The p21-activated kinase PAK3 forms heterodimers with PAK1 in brain implementing trans-regulation of PAK3 activity

Journal of Biological Chemistry

Volumn 287, Issue 36, 2012, Pages 30084-30096

  Combeau, Gaëlle ^a,b,c   Kreis, Patricia ^a,b,d   Domenichini, Florence ^a,b   Amar, Muriel ^a,b   Fossier, Philippe ^a,b   Rousseau, Véronique ^a,b   Barnier, Jean Vianney ^a,b  

^a CNRS   (France)

^b CNRS   (France)

^c KAROLINSKA INSTITUTE   (Sweden)

^d KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CONTROL-CELL; DENDRITIC SPINE; HETERODIMERIC COMPLEXES; HETERODIMERIZATION; HETERODIMERS; HOMODIMERIZATION; HOMODIMERIZE; INTELLECTUAL DISABILITY; KINASE ACTIVITY; KINASE ASSAYS; LYSATES; P-21 ACTIVATED KINASE; REGULATORY DOMAIN; SPLICE VARIANTS; SYNAPTIC PLASTICITY; SYNAPTIC TRANSMISSION;

DIMERIZATION; ENZYMES; GENES; NEURONS;

BRAIN;

BRAIN ENZYME; ENZYME VARIANT; HETERODIMER; P21 ACTIVATED KINASE 1; P21 ACTIVATED KINASE 3; P21 ACTIVATED KINASE 3A; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LYSATE; CONTROLLED STUDY; DENDRITIC SPINE; DIMERIZATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INHIBITION; ENZYME LOCALIZATION; ENZYME PURIFICATION; ENZYME REGULATION; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; INTELLECTUAL IMPAIRMENT; MUTATION; NERVE CELL; NONHUMAN; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION;

ALTERNATIVE SPLICING; ANIMALS; DENDRITIC SPINES; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENETIC DISEASES, X-LINKED; HELA CELLS; HUMANS; INTELLECTUAL DISABILITY; MICE; MUTATION; NERVE TISSUE PROTEINS; P21-ACTIVATED KINASES; POST-SYNAPTIC DENSITY; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION;

EID: 84865793920     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.355073     Document Type: Article

References (41)

1. Bokoch, G. M. (2003) Biology of the p21-activated kinases. Annu. Rev. Biochem. 72, 743-781
2. Burbelo, P. D., Drechsel, D., and Hall, A. (1995) A conserved binding motif defines numerous candidate target proteins for both Cdc42 and Rac GTPases. J. Biol. Chem. 270, 29071-29074
3. Bagrodia, S., Taylor, S. J., Jordon, K. A., Van Aelst, L., and Cerione, R. A. (1998) A novel regulator of p21-activated kinases. J. Biol. Chem. 273, 23633-23636
4. Manser, E., Huang, H. Y., Loo, T. H., Chen, X. Q., Dong, J. M., Leung, T., and Lim, L. (1997) Expression of constitutively active α-PAK reveals effects of the kinase on actin and focal complexes. Mol. Cell. Biol. 17, 1129-1143
5. Thévenot, E., Moreau, A. W., Rousseau, V., Combeau, G., Domenichini, F., Jacquet, C., Goupille, O., Amar, M., Kreis, P., Fossier, P., and Barnier, J. V. (2011) p21-Activated kinase 3 (PAK3) protein regulates synaptic transmission through its interaction with the Nck2/Grb4 protein adaptor. J. Biol. Chem. 286, 40044-40059
6. Lei, M., Lu, W., Meng, W., Parrini, M. C., Eck, M. J., Mayer, B. J., and Harrison, S. C. (2000) Structure of PAK1 in an autoinhibited conformation reveals a multistage activation switch. Cell 102, 387-397
7. Parrini, M. C., Lei, M., Harrison, S. C., and Mayer, B. J. (2002) Pak1 kinase homodimers are autoinhibited in trans and dissociated upon activation by Cdc42 and Rac1. Mol. Cell 9, 73-83
8. Zenke, F. T., King, C. C., Bohl, B. P., and Bokoch, G. M. (1999) Identification of a central phosphorylation site in p21-activated kinase regulating autoinhibition and kinase activity. J. Biol. Chem. 274, 32565-32573
9. Buchwald, G., Hostinova, E., Rudolph, M. G., Kraemer, A., Sickmann, A., Meyer, H. E., Scheffzek, K., and Wittinghofer, A. (2001) Conformational switch and role of phosphorylation in pak activation. Mol. Cell. Biol. 21, 5179-5189
10. Pirruccello, M., Sondermann, H., Pelton, J. G., Pellicena, P., Hoelz, A., Chernoff, J., Wemmer, D. E., and Kuriyan, J. (2006) A dimeric kinase assembly underlying autophosphorylation in the p21 activated kinases. J. Mol. Biol. 361, 312-326
11. Wang, J., Wu, J. W., and Wang, Z. X. (2011) Structural insights into the autoactivation mechanism of p21-activated protein kinase. Structure 19, 1752-1761
12. Chong, C., Tan, L., Lim, L., and Manser, E. (2001) The mechanism of PAK activation. Autophosphorylation events in both regulatory and kinase domains control activity. J. Biol. Chem. 276, 17347-17353
13. Parrini, M. C., Camonis, J., Matsuda, M., and de Gunzburg, J. (2009) Dissecting activation of the PAK1 kinase at protrusions in living cells. J. Biol. Chem. 284, 24133-24143
14. Allen, K. M., Gleeson, J. G., Bagrodia, S., Partington, M. W., MacMillan, J. C., Cerione, R. A., Mulley, J. C., and Walsh, C. A. (1998) PAK3 mutation in nonsyndromic X-linked mental retardation. Nat. Genet. 20, 25-30
15. Bienvenu, T., des Portes, V., McDonell, N., Carrié, A., Zemni, R., Couvert, P., Ropers, H. H., Moraine, C., van Bokhoven, H., Fryns, J. P., Allen, K., Walsh, C. A., Boué, J., Kahn, A., Chelly, J., and Beldjord, C. (2000) Missense mutation in PAK3, R67C, causes X-linked nonspecific mental retardation. Am. J. Med. Genet. 93, 294-298
16. Gedeon, A. K., Nelson, J., Gecz, J., and Mulley, J. C. (2003) X-linked mild non-syndromic mental retardation with neuropsychiatric problems and the missense mutation A365E in PAK3. Am. J. Med. Genet. 120, 509-517
17. Kreis, P., Rousseau, V., Thévenot, E., Combeau, G., and Barnier, J. V. (2008) The four mammalian splice variants encoded by the p21-activated kinase 3 gene have different biological properties. J. Neurochem. 106, 1184-1197
18. Arias-Romero, L. E., and Chernoff, J. (2008) A tale of two Paks. Biol. Cell 100, 97-108
19. Rousseau, V., Goupille, O., Morin, N., and Barnier, J. V. (2003) A new constitutively active brain PAK3 isoform displays modified specificities toward Rac and Cdc42 GTPases. J. Biol. Chem. 278, 3912-3920
20. Kreis, P., and Barnier, J. V. (2009) PAK signaling in neuronal physiology. Cell. Signal. 21, 384-393
21. Molli, P. R., Li, D. Q., Murray, B. W., Rayala, S. K., and Kumar, R. (2009) PAK signaling in oncogenesis. Oncogene 28, 2545-2555
22. Dummler, B., Ohshiro, K., Kumar, R., and Field, J. (2009) Pak protein kinases and their role in cancer. Cancer Metastasis Rev. 28, 51-63
23. Morel, N., Dedieu, J. C., and Philippe, J. M. (2003) Specific sorting of the a1 isoform of the V-H+ ATPase a subunit to nerve terminals where it associates with both synaptic vesicles and the presynaptic plasma membrane. J. Cell Sci. 116, 4751-4762
24. Kreis, P., Thévenot, E., Rousseau, V., Boda, B., Muller, D., and Barnier, J. V. (2007) The p21-activated kinase 3 implicated in mental retardation regulates spine morphogenesis through a Cdc42-dependent pathway. J. Biol. Chem. 282, 21497-21506
25. Crouin, C., Arnaud, M., Gesbert, F., Camonis, J., and Bertoglio, J. (2001) A yeast two-hybrid study of human p97/Gab2 interactions with its SH2 domain-containing binding partners. FEBS Lett. 495, 148-153
26. Poëa-Guyon, S., Amar, M., Fossier, P., and Morel, N. (2006) Alternative splicing controls neuronal expression of v-ATPase subunit a1 and sorting to nerve terminals. J. Biol. Chem. 281, 17164-17172
27. Sans, N., Racca, C., Petralia, R. S., Wang, Y. X., McCallum, J., and Wenthold, R. J. (2001) Synapse-associated protein 97 selectively associates with a subset of AMPA receptors early in their biosynthetic pathway. J. Neurosci. 21, 7506-7516
28. Standley, S., Roche, K. W., McCallum, J., Sans, N., and Wenthold, R. J. (2000) PDZ domain suppression of an ER retention signal in NMDA receptor NR1 splice variants. Neuron 28, 887-898
29. Boda, B., Alberi, S., Nikonenko, I., Node-Langlois, R., Jourdain, P., Moosmayer, M., Parisi-Jourdain, L., and Muller, D. (2004) The mental retardation protein PAK3 contributes to synapse formation and plasticity in hippocampus. J. Neurosci. 24, 10816-10825
30. Meng, J., Meng, Y., Hanna, A., Janus, C., and Jia, Z. (2005) Abnormal long-lasting synaptic plasticity and cognition in mice lacking the mental retardation gene Pak3. J. Neurosci. 25, 6641-6650
31. Rex, C. S., Lin, C. Y., Kramár, E. A., Chen, L. Y., Gall, C. M., and Lynch, G. (2007) Brain-derived neurotrophic factor promotes long-term potentiation-related cytoskeletal changes in adult hippocampus. J. Neurosci. 27, 3017-3029
32. Hayashi, M. L., Choi, S. Y., Rao, B. S., Jung, H. Y., Lee, H. K., Zhang, D., Chattarji, S., Kirkwood, A., and Tonegawa, S. (2004) Altered cortical synaptic morphology and impaired memory consolidation in forebrain- specific dominant-negative PAK transgenic mice. Neuron 42, 773-787
33. Dubos, A., Combeau, G., Bernardinelli, Y., Barnier, J. V., Hartley, O., Gaertner, H., Boda, B., and Muller, D. (2012) Alteration of synaptic network dynamics by the intellectual disability protein PAK3. J. Neurosci. 32, 519-527
34. Wan, P. T., Garnett, M. J., Roe, S. M., Lee, S., Niculescu-Duvaz, D., Good, V. M., Jones, C. M., Marshall, C. J., Springer, C. J., Barford, D., and Marais, R. (2004) Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF. Cell 116, 855-867
35. Lemmon, M. A., and Schlessinger, J. (2010) Cell signaling by receptor tyrosine kinases. Cell 141, 1117-1134
36. Yatime, L., Hein, K. L., Nilsson, J., and Nissen, P. (2011) Structure of the RACK1 dimer from Saccharomyces cerevisiae. J. Mol. Biol. 411:486-498
37. Wimmer, R., and Baccarini, M. (2010) Partner exchange: protein-protein interactions in the Raf pathway. Trends Biochem. Sci. 35, 660-668
38. Hatzivassiliou, G., Song, K., Yen, I., Brandhuber, B. J., Anderson, D. J., Alvarado, R., Ludlam, M. J., Stokoe, D., Gloor, S. L., Vigers, G., Morales, T., Aliagas, I., Liu, B., Sideris, S., Hoeflich, K. P., Jaiswal, B. S., Seshagiri, S., Koeppen, H., Belvin, M., Friedman, L. S., and Malek, S. (2010) RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth. Nature 464, 431-435
39. Eswaran, J., Soundararajan, M., Kumar, R., and Knapp, S. (2008) UnPAKing the class differences among p21-activated kinases. Trends Biochem. Sci. 33, 394-403
40. Asrar, S., Meng, Y., Zhou, Z., Todorovski, Z., Huang, W. W., and Jia, Z. (2009) Regulation of hippocampal long-term potentiation by p21-activated protein kinase 1 (PAK1). Neuropharmacology 56, 73-80
41. Huang, W., Zhou, Z., Asrar, S., Henkelman, M., Xie, W., and Jia, Z. (2011) p21-Activated kinases 1 and 3 control brain size through coordinating neuronal complexity and synaptic properties. Mol. Cell. Biol. 31, 388-403