Microglial control of astrocytes in response to microbial metabolites

Nature

Volumn 557, Issue 7707, 2018, Pages 724-728

  Rothhammer, Veit ^a   Borucki, Davis M ^a   Tjon, Emily C ^a   Takenaka, Maisa C ^a   Chao, Chun Cheih ^a   Ardura Fabregat, Alberto ^b   De Lima, Kalil Alves ^a   Gutiérrez Vázquez, Cristina ^a   Hewson, Patrick ^a   Staszewski, Ori ^b   Blain, Manon ^c   Healy, Luke ^c   Neziraj, Tradite ^a   Borio, Matilde ^a   Wheeler, Michael ^a   Dragin, Loic Lionel ^d   Laplaud, David A ^e   Antel, Jack ^c   Alvarez, Jorge Ivan ^d   Prinz, Marco ^b   Quintana, Francisco J ^a,f   more..

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF FREIBURG   (Germany)

^c MCGILL UNIVERSITY   (Canada)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e Centre National de la Recherche Scientifique   (France)

^f BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; CHEMOKINE RECEPTOR CX3CR1; EPIDERMAL GROWTH FACTOR RECEPTOR; TRANSFORMING GROWTH FACTOR ALPHA; VASCULOTROPIN A; VASCULOTROPIN B; FLT1 PROTEIN, MOUSE; LIPOPOLYSACCHARIDE RECEPTOR; TRYPTOPHAN; VASCULOTROPIN RECEPTOR 1;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTROCYTE; BONE MARROW CELL; CELL ACTIVATION; COMMENSAL; DISEASE ASSOCIATION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; LIGAND BINDING; METABOLITE; MICROGLIA; MOUSE; MULTIPLE SCLEROSIS; NERVE FIBER REGENERATION; NEUROMODULATION; NEUROTOXICITY; NONHUMAN; PROMOTER REGION; TRANSACTIVATION; UPREGULATION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CENTRAL NERVOUS SYSTEM; DEFICIENCY; DISEASE MODEL; FEMALE; INFLAMMATION; METABOLISM; MICROBIOLOGY; PATHOLOGY; SYMBIOSIS;

ANIMALS; ASTROCYTES; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; HUMANS; INFLAMMATION; LIPOPOLYSACCHARIDE RECEPTORS; MICE; MICE, INBRED C57BL; MICROGLIA; MULTIPLE SCLEROSIS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, ARYL HYDROCARBON; SYMBIOSIS; TRANSFORMING GROWTH FACTOR ALPHA; TRYPTOPHAN; VASCULAR ENDOTHELIAL GROWTH FACTOR B; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 85047764155     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/s41586-018-0119-x     Document Type: Article

References (35)

1. Ben Haim, L. & Rowitch, D. H. Functional diversity of astrocytes in neural circuit regulation. Nat. Rev. Neurosci. 18, 31-41 (2017).
2. Khakh, B. S. & Sofroniew, M. V. Diversity of astrocyte functions and phenotypes in neural circuits. Nat. Neurosci. 18, 942-952 (2015).
3. Sofroniew, M. V. Astrocyte barriers to neurotoxic inflammation. Nat. Rev. Neurosci. 16, 249-263 (2015).
4. Liddelow, S. A. & Barres, B. A. Reactive astrocytes: production, function, and therapeutic potential. Immunity 46, 957-967 (2017).
5. Prinz, M. & Priller, J. Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease. Nat. Rev. Neurosci. 15, 300-312 (2014).
6. Buttgereit, A. et al. Sall1 is a transcriptional regulator defining microglia identity and function. Nat. Immunol. 17, 1397-1406 (2016).
7. Lee, Y. H. et al. Aryl hydrocarbon receptor mediates both proinflammatory and anti-inflammatory effects in lipopolysaccharide-activated microglia. Glia 63, 1138-1154 (2015).
8. Goldmann, T. et al. A new type of microglia gene targeting shows TAK1 to be pivotal in CNS autoimmune inflammation. Nat. Neurosci. 16, 1618-1626 (2013).
9. Croxford, A. L. et al. The cytokine GM-CSF drives the inflammatory signature of CCR2+ monocytes and licenses autoimmunity. Immunity 43, 502-514 (2015).
10. Rothhammer, V. et al. Type I interferons and microbial metabolites of tryptophan modulate astrocyte activity and central nervous system inflammation via the aryl hydrocarbon receptor. Nat. Med. 22, 586-597 (2016).
11. Yeste, A. et al. Tolerogenic nanoparticles inhibit T cell-mediated autoimmunity through SOCS2. Sci. Signal. 9, ra61 (2016).
12. Matcovitch-Natan, O. et al. Microglia development follows a stepwise program to regulate brain homeostasis. Science 353, aad8670 (2016).
13. Liddelow, S. A. et al. Neurotoxic reactive astrocytes are induced by activated microglia. Nature 541, 481-487 (2017).
14. Quintana, F. J. & Sherr, D. H. Aryl hydrocarbon receptor control of adaptive immunity. Pharmacol. Rev. 65, 1148-1161 (2013).
15. Stockinger, B., Di Meglio, P., Gialitakis, M. & Duarte, J. H. The aryl hydrocarbon receptor: multitasking in the immune system. Annu. Rev. Immunol. 32, 403-432 (2014).
16. Mayo, L. et al. Regulation of astrocyte activation by glycolipids drives chronic CNS inflammation. Nat. Med. 20, 1147-1156 (2014).
17. Rothhammer, V. et al. Sphingosine 1-phosphate receptor modulation suppresses pathogenic astrocyte activation and chronic progressive CNS inflammation. Proc. Natl Acad. Sci. USA 114, 2012-2017 (2017).
18. Wheeler, M. A. & Quintana, F. J. Regulation of Astrocyte functions in multiple sclerosis. Cold Spring Harb. Perspect. Med. https://doi.org/10.1101/ cshperspect.a029009 (2018).
19. Gutiérrez-Vázquez, C. & Quintana, F. J. Regulation of the immune response by the aryl hydrocarbon receptor. Immunity 48, 19-33 (2018).
20. Wikoff, W. R. et al. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc. Natl Acad. Sci. USA 106, 3698-3703 (2009).
21. Girolamo, F., Coppola, C., Ribatti, D. & Trojano, M. Angiogenesis in multiple sclerosis and experimental autoimmune encephalomyelitis. Acta Neuropathol. Commun. 2, 84 (2014).
22. Mosher, K. I. et al. Neural progenitor cells regulate microglia functions and activity. Nat. Neurosci. 15, 1485-1487 (2012).
23. Mor, F., Quintana, F. J. & Cohen, I. R. Angiogenesis-inflammation cross-talk: vascular endothelial growth factor is secreted by activated T cells and induces Th1 polarization. J. Immunol. 172, 4618-4623 (2004).
24. Gaál, E. I. et al. Comparison of vascular growth factors in the murine brain reveals placenta growth factor as prime candidate for CNS revascularization. Blood 122, 658-665 (2013).
25. Li, X., Kumar, A., Zhang, F., Lee, C. & Tang, Z. Complicated life, complicated VEGF-B. Trends Mol. Med. 18, 119-127 (2012).
26. Nag, S., Eskandarian, M. R., Davis, J. & Eubanks, J. H. Differential expression of vascular endothelial growth factor-A (VEGF-A) and VEGF-B after brain injury. J. Neuropathol. Exp. Neurol. 61, 778-788 (2002).
27. Junier, M. P. What role(s) for TGF? in the central nervous system? Prog. Neurobiol. 62, 443-473 (2000).
28. White, R. E., Yin, F. Q. & Jakeman, L. B. TGF-? increases astrocyte invasion and promotes axonal growth into the lesion following spinal cord injury in mice. Exp. Neurol. 214, 10-24 (2008).
29. Anderson, M. A. et al. Astrocyte scar formation aids central nervous system axon regeneration. Nature 532, 195-200 (2016).
30. Kigerl, K. A. et al. Gut dysbiosis impairs recovery after spinal cord injury. J. Exp. Med. 213, 2603-2620 (2016).
31. Mildner, A. et al. Distinct and non-redundant roles of microglia and myeloid subsets in mouse models of Alzheimer's disease. J. Neurosci. 31, 11159-11171 (2011).
32. Mildner, A. et al. Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat. Neurosci. 10, 1544-1553 (2007).
33. Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protocols 7, 562-578 (2012).
34. Yan, Y. et al. CNS-specific therapy for ongoing EAE by silencing IL-17 pathway in astrocytes. Mol. Ther. 20, 1338-1348 (2012).
35. Jack, C. S. et al. TLR signaling tailors innate immune responses in human microglia and astrocytes. J. Immunol. 175, 4320-4330 (2005).