Macrophages retain hematopoietic stem cells in the spleen via VCAM-1

Journal of Experimental Medicine

Volumn 212, Issue 4, 2015, Pages 497-512

  Dutta, Partha ^a   Hoyer, Friedrich Felix ^a   Grigoryeva, Lubov S ^a   Sager, Hendrik B ^a   Leuschner, Florian ^b,c   Courties, Gabriel ^a   Borodovsky, Anna ^d   Novobrantseva, Tatiana ^d   Ruda, Vera M ^d   Fitzgerald, Kevin ^d   Iwamoto, Yoshiko ^a   Wojtkiewicz, Gregory ^a   Sun, Yuan ^a   Da Silva, Nicolas ^a   Libby, Peter ^e   Anderson, Daniel G ^f,g,h   Swirski, Filip K ^a   Weissleder, Ralph ^a   Nahrendorf, Matthias ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^c DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^d ALNYLAM PHARMACEUTICALS   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^g Massachusetts Institute of Technology Cambridge   (United States)

^h HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN; CHOLESTEROL; GAMMA INTERFERON; MESSENGER RNA; SMALL INTERFERING RNA; STEM CELL FACTOR; VASCULAR CELL ADHESION MOLECULE 1; VERY LATE ACTIVATION ANTIGEN 4; APOLIPOPROTEIN E; COLONY STIMULATING FACTOR RECEPTOR; NANOPARTICLE; SIALOADHESIN; SIGLEC1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE MARROW CELL; CARDIOVASCULAR MORTALITY; CELL COUNT; CELL CYCLE G0 PHASE; CELL CYCLE M PHASE; CELL DIFFERENTIATION; CELL MATURATION; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL DIET; CONTROLLED STUDY; EXPERIMENTAL ATHEROSCLEROSIS; EXPERIMENTAL MYOCARDIAL INFARCTION; EXTRAMEDULLARY HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; LEUKOCYTOSIS; MACROPHAGE; MOUSE; MYELOPOIESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; SPLEEN CELL; ANIMAL; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; GENE EXPRESSION REGULATION; GENETICS; HEART INFARCTION; IMMUNOLOGY; KNOCKOUT MOUSE; PATHOLOGY; RNA INTERFERENCE;

ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; GENE EXPRESSION REGULATION; HEMATOPOIESIS, EXTRAMEDULLARY; HEMATOPOIETIC STEM CELLS; MACROPHAGES; MICE; MICE, KNOCKOUT; MYELOPOIESIS; MYOCARDIAL INFARCTION; NANOPARTICLES; PLAQUE, ATHEROSCLEROTIC; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; RNA INTERFERENCE; SIALIC ACID BINDING IG-LIKE LECTIN 1; SPLEEN; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84928254121     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20141642     Document Type: Article

References (53)

1. Akinc, A., A. Zumbuehl, M. Goldberg, E.S. Leshchiner, V. Busini, N. Hossain, S.A. Bacallado, D.N. Nguyen, J. Fuller, R. Alvarez, et al. 2008. A combinatorial library of lipid-like materials for delivery of RNAi therapeutics. Nat. Biotechnol. 26:561-569. http://dx.doi.org/10.1038/nbt1402
2. Assmus, B., M. Iwasaki, V. Schächinger, T. Roexe, M. Koyanagi, K. Iekushi, Q. Xu, T. Tonn, E. Seifried, S. Liebner, et al. 2012. Acute myocardial infarction activates progenitor cells and increases Wnt signalling in the bone marrow. Eur. Heart J. 33:1911-1919. http://dx.doi.org/10.1093/eurheartj/ehr388
3. Auffray, C., M.H. Sieweke, and F. Geissmann. 2009. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 27:669-692. http://dx.doi.org/10.1146/annurev.immunol.021908.132557
4. Chow, A., D. Lucas, A. Hidalgo, S. Méndez-Ferrer, D. Hashimoto, C. Scheiermann, M. Battista, M. Leboeuf, C. Prophete, N. van Rooijen, et al. 2011. 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. http://dx.doi.org/10.1084/jem20101688
5. Clinton, S.K., R. Underwood, L. Hayes, M.L. Sherman, D.W. Kufe, and P. Libby. 1992. Macrophage colony-stimulating factor gene expression in vascular cells and in experimental and human atherosclerosis. Am. J. Pathol. 140:301-316.
6. Coelho, T., D. Adams, A. Silva, P. Lozeron, P.N. Hawkins, T. Mant, J. Perez, J. Chiesa, S. Warrington, E. Tranter, et al. 2013. Safety and efficacy of RNAi therapy for transthyretin amyloidosis. N. Engl. J. Med. 369:819-829. http://dx.doi.org/10.1056/NEJMoa1208760
7. Courties, G., T. Heidt, M. Sebas, Y. Iwamoto, D. Jeon, J. Truelove, B. Tricot, G. Wojtkiewicz, P. Dutta, H.B. Sager, et al. 2014. In vivo silencing of the transcription factor IRF5 reprograms the macrophage phenotype and improves infarct healing. J. Am. Coll. Cardiol. 63:1556-1566.
8. Dahlman, J.E., C. Barnes, O.F. Khan, A. Thiriot, S. Jhunjunwala, T.E. Shaw, Y. Xing, H.B. Sager, G. Sahay, L. Speciner, et al. 2014. In vivo endothelial siRNA delivery using polymeric nanoparticles with low molecular weight. Nat. Nanotechnol. 9:648-655. http://dx.doi.org/10.1038/nnano.2014.84
9. 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. http://dx.doi.org/10.1182/blood.V99.1.111
10. Ding, L., and S.J. Morrison. 2013. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature. 495:231-235. http://dx.doi.org/10.1038/nature11885
11. Ding, L., T.L. Saunders, G. Enikolopov, and S.J. Morrison. 2012. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature. 481:457-462. http://dx.doi.org/10.1038/nature10783
12. Dutta, P., G. Courties, Y. Wei, F. Leuschner, R. Gorbatov, C.S. Robbins, Y. Iwamoto, B. Thompson, A.L. Carlson, T. Heidt, et al. 2012. Myocardial infarction accelerates atherosclerosis. Nature. 487:325-329. http://dx.doi.org/10.1038/nature11260
13. Elices, M.J., L. Osborn, Y. Takada, C. Crouse, S. Luhowskyj, M.E. Hemler, and R.R. Lobb. 1990. VCAM-1 on activated endothelium interacts with the leukocyte integrin VLA-4 at a site distinct from the VLA-4/fibronectin binding site. Cell. 60:577-584. http://dx.doi.org/10.1016/0092-8674(90)90661-W
14. Frank-Kamenetsky, M., A. Grefhorst, N.N. Anderson, T.S. Racie, B. Bramlage, A. Akinc, D. Butler, K. Charisse, R. Dorkin, Y. Fan, et al. 2008. Therapeutic RNAi targeting PCSK9 acutely lowers plasma cholesterol in rodents and LDL cholesterol in nonhuman primates. Proc. Natl. Acad. Sci. USA. 105:11915-11920. http://dx.doi.org/10.1073/pnas.0805434105
15. Hume, D.A., and K.P. MacDonald. 2012. Therapeutic applications of macrophage colony-stimulating factor-1 (CSF-1) and antagonists of CSF-1 receptor (CSF-1R) signaling. Blood. 119:1810-1820. http://dx.doi.org/10.1182/blood-2011-09-379214
16. Kiel, M.J., O.H. Yilmaz, T. Iwashita, O.H. Yilmaz, C. Terhorst, and S.J. Morrison. 2005. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 121:1109-1121. http://dx.doi.org/10.1016/j.cell.2005.05.026
17. Kim, E.J., S. Kim, H.S. Seo, and D.O. Kang. 2014. The Metabolic Activity of the Spleen and Bone Marrow in Patients with Acute Myocardial Infarction Evaluated by 18F-FDG PET Imaging. Circ Cardiovasc Imaging. http://dx.doi.org/10.1161/CIRCIMAGING.113.001093
18. Leuschner, F., P. Dutta, R. Gorbatov, T.I. Novobrantseva, J.S. Donahoe, G. Courties, K.M. Lee, J.I. Kim, J.F. Markmann, B. Marinelli, et al. 2011. Therapeutic siRNA silencing in inflammatory monocytes in mice. Nat. Biotechnol. 29:1005-1010. http://dx.doi.org/10.1038/nbt.1989
19. Leuschner, F., P.J. Rauch, T. Ueno, R. Gorbatov, B. Marinelli, W.W. Lee, P. Dutta, Y. Wei, C. Robbins, Y. Iwamoto, et al. 2012. Rapid monocyte kinetics in acute myocardial infarction are sustained by extramedullary monocytopoiesis. J. Exp. Med. 209:123-137. http://dx.doi.org/10.1084/jem.20111009
20. Love, K.T., K.P. Mahon, C.G. Levins, K.A. Whitehead, W. Querbes, J.R. Dorkin, J. Qin, W. Cantley, L.L. Qin, T. Racie, et al. 2010. Lipidlike materials for low-dose, in vivo gene silencing. Proc. Natl. Acad. Sci. USA. 107:1864-1869. http://dx.doi.org/10.1073/pnas.0910603106
21. Lu, T.T., and J.G. Cyster. 2002. Integrin-mediated long-term B cell retention in the splenic marginal zone. Science. 297:409-412. http://dx.doi.org/10.1126/science.1071632
22. Majmudar, M.D., E.J. Keliher, T. Heidt, F. Leuschner, J. Truelove, B.F. Sena, R. Gorbatov, Y. Iwamoto, P. Dutta, G. Wojtkiewicz, et al. 2013. Monocyte-directed RNAi targeting CCR2 improves infarct healing in atherosclerosis-prone mice. Circulation. 127:2038-2046. http://dx.doi.org/10.1161/CIRCULATIONAHA.112.000116
23. Massa, M., V. Rosti, M. Ferrario, R. Campanelli, I. Ramajoli, R. Rosso, G.M. De Ferrari, M. Ferlini, L. Goffredo, A. Bertoletti, et al. 2005. Increased circulating hematopoietic and endothelial progenitor cells in the early phase of acute myocardial infarction. Blood. 105:199-206. http://dx.doi.org/10.1182/blood-2004-05-1831
24. Miyake, Y., K. Asano, H. Kaise, M. Uemura, M. Nakayama, and M. Tanaka. 2007. Critical role of macrophages in the marginal zone in the suppression of immune responses to apoptotic cell-associated antigens. J. Clin. Invest. 117:2268-2278. http://dx.doi.org/10.1172/JCI31990
25. Moore, K.J., and I. Tabas. 2011. Macrophages in the pathogenesis of atherosclerosis. Cell. 145:341-355. http://dx.doi.org/10.1016/j.cell.2011.04.005
26. Murphy, A.J., M. Akhtari, S. Tolani, T. Pagler, N. Bijl, C.L. Kuo, M. Wang, M. Sanson, S. Abramowicz, C. Welch, et al. 2011. ApoE regulates hematopoietic stem cell proliferation, monocytosis, and monocyte accumulation in atherosclerotic lesions in mice. J. Clin. Invest. 121:4138-4149. http://dx.doi.org/10.1172/JCI57559
27. Nahrendorf, M., F.K. Swirski, E. Aikawa, L. Stangenberg, T. Wurdinger, J.L. Figueiredo, P. Libby, R. Weissleder, and M.J. Pittet. 2007. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J. Exp. Med. 204:3037-3047. http://dx.doi.org/10.1084/jem.20070885
28. Novobrantseva, T.I., A. Borodovsky, J. Wong, B. Klebanov, M. Zafari, K. Yucius, W. Querbes, P. Ge, V.M. Ruda, S. Milstein, et al. 2012. Systemic RNAi-mediated Gene Silencing in Nonhuman Primate and Rodent Myeloid Cells. Mol Ther Nucleic Acids 1:e4. http://dx.doi.org/10.1038/mtna.2011.3
29. Panizzi, P., F.K. Swirski, J.L. Figueiredo, P. Waterman, D.E. Sosnovik, E. Aikawa, P. Libby, M. Pittet, R. Weissleder, and M. Nahrendorf. 2010. Impaired infarct healing in atherosclerotic mice with Ly-6C(hi) monocytosis. J. Am. Coll. Cardiol. 55:1629-1638. http://dx.doi.org/10.1016/j.jacc.2009.08.089
30. Qiao, J.H., J. Tripathi, N.K. Mishra, Y. Cai, S. Tripathi, X.P. Wang, S. Imes, M.C. Fishbein, S.K. Clinton, P. Libby, et al. 1997. Role of macrophage colony-stimulating factor in atherosclerosis: studies of osteopetrotic mice. Am. J. Pathol. 150:1687-1699.
31. Rajavashisth, T., J.H. Qiao, S. Tripathi, J. Tripathi, N. Mishra, M. Hua, X.P. Wang, A. Loussararian, S. Clinton, P. Libby, and A. Lusis. 1998. Heterozygous osteopetrotic (op) mutation reduces atherosclerosis in LDL receptor-deficient mice. J. Clin. Invest. 101:2702-2710. http://dx.doi.org/10.1172/JCI119891
32. Rauch, P.J., A. Chudnovskiy, C.S. Robbins, G.F. Weber, M. Etzrodt, I. Hilgendorf, E. Tiglao, J.L. Figueiredo, Y. Iwamoto, I. Theurl, et al. 2012. Innate response activator B cells protect against microbial sepsis. Science. 335:597-601. http://dx.doi.org/10.1126/science.1215173
33. Robbins, C.S., A. Chudnovskiy, P.J. Rauch, J.L. Figueiredo, Y. Iwamoto, R. Gorbatov, M. Etzrodt, G.F. Weber, T. Ueno, N. van Rooijen, et al. 2012. Extramedullary hematopoiesis generates Ly-6C(high) monocytes that infiltrate atherosclerotic lesions. Circulation. 125:364-374. http://dx.doi.org/10.1161/CIRCULATIONAHA.111.061986
34. Robbins, C.S., I. Hilgendorf, G.F. Weber, I. Theurl, Y. Iwamoto, J.L. Figueiredo, R. Gorbatov, G.K. Sukhova, L.M. Gerhardt, D. Smyth, et al. 2013. Local proliferation dominates lesional macrophage accumulation in atherosclerosis. Nat. Med. 19:1166-1172. http://dx.doi.org/10.1038/nm.3258
35. Rosas, M., L.C. Davies, P.J. Giles, C.T. Liao, B. Kharfan, T.C. Stone, V.B. O'Donnell, D.J. Fraser, S.A. Jones, and P.R. Taylor. 2014. The transcription factor Gata6 links tissue macrophage phenotype and proliferative renewal. Science. 344:645-648. http://dx.doi.org/10.1126/science.1251414
36. Salomon, R.N., R. Underwood, M.V. Doyle, A. Wang, and P. Libby. 1992. Increased apolipoprotein E and c-fms gene expression without elevated interleukin 1 or 6 mRNA levels indicates selective activation of macrophage functions in advanced human atheroma. Proc. Natl. Acad. Sci. USA. 89:2814-2818. http://dx.doi.org/10.1073/pnas.89.7.2814
37. Scott, L.M., G.V. Priestley, and T. Papayannopoulou. 2003. Deletion of alpha4 integrins from adult hematopoietic cells reveals roles in homeostasis, regeneration, and homing. Mol. Cell. Biol. 23:9349-9360. http://dx.doi.org/10.1128/MCB.23.24.9349-9360.2003
38. Shaposhnik, Z., X. Wang, and A.J. Lusis. 2010. Arterial colony stimulating factor-1 influences atherosclerotic lesions by regulating monocyte migration and apoptosis. J. Lipid Res. 51:1962-1970. http://dx.doi.org/10.1194/jlr.M005215
39. Sugiyama, T., H. Kohara, M. Noda, and T. Nagasawa. 2006. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity. 25:977-988. http://dx.doi.org/10.1016/j.immuni.2006.10.016
40. Swirski, F.K., and M. Nahrendorf. 2013. Leukocyte behavior in atherosclerosis, myocardial infarction, and heart failure. Science. 339:161-166. http://dx.doi.org/10.1126/science.1230719
41. Swirski, F.K., P. Libby, E. Aikawa, P. Alcaide, F.W. Luscinskas, R. Weissleder, and M.J. Pittet. 2007. Ly-6Chi monocytes dominate hypercholesterolemiaassociated monocytosis and give rise to macrophages in atheromata. J. Clin. Invest. 117:195-205. http://dx.doi.org/10.1172/JCI29950
42. Swirski, F.K., M. Nahrendorf, M. Etzrodt, M. Wildgruber, V. Cortez-Retamozo, P. Panizzi, J.L. Figueiredo, R.H. Kohler, A. Chudnovskiy, P. Waterman, et al. 2009. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science. 325:612-616. http://dx.doi.org/10.1126/science.1175202
43. Tagliani, E., C. Shi, P. Nancy, C.S. Tay, E.G. Pamer, and A. Erlebacher. 2011. Coordinate regulation of tissue macrophage and dendritic cell population dynamics by CSF-1. J. Exp. Med. 208:1901-1916. http://dx.doi.org/10.1084/jem.20110866
44. Takahashi, K., S. Umeda, L.D. Shultz, S. Hayashi, and S. Nishikawa. 1994. Effects of macrophage colony-stimulating factor (M-CSF) on the development, differentiation, and maturation of marginal metallophilic macrophages and marginal zone macrophages in the spleen of osteopetrosis (op) mutant mice lacking functional M-CSF activity. J. Leukoc . Biol. 55:581-588.
45. Takizawa, H., R.R. Regoes, C.S. Boddupalli, S. Bonhoeffer, and M.G. Manz. 2011. Dynamic variation in cycling of hematopoietic stem cells in steady state and inflammation. J. Exp. Med. 208:273-284. http://dx.doi.org/10.1084/jem.20101643
46. Trogan, E., J.E. Feig, S. Dogan, G.H. Rothblat, V. Angeli, F. Tacke, G.J. Randolph, and E.A. Fisher. 2006. Gene expression changes in foam cells and the role of chemokine receptor CCR7 during atherosclerosis regression in ApoE-deficient mice. Proc. Natl. Acad. Sci. USA. 103:3781-3786. http://dx.doi.org/10.1073/pnas.0511043103
47. Tsujioka, H., T. Imanishi, H. Ikejima, A. Kuroi, S. Takarada, T. Tanimoto, H. Kitabata, K. Okochi, Y. Arita, K. Ishibashi, et al. 2009. Impact of heterogeneity of human peripheral blood monocyte subsets on myocardial salvage in patients with primary acute myocardial infarction. J. Am. Coll. Cardiol. 54:130-138. http://dx.doi.org/10.1016/j.jacc.2009.04.021
48. Ulyanova, T., L.M. Scott, G.V. Priestley, Y. Jiang, B. Nakamoto, P.A. Koni, and T. Papayannopoulou. 2005. VCAM-1 expression in adult hematopoietic and nonhematopoietic cells is controlled by tissue-inductive signals and reflects their developmental origin. Blood. 106:86-94. http://dx.doi.org/10.1182/blood-2004-09-3417
49. van Gils, J.M., M.C. Derby, L.R. Fernandes, B. Ramkhelawon, T.D. Ray, K.J. Rayner, S. Parathath, E. Distel, J.L. Feig, J.I. Alvarez-Leite, et al. 2012. The neuroimmune guidance cue netrin-1 promotes atherosclerosis by inhibiting the emigration of macrophages from plaques. Nat. Immunol. 13:136-143. http://dx.doi.org/10.1038/ni.2205
50. Wang, M., M. Subramanian, S. Abramowicz, A.J. Murphy, A. Gonen, J. Witztum, C. Welch, I. Tabas, M. Westerterp, and A.R. Tall. 2014. Interleukin-3/granulocyte macrophage colony-stimulating factor receptor promotes stem cell expansion, monocytosis, and atheroma macrophage burden in mice with hematopoietic ApoE deficiency. Arterioscler. Thromb. Vasc. Biol. 34:976-984. http://dx.doi.org/10.1161/ATVBAHA.113.303097
51. Williams, D.A., M. Rios, C. Stephens, and V.P. Patel. 1991. Fibronectin and VLA-4 in haematopoietic stem cell-microenvironment interactions. Nature. 352:438-441. http://dx.doi.org/10.1038/352438a0
52. Winkler, I.G., N.A. Sims, A.R. Pettit, V. Barbier, B. Nowlan, F. Helwani, I.J. Poulton, N. van Rooijen, K.A. Alexander, L.J. Raggatt, and J.P. Lévesque. 2010. Bone marrow macrophages maintain hematopoietic stem cell (HSC) niches and their depletion mobilizes HSCs. Blood. 116:4815-4828. http://dx.doi.org/10.1182/blood-2009-11-253534
53. Yona, S., K.W. Kim, Y. Wolf, A. Mildner, D. Varol, M. Breker, D. Strauss-Ayali, S. Viukov, M. Guilliams, A. Misharin, et al. 2013. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity. 38:79-91. http://dx.doi.org/10.1016/j.immuni.2012.12.001