The cytoskeletal adaptor protein IQGAP1 regulates TCR-mediated signaling and filamentous actin dynamics

Journal of Immunology

Volumn 188, Issue 12, 2012, Pages 6135-6144

  Gorman, Jacquelyn A ^a   Babich, Alexander ^b   Dick, Christopher J ^a   Schoon, Renee A ^a   Koenig, Alexander ^c   Gomez, Timothy S ^a,c   Burkhardt, Janis K ^b   Billadeau, Daniel D ^a,c  

^a MAYO GRADUATE SCHOOL   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; GAMMA INTERFERON; INTERLEUKIN 2; IQ MOTIF CONTAINING GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 1; MESSENGER RNA; T LYMPHOCYTE RECEPTOR;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BIOACCUMULATION; CARBOXY TERMINAL SEQUENCE; CD8+ T LYMPHOCYTE; CELL MATURATION; CONTROLLED STUDY; FEMALE; GENE; GENE EXPRESSION REGULATION; IFN GAMMA GENE; IL 2 GENE; IMMUNOMODULATION; IMMUNOREGULATION; INTRACELLULAR SIGNALING; MALE; MICROTUBULE ORGANIZING CENTER; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; T LYMPHOCYTE ACTIVATION; THYMOCYTE;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; BLOTTING, WESTERN; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CYTOSKELETON; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; RAS GTPASE-ACTIVATING PROTEINS; RECEPTORS, ANTIGEN, T-CELL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84862626038     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1103487     Document Type: Article

References (65)

1. Campi, G., R. Varma, and M. L. Dustin. 2005. Actin and agonist MHC-peptide complex-dependent T cell receptor microclusters as scaffolds for signaling. J. Exp. Med. 202: 1031-1036.
2. Gomez, T. S., and D. D. Billadeau. 2008. T cell activation and the cytoskeleton: you can't have one without the other. Adv. Immunol. 97: 1-64. (Pubitemid 351711631)
3. Valitutti, S., M. Dessing, K. Aktories, H. Gallati, and A. Lanzavecchia. 1995. Sustained signaling leading to T cell activation results from prolonged T cell receptor occupancy. Role of T cell actin cytoskeleton. J. Exp. Med. 181: 577-584.
4. Holsinger, L. J., I. A. Graef, W. Swat, T. Chi, D. M. Bautista, L. Davidson, R. S. Lewis, F. W. Alt, and G. R. Crabtree. 1998. Defects in actin-cap formation in Vav-deficient mice implicate an actin requirement for lymphocyte signal transduction. Curr. Biol. 8: 563-572. (Pubitemid 28222890)
5. Stinchcombe, J. C., E. Majorovits, G. Bossi, S. Fuller, and G. M. Griffiths. 2006. Centrosome polarization delivers secretory granules to the immunological synapse. Nature 443: 462-465. (Pubitemid 44477283)
6. Nolz, J. C., T. S. Gomez, P. Zhu, S. Li, R. B. Medeiros, Y. Shimizu, J. K. Burkhardt, B. D. Freedman, and D. D. Billadeau. 2006. The WAVE2 complex regulates actin cytoskeletal reorganization and CRAC-mediated calcium entry during T cell activation. Curr. Biol. 16: 24-34. (Pubitemid 43049883)
7. Nolz, J. C., M. E. Fernandez-Zapico, and D. D. Billadeau. 2007. TCR/CD28- stimulated actin dynamics are required for NFAT1-mediated transcription of c-rel leading to CD28 response element activation. J. Immunol. 179: 1104-1112.
8. Suetsugu, S., H. Miki, and T. Takenawa. 1999. Identification of two human WAVE/SCAR homologues as general actin regulatory molecules which associate with the Arp2/3 complex. Biochem. Biophys. Res. Commun. 260: 296-302. (Pubitemid 29351823)
9. Huang, Y., and J. K. Burkhardt. 2007. T-cell-receptor-dependent actin regulatory mechanisms. J. Cell Sci. 120: 723-730. (Pubitemid 46523474)
10. Zeng, R., J. L. Cannon, R. T. Abraham, M. Way, D. D. Billadeau, J. Bubeck-Wardenberg, and J. K. Burkhardt. 2003. SLP-76 coordinates Nck-dependent Wiskott-Aldrich syndrome protein recruitment with Vav-1/Cdc42-dependent Wiskott-Aldrich syndrome protein activation at the T cell-APC contact site. J. Immunol. 171: 1360-1368. (Pubitemid 36900068)
11. Snapper, S. B., and F. S. Rosen. 1999. The Wiskott-Aldrich syndrome protein (WASP): roles in signaling and cytoskeletal organization. Annu. Rev. Immunol. 17: 905-929. (Pubitemid 29241143)
12. Gomez, T. S., S. D. McCarney, E. Carrizosa, C. M. Labno, E. O. Comiskey, J. C. Nolz, P. Zhu, B. D. Freedman, M. R. Clark, D. J. Rawlings, et al. 2006. HS1 functions as an essential actin-regulatory adaptor protein at the immune synapse. Immunity 24: 741-752. (Pubitemid 43867363)
13. Brandt, D. T., and R. Grosse. 2007. Get to grips: steering local actin dynamics with IQGAPs. EMBO Rep. 8: 1019-1023. (Pubitemid 350042336)
14. White, C. D., M. D. Brown, and D. B. Sacks. 2009. IQGAPs in cancer: a family of scaffold proteins underlying tumorigenesis. FEBS Lett. 583: 1817-1824.
15. Weissbach, L., J. Settleman, M. F. Kalady, A. J. Snijders, A. E. Murthy, Y. X. Yan, and A. Bernards. 1994. Identification of a human rasGAP-related protein containing calmodulin-binding motifs. J. Biol. Chem. 269: 20517-20521.
16. Noritake, J., T. Watanabe, K. Sato, S. Wang, and K. Kaibuchi. 2005. IQGAP1: a key regulator of adhesion and migration. J. Cell Sci. 118: 2085-2092. (Pubitemid 40872832)
17. Roy, M., Z. Li, and D. B. Sacks. 2004. IQGAP1 binds ERK2 and modulates its activity. J. Biol. Chem. 279: 17329-17337. (Pubitemid 38560493)
18. Roy, M., Z. Li, and D. B. Sacks. 2005. IQGAP1 is a scaffold for mitogen-activated protein kinase signaling. Mol. Cell. Biol. 25: 7940-7952. (Pubitemid 41262989)
19. Ren, J.-G., Z. Li, and D. B. Sacks. 2007. IQGAP1 modulates activation of B-Raf. Proc. Natl. Acad. Sci. USA 104: 10465-10469. (Pubitemid 47185688)
20. McCallum, S. J., W. J. Wu, and R. A. Cerione. 1996. Identification of a putative effector for Cdc42Hs with high sequence similarity to the RasGAP-related protein IQGAP1 and a Cdc42Hs binding partner with similarity to IQGAP2. J. Biol. Chem. 271: 21732-21737. (Pubitemid 26303788)
21. Kuroda, S., M. Fukata, K. Kobayashi, M. Nakafuku, N. Nomura, A. Iwamatsu, and K. Kaibuchi. 1996. Identification of IQGAP as a putative target for the small GTPases, Cdc42 and Rac1. J. Biol. Chem. 271: 23363-23367. (Pubitemid 26314782)
22. Hart, M. J., M. G. Callow, B. Souza, and P. Polakis. 1996. IQGAP1, a calmodulin- binding protein with a rasGAP-related domain, is a potential effector for cdc42Hs. EMBO J. 15: 2997-3005. (Pubitemid 26187748)
23. Yamaoka-Tojo, M., M. Ushio-Fukai, L. Hilenski, S. I. Dikalov, Y. E. Chen, T. Tojo, T. Fukai, M. Fujimoto, N. A. Patrushev, N. Wang, et al. 2004. IQGAP1, a novel vascular endothelial growth factor receptor binding protein, is involved in reactive oxygen species - dependent endothelial migration and proliferation. Circ. Res. 95: 276-283. (Pubitemid 39056288)
24. Watanabe, T., S. Wang, J. Noritake, K. Sato, M. Fukata, M. Takefuji, M. Nakagawa, N. Izumi, T. Akiyama, and K. Kaibuchi. 2004. Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. Dev. Cell 7: 871-883. (Pubitemid 39654731)
25. Watanabe, T., J. Noritake, and K. Kaibuchi. 2005. Roles of IQGAP1 in cell polarization and migration. Novartis Found. Symp. 269: 92-101; discussion 101-105, 223-230.
26. Mataraza, J. M., M. W. Briggs, Z. Li, A. Entwistle, A. J. Ridley, and D. B. Sacks. 2003. IQGAP1 promotes cell motility and invasion. J. Biol. Chem. 278: 41237-41245. (Pubitemid 37280951)
27. Li, Z., S. H. Kim, J. M. Higgins, M. B. Brenner, and D. B. Sacks. 1999. IQGAP1 and calmodulin modulate E-cadherin function. J. Biol. Chem. 274: 37885-37892. (Pubitemid 30026855)
28. Drees, F., S. Pokutta, S. Yamada, W. J. Nelson, and W. I. Weis. 2005. Alphacatenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly. Cell 123: 903-915. (Pubitemid 41721035)
29. Verma, S., A. M. Shewan, J. A. Scott, F. M. Helwani, N. R. den Elzen, H. Miki, T. Takenawa, and A. S. Yap. 2004. Arp2/3 activity is necessary for efficient formation of E-cadherin adhesive contacts. J. Biol. Chem. 279: 34062-34070. (Pubitemid 39063058)
30. Sahai, E., and C. J. Marshall. 2002. ROCK and Dia have opposing effects on adherens junctions downstream of Rho. Nat. Cell Biol. 4: 408-415. (Pubitemid 34746158)
31. Pelikan-Conchaudron, A., C. Le Clainche, D. Didry, and M.-F. Carlier. 2011. The IQGAP1 protein is a calmodulin-regulated barbed end capper of actin filaments: possible implications in its function in cell migration. J. Biol. Chem. 286: 35119-35128.
32. Brandt, D. T., S. Marion, G. Griffiths, T. Watanabe, K. Kaibuchi, and R. Grosse. 2007. Dia1 and IQGAP1 interact in cell migration and phagocytic cup formation. J. Cell Biol. 178: 193-200. (Pubitemid 47076456)
33. Le Clainche, C., D. Schlaepfer, A. Ferrari, M. Klingauf, K. Grohmanova, A. Veligodskiy, D. Didry, D. Le, C. Egile, M.-F. Carlier, and R. Kroschewski. 2007. IQGAP1 stimulates actin assembly through the N-WASP-Arp2/3 pathway. J. Biol. Chem. 282: 426-435. (Pubitemid 47076652)
34. Weissbach, L., A. Bernards, and D. W. Herion. 1998. Binding of myosin essential light chain to the cytoskeleton-associated protein IQGAP1. Biochem. Biophys. Res. Commun. 251: 269-276. (Pubitemid 28498101)
35. Fukata, M., T. Watanabe, J. Noritake, M. Nakagawa, M. Yamaga, S. Kuroda, Y. Matsuura, A. Iwamatsu, F. Perez, and K. Kaibuchi. 2002. Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell 109: 873-885. (Pubitemid 34786002)
36. Lansbergen, G., and A. Akhmanova. 2006. Microtubule plus end: a hub of cellular activities. Traffic 7: 499-507. (Pubitemid 44026748)
37. Sedwick, C. E., M. M. Morgan, L. Jusino, J. L. Cannon, J. Miller, and J. K. Burkhardt. 1999. TCR, LFA-1, and CD28 play unique and complementary roles in signaling T cell cytoskeletal reorganization. J. Immunol. 162: 1367-1375. (Pubitemid 29307007)
38. Williams, B. L., K. L. Schreiber, W. Zhang, R. L. Wange, L. E. Samelson, P. J. Leibson, and R. T. Abraham. 1998. Genetic evidence for differential coupling of Syk family kinases to the T-cell receptor: reconstitution studies in a ZAP-70-deficient Jurkat T-cell line. Mol. Cell. Biol. 18: 1388-1399. (Pubitemid 28100903)
39. Karnitz, L., S. L. Sutor, T. Torigoe, J. C. Reed, M. P. Bell, D. J. McKean, P. J. Leibson, and R. T. Abraham. 1992. Effects of p56lck deficiency on the growth and cytolytic effector function of an interleukin-2-dependent cytotoxic T-cell line. Mol. Cell. Biol. 12: 4521-4530.
40. Gil, D., A. G. Schrum, M. A. Daniels, and E. Palmer. 2008. A role for CD8 in the developmental tuning of antigen recognition and CD3 conformational change. J. Immunol. 180: 3900-3909.
41. Gomez, T. S., M. J. Hamann, S. McCarney, D. N. Savoy, C. M. Lubking, M. P. Heldebrant, C. M. Labno, D. J. McKean, M. A. McNiven, J. K. Burkhardt, and D. D. Billadeau. 2005. Dynamin 2 regulates T cell activation by controlling actin polymerization at the immunological synapse. Nat. Immunol. 6: 261-270. (Pubitemid 41724763)
42. Gomez, T. S., K. Kumar, R. B. Medeiros, Y. Shimizu, P. J. Leibson, and D. D. Billadeau. 2007. Formins regulate the actin-related protein 2/3 complex-independent polarization of the centrosome to the immunological synapse. Immunity 26: 177-190. (Pubitemid 46329435)
43. Arneson, L. N., C. M. Segovis, T. S. Gomez, R. A. Schoon, C. J. Dick, Z. Lou, D. D. Billadeau, and P. J. Leibson. 2008. Dynamin 2 regulates granule exocytosis during NK cell-mediated cytotoxicity. J. Immunol. 181: 6995-7001.
44. Li, S., Q. Wang, A. Chakladar, R. T. Bronson, and A. Bernards. 2000. Gastric hyperplasia in mice lacking the putative Cdc42 effector IQGAP1. Mol. Cell. Biol. 20: 697-701. (Pubitemid 30023111)
45. Windebank, K. P., R. T. Abraham, G. Powis, R. A. Olsen, T. J. Barna, and P. J. Leibson. 1988. Signal transduction during human natural killer cell activation: inositol phosphate generation and regulation by cyclic AMP. J. Immunol. 141: 3951-3957.
46. Gomez, T. S., and D. D. Billadeau. 2009. A FAM21-containing WASH complex regulates retromer-dependent sorting. Dev. Cell 17: 699-711.
47. Zhang, J.-S., A. Koenig, A. Harrison, A. V. Ugolkov, M. E. Fernandez-Zapico, F. J. Couch, and D. D. Billadeau. 2011. Mutant K-Ras increases GSK-3β gene expression via an ETS-p300 transcriptional complex in pancreatic cancer. Oncogene 30: 3705-3715.
48. Bunnell, S. C., V. A. Barr, C. L. Fuller, and L. E. Samelson. 2003. Highr-esolution multicolor imaging of dynamic signaling complexes in T cells stimulated by planar substrates. Sci. STKE 2003: PL8.
49. Schmidt, V. A., C. S. Chiariello, E. Capilla, F. Miller, and W. F. Bahou. 2008. Development of hepatocellular carcinoma in Iqgap2-deficient mice is IQGAP1 dependent. Mol. Cell. Biol. 28: 1489-1502.
50. Sharma, S., G. M. Findlay, H. S. Bandukwala, S. Oberdoerffer, B. Baust, Z. Li, V. Schmidt, P. G. Hogan, D. B. Sacks, and A. Rao. 2011. Dephosphorylation of the nuclear factor of activated T cells (NFAT) transcription factor is regulated by an RNA-protein scaffold complex. Proc. Natl. Acad. Sci. USA 108: 11381-11386.
51. Bunnell, S. C., V. Kapoor, R. P. Trible, W. Zhang, and L. E. Samelson. 2001. Dynamic actin polymerization drives T cell receptor-induced spreading: a role for the signal transduction adaptor LAT. Immunity 14: 315-329. (Pubitemid 32289295)
52. Brown, M. D., and D. B. Sacks. 2006. IQGAP1 in cellular signaling: bridging the GAP. Trends Cell Biol. 16: 242-249. (Pubitemid 43744436)
53. Kanwar, N., and J. A. Wilkins. 2011. IQGAP1 involvement in MTOC and granule polarization in NK-cell cytotoxicity. Eur. J. Immunol. 41: 2763-2773.
54. Rak, G. D., E. M. Mace, P. P. Banerjee, T. Svitkina, and J. S. Orange. 2011. Natural killer cell lytic granule secretion occurs through a pervasive actin network at the immune synapse. PLoS Biol. 9: e1001151.
55. Sanborn, K. B., G. D. Rak, S. Y. Maru, K. Demers, A. Difeo, J. A. Martignetti, M. R. Betts, R. Favier, P. P. Banerjee, and J. S. Orange. 2009. Myosin IIA associates with NK cell lytic granules to enable their interaction with F-actin and function at the immunological synapse. J. Immunol. 182: 6969-6984.
56. Lyubchenko, T. A., G. A. Wurth, and A. Zweifach. 2003. The actin cytoskeleton and cytotoxic T lymphocytes: evidence for multiple roles that could affect granule exocytosis-dependent target cell killing. J. Physiol. 547: 835-847. (Pubitemid 36367366)
57. Beemiller, P., and M. F. Krummel. 2010. Mediation of T-cell activation by actin meshworks. Cold Spring Harb. Perspect. Biol. 2: a002444.
58. Li, Y.-C., B.-M. Chen, P.-C. Wu, T.-L. Cheng, L.-S. Kao, M.-H. Tao, A. Lieber, and S. R. Roffler. 2010. Cutting Edge: mechanical forces acting on T cells immobilized via the TCR complex can trigger TCR signaling. J. Immunol. 184: 5959-5963.
59. Acuto, O., V. Di Bartolo, and F. Michel. 2008. Tailoring T-cell receptor signals by proximal negative feedback mechanisms. Nat. Rev. Immunol. 8: 699-712.
60. Pathmanathan, S., E. Hamilton, E. Atcheson, and D. J. Timson. 2011. The interaction of IQGAPs with calmodulin-like proteins. Biochem. Soc. Trans. 39: 694-699.
61. Routray, C., C. Liu, U. Yaqoob, D. D. Billadeau, K. D. Bloch, K. Kaibuchi, V. H. Shah, and N. Kang. 2011. Protein kinase G signaling disrupts Rac1-dependent focal adhesion assembly in liver specific pericytes. Am. J. Physiol. Cell Physiol. 301: C66-C74.
62. Bear, J. E., T. M. Svitkina, M. Krause, D. A. Schafer, J. J. Loureiro, G. A. Strasser, I. V. Maly, O. Y. Chaga, J. A. Cooper, G. G. Borisy, and F. B. Gertler. 2002. Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109: 509-521. (Pubitemid 34564477)
63. Paul, A. S., and T. D. Pollard. 2009. Review of the mechanism of processive actin filament elongation by formins. Cell Motil. Cytoskeleton 66: 606-617.
64. Umemoto, R., N. Nishida, S. Ogino, and I. Shimada. 2010. NMR structure of the calponin homology domain of human IQGAP1 and its implications for the actin recognition mode. J. Biomol. NMR 48: 59-64.
65. Mateer, S. C., L. E. Morris, D. A. Cromer, L. B. Benseñor, and G. S. Bloom. 2004. Actin filament binding by a monomeric IQGAP1 fragment with a single calponin homology domain. Cell Motil. Cytoskeleton 58: 231-241. (Pubitemid 38989670)