Survivin is released from cancer cells via exosomes

Apoptosis

Volumn 16, Issue 1, 2011, Pages 1-12

  Khan, Salma ^a   Jutzy, Jessica M S ^a   Aspe, Jonathan R ^a   McGregor, Dalmor W ^a   Neidigh, Jonathan W ^a   Wall, Nathan R ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Cancer; Exosomes; Microenvironment; Survivin

Indexed keywords

HEAT SHOCK PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN; SURVIVIN;

APOPTOSIS; ARTICLE; CANCER CELL; CELL HYPOXIA; CELL INVASION; CELL NUCLEUS; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CYTOPLASM; EXOCYTOSIS; EXOSOME; EXTRACELLULAR FLUID; EXTRACELLULAR SPACE; HELA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; MITOCHONDRION; MITOSIS; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTON RADIATION; QUANTITATIVE ANALYSIS; TUMOR CELL; UPREGULATION;

APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; CYSTEINE PROTEINASE INHIBITORS; CYTOSKELETON; EXOCYTOSIS; EXOSOMES; EXTRACELLULAR SPACE; FEMALE; GENE EXPRESSION; HELA CELLS; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; PROTONS; RADIOISOTOPES; SECRETORY PATHWAY; UP-REGULATION; UTERINE CERVICAL NEOPLASMS;

EID: 79951551519     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-010-0534-4     Document Type: Article

References (52)

1. S Aznavoorian ML Stracke H Krutzsch E Schiffmann LA Liotta 1990 Signal transduction for chemotaxis and haptotaxis by matrix molecules in tumor cells J Cell Biol 110 1427 1438 1:CAS:528:DyaK3cXktVeru78%3D 10.1083/jcb.110.4.1427 2324200
2. H Ohtani 1998 Stromal reaction in cancer tissue: pathophysiologic significance of the expression of matrix-degrading enzymes in relation to matrix turnover and immune/inflammatory reactions Pathol Int 48 1 9 1:CAS:528:Dya (Pubitemid 28204701)
3. MW Graner RI Cumming DD Bigner 2007 The heat shock response and chaperones/heat shock proteins in brain tumors: surface expression, release, and possible immune consequences J Neurosci 27 11214 11227 1:CAS:528: DC%2BD2sXht1ekur3O 10.1523/JNEUROSCI.3588-07.2007 17942716 (Pubitemid 47621325)
4. BK Eustace DG Jay 2004 Extracellular roles for the molecular chaperone, hsp90 Cell Cycle 3 1098 1100 1:CAS:528:DC%2BD2MXntVantb0%3D 10.4161/cc.3.9.1088 15326368 (Pubitemid 40268620)
5. J Radons G Multhoff 2005 Immunostimulatory functions of membrane-bound and exported heat shock protein 70 Exerc Immunol Rev 11 17 33 16385841
6. DC Altieri 2003 Survivin, versatile modulation of cell division and apoptosis in cancer Oncogene 22 8581 8589 1:CAS:528:DC%2BD3sXptFOmtbY%3D 10.1038/sj.onc.1207113 14634620 (Pubitemid 38019195)
7. F Li G Ambrosini EY Chu, et al. 1998 Control of apoptosis and mitotic spindle checkpoint by survivin Nature 396 580 584 1:CAS:528:DyaK1cXotVWns70%3D 10.1038/25141 9859993 (Pubitemid 28563719)
8. DC Altieri 2006 The case for survivin as a regulator of microtubule dynamics and cell-death decisions Curr Opin Cell Biol 18 609 615 1:CAS:528:DC%2BD28XhtF2qtbjJ 10.1016/j.ceb.2006.08.015 16934447 (Pubitemid 44692469)
9. P Fortugno NR Wall A Giodini, et al. 2002 Survivin exists in immunochemically distinct subcellular pools and is involved in spindle microtubule function J Cell Sci 115 575 585 1:CAS:528:DC%2BD38XitVWmurg%3D 11861764 (Pubitemid 34182984)
10. S Khan JR Aspe MG Asumen, et al. 2009 Extracellular, cell-permeable survivin inhibits apoptosis while promoting proliferative and metastatic potential Br J Cancer 100 1073 1086 1:CAS:528:DC%2BD1MXktVGksbY%3D 10.1038/sj.bjc.6604978 19293795
11. T Dohi E Beltrami NR Wall J Plescia DC Altieri 2004 Mitochondrial survivin inhibits apoptosis and promotes tumorigenesis J Clin Invest 114 1117 1127 1:CAS:528:DC%2BD2cXovVensrc%3D 15489959 (Pubitemid 39578701)
12. JC Ghosh T Dohi BH Kang DC Altieri 2008 Hsp60 regulation of tumor cell apoptosis J Biol Chem 283 5188 5194 1:CAS:528:DC%2BD1cXhvFektrg%3D 10.1074/jbc.M705904200 18086682
13. P Fortugno E Beltrami J Plescia, et al. 2003 Regulation of survivin function by Hsp90 Proc Natl Acad Sci USA 100 13791 13796 1:CAS:528: DC%2BD3sXpsFGisrc%3D 10.1073/pnas.2434345100 14614132 (Pubitemid 37499145)
14. J Plescia W Salz F Xia, et al. 2005 Rational design of shepherdin, a novel anticancer agent Cancer Cell 7 457 468 1:CAS:528:DC%2BD2MXkslyitLs%3D 10.1016/j.ccr.2005.03.035 15894266 (Pubitemid 40719129)
15. K Farsad 2002 Exosomes: novel organelles implicated in immunomodulation and apoptosis Yale J Biol Med 75 95 101 1:CAS:528:DC%2BD38Xntl2lsLY%3D 12230314 (Pubitemid 34925444)
16. X Yu SL Harris AJ Levine 2006 The regulation of exosome secretion: a novel function of the p53 protein Cancer Res 66 4795 4801 1:CAS:528: DC%2BD28XjvF2kt74%3D 10.1158/0008-5472.CAN-05-4579 16651434
17. QL Hao AJ Shah FT Thiemann EM Smogorzewska GM Crooks 1995 A functional comparison of CD34 + CD38- cells in cord blood and bone marrow Blood 86 3745 3753 1:CAS:528:DyaK2MXptlWjurY%3D 7579341
18. CY Wang W Azzo A Al-Katib N Chiorazzi DM Knowles 2nd 1984 Preparation and characterization of monoclonal antibodies recognizing three distinct differentiation antigens (BL1, BL2, BL3) on human B lymphocytes J Immunol 133 684 691 1:CAS:528:DyaL2cXkvVymtrg%3D 6429242 (Pubitemid 14093451)
19. H Ogawa K Ishiguro S Gaubatz DM Livingston Y Nakatani 2002 A complex with chromatin modifiers that occupies E2F- and Myc-responsive genes in G0 cells Science 296 1132 1136 1:CAS:528:DC%2BD38XjslamtLY%3D 10.1126/science.1069861 12004135 (Pubitemid 34517133)
20. Y Shi J Sawada G Sui, et al. 2003 Coordinated histone modifications mediated by a CtBP co-repressor complex Nature 422 735 738 1:CAS:528: DC%2BD3sXivFGhsLs%3D 10.1038/nature01550 12700765 (Pubitemid 36514114)
21. JK Eng AL McCormack JR Yates III 1994 An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database J Am Soc Mass Spectrom 5 976 989 1:CAS:528:DyaK2MXhvF2htLw%3D 10.1016/1044-0305(94)80016-2
22. DN Perkins DJ Pappin DM Creasy JS Cottrell 1999 Probability-based protein identification by searching sequence databases using mass spectrometry data Electrophoresis 20 3551 3567 1:CAS:528:DC%2BD3cXhtF2ntw%3D%3D 10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2 10612281 (Pubitemid 30007252)
23. R Craig RC Beavis 2004 TANDEM: matching proteins with tandem mass spectra Bioinformatics 20 1466 1467 1:CAS:528:DC%2BD2cXkvVSrtLs%3D 10.1093/ bioinformatics/bth092 14976030 (Pubitemid 38931421)
24. A Keller AI Nesvizhskii E Kolker R Aebersold 2002 Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search Anal Chem 74 5383 5392 1:CAS:528:DC%2BD38XmvVyktL4%3D 10.1021/ac025747h 12403597 (Pubitemid 35215372)
25. AI Nesvizhskii A Keller E Kolker R Aebersold 2003 A statistical model for identifying proteins by tandem mass spectrometry Anal Chem 75 4646 4658 1:CAS:528:DC%2BD3sXltlynt70%3D 10.1021/ac0341261 14632076 (Pubitemid 37082259)
26. A Savina M Furlan M Vidal MI Colombo 2003 Exosome release is regulated by a calcium-dependent mechanism in K562 cells J Biol Chem 278 20083 20090 1:CAS:528:DC%2BD3sXktVaqurk%3D 10.1074/jbc.M301642200 12639953 (Pubitemid 36799202)
27. Thery C, Clayton A, Amigorena S, Raposo G (2006) Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol (Suppl 30): 3.22.21-23.22.29
28. A Savina M Vidal MI Colombo 2002 The exosome pathway in K562 cells is regulated by Rab11 J Cell Sci 115 2505 2515 1:CAS:528:DC%2BD38XlsVCqur4%3D 12045221 (Pubitemid 34778068)
29. A Clayton J Court H Navabi, et al. 2001 Analysis of antigen presenting cell derived exosomes, based on immuno-magnetic isolation and flow cytometry J Immunol Methods 247 163 174 1:CAS:528:DC%2BD3MXitlymtA%3D%3D 10.1016/S0022-1759(00)00321-5 11150547 (Pubitemid 32057053)
30. DF Liao ZG Jin AS Baas, et al. 2000 Purification and identification of secreted oxidative stress-induced factors from vascular smooth muscle cells J Biol Chem 275 189 196 1:CAS:528:DC%2BD3cXjvVGrsA%3D%3D 10.1074/jbc.275.1.189 10617604 (Pubitemid 30038971)
31. P Caroni A Rothenfluh E McGlynn C Schneider 1991 S-cyclophilin. New member of the cyclophilin family associated with the secretory pathway J Biol Chem 266 10739 10742 1:CAS:528:DyaK38Xht1ertr0%3D 2040593 (Pubitemid 21906866)
32. B Sherry N Yarlett A Strupp A Cerami 1992 Identification of cyclophilin as a proinflammatory secretory product of lipopolysaccharide-activated macrophages Proc Natl Acad Sci USA 89 3511 3515 1:CAS:528:DyaK38XisFeku74%3D 10.1073/pnas.89.8.3511 1565646
33. M Iero R Valenti V Huber, et al. 2008 Tumour-released exosomes and their implications in cancer immunity Cell Death Differ 15 80 88 1:CAS:528: DC%2BD2sXhsVegur3J 10.1038/sj.cdd.4402237 17932500 (Pubitemid 350286175)
34. JD Bendtsen H Nielsen G von Heijne S Brunak 2004 Improved prediction of signal peptides: SignalP 3.0 J Mol Biol 340 783 795 10.1016/j.jmb.2004.05.028 15223320 (Pubitemid 38829638)
35. GI Lancaster MA Febbraio 2005 Exosome-dependent trafficking of HSP70: a novel secretory pathway for cellular stress proteins J Biol Chem 280 23349 23355 1:CAS:528:DC%2BD2MXltVygsrc%3D 10.1074/jbc.M502017200 15826944 (Pubitemid 40853248)
36. RM Johnstone 2006 Exosomes biological significance: a concise review Blood Cells Mol Dis 36 315 321 1:CAS:528:DC%2BD28XivVGrtr0%3D 10.1016/j.bcmd.2005.12.001 16487731
37. A Clayton A Turkes H Navabi MD Mason Z Tabi 2005 Induction of heat shock proteins in B-cell exosomes J Cell Sci 118 3631 3638 1:CAS:528: DC%2BD2MXhtVaktrjN 10.1242/jcs.02494 16046478 (Pubitemid 41309410)
38. HG Lamparski A Metha-Damani JY Yao, et al. 2002 Production and characterization of clinical grade exosomes derived from dendritic cells J Immunol Methods 270 211 226 1:CAS:528:DC%2BD38XnvVOntLg%3D 12379326
39. R Gastpar M Gehrmann MA Bausero, et al. 2005 Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells Cancer Res 65 5238 5247 1:CAS:528:DC%2BD2MXltFemu7w%3D 10.1158/0008-5472.CAN-04-3804 15958569 (Pubitemid 40827334)
40. A Mathew A Bell RM Johnstone 1995 Hsp-70 is closely associated with the transferrin receptor in exosomes from maturing reticulocytes Biochem J 308 Pt 3 823 830 1:CAS:528:DyaK2MXmsFWju7w%3D 8948438
41. Y Tajika T Matsuzaki T Suzuki, et al. 2005 Differential regulation of AQP2 trafficking in endosomes by microtubules and actin filaments Histochem Cell Biol 124 1 12 1:CAS:528:DC%2BD2MXpslahu70%3D 10.1007/s00418-005-0010-3 16049696 (Pubitemid 41253158)
42. K Takata 2006 Aquaporin-2 (AQP2): its intracellular compartment and trafficking Cell Mol Biol (Noisy-le-grand) 52 34 39 1:CAS:528: DC%2BD2sXksVSksLk%3D (Pubitemid 46683294)
43. G Mignot S Roux C Thery E Segura L Zitvogel 2006 Prospects for exosomes in immunotherapy of cancer J Cell Mol Med 10 376 388 1:CAS:528: DC%2BD2sXlvFCltbw%3D 10.1111/j.1582-4934.2006.tb00406.x 16796806 (Pubitemid 44870186)
44. JM Escola MJ Kleijmeer W Stoorvogel JM Griffith O Yoshie HJ Geuze 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 1:CAS:528:DyaK1cXlsVWgsbs%3D 10.1074/jbc.273.32.20121 9685355 (Pubitemid 28377568)
45. KM Valentijn FD Gumkowski JD Jamieson 1999 The subapical actin cytoskeleton regulates secretion and membrane retrieval in pancreatic acinar cells J Cell Sci 112 Pt 1 81 96 1:CAS:528:DyaK1MXpvFOrtg%3D%3D 9841906 (Pubitemid 29043837)
46. K Matter F Dreyer K Aktories 1989 Actin involvement in exocytosis from PC12 cells: studies on the influence of botulinum C2 toxin on stimulated noradrenaline release J Neurochem 52 370 376 1:CAS:528:DyaL1MXhtVykt7g%3D 10.1111/j.1471-4159.1989.tb09131.x 2492057 (Pubitemid 19037598)
47. K Sandvig B van Deurs 1990 Selective modulation of the endocytic uptake of ricin and fluid phase markers without alteration in transferrin endocytosis J Biol Chem 265 6382 6388 1:CAS:528:DyaK3cXhvFGktL8%3D 1969411
48. AC Mita MM Mita ST Nawrocki FJ Giles 2008 Survivin: key regulator of mitosis and apoptosis and novel target for cancer therapeutics Clin Cancer Res 14 5000 5005 1:CAS:528:DC%2BD1cXpslKgsbs%3D 10.1158/1078-0432.CCR-08-0746 18698017
49. NR Galloway JR Aspe C Sellers NR Wall 2009 Enhanced antitumor effect of combined gemcitabine and proton radiation in the treatment of pancreatic cancer Pancreas 38 782 790 1:CAS:528:DC%2BD1MXhtFOjtLvK 10.1097/MPA.0b013e3181a85999 19506533
50. S Mera M Magnusson A Tarkowski M Bokarewa 2008 Extracellular survivin up-regulates adhesion molecules on the surface of leukocytes changing their reactivity pattern J Leukoc Biol 83 149 155 1:CAS:528:DC%2BD1cXks1Sqsw%3D%3D 10.1189/jlb.0507287 17938276
51. M Bokarewa S Lindblad D Bokarew A Tarkowski 2005 Balance between survivin, a key member of the apoptosis inhibitor family, and its specific antibodies determines erosivity in rheumatoid arthritis Arthritis Res Ther 7 R349 R358 1:CAS:528:DC%2BD2MXhslagtLs%3D 10.1186/ar1498 15743483
52. EA Kapp F Schutz LM Connolly, et al. 2005 An evaluation, comparison, and accurate benchmarking of several publicly available MS/MS search algorithms: sensitivity and specificity analysis Proteomics 5 3475 3490 1:CAS:528: DC%2BD2MXps12itbs%3D 10.1002/pmic.200500126 16047398 (Pubitemid 41192052)