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The immune-genes regulation mediated mechanisms of probiotics to control salmonella infection in chicken

Published online by Cambridge University Press:  15 June 2017

M. ROYAN
M. ROYAN*
Affiliation:
North Region Branch, Agricultural Biotechnology Research Institute of Iran (ABRII), Agricultural Research, Education and Extension Organization (AREEO), Rasht, Iran
*
Corresponding author: m.royan@abrii.ac.ir

Abstract

Probiotics are live microorganisms with confirmed beneficial effects on poultry health, growth performance, immune system and gut microbial population. A better perception of the mechanisms underlying the immunomodulatory effects of probiotic bacteria is usually needed to give a superior direction to the development and administration of probiotics. The oral administration of probiotic bacteria influence host cytokine levels and therefore, alters both innate and adaptive host immune responses. Selected probiotics, including some lactobacillus isolates and enterococcal strains, have been considered to prevent salmonella colonisation. Part of the effect of probiotic bacteria may be mediated through changes in the immune system related genes, including cytokine expression. Administration of probiotics in chickens could moderate salmonella mediated changes in genes, including encoding pro-inflammatory cytokines, T helper (Th) 1 cytokines, and Th2 cytokines. This review summarises the findings on the mechanisms of salmonella inhibition by using probiotic bacteria at the molecular level.

Keywords

probioticssalmonellaimmune related geneschicken

Information

Type
Reviews
Information
World's Poultry Science Journal , Volume 73 , Issue 3 , September 2017 , pp. 603 - 610
Copyright
Copyright © World's Poultry Science Association 2017 

Introduction

The intestine, especially the ileum and caecum, are the main sites for the entry and colonisation of orally ingested pathogens in chickens, and altering the gut microbial population by probiotic bacteria supplementation could decrease pathogen load in the bird's gastrointestinal tract (Barrow et al., Reference BARROW, LOVELL and SIMPSON1988; Mead, Reference MEAD2000). Probiotics are live microorganisms which when fed at adequate levels, may improve the health status and performance of poultry through enhancements in immune response, manipulation of gut microflora and pathogen inhibition, histological alterations in small intestine tissue and changes in blood biochemical parameters (Gill and Prasad, Reference GILL and PRASAD2008; Noujaim et al., Reference NOUJAIM, ANDREATTI FILHO, LIMA, OKAMOTO, AMORIM and TORRES NETO2008; Kabir, Reference KABIR2009; Deriu et al., Reference DERIU, LIU, PEEZESHKI, EDWARDS, OCHOA, CONTRERAS, LIBBY, FANG and RAFFATELLU2013).

Different mechanisms may be involved in the effects of probiotic on the host's health. The effects of probiotic bacteria on the immune response, may be because of the stimulation of antibody production, activation of T cells and alterations in cytokine expression profiles (De Simone et al., Reference DE SIMONE, VESELY, BIANCHI-SALVADORI and JIRILLO1993; Christensen et al., Reference CHRISTENSEN, FROKIAER and PESTKA2002; Chen et al., Reference CHEN, LOUIE, SHI and WALKER2005; O'Hara et al., Reference O'HARA, O'REGAN, FANNING, O'MAHONY, MADSHARRY, LYONS, BIENENSTOCK, O'MAHONY and SHANAHAN2006; Haghighi et al., Reference HAGHIGHI, ABDUL-CAREEM, DARA, CHAMBERS and SHARIF2008), and consequently, changes in both innate and adaptive host immune responses (Dugas et al., Reference DUGAS, MERCENIER, LENOIR-WIJNKOOP, ARNAUD, DUGAS and POSTAIRE1999; Olivares et al., Reference OLIVARES, DIAZ-ROPERO, GOMEZ, LARA-VILLOSLADA, SIERRA, MALDONADO, MARTIN, RODRIGUEZ and XAUS2006). Haghighi et al. (Reference HAGHIGHI, ABDUL-CAREEM, DARA, CHAMBERS and SHARIF2008) suggested that some of the immunomodulatory properties of probiotics could attribute to the stimulation of IL-10 cytokine expression by chicken's gut-associated lymphoid tissue cells. Peroxisome proliferator-activated receptor gamma (PPARγ), a transcription factor from nuclear hormone receptor family, inhibits inflammatory cytokine expression (Wächtershäuser et al., Reference WÄCHTERSHÄUSER, LOITSCH and STEIN2000), and there are reports on the dietary manipulation effects on PPARγ gene expression (Royan et al., Reference ROYAN, MENG, OTHMAN, SAZILI and NAVIDSHAD2011), and this pathway may activate through probiotics, although this needs further research.

In a more recent study, Varmuzova et al. (Reference VARMUZOVA, KUBASOVA, DAVIDOVA-GERZOVA, SISAK, HAVLICKOVA, SEBKOVA, FALDYNOVA and RYCHLIK2016) demonstrated that transferring microbiota from three week old chickens to day-old chick's gastrointestinal tract stimulated the expression of cytokines such as IL1β, IL8, IL17, IL22, and IL18 and the microbial population from 42-week-old donors increased the expression of IL16, NK-lysin (NKL), IgY and IgA. On the other hand, some probiotic bacteria strains, such as Enterococcus faecium AL41, are able to produce enterocin M with inhibitory effects on the pathogenic bacteria (Lauková et al., Reference LAUKOVÁ, MAREK and STYRIAK2003; Mareková et al., Reference MAREKOVÁ, LAUKOVÁ, SKAUGEN and NES2007). The present review summarises the findings on the mechanisms of salmonella inhibition by using probiotic bacteria at the molecular level.

Salmonella infections in chicken

Wigley (Reference WIGLEY2014) comprehensively reviewed the salmonellosis-mediated changes in the chicken's body. The salmonella serovars are the cause of fowl typhoid and pullorum disease in chicken (Barrow and Freitas, 2011). The infection biology of avian salmonella is varied, although common broad-host range Salmonella enterica serovars infect the chicken through the colonisation of the lower gastrointestinal tract. In some serovars, particularly Salmonella typhimurium and S. enteritidis, this may be demonstrated as a weak systemic disease which is alleviated by cellular immunity within two to three weeks (Barrow et al., Reference BARROW, BUMSTEAD, MARSTON, LOVELL and WIGLEY2004; Beal et al., Reference BEAL, POWERS, WIGLEY, BARROW and SMITH2004). The colonisation of these serovars usually promotes inflammatory responses in the ileum and caeca (Withanage et al., Reference WITHANAGE, WIGLEY, KAISER, MASTROENI, BROOKS, POWERS, BEAL, BARROW, MASKELL and McCONNELL2005; Setta et al., Reference SETTA, BARROW, KAISER and JONES2012).

Salmonella gallinarum and S. pullorum serovars lead to high mortality through a systemic infection (Wigley et al., Reference WIGLEY, HULME, POWERS, BEAL, SMITH and BARROW2005) and dissimilar to the broad-host range serovars, the infection doesn't lead to inflammation (Henderson et al., Reference HENDERSON, BOUNOUS and LEE1999; Chappell et al., Reference CHAPPELL, KAISER, BARROW, JONES, JOHNSTON and WIGLEY2009; Setta et al., Reference SETTA, BARROW, KAISER and JONES2012).

The effects of salmonella infection on gene expression in poultry

Some studies have demonstrated that salmonellosis causes a strong Th1 response and that this, along with clearance in the chicken, is dependent on age and cellular development. Salmonella infection results in an increase of γδ lymphocytes and upregulation of IFN-γ, IL-12, and IL-18, leading to activation of the TH1 response (Berndt and Methner, Reference BERNDT and METHNER2001; Berndt et al., Reference BERNDT, PIEPER and METHNER2006).

There are reports that indicate salmonella infection in birds leads to the expression of proinflammatory cytokines and the chemokines CXCLi1 and CXCLi2, which are considered the counterpart of mammalian IL-8 (Withanage et al., Reference WITHANAGE, KAISER, WIGLEY, POWERS, MASTROENI, BROOKS, BARROW, SMITH, MASKELL and McCONNELL2004; Reference WITHANAGE, WIGLEY, KAISER, MASTROENI, BROOKS, POWERS, BEAL, BARROW, MASKELL and McCONNELL2005; Setta et al., Reference SETTA, BARROW, KAISER and JONES2012; Matulova et al., Reference MATULOVA, VARMUZOVA, SISAK, HAVLICKOVA, BABAK, STEJSKAL, ZDRAHAL and RYCHLIK2013). This results in an increased number of heterophils and monocytic phagocytes in the gut, which cause inflammation and damage to the villi. Mariani et al. (Reference MARIANI, BARROW, CHENG, GROENEN, NEGRINI and BUMSTEAD2001) identified the genetic locus SAL1 in chickens that shows a phenotype of resistance to systemic salmonella infection, whereby the derived macrophages show more rapid expression of key inflammatory and TH1-associated cytokines (Wigley et al., Reference WIGLEY, HULME, BUMSTEAD and BARROW2002; Reference WIGLEY, HULME, ROTHWELL, BUMSTEAD, KAISER and BARROW2006).

Stimulation of pro-inflammatory cytokines following salmonella infection has been well documented in the literature (Hu et al., Reference HU, YU, KULKARNI, SHARIF, CUI, XIE, NIE and GONG2015). Earlier reports have confirmed that infection with salmonella could significantly increase the expression of inflammatory cytokines and other innate immune genes in chicken caecal tonsils (Haghighi et al., Reference HAGHIGHI, ABDUL-CAREEM, DARA, CHAMBERS and SHARIF2008), spleen (Zhou and Lamont, Reference ZHOU and LAMONT2007), macrophages (Zhang et al., Reference ZHANG, LILLEHOJ, KIM, KEELER, BABU and ZJANG2008) and heterophils (Chiang et al., Reference CHIANG, SWAGGERTY, KOGUT, DOWD, LI, PEVZNER and ZHOU2008). Varmuzova et al. (Reference VARMUZOVA, KUBASOVA, DAVIDOVA-GERZOVA, SISAK, HAVLICKOVA, SEBKOVA, FALDYNOVA and RYCHLIK2016), observed mild up-regulation of genes coding for acute phase proteins (e.g., AVD, SAA, TRAP, ExFABP, IRG1), following Salmonella enteritidis infection.

Higgins et al. (Reference HIGGINS, WOLFENDEN, TELLEZ, HARGIS and PORTER2011) reported that cytochrome P450, polypeptide 4 (CYP1A4) family 1, subfamily A, was down-regulated in salmonella infected chickens. Withanage et al. (Reference WITHANAGE, KAISER, WIGLEY, POWERS, MASTROENI, BROOKS, BARROW, SMITH, MASKELL and McCONNELL2004; Reference WITHANAGE, WIGLEY, KAISER, MASTROENI, BROOKS, POWERS, BEAL, BARROW, MASKELL and McCONNELL2005) and Beal et al. (Reference BEAL, POWERS, WIGLEY, BARROW and SMITH2004) studied Salmonella typhimurium infection in chickens, and observed up-regulation of some cytokines and chemokines in macrophage cells, the caecal tonsils, ileum, spleen and liver. Withanage et al. (Reference WITHANAGE, WIGLEY, KAISER, MASTROENI, BROOKS, POWERS, BEAL, BARROW, MASKELL and McCONNELL2005) found that the IL-6, a well-known pro-inflammatory cytokine, was up-regulated in the ileum and spleen on days one and three days post infection with Salmonella typhimurium. However, IL-6 was up-regulated in caecal tonsils by 21 days post infection, which suggests that this late expression during the period of infection may mean that this cytokine is not involved in triggering an inflammatory response to Salmonella typhimurium (Withanage et al., Reference WITHANAGE, WIGLEY, KAISER, MASTROENI, BROOKS, POWERS, BEAL, BARROW, MASKELL and McCONNELL2005). The up-regulation of IL-10 cytokine has been recognised in the tissues of salmonella infected birds (Cheeseman et al., Reference CHEESEMAN, KAISER, CIRACI, KAISER and LAMONT2007). In a study by Haghighi et al. (Reference HAGHIGHI, ABDUL-CAREEM, DARA, CHAMBERS and SHARIF2008), IL-12 gene expression in caecal tonsils of chickens was significantly increased on days one and five post infection with Salmonella typhimurium compared to uninfected controls.

Based on these findings, Haghighi et al. (Reference HAGHIGHI, ABDUL-CAREEM, DARA, CHAMBERS and SHARIF2008) suggested a correlation between cytokine expression profiles in the host bird and resistance to Salmonella typhimurium. These authors reported a relationship between Th1 cytokines, IFN-γ down-regulation and IL-12 up-regulation and Salmonella typhimurium colonisation inhibition in the intestinal lumen. There are comparable reports for Th2 cytokine IL-4 (Stoycheva and Murdjeva, Reference STOYCHEVA and MURDJEVA2005; Berndt et al., Reference BERNDT, WILHELM, JUGERT, PIEPER, SACHSE and METHNER2007). Among the cytokines, interleukin IL-12, interferon IFN-g and IL-18 are involved in salmonella inhibition, while IL-4 and IL-10 are important to reduce subsequent inflammatory responses (Eckmann and Kagnoff, Reference ECKMANN and KAGNOFF2001; Beal et al., Reference BEAL, POWERS, WIGLEY, BARROW and SMITH2004; Withanage et al., Reference WITHANAGE, WIGLEY, KAISER, MASTROENI, BROOKS, POWERS, BEAL, BARROW, MASKELL and McCONNELL2005).

Effects of probiotics on immune gene expression

Different antibiotic alternative strategies have been proposed to control salmonella colonisation in the chicken intestine, of which the administration of probiotics is of note, however the underlying mechanism of probiotic protection against salmonella infection is not completely understood (Akbari et al., Reference AKBARI, HAGHIGHI, CHAMBERS, BRISBIN, READ and SHARIF2008). Probiotics could prevent salmonellosis in the chicken through enhancing antigen-specific and natural antibodies (Jie-Lun et al., Reference JIE-LUN, HAI, RAVEENDRA, SHAYAN, STEVE, MING-YONG, SHAO-PING and JOSHUA2015). Varmuzova et al. (Reference VARMUZOVA, KUBASOVA, DAVIDOVA-GERZOVA, SISAK, HAVLICKOVA, SEBKOVA, FALDYNOVA and RYCHLIK2016) reported that transferring a microbial population sample from three week old or older chickens to younger ones decreased the inflammatory response to infection with S. enteritidis. Haghighi et al. (Reference HAGHIGHI, ABDUL-CAREEM, DARA, CHAMBERS and SHARIF2008) suggested that probiotic-mediated control of salmonella infection may be via modulation of cytokines. Cytokines are immunoregulatory proteins involved in both innate and adaptive immune responses (Eckmann et al., 2001).

Yang et al. (Reference YANG, BRISBIN, YU, WANG, YIN, ZHANG, SABOUR, SHARIF and GONG2014) found that some lactobacillus isolates down-regulated caecal salmonella pathogenicity island 1 (SPI-1) virulence gene, which is a key regulator of intestinal invasion of the pathogen. Bobíková et al. (Reference BOBÍKOVÁ, REVAJOVA, KARAFFOVA, LEVKUTOVA and LEVKUT2015) studied the IgA mRNA expression in the caecum of chickens fed probiotic bacterial strain Enterococcus faecium AL41 and then infected with Salmonella enterica subspecies Enteritidis PT4. The results confirmed the favourable effect of probiotic on the mRNA expression of IgA and some IgA+ cells. These authors suggested that Enterococcus faecium AL41 increased the influx of IgA+cells into mucus of caecum and increased the relative mRNA expression of IgA in the caecum of chickens and a mild increase of CD4+ and IgM+ cells in the intestinal mucus. This confirmed the role of these immunocompetent cells to the IgA genome development and occurrence of intraepithelial IgA+ cells.

The lactobacilli are a well-known group of probiotic bacteria used to control salmonella infection through improvement of bird immunity (Zhang et al., Reference ZHANG, MA and DOYLE2007; Haghighi et al., Reference HAGHIGHI, ABDUL-CAREEM, DARA, CHAMBERS and SHARIF2008; Chambers and Gong, Reference CHAMBERS and GONG2011). Several cytokine-mediated immune pathways are involved in providing lactobacillus-mediated protection against salmonella infection, including inducing pro-inflammatory cytokines such as lipopolysaccharide-induced TNF factor and gamma interferon (IFN-γ), and anti-inflammatory cytokines such as interleukin (IL)-10 (Nava et al., Reference NAVA, BIEIKE, CALLAWAY and CASTANEDA2005; Castillo et al., Reference CASTILLO, PERDIGON and DE MORENO DE LEBLANC2011). Hu et al. (Reference HU, YU, KULKARNI, SHARIF, CUI, XIE, NIE and GONG2015) treated chickens with lactobacillus isolates and observed considerable changes in the expression of genes encoding pro-inflammatory cytokines, including lipopolysaccharide-induced TNF factor (LITAF), interleukin (IL)-6; IL-8, T helper (Th) 1 cytokines, including IL-12, interferon (IFN)-γ, and Th2 cytokines including IL-4 and IL-10) in salmonella infected birds. These authors suggested the administration of some lactobacillus isolates can successfully change salmonella-mediated cytokine gene expression induction and therefore, help to control infection in chickens. A more pronounced change could be down-regulating the salmonella virulence gene expression involved in intestinal invasion and altering cytokine gene expression to improve chicken immunity (Hu et al., Reference HU, YU, KULKARNI, SHARIF, CUI, XIE, NIE and GONG2015).

In a study by Akbari et al. (Reference AKBARI, HAGHIGHI, CHAMBERS, BRISBIN, READ and SHARIF2008), the avian beta-defensin 1 (AvBD1), AvBD2, AvBD4, AvBD6, and cathelicidin gene expression increased in response to salmonella challenge, and probiotic supplementation inhibited infection via the antimicrobial peptide expression. These authors suggested that the down-regulation of antimicrobial genes may be because of the probiotic-salmonella combination or, because of a decreased salmonella load in the intestine, as these genes could not be provoked (Akbari et al., Reference AKBARI, HAGHIGHI, CHAMBERS, BRISBIN, READ and SHARIF2008).

Haghighi et al. (Reference HAGHIGHI, ABDUL-CAREEM, DARA, CHAMBERS and SHARIF2008) fed probiotics to chickens on day one of age and then challenged them with Salmonella typhimurium on day two of age. The IL-12 gene expression was similar to that of uninfected birds and probiotic administrations decreased the IFN-g gene expression in the caecal tonsils of chickens infected with salmonella. These findings suggest that down-regulation of IL-12 and IFN-g genes in the gut-associated lymphoid tissues of the chicken are involved in the probiotic-associated reduction of S. typhimurium colonisation in the bird's intestine. Therefore, it is possible that probiotics prevent or decrease the cytokine-producing immune system cell movement following salmonella challenge into the tissue, which resulted in a reduction in cytokine gene expression in probiotic-fed chickens (Haghighi et al., Reference HAGHIGHI, ABDUL-CAREEM, DARA, CHAMBERS and SHARIF2008).

Higgins et al. (Reference HIGGINS, WOLFENDEN, TELLEZ, HARGIS and PORTER2011) challenged one day old chicks with Salmonella enterica serovar Enteritidis and 1 h later introduced a lactobacillus-based probiotic. They found considerable regulation of genes related to the nuclear factor kappa B complex, and genes involved in apoptosis. Taken together, it seems that probiotic-mediated differential regulation of growth arrest-specific 2 and cysteine-rich, angiogenic inducer 61 (CYR61) genes could increase apoptosis in the caeca of chickens, and because salmonella is an intracellular pathogen, it seems that more apoptosis may be a probiotic mediated way to decrease infection (Higgins et al., Reference HIGGINS, WOLFENDEN, TELLEZ, HARGIS and PORTER2011).

Effects of probiotics on antimicrobial peptides involved in salmonella control

Antimicrobial peptides have a key role in salmonellosis control (Wigley, Reference WIGLEY2014). Akbari et al. (Reference AKBARI, HAGHIGHI, CHAMBERS, BRISBIN, READ and SHARIF2008) investigated the potential role of antimicrobial peptides in salmonella infection and possible probiotic-mediated mechanisms. Antimicrobial peptides are innate defence systems (Sugiarto and Yu, Reference SUGIARTO and YU2004) and are divided into two major families, defensins and cathelicidins (Ganz, Reference GANZ2003). Based on the site of their disulphide bonds, defensins are subdivided into two main classes: alpha-defensins and beta-defensins (Menendez and Brett Finlay, 2007). Birds express only beta-defensins (Lynn et al., Reference LYNN, HIGGS, LOYD, O'FARRELLY, HERVE-GREPINET, NYS, BRINKMAN, YU, SOULIER, KAISER, ZHANG and LEHRER2007), and their heterophils or epithelial cells express these peptides (Sugiarto and Yu., 2004). Defensins show antimicrobial properties against gram-negative and gram-positive bacteria, fungi and certain viruses (Ganz, Reference GANZ2003) and may stimulate the acquired immune response against pathogens by improving maturation of dendritic cells and recruitment of effector T cells to challenged tissues (Yang et al., Reference YANG, BIRAGYN, KWAK and OPPENHEIM2002). There are reports that probiotic lactobacilli bacterial and cell wall preparations of Enterococcus faecalis (EC-12) can provoke the expression of defensins, for example AvBD2, in different tissues, including the tongue and the bursa of Fabricius (Sakai et al., Reference SAKAI, TSUKAHARA, BUKAWA, MATSUBARA and USHIDA2006; Schlee et al., Reference SCHLEE, HARDER, KOTEN, STANGE, WEHKAMP and FELLER-MANN2008).

Akbari et al. (Reference AKBARI, HAGHIGHI, CHAMBERS, BRISBIN, READ and SHARIF2008), measured the expressions of AvBD1, AvBD2, AvBD4, AvBD6, and cathelicidin in the caecal tonsils of chickens challenged with Salmonella typhimurium or treated with probiotics before salmonella infection. They observed up-regulation in all the studied antimicrobial peptides in salmonella infection birds, although probiotic administration before the challenge decreased the expression of these peptides. These authors suggested that probiotics may provoke the expression of beta-defensins. Consequently, it may be that when probiotic bacteria are associated with salmonella, they may show antagonistic properties against salmonella-mediated increase in defensin genes expression (Akbari et al., Reference AKBARI, HAGHIGHI, CHAMBERS, BRISBIN, READ and SHARIF2008). On the other hand, the lower expression of defensin genes in the probiotic-fed and salmonella challenged birds may be due to the inhibitory property of probiotic bacteria on salmonella and subsequent lower colonisation in the intestine may remove the inflammatory situations needed for the stimulation of these genes (Akbari et al., Reference AKBARI, HAGHIGHI, CHAMBERS, BRISBIN, READ and SHARIF2008). In a comparable report, Yoshimura et al. (Reference YOSHIMURA, OHASHI, SUBEDI, NISHIBORI and ISOBE2006) observed that infection of cell cultures of the hen oviduct with Salmonella enterica serovar Enteritidis and lipopolysaccharide (LPS) up-regulated the AvBD1, AvBD2, and AvBD3 genes.

Conclusions

Supplementation with probiotics in poultry diet results in changes in the immune system. Even though there are differences under infection and non-challenge conditions, it appears that probiotics may provide more beneficial immune modulation effects in salmonella infected birds. The modulatory effects of probiotics on immune responses in salmonella infected chickens can partly be attributed to altering immune system related gene expression. Probiotics have different effects on cytokine gene expression, based on the probiotic species and cellular response, including the antimicrobial peptide genes, encoding for pro-inflammatory cytokines, T helper (Th) 1 cytokines, and Th2 cytokine gene expression. However, the increased apoptosis of salmonella infected cells in the presence of lactobacillus-based probiotic cultures decreases the numbers of colonised bacteria in the caeca of chicks.

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