Flt3L controls the development of radiosensitive dendritic cells in the meninges and choroid plexus of the steady-state mouse brain

Journal of Experimental Medicine

Volumn 208, Issue 18, 2011, Pages 1695-1705

  Anandasabapathy, Niroshana ^a   Victora, Gabriel D ^a,b   Meredith, Matthew ^a   Feder, Rachel ^a   Dong, Baojun ^c   Kluger, Courtney ^a   Yao, Kaihui ^a   Dustin, Michael L ^b   Nussenzweig, Michel C ^a   Steinman, Ralph M ^a   Liu, Kang ^a,c  

^a ROCKEFELLER UNIVERSITY   (United States)

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

^c NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD135 ANTIGEN; FLT3 LIGAND; PATTERN RECOGNITION RECEPTOR; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; BRAIN; CELL DIFFERENTIATION; CELL MATURATION; CELL STRUCTURE; CHOROID PLEXUS; CONTROLLED STUDY; DENDRITIC CELL; GENE EXPRESSION PROFILING; MENINX; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; STEADY STATE; T LYMPHOCYTE;

ADOPTIVE TRANSFER; ANIMALS; CHOROID PLEXUS; DENDRITIC CELLS; FEMALE; FLOW CYTOMETRY; FMS-LIKE TYROSINE KINASE 3; HALF-LIFE; MENINGES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROARRAY ANALYSIS; MICROGLIA; MONOCYTES; RECEPTORS, PATTERN RECOGNITION; TRANSCRIPTION FACTORS;

EID: 79961160742     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20102657     Document Type: Article

References (54)

1. Axtell, R.C., and L. Steinman. 2009. Gaining entry to an uninflamed brain. Nat. Immunol. 10:453-455.
2. Bailey, S.L., P.A. Carpentier, E.J. McMahon, W.S. Begolka, and S.D. Miller. 2006. Innate and adaptive immune responses of the central nervous system. Crit. Rev. Immunol. 26:149-188.
3. Bailey, S.L., B. Schreiner, E.J. McMahon, and S.D. Miller. 2007. CNS myeloid DCs presenting endogenous myelin peptides 'preferentially' polarize CD4+ T(H)-17 cells in relapsing EAE. Nat. Immunol. 8:172-180.
4. Banchereau, J., and R.M. Steinman. 1998. Dendritic cells and the control of immunity. Nature. 392:245-252.
5. Bartholomäus, I., N. Kawakami, F. Odoardi, C. Schläger, D. Miljkovic, J.W. Ellwart, W.E. Klinkert, C. Flügel-Koch, T.B. Issekutz, H. Wekerle, and A. Flügel. 2009. Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature. 462:94-98.
6. Bettelli, E., M. Pagany, H.L. Weiner, C. Linington, R.A. Sobel, and V.K. Kuchroo. 2003. Myelin oligodendrocyte glycoprotein-specific T cell receptor transgenic mice develop spontaneous autoimmune optic neuritis. J. Exp. Med. 197:1073-1081.
7. Boes, M., J. Cerny, R. Massol, M. Op den Brouw, T. Kirchhausen, J. Chen, and H.L. Ploegh. 2002. T-cell engagement of dendritic cells rapidly rearranges MHC class II transport. Nature. 418:983-988.
8. 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.
9. Caton, M.L., M.R. Smith-Raska, and B. Reizis. 2007. Notch-RBP-J signaling controls the homeostasis of CD8? dendritic cells in the spleen. J. Exp. Med. 204:1653-1664.
10. Choi, J.H., Y. Do, C. Cheong, H. Koh, S.B. Boscardin, Y.S. Oh, L. Bozzacco, C. Trumpfheller, C.G. Park, and R.M. Steinman. 2009. Identification of antigen-presenting dendritic cells in mouse aorta and cardiac valves. J. Exp. Med. 206:497-505.
11. Derecki, N.C., A.N. Cardani, C.H. Yang, K.M. Quinnies, A. Crihfield, K.R. Lynch, and J. Kipnis. 2010. Regulation of learning and memory by meningeal immunity: a key role for IL-4. J. Exp. Med. 207:1067-1080.
12. Dudziak, D., A.O. Kamphorst, G.F. Heidkamp, V.R. Buchholz, C. Trumpfheller, S. Yamazaki, C. Cheong, K. Liu, H.W. Lee, C.G. Park, et al. 2007. Differential antigen processing by dendritic cell subsets in vivo. Science. 315:107-111.
13. Fogg, D.K., C. Sibon, C. Miled, S. Jung, P. Aucouturier, D.R. Littman, A. Cumano, and F. Geissmann. 2006. A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science. 311:83-87.
14. Geissmann, F., S. Jung, and D.R. Littman. 2003. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity. 19:71-82.
15. Geissmann, F., S. Gordon, D.A. Hume, A.M. Mowat, and G.J. Randolph. 2010. Unravelling mononuclear phagocyte heterogeneity. Nat. Rev. Immunol. 10:453-460.
16. + DCs. J. Exp. Med. 206:3115-3130.
17. Ginhoux, F., M. Greter, M. Leboeuf, S. Nandi, P. See, S. Gokhan, M.F. Mehler, S.J. Conway, L.G. Ng, E.R. Stanley, et al. 2010. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science. 330:841-845.
18. Gottfried-Blackmore, A., U.W. Kaunzner, J. Idoyaga, J.C. Felger, B.S. McEwen, and K. Bulloch. 2009. Acute in vivo exposure to interferon-gamma enables resident brain dendritic cells to become effective antigen presenting cells. Proc. Natl. Acad. Sci. USA. 106:20918-20923.
19. Greter, M., F.L. Heppner, M.P. Lemos, B.M. Odermatt, N. Goebels, T. Laufer, R.J. Noelle, and B. Becher. 2005. Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis. Nat. Med. 11:328-334.
20. Hacker, C., R.D. Kirsch, X.S. Ju, T. Hieronymus, T.C. Gust, C. Kuhl, T. Jorgas, S.M. Kurz, S. Rose-John, Y. Yokota, and M. Zenke. 2003. Transcriptional profiling identifies Id2 function in dendritic cell development. Nat. Immunol. 4:380-386.
21. Heath, W.R., and F.R. Carbone. 2009. Dendritic cell subsets in primary and secondary T cell responses at body surfaces. Nat. Immunol. 10:1237-1244.
22. Henri, S., M. Guilliams, L.F. Poulin, S. Tamoutounour, L. Ardouin, M. Dalod, and B. Malissen. 2010. Disentangling the complexity of the skin dendritic cell network. Immunol. Cell Biol. 88:366-375.
23. Hess, L.M., and K.C. Insel. 2007. Chemotherapy-related change in cognitive function: a conceptual model. Oncol. Nurs. Forum. 34:981-994.
24. Hickey, W.F. 1991. Migration of hematogenous cells through the blood-brain barrier and the initiation of CNS inflammation. Brain Pathol. 1:97-105.
25. Hildner, K., B.T. Edelson, W.E. Purtha, M. Diamond, H. Matsushita, M. Kohyama, B. Calderon, B.U. Schraml, E.R. Unanue, M.S. Diamond, et al. 2008. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science. 322:1097-1100.
26. Jung, S., D. Unutmaz, P. Wong, G. Sano, K. De los Santos, T. Sparwasser, S. Wu, S. Vuthoori, K. Ko, F. Zavala, et al. 2002. In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T cells by exogenous cell-associated antigens. Immunity. 17:211-220.
27. Kingston, D., M.A. Schmid, N. Onai, A. Obata-Onai, D. Baumjohann, and M.G. Manz. 2009. The concerted action of GM-CSF and Flt3-ligand on in vivo dendritic cell homeostasis. Blood. 114:835-843.
28. Kipnis, J., N.C. Derecki, C. Yang, and H. Scrable. 2008. Immunity and cognition: what do age-related dementia, HIV-dementia and 'chemo-brain' have in common? Trends Immunol. 29:455-463.
29. Kivisäkk, P., D.J. Mahad, M.K. Callahan, C. Trebst, B. Tucky, T. Wei, L. Wu, E.S. Baekkevold, H. Lassmann, S.M. Staugaitis, et al. 2003. Human cerebrospinal fluid central memory CD4+ T cells: evidence for trafficking through choroid plexus and meninges via P-selectin. Proc. Natl. Acad. Sci. USA. 100:8389-8394.
30. Kivisäkk, P., J. Imitola, S. Rasmussen, W. Elyaman, B. Zhu, R.M. Ransohoff, and S.J. Khoury. 2009. Localizing central nervous system immune surveillance: meningeal antigen-presenting cells activate T cells during experimental autoimmune encephalomyelitis. Ann. Neurol. 65:457-469.
31. Lemos, M.P., L. Fan, D. Lo, and T.M. Laufer. 2003. CD8alpha+ and CD11b+ dendritic cell-restricted MHC class II controls Th1 CD4+ T cell immunity. J. Immunol. 171:5077-5084.
32. Li, Y., Y. Song, L. Zhao, G. Gaidosh, A.M. Laties, and R. Wen. 2008. Direct labeling and visualization of blood vessels with lipophilic carbocyanine dye DiI. Nat. Protoc. 3:1703-1708.
33. Lindquist, R.L., G. Shakhar, D. Dudziak, H. Wardemann, T. Eisenreich, M.L. Dustin, and M.C. Nussenzweig. 2004. Visualizing dendritic cell networks in vivo. Nat. Immunol. 5:1243-1250.
34. Liu, K., C. Waskow, X. Liu, K. Yao, J. Hoh, and M. Nussenzweig. 2007. Origin of dendritic cells in peripheral lymphoid organs of mice. Nat. Immunol. 8:578-583.
35. Liu, K., G.D. Victora, T.A. Schwickert, P. Guermonprez, M.M. Meredith, K. Yao, F.F. Chu, G.J. Randolph, A.Y. Rudensky, and M. Nussenzweig. 2009. In vivo analysis of dendritic cell development and homeostasis. Science. 324:392-397.
36. Matyszak, M.K., and V.H. Perry. 1996. The potential role of dendritic cells in immune-mediated inflammatory diseases in the central nervous system. Neuroscience. 74:599-608.
37. McMenamin, P.G. 1999. Distribution and phenotype of dendritic cells and resident tissue macrophages in the dura mater, leptomeninges, and choroid plexus of the rat brain as demonstrated in wholemount preparations. J. Comp. Neurol. 405:553-562.
38. McMenamin, P.G., R.J. Wealthall, M. Deverall, S.J. Cooper, and B. Griffin. 2003. Macrophages and dendritic cells in the rat meninges and choroid plexus: three-dimensional localisation by environmental scanning electron microscopy and confocal microscopy. Cell Tissue Res. 313:259-269.
39. Mildner, A., H. Schmidt, M. Nitsche, D. Merkler, U.K. Hanisch, M. Mack, M. Heikenwalder, W. Brück, J. Priller, and M. Prinz. 2007. Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat. Neurosci. 10:1544-1553.
40. Naik, S.H., P. Sathe, H.Y. Park, D. Metcalf, A.I. Proietto, A. Dakic, S. Carotta, M. O'Keeffe, M. Bahlo, A. Papenfuss, et al. 2007. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat. Immunol. 8:1217-1226.
41. Onai, N., A. Obata-Onai, M.A. Schmid, T. Ohteki, D. Jarrossay, and M.G. Manz. 2007. Identification of clonogenic common Flt3+M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat. Immunol. 8:1207-1216.
42. Platten, M., and L. Steinman. 2005. Multiple sclerosis: trapped in deadly glue. Nat. Med. 11:252-253.
43. Price, R.W., B. Brew, J. Sidtis, M. Rosenblum, A.C. Scheck, and P. Cleary. 1988. The brain in AIDS: central nervous system HIV-1 infection and AIDS dementia complex. Science. 239:586-592.
44. Reboldi, A., C. Coisne, D. Baumjohann, F. Benvenuto, D. Bottinelli, S. Lira, A. Uccelli, A. Lanzavecchia, B. Engelhardt, and F. Sallusto. 2009. C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat. Immunol. 10:514-523.
45. Rescigno, M., and A. Di Sabatino. 2009. Dendritic cells in intestinal homeostasis and disease. J. Clin. Invest. 119:2441-2450.
46. Rudensky, A.Yu., S. Rath, P. Preston-Hurlburt, D.B. Murphy, and C.A. Janeway Jr. 1991. On the complexity of self. Nature. 353:660-662.
47. Serafini, B., B. Rosicarelli, R. Magliozzi, E. Stigliano, E. Capello, G.L. Mancardi, and F. Aloisi. 2006. Dendritic cells in multiple sclerosis lesions: maturation stage, myelin uptake, and interaction with proliferating T cells. J. Neuropathol. Exp. Neurol. 65:124-141.
48. Skarica, M., T. Wang, E. McCadden, D. Kardian, P.A. Calabresi, D. Small, and K.A. Whartenby. 2009. Signal transduction inhibition of APCs diminishes th17 and Th1 responses in experimental autoimmune encephalomyelitis. J. Immunol. 182:4192-4199.
49. Suzuki, S., K. Honma, T. Matsuyama, K. Suzuki, K. Toriyama, I. Akitoyo, K. Yamamoto, T. Suematsu, M. Nakamura, K. Yui, and A. Kumatori. 2004. Critical roles of interferon regulatory factor 4 in CD11bhighCD8alphadendritic cell development. Proc. Natl. Acad. Sci. USA. 101:8981-8986.
50. Varol, C., A. Vallon-Eberhard, E. Elinav, T. Aychek, Y. Shapira, H. Luche, H.J. Fehling, W.D. Hardt, G. Shakhar, and S. Jung. 2009. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity. 31:502-512.
51. Waskow, C., K. Liu, G. Darrasse-Jèze, P. Guermonprez, F. Ginhoux, M. Merad, T. Shengelia, K. Yao, and M. Nussenzweig. 2008. The receptor tyrosine kinase Flt3 is required for dendritic cell development in peripheral lymphoid tissues. Nat. Immunol. 9:676-683.
52. Wolf, S.A., B. Steiner, A. Akpinarli, T. Kammertoens, C. Nassenstein, A. Braun, T. Blankenstein, and G. Kempermann. 2009. CD4-positive T lymphocytes provide a neuroimmunological link in the control of adult hippocampal neurogenesis. J. Immunol. 182:3979-3984.
53. Wu, G.F., K.S. Shindler, E.J. Allenspach, T.L. Stephen, H.L. Thomas, R.J. Mikesell, A.H. Cross, and T.M. Laufer. 2011. Limited sufficiency of antigen presentation by dendritic cells in models of central nervous system autoimmunity. J. Autoimmun. 36:56-64.
54. Ziv, Y., N. Ron, O. Butovsky, G. Landa, E. Sudai, N. Greenberg, H. Cohen, J. Kipnis, and M. Schwartz. 2006. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat. Neurosci. 9:268-275.