Leukaemogenic effects of Ptpn11 activating mutations in the stem cell microenvironment

Nature

Volumn 539, Issue 7628, 2016, Pages 304-308

  Dong, Lei ^a   Yu, Wen Mei ^a   Zheng, Hong ^a   Loh, Mignon L ^b   Bunting, Silvia T ^a   Pauly, Melinda ^a   Huang, Gang ^c   Zhou, Muxiang ^a   Broxmeyer, Hal E ^d   Scadden, David T ^e   Qu, Cheng Kui ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CINCINNATI   (United States)

^d INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e Harvard University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 5; NESTIN; PROTEIN KINASE B; PROTEIN TYROSINE PHOSPHATASE SHP 2; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSCRIPTION FACTOR OSTERIX; PTPN11 PROTEIN, HUMAN; PTPN11 PROTEIN, MOUSE;

BONE; CANCER; CELLS AND CELL COMPONENTS; JUVENILE; MUTATION; PHOSPHATASE; PROTEIN; RODENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL ISOLATION; COLONY FORMING UNIT F; COLONY FORMING UNIT GM; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; ENDOTHELIUM CELL; GENE EXPRESSION PROFILING; GENE MUTATION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN TISSUE; IN VITRO STUDY; INTRACELLULAR SIGNALING; LEUKEMOGENESIS; MONOCYTE; MOUSE; MYELOPROLIFERATIVE NEOPLASM; NONHUMAN; NOONAN SYNDROME; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA SEQUENCE; TUMOR MICROENVIRONMENT; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL TRANSFORMATION; CYTOLOGY; DISEASE COURSE; FEMALE; GENETICS; JUVENILE MYELOMONOCYTIC LEUKEMIA; LEUKEMIA; MALE; MESENCHYMAL STROMA CELL; METABOLISM; MUTATION; PATHOLOGY; STEM CELL NICHE; STEM CELL TRANSPLANTATION;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; CELLULAR MICROENVIRONMENT; CHEMOKINE CCL3; DISEASE PROGRESSION; ENDOTHELIAL CELLS; FEMALE; HEMATOPOIETIC STEM CELLS; HUMANS; INTERLEUKIN-1BETA; LEUKEMIA; LEUKEMIA, MYELOMONOCYTIC, JUVENILE; MALE; MESENCHYMAL STROMAL CELLS; MICE; MONOCYTES; MUTATION; NOONAN SYNDROME; OSTEOBLASTS; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11; STEM CELL NICHE; STEM CELL TRANSPLANTATION;

EID: 85016130633     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature20131     Document Type: Article

References (39)

1. Mohi, M. G. & Neel, B. G. The role of Shp2 (PTPN11) in cancer. Curr. Opin. Genet. Dev. 17, 23-30 (2007).
2. Tartaglia, M. et al. Mutations in PTPN11, encoding the protein tyrosine phosphatase SHP-2, cause Noonan syndrome. Nat. Genet. 29, 465-468 (2001).
3. Roberts, A. E., Allanson, J. E., Tartaglia, M. & Gelb, B. D. Noonan syndrome. Lancet 381, 333-342 (2013).
4. Araki, T. et al. Mouse model of Noonan syndrome reveals cell type- and gene dosage-dependent effects of Ptpn11 mutation. Nat. Med. 10, 849-857 (2004).
5. Xu, D. et al. Non-lineage/stage-restricted effects of a gain-of-function mutation in tyrosine phosphatase Ptpn11 (Shp2) on malignant transformation of hematopoietic cells. J. Exp. Med. 208, 1977-1988 (2011).
6. Chan, G. et al. Leukemogenic Ptpn11 causes fatal myeloproliferative disorder via cell-autonomous effects on multiple stages of hematopoiesis. Blood 113, 4414-4424 (2009).
7. Mohi, M. G. et al. Prognostic, therapeutic, and mechanistic implications of a mouse model of leukemia evoked by Shp2 (PTPN11) mutations. Cancer Cell 7, 179-191 (2005).
8. Méndez-Ferrer, S. et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466, 829-834 (2010).
9. Kunisaki, Y. et al. Arteriolar niches maintain haematopoietic stem cell quiescence. Nature 502, 637-643 (2013).
10. Park, D. et al. Endogenous bone marrow MSCs are dynamic, fate-restricted participants in bone maintenance and regeneration. Cell Stem Cell 10, 259-272 (2012).
11. Walkley, C. R., Shea, J. M., Sims, N. A., Purton, L. E. & Orkin, S. H. Rb regulates interactions between hematopoietic stem cells and their bone marrow microenvironment. Cell 129, 1081-1095 (2007).
12. Kfoury, Y. & Scadden, D. T. Mesenchymal cell contributions to the stem cell niche. Cell Stem Cell 16, 239-253 (2015).
13. Mendelson, A. & Frenette, P. S. Hematopoietic stem cell niche maintenance during homeostasis and regeneration. Nat. Med. 20, 833-846 (2014).
14. Morrison, S. J. & Scadden, D. T. The bone marrow niche for haematopoietic stem cells. Nature 505, 327-334 (2014).
15. Mizoguchi, T. et al. Osterix marks distinct waves of primitive and definitive stromal progenitors during bone marrow development. Dev. Cell 29, 340-349 (2014).
16. Reynaud, D. et al. IL-6 controls leukemic multipotent progenitor cell fate and contributes to chronic myelogenous leukemia development. Cancer Cell 20, 661-673 (2011).
17. Zhang, B. et al. Altered microenvironmental regulation of leukemic and normal stem cells in chronic myelogenous leukemia. Cancer Cell 21, 577-592 (2012).
18. Schepers, K. et al. Myeloproliferative neoplasia remodels the endosteal bone marrow niche into a self-reinforcing leukemic niche. Cell Stem Cell 13, 285-299 (2013).
19. Wang, L. et al. Notch-dependent repression of miR-155 in the bone marrow niche regulates hematopoiesis in an NF-κ B-dependent manner. Cell Stem Cell 15, 51-65 (2014).
20. Walkley, C. R. et al. A microenvironment-induced myeloproliferative syndrome caused by retinoic acid receptor gamma deficiency. Cell 129, 1097-1110 (2007).
21. Khokha, R., Murthy, A. & Weiss, A. Metalloproteinases and their natural inhibitors in inflammation and immunity. Nat. Rev. Immunol. 13, 649-665 (2013).
22. Ding, L. & Morrison, S. J. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 495, 231-235 (2013).
23. Greenbaum, A. et al. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 495, 227-230 (2013).
24. Shi, C. & Pamer, E. G. Monocyte recruitment during infection and inflammation. Nat. Rev. Immunol. 11, 762-774 (2011).
25. Youn, B. S., Mantel, C. & Broxmeyer, H. E. Chemokines, chemokine receptors and hematopoiesis. Immunol. Rev. 177, 150-174 (2000).
26. Bruns, I. et al. Megakaryocytes regulate hematopoietic stem cell quiescence through CXCL4 secretion. Nat. Med. 20, 1315-1320 (2014).
27. Zhao, M. et al. Megakaryocytes maintain homeostatic quiescence and promote post-injury regeneration of hematopoietic stem cells. Nat. Med. 20, 1321-1326 (2014).
28. Kiel, M. J. et al. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121, 1109-1121 (2005).
29. Ding, L., Saunders, T. L., Enikolopov, G. & Morrison, S. J. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481, 457-462 (2012).
30. Tronche, F. et al. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat. Genet. 23, 99-103 (1999).
31. Kühn, R., Schwenk, F., Aguet, M. & Rajewsky, K. Inducible gene targeting in mice. Science 269, 1427-1429 (1995).
32. Stadtfeld, M. & Graf, T. Assessing the role of hematopoietic plasticity for endothelial and hepatocyte development by non-invasive lineage tracing. Development 132, 203-213 (2005).
33. Logan, M. et al. Expression of Cre Recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis 33, 77-80 (2002).
34. DeFalco, J. et al. Virus-assisted mapping of neural inputs to a feeding center in the hypothalamus. Science 291, 2608-2613 (2001).
35. Rodda, S. J. & McMahon, A. P. Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 133, 3231-3244 (2006).
36. Zhang, M. et al. Osteoblast-specific knockout of the insulin-like growth factor (IGF) receptor gene reveals an essential role of IGF signaling in bone matrix mineralization. J. Biol. Chem. 277, 44005-44012 (2002).
37. Monvoisin, A. et al. VE-cadherin-CreERT2 transgenic mouse: a model for inducible recombination in the endothelium. Dev. Dyn. 235, 3413-3422 (2006).
38. Yu, W. M. et al. Metabolic regulation by the mitochondrial phosphatase PTPMT1 is required for hematopoietic stem cell differentiation. Cell Stem Cell 12, 62-74 (2013).
39. Morikawa, S. et al. Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J. Exp. Med. 206, 2483-2496 (2009).