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Ghorani M. Antiviral Effects of Probiotic Metabolites. Iran J Med Microbiol 2022; 16 (2) :83-97
URL: http://ijmm.ir/article-1-1434-en.html
Pathobiology Department, Faculty of Veterinary Medicine, University of Tabriz, Tabriz, Iran , mo_gh66@yahoo.com
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Introduction

The rate of viral infections is rising dramatically around the world, and definitive solutions to them seem difficult. In addition, effective antiviral drugs are scarce due to the genetic mutations of many viruses. Respiratory infections and gastroenteritis are the leading causes of death worldwide in developing and developed countries. Despite the widespread adop-tion of vaccination strategies, some pathogens remain a threat to public health worldwide. Fassi et al. (2005) and the National Institutes of Health (NIH) reported the emergence of 16 new infectious diseases, six of which were considered recurrent infections (1). Hardy et al. (2013) consider strengthening the immune system as the most important key factor in preventing infectious diseases. Dietary balance in meals, presc-ribing supplements such as fiber and probiotics are three ways to strengthen and stimulate the immune system, thus protecting the mucosa against the entry of pathogens. Probiotics have been shown to stimulate and modulate the immune system (2). Alkasa et al. (2015) believe that in addition to the antibacterial activity of probiotics, some strains have shown effective antiviral activity that can be a solution to the deficiency of antiviral agents (3). In the following, the antiviral activities of probiotic meta-bolites are investigated.

Antiviral Activity of Probiotic Metabolites

1. Non-organic Substances

Hydrogen peroxide (H2O2) is an antimicrobial agent, which is made by various species of bacteria including Streptococcus pneumoniae (S. pneumonia) and Strep-tococcus pyogenes (S. pyogenes) that are pathogenic or opportunistic bacteria (4, 5). H2O2 is produced by some probiotic strains as a defense mechanism. Moreover, some species of Bifidobacteria are allowed by H2O2 to survive under microaerobic circumstances (6). H2O2 has a key role in animals and humans, particularly in the vaginal ecosystem. H2O2 is also made by some lactobacilli as a natural antimicrobial in the vaginal environment. It is toxic to some microorganisms such as HIV-1 and HSV-2 (7, 8). According to Mentel et al. (1977), a concentration of 3% hydrogen peroxide within 1-30 min, adeno type 3 and 6 viruses, influenza A and B, adeno type 4 viruses, coronavirus inactivates strain 229E, rhinovirus 1A and 1B and type 7, myxoma, and senile senile virus (9). Organic acids were classified by the Food and Drug Administration (FDA) as completely safe for humans. Most microorganisms are sensitive to organic acids since they are killed by a specific mechanism where undecomposed molecules are ionized within their own cell membrane. Therefore, by releasing hydrogen ions, the cells immediately react thus reducing the pH and consequently cell damage (10). Producing lactic acid is a key resistance mechanism preventing the acid-sensitive microorganisms’ growth including those causing infectious diseases (11). Kenti et al. (8) reported that the viability of microorganisms was significantly reduced by lactic acid physiological concentrations of (not acetic acid). Here, it is hypothesized that antimicrobial activity is not directly associated with pH, however, it is associated with the organic acid nature. All LAB species produce lactic acid as the end carbohydrate metabolism product. Lactic acid is in charge of the regulation of vaginal pH physiologically in the human ecosystem. HIV (12) and HSV-2 (13) are inactivated by acidic pH. Besides, HSV-2 is inactivated irreversibly by lactic acid in a healthy person’s vagina (8). It seems that compounds are produced by lactobacilli, which help host cells hinder the replication of the virus (14). Therefore, HSV-2 proliferation is effectively reduced in cell culture by a non-protein cell wall component extracted from vaginal Lactobacillus brevis. According to Strobe et al. (2011), lactic acid imposes antiviral impacts against non-envelope viruses like ECHO and FCV. It was also indicated that enteroviruses are inactivated based on the type of virus since the ECHO virus was more stable than FCV while existing lactic acid D / L (15).

2. Organic Substances 

Protein substances secreted by probiotic strains and LAB are further characterized molecules as a result of their consequent antiviral effect and antimicrobial activity. Though, the direct influences of various non-protein compounds have already been reported including polyphenols (16) or taflavins (17), against rotaviruses. However, proteinaceous materials with non-microbial origin are less explained based on their antiviral activity. Lactoferrin is the most extensively reported protein with at least part of the antiviral features of breast milk (18) and stops rotaviruses from being absorbed into target cells owing to its capability at binding to virus particles. (19). It was indicated that Capacazine has the antiviral activity to HuRoVs. Through glycan residues, it can bind rotavirus particles together (20).
2-1. Bacteriocins
Bacteriocins are antimicrobial peptides made in the ribosome pathway. Tag et al. (1976) indicated the activity of bacteriocins against bacteria related to the producer strain (21). However, it has been recently indicated that some bacteriocins made by lactic acid bacteria belonging to the enterococcus (enterosin E50-52 and enterosin E760) and genus Lactobacillus (bacteriocin OR7) (bacteriocin XDSM) have further activities such as Gram-positive and Gram-negative like Campylobacter jejuni, Salmonella, Yersinia, Escherichia coli O157: H7, Moganla Morgani, Shigella dysentery, Listeria, and Staphylococcus aureus (22-26). Clanhammer (1993) (27) classified bacteriocins into 4 groups in terms of primary amino acid sequence, structure, molecular weight (kDa), and stability with alterations in pH and temperature. This categorization was severely changed owing to various scientific results. Cotter et al. (28) presented the next classification into three categories. In this classi-fication, Class I is lantibiotics as the small hydrophobic peptides ( et al. divided this class into 6 subclasses (29). Class II peptides are non-antibiotic classified into 4 subclasses IIa, IIb, IIc, and IId. The Class II general properties are determined by thermal stability and a molecular weight less than KDa10. Heat-resistant bacteriocins are included in Class III as a protein, not a peptide since it has a higher molecular weight (> 30 KDa).

Lactic acid bacteria-produced bacteriocins have several benefits. Indeed, they provide a competitive effect for bacteriosynogenic lactic acid bacteria on access to nutrients in natural ecosystems comprising various microorganisms (30). They are preferred by humans in food preservation since they can be utilized as alternatives to antibiotics or combined with natural antibiotics (28, 31, 32). Although the bacteriocins’ antibacterial activity was described partially, their antiviral activity is not comprehended yet. Various speculated or reported models and unknown models are included in the set of bacteriocins with antiviral activity. Bacteriocins such as Staphylococcus 188, enterosin AAR-74, enterosin AAR-71and arvinusin NA4 were examined against the HSA coliform virus isolated from raw wastewater specimen (collected from a local wastewater treatment plant). Enterosin AAR-74 and staphylococcus aureus 188 reduced virus replication by factor 10. However, arvinusin NA4 and enterosin AAR-71 removed virus replication comple-tely (33). Moreover, Staphylococcus 188 was active against Newcastle disease virus and influenza virus in vitro and in vitro models (34). Antiviral activity against HSV-1 (35) was exhibited by Enterosin ST5Ha (ST5Ha). In particular, cell viability (CC50) was reduced by enterosin ST5Ha at a concentration of 8645 mg/ml by more than 50%. This concentration was higher than the ST4V and CRL35 bacteriocins’ antiviral concen-trations (2500 and 1600 mg/ml), respectively (36, 37). In Vero and BHK-21 cells, the antiviral activity of enterosin ST4V and CRL35 against positive and defective strains of herpes simplex thymidine kinase type 1 and 2 was found affecting the intracellular virus proliferation and inhibiting the last proliferation phases (36- 38). The CRL35 amino acid sequence plays a vital role in anti-HSV-1 and anti-HSV-2 activities. CRL35 derivatives were examined without at least two cysteine residues. It was indicated they have no antibacterial activity with no antiviral activity.
Bacteriocin ST5Ha (50 mg/mL) decreased HSV-1 viral production in cell culture by more than 50% (EC50) with a selective index (CC50 / CE50) of 173 (35). It was indicated that strong anti-listeria activity is exhibited by pediatric enterotin like NKR-5-3 C (35). Assessing the anti-HSV-1 activity of NKR-5-3C, its CC50 was found less than 1200 μg/mL. However, the CE50 value was 30 mg/ mL. Labyrinosopeptin A1 (LabyA1) is a sample peptide from a new group of carbocyclic lantibiotics (39). Widespread and persistent anti-HSV (EC50: 0.29-2.8mM) and anti-HIV (EC50: 0.70-3.3mM) activity were exhibited by LabyA1 in cell cultures (39). LabyA1 represented the virus’s cell-to-cell transmit-ssion between CD4 + T4 uninfected cells and HIV-infected T cells (EC50: 2.5 mM) thus preventing the transmission of HIV-derived DC-SIGN + cells to CD4 + T-infected cells (EC50: 4.1 mM) (38, 39). To demonstrate the synergistic effect on anti-HIV-1 and anti-HSV-2 activities, LabyA1 was used in dual combination with acyclovir, tenofovir, saquinavir, anfovovitid, and raltegravir (39).
It is not well known how bacteriocins work against viruses. Washman et al. (38) indicated that the receptors accumulation is hindered by bacteriocins on host cells resulting in the accumulation of viral particles. They can also hinder the key reactions in the proliferative cycle. Presently, a non-cytotoxic Lacto-bacillus delbrokii-produced class IV bacteriocin was isolated under Bulgarius 1043 and represented to kill the influenza virus (40). The bacteriocins' nature is responsible for the antiviral activity. Lang et al. supp-orted this hypothesis reporting that MuNoV, herpes-virus (FHV), H1N1, and Newcastle disease (NDV) viruses were not reduced by saccharin A nisin (41).

2-2. Non-ribosomal Peptides (NRPs)

NRPs are natural and biologically active compounds with various clinical applications. Some NRP‌s are utilized as antitumor drugs (bleomycin), antibiotics (daptomycin), immunosuppressants (cyclosporine), or antifungal drugs (42). This diverse biological activity can be clarified by the combination of these molecules in nature. NRPs are made by the secondary metabolism of fungi and bacteria by the amino acids sequential densification made by several non-riboso-mal synthetase peptides (NRPSs) and multimodular enzymes (42, 43). Several reports indicated that some NRPSs can be utilized as antiviral agents against enveloped viruses. In the study of Wollenbroch et al. (1997) (44), the surfactant biosurfactant (Bacillus subtilis-made NRPS antifungal) can be herpes simplex virus (HSV-1, HSV-2), Semicolon virus (SFV), and herpes simplex virus (SHV), vesicular stomatitis virus (VSV), feline calcareous virus (FCV) monkey immune-deficiency virus (SIV), and mouse encephalomyo-carditis virus (EMCV). Furthermore, the Coxsackie B4 virus can be inhibited by surfactants at lower concentrations.

Probiotics and Their Proteinaceous Metabolites

According to current clinical trials, some probiotic strains can enhance acute rotavirus diarrhea (45). It is thought that mucosal barrier enhancement, intestinal microbial balance, and modulation of the immune response protect against rotavirus diarrhea (46). Though, the underlying mechanisms for the protective effects of probiotics against viruses has been investigated in a few studies. Lee et al. (47) revealed that rotavirus infection is strongly prevented by Lactobacillus acidophilus (LA) and Bifidobacterium langum (IBG) in the Vero cell line, while they identify no mechanism.
Under Infentis CECT7210, bifidobacterium fungus represented the capability of inhibiting rotavirus replication in both in vivo and in vitro circumstances. In the study of Chanel et al. (48), the antiviral mechanism of this strain was investigated. Therefore, this supernatant was gathered and examined for RoV in both MA-104 and HT-29 cell lines. Based on the findings, the supernatant possessed antiviral activity, and protease digestion represented both the proteinaceous nature of the active substance. Moreover, the molecule inhibiting the rotavirus replication was released in the supernatant. Further purifying and identification was performed on the peptide. It was revealed that this antiviral peptide includes 11 amino acids with a molecular weight of 1.282 kDa and MHQPHQPLPPT sequence. After various experiments, it was found that a protease was secreted by Bifidobacterium langum secreted by Infentis CECT7210, which digested casein in MRS broth. Among the outcomes of casein digestion was antiviral peptide (48).
Galen et al. (2016) presented another mechanism by these two strains along with the blocking effects of Lactobacillus casei rotavirus and Bifidobacterium adelsantis, Olia. It was revealed that proteinaceous substances are secreted by these two strains interfering with the final quantity of intracellular NSP4, formerly explained as rotavirus enterotoxin. Thus, the duration and cell lysis of diarrhea were decreased. Moreover, Ca2 + can be also regulated by these metabolites thus preventing its release from the enterocytes' endoplasmic reticulum and reducing the cell damage (49).
VHHs are nanobodies formerly utilized for treating rotavirus-related diarrhea (50). These nanobodies are fragments of antibodies extracted from light chain-free immunoglobulins found in camels (51). Alvarez et al. selected LGGs, with antiviral activity represented by several mechanisms (56-52) for antiviral VHH expression (57). various strains of GG (ATCC 53103), LGG (GG (CMC), GG (UT), and GG (NCC 3003)) were examined for their capability to possess nanobodies in their cell wall. Only the GG (UT) strain could represent ARP1 (VHH antiviral rotavirus) on the bacteria surface since this strain includes the inactivated welF EPS and welE genes. No expression of EPS permits the efficient display of ARP1 on its surface. A mouse model was used in an in vitro experiment representing that GG strains (UT) had a protective level against rotavirus diarrhea. The lack of EPS had no effect on the antiviral activity. However, further studies are required on this strain, particularly on its capability at binding to enterocytes (57).

Unspecified Antiviral Metabolites

Various studies revealed the probiotics’ antiviral activity while not specifying the specific antiviral molecules.
Thus, further studies are required to assess low-toxicity, high-performance, and minor side effects of antivirals. Moreover, an urgent need exists for antiviral molecules against viral pathogens in animals and humans. In 1986, the antiviral activity (influenza virus) of boiled yogurt was screened among various milk preparations. According to the results, the infected mice treated with boiled yogurt had a longer survival rate than the infected mice. Furthermore, the treated mice had lower hemagglutinin titers compared to the infected mice (58). The cell-free supernatant (CFS) of seven probiotic strains was also tested for its antiviral activity against vesicular stomatitis virus (VSV). The strain included Bifidobacterium go DSM 20091, Lactobacillus para-casei F14, Bifidobacterium Langum Q 46, Lactobacillus rhamnosus Q 85, Lactobacillus 12S, Lactobacillus D1, which were cultured in MRS broth, a coated virus related to the rhabdoviridae family. All probiotic strains represented antiviral activity in their superficial fluids. Moreover, the viral infection rate was reduced by around 68%. It was revealed that this activity is associated with three possible mechanisms including the interaction between bacterial cells and host, trapping of viral particles via direct probiotic strains interaction, and ultimately neutralizing the viral particles via probiotic metabolites like protein mole-cules or organic acids (59).
Both yogurt and CSF MRS cultures of seven probiotic strains were examined by Choi et al. including Lactobacillus rhamnosus, Lactobacillus acidophilus, Streptococcus thermophilus, Lactobacillus plantarum, and Bifidobacterium bifidum. CFSs were examined against numerous RNA-infected viruses such as Influenza virus A / WS / 33; influenza A / PR / 8/34 virus; Influenzavirus B / Lee / 40; swine epidemic diarrhea virus D (PEDV) CV 777, and Coxsackievirus A16 (CA16), CB3 and CB4. Along with the nonexistence of cytotoxicity in the Vero and MDCK cell lines, these CFSs represented antiviral activity via inhibition of virus replication. Moreover, yogurt-derived CFSs represented the strongest activity (60). It was also indicated that yogurt-derived CFSs filtered by Amicon (Millipore, Bilrica, USA) with MW CO <3000 Da had the same antiviral activity. Moreover, the antiviral compounds’ MW was less than Da 3000.
The antiviral activity of CFS Lactococcus lactis subunit Lactis LM0230 was represented, which is a probiotic strain cultured in MRS broth. This CFS was assessed in the Crandell Reese (CRFK) cats’ kidneys against cat kidney virus (FCV) as a substitution for NoV. According to the results, the viral load was reduced by CFS. Though, the viral load was not affected by neutral CFS (pH = 7.0) (61). It was found that for denaturing the viral capsid lactic acid is essential (Roger et al.) (62).
Lang Stark et al. (41) assessed the antiviral activity of both D / L lactic acid and various LAB CFS sausages against H1N1, MuNoV, FHV and NDV followed by evaluating the sacacin A and nisin. D / L lactic acid was examined against H1N1 and MuNoV. The viral load was reduced by lactic acid by 2.5 and 3.25 units in H1N1 and MuNoV, respectively. There was no cytotoxicity in the lactic acid’s active concentration. Moreover, LF CFS was examined against MuNoV. According to the results, in MuNoV, only the culture supernatant of Lactobacillus corvatus 1 was active. Furthermore, catalytic refining, thermal refining, freezing, and neutralization of CFS Lactobacillus corvatus 1 revealed that the antiviral compound is a protein. By separating this CFS via chromatographic technique, it was hypothesized that this antiviral compound had the MW of kDa 2, which is very close to a bacteriocin. However, this hypothesis is disproved by the thermal variability of this compound since the heat-resistant bacteriocins possess an MW> 30 kDa (27). Shearer et al. (63) also reported the antiviral activity of CFSs for Enterococcus faecalis 19433 and Bacillus subtilis 168 against MuNoV 1 and Tulane virus. In CFSs, no direct effect was found on the viral particles. Nevertheless, a weak inhibitory effect was represented by CFSs on virus replication in LLCMK2 and RAW 264.7 cell lines.
The probiotics’ antiviral effect was also studied in a work, which showed no effect of probiotics on rota-virus infection in pregnant Lewis G14 mice while exis-ting Bifidobacterium M-16 V as a probiotic strain (64).


 

Conclusion

In both the medical and food sectors it is possible to activate some LAB and probiotic metabolites against various viruses like membrane and non-membrane viruses. The most significant antiviral compounds of probiotic metabolites are hydrogen peroxide, organic acids, and protein molecules. The safety of D / L lactic acid and bacteriocins was extensively studied. It appears that antiviral activity is molecularly specific since no antiviral activity was represented by LAB CFSs comprising lactic acid and some bacteriocins. Moreover, their activity is based on the virus’s type or subtype. There are complex experiments to evaluate these metabolites. The cytotoxicity of some metabo-lites has attracted a huge deal of attention to assessing the direct influences of these metabolites on the target virus. Levin-Le Maval and Servin (2014) indicated a cytotoxic effect of some Lactobacillus CFSs on Caco-2 cell lines possibly covering the primary antiviral effects of these CFSs, for instance in the rotavirus replication cycle. (65). To identify the true antiviral compound and in-depth investigate the mechanism of action of these molecules, broken CFS is vital.
Considering the arrival of antibiotic resistance, the recent frightening predictions regarding antibiotic resistance, and the spread of untreated emergent viral infections, probiotics, and prebiotics will be further required in the future. Hence, further studies are required to provide promising findings of the effects of probiotics.

 

Acknowledgment

None.

 

Conflicts of Interest

The authors declare no conflict of interest.
 


 

Type of Study: Review Article | Subject: Antimicrobial Substances
Received: 2021/08/16 | Accepted: 2022/01/15 | ePublished: 2022/02/10

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