IQGAP1 is a novel phosphatidylinositol 4,5 bisphosphate effector in regulation of directional cell migration

EMBO Journal

Volumn 32, Issue 19, 2013, Pages 2617-2630

  Choi, Suyong ^a   Thapa, Narendra ^a   Hedman, Andrew C ^a   Li, Zhigang ^b   Sacks, David B ^b   Anderson, Richard A ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

cell migration; IQGAP1; PIP2; PIPKIg; polybasic motif

Indexed keywords

GROWTH FACTOR RECEPTOR; INTEGRIN; IQ MOTIF CONTAINING GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 1; MUTANT PROTEIN; PHOSPHATIDYLINOSITOL 4 PHOSPHATE 3 KINASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE;

ACTIN POLYMERIZATION; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION;

CELL LINE, TUMOR; CELL MOVEMENT; HUMANS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); RAS GTPASE-ACTIVATING PROTEINS;

EID: 84885177444     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.191     Document Type: Article

References (67)

1. Anderson RA, Boronenkov IV, Doughman SD, Kunz J, Loijens JC (1999) Phosphatidylinositol phosphate kinases, a multifaceted family of signaling enzymes. J Biol Chem 274: 9907-9910
2. Bairstow SF, Ling K, Su X, Firestone AJ, Carbonara C, Anderson RA (2006) Type Igamma661 phosphatidylinositol phosphate kinase directly interacts with AP2 and regulates endocytosis. J Biol Chem 281: 20632-20642
3. BaumgartnerM, Sillman AL, Blackwood EM, Srivastava J, Madson N, Schilling JW, Wright JH, Barber DL (2006) The Nck-interacting kinase phosphorylates ERM proteins for formation of lamellipodium by growth factors. Proc Natl Acad Sci USA 103: 13391-13396
4. Brandt DT, Grosse R (2007) Get to grips: steering local actin dynamics with IQGAPs. EMBO Rep 8: 1019-1023
5. Brandt DT, Marion S, Griffiths G, Watanabe T, Kaibuchi K, Grosse R (2007) Dia1 and IQGAP1 interact in cell migration and phagocytic cup formation. J Cell Biol 178: 193-200
6. Briggs MW, Li Z, Sacks DB (2002) IQGAP1-mediated stimulation of transcriptional co-activation by beta-catenin is modulated by calmodulin. J Biol Chem 277: 7453-7465
7. Brown MD, Sacks DB (2006) IQGAP1 in cellular signaling: bridging the GAP. Trends Cell Biol 16: 242-249
8. Catimel B, Schieber C, Condron M, Patsiouras H, Connolly L, Catimel J, Nice EC, Burgess AW, Holmes AB (2008) The PI(3,5)P2 and PI(4,5)P2 interactomes. J Proteome Res 7: 5295-5313
9. Chao WT, Daquinag AC, Ashcroft F, Kunz J (2010) Type I PIPK-alpha regulates directed cell migration by modulating Rac1 plasma membrane targeting and activation. J Cell Biol 190: 247-262
10. Czech MP (2000) PIP2 and PIP3: complex roles at the cell surface. Cell 100: 603-606
11. Del Pozo MA, Kiosses WB, Alderson NB, Meller N, Hahn KM, Schwartz MA (2002) Integrins regulate GTP-Rac localized effector interactions through dissociation of Rho-GDI. Nat Cell Biol 4: 232-239
12. Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443: 651-657
13. Dixon MJ, Gray A, Boisvert FM, Agacan M, Morrice NA, Gourlay R, Leslie NR, Downes CP, Batty IH (2011) A screen for novel phosphoinositide 3-kinase effector proteins. Mol Cell Proteomics 10: M110 003178
14. Dixon MJ, Gray A, Schenning M, Agacan M, Tempel W, Tong Y, Nedyalkova L, Park HW, Leslie NR, van Aalten DM, Downes CP, Batty IH (2012) IQGAP proteins reveal an atypical phosphoinositide (aPI) binding domain with a pseudo C2 domain fold. J Biol Chem 287: 22483-22496
15. Fukata M, Nakagawa M, Itoh N, Kawajiri A, Yamaga M, Kuroda S, Kaibuchi K (2001) Involvement of IQGAP1, an effector of Rac1 and Cdc42 GTPases, in cell-cell dissociation during cell scattering. Mol Cell Biol 21: 2165-2183
16. Fukata M, Watanabe T, Noritake J, Nakagawa M, Yamaga M, Kuroda S, Matsuura Y, Iwamatsu A, Perez F, Kaibuchi K (2002) Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell 109: 873-885
17. Gabev E, Kasianowicz J, Abbott T, McLaughlin S (1989) Binding of neomycin to phosphatidylinositol 4,5-bisphosphate (PIP2). Biochim Biophys Acta 979: 105-112
18. Golub T, Caroni P (2005) PI(4,5)P2-dependent microdomain assemblies capture microtubules to promote and control leading edge motility. J Cell Biol 169: 151-165
19. Good MC, Zalatan JG, Lim WA (2011) Scaffold proteins: hubs for controlling the flow of cellular information. Science 332: 680-686
20. Grohmanova K, Schlaepfer D, Hess D, Gutierrez P, Beck M, Kroschewski R (2004) Phosphorylation of IQGAP1 modulates its binding to Cdc42, revealing a new type of rho-GTPase regulator. J Biol Chem 279: 48495-48504
21. Halstead JR, Savaskan NE, van den Bout I, Van Horck F, Hajdo-Milasinovic A, Snell M, Keune WJ, Ten Klooster JP, Hordijk PL, Divecha N (2010) Rac controls PIP5K localisation and PtdIns(4,5)P synthesis, which modulates vinculin localisation and neurite dynamics. J Cell Sci 123(Pt 20): 3535-3546
22. Heck JN, Mellman DL, Ling K, Sun Y, Wagoner MP, Schill NJ, Anderson RA (2007) A conspicuous connection: structure defines function for the phosphatidylinositol-phosphate kinase family. Crit Rev Biochem Mol Biol 42: 15-39
23. Heo WD, Inoue T, Park WS, Kim ML, Park BO, Wandless TJ, Meyer T (2006) PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314: 1458-1461
24. Ho YD, Joyal JL, Li Z, Sacks DB (1999) IQGAP1 integrates Ca2\+/calmodulin and Cdc42 signaling. J Biol Chem 274: 464-470
25. Jadeski L, Mataraza JM, Jeong HW, Li Z, Sacks DB (2008) IQGAP1 stimulates proliferation and enhances tumorigenesis of human breast epithelial cells. J Biol Chem 283: 1008-1017
26. Johnson M, Sharma M, Henderson BR (2009) IQGAP1 regulation and roles in cancer. Cell Signal 21: 1471-1478
27. Keely PJ (2001) Ras and Rho protein induction of motility and invasion in T47D breast adenocarcinoma cells. Methods Enzymol 333: 256-266
28. Lammermann T, Renkawitz J, Wu X, Hirsch K, Brakebusch C, Sixt M (2009) Cdc42-dependent leading edge coordination is essential for interstitial dendritic cell migration. Blood 113: 5703-5710
29. Le Clainche C, Schlaepfer D, Ferrari A, Klingauf M, Grohmanova K, Veligodskiy A, Didry D, Le D, Egile C, Carlier MF, Kroschewski R (2007) IQGAP1 stimulates actin assembly through the N-WASPArp2/3 pathway. J Biol Chem 282: 426-435
30. Li R, Debreceni B, Jia B, Gao Y, Tigyi G, Zheng Y (1999) Localization of the PAK1-, WASP-, and IQGAP1-specifying regions of Cdc42. J Biol Chem 274: 29648-29654
31. Li Z, McNulty DE, Marler KJ, Lim L, Hall C, Annan RS, Sacks DB (2005) IQGAP1 promotes neurite outgrowth in a phosphorylation-dependent manner. J Biol Chem 280: 13871-13878
32. Li Z, Sacks DB (2003) Elucidation of the interaction of calmodulin with the IQ motifs of IQGAP1. J Biol Chem 278: 4347-4352
33. Ling K, Bairstow SF, Carbonara C, Turbin DA, Huntsman DG, Anderson RA (2007) Type I gamma phosphatidylinositol phosphate kinase modulates adherens junction and E-cadherin trafficking via a direct interaction with mu 1B adaptin. J Cell Biol 176: 343-353
34. Ling K, Doughman RL, Firestone AJ, Bunce MW, Anderson RA (2002) Type I gamma phosphatidylinositol phosphate kinase targets and regulates focal adhesions. Nature 420: 89-93
35. Ling K, Schill NJ, Wagoner MP, Sun Y, Anderson RA (2006) Movin' on up: the role of PtdIns(4,5)P(2) in cell migration. Trends Cell Biol 16: 276-284
36. Mao YS, Yin HL (2007) Regulation of the actin cytoskeleton by phosphatidylinositol 4-phosphate 5 kinases. Pflugers Arch 455: 5-18
37. Mataraza JM, Briggs MW, Li Z, Entwistle A, Ridley AJ, Sacks DB (2003) IQGAP1 promotes cell motility and invasion. J Biol Chem 278: 41237-41245
38. McLaughlin S, Murray D (2005) Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438: 605-611
39. McLaughlin S, Wang J, Gambhir A, Murray D (2002) PIP(2) and proteins: interactions, organization, and information flow. Annu Rev Biophys Biomol Struct 31: 151-175
40. Noritake J,Watanabe T, Sato K,Wang S, Kaibuchi K (2005) IQGAP1: a key regulator of adhesion and migration. J Cell Sci 118(Pt 10): 2085-2092
41. Osman M (2010) An emerging role for IQGAP1 in regulating protein traffic. ScientificWorldJournal 10: 944-953
42. Papayannopoulos V, Co C, Prehoda KE, Snapper S, Taunton J, Lim WA (2005) A polybasic motif allows N-WASP to act as a sensor of PIP(2) density. Mol Cell 17: 181-191
43. Parsons JT, Horwitz AR, Schwartz MA (2010) Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol 11: 633-643
44. Raucher D, Stauffer T, Chen W, Shen K, Guo S, York JD, Sheetz MP, Meyer T (2000) Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 100: 221-228
45. Ren JG, Li Z, Sacks DB (2007) IQGAP1 modulates activation of B-Raf. Proc Natl Acad Sci USA 104: 10465-10469
46. Ridley AJ (2011) Life at the leading edge. Cell 145: 1012-1022
47. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR (2003) Cell migration: integrating signals from front to back. Science 302: 1704-1709
48. Rodriguez OC, Schaefer AW, Mandato CA, Forscher P, Bement WM, Waterman-Storer CM (2003) Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat Cell Biol 5: 599-609
49. Rohatgi R, Ho HY, Kirschner MW (2000) Mechanism of N-WASP activation by CDC42 and phosphatidylinositol 4, 5-bisphosphate. J Cell Biol 150: 1299-1310
50. Sakurai-Yageta M, Recchi C, Le Dez G, Sibarita JB, Daviet L, Camonis J, D'Souza-Schorey C, Chavrier P (2008) The interaction of IQGAP1 with the exocyst complex is required for tumor cell invasion downstream of Cdc42 and RhoA. J Cell Biol 181: 985-998
51. Schill NJ, Anderson RA (2009) Two novel phosphatidylinositol-4-phosphate 5-kinase type Igamma splice variants expressed in human cells display distinctive cellular targeting. Biochem J 422: 473-482
52. Schramp M, Thapa N, Heck J, Anderson R (2011) PIPKIgamma regulates beta-catenin transcriptional activity downstream of growth factor receptor signaling. Cancer Res 71: 1282-1291
53. Sokol SY, Li Z, Sacks DB (2001) The effect of IQGAP1 on Xenopus embryonic ectoderm requires Cdc42. J Biol Chem 276: 48425-48430
54. Solon J, Levental I, Sengupta K, Georges PC, Janmey PA (2007) Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys J 93: 4453-4461
55. Sun Y, Ling K, Wagoner MP, Anderson RA (2007) Type I gamma phosphatidylinositol phosphate kinase is required for EGF-stimulated directional cell migration. J Cell Biol 178: 297-308
56. Sun Y, Turbin DA, Ling K, Thapa N, Leung S, Huntsman DG, Anderson RA (2010) Type I gamma phosphatidylinositol phosphate kinase modulates invasion and proliferation and its expression correlates with poor prognosis in breast cancer. Breast Cancer Res 12: R6
57. Thapa N, Sun Y, Schramp M, Choi S, Ling K, Anderson RA (2012) Phosphoinositide signaling regulates the exocyst complex and polarized integrin trafficking in directionally migrating cells. Dev Cell 22: 116-130
58. van den Bout I, Divecha N (2009) PIP5K-driven PtdIns(4,5)P2 synthesis: regulation and cellular functions. J Cell Sci 122(Pt 21): 3837-3850
59. Wang Y, Lian L, Golden JA, Morrisey EE, Abrams CS (2007) PIP5KI gamma is required for cardiovascular and neuronal development. Proc Natl Acad Sci USA 104: 11748-11753
60. Wang Y, Litvinov RI, Chen X, Bach TL, Lian L, Petrich BG, Monkley SJ, Kanaho Y, Critchley DR, Sasaki T, Birnbaum MJ, Weisel JW, Hartwig J, Abrams CS (2008) Loss of PIP5KIgamma, unlike other PIP5KI isoforms, impairs the integrity of the mem-brane cytoskeleton in murine megakaryocytes. J Clin Invest 118: 812-819
61. Wang YJ, Li WH, Wang J, Xu K, Dong P, Luo X, Yin HL (2004) Critical role of PIP5KI{gamma}87 in InsP3-mediated Ca(2\+) signaling. J Cell Biol 167: 1005-1010
62. Watanabe T, Noritake J, Kaibuchi K (2005) Regulation of microtubules in cell migration. Trends Cell Biol 15: 76-83
63. Watanabe T, Wang S, Noritake J, Sato K, Fukata M, Takefuji M, Nakagawa M, Izumi N, Akiyama T, Kaibuchi K (2004) Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. Dev Cell 7: 871-883
64. White CD, Brown MD, Sacks DB (2009) IQGAPs in cancer: a family of scaffold proteins underlying tumorigenesis. FEBS Lett 583: 1817-1824
65. White CD, Erdemir HH, Sacks DB (2012) IQGAP1 and its binding proteins control diverse biological functions. Cell Signal 24: 826-834
66. Yin HL, Janmey PA (2003) Phosphoinositide regulation of the actin cytoskeleton. Annu Rev Physiol 65: 761-789
67. Zhang L, Mao YS, Janmey PA, Yin HL (2012) Phosphatidylinositol 4, 5 bisphosphate and the actin cytoskeleton. Subcell Biochem 59: 177-215