Characterization of the TGF-b1 signaling abnormalities in the Gata1low mouse model of myelofibrosis

Blood

Volumn 121, Issue 17, 2013, Pages 3345-3363

  Zingariello, Maria ^a   Martelli, Fabrizio ^a   Ciaffoni, Fiorella ^a   Masiello, Francesca ^a   Ghinassi, Barbara ^b,c   D’Amore, Emanuela ^a   Massa, Margherita ^d   Barosi, Giovanni ^d   Sancillo, Laura ^e   Li, Xiaochun ^c   Goldberg, Judith D ^c,f   Alba Rana, Rosa ^e   Rita Migliaccio, Anna ^a,c  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c Myeloproliferative Disorder Research Consortium   (United States)

^d FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

^e UNIVERSITY OF CHIETI   (Italy)

^f NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; COLONY STIMULATING FACTOR 1; CXCL1 CHEMOKINE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 9; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN P53; RANTES; SONIC HEDGEHOG PROTEIN; STAT1 PROTEIN; STROMAL CELL DERIVED FACTOR 1; TRANSCRIPTION FACTOR GATA 1; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR; UBIQUITIN; VASCULOTROPIN; CXCL12 PROTEIN, MOUSE; CYTOKINE; MTOR PROTEIN, HUMAN; SMALL INTERFERING RNA; TARGET OF RAPAMYCIN KINASE; TUMOR MARKER; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE MARROW; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EXTRAMEDULLARY HEMATOPOIESIS; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MEGAKARYOCYTE; MEGAKARYOPOIESIS; MIDDLE AGED; MOLECULAR PATHOLOGY; MOUSE; MYELOID METAPLASIA; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; OSTEOBLAST; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; SPLEEN; ANIMAL; CASE CONTROL STUDY; COMPARATIVE STUDY; DISEASE MODEL; DNA MICROARRAY; DRUG ANTAGONISM; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ADULT; ANIMALS; BLOTTING, WESTERN; BONE MARROW; CASE-CONTROL STUDIES; CHEMOKINE CXCL12; CYTOKINES; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; GATA1 TRANSCRIPTION FACTOR; GENE EXPRESSION PROFILING; HUMANS; MALE; MICE; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PRIMARY MYELOFIBROSIS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SPLEEN; TOR SERINE-THREONINE KINASES; TRANSFORMING GROWTH FACTOR BETA1; TUMOR MARKERS, BIOLOGICAL; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

MLCS; MLOWN;

EID: 84879390119     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-06-439661     Document Type: Article

References (50)

1. Massague J. TGFbeta in cancer. Cell. 2008; 134(2):215-230.
2. Assoian RK, Komoriya A, Meyers CA, Miller DM, Sporn MB. Transforming growth factor-beta in human platelets. Identification of a major storage site, purification, and characterization. J Biol Chem. 1983;258(11):7155-7160.
3. Van Obberghen-Schilling E, Roche NS, Flanders KC, Sporn MB, Roberts AB. Transforming growth factor beta 1 positively regulates its own expression in normal and transformed cells. J Biol Chem. 1988;263(16):7741-7746.
4. Liu T, Feng XH. Regulation of TGF-beta signaling by protein phosphatases. Biochem J. 2010; 430(2):191-198.
5. Flavell RA, Sanjabi S, Wrzesinski SH, Licona-Limon P. The polarization of immune cells in the tumour environment by TGFbeta. Nat Rev Immunol. 2010;10(8):554-567.
6. Tefferi A. Myelofibrosis with myeloid metaplasia. N Engl J Med. 2000;342(17):1255-1265.
7. Schmitt A, Jouault H, Guichard J, Wendling F, Drouin A, Cramer EM. Pathologic interaction between megakaryocytes and polymorphonuclear leukocytes in myelofibrosis. Blood. 2000;96(4): 1342-1347.
8. Chou JM, Li CY, Tefferi A. Bone marrow immunohistochemical studies of angiogenic cytokines and their receptors in myelofibrosis with myeloid metaplasia. Leuk Res. 2003;27(6): 499-504.
9. Le Bousse-Kerdiles MC, Chevillard S, Charpentier A, et al. Differential expression of transforming growth factor-beta, basic fibroblast growth factor, and their receptors in CD341 hematopoietic progenitor cells from patients with myelofibrosis and myeloid metaplasia. Blood. 1996;88(12): 4534-4546.
10. Campanelli R, Rosti V, Villani L, et al. Evaluation of the bioactive and total transforming growth factor beta1 levels in primary myelofibrosis. Cytokine. 2011;53(1):100-106.
11. Lataillade JJ, Pierre-Louis O, Hasselbalch HC, et al. Does primary myelofibrosis involve a defective stem cell niche? From concept to evidence. Blood. 2008;112(8):3026-3035.
12. Bumm TG, Elsea C, Corbin AS, et al. Characterization of murine JAK2V617F-positive myeloproliferative disease. Cancer Res. 2006; 66(23):11156-11165.
13. Tyner JW, Bumm TG, Deininger J, et al. CYT387, a novel JAK2 inhibitor, induces hematologic responses and normalizes inflammatory cytokines in murine myeloproliferative neoplasms. Blood. 2012;115(25):5232-5240.
14. Fleischman AG, Aichberger KJ, Luty SB, et al. TNFalpha facilitates clonal expansion of JAK2V617F positive cells in myeloproliferative neoplasms. Blood. 2011;118(24):6392-6398.
15. Bock O, Hoftmann J, Theophile K, et al. Bone morphogenetic proteins are overexpressed in the bone marrow of primary myelofibrosis and are apparently induced by fibrogenic cytokines. Am J Pathol. 2008;172(4):951-960.
16. Migliaccio AR, Martelli F, Verrucci M, et al. Altered SDF-1/CXCR4 axis in patients with primary myelofibrosis and in the Gata1low mouse model of the disease. Exp Hematol. 2008;36(2):158-171.
17. Broxmeyer HE. Chemokines in hematopoiesis. Curr Opin Hematol. 2008;15(1):49-58.
18. Bogani C, Ponziani V, Guglielmelli P, et al. Hypermethylation of CXCR4 promoter in CD341 cells from patients with primary myelofibrosis. Stem Cells. 2008;26(8):1920-1930.
19. Varricchio L, Mancini A, Migliaccio AR. Pathological interactions between hematopoietic stem cells and their niche revealed by mouse models of primary myelofibrosis. Expert Rev Hematol. 2009;2(3):315-334.
20. Tefferi A, Vainchenker W. Myeloproliferative neoplasms: molecular pathophysiology, essential clinical understanding, and treatment strategies. J Clin Oncol. 2011;29(5):573-582.
21. Chagraoui H, Komura E, Tulliez M, Giraudier S, Vainchenker W, Wendling F. Prominent role of TGF-beta 1 in thrombopoietin-induced myelofibrosis in mice. Blood. 2002;100(10): 3495-3503.
22. Danielsson S, Merup M, Olsson L, et al. X-bunden trombocytopeni med talassemi i två svenska familjer. Lakartidningen. 2012;109(34-35): 1474-1477.
23. Martelli F, Ghinassi B, Panetta B, et al. Variegation of the phenotype induced by the Gata1low mutation in mice of different genetic backgrounds. Blood. 2005;106(13):4102-4113.
24. Gastinne T, Vigant F, Lavenu-Bombled C, et al. Adenoviral-mediated TGF-beta1 inhibition in a mouse model of myelofibrosis inhibit bone marrow fibrosis development. Exp Hematol. 2007; 35(1):64-74.
25. Vannucchi AM, Bianchi L, Cellai C, et al. Development of myelofibrosis in mice genetically impaired for GATA-1 expression (GATA-1(low) mice). Blood. 2002;100(4):1123-1132.
26. Vannucchi AM, Bianchi L, Paoletti F, et al. A pathobiologic pathway linking thrombopoietin, GATA-1, and TGF-beta1 in the development of myelofibrosis. Blood. 2005;105(9):3493-3501.
27. Tefferi A, Thiele J, Orazi A, et al. Proposals and rationale for revision of the World Health Organization diagnostic criteria for polycythemia vera, essential thrombocythemia, and primary myelofibrosis: recommendations from an ad hoc international expert panel. Blood. 2007;110(4): 1092-1097.
28. Example of the informed consent form used for the study may be downloaded on the website http://www.mpd-rc.org/home.php.
29. Inman GJ, Nicolas FJ, Callahan JF, et al. SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol Pharmacol. 2002;62(1): 65-74.
30. Migliaccio AR, Martelli F, Verrucci M, et al. Gata1 expression driven by the alternative HS2 enhancer in the spleen rescues the hematopoietic failure induced by the hypomorphic Gata1low mutation. Blood. 2009;114(10):2107-2120.
31. Zetterberg E, Vannucchi AM, Migliaccio AR, et al. Pericyte coverage of abnormal blood vessels in myelofibrotic bone marrows. Haematologica. 2007;92(5):597-604.
32. Prasad K, Prabhu GK. Image analysis tools for evaluation of microscopic views of immunohistochemically stained specimen in medical research: a review. J Med Syst. 2011; 36(4):2621-2631.
33. Centurione L, Di Baldassarre A, Zingariello M, et al. Increased and pathologic emperipolesis of neutrophils within megakaryocytes associated with marrow fibrosis in GATA-1low mice. Blood. 2004;104(12):3573-3580.
34. Fitzmaurice G, Laird N, Ware J. Applied longitudinal analysis. Hoboken, NJ: Wiley; 2004.
35. Martyre MC, Romquin N, Le Bousse-Kerdiles MC, et al. Transforming growth factor-beta and megakaryocytes in the pathogenesis of idiopathic myelofibrosis. Br J Haematol. 1994;88(1):9-16.
36. Khandros E, Weiss MJ. Protein quality control during erythropoiesis and hemoglobin synthesis. Hematol Oncol Clin North Am. 2010;24(6): 1071-1088.
37. Grech G, Blazquez-Domingo M, Kolbus A, et al. Igbp1 is part of a positive feedback loop in stem cell factor-dependent, selective mRNA translation initiation inhibiting erythroid differentiation. Blood. 2008;112(7):2750-2760.
38. McDevitt MA, Shivdasani RA, Fujiwara Y, Yang H, Orkin SHA. “knockdown” mutation created by cis-element gene targeting reveals the dependence of erythroid cell maturation on the level of transcription factor GATA-1. Proc Natl Acad Sci USA. 1997;94(13):6781-6785.
39. Verrucci M, Pancrazzi A, Aracil M, et al. CXCR4-independent rescue of the myeloproliferative defect of the Gata1low myelofibrosis mouse model by Aplidin. J Cell Physiol. 2010;225(2):490-499.
40. He W, Dorn DC, Erdjument-Bromage H, Tempst P, Moore MA, Massague J. Hematopoiesis controlled by distinct TIF1gamma and Smad4 branches of the TGFbeta pathway. Cell. 2006; 125(5):929-941.
41. Vannucchi AM, Pancrazzi A, Guglielmelli P, et al. Abnormalities of GATA-1 in megakaryocytes from patients with idiopathic myelofibrosis. Am J Pathol. 2005;167(3):849-858.
42. Frandsen JL, Gunn B, Muratoglu S, Fossett N, Newfeld SJ. Salmonella pathogenesis reveals that BMP signaling regulates blood cell homeostasis and immune responses in Drosophila. Proc Natl Acad Sci USA. 2008; 105(39):14952-14957.
43. Gao H, Wu X, Fossett N. Odd-skipped maintains prohemocyte potency and blocks blood cell development in Drosophila. Genesis. 2011;49(3): 105-116.
44. Guglielmelli P, Barosi G, Rambaldi A, et al. Safety and efficacy of everolimus, a mTOR inhibitor, as single agent in a phase 1/2 study in patients with myelofibrosis. Blood. 2011;118(8):2069-2076.
45. Pardanani A, Tefferi A. Targeting myeloproliferative neoplasms with JAK inhibitors. Curr Opin Hematol. 2011;18(2):105-110.
46. Hoffman R, Xu M. Is bone marrow fibrosis the real problem? Blood. 2006;107(9):3421-3422.
47. Bobik R, Dabrowski Z. Emperipolesis of marrow cells within megakaryocytes in the bone marrow of sublethally irradiated mice. Ann Hematol. 1995; 70(2):91-95.
48. Rondelli D. Allogeneic hematopoietic stem cell transplantation for myelofibrosis. Haematologica. 2008;93(10):1449-1450.
49. Zon LI, Tsai SF, Burgess S, Matsudaira P, Bruns GA, Orkin SH. The major human erythroid DNA-binding protein (GF-1): primary sequence and localization of the gene to the X chromosome. Proc Natl Acad Sci USA. 1990;87(2):668-672.
50. Wang X, Prakash S, Lu M, et al. Spleens of myelofibrosis patients contain malignant hematopoietic stem cells. J Clin Invest. 2012; 122(11):3888-3899.