Macrophages support pathological erythropoiesis in polycythemia vera and β-thalassemia

Nature Medicine

Volumn 19, Issue 4, 2013, Pages 437-445

  Ramos, Pedro ^a   Casu, Carla ^a   Gardenghi, Sara ^a   Breda, Laura ^a   Crielaard, Bart J ^a   Guy, Ella ^a   Marongiu, Maria Franca ^a   Gupta, Ritama ^a   Levine, Ross L ^b   Abdel Wahab, Omar ^b   Ebert, Benjamin L ^c   Van Rooijen, Nico ^d   Ghaffari, Saghi ^e   Grady, Robert W ^a   Giardina, Patricia J ^a   Rivella, Stefano ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b Leukemia Service   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLODRONIC ACID; HEMOGLOBIN;

ANEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BETA THALASSEMIA; CELL PROLIFERATION; ENUCLEATION; ERYTHROBLAST; ERYTHROPOIESIS; HUMAN; HUMAN CELL; MACROPHAGE; MOUSE; NONHUMAN; POLYCYTHEMIA VERA; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; DISEASE MODEL; DRUG EFFECT; ERYTHROCYTE COUNT; FEMALE; HEMATOCRIT; MALE; PATHOPHYSIOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RETICULOCYTE;

ANIMALS; BETA-THALASSEMIA; CLODRONIC ACID; DISEASE MODELS, ANIMAL; ERYTHROCYTE COUNT; ERYTHROPOIESIS; FEMALE; HEMATOCRIT; HEMOGLOBINS; HUMANS; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; POLYCYTHEMIA VERA; RETICULOCYTES; STRESS, PHYSIOLOGICAL;

MLCS; MLOWN;

EID: 84878439561     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3126     Document Type: Article

References (62)

1. Tsiftsoglou, A.S., Vizirianakis, I.S. & Strouboulis, J. Erythropoiesis: model systems, molecular regulators, and developmental programs. IUBMB Life 61, 800-830 (2009).
2. Sathyanarayana, P. et al. EPO receptor circuits for primary erythroblast survival. Blood 111, 5390-5399 (2008).
3. Wojchowski, D.M. et al. Erythropoietin-dependent erythropoiesis: new insights and questions. Blood Cells Mol. Dis. 36, 232-238 (2006).
4. Wu, H., Klingmuller, U., Besmer, P. & Lodish, H.F. Interaction of the erythropoietin and stem-cell-factor receptors. Nature 377, 242-246 (1995).
5. Miyagawa, S., Kobayashi, M., Konishi, N., Sato, T. & Ueda, K. Insulin and insulin-like growth factor I support the proliferation of erythroid progenitor cells in bone marrow through the sharing of receptors. Br. J. Haematol. 109, 555-562 (2000).
6. Shaked, Y. et al. The splenic microenvironment is a source of proangiogenesis/inflammatory mediators accelerating the expansion of murine erythroleukemic cells. Blood 105, 4500-4507 (2005).
7. Cerdan, C., Rouleau, A. & Bhatia, M. VEGF-A165 augments erythropoietic development from human embryonic stem cells. Blood 103, 2504-2512 (2004).
8. Cervi, D. et al. Enhanced natural-killer cell and erythropoietic activities in VEGF-A-overexpressing mice delay F-MuLV-induced erythroleukemia. Blood 109, 2139-2146 (2007).
9. Lenox, L.E., Perry, J.M. & Paulson, R.F. BMP4 and Madh5 regulate the erythroid response to acute anemia. Blood 105, 2741-2748 (2005).
10. Porayette, P. & Paulson, R.F. BMP4/Smad5 dependent stress erythropoiesis is required for the expansion of erythroid progenitors during fetal development. Dev. Biol. 317, 24-35 (2008).
11. Millot, S. et al. Erythropoietin stimulates spleen BMP4-dependent stress erythropoiesis and partially corrects anemia in a mouse model of generalized inflammation. Blood 116, 6072-6081 (2010).
12. Bessis, M. [Erythroblastic island, functional unity of bone marrow.]. Rev. Hematol. 13, 8-11 (1958).
13. Chasis, J.A. & Mohandas, N. Erythroblastic islands: niches for erythropoiesis. Blood 112, 470-478 (2008).
14. Soni, S. et al. Absence of erythroblast macrophage protein (Emp) leads to failure of erythroblast nuclear extrusion. J. Biol. Chem. 281, 20181-20189 (2006).
15. Yoshida, H. et al. Phosphatidylserine-dependent engulfment by macrophages of nuclei from erythroid precursor cells. Nature 437, 754-758 (2005).
16. Seki, M. & Shirasawa, H. Role of the reticular cells during maturation process of the erythroblast. 3. The fate of phagocytized nucleus. Acta Pathol. Jpn. 15, 387-405 (1965).
17. Sadahira, Y. et al. Impaired splenic erythropoiesis in phlebotomized mice injected with CL2MDP-liposome: an experimental model for studying the role of stromal macrophages in erythropoiesis. J. Leukoc. Biol. 68, 464-470 (2000).
18. Liu, X.S. et al. Disruption of palladin leads to defects in definitive erythropoiesis by interfering with erythroblastic island formation in mouse fetal liver. Blood 110, 870-876 (2007).
19. Giuliani, A.L. et al. Aging of red blood cells and impaired erythropoiesis following prolonged administration of dichloromethylene diphosphonate containing liposomes in rats. Eur. J. Haematol. 75, 406-416 (2005).
20. Hanspal, M. & Hanspal, J.S. The association of erythroblasts with macrophages promotes erythroid proliferation and maturation: a 30-kD heparin-binding protein is involved in this contact. Blood 84, 3494-3504 (1994).
21. Giuliani, A.L. et al. Changes in murine bone marrow macrophages and erythroid burst-forming cells following the intravenous injection of liposome-encapsulated dichloromethylene diphosphonate (Cl2MDP). Eur. J. Haematol. 66, 221-229 (2001).
22. Rhodes, M.M., Kopsombut, P., Bondurant, M.C., Price, J.O. & Koury, M.J. Adherence to macrophages in erythroblastic islands enhances erythroblast proliferation and increases erythrocyte production by a different mechanism than erythropoietin. Blood 111, 1700-1708 (2008).
23. Fabriek, B.O. et al. The macrophage CD163 surface glycoprotein is an erythroblast adhesion receptor. Blood 109, 5223-5229 (2007).
24. Ulyanova, T., Jiang, Y., Padilla, S., Nakamoto, B. & Papayannopoulou, T. Combinatorial and distinct roles of α and α integrins in stress erythropoiesis in mice. Blood 117, 975-985 (2011).
25. Angelillo-Scherrer, A. et al. Role of Gas6 in erythropoiesis and anemia in mice. J. Clin. Invest. 118, 583-596 (2008).
26. Paulson, R.F., Shi, L. & Wu, D.C. Stress erythropoiesis: new signals and new stress progenitor cells. Curr. Opin. Hematol. 18, 139-145 (2011).
27. Ramos, P. et al. Enhanced erythropoiesis in Hfe-KO mice indicates a role for Hfe in the modulation of erythroid iron homeostasis. Blood 117, 1379-1389 (2011).
28. Longmore, G.D. A unique role for Stat5 in recovery from acute anemia. J. Clin. Invest. 116, 626-628 (2006).
29. Menon, M.P. et al. Signals for stress erythropoiesis are integrated via an erythropoietin receptor-phosphotyrosine-343-Stat5 axis. J. Clin. Invest. 116, 683-694 (2006).
30. Socolovsky, M. Molecular insights into stress erythropoiesis. Curr. Opin. Hematol. 14, 215-224 (2007).
31. Vemula, S. et al. Essential role for focal adhesion kinase in regulating stress hematopoiesis. Blood 116, 4103-4115 (2010).
32. Baxter, E.J. et al. Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders. Lancet 365, 1054-1061 (2005).
33. James, C. et al. A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature 434, 1144-1148 (2005).
34. Kralovics, R. et al. A gain-of-function mutation of JAK2 in myeloproliferative disorders. N. Engl. J. Med. 352, 1779-1790 (2005).
35. Levine, R.L. et al. Activating mutation in the tyrosine kinase JAK2 in polycythemia vera, essential thrombocythemia, and myeloid metaplasia with myelofibrosis. Cancer Cell 7, 387-397 (2005).
36. Levine, R.L. & Gilliland, D.G. Myeloproliferative disorders. Blood 112, 2190-2198 (2008).
37. Ginzburg, Y. & Rivella, S. β-thalassemia: a model for elucidating the dynamic regulation of ineffective erythropoiesis and iron metabolism. Blood 118, 4321-4330 (2011).
38. Rivella, S. Ineffective erythropoiesis and thalassemias. Curr. Opin. Hematol. 16, 187-194 (2009).
39. Libani, I.V. et al. Decreased differentiation of erythroid cells exacerbates ineffective erythropoiesis in β-thalassemia. Blood 112, 875-885 (2008).
40. Mullally, A. et al. Physiological Jak2V617F expression causes a lethal myeloproliferative neoplasm with differential effects on hematopoietic stem and progenitor cells. Cancer Cell 17, 584-596 (2010).
41. Tiedt, R. et al. Ratio of mutant JAK2-V617F to wild-type Jak2 determines the MPD phenotypes in transgenic mice. Blood 111, 3931-3940 (2008).
42. Pardanani, A. et al. TG101209, a small molecule JAK2-selective kinase inhibitor potently inhibits myeloproliferative disorder-associated JAK2V617F and MPLW515L/K mutations. Leukemia 21, 1658-1668 (2007).
43. Santos, F.P. & Verstovsek, S. JAK2 inhibitors: what's the true therapeutic potential? Blood Rev. 25, 53-63 (2011).
44. Verstovsek, S. Therapeutic potential of JAK2 inhibitors. Hematology Am. Soc. Hematol. Educ. Program 2009, 636-642 (2009).
45. Melchiori, L., Gardenghi, S. & Rivella, S. βeta-thalassemia: hiJAKing ineffective erythropoiesis and iron overload. Adv. Hematol. 2010, 938640 (2010).
46. Van Rooijen, N. & Sanders, A. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J. Immunol. Methods 174, 83-93 (1994).
47. Chow, A. et al. Bone marrow CD169+ macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche. J. Exp. Med. 208, 261-271 (2011).
48. Sadahira, Y., Yoshino, T. & Monobe, Y. Very late activation antigen 4-vascular cell adhesion molecule 1 interaction is involved in the formation of erythroblastic islands. J. Exp. Med. 181, 411-415 (1995).
49. Hentze, M.W., Muckenthaler, M.U., Galy, B. & Camaschella, C. Two to tango: regulation of mammalian iron metabolism. Cell 142, 24-38 (2010).
50. Ciavatta, D.J., Ryan, T.M., Farmer, S.C. & Townes, T.M. Mouse model of human β zero thalassemia: targeted deletion of the mouse β maj-and β min-globin genes in embryonic stem cells. Proc. Natl. Acad. Sci. USA 92, 9259-9263 (1995).
51. Gardenghi, S. et al. Hepcidin as a therapeutic tool to limit iron overload and improve anemia in β-thalassemic mice. J. Clin. Invest. 120, 4466-4477 (2010).
52. Li, H. et al. Transferrin therapy ameliorates disease in β-thalassemic mice. Nat. Med. 16, 177-182 (2010).
53. Ramos, E. et al. Evidence for distinct pathways of hepcidin regulation by acute and chronic iron loading in mice. Hepatology 53, 1333-1341 (2011).
54. Ramos, E. et al. Minihepcidins prevent iron overload in a hepcidin-deficient mouse model of severe hemochromatosis. Blood 120, 3829-3836 (2012).
55. Pollard, J.W. Trophic macrophages in development and disease. Nat. Rev. Immunol. 9, 259-270 (2009).
56. Richmond, T.D., Chohan, M. & Barber, D.L. Turning cells red: signal transduction mediated by erythropoietin. Trends Cell Biol. 15, 146-155 (2005).
57. Chow, A. et al. CD169+ macrophages provide a niche promoting erythropoiesis under homeostasis and stress. Nat. Med. advance online publication, doi:10.1038/nm.3057 (17 March 2013).
58. de Boer, J. et al. Transgenic mice with hematopoietic and lymphoid specific expression of Cre. Eur. J. Immunol. 33, 314-325 (2003).
59. Lesbordes-Brion, J.C. et al. Targeted disruption of the hepcidin 1 gene results in severe hemochromatosis. Blood 108, 1402-1405 (2006).
60. Gardenghi, S. et al. Ineffective erythropoiesis in β-thalassemia is characterized by increased iron absorption mediated by down-regulation of hepcidin and up-regulation of ferroportin. Blood 109, 5027-5035 (2007).
61. Sorensen, S., Rubin, E., Polster, H., Mohandas, N. & Schrier, S. The role of membrane skeletal-associated α-globin in the pathophysiology of β-thalassemia. Blood 75, 1333-1336 (1990).
62. Kong, Y. et al. Loss of α-hemoglobin-stabilizing protein impairs erythropoiesis and exacerbates β-thalassemia. J. Clin. Invest. 114, 1457-1466 (2004).