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Research Paper

Systemic exposure to bacterial amyloid curli alters the gut mucosal immune response and the microbiome, exacerbating Salmonella-induced arthritis

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Article: 2221813 | Received 25 Jan 2023, Accepted 31 May 2023, Published online: 14 Jun 2023

References

  • Schnabel J. Protein folding: the dark side of proteins. Nature. 2010;464(7290):828–18. doi:10.1038/464828a.
  • Ross CA, Poirier MA. Protein aggregation and neurodegenerative disease. Nat Med. 2004;10(Suppl):S10–7. doi:10.1038/nm1066.
  • Hull RL, Rebecca L, Westermark, GT ,Westermark, P and Kahn, SE. Islet amyloid: a critical entity in the pathogenesis of type 2 diabetes. J Clin Endocrinol Metab. 2004;89(8):3629–3643. doi:10.1210/jc.2004-0405.
  • Cherny I,Rockah, L, Levy-Nissenbaum, O, Gophna, Uri, Ron, EZ, Gazit, E. The formation of Escherichia coli curli amyloid fibrils is mediated by prion-like peptide repeats. J Mol Biol. 2005;352(2):245–252. doi:10.1016/j.jmb.2005.07.028.
  • Barnhart MM, Chapman MR. Curli biogenesis and function. Annu Rev Microbiol. 2006;60(1):131–147. doi:10.1146/annurev.micro.60.080805.142106.
  • Chapman MR, Robinson, LS, Pinkner, JS, Roth, R Heuser, J Hammar, M Normark, S Hultgren, SJ. Role of Escherichia coli curli operons in directing amyloid fiber formation. Science. 2002;295(5556):851–855. doi:10.1126/science.1067484.
  • Hufnagel DA, Tukel C, Chapman MR, True HL, True HL. Disease to dirt: the biology of microbial amyloids. PLoS Pathog. 2013;9(11):e1003740. doi:10.1371/journal.ppat.1003740.
  • Tursi S, Puligedda RD, Szabo P, Nicastro LK, Miller AL, Qiu C, Gallucci S, Relkin NR, Buttaro BA, Dessain SK, et al. Salmonella Typhimurium biofilm disruption by a human antibody that binds a pan-amyloid epitope on curli. Nat Commun. 2020;11(1). doi:10.1038/s41467-020-14685-3.
  • Tursi SA, Tukel C. Curli-containing enteric biofilms inside and out: matrix composition, immune recognition, and disease implications. Microbiol Mol Biol Rev. 2018;82(4). doi:10.1128/MMBR.00028-18.
  • White AP, Gibson, DL, Kim, W, Kay, WW, Surette, MG. Thin aggregative fimbriae and cellulose enhance long-term survival and persistence of Salmonella. J Bacteriol. 2006;188(9):3219–3227. doi:10.1128/JB.188.9.3219-3227.2006.
  • Vidakovic L, Singh PK, Hartmann R, Nadell CD, Drescher K. Dynamic biofilm architecture confers individual and collective mechanisms of viral protection. Nat Microbiol. 2018;3(1):26–31. doi:10.1038/s41564-017-0050-1.
  • McCrate OA, Zhou, X, Reichhardt, C, Cegelski, L. Sum of the parts: composition and architecture of the bacterial extracellular matrix. J Mol Biol. 2013;425(22):4286–4294. doi:10.1016/j.jmb.2013.06.022.
  • Tukel C, Raffatellu M, Humphries AD, Wilson RP, Andrews-Polymenis HL, Gull T, Figueiredo JF, Wong MH, Michelsen KS, Akçelik M, et al. CsgA is a pathogen-associated molecular pattern of Salmonella enterica serotype typhimurium that is recognized by Toll-like receptor 2. Mol Microbiol. 2005;58(1):289–304. doi:10.1111/j.1365-2958.2005.04825.x.
  • Hoshino K, Takeuchi, O, Kawai, T, Sanjo, H, Ogawa, T, Takeda, Y, Takeda, K Akira, S. Cutting edge: toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol. 1999;162(7):3749–3752. doi:10.4049/jimmunol.162.7.3749.
  • Gewirtz AT, Navas, TA, Lyons, S, Godowski, PJ, Madara, JL. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol. 2001;167(4):1882–1885. doi:10.4049/jimmunol.167.4.1882.
  • Franchi L, Amer A, Body-Malapel M, Kanneganti T-D, Özören N, Jagirdar R, Inohara N, Vandenabeele P, Bertin J, Coyle A, et al. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1β in salmonella-infected macrophages. Nat Immunol. 2006;7(6):576–582. doi:10.1038/ni1346.
  • Miao EA, Alpuche-Aranda CM, Dors M, Clark AE, Bader MW, Miller SI, Aderem A. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1β via Ipaf. Nat Immunol. 2006;7(6):569–575. doi:10.1038/ni1344.
  • Miller AL, Nicastro, LK, Bessho, S, Grando, K, White, AP, Zhang, Yi, Queisser, G, Buttaro, BA, Tukel, C. Nitrate is an Environmental Cue in the Gut for Salmonella enterica Serovar Typhimurium Biofilm Dispersal through Curli Repression and Flagellum Activation via Cyclic-di-GMP Signaling. mBio. 2022;13(1):e0288621. doi:10.1128/mbio.02886-21.
  • Tukel C, Nishimori JH, Wilson RP, Winter MG, Keestra AM, Van Putten JPM, Bäumler AJ. Toll-like receptors 1 and 2 cooperatively mediate immune responses to curli, a common amyloid from enterobacterial biofilms. Cell Microbiol. 2010;12(10):1495–1505. doi:10.1111/j.1462-5822.2010.01485.x.
  • Rapsinski GJ, Wynosky-Dolfi, MA, Oppong, GO, Tursi, SA, Wilson, RP, Brodsky, IE, Tukel, C. Toll-Like Receptor 2 and NLRP3 Cooperate to Recognize a Functional Bacterial Amyloid, Curli. Infect Immun. 2015;83(2):693–701. doi:10.1128/IAI.02370-14.
  • Tukel C, Wilson RP, Nishimori JH, Pezeshki M, Chromy BA, Bäumler AJ. Responses to amyloids of microbial and host origin are mediated through Toll-like receptor 2. Cell Host & Microbe. 2009;6(1):45–53. doi:10.1016/j.chom.2009.05.020.
  • Tursi SA, Lee, EY, Medeiros, NJ, Lee, MH, Nicastro, LK, Buttaro, B, Gallucci, S, Wilson, RP, Wong, GCL, Tukel, C. Bacterial amyloid curli acts as a carrier for DNA to elicit an autoimmune response via TLR2 and TLR9. PLoS Pathog. 2017;13(4):e1006315. doi:10.1371/journal.ppat.1006315.
  • Gallo PM, Rapsinski, GJ, Wilson, RP, Oppong, GO, Sriram, U, Goulian, M, Buttaro, B, Caricchio, R, Gallucci, S, Tukel, C. Amyloid-DNA Composites of Bacterial Biofilms Stimulate Autoimmunity. Immunity. 2015;42(6):1171–1184. doi:10.1016/j.immuni.2015.06.002.
  • Nishimori JH, Newman, TN, Oppong, GO, Rapsinski, GJ, Yen, JH, Biesecker, SG, Wilson, RP, Butler, BP, Winter, MG, Tsolis, RM. Microbial amyloids induce interleukin 17A (IL-17A) and IL-22 responses via Toll-like receptor 2 activation in the intestinal mucosa. Infect Immun. 2012;80(12):4398–4408. doi:10.1128/IAI.00911-12.
  • Miller AL. Microbiome or Infections: amyloid-Containing Biofilms as a Trigger for Complex Human Diseases. Front Immunol. 2021;12:638867. doi:10.3389/fimmu.2021.638867.
  • Sampson TR, Challis C, Jain N, Moiseyenko A, Ladinsky MS, Shastri GG, Thron T, Needham BD, Horvath I, Debelius JW, et al. A gut bacterial amyloid promotes α-synuclein aggregation and motor impairment in mice. Elife. 2020;9:9. doi:10.7554/eLife.53111.
  • Chen SG, Stribinskis V, Rane MJ, Demuth DR, Gozal E, Roberts AM, Jagadapillai R, Liu R, Choe K, Shivakumar B, et al. Exposure to the functional bacterial amyloid protein curli enhances alpha-synuclein aggregation in aged Fischer 344 rats and Caenorhabditis elegans. Sci Rep. 2016;6(1):34477. doi:10.1038/srep34477.
  • Friedland RP, Chapman MR, Bliska JB. The role of microbial amyloid in neurodegeneration. PLoS Pathog. 2017;13(12):e1006654. doi:10.1371/journal.ppat.1006654.
  • Nicastro L, Tukel C. Bacterial amyloids: the link between bacterial infections and autoimmunity. Trends Microbiol. 2019;27(11):954–963. doi:10.1016/j.tim.2019.07.002.
  • Miller AL, Pasternak JA, Medeiros NJ, Nicastro LK, Tursi SA, Hansen EG, Krochak R, Sokaribo AS, MacKenzie KD, Palmer MB, et al. In vivo synthesis of bacterial amyloid curli contributes to joint inflammation during S. Typhimurium Infect PLoS Pathog. 2020;16(7):e1008591. doi:10.1371/journal.ppat.1008591.
  • Pachucki RJ, Corradetti C, Kohler L, Ghadiali J, Gallo PM, Nicastro L, Tursi SA, Gallucci S, Tükel Ç, Caricchio R. Persistent bacteriuria and antibodies recognizing curli/eDNA complexes from Escherichia coli are linked to flares in systemic lupus erythematosus. Arthritis Rheumatol. 2020;72(11):1872–1881. doi:10.1002/art.41400.
  • Candelli M, Franza L, Pignataro G, Ojetti V, Covino M, Piccioni A, Gasbarrini A, Franceschi F. Interaction between lipopolysaccharide and gut microbiota in inflammatory bowel diseases. IJMS. 2021;22(12):6242. doi:10.3390/ijms22126242.
  • Tran HQ, Ley RE, Gewirtz AT, Chassaing B. Flagellin-elicited adaptive immunity suppresses flagellated microbiota and vaccinates against chronic inflammatory diseases. Nat Commun. 2019;10(1):5650. doi:10.1038/s41467-019-13538-y.
  • Lohr J, Knoechel, B, Wang, JJ, Villarino, AV, Abbas, AK. Role of IL-17 and regulatory T lymphocytes in a systemic autoimmune disease. J Exp Med. 2006;203(13):2785–2791. doi:10.1084/jem.20061341.
  • Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, Wei D, Goldfarb KC, Santee CA, Lynch SV, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009;139(3):485–498. doi:10.1016/j.cell.2009.09.033.
  • Nicastro LK, Tursi SA, Le LS, Miller AL, Efimov A, Buttaro B, Tam V, Tükel Ç. Cytotoxic curli intermediates form during salmonella biofilm development. J Bacteriol. 2019;201(18). doi:10.1128/JB.00095-19.
  • Nicastro LK, de Anda, J, Jain, N, Grando, KCM, Miller, AL, Bessho, S, Gallucci, S, Wong, GCL, Tukel, C. Assembly of ordered DNA-curli fibril complexes during Salmonella biofilm formation correlates with strengths of the type I interferon and autoimmune responses. PLoS Pathog. 2022;18(8):e1010742. doi:10.1371/journal.ppat.1010742.
  • Pan M, Kang I, Craft J, Yin Z. Resistance to development of collagen-induced arthritis in C57BL/6 mice is due to a defect in secondary, but not in primary, immune response. J Clin Immunol. 2004;24(5):481–491. doi:10.1023/B:JOCI.0000040919.16739.44.
  • Macfarlane S, Bahrami B, Macfarlane GT. Mucosal biofilm communities in the human intestinal tract. Adv Appl Microbiol. 2011;75:111–143.
  • Lu H, Que Y, Wu X, Guan T, Guo H. Metabolomics deciphered metabolic reprogramming required for biofilm formation. Sci Rep. 2019;9(1):13160. doi:10.1038/s41598-019-49603-1.
  • Hathroubi S, Mekni MA, Domenico P, Nguyen D, Jacques M. Biofilms: microbial shelters against antibiotics. Microb Drug Resist. 2017;23(2):147–156. doi:10.1089/mdr.2016.0087.
  • Hoiby N. A short history of microbial biofilms and biofilm infections. APMIS. 2017;125(4):272–275. doi:10.1111/apm.12686.
  • Koo H, Allan, RN, Howlin, RP, Stoodley, P, Hall-Stoodley, L. Targeting microbial biofilms: current and prospective therapeutic strategies. Nat Rev Microbiol. 2017;15(12):740–755. doi:10.1038/nrmicro.2017.99.
  • Tamayo R, Patimalla B, Camilli A. Growth in a biofilm induces a hyperinfectious phenotype in Vibrio cholerae. Infect Immun. 2010;78(8):3560–3569. doi:10.1128/IAI.00048-10.
  • Gallego-Hernandez AL, DePas WH, Park JH, Teschler JK, Hartmann R, Jeckel H, Drescher K, Beyhan S, Newman DK, Yildiz FH, et al. Upregulation of virulence genes promotes Vibrio cholerae biofilm hyperinfectivity. Proc Natl Acad Sci USA. 2020;117(20):11010–11017. doi:10.1073/pnas.1916571117.
  • Di Domizio J, Zhang R, Stagg LJ, Gagea M, Zhuo M, Ladbury JE, Cao W. Binding with nucleic acids or glycosaminoglycans converts soluble protein oligomers to amyloid. J Biol Chem. 2012;287(1):736–747. doi:10.1074/jbc.M111.238477.
  • Jimenez JS. Protein-DNA interaction at the origin of neurological diseases: a hypothesis. J Alzheimers Dis. 2010;22(2):375–391. doi:10.3233/JAD-2010-100189.
  • Maloney B, Lahiri DK. The Alzheimer’s amyloid beta-peptide (Abeta) binds a specific DNA Abeta-interacting domain (AbetaID) in the APP, BACE1, and APOE promoters in a sequence-specific manner: characterizing a new regulatory motif. Gene. 2011;488(1–2):1–12. doi:10.1016/j.gene.2011.06.004.
  • Grando K, Nicastro LK, Tursi SA, De Anda J, Lee EY, Wong GCL, Tükel Ç. Phenol-soluble modulins from staphylococcus aureus biofilms form complexes with DNA to drive autoimmunity. Front Cell Infect Microbiol. 2022;12. doi:10.3389/fcimb.2022.884065.
  • Oppong GO. Epithelial cells augment barrier function via activation of the toll-like receptor 2/phosphatidylinositol 3-kinase pathway upon recognition of salmonella enterica serovar typhimurium curli fibrils in the gut. Infect Immun. 2013;81(2):478–486. doi:10.1128/IAI.00453-12.
  • Alduraibi FK, Sullivan, KA, Chatham, WW, Hsu, HC, Mountz, JD. Interrelation of T cell cytokines and autoantibodies in systemic lupus erythematosus: a cross-sectional study. Clin Immunol. 2023;247:109239. doi:10.1016/j.clim.2023.109239.
  • Chaurasia S, Shasany AK, Aggarwal A, Misra R. Recombinant Salmonella typhimurium outer membrane protein a is recognized by synovial fluid CD8 cells and stimulates synovial fluid mononuclear cells to produce interleukin (IL)-17/IL-23 in patients with reactive arthritis and undifferentiated spondyloarthropathy. Clin Exp Immunol. 2016;185(2):210–218. doi:10.1111/cei.12799.
  • Terui H, Yamasaki K, Wada-Irimada M, Onodera-Amagai M, Hatchome N, Mizuashi M, Yamashita R, Kawabe T, Ishii N, Abe T, et al. Staphylococcus aureus skin colonization promotes SLE-like autoimmune inflammation via neutrophil activation and the IL-23/IL-17 axis. Sci Immunol. 2022;7(76):eabm9811. doi:10.1126/sciimmunol.abm9811.
  • Vijay-Kumar M, Aitken JD, Carvalho FA, Cullender TC, Mwangi S, Srinivasan S, Sitaraman SV, Knight R, Ley RE, Gewirtz AT, et al. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science. 2010;328(5975):228–231. doi:10.1126/science.1179721.
  • Alpizar-Rodriguez D, Lesker TR, Gronow A, Gilbert B, Raemy E, Lamacchia C, Gabay C, Finckh A, Strowig T. Prevotella copri in individuals at risk for rheumatoid arthritis. Ann Rheum Dis. 2019;78(5):590–593. doi:10.1136/annrheumdis-2018-214514.
  • Azzouz D, Omarbekova A, Heguy A, Schwudke D, Gisch N, Rovin BH, Caricchio R, Buyon JP, Alekseyenko AV, Silverman GJ, et al. Lupus nephritis is linked to disease-activity associated expansions and immunity to a gut commensal. Ann Rheum Dis. 2019;78(7):947–956. doi:10.1136/annrheumdis-2018-214856.
  • Ishigame H, Kakuta S, Nagai T, Kadoki M, Nambu A, Komiyama Y, Fujikado N, Tanahashi Y, Akitsu A, Kotaki H, et al. Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity. 2009;30(1):108–119. doi:10.1016/j.immuni.2008.11.009.
  • Lawrence AE, Berger RP, Hill DR, Huang S, Yadagiri VK, Bons B, Fields C, Sule GJ, Knight JS, Wobus CE, et al. Human neutrophil IL1β directs intestinal epithelial cell extrusion during Salmonella infection. PLoS Pathog. 2022;18(10):e1010855. doi:10.1371/journal.ppat.1010855.
  • Migliorini P, Italiani P, Pratesi F, Puxeddu I, Boraschi D. The IL-1 family cytokines and receptors in autoimmune diseases. Autoimmun Rev. 2020;19(9):102617. doi:10.1016/j.autrev.2020.102617.
  • Shlomchik MJ, Weisel F. Germinal center selection and the development of memory B and plasma cells. Immunol Rev. 2012;247(1):52–63. doi:10.1111/j.1600-065X.2012.01124.x.
  • Herlands RA, William J, Hershberg U, Shlomchik MJ. Anti-chromatin antibodies drive in vivo antigen-specific activation and somatic hypermutation of rheumatoid factor B cells at extrafollicular sites. Eur J Immunol. 2007;37(12):3339–3351. doi:10.1002/eji.200737752.
  • Sang A, Niu H, Cullen J, Choi SC, Zheng YY, Wang H, Shlomchik MJ, Morel L. Activation of rheumatoid factor–specific b cells is antigen dependent and occurs preferentially outside of germinal centers in the lupus-prone NZM2410 mouse model. J Immunol. 2014;193(4):1609–1621. doi:10.4049/jimmunol.1303000.
  • Di Niro R, Lee SJ, Vander Heiden JA, Elsner RA, Trivedi N, Bannock JM, Gupta NT, Kleinstein SH, Vigneault F, Gilbert TJ, et al. Salmonella infection drives promiscuous b cell activation followed by extrafollicular affinity maturation. Immunity. 2015;43(1):120–131. doi:10.1016/j.immuni.2015.06.013.
  • Larsen P, Nielsen, JL, Dueholm, MS, Wetzel, R, Otzen, D, Nielsen, PH. Amyloid adhesins are abundant in natural biofilms. Environ Microbiol. 2007;9(12):3077–3090. doi:10.1111/j.1462-2920.2007.01418.x.
  • Lim JY, May JM, Cegelski L. Dimethyl sulfoxide and ethanol elicit increased amyloid biogenesis and amyloid-integrated biofilm formation in Escherichia coli. Appl Environ Microbiol. 2012;78(9):3369–3378. doi:10.1128/AEM.07743-11.
  • Zhu W, Winter MG, Byndloss MX, Spiga L, Duerkop BA, Hughes ER, Büttner L, de Lima Romão E, Behrendt CL, Lopez CA, et al. Precision editing of the gut microbiota ameliorates colitis. Nature. 2018;553(7687):208–211. doi:10.1038/nature25172.
  • Wilson RP, Tursi SA, Rapsinski GJ, Medeiros NJ, Le LS, Kotredes KP, Patel S, Liverani E, Sun S, Zhu W, et al. STAT2 dependent Type I interferon response promotes dysbiosis and luminal expansion of the enteric pathogen Salmonella typhimurium. PLoS Pathog. 2019;15(4):e1007745. doi:10.1371/journal.ppat.1007745.
  • Kumar P, Monin L, Castillo P, Elsegeiny W, Horne W, Eddens T, Vikram A, Good M, Schoenborn AA, Bibby K, et al. (2016). Intestinal Interleukin-17 Receptor Signaling Mediates Reciprocal Control of the Gut Microbiota and Autoimmune Inflammation. Immunity, 44(3), 659–671. 10.1016/j.immuni.2016.02.007.
  • Sriram U,Varghese, L, Bennett, HL, Jog, NR, Shivers, DK, Ning, Yue, Behrens, EM, Caricchio, R, Gallucci, S. Myeloid dendritic cells from B6.NZM Sle1/Sle2/Sle3 lupus-prone mice express an IFN signature that precedes disease onset. J Immunol. 2012;189(1):80–91. doi:10.4049/jimmunol.1101686.
  • Noto Llana M, Sarnacki, SH, Vazquez, MV, Gartner, AS, Giacomodonato, MN, Cerquetti, MC. Salmonella enterica induces joint inflammation and expression of interleukin-17 in draining lymph nodes early after onset of enterocolitis in mice. Infect Immun. 2012;80(6):2231–2239. doi:10.1128/IAI.00324-12.