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Research Article

Epithelial cell invasion by salmonella typhimurium induces modulation of genes controlled by aryl hydrocarbon receptor signaling and involved in extracellular matrix biogenesis

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Article: 2158663 | Received 18 May 2022, Accepted 11 Dec 2022, Published online: 04 Jan 2023

References

  • Berg HC, Huxley, AF, Simmons, RM. Constraints on models for the flagellar rotary motor. Philos Trans R Soc Lond B Biol Sci. 2000;355(1396):491–16.
  • Hase K, Kawano K, Nochi T, et al. Uptake through glycoprotein 2 of FimH(+) bacteria by M cells initiates mucosal immune response. Nature. 2009;462(7270):226–230.
  • Grzymajlo K, Ugorski M, Suchanski J, et al. The novel type 1 fimbriae FimH receptor calreticulin plays a role in salmonella host specificity. Front Cell Infect Microbiol. 2017;7:326.
  • Chessa D, Dorsey CW, Winter M, et al. Binding specificity of salmonella plasmid-encoded fimbriae assessed by glycomics. J Biol Chem. 2008;283(13):8118–8124.
  • Dorsey CW, Laarakker MC, Humphries AD, et al. Salmonella enterica serotype typhimurium MisL is an intestinal colonization factor that binds fibronectin. Mol Microbiol. 2005;57(1):196–211.
  • Kingsley RA, Santos RL, Keestra AM, et al. Salmonella enterica serotype typhimurium ShdA is an outer membrane fibronectin-binding protein that is expressed in the intestine. Mol Microbiol. 2002;43(4):895–905.
  • Li X, Bleumink-Pluym NMC, Luijkx Y, et al. MUC1 is a receptor for the salmonella SiiE adhesin that enables apical invasion into enterocytes. PLOS Pathog. 2019;15(2):e1007566.
  • Singh B, Fleury C, Jalalvand F, et al. Human pathogens utilize host extracellular matrix proteins laminin and collagen for adhesion and invasion of the host. FEMS Microbiol Rev. 2012;36(6):61122–61180.
  • Velge P, Wiedemann A, Rosselin M, et al. Multiplicity of salmonella entry mechanisms, a new paradigm for salmonella pathogenesis. Microbiologyopen. 2012;1(3):243–258.
  • Fattinger SA, Bock D, Di Martino ML, et al. Salmonella typhimurium discreet-invasion of the murine gut absorptive epithelium. PLOS Pathog. 2020;16(5):e1008503.
  • Heffernan EJ, Wu L, Louie J, et al. Specificity of the complement resistance and cell association phenotypes encoded by the outer membrane protein genes rck from salmonella typhimurium and ail from yersinia enterocolitica. Infect Immun. 1994;62(11):5183–5186.
  • Rosselin M, Virlogeux-Payant I, Roy C, et al. Rck of salmonella enterica, subspecies enterica serovar enteritidis, mediates zipper-like internalization. Cell Res. 2010;20(6):647–664.
  • Lambert MA, Smith SG. The PagN protein mediates invasion via interaction with proteoglycan. FEMS Microbiol Lett. 2009;297:209–216.
  • Wiedemann A, Mijouin L, Ayoub MA, et al. Identification of the epidermal growth factor receptor as the receptor for salmonella Rck-dependent invasion. FASEB J. 2016;30(12):4180–4191.
  • Yang Y, Wan C, Xu H, et al. Identification of an outer membrane protein of salmonella enterica serovar typhimurium as a potential vaccine candidate for salmonellosis in mice. Microbes Infect. 2013;15(5):388–398.
  • Dyszel JL, Smith JN, Lucas DE, et al. Salmonella enterica serovar typhimurium can detect acyl homoserine lactone production by yersinia enterocolitica in mice. J Bacteriol. 2010;192(1):29–37.
  • Hannemann S, Gao B, Galan JE. Salmonella modulation of host cell gene expression promotes its intracellular growth. PLOS Pathog. 2013;9(10):e1003668.
  • Roche SM, Holbert S, Trotereau J, et al. Salmonella typhimurium invalidated for the three currently known invasion factors keeps its ability to invade several cell models. Front Cell Infect Microbiol. 2018;8:273.
  • Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A. 2000;97(12):6640–6645.
  • Mambu J, Barilleau E, Fragnet-Trapp L, et al. Rck of salmonella typhimurium delays the host cell cycle to facilitate bacterial invasion. Front Cell Infect Microbiol. 2020;10:586934.
  • Barilleau, E, Vedrine M, Koczerka M, et al. Investigation of the invasion mechanism mediated by the outer membrane protein PagN of salmonella typhimurium. BMC Microbiol. 2021;21(1):153.
  • Ritchie ME, Phipson B, Wu D, et al. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43(7):e47.
  • Benjamini Y, Hocheberg Y. Controlling the false discovery rate-a practical and powerful approach to multiple testing. J Roy Stat Soc. 1995;57(1):289–300.
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods. 2001;25(4):402–408.
  • Brionne A, Juanchich A, Hennequet-Antier C. ViSEAGO: a bioconductor package for clustering biological functions using gene ontology and semantic similarity. BioData Min. 2019;12(1):16.
  • Holbert S, Barilleau E, Roche SM, et al. Murine AML12 hepatocytes allow salmonella typhimurium T3SS1-independent invasion and intracellular fate. Sci Rep. 2021;11(1):22803.
  • Yusra, Semba S, Yokozaki H. Biological significance of tumor budding at the invasive front of human colorectal carcinoma cells. Int J Oncol. 2012;41:201–210.
  • Yi J, Bergstrom K, Fu J, et al. Dclk1 in tuft cells promotes inflammation-driven epithelial restitution and mitigates chronic colitis. Cell Death Differ. 2019;26(9):1656–1669.
  • Wu X, Qu D, Weygant N, et al. Cancer stem cell marker DCLK1 correlates with tumorigenic immune infiltrates in the colon and gastric adenocarcinoma microenvironments. Cancers (Basel). 2020;12(2):12.
  • Truong D, Boddy KC, Canadien V, et al. Salmonella exploits host Rho GTPase signalling pathways through the phosphatase activity of SopB. Cell Microbiol. 2018;20(10):e12938.
  • Radtke AL, Wilson JW, Sarker S, et al. Analysis of interactions of salmonella type three secretion mutants with 3-D intestinal epithelial cells. PLoS ONE. 2010;5(12):e15750.
  • Aiastui A, Pucciarelli MG, Garcia-Del Portillo F. Salmonella enterica serovar typhimurium invades fibroblasts by multiple routes differing from the entry into epithelial cells. Infect Immun. 2010;78(6):2700–2713.
  • Quaroni A, Wands J, Trelstad RL, et al. Epithelioid cell cultures from rat small intestine. Characterization by morphologic and immunologic criteria. J cell Biol. 1979;80(2):248.
  • Eckmann L, Smith JR, Housley MP, et al. Analysis by high density cDNA arrays of altered gene expression in human intestinal epithelial cells in response to infection with the invasive enteric bacteria salmonella. J Biol Chem. 2000;275(19):14084–14094.
  • Bruno VM, Hannemann S, Lara-Tejero M, et al. Salmonella typhimurium type III secretion effectors stimulate innate immune responses in cultured epithelial cells. PLOS Pathog. 2009;5(8):e1000538.
  • Forbester JL, Goulding D, Vallier L, et al. Interaction of salmonella enterica serovar typhimurium with intestinal organoids derived from human induced pluripotent stem cells. Infect Immun. 2015;83(7):2926–2934.
  • Powers TR, Haeberle AL, Predeus AV, et al. Intracellular niche-specific profiling reveals transcriptional adaptations required for the cytosolic lifestyle of salmonella enterica. PLOS Pathog. 2021;17(8):e1009280.
  • Berndt A, Muller J, Borsi L, et al. Reorganisation of the caecal extracellular matrix upon salmonella infection–relation between bacterial invasiveness and expression of virulence genes. Vet Microbiol. 2009;133(1–2):123–137.
  • Bhattacharya S, Ploplis VA, Castellino FJ. Bacterial plasminogen receptors utilize host plasminogen system for effective invasion and dissemination. J Biomed Biotechnol. 2012;2012:482096.
  • Haiko J, Laakkonen L, Juuti K, et al. The omptins of yersinia pestis and salmonella enterica cleave the reactive center loop of plasminogen activator inhibitor 1. J Bacteriol. 2010;192(18):4553–4561.
  • Sjobring U, Pohl G, Olsen A. Plasminogen, absorbed by Escherichia coli expressing curli or by salmonella enteritidis expressing thin aggregative fimbriae, can be activated by simultaneously captured tissue-type plasminogen activator (t-PA). Mol Microbiol. 1994;14(3):443–452.
  • Tang L, Han X. The urokinase plasminogen activator system in breast cancer invasion and metastasis. Biomed Pharmacother. 2013;67(2):179–182.
  • Chen CC, Mo FE, Lau LF. The angiogenic factor Cyr61 activates a genetic program for wound healing in human skin fibroblasts. J Biol Chem. 2001;276(50):47329–47337.
  • Brew K, Dinakarpandian D, Nagase H. Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochim Biophys Acta. 2000;1477(1–2):267–283.
  • Zepp JA, Zhao J, Liu C, et al. IL-17A-induced PLET1 expression contributes to tissue repair and colon tumorigenesis. J Immunol. 2017;199(11):3849–3857.
  • Lauer ME, Cheng G, Swaidani S, et al. Tumor necrosis factor-stimulated gene-6 (TSG-6) amplifies hyaluronan synthesis by airway smooth muscle cells. J Biol Chem. 2013;288(1):423–431.
  • Xie Y, Ostriker AC, Jin Y, et al. LMO7 is a negative feedback regulator of transforming growth factor beta signaling and fibrosis. Circulation. 2019;139(5):679–693.
  • Petersen SV, Oury TD, Ostergaard L, et al. Extracellular superoxide dismutase (EC-SOD) binds to type I collagen and protects against oxidative fragmentation. J Biol Chem. 2004;279(14):13705–13710.
  • Asai N, Ohkawara B, Ito M, et al. LRP4 induces extracellular matrix productions and facilitates chondrocyte differentiation. Biochem Biophys Res Commun. 2014;451(2):302–307.
  • Barrett R, Zhang X, Koon HW, et al. Constitutive TL1A expression under colitogenic conditions modulates the severity and location of gut mucosal inflammation and induces fibrostenosis. Am J Pathol. 2012;180(2):636–649.
  • Oda K, Yatera K, Izumi H, et al. Profibrotic role of WNT10A via TGF-beta signaling in idiopathic pulmonary fibrosis. Respir Res. 2016;17(1):39.
  • Lear T, McKelvey AC, Rajbhandari S, et al. Ubiquitin E3 ligase FIEL1 regulates fibrotic lung injury through SUMO-E3 ligase PIAS4. J Exp Med. 2016;213(6):1029–1046.
  • Burgi J, Kunz B, Abrami L, et al. CMG2/ANTXR2 regulates extracellular collagen VI which accumulates in hyaline fibromatosis syndrome. Nat Commun. 2017;8(1):15861.
  • Westling J, Fosang AJ, Last K, et al. ADAMTS4 cleaves at the aggrecanase site (Glu(373)-Ala(374)) and secondarily at the matrix metalloproteinase site (Asn(341)-Phe(342)) in the aggrecan interglobular domain. J Biol Chem. 2002;277(18):16059–16066.
  • Isogai C, Laug WE, Shimada H, et al. Plasminogen activator inhibitor-1 promotes angiogenesis by stimulating endothelial cell migration toward fibronectin. Cancer Res. 2001;61(14):5587–5594.
  • La Paglia L, Listi A, Caruso S, et al. Potential role of ANGPTL4 in the cross talk between metabolism and cancer through PPAR signaling pathway. PPAR Res. 2017;2017:8187235.
  • Gho YS, Kleinman HK, Sosne G. Angiogenic activity of human soluble intercellular adhesion molecule-1. Cancer Res. 1999;59(20):5128–5132.
  • Hedhli N, Russell KS. Cytostatic drugs, neuregulin activation of erbB receptors, and angiogenesis. Curr Hypertens Rep. 2010;12(6):411–417.
  • Larigot L, Juricek L, Dairou J, et al. AhR signaling pathways and regulatory functions. Biochim Open. 2018;7:1–9.
  • Qiu J, Heller JJ, Guo X, et al. The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity. 2012;36(1):92–104.
  • Torti MF, Giovannoni F, Quintana FJ, et al. The aryl hydrocarbon receptor as a modulator of anti-viral immunity. Front Immunol. 2021;12:624293.
  • Giovannoni F, Li Z, Remes-Lenicov F, et al. AHR signaling is induced by infection with coronaviruses. Nat Commun. 2021;12(1):5148.
  • He R, Zhao L, Xu X, et al. Aryl hydrocarbon receptor is required for immune response in epinephelus coioides and danio rerio infected by pseudomonas plecoglossicida. Fish Shellfish Immunol. 2020;97:564–570.
  • Rademacher F, Simanski M, Hesse B, et al. Staphylococcus epidermidis activates aryl hydrocarbon receptor signaling in human keratinocytes: implications for cutaneous defense. J Innate Immun. 2019;11(2):125–135.
  • Munck NA, Roth J, Sunderkotter C, et al. Aryl hydrocarbon receptor-signaling regulates early leishmania major-induced cytokine expression. Front Immunol. 2019;10:2442.
  • Ambrosio LF, Insfran C, Volpini X, et al. Role of aryl hydrocarbon receptor (AhR) in the regulation of immunity and immunopathology during trypanosoma cruzi infection. Front Immunol. 2019;10:631.
  • Bessede A, Gargaro M, Pallotta MT, et al. Aryl hydrocarbon receptor control of a disease tolerance defence pathway. Nature. 2014;511(7508):184–190.
  • Fueldner C, Riemschneider S, Haupt J, et al. Aryl hydrocarbon receptor activation by benzo[a]pyrene prevents development of septic shock and fatal outcome in a mouse model of systemic salmonella enterica infection. Cells. 2022;11(4):737.
  • Moura-Alves P, Fae K, Houthuys E, et al. AhR sensing of bacterial pigments regulates antibacterial defence. Nature. 2014;512(7515):387–392.
  • Tomlin H, and AM Piccinini. A complex interplay between the extracellular matrix and the innate immune response to microbial pathogens. Immunology. 2018;155(2):186–201.