Ultrastructure and lipid composition of detergent-resistant membranes derived from mammalian sperm and two types of epithelial cells

Cell and Tissue Research

Volumn 363, Issue 1, 2016, Pages 129-145

  van Gestel, Renske A ^a   Brouwers, Jos F ^a   Ultee, Anton ^b   Helms, J Bernd ^a   Gadella, Bart M ^a,c  

^a UTRECHT UNIVERSITY   (Netherlands)

^b Department of Pathology ^*  (Netherlands)

^c Faculty of Veterinary Medicine   (Netherlands)

Author keywords

Cholesterol; Detergent resistant membranes; Epithelial cell; Glycolipids; Lipid rafts; Phospholipids; Sperm; Ultrastructure

Indexed keywords

CERAMIDE; CERAMIDE DERIVATIVE; CHOLESTEROL; DETERGENT; GLYCEROLIPID; METHYL BETA CYCLODEXTRIN; PHOSPHATIDYLETHANOLAMINE; SEMINOLIPID; SPHINGOLIPID; SPHINGOMYELIN; SULFATIDE; UNCLASSIFIED DRUG; PHOSPHOLIPID;

ANIMAL CELL; CELL MEMBRANE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; DETERGENT RESISTANT MEMBRANE; EPITHELIUM CELL; LAMELLAR BODY; LIPID ANALYSIS; LIPID COMPOSITION; LIPID RAFT; MALE; MDCK CELL LINE; MEMBRANE STRUCTURE; NONHUMAN; PIG; PRIORITY JOURNAL; PROCESS MONITORING; PROTEIN LIPID INTERACTION; REVIEW; SOLUBILITY; SPERM; STOICHIOMETRY; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; CHEMISTRY; CYTOLOGY; DOG; SPERMATOZOON; ULTRASTRUCTURE;

ANIMALS; CHOLESTEROL; DETERGENTS; DOGS; EPITHELIAL CELLS; MALE; MEMBRANE MICRODOMAINS; PHOSPHOLIPIDS; SPERMATOZOA; SPHINGOLIPIDS; SPHINGOMYELINS; SWINE;

EID: 84952989972     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-015-2272-y     Document Type: Review

References (108)

1. Ackermann F, Zitranski N, Heydecke D, Wilhelm B, Gudermann T, Boekhoff I (2008) The multi-PDZ domain protein MUPP1 as a lipid raft-associated scaffolding protein controlling the acrosome reaction in mammalian spermatozoa. J Cell Physiol 214:757–768
2. Ahmed SN, Brown DA, London E (1997) On the origin of sphingolipid/cholesterol-rich detergent-insoluble cell membranes: physiological concentrations of cholesterol and sphingolipid induce formation of a detergent-insoluble, liquid-ordered lipid phase in model membranes. Biochemistry 36:10944–10953
3. Aitken RJ, Nixon B (2013) Sperm capacitation a distant landscape glimpsed but unexplored. Mol Hum Reprod 19:785–793
4. Anderson RG, Jacobson K (2002) A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296:1821–1825
5. Asano A, Selvaraj V, Buttke DE, Nelson JL, Green KM, Evans JE, Travis AJ (2009) Biochemical characterization of membrane fractions in murine sperm: identification of three distinct sub-types of membrane rafts. J Cell Physiol 218:537–548
6. Asano A, Nelson-Harrington JL, Travis AJ (2013a) Phospholipase B is activated in response to sterol removal and stimulates acrosome exocytosis in murine sperm. J Biol Chem 288:28104–28115
7. Asano A, Nelson-Harrington JL, Travis AJ (2013b) Membrane rafts regulate phospholipase B activation in murine sperm. Commun Integr Biol 6:e27362
8. Baltiérrez-Hoyos R, Roa-Espitia AL, Hernández-González EO (2012) The association between CDC42 and caveolin-1 is involved in the regulation of capacitation and acrosome reaction of guinea pig and mouse sperm. Reproduction 144:123–134
9. Bartlett GR (1959) Colorimetric assay methods for free and phosphorylated glyceric acids. J Biol Chem 234:469–471
10. Belmonte SA, López CI, Roggero CM, De Blas GA, Tomes CN, Mayorga LS (2005) Cholesterol content regulates acrosomal exocytosis by enhancing Rab3A plasma membrane association. Dev Biol 285:393–408
11. Bleijerveld OB, Brouwers JF, Vaandrager AB, Helms JB, Houweling M (2007) The CDP-ethanolamine pathway and phosphatidylserine decarboxylation generate different phosphatidylethanolamine molecular species. J Biol Chem 282:28362–28372
12. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917
13. Boerke A, Brouwers JF, Olkkonen VM, van de Lest CH, Sostaric E, Schoevers EJ, Helms JB, Gadella BM (2013) Involvement of bicarbonate-induced radical signaling in oxysterol formation and sterol depletion of capacitating mammalian sperm during in vitro fertilization. Biol Reprod 88:21
14. Botto L, Bernabò N, Palestini P, Barboni B (2010) Bicarbonate induces membrane reorganization and CBR1 and TRPV1 endocannabinoid receptor migration in lipid microdomains in capacitating boar spermatozoa. J Membr Biol 238:33–41
15. Brachet A, Norwood S, Brouwers JF, Palomer E, Helms JB, Dotti CG, Esteban JA (2015) LTP-triggered cholesterol redistribution activates Cdc42 and drives AMPA receptor synaptic delivery. J Cell Biol 208:791–806
16. Bromfield EG, Nixon B (2013) The function of chaperone proteins in the assemblage of protein complexes involved in gamete adhesion and fusion processes. Reproduction 45:R31–42
17. Bromfield EG, Aitken RJ, Gibb Z, Lambourne SR, Nixon B (2013) Capacitation in the presence of methyl-β-cyclodextrin results in enhanced zona pellucida-binding ability of stallion spermatozoa. Reproduction 147:153–166
18. Brouwers JF, Gadella BM, van Golde LM, Tielens AG (1988) Quantitative analysis of phosphatidylcholine molecular species using HPLC and light scattering detection. J Lipid Res 39:344–353
19. Brouwers JF, Versluis C, van Golde LM, Tielens AG (1998) 5-octadecenoic acid: evidence for a novel type of fatty acid modification in schistosomes. Biochem J 334:315–319
20. Brouwers JF, Vernooij EA, Tielens AG, van Golde LM (1999) Rapid separation and identification of phosphatidylethanolamine molecular species. J Lipid Res 40:164–169
21. Brouwers JF, Boerke A, Silva PF, Garcia-Gil N, van Gestel RA, Helms JB, van de Lest CH, Gadella BM (2011) Mass spectrometric detection of cholesterol oxidation in bovine sperm. Biol Reprod 85:128–36
22. Brown RE (1998) Sphingolipid organization in biomembranes: what physical studies of model membranes reveal. J Cell Sci 111:1–9
23. Brown DA (2006) Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology 21:430–439
24. Brown DA, London E (1998) Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 14:111–136
25. Brown DA, London E (2000) Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J Biol Chem 275:17221–17224
26. Caballero J, Frenette G, D’Amours O, Belleannée C, Lacroix-Pepin N, Robert C, Sullivan R (2012) Bovine sperm raft membrane associated glioma pathogenesis-related 1-like protein 1 (GliPr1L1) is modified during the epididymal transit and is potentially involved in sperm binding to the zonapellucida. J Cell Physiol 227:3876–886
27. Chen Y, Qin J, Chen ZW (2008) Fluorescence-topographic NSOM directly visualizes peak-valley polarities of GM1/GM3 rafts in cell membrane fluctuations. J Lipid Res 49:2268–2275
28. Crane JM, Tamm LK (2004) Role of cholesterol in the formation and nature of lipid rafts in planar and spherical model membranes. Biophys J 86:2965–2979
29. Cullis PR, Fenske DB, Hope MJ (1996) In: Vance DE, Vance J (eds) Biochemistry of lipids, lipoproteins and membranes. Elsevier, Amsterdam, pp 1–41
30. de Almeida RF, Fedorov A, Prieto (2003) Sphingomyelin/phosphatidylcholine/ cholesterol phase diagram: boundaries and composition of lipid rafts. Biophys J 85:2406–2416
31. DeLong CJ, Shen YJ, Thomas MJ, Cui Z (1999) Molecular distinction of phosphatidylcholine synthesis between the CDP-choline pathway and phosphatidylethanolamine methylation pathway. J Biol Chem 274:29683–29688
32. Dermine JF, Duclos S, Garin J, St Louis F, Rea S, Parton RG, Desjardins M (2001) Flotillin-1-enriched lipid raft domains accumulate on maturing phagosomes. J Biol Chem 276:18507–18512
33. Diaz-Rohrer BB, Levental KR, Simons K, Levental I (2014) Membrane raft association is a determinant of plasma membrane localization. Proc Natl Acad Sci U S A 111:8500–8505
34. Dietrich C, Yang B, Fujiwara T, Kusumi A, Jacobson K (2002) Relationship of lipid rafts to transient confinement zones detected by single particle tracking. Biophys J 82:274–284
35. Evans RW, Weaver DE, Clegg ED (1980) Diacyl, alkenyl, and alkyl ether phospholipids in ejaculated, in utero-, and in vitro-incubated porcine spermatozoa. J Lipid Res 21:223–228
36. Fan J, Sammalkorpi M, Haataja M (2010) Formation and regulation of lipid microdomains in cell membranes: theory, modeling, and speculation. FEBS Lett 584:1678–1684
37. Flesch FM, Gadella BM (2000) Dynamics of the mammalian sperm plasma membrane in the process of fertilization. Biochim Biophys Acta 1469:197–235
38. Flesch FM, Voorhout WF, Colenbrander B, van Golde LM, Gadella BM (1998) Use of lectins to characterize plasma membrane preparations from boar spermatozoa: a novel technique for monitoring membrane purity and quantity. Biol Reprod 59:1530–1539
39. Flesch FM, Brouwers JF, Nievelstein PF, Verkleij AJ, van Golde LM, Colenbrander B, Gadella BM (2001) Bicarbonate stimulated phospholipid scrambling induces cholesterol redistribution and enables cholesterol depletion in the sperm plasma membrane. J Cell Sci 114:3543–3555
40. Gadella BM, Evans JP (2011) Membrane fusions during mammalian fertilization. Adv Exp Med Biol 713:65–80
41. Gadella BM, Colenbrander B, van Golde LM, Lopes-Cardozo M (1992) Characterization of three arylsulfatases in semen: seminolipid sulfohydrolase activity is present in seminal plasma. Biochim Biophys Acta 1128:1551–1562
42. Gadella BM, Colenbrander B, Van Golde LM, Lopes-Cardozo M (1993) Boar seminal vesicles secrete arylsulfatases into seminal plasma: evidence that desulfation of seminolipid occurs only after ejaculation. Biol Reprod 48:483–489
43. Gadella BM, Gadella TW Jr, Colenbrander B, van Golde LM, Lopes-Cardozo M (1994) Visualization and quantification of glycolipid polarity dynamics in the plasma membrane of the mammalian spermatozoon. J Cell Sci 107:2151–2163
44. Gadella BM, Lopes-Cardozo M, van Golde LM, Colenbrander B, Gadella TW Jr (1995) 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 108:935–946
45. Gadella BM, Tsai PS, Boerke A, Brewis IA (2008) Sperm head membrane reorganisation during capacitation. Int J Dev Biol 52:473–480
46. Gallegos AM, Storey SM, Kier AB, Schroeder F, Ball JM (2006) Structure and cholesterol dynamics of caveolae/raft and nonraft plasma membrane domains. Biochemistry 45:12100–12116
47. Garofalo T, Manganelli V, Grasso M, Mattei V, Ferri A, Misasi R, Sorice M (2015) Role of mitochondrial raft-like microdomains in the regulation of cell apoptosis. Apoptosis 20:621–634
48. Gaus K, Gratton E, Kable EP, Jones AS, Gelissen I, Kritharides L, Jessup W (2003) Visualizing lipid structure and raft domains in living cells with two-photon microscopy. Proc Natl Acad Sci U S A 100:15554–15559
49. Gkantiragas I, Brugger B, Stuven E, Kaloyanova D, Li XY, Lohr K, Lottspeich F, Wieland FT, Helms JB (2001) Sphingomyelin-enriched microdomains at the golgi complex. Mol Biol Cell 12:1819–1833
50. Gruenberg J (2001) The endocytic pathway: a mosaic of domains. Nat Rev Mol Cell Biol 2:721–730
51. Hattersley KJ, Hein LK, Fuller M (2013) Lipid composition of membrane rafts, isolated with and without detergent, from the spleen of a mouse model of gaucher disease. Biochem Biophys Res Commun 442:62–67
52. Helms JB, Zurzolo C (2004) Lipids as targeting signals: lipid rafts and intracellular trafficking. Traffic 5:2472–54
53. Hooper NM (1999) Detergent-insoluble glycosphingolipid/cholesterol-rich membrane domains, lipid rafts and caveolae (review). Mol Membr Biol 16:145–156
54. Jones R, Howes E, Dunne PD, James P, Bruckbauer A, Klenerman D (2010) Tracking diffusion of GM1 gangliosides and zona pellucida binding molecules in sperm plasma membranes following cholesterol efflux. Dev Biol 339:398–406
55. Kean EL (1968) Rapid, sensitive spectrophotometric method for quantitative determination of sulfatides. J Lipid Res 9:319–327
56. Kusumi A, Koyama-Honda I, Suzuki K (2004) Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts. Traffic 5:213–230
57. Leahy T, Gadella BM (2015) New insights into the regulation of cholesterol efflux from the sperm membrane. Asian J Androl 17:561–567
58. Lingwood D (2014) Lipocalin 2 as a membrane-reorganizing agent. Sci Signal 7(338):pe19
59. Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327:46–50
60. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275
61. Lynch RD, Locicero J, Schneeberger EE (1986) Metabolism and incorporation into glycerolipids of exogenous 18:3(n-3) and 18:3(n-6) by MDCK cells. Lipids 21:447–453
62. Martens JR, Navarro-Polanco R, Coppock EA, Nishiyama A, Parshley L, Grobaski TD, Tamkun MM (2000) Differential targeting of shaker-like potassium channels to lipid rafts. J Biol Chem 275:7443–7446
63. Miranda PV, Allaire A, Sosnik J, Visconti PE (2009) Localization of low-density detergent-resistant membrane proteins in intact and acrosome-reacted mouse sperm. Biol Reprod 80:897–904
64. Mora R, Bonilha VL, Marmorstein A, Scherer PE, Brown D, Lisanti MP, Rodriguez-Boulan E (1999) Caveolin-2 localizes to the Golgi complex but redistributes to plasma membrane, caveolae, and rafts when co-expressed with caveolin-1. J Biol Chem 274:25708–25717
65. Moyano AL, Li G, Lopez-Rosas A, Månsson JE, van Breemen RB, Givogri MI (2014) Distribution of C16:0, C18:0, C24:1, and C24:0 sulfatides in central nervous system lipid rafts by quantitative ultra-high-pressure liquid chromatography tandem mass spectrometry. Anal Biochem 467:31–39
66. Nixon B, Aitken RJ (2009) The biological significance of detergent-resistant membranes in spermatozoa. J Reprod Immunol 83:8–13
67. Nixon B, Bielanowicz A, McLaughlin EA, Tanphaichitr N, Ensslin MA, Aitken RJ (2009) Composition and significance of detergent resistant membranes in mouse spermatozoa. J Cell Physiol 218:122–134
68. Nixon B, Mitchell LA, Anderson AL, McLaughlin EA, O’bryan MK, Aitken RJ (2011) Proteomic and functional analysis of human sperm detergent resistant membranes. J Cell Physiol 226(10):2651–65
69. Nyholm TK (2015) Lipid-protein interplay and lateral organization in biomembranes. Chem Phys Lipids 189:48–55
70. Pescio LG, Favale NO, Márquez MG, Sterin-Speziale NB (2012) Glycosphingolipid synthesis is essential for MDCK cell differentiation. Biochim Biophys Acta 1821:884–894
71. Pierce SK (2004) To cluster or not to cluster: FRETting over rafts. Nat Cell Biol 6:180–181
72. Pike LJ, Han X, Chung KN, Gross RW (2002) Lipid rafts are enriched in arachidonic acid and plasmenylethanolamine and their composition is independent of caveolin-1 expression: a quantitative electrospray ionization/mass spectrometric analysis. Biochemistry 41:2075–2088
73. Pike LJ, Han X, Gross RW (2005) Epidermal growth factor receptors are localized to lipid rafts that contain a balance of inner and outer leaflet lipids: a shotgun lipidomics study. J Biol Chem 280:26796–26804
74. Post H, Schwarz A, Brandenburger T, Aumüller G, Wilhelm B (2010) Arrangement of PMCA4 in bovine sperm membrane fractions. Int J Androl 33:775–783
75. Prior IA, Muncke C, Parton RG, Hancock JF (2003) Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J Cell Biol 160:165–170
76. Radeva G, Sharom FJ (2004) Isolation and characterization of lipid rafts with different properties from RBL-2H3 (rat basophilic leukaemia) cells. Biochem J 380:219–230
77. Radin NS (1984) Improved version of the Kean partition assay for cerebroside sulfate. J Lipid Res 25:651–652
78. Reid AT, Redgrove K, Aitken RJ, Nixon B (2011) Cellular mechanisms regulating sperm-zona pellucida interaction. Asian J Androl 13:88–96
79. Rietveld A, Simons K (1998) The differential miscibility of lipids as the basis for the formation of functional membrane rafts. Biochim Biophys Acta 1376:467–479
80. Róg T, Vattulainen I (2014) Cholesterol, sphingolipids, and glycolipids: what do we know about their role in raft-like membranes? Chem Phys Lipids 184:82–104
81. Sampson LJ, Dart C (2008) Lipid microdomains and k(+) channel compartmentation: detergent and non-detergent-based methods for the isolation and characterisation of cholesterol-enriched lipid rafts. Methods Mol Biol 491:91–101
82. Saslowsky DE, Lawrence J, Ren X, Brown DA, Henderson RM, Edwardson JM (2002) Placental alkaline phosphatase is efficiently targeted to rafts in supported lipid bilayers. J Biol Chem 277:26966–26970
83. Scheiffele P, Verkade P, Fra AM, Virta H, Simons K, Ikonen E (1998) Caveolin-1 and −2 in the exocytic pathway of MDCK cells. J Cell Biol 140:795–806
84. Scherfeld D, Kahya N, Schwille P (2003) Lipid dynamics and domain formation in model membranes composed of ternary mixtures of unsaturated and saturated phosphatidylcholines and cholesterol. Biophys J 85:3758–3768
85. Schuck S, Honsho M, Ekroos K, Shevchenko A, Simons K (2003) Resistance of cell membranes to different detergents. Proc Natl Acad Sci U S A 100:5795–5800
86. Selvaraj V, Asano A, Buttke DE, Sengupta P, Weiss RS, Travis AJ (2009) Mechanisms underlying the micron-scale segregation of sterols and GM1 in live mammalian sperm. J Cell Physiol 218:522–536
87. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569–572
88. Simons K, Ikonen E (2000) How cells handle cholesterol. Science 290:1721–1726
89. Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1:31–39
90. Simons K, Vaz WL (2004) Model systems, lipid rafts, and cell membranes. Annu Rev Biophys Biomol Struct 33:269–295
91. Stulnig TM, Huber J, Leitinger N, Imre EM, Angelisova P, Nowotny P, Waldhausl W (2001) Polyunsaturated eicosapentaenoic acid displaces proteins from membranerafts by altering raft lipid composition. J Biol Chem 276:37335–37340
92. Surma MA, Klose C, Simons K (2012) Lipid-dependent protein sorting at the trans-Golgi network. Biochim Biophys Acta 1821:1059–1067
93. Tanphaichitr N, Carmona E, Bou Khalil M, Xu H, Berger T, Gerton GL (2007) New insights into sperm-zona pellucida interaction: involvement of sperm lipid rafts. Front Biosci 12:1748–1766
94. Travis AJ, Merdiushev T, Vargas LA, Jones BH, Purdon MA, Nipper RW, Galatioto J, Moss SB, Hunnicutt GR, Kopf GS (2001) Expression and localization of caveolin-1, and the presence of membrane rafts, in mouse and guinea pig spermatozoa. Dev Biol 240:599–610
95. Tsai PS, De Vries KJ, De Boer-Brouwer M, Garcia-Gil N, Van Gestel RA, Colenbrander B, Gadella BM, Van Haeften T (2007) Syntaxin and VAMP association with lipid rafts depends on cholesterol depletion in capacitating sperm cells. Mol Membr Biol 24:313–324
96. Tsai PS, Garcia-Gil N, van Haeften T, Gadella BM (2010) How pig sperm prepares to fertilize: stable acrosome docking to the plasma membrane. PLoS ONE 5:e11204
97. Tsai PS, Brewis IA, van Maaren J, Gadella BM (2012) Involvement of complexin 2 in docking, locking and unlocking of different SNARE complexes during sperm capacitation and induced acrosomal exocytosis. PLoS ONE 7:e32603
98. van Gestel RA, Brewis IA, Ashton PR, Helms JB, Brouwers JF, Gadella BM (2005a) Capacitation-dependent concentration of lipid rafts in the apical ridge head area of porcine sperm cells. Mol Hum Reprod 11:583–590
99. van Gestel RA, Helms JB, Brouwers JF, Gadella BM (2005b) Effects of methyl-beta-cyclodextrin-mediated cholesterol depletion in porcine sperm compared to somatic cells. Mol Reprod Dev 72:386–395
100. van Gestel RA, Brewis IA, Ashton PR, Brouwers JF, Gadella BM (2007) Multiple proteins present in purified porcine sperm apical plasma membranes interact with the zona pellucida of the oocyte. Mol Hum Reprod 13(7):445–454
101. Vennema H, Godeke GJ, Rossen JW, Voorhout WF, Horzinek MC, Opstelten DJ, Rottier PJ (1996) Nucleocapsid-independent assembly of coronavirus-like particles by co-expression of viral envelope protein genes. EMBO J 15:2020–2028
102. Verkade P, Harder T, Lafont F, Simons K (2000) Induction of caveolae in the apical plasma membrane of madin-darby canine kidney cells. J Cell Biol 148:727–739
103. Vernooij EA, Brouwers JF, Kettenes-van de Bosch JJ, Crommelin DJ (2002) RP-HPLC/ESI MS determination of acyl positions in phospholipids. J Sep Sci 25:285–289
104. Vos JP, Lopes-Cardozo M, Gadella BM (1994) Metabolic and functional aspects of sulfogalactolipids. Biochim Biophys Acta 1211:125–149
105. Wang TY, Silvius JR (2001) Cholesterol does not induce segregation of liquid-ordered domains in bilayers modeling the inner leaflet of the plasma membrane. Biophys J 81:2762–2773
106. Watanabe H, Takeo T, Tojo H, Sakoh K, Berger T, Nakagata N, Mak TW, Kondoh G (2014) Lipocalin 2 binds to membrane phosphatidylethanolamine to induce lipid raft movement in a PKA-dependent manner and modulates sperm maturation. Development 141:2157–2164
107. Xu X, Bittman R, Duportail G, Heissler D, Vilcheze C, London E (2001) Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). Comparison of cholesterol to plant, fungal, and disease-associated sterols and comparison of sphingomyelin, cerebrosides, and ceramide. J Biol Chem 276:33540–33546
108. Zitranski N, Borth H, Ackermann F, Meyer D, Vieweg L, Breit A, Gudermann T, Boekhoff I (2010) The “acrosomal synapse”: subcellular organization by lipid rafts and scaffolding proteins exhibits high similarities in neurons and mammalian spermatozoa. Commun Integr Biol 3:513–521