A case study of proline isomerization in cell signaling

Frontiers in Bioscience

Volumn 10, Issue 1, 2005, Pages 385-397

  Min, Lie ^a   Fulton, D Bruce ^a   Andreotti, Amy H ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

Cyclophilin A; Dimerization; Itk; Kinase regulation; NMR spectroscopy; Proline isomerization; Review

Indexed keywords

CYCLOPHILIN; CYCLOPHILIN A; CYCLOSPORIN A; PROLINE; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE ITK; T LYMPHOCYTE RECEPTOR; TSUKUBAENOLIDE; TYROSINE; UNCLASSIFIED DRUG;

AUTOPHOSPHORYLATION; DIMERIZATION; ENZYME ACTIVATION; ENZYME INACTIVATION; ENZYME REGULATION; ISOMERIZATION; LIGAND BINDING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OLIGOMERIZATION; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

EID: 17444366952     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/1536     Document Type: Review

References (109)

1. Rosen, M. K., and Schreiber, S. L. Natural products as probes of cellular function: studies of immunophilins. Angew. Chem. Int. Ed Engl. 31, 384-400 (1992)
2. Harding, M. W., Galat, A., Uehling, D. E., and Schreiber, S. L. A receptor for the immunosuppressant FK506 is a cis-trans peptidyl-prolyl isomerase. Nature 341, 758-760 (1989)
3. Fischer, G., Wittmann-Liebold, B., Lang, K., Kiefhaber, T., and Schmid, F. X. Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature 337, 476-478 (1989)
4. Takahashi, N., Hayano, T., and Suzuki, M. Peptidyl-prolyl cis-trans isomerase is the cyclosporin A-binding protein cyclophilin. Nature 337, 473-475 (1989)
5. Jin, L., and Harrison, S. C. Crystal structure of human calcineurin complexed with cyclosporin A and human cyclophilin. Proc. Natl. Acad. Sci. U S A 99, 13522-13526 (2002)
6. Ke, H., and Huai, Q. Structures of calcineurin and its complexes with immunophilins-immunosuppressants. Biochem. Biophys. Res. Commun. 311, 1095-1102 (2003)
7. Liu, J., Farmer, J. D., Jr., Lane, W. S., Friedman, J., Weissman, I., and Schreiber, S. L. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes Cell 66, 807-815 (1991)
8. Lu, K. P., Hanes, S. D., and Hunter, T. A human peptidyl-prolyl isomerase essential for regulation of mitosis. Nature 380, 544-547 (1996)
9. Yaffe, M. B., Schutkowski, M., Shen, M., Zhou, X. Z., Stukenberg, P. T., Rahfeld, J. U., Xu, J., Kuang, J., Kirschner, M. W., Fischer, G., Cantley, L. C., and Lu, K. P. Sequence-specific and phosphorylation-dependent proline isomerization: a potential mitotic regulatory mechanism. Science 278, 1957-1960 (1997)
10. Lu, K. P., Liou, Y. C., and Zhou, X. Z. Pinning down proline-directed phosphorylation signaling. Trends Cell Biol. 12, 164-172 (2002)
11. Lu, K. P. Pinning down cell signaling, cancer and Alzheimer's disease. Trends Biochem. Sci. 29, 200-209 (2004)
12. Joseph, J. D., Yeh, E. S., Swenson, K. I., Means, A. R., and Winkler The peptidyl-prolyl isomerase Pin1. Prog. Cell Cycle Res. 5, 477-487 (2003)
13. Bergsma, D. J., Eder, C., Gross, M., Kersten, H., Sylvester, D., Appelbaum, E., Cusimano, D., Livi, G. P., McLaughlin, M. M., Kasyan, K., Porter, T. G., Silverman, C., Dunnington, D., Hand, A., Prichett, W. P., Bossard, M. J., Brandt, M., and Levy, M. The cyclophilin multigene family of peptidyl-prolyl isomerases. Characterization of three separate human isoforms. J. Biol. Chem. 266, 23204-23214 (1991)
14. Fischer, G., Bang, H., and Mech, C. [Determination of enzymatic catalysis for the cis-trans-isomerization of peptide binding in proline-containing peptides]. Biomed. Biochim. Acta 43, 1101-1111 (1984)
15. Lin, L. N., and Brandts, J. F. Role of cis-trans isomerism of the peptide bond in protease specificity. Kinetic studies on small proline-containing peptides and on polyproline. Biochemistry 18, 5037-5042 (1979)
16. Lin, L. N., and Brandts, J. F. Evidence suggesting that some proteolytic enzymes may cleave only the trans form of the peptide bond. Biochemistry 18, 43-47 (1979)
17. Balbach, J., and Schmid, F. X., eds Prolyl isomerization and its catalysis in protein folding., Oxford University Press, Oxford (2000)
18. Brandts, J. F., Halvorson, H. R., and Brennan, M. Consideration of the possibility that the slow step in protein denaturation reactions is due to cis-trans isomerism of proline residues. Biochemistry 14, 4953-4963 (1975)
19. Steinmann, B., Bruckner, P., and Superti-Furga, A. Cyclosporin A slows collagen triple-helix formation in vivo: indirect evidence for a physiologic role of peptidyl-prolyl cis-trans-isomerase. J. Biol. Chem. 266, 1299-1303 (1991)
20. Kruse, M., Brunke, M., Escher, A., Szalay, A. A., Tropschug, M., and Zimmermann, R. Enzyme assembly after de novo synthesis in rabbit reticulocyte lysate involves molecular chaperones and immunophilins. J. Biol. Chem. 270, 2588-2594 (1995)
21. Gothel, S. F., and Marahiel, M. A. Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell. Mol. Life Sci. 55, 423-436 (1999)
22. Schmid, F. X., Lang, K., Kiefhaber, T., Mayer, S., and Schonbrunner, R., eds Prolyl isomerase. Its role in protein folding and speculations on its function in the cell., American Association for the Advancement of Science, Washington DC (1991)
23. Uittenbogaard, A., Ying, Y., and Smart, E. J. Characterization of a cytosolic heat-shock protein-caveolin chaperone complex. Involvement in cholesterol trafficking. J. Biol. Chem. 273, 6525-6532 (1998)
24. Zander, K., Sherman, M. P., Tessmer, U., Bruns, K., Wray, V., Prechtel, A. T., Schubert, E., Henklein, P., Luban, J., Neidleman, J., Greene, W. C., and Schubert, U. Cyclophilin A interacts with HIV-1 Vpr and is required for its functional expression. J. Biol. Chem. 278, 43202-43213 (2003)
25. Krummrei, U., Bang, R., Schmidtchen, R., Brune, K., and Bang, H. Cyclophilin-A is a zinc-dependent DNA binding protein in macrophages. FEBS Lett. 371, 47-51 (1995)
26. Nahreini, P., Hovland, A. R., Kumar, B., Andreatta, C., Edwards-Prasad, J., and Prasad, K. N. Effects of altered cyclophilin A expression on growth and differentiation of human and mouse neuronal cells. Cell. Mol. Neurobiol. 21, 65-79 (2001)
27. Hamilton, G. S., and Steiner, J. P. Immunophilins: beyond immunosuppression. J. Med. Chem. 41, 5119-5143 (1998)
28. Brazin, K. N., Mallis, R. J., Fulton, D. B., and Andreotti, A. H. Regulation of the tyrosine kinase Itk by the peptidyl-prolyl isomerase cyclophilin A. Proc. Natl. Acad. Sci. U S A 99, 1899-1904 (2002)
29. Hong, F., Lee, J., Piao, Y. J., Jae, Y. K., Kim, Y. J., Oh, C., Seo, J. S., Yun, Y. S., Yang, C. W., Ha, J., and Kim, S. S. Transgenic mice overexpressing cyclophilin A are resistant to cyclosporin A-induced nephrotoxicity via peptidyl-prolyl cis-trans isomerase activity. Biochem. Biophys. Res. Commun. 316, 1073-1080 (2004)
30. Doyle, V., Virji, S., and Crompton, M. Evidence that cyclophilin-A protects cells against oxidative stress. Biochem. J. 341 (Pt 1), 127-132 (1999)
31. Lee, J. P., Palfrey, H. C., Bindokas, V. P., Ghadge, G. D., Ma, L., Miller, R. J., and Roos, R. P. The role of immunophilins in mutant superoxide dismutase-1 linked familial amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U S A 96, 3251-3256 (1999)
32. Rycyzyn, M. A., and Clevenger, C. V. The intranuclear prolactin/cyclophilin B complex as a transcriptional inducer. Proc. Natl. Acad. Sci. U S A 99, 6790-6795 (2002)
33. Yurchenko, V., Zybarth, G., O'Connor, M., Dai, W. W., Franchin, G., Hao, T., Guo, H., Hung, H. C., Toole, B., Gallay, P., Sherry, B., and Bukrinsky, M. Active site residues of cyclophilin A are crucial for its signaling activity via CD147. J. Biol. Chem. 277, 22959-22965 (2002)
34. Alonso, A., Sasin, J., Bottini, N., Friedberg, I., Osterman, A., Godzik, A., Hunter, T., Dixon, J., and Mustelin, T. Protein tyrosine phosphatases in the human genome. Cell 117, 699-711 (2004)
35. Pawson, T. Tyrosine kinase signalling pathways. Princess Takamatsu Symp. 24, 303-322 (1994)
36. Schwartzberg, P. L. The many faces of Src: multiple functions of a prototypical tyrosine kinase. Oncogene 17, 1463-1468 (1998)
37. Harrison, S. C. Variation on an Src-like theme. Cell 112, 737-740 (2003)
38. Williams, J. C., Wierenga, R. K., and Saraste, M. Insights into Src kinase functions: structural comparisons. Trends Biochem. Sci. 23, 179-184 (1998)
39. Sicheri, F., Moarefi, I., and Kuriyan, J. Crystal structure of the Src family tyrosine kinase Hck. Nature 385, 602-609 (1997)
40. Xu, W., Harrison, S. C., and Eck, M. J. Three-dimensional structure of the tyrosine kinase c-Src. Nature 385, 595-602 (1997)
41. Yamaguchi, H., and Hendrickson, W. A. Structural basis for activation of human lymphocyte kinase Lck upon tyrosine phosphorylation. Nature 384, 484-489 (1996)
42. Featherstone, C. Src structure crystallizes 20 years of oncogene research. Science 275, 1066 (1997)
43. Okada, M., Nada, S., Yamanashi, Y., Yamamoto, T., and Nakagawa, H. CSK: a protein-tyrosine kinase involved in regulation of src family kinases. J. Biol. Chem. 266, 24249-24252 (1991)
44. Nada, S., Okada, M., MacAuley, A., Cooper, J. A., and Nakagawa, H. Cloning of a complementary DNA for a protein-tyrosine kinase that specifically phosphorylates a negative regulatory site of p60c-src. Nature 351, 69-72 (1991)
45. Berg, L. J., Finkelstein, L. D., Lucas, J. A., and Schwartzberg, P. L. Tec Family Kinases in T lymphocyte development and function. Annual Review of Immunology (2004) in press.
46. Lucas, J. A., Miller, A. T., Atherly, L. O., and Berg, L. J. The role of Tec family kinases in T cell development and function. Immunol. Rev. 191, 119-138 (2003)
47. Miller, A. T., and Berg, L. J. New insights into the regulation and functions of Tec family tyrosine kinases in the immune system. Curr. Opin. Immunol. 14, 331-340 (2002)
48. Smith, C. I., Islam, T. C., Mattsson, P. T., Mohamed, A. J., Nore, B. F., and Vihinen, M. The Tec family of cytoplasmic tyrosine kinases: mammalian Btk, Bmx, Itk, Tec, Txk and homologs in other species. Bioessays 23, 436-446 (2001)
49. Andreotti, A. H., Bunnell, S. C., Feng, S., Berg, L. J., and Schreiber, S. L. Regulatory intramolecular association in a tyrosine kinase of the Tec family. Nature 385, 93-97 (1997)
50. Brazin, K. N., Fulton, D. B., and Andreotti, A. H. A specific intermolecular association between the regulatory domains of a Tec family kinase. J. Mol. Biol. 302, 607-623 (2000)
51. Laederach, A., Cradic, K. W., Brazin, K. N., Zamoon, J., Fulton, D. B., Huang, X. Y., and Andreotti, A. H. Competing modes of self-association in the regulatory domains of Bruton's tyrosine kinase: intramolecular contact versus asymmetric homodimerization. Protein Sci. 11, 36-45 (2002)
52. Laederach, A., Cradic, K. W., Fulton, D. B., and Andreotti, A. H. Determinants of intra versus intermolecular self-association within the regulatory domains of Rlk and Itk. J. Mol. Biol. 329, 1011-1020 (2003)
53. Pursglove, S. E., Mulhern, T. D., Mackay, J. P., Hinds, M. G., and Booker, G. W. The solution structure and intramolecular associations of the Tec kinase SRC homology 3 domain. J. Biol. Chem. 277, 755-762 (2002)
54. Hansson, H., Okoh, M. P., Smith, C. I., Vihinen, M., and Hard, T. Intermolecular interactions between the SH3 domain and the proline-rich TH region of Bruton's tyrosine kinase. FEBS Lett. 489, 67-70 (2001)
55. Xu, W., Doshi, A., Lei, M., Eck, M. J., and Harrison, S. C. Crystal structures of c-Src reveal features of its autoinhibitory mechanism. Mol. Cell 3, 629-638 (1999)
56. Heyeck, S. D., and Berg, L. J. Developmental regulation of a murine T-cell-specific tyrosine kinase gene, Tsk. Proc. Natl. Acad. Sci. U S A 90, 669-673 (1993)
57. Siliciano, J. D., Morrow, T. A., and Desiderio, S. V. itk, a T-cell-specific tyrosine kinase gene inducible by interleukin 2. Proc. Natl. Acad. Sci. U S A 89, 11194-11198 (1992)
58. Colgan, J., Asmal, M., Yu, B., Schneidkraut, J., Youngnam, L., Neagu, M., Andreotti, A. H., and Luban, J. Cyclophilin A regulates TCR signal strength in CD4+ T cells via a proline-directed conformational switch in Itk. Immunity (2004) in press.
59. Mallis, R. J., Brazin, K. N., Fulton, D. B., and Andreotti, A. H. Structural characterization of a proline-driven conformational switch within the Itk SH2 domain. Nat. Struct. Biol. 9, 900-905 (2002)
60. Breheny, P. J., Laederach, A., Fulton, D.B. and Andreotti, A.H. Ligand Specificity Modulated by Prolyl Imide Bond Cis/Trans Isomerization in the Itk SH2 Domain: A Quantitative NMR Study. Journal of the American Chemical Society 125, 15706-15707 (2003)
61. Grathwohl, C., and Wuthrich, K. NMR studies of the molecular conformations in the linear oligopeptides H-(L-Ala)n-L-Pro-OH. Biopolymers 15, 2043-2057 (1976)
62. Cheng, H. N., and Bovey, F. A. Cis-trans equilibrium and kinetic studies of acetyl-L-proline and glycyl-L-proline. Biopolymers 16, 1465-1472 (1977)
63. Grathwohl, C., and Wüthrich, K. NMR studies of the rates of proline cis-trans isomerization in oligopeptides. Biopolymers 20, 2623-2633 (1981)
64. Fischer, G. Chemical aspects of peptide bond isomerisation. Chemical Society Reviews 29, 119-127 (2000)
65. Stein, R. L. Mechanism of enzymatic and nonenzymatic prolyl cis-trans isomerization. Adv. Protein Chem. 44, 1-24 (1993)
66. Reimer, U., and Fischer, G. Local structural changes caused by peptidyl-prolyl cis/trans isomerization in the native state of proteins. Biophys. Chem. 96, 203-212 (2002)
67. Andreotti, A. H. Native state proline isomerization: an intrinsic molecular switch. Biochemistry 42, 9515-9524 (2003)
68. Mori, S., Abeygunawardana, C., Johnson, M. O., and van Zijl, P. C. Improved sensitivity of HSQC spectra of exchanging protons at short interscan delays using a new fast HSQC (FHSQC) detection scheme that avoids water saturation. J. Magn. Reson. B 108, 94-98 (1995)
69. Santiveri, C. M., Manuel Perez-Canadillas, J., Vadivelu, M. K., Allen, M. D., Rutherford, T. J., Watkins, N. A., and Bycroft, M. NMR structure of the alpha - hemoglobin chaperone AHSP: Insights into conformational heterogeneity and binding. J. Biol. Chem. (2004) in press.
70. Grochulski, P., Li, Y., Schrag, J. D., and Cygler, M. Two conformational states of Candida rugosa lipase. Protein Sci. 3, 82-91 (1994)
71. Yuan, X., Werner, J. M., Knott, V., Handford, P. A., Campbell, I. D., and Downing, K. Effects of proline cis-trans isomerization on TB domain secondary structure. Protein Sci. 7, 2127-2135 (1998)
72. Song, J., Laskowski, M., Jr., Qasim, M. A., and Markley, J. L. Two conformational states of Turkey ovomucoid third domain at low pH: three-dimensional structures, internal dynamics, and interconversion kinetics and thermodynamics. Biochemistry 42, 6380-6391 (2003)
73. Pawson, T., Gish, G. D., and Nash, P. SH2 domains, interaction modules and cellular wiring. Trends Cell. Biol. 11, 504-511 (2001)
74. Marengere, L. E., and Pawson, T. Structure and function of SH2 domains. J Cell Sci Suppl 18, 97-104 (1994)
75. Wilcox, H. M., and Berg, L. J. Itk phosphorylation sites are required for functional activity in primary T cells. J. Biol. Chem. 278, 37112-37121 (2003)
76. Heyeck, S. D., Wilcox, H. M., Bunnell, S. C., and Berg, L. J. Lck phosphorylates the activation loop tyrosine of the Itk kinase domain and activates Itk kinase activity. J. Biol. Chem. 272, 25401-25408 (1997)
77. Brown, K., Long, J. M., Vial, S. C., Dedi, N., Dunster, N. J., Renwick, S. B., Tanner, A. J., Frantz, J. D., Fleming, M. A., and Cheetham, G. M. Crystal structures of interleukin-2 tyrosine kinase and their implications for the design of selective inhibitors. J. Biol. Chem. 279, 18727-18732 (2004)
78. Mao, C., Zhou, M., and Uckun, F. M. Crystal structure of Bruton's tyrosine kinase domain suggests a novel pathway for activation and provides insights into the molecular basis of X-linked agammaglobulinemia. J. Biol. Chem. 276, 41435-41443 (2001)
79. Hawkins, J., and Marcy, A. Characterization of Itk tyrosine kinase: contribution of noncatalytic domains to enzymatic activity. Protein Expr. Purif. 22, 211-219 (2001)
80. Bunnell, S. C., Diehn, M., Yaffe, M. B., Findell, P. R., Cantley, L. C., and Berg, L. J. Biochemical interactions integrating Itk with the T cell receptor-initiated signaling cascade. J. Biol. Chem. 275, 2219-2230 (2000)
81. Ching, K. A., Grasis, J. A., Tailor, P., Kawakami, Y., Kawakami, T., and Tsoukas, C. D. TCR/CD3-Induced activation and binding of Emt/Itk to linker of activated T cell complexes: requirement for the Src homology 2 domain. J. Immunol. 165, 256-262 (2000)
82. Tsoukas, C. D., Grasis, J. A., Ching, K. A., Kawakami, Y., and Kawakami, T. Itk/Emt: a link between T cell antigen receptor-mediated Ca2+ events and cytoskeletal reorganization. Trends Immunol. 22, 17-20 (2001)
83. Morrogh, L. M., Hinshelwood, S., Costello, P., Cory, G. O., and Kinnon, C. The SH3 domain of Bruton's tyrosine kinase displays altered ligand binding properties when auto-phosphorylated in vitro. Eur. J. Immunol. 29, 2269-2279 (1999)
84. Gupta, S., Xie, J., Ma, J., and Davis, P. B. Intermolecular interaction between R domains of cystic fibrosis transmembrane conductance regulator. Am. J. Respir. Cell. Mol. Biol. 30, 242-248 (2004)
85. Thies, M. J., Mayer, J., Augustine, J. G., Frederick, C. A., Lilie, H., and Buchner, J. Folding and association of the antibody domain CH3: prolyl isomerization preceeds dimerization. J. Mol. Biol. 293, 67-79 (1999)
86. Martin, A., and Schmid, F. X. A proline switch controls folding and domain interactions in the gene-3-protein of the filamentous phage fd. J. Mol. Biol. 331, 1131-1140 (2003)
87. Golmohammadi, R., Valegard, K., Fridborg, K., and Liljas, L. The refined structure of bacteriophage MS2 at 2.8 Å resolution. J. Mol. Biol. 234, 620-639 (1993)
88. Stonehouse, N. J., Valegard, K., Golmohammadi, R., van den Worm, S., Walton, C., Stockley, P. G., and Liljas, L. Crystal structures of MS2 capsids with mutations in the subunit FG loop. J. Mol. Biol. 256, 330-339 (1996)
89. Jager, M., and Pluckthun, A. Folding and assembly of an antibody Fv fragment, a heterodimer stabilized by antigen. J. Mol. Biol. 285, 2005-2019 (1999)
90. Lesieur, C., Cliff, M. J., Carter, R., James, R. F., Clarke, A. R., and Hirst, T. R. A kinetic model of intermediate formation during assembly of cholera toxin B-subunit pentamers. J. Biol. Chem. 277, 16697-16704 (2002)
91. Satumba, W. J., and Mossing, M. C. Folding and assembly of lambda Cro repressor dimers are kinetically limited by proline isomerization. Biochemistry 41, 14216-14224 (2002)
92. Wood, D. C., Jurgensen, S. R., Geesin, J. C., and Harrison, J. H. Subunit Interactions in Mitochondrial Malate Dehydrogenase. J. Biol. Chem. 256, 2377-2382 (1981)
93. Franke, E. K., Yuan, H. E., and Luban, J. Specific incorporation of cyclophilin A into HIV-1 virions. Nature 372, 359-362 (1994)
94. Luban, J., Bossolt, K. L., Franke, E. K., Kalpana, G. V., and Goff, S. P. Human immunodeficiency virus type 1 Gag protein binds to cyclophilins A and B. Cell 73, 1067-1078 (1993)
95. Colgan, J., Yuan, H. E., Franke, E. K., and Luban, J. Binding of the human immunodeficiency virus type 1 Gag polyprotein to cyclophilin A is mediated by the central region of capsid and requires Gag dimerization. J. Virol. 70, 4299-4310 (1996)
96. Prodromou, C., Siligardi, G., O'Brien, R., Woolfson, D. N., Regan, L., Panaretou, B., Ladbury, J. E., Piper, P. W., and Pearl, L. H. Regulation of Hsp90 ATPase activity by tetratricopeptide repeat (TPR)-domain co-chaperones. EMBO J. 18, 754-762 (1999)
97. Carrello, A., Ingley, E., Minchin, R. F., Tsai, S., and Ratajczak, T. The common tetratricopeptide repeat acceptor site for steroid receptor-associated immunophilins and hop is located in the dimerization domain of Hsp90. J. Biol. Chem. 274, 2682-2689 (1999)
98. Grebe, M., Gadea, J., Steinmann, T., Kientz, M., Rahfeld, J. U., Salchert, K., Koncz, C., and Jurgens, G. A conserved domain of the arabidopsis GNOM protein mediates subunit interaction and cyclophilin 5 binding. Plant Cell 12, 343-356 (2000)
99. Bosco, D. A., Eisenmesser, E. Z., Pochapsky, S., Sundquist, W. I., and Kern, D. Catalysis of cis/trans isomerization in native HIV-1 capsid by human cyclophilin A. Proc. Natl. Acad. Sci. U S A 99, 5247-5252 (2002)
100. Edison, A. M., Barker, S. C., Kassel, D. B., Luther, M. A., and Knight, W. B. Exploration of the sequence specificity of pp60c-src tyrosine kinase. Minimal peptide sequence required for maximal activity. J. Biol. Chem. 270, 27112-27115 (1995)
101. Luo, X., Tang, Z., Xia, G., Wassmann, K., Matsumoto, T., Rizo, J., and Yu, H. The Mad2 spindle checkpoint protein has two distinct natively folded states. Nat. Struct. Mol. Biol. 11, 338-345 (2004)
102. Pawson, T. Specificity in signal transduction: from phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 116, 191-203 (2004)
103. Jabs, A., Weiss, M. S., and Hilgenfeld, R. Non-proline cis peptide bonds in proteins. J. Mol. Biol. 286, 291-304 (1999)
104. Weiss, M. S., Jabs, A., and Hilgenfeld, R. Peptide bonds revisited. Nat. Struct. Biol. 5, 676 (1998)
105. Fisher, A. J., Thompson, T. B., Thoden, J. B., Baldwin, T. O., and Rayment, I. The 1.5-Å resolution crystal structure of bacterial luciferase in low salt conditions. J. Biol. Chem. 271, 21956-21968 (1996)
106. Stewart, D. E., Sarkar, A., and Wampler, J. E. Occurrence and role of cis peptide bonds in protein structures. J. Mol. Biol. 214, 253-260 (1990)
107. Canyuk, B., Medrano, F. J., Wenck, M. A., Focia, P. J., Eakin, A. E., and Craig, S. P., 3rd Interactions at the dimer interface influence the relative efficiencies for purine nucleotide synthesis and pyrophosphorolysis in a phosphoribosyltransferase. J. Mol. Biol. 335, 905-921 (2004)
108. Svensson, A. K., O'Neill, J. C., Jr., and Matthews, C. R. The coordination of the isomerization of a conserved non-prolyl cis peptide bond with the rate-limiting steps in the folding of dihydrofolate reductase. J. Mol. Biol. 326, 569-583 (2003)
109. Scholz, C., Scherer, G., Mayr, L. M., Schindler, T., Fischer, G., and Schmid, F. X. Prolyl isomerases do not catalyze isomerization of non-prolyl peptide bonds. Biol. Chem. 379, 361-365 (1998)