دورية أكاديمية

Cdc42 localized in the CatSper signaling complex regulates cAMP-dependent pathways in mouse sperm.

التفاصيل البيبلوغرافية
العنوان: Cdc42 localized in the CatSper signaling complex regulates cAMP-dependent pathways in mouse sperm.
المؤلفون: Luque GM; Instituto de Biología y Medicina Experimental (IBYME-CONICET), Ciudad Autónoma de Buenos Aires, Argentina., Xu X; Department of Electrical and Computer Engineering, Colorado State University, Fort Collins, CO, USA., Romarowski A; Instituto de Biología y Medicina Experimental (IBYME-CONICET), Ciudad Autónoma de Buenos Aires, Argentina.; Department of Veterinary and Animal Science, University of Massachusetts, Amherst, MA, USA., Gervasi MG; Department of Veterinary and Animal Science, University of Massachusetts, Amherst, MA, USA., Orta G; Instituto de Biotecnología, UNAM, Cuernavaca, México., De la Vega-Beltrán JL; Instituto de Biotecnología, UNAM, Cuernavaca, México., Stival C; Instituto de Biología Molecular y Celular de Rosario (CONICET-UNR), Rosario, Santa Fe, Argentina., Gilio N; Instituto de Biología y Medicina Experimental (IBYME-CONICET), Ciudad Autónoma de Buenos Aires, Argentina., Dalotto-Moreno T; Instituto de Biología y Medicina Experimental (IBYME-CONICET), Ciudad Autónoma de Buenos Aires, Argentina., Krapf D; Instituto de Biología Molecular y Celular de Rosario (CONICET-UNR), Rosario, Santa Fe, Argentina., Visconti PE; Department of Veterinary and Animal Science, University of Massachusetts, Amherst, MA, USA., Krapf D; Department of Electrical and Computer Engineering, Colorado State University, Fort Collins, CO, USA., Darszon A; Instituto de Biotecnología, UNAM, Cuernavaca, México., Buffone MG; Instituto de Biología y Medicina Experimental (IBYME-CONICET), Ciudad Autónoma de Buenos Aires, Argentina.
المصدر: FASEB journal : official publication of the Federation of American Societies for Experimental Biology [FASEB J] 2021 Aug; Vol. 35 (8), pp. e21723.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Federation of American Societies for Experimental Biology Country of Publication: United States NLM ID: 8804484 Publication Model: Print Cited Medium: Internet ISSN: 1530-6860 (Electronic) Linking ISSN: 08926638 NLM ISO Abbreviation: FASEB J Subsets: MEDLINE
أسماء مطبوعة: Publication: 2020- : [Bethesda, Md.] : Hoboken, NJ : Federation of American Societies for Experimental Biology ; Wiley
Original Publication: [Bethesda, Md.] : The Federation, [c1987-
مواضيع طبية MeSH: Calcium Channels/*metabolism , Spermatozoa/*metabolism , cdc42 GTP-Binding Protein/*metabolism, Animals ; Calcium/metabolism ; Calcium Channels/deficiency ; Calcium Channels/genetics ; Calcium Signaling ; Cyclic AMP/metabolism ; Female ; Fertilization in Vitro ; Male ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Mice, Knockout ; Models, Biological ; Signal Transduction ; Sperm Capacitation/physiology ; Sperm Motility/physiology ; Sperm Tail/metabolism ; Spermatozoa/drug effects ; Spermatozoa/ultrastructure ; cdc42 GTP-Binding Protein/antagonists & inhibitors
مستخلص: Sperm acquire the ability to fertilize in a process called capacitation and undergo hyperactivation, a change in the motility pattern, which depends on Ca 2+ transport by CatSper channels. CatSper is essential for fertilization and it is subjected to a complex regulation that is not fully understood. Here, we report that similar to CatSper, Cdc42 distribution in the principal piece is confined to four linear domains and this localization is disrupted in CatSper1-null sperm. Cdc42 inhibition impaired CatSper activity and other Ca 2+ -dependent downstream events resulting in a severe compromise of the sperm fertilizing potential. We also demonstrate that Cdc42 is essential for CatSper function by modulating cAMP production by soluble adenylate cyclase (sAC), providing a new regulatory mechanism for the stimulation of CatSper by the cAMP-dependent pathway. These results reveal a broad mechanistic insight into the regulation of Ca 2+ in mammalian sperm, a matter of critical importance in male infertility as well as in contraception.
(© 2021 Federation of American Societies for Experimental Biology.)
References: Hall A. Rho family GTPases. Biochem Soc Trans. 2012;40(6):1378-1382. https://doi.org/10.1042/BST20120103.
Ducummon CC, Berger T. Localization of the Rho GTPases and some Rho effector proteins in the sperm of several mammalian species. Zygote. 2006;14(3):249-257. https://doi.org/10.1017/S0967199406003790.
Baltiérrez-Hoyos R, Roa-Espitia AL, Hernández-González EO, Baltierrez-Hoyos R, Roa-Espitia AL, Hernandez-González EO. The association between CDC42 and caveolin-1 is involved in the regulation of capacitation and acrosome reaction of guinea pig and mouse sperm. Reproduction. 2012;144(1):123-134. https://doi.org/10.1530/REP-11-0433.
Romarowski A, Battistone MA, La Spina FA, et al. PKA-dependent phosphorylation of LIMK1 and Cofilin is essential for mouse sperm acrosomal exocytosis. Dev Biol. 2015;405(2):237-249. https://doi.org/10.1016/j.ydbio.2015.07.008.
Delgado-Buenrostro NL, Hernández-González EO, Segura-nieto M, Mújica A. Actin polymerization in the equatorial and postacrosomal regions of guinea pig spermatozoa during the acrosome reaction is regulated by G proteins. Mol Reprod Dev. 2005;70(2):198-210. https://doi.org/10.1002/mrd.20192.
Fujita A, Nakamura K, Kato T, et al. Ropporin, a sperm-specific binding protein of rhophilin, that is localized in the fibrous sheath of sperm flagella. J Cell Sci. 2000;113(Pt 1):103-112.
Chen F, Ma L, Parrini MC, et al. Cdc42 is required for PIP(2)-induced actin polymerization and early development but not for cell viability. Curr Biol. 2000;10(13):758-765.
Wong EWP, Mruk DD, Lee WM, Cheng CY. Regulation of blood-testis barrier dynamics by TGF-β3 is a Cdc42-dependent protein trafficking event. Proc Natl Acad Sci U S A. 2010;107(25):11399-11404. https://doi.org/10.1073/pnas.1001077107.
Chapin RE, Wine RN, Harris MW, Borchers CH, Haseman JK. Structure and control of a cell-cell adhesion complex associated with spermiation in rat seminiferous epithelium. J Androl. 2001;22(6):1030-1052. https://doi.org/10.1002/j.1939-4640.2001.tb03444.x.
Chang MC. Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature. 1951;168(4277):697-698.
Austin CR. The capacitation of the mammalian sperm. Nature. 1952;170(4321):326. https://doi.org/10.1038/170326a0.
Visconti PE, Moore GD, Bailey JL, et al. Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development. 1995;121(4):1139-1150.
Alvau A, Battistone MA, Gervasi MG, et al. The tyrosine kinase FER is responsible for the capacitation-associated increase in tyrosine phosphorylation in murine sperm. Dev. 2016;143(13):2325-2333. https://doi.org/10.1242/dev.136499.
Navarrete FA, García-Vázquez FA, Alvau A, et al. Biphasic role of calcium in mouse sperm capacitation signaling pathways. J Cell Physiol. 2015;230(8):1758-1769. https://doi.org/10.1002/jcp.24873.
Orta G, Vega-Beltran JL, Hidalgo D, Santi CM, Visconti P, Darszon A. CatSper channels are regulated by protein kinase A. J Biol Chem. 2018;293:16830-16841. https://doi.org/10.1074/jbc.RA117.001566.
Balbach M, Hamzeh H, Jikeli JF, et al. Molecular mechanism underlying the action of zona-pellucida glycoproteins on mouse sperm. Front Cell Dev Biol. 2020;8. https://doi.org/10.3389/fcell.2020.572735.
Luque GM, Dalotto-Moreno T, Martín-Hidalgo D, et al. Only a subpopulation of mouse sperm displays a rapid increase in intracellular calcium during capacitation. J Cell Physiol. 2018;233(12):9685-9700. https://doi.org/10.1002/jcp.26883.
Suarez SS, Ho HC. Hyperactivation of mammalian sperm. Cell Mol Biol. 2003;49(3):351-356.
Demott RP, Suarez SS. Hyperactivated sperm progress in the mouse oviduct. Biol Reprod. 1992;46(5):779-785. https://doi.org/10.1095/biolreprod46.5.779.
Stauss CR, Votta TJ, Suarez SS. Sperm motility hyperactivation facilitates penetration of the hamster zona pellucida. Biol Reprod. 1995;53(6):1280-1285.
Ren D, Navarro B, Perez G, et al. A sperm ion channel required for sperm motility and male fertility. Nature. 2001;413(6856):603-609. https://doi.org/10.1038/35098027.
Quill TA, Ren D, Clapham DE, Garbers DL. A voltage-gated ion channel expressed specifically in spermatozoa. Proc Natl Acad Sci U S A. 2001;98(22):12527-12531. https://doi.org/10.1073/pnas.221454998.
Lobley A, Pierron V, Reynolds L, Allen L, Michalovich D. Identification of human and mouse CatSper3 and CatSper 4 genes: Characterisation of a common interaction domain and evidence for expression in testis. Reprod Biol Endocrinol. 2003;1. https://doi.org/10.1186/1477-7827-1-53.
Kirichok Y, Lishko PV. Rediscovering sperm ion channels with the patch-clamp technique. Mol Hum Reprod. 2011;17(8):478-499. https://doi.org/10.1093/molehr/gar044.
Navarro B, Kirichok Y, Chung J-J, Clapham DE. Ion channels that control fertility in mammalian spermatozoa. Int J Dev Biol. 2008;52(5-6):607-613. https://doi.org/10.1387/ijdb.072554bn.
Liu J, Xia J, Cho K-H, Clapham DE, Ren D. CatSperbeta, a novel transmembrane protein in the CatSper channel complex. J Biol Chem. 2007;282(26):18945-18952. https://doi.org/10.1074/jbc.M701083200.
Chung J-J, Navarro B, Krapivinsky G, Krapivinsky L, Clapham DE. A novel gene required for male fertility and functional CATSPER channel formation in spermatozoa. Nat Commun. 2011;2:153. https://doi.org/10.1038/ncomms1153.
Wang H, Liu J, Cho K-H, Ren D. A novel, single, transmembrane protein CATSPERG is associated with CATSPER1 channel protein. Biol Reprod. 2009;81(3):539-544. https://doi.org/10.1095/biolreprod.109.077107.
Chung J-J, Miki K, Kim D, et al. CatSperζ regulates the structural continuity of sperm Ca2+ signaling domains and is required for normal fertility. eLife. 2017;6:e23082. https://doi.org/10.7554/eLife.23082.
Hwang JY, Mannowetz N, Zhang Y, et al. Dual sensing of physiologic pH and calcium by EFCAB9 regulates sperm motility. Cell. 2019;177(6):1480-1494.e19. https://doi.org/10.1016/j.cell.2019.03.047.
Qi H, Moran MM, Navarro B, et al. All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility. Proc Natl Acad Sci U S A. 2007;104(4):1219-1223. https://doi.org/10.1073/pnas.0610286104.
Quill TA, Sugden SA, Rossi KL, Doolittle LK, Hammer RE, Garbers DL. Hyperactivated sperm motility driven by CatSper2 is required for fertilization. Proc Natl Acad Sci U S A. 2003;100(25):14869-14874. https://doi.org/10.1073/pnas.2136654100.
Avenarius MR, Hildebrand MS, Zhang Y, et al. Human male infertility caused by mutations in the CATSPER1 channel protein. Am J Hum Genet. 2009;84(4):505-510. https://doi.org/10.1016/j.ajhg.2009.03.004.
Avidan N, Tamary H, Dgany O, et al. CATSPER2, a human autosomal nonsyndromic male infertility gene. Eur J Hum Genet. 2003;11(7):497-502. https://doi.org/10.1038/sj.ejhg.5200991.
Smith JF, Syritsyna O, Fellous M, et al. Disruption of the principal, progesterone-activated sperm Ca2+ channel in a CatSper2-deficient infertile patient. Proc Natl Acad Sci U S A. 2013;110(17):6823-6828. https://doi.org/10.1073/pnas.1216588110.
Lishko PV, Botchkina IL, Kirichok Y. Progesterone activates the principal Ca2+ channel of human sperm. Nature. 2011;471(7338):387-391. https://doi.org/10.1038/nature09767.
Miller MR, Mansell SA, Meyers SA, Lishko PV. Flagellar ion channels of sperm: similarities and differences between species. Cell Calcium. 2015;58(1):105-113. https://doi.org/10.1016/j.ceca.2014.10.009.
Miller MR, Mannowetz N, Iavarone AT, et al. Unconventional endocannabinoid signaling governs sperm activation via the sex hormone progesterone. Science. 2016;352(6285):555-559. https://doi.org/10.1126/science.aad6887.
Kirichok Y, Navarro B, Clapham DE. Whole-cell patch-clamp measurements of spermatozoa reveal an alkaline-activated Ca2+ channel. Nature. 2006;439:737-740. https://doi.org/10.1038/nature04417.
Lishko PV, Botchkina IL, Fedorenko A, Kirichok Y. Acid extrusion from human spermatozoa is mediated by flagellar voltage-gated proton channel. Cell. 2010;140(3):327-337. https://doi.org/10.1016/j.cell.2009.12.053.
Lishko PV, Mannowetz N. CatSper: a unique calcium channel of the sperm flagellum. Curr Opin Physiol. 2018;2:109-113. https://doi.org/10.1016/j.cophys.2018.02.004.
Chung J-JJ, Shim S-HH, Everley RA, Gygi SP, Zhuang X, Clapham DE. Structurally distinct Ca2+ signaling domains of sperm flagella orchestrate tyrosine phosphorylation and motility. Cell. 2014;157(4):808-822. https://doi.org/10.1016/j.cell.2014.02.056.
Navarrete FA, Alvau A, Lee HC, et al. Transient exposure to calcium ionophore enables in vitro fertilization in sterile mouse models. Sci Rep. 2016;6:33589. https://doi.org/10.1038/srep33589.
Weigel AV, Simon B, Tamkun MM, Krapf D. Ergodic and nonergodic processes coexist in the plasma membrane as observed by single-molecule tracking. Proc Natl Acad Sci. 2011;108(16):6438-6443. https://doi.org/10.1073/pnas.1016325108.
Campagnola G, Nepal K, Schroder BW, Peersen OB, Krapf D. Superdiffusive motion of membrane-targeting C2 domains. Sci Rep. 2015;5(1):17721. https://doi.org/10.1038/srep17721.
Izeddin I, El Beheiry M, Andilla J, Ciepielewski D, Darzacq X, Dahan M. PSF shaping using adaptive optics for three-dimensional single-molecule super-resolution imaging and tracking. Opt Express. 2012;20(5):4957. https://doi.org/10.1364/OE.20.004957.
Gervasi MG, Xu X, Carbajal-Gonzalez B, Buffone MG, Visconti PE, Krapf D. The actin cytoskeleton of the mouse sperm flagellum is organized in a helical structure. J Cell Sci. 2018;131:jcs.215897. https://doi.org/10.1242/jcs.215897.
Huang B, Wang W, Bates M, Zhuang X. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science. 2008;319(5864):810-813. https://doi.org/10.1126/science.1153529.
Ovesný M, Křížek P, Borkovec J, Švindrych Z, Hagen GM. ThunderSTORM: a comprehensive ImageJ plug-in for PALM and STORM data analysis and super-resolution imaging. Bioinformatics. 2014;30(16):2389-2390. https://doi.org/10.1093/bioinformatics/btu202.
Stival C, Ritagliati C, Xu X, et al. Disruption of protein kinase A localization induces acrosomal exocytosis in capacitated mouse sperm. J Biol Chem. 2018;293(24):jbc.RA118.002286. https://doi.org/10.1074/jbc.RA118.002286.
Escoffier J, Krapf D, Navarrete F, Darszon A, Visconti PE. Flow cytometry analysis reveals a decrease in intracellular sodium during sperm capacitation. J Cell Sci. 2012;125(2):473-485. https://doi.org/10.1242/jcs.093344.
Demarco IA, Espinosa F, Edwards J, et al. Involvement of a Na+/HCO3-cotransporter in mouse sperm capacitation. J Biol Chem. 2003;278(9):7001-7009. https://doi.org/10.1074/jbc.M206284200.
López-González I, Torres-Rodríguez P, Sánchez-Carranza O, et al. Membrane hyperpolarization during human sperm capacitation. Mol Hum Reprod. 2014;20(7):619-629. https://doi.org/10.1093/molehr/gau029.
Ernesto JI, Weigel Muñoz M, Battistone MA, et al. CRISP1 as a novel CatSper regulator that modulates sperm motility and orientation during fertilization. J Cell Biol. 2015;210(7):1213-1224. https://doi.org/10.1083/jcb.201412041.
Rust MJ, Bates M, Zhuang X. STORM. Nat Meth. 2006;3(10):793-796. https://doi.org/10.1038/nmeth929.
Rossman KL, Der CJ, Sondek J. GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat Rev Mol Cell Biol. 2005;6(2):167-180. https://doi.org/10.1038/nrm1587.
Garcia-Mata R, Boulter E, Burridge K. The, “invisible hand”: regulation of RHO GTPases by RHOGDIs. Nat Rev Mol Cell Biol. 2011;12(8):493-504. https://doi.org/10.1038/nrm3153.
Surviladze Z, Waller A, Wu Y, et al. Identification of a small GTPase inhibitor using a high-throughput flow cytometry bead-based multiplex assay. J Biomol Screen. 2010;15(1):10-20. https://doi.org/10.1177/1087057109352240.
Espinosa F, Darszon A. Mouse sperm membrane potential: changes induced by Ca2+. FEBS Lett. 1995;372:119-125.
Torres-Flores V, Picazo-Juárez G, Hernández-Rueda Y, Darszon A, González-Martínez MT. Sodium influx induced by external calcium chelation decreases human sperm motility. Hum Reprod. 2011;26(10):2626-2635. https://doi.org/10.1093/humrep/der237.
Barratt CL, Publicover SJ. Sperm are promiscuous and CatSper is to blame…. EMBO J. 2012;31(7):1624-1626. https://doi.org/10.1038/emboj.2012.62.
Brenker C, Goodwin N, Weyand I, et al. The CatSper channel: a polymodal chemosensor in human sperm. EMBO J. 2012;31(7):1654-1665. https://doi.org/10.1038/emboj.2012.30.
Pelish HE, Peterson JR, Salvarezza SB, et al. Secramine inhibits Cdc42-dependent functions in cells and Cdc42 activation in vitro. Nat Chem Biol. 2006;2(1):39-46. https://doi.org/10.1038/nchembio751.
Peterson JR, Lebensohn AM, Pelish HE, Kirschner MW. Biochemical suppression of small-molecule inhibitors: a strategy to identify inhibitor targets and signaling pathway components. Chem Biol. 2006;13(4):443-452. https://doi.org/10.1016/j.chembiol.2006.02.009.
Friesland A, Zhao Y, Chen YH, Wang L, Zhou H, Lu Q. Small molecule targeting Cdc42-intersectin interaction disrupts Golgi organization and suppresses cell motility. Proc Natl Acad Sci U S A. 2013;110(4):1261-1266. https://doi.org/10.1073/pnas.1116051110.
Hong L, Kenney SRay, Phillips GK, et al. Characterization of a Cdc42 protein inhibitor and its use as a molecular probe. J Biol Chem. 2013;288(12):8531-8543. https://doi.org/10.1074/jbc.M112.435941.
Razani B, Engelman JA, Wang XB, et al. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem. 2001;276(41):38121-38138. https://doi.org/10.1074/jbc.M105408200.
Miyata H, Satouh Y, Mashiko D, et al. Sperm calcineurin inhibition prevents mouse fertility with implications for male contraceptive. Science. 2015;350(6259):442-445. https://doi.org/10.1126/science.aad0836.
Dey S, Eisa A, Kline D, Wagner FF, Abeysirigunawardena S, Vijayaraghavan S. Roles of glycogen synthase kinase 3 alpha and calcineurin in regulating the ability of sperm to fertilize eggs. FASEB J. 2020;34(1):1247-1269. https://doi.org/10.1096/fj.201902163R.
Angeles-Floriano T, Roa-Espitia AL, Baltiérrez-Hoyos R, Cordero-Martínez J, Elizondo G, Hernández-González EO. Absence of aryl hydrocarbon receptor alters CDC42 expression and prevents actin polymerization during capacitation. Mol Reprod Dev. 2016;83(11):1015-1026. https://doi.org/10.1002/mrd.22736.
Wang T, Young S, Krenz H, et al. The Ca2+ channel CatSper is not activated by cAMP/PKA signaling but directly affected by chemicals used to probe the action of cAMP and PKA. J Biol Chem. 2020;295(38):13181-13193. https://doi.org/10.1074/jbc.RA120.013218.
Miller MR, Kenny SJ, Mannowetz N, et al. Asymmetrically positioned flagellar control units regulate human sperm rotation. Cell Rep. 2018;24(10):2606-2613. https://doi.org/10.1016/j.celrep.2018.08.016.
Chávez JC, Ferreira JJ, Butler A, et al. SLO3 K+ channels control calcium entry through CATSPER channels in sperm. J Biol Chem. 2014;289(46):32266-32275. https://doi.org/10.1074/jbc.M114.607556.
Wang XF, Zhou CX, Shi QX, et al. Involvement of CFTR in uterine bicarbonate secretion and the fertilizing capacity of sperm. Nat Cell Biol. 2003;5(10):902-906. https://doi.org/10.1038/ncb1047.
Wang D, Hu J, Bobulescu IA, et al. A sperm-specific Na+/H+ exchanger (sNHE) is critical for expression and in vivo bicarbonate regulation of the soluble adenylyl cyclase (sAC). Proc Natl Acad Sci. 2007;104(22):9325-9330. https://doi.org/10.1073/pnas.0611296104.
Liu T, Huang J-C, Lu C-L, et al. Immunization with a DNA vaccine of testis-specific sodium-hydrogen exchanger by oral feeding or nasal instillation reduces fertility in female mice. Fertil Steril. 2010;93(5):1556-1566. https://doi.org/10.1016/j.fertnstert.2009.03.056.
Chen S-R, Chen M, Deng S-L, Hao X-X, Wang X-X, Liu Y-X. Sodium-hydrogen exchanger NHA1 and NHA2 control sperm motility and male fertility. Cell Death Dis. 2016;7(3):e2152. https://doi.org/10.1038/cddis.2016.65.
Frantz C, Karydis A, Nalbant P, Hahn KM, Barber DL. Positive feedback between Cdc42 activity and H+ efflux by the Na-H exchanger NHE1 for polarity of migrating cells. J Cell Biol. 2007;179(3):403-410. https://doi.org/10.1083/jcb.200704169.
فهرسة مساهمة: Keywords: calcium; capacitation; hyperactivation; sperm; super-resolution
المشرفين على المادة: 0 (Calcium Channels)
0 (Catsper1 protein, mouse)
0 (Cdc42 protein, mouse)
E0399OZS9N (Cyclic AMP)
EC 3.6.5.2 (cdc42 GTP-Binding Protein)
SY7Q814VUP (Calcium)
تواريخ الأحداث: Date Created: 20210705 Date Completed: 20210719 Latest Revision: 20210729
رمز التحديث: 20240829
DOI: 10.1096/fj.202002773RR
PMID: 34224609
قاعدة البيانات: MEDLINE
الوصف
تدمد:1530-6860
DOI:10.1096/fj.202002773RR