Hypoxia-induced autophagic response is associated with aggressive phenotype and elevated incidence of metastasis in orthotopic immunocompetent murine models of head and neck squamous cell carcinomas (HNSCC)

Experimental and Molecular Pathology

Volumn 90, Issue 2, 2011, Pages 215-225

  Vigneswaran, Nadarajah ^a   Wu, Jean ^a   Song, Anren ^a   Annapragada, Ananth ^a   Zacharias, Wolfgang ^b  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF LOUISVILLE SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Autophagy; Carbonic anhydrase IX; Head and neck squamous cell carcinoma; Hypoxia; Pimonidazole; Tumor model

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; BAGG ALBINO MOUSE; CANCER GROWTH; CANCER LOCALIZATION; CANCER MODEL; CELL STRAIN; CELL STRAIN B4B8; CELL STRAIN LY 2; CELL SURVIVAL; DISEASE ACTIVITY; GROWTH RATE; HEAD AND NECK CARCINOMA; HYPOXIA; IMMUNOCOMPETENCE; IN VITRO STUDY; INCIDENCE; METASTASIS POTENTIAL; MOUSE; NEWBORN; NONHUMAN; PHENOTYPE; SQUAMOUS CELL CARCINOMA;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CARCINOMA, SQUAMOUS CELL; CASPASE 3; CELL HYPOXIA; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; HEAD AND NECK NEOPLASMS; IMMUNOCOMPETENCE; IMMUNOHISTOCHEMISTRY; MICE; MOUTH NEOPLASMS; NEOPLASM METASTASIS; PHENOTYPE; UP-REGULATION;

MURINAE; MUS;

EID: 79251578964     PISSN: 00144800     EISSN: 10960945     Source Type: Journal    
DOI: 10.1016/j.yexmp.2010.11.011     Document Type: Article

References (85)

1. Aebersold D.M., et al. Expression of hypoxia-inducible factor-1alpha: a novel predictive and prognostic parameter in the radiotherapy of oropharyngeal cancer. Cancer Res. 2001, 61:2911-2916.
2. Azad M.B., et al. Hypoxia induces autophagic cell death in apoptosis-competent cells through a mechanism involving BNIP3. Autophagy 2008, 4:195-204.
3. Beasley N.J., et al. Carbonic anhydrase IX, an endogenous hypoxia marker, expression in head and neck squamous cell carcinoma and its relationship to hypoxia, necrosis, and microvessel density. Cancer Res. 2001, 61:5262-5267.
4. Bennewith K.L., et al. Orally administered pimonidazole to label hypoxic tumor cells. Cancer Res. 2002, 62:6827-6830.
5. Bozec A., et al. Combined effects of bevacizumab with erlotinib and irradiation: a preclinical study on a head and neck cancer orthotopic model. Br. J. Cancer 2008, 99:93-99.
6. Bristow R.G., Hill R.P. Hypoxia and metabolism. Hypoxia, DNA repair and genetic instability. Nat. Rev. Cancer 2008, 8:180-192.
7. Brizel D.M., et al. Tumor hypoxia adversely affects the prognosis of carcinoma of the head and neck. Int. J. Radiat. Oncol. Biol. Phys. 1997, 38:285-289.
8. Brown J.M., Giaccia A.J. The unique physiology of solid tumors: opportunities (and problems) for cancer therapy. Cancer Res. 1998, 58:1408-1416.
9. Bunn H.F., Poyton R.O. Oxygen sensing and molecular adaptation to hypoxia. Physiol. Rev. 1996, 76:839-885.
10. Cao X., et al. Glucose uptake inhibitor sensitizes cancer cells to daunorubicin and overcomes drug resistance in hypoxia. Cancer Chemother. Pharmacol. 2007, 59:495-505.
11. Cao Y., Klionsky D.J. Physiological functions of Atg6/Beclin 1: a unique autophagy-related protein. Cell Res. 2007, 17:839-849.
12. Capaccio P., et al. Cyclin D1 expression is predictive of occult metastases in head and neck cancer patients with clinically negative cervical lymph nodes. Head Neck 2000, 22:234-240.
13. Carmeliet P., et al. Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 1998, 394:485-490.
14. Chapman J.D., et al. Measuring hypoxia and predicting tumor radioresistance with nuclear medicine assays. Radiother. Oncol. 1998, 46:229-237.
15. Chaudary N., Hill R.P. Hypoxia and metastasis. Clin. Cancer Res. 2007, 13:1947-1949.
16. Chen Z., et al. Metastatic variants derived following in vivo tumor progression of an in vitro transformed squamous cell carcinoma line acquire a differential growth advantage requiring tumor-host interaction. Clin. Exp. Metastasis 1997, 15:527-537.
17. Cuisnier O., et al. Chronic hypoxia protects against gamma-irradiation-induced apoptosis by inducing bcl-2 up-regulation and inhibiting mitochondrial translocation and conformational change of bax protein. Int. J. Oncol. 2003, 23:1033-1041.
18. Dalby K.N., et al. Targeting the prodeath and prosurvival functions of autophagy as novel therapeutic strategies in cancer. Autophagy 2010, 6:322-329.
19. Day G.L., Blot W.J. Second primary tumors in patients with oral cancer. Cancer 1992, 70:14-19.
20. Dinesman A., et al. Development of a new in vivo model for head and neck cancer. Otolaryngol. Head Neck Surg. 1990, 103:766-774.
21. Eisbruch A., et al. Radiation concurrent with gemcitabine for locally advanced head and neck cancer: a phase I trial and intracellular drug incorporation study. J. Clin. Oncol. 2001, 19:792-799.
22. Eisenberg-Lerner A., et al. Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ. 2009, 16:966-975.
23. Evans S.M., et al. Detection of hypoxia in human squamous cell carcinoma by EF5 binding. Cancer Res. 2000, 60:2018-2024.
24. Forastiere A., et al. Head and neck cancer. N. Engl. J. Med. 2001, 345:1890-1900.
25. Fu K.K. Combined-modality therapy for head and neck cancer. Oncol. Huntingt 1997, 11:1781-1790. 1796; discussion 1796, 179.
26. Fu O.Y., et al. Cobalt chloride-induced hypoxia modulates the invasive potential and matrix metalloproteinases of primary and metastatic breast cancer cells. Anticancer Res. 2009, 29:3131-3138.
27. Goda N., et al. Hypoxia-inducible factor 1alpha is essential for cell cycle arrest during hypoxia. Mol. Cell. Biol. 2003, 23:359-369.
28. Goldberg M.A., Schneider T.J. Similarities between the oxygen-sensing mechanisms regulating the expression of vascular endothelial growth factor and erythropoietin. J. Biol. Chem. 1994, 269:4355-4359.
29. Haddad R.I., Shin D.M. Recent advances in head and neck cancer. N. Engl. J. Med. 2008, 359:1143-1154.
30. Harris A.L. Hypoxia-a key regulatory factor in tumour growth. Nat. Rev. Cancer 2002, 2:38-47.
31. Henson B., et al. An orthotopic floor-of-mouth model for locoregional growth and spread of human squamous cell carcinoma. J. Oral Pathol. Med. 2007, 36:363-370.
32. Isa A.Y., et al. Hypoxia in head and neck cancer. Br. J. Radiol. 2006, 79:791-798.
33. Janssen H.L., et al. Hypoxia in head and neck cancer: how much, how important?. Head Neck 2005, 27:622-638.
34. Karovic O., et al. Toxic effects of cobalt in primary cultures of mouse astrocytes. Similarities with hypoxia and role of HIF-1alpha. Biochem. Pharmacol. 2007, 73:694-708.
35. Kilic M., et al. Role of hypoxia inducible factor-1 alpha in modulation of apoptosis resistance. Oncogene 2007, 26:2027-2038.
36. Kim Y., et al. Hypoxia-regulated delta-like 1 homologue enhances cancer cell stemness and tumorigenicity. Cancer Res. 2009, 69:9271-9280.
37. Koshikawa N., et al. Hypoxia selects for high-metastatic Lewis lung carcinoma cells overexpressing Mcl-1 and exhibiting reduced apoptotic potential in solid tumors. Oncogene 2006, 25:917-928.
38. Koukourakis M.I., et al. Beclin 1 over- and underexpression in colorectal cancer: distinct patterns relate to prognosis and tumour hypoxia. Br. J. Cancer 2010, 103:1209-1214.
39. Kyasa M.J., et al. Gemcitabine and cisplatin in patients with locally advanced, recurrent, or metastatic head and neck cancer: results of a phase II trial. J. Appl. Res. 2008, 8:43-47.
40. Le Q.T. Identifying and targeting hypoxia in head and neck cancer: a brief overview of current approaches. Int. J. Radiat. Oncol. Biol. Phys. 2007, 69:S56-S58.
41. Le Q.T., et al. Galectin-1: a link between tumor hypoxia and tumor immune privilege. J. Clin. Oncol. 2005, 23:8932-8941.
42. Levine B., Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008, 132:27-42.
43. Liotta L.A., Kohn E.C. The microenvironment of the tumour-host interface. Nature 2001, 411:375-379.
44. Lopez-Albaitero A., Ferris R.L. Immune activation by epidermal growth factor receptor specific monoclonal antibody therapy for head and neck cancer. Arch. Otolaryngol. Head Neck Surg. 2007, 133:1277-1281.
45. Lorch J.H., et al. Induction chemotherapy in locally advanced head and neck cancer: a new standard of care?. Hematol. Oncol. Clin. North Am. 2008, 22:1155-1163. viii.
46. Lukashev D., et al. Hypoxia-dependent anti-inflammatory pathways in protection of cancerous tissues. Cancer Metastasis Rev. 2007, 26:273-279.
47. Marur S., Forastiere A.A. Head and neck cancer: changing epidemiology, diagnosis, and treatment. Mayo Clin. Proc. 2008, 83:489-501.
48. Mashberg A. Diagnosis of early oral and oropharyngeal squamous carcinoma: obstacles and their amelioration. Oral Oncol. 2000, 36:253-255.
49. Mognetti B., et al. Animal models in oral cancer research. Oral Oncol. 2006, 42:448-460.
50. Myers J.N., et al. An orthotopic nude mouse model of oral tongue squamous cell carcinoma. Clin. Cancer Res. 2002, 8:293-298.
51. Nordsmark M., et al. Prognostic value of tumor oxygenation in 397 head and neck tumors after primary radiation therapy. An international multi-center study. Radiother. Oncol. 2005, 77:18-24.
52. Nordsmark M., et al. Pretreatment oxygenation predicts radiation response in advanced squamous cell carcinoma of the head and neck. Radiother. Oncol. 1996, 41:31-39.
53. Parkin D.M., et al. Global cancer statistics. CA Cancer J. Clin. 1999, 49(33-64):1.
54. Peters L.J. Targeting hypoxia in head and neck cancer. Acta Oncol. 2001, 40:937-940.
55. Pignon J.P., et al. Chemotherapy added to locoregional treatment for head and neck squamous-cell carcinoma: three meta-analyses of updated individual data. MACH-NC Collaborative Group. Meta-Analysis of Chemotherapy on Head and Neck Cancer. Lancet 2000, 355:949-955.
56. Piret J.P., et al. Hypoxia and CoCl2 protect HepG2 cells against serum deprivation- and t-BHP-induced apoptosis: a possible anti-apoptotic role for HIF-1. Exp. Cell Res. 2004, 295:340-349.
57. Pitson G., et al. Tumor size and oxygenation are independent predictors of nodal diseases in patients with cervix cancer. Int. J. Radiat. Oncol. Biol. Phys. 2001, 51:699-703.
58. Pouyssegur J., et al. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 2006, 441:437-443.
59. Pursiheimo J.P., et al. Hypoxia-activated autophagy accelerates degradation of SQSTM1/p62. Oncogene 2009, 28:334-344.
60. Qiu C., et al. A cervical lymph node metastatic model of human tongue carcinoma: serial and orthotopic transplantation of histologically intact patient specimens in nude mice. J. Oral Maxillofac. Surg. 2003, 61:696-700.
61. Qu X., et al. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J. Clin. Invest. 2003, 112:1809-1820.
62. Reusch U., et al. Anti-CD3×anti-epidermal growth factor receptor (EGFR) bispecific antibody redirects T-cell cytolytic activity to EGFR-positive cancers in vitro and in an animal model. Clin. Cancer Res. 2006, 12:183-190.
63. Rofstad E.K., et al. Fluctuating and diffusion-limited hypoxia in hypoxia-induced metastasis. Clin. Cancer Res. 2007, 13:1971-1978.
64. Roh J.L., et al. The prognostic value of hypoxia markers in T2-staged oral tongue cancer. Oral Oncol. 2009, 45:63-68.
65. Sano D., Myers J.N. Xenograft models of head and neck cancers. Head Neck Oncol. 2009, 1:32.
66. Seiwert T.Y., Cohen E.E. State-of-the-art management of locally advanced head and neck cancer. Br. J. Cancer 2005, 92:1341-1348.
67. Shankaran V., et al. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 2001, 410:1107-1111.
68. Siemens D.R., et al. Hypoxia increases tumor cell shedding of MHC class I chain-related molecule: role of nitric oxide. Cancer Res. 2008, 68:4746-4753.
69. Song J., et al. Hypoxia-induced autophagy contributes to the chemoresistance of hepatocellular carcinoma cells. Autophagy 2009, 5:1131-1144.
70. Subarsky P., Hill R.P. The hypoxic tumour microenvironment and metastatic progression. Clin. Exp. Metastasis 2003, 20:237-250.
71. Sullivan R., Graham C.H. Hypoxia-driven selection of the metastatic phenotype. Cancer Metastasis Rev. 2007, 26:319-331.
72. Swann J.B., et al. Demonstration of inflammation-induced cancer and cancer immunoediting during primary tumorigenesis. Proc. Natl Acad. Sci. USA 2008, 105:652-656.
73. Thomas G.R., et al. Decreased expression of CD80 is a marker for increased tumorigenicity in a new murine model of oral squamous-cell carcinoma. Int. J. Cancer 1999, 82:377-384.
74. Tredan O., et al. Drug resistance and the solid tumor microenvironment. J. Natl Cancer Inst. 2007, 99:1441-1454.
75. Vaupel P., Mayer A. Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev. 2007, 26:225-239.
76. Vigneswaran N., et al. Differential susceptibility of metastatic and primary oral cancer cells to TRAIL-induced apoptosis. Int. J. Oncol. 2005, 26:103-112.
77. Vordermark D., Brown J.M. Endogenous markers of tumor hypoxia predictors of clinical radiation resistance?. Strahlenther. Onkol. 2003, 179:801-811.
78. Wan X.B., et al. Elevated Beclin 1 expression is correlated with HIF-1alpha in predicting poor prognosis of nasopharyngeal carcinoma. Autophagy 2010, 6:395-404.
79. Wickramasinghe N.S., et al. Hypoxia alters cathepsin B/inhibitor profiles in oral carcinoma cell lines. Anticancer Res. 2005, 25:2841-2849.
80. Wijffels K.I., et al. Tumour cell proliferation under hypoxic conditions in human head and neck squamous cell carcinomas. Oral Oncol. 2008, 44:335-344.
81. Yan L., et al. Antibody-based therapy for solid tumors. Cancer J. 2008, 14:178-183.
82. Yan L., et al. Autophagy in chronically ischemic myocardium. Proc. Natl Acad. Sci. USA 2005, 102:13807-13812.
83. Yu Z., et al. Cyclin d1 is a valuable prognostic marker in oropharyngeal squamous cell carcinoma. Clin. Cancer Res. 2005, 11:1160-1166.
84. Yuspa S.H., et al. A survey of transformation markers in differentiating epidermal cell lines in culture. Cancer Res. 1980, 40:4694-4703.
85. Zhang L., Hill R.P. Hypoxia enhances metastatic efficiency by up-regulating Mdm2 in KHT cells and increasing resistance to apoptosis. Cancer Res. 2004, 64:4180-4189.