Comparative Investigation of the Mechanisms of Calcium Response in Human and Murine Spermatozoa

Мұқаба

Дәйексөз келтіру

Толық мәтін

Ашық рұқсат Ашық рұқсат
Рұқсат жабық Рұқсат берілді
Рұқсат жабық Тек жазылушылар үшін

Аннотация

Calcium signaling is a principal method of signal transduction in cells of non-excitable tissues. In both mouse and human sperm, it can be induced in response to progesterone, manifesting as oscillations or single peaks and followed by the acrosomal reaction. However, the molecular mechanisms of progesterone activation may vary between species. In this study, we aim to compare the calcium signaling mechanisms in human and mouse spermatozoa. We investigated the calcium response in mouse sperm activated by progesterone. We employed spectrofluorometry to quantify the rise in calcium concentration in response to progesterone in Fura-2 loaded mouse sperm cells in suspension. Our experiments demonstrated that mouse sperm cells respond to 50 μM progesterone with a peak 120 ± 35 s wide and 0.8 ± 0.3 μM high. Based on literature data, a scheme for the induction of calcium signaling was constructed, suggesting an intermediate stage with the synthesis of a certain prostanoid (possibly PGE2) and activation of mouse sperm by this prostanoid through a G-protein-coupled receptor. Based on the obtained reaction scheme, two computational models were developed: a point model and a three-dimensional model. As with human sperm, the point model provided only a qualitative description of calcium responses, whereas the three-dimensional model produced the shape of the calcium peak and the frequency of calcium oscillations in response to progesterone that were similar to the experimentally obtained values. Using in silico analysis, it was shown that in mouse sperm, the spatial distribution of signaling enzymes regulates the type and form of the calcium response. We conclude that the presence of time delays due to the diffusion and spatial distribution of calcium signaling enzymes regulates the calcium response in both human and mouse sperm.

Толық мәтін

Рұқсат жабық

Авторлар туралы

J. Korobkina

Center for Theoretical Problems of Physico-Chemical Pharmacology, Russian Academy of Sciences

Хат алмасуға жауапты Автор.
Email: juliajessika@gmail.com
Ресей, Moscow, 109029

M. Panteleev

Center for Theoretical Problems of Physico-Chemical Pharmacology, Russian Academy of Sciences, Lomonosov Moscow State University
Dmitry Rogachev National Medical Research Centеr of Pediatric Hematology, Oncology and Immunology

Email: juliajessika@gmail.com
Ресей, Moscow, 109029; Moscow, 119991; Moscow, 119991

A. Sveshnikova

Center for Theoretical Problems of Physico-Chemical Pharmacology, Russian Academy of Sciences, Lomonosov Moscow State University
Dmitry Rogachev National Medical Research Centеr of Pediatric Hematology, Oncology and Immunology

Email: juliajessika@gmail.com
Ресей, Moscow, 109029; Moscow, 119991; Moscow, 119991

Әдебиет тізімі

  1. Ottolini M., Sonkusare S.K. 2021. The calcium signaling mechanisms in arterial smooth muscle and endothelial cells. Compr. Physiol. 11 (2), 1831–1869.
  2. Kalyanasundaram A., Li N., Hansen B.J., Zhao J., Fedorov V.V. 2019. Canine and human sinoatrial node: Differences and similarities in the structure, function, molecular profiles, and arrhythmia. J. Vet. Cardiol. 22, 2–19.
  3. Suarez S.S., Ho H.C. 2003. Hyperactivation of mammalian sperm. Cell Mol. Biol. (Noisy-le-grand). 49 (3), 351–356.
  4. Sanchez-Cardenas C., Servin-Vences M.R., Jose O., Trevino C.L., Hernandez-Cruz A., Darszon A. 2014. Acrosome reaction and Ca²⁺ imaging in single human spermatozoa: New regulatory roles of [Ca²⁺]i. Biol. Reprod. 91 (3), 67.
  5. Taraborrelli S. 2015. Physiology, production and action of progesterone. Acta Obstet. Gynecol. Scand. 94 Suppl 161, 8–16.
  6. Miller M.R., Mannowetz N., Iavarone A.T., Safavi R., Gracheva E.O., Smith J.F., Hill R.Z., Bautista D.M., Kirichok Y., Lishko P.V. 2016. Unconventional endocannabinoid signaling governs sperm activation via the sex hormone progesterone. Science. 352 (6285), 555–559.
  7. Nakamura Y., Fukami K. 2009. Roles of phospholipase C isozymes in organogenesis and embryonic development. Physiology (Bethesda). 24, 332–341.
  8. Kim Y.H., Park T.J., Lee Y.H., Baek K.J., Suh P.G., Ryu S.H., Kim K.T. 1999. Phospholipase C-delta1 is activated by capacitative calcium entry that follows phospholipase C-beta activation upon bradykinin stimulation. J. Biol. Chem. 274 (37), 26127–26134.
  9. Finkelstein M., Etkovitz N., Breitbart H. 2020. Ca²⁺ signaling in mammalian spermatozoa. Mol. Cell Endocrinol. 516, 110953.
  10. Alasmari W., Barratt C.L., Publicover S.J., Whalley K.M., Foster E., Kay V., Martins da Silva S., Oxenham S.K. 2013. The clinical significance of calcium-signalling pathways mediating human sperm hyperactivation. Hum. Reprod. 28 (4), 866–876.
  11. Schuh K., Cartwright E.J., Jankevics E., Bundschu K., Liebermann J., Williams J.C., Armesilla A.L., Emerson M., Oceandy D., Knobeloch K.P., Neyses L. 2004. Plasma membrane Ca²⁺ ATPase 4 is required for sperm motility and male fertility. J. Biol. Chem. 279 (27), 28220–28226.
  12. Harper C., Wootton L., Michelangeli F., Lefievre L., Barratt C., Publicover S. 2005. Secretory pathway Ca²⁺-ATPase (SPCA1) Ca²⁺ pumps, not SERCAs, regulate complex [Ca²⁺]i signals in human spermatozoa. J. Cell Sci. 118 (Pt 8), 1673–1685.
  13. Si Y., Olds-Clarke P. 2000. Evidence for the involvement of calmodulin in mouse sperm capacitation. Biol. Reprod. 62 (5), 1231–1239.
  14. Nakamura M., Oshio S., Tamura A., Okinaga S., Arai K. 1992. Antisera to calreticulin inhibits sperm motility in mice. Biochem. Biophys. Res. Commun. 186 (2), 984–990.
  15. Korobkin J., Balabin F.A., Yakovenko S.A., Simonenko E.Y., Sveshnikova A.N. 2021. Occurrence of calcium oscillations in human spermatozoa is based on spatial signaling enzymes distribution. Int. J. Mol. Sci. 22 (15), 8018.
  16. Rennhack A., Schiffer C., Brenker C., Fridman D., Nitao E.T., Cheng Y.M., Tamburrino L., Balbach M., Stolting G., Berger T.K., Kierzek M., Alvarez L., Wach-ten D., Zeng X.H., Baldi E., Publicover S.J., Kaupp U.B., Strunker T. 2018. A novel cross-species inhibitor to study the function of CatSper Ca²⁺ channels in sperm. Br J Pharmacol. 175 (15), 3144–3161.
  17. Herrick S.B., Schweissinger D.L., Kim S.W., Bayan K.R., Mann S., Cardullo R.A. 2005. The acrosomal vesicle of mouse sperm is a calcium store. J. Cell Physiol. 202 (3), 663–671.
  18. Pietrobon E.O., Soria M., Dominguez L.A., Monclus Mde L., Fornes M.W. 2005. Simultaneous activation of PLA2 and PLC are required to promote acrosomal reaction stimulated by progesterone via G-proteins. Mol. Reprod. Dev. 70 (1), 58–63.
  19. Herrero M.B., Cebral E., Franchi A., Motta A., Gimeno M.F. 1998. Progesterone enhances prostaglandin E2 production via interaction with nitric oxide in the mouse acrosome reaction. Biochem. Biophys. Res. Commun. 252 (2), 324–328.
  20. Joyce C.L., Nuzzo N.A., Wilson L., Jr., Zaneveld L.J. 1987. Evidence for a role of cyclooxygenase (prostaglandin synthetase) and prostaglandins in the sperm acrosome reaction and fertilization. J. Androl. 8 (2), 74–82.
  21. Lishko P.V., Botchkina I.L., Kirichok Y. 2011. Progesterone activates the principal Ca²⁺ channel of human sperm. Nature. 471 (7338), 387–391.
  22. Breyer R.M., Bagdassarian C.K., Myers S.A., Breyer M.D. 2001. Prostanoid receptors: subtypes and signaling. Annu. Rev. Pharmacol. Toxicol. 41, 661–690.
  23. Gao D.D., Lan C.F., Cao X.N., Chen L., Lei T.L., Peng L., Xu J.W., Qiu Z.E., Wang L.L., Sun Q., Huang Z.Y., Zhu Y.X., Zhou W.L., Zhang Y.L. 2022. G protein-coupled estrogen receptor promotes acrosome reaction via regulation of Ca²⁺ signaling in mouse spermdagger. Biol. Reprod. 107 (4), 1026–1034.
  24. Kawai T., Miyata H., Nakanishi H., Sakata S., Morioka S., Sasaki J., Watanabe M., Sakimura K., Fujimoto T., Sasaki T., Ikawa M., Okamura Y. 2019. Polarized PtdIns(4,5) P(2) distribution mediated by a voltage-sensing phosphatase (VSP) regulates sperm motility. Proc. Natl. Acad. Sci. USA. 116 (51), 26020–26028.
  25. Choi D., Lee E., Hwang S., Jun K., Kim D., Yoon B.K., Shin H.S., Lee J.H. 2001. The biological significance of phospholipase C beta 1 gene mutation in mouse sperm in the acrosome reaction, fertilization, and embryo development. J. Assist. Reprod. Genet. 18 (5), 305–310.
  26. Fukami K., Yoshida M., Inoue T., Kurokawa M., Fissore R.A., Yoshida N., Mikoshiba K., Takenawa T. 2003. Phospholipase Cdelta4 is required for Ca²⁺ mobilization essential for acrosome reaction in sperm. J. Cell Biol. 161 (1), 79–88.
  27. Ohlmann P., Hechler B., Cazenave J.P., Gachet C. 2004. Measurement and manipulation of [Ca²⁺]i in suspensions of platelets and cell cultures. Methods Mol. Biol. 273, 229–250.
  28. Mirabito Colafella K.M., Neuman R.I., Visser W., Danser A.H.J., Versmissen J. 2020. Aspirin for the prevention and treatment of pre-eclampsia: A matter of COX-1 and/or COX-2 inhibition? Basic Clin. Pharmacol. Toxicol. 127 (2), 132–141.
  29. Grynkiewicz G., Poenie M., Tsien R.Y. 1985. A new generation of Ca²⁺ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260 (6), 3440–3450.
  30. Bergmann F.T., Hoops S., Klahn B., Kummer U., Mendes P., Pahle J., Sahle S. 2017. COPASI and its applications in biotechnology. J. Biotechnol. 261, 215–220.
  31. Hoops S., Sahle S., Gauges R., Lee C., Pahle J., Simus N., Singhal M., Xu L., Mendes P., Kummer U. 2006. COPASI-a COmplex PAthway SImulator. Bioinformatics. 22 (24), 3067–3074.
  32. Moraru, II, Schaff J.C., Slepchenko B.M., Blinov M.L., Morgan F., Lakshminarayana A., Gao F., Li Y., Loew L.M. 2008. Virtual Cell modelling and simulation software environment. IET Syst. Biol. 2 (5), 352–362.
  33. Marhl M., Schuster S., Brumen M., Heinrich R. 1997. Modeling the interrelations between the calcium oscillations and ER membrane potential oscillations. Biophys. Chem. 63 (2–3), 221–239.
  34. Katanaev V.L., Chornomorets M. 2007. Kinetic diversity in G-protein-coupled receptor signalling. Biochem. J. 401 (2), 485–495.
  35. Romarowski A., Sanchez-Cardenas C., Ramirez-Gomez H.V., Puga Molina Ldel C., Trevino C.L., Hernandez-Cruz A., Darszon A., Buffone M.G. 2016. A specific transitory increase in intracellular calcium induced by progesterone promotes acrosomal exocytosis in mouse sperm. Biol. Reprod. 94 (3), 63.
  36. Klonowski W. 1983. Simplifying principles for chemical and enzyme reaction kinetics. Biophys. Chem. 18 (2), 73–87.
  37. Lopez-Gonzalez I., Torres-Rodriguez P., Sanchez-Carranza O., Solis-Lopez A., Santi C.M., Darszon A., Trevino C.L. 2014. Membrane hyperpolarization during human sperm capacitation. Mol. Hum. Reprod. 20 (7), 619–629.
  38. Smith D., Gaffney E., Blake J., Kirkman-Brown J. 2009. Human sperm accumulation near surfaces: a simulation study. J. Fluid Mechanics. 621, 289–320.
  39. Cummins J.M., Woodall P.F. 1985. On mammalian sperm dimensions. J. Reprod. Fertil. 75 (1), 153–175.
  40. Simons J., Fauci L. 2018. A model for the acrosome reaction in mammalian sperm. Bull Math Biol. 80 (9), 2481–2501.
  41. Kirkman-Brown J.C., Barratt C.L., Publicover S.J. 2004. Slow calcium oscillations in human spermatozoa. Biochem. J. 378 (Pt 3), 827–832.
  42. Lechleiter J., Girard S., Clapham D., Peralta E. 1991. Subcellular patterns of calcium release determined by G protein-specific residues of muscarinic receptors. Nature. 350 (6318), 505–508.
  43. Vera-Siguenza E., Pages N., Rugis J., Yule D.I., Sneyd J. 2019. A mathematical model of fluid transport in an accurate reconstruction of parotid acinar cells. Bull. Math. Biol. 81 (3), 699–721.
  44. Bell M., Bartol T., Sejnowski T., Rangamani P. 2019. Dendritic spine geometry and spine apparatus organization govern the spatiotemporal dynamics of calcium. J. Gen. Physiol. 151 (8), 1017–1034.
  45. Zador A., Koch C. 1994. Linearized models of calcium dynamics: formal equivalence to the cable equation. J. Neurosci. 14 (8), 4705–4715.
  46. Weber K., Waletzky A., Fendl D., Ordonez P., Takawale P., Hein F., Riedel W., Konig A., Kunze M., Leoni A.L., Rivera J., Quirici R., Romano I., Paepke S., Okazaki Y., Hardisty J.F. 2014. New method for sperm evaluation by 3-dimensional laser scanning microscopy in different laboratory animal species. Int. J. Toxicol. 33 (5), 353–361.
  47. Sunanda P., Panda B., Dash C., Padhy R.N., Routray P. 2018. An illustration of human sperm morphology and their functional ability among different group of subfertile males. Andrology. 6 (5), 680–689.
  48. Albrechtova J., Albrecht T., Dureje L., Pallazola V.A., Pialek J. 2014. Sperm morphology in two house mouse subspecies: Do wild-derived strains and wild mice tell the same story? PLoS One. 9 (12), e115669.
  49. Yeung C.H., Anapolski M., Cooper T.G. 2002. Measurement of volume changes in mouse spermatozoa using an electronic sizing analyzer and a flow cytometer: validation and application to an infertile mouse model. J. Androl. 23 (4), 522–528.
  50. Dickinson G.D., Ellefsen K.L., Dawson S.P., Pearson J.E., Parker I. 2016. Hindered cytoplasmic diffusion of inositol trisphosphate restricts its cellular range of action. Sci. Signal. 9 (453), ra108.
  51. Samtleben S., Jaepel J., Fecher C., Andreska T., Rehberg M., Blum R. 2013. Direct imaging of ER calcium with targeted-esterase induced dye loading (TED). J. Vis. Exp. (75), e50317.
  52. Li Y.X., Rinzel J. 1994. Equations for InsP3 receptor-mediated [Ca²⁺]i oscillations derived from a detailed kinetic model: A Hodgkin-Huxley like formalism. J. Theor. Biol. 166 (4), 461–473.
  53. De Young G.W., Keizer J. 1992. A single-pool inositol 1,4,5-trisphosphate-receptor-based model for agonist-stimulated oscillations in Ca²⁺ concentration. Proc. Natl. Acad. Sci. USA. 89 (20), 9895–9899.
  54. Cai X., Li X., Qi H., Wei F., Chen J., Shuai J. 2016. Comparison of gating dynamics of different IP(3) R channels with immune algorithm searching for channel parameter distributions. Phys. Biol. 13 (5), 056005.
  55. Li L.F., Xiang C., Zhu Y.B., Qin K.R. 2014. Modeling of progesterone-induced intracellular calcium signaling in human spermatozoa. J. Theor. Biol. 351, 58–66.
  56. Vais H., Foskett J.K., Mak D.O. 2010. Unitary Ca²⁺ current through recombinant type 3 InsP3 receptor channels under physiological ionic conditions. J. Gen. Physiol. 136 (6), 687–700.
  57. Olson S.D., Suarez S.S., Fauci L.J. 2010. A model of CatSper channel mediated calcium dynamics in mammalian spermatozoa. Bull. Math. Biol. 72 (8), 1925–1946.
  58. Kadamur G., Ross E.M. 2013. Mammalian phospholipase C. Annu. Rev. Physiol. 75, 127–154.
  59. Wang M., Weiss M., Simonovic M., Haertinger G., Schrimpf S.P., Hengartner M.O., von Mering C. 2012. PaxDb, a database of protein abundance averages across all three domains of life. Mol. Cell. Proteomics. 11 (8), 492–500.
  60. De Pitta M., Goldberg M., Volman V., Berry H., Ben-Jacob E. 2009. Glutamate regulation of calcium and IP3 oscillating and pulsating dynamics in astrocytes. J. Biol. Phys. 35 (4), 383–411.
  61. Sims C.E., Allbritton N.L. 1998. Metabolism of inositol 1,4,5-trisphosphate and inositol 1,3,4,5-tetrakisphosphate by the oocytes of Xenopus laevis. J. Biol. Chem. 273 (7), 4052–4058.
  62. Baksh S., Michalak M. 1991. Expression of calreticulin in Escherichia coli and identification of its Ca²⁺ binding domains. J. Biol. Chem. 266 (32), 21458–21465.
  63. Means S., Smith A.J., Shepherd J., Shadid J., Fowler J., Wojcikiewicz R.J., Mazel T., Smith G.D., Wilson B.S. 2006. Reaction diffusion modeling of calcium dynamics with realistic ER geometry. Biophys. J. 91 (2), 537–557.
  64. Michalak M., Corbett E.F., Mesaeli N., Nakamura K., Opas M. 1999. Calreticulin: One protein, one gene, many functions. Biochem. J. 344 (Pt 2), 281–292.
  65. Hoffman L., Chandrasekar A., Wang X., Putkey J.A., Waxham M.N. 2014. Neurogranin alters the structure and calcium binding properties of calmodulin. J. Biol Chem. 289 (21), 14644–14655.
  66. Wennemuth G., Babcock D.F., Hille B. 2003. Calcium clearance mechanisms of mouse sperm. J. Gen. Physiol. 122 (1), 115–128.
  67. Lytton J., Westlin M., Burk S.E., Shull G.E., MacLennan D.H. 1992. Functional comparisons between isoforms of the sarcoplasmic or endoplasmic reticulum family of calcium pumps. J. Biol. Chem. 267 (20), 14483–14489.
  68. Vila A., Rosengarth A., Piomelli D., Cravatt B., Marnett L.J. 2007. Hydrolysis of prostaglandin glycerol esters by the endocannabinoid-hydrolyzing enzymes, monoacylglycerol lipase and fatty acid amide hydrolase. Biochemistry. 46 (33), 9578–9585.
  69. Tyukhtenko S., Karageorgos I., Rajarshi G., Zvonok N., Pavlopoulos S., Janero D.R., Makriyannis A. 2016. Specific inter-residue interactions as determinants of human monoacylglycerol lipase catalytic competency: A role for global conformational changes. J. Biol. Chem. 291 (6), 2556–2565.
  70. Liu Y., Roth J.P. 2016. A revised mechanism for human cyclooxygenase-2. J. Biol. Chem. 291 (2), 948–958.
  71. Hwa J., Martin K. 2017. The Eicosanoids: Prostaglandins, Thromboxanes, Leukotrienes, & Related Compounds. In: Basic & Clinical Pharmacology. 14th ed. Ed. Katzung B.G. New York: McGraw-Hill Education.
  72. Marshall F.H., Patel K., Lundstrom K., Camacho J., Foord S.M., Lee M.G. 1997. Characterization of [3H]‐prostaglandin E2 binding to prostaglandin EP4 receptors expressed with Semliki Forest virus. Br.J. Pharmacol. 121 (8), 1673–1678.

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