Evolutionary divergence in the catalytic activity of the CAM-1, ROR1 and ROR2 kinase domains

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Bainbridge, Travis W ^a   DeAlmeida, Venita I ^a   Izrael Tomasevic, Anita ^a   Chalouni, Cécile ^a   Pan, Borlan ^a   Goldsmith, Joshua ^a   Schoen, Alia P ^a   Quiñones, Gabriel A ^a   Kelly, Ryan ^a   Lill, Jennie R ^a   Sandoval, Wendy ^a   Costa, Mike ^a   Polakis, Paul ^a   Arnott, David ^a   Rubinfeld, Bonnee ^a   Ernst, James A ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; CELL ADHESION MOLECULE 1; MUSK PROTEIN; PROTEIN TYROSINE KINASE; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR 1; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR 2; UNCLASSIFIED DRUG; WNT3A PROTEIN; WNT5A PROTEIN; CAENORHABDITIS ELEGANS PROTEIN; CAM-1 PROTEIN, C ELEGANS; LUCIFERASE; ROR1 PROTEIN, HUMAN; ROR2 PROTEIN, HUMAN;

AMINO ACID SUBSTITUTION; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME STRUCTURE; EVOLUTION; HUMAN; HUMAN CELL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ANIMAL; CAENORHABDITIS ELEGANS; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HEK293 CELL LINE; IMMUNOBLOTTING; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHOSPHORYLATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; SPECIES DIFFERENCE;

AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CATALYSIS; EVOLUTION, MOLECULAR; HEK293 CELLS; HUMANS; IMMUNOBLOTTING; LUCIFERASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; RECEPTOR TYROSINE KINASE-LIKE ORPHAN RECEPTORS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY;

EID: 84904326600     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102695     Document Type: Article

References (52)

1. Masiakowski P, Carroll RD (1992) A novel family of cell surface receptors with tyrosine kinase-like domain. J Biol Chem 267: 26181-26190. (Pubitemid 23014033)
2. Afzal AR, Rajab A, Fenske CD, Oldridge M, Elanko N, et al. (2000) Recessive Robinow syndrome, allelic to dominant brachydactyly type B, is caused by mutation of ROR2. Nat Genet 25: 419-422. (Pubitemid 32983434)
3. Wright TM, Brannon AR, Gordan JD, Mikels AJ, Mitchell C, et al. (2009) Ror2, a developmentally regulated kinase, promotes tumor growth potential in renal cell carcinoma. Oncogene 28: 2513-2523.
4. Enomoto M, Hayakawa S, Itsukushima S, Ren DY, Matsuo M, et al. (2009) Autonomous regulation of osteosarcoma cell invasiveness by Wnt5a/Ror2 signaling. Oncogene 28: 3197-3208.
5. Daneshmanesh AH, Mikaelsson E, Jeddi-Tehrani M, Bayat AA, Ghods R, et al. (2008) Ror1, a cell surface receptor tyrosine kinase is expressed in chronic lymphocytic leukemia and may serve as a putative target for therapy. Int J Cancer 123: 1190-1195.
6. Fukuda T, Chen L, Endo T, Tang L, Lu D, et al. (2008) Antisera induced by infusions of autologous Ad-CD154-leukemia B cells identify ROR1 as an oncofetal antigen and receptor for Wnt5a. Proc Natl Acad Sci U S A 105: 3047-3052. (Pubitemid 351723665)
7. Baskar S, Kwong KY, Hofer T, Levy JM, Kennedy MG, et al. (2008) Unique cell surface expression of receptor tyrosine kinase ROR1 in human B-cell chronic lymphocytic leukemia. Clin Cancer Res 14: 396-404. (Pubitemid 351226106)
8. Shabani M, Asgarian-Omran H, Jeddi-Tehrani M, Vossough P, Faranoush M, et al. (2007) Overexpression of orphan receptor tyrosine kinase Ror1 as a putative tumor-associated antigen in Iranian patients with acute lymphoblastic leukemia. Tumour Biol 28: 318-326. (Pubitemid 351567549)
9. Hudecek M, Schmitt TM, Baskar S, Lupo-Stanghellini MT, Nishida T, et al. (2010) The B-cell tumor-associated antigen ROR1 can be targeted with T cells modified to express a ROR1-specific chimeric antigen receptor. Blood 116: 4532-4541.
10. Nomi M, Oishi I, Kani S, Suzuki H, Matsuda T, et al. (2001) Loss of mRor1 enhances the heart and skeletal abnormalities in mRor2-deficient mice: redundant and pleiotropic functions of mRor1 and mRor2 receptor tyrosine kinases. Mol Cell Biol 21: 8329-8335. (Pubitemid 33108593)
11. Kim N, Stiegler AL, Cameron TO, Hallock PT, Gomez AM, et al. (2008) Lrp4 is a receptor for Agrin and forms a complex with MuSK. Cell 135: 334-342.
12. Henriquez JP, Salinas PC (2012) Dual roles for Wnt signalling during the formation of the vertebrate neuromuscular junction. Acta Physiol (Oxf) 204: 128-136.
13. van Amerongen R, Nusse R (2009) Towards an integrated view of Wnt signaling in development. Development 136: 3205-3214.
14. Angers S, Moon RT (2009) Proximal events in Wnt signal transduction. Nat Rev Mol Cell Biol 10: 468-477.
15. Peifer M, Polakis P (2000) Wnt signaling in oncogenesis and embryogenesis-a look outside the nucleus. Science 287: 1606-1609. (Pubitemid 30127755)
16. Masiakowski P, Yancopoulos GD (1998) The Wnt receptor CRD domain is also found in MuSK and related orphan receptor tyrosine kinases. Curr Biol 8: R407. (Pubitemid 28286265)
17. Xu YK, Nusse R (1998) The Frizzled CRD domain is conserved in diverse proteins including several receptor tyrosine kinases. Curr Biol 8: R405-406. (Pubitemid 28286264)
18. Green JL, Kuntz SG, Sternberg PW (2008) Ror receptor tyrosine kinases: orphans no more. Trends Cell Biol 18: 536-544.
19. Gao B, Song H, Bishop K, Elliot G, Garrett L, et al. (2011) Wnt signaling gradients establish planar cell polarity by inducing Vangl2 phosphorylation through Ror2. Dev Cell 20: 163-176.
20. Tice DA, Soloviev I, Polakis P (2002) Activation of the Wnt pathway interferes with serum response element-driven transcription of immediate early genes. J Biol Chem 277: 6118-6123. (Pubitemid 34968399)
21. Nomachi A, Nishita M, Inaba D, Enomoto M, Hamasaki M, et al. (2008) Receptor tyrosine kinase Ror2 mediates Wnt5a-induced polarized cell migration by activating c-Jun N-terminal kinase via actin-binding protein filamin A. J Biol Chem 283: 27973-27981.
22. Hanks SK, Quinn AM, Hunter T (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241: 42-52.
23. Forrester WC, Dell M, Perens E, Garriga G (1999) A C. elegans Ror receptor tyrosine kinase regulates cell motility and asymmetric cell division. Nature 400: 881-885. (Pubitemid 29406725)
24. Till JH, Becerra M, Watty A, Lu Y, Ma Y, et al. (2002) Crystal structure of the MuSK tyrosine kinase: insights into receptor autoregulation. Structure 10: 1187-1196. (Pubitemid 35254007)
25. Munshi S, Hall DL, Kornienko M, Darke PL, Kuo LC (2003) Structure of apo, unactivated insulin-like growth factor-1 receptor kinase at 1.5 A resolution. Acta Crystallogr D Biol Crystallogr 59: 1725-1730. (Pubitemid 37245124)
26. Favelyukis S, Till JH, Hubbard SR, Miller WT (2001) Structure and autoregulation of the insulin-like growth factor 1 receptor kinase. Nat Struct Biol 8: 1058-1063. (Pubitemid 33101627)
27. Gentile A, Lazzari L, Benvenuti S, Trusolino L, Comoglio PM (2011) Ror1 is a pseudokinase that is crucial for Met-driven tumorigenesis. Cancer Res 71: 3132-3141.
28. Akbarzadeh S, Wheldon LM, Sweet SM, Talma S, Mardakheh FK, et al. (2008) The deleted in brachydactyly B domain of ROR2 is required for receptor activation by recruitment of Src. PLoS One 3: e1873.
29. Mikels A, Minami Y, Nusse R (2009) Ror2 receptor requires tyrosine kinase activity to mediate Wnt5A signaling. J Biol Chem 284: 30167-30176.
30. Liu Y, Rubin B, Bodine PV, Billiard J (2008) Wnt5a induces homodimerization and activation of Ror2 receptor tyrosine kinase. J Cell Biochem 105: 497-502.
31. Willert K, Brown JD, Danenberg E, Duncan AW, Weissman IL, et al. (2003) Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423: 448-452. (Pubitemid 36626997)
32. Casnellie JE (1991) Assay of protein kinases using peptides with basic residues for phosphocellulose binding. Methods Enzymol 200: 115-120.
33. Vendel AC, Calemine-Fenaux J, Izrael-Tomasevic A, Chauhan V, Arnott D, et al. (2009) B and T lymphocyte attenuator regulates B cell receptor signaling by targeting Syk and BLNK. J Immunol 182: 1509-1517.
34. Castellana NE, McCutcheon K, Pham VC, Harden K, Nguyen A, et al. (2011) Resurrection of a clinical antibody: template proteogenomic de novo proteomic sequencing and reverse engineering of an anti-lymphotoxin-alpha antibody. Proteomics 11: 395-405.
35. DeAlmeida VI, Miao L, Ernst JA, Koeppen H, Polakis P, et al. (2007) The soluble wnt receptor Frizzled8CRD-hFc inhibits the growth of teratocarcinomas in vivo. Cancer Res 67: 5371-5379. (Pubitemid 46997277)
36. White MF, Haring HU, Kasuga M, Kahn CR (1984) Kinetic properties and sites of autophosphorylation of the partially purified insulin receptor from hepatoma cells. J Biol Chem 259: 255-264. (Pubitemid 14177650)
37. Zhang XH, Guo XN, Zhong L, Luo XM, Jiang HL, et al. (2007) Establishment of the active catalytic domain of human PDGFRbeta tyrosine kinase-based ELISA assay for inhibitor screening. Biochim Biophys Acta 1770: 1490-1497. (Pubitemid 47386023)
38. Mikels AJ, Nusse R (2006) Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol 4: e115.
39. Grumolato L, Liu G, Mong P, Mudbhary R, Biswas R, et al. (2010) Canonical and noncanonical Wnts use a common mechanism to activate completely unrelated coreceptors. Genes Dev 24: 2517-2530.
40. Nishita M, Itsukushima S, Nomachi A, Endo M, Wang Z, et al. (2010) Ror2/Frizzled complex mediates Wnt5a-induced AP-1 activation by regulating Dishevelled polymerization. Mol Cell Biol 30: 3610-3619.
41. Ho HY, Susman MW, Bikoff JB, Ryu YK, Jonas AM, et al. (2012) Wnt5a-Ror-Dishevelled signaling constitutes a core developmental pathway that controls tissue morphogenesis. Proc Natl Acad Sci U S A 109: 4044-4051.
42. Kim C, Forrester WC (2003) Functional analysis of the domains of the C elegans Ror receptor tyrosine kinase CAM-1. Dev Biol 264: 376-390. (Pubitemid 37490976)
43. Nishita M, Yoo SK, Nomachi A, Kani S, Sougawa N, et al. (2006) Filopodia formation mediated by receptor tyrosine kinase Ror2 is required for Wnt5a-induced cell migration. J Cell Biol 175: 555-562. (Pubitemid 44790609)
44. Murphy JM, Zhang Q, Young SN, Reese ML, Bailey FP, et al. (2014) A robust methodology to subclassify pseudokinases based on their nucleotide-binding properties. Biochem J 457: 323-334.
45. Hubbard SR, Mohammadi M, Schlessinger J (1998) Autoregulatory mechanisms in protein-tyrosine kinases. J Biol Chem 273: 11987-11990. (Pubitemid 28240552)
46. Fukuda K, Gupta S, Chen K, Wu C, Qin J (2009) The pseudoactive site of ILK is essential for its binding to alpha-Parvin and localization to focal adhesions. Mol Cell 36: 819-830.
47. Scheeff ED, Eswaran J, Bunkoczi G, Knapp S, Manning G (2009) Structure of the pseudokinase VRK3 reveals a degraded catalytic site, a highly conserved kinase fold, and a putative regulatory binding site. Structure 17: 128-138.
48. Labesse G, Gelin M, Bessin Y, Lebrun M, Papoin J, et al. (2009) ROP2 from Toxoplasma gondii: a virulence factor with a protein-kinase fold and no enzymatic activity. Structure 17: 139-146.
49. Qiu W, Wernimont A, Tang K, Taylor S, Lunin V, et al. (2009) Novel structural and regulatory features of rhoptry secretory kinases in Toxoplasma gondii. EMBO J 28: 969-979.
50. Shi F, Telesco SE, Liu Y, Radhakrishnan R, Lemmon MA (2010) ErbB3/HER3 intracellular domain is competent to bind ATP and catalyze autophosphorylation. Proc Natl Acad Sci U S A 107: 7692-7697.
51. Boudeau J, Scott JW, Resta N, Deak M, Kieloch A, et al. (2004) Analysis of the LKB1-STRAD-MO25 complex. J Cell Sci 117: 6365-6375. (Pubitemid 40214563)
52. Rajakulendran T, Sicheri F (2010) Allosteric protein kinase regulation by pseudokinases: insights from STRAD. Sci Signal 3: pe8.