Cytoskeletal remodeling in leukocyte function

Current Opinion in Hematology

Volumn 11, Issue 1, 2004, Pages 15-24

  Fenteany, Gabriel ^a   Glogauer, Michael ^b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Cell polarization and migration; Chemotaxis; Cytoskeleton; Phagocytosis; Phosphoinositides; Rho family small GTPases

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; F ACTIN; GUANOSINE TRIPHOSPHATASE; ISOPROTEIN; PHOSPHATIDYLINOSITIDE; RAC PROTEIN; RAC2 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ACTIN POLYMERIZATION; CELL ACTIVATION; CELL MIGRATION; CELL MOTILITY; CELL POLARITY; CELL SHAPE; CELLULAR IMMUNITY; CHEMOTAXIS; CYTOSKELETON; FEEDBACK SYSTEM; HUMAN; LEUKOCYTE FUNCTION; LEUKOCYTE MEMBRANE; LEUKOCYTE MIGRATION; NEUTROPHIL CHEMOTAXIS; PHAGOCYTOSIS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ACTINS; ANIMALS; CELL MEMBRANE; CHEMOTAXIS; CHEMOTAXIS, LEUKOCYTE; FLUORESCENT DYES; HUMANS; LEUKOCYTES; MICROFILAMENTS; PHAGOCYTOSIS; RAC GTP-BINDING PROTEINS; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 0346880066     PISSN: 10656251     EISSN: None     Source Type: Journal    
DOI: 10.1097/00062752-200401000-00004     Document Type: Review

References (124)

1. Lauffenburger DA, Horwitz AF: Cell migration: a physically integrated molecular process. Cell 1996, 84:359-369.
2. Carlier MF, Pantaloni D: Control of actin dynamics in cell motility. J Mol Biol 1997, 269:459-467.
3. Welch MD, Mallavarapu A, Rosenblatt J, Mitchison TJ: Actin dynamics in vivo. Curr Opin Cell Biol 1997, 9:54-61.
4. Stossel TP, Hartwig JH, Janmey PA, Kwiatkowski DJ: Cell crawling two decades after Abercrombie. Biochem Soc Symp 1999, 65:267-280.
5. Borisy GG, Svitkina TM: Actin machinery: pushing the envelope. Curr Opin Cell Biol 2000, 12:104-112.
6. Chen H, Bernstein BW, Bamburg JR: Regulating actin-filament dynamics in vivo. Trends Biochem Sci 2000, 25:19-23.
7. Pollard TD: Reflections on a quarter century of research on contractile systems. Trends Biochem Sci 2000, 25:607-611.
8. Pollard TD, Blanchoin L, Mullins RD: Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys Biomol Struct 2000, 29:545-576.
9. Wear MA, Schafer DA, Cooper JA: Actin dynamics: assembly and disassembly of actin networks. Curr Biol 2000, 10:R891-R895.
10. Higgs HN, Pollard TD: Regulation of actin filament network formation through Arp2/3 complex: activation by a diverse array of proteins. Annu Rev Biochem 2001, 70:649-676.
11. Pantaloni D, Le Clainche C, Carlier MF: Mechanism of actin-based motility. Science 2001, 292:1502-1506.
12. Small JV, Stradel T, Vignal E, Rottner K: The lamellipodium: where motility begins. Trends Cell Biol 2002, 12:112-120.
13. Welch MD, Mullins RD: Cellular control of actin nucleation. Annu Rev Cell Dev Biol 2002, 18:247-288.
14. Pollard TD, Borisy GG: Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003, 112:453-465.
15. Fenteany G, Zhu S: Small-molecule inhibitors of actin dynamics and cell motility. Curr Topics Med Chem 2003, 3:593-616.
16. Carlier MF, Clainche CL, Wiesner S, Pantaloni D: Actin-based motility: from molecules to movement. Bioessays 2003, 25:336-345.
17. Rodriguez OC, Schaefer AW, Mandato CA, et al.: Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat Cell Biol 2003, 5:599-609.
18. Vicente-Manzanares M, Sancho D, Yanez-Mo M, Sanchez-Madrid F: The leukocyte cytoskeleton in cell migration and immune interactions. Int Rev Cytol 2002, 216:233-289.
19. Worthylake RA, Burridge K: Leukocyte transendothelial migration: orchestrating the underlying molecular machinery. Curr Opin Cell Biol 2001, 13:569-577.
20. Luscinskas FW, Ma S, Nusrat A, et al.: Leukocyte transendothelial migration: a junctional affair. Semin Immunol 2002, 14:105-113.
21. Hordijk P: Endothelial signaling in leukocyte transmigration. Cell Biochem Biophys 2003, 38:305-322.
22. Cannon JL, Burkhardt JK: The regulation of actin remodeling during T-cell-APC conjugate formation. Immunol Rev 2002, 186:90-99.
23. Sancho D, Vicente-Manzanares M, Mittelbrunn M, et al.: Regulation of microtubule-organizing center orientation and actomyosin cytoskeleton rearrangement during immune interactions. Immunol Rev 2002, 189:84-97.
24. Sechi AS, Buer J, Wehland J, Probst-Kepper M: Changes in actin dynamics at the T-cell/APC interface: implications for T-cell anergy? Immunol Rev 2002, 189:98-110.
25. Vyas YM, Maniar H, Dupont B: Visualization of signaling pathways and cortical cytoskeleton in cytolytic and noncytolytic natural killer cell immune synapses. Immunol Rev 2002, 189:161-178.
26. Miletic AV, Swat M, Fujikawa K, Swat W: Cytoskeletal remodeling in lymphocyte activation. Curr Opin Immunol 2003, 15:261-268.
27. Samstag Y, Eibert SM, Klemke M, Wabnitz GH: Actin cytoskeletal dynamics in T lymphocyte activation and migration. J Leukoc Biol 2003, 73:30-48.
28. Castellano F, Chavrier P, Caron E: Actin dynamics during phagocytosis. Semin Immunol 2001, 13:347-355.
29. May RC, Machesky LM: Phagocytosis and the actin cytoskeleton. J Cell Sci 2001, 114:1061-1077.
30. Schafer DA: Coupling actin dynamics and membrane dynamics during endocytosis. Curr Opin Cell Biol 2002, 14:76-81.
31. Scholey JM, Brust-Mascher I, Mogilner A: Cell division. Nature 2003, 422:746-752.
32. Yin HL, Janmey PA: Phosphoinositide regulation of the actin cytoskeleton. Annu Rev Physiol 2003, 65:761-789.
33. Hall A, Nobes CD: Rho GTPases: molecular switches that control the organization and dynamics of the actin cytoskeleton. Philos Trans R Soc Lond B Biol Sci 2000, 355:965-970.
34. Schmitz AA, Govek EE, Bottner B, Van Aelst L: Rho GTPases: signaling, migration, and invasion. Exp Cell Res 2000, 261:1-12.
35. Ridley AJ: Rho GTPases and cell migration. J Cell Sci 2001, 114:2713-2722.
36. Ridley AJ: Rho family proteins: coordinating cell responses. Trends Cell Biol 2001, 11:471-477.
37. Etienne-Manneville S, Hall A: Rho GTPases in cell biology. Nature 2002, 420:629-635.
38. Cramer LP, Siebert M, Mitchison TJ: Identification of novel graded polarity actin filament bundles in locomoting heart fibroblasts: implications for the generation of motile force. J Cell Biol 1997, 136:1287-1305.
39. Takenawa T, Miki H: WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J Cell Sci 2001, 114:1801-1819.
40. Suetsugu S, Miki H, Takenawa T: Spatial and temporal regulation of actin polymerization for cytoskeleton formation through Arp2/3 complex and WASP/WAVE proteins. Cell Motil Cytoskeleton 2002, 51:113-122.
41. Caron E: Regulation of Wiskott-Aldrich syndrome protein and related molecules. Curr Opin Cell Biol 2002, 14:82-87.
42. Badour K, Zhang J, Siminovitch KA: The Wiskott-Aldrich syndrome protein: forging the link between actin and cell activation. Immunol Rev 2003, 192:98-112.
43. Thrasher AJ: WASp in immune-system organization and function. Nat Rev Immunol 2002, 2:635-646.
44. Jones GE, Zicha D, Dunn GA, et al.: Restoration of podosomes and chemotaxis in Wiskott-Aldrich syndrome macrophages following induced expression of WASp. Int J Biochem Cell Biol 2002, 34:806-815.
45. Launay S, Brown G, Machesky LM: Expression of WASP and Scar1/WAVE1 actin-associated proteins is differentially modulated during differentiation of HL-60 cells. Cell Motil Cytoskeleton 2003, 54:274-285. Evidence is provided for the possibility that modulation of the expression of different members of the WASP family may be part of the differentiation program of myeloid precursors, with different roles for WASP and Scar1/WAVE1 in leukocytes.
46. Caron E, Hall A: Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 1998, 282:1717-1721.
47. Olazabal IM, Caron E, May RC, et al.: Rho-kinase and myosin-II control phagocytic cup formation during CR, but not FcγR, phagocytosis. Curr Biol 2002, 12:1413-1418. Further delineating differences between phagocytosis through different receptors in macrophages, this study shows that Rho-kinase and myosin II are required for phagocytic cup formation through CR3 but not FcγR, which only requires myosin II for the later internalization of phagocytic vesicles.
48. Taunton J: Actin filament nucleation by endosomes, lysosomes and secretory vesicles. Curr Opin Cell Biol 2001, 13:85-91.
49. Cameron LA, Giardini PA, Soo FS, Theriot JA: Secrets of actin-based motility revealed by a bacterial pathogen. Nat Rev Mol Cell Biol 2000, 1:110-119.
50. Goldberg MB: Actin-based motility of intracellular microbial pathogens. Microbiol Mol Biol Rev 2001, 65:595-626.
51. Portnoy DA, Auerbuch V, Glomski IJ: The cell biology of Listeria monocytogenes infection: the intersection of bacterial pathogenesis and cell-mediated immunity. J Cell Biol 2002, 158:409-414.
52. Zhang F, Southwick FS, Purich DL: Actin-based phagosome motility. Cell Motil Cytoskeleton 2002, 53:81-88.
53. Southwick FS, Li W, Zhang F, et al.: Actin-based endosome and phagosome rocketing in macrophages: activation by the secretagogue antagonists lanthanum and zinc. Cell Motil Cytoskeleton 2003, 54:41-55. Phagosomes and early endosomes induced by treatment of macrophages with lanthanum and zinc are shown to assemble actin-rich rocket tails with recruitment of a number of known actin-binding and actin-regulatory proteins.
54. Devreotes P, Janetopoulos C: Eukaryotic chemotaxis: distinctions between directional sensing and polarization. J Biol Chem 2003, 278:20445-20448.
55. Zigmond SH: Ability of polymorphonuclear leukocytes to orient in gradients of chemotactic factors. J Cell Biol 1977, 75:606-616.
56. Zigmond SH, Levitsky HI, Kreel BJ: Cell polarity: an examination of its behavioral expression and its consequences for polymorphonuclear leukocyte chemotaxis. J Cell Biol 1981, 89:585-592.
57. Therrien S, Naccache PH: Guanine nucleotide-induced polymerization of actin in electropermeabilized human neutrophils. J Cell Biol 1989, 109:1125-1132.
58. Sarndahl E, Lindroth M, Bengtsson T, et al.: Association of ligand-receptor complexes with actin filaments in human neutrophils: a possible regulatory role for a G-protein. J Cell Biol 1989, 109:2791-2799.
59. Downey GP, Chan CK, Grinstein S: Actin assembly in electropermeabilized neutrophils: role of G-proteins. Biochem Biophys Res Commun 1989, 164:700-705.
60. Didsbury J, Weber RF, Bokoch GM, et al.: rac, a novel ras-related family of proteins that are botulinum toxin substrates. J Biol Chem 1989, 264:16378-16382.
61. Polakis PG, Weber RF, Nevins B, et al.: Identification of the ral and rac1 gene products, low molecular mass GTP-binding proteins from human platelets. J Biol Chem 1989, 264:16383-16389.
62. Madaule P, Axel R: A novel ras-related gene family. Cell 1985, 41:31-40.
63. Johnson DI, Jacobs CW, Pringle JR, et al.: Mapping of the Saccharomyces cerevisiae CDC3, CDC25, and CDC42 genes to chromosome XII by chromosome blotting and tetrad analysis. Yeast 1987, 3:243-253.
64. Bender A, Pringle JR: Multicopy suppression of the cdc24 budding defect in yeast by CDC42 and three newly identified genes including the ras-related gene RSR1. Proc Natl Acad Sci U S A 1989, 85:9976-9980.
65. Johnson DI, Pringle JR: Molecular characterization of CDC42, a Saccharomyces cerevisiae gene involved in the development of cell polarity. J Cell Biol 1990, 111:143-152.
66. Polakis PG, Snyderman R, Evans T: Characterization of G25K, a GTP-binding protein containing a novel putative nucleotide binding domain. Biochem Biophys Res Commun 1989, 160:25-32.
67. Munemitsu S, Innis MA, Clark R, et al.: Molecular cloning and expression of a G25K cDNA, the human homolog of the yeast cell cycle gene CDC42. Mol Cell Biol 1990, 10:5977-5982.
68. Shinjo K, Koland JG, Hart MJ, et al.: Molecular cloning of the gene for the human placental GTP-binding protein Gp (G25K): identification of this GTP-binding protein as the human homolog of the yeast cell-division-cycle protein CDC42. Proc Natl Acad Sci U S A 1990, 87:9853-9857.
69. Chardin P, Boquet P, Madaule P, et al.: The mammalian G protein rhoC is ADP-ribosylated by Clostridium botulinum exoenzyme C3 and affects actin microfilaments in Vero cells. EMBO J 1989, 8:1087-1092.
70. rho induces rapid changes in cell morphology. J Cell Biol 1990, 111:1001-1007.
71. Stasia MJ, Jouan A, Bourmeyster N, et al.: ADP-ribosylation of a small size GTP-binding protein in bovine neutrophils by the C3 exoenzyme of Clostridium botulinum and effect on the cell motility. Biochem Biophys Res Commun 1991, 180:615-622.
72. Morii N, Narumiya S: ras oncogene-related small molecular weight GTP-binding protein, rho gene product and botulinum C3 ADP-ribosyltransferase. Nippon Yakurigaku Zasshi 1992, 99:191-203.
73. Morii N, Teru-uchi T, Tominaga T, et al.: A rho gene product in human blood platelets. II. Effects of the ADP-ribosylation by botulinum C3 ADP-ribosyltransferase on platelet aggregation. J Biol Chem 1992, 267:20921-20926.
74. Ridley AJ, Hall A: Distinct patterns of actin organization regulated by the small GTP-binding proteins Rac and Rho. Cold Spring Harb Symp Quant Biol 1992, 57:661-671.
75. Ridley AJ, Paterson HF, Johnston CL, et al.: The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 1992, 70:401-410.
76. Ridley AJ, Hall A: The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 1992, 70:389-399.
77. Kozma R, Ahmed S, Best A, Lim L: The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol Cell Biol 1995, 15:1942-1952.
78. Li R, Zheng Y, Drubin DG: Regulation of cortical actin cytoskeleton assembly during polarized cell growth in budding yeast. J Cell Biol 1995, 128:599-615.
79. Nobes CD, Hall A: Rho, rac and cdc42 GTPases: regulators of actin structures, cell adhesion and motility. Biochem Soc Trans 1995, 23:456-459.
80. Cicchetti G, Allen PG, Glogauer M: Chemotactic signaling pathways in neutrophils: from receptor to actin assembly. Crit Rev Oral Biol Med 2002, 13:220-228.
81. Zhelev DV, Alteraifi A: Signaling in the motility responses of the human neutrophil. Ann Biomed Eng 2002, 30:356-370.
82. 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 2000, 150:785-796.
83. Evangelista M, Zigmond S, Boone C: Formins: signaling effectors for assembly and polarization of actin filaments. J Cell Sci 2003, 116:2603-2611.
84. Wallar BJ, Alberts AS: The formins: active scaffolds that remodel the cytoskeleton. Trends Cell Biol 2003, 13:435-446.
85. Dinauer MC: Regulation of neutrophil function by Rac GTPases. Curr Opin Hematol 2003, 10:8-15.
86. Ambruso DR, Knall C, Abell AN, et al.: Human neutrophil immunodeficiency syndrome is associated with an inhibitory Rac2 mutation. Proc Natl Acad Sci U S A 2000, 97:4654-4659.
87. phox. Evidence for its interaction with flavocytochrome b558. J Biol Chem 1994, 269:30749-30752.
88. Li S, Yamauchi A, Marchal CC, et al.: Chemoattractant-stimulated Rac activation in wild-type and Rac2-deficient murine neutrophils: preferential activation of Rac2 and Rac2 gene dosage effect on neutrophil functions. J Immunol 2002, 169:5043-5051. A detailed characterization of the level of activity and relative contribution made by Rac2 during neutrophil function.
89. Glogauer M, Marchal CC, Zhu F, et al.: Rac1 deletion in mouse neutrophils has selective effects on neutrophil functions. J Immunol 2003, 170:5652-5657. The first study to investigate the specific roles played by Rac1 in neutrophil functions using primary neutrophils.
90. Michaelson D, Silletti J, Murphy G, et al.: Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding. J Cell Biol 2001, 152:111-126.
91. 2 integrin-mediated adhesion of human neutrophils. J Biol Chem 2003, 278:24181-24188.
92. Niggli V: Rho-kinase in human neutrophils: a role in signalling for myosin light chain phosphorylation and cell migration. FEBS Lett 1999, 445:69-72.
93. Alblas J, Ulfman L, Hordijk P, Koenderman L: Activation of RhoA and ROCK are essential for detachment of migrating leukocytes. Mol Biol Cell 2001, 12:2137-2145.
94. Worthylake RA, Lemoine S, Watson JM, Burridge K: RhoA is required for monocyte tail retraction during transendothelial migration. J Cell Biol 2001, 154:147-160.
95. Liu L, Schwartz BR, Lin N, et al.: Requirement for RhoA kinase activation in leukocyte de-adhesion. J Immunol 2002, 169:2330-2336.
96. Worthylake RA, Burridge K: RhoA and ROCK promote migration by limiting membrane protrusions. J Biol Chem 2003, 278:13578-13584. This study demonstrates that Rho-kinase activity is required to restrict integrin activation and membrane protrusion to the leading edge in neutrophils through a pathway involving cofilin.
97. Yoshinaga-Ohara N, Takahashi A, Uchiyama T, Sasada M: Spatiotemporal regulation of moesin phosphoryiation and rear release by Rho and serine/threonine phosphatase during neutrophil migration. Exp Cell Res 2002, 278:112-122.
98. Gardiner EM, Pestonjamasp KN, Bohl BP, et al.: Spatial and temporal analysis of Rac activation during live neutrophil chemotaxis. Curr Biol 2002, 12:2029-2034. Rac is shown to be activated not only at the leading edge but also in the retracting tail of migrating neutrophils.
99. Insall RH, Weiner OD: PIP3, PIP2, and cell movement: similar messages, different meanings? Dev Cell 2001, 1:743-747.
100. Iijima M, Huang YE, Devreotes P: Temporal and spatial regulation of chemotaxis. Dev Cell 2002, 3:469-478.
101. March ME, Ravichandran K: Regulation of the immune response by SHIP. Semin Immunol 2002, 14:37-47.
102. Weiner OD: Regulation of cell polarity during eukaryotic chemotaxis: the chemotactic compass. Curr Opin Cell Biol 2002, 14:196-202.
103. Rickert P, Weiner OD, Wang F, et al.: Leukocytes navigate by compass: roles of PI3Kγ and its lipid products. Trends Cell Biol 2000, 10:466-473.
104. Bourne HR, Weiner O: A chemical compass. Nature 2002, 419:21.
105. 3.
106. 3 and actin dynamics in the establishment and maintenance of cell polarity.
107. 3-dependent positive feedback loop, while Cdc42 is critical to regulating the location and stability of the Rac-initiated leading edge.
108. 3-and Gβγ-regulated guanine-nucieotide exchange factor for Rac. Cell 2002, 108:809-821.
109. 12/13, Rho, Rho-kinase, and myosin II) during polarization and may explain neutrophil responses to chemoattractants.
110. Sasaki T, Irie-Sasaki J, Jones RG, et al.: Function of PI3Kγ in thymocyte development, T cell activation, and neutrophil migration. Science 2000, 287:1040-1046.
111. Li Z, Jiang H, Xie W, et al.: Roles of PLC-β2 and -β3 and PI3Kγ in chemoattractant-mediated signal transduction. Science 2000, 287:1046-1049.
112. Hirsch E, Katanaev VL, Garlanda C, et al.: Central role for G protein-coupled phosphoinositide 3-kinase γ in inflammation. Science 2000, 287:1049-1053.
113. Hannigan M, Zhan L, Li Z, et al.: Neutrophils lacking phosphoinositide 3-kinase γ show loss of directionality during N-formyl-Met-Leu-Phe- induced chemotaxis. Proc Natl Acad Sci U S A 2002, 99:3603-3608.
114. Sadhu C, Masinovsky B, Dick K, et al.: Essential role of phosphoinositide 3-kinase δ in neutrophil directional movement. J Immunol 2003, 170:2647-2654. A selective inhibitor of PI3Kδ was developed and used to show that this PI3K isoform is required for neutrophil polarization and chemotaxis, but not for random cell migration.
115. 3 appears to be involved in the localization of Cdc42 activity.
116. Bokoch GM: Biology of the p21-activated kinases. Annu Rev Biochem 2003, 72:743-781.
117. Ratner S, Piechocki MP, Galy A: Role of Rho-family GTPase Cdc42 in polarized expression of lymphocyte appendages. J Leukoc Biol 2003, 73:830-840.
118. Pierini LM, Eddy RJ, Fuortes M, et al.: Membrane lipid organization is critical for human neutrophil polarization. J Biol Chem 2003, 278:10831-10841.
119. Nebl T, Pestonjamasp KN, Leszyk JD, et al.: Proteomic analysis of a detergent-resistant membrane skeleton from neutrophil plasma membranes. J Biol Chem 2002, 277:43399-43409. A characterization of protein components of the neutrophil membrane skeleton and provides insight into the relationship between the membrane skeleton and lipid rafts.
120. Manes S, Ana Lacalle R, Gomez-Mouton C, Martinez AC: From rafts to crafts: membrane asymmetry in moving cells. Trends Immunol 2003, 24:320-326.
121. Mor-Vaknin N, Punturieri A, Sitwala K, Markovitz DM: Vimentin is secreted by activated macrophages. Nat Cell Biol 2003, 5:59-63.
122. Evans JG, Correia I, Krasavina O, et al.: Macrophage podosomes assemble at the leading lamella by growth and fragmentation. J Cell Biol 2003, 161:697-705. This work demonstrates that dynamic leading-edge podosomal adhesions in macrophages form by both de novo assembly/growth and fragmentation of precursor podosomes and that polarized formation and turnover of podosomes depends on microtubules.
123. Eddy RJ, Pierini LM, Maxfield FR: Microtubule asymmetry during neutrophil polarization and migration. Mol Biol Cell 2002, 13:4470-4483. This study shows that microtubules reorient toward the uropod during neutrophil polarization and that myosin II and an intact actin cytoskeleton are required for microtubule asymmetry.
124. i and PI3K.