The structural basis of Janus kinase 2 inhibition by a potent and specific pan-Janus kinase inhibitor

Blood

Volumn 107, Issue 1, 2006, Pages 176-183

  Lucet, Isabelle S ^c   Fantino, Emmanuelle ^c   Styles, Michelle ^c   Bamert, Rebecca ^c   Patel, Onisha ^c   Broughton, Sophie E ^c   Walter, Mark ^c   Burns, Christopher J ^c   Treutlein, Herbert ^c   Wilks, Andrew F ^b   Rossjohn, Jamie ^a  

^a MONASH UNIVERSITY   (Australia)

^b Cytopia Ltd   (Australia)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

ISOQUINOLINE DERIVATIVE; JANUS KINASE 2; JANUS KINASE INHIBITOR;

ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; ENZYME BINDING; ENZYME CONFORMATION; ENZYME INHIBITION; ENZYME STRUCTURE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; STRUCTURE ANALYSIS;

EID: 30144436273     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2005-06-2413     Document Type: Article

References (66)

1. Firmbach-Kraft I, Byers M, Shows T, Dalla-Favera R, Krolewski JJ. tyk2, prototype of a novel class of non-receptor tyrosine kinase genes. Oncogene. 1990;5:1329-1336.
2. Harpur AG, Andres AC, Ziemiecki A, Aston RR, Wilks AF. JAK2, a third member of the JAK family of protein tyrosine kinases. Oncogene. 1992;7:1347-1353.
3. Rane SG, Reddy EP. JAK3: a novel JAK kinase associated with terminal differentiation of hematopoietic cells. Oncogene. 1994;9:2415-2423.
4. Wilks AF. Two putative protein-tyrosine kinases identified by application of the polymerase chain reaction. Proc Natl Acad Sci U S A. 1989;86:1603-1607.
5. Wilks AF. Cloning members of protein-tyrosine kinase family using polymerase chain reaction. Methods Enzymol. 1991;200:533-546.
6. Sofer L, Kampa D, Burnside J. Molecular cloning of a chicken JAK homolog from activated T cells. Gene. 1998;215:29-36.
7. Oates AC, Brownlie A, Pratt SJ, et al. Gene duplication of zebrafish JAK2 homologs is accompanied by divergent embryonic expression patterns: only jak2a is expressed during erythropoiesis. Blood. 1999;94:2622-2636.
8. Dearolf CR. JAKs and STATs in invertebrate model organisms. Cell Mol Life Sci. 1999;55:1578-1584.
9. Rawlings JS, Rosler KM, Harrison DA. The JAK/STAT signaling pathway. J Cell Sci. 2004;117:1281-1283.
10. Duhe RJ, Farrar WL. Structural and mechanistic aspects of Janus kinases: how the two-faced god wields a double-edged sword. J Interferon Cytokine Res. 1998;18:1-15.
11. Kisseleva T, Bhattacharya S, Braunstein J, Schindler CW. Signaling through the JAK/STAT pathway, recent advances and future challenges. Gene. 2002;285:1-24.
12. Deon D, Ahmed S, Tai K, et al. Cross-talk between IL-1 and IL-6 signaling pathways in rheumatoid arthritis synovial fibroblasts. J Immunol. 2001;167:5395-5403.
13. Hu X, Herrero C, Li WP, et al. Sensitization of IFN-gamma Jak-STAT signaling during macrophage activation. Nat Immunol. 2002;3:859-866.
14. Baxter EJ, Scott LM, Campbell PJ, et al. Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders. Lancet. 2005;365:1054-1061.
15. Levine RL, Wadleigh M, Cools J, et al. Activating mutation in the tyrosine kinase JAK2 in polycythemia vera, essential thrombocythemia, and myeloid metaplasia with myelofibrosis. Cancer Cell. 2005;7:387-397.
16. James C, Ugo V, Le Couedic JP, et al. A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature. 2005;434:1144-1148.
17. Shannon K, Van Etten RA. JAKing up hematopoietic proliferation. Cancer Cell. 2005;7:291-293.
18. Benekli M, Baer MR, Baumann H, Wetzler M. Signal transducer and activator of transcription proteins in leukemias. Blood. 2003;101:2940-2954.
19. Peeters P, Raynaud SD, Cools J, et al. Fusion of TEL, the ETS-variant gene 6 (ETV6), to the receptor-associated kinase JAK2 as a result of t(9;12) in a lymphoid and t(9;15;12) in a myeloid leukemia. Blood. 1997;90:2535-2540.
20. Reiter A, Walz C, Watmore A, et al. The t(8;9)(p22;p24) is a recurrent abnormality in chronic and acute leukemia that fuses PCM1 to JAK2. Cancer Res. 2005;65:2662-2667.
21. Takemoto S, Mulloy JC, Cereseto A, et al. Proliferation of adult T cell leukemia/lymphoma cells is associated with the constitutive activation of JAK/STAT proteins. Proc Natl Acad Sci U S A. 1997;94:13897-13902.
22. Booz GW, Day JN, Speth R, Baker KM. Cytokine G-protein signaling crosstalk in cardiomyocytes: attenuation of Jak-STAT activation by endothelin-1. Mol Cell Biochem. 2002;240:39-46.
23. El-Adawi H, Deng L, Tramontano A, et al. The functional role of the JAK-STAT pathway in post-infarction remodeling. Cardiovasc Res. 2003;57:129-138.
24. Chen M, Cheng A, Candotti F, et al. Complex effects of naturally occurring mutations in the JAK3 pseudokinase domain: evidence for interactions between the kinase and pseudokinase domains. Mol Cell Biol. 2000;20:947-956.
25. Lindauer K, Loerting T, Liedl KR, Kroemer RT. Prediction of the structure of human Janus kinase 2 (JAK2) comprising the two carboxy-terminal domains reveals a mechanism for autoregulation. Protein Eng. 2001;14:27-37.
26. Luo H, Rose P, Barber D, et al. Mutation in the Jak kinase JH2 domain hyperactivates Drosophila and mammalian Jak-Stat pathways. Mol Cell Biol. 1997;17:1562-1571.
27. Saharinen P, Silvennoinen O. The pseudokinase domain is required for suppression of basal activity of Jak2 and Jak3 tyrosine kinases and for cytokine-inducible activation of signal transduction. J Biol Chem. 2002;277:47954-47963.
28. Saharinen P, Takaluoma K, Silvennoinen O. Regulation of the Jak2 tyrosine kinase by its pseudokinase domain. Mol Cell Biol. 2000;20:3387-3395.
29. Saharinen P, Vihinen M, Silvennoinen O. Autoinhibition of Jak2 tyrosine kinase is dependent on specific regions in its pseudokinase domain. Mol Biol Cell. 2003;14:1448-1459.
30. Kampa D, Burnside J. Computational and functional analysis of the putative SH2 domain in Janus kinases. Biochem Biophys Res Commun. 2000;278:175-182.
31. Girault JA, Labesse G, Mornon JP, Callebaut I. Janus kinases and focal adhesion kinases play in the 4.1 band: a superfamily of band 4.1 domains important for cell structure and signal transduction. Mol Med. 1998;4:751-769.
32. Giordanetto F, Kroemer RT. Prediction of the structure of human Janus kinase 2 (JAK2) comprising JAK homology domains 1 through 7. Protein Eng. 2002;15:727-737.
33. Frank SJ, Gilliland G, Kraft AS, Arnold CS. Interaction of the growth hormone receptor cytoplasmic domain with the JAK2 tyrosine kinase. Endocrinology. 1994;135:2228-2239.
34. Argetsinger LS, Campbell GS, Yang X, et al. Identification of JAK2 as a growth hormone receptor-associated tyrosine kinase. Cell. 1993;74:237-244.
35. He K, Wang X, Jiang J, et al. Janus kinase 2 determinants for growth hormone receptor association, surface assembly, and signaling. Mol Endocrinol. 2003;17:2211-2227.
36. Witthuhn BA, Quelle FW, Silvennoinen O, et al. JAK2 associates with the erythropoietin receptor and is tyrosine phosphorylated and activated following stimulation with erythropoietin. Cell. 1993;74:227-236.
37. Rui H, Kirken RA, Farrar WL. Activation of receptor-associated tyrosine kinase JAK2 by prolactin. J Biol Chem. 1994;269:5364-5368.
38. Nicholson SE, Oates AC, Harpur AG, Ziemiecki A, Wilks AF, Layton JE. Tyrosine kinase JAK1 is associated with the granulocyte-colony-stimulating factor receptor and both become tyrosine-phosphorylated after receptor activation. Proc Natl Acad Sci U S A. 1994;91:2985-2988.
39. Silvennoinen O, Witthuhn BA, Quelle FW, Cleveland JL, Yi T, Ihle JN. Structure of the murine Jak2 protein-tyrosine kinase and its role in interleukin 3 signal transduction. Proc Natl Acad Sci U S A. 1993;90:8429-8433.
40. Parganas E, Wang D, Stravopodis D, et al. Jak2 is essential for signaling through a variety of cytokine receptors. Cell. 1998;93:385-395.
41. Neubauer H, Cumano A, Muller M, Wu H, Huffstadt U, Pfeffer K. Jak2 deficiency defines an essential developmental checkpoint in definitive hematopoiesis. Cell. 1998;93:397-409.
42. Thompson JE, Cubbon RM, Cummings RT, et al. Photochemical preparation of a pyridone containing tetracycle: a Jak protein kinase inhibitor. Bioorg Med Chem Lett. 2002;12:1219-1223.
43. Brunger AT, Adams PD, Clore GM, et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr. 1998;54:905-921.
44. Jones TA, Zou JY, Cowan SW, Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A. 1991;47:110-119.
45. Murshudov GN, Vagin AA, Dodson EJ. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr. 1997;53:240-255.
46. Huse M, Kuriyan J. The conformational plasticity of protein kinases. Cell. 2002;109:275-282.
47. Feng J, Witthuhn BA, Matsuda T, Kohlhuber F, Kerr IM, Ihle JN. Activation of Jak2 catalytic activity requires phosphorylation of Y1007 in the kinase activation loop. Mol Cell Biol. 1997;17:2497-2501.
48. Flowers LO, Johnson HM, Mujtaba MG, Ellis MR, Haider SM, Subramaniam PS. Characterization of a peptide inhibitor of Janus kinase 2 that mimics suppressor of cytokine signaling 1 function. J Immunol. 2004;172:7510-7518.
49. Giordanetto F, Kroemer RT. A three-dimensional model of Suppressor Of Cytokine Signalling 1 (SOCS-1). Protein Eng. 2003;16:115-124.
50. Myers MP, Andersen JN, Cheng A, et al. TYK2 and JAK2 are substrates of protein-tyrosine phosphatase 1B. J Biol Chem. 2001;276:47771-47774.
51. Yoshikawa H, Matsubara K, Qian GS, et al. SOCS-1, a negative regulator of the JAK/STAT pathway, is silenced by methylation in human hepatocellular carcinoma and shows growth-suppression activity. Nat Genet. 2001;28:29-35.
52. Nicholls A, Sharp K, Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins. 1991;11:281-296.
53. Boggon TJ, Li Y, Manley PW, Eck MJ. Crystal structure of the Jak3 kinase domain in complex with a staurosporine analog. Blood. 2005;106:996-1002.
54. Mohammadi M, McMahon G, Sun L, et al. Structures of the tyrosine kinase domain of fibroblast growth factor receptor in complex with inhibitors. Science. 1997;276:955-960.
55. Nagar B, Bornmann WG, Pellicena P, et al. Crystal structures of the kinase domain of c-Abl in complex with the small molecule inhibitors PD173955 and imatinib (STI-571). Cancer Res. 2002;62:4236-4243.
56. Habeck M. FDA licences imatinib mesylate for CML. Lancet Oncol. 2002;3:6.
57. Blackledge G, Averbuch S. Gefitinib ("Iressa," ZD1839) and new epidermal growth factor receptor inhibitors. Br J Cancer. 2004;90:566-572.
58. Traxler P, Bold G, Buchdunger E, et al. Tyrosine kinase inhibitors: from rational design to clinical trials. Med Res Rev. 2001;21:499-512.
59. Luo C, Laaja P. Inhibitors of JAKs/STATs and the kinases: a possible new cluster of drugs. Drug Discov Today. 2004;9:268-275.
60. Sudbeck EA, Liu XP, Narla RK, et al. Structure-based design of specific inhibitors of Janus kinase 3 as apoptosis-inducing antileukemic agents. Clin Cancer Res. 1999;5:1569-1582.
61. Changelian PS, Flanagan ME, Ball DJ, et al. Prevention of organ allograft rejection by a specific Janus kinase 3 inhibitor. Science. 2003;302:875-878.
62. Fox T, Coll JT, Xie X, et al. A single amino acid substitution makes ERK2 susceptible to pyridinyl imidazole inhibitors of p38 MAP kinase. Protein Sci. 1998;7:2249-2255.
63. Tong L, Pav S, White DM, et al. A highly specific inhibitor of human p38 MAP kinase binds in the ATP pocket. Nat Struct Biol. 1997;4:311-316.
64. Wang Z, Canagarajah BJ, Boehm JC, et al. Structural basis of inhibitor selectivity in MAP kinases. Structure. 1998;6:1117-1128.
65. Wilson KP, McCaffrey PG, Hsiao K, et al. The structural basis for the specificity of pyridinylimidazole inhibitors of p38 MAP kinase. Chem Biol. 1997;4:423-431.
66. Auffinger P, Hays FA, Westhof E, Ho PS. Halogen bonds in biological molecules. Proc Natl Acad Sci U S A. 2004;101:16789-16794.