Electrophysiology of Human Gametes: A Systematic Review

Purpose Oocytes and spermatozoa are electrogenic cells with the ability to respond to electrical stimuli and modulate their electrical properties accordingly. Determination of the ionic events during the gamete maturation helps to design suitable culture media for gametes in assisted reproductive technology (ART). The present systematic review focuses on the electrophysiology of human gametes during different stages of maturation and also during fertilization. Materials and Methods The reports published in the English language between January 2000 and July 2021 were extracted from various electronic scientific databases following the PRISMA checklist using specific MeSH keywords. Results Subsequent to the screening process with defined inclusion and exclusion criteria, 60 articles have been included in this review. Among them, 11 articles were directly related to the electrophysiology of human oocytes and 49 physiology department to the electrophysiology of human spermatozoa. Conclusions Gametes generate electrical currents by ionic exchange, particularly Na+, K+, Cl-, H+, Zn2+, Cu2+, Se2+, Mg2+, HCO3-, and Ca2+ through specific ion channels in different stages of gamete maturation. The ionic concentrations, pH, and other physicochemical variables are modulated during the gametogenesis, maturation, activation, and the fertilization process following gamete function and metabolism. The electrical properties of human gametes change during different stages of maturation. Although it is demonstrated that the electrical properties are significant regulators of cell signaling and are fundamental to gamete maturation and fertilization, their exact roles in these processes are still poorly understood. Further research is required to unveil the intricate electrophysiological processes of human gamete maturation.

[1]  T. DeCoursey,et al.  Voltage-gated proton channels exist in the plasma membrane of human oocytes. , 2019, Human reproduction.

[2]  A. Agarwal,et al.  Reactive oxygen species and male reproductive hormones , 2018, Reproductive Biology and Endocrinology.

[3]  A. Agarwal,et al.  The Effects of Exposure to Low Frequency Electromagnetic Fields on Male Fertility. , 2018, Alternative therapies in health and medicine.

[4]  E. Baldi,et al.  A novel cross‐species inhibitor to study the function of CatSper Ca2+ channels in sperm , 2018, British journal of pharmacology.

[5]  W. D. De Vos,et al.  Strontium fails to induce Ca2+ release and activation in human oocytes despite the presence of functional TRPV3 channels , 2018, Human reproduction open.

[6]  M. Spehr,et al.  TRPV4 is the temperature-sensitive ion channel of human sperm , 2018, bioRxiv.

[7]  Y. Ye,et al.  Endothelin-1 promotes human germinal vesicle-stage oocyte maturation by downregulating connexin-26 expression in cumulus cells , 2018, Molecular human reproduction.

[8]  A. Gallo Toxicity of marine pollutants on the ascidian oocyte physiology: an electrophysiological approach , 2017, Zygote.

[9]  U. Kaupp,et al.  Photocontrol of the Hv1 Proton Channel. , 2017, ACS chemical biology.

[10]  Sean G Brown,et al.  Complex CatSper-dependent and independent [Ca2+]i signalling in human spermatozoa induced by follicular fluid , 2017, Human reproduction.

[11]  S. W. Lestari,et al.  Sperm Na+, K+-ATPase α4 and plasma membrane Ca2+-ATPase (PMCA) 4 regulation in asthenozoospermia , 2017, Systems biology in reproductive medicine.

[12]  N. Nikoloff,et al.  The copper transporter (SLC31A1/CTR1) is expressed in bovine spermatozoa and oocytes: Copper in IVF medium improves sperm quality. , 2017, Theriogenology.

[13]  Melissa R. Miller,et al.  Regulation of the sperm calcium channel CatSper by endogenous steroids and plant triterpenoids , 2017, Proceedings of the National Academy of Sciences.

[14]  L. Salkoff,et al.  A genetic variant of the sperm-specific SLO3 K+ channel has altered pH and Ca2+ sensitivities , 2017, The Journal of Biological Chemistry.

[15]  W. Bönigk,et al.  Post‐translational cleavage of Hv1 in human sperm tunes pH‐ and voltage‐dependent gating , 2017, The Journal of physiology.

[16]  P. Parsons,et al.  Associations between IVF outcomes and essential trace elements measured in follicular fluid and urine: a pilot study , 2017, Journal of Assisted Reproduction and Genetics.

[17]  T. Narender,et al.  Mitochondrial membrane potential (MMP) regulates sperm motility , 2016, In Vitro Cellular & Developmental Biology - Animal.

[18]  Sean G Brown,et al.  Depolarization of sperm membrane potential is a common feature of men with subfertility and is associated with low fertilization rate at IVF , 2016, Human reproduction.

[19]  Andjelka N. Hedrih,et al.  The effect of friction and impact angle on the spermatozoa-oocyte local contact dynamics. , 2016, Journal of theoretical biology.

[20]  A. Jovanovic,et al.  A spontaneous increase in intracellular Ca2+ in metaphase II human oocytes in vitro can be prevented by drugs targeting ATP-sensitive K+ channels , 2015, Human reproduction.

[21]  Melissa R. Miller,et al.  The Fungal Sexual Pheromone Sirenin Activates the Human CatSper Channel Complex , 2015, ACS chemical biology.

[22]  D. Armstrong,et al.  CaV3.2 T-type channels mediate Ca2+ entry during oocyte maturation and following fertilization , 2015, Journal of Cell Science.

[23]  P. Martin-DeLeon,et al.  Plasma membrane Ca2+-ATPase 4: interaction with constitutive nitric oxide synthases in human sperm and prostasomes which carry Ca2+/CaM-dependent serine kinase. , 2015, Molecular human reproduction.

[24]  Melissa R. Miller,et al.  Specific loss of CatSper function is sufficient to compromise fertilizing capacity of human spermatozoa , 2015, Human reproduction.

[25]  R. Krisher,et al.  The beneficial effects of reduced magnesium during the oocyte-to-embryo transition are conserved in mice, domestic cats and humans. , 2015, Reproduction, fertility, and development.

[26]  A. Darszon,et al.  Membrane hyperpolarization during human sperm capacitation. , 2014, Molecular human reproduction.

[27]  W. Bönigk,et al.  The Ca2+-activated K+ current of human sperm is mediated by Slo3 , 2014, eLife.

[28]  P. Vangheluwe,et al.  Regulation of endoplasmic reticulum Ca2+ oscillations in mammalian eggs , 2014, Development.

[29]  James F. Smith,et al.  Slo1 is the principal potassium channel of human spermatozoa , 2013, eLife.

[30]  J. Irazusta,et al.  The Voltage-Gated Sodium Channel Nav1.8 Is Expressed in Human Sperm , 2013, PloS one.

[31]  João Ramalho-Santos,et al.  p,p′-DDE activates CatSper and compromises human sperm function at environmentally relevant concentrations , 2013, Human reproduction.

[32]  Gabriel Capellá,et al.  DNA Methylation Biomarkers for Noninvasive Diagnosis of Colorectal Cancer , 2013, Cancer Prevention Research.

[33]  G. Palermo,et al.  Downregulation of store-operated Ca2+ entry during mammalian meiosis is required for the egg-to-embryo transition , 2013, Journal of Cell Science.

[34]  X. Tian,et al.  Acute dietary zinc deficiency before conception compromises oocyte epigenetic programming and disrupts embryonic development. , 2013, Developmental biology.

[35]  M. Fellous,et al.  Disruption of the principal, progesterone-activated sperm Ca2+ channel in a CatSper2-deficient infertile patient , 2013, Proceedings of the National Academy of Sciences.

[36]  H. Tsujii,et al.  Selenium and vitamin E improve the in vitro maturation, fertilization and culture to blastocyst of porcine oocytes. , 2012, The Journal of reproduction and development.

[37]  J. Baltz,et al.  Cell volume regulation in mammalian oocytes and preimplantation embryos , 2012, Molecular reproduction and development.

[38]  A. Papavassiliou,et al.  Histone modifications as a pathogenic mechanism of colorectal tumorigenesis. , 2012, The international journal of biochemistry & cell biology.

[39]  MohammadA Sabbaghi,et al.  Effects of selenium, calcium and calcium ionophore on human oocytes in vitro maturation in a chemically defined medium , 2012, Iranian journal of reproductive medicine.

[40]  A. Darszon,et al.  Human spermatozoa possess a calcium‐dependent chloride channel that may participate in the acrosomal reaction , 2012, The Journal of physiology.

[41]  U. Kaupp,et al.  The CatSper channel: a polymodal chemosensor in human sperm , 2012, The EMBO journal.

[42]  T. Dirami,et al.  The testis anion transporter TAT1 (SLC26A8) physically and functionally interacts with the cystic fibrosis transmembrane conductance regulator channel: a potential role during sperm capacitation. , 2012, Human molecular genetics.

[43]  Chonggang Wang,et al.  Seminal Plasma Metals Concentration with Respect to Semen Quality , 2012, Biological Trace Element Research.

[44]  Yuriy Kirichok,et al.  Rediscovering sperm ion channels with the patch-clamp technique. , 2011, Molecular human reproduction.

[45]  E. Baldi,et al.  Mitochondrial membrane potential profile and its correlation with increasing sperm motility. , 2011, Fertility and sterility.

[46]  P. Lishko,et al.  Progesterone activates the principal Ca2+ channel of human sperm , 2011, Nature.

[47]  Manabu Yoshida,et al.  Lipid Rafts: Keys to Sperm Maturation, Fertilization, and Early Embryogenesis , 2011, Journal of lipids.

[48]  T. Cooper The epididymis, cytoplasmic droplets and male fertility. , 2011, Asian journal of andrology.

[49]  H. Zenkevičs,et al.  Frog oocyte in vitro maturation test as a method to investigate Ni2+ toxicity , 2011 .

[50]  V. Kay,et al.  Human oocytes express ATP-sensitive K(+) channels. , 2010, Human reproduction.

[51]  Luís Rato,et al.  Tubular Fluid Secretion in the Seminiferous Epithelium: Ion Transporters and Aquaporins in Sertoli Cells , 2010, The Journal of Membrane Biology.

[52]  C. Yeung Aquaporins in spermatozoa and testicular germ cells: identification and potential role. , 2010, Asian journal of andrology.

[53]  F. Larrea,et al.  Recombinant human ZP3-induced sperm acrosome reaction: evidence for the involvement of T- and L-type voltage-gated calcium channels. , 2010, Biochemical and biophysical research communications.

[54]  P. Lishko,et al.  Acid Extrusion from Human Spermatozoa Is Mediated by Flagellar Voltage-Gated Proton Channel , 2010, Cell.

[55]  S. Alper,et al.  HCO3 −/Cl− Exchange Inactivation and Reactivation during Mouse Oocyte Meiosis Correlates with MEK/MAPK-Regulated Ae2 Plasma Membrane Localization , 2009, PloS one.

[56]  Hua-gang Ma,et al.  Blockade of epithelial sodium channels improves sperm motility in asthenospermia patients. , 2009, International journal of andrology.

[57]  S. Tanabe,et al.  Zinc is an essential trace element for spermatogenesis , 2009, Proceedings of the National Academy of Sciences.

[58]  F. Larrea,et al.  TRPM8, a Versatile Channel in Human Sperm , 2009, PloS one.

[59]  H. Baker,et al.  Relationship between seminal plasma zinc concentration and spermatozoa-zona pellucida binding and the ZP-induced acrosome reaction in subfertile men. , 2009, Asian journal of andrology.

[60]  G. Kidder,et al.  Connexin expression and gap junctional coupling in human cumulus cells: contribution to embryo quality , 2008, Journal of cellular and molecular medicine.

[61]  G. Balercia,et al.  Free thiols in human spermatozoa: are Na+/K+-ATPase, Ca2+-ATPase activities involved in sperm motility through peroxynitrite formation? , 2009, Reproductive biomedicine online.

[62]  A. Salicioni,et al.  Human sperm devoid of PLC, zeta 1 fail to induce Ca(2+) release and are unable to initiate the first step of embryo development. , 2008, The Journal of clinical investigation.

[63]  T. Cooper,et al.  Potassium channels involved in human sperm volume regulation—quantitative studies at the protein and mRNA levels , 2008, Molecular reproduction and development.

[64]  C. Migné,et al.  Spontaneous calcium oscillations and nuclear PLC‐β1 in human GV oocytes , 2008 .

[65]  M. González-Martínez,et al.  Intracellular sodium increase induced by external calcium removal in human sperm. , 2008, Journal of andrology.

[66]  R. Puglisi,et al.  Selenium, a key element in spermatogenesis and male fertility. , 2008, Advances in experimental medicine and biology.

[67]  J. Kirkman-Brown,et al.  Patch‐clamp ‘mapping’ of ion channel activity in human sperm reveals regionalisation and co‐localisation into mixed clusters , 2007, Journal of cellular physiology.

[68]  Wen Ying Chen,et al.  Cystic fibrosis transmembrane conductance regulator is vital to sperm fertilizing capacity and male fertility , 2007, Proceedings of the National Academy of Sciences.

[69]  F. Nielsen,et al.  Nickel deficiency diminishes sperm quantity and movement in rats , 2007, Biological Trace Element Research.

[70]  He-feng Huang,et al.  Function of aquaporins in female and male reproductive systems. , 2006, Human reproduction update.

[71]  L. Johnson,et al.  Manganese acts centrally to activate reproductive hormone secretion and pubertal development in male rats. , 2006, Reproductive toxicology.

[72]  P. Marchetti,et al.  The functionality of mitochondria differentiates human spermatozoa with high and low fertilizing capability. , 2006, Fertility and sterility.

[73]  J. Tash,et al.  The Na,K-ATPase alpha4 isoform from humans has distinct enzymatic properties and is important for sperm motility. , 2006, Molecular human reproduction.

[74]  T. Cooper,et al.  Physiological volume regulation by spermatozoa , 2006, Molecular and Cellular Endocrinology.

[75]  N. Zilberberg,et al.  Fluctuations in Xenopus oocytes protein phosphorylation levels during two-electrode voltage clamp measurements , 2006, Journal of Neuroscience Methods.

[76]  D. Clapham,et al.  Whole-cell patch-clamp measurements of spermatozoa reveal an alkaline-activated Ca2+ channel , 2006, Nature.

[77]  A. Szewczyk,et al.  [Mitochondrial ion channels]. , 2002, Postepy higieny i medycyny doswiadczalnej.

[78]  S. Oehninger,et al.  Mitochondrial membrane potential integrity and plasma membrane translocation of phosphatidylserine as early apoptotic markers: a comparison of two different sperm subpopulations. , 2006, Fertility and sterility.

[79]  T. Cooper,et al.  Characterization of potassium channels involved in volume regulation of human spermatozoa. , 2005, Molecular human reproduction.

[80]  T. Cooper,et al.  Chloride Channels in Physiological Volume Regulation of Human Spermatozoa1 , 2005, Biology of reproduction.

[81]  R. Rizzuto,et al.  Calcium and mitochondria: mechanisms and functions of a troubled relationship. , 2004, Biochimica et biophysica acta.

[82]  K. Kihara,et al.  Localization of aquaporin-7 in human testis and ejaculated sperm: possible involvement in maintenance of sperm quality. , 2004, The Journal of urology.

[83]  Claire V. Harper,et al.  Stimulation of Human Spermatozoa with Progesterone Gradients to Simulate Approach to the Oocyte , 2004, Journal of Biological Chemistry.

[84]  Y. Korchev,et al.  Multi-state, 4-aminopyridine-sensitive ion channels in human spermatozoa. , 2004, Developmental biology.

[85]  O. Liveira EFFECTS OF DIETARY ZINC SUPPLEMENTATION ON SPERMATIC CHARACTERISTICS OF RABBIT BREEDERS , 2004 .

[86]  M. González-Martínez,et al.  Induction of a Sodium-dependent Depolarization by External Calcium Removal in Human Sperm* , 2003, Journal of Biological Chemistry.

[87]  T. Cooper,et al.  Human sperm volume regulation. Response to physiological changes in osmolality, channel blockers and potential sperm osmolytes. , 2003, Human reproduction.

[88]  V. Tsutsumi,et al.  Transient receptor potential (TRPC) channels in human sperm: expression, cellular localization and involvement in the regulation of flagellar motility , 2003, FEBS letters.

[89]  B. Dale,et al.  Chaotic mosaicism in human preimplantation embryos is correlated with a low mitochondrial membrane potential. , 2003, Fertility and sterility.

[90]  K. Mikoshiba,et al.  Inositol 1,4,5-trisphosphate receptor function in human oocytes: calcium responses and oocyte activation-related phenomena induced by photolytic release of InsP(3) are blocked by a specific antibody to the type I receptor. , 2002, Molecular human reproduction.

[91]  M. Manikkam,et al.  Potassium Channel Antagonists Influence Porcine Granulosa Cell Proliferation, Differentiation, and Apoptosis1 , 2002, Biology of reproduction.

[92]  J. van Blerkom,et al.  Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos. , 2002, Human reproduction.

[93]  B. Bavister How animal embryo research led to the first documented human IVF. , 2002, Reproductive biomedicine online.

[94]  J. Baltz,et al.  Developmentally regulated cell cycle dependence of swelling-activated anion channel activity in the mouse embryo. , 2001, Development.

[95]  J. Bai,et al.  A patch-clamp study on human sperm Cl- channel reassembled into giant liposome. , 2001, Asian journal of andrology.

[96]  T. Cooper,et al.  Effects of the ion-channel blocker quinine on human sperm volume, kinematics and mucus penetration, and the involvement of potassium channels. , 2001, Molecular human reproduction.

[97]  S. Ichinose,et al.  Failure of the Expression of Phospholipid Hydroperoxide Glutathione Peroxidase in the Spermatozoa of Human Infertile Males1 , 2001, Biology of reproduction.

[98]  F. Di Virgilio,et al.  Intracellular calcium store depletion and acrosome reaction in human spermatozoa: role of calcium and plasma membrane potential. , 2001, Molecular human reproduction.

[99]  C. Arnoult,et al.  Identification and localisation of T-type voltage operated calcium channel subunits in human male germ cells – expression of multiple isoforms , 2001 .

[100]  R. Pergolizzi,et al.  L-type voltage-dependent calcium channel alpha-1C subunit mRNA is present in ejaculated human spermatozoa. , 2000, Molecular human reproduction.