The commensal microbiota and viral infection: A comprehensive review

Frontiers in Immunology

Volumn 10, Issue JULY, 2019, Pages

  Li, Na ^a   Ma, Wen Tao ^a   Pang, Ming ^a   Fan, Qin Lei ^b   Hua, Jin Lian ^a  

^a NORTHWEST A F UNIVERSITY   (China)

^b China Animal Health and Epidemiology Center   (China)

Author keywords

Antibiotics; Antiviral immunity; Commensal microbiota; Germ free; Virus; Virus infectivity

Indexed keywords

CAPSID PROTEIN; GAMMA INTERFERON; GUANIDINE;

BACTERIUM ADHERENCE; CD8+ T LYMPHOCYTE; COMMENSAL; DNA REPLICATION; DYSBIOSIS; ENTEROCOCCUS FAECALIS; FECAL MICROBIOTA TRANSPLANTATION; GENE EXPRESSION; GENETIC RECOMBINATION; HELA CELL LINE; HEPATITIS B VIRUS; HEPATITIS C VIRUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE EVASION; IMMUNE SYSTEM; INFLUENZA VIRUS; INTESTINE FLORA; MICROBIAL COMMUNITY; MICROENVIRONMENT; MOUSE MAMMARY TUMOR VIRUS; NONHUMAN; NOROVIRUS; PATHOGENESIS; PERSISTENT VIRUS INFECTION; POLIOMYELITIS; PUBLIC HEALTH; REVIEW; SIMIAN VIRUS; TARGET CELL; TEMPERATURE; THEILER'S MURINE ENCEPHALOMYELITIS VIRUS; VIRUS GENOME; VIRUS INFECTION; VIRUS INFECTIVITY; VIRUS REPLICATION; VIRUS TRANSMISSION; HOMEOSTASIS; IMMUNOLOGY; VIRUS;

GASTROINTESTINAL MICROBIOME; HOMEOSTASIS; HUMANS; VIRUS DISEASES; VIRUSES;

EID: 85069437158     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2019.01551     Document Type: Review

References (152)

1. Proctor DM, Relman DA. The landscape ecology and microbiota of the human nose, mouth, and throat. Cell Host Microbe. (2017) 21:421-32. doi: 10.1016/j.chom.2017.03.011
2. Gimblet C, Meisel JS, Loesche MA, Cole SD, Horwinski J, Novais FO, et al. Cutaneous leishmaniasis induces a transmissible dysbiotic skin microbiota that promotes skin inflammation. Cell Host Microbe. (2017) 22:13-24 e4. doi: 10.1016/j.chom.2017.06.006
3. Whiteside SA, Razvi H, Dave S, Reid G, Burton JP. The microbiome of the urinary tract-a role beyond infection. Nat Rev Urol. (2015) 12:81-90. doi: 10.1038/nrurol.2014.361
4. Rothschild D, Weissbrod O, Barkan E, Kurilshikov A, Korem T, Zeevi D, et al. Environment dominates over host genetics in shaping human gut microbiota. Nature. (2018) 555:210-5. doi: 10.1038/nature25973
5. Borgo F, Garbossa S, Riva A, Severgnini M, Luigiano C, Benetti A, et al. Body mass index and sex affect diverse microbial niches within the gut. Front Microbiol. (2018) 9:213. doi: 10.3389/fmicb.2018.00213
6. Goodrich JK, Davenport ER, Beaumont M, Jackson MA, Knight R, Ober C, et al. Genetic determinants of the gut microbiome in UK twins. Cell Host Microbe. (2016) 19:731-43. doi: 10.1016/j.chom.2016.04.017
7. Faust K, Raes J. Host-microbe interaction: Rules of the game for microbiota. Nature. (2016) 534:182-3. doi: 10.1038/534182a
8. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell. (2005) 122:107-18. doi: 10.1016/j.cell.2005.05.007
9. Chung H, Pamp SJ, Hill JA, Surana NK, Edelman SM, Troy EB, et al. Gut immune maturation depends on colonization with a host-specific microbiota. Cell. (2012) 149:1578-93. doi: 10.1016/j.cell.2012.04.037
10. Bouskra D, Brezillon C, Berard M, Werts C, Varona R, Boneca IG, et al. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature. (2008) 456:507-10. doi: 10.1038/nature07450
11. Tremaroli V, Backhed F. Functional interactions between the gut microbiota and host metabolism. Nature. (2012) 489:242-9. doi: 10.1038/nature11552
12. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, et al. Host-gut microbiota metabolic interactions. Science. (2012) 336:1262-7. doi: 10.1126/science.1223813
13. Piewngam P, Zheng Y, Nguyen TH, Dickey SW, Joo HS, Villaruz AE, et al. Pathogen elimination by probiotic Bacillus via signalling interference. Nature. (2018) 562:532-7. doi: 10.1038/s41586-018-0616-y
14. Kim YG, Sakamoto K, Seo SU, Pickard JM, Gillilland MG, Pudlo NA, et al. Neonatal acquisition of Clostridia species protects against colonization by bacterial pathogens. Science. (2017) 356:312-5. doi: 10.1126/science.aag2029
15. Sassone-Corsi M, Nuccio SP, Liu H, Hernandez D, Vu CT, Takahashi AA, et al. Microcins mediate competition among Enterobacteriaceae in the inflamed gut. Nature. (2016) 540:280-283. doi: 10.1038/nature20557
16. Schuijt TJ, Lankelma JM, Scicluna BP, Melo FD, Roelofs TH, de Boer JD, et al. The gut microbiota plays a protective role in the host defence against pneumococcal pneumonia. Gut. (2016) 65:575-83. doi: 10.1136/gutjnl-2015-309728
17. Karst SM, The influence of commensal bacteria on infection with enteric viruses. Nat Rev Microbiol. (2016) 14:197-204. doi: 10.1038/nrmicro.2015.25
18. Berger AK, Mainou BA. Interactions between enteric bacteria and eukaryotic viruses impact the outcome of infection. Viruses. (2018) 10:19. doi: 10.3390/v10010019
19. Pfeiffer JK, Virgin HW. Viral immunity. Transkingdom control of viral infection and immunity in the mammalian intestine. Science. (2016) 351:5872. doi: 10.1126/science.aad5872
20. Sullender ME, Baldridge MT. Norovirus interactions with the commensal microbiota. PLoS Pathog. (2018) 14:e1007183. doi: 10.1371/journal.ppat.1007183
21. Robinson CM, Pfeiffer JK. Viruses and the microbiota. Ann Rev Virol. (2014) 1:55-69. doi: 10.1146/annurev-virology-031413-085550
22. Erickson AK, Jesudhasan PR, Mayer MJ, Narbad A, Winter SE, Pfeiffer JK. Bacteria facilitate enteric virus co-infection of mammalian cells and promote genetic recombination. Cell Host Microbe. (2018) 23:77-88 e5. doi: 10.1016/j.chom.2017.11.007
23. Kuss SK, Best GT, Etheredge CA, Pruijssers AJ, Frierson JM, Hooper LV, et al. Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science. (2011) 334:249-52. doi: 10.1126/science.1211057
24. Robinson CM, Jesudhasan PR, Pfeiffer JK. Bacterial lipopolysaccharide binding enhances virion stability and promotes environmental fitness of an enteric virus. Cell Host Microbe. (2014) 15:36-46. doi: 10.1016/j.chom.2013.12.004
25. Berger AK, Yi H, Kearns DB, Mainou BA. Bacteria and bacterial envelope components enhance mammalian reovirus thermostability. PLoS Pathog. (2017) 13:e1006768. doi: 10.1371/journal.ppat.1006768
26. Gorres KL, Daigle D, Mohanram S, Miller G. Activation and repression of Epstein-Barr Virus and Kaposi's sarcoma-associated herpesvirus lytic cycles by short- A nd medium-chain fatty acids. J Virol. (2014) 88:8028-44. doi: 10.1128/JVI.00722-14
27. Wilen CB, Lee S, Hsieh LL, Orchard RC, Desai C, Hykes BL Jr, et al. Tropism for tuft cells determines immune promotion of norovirus pathogenesis. Science. (2018) 360:204-8. doi: 10.1126/science.aar3799
28. von Moltke J, Ji M, Liang HE, Locksley RM. Tuft-cell-derived IL-25 regulates an intestinal ILC2-epithelial response circuit. Nature. (2016) 529:221-5. doi: 10.1038/nature16161
29. Jones MK, Watanabe M, Zhu S, Graves CL, Keyes LR, Grau KR, et al. Enteric bacteria promote human and mouse norovirus infection of B cells. Science. (2014) 346:755-9. doi: 10.1126/science.1257147
30. Kane M, Case LK, Kopaskie K, Kozlova A, MacDearmid C, Chervonsky AV, et al. Successful transmission of a retrovirus depends on the commensal microbiota. Science. (2011) 334:245-9. doi: 10.1126/science.1210718
31. Jude BA, Pobezinskaya Y, Bishop J, Parke S, Medzhitov RM, Chervonsky AV, et al. Subversion of the innate immune system by a retrovirus. Nat Immunol. (2003) 4:573-8. doi: 10.1038/ni926
32. Wilks J, Lien E, Jacobson AN, Fischbach MA, Qureshi N, Chervonsky AV, et al. Mammalian lipopolysaccharide receptors incorporated into the retroviral envelope augment virus transmission. Cell Host Microbe. (2015) 18:456-62. doi: 10.1016/j.chom.2015.09.005
33. Baldridge MT, Nice TJ, McCune BT, Yokoyama CC, Kambal A, Wheadon M, et al. Commensal microbes and interferon-lambda determine persistence of enteric murine norovirus infection. Science. (2015) 347:266-9. doi: 10.1126/science.1258025
34. Uchiyama R, Chassaing B, Zhang BY, Gewirtz AT. Antibiotic treatment suppresses rotavirus infection and enhances specific humoral immunity. J Infect Dis. (2014) 210:171-82. doi: 10.1093/infdis/jiu037
35. Young GR, Eksmond U, Salcedo R, Alexopoulou L, Stoye JP, Kassiotis G. Resurrection of endogenous retroviruses in antibody-deficient mice. Nature. (2012) 491:774-48. doi: 10.1038/nature11599
36. Aguilera ER, Erickson AK, Jesudhasan PR, Robinson CM, Pfeiffer JK. Plaques formed by mutagenized viral populations have elevated coinfection frequencies. MBio. (2017) 8:16. doi: 10.1128/mBio.02020-16
37. Chen YH, Du W, Hagemeijer MC, Takvorian PM, Pau C, Cali A, et al. Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses. Cell. (2015) 160:619-30. doi: 10.1016/j.cell.2015.01.032
38. Combe M, Garijo R, Geller R, Cuevas JM, Sanjuan R. Single-cell analysis of RNA virus infection identifies multiple genetically diverse viral genomes within single infectious units. Cell Host Microbe. (2015) 18:424-32. doi: 10.1016/j.chom.2015.09.009
39. Ma SD, Hegde S, Young KH, Sullivan R, Rajesh D, Zhou Y, et al. A new model of Epstein-Barr virus infection reveals an important role for early lytic viral protein expression in the development of lymphomas. J Virol. (2011) 85:165-77. doi: 10.1128/JVI.01512-10
40. Asai S, Nakamura Y, Yamamura M, Ikezawa H, Namikawa I. Quantitative analysis of the Epstein-Barr virus-inducing properties of short-chain fatty acids present in the culture fluids of oral bacteria. Arch Virol. (1991) 119:291-6. doi: 10.1007/BF01310678
41. 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. (2016) 165:1332-45. doi: 10.1016/j.cell.2016.05.041
42. Sawicki CM, Livingston KA, Obin M, Roberts SB, Chung M, McKeown NM. Dietary fiber and the human gut microbiota: Application of evidence mapping methodology. Nutrients. (2017) 9:125. doi: 10.3390/nu9020125
43. Lee S, Wilen CB, Orvedahl A, McCune BT, Kim KW, Orchard RC, et al. Norovirus cell tropism is determined by combinatorial action of a viral non-structural protein and host cytokine. Cell Host Microbe. (2017) 22:449-59 e4. doi: 10.1016/j.chom.2017.08.021
44. Haga K, Fujimoto A, Takai-Todaka R, Miki M, Doan YH, Murakami K, et al. Functional receptor molecules CD300lf and CD300ld within the CD300 family enable murine noroviruses to infect cells. Proc Natl Acad Sci USA. (2016) 113:E6248-55. doi: 10.1073/pnas.1605575113
45. Miura T, Sano D, Suenaga A, Yoshimura T, Fuzawa M, Nakagomi T, et al. Histo-blood group antigen-like substances of human enteric bacteria as specific adsorbents for human noroviruses. J Virol. (2013) 87:9441-51. doi: 10.1128/JVI.01060-13
46. Tedesco D, Thapa M, Chin CY, Ge Y, Gong M, Li J, et al. Alterations in intestinal microbiota lead to production of interleukin 17 by intrahepatic gammadelta T-cell receptor-positive cells and pathogenesis of cholestatic liver disease. Gastroenterology. (2018) 154:2178-93. doi: 10.1053/j.gastro.2018.02.019
47. Yu H, Gagliani N, Ishigame H, Huber S, Zhu S, Esplugues E, et al. Intestinal type 1 regulatory T cells migrate to periphery to suppress diabetogenic T cells and prevent diabetes development. Proc Natl Acad Sci USA. (2017) 114:10443-8. doi: 10.1073/pnas.1705599114
48. Zhao Q, Elson CO. Adaptive immune education by gut microbiota antigens. Immunology. (2018) 154:28-37. doi: 10.1111/imm.12896
49. Sefik E, Geva-Zatorsky N, Oh S, Konnikova L, Zemmour D, McGuire AM, et al. Individual intestinal symbionts induce a distinct population of RORgamma(+) regulatory T cells. Science. (2015) 349:993-7. doi: 10.1126/science.aaa9420
50. Jakobsson HE, Abrahamsson TR, Jenmalm MC, Harris K, Quince C, Jernberg C, et al. Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut. (2014) 63:559-66. doi: 10.1136/gutjnl-2012-303249
51. Tanoue T, Atarashi K, Honda K. Development and maintenance of intestinal regulatory T cells. Nat Rev Immunol. (2016) 16:295-309. doi: 10.1038/nri.2016.36
52. Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci USA. (2010) 107:12204-9. doi: 10.1073/pnas.0909122107
53. Basic M, Keubler LM, Buettner M, Achard M, Breves G, Schroder B, et al. Norovirus triggered microbiota-driven mucosal inflammation in interleukin 10-deficient mice. Inflamm Bowel Dis. (2014) 20:431-43. doi: 10.1097/01.MIB.0000441346.86827.ed
54. Botic T, Klingberg TD, Weingartl H, Cencic A. A novel eukaryotic cell culture model to study antiviral activity of potential probiotic bacteria. Int J Food Microbiol. (2007) 115:227-34. doi: 10.1016/j.ijfoodmicro.2006.10.044
55. Wang ZY, Chai WD, Burwinkel M, Twardziok S, Wrede P, Palissa C, et al. Inhibitory influence of Enterococcus faecium on the propagation of swine influenza A virus in vitro. PLoS ONE. (2013) 8:e53043. doi: 10.1371/journal.pone.0053043
56. Bandoro C, Runstadler JA. Bacterial lipopolysaccharide destabilizes influenza viruses. mSphere. (2017) 2:17. doi: 10.1128/mSphere.00267-17
57. Chen HW, Liu PF, Liu YT, Kuo S, Zhang XQ, Schooley RT, et al. Nasal commensal Staphylococcus epidermidis counteracts influenza virus. Sci Rep. (2016) 6:27870. doi: 10.1038/srep27870
58. Tuyama CG, Cheshenko N, Carlucci MJ, Li JH, Li H, Goldberg CL, et al. ACIDFORM inactivates herpes simplex virus and prevents genital herpes in a mouse model: Optimal candidate for microbicide combinations. J Infect Dis. (2006) 194:795-803. doi: 10.1086/506948
59. Conti C, Malacrino C, Mastromarino P. Inhibition of herpes simplex virus type 2 by vaginal lactobacilli. J Physiol Pharmacol. (2009) 60:19-26.
60. Mastromarino P, Cacciotti F, Masci A, Mosca L. Antiviral activity of Lactobacillus brevis towards herpes simplex virus type 2: Role of cell wall associated components. Anaerobe. (2011) 17:334-6. doi: 10.1016/j.anaerobe.2011.04.022
61. Steed AL, Christophi GP, Kaiko GE, Sun LL, Goodwin VM, Jain U, et al. The microbial metabolite desaminotyrosine protects from influenza through type I interferon. Science. (2017) 357:498-502. doi: 10.1126/science.aam5336
62. Yitbarek A, Alkie T, Taha-Abdelaziz K, Astill J, Rodriguez-Lecompte JC, Parkinson J, et al. Gut microbiota modulates type I interferon and antibody-mediated immune responses in chickens infected with influenza virus subtype H9N2. Benef Microbes. (2018) 9:417-27. doi: 10.3920/BM2017.0088
63. Hensley-McBain T, Zevin AS, Manuzak J, Smith E, Gile J, Miller C, et al. Effects of fecal microbial transplantation on microbiome and immunity in simian immunodeficiency virus-infected macaques. J Virol. (2016) 90:4981-9. doi: 10.1128/JVI.00099-16
64. Abt MC, Osborne LC, Monticelli LA, Doering TA, Alenghat T, Sonnenberg GF, et al. Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity. (2012) 37:158-70. doi: 10.1016/j.immuni.2012.04.011
65. Ichinohe T, Pang IK, Kumamoto Y, Peaper DR, Ho JH, Murray TS, et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci USA. (2011) 108:5354-9. doi: 10.1073/pnas.1019378108
66. Oh JE, Kim BC, Chang DH, Kwon M, Lee SY, Kang D, et al. Dysbiosis-induced IL-33 contributes to impaired antiviral immunity in the genital mucosa. Proc Natl Acad Sci USA. (2016) 113:E762-71. doi: 10.1073/pnas.1518589113
67. Gonzalez-Perez G, Lamouse-Smith ES, Gastrointestinal microbiome dysbiosis in infant mice alters peripheral CD8+ T cell receptor signaling. Front Immunol. (2017) 8:265. doi: 10.3389/fimmu.2017.00265
68. Wang Z, MacLeod DT, Di Nardo A. Commensal bacteria lipoteichoic acid increases skin mast cell antimicrobial activity against vaccinia viruses. J Immunol. (2012) 189:1551-8. doi: 10.4049/jimmunol.1200471
69. Gonzalez-Perez G, Hicks AL, Tekieli TM, Radens CM, Williams BL, Lamouse-Smith ES. Maternal antibiotic treatment impacts development of the neonatal intestinal microbiome and antiviral immunity. J Immunol. (2016) 196:3768-79. doi: 10.4049/jimmunol.1502322
70. Rosshart SP, Vassallo BG, Angeletti D, Hutchinson DS, Morgan AP, Takeda K, et al. Wild mouse gut microbiota promotes host fitness and improves disease resistance. Cell. (2017) 171:1015-28 e13. doi: 10.1016/j.cell.2017.09.016
71. Grayson MH, Camarda LE, Hussain SA, Zemple SJ, Hayward M, Lam V, et al. Intestinal microbiota disruption reduces regulatory T cells and increases respiratory viral infection mortality through increased IFNgamma production. Front Immunol. (2018) 9:1587. doi: 10.3389/fimmu.2018.01587
72. Chou HH, Chien WH, Wu LL, Cheng CH, Chung CH, Horng JH, et al. Age-related immune clearance of hepatitis B virus infection requires the establishment of gut microbiota. Proc Natl Acad Sci USA. (2015) 112:2175-80. doi: 10.1073/pnas.1424775112
73. Fuglsang E, Pizzolla A, Krych L, Nielsen DS, Brooks AG, Frokiaer H, et al. Changes in gut microbiota prior to influenza A virus infection do not affect immune responses in pups or juvenile mice. Front Cell Infect Microbiol. (2018) 8:319. doi: 10.3389/fcimb.2018.00319
74. Miedema F, Hazenberg MD, Tesselaar K, van Baarle D, de Boer RJ, Borghans JA. Immune activation and collateral damage in AIDS pathogenesis. Front Immunol. (2013) 4:298. doi: 10.3389/fimmu.2013.00298
75. Lu W, Feng Y, Jing F, Han Y, Lyu N, Liu F, et al. Association between gut microbiota and CD4 recovery in HIV-1 infected patients. Front Microbiol. (2018) 9:1451. doi: 10.3389/fmicb.2018.01451
76. Paquin-Proulx D, Ching C, Vujkovic-Cvijin I, Fadrosh D, Loh L, Huang Y, et al. Bacteroides are associated with GALT iNKT cell function and reduction of microbial translocation in HIV-1 infection. Mucosal Immunol. (2017) 10:69-78. doi: 10.1038/mi.2016.34
77. Stewart CJ, Mansbach JM, Ajami NJ, Petrosino JF, Zhu Z, Liang L, et al. Serum metabolome is associated with nasopharyngeal microbiota and disease severity among infants with bronchiolitis. J Infect Dis. (2019) 219:2005-14. doi: 10.1093/infdis/jiz021
78. de Steenhuijsen Piters WA, Heinonen S, Hasrat R, Bunsow E, Smith B, Suarez-Arrabal MC, et al. Nasopharyngeal microbiota, host transcriptome, and disease severity in children with respiratory syncytial virus infection. Am J Res Critic Care Med. (2016) 194:1104-15. doi: 10.1164/rccm.201602-0220OC
79. Terrault NA, Bzowej NH, Chang KM, Hwang JP, Jonas MM, Murad MH, et al. AASLD guidelines for treatment of chronic hepatitis B. Hepatology. (2016) 63:261-83. doi: 10.1002/hep.28156
80. Ren YD, Ye ZS, Yang LZ, Jin LX, Wei WJ, Deng YY, et al. Fecal microbiota transplantation induces hepatitis B virus e-antigen (HBeAg) clearance in patients with positive HBeAg after long-term antiviral therapy. Hepatology. (2017) 65:1765-8. doi: 10.1002/hep.29008
81. Haak BW, Littmann ER, Chaubard JL, Pickard AJ, Fontana E, Adhi F, et al. Impact of gut colonization with butyrate-producing microbiota on respiratory viral infection following allo-HCT. Blood. (2018) 131:2978-86. doi: 10.1182/blood-2018-01-828996
82. Gopinath S, Kim MV, Rakib T, Wong PW, van Zandt M, Barry NA, et al. Topical application of aminoglycoside antibiotics enhances host resistance to viral infections in a microbiota-independent manner. Nat Microbiol. (2018) 3:611-21. doi: 10.1038/s41564-018-0138-2
83. Zhu S, Jones MK, Hickman D, Han S, Reeves W, Karst SM. Norovirus antagonism of B-cell antigen presentation results in impaired control of acute infection. Mucosal Immunol. (2016) 9:1559-70. doi: 10.1038/mi.2016.15
84. Wilks J, Beilinson H, Theriault B, Chervonsky A, Golovkina T. Antibody-mediated immune control of a retrovirus does not require the microbiota. J Virol. (2014) 88:6524-7. doi: 10.1128/JVI.00251-14
85. Isaak DD, Bartizal KF, Caulfield MJ. Decreased pathogenicity of murine leukemia virus-Moloney in gnotobiotic mice. Leukemia. (1988) 2:540-4.
86. Kouttab NM, Jutila JW. Friend leukemia virus infection in germfree mice following antigen stimulation. J Immunol. (1972) 108:591-5.
87. Mirand EA, Grace JT Jr. Responses of germ-free mice to friend virus. Nature. (1963) 200:92-3. doi: 10.1038/200092a0
88. Ammann CG, Messer RJ, Peterson KE, Hasenkrug KJ. Lactate dehydrogenase-elevating virus induces systemic lymphocyte activation via TLR7-dependent IFNalpha responses by plasmacytoid dendritic cells. PLoS ONE. (2009) 4:e6105. doi: 10.1371/journal.pone.0006105
89. Wilks J, Golovkina T. Influence of microbiota on viral infections. PLoS Pathog. (2012) 8:e1002681. doi: 10.1371/journal.ppat.1002681
90. Kumar A, Vlasova AN, Deblais L, Huang HC, Wijeratne A, Kandasamy S, et al. Impact of nutrition and rotavirus infection on the infant gut microbiota in a humanized pig model. BMC Gastroenterol. (2018) 18:93. doi: 10.1186/s12876-018-0810-2
91. Jang JY, Kim S, Kwon MS, Lee J, Yu DH, Song RH, et al. Rotavirus-mediated alteration of gut microbiota and its correlation with physiological characteristics in neonatal calves. J Microbiol. (2018) 57:113-21. doi: 10.1007/s12275-019-8549-1
92. Ma X, Wang Q, Li H, Xu C, Cui N, Zhao X. 16S rRNA genes Illumina sequencing revealed differential cecal microbiome in specific pathogen free chickens infected with different subgroup of avian leukosis viruses. Vet Microbiol. (2017) 207:195-204. doi: 10.1016/j.vetmic.2017.05.016
93. Zhao N, Li M, Luo J, Wang S, Liu S, Wang S, et al. Impacts of canine distemper virus infection on the giant panda population from the perspective of gut microbiota. Sci Rep. (2017) 7:39954. doi: 10.1038/srep39954
94. Ding ZF, Cao MJ, Zhu XS, Xu GH, Wang RL. Changes in the gut microbiome of the Chinese mitten crab (Eriocheir sinensis) in response to White spot syndrome virus (WSSV) infection. J Fish Dis. (2017) 40:1561-71. doi: 10.1111/jfd.12624
95. Li Y, Saxena D, Chen Z, Liu G, Abrams WR, Phelan JA, et al. HIV infection and microbial diversity in saliva. J Clin Microbiol. (2014) 52:1400-11. doi: 10.1128/JCM.02954-13
96. Dang AT, Cotton S, Sankaran-Walters S, Li CS, Lee CY, Dandekar S, et al. Evidence of an increased pathogenic footprint in the lingual microbiome of untreated HIV infected patients. BMC Microbiol. (2012) 12:153. doi: 10.1186/1471-2180-12-153
97. Mukherjee PK, Chandra J, Retuerto M, Sikaroodi M, Brown RE, Jurevic R, et al. Oral mycobiome analysis of HIV-infected patients: Identification of Pichia as an antagonist of opportunistic fungi. PLoS Pathog. (2014) 10:e1003996. doi: 10.1371/journal.ppat.1003996
98. Cribbs SK, Uppal K, Li S, Jones DP, Huang L, Tipton L, et al. Correlation of the lung microbiota with metabolic profiles in bronchoalveolar lavage fluid in HIV infection. Microbiome. (2016) 4:3. doi: 10.1186/s40168-016-0147-4
99. Moeller AH, Shilts M, Li Y, Rudicell RS, Lonsdorf EV, Pusey AE, et al. SIV-induced instability of the chimpanzee gut microbiome. Cell Host Microbe. (2013) 14:340-5. doi: 10.1016/j.chom.2013.08.005
100. Degnan PH, Pusey AE, Lonsdorf EV, Goodall J, Wroblewski EE, Wilson ML, et al. Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park. Proc Natl Acad Sci USA. (2012) 109:13034-9. doi: 10.1073/pnas.1110994109
101. Noguera-Julian M, Rocafort M, Guillen Y, Rivera J, Casadella M, Nowak P, et al. Gut microbiota linked to sexual preference and HIV infection. EBioMed. (2016) 5:135-46. doi: 10.1016/j.ebiom.2016.01.032
102. Vujkovic-Cvijin I, Dunham RM, Iwai S, Maher MC, Albright RG, Broadhurst MJ, et al. Dysbiosis of the gut microbiota is associated with HIV disease progression and tryptophan catabolism. Sci Transl Med. (2013) 5:193ra91. doi: 10.1126/scitranslmed.3006438
103. Sun Y, Ma Y, Lin P, Tang YW, Yang L, Shen Y, et al. Fecal bacterial microbiome diversity in chronic HIV-infected patients in China. Emerg Microbes Infect. (2016) 5:e31. doi: 10.1038/emi.2016.25
104. Ji Y, Zhang F, Zhang R, Shen Y, Liu L, Wang J, et al. Changes in intestinal microbiota in HIV-1-infected subjects following cART initiation: Influence of CD4+ T cell count. Emerg Microbes Infect. (2018) 7:113. doi: 10.1038/s41426-018-0117-y
105. Serrano-Villar S, Rojo D, Martinez-Martinez M, Deusch S, Vazquez-Castellanos JF, Sainz T, et al. HIV infection results in metabolic alterations in the gut microbiota different from those induced by other diseases. Sci Rep. (2016) 6:26192. doi: 10.1038/srep26192
106. Mayuzumi H, Inagaki-Ohara K, Uyttenhove C, Okamoto Y, Matsuzaki G. Interleukin-17A is required to suppress invasion of Salmonella enterica serovar Typhimurium to enteric mucosa. Immunology. (2010) 131:377-85. doi: 10.1111/j.1365-2567.2010.03310.x
107. Raffatellu M, Santos RL, Verhoeven DE, George MD, Wilson RP, Winter SE, et al. Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat Med. (2008) 14:421-8. doi: 10.1038/nm1743
108. Manfredi R, Chiodo F. Salmonella typhi disease in HIV-infected patients: Case reports and literature review. Infez Med. (1999) 7:49-53.
109. Haas A, Zimmermann K, Graw F, Slack E, Rusert P, Ledergerber B, et al. Systemic antibody responses to gut commensal bacteria during chronic HIV-1 infection. Gut. (2011) 60:1506-19. doi: 10.1136/gut.2010.224774
110. Edouard S, Million M, Bachar D, Dubourg G, Michelle C, Ninove L, et al. The nasopharyngeal microbiota in patients with viral respiratory tract infections is enriched in bacterial pathogens. Eur J Clin Microbiol Infect Dis. (2018) 37:1725-33. doi: 10.1007/s10096-018-3305-8
111. Li Y, Ding J, Xiao Y, Xu B, He W, Yang Y, et al. 16S rDNA sequencing analysis of upper respiratory tract flora in patients with influenza H1N1 virus infection. Front Lab Med. (2017) 1:16-26. doi: 10.1016/j.flm.2017.02.005
112. Wen Z, Xie G, Zhou Q, Qiu C, Li J, Hu Q, et al. Distinct nasopharyngeal and oropharyngeal microbiota of children with influenza a virus compared with healthy children. BioMed Res Intl. (2018) 2018:6362716. doi: 10.1155/2018/6362716
113. Borges L, Giongo A, Pereira LM, Trindade FJ, Gregianini TS, Campos FS, et al. Comparison of the nasopharynx microbiome between influenza and non-influenza cases of severe acute respiratory infections: A pilot study. Health Science Rep. (2018) 1:e47. doi: 10.1002/hsr2.47
114. Ramos-Sevillano E, Wade WG, Mann A, Gilbert A, Lambkin-Williams R, Killingley B, et al. The effect of influenza virus on the human oropharyngeal microbiome. Clin Infect Dis. (2019) 68:1993-2002. doi: 10.1093/cid/ciy821
115. Yildiz S, Mazel-Sanchez B, Kandasamy M, Manicassamy B, Schmolke M. Influenza A virus infection impacts systemic microbiota dynamics and causes quantitative enteric dysbiosis. Microbiome. (2018) 6:9. doi: 10.1186/s40168-017-0386-z
116. Groves HT, Cuthbertson L, James P, Moffatt MF, Cox MJ, Tregoning JS. Respiratory disease following viral lung infection alters the murine gut microbiota. Front Immunol. (2018) 9:182. doi: 10.3389/fimmu.2018.00182
117. Zhao N, Wang SP, Li HY, Liu SL, Li M, Luo J, et al. Influence of novel highly pathogenic avian influenza A(H5N1) virus infection on migrating whooper swans fecal microbiota. Front Cell Infect Microbiol. (2018) 8:46. doi: 10.3389/fcimb.2018.00046
118. Wang J, Li FQ, Wei HM, Lian ZX, Sun R, Tian ZG. Respiratory influenza virus infection induces intestinal immune injury via microbiota-mediated Th17 cell-dependent inflammation. J Exp Med. (2014) 211:2397-410. doi: 10.1084/jem.20140625
119. Yitbarek A, Weese JS, Alkie TN, Parkinson J, Sharif S. Influenza A virus subtype H9N2 infection disrupts the composition of intestinal microbiota of chickens. Fems Microbiol Ecol. (2018) 94:165. doi: 10.1093/femsec/fix165
120. Deriu E, Boxx GM, He XS, Pan C, Benavidez SD, Cen LJ, et al. Influenza virus affects intestinal microbiota and secondary salmonella infection in the gut through type I interferons. Plos Pathog. (2016) 12:e1005572. doi: 10.1371/journal.ppat.1005572
121. Wang J, Wang Y, Zhang X, Liu J, Zhang Q, Zhao Y, et al. Gut microbial dysbiosis is associated with altered hepatic functions and serum metabolites in chronic hepatitis B patients. Front Microbiol. (2017) 8:2222. doi: 10.3389/fmicb.2017.02222
122. Xu M, Wang B, Fu Y, Chen Y, Yang F, Lu H, et al. Changes of fecal Bifidobacterium species in adult patients with hepatitis B virus-induced chronic liver disease. Microb Ecol. (2012) 63:304-13. doi: 10.1007/s00248-011-9925-5
123. Inoue T, Nakayama J, Moriya K, Kawaratani H, Momoda R, Ito K, et al. Gut dysbiosis associated with hepatitis C virus infection. Clin Infect Dis. (2018) 67:869-77. doi: 10.1093/cid/ciy205
124. Aly AM, Adel A, El-Gendy AO, Essam TM, Aziz RK. Gut microbiome alterations in patients with stage 4 hepatitis C. Gut Pathog. (2016) 8:42. doi: 10.1186/s13099-016-0124-2
125. Chen Y, Chen ZJ, Guo RY, Chen N, Lu HF, Huang SA, et al. Correlation between gastrointestinal fungi and varying degrees of chronic hepatitis B virus infection. Diagn Micr Infec Dis. (2011) 70:492-8. doi: 10.1016/j.diagmicrobio.2010.04.005
126. Heidrich B, Vital M, Plumeier I, Doscher N, Kahl S, Kirschner J, et al. Intestinal microbiota in patients with chronic hepatitis C with and without cirrhosis compared with healthy controls. Liver Int. (2018) 38:50-8. doi: 10.1111/liv.13485
127. Lu H, Wu Z, Xu W, Yang J, Chen Y, Li L. Intestinal microbiota was assessed in cirrhotic patients with hepatitis B virus infection. Intestinal microbiota of HBV cirrhotic patients. Microb Ecol. (2011) 61:693-703. doi: 10.1007/s00248-010-9801-8
128. Ling Z, Liu X, Cheng Y, Jiang X, Jiang H, Wang Y, et al. decreased diversity of the oral microbiota of patients with hepatitis B virus-induced chronic liver disease: A pilot project. Sci Rep. (2015) 5:17098. doi: 10.1038/srep17098
129. Zhao Y, Mao YF, Tang YS, Ni MZ, Liu QH, Wang Y, et al. Altered oral microbiota in chronic hepatitis B patients with different tongue coatings. World J Gastroenterol. (2018) 24:3448-61. doi: 10.3748/wjg.v24.i30.3448
130. Nelson AM, Walk ST, Taube S, Taniuchi M, Houpt ER, Wobus CE, et al. Disruption of the human gut microbiota following Norovirus infection. PLoS ONE. (2012) 7:e48224. doi: 10.1371/journal.pone.0048224
131. Almand EA, Moore MD, Outlaw J, Jaykus LA. Human norovirus binding to select bacteria representative of the human gut microbiota. PLoS ONE. (2017) 12:e0173124. doi: 10.1371/journal.pone.0173124
132. Kernbauer E, Ding Y, Cadwell K. An enteric virus can replace the beneficial function of commensal bacteria. Nature. (2014) 516:94-8. doi: 10.1038/nature13960
133. Martin CR, Osadchiy V, Kalani A, Mayer EA. The brain-gut-microbiome axis. Cell Mol Gastroenterol Hepatol. (2018) 6:133-48. doi: 10.1016/j.jcmgh.2018.04.003
134. O'Mahony SM, Clarke G, Borre YE, Dinan TG, Cryan JF. Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behav Brain Res. (2015) 277:32-48. doi: 10.1016/j.bbr.2014.07.027
135. Dinan TG, Cryan JF. Gut instincts: Microbiota as a key regulator of brain development, ageing and neurodegeneration. J Physiol. (2017) 595:489-503. doi: 10.1113/JP273106
136. de Lartigue G, de La Serre CB, Raybould HE. Vagal afferent neurons in high fat diet-induced obesity; intestinal microflora, gut inflammation and cholecystokinin. Physiol Behav. (2011) 105:100-5. doi: 10.1016/j.physbeh.2011.02.040
137. Park AJ, Collins J, Blennerhassett PA, Ghia JE, Verdu EF, Bercik P, et al. Altered colonic function and microbiota profile in a mouse model of chronic depression. Neurogastroent Motil. (2013) 25:733-E575. doi: 10.1111/nmo.12153
138. Pulikkan J, Mazumder A, Grace T. Role of the gut microbiome in autism spectrum disorders. Adv Exp Med Biol. (2019) 1118:253-69. doi: 10.1007/978-3-030-05542-4-13
139. Berer K, Mues M, Koutrolos M, Rasbi ZA, Boziki M, Johner C, et al. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature. (2011) 479:538-41. doi: 10.1038/nature10554
140. Mohajeri MH, La Fata G, Steinert RE, Weber P. Relationship between the gut microbiome and brain function. Nutr Rev. (2018) 76:481-96. doi: 10.1093/nutrit/nuy009
141. Osadchiy V, Martin CR, Mayer EA. The gut-brain axis and the microbiome: Mechanisms and clinical implications. Clin Gastroenterol. (2019) 17:322-32. doi: 10.1016/j.cgh.2018.10.002
142. Carrillo-Salinas FJ, Mestre L, Mecha M, Feliu A, Del Campo R, Villarrubia N, et al. Gut dysbiosis and neuroimmune responses to brain infection with Theiler's murine encephalomyelitis virus. Sci Rep. (2017) 7:44377. doi: 10.1038/srep44377
143. O'Toole PW, Marchesi JR, Hill C. Next-generation probiotics: The spectrum from probiotics to live biotherapeutics. Nat Microbiol. (2017) 2:17057. doi: 10.1038/nmicrobiol.2017.57
144. Zuo T, Wong SH, Lam K, Lui R, Cheung K, Tang W, et al. Bacteriophage transfer during faecal microbiota transplantation in Clostridium difficile infection is associated with treatment outcome. Gut. (2018) 67:634-43. doi: 10.1136/gutjnl-2017-313952
145. Suez J, Zmora N, Zilberman-Schapira G, Mor U, Dori-Bachash M, Bashiardes S, et al. Post-antibiotic gut mucosal microbiome reconstitution is impaired by probiotics and improved by autologous FMT. Cell. (2018) 174:1406-23 e16. doi: 10.1016/j.cell.2018.08.047
146. Zmora N, Zilberman-Schapira G, Suez J, Mor U, Dori-Bachash M, Bashiardes S, et al. Personalized gut mucosal colonization resistance to empiric probiotics is associated with unique host and microbiome features. Cell. (2018) 174:1388-405 e21. doi: 10.1016/j.cell.2018.08.041
147. Limon JJ, Skalski JH, Underhill DM. Commensal fungi in health and disease. Cell Host Microbe. (2017) 22:156-65. doi: 10.1016/j.chom.2017.07.002
148. Barnett KC, Coronas-Serna JM, Zhou W, Ernandes MJ, Cao A, Kranzusch PJ, et al. Phosphoinositide interactions position cGAS at the plasma membrane to ensure efficient distinction between self- A nd viral DNA cell. (2019) 176:1432-1446.e11. doi: 10.1016/j.cell.2019.01.049
149. Lian H, Wei J, Zang R, Ye W, Yang Q, Zhang XN, et al. ZCCHC3 is a co-sensor of cGAS for dsDNA recognition in innate immune response. Nat Commun. (2018) 9:3349. doi: 10.1038/s41467-018-05559-w
150. Seo GJ, Kim C, Shin WJ, Sklan EH, Eoh H, Jung JU. TRIM56-mediated monoubiquitination of cGAS for cytosolic DNA sensing. Nat Commun. (2018) 9:613. doi: 10.1038/s41467-018-02936-3
151. Schoggins JW, MacDuff DA, Imanaka N, Gainey MD, Shrestha B, Eitson JL, et al. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature. (2014) 505:691-5. doi: 10.1038/nature12862
152. Mann EA, Harmel-Laws E, Cohen MB, Steinbrecher KA. Guanylate cyclase C limits systemic dissemination of a murine enteric pathogen. BMC Gastroenterol. (2013) 13:135. doi: 10.1186/1471-230X-13-135