Signaling events in apoptotic photokilling of 5-aminolevulinic acid-treated tumor cells: Inhibitory effects of nitric oxide

Free Radical Biology and Medicine

Volumn 47, Issue 6, 2009, Pages 731-740

  Bhowmick, Reshma ^a   Girotti, Albert W ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

5 Aminolevulinic acid; Apoptosis; Mitogen activated protein kinase (MAPK); Nitric oxide; Photodynamic therapy; Redox signaling; Tumor cells

Indexed keywords

AMINOLEVULINIC ACID; HEME OXYGENASE 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE; PROTEIN BAX; PROTEIN BCL XL; PROTEIN BID; PROTOPORPHYRIN; STRESS ACTIVATED PROTEIN KINASE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER RESISTANCE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INACTIVATION; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; PHOTODYNAMIC THERAPY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION;

AMINOLEVULINIC ACID; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE, TUMOR; CYTOPROTECTION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEME OXYGENASE-1; HUMANS; MAP KINASE KINASE 4; MAP KINASE SIGNALING SYSTEM; NITRIC OXIDE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOTOCHEMOTHERAPY; PHOTOSENSITIZING AGENTS; PROTOPORPHYRINS;

EID: 68349133592     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.06.009     Document Type: Article

References (63)

1. Henderson B.W., and Dougherty T.J. How does photodynamic therapy work?. Photochem. Photobiol. 55 (1992) 145-157
2. Dougherty T.J., Gomer C.J., Henderson B.W., Jori G., Kessel D., Korbelik M., Moan J., and Peng Q. Photodynamic therapy. J. Natl. Cancer Inst. 90 (1998) 889-895
3. Foote C.S. Mechanisms of photosensitized oxidation. Science 162 (1968) 963-970
4. Oleinick N.L., Morris R.L., and Belichenko I. The role of apoptosis in response to photodynamic therapy: what, where, why, and how. Photochem. Photobiol. Sci. 1 (2002) 1-21
5. Buytaert E., Dewaele M., and Agostinis P. Molecular effectors of multiple cell death pathways initiated by photodynamic therapy. Biochim. Biophys. Acta 1776 (2007) 86-107
6. Kessel D., Vicente M.G., and Reiners J.J. Initiation of apoptosis and autophagy by photodynamic therapy. Lasers Surg. Med. 38 (2006) 482-488
7. Ryter S.W., Kim H.P., Hoetzel A., Park J.W., Nakahira K., Wang X., and Choi A.M. Mechanism of cell death in oxidative stress. Antioxid. Redox Signal. 9 (2007) 49-89
8. Kriska T., Korytowski W., and Girotti A.W. Hyperresistance to photosensitized lipid peroxidation and apoptotic killing in 5-aminolevulinate-treated tumor cells overexpressing mitochondrial GPx4. Free Radic. Biol. Med. 33 (2002) 1389-1402
9. Kriska T., Korytowski W., and Girotti A.W. Role of mitochondrial cardiolipin peroxidation in apoptotic photokilling of 5-aminolevulinate-treated tumor cells. Arch. Biochem. Biophys. 433 (2005) 435-446
10. Moncada S.R., Palmer R.M.J., and Higgs E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43 (1991) 109-143
11. Wink D.A., and Mitchell J.B. Chemical biology of nitric oxide: insights into the regulatory, cytotoxic and cytoprotective mechanisms of nitric oxide. Free Radic. Biol. Med. 25 (1998) 434-456
12. Kim Y.M., Talanian R.V., and Billiar T.R. Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J. Biol. Chem. 272 (1997) 31138-31148
13. DeMeester S.L., Qiu Y., Buchman T.G., Hotchkiss R.S., Dunnigan K., Karl I.E., and Cobb J.P. Nitric oxide inhibits stress-induced endoghelial cell apoptosis. Crit. Care Med. 26 (1998) 1500-1509
14. Kim Y.M., Chung H.T., Kim S.S., Han J.A., Yoo Y.M., Kim K.M., Lee G.H., Yun H.Y., Green A., Li J., Simmons R.L., and Billiar T.R. Nitric oxide protects PC12 cells from serum deprivation-induced apoptosis by cGMP-dependent inhibition of caspase signaling. J. Neurosci. 19 (1999) 6740-6747
15. Kim J.E., and Tannenbaum S.R. S-Nitrosation regulates the activation of endogenous procaspase-9 in HT29 colon carcinoma cells. J. Biol. Chem. 279 (2004) 9757-9764
16. Rubbo H., Radi R., Trujillo M., Kalyanaraman B., Barnes S., and Freeman B.A. Nitric oxide regulation of superoxide- and peroxynitrite-dependent lipid peroxidation. J. Biol. Chem. 269 (1994) 26066-26075
17. Stoyanovsky D.A., Vlasova I.I., Belikova N.A., Kapralov A., Tyurin V., and Kagan V.E. Activation of NO donors in mitochondria: peroxidase metabolism of (2-hydroxyamino-vinyl)-triphenyl-phosphonium by cytochrome c releases NO and protects cells against apoptosis. FEBS Lett. 582 (2008) 725-728
18. Chung H.-T., Pae H.-O., Choi B.-M., Billiar T.R., and Kim Y.-M. Nitric oxide as a bioregulator of apoptosis. Biochem. Biophys. Res. Commun. 282 (2001) 1075-1079
19. Kwak H.-J., Park K.-M., Lee S., Lim H.-J., Go S.-H., Eom S.-M., and Park H.-Y. Preconditioning with low concentration NO attenuates subsequent NO-induced apoptosis in vascular smooth muscle cells via HO-1-dependent mitochondrial death pathway. Toxicol. Appl. Pharmacol. 217 (2006) 176-184
20. Niziolek M., Korytowski W., and Girotti A.W. Chair-breaking antioxidant and cytoprotective action of nitric oxide on photodynamically stressed tumor cells. Photochem. Photobiol. 78 (2003) 262-270
21. Niziolek M., Korytowski W., and Girotti A.W. Nitric oxide-induced resistance to lethal photooxidative damage in a breast tumor cell line. Free Radic. Biol. Med. 40 (2006) 1323-1331
22. Keefer L.K., Nims R.W., Davies K.M., and Wink D.A. "NONOates" (1-substituted diazen-1-ium-1,2-diolates) as nitric oxide donors: convenient nitric oxide dosage forms. Methods Enzymol. 268 (1996) 281-293
23. Esworthy R.S., Baker M.A., and Chu F.-F. Expression of selenium-dependent glutathione peroxidase in human breast tumor cell lines. Cancer Res. 55 (1995) 957-962
24. Spector D.L., Goldman R.D., and Leinwald L.A. Cells: a laboratory manual 1 (1997), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 15
25. Vantieghem A., Xu Y., Assefa Z., Piette J., Merlevede W.V., de Witte P.A.M., and Agostinis P. Phosphorylation of Bcl-2 in G2/M phase-arrested cells following photodynamic therapy with hypericin involves a CDK1-mediated signal and delays the onset of apoptosis. J. Biol.Chem. 277 (2002) 37718-37731
26. Aslanukov A., Bhowmick R., Guruju M., Oswald J., Raz D., Bush R.A., Sieving P.A., Lu X., Bock C.B., and Ferreira P.A. P. RanBP2 modulates Cox11 and hexokinase I activities and haploinsufficiency of RanBP2 causes deficits in glucose metabolism. PLoS. Genet. 2 (2006) 1653-1665
27. Bauer J., and Fornnarino J. High-performance liquid chromatographic analysis of "available" hemin in hematin solution. J. Chromatogr. 283 (1984) 378-382
28. Klotz L.-O., Fritsch C., Briviba K., Tsacmacidis N., Schliess F., and Sies H. Activation of JNK and p38 but not ERK MAP kinases in human skin cells by 5-aminolevulinate-photodynamic therapy. Cancer Res. 58 (1998) 4297-4300
29. Kyriakis J.M., and Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81 (2001) 807-869
30. Wada T., and Penninger J.M. Mitogen-activated protein kinases in apoptosis regulatin. Oncogene 23 (2004) 2838-2849
31. Porras A., Zuluaga S., Black E., Valladares A., Alvarez A., Ambrosino C., Benito M., and Nebreda A.R. p38α Mitogen-activated protein kinase sensitizes cells to apoptosis induced by different stimuli. Mol. Biol. Cell 15 (2004) 922-933
32. Silva G., Cunha A., Gregoire I.P., Seldon M.P., and Soares M.P. The antiapoptotic effect of heme oxygenase-1 in endothelial cells involves the degradation of p38α isoform. J. Immunol. 177 (2006) 1894-1903
33. Davies S.P., Reddy H., Caivano M., and Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351 (2000) 95-105
34. Bennett B.L., Sasaki D.T., Murray B.W., O'Leary E.C., Sakata S.T., Xu W., Leisten J.C., Motiwala A., Pierce S., Satoh Y., Bhagwat S.S., Manning A.M., and Anderson D.W. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. USA 98 (2001) 13681-13686
35. Yee E.L., Pitt B.P., Billiar T.R., and Kim Y.M. Effect of nitric oxide on heme metabolism in pulmonary artery endothelial cells. Am. J. Physiol. 271 (1996) L512-L518
36. Maines M.D. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J. 2 (1988) 2557-2568
37. Nowis D., Legat M., Grzela T., Niderla J., Wilczek E., Wilczynski G.M., Glodkowska E., Mrowka P., Issat T., Dulak J., Jozkowicz A., Was H., Adamek M., Wrzosek A., Nazarewski S., Makowski M., Stoklosa T., Jakobisiak M., and Golab J. Heme oxygenase-1 protects tumor cells against photodynamic therapy-mediated cytotoxicity. Oncogene 25 (2006) 3365-3374
38. Li H., Zhu H., Xu C.J., and Yuan J. Cleavage of Bid by Caspase 8 mediates mitochondrial damage in the Fas pathway of apoptosis. Cell 94 (1998) 491-501
39. Kralova J., Dvorak M., Koc M., and Dral V. p38 MAPK plays an essential role in apoptosis induced by photoactivation of a novel ethylene glycol porphyrin derivative. Oncogene 27 (2007) 3010-3020
40. Kocanova S., Buytaert E., Matroule J.Y., Piette J., Golab J., DeWitte P., and Agostinis P. Induction of heme-oxygenase 1 requires the p38MAPK and PI3K pathways and suppresses apoptotic cell death following hypericin-mediated photodynamic therapy. Apoptosis 12 (2007) 731-741
41. Weyergang A., Kaalhus O., and Berg K. Photodynamic therapy with an endocytically located photosensitizer cause a rapid activation of the mitogen-activated protein kinases extracellular signal-regulated kinase, p38, and c-Jun NH2 terminal kinase with opposing effects on cell survival. Mol. Cancer Ther. 7 (2008) 1740-1750
42. Peng Q., Berg K., Moan J., Kongshaug M., and Nesland J.M. 5-Aminolevulinic acid-based photodynamic therapy: principles and experimental research. Photochem. Photobiol. 65 (1997) 235-251
43. Grebenova D., Kuzelova K., Smetana K., Pluskalova M., Cajthamlova H., Marinov I., Fuchs O., Soucek J., Jarolim P., and Hrkal Z. Mitochondrial and endoplasmic reticulum stress-induced apoptotic pathways are activated by 5-aminolevulinic acid-based photodynamic therapy in HL60 leukemia cells. J. Photochem. Photobiol. B 69 (2003) 71-85
44. Krishna M., and Narang H. The complexity of mitogen-activated protein kinases (MAPKs) made simple. Cell. Mol. Life Sci. 65 (2008) 3525-3544
45. Zhuang S., Demirs J.T., and Kochevar I.E. p38 Mitogen-activated protein kinase mediates Bid cleavage, mitochondrial dysfunction, and caspase-3 activation during apoptosis induced by singlet oxygen, but not by hydrogen peroxide. J. Biol. Chem. 275 (2000) 25939-25948
46. Matsuzawa A., and Ichijo H. Redox control of cell fate by MAP kinases: physiological roles of the ASK1-MAP kinase pathway in stress signaling. Biochim. Biophys. Acta 1780 (2008) 1325-1336
47. Girotti A.W. Lipid hydroperoxide generation, turnover, and effector action in biological systems. J. Lipid Res. 39 (1998) 1529-1542
48. Girotti A.W., and Kriska T. Role of lipid hydroperoxides in photo-oxidative stress signaling. Antiox. Redox Signal. 6 (2004) 301-310
49. Moan J., and Berg K. The photodegradation of porphyrins in cells can be used to estimate the lifetime of singlet oxygen. Photochem. Photobiol. 53 (1991) 549-553
50. 2. J. Biol. Chem. 277 (2002) 46566-46575
51. Van Laetham A., Nys K., Van Kelst S., Claerhout S., Ichiro H., Vanderheede J.R., Garmyn M., and Agostinis P. Apoptosis signal regulating kinase-1 connects reactive oxygen species to p38 MAPK-induced mitochondrial apoptosis in UVB-irradiated human keratinocytes. Free Radic. Biol. Med. 41 (2006) 1361-1371
52. Zhang R., Al-Lamki R., Bai L., Streb J.W., Miano J.M., Bradley J., and Min W. Thioredoxin-2 inhibits mitochondria-located ASK1-mediated apoptosis in a JNK-independent manner. Circ. Res. 94 (2004) 1483-1491
53. Girotti A.W. Translocation as a means of disseminating lipid hydroperoxide-induced oxidative damage and effector action. Free Radic. Biol. Med. 44 (2008) 956-968
54. Bradham C., and McClay D.R. p38 MAPK in development and cancer. Cell Cycle 5 (2006) 824-828
55. Kim B.J., Ryu S.W., and Song B.J. JNK- and p38 kinase-mediated phosphorylation of Bax leads to its activation and mitochondrial translocation and to apoptosis of human hepatoma HepG2 cells. J. Biol. Chem. 281 (2006) 21256-21265
56. Tsuruta F., Sunayama J., Mori Y., Hattori S., Shimizu S., Tsujimoto Y., Yoshioka K., Masuyama N., and Gotoh Y. JNK promotes Bax translocation to mitochondria through phosphorylation of 14-3-3 proteins. EMBO J. 23 (2004) 1889-1899
57. Liu J., and Lin A. Role of JNK activation in apoptosis: a double-edged sword. Cell Res. 15 (2005) 36-42
58. Weston C.R., and Davis R.J. The JNK signal transduction pathway. Curr. Opin. Cell Biol. 19 (2007) 142-149
59. Miersch S., and Mutus B. Protein S-nitrosation: biochemistry and characterization of protein thiol-NO interactions as cellular signals. Clin. Biochem. 38 (2005) 777-791
60. Park H.S., Yu J.-W., Cho J.-H., Kim M.-S., Huh S.-H., Ryoo K., and Choi E.-J. Inhibition of apoptosis signal-regulating kinase 1 by nitric oxide through a thiol redox mechanism. J. Biol. Chem. 279 (2004) 7584-7590
61. Park H.S., Huh S.H., Kim M.S., Lee S.H., and Choi E.J. Nitric oxide negatively regulates c-Jun N-terminal kinase/stress-activated protein kinase by means of S-nitrosylation. Proc. Natl. Acad. Sci. USA 97 (2000) 14382-14387
62. Azad N., Vallyathan V., Wang L., Tantishaiyakul V., Stehlik C., Leonard S.S., and Rojanasakul Y. S-Nitrosylation of Bcl-2 inhibits its ubiquitin-proteasomal degradation. A novel antiapoptotic mechanism that suppresses apoptosis. J. Biol. Chem. 281 (2006) 34124-34134
63. Gao J., Kashfi K., Liu X., and Rigas B. NO-donating aspirin induces phase II enzymes in vitro and in vivo. Carcinogenesis 27 (2006) 803-810