Emergence of Lipid Droplets in the Mechanisms of Carcinogenesis and Therapeutic Responses

Cancer shares common risk factors with cardiovascular diseases such as dyslipidemia, obesity and inflammation. In both cases, dysregulations of lipid metabolism occur, and lipid vesicles emerge as important factors that can influence carcinogenesis. In this review, the role of different lipids known to be involved in cancer and its response to treatments is detailed. In particular, lipid droplets (LDs), initially described for their role in lipid storage, exert multiple functions, from the physiological prevention of LD coalescence and regulation of endoplasmic reticulum homeostasis to pathological involvement in tumor progression and aggressiveness. Analysis of LDs highlights the importance of phosphatidylcholine metabolism and the diversity of lipid synthesis enzymes. In many cancers, the phosphatidylcholine pathways are disrupted, modifying the expression of genes coding for metabolic enzymes. Tumor microenvironment conditions, such as hypoxia, different types of stress or inflammatory conditions, are also important determinants of LD behavior in cancer cells. Therefore, LDs represent therapeutic targets in cancer, and many lipid mediators have emerged as potential biomarkers for cancer onset, progression, and/or resistance.

[1]  M. Mahlapuu,et al.  Silencing of STE20-type kinase TAOK1 confers protection against hepatocellular lipotoxicity through metabolic rewiring , 2023, Hepatology communications.

[2]  K. Kharbanda,et al.  Lipidomic Analysis of Liver Lipid Droplets after Chronic Alcohol Consumption with and without Betaine Supplementation , 2023, Biology.

[3]  Cho-Rok Jung,et al.  GPX8 regulates clear cell renal cell carcinoma tumorigenesis through promoting lipogenesis by NNMT , 2023, Journal of Experimental & Clinical Cancer Research.

[4]  Lixing Jin,et al.  HIF2α‐induced upregulation of RNASET2 promotes triglyceride synthesis and enhances cell migration in clear cell renal cell carcinoma , 2023, FEBS open bio.

[5]  Jian-xing Ma,et al.  PNPLA2 mobilizes retinyl esters from retinosomes and promotes the generation of 11-cis-retinal in the visual cycle , 2023, Cell reports.

[6]  Daniel F Tardiff,et al.  Targeting de novo lipid synthesis induces lipotoxicity and impairs DNA damage repair in glioblastoma mouse models , 2023, Science Translational Medicine.

[7]  E. Gontier,et al.  Rewiring Lipid Metabolism by Targeting PCSK9 and HMGCR to Treat Liver Cancer , 2022, Cancers.

[8]  Huarong Zhang,et al.  Inhibition of integrated stress response protects against lipid-induced senescence in hypothalamic neural stem cells in adamantinomatous craniopharyngioma. , 2022, Neuro-oncology.

[9]  Yukio Fujiwara,et al.  Cholesterol metabolism and lipid droplet vacuoles; a potential target for the therapy of aggressive lymphoma , 2022, Journal of clinical and experimental hematopathology : JCEH.

[10]  Shuijun Zhang,et al.  AKR1C3-dependent lipid droplet formation confers hepatocellular carcinoma cell adaptability to targeted therapy , 2022, Theranostics.

[11]  Guan-Jhong Huang,et al.  Alpinumisoflavone Exhibits the Therapeutic Effect on Prostate Cancer Cells by Repressing AR and Co-Targeting FASN- and HMGCR-Mediated Lipid and Cholesterol Biosynthesis , 2022, Life.

[12]  B. Su,et al.  LPCAT1 acts as an independent prognostic biomarker correlated with immune infiltration in hepatocellular carcinoma , 2022, European Journal of Medical Research.

[13]  Hongjuan Zhao,et al.  ACSL3 regulates lipid droplet biogenesis and ferroptosis sensitivity in clear cell renal cell carcinoma , 2022, Cancer & Metabolism.

[14]  E. Bonora,et al.  Spartin: At the crossroad between ubiquitination and metabolism in cancer. , 2022, Biochimica et biophysica acta. Reviews on cancer.

[15]  K. Macleod,et al.  Lipid droplet turnover at the lysosome inhibits growth of hepatocellular carcinoma in a BNIP3-dependent manner , 2022, Science advances.

[16]  X. Ruan,et al.  HIF-2α-induced upregulation of CD36 promotes the development of ccRCC. , 2022, Experimental cell research.

[17]  P. Madureira,et al.  Androgens and low density lipoprotein-cholesterol interplay in modulating prostate cancer cell fate and metabolism. , 2022, Pathology, research and practice.

[18]  S. Causse,et al.  Downregulation of Elovl5 promotes breast cancer metastasis through a lipid-droplet accumulation-mediated induction of TGF-β receptors , 2022, Cell Death & Disease.

[19]  Qiang Wei,et al.  Histone methyltransferase KMT2D mediated lipid metabolism via peroxisome proliferator-activated receptor gamma in prostate cancer , 2022, Translational cancer research.

[20]  H. Negoro,et al.  ELOVL5‐mediated fatty acid elongation promotes cellular proliferation and invasion in renal cell carcinoma , 2022, Cancer science.

[21]  J. Brugarolas,et al.  An oncogenic JMJD6-DGAT1 axis tunes the epigenetic regulation of lipid droplet formation in clear cell renal cell carcinoma. , 2022, Molecular cell.

[22]  V. Bonifácio,et al.  Lipid Droplets in Cancer: From Composition and Role to Imaging and Therapeutics , 2022, Molecules.

[23]  Guangji Wang,et al.  Novel Strategy of Proxalutamide for the Treatment of Prostate Cancer through Coordinated Blockade of Lipogenesis and Androgen Receptor Axis , 2021, International journal of molecular sciences.

[24]  M. Lei,et al.  The structural basis for the phospholipid remodeling by lysophosphatidylcholine acyltransferase 3 , 2021, Nature Communications.

[25]  M. Spadea,et al.  Lipid Droplet Biosynthesis Impairment through DGAT2 Inhibition Sensitizes MCF7 Breast Cancer Cells to Radiation , 2021, International journal of molecular sciences.

[26]  Guillermo Bordanaba-Florit,et al.  Using single-vesicle technologies to unravel the heterogeneity of extracellular vesicles , 2021, Nature Protocols.

[27]  Jiangli Fan,et al.  A Novel Photosensitizer for Lipid Droplet–Location Photodynamic Therapy , 2021, Frontiers in Chemistry.

[28]  Fake Lu,et al.  Assessing fatty acid-induced lipotoxicity and its therapeutic potential in glioblastoma using stimulated Raman microscopy , 2021, Scientific Reports.

[29]  J. Kulbacka,et al.  Lipid composition of the cancer cell membrane , 2020, Journal of Bioenergetics and Biomembranes.

[30]  Xianlin Han,et al.  Targeting DGAT1 Ameliorates Glioblastoma by Increasing Fat Catabolism and Oxidative Stress. , 2020, Cell metabolism.

[31]  Meilin Liu,et al.  Recent Advances in Activatable Organic Photosensitizers for Specific Photodynamic Therapy. , 2020, ChemPlusChem.

[32]  K. Hoehn,et al.  CDP-DAG synthase 1 and 2 regulate lipid droplet growth through distinct mechanisms , 2019, The Journal of Biological Chemistry.

[33]  G. Sauter,et al.  Up-regulation of lysophosphatidylcholine acyltransferase 1 (LPCAT1) is linked to poor prognosis in breast cancer , 2019, Aging.

[34]  Jinpu Yang,et al.  CCT α is a novel biomarker for diagnosis of laryngeal squamous cell cancer , 2019, Scientific Reports.

[35]  Shujiro Okuda,et al.  Autophagy regulates lipid metabolism through selective turnover of NCoR1 , 2019, Nature Communications.

[36]  Aaron M. Streets,et al.  Quantitative imaging of lipid droplets in single cells. , 2019, The Analyst.

[37]  Jing Xu,et al.  Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines , 2018, Journal of Extracellular Vesicles.

[38]  Hao Zhang,et al.  Methylation-induced silencing of SPG20 facilitates gastric cancer cell proliferation by activating the EGFR/MAPK pathway. , 2018, Biochemical and biophysical research communications.

[39]  F. Ghiringhelli,et al.  LPCAT2 controls chemoresistance in colorectal cancer , 2018, Molecular & cellular oncology.

[40]  F. Ghiringhelli,et al.  Lysophosphatidylcholine acyltransferase 2-mediated lipid droplet production supports colorectal cancer chemoresistance , 2018, Nature Communications.

[41]  Graça Raposo,et al.  Shedding light on the cell biology of extracellular vesicles , 2018, Nature Reviews Molecular Cell Biology.

[42]  J. Klein-Seetharaman,et al.  Lipid bodies containing oxidatively truncated lipids block antigen cross-presentation by dendritic cells in cancer , 2017, Nature Communications.

[43]  S. Welford,et al.  HIF drives lipid deposition and cancer in ccRCC via repression of fatty acid metabolism , 2017, Nature Communications.

[44]  M. Kwiatkowski,et al.  Lipid Droplet Isolation for Quantitative Mass Spectrometry Analysis. , 2017, Journal of visualized experiments : JoVE.

[45]  Z. Bhujwalla,et al.  Targeting Phospholipid Metabolism in Cancer , 2016, Front. Oncol..

[46]  R. Cerione,et al.  Microvesicle Cargo and Function Changes upon Induction of Cellular Transformation* , 2016, The Journal of Biological Chemistry.

[47]  A. Yoshizawa,et al.  Lipid-rich carcinoma of the breast that is strongly positive for estrogen receptor: a case report and literature review , 2016, OncoTargets and therapy.

[48]  Henrik J Johansson,et al.  Cells release subpopulations of exosomes with distinct molecular and biological properties , 2016, Scientific Reports.

[49]  S. Savkovic,et al.  Epidermal growth factor receptor mediated proliferation depends on increased lipid droplet density regulated via a negative regulatory loop with FOXO3/Sirtuin6. , 2016 .

[50]  D. Savage,et al.  Lipid droplet-organelle interactions: emerging roles in lipid metabolism. , 2015, Current opinion in cell biology.

[51]  Michael A. Hollingsworth,et al.  Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver , 2015, Nature Cell Biology.

[52]  J. Goodman,et al.  The life cycle of lipid droplets. , 2015, Current opinion in cell biology.

[53]  Brian Keith,et al.  HIF2α-Dependent Lipid Storage Promotes Endoplasmic Reticulum Homeostasis in Clear-Cell Renal Cell Carcinoma. , 2015, Cancer discovery.

[54]  H. Abramczyk,et al.  The role of lipid droplets and adipocytes in cancer. Raman imaging of cell cultures: MCF10A, MCF7, and MDA-MB-231 compared to adipocytes in cancerous human breast tissue. , 2015, The Analyst.

[55]  Q. Gao,et al.  Seipin performs dissectible functions in promoting lipid droplet biogenesis and regulating droplet morphology , 2015, Molecular biology of the cell.

[56]  Mario Malerba,et al.  Lipid Droplets: A New Player in Colorectal Cancer Stem Cells Unveiled by Spectroscopic Imaging , 2014, Stem cells.

[57]  Christer S. Ejsing,et al.  Two different pathways of phosphatidylcholine synthesis, the Kennedy Pathway and the Lands Cycle, differentially regulate cellular triacylglycerol storage , 2014, BMC Cell Biology.

[58]  J. Balsinde,et al.  Phospholipase A2 regulation of lipid droplet formation. , 2014, Biochimica et biophysica acta.

[59]  A. Harris,et al.  Fatty acid uptake and lipid storage induced by HIF-1α contribute to cell growth and survival after hypoxia-reoxygenation. , 2014, Cell reports.

[60]  D. Silver,et al.  Cytosolic lipid droplets: From mechanisms of fat storage to disease , 2014, Critical reviews in biochemistry and molecular biology.

[61]  Yuping Zhang,et al.  Identification of adipophilin as a potential diagnostic tumor marker for lung adenocarcinoma. , 2014, International journal of clinical and experimental medicine.

[62]  P. Roingeard,et al.  Nuclear lipid droplets identified by electron microscopy of serial sections , 2013, BMC Research Notes.

[63]  G. Lambeau,et al.  Group X secreted phospholipase A2 induces lipid droplet formation and prolongs breast cancer cell survival , 2013, Molecular Cancer.

[64]  S. Gross,et al.  Cell-to-Cell Heterogeneity in Lipid Droplets Suggests a Mechanism to Reduce Lipotoxicity , 2013, Current Biology.

[65]  R. Parton,et al.  Rab18 Binds to Hepatitis C Virus NS5A and Promotes Interaction between Sites of Viral Replication and Lipid Droplets , 2013, PLoS pathogens.

[66]  E. White,et al.  Hypoxic and Ras-transformed cells support growth by scavenging unsaturated fatty acids from lysophospholipids , 2013, Proceedings of the National Academy of Sciences.

[67]  A. Greenberg,et al.  Fat-specific protein 27 modulates nuclear factor of activated T cells 5 and the cellular response to stress[S] , 2013, Journal of Lipid Research.

[68]  Robert V Farese,et al.  Triacylglycerol synthesis enzymes mediate lipid droplet growth by relocalizing from the ER to lipid droplets. , 2013, Developmental cell.

[69]  N. Ridgway The role of phosphatidylcholine and choline metabolites to cell proliferation and survival , 2013, Critical reviews in biochemistry and molecular biology.

[70]  J. Borén,et al.  Increased Expression of the Very Low-Density Lipoprotein Receptor Mediates Lipid Accumulation in Clear-Cell Renal Cell Carcinoma , 2012, PloS one.

[71]  L. Sillerud,et al.  Autophagy regulates lipolysis and cell survival through lipid droplet degradation in androgen‐sensitive prostate cancer cells , 2012, The Prostate.

[72]  J. Borén,et al.  Apoptosis-induced mitochondrial dysfunction causes cytoplasmic lipid droplet formation , 2012, Cell Death and Differentiation.

[73]  Hong Wang,et al.  Perilipin 5, a lipid droplet-associated protein, provides physical and metabolic linkage to mitochondria[S] , 2011, Journal of Lipid Research.

[74]  Clotilde Théry,et al.  Exosome Secretion: Molecular Mechanisms and Roles in Immune Responses , 2011, Traffic.

[75]  M. Wenk,et al.  The size and phospholipid composition of lipid droplets can influence their proteome. , 2011, Biochemical and biophysical research communications.

[76]  G. Mills,et al.  Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth , 2011, Nature Medicine.

[77]  Robert V Farese,et al.  Phosphatidylcholine synthesis for lipid droplet expansion is mediated by localized activation of CTP:phosphocholine cytidylyltransferase. , 2011, Cell metabolism.

[78]  T. Walther,et al.  A Role for Phosphatidic Acid in the Formation of “Supersized” Lipid Droplets , 2011, PLoS genetics.

[79]  B. Faubert,et al.  Carnitine palmitoyltransferase 1C promotes cell survival and tumor growth under conditions of metabolic stress. , 2011, Genes & development.

[80]  R. Lothe,et al.  SPG20, a novel biomarker for early detection of colorectal cancer, encodes a regulator of cytokinesis , 2011, Oncogene.

[81]  A. Shevchenko,et al.  Human Lysophosphatidylcholine Acyltransferases 1 and 2 Are Located in Lipid Droplets Where They Catalyze the Formation of Phosphatidylcholine* , 2011, The Journal of Biological Chemistry.

[82]  C. Hellerbrand,et al.  Hypoxia‐inducible protein 2 is a novel lipid droplet protein and a specific target gene of hypoxia‐inducible factor‐1 , 2010, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[83]  J. Viola,et al.  Lipid droplets in inflammation and cancer. , 2010, Prostaglandins, leukotrienes, and essential fatty acids.

[84]  R. Zechner,et al.  Fate of fat: the role of adipose triglyceride lipase in lipolysis. , 2009, Biochimica et biophysica acta.

[85]  Robert V Farese,et al.  The life of lipid droplets. , 2009, Biochimica et biophysica acta.

[86]  Y. Yonekura,et al.  Cytosolic acetyl‐CoA synthetase affected tumor cell survival under hypoxia: the possible function in tumor acetyl‐CoA/acetate metabolism , 2009, Cancer science.

[87]  M. Czaja,et al.  Autophagy regulates lipid metabolism , 2009, Nature.

[88]  P. Bieniasz,et al.  A role for ubiquitin ligases and Spartin/SPG20 in lipid droplet turnover , 2009, The Journal of cell biology.

[89]  Robert V Farese,et al.  The Endoplasmic Reticulum Enzyme DGAT2 Is Found in Mitochondria-associated Membranes and Has a Mitochondrial Targeting Signal That Promotes Its Association with Mitochondria* , 2009, Journal of Biological Chemistry.

[90]  N. Anderson,et al.  Molecular Mechanisms and Therapeutic Targets in Steatosis and Steatohepatitis , 2008, Pharmacological Reviews.

[91]  Robert V Farese,et al.  Functional genomic screen reveals genes involved in lipid-droplet formation and utilization , 2008, Nature.

[92]  J. Viola,et al.  Lipid bodies are reservoirs of cyclooxygenase-2 and sites of prostaglandin-E2 synthesis in colon cancer cells. , 2008, Cancer research.

[93]  Nicole A. Ducharme,et al.  Lipid droplets in lipogenesis and lipolysis. , 2008, Endocrinology.

[94]  Y. Mo,et al.  Fatty acid synthase gene is up-regulated by hypoxia via activation of Akt and sterol regulatory element binding protein-1. , 2008, Cancer research.

[95]  G. Francis,et al.  Hepatic CTP:Phosphocholine Cytidylyltransferase-α Is a Critical Predictor of Plasma High Density Lipoprotein and Very Low Density Lipoprotein* , 2008, Journal of Biological Chemistry.

[96]  D. Brasaemle Thematic review series: Adipocyte Biology. The perilipin family of structural lipid droplet proteins: stabilization of lipid droplets and control of lipolysis Published, JLR Papers in Press, September 18, 2007. , 2007, Journal of Lipid Research.

[97]  J. Borén,et al.  SNARE proteins mediate fusion between cytosolic lipid droplets and are implicated in insulin sensitivity , 2007, Nature Cell Biology.

[98]  H. Ploegh A lipid-based model for the creation of an escape hatch from the endoplasmic reticulum , 2007, Nature.

[99]  D. Brasaemle,et al.  A proposed model of fat packaging by exchangeable lipid droplet proteins , 2006, FEBS letters.

[100]  S. Gross,et al.  The Lipid-Droplet Proteome Reveals that Droplets Are a Protein-Storage Depot , 2006, Current Biology.

[101]  J. Shockey,et al.  Tung Tree DGAT1 and DGAT2 Have Nonredundant Functions in Triacylglycerol Biosynthesis and Are Localized to Different Subdomains of the Endoplasmic Reticulum[W] , 2006, The Plant Cell Online.

[102]  Y. Ohsaki,et al.  Cytoplasmic lipid droplets are sites of convergence of proteasomal and autophagic degradation of apolipoprotein B. , 2006, Molecular biology of the cell.

[103]  B. Chang,et al.  Protection against Fatty Liver but Normal Adipogenesis in Mice Lacking Adipose Differentiation-Related Protein , 2006, Molecular and Cellular Biology.

[104]  D. Brasaemle,et al.  Isolation of Lipid Droplets from Cells by Density Gradient Centrifugation , 2005, Current protocols in cell biology.

[105]  H. Robenek,et al.  PAT family proteins pervade lipid droplet cores Published, JLR Papers in Press, March 1, 2005. DOI 10.1194/jlr.M400323-JLR200 , 2005, Journal of Lipid Research.

[106]  V. Holla,et al.  Requirement of phospholipase D1 activity in H-RasV12-induced transformation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[107]  Y. Higashi,et al.  Identification of major proteins in the lipid droplet-enriched fraction isolated from the human hepatocyte cell line HuH7. , 2004, Biochimica et biophysica acta.

[108]  E. Burgermeister,et al.  Peroxisome proliferator-activated receptor-γ upregulates caveolin-1 and caveolin-2 expression in human carcinoma cells , 2003, Oncogene.

[109]  P. Weller,et al.  Extranuclear Lipid Bodies, Elicited by CCR3-mediated Signaling Pathways, Are the Sites of Chemokine-enhanced Leukotriene C4 Production in Eosinophils and Basophils* , 2001, The Journal of Biological Chemistry.

[110]  A. Kimmel,et al.  Perilipins, ADRP, and other proteins that associate with intracellular neutral lipid droplets in animal cells. , 1999, Seminars in cell & developmental biology.

[111]  Ariel D. Quiroga,et al.  Analysis of lipid droplets in hepatocytes. , 2013, Methods in cell biology.