Primary granule exocytosis in human neutrophils is regulated by Rac-dependent actin remodeling

American Journal of Physiology - Cell Physiology

Volumn 295, Issue 5, 2008, Pages

  Mitchell, Troy ^a   Lo, Andrea ^a   Logan, Michael R ^a   Lacy, Paige ^a   Eitzen, Gary ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Cytochalasin; Jasplakinolide; Latrunculin; NSC23766; Rac guanosine triphosphatase

Indexed keywords

ACTIN; ACTIN DEPOLYMERIZING FACTOR; CALCIUM IONOPHORE; CYTOCHALASIN B; F ACTIN; FORMYLPEPTIDE RECEPTOR; JASPAMIDE; LACTOFERRIN; LATRUNCULIN B; MYELOPEROXIDASE; RAC2 PROTEIN; RAL PROTEIN;

ACTIN POLYMERIZATION; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVATION; EXOCYTOSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; NEUTROPHIL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN STABILITY;

EID: 57349129589     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00239.2008     Document Type: Article

References (52)

1. Abdel-Latif D, Steward M, Macdonald DL, Francis GA, Dinauer MC, Lacy P. Rac2 is critical for neutrophil primary granule exocytosis. Blood 104: 832-839, 2004.
2. Benard V, Bohl BP, Bokoch GM. Characterization of rac and cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J Biol Chem 274: 13198-13204, 1999.
3. Billadeau DD, Brumbaugh KM, Dick CJ, Schoon RA, Bustelo XR, Leibson PJ. The Vav-Rac1 pathway in cytotoxic lymphocytes regulates the generation of cell-mediated killing. J Exp Med 188: 549-559, 1998.
4. Bromberg Y, Shani E, Joseph G, Gorzalczany Y, Sperling O, Pick E. The GDP-bound form of the small G protein Rac1 p21 is a potent activator of the superoxide-forming NADPH oxidase of macrophages. J Biol Chem 269: 7055-7058, 1994.
5. Brown AM, O'Sullivan AJ, Gomperts BD. Induction of exocytosis from permeabilized mast cells by the guanosine triphosphatases Rac and Cdc42. Mol Biol Cell 9: 1053-1063, 1998.
6. Bubb MR, Senderwoicz AM, Sausville EA, Duncan KL, Korn ED. Jasplakinolide, a cytotoxic natural product, induces actin polymerization and competitively inhibits the binding of phalloidin to F-actin. J Biol Chem 269: 14869-14871, 1994.
7. Burgoyne RD, Morgan A. Secretory granule exocytosis. Physiol Rev 83: 581-632, 2003.
8. Cancelas JA, Lee AW, Prabhakar R, Stringer KF, Zheng Y, Williams DA. Rac GTPases differentially integrate signals regulating hematopoietic stem cell localization. Nat Med 11: 886-891, 2005.
9. Cooper JA, Pollard TD. Methods to measure actin polymerization. Methods Enzymol 85: 182-210, 1982.
10. Desnos C, Schonn JS, Huet S, Tran VS, El-Amraoui A, Raposo G, Fanget I, Chapuis C, Ménasché G, de Saint Basile G, Petit C, Cribier S, Henry JP, Darchen F. Rab27A and its effector MyRIP link secretory granules to F-actin and control their motion towards release sites. J Cell Biol 163: 559-570, 2003.
11. Diebold BA, Bokoch GM. Rho GTPases and the control of the oxidative burst in polymorphonuclear leukocytes. Curr Top Microbiol Immunol 291: 91-111, 2005.
12. Downey GP, Elson EL, Schwab B, Erzurum SC, Young SK, Worthen GS. Biophysical properties and microfilament assembly in neutrophils: modulation by cyclic AMP. J Cell Biol 114: 1179-1190, 1991.
13. Eitzen G, Wang L, Thorngren N, Wickner W. Remodeling of organelle-bound actin is required for yeast vacuole fusion. J Cell Biol 158: 669-679, 2002.
14. Filippi MD, Harris CE, Meller J, Gu Y, Zheng Y, Williams DA. Localization of Rac2 via the C terminus and aspartic acid 150 specifies superoxide generation, actin polarity and chemotaxis in neutrophils. Nat Immunol 5: 744-751, 2004.
15. Gao Y, Dickerson JB, Guo F, Zheng J, Zheng Y. Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci USA 101: 7618-7623, 2004.
16. Gasman S, Chasserot-Golaz S, Malacombe M, Way M, Bader MF. Regulated exocytosis in neuroendocrine cells: a role for subplasmalemmal Cdc42/N-WASP-induced actin filaments. Mol Biol Cell 15: 520-531, 2004.
17. Geijsen N, van Delft S, Raaijmakers JA, Lammers JW, Collard JG, Koenderman L, Coffer PJ. Regulation of p21rac activation in human neutrophils. Blood 94: 1121-1130, 1999.
18. Glogauer M, Hartwig J, Stossel T. Two pathways through Cdc42 couple the N-formyl receptor to actin nucleation in permeabilized human neutrophils. J Cell Biol 150: 785-796, 2000.
19. Gu Y, Filippi MD, Cancelas JA, Siefring JE, Williams EP, Jasti AC, Harris CE, Lee AW, Prabhakar R, Atkinson SJ, Kwiatkowski DJ, Williams DA. Hematopoietic cell regulation by Rac1 and Rac2 guanosine triphosphatases. Science 302: 445-449, 2003.
20. Haddad EK, Wu X, Hammer JA 3rd, Henkart PA. Defective granule exocytosis in Rab27a-deficient lymphocytes from Ashen mice. J Cell Biol 152: 835-842, 2001.
21. Henson PM, Zanolari B, Schwartzman NA, Hong SR. Intracellular control of human neutrophil secretion. I. C5a-induced stimulus-specific desensitization and the effects of cytochalasin B. J Immunol 121: 851-855, 1978.
22. Heyworth PG, Bohl BP, Bokoch GM, Curnutte JT. Rac translocates independently of the neutrophil NADPH oxidase components p47phox and p67phox. Evidence for its interaction with flavocytochrome b558. J Biol Chem 269: 30749-30752, 1994.
23. Hogg JC. Neutrophil kinetics and lung injury. Physiol Rev 67: 1249-1295, 1987.
24. 2+ mobilization and degranulation in mutant RBL mast cells. Proc Natl Acad Sci USA 98: 1154-1159, 2001.
25. Isgandarova S, Jones L, Forsberg D, Loncar A, Dawson J, Tedrick K, Eitzen G. Stimulation of actin polymerization by vacuoles via Cdc42p-dependent signaling. J Biol Chem 282: 30466-30475, 2007.
26. Jaeschke H, Smith CW. Mechanisms of neutrophil-induced parenchymal cell injury. J Leukoc Biol 61: 647-653, 1997.
27. Jahraus A, Egeberg M, Hinner B, Habermann A, Sackman E, Pralle A, Faulstich H, Rybin V, Defacque H, Griffiths G. ATP-dependent membrane assembly of F-actin facilitates membrane fusion. Mol Biol Cell 12: 155-170, 2001.
28. Jog NR, Rane MJ, Lominadze G, Luerman GC, Ward RA, McLeish KR. The actin cytoskeleton regulates exocytosis of all neutrophil granule subsets. Am J Physiol Cell Physiol 292: C1690-C1700, 2007.
29. Khurana D, Leibson PJ. Regulation of lymphocyte-mediated killing by GTP-binding proteins. J Leukoc Biol 73: 333-338, 2003.
30. Kim C, Marchal CC, Penninger J, Dinauer MC. The hemopoietic Rho/Rac guanine nucleotide exchange factor Vav1 regulates N-formylmethionyl- leucyl-phenylalanine-activated neutrophil functions. J Immunol 171: 4425-4430, 2003.
31. Lacy P, Thompson N, Tian M, Solari R, Hide I, Newman TM, Gomperts BD. A survey of GTP-binding proteins and other potential key regulators of exocytotic secretion in eosinophils. Apparent absence of rab3 and vesicle fusion protein homologues. J Cell Sci 108: 3547-3556, 1995.
32. Lacy P, Mahmudi-Azer S, Bablitz B, Gilchrist M, Fitzharris P, Cheng D, Man SF, Bokoch GM, Moqbel R. Expression and translocation of Rac2 in eosinophils during superoxide generation. Immunology 98: 244-252, 1999.
33. Lacy P, Eitzen G. Control of granule exocytosis in neutrophils. Front Biosci 13: 5559-5570, 2008.
34. Lang T, Wacker I, Wunderlich I, Rohrbach A, Giese G, Soldati T, Almers W. Role of actin cortex in the subplasmalemmal transport of secretory granules in PC-12 cells. Biophys J 78: 2863-2877, 2000.
35. Logan MR, Odemuyiwa SO, Moqbel R. Understanding exocytosis in immune and inflammatory cells: the molecular basis of mediator secretion. J Allergy Clin Immunol 111: 923-932, 2003.
36. Malacombe M, Bader MF, Gasman S. Exocytosis in neuroendocrine cells: new tasks for actin. Biochim Biophys Acta 1763: 1175-1183, 2006.
37. Munafó DB, Johnson JL, Ellis BA, Rutschmann S, Beutler B, Catz SD. Rab27a is a key component of the secretory machinery of azurophilic granules in granulocytes. Biochem J 402: 229-239, 2007.
38. Norman JC, Price LS, Ridley AJ, Hall A, Koffer A. Actin filament organization in activated mast cells is regulated by heterotrimeric and small GTP-binding proteins. J Cell Biol 126: 1005-1015, 1994.
39. Norman JC, Price LS, Ridley AJ, Koffer A. The small GTP-binding proteins, Rac and Rho, regulate cytoskeletal organization and exocytosis in mast cells by parallel pathways. Mol Biol Cell 7: 1429-1442, 1996.
40. Oberhauser AF, Monck JR, Balch WE, Fernandez JM. Exocytotic fusion is activated by Rab3a peptides. Nature 360: 270-273, 1992.
41. Pestonjamasp KN, Forster C, Sun C, Gardiner EM, Bohl B, Weiner O, Bokoch GM, Glogauer M. Rac1 links leading edge and uropod events through Rho and myosin activation during chemotaxis. Blood 108: 2814-2820, 2006.
42. Rizoli SB, Rotstein OD, Parodo J, Phillips MJ, Kapus A. Hypertonic inhibition of exocytosis in neutrophils: central role for osmotic actin skeleton remodeling. Am J Physiol Cell Physiol 279: C619-C633, 2000.
43. Rosales JL, Ernst JD. GTP-dependent permeabilized neutrophil secretion requires a freely diffusible cytosolic protein. J Cell Biochem 80: 37-45, 2000.
44. Sengeløv H, Kjeldsen L, Borregaard N. Control of exocytosis in early neutrophil activation. J Immunol 150: 1535-1543, 1993.
45. Skubitz KM. Neutrophilic leukocytes. In: Wintrobe's Clinical Hematology (11th ed.), edited by Greer JP, Foerster J, Lukens J, Rodgers G, Paraskevas F, Glader B. Philadelphia, PA: Williams & Wilkins, 2004, p. 267-310.
46. Showell HJ, Freer RJ, Zigmond SH, Schiffmann E, Aswanikumar S, Corcoran B, Becker EL. The structure-activity relations of synthetic peptides as chemotactic factors and inducers of lysosomal secretion for neutrophils. J Exp Med 143: 1154-1169, 1976.
47. Spector I, Shochet NR, Blasberger D, Kashman Y. Latrunculins - novel marine macrolides that disrupt microfilament organization and affect cell growth. I. Comparison with cytochalasin D. Cell Motil Cytoskeleton 13: 127-144, 1989.
48. Stinchcombe JC, Barral DC, Mules EH, Booth S, Hume AN, Machesky LM, Seabra MC, Griffiths GM. Rab27a is required for regulated secretion in cytotoxic T lymphocytes. J Cell Biol 152: 825-834, 2001.
49. Sun CX, Magalhães MA, Glogauer M. Rac1 and Rac2 differentially regulate actin free barbed end formation downstream of the fMLP receptor. J Cell Biol 179: 239-245, 2007.
50. Welch HC, Condliffe AM, Milne LJ, Ferguson GJ, Hill K, Webb LM, Okkenhaug K, Coadwell WJ, Andrews SR, Thelen M, Jones GE, Hawkins PT, Stephens LR. P-Rex1 regulates neutrophil function. Curr Biol 15: 1867-1873, 2005.
51. Xu J, Wang F, van Keymeulen A, Herzmark P, Straight A, Kelly K, Takuwa Y, Sigimoto N, Mitchison T, Bourne HR. Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell 115: 201-214, 2003.
52. Zigmond SH, Levistsky HI, Krell BJ. Cell polarity: an examination of its behavioural expression and its consequences for polymorphonuclear leukocyte chemotaxis. J Cell Biol 89: 585-592, 1981.