5-ALA mediated photodynamic therapy induces autophagic cell death via AMP-activated protein kinase

Molecular Cancer

Volumn 9, Issue , 2010, Pages

  Ji, Hong Tai ^a   Chien, Li Ting ^a,b   Lin, Yu Hsin ^a   Chien, Hsiung Fei ^b   Chen, Chin Tin ^a,b  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOLEVULINIC ACID; CASPASE 3; CASPASE 9; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE; ADENYLATE KINASE; PHOTOSENSITIZING AGENT;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CANCER CELL; CONTROLLED STUDY; DNA FRAGMENTATION; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OXIDATIVE STRESS; PHOTODYNAMIC THERAPY; SURVIVAL RATE; ANIMAL; DRUG EFFECT; GENETIC TRANSFECTION; IMMUNOBLOTTING; METABOLISM; METHODOLOGY; MITOCHONDRION; PATHOLOGY; PHOTOCHEMOTHERAPY; PHYSIOLOGY; RAT; SIGNAL TRANSDUCTION;

ADENYLATE KINASE; AMINOLEVULINIC ACID; ANIMALS; AUTOPHAGY; DNA FRAGMENTATION; IMMUNOBLOTTING; MAP KINASE SIGNALING SYSTEM; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; OXIDATIVE STRESS; PHOTOCHEMOTHERAPY; PHOTOSENSITIZING AGENTS; RATS; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 77951555123     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-9-91     Document Type: Article

References (43)

1. Dougherty TJ, Gomer CJ, Henderson BW, Jori G, Kessel D, Korbelik M, Moan J, Peng Q. Photodynamic therapy. J Natl Cancer Inst 1998, 90:889-905. 10.1093/jnci/90.12.889, 9637138.
2. Dolmans DE, Fukumura D, Jain RK. Photodynamic therapy for cancer. Nat Rev Cancer 2003, 3:380-387. 10.1038/nrc1071, 12724736.
3. Gomer CJ, Rucker N, Ferrario A, Wong S. Properties and applications of photodynamic therapy. Radiat Res 1989, 120:1-18. 10.2307/3577632, 2678224.
4. Almeida RD, Manadas BJ, Carvalho AP, Duarte CB. Intracellular signaling mechanisms in photodynamic therapy. Biochim Biophys Acta 2004, 1704:59-86.
5. Buytaert E, Dewaele M, Agostinis P. Molecular effectors of multiple cell death pathways initiated by photodynamic therapy. Biochim Biophys Acta 2007, 1776:86-107.
6. Gardner LC, Smith SJ, Cox TM. Biosynthesis of delta-aminolevulinic acid and the regulation of heme formation by immature erythroid cells in man. J Biol Chem 1991, 266:22010-22018.
7. Hardie DG, Carling D. The AMP-activated protein kinase--fuel gauge of the mammalian cell?. Eur J Biochem 1997, 246:259-273. 10.1111/j.1432-1033.1997.00259.x, 9208914.
8. Kemp BE, Mitchelhill KI, Stapleton D, Michell BJ, Chen ZP, Witters LA. Dealing with energy demand: the AMP-activated protein kinase. Trends Biochem Sci 1999, 24:22-25. 10.1016/S0968-0004(98)01340-1, 10087918.
9. Hardie DG, Scott JW, Pan DA, Hudson ER. Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett 2003, 546:113-120. 10.1016/S0014-5793(03)00560-X, 12829246.
10. Ramamurthy S, Ronnett GV. Developing a head for energy sensing: AMP-activated protein kinase as a multifunctional metabolic sensor in the brain. J Physiol 2006, 574:85-93. 10.1113/jphysiol.2006.110122, 1817796, 16690704.
11. Blazquez C, Geelen MJ, Velasco G, Guzman M. The AMP-activated protein kinase prevents ceramide synthesis de novo and apoptosis in astrocytes. FEBS Lett 2001, 489:149-153. 10.1016/S0014-5793(01)02089-0, 11165240.
12. Russell RR, Li J, Coven DL, Pypaert M, Zechner C, Palmeri M, Giordano FJ, Mu J, Birnbaum MJ, Young LH. AMP-activated protein kinase mediates ischemic glucose uptake and prevents postischemic cardiac dysfunction, apoptosis, and injury. J Clin Invest 2004, 114:495-503. 503766, 15314686.
13. Stefanelli C, Stanic I, Bonavita F, Flamigni F, Pignatti C, Guarnieri C, Caldarera CM. Inhibition of glucocorticoid-induced apoptosis with 5-aminoimidazole-4-carboxamide ribonucleoside, a cell-permeable activator of AMP-activated protein kinase. Biochem Biophys Res Commun 1998, 243:821-826. 10.1006/bbrc.1998.8154, 9500985.
14. Dagon Y, Avraham Y, Berry EM. AMPK activation regulates apoptosis, adipogenesis, and lipolysis by eIF2alpha in adipocytes. Biochem Biophys Res Commun 2006, 340:43-47. 10.1016/j.bbrc.2005.11.159, 16377306.
15. Kefas BA, Cai Y, Ling Z, Heimberg H, Hue L, Pipeleers D, Casteele M. AMP-activated protein kinase can induce apoptosis of insulin-producing MIN6 cells through stimulation of c-Jun-N-terminal kinase. J Mol Endocrinol 2003, 30:151-161. 10.1677/jme.0.0300151, 12683939.
16. Meisse D, Casteele M, Beauloye C, Hainault I, Kefas BA, Rider MH, Foufelle F, Hue L. Sustained activation of AMP-activated protein kinase induces c-Jun N-terminal kinase activation and apoptosis in liver cells. FEBS Lett 2002, 526:38-42. 10.1016/S0014-5793(02)03110-1, 12208500.
17. Liang J, Shao SH, Xu ZX, Hennessy B, Ding Z, Larrea M, Kondo S, Dumont DJ, Gutterman JU, Walker CL, et al. The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis. Nat Cell Biol 2007, 9:218-224. 10.1038/ncb1537, 17237771.
18. Meley D, Bauvy C, Houben-Weerts JH, Dubbelhuis PF, Helmond MT, Codogno P, Meijer AJ. AMP-activated protein kinase and the regulation of autophagic proteolysis. J Biol Chem 2006, 281:34870-34879. 10.1074/jbc.M605488200, 16990266.
19. Papandreou I, Lim AL, Laderoute K, Denko NC. Hypoxia signals autophagy in tumor cells via AMPK activity, independent of HIF-1, BNIP3, and BNIP3L. Cell Death Differ 2008, 15:1572-1581. 10.1038/cdd.2008.84, 18551130.
20. Levine B, Yuan J. Autophagy in cell death: an innocent convict?. J Clin Invest 2005, 115:2679-2688. 10.1172/JCI26390, 1236698, 16200202.
21. Onodera J, Ohsumi Y. Autophagy is required for maintenance of amino acid levels and protein synthesis under nitrogen starvation. J Biol Chem 2005, 280:31582-31586. 10.1074/jbc.M506736200, 16027116.
22. Baehrecke EH. Autophagy: dual roles in life and death?. Nat Rev Mol Cell Biol 2005, 6:505-510. 10.1038/nrm1666, 15928714.
23. Oleinick NL, Morris RL, Belichenko I. The role of apoptosis in response to photodynamic therapy: what, where, why, and how. Photochem Photobiol Sci 2002, 1:1-21. 10.1039/b108586g, 12659143.
24. Kessel D, Vicente MG, Reiners JJ. Initiation of apoptosis and autophagy by photodynamic therapy. Lasers Surg Med 2006, 38:482-488. 10.1002/lsm.20334, 2749509, 16615135.
25. Tsai JC, Wu CL, Chien HF, Chen CT. Reorganization of cytoskeleton induced by 5-aminolevulinic acid-mediated photodynamic therapy and its correlation with mitochondrial dysfunction. Lasers Surg Med 2005, 36:398-408. 10.1002/lsm.20179, 15856508.
26. Jin S. Autophagy, mitochondrial quality control, and oncogenesis. Autophagy 2006, 2:80-84.
27. Greene LA, Tischler AS. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci USA 1976, 73:2424-2428. 10.1073/pnas.73.7.2424, 430592, 1065897.
28. Yang PC, Luh KT, Wu R, Wu CW. Characterization of the mucin differentiation in human lung adenocarcinoma cell lines. Am J Respir Cell Mol Biol 1992, 7:161-171.
29. Ji Z, Yang G, Vasovic V, Cunderlikova B, Suo Z, Nesland JM, Peng Q. Subcellular localization pattern of protoporphyrin IX is an important determinant for its photodynamic efficiency of human carcinoma and normal cell lines. J Photochem Photobiol B 2006, 84:213-220. 10.1016/j.jphotobiol.2006.03.006, 16709459.
30. Tsai T, Hong RL, Tsai JC, Lou PJ, Ling IF, Chen CT. Effect of 5-aminolevulinic acid-mediated photodynamic therapy on MCF-7 and MCF-7/ADR cells. Lasers Surg Med 2004, 34:62-72. 10.1002/lsm.10246, 14755426.
31. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J, Wu M, Ventre J, Doebber T, Fujii N, et al. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 2001, 108:1167-1174. 209533, 11602624.
32. Kessel D, Luo Y. Photodynamic therapy: a mitochondrial inducer of apoptosis. Cell Death Differ 1999, 6:28-35. 10.1038/sj.cdd.4400446, 10200545.
33. Biederbick A, Kern HF, Elsasser HP. Monodansylcadaverine (MDC) is a specific in vivo marker for autophagic vacuoles. Eur J Cell Biol 1995, 66:3-14.
34. Mizushima N. Methods for monitoring autophagy. Int J Biochem Cell Biol 2004, 36:2491-2502. 10.1016/j.biocel.2004.02.005, 15325587.
35. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000, 19:5720-5728. 10.1093/emboj/19.21.5720, 305793, 11060023.
36. Klotz LO, Fritsch C, Briviba K, Tsacmacidis N, Schliess F, Sies H. Activation of JNK and p38 but not ERK MAP kinases in human skin cells by 5-aminolevulinate-photodynamic therapy. Cancer Res 1998, 58:4297-4300.
37. Wong TW, Tracy E, Oseroff AR, Baumann H. Photodynamic therapy mediates immediate loss of cellular responsiveness to cytokines and growth factors. Cancer Res 2003, 63:3812-3818.
38. Kessel D, Antolovich M, Smith KM. The role of the peripheral benzodiazepine receptor in the apoptotic response to photodynamic therapy. Photochem Photobiol 2001, 74:346-349. 10.1562/0031-8655(2001)074<0346:TROTPB>2.0.CO;2, 11547575.
39. Furre IE, Shahzidi S, Luksiene Z, Moller MT, Borgen E, Morgan J, Tkacz-Stachowska K, Nesland JM, Peng Q. Targeting PBR by hexaminolevulinate-mediated photodynamic therapy induces apoptosis through translocation of apoptosis-inducing factor in human leukemia cells. Cancer Res 2005, 65:11051-11060. 10.1158/0008-5472.CAN-05-0510, 16322255.
40. Kriska T, Korytowski W, Girotti AW. Hyperresistance to photosensitized lipid peroxidation and apoptotic killing in 5-aminolevulinate-treated tumor cells overexpressing mitochondrial GPX4. Free Radic Biol Med 2002, 33:1389-1402. 10.1016/S0891-5849(02)01078-X, 12419471.
41. Buytaert E, Callewaert G, Hendrickx N, Scorrano L, Hartmann D, Missiaen L, Vandenheede JR, Heirman I, Grooten J, Agostinis P. Role of endoplasmic reticulum depletion and multidomain proapoptotic BAX and BAK proteins in shaping cell death after hypericin-mediated photodynamic therapy. FASEB J 2006, 20:756-758.
42. van Loo G, Saelens X, van Gurp M, MacFarlane M, Martin SJ, Vandenabeele P. The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet. Cell Death Differ 2002, 9:1031-1042. 10.1038/sj.cdd.4401088, 12232790.
43. Corcelle E, Nebout M, Bekri S, Gauthier N, Hofman P, Poujeol P, Fenichel P, Mograbi B. Disruption of autophagy at the maturation step by the carcinogen lindane is associated with the sustained mitogen-activated protein kinase/extracellular signal-regulated kinase activity. Cancer Res 2006, 66:6861-6870. 10.1158/0008-5472.CAN-05-3557, 16818664.