MicroRNA-199a-5p attenuates blood-brain barrier disruption following ischemic stroke by regulating PI3K/Akt signaling pathway

Guangxiao Ni; Lulu Kou; Chunqiao Duan; Ran Meng; Pu Wang

doi:10.1371/journal.pone.0306793

Peer Review History

Original SubmissionFebruary 1, 2024
2 Apr 2024 Decision Letter - Francesco Sessa, Editor PONE-D-24-00772MicroRNA-199a-5p attenuates blood-brain barrier disruption following ischemic stroke by regulating PI3K/Akt signaling pathwayPLOS ONE Dear Dr. NI, 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 May 17 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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Thank you for stating the following financial disclosure: "National Natural Science Foundation of China，（No.81273609） Natural Science Foundation of Hebei Province，(No. H2023206115)" Please state what role the funders took in the study. If the funders had no role, please state: ""The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript."" If this statement is not correct you must amend it as needed. Please include this amended Role of Funder statement in your cover letter; we will change the online submission form on your behalf. 4. We note that your Data Availability Statement is currently as follows: All relevant data are within the manuscript and its Supporting Information files. Please confirm at this time whether or not your submission contains all raw data required to replicate the results of your study. Authors must share the “minimal data set” for their submission. 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If there are ethical or legal restrictions on sharing a de-identified data set, please explain them in detail (e.g., data contain potentially sensitive information, data are owned by a third-party organization, etc.) and who has imposed them (e.g., an ethics committee). Please also provide contact information for a data access committee, ethics committee, or other institutional body to which data requests may be sent. If data are owned by a third party, please indicate how others may request data access. 5. Please ensure that you include a title page within your main document. You should list all authors and all affiliations as per our author instructions and clearly indicate the corresponding author. 6. Please include your full ethics statement in the ‘Methods’ section of your manuscript file. In your statement, please include the full name of the IRB or ethics committee who approved or waived your study, as well as whether or not you obtained informed written or verbal consent. If consent was waived for your study, please include this information in your statement as well. 7. Please include a separate caption for each figure in your manuscript. 8. Please include your tables as part of your main manuscript and remove the individual files. Please note that supplementary tables (should remain/ be uploaded) as separate ""supporting information"" files Additional Editor Comments: The reviewers raised several important concerns. I believe that authors should further improve their manuscript. Please, revise the manuscript solving all criticisms and providing the rebuttal letter. [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: No Reviewer #2: Yes ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: Yes ****** 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: No 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: No Reviewer #2: No ****** 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: In this manuscript, the authors studied the preventive and therapeutic effects of miR-199a-5p through PI3K/Akt pathway on ischemia stroke. On this basis, they further investigated the role of miR-199a-5p in BBB. Despite some highlights, this paper has a number of shortcomings, such as the logic of manuscript, the data etc, and page numbers and line numbers are missing. 1.The introduction lacks logic. Especially, it did not describe the relationship between miRNA and BBB. Please describe in detail. 2.Where are the tables? I can’t find them. Neurological function scores are better presented as bar graphs than table. 3.The improvement effect of miRNA on MCAO was only evaluated with neurological function score. It should add the data of infarct size and pathological status. 4.Although this study provides detailed evidence of the efficacy of CC, it does not provide in-depth mechanistic validation. 5.There is no logic in the results section. It should be showed from effect to mechanism. 6.Fig. 6A should add the merged figure. 7.The discussion lacks logic. Moreover, miR-199a-5p, as the key to this paper, has not been highlighted in the discussion. 8.Another obvious problem with this paper is lack of sufficient explanation of the results. More explanations on them seem necessary and helpful to readers. 9.The first paragraph of the discussion requires a brief summary of the research results. 10. It is noted that your manuscript needs careful editing by someone with expertise in technical English editing paying particular attention to English grammar, spelling, and sentence structure so that the goals and results of the study are clear to the reader. Reviewer #2: This is a well-organized study exploring the association of MicroRNA-199a-5p attenuates BBB disruption following ischemic stroke. Major: The concept of the study is not novel and the topic itself is important, however, the lack of clear rationale and mechanistic assessments reduces the scientific value of the paper. The English used in the manuscript is understandable but the text needs to be edited by a native speaker. Spelling, grammar, and syntax errors are present in the text. In the study implications, novelty aspects of the study and limitations are not indicated. Minor: please correct abbreviations - for example, in the introduction, CNS has already been used before, and TJs, not TJS - access to food and not diet - there are some misleading sentences in the text for example that miR-199a-5p was a main factor in the process of cerebral ischemia - introduction ****** 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: No ******** [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. Attachments Attachment Submitted filename: PONE-D-24-00772.docx https://doi.org/10.1371/journal.pone.0306793.r001
Revision 1
28 May 2024 Author Response Response to Reviewers Dear Editors and Reviewers: Thank you for your letter and for the reviewers’ comments concerning our manuscript entitled “MicroRNA-199a-5p attenuates blood-brain barrier disruption following ischemic stroke by regulating PI3K/Akt signaling pathway”. (ID: PONE-D-24-00772). Those comments are all valuable and very helpful for revising and improving our paper, as well as the important guiding significance to the research. We have studied comments carefully and have made correction which we hope meet with approval. Revised portion are marked in red in the paper. The main corrections in the paper and the responds to the reviewer’s comments are as following: Responds to the reviewer’s comments: 1.A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'. Response: A separate file labeled 'Revised Manuscript with Track Changes' has been uploaded. 2.Please state what role the funders took in the study. If the funders had no role, please state: ""The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript." Response : The funders "National Natural Science Foundation of China（No.81273609)" had a role in study design and preparation of the manuscript. The funders " Natural Science Foundation of Hebei Province (No. H2023206115)" had a role in data collection and analysis, decision to publish. 4. For example, authors should submit the following data: The values behind the means, standard deviations and other measures reported; The values used to build graphs; The points extracted from images for analysis. Authors do not need to submit their entire data set if only a portion of the data was used in the reported study. Response : The data has been upload as a separate file labeled " date of graphs and figures" has been uploaded. Reviewer #1: In this manuscript, the authors studied the preventive and therapeutic effects of miR-199a-5p through PI3K/Akt pathway on ischemia stroke. On this basis, they further investigated the role of miR-199a-5p in BBB. Despite some highlights, this paper has a number of shortcomings, such as the logic of manuscript, the data etc, and page numbers and line numbers are missing. Response: Considering the Reviewer’s suggestion, we have added page numbers and line numbers. 1.The introduction lacks logic. Especially, it did not describe the relationship between miRNA and BBB. Please describe in detail. Response: thank you for your suggestion. We have revised the introduction and described the relationship between miRNA and BBB. 2.Where are the tables? I can’t find them. Neurological function scores are better presented as bar graphs than table. Response: The tables were uploaded as separate file. Neurological function scores have been presented as bar graphs. 3.The improvement effect of miRNA on MCAO was only evaluated with neurological function score. It should add the data of infarct size and pathological status. Response: thank you for your suggestion. In the present study, we primarily investigated the protective effect of miR-199a-5p on the BBB in MCAO rats through regulating PI3K/Akt signaling pathway. Thus, the measurement of cerebral infarction volume was not considered in the study design. 4.Although this study provides detailed evidence of the efficacy of CC, it does not provide in-depth mechanistic validation. Response: In our study, the efficacy of CC was not validated, and it was not mentioned in the manuscript. 5.There is no logic in the results section. It should be showed from effect to mechanism. Response: In the results section, the results of the experiment were presented, and the relevant mechanisms are presented in the discussion section. 6.Fig. 6A should add the merged figure. Response: In Fig. 6A, the left side showed the staining of neuronal nuclei, and the right side showed the result of NEUN+/TUNEL+ staining, which was the merge figure. 7.The discussion lacks logic. Moreover, miR-199a-5p, as the key to this paper, has not been highlighted in the discussion. Response: Thank you for the reviewer's comments. As per the reviewer's recommendations, the discussion has been revised. Special emphasis was placed on miR-199a-5p. 8.Another obvious problem with this paper is lack of sufficient explanation of the results. More explanations on them seem necessary and helpful to readers. Response: Thank you for the reviewer's suggestion. In the discussion section, a detailed explanation of the results was provided. 9.The first paragraph of the discussion requires a brief summary of the research results. Response: Thank you for the reviewer's comments. A brief summary of the research results was presented in the first paragraph of the discussion section. 10. It is noted that your manuscript needs careful editing by someone with expertise in technical English editing paying particular attention to English grammar, spelling, and sentence structure so that the goals and results of the study are clear to the reader. Response: We appreciate the reviewer's suggestions. The manuscript has been revised by professionals to correct the grammar, tense, and sentence structure in the text, making it easier to read. Reviewer #2: This is a well-organized study exploring the association of MicroRNA-199a-5p attenuates BBB disruption following ischemic stroke. Major: The concept of the study is not novel and the topic itself is important, however, the lack of clear rationale and mechanistic assessments reduces the scientific value of the paper. The English used in the manuscript is understandable but the text needs to be edited by a native speaker. Spelling, grammar, and syntax errors are present in the text. In the study implications, novelty aspects of the study and limitations are not indicated. Response: We appreciate the reviewer's suggestions. The findings of the present study indicated that miR-199a-5p inhibit inflammation following ischemic stroke by activating the PI3K/Akt signaling pathway, reduced neuronal apoptosis in the ischemic penumbra, and upregulated Claudin-5 and VEGF to preserve the integrity of the BBB. miR-199a-5p will be anticipated to serve as a novel therapeutic target for cerebral ischemia. The manuscript has been revised by professionals to correct the grammar, tense, and sentence structure in the text, making it easier to read. Reviewer #2: This is a well-organized study exploring the association of MicroRNA-199a-5p attenuates BBB disruption following ischemic stroke. Minor: please correct abbreviations - for example, in the introduction, CNS has already been used before, and TJs, not TJS - access to food and not diet -there are some misleading sentences in the text for example that miR-199a-5p was a main factor in the process of cerebral ischemia - introduction Response: We appreciate the reviewer's attention to detail. We have made revisions one by one according to the suggestions. Attachments Attachment Submitted filename: Response to Reviewers.docx https://doi.org/10.1371/journal.pone.0306793.r002
18 Jun 2024 Decision Letter - Francesco Sessa, Editor PONE-D-24-00772R1MicroRNA-199a-5p attenuates blood-brain barrier disruption following ischemic stroke by regulating PI3K/Akt signaling pathwayPLOS ONE Dear Dr. NI, 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. ============================== ACADEMIC EDITOR: Despite Reviewer#1 rejecting the manuscript, in my opinion, the authors improved the manuscript substantially. I suggest revisiting it and inserting a separate section with the study limitations (the authors should insert the limitations described by reviewer#1). Please, insert it before conclusion: in this way, it could be published. ============================== Please submit your revised manuscript by Aug 02 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. Please include the following items when submitting your revised manuscript: A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'. A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'. An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'. If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter. If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols. We look forward to receiving your revised manuscript. Kind regards, Francesco Sessa, Ph.D., MS Academic Editor PLOS ONE Journal Requirements: Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice. Additional Editor Comments: Despite Reviewer#1 rejecting the manuscript, in my opinion, the authors improved the manuscript substantially. I suggest revisiting it and inserting a separate section with the study limitations (the authors should insert the limitations described by reviewer#1: "Although the authors have made numerous modifications for the manuscript, the current data do not support the conclusions. The data of infarct size and pathological status are important index for evaluating ischemic stroke. They are not provided."). [Note: HTML markup is below. Please do not edit.] Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation. Reviewer #1: (No Response) Reviewer #2: All comments have been addressed ******** 2. 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: Partly Reviewer #2: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: I Don't Know Reviewer #2: Yes ****** 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: No 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: Although the authors have made numerous modifications for the manuscript, the current data do not support the conclusions. The data of infarct size and pathological status are important index for evaluating ischemic stroke. They are not provided. 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: No ******** [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.0306793.r003
Revision 2
21 Jun 2024 Author Response The study limitations have been inserted before conclusion.Xiaoqing Wang was listed in the authorship. Attachments Attachment Submitted filename: Response to Reviewers.docx https://doi.org/10.1371/journal.pone.0306793.r004
25 Jun 2024 Decision Letter - Francesco Sessa, Editor MicroRNA-199a-5p attenuates blood-brain barrier disruption following ischemic stroke by regulating PI3K/Akt signaling pathway PONE-D-24-00772R2 Dear Dr. NI, 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, Francesco Sessa, Ph.D., MS Academic Editor PLOS ONE Additional Editor Comments (optional): The authors modified the manuscript following the reviewers' suggestions. Reviewers' comments: https://doi.org/10.1371/journal.pone.0306793.r005
Formally Accepted
27 Jun 2024 Acceptance Letter - Francesco Sessa, Editor PONE-D-24-00772R2 PLOS ONE Dear Dr. NI, 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 Lecturer Francesco Sessa Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0306793.r006

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