LNK/SH2B3 regulates IL-7 receptor signaling in normal and malignant B-progenitors

Journal of Clinical Investigation

Volumn 126, Issue 4, 2016, Pages 1267-1281

  Cheng, Ying ^a,b   Chikwava, Kudakwashe ^a   Wu, Chao ^a   Zhang, Haibing ^a   Bhagat, Anchit ^a   Pei, Dehua ^c   Choi, John K ^d   Tong, Wei ^a,b  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c OHIO STATE UNIVERSITY   (United States)

^d ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADAPTOR PROTEIN LNK; CYCLIN DEPENDENT KINASE INHIBITOR 2A; DACTOLISIB; INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR; JANUS KINASE; JANUS KINASE 3; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P53; RUXOLITINIB; SELUMETINIB; STAT5 PROTEIN; TOFACITINIB; TRAMETINIB; UNCLASSIFIED DRUG; JAK3 PROTEIN, HUMAN; JAK3 PROTEIN, MOUSE; LNK PROTEIN, MOUSE; MEMBRANE PROTEIN; MTOR PROTEIN, HUMAN; MTOR PROTEIN, MOUSE; PROTEIN; SH2B3 PROTEIN, HUMAN; SIGNAL PEPTIDE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TARGET OF RAPAMYCIN KINASE; TP53 PROTEIN, HUMAN;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL EXPANSION; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION PROFILING; GENE MUTATION; HOMEOSTASIS; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INVESTIGATIVE PROCEDURES; MOUSE; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; GENETICS; KNOCKOUT MOUSE; METABOLISM; MUTATION; PATHOLOGY; PHILADELPHIA 1 CHROMOSOME; TUMOR CELL LINE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL LINE, TUMOR; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; JANUS KINASE 3; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MUTATION; PHILADELPHIA CHROMOSOME; PHOSPHATIDYLINOSITOL 3-KINASES; PRECURSOR B-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PRECURSOR CELLS, B-LYMPHOID; PROTEINS; RECEPTORS, INTERLEUKIN-7; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; TOR SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84964632107     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI81468     Document Type: Article

References (50)

1. Mullighan CG. Molecular genetics of B-precursor acute lymphoblastic leukemia. J Clin Invest. 2012;122(10):3407-3415.
2. Roberts KG, et al. Genetic alterations activating kinase and cytokine receptor signaling in highrisk acute lymphoblastic leukemia. Cancer cell. 2012;22(2):153-166.
3. Harvey RC, et al. Identification of novel cluster groups in pediatric high-risk B-precursor acute lymphoblastic leukemia with gene expression profiling: correlation with genome-wide DNA copy number alterations, clinical characteristics, and outcome. Blood. 2010;116(23):4874-4884.
4. Loh ML, et al. Tyrosine kinome sequencing of pediatric acute lymphoblastic leukemia: A report from the Children's Oncology Group TARGET Project. Blood. 2013;121(3):485-488.
5. Schultz KR, et al. Risk-and response-based classification of childhood B-precursor acute lymphoblastic leukemia: A combined analysis of prognostic markers from the Pediatric Oncology Group (POG) and Children's Cancer Group (CCG). Blood. 2007;109(3):926-935.
6. Roberts KG, et al. Targetable kinase-activating lesions in Ph-like acute lymphoblastic leukemia. N Engl J Med. 2014;371(11):1005-1015.
7. Zhang J, et al. Key pathways are frequently mutated in high-risk childhood acute lymphoblastic leukemia: A report from the Children's Oncology Group. Blood. 2011;118(11):3080-3087.
8. Mullighan CG, et al. JAK mutations in high-risk childhood acute lymphoblastic leukemia. Proc Natl Acad Sci U S A. 2009;106(23):9414-9418.
9. Mullighan CG, et al. Rearrangement of CRLF2 in B-progenitor-and Down syndromeassociated acute lymphoblastic leukemia. Nat Genet. 2009;41(11):1243-1246.
10. Harvey RC, et al. Rearrangement of CRLF2 is associated with mutation of JAK kinases, alteration of IKZF1, Hispanic/Latino ethnicity, and a poor outcome in pediatric B-progenitor acute lymphoblastic leukemia. Blood. 2010;115(26):5312-5321.
11. Shochat C, et al. Gain-of-function mutations in interleukin-7 receptor-alpha (IL7R) in childhood acute lymphoblastic leukemias. J Exp Med. 2011;208(5):901-908.
12. Yoda A, et al. Functional screening identifies CRLF2 in precursor B-cell acute lymphoblastic leukemia. Proc Natl Acad Sci U S A. 2010;107(1):252-257.
13. Quentmeier H, et al. Cloning of human thymic stromal lymphopoietin (TSLP) and signaling mechanisms leading to proliferation. Leukemia. 2001;15(8):1286-1292.
14. Ziegler SF, Artis D. Sensing the outside world: TSLP regulates barrier immunity. Nat Immunol. 2010;11(4):289-293.
15. Levin SD, et al. Thymic stromal lymphopoietin: A cytokine that promotes the development of IgM+ B cells and signals via a novel mechanism. J Immunol. 1999;162(2):677-683.
16. Isaksen DE, Baumann H, Trobridge PA, Farr AG, Levin SD, Ziegler SF. Requirement for stat5 in thymic stromal lymphopoietin-mediated signal transduction. J Immunol. 1999;163(11):5971-5977.
17. Isaksen DE, et al. Uncoupling of proliferation and Stat5 activation in thymic stromal lymphopoietin-mediated signal transduction. J Immunol. 2002;168(7):3288-3294.
18. Zhong J, et al. TSLP signaling network revealed by SILAC-based phosphoproteomics. Mol Cell Proteomics. 2012;11(6):M112 017764.
19. Hertzberg L, et al. Down syndrome acute lymphoblastic leukemia, a highly heterogeneous disease in which aberrant expression of CRLF2 is associated with mutated JAK2: A report from the International BFM Study Group. Blood. 2010;115(5):1006-1017.
20. Bercovich D, et al. Mutations of JAK2 in acute lymphoblastic leukaemias associated with Down's syndrome. Lancet. 2008;372(9648):1484-1492.
21. Weigert O, et al. Genetic resistance to JAK2 enzymatic inhibitors is overcome by HSP90 inhibition. J Exp Med. 2012;209(2):259-273.
22. Takaki S, et al. Control of B cell production by the adaptor protein lnk. Definition Of a conserved family of signal-modulating proteins. Immunity. 2000;13(5):599-609.
23. Velazquez L, et al. Cytokine signaling and hematopoietic homeostasis are disrupted in Lnk-deficient mice. J Exp Med. 2002;195(12):1599-1611.
24. Ema H, et al. Quantification of self-renewal capacity in single hematopoietic stem cells from normal and Lnk-deficient mice. Dev Cell. 2005;8(6):907-914.
25. Seita J, et al. Lnk negatively regulates self-renewal of hematopoietic stem cells by modifying thrombopoietin-mediated signal transduction. Proc Natl Acad Sci U S A. 2007;104(7):2349-2354.
26. Bersenev A, Wu C, Balcerek J, Tong W. Lnk controls mouse hematopoietic stem cell self-renewal and quiescence through direct interactions with JAK2. J Clin Invest. 2008;118(8):2832-2844.
27. Buza-Vidas N, et al. Cytokines regulate postnatal hematopoietic stem cell expansion: opposing roles of thrombopoietin and LNK. Genes Dev. 2006;20(15):2018-2023.
28. Lin DC, et al. Adaptor protein Lnk binds to and inhibits normal and leukemic FLT3. Blood. 2012;120(16):3310-3317.
29. Zhang J, et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature. 2012;481(7380):157-163.
30. Perez-Garcia A, et al. Genetic loss of SH2B3 in acute lymphoblastic leukemia. Blood. 2013;122(14):2425-2432.
31. Bersenev A, et al. Lnk constrains myeloproliferative diseases in mice. J Clin Invest. 2010;120(6):2058-2069.
32. Hof J, et al. Mutations and deletions of the TP53 gene predict nonresponse to treatment and poor outcome in first relapse of childhood acute lymphoblastic leukemia. J Clin Oncol. 2011;29(23):3185-3193.
33. Chiaretti S, et al. TP53 mutations are frequent in adult acute lymphoblastic leukemia cases negative for recurrent fusion genes and correlate with poor response to induction therapy. Haematologica. 2013;98(5):e59-e61.
34. Donehower LA, et al. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature. 1992;356(6366):215-221.
35. Donehower LA, Lozano G. 20 years studying p53 functions in genetically engineered mice. Nat Rev Cancer. 2009;9(11):831-841.
36. Jacks T, et al. Tumor spectrum analysis in p53-mutant mice. Curr Biol. 1994;4(1):1-7.
37. Subramanian A, et al. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102(43):15545-15550.
38. Adolfsson J, et al. Identification of Flt3+ lymphomyeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell. 2005;121(2):295-306.
39. Kondo M, Weissman IL, Akashi K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell. 1997;91(5):661-672.
40. Min H, Montecino-Rodriguez E, Dorshkind K. Effects of aging on the common lymphoid progenitor to pro-B cell transition. J Immunol. 2006;176(2):1007-1012.
41. Hardy RR, Carmack CE, Shinton SA, Kemp JD, Hayakawa K. Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J Exp Med. 1991;173(5):1213-1225.
42. Miller JP, Allman D. The decline in B lymphopoiesis in aged mice reflects loss of very early B-lineage precursors. J Immunol. 2003;171(5):2326-2330.
43. Oh ST, et al. Novel mutations in the inhibitory adaptor protein LNK drive JAK-STAT signaling in patients with myeloproliferative neoplasms. Blood. 2010;116(6):988-992.
44. Abdel-Wahab O. Genetics of the myeloproliferative neoplasms. Curr Opin Hematol. 2011;18(2):117-123.
45. Louria-Hayon I, et al. Lnk adaptor suppresses radiation resistance and radiation-induced B-cell malignancies by inhibiting IL-11 signaling. Proc Natl Acad Sci U S A. 2013;110(51):20599-20604.
46. Hoelbl A, et al. Stat5 is indispensable for the maintenance of bcr/abl-positive leukaemia. EMBO Mol Med. 2010;2(3):98-110.
47. Joliot V, Cormier F, Medyouf H, Alcalde H, Ghysdael J. Constitutive STAT5 activation specifically cooperates with the loss of p53 function in B-cell lymphomagenesis. Oncogene. 2006;25(33):4573-4584.
48. Maude SL, et al. Targeting JAK1/2 and mTOR in murine xenograft models of Ph-like acute lymphoblastic leukemia. Blood. 2012;120(17):3510-3518.
49. Gurney AL, Carver-Moore K, de Sauvage FJ, Moore MW. Thrombocytopenia in c-mpl-deficient mice. Science. 1994;265(5177):1445-1447.
50. Smith KS, Rhee JW, Cleary ML. Transformation of bone marrow B-cell progenitors by E2a-Hlf requires coexpression of Bcl-2. Mol Cell Biol. 2002;22(21):7678-7687.