Microbiota-derived acetate protects against respiratory syncytial virus infection through a GPR43-type 1 interferon response

Nature Communications

Volumn 10, Issue 1, 2019, Pages

  Antunes, Krist Helen ^a   Fachi, José Luís ^b   de Paula, Rosemeire ^b   da Silva, Emanuelle Fraga ^a   Pral, Laís Passariello ^b   dos Santos, Adara Áurea ^c   Dias, Greicy Brisa Malaquias ^c   Vargas, José Eduardo ^d   Puga, Renato ^e   Mayer, Fabiana Quoos ^f   Maito, Fábio ^a   Zárate Bladés, Carlos R ^c   Ajami, Nadim J ^g   Sant’Ana, Marcella Ramos ^b   Candreva, Thamiris ^b   Rodrigues, Hosana Gomes ^b   Schmiele, Marcio ^h   Silva Clerici, Maria Teresa Pedrosa ^b   Proença Modena, José Luiz ^b   Vieira, Angélica Thomas ⁱ   Mackay, Charles R ^j   Mansur, Daniel ^c   Caballero, Mauricio T ^k   Marzec, Jacqui ^l   Li, Jianying ^l   Wang, Xuting ^l   Bell, Douglas ^l   Polack, Fernando P ^k,m   Kleeberger, Steven R ^l   Stein, Renato T ^a   Vinolo, Marco Aurélio Ramirez ^b   de Souza, Ana Paula Duarte ^a   more..

^a PONTIFICAL CATHOLIC UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b UNIVERSITY OF CAMPINAS   (Brazil)

^c FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^d UNIVERSITY OF PASSO FUNDO   (Brazil)

^e HOSPITAL ISRAELITA ALBERT EINSTEIN   (Brazil)

^f Veterinary Research Institute Desidério Finamor   (Brazil)

^g BAYLOR COLLEGE OF MEDICINE   (United States)

^h Federal University of the Jequitinhonha and Mucuri Valleys   (Brazil)

ⁱ FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^j MONASH UNIVERSITY   (Australia)

^k Ciudad Autónoma de Buenos Aires   (Argentina)

^l NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^m VANDERBILT UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; BETA INTERFERON; GPR43 PROTEIN; INTERFERON; PROTEIN; TYPE 1 INTERFERON; UNCLASSIFIED DRUG; ALPHA BETA INTERFERON RECEPTOR; FFAR2 PROTEIN, MOUSE; G PROTEIN COUPLED RECEPTOR; IFNAR1 PROTEIN, MOUSE; PROTECTIVE AGENT;

ACETATE; GENE; INFECTIVITY; MICROORGANISM; RESPIRATORY DISEASE; VIRUS;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL ACTIVITY; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; CYTOTOXICITY; EPITHELIUM CELL; FEMALE; GENE EXPRESSION; GENE FREQUENCY; HIGH FIBER DIET; IN VITRO STUDY; INTESTINE FLORA; LUNG ALVEOLUS CELL; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; MOUSE; NONHUMAN; PNEUMONIA; RESPIRATORY SYNCYTIAL VIRUS INFECTION; SIGNAL TRANSDUCTION; VERO CELL LINE; VIRUS LOAD; A-549 CELL LINE; ANIMAL; C57BL MOUSE; CELL LINE; CHLOROCEBUS AETHIOPS; DRUG EFFECT; GENETICS; HUMAN; KNOCKOUT MOUSE; LUNG; METABOLISM; MICROFLORA; SINGLE NUCLEOTIDE POLYMORPHISM; VIROLOGY;

MUS; RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

A549 CELLS; ACETATES; ANIMALS; CELL LINE; CHLOROCEBUS AETHIOPS; HUMANS; INTERFERON TYPE I; LUNG; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROBIOTA; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTECTIVE AGENTS; RECEPTOR, INTERFERON ALPHA-BETA; RECEPTORS, G-PROTEIN-COUPLED; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; VERO CELLS; VIRAL LOAD;

EID: 85070328736     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-019-11152-6     Document Type: Article

References (70)

1. Meissner, H. C. Viral bronchiolitis in children. N. Engl. J. Med. 374, 1793–1794 (2016).
2. Nair, H. et al. Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis. Lancet 375, 1545–1555 (2010).
3. Blanken, M. O., Rovers, M. M., Bont, L. & Dutch, R. S. V. N. N. Respiratory syncytial virus and recurrent wheeze. N. Engl. J. Med. 369, 782–783 (2013).
4. Mohapatra, S. S. & Boyapalle, S. Epidemiologic, experimental, and clinical links between respiratory syncytial virus infection and asthma. Clin. Microbiol. Rev. 21, 495–504 (2008).
5. Collins, P. L. & Melero, J. A. Progress in understanding and controlling respiratory syncytial virus: still crazy after all these years. Virus Res. 162, 80–99 (2011).
6. Barik, S. Respiratory syncytial virus mechanisms to interfere with type 1 interferons. Curr. Top. Microbiol. Immunol. 372, 173–191 (2013).
7. Schlender, J., Bossert, B., Buchholz, U. & Conzelmann, K. K. Bovine respiratory syncytial virus nonstructural proteins NS1 and NS2 cooperatively antagonize alpha/beta interferon-induced antiviral response. J. Virol. 74, 8234–8242 (2000).
8. Trompette, A. et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat. Med. 20, 159–166 (2014).
9. Maslowski, K. M. et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461, 1282–1286 (2009).
10. Thackray, L. B. et al. Oral antibiotic treatment of mice exacerbates the disease severity of multiple flavivirus infections. Cell Rep. 22, 3440–3453 e3446 (2018).
11. Koh, A., De Vadder, F., Kovatcheva-Datchary, P. & Backhed, F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 165, 1332–1345 (2016).
12. Rios-Covian, D. et al. Intestinal short chain fatty acids and their link with diet and human health. Front. Microbiol. 7, 185 (2016).
13. Park, J. et al. Short-chain fatty acids induce both effector and regulatory T cells by suppression of histone deacetylases and regulation of the mTOR-S6K pathway. Mucosal Immunol. 8, 80–93 (2015).
14. Furusawa, Y. et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504, 446–450 (2013).
15. Vieira, A. T. et al. Dietary fiber and the short-chain fatty acid acetate promote resolution of neutrophilic inflammation in a model of gout in mice. J. Leukoc. Biol. 101, 275–284 (2017).
16. Correa-Oliveira, R., Fachi, J. L., Vieira, A., Sato, F. T. & Vinolo, M. A. Regulation of immune cell function by short-chain fatty acids. Clin. Transl. Immunol. 5, e73 (2016).
17. Smith, P. M. et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341, 569–573 (2013).
18. Ferolla, F. M. et al. Macronutrients during pregnancy and life-threatening respiratory syncytial virus infections in children. Am. J. Respir. Crit. care Med. 187, 983–990 (2013).
19. Schijf, M. A. et al. Specific dietary oligosaccharides increase Th1 responses in a mouse respiratory syncytial virus infection model. J. Virol. 86, 11472–11482 (2012).
20. McFarlane, A. J. et al. Enteric helminth-induced type I interferon signaling protects against pulmonary virus infection through interaction with the microbiota. J. allergy Clin. Immunol. 140, 1068–1078 e1066 (2017).
21. Lynch, J. P. et al. Plasmacytoid dendritic cells protect from viral bronchiolitis and asthma through semaphorin 4a-mediated T reg expansion. J. Exp. Med., 10.1084/jem.20170298 (2017).
22. Thorburn, A. N. et al. Evidence that asthma is a developmental origin disease influenced by maternal diet and bacterial metabolites. Nat. Commun. 6, 7320 (2015).
23. Trompette, A. et al. Dietary fiber confers protection against flu by shaping Ly6c(-) patrolling monocyte hematopoiesis and CD8(+) T cell metabolism. Immunity 48, 992–1005 e1008 (2018).
24. Prado-Silva, L. P. et al. Sesame and resistant starch reduce the colon carcinogenesis and oxidative stress in 1,2-dimetilhydrazine-induced cancer in Wistar rats. Food Res. Int. 62, p609–p617 (2014).
25. Meehan, C. J. & Beiko, R. G. A phylogenomic view of ecological specialization in the Lachnospiraceae, a family of digestive tract-associated bacteria. Genome Biol. Evol. 6, 703–713 (2014).
26. Emeny, J. M. & Morgan, M. J. Susceptibility of various cells treated with interferon to the toxic effect of poly(rI).poly(rC) treatment. J. Gen. Virol. 43, 253–255 (1979).
27. Hiscott, J. Convergence of the NF-kappaB and IRF pathways in the regulation of the innate antiviral response. Cytokine Growth Factor Rev. 18, 483–490 (2007).
28. Honda, K., Takaoka, A. & Taniguchi, T. Type I interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors. Immunity 25, 349–360 (2006).
29. Caballero, M. T. et al. TLR4 genotype and environmental LPS mediate RSV bronchiolitis through Th2 polarization. J. Clin. Investig. 125, 571–582 (2015).
30. Wang, Y. et al. The first synthetic agonists of FFA2: Discovery and SAR of phenylacetamides as allosteric modulators. Bioorg. Med. Chem. Lett. 20, 493–498 (2010).
31. High, M. et al. Determinants of host susceptibility to murine respiratory syncytial virus (RSV) disease identify a role for the innate immunity scavenger receptor MARCO gene in human infants. EBioMedicine 11, 73–84 (2016).
32. Demoor, T. et al. IPS-1 signaling has a nonredundant role in mediating antiviral responses and the clearance of respiratory syncytial virus. J. Immunol. 189, 5942–5953 (2012).
33. Goritzka, M. et al. Alpha/beta interferon receptor signaling amplifies early proinflammatory cytokine production in the lung during respiratory syncytial virus infection. J. Virol. 88, 6128–6136 (2014).
34. Goritzka, M. et al. Alveolar macrophage-derived type I interferons orchestrate innate immunity to RSV through recruitment of antiviral monocytes. J. Exp. Med. 212, 699–714 (2015).
35. Kawashima, T. et al. Double-stranded RNA of intestinal commensal but not pathogenic bacteria triggers production of protective interferon-beta. Immunity 38, 1187–1197 (2013).
36. Abt, M. C. et al. Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity 37, 158–170 (2012).
37. Steed, A. L. et al. The microbial metabolite desaminotyrosine protects from influenza through type I interferon. Science 357, 498–502 (2017).
38. Schoggins, J. W. Interferon-stimulated genes: roles in viral pathogenesis. Curr. Opin. Virol. 6, 40–46 (2014).
39. Zhou, J. et al. A non-synonymous single nucleotide polymorphism in IFNAR1 affects susceptibility to chronic hepatitis B virus infection. J. viral Hepat. 16, 45–52 (2009).
40. Dhar, J. et al. 2’-5’-Oligoadenylate Synthetase-like Protein Inhibits Respiratory Syncytial Virus Replication And Is Targeted By The Viral Nonstructural Protein 1. J. Virol. 89, 10115–10119 (2015).
41. Ling, Z., Tran, K. C. & Teng, M. N. Human respiratory syncytial virus nonstructural protein NS2 antagonizes the activation of beta interferon transcription by interacting with RIG-I. J. Virol. 83, 3734–3742 (2009).
42. Ren, J. et al. A novel mechanism for the inhibition of interferon regulatory factor-3-dependent gene expression by human respiratory syncytial virus NS1 protein. J. Gen. Virol. 92, 2153–2159 (2011).
43. Whelan, J. N., Tran, K. C., van Rossum, D. B. & Teng, M. N. Identification of respiratory syncytial virus nonstructural protein 2 residues essential for exploitation of the host ubiquitin system and inhibition of innate immune responses. J. Virol. 90, 6453–6463 (2016).
44. Zhang, Y., Yang, L., Wang, H., Zhang, G. & Sun, X. Respiratory syncytial virus non-structural protein 1 facilitates virus replication through miR-29a-mediated inhibition of interferon-alpha receptor. Biochem. Biophys. Res. Commun. 478, 1436–1441 (2016).
45. Ravi, L. I. et al. A systems-based approach to analyse the host response in murine lung macrophages challenged with respiratory syncytial virus. BMC Genom. 14, 190 (2013).
46. Thomas, C. et al. Structural linkage between ligand discrimination and receptor activation by type I interferons. Cell 146, 621–632 (2011).
47. Li, H., Sharma, N., General, I. J., Schreiber, G. & Bahar, I. Dynamic modulation of binding affinity as a mechanism for regulating interferon signaling. J. Mol. Biol. 429, 2571–2589 (2017).
48. Song le, H. et al. Association of two variants of the interferon-alpha receptor-1 gene with the presentation of hepatitis B virus infection. Eur. cytokine Netw. 19, 204–210 (2008).
49. He, X. X. et al. Persistent effect of IFNAR-1 genetic polymorphism on the long-term pathogenesis of chronic HBV infection. Viral Immunol. 23, 251–257 (2010).
50. Diop, G. et al. Exhaustive genotyping of the interferon alpha receptor 1 (IFNAR1) gene and association of an IFNAR1 protein variant with AIDS progression or susceptibility to HIV-1 infection in a French AIDS cohort. Biomed. Pharmacother. Biomedecine Pharmacother. 60, 569–577 (2006).
51. Bridgman, S. L. et al. Fecal short-chain fatty acid variations by breastfeeding status in infants at 4 months: differences in relative versus absolute concentrations. Front. Nutr. 4, 11 (2017).
52. Dos Santos, P. F. et al. ISG15-induced IL-10 is a novel anti-inflammatory myeloid axis disrupted during active tuberculosis. J. Immunol. 200, 1434–1442 (2018).
53. Vinolo, M. A. et al. Suppressive effect of short-chain fatty acids on production of proinflammatory mediators by neutrophils. J. Nutr. Biochem. 22, 849–855 (2011).
54. Vinolo, M. A. et al. SCFAs induce mouse neutrophil chemotaxis through the GPR43 receptor. PloS ONE 6, e21205 (2011).
55. Correa, R. O. et al. Bacterial short-chain fatty acid metabolites modulate the inflammatory response against infectious bacteria. Cell. Microbiol. 19, e12720 (2017).
56. Imoto, Y. et al. Short-chain fatty acids induce tissue plasminogen activator in airway epithelial cells via GPR41&43. Clin. Exp. Allergy 48, 544–554 (2018).
57. Kim, M. H., Kang, S. G., Park, J. H., Yanagisawa, M. & Kim, C. H. Short-chain fatty acids activate GPR41 and GPR43 on intestinal epithelial cells to promote inflammatory responses in mice. Gastroenterology 145, 396-406–e391-310 (2013).
58. Kimura, I. et al. The gut microbiota suppresses insulin-mediated fat accumulation via the short-chain fatty acid receptor GPR43. Nat. Commun. 4, 1829 (2013).
59. Vieira, A. T. et al. A role for gut microbiota and the metabolite-sensing receptor GPR43 in a murine model of gout.Arthritis Rheumatol. 67, 1646–1656 (2015).
60. Galvão I. T. L. et al The metabolic sensor GPR43 receptor plays a role in the control of Klebsiella pneumonie infection in the lung. Front. Immunol., 10.3389/fimmu.2018.00142 (2018).
61. Zhao, Y. et al. GPR43 mediates microbiota metabolite SCFA regulation of antimicrobial peptide expression in intestinal epithelial cells via activation of mTOR and STAT3. Mucosal Immunol. 11, 752–762 (2018).
62. Sagheddu, V., Patrone, V., Miragoli, F., Puglisi, E. & Morelli, L. Infant early gut colonization by lachnospiraceae: high frequency of Ruminococcus gnavus. Front. Pediatr. 4, 57 (2016).
63. Groves, H. T. et al. Respiratory disease following viral lung infection alters the murine gut microbiota. Front. Immunol. 9, 182 (2018).
64. Hashemi, Z., Fouhse, J., Im, H. S., Chan, C. B. & Willing, B. P. Dietary pea fiber supplementation improves glycemia and induces changes in the composition of gut microbiota, serum short chain fatty acid profile and expression of mucins in glucose intolerant rats. Nutrients, 10.3390/nu9111236 (2017).
65. Barends, M. et al. Timing of infection and prior immunization with respiratory syncytial virus (RSV) in RSV-enhanced allergic inflammation. J. Infect. Dis. 189, 1866–1872 (2004).
66. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).
67. Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic acids Res. 41, D590–D596 (2013).
68. Ajami, N. J., Cope, J. L., Wong, M. C., Petrosino, J. F. & Chesnel, L. Impact of oral fidaxomicin administration on the intestinal microbiota and susceptibility to Clostridium difficile colonization in mice. Antimicrob. Agents Chemother., 10.1128/AAC.02112-17 (2018).
69. Stewart, C. J. et al. Temporal development of the gut microbiome in early childhood from the TEDDY study. Nature 562, 583–588 (2018).
70. Fellows, R. et al. Microbiota derived short chain fatty acids promote histone crotonylation in the colon through histone deacetylases. Nat. Commun. 9, 105 (2018).