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The response of neurons and glial cells of crayfish to photodynamic treatment: Transcription factors and epigenetic regulation

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Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology Aims and scope

Abstract

Photodynamic therapy (PDT) based on photoproduction of highly toxic singlet oxygen, which causes oxidative stress and death of stained cells, is used for treatment of cancer including that of brain tumors. The study of signaling and epigenetic mechanisms of photodynamic damage of normal neurons and glial cells was carried out on isolated crayfish mechanoreceptors consisting of single sensory neurons enveloped by glial cells. PDT effect caused necrosis of neurons and glial cells and apoptosis of glial cells. Application of specific inhibitors or activators of transcription factors: NF-?B (betulinic acid, parthenolide, CAPE), AP-1 (SR11302), STAT-3 (cucurbitacin, stattic), HIF-1 (KG-548, FM19G11, DMOG), and p53 (RITA, WR1065, nutlin-3, pifithrin-a) or those of epigenetic processes, such as DNA methylation (5-azacytidine, decitabine) or histone deacetylation (sodium valproate, trichostatin A, SBHA) demonstrated that PDTinduced death of neurons and glial cells is regulated by transcription factors and epigenetic regulators. Epigenetic processes did not influence PDT-induced necrosis of neurons. Among the transcription factors studied, only STAT-3 was involved in PDT-induced necrosis of neurons. DNA methylation and histone deacetylation, which suppress transcription, mediated PDT-induced necrosis of glial cells. The transcription factor NF-?B had antinecrotic effects on glia. All transcription factors studied and histone deacetylase were involved in apoptosis of glial cells. Their modulators might serve as potential gliaand neuroprotective agents.

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References

  1. Uzdensky A.B. 2010. Kletochno-molekulyarnye mekhanizmy fotodinamicheskoi terapii (Cellular and molecular mechanisms of photodynamic treatment). St. Petersburg, Nauka.

    Google Scholar 

  2. Eljamel S. 2010. Photodynamic applications in brain tumors: A comprehensive review of the literature. Photodiagn. Photodyn. Ther. 7 (1), 76–85.

    Article  CAS  Google Scholar 

  3. Kostron H. 2010. Photodynamic diagnosis and therapy and the brain. Meth. Mol. Biol. 635, 261–280.

    Article  CAS  Google Scholar 

  4. Uzdensky A.B., Berezhnaya E., Kovaleva V., Neginskaya M., Rudkovskii M., Sharifulina S. 2015. Photodynamic therapy: A review of applications in neurooncology and neuropathology. J. Biomed. Opt. 20 (6), 61108. doi: 10.1117/1.JBO.20.6.061108.

    Article  PubMed  Google Scholar 

  5. Artyukhov V.G., Basharina O.V. 2012. Molekulyarnaya biofizika: Mekhanismy protekaniya i regulyatsii vnutrikletochnykh protsesov (Molecular biophysics: Mechanisms and regulation of intracellular processes). Voronezh, Izd. VGU.

    Google Scholar 

  6. Gomperts B.D., Kramer I.M. Tatham P.E.R. 2009. Signal transduction. Amsterdam, Elsevier.

    Google Scholar 

  7. Almeida R.D., Manadas B., Carvalho A.P., Duarte C.B. 2004. Intracellular signaling mechanisms in photodynamic therapy. Biochim. Biophys. Acta. 1704, 59–86.

    PubMed  CAS  Google Scholar 

  8. Uzdensky A.B. 2008. Signal transduction and photodynamic therapy. Curr. Signal Transd. Ther. 3, 55–74.

    Article  CAS  Google Scholar 

  9. Uzdensky A.B. 2010. Controlled necrosis. Biochemistry (Moscow) Suppl. Ser. A: Membr. Cell Biol. 4 (1), 3–12.

    Article  Google Scholar 

  10. Uzdensky A.B., Rudkovskii M.V., Fedorenko G.M., Berezhnaya E.V., Ischenko I.A., Kovaleva V.D., Komandirov M.A., Neginskaya M.A., Khaitin A.M., Sharifulina S.A. 2013. Responses of crayfish neurons and glial cells to photodynamic impact: Intracellular signaling, ultrastructural changes, and neuroglial interactions. Biochemistry (Moscow) Suppl. Ser. A: Membr. Cell Biol. 30 (5–6), 334–349.

    Google Scholar 

  11. Allis C.D., Caparros M.-L., Jenuwein T., Reinberg D. (Eds.) 2015. Epigenetics, 2nd ed. New York, Cold Spring Harbor Lab Press.

    Google Scholar 

  12. Sultan F.A., Day J.J. 2011. Epigenetic mechanisms in memory and synaptic function. Epigenomics. 3 (2), 157–181. doi: 10.2217/epi.11.6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Mehler M.F. 2008. Epigenetic principles and mechanisms underlying nervous system functions in health and disease. Prog. Neurobiol. 86, 305–341. doi:10.1016/j.pneurobio.2008.10.001.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Gray S.G. 2011. Epigenetic treatment of neurological disease. Epigenomics. 3, 431–450. doi: 10.2217/epi.11.67.

    Article  PubMed  CAS  Google Scholar 

  15. Zawia N.H., Lahiri D.K., Cardozo-Pelaez F. 2009. Epigenetics, oxidative stress, and Alzheimer disease. Free Radic. Biol. Med., 46, 1241–1249. doi:10.1016/ j.freeradbiomed.2009.02.006.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Harrison I.F., Dexter D.T. 2013. Epigenetic targeting of histone deacetylase: therapeutic potential in Parkinson’s disease? Pharmacol. Ther. 140, 34–52. http://dx.doi.org/10.1016/j.pharmthera.2013.05.010

    Article  PubMed  CAS  Google Scholar 

  17. Hwang J.Y., Aromolaran K.A., Zukin, R.S. 2013. Epigenetic mechanisms in stroke and epilepsy. Neuropsychopharmacol. 38, 167–182. doi: 10.1038/npp.2012.134.

    Article  CAS  Google Scholar 

  18. Stankiewicz A.M, Swiergiel A.H., Lisowski P. 2013. Epigenetics of stress adaptations in the brain. Brain Res. Bull. 98, 76–92. doi: 10.1016/j.brainresbull.2013.07.003.

    Article  PubMed  CAS  Google Scholar 

  19. Demyanenko S.V., Uzdensky A.B., Sharifulina S.A., Lapteva T.O., Polyakova L.P. 2014. PDT-induced epigenetic changes in the mouse cerebral cortex: A protein microarray study. Biochim. Biophys. Acta–Gen. Subj. 1840 (1), 262–270.

    Article  CAS  Google Scholar 

  20. Uzdensky A., Kolosov M., Bragin D., Dergacheva O., Vanzha O., Oparina L. 2005. Involvement of adenylate cyclase and tyrosine kinase signaling pathways in response of crayfish stretch receptor neuron and satellite glia cell to photodynamic treatment. Glia. 49, 339–348.

    Article  PubMed  Google Scholar 

  21. Uzdensky A., Lobanov A., Bibov M., Petin Y. 2007. Involvement of Ca2+ and cyclic adenosine monophosphate-mediated signaling pathways in photodynamic injury of isolated crayfish neuron and satellite glial cells. J. Neurosci. Res. 85, 860–870.

    Article  PubMed  CAS  Google Scholar 

  22. Komandirov M.A., Knyazeva E.A., Fedorenko Y.P., Rudkovskii M.V., Stetsurin D.A., Uzdensky A.B. 2011. On the role of phosphatidylinositol 3-kinase, protein kinase B/Akt, and glycogen synthase kinase-3ß in photodynamic injury of crayfish neurons and glial cells. J. Mol. Neurosci. 45, 229–235.

    Article  PubMed  CAS  Google Scholar 

  23. Lobanov A.V., Uzdensky A.B. 2009. Protection of crayfish glial cells but not neurons from photodynamic injury by nerve growth factor. J. Mol. Neurosci. 39, 308–319.

    Article  PubMed  CAS  Google Scholar 

  24. Uzdensky A., Komandirov M., Fedorenko G., Lobanov A. 2013. Protection effect of GDNF and neurturin on photosensitized crayfish neurons and glial cells. J. Mol. Neurosci. 49, 480–490.

    Article  PubMed  CAS  Google Scholar 

  25. Kovaleva V.D., Berezhnaya E.V., Komandirov M.A., Rudkovskii M.V., Uzdensky A.B. 2013. Involvement of nitric oxide in photodynamic injury of neurons and glial cells. Nitric oxide. 29, 46–52.

    Article  PubMed  CAS  Google Scholar 

  26. Morgan M.J., Liu Z.G. 2011. Crosstalk of reactive oxygen species and NF-?B signaling. Cell Res. 21 (1), 103–115.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Siomek A. 2012. NF-?B signaling pathway and free radical impact. Acta. Biochim. Pol. 59 (3), 323–331.

    PubMed  CAS  Google Scholar 

  28. Berezhnaya E.V., Neginskaya M.A., Kovaleva V.D., Komandirov M.A., Rudkovskii M.V., Uzdensky A.B. 2013. The involvement of transcription factors NF-?B and AP-1 in responses of neurons and glial cells to photodynamic treatment. In: Retseptory i vnutrikletochnaya signalizatsiya (Receptors and intracellular signalization). Zinchenko V.P., Berezhnov A.V., Eds. Puschino. Vol. 2, p. 509–512.

    Google Scholar 

  29. Berezhnaya E.V., Neginskaya M.A., Kovaleva V.D., Rudkovskii M.V., Uzdensky A.B. 2014. The involvement of NF-?B in PDT-induced death of crayfish glial and nerve cells. Progr. Biomed. Opt. Imaging.–Proc. SPIE. 9448, 94480N-1.

    Google Scholar 

  30. Listwak S.J., Rathore P., Herkenham M. 2013. Minimal NF-?B activity in neurons. Neuroscience. 250, 282–299.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Aggarwal B.B., Sethi G., Nair A., Ichikawa H. 2006. Nuclear factor-?B: A holy grail in cancer prevention and therapy. Curr. Sign. Transduct. Therapy. 1, 25–52.

    Article  CAS  Google Scholar 

  32. Karmakar S., Banik N.L., Patel S.J., Ray S.K. 2007. 5-Aminolevulinic acid-based photodynamic therapy suppressed survival factors and activated proteases for apoptosis in human glioblastoma U87MG cells. Neurosci. Lett. 415 (3), 242–247.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Shaulian E., Karin M. 2002. AP-1 as a regulator of cell life and death. Nat. Cell Biol. 4 (5), E131–E136.

    Article  PubMed  CAS  Google Scholar 

  34. Vollgraf U., Wegner M., Richter-Landsberg C. 1999. Activation of AP-1 and nuclear factor-?B transcription factors is involved in hydrogen peroxide-induced apoptotic cell death of oligodendrocytes. J. Neurochem. 73 (6), 2501–2509.

    Article  PubMed  CAS  Google Scholar 

  35. Kick G., Messer G., Plewig G., Kind P., Goetz A.E. 1996. Strong and prolonged induction of c-jun and cfos proto-oncogenes by photodynamic therapy. Br. J. Cancer. 74 (1), 30–36.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Rawlings J.S., Rosler K.M., Harrison D.A. 2004. The JAK/STAT signaling pathway. J. Cell Sci. 117, 1281–1283.

    Article  PubMed  CAS  Google Scholar 

  37. Liu W., Oseroff A.R., Baumann H. 2004. Photodynamic therapy causes cross-linking of signal transducer and activator of transcription proteins and attenuation of interleukin-6 cytokine responsiveness in epithelial cells. Cancer Res. 64 (18), 6579–6587.

    Article  PubMed  CAS  Google Scholar 

  38. Koukourakis M.I., Giatromanolaki A., Skarlatos J., Corti L., Blandamura S., Piazza M., et al. 2001. Hypoxia-inducible factor (HIF-1a and HIF-2a) expression in early esophageal cancer and response to photodynamic therapy and radiotherapy. Cancer. 61 (5), 1830–1832.

    CAS  Google Scholar 

  39. Salceda S., Caro J. 1997. Hypoxia-inducible factor 1a (HIF-1a) protein is rapidly degraded by the ubiquitinproteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J. Biol. Chem. 272, 22642–22647.

    PubMed  CAS  Google Scholar 

  40. Mitra S., Cassar S.E., Niles D.J., Puskas J.A., Frelinger J.G., Foster T.H. 2006. Photodynamic therapy mediates the oxygen-independent activation of hypoxia-inducible factor 1a. Mol. Cancer Ther. 5 (12), 3268–3274.

    Article  PubMed  CAS  Google Scholar 

  41. Zheng X., Jiang F., Katakowski M., Zhang X., Jiang H., Zhang Z.G., Chopp M. 2008. Sensitization of cerebral tissue in nude mice with photodynamic therapy induces ADAM17/TACE and promotes glioma cell invasion. Cancer Lett. 265 (2), 177–187.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Berezhnaya E.V., Neginskaya M.A., Uzdensky A.B. 2015. The study of the role of HIF-1 in death of neurons and glial cells induced by photodynamic treatment. In: Retseptory i vnutrikletochnaya signalizatsiya (Receptors and intracellular signalization). Zinchenko V.P., Berezhnov A.V., Eds. Puschino. Vol. 2, pp. 535–539.

    Google Scholar 

  43. Culmsee C., Mattson M.P. 2005. p53 in neuronal apoptosis. Biochem. Biophys. Res. Communs. 2005. 331, 761–777.

    Article  CAS  Google Scholar 

  44. Checler F., Alves da Costa C. 2014. p53 in neurodegenerative diseases and brain cancers. Pharmacol. Ther. 142, 99–113.

    Article  PubMed  CAS  Google Scholar 

  45. Sharifulina S.A., Uzdensky A.B. 2014. Photodynamic injury of isolated crayfish neuron and surrounding glial cells: The role of p53. Progr. Biomed. Opt. Imaging.–Proc. SPIE. 9448, 94480L-1. doi: 10.1117/12.2179569.

    Google Scholar 

  46. Sharifulina S.A., Rudkovskii M.V., Uzdensky A.B. 2015. The involvement of p53 in the death of crayfish mechanoreceptor neuron and glial cells upon axotomy and photodynamic treatment. In: Retseptory i vnutrikletochnaya signalizatsiya (Receptors and intracellular signalization). Zinchenko V.P., Berezhnov A.V., Eds. Puschino. Vol. 2, pp. 575–579.

    Google Scholar 

  47. Fisher A.M., Ferrario A., Rucker N., Zhang S., Gomer C.J. 1999. Photodynamic therapy sensitivity is not altered in human tumor cells after abrogation of p53 function. Cancer Res. 59, 331–335.

    PubMed  CAS  Google Scholar 

  48. Tong Z., Singh G., Rainbow A.J. 2000. The role of the p53 tumor suppressor in the response of human cells to Photofrin-mediated photodynamic therapy. Photochem. Photobiol. 71, 201–210.

    Article  PubMed  CAS  Google Scholar 

  49. Zawacka-Pankau J., Krachulec J., Grulkowski I., Bielawski K.P., Selivanova G. 2008. The p53-mediated cytotoxicity of photodynamic therapy of cancer: recent advances. Toxicol. Appl. Pharmacol. 232, 487–497. doi: 10.1016/j.taap.2008.07.012.

    Article  PubMed  CAS  Google Scholar 

  50. Sharifulina S.A., Uzdensky A.B. 2015. The involvement of epigenetic mechanisms in PDT-induced death of glial cells, but not neurons of crayfish. In: Retseptory i vnutrikletochnaya signalizatsiya (Receptors and intracellular signalization). Zinchenko V.P., Berezhnov A.V., Eds. Puschino. Vol. 2, pp. 579–583.

    Google Scholar 

  51. Baylin S.B. 2005. DNA methylation and gene silencing in cancer. Nat. Clin. Pract. Oncol. 2 (Suppl. 1), 4–11.

    Article  CAS  Google Scholar 

  52. Sharifulina S.A., Komandirov M.A., Uzdensky A.B. 2014. Epigenetic regulation of death of crayfish glial cells but not neurons induced by photodynamic impact. Brain Res. Bull. 102, 15–21. doi: 10.1016/j.brainresbull.2014.01.005.

    Article  PubMed  CAS  Google Scholar 

  53. Haaf T. 1995. The effects of 5-azacytidine and 5azadeoxycytidine on chromosome structure and function: Implications for methylation-associated cellular processes. Pharmacol. Ther. 65, 19–46.

    Article  PubMed  CAS  Google Scholar 

  54. Konsoula Z., Barile F.A. 2012. Epigenetic histone acetylation and deacetylation mechanisms in experimental models of neurodegenerative disorders. J. Pharmacol. Toxicol. Methods 66, 215–220. http://dx.doi.org/ 10.1016/j.vascn.2012.08.001

    Article  PubMed  CAS  Google Scholar 

  55. Kanai H., Sawa A., Chen R.W., Leeds P., Chuang D.M. 2004. Valproic acid inhibits histone deacetylase activity and suppresses excitotoxicity-induced GAPDH nuclear accumulation and apoptotic death in neurons. Pharmacogenomics J. 4, 336–344.

    Article  PubMed  CAS  Google Scholar 

  56. Zhang Z., Qin X., Tong N., Zhao X., Gong Y., Shi Y., Wu X. 2012. Valproic acid-mediated neuroprotection in retinal ischemia injury via histone deacetylase inhibition and transcriptional activation. Exp. Eye Res. 94, 98–108.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to A. B. Uzdensky.

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Original Russian Text © A.B. Uzdensky, E.V. Berezhnaya, V.D. Kovaleva, M.A. Neginskaya, M.V. Rudkovskii, S.A. Sharifulina, 2015, published in Biologicheskie Membrany, 2015, Vol. 32, No. 5–6, pp. 437–445.

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Uzdensky, A.B., Berezhnaya, E.V., Kovaleva, V.D. et al. The response of neurons and glial cells of crayfish to photodynamic treatment: Transcription factors and epigenetic regulation. Biochem. Moscow Suppl. Ser. A 9, 329–336 (2015). https://doi.org/10.1134/S1990747815050190

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  • DOI: https://doi.org/10.1134/S1990747815050190

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