Rho GTPases regulate PTPμ-mediated nasal neurite outgrowth and temporal repulsion of retinal ganglion cell neurons

Molecular and Cellular Neuroscience

Volumn 34, Issue 3, 2007, Pages 453-467

  Major, Denice L ^a   Brady Kalnay, Susann M ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Actin cytoskeleton; Axon guidance; Cell adhesion molecule; Receptor protein tyrosine phosphatase; Retinal ganglion cell; Rho GTPase; Tyrosine phosphorylation

Indexed keywords

PROTEIN CDC42; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE MU; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSAY; EMBRYO; ENZYME REGULATION; MOLECULE; NERVE CELL; NERVE FIBER GROWTH; NONHUMAN; NOSE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; RETINA GANGLION CELL;

ANIMALS; AUTOANTIGENS; CDC42 GTP-BINDING PROTEIN; CHICK EMBRYO; IMMUNOHISTOCHEMISTRY; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; NEURITES; ORGAN CULTURE TECHNIQUES; PROTEIN BINDING; PROTEIN-TYROSINE-PHOSPHATASE; RAC1 GTP-BINDING PROTEIN; RETINA; RETINAL GANGLION CELLS; RHO GTP-BINDING PROTEINS;

EID: 33847326752     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2006.11.022     Document Type: Article

References (91)

1. Aricescu A.R., Hon W.C., Siebold C., Lu W., van der Merwe P.A., and Jones E.Y. Molecular analysis of receptor protein tyrosine phosphatase mu-mediated cell adhesion. EMBO J. 25 (2006) 701-712
2. Baker M.W., and Macagno E.R. RNAi of the receptor tyrosine phosphatase HmLAR2 in a single cell of an intact leech embryo leads to growth-cone collapse. Curr. Biol. 10 (2000) 1071-1074
3. Baker M.W., and Macagno E.R. The role of a LAR-like receptor tyrosine phosphatase in growth cone collapse and mutual-avoidance by sibling processes. J. Neurobiol. 44 (2000) 194-203
4. Baker M.W., Rauth S.J., and Macagno E.R. Possible role of the receptor protein tyrosine phosphatase HmLAR2 in interbranch repulsion in a leech embryonic cell. J. Neurobiol. 45 (2000) 47-60
5. Bishop A.L., and Hall A. Rho GTPases and their effector proteins. Biochem. J. 348 Pt. 2 (2000) 241-255
6. Bixby J.L., and Jhabvala P. Extracellular matrix molecules and cell adhesion molecules induce neurites through different mechanisms. J. Cell Biol. 111 (1990) 2725-2732
7. Bixby J.L., and Jhabvala P. Inhibition of tyrosine phosphorylation potentiates substrate-induced neurite growth. J. Neurobiol. 23 (1992) 468-480
8. Bixby J.L., and Jhabvala P. Tyrosine phosphorylation in early embryonic growth cones. J. Neurosci. 13 (1993) 3421-3432
9. Brady-Kalnay S.M. Protein tyrosine phosphatases. In: Beckerle M. (Ed). Cell Adhesion: Frontiers in Molecular Biology (2001), Oxford Univ. Press, Oxford, UK 217-258
10. Brady-Kalnay S.M., and Tonks N.K. Identification of the homophilic binding site of the receptor protein tyrosine phosphatase PTP mu. J. Biol. Chem. 269 (1994) 28472-28477
11. Brady-Kalnay S.M., Boghaert E.R., Zimmer S., and Brackenbury R. Increasing N-CAM-mediated cell-cell adhesion does not reduce invasion of RSV-transformed WC5 rat cerebellar cells. Clin. Exp. Metastasis 11 (1993) 313-324
12. Brady-Kalnay S.M., Mourton T., Nixon J.P., Kinch M., Chen H., Brackenbury R., Rimm D.L., Del Vecchio R.L., and Tonks N.K. Dynamic interaction of PTPμ with multiple cadherins in vivo. J. Cell Biol. 141 (1998) 287-296
13. Briggs M.W., Li Z., and Sacks D.B. IQGAP1-mediated stimulation of transcriptional co-activation by beta-catenin is modulated by calmodulin. J. Biol. Chem. 277 (2002) 7453-7465
14. Briggs M.W., and Sacks D.B. IQGAP proteins are integral components of cytoskeletal regulation. EMBO Rep. 4 (2003) 571-574
15. Burden-Gulley S.M., and Brady-Kalnay S.M. PTPμ regulates N-cadherin-dependent neurite outgrowth. J. Cell Biol. 144 (1999) 1323-1336
16. Burden-Gulley S.M., Ensslen S.E., and Brady-Kalnay S.M. Protein tyrosine phosphatase-mu differentially regulates neurite outgrowth of nasal and temporal neurons in the retina. J. Neurosci. 22 (2002) 3615-3627
17. Cheng J., Wu K., Armanini M., O'Rourke N., Dowbenko D., and Lasky L.A. A novel protein-tyrosine phosphatase related to the homotypically adhering κ and μ receptors. J. Biol. Chem. 272 (1997) 7264-7277
18. Cismasiu V.B., Denes S.A., Reilander H., Michel H., and Szedlacsek S.E. The MAM (meprin/A5-protein/PTPmu) domain is a homophilic binding site promoting the lateral dimerization of receptor-like protein-tyrosine phosphatase mu. J. Biol. Chem. 279 (2004) 26922-26931
19. Desai C., Gindhart J.G., Goldstein L.S.B., and Zinn K. Receptor tyrosine phosphatases are required for motor axon guidance in the Drosophila embryo. Cell 84 (1996) 599-609
20. Desai C.J., Sun Q., and Zinn K. Tyrosine phosphorylation and axon guidance: of mice and flies. Curr. Opin. Neurol. 7 (1997) 70-74
21. Dimitropoulou A., and Bixby J.L. Regulation of retinal neurite growth by alterations in MAPK/ERK kinase (MEK) activity. Brain Res. 858 (2000) 205-214
22. Doherty P., Williams G., and Williams E.J. CAMs and axonal growth: a critical evaluation of the role of calcium and the MAPK cascade. Mol. Cell. Neurosci. 16 (2000) 283-295
23. Drazba J., and Lemmon V. The role of cell adhesion molecules in neurite outgrowth on Müller cells. Dev. Biol. 138 (1990) 82-93
24. Drosopoulos N.E., Walsh F.S., and Doherty P. A soluble version of the receptor-like protein tyrosine phosphatase kappa stimulates neurite outgrowth via a Grb2/MEK1-dependent signaling cascade. Mol. Cell. Neurosci. 13 (1999) 441-449
25. Ensslen S.E., and Brady-Kalnay S.M. PTPmu signaling via PKCdelta is instructive for retinal ganglion cell guidance. Mol. Cell. Neurosci. 25 (2004) 558-571
26. Ensslen-Craig S.E., and Brady-Kalnay S.M. Receptor protein tyrosine phosphatases regulate neural development and axon guidance. Dev. Biol. 275 (2004) 12-22
27. Ensslen-Craig S.E., and Brady-Kalnay S.M. PTPmu expression and catalytic activity are required for PTPmu-mediated neurite outgrowth and repulsion. Mol. Cell. Neurosci. 28 (2005) 177-188
28. Erickson J.W., Cerione R.A., and Hart M.J. Identification of an actin cytoskeletal complex that includes IQGAP and the Cdc42 GTPase. J. Biol. Chem. 272 (1997) 24443-24447
29. Fukata M., Watanabe T., Noritake J., Nakagawa M., Yamaga M., Kuroda S., Matsuura Y., Iwamatsu A., Perez F., and Kaibuchi K. Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell 109 (2002) 873-885
30. Garrity P.A., Lee C.H., Salecker I., Robertson H.C., Desai C.J., Zinn K., and Zipursky S.L. Retinal axon target selection in Drosophila is regulated by a receptor protein tyrosine phosphatase. Neuron 22 (1999) 707-717
31. Gebbink M.F.B.G., Zondag G.C.M., Wubbolts R.W., Beijersbergen R.L., van Etten I., and Moolenaar W.H. Cell-cell adhesion mediated by a receptor-like protein tyrosine phosphatase. J. Biol. Chem. 268 (1993) 16101-16104
32. Gershon T.R., Baker M.W., Nitabach M., and Macagno E.R. The leech receptor protein tyrosine phosphatase HmLAR2 is concentrated in growth cones and is involved in process outgrowth. Development 125 (1998) 1183-1190
33. Giniger E. How do Rho family GTPases direct axon growth and guidance? A proposal relating signaling pathways to growth cone mechanics. Differentiation 70 (2002) 385-396
34. Govek E.E., Newey S.E., and Van Aelst L. The role of the Rho GTPases in neuronal development. Genes Dev. 19 (2005) 1-49
35. Haj F., McKinnell I., and Stoker A. Retinotectal ligands for the receptor tyrosine phosphatase CRYPalpha. Mol. Cell. Neurosci. 14 (1999) 225-240
36. Halfter W., Newgreen D.F., Sauter J., and Schwarz U. Oriented axon outgrowth from avian embryonic retinae in culture. Dev. Biol. 95 (1983) 56-64
37. Hamburger H., and Hamilton H. A series of normal stages in the development of the chick embryo. J. Morphol. 88 (1951) 49-92
38. Hart M.J., Callow M.G., Souza B., and Polakis P. IQGAP1, a calmodulin-binding protein with a rasGAP-related domain, is a potential effector for cdc42Hs. EMBO J. 15 (1996) 2997-3005
39. Johnson K.G., McKinnell I.W., Stoker A.W., and Holt C.E. Receptor protein tyrosine phosphatases regulate retinal ganglion cell axon outgrowth in the developing Xenopus visual system. J. Neurobiol. 49 (2001) 99-117
40. Johnson K.G., and Van Vactor D. Receptor protein tyrosine phosphatases in nervous system development. Physiol. Rev. 83 (2003) 1-24
41. Kabir N., Schaefer A.W., Nakhost A., Sossin W.S., and Forscher P. Protein kinase C activation promotes microtubule advance in neuronal growth cones by increasing average microtubule growth lifetimes. J. Cell Biol. 152 (2001) 1033-1044
42. Kaibuchi K., Kuroda S., Fukata M., and Nakagawa M. Regulation of cadherin-mediated cell-cell adhesion by the Rho family GTPases. Curr. Opin. Cell Biol. 11 (1999) 591-596
43. Kolkova K., Novitskaya V., Pedersen N., Berezin V., and Bock E. Neural cell adhesion molecule-stimulated neurite outgrowth depends on activation of protein kinase C and the Ras-mitogen-activated protein kinase pathway. J. Neurosci. 20 (2000) 2238-2246
44. Krueger N.X., Van Vactor D., Wan H.I., Gelbart W.M., Goodman C.S., and Saito H. The transmembrane tyrosine phosphatase DLAR controls motor axon guidance in Drosophila. Cell 84 (1996) 611-622
45. Kuroda S., Fukata M., Kobayashi K., Nakafuku M., Nomura N., Iwamatsu A., and Kaibuchi K. Identification of IQGAP as a putative target for the small GTPases, Cdc42 and Rac1. J. Biol. Chem. 271 (1996) 23363-23367
46. 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. Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherin-mediated cell-cell adhesion. Science 281 (1998) 832-835
47. Lagenaur C., and Lemmon V. An L1-like molecule, the 8D9 antigen, is a potent substrate for neurite extension. Proc. Natl. Acad. Sci. U. S. A. 84 (1987) 7753-7757
48. Ledig M.M., Haj F., Bixby J.L., Stoker A.W., and Mueller B.K. The receptor tyrosine phosphatase CRYPalpha promotes intraretinal axon growth. J. Cell Biol. 147 (1999) 375-388
49. Lemmon V., Burden S.M., Payne H.R., Elmslie G.J., and Hlavin M.L. Neurite growth on different substrates: permissive versus instructive influences and the role of adhesive strength. J. Neurosci. 12 (1992) 818-826
50. Li Z., Kim S.H., Higgins J.M., Brenner M.B., and Sacks D.B. IQGAP1 and calmodulin modulate E-cadherin function. J. Biol. Chem. 274 (1999) 37885-37892
51. Li Z., McNulty D.E., Marler K.J., Lim L., Hall C., Annan R.S., and Sacks D.B. IQGAP1 promotes neurite outgrowth in a phosphorylation-dependent manner. J. Biol. Chem. 280 (2005) 13871-13878
52. Maeda N., and Noda M. 6B4 proteoglycan/phosphacan is a repulsive substratum but promotes morphological differentiation of cortical neurons. Development 122 (1996) 647-658
53. Mateer S.C., McDaniel A.E., Nicolas V., Habermacher G.M., Lin M.J., Cromer D.A., King M.E., and Bloom G.S. The mechanism for regulation of the F-actin binding activity of IQGAP1 by calcium/calmodulin. J. Biol. Chem. 277 (2002) 12324-12333
54. McLaughlin T., Hindges R., and O'Leary D.D. Regulation of axial patterning of the retina and its topographic mapping in the brain. Curr. Opin. Neurobiol. 13 (2003) 57-69
55. Mikule K., Sunpaweravong S., Gatlin J.C., and Pfenninger K.H. Eicosanoid activation of protein kinase C epsilon: involvement in growth cone repellent signaling. J. Biol. Chem. 278 (2003) 21168-21177
56. Nikolic M. The role of Rho GTPases and associated kinases in regulating neurite outgrowth. Int. J. Biochem. Cell Biol. 34 (2002) 731-745
57. Nishiyama M., Hoshino A., Tsai L., Henley J.R., Goshima Y., Tessier-Lavigne M., Poo M.M., and Hong K. Cyclic AMP/GMP-dependent modulation of Ca2+ channels sets the polarity of nerve growth-cone turning. Nature 424 (2003) 990-995
58. Nobes C.D., and Hall A. Rho, rac and cdc42 GTPases: regulators of actin structures, cell adhesion and motility. Biochem. Soc. Trans. 23 (1995) 456-459
59. O'Leary D.D., and McLaughlin T. Mechanisms of retinotopic map development: Ephs, ephrins, and spontaneous correlated retinal activity. Prog. Brain Res. 147 (2005) 43-65
60. Perron J.C., and Bixby J.L. Distinct neurite outgrowth signaling pathways converge on ERK activation. Mol. Cell. Neurosci. 13 (1999) 362-378
61. Phillips-Mason P.J., Gates T.J., Sacks D.B., and Brady-Kalnay S.M. The receptor protein tyrosine phosphatase PTPμ interacts with IQGAP1. J. Biol. Chem. 281 (2006) 4903-4910
62. Powell E.M., Mercado M.L., Calle-Patino Y., and Geller H.M. Protein kinase C mediates neurite guidance at an astrocyte boundary. Glia 33 (2001) 288-297
63. Raftopoulou M., and Hall A. Cell migration: Rho GTPases lead the way. Dev. Biol. 265 (2004) 23-32
64. Redies C. Cadherins and the formation of neural circuitry in the vertebrate CNS. Cell. Tissue Res. 290 (1997) 405-413
65. Redies C., and Takeichi M. Cadherins in the developing central nervous system: an adhesive code for segmental and functional subdivisions. Dev. Biol. 180 (1996) 413-423
66. Ridley A.J. Rho proteins and cancer. Breast Cancer Res. Treat. 84 (2004) 13-19
67. Ron, D., Chen, C.H., Caldwell, J., Jamieson, L., Orr, E., Mochly-Rosen, D., 1994. Cloning of an intracellular receptor for protein kinase C: a homolog of the beta subunit of G proteins. Proc. Natl. Acad. Sci. U. S. A. 91, 839-843.
68. Rosdahl J.A., Mourton T.L., and Brady-Kalnay S.M. Protein kinase C delta (PKCdelta) is required for protein tyrosine phosphatase mu (PTPmu)-dependent neurite outgrowth. Mol. Cell. Neurosci. 19 (2002) 292-306
69. Rosdahl J.A., Ensslen S.E., Niedenthal J.A., and Brady-Kalnay S.M. PTP mu-dependent growth cone rearrangement is regulated by Cdc42. J. Neurobiol. 56 (2003) 199-208
70. Roy M., Li Z., and Sacks D.B. IQGAP1 binds ERK2 and modulates its activity. J. Biol. Chem. 279 (2004) 17329-17337
71. Sap J., Jiang Y.P., Friedlander D., Grumet M., and Schlessinger J. Receptor tyrosine phosphatase R-PTP-κ mediates homophilic binding. Mol. Cell. Biol. 14 (1994) 1-9
72. Skaper S.D., Moore S.E., and Walsh F.S. Cell signalling cascades regulating neuronal growth-promoting and inhibitory cues. Prog. Neurobiol. 65 (2001) 593-608
73. Soga N., Namba N., McAllister S., Cornelius L., Teitelbaum S.L., Dowdy S.F., Kawamura J., and Hruska K.A. Rho family GTPases regulate VEGF-stimulated endothelial cell motility. Exp. Cell Res. 269 (2001) 73-87
74. Song H.J., Ming G.L., and Poo M.M. cAMP-induced switching in turning direction of nerve growth cones. Nature 388 (1997) 275-279
75. Song H.J., Ming G.L., He Z., Lehman M., McKerracher L., Tessier-Lavigne M., and Poo M. Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 281 (1998) 1515-1518
76. Sun Q.L., Wang J., Bookman R.J., and Bixby J.L. Growth cone steering by receptor tyrosine phosphatase delta defines a distinct class of guidance cue. Mol. Cell. Neurosci. 16 (2000) 686-695
77. Swart-Mataraza J.M., Li Z., and Sacks D.B. IQGAP1 is a component of Cdc42 signaling to the cytoskeleton. J. Biol. Chem. 277 (2002) 24753-24763
78. Thanos S., and Mey J. Development of the visual system of the chick. II. Mechanisms of axonal guidance. Brain Res. Rev. 35 (2001) 205-245
79. Theodore L., Derossi D., Chassaing G., Llirbat B., Kubes M., Jordan P., Chneiweiss H., Godement P., and Prochiantz A. Intraneuronal delivery of protein kinase C pseudosubstrate leads to growth cone collapse. J. Neurosci. 15 (1995) 7158-7167
80. Tong J., Elowe S., Nash P., and Pawson T. Manipulation of EphB2 regulatory motifs and SH2 binding sites switches MAPK signaling and biological activity. J. Biol. Chem. 278 (2003) 6111-6119
81. van Horck F.P., Weinl C., and Holt C.E. Retinal axon guidance: novel mechanisms for steering. Curr. Opin. Neurobiol. 14 (2004) 61-66
82. Vielmetter J., Stolze B., Bonhoeffer F., and Stuermer C.A. In vitro assay to test differential substrate affinities of growing axons and migratory cells. Exp. Brain Res. 81 (1990) 283-287
83. Walter J., Henke-Fahle S., and Bonhoeffer F. Avoidance of posterior tectal membranes by temporal retinal axons. Development 101 (1987) 909-913
84. Walter J., Kern-Veits B., Huf J., Stolze B., and Bonhoeffer F. Recognition of position-specific properties of tectal cell membranes by retinal axons in vitro. Development 101 (1987) 685-696
85. Wang J., and Bixby J.L. Receptor tyrosine phosphatase-delta is a homophilic, neurite-promoting cell adhesion molecule for CNS neurons. Mol. Cell. Neurosci. 14 (1999) 370-384
86. Weissbach L., Settleman J., Kalady M.F., Snijders A.J., Murthy A.E., Yan Y.X., and Bernards A. Identification of a human rasGAP-related protein containing calmodulin-binding motifs. J. Biol. Chem. 269 (1994) 20517-20521
87. Xiang Y., Li Y., Zhang Z., Cui K., Wang S., Yuan X.B., Wu C.P., Poo M.M., and Duan S. Nerve growth cone guidance mediated by G protein-coupled receptors. Nat. Neurosci. 5 (2002) 843-848
88. Yamada M., Ikeuchi T., and Hatanaka H. The neurotrophic action and signalling of epidermal growth factor. Prog. Neurobiol. 51 (1997) 19-37
89. Zhang B., Wang Z.X., and Zheng Y. Characterization of the interactions between the small GTPase Cdc42 and its GTPase-activating proteins and putative effectors. Comparison of kinetic properties of Cdc42 binding to the Cdc42-interactive domains. J. Biol. Chem. 272 (1997) 21999-22007
90. Zheng J.Q. Turning of nerve growth cones induced by localized increases in intracellular calcium ions. Nature 403 (2000) 89-93
91. Zondag G., Koningstein G., Jiang Y.P., Sap J., Moolenaar W.H., and Gebbink M. Homophilic interactions mediated by receptor tyrosine phosphatases μ and κ. J. Biol. Chem. 270 (1995) 14247-14250