Microbial biofilms and some aspects of anti-inflammatory drug use

Rumynska, T. M.; Hural, A. R.; Konechnyi, Y. T.; Vynnytska, R. B.; Lozynskyi, A. V.; Salyha, Y. T.; Korniychuk, O. P.; Lesyk, R. B.

doi:10.7124/bc.000A57

Biopolym. Cell. 2021; 37(4):247-258.

http://dx.doi.org/10.7124/bc.000A57

Reviews

Microbial biofilms and some aspects of anti-inflammatory drug use

1Rumynska T. M., 1Hural A. R., 1Konechnyi Y. T., 2Vynnytska R. B., 1Lozynskyi A. V., 3Salyha Y. T., 1Korniychuk O. P., 1, 4Lesyk R. B.

Danylo Halytsky Lviv National Medical University
69, Pekarska Str., Lviv, Ukraine, 79010
Ivano-Frankivsk National Medical Universitу
2, Halytska Str., Ivano-Frankivsk, Ukraine, 76018
Institute of Animal Biology, NAAS of Ukraine
38, Stusa Str., Lviv, Ukraine, 79034
University of Information Technology and Management in Rzeszow
2, Sucharskiego Str., Rzeszow, Poland, 35-225

Abstract

The review presents literature data on the effect of nonsteroidal anti-inflammatory drugs (NSAIDs) on the formation of bacterial biofilms. The role of biofilm structures as a factor of virulence of microorganisms is shown, and the protective reactions of a macroorganism in infectious processes caused by bacteria — producers of biofilms are characterized. The article also provides the examples of methods for studying biofilm formation and strategies for managing this process. The prospects of further study of the complex interaction between bacterial pathogens in biofilms are shown, which may help to develop further therapeutic strategies against the biofilm-dependent infections.

Keywords: NSAIDs, microbiota, dysbiosis, prostanoids, cyclooxygenase, biofilms

Full text: (PDF, in English)

References

[1] Terraf MC, Juarez MS, Nader-Macias ME, Silva C. Screening of biofilm formation by beneficial vaginal lactobacilli and influence of culture media components. J Appl Microbiol. 2012; 113(6):1517-29.

[2] Lavryk HS, Korniychuk OP. Antimicrobial properties of Lactobacilli against Staphylococci isolated from biofilms of patients with Acne vulgaris. Mìkrobìologìâ ì bìotehnologìâ. 2020; 1(48):69-78.

[3] Costerton JW. Structure and plasticity at various organization levels in the bacterial cell. Can J Microbiol. 1988;34(4):513-21.

[4] Costerton JW, Geesey GG, Cheng KJ. How bacteria stick. Sci Am. 1978;238(1): 86-95.

[5] Bryers JD. Bacterial biofilms. Curr Opin Biotechnol. 1993;4(2):197-204.

[6] Toyofuku M, Inaba T, Kiyokawa T, Obana N, Yawata Y, Nomura N. Environmental factors that shape biofilm formation. Biosci Biotechnol Biochem. 2016;80(1):7-12.

[7] Dufour D, Leung V, Lévesque CM. Bacterial biofilm: structure, function, and antimicrobial resistance. Endod Topics. 2010;22(1):2-16.

[8] Momeni B. Division of labor: How microbes split their responsibility. Curr Biol. 2018;28(12):R697-9.

[9] Alhede M, Lorenz M, Fritz BG, Jensen PØ, Ring HC, Bay L, Bjarnsholt T. Bacterial aggregate size determines phagocytosis efficiency of polymorphonuclear leukocytes. Med Microbiol Immunol. 2020; 209(6):669-680.

[10] González JF, Hahn MM, Gunn JS. Chronic biofilm-based infections: skewing of the immune response. Pathog Dis. 2018;76(3):fty023.

[11] Deschaine BM, Heysel AR, Lenhart BA, Murphy HA. Biofilm formation and toxin production provide a fitness advantage in mixed colonies of environmental yeast isolates. Ecol Evol. 2018; 8(11):5541-5550.

[12] McDonough KA, Rodriguez A. The myriad roles of cyclic AMP in microbial pathogens: from signal to sword. Nat Rev Microbiol. 2011; 10(1):27-38.

[13] Shan Y, Brown Gandt A, Rowe SE, Deisinger JP, Conlon BP, Lewis K. ATP-dependent persister formation in Escherichia coli. MBio. 2017; 8(1): e02267-16.

[14] Singh PK, Schaefer AL, Parsek MR, Monin-ger TO, Welsh MJ, Greenberg EP. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature. 2000; 407(6805):762-764.

[15] Reigada I, Pérez-Tanoira R, Patel JZ, Savijoki K, Yli-Kauhaluoma J, Kinnari TJ, Fallarero A. Strategies to Prevent Biofilm Infections on Biomaterials: Effect of Novel Naturally-Derived Biofilm Inhibitors on a Competitive Colonization Model of Titanium by Staphylococcus aureus and SaOS-2 Cells. Microorganisms. 2020;8(3):345.

[16] Singh S, Singh SK, Chowdhury I, Singh R. Understanding the Mechanism of Bacterial Biofilms Resistance to Antimicrobial Agents. Open Microbiol J. 2017; 11:53-62.

[17] Lewis K. Persister cells, dormancy and infectious disease. Nat Rev Microbiol. 2007; 5(1):48-56.

[18] Gefen O, Chekol B, Strahilevitz J, Balaban NQ. TDtest: easy detection of bacterial tolerance and persistence in clinical isolates by a modified disk-diffusion assay. Sci Rep. 2017; 7:41284.

[19] Moormeier DE, Bayles KW. Staphylococcus aureus biofilm: a complex developmental organism. Mol Microbiol. 2017; 104(3):365-376.

[20] Kong C, Chee CF, Richter K, Thomas N, Abd Rahman N, Nathan S. Suppression of Staphylococcus aureus biofilm formation and virulence by a benzimidazole derivative, UM-C162. Sci Rep. 2018; 8(1):2758.

[21] Ramos-Vivas J, Chapartegui-González I, Fernández-Martínez M, González-Rico C, Fortún J, Escudero R, Marco F, Linares L, Montejo M, Aranzamendi M, Muñoz P, Valerio M, Aguado JM, Resino E, Ahufinger IG, Vega AP, Martínez-Martínez L, Fariñas MC. Biofilm formation by multidrug resistant Enterobacteriaceae strains isolated from solid organ transplant recipients. Sci Rep. 2019; 9(1):8928.

[22] Lajhar SA, Brownlie J, Barlow R. Characterization of biofilm-forming capacity and resistance to sanitizers of a range of E. coli O26 pathotypes from clinical cases and cattle in Australia. BMC Microbiol. 2018; 18(1):41.

[23] Kamali E, Jamali A, Ardebili A, Ezadi F, Mohebbi A. Evaluation of antimicrobial resistance, biofilm forming potential, and the presence of biofilm-related genes among clinical isolates of Pseudomonas aeruginosa. BMC Res Notes. 2020; 13(1):27.

[24] Zhong X, Wu Q, Zhang J, Ma Z, Wang J, Nie X, Ding Y, Xue L, Chen M, Wu S, Wei X, Zhang Y. Campylobacter jejuni in Biofilm Formation Under Aerobic Conditions and Inhibition by ZnO Nanoparticles. Front Microbiol. 2020; 11:207.

[25] Ramage G, Rajendran R, Sherry L, Williams C. Fungal biofilm resistance. Int J Microbiol. 2012; 2012:528521.

[26] Keshvardoust P, Huron VAA, Clemson M, Constancias F, Barraud N, Rice SA. Biofilm formation inhibition and dispersal of multi-species communities containing ammonia-oxidising bacteria. NPJ Biofilms Microbiomes. 2019; 5(1):22.

[27] Aldrich AL, Heim CE, Shi W, Fallet RW, Duan B, Kielian T. TLR2 and caspase-1 signaling are critical for bacterial containment but not clearance during craniotomy-associated biofilm infection. J Neuroinflammation. 2020; 17(1):114.

[28] Hänsch GM. Host defence against bacterial biofilms: "Mission Impossible"? Int Sch Res Notices. 2012; 2012:1-17.

[29] Babbar A, Barrantes I, Pieper DH, Itzek A. Superantigen SpeA attenuates the biofilm forming capacity of Streptococcus pyogenes. J Microbiol. 2019; 57(7):626-636.

[30] Mishra R, Panda AK, De Mandal S, Shakeel M, Bisht SS, Khan J. Natural Anti-biofilm Agents: Strategies to Control Biofilm-Forming Pathogens. Front Microbiol. 2020; 11:566325.

[31] Toyofuku M, Inaba T, Kiyokawa T, Obana N, Yawata Y, Nomura N. Environmental factors that shape biofilm formation. Biosci Biotechnol Biochem. 2016; 80(1):7-12.

[32] Lawrence JR, Korber DR, Hoyle BD, Costerton JW, Caldwell DE. Optical sectioning of microbial biofilms. J Bacteriol. 1991; 173(20):6558-6567.

[33] Korber DR, Wolfaardt GM, Brözel V, MacDonald R, Niepel T. Reporter systems for microscopic analysis of microbial biofilms. Methods Enzymol. 1999; 310:3-20.

[34] Kim J, Park HD, Chung S. Microfluidic approaches to bacterial biofilm formation. Molecules. 2012; 17(8):9818-9834.

[35] Roy R, Tiwari M, Donelli G, Tiwari V. Strategies for combating bacterial biofilms: A focus on anti-biofilm agents and their mechanisms of action. Virulence. 2018; 9(1):522-554.

[36] Coenye T, Nelis HJ. In vitro and in vivo model systems to study microbial biofilm formation. J Microbiol Methods. 2010; 83(2):89-105.

[37] Kadurugamuwa JL, Sin L, Albert E, Yu J, Francis K, DeBoer M, Rubin M, Bellinger-Kawahara C, Parr TR Jr, Contag PR. Direct continuous method for monitoring biofilm infection in a mouse model. Infect Immun. 2003; 71(2):882-90.

[38] Xiong YQ, Willard J, Kadurugamuwa JL, Yu J, Francis KP, Bayer AS. Real-time in vivo bioluminescent imaging for evaluating the efficacy of antibiotics in a rat Staphylococcus aureus endocarditis model. Antimicrob Agents Chemother. 2005; 49(1):380-387.

[39] Roche ED, Renick PJ, Tetens SP, Ramsay SJ, Da-niels EQ, Carson DL. Increasing the presence of biofilm and healing delay in a porcine model of MRSA-infected wounds. Wound Repair Regen. 2012; 20(4):537-543.

[40] Donlan RM. Biofilms: Microbial life on surfaces. Emerg Infect Dis. 2002; 8(9):881-890.

[41] Roy R, Tiwari M, Donelli G, Tiwari V. Strategies for combating bacterial biofilms: A focus on anti-biofilm agents and their mechanisms of action. Virulence. 2018; 9(1):522-554.

[42] Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB, Parsek MR, Rice SA, Eberl L, Molin S, Høiby N, Kjelleberg S, Givskov M. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology. 2002; 148(1):87-102.

[43] Shen Y, Köller T, Kreikemeyer B, Nelson DC. Rapid degradation of Streptococcus pyogenes biofilms by PlyC, a bacteriophage-encoded endolysin. J Antimicrob Chemother. 2013; 68(8):1818-1824.

[44] Kharidia R, Liang JF. The activity of a small lytic peptide PTP-7 on Staphylococcus aureus biofilms. J Microbiol. 2011; 49(4):663-668.

[45] Hsu ST, Breukink E, Tischenko E, Lutters MA, de Kruijff B, Kaptein R, Bonvin AM, van Nuland NA. The ni-sin-lipid II complex reveals a pyrophosphate cage that provides a blueprint for novel antibiotics. Nat Struct Mol Biol. 2004; 11(10):963-967.

[46] Parisot J, Carey S, Breukink E, Chan WC, Narbad A, Bonev B. Molecular mechanism of target recognition by subtilin, a class I lanthionine antibiotic. Antimicrob Agents Chemother. 2008; 52(2):612-618.

[47] Gagnon MG, Roy RN, Lomakin IB, Florin T, Mankin AS, Steitz TA. Structures of proline-rich peptides bound to the ribosome reveal a common mechanism of protein synthesis inhibition. Nucleic Acids Res. 2016; 44(5):2439-2450.

[48] Segev-Zarko L, Saar-Dover R, Brumfeld V, Mangoni ML, Shai Y. Mechanisms of biofilm inhibition and degradation by antimicrobial peptides. Biochem J. 2015; 468(2):259-270.

[49] Willcox MD, Hume EB, Aliwarga Y, Kumar N, Cole N. A novel cationic-peptide coating for the prevention of microbial colonization on contact lenses. J Appl Microbiol. 2008; 105(6):1817-1825.

[50] Wu S, Liu G, Jin W, Xiu P, Sun C. Antibiofilm and Anti-Infection of a Marine Bacterial Exopolysaccharide Against Pseudomonas aeruginosa. Front Microbiol. 2016; 7:102.

[51] Vane JR, Botting RM. Anti-inflammatory drugs and their mechanism of action. Inflamm Res. 1998; 47(2):78-87.

[52] Sambanthamoorthy K, Luo C, Pattabiraman N, Feng X, Koestler B, Waters CM, Palys TJ. Identification of small molecules inhibiting diguanylate cyclases to control bacterial biofilm development. Biofouling. 2014; 30(1):17-28.

[53] Engelsöy U, Rangel I, Demirel I. Impact of Proinflammatory Cytokines on the Virulence of Uropathogenic Escherichia coli. Front Microbiol. 2019;10:1051.

[54] Doster RS, Kirk LA, Tetz LM, Rogers LM, Aronoff DM, Gaddy JA. Staphylococcus aureus Infection of Human Gestational Membranes Induces Bacterial Biofilm Formation and Host Production of Cytokines. J Infect Dis. 2017; 215(4):653-657.

[55] Yimer EM, Mohammed OA, Mohammedseid SI. Pharmacological exploitation of nonsteroidal anti-inflammatory drugs as potential sources of novel antibacterial agents. Anti-Infect. Agents. 2019; 17(2):81-92.

[56] Laudy AE, Mrowka A, Krajewska J, Tyski S. The Influence of Efflux Pump Inhibitors on the Acti-vi-ty of Non-Antibiotic NSAIDS against Gram-Negative Rods. PloS One. 2016; 11(1):e0147131.

[57] Mohsen A, Gomaa A, Mohamed F, Ragab R, Mennatallah E, Al-Hussein A, Khalaf A, Kamal M, Mokhtar S, Hadeer M, Salah I, Abbas R, Sameh Abd El-Baky RM. Antibacterial, Anti-biofilm Activity of Some Nonsteroidal Anti-Inflammatory Drugs and N-acetyl Cysteine against Some Biofilm Producing Uropathogens. Am J Epidemiol Infect Dis. 2015; 3(1):1-9.

[58] Bhardwaj RG, Ellepolla A, Drobiova H, Karched M. Biofilm growth and IL-8 & TNF-α-inducing properties of Candida albicans in the presence of oral gram-positive and gram-negative bacteria. BMC Microbiol. 2020; 20(1):156.

[59] Roux D, Gaudry S, Khoy-Ear L, Aloulou M, Phillips-Houlbracq M, Bex J, Skurnik D, Denamur E, Monteiro RC, Dreyfuss D, Ricard JD. Airway fungal colonization compromises the immune system allowing bacterial pneumonia to prevail. Crit Care Med. 2013; 41(9):e191-199.

[60] Krause J, Geginat G, Tammer I. Prostaglandin E2 from Candida albicans Stimulates the Growth of Staphylococcus aureus in Mixed Biofilms. PLoS One. 2015; 10(8):e0135404.

[61] Alem MA, Douglas LJ. Effects of aspirin and other nonsteroidal anti-inflammatory drugs on biofilms and planktonic cells of Candida albicans. Antimicrob Agents Chemother. 2004; 48(1):41-47.

[62] de Matos RF, Mendonça LCV, da Silva Souza KG, Fonseca AAD, Costa EMS, de Lima MVD, Vieira JMDS, de Brito MTFM, Monteiro MC. Nimesulide inhibits pathogenic fungi: PGE2-dependent mechanisms. Folia Microbiol. 2017; 62(2):169-174.

[63] Ahmed EF, El-Baky RMA, Ahmed ABF, Waly NG, Gad GFM. Antibacterial Activity of Some Nonsteroidal An-ti-inflammatory Drugs against Bacteria Causing Urinary Tract Infection. Am J Infect Dis Microbiol. 2017; 5(1):66-73.

[64] Chen S, Chen Y, Feng Z, Chen X, Wang Z, Zhu J, Jin J, Yao Q, Xiang L, Yao L, Sun J, Zhao L, Fung H, Laiyi Wong E, Dong D. Barriers of effective health insurance coverage for rural-to-urban migrant workers in China: a systematic review and policy gap analysis. BMC Public Health. 2020; 20(1):408.