IQGAP1: A microtubule-microfilament scaffolding protein with multiple roles in nerve cell development and synaptic plasticity

Histology and Histopathology

Volumn 27, Issue 11, 2012, Pages 1385-1394

  Jausoro, Ignacio ^a   Mestres, Iván ^a   Remedi, Mónica ^a   Sanchez, Mónica ^a   Cáceres, Alfredo ^a  

^a INSTITUTO DE INVESTIGACIÓN MÉDICA MERCEDES Y MARTÍN FERREYRA   (Argentina)

Author keywords

Cytoskeleton; IQGAP1; Neurons; Plasticity; Signaling

Indexed keywords

GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; IQ MOTIF CONTAINING GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 1;

ANIMAL; GENETICS; METABOLISM; NERVE CELL; NERVE CELL PLASTICITY; REVIEW;

ANIMALS; NEURONAL PLASTICITY; NEURONS; RAS GTPASE-ACTIVATING PROTEINS;

EID: 84869480370     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (80)

1. Akhamanova A. and Hoogenraad C.C. (2005). Microtubule plus-endtracking proteins: mechanisms and functions. Curr. Op. Cell Biol. 17, 47-54.
2. Akhamanova A., Hoogenraad C.C., Drabek K., Stepanova T., Dortland B., Vermeulen T., Burgerin B.M., De Zeeuew C.L., Grosveld F. and Galjart N. (2001). Clasps are Clip-115 and-170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 104, 923-935.
3. Alvarez-Buylla A. and Garcia-Verdugo J.M. (2002). Neurogenesis in adult subventricular zone. J. Neurosci. 22, 629-634.
4. Arimura N. and Kaibuchi K. (2007). Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat. Rev. Neurosci. 8, 194-205.
5. Balenci L., Saoudi Y., Grunwald D., Deloulme J.C., Bernards A. and Baudier J. (2007). IQGAP1 Regulates Adult Neural Progenitors In Vivo and Vascular Endothelial Growth Factor-Triggered Neural Progenitor Migration In Vitro. J. Neurosci. 27, 4716-4724.
6. Barnes A. and Polleux F. (2009). Establishment of axon-dendritic polarity in developing neurons. Annu. Rev. Neurosci. 32, 347-381.
7. Barth A.I., Näthke I.S. and Nelson J.W. (1992). Cadherins, catenins and APC protein: interplay between cytoskeletal complexes and signaling pathways. Curr. Op. Cell Biol. 9, 683-690.
8. Bashour A.M., Fullertton A.G., Hart M.J. and Bloom G.S. (1997). IQGAP1, a Rac-and Cdc42-binding protein, directly binds and cross-links microfilaments. J. Cell Biol. 137, 1555-1566.
9. Benseñor L.B., Kan H.M., Wang N., Wallrabe H., Davidson L.A., Cai Y., Schafer D.A. and Bloom G.S. (2007). IQGAP1 regulates cell motility by linking growth factor signaling to actin assembly. J. Cell Sci. 120, 658-669.
10. Bisbal M., Conde C., Donoso M., Bollati F., Sesma J., Díaz Añel A., Quiroga S., Malhotra V., Marzolo M.P. and Cáceres A. (2008). Protein kinase D regulates trafficking of dendritic membrane proteins in developing neurons. J. Neurosci. 28, 9297-9308.
11. Bishop A.L. and Hall A. (2000). RhoGTPases and their effector proteins. Biochem. J. 348, 241-255.
12. Bourguignon L.Y. (2008). Hyaluronan-mediated CD44 activation of Rho-GTPase signaling and cytoskeletal function promotes tumor progression. Sem. Cancer Biol. 18, 251-259.
13. Bourguignon L.Y., Gilad E., Rothman K. and Peyrollier K. (2005). Hyaluronan-CD44 interaction with IQGAP1 promotes Cdc42 and ERK signaling, leading to actin binding, Elk-1/estrogen receptor transcriptional activation, and ovarian cancer progression. J. Biol. Chem. 280, 11961-11972.
14. Briggs M.W. and Sacks D.B. (2003). IQGAP proteins are integral components of cytoskeletal regulation. EMBO Rep. 4, 571-574.
15. Brill S., Li S., Lyman C.W., Church D.M., Wasmuth J.J., Weissbach L., Bernards A. and Sinjders A. (1996). The Ras GTPase-activatingprotein-related human protein IQGAP2 harbors a potential actin binding domain and interacts with calmodulin and Rho family GTPases. Mol. Cell. Biol. 16, 4869-4878.
16. Brown M.D. and Sacks D.B. (2006). IQGAP1 in cellular signaling: bridging the gap. Trends Cell Biol. 16, 242-249.
17. Conde C. and Cáceres A. (2009). Microtubule dynamics in axons, dendrites and at the synapse. Nat. Rev. Neurosci. 10, 319-332.
18. Conde C., Arias C., Robin M., Li A., Saito M., Chuang J.Z., Nairn A.C., Sung C.H. and Cáceres A. (2010). Evidence for the involvement of Lfc and Tctex-1 in axon formation. J. Neurosci. 30, 6793-6800.
19. Craig A.M. and Banker G. (1994). Neuronal polarity. Annu. Rev. Neurosci. 17, 267-310.
20. Dotti C.G., Sullivan C.A. and Banker G.A. (1988). The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8, 1454-1468.
21. Etienne-Manneville S. and Hall A. (2002). RhoGTPases in cell biology. Nature 420, 629-634.
22. Fukata M., Kuroda S., Fujii K., Nakamura T., Shoji I., Matsuura Y., Okawa K., Iwamatsu A., Kikuchi A. and Kaibuchi K. (1997). Regulation of crosslinking of actin filaments by IQGAP1, a target of Cdc42. J. Biol. Chem. 272, 29579-29583.
23. Fukata M., Watanabe T., Noritake J., Nakagawa M., Yamaga M., Kuroda S., Matsuura Y., Perez F. and Kaibuchi K. (2002). Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell 109, 873-885.
24. Fukata M., Nakagawa M. and Kaibuchi K. (2003). Roles of Rho-family GTPases in cell proliferation and directional migration. Curr. Op. Cell Biol. 15, 590-597.
25. Gao C., Frausto S.F., Guedea A., Tronson N., Jovasevic V., Leaderbrand K., Corcoran K., Guzman G., Swanson G.T. and Radulovic J. (2011). IQGAP1 regulates NR2A signaling, spine density, and cognitive processes. J. Neurosci. 31, 8533-8542.
26. Garcia Mata R., Boulter E. and Burridge K. (2011). The 'invisible hand': regulation of RHO GTPases by RHO GDIs. Nat. Rev. Mol. Cell. Biol. 12, 493-504.
27. Govek E., Newey S. and Van Aelst L. (2005). The role of the Rho GTPases in neuronal development. Genes Dev. 19, 1-49.
28. Gundersen G.G. (2002a). Evolutionary conservation of microtubulecapture mechanisms. Nat. Rev. Mol. Cell. Biol. 3, 296-304.
29. Gundersen G.G. (2002b). Microtubule capture: IQGAP and CLIP-170 expand the repertoire. Curr. Biol. 12, 645-647.
30. Hall A. (2009). The cytoskeleton and cancer. Cancer Metastasis Rev. 28, 5-14.
31. Hall A. and Lalli G. (2010). Rho and Ras GTPases in axon growth, guidance, and branching. Cold Spring Harb. Perspect. Biol. 2, a001818.
32. Hart M., Callow M., Souza B. and Polakis P. (1996). IQGAP1, a calmodulin-binding protein with a rasGAP-related domain, is a potential effector for cdc42Hs. EMBO J. 15, 2997-3005.
33. Hirotsune S., Fleck M.W., Gambello I., Bix G.J., Chen A., Clark G.D., Ledbetter D.H., McBain C.J. and Wynshaw-Boris A. (1998). Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nat. Gen. 19, 333-339.
34. Ho Y., Joyal J., Li Z. and Sacks D. (1999). IQGAP1 integrates Ca2+/calmodulin and Cdc42 signaling. J. Biol. Chem. 274, 464-470.
35. Hoogenraad C.C. and Bradke F. (2009). Control of neuronal polarity and plasticity-a renassaince for microtubules. Trend Cell Biol. 19, 669-672.
36. Hotulainen P. and Hoogenraad C.C. (2010). Actin in dendritic spines: connecting dynamics to function. J. Cell Biol. 189, 619-629.
37. Jan Y.N. and Jan L.Y. (2003). The control of dendritic development. Neuron 40, 229-242.
38. Jan Y.N. and Jan L.Y. (2010). Branching out: mechanisms of dendritic arborization. Nat. Rev. Neurosci. 11, 316-328.
39. Jaworski J., Spangler S., Seeburg D.P., Hoogenraad C.C. and Sheng M. (2005). Control of dendritic arborization by the phosphoinositide-3'-kinase-Akt mammalian target of rapamycin pathway. J. Neurosci. 25, 11300-11312.
40. Kemler R. (1993). From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion. Trends Gen. 9, 317-321.
41. Kholmanskikh S.S., Dobrin J.S., Wynshaw-Boris A., Letourneau P.C. and Ross M.E. (2003). Disregulated Rho GTPases and actin cytoskeleton contribute to the migration defect in Lis1-deficient neurons. J. Neurosci. 23, 8673-8681.
42. Kholmanskikh S.V., Koeller H.B., Wynshaw-Boris A., Gomez T., Letourneau P.C. and Ross M.E. (2006). Calcium-dependent interaction of Lis1 with IQGAP1 and Cdc42 promotes neuronal motility. Nat. Neurosci. 9, 50-57.
43. Korobova F. and Svitkina T. (2010). Molecular architecture of synaptic actin cytoskeleton in hippocampal neurons reveals a mechanism of dendritic spine morphogenesis. Mol. Biol. Cell 21, 165-176.
44. Kuroda S., Fukata M., Fujii K., Nakamura T., Izawa I. and Kaibuchi K. (1997). Regulation of cell-cell adhesion of MDCK cells by Cdc42 and Rac1 small GTPases. Biochem. Biophys. Res. Commun. 240, 430-435.
45. Kuroda S., Fukata M., Nakagawa M., Fujii K., Nakamura T., Ookubo T., Izawa I., Nagase T., Nomura N., Tani H., Shoji I., Matsuura Y., Yonehara S. and Kaibuchi K. (1998). Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherinmediated cell-cell adhesion. Science 281, 832-835.
46. Leventer R.J., Cardoso C., Ledbetter D.H. and Dobyns W.B. (2001). LIS1: from cortical malformation to essential protein to cellular dynamics. Trends Neurosci. 24, 489-492.
47. Li Z., McNulty D.E., Marker K.J.M., Lim L., Hal C., Annan R.S. and Sacks D.V. (2005). IQGAP1 promotes neurite outgrowth in a phosphorylation dependent manner. J. Biol. Chem. 280, 13871-13878.
48. Machesky L.M., Atkinson S.J., Ampe C., Vandekerckhove J. and Pollard T.D. (1994). Purification of a cortical complex containing two unconventional actins from Acanthamoeba by affinity chromatography on profilin agarose. J. Cell Biol. 127, 107-115.
49. Mataraza J.M., Briggs M.W., Li Z., Entwistle A., Ridley A.J. and Sacks D.B. (2003). IQGAP1 promotes cell motility and invasion. J. Biol. Chem. 278, 41237-41245.
50. Mataraza J.M., Li Z., Jeong H.W., Brown M.D. and Sacks D.B. (2007). Multiple proteins mediate IQGAP1 mediated cell migration. Cell Signal 19, 1857-1865.
51. Mimori-Kiyosue Y., Shiina N. and Tsukita S. (2000a). The dynamin behavior of the APC-binding protein EB1 on the distal ends of microtubules. Curr. Biol. 10, 865-868.
52. Mimori-Kiyosue Y., Shiina N. and Tsukita S. (2000b). Adenomatous polyposis coli (APC) protein moves along microtubules and concentrates at their growing ends in epithelial cells. J. Cell Biol. 148, 505-518.
53. Mimori-Kiyosue Y., Grigoriev I., Lansbergen G., Sasaki H., Matsui C., Severin F., Galjart N., Grosveld F., Vorobjev I., Tsukita S. and Akhmanova A. (2005). CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex. J. Cell Biol. 168, 141-153.
54. Montenegro C., Tortosa E., Rosso S., Peretti D., Bollati F., Bisbal M., Jausoro I., Avila J., Cáceres A. and Gonzalez-Billault C. (2010). MAP1B regulates axonal development by modulating Rho-GTPase Rac1 activity. Mol. Biol. Cell 21, 3518-3528.
55. Noritake J., Fukata M., Sato K., Nakagawa M., Watanabe T., Izumi N., Wang S., Fukata Y. and Kaibuchi K. (2004). Positive role of IQGAP1, an effector of Rac1, in actin-meshwork formation at sites of cell cell contact. Mol. Biol. Cell 15, 1065-1076.
56. Noritake J., Watanabe T., Sato K., Wang S. and Kaibuchi K. (2005). IQGAP1: a key regulator of adhesion and migration. J. Cell Sci. 118, 2085-2092.
57. Paglini G., Kunda K., Quiroga S., Kosik K. and Cáceres A. (1998). Suppression of radixin and moesin alters growth cone morphology, motility and process formation in primary cultured neurons. J. Cell Biol. 143, 443-455.
58. Parsons J., Horwitz A. and Swartz M. (2010). Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat. Rev. Mol. Cell. Biol. 11, 633-643.
59. Perez F., Diamantopoulos G.S., Stalder R. and Kreis T.E. (1999). CLIP-170 highlights growing microtubule ends in vivo. Cell 96, 517-527.
60. Pertz O. (2010). Spatio-temporal Rho GTPase signaling-where are we now? J. Cell Sci. 123, 1841-1850.
61. Phillips-Mason P.J., Gates T.J., Major D.L., Sacks D.B. and Brady-Kalnay S.M. (2006). The receptor protein-tyrosine phosphatase PTPμ interacts with IQGAP1. J. Biol. Chem. 281, 4903-4910.
62. Pollard T. and Borisy G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465.
63. Rossman K., Der C. and Sondek J. (2005). GEF means go: turning on RHO GTPases with guanine nucleotide exchange factors. Nat. Rev. Mol. Cell. Biol. 6, 167-189.
64. Roy M., Li Z. and Sacks D.B. (2004). IQGAP1 binds ERK2 and modulates its activity. J. Biol. Chem. 279, 17329-17337.
65. Roy M., Li Z. and Sacks D.B. (2005). IQGAP1 is a scaffold for mitogenactivated protein kinase signaling. Mol. Cell. Biol. 25, 7940-7952.
66. Scheffzek K., Ahmadian M. and Wittinghofer A. (1998). GTPaseactivating proteins: helping hands to complement an active site. Trends Biochem. Sci. 23, 257-262.
67. Schlessinger K., Hall A. and Tolwinski N. (2009). Wnt signaling pathways meet Rho GTPases. Genes Dev. 23, 265-277.
68. Schrick C., Fischer A., Srivastava D., Tronson N., Penzes P. and Radulovic J. (2007). N-cadherin regulates cytoskeletally associated IQGAP1/ERK signaling and memory formation. Neuron 55, 786-798.
69. Swiech L., Blazejczyk M., Urbanska M., Pietruszka P., Dortland B., Malik A., Wulf P., Hoogenraad C. and Jaworski J. (2011). CLIP-170 and IQGAP1 cooperatively regulate dendrite morphology. J. Neurosci. 31, 4555-4568.
70. Takeichi M. (1990). Cadherins: A molecular family important in selective cell-cell adhesion. Ann. Rev. Biochem. 59, 237-252.
71. Takeichi M. (1995). Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 7, 619-627.
72. Tsukita S., Tsukita S., Nagafuchi A. and Yonemura S. (1992). Molecular linkage between cadherins and actin filaments in cell-cell adherens junctions. Curr. Opin. Cell Biol. 4, 834-839.
73. Urban E., Jacob S., Nemethova M., Resch G.P. and Small V.J. (2010). Electron tomography reveals unbranched networks of actin filaments in lamellipodia. Nat. Cell Biol. 12, 429-435.
74. Wang S., Watanabe T., Noritake J., Fukata M., Yoshimura T., Itoh N., Harada T., Nakagawa M., Matsuura Y., Arimura N. and Kaibuchi K. (2007). IQGAP3, a novel effector of Rac1 and Cdc42, regulates neurite outgrowth. J. Cell Sci. 120, 567-577.
75. Watanabe T., Wang S., Noritake J., Sato K., Fukata M., Takefuji M., Nakagawa M., Izumi N., Akiyama T. and Kaibuchi K. (2004). Interaction with IQGAP1 links APC to rac1, cdc42, and actin filaments during cell polarization and migration. Dev. Cell 7, 871-883.
76. Watanabe T., Noritake J. and Kaibuchi K. (2005). Roles of IQGAP1 in cell polarization and migration. Novartis Found. Symp. 269, 92-101.
77. Watanabe T., Noritake J., Kakeno M., Matsui T., Harada T., Itoh N., Sato K., Matsuzawa K., Iwamatsu A., Galjart N. and Kaibuchi K. (2009). Phosphorylation of CLASP2 by GSK-3' regulates its interaction with IQGAP1, EB1 and microtubules. J. Cell Sci. 122, 2969-2979.
78. Weissbach L., Settleman L., Kalady M., Snijders A., Murthy A., Yan Y. and Bernards A. (1994). Identification of a human ras GAP-related protein containing calmodulin-binding motifs. J. Biol. Chem. 269, 20517-20521.
79. Yamaoka-Tojo M., Ushio-Fukai M., Hilenski L., Dikalov S.I., Chen Y.E., Tojo T., Fukai T., Fujimoto M., Patrushev N.A., Wang N., Kontos C.D., Bloom G.S. and Alexander R.W. (2004). IQGAP1, a Novel Vascular Endothelial Growth Factor Receptor Binding Protein, Is Involved in Reactive Oxygen Species Dependent Endothelial Migration and Proliferation. Cir. Res. 95, 276-283.
80. Ydenberg C.A., Smith B.A., Breitsprecher D., Gelles J. and Goode B.L. (2011). Cease-fire at the leading edge: New perspectives on actin filament branching, debranching, and cross-linking. Cytoskeleton (Hoboken) 68, 596-602.