Butyrate alters expression of cytochrome P450 1A1 and
metabolism of benzo[a] pyrene via its histone deacetylase
activity in colon epithelial cell models

J 2017

Butyrate alters expression of cytochrome P450 1A1 and metabolism of benzo[a] pyrene via its histone deacetylase activity in colon epithelial cell models

ZAPLETAL, Ondřej, Zuzana TYLICHOVÁ, Jiří NEČA, Jiří KOHOUTEK, Miroslav MACHALA et. al.

Basic information

Original name

Butyrate alters expression of cytochrome P450 1A1 and metabolism of benzo[a] pyrene via its histone deacetylase activity in colon epithelial cell models

Authors

ZAPLETAL, Ondřej (203 Czech Republic, belonging to the institution), Zuzana TYLICHOVÁ (203 Czech Republic, belonging to the institution), Jiří NEČA (203 Czech Republic), Jiří KOHOUTEK (203 Czech Republic), Miroslav MACHALA (203 Czech Republic), A. MILCOVA (203 Czech Republic), Michaela POKORNA (203 Czech Republic), Jan TOPINKA (203 Czech Republic), M.P. MOYER (840 United States of America), Jiřina HOFMANOVÁ (203 Czech Republic), Alois KOZUBÍK (203 Czech Republic) and Jan VONDRÁČEK (203 Czech Republic, guarantor)

Edition

ARCHIVES OF TOXICOLOGY, HEIDELBERG, SPRINGER HEIDELBERG, 2017, 0340-5761

Other information

Language

English

Type of outcome

Článek v odborném periodiku

Field of Study

10601 Cell biology

Country of publisher

United States of America

Confidentiality degree

není předmětem státního či obchodního tajemství

Impact factor

Impact factor: 5.728

RIV identification code

RIV/00216224:14310/17:00097700

Organization unit

Faculty of Science

DOI

http://dx.doi.org/10.1007/s00204-016-1887-4

UT WoS

000399875300008

Keywords in English

CYP1A1; Butyrate; Polycyclic aromatic hydrocarbons; DNA adducts; Histone deacetylases; Colon epithelial cells

Abstract

V originále

Butyrate, a short-chain fatty acid produced by fermentation of dietary fiber, is an important regulator of colonic epithelium homeostasis. In this study, we investigated the impact of this histone deacetylase (HDAC) inhibitor on expression/activity of cytochrome P450 family 1 (CYP1) and on metabolism of carcinogenic polycyclic aromatic hydrocarbon, benzo[a] pyrene (BaP), in colon epithelial cells. Sodium butyrate (NaBt) strongly potentiated the BaP-induced expression of CYP1A1 in human colon carcinoma HCT116 cells. It also co-stimulated the 7-ethoxyresorufin-O-deethylase (EROD) activity induced by the 2,3,7,8-tetrachlorodibenzo-p-dioxin, a prototypical ligand of the aryl hydrocarbon receptor. Up-regulation of CYP1A1 expression/activity corresponded with an enhanced metabolism of BaP and formation of covalent DNA adducts. NaBt significantly potentiated CYP1A1 induction and/or metabolic activation of BaP also in other human colon cell models, colon adenoma AA/C1 cells, colon carcinoma HT-29 cells, or in NCM460D cell line derived from normal colon mucosa. Our results suggest that the effects of NaBt were due to its impact on histone acetylation, because additional HDAC inhibitors (trichostatin A and suberanilohydroxamic acid) likewise increased both the induction of EROD activity and formation of covalent DNA adducts. NaBt-induced acetylation of histone II3 (at Lys14) and histone II4 (at Lys16), two histone modifications modulated during activation of CYP1A1 transcription, and it reduced binding of HDAC1 to the enhancer region of CYP1A1 gene. This in vitro study suggests that butyrate, through modulation of histone acetylation, may potentiate induction of CYP1A1 expression, which might in turn alter the metabolism of BaP within colon epithelial cells.

Citovat

ZAPLETAL, Ondřej, Zuzana TYLICHOVÁ, Jiří NEČA, Jiří KOHOUTEK, Miroslav MACHALA, A. MILCOVA, Michaela POKORNA, Jan TOPINKA, M.P. MOYER, Jiřina HOFMANOVÁ, Alois KOZUBÍK and Jan VONDRÁČEK. Butyrate alters expression of cytochrome P450 1A1 and metabolism of benzo[a] pyrene via its histone deacetylase activity in colon epithelial cell models. ARCHIVES OF TOXICOLOGY. HEIDELBERG: SPRINGER HEIDELBERG, 2017, vol. 91, No 5, p. 2135-2150. ISSN 0340-5761. Available from: https://dx.doi.org/10.1007/s00204-016-1887-4.

@article{1390856,
   author = {Zapletal, Ondřej and Tylichová, Zuzana and Neča, Jiří and Kohoutek, Jiří and Machala, Miroslav and Milcova, A. and Pokorna, Michaela and Topinka, Jan and Moyer, M.P. and Hofmanová, Jiřina and Kozubík, Alois and Vondráček, Jan},
   article_location = {HEIDELBERG},
   article_number = {5},
   doi = {http://dx.doi.org/10.1007/s00204-016-1887-4},
   keywords = {CYP1A1; Butyrate; Polycyclic aromatic hydrocarbons; DNA adducts; Histone deacetylases; Colon epithelial cells},
   language = {eng},
   issn = {0340-5761},
   journal = {ARCHIVES OF TOXICOLOGY},
   title = {Butyrate alters expression of cytochrome P450 1A1 and metabolism of benzo[a] pyrene via its histone deacetylase activity in colon epithelial cell models},
   volume = {91},
   year = {2017}
}

TY  - JOUR
ID  - 1390856
AU  - Zapletal, Ondřej - Tylichová, Zuzana - Neča, Jiří - Kohoutek, Jiří - Machala, Miroslav - Milcova, A. - Pokorna, Michaela - Topinka, Jan - Moyer, M.P. - Hofmanová, Jiřina - Kozubík, Alois - Vondráček, Jan
PY  - 2017
TI  - Butyrate alters expression of cytochrome P450 1A1 and metabolism of benzo[a] pyrene via its histone deacetylase activity in colon epithelial cell models
JF  - ARCHIVES OF TOXICOLOGY
VL  - 91
IS  - 5
SP  - 2135-2150
EP  - 2135-2150
PB  - SPRINGER HEIDELBERG
SN  - 03405761
KW  - CYP1A1
KW  - Butyrate
KW  - Polycyclic aromatic hydrocarbons
KW  - DNA adducts
KW  - Histone deacetylases
KW  - Colon epithelial cells
N2  - Butyrate, a short-chain fatty acid produced by fermentation of dietary fiber, is an important regulator of colonic epithelium homeostasis. In this study, we investigated the impact of this histone deacetylase (HDAC) inhibitor on expression/activity of cytochrome P450 family 1 (CYP1) and on metabolism of carcinogenic polycyclic aromatic hydrocarbon, benzo[a] pyrene (BaP), in colon epithelial cells. Sodium butyrate (NaBt) strongly potentiated the BaP-induced expression of CYP1A1 in human colon carcinoma HCT116 cells. It also co-stimulated the 7-ethoxyresorufin-O-deethylase (EROD) activity induced by the 2,3,7,8-tetrachlorodibenzo-p-dioxin, a prototypical ligand of the aryl hydrocarbon receptor. Up-regulation of CYP1A1 expression/activity corresponded with an enhanced metabolism of BaP and formation of covalent DNA adducts. NaBt significantly potentiated CYP1A1 induction and/or metabolic activation of BaP also in other human colon cell models, colon adenoma AA/C1 cells, colon carcinoma HT-29 cells, or in NCM460D cell line derived from normal colon mucosa. Our results suggest that the effects of NaBt were due to its impact on histone acetylation, because additional HDAC inhibitors (trichostatin A and suberanilohydroxamic acid) likewise increased both the induction of EROD activity and formation of covalent DNA adducts. NaBt-induced acetylation of histone II3 (at Lys14) and histone II4 (at Lys16), two histone modifications modulated during activation of CYP1A1 transcription, and it reduced binding of HDAC1 to the enhancer region of CYP1A1 gene. This in vitro study suggests that butyrate, through modulation of histone acetylation, may potentiate induction of CYP1A1 expression, which might in turn alter the metabolism of BaP within colon epithelial cells.
ER  -

ZAPLETAL, Ondřej, Zuzana TYLICHOVÁ, Jiří NEČA, Jiří KOHOUTEK, Miroslav MACHALA, A. MILCOVA, Michaela POKORNA, Jan TOPINKA, M.P. MOYER, Jiřina HOFMANOVÁ, Alois KOZUBÍK and Jan VONDRÁČEK. Butyrate alters expression of cytochrome P450 1A1 and metabolism of benzo[a] pyrene via its histone deacetylase activity in colon epithelial cell models. \textit{ARCHIVES OF TOXICOLOGY}. HEIDELBERG: SPRINGER HEIDELBERG, 2017, vol.~91, No~5, p.~2135-2150. ISSN~0340-5761. Available from: https://dx.doi.org/10.1007/s00204-016-1887-4.

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