Ways of microbial escape from the immune system: A brief overview

Year 2024, Volume: 41 Issue: 3, 653 - 662, 30.09.2024

Ghazal Pourbeiragh , Faezeh Mehdizadeh , Mehrdad Pashazadeh , Abolfazl Jafarı-sales

Abstract

Viruses, bacteria and other microbes always try to disable our body system. Our immune system has a complex structure that continuously tries to defend our body against "foreign enemies". Microbes that infect other organisms encounter host immune responses and must overcome or evade innate and adaptive immune responses to successfully establish infection, providing fascinating insights into attack and escape. Many pathogens appear to have developed parallel pathways for escape, and several principles of escape are shared not only among members of the same genus but even among different organisms such as bacteria, viruses, fungi, and parasites. In this article, according to the recent findings, the unique escape strategies of microorganisms will be analyzed in more detail. Part of our immune system is responsible for clearing pathogens, either killing the pathogen directly or marking it for destruction by other immune cells. Therefore, it is possible to develop a new targeted therapy when the mechanism of microorganisms is fully understood. This review describes the mechanisms of interaction between the pathogen and its host in the context of infection.

Keywords

Safety system, Safety response, Microorganism, Infection, Innate immune;, Adaptive immunity, Phagocytosis

References

• Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature. 2007;449(7164):819-26.
• Delves PJ, Roitt IM. The immune system. New England journal of medicine. 2000;343(1):37-49.
• Lee JS, Bukhari SNA, Fauzi NM. Effects of chalcone derivatives on players of the immune system. Drug Des Devel Ther. 2015;9:4761-78.
• Thakur A, Mikkelsen H, Jungersen G. Intracellular pathogens: host immunity and microbial persistence strategies. Journal of immunology research. 2019;(1):1356540
• Ali M, Abdallah MS, Jere S. Bacterial strategy of invading host immune system: A review. Clinical Research in Immunology. 2019;2(1):1-7.
• Janeway Jr CA. How the immune system protects the host from infection. Microbes and infection. 2001;3(13):1167-71.
• Herskovits AA, Auerbuch V, Portnoy DA. Bacterial ligands generated in a phagosome are targets of the cytosolic innate immune system. PLoS pathogens. 2007;3(3):e51.
• Cornejo E, Schlaermann P, Mukherjee S. How to rewire the host cell: A home improvement guide for intracellular bacteria. J Cell Biol. 2017;216(12):3931-48.
• Moore SR, Menon SS, Cortes C, Ferreira VP. Hijacking factor H for complement immune evasion. Front Immunol. 2021;12:602277.
• Hilleman MR. Strategies and mechanisms for host and pathogen survival in acute and persistent viral infections. Proceedings of the National Academy of Sciences. 2004;101(suppl_2):14560-6.
• Kotwal GJ. Microorganisms and their interaction with the immune system. J Leukoc Biol. 1997;62(4):415-29.
• Haleem KS, Ali YM, Yesilkaya H, Kohler T, Hammerschmidt S, Andrew PW, et al. The pneumococcal surface proteins PspA and PspC sequester host C4-binding protein to inactivate complement C4b on the bacterial surface. Infection and immunity. 2019;87(1):e00742-18.
• Gutiérrez-Martínez E, Planès R, Anselmi G, Reynolds M, Menezes S, Adiko AC, et al. Cross-presentation of cell-associated antigens by MHC class I in dendritic cell subsets. Frontiers in immunology. 2015;6:363.
• Pizarro-Cerdá J, Charbit A, Enninga J, Lafont F, Cossart P, editors. Manipulation of host membranes by the bacterial pathogens Listeria, Francisella, Shigella and Yersinia. Seminars in cell & developmental biology; 2016;60:155-67.
• Petrišič N, Kozorog M, Aden S, Podobnik M, Anderluh G. The molecular mechanisms of listeriolysin O-induced lipid membrane damage. Biochimica et Biophysica Acta (BBA)-Biomembranes. 2021;1863(7):183604.
• Flannagan RS, Kuiack RC, McGavin MJ, Heinrichs DE. Staphylococcus aureus uses the GraXRS regulatory system to sense and adapt to the acidified phagolysosome in macrophages. MBio. 2018;9(4):e001143-18.
• Nandi A, Bishayi B. Intracellularly survived Staphylococcus aureus after phagocytosis are more virulent in inducing cytotoxicity in fresh murine peritoneal macrophages utilizing TLR-2 as a possible target. Microbial pathogenesis. 2016;97:131-47.
• Jian L, Sun L, Li C, Yu R, Ma Z, Wang X, et al. Interleukin‐21 enhances Toll‐like receptor 2/4‐mediated cytokine production via phosphorylation in the STAT3, Akt and p38 MAPK signalling pathways in human monocytic THP‐1 cells. Scandinavian Journal of Immunology. 2019;89(6):e12761.
• McNab FW, Ewbank J, Howes A, Moreira-Teixeira L, Martirosyan A, Ghilardi N, et al. Type I IFN induces IL-10 production in an IL-27–independent manner and blocks responsiveness to IFN-γ for production of IL-12 and bacterial killing in Mycobacterium tuberculosis–infected macrophages. The Journal of Immunology. 2014;193(7):3600-12.
• Choi J, Groisman EA. Activation of master virulence regulator PhoP in acidic pH requires the Salmonella-specific protein UgtL. Science signaling. 2017;10(494):eaan6284.
• Vasicek EM, O’Neal L, Parsek MR, Fitch J, White P, Gunn JS. L-arabinose transport and metabolism in salmonella influences biofilm formation. Frontiers in Cellular and Infection Microbiology. 2021;11:698146.
• Zhang R, Zheng X, Kuang J, Edgar KJ. Glycan ester deacylation by TBAOH or TBAF: Regioselectivity vs. polysaccharide structure. Carbohydrate polymers. 2014;113:159-65.
• Fijałkowska M, Kowalski M, Koziej M, Antoszewski B. Elevated serum levels of cathelicidin and β-defensin 2 are associated with basal cell carcinoma. Central European Journal of Immunology. 2021;46(3):360-4.
• Radomski N, Rebbig A, Leonhardt RM, Knittler MR. Xenophagic pathways and their bacterial subversion in cellular self-defense–παντα ρει–everything is in flux. International Journal of Medical Microbiology. 2018;308(1):185-96.
• Maiden MCJ. The impact of nucleotide sequence analysis on meningococcal vaccine development and assessment. Frontiers in immunology. 2019;9:3151
• Majkowska-Skrobek G, Latka A, Berisio R, Squeglia F, Maciejewska B, Briers Y, et al. Phage-borne depolymerases decrease Klebsiella pneumoniae resistance to innate defense mechanisms. Frontiers in Microbiology. 2018;9:2517.
• Bastiat-Sempe B, Love JF, Lomayesva N, Wessels MR. Streptolysin O and NAD-glycohydrolase prevent phagolysosome acidification and promote group A Streptococcus survival in macrophages. MBio. 2014;5(5):e01690-14.
• Wilde S, Dash A, Johnson A, Mackey K, Okumura CY, LaRock CN. Detoxification of reactive oxygen species by the hyaluronic acid capsule of group A Streptococcus. Infection and Immunity. 2023;91(11):e0025823.
• Jończyk-Matysiak E, Łusiak-Szelachowska M, Kłak M, Bubak B, Międzybrodzki R, Weber-Dąbrowska B, et al. The effect of bacteriophage preparations on intracellular killing of bacteria by phagocytes. Journal of Immunology Research. 2015(1):482863.
• Kalia N, Singh J, Kaur M. The role of dectin-1 in health and disease. Immunobiology. 2021;226(2):152071.
• Vendele I, Willment JA, Silva LM, Palma AS, Chai W, Liu Y, et al. Mannan detecting C-type lectin receptor probes recognise immune epitopes with diverse chemical, spatial and phylogenetic heterogeneity in fungal cell walls. PLoS pathogens. 2020;16(1):e1007927.
• Oh S, Li K, Prince A, Wheeler ML, Hamade H, Nguyen C, et al. Pathogen size alters C-type lectin receptor signaling in dendritic cells to influence CD4 Th9 cell differentiation. Cell reports. 2022;38(13):110567.
• Cleare LG, Zamith-Miranda D, Nosanchuk JD. Heat shock proteins in Histoplasma and Paracoccidioides. Clinical and Vaccine Immunology. 2017;24(11):e00221-17.
• Harpf V, Rambach G, Würzner R, Lass-Flörl C, Speth C. Candida and complement: new aspects in an old battle. Frontiers in Immunology. 2020;11:1471.
• Luo ShanShan LS, Hipler U, Münzberg C, Skerka C, Zipfel P. Sequence variations and protein expression levels of the two immune evasion proteins Gpm1 and Pra1 influence virulence of clinical Candida albicans isolates. 2015;10(2):e0113192.
• Svoboda E, Schneider AE, Sándor N, Lermann U, Staib P, Kremlitzka M, et al. Secreted aspartic protease 2 of Candida albicans inactivates factor H and the macrophage factor H-receptors CR3 (CD11b/CD18) and CR4 (CD11c/CD18). Immunology letters. 2015;168(1):13-21.
• Staerck C, Gastebois A, Vandeputte P, Calenda A, Larcher G, Gillmann L, et al. Microbial antioxidant defense enzymes. Microbial Pathogenesis. 2017;110:56-65.
• Savers A, Rasid O, Parlato M, Brock M, Jouvion G, Ryffel B, et al. Infection-mediated priming of phagocytes protects against lethal secondary Aspergillus fumigatus challenge. PloS one. 2016;11(4):e0153829.
• Yan W, Zhao Y-s, Xie K, Xing Y, Xu F. Aspergillus fumigatus Influences Gasdermin-D-Dependent Pyroptosis of the Lung via Regulating Toll-Like Receptor 2-Mediated Regulatory T Cell Differentiation. Journal of Immunology Research. 2021;2021:5538612.
• Sari M, Prange A, Lelley JI, Hambitzer R. Screening of beta-glucan contents in commercially cultivated and wild growing mushrooms. Food Chemistry. 2017;216:45-51.
• Rabaan AA, Alfaraj AH, Alshengeti A, Alawfi A, Alwarthan S, Alhajri M, et al. Antibodies to Combat Fungal Infections: Development Strategies and Progress. Microorganisms. 2023;11(3):671.
• Kvam AJ, Burnham-Marusich AR, Mash M, Kozel TR. Rapid oxidative release of fungal mannan for detection by immunoassay. Medical Mycology. 2022;60(9):myac066.
• Ray SC, Rappleye CA, editors. Flying under the radar: Histoplasma capsulatum avoidance of innate immune recognition. Seminars in cell & developmental biology. 2019;89:91-8
• Wei Y, Wang Z, Liu Y, Liao B, Zong Y, Shi Y, et al. Extracellular vesicles of Candida albicans regulate its own growth through the L-arginine/nitric oxide pathway. Applied Microbiology and Biotechnology. 2023;107(1):355-67.
• Staerck C, Tabiasco J, Godon C, Delneste Y, Bouchara J-P, Fleury MJ. Transcriptional profiling of Scedosporium apiospermum enzymatic antioxidant gene battery unravels the involvement of thioredoxin reductases against chemical and phagocytic cells oxidative stress. Medical Mycology. 2019;57(3):363-73.
• Wang L, Pei W, Li J, Feng Y, Gao X, Jiang P, et al. Microplastics induced apoptosis in macrophages by promoting ROS generation and altering metabolic profiles. Ecotoxicology and Environmental Safety. 2024;271:115970.
• Ward RA, Vyas JM. The first line of defense: Effector pathways of anti-fungal innate immunity. Current opinion in microbiology. 2020;58:160-5.
• Luo S, Hipler U-C, Münzberg C, Skerka C, Zipfel PF. Sequence variations and protein expression levels of the two immune evasion proteins Gpm1 and Pra1 influence virulence of clinical Candida albicans isolates. PLoS One. 2015;10(2):e0113192.
• Kling HM, Norris KA. Vaccine-induced immunogenicity and protection against Pneumocystis pneumonia in a nonhuman primate model of HIV and Pneumocystis coinfection. The Journal of infectious diseases. 2016;213(10):1586-95.
• Kottom TJ, Carmona EM, Limper AH. Current state of carbohydrate recognition and c-type lectin receptors in pneumocystis innate immunity. Frontiers in immunology. 2021;12:798214.
• Luraschi A, Cissé OH, Pagni M, Hauser PM. Identification and functional ascertainment of the Pneumocystis jirovecii potential drug targets Gsc1 and Kre6 involved in glucan synthesis. journal of eukaryotic microbiology. 2017;64(4):481-90.
• Christiaansen A, Varga SM, Spencer JV. Viral manipulation of the host immune response. Current opinion in immunology. 2015;36:54-60.
• Webster RG, Govorkova EA. Continuing challenges in influenza. Annals of the New York Academy of Sciences. 2014;1323(1):115-39.
• Lin R-W, Chen G-W, Sung H-H, Lin R-J, Yen L-C, Tseng Y-L, et al. Naturally occurring mutations in PB1 affect influenza A virus replication fidelity, virulence, and adaptability. Journal of Biomedical Science. 2019;26:55.
• Ptaszyńska-Sarosiek I, Dunaj J, Zajkowska A, Niemcunowicz-Janica A, Król M, Pancewicz S, et al. Post-mortem detection of six human herpesviruses (HSV-1, HSV-2, VZV, EBV, CMV, HHV-6) in trigeminal and facial nerve ganglia by PCR. PeerJ. 2019;6:e6095.
• Horton NC, Mathew PA. NKp44 and natural cytotoxicity receptors as damage-associated molecular pattern recognition receptors. Frontiers in immunology. 2015;6:31.
• Koch PD, Miller HR, Yu G, Tallarico JA, Sorger PK, Wang Y, et al. A high content screen in macrophages identifies small molecule modulators of STING-IRF3 and NFkB signaling. ACS chemical biology. 2018;13(4):1066-81.
• Simons K, Peters H, Jukema JW, de Vries M, Quax P. A protective role of IRF 3 and IRF 7 signalling downstream TLR s in the development of vein graft disease via type I interferons. Journal of internal medicine. 2017;282(6):522-36.
• Komala Sari T, Gianopulos KA, Nicola AV. Glycoprotein C of herpes simplex virus 1 shields glycoprotein B from antibody neutralization. Journal of Virology. 2020;94(5):e01852-19.
• Hernaez B, Alcami A. New insights into the immunomodulatory properties of poxvirus cytokine decoy receptors at the cell surface. F1000Research. 2018;7:F1000 Faculty Rev-719.
• Hong S-N, Kim JY, Kim H, Kim D-Y, Won T-B, Han DH, et al. Duox2 is required for the transcription of pattern recognition receptors in acute viral lung infection: An interferon-independent regulatory mechanism. Antiviral research. 2016;134:1-5.
• Amet T, Lan J, Shepherd N, Yang K, Byrd D, Xing Y, et al. Glycosylphosphatidylinositol anchor deficiency attenuates the production of infectious HIV-1 and renders virions sensitive to complement attack. AIDS Research and Human Retroviruses. 2016;32(10-11):1100-12.
• Eugenia eAriza M, Williams MV. Human Herpesviruses-encoded dUTPases: A Family of Proteins that Modulate Dendritic Cell Function and Innate Immunity. 2014;5:504.
• Amin I, Vajeeha A, Younas S, Afzal S, Shahid M, Nawaz R, et al. HSV-1 infection: role of viral proteins and cellular receptors. Critical Reviews™ in Eukaryotic Gene Expression. 2019;29(5):461-9.
• de Castro Neto AL, Da Silveira JF, Mortara RA. Role of virulence factors of trypanosomatids in the insect vector and putative genetic events involved in surface protein diversity. Frontiers in Cellular and Infection Microbiology. 2022;12:807172.
• Herwaldt BL. Protozoa and helminths. Biological safety: principles and practices. 2006:115-61.
• VB M. Response of anaerobic protozoa to oxygen tension in anaerobic system. International Microbiology. 2019;22(3):355-61.
• Almeida B, Silva K, Venturin G, Chiku V, Leal A, Bosco A, et al. Induction of haem oxygenase‐1 increases infection of dog macrophages by L. infantum. Parasite Immunology. 2017;39(12):e12494.
• Jesus-Santos FH, Lobo-Silva J, Ramos PIP, Descoteaux A, Lima JB, Borges VM, et al. LPG2 gene duplication in Leishmania infantum: A case for CRISPR-Cas9 gene editing. Frontiers in Cellular and Infection Microbiology. 2020;10:408.
• Choudhary HH, Gupta R, Mishra S. PKAc is not required for the preerythrocytic stages of Plasmodium berghei. Life Science Alliance. 2019;2(3):e201900352.
• Srivastava PN, Mishra S. Disrupting a Plasmodium berghei putative phospholipase impairs efficient egress of merosomes. International Journal for Parasitology. 2022;52(8):547-58.
• Rehman A, Ahmad S, Shahid F, Albutti A, Alwashmi AS, Aljasir MA, et al. Integrated core proteomics, subtractive proteomics, and immunoinformatics investigation to unveil a potential multi-epitope vaccine against schistosomiasis. Vaccines. 2021;9(6):658.
• Divenuto F, Pavia G, Marascio N, Barreca GS, Quirino A, Matera G. Role of Treg, Breg and other cytokine sets in host protection and immunopathology during human leishmaniasis: Are they potential valuable markers in clinical settings and vaccine evaluation? Acta Tropica. 2023;240(11):106849.
• Toepp AJ, Petersen CA. The balancing act: Immunology of leishmaniosis. Research in veterinary science. 2020;130:19-25.
• Hsu L-H, Li K-P, Chu K-H, Chiang B-L. A B-1a cell subset induces Foxp3− T cells with regulatory activity through an IL-10-independent pathway. Cellular & molecular immunology. 2015;12(3):354-65.