Ca2+-stores in sperm: Their identities and functions

Reproduction

Volumn 138, Issue 3, 2009, Pages 425-437

  Costello, Sarah ^a,b   Michelangeli, Francesco ^a   Nash, Katherine ^a,b   Lefievre, Linda ^a,b   Morris, Jennifer ^a,b   Machado Oliveira, Gisela ^c   Barratt, Christopher ^d   Kirkman Brown, Jackson ^a,b   Publicover, Stephen ^a,b  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b BIRMINGHAM WOMEN S HOSPITAL   (United Kingdom)

^c INSTITUTO PIAGET   (Portugal)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CALCIUM CHELATING AGENT; CALCIUM ION; CATION TRANSPORT PROTEIN; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; RYANODINE RECEPTOR; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; TRANSIENT RECEPTOR POTENTIAL CHANNEL; CALCIUM;

ACROSOME; ACROSOME REACTION; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; CELL ACTIVITY; CELL FUNCTION; CELL NUCLEUS MEMBRANE; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HUMAN; LYSOSOME; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SOMATIC CELL; SPERM; SPERMATOZOON MIDPIECE; ANIMAL; BIOLOGICAL MODEL; CALCIUM SIGNALING; CELL ORGANELLE; CYTOLOGY; MALE; METABOLISM; PHYSIOLOGY; SPERMATOZOON;

MAMMALIA;

ANIMALS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; HUMANS; MALE; MODELS, BIOLOGICAL; ORGANELLES; SPERMATOZOA;

EID: 70449348498     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-09-0134     Document Type: Review

References (99)

1. Abramowitz J & Birnbaumer L 2009 Physiology and pathphysiology of canonical transient receptor potential channels. FASEB Journal 23 297-328.
2. 2+ in sea urchin sperm. Biochimica et Biophysica Acta 1787 15-24.
3. Arnoult C, Kazam IG, Visconti PE, Kopf GS, Villaz M & Florman HM 1999 Control of the low voltage-activated calcium channel of mouse sperm by egg ZP3 and by membrane hyperpolarization during capacitation. PNAS 96 6757-6762. (Pubitemid 29274956)
4. Babcock DF, First NL & Lardy HA 1976 Action of ionophore A23187 at the cellular level. Separation of effects at the plasma and mitochondrial membranes. Journal of Biological Chemistry 251 3881-3886.
5. Baldi E, Luconi M, Bonaccorsi L, Maggi M, Francavilla S, Gabriele A, Properzi G & Forti G 1999 Nongenomic progesterone receptor on human spermatozoa: biochemical aspects and clinical implications. Steroids 64 143-148. (Pubitemid 29168598)
6. Bedu-Addo K, Lefievre L, Moseley FL, Barratt CL & Publicover SJ 2005 Bicarbonate and bovine serum albumin reversibly 'switch' capacitation-induced events in human spermatozoa. Molecular Human Reproduction 11 683-691.
7. Bernardi P 1999 Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiological Reviews 79 1127-1155. (Pubitemid 29473313)
8. Berridge MJ 1993 Inositol trisphosphate and calcium signalling. Nature 361 315-325.
9. Berridge MJ 2002 The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32 235-249. (Pubitemid 36175747)
10. Berridge MJ, Bootman MD & Lipp P 1998 Calcium - a life and death signal. Nature 395 645-648.
11. Bianchi K, Rimessi A, Prandini A, Szabadkai G & Rizzuto R 2004 Calcium and mitochondria: mechanisms and functions of a troubled relationship. Biochimica et Biophysica Acta 1742 119-131. (Pubitemid 39601772)
12. Birnbaumer L, Zhu X, Jiang M, Boulay G, Peyton M, Vannier B, Brown D, Platano D, Sadeghi H, Stefani E et al. 1996 On the molecular basis and regulation of cellular capacitative calcium entry: roles for Trp proteins. PNAS 93 15195-15202. (Pubitemid 27009576)
13. Blackmore PF 1993 Thapsigargin elevates and potentiates the ability of progesterone to increase intracellular free calcium in human sperm: possible role of perinuclear calcium. Cell Calcium 14 53-60. (Pubitemid 23048723)
14. De Blas G, Michaut M, Trevino CL, Tomes CN, Yunes R, Darszon A & Mayorga LS 2002 The intraacrosomal calcium pool plays a direct role in acrosomal exocytosis. Journal of Biological Chemistry 277 49326-49331. (Pubitemid 36014363)
15. Bootman MD, Collins TJ, Peppiatt CM, Prothero LS, MacKenzie L, De Smet P, Travers M, Tovey SC, Seo JT, Berridge MJ et al. 2001 Calcium signaling - an overview. Seminars in Cell & Developmental Biology 12 3-10.
16. Breitbart H 2002 Intracellular calcium regulation in sperm capacitation and acrosomal reaction. Molecular and Cellular Endocrinology 187 139-144. (Pubitemid 34436942)
17. Breitbart H & Spungin B 1997 The biochemistry of the acrosome reaction. Molecular Human Reproduction 3 195-202.
18. Buffone MG, Foster JA & Gerton GL 2008 The role of the acrosomal matrix in fertilization. International Journal of Developmental Biology 52 511-522.
19. Calcraft PJ, Ruas M, Pan Z, Cheng X, Arredouani A, Hao X, Tang J, Rietdorf K, Teboul L, Chuang KT et al. 2009 NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459 596-600.
20. Castellano LE, Treviño CL, Rodríguez D, Serrano CJ, Pacheco J, Tsutsumi V, Felix R & Darszon A 2003 Transient receptor potential (TRPC) channels in human sperm: expression, cellular localization and involvement in the regulation of flagellar motility. FEBS Letters 541 69-74. (Pubitemid 36428919)
21. Chandler JA & Battersby S 1976 X-ray microanalysis of zinc and calcium in ultrathin sections of human sperm cells using the pyroantimonate technique. Journal of Histochemistry and Cytochemistry 24 740-748.
22. 2+ from reserve granules, lysosome-related organelles, in sea urchin eggs. Cell 111 703-708.
23. Darszon A, Labarca P, Nishigaki T & Espinosa F 1999 Ion channels in sperm physiology. Physiological Reviews 79 481-510.
24. Dong Z, Saikumar P, Weinberg JM & Venkatachalam MA 2006 Calcium in cell injury and death. Annual Review of Pathology 1 405-434.
25. 2+-ATPase regulates calcium influx and acrosomal exocytosis in bull and ran spermatozoa. Biology of Reproduction 61 1226-1234.
26. Echevarria D, Vieira C, Gimeno L & Martinez S 2003 Neuroepithelial secondary organizers and cell fate specification in the developing brain. Brain Research Reviews 43 179-191. (Pubitemid 37315652)
27. Espino J, Mediero M, Lozano GM, Bejarano I, Ortiz A, García JF, Pariente JA & Rodríguez AB 2009 Reduced levels of intracellular calcium releasing in spermatozoa from asthenozoospermic patients. Reproductive Biology and Endocrinology 7 11.
28. 2+- conducting channels in the plasma membrane of mammalian sperm. Reproduction 129 251-262.
29. Florman HM, Jungnickel MK & Sutton KA 2008 Regulating the acrosome reaction. International Journal of Developmental Biology 52 503-510.
30. Fukami K, Nakao K, Inoue T, Kataoka Y, Kurokawa M, Fissore RA, Nakamura K, Katsuki M, Mikoshiba K, Yoshida N et al. 2001 Requirement of phospholipase Cdelta4 for the zona pellucida-induced acrosome reaction. Science 292 920-923. (Pubitemid 32422487)
31. 2+ mobilization essential for acrosome reaction in sperm. Journal of Cell Biology 161 79-88.
32. 2+ from a thapsigargin-sensitive store in the nuclear envelope by activating ryanodine receptors. Journal of Cell Biology 163 271-282.
33. 2+ is required for the acrosome reaction in sea urchin sperm. Developmental Biology 236 220-229.
34. 2+-ATPase in sea urchin spermatozoa. FEBS Letters 580 3900-3904.
35. Gunter TE, Yule DI, Gunter KK, Eliseev RA & Salter JD 2004 Calcium and mitochondria. FEBS Letters 567 96-102.
36. i oscillations and cyclical transitions in flagellar beating. Journal of Biological Chemistry 279 46315-46325.
37. i signals in human spermatozoa. Journal of Cell Science 15 1673-1685.
38. Harper CV, Cummerson JA, White MR, Publicover SJ & Johnson PM 2008 Dynamic resolution of acrosomal exocytosis in human sperm. Journal of Cell Science 121 2130-2135.
39. Herrick SB, Schweissinger DL, Kim SW, Bayan KR, Mann S & Cardullo RA 2005 The acrosomal vesicle of mouse sperm is a calcium store. Journal of Cellular Physiology 202 663-671. (Pubitemid 40175841)
40. Hirohashi N & Vacquier VD 2003 Store-operated calcium channels trigger exocytosis of the sea urchin sperm acrosomal vesicle. Biochemical and Biophysical Research Communications 304 285-292. (Pubitemid 36452338)
41. 2+ store is involved in sperm hyperactivated motility. Biology of Reproduction 65 1606-1615.
42. Ho HC & Suarez SS 2003 Characterization of the intracellular calcium store at the base of the sperm flagellum that regulates hyperactivated motility. Biology of Reproduction 68 1590-1596.
43. Humbert J-P, Matter NM, Artault J-C, Köppler P & Malviya AN 1996 Inositol 1,4,5-trisphosphate receptor is located to the inner nuclear membrane vindicating regulation of nuclear calcium signaling by inositol 1,4,5-trisphosphate. Journal of Biological Chemistry 271 478-485.
44. Jeong SY & Seol DW 2008 The role of mitochondria in apoptosis. BMB Reports 41 11-22.
45. Jimenez-Gonzalez C, Michelangeli F, Harper CV, Barratt CL & Publicover SJ 2006 Calcium signalling in human spermatozoa: a specialized 'toolkit' of channels, transporters and stores. Human Reproduction Update 12 253-267.
46. 2+ into mouse sperm triggered by egg ZP3. Nature Cell Biology 3 499-502.
47. 2+ influx requires the channel function of orai1 and TRPC1. Journal of Biological Chemistry 284 9733-9741.
48. Kinnear NP, Boittin FX, Thomas JM, Galione A & Evans AM 2004 Lysosome-sacroplasmic reticulum junctions. A trigger zone for calcium signaling by nicotinic acid adenine dinucleotide phosphate and endothelin-1. Journal of Biological Chemistry 279 54319-54326. (Pubitemid 40053170)
49. Kirichok Y, Krapivinsky G & Clapham DE 2004 The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427 360-364. (Pubitemid 38133664)
50. Kirkman-Brown JC, Barratt CL & Publicover SJ 2004 Slow calcium oscillations in human spermatozoa. Biochemical Journal 378 827-832.
51. Krausz C, Bonaccorsi L, Luconi M, Fuzzi B, Criscuoli L, Pellegrini S, Forti G & Baldi E 1995 Intracellular calcium increase and acrosome reaction in response to progesterone in human spermatozoa are correlated with in-vitro fertilization. Human Reproduction 10 120-124.
52. 3) receptors in human sperm? Life Sciences 65 135-143.
53. Lanini L, Bachs O & Carafoli E 1992 The calcium pump of the liver nuclear membrane is identical to that of the endoplasmic reticulum. Journal of Biological Chemistry 267 11548-11552.
54. Lawson C, Dorval V, Goupil S & Leclerc P 2007 Identification and localisation of SERCA 2 isoforms in mammalian sperm. Molecular Human Reproduction 13 307-316. (Pubitemid 47061641)
55. Lefievre L, Chen Y, Conner SJ, Scott JL, Publicover SJ, Ford WC & Barratt CL 2007 Human spermatozoa contain multiple targets for protein S-nitrosylation: an alternative mechanism of the modulation of sperm function by nitric oxide? Proteomics 7 3066-3084.
56. 2+ stores and flagellar regulation in human sperm by S-nitrosylation: a role for NO synthesised in the female reproductive tract. Development 135 3677-3686.
57. 2+ to regulation of sperm motility: release of intracellular stores can hyperactivate CatSper1 and CatSper2 null sperm. Developmental Biology 303 214-221.
58. Mayorga LS, Tomes CN & Belmonte SA 2007 Acrosomal exocytosis, a special type of regulated secretion. IUBMB Life 59 286-292.
59. Meizel S & Turner KO 1993 Initiation of the human sperm acrosome reaction by thapsigargin. Journal of Experimental Zoology 267 350-355.
60. Michelangeli F, Mezna M, Tovey S & Sayers LG 1995 Pharmacological modulators of the inositol 1,4,5-trisphosphate receptor. Neuropharmacology 34 1111-1122.
61. 2+ stores. Current Opinion in Cell Biology 17 135-140.
62. Missiaen L, Van Acker K, Van Baelen K, Raeymaekers L, Wuytack F, Parys JB, De Smedt H, Vanoevelen J, Dode L, Rizzuto R et al. 2004 Calcium release from the Golgi apparatus and the endoplasmic reticulum in HeLa cells stably expressing targeted aequorin to these compartments. Cell Calcium 36 479-487.
63. Naaby-Hansen S, Wolkowicz MJ, Klotz K, Bush LA, Westbrook VA, Shibahara H, Shetty J, Coonrod SA, Reddi PP, Shannon J et al. 2001 Co-localization of the inositol 1,4,5-trisphosphate receptor and calreticulin in the equatorial segment and in membrane bounded vesicles in the cytoplasmic droplet of human spermatozoa. Molecular Human Reproduction 7 923-933. (Pubitemid 32952174)
64. Nakamura M, Michikawa Y, Baba T, Okinaga S & Arai K 1992 Calreticulin is present in the acrosome of spermatids of rat testis. Biochemical and Biophysical Research Communications 186 668-673.
65. Nakamura M, Moriya M, Baba T, Michikawa Y, Yamanobe T, Arai K, Okinaga S & Kobayashi T 1993 An endoplasmic reticulum protein, calreticulin, is transported into the acrosome of rat sperm. Experimental Cell Research 205 101-110.
66. Navarro B, Kirichok Y, Chung JJ & Clapham DE 2008 Ion channels that control fertility in mammalian spermatozoa. International Journal of Developmental Biology 52 607-613.
67. Orrenius S, Zhivotovsky B & Nicotera P 2003 Regulation of cell death: the calcium-apoptosis link. Nature Reviews. Molecular Cell Biology 47 552-565.
68. O'Toole CM, Arnoult C, Darzon A, Steinhardt RA & Florman HM 2000 Ca2+ entry through store-operated channels in mouse sperm is initiated by egg ZP3 and drives the acrosome reaction. Molecular Biology of the Cell 11 1571-1584. (Pubitemid 30307897)
69. Parekh AB & Putney JW Jr 2005 Store-operated calcium channels. Physiological Reviews 85 757-810.
70. 2+ channels and the acrosome reaction: which channels are present and what do they do? Human Reproduction 14 873-879.
71. i signalling in sperm - making the most of what you've got. Nature Cell Biology 9 235-242.
72. Rimessi A, Giorgi C, Pinton P & Rizzuto R 2008 The versatility of mitochondrial calcium signals: from stimulation of cell metabolism to induction of cell death. Biochimica et Biophysica Acta 1777 808-816.
73. Rossato M, Di Virgilio F, Rizzuto R, Galeazzi C & Foresta C 2001 Intracellular calcium store depletion and acrosome reaction in human spermatozoa: role of calcium and plasma membrane potential. Molecular Human Reproduction 7 119-128. (Pubitemid 32148338)
74. Spungin B & Breitbart H 1996 Calcium mobilization and influx during sperm exocytosis. Journal of Cell Science 109 1947-1955. (Pubitemid 26248640)
75. Stamboulian S, Moutin MJ, Treves S, Pochon N, Grunwald D, Zorzato F, De Waard M, Ronjat M & Arnoult C 2005 Junctate, an inositol 1,4,5-triphosphate receptor associated protein, is present in rodent sperm and binds TRPC2 and TRPC5 but not TRPC1 channels. Developmental Biology 286 326-337. (Pubitemid 41394066)
76. Storey BT & Keyhani E 1973 Interaction of calcium ion with the mitochondria in rabbit spermatozoa. FEBS Letters 37 33-36.
77. Storey BT & Keyhani E 1974 Energy metabolism of spermatozoa: III. Energy-linked uptake of calcium ion by the mitochondria of rabbit epididymal spermatozoa. Fertility and Sterility 25 976-984.
78. Strange K, Yan X, Lorin-Nebel C & Xing J 2007 Physiological roles of STIM1 and Orai1 homologs and CRAC channels in the genetic model organism Caenorhabditis elegans. Cell Calcium 42 193-203. (Pubitemid 47029597)
79. Suarez SS & Dai X 1995 Intracellular calcium reaches different levels of elevation in hyperactivated and acrosome-reacted hamster sperm. Molecular Reproduction and Development 42 325-333.
80. Surroca A & Wolff D 2000 Inositol 1,4,5-trisphosphate but not ryanodine-receptor agonists induces calcium release from rat liver Golgi apparatus membrane vesicles. Journal of Membrane Biology 177 243-249. (Pubitemid 32268860)
81. Sutton KA, Jungnickel MK, Wang Y, Cullen K, Lambert S & Florman HM 2004 Enkurin is a novel calmodulin and TRPC channel binding protein in sperm. Developmental Biology 274 426-435. (Pubitemid 39295731)
82. 2+ mobilization? Biochemical Society Transactions 23 637-642.
83. Thomas P & Meizel S 1989 Phosphatidylinositol 4,5-trisphosphate hydrolysis in human sperm stimulated with follicular fluid or progesterone is dependent upon Ca2+ influx. Biochemical Journal 264 539-546. (Pubitemid 20024526)
84. Tomes CN, McMaster CR & Saling PM 1996 Activation of mouse sperm phosphatidylinositol-4,5 bisphosphate-phospholiapase C by zona pellucida is modulated by tyrosine phosphorylation. Molecular Reproduction and Development 43 196-204. (Pubitemid 26049796)
85. 2+-ATPases. Trends in Pharmacological Sciences 19 131-135.
86. Trevino CL, Santi CM, Beltran C, Hernandez-Cruz A, Darzon A & Lomeli H 1998 Localisation of inositol trisphosphate and ryanodine receptors during mouse spermatogenesis: possible functional implications. Zygote 6 159-172. (Pubitemid 128566349)
87. Varano G, Lombardi A, Cantini G, Forti G, Baldi E & Luconi M 2008 Src activation triggers capacitation and acrosome reaction but not motility in human spermatozoa. Human Reproduction 23 2652-2662.
88. 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. Molecular Reproduction and Development 25 186-194. (Pubitemid 20096814)
89. Walensky LD & Snyder SH 1995 Inositol 1,4,5-trisphosphate receptors selectively localized to the acrosome of mammalian sperm. Journal of Cell Biology 130 857-869.
90. Wang Y, Deng X, Hewavitharana T, Soboloff J & Gill DL 2008 Stim, ORAI and TRPC channels in the control of calcium entry signals in smooth muscle. Clinical and Experimental Pharmacology & Physiology 35 1127-1133.
91. Wennemuth G, Babcock DF & Hille B 2003 Calcium clearance mechanisms of mouse sperm. Journal of General Physiology 122 115-128. (Pubitemid 36859135)
92. Williams KM & Ford WC 2003 Effects of Ca-ATPase inhibitors on the intracellular calcium activity and motility of human spermatozoa. International Journal of Andrology 26 366-375.
93. 2+pump isoforms 1, 2, and 3 to thapsigargin and other inhibitors. Journal of Biological Chemistry 281 6970-6976.
94. 2+-ATPase (SPCA1) in different mammalian tissues. Biochimica et Biophysica Acta 1664 189-197.
95. Xia J & Ren D 2009 Egg coat proteins activate calcium entry into mouse sperm via CATSPER channels. Biology of Reproduction 80 1092-1098.
96. 2+ entry into mouse sperm triggers a tail-to-head propagation. Biology of Reproduction 77 551-559.
97. Zalk R, Lehnart SE & Marks AR 2007 Modulation of the ryanodine receptor and intracellular calcium. Annual Review of Biochemistry 76 367-385.
98. Zapata O, Ralston J, Beltran C, Parys JB, Chen JL, Longo FJ & Darzon A 1997 Inositol trisphosphate receptors in sea urchin sperm. Zygote 5 355-364. (Pubitemid 127594324)
99. Zarelli VE, Rute MC, Roggero CM, Mayorga LS & Tomes CN 2009 PTB1B dephosphorylates NSF elicits SNARE complex disassembly during human sperm exocytosis. Journal of Biological Chemistry 284 10491-10503.