4,450
Views
19
CrossRef citations to date
0
Altmetric
Research Paper

A bovine lactoferricin-lactoferrampin-encoding Lactobacillus reuteri CO21 regulates the intestinal mucosal immunity and enhances the protection of piglets against enterotoxigenic Escherichia coli K88 challenge

ORCID Icon, , ORCID Icon, ORCID Icon, , , , , , , , , , , , , & ORCID Icon show all
Article: 1956281 | Received 31 Oct 2020, Accepted 02 Jul 2021, Published online: 07 Aug 2021

References

  • Clarke SC. Diarrhoeagenic Escherichia coli–an emerging problem?. Diagn Microbiol Infect Dis. 2001;41(3):93–23. doi:10.1016/s0732-8893(01)00303-0. PMID: 11750160.
  • Ratchtrachenchai OA, Subpasu S, Hayashi H, Ba-Thein W. Prevalence of childhood diarrhoea-associated Escherichia coli in Thailand. J Med Microbiol. 2004;53(Pt3):237–243. doi:10.1099/jmm.0.05413-0. PMID: 14970250.
  • Morelli L. Postnatal development of intestinal microflora as influenced by infant nutrition. J Nutr. 2008;138(9):1791S–1795S. doi:10.1093/jn/138.9.1791S. PMID: WOS: 000258802000035.
  • Gan Z, Wei W, Li Y, Wu J, Zhao Y, Zhang L, Wang T, Zhong X. Curcumin and resveratrol regulate intestinal bacteria and alleviate intestinal inflammation in weaned piglets. Molecules. 2019;24(12207). doi:10.3390/molecules24071220. PMID: WOS: 000464954700002.
  • Liu C, Zhu Q, Chang J, Yin Q, Song A, Li Z, Wang E, Lu F. Effects of lactobacillus casei and enterococcus faecalis on growth performance, immune function and gut microbiota of suckling piglets. Arch Anim Nutr. 2017;71(2):120–133. doi:10.1080/1745039X.2017.1283824. PMID: 28201936.
  • DLA DM, Del CS, Chatel JM, Azevedo V, Langella P, Bermudez-Humaran L, LeBlanc JG. Evaluation of the biosafety of recombinant lactic acid bacteria designed to prevent and treat colitis. J Med Microbiol. 2016;65(9):1038–1046. doi:10.1099/jmm.0.000323. PMID: 27469354.
  • Martin R, Chain F, Miquel S, Natividad JM, Sokol H, Verdu EF, Langella P, Bermudez-Humaran LG. Effects in the use of a genetically engineered strain of Lactococcus lactis delivering in situ IL-10 as a therapy to treat low-grade colon inflammation. Hum Vaccin Immunother. 2014;10(6):1611–1621. doi:10.4161/hv.28549. PMID: 24732667.
  • Kuczkowska K, Kleiveland CR, Minic R, Moen LF, Overland L, Tjaland R, Carlsen H, Lea T, Mathiesen G, Eijsink V. Immunogenic properties of lactobacillus plantarum producing surface-displayed mycobacterium tuberculosis antigens. Appl Environ Microbiol. 2017;83(2). doi:10.1128/AEM.02782-16. PMID: 27815271.
  • Yi H, Hu W, Chen S, Lu Z, Wang Y. Cathelicidin-WA improves intestinal epithelial barrier function and enhances host defense against enterohemorrhagic Escherichia coli O157: h7Infection. J Immunol. 2017;198(4):1696–1705. doi:10.4049/jimmunol.1601221. PMID: 28062699.
  • Sinha M, Kaushik S, Kaur P, Sharma S, Singh TP. Antimicrobial lactoferrin peptides: the hidden players in the protective function of a multifunctional protein. Int J Pept. 2013;2013:390230. doi:10.1155/2013/390230. PMID: 23554820.
  • Flores-Villasenor H, Canizalez-Roman A, Reyes-Lopez M, Nazmi K, De La Garza M, Zazueta-Beltran J, Leon-Sicairos N, Bolscher JG. Bactericidal effect of bovine lactoferrin, LFcin, LFampin and LFchimera on antibiotic-resistant staphylococcus aureus and Escherichia coli. Biometals. 2010;23(3):569–578. doi:10.1007/s10534-010-9306-4. PMID: 20195887.
  • Bolscher JG, Adao R, Nazmi K, Van Den Keybus PA, van THW, Nieuw AA, Bastos M, Veerman EC. Bactericidal activity of LFchimera is stronger and less sensitive to ionic strength than its constituent lactoferricin and lactoferrampin peptides. Biochimie. 2009;91(1):123–132. doi:10.1016/j.biochi.2008.05.019. PMID: 18573310.
  • Ruangcharoen S, Suwannarong W, Lachica M, Bolscher J, Nazmi K, Khunkitti W, Taweechaisupapong S. Killing activity of LFchimera on periodontopathic bacteria and multispecies oral biofilm formation in vitro. World J Microbiol Biotechnol. 2017;33(9):167. doi:10.1007/s11274-017-2334-2. PMID: 28823045.
  • Tang Z, Yin Y, Zhang Y, Huang R, Sun Z, Li T, Chu W, Kong X, Li L, Geng M. Effects of dietary supplementation with an expressed fusion peptide bovine lactoferricin-lactoferrampin on performance, immune function and intestinal mucosal morphology in piglets weaned at age 21 d. Br J Nutr. 2009;101(7):998–1005. doi:10.1017/S0007114508055633. PMID: 18840311.
  • Zhang L, Guo D, Liu Y, Shao Y, Wang Y, Xu Y, Jiang Y, Cui W, Li Y, Tang L. Probiotic lactobacillus casei expressing porcine antimicrobial peptide PR39 elevates antibacterial activity in the gastrointestinal tract. Can J Microbiol. 2016;62(11):961–969. doi:10.1139/cjm-2016-0130. PMID: 27718591.
  • Wong CC, Zhang L, Wu WK, Shen J, Chan RL, Lu L, Hu W, Li MX, Li LF, Ren SX. Cathelicidin-encoding Lactococcus lactis promotes mucosal repair in murine experimental colitis. J Gastroenterol Hepatol. 2017;32(3):609–619. doi:10.1111/jgh.13499. PMID: 27470075.
  • Wong CC, Zhang L, Li ZJ, Wu WK, Ren SX, Chen YC, Ng TB, Cho CH. Protective effects of cathelicidin-encoding Lactococcus lactis in murine ulcerative colitis. J Gastroenterol Hepatol. 2012;27(7):1205–1212. doi:10.1111/j.1440-1746.2012.07158.x. PMID: 22507188.
  • Dierick M, Van der Weken H, Rybarczyk J, Vanrompay D, Devriendt B, Cox E. Porcine and bovine forms of lactoferrin inhibit growth of porcine enterotoxigenic Escherichia coli and degrade its virulence factors. Appl Environ Microb. 2020;86(24). doi:10.1128/AEM.00524-20. PMID: 32631861.
  • Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, Van Den Brandt PA, Stobberingh EE. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118(2):511–521. doi:10.1542/peds.2005-2824. PMID: 16882802.
  • Kararli TT. Comparison of the gastrointestinal anatomy, physiology, and biochemistry of humans and commonly used laboratory animals. Biopharm Drug Dispos. 1995;16(5):351–380. doi:10.1002/bdd.2510160502. PMID: 8527686.
  • Miller ER, Ullrey DE. The pig as a model for human nutrition. Annu Rev Nutr. 1987;7(1):361–382. doi:10.1146/annurev.nu.07.070187.002045. PMID: 3300739.
  • Moughan PJ, Birtles MJ, Cranwell PD, Smith WC, Pedraza M. The piglet as a model animal for studying aspects of digestion and absorption in milk-fed human infants. World Rev Nutr Diet. 1992;67:40–113. doi:10.1159/000419461. PMID: 1557912.
  • Zhang Q, Widmer G, Tzipori S. A pig model of the human gastrointestinal tract. Gut Microbes. 2013;4(3):193–200. doi:10.4161/gmic.23867. PMID: 23549377.
  • Roos S, Karner F, Axelsson L, Jonsson H. Lactobacillus mucosae sp. nov., a new species with in vitro mucus-binding activity isolated from pig intestine. Int J Syst Evol Microbiol. 2000;50(Pt 1):251–258. doi:10.1099/00207713-50-1-251. PMID: 10826811.
  • Lee KW, Shim JM, Park S, Heo H, Kim H, Ham K, Kim JH. Isolation of lactic acid bacteria with probiotic potentials from kimchi, traditional Korean fermented vegetable. Lwt-Food Sci Technol. 2016;71:130–137. doi:10.1016/j.lwt.2016.03.029. PMID: WOS: 000376800100018.
  • Wang P, Li Y, Xiao H, Shi Y, Le GW, Sun J. Isolation of lactobacillus reuteri from peyer’s patches and their effects on sIgA production and gut microbiota diversity. Mol Nutr Food Res. 2016;60(9):2020–2030. doi:10.1002/mnfr.201501065. PMID: 27030202.
  • Liu DQ, Ge JW, Qiao XY, Jiang YP, Liu SM, Li YJ. High-level mucosal and systemic immune responses induced by oral administration with lactobacillus-expressed porcine epidemic diarrhea virus (PEDV) S1 region combined with lactobacillus-expressed N protein. Appl Microbiol Biotechnol. 2012;93(6):2437–2446. doi:10.1007/s00253-011-3734-0. PMID: 22134641.
  • Nandakumar MP, Shen J, Raman B, Marten MR. Solubilization of trichloroacetic acid (TCA) precipitated microbial proteins via naOH for two-dimensional electrophoresis. J Proteome Res. 2003;2(1):89–93. doi:10.1021/pr025541x. PMID: 12643547.
  • Zhou H, Li X, Wang Z, Yin J, Tan H, Wang L, Qiao X, Jiang Y, Cui W, Liu M. Construction and characterization of thymidine auxotrophic (deltathyA) recombinant lactobacillus casei expressing bovine lactoferricin. Bmc Vet Res. 2018;14(1):206. doi:10.1186/s12917-018-1516-y. PMID: 29945678.
  • Comstock SS, Reznikov EA, Contractor N, Donovan SM. Dietary bovine lactoferrin alters mucosal and systemic immune cell responses in neonatal piglets. J Nutr. 2014;144(4):525–532. doi:10.3945/jn.113.190264. PMID: 24553692.
  • Song L, Qiao X, Zhao D, Xie W, Bukhari SM, Meng Q, Wang L, Cui W, Jiang Y, Zhou H. Effects of Lactococcus lactis MG1363 producing fusion proteins of bovine lactoferricin-lactoferrampin on growth, intestinal morphology and immune function in weaned piglet. J Appl Microbiol. 2019;127(3):856–866. doi:10.1111/jam.14339. PMID: 31161702.
  • Hu J, Chen L, Zheng W, Shi M, Liu L, Xie C, Wang X, Niu Y, Hou Q, Xu X. Lactobacillus frumenti facilitates intestinal epithelial barrier function maintenance in early-weaned piglets. Front Microbiol. 2018;9:897. doi:10.3389/fmicb.2018.00897. PMID: 29867808.
  • Hu J, Nie Y, Chen J, Zhang Y, Wang Z, Fan Q, Yan X. Gradual changes of gut microbiota in weaned miniature piglets. Front Microbiol. 2016;7:1727. doi:10.3389/fmicb.2016.01727. PMID: 27853453.
  • Ren Y, Geng Y, Du Y, Li W, Lu ZM, Xu HY, Xu GH, Shi JS, Xu ZH. Polysaccharide of Hericium erinaceus attenuates colitis in C57BL/6 mice via regulation of oxidative stress, inflammation-related signaling pathways and modulating the composition of the gut microbiota. J Nutr Biochem. 2018;57:67–76. doi:10.1016/j.jnutbio.2018.03.005. PMID: 29677563.
  • Gao K, Wang C, Liu L, Dou X, Liu J, Yuan L, Zhang W, Wang H. Immunomodulation and signaling mechanism of lactobacillus rhamnosus GG and its components on porcine intestinal epithelial cells stimulated by lipopolysaccharide. J Microbiol Immunol Infect. 2017;50(5):700–713. doi:10.1016/j.jmii.2015.05.002. PMID: 26055689.
  • Lapthorne S, Pereira-Fantini PM, Fouhy F, Wilson G, Thomas SL, Dellios NL, Scurr M, O’Sullivan O, Ross RP, Stanton C. Gut microbial diversity is reduced and is associated with colonic inflammation in a piglet model of short bowel syndrome. Gut Microbes. 2013;4(3):212–221. doi:10.4161/gmic.24372. PMID: 23549027.
  • Kandasamy S, Chattha KS, Vlasova AN, Rajashekara G, Saif LJ. Lactobacilli and bifidobacteria enhance mucosal B cell responses and differentially modulate systemic antibody responses to an oral human rotavirus vaccine in a neonatal gnotobiotic pig disease model. Gut Microbes. 2014;5(5):639–651. doi:10.4161/19490976.2014.969972. PMID: 25483333.
  • Andrutis KA, Riggle PJ, Kumamoto CA, Tzipori S. Intestinal lesions associated with disseminated candidiasis in an experimental animal model. J Clin Microbiol. 2000;38(6):2317–2323. doi:10.1128/JCM.38.6.2317-2323.2000. PMID: 10834995.
  • Steele J, Feng H, Parry N, Tzipori S. Piglet models of acute or chronic clostridium difficile illness. J Infect Dis. 2010;201(3):428–434. doi:10.1086/649799. PMID: 20039803.
  • Brady MJ, Radhakrishnan P, Liu H, Magoun L, Murphy KC, Mukherjee J, Donohue-Rolfe A, Tzipori S, Leong JM. Enhanced actin pedestal formation by enterohemorrhagic Escherichia coli O157: h7Adapted to the mammalian host. Front Microbiol. 2011;2:226. doi:10.3389/fmicb.2011.00226. PMID: 22102844.
  • Jeong KI, Zhang Q, Nunnari J, Tzipori S. A piglet model of acute gastroenteritis induced by shigella dysenteriae type 1. J Infect Dis. 2010;201(6):903–911. doi:10.1086/650995. PMID: 20136414.
  • Meurens F, Summerfield A, Nauwynck H, Saif L, Gerdts V. The pig: a model for human infectious diseases. Trends Microbiol. 2012;20(1):50–57. doi:10.1016/j.tim.2011.11.002. PMID: 22153753.
  • Song L, Xie W, Liu Z, Guo D, Zhao D, Qiao X, Wang L, Zhou H, Cui W, Jiang Y. Oral delivery of a Lactococcus lactis strain secreting bovine lactoferricin-lactoferrampin alleviates the development of acute colitis in mice. Appl Microbiol Biotechnol. 2019;103(15):6169–6186. doi:10.1007/s00253-019-09898-6. PMID: 31165225.
  • Mu Q, Tavella VJ, Luo XM. Role of lactobacillus reuteri in human health and diseases. Front Microbiol. 2018;9:757. doi:10.3389/fmicb.2018.00757. PMID: 29725324.
  • Wang H, Zhou C, Huang J, Kuai X, Shao X. The potential therapeutic role of lactobacillus reuteri for treatment of inflammatory bowel disease. Am J Transl Res. 2020;12(5):1569–1583. PMID: 32509162.
  • Hou C, Zeng X, Yang F, Liu H, Qiao S. Study and use of the probiotic lactobacillus reuteri in pigs: a review. J Anim Sci Biotechnol. 2015;6(1):14. doi:10.1186/s40104-015-0014-3. PMID: 25954504.
  • Angmo K, Kumari A, Savitri BTC. Probiotic characterization of lactic acid bacteria isolated from fermented foods and beverage of Ladakh. Lwt-Food Sci Technol. 2016;66:428–435. doi:10.1016/j.lwt.2015.10.057. PMID: WOS: 000367413200059.
  • Wang J, Tian S, Yu H, Wang J, Zhu W. Response of colonic mucosa-associated microbiota composition, mucosal immune homeostasis, and barrier function to early life galactooligosaccharides intervention in suckling piglets. J Agric Food Chem. 2019;67(2):578–588. doi:10.1021/acs.jafc.8b05679. PMID: 30562014.
  • Zhu J, Gao M, Zhang R, Sun Z, Wang C, Yang F, Huang T, Qu S, Zhao L, Li Y. Effects of soybean meal fermented by L. plantarum, B. subtilis and S. cerevisieae on growth, immune function and intestinal morphology in weaned piglets. Microb Cell Fact. 2017;16(1):191. doi:10.1186/s12934-017-0809-3. PMID: 29121938.
  • Wang W, Chen J, Zhou H, Wang L, Ding S, Wang Y, Song D, Li A. Effects of microencapsulated lactobacillus plantarum and fructooligosaccharide on growth performance, blood immune parameters, and intestinal morphology in weaned piglets. Food Agr Immunol. 2018;29(1):84–94. doi:10.1080/09540105.2017.1360254. PMID: WOS: 000434711200002.
  • Negretti NM, Ye Y, Malavasi LM, Pokharel SM, Huynh S, Noh S, Klima CL, Gourley CR, Ragle CA, Bose S. A porcine ligated loop model reveals new insight into the host immune response against campylobacter jejuni. Gut Microbes. 2020;12(1):1–25. doi:10.1080/19490976.2020.1814121. PMID: 32887530.
  • Yu HT, Ding XL, Li N, Zhang XY, Zeng XF, Wang S, Liu HB, Wang YM, Jia HM, Qiao SY. Dietary supplemented antimicrobial peptide microcin J25 improves the growth performance, apparent total tract digestibility, fecal microbiota, and intestinal barrier function of weaned pigs. J Anim Sci. 2017;95(11):5064–5076. doi:10.2527/jas2017.1494. PMID: 29293710.
  • Yi H, Wang L, Xiong Y, Wang Z, Qiu Y, Wen X, Jiang Z, Yang X, Ma X. Lactobacillus reuteri LR1 improved expression of genes of tight junction Proteins via the MLCK pathway in IPEC-1 cells during infection with enterotoxigenic Escherichia coli K88. Mediators Inflamm. 2018;2018:6434910. doi:10.1155/2018/6434910. PMID: 30210262.
  • Zhao L, Luo L, Jia W, Xiao J, Huang G, Tian G, Li J, Xiao Y. Serum diamine oxidase as a hemorrhagic shock biomarker in a rabbit model. PLoS One. 2014;9(8):e102285. doi:10.1371/journal.pone.0102285. PMID: 25144315.
  • Smith F, Clark JE, Overman BL, Tozel CC, Huang JH, Rivier JE, Blikslager AT, Moeser AJ. Early weaning stress impairs development of mucosal barrier function in the porcine intestine. Am J Physiol Gastrointest Liver Physiol. 2010;298(3):G352–63. doi:10.1152/ajpgi.00081.2009. PMID: 19926814.
  • Hu L, Geng S, Li Y, Cheng S, Fu X, Yue X, Han X. Exogenous fecal microbiota transplantation from local adult pigs to crossbred newborn piglets. Front Microbiol. 2017;8:2663. doi:10.3389/fmicb.2017.02663. PMID: 29375527.
  • Li HH, Li YP, Zhu Q, Qiao JY, Wang WJ. Dietary supplementation with clostridium butyricum helps to improve the intestinal barrier function of weaned piglets challenged with enterotoxigenic Escherichia coli K88. J Appl Microbiol. 2018;125(4):964–975. doi:10.1111/jam.13936. PMID: 29851202.
  • Tsai PY, Zhang B, He WQ, Zha JM, Odenwald MA, Singh G, Tamura A, Shen L, Sailer A, Yeruva S. IL-22 upregulates epithelial claudin-2 to drive diarrhea and enteric pathogen clearance. Cell Host Microbe. 2017;21(6):671–681. PMID: 28618266. doi:10.1016/j.chom.2017.05.009. e4.
  • Nighot M, Al-Sadi R, Guo S, Rawat M, Nighot P, Watterson MD, Ma TY. Lipopolysaccharide-induced increase in intestinal epithelial tight permeability is mediated by toll-like receptor 4/myeloid differentiation primary response 88 (myD88) activation of myosin light chain kinase expression. Am J Pathol. 2017;187(12):2698–2710. doi:10.1016/j.ajpath.2017.08.005. PMID: 29157665.
  • Xu C, Guo Y, Qiao L, Ma L, Cheng Y, Roman A. Biogenic synthesis of novel functionalized Selenium nanoparticles by lactobacillus casei ATCC 393 and its protective effects on intestinal barrier dysfunction caused by enterotoxigenic Escherichia coli K88. Front Microbiol. 2018;9:1129. doi:10.3389/fmicb.2018.01129. PMID: 29967593.
  • Dianat M, Radan M, Badavi M, Mard SA, Bayati V, Ahmadizadeh M. Crocin attenuates cigarette smoke-induced lung injury and cardiac dysfunction by anti-oxidative effects: the role of Nrf2 antioxidant system in preventing oxidative stress. Respir Res. 2018;19(1):58. doi:10.1186/s12931-018-0766-3. PMID: 29631592.
  • Li T, Chen B, Du M, Song J, Cheng X, Wang X, Mao X. Casein glycomacropeptide hydrolysates exert cytoprotective effect against cellular oxidative stress by up-regulating HO-1 expression in HepG2 cells. Nutrients. 2017;9(1). doi:10.3390/nu9010031. PMID: 28098837.
  • Scott CL, Aumeunier AM, Mowat AM. Intestinal CD103+ dendritic cells: master regulators of tolerance?. Trends Immunol. 2011;32(9):412–419. doi:10.1016/j.it.2011.06.003. PMID: 21816673.
  • Thaiss CA, Semmling V, Franken L, Wagner H, Kurts C. Chemokines: a new dendritic cell signal for T cell activation. Front Immunol. 2011;2:31. doi:10.3389/fimmu.2011.00031. PMID: 22566821.
  • Song HY, Sik KW, Kim JM, Bak DH, Moo HJ, Lim ST, Byun EB. A hydroxyethyl derivative of chrysin exhibits anti-inflammatory activity in dendritic cells and protective effects against dextran sodium salt-induced colitis in mice. Int Immunopharmacol. 2019;77:105958. doi:10.1016/j.intimp.2019.105958. PMID: 31639615.
  • Lalor R, Bovine OS. κ-casein induces a hypo-responsive DC population which exhibit a reduced capacity to elicit T-cell responses. J Funct Foods. 2020;64:103620. doi:10.1016/j.jff.2019.103620.
  • Wang H, Chao K, Ng SC, Bai AH, Yu Q, Yu J, Li M, Cui Y, Chen M, Hu JF. Pro-inflammatory miR-223 mediates the cross-talk between the IL23 pathway and the intestinal barrier in inflammatory bowel disease. Genome Biol. 2016;17:58. doi:10.1186/s13059-016-0901-8. PMID: 27029486.
  • Chen J, Yu B, Chen D, Huang Z, Mao X, Zheng P, Yu J, Luo J, He J. Chlorogenic acid improves intestinal barrier functions by suppressing mucosa inflammation and improving antioxidant capacity in weaned pigs. J Nutr Biochem. 2018;59:84–92. doi:10.1016/j.jnutbio.2018.06.005. PMID: 29986311.
  • Wu Y, Zhu C, Chen Z, Chen Z, Zhang W, Ma X, Wang L, Yang X, Jiang Z. Protective effects of lactobacillus plantarum on epithelial barrier disruption caused by enterotoxigenic Escherichia coli in intestinal porcine epithelial cells. Vet Immunol Immunop. 2016;172:55–63. doi:10.1016/j.vetimm.2016.03.005. PMID: 27032504.
  • Dong N, Li X, Xue C, Zhang L, Wang C, Xu X, Shan A. Astragalus polysaccharides alleviates LPS-induced inflammation via the NF-kappaB/MAPK signaling pathway. J Cell Physiol. 2020;235(7–8):5525–5540. doi:10.1002/jcp.29452. PMID: 32037545.