Intestinal Innate Antiviral Immunity and Immunobiotics: Beneficial Effects Against Rotavirus Infection

Overview

Journal Front Immunol

Specialty Allergy & Immunology

Date 2016 Dec 21

PMID 27994593

Citations 54

Authors

Julio Villena

Maria Guadalupe Vizoso-Pinto

Haruki Kitazawa

Affiliations

Soon will be listed here.

Abstract

The mucosal tissues of the gastrointestinal tract are the main portal entry of pathogens such as rotavirus (RV), which is a leading cause of death due to diarrhea among young children across the globe and a major cause of severe acute intestinal infection in livestock animals. The interactions between intestinal epithelial cells (IECs) and immune cells with RVs have been studied for several years, and now, it is known that the innate immune responses triggered by this virus can have both beneficial and detrimental effects for the host. It was demonstrated that natural RV infection in infants and experimental challenges in mice result in the intestinal activation of pattern recognition receptors (PRRs) such as toll-like receptor 3 (TLR3) and striking secretion of proinflammatory mediators that can lead to increased local tissue damage and immunopathology. Therefore, modulating desregulated intestinal immune responses triggered by PRRs activation are a significant promise for reducing the burden of RV diseases. The ability of immunoregulatory probiotic microorganisms (immunobiotics) to protect against intestinal infections, such as those caused by RVs, is among the oldest effects studied for these important group of beneficial microbes. In this review, we provide an update of the current status on the modulation of intestinal antiviral innate immunity by immunobiotics and their beneficial impact on RV infection. In addition, we describe the research of our group that demonstrated the capacity of immunobiotic strains to beneficially modulated TLR3-triggered immune response in IECs, reduce the disruption of intestinal homeostasis caused by intraepithelial lymphocytes, and improve the resistance to RV infections.

Citing Articles

Probiotics beyond the farm: Benefits, costs, and considerations of using antibiotic alternatives in livestock.

Leistikow K, Beattie R, Hristova K Front Antibiot. 2025; 1():1003912.

PMID: 39816405 PMC: 11732145. DOI: 10.3389/frabi.2022.1003912.

Biotechnological Interventions for the Production of Subunit Vaccines Against Group A Rotavirus.

Prajapati M, Malik P, Sinha A, Yadav H, Jaiwal Y, Ahlawat Y Cell Biochem Funct. 2024; 42(8):e70031.

PMID: 39707603 PMC: 11662099. DOI: 10.1002/cbf.70031.

-derived peptides disrupt quorum sensing and biofilm assembly in multidrug-resistant .

Leistikow K, May D, Suh W, Vargas Asensio G, Schaenzer A, Currie C mSystems. 2024; 9(8):e0071224.

PMID: 38990088 PMC: 11334493. DOI: 10.1128/msystems.00712-24.

Vaccine targeting to mucosal lymphoid tissues promotes humoral immunity in the gastrointestinal tract.

Kocabiyik O, Amlashi P, Vo A, Suh H, Rodriguez-Aponte S, Dalvie N Sci Adv. 2024; 10(22):eadn7786.

PMID: 38809992 PMC: 11135404. DOI: 10.1126/sciadv.adn7786.

evaluation of the immunomodulatory and wakame assimilation properties of strains from swine milk.

Ohgi R, Saha S, Zhou B, Sakuma T, Sakurai M, Nakano Y Front Microbiol. 2024; 15:1324999.

PMID: 38343714 PMC: 10858614. DOI: 10.3389/fmicb.2024.1324999.

References

Guarino A, Canani R, Spagnuolo M, Albano F, Di Benedetto L . Oral bacterial therapy reduces the duration of symptoms and of viral excretion in children with mild diarrhea. J Pediatr Gastroenterol Nutr. 1997; 25(5):516-9. DOI: 10.1097/00005176-199711000-00005. View

Frias A, Jones R, Fifadara N, Vijay-Kumar M, Gewirtz A . Rotavirus-induced IFN-β promotes anti-viral signaling and apoptosis that modulate viral replication in intestinal epithelial cells. Innate Immun. 2011; 18(2):294-306. DOI: 10.1177/1753425911401930. View

Bardach A, Ciapponi A, Garcia-Marti S, Glujovsky D, Mazzoni A, Fayad A . Epidemiology of acute otitis media in children of Latin America and the Caribbean: a systematic review and meta-analysis. Int J Pediatr Otorhinolaryngol. 2011; 75(9):1062-70. DOI: 10.1016/j.ijporl.2011.05.014. View

Tada A, Zelaya H, Clua P, Salva S, Alvarez S, Kitazawa H . Immunobiotic Lactobacillus strains reduce small intestinal injury induced by intraepithelial lymphocytes after Toll-like receptor 3 activation. Inflamm Res. 2016; 65(10):771-83. DOI: 10.1007/s00011-016-0957-7. View

Barro M, Patton J . Rotavirus NSP1 inhibits expression of type I interferon by antagonizing the function of interferon regulatory factors IRF3, IRF5, and IRF7. J Virol. 2007; 81(9):4473-81. PMC: 1900170. DOI: 10.1128/JVI.02498-06. View

Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W . Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993; 75(2):263-74. DOI: 10.1016/0092-8674(93)80068-p. View

Tate J, Patel M, Cortese M, Lopman B, Gentsch J, Fleming J . Remaining issues and challenges for rotavirus vaccine in preventing global childhood diarrheal morbidity and mortality. Expert Rev Vaccines. 2012; 11(2):211-20. DOI: 10.1586/erv.11.184. View

Edmond K, Scott S, Korczak V, Ward C, Sanderson C, Theodoratou E . Long term sequelae from childhood pneumonia; systematic review and meta-analysis. PLoS One. 2012; 7(2):e31239. PMC: 3285155. DOI: 10.1371/journal.pone.0031239. View

Jiang W, Wang X, Zeng B, Liu L, Tardivel A, Wei H . Recognition of gut microbiota by NOD2 is essential for the homeostasis of intestinal intraepithelial lymphocytes. J Exp Med. 2013; 210(11):2465-76. PMC: 3804938. DOI: 10.1084/jem.20122490. View

10.

Hansen C, Holm T, Krych L, Andresen L, Nielsen D, Rune I . Gut microbiota regulates NKG2D ligand expression on intestinal epithelial cells. Eur J Immunol. 2012; 43(2):447-57. DOI: 10.1002/eji.201242462. View

11.

Bryce J, Victora C . Child survival: countdown to 2015. Lancet. 2005; 365(9478):2153-4. DOI: 10.1016/S0140-6736(05)66752-9. View

12.

Suzuki H, Jeong K, Itoh K, Doi K . Regional variations in the distributions of small intestinal intraepithelial lymphocytes in germ-free and specific pathogen-free mice. Exp Mol Pathol. 2002; 72(3):230-5. DOI: 10.1006/exmp.2002.2433. View

13.

Kandasamy S, Vlasova A, Fischer D, Kumar A, Chattha K, Rauf A . Differential Effects of Escherichia coli Nissle and Lactobacillus rhamnosus Strain GG on Human Rotavirus Binding, Infection, and B Cell Immunity. J Immunol. 2016; 196(4):1780-9. PMC: 4744595. DOI: 10.4049/jimmunol.1501705. View

14.

Arnold M, Sen A, Greenberg H, Patton J . The battle between rotavirus and its host for control of the interferon signaling pathway. PLoS Pathog. 2013; 9(1):e1003064. PMC: 3554623. DOI: 10.1371/journal.ppat.1003064. View

15.

Sen A, Rothenberg M, Mukherjee G, Feng N, Kalisky T, Nair N . Innate immune response to homologous rotavirus infection in the small intestinal villous epithelium at single-cell resolution. Proc Natl Acad Sci U S A. 2012; 109(50):20667-72. PMC: 3528539. DOI: 10.1073/pnas.1212188109. View

16.

MacPherson C, Audy J, Mathieu O, Tompkins T . Multistrain probiotic modulation of intestinal epithelial cells' immune response to a double-stranded RNA ligand, poly(i·c). Appl Environ Microbiol. 2013; 80(5):1692-700. PMC: 3957618. DOI: 10.1128/AEM.03411-13. View

17.

Isolauri E, Kaila M, Mykkanen H, Ling W, Salminen S . Oral bacteriotherapy for viral gastroenteritis. Dig Dis Sci. 1994; 39(12):2595-600. DOI: 10.1007/BF02087695. View

18.

Ciarlet M, Estes M . Rotavirus and calicivirus infections of the gastrointestinal tract. Curr Opin Gastroenterol. 2006; 17(1):10-6. DOI: 10.1097/00001574-200101000-00003. View

19.

Kawai T, Akira S . Innate immune recognition of viral infection. Nat Immunol. 2006; 7(2):131-7. DOI: 10.1038/ni1303. View

20.

Kawaguchi M, Nanno M, Umesaki Y, Matsumoto S, Okada Y, Cai Z . Cytolytic activity of intestinal intraepithelial lymphocytes in germ-free mice is strain dependent and determined by T cells expressing gamma delta T-cell antigen receptors. Proc Natl Acad Sci U S A. 1993; 90(18):8591-4. PMC: 47403. DOI: 10.1073/pnas.90.18.8591. View