Dry Preservation of Spermatozoa: Considerations for Different Species.

The current gold standard for sperm preservation is storage at cryogenic temperatures. Dry preservation is an attractive alternative, eliminating the need for ultralow temperatures, reducing storage maintenance costs, and providing logistical flexibility for shipping. Many seeds and anhydrobiotic organisms are able to survive extended periods in a dry state through the accumulation of intracellular sugars and other osmolytes and are capable of returning to normal physiology postrehydration. Using techniques inspired by nature's adaptations, attempts have been made to dehydrate and dry preserve spermatozoa from a variety of species. Most of the anhydrous preservation research performed to date has focused on mouse spermatozoa, with only a small number of studies in nonrodent mammalian species. There is a significant difference between sperm function in rodent and nonrodent mammalian species with respect to centrosomal inheritance. Studies focused on reproductive technologies have demonstrated that in nonrodent species, the centrosome must be preserved to maintain sperm function as the spermatozoon centrosome contributes the dominant nucleating seed, consisting of the proximal centriole surrounded by pericentriolar components, onto which the oocyte's centrosomal material is assembled. Preservation techniques used for mouse sperm may therefore not necessarily be applicable to nonrodent spermatozoa. The range of technologies used to dehydrate sperm and the effect of processing and storage conditions on fertilization and embryogenesis using dried sperm are reviewed in the context of reproductive physiology and cellular morphology in different species.

[1]  L. Gil,et al.  Freeze-dried spermatozoa: A future tool? , 2017, Reproduction in domestic animals = Zuchthygiene.

[2]  G. Elliott,et al.  Effects of Water on Structure and Dynamics of Trehalose Glasses at Low Water Contents and its Relationship to Preservation Outcomes , 2016, Scientific Reports.

[3]  S. Hochi Microtubule assembly crucial to bovine embryonic development in assisted reproductive technologies , 2016, Animal science journal = Nihon chikusan Gakkaiho.

[4]  R. Carle,et al.  Preparation of High-Grade Powders from Tomato Paste Using a Vacuum Foam Drying Method. , 2015, Journal of food science.

[5]  G. Elliott,et al.  Resilience of oocyte germinal vesicles to microwave-assisted drying in the domestic cat model. , 2015, Biopreservation and biobanking.

[6]  G. Elliott,et al.  Local minimum in fragility for trehalose/glycerol mixtures: implications for biopharmaceutical stabilization. , 2015, The journal of physical chemistry. B.

[7]  Hideyuki Ito,et al.  Sperm Preservation by Freeze-Drying for the Conservation of Wild Animals , 2014, PloS one.

[8]  C. Malo,et al.  Current status of freeze-drying technology to preserve domestic animals sperm. , 2014, Reproduction in domestic animals = Zuchthygiene.

[9]  M. Toner,et al.  Live Pups from Evaporatively Dried Mouse Sperm Stored at Ambient Temperature for up to 2 Years , 2014, PloS one.

[10]  P. Loi,et al.  Towards storage of cells and gametes in dry form. , 2013, Trends in biotechnology.

[11]  G. Elliott,et al.  Advancing microwave technology for dehydration processing of biologics. , 2013, Biopreservation and biobanking.

[12]  J. Gosálvez,et al.  Types, Causes, Detection and Repair of DNA Fragmentation in Animal and Human Sperm Cells , 2012, International journal of molecular sciences.

[13]  A. Fujiyama,et al.  Two Novel Heat-Soluble Protein Families Abundantly Expressed in an Anhydrobiotic Tardigrade , 2012, PloS one.

[14]  T. Serikawa,et al.  Long-term preservation of freeze-dried mouse spermatozoa. , 2012, Cryobiology.

[15]  L. Gianaroli,et al.  DNA integrity is maintained after freeze-drying of human spermatozoa. , 2012, Fertility and sterility.

[16]  T. Serikawa,et al.  Successful Long-Term Preservation of Rat Sperm by Freeze-Drying , 2012, PloS one.

[17]  J. Douglas,et al.  β-Relaxation governs protein stability in sugar-glass matrices , 2012 .

[18]  M. Toner,et al.  Preservation of Mouse Sperm by Convective Drying and Storing in 3-O-Methyl-D-Glucose , 2012, PloS one.

[19]  A. Borini,et al.  Human Sperm Cryopreservation: Update on Techniques, Effect on DNA Integrity, and Implications for ART , 2011, Advances in urology.

[20]  A. E. Oliver Dry state preservation of nucleated cells: progress and challenges. , 2011, Biopreservation and biobanking.

[21]  H. Schatten,et al.  New insights into the role of centrosomes in mammalian fertilization and implications for ART. , 2011, Reproduction.

[22]  Charles C. Love,et al.  Production of live foals via intracytoplasmic injection of lyophilized sperm and sperm extract in the horse. , 2011, Reproduction.

[23]  J. Ringleb,et al.  Prolonged storage of epididymal spermatozoa does not affect their capacity to fertilise in vitro-matured domestic cat (Felis catus) oocytes when using ICSI. , 2011, Reproduction, fertility, and development.

[24]  M. Hirabayashi,et al.  Procedure for bovine ICSI, not sperm freeze-drying, impairs the function of the microtubule-organizing center. , 2011, The Journal of reproduction and development.

[25]  M. Toner,et al.  A Spin-Drying Technique for Lyopreservation of Mammalian Cells , 2011, Annals of Biomedical Engineering.

[26]  I. Hinduja,et al.  Correlation of human sperm centrosomal proteins with fertility , 2010, Journal of human reproductive sciences.

[27]  Y. Yue,et al.  A new threshold of uncovering the nature of glass transition: The slow ß relaxation in glassy states , 2010 .

[28]  H. Schatten,et al.  The role of centrosomes in mammalian fertilization and its significance for ICSI. , 2009, Molecular human reproduction.

[29]  N. Nakagata,et al.  Importance of primary culture conditions for the development of rat ICSI embryos and long-term preservation of freeze-dried sperm. , 2009, Cryobiology.

[30]  S. Blottner,et al.  Chromatin condensation in cat spermatozoa during epididymal transit as studied by aniline blue and acridine orange staining , 2009, Andrologia.

[31]  E. Walters,et al.  The history of sperm cryopreservation , 2009 .

[32]  I. Roy,et al.  Effect of trehalose on protein structure , 2008, Protein science : a publication of the Protein Society.

[33]  K. Chatdarong,et al.  The effect of antioxidants on motility, viability, acrosome integrity and DNA integrity of frozen-thawed epididymal cat spermatozoa. , 2008, Theriogenology.

[34]  G. Elliott,et al.  A role for microwave processing in the dry preservation of mammalian cells , 2008, Biotechnology and bioengineering.

[35]  Megumi Kato,et al.  Live rats resulting from injection of oocytes with spermatozoa freeze‐dried and stored for one year , 2008, Molecular reproduction and development.

[36]  A. Gutiérrez-Adán,et al.  Long-Term Effects of Mouse Intracytoplasmic Sperm Injection with DNA-Fragmented Sperm on Health and Behavior of Adult Offspring1 , 2008, Biology of reproduction.

[37]  C. Simerly,et al.  Freeze-dried primate sperm retains early reproductive potential after intracytoplasmic sperm injection. , 2008, Fertility and sterility.

[38]  T. Nakahara,et al.  Survival of freeze-dried bacteria. , 2008, The Journal of general and applied microbiology.

[39]  Steffen Hengherr,et al.  Trehalose and anhydrobiosis in tardigrades – evidence for divergence in responses to dehydration , 2008, The FEBS journal.

[40]  R. Yanagimachi,et al.  Mouse and human spermatozoa can be freeze-dried without damaging their chromosomes. , 2007, Human reproduction.

[41]  S. Báo,et al.  Effects of freeze-drying on cytology, ultrastructure, DNA fragmentation, and fertilizing ability of bovine sperm. , 2007, Theriogenology.

[42]  K. C. K. Lloyd,et al.  Long-term storage of mouse spermatozoa after evaporative drying. , 2007, Reproduction.

[43]  K. Jishage,et al.  Effect of pressure at primary drying of freeze-drying mouse sperm reproduction ability and preservation potential. , 2007, Reproduction.

[44]  T. Fischer,et al.  Lyophilized Platelets: Fifty Years in the Making , 2007, Artificial cells, blood substitutes, and immobilization biotechnology.

[45]  J. Acker,et al.  Mammalian Cell Desiccation: Facing The Challenges , 2006 .

[46]  B. Pukazhenthi,et al.  Poor Centrosomal Function of Cat Testicular Spermatozoa Impairs Embryo Development In Vitro after Intracytoplasmic Sperm Injection1 , 2006, Biology of reproduction.

[47]  P. Chow,et al.  Male genital tract antioxidant enzymes—Their ability to preserve sperm DNA integrity , 2006, Molecular and Cellular Endocrinology.

[48]  M. Toner,et al.  Trehalose uptake through P2X7 purinergic channels provides dehydration protection. , 2006, Cryobiology.

[49]  J. Clegg Desiccation Tolerance in Encysted Embryos of the Animal Extremophile, Artemia1 , 2005, Integrative and comparative biology.

[50]  Paolo De Paoli,et al.  Biobanking in microbiology: From sample collection to epidemiology, diagnosis and research , 2005, FEMS Microbiology Reviews.

[51]  M. Toner,et al.  Mouse Sperm Desiccated and Stored in Trehalose Medium Without Freezing1 , 2005, Biology of reproduction.

[52]  N. Nakagata,et al.  Relation between storage temperature and fertilizing ability of freeze-dried mouse spermatozoa. , 2005, Comparative medicine.

[53]  K. Jishage,et al.  Possibility of Long-Term Preservation of Freeze-Dried Mouse Spermatozoa1 , 2005, Biology of reproduction.

[54]  K. Niwa,et al.  Activation, Pronuclear Formation, and Development In Vitro of Pig Oocytes Following Intracytoplasmic Injection of Freeze-Dried Spermatozoa1 , 2004, Biology of reproduction.

[55]  A. E. Oliver,et al.  Loading Human Mesenchymal Stem Cells with Trehalose by Fluid-Phase Endocytosis , 2004 .

[56]  Charles L Bormann,et al.  Freeze-Dried Sperm Fertilization Leads to Full-Term Development in Rabbits1 , 2004, Biology of reproduction.

[57]  J. Biggers,et al.  Long-Term Preservation of Mouse Spermatozoa after Freeze-Drying and Freezing Without Cryoprotection1 , 2003, Biology of reproduction.

[58]  J. Ballescà,et al.  Marked differences in protamine content and P1/P2 ratios in sperm cells from percoll fractions between patients and controls. , 2003, Journal of andrology.

[59]  M. Toner,et al.  Desiccation Tolerance of Spermatozoa Dried at Ambient Temperature: Production of Fetal Mice1 , 2003, Biology of reproduction.

[60]  A. Elbein,et al.  New insights on trehalose: a multifunctional molecule. , 2003, Glycobiology.

[61]  W. Liu,et al.  Protection of sperm DNA against oxidative stress in vivo by accessory sex gland secretions in male hamsters. , 2002, Reproduction.

[62]  B. Brackett,et al.  Bovine Blastocyst Development from Oocytes Injected with Freeze-Dried Spermatozoa1 , 2002, Biology of reproduction.

[63]  M. Toner,et al.  Survival of Desiccated Mammalian Cells: Beneficial Effects of Isotonic Media , 2002 .

[64]  D. Brison,et al.  The spectrum of DNA damage in human sperm assessed by single cell gel electrophoresis (Comet assay) and its relationship to fertilization and embryo development. , 2002, Human reproduction.

[65]  E. Chantler,et al.  Response of midpiece vesicles on human sperm to osmotic stress. , 2002, Human reproduction.

[66]  R. Aitken,et al.  Oxidative stress, DNA damage and the Y chromosome. , 2001, Reproduction.

[67]  A. E. Oliver,et al.  The trehalose myth revisited: introduction to a symposium on stabilization of cells in the dry state. , 2001, Cryobiology.

[68]  H. Bayley,et al.  Beneficial effect of intracellular trehalose on the membrane integrity of dried mammalian cells. , 2001, Cryobiology.

[69]  J. Crowe,et al.  Human platelets loaded with trehalose survive freeze-drying. , 2001, Cryobiology.

[70]  Wei Wang Lyophilization and development of solid protein pharmaceuticals. , 2000, International journal of pharmaceutics.

[71]  A. Barnes,et al.  Sperm chromatin structure assay parameters as predictors of failed pregnancy following assisted reproductive techniques. , 2000, Human reproduction.

[72]  N. Mcclure,et al.  Differences in nuclear DNA fragmentation and mitochondrial integrity of semen and prepared human spermatozoa. , 2000, Human reproduction.

[73]  M. Toner,et al.  Literature review: supplemented phase diagram of the trehalose-water binary mixture. , 2000, Cryobiology.

[74]  J. Crowe,et al.  Preservation of mammalian cells—learning nature's tricks , 2000, Nature Biotechnology.

[75]  F. Levine,et al.  Trehalose expression confers desiccation tolerance on human cells , 2000, Nature Biotechnology.

[76]  Mehmet Toner,et al.  Intracellular trehalose improves the survival of cryopreserved mammalian cells , 2000, Nature Biotechnology.

[77]  Z. Rosenwaks,et al.  Sperm integrity is critical for normal mitotic division and early embryonic development. , 1999, Molecular human reproduction.

[78]  R. Aitken,et al.  Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. , 1998, Biology of reproduction.

[79]  Hoekstra,et al.  Influence of water content and temperature on molecular mobility and intracellular glasses in seeds and pollen , 1998, Plant physiology.

[80]  B. T. Storey,et al.  Comparison of glycerol, other polyols, trehalose, and raffinose to provide a defined cryoprotectant medium for mouse sperm cryopreservation. , 1998, Cryobiology.

[81]  R. Aitken,et al.  Oxidative damage to DNA in human spermatozoa does not preclude pronucleus formation at intracytoplasmic sperm injection. , 1998, Human reproduction.

[82]  J. Chirife,et al.  Adsorption isotherm of amorphous trehalose , 1997 .

[83]  P. Devroey,et al.  Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte , 1992, The Lancet.

[84]  P. Mazur Equilibrium, quasi-equilibrium, and nonequilibrium freezing of mammalian embryos , 1990, Cell Biophysics.

[85]  P. Wassarman,et al.  Fertilization in mammals. , 1988, Scientific American.

[86]  J. K. Sherman,et al.  Ultrastructure before freezing, while frozen, and after thawing in assessing cryoinjury of mouse epididymal spermatozoa. , 1982, Cryobiology.

[87]  M. Melamed,et al.  Relation of mammalian sperm chromatin heterogeneity to fertility. , 1980, Science.

[88]  J. K. Sherman Freezing and freeze-drying of human spermatozoa. , 1954, Fertility and sterility.

[89]  A. S. Parkes,et al.  Revival of Spermatozoa after Vitrification and Dehydration at Low Temperatures , 1949, Nature.

[90]  Scolnick,et al.  Preservation of Membranes in Anhydrobiotic Organisms : The Role of Trehalose , 2013 .

[91]  J. Crowe Trehalose as a "chemical chaperone": fact and fantasy. , 2007, Advances in experimental medicine and biology.

[92]  A. S. Rodrigues,et al.  Probing the Structure and Function of Mammalian Sperm using Optical and Fluorescence Microscopy , 2007 .

[93]  J. Crowe Trehalose As a “Chemical Chaperone” , 2007 .

[94]  KyungBon Lee,et al.  Fertilization and Development In Vitro of Bovine Oocytes Following Intracytoplasmic Injection of Heat-Dried Sperm Heads , 2006, Biology of reproduction.

[95]  Mehmet Toner,et al.  Beneficial effect of microinjected trehalose on the cryosurvival of human oocytes. , 2002, Fertility and sterility.

[96]  W. Ratnasooriya,et al.  Characterization of human gamete centrosomes for assisted reproduction. , 2001, Italian journal of anatomy and embryology = Archivio italiano di anatomia ed embriologia.

[97]  D. Gao,et al.  Mechanisms of cryoinjury in living cells. , 2000, ILAR journal.

[98]  Teruhiko Wakayama,et al.  Development of normal mice from oocytes injected with freeze-dried spermatozoa , 1998, Nature Biotechnology.

[99]  J. Carpenter,et al.  The role of vitrification in anhydrobiosis. , 1998, Annual review of physiology.

[100]  Z. Rosenwaks,et al.  The human sperm centrosome is responsible for normal syngamy and early embryonic development. , 1997, Reviews of reproduction.

[101]  S. N. Timasheff,et al.  The control of protein stability and association by weak interactions with water: how do solvents affect these processes? , 1993, Annual review of biophysics and biomolecular structure.

[102]  C. Angell,et al.  Phase relations and vitrification in saccharide-water solutions and the trehalose anomaly , 1989 .

[103]  N. Desai,et al.  Reproductive Biology and Endocrinology Open Access Paternal Effect on Genomic Activation, Clinical Pregnancy and Live Birth Rate after Icsi with Cryopreserved Epididymal versus Testicular Spermatozoa , 2022 .