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Influence of cryopreservation on structure and function of mammalian spermatozoa: an overview

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Abstract

Cryopreservation is a useful approach to preserve male fertility for assisted reproduction technique and other evaluations. In spite of extensive development in the cryopreservation field, there are biological and biochemical points including DNA fragmentation and antioxidant which should be illuminated to preserve fertility in safe form. Several molecular markers such as coding and noncoding RNAs are transferred from spermatozoa into oocyte via fertilization. These biomarkers affect fertility potential during the cryopreservation. Despite its impact, sperm cryopreservation has some destructive effect including loss of sperm motility and viability, acrosomal damage, mitochondrial membrane depolarization, plasma membrane permeability alteration even nuclear, and DNA damage. There is a growing concern about the impact of sperm cryopreservation on biological factors which can interrupt successful fertility procedures such as in vitro fertilization. Additionally, cryo-damage can decrease embryonic development extent. Promoting cryopreservation method via investigating the wide range of non-invasive factors may be increasingly important to have access to safe approach of freezing. Therefore, the aim of this study is the assessment of biological factors which can penetrate the fertility potential during the freezing procedure, explicate innovative methods in fertility preservation.

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References

  • AbdelHafez F, Bedaiwy M, El-Nashar SA, Sabanegh E, Desai N (2008) Techniques for cryopreservation of individual or small numbers of human spermatozoa: a systematic review. Hum Reprod Update 15:153–164

    PubMed  Google Scholar 

  • Aitken RJ, De Iuliis GN, McLachlan RI (2009) Biological and clinical significance of DNA damage in the male germ line. Int J Androl 32:46–56

    CAS  PubMed  Google Scholar 

  • Al-Hasani S et al (1999) Pregnancies achieved after frozen–thawed pronuclear oocytes obtained by intracytoplasmic sperm injection with spermatozoa extracted from frozen–thawed testicular tissues from non-obstructive azoospermic men. Hum Reprod 14:2031–2035

    CAS  PubMed  Google Scholar 

  • Aliakbari F et al (2016) Improving the efficacy of cryopreservation of spermatogonia stem cells by antioxidant supplements. Cell Reprogram 18:87–95

    CAS  PubMed  Google Scholar 

  • Alvarez JG, Touchstone JC, Blasco L, Storey BT (1987) Spontaneous lipid peroxidation and production of hydrogen peroxide and superoxide in human spermatozoa Superoxide dismutase as major enzyme protectant against oxygen toxicity. J Androl 8:338–348

    CAS  PubMed  Google Scholar 

  • Amor H, Zeyad A, Alkhaled Y, Laqqan M, Saad A, Ben Ali H, Hammadeh M (2018) Relationship between nuclear DNA fragmentation, mitochondrial DNA damage and standard sperm parameters in spermatozoa of fertile and sub-fertile men before and after freeze-thawing procedure. Andrologia 50:e12998

    CAS  PubMed  Google Scholar 

  • Anzar M, He L, Buhr MM, Kroetsch TG, Pauls KP (2002) Sperm apoptosis in fresh and cryopreserved bull semen detected by flow cytometry and its relationship with fertility. Biol Reprod 66:354–360

    CAS  PubMed  Google Scholar 

  • Arav A, Yavin S, Zeron Y, Natan D, Dekel I, Gacitua H (2002) New trends in gamete's cryopreservation. Mol Cell Endocrinol 187:77–81

    CAS  PubMed  Google Scholar 

  • Ashrafi I, Kohram H, Ardabili FF (2013) Antioxidative effects of melatonin on kinetics, microscopic and oxidative parameters of cryopreserved bull spermatozoa. Anim Reprod Sci 139:25–30

    CAS  PubMed  Google Scholar 

  • Aydin MS, Senturk GE, Ercan F (2013) Cryopreservation increases DNA fragmentation in spermatozoa of smokers. Acta Histochem 115:394–400

    CAS  PubMed  Google Scholar 

  • Aziz SG-G, Fardyazar Z, Pashaei-Asl F, Rahmati-Yamchi M, Khodadadi K, Pashaiasl M (2018) Human amniotic fluid stem cells (hAFSCs) expressing p21 and cyclin D1 genes retain excellent viability after freezing with (dimethyl sulfoxide) DMSO. Bosn J Basic Med Sci 19:43–51

  • Bailey JL, Blodeau JF, Cormier N (2000) Semen cryopreservation in domestic animals: a damaging and capacitating phenomenon minireview. J Androl 21:1–7

    CAS  PubMed  Google Scholar 

  • Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233

    CAS  PubMed  PubMed Central  Google Scholar 

  • Berkovitz A, Miller N, Silberman M, Belenky M, Itsykson P (2018) A novel solution for freezing small numbers of spermatozoa using a sperm vitrification device. Hum Reprod 33:1975–1983

    CAS  PubMed  Google Scholar 

  • Bevers EM, Comfurius P, Dekkers DW, Zwaal RF (1999) Lipid translocation across the plasma membrane of mammalian cells. Biochim Biophys Acta (BBA) Mol Cell Biol Lipids 1439:317–330

    CAS  Google Scholar 

  • Biggar KK, Dubuc A, Storey K (2009) MicroRNA regulation below zero: differential expression of miRNA-21 and miRNA-16 during freezing in wood frogs. Cryobiology 59:317–321

    CAS  PubMed  Google Scholar 

  • Bommer GT et al (2007) p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr Biol 17:1298–1307

    CAS  PubMed  Google Scholar 

  • Branco CS, Garcez ME, Pasqualotto FF, Erdtman B, Salvador M (2010) Resveratrol and ascorbic acid prevent DNA damage induced by cryopreservation in human semen. Cryobiology 60:235–237

    CAS  PubMed  Google Scholar 

  • Brennecke J, Hipfner DR, Stark A, Russell RB, Cohen SM (2003) Bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 113:25–36

    CAS  PubMed  Google Scholar 

  • Bushati N, Cohen SM (2007) microRNA functions. Annu Rev Cell Dev Biol 23:175–205

    CAS  PubMed  Google Scholar 

  • Calamera JC et al (2010) Effect of thawing temperature on the motility recovery of cryopreserved human spermatozoa. Fertil Steril 93:789–794

    PubMed  Google Scholar 

  • Capra E et al (2017) Small RNA sequencing of cryopreserved semen from single bull revealed altered miRNAs and piRNAs expression between High-and Low-motile sperm populations. BMC Genom 18:14

    CAS  Google Scholar 

  • Castro L, Hamilton T, Mendes C, Nichi M, Barnabe V, Visintin J, Assumpção M (2016) Sperm cryodamage occurs after rapid freezing phase: flow cytometry approach and antioxidant enzymes activity at different stages of cryopreservation. J Anim Sci Biotechnol 7:17

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chabory E et al (2009) Epididymis seleno-independent glutathione peroxidase 5 maintains sperm DNA integrity in mice. J Clin Investig 119:2074–2085

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chaudhari D, Dhami A, Hadiya K, Patel J (2015) Relative efficacy of egg yolk and soya milk-based extenders for cryopreservation (− 196 C) of buffalo semen. Vet World 8:239

    CAS  PubMed  PubMed Central  Google Scholar 

  • Consuegra C et al. (2019) Vitrification of large volumes of stallion sperm in comparison with spheres and conventional freezing: effect of warming procedures and sperm selection. J Equine Vet Sci

  • Cortés VDLG (2008) Inducción hormonal de la espermiación y criopreservación de esperma en anguila europea (Anguilla anguilla)

  • Curry E, Ellis S, Pratt S (2009) Detection of porcine sperm microRNAs using a heterologous microRNA microarray and reverse transcriptase polymerase chain reaction. Mol Reprod Dev Inc Gamete Res 76:218–219

    CAS  Google Scholar 

  • Curry E, Safranski TJ, Pratt SL (2011) Differential expression of porcine sperm microRNAs and their association with sperm morphology and motility. Theriogenology 76:1532–1539

    CAS  PubMed  Google Scholar 

  • De Vries K, Wiedmer T, Sims P, Gadella B (2003) Caspase-independent exposure of aminophospholipids and tyrosine phosphorylation in bicarbonate responsive human sperm cells. Biol Reprod 68:2122–2134

    PubMed  Google Scholar 

  • DeJarnette JM (2005) The effect of semen quality on reproductive efficiency. Vet Clin Food Anim Pract 21:409–418

    Google Scholar 

  • Devireddy R, Swanlund D, Olin T, Vincente W, Troedsson M, Bischof J, Roberts K (2002) Cryopreservation of equine sperm: optimal cooling rates in the presence and absence of cryoprotective agents determined using differential scanning calorimetry. Biol Reprod 66:222–231

    CAS  PubMed  Google Scholar 

  • Di Santo M, Tarozzi N, Nadalini M, Borini A (2012) Human sperm cryopreservation: update on techniques, effect on DNA integrity, and implications for ART. Adv Urol 2012:854–837

  • Diedrich K, Fauser B, Devroey P (2011) Cancer and fertility: strategies to preserve fertility. Reprod Biomed Online 22:232–248

    CAS  PubMed  Google Scholar 

  • Donnelly ET, McClure N, Lewis SE (2001) Cryopreservation of human semen and prepared sperm: effects on motility parameters and DNA integrity. Fertil Steril 76:892–900

    CAS  PubMed  Google Scholar 

  • Dubuc A, Storey KB (2008) Differential expression of microRNA species in organs of hibernating ground squirrels: a role in translational suppression during torpor. Biochim Biophys Acta (BBA) Gene Regul Mech 1779:628–633

  • Esau C et al (2004) MicroRNA-143 regulates adipocyte differentiation. J Biol Chem 279:52361–52365

    CAS  PubMed  Google Scholar 

  • Esmaeili V, Shahverdi A, Moghadasian M, Alizadeh A (2015) Dietary fatty acids affect semen quality: a review. Andrology 3:450–461

    CAS  PubMed  Google Scholar 

  • Feng H (2003) Molecular biology of male infertility. Arch Androl 49:19–27

    CAS  PubMed  Google Scholar 

  • Friedman RC, Farh KK-H, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19:92–105

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gadella B, Harrison R (2002) Capacitation induces cyclic adenosine 3′, 5′-monophosphate-dependent, but apoptosis-unrelated, exposure of aminophospholipids at the apical head plasma membrane of boar sperm cells. Biol Reprod 67:340–350

    CAS  PubMed  Google Scholar 

  • Gao D, Critser J (2000) Mechanisms of cryoinjury in living cells. ILAR J 41:187–196

    CAS  PubMed  Google Scholar 

  • García BM et al (2012) Toxicity of glycerol for the stallion spermatozoa: effects on membrane integrity and cytoskeleton, lipid peroxidation and mitochondrial membrane potential. Theriogenology 77:1280–1289

    Google Scholar 

  • Gholizadeh-Ghaleh Aziz S, Pashaei-Asl F, Fardyazar Z, Pashaiasl M (2016) Isolation, characterization, cryopreservation of human amniotic stem cells and differentiation to osteogenic and adipogenic cells. PLoS ONE 11:e0158281. https://doi.org/10.1371/journal.pone.0158281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilmore J, Liu J, Gao D, Critser J (1997) Determination of optimal cryoprotectants and procedures for their addition and removal from human spermatozoa. Hum Reprod (Oxf Engl) 12:112–118

    CAS  Google Scholar 

  • Giraud M, Motta C, Boucher D, Grizard G (2000) Membrane fluidity predicts the outcome of cryopreservation of human spermatozoa. Hum Reprod 15:2160–2164

    CAS  PubMed  Google Scholar 

  • Glander H (1984) Sperm metabolism, sperm vitality and cryopreservation. Zentralbl Gynakol 106:892–899

    CAS  PubMed  Google Scholar 

  • Grunewald S, Paasch U, Said TM, Rasch M, Agarwal A, Glander H-J (2006) Magnetic-activated cell sorting before cryopreservation preserves mitochondrial integrity in human spermatozoa. Cell Tissue Bank 7:99–104

    PubMed  Google Scholar 

  • Guthrie H, Welch G, Long J (2008) Mitochondrial function and reactive oxygen species action in relation to boar motility. Theriogenology 70:1209–1215

    CAS  PubMed  Google Scholar 

  • Hammerstedt RH, Graham JK, Nolan JP (1990) Cryopreservation of mammalian sperm: what we ask them to survive. J Androl 11:73–88

    CAS  PubMed  Google Scholar 

  • He Y, Li H, Wang K, Zhang Y, Zhao X (2017) Loss of protein kinase 2 subunit alpha 2 (CK2α’) effect ram sperm function after freezing and thawing process. Anim Reprod Sci 181:9–15

    CAS  PubMed  Google Scholar 

  • Hovatta O (2003) Cryobiology of ovarian and testicular tissue. Best Pract Res Clin Obstet Gynaecol 17:331–342

    PubMed  Google Scholar 

  • Hovatta O, Foudila T, Siegberg R, Johansson K, von Smitten K, Reima D (1996) Case report: pregnancy resulting from intracytoplasmic injection of spermatozoa from a frozen-thawed testicular biopsy specimen. Hum Reprod 11:2472–2473

    CAS  PubMed  Google Scholar 

  • Huang S, Li H, Ding X, Xiong C (2009) Presence and characterization of cell-free seminal RNA in healthy individuals: implications for noninvasive disease diagnosis and gene expression studies of the male reproductive system. Clin Chem 55:1967–1976

    CAS  PubMed  Google Scholar 

  • Isachenko E, Isachenko V, Katkov II, Dessole S, Nawroth F (2003) Vitrification of mammalian spermatozoa in the absence of cryoprotectants: from past practical difficulties to present success. Reprod Biomed Online 6:191–200

    PubMed  Google Scholar 

  • Isachenko V et al (2011) Cryoprotectant-free vitrification of human spermatozoa in large (up to 0.5 mL) volume: a novel technology. Clin Lab 57:643–650

    CAS  PubMed  Google Scholar 

  • Izadyar F, Matthijs‐Rijsenbilt J, Den Ouden K, Creemers LB, Woelders H, de Rooij DG (2002) Development of a cryopreservation protocol for type A spermatogonia. J Androl 23:537–545

    CAS  PubMed  Google Scholar 

  • Jahnukainen K, Ehmcke J, Hou M, Schlatt S (2011) Testicular function and fertility preservation in male cancer patients Best practice & research. Clin Endocrinol Metab 25:287–302

    Google Scholar 

  • Jenkins TG, Aston KI, Carrell DT (2011) Supplementation of cryomedium with ascorbic acid–2-glucoside (AA2G) improves human sperm post-thaw motility. Fertil Steril 95:2001–2004

    CAS  PubMed  Google Scholar 

  • Jeyendran RS, Acosta VC, Land S, Coulam CB (2008) Cryopreservation of human sperm in a lecithin-supplemented freezing medium. Fertil Steril 90:1263–1265

    PubMed  Google Scholar 

  • Kalthur G, Raj S, Thiyagarajan A, Kumar S, Kumar P, Adiga SK (2011) Vitamin E supplementation in semen-freezing medium improves the motility and protects sperm from freeze-thaw–induced DNA damage. Fertil Steril 95:1149–1151

    CAS  PubMed  Google Scholar 

  • Katepogu K, Chittor P, Kurumala D, Mallepogu V, Kamity V, Kedam TR (2013) Freeze and thaw creates oxidative stress and DNA damage in frozen human spermatozoa Indo. Am J Pharm Res 3:7184–7191

    Google Scholar 

  • Keros V, Rosenlund B, Hultenby K, Aghajanova L, Levkov L, Hovatta O (2005) Optimizing cryopreservation of human testicular tissue: comparison of protocols with glycerol, propanediol and dimethylsulphoxide as cryoprotectants. Hum Reprod 20:1676–1687

    CAS  PubMed  Google Scholar 

  • Kloosterman WP, Plasterk RH (2006) The diverse functions of microRNAs in animal development and disease. Dev Cell 11:441–450

    CAS  PubMed  Google Scholar 

  • Kotdawala AP et al (2012) Addition of zinc to human ejaculate prior to cryopreservation prevents freeze-thaw-induced DNA damage and preserves sperm function. J Assist Reprod Genet 29:1447–1453

    PubMed  PubMed Central  Google Scholar 

  • Kothari S, Thompson A, Agarwal A, du Plessis SS (2010) Free radicals: their beneficial and detrimental effects on sperm function. Indian J Exp Biol 48:425–435

    CAS  PubMed  Google Scholar 

  • Kubota H, Avarbock MR, Brinster RL (2004) Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci 101:16489–16494

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lasso JL, Noiles EE, Alvarez JG, Storey BT (1994) Mechanism of superoxide dismutase loss from human sperm cells during cryopreservation. J Androl 15:255–265

    CAS  PubMed  Google Scholar 

  • Lee Y-A et al (2013) Cryopreservation of mouse spermatogonial stem cells in dimethylsulfoxide and polyethylene glycol. Biol Reprod 89(109):101–109

    Google Scholar 

  • Leffers H, Andersson A, Juul A, Carlsen E, Mortensen G, Jensen T, Toppari J (2006) Is human fecundity declining. Int J Androl 29:211

  • Lemaire-Ewing S, Desrumaux C, Néel D, Lagrost L (2010) Vitamin E transport, membrane incorporation and cell metabolism: Is α-tocopherol in lipid rafts an oar in the lifeboat? Mol Nutr Food Res 54:631–640

    CAS  PubMed  Google Scholar 

  • Lewis SE (2007) Is sperm evaluation useful in predicting human fertility? Reproduction 134:31–40

    CAS  PubMed  Google Scholar 

  • Li P et al (2010) Ice-age endurance: the effects of cryopreservation on proteins of sperm of common carp, Cyprinus carpio L. Theriogenology 74:413–423

    CAS  PubMed  Google Scholar 

  • Li P, Li Z-H, Dzyuba B, Hulak M, Rodina M, Linhart O (2010) Evaluating the impacts of osmotic and oxidative stress on common carp (Cyprinus carpio, L.) sperm caused by cryopreservation techniques. Biol Reprod 83:852–858

    CAS  PubMed  Google Scholar 

  • Lian J et al (2009) Altered microRNA expression in patients with non-obstructive azoospermia. Reprod Biol Endocrinol 7:13

    PubMed  PubMed Central  Google Scholar 

  • Liu T et al (2016) The effect of two cryopreservation methods on human sperm DNA damage. Cryobiology 72:210–215

    CAS  PubMed  Google Scholar 

  • Love C, Brinsko S, Rigby S, Thompson J, Blanchard T, Varner D (2005) Relationship of seminal plasma level and extender type to sperm motility and DNA integrity. Theriogenology 63:1584–1591

    CAS  PubMed  Google Scholar 

  • Lovelock J (1953) The haemolysis of human red blood-cells by freezing and thawing. Biochem Biophys Acta 10:414–426

    CAS  PubMed  Google Scholar 

  • Luyet BJ, Hodapp EL (1938) Revival of frog's spermatozoa vitrified in liquid air. Proc Soc Exp Biol Med 39:433–434

    Google Scholar 

  • Lyons PJ, Lang-Ouellette D (2013) CryomiRs: towards the identification of a cold-associated family of microRNAs. Comp Biochem Physiol D Genom Proteom 8:358–364

    CAS  Google Scholar 

  • Magnes L, Li T (1980) Isolation and properties of superoxide dismutase from bovine spermatozoa. Biol Reprod 22:965–969

    CAS  PubMed  Google Scholar 

  • Maldjian A, Pizzi F, Gliozzi T, Cerolini S, Penny P, Noble R (2005) Changes in sperm quality and lipid composition during cryopreservation of boar semen. Theriogenology 63:411–421

    CAS  PubMed  Google Scholar 

  • Mann T, Lutwak-Mann C (2012) Male reproductive function and semen: themes and trends in physiology, biochemistry and investigative andrology. Springer, New York

    Google Scholar 

  • Mansilla M, Merino O, Risopatron J, Isachenko V, Isachenko E, Sanchez R (2016) High temperature is essential for preserved human sperm function during the devitrification process. Andrologia 48:111–113

    CAS  PubMed  Google Scholar 

  • Martin G, Sabido O, Durand P, Levy R (2004) Cryopreservation induces an apoptosis-like mechanism in bull sperm. Biol Reprod 71:28–37

    CAS  PubMed  Google Scholar 

  • Martinez C et al (2019) High pre-freezing sperm dilution improves monospermy without affecting the penetration rate in porcine IVF. Theriogenology 131:162–168

    CAS  PubMed  Google Scholar 

  • Mazur P, Seki S (2011) Survival of mouse oocytes after being cooled in a vitrification solution to− 196 C at 95 to 70,000 C/min and warmed at 610 to 118,000 C/min: A new paradigm for cryopreservation by vitrification. Cryobiology 62:1–7

    CAS  PubMed  Google Scholar 

  • Mazzilli F, Rossi T, Sabatini L, Pulcinelli F, Rapone S, Dondero F, Gazzaniga P (1995) Human sperm cryopreservation and reactive oxygen species (ROS) production. Acta Eur Fertil 26:145–148

    CAS  PubMed  Google Scholar 

  • McLaughlin E, Ford W, Hull M (1994) Adenosine triphosphate and motility characteristics of fresh and cryopreserved human spermatozoa. Int J Androl 17:19–23

    CAS  PubMed  Google Scholar 

  • Meamar M et al (2012) Sperm DNA fragmentation induced by cryopreservation: new insights and effect of a natural extract from Opuntia ficus-indica. Fertil Steril 98:326–333

    CAS  PubMed  Google Scholar 

  • Melo C et al. (2008) Comparison of three different extenders for freezing epididymal stallion sperm. Anim Reproduction Science:331–331

    Google Scholar 

  • Miller C (2008) Optimizing the use of frozen–thawed equine semen. Theriogenology 70:463–468

    CAS  PubMed  Google Scholar 

  • Mirzapour T, Movahedin M, Tengku Ibrahim T, Haron A, Nowroozi M (2013) Evaluation of the effects of cryopreservation on viability, proliferation and colony formation of human spermatogonial stem cells in vitro culture. Andrologia 45:26–34

    CAS  PubMed  Google Scholar 

  • Mishima T et al (2008) MicroRNA (miRNA) cloning analysis reveals sex differences in miRNA expression profiles between adult mouse testis and ovary. Reproduction 136:811–822

    CAS  PubMed  Google Scholar 

  • Mohaqiq M, Movahedin M, Mazaheri Z, Amirjannati N (2019) In vitro transplantation of spermatogonial stem cells isolated from human frozen–thawed testis tissue can induce spermatogenesis under 3-dimensional tissue culture conditions. Biol Res 52:16

    PubMed  PubMed Central  Google Scholar 

  • Morris GJ, Acton E, Murray BJ, Fonseca F (2012) Freezing injury: the special case of the sperm cell. Cryobiology 64:71–80

    Google Scholar 

  • Moskwa P et al (2011) miR-182-mediated downregulation of BRCA1 impacts DNA repair and sensitivity to PARP inhibitors. Mol Cell 41:210–220

    CAS  PubMed  Google Scholar 

  • Moustafa MH, Sharma RK, Thornton J, Mascha E, Abdel-Hafez MA, Thomas AJ, Agarwal A (2004) Relationship between ROS production, apoptosis and DNA denaturation in spermatozoa from patients examined for infertility. Hum Reprod 19:129–138

    CAS  PubMed  Google Scholar 

  • Najafi A et al (2018) Melatonin affects membrane integrity, intracellular reactive oxygen species, caspase3 activity and AKT phosphorylation in frozen thawed human sperm. Cell Tissue Res 372:149–159

    CAS  PubMed  Google Scholar 

  • O'connell M, McClure N, Lewis S (2002) The effects of cryopreservation on sperm morphology, motility and mitochondrial function. Hum Reprod 17:704–709

    CAS  PubMed  Google Scholar 

  • Oettle E, Soley J (1986) Ultrastructural changes in the acrosome of human sperm during freezing and thawing: a pilot trial. Arch Androl 17:145–150

    CAS  PubMed  Google Scholar 

  • O'flaherty C, de Lamirande E, Gagnon C (2006) Positive role of reactive oxygen species in mammalian sperm capacitation: triggering and modulation of phosphorylation events. Free Radical Biol Med 41:528–540

    CAS  Google Scholar 

  • Okada H, Tajima A, Shichiri K, Tanaka A, Tanaka K, Inoue I (2008) Genome-wide expression of azoospermia testes demonstrates a specific profile and implicates ART3 in genetic susceptibility. PLoS Genet 4:e26

    PubMed  PubMed Central  Google Scholar 

  • Paasch U, Grunewald S, Agarwal A, Glandera H-J (2004a) Activation pattern of caspases in human spermatozoa. Fertil Steril 81:802–809

    CAS  PubMed  Google Scholar 

  • Paasch U et al (2004b) Cryopreservation and thawing is associated with varying extent of activation of apoptotic machinery in subsets of ejaculated human spermatozoa. Biol Reprod 71:1828–1837

    CAS  PubMed  Google Scholar 

  • Papa FO, Melo C, Fioratti E, Dell’Aqua J Jr, Zahn F, Alvarenga MA (2008) Freezing of stallion epididymal sperm. Anim Reprod Sci 107:293–301

    CAS  PubMed  Google Scholar 

  • Pashaiasl M, Khodadadi K, Richings NM, Holland MK, Verma PJ (2013) Cryopreservation and long-term maintenance of bovine embryo-derived cell lines. Reprod Fertil Dev 25:707–718

    CAS  PubMed  Google Scholar 

  • Paynter S, Cooper A, Gregory L, Fuller B, Shaw R (1999) Permeability characteristics of human oocytes in the presence of the cryoprotectant dimethylsulphoxide. Hum Reprod 14:2338–2342

    CAS  PubMed  Google Scholar 

  • Peris SI, Bilodeau JF, Dufour M, Bailey JL (2007) Impact of cryopreservation and reactive oxygen species on DNA integrity, lipid peroxidation, and functional parameters in ram sperm. Mol Reprod Dev 74:878–892

    CAS  PubMed  Google Scholar 

  • Polge C, Smith AU, Parkes AS (1949) Revival of spermatozoa after vitrification and dehydration at low temperatures. Nature 164:666

    CAS  PubMed  Google Scholar 

  • Pradiee J, Esteso M, Castaño C, Toledano-Díaz A, Lopez-Sebastián A, Guerra R, Santiago-Moreno J (2017) Conventional slow freezing cryopreserves mouflon spermatozoa better than vitrification. Andrologia 49:e12629

    Google Scholar 

  • Rahbar S et al (2017) New insights into the expression profile of MicroRNA-34c and P53 in infertile men spermatozoa and testicular tissue. Cell Mol Biol (Noisy-le-Grand France) 63:77–83

    CAS  PubMed  Google Scholar 

  • Redden E et al (2009) Large quantity cryopreservation of bovine testicular cells and its effect on enrichment of type A spermatogonia. Cryobiology 58:190–195

    CAS  PubMed  Google Scholar 

  • Reiter RJ, Tan D-X, Manchester LC, Paredes SD, Mayo JC, Sainz RM (2009) Melatonin and reproduction revisited. Biol Reprod 81:445–456

    CAS  PubMed  Google Scholar 

  • Roelen B (2010) An overview on the diversity of cellular organelles during the germ cell cycle. Histol Histopathol 25:267–276

    PubMed  Google Scholar 

  • Saacke R, Nadir S, Nebel R (1994) Relationship of semen quality to sperm transport, fertilization, and embryo quality in ruminants. Theriogenology 41:45–50

    Google Scholar 

  • Said TM, Gaglani A, Agarwal A (2010) Implication of apoptosis in sperm cryoinjury. Reprod Biomed Online 21:456–462

    PubMed  Google Scholar 

  • Sánchez R, Risopatrón J, Schulz M, Villegas J, Isachenko V, Kreinberg R, Isachenko E (2011) Canine sperm vitrification with sucrose: effect on sperm function. Andrologia 43:233–241

    PubMed  Google Scholar 

  • Santos JH, Meyer JN, Mandavilli BS, Van Houten B (2006) Quantitative PCR-based measurement of nuclear and mitochondrial DNA damage and repair in mammalian cells. In: Bjergbæk L (ed) DNA repair protocols. Springer, New York, pp 183–199

    Google Scholar 

  • Schiller J, Arnhold J, Glander H-J, Arnold K (2000) Lipid analysis of human spermatozoa and seminal plasma by MALDI-TOF mass spectrometry and NMR spectroscopy—effects of freezing and thawing. Chem Phys Lipid 106:145–156

    CAS  Google Scholar 

  • Selbach M, Schwanhäusser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N (2008) Widespread changes in protein synthesis induced by microRNAs. Nature 455:58

    CAS  PubMed  Google Scholar 

  • Serafini PC, Hauser D, Moyer D, Marrs RP (1986) Cryopreservation of human spermatozoa: correlations of ultrastructural sperm head configuration with sperm motility and ability to penetrate zona-free hamster ova. Fertil Steril 46:691–695

    CAS  PubMed  Google Scholar 

  • Serafini R, Varner D, Blanchard T, Teague S, LaCaze K, Love C (2018) Effects of seminal plasma and flash-freezing on DNA structure of stallion epididymal sperm exposed to different potentiators of DNA damage. Theriogenology 117:34–39

    CAS  PubMed  Google Scholar 

  • Shahverdi A et al (2015) Fertility and flow cytometric evaluations of frozen-thawed rooster semen in cryopreservation medium containing low-density lipoprotein. Theriogenology 83:78–85

    CAS  PubMed  Google Scholar 

  • Shaman JA, Ward WS (2006) Sperm chromatin stability and susceptibility to damage in relation to its structure. In: The sperm cell: production, maturation, fertilization and regeneration, pp 31–48

  • Sherman JK (1964) Research on frozen human semen: past, present, and future. Fertil Steril 15:485–500

    CAS  PubMed  Google Scholar 

  • Sherman J (1968) Practical applications and technical problems of preserving spermatozoa by freezing. In: Federation proceedings, pp S288–S296

  • Sherman JK (1973) Synopsis of the use of frozen human semen since 1964: state of the art of human semen banking. Fertil Steril 24:397

    CAS  PubMed  Google Scholar 

  • Shetty G et al (2013) Hormone suppression with GnRH antagonist promotes spermatogenic recovery from transplanted spermatogonial stem cells in irradiated cynomolgus monkeys. Andrology 1:886–898

    CAS  PubMed  PubMed Central  Google Scholar 

  • Silva E, Cajueiro J, Silva S, Soares P, Guerra M (2012) Effect of antioxidants resveratrol and quercetin on in vitro evaluation of frozen ram sperm. Theriogenology 77:1722–1726

    CAS  PubMed  Google Scholar 

  • Sion B, Janny L, Boucher D, Grizard G (2004) Annexin V binding to plasma membrane predicts the quality of human cryopreserved spermatozoa. Int J Androl 27:108–114

    CAS  PubMed  Google Scholar 

  • Siu AW, Maldonado M, Sanchez-Hidalgo M, Tan DX, Reiter RJ (2006) Protective effects of melatonin in experimental free radical-related ocular diseases. J Pineal Res 40:101–109

    CAS  PubMed  Google Scholar 

  • Slabbert M, Du Plessis S, Huyser C (2015) Large volume cryoprotectant-free vitrification: an alternative to conventional cryopreservation for human spermatozoa. Andrologia 47:594–599

    CAS  PubMed  Google Scholar 

  • Słowińska M, Karol H, Ciereszko A (2008) Comet assay of fresh and cryopreserved bull spermatozoa. Cryobiology 56:100–102

    PubMed  Google Scholar 

  • Storey KB, Storey JM (1986) Freeze tolerance and intolerance as strategies of winter survival in terrestrially-hibernating amphibians. Comp Biochem Physiol A Comp Physiol 83:613–617

    CAS  PubMed  Google Scholar 

  • Storey KB, Storey JM (2013) Molecular biology of freezing tolerance. Compr Physiol 3:1283–1308

    PubMed  Google Scholar 

  • Tahmasbpour E, Balasubramanian D, Agarwal A (2014) A multi-faceted approach to understanding male infertility: gene mutations, molecular defects and assisted reproductive techniques (ART). J Assist Reprod Genet 31:1115–1137

    PubMed  PubMed Central  Google Scholar 

  • Tatone C, Di Emidio G, Vento M, Ciriminna R, Artini PG (2010) Cryopreservation and oxidative stress in reproductive cells. Gynecol Endocrinol 26:563–567

    PubMed  Google Scholar 

  • Taylor K, Roberts P, Sanders K, Burton P (2009) Effect of antioxidant supplementation of cryopreservation medium on post-thaw integrity of human spermatozoa. Reprod Biomed Online 18:184–189

    PubMed  Google Scholar 

  • Thomson LK, Fleming SD, Aitken RJ, De Iuliis GN, Zieschang J-A, Clark AM (2009) Cryopreservation-induced human sperm DNA damage is predominantly mediated by oxidative stress rather than apoptosis. Hum Reprod 24:2061–2070

    CAS  PubMed  Google Scholar 

  • Thuwanut P, Chatdarong K, Johannisson A, Bergqvist A-S, Söderquist L, Axnér E (2010) Cryopreservation of epididymal cat spermatozoa: effects of in vitro antioxidative enzymes supplementation and lipid peroxidation induction. Theriogenology 73:1076–1087

    CAS  PubMed  Google Scholar 

  • Tremellen K (2008) Oxidative stress and male infertility—a clinical perspective. Hum Reprod Update 14:243–258

    CAS  PubMed  Google Scholar 

  • Valko M, Rhodes C, Moncol J, Izakovic M, Mazur M (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 160:1–40

    CAS  PubMed  Google Scholar 

  • van Overveld FW, Haenen GR, Rhemrev J, Vermeiden JP, Bast A (2000) Tyrosine as important contributor to the antioxidant capacity of seminal plasma. Chem Biol Interact 127:151–161

    PubMed  Google Scholar 

  • Volonté D, Galbiati F, Pestell RG, Lisanti MP (2001) Cellular stress induces the tyrosine phosphorylation of caveolin-1 (Tyr14) via activation of p38 mitogen-activated protein kinase and c-Src kinase evidence for caveolae, the actin cytoskeleton, and focal adhesions as mechanical sensors of osmotic stress. J Biol Chem 276:8094–8103

    PubMed  Google Scholar 

  • Wang X, Sharma RK, Sikka SC, Thomas AJ Jr, Falcone T, Agarwal A (2003) Oxidative stress is associated with increased apoptosis leading to spermatozoa DNA damage in patients with male factor infertility. Fertil Steril 80:531–535

    PubMed  Google Scholar 

  • Ward WS, Coffey D (1991) DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol Reprod 44:569–574

    CAS  PubMed  Google Scholar 

  • Watson P (2000) The causes of reduced fertility with cryopreserved semen. Anim Reprod Sci 60:481–492

    PubMed  Google Scholar 

  • White I (1993) Lipids and calcium uptake of sperm in relation to cold shock and preservation: a review. Reprod Fertil Dev 5:639–658

    CAS  PubMed  Google Scholar 

  • Whittingham D (1971) Survival of mouse embryos after freezing and thawing. Nature 233:125

    CAS  PubMed  Google Scholar 

  • Winterbone MS, Sampson MJ, Saha S, Hughes JC, Hughes DA (2007) Pro-oxidant effect of α-tocopherol in patients with Type 2 Diabetes after an oral glucose tolerance test–a randomised controlled trial. Cardiovasc Diabetol 6:8

    PubMed  PubMed Central  Google Scholar 

  • World Health Organization (1999) WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction. Cambridge University Press, Cambridge

    Google Scholar 

  • World Health Organization (2010) WHO laboratory manual for the examination and processing of human semen. WHO, Geneva

    Google Scholar 

  • Wu X, Goodyear SM, Abramowitz LK, Bartolomei MS, Tobias JW, Avarbock MR, Brinster RL (2012) Fertile offspring derived from mouse spermatogonial stem cells cryopreserved for more than 14 years. Hum Reprod 27:1249–1259

    PubMed  PubMed Central  Google Scholar 

  • Xia H-F, Jin X-H, Cao Z-F, Shi T, Ma X (2014) MiR-98 is involved in rat embryo implantation by targeting Bcl-xl. FEBS Lett 588:574–583

    CAS  PubMed  Google Scholar 

  • Yousef M, Abdallah G, Kamel K (2003) Effect of ascorbic acid and vitamin E supplementation on semen quality and biochemical parameters of male rabbits. Anim Reprod Sci 76:99–111

    CAS  PubMed  Google Scholar 

  • Zeke J, Konc J, Kanyo K, Kriston R, Cseh S (2012) Birth and clinical pregnancy from fresh and frozen oocytes fertilized with cryopreserved testicular spermatozoa. Syst Biol Reprod Med 58:165–167

    PubMed  Google Scholar 

  • Zeng C, He L, Peng W, Ding L, Tang K, Fang D, Zhang Y (2014) Selection of optimal reference genes for quantitative RT-PCR studies of boar spermatozoa cryopreservation. Cryobiology 68:113–121

    CAS  PubMed  Google Scholar 

  • Zhang DX, Gutterman DD (2007) Mitochondrial reactive oxygen species-mediated signaling in endothelial cells. Am J Physiol Heart Circ Physiol 292:H2023–H2031

    CAS  PubMed  Google Scholar 

  • Zhang Y, Zeng C-J, He L, Ding L, Tang K-Y, Peng W-P (2015) Selection of endogenous reference microRNA genes for quantitative reverse transcription polymerase chain reaction studies of boar spermatozoa cryopreservation. Theriogenology 83:634–641

    CAS  PubMed  Google Scholar 

  • Zhang Y et al (2017) Cryopreservation of boar sperm induces differential microRNAs expression. Cryobiology 76:24–33

    CAS  PubMed  Google Scholar 

  • Zingg J-M (2007) Vitamin E: an overview of major research directions. Mol Asp Med 28:400–422

    CAS  Google Scholar 

  • Zribi N et al (2012) Effect of freezing–thawing process and quercetin on human sperm survival and DNA integrity. Cryobiology 65:326–331

    CAS  PubMed  Google Scholar 

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Acknowledgements

This article is in line with Dr. Maryam Ezzati’s thesis about the effect of cryopreservation on male fertility to acquire a Ph.D. in Tabriz Medical University. This study was endorsed by Immunology Research Center, Tabriz University of Medical Sciences, Tabriz/Iran (60961).

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Correspondence to Maryam Pashaiasl.

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Ezzati, M., Shanehbandi, D., Hamdi, K. et al. Influence of cryopreservation on structure and function of mammalian spermatozoa: an overview. Cell Tissue Bank 21, 1–15 (2020). https://doi.org/10.1007/s10561-019-09797-0

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