Endoplasmic reticulum stress and lipid dysregulation

Stephen M. Colgan; Ali A. Al-Hashimi; Richard C. Austin

doi:10.1017/S1462399410001742

Endoplasmic reticulum stress and lipid dysregulation

Published online by Cambridge University Press: 03 February 2011

Stephen M. Colgan ,

Ali A. Al-Hashimi and

Richard C. Austin

Show author details

Stephen M. Colgan: Affiliation:
Department of Medicine and Division of Nephrology, St Joseph's Healthcare Hamilton and McMaster University, Hamilton, Ontario, Canada.
Ali A. Al-Hashimi: Affiliation:
Department of Medicine and Division of Nephrology, St Joseph's Healthcare Hamilton and McMaster University, Hamilton, Ontario, Canada.
Richard C. Austin*: Affiliation:
Department of Medicine and Division of Nephrology, St Joseph's Healthcare Hamilton and McMaster University, Hamilton, Ontario, Canada.
*: *Corresponding author: Richard C. Austin, 50 Charlton Avenue East, Room T-3313, Hamilton, Ontario, CanadaL8N 4A6. E-mail: austinr@taari.ca

Article contents

Abstract
References

Get access

Rights & Permissions

Abstract

Cellular cholesterol homeostasis is a fundamental and highly regulated process. Transcription factors known as sterol regulatory element binding proteins (SREBPs) coordinate the expression of many genes involved in the biosynthesis and uptake of cholesterol. Dysregulation of SREBP activation and cellular lipid accumulation has been associated with endoplasmic reticulum (ER) stress and activation of the unfolded protein response (UPR). This review will provide an overview of ER stress and the UPR as well as cholesterol homeostasis and SREBP regulation, with an emphasis on their interaction and biological relevance.

Information

Type: Review Article
Information: Expert Reviews in Molecular Medicine , Volume 13 , March 2011 , e4

DOI: https://doi.org/10.1017/S1462399410001742 [Opens in a new window]
Copyright: Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

1Lee, A.S. (2001) The glucose-regulated proteins: stress induction and clinical applications. Trends in Biochemical Sciences 26, 504-510CrossRef Google Scholar PubMed

2Ellgaard, L. and Helenius, A. (2003) Quality control in the endoplasmic reticulum. Nature Reviews. Molecular Cell Biology 4, 181-191CrossRef Google Scholar PubMed

3Hebert, D.N., Foellmer, B. and Helenius, A. (1995) Glucose trimming and reglucosylation determine glycoprotein association with calnexin in the endoplasmic reticulum. Cell 81, 425-433CrossRef Google Scholar PubMed

4Sitia, R. and Braakman, I. (2003) Quality control in the endoplasmic reticulum protein factory. Nature 426, 891-894CrossRef Google Scholar PubMed

5Ma, Y. and Hendershot, L.M. (2004) ER chaperone functions during normal and stress conditions. Journal of Chemical Neuroanatomy 28, 51-65CrossRef Google Scholar PubMed

6Flynn, G.C. et al. (1991) Peptide-binding specificity of the molecular chaperone BiP. Nature 353, 726-730CrossRef Google Scholar PubMed

7Chung, K.T., Shen, Y. and Hendershot, L.M. (2002) BAP, a mammalian BiP-associated protein, is a nucleotide exchange factor that regulates the ATPase activity of BiP. Journal of Biological Chemistry 277, 47557-47563CrossRef Google Scholar PubMed

8Hendershot, L. et al. (1996) Inhibition of immunoglobulin folding and secretion by dominant negative BiP ATPase mutants. Proceedings of the National Academy of Sciences of the United States of America 93, 5269-5274CrossRef Google Scholar PubMed

9Kaufman, R.J. (2002) Orchestrating the unfolded protein response in health and disease. Journal of Clinical Investigation 110, 1389-1398CrossRef Google Scholar PubMed

10Ron, D. (2002) Translational control in the endoplasmic reticulum stress response. Journal of Clinical Investigation 110, 1383-1388CrossRef Google Scholar PubMed

11Lawrence de Koning, A.B. et al. (2003) Hyperhomocysteinemia and its role in the development of atherosclerosis. Clinical Biochemistry 36, 431-441CrossRef Google Scholar PubMed

12Rutkowski, D.T. and Kaufman, R.J. (2004) A trip to the ER: coping with stress. Trends in Cell Biology 14, 20-28CrossRef Google Scholar

13Ron, D. and Hubbard, S.R. (2008) How IRE1 reacts to ER stress. Cell 132, 24-26CrossRef Google Scholar PubMed

14Pincus, D. et al. (2010) BiP binding to the ER-stress sensor Ire1 tunes the homeostatic behavior of the unfolded protein response. PLoS Biology 8, e1000415CrossRef Google Scholar

15Yoshida, H. et al. (1998) Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors. Journal of Biological Chemistry 273, 33741-33749CrossRef Google Scholar PubMed

16Yoshida, H. et al. (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107, 881-891CrossRef Google Scholar PubMed

17Tirasophon, W. et al. (2000) The endoribonuclease activity of mammalian IRE1 autoregulates its mRNA and is required for the unfolded protein response. Genes and Development 14, 2725-2736CrossRef Google Scholar PubMed

18Chen, X., Shen, J. and Prywes, R. (2002) The luminal domain of ATF6 senses endoplasmic reticulum (ER) stress and causes translocation of ATF6 from the ER to the Golgi. Journal of Biological Chemistry 277, 13045-13052CrossRef Google Scholar PubMed

19Shen, J. et al. (2002) ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Developmental Cell 3, 99-111CrossRef Google Scholar PubMed

20Haze, K. et al. (1999) Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Molecular Biology of the Cell 10, 3787-3799CrossRef Google Scholar PubMed

21Ye, J. et al. (2000) ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Molecular Cell 6, 1355-1364CrossRef Google Scholar PubMed

22Lee, K. et al. (2002) IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes and Development 16, 452-466CrossRef Google Scholar PubMed

23Harding, H.P., Zhang, Y. and Ron, D. (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271-274CrossRef Google Scholar PubMed

24Damiano, F. et al. (2010) Translational control of the sterol-regulatory transcription factor SREBP-1 mRNA in response to serum starvation or ER stress is mediated by an internal ribosome entry site. Biochemical Journal 429, 603-612CrossRef Google Scholar PubMed

25Feng, B. et al. (2003) The endoplasmic reticulum is the site of cholesterol-induced cytotoxicity in macrophages. Nature Cell Biology 5, 781-792CrossRef Google Scholar PubMed

26Hossain, G.S. et al. (2003) TDAG51 is induced by homocysteine, promotes detachment-mediated programmed cell death, and contributes to the cevelopment of atherosclerosis in hyperhomocysteinemia. Journal of Biological Chemistry 278, 30317-30327CrossRef Google Scholar

27Morishima, N. et al. (2002) An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. Journal of Biological Chemistry 277, 34287-34294CrossRef Google Scholar PubMed

28Nakagawa, T. et al. (2000) Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403, 98-103CrossRef Google Scholar PubMed

29Maxfield, F.R. and Wustner, D. (2002) Intracellular cholesterol transport. Journal of Clinical Investigation 110, 891-898CrossRef Google Scholar PubMed

30Maxfield, F.R. and Tabas, I. (2005) Role of cholesterol and lipid organization in disease. Nature 438, 612-621CrossRef Google Scholar PubMed

31Chang, T.Y. et al. (2005) Niemann–Pick type C disease and intracellular cholesterol trafficking. Journal of Biological Chemistry 280, 20917-20920CrossRef Google Scholar PubMed

32Soccio, R.E. and Breslow, J.L. (2004) Intracellular cholesterol transport. Arteriosclerosis, Thrombosis, and Vascular Biology 24, 1150-1160CrossRef Google Scholar PubMed

33Espenshade, P.J. and Hughes, A.L. (2007) Regulation of sterol synthesis in eukaryotes. Annual Review of Genetics 41, 401-427CrossRef Google Scholar PubMed

34Sakashita, N. et al. (2000) Localization of human acyl-coenzyme A: cholesterol acyltransferase-1 (ACAT-1) in macrophages and in various tissues. American Journal of Pathology 156, 227-236CrossRef Google Scholar PubMed

35Chang, T.Y. et al. (2006) Cholesterol sensing, trafficking, and esterification. Annual Review of Cell and Developmental Biology 22, 129-157CrossRef Google Scholar PubMed

36Goldstein, J.L. and Brown, M.S. (2008) From fatty streak to fatty liver: 33 years of joint publications in the JCI. Journal of Clinical Investigation 118, 1220-1222CrossRef Google Scholar PubMed

37Briggs, M.R. et al. (1993) Nuclear protein that binds sterol regulatory element of low density lipoprotein receptor promoter. I. Identification of the protein and delineation of its target nucleotide sequence. Journal of Biological Chemistry 268, 14490-14496CrossRef Google Scholar PubMed

38Horton, J.D., Goldstein, J.L. and Brown, M.S. (2002) SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. Journal of Clinical Investigation 109, 1125-1131CrossRef Google Scholar PubMed

39Hua, X. et al. (1993) SREBP-2, a second basic-helix-loop-helix-leucine zipper protein that stimulates transcription by binding to a sterol regulatory element. Proceedings of the National Academy of Sciences of the United States of America 90, 11603-11607CrossRef Google Scholar PubMed

40Rawson, R.B. (2003) The SREBP pathway – insights from Insigs and insects. Nature Reviews. Molecular Cell Biology 4, 631-640CrossRef Google Scholar PubMed

41Wang, X. et al. (1993) Nuclear protein that binds sterol regulatory element of low density lipoprotein receptor promoter. II. Purification and characterization. Journal of Biological Chemistry 268, 14497-14504CrossRef Google Scholar PubMed

42Yokoyama, C. et al. (1993) SREBP-1, a basic-helix-loop-helix-leucine zipper protein that controls transcription of the low density lipoprotein receptor gene. Cell 75, 187-197CrossRef Google Scholar PubMed

43Jeong, H.J. et al. (2008) Sterol-dependent regulation of proprotein convertase subtilisin/kexin type 9 expression by sterol-regulatory element binding protein-2. Journal of Lipid Research 49, 399-409CrossRef Google Scholar PubMed

44Seidah, N.G., Khatib, A.M. and Prat, A. (2006) The proprotein convertases and their implication in sterol and/or lipid metabolism. Biological Chemistry 387, 871-877CrossRef Google Scholar PubMed

45Goldstein, J.L. and Brown, M.S. (1990) Regulation of the mevalonate pathway. Nature 343, 425-430CrossRef Google Scholar PubMed

46Vallett, S.M. et al. (1996) A direct role for sterol regulatory element binding protein in activation of 3-hydroxy-3-methylglutaryl coenzyme A reductase gene. Journal of Biological Chemistry 271, 12247-12253CrossRef Google Scholar PubMed

47Sheng, Z. et al. (1995) Independent regulation of sterol regulatory element-binding proteins 1 and 2 in hamster liver. Proceedings of the National Academy of Sciences of the United States of America 92, 935-938CrossRef Google Scholar PubMed

48Wang, X. et al. (1994) SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis. Cell 77, 53-62CrossRef Google Scholar PubMed

49Hua, X. et al. (1995) Structure of the human gene encoding sterol regulatory element binding protein-1 (SREBF1) and localization of SREBF1 and SREBF2 to chromosomes 17p11.2 and 22q13. Genomics 25, 667-673CrossRef Google Scholar PubMed

50Shimomura, I. et al. (1997) Differential expression of exons 1a and 1c in mRNAs for sterol regulatory element binding protein-1 in human and mouse organs and cultured cells. Journal of Clinical Investigation 99, 838-845CrossRef Google Scholar PubMed

51Horton, J.D. et al. (1998) Activation of cholesterol synthesis in preference to fatty acid synthesis in liver and adipose tissue of transgenic mice overproducing sterol regulatory element-binding protein-2. Journal of Clinical Investigation 101, 2331-2339CrossRef Google Scholar PubMed

52Hua, X. et al. (1996) Sterol resistance in CHO cells traced to point mutation in SREBP cleavage-activating protein. Cell 87, 415-426CrossRef Google Scholar

53Nohturfft, A., Brown, M.S. and Goldstein, J.L. (1998) Topology of SREBP cleavage-activating protein, a polytopic membrane protein with a sterol-sensing domain. Journal of Biological Chemistry 273, 17243-17250CrossRef Google Scholar PubMed

54Sakai, J. et al. (1998) Cleavage of sterol regulatory element-binding proteins (SREBPs) at site-1 requires interaction with SREBP cleavage-activating protein. Evidence from in vivo competition studies. Journal of Biological Chemistry 273, 5785-5793CrossRef Google Scholar PubMed

55Sakai, J. et al. (1997) Identification of complexes between the COOH-terminal domains of sterol regulatory element-binding proteins (SREBPs) and SREBP cleavage-activating protein. Journal of Biological Chemistry 272, 20213-20221CrossRef Google Scholar PubMed

56Yang, T., Goldstein, J.L. and Brown, M.S. (2000) Overexpression of membrane domain of SCAP prevents sterols from inhibiting SCAP.SREBP exit from endoplasmic reticulum. Journal of Biological Chemistry 275, 29881-29886CrossRef Google Scholar PubMed

57Nohturfft, A. et al. (2000) Regulated step in cholesterol feedback localized to budding of SCAP from ER membranes. Cell 102, 315-323CrossRef Google Scholar PubMed

58Nohturfft, A., Brown, M.S. and Goldstein, J.L. (1998) Sterols regulate processing of carbohydrate chains of wild-type SREBP cleavage-activating protein (SCAP), but not sterol-resistant mutants Y298C or D443N. Proceedings of the National Academy of Sciences of the United States of America 95, 12848-12853CrossRef Google Scholar PubMed

59Yang, T. et al. (2002) Crucial step in cholesterol homeostasis: sterols promote binding of SCAP to INSIG-1, a membrane protein that facilitates retention of SREBPs in ER. Cell 110, 489-500CrossRef Google Scholar PubMed

60Yabe, D., Brown, M.S. and Goldstein, J.L. (2002) Insig-2, a second endoplasmic reticulum protein that binds SCAP and blocks export of sterol regulatory element-binding proteins. Proceedings of the National Academy of Sciences of the United States of America 99, 12753-12758CrossRef Google Scholar PubMed

61Sun, L.P. et al. (2005) Insig required for sterol-mediated inhibition of Scap/SREBP binding to COPII proteins in vitro. Journal of Biological Chemistry 280, 26483-26490CrossRef Google Scholar PubMed

62Sun, L.P. et al. (2007) Sterol-regulated transport of SREBPs from endoplasmic reticulum to Golgi: Insig renders sorting signal in Scap inaccessible to COPII proteins. Proceedings of the National Academy of Sciences of the United States of America 104, 6519-6526CrossRef Google Scholar PubMed

63Hua, X. et al. (1996) Regulated cleavage of sterol regulatory element binding proteins requires sequences on both sides of the endoplasmic reticulum membrane. Journal of Biological Chemistry 271, 10379-10384CrossRef Google Scholar PubMed

64Sakai, J. et al. (1996) Sterol-regulated release of SREBP-2 from cell membranes requires two sequential cleavages, one within a transmembrane segment. Cell 85, 1037-1046CrossRef Google Scholar PubMed

65Nohturfft, A. et al. (1999) Sterols regulate cycling of SREBP cleavage-activating protein (SCAP) between endoplasmic reticulum and Golgi. Proceedings of the National Academy of Sciences of the United States of America 96, 11235-11240CrossRef Google Scholar PubMed

66Hegarty, B.D. et al. (2005) Distinct roles of insulin and liver X receptor in the induction and cleavage of sterol regulatory element-binding protein-1c. Proceedings of the National Academy of Sciences of the United States of America 102, 791-796CrossRef Google Scholar PubMed

67Yellaturu, C.R. et al. (2009) Insulin enhances the biogenesis of nuclear sterol regulatory element-binding protein (SREBP)-1c by posttranscriptional down-regulation of Insig-2A and its dissociation from SREBP cleavage-activating protein (SCAP).SREBP-1c complex. Journal of Biological Chemistry 284, 31726-31734CrossRef Google Scholar PubMed

68Yabe, D. et al. (2003) Liver-specific mRNA for Insig-2 down-regulated by insulin: implications for fatty acid synthesis. Proceedings of the National Academy of Sciences of the United States of America 100, 3155-3160CrossRef Google Scholar PubMed

69Shimomura, I. et al. (1997) Cholesterol feeding reduces nuclear forms of sterol regulatory element binding proteins in hamster liver. Proceedings of the National Academy of Sciences of the United States of America 94, 12354-12359CrossRef Google Scholar PubMed

70Esfandiari, F. et al. (2005) Chronic ethanol feeding and folate deficiency activate hepatic endoplasmic reticulum stress pathway in micropigs. American Journal of Physiology. Gastrointestinal Liver Physiology 289, G54-G63CrossRef Google Scholar PubMed

71Ji, C. and Kaplowitz, N. (2003) Betaine decreases hyperhomocysteinemia, endoplasmic reticulum stress, and liver injury in alcohol-fed mice. Gastroenterology 124, 1488-1499CrossRef Google Scholar PubMed

72Kim, A.J. et al. (2005) Valproate protects cells from ER stress-induced lipid accumulation and apoptosis by inhibiting glycogen synthase kinase-3. Journal of Cell Science 118, 89-99CrossRef Google Scholar PubMed

73Werstuck, G.H. et al. (2001) Homocysteine-induced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways. Journal of Clinical Investigation 107, 1263-1273CrossRef Google Scholar PubMed

74Kammoun, H.L. et al. (2009) GRP78 expression inhibits insulin and ER stress-induced SREBP-1c activation and reduces hepatic steatosis in mice. Journal of Clinical Investigation 119, 1201-1215CrossRef Google Scholar PubMed

75Colgan, S.M. et al. (2007) Endoplasmic reticulum stress causes the activation of sterol regulatory element binding protein-2. International Journal of Biochemistry and Cell Biology 39, 1843-1851CrossRef Google Scholar PubMed

76Zhou, J. and Austin, R.C. (2009) Contributions of hyperhomocysteinemia to atherosclerosis: causal relationship and potential mechanisms. Biofactors 35, 120-129CrossRef Google Scholar PubMed

77Outinen, P.A. et al. (1999) Homocysteine-induced endoplasmic reticulum stress and growth arrest leads to specific changes in gene expression in human vascular endothelial cells. Blood 94, 959-967CrossRef Google Scholar PubMed

78Outinen, P.A. et al. (1998) Characterization of the stress-inducing effects of homocysteine. Biochemical Journal 332 (Pt 1), 213-221CrossRef Google Scholar PubMed

79Woo, C.W. et al. (2005) Hyperhomocysteinemia induces hepatic cholesterol biosynthesis and lipid accumulation via activation of transcription factors. American Journal of Physiology. Endocrinology and Metabolism 288, E1002-E1010CrossRef Google Scholar PubMed

80Bobrovnikova-Marjon, E. et al. (2008) PERK-dependent regulation of lipogenesis during mouse mammary gland development and adipocyte differentiation. Proceedings of the National Academy of Sciences of the United States of America 105, 16314-16319CrossRef Google Scholar PubMed

81Wang, X. et al. (1995) Purification of an interleukin-1 beta converting enzyme-related cysteine protease that cleaves sterol regulatory element-binding proteins between the leucine zipper and transmembrane domains. Journal of Biological Chemistry 270, 18044-18050CrossRef Google Scholar PubMed

82Pai, J.T., Brown, M.S. and Goldstein, J.L. (1996) Purification and cDNA cloning of a second apoptosis-related cysteine protease that cleaves and activates sterol regulatory element binding proteins. Proceedings of the National Academy of Sciences of the United States of America 93, 5437-5442CrossRef Google Scholar PubMed

83Wang, X. et al. (1996) Cleavage of sterol regulatory element binding proteins (SREBPs) by CPP32 during apoptosis. EMBO Journal 15, 1012-1020CrossRef Google Scholar PubMed

84Higgins, M.E. and Ioannou, Y.A. (2001) Apoptosis-induced release of mature sterol regulatory element-binding proteins activates sterol-responsive genes. Journal of Lipid Research 42, 1939-1946CrossRef Google Scholar PubMed

85Lee, J.N. and Ye, J. (2004) Proteolytic activation of sterol regulatory element-binding protein induced by cellular stress through depletion of Insig-1. Journal of Biological Chemistry 279, 45257-45265CrossRef Google Scholar PubMed

86Rao, R.V. et al. (2002) Coupling endoplasmic reticulum stress to the cell death program. An Apaf-1-independent intrinsic pathway. Journal of Biological Chemistry 277, 21836-21842CrossRef Google Scholar

87Shiraishi, H. et al. (2006) ER stress-induced apoptosis and caspase-12 activation occurs downstream of mitochondrial apoptosis involving Apaf-1. Journal of Cell Science 119, 3958-3966CrossRef Google Scholar PubMed

88Shimano, H. et al. (1996) Overproduction of cholesterol and fatty acids causes massive liver enlargement in transgenic mice expressing truncated SREBP-1a. Journal of Clinical Investigation 98, 1575-1584CrossRef Google Scholar PubMed

89Horton, J.D. et al. (2003) Overexpression of sterol regulatory element-binding protein-1a in mouse adipose tissue produces adipocyte hypertrophy, increased fatty acid secretion, and fatty liver. Journal of Biological Chemistry 278, 36652-36660CrossRef Google Scholar PubMed

90Shimomura, I. et al. (1998) Insulin resistance and diabetes mellitus in transgenic mice expressing nuclear SREBP-1c in adipose tissue: model for congenital generalized lipodystrophy. Genes and Development 12, 3182-3194CrossRef Google Scholar PubMed

91Zager, R.A. and Johnson, A. (2001) Renal cortical cholesterol accumulation is an integral component of the systemic stress response. Kidney International 60, 2299-2310CrossRef Google Scholar PubMed

92Zager, R.A. et al. (2001) Cholesterol ester accumulation: an immediate consequence of acute in vivo ischemic renal injury. Kidney International 59, 1750-1761CrossRef Google Scholar PubMed

93Zager, R.A. et al. (2003) Acute tubular injury causes dysregulation of cellular cholesterol transport proteins. American Journal of Pathology 163, 313-320CrossRef Google Scholar PubMed

94Zager, R.A. et al. (2002) The mevalonate pathway during acute tubular injury: selected determinants and consequences. American Journal of Pathology 161, 681-692CrossRef Google Scholar

95Zager, R.A., Johnson, A.C. and Hanson, S.Y. (2005) Renal tubular triglyercide accumulation following endotoxic, toxic, and ischemic injury. Kidney International 67, 111-121CrossRef Google Scholar PubMed

96Zager, R.A. (2000) Plasma membrane cholesterol: a critical determinant of cellular energetics and tubular resistance to attack. Kidney International 58, 193-205CrossRef Google Scholar PubMed

97Zager, R.A. et al. (1999) Increased proximal tubular cholesterol content: implications for cell injury and “acquired cytoresistance”. Kidney International 56, 1788-1797CrossRef Google Scholar PubMed

98Zager, R.A. and Kalhorn, T.F. (2000) Changes in free and esterified cholesterol: hallmarks of acute renal tubular injury and acquired cytoresistance. American Journal of Pathology 157, 1007-1016CrossRef Google Scholar PubMed

99Kimura, K. et al. (2008) Dysfunction of the ER chaperone BiP accelerates the renal tubular injury. Biochemical and Biophysical Research Communications 366, 1048-1053CrossRef Google Scholar PubMed

100Zinszner, H. et al. (1998) CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes and Development 12, 982-995CrossRef Google Scholar PubMed

101Moore, K.J. and Freeman, M.W. (2006) Scavenger receptors in atherosclerosis: beyond lipid uptake. Arteriosclerosis, Thrombosis, and Vascular Biology 26, 1702-1711CrossRef Google Scholar PubMed

102Manning-Tobin, J.J. et al. (2009) Loss of SR-A and CD36 activity reduces atherosclerotic lesion complexity without abrogating foam cell formation in hyperlipidemic mice. Arteriosclerosis, Thrombosis, and Vascular Biology 29, 19-26CrossRef Google Scholar PubMed

103Ecker, J. et al. (2010) Induction of fatty acid synthesis is a key requirement for phagocytic differentiation of human monocytes. Proceedings of the National Academy of Sciences of the United States of America 107, 7817-7822CrossRef Google Scholar PubMed

104Zhou, R.H. et al. (2004) Vascular endothelial growth factor activation of sterol regulatory element binding protein: a potential role in angiogenesis. Circulation Research 95, 471-478CrossRef Google Scholar PubMed

105Yeh, M. et al. (2004) Role for sterol regulatory element-binding protein in activation of endothelial cells by phospholipid oxidation products. Circulation Research 95, 780-788CrossRef Google Scholar PubMed

Article contents

Endoplasmic reticulum stress and lipid dysregulation

Abstract

Information

Access options

Article purchase

Temporarily unavailable

References

References

Further reading, resources and contacts

This article has been cited by the following publications. This list is generated based on data provided by Crossref.

Article contents

Endoplasmic reticulum stress and lipid dysregulation

Abstract

Information

Access options

Article purchase

Temporarily unavailable

References

References

Further reading, resources and contacts

Save article to Kindle

Save article to Dropbox

Save article to Google Drive

Reply to: Submit a response

Your details

You have entered the maximum number of contributors

Conflicting interests