Heme oxygenase-1 inhibits rat and human breast cancer cell proliferation: Mutual cross inhibition with indoleamine 2,3-dioxygenase

FASEB Journal

Volumn 19, Issue 14, 2005, Pages 1957-1968

  Hill, Marcelo ^a   Pereira, Victoria ^b   Chauveau, Christine ^a   Zagani, Rachid ^a   Remy, Séverine ^a   Tesson, Laurent ^a   Mazal, Daniel ^b   Ubillos, Luis ^b   Brion, Régis ^a   Ashgar, Kashif ^c   Mashreghi, Mir Farzin ^c   Kotsch, Katja ^c   Moffett, John ^d   Doebis, Cornelia ^c   Seifert, Martina ^c   Boczkowski, Jorge ^a   Osinaga, Eduardo ^b   Anegon, Ignacio ^a  

^a INSERM   (France)

^b DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

Apoptosis; Breast cancer; HO 1; IDO; Proliferation

Indexed keywords

ANTIOXIDANT; HEME OXYGENASE 1; INDOLEAMINE 2,3 DIOXYGENASE; KYNURENIC ACID; METHYLNITROSOUREA; SMALL INTERFERING RNA; TRYPTOPHAN;

ANIMAL CELL; APOPTOSIS; ARTICLE; BREAST ADENOCARCINOMA; BREAST CANCER; CANCER CELL CULTURE; CATABOLISM; CELL PROLIFERATION; CELL STRAIN MCF 7; CELL STRAIN T47D; ENZYME INHIBITION; GENE OVEREXPRESSION; GENETIC REGULATION; HEME SYNTHESIS; HUMAN; HUMAN CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE FIBER; STARVATION;

ANIMALIA; MINK CELL FOCUS-FORMING VIRUS;

EID: 28744447937     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.05-3875com     Document Type: Article

References (57)

1. Evan, G. I., and Vousden, K. H. (2001) Proliferation, cell cycle and apoptosis in cancer. Nature (London) 411, 342-348
2. Hanahan, D., and Weinberg, R. A. (2000) The hallmarks of cancer. Cell 100, 57-70
3. Kaufmann, S. H., and Vaux, D. L. (2003) Alterations in the apoptotic machinery and their potential role in anticancer drug resistance. Oncogene 22, 7414-7430
4. Khong, H. T., and Restifo, N. P. (2002) Natural selection of tumor variants in the generation of "tumor escape" phenotypes. Nat. Immunol. 3, 999-1005
5. Brown, N. S., and Bicknell, R. (2001) Hypoxia and oxidative stress in breast cancer. Oxidative stress: its effects on the growth, metastatic potential and response to therapy of breast cancer. Breast Cancer Res. 3, 323-327
6. Burdick, A. D., Davis, J. W., II, Liu, K. J., Hudson, L. G., Shi, H., Monske, M. L., and Burchiel, S. W. (2003) Benzo(a)pyrene quinones increase cell proliferation, generate reactive oxygen species, and transactivate the epidermal growth factor receptor in breast epithelial cells. Cancer Res. 63, 7825-7833
7. Policastro, L., Molinari, B., Larcher, F., Blanco, P., Podhajcer, O. L., Costa, C. S., Rojas, P., and Duran, H. (2004) Imbalance of antioxidant enzymes in tumor cells and inhibition of proliferation and malignant features by scavenging hydrogen peroxide. Mol. Carcinog. 39, 103-113
8. Kampa, M., Alexaki, V. I., Notas, G., Nifli, A. P., Nistikaki, A., Hatzoglou, A., Bakogeorgou, E., Kouimtzoglou, E., Blekas, G., Boskou, D., et al. (2004) Antiproliferative and apoptotic effects of selective phenolic acids on T47D human breast cancer cells: potential mechanisms of action. Breast Cancer Res. 6, R63-R74
9. Maines, M. D. (1997) The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 37, 517-554
10. Choi, A. M., and Alam, J. (1996) Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am. J. Respir. Cell Mol. Biol. 15, 9-19
11. Otterbein, L. E., Soares, M. P., Yamashita, K., and Bach, F. H. (2003) Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol. 24, 449-455
12. Zhang, M., Zhang, B. H., Chen, L., and An, W. (2002) Overexpression of heme oxygenase-1 protects smooth muscle cells against oxidative injury and inhibits cell proliferation. Cell Res. 12, 123-132
13. Taille, C., Almolki, A., Benhamed, M., Zedda, C., Megret, J., Berger, P., Leseche, G., Fadel, E., Yamaguchi, T., Marthan, R., et al. (2003) Heme oxygenase inhibits human airway smooth muscle proliferation via a bilirubin-dependent modulation of ERK1/2 phosphorylation. J. Biol. Chem. 278, 27160-27168
14. Fang, J., Sawa, T., Akaike, T., Akuta, T., Sahoo, S. K., Khaled, G., Hamada, A., and Maeda, H. (2003) In vivo antitumor activity of pegylated zinc protoporphyrin: targeted inhibition of heme oxygenase in solid tumor. Cancer Res. 63, 3567-3574
15. Tanaka, S., Akaike, T., Fang, J., Beppu, T., Ogawa, M., Tamura, F., Miyamoto, Y., and Maeda, H. (2003) Antiapoptotic effect of haem oxygenase-1 induced by nitric oxide in experimental solid tumour. Br. J. Cancer 88, 902-909
16. Sunamura, M., Duda, D. G., Ghattas, M. H., Lozonschi, L., Motoi, F., Yamauchi, J., Matsuno, S., Shibahara, S., and Abraham, N. G. (2003) Heme oxygenase-1 accelerates tumor angiogenesis of human pancreatic cancer. Angiogenesis 6, 15-24
17. Yanagawa, T., Omura, K., Harada, H., Nakaso, K., Iwasa, S., Koyama, Y., Onozawa, K., Yusa, H., and Yoshida, H. (2004) Heme oxygenase-1 expression predicts cervical lymph node metastasis of tongue squamous cell carcinomas. Oral Oncol. 40, 21-27
18. Shimizu, T., Nomiyama, S., Hirata, F., and Hayaishi, O. (1978) Indoleamine 2,3-dioxygenase. Purification and some properties. J. Biol. Chem. 253, 4700-4706
19. Takikawa, O., Kuroiwa, T., Yamazaki, F., and Kido, R. (1988) Mechanism of interferon-gamma action. Characterization of indoleamine 2,3-dioxygenase in cultured human cells induced by interferon-gamma and evaluation of the enzyme-mediated tryptophan degradation in its anticellular activity. J. Biol. Chem. 263, 2041-2048
20. Uyttenhove, C., Pilotte, L., Theate, I., Stroobant, V., Colau, D., Parmentier, N., Boon, T., and Van den Eynde, B. J. (2003) Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat. Med. 9, 1269-1274
21. Hill, M., Bausero, M. A., Mazal, D., Ménoret, S., Khalife, J., Anegon, I., and Osinaga, E. (2004) Immunobiological characterization of N-nitrosomethylurea-induced rat breast carcinomas: tumoral IL-10 expression as a possible immune escape mechanism. Breast Cancer Res. Treat. 84, 107-116
22. Moffett, J. R., Espey, M. G., Gaudet, S. J., and Namboodiri, M. A. (1993) Antibodies to quinolinic acid reveal localization in select immune cells rather than neurons or astroglia. Brain Res. 623, 337-340
23. Shimizu, S., Izumi, Y., Yamazaki, M., Shimizu, K., Yamaguchi, T., and Nakajima, H. (1988) Anti-bilirubin monoclonal antibody. I. Preparation and properties of monoclonal antibodies to covalently coupled bilirubin-albumin. Biochim. Biophys. Acta 967, 255-260
24. Cohen, L. A. (1982) Isolation and characterization of a serially cultivated, neoplastic, epithelial cell line from the N-nitrosomethylurea induced rat mammary adenocarcinoma. In Vitro 18, 565-575
25. Fallarino, F., Vacca, C., Orabona, C., Belladonna, M. L., Bianchi, R., Marshall, B., Keskin, D. B., Mellor, A. L., Fioretti, M. C., Grohmann, U., et al. (2002) Functional expression of indoleamine 2,3-dioxygenase by murine CD8 alpha(+) dendritic cells. Int. Immunol. 14, 65-68
26. Bloxam, D. L., and Warren, W. H. (1974) Error in the determination of tryptophan by the method of Denkla and Dewey. A revised procedure. Anal. Biochem. 60, 621-625
27. Werner-Felmayer, G., Werner, E. R., Fuchs, D., Hausen, A., Reibnegger, G., and Wachter, H. (1989) Characteristics of interferon induced tryptophan metabolism in human cells in vitro. Biochim. Biophys. Acta 1012, 140-147
28. Chauveau, C., Bouchet, D., Roussel, J.-C., Mathieu, P., Braudeau, C., Renaudin, K., Tesson, L., Soulillou, J.-P., Buelow, R., and Anegon, I. (2002) Gene transfer of heme-oxygenase 1 and carbon monoxyde delivery inhibit chronic rejection. Am. J. Transplant. 2, 581-592
29. Follenzi, A., Ailles, L. E., Bakovic, S., Geuna, M., and Naldini, L. (2000) Gene transfer by lentiviral vectors is limited by nuclear translocation and rescued by HIV-1 pol sequences. Nat. Genet. 25, 217-222
30. Brouard, S., Otterbein, L. E., Anrather, J., Tobiasch, E., Bach, F. H., Choi, A. M., and Soares, M. P. (2000) Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J. Exp. Med. 192, 1015-1026
31. Drummond, G. S., and Kappas, A. (1981) Prevention of neonatal hyperbilirubinemia by tin protoporphyrin IX, a potent competitive inhibitor of heme oxidation. Proc. Natl. Acad. Sci. USA 78, 6466-6470
32. Yoshinaga, T., Sassa, S., and Kappas, A. (1982) Purification and properties of bovine spleen heme oxygenase. Amino acid composition and sites of action of inhibitors of heme oxidation. J. Biol. Chem. 257, 7778-7785
33. McDaid, J., Yamashita, K., Chora, A., Ollinger, R., Strom, T. B., Li, X. C., Bach, F. H., and Soares, M. P. (2005) Heme oxygenase-1 modulates the allo-immune response by promoting activation-induced cell death of T cells. FASEB J. 458-460
34. Cady, S. G., and Sono, M. (1991) 1-Methyl-DL-tryptophan, beta-(3-benzofuranyl)-DL-alanine (the oxygen analog of tryptophan), and beta-[3-benzo(b)thienyl]-DL-alanine (the sulfur analog of tryptophan) are competitive inhibitors for indoleamine 2,3-dioxygenase. Arch. Biochem. Biophys. 291, 326-333
35. Hwu, P., Du, M. X., Lapointe, R., Do, M., Taylor, M. W., and Young, H. A. (2000) Indoleamine 2,3-dioxygenase production by human dendritic cells results in the inhibition of T cell proliferation. J. Immunol. 164, 3596-3599
36. Liu, Z. M., Chen, G. G., Ng, E. K., Leung, W. K., Sung, J. J., and Chung, S. S. (2004) Upregulation of heme oxygenase-1 and p21 confers resistance to apoptosis in human gastric cancer cells. Oncogene 23, 503-513
37. Mayerhofer, M., Florian, S., Krauth, M. T., Aichberger, K. J., Bilban, M., Marculescu, R., Printz, D., Fritsch, G., Wagner, O., Selzer, E., et al. (2004) Identification of heme oxygenase-1 as a novel BCR/ABL-dependent survival factor in chronic myeloid leukemia. Cancer Res. 64, 3148-3154
38. Lala, P. K., and Chakraborty, C. (2001) Role of nitric oxide in carcinogenesis and tumour progression. Lancet Oncol. 2, 149-156
39. Duckers, H. J., Boehm, M., True, A. L., Yet, S. F., San, H., Park, J. L., Clinton Webb, R., Lee, M. E., Nabel, G. J., and Nabel, E. G. (2001) Heme oxygenase-1 protects against vascular constriction and proliferation. Nat. Med. 7, 693-698
40. Ozawa, N., Goda, N., Makino, N., Yamaguchi, T., Yoshimura, Y., and Suematsu, M. (2002) Leydig cell-derived heme oxygenase-1 regulates apoptosis of premeiotic germ cells in response to stress. J. Clin. Invest. 109, 457-467
41. Liu, X. M., Chapman, G. B., Wang, H., and Durante, W. (2002) Adenovirus-mediated heme oxygenase-1 gene expression stimulates apoptosis in vascular smooth muscle cells. Circulation 105, 79-84
42. Chen, G. G., Liu, Z. M., Vlantis, A. C., Tse, G. M., Leung, B. C., and Van Hasselt, C. A. (2004) Heme oxygenase-1 protects against apoptosis induced by tumor necrosis factor-alpha and cycloheximide in papillary thyroid carcinoma cells. J. Cell. Biochem. 92, 1246-1256
43. Pozo-Guisado, E., Alvarez-Barrientos, A., Mulero-Navarro, S., Santiago-Josefat, B., and Fernandez-Salguero, P. M. (2002) The anti-proliferative activity of resveratrol results in apoptosis in MCF-7 but not in MDA-MB-231 human breast cancer cells: cell-specific alteration of the cell cycle. Biochem. Pharmacol. 64, 1375-1386
44. Song, R., Zhou, Z., Kim, P. K., Shapiro, R. A., Liu, F., Ferran, C., Choi, A. M., and Otterbein, L. E. (2004) Carbon monoxide promotes Fas/CD95-induced apoptosis in Jurkat cells. J. Biol. Chem. 279, 4423-4434.
45. Santen, R. J., Song, R. X., McPherson, R., Kumar, R., Adam, L., Jeng, M. H., and Yue, W. (2002) The role of mitogen-activated protein (MAP) kinase in breast cancer. J. Steroid Biochem. Mol. Biol. 80, 239-256
46. Shilkaitis, A., Green, A., Steele, V., Lubet, R., Kelloff, G., and Christov, K. (2000) Neoplastic transformation of mammary epithelial cells in rats is associated with decreased apoptotic cell death. Carcinogenesis 21, 227-233
47. Munn, D. H., Sharma, M. D., Hou, D., Baban, B., Lee, J. R., Antonia, S. J., Messina, J. L., Chandler, P., Koni, P. A., and Mellor, A. L. (2004) Expression of indoleamine 2,3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes. J. Clin. Invest. 114, 280-290
48. Xiao, B. G., Liu, X., and Link, H. (2004) Antigen-specific T cell functions are suppressed over the estrogen-dendritic cell-indoleamine 2,3-dioxygenase axis. Steroids 69, 653-659
49. Kudo, Y., Hara, T., Katsuki, T., Toyofuku, A., Katsura, Y., Kakikawa, O., Fujii, T., and Ohama, K. (2004) Mechanisms regulating the expression of indoleamine 2,3-dioxygenase during decidualization of human endometrium. Hum. Reprod. 19, 1222-1230
50. Thomas, S. R., Salahifar, H., Mashima, R., Hunt, N. H., Richardson, D. R., and Stocker, R. (2001) Antioxidants inhibit indoleamine 2,3-dioxygenase in IFN-gamma-activated human macrophages: posttranslational regulation by pyrrolidine dithiocarbamate. J. Immunol. 166, 6332-6340
51. Sono, M., Taniguchi, T., Watanabe, Y., and Hayaishi, O. (1980) Indoleamine 2,3-dioxygenase. Equilibrium studies of the tryptophan binding to the ferric, ferrous, and CO-bound enzymes. J. Biol. Chem. 255, 1339-1345
52. Turcanu, V., Dhouib, M., and Poindron, P. (1998) Heme oxygenase inhibits nitric oxide synthase by degrading heme: a negative feedback regulation mechanism for nitric oxide production. Transplant. Proc. 30, 4184-4185
53. Turcanu, V., Dhouib, M., and Poindron, P. (1998) Nitric oxide synthase inhibition by haem oxygenase decreases macrophage nitric-oxide-dependent cytotoxicity: a negative feedback mechanism for the regulation of nitric oxide production. Res. Immunol. 149, 741-744
54. Haider, A., Olszanecki, R., Gryglewski, R., Schwartzman, M. L., Lianos, E., Kappas, A., Nasjletti, A., and Abraham, N. G. (2002) Regulation of cyclooxygenase by the heme-heme oxygenase system in microvessel endothelial cells. J. Pharmacol. Exp. Ther. 300, 188-194
55. Taille, C., El-Benna, J., Lanone, S., Dang, M. C., Ogier-Denis, E., Aubier, M., and Boczkowski, J. (2004) Induction of heme oxygenase-1 inhibits NAD(P)H oxidase activity by down-regulating cytochrome b558 expression via the reduction of heme availability. J. Biol. Chem. 279, 28681-28688
56. Oh, G. S., Pae, H. O., Choi, B. M., Chae, S. C., Lee, H. S., Ryu, D. G., and Chung, H. T. (2004) 3-Hydroxyanthranilic acid, one of metabolites of tryptophan via indoleamine 2,3-dioxygenase pathway, suppresses inducible nitric oxide synthase expression by enhancing heme oxygenase-1 expression. Biochem. Biophys. Res. Commun. 320, 1156-1162
57. Munn, D. H., Sharma, M. D., Baban, B., Harding, H. P., Zhang, Y., Ron, D., and Mellor, A. L. (2005) GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity 22, 633-642