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Current Topics in Medicinal Chemistry

Author(s): Rashmi Rana*, Shikha Joon, Kirti Chauhan, Vaishnavi Rathi, Nirmal Kumar Ganguly, Chandni Kumari and Dharmendra Kumar Yadav*

DOI: 10.2174/1568026620666201207100139

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Role of Extracellular Vesicles in Glioma Progression: Deciphering Cellular Biological Processes to Clinical Applications

Page: [696 - 704] Pages: 9

  • * (Excluding Mailing and Handling)

Abstract

Glioma predominantly targets glial cells in the brain and spinal cord. There are grade I, II, III, and IV gliomas with anaplastic astrocytoma and glioblastoma multiforme as the most severe forms of the disease. Current diagnostic methods are limited in their data acquisition and interpretation, markedly affecting treatment modalities, and patient outcomes. Circulating extracellular vesicles (EVs) or “magic bullets” contain bioactive signature molecules such as DNA, RNA, proteins, lipids, and metabolites. These secretory “smart probes” participate in myriad cellular activities, including glioma progression. EVs are released by all cell populations and may serve as novel diagnostic biomarkers and efficient nano-vehicles in the targeted delivery of encapsulated therapeutics. The present review describes the potential of EV-based biomarkers for glioma management.

Keywords: Biomarker, Diagnostic, Extracellular vesicle, Glioma, Therapeutic, Smart probes.

Graphical Abstract

[1]
Merchant, T.E.; Pollack, I.F.; Loeffler, J.S. Brain tumors across the age spectrum: biology, therapy, and late effects. Semin. Radiat. Oncol., 2010, 20(1), 58-66.
[http://dx.doi.org/10.1016/j.semradonc.2009.09.005] [PMID: 19959032]
[2]
Dasgupta, A.; Gupta, T.; Jalali, R. Indian data on central nervous tumors: A summary of published work. South Asian J. Cancer, 2016, 5(3), 147-153.
[http://dx.doi.org/10.4103/2278-330X.187589] [PMID: 27606302]
[3]
Wilhelm, I.; Molnár, J.; Fazakas, C.; Haskó, J.; Krizbai, I.A. Role of the blood-brain barrier in the formation of brain metastases. Int. J. Mol. Sci., 2013, 14(1), 1383-1411.
[http://dx.doi.org/10.3390/ijms14011383] [PMID: 23344048]
[4]
Goodenberger, M.L.; Jenkins, R.B. Genetics of adult glioma. Cancer Genet., 2012, 205(12), 613-621.
[http://dx.doi.org/10.1016/j.cancergen.2012.10.009] [PMID: 23238284]
[5]
Perry, A.; Wesseling, P. Histologic classification of gliomas. Handb. Clin. Neurol., 2016, 134, 71-95.
[http://dx.doi.org/10.1016/B978-0-12-802997-8.00005-0] [PMID: 26948349]
[6]
Forst, D.A.; Nahed, B.V.; Loeffler, J.S.; Batchelor, T.T. Low-grade gliomas. Oncologist, 2014, 19(4), 403-413.
[http://dx.doi.org/10.1634/theoncologist.2013-0345] [PMID: 24664484]
[7]
Ellor, S.V.; Pagano-Young, T.A.; Avgeropoulos, N.G. Glioblastoma: background, standard treatment paradigm, and supportive care considerations. NG J Law Med Ethics, 2014, 42, 17-82.
[http://dx.doi.org/10.1111/jlme.12133]
[8]
Hochberg, F.H.; Atai, N.A.; Gonda, D.; Hughes, M.S.; Mawejje, B.; Balaj, L.; Carter, R.S. Glioma diagnostics and biomarkers: an ongoing challenge in the field of medicine and science. Expert Rev. Mol. Diagn., 2014, 14(4), 439-452.
[http://dx.doi.org/10.1586/14737159.2014.905202] [PMID: 24746164]
[9]
Walbert, T.; Mikkelsen, T. Recurrent high-grade glioma: a diagnostic and therapeutic challenge. Expert Rev. Neurother., 2011, 11(4), 509-518.
[http://dx.doi.org/10.1586/ern.11.37] [PMID: 21469924]
[10]
Mrugala, M.M. Advances and challenges in the treatment of glioblastoma: a clinician’s perspective. Discov. Med., 2013, 15(83), 221-230.
[PMID: 23636139]
[11]
Young, R.M.; Jamshidi, A.; Davis, G.; Sherman, J.H. Current trends in the surgical management and treatment of adult glioblastoma. Ann. Transl. Med., 2015, 3(9), 121.
[PMID: 26207249]
[12]
Rahman, M.; Abbatematteo, J.; De Leo, E.K.; Kubilis, P.S.; Vaziri, S.; Bova, F.; Sayour, E.; Mitchell, D.; Quinones-Hinojosa, A. The effects of new or worsened postoperative neurological deficits on survival of patients with glioblastoma. J. Neurosurg., 2017, 127(1), 123-131.
[http://dx.doi.org/10.3171/2016.7.JNS16396] [PMID: 27689459]
[13]
Seyfried, T.N.; Huysentruyt, L.C. On the origin of cancer metastasis. Crit. Rev. Oncog., 2013, 18(1-2), 43-73.
[http://dx.doi.org/10.1615/CritRevOncog.v18.i1-2.40] [PMID: 23237552]
[14]
Berger, M.S.; Bruce, J.N.; Chen, T.C.; Zadeh, G. Introduction: Glioblastoma: an update on pathophysiology and management strategies. Neurosurg. Focus, 2014, 37(6)
[http://dx.doi.org/10.3171/2014.9.FOCUS14677] [PMID: 25434392]
[15]
Lane, R.E.; Korbie, D.; Hill, M.M.; Trau, M. Extracellular vesicles as circulating cancer biomarkers: opportunities and challenges. Clin. Transl. Med., 2018, 7(1), 14.
[http://dx.doi.org/10.1186/s40169-018-0192-7] [PMID: 29855735]
[16]
Cufaro, M.C.; Pieragostino, D.; Lanuti, P.; Rossi, C.; Cicalini, I.; Federici, L.; De Laurenzi, V.; Del Boccio, P. Extracellular vesicles and their potential use in monitoring cancer progression and therapy: the contribution of proteomics. J. Oncol., 2019, 2019, 1639854.
[http://dx.doi.org/10.1155/2019/1639854] [PMID: 31281356]
[17]
Abels, E.R.; Breakefield, X.O. Introduction to extracellular vesicles: biogenesis, rna cargo selection, content, release, and uptake. Cell. Mol. Neurobiol., 2016, 36(3), 301-312.
[http://dx.doi.org/10.1007/s10571-016-0366-z] [PMID: 27053351]
[18]
Zaborowski, M.P.; Balaj, L.; Breakefield, X.O.; Lai, C.P. Extracellular vesicles: composition, biological relevance, and methods of study. Bioscience, 2015, 65(8), 783-797.
[http://dx.doi.org/10.1093/biosci/biv084] [PMID: 26955082]
[19]
Crenshaw, B.J.; Gu, L.; Sims, B.; Matthews, Q.L. Exosome biogenesis and biological function in response to viral infections. Open Virol. J., 2018, 12, 134-148.
[http://dx.doi.org/10.2174/1874357901812010134] [PMID: 30416610]
[20]
Maas, S.L.N.; Breakefield, X.O.; Weaver, A.M. Extracellular vesicles: unique intercellular delivery vehicles. Trends Cell Biol., 2017, 27(3), 172-188.
[http://dx.doi.org/10.1016/j.tcb.2016.11.003] [PMID: 27979573]
[21]
Raimondo, S.; Giavaresi, G.; Lorico, A.; Alessandro, R. Extracellular vesicles as biological shuttles for targeted therapies. Int. J. Mol. Sci., 2019, 20(8), 1-18.
[http://dx.doi.org/10.3390/ijms20081848] [PMID: 30991632]
[22]
Becker, A.; Thakur, B.K.; Weiss, J.M.; Kim, H.S.; Peinado, H.; Lyden, D. Extracellular vesicles in cancer: cell-to-cell mediators of metastasis. Cancer Cell, 2016, 30(6), 836-848.
[http://dx.doi.org/10.1016/j.ccell.2016.10.009] [PMID: 27960084]
[23]
Maacha, S.; Bhat, A.A.; Jimenez, L.; Raza, A.; Haris, M.; Uddin, S.; Grivel, J.C. Extracellular vesicles-mediated intercellular communication: roles in the tumor microenvironment and anti-cancer drug resistance. Mol. Cancer, 2019, 18(1), 55.
[http://dx.doi.org/10.1186/s12943-019-0965-7] [PMID: 30925923]
[24]
You, B.; Xu, W.; Zhang, B. Engineering exosomes: a new direction for anticancer treatment. Am. J. Cancer Res., 2018, 8(8), 1332-1342.
[PMID: 30210908]
[25]
Chandana, S.R.; Movva, S.; Arora, M.; Singh, T. Primary brain tumors in adults. Am. Fam. Physician, 2008, 77(10), 1423-1430.
[PMID: 18533376]
[26]
Preston-Martin, S.; Pogoda, J.M.; Schlehofer, B.; Blettner, M.; Howe, G.R.; Ryan, P.; Menegoz, F.; Giles, G.G.; Rodvall, Y.; Choi, N.W.; Little, J.; Arslan, A. An international case-control study of adult glioma and meningioma: the role of head trauma. Int. J. Epidemiol., 1998, 27(4), 579-586.
[http://dx.doi.org/10.1093/ije/27.4.579] [PMID: 9758110]
[27]
Magnavita, N.; Placentino, R.A.; Mei, D.; Ferraro, D.; Di Trapani, G. Occupational head injury and subsequent glioma. Neurol. Sci., 2003, 24(1), 31-33.
[http://dx.doi.org/10.1007/s100720300018] [PMID: 12754654]
[28]
Ferlay, J.; Soerjomataram, I.; Dikshit, R.; Eser, S.; Mathers, C.; Rebelo, M.; Parkin, D.M.; Forman, D.; Bray, F. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer, 2015, 136(5), E359-E386.
[http://dx.doi.org/10.1002/ijc.29210] [PMID: 25220842]
[29]
Nelson, J.S.; Burchfiel, C.M.; Fekedulegn, D.; Andrew, M.E. Potential risk factors for incident glioblastoma multiforme: the honolulu heart program and honolulu-asia aging study. J. Neurooncol., 2012, 109(2), 315-321.
[http://dx.doi.org/10.1007/s11060-012-0895-3] [PMID: 22588335]
[30]
Adamson, C.; Kanu, O.O.; Mehta, A.I.; Di, C.; Lin, N.; Mattox, A.K.; Bigner, D.D. Glioblastoma multiforme: a review of where we have been and where we are going. Expert Opin. Investig. Drugs, 2009, 18(8), 1061-1083.
[http://dx.doi.org/10.1517/13543780903052764] [PMID: 19555299]
[31]
Singh, D.; Chan, J.M.; Zoppoli, P.; Niola, F.; Sullivan, R.; Castano, A.; Liu, E.M.; Reichel, J.; Porrati, P.; Pellegatta, S.; Qiu, K.; Gao, Z.; Ceccarelli, M.; Riccardi, R.; Brat, D.J.; Guha, A.; Aldape, K.; Golfinos, J.G.; Zagzag, D.; Mikkelsen, T.; Finocchiaro, G.; Lasorella, A.; Rabadan, R.; Iavarone, A. Transforming fusions of FGFR and TACC genes in human glioblastoma. Science, 2012, 337(6099), 1231-1235.
[http://dx.doi.org/10.1126/science.1220834] [PMID: 22837387]
[32]
Ostrom, Q.T.; Cote, D.J.; Ascha, M.; Kruchko, C.; Barnholtz-Sloan, J.S. Adult glioma incidence and survival by race or ethnicity in the United States from 2000 to 2014. JAMA Oncol., 2018, 4(9), 1254-1262.
[http://dx.doi.org/10.1001/jamaoncol.2018.1789] [PMID: 29931168]
[33]
Lee, S.C. Diffuse gliomas for nonneuropathologists: The new integrated molecular diagnostics. Arch. Pathol. Lab. Med., 2018, 142(7), 804-814.
[http://dx.doi.org/10.5858/arpa.2017-0449-RA] [PMID: 29775073]
[34]
Wong, T.T.; Chen, H.H.; Liang, M.L.; Hsieh, K.L.; Yang, Y.S.; Ho, D.M.; Chang, K.P.; Lee, Y.Y.; Lin, S.C.; Hsu, T.R.; Chen, Y.W.; Yen, S.H.; Chang, F.C.; Guo, W.Y.; Chen, K.W.; Kwang, W.K.; Hou, W.Y.; Wang, C.Y. Clinical considerations and surgical approaches for low-grade gliomas in deep hemispheric locations: thalamic lesions. Childs Nerv. Syst., 2016, 32(10), 1895-1906.
[http://dx.doi.org/10.1007/s00381-016-3148-5] [PMID: 27659831]
[35]
Wu, A.; Weingart, J.D.; Gallia, G.L.; Lim, M.; Brem, H.; Bettegowda, C.; Chaichana, K.L. Risk factors for preoperative seizures and loss of seizure control in patients undergoing surgery for metastatic brain tumors. World Neurosurg., 2017, 104, 120-128.
[http://dx.doi.org/10.1016/j.wneu.2017.05.028] [PMID: 28512046]
[36]
Louis, D.N.; Perry, A.; Reifenberger, G.; von Deimling, A.; Figarella-Branger, D.; Cavenee, W.K.; Ohgaki, H.; Wiestler, O.D.; Kleihues, P.; Ellison, D.W. The 2016 World health organization classification of tumors of the central nervous system: a summary. Acta Neuropathol., 2016, 131(6), 803-820.
[http://dx.doi.org/10.1007/s00401-016-1545-1] [PMID: 27157931]
[37]
Laws, E.R., Jr; Penn, D.L.; Repetti, C.S. Advances and controversies in the classification and grading of pituitary tumors. J. Endocrinol. Invest., 2019, 42(2), 129-135.
[http://dx.doi.org/10.1007/s40618-018-0901-5] [PMID: 29858984]
[38]
Komori, T. The 2016 WHO classification of tumours of the central nervous system: the major points of revision. Neurol. Med. Chir. (Tokyo), 2017, 57(7), 301-311.
[http://dx.doi.org/10.2176/nmc.ra.2017-0010] [PMID: 28592714]
[39]
Citak-Er, F.; Firat, Z.; Kovanlikaya, I.; Ture, U.; Ozturk-Isik, E. Jain, K.K. A critical overview of targeted therapies for glioblastoma. Front. Oncol., 2018, 8, 1-19.
[40]
Ostrom, Q.T.; Gittleman, H.; Liao, P.; Vecchione-Koval, T.; Wolinsky, Y.; Kruchko, C.; Barnholtz-Sloan, J.S. CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2010-2014. Neuro-oncol., 2017. 19(suppl_5), v1-v88.
[http://dx.doi.org/10.1093/neuonc/nox158] [PMID: 29117289]
[41]
Hanif, F.; Muzaffar, K.; Perveen, K.; Malhi, S.M.; Simjee, ShU. Glioblastoma multiforme: a review of its epidemiology and pathogenesis through clinical presentation and treatment. Asian Pac. J. Cancer Prev., 2017, 18(1), 3-9.
[PMID: 28239999]
[42]
Dolecek, T.A.; Propp, J.M.; Stroup, N.E.; Kruchko, C. CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2005-2009. Neuro-oncol., 2012, 14(Suppl. 5), v1-v49.
[http://dx.doi.org/10.1093/neuonc/nos218] [PMID: 23095881]
[43]
McCarthy, B.J.; Rankin, K.M.; Aldape, K.; Bondy, M.L.; Brännström, T.; Broholm, H.; Feychting, M.; Il’yasova, D.; Inskip, P.D.; Johansen, C.; Melin, B.S.; Ruder, A.M.; Butler, M.A.; Scheurer, M.E.; Schüz, J.; Schwartzbaum, J.A.; Wrensch, M.R.; Davis, F.G. Risk factors for oligodendroglial tumors: a pooled international study. Neuro-oncol., 2011, 13(2), 242-250.
[http://dx.doi.org/10.1093/neuonc/noq173] [PMID: 21149253]
[44]
Ohgaki, H.; Kleihues, P. Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas. J. Neuropathol. Exp. Neurol., 2005, 64(6), 479-489.
[http://dx.doi.org/10.1093/jnen/64.6.479] [PMID: 15977639]
[45]
Huang, Y. Subependymoma with extensive microcystic transformation: a case report. Int. J. Clin. Exp. Pathol., 2015, 8(2), 2191-2194.
[PMID: 25973126]
[46]
Weber, D.C.; Wang, Y.; Miller, R.; Villà, S.; Zaucha, R.; Pica, A.; Poortmans, P.; Anacak, Y.; Ozygit, G.; Baumert, B.; Haller, G.; Preusser, M.; Li, J. Long-term outcome of patients with spinal myxopapillary ependymoma: treatment results from the MD Anderson Cancer Center and institutions from the Rare Cancer Network. Neuro-oncol., 2015, 17(4), 588-595.
[http://dx.doi.org/10.1093/neuonc/nou293] [PMID: 25301811]
[47]
Grier, J.T.; Batchelor, T. Low-grade gliomas in adults. Oncologist, 2006, 11(6), 681-693.
[http://dx.doi.org/10.1634/theoncologist.11-6-681] [PMID: 16794247]
[48]
Sarıkafa, Ş.; Çelik, S.E.; Yarikkaya, E.; Sayılgan, A. Malignant transformation of grade ii ependymoma in a 2-year-old child: case report. J. Neurol. Surg. Rep., 2015, 76(1), e151-e155.
[http://dx.doi.org/10.1055/s-0035-1549311] [PMID: 26251794]
[49]
Taylor, L.P. Diagnosis, treatment, and prognosis of glioma: five new things. Neurology, 2010, 75(18)(Suppl. 1), S28-S32.
[http://dx.doi.org/10.1212/WNL.0b013e3181fb3661] [PMID: 21041768]
[50]
Walid, M.S. Prognostic factors for long-term survival after glioblastoma. Perm. J., 2008, 12(4), 45-48.
[http://dx.doi.org/10.7812/TPP/08-027] [PMID: 21339920]
[51]
Kumar, N.; Kumar, P.; Angurana, S.L.; Khosla, D.; Mukherjee, K.K.; Aggarwal, R.; Kumar, R.; Bera, A.; Sharma, S.C. Evaluation of outcome and prognostic factors in patients of glioblastoma multiforme: A single institution experience. J. Neurosci. Rural Pract., 2013, 4(Suppl. 1), S46-S55.
[http://dx.doi.org/10.4103/0976-3147.116455] [PMID: 24174800]
[52]
Neill, E.; Luks, T.; Dayal, M.; Phillips, J.J.; Perry, A.; Jalbert, L.E.; Cha, S.; Molinaro, A.; Chang, S.M.; Nelson, S.J. Quantitative multi-modal MR imaging as a non-invasive prognostic tool for patients with recurrent low-grade glioma. J. Neurooncol., 2017, 132(1), 171-179.
[http://dx.doi.org/10.1007/s11060-016-2355-y] [PMID: 28124178]
[53]
Yang, I.; Liau, L.M. american association for cancer research genetics and biology of brain cancers 2009, december 13-15, 2009, San Diego, CA. J. Neurooncol., 2010, 99(2), 297-306.
[http://dx.doi.org/10.1007/s11060-010-0332-4] [PMID: 20714783]
[54]
Yin, A.A.; Zhang, L.H.; Cheng, J.X.; Dong, Y.; Liu, B.L.; Han, N.; Zhang, X. The predictive but not prognostic value of MGMT promoter methylation status in elderly glioblastoma patients: a meta-analysis. PLoS One, 2014, 9(1), e85102.
[http://dx.doi.org/10.1371/journal.pone.0085102] [PMID: 24454798]
[55]
Perazzoli, G.; Prados, J.; Ortiz, R.; Caba, O.; Cabeza, L.; Berdasco, M.; Gónzalez, B.; Melguizo, C. Temozolomide resistance in glioblastoma cell lines: implication of mgmt, mmr, p-glycoprotein and cd133 expression. PLoS One, 2015, 10, 1-23.
[http://dx.doi.org/10.1371/journal.pone.0140131]
[56]
Franceschi, S.; Mazzanti, C.M.; Lessi, F.; Aretini, P.; Carbone, F.G. LA Ferla, M.; Scatena, C.; Ortenzi, V.; Vannozzi, R.; Fanelli, G.; Pasqualetti, F.; Bevilacqua, G.; Zavaglia, K.; Naccarato, A.G. Investigating molecular alterations to profile short- and long-term recurrence-free survival in patients with primary glioblastoma. Oncol. Lett., 2015, 10(6), 3599-3606.
[http://dx.doi.org/10.3892/ol.2015.3738] [PMID: 26788176]
[57]
Grossman, R.; Burger, P.; Soudry, E.; Tyler, B.; Chaichana, K.L.; Weingart, J.; Olivi, A.; Gallia, G.L.; Sidransky, D.; Quiñones-Hinojosa, A.; Ye, X.; Brem, H. MGMT inactivation and clinical response in newly diagnosed GBM patients treated with Gliadel. J. Clin. Neurosci., 2015, 22(12), 1938-1942.
[http://dx.doi.org/10.1016/j.jocn.2015.07.003] [PMID: 26249244]
[58]
Weller, M.; Tabatabai, G.; Kästner, B.; Felsberg, J.; Steinbach, J.P.; Wick, A.; Schnell, O.; Hau, P.; Herrlinger, U.; Sabel, M.C.; Wirsching, H.G.; Ketter, R.; Bähr, O.; Platten, M.; Tonn, J.C.; Schlegel, U.; Marosi, C.; Goldbrunner, R.; Stupp, R.; Homicsko, K.; Pichler, J.; Nikkhah, G.; Meixensberger, J.; Vajkoczy, P.; Kollias, S.; Hüsing, J.; Reifenberger, G.; Wick, W. DIRECTOR Study Group. MGMT promoter methylation is a strong prognostic biomarker for benefit from dose-intensified temozolomide rechallenge in progressive glioblastoma: the director trial. Clin. Cancer Res., 2015, 21(9), 2057-2064.
[http://dx.doi.org/10.1158/1078-0432.CCR-14-2737] [PMID: 25655102]
[59]
Beiko, J.; Suki, D.; Hess, K.R.; Fox, B.D.; Cheung, V.; Cabral, M.; Shonka, N.; Gilbert, M.R.; Sawaya, R.; Prabhu, S.S.; Weinberg, J.; Lang, F.F.; Aldape, K.D.; Sulman, E.P.; Rao, G.; McCutcheon, I.E.; Cahill, D.P. IDH1 mutant malignant astrocytomas are more amenable to surgical resection and have a survival benefit associated with maximal surgical resection. Neuro-oncol., 2014, 16(1), 81-91.
[http://dx.doi.org/10.1093/neuonc/not159] [PMID: 24305719]
[60]
Chesnelong, C.; Chaumeil, M.M.; Blough, M.D.; Al-Najjar, M.; Stechishin, O.D.; Chan, J.A.; Pieper, R.O.; Ronen, S.M.; Weiss, S.; Luchman, H.A.; Cairncross, J.G. Lactate dehydrogenase A silencing in IDH mutant gliomas. Neuro-oncol., 2014, 16(5), 686-695.
[http://dx.doi.org/10.1093/neuonc/not243] [PMID: 24366912]
[61]
Sabha, N.; Knobbe, C.B.; Maganti, M.; Al Omar, S.; Bernstein, M.; Cairns, R.; Çako, B.; von Deimling, A.; Capper, D.; Mak, T.W.; Kiehl, T.R.; Carvalho, P.; Garrett, E.; Perry, A.; Zadeh, G.; Guha, A. Sidney Croul, Analysis of IDH mutation, 1p/19q deletion, and PTEN loss delineates prognosis in clinical low-grade diffuse gliomas. Neuro-oncol., 2014, 16(7), 914-923.
[http://dx.doi.org/10.1093/neuonc/not299] [PMID: 24470545]
[62]
Mur, P.; Mollejo, M.; Hernández-Iglesias, T.; de Lope, Á.R.; Castresana, J.S.; García, J.F.; Fiaño, C.; Ribalta, T.; Rey, J.A.; Meléndez, B. Molecular classification defines 4 prognostically distinct glioma groups irrespective of diagnosis and grade. J. Neuropathol. Exp. Neurol., 2015, 74(3), 241-249.
[http://dx.doi.org/10.1097/NEN.0000000000000167] [PMID: 25668564]
[63]
Cairncross, J.G.; Wang, M.; Jenkins, R.B.; Shaw, E.G.; Giannini, C.; Brachman, D.G.; Buckner, J.C.; Fink, K.L.; Souhami, L.; Laperriere, N.J.; Huse, J.T.; Mehta, M.P.; Curran, W.J., Jr Benefit from procarbazine, lomustine, and vincristine in oligodendroglial tumors is associated with mutation of IDH. J. Clin. Oncol., 2014, 32(8), 783-790.
[http://dx.doi.org/10.1200/JCO.2013.49.3726] [PMID: 24516018]
[64]
Minniti, G.; Scaringi, C.; Arcella, A.; Lanzetta, G.; Di Stefano, D.; Scarpino, S.; Bozzao, A.; Pace, A.; Villani, V.; Salvati, M.; Esposito, V.; Giangaspero, F.; Enrici, R.M. IDH1 mutation and MGMT methylation status predict survival in patients with anaplastic astrocytoma treated with temozolomide-based chemoradiotherapy. J. Neurooncol., 2014, 118(2), 377-383.
[http://dx.doi.org/10.1007/s11060-014-1443-0] [PMID: 24748470]
[65]
Li, H.; Li, J.; Cheng, G.; Zhang, J.; Li, X. IDH mutation and MGMT promoter methylation are associated with the pseudoprogression and improved prognosis of glioblastoma multiforme patients who have undergone concurrent and adjuvant temozolomide-based chemoradiotherapy. Clin. Neurol. Neurosurg., 2016, 151, 31-36.
[http://dx.doi.org/10.1016/j.clineuro.2016.10.004] [PMID: 27764705]
[66]
Barbagallo, G.M.V.; Morrone, A.; Certo, F. Intraoperative CT and awake craniotomy: a useful and safe combination in brain surgery. World Neurosurg., 2018, 119, 159-166.
[http://dx.doi.org/10.1016/j.wneu.2018.07.078]
[67]
Ahmed, R.; Oborski, M.J.; Hwang, M.; Lieberman, F.S.; Mountz, J.M. Malignant gliomas: current perspectives in diagnosis, treatment, and early response assessment using advanced quantitative imaging methods. Cancer Manag. Res., 2014, 6, 149-170.
[PMID: 24711712]
[68]
Ghazanwy, M.; Chakrabarti, R.; Tewari, A.; Sinha, A. Awake craniotomy: A qualitative review and future challenges. Saudi J. Anaesth., 2014, 8(4), 529-539.
[http://dx.doi.org/10.4103/1658-354X.140890] [PMID: 25422613]
[69]
Parney, I.F.; Goerss, S.J.; McGee, K.; Huston, J., III; Perkins, W.J.; Meyer, F.B. Awake craniotomy, electrophysiologic mapping, and tumor resection with high-field intraoperative MRI. World Neurosurg., 2010, 73(5), 547-551.
[http://dx.doi.org/10.1016/j.wneu.2010.02.003] [PMID: 20920940]
[70]
Batash, R.; Asna, N.; Schaffer, P.; Francis, N.; Schaffer, M. Glioblastoma multiforme, diagnosis and treatment; recent literature review. Curr. Med. Chem., 2017, 24(27), 3002-3009.
[http://dx.doi.org/10.2174/0929867324666170516123206] [PMID: 28521700]
[71]
Alifieris, C.; Trafalis, D.T. Glioblastoma multiforme: Pathogenesis and treatment. Pharmacol. Ther., 2015, 152, 63-82.
[http://dx.doi.org/10.1016/j.pharmthera.2015.05.005] [PMID: 25944528]
[72]
Fine, H.A.; Dear, K.B.; Loeffler, J.S.; Black, P.M.; Canellos, G.P. Meta-analysis of radiation therapy with and without adjuvant chemotherapy for malignant gliomas in adults. Cancer, 1993, 71(8), 2585-2597.
[http://dx.doi.org/10.1002/1097-0142(19930415)71:8<2585:AID-CNCR2820710825>3.0.CO;2-S] [PMID: 8453582]
[73]
Salazar, A.M.; Levy, H.B.; Ondra, S.; Kende, M.; Scherokman, B.; Brown, D.; Mena, H.; Martin, N.; Schwab, K.; Donovan, D.; Dougherty, D.; Pulliam, M.; Ippolito, M.; Graves, M.; Brown, H.; Ommaya, A. Long-term treatment of malignant gliomas with intramuscularly administered polyinosinic-polycytidylic acid stabilized with polylysine and carboxymethylcellulose: an open pilot study. Neurosurgery, 1996, 38(6), 1096-1103.
[http://dx.doi.org/10.1227/00006123-199606000-00006] [PMID: 8727138]
[74]
Shih, H.A.; Sherman, J.C.; Nachtigall, L.B.; Colvin, M.K.; Fullerton, B.C.; Daartz, J.; Winrich, B.K.; Batchelor, T.T.; Thornton, L.T.; Mancuso, S.M.; Saums, M.K.; Oh, K.S.; Curry, W.T.; Loeffler, J.S.; Yeap, B.Y. Proton therapy for low-grade gliomas: Results from a prospective trial. Cancer, 2015, 121(10), 1712-1719.
[http://dx.doi.org/10.1002/cncr.29237] [PMID: 25585890]
[75]
Robert Lee, W. Practical radiation oncology (PRO). Pract. Radiat. Oncol., 2014, 4(4), 207.
[http://dx.doi.org/10.1016/j.prro.2014.05.001] [PMID: 25012826]
[76]
Park, J.; Park, Y.; Lee, S.U.; Kim, T.; Choi, Y.K.; Kim, J.Y. Differential dosimetric benefit of proton beam therapy over intensity modulated radiotherapy for a variety of targets in patients with intracranial germ cell tumors. Radiat. Oncol., 2015, 10, 135.
[http://dx.doi.org/10.1186/s13014-015-0441-5] [PMID: 26112360]
[77]
Yung, W.K.; Albright, R.E.; Olson, J.; Fredericks, R.; Fink, K.; Prados, M.D.; Brada, M.; Spence, A.; Hohl, R.J.; Shapiro, W.; Glantz, M.; Greenberg, H.; Selker, R.G.; Vick, N.A.; Rampling, R.; Friedman, H.; Phillips, P.; Bruner, J.; Yue, N.; Osoba, D.; Zaknoen, S.; Levin, V.A. A phase II study of temozolomide vs. procarbazine in patients with glioblastoma multiforme at first relapse. Br. J. Cancer, 2000, 83(5), 588-593.
[http://dx.doi.org/10.1054/bjoc.2000.1316] [PMID: 10944597]
[78]
Solimando, D.A., Jr; Waddell, J.A. Procarbazine, lomustine, and vincristine (pcv) regimen for central nervous system tumors. Hosp. Pharm., 2017, 52(2), 98-104.
[http://dx.doi.org/10.1310/hpj5202-98] [PMID: 28321136]
[79]
Taal, W.; Bromberg, J.E.C.; van den Bent, M.J. Chemotherapy in glioma. CNS Oncol., 2015, 4(3), 179-192.
[http://dx.doi.org/10.2217/cns.15.2] [PMID: 25906059]
[80]
Lynes, J.; Sanchez, V.; Dominah, G.; Nwankwo, A.; Nduom, E. Current options and future directions in immune therapy for glioblastoma. Front. Oncol., 2018, 8, 578.
[http://dx.doi.org/10.3389/fonc.2018.00578] [PMID: 30568917]
[81]
Mahmoodi Chalbatani, G.; Dana, H.; Gharagouzloo, E.; Grijalvo, S.; Eritja, R.; Logsdon, C.D.; Memari, F.; Miri, S.R.; Rad, M.R.; Marmari, V. Small interfering RNAs (siRNAs) in cancer therapy: a nano-based approach. Int. J. Nanomedicine, 2019, 14, 3111-3128.
[http://dx.doi.org/10.2147/IJN.S200253] [PMID: 31118626]
[82]
Riley, R.S.; June, C.H.; Langer, R.; Mitchell, M.J. Delivery technologies for cancer immunotherapy. Nat. Rev. Drug Discov., 2019, 18(3), 175-196.
[http://dx.doi.org/10.1038/s41573-018-0006-z] [PMID: 30622344]
[83]
Yáñez-Mó, M.; Siljander, P.R.; Andreu, Z.; Zavec, A.B.; Borràs, F.E.; Buzas, E.I.; Buzas, K.; Casal, E.; Cappello, F.; Carvalho, J.; Colás, E.; Cordeiro-da, S.A.; Fais, S.; Falcon-Perez, J.M.; Ghobrial, I.M.; Giebel, B.; Gimona, M.; Graner, M.; Gursel, I.; Gursel, M.; Heegaard, N.H.; Hendrix, A.; Kierulf, P.; Kokubun, K.; Kosanovic, M.; Kralj-Iglic, V.; Krämer-Albers, E.M.; Laitinen, S.; Lässer, C.; Lener, T.; Ligeti, E.; Linē, A.; Lipps, G.; Llorente, A.; Lötvall, J.; Manček-Keber, M.; Marcilla, A.; Mittelbrunn, M.; Nazarenko, I.; Nolte-’t Hoen, E.N.; Nyman, T.A.; O’Driscoll, L. 4.; Olivan, M.; Oliveira, C.; Pállinger, É.; Del Portillo, H.A.; Reventós, J., Rigau, M.; Rohde, E.; Sammar, M.; Sánchez-Madrid, F.; Santarém, N.; Schallmoser, K.; Ostenfeld, M.S.; Stoorvogel, W.; Stukelj, R.; Van der Grein, S.G.; Vasconcelos, M.H.; Wauben, M.H.; De Wever, O. Biological properties of extracellular vesicles and their physiological functions. J. Extracell. Vesicles, 2015, 4, 1-60.
[84]
Kahlert, C.; Melo, S.A.; Protopopov, A.; Tang, J.; Seth, S.; Koch, M.; Zhang, J.; Weitz, J.; Chin, L.; Futreal, A.; Kalluri, R. Identification of double-stranded genomic DNA spanning all chromosomes with mutated KRAS and p53 DNA in the serum exosomes of patients with pancreatic cancer. J. Biol. Chem., 2014, 289(7), 3869-3875.
[http://dx.doi.org/10.1074/jbc.C113.532267] [PMID: 24398677]
[85]
Lo Cicero, A.; Stahl, P.D.; Raposo, G. Extracellular vesicles shuffling intercellular messages: for good or for bad. Curr. Opin. Cell Biol., 2015, 35, 69-77.
[http://dx.doi.org/10.1016/j.ceb.2015.04.013] [PMID: 26001269]
[86]
Trams, E.G.; Lauter, C.J.; Salem, N., Jr; Heine, U. Exfoliation of membrane ecto-enzymes in the form of micro-vesicles. Biochim. Biophys. Acta, 1981, 645(1), 63-70.
[http://dx.doi.org/10.1016/0005-2736(81)90512-5] [PMID: 6266476]
[87]
Keller, S.; Sanderson, M.P.; Stoeck, A.; Altevogt, P. Exosomes: from biogenesis and secretion to biological function. Immunol. Lett., 2006, 107(2), 102-108.
[http://dx.doi.org/10.1016/j.imlet.2006.09.005] [PMID: 17067686]
[88]
Bianco, F.; Perrotta, C.; Novellino, L.; Francolini, M.; Riganti, L.; Menna, E.; Saglietti, L.; Schuchman, E.H.; Furlan, R.; Clementi, E.; Matteoli, M.; Verderio, C. Acid sphingomyelinase activity triggers microparticle release from glial cells. EMBO J., 2009, 28(8), 1043-1054.
[http://dx.doi.org/10.1038/emboj.2009.45] [PMID: 19300439]
[89]
Elia, I.; Doglioni, G.; Fendt, S.M. Metabolic hallmarks of metastasis formation. Trends Cell Biol., 2018, 28(8), 673-684.
[http://dx.doi.org/10.1016/j.tcb.2018.04.002] [PMID: 29747903]
[90]
Raposo, G.; Stoorvogel, W. Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell Biol., 2013, 200(4), 373-383.
[http://dx.doi.org/10.1083/jcb.201211138] [PMID: 23420871]
[91]
Joyce, J.A.; Pollard, J.W. Microenvironmental regulation of metastasis. Nat. Rev. Cancer, 2009, 9(4), 239-252.
[http://dx.doi.org/10.1038/nrc2618] [PMID: 19279573]
[92]
Webber, J.; Steadman, R.; Mason, M.D.; Tabi, Z.; Clayton, A. Cancer exosomes trigger fibroblast to myofibroblast differentiation. Cancer Res., 2010, 70(23), 9621-9630.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-1722] [PMID: 21098712]
[93]
Lee, Y.; El Andaloussi, S.; Wood, M.J. Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy. Hum. Mol. Genet., 2012, 21(R1), R125-R134.
[http://dx.doi.org/10.1093/hmg/dds317] [PMID: 22872698]
[94]
EL Andaloussi, S.; Mäger, I.; Breakefield, X.O.; Wood, M.J. E.L Andaloussi S. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat. Rev. Drug Discov., 2013, 12(5), 347-357.
[http://dx.doi.org/10.1038/nrd3978] [PMID: 23584393]
[95]
Park, S.H.; Won, J.; Kim, S.I.; Lee, Y.; Park, C.K.; Kim, S.K.; Choi, S.H. Molecular testing of brain tumor. J. Pathol. Transl. Med., 2017, 51(3), 205-223.
[http://dx.doi.org/10.4132/jptm.2017.03.08] [PMID: 28535583]
[96]
van Dijken, B.R.J.; van Laar, P.J.; Holtman, G.A.; van der Hoorn, A. Diagnostic accuracy of magnetic resonance imaging techniques for treatment response evaluation in patients with high-grade glioma, a systematic review and meta-analysis. Eur. Radiol., 2017, 27(10), 4129-4144.
[http://dx.doi.org/10.1007/s00330-017-4789-9] [PMID: 28332014]
[97]
Verduin, M.; Compter, I.; Steijvers, D.; Postma, A.A.; Eekers, D.B.P.; Anten, M.M.; Ackermans, L.; Ter Laan, M.; Leijenaar, R.T.H.; van de Weijer, T.; Tjan-Heijnen, V.C.G.; Hoeben, A.; Vooijs, M. Noninvasive glioblastoma testing: multimodal approach to monitoring and predicting treatment response. Dis. Markers, 2018, 2018, 2908609. (Online ahead of Print)
[http://dx.doi.org/10.1155/2018/2908609] [PMID: 29581794]
[98]
Guzmán-De-Villoria, J.A.; Mateos-Pérez, J.M.; Fernández-García, P.; Castro, E.; Desco, M. Added value of advanced over conventional magnetic resonance imaging in grading gliomas and other primary brain tumors. Cancer Imaging, 2014, 14, 35.
[http://dx.doi.org/10.1186/s40644-014-0035-8] [PMID: 25608821]
[99]
Rampling, R.; James, A.; Papanastassiou, V. The present and future management of malignant brain tumours: surgery, radiotherapy, chemotherapy. J. Neurol. Neurosurg. Psychiatry, 2004, 75(Suppl. 2), ii24-ii30.
[http://dx.doi.org/10.1136/jnnp.2004.040535] [PMID: 15146036]
[100]
Chowdhary, M.M.; Ene, C.I.; Silbergeld, D.L. Treatment of Gliomas: How did we get here? Surg. Neurol. Int., 2015, 6(Suppl. 1), S85-S88.
[http://dx.doi.org/10.4103/2152-7806.151348] [PMID: 25722937]
[101]
Bonucci, E. The origin of matrix vesicles and their role in the calcification of cartilage and bone. In:International Cell Biology; Springer: Berlin, 1980, pp. 993-1003.
[102]
Pan, B.T.; Johnstone, R.M. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell, 1983, 33(3), 967-978.
[http://dx.doi.org/10.1016/0092-8674(83)90040-5] [PMID: 6307529]
[103]
Pan, B.T.; Teng, K.; Wu, C.; Adam, M.; Johnstone, R.M. Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J. Cell Biol., 1985, 101(3), 942-948.
[http://dx.doi.org/10.1083/jcb.101.3.942] [PMID: 2993317]
[104]
Maia, J.; Caja, S.; Carolina, M.; Morae, S.; Couto, N.; Costa-Silva, B. Exosome-based cell-cell communication in the tumor microenvironment. Front. Cell Dev. Biol., 2018, 6, 1-47.
[http://dx.doi.org/10.3389/fcell.2018.00018]
[105]
Ramirez, S.H.; Andrews, A.M.; Paul, D.; Pachter, J.S. Extracellular vesicles: mediators and biomarkers of pathology along CNS barriers. Fluids Barriers CNS, 2018, 15(1), 19.
[http://dx.doi.org/10.1186/s12987-018-0104-7] [PMID: 29960602]
[106]
Dubois, L.G.; Campanati, L.; Righy, C.; D’Andrea-Meira, I.; Spohr, T.C.; Porto-Carreiro, I.; Pereira, C.M.; Balça-Silva, J.; Kahn, S.A.; DosSantos, M.F. Oliveira, Mde.A.; Ximenes-da-Silva, A.; Lopes, M.C.; Faveret, E.; Gasparetto, E.L.; Moura-Neto, V. Gliomas and the vascular fragility of the blood brain barrier. Front. Cell. Neurosci., 2014, 8, 418.
[http://dx.doi.org/10.3389/fncel.2014.00418] [PMID: 25565956]
[107]
Yoshioka, Y.; Konishi, Y.; Kosaka, N.; Katsuda, T.; Kato, T.; Ochiya, T. Comparative marker analysis of extracellular vesicles in different human cancer types. J. Extracell. Vesicles, 2013, 2, 1-9.
[http://dx.doi.org/10.3402/jev.v2i0.20424] [PMID: 24009892]