High fluence low-power laser irradiation induces apoptosis via inactivation of Akt/GSK3β signaling pathway

Journal of Cellular Physiology

Volumn 226, Issue 3, 2011, Pages 588-601

  Huang, Lei ^a   Wu, Shengnan ^a   Xing, Da ^a  

^a SOUTH CHINA NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ASCORBIC ACID; GLYCOGEN SYNTHASE KINASE 3BETA; LITHIUM CHLORIDE; PROTEIN BAX; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FLOW CYTOMETRY; FLUORESCENCE; HUMAN; HUMAN CELL; IRRADIATION; LOW LEVEL LASER THERAPY; PRIORITY JOURNAL; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL LINE; CELL NUCLEUS; DOSE-RESPONSE RELATIONSHIP, RADIATION; DOWN-REGULATION; ENZYME ACTIVATION; GLYCOGEN SYNTHASE KINASE 3; HUMANS; LASER THERAPY, LOW-LEVEL; LIGHT; MODELS, BIOLOGICAL; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 78650660969     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22367     Document Type: Article

References (61)

1. Beaulieu JM, Sotnikova TD, Marion S, Lefkowitz RJ, Gainetdinov RR, Caron MG. 2005. An Akt/beta-arrestin 2/PP2A signaling complex mediates dopaminergic neurotransmission and behavior. Cell 122: 261-273.
2. Bezombes C, Plo I, Mansat-De Mas V, Quillet-Mary A, Negre-Salvayre A, Laurent G, Jaffrezou JP. 2001. Oxidative stress-induced activation of Lyn recruits sphingomyelinase and is requisite for its stimulation by Ara-C. FASEB J 15: 1583-1585.
3. Bijur GN, Jope RS. 2001. Proapoptotic stimuli induce nuclear accumulation of glycogen synthase kinase-3 beta. J Biol Chem 276: 37436-37442.
4. Bijur GN, De Sarno P, Jope RS. 2000. Glycogen synthase kinase-3beta facilitates staurosporine- and heat shock-induced apoptosis. Protection by lithium. J Biol Chem 275: 7583-7590.
5. Chalfant CE, Kishikawa K, Mumby MC, Kamibayashi C, Bielawska A, Hannun YA. 1999. Long chain ceramides activate protein phosphatase-1 and protein phosphatase-2A. Activation is stereospecific and regulated by phosphatidic acid. J Biol Chem 274: 20313-20317.
6. Chen Q, Chai YC, Mazumder S, Jiang C, Macklis RM, Chisolm GM, Almasan A. 2003. The late increase in intracellular free radical oxygen species during apoptosis is associated with cytochrome c release, caspase activation, and mitochondrial dysfunction. Cell Death Differ 10: 323-334.
7. Chen L, Xu B, Liu L, Luo Y, Yin J, Zhou H, Chen W, Shen T, Han X, Huang S. 2010. Hydrogen peroxide inhibits mTOR signaling by activation of AMPKalpha leading to apoptosis of neuronal cells. Lab Invest 90: 762-773.
8. Ciani L, Salinas PC. 2005. WNTs in the vertebrate nervous system: From patterning to neuronal connectivity. Nat Rev Neurosci 6: 351-362.
9. Cicchillitti L, Fasanaro P, Biglioli P, Capogrossi MC, Martelli F. 2003. Oxidative stress induces protein phosphatase 2A-dependent dephosphorylation of the pocket proteins pRb, p107, and p130. J Biol Chem 278: 19509-19517.
10. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA. 1995. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378: 785-789.
11. de Groot RP, Auwerx J, Bourouis M, Sassone-Corsi P. 1993. Negative regulation of Jun/AP-1: Conserved function of glycogen synthase kinase 3 and the Drosophila kinase shaggy. Oncogene 8: 841-847.
12. Diehl JA, Cheng M, Roussel MF, Sherr CJ. 1998. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 12: 3499-3511.
13. Ding Q, He X, Hsu JM, Xia W, Chen CT, Li LY, Lee DF, Liu JC, Zhong Q, Wang X, Hung MC. 2007. Degradation of Mcl-1 by beta-TrCP mediates glycogen synthase kinase 3-induced tumor suppression and chemosensitization. Mol Cell Biol 27: 4006-4017.
14. Doble BW, Woodgett JR. 2003. GSK-3: Tricks of the trade for a multi-tasking kinase. J Cell Sci 116: 1175-1186.
15. Dobrowsky RT, Kamibayashi C, Mumby MC, Hannun YA. 1993. Ceramide activates heterotrimeric protein phosphatase 2A. J Biol Chem 268: 15523-15530.
16. Frame S, Cohen P. 2001. GSK3 takes centre stage more than 20 years after its discovery. Biochem J 359: 1-16.
17. Gao T, Furnari F, Newton AC. 2005. PHLPP: A phosphatase that directly dephosphorylates Akt, promotes apoptosis, and suppresses tumor growth. Mol Cell 18: 13-24.
18. Goldbaum O, Richter-Landsberg C. 2002. Activation of PP2A-like phosphatase and modulation of tau phosphorylation accompany stress-induced apoptosis in cultured oligodendrocytes. Glia 40: 271-282.
19. 2 acts on cellular membranes to generate ceramide signaling and initiate apoptosis in tracheobronchial epithelial cells. J Cell Sci 111: 3209-3220.
20. Grimes CA, Jope RS. 2001. The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog Neurobiol 65: 391-426.
21. Gross AJ, Jelkmann W. 1990. Helium-neon laser irradiation inhibits the growth of kidney epithelial cells in culture. Lasers Surg Med 10: 40-44.
22. Hanger DP, Hughes K, Woodgett JR, Brion JP, Anderton BH. 1992. Glycogen synthase kinase-3 induces Alzheimer's disease-like phosphorylation of tau: Generation of paired helical filament epitopes and neuronal localisation of the kinase. Neurosci Lett 147: 58-62.
23. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW. 1998. Identification of c-MYC as a target of the APC pathway. Science 281: 1509-1512.
24. Hetman M, Cavanaugh JE, Kimelman D, Xia Z. 2000. Role of glycogen synthase kinase-3beta in neuronal apoptosis induced by trophic withdrawal. J Neurosci 20: 2567-2574.
25. Hongisto V, Vainio JC, Thompson R, Courtney MJ, Coffey ET. 2008. The Wnt pool of glycogen synthase kinase 3beta is critical for trophic-deprivation-induced neuronal death. Mol Cell Biol 28: 1515-1527.
26. Ivaska J, Nissinen L, Immonen N, Eriksson JE, Kahari VM, Heino J. 2002. Integrin alpha 2 beta 1 promotes activation of protein phosphatase 2A and dephosphorylation of Akt and glycogen synthase kinase 3 beta. Mol Cell Biol 22: 1352-1359.
27. Karu T. 1989. Photobiology of low-power laser effects. Health Phys 56: 691-704.
28. Kim AJ, Shi Y, Austin RC, Werstuck GH. 2005. Valproate protects cells from ER stress-induced lipid accumulation and apoptosis by inhibiting glycogen synthase kinase-3. J Cell Sci 118: 89-99.
29. Li M, Wang X, Meintzer MK, Laessig T, Birnbaum MJ, Heidenreich KA. 2000. Cyclic AMP promotes neuronal survival by phosphorylation of glycogen synthase kinase 3beta. Mol Cell Biol 20: 9356-9363.
30. Li L, Ren CH, Tahir SA, Ren C, Thompson TC. 2003. Caveolin-1 maintains activated Akt in prostate cancer cells through scaffolding domain binding site interactions with and inhibition of serine/threonine protein phosphatases PP1 and PP2A. Mol Cell Biol 23: 9389-9404.
31. Lin CF, Chen CL, Chiang CW, Jan MS, Huang WC, Lin YS. 2007. GSK-3beta acts downstream of PP2A and the PI 3-kinase-Akt pathway, and upstream of caspase-2 in ceramide-induced mitochondrial apoptosis. J Cell Sci 120: 2935-2943.
32. Linseman DA, Butts BD, Precht TA, Phelps RA, Le SS, Laessig TA, Bouchard RJ, Florez-McClure ML, Heidenreich KA. 2004. Glycogen synthase kinase-3beta phosphorylates Bax and promotes its mitochondrial localization during neuronal apoptosis. J Neurosci 24: 9993-10002.
33. 2 induce caspase-3-independent degradation of Akt/protein kinase B. J Biol Chem 277: 42943-42952.
34. Mora A, Sabio G, Risco AM, Cuenda A, Alonso JC, Soler G, Centeno F. 2002. Lithium blocks the PKB and GSK3 dephosphorylation induced by ceramide through protein phosphatase-2A. Cell Signal 14: 557-562.
35. Munoz-Pinedo C, Guio-Carrion A, Goldstein JC, Fitzgerald P, Newmeyer DD, Green DR. 2006. Different mitochondrial intermembrane space proteins are released during apoptosis in a manner that is coordinately initiated but can vary in duration. Proc Natl Acad Sci USA 103: 11573-11578.
36. Nair VD, Olanow CW. 2008. Differential modulation of Akt/glycogen synthase kinase-3beta pathway regulates apoptotic and cytoprotective signaling responses. J Biol Chem 283: 15469-15478.
37. O'Kane S, Shields TD, Gilmore WS, Allen JM. 1994. Low intensity laser irradiation inhibits tritiated thymidine incorporation in the hemopoietic cell lines HL-60 and U937. Lasers Surg Med 14: 34-39.
38. Pap M, Cooper GM. 1998. Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-kinase/Akt cell survival pathway. J Biol Chem 273: 19929-19932.
39. Pap M, Cooper GM. 2002. Role of translation initiation factor 2B in control of cell survival by the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3beta signaling pathway. Mol Cell Biol 22: 578-586.
40. Rao RK, Clayton LW. 2002. Regulation of protein phosphatase 2A by hydrogen peroxide and glutathionylation. Biochem Biophys Res Commun 293: 610-616.
41. Ruvolo PP, Deng X, Ito T, Carr BK, May WS. 1999. Ceramide induces Bcl2 dephosphorylation via a mechanism involving mitochondrial PP2A. J Biol Chem 274: 20296-20300.
42. Sato S, Fujita N, Tsuruo T. 2000. Modulation of Akt kinase activity by binding to Hsp90. Proc Natl Acad Sci USA 97: 10832-10837.
43. Shi CS, Huang NN, Harrison K, Han SB, Kehrl JH. 2006. The mitogen-activated protein kinase kinase kinase kinase GCKR positively regulates canonical and noncanonical Wnt signaling in B lymphocytes. Mol Cell Biol 26: 6511-6521.
44. Shin SY, Kim CG, Jho EH, Rho MS, Kim YS, Kim YH, Lee YH. 2004. Hydrogen peroxide negatively modulates Wnt signaling through downregulation of beta-catenin. Cancer Lett 212: 225-231.
45. Shin SY, Chin BR, Lee YH, Kim JH. 2006. Involvement of glycogen synthase kinase-3beta in hydrogen peroxide-induced suppression of Tcf/Lef-dependent transcriptional activity. Cell Signal 18: 601-607.
46. Simon HU, Haj-Yehia A, Levi-Schaffer F. 2000. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5: 415-418.
47. Stambolic V, Woodgett JR. 1994. Mitogen inactivation of glycogen synthase kinase-3 beta in intact cells via serine 9 phosphorylation. Biochem J 303: 701-704.
48. Tan J, Geng L, Yazlovitskaya EM, Hallahan DE. 2006. Protein kinase B/Akt-dependent phosphorylation of glycogen synthase kinase-3beta in irradiated vascular endothelium. Cancer Res 66: 2320-2327.
49. Tsuruta F, Masuyama N, Gotoh Y. 2002. The phosphatidylinositol 3-kinase (PI3K)-Akt pathway suppresses Bax translocation to mitochondria. J Biol Chem 277: 14040-14047.
50. Ushio-Fukai M, Alexander RW, Akers M, Yin Q, Fujio Y, Walsh K, Griendling KK. 1999. Reactive oxygen species mediate the activation of Akt/protein kinase B by angiotensin II in vascular smooth muscle cells. J Biol Chem 274: 22699-22704.
51. Valentijn AJ, Metcalfe AD, Kott J, Streuli CH, Gilmore AP. 2003. Spatial and temporal changes in Bax subcellular localization during anoikis. J Cell Biol 162: 599-612.
52. Wang Q, Wang X, Hernandez A, Hellmich MR, Gatalica Z, Evers BM. 2002. Regulation of TRAIL expression by the phosphatidylinositol 3-kinase/Akt/GSK-3 pathway in human colon cancer cells. J Biol Chem 277: 36602-36610.
53. Wang F, Chen TS, Xing D, Wang JJ, Wu YX. 2005. Measuring dynamics of caspase-3 activity in living cells using FRET technique during apoptosis induced by high fluence low-power laser irradiation. Lasers Surg Med 36: 2-7.
54. Whisler RL, Goyette MA, Grants IS, Newhouse YG. 1995. Sublethal levels of oxidant stress stimulate multiple serine/threonine kinases and suppress protein phosphatases in Jurkat T cells. Arch Biochem Biophys 319: 23-35.
55. Wu S, Xing D, Wang F, Chen T, Chen WR. 2007. Mechanistic study of apoptosis induced by high-fluence low-power laser irradiation using fluorescence imaging techniques. J Biomed Opt 12: 064015.
56. Wu S, Xing D, Gao X, Chen WR. 2009. High fluence low-power laser irradiation induces mitochondrial permeability transition mediated by reactive oxygen species. J Cell Physiol 218: 603-611.
57. Yamada T, Katagiri H, Asano T, Inukai K, Tsuru M, Kodama T, Kikuchi M, Oka Y. 2001. 3-Phosphoinositide-dependent protein kinase 1, an Akt1 kinase, is involved in dephosphorylation of Thr-308 of Akt1 in Chinese hamster ovary cells. J Biol Chem 276: 5339-5345.
58. Yang L, Sun M, Sun XM, Cheng GZ, Nicosia SV, Cheng JQ. 2007. Akt attenuation of the serine protease activity of HtrA2/Omi through phosphorylation of serine 212. J Biol Chem 282: 10981-10987.
59. Zhang J, Xing D, Gao X. 2008. Low-power laser irradiation activates Src tyrosine kinase through reactive oxygen species-mediated signaling pathway. J Cell Physiol 217: 518-528.
60. Zhang L, Xing D, Gao X, Wu S. 2009. Low-power laser irradiation promotes cell proliferation by activating PI3K/Akt pathway. J Cell Physiol 219: 553-562.
61. Zhang L, Zhang Y, Xing D. 2010. LPLI Inhibits apoptosis upstream of Bax translocation via a GSK-3β-inactivation mechanism. J Cell Physiol 224: 218-228.