Anti-vascular endothelial growth factor therapy-induced glioma invasion is associated with accumulation of Tie2-expressing monocytes

Oncotarget

Volumn 5, Issue 8, 2014, Pages 2208-2220

  Gabrusiewicz, Konrad ^a   Liu, Dan ^a   Cortes Santiago, Nahir ^a   Hossain, Mohammad B ^a   Conrad, Charles A ^a   Aldape, Kenneth D ^a   Fuller, Gregory N ^a   Marini, Frank C ^b   Alonso, Marta M ^c   Idoate, Miguel Angel ^c   Gilbert, Mark R ^a   Fueyo, Juan ^a   Gomez Manzano, Candelaria ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

^c Universidad Pública de Navarra   (Spain)

Author keywords

Antiangiogenesis; Brain tumors; Monocyte; Tie2; Tumor microenvironment

Indexed keywords

AFLIBERCEPT; ANGIOPOIETIN RECEPTOR; BEVACIZUMAB; GELATINASE B; TEMOZOLOMIDE; VASCULOTROPIN; ANGIOGENESIS INHIBITOR; MONOCLONAL ANTIBODY; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC THERAPY; ARTICLE; CANCER RECURRENCE; CELL FUNCTION; CELL POPULATION; CONTROLLED STUDY; GLIOBLASTOMA; GLIOMA; GLIOMA CELL; HUMAN; HUMAN CELL; MACROPHAGE; MONOCYTE; MOUSE; NONHUMAN; PROTEIN BLOOD LEVEL; TUMOR INVASION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; BRAIN NEOPLASMS; CONFOCAL MICROSCOPY; DRUG RESISTANCE; DRUG SCREENING; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOHISTOCHEMISTRY; METABOLISM; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; TUMOR RECURRENCE;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; BRAIN NEOPLASMS; DRUG RESISTANCE, NEOPLASM; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GLIOMA; HUMANS; IMMUNOHISTOCHEMISTRY; MATRIX METALLOPROTEINASE 9; MICE; MICE, NUDE; MICROSCOPY, CONFOCAL; MONOCYTES; NEOPLASM INVASIVENESS; NEOPLASM RECURRENCE, LOCAL; RECEPTOR, TIE-2; VASCULAR ENDOTHELIAL GROWTH FACTOR A; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84899554487     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.1893     Document Type: Article

References (42)

1. Dolecek TA, Propp JM, Stroup NE and 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:v1-49.
2. Van Meir EG, Hadjipanayis CG, Norden AD, Shu HK, Wen PY and Olson JJ. Exciting new advances in neurooncology: the avenue to a cure for malignant glioma. CA Cancer J Clin 2010; 60:166-193.
3. Wen PY and Kesari S. Malignant gliomas in adults. N Engl J Med 2008; 359:492-507.
4. Kreisl TN, Kim L, Moore K, Duic P, Royce C, Stroud I, Garren N, Mackey M, Butman JA, Camphausen K, Park J, Albert PS and Fine HA. Phase II trial of single-agent bevacizumab followed by bevacizumab plus irinotecan at tumor progression in recurrent glioblastoma. J Clin Oncol 2009; 27:740-745.
5. Friedman HS, Prados MD, Wen PY, Mikkelsen T, Schiff D, Abrey LE, Yung WK, Paleologos N, Nicholas MK, Jensen R, Vredenburgh J, Huang J, Zheng M and Cloughesy T. Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J Clin Oncol 2009; 27:4733-4740.
6. Kleihues P, Cavenee WK and International Agency for Research on Cancer. (2000). Pathology and genetics of tumours of the nervous system. (Lyon: IARC Press).
7. Jain RK, di Tomaso E, Duda DG, Loeffler JS, Sorensen AG and Batchelor TT. Angiogenesis in brain tumours. Nat Rev Neurosci 2007; 8:610-622.
8. Plate KH, Breier G, Millauer B, Ullrich A and Risau W. Up-regulation of vascular endothelial growth factor and its cognate receptors in a rat glioma model of tumor angiogenesis. Cancer Res 1993; 53:5822-5827.
9. Plate KH, Scholz A and Dumont DJ. Tumor angiogenesis and anti-angiogenic therapy in malignant gliomas revisited. Acta Neuropathol 2012; 124:763-775.
10. Chinot OL, Wick W, Mason W, Henriksson R, Saran F, Nishikawa R, Carpentier AF, Hoang-Xuan K, Kavan P, Cernea D, Brandes AA, Hilton M, Abrey L and Cloughesy T. Bevacizumab plus radiotherapy-temozolomide for newlydiagnosed glioblastoma. N Engl J Med 2014; 370:709-722.
11. Gilbert MR, Dignam JJ, Armstrong TS, Wefel JS, Blumenthal DT, Vogelbaum MA, Colman H, Chakravarti A, Pugh S, Won M, Jeraj R, Brown PD, Jaeckle KA, Schiff D, Stieber VW, Brachman DG, et al. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med 2014; 370:699-708.
12. de Groot JF, Fuller G, Kumar AJ, Piao Y, Eterovic K, Ji Y and Conrad CA. Tumor invasion after treatment of glioblastoma with bevacizumab: radiographic and pathologic correlation in humans and mice. Neuro Oncol 2010; 12:233-242.
13. Keunen O, Johansson M, Oudin A, Sanzey M, Rahim SA, Fack F, Thorsen F, Taxt T, Bartos M, Jirik R, Miletic H, Wang J, Stieber D, Stuhr L, Moen I, Rygh CB, et al. Anti-VEGF treatment reduces blood supply and increases tumor cell invasion in glioblastoma. Proc Natl Acad Sci U S A 2011; 108:3749-3754.
14. Narayana A, Gruber D, Kunnakkat S, Golfinos JG, Parker E, Raza S, Zagzag D, Eagan P and Gruber ML. A clinical trial of bevacizumab, temozolomide, and radiation for newly diagnosed glioblastoma. J Neurosurg 2012; 116:341-345.
15. Norden AD, Young GS, Setayesh K, Muzikansky A, Klufas R, Ross GL, Ciampa AS, Ebbeling LG, Levy B, Drappatz J, Kesari S and Wen PY. Bevacizumab for recurrent malignant gliomas: efficacy, toxicity, and patterns of recurrence. Neurology 2008; 70:779-787.
16. Paez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Vinals F, Inoue M, Bergers G, Hanahan D and Casanovas O. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009; 15:220-231.
17. Shojaei F, Wu X, Malik AK, Zhong C, Baldwin ME, Schanz S, Fuh G, Gerber HP and Ferrara N. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells. Nat Biotechnol 2007; 25:911-920.
18. de Groot JF, Piao Y, Tran H, Gilbert M, Wu HK, Liu J, Bekele BN, Cloughesy T, Mehta M, Robins HI, Lassman A, DeAngelis L, Camphausen K, Chen A, Yung WK, Prados M, et al. Myeloid biomarkers associated with glioblastoma response to anti-VEGF therapy with aflibercept. Clin Cancer Res 2011; 17:4872-4881.
19. di Tomaso E, Snuderl M, Kamoun WS, Duda DG, Auluck PK, Fazlollahi L, Andronesi OC, Frosch MP, Wen PY, Plotkin SR, Hedley-Whyte ET, Sorensen AG, Batchelor TT and Jain RK. Glioblastoma recurrence after cediranib therapy in patients: lack of "rebound" revascularization as mode of escape. Cancer Res 2011; 71:19-28.
20. Lu-Emerson C, Snuderl M, Kirkpatrick ND, Goveia J, Davidson C, Huang Y, Riedemann L, Taylor J, Ivy P, Duda DG, Ancukiewicz M, Plotkin SR, Chi AS, Gerstner ER, Eichler AF, Dietrich J, 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.
21. De Palma M, Venneri MA, Galli R, Sergi Sergi L, Politi LS, Sampaolesi M and Naldini L. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 2005; 8:211-226.
22. Pucci F, Venneri MA, Biziato D, Nonis A, Moi D, Sica A, Di Serio C, Naldini L and De Palma M. A distinguishing gene signature shared by tumor-infiltrating Tie2-expressing monocytes, blood "resident" monocytes, and embryonic macrophages suggests common functions and developmental relationships. Blood 2009; 114:901-914.
23. Venneri MA, De Palma M, Ponzoni M, Pucci F, Scielzo C, Zonari E, Mazzieri R, Doglioni C and Naldini L. Identification of proangiogenic TIE2-expressing monocytes (TEMs) in human peripheral blood and cancer. Blood 2007; 109:5276-5285.
24. De Palma M, Murdoch C, Venneri MA, Naldini L and Lewis CE. Tie2-expressing monocytes: regulation of tumor angiogenesis and therapeutic implications. Trends Immunol 2007; 28:519-524.
25. Gomez-Manzano C, Holash J, Fueyo J, Xu J, Conrad CA, Aldape KD, de Groot JF, Bekele BN and Yung WK. VEGF Trap induces antiglioma effect at different stages of disease. Neuro Oncol 2008; 10:940-945.
26. Lee OH, Fueyo J, Xu J, Yung WK, Lemoine MG, Lang FF, Bekele BN, Zhou X, Alonso MA, Aldape KD, Fuller GN and Gomez-Manzano C. Sustained angiopoietin-2 expression disrupts vessel formation and inhibits glioma growth. Neoplasia 2006; 8:419-428.
27. Ferrara N. Role of myeloid cells in vascular endothelial growth factor-independent tumor angiogenesis. Curr Opin Hematol 2010; 17:219-224.
28. Hao NB,Lu MH, Fan YH, Cao YL, Zhang ZR and Yang SM. Macrophages in tumor microenvironments and the progression of tumors. Clin Dev Immunol 2012; 2012:948098.
29. Coffelt SB, Tal AO, Scholz A, De Palma M, Patel S, Urbich C, Biswas SK, Murdoch C, Plate KH, Reiss Y and Lewis CE. Angiopoietin-2 regulates gene expression in TIE2-expressing monocytes and augments their inherent proangiogenic functions. Cancer Res 2010; 70:5270-5280.
30. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 2003; 3:23-35.
31. Tjiu JW, Chen JS, Shun CT, Lin SJ, Liao YH, Chu CY, Tsai TF, Chiu HC, Dai YS, Inoue H, Yang PC, Kuo ML and Jee SH. Tumor-associated macrophage-induced invasion and angiogenesis of human basal cell carcinoma cells by cyclooxygenase-2 induction. J Invest Dermatol 2009; 129:1016-1025.
32. Park EH, Lee JM, Blais JD, Bell JC and Pelletier J. Internal translation initiation mediated by the angiogenic factor Tie2. J Biol Chem 2005; 280:20945-20953.
33. Nakada M, Okada Y and Yamashita J. The role of matrix metalloproteinases in glioma invasion. Front Biosci 2003; 8:e261-269.
34. Bergers G and Hanahan D. Modes of resistance to antiangiogenic therapy. Nat Rev Cancer 2008; 8:592-603.
35. Jain RK and Carmeliet P. SnapShot: Tumor angiogenesis. Cell 2012; 149:1408-1408 e1401.
36. Zerrouqi A and Van Meir EG. A conspiracy of glioma and endothelial cells to invade the normal brain. Oncotarget 2011; 2:1-4.
37. Kunkel P, Ulbricht U, Bohlen P, Brockmann MA, Fillbrandt R, Stavrou D, Westphal M and Lamszus K. Inhibition of glioma angiogenesis and growth in vivo by systemic treatment with a monoclonal antibody against vascular endothelial growth factor receptor-2. Cancer Res 2001; 61:6624-6628.
38. Rubenstein JL, Kim J, Ozawa T, Zhang M, Westphal M, Deen DF and Shuman MA. Anti-VEGF antibody treatment of glioblastoma prolongs survival but results in increased vascular cooption. Neoplasia 2000; 2:306-314.
39. Mazzieri R, Pucci F, Moi D, Zonari E, Ranghetti A, Berti A, Politi LS, Gentner B, Brown JL, Naldini L and De Palma M. Targeting the ANG2/TIE2 axis inhibits tumor growth and metastasis by impairing angiogenesis and disabling rebounds of proangiogenic myeloid cells. Cancer Cell 2011; 19:512-526.
40. Murdoch C, Muthana M, Coffelt SB and Lewis CE. The role of myeloid cells in the promotion of tumour angiogenesis. Nat Rev Cancer 2008; 8:618-631.
41. Liu D, Martin V, Fueyo J, Lee OH, Xu J, Cortes-Santiago N, Alonso MM, Aldape K, Colman H and Gomez-Manzano C. Tie2/TEK modulates the interaction of glioma and brain tumor stem cells with endothelial cells and promotes an invasive phenotype. Oncotarget 2010; 1:700-709.
42. Repnik U, Knezevic M and Jeras M. Simple and costeffective isolation of monocytes from buffy coats. J Immunol Methods 2003; 278:283-292.