A metalloporphyrin antioxidant alters cytokine responses after irradiation in a prostate tumor model

Radiation Research

Volumn 173, Issue 4, 2010, Pages 441-452

  Makinde, Adeola Y ^a   Rizvi, Asma ^b   Crapo, James D ^c   Pearlstein, Robert D ^d   Slater, James M ^b   Gridley, Daila S ^a,b  

^a LOMA LINDA UNIVERSITY MEDICAL CENTER   (United States)

^b LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; COBALT 60; CYTOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 9; KERATINOCYTE DERIVED CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MANGANESE TETRAKIS(N ETHYLPYRIDINIUM 2 YL)PORPHYRIN; METALLOPORPHYRIN; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD SAMPLING; CANCER MODEL; CANCER RADIOTHERAPY; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; GAMMA RADIATION; HOMOGENATE; IMMUNE RESPONSE; MALE; MOUSE; MULTIPLEX BEAD ARRAY TECHNOLOGY; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; QUANTITATIVE ANALYSIS; RADIATION DOSE FRACTIONATION; SPLEEN; SPLEEN CELL; SUPERNATANT; T LYMPHOCYTE ACTIVATION; TECHNOLOGY;

ANIMALS; ANTIOXIDANTS; CELL LINE, TUMOR; COMBINED MODALITY THERAPY; CYTOKINES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; MALE; METALLOPORPHYRINS; MICE; MICE, INBRED C57BL; PROSTATIC NEOPLASMS; RADIATION DOSAGE; RADIOTHERAPY, CONFORMAL; TREATMENT OUTCOME;

MUS;

EID: 77950271104     PISSN: 00337587     EISSN: None     Source Type: Journal    
DOI: 10.1667/RR1765.1     Document Type: Article

References (63)

1. M. J. Zelefsky, H. Chan, M. Hunt, Y. Yamada, A. M. Shippy and H. Amols, Long term outcome of high dose intensity modulated radiation therapy for patients with clinically localized prostate cancer. J. Urol. 176, 1415-1419 (2006).
2. G. E. Hanks, L. R. Coia and J. Curry, Patterns of care studies: past, present, and future. Semin. Radiat. Oncol. 7, 97-100 (1997).
3. G. E. Hanks, K. L. Martz and J. J. Diamond, The effect of dose on local control of prostate cancer. Int. J. Radiat. Oncol. Biol. Phys. 15, 1299-1305 (1988).
4. S. R. Smalley, The effect of dose on local control of prostate cancer. Int. J. Radiat. Oncol. Biol. Phys. 17, 697-698 (1989).
5. M. R. Storey, A. Pollack, G. Zagars, L. Smith, J. Antolak and I. Rosen, Complications from radiotherapy dose escalation in prostate cancer: preliminary results of a randomized trial. Int. J. Radiat. Oncol. Biol. Phys. 48, 635-642 (2000).
6. L. J. Wu, G. Randers-Pehrson, A. Xu, C. A. Waldren, C. R. Geard, Z. Yu and T. K. Hei, Targeted cytoplasmic irradiation with alpha particles induces mutations in mammalian cells. Proc. Natl. Acad. Sci. USA 96, 4959-4964 (1999).
7. T. K. Lee and I. Stupans, Radioprotection: the non-steroidal anti-inflammatory drugs (NSAIDs) and prostaglandins. J. Pharm. Pharmacol. 54, 1435-1445 (2002).
8. I. Fridovich, Superoxide radical and superoxide dismutases. Annu. Rev. Biochem. 64, 97-112 (1995).
9. D. Salvemini, D. P. Riley and S. Cuzzocrea, SOD mimetics are coming of age. Nat. Rev. Drug Discov. 1, 367-374 (2002).
10. G. Ferrer-Sueta, D. Vitturi, I. Batinic-Haberle, I. Fridovich, S. Goldstein, G. Czapski and R. Radi, Reactions of manganese porphyrins with peroxynitrite and carbonate radical anion. J. Biol. Chem. 278, 27432-27438 (2003).
11. I. Spasojevic, I. Batinic-Haberle and I. Fridovich, Nitrosylation of manganese(II) tetrakis(N-ethylpyridinium-2-yl)porphyrin: a simple and sensitive spectrophotometric assay for nitric oxide. Nitric Oxide 4, 526-533 (2000).
12. G. Ferrer-Sueta, C. Quijano, B. Alvarez and R. Radi, Reactions of manganese porphyrins and manganese-superoxide dismutase with peroxynitrite. Methods Enzymol. 349, 23-37 (2002).
13. K. Shimizu, N. Rajapakse, T. Horiguchi, R. M. Payne and D. W. Busija, Protective effect of a new nonpeptidyl mimetic of SOD, M40401, against focal cerebral ischemia in the rat. Brain Res. 963, 8-14 (2003).
14. R. P. Bowler, H. Sheng, J. J. Enghild, R. D. Pearlstein, D. S. Warner and J. D. Crapo, A catalytic antioxidant (AEOL 10150) attenuates expression of inflammatory genes in stroke. Free Radic. Biol. Med. 33, 1141-1152 (2002).
15. K. Haskins, B. Bradley, K. Powers, V. Fadok, S. Flores, X. Ling, S. Pugazhenthi, J. Reusch and J. Kench, Oxidative stress in type 1 diabetes. Ann. NY Acad. Sci. 1005, 43-54 (2003).
16. D. K. Kaul, X. D. Liu, X. Zhang, L. Ma, C. J. Hsia and R. L. Nagel, Inhibition of sickle red cell adhesion and vasoocclusion in the microcirculation by antioxidants. Am. J. Physiol. Heart Circ. Physiol. 291, H167-H175 (2006).
17. S. Melov, J. A. Schneider, B. J. Day, D. Hinerfeld, P. Coskun, S. S. Mirra, J. D. Crapo and D. C. Wallace, A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase. Nat. Genet. 18, 159-163 (1998).
18. B. J. Traynor, L. Bruijn, R. Conwit, F. Beal, G. O'Neill, S. C. Fagan and M. E. Cudkowicz, Neuroprotective agents for clinical trials in ALS: a systematic assessment. Neurology 67, 20-27 (2006).
19. L. Y. Chang and J. D. Crapo, Inhibition of airway inflammation and hyperreactivity by an antioxidant mimetic. Free Radic. Biol. Med. 33, 379-386 (2002).
20. E. Masini, D. Bani, A. Vannacci, S. Pierpaoli, P. F. Mannaioni, S. A. Comhair, W. Xu, C. Muscoli, S. C. Erzurum and D. Salvemini, Reduction of antigen-induced respiratory abnormalities and airway inflammation in sensitized guinea pigs by a superoxide dismutase mimetic. Free Radic. Biol. Med. 39, 520-531 (2005).
21. K. R. Smith, D. L. Uyeminami, U. P. Kodavanti, J. D. Crapo, L. Y. Chang and K. E. Pinkerton, Inhibition of tobacco smoke-induced lung inflammation by a catalytic antioxidant. Free Radic. Biol. Med. 33, 1106-1114 (2002).
22. H. M. Tse, M. J. Milton and J. D. Piganelli, Mechanistic analysis of the immunomodulatory effects of a catalytic antioxidant on antigen-presenting cells: implication for their use in targeting oxidation-reduction reactions in innate immunity. Free Radic. Biol. Med. 36, 233-247 (2004).
23. Z. N. Rabbani, F. K. Salahuddin, P. Yarmolenko, I. Batinic-Haberle, B. A. Thrasher, B. Gauter-Fleckenstein, M. W. Dewhirst, M. S. Anscher and Z. Vujaskovic, Low molecular weight catalytic metalloporphyrin antioxidant AEOL 10150 protects lungs from fractionated radiation. Free Radic. Res. 41, 1273-1282 (2007).
24. A. Y. Makinde, X. Luo-Owen, A. Rizvi, J. D. Crapo, R. D. Pearlstein, J. M. Slater and D. S. Gridley, Effect of a metalloporphyrin antioxidant (MnTE-2-PyP) on the response of a mouse prostate cancer model to radiation. Anticancer Res. 29, 107-118 (2009).
25. D. S. Gridley, A. Y. Makinde, X. Luo, A. Rizvi, J. D. Crapo, M. W. Dewhirst, B. J. Moeller, R. D. Pearlstein and J. M. Slater, Radiation and a metalloporphyrin radioprotectant in a mouse prostate tumor model. Anticancer Res. 27, 3101-3109 (2007).
26. B. J. Moeller, I. Batinic-Haberle, I. Spasojevic, Z. N. Rabbani, M. S. Anscher, Z. Vujaskovic and M. W. Dewhirst, A manganese porphyrin superoxide dismutase mimetic enhances tumor radio-responsiveness. Int. J. Radiat. Oncol. Biol. Phys. 63, 545-552 (2005).
27. T. C. Thompson, T. L. Timme, S. H. Park, G. Yang and C. Ren, Mouse prostate reconstitution model system: A series of in vivo and in vitro models for benign and malignant prostatic disease. Prostate 43, 248-254 (2000).
28. G. M. Miller, M. L. Andres and D. S. Gridley, NK cell depletion results in accelerated tumor growth and attenuates the antitumor effect of total body irradiation. Int. J. Oncol. 23, 1585-1592 (2003).
29. G. Zurawski and J. E. de Vries, Interleukin 13, an interleukin 4-like cytokine that acts on monocytes and B cells, but not on T cells. Immunol. Today 15, 19-26 (1994).
30. M. Terabe, J. Park and J. Berzofsky, Role of IL-13 in regulation of anti-tumor immunity and tumor growth. Cancer Immunol, Immunother. 53, 79-85 (2004).
31. S. K. Manna and B. B. Aggarwal, IL-13 suppresses TNF-induced activation of nuclear factor-kappa B, activation protein-1, and apoptosis. J. Immunol. 161, 2863-2872 (1998).
32. C. Conticello, F. Pedini, A. Zeuner, M. Patti, M. Zerilli, G. Stassi, A. Messina, C. Peschle and R. De Maria, IL-4 protects tumor cells from anti-CD95 and chemotherapeutic agents via up-regulation of antiapoptotic proteins. J. Immunol. 172, 5467-5477 (2004).
33. Z. Li, J. Jiang, Z. Wang, J. Zhang, M. Xiao, C. Wang, Y. Lu and Z. Qin, Endogenous interleukin-4 promotes tumor development by increasing tumor cell resistance to apoptosis. Cancer Res. 68, 8687-8694 (2008).
34. S. M. Pope, E. B. Brandt, A. Mishra, S. P. Hogan, N. Zimmermann, K. I. Matthaei, P. S. Foster and M. E. Rothenberg, IL-13 induces eosinophil recruitment into the lung by an IL-5-and eotaxin-dependent mechanism. J. Allergy Clin. Immunol. 108, 594-601 (2001).
35. Y. Becker, Molecular immunological approaches to biotherapy of human cancers\a review, hypothesis and implications. Anticancer Res. 26, 1113-1134 (2006).
36. M. Todaro, Y. Lombardo, M. G. Francipane, M. P. Alea, P. Cammareri, F. Iovino, A. B. Di Stefano, C. Di Bernardo, A. Agrusa and G. Stassi, Apoptosis resistance in epithelial tumors is mediated by tumor-cell-derived interleukin-4. Cell Death Differ. 15, 762-772 (2008).
37. C. Jakubzick, S. Kunkel, R. Puri and C. Hogaboam, Therapeutic targeting of IL-4-and IL-13-responsive cells in pulmonary fibrosis. Immunol. Res. 30, 339-349 (2004).
38. W. Westermann, R. Schobl, E. P. Rieber and K. H. Frank, Th2 cells as effectors in postirradiation pulmonary damage preceding fibrosis in the rat. Int. J. Radiat. Biol. 75, 629-638 (1999).
39. O. Akbari, P. Stock, E. Meyer, M. Kronenberg, S. Sidobre, T. Nakayama, M. Taniguchi, M. J. Grusby, R. H. DeKruyff and D. T. Umetsu, Essential role of NKT cells producing IL-4 and IL-13 in the development of allergen-induced airway hyperreactivity. Nat. Med. 9, 582-588 (2003).
40. B. Bierie and H. L. Moses, TGF-beta and cancer. Cytokine Growth Factor Rev. 17, 29-40 (2006).
41. C. Abate-Shen and M. M. Shen, Molecular genetics of prostate cancer. Genes Dev. 14, 2410-2434 (2000).
42. J. Rich, A. Borton and X. Wang, Transforming growth factor-beta signaling in cancer. Microsc. Res. Tech. 52, 363-373 (2001).
43. J. J. Letterio and A. B. Roberts, Regulation of immune responses by TGF-beta. Annu. Rev. Immunol. 16, 137-161 (1998).
44. B. A. Teicher, Transforming growth factor-beta and the immune response to malignant disease. Clin. Cancer Res. 13, 6247-6251 (2007).
45. T. Fujita, K. Teramoto, Y. Ozaki, J. Hanaoka, N. Tezuka, Y. Itoh, T. Asai, S. Fujino, K. Kontani and K. Ogasawara, Inhibition of transforming growth factor-beta-mediated immunosuppression in tumor-draining lymph nodes augments antitumor responses by various immunologic cell types. Cancer Res. 69, 5142-5150 (2009).
46. S. H. Wrzesinski, Y. Y. Wan and R. A. Flavell, Transforming growth factor-beta and the immune response: implications for anticancer therapy. Clin. Cancer Res. 13, 5262-5270 (2007).
47. Y. Y. Wan and R. A. Flavell, 'Yin-Yang' functions of transforming growth factor-beta and T regulatory cells in immune regulation. Immunol. Rev. 220, 199-213 (2007).
48. Y. Y. Wan and R. A. Flavell, Regulatory T cells, transforming growth factor-beta, and immune suppression. Proc. Am. Thorac. Soc. 4, 271-276 (2007).
49. Y. Nasu, C. H. Bangma, G. W. Hull, G. Yang, J. Wang, S. Shimura, M. A. McCurdy, S. Ebara, H. M. Lee and T. C. Thompson, Combination gene therapy with adenoviral vector-mediated HSV-tkzGCV and IL-12 in an orthotopic mouse model for prostate cancer. Prostate Cancer Prostatic Dis. 4, 44-55 (2001).
50. D. Pohlers, J. Brenmoehl, I. Loffler, C. K. Muller, C. Leipner, S. Schultze-Mosgau, A. Stallmach, R. W. Kinne and G. Wolf, TGF-beta and fibrosis in different organs\molecular pathway imprints. Biochim. Biophys. Acta 1792, 746-756 (2009).
51. P. Allavena, C. Garlanda, M. G. Borrello, A. Sica and A. Mantovani, Pathways connecting inflammation and cancer. Curr. Opin. Genet. Dev. 18, 3-10 (2008).
52. Y. Manome, P. Y. Wen, A. Hershowitz, T. Tanaka, B. J. Rollins, D.W. Kufe and H. A. Fine, Monocyte chemoattractant protein-1 (MCP-1) gene transduction: an effective tumor vaccine strategy for non-intracranial tumors. Cancer Immunol. Immunother. 41, 227-235 (1995).
53. C. Lamagna, M. Aurrand-Lions and B. A. Imhof, Dual role of macrophages in tumor growth and angiogenesis. J. Leukoc. Biol. 80, 705-713 (2006).
54. C. E. Lewis and J. W. Pollard, Distinct role of macrophages in different tumor microenvironments. Cancer Res. 66, 605-612 (2006).
55. T. D. Kim, G. Li, K. S. Song, J. M. Kim, J. S. Kim, E. J. Yun, J. I. Park, H. D. Park, B. D. Hwang and W. H. Yoon, Radiation-induced thymidine phosphorylase upregulation in rectal cancer is mediated by tumor-associated macrophages by monocyte chemoattractant protein-1 from cancer cells. Int. J. Radiat. Oncol. Biol. Phys. 73, 853-860 (2009).
56. Y. Yamamoto, M. Toi, S. Kondo, T. Matsumoto, H. Suzuki, M. Kitamura, K. Tsuruta, T. Taniguchi, A. Okamoto and T. Tominaga, Concentrations of vascular endothelial growth factor in the sera of normal controls and cancer patients. Clin. Cancer Res. 2, 821-826 (1996).
57. G. Frumento, T. Piazza, E. Di Carlo and S. Ferrini, Targeting tumor-related immunosuppression for cancer immunotherapy. Endocr. Metab. Immune Disord. Drug Targets 6, 233-237 (2006).
58. D. O. Croci, M. F. Zacarias Fluck, M. J. Rico, P. Matar, G. A. Rabinovich and O. G. Scharovsky, Dynamic cross-talk between tumor and immune cells in orchestrating the immunosuppressive network at the tumor microenvironment. Cancer Immunol. Immunother. 56, 1687-1700 (2007).
59. S. Kusmartsev and D. I. Gabrilovich, Immature myeloid cells and cancer-associated immune suppression. Cancer Immunol. Immunother. 51, 293-298 (2002).
60. S. Kusmartsev and D. I. Gabrilovich, Role of immature myeloid cells in mechanisms of immune evasion in cancer. Cancer Immunol. Immunother. 55, 237-245 (2006).
61. C. A. Corzo, M. J. Cotter, P. Cheng, F. Cheng, S. Kusmartsev, E. Sotomayor, T. Padhya, T. V. McCaffrey, J. C. McCaffrey and D. I. Gabrilovich, Mechanism regulating reactive oxygen species in tumor-induced myeloid-derived suppressor cells. J. Immunol. 182, 5693-5701 (2009).
62. K. J. Malmberg, Effective immunotherapy against cancer: a question of overcoming immune suppression and immune escape? Cancer Immunol. Immunother. 53, 879-892 (2004).
63. T. H. Brill, H. R. Kubler, H. von Randenborgh, F. Fend, H. Pohla, J. Breul, R. Hartung, R. Paul, D. J. Schendel and B. Gansbacher, Allogeneic retrovirally transduced, IL-2-and IFN-gamma-secreting cancer cell vaccine in patients with hormone refractory prostate cancer\a phase I clinical trial. J. Gene Med. 9, 547-560 (2007).