Upregulation of heme oxygenase-1 in colorectal cancer patients with increased circulation carbon monoxide levels, potentially affects chemotherapeutic sensitivity

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Yin, Hongzhuan ^a,b   Fang, Jun ^b,c   Liao, Long ^b   Maeda, Hiroshi ^b   Su, Qi ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b SOJO UNIVERSITY   (Japan)

^c ANHUI MEDICAL UNIVERSITY   (China)

Author keywords

Carbon monoxide; Carboxyhemoglobin; Chemosensitivity; Colorectal cancer; Heme oxygenase 1

Indexed keywords

CARBON MONOXIDE; CARBOXYHEMOGLOBIN; HEME OXYGENASE 1; HEMIN; PIRARUBICIN; PROTOPORPHYRIN ZINC; ANTINEOPLASTIC AGENT;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CHEMOTHERAPY; COLORECTAL CANCER; COLORECTAL CANCER CELL LINE; COLORECTAL CARCINOMA; COLORECTAL POLYP; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG POTENTIATION; DRUG SENSITIVITY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TUMOR DIFFERENTIATION; TUMOR GROWTH; UPREGULATION; ANIMAL; CANCER STAGING; COLORECTAL NEOPLASMS; DISEASE MODEL; DRUG RESISTANCE; DRUG SCREENING; GENE EXPRESSION; GENETICS; HT 29 CELL LINE; IMMUNOHISTOCHEMISTRY; METABOLISM; METASTASIS; MIDDLE AGED; PROTEIN TRANSPORT; TUMOR CELL LINE; TUMOR VOLUME; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; ANTINEOPLASTIC AGENTS; CARBON MONOXIDE; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION; HEME OXYGENASE-1; HT29 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MIDDLE AGED; NEOPLASM METASTASIS; NEOPLASM STAGING; PROTEIN TRANSPORT; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84902066943     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-436     Document Type: Article

References (52)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013, 63(1):11-30.
2. André T, Boni C, Navarro M, Tabernero J, Hickish T, Topham C, Bonetti A, Clingan P, Bridgewater J, Rivera F. Improved overall survival with oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment in stage II or III colon cancer in the MOSAIC trial. J clin oncol 2009, 27(19):3109-3116.
3. Jayne DG, Thorpe HC, Copeland J, Quirke P, Brown JM, Guillou PJ. Five year follow up of the Medical Research Council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer. Br J Surg 2010, 97(11):1638-1645.
4. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011, 61(2):69-90.
5. Dewdney A, Cunningham D, Tabernero J, Capdevila J, Glimelius B, Cervantes A, Tait D, Brown G, Wotherspoon A, de Castro DG. Multicenter randomized phase II clinical trial comparing neoadjuvant oxaliplatin, capecitabine, and preoperative radiotherapy with or without cetuximab followed by total mesorectal excision in patients with high-risk rectal cancer (EXPERT-C). J Clil Oncol 2012, 30(14):1620-1627.
6. Morse D, Choi AMK. Heme oxygenase-1: the " emerging molecule" has arrived. Am J Respir Cell Mol Biol 2002, 27(1):8-16.
7. Matsumoto A, Hanayama R, Nakamura M, Suzuki K, Fujii J, Tatsumi H, Taniguchi N. A high expression of heme oxygenase-1 in the liver of LEC rats at the stage of hepatoma: the possible implication of induction in uninvolved tissue. Free Radic Res 1998, 28(4):383-391.
8. Lo S, Bell HS, Yamaguchi S, Wharton SB, Whittle IR. Heme oxygenase (HO) isoforms in experimental C6 glioma: an immunocytochemical study. Br J Neurosurg 2001, 15(5):416-418.
9. Fang J, Sawa T, Akaike T, Greish K, Maeda H. Enhancement of chemotherapeutic response of tumor cells by a heme oxygenase inhibitor, pegylated zinc protoporphyrin. Int J Cancer 2004, 109(1):1-8.
10. Nowis D, Legat M, Grzela T, Niderla J, Wilczek E, Wilczynski GM, Glodkowska E, Mrowka P, Issat T, Dulak J, Józkowicz A, Waś H, Adamek M, Wrzosek A, Nazarewski S, Makowski M, Stokłosa T, Jakóbisiak M, Gołab J. Heme oxygenase-1 protects tumor cells against photodynamic therapy-mediated cytotoxicity. Oncogene 2006, 25(24):3365-3374.
11. Maines MD, Abrahamsson PA. Expression of heme oxygenase-1 (HSP32) in human prostate: normal, hyperplastic, and tumor tissue distribution. Urology 1996, 47(5):727-733.
12. Srisook K, Jung NH, Kim BR, Cha SH, Kim HS, Cha YN. Heme oxygenase-1-mediated partial cytoprotective effect by NO on cadmium-induced cytotoxicity in C6 rat glioma cells. Toxicol In Vitro 2005, 19(1):31-39.
13. Raval CM, Lee PJ. Heme oxygenase-1 in lung disease. Curr Drug Targets 2010, 11(12):1532-1540.
14. Durante W. Protective role of heme oxygenase-1 against inflammation in atherosclerosis. Front Biosci (Landmark Ed) 2011, 16:2372-2788.
15. Wu M-L, Ho Y-C, Yet S-F. A central role of heme oxygenase-1 in cardiovascular protection. Antioxid Redox Signal 2011, 15(7):1835-1846.
16. Doi K, Akaike T, Fujii S, Tanaka S, Ikebe N, Beppu T, Shibahara S, Ogawa M, Maeda H. Induction of haem oxygenase-1 nitric oxide and ischaemia in experimental solid tumours and implications for tumour growth. Br J Cancer 1999, 80(12):1945-1954.
17. Tanaka S, Akaike T, Fang J, Beppu T, Ogawa M, Tamura F, Miyamoto Y, Maeda H. Antiapoptotic effect of haem oxygenase-1 induced by nitric oxide in experimental solid tumour. Br J Cancer 2003, 88(6):902-909.
18. Fang J, Sawa T, Akaike T, Akuta T, Sahoo SK, Khaled G, Hamada A, Maeda H. In vivo antitumor activity of pegylated zinc protoporphyrin: targeted inhibition of heme oxygenase in solid tumor. Cancer Res 2003, 63(13):3567-3574.
19. Deininger MH, Meyermann R, Trautmann K, Duffner F, Grote EH, Wickboldt J, Schluesener HJ. Heme oxygenase (HO)-1 expressing macrophages/microglial cells accumulate during oligodendroglioma progression. Brain Res 2000, 882(1-2):1-8.
20. Goodman AI, Choudhury M, da Silva JL, Schwartzman ML, Abraham NG. Overexpression of the heme oxygenase gene in renal cell carcinoma. Proc Soc Exp Biol Med 1997, 214(1):54-61.
21. Tsuji MH, Yanagawa T, Iwasa S, Tabuchi K, Onizawa K, Bannai S, Toyooka H, Yoshida H. Heme oxygenase-1 expression in oral squamous cell carcinoma as involved in lymph node metastasis. Cancer Lett 1999, 138(1-2):53-59.
22. Mayerhofer M, Florian S, Krauth MT, Aichberger KJ, Bilban M, Marculescu R, Printz D, Fritsch G, Wagner O, Selzer E, Sperr WR, Valent P, Sillaber C. Identification of heme oxygenase-1 as a novel BCR/ABL-dependent survival factor in chronic myeloid leukemia. Cancer Res 2004, 64(9):3148-3154.
23. Ferrando M, Gueron G, Elguero B, Giudice J, Salles A, Leskow FC, Jares-Erijman EA, Colombo L, Meiss R, Navone N. Heme oxygenase 1 (HO-1) challenges the angiogenic switch in prostate cancer. Angiogenesis 2011, 14(4):467-479.
24. Jozkowicz A, Was H, Dulak J. Heme oxygenase-1 in tumors: is it a false friend?. Antioxid Redox Signal 2007, 9(12):2099-2117.
25. Fang J, Qin H, Nakamura H, Tsukigawa K, Shin T, Maeda H. Carbon monoxide, generated by heme oxygenase-1, mediates the enhanced permeability and retention effect in solid tumors. Cancer Sci 2012, 103(3):535-541.
26. Gullotta F, di Masi A, Ascenzi P. Carbon monoxide: an unusual drug. IUBMB life 2012, 64(5):378-386.
27. Kim DS, Chae SW, Kim HR, Chae HJ. CO and bilirubin inhibit doxorubicin-induced cardiac cell death. Immunopharmacol Immunotoxicol 2009, 31(1):64-70.
28. Motterlini R, Otterbein LE. The therapeutic potential of carbon monoxide. Nat Rev Drug Discov 2010, 9(9):728-743.
29. Suematsu M, Kajimura M, Kabe Y. Roles of Stress-Inducible Carbon Monoxide in the Regulation of Liver Function. Gas Biology Research in Clinical Practice 2011, 1-5. Basel: Karger, Yoshikawa T, Naito Y.
30. Ishikawa T, Yoshida N, Higashihara H, Inoue M, Uchiyama K, Takagi T, Handa O, Kokura S, Naito Y, Okanoue T, Yoshikawa T. Different effects of constitutive nitric oxide synthase and heme oxygenase on pulmonary or liver metastasis of colon cancer in mice. Clin Exp Metastasis 2003, 20(5):445-450.
31. Nuhn P, Kunzli BM, Hennig R, Mitkus T, Ramanauskas T, Nobiling R, Meuer SC, Friess H, Berberat PO. Heme oxygenase-1 and its metabolites affect pancreatic tumor growth in vivo. Mol Cancer 2009, 8:37.
32. Fang J, Akaike T, Maeda H. Antiapoptotic role of heme oxygenase (HO) and the potential of HO as a target in anticancer treatment. Apoptosis 2004, 9(1):27-35.
33. Iyer AK, Greish K, Fang J, Murakami R, Maeda H. High-loading nanosized micelles of copoly(styrene-maleic acid)-zinc protoporphyrin for targeted delivery of a potent heme oxygenase inhibitor. Biomaterials 2007, 28(10):1871-1881.
34. Maines MD. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J 1988, 2(10):2557-2568.
35. Abraham NG, Kappas A. Pharmacological and clinical aspects of heme oxygenase. Pharmacol Rev 2008, 60(1):79-127.
36. Tsai J-R, Wang H-M, Liu P-L, Chen Y-H, Yang M-C, Chou S-H, Cheng Y-J, Yin W-H, Hwang J-J, Chong I-W. High expression of heme oxygenase-1 is associated with tumor invasiveness and poor clinical outcome in non-small cell lung cancer patients. Cell Oncol (Dordr) 2012, 35(6):461-471.
37. Liu P, Tsai J, Wang T, Hwang J, Chong I. Overexpression of heme oxygenase-1 gene increases cell metastatic ability in non-small cell lung cancer. Am J Respir Crit Care Med 2010, 181:A2049.
38. Dhawan S. Heme oxygenase-1 activation inhibits XMRV pathogenesis and carcinogenesis in prostate cancer cells. Retrovirology 2011, 8(Suppl 1):A218.
39. Lo S-S, Lin S-C, Wu C-W, Chen J-H, Yeh W-I, Chung M-Y, Lui W-Y. Heme oxygenase-1 gene promoter polymorphism is associated with risk of gastric adenocarcinoma and lymphovascular tumor invasion. Ann Surg Oncol 2007, 14(8):2250-2256.
40. Vashist YK, Uzungolu G, Kutup A, Gebauer F, Koenig A, Deutsch L, Zehler O, Busch P, Kalinin V, Izbicki JR. Heme oxygenase 1 germ line GTn promoter polymorphism is an independent prognosticator of tumor recurrence and survival in pancreatic cancer. J Surg Oncol 2011, 104(3):305-311.
41. Ruiz-Ramos R, Lopez-Carrillo L, Rios-Perez AD, De Vizcaya-Ruíz A, Cebrian ME. Sodium arsenite induces ROS generation, DNA oxidative damage, HO-1 and c-Myc proteins, NF-κB activation and cell proliferation in human breast cancer MCF-7 cells. Mutat Res 2009, 674(1):109-115.
42. Shi L, Fang J. Implication of heme oxygenase-1 in the sensitivity of nasopharyngeal carcinomas to radiotherapy. J Exp Clin Cancer Res 2008, 27:13.
43. Yin Y, Liu Q, Wang B, Chen G, Xu L, Zhou H. Expression and function of heme oxygenase-1 in human gastric cancer. Exp Biol Med (Maywood) 2012, 237(4):362-371.
44. Was H, Cichon T, Smolarczyk R, Rudnicka D, Stopa M, Chevalier C, Leger JJ, Lackowska B, Grochot A, Bojkowska K, Ratajska A, Kieda C, Szala S, Dulak J, Jozkowicz A. Overexpression of heme oxygenase-1 in murine melanoma: increased proliferation and viability of tumor cells, decreased survival of mice. The Am J Pathol 2006, 169(6):2181-2198.
45. Birrane G, Li H, Yang S, Tachado SD, Seng S. Cigarette smoke induces nuclear translocation of heme oxygenase 1 (HO-1) in prostate cancer cells: nuclear HO-1 promotes vascular endothelial growth factor secretion. Int J Oncol 2013, 42(6):1919-1928.
46. Tibullo D, Barbagallo I, Giallongo C, La Cava P, Parrinello N, Vanella L, Stagno F, Palumbo GA, Li Volti G, Di Raimondo F. Nuclear translocation of heme oxygenase-1 confers resistance to imatinib in chronic myeloid leukemia cells. Curr Pharm Des 2013, 19(15):2765-2770.
47. Watts RN, Richardson DR. Differential effects on cellular iron metabolism of the physiologically relevant diatomic effector molecules, NO and CO, that bind iron. Biochim Biophys Acta 2004, 1692(1):1-15.
48. Chung HT, Choi BM, Kwon YG, Kim YM. Interactive relations between nitric oxide (NO) and carbon monoxide (CO): heme oxygenase-1/CO pathway is a key modulator in NO-mediated antiapoptosis and anti-inflammation. Methods Enzymol 2008, 441:329-338.
49. Wegiel B, Gallo D, Csizmadia E, Harris C, Belcher J, Vercellotti GM, Penacho N, Seth P, Sukhatme V, Ahmed A, Pandolfi PP, Helczynski L, Bjartell A, Persson JL, Otterbein LE. Carbon monoxide expedites metabolic exhaustion to inhibit tumor growth. CancerRes 2013, 73(23):7009-7021.
50. Skrzypek K, Tertil M, Golda S, Ciesla M, Weglarczyk K, Collet G, Guichard A, Kozakowska M, Boczkowski J, Was H, Gil T, Kuzdzal J, Muchova L, Vitek L, Loboda A, Jozkowicz A, Kieda C, Dulak J. Interplay between heme oxygenase-1 and miR-378 affects non-small cell lung carcinoma growth, vascularization, and metastasis. Antioxid Redox Signal 2013, 19(7):644-660.
51. 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.
52. Berberat PO, Dambrauskas Z, Gulbinas A, Giese T, Giese N, Künzli B, Autschbach F, Meuer S, Büchler MW, Friess H. Inhibition of heme oxygenase-1 increases responsiveness of pancreatic cancer cells to anticancer treatment. Clin Cancer Res 2005, 11(10):3790-3798.