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(The FASEB Journal. 2000;14:231-241.)
© 2000 FASEB

The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains

BRIAN K. KAY*1, MICHAEL P. WILLIAMSON{dagger} and MARIUS SUDOL{ddagger}

* Department of Pharmacology, University of Wisconsin-Madison, Madison, Wisconsin 53706-1532, USA;
{dagger} Department of Molecular Biology and Biotechnology, University of Sheffield, Western Bank, Sheffield S10 2TN, United Kingdom;
{ddagger} Department of Biochemistry and Molecular Biology, Mount Sinai School of Medicine, New York, New York 10029-6574, USA

1Correspondence: Department of Pharmacology, University of Wisconsin, 1300 University Ave., Madison, WI 53706-1532, USA. E-mail: bkkay{at}facstaff.wisc.edu

Acommon focus among molecular and cellular biologists is the identification of proteins that interact with each other. Yeast two-hybrid, cDNA expression library screening, and coimmunoprecipitation experiments are powerful methods for identifying novel proteins that bind to one’s favorite protein for the purpose of learning more regarding its cellular function. These same techniques, coupled with truncation and mutagenesis experiments, have been used to define the region of interaction between pairs of proteins. One conclusion from this work is that many interactions occur over short regions, often less than 10 amino acids in length within one protein. For example, mapping studies and 3-dimensional analyses of antigen–antibody interactions have revealed that epitopes are typically 4–7 residues long (1) . Other examples include protein-interaction modules, such as Src homology (SH) 2 and 3 domains, phosphotyrosine binding domains (PTB), postsynaptic density/disc-large/ZO1 (PDZ) domains, WW domains, Eps15 homology (EH) domains, and 14–3-3 proteins that typically recognize linear regions of 3–9 amino acids. Each of these domains has been the subject of recent reviews published elsewhere (2 3 4 5 6 7) . Among the primary structures of many ligands for protein–protein interactions, the amino acid proline is critical. In particular, SH3, WW, and several new protein-interaction domains prefer ligand sequences that are proline-rich. In addition, even though ligands for EH domains and 14–3-3 domains are not proline-rich, they do include a single proline residue. This review highlights the analysis of those protein–protein interactions that involve proline residues, the biochemistry of proline, and current drug discovery efforts based on proline peptidomimetics.—Kay, B. K., Williamson, M. P., Sudol, M. The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains.




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J. S. Lee, J. H. Kim, I. H. Jang, H. S. Kim, J. M. Han, A. Kazlauskas, H. Yagisawa, P.-G. Suh, and S. H. Ryu
Phosphatidylinositol (3,4,5)-trisphosphate specifically interacts with the phox homology domain of phospholipase D1 and stimulates its activity
J. Cell Sci., October 1, 2005; 118(19): 4405 - 4413.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
M. Kofler, K. Motzny, M. Beyermann, and C. Freund
Novel Interaction Partners of the CD2BP2-GYF Domain
J. Biol. Chem., September 30, 2005; 280(39): 33397 - 33402.
[Abstract] [Full Text] [PDF]


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Circ. Res.Home page
W. S. Choi, A. Khurana, R. Mathur, V. Viswanathan, D. F. Steele, and D. Fedida
Kv1.5 Surface Expression Is Modulated by Retrograde Trafficking of Newly Endocytosed Channels by the Dynein Motor
Circ. Res., August 19, 2005; 97(4): 363 - 371.
[Abstract] [Full Text] [PDF]


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JCOHome page
A. Mani and E. P. Gelmann
The Ubiquitin-Proteasome Pathway and Its Role in Cancer
J. Clin. Oncol., July 20, 2005; 23(21): 4776 - 4789.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
E. Solomaha, F. L. Szeto, M. A. Yousef, and H. C. Palfrey
Kinetics of Src Homology 3 Domain Association with the Proline-rich Domain of Dynamins: SPECIFICITY, OCCLUSION, AND THE EFFECTS OF PHOSPHORYLATION
J. Biol. Chem., June 17, 2005; 280(24): 23147 - 23156.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
J. C. Ferreon, A. C. M. Ferreon, K. Li, and S. M. Lemon
Molecular Determinants of TRIF Proteolysis Mediated by the Hepatitis C Virus NS3/4A Protease
J. Biol. Chem., May 27, 2005; 280(21): 20483 - 20492.
[Abstract] [Full Text] [PDF]


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RNAHome page
R. J. GRAINGER and J. D. BEGGS
Prp8 protein: At the heart of the spliceosome
RNA, May 1, 2005; 11(5): 533 - 557.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
G. Bour, J.-L. Plassat, A. Bauer, S. Lalevee, and C. Rochette-Egly
Vinexin {beta} Interacts with the Non-phosphorylated AF-1 Domain of Retinoid Receptor {gamma} (RAR{gamma}) and Represses RAR{gamma}-mediated Transcription
J. Biol. Chem., April 29, 2005; 280(17): 17027 - 17037.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
E. Wessels, D. Duijsings, R. A. Notebaart, W. J. G. Melchers, and F. J. M. van Kuppeveld
A Proline-Rich Region in the Coxsackievirus 3A Protein Is Required for the Protein To Inhibit Endoplasmic Reticulum-to-Golgi Transport
J. Virol., April 15, 2005; 79(8): 5163 - 5173.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
N. Watanabe and E. Lam
Two Arabidopsis Metacaspases AtMCP1b and AtMCP2b Are Arginine/Lysine-specific Cysteine Proteases and Activate Apoptosis-like Cell Death in Yeast
J. Biol. Chem., April 15, 2005; 280(15): 14691 - 14699.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Gastrointest. Liver Physiol.Home page
H. I. Akbarali
Signal-Transduction Pathways that Regulate Smooth Muscle Function II. Receptor-ion channel coupling mechanisms in gastrointestinal smooth muscle
Am J Physiol Gastrointest Liver Physiol, April 1, 2005; 288(4): G598 - G602.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
M. Srinivasan, D. Lu, R. Eri, D. D. Brand, A. Haque, and J. S. Blum
CD80 Binding Polyproline Helical Peptide Inhibits T Cell Activation
J. Biol. Chem., March 18, 2005; 280(11): 10149 - 10155.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
G. Zhu, K. Fujii, N. Belkina, Y. Liu, M. James, J. Herrero, and S. Shaw
Exceptional Disfavor for Proline at the P+1 Position among AGC and CAMK Kinases Establishes Reciprocal Specificity between Them and the Proline-directed Kinases
J. Biol. Chem., March 18, 2005; 280(11): 10743 - 10748.
[Abstract] [Full Text] [PDF]


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Mol. Cell. Biol.Home page
M. J. Winters and P. M. Pryciak
Interaction with the SH3 Domain Protein Bem1 Regulates Signaling by the Saccharomyces cerevisiae p21-Activated Kinase Ste20
Mol. Cell. Biol., March 15, 2005; 25(6): 2177 - 2190.
[Abstract] [Full Text] [PDF]


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Hum Mol GenetHome page
Q. Y. Zheng, D. Yan, X. M. Ouyang, L. L. Du, H. Yu, B. Chang, K. R. Johnson, and X. Z. Liu
Digenic inheritance of deafness caused by mutations in genes encoding cadherin 23 and protocadherin 15 in mice and humans
Hum. Mol. Genet., January 1, 2005; 14(1): 103 - 111.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
M. Pekkala, R. Hieta, U. Bergmann, K. I. Kivirikko, R. K. Wierenga, and J. Myllyharju
The Peptide-Substrate-binding Domain of Collagen Prolyl 4-Hydroxylases Is a Tetratricopeptide Repeat Domain with Functional Aromatic Residues
J. Biol. Chem., December 10, 2004; 279(50): 52255 - 52261.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
X. Gan, Z. Ma, N. Deng, J. Wang, J. Ding, and L. Li
Involvement of the C-terminal Proline-rich Motif of G Protein-coupled Receptor Kinases in Recognition of Activated Rhodopsin
J. Biol. Chem., November 26, 2004; 279(48): 49741 - 49746.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
T. K. Peterman, Y. M. Ohol, L. J. McReynolds, and E. J. Luna
Patellin1, a Novel Sec14-Like Protein, Localizes to the Cell Plate and Binds Phosphoinositides
Plant Physiology, October 1, 2004; 136(2): 3080 - 3094.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
B. Perez-Villamil, M. Mirasierra, and M. Vallejo
The Homeoprotein Alx3 Contains Discrete Functional Domains and Exhibits Cell-specific and Selective Monomeric Binding and Transactivation
J. Biol. Chem., September 3, 2004; 279(36): 38062 - 38071.
[Abstract] [Full Text] [PDF]


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Infect. Immun.Home page
T. B. Seifert, A. S. Bleiweis, and L. J. Brady
Contribution of the Alanine-Rich Region of Streptococcus mutans P1 to Antigenicity, Surface Expression, and Interaction with the Proline-Rich Repeat Domain
Infect. Immun., August 1, 2004; 72(8): 4699 - 4706.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
Y. Kato, K. Nagata, M. Takahashi, L. Lian, J. J. Herrero, M. Sudol, and M. Tanokura
Common Mechanism of Ligand Recognition by Group II/III WW Domains: REDEFINING THEIR FUNCTIONAL CLASSIFICATION
J. Biol. Chem., July 23, 2004; 279(30): 31833 - 31841.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
L. Bacon, R. A. Eagle, M. Meyer, N. Easom, N. T. Young, and J. Trowsdale
Two Human ULBP/RAET1 Molecules with Transmembrane Regions Are Ligands for NKG2D
J. Immunol., July 15, 2004; 173(2): 1078 - 1084.
[Abstract] [Full Text] [PDF]


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Mol Biol EvolHome page
H. Johannesson, P. Vidal, J. Guarro, R. A. Herr, G. T. Cole, and J. W. Taylor
Positive Directional Selection in the Proline-Rich Antigen (PRA) Gene Among the Human Pathogenic Fungi Coccidioides immitis, C. posadasii and Their Closest Relatives
Mol. Biol. Evol., June 1, 2004; 21(6): 1134 - 1145.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
F. Cocchi, D. Fusco, L. Menotti, T. Gianni, R. J. Eisenberg, G. H. Cohen, and G. Campadelli-Fiume
The soluble ectodomain of herpes simplex virus gD contains a membrane-proximal pro-fusion domain and suffices to mediate virus entry
PNAS, May 11, 2004; 101(19): 7445 - 7450.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
N. B. Reuven, S. Antoku, and S. K. Weller
The UL12.5 Gene Product of Herpes Simplex Virus Type 1 Exhibits Nuclease and Strand Exchange Activities but Does Not Localize to the Nucleus
J. Virol., May 1, 2004; 78(9): 4599 - 4608.
[Abstract] [Full Text] [PDF]


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Mol. Endocrinol.Home page
F. Barletta, C.-W. Wong, C. McNally, B. S. Komm, B. Katzenellenbogen, and B. J. Cheskis
Characterization of the Interactions of Estrogen Receptor and MNAR in the Activation of cSrc
Mol. Endocrinol., May 1, 2004; 18(5): 1096 - 1108.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
M. A. Suico, H. Yoshida, Y. Seki, T. Uchikawa, Z. Lu, T. Shuto, K. Matsuzaki, M. Nakao, J.-D. Li, and H. Kai
Myeloid Elf-1-like Factor, an ETS Transcription Factor, Up-regulates Lysozyme Transcription in Epithelial Cells through Interaction with Promyelocytic Leukemia Protein
J. Biol. Chem., April 30, 2004; 279(18): 19091 - 19098.
[Abstract] [Full Text] [PDF]


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Mol Cancer ResHome page
Y. Cui, Y.-C. Liao, and S. H. Lo
Epidermal Growth Factor Modulates Tyrosine Phosphorylation of a Novel Tensin Family Member, Tensin3
Mol. Cancer Res., April 1, 2004; 2(4): 225 - 232.
[Abstract] [Full Text] [PDF]


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JCBHome page
J. I.S. MacDonald, C. J. Kubu, and S. O. Meakin
Nesca, a novel adapter, translocates to the nuclear envelope and regulates neurotrophin-induced neurite outgrowth
J. Cell Biol., March 15, 2004; 164(6): 851 - 862.
[Abstract] [Full Text] [PDF]


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DevelopmentHome page
J. R. Dinneny, R. Yadegari, R. L. Fischer, M. F. Yanofsky, and D. Weigel
The role of JAGGED in shaping lateral organs
Development, March 1, 2004; 131(5): 1101 - 1110.
[Abstract] [Full Text] [PDF]


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Protein Eng Des SelHome page
B. Ravi Chandra, R. Gowthaman, R. Raj Akhouri, D. Gupta, and A. Sharma
Distribution of proline-rich (PxxP) motifs in distinct proteomes: functional and therapeutic implications for malaria and tuberculosis
Protein Eng. Des. Sel., February 1, 2004; 17(2): 175 - 182.
[Abstract] [Full Text] [PDF]


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Mol. Biol. CellHome page
A. Nagasaki and T. Q.P. Uyeda
DWWA, a Novel Protein Containing Two WW Domains and an IQ Motif, Is Required for Scission of the Residual Cytoplasmic Bridge during Cytokinesis in Dictyostelium
Mol. Biol. Cell, February 1, 2004; 15(2): 435 - 446.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
P. Alvarez, C. A. Buscaglia, and O. Campetella
Improving Protein Pharmacokinetics by Genetic Fusion to Simple Amino Acid Sequences
J. Biol. Chem., January 30, 2004; 279(5): 3375 - 3381.
[Abstract] [Full Text] [PDF]




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