Infection-induced changes in hematopoiesis

Journal of Immunology

Volumn 192, Issue 1, 2014, Pages 27-33

  Zaretsky, Arielle Glatman ^a   Engiles, Julie B ^b   Hunter, Christopher A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE; BACTERIAL INFECTION; BONE MARROW CELL; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL POPULATION; CELLULAR IMMUNITY; DISEASE ACTIVITY; DISEASE ASSOCIATION; ERYTHROPOIESIS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNE RESPONSE; INFECTION; INFLAMMATION; LYMPHOPOIESIS; MEMORY T LYMPHOCYTE; MOLECULAR DYNAMICS; NONHUMAN; PARASITOSIS; PLASMA CELL; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STEM CELL NICHE; VIRUS INFECTION;

EID: 84891124850     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302061     Document Type: Review

References (109)

1. Yang, M., G. Büsche, A. Ganser, and Z. Li. 2013. Morphology and quantitative composition of hematopoietic cells in murine bone marrow and spleen of healthy subjects. Ann. Hematol. 92: 587-594.
2. Travlos, G. S. 2006. Normal structure, function, and histology of the bone marrow. Toxicol. Pathol. 34: 548-565.
3. Tokoyoda, K., A. E. Hauser, T. Nakayama, and A. Radbruch. 2010. Organization of immunological memory by bone marrow stroma. Nat. Rev. Immunol. 10: 193-200.
4. Tokoyoda, K., T. Egawa, T. Sugiyama, B.-I. Choi, and T. Nagasawa. 2004. Cellular niches controlling B lymphocyte behavior within bone marrow during development. Immunity 20: 707-718.
5. Nombela-Arrieta, C., G. Pivarnik, B. Winkel, K. J. Canty, B. Harley, J. E. Mahoney, S. Y. Park, J. Lu, A. Protopopov, and L. E. Silberstein. 2013. Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment. Nat. Cell Biol. 15: 533-543.
6. Ding, L., T. L. Saunders, G. Enikolopov, and S. J. Morrison. 2012. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481: 457-462.
7. Krause, D. S., D. T. Scadden, and F. I. Preffer. 2013. The hematopoietic stem cell niche - home for friend and foe? Cytometry B Clin. Cytom. 84: 7-20.
8. Kondo, M. 2010. Lymphoid and myeloid lineage commitment in multipotent hematopoietic progenitors. Immunol. Rev. 238: 37-46.
9. King, K. Y., and M. A. Goodell. 2011. Inflammatory modulation of HSCs: viewing the HSC as a foundation for the immune response. Nat. Rev. Immunol. 11: 685-692.
10. Méndez-Ferrer, S., T. V. Michurina, F. Ferraro, A. R. Mazloom, B. D. Macarthur, S. A. Lira, D. T. Scadden, A. Ma'ayan, G. N. Enikolopov, and P. S. Frenette. 2010. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466: 829-834.
11. Greenbaum, A., Y. M. Hsu, R. B. Day, L. G. Schuettpelz, M. J. Christopher, J. N. Borgerding, T. Nagasawa, and D. C. Link. 2013. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 495: 227-230.
12. 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.
13. Zhang, J., C. Niu, L. Ye, H. Huang, X. He, W. G. Tong, J. Ross, J. Haug, T. Johnson, J. Q. Feng, et al. 2003. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425: 836-841.
14. Motabi, I. H., and J. F. DiPersio. 2012. Advances in stem cell mobilization. Blood Rev. 26: 267-278.
15. Ma, Q., D. Jones, and T. A. Springer. 1999. The chemokine receptor CXCR4 is required for the retention of B lineage and granulocytic precursors within the bone marrow microenvironment. Immunity 10: 463-471.
16. Ding, L., and S. J. Morrison. 2013. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 495: 231-235.
17. Shiozawa, Y., and R. S. Taichman. 2012. Getting blood from bone: an emerging understanding of the role that osteoblasts play in regulating hematopoietic stem cells within their niche. Exp. Hematol. 40: 685-694.
18. Sugiyama, T., and T. Nagasawa. 2012. Bone marrow niches for hematopoietic stem cells and immune cells. Inflamm. Allergy Drug Targets 11: 201-206.
19. Honczarenko, M., R. S. Douglas, C. Mathias, B. Lee, M. Z. Ratajczak, and L. E. Silberstein. 1999. SDF-1 responsiveness does not correlate with CXCR4 expression levels of developing human bone marrow B cells. Blood 94: 2990-2998.
20. Rettig, M. P., G. Ansstas, and J. F. DiPersio. 2012. Mobilization of hematopoietic stem and progenitor cells using inhibitors of CXCR4 and VLA-4. Leukemia 26: 34-53.
21. Villeval, J. L., A. Gearing, and D. Metcalf. 1990. Changes in hemopoietic and regulator levels in mice during fatal or nonfatal malarial infections. II. Nonerythroid populations. Exp. Parasitol. 71: 375-385.
22. Villeval, J. L., A. Lew, and D. Metcalf. 1990. Changes in hemopoietic and regulator levels in mice during fatal or nonfatal malarial infections. I. Erythropoietic populations. Exp. Parasitol. 71: 364-374.
23. Petakov, M., N. Stojanović, G. Jovcić, D. Bugarski, V. Todorović, and O. Djurković-Djaković. 2002. Hematopoiesis during acute Toxoplasma gondii infection in mice. Haematologia (Budap.) 32: 439-455.
24. Chou, D. B., B. Sworder, N. Bouladoux, C. N. Roy, A. M. Uchida, M. Grigg, P. G. Robey, and Y. Belkaid. 2012. Stromal-derived IL-6 alters the balance of myeloerythroid progenitors during Toxoplasma gondii infection. J. Leukoc. Biol. 92: 123-131.
25. Shi, X., P. Zhang, G. D. Sempowski, and J. E. Shellito. 2011. Thymopoietic and bone marrow response to murine Pneumocystis pneumonia. Infect. Immun. 79: 2031-2042.
26. Belyaev, N. N., D. E. Brown, A. I. Diaz, A. Rae, W. Jarra, J. Thompson, J. Langhorne, and A. J. Potocnik. 2010. Induction of an IL7-R(+)c-Kit(hi) myelolymphoid progenitor critically dependent on IFN-gamma signaling during acute malaria. Nat. Immunol. 11: 477-485.
27. Singh, P., Y. Yao, A. Weliver, H. E. Broxmeyer, S. C. Hong, and C. H. Chang. 2008. Vaccinia virus infection modulates the hematopoietic cell compartments in the bone marrow. Stem Cells 26: 1009-1016.
28. Yáñez, A., C. Murciano, J. E. O'Connor, D. Gozalbo, and M. L. Gil. 2009. Candida albicans triggers proliferation and differentiation of hematopoietic stem and progenitor cells by a MyD88-dependent signaling. Microbes Infect. 11: 531-535.
29. Zhang, P., S. Nelson, G. J. Bagby, R. Siggins, II, J. E. Shellito, and D. A. Welsh. 2008. The lineage-c-Kit+Sca-1+ cell response to Escherichia coli bacteremia in Balb/c mice. Stem Cells 26: 1778-1786.
30. Scumpia, P., K. Kelly-Scumpia, M. Delano, J. Weinstein, A. Cuenca, S. Al-Quran, I. Bovio, S. Akira, Y. Kumagai, and L. Moldawer. 2010. Cutting edge: bacterial The Journal of Immunology 31 Downloaded from http://www.jimmunol.org/ at Elsevier BV on December 26, 2013 infection induces hematopoietic stem and progenitor cell expansion in the absence of TLR signaling. J. Immunol. 184: 2247-2251.
31. Glatman Zaretsky, A., J. S. Silver, M. Siwicki, A. Durham, C. F. Ware, and C. A. Hunter. 2012. Infection with Toxoplasma gondii alters lymphotoxin expression associated with changes in splenic architecture. Infect. Immun. 80: 3602-3610.
32. MacNamara, K. C., R. Racine, M. Chatterjee, D. Borjesson, and G. M. Winslow. 2009. Diminished hematopoietic activity associated with alterations in innate and adaptive immunity in a mouse model of human monocytic ehrlichiosis. Infect. Immun. 77: 4061-4069.
33. MacNamara, K. C., M. Jones, O. Martin, and G. M. Winslow. 2011. Transient activation of hematopoietic stem and progenitor cells by IFNg during acute bacterial infection. PLoS ONE 6: e28669.
34. Das, B., S. S. Kashino, I. Pulu, D. Kalita, V. Swami, H. Yeger, D. W. Felsher, and A. Campos-Neto. 2013. CD271(+) bone marrow mesenchymal stem cells may provide a niche for dormant Mycobacterium tuberculosis. Sci. Transl. Med 5: 170ra113.
35. Bro-Jorgensen, K., and M. Volkert. 1972. Haemopoietic defects in mice infected with lymphocytic choriomeningitis virus. 1. The enhanced x-ray sensitivity of virus infected mice. Acta Pathol. Microbiol. Scand. B Microbiol. Immunol. 80: 845-852.
36. Petursson, S. R., P. A. Chervenick, and B. Wu. 1984. Megakaryocytopoiesis and granulopoiesis after murine cytomegalovirus infection. J. Lab. Clin. Med. 104: 381-390.
37. Ferenczy, M. W., L. J. Marshall, C. D. Nelson, W. J. Atwood, A. Nath, K. Khalili, and E. O. Major. 2012. Molecular biology, epidemiology, and pathogenesis of progressive multifocal leukoencephalopathy, the JC virus-induced demyelinating disease of the human brain. Clin. Microbiol. Rev. 25: 471-506.
38. Jing, D., U. Oelschlaegel, R. Ordemann, K. Hölig, G. Ehninger, H. Reichmann, T. Ziemssen, and M. Bornhäuser. 2010. CD49d blockade by natalizumab in patients with multiple sclerosis affects steady-state hematopoiesis and mobilizes progenitors with a distinct phenotype and function. Bone Marrow Transplant. 45: 1489-1496.
39. Apperley, J. F., C. Dowding, J. Hibbin, J. Buiter, E. Matutes, P. J. Sissons, M. Gordon, and J. M. Goldman. 1989. The effect of cytomegalovirus on hemopoiesis: in vitro evidence for selective infection of marrow stromal cells. Exp. Hematol. 17: 38-45.
40. Ganser, A., O. G. Ottmann, H. von Briesen, B. Völkers, H. Rübsamen-Waigmann, and D. Hoelzer. 1990. Changes in the haematopoietic progenitor cell compartment in the acquired immunodeficiency syndrome. Res. Virol. 141: 185-193.
41. Isgrò, A., I. Mezzaroma, A. Aiuti, L. De Vita, F. Franchi, F. Pandolfi, C. Alario, F. Ficara, E. Riva, G. Antonelli, and F. Aiuti. 2000. Recovery of hematopoietic activity in bone marrow from human immunodeficiency virus type 1-infected patients during highly active antiretroviral therapy. AIDS Res. Hum. Retroviruses 16: 1471-1479.
42. Thiebot, H., B. Vaslin, S. Derdouch, J. M. Bertho, F. Mouthon, S. Prost, G. Gras, P. Ducouret, D. Dormont, and R. Le Grand. 2005. Impact of bone marrow hematopoiesis failure on T-cell generation during pathogenic simian immunodeficiency virus infection in macaques. Blood 105: 2403-2409.
43. Thomsen, A. R., P. Pisa, K. Bro-Jørgensen, and R. Kiessling. 1986. Mechanisms of lymphocytic choriomeningitis virus-induced hemopoietic dysfunction. J. Virol. 59: 428-433.
44. Boiko, J. R., and L. Borghesi. 2012. Hematopoiesis sculpted by pathogens: Tolllike receptors and inflammatory mediators directly activate stem cells. Cytokine 57: 1-8.
45. Ciriza, J., H. Thompson, R. Petrosian, J. O. Manilay, and M. E. García-Ojeda. 2013. The migration of hematopoietic progenitors from the fetal liver to the fetal bone marrow: lessons learned and possible clinical applications. Exp. Hematol. 41: 411-423.
46. Nagai, Y., K. P. Garrett, S. Ohta, U. Bahrun, T. Kouro, S. Akira, K. Takatsu, and P. W. Kincade. 2006. Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity 24: 801-812.
47. Welner, R. S., R. Pelayo, Y. Nagai, K. P. Garrett, T. R. Wuest, D. J. Carr, L. A. Borghesi, M. A. Farrar, and P. W. Kincade. 2008. Lymphoid precursors are directed to produce dendritic cells as a result of TLR9 ligation during herpes infection. Blood 112: 3753-3761.
48. Stein, B. L. 2012. The anemia of inflammation. J. Clin. Rheumatol. 18: 437-442.
49. Nishimura, K., H. Nakaya, H. Nakagawa, S. Matsuo, Y. Ohnishi, and S. Yamasaki. 2011. Effect of Trypanosoma brucei brucei on erythropoiesis in infected rats. J. Parasitol. 97: 88-93.
50. Hunfeld, K. P., A. Hildebrandt, and J. S. Gray. 2008. Babesiosis: recent insights into an ancient disease. Int. J. Parasitol. 38: 1219-1237.
51. Akinosoglou, K. S., E. E. Solomou, and C. A. Gogos. 2012. Malaria: a haematological disease. Hematology 17: 106-114.
52. Mullarky, I. K., F. M. Szaba, L. W. Kummer, L. B. Wilhelm, M. A. Parent, L. L. Johnson, and S. T. Smiley. 2007. Gamma interferon suppresses erythropoiesis via interleukin-15. Infect. Immun. 75: 2630-2633.
53. Hartmann, D. W., M. A. Entringer, W. A. Robinson, M. L. Vasil, C. J. Drebing, N. J. Morton, and L. True. 1981. Regulation of granulopoiesis and distribution of granulocytes in early phase of bacterial infection. J. Cell. Physiol. 109: 17-24.
54. Mungyer, G., L. G. Poels, C. Jerusalem, and R. Jerusalem. 1983. Plasmodium berghei: influence on granulopoiesis and macrophage production in BALB/c mice. Exp. Parasitol. 56: 266-276.
55. Ojok, L., I. Kaeufer-Weiss, and E. Weiss. 2001. Bone marrow response to acute and chronic Trypanosoma congolense infection in multimammate rats (Mastomys coucha). J. Comp. Pathol. 124: 149-158.
56. Van Ginderachter, J. A., A. Beschin, P. De Baetselier, and G. Raes. 2010. Myeloid-derived suppressor cells in parasitic infections. Eur. J. Immunol. 40: 2976-2985.
57. Siracusa, M. C., S. A. Saenz, D. A. Hill, B. S. Kim, M. B. Headley, T. A. Doering, E. J. Wherry, H. K. Jessup, L. A. Siegel, T. Kambayashi, et al. 2011. TSLP promotes interleukin-3-independent basophil haematopoiesis and type 2 inflammation. Nature 477: 229-233.
58. Demetri, G. D., and J. D. Griffin. 1991. Granulocyte colony-stimulating factor and its receptor. Blood 78: 2791-2808.
59. Lieschke, G. J., D. Grail, G. Hodgson, D. Metcalf, E. Stanley, C. Cheers, K. J. Fowler, S. Basu, Y. F. Zhan, and A. R. Dunn. 1994. Mice lacking granulocyte colony-stimulating factor have chronic neutropenia, granulocyte and macrophage progenitor cell deficiency, and impaired neutrophil mobilization. Blood 84: 1737-1746.
60. Hirai, H., P. Zhang, T. Dayaram, C. J. Hetherington, S. Mizuno, J. Imanishi, K. Akashi, and D. G. Tenen. 2006. C/EBPbeta is required for "emergency" granulopoiesis. Nat. Immunol. 7: 732-739.
61. Panopoulos, A. D., L. Zhang, J. W. Snow, D. M. Jones, A. M. Smith, K. C. El Kasmi, F. Liu, M. A. Goldsmith, D. C. Link, P. J. Murray, and S. S. Watowich. 2006. STAT3 governs distinct pathways in emergency granulopoiesis and mature neutrophils. Blood 108: 3682-3690.
62. Cain, D. W., P. B. Snowden, G. D. Sempowski, and G. Kelsoe. 2011. Inflammation triggers emergency granulopoiesis through a density-dependent feedback mechanism. PLoS ONE 6: e19957.
63. 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.
64. Serbina, N. V., T. Jia, T. M. Hohl, and E. G. Pamer. 2008. Monocyte-mediated defense against microbial pathogens. Annu. Rev. Immunol. 26: 421-452.
65. Robben, P. M., M. LaRegina, W. A. Kuziel, and L. D. Sibley. 2005. Recruitment of Gr-1+ monocytes is essential for control of acute toxoplasmosis. J. Exp. Med. 201: 1761-1769.
66. Kurihara, T., G. Warr, J. Loy, and R. Bravo. 1997. Defects in macrophage recruitment and host defense in mice lacking the CCR2 chemokine receptor. J. Exp. Med. 186: 1757-1762.
67. Serbina, N. V., and E. G. Pamer. 2006. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat. Immunol. 7: 311-317.
68. de Bruin, A. M., S. F. Libregts, M. Valkhof, L. Boon, I. P. Touw, and M. A. Nolte. 2012. IFNg induces monopoiesis and inhibits neutrophil development during inflammation. Blood 119: 1543-1554.
69. Bockstal, V., P. Guirnalda, G. Caljon, R. Goenka, J. C. Telfer, D. Frenkel, M. Radwanska, S. Magez, and S. J. Black. 2011. T. brucei infection reduces B lymphopoiesis in bone marrow and truncates compensatory splenic lymphopoiesis through transitional B-cell apoptosis. PLoS Pathog. 7: e1002089.
70. Castro-Eguiluz, D., R. Pelayo, V. Rosales-Garcia, R. Rosales-Reyes, C. Alpuche-Aranda, and V. Ortiz-Navarrete. 2009. B cell precursors are targets for Salmonella infection. Microb. Pathog. 47: 52-56.
71. Borrow, P., S. Hou, S. Gloster, M. Ashton, and L. Hyland. 2005. Virus infectionassociated bone marrow B cell depletion and impairment of humoral immunity to heterologous infection mediated by TNF-alpha/LTalpha. Eur. J. Immunol. 35: 524-532.
72. Sedger, L. M., S. Hou, S. R. Osvath, M. B. Glaccum, J. J. Peschon, N. van Rooijen, and L. Hyland. 2002. Bone marrow B cell apoptosis during in vivo influenza virus infection requires TNF-alpha and lymphotoxin-alpha. J. Immunol. 169: 6193-6201.
73. Jyonouchi, H., P. W. Kincade, and R. A. Good. 1981. Immunosuppression of marrow B lymphocytes by administration of Corynebacterium parvum in mice. J. Immunol. 127: 2502-2507.
74. Nagaoka, H., G. Gonzalez-Aseguinolaza, M. Tsuji, and M. C. Nussenzweig. 2000. Immunization and infection change the number of recombination activating gene (RAG)-expressing B cells in the periphery by altering immature lymphocyte production. J. Exp. Med. 191: 2113-2120.
75. Ueda, Y., M. Kondo, and G. Kelsoe. 2005. Inflammation and the reciprocal production of granulocytes and lymphocytes in bone marrow. J. Exp. Med. 201: 1771-1780.
76. Ueda, Y., K. Yang, S. J. Foster, M. Kondo, and G. Kelsoe. 2004. Inflammation controls B lymphopoiesis by regulating chemokine CXCL12 expression. J. Exp. Med. 199: 47-58.
77. O'Connor, B. P., V. S. Raman, L. D. Erickson, W. J. Cook, L. K. Weaver, C. Ahonen, L. L. Lin, G. T. Mantchev, R. J. Bram, and R. J. Noelle. 2004. BCMA is essential for the survival of long-lived bone marrow plasma cells. J. Exp. Med. 199: 91-98.
78. Chu, V. T., and C. Berek. 2013. The establishment of the plasma cell survival niche in the bone marrow. Immunol. Rev. 251: 177-188.
79. Chu, V. T., A. Fröhlich, G. Steinhauser, T. Scheel, T. Roch, S. Fillatreau, J. J. Lee, M. Löhning, and C. Berek. 2011. Eosinophils are required for the maintenance of plasma cells in the bone marrow. Nat. Immunol. 12: 151-159.
80. Rodriguez Gomez, M., Y. Talke, N. Goebel, F. Hermann, B. Reich, and M. Mack. 2010. Basophils support the survival of plasma cells in mice. J. Immunol. 185: 7180-7185.
81. Winter, O., K. Moser, E. Mohr, D. Zotos, H. Kaminski, M. Szyska, K. Roth, D. M. Wong, C. Dame, D. M. Tarlinton, et al. 2010. Megakaryocytes constitute a functional component of a plasma cell niche in the bone marrow. Blood 116: 1867-1875.
82. Slifka, M. K., R. Antia, J. K. Whitmire, and R. Ahmed. 1998. Humoral immunity due to long-lived plasma cells. Immunity 8: 363-372.
83. Manz, R. A., A. Thiel, and A. Radbruch. 1997. Lifetime of plasma cells in the bone marrow. Nature 388: 133-134.
84. Tokoyoda, K., and A. Radbruch. 2012. Signals controlling rest and reactivation of T helper memory lymphocytes in bone marrow. Cell. Mol. Life Sci. 69: 1609-1613.
85. Tokoyoda, K., S. Zehentmeier, A. N. Hegazy, I. Albrecht, J. R. Grün, M. Löhning, and A. Radbruch. 2009. Professional memory CD4+ T lymphocytes preferentially reside and rest in the bone marrow. Immunity 30: 721-730.
86. Kondrack, R. M., J. Harbertson, J. T. Tan, M. E. McBreen, C. D. Surh, and L. M. Bradley. 2003. Interleukin 7 regulates the survival and generation of memory CD4 cells. J. Exp. Med. 198: 1797-1806.
87. Herndler-Brandstetter, D., K. Landgraf, B. Jenewein, A. Tzankov, R. Brunauer, S. Brunner, W. Parson, F. Kloss, R. Gassner, G. Lepperdinger, and B. Grubeck-Loebenstein. 2011. Human bone marrow hosts polyfunctional memory CD4+ and CD8+ T cells with close contact to IL-15-producing cells. J. Immunol. 186: 6965-6971.
88. Becker, T., S. Coley, E. Wherry, and R. Ahmed. 2005. Bone marrow is a preferred site for homeostatic proliferation of memory CD8 T cells. J. Immunol. 174: 1269-1273.
89. Parretta, E., G. Cassese, P. Barba, A. Santoni, J. Guardiola, and F. Di Rosa. 2005. CD8 cell division maintaining cytotoxic memory occurs predominantly in the bone marrow. J. Immunol. 174: 7654-7664.
90. Palendira, U., R. Chinn, W. Raza, K. Piper, G. Pratt, L. Machado, A. Bell, N. Khan, A. D. Hislop, R. Steyn, et al. 2008. Selective accumulation of virusspecific CD8+ T cells with unique homing phenotype within the human bone marrow. Blood 112: 3293-3302.
91. López, C. B., and T. Hermesh. 2011. Systemic responses during local viral infections: type I IFNs sound the alarm. Curr. Opin. Immunol. 23: 495-499.
92. Sato, T., N. Onai, H. Yoshihara, F. Arai, T. Suda, and T. Ohteki. 2009. Interferon regulatory factor-2 protects quiescent hematopoietic stem cells from type I interferondependent exhaustion. Nat. Med. 15: 696-700.
93. Hermesh, T., B. Moltedo, T. M. Moran, and C. B. López. 2010. Antiviral instruction of bone marrow leukocytes during respiratory viral infections. Cell Host Microbe 7: 343-353.
94. de Bruin, A. M., O. Demirel, B. Hooibrink, C. H. Brandts, and M. A. Nolte. 2013. Interferon-g impairs proliferation of hematopoietic stem cells in mice. Blood 121: 3578-3585.
95. Baldridge, M. T., K. Y. King, N. C. Boles, D. C. Weksberg, and M. A. Goodell. 2010. Quiescent haematopoietic stem cells are activated by IFN-gamma in response to chronic infection. Nature 465: 793-797.
96. Teitelbaum, S. L. 2006. Osteoclasts; culprits in inflammatory osteolysis. Arthritis Res. Ther. 8: 201.
97. Chakravarti, A., M. A. Raquil, P. Tessier, and P. E. Poubelle. 2009. Surface RANKL of Toll-like receptor 4-stimulated human neutrophils activates osteoclastic bone resorption. Blood 114: 1633-1644.
98. Bussard, K. M., C. V. Gay, and A. M. Mastro. 2008. The bone microenvironment in metastasis; what is special about bone? Cancer Metastasis Rev. 27: 41-55.
99. Fujisaki, J., J. Wu, A. L. Carlson, L. Silberstein, P. Putheti, R. Larocca, W. Gao, T. I. Saito, C. Lo Celso, H. Tsuyuzaki, et al. 2011. In vivo imaging of Treg cells providing immune privilege to the haematopoietic stem-cell niche. Nature 474: 216-219.
100. Zeng, D., P. Hoffmann, F. Lan, P. Huie, J. Higgins, and S. Strober. 2002. Unique patterns of surface receptors, cytokine secretion, and immune functions distinguish T cells in the bone marrow from those in the periphery: impact on allogeneic bone marrow transplantation. Blood 99: 1449-1457.
101. Nguyen, V. H., R. Zeiser, and R. S. Negrin. 2006. Role of naturally arising regulatory T cells in hematopoietic cell transplantation. Biol. Blood Marrow Transplant. 12: 995-1009.
102. Zaiss, M. M., B. Frey, A. Hess, J. Zwerina, J. Luther, F. Nimmerjahn, K. Engelke, G. Kollias, T. Hünig, G. Schett, and J. P. David. 2010. Regulatory T cells protect from local and systemic bone destruction in arthritis. J. Immunol. 184: 7238-7246.
103. Jang, E., W. S. Cho, M. L. Cho, H. J. Park, H. J. Oh, S. M. Kang, D. J. Paik, and J. Youn. 2011. Foxp3+ regulatory T cells control humoral autoimmunity by suppressing the development of long-lived plasma cells. J. Immunol. 186: 1546-1553.
104. Hall, A. O., D. P. Beiting, C. Tato, B. John, G. Oldenhove, C. G. Lombana, G. H. Pritchard, J. S. Silver, N. Bouladoux, J. S. Stumhofer, et al. 2012. The cytokines interleukin 27 and interferon-g promote distinct Treg cell populations required to limit infection-induced pathology. Immunity 37: 511-523.
105. Oldenhove, G., N. Bouladoux, E. A. Wohlfert, J. A. Hall, D. Chou, L. Dos Santos, S. O'Brien, R. Blank, E. Lamb, S. Natarajan, et al. 2009. Decrease of Foxp3+ Treg cell number and acquisition of effector cell phenotype during lethal infection. Immunity 31: 772-786.
106. Koch, M. A., G. Tucker-Heard, N. R. Perdue, J. R. Killebrew, K. B. Urdahl, and D. J. Campbell. 2009. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat. Immunol. 10: 595-602.
107. Rossi, M. I., H. S. Dutra, M. C. El-Cheikh, A. Bonomo, and R. Borojevic. 1999. Extramedullar B lymphopoiesis in liver schistosomal granulomas: presence of the early stages and inhibition of the full B cell differentiation. Int. Immunol. 11: 509-518.
108. Rowland, S. L., K. Tuttle, R. M. Torres, and R. Pelanda. 2013. Antigen and cytokine receptor signals guide the development of the naïve mature B cell repertoire. Immunol. Res. 55: 231-240.
109. Stefanovic, S., F. Schuetz, C. Sohn, P. Beckhove, and C. Domschke. 2013. Bone marrow microenvironment in cancer patients: immunological aspects and clinical implications. Cancer Metastasis Rev. 32: 163-178.