Malignant cell-derived extracellular vesicles express different chromogranin epitopes compared to prostasomes

Prostate

Volumn 75, Issue 10, 2015, Pages 1063-1073

  Dubois, Louise ^a   Stridsberg, Mats ^a   Kharaziha, Pedram ^b   Chioureas, Dimitris ^b   Meersman, Niels ^c   Panaretakis, Theocharis ^b   Ronquist, K Göran ^a  

^a UPPSALA UNIVERSITY HOSPITAL   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c KAHO   (Belgium)

Author keywords

chromogranins; DU145; extracellular vesicles; LNCaP; PC3; prostasomes; prostate cancer; synaptophysin

Indexed keywords

CHROMOGRANIN A; CHROMOGRANIN B; PROPROTEIN CONVERTASE 1; PROPROTEIN CONVERTASE 2; PROTEIN; PROTEIN ALIX; RAB PROTEIN; SECRETOGRANIN V; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; CHROMOGRANIN;

ANTIBODY AFFINITY; ARTICLE; CANCER CELL; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXOSOME; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MALE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROSTASOME; PROSTATE; PROSTATE CANCER CELL LINE; PROTEIN EXPRESSION; SEMINAL PLASMA; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; CHEMISTRY; EPITHELIUM CELL; EXOCYTOSIS; EXTRACELLULAR SPACE; PROSTATE TUMOR; SPERM; TUMOR CELL LINE; ULTRASTRUCTURE;

BLOTTING, WESTERN; CELL LINE, TUMOR; CHROMOGRANINS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITHELIAL CELLS; EXOCYTOSIS; EXOSOMES; EXTRACELLULAR SPACE; HUMANS; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; PROSTATIC NEOPLASMS; SEMEN;

EID: 84929989707     PISSN: 02704137     EISSN: 10970045     Source Type: Journal    
DOI: 10.1002/pros.22990     Document Type: Article

References (68)

1. Ronquist G,. Prostasomes are mediators of intercellular communication: From basic research to clinical implications. J Intern Med 2012; 271: 400-413.
2. Saez F, Frenette G, Sullivan R,. Epididymosomes and prostasomes: Their roles in posttesticular maturation of the sperm cells. J Androl 2003; 24: 149-154.
3. Ronquist GK, Larsson A, Stavreus-Evers A, Ronquist G,. Prostasomes are heterogeneous regarding size and appearance but affiliated to one DNA-containing exosome family. Prostate 2012; 72: 1736-1745.
4. Ronquist G, Brody I, Gottfries A, Stegmayr B,. An Mg2+ and Ca2+-stimulated adenosine triphosphatase in human prostatic fluid-part II. Andrologia 1978; 10: 427-433.
5. Ronquist G, Brody I, Gottfries A, Stegmayr B,. An Mg2+ and Ca2+-stimulated adenosine triphosphatase in human prostatic fluid: Part I. Andrologia 1978; 10: 261-272.
6. Poliakov A, Spilman M, Dokland T, Amling CL, Mobley JA,. Structural heterogeneity and protein composition of exosome-like vesicles (prostasomes) in human semen. Prostate 2009; 69: 159-167.
7. Brouwers JF, Aalberts M, Jansen JW, van NG, Wauben MH, Stout TA, Helms JB, Stoorvogel W,. Distinct lipid compositions of two types of human prostasomes. Proteomics 2013; 13: 1660-1666.
8. Aalberts M, van Dissel-Emiliani FM, van Adrichem NP, van WM, Wauben MH, Stout TA, Stoorvogel W,. Identification of distinct populations of prostasomes that differentially express prostate stem cell antigen, annexin A1, and GLIPR2 in humans. Biol Reprod 2012; 86: 82.
9. 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.
10. Stegmayr B, Ronquist G,. Promotive effect on human sperm progressive motility by prostasomes. Urol Res 1982; 10: 253-257.
11. Fabiani R, Johansson L, Lundkvist O, Ronquist G,. Enhanced recruitment of motile spermatozoa by prostasome inclusion in swim-up medium. Hum Reprod 1994; 9: 1485-1489.
12. Kelly RW, Holland P, Skibinski G, Harrison C, McMillan L, Hargreave T, James K,. Extracellular organelles (prostasomes) are immunosuppressive components of human semen. Clin Exp Immunol 1991; 86: 550-556.
13. Rooney IA, Atkinson JP, Krul ES, Schonfeld G, Polakoski K, Saffitz JE, Morgan BP,. 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 1993; 177: 1409-1420.
14. Llorente A, van DB, Sandvig K,. Cholesterol regulates prostasome release from secretory lysosomes in PC-3 human prostate cancer cells. Eur J Cell Biol 2007; 86: 405-415.
15. Sahlen G, Ahlander A, Frost A, Ronquist G, Norlen BJ, Nilsson BO,. Prostasomes are secreted from poorly differentiated cells of prostate cancer metastases. Prostate 2004; 61: 291-297.
16. Carlsson L, Nilsson O, Larsson A, Stridsberg M, Sahlen G, Ronquist G,. Characteristics of human prostasomes isolated from three different sources. Prostate 2003; 54: 322-330.
17. 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.
18. Ekdahl KN, Ronquist G, Nilsson B, Babiker AA,. Possible immunoprotective and angiogenesis-promoting roles for malignant cell-derived prostasomes: A new paradigm for prostatic cancer?. Adv Exp Med Biol 2006; 586: 107-119.
19. Frenette G, Sullivan R,. Prostasome-like particles are involved in the transfer of P25b from the bovine epididymal fluid to the sperm surface. Mol Reprod Dev 2001; 59: 115-121.
20. Sullivan R, Frenette G, Girouard J,. Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit. Asian J Androl 2007; 9: 483-491.
21. 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.
22. Carlsson L, Ronquist G, Eliasson R, Egberg N, Larsson A,. Flow cytometric technique for determination of prostasomal quantity, size and expression of CD10, CD13, CD26 and CD59 in human seminal plasma. Int J Androl 2006; 29: 331-338.
23. Schrimpf SP, Hellman U, Carlsson L, Larsson A, Ronquist G, Nilsson BO,. Identification of dipeptidyl peptidase IV as the antigen of a monoclonal anti-prostasome antibody. Prostate 1999; 38: 35-39.
24. Wilson MJ, Ruhland AR, Pryor JL, Ercole C, Sinha AA, Hensleigh H, Kaye KW, Dawkins HJ, Wasserman NF, Reddy P, Ahmed K,. Prostate specific origin of dipeptidylpeptidase IV (CD-26) in human seminal plasma. J Urol 1998; 160: 1905-1909.
25. Sahlen G, Nilsson O, Larsson A, Carlsson L, Norlen BJ, Ronquist G,. Secretions from seminal vesicles lack characteristic markers for prostasomes. Ups J Med Sci 2010; 115: 107-112.
26. Nilsson BO, Jin M, Einarsson B, Persson BE, Ronquist G,. Monoclonal antibodies against human prostasomes. Prostate 1998; 35: 178-184.
27. Banks P, Helle K,. The release of protein from the stimulated adrenal medulla. Biochem J 1965; 97: 40C-41C.
28. Lee RW, Huttner WB,. Tyrosine-O-sulfated proteins of PC12 pheochromocytoma cells and their sulfation by a tyrosylprotein sulfotransferase. J Biol Chem 1983; 258: 11326-11334.
29. Zanini A, Rosa P,. Characterization of adenohypophysial polypeptides by two-dimensional gel electrophoresis. I. L-[3H]leucine-labeled polypeptides. Mol Cell Endocrinol 1981; 24: 165-179.
30. Ottiger HP, Battenberg EF, Tsou AP, Bloom FE, Sutcliffe JG,. B1075: A brain- and pituitary-specific mRNA that encodes a novel chromogranin/secretogranin-like component of intracellular vesicles. J Neurosci 1990; 10: 3135-3147.
31. Krisch K, Buxbaum P, Horvat G, Krisch I, Neuhold N, Ulrich W, Srikanta S,. Monoclonal antibody HISL-19 as an immunocytochemical probe for neuroendocrine differentiation. Its application in diagnostic pathology. Am J Pathol 1986; 123: 100-108.
32. Mbikay M, Seidah NG, Chretien M,. Neuroendocrine secretory protein 7 B2: Structure, expression and functions. Biochem J 2001; 357: 329-342.
33. Ischia R, Lovisetti-Scamihorn P, Hogue-Angeletti R, Wolkersdorfer M, Winkler H, Fischer-Colbrie R,. Molecular cloning and characterization of NESP55, a novel chromogranin-like precursor of a peptide with 5-HT1B receptor antagonist activity. J Biol Chem 1997; 272: 11657-11662.
34. Grimes M, Iacangelo A, Eiden LE, Godfrey B, Herbert E,. Chromogranin A: The primary structure deduced from cDNA clones reveals the presence of pairs of basic amino acids. Ann N Y Acad Sci 1987; 493: 351-378.
35. Reiffen FU, Gratzl M,. Chromogranins, widespread in endocrine and nervous tissue, bind Ca2+. FEBS Lett 1986; 195: 327-330.
36. Gorr SU, Shioi J, Cohn DV,. Interaction of calcium with porcine adrenal chromogranin A (secretory protein-I) and chromogranin B (secretogranin I). Am J Physiol 1989; 257: E247-E254.
37. Gerdes HH, Rosa P, Phillips E, Baeuerle PA, Frank R, Argos P, Huttner WB,. The primary structure of human secretogranin II, a widespread tyrosine-sulfated secretory granule protein that exhibits low pH- and calcium-induced aggregation. J Biol Chem 1989; 264: 12009-12015.
38. Yoo SH, Kang YK,. Identification of the secretory vesicle membrane binding region of chromogranin B. FEBS Lett 1997; 406: 259-262.
39. Kang YK, Yoo SH,. Identification of the secretory vesicle membrane binding region of chromogranin A. FEBS Lett 1997; 404: 87-90.
40. Hosaka M, Watanabe T, Sakai Y, Kato T, Takeuchi T,. Interaction between secretogranin III and carboxypeptidase E facilitates prohormone sorting within secretory granules. J Cell Sci 2005; 118: 4785-4795.
41. Ferrero-Pous M, Hersant AM, Pecking A, Bresard-Leroy M, Pichon MF,. Serum chromogranin-A in advanced prostate cancer. BJU Int 2001; 88: 790-796.
42. Krauss DJ, Amin M, Stone B, Ye H, Hayek S, Cotant M, Hafron J, Brabbins DS,. Chromogranin A staining as a prognostic variable in newly diagnosed Gleason score 7-10 prostate cancer treated with definitive radiotherapy. Prostate 2014; 74: 520-527.
43. Burchardt T, Burchardt M, Chen MW, Cao Y, de la Taille A, Shabsigh A, Hayek O, Dorai T, Buttyan R,. Transdifferentiation of prostate cancer cells to a neuroendocrine cell phenotype in vitro and in vivo. J Urol 1999; 162: 1800-1805.
44. Leiblich A, Cross SS, Catto JW, Pesce G, Hamdy FC, Rehman I,. Human prostate cancer cells express neuroendocrine cell markers PGP 9. 5 and chromogranin A. Prostate 2007; 67: 1761-1769.
45. Terry S, Beltran H,. The many faces of neuroendocrine differentiation in prostate cancer progression. Front Oncol 2014; 4: 60.
46. Sciarra A, Voria G, Monti S, Mazzone L, Mariotti G, Pozza M, D'Eramo G, Silverio FD,. Clinical understaging in patients with prostate adenocarcinoma submitted to radical prostatectomy: Predictive value of serum chromogranin A. Prostate 2004; 58: 421-428.
47. Weinstein MH, Partin AW, Veltri RW, Epstein JI,. Neuroendocrine differentiation in prostate cancer: enhanced prediction of progression after radical prostatectomy. Hum Pathol 1996; 27: 683-687.
48. Alessandro S, Vincenzo G, Maria AG, Stefano S, Alessandro G, Salvatore M, Vincenzo T, Franco DS,. Chromogranin A and biochemical progression-free survival in prostate adenocarcinomas submitted to radical prostatectomy. Endocr Relat Cancer 2007; 14: 625-632.
49. Gkonos PJ, Krongrad A, Roos BA,. Neuroendocrine peptides in the prostate. Urol Res 1995; 23: 81-87.
50. Jen PY, Dixon JS,. Development of peptide-containing nerves in the human fetal prostate gland. J Anat 1995; 187 (Pt 1): 169-179.
51. Tainio H,. Peptidergic innervation of the human prostate, seminal vesicle and vas deferens. Acta Histochem 1995; 97: 113-119.
52. Stridsberg M, Fabiani R, Lukinius A, Ronquist G,. Prostasomes are neuroendocrine-like vesicles in human semen. Prostate 1996; 29: 287-295.
53. Ronquist GK, Larsson A, Ronquist G, Isaksson A, Hreinsson J, Carlsson L, Stavreus-Evers A,. Prostasomal DNA characterization and transfer into human sperm. Mol Reprod Dev 2011; 78: 467-476.
54. Ronquist G, Brody I,. The prostasome: Its secretion and function in man. Biochim Biophys Acta 1985; 822: 203-218.
55. Escola JM, Kleijmeer MJ, Stoorvogel W, Griffith JM, Yoshie O, Geuze HJ,. Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J Biol Chem 1998; 273: 20121-20127.
56. Stridsberg M, Eriksson B, Oberg K, Janson ET,. A panel of 11 region-specific radioimmunoassays for measurements of human chromogranin A. Regul Pept 2004; 117: 219-227.
57. Stridsberg M, Eriksson B, Oberg K, Janson ET,. A panel of 13 region-specific radioimmunoassays for measurements of human chromogranin B. Regul Pept 2005; 125: 193-199.
58. Stridsberg M, Grimelius L, Portela-Gomes GM,. Immunohistochemical staining of human islet cells with region-specific antibodies against secretogranins II and III. J Anat 2008; 212: 229-234.
59. Portela-Gomes GM, Grimelius L, Stridsberg M,. Prohormone convertases 1/3, 2, furin and protein 7B2 (Secretogranin V) in endocrine cells of the human pancreas. Regul Pept 2008; 146: 117-124.
60. Stridsberg M, Lundqvist G, Engstrom U, Wilander E, Su H, Gobl A, Oberg K,. Development of polyclonal antibodies and evaluation of a sensitive radioimmunoassay for detection and measurement of synaptophysin. Acta Neuropathol 1994; 87: 635-641.
61. Hurley JH, Odorizzi G,. Get on the exosome bus with ALIX. Nat Cell Biol 2012; 14: 654-655.
62. Llorente A, van DB, Sandvig K,. Cholesterol regulates prostasome release from secretory lysosomes in PC-3 human prostate cancer cells. Eur J Cell Biol 2007; 86: 405-415.
63. Wiedenmann B, Franke WW, Kuhn C, Moll R, Gould VE,. Synaptophysin: A marker protein for neuroendocrine cells and neoplasms. Proc Natl Acad Sci USA 1986; 83: 3500-3504.
64. Bonanomi D, Rusconi L, Colombo CA, Benfenati F, Valtorta F,. Synaptophysin I selectively specifies the exocytic pathway of synaptobrevin 2/VA MP2. Biochem J 2007; 404: 525-534.
65. Arthur CP, Stowell MH,. Structure of synaptophysin: A hexameric MARVEL-domain channel protein. Structure 2007; 15: 707-714.
66. Leube RE, Leimer U, Grund C, Franke WW, Harth N, Wiedenmann B,. Sorting of synaptophysin into special vesicles in nonneuroendocrine epithelial cells. J Cell Biol 1994; 127: 1589-1601.
67. Tavoosidana G, Ronquist G, Darmanis S, Yan J, Carlsson L, Wu D, Conze T, Ek P, Semjonow A, Eltze E, Larsson A, Landegren UD, Kamali-Moghaddam M,. Multiple recognition assay reveals prostasomes as promising plasma biomarkers for prostate cancer. Proc Natl Acad Sci USA 2011; 108: 8809-8814.
68. Bonkhoff H,. Neuroendocrine differentiation in human prostate cancer. Morphogenesis, proliferation and androgen receptor status. Ann Oncol 2001; 12 (Suppl 2): S141-S144.