DNGR-1+ dendritic cells are located in meningeal membrane and choroid plexus of the noninjured brain

GLIA

Volumn 63, Issue 12, 2015, Pages 2231-2248

  Quintana, Elena ^a   Fernández, Andrés ^a   Velasco, Patricia ^a   de Andrés, Belén ^b   Liste, Isabel ^a   Sancho, David ^c   Gaspar, María Luisa ^b   Cano, Eva ^a  

^a Unidad Funcional de Investigación en Enfermedades Crónicas   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

Author keywords

Batf3; C type lectin receptors; CD11c; Flt3L; Myeloid cells; Neuroinflammation

Indexed keywords

CD103 ANTIGEN; CD11B ANTIGEN; FLT3 LIGAND; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; LECTIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CD45 ANTIGEN; CLEC9A PROTEIN, MOUSE; ENHANCED GREEN FLUORESCENT PROTEIN; FLT3 LIGAND PROTEIN; GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN RECEPTOR; INTERFERON REGULATORY FACTOR; MEMBRANE PROTEIN; PTPRC PROTEIN, MOUSE; REPRESSOR PROTEIN; SNFT PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; BONE MARROW CELL; BRAIN; CELL FUNCTION; CELLULAR DISTRIBUTION; CHOROID PLEXUS; CONTROLLED STUDY; DENDRITIC CELL; MENINX; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; CYTOLOGY; GENE; GENETICS; MALE; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD45; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CHOROID PLEXUS; DENDRITIC CELLS; GENES, MHC CLASS II; GREEN FLUORESCENT PROTEINS; INTERFERON REGULATORY FACTORS; LECTINS, C-TYPE; MALE; MEMBRANE PROTEINS; MENINGES; MICE, INBRED C57BL; MICE, TRANSGENIC; RECEPTORS, IMMUNOLOGIC; REPRESSOR PROTEINS; RNA, MESSENGER;

EID: 84943581188     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22889     Document Type: Article

References (66)

1. Ajami B, Bennett JL, Krieger C, Tetzlaff W, Rossi FM. 2007. Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci 10:1538-1543.
2. Anandasabapathy N, Victora GD, Meredith M, Feder R, Dong B, Kluger C, Yao K, Dustin ML, Nussenzweig MC, Steinman RM, Liu K. 2011. Flt3L controls the development of radiosensitive dendritic cells in the meninges and choroid plexus of the steady-state mouse brain. J Exp Med 208:1695-1705.
3. Axtell RC, Steinman L. 2009. Gaining entry to an uninflamed brain. Nat Immunol 10:453-455.
4. Bulloch K, Miller MM, Gal-Toth J, Milner TA, Gottfried-Blackmore A, Waters EM, Kaunzner UW, Liu K, Lindquist R, Nussenzweig MC, Steinman RM, McEwen BS. 2008. CD11c/EYFP transgene illuminates a discrete network of dendritic cells within the embryonic, neonatal, adult, and injured mouse brain. J Comp Neurol 508:687-710.
5. Caminschi I, Lahoud MH, Shortman K. 2009. Enhancing immune responses by targeting antigen to DC. Eur J Immunol 39:931-938.
6. Caminschi I, Proietto AI, Ahmet F, Kitsoulis S, Shin TJ, Lo JC, Rizzitelli A, Wu L, Vremec D, van Dommelen SL, Campbell IK, Maraskovsky E, Braley H, Davey GM, Mottram P, van d V, Jensen K, Lew AM, Wright MD, Heath WR, Shortman K, Lahoud MH. 2008. The dendritic cell subtype-restricted C-type lectin Clec9A is a target for vaccine enhancement. Blood 112:3264-3273.
7. Carson MJ, Reilly CR, Sutcliffe JG, Lo D. 1998. Mature microglia resemble immature antigen-presenting cells. Glia 22:72-85.
8. D'Agostino PM, Gottfried-Blackmore A, Anandasabapathy N, Bulloch K. 2012. Brain dendritic cells: biology and pathology. Acta Neuropathol 124:599-614.
9. del Rio ML, Bernhardt G, Rodriguez-Barbosa JI, Forster R. 2010. Development and functional specialization of CD103+ dendritic cells. Immunol Rev 234:268-281.
10. Elmore MR, Najafi AR, Koike MA, Dagher NN, Spangenberg EE, Rice RA, Kitazawa M, Matusow B, Nguyen H, West BL, Green KN. 2014. Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain. Neuron 82:380-397.
11. Engelhardt B, Ransohoff RM. 2005. The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms. Trends Immunol 26:485-495.
12. Erblich B, Zhu L, Etgen AM, Dobrenis K, Pollard JW. 2011. Absence of colony stimulation factor-1 receptor results in loss of microglia, disrupted brain development and olfactory deficits. PLoS One 6:e26317-
13. Ferron SR, Andreu-Agullo C, Mira H, Sanchez P, Marques-Torrejon MA, Farinas I. 2007. A combined ex/in vivo assay to detect effects of exogenously added factors in neural stem cells. Nat Protoc 2:849-859.
14. Fischer HG, Reichmann G. 2001. Brain dendritic cells and macrophages/microglia in central nervous system inflammation. J Immunol 166:2717-2726.
15. Ford AL, Goodsall AL, Hickey WF, Sedgwick JD. 1995. Normal adult ramified microglia separated from other central nervous system macrophages by flow cytometric sorting. Phenotypic differences defined and direct ex vivo antigen presentation to myelin basic protein-reactive CD4+ T cells compared. J Immunol 154:4309-4321.
16. Galea I, Bechmann I, Perry VH. 2007. What is immune privilege (not)?. Trends Immunol 28:12-18.
17. Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, Mehler MF, Conway SJ, Ng LG, Stanley ER, Samokhvalov IM, Merad M. 2010. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330:841-845.
18. Ginhoux F, Liu K, Helft J, Bogunovic M, Greter M, Hashimoto D, Price J, Yin N, Bromberg J, Lira SA, Stanley ER, Nussenzweig M, Merad M. 2009. The origin and development of nonlymphoid tissue CD103+ DCs. J Exp Med 206:3115-3130.
19. Greter M, Heppner FL, Lemos MP, Odermatt BM, Goebels N, Laufer T, Noelle RJ, Becher B. 2005. Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis. Nat Med 11:328-334.
20. Guo W, Patzlaff NE, Jobe EM, Zhao X. Microdissection of the SVZ and the DG of a single adult mouse. Isolation of multipotent neural stem or progenitor cells from both the dentate gyrus and subventricular zone of a single adult mouse. Nature Protocols 7, 2005-2012 (2012).
21. Heath WR, Carbone FR. 2009. Dendritic cell subsets in primary and secondary T cell responses at body surfaces. Nat Immunol 10:1237-1244.
22. Hildner K, Edelson BT, Purtha WE, Diamond M, Matsushita H, Kohyama M, Calderon B, Schraml BU, Unanue ER, Diamond MS, Schreiber RD, Murphy TL, Murphy KM. 2008. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 322:1097-1100.
23. Huysamen C, Brown GD. 2009. The fungal pattern recognition receptor, Dectin-1, and the associated cluster of C-type lectin-like receptors. FEMS Microbiol Lett 290:121-128.
24. Huysamen C, Willment JA, Dennehy KM, Brown GD. 2008. CLEC9A is a novel activation C-type lectin-like receptor expressed on BDCA3+ dendritic cells and a subset of monocytes. J Biol Chem 283:16693-16701.
25. Iborra S, Izquierdo HM, Martinez-Lopez M, Blanco-Menendez N, Reis e Sousa, Sancho D. 2012. The DC receptor DNGR-1 mediates cross-priming of CTLs during vaccinia virus infection in mice. J Clin Invest 122:1628-1643.
26. Immig K, Gericke M, Menzel F, Merz F, Krueger M, Schiefenhovel F, Losche A, Jager K, Hanisch UK, Biber K, Bechmann I. 2015. CD11c-positive cells from brain, spleen, lung, and liver exhibit site-specific immune phenotypes and plastically adapt to new environments. Glia 63:611-625.
27. Inaba K, Turley S, Yamaide F, Iyoda T, Mahnke K, Inaba M, Pack M, Subklewe M, Sauter B, Sheff D, Albert M, Bhardwaj N, Mellman I, Steinman RM. 1998. Efficient presentation of phagocytosed cellular fragments on the major histocompatibility complex class II products of dendritic cells. J Exp Med 188:2163-2173.
28. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, Kohsaka S. 1998. Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res 57:1-9.
29. Iyoda T, Inaba K. 2002. [Immune regulation by dendritic cells]. Tanpakushitsu Kakusan Koso 47:2133-2138.
30. Jung S, Unutmaz D, Wong P, Sano G, De los SK, Sparwasser T, Wu S, Vuthoori S, Ko K, Zavala F, Pamer EG, Littman DR, Lang RA. 2002. In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T cells by exogenous cell-associated antigens. Immunity 17:211-220.
31. Karman J, Chu HH, Co DO, Seroogy CM, Sandor M, Fabry Z. 2006. Dendritic cells amplify T cell-mediated immune responses in the central nervous system. J Immunol 177:7750-7760.
32. Lindquist RL, Shakhar G, Dudziak D, Wardemann H, Eisenreich T, Dustin ML, Nussenzweig MC. 2004. Visualizing dendritic cell networks in vivo. Nat Immunol 5:1243-1250.
33. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-408.
34. Lv M, Liu Y, Zhang J, Sun L, Liu Z, Zhang S, Wang B, Su D, Su Z. 2011. Roles of inflammation response in microglia cell through Toll-like receptors 2/interleukin-23/interleukin-17 pathway in cerebral ischemia/reperfusion injury. Neuroscience 176:162-172.
35. Matyszak MK, Lawson LJ, Perry VH, Gordon S. 1992. Stromal macrophages of the choroid plexus situated at an interface between the brain and peripheral immune system constitutively express major histocompatibility class II antigens. J Neuroimmunol 40:173-181.
36. Matyszak MK, Perry VH. 1996. The potential role of dendritic cells in immune-mediated inflammatory diseases in the central nervous system. Neuroscience 74:599-608.
37. McMahon EJ, Bailey SL, Castenada CV, Waldner H, Miller SD. 2005. Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis. Nat Med 11:335-339.
38. McMenamin PG. 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.
39. McMenamin PG, Wealthall RJ, Deverall M, Cooper SJ, Griffin B. 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.
40. Mildner A, Schmidt H, Nitsche M, Merkler D, Hanisch UK, Mack M, Heikenwalder M, Bruck W, Priller J, Prinz M. 2007. Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat Neurosci 10:1544-1553.
41. Murphy KM. 2013. Transcriptional control of dendritic cell development. Adv Immunol 120:239-267.
42. Nimmerjahn A, Kirchhoff F, Helmchen F. 2005. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308:1314-1318.
43. Pashenkov M, Teleshova N, Link H. 2003. Inflammation in the central nervous system: The role for dendritic cells. Brain Pathol 13:23-33.
44. Piva L, Tetlak P, Claser C, Karjalainen K, Renia L, Ruedl C. 2012. Cutting edge: Clec9A+ dendritic cells mediate the development of experimental cerebral malaria. J Immunol 189:1128-1132.
45. Pooley JL, Heath WR, Shortman K. 2001. Cutting edge: intravenous soluble antigen is presented to CD4 T cells by CD8- dendritic cells, but cross-presented to CD8 T cells by CD8+ dendritic cells. J Immunol 166:5327-5330.
46. Poulin LF, Reyal Y, Uronen-Hansson H, Schraml BU, Sancho D, Murphy KM, Hakansson UK, Moita LF, Agace WW Bonnet D., Reis e Sousa . 2012. DNGR-1 is a specific and universal marker of mouse and human Batf3-dependent dendritic cells in lymphoid and nonlymphoid tissues. Blood 119:6052-6062.
47. Poulin LF, Salio M, Griessinger E, Anjos-Afonso F, Craciun L, Chen JL, Keller AM, Joffre O, Zelenay S, Nye E, Le Moine A, Faure F, Donckier V, Sancho D, Cerundolo V Bonnet D., Reis e Sousa . 2010. Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8alpha+ dendritic cells. J Exp Med 207:1261-1271.
48. Prinz M, Tay TL, Wolf Y, Jung S. 2014. Microglia: unique and common features with other tissue macrophages. Acta Neuropathol 128:319-331.
49. Probst HC, Tschannen K, Odermatt B, Schwendener R, Zinkernagel RM, van den Broek M. 2005. Histological analysis of CD11c-DTR/GFP mice after in vivo depletion of dendritic cells. Clin Exp Immunol 141:398-404.
50. Prodinger C, Bunse J, Kruger M, Schiefenhovel F, Brandt C, Laman JD, Greter M, Immig K, Heppner F, Becher B, Bechmann I. 2011. CD11c-expressing cells reside in the juxtavascular parenchyma and extend processes into the glia limitans of the mouse nervous system. Acta Neuropathol 121:445-458.
51. Puntener U, Booth SG, Perry VH, Teeling JL. 2012. Long-term impact of systemic bacterial infection on the cerebral vasculature and microglia. J Neuroinflammation 9:146-
52. Ransohoff RM, Cardona AE. 2010. The myeloid cells of the central nervous system parenchyma. Nature 468:253-262.
53. Ransohoff RM, Engelhardt B. 2012. The anatomical and cellular basis of immune surveillance in the central nervous system. Nat Rev Immunol 12:623-635.
54. Sancho D, Joffre OP, Keller AM, Rogers NC, Martinez D, Hernanz-Falcon P Rosewell I., Reis e Sousa . 2009. Identification of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature 458:899-903.
55. Sancho D, Mourao-Sa D, Joffre OP, Schulz O, Rogers NC, Pennington DJ Carlyle JR., Reis e Sousa . 2008. Tumor therapy in mice via antigen targeting to a novel, DC-restricted C-type lectin. J Clin Invest 118:2098-2110.
56. Sasmono RT, Oceandy D, Pollard JW, Tong W, Pavli P, Wainwright BJ, Ostrowski MC, Himes SR, Hume DA. 2003. A macrophage colony-stimulating factor receptor-green fluorescent protein transgene is expressed throughout the mononuclear phagocyte system of the mouse. Blood 101:1155-1163.
57. Schraml BU, van BJ, Zelenay S, Whitney PG, Filby A, Acton SE, Rogers NC, Moncaut N Carvajal JJ., Reis e Sousa . 2013. Genetic tracing via DNGR-1 expression history defines dendritic cells as a hematopoietic lineage. Cell 154:843-858.
58. Schulz O., Reis e Sousa . 2002. Cross-presentation of cell-associated antigens by CD8alpha+ dendritic cells is attributable to their ability to internalize dead cells. Immunology 107:183-189.
59. Serafini B, Columba-Cabezas S, Di RF, Aloisi F. 2000. Intracerebral recruitment and maturation of dendritic cells in the onset and progression of experimental autoimmune encephalomyelitis. Am J Pathol 157:1991-2002.
60. Serrano-Perez MC, Martin ED, Vaquero CF, Azcoitia I, Calvo S, Cano E, Tranque P. 2011. Response of transcription factor NFATc3 to excitotoxic and traumatic brain insults: Identification of a subpopulation of reactive astrocytes. Glia 59:94-107.
61. Shechter R, London A, Schwartz M. 2013. Orchestrated leukocyte recruitment to immune-privileged sites: Absolute barriers versus educational gates. Nat Rev Immunol 13:206-218.
62. Shortman K, Heath WR. 2010. The CD8+ dendritic cell subset. Immunol Rev 234:18-31.
63. Sierra A, Gottfried-Blackmore AC, McEwen BS, Bulloch K. 2007. Microglia derived from aging mice exhibit an altered inflammatory profile. Glia 55:412-424.
64. van Rijt LS, Jung S, KleinJan A, Vos N, Willart M, Duez C, Hoogsteden HC, Lambrecht BN. 2005. In vivo depletion of lung CD11c+ dendritic cells during allergen challenge abrogates the characteristic features of asthma. J Exp Med 201:981-991.
65. Watowich SS, Liu YJ. 2010. Mechanisms regulating dendritic cell specification and development. Immunol Rev 238:76-92.
66. Zelenay S, Keller AM, Whitney PG, Schraml BU, Deddouche S, Rogers NC, Schulz O Sancho D., Reis e Sousa . 2012. The dendritic cell receptor DNGR-1 controls endocytic handling of necrotic cell antigens to favor cross-priming of CTLs in virus-infected mice. J Clin Invest 122:1615-1627.