The limited capacity of malignant glioma-derived exosomes to suppress peripheral immune effectors

Journal of Neuroimmunology

Volumn 290, Issue , 2016, Pages 103-108

  Iorgulescu, J Bryan ^a,b   Ivan, Michael E ^a,c   Safaee, Michael ^a   Parsa, Andrew T ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Exosome; Glioma; Immunosuppression; Immunotherapy; Microvesicle

Indexed keywords

B7 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; HLA DR ANTIGEN; PROGRAMMED DEATH 1 LIGAND 1;

ANTIGEN PRESENTATION; ARTICLE; CANCER CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CYTOTOXIC T LYMPHOCYTE; EXOSOME; GLIOMA; HUMAN; HUMAN CELL; IMMUNOMODULATION; LIGAND BINDING; MONOCYTE MACROPHAGE PRECURSOR CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; T LYMPHOCYTE ACTIVATION; ASTROCYTE; CELL CULTURE; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; MONOCYTE; TUMOR CELL LINE;

ASTROCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CELLS, CULTURED; EXOSOMES; GLIOMA; HUMANS; IMMUNE TOLERANCE; MONOCYTES;

EID: 84955075165     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2015.11.025     Document Type: Article

References (43)

1. Albesiano E., Han J.E., Lim M. Mechanisms of local immunoresistance in glioma. Neurosurg. Clin. N. Am. 2010, 21:17-29.
2. Al-Nedawi K., Meehan B., Micallef J., Lhotak V., May L., Guha A., Rak J. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat. Cell Biol. 2008, 10:619-624.
3. André F., Chaput N., Schartz N.E.C., Flament C., Aubert N., Bernard J., Lemonnier F., Raposo G., Escudier B., Hsu D.-H., Tursz T., Amigorena S., Angevin E., Zitvogel L. Exosomes as potent cell-free peptide-based vaccine. I. Dendritic cell-derived exosomes transfer functional MHC class I/peptide complexes to dendritic cells. J. Immunol. 2004, 1950(172):2126-2136.
4. Bendz H., Ruhland S.C., Pandya M.J., Hainzl O., Riegelsberger S., Braüchle C., Mayer M.P., Buchner J., Issels R.D., Noessner E. Human heat shock protein 70 enhances tumor antigen presentation through complex formation and intracellular antigen delivery without innate immune signaling. J. Biol. Chem. 2007, 282:31688-31702.
5. Bloch O., Crane C.A., Kaur R., Safaee M., Rutkowski M.J., Parsa A.T. Gliomas promote immunosuppression through induction of B7-H1 expression in tumor-associated macrophages. Clin. Cancer Res. 2013, 19:3165-3175.
6. Bloch O., Crane C.A., Fuks Y., Kaur R., Aghi M.K., Berger M.S., Butowski N.A., Chang S.M., Clarke J.L., McDermott M.W., Prados M.D., Sloan A.E., Bruce J.N., Parsa A.T. Heat-shock protein peptide complex-96 vaccination for recurrent glioblastoma: a phase II, single-arm trial. Neuro-Oncology 2014, 16:274-279.
7. Bronisz A., Wang Y., Nowicki M.O., Peruzzi P., Ansari K.I., Ogawa D., Balaj L., De Rienzo G., Mineo M., Nakano I., Ostrowski M.C., Hochberg F., Weissleder R., Lawler S.E., Chiocca E.A., Godlewski J. Extracellular vesicles modulate the glioblastoma microenvironment via a tumor suppression signaling network directed by miR-1. Cancer Res. 2014, 74:738-750.
8. Bu N., Wu H., Sun B., Zhang G., Zhan S., Zhang R., Zhou L. Exosome-loaded dendritic cells elicit tumor-specific CD8+ cytotoxic T cells in patients with glioma. J. Neuro-Oncol. 2011, 104:659-667.
9. Chalmin F., Ladoire S., Mignot G., Vincent J., Bruchard M., Remy-Martin J.-P., Boireau W., Rouleau A., Simon B., Lanneau D., De Thonel A., Multhoff G., Hamman A., Martin F., Chauffert B., Solary E., Zitvogel L., Garrido C., Ryffel B., Borg C., Apetoh L., Rébé C., Ghiringhelli F. Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J. Clin. Invest. 2010, 120:457-471.
10. Chen C., Skog J., Hsu C.-H., Lessard R.T., Balaj L., Wurdinger T., Carter B.S., Breakefield X.O., Toner M., Irimia D. Microfluidic isolation and transcriptome analysis of serum microvesicles. Lab Chip 2010, 10:505-511.
11. Cho J., Lee Y.-S., Kim S.-H., Ko J.-K., Kim C.-W. MHC independent anti-tumor immune responses induced by Hsp70-enriched exosomes generate tumor regression in murine models. Cancer Lett. 2009, 275:256-265.
12. Crane C.A., Ahn B.J., Han S.J., Parsa A.T. Soluble factors secreted by glioblastoma cell lines facilitate recruitment, survival, and expansion of regulatory T cells: implications for immunotherapy. Neuro-Oncology 2012, 14:584-595.
13. Crane C.A., Han S.J., Ahn B., Oehlke J., Kivett V., Fedoroff A., Butowski N., Chang S.M., Clarke J., Berger M.S., McDermott M.W., Prados M.D., Parsa A.T. Individual patient-specific immunity against high-grade glioma after vaccination with autologous tumor derived peptides bound to the 96 KD chaperone protein. Clin. Cancer Res. 2013, 19:205-214.
14. Curran M.A., Montalvo W., Yagita H., Allison J.P. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:4275-4280.
15. Graner M.W., Cumming R.I., Bigner D.D. The heat shock response and chaperones/heat shock proteins in brain tumors: surface expression, release, and possible immune consequences. J. Neurosci. 2007, 27:11214-11227.
16. Graner M.W., Alzate O., Dechkovskaia A.M., Keene J.D., Sampson J.H., Mitchell D.A., Bigner D.D. Proteomic and immunologic analyses of brain tumor exosomes. FASEB J. 2009, 23:1541-1557.
17. Han S.J., Ahn B.J., Waldron J.S., Yang I., Fang S., Crane C.A., Pieper R.O., Parsa A.T. Gamma interferon-mediated superinduction of B7-H1 in PTEN-deficient glioblastoma: a paradoxical mechanism of immune evasion. Neuroreport 2009, 20:1597-1602.
18. Han S.J., Zygourakis C., Lim M., Parsa A.T. Immunotherapy for glioma: promises and challenges. Neurosurg. Clin. N. Am. 2012, 23:357-370.
19. Henriksen M., Johnsen K.B., Olesen P., Pilgaard L., Duroux M. MicroRNA expression signatures and their correlation with clinicopathological features in glioblastoma multiforme. Neruomol. Med. 2014, 16:565-577.
20. Kucharzewska P., Christianson H.C., Welch J.E., Svensson K.J., Fredlund E., Ringnér M., Mörgelin M., Bourseau-Guilmain E., Bengzon J., Belting M. Exosomes reflect the hypoxic status of glioma cells and mediate hypoxia-dependent activation of vascular cells during tumor development. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:7312-7317.
21. Li C.C.Y., Eaton S.A., Young P.E., Lee M., Shuttleworth R., Humphreys D.T., Grau G.E., Combes V., Bebawy M., Gong J., Brammah S., Buckland M.E., Suter C.M. Glioma microvesicles carry selectively packaged coding and non-coding RNAs which alter gene expression in recipient cells. RNA Biol. 2013, 10:1333-1344.
22. Manterola L., Guruceaga E., Gállego Pérez-Larraya J., González-Huarriz M., Jauregui P., Tejada S., Diez-Valle R., Segura V., Samprón N., Barrena C., Ruiz I., Agirre A., Ayuso A., Rodríguez J., González A., Xipell E., Matheu A., López de Munain A., Tuñón T., Zazpe I., García-Foncillas J., Paris S., Delattre J.Y., Alonso M.M. A small noncoding RNA signature found in exosomes of GBM patient serum as a diagnostic tool. Neuro-Oncology 2014, 16:520-527.
23. Mignot G., Roux S., Thery C., Ségura E., Zitvogel L. Prospects for exosomes in immunotherapy of cancer. J. Cell. Mol. Med. 2006, 10:376-388.
24. Noerholm M., Balaj L., Limperg T., Salehi A., Zhu L.D., Hochberg F.H., Breakefield X.O., Carter B.S., Skog J. RNA expression patterns in serum microvesicles from patients with glioblastoma multiforme and controls. BMC Cancer 2012, 12:22.
25. Ostrowski M., Carmo N.B., Krumeich S., Fanget I., Raposo G., Savina A., Moita C.F., Schauer K., Hume A.N., Freitas R.P., Goud B., Benaroch P., Hacohen N., Fukuda M., Desnos C., Seabra M.C., Darchen F., Amigorena S., Moita L.F., Thery C. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol. 2010, 12:19-30. (sup pp 1-13).
26. Parsa A.T., Waldron J.S., Panner A., Crane C.A., Parney I.F., Barry J.J., Cachola K.E., Murray J.C., Tihan T., Jensen M.C., Mischel P.S., Stokoe D., Pieper R.O. Loss of tumor suppressor PTEN function increases B7-H1 expression and immunoresistance in glioma. Nat. Med. 2007, 13:84-88.
27. Parsa A.T., Bloch O., Crane C., Kaur R., Safae M. Gliomas promote induction of b7-h1/pd-l1 expression on monocytes: clinical evidence of an immunosuppressive mechanism that can be targeted with antibody blockade. Neuro-Oncology 2014, 16(Suppl. 3):iii41.
28. Sayegh E.T., Oh T., Fakurnejad S., Bloch O., Parsa A.T. Vaccine Therapies for Patients with Glioblastoma 2014, J. Neurooncol.
29. Shao H., Chung J., Balaj L., Charest A., Bigner D.D., Carter B.S., Hochberg F.H., Breakefield X.O., Weissleder R., Lee H. Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy. Nat. Med. 2012, 18:1835-1840.
30. Skog J., Würdinger T., van Rijn S., Meijer D.H., Gainche L., Sena-Esteves M., Curry W.T., Carter B.S., Krichevsky A.M., Breakefield X.O. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 2008, 10:1470-1476.
31. Stupp R., Mason W.P., van den Bent M.J., Weller M., Fisher B., Taphoorn M.J.B., Belanger K., Brandes A.A., Marosi C., Bogdahn U., Curschmann J., Janzer R.C., Ludwin S.K., Gorlia T., Allgeier A., Lacombe D., Cairncross J.G., Eisenhauer E., Mirimanoff R.O., European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups, National Cancer Institute of Canada Clinical Trials Group Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 2005, 352:987-996.
32. Svensson K.J., Kucharzewska P., Christianson H.C., Sköld S., Löfstedt T., Johansson M.C., Mörgelin M., Bengzon J., Ruf W., Belting M. Hypoxia triggers a proangiogenic pathway involving cancer cell microvesicles and PAR-2-mediated heparin-binding EGF signaling in endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:13147-13152.
33. Traugott U. Multiple sclerosis: relevance of class I and class II MHC-expressing cells to lesion development. J. Neuroimmunol. 1987, 16:283-302.
34. Valenti R., Huber V., Filipazzi P., Pilla L., Sovena G., Villa A., Corbelli A., Fais S., Parmiani G., Rivoltini L. Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-beta-mediated suppressive activity on T lymphocytes. Cancer Res. 2006, 66:9290-9298.
35. Wachstein J., Tischer S., Figueiredo C., Limbourg A., Falk C., Immenschuh S., Blasczyk R., Eiz-Vesper B. HSP70 enhances immunosuppressive function of CD4(+)CD25(+)FoxP3(+) T regulatory cells and cytotoxicity in CD4(+)CD25(-) T cells. PLoS One 2012, 7.
36. Waldron J.S., Yang I., Han S., Tihan T., Sughrue M.E., Mills S.A., Pieper R.O., Parsa A.T. Implications for immunotherapy of tumor-mediated T-cell apoptosis associated with loss of the tumor suppressor PTEN in glioblastoma. J. Clin. Neurosci. 2010, 17:1543-1547.
37. Waziri A. Glioblastoma-derived mechanisms of systemic immunosuppression. Neurosurg. Clin. N. Am. 2010, 21:31-42.
38. 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.
39. Yang I., Fang S., Parsa A.T. Heat shock proteins in glioblastomas. Neurosurg. Clin. N. Am. 2010, 21:111-123.
40. Yang C., Ruffner M.A., Kim S.-H., Robbins P.D. Plasma-derived MHC class II+ exosomes from tumor-bearing mice suppress tumor antigen-specific immune responses. Eur. J. Immunol. 2012, 42:1778-1784.
41. Zhang H.-G., Grizzle W.E. Exosomes and cancer: a newly described pathway of immune suppression. Clin. Cancer Res. 2011, 17:959-964.
42. Zhang H., Hu H., Jiang X., He H., Cui L., He W. Membrane HSP70: the molecule triggering gammadelta T cells in the early stage of tumorigenesis. Immunol. Investig. 2005, 34:453-468.
43. Zou J.P., Morford L.A., Chougnet C., Dix A.R., Brooks A.G., Torres N., Shuman J.D., Coligan J.E., Brooks W.H., Roszman T.L., Shearer G.M. Human glioma-induced immunosuppression involves soluble factor(s) that alters monocyte cytokine profile and surface markers. J. Immunol. 1999, 1950(162):4882-4892.