Skip to main content
PMC home page
Elsevier - PMC COVID-19 Collection logoLink to Elsevier - PMC COVID-19 Collection
. 2012 Apr 10;16(2):129–135. doi: 10.1016/S1413-8670(12)70293-3

In vitro study of the effect of a probiotic bacterium Lactobacillus rhamnosus against herpes simplex virus type 1

Soghra Khani a, Mohammad Motamedifar a,*, Hossein Golmoghaddam b, Hamideh Mahmoodzadeh Hosseini c, Zahra Hashemizadeh a
PMCID: PMC7128665  PMID: 22552453

Abstract

Background

Due to the emergence of drug resistance in herpes simplex virus type 1 (HSV-1), researchers are trying to find other methods for treating herpes simplex virus type 1 infections. Probiotic bacteria are effective in macrophage activation and may have antiviral activities.

Objective

This study aimed at verifying the direct effect of Lactobacillus rhamnosus, a probiotic bacterium, in comparison with Escherichia coli, a non-probiotic one, on HSV-1 infection, and determining its effect on macrophage activation for in vitro elimination of HSV-1 infection.

Methods

The above bacteria were introduced into HSV-1 infected Vero cells, and their effects were examined using both MTT and plaque assay. To determine macrophage activation against in vitro HSV-1 infection, J774 cells were exposed to these bacteria; then, macrophage viability was examined with the MTT method, and tumor necrosis factor alpha (TNF-α), Interferon-gamma (IFN-γ), and nitric oxide (NO) assessments were performed using the ELISA method.

Results

A significant increased viability of macrophages was observed (p < 0.05) in the presence of Lactobacillus rhamnosus before and after HSV-1 infection when compared with Escherichia coli as a non-probiotic bacterium. However, tumor necrosis factor α concentration produced by Escherichia coli-treated J774 cells was significantly higher than Lactobacillus rhamnosus-treated J774 cells (p < 0.05). Interferon-gamma and NO production were not different in the groups treated with Escherichia coli or with Lactobacillus rhamnosus.

Conclusion

The results of this study indicate that Lactobacillus rhamnosus enhances macrophage viability for HSV-1 elimination and activation against HSV-1 more effectively, when compared with non-probiotic Escherichia coli. It also seems that receptor occupation of macrophage sites decreases HSV-1 infectivity by both of the studied bacteria.

Keywords: Probiotic, Lactobacillus rhamnosus, Herpes simplex virus type 1

References

  • 1.Geo F.B., Carroll K.C., Butel J.S., Morse S.A. Herpesviruses. In: Jawetz, Melnick, Adelberg's, editors. Medical Microbiology. 24th ed. McGraw-Hill Companies USA; 2007. pp. 428–437. [Google Scholar]
  • 2.Kapikian A., Hoshino Y., Chanock R. Rotaviruses. In: Knipe D., Howley P., editors. Fields Virology. 5 ed. Lippincott Williams & Wilkins; Philadelphia: 2007. pp. 2479–2601. [Google Scholar]
  • 3.Whitley R.J. Herpes simplex virus infection. Semin Pediatr Infect Dis. 2002;13(1):6–11. doi: 10.1053/spid.2002.29752. [DOI] [PubMed] [Google Scholar]
  • 4.Biswas S., Tiley L.S., Zimmermann H. Mutations close to functional motif IV in HSV-1 UL5 helicase that confer resistance to HSV helicase-primase inhibitors, variously affect virus growth rate and pathogenicity. Antiviral Res. 2008;80(1):81–85. doi: 10.1016/j.antiviral.2008.04.005. [DOI] [PubMed] [Google Scholar]
  • 5.Frobert E., Thouvenot D., Lina B. Genotyping diagnosis of acyclovir resistant herpes simplex virus. J Pathol Biol. 2007;55(10):504–511. doi: 10.1016/j.patbio.2007.08.005. [DOI] [PubMed] [Google Scholar]
  • 6.Pietka-Ottlik M., Wójtowicz-Młochowska H., Kołodziejczyk K. New organoselenium compounds active against pathogenic bacteria, fungi and viruses. Chem Pharm Bull. 2008;56(10):1423–1427. doi: 10.1248/cpb.56.1423. [DOI] [PubMed] [Google Scholar]
  • 7.Wang H., Vincent Ooi E., Ang P.O., Jr. Antiviral activities of extracts from Hong Kong seaweeds. J Zhejiang Univ Sci B. 2008;9(12):969–976. doi: 10.1631/jzus.B0820154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Kratz J.M., Andrighetti-Fröhner C.R., Kolling D.J. Anti- HSV-1 and anti-HIV-1 activity of gallic acid and pentyl gallate. Mem Inst Oswaldo Cruz. 2008;103(5):437–442. doi: 10.1590/s0074-02762008000500005. [DOI] [PubMed] [Google Scholar]
  • 9.Rajbhandari M., Mentel R., Jha P.K. Antiviral activity of some plants used in nepalese traditional medicine. Evid Based Complement Alternat Med. 2009;6(4):517–522. doi: 10.1093/ecam/nem156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Koch C., Reichling J., Kehm R. Efficacy of anise oil, dwarfpine oil and chamomile oil against thymidine-kinase-positive and thymidine-kinase-negative herpesviruses. J Pharm Pharmacol. 2008;60(11):1545–1550. doi: 10.1211/jpp/60.11.0017. [DOI] [PubMed] [Google Scholar]
  • 11.Ivec M., Botic T., Koren S. Interactions of macrophages with probiotic bacteria lead to increased antiviral response against vesicular stomatitis virus. Antiviral Res. 2007;75(3):266–274. doi: 10.1016/j.antiviral.2007.03.013. [DOI] [PubMed] [Google Scholar]
  • 12.Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol. 2003;3:133–146. doi: 10.1038/nri1001. [DOI] [PubMed] [Google Scholar]
  • 13.Denis M. Human monocytes/macrophages: NO or no NO? J Leukoc Biol. 1994;55(5):682–684. doi: 10.1002/jlb.55.5.682. [DOI] [PubMed] [Google Scholar]
  • 14.MacMicking J., Xie Q.W., Nathan C. Nitric oxide and macrophage function. Annu Rev Immunol. 1997;15:323–509. doi: 10.1146/annurev.immunol.15.1.323. [DOI] [PubMed] [Google Scholar]
  • 15.Ellermann-Eriksen S. Macrophages and cytokines in the early defence against herpes simplex virus. J Virol. 2005;2:59–89. doi: 10.1186/1743-422X-2-59. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Miettinen M., Lehtonen A., Julkunen I., Matikainen S. Lactobacilli and Streptococci Activate NF-kB and STAT Signaling Pathways in Human Macrophages. J Immunol. 2000;164(7):3733–3740. doi: 10.4049/jimmunol.164.7.3733. [DOI] [PubMed] [Google Scholar]
  • 17.Morita H., He F., Fuse T. Cytokine production by the murine macrophage cell line J774.1 after exposure to lactobacilli. Biosci Biotechnol Biochem. 2002;66(9):1963–1966. doi: 10.1271/bbb.66.1963. [DOI] [PubMed] [Google Scholar]
  • 18.Gessani S., Belardelli F., Pecorelli A. Bacterial lipopolisaccharide and gamma interferon induce transcription of beta interferon mRNA and interferon secretion in murine macrophages. J Virol. 1989;63(6):2785–2789. doi: 10.1128/jvi.63.6.2785-2789.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Kidd P. Th1/Th2 balance: the hypothesis, its limitations, and implications for health and disease. Altern Med Rev. 2003;8(3):223–246. [PubMed] [Google Scholar]
  • 20.Kim D.W., Cho S.B., Yun C.H. Induction of cytokines and nitric oxide in murine macrophages stimulated with enzymatically digested lactobacillus strains. J Microbiol. 2007;45(5):373–378. [PubMed] [Google Scholar]
  • 21.Martin L. Cross. Immunoregulation by probiotic Lactobacilli: pro-Th1 signals and their relevance to human health. Clin Applied Immunol. 2002;3(3):115–125. [Google Scholar]
  • 22.Acheson D.W., Luccioli S. Microbial-gut interactions in health and disease. Mucosal immune responses. Best Pract Res Clin Gastroenterol. 2004;18(2):387–404. doi: 10.1016/j.bpg.2003.11.002. [DOI] [PubMed] [Google Scholar]
  • 23.Oberhelman R.A., Gilman R.H., Sheen P. A placebocontrolled trial of Lactobacillus GG to prevent diarrhea in undernourished Peruvian children. J Pediatr. 1999;134(1):15–20. doi: 10.1016/s0022-3476(99)70366-5. [DOI] [PubMed] [Google Scholar]
  • 24.Parvez S., Malik K.A., Ah Kang S., Kim H.Y. Probiotics and their fermented food products are beneficial for health. J Appl Microbiol. 2006;100(6):1171–1185. doi: 10.1111/j.1365-2672.2006.02963.x. [DOI] [PubMed] [Google Scholar]
  • 25.Rizzello V., Bonaccorsi I., Dongarra M.L. Role of natural killer and dendritic cell crosstalk in immunomodulation by commensal bacteria probiotics. J Biomed and Biotechnol. 2011:473097. doi: 10.1155/2011/473097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Takeda K., Suzuki T., Shimada S.I. Interleukin-12 is involved in the enhancement of human natural killer cell activity by Lactobacillus casei Shirota. Clin and Experimental Immunol. 2006;146:109–115. doi: 10.1111/j.1365-2249.2006.03165.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.LiaskovskInline graphic T.M., Rybalko S.L., PidhorskyInline graphic V.S. Effect of probiotic Lactic acid bacteria strains on virus infection. Microbiol Z. 2007;69(2):55–63. [PubMed] [Google Scholar]
  • 28.Motamedifar M., Nekooeian A.A., Moatari A. The effect of hydroalcoholic extract of olive leaves against herpes simplex virus type 1. Iran J Med Sci. 2007;32:222–226. [Google Scholar]
  • 29.Leary J.J., Wittrock R., Sarisky R.T. Susceptibilities of herpes simplex viruses to penciclovir and acyclovir in eight cell lines. Antimicrob Agents Chemother. 2002;46(3):762–768. doi: 10.1128/AAC.46.3.762-768.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Bergamini A., Perno C.F., Capozzi M. Tetrazolium-based colorimetric assay for quantificationof HIV-1-induced cytopathogenicity in monocyte-macrophages exposed tomacrophage-colony-stimulating factor. J Virol Methods. 1992;40(3):275–286. doi: 10.1016/0166-0934(92)90086-s. [DOI] [PubMed] [Google Scholar]
  • 31.Green L.C., Wagner D.A., Glogowski J. Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Anal Biochem. 1982;126(1):131–138. doi: 10.1016/0003-2697(82)90118-x. [DOI] [PubMed] [Google Scholar]
  • 32.Szajewska H., Mrukowicz J.Z. Probiotics in the treatment and prevention of acute infectious diarrhea in infants and children: a systematic review of published randomized, double-blind, placebo-controlled trials. J Pediatr Gastroenterol Nutr. 2001;33(Suppl 2):17–25. doi: 10.1097/00005176-200110002-00004. [DOI] [PubMed] [Google Scholar]
  • 33.Conti C., Malaciino C., Mastromarino P. Inhibition of herpes simplex virus type 2 by vaginal Lactobacilli. J Physiol Pharmacol. 2009;60(Suppl 6):19–26. [PubMed] [Google Scholar]
  • 34.Botic T., Klingberg T.D., Weingartl H. A novel eukaryotic cell culture model to study antiviral activity of potential probiotic bacteria. Int J Food Microbiol. 2007;115(2):227–234. doi: 10.1016/j.ijfoodmicro.2006.10.044. [DOI] [PubMed] [Google Scholar]
  • 35.Jozsef L., Khreiss T., Filep J.G. CpG motifs in bacterial DNA delay apoptosis of neutrophil granulocytes. FASEB J. 2004;18(14):1776–1778. doi: 10.1096/fj.04-2048fje. [DOI] [PubMed] [Google Scholar]
  • 36.Abbas A.K., Lichtman A.H., Pillai S. 6th ed. Elsevier; Philadelphia: 2007. Cellular And Molecular Immunology. [Google Scholar]
  • 37.Korhonen R., Korpela R., Saxelin M. Induction of Nitric Oxide Synthesis by Probiotic Lactobacillus rhamnosus GG in J774 Macrophages and Human T84 Intestinal Epithelial Cells. Inflammation. 2001;25(4):223–232. doi: 10.1023/a:1010971703271. [DOI] [PubMed] [Google Scholar]

Articles from The Brazilian Journal of Infectious Diseases are provided here courtesy of Elsevier

RESOURCES