Proteomic profiling of detergent resistant membranes (lipid rafts) of prostasomes

Molecular and Cellular Proteomics

Volumn 14, Issue 11, 2015, Pages 3015-3022

  Dubois, Louise ^a   Ronquist, Karl Göran ^a   Ek, Bo ^b   Ronquist, Gunnar ^a   Larsson, Anders ^a  

^a UPPSALA UNIVERSITY HOSPITAL   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

DETERGENT; ESCRT PROTEIN; PHOSPHATE BUFFERED SALINE; PROTEIN; SUCROSE; TETRASPANIN; TRITON X 100; LIPID; OCTOXINOL; PROTEOME; RAS PROTEIN;

ARTICLE; CONTROLLED STUDY; DENSITY; DENSITY GRADIENT CENTRIFUGATION; EXOSOME; LIPID RAFT; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROSTASOME; PROTEIN ANALYSIS; PROTEOMICS; TANDEM MASS SPECTROMETRY; CELL MEMBRANE; CHEMISTRY; HUMAN; ISOLATION AND PURIFICATION; LIQUID PHASE MICROEXTRACTION; MALE; METABOLISM; MOLECULAR GENETICS; PROCEDURES; PROSTATE;

CENTRIFUGATION, DENSITY GRADIENT; CHROMATOGRAPHY, LIQUID; DETERGENTS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; EXOSOMES; HUMANS; LIPIDS; LIQUID PHASE MICROEXTRACTION; MALE; MASS SPECTROMETRY; MEMBRANE MICRODOMAINS; MOLECULAR SEQUENCE ANNOTATION; OCTOXYNOL; PROSTATE; PROTEOME; RAS PROTEINS; TETRASPANINS;

EID: 84946100063     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M114.047530     Document Type: Article

References (63)

1. Aalberts, M., Stout, T. A., and Stoorvogel, W. (2014) Prostasomes: extracellular vesicles from the prostate. Reproduction 147, R1-14
2. Raposo, G., and Stoorvogel, W. (2013) Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell Biol. 200, 373-383
3. Trajkovic, K., Hsu, C., Chiantia, S., Rajendran, L., Wenzel, D., Wieland, F., Schwille, P., Brügger, B., and Simons, M. (2008) Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319, 1244-1247
4. Gulbins, E., and Kolesnick, R. (2003) Raft ceramide in molecular medicine. Oncogene 22, 7070-7077
5. Clarke, C. J., Snook, C. F., Tani, M., Matmati, N., Marchesini, N., and Hannun, Y. A. (2006) The extended family of neutral sphingomyelinases. Biochemistry 45, 11247-11256
6. Poliakov, A., Spilman, M., Dokland, T., Amling, C. L., and Mobley, J. A. (2009) Structural heterogeneity and protein composition of exosome-like vesicles (prostasomes) in human semen. Prostate 69, 159-167
7. Ronquist, G., and Brody, I. (1985) The prostasome: its secretion and function in man. Biochim. Biophys. Acta 822, 203-218
8. Sahlén, G. E., Egevad, L., Ahlander, A., Norlén, B. J., Ronquist, G., and Nilsson, B. O. (2002) Ultrastructure of the secretion of prostasomes from benign and malignant epithelial cells in the prostate. Prostate 53, 192-199
9. 2+-stimulated adenosine triphosphatase at the outer surface of Ehrlich ascites tumor cells. Cancer Res. 35, 1402-1406
10. Ronquist, G. (1987) Effect of modulators on prostasome membrane-bound ATPase in human seminal plasma. Eur. J. Clin. Investig. 17, 231-236
11. Ronquist, G. (2012) Prostasomes are mediators of intercellular communication: from basic research to clinical implications. J. Intern. Med. 271, 400-413
12. Kelly, R. W., Holland, P., Skibinski, G., Harrison, C., McMillan, L., Hargreave, T., and James, K. (1991) Extracellular organelles (prostasomes) are immunosuppressive components of human semen. Clin. Exp. Immunol. 86, 550-556
13. Rooney, I. A., Atkinson, J. P., Krul, E. S., Schonfeld, G., Polakoski, K., Saffitz, J. E., and Morgan, B. P. (1993) Physiologic relevance of the membrane attack complex inhibitory protein CD59 in human seminal plasma: CD59 is present on extracellular organelles (prostasomes), binds cell membranes, and inhibits complement-mediated lysis. J. Exp. Med. 177, 1409-1420
14. Ronquist, G., Nilsson, B. O., and Hjertën, S. (1990) Interaction between prostasomes and spermatozoa from human semen. Arch. Androl. 24, 147-157
15. Arienti, G., Carlini, E., and Palmerini, C. A. (1997) Fusion of human sperm to prostasomes at acidic pH. J. Membr. Biol. 155, 89-94
16. 2+ signaling tools acquired from prostasomes are required for progesterone-induced sperm motility. Sci. Signal. 4, ra31
17. Saez, F., Motta, C., Boucher, D., and Grizard, G. (1998) Antioxidant capacity of prostasomes in human semen. Mol. Human Reprod. 4, 667-672
18. Carlsson, L., Påhlson, C., Bergquist, M., Ronquist, G., and Stridsberg, M. (2000) Antibacterial activity of human prostasomes. Prostate 44, 279-286
19. Arvidson, G., Ronquist, G., Wikander, G., and Ojteg, A. C. (1989) Human prostasome membranes exhibit very high cholesterol/phospholipid ratios yielding high molecular ordering. Biochim. Biophys. Acta 984, 167-173
20. Arienti, G., Carlini, E., Polci, A., Cosmi, E. V., and Palmerini, C. A. (1998) Fatty acid pattern of human prostasome lipid. Arch. Biochem. Biophys. 358, 391-395
21. Singer, S. J., and Nicolson, G. L. (1972) The fluid mosaic model of the structure of cell membranes. Science 175, 720-731
22. Davson, H., and Danielli, J. F. (1938) Studies on the permeability of erythrocytes: Factors in cation permeability. Biochem. J. 32, 991-1001
23. Palade, G. E. (1953) An electron microscope study of the mitochondrial structure. J. Histochem. Cytochem. 1, 188-211
24. Yamada, E. (1955) The fine structure of the renal glomerulus of the mouse. J. Histochem. Cytochem. 3, 309
25. Van Meer, G., and Simons, K. (1988) Lipid polarity and sorting in epithelial cells. J. Cell. Biochem. 36, 51-58
26. Simons, K., and Ikonen, E. (1997) Functional rafts in cell membranes. Nature 387, 569-572
27. Pike, L. J. (2003) Lipid rafts: bringing order to chaos. J. Lipid Res. 44, 655-667
28. Brown, D. A., and Rose, J. K. (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533-544
29. Brown, D. A., and London, E. (2000) Structure and function of sphingolipidand cholesterol-rich membrane rafts. J. Biol. Chem. 275, 17221-17224
30. Head, B. P., Patel, H. H., Roth, D. M., Murray, F., Swaney, J. S., Niesman, I. R., Farquhar, M. G., and Insel, P. A. (2006) Microtubules and actin microfilaments regulate lipid raft/caveolae localization of adenylyl cyclase signaling components. J. Biol. Chem. 281, 26391-26399
31. Stuermer, C. A. (2010) The reggie/flotillin connection to growth. Trends Cell Biol. 20, 6-13
32. Hancock, J. F. (2006) Lipid rafts: contentious only from simplistic standpoints. Nat. Rev. Mol. Cell Biol. 7, 456-462
33. Lingwood, D., and Simons, K. (2010) Lipid rafts as a membrane-organizing principle. Science 327, 46-50
34. Damm, E. M., Pelkmans, L., Kartenbeck, J., Mezzacasa, A., Kurzchalia, T., and Helenius, A. (2005) Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J. Cell Biol. 168, 477-488
35. Riento, K., Frick, M., Schafer, I., and Nichols, B. J. (2009) Endocytosis of flotillin-1 and flotillin-2 is regulated by Fyn kinase. J. Cell Sci. 122, 912-918
36. Ronquist, G. K., Larsson, A., Ronquist, G., Isaksson, A., Hreinsson, J., Carlsson, L., and Stavreus-Evers, A. (2011) Prostasomal DNA characterization and transfer into human sperm. Mol. Reprod. Dev. 78, 467-476
37. Stegmayr, B., and Ronquist, G. (1982) Promotive effect on human sperm progressive motility by prostasomes. Urol. Res. 10, 253-257
38. Escola, J. M., Kleijmeer, M. J., Stoorvogel, W., Griffith, J. M., Yoshie, O., and Geuze, H. J. (1998) Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J. Biol. Chem. 273, 20121-20127
39. McGuinn, K. P., and Mahoney, M. G. (2014) Lipid Rafts and Detergent-Resistant Membranes in Epithelial Keratinocytes. Methods. Mol. Biol. 1195, 133-144
40. Wisniewski, J. R., Zougman, A., Nagaraj, N., and Mann, M. (2009) Universal sample preparation method for proteome analysis. Nat. Meth. 6, 359-362
41. Rappsilber, J., Mann, M., and Ishihama, Y. (2007) Protocol for micropurification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protocols 2, 1896-1906
42. Ronquist, K. G., Ek, B., Morrell, J., Stavreus-Evers, A., Ström Holst, B., Humblot, P., Ronquist, G., and Larsson, A. (2013) Prostasomes from four different species are able to produce extracellular adenosine triphosphate (ATP). Biochim. Biophys. Acta 1830, 4604-4610
43. Schrimpf, S. P., Hellman, U., Carlsson, L., Larsson, A., Ronquist, G., and Nilsson, B. O. (1999) Identification of dipeptidyl peptidase IV as the antigen of a monoclonal anti-prostasome antibody. Prostate 38, 35-39
44. Kameoka, J., Tanaka, T., Nojima, Y., Schlossman, S. F., and Morimoto, C. (1993) Direct association of adenosine deaminase with a T cell activation antigen, CD26. Science 261, 466-469
45. Ciruela, F., Saura, C., Canela, E. I., Mallol, J., Lluis, C., and Franco, R. (1996) Adenosine deaminase affects ligand-induced signalling by interacting with cell surface adenosine receptors. FEBS Lett. 380, 219-223
46. Fabiani, R., and Ronquist, G. (1995) Abundance of guanine, guanosine, inosine and adenosine in human seminal plasma. Int. J. Clin. Lab. Res. 25, 47-51
47. Franco, R., Valenzuela, A., Lluis, C., and Blanco, J. (1998) Enzymatic and extraenzymatic role of ecto-adenosine deaminase in lymphocytes. Immunol. Rev. 161, 27-42
48. Minelli, A., Allegrucci, C., Mezzasoma, I., Ronquist, G., Lluis, C., and Franco, R. (1999) CD26 and adenosine deaminase interaction: its role in the fusion between horse membrane vesicles and spermatozoa. Biol. Reprod. 61, 802-808
49. Babiker, A. A., Ronquist, G., Nilsson, U. R., and Nilsson, B. (2002) Transfer of prostasomal CD59 to CD59-deficient red blood cells results in protection against complement-mediated hemolysis. Am. J. Reprod. Immunol. 47, 183-192
50. Andreu, Z., and Yanez-Mo, M. (2014) Tetraspanins in extracellular vesicle formation and function. Frontiers Immunol. 5, 442
51. Charrin, S., Le Naour, F., Silvie, O., Milhiet, P. E., Boucheix, C., and Rubinstein, E. (2009) Lateral organization of membrane proteins: tetraspanins spin their web. Biochem. J. 420, 133-154
52. Perez-Hernandez, D., Gutiérrez-Vázquez, C., Jorge, I., López-Martin, S., Ursa, A., Sánchez-Madrid, F., Vázquez, J., and Yáñez-Mó, M. (2013) The intracellular interactome of tetraspanin-enriched microdomains reveals their function as sorting machineries toward exosomes. J. Biol. Chem. 288, 11649-11661
53. Buschow, S. I., Nolte-'t Hoen, E. N., Van Niel, G., Pols, M. S., Ten Broeke, T., Lauwen, M., Ossendorp, F., Melief, C. J., Raposo, G., Wubbolts, R., Wauben, M. H., and Stoorvogel, W. (2009) MHC II in dendritic cells is targeted to lysosomes or T cell-induced exosomes via distinct multivesicular body pathways. Traffic 10, 1528-1542
54. Van Niel, G., Charrin, S., Simoes, S., Romao, M., Rochin, L., Saftig, P., Marks, M. S., Rubinstein, E., and Raposo, G. (2011) The tetraspanin CD63 regulates ESCRT-independent and -dependent endosomal sorting during melanogenesis. Develop. Cell 21, 708-721
55. Henne, W. M., Buchkovich, N. J., and Emr, S. D. (2011) The ESCRT pathway. Develop. Cell 21, 77-91
56. Babst, M. (2011) MVB vesicle formation: ESCRT-dependent, ESCRT-independent and everything in between. Curr. Opinion Cell Biol. 23, 452-457
57. Baietti, M. F., Zhang, Z., Mortier, E., Melchior, A., Degeest, G., Geeraerts, A., Ivarsson, Y., Depoortere, F., Coomans, C., Vermeiren, E., Zimmermann, P., and David, G. (2012) Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat. Cell Biol. 14, 677-685
58. Greaves, J., Gorleku, O. A., Salaun, C., and Chamberlain, L. H. (2010) Palmitoylation of the SNAP25 protein family: specificity and regulation by DHHC palmitoyl transferases. J. Biol. Chem. 285, 24629-24638
59. Sharma, C., Yang, X. H., and Hemler, M. E. (2008) DHHC2 affects palmitoylation, stability, and functions of tetraspanins CD9 and CD151. Mol. Biol. Cell 19, 3415-3425
60. Stenmark, H. (2009) Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10, 513-525
61. Ostrowski, M., Carmo, N. B., Krumeich, S., Fanget, I., Raposo, G., Savina, A., Moita, C. F., Schauer, K., Hume, A. N., Freitas, R. P., Goud, B., Benaroch, P., Hacohen, N., Fukuda, M., Desnos, C., Seabra, M. C., Darchen, F., Amigorena, S., Moita, L. F., and Thery, C. (2010) Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol. 12, 19-30
62. Ronquist, K. G., Carlsson, L., Ronquist, G., Semjonow, A., Wülfing, C., and Larsson, A. (2008) Serum antibodies against prostasomal clusterin in prostate cancer patients. Scand. J. Clin. Lab. Invest. 68, 219-227
63. Vizcaíno, J. A., Deutsch, E. W., Wang, R., Csordas, A., Reisinger, F., Rios, D., Dianes, J. A., Sun, Z., Farrah, T., Bandeira, N., Binz, P. A., Xenarios, I., Eisenacher, M., Mayer, G., Gatto, L., Campos, A., Chalkley, R. J., Kraus, H. J., Albar, J. P., Martinez-Bartolome, S., Apweiler, R., Omenn, G. S., Martens, L., Jones, A. R., and Hermjakob, H. (2014) ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat. Biotechnol. 32, 223-226