Protein tyrosine phosphatase SHP2/PTPN11 mistargeting as a consequence of SH2-domain point mutations associated with Noonan Syndrome and leukemia

Journal of Proteomics

Volumn 84, Issue , 2013, Pages 132-147

  Müller, Pia J ^a   Rigbolt, Kristoffer T G ^b   Paterok, Dirk ^c   Piehler, Jacob ^c   Vanselow, Jens ^d   Lasonder, Edwin ^e   Andersen, Jens S ^d   Schaper, Fred ^a,f   Sobota, Radoslaw M ^a,d,g  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY OF OSNABRÜCK   (Germany)

^d UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^e RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^f OTTO VON GUERICKE UNIVERSITY   (Germany)

^g AGENCY FOR SCIENCE   (Singapore)

Author keywords

JMML; Mass spectrometry; Noonan Syndrome; PTPN11; SHP2; SILAC

Indexed keywords

MUTANT PROTEIN; PROTEIN SH2; PROTEIN TYROSINE PHOSPHATASE SHP 2;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; LEUKEMIA; MASS SPECTROMETRY; MOLECULAR DYNAMICS; NOONAN SYNDROME; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION;

AMINO ACID SUBSTITUTION; HELA CELLS; HUMANS; LEUKEMIA; MUTATION, MISSENSE; NEOPLASM PROTEINS; NOONAN SYNDROME; PROTEIN BINDING; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11; SRC HOMOLOGY DOMAINS;

EID: 84877102677     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.04.005     Document Type: Article

References (61)

1. Lehmann U., Schmitz J., Weissenbach M., Sobota R.M., Hortner M., Friederichs K., et al. SHP2 and SOCS3 contribute to Tyr-759-dependent attenuation of interleukin-6 signaling through gp130. J Biol Chem 2003, 278:661-671.
2. Anhuf D., Weissenbach M., Schmitz J., Sobota R., Hermanns H.M., Radtke S., et al. Signal transduction of IL-6, leukemia-inhibitory factor, and oncostatin M: Structural receptor requirements for signal attenuation. J Immunol 2000, 165:2535-2543.
3. Case R.D., Piccione E., Wolf G., Benett A.M., Lechleider R.J., Neel B.G., et al. SH-PTP2/Syp SH2 domain binding specificity is defined by direct interactions with platelet-derived growth factor beta-receptor, epidermal growth factor receptor, and insulin receptor substrate-1-derived phosphopeptides. J Biol Chem 1994, 269:10467-10474.
4. Tonks N.K. Protein tyrosine phosphatases: From genes, to function, to disease. Nat Rev Mol Cell Biol 2006, 7:833-846.
5. Neel B.G., Gu H., Pao L. The 'Shp'ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends Biochem Sci 2003, 28:284-293.
6. Sugimoto S., Lechleider R.J., Shoelson S.E., Neel B.G., Walsh C.T. Expression, purification, and characterization of SH2-containing protein tyrosine phosphatase, SH-PTP2. J Biol Chem 1993, 268:22771-22776.
7. Plutzky J., Neel B.G., Rosenberg R.D. Isolation of a src homology 2-containing tyrosine phosphatase. Proc Natl Acad Sci U S A 1992, 89:1123-1127.
8. Lu W., Shen K., Cole P.A. Chemical dissection of the effects of tyrosine phosphorylation of SHP-2. Biochemistry 2003, 42:5461-5468.
9. Lu W., Gong D., Bar-Sagi D., Cole P.A. Site-specific incorporation of a phosphotyrosine mimetic reveals a role for tyrosine phosphorylation of SHP-2 in cell signaling. Mol Cell 2001, 8:759-769.
10. Nakajima K., Yamanaka Y., Nakae K., Kojima H., Ichiba M., Kiuchi N., et al. A central role for Stat3 in IL-6-induced regulation of growth and differentiation in M1 leukemia cells. EMBO J 1996, 15:3651-3658.
11. Schiemann W.P., Bartoe J.L., Nathanson N.M. Box3-independent signaling mechanisms are involved in leukemia inhibitory factor receptor alpha- and gp130-mediated stimulation of mitogen-activated protein kinase. Evidence for participation of multiple signaling pathways which converge at Ras. J Biol Chem 1997, 272:16631-16636.
12. Chan R.J., Feng G.S. PTPN11 is the first identified proto-oncogene that encodes a tyrosine phosphatase. Blood 2007, 109:862-867.
13. Bentires-Alj M., Paez J.G., David F.S., Keilhack H., Halmos B., Naoki K., et al. Activating mutations of the Noonan syndrome-associated SHP2/PTPN11 gene in human solid tumors and adult acute myelogenous leukemia. Cancer Res 2004, 64:8816-8820.
14. Fragale A., Tartaglia M., Wu J., Gelb B.D. Noonan syndrome-associated SHP2/PTPN11 mutants cause EGF-dependent prolonged GAB1 binding and sustained ERK2/MAPK1 activation. Hum Mutat 2004, 23:267-277.
15. Kontaridis M.I., Swanson K.D., David F.S., Barford D., Neel B.G. PTPN11 (Shp2) mutations in LEOPARD syndrome have dominant negative, not activating, effects. J Biol Chem 2006, 281:6785-6792.
16. Tartaglia M., Kalidas K., Shaw A., Song X., Musat D.L., van der Burgt I., et al. PTPN11 mutations in Noonan syndrome: Molecular spectrum, genotype-phenotype correlation, and phenotypic heterogeneity. Am J Hum Genet 2002, 70:1555-1563.
17. Martinelli S., Torreri P., Tinti M., Stella L., Bocchinfuso G., Flex E., et al. Diverse driving forces underlie the invariant occurrence of the T42A, E139D, I282V and T468M SHP2 amino acid substitutions causing Noonan and LEOPARD syndromes. Hum Mol Genet 2008, 17:2018-2029.
18. Tartaglia M., Niemeyer C.M., Fragale A., Song X., Buechner J., Jung A., et al. Somatic mutations in PTPN11 in juvenile myelomonocytic leukemia, myelodysplastic syndromes and acute myeloid leukemia. Nat Genet 2003, 34:148-150.
19. Huyer G., Ramachandran C. The specificity of the N-terminal SH2 domain of SHP-2 is modified by a single point mutation. Biochemistry 1998, 37:2741-2747.
20. Tartaglia M., Gelb B.D. Germ-line and somatic PTPN11 mutations in human disease. Eur J Med Genet 2005, 48:81-96.
21. Sweeney M.C., Wavreille A.S., Park J., Butchar J.P., Tridandapani S., Pei D. Decoding protein-protein interactions through combinatorial chemistry: Sequence specificity of SHP-1, SHP-2, and SHIP SH2 domains. Biochemistry 2005, 44:14932-14947.
22. Imhof D., Wavreille A.S., May A., Zacharias M., Tridandapani S., Pei D. Sequence specificity of SHP-1 and SHP-2 Src homology 2 domains. Critical roles of residues beyond the pY+3 position. J Biol Chem 2006, 281:20271-20282.
23. Ong S.E., Blagoev B., Kratchmarova I., Kristensen D.B., Steen H., Pandey A., et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 2002, 1:376-386.
24. Wisniewski J.R., Zougman A., Nagaraj N., Mann M. Universal sample preparation method for proteome analysis. Nat Methods 2009, 6:359-362.
25. Hubner N.C., Ren S., Mann M. Peptide separation with immobilized pI strips is an attractive alternative to in-gel protein digestion for proteome analysis. Proteomics 2008, 8:4862-4872.
26. Rappsilber J., Ishihama Y., Mann M. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal Chem 2003, 75:663-670.
27. Cox J., Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 2008, 26:1367-1372.
28. Cox J., Matic I., Hilger M., Nagaraj N., Selbach M., Olsen J.V., et al. A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat Protoc 2009, 4:698-705.
29. Keilhack H., David F.S., McGregor M., Cantley L.C., Neel B.G. Diverse biochemical properties of Shp2 mutants. Implications for disease phenotypes. J Biol Chem 2005, 280:30984-30993.
30. Olsen J.V., Blagoev B., Gnad F., Macek B., Kumar C., Mortensen P., et al. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006, 127:635-648.
31. Clahsen T., Lehmann U., Stross C., Hermanns H.M., Volkmer-Engert R., Schneider-Mergener J., et al. The tyrosine 974 within the LIF-R-chain of the gp130/LIF-R heteromeric receptor complex mediates negative regulation of LIF signalling. Cell Signal 2005, 17:559-569.
32. Li L., Wu C., Huang H., Zhang K., Gan J., Li S.S. Prediction of phosphotyrosine signaling networks using a scoring matrix-assisted ligand identification approach. Nucleic Acids Res 2008, 36:3263-3273.
33. Maegawa H., Hasegawa M., Sugai S., Obata T., Ugi S., Morino K., et al. Expression of a dominant negative SHP-2 in transgenic mice induces insulin resistance. J Biol Chem 1999, 274:30236-30243.
34. Gunaje J.J., Bhat G.J. Involvement of tyrosine phosphatase PTP1D in the inhibition of interleukin-6-induced Stat3 signaling by alpha-thrombin. Biochem Biophys Res Commun 2001, 288:252-257.
35. Scholzen T., Gerdes J. The Ki-67 protein: From the known and the unknown. J Cell Physiol 2000, 182:311-322.
36. Kim J.W., Cho H.S., Kim J.H., Hur S.Y., Kim T.E., Lee J.M., et al. AAC-11 overexpression induces invasion and protects cervical cancer cells from apoptosis. Lab Invest 2000, 80:587-594.
37. Wang Z., Liu H., Liu B., Ma W., Xue X., Chen J., et al. Gene expression levels of CSNK1A1 and AAC-11, but not NME1, in tumor tissues as prognostic factors in NSCLC patients. Med Sci Monit 2010, 16:CR357-CR364.
38. Sasaki H., Moriyama S., Yukiue H., Kobayashi Y., Nakashima Y., Kaji M., et al. Expression of the antiapoptosis gene, AAC-11, as a prognosis marker in non-small cell lung cancer. Lung Cancer 2001, 34:53-57.
39. Korshunov V.A. Axl-dependent signalling: A clinical update. Clin Sci (Lond) 2012, 122:361-368.
40. Bennett A.M., Tang T.L., Sugimoto S., Walsh C.T., Neel B.G. Protein-tyrosine-phosphatase SHPTP2 couples platelet-derived growth factor receptor beta to Ras. Proc Natl Acad Sci U S A 1994, 91:7335-7339.
41. Berchtold S., Volarevic S., Moriggl R., Mercep M., Groner B. Dominant negative variants of the SHP-2 tyrosine phosphatase inhibit prolactin activation of Jak2 (janus kinase 2) and induction of Stat5 (signal transducer and activator of transcription 5)-dependent transcription. Mol Endocrinol 1998, 12:556-567.
42. Reeves S.A., Sinha B., Baur I., Reinhold D., Harsh G. An alternative role for the src-homology-domain-containing phosphotyrosine phosphatase (SH-PTP2) in regulating epidermal-growth-factor-dependent cell growth. Eur J Biochem 1995, 233:55-61.
43. Symes A., Stahl N., Reeves S.A., Farruggella T., Servidei T., Gearan T., et al. The protein tyrosine phosphatase SHP-2 negatively regulates ciliary neurotrophic factor induction of gene expression. Curr Biol 1997, 7:697-700.
44. Hausdorff S.F., Bennett A.M., Neel B.G., Birnbaum M.J. Different signaling roles of SHPTP2 in insulin-induced GLUT1 expression and GLUT4 translocation. J Biol Chem 1995, 270:12965-12968.
45. Eck M.J., Pluskey S., Trub T., Harrison S.C., Shoelson S.E. Spatial constraints on the recognition of phosphoproteins by the tandem SH2 domains of the phosphatase SH-PTP2. Nature 1996, 379:277-280.
46. Blagoev B., Kratchmarova I., Ong S.E., Nielsen M., Foster L.J., Mann M. A proteomics strategy to elucidate functional protein-protein interactions applied to EGF signaling. Nat Biotechnol 2003, 21:315-318.
47. Rotin D., Margolis B., Mohammadi M., Daly R.J., Daum G., Li N., et al. SH2 domains prevent tyrosine dephosphorylation of the EGF receptor: Identification of Tyr992 as the high-affinity binding site for SH2 domains of phospholipase C gamma. EMBO J 1992, 11:559-567.
48. Pandey A., Podtelejnikov A.V., Blagoev B., Bustelo X.R., Mann M., Lodish H.F. Analysis of receptor signaling pathways by mass spectrometry: Identification of vav-2 as a substrate of the epidermal and platelet-derived growth factor receptors. Proc Natl Acad Sci U S A 2000, 97:179-184.
49. Rodriguez M., Li S.S., Harper J.W., Songyang Z. An oriented peptide array library (OPAL) strategy to study protein-protein interactions. J Biol Chem 2004, 279:8802-8807.
50. Songyang Z., Shoelson S.E., Chaudhuri M., Gish G., Pawson T., Haser W.G., et al. SH2 domains recognize specific phosphopeptide sequences. Cell 1993, 72:767-778.
51. Cochrane D., Webster C., Masih G., McCafferty J. Identification of natural ligands for SH2 domains from a phage display cDNA library. J Mol Biol 2000, 297:89-97.
52. Machida K., Thompson C.M., Dierck K., Jablonowski K., Karkkainen S., Liu B., et al. High-throughput phosphotyrosine profiling using SH2 domains. Mol Cell 2007, 26:899-915.
53. Tartaglia M., Mehler E.L., Goldberg R., Zampino G., Brunner H.G., Kremer H., et al. Mutations in PTPN11, encoding the protein tyrosine phosphatase SHP-2, cause Noonan syndrome. Nat Genet 2001, 29:465-468.
54. Zenker M., Buheitel G., Rauch R., Koenig R., Bosse K., Kress W., et al. Genotype-phenotype correlations in Noonan syndrome. J Pediatr 2004, 144:368-374.
55. Liu B.A., Engelmann B.W., Jablonowski K., Higginbotham K., Stergachis A.B., Nash P.D. SRC homology 2 domain binding sites in insulin, IGF-1 and FGF receptor mediated signaling networks reveal an extensive potential interactome. Cell Commun Signal 2012, 10:27.
56. Huang H., Li L., Wu C., Schibli D., Colwill K., Ma S., et al. Defining the specificity space of the human SRC homology 2 domain. Mol Cell Proteomics 2008, 7:768-784.
57. Chughtai N., Schimchowitsch S., Lebrun J.J., Ali S. Prolactin induces SHP-2 association with Stat5, nuclear translocation, and binding to the beta-casein gene promoter in mammary cells. J Biol Chem 2002, 277:31107-31114.
58. Zhang W., Chan R.J., Chen H., Yang Z., He Y., Zhang X., et al. Negative regulation of Stat3 by activating PTPN11 mutants contributes to the pathogenesis of Noonan syndrome and juvenile myelomonocytic leukemia. J Biol Chem 2009, 284:22353-22363.
59. Jongmans M., Sistermans E.A., Rikken A., Nillesen W.M., Tamminga R., Patton M., et al. Genotypic and phenotypic characterization of Noonan syndrome: New data and review of the literature. Am J Med Genet A 2005, 134A:165-170.
60. Martinelli S., Nardozza A.P., Delle Vigne S., Sabetta G., Torreri P., Bocchinfuso G., et al. Counteracting effects operating on Src homology 2 domain-containing protein-tyrosine phosphatase 2 (SHP2) function drive selection of the recurrent Y62D and Y63C substitutions in Noonan syndrome. J Biol Chem 2012, 287:27066-27077.
61. Hof P., Pluskey S., Dhe-Paganon S., Eck M.J., Shoelson S.E. Crystal structure of the tyrosine phosphatase SHP-2. Cell 1998, 92:441-450.