Abstract
Due to the lower efficacy of currently approved live attenuated rotavirus (RV) vaccines in developing countries, a new approach to the development of safe mucosally administered live bacterial vectors is being considered, using probiotic bacteria as an efficient delivery platform for heterologous RV antigens. Lactic acid bacteria (LAB), which are considered food-grade bacteria and normal microbiota, have been utilized throughout history as probiotics and developed since the 1990s as a delivery system for recombinant heterologous proteins. Over the last decade, LAB have frequently been used as a platform for the delivery of various RV antigens to the mucosa. Given the appropriate safety profile for neonates and providing the benefits of probiotics, recombinant LAB-based vaccines could potentially address the need for a subunit RV vaccine. The present review focuses mainly on different recombinant LAB vaccine constructs for RV and their potential as an alternative recombinant vaccine against RV disease.
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Afchangi A, Arashkia A, Shahosseini Z, Jalilvand S, Marashi SM, Roohvand F, Mohajel N, Shoja Z (2018) Immunization of mice by rotavirus NSP4-VP6 fusion protein elicited stronger responses compared to VP6 alone. Viral Immunol 31:233–241
Afchangi A, Jalilvand S, Mohajel N, Marashi SM, Shoja Z (2019) Rotavirus VP6 as a potential vaccine candidate. Rev Med Virol 29:e2027
Ahmed SM, Hall AJ, Robinson AE, Verhoef L, Premkumar P, Parashar UD, Koopmans M, Lopman BA (2014) Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis 14:725–730
Al Kassaa I (2016) New insights on antiviral probiotics: from research to applications. Springer
Al Kassaa I (2017) Antiviral Probiotics: A New Concept in Medical Sciences. New Insights on Antiviral Probiotics. Springer, pp 1-46
Álvarez B, Krogh-Andersen K, Tellgren-Roth C, Martínez N, Günaydın G, Lin Y, Martín MC, Álvarez MA, Hammarström L, Marcotte H (2015) An exopolysaccharide-deficient mutant of Lactobacillus rhamnosus GG efficiently displays a protective llama antibody fragment against rotavirus on its surface. Appl Environ Microbiol 81:5784–5793
Aoki-Yoshida A, Saito S, Fukiya S, Aoki R, Takayama Y, Suzuki C, Sonoyama K (2016) Lactobacillus rhamnosus GG increases Toll-like receptor 3 gene expression in murine small intestine ex vivo and in vivo. Benef Microbes 7:421–429
Armah GE, Sow SO, Breiman RF, Dallas MJ, Tapia MD, Feikin DR, Binka FN, Steele AD, Laserson KF, Ansah NA, Levine MM, Lewis K, Coia ML, Attah-Poku M, Ojwando J, Rivers SB, Victor JC, Nyambane G, Hodgson A, Schodel F, Ciarlet M, Neuzil KM (2010) Efficacy of pentavalent rotavirus vaccine against severe rotavirus gastroenteritis in infants in developing countries in sub-Saharan Africa: a randomised, double-blind, placebo-controlled trial. Lancet 376:606–614
Azagra-Boronat I, Massot-Cladera M, Knipping K, Garssen J, Ben Amor K, Knol J, Franch À, Castell M, Rodríguez-Lagunas MJ, Pérez-Cano FJ (2020) Strain-Specific probiotic properties of bifidobacteria and lactobacilli for the prevention of diarrhea caused by rotavirus in a preclinical model. Nutrients 12:498
Banyai K, Estes MK, Martella V, Parashar UD (2018) Viral gastroenteritis. Lancet 392:175–186
Baral TN, MacKenzie R, Arbabi Ghahroudi M (2013) Single‐domain antibodies and their utility. Curr Protocols Immunol 103:2.17. 11-12.17. 57
Bermudez-Brito M, Plaza-Díaz J, Muñoz-Quezada S, Gómez-Llorente C, Gil A (2012) Probiotic mechanisms of action. Ann Nutr Metab 61:160–174
Bernet M-F, Brassart D, Neeser J-R, Servin A (1994) Lactobacillus acidophilus LA 1 binds to cultured human intestinal cell lines and inhibits cell attachment and cell invasion by enterovirulent bacteria. Gut 35:483–489
Besselink MG, van Santvoort HC, Buskens E, Boermeester MA, van Goor H, Timmerman HM, Nieuwenhuijs VB, Bollen TL, van Ramshorst B, Witteman BJ (2008) Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial. The Lancet 371:651–659
Bhandari N, Rongsen-Chandola T, Bavdekar A, John J, Antony K, Taneja S, Goyal N, Kawade A, Kang G, Rathore SS, Juvekar S, Muliyil J, Arya A, Shaikh H, Abraham V, Vrati S, Proschan M, Kohberger R, Thiry G, Glass R, Greenberg HB, Curlin G, Mohan K, Harshavardhan GV, Prasad S, Rao TS, Boslego J, Bhan MK, India Rotavirus Vaccine G (2014) Efficacy of a monovalent human-bovine (116E) rotavirus vaccine in Indian children in the second year of life. Vaccine 32(Suppl 1):A110-116
Bhandari N, Rongsen-Chandola T, Bavdekar A, John J, Antony K, Taneja S, Goyal N, Kawade A, Kang G, Rathore SS, Juvekar S, Muliyil J, Arya A, Shaikh H, Abraham V, Vrati S, Proschan M, Kohberger R, Thiry G, Glass R, Greenberg HB, Curlin G, Mohan K, Harshavardhan GV, Prasad S, Rao TS, Boslego J, Bhan MK, India Rotavirus Vaccine G (2014) Efficacy of a monovalent human-bovine (116E) rotavirus vaccine in Indian infants: a randomised, double-blind, placebo-controlled trial. Lancet 383:2136–2143
Bishop RF, Davidson GP, Holmes IH, Ruck BJ (1973) Virus particles in epithelial cells of duodenal mucosa from children with acute non-bacterial gastroenteritis. Lancet 2:1281–1283
Bishop RF, Davidson GP, Holmes IH, Ruck BJ (1974) Detection of a new virus by electron microscopy of faecal extracts from children with acute gastroenteritis. Lancet 1:149–151
Britton RA, Versalovic J (2008) Probiotics and gastrointestinal infections. Interdiscip Perspect Infect Dis 2008
Brown EM, Ke X, Hitchcock D, Jeanfavre S, Avila-Pacheco J, Nakata T, Arthur TD, Fornelos N, Heim C, Franzosa EA (2019) Bacteroides-derived sphingolipids are critical for maintaining intestinal homeostasis and symbiosis. Cell Host Microbe 25(668–680):e667
Burke RM, Tate JE, Kirkwood CD, Steele AD, Parashar UD (2019) Current and new rotavirus vaccines. Curr Opin Infect Dis 32:435–444
Burnett E, Parashar UD, Tate JE (2020) Real-world effectiveness of rotavirus vaccines, 2006–19: a literature review and meta-analysis. Lancet Global Health 8:e1195–e1202
Caddy SL, Vaysburd M, Wing M, Foss S, Andersen JT, O ‘Connell K, Mayes K, Higginson K, Iturriza-Gómara M, Desselberger U, James LC (2020) Intracellular neutralisation of rotavirus by VP6-specific IgG. PLoS pathogens 16:e1008732
Cano-Garrido O, Seras-Franzoso J, Garcia-Fruitós E (2015) Lactic acid bacteria: reviewing the potential of a promising delivery live vector for biomedical purposes. Microbial Cell Factor 14:1–12
Castiglione F, Lazzarini A, Carrano L, Corti E, Ciciliato I, Gastaldo L, Candiani P, Losi D, Marinelli F, Selva E (2008) Determining the structure and mode of action of microbisporicin, a potent lantibiotic active against multiresistant pathogens. Chem Biol 15:22–31
Choi AH, McNeal MM, Basu M, Flint JA, Stone SC, Clements JD, Bean JA, Poe SA, VanCott JL, Ward RL (2002) Intranasal or oral immunization of inbred and outbred mice with murine or human rotavirus VP6 proteins protects against viral shedding after challenge with murine rotaviruses. Vaccine 20:3310–3321
Conner M, Zarley C, Hu B, Parsons S, Drabinski D, Greiner S, Smith R, Jiang B, Corsaro B, Madore H (1996) Virus-like particles as a rotavirus subunit vaccine. J Infect Dis 174:S88–S92
De Vrese M, Offick B (2010) Probiotics and prebiotics: effects on diarrhea. Bioactive foods in promoting health. Elsevier, pp 205–227
Desselberger U (2017) Differences of rotavirus vaccine effectiveness by country: likely causes and contributing factors. Pathogens 6:65
Didari T, Solki S, Mozaffari S, Nikfar S, Abdollahi M (2014) A systematic review of the safety of probiotics. Expert Opinion Drug Safety 13:227–239
Dieye Y, Usai S, Clier F, Gruss A, Piard J-C (2001) Design of a protein-targeting system for lactic acid bacteria. J Bacteriol 183:4157–4166
Ding C, Ma J, Dong Q, Liu Q (2018) Live bacterial vaccine vector and delivery strategies of heterologous antigen: a review. Immunol Lett 197:70–77
do Carmo MS, itapary dos Santos C, Araújo MC, Girón JA, Fernandes ES, Monteiro-Neto V (2018) Probiotics, mechanisms of action, and clinical perspectives for diarrhea management in children. Food Funct 9:5074–5095
Enouf V, Langella P, Commissaire J, Cohen J, Corthier G (2001) Bovine rotavirus nonstructural protein 4 produced by Lactococcus lactis is antigenic and immunogenic. Appl Environm Microbiol 67:1423–1428
Esteban LE, Temprana CF, Argüelles M, Glikmann G, Castello AA (2013) Antigenicity and immunogenicity of rotavirus VP6 protein expressed on the surface of Lactococcus lactis. BioMed Res Int 2013:298598
Esteban LE, Temprana CF, Argüelles M, Glikmann G, Castello AA (2013) Antigenicity and immunogenicity of rotavirus VP6 protein expressed on the surface of Lactococcus lactis. BioMed Res Int
Feng N, Lawton JA, Gilbert J, Kuklin N, Vo P, Prasad BV, Greenberg HB (2002) Inhibition of rotavirus replication by a non-neutralizing, rotavirus VP6-specific IgA mAb. J Clin Investig 109:1203–1213
Fernandez-Duarte KP, Olaya-Galán NN, Salas-Cárdenas SP, Lopez-Rozo J, Gutierrez-Fernandez MF (2018) Bifidobacterium adolescentis (DSM 20083) and lactobacillus casei (Lafti L26-DSL): probiotics able to block the in vitro adherence of rotavirus in MA104 cells. Probiot Antimicrob Prot 10:56–63
Figueroa-González I, Cruz-Guerrero A, Quijano G (2011) The benefits of probiotics on human health. J Microbial Biochem Technol S 1:1948–5948
Flewett TH, Bryden AS, Davies H (1973) Letter: Virus particles in gastroenteritis. Lancet 2:1497
Gampa A, Engen PA, Shobar R, Mutlu EA (2017) Relationships between gastrointestinal microbiota and blood group antigens. Physiolog Genom 49:473–483
Garaicoechea L, Aguilar A, Parra GI, Bok M, Sosnovtsev SV, Canziani G, Green KY, Bok K, Parreño V (2015) Llama nanoantibodies with therapeutic potential against human norovirus diarrhea. PloS one 10:e0133665
Glass RI, Parashar UD, Bresee JS, Turcios R, Fischer TK, Widdowson MA, Jiang B, Gentsch JR (2006) Rotavirus vaccines: current prospects and future challenges. Lancet 368:323–332
Gonzalez-Ochoa G, Flores-Mendoza LK, Icedo-Garcia R, Gomez-Flores R, Tamez-Guerra P (2017) Modulation of rotavirus severe gastroenteritis by the combination of probiotics and prebiotics. Arch Microbiol 199:953–961
Grandy G, Medina M, Soria R, Terán CG, Araya M (2010) Probiotics in the treatment of acute rotavirus diarrhoea. A randomized, double-blind, controlled trial using two different probiotic preparations in Bolivian children. BMC Infect Diseases 10:253
Grangette C, Müller-Alouf H, Hols P, Goudercourt D, Delcour J, Turneer M, Mercenier A (2004) Enhanced mucosal delivery of antigen with cell wall mutants of lactic acid bacteria. Infect Immun 72:2731–2737
Guandalini S, Pensabene L, Zikri MA, Dias JA, Casali LG, Hoekstra H, Kolacek S, Massar K, Micetic-Turk D, Papadopoulou A (2000) Lactobacillus GG administered in oral rehydration solution to children with acute diarrhea: a multicenter European trial. J Pediat Gastroenterol Nutr 30:54–60
Guerin-Danan C, Meslin J-C, Chambard A, Charpilienne A, Relano P, Bouley C, Cohen J, Andrieux C (2001) Food supplementation with milk fermented by Lactobacillus casei DN-114 001 protects suckling rats from rotavirus-associated diarrhea. J Nutr 131:111–117
Günaydın G, Zhang R, Hammarström L, Marcotte H (2014) Engineered Lactobacillus rhamnosus GG expressing IgG-binding domains of protein G: Capture of hyperimmune bovine colostrum antibodies and protection against diarrhea in a mouse pup rotavirus infection model. Vaccine 32:470–477
Hanniffy S, Wiedermann U, Repa A, Mercenier A, Daniel C, Fioramonti J, Tlaskolova H, Kozakova H, Israelsen H, Madsen S (2004) Potential and opportunities for use of recombinant lactic acid bacteria in human health. Adv Appl Microbiol 56:1–64
He B, Xu W, Santini PA, Polydorides AD, Chiu A, Estrella J, Shan M, Chadburn A, Villanacci V, Plebani A (2007) Intestinal bacteria trigger T cell-independent immunoglobulin A2 class switching by inducing epithelial-cell secretion of the cytokine APRIL. Immunity 26:812–826
Henriksen CM, Nilsson D, Hansen S, Johansen E (1999) Industrial applications of genetically modified microorganisms: gene technology at Chr Hansen A/S. Int Dairy J 9:17–23
Hilpert H, Briissow H, Mietens C, Sidoti J, Lerner L, Werchau H (1987) Use of bovine milk concentrate containing antibody to rotavirus to treat rotavirus gastroenteritis in infants. J Infect Dis 156:158–166
Hooper LV, Gordon JI (2001) Commensal host-bacterial relationships in the gut. Science 292:1115–1118
Isanaka S, Guindo O, Langendorf C, Matar Seck A, Plikaytis BD, Sayinzoga-Makombe N, McNeal MM, Meyer N, Adehossi E, Djibo A, Jochum B, Grais RF (2017) Efficacy of a Low-Cost, Heat-Stable Oral Rotavirus Vaccine in Niger. N Engl J Med 376:1121–1130
ISMAIL B (2017) The use of probiotics as vaccine vectors to prevent viral infections. New Insights on Antiviral Probiotics. Springer, pp 47–60. https://doi.org/10.1007/1978-1003-1319-49688-49687_49682
Jalilvand S, Marashi SM, Shoja Z (2015) Rotavirus VP6 preparations as a non-replicating vaccine candidates. Vaccine 33:3281–3287
Jiang B, Gentsch JR, Glass RI (2008) Inactivated rotavirus vaccines: a priority for accelerated vaccine development. Vaccine 26:6754–6758
Jiang B, Wang Y, Saluzzo J-F, Bargeron K, Frachette M-J, Glass RI (2008) Immunogenicity of a thermally inactivated rotavirus vaccine in mice. Human Vaccin 4:143–147
Kang JY, Lee DK, Ha NJ, Shin HS (2015) Antiviral effects of Lactobacillus ruminis SPM0211 and Bifidobacterium longum SPM1205 and SPM1206 on rotavirus-infected Caco-2 cells and a neonatal mouse model. J Microbiol 53:796–803
Kapikian AZ, Kim HW, Wyatt RG, Rodriguez WJ, Ross S, Cline WL, Parrott RH, Chanock RM (1974) Reoviruslike agent in stools: association with infantile diarrhea and development of serologic tests. Science 185:1049–1053
Kawahara T, Makizaki Y, Oikawa Y, Tanaka Y, Maeda A, Shimakawa M, Komoto S, Moriguchi K, Ohno H, Taniguchi K (2017) Oral administration of Bifidobacterium bifidum G9–1 alleviates rotavirus gastroenteritis through regulation of intestinal homeostasis by inducing mucosal protective factors. PloS One 12:e0173979
Koh A, De Vadder F, Kovatcheva-Datchary P, Bäckhed F (2016) From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 165:1332–1345
Koh A, Bäckhed F (2020) From Association to Causality: the Role of the Gut Microbiota and Its Functional Products on Host Metabolism. Molecular Cell 78:584–596
Kovatcheva-Datchary P, Shoaie S, Lee S, Wahlström A, Nookaew I, Hallen A, Perkins R, Nielsen J, Bäckhed F (2019) Simplified intestinal microbiota to study microbe-diet-host interactions in a mouse model. Cell Rep 26(3772–3783):e3776
Kumar M, Dhaka P, Vijay D, Vergis J, Mohan V, Kumar A, Kurkure NV, Barbuddhe SB, Malik S, Rawool DB (2016) Antimicrobial effects of Lactobacillus plantarum and Lactobacillus acidophilus against multidrug-resistant enteroaggregative Escherichia coli. Int J Antimicrob Agents 48:265–270
Kumar M, Ji B, Babaei P, Das P, Lappa D, Ramakrishnan G, Fox TE, Haque R, Petri WA, Bäckhed F (2018) Gut microbiota dysbiosis is associated with malnutrition and reduced plasma amino acid levels: lessons from genome-scale metabolic modeling. Metabol Eng 49:128–142
Land MH, Rouster-Stevens K, Woods CR, Cannon ML, Cnota J, Shetty AK (2005) Lactobacillus sepsis associated with probiotic therapy. Pediatrics 115:178–181
LeCureux JS, Dean GA (2018) Lactobacillus mucosal vaccine vectors: immune responses against bacterial and viral antigens. mSphere 3:e00061–00018
Lepault J, Petitpas I, Erk I, Navaza J, Bigot D, Dona M, Vachette P, Cohen J, Rey FA (2001) Structural polymorphism of the major capsid protein of rotavirus. EMBO J 20:1498–1507
Li Y-j, Ma G-p, Li G-w, Qiao X-y, Ge J-w, Tang L-j, Liu M, Liu L-w (2010) Oral vaccination with the porcine rotavirus VP4 outer capsid protein expressed by Lactococcus lactis induces specific antibody production. BioMed Res Int 2010:708460
Liévin-Le Moal V, Servin AL (2006) The front line of enteric host defense against unwelcome intrusion of harmful microorganisms: mucins, antimicrobial peptides, and microbiota. Clin Microbiol Rev 19:315–337
Mack DR, Michail S, Wei S, McDougall L, Hollingsworth MA (1999) Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. Am J Physiol Gastrointest Liver Physiol 276:G941–G950
Madhi SA, Cunliffe NA, Steele D, Witte D, Kirsten M, Louw C, Ngwira B, Victor JC, Gillard PH, Cheuvart BB, Han HH, Neuzil KM (2010) Effect of human rotavirus vaccine on severe diarrhea in African infants. N Engl J Med 362:289–298
Majamaa H, Isolauri E, Saxelin M, Vesikari T (1995) Lactic acid bacteria in the treatment of acute rotavirus gastroenteritis. J Pediatric Gastroenterol Nutr 20:333–338
Mäkivuokko H, Lahtinen SJ, Wacklin P, Tuovinen E, Tenkanen H, Nikkilä J, Björklund M, Aranko K, Ouwehand AC, Mättö J (2012) Association between the ABO blood group and the human intestinal microbiota composition. BMC Microbiol 12:94
Makki K, Deehan EC, Walter J, Bäckhed F (2018) The impact of dietary fiber on gut microbiota in host health and disease. Cell Host Microbe 23:705–715
Mao X, Gu C, Hu H, Tang J, Chen D, Yu B, He J, Yu J, Luo J, Tian G (2016) Dietary Lactobacillus rhamnosus GG supplementation improves the mucosal barrier function in the intestine of weaned piglets challenged by porcine rotavirus. PloS One 11:e0146312
Marashi SM, Jalilvand S, Mollaei-Kandelous Y, Shahmahmoodi S, Rezaei F, Salimi V, Nejati A, Validi M, Shoja Z (2014) Intra-peritoneal and intra-rectal immunogenicity induced by rotavirus virus like particles 2/6/7 in mice. Microb Pathogen 67–68:48–54
Marelli B, Perez AR, Banchio C, de Mendoza D, Magni C (2011) Oral immunization with live Lactococcus lactis expressing rotavirus VP8* subunit induces specific immune response in mice. J Virolog Methods 175:28–37
Massacand JC, Kaiser P, Ernst B, Tardivel A, Bürki K, Schneider P, Harris NL (2008) Intestinal bacteria condition dendritic cells to promote IgA production. PloS One 3:e2588
Medina E, Guzmán CA (2001) Use of live bacterial vaccine vectors for antigen delivery: potential and limitations. Vaccine 19:1573–1580
Muñoz JAM, Chenoll E, Casinos B, Bataller E, Ramón D, Genovés S, Montava R, Ribes JM, Buesa J, Fàbrega J (2011) Novel probiotic Bifidobacterium longum subsp. infantis CECT 7210 strain active against rotavirus infections. Appl Environm Microbiol 77:8775–8783
Nakamura Y, Terahara M, Iwamoto T, Yamada K, Asano M, Kakuta S, Iwakura Y, Totsuka M (2012) Upregulation of Polymeric Immunoglobulin Receptor Expression by the Heat-Inactivated Potential Probiotic Bifidobacterium bifidum OLB6378 in a Mouse Intestinal Explant Model. Scand J Immunol 75:176–183
Oberhelman RA, Gilman RH, Sheen P, Taylor DN, Black RE, Cabrera L, Lescano AG, Meza R, Madico G (1999) A placebo-controlled trial of Lactobacillus GG to prevent diarrhea in undernourished Peruvian children. J Pediatr 134:15–20
Olaya Galán N, Ulloa Rubiano J, Velez Reyes F, Fernandez Duarte K, Salas Cardenas S, Gutierrez Fernandez M (2016) In vitro antiviral activity of Lactobacillus casei and Bifidobacterium adolescentis against rotavirus infection monitored by NSP 4 protein production. J Appl Microbiol 120:1041–1051
Pant N, Hultberg A, Zhao Y, Svensson L, Pan-Hammarström Q, Johansen K, Pouwels PH, Ruggeri FM, Hermans P, Frenken L (2006) Lactobacilli expressing variable domain of llama heavy-chain antibody fragments (lactobodies) confer protection against rotavirus-induced diarrhea. J Infect Dis 194:1580–1588
Pant N, Marcotte H, Brüssow H, Svensson L, Hammarström L (2007) Effective prophylaxis against rotavirus diarrhea using a combination of Lactobacillus rhamnosus GG and antibodies. BMC Microbiol 7:1–9
Parez N (2008) Rotavirus gastroenteritis: why to back up the development of new vaccines? Compar Immunol Microbiol Infect Dis 31:253–269
Parker EP, Ramani S, Lopman BA, Church JA, Iturriza-Gomara M, Prendergast AJ, Grassly NC (2018) Causes of impaired oral vaccine efficacy in developing countries. Future Microbiol 13:97–118
Perez C, Eichwald C, Burrone O, De Mendoza D (2005) Rotavirus vp7 antigen produced by Lactococcus lactis induces neutralizing antibodies in mice. J Appl Microbiol 99:1158–1164
Plaza-Diaz J, Gomez-Llorente C, Fontana L, Gil A (2014) Modulation of immunity and inflammatory gene expression in the gut, in inflammatory diseases of the gut and in the liver by probiotics. World J Gastroenterol WJG 20:15632
Plaza-Diaz J, Ruiz-Ojeda FJ, Gil-Campos M, Gil A (2019) Mechanisms of action of probiotics. Adv Nutr 10:S49–S66
Pontes DS, De Azevedo MSP, Chatel J-M, Langella P, Azevedo V, Miyoshi A (2011) Lactococcus lactis as a live vector: heterologous protein production and DNA delivery systems. Prot Express Purif 79:165–175
Preidis GA, Saulnier DM, Blutt SE, Mistretta T-A, Riehle KP, Major AM, Venable SF, Barrish JP, Finegold MJ, Petrosino JF (2012) Host response to probiotics determined by nutritional status of rotavirus-infected neonatal mice. J Pediatr Gastroenterol Nutr 55:299
Qiao X, Li G, Wang X, Li X, Liu M, Li Y (2009) Recombinant porcine rotavirus VP4 and VP4-LTB expressed in Lactobacillus casei induced mucosal and systemic antibody responses in mice. BMC Microbiol 9:249
Rangan KJ, Hang HC (2017) Biochemical mechanisms of pathogen restriction by intestinal bacteria. Trends Biochem Sci 42:887–898
Ray P, Malik J, Singh RK, Bhatnagar S, Bahl R, Kumar R, Bhan MK (2003) Rotavirus nonstructural protein NSP4 induces heterotypic antibody responses during natural infection in children. J Infect Dis 187:1786–1793
Ringø E, Hoseinifar SH, Ghosh K, Doan HV, Beck BR, Song SK (2018) Lactic acid bacteria in finfish—An update. Front Microbiol 9:1818
Rodríguez-Díaz J, Montava R, Viana R, Buesa J, Pérez-Martínez G, Monedero V (2011) Oral immunization of mice with Lactococcus lactis expressing the rotavirus VP8* protein. Biotechnol Lett 33:1169–1175
Rosales-Mendoza S, Angulo C, Meza B (2016) Food-grade organisms as vaccine biofactories and oral delivery vehicles. Trends Biotechnol 34:124–136
Rottiers P, De Smedt T, Steidler L (2009) Modulation of gut-associated lymphoid tissue functions with genetically modified Lactococcus lactis. Int Rev Immunol 28:465–486
Ruggeri FM, Greenberg HB (1991) Antibodies to the trypsin cleavage peptide VP8 neutralize rotavirus by inhibiting binding of virions to target cells in culture. J Virol 65:2211–2219
Ruiz-Palacios GM, Perez-Schael I, Velazquez FR, Abate H, Breuer T, Clemens SC, Cheuvart B, Espinoza F, Gillard P, Innis BL, Cervantes Y, Linhares AC, Lopez P, Macias-Parra M, Ortega-Barria E, Richardson V, Rivera-Medina DM, Rivera L, Salinas B, Pavia-Ruz N, Salmeron J, Ruttimann R, Tinoco JC, Rubio P, Nunez E, Guerrero ML, Yarzabal JP, Damaso S, Tornieporth N, Saez-Llorens X, Vergara RF, Vesikari T, Bouckenooghe A, Clemens R, De Vos B, O’Ryan M, Human Rotavirus Vaccine Study G (2006) Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N Engl J Med 354:11–22
Salazar-Lindo E, Miranda-Langschwager P, Campos-Sanchez M, Chea-Woo E, Sack RB (2004) Lactobacillus caseistrain GG in the treatment of infants with acute watery diarrhea: A randomized, double-blind, placebo controlled clinical trial [ISRCTN67363048]. BMC Pediatr 4:18
Salminen MK, Rautelin H, Tynkkynen S, Poussa T, Saxelin M, Valtonen V, Järvinen A (2004) Lactobacillus bacteremia, clinical significance, and patient outcome, with special focus on probiotic L. rhamnosus GG. Clin Infect Dis 38:62–69
Sarker SA, Casswall TH, Mahalanabis D, Alam NH, Albert MJ, Brüssow H, Fuchs GJ, Hammerström L (1998) Successful treatment of rotavirus diarrhea in children with immunoglobulin from immunized bovine colostrum. Pediatr Infect Dis J 17:1149–1154
Serkedjieva J, Danova S, Ivanova I (2000) Antiinfluenza virus activity of a bacteriocin produced by Lactobacillus delbrueckii. Appl Biochem Biotechnol 88:285–298
Shoja Z, Tagliamonte M, Jalilvand S, Mollaei-Kandelous Y, De Stradis A, Tornesello ML, Buonaguro FM, Buonaguro L (2015) Formation of self-assembled triple-layered rotavirus-like particles (tlRLPs) by constitutive co-expression of VP2, VP6, and VP7 in stably transfected high-five insect cell lines. J Med Virol 87:102–111
Shornikova A-V, Casas IA, Isolauri E, Mykkänen H, Vesikari T (1997) Lactobacillus reuteri as a therapeutic agent in acute diarrhea in young children. J Pediatr Gastroenterol Nutr 24:399–404
Sindhu KN, Sowmyanarayanan TV, Paul A, Babji S, Ajjampur SS, Priyadarshini S, Sarkar R, Balasubramanian K, Wanke CA, Ward HD (2014) Immune response and intestinal permeability in children with acute gastroenteritis treated with Lactobacillus rhamnosus GG: a randomized, double-blind, placebo-controlled trial. Clin Infect Dis 58:1107–1115
Soares‐Weiser K, Bergman H, Henschke N, Pitan F, Cunliffe N (2019) Vaccines for preventing rotavirus diarrhoea: vaccines in use. Cochrane Database System Rev 2019:CD008521
Szajewska H, Mrukowicz JZ (2001) 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 33:S17–S25
Szatraj K, Szczepankowska AK, Chmielewska-Jeznach M (2017) Lactic acid bacteria—promising vaccine vectors: possibilities, limitations, doubts. J Appl Microbiol 123:325–339
Tate JE, Burton AH, Boschi-Pinto C, Steele AD, Duque J, Parashar UD, W-cGRS Network (2012) 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect Dis 12:136–141
Temprana CF, Arguelles MH, Gutierrez NM, Barril PA, Esteban LE, Silvestre D, Mandile MG, Glikmann G, Castello AA (2018) Rotavirus VP6 protein mucosally delivered by cell wall-derived particles from Lactococcus lactis induces protection against infection in a murine model. PloS One 13:e0203700
Temprana CF, Argüelles MH, Gutierrez NM, Barril PA, Esteban LE, Silvestre D, Mandile MG, Glikmann G, Castello AA (2018) Rotavirus VP6 protein mucosally delivered by cell wall-derived particles from Lactococcus lactis induces protection against infection in a murine model. PloS One 13:e0203700
Thompson A, Van Moorlehem E, Aich P (2010) Probiotic-induced priming of innate immunity to protect against rotaviral infection. Probiot Antimicrob Prot 2:90–97
Thouvenin E, Schoehn G, Rey F, Petitpas I, Mathieu M, Vaney M-C, Cohen J, Kohli E, Pothier P, Hewat E (2001) Antibody inhibition of the transcriptase activity of the rotavirus DLP: a structural view. J Mol Biol 307:161–172
Troeger C, Khalil IA, Rao PC, Cao S, Blacker BF, Ahmed T, Armah G, Bines JE, Brewer TG, Colombara DV, Kang G, Kirkpatrick BD, Kirkwood CD, Mwenda JM, Parashar UD, Petri WA Jr, Riddle MS, Steele AD, Thompson RL, Walson JL, Sanders JW, Mokdad AH, Murray CJL, Hay SI, Reiner RC Jr (2018) Rotavirus Vaccination and the Global Burden of Rotavirus Diarrhea Among Children Younger Than 5 Years. JAMA Pediatr 172:958–965
Van Zyl WF, Deane SM, Dicks LM (2020) Molecular insights into probiotic mechanisms of action employed against intestinal pathogenic bacteria. Gut Microbes 12:1831339
Vandenbroucke K, Hans W, Van Huysse J, Neirynck S, Demetter P, Remaut E, Rottiers P, Steidler L (2004) Active delivery of trefoil factors by genetically modified Lactococcus lactis prevents and heals acute colitis in mice. Gastroenterology 127:502–513
Vega CG, Bok M, Vlasova AN, Chattha KS, Gómez-Sebastián S, Nuñez C, Alvarado C, Lasa R, Escribano JM, Garaicoechea LL (2013) Recombinant monovalent llama-derived antibody fragments (VHH) to rotavirus VP6 protect neonatal gnotobiotic piglets against human rotavirus-induced diarrhea. PLoS Pathog 9:e1003334
Vesikari T, Clark HF, Offit PA, Dallas MJ, DiStefano DJ, Goveia MG, Ward RL, Schodel F, Karvonen A, Drummond JE, DiNubile MJ, Heaton PM (2006) Effects of the potency and composition of the multivalent human-bovine (WC3) reassortant rotavirus vaccine on efficacy, safety and immunogenicity in healthy infants. Vaccine 24:4821–4829
Vesikari T, Matson DO, Dennehy P, Van Damme P, Santosham M, Rodriguez Z, Dallas MJ, Heyse JF, Goveia MG, Black SB, Shinefield HR, Christie CD, Ylitalo S, Itzler RF, Coia ML, Onorato MT, Adeyi BA, Marshall GS, Gothefors L, Campens D, Karvonen A, Watt JP, O’Brien KL, DiNubile MJ, Clark HF, Boslego JW, Offit PA, Heaton PM, Rotavirus E, Safety Trial Study T (2006) Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N Engl J Med 354:23–33
Villena J, Aso H, Kitazawa H (2014) Regulation of toll-like receptors-mediated inflammation by immunobiotics in bovine intestinal epitheliocytes: role of signaling pathways and negative regulators. Front Immunol 5:421
Vincke C, Muyldermans S (2012) Introduction to heavy chain antibodies and derived Nanobodies. Single Domain Antibod 911:15–26
Vizzi E, Calvino E, Gonzalez R, Perez-Schael I, Ciarlet M, Kang G, Estes MK, Liprandi F, Ludert JE (2005) Evaluation of serum antibody responses against the rotavirus nonstructural protein NSP4 in children after rhesus rotavirus tetravalent vaccination or natural infection. Clin Diagn Labor Immunol 12:1157–1163
Vlasova AN, Kandasamy S, Chattha KS, Rajashekara G, Saif LJ (2016) Comparison of probiotic lactobacilli and bifidobacteria effects, immune responses and rotavirus vaccines and infection in different host species. Veterin Immunol Immunopathol 172:72–84
Vlasova AN, Takanashi S, Miyazaki A, Rajashekara G, Saif LJ (2019) How the gut microbiome regulates host immune responses to viral vaccines. Curr Opin Virol 37:16–25
Wachsman MB, López EM, Ramirez JA, Galagovsky LR, Coto CE (2000) Antiviral effect of brassinosteroids against herpes virus and arenaviruses. Antiviral Chem Chemotherapy 11:71–77
Wachsman MB, Castilla V, de Ruiz Holgado AP, de Torres RA, Sesma F, Coto CE (2003) Enterocin CRL35 inhibits late stages of HSV-1 and HSV-2 replication in vitro. Antiviral Res 58:17–24
Wang H, Gao K, Wen K, Allen IC, Li G, Zhang W, Kocher J, Yang X, Giri-Rachman E, Li G-H (2016) Lactobacillus rhamnosus GG modulates innate signaling pathway and cytokine responses to rotavirus vaccine in intestinal mononuclear cells of gnotobiotic pigs transplanted with human gut microbiota. BMC Microbiol 16:1–14
Wang Y, Azevedo M, Saif LJ, Gentsch JR, Glass RI, Jiang B (2010) Inactivated rotavirus vaccine induces protective immunity in gnotobiotic piglets. Vaccine 28:5432–5436
Ward RL, McNeal MM (2010) VP6: A candidate rotavirus vaccine. J Infect Dis 202:S101–S107
Wells JM, Mercenier A (2008) Mucosal delivery of therapeutic and prophylactic molecules using lactic acid bacteria. Nat Rev Microbiol 6:349–362
Wen K, Tin C, Wang H, Yang X, Li G, Giri-Rachman E, Kocher J, Bui T, Clark-Deener S, Yuan L (2014) Probiotic Lactobacillus rhamnosus GG enhanced Th1 cellular immunity but did not affect antibody responses in a human gut microbiota transplanted neonatal gnotobiotic pig model. PloS One 9:e94504
Wen K, Liu F, Li G, Bai M, Kocher J, Yang X, Wang H, Clark-Deener S, Yuan L (2015) Lactobacillus rhamnosus GG dosage affects the adjuvanticity and protection against rotavirus diarrhea in gnotobiotic pigs. J Pediatric Gastroenterol Nutr 60:834–843
Wyszyńska A, Kobierecka P, Bardowski J, Jagusztyn-Krynicka EK (2015) Lactic acid bacteria—20 years exploring their potential as live vectors for mucosal vaccination. Appl Microbiol Biotechnol 99:2967–2977
Yang Y, Pei J, Qin Z, Wei L (2019) Efficacy of probiotics to prevent and/or alleviate childhood rotavirus infections. J Funct Foods 52:90–99
Yasui H, Kiyoshima J, Ushijima H (1995) Passive protection against rotavirus-induced diarrhea of mouse pups born to and nursed by dams fed Bifidobacterium breve YIT4064. J Infect Dis 172:403–409
Yin J-Y, Guo C-Q, Wang Z, Yu M-L, Gao S, Bukhari SM, Tang L-J, Xu Y-G, Li Y-J (2016) Directed chromosomal integration and expression of porcine rotavirus outer capsid protein VP4 in Lactobacillus casei ATCC393. Appl Microbiol Biotechnol 100:9593–9604
Yu J, Langridge WH (2001) A plant-based multicomponent vaccine protects mice from enteric diseases. Nat Biotechnol 19:548–552
Zaman K, Dang DA, Victor JC, Shin S, Yunus M, Dallas MJ, Podder G, Vu DT, Le TP, Luby SP, Le HT, Coia ML, Lewis K, Rivers SB, Sack DA, Schodel F, Steele AD, Neuzil KM, Ciarlet M (2010) Efficacy of pentavalent rotavirus vaccine against severe rotavirus gastroenteritis in infants in developing countries in Asia: a randomised, double-blind, placebo-controlled trial. Lancet 376:615–623
Zhang Z, Xiang Y, Li N, Wang B, Ai H, Wang X, Huang L, Zheng Y (2013) Protective effects of Lactobacillus rhamnosus GG against human rotavirus-induced diarrhoea in a neonatal mouse model. Pathog Dis 67:184–191
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The present study was funded and supported by Pasteur Institute of Iran (Grant no. 881).
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Afchangi, A., Latifi, T., Jalilvand, S. et al. Combined use of lactic-acid-producing bacteria as probiotics and rotavirus vaccine candidates expressing virus-specific proteins. Arch Virol 166, 995–1006 (2021). https://doi.org/10.1007/s00705-021-04964-9
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DOI: https://doi.org/10.1007/s00705-021-04964-9