Skip to main content
  • American Heart Association
  • Science Volunteer
  • Warning Signs
  • Advanced Search
  • Donate

  • Home
  • About this Journal
    • Editorial Board
    • Meet the Editors
    • ATVB Journal History
    • General Statistics
  • All Issues
  • Subjects
    • All Subjects
    • Arrhythmia and Electrophysiology
    • Basic, Translational, and Clinical Research
    • Critical Care and Resuscitation
    • Epidemiology, Lifestyle, and Prevention
    • Genetics
    • Heart Failure and Cardiac Disease
    • Hypertension
    • Imaging and Diagnostic Testing
    • Intervention, Surgery, Transplantation
    • Quality and Outcomes
    • Stroke
    • Vascular Disease
  • Browse Features
    • Cover Art Award
    • ATVB Early Career Award
    • ATVB in Focus
    • Recent Brief Reviews of ATVB
    • Lecture Series
    • Collections
    • Recent Highlights of ATVB
    • Commentaries
    • Browse Abstracts
    • Insight into ATVB Authors
  • Resources
    • Instructions for Authors
    • Online Submission/Peer Review Site
    • Council on ATVB
    • Permissions and Rights Q&A
    • AHA Guidelines and Statements
    • Customer Service and Ordering Information
    • Author Reprints
    • International Users
    • AHA Newsroom
  • AHA Journals
    • AHA Journals Home
    • Arteriosclerosis, Thrombosis, and Vascular Biology (ATVB)
    • Circulation
    • → Circ: Arrhythmia and Electrophysiology
    • → Circ: Genomic and Precision Medicine
    • → Circ: Cardiovascular Imaging
    • → Circ: Cardiovascular Interventions
    • → Circ: Cardiovascular Quality & Outcomes
    • → Circ: Heart Failure
    • Circulation Research
    • Hypertension
    • Stroke
    • Journal of the American Heart Association
  • Facebook
  • LinkedIn
  • Twitter

  • My alerts
  • Sign In
  • Join

  • Advanced search

Header Publisher Menu

  • American Heart Association
  • Science Volunteer
  • Warning Signs
  • Advanced Search
  • Donate

Arteriosclerosis, Thrombosis, and Vascular Biology

  • My alerts
  • Sign In
  • Join

  • Facebook
  • LinkedIn
  • Twitter
  • Home
  • About this Journal
    • Editorial Board
    • Meet the Editors
    • ATVB Journal History
    • General Statistics
  • All Issues
  • Subjects
    • All Subjects
    • Arrhythmia and Electrophysiology
    • Basic, Translational, and Clinical Research
    • Critical Care and Resuscitation
    • Epidemiology, Lifestyle, and Prevention
    • Genetics
    • Heart Failure and Cardiac Disease
    • Hypertension
    • Imaging and Diagnostic Testing
    • Intervention, Surgery, Transplantation
    • Quality and Outcomes
    • Stroke
    • Vascular Disease
  • Browse Features
    • Cover Art Award
    • ATVB Early Career Award
    • ATVB in Focus
    • Recent Brief Reviews of ATVB
    • Lecture Series
    • Collections
    • Recent Highlights of ATVB
    • Commentaries
    • Browse Abstracts
    • Insight into ATVB Authors
  • Resources
    • Instructions for Authors
    • Online Submission/Peer Review Site
    • Council on ATVB
    • Permissions and Rights Q&A
    • AHA Guidelines and Statements
    • Customer Service and Ordering Information
    • Author Reprints
    • International Users
    • AHA Newsroom
  • AHA Journals
    • AHA Journals Home
    • Arteriosclerosis, Thrombosis, and Vascular Biology (ATVB)
    • Circulation
    • → Circ: Arrhythmia and Electrophysiology
    • → Circ: Genomic and Precision Medicine
    • → Circ: Cardiovascular Imaging
    • → Circ: Cardiovascular Interventions
    • → Circ: Cardiovascular Quality & Outcomes
    • → Circ: Heart Failure
    • Circulation Research
    • Hypertension
    • Stroke
    • Journal of the American Heart Association
ATVB in Focus: New Developments in Hepatic Lipoprotein Production and Clinical Relevance

CIDE Proteins and Lipid Metabolism

Li Xu, Linkang Zhou, Peng Li
Download PDF
https://doi.org/10.1161/ATVBAHA.111.241489
Arteriosclerosis, Thrombosis, and Vascular Biology. 2012;32:1094-1098
Originally published April 18, 2012
Li Xu
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Linkang Zhou
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Peng Li
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Article
  • Figures & Tables
  • Info & Metrics
  • eLetters

Jump to

  • Article
    • Abstract
    • Introduction
    • CIDE Proteins in Lipid Storage and LD Growth
    • CIDE Proteins in VLDL Lipidation and Maturation in Hepatocytes
    • Conclusion
    • Sources of Funding
    • Disclosures
    • References
  • Figures & Tables
  • Info & Metrics
  • eLetters
Loading

Abstract

Lipid homeostasis is maintained through the coordination of lipid metabolism in various tissues, including adipose tissue and the liver. The disruption of lipid homeostasis often results in the development of metabolic disorders such as obesity, diabetes mellitus, liver steatosis, and cardiovascular diseases. Cell death–inducing DNA fragmentation factor 45-like effector family proteins, including Cidea, Cideb, and Fsp27 (Cidec), are emerging as important regulators of various lipid metabolic pathways and play pivotal roles in the development of metabolic disorders. This review summarizes the latest cell death–inducing DNA fragmentation factor 45-like effector protein discoveries related to the control of lipid metabolism, with emphasis on the role of these proteins in lipid droplet growth in adipocytes and in the regulation of very low-density lipoprotein lipidation and maturation in hepatocytes.

  • cell death–inducing DNA fragmentation factor 45-like effector
  • lipid droplet
  • lipid metabolism
  • metabolic disorders
  • very low-density lipoprotein

Introduction

The cell death–inducing DNA fragmentation factor 45-like effector (CIDE) proteins, including Cidea, Cideb, and Cidec (or Fsp27 in mice), have been shown to play important roles in the development of metabolic disorders.1,2 Mice with a deficiency in CIDE proteins exhibit a lean phenotype, resistance to high-fat diet–induced obesity, improved insulin sensitivity, and an increased whole-body metabolic rate.1,3–6 Cidea and Cidec are expressed in the white adipose tissue of humans, and their expression positively correlates with the development of insulin sensitivity in obese people.7,8 A patient who expresses a prematurely terminated Cidec protein develops ketosis-prone insulin resistance and partial lipodystrophy.9 In addition, increased Cidea and Fsp27 expression have been observed in the livers of high-fat diet-fed and ob/ob mice and under the condition of hepatic steatosis in humans.10,11 The levels of hepatic expression of Cidea and Cidec also positively correlate with body mass index.12 Furthermore, hepatic Cidec mRNA levels are decreased in obese patients who lose weight as a result of gastric bypass surgery.12 Fsp27 has been identified as a peroxisome proliferator–activated receptor-γ target and plays a crucial role in peroxisome proliferator–activated receptor-γ–induced hepatic steatosis.10 In addition, Cidea is identified as a sensor of dietary saturated fatty for the development of hepatic steatosis.11 Cideb is expressed at high levels in the liver, and modulates very low-density lipoprotein (VLDL) lipidation and cholesterol homeostasis in hepatocytes.4,13–15 Recently, the levels of Cideb and Cidec have been found to be upregulated in macrophages in the presence of oxidized low-density lipoprotein, suggesting potential roles of Cideb and Cidec in foam cell formation and the development of atherosclerosis.16 Intriguingly, Cidea is observed to be highly expressed in lactating mammary gland and regulates milk lipid secretion by acting as a potential cofactor of CCAAT/enhancer-binding protein beta.17 Therefore, CIDE proteins are crucial factors to control multiple lipid metabolic pathways and maintain lipid homeostasis. The roles of CIDE proteins in cell death, energy metabolism and metabolic disorders, their transcriptional regulation, and their posttranslational modification have been extensively discussed previously.1,2 We will summarize the roles of CIDE proteins in the regulation of lipid metabolism, focusing on lipid droplet (LD) growth and VLDL lipidation.

CIDE Proteins in Lipid Storage and LD Growth

Despite their diverse tissue expression patterns, deficiencies in all CIDE proteins result in 1 common phenotype: the accumulation of small LDs in the respective cell types.3,4,8,18–21 For example, brown adipocytes with a Cidea deficiency contain significantly smaller LDs.3 In addition, white adipocytes from Fsp27-deficient mice5,6 or from humans with Cidec mutations9 all exhibit the accumulation of smaller LDs. Therefore, CIDE proteins appear to play a unique role in the control of the sizes of cytosolic LDs in various cell types. Interestingly, CIDE proteins are localized to the surface of cytosolic LDs and the endoplasmic reticulum (ER)1,2 where nascent LDs are synthesized. LDs are important subcellular organelles responsible for neutral lipid storage in all cell types. Recently, LDs were shown to regulate viral assembly and intracellular protein and lipid trafficking.22,23 More importantly, white adipocytes contain a giant unilocular LD, and the sizes of LDs in adipocytes reflect the lipid storage capacity and have been linked to the development of obesity and insulin resistance.9,24–26 Genetic screens in Drosophila and yeast cells have uncovered links between factors involved in phospholipid synthesis,27,28 vesicular transport,29,30 and seipin/Fldp28,31,32 and regulation of LD size and morphology. However, the mechanisms of LD growth and the formation of unilocular LDs in adipocytes remain elusive.

Our recent research on the roles of Fsp27 and Cidea in the control of LD growth uncovered a novel molecular mechanism for LD growth and the formation of unilocular LDs in adipocytes.33 We have observed that both Fsp27 and Cidea are enriched at a particular sub-LD location: the LD-LD contact site (LDCS). The enrichment of Fsp27 at LDCSs is a critical first step for Fsp27-mediated LD growth. Interestingly, we observed that once Fsp27 and Cidea are enriched at LDCSs, rapid lipid exchange among contacted LD pairs is detected. In addition, a directional net transfer of neutral lipids from smaller to larger LDs occurs at Fsp27-positive LDCS, resulting in the merging of smaller LDs to form large LDs. The phenomenon of Fsp27 facilitating LD clustering was also observed in another study.34 Intriguingly, Fsp27-mediated directional lipid transfer can be observed in vitro in an autonomous or cytosolic factor-independent manner. In addition, we observed a 50-fold higher lipid exchange activity in differentiated adipocytes than in preadipocytes overexpressing Fsp27, suggesting that additional adipocyte-specific factors are required to accelerate Fsp27-mediated LD growth in adipocytes.33

Fsp27- and Cidea-mediated lipid transfer and LD growth is a unique process that is distinct from other membrane fusion processes, including vesicle fusion,35,36 ER fusion,37,38 and mitochondria fusion.39 Vesicle fusion involves the merging of lipid bilayers, the formation of an interconnected membrane structure and a fusion pore in a short period of time, and the mixing of the internal contents of the 2 vesicles. However, Fsp27- and Cidea-mediated lipid transfer and LD growth require these proteins to first be clustered and enriched at LDCSs. The clustering of Fsp27 and Cidea may provide a tethering force for stable LD attachment. In addition, the clustering of Fsp27 at LDCSs may recruit other proteins that deform the monolayer phospholipids at the LDCS to form a pore or a lipid transfer channel to initiate neutral lipid exchange among LDs that are in contact, resulting in net lipid transfer from smaller to larger LDs due to the difference in internal pressure (Figure). Fsp27-mediated LD growth is a relatively slow process that depends on the size of the LDs that are in contact, whereas vesicle fusion usually proceeds very rapidly, and a size requirement is not observed. Therefore, Fsp27-mediated lipid transfer and LD growth can be defined as a special LD fusion process that involves a localized and defined boundary (LDCS) and the directional transfer of lipids gradually from smaller to larger LDs. Such a slow process is likely favorable in adipocytes because the 1-step mixing of the LD cores of large LDs due to fusion pore expansion may generate mechanical stress in cells. The presence of phospholipid monolayer in LDs may lower the energy barrier for Fsp27-mediated LD growth relative to the energy barriers for other bilayer membrane fusion mechanisms. Further analyses including the complete identification of protein complex that facilitates Fsp27- or Cidea-mediated lipid transfer at the LDCS, structural characterization of Fsp27 and its associated proteins, and in vitro biochemical reconstitution of Fsp27-mediated lipid transfer will be needed to elucidate the molecular basis of CIDE proteins in controlling LD growth in adipocytes.

Figure.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure.

The proposed model of Fsp27-mediated lipid transfer and lipid droplet (LD) growth. When clustering and enriching at the LD contacting site (LDCS), Fsp27 may provide a tethering force for stable LD attachment and recruit unidentified proteins (X, Y, Z) to form a complex at the LDCS. Fsp27-initiated protein complex may deform phospholipid monolayer to generate a pore (or channel-like) structure at the LDCSs, resulting in neutral lipid exchange among contacted LDs and net lipid transfer from smaller to larger LDs due to the internal pressure difference.33

Regulation of LD size and lipid storage by Fsp27 and Cidea may also be mediated by its activity in controlling lipolysis, as Fsp27 and Cidea deficiencies result in an increased lipolysis,3,5,6 whereas overexpression of Cidea and Fsp27 leads to reduced lipolysis.7,8,20,40,41 The mechanism by which CIDE proteins control lipolysis is unclear. Several sequence homologous regions between CIDE proteins and perilipin are identified,2,8,42 raising the possibility that CIDE proteins could play dual roles in lipolysis as perilipin does.43 Alternatively, CIDE proteins may act as physical barriers to protect LDs from lipolysis, similar to that of adipose differentiation–related protein and TIP47 in contributing to LD stabilization.43,44

Interestingly, Cidea and Fsp27 are also reported to be markedly upregulated in the livers of high-fat diet–fed and ob/ob mice. Overexpression of Cidea and Fsp27 in hepatocytes promotes the formation of larger LDs in hepatocytes.10,11,45 In contrast, Cidea and Fsp27 deficiency leads to reduced hepatic triacylglycerol (TAG) levels, the accumulation of smaller sized LDs, and alleviation of ob/ob or high-fat diet-induced hepatic steatosis.10,11,45 Therefore, Cidea and Fsp27 are likely to play similar roles in promoting LD growth in hepatocytes. However, the expressions of Cidea and Fsp27 in hepatocytes are differentially regulated upon fat challenge as Cidea is upregulated in the presence of dietary saturated fatty acids, which is mediated by sterol-regulatory-element-binding protein-1c, whereas Fsp27 gene expression is controlled by peroxisome proliferator–activated receptor-γ pathway.10,11,45 Therefore, these 2 proteins may play different roles at the different stages of LD growth in hepatocytes. In addition, the sizes of LDs in hepatocytes are much smaller than those of adipocytes, possibly due to the lack of some crucial cofactors required to accelerate the activity of Fsp27 and Cidea.

CIDE Proteins in VLDL Lipidation and Maturation in Hepatocytes

The assembly and maturation of VLDL in hepatocytes is generally thought to involve 2 steps.43,46 The first step of VLDL assembly occurs in the ER with the formation of lipid- poor lipoprotein particles (pre-VLDL),46 which is dependent on MTP to transfer locally synthesized TAG to apoB-100.47 Lipid-poor pre-VLDL particles are then further lipidated to generate TAG-rich and mature VLDL particles for secretion.43,48 The subcellular location of VLDL lipidation and maturation, the source of the lipids, and the factors promoting VLDL lipidation remain subjects of intense debate and investigation. Some researchers suggest that the ER may be the site of VLDL lipidation because the majority of TAG is synthesized in the ER, and apoB-100 has been shown to be localized to the ER membrane.49–51 Other researchers have demonstrated that pre-VLDL particles exit the ER and that VLDL lipidation occurs primarily in the Golgi apparatus or post-ER compartments.43,52–54 The factors affecting VLDL assembly and maturation in hepatocytes have recently been reviewed.55

Two types of LDs, cytosolic LDs and ER-lumenal LDs, have been identified using the biochemical method.56–59 Two hypotheses regarding the source of the lipids involved in VLDL lipidation have been proposed. First, TAG is directly transferred through the fusion of ER-lumenal LDs to TAG-poor VLDL particles.51,60 Second, TAG from cytosolic LDs has been reported to be hydrolyzed to yield free fatty acids that are then re-esterified on the lumenal side of secretory apparatuses, such as the Golgi, generating lipid-rich VLDL particles.61 The fusion of ER-lumenal LDs with VLDL particles during VLDL lipidation and maturation is proposed to be mediated by ApoC III.62,63 One remaining question is whether TAG from cytosolic LDs, which are the most abundant source of neutral lipids, can be directly transferred to TAG-poor VLDL particles to form lipid-rich VLDL particles. Many factors, including ADP ribosylation factor 1 (ARF1, a small GTPase involved in vesicular trafficking),64 phospholipase D,64 the phospholipase iPLA2β,65 phosphoinositide-3 kinase,66 and coat protein complex II,53 are involved in VLDL lipidation and secretion. In addition, the synthesis of phosphatidylcholine and phosphatidylethanolamine, and their ratio regulate the VLDL assembly and secretion.67,68

Cideb, a member of the CIDE family of proteins, is expressed at higher levels in the liver and kidney.4 Cideb−/− mice exhibit an increased whole-body metabolic rate and reduced serum TAG levels and are resistant to diet-induced obesity.4 Further analyses reveal that the VLDL particles secreted from Cideb−/− mice or isolated Cideb−/− hepatocytes contain significantly less TAG but have similar levels of apoB-100/-48, indicating an impairment in VLDL lipidation in Cideb-deficient hepatocytes. In addition, Cideb is localized to LDs and the ER and interacts with apoB-100/-48. The interaction between Cideb and apoB-100 is required for VLDL lipidation in hepatocytes.13 Interestingly, the overexpression of Plin2, another LD-associated protein, has also been shown to decrease the production and secretion of lipid-rich VLDL particles and to increase cytosolic TAG accumulation in McA-RH7777 cells.69 In contrast, mice with Plin2 and leptin double deficiency exhibit increased VLDL lipidation,70 suggesting that Plin2 negatively controls VLDL lipidation. Therefore, LD-associated proteins appear to play important roles in controlling VLDL lipidation and maturation. However, the mechanisms of Cideb-mediated VLDL lipidation and maturation remain elusive. Future studies will focus on the following questions: (1) Where does Cideb-mediated VLDL lipidation occur? ER, post-ER compartments, or the Golgi apparatus? (2) Does Cideb-mediated VLDL lipidation require the cooperation of Cideb with other LD- or ER-associated proteins? (3) Does Cideb-mediated VLDL lipidation involve direct neutral lipid transfer from cytosolic (or ER-associated) LDs to TAG-poor VLDL particles? Alternatively, Cideb-mediated VLDL lipidation may require the hydrolysis of TAGs in cytosolic LDs. Genetically modified animal models and a well-established cell model will be good tools to address these questions.71 The function of Cideb in hepatocytes may be dependent on its subcellular localization. When localized to LDs, Cideb mediates lipid transfer and LD growth using similar mechanism to that of Cidea and Fsp27. When in close contact with pre-VLDL particles, Cideb promotes VLDL lipidation and maturation possibly by mediating direct transfer of TAG from cytosolic LDs to pre-VLDL particles or the second step, bulk TAG pool.71

Conclusion

CIDE proteins are important modulators of diverse lipid metabolic pathways, including lipolysis, fatty acid oxidation, VLDL lipidation, and LD growth in adipocytes and hepatocytes. By localizing to LDs and the ER, Cideb controls VLDL lipidation and maturation in hepatocytes. Furthermore, Fsp27 and Cidea are enriched at LDCSs and promote lipid exchange and lipid transfer between LDs that are in contact, resulting in the final growth and enlargement of LDs in adipocytes. However, our understanding of the mechanistic details of CIDE protein functions in controlling lipid metabolism is still in its early stages. Much effort will be needed to determine how CIDE proteins modulate the processes involved in lipid homeostasis, including VLDL lipidation and LD growth in hepatocytes and adipocytes and perhaps in other cells. CIDE proteins may be new drug targets for the treatment of metabolic disorders.

Sources of Funding

The work that formed the basis for opinions expressed in this review was supported by grants from the National Basic Research Program (2011CB910800) and National High Technology Research and Development program (2010AA023002) from the Ministry of Science and Technology of China and National Natural Science Foundation of China (30800555 to L.X. and 31030038 to P.L.). Dr Li is a professor and investigator for Tsinghua-Peking Center for Life Sciences.

Disclosures

None.

  • Received February 1, 2012.
  • Accepted March 12, 2012.
  • © 2012 American Heart Association, Inc.

References

  1. 1.↵
    1. Gong J,
    2. Sun Z,
    3. Li P
    . CIDE proteins and metabolic disorders. Curr Opin Lipidol. 2009;20:121–126.
    OpenUrlCrossRefPubMed
  2. 2.↵
    1. Yonezawa T,
    2. Kurata R,
    3. Kimura M,
    4. Inoko H
    . Which CIDE are you on? Apoptosis and energy metabolism. Mol Biosyst. 2011;7:91–100.
    OpenUrlCrossRefPubMed
  3. 3.↵
    1. Zhou Z,
    2. Yon Toh S,
    3. Chen Z,
    4. Guo K,
    5. Ng CP,
    6. Ponniah S,
    7. Lin SC,
    8. Hong W,
    9. Li P
    . Cidea-deficient mice have lean phenotype and are resistant to obesity. Nat Genet. 2003;35:49–56.
    OpenUrlCrossRefPubMed
  4. 4.↵
    1. Li JZ,
    2. Ye J,
    3. Xue B,
    4. Qi J,
    5. Zhang J,
    6. Zhou Z,
    7. Li Q,
    8. Wen Z,
    9. Li P
    . Cideb regulates diet-induced obesity, liver steatosis, and insulin sensitivity by controlling lipogenesis and fatty acid oxidation. Diabetes. 2007;56:2523–2532.
    OpenUrlAbstract/FREE Full Text
  5. 5.↵
    1. Toh SY,
    2. Gong J,
    3. Du G,
    4. Li JZ,
    5. Yang S,
    6. Ye J,
    7. Yao H,
    8. Zhang Y,
    9. Xue B,
    10. Li Q,
    11. Yang H,
    12. Wen Z,
    13. Li P,
    14. PLoS ONE
    . Up-regulation of mitochondrial activity and acquirement of brown adipose tissue-like property in the white adipose tissue of fsp27 deficient mice. 2008;3:e2890.
  6. 6.↵
    1. Nishino N,
    2. Tamori Y,
    3. Tateya S,
    4. Kawaguchi T,
    5. Shibakusa T,
    6. Mizunoya W,
    7. Inoue K,
    8. Kitazawa R,
    9. Kitazawa S,
    10. Matsuki Y,
    11. Hiramatsu R,
    12. Masubuchi S,
    13. Omachi A,
    14. Kimura K,
    15. Saito M,
    16. Amo T,
    17. Ohta S,
    18. Yamaguchi T,
    19. Osumi T,
    20. Cheng J,
    21. Fujimoto T,
    22. Nakao H,
    23. Nakao K,
    24. Aiba A,
    25. Okamura H,
    26. Fushiki T,
    27. Kasuga M
    . FSP27 contributes to efficient energy storage in murine white adipocytes by promoting the formation of unilocular lipid droplets. J Clin Invest. 2008;118:2808–2821.
    OpenUrlCrossRefPubMed
  7. 7.↵
    1. Nordström EA,
    2. Rydén M,
    3. Backlund EC,
    4. Dahlman I,
    5. Kaaman M,
    6. Blomqvist L,
    7. Cannon B,
    8. Nedergaard J,
    9. Arner P
    . A human-specific role of cell death-inducing DFFA (DNA fragmentation factor-alpha)-like effector A (CIDEA) in adipocyte lipolysis and obesity. Diabetes. 2005;54:1726–1734.
    OpenUrlAbstract/FREE Full Text
  8. 8.↵
    1. Puri V,
    2. Ranjit S,
    3. Konda S,
    4. Nicoloro SM,
    5. Straubhaar J,
    6. Chawla A,
    7. Chouinard M,
    8. Lin C,
    9. Burkart A,
    10. Corvera S,
    11. Perugini RA,
    12. Czech MP,
    13. Sci USA
    . Cidea is associated with lipid droplets and insulin sensitivity in humans. Proc Natl Acad 2008;105:7833–7838.
    OpenUrlAbstract/FREE Full Text
  9. 9.↵
    1. Rubio-Cabezas O,
    2. Puri V,
    3. Murano I,
    4. Saudek V,
    5. Semple RK,
    6. Dash S,
    7. Hyden CS,
    8. Bottomley W,
    9. Vigouroux C,
    10. Magré J,
    11. Raymond-Barker P,
    12. Murgatroyd PR,
    13. Chawla A,
    14. Skepper JN,
    15. Chatterjee VK,
    16. Suliman S,
    17. Patch AM,
    18. Agarwal AK,
    19. Garg A,
    20. Barroso I,
    21. Cinti S,
    22. Czech MP,
    23. Argente J,
    24. O’Rahilly S,
    25. Savage DB
    ; LD Screening Consortium. Partial lipodystrophy and insulin resistant diabetes in a patient with a homozygous nonsense mutation in CIDEC. EMBO Mol Med. 2009;1:280–287.
    OpenUrlAbstract/FREE Full Text
  10. 10.↵
    1. Matsusue K,
    2. Kusakabe T,
    3. Noguchi T,
    4. Takiguchi S,
    5. Suzuki T,
    6. Yamano S,
    7. Gonzalez FJ
    . Hepatic steatosis in leptin-deficient mice is promoted by the PPARgamma target gene Fsp27. Cell Metab. 2008;7:302–311.
    OpenUrlCrossRefPubMed
  11. 11.↵
    1. Zhou L,
    2. Xu L,
    3. Ye J,
    4. Li D,
    5. Wang W,
    6. Li X,
    7. Wu L,
    8. Wang H,
    9. Guan F,
    10. Li P
    . Cidea promotes hepatic steatosis by sensing dietary fatty acids. Hepatology. 2012; doi: 10.1002/hep.25611.
  12. 12.↵
    1. Hall AM,
    2. Brunt EM,
    3. Klein S,
    4. Finck BN
    . Hepatic expression of cell death-inducing DFFA-like effector C in obese subjects is reduced by marked weight loss. Obesity (Silver Spring). 2010;18:417–419.
    OpenUrlCrossRefPubMed
  13. 13.↵
    1. Ye J,
    2. Li JZ,
    3. Liu Y,
    4. Li X,
    5. Yang T,
    6. Ma X,
    7. Li Q,
    8. Yao Z,
    9. Li P
    . Cideb, an ER- and lipid droplet-associated protein, mediates VLDL lipidation and maturation by interacting with apolipoprotein B. Cell Metab. 2009;9:177–190.
    OpenUrlCrossRefPubMed
  14. 14.↵
    1. Chen Z,
    2. Norris JY,
    3. Finck BN
    . Peroxisome proliferator-activated receptor-gamma coactivator-1alpha (PGC-1alpha) stimulates VLDL assembly through activation of cell death-inducing DFFA-like effector B (CideB). J Biol Chem. 2010;285:25996–26004.
    OpenUrlAbstract/FREE Full Text
  15. 15.↵
    1. Li JZ,
    2. Lei Y,
    3. Wang Y,
    4. Zhang Y,
    5. Ye J,
    6. Xia X,
    7. Pan X,
    8. Li P
    . Control of cholesterol biosynthesis, uptake and storage in hepatocytes by Cideb. Biochim Biophys Acta. 2010;1801:577–586.
    OpenUrlPubMed
  16. 16.↵
    1. Li H,
    2. Song Y,
    3. Li F,
    4. Zhang L,
    5. Gu Y,
    6. Zhang L,
    7. Jiang L,
    8. Dong W,
    9. Ye J,
    10. Li Q
    . Identification of lipid droplet-associated proteins in the formation of macrophage-derived foam cells using microarrays. Int J Mol Med. 2010;26:231–239.
    OpenUrlPubMed
  17. 17.↵
    1. Wang W,
    2. Lv N,
    3. Zhang S,
    4. Shui G,
    5. Qian H,
    6. Zhang J,
    7. Chen Y,
    8. Ye J,
    9. Xie Y,
    10. Shen Y,
    11. Wenk MR,
    12. Li P
    . Cidea is an essential transcriptional coactivator regulating mammary gland secretion of milk lipids. Nat Med. 2012;18:235–243.
    OpenUrlCrossRefPubMed
  18. 18.↵
    1. Keller P,
    2. Petrie JT,
    3. De Rose P,
    4. Gerin I,
    5. Wright WS,
    6. Chiang SH,
    7. Nielsen AR,
    8. Fischer CP,
    9. Pedersen BK,
    10. MacDougald OA
    . Fat-specific protein 27 regulates storage of triacylglycerol. J Biol Chem. 2008;283: 14355–14365.
    OpenUrlAbstract/FREE Full Text
  19. 19.↵
    1. Liu K,
    2. Zhou S,
    3. Kim JY,
    4. Tillison K,
    5. Majors D,
    6. Rearick D,
    7. Lee JH,
    8. Fernandez-Boyanapalli RF,
    9. Barricklow K,
    10. Houston MS,
    11. Smas CM
    . Functional analysis of FSP27 protein regions for lipid droplet localization, caspase-dependent apoptosis, and dimerization with CIDEA. Am J Physiol Endocrinol Metab. 2009;297:E1395–E1413.
    OpenUrlAbstract/FREE Full Text
  20. 20.↵
    1. Puri V,
    2. Konda S,
    3. Ranjit S,
    4. Aouadi M,
    5. Chawla A,
    6. Chouinard M,
    7. Chakladar A,
    8. Czech MP
    . Fat-specific protein 27, a novel lipid droplet protein that enhances triglyceride storage. J Biol Chem. 2007;282:34213–34218.
    OpenUrlAbstract/FREE Full Text
  21. 21.↵
    1. Li D,
    2. Zhang Y,
    3. Xu L,
    4. Zhou L,
    5. Wang Y,
    6. Xue B,
    7. Wen Z,
    8. Li P,
    9. Sang J
    . Regulation of gene expression by FSP27 in white and brown adipose tissue. BMC Genomics. 2010;11:446.
    OpenUrlCrossRefPubMed
  22. 22.↵
    1. Miyanari Y,
    2. Atsuzawa K,
    3. Usuda N,
    4. Watashi K,
    5. Hishiki T,
    6. Zayas M,
    7. Bartenschlager R,
    8. Wakita T,
    9. Hijikata M,
    10. Shimotohno K
    . The lipid droplet is an important organelle for hepatitis C virus production. Nat Cell Biol. 2007;9:1089–1097.
    OpenUrlCrossRefPubMed
  23. 23.↵
    1. Fukasawa M
    . Cellular lipid droplets and hepatitis C virus life cycle. Biol Pharm Bull. 2010;33:355–359.
    OpenUrlCrossRefPubMed
  24. 24.↵
    1. Bell M,
    2. Wang H,
    3. Chen H,
    4. McLenithan JC,
    5. Gong DW,
    6. Yang RZ,
    7. Yu D,
    8. Fried SK,
    9. Quon MJ,
    10. Londos C,
    11. Sztalryd C
    . Consequences of lipid droplet coat protein downregulation in liver cells: abnormal lipid droplet metabolism and induction of insulin resistance. Diabetes. 2008;57:2037–2045.
    OpenUrlAbstract/FREE Full Text
  25. 25.↵
    1. Meex RC,
    2. Schrauwen P,
    3. Hesselink MK
    . Modulation of myocellular fat stores: lipid droplet dynamics in health and disease. Am J Physiol Regul Integr Comp Physiol. 2009;297:R913–R924.
    OpenUrlAbstract/FREE Full Text
  26. 26.↵
    1. Lungu AO,
    2. Zadeh ES,
    3. Goodling A,
    4. Cochran E,
    5. Gorden P
    . Insulin resistance is a sufficient basis for hyperandrogenism in lipodystrophic women with polycystic ovarian syndrome. J Clin Endocrinol Metab. 2012;97:563–567.
    OpenUrlCrossRefPubMed
  27. 27.↵
    1. Krahmer N,
    2. Guo Y,
    3. Wilfling F,
    4. Hilger M,
    5. Lingrell S,
    6. Heger K,
    7. Newman HW,
    8. Schmidt-Supprian M,
    9. Vance DE,
    10. Mann M,
    11. Farese RV Jr.,
    12. Walther TC
    . Phosphatidylcholine synthesis for lipid droplet expansion is mediated by localized activation of CTP:phosphocholine cytidylyltransferase. Cell Metab. 2011;14:504–515.
    OpenUrlCrossRefPubMed
  28. 28.↵
    1. Fei W,
    2. Shui G,
    3. Zhang Y,
    4. Krahmer N,
    5. Ferguson C,
    6. Kapterian TS,
    7. Lin RC,
    8. Dawes IW,
    9. Brown AJ,
    10. Li P,
    11. Huang X,
    12. Parton RG,
    13. Wenk MR,
    14. Walther TC,
    15. Yang H
    . A role for phosphatidic acid in the formation of “supersized” lipid droplets. PLoS Genet. 2011;7:e1002201.
    OpenUrlCrossRefPubMed
  29. 29.↵
    1. Beller M,
    2. Sztalryd C,
    3. Southall N,
    4. Bell M,
    5. Jäckle H,
    6. Auld DS,
    7. Oliver B
    . COPI complex is a regulator of lipid homeostasis. PLoS Biol. 2008;6:e292.
    OpenUrlCrossRefPubMed
  30. 30.↵
    1. Guo Y,
    2. Walther TC,
    3. Rao M,
    4. Stuurman N,
    5. Goshima G,
    6. Terayama K,
    7. Wong JS,
    8. Vale RD,
    9. Walter P,
    10. Farese RV
    . Functional genomic screen reveals genes involved in lipid-droplet formation and utilization. Nature. 2008;453:657–661.
    OpenUrlCrossRefPubMed
  31. 31.↵
    1. Fei W,
    2. Shui G,
    3. Gaeta B,
    4. Du X,
    5. Kuerschner L,
    6. Li P,
    7. Brown AJ,
    8. Wenk MR,
    9. Parton RG,
    10. Yang H
    . Fld1p, a functional homologue of human seipin, regulates the size of lipid droplets in yeast. J Cell Biol. 2008;180:473–482.
    OpenUrlAbstract/FREE Full Text
  32. 32.↵
    1. Szymanski KM,
    2. Binns D,
    3. Bartz R,
    4. Grishin NV,
    5. Li WP,
    6. Agarwal AK,
    7. Garg A,
    8. Anderson RG,
    9. Goodman JM
    . The lipodystrophy protein seipin is found at endoplasmic reticulum lipid droplet junctions and is important for droplet morphology. Proc Natl Acad Sci USA. 2007;104: 20890–20895.
    OpenUrlAbstract/FREE Full Text
  33. 33.↵
    1. Gong J,
    2. Sun Z,
    3. Wu L,
    4. Xu W,
    5. Schieber N,
    6. Xu D,
    7. Shui G,
    8. Yang H,
    9. Parton RG,
    10. Li P
    . Fsp27 promotes lipid droplet growth by lipid exchange and transfer at lipid droplet contact sites. J Cell Biol. 2011;195:953–963.
    OpenUrlAbstract/FREE Full Text
  34. 34.↵
    1. Jambunathan S,
    2. Yin J,
    3. Khan W,
    4. Tamori Y,
    5. Puri V
    . FSP27 promotes lipid droplet clustering and then fusion to regulate triglyceride accumulation. PLoS ONE. 2011;6:e28614.
    OpenUrlCrossRefPubMed
  35. 35.↵
    1. Rizo J,
    2. Rosenmund C
    . Synaptic vesicle fusion. Nat Struct Mol Biol. 2008;15:665–674.
    OpenUrlCrossRefPubMed
  36. 36.↵
    1. Wickner W,
    2. Schekman R
    . Membrane fusion. Nat Struct Mol Biol. 2008;15:658–664.
    OpenUrlCrossRefPubMed
  37. 37.↵
    1. Hu J,
    2. Shibata Y,
    3. Zhu PP,
    4. Voss C,
    5. Rismanchi N,
    6. Prinz WA,
    7. Rapoport TA,
    8. Blackstone C
    . A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell. 2009;138:549–561.
    OpenUrlCrossRefPubMed
  38. 38.↵
    1. Orso G,
    2. Pendin D,
    3. Liu S,
    4. Tosetto J,
    5. Moss TJ,
    6. Faust JE,
    7. Micaroni M,
    8. Egorova A,
    9. Martinuzzi A,
    10. McNew JA,
    11. Daga A
    . Homotypic fusion of ER membranes requires the dynamin-like GTPase atlastin. Nature. 2009;460:978–983.
    OpenUrlCrossRefPubMed
  39. 39.↵
    1. Chan DC
    . Mitochondria: dynamic organelles in disease, aging, and development. Cell. 2006;125:1241–1252.
    OpenUrlCrossRefPubMed
  40. 40.↵
    1. Christianson JL,
    2. Boutet E,
    3. Puri V,
    4. Chawla A,
    5. Czech MP
    . Identification of the lipid droplet targeting domain of the Cidea protein. J Lipid Res. 2010;51:3455–3462.
    OpenUrlAbstract/FREE Full Text
  41. 41.↵
    1. Ranjit S,
    2. Boutet E,
    3. Gandhi P,
    4. Prot M,
    5. Tamori Y,
    6. Chawla A,
    7. Greenberg AS,
    8. Puri V,
    9. Czech MP
    . Regulation of fat specific protein 27 by isoproterenol and TNF-a to control lipolysis in murine adipocytes. J Lipid Res. 2011;52:221–236.
    OpenUrlAbstract/FREE Full Text
  42. 42.↵
    1. Miyoshi H,
    2. Perfield JW 2nd.,
    3. Souza SC,
    4. Shen WJ,
    5. Zhang HH,
    6. Stancheva ZS,
    7. Kraemer FB,
    8. Obin MS,
    9. Greenberg AS
    . Control of adipose triglyceride lipase action by serine 517 of perilipin A globally regulates protein kinase A-stimulated lipolysis in adipocytes. J Biol Chem. 2007;282: 996–1002.
    OpenUrlAbstract/FREE Full Text
  43. 43.↵
    1. Olofsson SO,
    2. Boström P,
    3. Andersson L,
    4. Rutberg M,
    5. Perman J,
    6. Borén J
    . Lipid droplets as dynamic organelles connecting storage and efflux of lipids. Biochim Biophys Acta. 2009;1791:448–458.
    OpenUrlCrossRefPubMed
  44. 44.↵
    1. Brasaemle DL
    . Thematic review series: adipocyte biology. The perilipin family of structural lipid droplet proteins: stabilization of lipid droplets and control of lipolysis. J Lipid Res. 2007;48:2547–2559.
    OpenUrlAbstract/FREE Full Text
  45. 45.↵
    1. Wang R,
    2. Kong X,
    3. Cui A,
    4. Liu X,
    5. Xiang R,
    6. Yang Y,
    7. Guan Y,
    8. Fang F,
    9. Chang Y,
    10. Biochem J
    . Sterol-regulatory-element-binding protein 1c mediates the effect of insulin on the expression of Cidea in mouse hepatocytes. 2010;430:245–254.
  46. 46.↵
    1. Rustaeus S,
    2. Lindberg K,
    3. Stillemark P,
    4. Claesson C,
    5. Asp L,
    6. Larsson T,
    7. Borén J,
    8. Olofsson SO
    . Assembly of very low density lipoprotein: a two-step process of apolipoprotein B core lipidation. J Nutr. 1999;129(2S Suppl):463S–466S.
    OpenUrlPubMed
  47. 47.↵
    1. Gordon DA,
    2. Jamil H
    . Progress towards understanding the role of microsomal triglyceride transfer protein in apolipoprotein-B lipoprotein assembly. Biochim Biophys Acta. 2000;1486:72–83.
    OpenUrlPubMed
  48. 48.↵
    1. Rutledge AC,
    2. Su Q,
    3. Adeli K
    . Apolipoprotein B100 biogenesis: a complex array of intracellular mechanisms regulating folding, stability, and lipoprotein assembly. Biochem Cell Biol. 2010;88:251–267.
    OpenUrlCrossRefPubMed
  49. 49.↵
    1. Yamaguchi J,
    2. Gamble MV,
    3. Conlon D,
    4. Liang JS,
    5. Ginsberg HN
    . The conversion of apoB100 low density lipoprotein/high density lipoprotein particles to apoB100 very low density lipoproteins in response to oleic acid occurs in the endoplasmic reticulum and not in the Golgi in McA RH7777 cells. J Biol Chem. 2003;278:42643–42651.
    OpenUrlAbstract/FREE Full Text
  50. 50.↵
    1. Gibbons GF,
    2. Wiggins D,
    3. Brown AM,
    4. Hebbachi AM
    . Synthesis and function of hepatic very-low-density lipoprotein. Biochem Soc Trans. 2004;32(Pt 1):59–64.
    OpenUrlCrossRefPubMed
  51. 51.↵
    1. Fisher EA,
    2. Ginsberg HN
    . Complexity in the secretory pathway: the assembly and secretion of apolipoprotein B-containing lipoproteins. J Biol Chem. 2002;277:17377–17380.
    OpenUrlFREE Full Text
  52. 52.↵
    1. Blasiole DA,
    2. Oler AT,
    3. Attie AD
    . Regulation of ApoB secretion by the low density lipoprotein receptor requires exit from the endoplasmic reticulum and interaction with ApoE or ApoB. J Biol Chem. 2008;283:11374–11381.
    OpenUrlAbstract/FREE Full Text
  53. 53.↵
    1. Gusarova V,
    2. Brodsky JL,
    3. Fisher EA
    . Apolipoprotein B100 exit from the endoplasmic reticulum (ER) is COPII-dependent, and its lipidation to very low density lipoprotein occurs post-ER. J Biol Chem. 2003;278:48051–48058.
    OpenUrlAbstract/FREE Full Text
  54. 54.↵
    1. Stillemark P,
    2. Borén J,
    3. Andersson M,
    4. Larsson T,
    5. Rustaeus S,
    6. Karlsson KA,
    7. Olofsson SO
    . The assembly and secretion of apolipoprotein B-48-containing very low density lipoproteins in McA-RH7777 cells. J Biol Chem. 2000;275:10506–10513.
    OpenUrlAbstract/FREE Full Text
  55. 55.↵
    1. Sundaram M,
    2. Yao Z
    . Recent progress in understanding protein and lipid factors affecting hepatic VLDL assembly and secretion. Nutr Metab (Lond). 2010;7:35.
    OpenUrlCrossRefPubMed
  56. 56.↵
    1. Boström P,
    2. Andersson L,
    3. Rutberg M,
    4. Perman J,
    5. Lidberg U,
    6. Johansson BR,
    7. Fernandez-Rodriguez J,
    8. Ericson J,
    9. Nilsson T,
    10. Borén J,
    11. Olofsson SO
    . SNARE proteins mediate fusion between cytosolic lipid droplets and are implicated in insulin sensitivity. Nat Cell Biol. 2007;9:1286–1293.
    OpenUrlCrossRefPubMed
  57. 57.↵
    1. Marchesan D,
    2. Rutberg M,
    3. Andersson L,
    4. Asp L,
    5. Larsson T,
    6. Borén J,
    7. Johansson BR,
    8. Olofsson SO
    . A phospholipase D-dependent process forms lipid droplets containing caveolin, adipocyte differentiation-related protein, and vimentin in a cell-free system. J Biol Chem. 2003;278: 27293–27300.
    OpenUrlAbstract/FREE Full Text
  58. 58.↵
    1. Cermelli S,
    2. Guo Y,
    3. Gross SP,
    4. Welte MA
    . The lipid-droplet proteome reveals that droplets are a protein-storage depot. Curr Biol. 2006;16:1783–1795.
    OpenUrlCrossRefPubMed
  59. 59.↵
    1. Wang H,
    2. Gilham D,
    3. Lehner R
    . Proteomic and lipid characterization of apolipoprotein B-free luminal lipid droplets from mouse liver microsomes: implications for very low density lipoprotein assembly. J Biol Chem. 2007;282:33218–33226.
    OpenUrlAbstract/FREE Full Text
  60. 60.↵
    1. Pan M,
    2. Liang Js JS,
    3. Fisher EA,
    4. Ginsberg HN
    . The late addition of core lipids to nascent apolipoprotein B100, resulting in the assembly and secretion of triglyceride-rich lipoproteins, is independent of both microsomal triglyceride transfer protein activity and new triglyceride synthesis. J Biol Chem. 2002;277:4413–4421.
    OpenUrlAbstract/FREE Full Text
  61. 61.↵
    1. Gibbons GF,
    2. Wiggins D
    . Intracellular triacylglycerol lipase: its role in the assembly of hepatic very-low-density lipoprotein (VLDL). Adv Enzyme Regul. 1995;35:179–198.
    OpenUrlCrossRefPubMed
  62. 62.↵
    1. Qin W,
    2. Sundaram M,
    3. Wang Y,
    4. Zhou H,
    5. Zhong S,
    6. Chang CC,
    7. Manhas S,
    8. Yao EF,
    9. Parks RJ,
    10. McFie PJ,
    11. Stone SJ,
    12. Jiang ZG,
    13. Wang C,
    14. Figeys D,
    15. Jia W,
    16. Yao Z
    . Missense mutation in APOC3 within the C-terminal lipid binding domain of human ApoC-III results in impaired assembly and secretion of triacylglycerol-rich very low density lipoproteins: evidence that ApoC-III plays a major role in the formation of lipid precursors within the microsomal lumen. J Biol Chem. 2011;286:27769–27780.
    OpenUrlAbstract/FREE Full Text
  63. 63.↵
    1. Sundaram M,
    2. Zhong S,
    3. Bou Khalil M,
    4. Links PH,
    5. Zhao Y,
    6. Iqbal J,
    7. Hussain MM,
    8. Parks RJ,
    9. Wang Y,
    10. Yao Z
    . Expression of apolipoprotein C-III in McA-RH7777 cells enhances VLDL assembly and secretion under lipid-rich conditions. J Lipid Res. 2010;51:150–161.
    OpenUrlAbstract/FREE Full Text
  64. 64.↵
    1. Asp L,
    2. Claesson C,
    3. Boren J,
    4. Olofsson SO
    . ADP-ribosylation factor 1 and its activation of phospholipase D are important for the assembly of very low density lipoproteins. J Biol Chem. 2000;275:26285–26292.
    OpenUrlAbstract/FREE Full Text
  65. 65.↵
    1. Tran K,
    2. Wang Y,
    3. DeLong CJ,
    4. Cui Z,
    5. Yao Z
    . The assembly of very low density lipoproteins in rat hepatoma McA-RH7777 cells is inhibited by phospholipase A2 antagonists. J Biol Chem. 2000;275:25023–25030.
    OpenUrlAbstract/FREE Full Text
  66. 66.↵
    1. Brown AM,
    2. Gibbons GF
    . Insulin inhibits the maturation phase of VLDL assembly via a phosphoinositide 3-kinase-mediated event. Arterioscler Thromb Vasc Biol. 2001;21:1656–1661.
    OpenUrlAbstract/FREE Full Text
  67. 67.↵
    1. Jacobs RL,
    2. Devlin C,
    3. Tabas I,
    4. Vance DE
    . Targeted deletion of hepatic CTP:phosphocholine cytidylyltransferase alpha in mice decreases plasma high density and very low density lipoproteins. J Biol Chem. 2004;279:47402–47410.
    OpenUrlAbstract/FREE Full Text
  68. 68.↵
    1. Li Z,
    2. Agellon LB,
    3. Allen TM,
    4. Umeda M,
    5. Jewell L,
    6. Mason A,
    7. Vance DE
    . The ratio of phosphatidylcholine to phosphatidylethanolamine influences membrane integrity and steatohepatitis. Cell Metab. 2006;3:321–331.
    OpenUrlCrossRefPubMed
  69. 69.↵
    1. Magnusson B,
    2. Asp L,
    3. Boström P,
    4. Ruiz M,
    5. Stillemark-Billton P,
    6. Lindén D,
    7. Borén J,
    8. Olofsson SO
    . Adipocyte differentiation-related protein promotes fatty acid storage in cytosolic triglycerides and inhibits secretion of very low-density lipoproteins. Arterioscler Thromb Vasc Biol. 2006;26:1566–1571.
    OpenUrlAbstract/FREE Full Text
  70. 70.↵
    1. Chang BH,
    2. Li L,
    3. Saha P,
    4. Chan L
    . Absence of adipose differentiation related protein upregulates hepatic VLDL secretion, relieves hepatosteatosis, and improves whole body insulin resistance in leptin-deficient mice. J Lipid Res. 2010;51:2132–2142.
    OpenUrlAbstract/FREE Full Text
  71. 71.↵
    1. Wang Y,
    2. Tran K,
    3. Yao Z
    . The activity of microsomal triglyceride transfer protein is essential for accumulation of triglyceride within microsomes in McA-RH7777 cells. A unified model for the assembly of very low density lipoproteins. J Biol Chem. 1999;274:27793–27800.
    OpenUrlAbstract/FREE Full Text
View Abstract
Back to top
Previous ArticleNext Article

This Issue

Arteriosclerosis, Thrombosis, and Vascular Biology
May 2012, Volume 32, Issue 5
  • Table of Contents
Previous ArticleNext Article

Jump to

  • Article
    • Abstract
    • Introduction
    • CIDE Proteins in Lipid Storage and LD Growth
    • CIDE Proteins in VLDL Lipidation and Maturation in Hepatocytes
    • Conclusion
    • Sources of Funding
    • Disclosures
    • References
  • Figures & Tables
  • Info & Metrics
  • eLetters

Article Tools

  • Print
  • Citation Tools
    CIDE Proteins and Lipid Metabolism
    Li Xu, Linkang Zhou and Peng Li
    Arteriosclerosis, Thrombosis, and Vascular Biology. 2012;32:1094-1098, originally published April 18, 2012
    https://doi.org/10.1161/ATVBAHA.111.241489

    Citation Manager Formats

    • BibTeX
    • Bookends
    • EasyBib
    • EndNote (tagged)
    • EndNote 8 (xml)
    • Medlars
    • Mendeley
    • Papers
    • RefWorks Tagged
    • Ref Manager
    • RIS
    • Zotero
  •  Download Powerpoint
  • Article Alerts
    Log in to Email Alerts with your email address.
  • Save to my folders

Share this Article

  • Email

    Thank you for your interest in spreading the word on Arteriosclerosis, Thrombosis, and Vascular Biology.

    NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

    Enter multiple addresses on separate lines or separate them with commas.
    CIDE Proteins and Lipid Metabolism
    (Your Name) has sent you a message from Arteriosclerosis, Thrombosis, and Vascular Biology
    (Your Name) thought you would like to see the Arteriosclerosis, Thrombosis, and Vascular Biology web site.
  • Share on Social Media
    CIDE Proteins and Lipid Metabolism
    Li Xu, Linkang Zhou and Peng Li
    Arteriosclerosis, Thrombosis, and Vascular Biology. 2012;32:1094-1098, originally published April 18, 2012
    https://doi.org/10.1161/ATVBAHA.111.241489
    del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo

Related Articles

Cited By...

Subjects

  • Epidemiology, Lifestyle, and Prevention
    • Obesity
  • Basic, Translational, and Clinical Research
    • Lipids and Cholesterol
    • Cell Signaling/Signal Transduction

Arteriosclerosis, Thrombosis, and Vascular Biology

  • About ATVB
  • Instructions for Authors
  • AHA CME
  • Meeting Abstracts
  • Permissions
  • Email Alerts
  • Open Access Information
  • AHA Journals RSS
  • AHA Newsroom

Contact the Editorial Office:
email: atvb@atvb.org

Information for:
  • Advertisers
  • Subscribers
  • Subscriber Help
  • Institutions / Librarians
  • Institutional Subscriptions FAQ
  • International Users
American Heart Association Learn and Live
National Center
7272 Greenville Ave.
Dallas, TX 75231

Customer Service

  • 1-800-AHA-USA-1
  • 1-800-242-8721
  • Local Info
  • Contact Us

About Us

Our mission is to build healthier lives, free of cardiovascular diseases and stroke. That single purpose drives all we do. The need for our work is beyond question. Find Out More about the American Heart Association

  • Careers
  • SHOP
  • Latest Heart and Stroke News
  • AHA/ASA Media Newsroom

Our Sites

  • American Heart Association
  • American Stroke Association
  • For Professionals
  • More Sites

Take Action

  • Advocate
  • Donate
  • Planned Giving
  • Volunteer

Online Communities

  • AFib Support
  • Garden Community
  • Patient Support Network
  • Professional Online Network

Follow Us:

  • Follow Circulation on Twitter
  • Visit Circulation on Facebook
  • Follow Circulation on Google Plus
  • Follow Circulation on Instagram
  • Follow Circulation on Pinterest
  • Follow Circulation on YouTube
  • Rss Feeds
  • Privacy Policy
  • Copyright
  • Ethics Policy
  • Conflict of Interest Policy
  • Linking Policy
  • Diversity
  • Careers

©2018 American Heart Association, Inc. All rights reserved. Unauthorized use prohibited. The American Heart Association is a qualified 501(c)(3) tax-exempt organization.
*Red Dress™ DHHS, Go Red™ AHA; National Wear Red Day ® is a registered trademark.

  • PUTTING PATIENTS FIRST National Health Council Standards of Excellence Certification Program
  • BBB Accredited Charity
  • Comodo Secured