Development of a broad-spectrum epitope-based vaccine against Streptococcus pneumoniae

Md. Nahian; Muhammad Shahab; Md. Rasel Khan; Shopnil Akash; Tanjina Akhtar Banu; Murshed Hasan Sarkar; Barna Goswami; Sanjana Fatema Chowdhury; Mohammad Ariful Islam; Ahmed Abu Rus’d; Shamima Begum; Ahashan Habib; Aftab Ali Shaikh; Jonas Ivan Nobre Oliveira; Shahina Akter

doi:10.1371/journal.pone.0317216

Peer Review History

Original SubmissionJune 14, 2024
17 Jul 2024 Decision Letter - Rajesh Kumar Pathak, Editor PONE-D-24-24274Development of a Broad-Spectrum Epitope-Based Vaccine Against Streptococcus pneumoniaePLOS ONE Dear Dr. Akter, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please submit your revised manuscript by Aug 31 2024 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. 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If you are unable to adhere to our open data policy, please kindly revise your statement to explain your reasoning and we will seek the editor's input on an exemption. Please be assured that, once you have provided your new statement, the assessment of your exemption will not hold up the peer review process. 4. Please include captions for your Supporting Information files at the end of your manuscript, and update any in-text citations to match accordingly. Please see our Supporting Information guidelines for more information: http://journals.plos.org/plosone/s/supporting-information. Additional Editor Comments: The manuscript in its present form lacks clarity and requires extensive revision. Information about the half-life of the vaccine needs to be mentioned. The results of the molecular dynamics simulation need to be explained in detail during revision. Important analyses such as RMSD and RMSF are missing and should be included. Additionally, the concerns raised by the reviewers need to be thoroughly addressed in the revised manuscript. [Note: HTML markup is below. Please do not edit.] Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #1: Yes Reviewer #2: Partly ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: N/A Reviewer #2: No ****** 3. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #1: Yes Reviewer #2: Yes ****** 4. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: Yes Reviewer #2: Yes ****** 5. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #1: 1. Use Escherichia coli (E. coli) for the first time in the manuscript, and E. coli will be used from then on. Please do the same for toll-like receptors (TLRs). 2. The words "in silico", "in vivo", and "invitro" should be written in italics. 3. In the topic of this work, the word "prediction" is not the right word, use "prediction" instead. 4. Modeling, refining, validation of the three-dimensional structure 3D structure of CbpA and PspA proteins, as well as predicting structural B-cell epitopes based on their 3D structure, are trivial tasks. Please remove these parts from the manuscript. 5. Authors must provide a rationale for using each linker in the vaccine structure. 6. The authors only reported the value of the quality assessment parameters of the refined 3D model if they did not mention the reason for choosing the model. The output of the GalaxyRefine server is 5 refined models, in which the quality evaluation parameters of the refined 3D model are presented. Please provide this table in the manuscript, describe each parameter in detail, and explain why this model was chosen. 7. Authors should provide the definition of each physicochemical parameter in the Materials and Methods section. 8. The authors reported the results of the molecular dynamics simulation in a very general way. Please explain the results of this section in detail. 9. The authors should perform structural disulfide engineering of the 3D structure of the vaccines 10. Please perform the molecular docking between T-cell epitopes and MHC molecules. 11. Please compare the characteristics of the vaccines designed in this study with the vaccines designed in other authors' studies. For this, please use the following references and cite them. https://doi.org/10.3390/vaccines11020263 https://doi.org/10.2174/1573409919666230612125440 https://doi.org/10.1080/07391102.2023.2258403 https://doi.org/10.1016/j.ijbiomac.2024.131517 https://doi.org/10.1007/s12033-023-00949-y Reviewer #2: In the current study, authors constructed a multi-epitope vaccine using bioinformatics analysis. Here are some comments needs to be addressed. Minor Keep the font size constant throughout the paper. See 2.6 is smaller compared to others. Major 1. Authors identified 23 virulence protein in S. pneumoniae based on their search. I am curious to know in general how many total proteins are encoded in the S. pneumoniae genome. What will be the scores of other proteins not covered in this study. Current score of top2 proteins is not very high. Also, has somebody previously reported about these proteins? 2. I am not very confident with the various webserver-based results as the values are too low for many of the analysis ranging from 0.4-0.6 in many cases. I am concerned regarding the efficacy of the vaccine. 3. Authors have not mentioned about the stability of half-life of the vaccine in the blood? ****** 6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #1: No Reviewer #2: Yes: Piyush Agrawal, Ph.D. ******** [NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.] While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step. https://doi.org/10.1371/journal.pone.0317216.r001
Revision 1
17 Oct 2024 Author Response PONE-D-24-24274 Development of a Broad-Spectrum Epitope-Based Vaccine Against Streptococcus pneumoniae PLOS ONE Comments from the Editors: The manuscript in its present form lacks clarity and requires extensive revision. Information about the half-life of the vaccine needs to be mentioned. The results of the molecular dynamics simulation need to be explained in detail during revision. Important analyses such as RMSD and RMSF are missing and should be included. Additionally, the concerns raised by the reviewers need to be thoroughly addressed in the revised manuscript. Ans: We thank the academic editor for the careful reading of the manuscript and the constructive remarks. We have addressed your comments to improve and clarify the manuscript throughout. As suggested, we have incorporated detailed information regarding the half-life of the vaccine. Initially, the vaccine construct demonstrated an unsatisfactory half-life, prompting us to optimize the adjuvant sequence. This optimization resulted in a significant improvement in the half-life, ensuring greater stability and efficacy of the vaccine. These findings are now clearly presented in the revised manuscript. To further strengthen the results, we have conducted additional molecular dynamics simulations and included crucial analyses such as RMSD, RMSF, Rg, and hydrogen bonding patterns. To facilitate the review process, we have also submitted a track-changes document highlighting the modifications made. Figures have been uploaded separately in accordance with the journal's requirements. Additionally, we have provided a point-by-point response to all reviewers' comments. (reviewers’ comments in black, our replies in blue). Reviewer #1: 1. Use Escherichia coli (E. coli) for the first time in the manuscript, and E. coli will be used from then on. Please do the same for toll-like receptors (TLRs). Ans: Thank you for your valuable feedback. We have revised the manuscript to use the full term "Escherichia coli" the first time it is mentioned, with "E. coli" used in subsequent references. Similarly, we have spelled out "toll-like receptors" at their initial mention and used "TLRs" thereafter. 2. The words "in silico", "in vivo", and "invitro" should be written in italics. Ans: Thank you for suggesting this specific point. We have made the terms "in silico," "in vivo," and "in vitro" italic throughout the manuscript as per your suggestion. 3. In the topic of this work, the word "prediction" is not the right word, use "prediction" instead. Ans: Thank you for your comment. We have reviewed the manuscript and corrected the use of the word 'prediction' as suggested. 4. Modeling, refining, validation of the three-dimensional structure 3D structure of CbpA and PspA proteins, as well as predicting structural B-cell epitopes based on their 3D structure, are trivial tasks. Please remove these parts from the manuscript. Ans: We appreciate your insightful comment. We have removed the sections pertaining to the modeling, refining, validation of the 3D structures of CbpA and PspA proteins, as well as the prediction of structural B-cell epitopes. 5. Authors must provide a rationale for using each linker in the vaccine structure. Ans: We have carefully considered the rationale for each linker used in the vaccine structure and have provided a detailed explanation for their inclusion is provided in the 'Methodology' section of the revised manuscript. 6. The authors only reported the value of the quality assessment parameters of the refined 3D model if they did not mention the reason for choosing the model. The output of the GalaxyRefine server is 5 refined models, in which the quality evaluation parameters of the refined 3D model are presented. Please provide this table in the manuscript, describe each parameter in detail, and explain why this model was chosen. Ans: Thank you for your valuable feedback. A table presenting the quality assessment parameters of all five refined 3D models generated by the GalaxyRefine server has been included in the manuscript. Each parameter has been described in detail, and a clear rationale for the selection of the final model is provided. 7. Authors should provide the definition of each physicochemical parameter in the Materials and Methods section. Ans: Thank you for this insightful comment. The definitions of all physicochemical parameters used in the study have been clearly provided in the 'Methodology' section of the revised manuscript. 8. The authors reported the results of the molecular dynamics simulation in a very general way. Please explain the results of this section in detail. Ans: As suggested by the reviewer, we have now provided a detailed explanation of the molecular dynamics simulation results in the revised manuscript. To gain deeper insights into the molecular dynamics, we employed the Amber v.22 tool to analyze key parameters such as RMSD, RMSF, Rg, and hydrogen bonding patterns. 9. The authors should perform structural disulfide engineering of the 3D structure of the vaccines Ans: As suggested by the reviewer, we have now performed structural disulfide engineering on the 3D structure of the vaccines. The results of this analysis are included in the revised manuscript. 10. Please perform the molecular docking between T-cell epitopes and MHC molecules. Ans: As suggested by the reviewer, we have now performed molecular docking between the T-cell epitopes and MHC molecules. The results of this analysis are included in the revised manuscript. 11. Please compare the characteristics of the vaccines designed in this study with the vaccines designed in other authors' studies. For this, please use the following references and cite them. https://doi.org/10.3390/vaccines11020263 https://doi.org/10.2174/1573409919666230612125440 https://doi.org/10.1080/07391102.2023.2258403 https://doi.org/10.1016/j.ijbiomac.2024.131517 https://doi.org/10.1007/s12033-023-00949-y Ans: Thank you for your suggestion. We have now compared the characteristics of the vaccines designed in our study with those from the studies referenced and have included the appropriate citations. Reviewer #2: In the current study, authors constructed a multi-epitope vaccine using bioinformatics analysis. Here are some comments needs to be addressed. Minor Keep the font size constant throughout the paper. See 2.6 is smaller compared to others. Ans: Thank you for your comment. We have carefully reviewed the manuscript and ensured that the font size is consistent throughout the entire document, Major 1. Authors identified 23 virulence protein in S. pneumoniae based on their search. I am curious to know in general how many total proteins are encoded in the S. pneumoniae genome. What will be the scores of other proteins not covered in this study. Current score of top2 proteins is not very high. Also, has somebody previously reported about these proteins? Ans: We thank you for the insightful comments. We have modified our ‘’Methodology’ section to remove any ambiguity and have also provided the following information regarding our selection criteria for the protein candidates. Total Proteins in S. pneumoniae Genome: The exact number of proteins encoded in the S. pneumoniae genome can vary slightly depending on the specific strain. However, recent estimates suggest that S. pneumoniae has approximately 2,000-2,300 protein-coding genes. Potential Scores of Other Proteins: It is possible that other proteins not included in this study could also score well in bioinformatic predictions. However, our study did not aim to conduct a comprehensive proteome analysis. Instead, we focused on proteins that have already been validated as potential vaccine candidates through various experimental studies. Numerous previous studies have identified certain proteins in S. pneumoniae that demonstrate significant efficacy as vaccine targets. Therefore, we initially selected our protein vaccine candidates based on their established immunogenic properties identified through literature mining. Current Scores of Top 2 Proteins: To further refine our selection, we employed VaxiJen and PsortB to predict antigenicity and subcellular localization, respectively. While we acknowledge that other proteins within the S. pneumoniae proteome may exhibit similar or even higher scores, our approach allowed us to identify two promising candidates, CbpA and PspA, with exceptional characteristics. Their VaxiJen scores of 0.7721 and 0.6565, significantly surpassing the cutoff of 0.4, strongly indicate their antigenic potential. Moreover, their PsortB scores of 9.73 each, well above the cutoff of 7.5, suggest a high probability of extracellular localization, a crucial factor for vaccine efficacy. Previous Reports on the Selected Proteins: CbpA and PspA have been previously identified in the literature as potential vaccine candidates due to their roles as virulence factors in S. pneumoniae and their capacity to elicit an immune response. We also evaluated these proteins using bioinformatic tools to assess their antigenicity and subcellular localization, thereby strengthening the case for their inclusion in a multi-epitope vaccine construct. We are also aware of previous studies that have incorporated S. pneumoniae proteins into multi-epitope vaccine construction. However, to the best of our knowledge, the specific combination of CbpA and PspA as potential targets in a multi-epitope-based vaccine has not been previously reported. The vaccine construct we developed, consisting of epitopes from both CbpA and PspA, represents a novel approach. 2. I am not very confident with the various webserver-based results as the values are too low for many of the analysis ranging from 0.4-0.6 in many cases. I am concerned regarding the efficacy of the vaccine. Ans: Thank you for your valuable comment. We appreciate your concern regarding the efficacy of the vaccine. With due respect, we would like to inform you that the antigenicity scores generated by VaxiJen (1.371) and ANTIGENpro (0.89) are within acceptable ranges and indicative of potential immunogenicity. Experiments conducted by other tools have also yielded promising results, suggesting the potential efficacy of our vaccine construct, which is discussed in detail in the 'Discussion' section. These results collectively support the potential of our vaccine and suggest it is suitable for subsequent wet lab experiments for further verification. 3. Authors have not mentioned about the stability of half-life of the vaccine in the blood. Ans: Thank you for your careful remark. We have now incorporated information regarding the stability and half-life of the vaccine in the blood. Attachments Attachment Submitted filename: Response to Reviewers.docx https://doi.org/10.1371/journal.pone.0317216.r002
12 Nov 2024 Decision Letter - Rajesh Kumar Pathak, Editor PONE-D-24-24274R1Development of a Broad-Spectrum Epitope-Based Vaccine Against Streptococcus pneumoniaePLOS ONE Dear Dr. Akter, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please submit your revised manuscript by Dec 27 2024 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. 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Reviewer #1: N/A Reviewer #2: N/A ****** 4. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #1: Yes Reviewer #2: Yes ****** 5. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: Yes Reviewer #2: Yes ****** 6. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #1: The authors considered all the comments correctly. I hope this article is an important reference in the field of vaccine design Reviewer #2: (No Response) ****** 7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #1: No Reviewer #2: Yes: Piyush Agrawal ******** [NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.] While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step. https://doi.org/10.1371/journal.pone.0317216.r003
Revision 2
17 Dec 2024 Author Response We have carefully checked the reviewers comments and revised accordingly Attachments Attachment Submitted filename: Response to Reviewers.docx https://doi.org/10.1371/journal.pone.0317216.r004
23 Dec 2024 Decision Letter - Rajesh Kumar Pathak, Editor Development of a Broad-Spectrum Epitope-Based Vaccine Against Streptococcus pneumoniae PONE-D-24-24274R2 Dear Dr. Akter, We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements. Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication. An invoice will be generated when your article is formally accepted. Please note, if your institution has a publishing partnership with PLOS and your article meets the relevant criteria, all or part of your publication costs will be covered. Please make sure your user information is up-to-date by logging into Editorial Manager at Editorial Manager® and clicking the ‘Update My Information' link at the top of the page. If you have any questions relating to publication charges, please contact our Author Billing department directly at authorbilling@plos.org. If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org. Kind regards, Rajesh Kumar Pathak, Ph.D. Academic Editor PLOS ONE Additional Editor Comments (optional): The manuscript can be accepted for publication. Reviewers' comments: https://doi.org/10.1371/journal.pone.0317216.r005
Formally Accepted
7 Jan 2025 Acceptance Letter - Rajesh Kumar Pathak, Editor PONE-D-24-24274R2 PLOS ONE Dear Dr. Akter, I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team. At this stage, our production department will prepare your paper for publication. This includes ensuring the following: * All references, tables, and figures are properly cited * All relevant supporting information is included in the manuscript submission, * There are no issues that prevent the paper from being properly typeset If revisions are needed, the production department will contact you directly to resolve them. If no revisions are needed, you will receive an email when the publication date has been set. At this time, we do not offer pre-publication proofs to authors during production of the accepted work. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few weeks to review your paper and let you know the next and final steps. Lastly, if your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org. If we can help with anything else, please email us at customercare@plos.org. Thank you for submitting your work to PLOS ONE and supporting open access. Kind regards, PLOS ONE Editorial Office Staff on behalf of Dr. Rajesh Kumar Pathak Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0317216.r006

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