Analysis of jak2 catalytic function by peptide microarrays: The role of the JH2 domain and V617F mutation

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Sanz, Arturo ^a   Ungureanu, Daniela ^b   Pekkala, Tuija ^b   Ruijtenbeek, Rob ^c   Touw, Ivo P ^a   Hilhorst, Riet ^c   Silvennoinen, Olli ^b,d  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^c PamGene International BV   (Netherlands)

^d TAMPERE UNIVERSITY HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; JANUS KINASE 2; PEPTIDE; PHENYLALANINE; PHOSPHOTRANSFERASE; PSEUDOKINASE; RECOMBINANT ENZYME; RECOMBINANT JANUS KINASE 2; UNCLASSIFIED DRUG; VALINE;

ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SPECIFICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PEPTIDE MICROARRAY; PROTEIN DOMAIN; PROTEIN MICROARRAY; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; AMINO ACID SEQUENCE; ANIMAL; ARMYWORM; BIOCATALYSIS; CELL LINE; CHEMISTRY; KINETICS; METABOLISM; MISSENSE MUTATION; MOLECULAR GENETICS; PHOSPHORYLATION; POINT MUTATION;

AMINO ACID SEQUENCE; ANIMALS; BIOCATALYSIS; CELL LINE; JANUS KINASE 2; KINETICS; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PEPTIDES; PHOSPHORYLATION; POINT MUTATION; PROTEIN ARRAY ANALYSIS; SPODOPTERA; SUBSTRATE SPECIFICITY;

EID: 79955136973     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018522     Document Type: Article

References (56)

1. Haan C, Kreis S, Margue C, Behrmann I, (2006) Jaks and cytokine receptors- An intimate relationship. Biochem Pharmacol 72: 1538-1546.
2. Schindler C, Plumlee C, (2008) Inteferons pen the JAK-STAT pathway. Semin Cell Dev Biol 19: 311-318.
3. Boudeau J, Miranda-Saavedra D, Barton GJ, Alessi DR, (2006) Emerging roles of pseudokinases. Trends Cell Biol 16: 443-452.
4. Saharinen P, Silvennoinen O, (2002) 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 277: 47954-47963.
5. Saharinen P, Takaluoma K, Silvennoinen O, (2000) Regulation of the Jak2 Tyrosine Kinase by Its Pseudokinase Domain. Mol Cell Biol 20: 3387-3395.
6. Baxter EJ, Scott LM, Campbell PJ, East C, Fourouclas N, et al. (2005) Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders. The Lancet 365: 1054-1061.
7. Kralovics R, Passamonti F, Buser AS, Teo S-S, Tiedt R, et al. (2005) A Gain-of-Function Mutation of JAK2 in Myeloproliferative Disorders. N Engl J Med 352: 1779-1790.
8. Levine RL, Wadleigh M, Cools J, Ebert BL, Wernig G, et al. (2005) Activating mutation in the tyrosine kinase JAK2 in polycythemia vera, essential thrombocythemia, and myeloid metaplasia with myelofibrosis. Cancer Cell 7: 387-397.
9. James C, Ugo V, Le Couedic J-P, Staerk J, Delhommeau F, et al. (2005) A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature 434: 1144-1148.
10. Lacout C, Pisani DF, Tulliez M, Gachelin FM, Vainchenker W, et al. (2006) JAK2V617F expression in murine hematopoietic cells leads to MPD mimicking human PV with secondary myelofibrosis. Blood 108: 1652-1660.
11. Wernig G, Mercher T, Okabe R, Levine RL, Lee BH, et al. (2006) Expression of Jak2V617F causes a polycythemia vera-like disease with associated myelofibrosis in a murine bone marrow transplant model. Blood 107: 4274-4281.
12. Zaleskas VM, Krause DS, Lazarides K, Patel N, Hu Y, et al. (2006) Molecular pathogenesis and therapy of polycythemia induced in mice by JAK2 V617F. PLoS One 1.
13. Haan CBI, Haan S, (2010) Perspectives for the use of structural information and chemical genetics to develop inhibitors of Janus kinases. J Cell Mol Med 14: 504-527.
14. Vainchenker W, Dusa A, Constantinescu SN, (2008) JAKs in pathology: Role of Janus kinases in hematopoietic malignancies and immunodeficiencies. Semin Cell Dev Biol 19: 385-393.
15. Saharinen P, Vihinen M, Silvennoinen O, (2003) Autoinhibition of Jak2 Tyrosine Kinase Is Dependent on Specific Regions in Its Pseudokinase Domain. Mol Cell Biol 14: 1448-1459.
16. Songyang Z, Carraway KL, Eck MJ, Harrison SC, Feldman RA, et al. (1995) Catalytic specificity of protein-tyrosine kinases is critical for selective signalling. Nature 373: 536-539.
17. Knebel A, Morrice N, Cohen P, (2001) A novel method to identify protein kinase substrates: eEF2 kinase is phosphorylated and inhibited by SAPK4/p38[delta]. EMBO J 20: 4360-4369.
18. Songyang Z, Blechner S, Hoagland N, Hoekstra MF, Piwnica-Worms H, et al. (1994) Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr Biol 4: 973-982.
19. Songyang Z, Gish G, Mbamalu G, Pawson T, Cantley LC, (1995) A Single Point Mutation Switches the Specificity of Group III Src Homology (SH) 2 Domains to That of Group I SH2 Domains. J Biol Chem 270: 26029-26032.
20. Vivanco I, Rohle D, Versele M, Iwanami A, Kuga D, et al. (2010) The phosphatase and tensin homolog regulates epidermal growth factor receptor (EGFR) inhibitor response by targeting EGFR for degradation. Proc Natl Acad Sci U S A 107: 6459-6464.
21. Lemeer S, Ruijtenbeek R, Pinkse MWH, Jopling C, Heck AJR, et al. (2007) Endogenous Phosphotyrosine Signaling in Zebrafish Embryos. Mol Cell Proteomics 6: 2088-2099.
22. Jinnin M, Medici D, Park L, Limaye N, Liu Y, et al. (2008) Suppressed NFAT-dependent VEGFR1 expression and constitutive VEGFR2 signaling in infantile hemangioma. Nat Med 14: 1236-1246.
23. De Keersmaecker K, Versele M, Cools J, Superti-Furga G, Hantschel O, (2008) Intrinsic differences between the catalytic properties of the oncogenic NUP214-ABL1 and BCR-ABL1 fusion protein kinases. Leukemia 22: 2208-2216.
24. Hilhorst R, Houkes L, van den Berg A, Ruijtenbeek R, (2009) Peptide microarrays for detailed, high-throughput substrate identification, kinetic characterization, and inhibition studies on protein kinase A. Anal Biochem 387: 150-161.
25. Poot AJ, van Ameijde J, Slijper M, van den Berg A, Hilhorst R, et al. (2009) Development of Selective Bisubstrate-Based Inhibitors Against Protein Kinase C (PKC) Isozymes By Using Dynamic Peptide Microarrays. ChemBioChem 10: 2042-2051.
26. Feng J, Witthuhn BA, Matsuda T, Kohlhuber F, Kerr IM, et al. (1997) Activation of Jak2 catalytic activity requires phosphorylation of Y1007 in the kinase activation loop. Mol Cell Biol 17: 2497-2501.
27. Rodriguez M, Li SSC, Harper JW, Songyang Z, (2004) An Oriented Peptide Array Library (OPAL) Strategy to Study Protein-Protein Interactions. J Biol Chem 279: 8802-8807.
28. Hall T, Emmons TL, Chrencik JE, Gormley JA, Weinberg RA, et al. (2010) Expression, purification, characterization and crystallization of non- and phosphorylated states of JAK2 and JAK3 kinase domain. Protein Expr Purif 69: 54-63.
29. Copeland RA, (2000) Enzymes: A Practical Introduction to Structure, Mechanism, and Data Analysis: Wiley-VCH, Inc.
30. Ubersax JA, Ferrell JE Jr, (2007) Mechanisms of specificity in protein phosphorylation. Nat Rev Mol Cell Biol 8: 530-541.
31. Boggon TJ, Li Y, Manley PW, Eck MJ, (2005) Crystal structure of the Jak3 kinase domain in complex with a staurosporine analog. Blood 106: 996-1002.
32. Lucet IS, Fantino E, Styles M, Bamert R, Patel O, et al. (2006) The structural basis of Janus kinase 2 inhibition by a potent and specific pan-Janus kinase inhibitor. Blood 107: 176-183.
33. Workman CT, Yin Y, Corcoran DL, Ideker T, Stormo GD, et al. (2005) enoLOGOS: a versatile web tool for energy normalized sequence logos. Nucleic Acids Res 33: W389-392.
34. Songyang Z, (1999) Recognition and regulation of primary-sequence motifs by signaling modular domains. Progress in Biophysics and Molecular Biology 71: 359-372.
35. Matsuda T, Feng J, Witthuhn BA, Sekine Y, Ihle JN, (2004) Determination of the transphosphorylation sites of Jak2 kinase. Biochem Biophys Res Commun 325: 586-594.
36. Argetsinger LS, Kouadio J-LK, Steen H, Stensballe A, Jensen ON, et al. (2004) Autophosphorylation of JAK2 on Tyrosines 221 and 570 Regulates Its Activity. Mol Cell Biol 24: 4955-4967.
37. Kurzer JH, Argetsinger LS, Zhou Y-J, Kouadio J-LK, O'Shea JJ, et al. (2004) Tyrosine 813 Is a Site of JAK2 Autophosphorylation Critical for Activation of JAK2 by SH2-B{beta}. Mol Cell Biol 24: 4557-4570.
38. Peter VH, Indy C, Jon MK, Elzbieta S, Bin Z, (2004) PhosphoSite: A bioinformatics resource dedicated to physiological protein phosphorylation. Proteomics 4: 1551-1561.
39. Haan C, Behrmann I, Haan S, (2010) Perspectives for the use of structural information and chemical genetics to develop inhibitors of Janus kinases. J Cell Mol Med 14: 504-527.
40. Kundrapu K, Colenberg L, Duhé RJ, (2008) Activation Loop Tyrosines Allow the JAK2(V617F) Mutant to Attain Hyperactivation Cell Biochem Biophys 2: 103-112.
41. Giordanetto F, Kroemer RT, (2002) Prediction of the structure of human Janus kinase 2 (JAK2) comprising JAK homology domains 1 through 7. Protein Eng 15: 727-737.
42. Lindauer K, Loerting T, Liedl KR, Kroemer RT, (2001) Prediction of the structure of human Janus kinase 2 (JAK2) comprising the two carboxy-terminal domains reveals a mechanism for autoregulation. Protein Eng 14: 27-37.
43. Lee T-S, Ma W, Zhang X, Kantarjian H, Albitar M, (2009) Structural effects of clinically observed mutations in JAK2 exons 13-15: comparison with V617F and exon 12 mutations. BMC Struct Biol 9: 58.
44. Lee TS, Ma W, Zhang X, Giles F, Kantarjian H, et al. (2009) Mechanisms of constitutive activation of Janus kinase 2-V617F revealed at the atomic level through molecular dynamics simulations. Cancer 115: 1692-1700.
45. Huse M, Kuriyan J, (2002) The Conformational Plasticity of Protein Kinases. Cell 109: 275-282.
46. Krupa A, Preethi G, Srinivasan N, (2004) Structural Modes of Stabilization of Permissive Phosphorylation Sites in Protein Kinases: Distinct Strategies in Ser/Thr and Tyr Kinases. Journal of Molecular Biology 339: 1025-1039.
47. Zeqiraj E, Filippi BM, Goldie S, Navratilova I, Boudeau Jrm, et al. (2009) ATP and MO25á Regulate the Conformational State of the STRADá Pseudokinase and Activation of the LKB1 Tumour Suppressor. PLoS Biol 7: e1000126.
48. Mukherjee K, Sharma M, Urlaub H, Bourenkov GP, Jahn R, et al. (2008) CASK Functions as a Mg2+-Independent Neurexin Kinase. Cell 133: 328-339.
49. Xu B-e, English JM, Wilsbacher JL, Stippec S, Goldsmith EJ, et al. (2000) WNK1, a Novel Mammalian Serine/Threonine Protein Kinase Lacking the Catalytic Lysine in Subdomain II. J Biol Chem 275: 16795-16801.
50. Kawagoe T, Sato S, Matsushita K, Kato H, Matsui K, et al. (2008) Sequential control of Toll-like receptor-dependent responses by IRAK1 and IRAK2. Nat Immunol 9: 684-691.
51. Huang LJ-s, Constantinescu SN, Lodish HF, (2001) The N-Terminal Domain of Janus Kinase 2 Is Required for Golgi Processing and Cell Surface Expression of Erythropoietin Receptor. Molecular Cell 8: 1327-1338.
52. Tong W, Sulahian R, Gross AW, Hendon N, Lodish HF, et al. (2006) The Membrane-proximal Region of the Thrombopoietin Receptor Confers Its High Surface Expression by JAK2-dependent and-independent Mechanisms. J Biol Chem 281: 38930-38940.
53. Funakoshi-Tago M, Pelletier S, Matsuda T, Parganas E, Ihle JN, (2006) Receptor specific downregulation of cytokine signaling by autophosphorylation in the FERM domain of Jak2. EMBO J 25: 4763-4772.
54. Ishida-Takahashi R, Rosario F, Gong Y, Kopp K, Stancheva Z, et al. (2006) Phosphorylation of Jak2 on Ser523 Inhibits Jak2-Dependent Leptin Receptor Signaling. Mol Cell Biol 26: 4063-4073.
55. Mazurkiewicz-Munoz AM, Argetsinger LS, Kouadio J-LK, Stensballe A, Jensen ON, et al. (2006) Phosphorylation of JAK2 at Serine 523: a Negative Regulator of JAK2 That Is Stimulated by Growth Hormone and Epidermal Growth Factor. Mol Cell Biol 26: 4052-4062.
56. Funakoshi-Tago M, Pelletier S, Moritake H, Parganas E, Ihle JN, (2008) Jak2 FERM Domain Interaction with the Erythropoietin Receptor Regulates Jak2 Kinase Activity. Molecular and Cellular Biology 28: 1792-1801.