Soluble and membrane associated adenylate cyclases participate in capacitation with hyaluronic acid in bovine spermatozoa
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Abstract
Hyaluronic acid (HA), a glycosaminoglycan present in the female reproductive tract, mediates sperm motility, maturation and capacitation. Two adenylate cyclases, soluble (sAC) and membrane-associated (mAC), isoenzymes are present in spermatozoa, participating in different signaling mechanisms. The aim of this study was to determine the effect of adenylate cyclase isoenzymes inhibition on bovine sperm processes, such as capacitation, motility, viability, mitochondrial activity and fertilizing capacity, during sperm capacitation with HA. HA was used as a capacitation inducer, while LRE-1 (a specific sAC inhibitor) and 2,5-dideoxyadenosine (2,5-D) were used as sAC and mAC inhibitors, respectively. We evaluated sperm capacitation (chlortetracycline [CTC] technique), viability (trypan blue stain and differential interference contrast), mitochondrial activity (fluorochrome 5,5′,6,6′-tetrachloro-1,1′,3,3′-tetraethylbenzimidazolylcarbocyanine iodide [JC-1]) and motility (computer-assisted sperm analysis). We carried out in vitro fertilization (IVF) in IVF- modified synthetic oviductal fluid (mSOF) with frozen-thawed semen. We then cultured presumptive zygotes for 48 hours and analysed the cleavage rate. The addition of sAC or mAC inhibitors, alone or combined, produced a significant decrease in capacitation, mitochondrial activity and motility with respect to sperm samples incubated only with HA and controls (P < 0.05). Cleavage rates decreased with the addition of adeylate cyclase (AC) inhibitors compared to HA alone. We observed a greater decrease in cleavage rate with the addition of LRE-1 than with 2,5-D (P < 0.05). The combination of both inhibitors decreased the cleavage rate with respect to each inhibitor alone (P < 0.05). In bovine spermatozoa, both soluble and membrane-associated adenylate cyclase isoenzymes could participate in the intracellular signaling mechanism and mitochondrial function, which modulate HA capacitation and sperm fertilizing ability.
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References
Lee CN, Ax RL. Concentrations and composition of glycosaminoglycans in the female bovine reproductive tract. Journal Dairy Science. 1984;(67):2006–2009. doi.org/10.3168/jds.S0022-0302(84)81536-2. DOI: https://doi.org/10.3168/jds.S0022-0302(84)81536-2
Suchanek E, Simunic V, Juretic D, Grizelj V. Follicular fluid contents of hyaluronic acid, follicle-stimulating hormone and steroids relative to the success of in vitro fertilization of human oocytes. Fertilityand Sterility. 1994;62:347–352. doi.org/10.1016/s0015-0282(16)56890-3. DOI: https://doi.org/10.1016/S0015-0282(16)56890-3
Eppig JJ. FSH stimulates hyaluronic acid synthesis in oocyte-cumulus cell complexes from mouse preovulatoryfollicules. Nature. 1979;281(5731):483–484. doi.org/10.1038/281483a0. DOI: https://doi.org/10.1038/281483a0
Binette JP, Ohishi H, Burgi W, Kimura A, Suyemitsu T, Seno N, et al. The content and distribution of glycosaminoglycans in the ejaculates of normal and vasectomized men. Andrologia. 1996;28(3):145–149. doi.org/10.1111/j.1439-0272.1996.tb02773.x. DOI: https://doi.org/10.1111/j.1439-0272.1996.tb02773.x
Aruffo A, Stamenkovic I, Melnick M, Underhill CB, Seed B. CD44 is the principal cell surface receptor for hyaluronate. Cell. 1990;61:1303–1313. doi.org/10.1016/0092-8674(90)90694-a. DOI: https://doi.org/10.1016/0092-8674(90)90694-A
Furnus CC, Valcarcel A, Dulout FN, Errecalde AL. The hyaluronic acid receptor (CD44) is expressed in bovine oocytes and early stage embryos. Theriogenology. 2003;60:1633–1644. doi.org/10.1016/s0093-691x(03)00116-x. DOI: https://doi.org/10.1016/S0093-691X(03)00116-X
Álvarez Rodriguez M, Vicente-Carillo A, Rodriguez-Martinez H. Hyaluronan improves neither the long-term storage nor the cryosurvival of liquid-stored CD44-bearing AI boar spermatozoa. Journalof Reproduction and Development. 2018;64(4):351–360. doi.org/10.1262/jrd.2017-141. DOI: https://doi.org/10.1262/jrd.2017-141
Bains R, Adeghe J, Carson RJ. Human sperm cells express CD44. Fertility and Sterility. 2002;78:307–312. doi.org/10.1016/s0015-0282(02)03230-2. DOI: https://doi.org/10.1016/S0015-0282(02)03230-2
Bergqvist AS, Yokoo M, Heldin P, Frendin J, Sato E, Rodríguez-Martínez H. Hyaluronan and its binding proteins in the epithelium and intraluminal fluid of the bovine oviduct. Zygote. 2005;19:207-218. doi.org/10.1017/s0967199405003266. DOI: https://doi.org/10.1017/S0967199405003266
Zhuo L, Kimata K. Cumulus oophorus extracellular matrix: its construction and regulation. Cell Structureand Function. 2001;26(4):189–196. doi.org/10.1247/csf.26.189. DOI: https://doi.org/10.1247/csf.26.189
Suzuki K, Eriksson B, Shimizu H, Nagai T, Rodríguez-Martinez H. Effect of hyaluronan on monospermic penetration of porcine oocytes fertilized in vitro. International Journal of Andrology. 2000;23:13–21. doi.org/10.1046/j.1365-2605.2000.t01-1-00198.x. DOI: https://doi.org/10.1046/j.1365-2605.2000.t01-1-00198.x
Myles DG, Primakoff P. Why did the sperm cross the cumulus? To get to the oocyte. Functions of the sperm surface proteins PH-20 and fertilin in arriving at, and fusing with, the egg. Biology of Reproduction. 1997;56(2):320–327. doi.org/10.1095/biolreprod56.2.320. DOI: https://doi.org/10.1095/biolreprod56.2.320
Seol DW, Joo SH, Kim YH, Song BS, Sim BW, Kim SU, et al. The efficacy of hyaluronic acid binding (HAB) in the treatment of male infertility: asystematic review of the titerature.DNA.2022;2:149–171. doi.org/10.3390/dna2030011. DOI: https://doi.org/10.3390/dna2030011
RashkiGhaleno L, RezazadehValojerdi M, Chehrazi M, SahraneshinSamani F, Salman Yazdi R. Hyaluronic Acid Binding Assay Is Highly Sensitive to Select Human Spermatozoa with Good Progressive Motility, Morphology, and Nuclear Maturity. Gynecologic and Obstetric Investigation. 2016;81(3):244–250. doi.org/10.1159/000439530. DOI: https://doi.org/10.1159/000439530
Huszar G, Jakab A, Sakkas D, Ozenci CC, Cayli S, Delpiano E, et al. Fertility testing and ICSI sperm selection by hyaluronic acid binding: clinical and genetic aspects. Reproductive Biomedicine Online. 2007;14(5):650–663. doi.org/10.1016/s1472-6483(10)61060-7. DOI: https://doi.org/10.1016/S1472-6483(10)61060-7
Signorelli J, Diaz ES, Morales P. Kinases, phosphatases and proteases during sperm capacitation. Cell and Tissue Research. 2012;349(3):765–782. doi.org/10.1007/s00441-012-1370-3. DOI: https://doi.org/10.1007/s00441-012-1370-3
Adeoya-Osiguwa SA, Fraser LR. Fertilization promoting peptide and adenosine, acting as first messengers, regulate cAMP production and consequent protein tyrosine phosphorylation in a capacitation-dependent manner. Molecular Reproduction and Development. 2000;57(4):384–392. doi.org/10.1002/1098-2795(200012)57:4<384::AID-MRD11>3.0.CO;2-U. DOI: https://doi.org/10.1002/1098-2795(200012)57:4<384::AID-MRD11>3.0.CO;2-U
Fraser LR, Adeoya-Osiguwa S, Baxendale RW, Mededovic S, Osiguwa OO. First messenger regulation of mammalian sperm function via adenylyl cyclase/cAMP. Journal of Reproduction and Development. 2005;51:37–46. doi.org/10.1262/jrd.51.37. DOI: https://doi.org/10.1262/jrd.51.37
Baxendale RW, Fraser LR. Evidence for multiple distinctly localized adenylyl cyclase isoforms in mammalian spermatozoa. Molecular Reproduction and Development. 2003; 66:181–189. doi.org/10.1002/mrd.10344. DOI: https://doi.org/10.1002/mrd.10344
Ramos-Espiritu L, Kleinboelting S, Navarrete FA, Alvau A, Visconti PE, Valsecchi F, et al. Discovery of LRE1 as a specific and allosteric inhibitor of soluble adenylyl cyclase. Nature Chemical Biology. 2016;12(10):838–844. doi.org/10.1038/nchembio.2151. DOI: https://doi.org/10.1038/nchembio.2151
Hafez ESE, Hafez B. Reproducción e inseminación artificial en animales. 7th edition. Distrito Federal, México: McGraw-Hill InteramericanaEditores; 2002.
Fernández S, Córdoba M. Hyaluronic acid as capacitation inductor: metabolic changes and membrane-associated adenylate cyclase regulation. Reproduction in Domestic Animals. 2014;49:941–946. doi.org/10.1111/rda.12410. DOI: https://doi.org/10.1111/rda.12410
Fernández S, Córdoba M. A membrane-associated adenylate cyclase modulates lactate dehydrogenase and creatine kinase activities required for bull sperm capacitation induced by hyaluronic acid. Animal Reproduction Science. 2017;179:80–87. doi.org/10.1016/j.anireprosci.2017.02.004. DOI: https://doi.org/10.1016/j.anireprosci.2017.02.004
Fernández S, Córdoba M. Hyaluronic acid-induced capacitation involves protein kinase C and tyrosine kinase activity modulation with a lower oxidative metabolism in cryopreserved bull sperm. Theriogenology. 2018;122:68–73. doi.org/10.1016/j.theriogenology.2018.09.005. DOI: https://doi.org/10.1016/j.theriogenology.2018.09.005
Córdoba M, Pintos LN, Beconi MT. Heparin and quercetin generate differential metabolic pathways that involve aminotransferases and LDH-X dehydrogenase in cryopreserved bovine spermatozoa. Theriogenology. 2007;67:648–654. doi.org/10.1016/j.theriogenology.2006.09.041. DOI: https://doi.org/10.1016/j.theriogenology.2006.09.041
Córdoba M, Pintos L, Beconi MT. Variations in creatine kinase activity and reactive oxygen species levels are involved in capacitation of bovine spermatozoa. Andrologia. 2008;40:370–376. doi.org/10.1111/j.1439-0272.2008.00871.x. DOI: https://doi.org/10.1111/j.1439-0272.2008.00871.x
Córdoba M, Mora N, Beconi MT. Respiratory burst and NAD(P)H oxidase activity are involved in capacitation of cryopreserved bovine spermatozoa. Theriogenology. 2006;65:882–892. doi.org/10.1016/j.theriogenology.2005.06.015. DOI: https://doi.org/10.1016/j.theriogenology.2005.06.015
Schober D, Aurich C, Nohl H, Gille L. Influence of cryopreservation on mitochondrial functions in equine spermatozoa. Theriogenology. 2007;68:745–754. doi.org/10.1016/j.theriogenology.2007.06.004. DOI: https://doi.org/10.1016/j.theriogenology.2007.06.004
Kato Y, Nagao Y. Changes in sperm motility and capacitation induce chromosomal aberration of the bovine embryo following intracytoplasmic sperm injection. PlosOne. 2015;(6):e0129285. doi.org/10.1371/journal.pone.0129285. DOI: https://doi.org/10.1371/journal.pone.0129285
Contri A, Valorz C, Faustini M, Wegher L, Carluccio A. Effect of semen preparation on casa motility results in cryopreserved bull spermatozoa. Theriogenology. 2010;74(3):424–435. doi.org/10.1016/j.theriogenology.2010.02.025. DOI: https://doi.org/10.1016/j.theriogenology.2010.02.025
Kim EY, Noh EH, Nob EJ, Park MJ, Park HY, Lee DS, et al. Effect of glycosaminoglycans on in vitro fertilizing ability and in vitro developmental potential of bovine embryos. Asian-Australasian Journal of Animal Sciences. 2013;26:178–188. doi.org/10.5713/ajas.2012.12406. DOI: https://doi.org/10.5713/ajas.2012.12406
Sarıözkan S, Bucak MN, Tuncer PB, Büyükleblebici S, Eken A, Akay C. Influence of fetuin and hyaluronan on the post-thaw quality and fertilizing ability of Holstein bull semen. Cryobiology. 2015;71:119–124. doi.org/10.1016/j.cryobiol.2015.04.011. DOI: https://doi.org/10.1016/j.cryobiol.2015.04.011
Cetica PD, Dalvit GC, Beconi MT. Study of evaluation criteria used for in vitro bovine oocyte selection and maturation. Biocell. 1999;23(2):125–133.
Morado S, Cetica P, Beconi M, Thompson J, Dalvit G. Reactive oxygen species production and redox state in parthenogenetic and sperm mediated bovine oocyte activation. Reproduction. 2013;145:471–478. doi.org/10.1530/REP-13-0017. DOI: https://doi.org/10.1530/REP-13-0017
Fouladi-Nashta AA, Raheem KA, Marei WF, Ghafari F, Hartshorne GM. Regulation and roles of the hyaluronan system in mammalian reproduction. Reproduction. 2017;153(2):R43–R58. doi.org/10.1530/REP-16-0240. DOI: https://doi.org/10.1530/REP-16-0240
Gómez-Torres MJ, Hernández-Falcó M, López-Botella A, Huerta-Retamal N, Sáez-Espinosa P.IZUMO1 receptor localization during hyaluronic acid selection in human spermatozoa. Biomedicines. 2023;11(11):2872. doi.org/10.3390/biomedicines11112872. DOI: https://doi.org/10.3390/biomedicines11112872
Liaudat AC, Blois D, Capella V, Morilla G, Rivero R, Barbero C, et al. Bull sperm selection by attachment to hyaluronic acid semi-interpenetrated hydrogels. Reproduction in Domestic Animals. 2021;57(2):228–232. doi.org/10.1111/rda.13943. DOI: https://doi.org/10.1111/rda.13943
Erberelli RF, Salgado RM, Pereira DH, Wolff P. Hyaluronan-binding system for sperm selection enhances pregnancy rates in ICSI cycles associated with male factor infertility. JBRA Assisted Reproduction. 2017;21(1):2–6. doi.org/10.5935/1518-0557.20170002. DOI: https://doi.org/10.5935/1518-0557.20170002
Colleoni S, LagutinaI, Lazzari G, Rodriguez-Martínez H, Galli C, Morrell J. New methods for selecting stallion spermatozoa for assisted reproduction. Journalof Equine Veterinary Science. 2011;31:536–541. doi.org/10.1016/j.jevs.2011.03.009. DOI: https://doi.org/10.1016/j.jevs.2011.03.009
West R, Coomarasamy A, Frew L, Hutton R, Kirkman-Brown J, Lawlor M, et al. Sperm selection with hyaluronic acid improved live birth outcomes among older couples and was connected to sperm DNA quality, potentially affecting all treatment outcomes. Human Reproduction. 2022;37(6):1106–1125. doi.org/10.1093/humrep/deac058.. DOI: https://doi.org/10.1093/humrep/deac058
Gutnisky C, Dalvit G, Pintos L, Thompson J, Beconi M, Cetica P. Influence of hyaluronic acid synthesis and cumulus mucification on bovine oocyte in vitromaduration, fertilization and embryo development. Reproduction Fertility and Development. 2007;19:488–497. doi.org/10.1071/rd06134. DOI: https://doi.org/10.1071/RD06134
Kothapalli D, Flowers J, Xu T, Puré E, Assoian RK. Differential activation of ERK and Rac mediates the proliferative and anti-proliferative effects of hyaluronan and CD44. Journal of Biological Chemistry. 2008;283(46):31823–31829. doi.org/10.1074/jbc.M802934200. DOI: https://doi.org/10.1074/jbc.M802934200
Puré E, Assoian RK. Rheostatic signaling by CD44 and hyaluronan. Cellular Signalling. 2009;(5):651–655. doi.org/10.1016/j.cellsig.2009.01.024. DOI: https://doi.org/10.1016/j.cellsig.2009.01.024
Wertheimer E, Krapf D, de la Vega-Beltran JL, Sánchez-Cárdenas C, Navarrete F, Haddad D, et al. Compartmentalization of distinct cAMP signaling pathways in mammalian sperm. Journal of Biological Chemistry. 2013;288(49):35307–35320. doi.org/10.1074/jbc.M113.489476. DOI: https://doi.org/10.1074/jbc.M113.489476
Fernández S, Morado S, Cetica P, Córdoba M. Hyaluronic acid capacitation induces intracellular signals modulated by membrane-associated adenylate cyclase and tyrosine kinase involved in bovine in vitro fertilization. Theriogenology. 2020;148:174–179. doi.org/10.1016/j.theriogenology.2020.02.033. DOI: https://doi.org/10.1016/j.theriogenology.2020.02.033
Garrett LJA, Revell SG, Leese HJ. Adenosine triphosphate production by bovine spermatozoa and its relationship to semen fertilizing ability. Journal of Andrology. 2008;29:449–458. doi.org/10.2164/jandrol.107.003533. DOI: https://doi.org/10.2164/jandrol.107.003533
Binet MT, Doyle CJ, Williamson JE, Schlegel P. Use of JC-1 to assess mitochondrial membrane potential in sea urchin sperm. Journal of Experimental Marine Biology and Ecology. 2014;452:91–100. doi.org/10.1016/j.jembe.2013.12.008. DOI: https://doi.org/10.1016/j.jembe.2013.12.008
Nichi M, Rijsselaere T, Losano J, Angrimani D, Kawai G, Goovaerts I, et al. Evaluation of epididymis storage temperature and cryopreservation conditions for improved mitochondrial membrane potential, membrane integrity, sperm motility and in vitro fertilization in bovine epididymal sperm. Reproduction in Domestic Animals. 2017;52:257–263. doi.org/10.1111/rda.12888. DOI: https://doi.org/10.1111/rda.12888
BuffoneMG, Wertheimer EV, Visconti PE, Krapf D. Central role of soluble adenylyl cyclase and cAMP in sperm physiology. Biochimica et BiophysicaActa. 2014;1842(12 Pt B):2610–2620. doi.org/10.1016/j.bbadis.2014.07.013. DOI: https://doi.org/10.1016/j.bbadis.2014.07.013
Hess KC, Jones BH, Marquez B, Chen Y, Ord TS, Kamenetsky M, et al. The "soluble" adenylyl cyclase in sperm mediates multiple signaling events required for fertilization. Developmental Cell. 2005;9(2):249–259. doi.org/10.1016/j.devcel.2005.06.007. DOI: https://doi.org/10.1016/j.devcel.2005.06.007
Xie F, Garcia MA, Carlson AE, Schuh SM, Babcock DF, Jaiswal BS, et al. Soluble adenylyl cyclase (sAC) is indispensable for sperm function and fertilization. Developmental Biology. 2006;296(2):353–362. doi.org/10.1016/j.ydbio.2006.05.038. DOI: https://doi.org/10.1016/j.ydbio.2006.05.038
Livera G, Xie F, Garcia MA, Jaiswal B, Chen J, Law E, et al. Inactivation of the mouse adenylyl cyclase 3 gene disrupts male fertility and spermatozoon function. Molecular Endocrinology. 2005;19(5):1277–1290. doi.org/10.1210/me.2004-0318. DOI: https://doi.org/10.1210/me.2004-0318
Leclerc P, de Lamirande E, Gagnon C. Regulation of protein-tyrosine phosphorylation and human sperm capacitation by reactive oxygen derivatives. Free Radical Biology and Medicine. 1997;22:643–656. doi.org/10.1016/s0891-5849(96)00379-6. DOI: https://doi.org/10.1016/S0891-5849(96)00379-6
Monks NJ, Stein DM, Fraser LR. Adenylate cyclase activity of mouse sperm during capacitation in vitro: effect of calcium and a GTP analogue. International Journal of Andrology. 1986;9(1):67–76. doi.org/10.1111/j.1365-2605.1986.tb00868.x. DOI: https://doi.org/10.1111/j.1365-2605.1986.tb00868.x
Balakier H, Kuznyetsova I, Librach CL. The impact of hyaluronan-enriched culture medium and intrauterine infusion of human chorionic gonadotropin on clinical outcomes in blastocyst transfer cycles. Systems Biology in Reproductive Medicine. 2020;66(2):79–88. doi.org/10.1080/19396368.2020.1727995. DOI: https://doi.org/10.1080/19396368.2020.1727995
Wang F, Chang HM, Yi Y, Li H, Leung PCK. TGF-β1 promotes hyaluronan synthesis by upregulating hyaluronan synthase 2 expression in human granulosa-lutein cells. Cell Signalling. 2019 63:109392. doi.org/10.1016/j.cellsig.2019.109392. DOI: https://doi.org/10.1016/j.cellsig.2019.109392
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