Skip to main content
Top
Published in: Calcified Tissue International 6/2016

01-06-2016 | Original Research

Inhibition of ABCA1 Protein Expression and Cholesterol Efflux by TNF α in MLO-Y4 Osteocytes

Authors: Kent R. Wehmeier, William Kurban, Chandrikha Chandrasekharan, Luisa Onstead-Haas, Arshag D. Mooradian, Michael J. Haas

Published in: Calcified Tissue International | Issue 6/2016

Login to get access

Abstract

Hip fracture and myocardial infarction cause significant morbidity and mortality. In vivo studies raising serum cholesterol levels as well as pro-inflammatory cytokines such as TNF α manifest bone loss and atherosclerotic vascular disease, suggesting that abnormalities of cholesterol transport may contribute to osteoporosis. We used the mouse osteocyte cell line (MLO-Y4) to investigate the effects of TNF α on the expression of cholesterol acceptor proteins such as apolipoprotein A-I (apo A-I) and apolipoprotein E (apo E), as well as on the cholesterol transporters ATP-binding cassette-1 (ABCA1), scavenger receptor class B type 1 (SRB1), and cluster of differentiation 36 (CD36). MLO-Y4 cells do not express apo A-I or apo E; however, they do express all three cholesterol transporters (ABCA1, SRB1, and CD36). Treatment of MLO-Y4 cells with TNF α had no effect on SRB1, CD36, and osteocalcin levels; however, TNF α reduced ABCA1 protein levels in a dose-dependent manner and cholesterol efflux to apo A-I. Interestingly, TNF α treatment increased ABCA1 promoter activity and ABCA1 mRNA levels, and increased liver X receptor α protein expression, but had no effect on retinoid X receptor α and retinoic acid receptor α levels. Pharmacological inhibition of p38 mitogen-activated protein (MAP) kinase, but not c-jun-N-terminal kinase 1 or mitogen-activated protein kinase (MEK), restored ABCA1 protein levels in TNF α-treated cells. These results suggest that pro-inflammatory cytokines regulate cholesterol metabolism in osteocytes in part by suppressing ABCA1 levels post-translationally in a p38 MAP kinase-dependent manner.
Literature
2.
go back to reference Anderson JB, Barnett E, Nordin BE (1964) The relation between osteoporosis and aortic calcification. Br J Radiol 37:910–912CrossRefPubMed Anderson JB, Barnett E, Nordin BE (1964) The relation between osteoporosis and aortic calcification. Br J Radiol 37:910–912CrossRefPubMed
3.
go back to reference Marcovitz PA, Tran HH, Franklin BA, O’Neill WW, Yerkey M, Boura J, Kleerekoper M, Dickinson CZ (2005) Usefulness of bone mineral density to predict significant coronary artery disease. Am J Cardiol 96:1059–1063CrossRefPubMed Marcovitz PA, Tran HH, Franklin BA, O’Neill WW, Yerkey M, Boura J, Kleerekoper M, Dickinson CZ (2005) Usefulness of bone mineral density to predict significant coronary artery disease. Am J Cardiol 96:1059–1063CrossRefPubMed
4.
go back to reference Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confaverux C, Dacquin R, Mee PJ, McKee MD, Jung DY, Zhang Z, Kim JK, Mauvais-Jarvis F, Ducy P, Karsenty G (2007) Endocrine regulation of energy metabolism by the skeleton. Cell 130:456–469CrossRefPubMedPubMedCentral Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confaverux C, Dacquin R, Mee PJ, McKee MD, Jung DY, Zhang Z, Kim JK, Mauvais-Jarvis F, Ducy P, Karsenty G (2007) Endocrine regulation of energy metabolism by the skeleton. Cell 130:456–469CrossRefPubMedPubMedCentral
6.
go back to reference Fontova R, Gutierrez C, Vendrell J, Broch M, Vendrell I, Simon I, Fernández-Real JM, Richart C (2002) Bone mineral mass is associated with interleukin 1 receptor autoantigen and TNF-alpha gene polymorphisms in post-menopausal Mediterranean women. J Endocrinol Invest 25:684–690CrossRefPubMed Fontova R, Gutierrez C, Vendrell J, Broch M, Vendrell I, Simon I, Fernández-Real JM, Richart C (2002) Bone mineral mass is associated with interleukin 1 receptor autoantigen and TNF-alpha gene polymorphisms in post-menopausal Mediterranean women. J Endocrinol Invest 25:684–690CrossRefPubMed
7.
go back to reference Parra-Rojas I, Ruiz-Madrigal B, Martinez-Lopez E, Panduro A (2006) Influence of the -308 TNF-alpha and -174 IL-6 polymorphisms on lipid profile in Mexican subjects. Hereditas 143:167–172CrossRefPubMed Parra-Rojas I, Ruiz-Madrigal B, Martinez-Lopez E, Panduro A (2006) Influence of the -308 TNF-alpha and -174 IL-6 polymorphisms on lipid profile in Mexican subjects. Hereditas 143:167–172CrossRefPubMed
8.
go back to reference Li Y, Li A, Strait K, Zhang H, Nanes MS, Weitzmann MN (2007) Endogenous TNFalpha lowers maximum bone mass and inhibits osteoblastic Smad activation through NF-kappaB. J Bone Miner Res 22:646–655CrossRefPubMed Li Y, Li A, Strait K, Zhang H, Nanes MS, Weitzmann MN (2007) Endogenous TNFalpha lowers maximum bone mass and inhibits osteoblastic Smad activation through NF-kappaB. J Bone Miner Res 22:646–655CrossRefPubMed
12.
go back to reference Zhang K, Barragan-Adjemian C, Ye L, Kotha S, Dallas M, Lu Y, Zhao S, Harris M, Harris SE, Feng JQ, Bonewald LF (2006) E11/gp38 selective expression in osteocytes: regulation by mechanical strain and role in dendrite elongation. Mol Cell Biol 26:4539–4552CrossRefPubMedPubMedCentral Zhang K, Barragan-Adjemian C, Ye L, Kotha S, Dallas M, Lu Y, Zhao S, Harris M, Harris SE, Feng JQ, Bonewald LF (2006) E11/gp38 selective expression in osteocytes: regulation by mechanical strain and role in dendrite elongation. Mol Cell Biol 26:4539–4552CrossRefPubMedPubMedCentral
14.
go back to reference Bodzioch M, Orso E, Klucken J, Langmann T, Böttcher A, Diederich W, Drobnik W, Barlage S, Büchler C, Porsch-Ozcürümez M, Kaminski WE, Hahmann HW, Oette K, Rothe G, Aslanidis C, Lackner KJ, Schmitz G (1999) The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat Genet 22:347–351CrossRefPubMed Bodzioch M, Orso E, Klucken J, Langmann T, Böttcher A, Diederich W, Drobnik W, Barlage S, Büchler C, Porsch-Ozcürümez M, Kaminski WE, Hahmann HW, Oette K, Rothe G, Aslanidis C, Lackner KJ, Schmitz G (1999) The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat Genet 22:347–351CrossRefPubMed
18.
go back to reference Khovidhunkit W, Moser AH, Shigenaga JK, Grunfeld C, Feingold KR (2003) Endotoxin down-regulates ABCG5 and ABCG8 in mouse liver and ABCA1 and ABCG1 in J774 murine macrophages: differential role of LXR. J Lipid Res 44:1728–1736CrossRefPubMed Khovidhunkit W, Moser AH, Shigenaga JK, Grunfeld C, Feingold KR (2003) Endotoxin down-regulates ABCG5 and ABCG8 in mouse liver and ABCA1 and ABCG1 in J774 murine macrophages: differential role of LXR. J Lipid Res 44:1728–1736CrossRefPubMed
20.
go back to reference Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85CrossRefPubMed Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85CrossRefPubMed
21.
go back to reference Herbomel P, Bourachot B, Yaniv M (1984) Two distinct enhancers with different cell specificities coexist in the regulatory region of polyoma. Cell 39:653–662CrossRefPubMed Herbomel P, Bourachot B, Yaniv M (1984) Two distinct enhancers with different cell specificities coexist in the regulatory region of polyoma. Cell 39:653–662CrossRefPubMed
22.
go back to reference Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 132:6–13 Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 132:6–13
25.
go back to reference Costet P, Luo Y, Wang N, Tall AR (2000) Sterol-dependent transactivation of the ABC1 promoter by the liver X receptor/retinoid X receptor. J Biol Chem 275:28240–28245PubMed Costet P, Luo Y, Wang N, Tall AR (2000) Sterol-dependent transactivation of the ABC1 promoter by the liver X receptor/retinoid X receptor. J Biol Chem 275:28240–28245PubMed
26.
go back to reference Schwartz K, Lawn RM, Wade DP (2000) ABC1 gene expression and apo-AI-mediated cholesterol efflux are regulated by LXR. Biochem Biophys Res Commun 274:794–802CrossRefPubMed Schwartz K, Lawn RM, Wade DP (2000) ABC1 gene expression and apo-AI-mediated cholesterol efflux are regulated by LXR. Biochem Biophys Res Commun 274:794–802CrossRefPubMed
27.
go back to reference Costet P, Lalanne F, Gerbod-Giannone MC, Molina JR, Fu X, Lund EG, Gudas LJ, Tall AR (2003) Retinoic acid receptor-mediated induction of ABCA1 in macrophages. Mol Cell Biol 23:7756–7766CrossRefPubMedPubMedCentral Costet P, Lalanne F, Gerbod-Giannone MC, Molina JR, Fu X, Lund EG, Gudas LJ, Tall AR (2003) Retinoic acid receptor-mediated induction of ABCA1 in macrophages. Mol Cell Biol 23:7756–7766CrossRefPubMedPubMedCentral
28.
go back to reference Guy GR, Chua SP, Wong NS, Ng SB, Tan YH (1991) Interleukin 1 and tumor necrosis factor activate common multiple protein kinases in human fibroblasts. J Biol Chem 266:14343–14352PubMed Guy GR, Chua SP, Wong NS, Ng SB, Tan YH (1991) Interleukin 1 and tumor necrosis factor activate common multiple protein kinases in human fibroblasts. J Biol Chem 266:14343–14352PubMed
29.
go back to reference Kyriakis JM, Avruch J (2001) Mammalian mitogen-activated protein kinase and signal transduction pathways activated by stress and inflammation. Physiol Rev 81:807–869PubMed Kyriakis JM, Avruch J (2001) Mammalian mitogen-activated protein kinase and signal transduction pathways activated by stress and inflammation. Physiol Rev 81:807–869PubMed
30.
go back to reference Yang H, Sadda MR, Yu V, Zeng Y, Lee TD, Ou X, Chen L, Lu SC (2003) Induction of human methionine adenosyltransferase 2A expression by tumor necrosis factor a. Role of NF-κB and AP-1. J Biol Chem 278:50887–50896CrossRefPubMed Yang H, Sadda MR, Yu V, Zeng Y, Lee TD, Ou X, Chen L, Lu SC (2003) Induction of human methionine adenosyltransferase 2A expression by tumor necrosis factor a. Role of NF-κB and AP-1. J Biol Chem 278:50887–50896CrossRefPubMed
31.
go back to reference Bachner D, Schroeder D, Betat N, Ahrens M, Gross G (1999) Apolipoprotein E (ApoE), a BMP-2 (bone morphogenetic protein) upregulated gene in mesenchymal progenitors (C3H10T1/2), is highly expressed in murine embryonic development. BioFactors 9:11–17CrossRefPubMed Bachner D, Schroeder D, Betat N, Ahrens M, Gross G (1999) Apolipoprotein E (ApoE), a BMP-2 (bone morphogenetic protein) upregulated gene in mesenchymal progenitors (C3H10T1/2), is highly expressed in murine embryonic development. BioFactors 9:11–17CrossRefPubMed
32.
go back to reference Laskowitz DT, Lee DM, Schmechel D, Staats HF (2000) Altered immune responses in apolipoprotein E-deficient mice. J Lipid Res 41:613–620PubMed Laskowitz DT, Lee DM, Schmechel D, Staats HF (2000) Altered immune responses in apolipoprotein E-deficient mice. J Lipid Res 41:613–620PubMed
33.
go back to reference Suda T, Takahashi N, Udagawa N, Jimi E, Gillespie MT, Martin TJ (1999) Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr Rev 20:342–345 Suda T, Takahashi N, Udagawa N, Jimi E, Gillespie MT, Martin TJ (1999) Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr Rev 20:342–345
34.
go back to reference Rao A, Luo C, Hogan PC (1997) Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol 15:707–747CrossRefPubMed Rao A, Luo C, Hogan PC (1997) Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol 15:707–747CrossRefPubMed
37.
go back to reference Beigneux AP, Moser AH, Shigenega JK, Grunfeld C, Feingold KR (2000) The acute phase response is associated with retinoid X receptor repression in rodent liver. J Biol Chem 275:16390–16399CrossRefPubMed Beigneux AP, Moser AH, Shigenega JK, Grunfeld C, Feingold KR (2000) The acute phase response is associated with retinoid X receptor repression in rodent liver. J Biol Chem 275:16390–16399CrossRefPubMed
38.
go back to reference Beigneux AP, Moser AH, Shigenega JK, Grunfeld C, Feingold KR (2003) Sick euthyroid syndrome is associated with decreased TR expression and DNA binding in mouse liver. Am J Physiol Endocrinol Metab 284:E228–E236CrossRefPubMed Beigneux AP, Moser AH, Shigenega JK, Grunfeld C, Feingold KR (2003) Sick euthyroid syndrome is associated with decreased TR expression and DNA binding in mouse liver. Am J Physiol Endocrinol Metab 284:E228–E236CrossRefPubMed
39.
go back to reference Morishima A, Ohkubo N, Maeda N, Miki T, Mitsuda N (2003) NFκB regulates plasma apolipoprotein A-I and high density lipoprotein cholesterol through inhibition of peroxisome proliferator-activated receptor α. J Biol Chem 278:38188–38193CrossRefPubMed Morishima A, Ohkubo N, Maeda N, Miki T, Mitsuda N (2003) NFκB regulates plasma apolipoprotein A-I and high density lipoprotein cholesterol through inhibition of peroxisome proliferator-activated receptor α. J Biol Chem 278:38188–38193CrossRefPubMed
41.
go back to reference Jessup W, Gelissen IC, Gaus K, Kritharides L (2006) Roles of ATP binding cassette transporters A1 and G1, scavenger receptor B1 and membrane lipid domains in cholesterol export from macrophages. Curr Opin Lipidol 17:247–257CrossRefPubMed Jessup W, Gelissen IC, Gaus K, Kritharides L (2006) Roles of ATP binding cassette transporters A1 and G1, scavenger receptor B1 and membrane lipid domains in cholesterol export from macrophages. Curr Opin Lipidol 17:247–257CrossRefPubMed
Metadata
Title
Inhibition of ABCA1 Protein Expression and Cholesterol Efflux by TNF α in MLO-Y4 Osteocytes
Authors
Kent R. Wehmeier
William Kurban
Chandrikha Chandrasekharan
Luisa Onstead-Haas
Arshag D. Mooradian
Michael J. Haas
Publication date
01-06-2016
Publisher
Springer US
Published in
Calcified Tissue International / Issue 6/2016
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-015-0106-2

Other articles of this Issue 6/2016

Calcified Tissue International 6/2016 Go to the issue