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Published in: Child's Nervous System 10/2012

01-10-2012 | Original Paper

Sodium butyrate increases the effect of the photodynamic therapy: a mechanism that involves modulation of gene expression and differentiation in astrocytoma cells

Authors: José Bueno-Carrazco, Violeta Castro-Leyva, Fanny García-Gomez, Mario Solís-Paredes, Eva Ramon-Gallegos, Alfredo Cruz-Orea, Pilar Eguía-Aguilar, Francisco Arenas-Huertero

Published in: Child's Nervous System | Issue 10/2012

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Abstract

Objectives

In order to evaluate the improvement of the photodynamic therapy (PDT) due to sodium butyrate (NaBu), its effectiveness in U373-MG and D54-MG astrocytoma cell lines was evaluated.

Methods

Cells were exposed to delta-aminolevulinic acid (δ-ALA) as a precursor to endogenous photosensitizer protoporphyrin IX (PpIX). In both astrocytoma cells, an important increase by ALA was observed in uroporphyrinogen synthetase gene expression: 1.8- and 52-fold for D54-MG and U373-MG cells, respectively. After irradiation, they showed 16.67 and 28.9 % of mortality in U373-MG and D54-MG, respectively. These mortalities increased to 70.62 and 96.7 % when U373-MG and D54-MG cells, respectively, were exposed 24 h to 8 mM NaBu, before to PpIX induction. NaBu induced expression of caspase-3, caspase-9, and Bcl-2 and increased Bax in U373-MG cells. ALA-induced morphological changes are compatible to differentiation.

Conclusions

Genes and differentiation induced mainly by NaBu improve cell death performed by PDT in astrocytoma cells. These facts prove the synergistic effect of NaBu on cytotoxic damage induced by PDT.
Literature
1.
go back to reference Chico-Ponce de León F, Castro-Sierra E, Pérezpeña-Diazconti M, Gordillo-Domínguez LF, Santana-Montero BL, Rocha-Rivero LE, Vaca-Ruíz MA, Ríos-Alanís M, Sánchez-Herrera F, Valdéz-Orduño R (2006) Tumores intracraneanos del niño. Bol Med Hosp Infant Mex 63:367–381 Chico-Ponce de León F, Castro-Sierra E, Pérezpeña-Diazconti M, Gordillo-Domínguez LF, Santana-Montero BL, Rocha-Rivero LE, Vaca-Ruíz MA, Ríos-Alanís M, Sánchez-Herrera F, Valdéz-Orduño R (2006) Tumores intracraneanos del niño. Bol Med Hosp Infant Mex 63:367–381
2.
go back to reference Kleihues P, Ohgaki H (1999) Primary and secondary glioblastomas: from concept to clinical diagnosis. Neurooncology 1:44–51 Kleihues P, Ohgaki H (1999) Primary and secondary glioblastomas: from concept to clinical diagnosis. Neurooncology 1:44–51
3.
go back to reference Schmidt-Erfurth U, Diddens H, Birngruber R, Hasan T (1997) Photodynamic targeting of human retinoblastoma cells using covalent low-density lipoprotein conjugates. Br J Cancer 75:54–61PubMedCrossRef Schmidt-Erfurth U, Diddens H, Birngruber R, Hasan T (1997) Photodynamic targeting of human retinoblastoma cells using covalent low-density lipoprotein conjugates. Br J Cancer 75:54–61PubMedCrossRef
4.
go back to reference Kessel D, Woodburn K (1993) Biodistribution of photosensitizing agents. Int J Biochem 25:1377–1383PubMedCrossRef Kessel D, Woodburn K (1993) Biodistribution of photosensitizing agents. Int J Biochem 25:1377–1383PubMedCrossRef
5.
go back to reference Oleinick NL, Morris RL, Belichenko I (2002) The role of apoptosis in response to photodynamic therapy: what, where, why and how. Photochem Photobiol Sci 1:1–21PubMedCrossRef Oleinick NL, Morris RL, Belichenko I (2002) The role of apoptosis in response to photodynamic therapy: what, where, why and how. Photochem Photobiol Sci 1:1–21PubMedCrossRef
6.
go back to reference Wu SM, Ren QG, Zhou MO, Peng Q, Chen JY (2003) Protopporphyrin IX production and its photodynamic effects on glioma cells, neuroblastoma cells and normal cerebellar granule cells in vitro with 5-aminolevulinic acid and its hexylester. Cancer Let 200:123–131CrossRef Wu SM, Ren QG, Zhou MO, Peng Q, Chen JY (2003) Protopporphyrin IX production and its photodynamic effects on glioma cells, neuroblastoma cells and normal cerebellar granule cells in vitro with 5-aminolevulinic acid and its hexylester. Cancer Let 200:123–131CrossRef
7.
go back to reference Ruiz-Galindo E, Arenas-Huertero F, Ramón-Gallegos E (2007) Expression of genes involved in heme biosynthesis in the human retinoblastoma cell lines WERI-Rb-1 and Y79: implications for photodynamic therapy. J Exp Clin Cancer Res 26:195–200PubMed Ruiz-Galindo E, Arenas-Huertero F, Ramón-Gallegos E (2007) Expression of genes involved in heme biosynthesis in the human retinoblastoma cell lines WERI-Rb-1 and Y79: implications for photodynamic therapy. J Exp Clin Cancer Res 26:195–200PubMed
8.
go back to reference Olivo M, Wilson BC (2004) Mapping ALA-induced PPIX fluorescence in normal brain and brain tumour using confocal fluorescence microscopy. Int J Oncol 25:37–45PubMed Olivo M, Wilson BC (2004) Mapping ALA-induced PPIX fluorescence in normal brain and brain tumour using confocal fluorescence microscopy. Int J Oncol 25:37–45PubMed
9.
go back to reference Dailey HA, Smith A (1984) Differential interaction of porphyrins used in photoradiation therapy with ferrochelatase. Biochem J 223:441–445PubMed Dailey HA, Smith A (1984) Differential interaction of porphyrins used in photoradiation therapy with ferrochelatase. Biochem J 223:441–445PubMed
10.
go back to reference Wild PJ, Krieg RC, Seidl J et al (2005) RNA expression profiling of normal and tumor cells following photodynamic therapy with 5-aminolevulinic acid-induced protoporphyrin IX in vitro. Mol Cancer Ther 4:516–528PubMedCrossRef Wild PJ, Krieg RC, Seidl J et al (2005) RNA expression profiling of normal and tumor cells following photodynamic therapy with 5-aminolevulinic acid-induced protoporphyrin IX in vitro. Mol Cancer Ther 4:516–528PubMedCrossRef
11.
go back to reference Urnov FD (2003) Chromatin remodeling as a guide to transcriptional regulatory networks in mammals. J Cell Biochem 88:684–694PubMedCrossRef Urnov FD (2003) Chromatin remodeling as a guide to transcriptional regulatory networks in mammals. J Cell Biochem 88:684–694PubMedCrossRef
12.
go back to reference Gore SD, Carducci MA (2000) Modifying histones to care cancer: clinical development of sodium phenylbutyrate and other histone deacetylase inhibitors. Expert Opin Invest Drugs 9:2923–2934CrossRef Gore SD, Carducci MA (2000) Modifying histones to care cancer: clinical development of sodium phenylbutyrate and other histone deacetylase inhibitors. Expert Opin Invest Drugs 9:2923–2934CrossRef
13.
go back to reference Marks PA, Richon VM, Rifkind RA (2000) Histone deacetylase inhibitors: inducers of differentiation or apoptosis of transformed cells. J Natl Cancer Inst 92:1210–1216PubMedCrossRef Marks PA, Richon VM, Rifkind RA (2000) Histone deacetylase inhibitors: inducers of differentiation or apoptosis of transformed cells. J Natl Cancer Inst 92:1210–1216PubMedCrossRef
14.
go back to reference Widmer J, Fassihi KS, Schlichter SC, Wheeler KS, Crute BE, King N, Nutile-McMenemy N, Noll WW, Daniel S, Ha J, Kim KH, Witters LA (1996) Identification of a second human acetyl-CoA carboxylase gene. Biochem J 316:915–922PubMed Widmer J, Fassihi KS, Schlichter SC, Wheeler KS, Crute BE, King N, Nutile-McMenemy N, Noll WW, Daniel S, Ha J, Kim KH, Witters LA (1996) Identification of a second human acetyl-CoA carboxylase gene. Biochem J 316:915–922PubMed
15.
go back to reference Wang J, Saunthararajah Y, Redner RL, Liu JM (1999) Inhibitors of histone deacetylase relieve ETO-mediated repression and induce differentiation of AML1-ETO leukemia cells. Cancer Res 59:2766–2769PubMed Wang J, Saunthararajah Y, Redner RL, Liu JM (1999) Inhibitors of histone deacetylase relieve ETO-mediated repression and induce differentiation of AML1-ETO leukemia cells. Cancer Res 59:2766–2769PubMed
16.
go back to reference Butler LM, Agus DB, Scher HI, Higgins B, Rose A, Cordon-Cardo C, Thaler HT, Rifkind RA, Marks PA, Richon VM (2000) Suberoylanilide hydroxamic acid, an inhibitor of histone deacetylase, suppresses the growth of prostate cancer cells in vitro and in vivo. Cancer Res 60:5165–5170PubMed Butler LM, Agus DB, Scher HI, Higgins B, Rose A, Cordon-Cardo C, Thaler HT, Rifkind RA, Marks PA, Richon VM (2000) Suberoylanilide hydroxamic acid, an inhibitor of histone deacetylase, suppresses the growth of prostate cancer cells in vitro and in vivo. Cancer Res 60:5165–5170PubMed
17.
go back to reference Piomelli SA (1973) Micromethod for free erythrocyte porphyrins: the FEP test. J Lab Clin Med 81:932–940PubMed Piomelli SA (1973) Micromethod for free erythrocyte porphyrins: the FEP test. J Lab Clin Med 81:932–940PubMed
18.
go back to reference Ramón-Gallegos E, DeLeón-Rodríguez I, Martínez-Guzmán LA, Pérez-Zapata AJ (1999) In vitro study of biosíntesis of protoporphyrin IX induced by δ-aminolevulinic acid in normal and cancerous cells of the human cervix. Arch Med Res 30:163–170CrossRef Ramón-Gallegos E, DeLeón-Rodríguez I, Martínez-Guzmán LA, Pérez-Zapata AJ (1999) In vitro study of biosíntesis of protoporphyrin IX induced by δ-aminolevulinic acid in normal and cancerous cells of the human cervix. Arch Med Res 30:163–170CrossRef
19.
go back to reference Kennedy JC, Pottier RH, Pross DC (1990) Photodynamic therapy with endogenous protoporphyrin IX: basic principles and present clinical experience. J Photochem Photobiol 6:143–148CrossRef Kennedy JC, Pottier RH, Pross DC (1990) Photodynamic therapy with endogenous protoporphyrin IX: basic principles and present clinical experience. J Photochem Photobiol 6:143–148CrossRef
20.
go back to reference Kemmner W, Wan K, Rüttinger S et al (2008) Silencing of human ferrochelatase causes abundant protoporphyrin-IX accumulation in colon cancer. FASEB J 22:500–509PubMedCrossRef Kemmner W, Wan K, Rüttinger S et al (2008) Silencing of human ferrochelatase causes abundant protoporphyrin-IX accumulation in colon cancer. FASEB J 22:500–509PubMedCrossRef
21.
go back to reference Uzdensky A, Juzeniene A, Ma LW, Moan J (2004) Photodynamic inhibition of enzymatic detachment of human cancer cells from a substratum. Biochem Biophys Res Commun 322:452–457PubMedCrossRef Uzdensky A, Juzeniene A, Ma LW, Moan J (2004) Photodynamic inhibition of enzymatic detachment of human cancer cells from a substratum. Biochem Biophys Res Commun 322:452–457PubMedCrossRef
22.
go back to reference Oltvai ZN, Milliman CL, Korsmeyer SJ (1993) Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609–619PubMedCrossRef Oltvai ZN, Milliman CL, Korsmeyer SJ (1993) Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609–619PubMedCrossRef
23.
go back to reference Neise D, Graupner V, Gillissen BF, Daniel PT, Schulze-Osthoff K, Janicke RU, Essmann F (2008) Activation of the mitochondrial death pathway is commonly mediated by a preferential engagement of Bak. Oncogene 27:1387–1396PubMedCrossRef Neise D, Graupner V, Gillissen BF, Daniel PT, Schulze-Osthoff K, Janicke RU, Essmann F (2008) Activation of the mitochondrial death pathway is commonly mediated by a preferential engagement of Bak. Oncogene 27:1387–1396PubMedCrossRef
24.
go back to reference Karmakar S, Banik NL, Patel SJ, Ray SK (2007) 5-Aminolevulinic acid-based photodynamic therapy suppressed survival factors and activated proteases for apoptosis in human glioblastoma U87MG cells. Neurosci Lett 415:242–247PubMedCrossRef Karmakar S, Banik NL, Patel SJ, Ray SK (2007) 5-Aminolevulinic acid-based photodynamic therapy suppressed survival factors and activated proteases for apoptosis in human glioblastoma U87MG cells. Neurosci Lett 415:242–247PubMedCrossRef
25.
go back to reference Ortel B, Chen N, Brissette J, Dotto GP, Maytin E, Hasan T (1998) Differentiation-specific increase in ALA-induced protoporphyrin IX accumulation in primary mouse keratinocytes. Br J Cancer 77:1744–1751PubMedCrossRef Ortel B, Chen N, Brissette J, Dotto GP, Maytin E, Hasan T (1998) Differentiation-specific increase in ALA-induced protoporphyrin IX accumulation in primary mouse keratinocytes. Br J Cancer 77:1744–1751PubMedCrossRef
26.
go back to reference Appelskog IB, Ammerpohl O, Svechnikova IG, Lui WO, Almqvist PM, Ekström TJ (2004) Histone deacetylase inhibitor 4-phenylbutyrate suppresses GAPDH mRNA expression in glioma cells. Int J Oncol 24:1419–1425PubMed Appelskog IB, Ammerpohl O, Svechnikova IG, Lui WO, Almqvist PM, Ekström TJ (2004) Histone deacetylase inhibitor 4-phenylbutyrate suppresses GAPDH mRNA expression in glioma cells. Int J Oncol 24:1419–1425PubMed
27.
go back to reference Flores-Ancona RM, Garcia-Gomez FY, Jimenez-Betanzos AM, Solis-Paredes M, Castro-Leyva V, Cruz-Orea A, Arenas-Huertero F, Ramon-Gallegos E (2009) Effects of sodium butyrate on cell death induced by photodynamic therapy in U373-MG and D54-MG astrocytoma cell lines. Photochem Photobiol 85:1182–1188PubMedCrossRef Flores-Ancona RM, Garcia-Gomez FY, Jimenez-Betanzos AM, Solis-Paredes M, Castro-Leyva V, Cruz-Orea A, Arenas-Huertero F, Ramon-Gallegos E (2009) Effects of sodium butyrate on cell death induced by photodynamic therapy in U373-MG and D54-MG astrocytoma cell lines. Photochem Photobiol 85:1182–1188PubMedCrossRef
28.
go back to reference Li X-N, Shu Q, Su JM-F, Perlaky L, Blaney SM, Lau Ch C (2005) Valproic acid induces growth arrest, apoptosis, and senescence in medulloblastomas by increasing histone hyperacetylation and regulating expression of p21Cip1, CDK4, and CMYC. Mol Cancer Ther 4:1921–1922 Li X-N, Shu Q, Su JM-F, Perlaky L, Blaney SM, Lau Ch C (2005) Valproic acid induces growth arrest, apoptosis, and senescence in medulloblastomas by increasing histone hyperacetylation and regulating expression of p21Cip1, CDK4, and CMYC. Mol Cancer Ther 4:1921–1922
Metadata
Title
Sodium butyrate increases the effect of the photodynamic therapy: a mechanism that involves modulation of gene expression and differentiation in astrocytoma cells
Authors
José Bueno-Carrazco
Violeta Castro-Leyva
Fanny García-Gomez
Mario Solís-Paredes
Eva Ramon-Gallegos
Alfredo Cruz-Orea
Pilar Eguía-Aguilar
Francisco Arenas-Huertero
Publication date
01-10-2012
Publisher
Springer-Verlag
Published in
Child's Nervous System / Issue 10/2012
Print ISSN: 0256-7040
Electronic ISSN: 1433-0350
DOI
https://doi.org/10.1007/s00381-012-1828-3

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