Pretransplant CSF-1 therapy expands recipient macrophages and ameliorates GVHD after allogeneic hematopoietic cell transplantation

Journal of Experimental Medicine

Volumn 208, Issue 5, 2011, Pages 1069-1082

  Hashimoto, Daigo ^a   Chow, Andrew ^a,d   Greter, Melanie ^a   Saenger, Yvonne ^a   Kwan, Wing Hong ^a   Leboeuf, Marylene ^a   Ginhoux, Florent ^a,b   Ochando, Jordi C ^c   Kunisaki, Yuya ^d   van Rooijen, Nico ^e   Liu, Chen ^f   Teshima, Takanori ^g   Heeger, Peter S ^a   Stanley, E Richard ^d   Frenette, Paul S ^d   Merad, Miriam ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b AGENCY FOR SCIENCE   (Singapore)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^e VU UNIVERSITY AMSTERDAM   (Netherlands)

^f UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^g KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA COLONY STIMULATING FACTOR 1 RECEPTOR; CD47 ANTIGEN; COLONY STIMULATING FACTOR 1; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL EXPANSION; CELLULAR IMMUNITY; CONTROLLED STUDY; DONOR; ENGRAFTMENT; GRAFT VERSUS HOST REACTION; IRRADIATION; LYMPHOCYTE PROLIFERATION; MACROPHAGE; MORBIDITY; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECIPIENT; T LYMPHOCYTE;

ANIMALS; ANTIGEN-PRESENTING CELLS; FEMALE; GRAFT VS HOST DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; T-LYMPHOCYTES; TRANSPLANTATION, HOMOLOGOUS;

EID: 79956068261     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20101709     Document Type: Article

References (73)

1. Abe, M., J. Cheng, J. Qi, R.M. Glaser, A.D. Thall, M. Sykes, and Y.-G. Yang. 2002. Elimination of porcine hemopoietic cells by macrophages in mice. J. Immunol. 168:621-628.
2. Allavena, P., A. Sica, C. Garlanda, and A. Mantovani. 2008. The Yin-Yang of tumor-associated macrophages in neoplastic progression and immune surveillance. Immunol. Rev. 222:155-161.
3. Alyea, E., E. Weller, R. Schlossman, C. Canning, I. Webb, D. Doss, P. Mauch, K. Marcus, D. Fisher, A. Freeman, et al. 2001. T-cell- depleted allogeneic bone marrow transplantation followed by donor lymphocyte infusion in patients with multiple myeloma: induction of graft-versus-myeloma effect. Blood. 98:934-939.
4. Banovic, T., K.P. MacDonald, E.S. Morris, V. Rowe, R. Kuns, A. Don, J. Kelly, S. Ledbetter, A.D. Clouston, and G.R. Hill. 2005. TGF-beta in allogeneic stem cell transplantation: friend or foe? Blood. 106:2206- 2214.
5. Bartocci, A., D.S. Mastrogiannis, G. Migliorati, R.J. Stockert, A.W. Wolkoff, and E.R. Stanley. 1987. Macrophages specifically regulate the concentration of their own growth factor in the circulation. Proc. Natl. Acad. Sci. USA. 84:6179-6183.
6. Beilhack, A., S. Schulz, J. Baker, G.F. Beilhack, C.B. Wieland, E.I. Herman, E.M. Baker, Y.A. Cao, C.H. Contag, and R.S. Negrin. 2005. In vivo analyses of early events in acute graft-versus-host disease reveal sequential infiltration of T-cell subsets. Blood. 106:1113-1122.
7. Bishop, M.R., J.W. Hou, W.H. Wilson, S.M. Steinberg, J. Odom, K. Castro, C. Kasten-Sportes, J. Gea-Banacloche, D. Marchigiani, R. Gress, and D.H. Fowler. 2003. Establishment of early donor engraftment after reduced-intensity allogeneic hematopoietic stem cell transplantation to potentiate the graft-versus-lymphoma effect against refractory lymphomas. Biol. Blood Marrow Transplant. 9:162-169.
8. Blazar, B.R., S.L. Aukerman, and D.A. Vallera. 1992. Effect of recombinant human macrophage colony-stimulating factor in irradiated murine recipients of T-cell-depleted allogeneic or non-depleted syngeneic bone marrow transplants. Blood. 79:1636-1642.
9. Blazar, B.R., F.P. Lindberg, E. Ingulli, A. Panoskaltsis-Mortari, P.A. Oldenborg, K. Iizuka, W.M. Yokoyama, and P.A. Taylor. 2001. CD47 (integrin-associated protein) engagement of dendritic cell and macrophage counterreceptors is required to prevent the clearance of donor lymphohematopoietic cells. J. Exp. Med. 194:541-549.
10. Blazar, B.R., B.M. Carreno, A. Panoskaltsis-Mortari, L. Carter, Y. Iwai, H. Yagita, H. Nishimura, and P.A. Taylor. 2003. Blockade of programmed death-1 engagement accelerates graft-versus-host disease lethality by an IFN-gamma-dependent mechanism. J. Immunol. 171:1272-1277.
11. Bogunovic, M., F. Ginhoux, J. Helft, L. Shang, D. Hashimoto, M. Greter, K. Liu, C. Jakubzick, M.A. Ingersoll, M. Leboeuf, et al. 2009. Origin of the lamina propria dendritic cell network. Immunity. 31:513-525.
12. Burnett, S.H., E.J. Kershen, J. Zhang, L. Zeng, S.C. Straley, A.M. Kaplan, and D.A. Cohen. 2004. Conditional macrophage ablation in transgenic mice expressing a Fas-based suicide gene. J. Leukoc. Biol. 75:612-623.
13. Cecchini, M.G., M.G. Dominguez, S. Mocci, A. Wetterwald, R. Felix, H. Fleisch, O. Chisholm, W. Hofstetter, J.W. Pollard, and E.R. Stanley. 1994. Role of colony stimulating factor-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse. Development. 120:1357-1372.
14. Chitu, V., and E.R. Stanley. 2006. Colony-stimulating factor-1 in immunity and inflammation. Curr. Opin. Immunol. 18:39-48.
15. Collin, M.P., M. Bogunovic, and M. Merad. 2007. DC homeostasis in hematopoietic stem cell transplantation. Cytotherapy. 9:521-531.
16. Cooke, K.R., L. Kobzik, T.R. Martin, J. Brewer, J. Delmonte Jr., J.M. Crawford, and J.L. Ferrara. 1996. An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation: I. The roles of minor H antigens and endotoxin. Blood. 88:3230-3239.
17. Dai, X.M., G.R. Ryan, A.J. Hapel, M.G. Dominguez, R.G. Russell, S. Kapp, V. Sylvestre, and E.R. Stanley. 2002. Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood. 99:111-120.
18. Dreger, P., R. Brand, J. Hansz, D. Milligan, P. Corradini, J. Finke, G.L. Deliliers, R. Martino, N. Russell, A. Van Biezen, et al; Chronic Leukemia Working Party of the EBMT. 2003. Treatment-related mortality and graft-versus-leukemia activity after allogeneic stem cell transplantation for chronic lymphocytic leukemia using intensity-reduced conditioning. Leukemia. 17:841-848.
19. Drobyski, W.R., C.A. Keever, G.A. Hanson, T. McAuliffe, and O.W. Griffith. 1994. Inhibition of nitric oxide production is associated with enhanced weight loss, decreased survival, and impaired alloengraftment in mice undergoing graft-versus-host disease after bone marrow transplantation. Blood. 84:2363-2373.
20. Duffner, U.A., Y. Maeda, K.R. Cooke, P. Reddy, R. Ordemann, C. Liu, J.L. Ferrara, and T. Teshima. 2004. Host dendritic cells alone are sufficient to initiate acute graft-versus-host disease. J. Immunol. 172:7393-7398.
21. Ehlenberger, A.G., and V. Nussenzweig. 1977. The role of membrane receptors for C3b and C3d in phagocytosis. J. Exp. Med. 145:357-371.
22. Facon, T., A. Janin, M.P. Noel, and J.P. Jouet. 1995. Involvement of macrophages in lethal forms of graft-versus-host disease. Lancet. 345:392.
23. Felix, R., M.G. Cecchini, and H. Fleisch. 1990. Macrophage colony stimulating factor restores in vivo bone resorption in the op/op osteopetrotic mouse. Endocrinology. 127:2592-2594.
24. Fraser, C.C., B.P. Chen, S. Webb, N. van Rooijen, and G. Kraal. 1995. Circulation of human hematopoietic cells in severe combined immunodeficient mice after Cl2MDP-liposome-mediated macrophage depletion. Blood. 86:183-192.
25. Garcia, M.R., L. Ledgerwood, Y. Yang, J. Xu, G. Lal, B. Burrell, G. Ma, D. Hashimoto, Y. Li, P. Boros, et al. 2010. Monocytic suppressive cells mediate cardiovascular transplantation tolerance in mice. J. Clin. Invest. 120:2486-2496.
26. Ginhoux, F., F. Tacke, V. Angeli, M. Bogunovic, M. Loubeau, X.M. Dai, E.R. Stanley, G.J. Randolph, and M. Merad. 2006. Langerhans cells arise from monocytes in vivo. Nat. Immunol. 7:265-273.
27. + dendritic cells survey the skin in the steady state. J. Exp. Med. 204:3133-3146.
28. + DCs. J. Exp. Med. 206:3115- 3130.
29. Haniffa, M., F. Ginhoux, X.N. Wang, V. Bigley, M. Abel, I. Dimmick, S. Bullock, M. Grisotto, T. Booth, P. Taub, et al. 2009. Differential rates of replacement of human dermal dendritic cells and macrophages during hematopoietic stem cell transplantation. J. Exp. Med. 206:371-385.
30. Helft, J., F. Ginhoux, M. Bogunovic, and M. Merad. 2010. Origin and functional heterogeneity of non-lymphoid tissue dendritic cells in mice. Immunol. Rev. 234:55-75.
31. Hill, G.R., J.M. Crawford, K.R. Cooke, Y.S. Brinson, L. Pan, and J.L. Ferrara. 1997. Total body irradiation and acute graft-versus-host disease: the role of gastrointestinal damage and inflammatory cytokines. Blood. 90:3204-3213.
32. Hill, G.R., K.R. Cooke, T. Teshima, J.M. Crawford, J.C. Keith Jr., Y.S. Brinson, D. Bungard, and J.L. Ferrara. 1998. Interleukin-11 promotes T cell polarization and prevents acute graft-versus-host disease after allogeneic bone marrow transplantation. J. Clin. Invest. 102:115-123.
33. Hume, D.A., P. Pavli, R.E. Donahue, and I.J. Fidler. 1988. The effect of human recombinant macrophage colony-stimulating factor (CSF-1) on the murine mononuclear phagocyte system in vivo. J. Immunol. 141:3405-3409.
34. Ide, K., H. Wang, H. Tahara, J. Liu, X. Wang, T. Asahara, M. Sykes, Y.-G. Yang, and H. Ohdan. 2007. Role for CD47-SIRPalpha signaling in xenograft rejection by macrophages. Proc. Natl. Acad. Sci. USA. 104:5062- 5066.
35. Jasperson, L.K., C. Bucher, A. Panoskaltsis-Mortari, A.L. Mellor, D.H. Munn, and B.R. Blazar. 2009. Inducing the tryptophan catabolic pathway, indoleamine 2,3-dioxygenase (IDO), for suppression of graft-versushost disease (GVHD) lethality. Blood. 114:5062-5070.
36. Jenq, R.R., and M.R.M. van den Brink. 2010. Allogeneic haematopoietic stem cell transplantation: individualized stem cell and immune therapy of cancer. Nat. Rev. Cancer. 10:213-221.
37. Koyama, M., D. Hashimoto, K. Aoyama, K.-I. Matsuoka, K. Karube, H. Niiro, M. Harada, M. Tanimoto, K. Akashi, and T. Teshima. 2009. Plasmacytoid dendritic cells prime alloreactive T cells to mediate graftversus-host disease as antigen-presenting cells. Blood. 113:2088-2095.
38. Krenger, W., G. Falzarano, J. Delmonte Jr., K.M. Snyder, J.C. Byon, and J.L. Ferrara. 1996. Interferon-gamma suppresses T-cell proliferation to mitogen via the nitric oxide pathway during experimental acute graftversus-host disease. Blood. 88:1113-1121.
39. Krenger, W., S. Rossi, L. Piali, and G.A. Holländer. 2000. Thymic atrophy in murine acute graft-versus-host disease is effected by impaired cell cycle progression of host pro-T and pre-T cells. Blood. 96:347-354.
40. Lin, H., E. Lee, K. Hestir, C. Leo, M. Huang, E. Bosch, R. Halenbeck, G. Wu, A. Zhou, D. Behrens, et al. 2008. Discovery of a cytokine and its receptor by functional screening of the extracellular proteome. Science. 320:807-811.
41. MacDonald, K.P.A., J.S. Palmer, S. Cronau, E. Seppanen, S. Olver, N.C. Raffelt, R. Kuns, A.R. Pettit, A. Clouston, B. Wainwright, et al. 2010. An antibody against the colony-stimulating factor 1 receptor depletes the resident subset of monocytes and tissue- and tumor-associated macrophages but does not inhibit inflammation. Blood. 116:3955-3963.
42. Maris, M.B., B.M. Sandmaier, B.E. Storer, T. Chauncey, M.J. Stuart, R.T. Maziarz, E. Agura, A.A. Langston, M. Pulsipher, R. Storb, and D.G. Maloney. 2004. Allogeneic hematopoietic cell transplantation after fludarabine and 2 Gy total body irradiation for relapsed and refractory mantle cell lymphoma. Blood. 104:3535-3542.
43. Matozaki, T., Y. Murata, H. Okazawa, and H. Ohnishi. 2009. Functions and molecular mechanisms of the CD47-SIRPalpha signalling pathway. Trends Cell Biol. 19:72-80.
44. Mempel, T.R., S.E. Henrickson, and U.H. Von Andrian. 2004. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature. 427:154-159.
45. Menke, J., Y. Iwata, W.A. Rabacal, R. Basu, Y.G. Yeung, B.D. Humphreys, T. Wada, A. Schwarting, E.R. Stanley, and V.R. Kelley. 2009. CSF-1 signals directly to renal tubular epithelial cells to mediate repair in mice. J. Clin. Invest. 119:2330-2342.
46. Merad, M., and M.G. Manz. 2009. Dendritic cell homeostasis. Blood. 113:3418-3427.
47. Merad, M., P. Hoffmann, E. Ranheim, S. Slaymaker, M.G. Manz, S.A. Lira, I. Charo, D.N. Cook, I.L. Weissman, S. Strober, and E.G. Engleman. 2004. Depletion of host Langerhans cells before transplantation of donor alloreactive T cells prevents skin graft-versus-host disease. Nat. Med. 10:510-517.
48. Mielcarek, M., P.J. Martin, W. Leisenring, M.E. Flowers, D.G. Maloney, B.M. Sandmaier, M.B. Maris, and R. Storb. 2003. Graft-versus-host disease after nonmyeloablative versus conventional hematopoietic stem cell transplantation. Blood. 102:756-762.
49. Miller, M.J., S.H. Wei, I. Parker, and M.D. Cahalan. 2002. Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science. 296:1869-1873.
50. Na, I.K., J.C. Markley, J.J. Tsai, N.L. Yim, B.J. Beattie, A.D. Klose, A.M. Holland, A. Ghosh, U.K. Rao, M.T. Stephan, et al. 2010. Concurrent visualization of trafficking, expansion, and activation of T lymphocytes and T-cell precursors in vivo. Blood. 116:e18-e25.
51. Namba, N., K. Shinagawa, N. Fujii, Y. Maeda, F. Ishimaru, K. Ikeda, T. Matsui, M. Tanimoto, and Y. Katayama. 2007. Predominant infiltration of monocytes in chronic graft-versus-host disease. Transplantation. 83:220-224.
52. Nemunaitis, J., K. Shannon-Dorcy, F.R. Appelbaum, J. Meyers, A. Owens, R. Day, D. Ando, C. O'Neill, D. Buckner, and J. Singer. 1993. Longterm follow-up of patients with invasive fungal disease who received adjunctive therapy with recombinant human macrophage colonystimulating factor. Blood. 82:1422-1427.
53. Okamoto, A., K. Fujio, N. van Rooijen, N.H. Tsuno, K. Takahashi, H. Tsurui, S. Hirose, K.B. Elkon, and K. Yamamoto. 2008. Splenic phagocytes promote responses to nucleosomes in (NZB x NZW) F1 mice. J. Immunol. 181:5264-5271.
54. Panoskaltsis-Mortari, A., A. Price, J.R. Hermanson, E. Taras, C. Lees, J.S. Serody, and B.R. Blazar. 2004. In vivo imaging of graft-versus-host-disease in mice. Blood. 103:3590-3598.
55. Pavletic, Z.S., E.R. Arrowsmith, P.J. Bierman, S.A. Goodman, J.M. Vose, S.R. Tarantolo, R.S. Stein, G. Bociek, J.P. Greer, C.D. Wu, et al. 2000. Outcome of allogeneic stem cell transplantation for B cell chronic lymphocytic leukemia. Bone Marrow Transplant. 25:717-722.
56. Peggs, K.S., S. Mackinnon, and D.C. Linch. 2005. The role of allogeneic transplantation in non-Hodgkin's lymphoma. Br. J. Haematol. 128:153- 168.
57. Pollard, J.W. 2004. Tumour-educated macrophages promote tumour progression and metastasis. Nat. Rev. Cancer. 4:71-78.
58. Rabinowe, S.N., R.J. Soiffer, J.G. Gribben, H. Daley, A.S. Freedman, J. Daley, K. Pesek, D. Neuberg, G. Pinkus, P.R. Leavitt, et al. 1993. Autologous and allogeneic bone marrow transplantation for poor prognosis patients with B-cell chronic lymphocytic leukemia. Blood. 82:1366-1376.
59. Rozemuller, H., S. Knaän-Shanzer, A. Hagenbeek, L. van Bloois, G. Storm, and A.C.M. Martens. 2004. Enhanced engraftment of human cells in RAG2/gammac double-knockout mice after treatment with CL2MDP liposomes. Exp. Hematol. 32:1118-1125.
60. Shlomchik, W.D., M.S. Couzens, C.B. Tang, J. McNiff, M.E. Robert, J. Liu, M.J. Shlomchik, and S.G. Emerson. 1999. Prevention of graft versus host disease by inactivation of host antigen-presenting cells. Science. 285:412-415.
61. Sorror, M.L., M.B. Maris, B.M. Sandmaier, B.E. Storer, M.J. Stuart, U. Hegenbart, E. Agura, T.R. Chauncey, J. Leis, M. Pulsipher, et al. 2005. Hematopoietic cell transplantation after nonmyeloablative conditioning for advanced chronic lymphocytic leukemia. J. Clin. Oncol. 23:3819- 3829.
62. Sudo, T., S. Nishikawa, M. Ogawa, H. Kataoka, N. Ohno, A. Izawa, S. Hayashi, and S. Nishikawa. 1995. Functional hierarchy of c-kit and c-fms in intramarrow production of CFU-M. Oncogene. 11:2469-2476.
63. Tacke, F., F. Ginhoux, C. Jakubzick, N. van Rooijen, M. Merad, and G.J. Randolph. 2006. Immature monocytes acquire antigens from other cells in the bone marrow and present them to T cells after maturing in the periphery. J. Exp. Med. 203:583-597.
64. Takai, T., M. Li, D. Sylvestre, R. Clynes, and J.V. Ravetch. 1994. FcR gamma chain deletion results in pleiotrophic effector cell defects. Cell. 76:519-529.
65. Takenaka, K., T.K. Prasolava, J.C.Y. Wang, S.M. Mortin-Toth, S. Khalouei, O.I. Gan, J.E. Dick, and J.S. Danska. 2007. Polymorphism in Sirpa modulates engraftment of human hematopoietic stem cells. Nat. Immunol. 8:1313-1323.
66. Teshima, T., R. Ordemann, P. Reddy, S. Gagin, C. Liu, K.R. Cooke, and J.L. Ferrara. 2002. Acute graft-versus-host disease does not require alloantigen expression on host epithelium. Nat. Med. 8:575-581.
67. van Besien, K., K.A. Sobocinski, P.A. Rowlings, S.C. Murphy, J.O. Armitage, M.R. Bishop, O.K. Chaekal, R.P. Gale, J.P. Klein, H.M. Lazarus, et al. 1998. Allogeneic bone marrow transplantation for lowgrade lymphoma. Blood. 92:1832-1836.
68. Van Rooijen, N., and A. Sanders. 1994. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J. Immunol. Methods. 174:83-93.
69. Wiktor-Jedrzejczak, W., A. Bartocci, A.W. Ferrante Jr., A. Ahmed-Ansari, K.W. Sell, J.W. Pollard, and E.R. Stanley. 1990. Total absence of colony-stimulating factor 1 in the macrophage-deficient osteopetrotic (op/ op) mouse. Proc. Natl. Acad. Sci. USA. 87:4828-4832.
70. Wynn, T.A., and L. Barron. 2010. Macrophages: master regulators of inflammation and fibrosis. Semin. Liver Dis. 30:245-257.
71. Yoshida, H., S. Hayashi, T. Kunisada, M. Ogawa, S. Nishikawa, H. Okamura, T. Sudo, L.D. Shultz, and S. Nishikawa. 1990. The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature. 345:442-444.
72. Zhang, Y., J.-P. Louboutin, J. Zhu, A.J. Rivera, and S.G. Emerson. 2002a. Preterminal host dendritic cells in irradiated mice prime CD8+ T cell-mediated acute graft-versus-host disease. J. Clin. Invest. 109: 1335-1344.
73. Zhang, Y., W.D. Shlomchik, G. Joe, J.P. Louboutin, J. Zhu, A. Rivera, D. Giannola, and S.G. Emerson. 2002b. APCs in the liver and spleen recruit activated allogeneic CD8+ T cells to elicit hepatic graft-versushost disease. J. Immunol. 169:7111-7118.