptors in Escherichia coli. J Bacteriol 1991; 173:1120-1124.
20. Mori I, Ohshima Y. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 1995; 376:344-348.
21. Samuel ADT, Silva RA, Murthy VN. Synaptic activity of the AFD neuron in Caenorhabditis elegans correlates with thermotactic memory. J Neurosci 2003; 23:373-376.
22. Hedgecock EM, Russell RL. Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A 1975; 72:4061-4065.
23. Mori I. Genetics of chemotaxis and thermotaxis in the nematode Caenorhabditis elegans. Annu Rev Genet 1999; 33:399-422.
24. Montell C. The TRP superfamily of cation channels. Sci STKE 2005; 2005:1-24.
25. Patapoutian A, Peier AM, Story GM, Viswanath V. ThermoTRP channels and beyond: mechanisms of temperature sensation. Nat Rev Neurosci 2003; 4:529-539. (Pubitemid 37271364)
26. Tominaga M, Caterina MJ. Thermosensation and pain. J Neurobiol 2004; 61:3-12.
27. Mizushima T, Obata K, Katsura H, Yamanaka H, Kobayashi K, Dai Y, Fukuoka T, Tokunaga A, Mashimo T, Noguchi K. Noxious cold stimulation induces mitogen-activated protein kinase activation in transient receptor potential (TRP) channels TRPA1- and TRPM8-containing small sensory neurons. Neuroscience 2006; 140:1337-1348. (Pubitemid 43928288)
28. Maccarrone M, Barboni B, Paradisi A, Bernabo N, Gasperi V, Pistilli MG, Fezza F, Lucidi P, Mattioli M. Characterization of the endocannabinoid system in boar spermatozoa and implications for sperm capacitation and acrosome reaction. J Cell Sci 2005; 118:4393-4404. (Pubitemid 41556338)
29. Liedtke W, Choe Y, Marti-Renom MA, Bell AM, Denis CS, Sali A, Hudspeth AJ, Friedman JM, Heller S. Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 2000; 103:525-535.
30. De Blas GA, Darszon A, Ocampo AY, Serrano CJ, Castellano LE, Hernandez-Gonzalez EO, Chirinos M, Larrea F, Beltran C, Trevino CL. TRPM8, a versatile channel in human sperm. PLoS One 2009; 4:e6095.
31. 2+ into mouse sperm triggered by egg ZP3. Nat Cell Biol 2001; 3:499-502.
32. Trevino CL, Serrano CJ, Beltran C, Felix R, Darszon A. Identification of mouse trp homologs and lipid rafts from spermatogenic cells and sperm. FEBS Lett 2001; 509:119-125. (Pubitemid 33153093)
33. Castellano LE, Treviño CL, Rodríguez D, Serrano CJ, Pacheco J, Tsutsumi V, Felix R, Darszon A. Transient receptor potential (TRPC) channels in human sperm: expression, cellular localization and involvement in the regulation of flagellar motility. FEBS Lett 2003; 541:69-74. (Pubitemid 36428919)
34. 2+ channels were activated by heating and cooling. J Membr Biol 1999; 168:283-287.
35. Zocchi E, Carpaneto A, Cerrano C, Bavestrello G, Giovine M, Bruzzone S, Guida L, Franco L, Usai C. The temperature-signaling cascade in sponges involves a heat-gated cation channel, abscisic acid, and cyclic ADP-ribose. Proc Natl Acad Sci U S A 2001; 98:14859-14864. (Pubitemid 34013935)
36. + channel. EMBO J 2000; 19:2483-2491.
37. 2+ entry and control of flagellar function in sperm. Proc Natl Acad Sci U S A 2003; 100:14864-14868.
38. Suarez S, Ho HC. Hyperactivated motility in sperm. Reprod Domest Anim 2003; 38:119-124.
39. 2+ signalling in the control of motility and guidance in mammalian sperm. Front Biosci 2008; 13:5623-5637.
40. Jaiswal BS, Eisenbach M. Capacitation. In: Hardy DM (ed.), Fertilization. San Diego: Academic Press; 2002:57-117.
41. 2+ signaling and acrosome reaction in human spermatozoa. J Androl 2002; 23:306-315.
42. Eisenbach M. Sperm chemotaxis. Rev Reprod 1999; 4:56-66.
43. Spehr M, Gisselmann G, Poplawski A, Riffell JA, Wetzel CH, Zimmer RK, Hatt H. Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science 2003; 299:2054-2058. (Pubitemid 36383730)
44. Kaupp UB, Solzin J, Hildebrand E, Brown JE, Helbig A, Hagen V, Beyermann M, Pampaloni F, Weyand I. The signal flow and motor response controlling chemotaxis of sea urchin sperm. Nat Cell Biol 2003; 5:109-117. (Pubitemid 36204193)
45. Böhmer M, Van Q, Weyand I, Hagen V, Beyermann M, Matsumoto M, Hoshi M, Hildebrand E, Kaupp UB. Ca2+ spikes in the flagellum control chemotactic behavior of sperm. EMBO J 2005; 24:2741-2752. (Pubitemid 41170024)
46. Cook SP, Brokaw CJ, Muller CH, Babcock DF. Sperm chemotaxis: egg peptides control cytosolic calcium to regulate flagellar responses. Dev Biol 1994; 165:10-19.
47. Kaupp UB, Hildebrand E, Weyand I. Sperm chemotaxis in marine invertebrates-molecules and mechanism. J Cell Physiol 2006; 208:487-494. (Pubitemid 44141873)
48. Dohrmann U, Fisher PR, Bruderlein M, Williams KL. Transitions in Dictyostelium discoideum behaviour: influence of calcium and fluoride on slug phototaxis and thermotaxis. J Cell Sci 1984; 65:111-121.
49. Norris V, Grant S, Freestone P, Canvin J, Sheikh FN, Toth I, Trinei M, Modha K, Norman RI. Calcium signalling in bacteria. J Bacteriol 1996; 178:3677-3682.
50. Zhang Y, Chou JH, Bradley J, Bargmann CI, Zinn K. The Caenorhabditis elegans seven-transmembrane protein ODR-10 functions as an odorant receptor in mammalian cells. Proc Natl Acad Sci U S A 1997; 94:12162-12167. (Pubitemid 27467860)
51. Jimenez-Gonzalez C, Michelangeli F, Harper CV, Barratt CL, Publicover SJ. Calcium signalling in human spermatozoa: a specialized 'toolkit' of channels, transporters and stores. Hum Reprod Update 2006; 12:253-267.
52. Biggers JD, Whitten WK, Whittingham DG. The culture of mouse embryos in vitro. In: Daniel JD (ed.), Methods in Mammalian Embryology. San Francisco: Freeman; 1971:86-116.
53. World Health Organization. WHO Laboratory Manual for the Examination of Human Semen and Semen-Cervical Mucus Interaction. New York: Cambridge University Press; 1993.
54. Davis RO, Siemers RJ. Derivation and reliability of kinematic measures of sperm motion. Reprod Fertil Dev 1995; 7:857-869.
55. Mortimer ST. A critical review of the physiological importance and analysis of sperm movement in mammals. Hum Reprod Update 1997; 3:403-439.
56. Mortimer D, Fraser L. Consensus workshop on advanced diagnostic andrology techniques. Hum Reprod 1996; 11:1463-1479.
57. 2+ ions in chick sensory neurones. J Physiol 1997; 504(pt 1):1-15.
58. Gonzalez-Martinez MT. Induction of a sodium-dependent depolarization by external calcium removal in human sperm. J Biol Chem 2003; 278:36304-36310.
59. Minke B, Cook B. TRP channel proteins and signal transduction. Physiol Rev 2002; 82:429-472. (Pubitemid 34654458)
60. Huang CL. The transient receptor potential superfamily of ion channels. J Am Soc Nephrol 2004; 15:1690-1699. (Pubitemid 38822047)
61. De Blas G, Michaut M, Trevino CL, Tomes CN, Yunes R, Darszon A, Mayorga LS. The intraacrosomal calcium pool plays a direct role in acrosomal exocytosis. J Biol Chem 2002; 277:49326-49331. (Pubitemid 36014363)
62. Guatteo E, Chung KK, Bowala TK, Bernardi G, Mercuri NB, Lipski J. Temperature sensitivity of dopaminergic neurons of the substantia nigra pars compacta: involvement of transient receptor potential channels. J Neurophysiol 2005; 94:3069-3080. (Pubitemid 41504750)
63. Rosenzweig M, Brennan KM, Tayler TD, Phelps PO, Patapoutian A, Garrity PA. The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. Genes Dev 2005; 19:419-424. (Pubitemid 40256272)
64. Van Breemen C. Blockade of membrane calcium fluxes by lanthanum in relation to vascular smooth muscle contractility. Arch Int Physiol Biochim 1969; 77:710-716.
65. 3+ in cultured cortical neurones. J Neurochem 2004; 91:471-483.
66. Schultz JE, Schonefeld U, Klumpp S. Calcium/calmodulin-regulated guanylate cyclase and calcium-permeability in the ciliary membrane from Tetrahymena. Eur J Biochem 1983; 137:89-94.
67. Mills JS, Johnson JD. Metal ions as allosteric regulators of calmodulin. J Biol Chem 1985; 260:15100-15105.
68. Cervetto L, McNaughton PA. The effects of phosphodiesterase inhibitors and lanthanum ions on the light-sensitive current of toad retinal rods. J Physiol 1986; 370:91-109. (Pubitemid 16185821)
69. Reichling DB, MacDermott AB. Lanthanum actions on excitatory amino acid-gated currents and voltage-gated calcium currents in rat dorsal horn neurons. J Physiol 1991; 441:199-218.
70. Powis DA, Clark CL, O'Brien KJ. Lanthanum can be transported by the sodium-calcium exchange pathway and directly triggers catecholamine release from bovine chromaffin cells. Cell Calcium 1994; 16:377-390.
71. Clapham DE, Runnels LW, Strubing C. The TRP ion channel family. Nat Rev Neurosci 2001; 2:387-396.
72. Li Y, Jia YC, Cui K, Li N, Zheng ZY, Wang YZ, Yuan XB. Essential role of TRPC channels in the guidance of nerve growth cones by brain-derived neurotrophic factor. Nature 2005; 434:894-898. (Pubitemid 40559001)
73. Zufall F. The TRPC2 ion channel and pheromone sensing in the accessory olfactory system. Naunyn Schmiedebergs Arch Pharmacol 2005; 371:245-250.
74. Kiselyov K, Kim JY, Zeng W, Muallem S. Protein-protein interaction and functionTRPC channels. Pflugers Arch 2005; 451:116-124.
75. Blackmore PF, Eisoldt S. The neoglycoprotein mannose-bovine serum albumin, but not progesterone, activates T-type calcium channels in human spermatozoa. Mol Hum Reprod 1999; 5:498-506.
76. Kirkman-Brown JC, Barratt CL, Publicover SJ. Nifedipine reveals the existence of two discrete components of the progesterone-induced [Ca2+]i transient in human spermatozoa. Dev Biol 2003; 259:71-82.
77. Mathie A, Wooltorton JR, Watkins CS. Voltage-activated potassium channels in mammalian neurons and their block by novel pharmacological agents. Gen Pharmacol 1998; 30:13-24.
78. Yeung CH, Cooper TG. Effects of the ion-channel blocker quinine on human sperm volume, kinematics and mucus penetration, and the involvement of potassium channels. Mol Hum Reprod 2001; 7:819-828.
79. Hofmann SL, Majerus PW. Modulation of phosphatidylinositol-specific phospholipase C activity by phospholipid interactions, diglycerides, and calcium ions. J Biol Chem 1982; 257:14359-14364.
80. Bootman MD, Collins TJ, Mackenzie L, Roderick HL, Berridge MJ, Peppiatt CM. 2-aminoethoxydiphenyl borate (2-APB) is a reliable blocker of store-operated Ca2+ entry but an inconsistent inhibitor of InsP3-induced Ca2+ release. FASEB J 2002; 16:1145-1150. (Pubitemid 34815402)
81. Dutta D. Mechanism of store-operated calcium entry. J Biosci 2000; 25:397-404.
82. Broad LM, Cannon TR, Taylor CW. A non-capacitative pathway activated by arachidonic acid is the major Ca2+ entry mechanism in rat A7r5 smooth muscle cells stimulated with low concentrations of vasopressin. J Physiol 1999; 517(pt 1):121-134.
83. Ralt D, Manor M, Cohen-Dayag A, Tur-Kaspa I, Makler A, Yuli I, Dor J, Blumberg S, Mashiach S, Eisenbach M. Chemotaxis and chemokinesis of human spermatozoa to follicular factors. Biol Reprod 1994; 50:774-785.
84. Perez JF, Ruiz MC, Chemello ME, Michelangeli F. Characterization of a membrane calcium pathway induced by rotavirus infection in cultured cells. J Virol 1999; 73:2481-2490.
85. 2+ chelators. J Cereb Blood Flow Metab 1994; 14:911-923.
86. 2+ influx and the acrosome reaction in human sperm. Cell Signal 1993; 5:531-538.
87. Dragileva E, Rubinstein S, Breitbart H. Intracellular Ca(2+)-Mg(2+)-ATPase regulates calcium influx and acrosomal exocytosis in bull and ram spermatozoa. Biol Reprod 1999; 61:1226-1234.
88. 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.
89. Malchow D, Mutzel R, Schlatterer C. On the role of calcium during chemotactic signalling and differentiation of the cellular slime mould Dictyostelium discoideum. Int J Dev Biol 1996; 40:135-139. (Pubitemid 26151255)
90. Anderson R, Steel HC, Tintinger GR. Inositol 1,4,5-triphosphate-mediated shuttling between intracellular stores and the cytosol contributes to the sustained elevation in cytosolic calcium in FMLP-activated human neutrophils. Biochem Pharmacol 2005; 69:1567-1575.
91. Yoshida M, Ishikawa M, Izumi H, De Santis R, Morisawa M. Store-operated calcium channel regulates the chemotactic behavior of ascidian sperm. Proc Natl Acad Sci U S A 2003; 100:149-154. (Pubitemid 36078043)
92. O'Toole CM, Arnoult C, Darszon A, Steinhardt RA, Florman HM. Ca2+ entry through store-operated channels in mouse sperm is initiated by egg ZP3 and drives the acrosome reaction. Mol Biol Cell 2000; 11:1571-1584. (Pubitemid 30307897)
93. Howell KP, Skipwith A, Galione A, Eckberg WR. Phospholipase C-dependent Ca2+ release by worm and mammal sperm factors. Biochem Biophys Res Commun 2003; 307:47-51. (Pubitemid 36808534)
94. Spehr M, Leinders-Zufall T. One neuron-multiple receptors: increased complexity in olfactory coding? Sci STKE 2005; 2005:pe25.
95. Kernan MJ. Mechanotransduction and auditory transduction in Drosophila. Pflugers Arch 2007: 454:703-720.
96. Nikolich-Zugich J, Slifka MK, Messaoudi I. The many important facets of T-cell repertoire diversity. Nat Rev Immunol 2004; 4:123-132. (Pubitemid 38209206)
97. Varla-Leftherioti M. The significance of the women's repertoire of natural killer cell receptors in the maintenance of pregnancy. Chem Immunol Allergy 2005; 89:84-95.
98. Brokaw CJ, Josslin R, Bobrow L. Calcium ion regulation of flagellar beat symmetry in reactivated sea urchin spermatozoa. Biochem Biophys Res Commun 1974; 58:795-800.
99. Lindemann CB, Goltz JS. Calcium regulation of flagellar curvature and swimming pattern in Triton X-100-extracted rat sperm. Cell Motil Cytoskeleton 1988; 10:420-431.