Journal of Reproductive Immunology
Volume 83, Issue 1 , Pages 8-13 , December 2009

The biological significance of detergent-resistant membranes in spermatozoa

  • Brett Nixon

      Affiliations

    • Reproductive Science Group, Discipline of Biological Sciences, School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW 2308, Australia
    • Corresponding Author InformationCorresponding author. Tel.: +61 2 4921 6977; fax: +61 2 4921 6308.
    • ,
  • R. John Aitken

      Affiliations

    • Reproductive Science Group, Discipline of Biological Sciences, School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW 2308, Australia
    • ARC Centre of Excellence in Biotechnology and Development, Discipline of Biological Sciences, School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW 2308, Australia

Received 11 November 2008 ,Revised 1 May 2009 ,Accepted 19 June 2009.

References 

  1. Abou-Haila A, Tulsiani DR. Evidence for the capacitation-associated membrane priming of mouse spermatozoa. Histochem. Cell Biol. 2003;119:179–187
  2. Asano A, Selvaraj V, Buttke DE, Nelson JL, Green KM, Evans JE, et al. Biochemical characterization of membrane fractions in murine sperm: identification of three distinct sub-types of membrane rafts. J. Cell. Physiol. 2009;218:537–548
  3. Asquith KL, Baleato RM, McLaughlin EA, Nixon B, Aitken RJ. Tyrosine phosphorylation activates surface chaperones facilitating sperm–zona recognition. J. Cell Sci. 2004;117:3645–3657
  4. Asquith KL, Harman AJ, McLaughlin EA, Nixon B, Aitken RJ. Localisation and significance of molecular chaperones. Heat Shock Protein 1 (Hspd1) and Tumor Rejection Antigen gp96 (Tra1), in the male reproductive tract and during capacitation and acrosome reaction. Biol. Reprod. 2005;72:328–337
  5. Boerke A, Tsai PS, Garcia-Gil N, Brewis IA, Gadella BM. Capacitation-dependent reorganization of microdomains in the apical sperm head plasma membrane: functional relationship with zona binding and the zona-induced acrosome reaction. Theriogenology. 2008;70:1188–1196
  6. Bou Khalil M, Chakrabandhu K, Xu H, Weerachatyanukul W, Buhr M, Berger T, et al. Sperm capacitation induces an increase in lipid rafts having zona pellucida binding ability and containing sulfogalactosylglycerolipid. Dev. Biol. 2006;290:220–235
  7. Brahmaraju M, Shoeb M, Laloraya M, Kumar PG. Spatio-temporal organization of Vam6P and SNAP on mouse spermatozoa and their involvement in sperm–zona pellucida interactions. Biochem. Biophys. Res. Commun. 2004;318:148–155
  8. Broquet AH, Thomas G, Masliah JI, Trugnan G, Bachelet M. Expression of the molecular chaperone Hsp70 in detergent-resistant microdomains correlates with its membrane delivery and release. J. Biol. Chem. 2003;278:21601–21606
  9. Bruckbauer A, James P, Zhou D, Yoon JW, Excell D, Korchev Y, et al. Nanopipette delivery of individual molecules to cellular compartments for single-molecule fluorescence tracking. Biophys. J. 2007;93:3120–3131
  10. Chakravarty S, Suraj K, Gupta SK. Baculovirus-expressed recombinant human zona pellucida glycoprotein-B induces acrosomal exocytosis in capacitated spermatozoa in addition to zona pellucida glycoprotein-C. Mol. Hum. Reprod. 2005;11:365–372
  11. Chen S, Bawa D, Besshoh S, Gurd JW, Brown IR. Association of heat shock proteins and neuronal membrane components with lipid rafts from the rat brain. J. Neurosci. Res. 2005;81:522–529
  12. Chiu PC, Wong BS, Chung MK, Lam KK, Pang RT, Lee KF, et al. Effects of native human zona pellucida glycoproteins 3 and 4 on acrosome reaction and zona pellucida binding of human spermatozoa. Biol. Reprod. 2008;79:869–877
  13. Clark GF, Dell A. Molecular models for murine sperm–egg binding. J. Biol. Chem. 2006;281:13853–13856
  14. De Blas GA, Roggero CM, Tomes CN, Mayorga LS. Dynamics of SNARE assembly and disassembly during sperm acrosomal exocytosis. PLoS Biol. 2005;3:e323
  15. de Vries KJ, Wiedmer T, Sims PJ, Gadella BM. Caspase-independent exposure of aminophospholipids and tyrosine phosphorylation in bicarbonate responsive human sperm cells. Biol. Reprod. 2003;68:2122–2134
  16. Elhyany S, Assa-Kunik E, Tsory S, Muller T, Fedida S, Segal S, et al. The integrity of cholesterol-enriched microdomains is essential for the constitutive high activity of protein kinase B in tumour cells. Biochem. Soc. Trans. 2004;32:837–839
  17. Ensslin MA, Shur BD. Identification of mouse sperm SED1, a bimotif EGF repeat and discoidin-domain protein involved in sperm–egg binding. Cell. 2003;114:405–417
  18. Foster LJ, De Hoog CL, Mann M. Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc. Natl. Acad. Sci. U.S.A. 2003;100:5813–5818
  19. Gadella BM, Flesch FM, van Golde LM, Colenbrander B. Dynamics in the membrane organization of the mammalian sperm cell and functionality in fertilization. Vet. Quart. 1999;21:142–146
  20. Gomez-Mouton C, Lacalle RA, Mira E, Jimenez-Baranda S, Barber DF, Carrera AC, et al. Dynamic redistribution of raft domains as an organizing platform for signaling during cell chemotaxis. J. Cell Biol. 2004;164:759–768
  21. James PS, Hennessy C, Berge T, Jones R. Compartmentalisation of the sperm plasma membrane: a FRAP FLIP and SPFI analysis of putative diffusion barriers on the sperm head. J. Cell Sci. 2004;117:6485–6495
  22. Jones R, James PS, Howes L, Bruckbauer A, Klenerman D. Supramolecular organization of the sperm plasma membrane during maturation and capacitation. Asian J. Androl. 2007;9:438–444
  23. Kim KS, Cha MC, Gerton GL. Mouse sperm protein sp56 is a component of the acrosomal matrix. Biol. Reprod. 2001;64:36–43
  24. Kurth BE, Klotz K, Flickinger CJ, Herr JC. Localization of sperm antigen SP-10 during the six stages of the cycle of the seminiferous epithelium in man. Biol. Reprod. 1991;44:814–821
  25. Lu Q, Shur BD. Sperm from beta 1,4-galactosyltransferase-null mice are refractory to ZP3-induced acrosome reactions and penetrate the zona pellucida poorly. Development. 1997;124:4121–4131
  26. Manes S, Viola A. Lipid rafts in lymphocyte activation and migration. Mol. Membr. Biol. 2006;23:59–69
  27. Munro S. Lipid rafts: elusive or illusive?. Cell. 2003;115:377–388
  28. Nikolajczyk BS, O’Rand MG. Characterization of rabbit testis beta-galactosidase and arylsulfatase A: purification and localization in spermatozoa during the acrosome reaction. Biol. Reprod. 1992;46:366–378
  29. Nixon B, Aitken RJ, McLaughlin EA. New insights into the molecular mechanisms of sperm–egg interaction. Cell. Mol. Life Sci. 2007;64:1805–1823
  30. Nixon B, Bielanowicz A, McLaughlin EA, Tanphaichitr N, Ensslin MA, Aitken RJ. Composition and significance of detergent resistant membranes in mouse spermatozoa. J. Cell. Physiol. 2009;218:122–134
  31. Pike LJ. Lipid rafts: bringing order to chaos. J. Lipid Res. 2003;44:655–667
  32. Pike LJ. Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. J. Lipid Res. 2006;47:1597–1598
  33. Schuck S, Honsho M, Ekroos K, Shevchenko A, Simons K. Resistance of cell membranes to different detergents. Proc. Natl. Acad. Sci. U.S.A. 2003;100:5795–5800
  34. Schulz JR, Sasaki JD, Vacquier VD. Increased association of synaptosome-associated protein of 25kDa with syntaxin and vesicle-associated membrane protein following acrosomal exocytosis of sea urchin sperm. J. Biol. Chem. 1998;273:24355–24359
  35. Selvaraj V, Asano A, Buttke DE, McElwee JL, Nelson JL, Wolff CA, et al Segregation of micron-scale membrane sub-domains in live murine sperm. J. Cell. Physiol. 2006;206:636–646
  36. Shadan S, James PS, Howes EA, Jones R. Cholesterol efflux alters lipid raft stability and distribution during capacitation of boar spermatozoa. Biol. Reprod. 2004;71:253–265
  37. Simons K, van Meer G. Lipid sorting in epithelial cells. Biochemistry. 1988;27:6197–6202
  38. Simons K, Vaz WL. Model systems, lipid rafts, and cell membranes. Annu. Rev. Biophys. Biomol. Struct. 2004;33:269–295
  39. Skudlarek MD, Abou-Haila A, Tulsiani DR. Rat spermatogenic cell beta-d-galactosidase: characterization, biosynthesis, and immunolocalization. Exp. Cell Res. 2000;261:139–149
  40. Sleight SB, Miranda PV, Plaskett NW, Maier B, Lysiak J, Scrable H, et al. Isolation and proteomic analysis of mouse sperm detergent-resistant membrane fractions: evidence for dissociation of lipid rafts during capacitation. Biol. Reprod. 2005;73:721–729
  41. Srivastava S, Kaur R, Bawa SR, Phadke RS, Bains HK, Sehgal S, et al. Maturation, capacitation, and metabolism of goat spermatozoa using magnetic resonance methods. Andrologia. 1993;25:223–227
  42. Tanphaichitr N, Carmona E, Bou Khalil M, Xu H, Berger T, Gerton GL. New insights into sperm–zona pellucida interaction: involvement of sperm lipid rafts. Front. Biosci. 2007;12:1748–1766
  43. Tomes CN, Michaut M, De Blas G, Visconti P, Matti U, Mayorga LS. SNARE complex assembly is required for human sperm acrosome reaction. Dev. Biol. 2002;243:326–338
  44. Travis AJ, Merdiushev T, Vargas LA, Jones BH, Purdon MA, Nipper RW, et al. Expression and localization of caveolin-1, and the presence of membrane rafts, in mouse and Guinea pig spermatozoa. Dev. Biol. 2001;240:599–610
  45. Tsai PS, de Vries KJ, de Boer-Brouwer M, Garcia-Gil N, van Gestel RA, Colenbrander B, et al. Syntaxin and VAMP association with lipid rafts depends on cholesterol depletion in capacitating sperm cells. Mol. Membr. Biol. 2007;24:313–324
  46. van Gestel RA, Brewis IA, Ashton PR, Brouwers JF, Gadella BM. Multiple proteins present in purified porcine sperm apical plasma membranes interact with the zona pellucida of the oocyte. Mol. Hum. Reprod. 2007;13:445–454
  47. van Gestel RA, Brewis IA, Ashton PR, Helms JB, Brouwers JF, Gadella BM. Capacitation-dependent concentration of lipid rafts in the apical ridge head area of porcine sperm cells. Mol. Hum. Reprod. 2005;11:583–590
  48. Wassarman PM, Litscher ES. Towards the molecular basis of sperm and egg interaction during mammalian fertilization. Cells Tissues Organs. 2001;168:36–45
  49. Zhao L, Shi X, Li L, Miller DJ. Dynamin 2 associates with complexins and is found in the acrosomal region of mammalian sperm. Mol. Reprod. Dev. 2007;74:750–757

PII: S0165-0378(09)00457-4

doi: 10.1016/j.jri.2009.06.258

Journal of Reproductive Immunology
Volume 83, Issue 1 , Pages 8-13 , December 2009

Article Tools

* Image Usage & Resolution