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PMID: 24941006 Published · epublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Comparative proteome analysis of cryopreserved flagella and head plasma membrane proteins from sea bream spermatozoa: effect of antifreeze proteins.

PloS one ·Vol. 9 ·No. 6 ·2014-00-00 ·Pages e99992

Zilli L, Beirão J, Schiavone R, Herraez MP, Gnoni A, Vilella S

Abstract

Cryopreservation induces injuries to fish spermatozoa that in turn affect sperm quality in terms of fertilization ability, motility, DNA and protein integrity and larval survival. To reduce the loss of sperm quality due to freezing-thawing, it is necessary to improve these procedures. In the present study we investigated the ability of two antifreeze proteins (AFPI and AFPIII) to reduce the loss of quality of sea bream spermatozoa due to cryopreservation. To do so, we compared viability, motility, straight-line velocity and curvilinear velocity of fresh and (AFPs)-cryopreserved spermatozoa. AFPIII addition to cryopreservation medium improved viability, motility and straight-line velocity with respect to DMSO or DMSO plus AFPI. To clarify the molecular mechanism(s) underlying these findings, the protein profile of two different cryopreserved sperm domains, flagella and head plasma membranes, was analysed. The protein profiles differed between fresh and frozen-thawed semen and results of the image analysis demonstrated that, after cryopreservation, out of 270 proteins 12 were decreased and 7 were increased in isolated flagella, and out of 150 proteins 6 showed a significant decrease and 4 showed a significant increase in head membranes. Mass spectrometry analysis identified 6 proteins (4 from isolated flagella and 2 present both in flagella and head plasma membranes) within the protein spots affected by the freezing-thawing procedure. 3 out of 4 proteins from isolated flagella were involved in the sperm bioenergetic system. Our results indicate that the ability of AFPIII to protect sea bream sperm quality can be, at least in part, ascribed to reducing changes in the sperm protein profile occurring during the freezing-thawing procedure. Our results clearly demonstrated that AFPIII addition to cryopreservation medium improved the protection against freezing respect to DMSO or DMSO plus AFPI. In addition we propose specific proteins of spermatozoa as markers related to the procedures of fish sperm cryopreservation.

MeSH Terms
Animals Antifreeze Proteins/pharmacology Cell Membrane/drug effects,metabolism Cell Survival/drug effects Cryopreservation Cryoprotective Agents/pharmacology Electrophoresis, Gel, Two-Dimensional Fertilization/drug effects Fish Proteins/metabolism Flagella/metabolism Male Mass Spectrometry Membrane Proteins/metabolism Proteome/metabolism Proteomics/methods Sea Bream/metabolism Sperm Head/drug effects,metabolism Sperm Motility/drug effects
Chemicals
Antifreeze Proteins Cryoprotective Agents Fish Proteins Membrane Proteins Proteome
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Zilli Loredana
Department of Biological and Environmental Sciences and Technologies, University of Salento, Lecce, Italy.
Beirão José
Department of Molecular Biology, University of León, León, Spain.
Schiavone Roberta
Department of Biological and Environmental Sciences and Technologies, University of Salento, Lecce, Italy.
Herraez Maria Paz
Department of Molecular Biology, University of León, León, Spain.
Gnoni Antonio
Department of Basic Medical Sciences, Neurosciences and Sense Organs, University of Bari, Bari, Italy.
Vilella Sebastiano
Department of Biological and Environmental Sciences and Technologies, University of Salento, Lecce, Italy.
References (42)
42 references, click to expand
  1. Relationship between sperm ATP content and motility of carp spermatozoa.
    J Cell Sci. 1995 Feb;108 ( Pt 2):747-53 PMID: 7769016
  2. Mitochondrial proteome analysis reveals depression of the Ndufs3 subunit and activity of complex I in diabetic rat brain.
    J Proteomics. 2012 Apr 18;75(8):2331-41 PMID: 22387129
  3. Human spermatozoal RNAs.
    Fertil Steril. 2012 Feb;97(2):275-81 PMID: 22289287
  4. Hypothermic protection--a fundamental property of "antifreeze" proteins.
    Biochem Biophys Res Commun. 1991 Oct 31;180(2):566-71 PMID: 1953726
  5. Chemical and physical properties of freezing point-depressing glycoproteins from Antarctic fishes.
    J Biol Chem. 1970 Jun 10;245(11):2901-8 PMID: 5488456
  6. A mechanism for stabilization of membranes at low temperatures by an antifreeze protein.
    Biophys J. 2002 Feb;82(2):874-81 PMID: 11806929
  7. Properties, potentials, and prospects of antifreeze proteins.
    Crit Rev Biotechnol. 2008;28(1):57-82 PMID: 18322856
  8. Cryopreservation-induced decrease in heat-shock protein 90 in human spermatozoa and its mechanism.
    Asian J Androl. 2003 Mar;5(1):43-6 PMID: 12647002
  9. Evaluation of DNA damage as a quality marker for rainbow trout sperm cryopreservation and use of LDL as cryoprotectant.
    Theriogenology. 2010 Jul 15;74(2):282-9 PMID: 20494425
  10. Superoxide dismutase isoenzymes in human seminal plasma and spermatozoa.
    Mol Hum Reprod. 1997 Dec;3(12):1061-6 PMID: 9464851
  11. Evaluation of DNA damage in Dicentrarchus labrax sperm following cryopreservation.
    Cryobiology. 2003 Dec;47(3):227-35 PMID: 14697734
  12. Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility.
    Proc Natl Acad Sci U S A. 2004 Nov 23;101(47):16501-6 PMID: 15546993
  13. Cryopreservation of sperm in common carp Cyprinus carpio: sperm motility and hatching success of embryos.
    Cryobiology. 2000 Nov;41(3):241-50 PMID: 11161556
  14. Improving sperm cryopreservation with antifreeze proteins: effect on gilthead seabream (Sparus aurata) plasma membrane lipids.
    Biol Reprod. 2012 Feb 29;86(2):59 PMID: 22088915
  15. Expression and compartmentalisation of the glycolytic enzymes GAPDH and pyruvate kinase in boar spermatogenesis.
    Reprod Fertil Dev. 2008;20(6):713-23 PMID: 18671919
  16. Changes in sperm quality and lipid composition during cryopreservation of boar semen.
    Theriogenology. 2005 Jan 15;63(2):411-21 PMID: 15626408
  17. Cryopreservation of tench, Tinca tinca, sperm: Sperm motility and hatching success of embryos.
    Theriogenology. 2007 Mar 15;67(5):931-40 PMID: 17182092
  18. Evaluation of oxidative DNA damage promoted by storage in sperm from sex-reversed rainbow trout.
    Theriogenology. 2009 Mar 1;71(4):605-13 PMID: 19117601
  19. Cryopreservation of Atlantic croaker spermatozoa: evaluation of morphological changes.
    J Exp Zool. 1992 Dec 15;264(4):444-53 PMID: 1460442
  20. A suite of novel human spermatozoal RNAs.
    J Androl. 2005 Jan-Feb;26(1):70-4 PMID: 15611569
  21. A new technique for the precise location of lactate and malate dehydrogenases in goat, boar and water buffalo spermatozoa using gel incubation film.
    J Reprod Fertil. 1992 May;95(1):201-9 PMID: 1625237
  22. Spontaneous lipid peroxidation in rabbit epididymal spermatozoa: its effect on sperm motility.
    Biol Reprod. 1982 Dec;27(5):1102-8 PMID: 6297627
  23. Evaluation of gilthead sea bream, Sparus aurata, sperm quality after cryopreservation in 5 ml macrotubes.
    Cryobiology. 2005 Jun;50(3):273-84 PMID: 15925579
  24. Effect of cryopreservation on phosphorylation state of proteins involved in sperm motility initiation in sea bream.
    Cryobiology. 2008 Oct;57(2):150-5 PMID: 18700136
  25. Control of flatfish sperm motility by CO2 and carbonic anhydrase.
    Cell Motil Cytoskeleton. 2003 Jul;55(3):174-87 PMID: 12789662
  26. Substantial decrease of heat-shock protein 90 precedes the decline of sperm motility during cooling of boar spermatozoa.
    Theriogenology. 1999 Apr 1;51(5):1007-16 PMID: 10729022
  27. The effects of antifreeze peptide III (AFP) and insulin transferrin selenium (ITS) on cryopreservation of chimpanzee (Pan troglodytes) spermatozoa.
    J Androl. 1998 Mar-Apr;19(2):207-14 PMID: 9570745
  28. Lipid peroxidation in human spermatozoa as related to midpiece abnormalities and motility.
    Gamete Res. 1989 Oct;24(2):127-34 PMID: 2793053
  29. Applications of type I antifreeze proteins: studies with model membranes & cryoprotectant properties.
    Curr Protein Pept Sci. 2006 Dec;7(6):509-22 PMID: 17168784
  30. Effect of cryopreservation on fish sperm subpopulations.
    Cryobiology. 2011 Feb;62(1):22-31 PMID: 21112321
  31. A comprehensive evaluation of the effects and mechanisms of antifreeze proteins during low-temperature preservation.
    Cryobiology. 2000 Aug;41(1):1-9 PMID: 11017755
  32. Effect of sperm cryopreservation on sperm DNA stability and progeny development in rainbow trout.
    Mol Reprod Dev. 2001 Nov;60(3):397-404 PMID: 11599051
  33. Complementary deoxyribonucleic acid cloning and characterization of a putative human axonemal dynein light chain gene.
    J Clin Endocrinol Metab. 1997 Sep;82(9):3047-53 PMID: 9284741
  34. Characterization of sperm plasma membrane properties after cholesterol modification: consequences for cryopreservation of rainbow trout spermatozoa.
    Biol Reprod. 2008 Mar;78(3):390-9 PMID: 18003944
  35. Neutron structure of type-III antifreeze protein allows the reconstruction of AFP-ice interface.
    J Mol Recognit. 2011 Jul-Aug;24(4):724-32 PMID: 21472814
  36. Effect of cryopreservation on sea bass sperm proteins.
    Biol Reprod. 2005 May;72(5):1262-7 PMID: 15659707
  37. Cryopreservation alters the levels of the bull sperm surface protein P25b.
    J Androl. 2000 Sep-Oct;21(5):700-7 PMID: 10975417
  38. Stallion sperm transcriptome comprises functionally coherent coding and regulatory RNAs as revealed by microarray analysis and RNA-seq.
    PLoS One. 2013;8(2):e56535 PMID: 23409192
  39. Type I antifreeze protein attenuates cell recoveries following cryopreservation.
    Transplant Proc. 1993 Dec;25(6):3182-4 PMID: 8266508
  40. Impact of antifreeze proteins and antifreeze glycoproteins on bovine sperm during freeze-thaw.
    Theriogenology. 2006 Nov;66(8):1894-900 PMID: 16777208
  41. Lipid rafts: heterogeneity on the high seas.
    Biochem J. 2004 Mar 1;378(Pt 2):281-92 PMID: 14662007
  42. Cryopreservation of seabream (Sparus aurata) spermatozoa.
    Cryobiology. 2000 Feb;40(1):46-53 PMID: 10679149
Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
Published
2014-00-00
Epub
2014-00-18
Pages
e99992
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC4062426
Subset
IM
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