Abl family kinases regulate FcγR-mediated phagocytosis in murine macrophages

Journal of Immunology

Volumn 189, Issue 11, 2012, Pages 5382-5392

  Greuber, Emileigh K ^a   Pendergast, Ann Marie ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; ARGININE KINASE; FC RECEPTOR; IMATINIB; PROTEIN KINASE SYK; ZYMOSAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CROSS LINKING; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ERYTHROCYTE; FLOW CYTOMETRY; GENETIC TRANSFECTION; IMMUNOPRECIPITATION; INTERNALIZATION; MACROPHAGE; MICROSCOPY; MOLECULAR CLONING; MOUSE; NONHUMAN; PERITONITIS; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHEEP;

ANIMALS; ERYTHROCYTES; GENE EXPRESSION REGULATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MACROPHAGES; MACROPHAGES, PERITONEAL; MICE; PHAGOCYTOSIS; PHOSPHORYLATION; PIPERAZINES; PRIMARY CELL CULTURE; PROTEIN BINDING; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-ABL; PYRIMIDINES; RECEPTORS, IGG; SHEEP; SIGNAL TRANSDUCTION;

EID: 84869792698     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200974     Document Type: Article

References (74)

1. Cox, D., and S. Greenberg. 2001. Phagocytic signaling strategies: Fc(gamma) receptor-mediated phagocytosis as a model system. Semin. Immunol. 13: 339-345. (Pubitemid 33121959)
2. Indik, Z. K., J. G. Park, S. Hunter, and A. D. Schreiber. 1995. The molecular dissection of Fc gamma receptor mediated phagocytosis. Blood 86: 4389-4399.
3. Flannagan, R. S., V. Jaumouillé, and S. Grinstein. 2012. The cell biology of phagocytosis. Annu. Rev. Pathol. 7: 61-98.
4. Bruhns, P. 2012. Properties of mouse and human IgG receptors and their contribution to disease models. Blood 119: 5640-5649.
5. Daëron, M. 1997. Fc receptor biology. Annu. Rev. Immunol. 15: 203-234.
6. Gomez, F., P. Ruiz, and A. D. Schreiber. 1994. Impaired function of macrophage Fc gamma receptors and bacterial infection in alcoholic cirrhosis. N. Engl. J. Med. 331: 1122-1128. (Pubitemid 24321217)
7. Ruiz, P., F. Gomez, and A. D. Schreiber. 1990. Impaired function of macrophage Fc gamma receptors in end-stage renal disease. N. Engl. J. Med. 322: 717-722. (Pubitemid 20092806)
8. Ravetch, J. V., and S. Bolland. 2001. IgG Fc receptors. Annu. Rev. Immunol. 19: 275-290. (Pubitemid 32368037)
9. Strzelecka, A., K. Kwiatkowska, and A. Sobota. 1997. Tyrosine phosphorylation and Fcgamma receptor-mediated phagocytosis. FEBS Lett. 400: 11-14. (Pubitemid 27046812)
10. DeFranco, A. L. 1995. Transmembrane signaling by antigen receptors of B and T lymphocytes. Curr. Opin. Cell Biol. 7: 163-175.
11. Meng, F., and C. A. Lowell. 1997. Lipopolysaccharide (LPS)-induced macrophage activation and signal transduction in the absence of Src-family kinases Hck, Fgr, and Lyn. J. Exp. Med. 185: 1661-1670. (Pubitemid 27203262)
12. Fitzer-Attas, C. J., M. Lowry, M. T. Crowley, A. J. Finn, F. Meng, A. L. DeFranco, and C. A. Lowell. 2000. Fcgamma receptor-mediated phagocytosis in macrophages lacking the Src family tyrosine kinases Hck, Fgr, and Lyn. J. Exp. Med. 191: 669-682.
13. Matsuda, M., J. G. Park, D. C. Wang, S. Hunter, P. Chien, and A. D. Schreiber. 1996. Abrogation of the Fc gamma receptor IIA-mediated phagocytic signal by stem-loop Syk antisense oligonucleotides. Mol. Biol. Cell 7: 1095-1106. (Pubitemid 26244206)
14. Crowley, M. T., P. S. Costello, C. J. Fitzer-Attas, M. Turner, F. Meng, C. Lowell, V. L. Tybulewicz, and A. L. DeFranco. 1997. A critical role for Syk in signal transduction and phagocytosis mediated by Fcgamma receptors on macrophages. J. Exp. Med. 186: 1027-1039. (Pubitemid 27441147)
15. Kiefer, F., J. Brumell, N. Al-Alawi, S. Latour, A. Cheng, A. Veillette, S. Grinstein, and T. Pawson. 1998. The Syk protein tyrosine kinase is essential for Fcgamma receptor signaling in macrophages and neutrophils. Mol. Cell. Biol. 18: 4209-4220. (Pubitemid 28287944)
16. Majeed, M., E. Caveggion, C. A. Lowell, and G. Berton. 2001. Role of Src kinases and Syk in Fcgamma receptor-mediated phagocytosis and phagosomelysosome fusion. J. Leukoc. Biol. 70: 801-811. (Pubitemid 33127015)
17. Pendergast, A. M. 2002. The Abl family kinases: mechanisms of regulation and signaling. Adv. Cancer Res. 85: 51-100.
18. Van Etten, R. A., P. K. Jackson, D. Baltimore, M. C. Sanders, P. T. Matsudaira, and P. A. Janmey. 1994. The COOH terminus of the c-Abl tyrosine kinase contains distinct F- and G-actin binding domains with bundling activity. J. Cell Biol. 124: 325-340.
19. Wang, Y., A. L. Miller, M. S. Mooseker, and A. J. Koleske. 2001. The Abl-related gene (Arg) nonreceptor tyrosine kinase uses two F-actin-binding domains to bundle F-actin. Proc. Natl. Acad. Sci. USA 98: 14865-14870. (Pubitemid 34013936)
20. Bradley, W. D., and A. J. Koleske. 2009. Regulation of cell migration and morphogenesis by Abl-family kinases: emerging mechanisms and physiological contexts. J. Cell Sci. 122: 3441-3454.
21. Zandy, N. L., M. Playford, and A. M. Pendergast. 2007. Abl tyrosine kinases regulate cell-cell adhesion through Rho GTPases. Proc. Natl. Acad. Sci. USA 104: 17686-17691. (Pubitemid 350210895)
22. Li, R., and A. M. Pendergast. 2011. Arg kinase regulates epithelial cell polarity by targeting β1-integrin and small GTPase pathways. Curr. Biol. 21: 1534-1542.
23. Gu, J. J., C. P. Lavau, E. Pugacheva, E. J. Soderblom, M. A. Moseley, and A. M. Pendergast. 2012. Abl family kinases modulate T cell-mediated inflammation and chemokine-induced migration through the adaptor HEF1 and the GTPase Rap1. Sci. Signal. 5: ra51.
24. Smith-Pearson, P. S., E. K. Greuber, G. Yogalingam, and A. M. Pendergast. 2010. Abl kinases are required for invadopodia formation and chemokine-induced invasion. J. Biol. Chem. 285: 40201-40211.
25. Koleske, A. J., A. M. Gifford, M. L. Scott, M. Nee, R. T. Bronson, K. A. Miczek, and D. Baltimore. 1998. Essential roles for the Abl and Arg tyrosine kinases in neurulation. Neuron 21: 1259-1272. (Pubitemid 29022529)
26. Tybulewicz, V. L., C. E. Crawford, P. K. Jackson, R. T. Bronson, and R. C. Mulligan. 1991. Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl proto-oncogene. Cell 65: 1153-1163. (Pubitemid 121001329)
27. Zipfel, P. A., W. Zhang, M. Quiroz, and A. M. Pendergast. 2004. Requirement for Abl kinases in T cell receptor signaling. Curr. Biol. 14: 1222-1231. (Pubitemid 38991808)
28. Zipfel, P. A., M. Grove, K. Blackburn, M. Fujimoto, T. F. Tedder, and A. M. Pendergast. 2000. The c-Abl tyrosine kinase is regulated downstream of the B cell antigen receptor and interacts with CD19. J. Immunol. 165: 6872-6879. (Pubitemid 32001156)
29. Gu, J. J., J. R. Ryu, and A. M. Pendergast. 2009. Abl tyrosine kinases in T-cell signaling. Immunol. Rev. 228: 170-183.
30. Huang, Y., E. O. Comiskey, R. S. Dupree, S. Li, A. J. Koleske, and J. K. Burkhardt. 2008. The c-Abl tyrosine kinase regulates actin remodeling at the immune synapse. Blood 112: 111-119.
31. Silberman, I., R. V. Sionov, V. Zuckerman, S. Haupt, Z. Goldberg, A. Strasser, Z. S. Ben-Sasson, M. Baniyash, A. J. Koleske, and Y. Haupt. 2008. T cell survival and function requires the c-Abl tyrosine kinase. Cell Cycle 7: 3847-3857.
32. Gu, J. J., N. Zhang, Y. W. He, A. J. Koleske, and A. M. Pendergast. 2007. Defective T cell development and function in the absence of Abelson kinases. J. Immunol. 179: 7334-7343.
33. Cui, L., C. Chen, T. Xu, J. Zhang, X. Shang, J. Luo, L. Chen, X. Ba, and X. Zeng. 2009. c-Abl kinase is required for beta 2 integrin-mediated neutrophil adhesion. J. Immunol. 182: 3233-3242.
34. Baruzzi, A., I. Iacobucci, S. Soverini, C. A. Lowell, G. Martinelli, and G. Berton. 2010. c-Abl and Src-family kinases cross-talk in regulation of myeloid cell migration. FEBS Lett. 584: 15-21.
35. Baruzzi, A., and G. Berton. 2012. The tyrosine kinase Abl is a component of macrophage podosomes and is required for podosome formation and function. Eur. J. Immunol. In press.
36. Plattner, R., B. J. Irvin, S. Guo, K. Blackburn, A. Kazlauskas, R. T. Abraham, J. D. York, and A. M. Pendergast. 2003. A new link between the c-Abl tyrosine kinase and phosphoinositide signalling through PLC-gamma1. Nat. Cell Biol. 5: 309-319. (Pubitemid 36432295)
37. Moresco, E. M., S. Donaldson, A. Williamson, and A. J. Koleske. 2005. Integrin-mediated dendrite branch maintenance requires Abelson (Abl) family kinases. J. Neurosci. 25: 6105-6118. (Pubitemid 40923477)
38. Plattner, R., L. Kadlec, K. A. DeMali, A. Kazlauskas, and A. M. Pendergast. 1999. c-Abl is activated by growth factors and Src family kinases and has a role in the cellular response to PDGF. Genes Dev. 13: 2400-2411. (Pubitemid 29453611)
39. Fabian, M. A., W. H. Biggs, III, D. K. Treiber, C. E. Atteridge, M. D. Azimioara, M. G. Benedetti, T. A. Carter, P. Ciceri, P. T. Edeen, M. Floyd, et al. 2005. A small molecule-kinase interaction map for clinical kinase inhibitors. Nat. Biotechnol. 23: 329-336. (Pubitemid 41094421)
40. Taylor, J. R., N. Brownlow, J. Domin, and N. J. Dibb. 2006. FMS receptor for MCSF (CSF-1) is sensitive to the kinase inhibitor imatinib and mutation of Asp-802 to Val confers resistance. Oncogene 25: 147-151. (Pubitemid 43050013)
41. Choi, Y., M. A. Seeliger, S. B. Panjarian, H. Kim, X. Deng, T. Sim, B. Couch, A. J. Koleske, T. E. Smithgall, and N. S. Gray. 2009. N-myristoylated c-Abl tyrosine kinase localizes to the endoplasmic reticulum upon binding to an allosteric inhibitor. J. Biol. Chem. 284: 29005-29014.
42. Zhang, J., F. J. Adrián, W. Jahnke, S. W. Cowan-Jacob, A. G. Li, R. E. Iacob, T. Sim, J. Powers, C. Dierks, F. Sun, et al. 2010. Targeting Bcr-Abl by combining allosteric with ATP-binding-site inhibitors. Nature 463: 501-506.
43. de Jong, R., J. ten Hoeve, N. Heisterkamp, and J. Groffen. 1997. Tyrosine 207 in CRKL is the BCR/ABL phosphorylation site. Oncogene 14: 507-513. (Pubitemid 27090952)
44. Clausen, B. E., C. Burkhardt, W. Reith, R. Renkawitz, and I. Förster. 1999. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8: 265-277. (Pubitemid 29523965)
45. Swanson, J. A. 2008. Shaping cups into phagosomes and macropinosomes. Nat. Rev. Mol. Cell Biol. 9: 639-649.
46. Berton, G., A. Mócsai, and C. A. Lowell. 2005. Src and Syk kinases: key regulators of phagocytic cell activation. Trends Immunol. 26: 208-214. (Pubitemid 41556858)
47. Calalb, M. B., T. R. Polte, and S. K. Hanks. 1995. Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases. Mol. Cell. Biol. 15: 954-963.
48. Raeder, E. M., P. J. Mansfield, V. Hinkovska-Galcheva, J. A. Shayman, and L. A. Boxer. 1999. Syk activation initiates downstream signaling events during human polymorphonuclear leukocyte phagocytosis. J. Immunol. 163: 6785-6793.
49. Geahlen, R. L. 2009. Syk and pTyr'd: Signaling through the B cell antigen receptor. Biochim. Biophys. Acta 1793: 1115-1127.
50. Zhang, J., M. L. Billingsley, R. L. Kincaid, and R. P. Siraganian. 2000. Phosphorylation of Syk activation loop tyrosines is essential for Syk function. An in vivo study using a specific anti-Syk activation loop phosphotyrosine antibody. J. Biol. Chem. 275: 35442-35447.
51. Shiue, L., M. J. Zoller, and J. S. Brugge. 1995. Syk is activated by phosphotyrosine-containing peptides representing the tyrosine-based activation motifs of the high affinity receptor for IgE. J. Biol. Chem. 270: 10498-10502.
52. Keshvara, L. M., C. C. Isaacson, T. M. Yankee, R. Sarac, M. L. Harrison, and R. L. Geahlen. 1998. Syk- and Lyn-dependent phosphorylation of Syk on multiple tyrosines following B cell activation includes a site that negatively regulates signaling. J. Immunol. 161: 5276-5283. (Pubitemid 28519087)
53. El-Hillal, O., T. Kurosaki, H. Yamamura, J. P. Kinet, and A. M. Scharenberg. 1997. syk kinase activation by a src kinase-initiated activation loop phosphorylation chain reaction. Proc. Natl. Acad. Sci. USA 94: 1919-1924. (Pubitemid 27113937)
54. Burton, E. A., R. Plattner, and A. M. Pendergast. 2003. Abl tyrosine kinases are required for infection by Shigella flexneri. EMBO J. 22: 5471-5479. (Pubitemid 37279956)
55. Burton, E. A., T. N. Oliver, and A. M. Pendergast. 2005. Abl kinases regulate actin comet tail elongation via an N-WASP-dependent pathway. Mol. Cell. Biol. 25: 8834-8843. (Pubitemid 41429075)
56. Burton, E. A., A. M. Pendergast, and A. Aballay. 2006. The Caenorhabditis elegans ABL-1 tyrosine kinase is required for Shigella flexneri pathogenesis. Appl. Environ. Microbiol. 72: 5043-5051. (Pubitemid 44078837)
57. Elwell, C. A., A. Ceesay, J. H. Kim, D. Kalman, and J. N. Engel. 2008. RNA interference screen identifies Abl kinase and PDGFR signaling in Chlamydia trachomatis entry. PLoS Pathog. 4: e1000021.
58. Harmon, B., N. Campbell, and L. Ratner. 2010. Role of Abl kinase and the Wave2 signaling complex in HIV-1 entry at a post-hemifusion step. PLoS Pathog. 6: e1000956.
59. Swimm, A. I., W. Bornmann, M. Jiang, M. J. Imperiale, A. E. Lukacher, and D. Kalman. 2010. Abl family tyrosine kinases regulate sialylated ganglioside receptors for polyomavirus. J. Virol. 84: 4243-4251.
60. Wetzel, D. M., D. McMahon-Pratt, and A. J. Koleske. 2012. The Abl and Arg kinases mediate distinct modes of phagocytosis and are required for maximal Leishmania infection. Mol. Cell. Biol. 32: 3176-3186.
61. Lowell, C. A. 2011. Src-family and Syk kinases in activating and inhibitory pathways in innate immune cells: signaling cross talk. Cold Spring Harb. Perspect. Biol. 3: 3.
62. Brdicka, T., T. A. Kadlecek, J. P. Roose, A. W. Pastuszak, and A. Weiss. 2005. Intramolecular regulatory switch in ZAP-70: analogy with receptor tyrosine kinases. Mol. Cell. Biol. 25: 4924-4933. (Pubitemid 40781094)
63. Chen, C., X. Shang, T. Xu, L. Cui, J. Luo, X. Ba, S. Hao, and X. Zeng. 2007. c-Abl is required for the signaling transduction induced by L-selectin ligation. Eur. J. Immunol. 37: 3246-3258. (Pubitemid 350131303)
64. Lee, W. L., G. Cosio, K. Ireton, and S. Grinstein. 2007. Role of CrkII in Fcgamma receptor-mediated phagocytosis. J. Biol. Chem. 282: 11135-11143. (Pubitemid 47100794)
65. Park, H., and D. Cox. 2009. Cdc42 regulates Fc gamma receptor-mediated phagocytosis through the activation and phosphorylation of Wiskott-Aldrich syndrome protein (WASP) and neural-WASP. Mol. Biol. Cell 20: 4500-4508.
66. Tsuboi, S., and J. Meerloo. 2007. Wiskott-Aldrich syndrome protein is a key regulator of the phagocytic cup formation in macrophages. J. Biol. Chem. 282: 34194-34203. (Pubitemid 350159472)
67. Torres, E., and M. K. Rosen. 2003. Contingent phosphorylation/ dephosphorylation provides a mechanism of molecular memory in WASP. Mol. Cell 11: 1215-1227. (Pubitemid 36645141)
68. Rhee, C. K., J. W. Kim, C. K. Park, J. S. Kim, J. Y. Kang, S. J. Kim, S. C. Kim, S. S. Kwon, Y. K. Kim, S. H. Park, and S. Y. Lee. 2011. Effect of imatinib on airway smooth muscle thickening in a murine model of chronic asthma. Int. Arch. Allergy Immunol. 155: 243-251.
69. Eklund, K. K., K. Lindstedt, C. Sandler, P. T. Kovanen, L. Laasonen, A. Juurikivi, H.Wolff, M. Mykkänen, and H. Joensuu. 2008. Maintained efficacy of the tyrosine kinase inhibitor imatinib mesylate in a patient with rheumatoid arthritis. J. Clin. Rheumatol. 14: 294-296.
70. Huang, P., X. S. Zhao, M. Fields, R. M. Ransohoff, and L. Zhou. 2009. Imatinib attenuates skeletal muscle dystrophy in mdx mice. FASEB J. 23: 2539-2548.
71. Sadanaga, A., H. Nakashima, K. Masutani, K. Miyake, S. Shimizu, T. Igawa, N. Sugiyama, H. Niiro, H. Hirakata, and M. Harada. 2005. Amelioration of autoimmune nephritis by imatinib in MRL/lpr mice. Arthritis Rheum. 52: 3987-3996. (Pubitemid 41798238)
72. Dewar, A. L., K. V. Doherty, T. P. Hughes, and A. B. Lyons. 2005. Imatinib inhibits the functional capacity of cultured human monocytes. Immunol. Cell Biol. 83: 48-56. (Pubitemid 40179401)
73. Rix, U., O. Hantschel, G. Dürnberger, L. L. Remsing Rix, M. Planyavsky, N. V. Fernbach, I. Kaupe, K. L. Bennett, P. Valent, J. Colinge, et al. 2007. Chemical proteomic profiles of the BCR-ABL inhibitors imatinib, nilotinib, and dasatinib reveal novel kinase and nonkinase targets. Blood 110: 4055-4063. (Pubitemid 350248462)
74. Nakamura, A., T. Kubo, and T. Takai. 2008. Fc receptor targeting in the treatment of allergy, autoimmune diseases and cancer. Adv. Exp. Med. Biol. 640: 220-233.