Massive release of extracellular vesicles from cancer cells after photodynamic treatment or chemotherapy

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Aubertin, Kelly ^a   Silva, Amanda K A ^a   Luciani, Nathalie ^a   Espinosa, Ana ^a   Djemat, Aurélie ^b   Charue, Dominique ^c   Gallet, François ^a   Blanc Brude, Olivier ^c   Wilhelm, Claire ^a  

^a UNIVERSITÉ PARIS DIDEROT   (France)

^b INSTITUT JACQUES MONOD   (France)

^c PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; MICRORNA;

ANIMAL; DRUG EFFECT; DRUG SCREENING; EXOSOME; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MACROPHAGE; MALE; MOUSE; PATHOLOGY; PHOTOCHEMOTHERAPY; PROSTATE TUMOR; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; DOXORUBICIN; EXTRACELLULAR VESICLES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MACROPHAGES; MALE; MICE; MICRORNAS; PHOTOCHEMOTHERAPY; PROSTATIC NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84993967403     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep35376     Document Type: Article

References (52)

1. Balkwill, F., Charles K. A. & Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 7, 211-217 (2005).
2. Lin, W.-W. & Karin M. A cytokine-mediated link between innate immunity, inflammation, and cancer. J Clin Invest 117, 1175-1183 (2007).
3. Parmiani, G. & Maccalli C. The early antitumor immune response is necessary for tumor growth: Re-visiting Prehns hypothesis in the human melanoma system. Oncoimmunology 1, 930-934 (2012).
4. Rivoltini, L. et al. Escape strategies and reasons for failure in the interaction between tumour cells and the immune system: how can we tilt the balance towards immune-mediated cancer control? Expert Opin Biol Ther 5, 463-476 (2005).
5. Zou, W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 5, 263-274 (2005).
6. Motz, Greg T. & Coukos G. Deciphering and Reversing Tumor Immune Suppression. Immunity 39, 61-73 (2013).
7. Iero, M. et al. Tumour-released exosomes and their implications in cancer immunity. Cell Death Differ 15, 80-88 (2007).
8. Al-Nedawi, K., Meehan B. & Rak J. Microvesicles: messengers and mediators of tumor progression. Cell Cycle 8, 2014-2018 (2009).
9. Al-Nedawi, K., Meehan B., Kerbel R. S., Allison A. C. & Rak J. Endothelial expression of autocrine VEGF upon the uptake of tumorderived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci USA 106, 3794-3799 (2009).
10. Al-Nedawi, K. et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol 10, 619-624 (2008).
11. Krause, M., Samoylenko A. & Vainio S. J. Exosomes as renal inductive signals in health and disease, and their application as diagnostic markers and therapeutic agents. Front Cell Dev Biol 3, 65 (2015).
12. Kim, J. W. et al. Fas ligand-positive membranous vesicles isolated from sera of patients with oral cancer induce apoptosis of activated T lymphocytes. Clin Cancer Res 11, 1010-1020 (2005).
13. Valenti, R. et al. Tumor-released microvesicles as vehicles of immunosuppression. Cancer Res 67, 2912-2915 (2007).
14. Dolo, V. et al. Matrix-degrading proteinases are shed in membrane vesicles by ovarian cancer cells in vivo and in vitro. Clin Exp Metastasis 17, 131-140 (1999).
15. Kim, C. W. et al. Extracellular membrane vesicles from tumor cells promote angiogenesis via sphingomyelin. Cancer Res 62, 6312-6317 (2002).
16. Safaei, R. et al. Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells. Mol Cancer Ther 4, 1595-1604 (2005).
17. Gong, J. et al. Microparticles and their emerging role in cancer multidrug resistance. Cancer Treat Rev 38, 226-234 (2012).
18. Ciravolo, V. et al. Potential role of HER2-overexpressing exosomes in countering trastuzumab-based therapy. J Cell Physiol 227, 658-667 (2012).
19. Shedden, K., Xie X. T., Chandaroy P., Chang Y. T. & Rosania G. R. Expulsion of small molecules in vesicles shed by cancer cells association with gene expression and chemosensitivity profiles. Cancer Res 63, 4331-4337 (2003).
20. Brown, S. B., Brown E. A. & Walker I. The present and future role of photodynamic therapy in cancer treatment. Lancet Oncol 5, 497-508 (2004).
21. Allison, R. R. & Sibata C. H. Oncologic photodynamic therapy photosensitizers: A clinical review. Photodiagnosis Photodyn Ther 7, 61-75 (2010).
22. Evens, A. M. et al. The efficacy and tolerability of adriamycin, bleomycin, vinblastine, dacarbazine and Stanford V in older Hodgkin lymphoma patients: a comprehensive analysis from the North American intergroup trial E2496. Br J Haematol 161, 76-86 (2013).
23. Gupta, A., Yao X., Verma S., Mackay H. & Hopkins L. Chemotherapy (gemcitabine, docetaxel plus gemcitabine, doxorubicin, or trabectedin) in inoperable, locally advanced, recurrent, or metastatic uterine leiomyosarcoma: a clinical practice guideline. Curr Oncol 20, e448 (2013).
24. Senge, M. O. & Brandt J. C. Temoporfin (Foscan, 5, 10, 15, 20-Tetra (m-hydroxyphenyl) chlorin) - A Second-generation Photosensitizer. Photochem Photobiol 87, 1240-1296 (2011).
25. Moore, C. et al. Photodynamic therapy using meso tetra hydroxy phenyl chlorin (mTHPC) in early prostate cancer. Lasers Surg Med 38, 356-363 (2006).
26. Souza, C. S. et al. Long-term follow-up of topical 5-aminolaevulinic acid photodynamic therapy diode laser single session for nonmelanoma skin cancer. Photodiagnosis Photodyn Ther 6, 207-213 (2009).
27. Speth, P., Van Hoesel Q. & Haanen C. Clinical pharmacokinetics of doxorubicin. Clin Pharmacokinet 15, 15-31 (1988).
28. Sasnouski, S. et al. Investigation of Foscan interactions with plasma proteins. Biochim Biophys Acta 1725, 394-402 (2005).
29. Mojzisova, H., Bonneau S. & Brault D. Structural and physico-chemical determinants of the interactions of macrocyclic photosensitizers with cells. Eur Biophys J 36, 943-953 (2007).
30. Janes, K. A., Fresneau M. P., Marazuela A., Fabra A. & Alonso, M. a. J. Chitosan nanoparticles as delivery systems for doxorubicin. J Control Release 73, 255-267 (2001).
31. Zeman, S. M., Phillips D. R. & Crothers D. M. Characterization of covalent Adriamycin-DNA adducts. Proc Natl Acad Sci USA 95, 11561-11565 (1998).
32. Hugel, B., Martinez M. C., Kunzelmann C. & Freyssinet J.-M. Membrane microparticles: two sides of the coin. Physiology 20, 22-27 (2005).
33. Yang, X.-H. et al. Reconstitution of caspase 3 sensitizes MCF-7 breast cancer cells to doxorubicin-and etoposide-induced apoptosis. Cancer Res 61, 348-354 (2001).
34. Kluza, J. et al. Mitochondrial proliferation during apoptosis induced by anticancer agents: effects of doxorubicin and mitoxantrone on cancer and cardiac cells. Oncogene 23, 7018-7030 (2004).
35. Dragovic, R. A. et al. Sizing and phenotyping of cellular vesicles using Nanoparticle Tracking Analysis. Sizing and phenotyping of cellular vesicles using Nanoparticle Tracking Analysis 7, 780-788 (2011).
36. Arraud, N., Gounou C., Turpin D. & Brisson A. R. Fluorescence triggering: A general strategy for enumerating and phenotyping extracellular vesicles by flow cytometry. Cytometry A 89, 184-195 (2016).
37. Pol, E. et al. Particle size distribution of exosomes and microvesicles determined by transmission electron microscopy, flow cytometry, nanoparticle tracking analysis, and resistive pulse sensing. J Thromb Haemost 12, 1182-1192 (2014).
38. Loubery, S. et al. Different microtubule motors move early and late endocytic compartments. Traffic 9, 492-509 (2008).
39. Andriola Silva, A. K., Di Corato R., Gazeau F., Pellegrino T. & Wilhelm C. Magnetophoresis at the nanoscale: tracking the magnetic targeting efficiency of nanovectors. Nanomedicine 7, 1713-1727 (2012).
40. Thery, C., Ostrowski M. & Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9, 581-593 (2009).
41. Balaj, L. et al. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun 2, 180 (2011).
42. Antonyak, M. A. et al. Cancer cell-derived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells. Proc Natl Acad Sci USA 108, 4852-4857 (2011).
43. Peinado, H. et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 18, 883-891 (2012).
44. Chen, V. Y., Posada M. M., Blazer L. L., Zhao T. & Rosania G. R. The role of the VPS4A-exosome pathway in the intrinsic egress route of a DNA-binding anticancer drug. Pharm Res 23, 1687-1695 (2006).
45. Shao, H. et al. Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy. Nat Med 18, 1835-1840 (2012).
46. Mitchell, P. J. et al. Can urinary exosomes act as treatment response markers in prostate cancer. J Transl Med 7 (2009).
47. Mege, D. et al. The origin and concentration of circulating microparticles differ according to cancer type and evolution: A prospective single-center study. Int J Cancer 138, 939-948 (2016).
48. Zheng, X. et al. Sensitization of cerebral tissue in nude mice with photodynamic therapy induces ADAM17/TACE and promotes glioma cell invasion. Cancer Lett 265, 177-187 (2008).
49. Ferrario, A. et al. Antiangiogenic Treatment Enhances Photodynamic Therapy Responsiveness in a Mouse Mammary Carcinoma. Cancer Res 60, 4066-4069 (2000).
50. Ferrario, A. et al. The Matrix Metalloproteinase Inhibitor Prinomastat Enhances Photodynamic Therapy Responsiveness in a Mouse Tumor Model. Cancer Res 64, 2328-2332 (2004).
51. Camus, S. M. et al. Erythrocyte microparticles can induce kidney vaso-occlusions in a murine model of sickle cell disease. Blood 120, 5050-5058 (2012).
52. Camus, S. M. et al. Circulating cell membrane microparticles transfer heme to endothelial cells and trigger vasoocclusions in sickle cell disease. Blood 125, 3805-3814 (2015).