Regulation of Kalirin by Cdk5

Journal of Cell Science

Volumn 121, Issue 15, 2008, Pages 2601-2611

  Xin, Xiaonan ^a   Wang, Yanping ^a   Ma, Xin Ming ^a   Rompolas, Panteleimon ^a   Keutmann, Henry T ^b   Mains, Richard E ^a   Eipper, Betty A ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Calyculin A; PC12 cells; Phosphorylation; PP 1; RhoGEF; Roscovitine; Spectrin like repeats

Indexed keywords

ALANINE; ASPARAGINE; CALYCULIN A; CYCLIN DEPENDENT KINASE 5; KALIRIN 7; MUTANT PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; ROSCOVITINE; SPECTRIN; THREONINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL DIFFERENTIATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOPLASM; DENDRITIC SPINE; ENZYME PHOSPHORYLATION; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; WILD TYPE;

ANIMALS; ASPARTIC ACID; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE 5; DENDRITIC SPINES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; MODELS, BIOLOGICAL; PC12 CELLS; PHOSPHORYLATION; PROTEIN PHOSPHATASE 1; RATS; THREONINE;

EID: 50249119624     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.016089     Document Type: Article

References (57)

1. Alam, M. R., Johnson, R. C., Darlington, D. N., Hand, T. A., Mains, R. E. and Eipper, B. A. (1997). Kalirin, a cytosotic protein with spectrin-like and GDP/GTP exchange factor-like domains that interacts with peptidylglycine α-amidating monooxygenase, an integral membrane peptide-processing enzyme. J. Biol. Chem. 272, 12667-12675.
2. Aoki, K., Nakamura, T. and Matsuda. M. (2004). Spatio-temporal regulation of Rac1 and Cdc42 activity during nerve growth factor-induced neurite outgrowth in PC12 cells. J. Biol. Chem. 279, 713-719.
3. Awasaki, T., Saito, M., Sone, M., Suzuki Sakai, E. R., Ito, K. and Hama, C. (2000). The Drosophila Trio plays an essential role in patterning of axons by regulating their directional extension. Neuron 26, 119-131.
4. Bateman, J., Shu, H. and Van Vactor, D. (2000). The GEF Trio mediates axonal development in the Drosophila embryo. Neuron 26, 93-106.
5. Bibb, J. A., Chen, J., Taylor, J. R., Svenningsson, P., Nishi, A., Snyder, G. L., Yan, Z., Sagawa, Z. K., Ouimet, C. C, Nairn, A. C. et al. (2001a). Effects of chronic exposure to cocaine are regulated by the neuronal protein Cdk5. Nature 410, 376-380.
6. Bibb, J. A., Nishi, A., O'Callaghan, J. P., Ule, J., Lan, M. S., Snyder, G. L., Horiuchi, A., Saito, T., Hisanaga, S. I., Czernik, A. J. et al. (2001b). Phosphorylation of protein phosphatase inhibitor-1 by cdk5. J. Biol. Chem. 276, 14490-14497.
7. Black, M. M., Aletta, J. M. and Greene, L. A. (1986). Regulation of microtubule composition and stability during nerve growth factor-promoted neurite outgrowth. J. Cell Biol. 103, 545-557.
8. Briancon-Marjollet, A., Ghogha,A., Nawabi, H., Triki, I., Auziol, C., Fromont, S., Piche, C., Enslen, H., Chebli, K., Cloutier, J. F. et al. (2008). Trio mediates netrin-1-induced Rac1 activation in axon outgrowth and guidance. Mol. Cell. Biol. 28, 2314-2323.
9. Canduri, F., Uchoa, H. B. and de Azevedo, W. F. J. (2004). Molecular models of cyclin-dependent kinase 1 complexed with inhibitors. Biochem. Biophys. Res. Commun. 324, 661-666.
10. Castillo-Liuva, S., Alvarez-Tabares, I., Weber, G. Steinberg, I. and Perez-Martin, J. (2007). Sustained cell polarity and virulence in the phytopathogenic fungus Ustilago maydis depends on an essential cyclin-dependent kinase from the Cdk5/Pho85 family. J. Cell Sci. 120, 1584-1595.
11. Chakrabarti, K., Lin, R., Schiller, N. I., Wang, Y., Koubi, D., Fan, Y. X., Rudkin, B. B., Johnson, G. R. and Schiller, M. R. (2005). Critical role for Kahrin in nerve growth factor signaling through TrkA. Mol. Cell. Biol. 25, 5106-5118.
12. Cheung, Zh., Fu, A. K. and Ip, N. Y. (2006). Synaptic roles of Cdk5: implications in higher cognitive functions and neurodegenerative diseases, Neuron 50, 13-18.
13. Cohen, P. T. W. (2002). Protein phosphatase 1-targeted in many directions. J. Cell Sci. 115, 241-256.
14. Colomer, V., Engelender, S., Sharp, A. H., Duan, K., Cooper, J. K., Lanahan, A., Lyford, G., Worley, P. and Ross, C. A. (1997). Huntingtin-associated protein 1 (HAP1) binds to a Trio-like polypeptide, with a rac1 guanine nucleotide exchange factor domain. Hum. Mol. Genet. 6, 1519-1525.
15. Debant, A., Serra-Pages, C., Seipel, K., O'Brien, S., Tang, M., Park, S. H. and Streuli, M. (1996). The multidomain protein Trio binds the LAR transmembrane tyrosine phosphatase, contains a protein kinase domain, and has separate rac-specific and rho-specific guanine nucleotide exchange factor domains. Proc. Natl. Acad. Sci. USA 93, 5466-5471.
16. Dhavan, R. and Tsai, L. H. (2001). A decade of Cdk5. Nat. Rev. Mol. Cell Biol. 2, 749-759.
17. Estrach, S., Schmidt, S., Diriong, S., Penna, A., Blangy, A., Fort, P. and Debant, A. (2002). The Human Rho-GEF Trio and Its Target GTPase RhoG Are Involved in the NGF Pathway, Leading to Neurite Outgrowth. Curr. Biol. 12, 307-312.
18. Fu, W. Y., Chen, Y., Sabin, M., Zhao, X. S., Shi, L., Bikoff, J. B., Lai, K. O., Yung, W. H., Fu, A. K., Greenberg, M. E. et al. (2007). Cdk5 regulates EphA4-mediated dendritic spine retraction through an ephexin1-dependent mechanism. Nat. Neurosci. 10, 67-76.
19. Greengard, P., Allen, P. B. and Nairn, A. C. (1999). Beyond the dopamine receptor: the DARPP-32/protein phosphatase-1 cascade. Neuron 23, 435-447.
20. Gulli, M. P., Jaquenoud, M., Shimada, Y., Niederbluser, G., Wiget, P. and Peter, M. (2000). Phosphorylation of the Cdc42 exchange factor Cdc24 by the PAK-like kinase Cla4 may regulate polarized growth in yeast. Mol. Cell 6, 1155-1167.
21. Hahn, C. M., Kleinholz, H., Koester, M. P., Grieser, S., Thelen, K. and Pollerberg, G. E. (2005). Role of Cyclin-Dependent Kinase and Its Activator P35 in Local Axon and Growth Cone Stabilization. Neuroscience 134, 449-465.
22. Harada, T., Morooka, T., Ogawa, S. and Nishida, E. (2001). ERK induces p35, a neuron-specific activator of Cdk5, through induction of Egr1. Nat. Cell Biol. 3, 453-459.
23. Humbert, S., Dhavan, R. and Tsai, L. H. (2002). p39 activates Cdk5 in neurons, and is associated with the actin cytoskeleton. J. Cell Sci. 113, 975-983.
24. Johnson, R. C., Penzes, P., Upper, B. A. and Mains, R. E. (2000). Isoforms of kalirin, a neuronal Dbl family member, generated through use of different 5′- and 3′-ends along with an internal translational initiation site. J. Biol. Chem. 275, 19324-19333.
25. Kesavapany, S., Amin, N., Zheng, Y., Nijhara, R., Jaffe, H., Sihag, R., Gutkind, J. S., Takahashi, S., Kulkarni, A., Grant, Ph. et al. (2004). p35/cyclin-dependent kinase 5 phosphorylation of ras guanine nucleotide releasing factor 2 (RasGRF2) mediates Rac-dependent Extracellular Signal-regulated kinase 1/2 activity, altering RasGRF2 and microtubule-associated protein 1b distribution in neurons. J. Neurosci. 24, 4421-4431.
26. Kesavapany, S., Pareek, T. K., Zheng, Y. L., Amin, N., Gutkind, J. S., Ma, W., Kulkarni, A. B., Grant, Ph. and Pant, H. C. (2006). Neuronal nuclear organization is controlled by cyclin-dependent kinase 5 phosphorylation of Ras Guanine nucleotide releasing factor-1. Neurosignals 15, 157-173.
27. Lee, K. Y., Rosales, J. L., Tang, D. and Wang, J. H. (1996). Interaction of cyclin-dependent kinase 5 (Cdk5) and neuronal Cdk5 activator in bovine brain. J. Biol. Chem. 271, 1538-1543.
28. Ma, X. M., Huang, J., Wang, Y. P., Eipper, B. A. and Mains, R. E. (2003). Kalirin, a Multifunctional Rho Guanine Nucleotide Exchange Fector, Is Necessary for Maintenance of Hippocampal Pyramidal Neuron Dendrites and Dendritic Spines. J. Neurosci. 23, 10593-10603.
29. Ma, X. M., Wang, Y., Ferraro, F., Mains, R. E. and Eipper, B. A. (2008). Kalirin-7 is an essential component of both shaft and spine excitatory synapses in hippocampal interneurons. J. Neurosci. 28, 711-724.
30. May, V., Schiller, M. R., Eipper, B. A. and Mains, R. E. (2002). Kalirin Db1-homology GEF1 domain initiates new axon outgrowths through RhoG-mediated mechanisms. J. Neurosci. 22, 6980-6990.
31. McPherson, C. E., Eipper, B. A. and Mains, R. E. (2004). Multiple novel isoforms of Trio are expressed in the developing rat brain. Gene 347, 125-135.
32. Meikrantz, W. and Schlege, R. (1996). Suppression of appoptosis by dominant negative mutants of cyclin-dependam protein kinases. J. Biol. Chem., 271, 10205-10209.
33. Morishita, W., Connor, J. H., Xia, H., Quinlan, E. M., Shenolikar, S. and Malenka, R. C. (2001). Regulation of synaptic strength by protein phosphatase 1. Neuron 32, 1133-1148.
34. Newsome, T. P., Schmidt, S., Dietzl, G., Keleman, K., Asling, B., Debant, A. and Dickson, B. J. (2000). Trio combines with Dock to regulate Pak activity during photoreceptor axon pathfinding in Drosophila. Cell 101, 283-294.
35. Nikolic, M. (2002). The role of Rho GTPases and associated kinases in regulating neurite outgrowth. Int. J. Biochem. Cell Biol. 34, 731-745.
36. Nikolic, M., Chou, M. M., Lu, W., Mayer, B. J. and Tsai, L. H. (1999). The p35/Cdk5 kinase is a neuron-specific Rae effector that inhibits PakI activity. Nature 395, 194-198.
37. O'Brien, L. E., Jou, Tz. Sh., Pollack, A. L., Zhang, Q., Hansen, St. H., Yurchenco, P. and Mostov, K. E. (2001). Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nature Cell Biol. 3, 831-838.
38. Oh, Y. and Fung, L. W. M. (2007). Brain proteins interacting with the tetramerization region of non-erythroid alpha spectrin. Cell. Mol. Biol. Lett. 12, 604-620.
39. Penzes, P., Johnson, R. C., Alam, M. R., Kambampati, V., Mains, R. E. and Eipper, B. A. (2000). An isoform of Kalirin, a brain-specific GDP/GTP exchange factor, is enriched in the postsynaptic density firaction. J. Biol. Chem. 275, 6395-6403.
40. Penzes, P., Johnson, R. C., Sattler, R., Zhang, X., Huganir, R. L., Kambampati, V., Mains, R. E. and Eipper, B. A. (2001). The neuronal Rho-GEF Kalirin-7 interacts with PDZ domain-cortaining proteins and regulates dendritic morphogenesis. Neuron 29, 229-242.
41. Penzes, P., Beeser, A., Chernoff, J., Schiller, M. R., Eipper, B. A., Mains, R. E. and Huganir, R. L. (2003). Rapid induction of dendrific spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kahrin. Neuron 37, 263-274.
42. Qi, Z., Huang, Q. Q., Lee, K. Y., Lew, J. and Wang, J. H. (1995). Reconstitution of neuronal Cdc2-like kinase from bacteria-expressed Cdk5 and an active fragment of the brain-specific activator. J. Biol. Chem. 270, 10847-10854.
43. Ratovitski, E. A., Alam, M. R., Quick, R. A., McMillan, A., Bao, C., Hand, T. A., Johnson, R. C., Mains, R. E., Eipper, B. A. and Lowenstein, C. J. (1999). Kalirin inhibition of inducible nitric oxide synthase. J. Biol. Chem. 274, 993-999.
44. Rossman, K. L., Der, C. J. and Sondek, J. (2005). GEF means go: turning on Rho GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell. Biol. 6, 167-180.
45. Ryan, X. P., Alldritt, J., Svenningsson, P., Allen, P. B., Wu, G. Y., Nairn, A. C. and Greengard, P. (2005). The Rho-specific GEF Lfc interacts with neurabin and spinophilin to regulate dendritic spine morphology. Neuron 47, 85-100.
46. Schiller, M. R., Blangy, A., Huang, J., Mains, R. E. and Eipper, B. A. (2005). Induction of lamellipodia by Kalirin does not require its guanine nucleotide exchange factor activity. Exp. Cell Res. 307, 402-417.
47. Schiller, M. R., Chakrabarti, K., King, G., Schiller, N., Eipper, B. and Maciejewski, M. (2006). Regulation of RhoGEF activity by intramolecular and intermolecular SH3 interactions. J. Biol. Chem. 281, 18774-18786.
48. Schiller, M. R., Ferraro, F., Wang, Y., Ma, X.-M., McPherson, C. E., Sobota, J. A., Schiller, N. L, Mains, R. E. and Eipper, B. A. (2008). Autonomous functions for the Sec14p/spechrin-repeat region of Kahrin. Exp. Cell Res. PMID:18585704.
49. Sharma, P., Sharma, M., Amin, N. D, Albers, R. W. and Pant. H. C. (1999). Regulation of cyclin-dependent kinase 5 catalytic activity by phosphorylation. Proc. Natl. Acad. Sci. USA 96, 11156-11160.
50. Steven, R., Kubiseski, T. J., Zheng, H., Kulkarni, S., Mancillas, J., Morales, A. R., Hogue, C. W. V., Pawson, T. and Culotti, J. G. (1998). Unc-73 activates the Rac GTPase and is required for cell and growth cone migrations in C elegans. Cell 92, 785-795.
51. Takaki, M., Paek, M., Kamiya, A., Balkissoon, R., Tomoda, T., Penzes, P. and Sawa, A. (2005). Disrupted-in-schizophrenia-1 (DISC1) binds to Kalirin-7 and modulates its function as a GDP/GTP exchange factor. Soc. Neurosci. Abstr. program No. 674.9.
52. Takashima, A., Murayama, M., Yasutake, K., Takahashi, H., Yokoyama, M. and Ishiguro, K. (2001). Involvement ofcdk5 activator p25 on tauphosphorylation in mouse brain. Neurosci. Lett. 22, 37-40.
53. Tan, T. C., Valova, V. A., Malladi, CH. S., Graham, M. E. and Robinson, Ph. J. (2003). Cdk5 is essential for synaptic vesicle endocytosis. Nat, Cell Biol. 5, 701-710.
54. Tang, A., Yeung, J., Lee, K. Y., Matsushita, M., Matsui, H., Tomizawa, K., Hatase, O. and Wang, J. H. (1995). An isoform of the neuronal cyclin-dependent kinase 5 (Cdk5) activity. J. Biol. Chem. 270, 26897-26903.
55. Xie, Z., Srivastava, D. P., Photowala, H., Kai, L., Cahill, M. E., Woolfrey, K. M., Shum, C. Y., Surmeirer, D. J. and Penzes, P. (2007). Kalirin-7 controls activity-dependent structural and functional plasticity of dendritic spines. Neuron 56, 640-656.
56. Xin, X., Ferraro, F., Back, N., Eipper, B. A. and Mains, R. E. (2004). Cdk5 and Trio modulate endocrine cell exocytosis. J. Cell Sci. 117, 4739-4748.
57. Zhang, B., Tan, V. B., Lim, K. M., Tay, T. E. and Zhuang, S. (2006). Study of the inhibition of cyclin-dependent kinases with roscovitine and indirubin-3′-oxime from molecular dynamics simulations. J. Mol. Model 13, 78-89.