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IJMS
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Vaccination against Enterobacteriaceae: From Pre-clinical Models to Translation
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Vaccination against Enterobacteriaceae: From Pre-clinical Models to Translation

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Microbiology".

Deadline for manuscript submissions: 30 September 2024 | Viewed by 4095

Special Issue Editor

Prof. Dr. Jochen Mattner

E-Mail Website
Guest Editor
Medical Immunology Campus Erlangen, FAU Erlangen-Nürnberg, 91054 Erlangen, Germany
Interests: mucosal immunology; inflammatory bowel disease; lipid biology; cytokines; microbiota; gastrointestinal infections; allelic variations; genetic susceptibility; vaccination
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Some members of the family of Enterobacteriaceae are part of the physiological gut microbiota or transiently colonize the intestine without causing any harm. However, Enterobacteriaceae can also cause severe and even life-threatening infections of multiple organ systems following the acquisition of virulence plasmids or the disruption of commensal microbiota (dysbiosis). Due to the increasing frequency of infections with Enterobacteriaceae in clinical settings and the outbreaks of multi-resistant strains, the use of antibiotics for treatment is increasingly limited. To prevent the spread of multi-drug-resistant Enterobacteriaceae, vaccination next to antibiotic stewardship programs is an alternative promising option. Depending on the species-specific infection sites, the presentation of antigens and the route of immunization need to be carefully considered. Furthermore, the unavailability of suitable animal models for some Enterobacteriaceae hampers preclinical testing and the subsequent design of clinical trials. Thus, novel avenues need to be pursued to characterize the nature of bacterial antigens and to obtain effective vaccine candidates.

Since IJMS is a journal of molecular science, pure clinical studies are not suitable. However, we welcome clinical submissions with biomolecular experiments and encourage authors to reveal new molecular mechanisms in their research.

Prof. Dr. Jochen Mattner
Guest Editor

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. International Journal of Molecular Sciences is an international peer-reviewed open access semimonthly journal published by MDPI.

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Keywords

  • enterobacteriaceae
  • (mucosal) vaccines
  • immunity
  • intestinal microbiota
  • dysbiosis
  • microbial pathogenesis
  • animal models

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Published Papers (4 papers)

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Research

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15 pages, 1852 KiB  
Article
UNAM-HIMFG Bacterial Lysate Activates the Immune Response and Inhibits Colonization of Bladder of Balb/c Mice Infected with the Uropathogenic CFT073 Escherichia coli Strain
by Salvador Eduardo Acevedo-Monroy, Ulises Hernández-Chiñas, Luz María Rocha-Ramírez, Oscar Medina-Contreras, Osvaldo López-Díaz, Ricardo Ernesto Ahumada-Cota, Daniel Martínez-Gómez, Sara Huerta-Yepez, Ana Belén Tirado-Rodríguez, José Molina-López, Raúl Castro-Luna, Leonel Martínez-Cristóbal, Frida Elena Rojas-Castro, María Elena Chávez-Berrocal, Antonio Verdugo-Rodríguez and Carlos Alberto Eslava-Campos
Int. J. Mol. Sci. 2024, 25(18), 9876; https://doi.org/10.3390/ijms25189876 - 12 Sep 2024
Viewed by 260
Abstract
Urinary tract infections (UTIs) represent a clinical and epidemiological problem of worldwide impact that affects the economy and the emotional state of the patient. Control of the condition is complicated due to multidrug resistance of pathogens associated with the disease. Considering the difficulty [...] Read more.
Urinary tract infections (UTIs) represent a clinical and epidemiological problem of worldwide impact that affects the economy and the emotional state of the patient. Control of the condition is complicated due to multidrug resistance of pathogens associated with the disease. Considering the difficulty in carrying out effective treatment with antimicrobials, it is necessary to propose alternatives that improve the clinical status of the patients. With this purpose, in a previous study, the safety and immunostimulant capacity of a polyvalent lysate designated UNAM-HIMFG prepared with different bacteria isolated during a prospective study of chronic urinary tract infection (CUTI) was evaluated. In this work, using an animal model, results are presented on the immunostimulant and protective activity of the polyvalent UNAM-HIMFG lysate to define its potential use in the control and treatment of CUTI. Female Balb/c mice were infected through the urethra with Escherichia coli CFT073 (UPEC O6:K2:H1) strain; urine samples were collected before the infection and every week for up to 60 days. Once the animals were colonized, sublingual doses of UNAM-HIMFG lysate were administrated. The colonization of the bladder and kidneys was evaluated by culture, and their alterations were assessed using histopathological analysis. On the other hand, the immunostimulant activity of the compound was analyzed by qPCR of spleen mRNA. Uninfected animals receiving UNAM-HIMFG lysate and infected animals administered with the physiological saline solution were used as controls. During this study, the clinical status and evolution of the animals were evaluated. At ninety-six hours after infection, the presence of CFT073 was identified in the urine of infected animals, and then, sublingual administration of UNAM-HIMFG lysate was started every week for 60 days. The urine culture of mice treated with UNAM-HIMFG lysate showed the presence of bacteria for three weeks post-treatment; in contrast, in the untreated animals, positive cultures were observed until the 60th day of this study. The histological analysis of bladder samples from untreated animals showed the presence of chronic inflammation and bacteria in the submucosa, while tissues from mice treated with UNAM-HIMFG lysate did not show alterations. The same analysis of kidney samples of the two groups (treated and untreated) did not present alterations. Immunostimulant activity assays of UNAM-HIMFG lysate showed overexpression of TNF-α and IL-10. Results suggest that the lysate activates the expression of cytokines that inhibit the growth of inoculated bacteria and control the inflammation responsible for tissue damage. In conclusion, UNAM-HIMFG lysate is effective for the treatment and control of CUTIs without the use of antimicrobials. Full article
(This article belongs to the Special Issue Vaccination against Enterobacteriaceae: From Pre-clinical Models to Translation)
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Figure 1

Figure 1
<p>Urinary tract infection induced with UPEC strains in Balb/c, C57BL/6, and CD-1 mice. This study was conducted over eight weeks, analyzing the presence of bacteria in urine.</p> Full article ">Figure 2
<p><span class="html-italic">E. coli</span> CFT073 recovered from urine samples in Balb/c mice to which it was administered UNAM-HIMFG lysate or PSS. Abbreviations: (CFT073 + PSS) <span class="html-italic">E. coli</span> CFT073 infected and PSS administered; (CFT073 + UNAM-HIMFG) <span class="html-italic">E. coli</span> CFT073 infected and UNAM-HIMFG lysate treated.</p> Full article ">Figure 3
<p>Expression of TNF-α (<b>A</b>) and IL-10 (<b>B</b>) in mice spleen mRNA of UI + PSS, CFT073 + PSS, CFT073 +UNAM-HIMFG, and UI + UNAM-HIMFG animal groups.</p> Full article ">Figure 4
<p>Histological analysis of bladder from Balb/c mice. (<b>A</b>) UI + PSS; (<b>B</b>) CFT073 + UNAM-HIMFG; (<b>C</b>–<b>F</b>) CFT073 + PSS; (<b>C</b>) The arrow indicates Granulomatous inflammation; (<b>D</b>) Arrow shows areas of mild inflammation and leukocytic infiltration; (<b>E</b>,<b>F</b>) Arrows show Gram-negative bacilli forming colony-like communities. Magnification: 400× (<b>A</b>–<b>D</b>) and 1000× (<b>E</b>,<b>F</b>). Hematoxylin/Eosin stain (<b>A</b>–<b>D</b>); Sandiford stain (<b>E</b>,<b>F</b>).</p> Full article ">
20 pages, 3188 KiB  
Article
Deep Intraclonal Analysis for the Development of Vaccines against Drug-Resistant Klebsiella pneumoniae Lineages
by Ana Tajuelo, Eva Gato, Jesús Oteo-Iglesias, María Pérez-Vázquez, Michael J. McConnell, Antonio J. Martín-Galiano and Astrid Pérez
Int. J. Mol. Sci. 2024, 25(18), 9837; https://doi.org/10.3390/ijms25189837 - 11 Sep 2024
Viewed by 279
Abstract
Despite its medical relevance, there is no commercial vaccine that protects the population at risk from multidrug-resistant (MDR) Klebsiella pneumoniae infections. The availability of massive omic data and novel algorithms may improve antigen selection to develop effective prophylactic strategies. Up to 133 exposed [...] Read more.
Despite its medical relevance, there is no commercial vaccine that protects the population at risk from multidrug-resistant (MDR) Klebsiella pneumoniae infections. The availability of massive omic data and novel algorithms may improve antigen selection to develop effective prophylactic strategies. Up to 133 exposed proteins in the core proteomes, between 516 and 8666 genome samples, of the six most relevant MDR clonal groups (CGs) carried conserved B-cell epitopes, suggesting minimized future evasion if utilized for vaccination. Antigens showed a range of epitopicity, functional constraints, and potential side effects. Eleven antigens, including three sugar porins, were represented in all MDR-CGs, constitutively expressed, and showed limited reactivity with gut microbiota. Some of these antigens had important interactomic interactions and may elicit adhesion-neutralizing antibodies. Synergistic bivalent to pentavalent combinations that address expression conditions, interactome location, virulence activities, and clone-specific proteins may overcome the limiting protection of univalent vaccines. The combination of five central antigens accounted for 41% of all non-redundant interacting partners of the antigen dataset. Specific antigen mixtures represented in a few or just one MDR-CG further reduced the chance of microbiota interference. Rational antigen selection schemes facilitate the design of high-coverage and “magic bullet” multivalent vaccines against recalcitrant K. pneumoniae lineages. Full article
(This article belongs to the Special Issue Vaccination against Enterobacteriaceae: From Pre-clinical Models to Translation)
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Figure 1

Figure 1
<p>Sizes of genome datasets, pan-proteomes, core proteomes, and exposed proteins in <span class="html-italic">K. pneumoniae</span> MDR-CGs. Circles are proportional to the number of genomes and were expressed as sector diagrams when more than one ST was involved to denote the proportion of the genome contribution of each ST to the MDR-CG.</p> Full article ">Figure 2
<p>MDR-CG antigens and epitopes. (<b>a</b>) Distribution of antigens according to MDR-CG coverage. (<b>b</b>) Length distribution of epitopes, including raw predictions by BepiPred3 and those conserved in MDR-CGs. (<b>c</b>) Dendrogram and heatmap showing antigen co-existence between all MDR-CG pairs. The percentage of antigenic matching is color-ranked and indicated within the cells. (<b>d</b>) Boxplot showing the ST <span class="html-italic">K. pneumoniae</span> spread of MDR-CG antigens binned by MDR-CG prevalence. Orange dash indicates the median value. Box limits indicate the interquartile range. Whiskers were adjusted to maximal and minimal values if lower than 1.5 times the IQR. Further outliers are indicated as circles.</p> Full article ">Figure 3
<p>Potential cross-reactivity between <span class="html-italic">K. pneumoniae</span> MDR-CG antigens and human gut microbiota proteomes. (<b>a</b>) Number of antigens showing homologs with gut microbiota isolates at different sequence identity cutoffs. (<b>b</b>) Number of antigens showing homologs with gut microbiota isolates above 60% identity according to MDR-CG coverage. Bars for global, intermediate, and specific MDR-CG antigens are colored in red, orange, and green, respectively. (<b>c</b>) Number of antigens sharing epitopes with five residues or with homologs in gut microbiota isolates according to MDR-CG coverage. Bars for global, intermediate, and specific MDR-CG antigens are colored in red, orange, and green, respectively. (<b>d</b>) Boxplot showing length distribution of MDR-CG epitopes shared with human gut microbiota. Values were organized by the number of MDR-CGs represented by the epitope. Orange dash indicates the median value. Box limits indicate the interquartile range. Whiskers were adjusted to maximal and minimal values if lower than 1.5 times the IQR. Further outliers are indicated as circles.</p> Full article ">Figure 4
<p>Functional constraints of MDR-CG antigens. (<b>a</b>) General functional category of antigens according to MDR-CG coverage. Only categories with at least 4% COG assignation in a MDR-CG coverage bin were included. (<b>b</b>) Weighted three-class Venn diagrams showing the number of expressed antigens during planktonic, biofilm, and biofilm dispersed stages. Low (≥50 DESeq, <b>left</b>) and high (≥500 DESeq, <b>right</b>) RNA-Seq detection thresholds were considered. The Venn diagrams were depicted using the <span class="html-italic">Venn_3</span> method of the <span class="html-italic">matplotlib</span> Python library. (<b>c</b>) Species origin of putative virulence antigens (<b>left</b>). Prevalence of VF categories for antigens (<b>right</b>).</p> Full article ">Figure 5
<p>Interactomic properties of MDR-CG antigens. (<b>a</b>) Antigen distribution according to the total number of PPIs and VF-PPIs. (<b>b</b>) Prevalence of VF categories for first-rank interactions of antigens. The cumulative number of PPIs, i.e., one protein can interact with several antigen partners, is shown. (<b>c</b>) Antigen distribution according to BC values. (<b>d</b>) Topology of the <span class="html-italic">K. pneumoniae</span> interacting network. Antigens are colored by virulence categories if applicable. The sphere diameter of antigen nodes is proportional to BC value. Antigen nodes are name-labeled when above a BC cutoff of 0.3% or 0.1% if they are VFs. Non-antigen nodes are shown as small dots in gray. Edges are shown in gray.</p> Full article ">Figure 6
<p>Antigens selected for univalent vaccines against <span class="html-italic">K. pneumoniae</span> MDR-CGs. Antigens were inversely sorted by the raw number of conserved B-cell epitope residues. Values for filtering criteria were color-ranked where the intensity was proportional to the positive condition. The number of first-order interactive partners grouped by virulence class is provided in brackets.</p> Full article ">Figure 7
<p>Aggregated number of all PPIs and those with non-redundant partners of antigens. Antigens were reversely sorted on the x-axis by their contribution to the interactome.</p> Full article ">Figure 8
<p>Intermediate MDR-CG antigens showing low gut microbiota and low general <span class="html-italic">K. pneumoniae</span> ST predicted cross-reactivities. Representation (filled cells) and non-representation (empty cells) of the MDR-CGs by the antigen are indicated.</p> Full article ">Figure 9
<p>Specific MDR-CG antigens showing low gut microbiota and low general <span class="html-italic">K. pneumoniae</span> ST predicted cross-reactivity. Representation (filled cells) and non-representation (empty cells) of the MDR-CGs by the antigen are indicated.</p> Full article ">
20 pages, 4216 KiB  
Article
Polyvalent Bacterial Lysate with Potential Use to Treatment and Control of Recurrent Urinary Tract Infections
by Salvador Eduardo Acevedo-Monroy, Luz María Rocha-Ramírez, Daniel Martínez Gómez, Francisco Javier Basurto-Alcántara, Óscar Medina-Contreras, Ulises Hernández-Chiñas, María Alejandra Quiñones-Peña, Daniela Itzel García-Sosa, José Ramírez-Lezama, José Alejandro Rodríguez-García, Edgar González-Villalobos, Raúl Castro-Luna, Leonel Martínez-Cristóbal and Carlos Alberto Eslava-Campos
Int. J. Mol. Sci. 2024, 25(11), 6157; https://doi.org/10.3390/ijms25116157 - 3 Jun 2024
Viewed by 898
Abstract
Overuse of antimicrobials has greatly contributed to the increase in the emergence of multidrug-resistant bacteria, a situation that hinders the control and treatment of infectious diseases. This is the case with urinary tract infections (UTIs), which represent a substantial percentage of worldwide public [...] Read more.
Overuse of antimicrobials has greatly contributed to the increase in the emergence of multidrug-resistant bacteria, a situation that hinders the control and treatment of infectious diseases. This is the case with urinary tract infections (UTIs), which represent a substantial percentage of worldwide public health problems, thus the need to look for alternatives for their control and treatment. Previous studies have shown the usefulness of autologous bacterial lysates as an alternative for the treatment and control of UTIs. However, a limitation is the high cost of producing individual immunogens. At the same time, an important aspect of vaccines is their immunogenic amplitude, which is the reason why they must be constituted of diverse antigenic components. In the case of UTIs, the etiology of the disease is associated with different bacteria, and even Escherichia coli, the main causal agent of the disease, is made up of several antigenic variants. In this work, we present results on the study of a bacterial lysate composed of 10 serotypes of Escherichia coli and by Klebsiella pneumoniae, Klebsiella aerogenes, Enterococcus faecalis, Proteus mirabilis, Citrobacter freundii, and Staphylococcus haemolyticus. The safety of the compound was tested on cells in culture and in an animal model, and its immunogenic capacity by analysing in vitro human and murine macrophages (cell line J774 A1). The results show that the polyvalent lysate did not cause damage to the cells in culture or alterations in the animal model used. The immunostimulatory activity assay showed that it activates the secretion of TNF-α and IL-6 in human macrophages and TNF-α in murine cells. The obtained results suggest that the polyvalent lysate evaluated can be an alternative for the treatment and control of chronic urinary tract infections, which will reduce the use of antimicrobials. Full article
(This article belongs to the Special Issue Vaccination against Enterobacteriaceae: From Pre-clinical Models to Translation)
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Figure 1

Figure 1
<p>SDS PAGE of polyvalent and monovalent lysate components Silver stained. (<b>A</b>): Lines: (1) Polyvalent lysate (UNAM-HIMFG), (2) <span class="html-italic">E.coli</span> O25, (3) <span class="html-italic">E.coli</span> O20, (4) <span class="html-italic">Citrobacter</span>, (<b>B</b>): Lines: (1) <span class="html-italic">Klebsiella</span>, (2) <span class="html-italic">Enterococcus</span>, (3) <span class="html-italic">Staphylococcus</span>, and (4) <span class="html-italic">Proteus</span>. <span class="html-italic">MW Molecular Weight: PageRuler Plus Prestained Protein Ladder</span> (ThermoScientific).</p> Full article ">Figure 2
<p>Western blot of polyvalent (UNAM-HIMFG) and monovalent lysates. The lysates were challenged with a serum sample obtained from a patient previously treated with a lysate prepared with an O25 <span class="html-italic">E. coli</span> strain. Lines: (1) UNAM-HIMFG; (2) <span class="html-italic">E.coli</span> O25; (3) <span class="html-italic">E.coli</span> O20; and (4) <span class="html-italic">Citrobacter</span>. <span class="html-italic">MW Molecular Weight</span>: <span class="html-italic">PageRuler Plus Prestained Protein Ladder</span>.</p> Full article ">Figure 3
<p>Western blot of different preparations of the UNAM-HIMFG polyvalent lysate. The WB was developed with polyvalent rabbit antibodies obtained against OmpA. Lines: 1, 2, and 3, samples of different preparations of polyvalent lysate. (Arrow indicates OmpA 35 kDa) <span class="html-italic">MW Molecular Weight</span>: Page Ruler Plus Protein Ladder pre-dye.</p> Full article ">Figure 4
<p>Histological evaluation of mice tissues treated with physiological saline solution (<b>left</b>) or the polyvalent bacterial lysate (<b>right</b>). (<b>A</b>,<b>B</b>) Stomach epithelium, (<b>C</b>,<b>D</b>) Intestinal epithelium. Samples were stained with Eosin and Hematoxylin and observed to ×400.</p> Full article ">Figure 5
<p>Secretion of TNF-α in J774 A.1 murine macrophages with different concentrations of the lysates. (<b>A</b>) UNAM-HIMFG, (<b>B</b>) <span class="html-italic">E. coli</span> O 25:H4, (<b>C</b>) <span class="html-italic">E. coli</span> O20:H9, (<b>D</b>) <span class="html-italic">K. pneumoniae</span>, and (<b>E</b>) <span class="html-italic">E. faecalis</span>. Results are the average of three tests performed in duplicate <span class="html-italic">p</span> ≤ 0.005. SSF: Physiological saline solution; PMB: polymyxin B 100 μg/μL; LPS: Lipopolysaccharide 100 ng/μL.</p> Full article ">Figure 6
<p>TNF-α and IL-6 production of human macrophages activated by UNAM-HIMFG, <span class="html-italic">E. coli</span> O 25:H4, and <span class="html-italic">E. faecalis</span> lysates. UNAM-HIMFG (<b>A</b>,<b>D</b>), <span class="html-italic">E. coli</span> O 25:H4 (<b>B</b>,<b>E</b>), y <span class="html-italic">E. faecalis</span>. (<b>C</b>,<b>F</b>). Results are the average of three tests performed in duplicate. <span class="html-italic">p</span> ≤ 0.005. SSF: Physiological saline solution; PMB: polymyxin B 100 μg/μL; LPS: Lipopolysaccharide 100 ng/μL.</p> Full article ">

Review

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25 pages, 2078 KiB  
Review
Shigella Vaccines: The Continuing Unmet Challenge
by Ti Lu, Sayan Das, Debaki R. Howlader, William D. Picking and Wendy L. Picking
Int. J. Mol. Sci. 2024, 25(8), 4329; https://doi.org/10.3390/ijms25084329 - 13 Apr 2024
Cited by 2 | Viewed by 2191
Abstract
Shigellosis is a severe gastrointestinal disease that annually affects approximately 270 million individuals globally. It has particularly high morbidity and mortality in low-income regions; however, it is not confined to these regions and occurs in high-income nations when conditions allow. The ill effects [...] Read more.
Shigellosis is a severe gastrointestinal disease that annually affects approximately 270 million individuals globally. It has particularly high morbidity and mortality in low-income regions; however, it is not confined to these regions and occurs in high-income nations when conditions allow. The ill effects of shigellosis are at their highest in children ages 2 to 5, with survivors often exhibiting impaired growth due to infection-induced malnutrition. The escalating threat of antibiotic resistance further amplifies shigellosis as a serious public health concern. This review explores Shigella pathology, with a primary focus on the status of Shigella vaccine candidates. These candidates include killed whole-cells, live attenuated organisms, LPS-based, and subunit vaccines. The strengths and weaknesses of each vaccination strategy are considered. The discussion includes potential Shigella immunogens, such as LPS, conserved T3SS proteins, outer membrane proteins, diverse animal models used in Shigella vaccine research, and innovative vaccine development approaches. Additionally, this review addresses ongoing challenges that necessitate action toward advancing effective Shigella prevention and control measures. Full article
(This article belongs to the Special Issue Vaccination against Enterobacteriaceae: From Pre-clinical Models to Translation)
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Figure 1

Figure 1
<p>Timeline of vaccine development against <span class="html-italic">Shigella</span> infection. This figure illustrates key milestones in the field of <span class="html-italic">Shigella</span> research and vaccine development, highlighting breakthroughs and advances achieved over the years. Figure created using <a href="http://BioRender.com" target="_blank">BioRender.com</a> (accessed on 17 October 2023).</p> Full article ">Figure 2
<p><span class="html-italic">Shigella</span> pathogenesis. (<b>Left</b>) Stepwise evasion of the host immune system by <span class="html-italic">Shigella</span> during its journey from ingestion to the colonization of the intestine. This figure highlights key mechanisms employed by <span class="html-italic">Shigella</span> to evade immune detection and clearance at various stages of infection. (<b>Right</b>) Detailed depiction of the process of <span class="html-italic">Shigella</span> invasion into host cells via genetic changes and acquisition of virulence plasmids (<b>right top</b>) providing insights into the intricate mechanisms by which <span class="html-italic">Shigella</span> breaches the host epithelial barrier and initiates intracellular replication by using the type III secretion system (T3SS) or enterotoxins (<b>right middle</b>), leading to infection and pathogenesis (<b>right bottom</b>). The straight arrows at the top represent mechanisms, while the straight arrows in the middle indicate different infections. Curved arrows in the middle and bottom denote the release of toxins. Figure created using <a href="http://BioRender.com" target="_blank">BioRender.com</a> (accessed on 17 October 2023).</p> Full article ">Figure 3
<p>Current <span class="html-italic">Shigella</span> vaccines in development. This figure provides an overview of the diverse vaccine candidates currently under development against <span class="html-italic">Shigella</span> infections. Each vaccine candidate is displayed along with its corresponding target antigens. Figure created with <a href="http://BioRender.com" target="_blank">BioRender.com</a> (accessed on 17 October 2023).</p> Full article ">Figure 4
<p>Animal models for vaccine development against <span class="html-italic">Shigella</span> infection. (<b>Left</b>) Various challenge routes can be used in mouse models. The figure outlines different routes, such as (<b>A</b>) intranasal delivery, (<b>B</b>) intraperitoneal injection, and (<b>C</b>) oral administration. (<b>Right</b>) Non-mouse animal models employed in <span class="html-italic">Shigella</span> vaccine development research. This includes (<b>D</b>,<b>G</b>) primate models, (<b>E</b>) rabbit models, and (<b>F</b>) guinea pig models. Each offers unique advantages and insights into <span class="html-italic">Shigella</span> pathogenesis and vaccine responses. Figure created using <a href="http://BioRender.com" target="_blank">BioRender.com</a> (accessed on 17 October 2023).</p> Full article ">
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