Quantifying raft proteins in neonatal mouse brain by 'tube-gel' protein digestion label-free shotgun proteomics

Proteome Science

Volumn 5, Issue , 2007, Pages

  Yu, Hongwei ^a   Wakim, Bassam ^a   Li, Man ^a,d   Halligan, Brian ^a   Tint, G Stephen ^b,e   Patel, Shailendra B ^a,c  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c CLEMENT J ZABLOCKI VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d SHANDONG UNIVERSITY   (China)

^e RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ALPHA ENOLASE; CADHERIN; CALCIUM CHANNEL L TYPE; CALPHOBINDIN II; CD47 ANTIGEN; CELL ADHESION MOLECULE; CLATHRIN HEAVY CHAIN; CONTACTIN; DETERGENT; GLYPICAN; GLYPICAN 1; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; LIPOCORTIN 5; LYMPHOCYTE ANTIGEN; MEMBRANE PROTEIN; NERVE CELL ADHESION MOLECULE; NEUROMODULIN; PHOSPHOPROTEIN; POLYACRYLAMIDE; PROTEIN KINASE FYN; RAS PROTEIN; STATHMIN; SYNAPTOBREVIN 2; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNAPTOTAGMIN; SYNTAXIN 1A; TRITON X 100;

ACCURACY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; HYDROPHOBICITY; LIPID RAFT; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MATERIALS HANDLING; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PREDICTION; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN PURIFICATION; PROTEOMICS; QUANTITATIVE ANALYSIS; REPRODUCIBILITY; TANDEM MASS SPECTROMETRY; UNINDEXED SEQUENCE;

EID: 35648988480     PISSN: None     EISSN: 14775956     Source Type: Journal    
DOI: 10.1186/1477-5956-5-17     Document Type: Article

References (77)

1. Brown DA Lipid rafts, detergent-resistant membranes, and raft targeting signals Physiology (Bethesda) 2006, 21:430-439. 17119156
2. Allen JA Halverson-Tamboli RA Rasenick MM Lipid raft microdomains and neurotransmitter signalling Nat Rev Neurosci 2007, 8:128-140. 10.1038/ nrn2059 17195035
3. Pike LJ Lipid rafts: Heterogeneity on the high seas Biochem J 2004, 378:281-292. 1223991 14662007 10.1042/BJ20031672
4. Simons K Ehehalt R Cholesterol, lipid rafts, and disease J Clin Invest 2002, 110:597-603. 151114 12208858 10.1172/JCI200216390
5. Simons K Vaz WL Model systems, lipid rafts, and cell membranes Annu Rev Biophys Biomol Struct 2004, 33:269-295. 10.1146/ annurev.biophys.32.110601.141803 15139814
6. Blonder J Hale ML Lucas DA Schaefer CF Yu LR Conrads TP Issaq HJ Stiles BG Veenstra TD Proteomic analysis of detergent-resistant membrane rafts Electrophoresis 2004, 25:1307-1318. 10.1002/elps.200405891 15174053
7. Martosella J Zolotarjova N Liu H Moyer SC Perkins PD Boyes BE High recovery HPLC separation of lipid rafts for membrane proteome analysis J Proteome Res 2006, 5:1301-1312. 10.1021/pr060051g 16739982
8. Magee AI Parmryd I Detergent-resistant membranes and the protein composition of lipid rafts Genome Biol 2003, 4:234. 329107 14611651 10.1186/gb-2003-4-11-234
9. MacLellan DL Steen H Adam RM Garlick M Zurakowski D Gygi SP Freeman MR Solomon KR A quantitative proteomic analysis of growth factor-induced compositional changes in lipid rafts of human smooth muscle cells Proteomics 2005, 5:4733-4742. 10.1002/pmic.200500044 16267816
10. Elortza F Nuhse TS Foster LJ Stensballe A Peck SC Jensen ON Proteomic analysis of glycosylphosphatidylinositol-anchored membrane proteins Mol Cell Proteomics 2003, 2:1261-1270. 10.1074/mcp.M300079-MCP200 14517339
11. Foster LJ De Hoog CL Mann M Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors Proc Natl Acad Sci U S A 2003, 100:5813-5818. 156283 12724530 10.1073/pnas.0631608100
12. Gupta N Wollscheid B Watts JD Scheer B Aebersold R DeFranco AL Quantitative proteomic analysis of B cell lipid rafts reveals that ezrin regulates antigen receptor-mediated lipid raft dynamics Nat Immunol 2006, 7:625-633. 10.1038/ni1337 16648854
13. Jia JY Lamer S Schumann M Schmidt MR Krause E Haucke V Quantitative proteomics analysis of detergent-resistant membranes from chemical synapses: Evidence for cholesterol as spatial organizer of synaptic vesicle cycling Mol Cell Proteomics 2006, 5:2060-2071. 10.1074/ mcp.M600161-MCP200 16861260
14. Sprenger RR Horrevoets AJ Proteomic study of caveolae and rafts isolated from human endothelial cells Methods Mol Biol 2007, 357:199-213. 17172689
15. Lu X Zhu H Tube-gel digestion: A novel proteomic approach for high throughput analysis of membrane proteins Mol Cell Proteomics 2005, 4:1948-1958. 1360194 16150870 10.1074/mcp.M500138-MCP200
16. Ishmael JE Safic M Amparan D Vogel WK Pham T Marley K Filtz TM Maier CS Nonmuscle myosins II-B and Va are components of detergent-resistant membrane skeletons derived from mouse forebrain Brain Res 2007, 1143:46-59. 10.1016/j.brainres.2007.01.061 17321505
17. Kim KB Lee JW Lee CS Kim BW Choo HJ Jung SY Chi SG Yoon YS Yoon G Ko YG Oxidation-reduction respiratory chains and ATP synthase complex are localized in detergent-resistant lipid rafts Proteomics 2006, 6:2444-2453. 10.1002/pmic.200500574 16526083
18. Kisby GE Standley M Park T Olivas A Fei S Jacob T Reddy A Lu X Pattee P Nagalla SR Proteomic analysis of the genotoxicant methylazoxymethanol (MAM)-induced changes in the developing cerebellum J Proteome Res 2006, 5:2656-2665. 10.1021/pr060126g 17022636
19. Sheikh AM Barrett C Villamizar N Alzate O Miller S Shelburne J Lodge A Lawson J Jaggers J Proteomics of cerebral injury in a neonatal model of cardiopulmonary bypass with deep hypothermic circulatory arrest J Thorac Cardiovasc Surg 2006, 132:820-828. 10.1016/j.jtcvs.2006.07.002 17000293
20. Spitzer AR Chace D Mass spectrometry in neonatal medicine and clinical diagnosis - the [corrected] potential use of mass spectrometry in neonatal brain [corrected] monitoring Clin Perinatol 2006, 33:729-44, viii. 10.1016/j.clp.2006.06.005 16950322
21. Yang ZJ Appleby VJ Coyle B Chan WI Tahmaseb M Wigmore PM Scotting PJ Novel strategy to study gene expression and function in developing cerebellar granule cells J Neurosci Methods 2004, 132:149-160. 10.1016/ j.jneumeth.2003.09.031 14706712
22. Kovacs WJ Shackelford JE Tape KN Richards MJ Faust PL Fliesler SJ Krisans SK Disturbed cholesterol homeostasis in a peroxisome-deficient PEX2 knockout mouse model Mol Cell Biol 2004, 24:1-13. 303355 14673138 10.1128/MCB.24.1.1-13.2004
23. Edison R Muenke M The interplay of genetic and environmental factors in craniofacial morphogenesis: Holoprosencephaly and the role of cholesterol Congenit Anom (Kyoto) 2003 43 1 21 12692399
24. Nissenkorn A Michelson M Ben-Zeev B Lerman-Sagie T Inborn errors of metabolism: A cause of abnormal brain development Neurology 2001, 56:1265-1272. 11383558
25. FitzPatrick DR Keeling JW Evans MJ Kan AE Bell JE Porteous ME Mills K Winter RM Clayton PT Clinical phenotype of desmosterolosis Am J Med Genet 1998, 75:145-152. 10.1002/ (SICI)1096-8628(19980113)75:2<145::AID-AJMG5>3.0.CO;2-S 9450875
26. Opitz JM de la Cruz F Cholesterol metabolism in the RSH/ Smith-Lemli-Opitz syndrome: Summary of an NICHD conference Am J Med Genet 1994, 50:326-338. 10.1002/ajmg.1320500406 7632194
27. Powers JM Tummons RC Moser AB Moser HW Huff DS Kelley RI Neuronal lipidosis and neuroaxonal dystrophy in cerebro-hepato-renal (Zellweger) syndrome Acta Neuropathol (Berl) 1987, 73:333-343. 10.1007/BF00688256 3618126
28. Li N Shaw AR Zhang N Mak A Li L Lipid raft proteomics: Analysis of in-solution digest of sodium dodecyl sulfate-solubilized lipid raft proteins by liquid chromatography-matrix-assisted laser desorption/ ionization tandem mass spectrometry Proteomics 2004, 4:3156-3166. 10.1002/pmic.200400832 15378691
29. Old WM Meyer-Arendt K Aveline-Wolf L Pierce KG Mendoza A Sevinsky JR Resing KA Ahn NG Comparison of label-free methods for quantifying human proteins by shotgun proteomics Mol Cell Proteomics 2005, 4:1487-1502. 10.1074/mcp.M500084-MCP200 15979981
30. Mukherjee A Arnaud L Cooper JA Lipid-dependent recruitment of neuronal Src to lipid rafts in the brain J Biol Chem 2003, 278:40806-40814. 10.1074/jbc.M306440200 12912979
31. Melkonian KA Ostermeyer AG Chen JZ Roth MG Brown DA Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated J Biol Chem 1999, 274:3910-3917. 10.1074/jbc.274.6.3910 9920947
32. Santoni V Molloy M Rabilloud T Membrane proteins and proteomics: Un amour impossible? Electrophoresis 2000, 21:1054-1070. 10.1002/ (SICI)1522-2683(20000401)21:6<1054::AID-ELPS1054>3.0.CO;2-8 10786880
33. Blonder J Chan KC Issaq HJ Veenstra TD Identification of membrane proteins from mammalian cell/tissue using methanol-facilitated solubilization and tryptic digestion coupled with 2D-LC-MS/MS Nat Protoc 2006, 1:2784-2790. 10.1038/nprot.2006.359 17406535
34. States DJ Omenn GS Blackwell TW Fermin D Eng J Speicher DW Hanash SM Challenges in deriving high-confidence protein identifications from data gathered by a HUPO plasma proteome collaborative study Nat Biotechnol 2006, 24:333-338. 10.1038/nbt1183 16525410
35. Elmariah SB Hughes EG Oh EJ Balice-Gordon RJ Neurotrophin signaling among neurons and glia during formation of tripartite synapses Neuron Glia Biol 2005, 1:1-11. 1397704 16528404 10.1017/S1740925X05000189
36. Foty RA Steinberg MS Cadherin-mediated cell-cell adhesion and tissue segregation in relation to malignancy Int J Dev Biol 2004, 48:397-409. 10.1387/ijdb.041810rf 15349815
37. Scheiffele P Cell-cell signaling during synapse formation in the CNS Annu Rev Neurosci 2003, 26:485-508. 10.1146/ annurev.neuro.26.043002.094940 12626697
38. Fetissov SO Bergstrom U Johansen JE Hokfelt T Schalling M Ranscht B Alterations of arcuate nucleus neuropeptidergic development in contactin-deficient mice: Comparison with anorexia and food-deprived mice Eur J Neurosci 2005, 22:3217-3228. 10.1111/j.1460-9568.2005.04513.x 16367788
39. Yang JW Rodrigo R Felipo V Lubec G Proteome analysis of primary neurons and astrocytes from rat cerebellum J Proteome Res 2005, 4:768-788. 10.1021/pr049774v 15952724
40. Dremina ES Sharov VS Schoneich C Protein tyrosine nitration in rat brain is associated with raft proteins, flotillin-1 and alpha-tubulin: Effect of biological aging J Neurochem 2005, 93:1262-1271. 10.1111/ j.1471-4159.2005.03115.x 15934946
41. Head BP Patel HH Roth DM Murray F Swaney JS Niesman IR Farquhar MG Insel PA Microtubules and actin microfilaments regulate lipid raft/caveolae localization of adenylyl cyclase signaling components J Biol Chem 2006, 281:26391-26399. 10.1074/jbc.M602577200 16818493
42. Chen S Bawa D Besshoh S Gurd JW Brown IR Association of heat shock proteins and neuronal membrane components with lipid rafts from the rat brain J Neurosci Res 2005, 81:522-529. 10.1002/jnr.20575 15948182
43. Say YH Hooper NM Contamination of nuclear fractions with plasma membrane lipid rafts Proteomics 2007, 7:1059-1064. 10.1002/pmic.200600849 17351887
44. Bae TJ Kim MS Kim JW Kim BW Choo HJ Lee JW Kim KB Lee CS Kim JH Chang SY Kang CY Lee SW Ko YG Lipid raft proteome reveals ATP synthase complex in the cell surface Proteomics 2004, 4:3536-3548. 10.1002/pmic.200400952 15378739
45. Igbavboa U Eckert GP Malo TM Studniski AE Johnson LN Yamamoto N Kobayashi M Fujita SC Appel TR Muller WE Wood WG Yanagisawa K Murine synaptosomal lipid raft protein and lipid composition are altered by expression of human apoE 3 and 4 and by increasing age J Neurol Sci 2005, 229-230: 225-232. 10.1016/j.jns.2004.11.037 15760644
46. Thouvenot E Lafon-Cazal M Demettre E Jouin P Bockaert J Marin P The proteomic analysis of mouse choroid plexus secretome reveals a high protein secretion capacity of choroidal epithelial cells Proteomics 2006, 6:5941-5952. 10.1002/pmic.200600096 17051638
47. Pelkmans L Puntener D Helenius A Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae Science 2002, 296:535-539. 10.1126/science.1069784 11964480
48. Chang L Goldman RD Intermediate filaments mediate cytoskeletal crosstalk Nat Rev Mol Cell Biol 2004, 5:601-613. 10.1038/nrm1438 15366704
49. Franzen R Tanner SL Dashiell SM Rottkamp CA Hammer JA Quarles RH Microtubule-associated protein 1B: A neuronal binding partner for myelin-associated glycoprotein J Cell Biol 2001, 155:893-898. 10.1083/ jcb.200108137 11733546
50. Fu H Subramanian RR Masters SC 14-3-3 proteins: Structure, function, and regulation Annu Rev Pharmacol Toxicol 2000, 40:617-647. 10.1146/ annurev.pharmtox.40.1.617 10836149
51. Watson K Edwards RJ Shaunak S Parmelee DC Sarraf C Gooderham NJ Davies DS Extra-nuclear location of histones in activated human peripheral blood lymphocytes and cultured T-cells Biochem Pharmacol 1995, 50:299-309. 10.1016/0006-2952(95)00142-M 7646532
52. Lawen A Ly JD Lane DJ Zarschler K Messina A De Pinto V Voltage-dependent anion-selective channel 1 (VDAC1) - a mitochondrial protein, rediscovered as a novel enzyme in the plasma membrane Int J Biochem Cell Biol 2005, 37:277-282. 10.1016/j.biocel.2004.05.013 15474974
53. Andreev VP Li L Cao L Gu Y Rejtar T Wu SL Karger BL A New Algorithm Using Cross-Assignment for Label-Free Quantitation with LC-LTQ-FT MS J Proteome Res 2007. 17441747
54. Wienkoop S Larrainzar E Niemann M Gonzalez EM Lehmann U Weckwerth W Stable isotope-free quantitative shotgun proteomics combined with sample pattern recognition for rapid diagnostics J Sep Sci 2006, 29:2793-2801. 10.1002/jssc.200600290 17305241
55. Le Bihan T Goh T Stewart Salter AM Bukhman YV Dharsee M Ewing R Wisniewski JR Differential analysis of membrane proteins in mouse fore- and hindbrain using a label-free approach J Proteome Res 2006, 5:2701-2710. 10.1021/pr060190y 17022641
56. Wang G Wu WW Zeng W Chou CL Shen RF Label-free protein quantification using LC-coupled ion trap or FT mass spectrometry: Reproducibility, linearity, and application with complex proteomes J Proteome Res 2006. 5:1214-1223. 10.1021/pr050406g 16674111
57. Ru QC Zhu LA Silberman J Shriver CD Label-free semiquantitative peptide feature profiling of human breast cancer and breast disease sera via two-dimensional liquid chromatography-mass spectrometry Mol Cell Proteomics 2006, 5:1095-1104. 10.1074/mcp.M500387-MCP200 16546996
58. Cui XY Hu QD Tekaya M Shimoda Y Ang BT Nie DY Sun L Hu WP Karsak M Duka T Takeda Y Ou LY Dawe GS Yu FG Ahmed S Jin LH Schachner M Watanabe K Arsenijevic Y Xiao ZC NB-3/Notch1 pathway via Deltex1 promotes neural progenitor cell differentiation into oligodendrocytes J Biol Chem 2004, 279:25858-25865. 10.1074/jbc.M313505200 15082708
59. Brady ST Lasek RJ Nerve-specific enolase and creatine phosphokinase in axonal transport: Soluble proteins and the axoplasmic matrix Cell 1981, 23:515-523. 10.1016/0092-8674(81)90147-1 6162572
60. Deininger SO Rajendran L Lottspeich F Przybylski M Illges H Stuermer CA Reuter A Identification of teleost Thy-1 and association with the microdomain/lipid raft reggie proteins in regenerating CNS axons Mol Cell Neurosci 2003, 22:544-554. 10.1016/S1044-7431(03)00028-9 12727449
61. Hu QD Ang BT Karsak M Hu WP Cui XY Duka T Takeda Y Chia W Sankar N Ng YK Ling EA Maciag T Small D Trifonova R Kopan R Okano H Nakafuku M Chiba S Hirai H Aster JC Schachner M Pallen CJ Watanabe K Xiao ZC F3/contactin acts as a functional ligand for Notch during oligodendrocyte maturation Cell 2003, 115:163-175. 10.1016/S0092-8674(03)00810-9 14567914
62. Guirland C Suzuki S Kojima M Lu B Zheng JQ Lipid rafts mediate chemotropic guidance of nerve growth cones Neuron 2004, 42:51-62. 10.1016/S0896-6273(04)00157-6 15066264
63. Kashihara M Miyata S Kumanogoh H Funatsu N Matsunaga W Kiyohara T Sokawa Y Maekawa S Changes in the localization of NAP-22, a calmodulin binding membrane protein, during the development of neuronal polarity Neurosci Res 2000, 37:315-325. 10.1016/S0168-0102(00)00132-2 10958980
64. Leshchyns'ka I Sytnyk V Morrow JS Schachner M Neural cell adhesion molecule (NCAM) association with PKCbeta2 via betaI spectrin is implicated in NCAM-mediated neurite outgrowth J Cell Biol 2003, 161:625-639. 10.1083/jcb.200303020 12743109
65. Maekawa S Morii H Kumanogoh H Sano M Naruse Y Sokawa Y Mori N Localization of neuronal growth-associated, microtubule-destabilizing factor SCG10 in brain-derived raft membrane microdomains J Biochem (Tokyo) 2001, 129:691-697. 11328590
66. Miyata S Funatsu N Matsunaga W Kiyohara T Sokawa Y Maekawa S Expression of the IgLON cell adhesion molecules Kilon and OBCAM in hypothalamic magnocellular neurons J Comp Neurol 2000, 424:74-85. 10.1002/ 1096-9861(20000814)424:1<74::AID-CNE6>3.0.CO;2-5 10888740
67. Roussel G Nussbaum F Schoentgen F Jolles P Nussbaum JL Immunological investigation of a 21-kilodalton cytosolic basic protein in rat brain Dev Neurosci 1988, 10:65-74. 3402357
68. Schaeren-Wiemers N Bonnet A Erb M Erne B Bartsch U Kern F Mantei N Sherman D Suter U The raft-associated protein MAL is required for maintenance of proper axon - glia interactions in the central nervous system J Cell Biol 2004, 166:731-742. 10.1083/jcb.200406092 15337780
69. Schlicht K Buttner A Siedler F Scheffer B Zill P Eisenmenger W Ackenheil M Bondy B Comparative proteomic analysis with postmortem prefrontal cortex tissues of suicide victims versus controls J Psychiatr Res 2007, 41:493-501. 10.1016/j.jpsychires.2006.04.006 16750834
70. Yanagisawa M Nakamura K Taga T Roles of lipid rafts in integrin-dependent adhesion and gp130 signalling pathway in mouse embryonic neural precursor cells Genes Cells 2004, 9:801-809. 10.1111/ j.1365-2443.2004.00764.x 15330857
71. Yang JW Suder P Silberring J Lubec G Proteome analysis of mouse primary astrocytes Neurochem Int 2005, 47:159-172. 10.1016/j.neuint.2005.04.017 15908045
72. Schirle M Heurtier MA Kuster B Profiling core proteomes of human cell lines by one-dimensional PAGE and liquid chromatography-tandem mass spectrometry Mol Cell Proteomics 2003, 2:1297-1305. 10.1074/ mcp.M300087-MCP200 14532353
73. Yu H Li M Tint GS Chen J Xu G Patel SB Selective reconstitution of liver cholesterol biosynthesis promotes lung maturation but does not prevent neonatal lethality in Dhcr7 null mice BMC Dev Biol 2007, 7:27. 1855921 17408495 10.1186/1471-213X-7-27
74. Hicks WA Halligan BD Slyper RY Twigger SN Greene AS Olivier M Simultaneous quantification and identification using 18O labeling with an ion trap mass spectrometer and the analysis software application "ZoomQuant" J Am Soc Mass Spectrom 2005, 16:916-925. 10.1016/ j.jasms.2005.02.024 15907706
75. Mirza SP Halligan BD Greene AS Olivier M An improved method for the analysis of membrane proteins by mass spectrometry Physiol Genomics 2007. 17341690
76. Halligan BD Slyper RY Twigger SN Hicks W Olivier M Greene AS ZoomQuant: an application for the quantitation of stable isotope labeled peptides J Am Soc Mass Spectrom 2005, 16:302-306. 10.1016/j.jasms.2004.11.014 15734322
77. Bielawski J Szulc ZM Hannun YA Bielawska A Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry Methods 2006, 39:82-91. 10.1016/ j.ymeth.2006.05.004 16828308