Changes in gene expression of cervical collagens, metalloproteinases, and tissue inhibitors of metalloproteinases after partial cervical excision-induced preterm labor in mice

Hyun Chul Jeong; Ho Yeon Kim; Hee Youn Kim; Eun-Jin Wang; Ki Hoon Ahn; Min-Jeong Oh; Byung Min Choi; Hai-Joong Kim

doi:10.1371/journal.pone.0250108

Peer Review History

Original SubmissionNovember 24, 2020
19 Jan 2021 Decision Letter - Carlos Zaragoza, Editor PONE-D-20-36937 Changes in gene expression of cervical collagens, metalloproteinases, and tissue inhibitors of metalloproteinases after partial cervical excision-induced preterm labor in mice PLOS ONE Dear Dr. Ahn, 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 Feb 14 2021 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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Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols We look forward to receiving your revised manuscript. Kind regards, Carlos Zaragoza, Ph.D. Academic Editor PLOS ONE Journal Requirements: When submitting your revision, we need you to address these additional requirements. 1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf 2. We note that you have indicated that data from this study are available upon request. 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We note that you have provided funding information that is not currently declared in your Funding Statement. However, funding information should not appear in the Acknowledgments section or other areas of your manuscript. We will only publish funding information present in the Funding Statement section of the online submission form. Please remove any funding-related text from the manuscript and let us know how you would like to update your Funding Statement. Currently, your Funding Statement reads as follows: "The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript." Please include your amended statements within your cover letter; we will change the online submission form on your behalf. [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: Partly 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: 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: To test the changes in the levels of cervical collagens MMPs and TIMPs, it would be convenient for the authors to perform immunoblot with the available samples. In the line 121, when the authors mention their previous studies in the methods, they should include a reference if they are published. When the authors explain the cervical excision, it would be convenient included if any kind of analgesia has been administered to the animals after the surgery. In the results, in line 175 authors should include the SD in the gestational periods. On the y-axis of the figures, authors should include the name of the collagenase, MMP or TIMs studied instead of fold. In figure 2 authors should check the letters off the graphs Reviewer #2: In the present manuscript the authors show the changes in the expression of cervical collagens, metalloproteinases and tissue inhibitors of metalloproteinases that are produced in a model of preterm labor induced by a partial cervical excision in mice. Thus, the authors justify that these components and proteins participate in the remodeling after a spontaneous premature birth after inflation added to a cervical excision. However, the study lacks of novelty. The comments are shown below. Introduction Minor comments - The authors should show that it is not only TIMPs that are regulating MMPS activity. There are other proteins that can participate in this signaling pathway, such as CD147, also known as EMMPRIN (Extracellular Matrix Metalloproteinase INducer). Line 94. - Paragraph staring from line 86 to 90 is necessary to remove it. Experimentation and research on humans are totally forbidden and does not need to be discussed. Methods - What is the concentration of LPS given to the mice? - Why was the administration of LPS done on the 16th day gestational? Results - Figure 2 shows graphically significant differences in the expression levels of MMP2 and TIMP-1 that the authors do not comment. - Why does the LPS group have a low n compared to the other groups? - Figure 2, the graphics are incorrectly listed - Due to the fact that there are a wide number of Metalloproteinases and TIMPs involved in remodeling processes in response to an injury, the authors should screen for these proteins (MMP-9, TIMP-2, MMP-13...) - To complete the study, the authors must show the protein expression of the MMPs through Western Blot and must also show the activity of these proteins using a Zymography - In relation to line 299 to 301, the authors should use for basic techniques like Hematoxylin/Eosin or Masson's Trichrome stain to show a change in the cervix ECM before/after excision ****** 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. 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Revision 1
24 Feb 2021 Author Response 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: Partly 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: 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) Response to Reviewer Reviewer #1: To test the changes in the levels of cervical collagens MMPs and TIMPs, it would be convenient for the authors to perform immunoblot with the available samples. � We truly aware of your critical advice. Immunoblot would make our data more understandable however we tried to quantify gene expression of cervical collagens, MMPs and TIMPs using our cervical excision mouse model. Now our team don’t have available samples because this project already ended. Spite of the absence of protein expression data, this study might be meaningful as a pilot study. This limitation has been inserted as a limitation in Discussion section. Thank you for your understanding. In the line 121, when the authors mention their previous studies in the methods, they should include a reference if they are published. � We added the reference of our prior experiment. � 11. Ahn KH, Jeong HC, Kim HY, Kang D, Hong SC, Cho GJ et al. Relationship between partial uterine cervical tissue excision and preterm birth: an experimental animal study. Am J Perinatol. 2017;34:1072–1077. When the authors explain the cervical excision, it would be convenient included if any kind of analgesia has been administered to the animals after the surgery. � For the cervical excision surgery, xylazine (Rompun®, Bayer, Toronto, Canada) is administered intravenously immediately before surgery. This information has been added in Method section. (Line 102-103) In the results, in line 175 authors should include the SD in the gestational periods. � As per comment, we have added the SD value in the gestational periods. On the y-axis of the figures, authors should include the name of the collagenase, MMP or TIMs studied instead of fold. � We included the name of the collagenase, MMP or TIMPs on the y-axis of the figures as suggested instead of fold. In figure 2 authors should check the letters off the graphs � We corrected as suggested in Figure 2. Reviewer #2: In the present manuscript the authors show the changes in the expression of cervical collagens, metalloproteinases and tissue inhibitors of metalloproteinases that are produced in a model of preterm labor induced by a partial cervical excision in mice. Thus, the authors justify that these components and proteins participate in the remodeling after a spontaneous premature birth after inflation added to a cervical excision. However, the study lacks of novelty. The comments are shown below. Introduction Minor comments - The authors should show that it is not only TIMPs that are regulating MMPS activity. There are other proteins that can participate in this signaling pathway, such as CD147, also known as EMMPRIN (Extracellular Matrix Metalloproteinase INducer). Line 94. � As per comment, we added EMMPRIN as a regulator of MMPs with a reference. � 8. Li K, Nowak RA. The role of basigin in reproduction. Reproduction. 2019 Sep 1:REP-19-0268.R1. - Paragraph staring from line 86 to 90 is necessary to remove it. Experimentation and research on humans are totally forbidden and does not need to be discussed.\\ � As per comment, we deleted sentences in line 86 to 90. Methods - What is the concentration of LPS given to the mice? � We gave 100 μg of LPS in each mice. We added more detailed explanation for volume of LPS concentration in Material and Methods section. - Why was the administration of LPS done on the 16th day gestational? � Preterm birth is defined before gestational day 18 in mouse therefore LPS induction is usually performed on gestational day 15-17 to induce preterm birth. In addition, this protocol using LPS induced preterm birth is usually performed on gestational day 15-17 in previous studies. Following reference shows similar protocol. � The Local and Systemic Immune Response to Intrauterine LPS in the Prepartum Mouse. Edey LF, O'Dea KP, Herbert BR, Hua R, Waddington SN, MacIntyre DA, Bennett PR, Takata M, Johnson MR. Biol Reprod. 2016 Dec;95(6):125. doi: 10.1095/biolreprod.116.143289. Epub 2016 Oct 19. Results - Figure 2 shows graphically significant differences in the expression levels of MMP2 and TIMP-1 that the authors do not comment. � We made comments on MMP2 and TIMP-1 in results line 167-173 as follows. � There were no significant differences in the expression of MMP-2 and TIMP-1 among the experimental groups, but MMP-2 expression showed an increasing trend in the partial cervical tissue excision, administration of LPS, and partial cervical tissue excision plus administration of LPS groups compared to the sham group. In addition, TIMP-1 expression did not show significant differences although its expression in the partial cervical tissue excision plus administration of LPS group was lower compared to the other groups. - Why does the LPS group have a low n compared to the other groups? � Thank you for your comment. To minimize the conditions affecting the experiment, mouse experiments were conducted at once. The mice were randomly assigned to one of four groups and distributed 10 mice per group. Mice was bred in the eighth week, and mice that were not pregnant for more than eight weeks were sacrificed. The LPS groups had fewer mice pregnant at week 8 compared to other groups. - Figure 2, the graphics are incorrectly listed � We corrected Figure 2. - Due to the fact that there are a wide number of Metalloproteinases and TIMPs involved in remodeling processes in response to an injury, the authors should screen for these proteins (MMP-9, TIMP-2, MMP-13...) � We appreciate suggestion on screening for MMP-9 and other MMPs and TIMPs which have been widely studied in abortion, preeclampsia, and preterm birth. We conducted this study to elucidate the function of MMP-2, MMP-7, MMP-14 and TIMP-1 which are closely related to Col4 and Col5 utilizing our cervical excision model. We focused on the Col4 and Col5 and related enzymes in this study. - To complete the study, the authors must show the protein expression of the MMPs through Western Blot and must also show the activity of these proteins using a Zymography � Thank you for your comment. Although the current study is focusing on the gene quantification of collagens, MMPs and TIMPs of partial cervical excision plus LPS, authors agree with the reviewer’s viewpoint. We addressed your points as a limitation in the Discussion line 284-285. - In relation to line 299 to 301, the authors should use for basic techniques like Hematoxylin/Eosin or Masson's Trichrome stain to show a change in the cervix ECM before/after excision � Thank you for your comment. In our study, the cervical excision and LPS injection is one treatment option, which is compared to sham group. Therefore, change in the collagen and its enzymes after the treatment (cervical excision and LPS injection as a whole) is important. We have a future plan for the study on ECM change before vs. periodic follow-up after excision. Your advice is commented as a limitation in the main text. 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. 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23 Mar 2021 Decision Letter - Carlos Zaragoza, Editor PONE-D-20-36937R1 Changes in gene expression of cervical collagens, metalloproteinases, and tissue inhibitors of metalloproteinases after partial cervical excision-induced preterm labor in mice PLOS ONE Dear Dr. Ahn, 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 07 2021 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: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols We look forward to receiving your revised manuscript. Kind regards, Carlos Zaragoza, Ph.D. 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. [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: All comments have been addressed 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: Yes Reviewer #2: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes 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: 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: Authors should check in line 117 of the new manuscript if the reference to the previous study is number 10 or 11 "The method of animal experimentation is described in our previous study". Reviewer #2: All comments have been addressed correctly. The authors have made the manuscript better and improved the quality of the work. ****** 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.0250108.r003
Revision 2
24 Mar 2021 Author Response Response to editor � Thank you for your positive decision. Response to reviewers Reviewer #1: Authors should check in line 117 of the new manuscript if the reference to the previous study is number 10 or 11 "The method of animal experimentation is described in our previous study". � As per your comment, we have corrected the number of the reference. (11 instead of 10) Reviewer #2: All comments have been addressed correctly. The authors have made the manuscript better and improved the quality of the work. � Thank you for your positive answer. Attachments Attachment Submitted filename: Response to editor and reviewers.docx https://doi.org/10.1371/journal.pone.0250108.r004
31 Mar 2021 Decision Letter - Carlos Zaragoza, Editor Changes in gene expression of cervical collagens, metalloproteinases, and tissue inhibitors of metalloproteinases after partial cervical excision-induced preterm labor in mice PONE-D-20-36937R2 Dear Dr. Ahn, 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 for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, 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, Carlos Zaragoza, Ph.D. Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: https://doi.org/10.1371/journal.pone.0250108.r005
Formally Accepted
5 Apr 2021 Acceptance Letter - Carlos Zaragoza, Editor PONE-D-20-36937R2 Changes in gene expression of cervical collagens, metalloproteinases, and tissue inhibitors of metalloproteinases after partial cervical excision-induced preterm labor in mice Dear Dr. Ahn: I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department. 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 plosone@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 Carlos Zaragoza Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0250108.r006

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