Identification of distinct populations of prostasomes that differentially express prostate stem cell antigen, annexin A1, and GLIPR2 in humans

Biology of Reproduction

Volumn 86, Issue 3, 2012, Pages

  Aalberts, Marian ^a,b   van Dissel Emiliani, Federica M F ^a,b   van Adrichem, Nick P H ^c   van Wijnen, Merel ^c   Wauben, Marca H M ^a   Stout, Tom A E ^b   Stoorvogel, Willem ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c MEANDER MEDICAL CENTER   (Netherlands)

Author keywords

Annexin A1; Exosomes; Extracellular membrane vesicles; GLIPR2; Prostasomes; PSCA

Indexed keywords

CD9 ANTIGEN; GAMMA GLUTAMYLTRANSFERASE; GLI PATHOGENESIS RELATED PROTEIN 2; IDITOL DEHYDROGENASE; LIPOCORTIN 1; PROLACTIN; PROSTATE STEM CELL ANTIGEN; PROTEIN; SUCROSE; UNCLASSIFIED DRUG; XYLULOSE REDUCTASE; GLIPR2 PROTEIN, HUMAN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; MEMBRANE PROTEIN; PSCA PROTEIN, HUMAN; TUMOR ANTIGEN; TUMOR PROTEIN;

ANTIGEN EXPRESSION; ARTICLE; CELL DENSITY; CELL HETEROGENEITY; CELL POPULATION; CELL SIZE; EPIDIDYMIS; EXOSOME; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MEMBRANE VESICLE; NORMAL HUMAN; PRIORITY JOURNAL; PROSTASOME; SEMINAL PLASMA; TESTIS; VASECTOMY; COMPARATIVE STUDY; CYTOLOGY; CYTOPLASM VESICLE; EPITHELIUM; IMMUNOELECTRON MICROSCOPY; METABOLISM; PROSTATE; SPERM; ULTRASTRUCTURE;

ANNEXIN A1; ANTIGENS, NEOPLASM; CYTOPLASMIC VESICLES; EPITHELIUM; GPI-LINKED PROTEINS; HUMANS; MALE; MEMBRANE PROTEINS; MICROSCOPY, IMMUNOELECTRON; NEOPLASM PROTEINS; PROSTATE; SEMEN; VASECTOMY;

EID: 84860647491     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.095760     Document Type: Article

References (61)

1. Sahlen GE, Egevad L, Ahlander A, Norlen BJ, Ronquist G, Nilsson BO. Ultrastructure of the secretion of prostasomes from benign and malignant epithelial cells in the prostate. Prostate 2002; 53:192-199.
2. Llorente A, de Marco MC, Alonso MA. Caveolin-1 and MAL are located on prostasomes secreted by the prostate cancer PC-3 cell line. J Cell Sci 2004; 117:5343-5351.
3. Sullivan R, Saez F, Girouard J, Frenette G. Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood Cells Mol Dis 2005; 35:1-10.
4. Renneberg H, Konrad L, Dammshauser I, Seitz J, Aumuller G. Immunohistochemistry of prostasomes from human semen. Prostate 1997; 30:98-106.
5. Ronquist G, Nilsson BO. The Janus-faced nature of prostasomes: their pluripotency favours the normal reproductive process and malignant prostate growth. Prostate Cancer Prostatic Dis 2004; 7:21-31.
6. Ronquist KG, Ronquist G, Carlsson L, Larsson A. Human prostasomes contain chromosomal DNA. Prostate 2009; 69:159-167.
7. Utleg AG, Yi EC, Xie T, Shannon P, White JT, Goodlett DR, Hood L, Lin B. Proteomic analysis of human prostasomes. Prostate 2003; 56:150-161.
8. Jones JL, Saraswati S, Block AS, Lichti CF, Mahadevan M, Diekman AB. Galectin-3 is associated with prostasomes in human semen. Glycoconj J 2010; 27:227-236.
9. Simons M, Raposo G. Exosomes-vesicular carriers for intercellular communication. Curr Opin Cell Biol 2009; 21:575-581.
10. Stoorvogel W, Kleijmeer MJ, Geuze HJ, Raposo G. The biogenesis and functions of exosomes. Traffic 2002; 3:321-330.
11. Pisitkun T, Shen RF, Knepper MA. Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci U S A 2004; 101:13368-13373.
12. Palanisamy V, Sharma S, Deshpande A, Zhou H, Gimzewski J, Wong DT. Nanostructural and transcriptomic analyses of human saliva derived exosomes. Plos One 5:e8577.
13. Caby MP, Lankar D, Vincendeau-Scherrer C, Raposo G, Bonnerot C. Exosomal-like vesicles are present in human blood plasma. Int Immunol 2005; 17:879-887.
14. Vella LJ, Greenwood DL, Cappai R, Scheerlinck JP, Hill AF. Enrichment of prion protein in exosomes derived from ovine cerebral spinal fluid. Vet Immunol Immunopathol 2008; 124:385-393.
15. Andre F, Schartz NE, Movassagh M, Flament C, Pautier P, Morice P, Pomel C, Lhomme C, Escudier B, Le Chevalier T, Tursz T, Amigorena S, et al. Malignant effusions and immunogenic tumour-derived exosomes. Lancet 2002; 360:295-305.
16. Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009; 9:581-593.
17. Frenette G, Girouard J, D'Amours O, Allard N, Tessier L, Sullivan R. Characterization of two distinct populations of epididymosomes collected in the intraluminal compartment of the bovine cauda epididymis. Biol Reprod 2010; 83:473-480.
18. Frenette G, Lessard C, Madore E, Fortier MA, Sullivan R. Aldose reductase and macrophage migration inhibitory factor are associated with epididymosomes and spermatozoa in the bovine epididymis. Biol Reprod 2003; 69:1586-1592.
19. Burden HP, Holmes CH, Persad R, Whittington K. Prostasomes-their effects on human male reproduction and fertility. Hum Reprod Update 2006; 12:283-292.
20. Arienti G, Carlini E, Nicolucci A, Cosmi EV, Santi F, Palmerini CA. The motility of human spermatozoa as influenced by prostasomes at various pH levels. Biol Cell 1999; 91:51-54.
21. Park KH, Kim BJ, Kang J, Nam TS, Lim JM, Kim HT, Park JK, Kim YG, Chae SW, Kim UH. Ca2+ signaling tools acquired from prostasomes are required for progesterone-induced sperm motility. Sci Signal 2011; 4: ra31.
22. Cross NL, Mahasreshti P. Prostasome fraction of human seminal plasma prevents sperm from becoming acrosomally responsive to the agonist progesterone. Arch Androl 1997; 39:39-44.
23. Palmerini CA, Saccardi C, Carlini E, Fabiani R, Arienti G. Fusion of prostasomes to human spermatozoa stimulates the acrosome reaction. Fertil Steril 2003; 80:1181-1184.
24. Babiker AA, Ronquist G, Nilsson UR, Nilsson B. Transfer of prostasomal CD59 to CD59-deficient red blood cells results in protection against complement-mediated hemolysis. Am J Reprod Immunol 2002; 47:183-192.
25. Kitamura M, Namiki M, Matsumiya K, Tanaka K, Matsumoto M, Hara T, Kiyohara H, Okabe M, Okuyama A, Seya T. Membrane cofactor protein (CD46) in seminal plasma is a prostasome-bound form with complement regulatory activity and measles virus neutralizing activity. Immunology 1995; 84:626-632.
26. Kelly RW. Immunosuppressive mechanisms in semen: implications for contraception. Hum Reprod (Oxford) 1995; 10:1686-1693.
27. Skibinski G, Kelly RW, Harkiss D, James K. Immunosuppression by human seminal plasma-extracellular organelles (prostasomes) modulate activity of phagocytic cells. Am J Reprod Immunol 1992; 28:97-103.
28. Tarazona R, Delgado E, Guarnizo MC, Roncero RG, Morgado S, Sanchez-Correa B, Gordillo JJ, Dejulian J, Casado JG. Human prostasomes express CD48 and interfere with NK cell function. Immunobiology 2011; 216:41-46.
29. Eberle HB, Serrano RL, Fullekrug J, Schlosser A, Lehmann WD, Lottspeich F, Kaloyanova D, Wieland FT, Helms JB. Identification and characterization of a novel human plant pathogenesis-related protein that localizes to lipid-enriched microdomains in the Golgi complex. J Cell Sci 2002; 115:827-838.
30. Dong HY, Weisberger J, Liu Z, Tugulea S. Immunophenotypic analysis of CD103+ B-lymphoproliferative disorders: hairy cell leukemia and its mimics. Am J Clin Pathol 2009; 131:586-595.
31. Wilm M, Shevchenko A, Houthaeve T, Breit S, Schweigerer L, Fotsis T, Mann M. Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 1996; 379:466-469.
32. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, Geuze HJ. B lymphocytes secrete antigen-presenting vesicles. J Exp Med 1996; 183:1161-1172.
33. Poliakov A, Spilman M, Dokland T, Amling CL, Mobley JA. Structural heterogeneity and protein composition of exosome-like vesicles (prostasomes) in human semen. The Prostate 2009; 69:159-167.
34. Fevrier B, Raposo G. Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr Opin Cell Biol 2004; 16:415-421.
35. Mathivanan S, Simpson RJ. ExoCarta: a compendium of exosomal proteins and RNA. Proteomics 2009; 9:4997-5000.
36. Kovalenko OV, Metcalf DG, DeGrado WF, Hemler ME. Structural organization and interactions of transmembrane domains in tetraspanin proteins. BMC Struct Biol 2005; 5:11.
37. Arnott D, Kishiyama A, Luis EA, Ludlum SG, Marsters JC Jr, Stults JT. Selective detection of membrane proteins without antibodies: a mass spectrometric version of the Western blot. Mol Cell Proteomics 2002; 1:148-156.
38. Nolte-'t Hoen EN, Buschow SI, Anderton SM, Stoorvogel W, Wauben MH. Activated T cells recruit exosomes secreted by dendritic cells via LFA-1. Blood 2009; 113:1977-1981.
39. Christmas P, Callaway J, Fallon J, Jones J, Haigler HT. Selective secretion of annexin 1, a protein without a signal sequence, by the human prostate gland. J Biol Chem 1991; 266:2499-2507.
40. Carlsson L, Nilsson O, Larsson A, Stridsberg M, Sahlen G, Ronquist G. Characteristics of human prostasomes isolated from three different sources. The Prostate 2003; 54:322-330.
41. Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 1999; 94:3791-3799.
42. Cunha AC, Weigle B, Kiessling A, Bachmann M, Rieber EP. Tissuespecificity of prostate specific antigens: comparative analysis of transcript levels in prostate and non-prostatic tissues. Cancer Lett 2006; 236:229-238.
43. Reiter RE, Gu Z, Watabe T, Thomas G, Szigeti K, Davis E, Wahl M, Nisitani S, Yamashiro J, Le Beau MM, Loda M, Witte ON. Prostate stem cell antigen: a cell surface marker overexpressed in prostate cancer. Proc Natl Acad Sci U S A 1998; 95:1735-1740.
44. Study Group of Millennium Genome Project for Cancer, Sakamoto H, Yoshimura K, Saeki N, Katai H, Shimoda T, Matsuno Y, Saito D, Sugimura H, Tanioka F, Kato S, Matsukura N, et al. Genetic variation in PSCA is associated with susceptibility to diffuse-type gastric cancer. Nat Genet 2008; 40:730-740.
45. Ross S, Spencer SD, Holcomb I, Tan C, Hongo J, Devaux B, Rangell L, Keller GA, Schow P, Steeves RM, Lutz RJ, Frantz G, et al. Prostate stem cell antigen as therapy target: tissue expression and in vivo efficacy of an immunoconjugate. Cancer Res 2002; 62:2546-2553.
46. Gu Z, Thomas G, Yamashiro J, Shintaku IP, Dorey F, Raitano A, Witte ON, Said JW, Loda M, Reiter RE. Prostate stem cell antigen (PSCA) expression increases with high gleason score, advanced stage and bone metastasis in prostate cancer. Oncogene 2000; 19:1288-1296.
47. Brody I, Ronquist G, Gottfries A. Ultrastructural localization of the prostasome-an organelle in human seminal plasma. Ups J Med Sci 1983; 88:63-80.
48. Zhigang Z, Wenlu S. Complete androgen ablation suppresses prostate stem cell antigen (PSCA) mRNA expression in human prostate carcinoma. Prostate 2005; 65:299-305.
49. Moore ML, Teitell MA, Kim Y, Watabe T, Reiter RE, Witte ON, Dubey P. Deletion of PSCA increases metastasis of TRAMP-induced prostate tumors without altering primary tumor formation. Prostate 2008; 68:139-151.
50. Bahrenberg G, Brauers A, Joost HG, Jakse G. Reduced expression of PSCA, a member of the LY-6 family of cell surface antigens, in bladder, esophagus, and stomach tumors. Biochem Biophys Res Commun 2000; 275:783-788.
51. Raff AB, Gray A, Kast WM. Prostate stem cell antigen: a prospective therapeutic and diagnostic target. Cancer Lett 2009; 277:126-132.
52. Eisenberg I, Barash M, Kahan T, Mitrani-Rosenbaum S. Cloning and characterization of a human novel gene C9orf19 encoding a conserved putative protein with an SCP-like extracellular protein domain. Gene 2002; 293:141-148.
53. Serrano RL, Kuhn A, Hendricks A, Helms JB, Sinning I, Groves MR. Structural analysis of the human Golgi-associated plant pathogenesis related protein GAPR-1 implicates dimerization as a regulatory mechanism. J Mol Biol 2004; 339:173-183.
54. Gkantiragas I, Brugger B, Stuven E, Kaloyanova D, Li XY, Lohr K, Lottspeich F, Wieland FT, Helms JB. Sphingomyelin-enriched microdomains at the Golgi complex. Mol Biol Cell 2001; 12:1819-1833.
55. Van Galen J, Van Balkom BW, Serrano RL, Kaloyanova D, Eerland R, Stuven E, Helms JB. Binding of GAPR-1 to negatively charged phospholipid membranes: unusual binding characteristics to phosphatidylinositol. Mol Membr Biol 2010; 27:81-91.
56. Gibbs GM, Roelants K, O'Bryan MK. The CAP superfamily: cysteinerich secretory proteins, antigen 5, and pathogenesis-related 1 proteins-roles in reproduction, cancer, and immune defense. Endocr Rev 2008; 29:865-897.
57. Doty A, Buhi WC, Benson S, Scoggin KE, Pozor M, Macpherson M, Mutz M, Troedsson MH. Equine CRISP3 modulates interaction between spermatozoa and polymorphonuclear neutrophils (PMNs). Biol Reprod 2011; 85:157-164.
58. Ablin RJ, Bartkus JM, Polgar J. Effect of human seminal plasma on the lytic activity of natural killer cells and presumptive identification of participant macromolecules. Am J Reprod Immunol 1990; 24:15-21.
59. Lim LH, Pervaiz S. Annexin 1: the new face of an old molecule. FASEB J 2007; 21:968-975.
60. Paweletz CP, Ornstein DK, Roth MJ, Bichsel VE, Gillespie JW, Calvert VS, Vocke CD, Hewitt SM, Duray PH, Herring J, Wang QH, Hu N, et al. Loss of annexin 1 correlates with early onset of tumorigenesis in esophageal and prostate carcinoma. Cancer Res 2000; 60:6293-6297.
61. Xin W, Rhodes DR, Ingold C, Chinnaiyan AM, Rubin MA. Dysregulation of the annexin family protein family is associated with prostate cancer progression. Am J Pathol 2003; 162:255-261.