Targeting protein tyrosine phosphatase SHP2 for the treatment of PTPN11-associated malignancies

Molecular Cancer Therapeutics

Volumn 12, Issue 9, 2013, Pages 1738-1748

  Yu, Bing ^a,b   Liu, Wei ^a,b,c   Yu, Wen Mei ^a   Loh, Mignon L ^d   Alter, Shawn ^a   Guvench, Olgun ^e   MacKerell Jr , Alexander D ^f   Tang, Li Da ^b   Qu, Cheng Kui ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TIANJIN INSTITUTE OF PHARMACEUTICAL RESEARCH   (China)

^c TIANJIN MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF NEW ENGLAND   (United States)

^f UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; PROTEIN TYROSINE PHOSPHATASE SHP 2; PROTEIN TYROSINE PHOSPHATASE SHP 2 INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; DRUG DESIGN; DRUG EFFECT; DRUG EFFICACY; DRUG PROTEIN BINDING; DRUG TARGETING; ENZYME ACTIVE SITE; FLUORESCENCE ANALYSIS; GENE; GENE MUTATION; HUMAN; HUMAN CELL; IC 50; LEUKEMIA; LEUKEMIA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PTPN11 GENE; SIGNAL TRANSDUCTION;

ANIMALS; CATALYTIC DOMAIN; CELL LINE; CELL PROLIFERATION; CHILD; DRUG DESIGN; DRUG EVALUATION, PRECLINICAL; DRUG SCREENING ASSAYS, ANTITUMOR; ENZYME INHIBITORS; GENE KNOCKOUT TECHNIQUES; HUMANS; INDOLES; LEUKEMIA, MYELOID; MICE; MOLECULAR STRUCTURE; MUTATION; NOONAN SYNDROME; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11; SIGNAL TRANSDUCTION; TRIAZINES; TUMOR CELLS, CULTURED;

EID: 84884526416     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-13-0049-T     Document Type: Article

References (52)

1. Xu D,QuCK. Protein tyrosine phosphatases in the JAK/STATpathway. Front Biosci 2008;13:4925-32.
2. Chan G, Kalaitzidis D, Neel BG. The tyrosine phosphatase Shp2 (PTPN11) in cancer. Cancer Metastasis Rev 2008;27:179-92.
3. Tonks NK. Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol 2006;7:833-46.
4. Zhao R, Fu X, Teng L, Li Q, Zhao ZJ. Blocking the function of tyrosine phosphatase SHP-2 by targeting its Src homology 2 domains. J Biol Chem 2003;278:42893-8.
5. Pawson T. Specificity in signal transduction: from phosphotyrosine- SH2 domain interactions to complex cellular systems. Cell 2004; 116:191-203.
6. Barford D, Neel BG. Revealing mechanisms for SH2 domain mediated regulation of the protein tyrosine phosphatase SHP-2. Structure 1998; 6:249-54.
7. Eck MJ, Pluskey S, Trub T, Harrison SC, Shoelson SE. Spatial constraints on the recognition of phosphoproteins by the tandem SH2 domains of the phosphatase SH-PTP2. Nature 1996;379: 277-80.
8. Hof P, Pluskey S, Dhe-Paganon S, Eck MJ, Shoelson SE. Crystal structure of the tyrosine phosphatase SHP-2. Cell 1998;92:441-50.
9. Loh ML, Vattikuti S, Schubbert S, Reynolds MG, Carlson E, Lieuw KH, et al. Mutations in PTPN11 implicate the SHP-2 phosphatase in leukemogenesis. Blood 2004;103:2325-31.
10. Loh ML, Reynolds MG, Vattikuti S, Gerbing RB, Alonzo TA, Carlson E, et al. PTPN11 mutations in pediatric patients with acute myeloid leukemia: results from the Children's Cancer Group. Leukemia 2004; 18:1831-4.
11. Tartaglia M, Martinelli S, Cazzaniga G, Cordeddu V, Iavarone I, Spinelli M, et al. Genetic evidence for lineage-related and differentiation stagerelated contribution of somatic PTPN11 mutations to leukemogenesis in childhood acute leukemia. Blood 2004;104:307-13.
12. Tartaglia M, Mehler EL, Goldberg R, Zampino G, Brunner HG, Kremer H, et al. Mutations in PTPN11, encoding the protein tyrosine phosphatase SHP-2, cause Noonan syndrome. Nat Genet 2001; 29:465-8.
13. Tartaglia M, Niemeyer CM, 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;34:148-50.
14. Bentires-Alj M, Paez JG, David FS, 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;64:8816-20.
15. Keilhack H, David FS, McGregor M, Cantley LC, Neel BG. Diverse biochemical properties of Shp2 mutants. Implications for disease phenotypes. J Biol Chem 2005;280:30984-93.
16. Loh ML, Sakai DS, Flotho C, Kang M, Fliegauf M, Archambeault S, et al. Mutations in CBL occur frequently in juvenile myelomonocytic leukemia. Blood 2009;114:1859-63.
17. Muramatsu H, Makishima H, Jankowska AM, Cazzolli H, O'Keefe C, Yoshida N, et al. Mutations of an E3 ubiquitin ligase c-Cbl but not TET2 mutations are pathogenic in juvenile myelomonocytic leukemia. Blood 2010;115:1969-75.
18. Araki T, Mohi MG, Ismat FA, Bronson RT, Williams IR, Kutok JL, et al. Mouse model of Noonan syndrome reveals cell type- and gene dosage-dependent effects of Ptpn11 mutation. Nat Med 2004; 10:849-57.
19. Chan G, Kalaitzidis D, Usenko T, Kutok JL, Yang W, Mohi MG, et al. Leukemogenic Ptpn11 causes fatal myeloproliferative disorder via cell-autonomous effects on multiple stages of hematopoiesis. Blood 2009;113:4414-24.
20. Chan RJ, Leedy MB, Munugalavadla V, Voorhorst CS, Li Y, Yu M, et al. Human somatic PTPN11 mutations induce hematopoietic-cellhypersensitivity to granulocyte-macrophage colony-stimulating factor. Blood 2005;105:3737-42.
21. Schubbert S, Lieuw K, Rowe SL, Lee CM, Li X, Loh ML, et al. Functional analysis of leukemia-associated PTPN11 mutations in primary hematopoietic cells. Blood 2005;106:311-7.
22. Xu D, Liu X, Yu WM, Meyerson HJ, Guo C, Gerson SL, et al. Nonlineage/ stage-restricted effects of a gain-of-function mutation in tyrosine phosphatase Ptpn11 (Shp2) on malignant transformation of hematopoietic cells. J Exp Med 2011;208:1977-88.
23. Yu WM, Daino H, Chen J, Bunting KD, Qu CK. Effects of a leukemiaassociated gain-of-function mutation of SHP-2 phosphatase on interleukin- 3 signaling. J Biol Chem 2006;281:5426-34.
24. Yu WM, Guvench O, Mackerell AD, Qu CK. Identification of small molecular weight inhibitors of Src homology 2 domain-containing tyrosine phosphatase 2 (SHP-2) via in silico database screening combined with experimental assay. J Med Chem 2008;51:7396-404.
25. Burch JD, Belley M, Fortin R, Deschenes D, Girard M, Colucci J, et al. Structure-activity relationships and pharmacokinetic parameters of quinoline acylsulfonamides as potent and selective antagonists of the EP(4) receptor. Bioorg Med Chem Lett 2008;18:2048-54.
26. Best RB, Zhu X, Shim J, Lopes PE, Mittal J, Feig M, et al. Optimization of the additive CHARMM all-atom protein force field targeting improved sampling of the backbone phi, psi and side-chain chi(1) and chi(2) dihedral angles. J Chem Theory Comput 2012;8:3257-73.
27. Vanommeslaeghe K, Hatcher E, Acharya C, Kundu S, Zhong S, Shim J, et al.CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. J Comput Chem 2010;31:671-90.
28. Lee MS, Feig M, Salsbury FR Jr, Brooks CL III. New analytic approximation to the standard molecular volume definition and its application to generalized Born calculations. J Comput Chem 2003;24:1348-56.
29. Lee MS, Salsbury FR, Brooks CL III. Novel generalized Born methods. J Chem Phys 2002;116:10606-14.
30. Vanommeslaeghe K, MacKerell AD Jr. Automation of the CHARMM General Force Field (CGenFF) I: bond perception and atom typing. J Chem Inf Model 2012;52:3144-54.
31. Vanommeslaeghe K, Raman EP, MacKerell AD Jr. Automation of the CHARMM General Force Field (CGenFF) II: assignment of bonded parameters and partial atomic charges. J Chem Inf Model 2012; 52:3155-68.
32. Ryckaert JP, Ciccotti G, Berendsen HJC. Numerical integration of Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 1977;23:327-41.
33. Steinbach PJ, Brooks BR. New spherical-cutoff methods for longrange forces in macromolecular simulation. J Comput Chem 1994; 15:667-83.
34. Pastor RW. Techniques and applications of langevin dynamics simulations. In:Luckhurst GR, Veracini CA, editors. The molecular dynamics of liquid crystals. the Netherlands: Kluwer Academic Publishers; 1994. p. 85-138.
35. Brooks BR, Brooks CL III, Mackerell AD Jr, Nilsson L, Petrella RJ, Roux B, et al. CHARMM: the biomolecular simulation program. J Comput Chem 2009;30:1545-614.
36. Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics. J Mol Graph 1996;14:33-8.
37. Macias AT, Mia MY, Xia G, Hayashi J, MacKerell AD Jr. Lead validation and SAR development via chemical similarity searching; application to compounds targeting the pY+3 site of the SH2 domain of p56lck. J Chem Inf Model 2005;45:1759-66.
38. Tartaglia M, Cotter PD, Zampino G, Gelb BD, Rauen KA. Exclusion of PTPN11 mutations in Costello syndrome: further evidence for distinct genetic etiologies for Noonan, cardio-facio-cutaneous and Costello syndromes. Clin Genet 2003;63:423-6.
39. Tartaglia M, Martinelli S, Stella L, Bocchinfuso G, Flex E, Cordeddu V, et al. Diversity and functional consequences of germline and somatic PTPN11 mutations in human disease. Am J Hum Genet 2006;78: 279-90.
40. Yu WM, Hawley TS, Hawley RG, Qu CK. Catalytic-dependent and -independent roles of SHP-2 tyrosine phosphatase in interleukin-3 signaling. Oncogene 2003;22:5995-6004.
41. Bennett AM, Hausdorff SF, O'Reilly AM, Freeman RM, Neel BG. Multiple requirements for SHPTP2 in epidermal growth factor-mediated cell cycle progression. Mol Cell Biol 1996;16:1189-202.
42. Nishida K, Hirano T. The role of Gab family scaffolding adapter proteins in the signal transduction of cytokine and growth factor receptors. Cancer Sci 2003;94:1029-33.
43. Gu H, Neel BG. The "Gab" in signal transduction. Trends Cell Biol 2003;13:122-30.
44. Emanuel PD, Bates LJ, Castleberry RP, Gualtieri RJ, Zuckerman KS. Selective hypersensitivity to granulocyte-macrophage colony-stimulating factor by juvenile chronic myeloid leukemia hematopoietic progenitors. Blood 1991;77:925-9.
45. Lyubynska N, Gorman MF, Lauchle JO, Hong WX, Akutagawa JK, Shannon K, et al. A MEK inhibitor abrogates myeloproliferative disease in Kras mutant mice. Sci Transl Med 2011;3: 76ra27.
46. Zhang X, He Y, Liu S, Yu Z, Jiang ZX, Yang Z, et al. Salicylic acid based small molecule inhibitor for the oncogenic Src homology-2 domain containing protein tyrosine phosphatase-2 (SHP2). J Med Chem 2010;53:2482-93.
47. Hellmuth K, Grosskopf S, Lum CT, Wurtele M, Roder N, von Kries JP, et al. Specific inhibitors of the protein tyrosine phosphatase Shp2 identified by high-throughput docking. Proc Natl Acad Sci U S A 2008;105:7275-80.
48. Dawson MI, Xia Z, Jiang T, Ye M, Fontana JA, Farhana L, et al. Adamantyl-substituted retinoid-derived molecules that interact with the orphan nuclear receptor small heterodimer partner: effects of replacing the 1-adamantyl or hydroxyl group on inhibition of cancer cell growth, induction of cancer cell apoptosis, and inhibition of SRC homology 2 domain-containing protein tyrosine phosphatase-2 activity. J Med Chem 2008;51: 5650-62.
49. Chen L, Sung SS, Yip ML, Lawrence HR, Ren Y, Guida WC, et al. Discovery of a novel shp2 protein tyrosine phosphatase inhibitor. Mol Pharmacol 2006;70:562-70.
50. Chan G, Cheung LS, Yang W, Milyavsky M, Sanders AD, Gu S, et al. Essential role for Ptpn11 in survival of hematopoietic stem and progenitor cells. Blood 2011;117:4253-61.
51. Yang W, Klaman LD, Chen B, Araki T, Harada H, Thomas SM, et al. An Shp2/SFK/Ras/Erk signaling pathway controls trophoblast stem cell survival. Dev Cell 2006;10:317-27.
52. Zhu HH, Ji K, Alderson N, He Z, Li S, Liu W, et al. Kit-Shp2-Kit signaling acts to maintain a functional hematopoietic stem and progenitor cell pool. Blood 2011;117:5350-61.