Expression of heme oxygenase-1 in non-small cell lung cancer (NSCLC) and its correlation with clinical data

Lung Cancer

Volumn 77, Issue 1, 2012, Pages 168-175

  Degese, María S ^a   Mendizabal, Javier E ^a   Gandini, Norberto A ^b   Gutkind, J Silvio ^c   Molinolo, Alfredo ^c   Hewitt, Stephen M ^d   Curino, Alejandro C ^b   Coso, Omar A ^a   Facchinetti, María M ^b  

^a INSTITUTO DE FISIOLOGÍA   (Argentina)

^b Instituto de Investigaciones Bioquimicas Bahia Blanca   (Argentina)

^c NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Heme oxygenase 1; Immunohistochemistry; Lung cancer; NSCLC; Tissue microarray

Indexed keywords

HEME OXYGENASE 1;

ADULT; ARTICLE; CANCER STAGING; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LUNG CARCINOMA; LUNG NON SMALL CELL CANCER; LYMPH NODE; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; TISSUE MICROARRAY; UPREGULATION;

ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION; HEME OXYGENASE-1; HUMANS; KAPLAN-MEIER ESTIMATE; LUNG NEOPLASMS; LYMPHATIC METASTASIS; MALE; MICE; NIH 3T3 CELLS; REAL-TIME POLYMERASE CHAIN REACTION; TISSUE ARRAY ANALYSIS; UP-REGULATION;

EID: 84861730556     PISSN: 01695002     EISSN: 18728332     Source Type: Journal    
DOI: 10.1016/j.lungcan.2012.02.016     Document Type: Article

References (38)

1. Tenhunen R., Marver H.S., Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA 1968, 61:748-755.
2. Applegate L.A., Luscher P., Tyrrell R.M. Induction of heme oxygenase: a general response to oxidant stress in cultured mammalian cells. Cancer Res 1991, 51:974-978.
3. Slebos D.J., Ryter S.W., Choi A.M. Heme oxygenase-1 and carbon monoxide in pulmonary medicine. Respir Res 2003, 4:7-10.
4. Fredenburgh L.E., Perrella M.A., Mitsialis A. The role of heme-oxygenase-1 in pulmonary disease. Am J Respir Cell Mol Biol 2007, 36:158-165.
5. Zhou H., Lu F., Latham C., Zander D.S., Visner G.A. Heme oxygenase-1 expression in human lungs with cystic fibrosis and cytoprotective effects against Pseudomonas aeruginosa in vitro. Am J Respir Crit Care Med 2004, 170(6):633-640.
6. Mumby S., Upton R.L., Chen Y., Stanford S.J., Quinlan G.J., Nicholson A.G., et al. Lung heme oxygenase-1 is elevated in acute respiratory distress syndrome. Crit Care Med 2004, 32(5):1130-1135.
7. Siner J.M., Jiang G., Cohen Z.I., Shan P., Zhang X., Lee C.G., et al. VEGF-induced heme oxygenase-1 confers cytoprotection from lethal hyperoxia in vivo. FASEB J 2007, 21:1422-1432.
8. Repine J.E., Bast A., Lankhorst I. Oxidative stress in chronic obstructive pulmonary disease. Oxidative stress study group. Am J Respir Crit Care Med 1997, 156(2 Pt 1):341-357.
9. Jozkowicz A., Was H., Dulak J. Heme oxygenase-1 in tumors: is it a false friend?. Antioxid Redox Signal 2007, 9:2099-2115.
10. Hirai K., Sasahira T., Ohmori H., Fujii K., Kuniyasu H. Inhibition of heme oxygenase-1 by zinc protoporphyrin IX reduces tumor growth of LL/2 lung cancer in C57BL mice. Int J Cancer 2007, 120(3):500-505.
11. Kuroda H., Takeno M., Murakami S., Miyazawa N., Kaneko T., Ishigatsubo Y. Inhibition of heme oxygenase-1 with an epidermal growth factor receptor inhibitor and cisplatin decreases proliferation of lung cancer A549 cells. Lung Cancer 2010, 67(1):31-36.
12. Kim H.R., Kim S., Kim E.J., Park J.H., Yang S.H., Jeong E.T., et al. Suppression of Nrf2-driven heme oxygenase-1 enhances the chemosensitivity of lung cancer A549 cells toward cisplatin. Lung Cancer 2008, 60(1):47-56.
13. Kikuchi A., Yamaya M., Suzuki S., Yasuda H., Kubo H., Nakayama K., et al. Association of susceptibility to the development of lung adenocarcinoma with the heme oxygenase-1 gene promoter polymorphism. Hum Genet 2005, 116(5):354-360.
14. Boschetto P., Zeni E., Mazzetti L., Miotto D., Lo Cascio N., Maestrelli P., et al. Decreased heme-oxygenase (HO)-1 in the macrophages of non-small cell lung cancer. Lung Cancer 2008, 59(2):192-197.
15. Li M.Y., Yip J., Hsin M.K., Mok T.S., Wu Y., Underwood M.J., et al. Haem oxygenase-1 plays a central role in NNK-mediated lung carcinogenesis. Eur Respir J 2008, 32(4):911-923.
16. Hewitt S.M. Design, construction, and use of tissue microarrays. Methods Mol Biol 2004, 264:61-72.
17. Kononen J., Bubendorf L., Kallioniemi A., Bärlund M., Schraml P., Leighton S., et al. Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nat Med 1998, 4(7):844-847.
18. Facchinetti M.M., Gandini N.A., Fermento M.E., Sterin-Speziale N.B., Ji Y., Patel V., et al. The expression of sphingosine kinase-1 in head and neck carcinoma. Cells Tissues Organs 2010, 192(5):314-324.
19. Marinissen M.J., Tanos T., Bolós M., de Sagarra M.R., Coso O.A., Cuadrado A. Inhibition of heme oxygenase-1 interferes with the transforming activity of the Kaposi sarcoma herpesvirus-encoded G protein-coupled receptor. J Biol Chem 2006, 281(16):11332-11346.
20. De Palma G., Mozzoni P., Acampa O., Internullo E., Carbognani P., Rusca M., et al. Expression levels of some antioxidant and epidermal growth factor receptor genes in patients with early-stage non-small cell lung cancer. J Nucleic Acids 2010, 2010:1-6. [pii 147528].
21. Was H., Dulak J., Jozkowicz A. Heme oxygenase-1 in tumor biology and therapy. Curr Drug Targets 2010, 11(12):1551-1570.
22. Maines M.D., Abrahamsson P.A. Expression of heme oxygenase-1 (HSP32) in human prostate: normal, hyperplastic, and tumor tissue distribution. Urology 1996, 47:727-733.
23. Alaoui-Jamali M.A., Bismar T.A., Gupta A., Szarek W.A., Su J., Song W., et al. A novel experimental heme oxygenase-1-targeted therapy for hormone refractory prostate cancer. Cancer Res 2009, 69:8017-8024.
24. Hara E., Takahashi K., Tominaga T. Expression of heme oxygenase and inducible nitric oxide synthase mRNA in human brain tumors. Biochem Biophys Res Commun 1996, 224:153-158.
25. Mayerhofer M., Florian S., Krauth M.T., Aichberger K.J., Bilban M., Marculescu R., et al. Identification of heme oxygenase-1 as a novel BCR/ABL-dependent survival factor in chronic myeloid leukemia. Cancer Res 2004, 64:3148-3154.
26. Torisu-Itakura H., Furue M., Kuwano M., Ono M. Co-expression of thymidine phosphorylase and heme oxygenase-1 in macrophages in human malignant vertical growth melanomas. Jpn J Cancer Res 2000, 91:906-910.
27. Berberat P.O., Dambrauskas Z., Gulbinas A., Giese T., Giese N., Künzli B., et al. Inhibition of heme oxygenase-1 increases responsiveness of pancreatic cancer cells to anticancer treatment. Clin Cancer Res 2005, 11(10):3790-3798.
28. Goodman A.I., Choudhury M., da Silva J.L., Schwartzman M.L., Abraham N.G. Overexpression of the heme oxygenase gene in renal cell carcinoma. Proc Soc Exp Biol Med 1997, 214:54-61.
29. Tsuji M.H., Yanagawa T., Iwasa S., Tabuchi K., Onizawa K., Bannai S., et al. Heme oxygenase-1 expression in oral squamous cell carcinoma as involved in lymph node metastasis. Cancer Lett 1999, 138:53-59.
30. Lee J., Lee S.K., Lee B.U., Lee H.J., Cho N.P., Yoon J.H., et al. Upregulation of heme oxygenase-1 in oral epithelial dysplasias. Int J Oral Maxillofac Surg 2008, 37:287-292.
31. Lin Q., Weis S., Yang G., Weng Y.H., Helston R., Rish K., et al. Heme oxygenase-1 protein localizes to the nucleus and activates transcription factors important in oxidative stress. J Biol Chem 2007, 282:20621-20633.
32. Sacca P., Meiss R., Casas G., Mazza O., Calvo J.C., Navone N., et al. Nuclear translocation of haeme oxygenase-1 is associated to prostate cancer. Br J Cancer 2007, 97(12):1683-1689.
33. Suttner D.M., Sridhar K., Lee C.S., Tomura T., Hansen T.N., Dennery P.A. Protective effects of transient HO-1 overexpression on susceptibility to oxygen toxicity in lung cells. Am J Physiol 1999, 276:L443-L451.
34. Yim M.S., Ha Y.S., Kim I.Y., Yun S.J., Choi Y.H., Kim W.J. HMOX1 is an important prognostic indicator of non-muscle invasive bladder cancer recurrence and progression. J Urol 2011, 185(2):701-705.
35. Yanagawa T., Omura K., Harada H., Nakaso K., Iwasa S., Koyama Y., et al. Heme oxygenase-1 expression predicts cervical lymph node metastasis of tongue squamous cell carcinomas. Oral Oncol 2004, 40(1):21-27.
36. Becker J.C., Fukui H., Imai Y., Sekikawa A., Kimura T., Yamagishi H., et al. Colonic expression of heme oxygenase-1 is associated with a better long-term survival in patients with colorectal cancer. Scand J Gastroenterol 2007, 42(7):852-858.
37. Maestrelli P., Páska C., Saetta M., Turato G., Nowicki Y., Monti S., et al. Decreased haem oxygenase-1 and increased inducible nitric oxide synthase in the lung of severe COPD patients. Eur Respir J 2003, 21(6):971-976.
38. Lee J., Lee S.K., Lee B.U., Lee H.J., Cho N.P., Yoon J.H., et al. Upregulation of heme oxygenase-1 in oral epithelial dysplasias. Int J Oral Maxillofac Surg 2008, 37(3):287-292.