Asian Pacific Journal of Cancer Prevention

Asian Pacific Journal of Cancer Prevention (아시아태평양암예방학회)
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Prognostic Role of Hypoxic Inducible Factor Expression in Non-small Cell Lung Cancer: A Meta-analysis

  • Li, Cong (Huaxi Student Society of Oncology Research (HASSOR), West China School of Medicine, Sichuan University) ;
  • Lu, Hua-Jun (Huaxi Student Society of Oncology Research (HASSOR), West China School of Medicine, Sichuan University) ;
  • Na, Fei-Fei (Huaxi Student Society of Oncology Research (HASSOR), West China School of Medicine, Sichuan University) ;
  • Deng, Lei (Huaxi Student Society of Oncology Research (HASSOR), West China School of Medicine, Sichuan University) ;
  • Xue, Jian-Xin (Department of Thoracic Cancer, Cancer Center and State Key Laboratory of Biotherapy, West China Hospital) ;
  • Wang, Jing-Wen (Huaxi Student Society of Oncology Research (HASSOR), West China School of Medicine, Sichuan University) ;
  • Wang, Yu-Qing (West China School of Medicine, Sichuan University) ;
  • Li, Qiao-Ling (West China School of Medicine, Sichuan University) ;
  • Lu, You (Department of Thoracic Cancer, Cancer Center and State Key Laboratory of Biotherapy, West China Hospital)
  • Published : 2013.06.30
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Abstract

Introduction: Reported prognostic roles of hypoxic inducible factor (HIF) expression in non-small cell lung cancer (NSCLC) have varied. This meta-analysis aimed to examine the relationship between HIF expression and clinical outcome in NSCLC patients. Methods: PubMed were used to identify relevant literature with the last report up to December $20^{th}$, 2012. After careful review, survival data were collected from eligible studies. We completed the meta-analysis using Stata statistical software (Version 11) and combined hazard ratio (HR) for overall survival (OS). Subgroup specificity, heterogeneity and publication bias were also assessed. All of the results were verified by two persons to ensure accuracy. Results: Eight studies were finally stepped into this meta-analysis in which seven had available data for HIF-$1{\alpha}$ and three for HIF-$2{\alpha}$. Combined HRs suggested that higher expression of $HIF1{\alpha}$ had a negative impact on NSCLC patient survival (HR=1.50; 95%CI=1.07-2.10; p=0.019). The expression of HIF-$2{\alpha}$ was also relative to a poorer survival (HR=2.02; 95%CI=1.47-2.77; p=0.000). No bias existed in either of the two groups. Conclusion: This study suggests that elevations of HIF-$1{\alpha}$ and HIF-$2{\alpha}$ expression are both associated with poor outcome for patients with NSCLC. The data support further and high quality investigation of HIF expression for predicting poor outcome in patients with NSCLC.

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References

  1. Altman DG, McShane LM, Sauerbrei W, Taube SE (2012). Reporting Recommendations for Tumor Marker Prognostic Studies (REMARK): explanation and elaboration. PLoS Med, 9, e1001216. https://doi.org/10.1371/journal.pmed.1001216
  2. Bangoura G, Liu ZS, Qian Q, et al (2007). Prognostic significance of HIF-2alpha/EPAS1 expression in hepatocellular carcinoma. World J Gastroenterol, 13, 3176-82.
  3. Chansky K, Sculier JP, Crowley JJ, et al (2009). The International Association for the Study of Lung Cancer Staging Project: prognostic factors and pathologic TNM stage in surgically managed non-small cell lung cancer. J Thorac Oncol, 4, 792-801. https://doi.org/10.1097/JTO.0b013e3181a7716e
  4. Chen M, Cai E, Huang J (2012). Prognostic Value of Vascular Endothelial Growth Factor Expression in Patients with Esophageal Cancer: A Systematic Review and Meta-analysis. Cancer Epidemiol Biomarkers Prev, 21, 1126-34. https://doi.org/10.1158/1055-9965.EPI-12-0020
  5. Daniel E.B. Swinson, et al (2004). Hypoxia-inducible factor-$1\alpha$ in non small cell lung cancer: relation to growth factor, protease and apoptosis pathways. Int J Cancer, 111, 43-50. https://doi.org/10.1002/ijc.20052
  6. DerSimonian R, Kacker R (2007). Random-effects model for meta-analysis of clinical trials: an update. Contemp Clin Trials, 28, 105-14. https://doi.org/10.1016/j.cct.2006.04.004
  7. Dinnes J, Deeks J, Kirby J, et al (2005). A methodological review of how heterogeneity has been examined in systematic reviews of diagnostic test accuracy. Health Technol Assess, 9, 1-113.
  8. Giatromanolaki A, et al (2001). Relation of hypoxia inducible factor $1\alpha$and 2αin operable non-small cell lung cancer to angiogenic/molecular profile of tumours and survival. British Journal of Cancer, 85, 881-90. https://doi.org/10.1054/bjoc.2001.2018
  9. Giatromanolaki A, Sivridis E, Kouskoukis C, et al (2003). Hypoxiainducible factors 1alpha and 2alpha are related to vascular endothelial growth factor expression and a poorer prognosis in nodular malignant melanomas of the skin. Melanoma Res, 13, 493-501. https://doi.org/10.1097/00008390-200310000-00008
  10. Greenberger LM, Horak ID, Filpula D, et al (2008). A RNA antagonist of hypoxia-inducible factor-1alpha, EZN-2968, inhibits tumor cell growth. Mol. Cancer Ther, 7, 3598-608. https://doi.org/10.1158/1535-7163.MCT-08-0510
  11. Hanahan D, Weinberg RA (2011). Hallmarks of cancer: the next generation. Cell, 144, 646-74. https://doi.org/10.1016/j.cell.2011.02.013
  12. Harris AL(2002). Hypoxia-a key regulatory factor in tumour growth. Nat Rev Cancer, 2, 38-47. https://doi.org/10.1038/nrc704
  13. Hsu CL, Chen KY, Shih JY, et al (2012). Advanced non-small cell lung cancer in patients aged 45 years or younger: outcomes and prognostic factors. BMC Cancer, 12, 241 https://doi.org/10.1186/1471-2407-12-241
  14. Hu CJ, Wang LY, Chodosh LA, et al (2003). Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol Cell Biol, 23, 9361-74. https://doi.org/10.1128/MCB.23.24.9361-9374.2003
  15. Hui EP, Chan AT, Pezzella F, et al (2002). Coexpression of hypoxiainducible factors 1alpha and 2alpha, carbonic anhydrase IX, and vascular endothelial growth factor in nasopharyngeal carcinoma and relationship to survival. Clin Cancer Res, 8, 2595-604.
  16. Hung JJ, et al (2009). Prognostic significance of hypoxia-inducible factor-$1\alpha$, TWIST1 and Snail expression in resectable nonsmall cell lung cancer. Thorax, 64, 1082-9. https://doi.org/10.1136/thx.2009.115691
  17. Jackson AL, Zhou B, Kim WY (2010). HIF, hypoxia and the role of angiogenesis in non-small cell lung cancer. Expert Opin Ther Targets, 14, 1047-57. https://doi.org/10.1517/14728222.2010.511617
  18. Koh MY, Spivak-Kroizman T, Venturini S, et al (2008). Molecular mechanisms for the activity of PX-478, an antitumor inhibitor of the hypoxia-inducible factor-1A. Mol. Cancer Ther, 7, 90-100. https://doi.org/10.1158/1535-7163.MCT-07-0463
  19. Kong D, Park EJ, Stephen AG, et al (2005). Echinomycin, a smallmolecule inhibitor of hypoxia inducible factor-1 DNA-binding activity. Cancer Res, 65, 9047-55. https://doi.org/10.1158/0008-5472.CAN-05-1235
  20. Koppenol WH, Bounds PL, Dang CV (2011). Otto Warburg's contributions to current concepts of cancer metabolism. Nat Rev Cancer, 11, 325-37. https://doi.org/10.1038/nrc3038
  21. Lee CH, Lee MK, Kang CD, et al (2003). Differential expression of hypoxic inducible fator-$1\alpha$ and tumor cell proliferation between squamous cell carcinoma and adenocarcinomas among operable non-small cell lung cacinomas. J Korean Med Sci, 18, 196-203. https://doi.org/10.3346/jkms.2003.18.2.196
  22. Lofstedt T, Fredlund E, Holmquist-Mengelbier L, et al (2007). Hypoxia Inducible Factor-2α in Cancer. Cell Cycle, 6, 919-26. https://doi.org/10.4161/cc.6.8.4133
  23. Ma YX, Tian ZN, Zhang W (2012). Circulating miR-125b is a novel biomarker for screening non-small-cell lung cancer and predicts poor prognosis. J Cancer Res Clin Oncol, 138, 2045-50. https://doi.org/10.1007/s00432-012-1285-0
  24. McKee TC, Rabe D, Bokesch HR, et al (2012). Inhibition of hypoxia inducible factor-2 transcription: isolation of active modulators from marine sponges. J Nat Prod, 75, 1632-6. https://doi.org/10.1021/np300211x
  25. Moldvay J (2012). Personalized therapy in non-small cell lung cancer: from diagnosis to therapy. Orv Hetil, 153, 909-16. https://doi.org/10.1556/OH.2012.29397
  26. Mottet D, Dumont V, Deccache Y, et al (2003). Regulation of hypoxia-inducible factor-1alpha protein level during hypoxic conditions by the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3beta pathway in HepG2 cells. J Biol Chem, 278, 1277-85.
  27. Oldenhuis CN, Oosting SF, Gietema JA, et al (2008). Prognostic versus predictive value of biomarkers in oncology. Eur J Cancer, 44, 946-53. https://doi.org/10.1016/j.ejca.2008.03.006
  28. Ortiz-Barahona A, Villar D, Pescador N, et al (2010). Genome-wide identification of hypoxia-inducible factor binding sites and target genes by aprobabilistic model integrating transcriptionprofiling data and in silico binding site prediction. Nucleic Acids Res, 38, 2332-45. https://doi.org/10.1093/nar/gkp1205
  29. Osada R, Horiuchi A, Kikuchi N, et al (2007). Expression of hypoxia-inducible factor 1alpha, hypoxia-inducible factor 2alpha, and von Hippel-Lindau protein in epithelial ovarian neoplasms and allelic loss of von Hippel-Lindau gene: nuclear expression ofhypoxia-inducible factor 1alpha is an independent prognostic factor in ovarian carcinoma. Hum Pathol, 38, 1310-20. https://doi.org/10.1016/j.humpath.2007.02.010
  30. Park S, Ha SY, Cho HY, et al (2010). Prognostic implications of hypoxia-inducible factor-1 in epidermal growth factor receptornegative non-small cell lung cancer. Lung Cancer, 72, 100-7.
  31. Rankin EB, Giaccia AJ (2008). The role of hypoxia-inducible factors in tumorigenesis. Cell Death and Differentiation, 15, 678-85. https://doi.org/10.1038/cdd.2008.21
  32. Shibaji T, Nagao M, Ikeda N, et al (2003). Prognostic significance of HIF-1 alpha overexpression in human pancreatic cancer. Anticancer Res, 23, 4721-7.
  33. Simon JM (2007). Hypoxia and angiogenesis. Bull Cancer, 94, S160-5.
  34. Talks KL, Turley H, Gatter KC, et al (2000). The expression and distribution of the hypoxia-inducible factors HIF-1alpha and HIF-2alpha in normal human tissues, cancers, and tumorassociated macrophages. Am J Pathol, 157, 411-21. https://doi.org/10.1016/S0002-9440(10)64554-3
  35. Tang CM, Yu J (2013). Hypoxia-inducible factor-1 as a therapeutic target in cancer. Journal of Gastroenterology and Hepatology, 28, 401-5 https://doi.org/10.1111/jgh.12038
  36. Tierney JF, Stewart LA, Ghersi D (2007). Practical methods for incorporating summary time-to-event data Into meta-analysis. Trials, 8, 16. https://doi.org/10.1186/1745-6215-8-16
  37. Uchida T, Rossignol F, Matthay MA, et al (2004). Prolonged hypoxia differentially regulates hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha expression in lung epithelial cells: implication of natural antisense HIF-1 alpha. J Bioi Chem, 279, 14871-8. https://doi.org/10.1074/jbc.M400461200
  38. Wei LF, Liu XL, Hu CH (2011). [Correlation between expression of HIF-2alpha and OCT-4 and prognosis of NSCLC]. J Cent South Univ(Med Sci), 36, 854-8
  39. Winter SC, Shah KA, Han C, et al (2006). The relation between hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha expression with anemia and outcome in surgically treated head and neck cancer. Cancer, 107, 757-66. https://doi.org/10.1002/cncr.21983
  40. Wood DE, Eapen GA, Ettinger DS, et al (2012). Lung cancer screening. J Natl Compr Canc Netw, 10, 240-65.
  41. Wu SW, Cheng ZN, Yu L, et al (2011). [Expression of CD82/KAI1 and HIF-1alpha in non-small cell lung cancer and their relationship to vasculogenic mimicry]. Chin J Lung Cancer, 14, 918-25.
  42. Wu XH, Qian C, Yuan K (2011). Correlations of hypoxiainducible factor-$1\alpha$/hypoxia-inducible factor-2 expression with angiogenesis factors expression and prognosis in non-small cell lung cancer. Chin Med J (Engl), 124, 11-8.
  43. Yoshimura H, Dhar DK, Kohno H, et al (2004). Prognostic impact of hypoxia-inducible factors 1alpha and 2alpha in colorectal cancer patients: correlation with tumor angiogenesis and cyclooxygenase-2 expression. Clin Cancer Res, 10, 8554-60. https://doi.org/10.1158/1078-0432.CCR-0946-03
  44. Zhang LQ, Wang J, Jiang F, et al (2012). Prognostic value of survivin in patients with non-small cell lung carcinoma: a systematic review with meta-analysis. Plos One, 7, e34100 https://doi.org/10.1371/journal.pone.0034100
  45. Zhao T, Lv J, Zhao J, Nzekebaloudou M (2009). Hypoxia-inducible factor-$1\alpha$ gene polymorphisms and cancer risk: a metaanalysis. J Exp Clin Cancer Res, 28, 159. https://doi.org/10.1186/1756-9966-28-159

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