Mutational analysis reveals a single binding interface between RhoA and its effector, PRK1

Biochemistry

Volumn 50, Issue 14, 2011, Pages 2860-2869

  Hutchinson, Catherine L ^a   Lowe, Peter N ^b   McLaughlin, Stephen H ^a,c   Mott, Helen R ^a   Owen, Darerca ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b Biomolecular Interactions Consultancy   (United Kingdom)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE-SCANNING MUTAGENESIS; BINDING INTERFACE; BINDING MOTIF; BIOPHYSICAL PROPERTIES; CONTACT SITES; FOLDED STATE; G PROTEIN; MUTATIONAL ANALYSIS; POTENTIAL CONTACTS; PROTEIN KINASE C; RHO FAMILY; THERMAL STABILITY; THERMALLY STABLE; TWO DOMAINS;

AMINO ACIDS; ENZYMES; MUTAGENESIS; THERMODYNAMIC STABILITY;

BINDING SITES;

ALANINE; GLUTATHIONE TRANSFERASE; GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN KINASE C; PROTEIN KINASE C RELATED KINASE 1; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; CRYSTAL STRUCTURE; ENZYME ACTIVATION; MUTAGENESIS; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; SITE DIRECTED MUTAGENESIS; THERMOSTABILITY;

ALGORITHMS; BINDING SITES; CIRCULAR DICHROISM; DNA MUTATIONAL ANALYSIS; HUMANS; KINETICS; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN KINASE C; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RHOA GTP-BINDING PROTEIN; SOLUTIONS;

EID: 79953683448     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200039u     Document Type: Article

References (42)

1. Ridley, A. J., Allen, W. E., Peppelenbosch, M., and Jones, G. E. (1999) Rho family proteins and cell migration Biochem. Soc. Symp., 111-123 (Pubitemid 129541617)
2. Govek, E. E., Newey, S. E., and Van Aelst, L. (2005) The role of the Rho GTPases in neuronal development Genes Dev. 19, 1-49 (Pubitemid 40095815)
3. Salminen, A., Suuronen, T., and Kaarniranta, K. (2008) ROCK, PAK, and Toll of synapses in Alzheimers disease Biochem. Biophys. Res. Commun. 371, 587-590
4. Mueller, B. K., Mack, H., and Teusch, N. (2005) Rho kinase, a promising drug target for neurological disorders Nat. Rev. Drug Discovery 4, 387-398 (Pubitemid 40704122)
5. Budzyn, K., Marley, P. D., and Sobey, C. G. (2006) Targeting Rho and Rho-kinase in the treatment of cardiovascular disease Trends Pharmacol. Sci. 27, 97-104 (Pubitemid 43184031)
6. Vega, F. M. and Ridley, A. J. (2008) Rho GTPases in cancer cell biology FEBS Lett. 582, 2093-2101
7. Fujisawa, K., Madaule, P., Ishizaki, T., Watanabe, G., Bito, H., Saito, Y., Hall, A., and Narumiya, S. (1998) Different regions of Rho determine Rho-selective binding of different classes of Rho target molecules J. Biol. Chem. 273, 18943-18949 (Pubitemid 28366283)
8. Palmer, R. H., Ridden, J., and Parker, P. J. (1995) Cloning and Expression Patterns of 2 Members of a Novel Protein-Kinase-C-Related Kinase Family Eur. J. Biochem. 227, 344-351
9. Watanabe, G., Saito, Y., Madaule, P., Ishizaki, T., Fujisawa, K., Morii, N., Mukai, H., Ono, Y., Kakizuka, A., and Narumiya, S. (1996) Protein kinase N (PKN) and PKN-related protein rhophilin as targets of small GTPase Rho Science 271, 645-648 (Pubitemid 26053455)
10. Mukai, H. (2003) The structure and function of PKN, a protein kinase having a catalytic domain homologous to that of PKC J. Biochem. 133, 17-27 (Pubitemid 36240974)
11. Mukai, H., Toshimori, M., Shibata, H., Kitagawa, M., Shimakawa, M., Miyahara, M., Sunakawa, H., and Ono, Y. (1996) PKN associates and phosphorylates the head-rod domain of neurofilament protein J. Biol. Chem. 271, 9816-9822 (Pubitemid 26137395)
12. Matsuzawa, K., Kosako, H., Inagaki, N., Shibata, H., Mukai, H., Ono, Y., Amano, M., Kaibuchi, K., Matsuura, Y., Azuma, I., and Inagaki, M. (1997) Domain-specific phosphorylation of vimentin and glial fibrillary acidic protein by PKN Biochem. Biophys. Res. Commun. 234, 621-625 (Pubitemid 27281167)
13. Kawamata, T., Taniguchi, T., Mukai, H., Kitagawa, M., Hashimoto, T., Maeda, K., Ono, Y., and Tanaka, C. (1998) A protein kinase, PKN, accumulates in Alzheimer neurofibrillary tangles and associated endoplasmic reticulum-derived vesicles and phosphorylates tau protein J. Neurosci. 18, 7402-7410 (Pubitemid 28425824)
14. Metzger, E., Muller, J. M., Ferrari, S., Buettner, R., and Schule, R. (2003) A novel inducible transactivation domain in the androgen receptor: implications for PRK in prostate cancer EMBO J. 22, 270-280 (Pubitemid 36119433)
15. Gao, Q. S., Kumar, A., Srinivasan, S., Singh, L., Mukai, H., Ono, Y., Wazer, D. E., and Band, V. (2000) PKN binds and phosphorylates human papillomavirus E6 oncoprotein J. Biol. Chem. 275, 14824-14830 (Pubitemid 30337194)
16. Quilliam, L. A., Lambert, Q. T., MickelsonYoung, L. A., Westwick, J. K., Sparks, A. B., Kay, B. K., Jenkins, N. A., Gilbert, D. J., Copeland, N. G., and Der, C. J. (1996) Isolation of a NCK-associated kinase, PRK2, an SH3-binding protein and potential effector of Rho protein signaling J. Biol. Chem. 271, 28772-28776 (Pubitemid 26382572)
17. Vincent, S. and Settleman, J. (1997) The PRK2 kinase is a potential effector target of both Rho and Rac GTPases and regulates actin cytoskeletal organization Mol. Cell. Biol. 17, 2247-2256 (Pubitemid 27133312)
18. Takahashi, M., Mukai, H., Toshimori, M., Mlyamoto, M., and Ono, Y. (1998) Proteolytic activation of PKN by caspase-3 or related protease during apoptosis Proc. Natl. Acad. Sci. U.S.A. 95, 11566-11571 (Pubitemid 28460455)
19. Dong, L. Q., Landa, L. R., Wick, M. J., Zhu, L., Mukai, H., Ono, Y., and Liu, F. (2000) Phosphorylation of protein kinase N by phosphoinositide-dependent protein kinase-1 mediates insulin signals to the actin cytoskeleton Proc. Natl. Acad. Sci. U.S.A. 97, 5089-5094 (Pubitemid 30313676)
20. Yoshinaga, C., Mukai, H., Toshimori, M., Miyamoto, M., and Ono, Y. (1999) Mutational analysis of the regulatory mechanism of PKN: The regulatory region of PKN contains an arachidonic acid-sensitive autoinhibitory domain J. Biochem. 126, 475-484 (Pubitemid 29452611)
21. Flynn, P., Mellor, H., Palmer, R., Panayotou, G., and Parker, P. J. (1998) Multiple interactions of PRK1 with RhoA: Functional assignment of the HR1 repeat motif J. Biol. Chem. 273, 2698-2705 (Pubitemid 28133914)
22. Owen, D., Lowe, P. N., Nietlispach, D., Brosnan, C. E., Chirgadze, D. Y., Parker, P. J., Blundell, T. L., and Mott, H. R. (2003) Molecular dissection of the interaction between the small G proteins Rac1 and RhoA and protein kinase C-related kinase 1 (PRK1) J. Biol. Chem. 278, 50578-50587 (Pubitemid 37548905)
23. Blumenstein, L. and Ahmadian, M. R. (2004) Models of the cooperative mechanism for Rho effector recognition: Implications for RhoA-mediated effector activation J. Biol. Chem. 279, 53419-53426 (Pubitemid 40051846)
24. Maesaki, R., Ihara, K., Shimizu, T., Kuroda, S., Kaibuchi, K., and Hakoshima, T. (1999) The structural basis of Rho effector recognition revealed by the crystal structure of human RhoA complexed with the effector domain of PKN/PRK1 Mol. Cell 4, 793-803
25. Modha, R., Campbell, L. J., Nietlispach, D., Buhecha, H. R., Owen, D., and Mott, H. R. (2008) The Rac1 Polybasic Region Is Required for Interaction with Its Effector PRK1 J. Biol. Chem. 283, 1492-1500
26. Strugnell, S. A., Wiefling, B. A., and DeLuca, H. F. (1997) A modified pGEX vector with a C-terminal histidine tag: Recombinant double-tagged protein obtained in greater yield and purity Anal. Biochem. 254, 147-149 (Pubitemid 27523241)
27. Long, A. C., Orr, D. C., Cameron, J. M., Dunn, B. M., and Kay, J. (1989) A Consensus Sequence for Substrate Hydrolysis by Rhinovirus 3c Proteinase FEBS Lett. 258, 75-78 (Pubitemid 19283731)
28. Mach, H., Middaugh, C. R., and Lewis, R. V. (1992) Statistical Determination of the Average Values of the Extinction Coefficients of Tryptophan and Tyrosine in Native Proteins Anal. Biochem. 200, 74-80
29. Fenwick, R. B., Prasannan, S., Campbell, L. J., Nietlispach, D., Evetts, K. A., Camonis, J., Mott, H. R., and Owen, D. (2009) Solution Structure and Dynamics of the Small GTPase RalB in Its Active Conformation: Significance for Effector Protein Binding Biochemistry 48, 2192-2206
30. Graham, D. L., Eccleston, J. F., and Lowe, P. N. (1999) The conserved arginine in Rho-GTPase-activating protein is essential for efficient catalysis but not for complex formation with rho CDP and aluminum fluoride Biochemistry 38, 985-991
31. Whitmore, L. and Wallace, B. A. (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data Nucleic Acids Res. 32, W668-W673
32. Whitmore, L. and Wallace, B. A. (2008) Protein secondary structure analyses from circular dichroism spectroscopy: Methods and reference databases Biopolymers 89, 392-400
33. Compton, L. A. and Johnson, W. C. (1986) Analysis of Protein Circular-Dichroism Spectra for Secondary Structure Using a Simple Matrix Multiplication Anal. Biochem. 155, 155-167 (Pubitemid 16034476)
34. Sreerama, N. and Woody, R. W. (2000) Analysis of protein CD spectra: Comparison of CONTIN, SELCON3, and CDSSTR methods in CDPro software Biophys. J. 78, 334A-334A
35. Fenwick, R. B., Campbell, L. J., Rajasekar, K., Prasannan, S., Nietlispach, D., Camonis, J., Owen, D., and Mott, H. R. (2010) The RaIB-RLIP76 Complex Reveals a Novel Mode of RaI-Effector Interaction Structure 18, 985-995
36. Li, Y., Kaur, H., and Oakley, M. G. (2008) Probing the recognition properties of the antiparallel coiled coil motif from PKN by protein grafting Biochemistry 47, 13564-13572
37. Linding, R., Russell, R. B., Neduva, V., and Gibson, T. J. (2003) GlobPlot: Exploring protein sequences for globularity and disorder Nucleic Acids Res. 31, 3701-3708 (Pubitemid 37442227)
38. Rost, B., Yachdav, G., and Liu, J. F. (2004) The PredictProtein server Nucleic Acids Res. 32, W321-W326
39. Moreira, I. S., Fernandes, P. A., and Ramos, M. J. (2007) Hot spots: A review of the protein-protein interface determinant amino-acid residues Proteins 68, 803-812 (Pubitemid 47434705)
40. Elliot-Smith, A. E., Mott, H. R., Lowe, P. N., Laue, E. D., and Owen, D. (2005) Specificity Determinants on Cdc42 for Binding Its Effector Protein ACK Biochemistry 44, 12373-12383 (Pubitemid 41324329)
41. Kitagawa, M., Shibata, H., Toshimori, M., Mukai, H., and Ono, Y. (1996) The role of the unique motifs in the amino-terminal region of PKN on its enzymatic activity Biochem. Biophys. Res. Commun. 220, 963-968 (Pubitemid 26198622)
42. Lu, Y. and Settleman, J. (1999) The Drosophila Pkn protein kinase is a Rho Rac effector target required for dorsal closure during embryogenesis Genes Dev. 13, 1168-1180 (Pubitemid 29233147)