Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice

Journal of Clinical Investigation

Volumn 120, Issue 3, 2010, Pages 694-705

  Kioi, Mitomu ^a   Vogel, Hannes ^a   Schultz, Geoffrey ^a   Hoffman, Robert M ^b,c   Harsh, Griffith R ^a   Brown, J Martin ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ANTICANCER INC   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CHEMOKINE RECEPTOR CXCR4; HYPOXIA INDUCIBLE FACTOR 1; NEUTRALIZING ANTIBODY; PLERIXAFOR; STROMAL CELL DERIVED FACTOR 1;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CANCER RADIOTHERAPY; CELL SURVIVAL; CONTROLLED STUDY; GLIOBLASTOMA; HUMAN; HUMAN CELL; INTRACRANIAL TUMOR; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RADIATION DOSE; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR RECURRENCE; TUMOR VASCULARIZATION; VASCULARIZATION; XENOGRAFT;

ANIMALS; ANTI-HIV AGENTS; ANTIBODIES, NEUTRALIZING; ANTIGENS, CD11B; ANTINEOPLASTIC AGENTS; BONE MARROW CELLS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOKINE CXCL12; GLIOBLASTOMA; HETEROCYCLIC COMPOUNDS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; MICE; MICE, NUDE; MONOCYTES; NEOPLASM RECURRENCE, LOCAL; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; RECEPTORS, CXCR4; TRANSPLANTATION, HETEROLOGOUS; WHOLE-BODY IRRADIATION;

EID: 77949697909     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI40283     Document Type: Article

References (56)

1. Souhami L, et al. Randomized comparison of stereotactic radiosurgery followed by conventional radiotherapy with carmustine to conventional radiotherapy with carmustine for patients with glioblastoma multiforme: report of Radiation Therapy Oncology Group 93-05 protocol. Int J Radiat Oncol Biol Phys. 2004;60(3):853-860.
2. Hochberg FH, Pruitt A. Assumptions in the radiotherapy of glioblastoma. Neurology. 1980;30(9):907-911.
3. Liang BC, Thornton AF Jr, Sandler HM, Greenberg HS. Malignant astrocytomas: focal tumor recurrence after focal external beam radiation therapy. J Neurosurg. 1991;75(4):559-563.
4. Sneed PK, et al. Patterns of recurrence of glioblastoma multiforme after external irradiation followed by implant boost. Int J Radiat Oncol Biol Phys. 1994;29(4):719-727.
5. Garcia-Barros M, et al. Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science. 2003;300(5622):1155-1159.
6. Ogawa K, Boucher Y, Kashiwagi S, Fukumura D, Chen D, Gerweck LE. Influence of tumor cell and stroma sensitivity on tumor response to radiation. Cancer Res. 2007;67(9):4016-4021.
7. Ceradini DJ, et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med. 2004;10(8):858-864.
8. Takahashi T, et al. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med. 1999;5(4):434-438.
9. Rafii S, Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med. 2003;9(6):702-712.
10. Orlic D, et al. Bone marrow cells regenerate infarcted myocardium. Nature. 2001;410(6829):701-705.
11. Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420(6917):860-867.
12. Condeelis J, Pollard JW. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell. 2006;124(2):263-266.
13. Erler JT, et al. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell. 2009; 15(1):35-44.
14. Lyden D, et al. Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature. 1999;401(6754):670-677.
15. Lyden D, et al. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med. 2001;7(11):1194-1201.
16. Gothert JR, et al. Genetically tagging endothelial cells in vivo: bone marrow-derived cells do not contribute to tumor endothelium. Blood. 2004; 104(6):1769-1777.
17. De Palma M, Venneri MA, Roca C, Naldini L. Targeting exogenous genes to tumor angiogenesis by transplantation of genetically modified hematopoietic stem cells. Nat Med. 2003;9(6):789-795.
18. Moldovan NI, Goldschmidt-Clermont PJ, Parker-Thornburg J, Shapiro SD, Kolattukudy PE. Contribution of monocytes/macrophages to compensatory neovascularization: the drilling of metalloelastase-positive tunnels in ischemic myocardium. Circ Res. 2000;87(5):378-384.
19. Capoccia BJ, Shepherd RM, Link DC. G-CSF and AMD3100 mobilize monocytes into the blood that stimulate angiogenesis in vivo through a paracrine mechanism. Blood. 2006;108(7):2438-2445.
20. Bailey AS, et al. Myeloid lineage progenitors give rise to vascular endothelium. Proc Natl Acad Sci U S A. 2006;103(35):13156-13161.
21. Ruzinova MB, et al. Effect of angiogenesis inhibition by Id loss and the contribution of bone-marrow-derived endothelial cells in spontaneous murine tumors. Cancer Cell. 2003;4(4):277-289.
22. Ahn GO, Brown JM. Matrix metalloproteinase-9 is required for tumor vasculogenesis but not for angiogenesis: role of bone marrow-derived myelomonocytic cells. Cancer Cell. 2008;13(3):193-205.
23. Bertout JA, Patel SA, Simon MC. The impact of O2 availability on human cancer. Nat Rev Cancer. 2008;8(12):967-975.
24. Du R, et al. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell. 2008;13(3):206-220.
25. Sasai K, Brown JM. Discrepancies between measured changes of radiobiological hypoxic fraction and oxygen tension monitoring using two assay systems. Int J Radiat Oncol Biol Phys. 1994;30(2):355-361.
26. Zips D, et al. Impact of the tumour bed effect on microenvironment, radiobiological hypoxia and the outcome of fractionated radiotherapy of human FaDu squamous-cell carcinoma growing in the nude mouse. Int J Radiat Biol. 2001;77(12):1185-1193.
27. Rofstad EK, Mathiesen B, Henriksen K, Kindem K, Galappathi K. The tumor bed effect: increased metastatic dissemination from hypoxia-induced up-regulation of metastasis-promoting gene products. Cancer Res. 2005;65(6):2387-2396.
28. Moeller BJ, Cao Y, Li CY, Dewhirst MW. Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell. 2004;5(5):429-441.
29. Wang Y, Haider H, Ahmad N, Zhang D, Ashraf M. Evidence for ischemia induced host-derived bone marrow cell mobilization into cardiac allografts. J Mol Cell Cardiol. 2006;41(3):478-487.
30. Jin DK, et al. Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4+ hemangiocytes. Nat Med. 2006; 12(5):557-567.
31. Aghi M, Cohen KS, Klein RJ, Scadden DT, Chiocca EA. Tumor stromal-derived factor-1 recruits vascular progenitors to mitotic neovasculature, where microenvironment influences their differentiated phenotypes. Cancer Res. 2006;66(18):9054-9064.
32. Grunewald M, et al. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell. 2006;124(1):175-189.
33. Gerlach LO, Skerlj RT, Bridger GJ, Schwartz TW. Molecular interactions of cyclam and bicyclam nonpeptide antagonists with the CXCR4 chemokine receptor. J Biol Chem. 2001;276(17):14153-14160.
34. Yang M, Reynoso J, Jiang P, Li L, Moossa AR, Hoffman RM. Transgenic nude mouse with ubiquitous green fluorescent protein expression as a host for human tumors. Cancer Res. 2004;64(23):8651-8656.
35. De Palma M, et al. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell. 2005;8(3):211-226.
36. Jodele S, et al. The contribution of bone marrow-derived cells to the tumor vasculature in neuroblastoma is matrix metalloproteinase-9 dependent. Cancer Res. 2005;65(8):3200-3208.
37. Song S, Ewald AJ, Stallcup W, Werb Z, Bergers G. PDGFRbeta+ perivascular progenitor cells in tumours regulate pericyte differentiation and vascular survival. Nat Cell Biol. 2005;7(9):870-879.
38. Bussink J, Kaanders JH, Rijken PF, Raleigh JA, Van der Kogel AJ. Changes in blood perfusion and hypoxia after irradiation of a human squamous cell carcinoma xenograft tumor line. Radiat Res. 2000; 153(4):398-404.
39. Harada H, Kizaka-Kondoh S, Hiraoka M. Optical imaging of tumor hypoxia and evaluation of efficacy of a hypoxia-targeting drug in living animals. Mol Imaging. 2005;4(3):182-193.
40. Chau NM, et al. Identification of novel small molecule inhibitors of hypoxia-inducible factor-1 that differentially block hypoxia-inducible factor-1 activity and hypoxia-inducible factor-1alpha induction in response to hypoxic stress and growth factors. Cancer Res. 2005;65(11):4918-4928.
41. Palmowski M, et al. Vessel fractions in tumor xenografts depicted by flow- or contrast-sensitive three-dimensional high-frequency Doppler ultrasound respond differently to antiangiogenic treatment. Cancer Res. 2008;68(17):7042-7049.
42. Heissig B, et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell. 2002; 109(5):625-637.
43. Hattori K, et al. Plasma elevation of stromal cell-derived factor-1 induces mobilization of mature and immature hematopoietic progenitor and stem cells. Blood. 2001;97(11):3354-3360.
44. Ishizaka S, Kuriyama S, Tsujii T. In vivo depletion of macrophages by desulfated iota-carrageenan in mice. J Immunol Methods. 1989;124(1):17-24.
45. Prionas SD, Kowalski J, Fajardo LF, Kaplan I, Kwan HH, Allison AC. Effects of X irradiation on angiogenesis. Radiat Res. 1990;124(1):43-49.
46. Broxmeyer HE, et al. Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med. 2005;201(8):1307-1318.
47. Rubin JB, et al. A small-molecule antagonist of CXCR4 inhibits intracranial growth of primary brain tumors. Proc Natl Acad Sci U S A. 2003; 100(23):13513-13518.
48. Bronte V, et al. Identification of a CD11b(+)/Gr-1(+)/CD31(+) myeloid progenitor capable of activating or suppressing CD8(+) T cells. Blood. 2000; 96(12):3838-3846.
49. Almand B, et al. Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J Immunol. 2001; 166(1):678-689.
50. Pollard JW. Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer. 2004;4(1):71-78.
51. Shojaei F, et al. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b(+)Gr1(+) myeloid cells. Nat Biotechnol. 2007;25(8):911-920.
52. Pucci F, et al. 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(4):901-914.
53. Bergers G, Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer. 2008; 8(8):592-603.
54. Paez-Ribes M, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell. 2009; 15(3):220-231.
55. Kawakami K, Kioi M, Liu Q, Kawakami M, Puri RK. Evidence that IL-13R alpha2 chain in human glioma cells is responsible for the antitumor activity mediated by receptor-directed cytotoxin therapy. J Immunother. 2005;28(3):193-202.
56. Rockwell P, Neufeld G, Glassman A, Caron D, Goldstein NI. In vitro neutralization of vascular endothelial growth factor activation of Flk-1 by a monoclonal antibody. Mol Cell Differ. 1995;3(1):91-109.