year 16, Issue 2 (March - April 2022)                   Iran J Med Microbiol 2022, 16(2): 83-97 | Back to browse issues page


XML Persian Abstract Print


Pathobiology Department, Faculty of Veterinary Medicine, University of Tabriz, Tabriz, Iran , mo_gh66@yahoo.com
Abstract:   (1834 Views)

Presently, viral diseases are incrementing all over the world, for which the definitive solutions are difficult since there are no effective drugs. In the 1990s, antiviral probiotics first appeared when they acted as drugs for protecting the intestinal epithelium against viral infection and reducing diarrhea. Thus, further studies have been performed to define the mechanisms behind this antiviral impact. Over 100 years ago, lactic acid bacteria (LAB) were accidentally utilized naturally exist in fermented products, against viral infections. Producing several active ingredients like active ribosomal proteins, acids, hydrogen peroxide, non-ribosomal synthetase peptides (NRPS), and other metabolites is an important feature of lactic acid bacteria. Numerous studies have recently assessed the significance of these active ingredients in both nutrition and medicine. LAB was utilized in food fermentation to present a good taste for food while protecting it from pathogenic microorganisms and spoilage. In this article, the LAB metabolites’ antiviral activity was assessed.

Full-Text [PDF 1118 kb]   (937 Downloads) |   |   Full-Text (HTML)  (993 Views)  
Type of Study: Review Article | Subject: Antimicrobial Substances
Received: 2021/08/16 | Accepted: 2022/01/15 | ePublished: 2022/02/10

References
1. Fauci AS, Touchette NA, Folkers GK. Emerging infectious diseases: a 10-year perspective from the National Institute of Allergy and Infectious Diseases. Int J Risk Saf Med. 2005;17(3, 4):157-67. [DOI:10.3201/eid1104.041167] [PMID] [PMCID]
2. Hardy H, Harris J, Lyon E, Beal J, Foey AD. Probiotics, prebiotics and immunomodulation of gut mucosal defences: homeostasis and immunopathology. Nutrients. 2013;5(6):1869-912. [DOI:10.3390/nu5061869] [PMID] [PMCID]
3. Al Kassaa I, Hober D, Hamze M, Caloone D, Dewilde A, Chihib N-e, et al. Vaginal Lactobacillus gasseri CMUL57 can inhibit herpes simplex type 2 but not Coxsackievirus B4E2. Arch Microbiol. 2015;197(5):657-64. [DOI:10.1007/s00203-015-1101-8] [PMID] [PMCID]
4. Pericone CD, Park S, Imlay JA, Weiser JN. Factors contributing to hydrogen peroxide resistance in Streptococcus pneumoniae include pyruvate oxidase (SpxB) and avoidance of the toxic effects of the Fenton reaction. J Bacteriol. 2003;185(23):6815-25. [DOI:10.1128/JB.185.23.6815-6825.2003] [PMID] [PMCID]
5. Seki M, Iida K-i, Saito M, Nakayama H, Yoshida S-i. Hydrogen peroxide production in Streptococcus pyogenes: involvement of lactate oxidase and coupling with aerobic utilization of lactate. J Bacteriol. 2004;186(7):2046-51. [DOI:10.1128/JB.186.7.2046-2051.2004] [PMID] [PMCID]
6. Kawasaki S, Satoh T, Todoroki M, Niimura Y. b-Type dihydroorotate dehydrogenase is purified as a H2O2-forming NADH oxidase from Bifidobacterium bifidum. Appl Environment Microbiol. 2009;75(3):629-36. [DOI:10.1128/AEM.02111-08] [PMID] [PMCID]
7. Klebanoff SJ, Coombs RW. Viricidal effect of Lactobacillus acidophilus on human immunodeficiency virus type 1: possible role in heterosexual transmission. J Experiment Med. 1991;174(1):289-92. [DOI:10.1084/jem.174.1.289] [PMID] [PMCID]
8. Conti C, Malacrino C, Mastromarino P. Inhibition of herpes simplex virus type 2 by vaginal lactobacilli. J Physiol Pharmacol. 2009;60(6):19-26.
9. Mentel R, Shirrmakher R, Kevich A, Dreĭzin R, Shmidt I. Virus inactivation by hydrogen peroxide. Voprosy Virusologii. 1977(6):731-3.
10. In YW, Kim JJ, Kim HJ, Oh SW. Antimicrobial activities of acetic acid, citric acid and lactic acid against S higella species. J Food Saf. 2013;33(1):79-85. [DOI:10.1111/jfs.12025]
11. Boskey E, Telsch K, Whaley K, Moench T, Cone R. Acid production by vaginal flora in vitro is consistent with the rate and extent of vaginal acidification. Infect Immun. 1999;67(10):5170-5. [DOI:10.1128/IAI.67.10.5170-5175.1999] [PMID] [PMCID]
12. Martín V, Maldonado A, Fernández L, Rodríguez JM, Connor RI. Inhibition of human immunodeficiency virus type 1 by lactic acid bacteria from human breastmilk. Breastfeeding Med. 2010;5(4):153-8. [DOI:10.1089/bfm.2010.0001] [PMID] [PMCID]
13. Tuyama AC, Cheshenko N, Carlucci MJ, Li J-H, Goldberg CL, Waller DP, et al. ACIDFORM inactivates herpes simplex virus and prevents genital herpes in a mouse model: optimal candidate for microbicide combinations. J Infect Dis. 2006;194(6):795-803. [DOI:10.1086/506948] [PMID]
14. Mastromarino P, Hemalatha R, Barbonetti A, Cinque B, Cifone M, Tammaro F, et al. Biological control of vaginosis to improve reproductive health. Indian J Med Res. 2014;140(1):91.
15. Straube J, Albert T, Manteufel J, Heinze J, Fehlhaber K, Truyen U. In vitro influence of d/l-lactic acid, sodium chloride and sodium nitrite on the infectivity of feline calicivirus and of ECHO virus as potential surrogates for foodborne viruses. Int J Food Microbiol. 2011;151(1):93-7. [DOI:10.1016/j.ijfoodmicro.2011.08.010] [PMID]
16. Kwon H-J, Kim H-H, Ryu YB, Kim JH, Jeong HJ, Lee S-W, et al. In vitro anti-rotavirus activity of polyphenol compounds isolated from the roots of Glycyrrhiza uralensis. Bioorganic & Med Chem. 2010;18(21):7668-74. [DOI:10.1016/j.bmc.2010.07.073] [PMID]
17. Clark K, Grant P, Sarr A, Belakere J, Swaggerty C, Phillips T, et al. An in vitro study of theaflavins extracted from black tea to neutralize bovine rotavirus and bovine coronavirus infections. Vet Microbiol. 1998;63(2-4):147-57. [DOI:10.1016/S0378-1135(98)00242-9]
18. Van der Strate B, Beljaars L, Molema G, Harmsen M, Meijer D. Antiviral activities of lactoferrin. Antiviral Res. 2001;52(3):225-39. [DOI:10.1016/S0166-3542(01)00195-4]
19. Superti F, Ammendolia M, Valenti P, Seganti L. Antirotaviral activity of milk proteins: lactoferrin prevents rotavirus infection in the enterocyte-like cell line HT-29. Med Microbiol Immunol. 1997;186(2):83-91. [DOI:10.1007/s004300050049] [PMID]
20. Inagaki M, Muranishi H, Yamada K, Kakehi K, Uchida K, Suzuki T, et al. Bovine κ-casein inhibits human rotavirus (HRV) infection via direct binding of glycans to HRV. J Dairy Sci. 2014;97(5):2653-61. [DOI:10.3168/jds.2013-7792] [PMID]
21. Tagg JR, Dajani AS, Wannamaker LW. Bacteriocins of gram-positive bacteria. Bacteriol Rev. 1976;40(3):722-56. [DOI:10.1128/br.40.3.722-756.1976] [PMID] [PMCID]
22. Line J, Svetoch E, Eruslanov B, Perelygin V, Mitsevich E, Mitsevich I, et al. Isolation and purification of enterocin E-760 with broad antimicrobial activity against gram-positive and gram-negative bacteria. Antimicrob Agents Chem. 2008;52(3):1094-100. [DOI:10.1128/AAC.01569-06] [PMID] [PMCID]
23. Stern N, Svetoch E, Eruslanov B, Perelygin V, Mitsevich E, Mitsevich I, et al. Isolation of a Lactobacillus salivarius strain and purification of its bacteriocin, which is inhibitory to Campylobacter jejuni in the chicken gastrointestinal system. Antimicrob Agents Chem. 2006;50(9):3111-6. [DOI:10.1128/AAC.00259-06] [PMID] [PMCID]
24. Svetoch EA, Eruslanov BV, Perelygin VV, Mitsevich EV, Mitsevich IP, Borzenkov VN, et al. Diverse antimicrobial killing by Enterococcus faecium E 50-52 bacteriocin. J Agri Food Chem. 2008;56(6):1942-8. [DOI:10.1021/jf073284g] [PMID]
25. Messaoudi S, Kergourlay G, Rossero A, Ferchichi M, Prévost H, Drider D, et al. Identification of lactobacilli residing in chicken ceca with antagonism against Campylobacter. Int Microbiol. 2011;14(2):103-10.
26. Messaoudi S, Kergourlay G, Dalgalarrondo M, Choiset Y, Ferchichi M, Prévost H, et al. Purification and characterization of a new bacteriocin active against Campylobacter produced by Lactobacillus salivarius SMXD51. Food Microbiol. 2012;32(1):129-34. [DOI:10.1016/j.fm.2012.05.002] [PMID]
27. Klaenhammer TR. Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol Rev. 1993;12(1-3):39-85. [DOI:10.1016/0168-6445(93)90057-G]
28. Cotter PD, Hill C, Ross RP. Bacteriocins: developing innate immunity for food. Nature Rev Microbiol. 2005;3(10):777-88. [DOI:10.1038/nrmicro1273] [PMID]
29. Rea MC, Ross RP, Cotter PD, Hill C. Classification of bacteriocins from Gram-positive bacteria. Prokaryotic Antimicrob Peptides: Springer; 2011. p. 29-53. [DOI:10.1007/978-1-4419-7692-5_3]
30. O'Shea EF, Gardiner GE, O'Connor PM, Mills S, Ross RP, Hill C. Characterization of enterocin-and salivaricin-producing lactic acid bacteria from the mammalian gastrointestinal tract. FEMS Microbiol Let. 2009;291(1):24-34. [DOI:10.1111/j.1574-6968.2008.01427.x] [PMID]
31. Naghmouchi K, Baah J, Hober D, Jouy E, Rubrecht C, Sané F, et al. Synergistic effect between colistin and bacteriocins in controlling Gram-negative pathogens and their potential to reduce antibiotic toxicity in mammalian epithelial cells. Antimicrob Agents Chem. 2013;57(6):2719-25. [DOI:10.1128/AAC.02328-12] [PMID] [PMCID]
32. Naghmouchi K, Le Lay C, Baah J, Drider D. Antibiotic and antimicrobial peptide combinations: synergistic inhibition of Pseudomonas fluorescens and antibiotic-resistant variants. Res Microbiol. 2012;163(2):101-8. [DOI:10.1016/j.resmic.2011.11.002] [PMID]
33. Qureshi H, Saeed S, Ahmed S, Rasool SA. Coliphage hsa as a model for antiviral studies/spectrum by some indigenous bacteriocin like inhibitory substances (BLIS). Pak J Pharma Sci. 2006;19(3):182-5.
34. Saeed S, Rasool S, Ahmad S, Zaidi S, Rehmani S. Antiviral activity of staphylococcin 188: A purified bacteriocin like inhibitory substance isolated from Staphylococcus aureus AB188. Res J Microbiol. 2007;2(11):796-806. [DOI:10.3923/jm.2007.796.806]
35. Todorov SD, Wachsman M, Tomé E, Dousset X, Destro MT, Dicks LMT, et al. Characterisation of an antiviral pediocin-like bacteriocin produced by Enterococcus faecium. Food Microbiol. 2010;27(7):869-79. [DOI:10.1016/j.fm.2010.05.001] [PMID]
36. Todorov SD, Wachsman MB, Knoetze H, Meincken M, Dicks LM. An antibacterial and antiviral peptide produced by Enterococcus mundtii ST4V isolated from soya beans. Int J Antimicrob Agents. 2005;25(6):508-13. [DOI:10.1016/j.ijantimicag.2005.02.005] [PMID]
37. Wachsman MB, Farı́as MaE, Takeda E, Sesma F, de Ruiz Holgado AP, de Torres RA, et al. Antiviral activity of enterocin CRL35 against herpesviruses. Int J Antimicrob Agents. 1999;12(4):293-9. [DOI:10.1016/S0924-8579(99)00078-3]
38. Wachsman MB, Castilla V, de Ruiz Holgado AP, de Torres RA, Sesma F, Coto CE. Enterocin CRL35 inhibits late stages of HSV-1 and HSV-2 replication in vitro. Antiviral Res. 2003;58(1):17-24. [DOI:10.1016/S0166-3542(02)00099-2]
39. Férir G, Petrova MI, Andrei G, Huskens D, Hoorelbeke B, Snoeck R, et al. The lantibiotic peptide labyrinthopeptin A1 demonstrates broad anti-HIV and anti-HSV activity with potential for microbicidal applications. PLOS ONE. 2013;8(5):e64010. [DOI:10.1371/journal.pone.0064010] [PMID] [PMCID]
40. Al Kassaa I, Hober D, Hamze M, Chihib NE, Drider D. Antiviral potential of lactic acid bacteria and their bacteriocins. Probiotics Antimicrob Protein. 2014;6(3-4):177-85. [DOI:10.1007/s12602-014-9162-6] [PMID]
41. Lange-Starke A, Petereit A, Truyen U, Braun P, Fehlhaber K, Albert T. Antiviral potential of selected starter cultures, bacteriocins and d, l-lactic acid. Food Environment Virol. 2014;6(1):42-7. [DOI:10.1007/s12560-013-9135-z] [PMID] [PMCID]
42. Walsh CT. The chemical versatility of natural-product assembly lines. Accounts Chem Res. 2008;41(1):4-10. [DOI:10.1021/ar7000414] [PMID]
43. Finking R, Marahiel MA. Biosynthesis of nonribosomal peptides. Annu Rev Microbiol. 2004;58:453-88. [DOI:10.1146/annurev.micro.58.030603.123615] [PMID]
44. Vollenbroich D, Özel M, Vater J, Kamp RM, Pauli G. Mechanism of inactivation of enveloped viruses by the biosurfactant surfactin from Bacillus subtilis. Biologicals. 1997;25(3):289-97. [DOI:10.1006/biol.1997.0099] [PMID]
45. Grandy G, Medina M, Soria R, Terán CG, Araya M. Probiotics in the treatment of acute rotavirus diarrhea. A randomized, double-blind, controlled trial using two different probiotic preparations in Bolivian children. BMC Infec Dis. 2010;10(1):1-7. [DOI:10.1186/1471-2334-10-253] [PMID] [PMCID]
46. Kotzampassi K, Giamarellos-Bourboulis EJ. Probiotics for infectious diseases: more drugs, less dietary supplementation. Int J Antimicrob Agents. 2012;40(4):288-96. [DOI:10.1016/j.ijantimicag.2012.06.006] [PMID]
47. Lee DK, Park JE, Kim MJ, Seo JG, Lee JH, Ha NJ. Probiotic bacteria, B. longum and L. acidophilus inhibit infection by rotavirus in vitro and decrease the duration of diarrhea in pediatric patients. Clin Res in Hepatol Gastroenterol. 2015;39(2):237-44. [DOI:10.1016/j.clinre.2014.09.006] [PMID]
48. Chenoll E, Casinos B, Bataller E, Buesa J, Ramón D, Genovés S, et al. Identification of a peptide produced by Bifidobacterium longum CECT 7210 with antirotaviral activity. Front Microbiol. 2016;7:655. [DOI:10.3389/fmicb.2016.00655] [PMID] [PMCID]
49. Olaya Galán N, Ulloa Rubiano J, Velez Reyes F, Fernandez Duarte K, Salas Cardenas S, Gutierrez Fernandez M. In vitro antiviral activity of Lactobacillus casei and Bifidobacterium adolescentis against rotavirus infection monitored by NSP 4 protein production. J Appl Microbiol. 2016;120(4):1041-51. [DOI:10.1111/jam.13069] [PMID]
50. Garaicoechea L, Olichon A, Marcoppido G, Wigdorovitz A, Mozgovoj M, Saif L, et al. Llama-derived single-chain antibody fragments directed to rotavirus VP6 protein possess broad neutralizing activity in vitro and confer protection against diarrhea in mice. J Virol. 2008;82(19):9753-64. [DOI:10.1128/JVI.00436-08] [PMID] [PMCID]
51. Hamers-Casterman C, Atarhouch T, Muyldermans Sa, Robinson G, Hammers C, Songa EB, et al. Naturally occurring antibodies devoid of light chains. Nature. 1993;363(6428):446-8. [DOI:10.1038/363446a0] [PMID]
52. Aoki-Yoshida A, Saito S, Fukiya S, Aoki R, Takayama Y, Suzuki C, et al. Lactobacillus rhamnosus GG increases Toll-like receptor 3 gene expression in murine small intestine ex vivo and in vivo. Benef Microb. 2016;7(3):421-9. [DOI:10.3920/BM2015.0169] [PMID]
53. Hagbom M, Sharma S, Lundgren O, Svensson L. Towards a human rotavirus disease model. Current Opinion Virol. 2012;2(4):408-18. [DOI:10.1016/j.coviro.2012.05.006] [PMID]
54. Liu F, Li G, Wen K, Bui T, Cao D, Zhang Y, et al. Porcine small intestinal epithelial cell line (IPEC-J2) of rotavirus infection as a new model for the study of innate immune responses to rotaviruses and probiotics. Viral Immunol. 2010;23(2):135-49. [DOI:10.1089/vim.2009.0088] [PMID] [PMCID]
55. Mao X, Gu C, Hu H, Tang J, Chen D, Yu B, et al. Dietary Lactobacillus rhamnosus GG supplementation improves the mucosal barrier function in the intestine of weaned piglets challenged by porcine rotavirus. PLOS ONE. 2016;11(1):e0146312. [DOI:10.1371/journal.pone.0146312] [PMID] [PMCID]
56. Szajewska H, Wanke M, Patro B. Meta‐analysis: The effects of Lactobacillus rhamnosus GG supplementation for the prevention of healthcare‐associated diarrhea in children. Alimen Pharma Ther. 2011;34(9):1079-87. [DOI:10.1111/j.1365-2036.2011.04837.x] [PMID]
57. Álvarez B, Krogh-Andersen K, Tellgren-Roth C, Martínez N, Günaydın G, Lin Y, et al. An exopolysaccharide-deficient mutant of Lactobacillus rhamnosus GG efficiently displays a protective llama antibody fragment against rotavirus on its surface. Appl Environm Microbiol. 2015;81(17):5784-93. [DOI:10.1128/AEM.00945-15] [PMID] [PMCID]
58. Prahoveanu E, Eşanu V, Cajal N, Veidenfeld-Stein R, Brinduşă-Diaconescu E. Effect of several unpurified milk preparations on experimental influenza infection in mice. Virologie. 1986;37(1):49-53.
59. Botić T, Danø T, Weingartl H, Cencič A. A novel eukaryotic cell culture model to study antiviral activity of potential probiotic bacteria. Int J Food Microbiol. 2007;115(2):227-34. [DOI:10.1016/j.ijfoodmicro.2006.10.044] [PMID]
60. Choi H-J, Song J-H, Ahn Y-J, Baek S-H, Kwon D-H. Antiviral activities of cell-free supernatants of yogurts metabolites against some RNA viruses. Europ Food Res Tech. 2009;228(6):945-50. [DOI:10.1007/s00217-009-1009-0]
61. Aboubakr HA, El-Banna AA, Youssef MM, Al-Sohaimy SA, Goyal SM. Antiviral effects of Lactococcus lactis on feline calicivirus, a human norovirus surrogate. Food Environm Virol. 2014;6(4):282-9. [DOI:10.1007/s12560-014-9164-2] [PMID] [PMCID]
62. Rodger SM, Schnagl RD, Holmes I. Further biochemical characterization, including the detection of surface glycoproteins, of human, calf, and simian rotaviruses. J Virol. 1977;24(1):91-8. [DOI:10.1128/jvi.24.1.91-98.1977] [PMID] [PMCID]
63. Shearer AE, Hoover DG, Kniel KE. Effect of bacterial cell-free supernatants on infectivity of norovirus surrogates. J Food Protect. 2014;77(1):145-9. [DOI:10.4315/0362-028X.JFP-13-204] [PMID]
64. Rigo-Adrover M, Saldaña-Ruíz S, Van Limpt K, Knipping K, Garssen J, Knol J, et al. A combination of scGOS/lcFOS with Bifidobacterium breve M-16V protects suckling rats from rotavirus gastroenteritis. Europ J Nut. 2017;56(4):1657-70. [DOI:10.1007/s00394-016-1213-1] [PMID]
65. Liévin-Le Moal V, Servin AL. Anti-infective activities of lactobacillus strains in the human intestinal microbiota: from probiotics to gastrointestinal anti-infectious biotherapeutic agents. Clin Microbiol Rev. 2014;27(2):167-99. [DOI:10.1128/CMR.00080-13] [PMID] [PMCID]

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.