Pathologic and protective roles for microglial subsets and bone marrow- and blood-derived myeloid cells in central nervous system inflammation

Frontiers in Immunology

Volumn 6, Issue SEP, 2015, Pages

  Wlodarczyk, Agnieszka ^a   Cédile, Oriane ^a   Jensen, Kirstine Nolling ^a   Jasson, Agathe ^a,b   Mony, Jyothi Thyagabhavan ^a   Khorooshi, Reza ^a   Owens, Trevor ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b UNIVERSITÉ DE LYON   (France)

Author keywords

CD11c; CNS; EAE; M1 M2; Microglia; Myeloid cells

Indexed keywords

BETA INTERFERON; CHEMOKINE RECEPTOR CX3CR1; COLONY STIMULATING FACTOR 1; GLYCOPROTEIN P 15095; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; TRANSCRIPTION FACTOR T BET;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL FUNCTION; CELL HETEROGENEITY; CONTROLLED STUDY; IMMUNOREGULATION; MICROGLIA; MOUSE; MULTIPLE SCLEROSIS; NERVE REGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN;

EID: 84949546319     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00463     Document Type: Article

References (55)

1. Gertig U, Hanisch UK. Microglial diversity by responses and responders. Front Cell Neurosci (2014) 8:101. doi:10.3389/fncel.2014.00101
2. Goverman J. Autoimmune T cell responses in the central nervous system. Nat Rev Immunol (2009) 9:393-407. doi:10.1038/nri2550
3. Chen SJ, Wang YL, Fan HC, Lo WT, Wang CC, Sytwu HK. Current status of the immunomodulation and immunomediated therapeutic strategies for multiple sclerosis. Clin Dev Immunol (2012) 2012:970789. doi:10.1155/2012/970789
4. Schwartz M, Moalem G, Leibowitz-Amit R, Cohen IR. Innate and adaptive immune responses can be beneficial for CNS repair. Trends Neurosci (1999) 22:295-9. doi:10.1016/S0166-2236(99)01405-8
5. Hvilsted Nielsen H, Toft-Hansen H, Lambertsen KL, Owens T, Finsen B. Stimulation of adult oligodendrogenesis by myelin-specific T cells. Am J Pathol (2011) 179:2028-41. doi:10.1016/j.ajpath.2011.06.006
6. Aloisi F, Ria F, Columba-Cabezas S, Hess H, Penna G, Adorini L. Relative efficiency of microglia, astrocytes, dendritic cells and B cells in naive CD4+ T cell priming and Th1/Th2 cell restimulation. Eur J Immunol (1999) 29:2705-14. doi:10.1002/(SICI)1521-4141(199909)29:09<2705::AID-IMMU2705>3.0.CO;2-1
7. Chabot S, Williams G, Hamilton M, Sutherland G, Yong VW. Mechanisms of IL-10 production in human microglia-T cell interaction. J Immunol (1999) 162:6819-28.
8. Matyszak MK, Denis-Donini S, Citterio S, Longhi R, Granucci F, Ricciardi-Castagnoli P. Microglia induce myelin basic protein-specific T cell anergy or T cell activation, according to their state of activation. Eur J Immunol (1999) 29:3063-76. doi:10.1002/(SICI)1521-4141(199910)29:10<3063::AID-IMMU3063>3.0.CO;2-G
9. Becher B, Blain M, Antel JP. CD40 engagement stimulates IL-12 p70 production by human microglial cells: basis for Th1 polarization in the CNS. J Neuroimmunol (2000) 102:44-50. doi:10.1016/S0165-5728(99)00152-6
10. Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci (2007) 10:1387-94. doi:10.1038/nn1997
11. Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science (2010) 330:841-5. doi:10.1126/science.1194637
12. Ajami B, Bennett JL, Krieger C, Tetzlaff W, Rossi FM. Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci (2007) 10:1538-43. doi:10.1038/nn2014
13. Sedgwick JD, Schwender S, Imrich H, Dorries R, Butcher GW, Ter Meulen V. Isolation and direct characterization of resident microglial cells from the normal and inflamed central nervous system. Proc Natl Acad Sci U S A (1991) 88:7438-42. doi:10.1073/pnas.88.16.7438
14. Ford AL, Goodsall AL, Hickey WF, Sedgwick JD. 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 (1995) 154:4309-21.
15. Perry VH, Hume DA, Gordon S. Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience (1985) 15:313-26. doi:10.1016/0306-4522(85)90215-5
16. Giulian D, Baker TJ. Characterization of ameboid microglia isolated from developing mammalian brain. J Neurosci (1986) 6:2163-78.
17. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, Kohsaka S. Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res (1998) 57:1-9. doi:10.1016/S0169-328X(98)00040-0
18. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, et al. Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci (2006) 9:917-24. doi:10.1038/nn1715
19. Wlodarczyk A, Lobner M, Cedile O, Owens T. Comparison of microglia and infiltrating CD11c(+) cells as antigen presenting cells for T cell proliferation and cytokine response. J Neuroinflammation (2014) 11:57. doi:10.1186/1742-2094-11-57
20. Immig K, Gericke M, Menzel F, Merz F, Krueger M, Schiefenhovel F, et al. CD11c-positive cells from brain, spleen, lung, and liver exhibit site-specific immune phenotypes and plastically adapt to new environments. Glia (2015) 63:611-25. doi:10.1002/glia.22771
21. Mizutani M, Pino PA, Saederup N, Charo IF, Ransohoff RM, Cardona AE. The fractalkine receptor but not CCR2 is present on microglia from embryonic development throughout adulthood. J Immunol (2012) 188:29-36. doi:10.4049/jimmunol.1100421
22. Khorooshi R, Wlodarczyk A, Asgari N, Owens T. Neuromyelitis optica-like pathology is dependent on type I interferon response. Exp Neurol (2013) 247:744-7. doi:10.1016/j.expneurol.2013.02.005
23. Remington LT, Babcock AA, Zehntner SP, Owens T. Microglial recruitment, activation, and proliferation in response to primary demyelination. Am J Pathol (2007) 170:1713-24. doi:10.2353/ajpath.2007.060783
24. Khorooshi R, Owens T. Detection and cellular localization of phospho-STAT2 in the central nervous system by immunohistochemical staining. Methods Mol Biol (2013) 967:179-88. doi:10.1007/978-1-62703-242-1_13
25. Gomez-Nicola D, Fransen NL, Suzzi S, Perry VH. Regulation of microglial proliferation during chronic neurodegeneration. J Neurosci (2013) 33:2481-93. doi:10.1523/JNEUROSCI.4440-12.2013
26. Akiyama H, McGeer PL. Brain microglia constitutively express beta-2 integrins. J Neuroimmunol (1990) 30:81-93. doi:10.1016/0165-5728(90)90055-R
27. Bulloch K, Miller MM, Gal-Toth J, Milner TA, Gottfried-Blackmore A, Waters EM, et al. CD11c/EYFP transgene illuminates a discrete network of dendritic cells within the embryonic, neonatal, adult, and injured mouse brain. J Comp Neurol (2008) 508:687-710. doi:10.1002/cne.21668
28. Butovsky O, Kunis G, Koronyo-Hamaoui M, Schwartz M. Selective ablation of bone marrow-derived dendritic cells increases amyloid plaques in a mouse Alzheimer's disease model. Eur J Neurosci (2007) 26:413-6. doi:10.1111/j.1460-9568.2007.05652.x
29. Nishiyori A, Minami M, Ohtani Y, Takami S, Yamamoto J, Kawaguchi N, et al. Localization of fractalkine and CX3CR1 mRNAs in rat brain: does fractalkine play a role in signaling from neuron to microglia? FEBS Lett (1998) 429:167-72. doi:10.1016/S0014-5793(98)00583-3
30. Wolf Y, Yona S, Kim KW, Jung S. Microglia, seen from the CX3CR1 angle. Front Cell Neurosci (2013) 7:26. doi:10.3389/fncel.2013.00026
31. Garcia JA, Pino PA, Mizutani M, Cardona SM, Charo IF, Ransohoff RM, et al. Regulation of adaptive immunity by the fractalkine receptor during autoimmune inflammation. J Immunol (2013) 191:1063-72. doi:10.4049/jimmunol.1300040
32. Hanisch UK. Functional diversity of microglia - how heterogeneous are they to begin with? Front Cell Neurosci (2013) 7:65. doi:10.3389/fncel.2013.00065
33. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol (2008) 8:958-69. doi:10.1038/nri2448
34. Butovsky O, Koronyo-Hamaoui M, Kunis G, Ophir E, Landa G, Cohen H, et al. Glatiramer acetate fights against Alzheimer's disease by inducing dendritic-like microglia expressing insulin-like growth factor 1. Proc Natl Acad Sci U S A (2006) 103:11784-9. doi:10.1073/pnas.0604681103
35. Kocur M, Schneider R, Pulm AK, Bauer J, Kropp S, Gliem M, et al. IFNbeta secreted by microglia mediates clearance of myelin debris in CNS autoimmunity. Acta Neuropathol Commun (2015) 3:20. doi:10.1186/s40478-015-0192-4
36. Khorooshi R, Morch MT, Holm TH, Berg CT, Dieu RT, Draeby D, et al. Induction of endogenous type I interferon within the central nervous system plays a protective role in experimental autoimmune encephalomyelitis. Acta Neuropathol (2015) 130:107-18. doi:10.1007/s00401-015-1418-z
37. Compston A, Coles A. Multiple sclerosis. Lancet (2008) 372:1502-17. doi:10.1016/S0140-6736(08)61620-7
38. Yamasaki R, Lu H, Butovsky O, Ohno N, Rietsch AM, Cialic R, et al. Differential roles of microglia and monocytes in the inflamed central nervous system. J Exp Med (2014) 211:1533-49. doi:10.1084/jem.20132477
39. Biber K, Owens T, Boddeke E. What is microglia neurotoxicity (Not)? Glia (2014) 62:841-54. doi:10.1002/glia.22654
40. Elmore MR, Najafi AR, Koike MA, Dagher NN, Spangenberg EE, Rice RA, et al. Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain. Neuron (2014) 82:380-97. doi:10.1016/j.neuron.2014.02.040
41. Fischer HG, Reichmann G. Brain dendritic cells and macrophages/microglia in central nervous system inflammation. J Immunol (2001) 166:2717-26. doi:10.4049/jimmunol.166.4.2717
42. Szabo SJ, Kim ST, Costa GL, Zhang X, Fathman CG, Glimcher LH. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell (2000) 100:655-69. doi:10.1016/S0092-8674(00)80702-3
43. Lazarevic V, Glimcher LH, Lord GM. T-bet: a bridge between innate and adaptive immunity. Nat Rev Immunol (2013) 13:777-89. doi:10.1038/nri3536
44. Gocke AR, Cravens PD, Ben LH, Hussain RZ, Northrop SC, Racke MK, et al. T-bet regulates the fate of Th1 and Th17 lymphocytes in autoimmunity. J Immunol (2007) 178:1341-8. doi:10.4049/jimmunol.178.3.1341
45. Lugo-Villarino G, Maldonado-Lopez R, Possemato R, Penaranda C, Glimcher LH. T-bet is required for optimal production of IFN-gamma and antigen-specific T cell activation by dendritic cells. Proc Natl Acad Sci U S A (2003) 100:7749-54. doi:10.1073/pnas.1332767100
46. Sullivan BM, Juedes A, Szabo SJ, Von Herrath M, Glimcher LH. Antigen-driven effector CD8 T cell function regulated by T-bet. Proc Natl Acad Sci U S A (2003) 100:15818-23. doi:10.1073/pnas.2636938100
47. Cravens PD, Hussain RZ, Zacharias TE, Ben LH, Herndon E, Vinnakota R, et al. Lymph node-derived donor encephalitogenic CD4+ T cells in C57BL/6 mice adoptive transfer experimental autoimmune encephalomyelitis highly express GM-CSF and T-bet. J Neuroinflammation (2011) 8:73. doi:10.1186/1742-2094-8-73
48. Codarri L, Greter M, Becher B. Communication between pathogenic T cells and myeloid cells in neuroinflammatory disease. Trends Immunol (2013) 34:114-9. doi:10.1016/j.it.2012.09.007
49. Yang Y, Weiner J, Liu Y, Smith AJ, Huss DJ, Winger R, et al. T-bet is essential for encephalitogenicity of both Th1 and Th17 cells. J Exp Med (2009) 206:1549-64. doi:10.1084/jem.20082584
50. Spath S, Becher B. T-bet or not T-bet: taking the last bow on the autoimmunity stage. Eur J Immunol (2013) 43:2810-3. doi:10.1002/eji.201344109
51. Alcaide P, Jones TG, Lord GM, Glimcher LH, Hallgren J, Arinobu Y, et al. Dendritic cell expression of the transcription factor T-bet regulates mast cell progenitor homing to mucosal tissue. J Exp Med (2007) 204:431-9. doi:10.1084/jem.20060626
52. Reynier F, De Vos AF, Hoogerwerf JJ, Bresser P, Van Der Zee JS, Paye M, et al. Gene expression profiles in alveolar macrophages induced by lipopolysaccharide in humans. Mol Med (2012) 18:1303-11. doi:10.2119/molmed.2012.00230
53. Mantovani A, Sica A, Locati M. Macrophage polarization comes of age. Immunity (2005) 23:344-6. doi:10.1016/j.immuni.2005.10.001
54. Ajmone-Cat MA, Mancini M, De Simone R, Cilli P, Minghetti L. Microglial polarization and plasticity: evidence from organotypic hippocampal slice cultures. Glia (2013) 61:1698-711. doi:10.1002/glia.22550
55. Babcock AA, Ilkjaer L, Clausen BH, Villadsen B, Dissing-Olesen L, Bendixen AT, et al. Cytokine-producing microglia have an altered beta-amyloid load in aged APP/PS1 Tg mice. Brain Behav Immun (2015) 48:86-101. doi:10.1016/j.bbi.2015.03.006