Lipidomics applications for disease biomarker discovery in mammal models

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

• 1 Han X, Gross RW. Global analyses of cellular lipidomes directly from crude extracts of biological samples by ESI mass spectrometry: a bridge to lipidomics. J. Lipid Res. 44(6), 1071–1079 (2003).•• Lipidomics was first put forward by Han and Gross in 2003. Lipidomics opens the way for a more complete characterization of lipids metabolism in different biological samples.
  Medline CASGoogle Scholar
• 2 Spener F, Lagarde M, Geloen A, Record M. What is lipidomics? Eur. J. Lipid Sci. Technol. 105(9), 481–482 (2003).
  Google Scholar
• 3 Hu C, van der Heijden R, Wang M, van der Greef J, Hankemeier T, Xu G. Analytical strategies in lipidomics and applications in disease biomarker discovery. J. Chromatogr. B 877(26), 2836–2846 (2009).
  CASGoogle Scholar
• 4 Fahy E, Subramaniam S, Brown HA et al. A comprehensive classification system for lipids. J. Lipid Res. 46(5), 839–862 (2005).• Classification system for lipids has been reported for the first time.
  Medline CASGoogle Scholar
• 5 Fahy E, Subramaniam S, Murphy RC et al. Update of the LIPID MAPS comprehensive classification system for lipids. J. Lipid Res. 50(S), 9–14 (2009).
  Google Scholar
• 6 Folch J, Lees M, Sloane-Stanley GH. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226(1), 497–509 (1957).
  Medline CASGoogle Scholar
• 7 Hermansson M, Käkelä R, Berghäll M, Lehesjoki AE, Somerharju P, Lahtinen U. Mass spectrometric analysis reveals changes in phospholipid, neutral sphingolipid and sulfatide molecular species in progressive epilepsy with mental retardation, EPMR, brain: a case study. J. NeuroChem. 95(3), 609–617 (2005).
  Medline CASGoogle Scholar
• 8 Löfgren L, Ståhlman M, Forsberg GB, Saarinen S, Nilsson R, Hansson GI. The BUME method: a novel automated chloroform-free 96-well total lipid extraction method for blood plasma. J. Lipid Res. 53(8), 1690–1700 (2012).
  MedlineGoogle Scholar
• 9 Saunders RD, Horrocks LA. Simultaneous extraction and preparation for high-performance liquid chromatography of prostaglandins and phospholipids. Anal. BioChem. 143(1), 71–75 (1984).
  Medline CASGoogle Scholar
• 10 Chen S, Hoene M, Li J et al. Simultaneous extraction of metabolome and lipidome with methyl tert-butyl ether from a single small tissue sample for ultra-high performance liquid chromatography/mass spectrometry. J. Chromatogr. A 1298, 9–16 (2013).
  Medline CASGoogle Scholar
• 11 Kim HY, Salem N Jr. Separation of lipid classes by solid phase extraction. J. Lipid Res. 31(12), 2285–2289 (1990).
  Medline CASGoogle Scholar
• 12 Hauff S, Vetter W. Quantification of fatty acids as methyl esters and phospholipids in cheese samples after separation of triacylglycerides and phospholipids. Anal. Chim. Acta 636(2), 229–235 (2009).
  Medline CASGoogle Scholar
• 13 Sheng J, Vannela R, Rittmann BE. Evaluation of methods to extract and quantify lipids from Synechocystis PCC 6803. Bioresour. Technol. 102(2), 1697–1703 (2011).
  Medline CASGoogle Scholar
• 14 Luque-García JL, Luque de Castro MD. Focused microwave-assisted Soxhlet extraction: devices and applications. Talanta 64(3), 571–577 (2004).
  Medline CASGoogle Scholar
• 15 Luque-García JL, Luque de Castro MD. Ultrasound-assisted Soxhlet extraction: an expeditive approach for solid sample treatment. Application to the extraction of total fat from oleaginous seeds. J. Chromatogr. A 1034(1–2), 237–242 (2004).
  Medline CASGoogle Scholar
• 16 Pizarro C, Arenzana-Rámila I, Pérez-del-Notario N, Pérez-Matute P, González-Sáiz JM. Plasma lipidomic profiling method based on ultrasound extraction and liquid chromatography mass spectrometry. Anal. Chem. 85(24), 12085–12092 (2013).
  Medline CASGoogle Scholar
• 17 Isaac G. Development of enhanced analytical methodology for lipid analysis from sampling to detection. A Targeted Lipidomics Approach. Uppsala University, Sweden (2005). www.diva-portal.org/smash/get/diva2:166474/FULLTEXT01.pdf.
  Google Scholar
• 18 Self R. Extraction of Organic Analytes from Foods, The Royal Society of Chemistry, Cambridge, UK (2005).
  Google Scholar
• 19 Gross RW, Han X. Shotgun lipidomics of neutral lipids as an enabling technology for elucidation of lipid-related diseases. Am. J. Physiol. Endocrinol. Metab. 297(2), E297–E303 (2009).
  Medline CASGoogle Scholar
• 20 Han X, Gross RW. Shotgun lipidomics-multidimensional MS analysis of cellular lipidomes. Expert Rev. Proteomics 2(2), 253–264 (2005).
  Medline CASGoogle Scholar
• 21 Ståhlman M, Ejsing CS, Tarasov K, Perman J, Borén J, Ekroos K. High-throughput shotgun lipidomics by quadrupole time-of-flight mass spectrometry. J. Chromatogr. B 877(26), 2664–2672 (2009).
  CASGoogle Scholar
• 22 Zehethofer N, Pinto DM. Recent developments in tandem mass spectrometry for lipidomic analysis. Anal. Chim. Acta 627(1), 62–70 (2008).
  Medline CASGoogle Scholar
• 23 Wenk MR. The emerging field of lipidomics. Nat. Rev. Drug Discov. 4(7), 594–610 (2005).
  Medline CASGoogle Scholar
• 24 Wenk MR, Lucast L, Di Paolo G et al. Phosphoinositide profiling in complex lipid mixtures using electrospray ionization mass spectrometry. Nat. BioTechnol. 21(7), 813–817 (2003).
  Medline CASGoogle Scholar
• 25 Koivusalo M, Haimi P, Heikinheimo L, Kostiainen R, Somerharju P. Quantitative determination of phospholipid compositions by ESI-MS: effects of acyl chain length, unsaturation, and lipid concentration on instrument response. J. Lipid Res. 42(4), 663–672 (2001).
  MedlineGoogle Scholar
• 26 Brügger B, Erben G, Sandhoff R, Wieland FT, Lehmann WD. Quantitative analysis of biological membrane lipids at the low picomole level by nano-electrospray ionization tandem mass spectrometry. Proc. Natl Acad. Sci. USA 94(6), 2339–2344 (1997).
  Medline CASGoogle Scholar
• 27 Taguchi R, Hayakawa J, Takeuchi Y, Ishida M. Two-dimensional analysis of phospholipids by capillary liquid chromatography/electrospray ionization mass spectrometry. J. Mass Spectrom. 35(8), 953–966 (2000).
  Medline CASGoogle Scholar
• 28 Houjou T, Yamatani K, Imagawa M, Shimizu T, Taguchi R. A shotgun tandem mass spectrometric analysis of phospholipids with normal-phase and/or reverse-phase liquid chromatography/electrospray ionization mass spectrometry. Rapid Commun. Mass Spectrom. 19(5), 654–666 (2005).
  Medline CASGoogle Scholar
• 29 Avigan J, Goodman DS, Steinberg D. Thin-layer chromatography of sterols and steroids. J. Lipid Res. 4(1), 100–101 (1963).
  Medline CASGoogle Scholar
• 30 Sommerer D, Süss R, Hammerschmidt S, Wirtz H, Arnold K, Schiller J. Analysis of the phospholipid composition of bronchoalveolar lavage (BAL) fluid from man and minipig by MALDI-TOF mass spectrometry in combination with TLC. J. Pharm. BioMed. Anal. 35(1), 199–206 (2004).
  Medline CASGoogle Scholar
• 31 Fuchs B, Schiller J, Süss R et al. Analysis of stem cell lipids by offline HPTLC-MALDI-TOF MS. Anal. BioAnal. Chem. 392(5), 849–860 (2008).
  Medline CASGoogle Scholar
• 32 Gao F, Tian X, Wen D, Liao J, Wang T, Liu H. Analysis of phospholipid species in rat peritoneal surface layer by liquid chromatography/electrospray ionization ion-trap mass spectrometry. Biochim. Biophys. Acta 1761(7), 667–676 (2006).
  Medline CASGoogle Scholar
• 33 Olsson P, Holmbäck J, Nilsson U. Herslöf B. Separation and identification of lipid classes by normal phase LC-ESI/MS/MS on a cyanopropyl column. Eur. J. Lipid Sci. Technol. 116(5), 653–658 (2014).
  CASGoogle Scholar
• 34 Leskinen H, Suomela JP, Pinta J, Kallio H. Regioisomeric structure determination of alpha- and gamma-linolenoyldilinoleoylglycerol in blackcurrant seed oil by silver ion high-performance liquid chromatography and mass spectrometry. Anal. Chem. 80(15), 5788–5793 (2008).
  Medline CASGoogle Scholar
• 35 Deng L, Nakano H, Iwasaki Y. Direct separation of monoacylglycerol isomers by enantioselective high-performance liquid chromatography. J. Chromatogr. A 1198–1199, 67–72 (2008).
  Medline CASGoogle Scholar
• 36 Rainville PD, Stumpf CL, Shockcor JP, Plumb RS, Nicholson JK. Novel application of reversed-phase UPLC-oaTOF-MS for lipid analysis in complex biological mixtures: a new tool for lipidomics. J. Proteome Res. 6(2), 552–558 (2007).
  Medline CASGoogle Scholar
• 37 Chen S, Wei C, Gao P et al. Effect of Allium macrostemon on a rat model of depression studied by using plasma lipid and acylcarnitine profiles from liquid chromatography/mass spectrometry. J. Pharm. BioMed. Anal. 89, 122–129 (2014).
  Medline CASGoogle Scholar
• 38 Zhao YY, Wu SP, Liu S, Zhang Y, Lin RC. Ultra-performance liquid chromatography-mass spectrometry as a sensitive and powerful technology in lipidomic applications. Chem. Biol. Interact. 220, 181–192 (2014).•• This review reported UPLC-MS as a sensitive and powerful technology in lipidomic applications.
  Medline CASGoogle Scholar
• 39 Wrona M, Mauriala T, Bateman KP, Mortishire-Smith RJ, O'Connor D. ‘All-in-One’ analysis for metabolite identification using liquid chromatography/hybrid quadrupole time-of-flight mass spectrometry with collision energy switching. Rapid Commun. Mass Spectrom. 19(18), 2597–2602 (2005).
  Medline CASGoogle Scholar
• 40 Zhao YY, Lin RC. UPLC–MS^E application in disease biomarker discovery: the discoveries in proteomics to metabolomics. Chem. Biol. Interact. 215, 7–16 (2014).•• UPLC–MSE is regarded as one of the more suitable techniques in proteomics and metabolomics. This technique will widely apply to lipidomics in the future.
  Medline CASGoogle Scholar
• 41 Zhao YY. Metabolomics in chronic kidney disease. Clin. Chim. Acta 422, 59–69 (2013).
  Medline CASGoogle Scholar
• 42 Zhao YY, Lin RC. Metabolomics in nephrotoxicity. Adv. Clin. Chem. 65, 69–89 (2014).
  Medline CASGoogle Scholar
• 43 Zhao YY, Cheng XL, Wei F et al. Intrarenal metabolomic investigation of chronic kidney disease and its TGF-β1 mechanism in induced-adenine rats using UPLC Q-TOF/HSMS/MS^E. J. Proteome Res. 12(2), 692–703 (2013).
  Medline CASGoogle Scholar
• 44 Zhao YY, Liu J, Cheng XL, Bai X, Lin RC. Urinary metabonomics study on biochemical changes in an experimental model of chronic renal failure by adenine based on UPLC Q-TOF/MS. Clin. Chim. Acta 413(5–6), 642–649 (2012).
  Medline CASGoogle Scholar
• 45 Zhao YY, Shen X, Cheng XL, Wei F, Bai X, Lin RC. Urinary metabonomics study on the protective effects of ergosta-4,6,8(14),22-tetraen-3-one on chronic renal failure in rats using UPLC Q-TOF/MS and a novel MS^E data collection technique. Process BioChem. 47(12), 1980–1987 (2012).
  CASGoogle Scholar
• 46 Zhao YY, Zhang L, Long FY et al. UPLC-Q-TOF/HSMS/MS^E-based metabonomics for adenine-induced changes in metabolic profiles of rat faeces and intervention effects of ergosta-4,6,8(14),22-tetraen-3-one. Chem. Biol. Interact. 301(1–3), 31–38 (2013).
  Google Scholar
• 47 Zhao YY, Lei P, Chen DQ, Feng YL, Bai X. Renal metabolic profiling of early renal injury and renoprotective effects of poria cocos epidermis using UPLC Q-TOF/HSMS/MS^E. J. Pharm. BioMed. Anal. 81–82(1), 202–209 (2013).
  Medline CASGoogle Scholar
• 48 Guo X, Lankmayr E. Multidimensional approaches in LC and MS for phospholipid bioanalysis. Bioanalysis 2(6), 1109–1123 (2010).
  Medline CASGoogle Scholar
• 49 Kliman M, May JC, McLean JA. Lipid analysis and lipidomics by structurally selective ion mobility-mass spectrometry. Biochim. Biophys. Acta 1811(11), 935–945 (2011).
  Medline CASGoogle Scholar
• 50 Vilella F, Ramirez LB, Simón C. Lipidomics as an emerging tool to predict endometrial receptivity. Fertil. Steril. 99(4), 1100–1106 (2013).
  Medline CASGoogle Scholar
• 51 Zietkowski D, Payne GS, Nagy E, Mobberley MA, Ryder TA, deSouza NM. Comparison of NMR lipid profiles in mitotic arrest and apoptosis as indicators of paclitaxel resistance in cervical cell lines. Magn. Reson. Med. 68(2), 369–377 (2012).
  Medline CASGoogle Scholar
• 52 Gawrisch K, Eldho NV, Polozov IV. Novel NMR tools to study structure and dynamics of biomembranes. Chem. Phys. Lipids 116(1–2), 135–151 (2002).
  Medline CASGoogle Scholar
• 53 Sharman MJ, Shui G, Fernandis AZ et al. Profiling brain and plasma lipids in human APOE epsilon2, epsilon3, and epsilon4 knock-in mice using electrospray ionization mass spectrometry. J. Alzheimers Dis. 20(1), 105–111 (2010).
  Medline CASGoogle Scholar
• 54 Oliveira TG, Chan RB, Tian H et al. Phospholipase D2 ablation ameliorates Alzheimer's disease-linked synaptic dysfunction and cognitive deficits. J. Neurosci. 30(49), 16419–16428 (2010).
  Medline CASGoogle Scholar
• 55 Chan C, Qi X, Li MW, Wong FL, Lam HM. Recent developments of genomic research in soybean. J. Genet. Genomics 39(7), 317–324 (2012).
  Medline CASGoogle Scholar
• 56 Barceló-Coblijn G, Golovko MY, Weinhofer I, Berger J, Murphy EJ. Brain neutral lipids mass is increased in alpha-synuclein gene-ablated mice. J. NeuroChem. 101(1), 132–141 (2007).
  Medline CASGoogle Scholar
• 57 Rappley I, Myers DS, Milne SB et al. Lipidomic profiling in mouse brain reveals differences between ages and genders, with smaller changes associated with α-synuclein genotype. J. NeuroChem. 111(1), 15–25 (2009).
  Medline CASGoogle Scholar
• 58 Bijl N, Sokolović M, Vrins C et al. Modulation of glyco-sphingolipid metabolism significantly improves hepatic insulin sensitivity and reverses hepatic steatosis in mice. Hepatology 50(5), 1431–1441 (2009).
  Medline CASGoogle Scholar
• 59 van Eijk M, Aten J, Bijl N et al. Reducing glycosphingolipid content in adipose tissue of obese mice restores insulin sensitivity, adipogenesis and reduces inflammation. PLoS ONE 4(3), e4723 (2009).
  MedlineGoogle Scholar
• 60 Shui G, Lam SM, Stebbins J et al. Polar lipid derangements in Type 2 diabetes mellitus: potential pathological relevance of fatty acyl heterogeneity in sphingolipids. Metabolomics 9(4), 786–799 (2013).• The study identifies metabolic alterations in sphingolipid pathways as early events in Type 2 diabetes mellitus pathogenesis, and provides new insights relevant for larger scale clinical studies aimed at identification of early molecular biomarkers of Type 2 diabetes mellitus.
  CASGoogle Scholar
• 61 Puri P, Wiest MM, Cheung O et al. The plasma lipidomic signature of nonalcoholic steatohepatitis. Hepatology 50(6), 1827–1838 (2009).
  Medline CASGoogle Scholar
• 62 González-Périz A, Horrillo R, Ferré N et al. Obesity-induced insulin resistance and hepatic steatosis are alleviated by omega-3 fatty acids: a role for resolvins and protectins. FASEB J. 23(6), 1946–1957 (2009).
  Medline CASGoogle Scholar
• 63 Hall D, Poussin C, Velagapudi VR et al. Peroxisomal and microsomal lipid pathways associated with resistance to hepatic steatosis and reduced pro-inflammatory state. J. Biol. Chem. 285(40), 31011–31023 (2010).
  Medline CASGoogle Scholar
• 64 Dória ML, Cotrim Z, Macedo B et al. Lipidomic approach to identify patterns in phospholipid profiles and define class differences in mammary epithelial and breast cancer cells. Breast Cancer Res. Treat. 133(2), 635–648 (2012).
  Medline CASGoogle Scholar
• 65 Dória ML, Cotrim CZ, Simões C et al. Lipidomic analysis of phospholipids from human mammary epithelial and breast cancer cell lines. J. Cell Physiol. 228(2), 457–468 (2013).
  Medline CASGoogle Scholar
• 66 Zhang L, Peterson BL, Cummings BS. The effect of inhibition of Ca²⁺-independent phospholipase A2 on chemotherapeutic-induced death and phospholipid profiles in renal cells. BioChem. Pharmacol. 70(11), 1697–1706 (2005).
  Medline CASGoogle Scholar
• 67 Mal M, Koh PK, Cheah PY, Chan EC. Ultra-pressure liquid chromatography/tandem mass spectrometry targeted profiling of arachidonic acid and eicosanoids in human colorectal cancer. Rapid Commun. Mass Spectrom. 25(6), 755–764 (2011).• This study demonstrated that eicosanoids play an important role in associating inflammation with human colorectal cancer.
  Medline CASGoogle Scholar
• 68 Muir K, Hazim A, He Y et al. Proteomic and lipidomic signatures of lipid metabolism in NASH-associated hepatocellular carcinoma. Cancer Res. 73(15), 4722–4731 (2013).
  Medline CASGoogle Scholar
• 69 Chan R, Uchil PD, Jin J et al. Retroviruses human immunodeficiency virus and murine leukemia virus are enriched in phosphoinositides. J. Virol. 82(22), 11228–11238 (2008).
  Medline CASGoogle Scholar
• 70 Low KL, Rao PS, Shui G et al. Triacylglycerol utilization is required for regrowth of in vitro hypoxic nonreplicating Mycobacterium bovis bacillus Calmette–Guérin. J. Bacteriol. 191(16), 5037–5043 (2008).
  Google Scholar
• 71 Low KL, Shui G, Natter K et al. Lipid droplet-associated proteins are involved in the biosynthesis and hydrolysis of triacylglycerol in Mycobacterium bovis bacillus Calmette–Guérin. J. Biol. Chem. 285(28), 21662–21670 (2010).
  Medline CASGoogle Scholar
• 72 Hartmann T, Kuchenbecker J, Grimm MOW. Alzheimer's disease: the lipid connection. J. Neurochem. 103(S1), 159–170 (2007).
  Medline CASGoogle Scholar
• 73 Berman DE, Dall'Armi C, Voronov SV et al. Oligomeric amyloid-beta peptide disrupts phosphatidylinositol-4,5-bisphosphate metabolism. Nat. Neurosci. 11(5), 547–554 (2008).
  Medline CASGoogle Scholar
• 74 Davignon J, Gregg RE, Sing CF. Apolipoprotein E polymorphism and atherosclerosis. Arteriosclerosis 8(1), 1–21 (1988).
  Medline CASGoogle Scholar
• 75 Lim WL, Lam SM, Shui G et al. Effects of high-fat, high-cholesterol diet on brain lipid profiles in apolipoprotein E 33 and 34 knock-in mice. NeuroBiol. Aging 34(9), 221722–221724 (2013).
  Google Scholar
• 76 Zeng Y, Cheng H, Jiang X, Han X. Endosomes and lysosomes play distinct roles in sulfatide-induced neuroblastoma apoptosis: potential mechanisms contributing to abnormal sulfatide metabolism in related neuronal diseases. BioChem. J. 410(1), 81–92 (2008).
  Medline CASGoogle Scholar
• 77 Sanchez-Mejia RO, Newman JW, Toh S et al. Phospholipase A2 reduction ameliorates cognitive deficits in a mouse model of Alzheimer's disease. Nat. Neurosci. 11(11), 1311–1318 (2008).
  Medline CASGoogle Scholar
• 78 Singh IN, McCartney DG, Kanfer JN. Amyloid-beta protein (25–35) stimulation of phospholipases A, C and D activities of La-N-2 cells. Febs Lett. 365(2–3), 125–128 (1995).
  Medline CASGoogle Scholar
• 79 Kim JH, Lee BD, Kim Y, Lee SD, Suh PG, Ryu SH. Cytosolic phospholipase A2-mediated regulation of phospholipase D2 in leukocyte cell lines. J. Immunol. 163(10), 5462–5470 (1999).
  Medline CASGoogle Scholar
• 80 Gai WP, Yuan HX, Li XQ, Power JT, Blumbergs PC, Jensen PH. In situ and in vitro study of colocalization and segregation of alpha-synuclein, ubiquitin, and lipids in Lewy bodies. Exp. Neurol. 166(2), 324–333 (2000).
  Medline CASGoogle Scholar
• 81 Ruipérez V, Darios F, Davletov B. Alpha-synuclein, lipids and Parkinson's disease. Prog. Lipid Res. 49(4), 420–428 (2009).
  Google Scholar
• 82 Bosco DA, Fowler DM, Zhang Q et al. Elevated levels of oxidized cholesterol metabolites in Lewy body disease brains accelerate alpha-synuclein fibrilization. Nat. Chem. Biol. 2(5), 249–253 (2006).
  Medline CASGoogle Scholar
• 83 Bar-On P, Crews L, Koob AO et al. Statins reduce neuronal alpha-synuclein aggregation in in vitro models of Parkinson's disease. J. NeuroChem. 105(5), 1656–1667 (2008).
  Medline CASGoogle Scholar
• 84 Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M. Alpha-synuclein in Lewy bodies. Nature 388(6645), 839–840 (1997).
  Medline CASGoogle Scholar
• 85 Polymeropoulos MH, Lavedan C, Leroy E et al. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276(5321), 2045–2047 (1997).
  Medline CASGoogle Scholar
• 86 Kruger R, Kuhn W, Muller T et al. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat. Genet. 18(2), 106–108 (1988).
  Google Scholar
• 87 Zarranz JJ, Alegre J, Gomez-Esteban JC et al. The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann. Neurol. 55(2), 164–173 (2004).
  Medline CASGoogle Scholar
• 88 Singleton AB, Farrer M, Johnson J et al. Alpha-synuclein locus triplication causes Parkinson's disease. Science 302(5646), 841 (2003).
  Medline CASGoogle Scholar
• 89 Ibanez P, Bonnet AM, Debarges B et al. Causal relation between alpha-synuclein gene duplication and familial Parkinson's disease. Lancet 364(9440), 1169–1171 (2004).
  Medline CASGoogle Scholar
• 90 Chen H, Miao H, Feng YL, Zhao YY, Lin RC. Metabolomics in dyslipidemia. Adv. Clin. Chem. 66, 101–119 (2014).
  Medline CASGoogle Scholar
• 91 Miao H, Chen H, Zhang X et al. Urinary metabolomics on the biochemical profiles in diet-induced hyperlipidemia rat using ultra-performance liquid chromatography coupled with quadrupole time-of-flight synapt high-definition mass spectrometry. J. Anal. Methods Chem. 184162 (2014) (2014).
  MedlineGoogle Scholar
• 92 Fletcher MJ. A colorimetric method for estimating serum triglycerides. Clin. Chim. Acta 22(3), 393–397 (1968).
  Medline CASGoogle Scholar
• 93 Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27(10), 1047–1053 (2004).
  MedlineGoogle Scholar
• 94 Li J, Romestaing C, Han X et al. Cardiolipin remodeling by ALCAT1 links oxidative stress and mitochondrial dysfunction to obesity. Cell Metab. 12(2), 154–165 (2010).
  Medline CASGoogle Scholar
• 95 Cinti S, Mitchell G, Barbatelli G et al. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J. Lipid Res. 46(11), 2347–2355 (2005).
  Medline CASGoogle Scholar
• 96 Inokuchi JI. Membrane microdomains and insulin resistance. FEBS Lett. 584(9), 1864–1871 (2010).
  Medline CASGoogle Scholar
• 97 Haus JM, Kashyap, SR, Kasumov T et al. Plasma ceramides are elevated in obese subjects with Type 2 diabetes and correlate with the severity of insulin resistance. Diabetes 58(2), 337–343 (2009).
  Medline CASGoogle Scholar
• 98 de Mello VDF, Lankinen M, Schwab U et al. Link between plasma ceramides, inflammation and insulin resistance: association with serum IL-6 concentration in patients with coronary heart disease. Diabetologia 52(12), 2612–2615 (2009).
  Medline CASGoogle Scholar
• 99 Holland WL, Bikman BT, Wang LP et al. Lipid-induced insulin resistance mediated by the proinflammatory receptor TLR4 requires saturated fatty acid-induced ceramide biosynthesis in mice. J. Clin. Invest. 121(5), 1858–1870 (2011).
  Medline CASGoogle Scholar
• 100 Tagami S, Inokuchi Ji JI, Kabayama K et al. Ganglioside GM3 participates in the pathological conditions of insulin resistance. J. Biol. Chem. 277(5), 3085–3092 (2002).
  Medline CASGoogle Scholar
• 101 Kabayama K, Sato T, Saito K et al. Dissociation of the insulin receptor and caveolin-1 complex by ganglioside GM3 in the state of insulin resistance. Proc. Natl Acad. Sci. USA 104(34), 13678–13683 (2007).
  Medline CASGoogle Scholar
• 102 Watkins SM, Reifsnyder PR, Pan HJ, German JB, Leiter EH. Lipid metabolome-wide effects of the PPAR gamma agonist rosiglitazone. J. Lipid Res. 43(11), 1809–1817 (2002).
  Medline CASGoogle Scholar
• 103 Malhi H, Bronk SF, Werneburg NW, Gores GJ. Free fatty acids induce JNK-dependent hepatocyte lipoapoptosis. J. Biol. Chem. 281(17), 12093–12101 (2006).
  Medline CASGoogle Scholar
• 104 Cao H, Gerhold K, Mayers JR, Wiest MM, Watkins SM, Hotamisligil GS. Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism. Cell 134(6), 933–944 (2008).
  Medline CASGoogle Scholar
• 105 Yki-Jarvinen H. Thiazolidinediones and the liver in humans. Curr. Opin. Lipidol. 20(6), 477–483 (2009).
  MedlineGoogle Scholar
• 106 Culp BR, Titus BG, Lands WE. Inhibition of prostaglandin biosynthesis by eicosapentaenoic acid. Prostaglandins Med. 3(5), 269–278 (1979).
  Medline CASGoogle Scholar
• 107 López-Parra M, Titos E, Horrillo R et al. Regulatory effects of arachidonate 5-lipoxygenase on hepatic MTP activity and VLDL-TG and ApoB secretion in obese mice. J. Lipid Res. 49(12), 2513–2523 (2008).
  Medline CASGoogle Scholar
• 108 Merched AJ, Ko K, Gotlinger KH, Serhan CN, Chan L. Atherosclerosis: evidence for impairment of resolution of vascular inflammation governed by specific lipid mediators. FASEB J. 22(10), 3595–3606 (2008).
  Medline CASGoogle Scholar
• 109 Fernandis AZ, Wenk MR. Lipid-based biomarkers for cancer. J. Chromatogr. B 877(26), 2830–2835 (2009).
  CASGoogle Scholar
• 110 Patra SK. Dissecting lipid raft facilitated cell signaling pathways in cancer. Biochim. Biophys. Acta Rev. Cancer 1785(2), 182–206 (2008).
  Medline CASGoogle Scholar
• 111 Ackerstaff E, Glunde K, Bhujwalla ZM. Choline phospholipid metabolism: a target in cancer cells? J. Cell BioChem. 90(3), 525–533 (2003).
  Medline CASGoogle Scholar
• 112 Bian D, Su S, Mahanivong C et al. Lysophosphatidic acid stimulates ovarian cancer cell migration via a Ras-MEK kinase 1 pathway. Cancer Res. 64(12), 4209–4217 (2004).
  Medline CASGoogle Scholar
• 113 Cummings BS, Gelasco AK, Kinsey GR, McHowat J, Schnellmann RG. Inactivation of endoplasmic reticulum bound Ca²⁺-independent phospholipase A2 in renal cells during oxidative stress. J. Am. Soc. Nephrol. 15(6), 1441–1451 (2004).
  Medline CASGoogle Scholar
• 114 Llorente A, Skotland T, Sylvänne T et al. Molecular lipidomics of exosomes released by PC-3 prostate cancer cells. Biochim. Biophys. Acta 1831(7), 1302–1309 (2013).
  Medline CASGoogle Scholar
• 115 Chan AT, Giovannucci EL, Meyerhardt JA, Schernhammer ES, Curhan GC, Fuchs CS. Long-term use of aspirin and nonsteroidal anti-inflammatory drugs and risk of colorectal cancer. J. Am. Med. Assn. 294(8), 914–923 (2005).
  Medline CASGoogle Scholar
• 116 Soslow RA, Dannenberg AJ, Rush D et al. COX-2 is expressed in human pulmonary, colonic, and mammary tumors. Cancer 89(12), 2637–2645 (2000).
  Medline CASGoogle Scholar
• 117 Melstrom LG1, Bentrem DJ, Salabat MR et al. Overexpression of 5-lipoxygenase in colon polyps and cancer and the effect of 5-LOX inhibitors in vitro and in a murine model. Clin. Cancer Res. 14(20), 6525–6530 (2008).
  Medline CASGoogle Scholar
• 118 Maskrey BH, Megson IL, Rossi AG, Whitfield PD. Emerging importance of omega-3 fatty acids in the innate immune response: Molecular mechanisms and lipidomic strategies for their analysis. Mol. Nutr. Food Res. 57(8), 1390–1400 (2013).
  Medline CASGoogle Scholar
• 119 Weylandt KH, Krause LF, Gomolka B et al. Suppressed liver tumorigenesis in fat-1 mice with elevated omega-3 fatty acids is associated with increased omega-3 derived lipid mediators and reduced TNF-α. Carcinogenesis 32(6), 897–903 (2011).
  Medline CASGoogle Scholar
• 120 Horie Y, Suzuki A, Kataoka E et al. Hepatocyte-specific Pten deficiency results in steatohepatitis and hepatocellular carcinomas. J. Clin. Invest. 113(12), 1774–1783 (2014).
  Google Scholar
• 121 Jelonek K, Ros M, Pietrowska1 M, Widlak P. Cancer biomarkers and mass spectrometry-based analyses of phospholipids in body fluids. Clin. Lipidol. 8(1), 137–150 (2013).
  CASGoogle Scholar
• 122 van der Meer-Janssen YP, van Galen J, Batenburg JJ, Helms JB. Lipids in host–pathogen interactions: pathogens exploit the complexity of the host cell lipidome. Prog. Lipid Res. 49(1), 1–26 (2010).
  Medline CASGoogle Scholar
• 123 Aloia RC, Tian H, Jensen FC. Lipid composition and fluidity of the human immunodeficiency virus envelope and host cell plasma membranes. Proc. Natl Acad. Sci. USA 90(11), 5181–5185 (1993).
  Medline CASGoogle Scholar
• 124 Saad JS, Miller J, Tai J, Kim A, Ghanam RH, Summers MF. Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly. Proc. Natl Acad. Sci. USA 103(30), 11364–11369 (2006).
  Medline CASGoogle Scholar
• 125 Ehrt S, Schnappinger D. Mycobacterium tuberculosis virulence: lipids inside and out. Nat. Med. 13(3), 284–285 (2007).
  Medline CASGoogle Scholar
• 126 Zhao YY, Cheng XL, Vaziri ND, Liu S, Lin RC. UPLC-based metabonomics applications for discovering biomarkers of diseases in clinical chemistry. Clin. BioChem. 47(15), 16–26 (2014).
  Medline CASGoogle Scholar
• 127 Zhao YY, Cheng XL, Wei F et al. Serum metabonomics study of adenine-induced chronic renal failure rat by ultra performance liquid chromatography coupled with quadrupole time-of-flight mass spectrometry. Biomarkers 17(1), 48–55 (2012).
  Medline CASGoogle Scholar
• 128 Zhao YY, Feng YL, Bai X, Tan XJ, Lin RC, Mei Q. Ultra performance liquid chromatography-based metabonomic study of therapeutic effect of the surface layer of Poria cocos on adenine-induced chronic kidney disease provides new insight into anti-fibrosis mechanism. PLoS ONE 8(3), e59617 (2013).
  Medline CASGoogle Scholar
• 129 Zhao YY, Li HT, Feng YL, Bai X, Lin RC. Urinary metabonomic study of the surface layer of poria cocos as an effective treatment for chronic renal injury in rats. J. Ethnopharmacol. 148(2), 403–410 (2013).
  Medline CASGoogle Scholar
• 130 Zhao YY, Cheng XL, Wei F, Bai X, Lin RC. Application of faecal metabonomics on an experimental model of tubulointerstitial fibrosis by ultra performance liquid chromatography/high-sensitivity mass spectrometry with MS^E data collection technique. Biomarkers 17(8), 721–729 (2012).
  Medline CASGoogle Scholar