Arp2/3 Complex Is Required for Macrophage Integrin Functions but Is Dispensable for FcR Phagocytosis and In Vivo Motility

Developmental Cell

Volumn 42, Issue 5, 2017, Pages 498-513.e6

  Rotty, Jeremy D ^a,b   Brighton, Hailey E ^a,b   Craig, Stephanie L ^a,b   Asokan, Sreeja B ^a,b   Cheng, Ning ^a,b,c   Ting, Jenny P ^a,b,c   Bear, James E ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

actin; Arp2 3; directed migration; integrin; macrophage; phagocytosis

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; ACTIN RELATED PROTEIN 2-3 COMPLEX; ALPHA M INTEGRIN; BLEBBISTATIN; CD18 ANTIGEN; CHEMOKINE RECEPTOR CCR3; COLONY STIMULATING FACTOR 1; F ACTIN; FC RECEPTOR; FIBRONECTIN; FRACTALKINE; G PROTEIN COUPLED RECEPTOR; IMMUNOGLOBULIN G; INTEGRIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYOSIN II; UNCLASSIFIED DRUG; VINCULIN; ACTIN; CD11B ANTIGEN; COLONY STIMULATING FACTOR; LIGAND; MYOSIN HEAVY CHAIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CELL MOTILITY; CELL PHAGOCYTOSIS; CELL STRUCTURE; CHEMOTAXIS; CLINICAL ASSESSMENT; CONTROLLED STUDY; EAR DISEASE; IN VIVO STUDY; MACROPHAGE FUNCTION; MONOCYTE; MOUSE; NONHUMAN; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; WOUND HEALING; ANIMAL; C57BL MOUSE; CELL MOTION; CELL SHAPE; CYTOLOGY; DRUG EFFECTS; FEMALE; MACROPHAGE; MALE; METABOLISM; PHAGOCYTOSIS; PHENOTYPE; SIGNAL TRANSDUCTION; ULTRASTRUCTURE;

ACTIN-RELATED PROTEIN 2-3 COMPLEX; ACTINS; ANIMALS; CELL MOVEMENT; CELL SHAPE; CHEMOKINE CX3CL1; CHEMOTAXIS; COLONY-STIMULATING FACTORS; FEMALE; FIBRONECTINS; INTEGRINS; LIGANDS; MACROPHAGE-1 ANTIGEN; MACROPHAGES; MALE; MICE, INBRED C57BL; MYOSIN HEAVY CHAINS; PHAGOCYTOSIS; PHENOTYPE; RECEPTORS, FC; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 85028504166     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2017.08.003     Document Type: Article

References (69)

1. Allen, L.A., 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.
2. Asokan, S.B., Johnson, H.E., Rahman, A., King, S.J., Rotty, J.D., Lebedeva, I.P., Haugh, J.M., Bear, J.E., Mesenchymal chemotaxis requires selective inactivation of myosin II at the leading edge via a noncanonical PLCγ/PKCα pathway. Dev. Cell 31 (2014), 747–760.
3. Barkan, D., Green, J.E., Chambers, A.F., Extracellular matrix: a gatekeeper in the transition from dormancy to metastatic growth. Eur. J. Cancer 46 (2010), 1181–1188.
4. Boczkowska, M., Rebowski, G., Kast, D.J., Dominguez, R., Structural analysis of the transitional state of Arp2/3 complex activation by two actin-bound WCAs. Nat. Commun., 5, 2014, 3308.
5. Boulter, E., Garcia-Mata, R., Guilluy, C., Dubash, A., Rossi, G., Brennwald, P.J., Burridge, K., Regulation of Rho GTPase crosstalk, degradation and activity by RhoGDI1. Nat. Cell Biol. 12 (2010), 477–483.
6. Brancato, S.K., Albina, J.E., Wound macrophages as key regulators of repair: origin, phenotype, and function. Am. J. Pathol. 178 (2011), 19–25.
7. Büscher, D., Hipskind, R.A., Krautwald, S., Reimann, T., Baccarini, M., Ras-dependent and -independent pathways target the mitogen-activated protein kinase network in macrophages. Mol. Cell. Biol. 15 (1995), 466–475.
8. Cambien, B., Signal transduction pathways involved in soluble fractalkine-induced monocytic cell adhesion. Blood 97 (2001), 2031–2037.
9. Caron, E., Hall, A., Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 282 (1998), 1717–1721.
10. Chan, K.T., Asokan, S.B., King, S.J., Bo, T., Dubose, E.S., Liu, W., Berginski, M.E., Simon, J.M., Davis, I.J., Gomez, S.M., et al. LKB1 loss in melanoma disrupts directional migration toward extracellular matrix cues. J. Cell Biol. 207 (2014), 299–315.
11. Coleman, M.L., Sahai, E.A., Yeo, M., Bosch, M., Dewar, A., Olson, M.F., Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat. Cell Biol. 3 (2001), 339–345.
12. Collins, S.R., Yang, H.W., Bonger, K.M., Guignet, E.G., Wandless, T.J., Meyer, T., Using light to shape chemical gradients for parallel and automated analysis of chemotaxis. Mol. Syst. Biol., 11, 2015, 804.
13. Davidson, A.J., Wood, W., Unravelling the actin cytoskeleton: a new competitive edge?. Trends Cell Biol. 26 (2016), 569–576.
14. DeMali, K.A., Barlow, C.A., Burridge, K., Recruitment of the Arp2/3 complex to vinculin: coupling membrane protrusion to matrix adhesion. J. Cell Biol. 159 (2002), 881–891.
15. Derry, J.M., Ochs, H.D., Francke, U., Isolation of a novel gene mutated in Wiskott-Aldrich syndrome. Cell 78 (1994), 635–644.
16. Flannagan, R.S., Jaumouillé, V., Grinstein, S., The cell biology of phagocytosis. Annu. Rev. Pathol. Mech. Dis. 7 (2012), 61–98.
17. Freeman, S.A., Grinstein, S., Phagocytosis: receptors, signal integration, and the cytoskeleton. Immunol. Rev. 262 (2014), 193–215.
18. Freeman, S.A., Goyette, J., Furuya, W., Woods, E.C., Bertozzi, C.R., Bergmeier, W., Hinz, B., van der Merwe, P.A., Das, R., Grinstein, S., Integrins form an expanding diffusional barrier that coordinates phagocytosis. Cell 164 (2016), 128–140.
19. Goley, E.D., Rodenbusch, S.E., Martin, A.C., Welch, M.D., Critical conformational changes in the Arp2/3 complex are induced by nucleotide and nucleation promoting factor. Mol. Cell 16 (2004), 269–279.
20. Grinnell, F., Billingham, R.E., Burgess, L., Distribution of fibronectin during wound healing in vivo. J. Invest. Dermatol. 76 (1981), 181–189.
21. Hall, A.B., Gakidis, M.A.M., Glogauer, M., Wilsbacher, J.L., Gao, S., Swat, W., Brugge, J.S., Requirements for vav guanine nucleotide exchange factors and Rho GTPases in FcγR- and complement-mediated phagocytosis. Immunity 24 (2006), 305–316.
22. Ishihara, D., Dovas, A., Park, H., Isaac, B.M., Cox, D., The chemotactic defect in Wiskott-Aldrich syndrome macrophages is due to the reduced persistence of directional protrusions. PLoS One, 7, 2012, e30033.
23. Ishizaki, T., Uehata, M., Tamechika, I., Keel, J., Nonomura, K., Maekawa, M., Narumiya, S., Pharmacological properties of Y-27632, a specific inhibitor of rho-associated kinases. Mol. Pharmacol. 57 (2000), 976–983.
24. Jay, P.Y., Pham, P.A., Wong, S.A., Elson, E.L., A mechanical function of myosin II in cell motility. J. Cell Sci. 108 (1995), 387–393.
25. Kheir, W.A., Gevrey, J.-C., Yamaguchi, H., Isaac, B., Cox, D., A WAVE2-Abi1 complex mediates CSF-1-induced F-actin-rich membrane protrusions and migration in macrophages. J. Cell Sci. 118 (2005), 5369–5379.
26. King, S.J., Asokan, S.B., Haynes, E.M., Zimmerman, S.P., Rotty, J.D., Alb, J.G., Tagliatela, A., Blake, D.R., Lebedeva, I.P., Marston, D., et al. Lamellipodia are crucial for haptotactic sensing and response. J. Cell Sci. 129 (2016), 2329–2342.
27. Koh, T.J., DiPietro, L.A., Inflammation and wound healing: the role of the macrophage. Expert Rev. Mol. Med., 13, 2011, e23.
28. Kong, F., García, A.J., Mould, A.P., Humphries, M.J., Zhu, C., Demonstration of catch bonds between an integrin and its ligand. J. Cell Biol. 185 (2009), 1275–1284.
29. Kong, F., Li, Z., Parks, W.M., Dumbauld, D.W., García, A.J., Mould, A.P., Humphries, M.J., Zhu, C., Cyclic mechanical reinforcement of integrin-ligand interactions. Mol. Cell 49 (2013), 1060–1068.
30. Kovacs, E.M., Verma, S., Ali, R.G., Ratheesh, A., Hamilton, N.A., Akhmanova, A., Yap, A.S., N-WASP regulates the epithelial junctional actin cytoskeleton through a non-canonical post-nucleation pathway. Nat. Cell Biol. 13 (2011), 934–943.
31. Kovács, M., Tóth, J., Hetényi, C., Málnási-Csizmadia, A., Sellers, J.R., Mechanism of blebbistatin inhibition of myosin II. J. Biol. Chem. 279 (2004), 35557–35563.
32. Leithner, A., Eichner, A., Müller, J., Reversat, A., Brown, M., Schwarz, J., Merrin, J., de Gorter, D.J., Schur, F., Bayerl, J., et al. Diversified actin protrusions promote environmental exploration but are dispensable for locomotion of leukocytes. Nat. Cell Biol. 18 (2016), 1253–1259.
33. Lemière, J., Valentino, F., Campillo, C., Sykes, C., How cellular membrane properties are affected by the actin cytoskeleton. Biochimie 130 (2016), 33–40.
34. Machesky, L.M., Insall, R.H., Scar1 and the related Wiskott-Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex. Curr. Biol. 8 (1998), 1347–1356.
35. Machesky, L.M., Mullins, R.D., Higgs, H.N., Kaiser, D.A., Blanchoin, L., May, R.C., Hall, M.E., Pollard, T.D., Scar, a WASp-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc. Natl. Acad. Sci. USA 96 (1999), 3739–3744.
36. Machesky, L.M., May, R.C., Caron, E., Hall, A., Involvement of the Arp2/3 complex in phagocytosis mediated by FcgammaR or CR3. Nat. Cell Biol. 2 (2000), 246–248.
37. Nolen, B.J., Tomasevic, N., Russell, A., Pierce, D.W., Jia, Z., McCormick, C.D., Hartman, J., Sakowicz, R., Pollard, T.D., Characterization of two classes of small molecule inhibitors of Arp2/3 complex. Nature 460 (2009), 1031–1034.
38. Nolz, J.C., Medeiros, R.B., Mitchell, J.S., Zhu, P., Freedman, B.D., Shimizu, Y., Billadeau, D.D., WAVE2 regulates high-affinity integrin binding by recruiting vinculin and talin to the immunological synapse. Mol. Cell. Biol. 27 (2007), 5986–6000.
39. Olazabal, I.M., Caron, E., May, R.C., Schilling, K., Knecht, D.A., Machesky, L.M., Rho-kinase and myosin-II control phagocytic cup formation during CR, but not FcgammaR, phagocytosis. Curr. Biol. 12 (2002), 1413–1418.
40. Oudin, M.J., Jonas, O., Kosciuk, T., Broye, L.C., Guido, B.C., Wyckoff, J., Riquelme, D., Lamar, J.M., Asokan, S.B., Whittaker, C., et al. Tumor cell-driven extracellular matrix remodeling drives haptotaxis during metastatic progression. Cancer Discov. 6 (2016), 516–531.
41. Padrick, S.B., Doolittle, L.K., Brautigam, C.A., King, D.S., Rosen, M.K., Arp2/3 complex is bound and activated by two WASP proteins. Proc. Natl. Acad. Sci. USA 108 (2011), E472–E479.
42. Park, H., Cox, D., Cdc42 regulates Fc receptor-mediated phagocytosis through the activation and phosphorylation of Wiskott-Aldrich Syndrome Protein (WASP) and neural-WASP. Mol. Biol. Cell 20 (2009), 4500–4508.
43. Park, H., Cox, D., Syk regulates multiple signaling pathways leading to CX3CL1 chemotaxis in macrophages. J. Biol. Chem. 286 (2011), 14762–14769.
44. Parkhurst, C.N., Yang, G., Ninan, I., Savas, J.N., Yates, J.R., Lafaille, J.J., Hempstead, B.L., Littman, D.R., Gan, W.-B., Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 155 (2013), 1596–1609.
45. Patel, P.C., Harrison, R.E., Membrane ruffles capture C3bi-opsonized particles in activated macrophages. Mol. Biol. Cell 19 (2008), 4628–4639.
46. Paul, N.R., Allen, J.L., Chapman, A., Morlan-Mairal, M., Zindy, E., Jacquemet, G., Fernandez del Ama, L., Ferizovic, N., Green, D.M., Howe, J.D., et al. α5β1 integrin recycling promotes Arp2/3-independent cancer cell invasion via the formin FHOD3. J. Cell Biol. 210 (2015), 1013–1031.
47. Piotrowski, J.T., Gomez, T.S., Schoon, R.A., Mangalam, A.K., Billadeau, D.D., WASH knockout T cells demonstrate defective receptor trafficking, proliferation, and effector function. Mol. Cell. Biol. 33 (2013), 958–973.
48. Pollard, T.D., Marchand, J.-B., Kaiser, D.A., Higgs, H.N., Interaction of WASP/Scar proteins with actin and vertebrate Arp2/3 complex. Nat. Cell Biol. 3 (2001), 76–82.
49. Price, J., Vance, R., The macrophage paradox. Immunity 41 (2014), 685–693.
50. Proctor, R.A., Fibronectin: an enhancer of phagocyte function. Clin. Infect. Dis. 9 (1987), S412–S419.
51. Rotty, J.D., Wu, C., Haynes, E.M., Suarez, C., Winkelman, J.D., Johnson, H.E., Haugh, J.M., Kovar, D.R., Bear, J.E., Profilin-1 serves as a gatekeeper for actin assembly by Arp2/3-dependent and -independent pathways. Dev. Cell 32 (2015), 54–67.
52. Rougerie, P., Miskolci, V., Cox, D., Generation of membrane structures during phagocytosis and chemotaxis of macrophages: role and regulation of the actin cytoskeleton. Immunol. Rev. 256 (2013), 222–239.
53. Seaman, M.N.J., The retromer complex - endosomal protein recycling and beyond. J. Cell Sci. 125 (2012), 4693–4702.
54. Serrano, M., Lee, H., Chin, L., Cordon-Cardo, C., Beach, D., DePinho, R.A., Role of the INK4a locus in tumor suppression and cell mortality. Cell 85 (1996), 27–37.
55. Serrels, B., Serrels, A., Brunton, V.G., Holt, M., McLean, G.W., Gray, C.H., Jones, G.E., Frame, M.C., Focal adhesion kinase controls actin assembly via a FERM-mediated interaction with the Arp2/3 complex. Nat. Cell Biol. 9 (2007), 1046–1056.
56. Shi, C., Pamer, E.G., Monocyte recruitment during infection and inflammation. Nat. Rev. Immunol. 11 (2011), 762–774.
57. Suarez, C., Kovar, D.R., Internetwork competition for monomers governs actin cytoskeleton organization. Nat. Rev. Mol. Cell Biol. 17 (2016), 799–810.
58. Svitkina, T.M., Ultrastructure of protrusive actin filament arrays. Curr. Opin. Cell Biol. 25 (2013), 574–581.
59. Svitkina, T.M., Borisy, G.G., Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J. Cell Biol. 145 (1999), 1009–1026.
60. Swaminathan, V., Fischer, R.S., Waterman, C.M., The FAK-Arp2/3 interaction promotes leading edge advance and haptosensing by coupling nascent adhesions to lamellipodia actin. Mol. Biol. Cell 27 (2016), 1085–1100.
61. Thevenaz, P., Ruttimann, U.E., Unser, M., A pyramid approach to subpixel registration based on intensity. IEEE Trans. Image Process. 7 (1998), 27–41.
62. Thrasher, A.J., Burns, S.O., WASP: a key immunological multitasker. Nat. Rev. Immunol. 10 (2010), 182–192.
63. Ti, S.-C., Jurgenson, C.T., Nolen, B.J., Pollard, T.D., Structural and biochemical characterization of two binding sites for nucleation-promoting factor WASp-VCA on Arp2/3 complex. Proc. Natl. Acad. Sci. USA 108 (2011), E463–E471.
64. Tzircotis, G., Braga, V.M.M., Caron, E., RhoG is required for both FcγR- and CR3-mediated phagocytosis. J. Cell Sci. 124 (2011), 2897–2902.
65. Vargas, P., Maiuri, P., Bretou, M., Sáez, P.J., Pierobon, P., Maurin, M., Chabaud, M., Lankar, D., Obino, D., Terriac, E., et al. Innate control of actin nucleation determines two distinct migration behaviours in dendritic cells. Nat. Cell Biol. 18 (2015), 43–53.
66. Wheeler, A.P., Wells, C.M., Smith, S.D., Vega, F.M., Henderson, R.B., Tybulewicz, V.L., Ridley, A.J., Rac1 and Rac2 regulate macrophage morphology but are not essential for migration. J. Cell Sci. 119 (2006), 2749–2757.
67. Wu, C., Asokan, S.B., Berginski, M.E., Haynes, E.M., Sharpless, N.E., Griffith, J.D., Gomez, S.M., Bear, J.E., Arp2/3 is critical for lamellipodia and response to extracellular matrix cues but is dispensable for chemotaxis. Cell 148 (2012), 973–987.
68. Zech, T., Calaminus, S.D.J., Caswell, P., Spence, H.J., Carnell, M., Insall, R.H., Norman, J., Machesky, L.M., The Arp2/3 activator WASH regulates 5 1-integrin-mediated invasive migration. J. Cell Sci. 124 (2011), 3753–3759.
69. Zicha, D., Allen, W.E., Brickell, P.M., Kinnon, C., Dunn, G.A., Jones, G.E., Thrasher, A.J., Chemotaxis of macrophages is abolished in the Wiskott-Aldrich syndrome. Br. J. Haematol. 101 (1998), 659–665.