Major challenges and potential microenvironment-targeted therapies in glioblastoma

International Journal of Molecular Sciences

Volumn 18, Issue 12, 2017, Pages

  Arbab, Ali S ^a   Rashid, Mohammad H ^a   Angara, Kartik ^a   Borin, Thaiz F ^a   Lin, Ping Chang ^a   Jain, Meenu ^a   Achyut, Bhagelu R ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Antiangiogenic therapy; Bone marrow derived cells; Glioblastoma; Myeloid cells; Neovascularization; Resistance; Tumor microenvironment

Indexed keywords

CYTOCHROME P450 4A; ANGIOGENESIS INHIBITOR;

ANGIOGENESIS; ANTIANGIOGENIC THERAPY; BONE MARROW CELL; CANCER ADJUVANT THERAPY; GENE EXPRESSION PROFILING; GENETIC HETEROGENEITY; GLIOBLASTOMA; HUMAN; HYPOXIA; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOTHERAPY; LIFE EXPECTANCY; MOLECULARLY TARGETED THERAPY; NUCLEAR MAGNETIC RESONANCE IMAGING; REVIEW; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; VASCULARIZATION; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY;

ANGIOGENESIS INHIBITORS; GLIOBLASTOMA; HUMANS; MYELOID CELLS; NEOVASCULARIZATION, PATHOLOGIC; TUMOR MICROENVIRONMENT;

EID: 85038413424     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms18122732     Document Type: Review

References (159)

1. Thakkar, J.P.; Dolecek, T.A.; Horbinski, C.; Ostrom, Q.T.; Lightner, D.D.; Barnholtz-Sloan, J.S.; Villano, J.L. Epidemiologic and molecular prognostic review of glioblastoma. Cancer Epidemiol. Biomarkers Prev. 2014, 23, 1985–1996. [CrossRef] [PubMed]
2. 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. [CrossRef] [PubMed]
3. Oliver, L.; Olivier, C.; Marhuenda, F.B.; Campone, M.; Vallette, F.M. Hypoxia and the malignant glioma microenvironment: Regulation and implications for therapy. Curr. Mol. Pharmacol. 2009, 2, 263–284. [CrossRef] [PubMed]
4. Brem, S.; Cotran, R.; Folkman, J. Tumor angiogenesis: A quantitative method for histologic grading. J. Natl. Cancer Inst. 1972, 48, 347–356. [PubMed]
5. Wang, N.; Jain, R.K.; Batchelor, T.T. New Directions in Anti-Angiogenic Therapy for Glioblastoma. Neurotherapeutics 2017, 14, 321–332. [CrossRef] [PubMed]
6. Hanash, S.; Schliekelman, M. Proteomic profiling of the tumor microenvironment: Recent insights and the search for biomarkers. Genome Med. 2014, 6, 12. [CrossRef] [PubMed]
7. Charles, N.A.; Holland, E.C.; Gilbertson, R.; Glass, R.; Kettenmann, H. The brain tumor microenvironment. Glia 2011, 59, 1169–1180. [CrossRef] [PubMed]
8. Koch, S.; Tugues, S.; Li, X.; Gualandi, L.; Claesson-Welsh, L. Signal transduction by vascular endothelial growth factor receptors. Biochem. J. 2011, 437, 169–183. [CrossRef] [PubMed]
9. Du, R.; Lu, K.V.; Petritsch, C.; Liu, P.; Ganss, R.; Passegue, E.; Song, H.; Vandenberg, S.; Johnson, R.S.; Werb, Z. et al. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 2008, 13, 206–220. [CrossRef] [PubMed]
10. Plate, K.H.; Breier, G.; Weich, H.A.; Risau, W. Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 1992, 359, 845–848. [CrossRef] [PubMed]
11. Jones, M.K.; Itani, R.M.; Wang, H.; Tomikawa, M.; Sarfeh, I.J.; Szabo, S.; Tarnawski, A.S. Activation of VEGF and Ras genes in gastric mucosa during angiogenic response to ethanol injury. Am. J. Physiol. 1999, 276, G1345–G1355. [CrossRef]
12. Gomez-Manzano, C.; Fueyo, J.; Jiang, H.; Glass, T.L.; Lee, H.Y.; Hu, M.; Liu, J.L.; Jasti, S.L.; Liu, T.J.; Conrad, C.A. et al. Mechanisms underlying PTEN regulation of vascular endothelial growth factor and angiogenesis. Ann. Neurol. 2003, 53, 109–117. [CrossRef] [PubMed]
13. Takahashi, T.; Shibuya, M. The 230 kDa mature form of KDR/Flk-1 (VEGF receptor-2) activates the PLC-gamma pathway and partially induces mitotic signals in NIH3T3 fibroblasts. Oncogene 1997, 14, 2079–2089. [CrossRef] [PubMed]
14. Saino, M.; Maruyama, T.; Sekiya, T.; Kayama, T.; Murakami, Y. Inhibition of angiogenesis in human glioma cell lines by antisense RNA from the soluble guanylate cyclase genes, GUCY1A3 and GUCY1B3. Oncol. Rep. 2004, 12, 47–52. [CrossRef] [PubMed]
15. Tsai, J.C.; Goldman, C.K.; Gillespie, G.Y. Vascular endothelial growth factor in human glioma cell lines: Induced secretion by EGF, PDGF-BB, and bFGF. J. Neurosurg. 1995, 82, 864–873. [CrossRef] [PubMed]
16. Kerbel, R.S. Tumor angiogenesis. N. Engl. J. Med. 2008, 358, 2039–2049. [CrossRef] [PubMed]
17. Talasila, K.M.; Rosland, G.V.; Hagland, H.R.; Eskilsson, E.; Flones, I.H.; Fritah, S.; Azuaje, F.; Atai, N.; Harter, P.N.; Mittelbronn, M. et al. The angiogenic switch leads to a metabolic shift in human glioblastoma. Neuro Oncol. 2017, 19, 383–393. [CrossRef] [PubMed]
18. Folkman, J. Tumor angiogenesis: Therapeutic implications. N. Engl. J. Med. 1971, 285, 1182–1186. [PubMed]
19. Folkman, J.; Shing, Y. Angiogenesis. J. Biol. Chem. 1992, 267, 10931–10934. [PubMed]
20. Ferrara, N. VEGF and Intraocular Neovascularization: From Discovery to Therapy. Transl. Vis. Sci. Technol. 2016, 5, 10. [CrossRef] [PubMed]
21. Folkman, J.; Long, D.M., Jr.; Becker, F.F. Growth and metastasis of tumor in organ culture. Cancer 1963, 16, 453–467. [CrossRef]
22. Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: The next generation. Cell 2011, 144, 646–674. [CrossRef] [PubMed]
23. Mittal, K.; Ebos, J.; Rini, B. Angiogenesis and the tumor microenvironment: Vascular endothelial growth factor and beyond. Semin. Oncol. 2014, 41, 235–251. [CrossRef] [PubMed]
24. Bruno, A.; Pagani, A.; Magnani, E.; Rossi, T.; Noonan, D.M.; Cantelmo, A.R.; Albini, A. Inflammatory angiogenesis and the tumor microenvironment as targets for cancer therapy and prevention. Cancer Treat. Res. 2014, 159, 401–426. [PubMed]
25. Samples, J.; Willis, M.; Klauber-Demore, N. Targeting angiogenesis and the tumor microenvironment. Surg. Oncol. Clin. N. Am. 2013, 22, 629–639. [CrossRef] [PubMed]
26. Saharinen, P.; Eklund, L.; Pulkki, K.; Bono, P.; Alitalo, K. VEGF and angiopoietin signaling in tumor angiogenesis and metastasis. Trends Mol. Med. 2011, 17, 347–362. [CrossRef] [PubMed]
27. Rahman, R.; Smith, S.; Rahman, C.; Grundy, R. Antiangiogenic therapy and mechanisms of tumor resistance in malignant glioma. J. Oncol. 2010, 2010, 251231. [CrossRef] [PubMed]
28. Dietrich, J.; Norden, A.D.; Wen, P.Y. Emerging antiangiogenic treatments for gliomas—Efficacy and safety issues. Curr. Opin. Neurol. 2008, 21, 736–744. [CrossRef] [PubMed]
29. Miller, K.D.; Sweeney, C.J.; Sledge, G.W., Jr. Can tumor angiogenesis be inhibited without resistance? In Mechanisms of Angiogenesis; Matthias, C., Georg, B., Eds.; Birkhäuser Basel: Basel, Switzerland; pp. 95–112.
30. Ali, M.M.; Kumar, S.; Shankar, A.; Varma, N.R.; Iskander, A.S.; Janic, B.; Chwang, W.B.; Jain, R.; Babajeni-Feremi, A.; Borin, T.F. et al. Effects of tyrosine kinase inhibitors and CXCR4 antagonist on tumor growth and angiogenesis in rat glioma model: MRI and protein analysis study. Transl. Oncol. 2013, 6, 660–669. [CrossRef] [PubMed]
31. Ali, M.M.; Janic, B.; Babajani-Feremi, A.; Varma, N.R.; Iskander, A.S.; Anagli, J.; Arbab, A.S. Changes in vascular permeability and expression of different angiogenic factors following anti-angiogenic treatment in rat glioma. PLoS ONE 2010, 5, e8727. [CrossRef] [PubMed]
32. Batchelor, T.T.; Duda, D.G.; di Tomaso, E.; Ancukiewicz, M.; Plotkin, S.R.; Gerstner, E.; Eichler, A.F.; Drappatz, J.; Hochberg, F.H.; Benner, T. et al. Phase II study of cediranib, an oral pan-vascular endothelial growth factor receptor tyrosine kinase inhibitor, in patients with recurrent glioblastoma. J. Clin. Oncol. 2010, 28, 2817–2823. [CrossRef] [PubMed]
33. Kamoun, W.S.; Ley, C.D.; Farrar, C.T.; Duyverman, A.M.; Lahdenranta, J.; Lacorre, D.A.; Batchelor, T.T.; di Tomaso, E.; Duda, D.G.; Munn, L.L. et al. Edema control by cediranib, a vascular endothelial growth factor receptor-targeted kinase inhibitor, prolongs survival despite persistent brain tumor growth in mice. J. Clin. Oncol. 2009, 27, 2542–2552. [CrossRef] [PubMed]
34. Neyns, B.; Sadones, J.; Chaskis, C.; Dujardin, M.; Everaert, H.; Lv, S.; Duerinck, J.; Tynninen, O.; Nupponen, N.; Michotte, A. et al. Phase II study of sunitinib malate in patients with recurrent high-grade glioma. J. Neurooncol. 2011, 103, 491–501. [CrossRef] [PubMed]
35. Reardon, D.A.; Vredenburgh, J.J.; Coan, A.; Desjardins, A.; Peters, K.B.; Gururangan, S.; Sathornsumetee, S.; Rich, J.N.; Herndon, J.E.; Friedman, H.S. Phase I study of sunitinib and irinotecan for patients with recurrent malignant glioma. J. Neurooncol. 2011, 105, 621–627. [CrossRef] [PubMed]
36. Reardon, D.A.; Egorin, M.J.; Desjardins, A.; Vredenburgh, J.J.; Beumer, J.H.; Lagattuta, T.F.; Gururangan, S.; Herndon, J.E., 2nd; Salvado, A.J.; Friedman, H.S. Phase I pharmacokinetic study of the vascular endothelial growth factor receptor tyrosine kinase inhibitor vatalanib (PTK787) plus imatinib and hydroxyurea for malignant glioma. Cancer 2009, 115, 2188–2198. [CrossRef] [PubMed]
37. Achyut, B.R.; Shankar, A.; Iskander, A.S.; Ara, R.; Knight, R.A.; Scicli, A.G.; Arbab, A.S. Chimeric Mouse model to track the migration of bone marrow derived cells in glioblastoma following anti-angiogenic treatments. Cancer Biol. Ther. 2016, 17, 280–290. [CrossRef] [PubMed]
38. Shaaban, S.; Alsulami, M.; Arbab, S.A.; Ara, R.; Shankar, A.; Iskander, A.; Angara, K.; Jain, M.; Bagher-Ebadian, H.; Achyut, B.R. et al. Targeting Bone Marrow to Potentiate the Anti-Tumor Effect of Tyrosine Kinase Inhibitor in Preclinical Rat Model of Human Glioblastoma. Int. J. Cancer Res. 2016, 12, 69–81. [PubMed]
39. Achyut, B.R.; Shankar, A.; Iskander, A.S.; Ara, R.; Angara, K.; Zeng, P.; Knight, R.A.; Scicli, A.G.; Arbab, A.S. Bone marrow derived myeloid cells orchestrate antiangiogenic resistance in glioblastoma through coordinated molecular networks. Cancer Lett. 2015, 369, 416–426. [CrossRef] [PubMed]
40. Achyut, B.R.; Angara, K.; Jain, M.; Borin, T.F.; Rashid, M.H.; Iskander, A.S.M.; Ara, R.; Kolhe, R.; Howard, S.; Venugopal, N. et al. Canonical NFkappaB signaling in myeloid cells is required for the glioblastoma growth. Sci. Rep. 2017, 7, 13754. [CrossRef] [PubMed]
41. Rosen, L.S. Clinical experience with angiogenesis signaling inhibitors: Focus on vascular endothelial growth factor (VEGF) blockers. Cancer Control 2002, 9 (Suppl. 2), 36–44. [CrossRef] [PubMed]
42. Norden, A.D.; Young, G.S.; Setayesh, K.; Muzikansky, A.; Klufas, R.; Ross, G.L.; Ciampa, A.S.; Ebbeling, L.G.; Levy, B.; Drappatz, J. et al. Bevacizumab for recurrent malignant gliomas: Efficacy, toxicity, and patterns of recurrence. Neurology 2008, 70, 779–787. [CrossRef] [PubMed]
43. Kreisl, T.N.; Zhang, W.; Odia, Y.; Shih, J.H.; Butman, J.A.; Hammoud, D.; Iwamoto, F.M.; Sul, J.; Fine, H.A. A phase II trial of single-agent bevacizumab in patients with recurrent anaplastic glioma. Neuro Oncol. 2011, 13, 1143–1150. [CrossRef] [PubMed]
44. Reardon, D.A.; Desjardins, A.; Peters, K.B.; Gururangan, S.; Sampson, J.H.; McLendon, R.E.; Herndon, J.E., 2nd; Bulusu, A.; Threatt, S.; Friedman, A.H. et al. Phase II study of carboplatin, irinotecan, and bevacizumab for bevacizumab naive, recurrent glioblastoma. J. Neurooncol. 2012, 107, 155–164. [CrossRef] [PubMed]
45. Wick, W.; Gorlia, T.; Bendszus, M.; Taphoorn, M.; Sahm, F.; Harting, I.; Brandes, A.A.; Taal, W.; Domont, J.; Idbaih, A. et al. Lomustine and Bevacizumab in Progressive Glioblastoma. N. Engl. J. Med. 2017, 377, 1954–1963. [CrossRef] [PubMed]
46. Kumar, S.; Arbab, A.S. Neovascularization in Glioblastoma: Current Pitfall in Anti-angiogenic therapy. Zhong Liu Za Zhi 2013, 1, 16–19. [PubMed]
47. Hardee, M.E.; Zagzag, D. Mechanisms of glioma-associated neovascularization. Am. J. Pathol. 2012, 181, 1126–1141. [CrossRef] [PubMed]
48. Carmeliet, P.; Jain, R.K. Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat. Rev. Drug Discov. 2011, 10, 417–427. [CrossRef] [PubMed]
49. Angara, K.; Rashid, M.H.; Shankar, A.; Ara, R.; Iskander, A.; Borin, T.F.; Jain, M.; Achyut, B.R.; Arbab, A.S. Vascular mimicry in glioblastoma following anti-angiogenic and anti-20-HETE therapies. Histol. Histopathol. 2017, 32, 917–928. [PubMed]
50. Angara, K.; Borin, T.F.; Arbab, A.S. Vascular Mimicry: A Novel Neovascularization Mechanism Driving Anti-Angiogenic Therapy (AAT) Resistance in Glioblastoma. Transl. Oncol. 2017, 10, 650–660. [CrossRef] [PubMed]
51. Arbab, A.S.; Jain, M.; Achyut, B.R. Vascular Mimicry: The Next Big Glioblastoma Target. Biochem. Physiol. 2015, 4, e410. [PubMed]
52. Folberg, R.; Hendrix, M.J.; Maniotis, A.J. Vasculogenic mimicry and tumor angiogenesis. Am. J. Pathol. 2000, 156, 361–381. [CrossRef]
53. Maniotis, A.J.; Folberg, R.; Hess, A.; Seftor, E.A.; Gardner, L.M.; Pe’er, J.; Trent, J.M.; Meltzer, P.S.; Hendrix, M.J. Vascular channel formation by human melanoma cells in vivo and in vitro: Vasculogenic mimicry. Am. J. Pathol. 1999, 155, 739–752. [CrossRef]
54. Sullivan, J.P.; Nahed, B.V.; Madden, M.W.; Oliveira, S.M.; Springer, S.; Bhere, D.; Chi, A.S.; Wakimoto, H.; Rothenberg, S.M.; Sequist, L.V. et al. Brain tumor cells in circulation are enriched for mesenchymal gene expression. Cancer Discov. 2014, 4, 1299–1309. [CrossRef] [PubMed]
55. Ortensi, B.; Setti, M.; Osti, D.; Pelicci, G. Cancer stem cell contribution to glioblastoma invasiveness. Stem Cell Res. Ther. 2013, 4, 18. [CrossRef] [PubMed]
56. Carmeliet, P.; Jain, R.K. Molecular mechanisms and clinical applications of angiogenesis. Nature 2011, 473, 298–307. [CrossRef] [PubMed]
57. Zhou, W.; Chen, C.; Shi, Y.; Wu, Q.; Gimple, R.C.; Fang, X.; Huang, Z.; Zhai, K.; Ke, S.Q.; Ping, Y.F. et al. Targeting Glioma Stem Cell-Derived Pericytes Disrupts the Blood-Tumor Barrier and Improves Chemotherapeutic Efficacy. Cell Stem Cell 2017, 21, 591–603. [CrossRef] [PubMed]
58. Yi, Y.; Hsieh, I.Y.; Huang, X.; Li, J.; Zhao, W. Glioblastoma Stem-Like Cells: Characteristics, Microenvironment, and Therapy. Front. Pharmacol. 2016, 7, 477. [CrossRef] [PubMed]
59. Liebelt, B.D.; Shingu, T.; Zhou, X.; Ren, J.; Shin, S.A.; Hu, J. Glioma Stem Cells: Signaling, Microenvironment, and Therapy. Stem Cells Int. 2016, 2016, 7849890. [CrossRef] [PubMed]
60. Audia, A.; Conroy, S.; Glass, R.; Bhat, K.P.L. The Impact of the Tumor Microenvironment on the Properties of Glioma Stem-Like Cells. Front. Oncol. 2017, 7, 143. [CrossRef] [PubMed]
61. Soda, Y.; Marumoto, T.; Friedmann-Morvinski, D.; Soda, M.; Liu, F.; Michiue, H.; Pastorino, S.; Yang, M.; Hoffman, R.M.; Kesari, S. et al. Transdifferentiation of glioblastoma cells into vascular endothelial cells. Proc. Natl. Acad. Sci. USA 2011, 108, 4274–4280. [CrossRef] [PubMed]
62. Wang, R.; Chadalavada, K.; Wilshire, J.; Kowalik, U.; Hovinga, K.E.; Geber, A.; Fligelman, B.; Leversha, M.; Brennan, C.; Tabar, V. Glioblastoma stem-like cells give rise to tumour endothelium. Nature 2010, 468, 829–833. [CrossRef] [PubMed]
63. Wang, S.Y.; Ke, Y.Q.; Lu, G.H.; Song, Z.H.; Yu, L.; Xiao, S.; Sun, X.L.; Jiang, X.D.; Yang, Z.L.; Hu, C.C. Vasculogenic mimicry is a prognostic factor for postoperative survival in patients with glioblastoma. J. Neurooncol. 2013, 112, 339–345. [CrossRef] [PubMed]
64. Liu, X.M.; Zhang, Q.P.; Mu, Y.G.; Zhang, X.H.; Sai, K.; Pang, J.C.; Ng, H.K.; Chen, Z.P. Clinical significance of vasculogenic mimicry in human gliomas. J. Neurooncol. 2011, 105, 173–179. [CrossRef] [PubMed]
65. Malmstrom, A.; Gronberg, B.H.; Marosi, C.; Stupp, R.; Frappaz, D.; Schultz, H.; Abacioglu, U.; Tavelin, B.; Lhermitte, B.; Hegi, M.E. et al. Temozolomide versus standard 6-week radiotherapy versus hypofractionated radiotherapy in patients older than 60 years with glioblastoma: The Nordic randomised, phase 3 trial. Lancet Oncol. 2012, 13, 916–926. [CrossRef]
66. Stupp, R.; Mason, W.P.; van den Bent, M.J.; Weller, M.; Fisher, B.; Taphoorn, M.J.; Belanger, K.; Brandes, A.A.; Marosi, C.; Bogdahn, U. et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 2005, 352, 987–996. [CrossRef] [PubMed]
67. Ellor, S.V.; Pagano-Young, T.A.; Avgeropoulos, N.G. Glioblastoma: Background, standard treatment paradigms, and supportive care considerations. J. Law Med. Ethics 2014, 42, 171–182. [CrossRef] [PubMed]
68. Walid, M.S. Prognostic factors for long-term survival after glioblastoma. Perm. J. 2008, 12, 45–48. [CrossRef] [PubMed]
69. Stupp, R.; Hegi, M.E.; Mason, W.P.; van den Bent, M.J.; Taphoorn, M.J.; Janzer, R.C.; Ludwin, S.K.; Allgeier, A.; Fisher, B.; Belanger, K. et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009, 10, 459–466. [CrossRef]
70. Van Meir, E.G.; Hadjipanayis, C.G.; Norden, A.D.; Shu, H.K.; Wen, P.Y.; Olson, J.J. Exciting new advances in neuro-oncology: The avenue to a cure for malignant glioma. CA Cancer J. Clin. 2010, 60, 166–193. [CrossRef] [PubMed]
71. Woehrer, A.; Bauchet, L.; Barnholtz-Sloan, J.S. Glioblastoma survival: Has it improved? Evidence from population-based studies. Curr. Opin. Neurol. 2014, 27, 666–674. [CrossRef] [PubMed]
72. Swartz, A.M.; Li, Q.J.; Sampson, J.H. Rindopepimut: A promising immunotherapeutic for the treatment of glioblastoma multiforme. Immunotherapy 2014, 6, 679–690. [CrossRef] [PubMed]
73. Swartz, A.M.; Batich, K.A.; Fecci, P.E.; Sampson, J.H. Peptide vaccines for the treatment of glioblastoma. J. Neurooncol. 2014, 123, 433–440. [CrossRef] [PubMed]
74. Venur, V.A.; Peereboom, D.M.; Ahluwalia, M.S. Current medical treatment of glioblastoma. Cancer Treat. Res. 2015, 163, 103–115. [PubMed]
75. Hoffermann, M.; Bruckmann, L.; Kariem Mahdy, A.; Asslaber, M.; Payer, F.; von Campe, G. Treatment results and outcome in elderly patients with glioblastoma multiforme—A retrospective single institution analysis. Clin. Neurol. Neurosurg. 2015, 128, 60–69. [CrossRef] [PubMed]
76. Tsang, D.S.; Khan, L.; Perry, J.R.; Soliman, H.; Sahgal, A.; Keith, J.L.; Mainprize, T.G.; Das, S.; Zhang, L.; Tsao, M.N. Survival Outcomes in Elderly Patients with Glioblastoma. Clin. Oncol. 2015, 27, 176–183. [CrossRef] [PubMed]
77. Lau, D.; Magill, S.T.; Aghi, M.K. Molecularly targeted therapies for recurrent glioblastoma: Current and future targets. Neurosurg. Focus 2014, 37, E15. [CrossRef] [PubMed]
78. Multhoff, G.; Radons, J. Radiation, Inflammation, and Immune Responses in Cancer. Front. Oncol. 2012, 2, 58. [CrossRef] [PubMed]
79. Yeung, Y.T.; McDonald, K.L.; Grewal, T.; Munoz, L. Interleukins in glioblastoma pathophysiology: Implications for therapy. Br. J. Pharmacol. 2013, 168, 591–606. [CrossRef] [PubMed]
80. Hardee, M.E.; Marciscano, A.E.; Medina-Ramirez, C.M.; Zagzag, D.; Narayana, A.; Lonning, S.M.; Barcellos-Hoff, M.H. Resistance of Glioblastoma-Initiating Cells to Radiation Mediated by the Tumor Microenvironment Can Be Abolished by Inhibiting Transforming Growth Factor-β. Cancer Res. 2012, 72, 4119–4129. [CrossRef] [PubMed]
81. Lu-Emerson, C.; Snuderl, M.; Kirkpatrick, N.D.; Goveia, J.; Davidson, C.; Huang, Y.; Riedemann, L.; Taylor, J.; Ivy, P.; Duda, D.G. et al. Increase in tumor-associated macrophages after antiangiogenic therapy is associated with poor survival among patients with recurrent glioblastoma. Neuro Oncol. 2013, 15, 1079–1087. [CrossRef] [PubMed]
82. Allavena, P.; Garlanda, C.; Borrello, M.G.; Sica, A.; Mantovani, A. Pathways connecting inflammation and cancer. Curr. Opin. Genet. Dev. 2008, 18, 3–10. [CrossRef] [PubMed]
83. DeNardo, D.G.; Brennan, D.J.; Rexhepaj, E.; Ruffell, B.; Shiao, S.L.; Madden, S.F.; Gallagher, W.M.; Wadhwani, N.; Keil, S.D.; Junaid, S.A. et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov. 2011, 1, 54–67. [CrossRef] [PubMed]
84. Fadul, C.E.; Fisher, J.L.; Gui, J.; Hampton, T.H.; Cote, A.L.; Ernstoff, M.S. Immune modulation effects of concomitant temozolomide and radiation therapy on peripheral blood mononuclear cells in patients with glioblastoma multiforme. Neuro Oncol. 2011, 13, 393–400. [CrossRef] [PubMed]
85. Sengupta, S.; Marrinan, J.; Frishman, C.; Sampath, P. Impact of temozolomide on immune response during malignant glioma chemotherapy. Clin. Dev. Immunol. 2012, 2012, 831090. [CrossRef] [PubMed]
86. Achyut, B.R.; Arbab, A.S. Myeloid cell signatures in tumor microenvironment predicts therapeutic response in cancer. OncoTargets Ther. 2016, 9, 1047–1055.
87. Bruchard, M.; Mignot, G.; Derangere, V.; Chalmin, F.; Chevriaux, A.; Vegran, F.; Boireau, W.; Simon, B.; Ryffel, B.; Connat, J.L. et al. Chemotherapy-triggered cathepsin B release in myeloid-derived suppressor cells activates the Nlrp3 inflammasome and promotes tumor growth. Nat. Med. 2013, 19, 57–64. [CrossRef] [PubMed]
88. Wang, X.; Chen, J.X.; Liu, J.P.; You, C.; Liu, Y.H.; Mao, Q. Gain of function of mutant TP53 in glioblastoma: Prognosis and response to temozolomide. Ann. Surg. Oncol. 2014, 21, 1337–1344. [CrossRef] [PubMed]
89. Brazdova, M.; Quante, T.; Togel, L.; Walter, K.; Loscher, C.; Tichy, V.; Cincarova, L.; Deppert, W.; Tolstonog, G.V. Modulation of gene expression in U251 glioblastoma cells by binding of mutant p53 R273H to intronic and intergenic sequences. Nucleic Acids Res. 2009, 37, 1486–1500. [CrossRef] [PubMed]
90. Hegi, M.E.; Diserens, A.C.; Gorlia, T.; Hamou, M.F.; de Tribolet, N.; Weller, M.; Kros, J.M.; Hainfellner, J.A.; Mason, W.; Mariani, L. et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N. Engl. J. Med. 2005, 352, 997–1003. [CrossRef] [PubMed]
91. Davis, M.E. Glioblastoma: Overview of Disease and Treatment. Clin. J. Oncol. Nurs. 2016, 20, S2–S8. [CrossRef] [PubMed]
92. Olar, A.; Aldape, K.D. Using the molecular classification of glioblastoma to inform personalized treatment. J. Pathol. 2014, 232, 165–177. [CrossRef] [PubMed]
93. Verhaak, R.G.; Hoadley, K.A.; Purdom, E.; Wang, V.; Qi, Y.; Wilkerson, M.D.; Miller, C.R.; Ding, L.; Golub, T.; Mesirov, J.P. et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010, 17, 98–110. [CrossRef] [PubMed]
94. 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 2016World Health Organization Classification of Tumors of the Central Nervous System: A summary. Acta Neuropathol. 2016, 131, 803–820. [CrossRef] [PubMed]
95. Hoshide, R.; Jandial, R. 2016World Health Organization Classification of Central Nervous System Tumors: An Era of Molecular Biology. World Neurosurg. 2016, 94, 561–562. [CrossRef] [PubMed]
96. Yan, H.; Parsons, D.W.; Jin, G.; McLendon, R.; Rasheed, B.A.; Yuan, W.; Kos, I.; Batinic-Haberle, I.; Jones, S.; Riggins, G.J. et al. IDH1 and IDH2 mutations in gliomas. N. Engl. J. Med. 2009, 360, 765–773. [CrossRef] [PubMed]
97. Ohgaki, H.; Kleihues, P. The definition of primary and secondary glioblastoma. Clin. Cancer Res. 2013, 19, 764–772. [CrossRef] [PubMed]
98. Broniscer, A.; Tatevossian, R.G.; Sabin, N.D.; Klimo, P., Jr.; Dalton, J.; Lee, R.; Gajjar, A.; Ellison, D.W. Clinical, radiological, histological and molecular characteristics of paediatric epithelioid glioblastoma. Neuropathol. Appl. Neurobiol. 2014, 40, 327–336. [CrossRef] [PubMed]
99. Kleinschmidt-DeMasters, B.K.; Aisner, D.L.; Foreman, N.K. BRAF VE1 immunoreactivity patterns in epithelioid glioblastomas positive for BRAF V600E mutation. Am. J. Surg. Pathol. 2015, 39, 528–540. [CrossRef] [PubMed]
100. Parsons, D.W.; Jones, S.; Zhang, X.; Lin, J.C.; Leary, R.J.; Angenendt, P.; Mankoo, P.; Carter, H.; Siu, I.M.; Gallia, G.L. et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008, 321, 1807–1812. [CrossRef] [PubMed]
101. Appin, C.L.; Gao, J.; Chisolm, C.; Torian, M.; Alexis, D.; Vincentelli, C.; Schniederjan, M.J.; Hadjipanayis, C.; Olson, J.J.; Hunter, S. et al. Glioblastoma with oligodendroglioma component (GBM-O): Molecular genetic and clinical characteristics. Brain Pathol. 2013, 23, 454–461. [CrossRef] [PubMed]
102. Hinrichs, B.H.; Newman, S.; Appin, C.L.; Dunn, W.; Cooper, L.; Pauly, R.; Kowalski, J.; Rossi, M.R.; Brat, D.J. Farewell to GBM-O: Genomic and transcriptomic profiling of glioblastoma with oligodendroglioma component reveals distinct molecular subgroups. Acta Neuropathol. Commun. 2016, 4, 4. [CrossRef] [PubMed]
103. Labussiere, M.; Idbaih, A.; Wang, X.W.; Marie, Y.; Boisselier, B.; Falet, C.; Paris, S.; Laffaire, J.; Carpentier, C.; Criniere, E. et al. All the 1p19q codeleted gliomas are mutated on IDH1 or IDH2. Neurology 2010, 74, 1886–1890. [CrossRef] [PubMed]
104. Xiong, J.; Liu, Y.; Wang, Y.; Ke, R.H.; Mao, Y.; Ye, Z.R. Chromosome 1p/19q status combined with expression of p53 protein improves the diagnostic and prognostic evaluation of oligodendrogliomas. Chin. Med. J. (Engl.) 2010, 123, 3566–3573. [PubMed]
105. Eoli, M.; Menghi, F.; Bruzzone, M.G.; De Simone, T.; Valletta, L.; Pollo, B.; Bissola, L.; Silvani, A.; Bianchessi, D.; D’Incerti, L. et al. Methylation of O6-methylguanine DNA methyltransferase and loss of heterozygosity on 19q and/or 17p are overlapping features of secondary glioblastomas with prolonged survival. Clin. Cancer Res. 2007, 13, 2606–2613. [CrossRef] [PubMed]
106. Achyut, B.R. Impact of Microenvironment in Therapy-Induced Neovascularization of Glioblastoma. Biochem. Physiol. 2013, 2, e121. [CrossRef]
107. Achyut, B.R.; Yang, L. Transforming growth factor-beta in the gastrointestinal and hepatic tumor microenvironment. Gastroenterology 2011, 141, 1167–1178. [CrossRef] [PubMed]
108. Lahmar, Q.; Keirsse, J.; Laoui, D.; Movahedi, K.; Van Overmeire, E.; Van Ginderachter, J.A. Tissue-resident versus monocyte-derived macrophages in the tumor microenvironment. Biochim. Biophys. Acta 2016, 1865, 23–34. [CrossRef] [PubMed]
109. El Gazzar, M. microRNAs as potential regulators of myeloid-derived suppressor cell expansion. Innate Immun. 2014, 20, 227–238. [CrossRef] [PubMed]
110. Nakasone, E.S.; Askautrud, H.A.; Kees, T.; Park, J.H.; Plaks, V.; Ewald, A.J.; Fein, M.; Rasch, M.G.; Tan, Y.X.; Qiu, J. et al. Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance. Cancer Cell 2012, 21, 488–503. [CrossRef] [PubMed]
111. De Visser, K.E.; Eichten, A.; Coussens, L.M. Paradoxical roles of the immune system during cancer development. Nat. Rev. Cancer 2006, 6, 24–37. [CrossRef] [PubMed]
112. Campbell, M.; Tonlaar, N.; Garwood, E.; Huo, D.; Moore, D.; Khramtsov, A.; Au, A.; Baehner, F.; Chen, Y.; Malaka, D. et al. Proliferating macrophages associated with high grade, hormone receptor negative breast cancer and poor clinical outcome. Breast Cancer Res. Treat. 2011, 128, 703–711. [CrossRef] [PubMed]
113. Jinushi, M.; Baghdadi, M.; Chiba, S.; Yoshiyama, H. Regulation of cancer stem cell activities by tumor-associated macrophages. Am. J. Cancer Res. 2012, 2, 529–539. [PubMed]
114. Shostak, K.; Chariot, A. NF-κB, stem cells and breast cancer: The links get stronger. Breast Cancer Res. BCR 2011, 13, 214. [CrossRef] [PubMed]
115. Andrade, J.; Ge, S.; Symbatyan, G.; Rosol, M.S.; Olch, A.J.; Crooks, G.M. Effects of sublethal irradiation on patterns of engraftment after murine bone marrow transplantation. Biol. Blood Marrow Transplant. 2011, 17, 608–619. [CrossRef] [PubMed]
116. Achyut, B.R.; Arbab, A.S. Myeloid Derived Suppressor Cells: Fuel the Fire. Biochem. Physiol. 2014, 3, e123. [PubMed]
117. Gabrilovich, D.I.; Ostrand-Rosenberg, S.; Bronte, V. Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 2012, 12, 253–268. [CrossRef] [PubMed]
118. Shojaei, F.; Wu, X.; Qu, X.; Kowanetz, M.; Yu, L.; Tan, M.; Meng, Y.G.; Ferrara, N. G-CSF-initiated myeloid cell mobilization and angiogenesis mediate tumor refractoriness to anti-VEGF therapy in mouse models. Proc. Natl. Acad. Sci. USA 2009, 106, 6742–6747. [CrossRef] [PubMed]
119. Shojaei, F.; Wu, X.; Malik, A.K.; Zhong, C.; Baldwin, M.E.; Schanz, S.; Fuh, G.; Gerber, H.P.; Ferrara, N. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells. Nat. Biotechnol. 2007, 25, 911–920. [CrossRef] [PubMed]
120. Piao, Y.; Liang, J.; Holmes, L.; Zurita, A.J.; Henry, V.; Heymach, J.V.; de Groot, J.F. Glioblastoma resistance to anti-VEGF therapy is associated with myeloid cell infiltration, stem cell accumulation, and a mesenchymal phenotype. Neuro Oncol. 2012, 14, 1379–1392. [CrossRef] [PubMed]
121. Chung, A.S.; Wu, X.; Zhuang, G.; Ngu, H.; Kasman, I.; Zhang, J.; Vernes, J.M.; Jiang, Z.; Meng, Y.G.; Peale, F.V. et al. An interleukin-17-mediated paracrine network promotes tumor resistance to anti-angiogenic therapy. Nat. Med. 2013, 19, 1114–1123. [CrossRef] [PubMed]
122. Sawanobori, Y.; Ueha, S.; Kurachi, M.; Shimaoka, T.; Talmadge, J.E.; Abe, J.; Shono, Y.; Kitabatake, M.; Kakimi, K.; Mukaida, N. et al. Chemokine-mediated rapid turnover of myeloid-derived suppressor cells in tumor-bearing mice. Blood 2008, 111, 5457–5466. [CrossRef] [PubMed]
123. Lin, E.Y.; Nguyen, A.V.; Russell, R.G.; Pollard, J.W. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J. Exp. Med. 2001, 193, 727–740. [CrossRef] [PubMed]
124. Movahedi, K.; Guilliams, M.; Van den Bossche, J.; Van den Bergh, R.; Gysemans, C.; Beschin, A.; De Baetselier, P.; Van Ginderachter, J.A. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 2008, 111, 4233–4244. [CrossRef] [PubMed]
125. Xu, J.; Escamilla, J.; Mok, S.; David, J.; Priceman, S.; West, B.; Bollag, G.; McBride, W.; Wu, L. CSF1R signaling blockade stanches tumor-infiltrating myeloid cells and improves the efficacy of radiotherapy in prostate cancer. Cancer Res. 2013, 73, 2782–2794. [CrossRef] [PubMed]
126. MacDonald, K.P.; Rowe, V.; Bofinger, H.M.; Thomas, R.; Sasmono, T.; Hume, D.A.; Hill, G.R. The colony-stimulating factor 1 receptor is expressed on dendritic cells during differentiation and regulates their expansion. J. Immunol. 2005, 175, 1399–1405. [CrossRef] [PubMed]
127. Hamilton, J.A. Colony-stimulating factors in inflammation and autoimmunity. Nat. Rev. Immunol. 2008, 8, 533–544. [CrossRef] [PubMed]
128. Hume, D.A.; MacDonald, K.P. Therapeutic applications of macrophage colony-stimulating factor-1 (CSF-1) and antagonists of CSF-1 receptor (CSF-1R) signaling. Blood 2012, 119, 1810–1820. [CrossRef] [PubMed]
129. Priceman, S.J.; Sung, J.L.; Shaposhnik, Z.; Burton, J.B.; Torres-Collado, A.X.; Moughon, D.L.; Johnson, M.; Lusis, A.J.; Cohen, D.A.; Iruela-Arispe, M.L. et al. Targeting distinct tumor-infiltrating myeloid cells by inhibiting CSF-1 receptor: Combating tumor evasion of antiangiogenic therapy. Blood 2010, 115, 1461–1471. [CrossRef] [PubMed]
130. Zhu, Y.; Knolhoff, B.L.; Meyer, M.A.; Nywening, T.M.; West, B.L.; Luo, J.; Wang-Gillam, A.; Goedegebuure, S.P.; Linehan, D.C.; DeNardo, D.G. CSF1/CSF1R blockade reprograms tumor-infiltrating macrophages and improves response to T-cell checkpoint immunotherapy in pancreatic cancer models. Cancer Res. 2014, 74, 5057–5069. [CrossRef] [PubMed]
131. Pyonteck, S.M.; Akkari, L.; Schuhmacher, A.J.; Bowman, R.L.; Sevenich, L.; Quail, D.F.; Olson, O.C.; Quick, M.L.; Huse, J.T.; Teijeiro, V. et al. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat. Med. 2013, 19, 1264–1272. [CrossRef] [PubMed]
132. Quail, D.F.; Bowman, R.L.; Akkari, L.; Quick, M.L.; Schuhmacher, A.J.; Huse, J.T.; Holland, E.C.; Sutton, J.C.; Joyce, J.A. The tumor microenvironment underlies acquired resistance to CSF-1R inhibition in gliomas. Science 2016, 352, aad3018. [CrossRef] [PubMed]
133. Quail, D.F.; Joyce, J.A. Molecular Pathways: Deciphering Mechanisms of Resistance to Macrophage-Targeted Therapies. Clin. Cancer Res. 2017, 23, 876–884. [CrossRef] [PubMed]
134. Couzin-Frankel, J. Breakthrough of the year 2013. Cancer immunotherapy. Science 2013, 342, 1432–1433. [CrossRef] [PubMed]
135. Farkona, S.; Diamandis, E.P.; Blasutig, I.M. Cancer immunotherapy: The beginning of the end of cancer? BMC Med. 2016, 14, 73. [CrossRef] [PubMed]
136. Liu, K.G.; Gupta, S.; Goel, S. Immunotherapy: Incorporation in the evolving paradigm of renal cancer management and future prospects. Oncotarget 2017, 8, 17313–17327. [CrossRef] [PubMed]
137. Thallinger, C.; Fureder, T.; Preusser, M.; Heller, G.; Mullauer, L.; Holler, C.; Prosch, H.; Frank, N.; Swierzewski, R.; Berger, W. et al. Review of cancer treatment with immune checkpoint inhibitors: Current concepts, expectations, limitations and pitfalls. Wien. Klin. Wochenschr. 2017, 1–7. [CrossRef] [PubMed]
138. Restifo, N.P.; Smyth, M.J.; Snyder, A. Acquired resistance to immunotherapy and future challenges. Nat. Rev. Cancer 2016, 16, 121–126. [CrossRef] [PubMed]
139. Zaretsky, J.M.; Garcia-Diaz, A.; Shin, D.S.; Escuin-Ordinas, H.; Hugo, W.; Hu-Lieskovan, S.; Torrejon, D.Y.; Abril-Rodriguez, G.; Sandoval, S.; Barthly, L. et al. Mutations Associated with Acquired Resistance to PD-1 Blockade in Melanoma. N. Engl. J. Med. 2016, 375, 819–829. [CrossRef] [PubMed]
140. Huang, B.; Zhang, H.; Gu, L.; Ye, B.; Jian, Z.; Stary, C.; Xiong, X. Advances in Immunotherapy for Glioblastoma Multiforme. J. Immunol. Res. 2017, 2017, 3597613. [CrossRef] [PubMed]
141. Guo, A.M.; Sheng, J.; Scicli, G.M.; Arbab, A.S.; Lehman, N.L.; Edwards, P.A.; Falck, J.R.; Roman, R.J.; Scicli, A.G. Expression of CYP4A1 in U251 human glioma cell induces hyperproliferative phenotype in vitro and rapidly growing tumors in vivo. J. Pharmacol. Exp. Ther. 2008, 327, 10–19. [CrossRef] [PubMed]
142. Guo, M.; Roman, R.J.; Fenstermacher, J.D.; Brown, S.L.; Falck, J.R.; Arbab, A.S.; Edwards, P.A.; Scicli, A.G. 9L gliosarcoma cell proliferation and tumor growth in rats are suppressed by N-hydroxy-N’-(4-butyl-2-methylphenol) formamidine (HET0016), a selective inhibitor of CYP4A. J. Pharmacol. Exp. Ther. 2006, 317, 97–108. [CrossRef] [PubMed]
143. Shankar, A.; Borin, T.F.; Iskander, A.; Varma, N.R.; Achyut, B.R.; Jain, M.; Mikkelsen, T.; Guo, A.M.; Chwang, W.B.; Ewing, J.R. et al. Combination of vatalanib and a 20-HETE synthesis inhibitor results in decreased tumor growth in an animal model of human glioma. OncoTargets Ther. 2016, 9, 1205–1219.
144. Borin, T.F.; Shankar, A.; Angara, K.; Rashid, M.H.; Jain, M.; Iskander, A.; Ara, R.; Lebedyeva, I.; Korkaya, H.; Achyut, B.R. et al. HET0016 decreases lung metastasis from breast cancer in immune-competent mouse model. PLoS ONE 2017, 12, e0178830. [CrossRef] [PubMed]
145. Guo, A.M.; Janic, B.; Sheng, J.; Falck, J.R.; Roman, R.J.; Edwards, P.A.; Arbab, A.S.; Scicli, A.G. The cytochrome P450 4A/F-20-hydroxyeicosatetraenoic acid system: A regulator of endothelial precursor cells derived from human umbilical cord blood. J. Pharmacol. Exp. Ther. 2011, 338, 421–429. [CrossRef] [PubMed]
146. Jain, M.; Gamage, N.H.; Alsulami, M.; Shankar, A.; Achyut, B.R.; Angara, K.; Rashid, M.H.; Iskander, A.; Borin, T.F.; Wenbo, Z. et al. Intravenous Formulation of HET0016 Decreased Human Glioblastoma Growth and Implicated Survival Benefit in Rat Xenograft Models. Sci. Rep. 2017, 7, 41809. [CrossRef] [PubMed]
147. Achyut, B.R.; Bader, D.A.; Robles, A.I.; Wangsa, D.; Harris, C.C.; Ried, T.; Yang, L. Inflammation-mediated genetic and epigenetic alterations drive cancer development in the neighboring epithelium upon stromal abrogation of TGF-beta signaling. PLoS Genet. 2013, 9, e1003251. [CrossRef] [PubMed]
148. Dondossola, E.; Rangel, R.; Guzman-Rojas, L.; Barbu, E.M.; Hosoya, H.; St John, L.S.; Molldrem, J.J.; Corti, A.; Sidman, R.L.; Arap, W. et al. CD13-positive bone marrow-derived myeloid cells promote angiogenesis, tumor growth, and metastasis. Proc. Natl. Acad. Sci. USA 2013, 110, 20717–20722. [CrossRef] [PubMed]
149. Seton-Rogers, S. Tumour microenvironment: Means of resistance. Nat. Rev. Cancer 2013, 13, 607. [CrossRef] [PubMed]
150. Wang, C.; Li, Y.; Chen, H.; Zhang, J.; Zhang, J.; Qin, T.; Duan, C.; Chen, X.; Liu, Y.; Zhou, X. et al. Inhibition of CYP4A by a novel flavonoid FLA-16 prolongs survival and normalizes tumor vasculature in glioma. Cancer Lett. 2017, 402, 131–141. [CrossRef] [PubMed]
151. Chen, X.W.; Yu, T.J.; Zhang, J.; Li, Y.; Chen, H.L.; Yang, G.F.; Yu, W.; Liu, Y.Z.; Liu, X.X.; Duan, C.F. et al. CYP4A in tumor-associated macrophages promotes pre-metastatic niche formation and metastasis. Oncogene 2017, 36, 5045–5057. [CrossRef] [PubMed]
152. Borin, T.F.A.K.; Rashid, M.H.; Achyut, B.R.; Arbab, A.S. Arachidonic Acid Metabolite as a Novel Therapeutic Target in Breast Cancer Metastasis. Int. J. Mol. Sci. 2017, 18, 2661. [CrossRef]
153. Acharyya, S.; Oskarsson, T.; Vanharanta, S.; Malladi, S.; Kim, J.; Morris, P.G.; Manova-Todorova, K.; Leversha, M.; Hogg, N.; Seshan, V.E. et al. A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell 2012, 150, 165–178. [CrossRef] [PubMed]
154. Fakhrejahani, E.; Toi, M. Antiangiogenesis therapy for breast cancer: An update and perspectives from clinical trials. Jpn. J. Clin. Oncol. 2014, 44, 197–207. [CrossRef] [PubMed]
155. Arbab, A.S. Activation of alternative pathways of angiogenesis and involvement of stem cells following anti-angiogenesis treatment in glioma. Histol. Histopathol. 2012, 27, 549–557. [PubMed]
156. Polivka, J., Jr.; Polivka, J.; Holubec, L.; Kubikova, T.; Priban, V.; Hes, O.; Pivovarcikova, K.; Treskova, I. Advances in Experimental Targeted Therapy and Immunotherapy for Patients with Glioblastoma Multiforme. Anticancer Res. 2017, 37, 21–33. [CrossRef] [PubMed]
157. Lenting, K.; Verhaak, R.; Ter Laan, M.; Wesseling, P.; Leenders, W. Glioma: Experimental models and reality. Acta Neuropathol. 2017, 133, 263–282. [CrossRef] [PubMed]
158. Chen, L.; Zhang, Y.; Yang, J.; Hagan, J.P.; Li, M. Vertebrate animal models of glioma: Understanding the mechanisms and developing new therapies. Biochim. Biophys. Acta 2013, 1836, 158–165. [CrossRef] [PubMed]
159. Ben-David, U.; Ha, G.; Tseng, Y.Y.; Greenwald, N.F.; Oh, C.; Shih, J.; McFarland, J.M.; Wong, B.; Boehm, J.S.; Beroukhim, R. et al. Patient-derived xenografts undergo mouse-specific tumor evolution. Nat. Genet. 2017, 49, 1567–1575. [CrossRef] [PubMed]