Cited by 12Reproductive Biology and FertilitySperm and Testicular FunctionReproductive biology and impacts on aquatic species

Long-term storage of gametes and gonadal tissues at room temperatures: The end of the ice age?

Open access
Comizzoli, Pierre, Loi, Pasqualino, Patrizio, Pasquale, Hubel, Allison·2022·Journal of Assisted Reproduction and Genetics

Abstract

Long-term preservation of viable spermatozoa, eggs, embryos, and gonadal tissues of good quality is essential in human reproductive medicine and for the population management of livestock, laboratory, and wild species. Instead of using freezing temperatures, encouraging findings indicate that structures and functions of gametes or gonadal tissues can be suspended in trehalose glass after dehydration and then preserved at supra-zero temperatures. As a new era in fertility preservation and biobanking is about to start, the advantages, needs, and implications of germplasm storage at room temperatures must be carefully examined. Although very promising, the development of alternate biobanking strategies does not necessarily mean that the end of the "ice age" (cryopreservation) is near.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1007/s10815-021-02392-x

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

No references could be resolved yet.

Research works printed but not linked: 31

  1. [1]Saragusty J, Anzalone DA, Palazzese L, Arav A, Patrizio P, Gosálvez J, et al. Dry biobanking as a conservation tool in the Anthropocene. Theriogenology [Internet]. Theriogenology; 2020 [cited 2021 Dec 1];150:130–8. Available from: https://pubmed.ncbi.nlm.nih.gov/31980207/ [DOI] [PubMed]
  2. [2]Paulson RJ, Comizzoli P. Addressing challenges in developing and implementing successful in vitro fertilization in endangered species: an opportunity for humanity to “give back.” Fertil. Steril. [Internet]. Fertil Steril; 2018 [cited 2021 Dec 28];109:418–9. Available from: https://pubmed.ncbi.nlm.nih.gov/29526478/ [DOI] [PubMed]
  3. [3]Comizzoli P, Paulson EE, McGinnis LK. The mutual benefits of research in wild animal species and human-assisted reproduction. J. Assist. Reprod. Genet. Journal of Assisted Reproduction and Genetics; 2018;35:551–60. [DOI] [PMC free article] [PubMed]
  4. [4]Hubel A, Spindler R, Skubitz APN. Storage of human biospecimens: selection of the optimal storage temperature. Biopreserv. Biobank. [Internet]. Biopreserv Biobank; 2014 [cited 2021 Dec 2];12:165–75. Available from: https://pubmed.ncbi.nlm.nih.gov/24918763/ [DOI] [PubMed]
  5. [5]Comizzoli P, Wildt DE. Mammalian fertility preservation through cryobiology: value of classical comparative studies and the need for new preservation options. Reprod Fertil Dev [Internet]. 2013;26:91–8. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3929269&tool=pmcentrez&rendertype=abstract [DOI] [PMC free article] [PubMed]
  6. [7]Rall WF, Fahy GM. Ice-free cryopreservation of mouse embryos at -196°C by vitrification. Nature [Internet]. Nature; 1985 [cited 2021 Mar 27];313:573–5. Available from: https://pubmed.ncbi.nlm.nih.gov/3969158/ [DOI] [PubMed]
  7. [8]Keilin D. The Leeuwenhoek lecture - the problem of anabiosis or latent life: history and current concept. Proc. R. Soc. London. Ser. B - Biol. Sci. [Internet]. Proc R Soc Lond B Biol Sci; 1959 [cited 2021 Dec 1];150:149–91. Available from: https://pubmed.ncbi.nlm.nih.gov/13633975/ [DOI] [PubMed]
  8. [9]Crowe JH. Introduction: stabilization of dry biological materials. Biopreserv Biobank. 2012;10:375–375. doi: 10.1089/bio.2012.1043. [DOI] [PubMed] [Google Scholar] · DOI
  9. [10]Chen T, Fowler A, Toner M. Literature review: supplemented phase diagram of the trehalose-water binary mixture. Cryobiology [Internet]. 2000 [cited 2017 Jun 1];40:277–82. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0011224000922442 [DOI] [PubMed]
  10. [11]Voronina TA, Nesmelov AA, Kondratyeva SA, Deviatiiarov RM, Miyata Y, Tokumoto S, et al. New group of transmembrane proteins associated with desiccation tolerance in the anhydrobiotic midge Polypedilum vanderplanki. Sci. Rep. [Internet]. Sci Rep; 2020 [cited 2021 Dec 1];10. Available from: https://pubmed.ncbi.nlm.nih.gov/32669703/ [DOI] [PMC free article] [PubMed]
  11. [12]Anderson JM, Hand SC. Transgenic expression of late embryogenesis abundant proteins improves tolerance to water stress in Drosophila melanogaster. J. Exp. Biol. [Internet]. J Exp Biol; 2021 [cited 2021 Dec 1];224. Available from: https://pubmed.ncbi.nlm.nih.gov/33431592/ [DOI] [PubMed]
  12. [13]Belott C, Janis B, Menze MA. Liquid-liquid phase separation promotes animal desiccation tolerance. Proc. Natl. Acad. Sci. U. S. A. [Internet]. Proc Natl Acad Sci U S A; 2020 [cited 2021 Dec 1];117:27676–84. Available from: https://pubmed.ncbi.nlm.nih.gov/33077592/ [DOI] [PMC free article] [PubMed]
  13. [14]Czernik M, Fidanza A, Luongo FP, Valbonetti L, Scapolo PA, Patrizio P, et al. Late embryogenesis abundant (LEA) proteins confer water stress tolerance to mammalian somatic cells. Cryobiology [Internet]. Cryobiology; 2020 [cited 2021 Dec 1];92:189–96. Available from: https://pubmed.ncbi.nlm.nih.gov/31952948/ [DOI] [PubMed]
  14. [15]Wakayama T, Yanagimachi R. Development of normal mice from oocytes injected with freeze-dried spermatozoa. Nat. Biotechnol. [Internet]. Nat Biotechnol; 1998 [cited 2021 Dec 1];16:639–41. Available from: https://pubmed.ncbi.nlm.nih.gov/9661196/ [DOI] [PubMed]
  15. [16]Ito D, Wakayama S, Emura R, Ooga M, Wakayama T. Mailing viable mouse freeze-dried spermatozoa on postcards. iScience [Internet]. iScience; 2021 [cited 2021 Dec 1];24:102815. Available from: https://pubmed.ncbi.nlm.nih.gov/34471856/ [DOI] [PMC free article] [PubMed]
  16. [17]Arav A, Idda A, Nieddu SM, Natan Y, Ledda S. High post-thaw survival of ram sperm after partial freeze-drying. J. Assist. Reprod. Genet. [Internet]. J Assist Reprod Genet; 2018 [cited 2021 Dec 1];35:1149–55. Available from: https://pubmed.ncbi.nlm.nih.gov/29536382/ [DOI] [PMC free article] [PubMed]
  17. [18]Anzalone DA, Palazzese L, Iuso D, Martino G, Loi P. Freeze-dried spermatozoa: an alternative biobanking option for endangered species. Anim. Reprod. Sci. [Internet]. Anim Reprod Sci; 2018 [cited 2021 Dec 1];190:85–93. Available from: https://pubmed.ncbi.nlm.nih.gov/29397252/ [DOI] [PubMed]
  18. [19]Choi YH, Varner DD, Love CC, Hartman DL, Hinrichs K. Production of live foals via intracytoplasmic injection of lyophilized sperm and sperm extract in the horse. Reproduction [Internet]. 2011 [cited 2017 Feb 1];142:529–38. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21846810 [DOI] [PubMed]
  19. [20]Keskintepe L, Pacholczyk G, Machnicka A, Norris K, Curuk MA, Khan I, et al. Bovine blastocyst development from oocytes injected with freeze-dried spermatozoa. Biol. Reprod. [Internet]. 2002 [cited 2017 Feb 1];67:409–15. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12135874 [DOI] [PubMed]
  20. [21]Keskintepe L, Eroglu A. Preservation of mammalian sperm by freeze-drying. Methods Mol. Biol. [Internet]. Humana Press Inc.; 2021 [cited 2021 Mar 28]. p. 721–30. Available from: https://pubmed.ncbi.nlm.nih.gov/32797445/ [DOI] [PubMed]
  21. [22]Gianaroli L, Magli MC, Stanghellini I, Crippa A, Crivello AM, Pescatori ES, et al. DNA integrity is maintained after freeze-drying of human spermatozoa. Fertil. Steril. [Internet]. Fertil Steril; 2012 [cited 2021 Dec 1];97. Available from: https://pubmed.ncbi.nlm.nih.gov/22386843/ [DOI] [PubMed]
  22. [23]Alexandrova S, Arav A, Hood K, Natan Y, Zhang J, Patrizio P. Successful production of normal euploid human blastocysts derived from sperm after partial freeze drying, rehydration and ICSI: towards developing a novel method for safe storage of biological samples. Fertil Steril 2020;114:e37–8
  23. [24]Dang-Nguyen TQ, Nguyen HT, Nguyen MT, Somfai T, Noguchi J, Kaneko H, et al. Maturation ability after transfer of freeze-dried germinal vesicles from porcine oocytes. Anim. Sci. J. [Internet]. Blackwell Publishing; 2018 [cited 2021 Mar 28];89:1253–60. Available from: https://pubmed.ncbi.nlm.nih.gov/29943513/ [DOI] [PubMed]
  24. [25]Bebbere D, Arav A, Nieddu SM, Burrai G Pietro, Succu S, Patrizio P, et al. Molecular and histological evaluation of sheep ovarian tissue subjected to lyophilization. Anim. 2021, Vol. 11, Page 3407 [Internet]. Multidisciplinary Digital Publishing Institute; 2021 [cited 2021 Dec 2];11:3407. Available from: https://www.mdpi.com/2076-2615/11/12/3407/htm [DOI] [PMC free article] [PubMed]
  25. [26]Elliott GD, Lee PC, Paramore E, Van Vorst M, Comizzoli P. Resilience of oocyte germinal vesicles to microwave-assisted drying in the domestic cat model. Biopreserv Biobank. [Internet]. 2015 [cited 2015 Dec 4];13:164–71. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26035005 [DOI] [PMC free article] [PubMed]
  26. [27]Wang S, Lee PC, Elsayed A, Zhang F, Zhang Y, Comizzoli P, et al. Preserving the female genome in trehalose glass at supra-zero temperatures: the relationship between moisture content and DNA damage in feline germinal vesicles. Cell. Mol. Bioeng. [Internet]. Cell Mol Bioeng; 2020 [cited 2021 Dec 28];14:101–12. Available from: https://pubmed.ncbi.nlm.nih.gov/33643469/ [DOI] [PMC free article] [PubMed]
  27. [28]Lee PC, Zahmel J, Jewgenow K, Comizzoli P. Desiccated cat spermatozoa retain DNA integrity and developmental potential after prolonged storage and shipping at non-cryogenic temperatures. J Assist Reprod Genet. J Assist Reprod Genet; 2021. Available from: https://pubmed.ncbi.nlm.nih.gov/34609666/ [DOI] [PMC free article] [PubMed]
  28. [29]Lee PC, Adams DM, Amelkina O, White KK, Amoretti LA, Whitaker MG, et al. Influence of microwave-assisted dehydration on morphological integrity and viability of cat ovarian tissues: first steps toward long-term preservation of complex biomaterials at supra-zero temperatures. PLoS One [Internet]. PLoS One; 2019 [cited 2021 Dec 28];14. Available from: https://pubmed.ncbi.nlm.nih.gov/31800613/ [DOI] [PMC free article] [PubMed]
  29. [30]Silva HVR, Da Silva AM, Lee PC, Brito BF, Silva AR, Da Silva LDM, et al. Influence of microwave-assisted drying on structural integrity and viability of testicular tissues from adult and prepubertal domestic cats. Biopreserv. Biobank. [Internet]. Biopreserv Biobank; 2020 [cited 2021 Dec 28];18:415–24. Available from: https://pubmed.ncbi.nlm.nih.gov/32780644/ [DOI] [PubMed]
  30. [31]Patrick JL, Elliott GD, Comizzoli P. Structural integrity and developmental potential of spermatozoa following microwave-assisted drying in the domestic cat model. Theriogenology [Internet]. Theriogenology; 2017 [cited 2021 Dec 28];103:36–43. Available from: https://pubmed.ncbi.nlm.nih.gov/28772113/ [DOI] [PubMed]
  31. [32]Palazzese L, Anzalone DA, Turri F, Faieta M, Donnadio A, Pizzi F, et al. Whole genome integrity and enhanced developmental potential in ram freeze-dried spermatozoa at mild sub-zero temperature. Sci. Rep. [Internet]. Sci Rep; 2020 [cited 2021 Dec 1];10. Available from: https://pubmed.ncbi.nlm.nih.gov/33139842/ [DOI] [PMC free article] [PubMed]

Cited by

Sorted by citations

Authors
Comizzoli, P., Loi, P., Patrizio, P., & Hubel, A.
Affiliations
  • Smithsonian Conservation Biology Institute (US)
  • University of Teramo (IT)
  • University of Miami (US)
  • University of Minnesota (US)
Corresponding author
Comizzoli, Pierre
Venue
Journal of Assisted Reproduction and Genetics
Published
2022-01-04
Volume
39
Issue
2
Pages
321-325
ISSN
  • 0740-7769 (ISSN-L)
  • 1058-0468
  • 1573-7330
OpenAlex
W4206568342
Cited by
12
References
0
Citations by year
2026: 2 · 2024: 2 · 2023: 1 · 2022: 6
FWCI
1.90
Type
journal article
Language
en
Open access
Locations
  • Journal of Assisted Reproduction and Genetics (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, cc-by)
  • UniTERAMO Research Catalog (University of Teramo) (submittedVersion)
  • Zenodo (CERN European Organization for Nuclear Research) (cc-by)
Funders
National Institutes of Health (R01OD023139)
Topics
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
  • Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Reproductive biology and impacts on aquatic species
Keywords
gamete preservation, spermatozoa, eggs, embryo, fertility preservation
MeSH terms
Germ Cells, Humans, Male, Spermatozoa, Temperature, Cryopreservation, Biological Specimen Banks, Fertility Preservation

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review