Exocytosis of neutrophil granule subsets and activation of prolyl isomerase 1 are required for respiratory burst priming

Journal of Innate Immunity

Volumn 5, Issue 3, 2013, Pages 277-289

  McLeish, Kenneth R ^a,b,c   Uriarte, Silvia M ^a   Tandon, Shweta ^a   Creed, Timothy M ^a   Le, Junyi ^a   Ward, Richard A ^a  

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

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

Exocytosis; MAPK; NADPH oxidase; Neutrophils; p38; Pin1; Priming

Indexed keywords

GELATINASE; HYDROGEN PEROXIDE; LATRUNCULIN A; PEPTIDYLPROLYL ISOMERASE PIN1; SNARE PROTEIN; SUPEROXIDE; SYNAPTOSOMAL ASSOCIATED PROTEIN 23; SYNTAXIN 4;

ACTIN FILAMENT; ARTICLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; EXOCYTOSIS; HUMAN; HUMAN CELL; NEUTROPHIL GRANULE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; RESPIRATORY BURST; SECRETORY VESICLE;

ENZYME ACTIVATION; EXOCYTOSIS; FEMALE; HUMANS; MALE; N-FORMYLMETHIONINE LEUCYL-PHENYLALANINE; NEUTROPHILS; PEPTIDYLPROLYL ISOMERASE; QA-SNARE PROTEINS; QB-SNARE PROTEINS; QC-SNARE PROTEINS; RESPIRATORY BURST; SECRETORY VESICLES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84876782873     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000345992     Document Type: Article

References (37)

1. Condliffe AM, Kitchen E, Clivers ER: Neu-trophil priming: pathophysiological consequences and underlying mechanisms. Clin Sci 1998; 94:461-471.
2. El-Benna J, Dang PM-C, Gougerot-Pocidalo M-A: Priming of the neutrophil NADPH oxi-dase activation: role of p47phox phosphoryla-tion and NOX2 mobilization to the plasma membrane. Semin Immunopathol 2008; 30: 279-289.
3. Babior BM: NADPH oxidase: an update. Blood 1999; 93:1464-1476.
4. Sheppard FR, Kelher MR, Moore EE, McLaughlin NJD, Banerjee A, Silliman CG: Structural organization of the neutrophil NADPH oxidase: phosphorylation and trans-location during priming and activation. J Leu-koc Biol 2005; 78:1025-1042.
5. Borregaard N, Heiple JM, Simons ER, Clark RA: Subcellular localization of the b-cyto-chrome component of the human neutrophil microbicidal oxidase: translocation during activation. J Cell Biol 1983; 97:52-61.
6. Calafat J, Kuijpers TW, Janssen H, Borregaard N, Verhoeven AJ, Roos D: Evidence for small intracellular vesicles in human blood phagocytes containing cytochrome b558 and the adhesion molecule CD11b/CD18. Blood 1993; 81:3122-3129.
7. Kjeldsen L, Sengeløv H, Lollike K, Nielsen MH, Borregaard N: Isolation and characterization of gelatinase granules from human neutrophils. Blood 1994; 83:1640-1649.
8. DeLeo FR, Renee J, McCormick S, Nakamura M, Apicella M, Weiss JP, Nauseef WM: Neu-trophils exposed to bacterial lipopolysaccha-ride upregulate NADPH oxidase assembly. J Clin Invest 1998; 101:455-463.
9. Ward RA, Nakamura M, McLeish KR: Priming of the neutrophil respiratory burst involves p38 mitogen-activated protein kinase-dependent exocytosis of flavocytochrome b558-containing granules. J Biol Chem 2000; 275:36713-36719.
10. Uriarte SM, Rane MJ, Luerman GC, Barati MT, Ward RA, Nauseef WM, McLeish KR: Granule exocytosis contributes to priming and activation of the human neutrophil respiratory burst. J Immunol 2011; 187:391-400.
11. Dang PM-C, Stensballe A, Bousetta T, Raad H, Dewas C, Kroviarski Y, Hayem G, Jensen ON, Gougerot-Pocidalo M-A, El-Benna J: A specific p47phox-serine phosphorylated by convergent MAPKs mediates neutrophil NADPH oxidase priming at inflammatory sites. J Clin Invest 2006; 116:2033-2043.
12. Boussetta T, Gougerot-Pocidalo M-A, Hayem G, Ciappelloni S, Raad H, Derkawi RA, Bournier O, Kroviarski Y, Zhou XZ, Malter JS, Lu PK, Bartegi A, Dang PM-C, El-Benna J: The prolyl isomerase Pin1 acts as a novel molecular switch for TNF-alpha-induced priming of the NAPDH oxidase in human neutro-phils. Blood 2010; 116:5795-5802.
13. McLeish KR, Knall C, Ward RA, Gerwins P, Coxon PY, Klein JB, Johnson GL: Activation of mitogen-activated protein kinase cascades during priming of human neutrophils by TNF-alpha and GM-CSF. J Leukoc Biol 1998; 64:537-545.
14. Haslett C, Guthrie LA, Kopaniak MG, Johnston RB, Henson PM: Modulation of multiple neutrophil functions by preparative methods or trace concentrations of bacterial lipopoly-saccharide. Am J Pathol 1985; 119:101-110.
15. Jog NR, Rane MJ, Lominadze G, Luerman GC, Ward RA, McLeish KR: The actin cyto-skeleton regulates exocytosis of all neutrophil granule subsets. Am J Physiol Cell Physiol 2007; 292:1690-1700.
16. Johnston RB, Keele BB, Misra HP, Lehmeyer JE, Webb LS, Baehner RL, Rajagopalan KV: The role of superoxide anion generation in phagocytic bactericidal activity. J Clin Invest 1975; 55:1357-1372.
17. Omori K, Ohira T, Uchida Y, Ayilavarapu S, Batista EL, Yagi M, Iwata T, Liu H, Hasturk H, Kantarci A, Van Dyke TE: Priming of neu-trophil oxidative burst in diabetes requires preassembly of the NADPH oxidase. J Leukoc Biol 2008; 84:292-301.
18. Rasband WS: ImageJ. Bethesda, US National Institutes of Health, http://imagej.nih.gov/ij/, 1997-2011.
19. Zu YL, Ai Y, Gilchrist A, Labadia ME, Sha'afi RI, Huang CK: Activation of MAP kinase-ac-tivated protein kinase 2 in human neutrophils after phorbol ester or fMLP peptide stimulation. Blood 1996; 87:5287-5296.
20. Hannigan MO, Zhan L, Ai Y, Kotlyarov A, Gaestel M, Huang C-K: Abnormal migration phenotype of mitogen-activated protein ki-nase-activated protein kinase 2-/-neutrophils in Zigmond chambers containing formyl-me-thionyl-leucyl-phenylalanine gradients. J Immunol 2001; 167:3953-3961.
21. Coxon PY, Rane MJ, Uriarte S, Powell DW, Singh S, Butt W, Chen Q, McLeish KR: MAPK-activated protein kinase-2 participates in p38 MAPK-dependent and ERK-de-pendent functions in human neutrophils. Cell Signal 2003; 15:993-1001.
22. McColl SR, Beauseigle D, Gilbert C, Naccache PH: Priming of the human neutrophil respiratory burst by granulocyte-macrophage colony-stimulating factor and tumor necrosis factor-alpha involves regulation at a post-cell surface receptor level. Enhancement of the effect of agents which directly activate G proteins. J Immunol 1990; 145:3047-3053.
23. McLeish KR, Klein JB, Schepers T, Sonnen-feld G: Modulation of transmembrane signaling in HL-60 granulocytes by tumour necrosis factor-alpha. Biochem J 1991; 279:455-460.
24. Klein JB, Scherzer JA, Harding GB, Jacobs AA, McLeish KR: TNF-alpha stimulates increased plasma membrane guanine nucleo-tide binding protein activity in polymorpho-nuclear leukocytes. J Leukoc Biol 1995; 57: 500-506.
25. Fäldt J, Dahlgren C, Ridell M, Karlsson A: Priming of human neutrophils by mycobacte-rial lipoarabinomannans: role of granule mobilization. Microbes Infect 2001; 3:1101-1109.
26. Mansfield PJ, Hinkovska-Galcheva V, Shay-man JA, Boxer LA: Granulocyte colony-stimulating factor primes NADPH oxidase in neu-trophils through translocation of cytochrome b558 by gelatinase-granule release. J Lab Clin Med 2002; 140:9-16.
27. Elbim C, Guichard C, Dang PM-C, Fay M, Pedruzzi E, Demur H, Pouzet C, El Benna J, Gougerot-Pocidalo M-A: Interleukin-18 primes the oxidative burst of neutrophils in response to formyl-peptides: role of cyto-chrome b558 translocation and N-formyl peptide receptor endocytosis. Clin Diagn Lab Immunol 2005; 12:436-446.
28. Mollinedo F, Calafat J, Janssen H, Martín-Martín B, Canchado J, Nabokina SM, Gajate C: Combinatorial SNARE complexes modulate the secretion of cytoplasmic granules in human neutrophils. J Immunol 2006; 177: 2831-2841.
29. Leung YM, Kwan EP, Ng B, Kang Y, Gaisano HY: SNAREing voltage-gated K+ and ATP-sensitive K+ channels: tuning beta-cell excitability with syntaxin-1A and other exocytotic proteins. Endocr Rev 2007; 28:653-663.
30. Lominadze G, Powell DW, Luerman GC, Link AJ, Ward RA, McLeish KR: Proteomic analysis of human neutrophil granules. Mol Cell Proteomics 2005; 4:1503-1521.
31. Uriarte SM, Ward RA, Powell DW, Cummins TD, Merchant ML, Luerman GC, Jog NR, McLeish KR: Comparison of the membrane proteomes from human neutrophil secretory vesicles and plasma membrane. J Immunol 2008; 180:5575-5581.
32. Kjeldsen L, Sengelov H, Lollike K, Nielsen MH, Borregaard N: Isolation and characterization of gelatinase granules from human neutrophils. Blood 1994; 83:1640-1649.
33. Mansfield PJ, Hinkovska-Galcheva V, Shay-man JA, Boxer LA: Granulocyte colony-stimulating factor primes NADPH oxidase in neu-trophils through translocation of cytochrome b558 by gelatinase granule release. J Lab Clin Med 2002; 140:9-16.
34. Anrather J, Racchumi G, Iadecola C: NF-kap-paB regulates phagocytic NADPH oxidase by inducing the expression of gp91phox. J Biol Chem 2006; 281:5657-5667.
35. Clark RA, Volpp BD, Leidal KG, Nauseef WM: Two cytosolic components of the human neutrophil respiratory burst oxidase translocate to the plasma membrane during cell activation. J Clin Invest 1990; 85:714-721.
36. El Benna J, Han J, Park J-W, Schmid E, Ule-vitch RJ, Babior BM: Activation of p38 in stimulated human neutrophils: phosphoryla-tion of the oxidase component p47phox by p38 and ERK but not by JNK. Arch Biochem Biophys 1996; 334:395-400.
37. Krump E, Sangher JS, Pelech SL, Furuya W, Grinstein S: Chemotactic peptide N-formyl-Met-Leu-Phe activation of p38 mitogen-acti-vated protine kinase (MAPK) and MAPK-ac-tivated protein kinase-2 in human neutro-phils. J Biol Chem 1997; 272:937-944.