Reorganization of lipid rafts during capacitation of human sperm

Biology of Reproduction

Volumn 71, Issue 4, 2004, Pages 1367-1373

  Cross, Nicholas L ^a  

^a OKLAHOMA STATE UNIVERSITY   (United States)

Author keywords

Acrosome reaction; Fertilization; Sperm; Sperm capacitation

Indexed keywords

CD59 ANTIGEN; FLOTILLIN 2; GANGLIOSIDE GM1; MEMBRANE LIPID; MEMBRANE PROTEIN; STEROL; UNCLASSIFIED DRUG;

ACROSOME; ACROSOME REACTION; ANTIGEN EXPRESSION; ARTICLE; CELL MEMBRANE RESISTANCE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; MALE; MEMBRANE STABILIZATION; MEMBRANE STRUCTURE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STABILITY; SPERMATOZOON; SPERMATOZOON CAPACITATION; SPERMATOZOON MIDPIECE; SPERMATOZOON TAIL; SURFACE PROPERTY; UPREGULATION;

ACROSOME REACTION; ANTIGENS, CD59; G(M1) GANGLIOSIDE; HUMANS; LIPID METABOLISM; MALE; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; SPERM CAPACITATION; SPERMATOZOA;

MAMMALIA;

EID: 4544342119     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.104.030502     Document Type: Article

References (60)

1. Yanagimachi R. Mammalian fertilization. In: Knobil E, Neill JD (eds.), The Physiology of Reproduction, 2nd ed. New York: Raven Press; 1994:189-317.
2. Cross NL. Role of cholesterol in sperm capacitation. Biol Reprod 1998; 59:7-11.
3. Flesch FM, Gadella BM. Dynamics of the mammalian sperm plasma membrane in the process of fertilization. Biochim Biophys Acta 2000; 1469:197-235.
4. Zarintash RJ, Cross NL. Unesterified cholesterol content of human sperm regulates the response of the acrosome to the agonist, progesterone. Biol Reprod 1996; 55:19-24.
5. Cross NL. Effect of cholesterol and other sterols on human sperm acrosomal responsiveness. Mol Reprod Dev 1996; 45:212-217.
6. Visconti PE, Ning X, Fornes MW, Alvarez JG, Stein P, Connors SA, Kopf GS. Cholesterol efflux-mediated signal transduction in mammalian sperm: cholesterol release signals an increase in protein tyrosine phosphorylation during mouse sperm capacitation. Dev Biol 1999; 214:429-443.
7. Davis BK. Influence of serum albumin on the fertilizing ability in vitro of rat spermatozoa. Proc Soc Exp Biol Med 1976; 151:240-243.
8. Davis BK. Inhibitory effect of synthetic phospholipid vesicles containing cholesterol on the fertilizing ability of rabbit spermatozoa. Proc Soc Exp Biol Med 1976; 152:257-261.
9. Go KJ, Wolf DP. Albumin-mediated changes in sperm sterol content during capacitation. Biol Reprod 1985; 32:145-153.
10. Cross NL, Razy-Faulkner P. Control of human sperm intracellular pH by cholesterol and its relationship to the response of the acrosome to progesterone. Biol Reprod 1997; 56:1169-1174.
11. Parrish JJ, Susko-Parrish JL, First NL. Capacitation of bovine sperm by heparin: inhibitory effect of glucose and role of intracellular pH. Biol Reprod 1989; 41:683-699.
12. --dependent and arylaminobenzoate-dependent regulatory mechanisms and characterization of their roles in sperm capacitation. Dev Biol 1996; 173:510-520.
13. Parks JE, Arion JW, Foote RH. Lipids of plasma membrane and outer acrosomal membranes from bovine spermatozoa. Biol Reprod 1987; 37:1249-1258.
14. Tesarik J, Flechon JE. Distribution of sterols and anionic lipids in human sperm plasma membrane: effects on in vitro capacitation. J Ultrastruct Mol Struct Res 1986; 97:227-237.
15. Davis BK. Inhibition of fertilizing capacity in mammalian spermatozoa by natural and synthetic vesicles. In: Kabara JJ (ed.), Symposium on the Pharmacological Effects of Lipids. Champaign, IL: The American Oil Chemists Society; 1978:145-157.
16. Nimmo MR, Cross NL. Structural features of sterols required to inhibit human sperm capacitation. Biol Reprod 2003; 68:1308-1317.
17. Yeagle PL. Cholesterol and the cell membrane. Biochim Biophys Acta 1985; 822:267-287.
18. Cross NL. Decrease in order of human sperm lipids during capacitation. Biol Reprod 2003; 69:529-534.
19. 2, an effector of capacitation induces a rapid and reversible change in the lipid architecture of boar sperm plasma membranes. Mol Reprod Dev 1996; 45:378-391.
20. Brown DA, London E. Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 1998; 14:111-136.
21. Brown DA, London E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J Biol Chem 2000; 275:17221-17224.
22. Simons K, Ikonen E. Functional rafts in cell membranes. Nature 1997; 387:569-572.
23. Simons K, Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 2000; 1:31-39.
24. Gidwani A, Holowka D, Baird B. Fluorescence anisotropy measurements of lipid order in plasma membranes and lipid rafts from RBL-2H3 mast cells. Biochemistry 2001; 40:12422-12429.
25. Ohta K, Sato C, Matsuda T, Toriyama M, Lennarz WJ, Kitajima K. Isolation and characterization of low density detergent-insoluble membrane (LD-DIM) fraction from sea urchin sperm. Biochem Biophys Res Commun 1999; 258:616-623.
26. Travis AJ, Merdiushev T, Vargas LA, Jones BH, Purdon MA, Nipper RW, Galatioto J, Moss SB, Hunnicutt GR, Kopf GS. Expression and localization of caveolin-1, and the presence of membrane rafts, in mouse and guinea pig spermatozoa. Dev Biol 2001; 240:599-610.
27. 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.
28. Fenichel P, Cervoni F, Hofmann P, Deckert M, Emiliozzi C, Hsi BL, Rossi B. Expression of the complement regulatory protein CD59 on human spermatozoa: characterization and role in gametic interaction. Mol Reprod Dev 1994; 38:338-346.
29. Harder T, Simons K. Clusters of glycolipid and glycosylphosphatidylinositol-anchored proteins in lymphoid cells: accumulation of actin regulated by local tyrosine phosphorylation. Eur J Immunol 1999; 29: 556-562.
30. Horejsi V, Drbal K, Cebecauer M, Cerny J, Brdicka T, Angelisova P, Stockinger H. GPI-microdomains: a role in signaling via immunoreceptors. Immunol Today 1999; 20:356-361.
31. Nichols BJ, Kenworthy AK, Polishchuk RS, Lodge R, Roberts TH, Hirschberg K, Phair RD, Lippincott-Schwartz J. Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J Cell Biol 2001; 153:529-541.
32. Bickel PE, Scherer PE, Schnitzer JE, Oh P, Lisanti MP, Lodish HE. Flotillin and epidermal surface antigen define a new family of caveolae-associated integral membrane proteins. J Biol Chem 1997; 272: 13793-13802.
33. Bickel PE. Lipid rafts and insulin signaling. J Physiol Endocrinol Metab 2002; 282:E1-E10.
34. Neumann-Giesen C, Falkenbach B, Beicht P, Claasen S, Luers G, Stuermer CA, Herzog V, Tikkanen R. Membrane and raft association of reggie-1/flotillin-2: role of myristoylation, palmitoylation and oligomerization and induction of filopodia by overexpression. Biochem J 2004; 378:509-518.
35. Siiteri JE, Dandekar P, Meizel S. Human sperm acrosome reaction-initiating activity associated with the human cumulus oophorus and mural granulosa cells. J Exp Zool 1998; 246:71-80.
36. Cross NL. Multiple effects of seminal plasma on the acrosome reaction of human sperm. Mol Reprod Dev 1993; 35:316-323.
37. Suarez SS, Wolf DP, Meizel S. Induction of the acrosome reaction in human spermatozoa by a fraction of human follicular fluid. Gamete Res 1986; 14:107-121.
38. 2 is not required for zona pellucida- or progesterone-induced acrosomal exocytosis of mouse spermatozoa but is essential for capacitation. Biol Reprod 1995; 52:540-546.
39. Schuffner AA, Bastiaan HS, Duran HE, Lin ZY, Morshedi M, Franken DR, Oehninger S. Zona pellucida-induced, acrosome reaction in human sperm: dependency on activation of pertussis toxin-sensitive G(i) protein and extracellular calcium, and priming effect of progesterone and follicular fluid. Mol Hum Reprod 2002; 8:722-727.
40. Harder T, Scheiffele P, Verkade P, Simons K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol 1998; 141:929-942.
41. Hansen GH, Niels-Christiansen L-L, Thorsen E, Immerdal L, Danielsen EM. Cholesterol depletion of enterocytes: effect on the Golgi complex and apical membrane trafficking. J Biol Chem 2000; 275: 5136-5142.
42. Cross NL. Effect of cholesterol and other sterols on human sperm acrosomal responsiveness. Mol Reprod Dev 1996; 45:212-217.
43. Purohit SB, Laloraya M, Kumar P. Acrosome reaction inducers impose alterations in repulsive strain and hydration barrier in human sperm membranes. Biochem Mol Biol Int 1998; 45:227-235.
44. Davis BK, Byrne R, Hungund B. Studies on the mechanism of capacitation. II. Evidence for lipid transfer between plasma membrane of rat sperm and serum albumin during capacitation in vitro. Biochim Biophys Acta 1979; 558:257-266.
45. Stojanoff A, Bourne H, Andrews AG, Hyne RV. Phospholipid composition of isolated guinea pig sperm outer acrosomal membrane and plasma membrane during capacitation in vitro. Gamete Res 1988; 21: 297-311.
46. 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.
47. Gadella BM, Lopes-Cardozo M, van Golde LM, Colenbrander B, Gadella TW Jr. Glycolipid migration from the apical to the equatorial subdomains of the sperm head plasma membrane precedes the acrosome reaction: evidence for a primary capacitation event in boar spermatozoa. J Cell Sci 1995; 108:935-946.
48. Xu X, London E. The effect of sterol structure on membrane lipid domains reveals how cholesterol can induce lipid domain formation. Biochemistry 2000; 39:843-849.
49. Xu X, Bittmann R, Duportail G, Heissler D, Vilcheze C, London E. Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). J Biol Chem 2001; 276:33540-33546.
50. 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.
51. Miller-Podraza H, Bradley RM, Fishman PH. Biosynthesis and localization of gangliosides in cultured cells. Biochemistry 1982; 21:3260-3265.
52. Yeung CH, Perez-Sanchez F, Schroter S, Kirchhoff C, Cooper TG. Changes of the major sperm maturation-associated epididymal protein HE5 (CD52) on human ejaculated spermatozoa during incubation. Mol Hum Reprod 2001; 7:617-624.
53. Sabeur K, Cherr GN, Yudin AI, Primakoff P, Li M, Overstreet JW. The PH-20 protein in human spermatozoa. J Androl 1997; 18:151-158.
54. Roberts KP, Wamstad JA, Ensrud KM, Hamilton DW. Inhibition of capacitation-associated tyrosine phosphorylation signaling in rat sperm by epididymal protein Crisp-1. Biol Reprod 2003; 69:572-581.
55. Trevino CL, Serrano CJ, Beltran C, Felix R, Darszon A. Identification of mouse trp homologs and lipid rafts from spermatogenic cells and sperm. FEBS Lett 2001; 509:119-125.
56. Schnitzer JE, McIntosh DP, Dvorak AM, Liu J, Oh P. Separation of caveolae from associated microdomains of GPI-anchored proteins. Science 1995; 269:1435-1439.
57. Millán J, Quaidi M, Alonso MA. Segregation of co-stimulatory components into specific T cell surface lipid rafts. Eur J Immunol 2001; 31:467-473.
58. Janes PW, Ley SC, Magee AI. Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J Cell Biol 1999; 147:447-461.
59. Stuermer CA, Lang DM, Kirsch F, Wiechers M, Deininger SO, Plattner H. Glycosylphosphatidyl inositol-anchored proteins and fyn kinase assemble in noncaveolar plasma membrane microdomains defined by reggie-1 and -2. Mol Biol Cell 2001; 12:3031-3045.
60. Rajendran L, Masilamani M, Solomon S, Tikkanen R, Stuermer CA, Plattner H, Illges H. Asymmetric localization of flotillins/reggies in preassembled platforms confers inherent polarity to hematopoietic cells. Proc Natl Acad Sci U S A 2003; 100:8241-8246.