SpringerLink
Log in

FOXO1 and LXRα downregulate the apolipoprotein A-I gene expression during hydrogen peroxide-induced oxidative stress in HepG2 cells

  • Original Paper
  • Published:
Cell Stress and Chaperones Aims and scope

Abstract

Reactive oxygen species damage various cell components including DNA, proteins, and lipids, and these impairments could be a reason for severe human diseases including atherosclerosis. Forkhead box O1 (FOXO1), an important metabolic transcription factor, upregulates antioxidant and proapoptotic genes during oxidative stress. Apolipoprotein A-I (ApoA-I) forms high density lipoprotein (HDL) particles that are responsible for cholesterol transfer from peripheral tissues to liver for removal in bile in vertebrates. The main sources for plasma ApoA-I in mammals are liver and jejunum. Hepatic apoA-I transcription depends on a multitude of metabolic transcription factors. We demonstrate that ApoA-I synthesis and secretion are decreased during H2O2-induced oxidative stress in human hepatoma cell line HepG2. Here, we first show that FOXO1 binds to site B of apoA-I hepatic enhancer and downregulates apoA-I gene activity in HepG2 cells. Moreover, FOXO1 and LXRα transcription factors participate in H2O2-triggered downregulation of apoA-I gene together with Src, JNK, p38, and AMPK kinase cascades. Mutations of sites B or C as well as the administration of siRNAs against FOXO1 or LXRα to HepG2 cells abolished the hydrogen peroxide-mediated suppression of apoA-I gene.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aikawa R, Komuro I, Yamazaki T, Zou Y, Kudoh S, Tanaka M, Shiojima I, Hiro Y, Yazaki Y (1997) Oxidative stress activates extracellular signal-regulated kinases through Src and Ras in cultured cardiac myocytes of neonatal rats. J Clin Invest 100:1813–1821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andrews NC, Faller DV (1991) A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res 19:2499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asada S, Daitoku H, Matsuzaki H, Saito T, Sudo T, Mukai H, Iwashita S, Kako K, Kishi T, Kasuya Y, Fukamizu A (2007) Mitogen-activated protein kinases, Erk and p38, phosphorylate and regulate Foxo1. Cell Signal 19:519–527. doi:10.1016/j.cellsig.2006.08.015

    Article  CAS  PubMed  Google Scholar 

  • Assmann G, Schulte H, Schriewer H (1984) The effects of cigarette smoking on serum levels of HDL cholesterol and HDL apolipoprotein A-I. Findings of a prospective epidemiological study on employees of several companies in Westphalia, West Germany. J Clin Chem Clin Biochem 22:397–402

    CAS  PubMed  Google Scholar 

  • Awad H, Nolette N, Hinton M, Dakshinamurti S (2014) AMPK and FoxO1 regulate catalase expression in hypoxic pulmonary arterial smooth muscle. Pediatr Pulmonol 49:885–897. doi:10.1002/ppul.22919

    Article  PubMed  Google Scholar 

  • Bedard K, Krause K-H (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245–313. doi:10.1152/physrev.00044.2005

    Article  CAS  PubMed  Google Scholar 

  • Chan J, Nakabayashi H, Wong NC (1993) HNF-4 increases activity of the rat Apo A1 gene. Nucleic Acids Res 21:1205–1211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng Z, Guo S, Copps K, Dong X, Kollipara R, Rodgers JT, Depinho RA, Puigserver P, White MF (2009) Foxo1 integrates insulin signaling with mitochondrial function in the liver. Nat Med 15:1307–1311. doi:10.1038/nm.2049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi J, Oh S, Lee D, Oh HJ, Park JY, Lee SB, Lim DS (2009) Mst1-FoxO signaling protects naive T lymphocytes from cellular oxidative stress in mice. PLoS One 4:1–10. doi:10.1371/journal.pone.0008011

    Article  Google Scholar 

  • Cuthbert C, Wang Z, Zhang X, Tam SP (1997) Regulation of human apolipoprotein A-I gene expression by gramoxone. J Biol Chem 272:14954–14960. doi:10.1074/jbc.272.23.14954

    Article  CAS  PubMed  Google Scholar 

  • Görlach A, Dimova EY, Petry A, Martínez-Ruiz A, Hernansanz-Agustín P, Rolo AP, Palmeira CM, Kietzmann T (2015) Reactive oxygen species, nutrition, hypoxia and diseases: problems solved? Redox Biol 6:372–385. doi:10.1016/j.redox.2015.08.016

    Article  PubMed  PubMed Central  Google Scholar 

  • Dizhe EB, Ignatovich IA, Burov SV, Pohvoscheva AV, Akifiev BN, Efremov AM, Perevozchikov AP, Orlov SV (2006) Complexes of DNA with cationic peptides: conditions of formation and factors effecting internalization by mammalian cells. Biochem Mosc 71:1350–1356

    Article  CAS  Google Scholar 

  • Donath MY, Shoelson SE (2011) Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 11:98–107. doi:10.1038/nri2925

    Article  CAS  PubMed  Google Scholar 

  • Eggerman TL, Hoeg JM, Meng MS, Tombragel A, Bojanovski D, Brewer JHB (1991) Differential tissue-specific expression of human apoA-l and apoA-II. J Lipid Res 32:821–828

    CAS  PubMed  Google Scholar 

  • Essers MG, Weijzen S, de Vries-Smits AMM, Saarloos I, de Ruiter ND, Bos JL, Burgering BMT (2004) FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. EMBO J 23:4802–4812. doi:10.1038/sj.emboj.7600476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giannoni E, Buricchi F, Raugei G, Ramponi G, Chiarugi P (2005) Intracellular reactive oxygen species activate Src tyrosine kinase during cell adhesion and anchorage-dependent cell growth. Mol Cell Biol 25:6391–6403. doi:10.1128/MCB.25.15.6391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ginsburg GS, Ozer J, Karathanasis SK (1995) Intestinal apolipoprotein AI gene transcription is regulated by multiple distinct DNA elements and is synergistically activated by the orphan nuclear receptor, hepatocyte nuclear factor 4. J Clin Invest 96:528–538. doi:10.1172/JCI118065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haas MJ, Horani M, Mreyoud A, Plummer B, Wong NCW, Mooradian AD (2003) Suppression of apolipoprotein AI gene expression in HepG2 cells by TNFalpha and IL-1beta. Biochim Biophys Acta 1623:120–128. doi:10.1016/j.bbagen.2003.08.004

    Article  CAS  PubMed  Google Scholar 

  • Han Y, Wang Q, Song P, Zhu Y, Zou MH (2010) Redox regulation of the AMP-activated protein kinase. PLoS One 5:e15420. doi:10.1371/journal.pone.0015420

    Article  PubMed  PubMed Central  Google Scholar 

  • Harnish DC, Malik S, Karathanasis SK (1994) Activation of apolipoprotein AI gene transcription by the liver-enriched factor HNF-3. J Biol Chem 269:28220–28226

    CAS  PubMed  Google Scholar 

  • Harnish DC, Malik S, Kilbourne E, Costa R, Karathanasis SK (1996) Control of apolipoprotein AI gene expression through synergistic interactions between hepatocyte nuclear factors 3 and 4. J Biol Chem 271:13621–13628

    Article  CAS  PubMed  Google Scholar 

  • Higuchi K, Law SW, Hoeg JM, Schumacher UK, Meglin N, Brewer HB (1988) Tissue-specific expression of apolipoprotein A-I (apoA-I) is regulated by the 5′-flanking region of the human apoA-I gene. J Biol Chem 263:18530–18536

    CAS  PubMed  Google Scholar 

  • Hirota K, Sakamaki JI, Ishida J, Shimamoto Y, Nishihara S, Kodama N, Ohta K, Yamamoto M, Tanimoto K, Fukamizu A (2008) A combination of HNF-4 and Foxo1 is required for reciprocal transcriptional regulation of glucokinase and glucose-6-phosphatase genes in response to fasting and feeding. J Biol Chem 283:32432–32441. doi:10.1074/jbc.M806179200

    Article  CAS  PubMed  Google Scholar 

  • Hopkins PN (2013) Molecular biology of atherosclerosis. Physiol Rev 93:1317–1542. doi:10.1152/physrev.00004.2012

    Article  CAS  PubMed  Google Scholar 

  • Huuskonen J, Vishnu M, Chau P, Fielding PE, Fielding CJ (2006) Liver X receptor inhibits the synthesis and secretion of apolipoprotein A1 by human liver-derived cells. Biochemistry 45:15068–15074. doi:10.1021/bi061378y

    Article  CAS  PubMed  Google Scholar 

  • Hwahng SH, Ki SH, Bae EJ, Kim HE, Kim SG (2009) Role of adenosine monophosphate-activated protein kinase-p70 ribosomal S6 kinase-1 pathway in repression of liver X receptor-alpha-dependent lipogenic gene induction and hepatic steatosis by a novel class of dithiolethiones. Hepatology 49:1913–1925. doi:10.1002/hep.22887

    Article  CAS  PubMed  Google Scholar 

  • Kim MJ, Byun JY, Yun CH, Park IC, Lee KH, Lee SJ (2008) c-Src-p38 mitogen-activated protein kinase signaling is required for Akt activation in response to ionizing radiation. Mol Cancer Res 6:1872–1880. doi:10.1158/1541-7786.MCR-08-0084

    Article  CAS  PubMed  Google Scholar 

  • Kitamura T, Ido Kitamura Y (2007) Role of FoxO proteins in pancreatic beta cells. Endocr J 54:507–515

    Article  CAS  PubMed  Google Scholar 

  • Klotz LO, Sánchez-Ramos C, Prieto-Arroyo I, Urbánek P, Steinbrenner H, Monsalve M (2015) Redox regulation of FoxO transcription factors. Redox Biol 6:51–72. doi:10.1016/j.redox.2015.06.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kontush A, Chapman MJ (2006) Functionally defective high-density lipoprotein: a new therapeutic target at the crossroads of dyslipidemia, inflammation, and atherosclerosis. Pharmacol Rev 58:342–374. doi:10.1124/pr.58.3.1

    Article  CAS  PubMed  Google Scholar 

  • Kyriakis JM, Avruch J (2012) Mammalian MAPK signal transduction pathways activated by stress and inflammation: a 10-year update. Physiol Rev 92:689–737. doi:10.1152/physrev.00028.2011

    Article  CAS  PubMed  Google Scholar 

  • Lapikov IA, Mogilenko DA, Dizhe EB, Ignatovich IA, Orlov SV, Perevozchikov AP (2008) Ap1-like cis-elements in 5′-regulatory region of human apolipoprotein A-I gene. Mol Biol (Mosk) 42:295–305

    Article  CAS  Google Scholar 

  • Lehtinen MK, Yuan Z, Boag PR, Yang Y, Villen J, Becker EB, DiBacco S, de la Iglesia N, Gygi S, Blackwell TK, Bonni A (2006) A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 125:987–1001. doi:10.1016/j.cell.2006.03.046

    Article  CAS  PubMed  Google Scholar 

  • Lewis GF, Rader DJ (2005) New insights into the regulation of HDL metabolism and reverse cholesterol transport. Circ Res 96:1221–1232. doi:10.1161/01.RES.0000170946.56981.5c

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Cui Y, Li M, Xu H, Zuo J, Fang F, Chang Y (2013) Cobalt protoporphyrin induces HO-1 expression mediated partially by FOXO1 and reduces mitochondria-derived reactive oxygen species production. PLoS One 8:1–9. doi:10.1371/journal.pone.0080521

    Google Scholar 

  • Malik S, Karathanasis SK (1996) TFIIB-directed transcriptional activation by the orphan nuclear receptor hepatocyte nuclear factor 4. Mol Cell Biol 16:1824–1831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin G, Duez H, Blanquart C, Berezowski V, Poulain P, Fruchart JC, Najib-Fruchart J, Glineur C, Staels B (2001) Statin-induced inhibition of the rho-signaling pathway activates PPARα and induces HDL apoA-I. J Clin Invest 107:1423–1432. doi:10.1172/JCI10852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez SC, Tanabe K, Crasme C, Abumrad NA, Bernal-mizrachi E, Permutt MA (2008) Inhibition of Foxo1 protects pancreatic islet beta-cells stress against fatty acid and endoplasmic reticulum stress–induced apoptosis. Diabetes 57:846–859. doi:10.2337/db07-0595

    Article  CAS  PubMed  Google Scholar 

  • McVicar JP, Kunitake ST, Hamilton RL, Kane JP (1984) Characteristics of human lipoproteins isolated by selected-affinity immunosorption of apolipoprotein A-I. Proc Natl Acad Sci U S A 81:1356–1360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mogilenko DA, Dizhe EB, Shavva VS, Lapikov IA, Orlov SV, Perevozchikov AP (2009) Role of the nuclear receptors HNF4 alpha, PPAR alpha, and LXRs in the TNF alpha-mediated inhibition of human apolipoprotein A-I gene expression in HepG2 cells. Biochemistry 48:11950–11960. doi:10.1021/bi9015742

    Article  CAS  PubMed  Google Scholar 

  • Mogilenko DA, Kudriavtsev IV, Shavva VS, Dizhe EB, Vilenskaya EG, Efremov AM, Perevozchikov AP, Orlov SV (2013) Peroxisome proliferator-activated receptor α positively regulates complement C3 expression but inhibits tumor necrosis factor α-mediated activation of C3 gene in mammalian hepatic-derived cells. J Biol Chem 288:1726–1738. doi:10.1074/jbc.M112.437525

    Article  CAS  PubMed  Google Scholar 

  • Mogilenko DA, Kudriavtsev IV, Trulioff AS, Shavva VS, Dizhe EB, Missyul BV, Zhakhov AV, Ischenko AM, Perevozchikov AP, Orlov SV (2012a) Modified low density lipoprotein stimulates complement C3 expression and secretion via liver X receptor and toll-like receptor 4 activation in human macrophages. J Biol Chem 287:5954–5968. doi:10.1074/jbc.M111.289322

    Article  CAS  PubMed  Google Scholar 

  • Mogilenko DA, Orlov SV, Trulioff AS, Ivanov AV, Nagumanov VK, Kudriavtsev IV, Shavva VS, Tanyanskiy DA, Perevozchikov AP (2012b) Endogenous apolipoprotein A-I stabilizes ATP-binding cassette transporter A1 and modulates toll-like receptor 4 signaling in human macrophages. FASEB J 26:2019–2030. doi:10.1096/fj.11-193946

    Article  CAS  PubMed  Google Scholar 

  • Morishima A, Ohkubo N, Maeda N, Miki T, Mitsuda N (2003) NFkappaB regulates plasma apolipoprotein A-I and high density lipoprotein cholesterol through inhibition of peroxisome proliferator-activated receptor alpha. J Biol Chem 278:38188–38193. doi:10.1074/jbc.M306336200

    Article  CAS  PubMed  Google Scholar 

  • Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxic assays. J Immunol Meth 65:55–63

    Article  CAS  Google Scholar 

  • Oleaga C, Ciudad CJ, Izquierdo-Pulido M, Noé V (2013) Cocoa flavanol metabolites activate HNF-3β, Sp1, and NFY-mediated transcription of apolipoprotein AI in human cells. Mol Nutr Food Res 57:986–995. doi:10.1002/mnfr.201200507

    Article  CAS  PubMed  Google Scholar 

  • Orlov SV, Kuteykin-Teplyakov KB, Ignatovich IA, Dizhe EB, Mirgorodskaya OA, Grishin AV, Guzhova OB, Prokhortchouk EB, Guliy PV, Perevozchikov AP (2007) Novel repressor of the human FMR1 gene—identification of p56 human (GCC)n-binding protein as a Kruppel-like transcription factor ZF5. FEBS J 274:4848–4862. doi:10.1111/j.1742-4658.2007.06006.x

    Article  CAS  PubMed  Google Scholar 

  • Orlov SV, Mogilenko DA, Shavva VS, Dizhe EB, Ignatovich IA, Perevozchikov AP (2010) Effect of TNFalpha on activities of different promoters of human apolipoprotein A-I gene. Biochem Biophys Res Commun 398:224–230. doi:10.1016/j.bbrc.2010.06.064

    Article  CAS  PubMed  Google Scholar 

  • Rani V, Deep G, Singh RK, Palle K, Yadav UCS (2016) Oxidative stress and metabolic disorders: pathogenesis and therapeutic strategies. Life Sci 148:183–193. doi:10.1016/j.lfs.2016.02.002

    Article  CAS  PubMed  Google Scholar 

  • Rena G, Guo S, Cichy SC, Unterman TG, Cohen P (1999) Phosphorylation of the transcription factor forkhead family member FKHR by protein kinase B. J Biol Chem 274:17179–17183. doi:10.1074/jbc.274.24.17179

    Article  CAS  PubMed  Google Scholar 

  • Sastry KN, Seedorf U, Karathanasis SK (1988) Different cis-acting DNA elements control expression of the human apolipoprotein AI gene in different cell types. Mol Cell Biol 8:605–614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schieber M, Chandel NS (2014) ROS function in redox signaling and oxidative stress. Curr Biol 24:R453–R462. doi:10.1016/j.cub.2014.03.034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmoll D, Walker KS, Alessi DR, Grempler R, Burchell A, Guo S, Walther R, Unterman TG (2000) Regulation of glucose-6-phosphatase gene expression by protein kinase Balpha and the forkhead transcription factor FKHR. Evidence for insulin response unit-dependent and-independent effects of insulin on promoter activity. J Biol Chem 275:36324–36333. doi:10.1074/jbc.M003616200

    Article  CAS  PubMed  Google Scholar 

  • Sengupta A, Molkentin JD, Paik JH, DePinho RA, Yutzey KE (2011) FoxO transcription factors promote cardiomyocyte survival upon induction of oxidative stress. J Biol Chem 286:7468–7478. doi:10.1074/jbc.M110.179242

    Article  CAS  PubMed  Google Scholar 

  • Shavva VS, Bogomolova AM, Nikitin AA, Dizhe EB, Tanyanskiy DA, Efremov AM, Oleinikova GN, Perevozchikov AP, Orlov SV (2016a) Insulin-mediated downregulation of apolipoprotein A-I gene in human hepatoma cell line HepG2: the role of interaction between FOXO1 and LXRβ transcription factors. J Cell Biochem. doi:10.1002/jcb.25651

    Google Scholar 

  • Shavva VS, Mogilenko DA, Bogomolova AM, Nikitin AA, Dizhe EB, Efremov AM, Oleinikova GN, Perevozchikov AP, Orlov SV (2016b) PPARγ represses apolipoprotein A-I gene but impedes TNFα-mediated apoA-I downregulation in HepG2 cells. J Cell Biochem 117:2010–2022. doi:10.1002/jcb.25498

    Article  CAS  PubMed  Google Scholar 

  • Shen M, Lin F, Zhang J, Tang Y, Chen WK, Liu H (2012) Involvement of the up-regulated FoxO1 expression in follicular granulosa cell apoptosis induced by oxidative stress. J Biol Chem 287:25727–25740. doi:10.1074/jbc.M112.349902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song H, Saito K, Fujigaki S, Noma A, Ishiguro H, Nagatsu T, Seishima M (1998) IL-1 beta and TNF-alpha suppress apolipoprotein (apo) E secretion and apo A-I expression in HepG2 cells. Cytokine 10:275–280

    Article  CAS  PubMed  Google Scholar 

  • Sunayama J, Tsuruta F, Masuyama N, Gotoh Y (2005) JNK antagonizes Akt-mediated survival signals by phosphorylating 14-3-3. J Cell Biol 170:295–304. doi:10.1083/jcb.200409117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tangeman L, Wyatt CN, Brown TL (2012) Knockdown of AMP-activated protein kinase alpha 1 and alpha 2 catalytic subunits. J RNAi Gene Silenc 8:470–478

    CAS  Google Scholar 

  • Van Der Heide LP, Hoekman MFM, Smidt MP (2004) The ins and outs of FoxO shuttling: mechanisms of FoxO translocation and transcriptional regulation. Biochem J 380:297–309. doi:10.1042/BJ20040167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vander Kooi BT, Streeper RS, Svitek CA, Oeser JK, Powell DR, O’Brien RM (2003) The three insulin response sequences in the glucose-6-phosphatase catalytic subunit gene promoter are functionally distinct. J Biol Chem 278:11782–11793. doi:10.1074/jbc.M212570200

    Article  CAS  PubMed  Google Scholar 

  • Widom RL, Ladias J, Kouidou S, Karathanasis SK (1991) Synergistic interactions between transcription factors control expression of the apolipoprotein AI gene in liver cells. Mol Cell Biol 11:677–687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamagata K, Daitoku H, Takahashi Y, Namiki K, Hisatake K, Kako K, Mukai H, Kasuya Y, Fukamizu A (2008) Arginine methylation of FOXO transcription factors inhibits their phosphorylation by Akt. Mol Cell 32:221–231. doi:10.1016/j.molcel.2008.09.013

    Article  CAS  PubMed  Google Scholar 

  • Yeagley D, Guo S, Unterman T, Quinn PG (2001) Gene- and activation-specific mechanisms for insulin inhibition of basal and glucocorticoid-induced insulin-like growth factor binding protein-1 and phosphoenolpyruvate carboxykinase transcription. Roles of forkhead and insulin response sequences. J Biol Chem 276:33705–33710. doi:10.1074/jbc.M101215200

    Article  CAS  PubMed  Google Scholar 

  • Yinghua JU, Taojun XU, Zhang H, Aiming YU (2014) FOXO1-dependent DNA damage repair is regulated by JNK in lung cancer cells. Int J Oncol 44:1284–1292. doi:10.3892/ijo.2014.2269

    Google Scholar 

  • Yoshizumi M, Abe J, Haendeler J, Huang Q, Berk BC (2000) Src and Cas mediate JNK activation but not ERK1/2 and p38 kinases by reactive oxygen species. J Biol Chem 275:11706–11712. doi:10.1074/jbc.275.16.11706

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The work has been supported by the Russian Foundation for Basic Research (Grants 15-04-07512, 15-04-08186, 15-04-07918 and 16-04-01312).

Author information

Authors and Affiliations

  1. Department of Biochemistry, Institute of Experimental Medicine, Russian Academy of Medical Sciences, Acad. Pavlov St., 12, St. Petersburg, 197376, Russia

    Vladimir S. Shavva, Artemy A. Nikitin, Ella B. Dizhe, Galina N. Oleinikova, Dmitry A. Tanyanskiy, Andrej P. Perevozchikov & Sergey V. Orlov

  2. Department of Embryology, St. Petersburg State University, St. Petersburg, Russia

    Vladimir S. Shavva, Ivan A. Lapikov, Andrej P. Perevozchikov & Sergey V. Orlov

  3. Department of Biochemistry, St. Petersburg State University, St. Petersburg, Russia

    Alexandra M. Bogomolova & Artemy A. Nikitin

  4. Department of Fundamental Medicine and Medical Technologies, St. Petersburg State University, St. Petersburg, Russia

    Dmitry A. Tanyanskiy

Authors
  1. Vladimir S. Shavva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexandra M. Bogomolova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Artemy A. Nikitin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ella B. Dizhe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Galina N. Oleinikova
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ivan A. Lapikov
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Dmitry A. Tanyanskiy
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Andrej P. Perevozchikov
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Sergey V. Orlov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Vladimir S. Shavva or Sergey V. Orlov.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shavva, V.S., Bogomolova, A.M., Nikitin, A.A. et al. FOXO1 and LXRα downregulate the apolipoprotein A-I gene expression during hydrogen peroxide-induced oxidative stress in HepG2 cells. Cell Stress and Chaperones 22, 123–134 (2017). https://doi.org/10.1007/s12192-016-0749-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12192-016-0749-6

Keywords

Search

Navigation