Tumor cells derived exosomes contain hTERT mRNA and transform nonmalignant fibroblasts into telomerase positive cells

Oncotarget

Volumn 7, Issue 37, 2016, Pages 59173-59188

  Gutkin, Anna ^a   Uziel, Orit ^a,b   Beery, Einat ^a   Nordenberg, Jardena ^a,b   Pinchasi, Maria ^a,b   Goldvaser, Hadar ^a   Henick, Steven ^a   Goldberg, Michal ^c   Lahav, Meir ^a,b  

^a RABIN MEDICAL CENTER   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Exosomes; Telomerase

Indexed keywords

DNA; MESSENGER RNA; PHLEOMYCIN; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; TERT PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CELL AGING; CELL ISOLATION; CELL PROLIFERATION; CELL TRANSFORMATION; DNA DAMAGE; ENZYME ACTIVITY; ENZYME RELEASE; EXOSOME; FIBROBLAST; HUMAN; HUMAN CELL; LIFESPAN; LUNG CANCER; PANCREAS CANCER; PHENOTYPE; PROTEIN EXPRESSION; TUMOR CELL; TUMOR MICROENVIRONMENT; CELL SELF-RENEWAL; CELL SURVIVAL; GENETICS; JURKAT CELL LINE; K-562 CELL LINE; LUNG TUMOR; METABOLISM; PANCREAS TUMOR; PATHOLOGY;

CELL SELF RENEWAL; CELL SURVIVAL; CELLULAR SENESCENCE; EXOSOMES; FIBROBLASTS; HUMANS; JURKAT CELLS; K562 CELLS; LUNG NEOPLASMS; PANCREATIC NEOPLASMS; RNA, MESSENGER; TELOMERASE; TUMOR MICROENVIRONMENT;

EID: 84991338093     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.10384     Document Type: Article

References (50)

1. Bryan TM, & Cech TR, Telomerase and the maintenance of chromosome ends. Curr. Opin. Cell Biol. 1999; 11: 318-24
2. Jaiswal RK, Kumar P, Yadava PK. Telomerase and its extracurricular activities. Cell Mol Biol Lett. 2013 18:538-54
3. Shay, JW. Telomerase and cancer. Hum. Mol. Genet. 2001; 10: 677-85
4. Hoffman RM. Stromal-cell and cancer-cell exosomes leading the metastatic exodus for the promised niche. Breast Cancer Res. 2013; 15:310
5. Johnstone, RM, Adam, M, Hammond, J R, Orr L & Turbide C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J. Biol. Chem. 1987; 262: 9412-20
6. Mathivanan S, Simpson RJ. ExoCarta: A compendium of exosomal proteins and RNA. Proteomics 2009; 9:4997-5000
7. Wolfers J, Lozier A, Raposo G, Regnault A, Théry C, Masurier C, Flament C, Pouzieux S, Faure F, Tursz T, Angevin E, Amigorena S, Zitvogel L. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med 2001; 7:297-303
8. Ge R, Tan E, Sharghi-Namini S, and Asada H H. Exosomes in Cancer Microenvironment and Beyond: have we Overlooked these Extracellular Messengers? Cancer Microenviron. 2012; 5: 323-32
9. Bissell MJ, Hines WC. Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat Med 2011; 17:320-9
10. Kenny PA, Lee GY, Bissell MJ. Targeting the tumor microenvironment. Front Biosci 2007; 12:3468-74
11. Hong BS, Cho JH, Kim H, Choi EJ, Rho S, Kim J, Kim JH, Choi DS, Kim YK, Hwang D, Gho YS. Colorectal cancer cell derived microvesicles are enriched in cell cycle-related mRNAs that promote proliferation of endothelial cells. BMC Genomics 2009; 10:556
12. Al-Nedawi K, Meehan B, Kerbel RS, Allison AC, Rak J. Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci U S A 2009; 106:3794-99
13. Gesierich S, Berezovskiy I, Ryschich E, Zoller M. Systemic induction of the angiogenesis switch by the tetraspanin D6.1A/CO-029. Cancer Res 2006; 66:7083-94
14. Nazarenko I, Rana S, Baumann A, McAlear J, Hellwig A, Trendelenburg M, Lochnit G, Preissner KT, Zöller M. Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation. Cancer Res 2010; 70:1668-78
15. Hood JL, Pan H, LanzaGM, Wickline SA. Paracrine induction of endothelium by tumor exosomes. Lab Invest 2009; 89:1317-28
16. Skog J, Würdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT Jr, Carter BS, Krichevsky AM, Breakefield XO. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008; 10:1470-6
17. Webber J, Steadman R, Mason MD, Tabi Z, Clayton A. Cancer exosomes trigger fibroblast to myofibroblast differentiation. Cancer Res 2010; 70:9621-30
18. Runz S, Keller S, Rupp C, Stoeck A, Issa Y, Koensgen D, Mustea A, Sehouli J, Kristiansen G, Altevogt P. Malignant ascitesderived exosomes of ovarian carcinoma patients contain CD24 and EpCAM. Gynecol Oncol 2007; 107:563-71
19. Dolo V, D'Ascenzo S, Violini S, Pompucci L, Festuccia C, Ginestra A, et al. Matrixdegrading proteinases are shed in membrane vesicles by ovarian cancer cells in vivo and in vitro. Clin Exp Metastasis 1999; 17:131-40
20. Dolo V, Ginestra A, Cassara D, Ghersi G, Nagase H, Vittorelli ML. Shed membrane vesicles and selective localization of gelatinases and MMP-9/TIMP-1 complexes. Ann NY Acad Sci 1999; 878:497-9
21. Graves LE, Ariztia EV, Navari JR, Matzel HJ, Stack MS, Fishman DA. Proinvasive properties of ovarian cancer ascitesderived membrane vesicles. Cancer Res 2004; 64:7045-9
22. Gutwein P, Stoeck A, Riedle S, Gast D, Runz S, Condon TP, Marmé A, Phong MC, Linderkamp O, Skorokhod A, Altevogt P. Cleavage of L1 in exosomes and apoptotic membrane vesicles released from ovarian carcinoma cells. Clin Cancer Res 2005; 11:2492-501
23. Stoeck A, Keller S, Riedle S, Sanderson MP, Runz S, Le Naour, Gutwein P, Ludwig A, Rubinstein E, Altevogt P. A role for exosomes in the constitutive and stimulus-induced ectodomain cleavage of L1 and CD44. Biochem J 2006; 393:609-18
24. Curtis L, Machalinski B, Ratajczak J, Ratajczak MZ. Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int J Cancer 2005; 113:752-60
25. Janowska-Wieczorek A, Marquez-Curtis LA, Wysoczynski M, Ratajczak MZ. Enhancing effect of platelet-derived microvesicles on the invasive potential of breast cancer cells. Transfusion 2006; 46:1199-1209
26. Deregibus MC, Cantaluppi V, Calogero R, Lo Iacono M, Tetta C, Biancone L, Bruno S, Bussolati B, Camussi G. Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 2007; 110:2440-8
27. Campello E, Spiezia L, Radu CM, Bulato C, Castelli M, Gavasso S, Simioni P. al. Endothelial, platelet, and tissue factorbearing microparticles in cancer patients with and without venous thromboembolism. Thromb Res 2011; 127:473-7
28. Milane L, Singh A, Mattheolabakis G, Suresh M, Amiji MM. Exosome mediated communication within the tumor microenvironment. J Control Release 2015; 219:278-94
29. K Hiyama, E Hiyama, S Ishioka, M Yamakido, K Inai, A F. Gazdar, M A. Piatyszek and Jerry W. Shay. Telomerase Activity in Small-Cell and Non-Small-Cell Lung Cancers. JNCI 1995; 87: 895-902)
30. Ram R, Uziel O, Lahav M. The importance of the telomere and telomerase system in hematological malignancies. Leuk Lymphoma 2005; 46:1121-35
31. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007; 9:654-9
32. Skog J, Würdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves Curry WT Jr, Carter BS, Krichevsky AM, Breakefield XO. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008; 10:1470-6
33. Jaiswal RK, Kumar P, Yadava PK. Telomerase and its extracurricular activities. Cell Mol Biol Lett. 2013; 18:538-54
34. Stewart SA. Multiple levels of telomerase regulation. Mol Interv. 2002; 2:481-3
35. Nazarenko I., Rana S., Baumann A. McAlear J, Hellwig A, Trendelenburg M, Lochnit G, Preissner KT, Zöller M. Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation. Cancer Research 2010; 70: 1668-78
36. Wu ZQ, Guo QL, You QD, Zhao L, Gu HY. Gambogic acid inhibits proliferation of human lung carcinoma SPC-A1 cells in vivo and in vitro and represses telomerase activity and telomerase reverse transcriptase mRNA expression in the cells. Biol Pharm Bull. 2004; 27:1769-74
37. Uziel O, Kanfer G, Beery E, Yelin D, Shepshelovich D, Bakhanashvili M, Nordenberg J, Lahav M. The effects of erythropoietin signaling on telomerase regulation in nonerythroid malignant and non-malignant cells. Biochem Biophys Res Commun. 2014; 450:274-82
38. Cao Y, Li H, Deb S, Liu JP. TERT regulates cell survival independent of telomerase enzymatic activity. Oncogene. 2002; 21:3130-8
39. Chadeneau C, Siegel P, Harley CB, Muller WJ, Bacchetti S. Telomerase activity in normal and malignant murine tissues. Oncogene. 1995; 11:893-8
40. Sarin KY, Cheung P, Gilison D, Lee E, Tennen RI, Wang E, Artandi MK, Oro AE, Artandi SE. Conditional telomerase induction causes proliferation of hair follicle stem cells. Nature. 2005; 436:1048-52
41. Jiang XR, Jimenez G, Chang E, Frolkis M, Kusler B, Sage M, Beeche M, Bodnar AG, Wahl GM, Tlsty TD, Chiu CP. Telomerase expression in human somatic cells does not induce changes associated with a transformed phenotype. Nat Genet. 1999; 21:111-4
42. Bonifacio LN, Jarstfer MB. MiRNA profile associated with replicative senescence, extended cell culture, and ectopic telomerase expression in human foreskin fibroblasts. PLoS One. 2010; 5. pii: e12519
43. Bodnar AG, Ouellette M, Frolkis M, Holt SE, Chiu CP, Morin GB, Harley CB, Shay JW, Lichtsteiner S, Wright WE. Extension of life-span by introduction of telomerase into normal human cells. Science. 1998; 279:349-52
44. Ohshima S. Apoptosis and necrosis in senescent human fibroblasts. Ann N Y Acad Sci. 2006; 1067:228-34
45. Raz V, Vermolen BJ, Garini Y, Onderwater JJ, Mommaas-Kienhuis MA, Koster AJ. The nuclear lamina promotes telomere aggregation and centromere peripheral localization during senescence of human mesenchymal stem cells. J Cell Sci. 2008; 121:4018-28
46. Haithcock E, Dayani Y, Neufeld E, Zahand A J, Feinstein, AMattout N, Gruenbaum Y, Liu J. Age-related changes of nuclear architecture in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 200; 102:16690-5
47. Colombo M, Moita C, van Niel G, Kowal J, Vigneron J, Benaroch P, Manel N, Moita LF, Théry C, Raposo G. Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J Cell Sci. 2013; 126:5553-65
48. Asai A, Oshima Y, Yamamoto Y, Uochi TA, Kusaka H, Akinaga S, Yamashita Y, Pongracz K, Pruzan R, Wunder E, Piatyszek M, Li S, Chin AC, Harley CB, Gryaznov S. A novel telomerase template antagonist (GRN163) as a potential anticancer agent. Cancer Res. 2003; 63:3931-9
49. Lukas C, Melander F, Stucki M, Falck J, Bekker-Jensen S, Goldberg M, Lerenthal Y, Jackson SP, Bartek J, Lukas J. Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J. 2004; 23:2674-83
50. Riahi Y, Kaiser N, Cohen G, Abd-Elrahman I, Blum G, Shapira OM, Koler T, Simionescu M, Sima AV, Zarkovic N, Zarkovic K, Orioli M, Aldini G, Cerasi E, Leibowitz G, Sasson S. Foam cell-derived 4-hydroxynonenal induces endothelial cell senescence in a TXNIP-dependent manner. J Cell Mol Med. 2015; 19:1887-99