Targeting Hypoxia-Inducible Factor 1α in a New Orthotopic Model of Glioblastoma Recapitulating the Hypoxic Tumor Microenvironment

Journal of Neuropathology and Experimental Neurology

Volumn 74, Issue 7, 2015, Pages 710-722

  Nigim, Fares ^a   Cavanaugh, Jill ^a   Patel, Anoop P ^a   Curry, William T ^a   Esaki, Shin Ichi ^a   Kasper, Ekkehard M ^b   Chi, Andrew S ^c   Louis, David N ^a   Martuza, Robert L ^a   Rabkin, Samuel D ^a   Wakimoto, Hiroaki ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

Author keywords

Glioblastoma; Glioblastoma stem cells; Hypoxia; Hypoxia inducible factor 1 (HIF 1 ); Molecular targeted therapy; Necrosis; Orthotopic xenograft model

Indexed keywords

CD34 ANTIGEN; DIGOXIN; HERMES ANTIGEN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; KI 67 ANTIGEN; TRANSCRIPTION FACTOR SOX2; VASCULOTROPIN; ENZYME INHIBITOR; LEUKOCYTE ANTIGEN; SOX2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; CELL SURVIVAL; CONTROLLED STUDY; GLIOBLASTOMA; HUMAN; HUMAN CELL; HYPOXIC CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOLECULARLY TARGETED THERAPY; MOUSE; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR MICROENVIRONMENT; TUMOR MODEL; ANIMAL; BRAIN TUMOR; CELL HYPOXIA; COHORT ANALYSIS; DISEASE MODEL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MIDDLE AGED; PHYSIOLOGY; SCID MOUSE; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD; BRAIN NEOPLASMS; CELL HYPOXIA; CELL LINE, TUMOR; COHORT STUDIES; DIGOXIN; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; KI-67 ANTIGEN; MICE; MICE, SCID; MIDDLE AGED; SOXB1 TRANSCRIPTION FACTORS; TUMOR MICROENVIRONMENT; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84934343090     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0000000000000210     Document Type: Article

References (60)

1. Porter KR, McCarthy BJ, Freels S, et al. Prevalence estimates for primary brain tumors in the United States by age, gender, behavior, and histology. Neuro Oncol 2010;12:520-7
2. Wen PY, Kesari S. Malignant gliomas in adults. New Engl J Med 2008;359:492-507
3. Raza SM, Lang FF, Aggarwal BB, et al. Necrosis and glioblastoma: a friend or a foe? A review and a hypothesis. Neurosurgery 2002;51:2-12; discussion -3
4. Rong Y, Durden DL, Van Meir EG, et al. 'Pseudopalisading' necrosis in glioblastoma: a familiar morphologic feature that links vascular pathology, hypoxia, and angiogenesis. J Neuropathol Exp Neurol 2006;65:529-39
5. Homma T, Fukushima T, Vaccarella S, et al. Correlation among pathology, genotype, and patient outcomes in glioblastoma. J Neuropathol Exp Neurol 2006;65:846-54
6. Nelson JS, Tsukada Y, Schoenfeld D, et al. Necrosis as a prognostic criterion in malignant supratentorial, astrocytic gliomas. Cancer 1983;52:550-4
7. Sathornsumetee S, Cao Y, Marcello JE, et al. Tumor angiogenic and hypoxic profiles predict radiographic response and survival in malignant astrocytoma patients treated with bevacizumab and irinotecan. J Clin Oncol 2008;26:271-8
8. Amberger-Murphy V. Hypoxia helps glioma to fight therapy. Curr Cancer Drug Targets 2009;9:381-90
9. Fischer I, Gagner JP, Law M, et al. Angiogenesis in gliomas: biology and molecular pathophysiology. Brain Pathol 2005;15:297-310
10. Jensen RL. Hypoxia in the tumorigenesis of gliomas and as a potential target for therapeutic measures. Neurosurg Focus 2006;20:E24
11. Kaur B, Khwaja FW, Severson EA, et al. Hypoxia and the hypoxia-inducible-factor pathway in glioma growth and angiogenesis. Neuro Oncol 2005;7:134-53
12. Keith B, Simon MC. Hypoxia-inducible factors, stem cells, and cancer. Cell 2007;129:465-72
13. Vaupel P. Hypoxia and aggressive tumor phenotype: implications for therapy and prognosis. Oncologist 2008;13(Suppl 3):21-6
14. Yang L, Lin C, Wang L, et al. Hypoxia and hypoxia-inducible factors in glioblastoma multiforme progression and therapeutic implications. Exp Cell Res 2012;318:2417-26
15. Harris AL. Hypoxia - a key regulatory factor in tumour growth. Nat Rev Cancer 2002;2:38-47
16. Semenza GL. Hypoxia, clonal selection, and the role of HIF-1 in tumor progression. Crit Rev Biochem Mol Biol 2000;35:71-103
17. Vaupel P, Mayer A. Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev 2007;26:225-39
18. Bar EE, Lin A, Mahairaki V, et al. Hypoxia increases the expression of stem-cell markers and promotes clonogenicity in glioblastoma neurospheres. Am J Pathol 2010;177:1491-502
19. Heddleston JM, Li Z, McLendon RE, et al. The hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotype. Cell Cycle 2009;8:3274-84
20. Seidel S, Garvalov BK, Wirta V, et al. A hypoxic niche regulates glioblastoma stem cells through hypoxia inducible factor 2 alpha. Brain 2010;133:983-95
21. Soeda A, Park M, Lee D, et al. Hypoxia promotes expansion of the CD133-positive glioma stem cells through activation of HIF-1alpha. Oncogene 2009;28:3949-59
22. Sgubin D, Wakimoto H, Kanai R, et al. Oncolytic herpes simplex virus counteracts the hypoxia-induced modulation of glioblastoma stem-like cells. Stem Cells Trans Med 2012;1:322-32
23. Semenza GL. Hypoxia-inducible factors: mediators of cancer progression and targets for cancer therapy. Trends Pharm Sci 2012;33:207-14
24. Semenza GL. HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J Appl Physiol 2000;88:1474-80
25. Sondergaard KL, Hilton DA, Penney M, et al. Expression of hypoxia-inducible factor 1alpha in tumours of patients with glioblastoma. Neuropathol Appl Neurobiol 2002;28:210-7
26. Zagzag D, Zhong H, Scalzitti JM, et al. Expression of hypoxia-inducible factor 1alpha in brain tumors: association with angiogenesis, invasion, and progression. Cancer 2000;88:2606-18
27. Korkolopoulou P, Patsouris E, Konstantinidou AE, et al. Hypoxia-inducible factor 1alpha/vascular endothelial growth factor axis in astrocytomas. Associations with microvessel morphometry, proliferation and prognosis. Neuropathol Appl Neurobiol 2004;30:267-78
28. Chen L, Feng P, Li S, et al. Effect of hypoxia-inducible factor-1alpha silencing on the sensitivity of human brain glioma cells to doxorubicin and etoposide. Neurochem Res 2009;34:984-90
29. Newcomb EW, Lukyanov Y, Smirnova I, et al. Noscapine induces apoptosis in human glioma cells by an apoptosis-inducing factor-dependent pathway. Anticancer Drugs 2008;19:553-63
30. Fujiwara S, Nakagawa K, Harada H, et al. Silencing hypoxia-inducible factor-1alpha inhibits cell migration and invasion under hypoxic environment in malignant gliomas. Int J Oncol 2007;30:793-802
31. Keith B, Johnson RS, Simon MC. HIF1alpha and HIF2alpha: sibling rivalry in hypoxic tumour growth and progression. Nature Rev Cancer 2012;12:9-22
32. Chen L, Zhang Y, Yang J, et al. Vertebrate animal models of glioma: understanding the mechanisms and developing new therapies. Biochim Biophys Acta 2013;1836:158-65
33. Huszthy PC, Daphu I, Niclou SP, et al. In vivo models of primary brain tumors: pitfalls and perspectives. Neuro Oncol 2012;14:979-93
34. Wakimoto H, Kesari S, Farrell CJ, et al. Human glioblastoma-derived cancer stem cells: establishment of invasive glioma models and treatment with oncolytic herpes simplex virus vectors. Cancer Res 2009:693472-81
35. Wakimoto H, Mohapatra G, Kanai R, et al. Maintenance of primary tumor phenotype and genotype in glioblastoma stem cells. Neuro Oncol 2012;14:132-44
36. Giatromanolaki A, Koukourakis MI, Sivridis E, et al. Relation of hypoxia inducible factor 1 alpha and 2 alpha in operable non-small cell lung cancer to angiogenic/molecular profile of tumours and survival. Br J Cancer 2001;85:881-90
37. Enatsu S, Iwasaki A, Shirakusa T, et al. Expression of hypoxia-inducible factor-1 alpha and its prognostic significance in small-sized adenocarcinomas of the lung. Eur J Cardiothorac Surg 2006;29:891-5
38. Nakanishi K, Hiroi S, Tominaga S, et al. Expression of hypoxia-inducible factor-1alpha protein predicts survival in patients with transitional cell carcinoma of the upper urinary tract. Clini Cancer Res 2005;11:2583-90
39. Ban HS, Uto Y, Nakamura H. Hypoxia-inducible factor inhibitors: a survey of recent patented compounds (2004-2010). Expt Opin Ther Patents 2011;21:131-46
40. Koh MY, Spivak-Kroizman TR, Powis G. HIF-1alpha and cancer therapy. Recent Results Cancer Res 2010;180:15-34
41. Onnis B, Rapisarda A, Melillo G. Development of HIF-1 inhibitors for cancer therapy. J Cell Molec Med 2009;13:2780-6
42. Zhang H, Qian DZ, Tan YS, et al. Digoxin and other cardiac glycosides inhibit HIF-1alpha synthesis and block tumor growth. Proc Nat Acad Sci USA 2008;105:19579-86
43. Candolfi M, Curtin JF, Nichols WS, et al. Intracranial glioblastoma models in preclinical neuro-oncology: neuropathological characterization and tumor progression. J Neuro Oncol 2007;85:133-48
44. de Vries NA, Beijnen JH, van Tellingen O. High-grade glioma mouse models and their applicability for preclinical testing. Cancer Treatment Rev 2009;35:714-23
45. Radaelli E, Ceruti R, Patton V, et al. Immunohistopathological and neuroimaging characterization of murine orthotopic xenograft models of glioblastoma multiforme recapitulating the most salient features of human disease. Histol Histopathol 2009;24:879-91
46. Camphausen K, Purow B, Sproull M, et al. Orthotopic growth of human glioma cells quantitatively and qualitatively influences radiation-induced changes in gene expression. Cancer Res 2005;65:10389-93
47. Jacobs VL, Valdes PA, Hickey WF, et al. Current review of in vivo GBM rodent models: emphasis on the CNS-1 tumour model. ASN Neuro 2011;3:e00063
48. Gunther HS, Schmidt NO, Phillips HS, et al. Glioblastoma-derived stem cell-enriched cultures form distinct subgroups according to molecular and phenotypic criteria. Oncogene 2008;27:2897-909
49. Joo KM, Kim J, Jin J, et al. Patient-specific orthotopic glioblastoma xenograft models recapitulate the histopathology and biology of human glioblastomas in situ. Cell Rep 2013;3:260-73
50. Giannini C, Sarkaria JN, Saito A, et al. Patient tumor EGFR and PDGFRA gene amplifications retained in an invasive intracranial xenograft model of glioblastoma multiforme. Neuro Oncol 2005;7:164-76
51. Semenza GL. HIF-1 mediates metabolic responses to intratumoral hypoxia and oncogenic mutations. J Clin Invest 2013;123:3664-71
52. Dong S, Nutt CL, Betensky RA, et al. Histology-based expression profiling yields novel prognostic markers in human glioblastoma. J Neuropathol Exp Neurol 2005;64:948-55
53. Vaupel P, Mayer A. The clinical importance of assessing tumor hypoxia: relationship of tumor hypoxia to prognosis and therapeutic opportunities. Antioxid Redox Signal 2015;22:878-80
54. Isaacs JS, Jung YJ, Mimnaugh EG, et al. Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1 alpha-degradative pathway. J Biol Chem 2002;277:29936-44
55. Mabjeesh NJ, Post DE, Willard MT, et al. Geldanamycin induces degradation of hypoxia-inducible factor 1alpha protein via the proteosome pathway in prostate cancer cells. Cancer Res 2002;62:2478-82
56. Kong D, Park EJ, Stephen AG, et al. Echinomycin, a small-molecule inhibitor of hypoxia-inducible factor-1 DNA-binding activity. Cancer Research 2005;65:9047-55
57. Van Dyke MM, Dervan PB. Echinomycin binding sites on DNA. Science 1984;225:1122-7
58. Yeo EJ, Chun YS, Cho YS, et al. YC-1: a potential anticancer drug targeting hypoxia-inducible factor 1. J Nat Cancer Inst 2003;95:516-25
59. Newcomb EW, Ali MA, Schnee T, et al. Flavopiridol downregulates hypoxia-mediated hypoxia-inducible factor-1alpha expression in human glioma cells by a proteasome-independent pathway: implications for in vivo therapy. Neuro Oncol 2005;7:225-35
60. Chou CW, Wang CC, Wu CP, et al. Tumor cycling hypoxia induces chemoresistance in glioblastoma multiforme by upregulating the expression and function of ABCB1. Neuro Oncol 2012;14:1227-38