Nitrosylhemoglobin in photodynamically stressed human tumors growing in nude mice

Nitric Oxide - Biology and Chemistry

Volumn 35, Issue , 2013, Pages 79-88

  Jakubowska, Monika ^a   Michalczyk Wetula, Dominika ^a   Pyka, Janusz ^a   Susz, Anna ^a   Urbanska, Krystyna ^a   Płonka, Beata K ^a   Kuleta, Patryk ^a   Ła̧cki, Piotr ^a   Krzykawska Serda, Martyna ^a   Fiedor, Leszek ^a   Płonka, Przemysław M ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

Adenocarcinoma; Electron paramagnetic resonance; Nitric oxide; Photodynamic therapy; Zinc pheophorbide a

Indexed keywords

NITRIC OXIDE; NITROSYLHEMOGLOBIN; TUMOR MARKER; UNCLASSIFIED DRUG; HEMOGLOBIN; NITROSYL HEMOGLOBIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; EXTRAVASATION; HISTOLOGY; LIVER; LUNG ADENOCARCINOMA; MOUSE; NONHUMAN; PHOTODYNAMIC THERAPY; PHOTODYNAMICS; PRIORITY JOURNAL; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CHEMISTRY; HUMAN; MALE; METABOLISM; NEOPLASMS, EXPERIMENTAL; NUDE MOUSE; PATHOLOGY; PHOTOCHEMOTHERAPY; RADIATION RESPONSE; SPLEEN; TUMOR CELL LINE; XENOGRAFT;

MUS MUSCULUS;

ANIMALS; CELL LINE, TUMOR; ELECTRON SPIN RESONANCE SPECTROSCOPY; HEMOGLOBINS; HETEROGRAFTS; HUMANS; LIVER; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, NUDE; NEOPLASMS, EXPERIMENTAL; NITRIC OXIDE; PHOTOCHEMOTHERAPY; SPLEEN;

EID: 84884340929     PISSN: 10898603     EISSN: 10898611     Source Type: Journal    
DOI: 10.1016/j.niox.2013.08.004     Document Type: Article

References (67)

1. D. Ingram, and J. Bennett Paramagnetic resonance in phthalocyanine, haemoglobin, and other organic derivatives Discuss. Faraday Soc. 19 1955 140 146
2. W. Gordy, and H. Rexroad Electron paramagnetic resonance studies of cytochrome and hemoglobin (irradiated and unirradiated) M.J. Blois, H. Brown, R. Lemmon, R. Lindblom, M. Weissbluth, Free Radicals in Biological Systems. Proceedings of a Symposium Held at Stanford University, March, 1960 1961 Academic Press New York, London 263 278
3. N.M. Emanuel, A.N. Saprin, V.A. Shabalkin, L.E. Kozlova, and K.E. Krugljakova Detection and investigation of a new type of ESR signal characteristic of some tumour tissues Nature 222 1969 165 167
4. M.J. Brennan, T. Cole, and J.A. Singley A unique hyperfine ESR spectrum in mouse neoplasms analyzed by computer simulation Proc. Soc. Exp. Biol. Med. 123 1966 715 718
5. Y.J. Azhipa, L.P. Kaiushin, and E.I. Nikishkin Electron spin resonance in animal tissues in some kinds of tissue hypoxia Biofizika 11 1966 710 713 [Article in Russian]
6. T. Maruyama, N. Kataoka, S. Nagase, H. Nakada, H. Sato, and H. Sasaki Identification of three-line electron spin resonance signal and its relationship to ascites tumors Cancer Res. 31 1971 179 184
7. A.F. Vanin, P.I. Mordvintsev, and A.L. Kleshchov Nitrogen oxide appearance in animal tissues in vivo Studia Biophys. 192 1984 135 143 [Article in Russian]
8. R.M. Palmer, A.G. Ferrige, and S. Moncada Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor Nature 327 1987 524 526 (Pubitemid 17085822)
9. S. Lukiewicz, and J.L. Zweier Nitric Oxide in Transplant Rejection and Anti-Tumour Defense 1998 Kluwer Academic Publishers Boston/Dordrecht/London
10. D.C. Jenkins, I.G. Charles, L.L. Thomsen, D.W. Moss, L.S. Holmes, S.A. Baylis, P. Rhodes, K. Westmore, P.C. Emson, and S. Moncada Roles of nitric oxide in tumor growth Proc. Natl. Acad. Sci. U.S.A. 92 1995 392 396
11. P.K. Lala, and C. Chakraborty Role of nitric oxide in carcinogenesis and tumor progression Lancet Oncol. 2 2001 149 156 (Pubitemid 33585926)
12. J.A. Coulter, N.L. Page, J. Worthington, T. Robson, D.G. Hirst, and H.O. McCarthy Transcriptional regulation of inducible nitric oxide synthase gene therapy: targeting early stage and advanced prostate cancer J. Gene Med. 12 2010 755 765
13. P. Plonka, B. Plonka, K. Cieszka, J. Raczek, and S. Lukiewicz EPR analysis of tumor-host interactions S. Lukiewicz, J.Z. Zweier, Nitric Oxide in Transplant Rejection and Anti-tumor Defense 1998 Kluwer Academic Publishers Boston/Dordrecht/London 313 326
14. P.M. Plonka, B.K. Plonka, S. Pajak, and S.J. Lukiewicz ESR studies on the generation of nitric oxide in rejecting rat heart allografts and in situ growing tumors Curr. Top. Biophys. 20 1 1996 46 52
15. C.Y. Yim, N.R. Bastian, J.C. Smith, J.B.J. Hibbs, and W.E. Samlowski Macrophage nitric oxide synthesis delays progression of ultraviolet light-induced murine skin cancers Cancer Res. 53 1993 5507 5511 (Pubitemid 23342175)
16. H. Kusnierczyk, E. Pajtasz-Piasecka, J.W. Koten, C. Bijleveld, K. Krawczyk, and W. Den Otter Further development of local IL-2 therapy of cancer: multiple versus single IL-2 treatment of transplanted murine colon carcinoma Cancer Immunol. Immunother. 53 2004 445 452 (Pubitemid 38678534)
17. U. Westenberger, S. Thanner, H.H. Ruf, K. Gersonde, G. Sutter, and O. Trentz Formation of free radicals and nitric oxide derivative of hemoglobin in rats during shock syndrome Free Radic. Res. Commun. 11 1990 167 178
18. P.M. Plonka, S. Chlopicki, B.K. Plonka, J. Jawien, and R.J. Gryglewski Endotoxaemia in rats: detection of nitrosyl-haemoglobin in blood and lung by EPR Curr. Top. Biophys. 23 1999 47 53
19. w-Monomethyl-L-Arginine inhibits nitric oxide production in murine cardiac allografts but does not affect graft rejection Biochim. Biophys. Acta 1226 1994 225 231
20. S.J. Lukiewicz, P. Plonka, and J.L. Zweier Measurement of nitric oxide generation in heart transplant rejection using electron paramagnetic resonance spectroscopy J. Magn. Reson. Anal. 1 1995 4 8
21. J.R.J. Lancaster, J.M. Langrehr, H.A. Bergonia, N. Murase, R.L. Simmons, and R.A. Hoffman EPR detection of heme and nonheme iron-containing protein nitrosylation by nitric oxide during rejection of rat heart allograft J. Biol. Chem. 267 1992 10994 10998
22. J.A. Coulter, H.O. McCarthy, J. Xiang, W. Roedl, E. Wagner, T. Robson, and D.G. Hirst Nitric oxide - a novel therapeutic for cancer Nitric Oxide 19 2008 192 198
23. E. Galea, and D.L. Feinstein Regulation of the expression of the inflammatory nitric oxide synthase (NOS2) by cyclic AMP FASEB J. 13 1999 2125 2137
24. B.S. Taylor, and D.A. Geller Molecular regulation of the human inducible nitric oxide synthase (iNOS) gene Shock 13 2000 413 424
25. W.E. Salmowski, J.R. McGregor, and N.R. Bastian Identification of nitric oxide-derived EPR signals in human cancers S. Lukiewicz, J.Z. Zweier, Nitric Oxide in Transplant Rejection and Anti-tumor Defense 1998 Kluwer Academic Publishers Boston/Dordrecht/London 341 352
26. S. Loibl, G. von Minckwitz, S. Weber, H.P. Sinn, V.B. Schini-Kerth, I. Lobysheva, F. Nepveu, G. Wolf, K. Strebhardt, and M. Kaufmann Expression of endothelial and inducible nitric oxide synthase in benign and malignant lesions of the breast and measurement of nitric oxide using electron paramagnetic resonance spectroscopy Cancer 95 2002 1191 1198 (Pubitemid 35013051)
27. M.C. Symons, I.J. Rowland, N. Deighton, K. Shorrock, and K.P. West Electron spin resonance studies of nitrosyl haemoglobin in human liver, colon and stomach tumour tissues Free Radic. Res. 21 1994 197 202 (Pubitemid 2137680)
28. M. Elas, J. Raczek, A. Bratasz, B. Rudnicka, K. Krawczyk, R. Szypułka, K. Hodor, and S. Lukiewicz Paramagnetic center observed in human tumors by EPR technique Curr. Top. Biophys. 23 1999 39 45
29. E.M. Pantelouris Absence of thymus in a mouse mutant Nature 217 1968 370 371
30. E.M. Pantelouris, and J. Hari Thymus dysgenesis in nude (nu nu) mice J. Embryol. Exp. Morphol. 24 1970 615 623
31. T.J. Dougherty, C.J. Gomer, B.W. Henderson, G. Jori, D. Kessel, M. Korbelik, J. Moan, and Q. Peng Photodynamic therapy J. Natl. Cancer Inst. 90 1998 889 905 (Pubitemid 28304157)
32. D. Nowis, and J. Golab Photodynamic therapy and oxidative stress M.R. Hamblin, P. Mróz, Advances in Photodynamic Therapy. Basic, Translational, and Clinical 2008 Artech House Boston/London 151 178
33. P. Agostinis, K. Berg, K. Cengel, T. Foster, A. Girotti, S. Gollnick, S. Hahn, M. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, M. Mroz, D. Nowis, J. Piette, B. Wilson, and J. Golab Photodynamic therapy of cancer: an update CA Cancer J. Clin. 61 2011 250 281
34. M. Jakubowska, M. Szczygiel, D. Michalczyk-Wetula, A. Susz, G. Stochel, M. Elas, L. Fiedor, and K. Urbanska Zinc-pheophorbide a-highly efficient low-cost photosensitizer against human adenocarcinoma in cellular and animal models Photodiagn. Photodyn. Ther. 10 2013 266 277
35. A.P. Castano, P. Mroz, and M.R. Hamblin Photodynamic therapy and anti-tumour immunity Nature Rev. Cancer 6 2006 535 545 (Pubitemid 43980542)
36. M. Ochsner Photophysical and photobiological processes in the photodynamic therapy of tumors J. Photochem. Photobiol. B: Biol. 39 1996 1 18
37. L. Fiedor, A. Kania, B. Myśliwa-Kurdziel, Ł. Orzeł, and G. Stochel Understanding chlorophylls: central magnesium ion and phytyl as structural determinants Biochim. Biophys. Acta 1777 2008 1491 1500
38. A. Drzewiecka-Matuszek, A. Skalna, A. Karocki, G. Stochel, and L. Fiedor Effects of heavy central metal on the ground and excited states of chlorophyll J. Biol. Inorg. Chem. 10 2005 453 462 (Pubitemid 41400734)
39. L. Fiedor, A.A. Gorman, I. Hamblett, V. Rosenbach-Belkin, Y. Salomon, A. Scherz, and I. Tregub A pulsed laser and pulse radiolysis study of amphiphilic chlorophyll derivatives with PDT activity toward malignant melanoma Photochem. Photobiol. 5 1993 506 511 (Pubitemid 2001662)
40. A.S. Brandis, Y. Salomon, and A. Scherz Chlorophyll sensitizers in photodynamic therapy B. Grimm, R.J. Porra, W. Rudiger, H. Scheer, Chlorophylls and Bacteriochlorophylls. Biochemistry, Biophysics, Functions and Applications 2006 Springer Dordrecht 462 483
41. A.S. Brandis, Y. Salomon, and A. Scherz Bacteriochlorophyll sensitizers in photodynamic therapy B. Grimm, R.J. Porra, W. Rudiger, H. Scheer, Chlorophylls and Bacteriochlorophylls. Biochemistry, Biophysics, Functions and Applications 2006 Springer Dordrecht 485 506
42. M. Szczygieł, K. Urbanska, P. Jurecka, I. Stawowska, G. Stochel, and L. Fiedor Central metal determines pharmacokinetics of chlorophyll-derived xenobiotics J. Med. Chem. 51 2008 4412 4418
43. M. Niziolek, W. Korytowski, and A.W. Girotti Chain-breaking antioxidant and cytoprotective action of nitric oxide on photodynamically stressed tumor cells Photochem. Photobiol. 78 2003 262 270
44. M. Zareba, M. Niziolek, W. Korytowski, and A.W. Girotti Merocyanine 540-sensitized photokilling of leukemia cells: role of post-irradiation chain peroxidation of plasma membrane lipids as revealed by nitric oxide protection Bichim. Biophys. Acta 1722 2005 51 59 (Pubitemid 40222405)
45. Z. Lu, Y. Tao, Z. Zhou, J. Zhang, C. Li, L. Ou, and B. Zhao Mitochondrial reactive oxygen species and nitric oxide-mediated cancer cell apoptosis in 2-butylamino-2-demethoxyhypocrellin B photodynamic therapy Free Radic. Biol. Med. 41 2006 1590 1605 (Pubitemid 44528256)
46. T. Dalbasti, S. Cagli, E. Kilinc, N. Oktar, and M. Ozsoz Online electrochemical monitoring of nitric oxide during photodynamic therapy Nitric Oxide 7 2002 301 305 (Pubitemid 35365676)
47. B. Halliwell, and J.M.C. Gutteridge Free Radicals in Biology and Medicine 1999 Oxford University Press Oxford
48. L. Fiedor, V. Rosenbach-Belkin, and A. Scherz The stereospecific interaction between chlorophylls and chlorophyllase. Possible implication for chlorophyll biosynthesis and degradation J. Biol. Chem. 267 1992 22043 22047
49. R. Schreck Further quantitative methods for the study of transplantable tumors. The growth of R39 sarcoma and brown-pearce carcinomas Am. J. Cancer 28 1936 345 363
50. J.P. Feldman, R. Goldwasser, S. Mark, J. Schwartz, and I. Orion A mathematical model for tumor volume evaluation using two-dimensions J. Appl. Quant. Methods 4 2009 455 462
51. J. Goła̧b, G. Wilczyński, R. Zagożdżon, T. Stokłosa, A. Da̧browska, J. Rybczyńska, M. Wa̧sik, E. Machaj, T. Ołdak, K. Kozar, R. Kamiński, A. Giermasz, A. Czajka, W. Lasek, W. Feleszko, and M. Jakóbisiak Potentiation of the anti-tumour effects of photofrin-based photodynamic therapy by localized treatment with G-CSF Br. J. Cancer 82 2000 1485 1491 (Pubitemid 30175918)
52. Q. Peng, T. Warloe, J. Moan, A. Godal, F. Apricena, K.-E. Giercksky, and J.M. Nesland Antitumor effect of 5-aminolevulinic acid-mediated photodynamic therapy can be enhanced by the use of a low dose of photofrin in human Cancer Res. 61 2001 5824 5832 (Pubitemid 32769101)
53. R. Hille, J. Olson, and G. Palmer Spectral transitions of nitrosyl hemes during ligand binding to hemoglobin J. Biol. Chem. 254 1979 12110 12120 (Pubitemid 10143683)
54. H. Kon, and N. Kataoka Electron paramagnetic resonance of nitric oxide-protoheme complexes with some nitrogenous base. Model systems of nitric oxide hemoproteins Biochemistry 1969 4757 4762
55. M. Elas, J. Bielanska, K. Pustelny, P.M. Plonka, L. Drelicharz, T. Skorka, U. Tyrankiewicz, M. Wozniak, S. Heinze-Paluchowska, M. Walski, L. Wojnar, D. Fortin, R. Ventura-Clapier, and S. Chlopicki Detection of mitochondrial dysfunction by EPR technique in mouse model of dilated cardiomyopathy Free Radic. Biol. Med. 5 2008 321 328
56. W. Chamulitrat, S. Jordan, R. Mason, A. Litton, J. Wilson, E. Wood, G. Wolberg, and L. Molina y Veida Targets of nitric oxide in a mouse of liver inflammation by Corynebacterium parvum Arch. Biochem. Biophys. 316 1995 30 37
57. M. Ziaja, J. Pyka, B. Boczkus, B.K. Plonka, and P.M. Plonka Changes in the nitric oxide level in the rat liver as a response to brain injury Nitric Oxide 25 2011 423 430
58. A. Janczyk, A. Wolnicka-Glubisz, A. Chmura, M. Elas, Z. Matuszak, G. Stochel, and K. Urbanska NO-dependent phototoxicity of Roussin's black salt against cancer cells Nitric Oxide 10 2004 42 50 (Pubitemid 38410894)
59. A.A. Eroy-Reveles, Y. Leung, C.M. Beavers, M.M. Olmstead, and P.K. Mascharak Near-Infrared activated release of nitric oxide from designed photoactive manganese nitrosyls: strategy, design, and potential as NO donors J. Am. Chem. Soc. 130 2008 4447 4458 (Pubitemid 351466440)
60. V.D. Kovaleva, E.V. Berezhnaya, M.A. Komandirov, M.V. Rudkovskii, and A.B. Uzdensky Involvement of nitric oxide in photodynamic injury of neurons and glial cells Nitric Oxide 29 2013 46 52
61. V. Rapozzi, E.D. Pietra, S. Zorzet, M. Zacchigna, B. Bonavida, and L.E. Xodo Nitric oxide-mediated activity in anti-cancer photodynamic therapy Nitric Oxide 30 2013 26 35
62. P. Plonka, B. Plonka, and S. Lukiewicz Evaluation of implant - recipient interactions by ESR spectroscopy Curr. Top. Biophys. 18 1 1994 46 53
63. R.A. Morgan, M.E. Dudley, J.R. Wunderlich, M.S. Hughes, J.C. Yang, R.M. Sherry, R.E. Royal, S.L. Topalian, U.S. Kammula, N.P. Restifo, Z. Zheng, A. Nahvi, C.R. de Vries, L.J. Rogers-Freezer, S.A. Mavroukakis, and S.A. Rosenberg Cancer regression in patients after transfer of genetically engineered lymphocytes Science 314 2006 126 129 (Pubitemid 44547756)
64. L.L. Thomsen, L.M. Ching, W.R. Joseph, B.C. Baguley, and J.B. Gavin Nitric oxide production in endotoxin-resistant C3H/HeJ mice stimulated with flavone-8-acetic acid and xanthenone-4-acetic acid analogues Biochem. Pharmacol. 43 1992 2401 2406
65. B.G. Winsborrow, H. Grondey, H. Savoie, C.A. Fyfe, and D. Dolphin Magnetic resonance imaging evaluation of photodynamic therapy-induced hemorrhagic necrosis in the murine MI tumor model Photochem. Photobiol. 66 1997 847 852 (Pubitemid 127470126)
66. E. Veszelovszky, L.L. Thomsen, L. Zhuang, and B.C. Baguley Flavone acetic acid and 5,6-dimethylxanthenone-4-acetic acid: relationship between plasma nitrate elevation and the induction of tumour necrosis Eur. J. Cancer 29A 1993 404 408 (Pubitemid 23025751)
67. A.K. Wege, W. Ernst, J. Eckl, B. Frankenberg, A. Vollmann-Zwerenz, D.N. Mannel, O. Ortmann, A. Kroemer, and G. Brockhoff Humanized tumor mice-a new model to study and manipulate the immune response in advanced cancer therapy Int. J. Cancer 129 2011 2194 2206