The mammalian actin-binding protein 1 (mAbp1): A novel molecular player in leukocyte biology

Trends in Cell Biology

Volumn 21, Issue 4, 2011, Pages 247-255

  Schymeinsky, Jürgen ^a   Sperandio, Markus ^a   Walzog, Barbara ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; ACTIN DEPOLYMERIZING FACTOR; ACTIN DEPOLYMERIZING FACTOR HOMOLOGY; B LYMPHOCYTE RECEPTOR; BETA2 INTEGRIN; COMPLEMENT; CYTOSKELETON PROTEIN; INTEGRIN; MAMMALIAN ACTIN BINDING PROTEIN 1; PROTEIN KINASE SYK; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; T LYMPHOCYTE RECEPTOR; TALIN; UNCLASSIFIED DRUG; WISKOTT ALDRICH SYNDROME PROTEIN;

ANTIGEN PRESENTING CELL; APOPTOSIS; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL CYCLE ARREST; CELL FUNCTION; CELL MIGRATION; CELL STRUCTURE; CYTOLOGY; CYTOPLASM; CYTOSKELETON; DENDRITIC CELL; HUMAN; INFLAMMATION; LEUKOCYTE; LEUKOCYTE ADHERENCE; LYMPHOCYTE; MACROPHAGE; MAMMAL; MOLECULAR BIOLOGY; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ANIMALS; CELL ADHESION; CELL MOVEMENT; HUMANS; LEUKOCYTES; MICROFILAMENT PROTEINS; PROTEIN BINDING;

MAMMALIA;

EID: 79953161643     PISSN: 09628924     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tcb.2010.12.001     Document Type: Review

References (80)

1. Nathan C., Ding A. Nonresolving inflammation. Cell 2010, 140:871-882.
2. Nourshargh S., et al. Breaching multiple barriers: leukocyte motility through venular walls and the interstitium. Nat. Rev. Mol. Cell Biol. 2010, 11:366-378.
3. Burkhardt J.K., et al. The actin cytoskeleton in T cell activation. Annu. Rev. Immunol. 2008, 26:233-259.
4. Parsons J.T., et al. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat. Rev. Mol. Cell Biol. 2010, 11:633-643.
5. Abram C.L., Lowell C.A. The ins and outs of leukocyte integrin signaling. Annu. Rev. Immunol. 2009, 27:339-362.
6. Evans R., et al. Integrins in immunity. J. Cell Sci. 2009, 122:215-225.
7. Frommhold D., et al. RAGE and ICAM-1 cooperate in mediating leukocyte recruitment during acute inflammation in vivo. Blood 2010, 116:841-849.
8. Legate K.R., Fassler R. Mechanisms that regulate adaptor binding to β-integrin cytoplasmic tails. J. Cell Sci. 2009, 122:187-198.
9. Shattil S.J., et al. The final steps of integrin activation: the end game. Nat. Rev. Mol. Cell Biol. 2010, 11:288-300.
10. Moser M., et al. Kindlin-3 is required for beta2 integrin-mediated leukocyte adhesion to endothelial cells. Nat. Med. 2009, 15:300-305.
11. Harwood N.E., Batista F.D. Early events in B cell activation. Annu. Rev. Immunol. 2010, 28:185-210.
12. Arana E., et al. Regulation of integrin activation through the B-cell receptor. J. Cell Sci. 2008, 121:2279-2286.
13. Kessels M.M., et al. Association of mouse actin-binding protein 1 (mAbp1/SH3P7), an Src kinase target, with dynamic regions of the cortical actin cytoskeleton in response to Rac1 activation. Mol. Biol. Cell 2000, 11:393-412.
14. Paavilainen V.O., et al. Regulation of cytoskeletal dynamics by actin-monomer-binding proteins. Trend Cell Biol. 2004, 14:386-394.
15. Kaksonen M., et al. A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 2005, 123:305-320.
16. Kessels M.M., et al. Mammalian Abp1, a signal-responsive F-actin-binding protein, links the actin cytoskeleton to endocytosis via the GTPase dynamin. J. Cell Biol. 2001, 153:351-366.
17. Connert S., et al. SH3P7/mAbp1 deficiency leads to tissue and behavioral abnormalities and impaired vesicle transport. EMBO J. 2006, 25:1611-1622.
18. Luo B.H., et al. Structural basis of integrin regulation and signaling. Annu. Rev. Immunol. 2007, 25:619-647.
19. Alon R., Dustin M.L. Force as a facilitator of integrin conformational changes during leukocyte arrest on blood vessels and antigen-presenting cells. Immunity 2007, 26:17-27.
20. Shulman Z., et al. Lymphocyte crawling and transendothelial migration require chemokine triggering of high-affinity LFA-1 integrin. Immunity 2009, 30:384-396.
21. Phillipson M., et al. Intraluminal crawling of neutrophils to emigration sites: a molecularly distinct process from adhesion in the recruitment cascade. J. Exp. Med. 2006, 203:2569-2575.
22. Shimonaka M., et al. Rap1 translates chemokine signals to integrin activation, cell polarization, and motility across vascular endothelium under flow. J. Cell Biol. 2003, 161:417-427.
23. Sarantos M.R., et al. Transmigration of neutrophils across inflamed endothelium is signaled through LFA-1 and Src family kinase. J. Immunol. 2008, 181:8660-8669.
24. Schymeinsky J., et al. A fundamental role of mAbp1 in neutrophils: impact on β2 integrin-mediated phagocytosis and adhesion in vivo. Blood 2009, 114:4209-4220.
25. Cairo C.W., et al. Cytoskeletal regulation couples LFA-1 conformational changes to receptor lateral mobility and clustering. Immunity 2006, 25:297-308.
26. Zhu J., et al. Structure of a complete integrin ectodomain in a physiologic resting state and activation and deactivation by applied forces. Mol. Cell 2008, 32:849-861.
27. Phillipson M., et al. Vav1 is essential for mechanotactic crawling and migration of neutrophils out of the inflamed microvasculature. J. Immunol. 2009, 182:6870-6878.
28. Hou P., et al. Fgd1, the Cdc42 GEF responsible for faciogenital dysplasia, directly interacts with cortactin and mAbp1 to modulate cell shape. Hum. Mol. Genet. 2003, 12:1981-1993.
29. Ayala I., et al. Faciogenital dysplasia protein Fgd1 regulates invadopodia biogenesis and extracellular matrix degradation and is up-regulated in prostate and breast cancer. Canc. Res. 2009, 69:747-752.
30. Alon R., Ley K. Cells on the run: shear-regulated integrin activation in leukocyte rolling and arrest on endothelial cells. Curr. Opin. Cell Biol. 2008, 20:525-532.
31. Kuwano Y., et al. Rolling on E- or P-selectin induces the extended but not high-affinity conformation of LFA-1 in neutrophils. Blood 2010, 116:617-624.
32. Yago T., et al. E-selectin engages PSGL-1 and CD44 through a common signaling pathway to induce integrin αLβ2-mediated slow leukocyte rolling. Blood 2010, 116:485-494.
33. Zarbock A., et al. Spleen tyrosine kinase Syk is necessary for E-selectin-induced αLβ2 integrin-mediated rolling on intercellular adhesion molecule-1. Immunity 2007, 26:773-783.
34. Mocsai A., et al. The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat. Rev. Immunol. 2010, 10:387-402.
35. Frommhold D., et al. Spleen tyrosine kinase Syk is critical for sustained leukocyte adhesion during inflammation in vivo. BMC Immunol. 2007, 8:31.
36. Tucker K.L., et al. Proteomic analysis of resting and thrombin-stimulated platelets reveals the translocation and functional relevance of HIP-55 in platelets. Proteomics 2009, 9:4340-4354.
37. Swanson J.A. Shaping cups into phagosomes and macropinosomes. Nat. Rev. Mol. Cell Biol. 2008, 9:639-649.
38. Schymeinsky J., et al. The Vav binding site of the non-receptor tyrosine kinase Syk at Tyr 348 is critical for β2 integrin (CD11/CD18)-mediated neutrophil migration. Blood 2006, 108:3919-3927.
39. Schymeinsky J., et al. Syk-mediated translocation of PI3Kδ to the leading edge controls lamellipodium formation and migration of leukocytes. PLoS ONE 2007, 2:e1132.
40. Weber M., et al. Phospholipase C-γ2 and Vav cooperate within signaling microclusters to propagate B cell spreading in response to membrane-bound antigen. J. Exp. Med. 2008, 205:853-868.
41. Shi Y., et al. Protein-tyrosine kinase Syk is required for pathogen engulfment in complement-mediated phagocytosis. Blood 2006, 107:4554-4562.
42. Van Ziffle J.A., Lowell C.A. Neutrophil specific deletion of Syk kinase results in reduced host defense to bacterial infection. Blood 2009, 114:4871-4882.
43. Larbolette O., et al. SH3P7 Is a cytoskeleton adapter protein and is coupled to signal transduction from lymphocyte antigen receptors. Mol. Cell Biol. 1999, 19:1539-1546.
44. Lock P., et al. A new method for isolating tyrosine kinase substrates used to identify fish, an SH3 and PX domain-containing protein, and Src substrate. EMBO J. 1998, 17:4346-4357.
45. Larive R.M., et al. Phosphoproteomic analysis of Syk kinase signaling in human cancer cells reveals its role in cell-cell adhesion. Oncogene 2009, 28:2337-2347.
46. Han J., et al. The SH3 domain-containing adaptor HIP-55 mediates c-Jun N-terminal kinase activation in T cell receptor signaling. J. Biol. Chem. 2003, 278:52195-52202.
47. Han J., et al. HIP-55 is important for T-cell proliferation, cytokine production, and immune responses. Mol. Cell Biol. 2005, 25:6869-6878.
48. Le Bras S., et al. Abl-SH3 binding protein 2, 3BP2, interacts with CIN85 and HIP-55. FEBS Lett. 2007, 581:967-974.
49. Onabajo O.O., et al. Actin-binding protein 1 regulates B cell receptor-mediated antigen processing and presentation in response to B cell receptor activation. J. Immunol. 2008, 180:6685-6695.
50. Le Bras S., et al. Recruitment of the actin-binding protein HIP-55 to the immunological synapse regulates T cell receptor signaling and endocytosis. J. Biol. Chem. 2004, 279:15550-15560.
51. Peterson E.J., et al. Coupling of the TCR to integrin activation by Slap-130/Fyb. Science 2001, 293:2263-2265.
52. Yuan M., et al. Fyn binding protein, Fyb, interacts with mammalian actin binding protein, mAbp1. FEBS Lett. 2005, 579:2339-2347.
53. Le Roux D., et al. Syk-dependent actin dynamics regulate endocytic trafficking and processing of antigens internalized through the B-cell receptor. Mol. Biol. Cell 2007, 18:3451-3462.
54. Thrasher A.J., Burns S.O. WASP: a key immunological multitasker. Nat. Rev. Immunol. 2010, 10:182-192.
55. Lu T.T., Cyster J.G. Integrin-mediated long-term B cell retention in the splenic marginal zone. Science 2002, 297:409-412.
56. Pinyol R., et al. Regulation of N-WASP and the Arp2/3 complex by Abp1 controls neuronal morphology. PLoS ONE 2007, 2:e400.
57. Schaff U.Y., et al. Calcium flux in neutrophils synchronizes β2 integrin adhesive and signaling events that guide inflammatory recruitment. Ann. Biomed. Eng. 2008, 36:632-646.
58. Moser M., et al. The tail of integrins, talin, and kindlins. Science 2009, 324:895-899.
59. Cortesio C.L., et al. Actin binding protein-1 interacts with WIP to regulate growth factor-induced dorsal ruffle formation. Mol. Biol. Cell 2009, 21:186-197.
60. Chen Y.R., et al. Caspase-mediated cleavage of actin-binding and SH3-domain-containing proteins cortactin, HS1, and HIP-55 during apoptosis. Biochem. Biophys. Res. Commun. 2001, 288:981-989.
61. Denis F.M., et al. PRAM-1 potentiates arsenic trioxide-induced JNK activation. J. Biol. Chem. 2005, 280:9043-9048.
62. Geiger B., et al. Environmental sensing through focal adhesions. Nat. Rev. Mol. Cell Biol. 2009, 10:21-33.
63. Giannone G., et al. Multi-level molecular clutches in motile cell processes. Trend Cell Biol. 2009, 19:475-486.
64. Caswell P.T., et al. Integrins: masters and slaves of endocytic transport. Nat. Rev. Mol. Cell Biol. 2009, 10:843-853.
65. Fabbri M., et al. Dynamic partitioning into lipid rafts controls the endo-exocytic cycle of the αL/β2 integrin, LFA-1, during leukocyte chemotaxis. Mol. Biol. Cell 2005, 16:5793-5803.
66. Fazi B., et al. Unusual binding properties of the SH3 domain of the yeast actin-binding protein Abp1: structural and functional analysis. J. Biol. Chem. 2002, 277:5290-5298.
67. Goode B.L., et al. Activation of the Arp2/3 complex by the actin filament binding protein Abp1p. J. Cell Biol. 2001, 153:627-634.
68. Stollar E.J., et al. Structural, functional, and bioinformatic studies demonstrate the crucial role of an extended peptide binding site for the SH3 domain of yeast Abp1p. J. Biol. Chem. 2009, 284:26918-26927.
69. Gourlay C.W., et al. An interaction between Sla1p and Sla2p plays a role in regulating actin dynamics and endocytosis in budding yeast. J. Cell Sci. 2003, 116:2551-2564.
70. Boomer J.S., Tan T.H. Functional interactions of HPK1 with adaptor proteins. J. Cell Biochem. 2005, 95:34-44.
71. Fenster S.D., et al. Interactions between Piccolo and the actin/dynamin-binding protein Abp1 link vesicle endocytosis to presynaptic active zones. J. Biol. Chem. 2003, 278:20268-20277.
72. Qualmann B., et al. Linkage of the actin cytoskeleton to the postsynaptic density via direct interactions of Abp1 with the ProSAP/Shank family. J. Neurosci. 2004, 24:2481-2495.
73. Haynes J., et al. The biologically relevant targets and binding affinity requirements for the function of the yeast actin-binding protein 1 Src-homology 3 domain vary with genetic context. Genetics 2007, 176:193-208.
74. Gottfried I., et al. The Sla2p/HIP1/HIP1R family: similar structure, similar function in endocytosis. Biochem. Soc. Trans. 2010, 38:187-191.
75. Shamri R., et al. Lymphocyte arrest requires instantaneous induction of an extended LFA-1 conformation mediated by endothelium-bound chemokines. Nat. Immunol. 2005, 6:497-506.
76. Lim J., et al. An essential role for talin during αMβ2-mediated phagocytosis. Mol. Biol. Cell 2007, 18:976-985.
77. Lee S.E., et al. Force-induced activation of talin and its possible role in focal adhesion mechanotransduction. J. Biomech. 2007, 40:2096-2106.
78. del Rio A., et al. Stretching single talin rod molecules activates vinculin binding. Science 2009, 323:638-641.
79. Zhang H., et al. Impaired integrin-dependent function in Wiskott-Aldrich syndrome protein-deficient murine and human neutrophils. Immunity 2006, 25:285-295.
80. Anton I.M., et al. WASP-interacting protein (WIP): working in polymerisation and much more. Trend Cell Biol. 2007, 11:555-562.