Bioinformatics strategies for lipidomics analysis: characterization of obesity related hepatic steatosis

BMC Systems Biology - Tập 1 Số 1 - 2007
Laxman Yetukuri1, Mikko Katajamaa2, Gema Medina-Gómez3, Tuulikki Seppänen‐Laakso1, Antonio Vidal‐Puig3, Matej Orešič1
1VTT Technical Research Centre of Finland, Tietotie 2, FIN-02044, Espoo, Finland
2Turku Centre for Biotechnology, Tykistökatu 6, FIN-20521, Turku, Finland
3University of Cambridge Department of Clinical Biochemistry, Addenbrooke's Hospital, Hills Road, CB2 2QR, Cambridge, UK

Tóm tắt

Abstract Background

Lipids are an important and highly diverse class of molecules having structural, energy storage and signaling roles. Modern analytical technologies afford screening of many lipid molecular species in parallel. One of the biggest challenges of lipidomics is elucidation of important pathobiological phenomena from the integration of the large amounts of new data becoming available.

Results

We present computational and informatics approaches to study lipid molecular profiles in the context of known metabolic pathways and established pathophysiological responses, utilizing information obtained from modern analytical technologies. In order to facilitate identification of lipids, we compute the scaffold of theoretically possible lipids based on known lipid building blocks such as polar head groups and fatty acids. Each compound entry is linked to the available information on lipid pathways and contains the information that can be utilized for its automated identification from high-throughput UPLC/MS-based lipidomics experiments. The utility of our approach is demonstrated by its application to the lipidomic characterization of the fatty liver of the genetically obese insulin resistant ob/ob mouse model. We investigate the changes of correlation structure of the lipidome using multivariate analysis, as well as reconstruct the pathways for specific molecular species of interest using available lipidomic and gene expression data.

Conclusion

The methodology presented herein facilitates identification and interpretation of high-throughput lipidomics data. In the context of the ob/ob mouse liver profiling, we have identified the parallel associations between the elevated triacylglycerol levels and the ceramides, as well as the putative activated ceramide-synthesis pathways.

Từ khóa


Tài liệu tham khảo

Vance DE, Vance JE: Biochemistry of lipids, lipoproteins and membranes. Edited by: Bernardi G. 2004, Amsterdam, The Netherlands, Elsevier B. V., 4th

Fahy E, Subramaniam S, Brown HA, Glass CK, Merrill AH, Murphy RC, Raetz CRH, Russell DW, Seyama Y, Shaw W, Shimizu T, Spener F, van Meer G, VanNieuwenhze MS, White SH, Witztum JL, Dennis EA: A comprehensive classification system for lipids. J Lipid Res. 2005, 46: 839-862. 10.1194/jlr.E400004-JLR200

Wenk MR: The emerging field of lipidomics. Nat Rev Drug Discov. 2005, 4: 594-610. 10.1038/nrd1776

van Meer G: Cellular lipidomics. EMBO J. 2005, 24: 3159-3165. 10.1038/sj.emboj.7600798

Watson AD: Thematic review series: systems biology approaches to metabolic and cardiovascular disorders. Lipidomics: a global approach to lipid analysis in biological systems. J Lipid Res. 2006, 47: 2101-2111. 10.1194/jlr.R600022-JLR200

Lagarde M, Geloen A, Record M, Vance D, Spener F: Lipidomics is emerging. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids. 2003, 1634: 61-10.1016/j.bbalip.2003.11.002.

LIPID MAPS. http://www.lipidmaps.org

Cotter D, Maer A, Guda C, Saunders B, Subramaniam S: LMPD: LIPID MAPS proteome database. Nucl Acids Res. 2006, 34: D507-510. 10.1093/nar/gkj122

LipidBank. http://www.lipidbank.jp

CyberLipids. http://www.cyberlipid.org/

LIPIDAT. http://www.lipidat.chemistry.ohio-state.edu/home.stm

Hermansson M, Uphoff A, Kakela R, Somerharju P: Automated quantitative analysis of complex lipidomes by liquid chromatography/mass spectrometry. Anal Chem. 2005, 77: 2166-2175. 10.1021/ac048489s

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 Comm Mass Spectrom. 2005, 19: 654-666. 10.1002/rcm.1836.

Guan XL, He X, Ong WY, Yeo WK, Shui G, Wenk MR: Non-targeted profiling of lipids during kainate-induced neuronal injury. FASEB J. 2006, 20: 1152-1161. 10.1096/fj.05-5362com

Bijlsma S, Bobeldijk I, Verheij ER, Ramaker R, Kochhar S, Macdonald IA, vanOmmen B, Smilde AK: Large-scale human metabolomics studies: A strategy for data (pre-) processing and validation. Anal Chem. 2006, 78: 567-574. 10.1021/ac051495j

Ekroos K, Chernushevich IV, Simons K, Shevchenko A: Quantitative profiling of phospholipids by multiple precursor ion scanning on a hybrid quadrupole time-of-flight mass spectrometer. Anal Chem. 2002, 74: 941 -9949. 10.1021/ac015655c

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. 2003, 44: 1071-1079. 10.1194/jlr.R300004-JLR200

Schwudke D, Oegema J, Burton L, Entchev E, Hannich JT, Ejsing CS, Kurzchalia T, Shevchenko A: Lipid profiling by multiple precursor and neutral loss scanning driven by the data-dependent acquisition. Anal Chem. 2006, 78: 585-595. 10.1021/ac051605m

McAnoy AM, Wu CC, Murphy RC: Direct qualitative analysis of triacylglycerols by electrospray mass spectrometry using a linear ion trap. J Am Soc Mass Spectrom. 2005, 16: 1498-1509. 10.1016/j.jasms.2005.04.017

Lu Y, Hong S, Tjonahen E, Serhan CN: Mediator-lipidomics: databases and search algorithms for PUFA-derived mediators. J Lipid Res. 2005, 46: 790-802. 10.1194/jlr.D400020-JLR200

Katajamaa M, Oresic M: Processing methods for differential analysis of LC/MS profile data. BMC Bioinformatics. 2005, 6: 179- 10.1186/1471-2105-6-179

Katajamaa M, Miettinen J, Oresic M: MZmine: toolbox for processing and visualization of mass spectrometry based molecular profile data. Bioinformatics. 2006, 22: 634-636. 10.1093/bioinformatics/btk039

Stolt R, Torgrip RJO, Lindberg J, Csenki L, Kolmert J, Schuppe-Koistinen I, Jacobsson SP: Second-order peak detection for multicomponent high-resolution LC/MS data. Anal Chem. 2006, 78: 975-983. 10.1021/ac050980b

Prakash A, Mallick P, Whiteaker J, Zhang H, Paulovich A, Flory M, Lee H, Aebersold R, Schwikowski B: Signal maps for mass spectrometry-based comparative proteomics. Mol Cell Proteomics. 2006, 5: 423-432. 10.1074/mcp.M500133-MCP200

Smilde AK, vanderWerf MJ, Bijlsma S, vanderWerff-vanderVat BJC, Jellema RH: Fusion of mass spectrometry-based metabolomics data. Anal Chem. 2005, 77: 6729-6736. 10.1021/ac051080y

Oresic M, Clish CB, Davidov EJ, Verheij E, Vogels JTWE, Havekes LM, Neumann E, Adourian A, Naylor S, Greef J, Plasterer T: Phenotype characterization using integrated gene transcript, protein and metabolite profiling. Appl Bioinformatics. 2004, 3: 205-217. 10.2165/00822942-200403040-00002

Medina-Gomez G, Virtue S, Lelliott C, Boiani R, Campbell M, Christodoulides C, Perrin C, Jimenez-Linan M, Blount M, Dixon J, Zahn D, Thresher RR, Aparicio S, Carlton M, Colledge WH, Kettunen MI, Seppanen-Laakso T, Sethi JK, O'Rahilly S, Brindle K, Cinti S, Oresic M, Burcelin R, Vidal-Puig A: The link between nutritional status and insulin sensitivity is dependent on the adipocyte-specific Peroxisome Proliferator-Activated Receptor-{gamma}2 isoform. Diabetes. 2005, 54: 1706-1716.

Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M: The KEGG resource for deciphering the genome. Nucl Acids Res. 2004, 32: D277-280. 10.1093/nar/gkh063

Weininger D: Hanbbook of chemoinformatics - from data to knowledge. Edited by: Gasteiger J. 2003, 1: , Wiley-VCH Verlag GmBH & Co.KGaA, Weinheim

Weininger D: SMILES, a chemical language and information system. 1. Introduction to methodology and encoding rules. J Chem Inf Comput Sci. 1988, 28: 31-36. 10.1021/ci00057a005.

Lide DR: CRC Handbook of chemistry and physics. 2004, , CRC Press, 85th

Laaksonen R, Katajamaa M, Päivä H, Sysi-Aho M, Saarinen L, Junni P, Lütjohann D, Smet J, Coster RV, Seppänen-Laakso T, Lehtimäki T, Soini J, Oresic M: A systems biology strategy reveals biological pathways and plasma biomarker candidates for potentially toxic statin induced changes in muscle. PLoS ONE. 2006, 1: e97- 10.1371/journal.pone.0000097

Isotope Pattern Calculator. http://isotopatcalc.sourceforge.net

Camacho D, de la Fuente A, Mendes P: The origin of correlations in metabolomics data. Metabolomics. 2005, 1: 53-63. 10.1007/s11306-005-1107-3.

Kose F, Weckwerth W, Linke T, Fiehn O: Visualizing plant metabolomic correlation network using clique-metabolite matrices. Bioinformatics. 2001, 17: 1198-1208. 10.1093/bioinformatics/17.12.1198

Rischer H, Oresic M, Seppanen-Laakso T, Katajamaa M, Lammertyn F, Ardiles-Diaz W, Van Montagu MCE, Inze D, Oksman-Caldentey KM, Goossens A: Gene-to-metabolite networks for terpenoid indole alkaloid biosynthesis in Catharanthus roseus cells. PNAS. 2006, 103: 5614-5619. 10.1073/pnas.0601027103

Steuer R, Kurths J, Fiehn O, Weckwerth W: Observing and interpreting correlations in metabolomic networks. Bioinformatics. 2003, 19: 1019-1026. 10.1093/bioinformatics/btg120

Gopalacharyulu PV, Lindfors E, Bounsaythip C, Kivioja T, Yetukuri L, Hollmen J, Oresic M: Data integration and visualization system for enabling conceptual biology. Bioinformatics. 2005, 21: i177-185. 10.1093/bioinformatics/bti1015

Adiels M, Packard C, Caslake MJ, Stewart P, Soro A, Westerbacka J, Wennberg B, Olofsson SO, Taskinen MR, Boren J: A new combined multicompartmental model for apolipoprotein B-100 and triglyceride metabolism in VLDL subfractions. J Lipid Res. 2005, 46: 58-67. 10.1194/jlr.M400108-JLR200

Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM: Positional cloning of the mouse obese gene and its human homologue. Nature. 1994, 372: 425-432. 10.1038/372425a0

Browning JD, Horton JD: Molecular mediators of hepatic steatosis and liver injury. J Clin Invest. 2004, 114: 147-152. 10.1172/JCI200422422

Yang SQ, Lin HZ, Lane MD, Clemens M, Diehl AM: Obesity increases sensitivity to endotoxin liver injury: Implications for the pathogenesis of steatohepatitis. PNAS. 1997, 94: 2557-2562. 10.1073/pnas.94.6.2557

Lin HZ, Yang SQ, Chuckaree C, Kuhajda F, Ronnet G, Diehl AM: Metformin reverses fatty liver disease in obese, leptin-deficient mice. Nat Med. 2000, 6: 998-1003. 10.1038/79697

Geladi P, Kowalski BR: Partial least-squares regression: a tutorial. Anal Chim Acta. 1986, 185: 1-17. 10.1016/0003-2670(86)80028-9.

Barker M, Rayens W: Partial least squares for discrimination. J Chemometrics. 2003, 17: 166-173. 10.1002/cem.785.

de Jong S: SIMPLS: An alternative approach to partial least squares regression. Chemometr Intell Lab Syst. 1993, 18: 251-263. 10.1016/0169-7439(93)85002-X.

Pears MR, Cooper JD, Mitchison HM, Mortishire-Smith RJ, Pearce DA, Griffin JL: High resolution 1H NMR-based metabolomics indicates a neurotransmitter cycling deficit in cerebral tissue from a mouse model of Batten Disease. J Biol Chem. 2005, 280: 42508-42514. 10.1074/jbc.M507380200

Brindle JT, Antti H, Holmes E, Tranter G, Nicholson JK, Bethell HWL, Clarke S, Schofield PM, McKilligin E, Mosedale DE, Grainger DJ: Rapid and noninvasive diagnosis of the presence and severity of coronary heart disease using 1H-NMR-based metabonomics. Nat Med. 2002, 8: 1439-1445. 10.1038/nm802

Wise BM, Gallagher NB, Bro R, Shaver JM, Windig W, Koch JS: PLS Toolbox 3.5 for use with Matlab. 2005, Manson, WA, Eigenvector Research Inc.

Summers SA: Ceramides in insulin resistance and lipotoxicity. Prog Lipid Res. 2006, 45: 42-72. 10.1016/j.plipres.2005.11.002

KEGG Glycerolipid Metabolism. http://www.genome.jp/kegg/pathway/map/map00561.html

KEGG Sphingolipid Metabolism. http://www.genome.jp/kegg/pathway/map/map00600.html

ChipperDB: Diabetes Genome Anatomy Project. http://www.diabetesgenome.org/chipperdb/expt.cgi?id=65

Yamashita T, Hashiramoto A, Haluzik M, Mizukami H, Beck S, Norton A, Kono M, Tsuji S, Daniotti JL, Werth N, Sandhoff R, Sandhoff K, Proia RL: Enhanced insulin sensitivity in mice lacking ganglioside GM3. PNAS. 2003, 100: 3445-3449. 10.1073/pnas.0635898100