САЛЬМОНЕЛЬОЗНА ІНФЕКЦІЯ: ВЗАЄМОДІЯ МІЖ ЕФЕКТОРАМИ T3SSS ТА СИГНАЛЬНИМ ШЛЯХОМ NF-ΚB
Ключові слова:
сальмонели; T3SSs ефектори; сигнальний шлях NF-κB; імунний захист господаря; патогенний механізм.
Анотація
Сальмонела є важливим харчовим патогеном, який може уникати імунного захисту хазяїна за допомогою унікальних механізмів. Сальмонели маніпулюють різними сигнальними шляхами клітини-господаря, доставляючи специфічні ефектори в клітини-мішені для встановлення інфекції. Ядерний фактор-κB (NF-κB) є важливим ядерним фактором транскрипції, який регулює імунну систему хазяїна при зарженні Salmonella. Острівець патоген- ності сальмонели 1 (SPI-1) і острівець патогенності сальмонели 2 (SPI-2) кодують системи секреції III типу (T3SSs), ефектори, які пов’язані з сигнальним шляхом NF-κB через регуляцію запальної реакції господаря. Дослі- дження показали, що ефектори T3SS1 та/або T3SS2, такі як GtgA, GogA та PipA, містять два залишки гістидину та мають металопротеазну активність для контролю реплікації Salmonella. Ці металопротеази цинку надмірно націлені на NF-κB субодиниці p65, RelB і c-Rel, тоді як GogA і GtgA лише інгібують NF-κB-залежну транскрипцію гена. Ефектори T3SS2 SseK1, SseK2 і SseK3 є білками, що містять домен смерті з характеристиками N-пов’яза- ної глікозилтрансферази, які можуть пригнічувати активність NF-κB шляхом інгібування фосфорилювання IκBα в клітинах 293ET, оброблених TNF-α. Серед них SseK1 і SseK3 також пригнічують індуковану Salmonella NF-κB активність у макрофагах. SseK3-опосередковане інгібування сигнального шляху NF-B не вимагається для білка 32, що містить тристоронній E3-убіквітинлігазний мотив. Крім того, ефектор SPI-2 T3SS SpvD інгібує актив- ність NF-κB, запобігаючи ядерній транслокації p65 через взаємодію з Exportin-2, але це не впливає на деградацію IκBα, що в кінцевому підсумку призводить до системного росту сальмонели. Ефектори SPI-1 SipA, SopE, SopE2 і SopB можуть активувати сигнальний шлях NF-κB, щоб сприяти інвазії Salmonella та внутрішньоклітинному переноснику. Однак інші ефектори SptP, AvrA, IpaJ, SspH1, GtgA, GogA та SPI-2, кодовані SseL, SpvB, SseK1 та GogB, можуть ефективно інгібувати шлях передачі сигналів NF-κB та сприяти внутрішньоклітинній реплікації та вірулентності Salmonella. У цьому міні-огляді ми підсумовуємо спеціальний механізм того, як сигнальний шлях NF-κB регулюється ефекторами T3SSs Salmonella при персистуючій інфекції Salmonella, що дозволить додат- ково з’ясувати патогенез Salmonella.
Посилання
1. Bruno, V. M., Hannemann, S., Lara-Tejero, M., Flavell, R. A., Kleinstein, S. H., Galán, J. E. (2009). Salmonella Typhimurium type III secretion effectors stimulate innate immune responses in cultured epithelial cells. PLoS Pathog, 5(8), e1000538. doi: 10.1371/journal.ppat.1000538
2. Bliska, J. B., van der Velden, A. W. (2012). Salmonella "sops" up a preferred electron receptor in the inflamed intestine. mBio, 3(4), e00226-12. doi: 10.1128/mBio.00226-12
3. Broz, P., Ohlson, M. B., Monack, D. M. (2012). Innate immune response to Salmonella Typhimurium, a model enteric pathogen. Gut Microbes, 3(2), 62-70. doi: 10.4161/gmic.19141
4. Burnaevskiy, N., Fox, T. G., Plymire, D. A., Ertelt, J. M., Weigele, B. A., Selyunin, A. S., Way, S. S., Patrie, S. M., Alto, N. M. (2013). Proteolytic elimination of N-myristoyl modifications by the Shigella virulence factor IpaJ. Nature, 496(7443), 106-9. doi: 10.1038/nature12004
5. Batkhishig, D., Bilguun, K., Enkhbayar, P., Miyashita, H., Kretsinger, R. H., Matsushima, N. (2018). Super secondary structure consisting of a polyproline II helix and a β-turn in leucine rich repeats in bacterial type III secretion system effectors. Protein J, 37(3), 223-236. doi: 10.1007/s10930-018-9767-9
6. Brink, T., Leiss, V., Siegert, P., Jehle, D., Ebner, J. K., Schwan, C., Shymanets, A., Wiese, S., Nürnberg, B., Hensel, M., Aktories, K., Orth, J. H. C. (2018). Salmonella Typhimurium effector SseI inhibits chemotaxis and increases host cell survival by deamidation of heterotrimeric Gi proteins. PLoS Pathog, 14(8), e1007248. doi: 10.1371/journal. ppat.1007248
7. Bariana, M., Cassella, E., Rateshwar, J., Ouk, S., Liou, H. C., Heller, C., Colorado, I., Feinman, R., Makhdoom, A., Siegel, D. S., Heller, G., Tuckett, A., Mondello P., Zakrzewski, J. L. (2022). Inhibition of NF-κB DNA binding suppresses myeloma growth via intracellular redox and tumor microenvironment modulation. Mol Cancer Ther, 21(12), 1798-1809. doi: 10.1158/1535-7163.MCT-22-0257
8. Coombes, B. K., Wickham, M. E., Brown, N. F., Lemire, S., Bossi, L., Hsiao, W. W., Brinkman, F. S., Finlay, B. B. (2005). Genetic and molecular analysis of GogB, a phage-encoded type III-secreted substrate in Salmonella enterica serovar Typhimurium with autonomous expression from its associated phage. J Mol Biol, 348(4), 817-30. doi: 10.1016/j. jmb.2005.03.024
9. Coburn, B., Grassl, G. A., Finlay, B. B. (2007). Salmonella, the host and disease: a brief review. Immunol Cell Biol, 85(2), 112-8. doi: 10.1038/sj.icb.7100007
10. Cain, R. J., Hayward, R. D., Koronakis, V. (2008). Deciphering interplay between Salmonella invasion effectors. PLoS Pathog, 4(4), e1000037. doi: 10.1371/journal.ppat.1000037
11. Cuadrado, A., Martín-Moldes, Z., Ye, J., Lastres-Becker, I. (2014). Transcription factors NRF2 and NF-κB are coordinated effectors of the Rho family, GTP-binding protein RAC1 during inflammation. J Biol Chem, 289(22), 15244-58. doi: 10.1074/jbc.M113.540633
12. Cook, M., Delbecq, S. P., Schweppe, T. P., Guttman, M., Klevit, R. E., Brzovic, P. S. (2019). The ubiquitin ligase SspH1 from Salmonella uses a modular and dynamic E3 domain to catalyze substrate ubiquitylation. J Biol Chem, 294(3), 783-793. doi: 10.1074/jbc.RA118.004247
13. Cohen, E., Azriel, S., Auster, O., Gal, A., Zitronblat, C., Mikhlin, S., Scharte, F., Hensel, M., Rahav, G., Gal-Mor, O. (2021). Pathoadaptation of the passerine-associated Salmonella enterica serovar Typhimurium lineage to the avian host. PLoS Pathog, 17(3), e1009451. doi: 10.1371/journal.ppat.1009451
14. de Jong, H. K., Parry, C. M., van der Poll, T., Wiersinga, W. J. (2012). Host-pathogen interaction in invasive Salmonellosis. PLoS Pathog, 8(10), e1002933. doi: 10.1371/journal.ppat.1002933
15. Dos Santos, A. M. P., Ferrari, R. G., Conte-Junior, C. A. (2020). Type three secretion system in Salmonella Typhimurium: the key to infection. Genes Genomics, 42(5), 495-506. doi: 10.1007/s13258-020-00918-8
16. Fu, Y., Galán, J. E. (1999). A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature, 401(6750), 293-7. doi: 10.1038/45829
17. Figueira, R., Watson, K. G., Holden, D. W., Helaine, S. (2013). Identification of Salmonella pathogenicity island-2 type III secretion system effectors involved in intramacrophage replication of S. enterica serovar Typhimurium: implications for rational vaccine design. mBio, 4(2), e00065. doi: 10.1128/mBio.00065-13
18. Finn, C. E., Chong, A., Cooper, K. G., Starr, T., Steele-Mortimer, O. (2017). A second wave of Salmonella T3SS1 activity prolongs the lifespan of infected epithelial cells. PLoS Pathog, 13(4), e1006354. doi: 10.1371/journal.ppat.1006354
19. Giogha, C., Lung, T. W., Pearson, J. S., Hartland, E. L. (2014). Inhibition of death receptor signaling by bacterial gut pathogens. Cytokine Growth Factor Rev, 25(2), 235-43. doi: 10.1016/j.cytogfr.2013.12.012
20. Günster, R. A., Matthews, S. A., Holden, D. W., Thurston, T. L. M. (2017). SseK1 and SseK3 type III secretion system effectors inhibit NF-κB signaling and necroptotic cell death in Salmonella-infected macrophages. Infect Immun, 85(3), e00010-17. doi: 10.1128/IAI.00010-17
21. Gal-Mor, O. Persistent Infection and long-term carriage of typhoidal and nontyphoidal Salmonellae. (2018). Clin Microbiol Rev, 32(1), e00088-18. doi: 10.1128/CMR.00088-18
22. Geng, S., Wang, Y., Xue, Y., Wang, H., Cai, Y., Zhang, J., Barrow, P., Pan, Z., Jiao, X. (2019). The SseL protein inhibits the intracellular NF-κB pathway to enhance the virulence of Salmonella Pullorum in a chicken model. Microb Pathog, 129, 1-6. doi: 10.1016/j.micpath.2019.01.035
23. Galán, J. E. (2021). Salmonella Typhimurium and inflammation: a pathogen-centric affair. Nat Rev Microbiol, 19(11), 716-725. doi: 10.1038/s41579-021-00561-4 24. Gómez-Chávez, F., Correa, D., Navarrete-Meneses, P., Cancino-Diaz, J. C., Cancino-Diaz, M. E., Rodríguez- Martínez, S. (2021). NF-κB and its regulators during pregnancy. Front Immunol, 12, 679106. doi: 10.3389/fimmu.2021.679106
25. Haraga, A., Miller, S, I. (2006). A Salmonella type III secretion effector interacts with the mammalian serine/threonine protein kinase PKN1. Cell Microbiol, 8(5), 837-46. doi: 10.1111/j.1462-5822.2005.00670.x
26. Hayden, M. S., Ghosh, S. (2008). Shared principles in NF-kappaB signaling. Cell, 132(3), 344-62. doi: 10.1016/j. cell.2008.01.020
27. Haneda, T., Ishii, Y., Shimizu, H., Ohshima, K., Iida, N., Danbara, H., Okada, N. (2012). Salmonella type III effector SpvC, a phosphothreonine lyase, contributes to reduction in inflammatory response during intestinal phase of infection. Cell Microbiol, 14(4), 485-99. doi: 10.1111/j.1462-5822.2011.01733.x
28. Jiang, Y., He, L., Ju, C., Pei, Y., Ji, M., Li, Y., Liao, L., Jang, S., Zhu, Z., Wang, Y. (2015). Isolation and expression of grass carp toll-like receptor 5a (CiTLR5a) and 5b (CiTLR5b) gene involved in the response to flagellin stimulation and grass carp reovirus infection. Fish Shellfish Immunol, 44(1), 88-99. doi: 10.1016/j.fsi.2015.01.024
29. Jennings, E., Thurston, T. L. M., Holden, D. W. (2017). Salmonella SPI-2 type III secretion system effectors: molecular mechanisms and physiological consequences. Cell Host Microbe, 22(2), 217-231. doi: 10.1016/j.chom.2017.07.009
30. Johnson, R., Byrne, A., Berger, C. N., Klemm, E., Crepin, V. F., Dougan, G., Frankel, G. (2017). The type III secretion system effector SptP of Salmonella enterica serovar typhi. J Bacteriol, 199(4), e00647-16. doi: 10.1128/JB.00647-16
31. Jiao, Y., Zhang, Y. G., Lin, Z., Lu, R., Xia, Y., Meng, C., Pan, Z., Xu, X., Jiao, X., Sun, J. (2020). Salmonella Enteritidis effector AvrA suppresses autophagy by reducing beclin-1 protein. Front Immunol, 11, 686. doi: 10.3389/fimmu.2020.00686
32. Jia, H., Song, N., Ma, Y., Zhang, F., Yue, Y., Wang, W., Li, C., Li, H., Wang, Q., Gu, L., Li, B. (2022). Salmonella facilitates iron acquisition through UMPylation of ferric uptake regulator. mBio, 13(3), e0020722. doi: 10.1128/mbio.00207-22
33. Keestra, A. M., Winter, M. G., Auburger, J. J., Frässle, S. P., Xavier, M. N., Winter, S. E., Kim, A., Poon, V., Ravesloot, M. M., Waldenmaier, J. F., Tsolis, R. M., Eigenheer, R. A., Bäumler, A. J. (2013). Manipulation of small Rho GTPases is a pathogen-induced process detected by NOD1. Nature, 496(7444), 233-7. doi: 10.1038/nature12025
34. Keszei, A. F., Tang, X., McCormick, C., Zeqiraj, E., Rohde, J. R., Tyers, M., Sicheri, F. (2014). Structure of an SspH1-PKN1 complex reveals the basis for host substrate recognition and mechanism of activation for a bacterial E3 ubiquitin ligase. Mol Cell Biol, 34(3), 362-73. doi: 10.1128/MCB.01360-13
35. Kogut, M. H., Lee, A., Santin, E. (2020). Microbiome and pathogen interaction with the immune system. Poult Sci, 99(4), 1906-1913. doi: 10.1016/j.psj.2019.12.011
36. Krukonis, E. S., Thomson, J. J. (2020). Complement evasion mechanisms of the systemic pathogens Yersiniae and Salmonellae. FEBS Lett, 594(16), 2598-2620. doi: 10.1002/1873-3468.13771
37. Keestra, A. M., Winter, M. G., Klein-Douwel, D., Xavier, M. N., Winter, S. E., Kim, A., Tsolis, R. M., Bäumler, A. J. (2011). A Salmonella virulence factor activates the NOD1/NOD2 signaling pathway. mBio, 2(6), e00266-11. doi: 10.1128/ mBio.00266-11
38. LaRock, D. L., Chaudhary, A., Miller, S. I. (2015). Salmonellae interactions with host processes. Nat Rev Microbiol, 13(4), 191-205. doi: 10.1038/nrmicro3420
39. Lhocine, N., Arena, E. T., Bomme, P., Ubelmann, F., Prévost, M. C., Robine, S., Sansonetti, P. J. (2015). Apical invasion of intestinal epithelial cells by Salmonella Typhimurium requires villin to remodel the brush border actin cytoskeleton. Cell Host Microbe, 17(2), 164-77. doi: 10.1016/j.chom.2014.12.003
40. Liu, W., Zhuang, J., Jiang, Y., Sun, J., Prinz, R. A., Sun, J., Jiao, X., Xu, X. (2019). Toll-like receptor signalling cross-activates the autophagic pathway to restrict Salmonella Typhimurium growth in macrophages. Cell Microbiol, 21(12), e13095. doi: 10.1111/cmi.13095
41. Lin, Z., Zhang, Y. G., Xia, Y., Xu, X., Jiao, X., Sun, J. (2016). Salmonella enteritidis effector AvrA stabilizes intestinal tight junctions via the JNK pathway. J Biol Chem, 291(52), 26837-26849. doi: 10.1074/jbc.M116.757393
42. Li, Q., Xu, L., Yin, C., Liu, Z., Li, Y., Yuan, Y., Hu, Y., Jiao, X. (2020). The invasion plasmid antigen J (IpaJ) from Salmonella inhibits NF-κB activation by suppressing IκBα ubiquitination. Infect Immun, 88(3), e00875-19. doi: 10.1128/ IAI.00875-19
43. Liu, Y., Dou, Y., Yan, L., Yang, X., He, B., Kong, L., Smith, W. (2020). The role of Rho GTPases' substrates Rac and Cdc42 in osteoclastogenesis and relevant natural medicinal products study. Biosci Rep, 40(7), BSR20200407. doi: 10.1042/ BSR20200407
44. Lawrence, A. E., Abuaita, B. H., Berger, R. P., Hill, D. R., Huang, S., Yadagiri, V. K., Bons, B., Fields, C., Wobus, C. E., Spence, J. R., Young, V. B., O'Riordan, M. X. (2021). Salmonella enterica serovar Typhimurium SPI-1 and SPI-2 shape the global transcriptional landscape in a human intestinal organoid model system. mBio, 12(3), e00399-21. doi: 10.1128/mBio.00399-21
45. Liao, Z., Su, J. (2021). Progresses on three pattern recognition receptor families (TLRs, RLRs and NLRs) in teleost. Dev Comp Immunol, 122, 104131. doi: 10.1016/j.dci.2021.104131
46. Li, R., Zhou, Y., Zhang, S., Li, J., Zheng, Y., Fan, X. (2022). The natural (poly)phenols as modulators of microglia polarization via TLR4/NF-κB pathway exert anti-inflammatory activity in ischemic stroke. Eur J Pharmacol, 914, 174660. doi: 10.1016/j.ejphar.2021.174660
47. Lu, X., Zhang, M., Yang, S., Deng, Y., Jiao, Y. (2022). Transcriptome analysis reveals the diverse response of pearl oyster pinctada fucata martensii after different PAMP stimulation. Fish Shellfish Immunol, 131, 881-890. doi: 10.1016/j. fsi.2022.10.058
48. Mesquita, F. S., Holden, D. W., Rolhion, N. (2013). Lack of effect of the Salmonella deubiquitinase SseL on the NF-κB pathway. PLoS One, 8(1), e53064. doi: 10.1371/journal.pone.0053064
49. Markowiak, P., Śliżewska, K. (2017). Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients, 9(9), 1021. doi: 10.3390/nu9091021
50. Noster, J., Chao, T. C., Sander, N., Schulte, M., Reuter, T., Hansmeier, N., Hensel, M. (2019). Proteomics of intracellular Salmonella enterica reveals roles of Salmonella pathogenicity island 2 in metabolism and antioxidant defense. PLoS Pathog, 15(4), e1007741. doi: 10.1371/journal.ppat.1007741
51. Ménard, S., Lacroix-Lamandé, S., Ehrhardt, K., Yan, J., Grassl, G. A., Wiedemann, A. (2022). Cross-talk between the intestinal epithelium and Salmonella Typhimurium. Front Microbiol, 13, 906238. doi: 10.3389/fmicb.2022.906238
52. Pilar, A. V., Reid-Yu, S. A., Cooper, C. A., Mulder, D. T., Coombes, B. K. (2012). GogB is an anti-inflammatory effector that limits tissue damage during Salmonella infection through interaction with human FBXO22 and Skp1. PLoS Pathog, 8(6), e1002773. doi: 10.1371/journal.ppat.1002773
53. Passaris, I., Cambré, A., Govers, S. K., Aertsen, A. (2018). Bimodal expression of the Salmonella Typhimurium spv operon. Genetics, 210(2), 621-635. doi: 10.1534/genetics.118.300822
54. Pinaud, L., Sansonetti, P. J., Phalipon, A. (2018). Host cell targeting by enteropathogenic bacteria T3SS effectors. Trends Microbiol, 26(4), 266-283. doi: 10.1016/j.tim.2018.01.010
55. Parween, F., Yadav, J., Qadri, A. (2019). The virulence polysaccharide of Salmonella Typhi suppresses activation of Rho family GTPases to limit inflammatory responses from epithelial cells. Front Cell Infect Microbiol, 9, 141. doi: 10.3389/ fcimb.2019.00141
56. Potrykus, M., Czaja-Stolc, S., Stankiewicz, M., Kaska, Ł., Małgorzewicz, S. (2021). Intestinal microbiota as a contributor to chronic inflammation and its potential modifications. Nutrients, 13(11), 3839. doi: 10.3390/nu13113839
57. Rytkönen, A., Poh, J., Garmendia, J., Boyle, C., Thompson, A., Liu, M., Freemont, P., Hinton, J. C., Holden, D. W. (2007). SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc Natl Acad Sci USA, 104(9), 3502-7. doi: 10.1073/pnas.0610095104
58. Rolhion, N., Furniss, R. C., Grabe, G., Ryan, A., Liu, M., Matthews, S. A., Holden, D. W. (2016). Inhibition of nuclear transport of NF-ĸB p65 by the Salmonella type III secretion system effector SpvD. PLoS Pathog, 12(5), e1005653. doi: 10.1371/journal.ppat.1005653
59. Stanley, A., Thompson, K., Hynes, A., Brakebusch, C., Quondamatteo, F. (2014). NADPH oxidase complex-derived reactive oxygen species, the actin cytoskeleton, and Rho GTPases in cell migration. Antioxid Redox Signal, 20(13), 2026-42. doi: 10.1089/ars.2013.5713
60. Sun, H., Kamanova, J., Lara-Tejero, M., Galán, J. E. (2016). A family of Salmonella type III secretion effector proteins selectively targets the NF-κB signaling pathway to preserve host homeostasis. PLoS Pathog, 12(3), e1005484. doi: 10.1371/journal.ppat.1005484
61. Stormberg, T., Filliaux, S., Baughman, H. E. R., Komives, E. A., Lyubchenko, Y. L. (2021). Transcription factor NF-κB unravels nucleosomes. Biochim Biophys Acta Gen Subj, 1865(9), 129934. doi: 10.1016/j.bbagen.2021.129934
62. Sharma, A., Raman, V., Lee, J., Forbes, N. S. (2022). Microbial imbalance induces inflammation by promoting Salmonella penetration through the mucosal barrier. ACS Infect Dis, 8(5), 969-981. doi: 10.1021/acsinfecdis.1c00530
63. Svahn, A. J., Suster, C. J. E., Chang, S. L., Rockett, R. J., Sim, E. M., Cliff, O. M., Wang, Q., Arnott, A., Ramsperger, M., Sorrell, T. C., Sintchenko, V., Prokopenko, M. (2023). Pangenome analysis of a Salmonella Enteritidis population links a major outbreak to a Gifsy-1-like prophage containing anti-Inflammatory gene gogB. Microbiol Spectr, e0279122. doi: 10.1128/spectrum.02791-22
64. Takemura, M., Haneda, T., Idei, H., Miki, T., Okada, N. (2021). A Salmonella type III effector, PipA, works in a different manner than the PipA family effectors GogA and GtgA. PLoS One, 16(3), e0248975. doi: 10.1371/journal.pone.0248975
65. Tao, H., Li, W., Zhang, W., Yang, C., Zhang, C., Liang, X., Yin, J., Bai, J., Ge, G., Zhang, H., Yang, X., Li, H., Xu, Y., Hao, Y., Liu, Y., Geng, D. (2021). Urolithin A suppresses RANKL-induced osteoclastogenesis and postmenopausal osteoporosis by, suppresses inflammation and downstream NF-κB activated pyroptosis pathways. Pharmacol Res, 174, 105967. doi: 10.1016/j.phrs.2021.105967
66. Wu, H., Jones, R. M., Neish, A, S. (2012). The Salmonella effector AvrA mediates bacterial intracellular survival during infection in vivo. Cell Microbiol, 14(1), 28-39. doi: 10.1111/j.1462-5822.2011.01694.x
67. Wang, L., Li, Y., Liu, Y., Zuo, L., Li, Y., Wu, S., Huang, R. (2019). Salmonella spv locus affects type I interferon response and the chemotaxis of neutrophils via suppressing autophagy. Fish Shellfish Immunol, 87, 721-729. doi: 10.1016/j. fsi.2019.02.009
68. Walch, P., Selkrig, J., Knodler, L. A., Rettel, M., Stein, F., Fernandez, K., Viéitez, C., Potel, C. M., Scholzen, K., Geyer, M., Rottner, K., Steele-Mortimer, O., Savitski, M. M., Holden, D. W., Typas, A. (2021). Global mapping of Salmonella enterica-host protein-protein interactions during infection. Cell Host Microbe, 29(8), 1316-1332.e12. doi: 10.1016/j. chom.2021.06.004
69. Xie, Z., Zhang, Y., Huang, X. (2020). Evidence and speculation: the response of Salmonella confronted by autophagy in macrophages. Future Microbiol, 15, 1277-1286. doi: 10.2217/fmb-2020-0125
70. Ye, Z., Petrof, E. O., Boone, D., Claud, E. C., Sun, J. (2007). Salmonella effector AvrA regulation of colonic epithelial cell inflammation by deubiquitination. Am J Pathol, 171(3), 882-92. doi: 10.2353/ajpath.2007.070220
71. Yang, Z., Soderholm, A., Lung, T. W., Giogha, C., Hill, M. M., Brown, N. F., Hartland, E., Teasdale, R. D. (2015). SseK3 is a Salmonella effector that binds TRIM32 and modulates the host's NF-κB signalling activity. PLoS One, 10(9), e0138529. doi: 10.1371/journal.pone.0138529
72. Yin, C., Gu, J., Gu, D., Wang, Z., Ji, R., Jiao, X., Li, Q. (2022). The Salmonella T3SS1 effector IpaJ is regulated by ItrA and inhibits the MAPK signaling pathway. PLoS Pathog, 18(12), e1011005. doi: 10.1371/journal.ppat.1011005
73. Zhang, Y., Wu, S., Ma, J., Xia, Y., Ai, X., Sun, J. (2015). Bacterial protein AvrA stabilizes intestinal epithelial tight junctions via blockage of the C-Jun N-terminal kinase pathway. Tissue Barriers, 3(1-2), e972849. doi: 10.4161/21688362.2014.972849
74. Zhang, K., Riba, A., Nietschke, M., Torow, N., Repnik, U., Pütz, A., Fulde, M., Dupont, A., Hensel, M., Hornef, M. (2018). Minimal SPI1-T3SS effector requirement for Salmonella enterocyte invasion and intracellular proliferation in vivo. PLoS Pathog, 14(3), e1006925. doi: 10.1371/journal.ppat.1006925
2. Bliska, J. B., van der Velden, A. W. (2012). Salmonella "sops" up a preferred electron receptor in the inflamed intestine. mBio, 3(4), e00226-12. doi: 10.1128/mBio.00226-12
3. Broz, P., Ohlson, M. B., Monack, D. M. (2012). Innate immune response to Salmonella Typhimurium, a model enteric pathogen. Gut Microbes, 3(2), 62-70. doi: 10.4161/gmic.19141
4. Burnaevskiy, N., Fox, T. G., Plymire, D. A., Ertelt, J. M., Weigele, B. A., Selyunin, A. S., Way, S. S., Patrie, S. M., Alto, N. M. (2013). Proteolytic elimination of N-myristoyl modifications by the Shigella virulence factor IpaJ. Nature, 496(7443), 106-9. doi: 10.1038/nature12004
5. Batkhishig, D., Bilguun, K., Enkhbayar, P., Miyashita, H., Kretsinger, R. H., Matsushima, N. (2018). Super secondary structure consisting of a polyproline II helix and a β-turn in leucine rich repeats in bacterial type III secretion system effectors. Protein J, 37(3), 223-236. doi: 10.1007/s10930-018-9767-9
6. Brink, T., Leiss, V., Siegert, P., Jehle, D., Ebner, J. K., Schwan, C., Shymanets, A., Wiese, S., Nürnberg, B., Hensel, M., Aktories, K., Orth, J. H. C. (2018). Salmonella Typhimurium effector SseI inhibits chemotaxis and increases host cell survival by deamidation of heterotrimeric Gi proteins. PLoS Pathog, 14(8), e1007248. doi: 10.1371/journal. ppat.1007248
7. Bariana, M., Cassella, E., Rateshwar, J., Ouk, S., Liou, H. C., Heller, C., Colorado, I., Feinman, R., Makhdoom, A., Siegel, D. S., Heller, G., Tuckett, A., Mondello P., Zakrzewski, J. L. (2022). Inhibition of NF-κB DNA binding suppresses myeloma growth via intracellular redox and tumor microenvironment modulation. Mol Cancer Ther, 21(12), 1798-1809. doi: 10.1158/1535-7163.MCT-22-0257
8. Coombes, B. K., Wickham, M. E., Brown, N. F., Lemire, S., Bossi, L., Hsiao, W. W., Brinkman, F. S., Finlay, B. B. (2005). Genetic and molecular analysis of GogB, a phage-encoded type III-secreted substrate in Salmonella enterica serovar Typhimurium with autonomous expression from its associated phage. J Mol Biol, 348(4), 817-30. doi: 10.1016/j. jmb.2005.03.024
9. Coburn, B., Grassl, G. A., Finlay, B. B. (2007). Salmonella, the host and disease: a brief review. Immunol Cell Biol, 85(2), 112-8. doi: 10.1038/sj.icb.7100007
10. Cain, R. J., Hayward, R. D., Koronakis, V. (2008). Deciphering interplay between Salmonella invasion effectors. PLoS Pathog, 4(4), e1000037. doi: 10.1371/journal.ppat.1000037
11. Cuadrado, A., Martín-Moldes, Z., Ye, J., Lastres-Becker, I. (2014). Transcription factors NRF2 and NF-κB are coordinated effectors of the Rho family, GTP-binding protein RAC1 during inflammation. J Biol Chem, 289(22), 15244-58. doi: 10.1074/jbc.M113.540633
12. Cook, M., Delbecq, S. P., Schweppe, T. P., Guttman, M., Klevit, R. E., Brzovic, P. S. (2019). The ubiquitin ligase SspH1 from Salmonella uses a modular and dynamic E3 domain to catalyze substrate ubiquitylation. J Biol Chem, 294(3), 783-793. doi: 10.1074/jbc.RA118.004247
13. Cohen, E., Azriel, S., Auster, O., Gal, A., Zitronblat, C., Mikhlin, S., Scharte, F., Hensel, M., Rahav, G., Gal-Mor, O. (2021). Pathoadaptation of the passerine-associated Salmonella enterica serovar Typhimurium lineage to the avian host. PLoS Pathog, 17(3), e1009451. doi: 10.1371/journal.ppat.1009451
14. de Jong, H. K., Parry, C. M., van der Poll, T., Wiersinga, W. J. (2012). Host-pathogen interaction in invasive Salmonellosis. PLoS Pathog, 8(10), e1002933. doi: 10.1371/journal.ppat.1002933
15. Dos Santos, A. M. P., Ferrari, R. G., Conte-Junior, C. A. (2020). Type three secretion system in Salmonella Typhimurium: the key to infection. Genes Genomics, 42(5), 495-506. doi: 10.1007/s13258-020-00918-8
16. Fu, Y., Galán, J. E. (1999). A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature, 401(6750), 293-7. doi: 10.1038/45829
17. Figueira, R., Watson, K. G., Holden, D. W., Helaine, S. (2013). Identification of Salmonella pathogenicity island-2 type III secretion system effectors involved in intramacrophage replication of S. enterica serovar Typhimurium: implications for rational vaccine design. mBio, 4(2), e00065. doi: 10.1128/mBio.00065-13
18. Finn, C. E., Chong, A., Cooper, K. G., Starr, T., Steele-Mortimer, O. (2017). A second wave of Salmonella T3SS1 activity prolongs the lifespan of infected epithelial cells. PLoS Pathog, 13(4), e1006354. doi: 10.1371/journal.ppat.1006354
19. Giogha, C., Lung, T. W., Pearson, J. S., Hartland, E. L. (2014). Inhibition of death receptor signaling by bacterial gut pathogens. Cytokine Growth Factor Rev, 25(2), 235-43. doi: 10.1016/j.cytogfr.2013.12.012
20. Günster, R. A., Matthews, S. A., Holden, D. W., Thurston, T. L. M. (2017). SseK1 and SseK3 type III secretion system effectors inhibit NF-κB signaling and necroptotic cell death in Salmonella-infected macrophages. Infect Immun, 85(3), e00010-17. doi: 10.1128/IAI.00010-17
21. Gal-Mor, O. Persistent Infection and long-term carriage of typhoidal and nontyphoidal Salmonellae. (2018). Clin Microbiol Rev, 32(1), e00088-18. doi: 10.1128/CMR.00088-18
22. Geng, S., Wang, Y., Xue, Y., Wang, H., Cai, Y., Zhang, J., Barrow, P., Pan, Z., Jiao, X. (2019). The SseL protein inhibits the intracellular NF-κB pathway to enhance the virulence of Salmonella Pullorum in a chicken model. Microb Pathog, 129, 1-6. doi: 10.1016/j.micpath.2019.01.035
23. Galán, J. E. (2021). Salmonella Typhimurium and inflammation: a pathogen-centric affair. Nat Rev Microbiol, 19(11), 716-725. doi: 10.1038/s41579-021-00561-4 24. Gómez-Chávez, F., Correa, D., Navarrete-Meneses, P., Cancino-Diaz, J. C., Cancino-Diaz, M. E., Rodríguez- Martínez, S. (2021). NF-κB and its regulators during pregnancy. Front Immunol, 12, 679106. doi: 10.3389/fimmu.2021.679106
25. Haraga, A., Miller, S, I. (2006). A Salmonella type III secretion effector interacts with the mammalian serine/threonine protein kinase PKN1. Cell Microbiol, 8(5), 837-46. doi: 10.1111/j.1462-5822.2005.00670.x
26. Hayden, M. S., Ghosh, S. (2008). Shared principles in NF-kappaB signaling. Cell, 132(3), 344-62. doi: 10.1016/j. cell.2008.01.020
27. Haneda, T., Ishii, Y., Shimizu, H., Ohshima, K., Iida, N., Danbara, H., Okada, N. (2012). Salmonella type III effector SpvC, a phosphothreonine lyase, contributes to reduction in inflammatory response during intestinal phase of infection. Cell Microbiol, 14(4), 485-99. doi: 10.1111/j.1462-5822.2011.01733.x
28. Jiang, Y., He, L., Ju, C., Pei, Y., Ji, M., Li, Y., Liao, L., Jang, S., Zhu, Z., Wang, Y. (2015). Isolation and expression of grass carp toll-like receptor 5a (CiTLR5a) and 5b (CiTLR5b) gene involved in the response to flagellin stimulation and grass carp reovirus infection. Fish Shellfish Immunol, 44(1), 88-99. doi: 10.1016/j.fsi.2015.01.024
29. Jennings, E., Thurston, T. L. M., Holden, D. W. (2017). Salmonella SPI-2 type III secretion system effectors: molecular mechanisms and physiological consequences. Cell Host Microbe, 22(2), 217-231. doi: 10.1016/j.chom.2017.07.009
30. Johnson, R., Byrne, A., Berger, C. N., Klemm, E., Crepin, V. F., Dougan, G., Frankel, G. (2017). The type III secretion system effector SptP of Salmonella enterica serovar typhi. J Bacteriol, 199(4), e00647-16. doi: 10.1128/JB.00647-16
31. Jiao, Y., Zhang, Y. G., Lin, Z., Lu, R., Xia, Y., Meng, C., Pan, Z., Xu, X., Jiao, X., Sun, J. (2020). Salmonella Enteritidis effector AvrA suppresses autophagy by reducing beclin-1 protein. Front Immunol, 11, 686. doi: 10.3389/fimmu.2020.00686
32. Jia, H., Song, N., Ma, Y., Zhang, F., Yue, Y., Wang, W., Li, C., Li, H., Wang, Q., Gu, L., Li, B. (2022). Salmonella facilitates iron acquisition through UMPylation of ferric uptake regulator. mBio, 13(3), e0020722. doi: 10.1128/mbio.00207-22
33. Keestra, A. M., Winter, M. G., Auburger, J. J., Frässle, S. P., Xavier, M. N., Winter, S. E., Kim, A., Poon, V., Ravesloot, M. M., Waldenmaier, J. F., Tsolis, R. M., Eigenheer, R. A., Bäumler, A. J. (2013). Manipulation of small Rho GTPases is a pathogen-induced process detected by NOD1. Nature, 496(7444), 233-7. doi: 10.1038/nature12025
34. Keszei, A. F., Tang, X., McCormick, C., Zeqiraj, E., Rohde, J. R., Tyers, M., Sicheri, F. (2014). Structure of an SspH1-PKN1 complex reveals the basis for host substrate recognition and mechanism of activation for a bacterial E3 ubiquitin ligase. Mol Cell Biol, 34(3), 362-73. doi: 10.1128/MCB.01360-13
35. Kogut, M. H., Lee, A., Santin, E. (2020). Microbiome and pathogen interaction with the immune system. Poult Sci, 99(4), 1906-1913. doi: 10.1016/j.psj.2019.12.011
36. Krukonis, E. S., Thomson, J. J. (2020). Complement evasion mechanisms of the systemic pathogens Yersiniae and Salmonellae. FEBS Lett, 594(16), 2598-2620. doi: 10.1002/1873-3468.13771
37. Keestra, A. M., Winter, M. G., Klein-Douwel, D., Xavier, M. N., Winter, S. E., Kim, A., Tsolis, R. M., Bäumler, A. J. (2011). A Salmonella virulence factor activates the NOD1/NOD2 signaling pathway. mBio, 2(6), e00266-11. doi: 10.1128/ mBio.00266-11
38. LaRock, D. L., Chaudhary, A., Miller, S. I. (2015). Salmonellae interactions with host processes. Nat Rev Microbiol, 13(4), 191-205. doi: 10.1038/nrmicro3420
39. Lhocine, N., Arena, E. T., Bomme, P., Ubelmann, F., Prévost, M. C., Robine, S., Sansonetti, P. J. (2015). Apical invasion of intestinal epithelial cells by Salmonella Typhimurium requires villin to remodel the brush border actin cytoskeleton. Cell Host Microbe, 17(2), 164-77. doi: 10.1016/j.chom.2014.12.003
40. Liu, W., Zhuang, J., Jiang, Y., Sun, J., Prinz, R. A., Sun, J., Jiao, X., Xu, X. (2019). Toll-like receptor signalling cross-activates the autophagic pathway to restrict Salmonella Typhimurium growth in macrophages. Cell Microbiol, 21(12), e13095. doi: 10.1111/cmi.13095
41. Lin, Z., Zhang, Y. G., Xia, Y., Xu, X., Jiao, X., Sun, J. (2016). Salmonella enteritidis effector AvrA stabilizes intestinal tight junctions via the JNK pathway. J Biol Chem, 291(52), 26837-26849. doi: 10.1074/jbc.M116.757393
42. Li, Q., Xu, L., Yin, C., Liu, Z., Li, Y., Yuan, Y., Hu, Y., Jiao, X. (2020). The invasion plasmid antigen J (IpaJ) from Salmonella inhibits NF-κB activation by suppressing IκBα ubiquitination. Infect Immun, 88(3), e00875-19. doi: 10.1128/ IAI.00875-19
43. Liu, Y., Dou, Y., Yan, L., Yang, X., He, B., Kong, L., Smith, W. (2020). The role of Rho GTPases' substrates Rac and Cdc42 in osteoclastogenesis and relevant natural medicinal products study. Biosci Rep, 40(7), BSR20200407. doi: 10.1042/ BSR20200407
44. Lawrence, A. E., Abuaita, B. H., Berger, R. P., Hill, D. R., Huang, S., Yadagiri, V. K., Bons, B., Fields, C., Wobus, C. E., Spence, J. R., Young, V. B., O'Riordan, M. X. (2021). Salmonella enterica serovar Typhimurium SPI-1 and SPI-2 shape the global transcriptional landscape in a human intestinal organoid model system. mBio, 12(3), e00399-21. doi: 10.1128/mBio.00399-21
45. Liao, Z., Su, J. (2021). Progresses on three pattern recognition receptor families (TLRs, RLRs and NLRs) in teleost. Dev Comp Immunol, 122, 104131. doi: 10.1016/j.dci.2021.104131
46. Li, R., Zhou, Y., Zhang, S., Li, J., Zheng, Y., Fan, X. (2022). The natural (poly)phenols as modulators of microglia polarization via TLR4/NF-κB pathway exert anti-inflammatory activity in ischemic stroke. Eur J Pharmacol, 914, 174660. doi: 10.1016/j.ejphar.2021.174660
47. Lu, X., Zhang, M., Yang, S., Deng, Y., Jiao, Y. (2022). Transcriptome analysis reveals the diverse response of pearl oyster pinctada fucata martensii after different PAMP stimulation. Fish Shellfish Immunol, 131, 881-890. doi: 10.1016/j. fsi.2022.10.058
48. Mesquita, F. S., Holden, D. W., Rolhion, N. (2013). Lack of effect of the Salmonella deubiquitinase SseL on the NF-κB pathway. PLoS One, 8(1), e53064. doi: 10.1371/journal.pone.0053064
49. Markowiak, P., Śliżewska, K. (2017). Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients, 9(9), 1021. doi: 10.3390/nu9091021
50. Noster, J., Chao, T. C., Sander, N., Schulte, M., Reuter, T., Hansmeier, N., Hensel, M. (2019). Proteomics of intracellular Salmonella enterica reveals roles of Salmonella pathogenicity island 2 in metabolism and antioxidant defense. PLoS Pathog, 15(4), e1007741. doi: 10.1371/journal.ppat.1007741
51. Ménard, S., Lacroix-Lamandé, S., Ehrhardt, K., Yan, J., Grassl, G. A., Wiedemann, A. (2022). Cross-talk between the intestinal epithelium and Salmonella Typhimurium. Front Microbiol, 13, 906238. doi: 10.3389/fmicb.2022.906238
52. Pilar, A. V., Reid-Yu, S. A., Cooper, C. A., Mulder, D. T., Coombes, B. K. (2012). GogB is an anti-inflammatory effector that limits tissue damage during Salmonella infection through interaction with human FBXO22 and Skp1. PLoS Pathog, 8(6), e1002773. doi: 10.1371/journal.ppat.1002773
53. Passaris, I., Cambré, A., Govers, S. K., Aertsen, A. (2018). Bimodal expression of the Salmonella Typhimurium spv operon. Genetics, 210(2), 621-635. doi: 10.1534/genetics.118.300822
54. Pinaud, L., Sansonetti, P. J., Phalipon, A. (2018). Host cell targeting by enteropathogenic bacteria T3SS effectors. Trends Microbiol, 26(4), 266-283. doi: 10.1016/j.tim.2018.01.010
55. Parween, F., Yadav, J., Qadri, A. (2019). The virulence polysaccharide of Salmonella Typhi suppresses activation of Rho family GTPases to limit inflammatory responses from epithelial cells. Front Cell Infect Microbiol, 9, 141. doi: 10.3389/ fcimb.2019.00141
56. Potrykus, M., Czaja-Stolc, S., Stankiewicz, M., Kaska, Ł., Małgorzewicz, S. (2021). Intestinal microbiota as a contributor to chronic inflammation and its potential modifications. Nutrients, 13(11), 3839. doi: 10.3390/nu13113839
57. Rytkönen, A., Poh, J., Garmendia, J., Boyle, C., Thompson, A., Liu, M., Freemont, P., Hinton, J. C., Holden, D. W. (2007). SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc Natl Acad Sci USA, 104(9), 3502-7. doi: 10.1073/pnas.0610095104
58. Rolhion, N., Furniss, R. C., Grabe, G., Ryan, A., Liu, M., Matthews, S. A., Holden, D. W. (2016). Inhibition of nuclear transport of NF-ĸB p65 by the Salmonella type III secretion system effector SpvD. PLoS Pathog, 12(5), e1005653. doi: 10.1371/journal.ppat.1005653
59. Stanley, A., Thompson, K., Hynes, A., Brakebusch, C., Quondamatteo, F. (2014). NADPH oxidase complex-derived reactive oxygen species, the actin cytoskeleton, and Rho GTPases in cell migration. Antioxid Redox Signal, 20(13), 2026-42. doi: 10.1089/ars.2013.5713
60. Sun, H., Kamanova, J., Lara-Tejero, M., Galán, J. E. (2016). A family of Salmonella type III secretion effector proteins selectively targets the NF-κB signaling pathway to preserve host homeostasis. PLoS Pathog, 12(3), e1005484. doi: 10.1371/journal.ppat.1005484
61. Stormberg, T., Filliaux, S., Baughman, H. E. R., Komives, E. A., Lyubchenko, Y. L. (2021). Transcription factor NF-κB unravels nucleosomes. Biochim Biophys Acta Gen Subj, 1865(9), 129934. doi: 10.1016/j.bbagen.2021.129934
62. Sharma, A., Raman, V., Lee, J., Forbes, N. S. (2022). Microbial imbalance induces inflammation by promoting Salmonella penetration through the mucosal barrier. ACS Infect Dis, 8(5), 969-981. doi: 10.1021/acsinfecdis.1c00530
63. Svahn, A. J., Suster, C. J. E., Chang, S. L., Rockett, R. J., Sim, E. M., Cliff, O. M., Wang, Q., Arnott, A., Ramsperger, M., Sorrell, T. C., Sintchenko, V., Prokopenko, M. (2023). Pangenome analysis of a Salmonella Enteritidis population links a major outbreak to a Gifsy-1-like prophage containing anti-Inflammatory gene gogB. Microbiol Spectr, e0279122. doi: 10.1128/spectrum.02791-22
64. Takemura, M., Haneda, T., Idei, H., Miki, T., Okada, N. (2021). A Salmonella type III effector, PipA, works in a different manner than the PipA family effectors GogA and GtgA. PLoS One, 16(3), e0248975. doi: 10.1371/journal.pone.0248975
65. Tao, H., Li, W., Zhang, W., Yang, C., Zhang, C., Liang, X., Yin, J., Bai, J., Ge, G., Zhang, H., Yang, X., Li, H., Xu, Y., Hao, Y., Liu, Y., Geng, D. (2021). Urolithin A suppresses RANKL-induced osteoclastogenesis and postmenopausal osteoporosis by, suppresses inflammation and downstream NF-κB activated pyroptosis pathways. Pharmacol Res, 174, 105967. doi: 10.1016/j.phrs.2021.105967
66. Wu, H., Jones, R. M., Neish, A, S. (2012). The Salmonella effector AvrA mediates bacterial intracellular survival during infection in vivo. Cell Microbiol, 14(1), 28-39. doi: 10.1111/j.1462-5822.2011.01694.x
67. Wang, L., Li, Y., Liu, Y., Zuo, L., Li, Y., Wu, S., Huang, R. (2019). Salmonella spv locus affects type I interferon response and the chemotaxis of neutrophils via suppressing autophagy. Fish Shellfish Immunol, 87, 721-729. doi: 10.1016/j. fsi.2019.02.009
68. Walch, P., Selkrig, J., Knodler, L. A., Rettel, M., Stein, F., Fernandez, K., Viéitez, C., Potel, C. M., Scholzen, K., Geyer, M., Rottner, K., Steele-Mortimer, O., Savitski, M. M., Holden, D. W., Typas, A. (2021). Global mapping of Salmonella enterica-host protein-protein interactions during infection. Cell Host Microbe, 29(8), 1316-1332.e12. doi: 10.1016/j. chom.2021.06.004
69. Xie, Z., Zhang, Y., Huang, X. (2020). Evidence and speculation: the response of Salmonella confronted by autophagy in macrophages. Future Microbiol, 15, 1277-1286. doi: 10.2217/fmb-2020-0125
70. Ye, Z., Petrof, E. O., Boone, D., Claud, E. C., Sun, J. (2007). Salmonella effector AvrA regulation of colonic epithelial cell inflammation by deubiquitination. Am J Pathol, 171(3), 882-92. doi: 10.2353/ajpath.2007.070220
71. Yang, Z., Soderholm, A., Lung, T. W., Giogha, C., Hill, M. M., Brown, N. F., Hartland, E., Teasdale, R. D. (2015). SseK3 is a Salmonella effector that binds TRIM32 and modulates the host's NF-κB signalling activity. PLoS One, 10(9), e0138529. doi: 10.1371/journal.pone.0138529
72. Yin, C., Gu, J., Gu, D., Wang, Z., Ji, R., Jiao, X., Li, Q. (2022). The Salmonella T3SS1 effector IpaJ is regulated by ItrA and inhibits the MAPK signaling pathway. PLoS Pathog, 18(12), e1011005. doi: 10.1371/journal.ppat.1011005
73. Zhang, Y., Wu, S., Ma, J., Xia, Y., Ai, X., Sun, J. (2015). Bacterial protein AvrA stabilizes intestinal epithelial tight junctions via blockage of the C-Jun N-terminal kinase pathway. Tissue Barriers, 3(1-2), e972849. doi: 10.4161/21688362.2014.972849
74. Zhang, K., Riba, A., Nietschke, M., Torow, N., Repnik, U., Pütz, A., Fulde, M., Dupont, A., Hensel, M., Hornef, M. (2018). Minimal SPI1-T3SS effector requirement for Salmonella enterocyte invasion and intracellular proliferation in vivo. PLoS Pathog, 14(3), e1006925. doi: 10.1371/journal.ppat.1006925
Опубліковано
2023-11-20
Як цитувати
Ли, Ж., Фотін, А. І., Петров, Р. В., Ма, Д., & Фотіна, Т. І. (2023). САЛЬМОНЕЛЬОЗНА ІНФЕКЦІЯ: ВЗАЄМОДІЯ МІЖ ЕФЕКТОРАМИ T3SSS ТА СИГНАЛЬНИМ ШЛЯХОМ NF-ΚB. Вісник Сумського національного аграрного університету. Серія: Ветеринарна медицина, (3(62), 3-11. https://doi.org/10.32782/bsnau.vet.2023.3.1
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