Application of proteomics to neutrophil biology

Journal of Proteomics

Volumn 73, Issue 3, 2010, Pages 552-561

  Luerman, Gregory C ^a   Uriarte, Silvia M ^b   Rane, Madhavi J ^a,b   McLeish, Kenneth R ^a,b,c  

^a UNIVERSITY OF LOUISVILLE   (United States)

^b University of Louisville School of Medicine   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Inflammation; Neutrophils; Signal transduction

Indexed keywords

HUMAN; INFLAMMATION; LEUKOCYTE ACTIVATION; LIQUID CHROMATOGRAPHY; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEOMICS; REVIEW; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

CELL BIOLOGY; HUMANS; INFLAMMATION; NEUTROPHIL ACTIVATION; NEUTROPHILS; PROTEOMICS;

EID: 72149115656     PISSN: 18743919     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jprot.2009.06.013     Document Type: Review

References (80)

1. Hidalgo A., Chang J., Jang J.E., Peired A.J., Chiang E.Y., and Frenette P.S. Heterotypic interactions enabled by polarized neutrophil microdomains mediate thromboinflammatory injury. Nat Med 15 (2009) 384-391
2. Smith C.W. Leukocyte-endothelial cell interactions. Semin Hematol 30 (1993) 45-53
3. Zarbock A., and Ley K. Mechanisms and consequences of neutrophil interaction with the endothelium. Am J Pathol 172 (2008) 1-7
4. Yang J., Hirata T., Croce K., Merrill-Skoloff G., Tchernychev B., Williams E., et al. Targeted gene disruption demonstrates that P-selectin glycoprotein ligand 1 (PSGL-1) is required for P-selectin-mediated but not E-selectin-mediated neutrophil rolling and migration. J Exp Med 190 (1999) 1769-1792
5. Burns A.R., Bowden R.A., MacDonell S.D., Walker D.C., Odebunmi T.O., Donnachie E.M., et al. Analysis of tight junctions during neutrophil transendothelial migration. J Cell Sci 113 (2000) 45-57
6. Ley K., Laudanna C., Cybulsky M.I., and Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 7 (2007) 678-689
7. Dias-Baruffi M., Roque-Barreira M.C., Cunha F.Q., and Ferreira S.H. Biological characterization of purified macrophage-derived neutrophil chemotactic factor. Mediat Inflamm 4 (1995) 263-269
8. Mansfield P.J., and Suchard S.J. Thrombospondin promotes both chemotaxis and haptotaxis in neutrophil-like HL-60 cells. J Immunol 150 (1993) 1959-1970
9. Allen L.A., and Aderem A. Molecular definition of distinct cytoskeletal structures involved in complement- and Fc receptor-mediated phagocytosis in macrophages. J Exp Med 184 (1996) 627-637
10. Sengeløv H., Kjeldsen L., and Borregaard N. Control of exocytosis in early neutrophil activation. J Immunol 150 (1993) 1535-1543
11. Sengeløv H., Follin P., Kjeldsen L., Lollike K., Dahlgren C., and Borregaard N. Mobilization of granules and secretory vesicles during in vivo exudation of human neutrophils. J. Immunol. 154 (1995) 4157-4165
12. Evans T.J., Buttery L.D.K., Carpenter A., Springall D.R., Polak J.M., and Cohen J. Cytokine-treated human neutrophils contain inducible nitric oxide synthase that produces nitration of ingested bacteria. Proc Natl Acad Sci USA 93 (1995) 9553-9558
13. Segal T. How neutrophils kill microbes. Annu Rev Immunol 23 (2005) 197-223
14. Levy B.D., Clish C.B., Schmidt B., Gronert K., and Serhan C.N. Lipid mediator class switching during acute inflammation: signals in resolution. Nat Immunol 2 (2001) 612-619
15. Mulligan M.S., Warner R.L., Foreback J.L., Shanley T.P., and Ward P.A. Protective effects of IL-4, IL-1 0, IL-12, and IL-13 in IgG immune complex-induced lung injury. J Immunol 159 (1997) 3483-3489
16. Ariel A., and Serhan C.N. Resolvins and protectins in the termination program of acute inflammation. TRENDS Immunol 28 (2007) 176-182
17. Serhan C.N., Hong S., Gronert K., Colgan S.P., Devchand P.R., Mirick G., et al. Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med 196 (2002) 1025-1037
18. Kobayashi S.D., Voyich J.M., Burlak C., and DeLeo F.R. Neutrophils in the innate immune response. Arch Immunol Ther Exp 53 (2005) 505-517
19. Dransfield I., and Rossi A.G. Granulocyte apoptosis: who would work with a 'real' inflammatory cell?. Biochem Soc Trans 32 (2004) 447-451
20. Kantari C, Pederzoli-Ribeil M, Witko-Sarsat V. The role of neutrophils and monocytes in innate immunity. Contrib Microbiol 2008;15:118-46 submitted for publication.
21. Serhan C.N., and Savill J. Resolution of inflammation: the beginning programs the end. Nat Immunol 6 (2005) 1191-1196
22. Krishnan J., Selvarajoo K., Tsuchiya M., Lee G., and Choi S. Toll-like receptor signal transduction. Exp Mol Med 39 (2007) 421-438
23. Abram C.L., and Lowell C.A. The ins and outs of leukocyte integrin signaling. Annu Rev Immunol 27 (2009) 339-362
24. Ibarrola I., Vossebeld P.J., Homburg C.H., Thelen M., Roos D., and Verhoeven A.J. Influence of tyrosine phosphorylation on protein interaction with FcgammaRIIa. Biochem Biophys Acta 1357 (1997) 348-358
25. Forsberg M., Druid P., Zheng L., Stendahl O., and Sarndahl E. Activation of Rac2 and Cdc42 on Fc and complement receptor ligation in human neutrophils. J Leukoc Biol 74 (2003) 611-619
26. Pacquelet S., Johnson J.L., Ellis B.A., Brzezinska A.A., Lane W.S., Munafo D.B., et al. Cross-talk between IRAK-4 and the NADPH oxidase. Biochem J 403 (2007) 451-461
27. McLeish K.R., Knall C., Ward R.A., Gerwins P., Coxon P.Y., Klein J.B., et al. Activation of mitogen-activated protein kinase cascades during priming of human neutrophils by TNF-alpha and GM-CSF. J Leukoc Biol 64 (1998) 537-545
28. Ward R.A., Nakamura M., and McLeish K.R. Priming of the neutrophil respiratory burst involves p38 mitogen-activated protein kinase-dependent exocytosis of flavocytochrome b558-containing granules. J Biol Chem 275 (2000) 36713-36719
29. Brown G.E., Stewart M.Q., Bissonnette S.A., Elia A.E., Wilker E., and Yaffe M.B. Distinct ligand-dependent roles for p38 MAPK in priming and activation of the neutrophil NADPH oxidase. J Biol Chem 279 (2004) 27059-27068
30. Zu Y.L., Gilchrist A., Fernandex G.A., Vazquez-Abad D., Kreutzer D.L., Huang C.K., et al. p38 mitogen-activated protein kinase activation is required for human neutrophil function triggered by TNF-alpha or FMLF stimulation. J Immunol 160 (1998) 1982-1989
31. Aoshiba K., Yasui S., Hayashi M., Tamaoki J., and Nagai A. Role of p38-mitogen-activated protein kinase in spontaneous apoptosis of human neutrophils. J Immunol 162 (1999) 1692-1700
32. Rane M.J., Coxon P.Y., Powell D.W., Webster R., Klein J.B., Pierce W., et al. p38 Kinase-dependent MAPKAPK-2 activation functions as 3-phosphoinositide-dependent kinase-2 for Akt in human neutrophils. J Biol Chem 276 (2001) 3517-3523
33. Rane M.J., Pan Y., Singh S., Powell D.W., Wu R., Cummins T.D., et al. Heat shock protein 27 controls apoptosis by regulating Akt activation. J Biol Chem 278 (2003) 27828-27835
34. Wu R., Kausar H., Johnson P., Montoya-Durango D.E., Merchant M., and Rane M.J. Hsp27 regulates Akt activation and polymorphonuclear leukocyte apoptosis by scaffolding MK2 to Akt signal complex. J Biol Chem 282 (2007) 21598-21608
35. Fessler M.B., Malcolm K.C., Duncan M.W., and Worthen G.S. Lipopolysaccharide stimulation of the human neutrophil: an analysis of changes in gene transcription and protein expression by oligonucleotide microarrays and proteomics. Chest 131 (2002) 75S-76S
36. Lian Z., Wang L., Yamaga S., Bonds W., Beazer-Barclay Y., Kluger Y., et al. Genomic and proteomic analysis of the myeloid differentiation program. Blood 98 (2001) 513-524
37. Piubelli C., Galvani M., Hamdam M., Domenici E., and Righetti P.G. Proteome analysis of rat polymorphonuclear leukocytes: a two-dimensional electrophoresis/mass spectrometry approach. Electrophoresis 23 (2002) 298-310
38. Lippolis J.D., and Reinhardt T.A. Proteomic survey of bovine neutrophils. Vet Immunol Immunopath 103 (2005) 53-65
39. Lominadze G., Powell D.W., Luerman G.C., Link A.J., Ward R.A., and McLeish K.R. Proteomic analysis of human neutrophil granules. Mol Cell Proteom. 4 (2005) 1503-1521
40. Feuk-Lagerstedt E., Movitz C., Pellmé S., Dahlgren C., and Karlsson A. Lipid raft proteome of the human neutrophil azurophil granule. Proteomics 7 (2007) 194-205
41. Nebl T., Pestonjamasp K.N., Leszyk J.D., Crowley J.L., Oh S.W., and Luna E.J. Proteomic analysis of a detergent-resistant membrane skeleton from neutrophil plasma membranes. J Biol Chem 277 (2002) 43399-43409
42. Jethwaney D., Islam M.R., Leidal K.G., de Bernabe D.B., Cambell K.P., Nauseef W.M., et al. Proteomic analysis of plasma membrane and secretory vesicles from human neutrophils. Proteome Sci 10 (2007) 12
43. Uriarte S.M., Powell D.W., Luerman G.C., Merchant M.L., Cummins T.D., Jog N.R., et al. Comparison of proteins expressed on secretory vesicle membranes and plasma membranes of human neutrophils. J Immunol 180 (2008) 5575-5581
44. Fischer F., Wolters D., Rögner M., and Poetsch A. Toward the complete membrane proteome: high coverage of integral membrane proteins through transmembrane peptide detection. Mol Cell Proteomics 5 (2006) 444-453
45. Burlak C.B., Whitney A.R., Mead D.J., Hackstadt T., and DeLeo F.R. Maturation of human neutrophil phagosomes includes incorporation of molecular chaperones and endoplasmic reticulum quality control machinery. Mol Cell Proteom 5 (2006) 620-634
46. Desjardins M. ER-mediated phagocytosis: a new membrane for new functions. Nat Rev Immunol 3 (2003) 280-291
47. Jutras I., Houde M., Currier N., Boulais J., Duclos S., LaBoissière S., et al. Modulation of the phagosome proteome by interferon-gamma. Mol Cell Proteom 7 (2008) 697-715
48. Burlak C., Whitney A.R., Mead D.J., Hackstadt T., and DeLeo F.R. Maturation of human neutrophil phagosomes includes incorporation of molecular chaperones and endoplasmic reticulum quality control machinery. Mol Cell Proteom 5 (2006) 620-634
49. Garin J., Diez R., Kieffer S., Dermine J.F., Duclos S., Gagnon E., et al. The phagosome proteome: insight into phagosome functions. J Cell Biol 152 (2001) 165-180
50. Xu P., Crawford M., Way M., Godovac-Zimmermann J., Segal A.W., and Radulovic M. Subproteome analysis of the neutrophil cytoskeleton. Proteomics 9 (2009)
51. Shimada S., Nakamura M., Tanaka Y., Tsutsumi K., Katano M., Masuko K., et al. Crosslinking of the CD69 molecule enhances S100A9 production in activated neutrophils. Microbiol Immunol 51 (2007) 87-98
52. Fessler M.B., Malcolm K.C., Duncan M.W., and Worthen G.S. A genomic and proteomic analysis of activation of the human neutrophil by lipopolysaccharide and its mediation by p38 mitogen-activated protein kinase. J Biol Chem. 277 (2002) 31291-31302
53. Serhan C.N., Clish C.B., Brannon J., Colgan S.P., Chiang N., and Gronert K. Novel functional sets of lipid-derived mediators with antiinflammatory actions generated from omega-3 fatty acids via cyclooxygenase 2-nonsteroidal antiinflammatory drugs and transcellular processing. J Exp Med 2000 8 (2000) 1197-1204
54. Lu Y., Song H., Gotlinger K., and Serhan C.N. Lipid mediator informatics and proteomics in inflammation resolution. Sci World J 6 (2006) 589-614
55. Haas-Stapleton E.J., Lu Y., Hong S., Arita M., Favoreto S., Nigam S., et al. Candida albicans modulates host defense by biosynthesizing the pro-resolving mediator resolvin E1. PLoS ONE 2 (2007) e1316
56. Ohira T., Bannenberg G., Arita M., Takahashi M., Ge Q., VanDyke T.E., et al. A stable aspirin-triggered lipoxin A4 analog blocks phosphorylation of leukocyte-specific protein 1 in human neutrophils. J Immunol 173 (2004) 2091-2098
57. Greenlee K.J., Corry D.B., Engler D.A., Matsunami R.K., Tessier P., Cook R.G., et al. Proteomic identification of in vivo substrates for matrix metalloproteinases 2 and 9 reveals a mechanism for resolution of inflammation. J Immunol 177 (2006) 7312-7321
58. Gardiner E.M., Pestonjamasp K.N., Bohl B.P., Chamberlain C., Hahn K.M., and Bokoch G.M. Spatial and temporal analysis of Rac activation during live neutrophil chemotaxis. Curr Biol 12 (2002) 2029-2034
59. Johnson J.L., Ellis B.A., Munafo D.B., Brzezinska A.A., and Catz S.D. Gene transfer and expression in human neutrophils. The phox homology domain of p47phox translocates to the plasma membrane but not to the membrane of mature phagosomes. BMC Immunol 7 (2006) 28
60. Rane M.J., Gozal D., Butt W., Gozal E., Pierce Jr. W.M., Guo S.Z., et al. Gamma-amino butyric acid type B receptors stimulate neutrophil chemotaxis during ischemia-reperfusion. J Immunol 174 (2005) 7242-7249
61. Kim Y.H., Kim Y.S., Park C.H., Chung I.Y., Yoo J.M., Kim J.G., et al. Protein kinase C-delta mediates neuronal apoptosis in the retinas of diabetic rats via the Akt signaling pathway. Diabetes 57 (2008) 2181-2190
62. Taylor R.M., Baniulis D., Burritt J.B., Gripentrog J.M., Lord C.I., Riesselman M.H., et al. Analysis of human phagocyte flavocytochrome b(558) by mass spectrometry. J Biol Chem 281 (2006) 37045-37056
63. Manning G., Whyte D.B., Martinez R., Hunter T., and Sudarsanam S. The protein kinase complement of the human genome. Science 298 (2002) 1912-1934
64. Powell D.W., Rane M.J., Joughin B.A., Kalmukova R., Hong J.H., and Tidor B. Proteomic identification of 14-3-3zeta as a mitogen-activated protein kinase-activated protein kinase 2 substrate: role in dimer formation and ligand binding. Mol Cell Biol 23 (2003) 5376
65. Singh S., Powell D.W., Rane M.J., Millard T.H., Trent J.O., Pierce W.M., et al. Identification of the p16-Arc subunit of the Arp 2/3 complex as a substrate of MAPK-activated protein kinase 2 by proteomic analysis. J Biol Chem 278 (2003) 36410-36417
66. Lominadze G., Rane M.J., Merchant M., Cai J., Ward R.A., and McLeish K.R. Myeloid-related protein-14 is a p38 MAPK substrate in human neutrophils. J Immunol 174 (2005) 7257-7267
67. Kettritz R., Xu Y.X., Faass B., Klein J.B., Müller E.C., Otto A., et al. TNF-α-mediated neutrophil apoptosis involves Ly-GDI, a Rho GTPase regulator. J Leukoc Biol 68 (2000) 277-283
68. Boldt K., Rist W., Weiss S.M., Weith A., and Lenter M.C. FPRL-1 induces modifications of migration-associated proteins in human neutrophils. Proteomics 6 (2006) 4790-4799
69. Dang P.M., Stensballe A., Boussetta T., Raad H., Dewas C., Kroviarski Y., et al. A specific p47phox -serine phosphorylated by convergent MAPKs mediates neutrophil NADPH oxidase priming at inflammatory sites. J Clin Invest 116 (2006) 2033-2043
70. Larsen M.R., Thingholm T.E., Jensen O.N., Roepstorff P., and Jørgensen T.J.D. Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol Cell Proteom 4 (2005) 873-886
71. Klemm C., Otto S., Wolf C., Haseloff R.F., Beyermann M., and Krause E. Evaluation of the titanium dioxide approach for MS analysis of phosphopeptides. J Mass Spectrom 41 (2006) 1623-1632
72. Lim K.B., and Kassel D.B. Phosphopeptides enrichment using on-line two-dimensional strong cation exchange followed by reversed-phase liquid chromatography/mass spectrometry. Anal Biochem 354 (2006) 213-219
73. Fukuda M. Versatile role of Rab27 in membrane trafficking: focus on the Rab27 effector families. J Biochem 137 (2005) 9-16
74. Ortega-Pérez I., Cano E., Were F., Villar M., Vázquez J., and Redondo J.M. c-Jun N-terminal kinase (JNK) positively regulates NFATc2 transactivation through phosphorylation within the N-terminal regulatory domain. J Biol Chem 280 (2005) 20867-20878
75. Xue Y., Ren J., Gao X., Jin C., Wen L., and Yao X. GPS 2.0, a tool to predict kinase-specific phosphorylation sites in hierarchy. Mol Cell Proteomics 7 (2008) 1598-1608
76. Mócsai A., Jakus Z., Vántus T., Berton G., Lowell C.A., and Ligeti E. Kinase pathways in chemoattractant-induced degranulation of neutrophils: the role of p38 mitogen-activated protein kinase activated by Src family kinases. J Immunol 164 (2000) 4321-4331
77. Jog N.R., Vala V.R., Ward R.A., Rane M.J., Bodulluri H., and McLeish K.R. Heat shock protein 27 (Hsp27) regulates neutrophil chemotaxis and exocytosis through two different mechanisms. J Immunol 178 (2007) 2421-2428
78. Hell S.W. Microscopy and its focal switch. Nature Methods 6 (2009) 24-32
79. Blow N. Mass spectrometry: playing catch up. Nature Methods 4 (2007) 1059-1064
80. Sykora C., Hoffmann R., and Hoffmann P. Enrichment of multiphosphorylated peptides by immobilized metal affinity chromatography using Ga(III)- and Fe(III)-complexes. Prot Pept Lett 14 (2007) 489-496