Nucleolar sequestration of cannabinoid type-2 receptors in triple-negative breast cancer cells

Linley P. Prado-Celis; Rodrigo Zamora-Cárdenas; Javier Alamilla; Enrique A. Sánchez-Pastor; Tania Ferrer; Eloy G. Moreno-Galindo; Ricardo A. Navarro-Polanco

doi:10.1371/journal.pone.0323554

Peer Review History

Original SubmissionOctober 22, 2024
22 Oct 2024 Author Response Attachments Attachment Submitted filename: Responses to reviewers R1.docx https://doi.org/10.1371/journal.pone.0323554.r001
26 Dec 2024 Decision Letter - Muhammad Ahmad, Editor PONE-D-24-47936Nlucleolar Sequestration of Cannabinoid Type-2 Receptor in Triple-Negative Breast Cancer CellsPLOS ONE Dear Dr. Navarro-Polanco, 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 09 2025 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. 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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. PLOS requires an ORCID iD for the corresponding author in Editorial Manager on papers submitted after December 6th, 2016. Please ensure that you have an ORCID iD and that it is validated in Editorial Manager. To do this, go to ‘Update my Information’ (in the upper left-hand corner of the main menu), and click on the Fetch/Validate link next to the ORCID field. This will take you to the ORCID site and allow you to create a new iD or authenticate a pre-existing iD in Editorial Manager. 3. Thank you for stating the following financial disclosure: This work was funded by Consejo Nacional de Humanidades, Ciencia y Tecnologia, Mexico: to R.A.N-P., E.G.M-G., and J.A. (Grant No. FC2015-1-121) and Infrastructure Grant No. 321696. L.P.P-C. and R.Z-C. were supported by Doctoral Fellowships (No. CVU 933434 and 618681, respectively) from CONAHCYT, Mexico. 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. 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. 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 Reviewer #3: Yes Reviewer #4: Yes ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: Yes Reviewer #3: Yes Reviewer #4: N/A ****** 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 Reviewer #3: No Reviewer #4: No ****** 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 Reviewer #3: Yes Reviewer #4: 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: Thank you so much for your responses to the Reviewers' comments. I have no further concerns at the moment. Congrats on your work. I believe that this article is now acceptable for publication in Plos One. Reviewer #2: The current version of the paper has been already reviewed by three other reviewers in the first round of the review process and the authors addressed all the comments of the previous round properly and the paper can be accepted for publication. Reviewer #3: This study investigates the expression and subcellular localization of the cannabinoid type-2 receptor (CB2R) in triple-negative breast cancer (TNBC) cell lines at different stages of disease progression and compares them to a non-tumoral mammary epithelial cell line. The authors demonstrate that CB2R is significantly overexpressed in TNBC cells and predominantly accumulates in the nucleoli. Interestingly, activating CB2R with a specific agonist (HU-308) redistributes the receptor away from the nucleoli to the nucleoplasm and cytoplasm, and this redistribution is accompanied by reduced cell migration and proliferation. The authors propose that nucleolar sequestration of CB2R could serve as a diagnostic marker and potentially influence TNBC progression. The work is technically sound, well-reported, and potentially impactful for TNBC research. The authors should address the points about data accessibility, provide a bit more mechanistic speculation or references, and refine the discussion on the translational implications. After these minor improvements, the manuscript would be suitable for publication in PLOS ONE. A number of minor revisions regarding discussion part are suggested before to proceed publishing: 1. While the study reveals nucleolar accumulation of CB2R, the mechanism underlying this sequestration remains unclear. Elaborating on potential nucleolar retention signals or interacting proteins would strengthen the manuscript’s impact. This may not be essential for publication, but providing a brief discussion of possible mechanisms or future directions would be helpful. 2. Although HU-308 reduces nucleolar CB2R and decreases proliferation and migration, it appears more effective in metastatic MDA-MB-231 cells than in early-stage HCC-1395 cells. A brief exploration or discussion as to why this differential response occurs would be valuable. 3. Additional discussion on the potential clinical implications or how one might translate these findings into diagnostic or therapeutic approaches could strengthen the relevance. 4. The manuscript would benefit from a clear statement on data availability, including any raw images or numerical data. This will support reproducibility and compliance with PLOS ONE’s policies 5. In Figure legends, more details on sample sizes and exact statistical tests used for each comparison would help clarify the results. Reviewer #4: What is conclusion of that study?? Elaborate the statistical model used? There is need to define the study design briefly? Image J is used where it is impleneted in fig ….? Go through these articles to support the manuscript and further understanding https://www.pvj.com.pk/pdf-files/23-430.pdf https://www.pvj.com.pk/pdf-files/24-471.pdf https://pvj.com.pk/pdf-files/23-052.pdf https://www.ijvets.com/pdf-files/24-427.pdf ****** 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: Yes: Alex Mabou Tagne Reviewer #2: No Reviewer #3: No Reviewer #4: 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.0323554.r002
Revision 1
10 Feb 2025 Author Response RESPONSES TO THE REVIEWERS’ COMMENTS We thank the reviewers, both the previous and the new ones, for their comments on our study and the suggestions to improve our MS. As in the preceding resubmission, changes in the MS are shown in red font, while responses (R) to your specific comments are denoted in blue font. Reviewer #1: Thank you so much for your responses to the Reviewers' comments. I have no further concerns at the moment. Congrats on your work. I believe that this article is now acceptable for publication in Plos One. Reviewer #2: The current version of the paper has been already reviewed by three other reviewers in the first round of the review process and the authors addressed all the comments of the previous round properly and the paper can be accepted for publication. Reviewer #3: This study investigates the expression and subcellular localization of the cannabinoid type-2 receptor (CB2R) in triple-negative breast cancer (TNBC) cell lines at different stages of disease progression and compares them to a non-tumoral mammary epithelial cell line. The authors demonstrate that CB2R is significantly overexpressed in TNBC cells and predominantly accumulates in the nucleoli. Interestingly, activating CB2R with a specific agonist (HU-308) redistributes the receptor away from the nucleoli to the nucleoplasm and cytoplasm, and this redistribution is accompanied by reduced cell migration and proliferation. The authors propose that nucleolar sequestration of CB2R could serve as a diagnostic marker and potentially influence TNBC progression. The work is technically sound, well-reported, and potentially impactful for TNBC research. The authors should address the points about data accessibility, provide a bit more mechanistic speculation or references, and refine the discussion on the translational implications. After these minor improvements, the manuscript would be suitable for publication in PLOS ONE. A number of minor revisions regarding discussion part are suggested before to proceed publishing: 1. While the study reveals nucleolar accumulation of CB2R, the mechanism underlying this sequestration remains unclear. Elaborating on potential nucleolar retention signals or interacting proteins would strengthen the manuscript’s impact. This may not be essential for publication, but providing a brief discussion of possible mechanisms or future directions would be helpful. R = Yes, you are right that including the mechanism by which CB2R is sequestered in the nucleolus of cancerous cells would increase the manuscript’s impact, although the precise mechanism for the nucleolar sequestration is unknown, especially for a GPCR, being this work the first report on this topic. Therefore, we don´t feel comfortable speculating (even a bit) about a virtually unknown mechanism. In the Discussion, we added two lines mentioning this limitation (lines 6-8, page 17). We hope that this point of view is not problematic for you. 2. Although HU-308 reduces nucleolar CB2R and decreases proliferation and migration, it appears more effective in metastatic MDA-MB-231 cells than in early-stage HCC-1395 cells. A brief exploration or discussion as to why this differential response occurs would be valuable. R = In the Discussion section, we delineated a plausible reasoning for the more pronounced impact of HU-308 on MDA-MB-231 cells, focusing on the removal of CB2R from the nucleolus (lines 12, 14-17, page 17). 3. Additional discussion on the potential clinical implications or how one might translate these findings into diagnostic or therapeutic approaches could strengthen the relevance. R = Done (lines 13-15, page 18). 4. The manuscript would benefit from a clear statement on data availability, including any raw images or numerical data. This will support reproducibility and compliance with PLOS ONE’s policies R = We included the data availability statement in the document along with an Excel file in the Supporting Information section with all the raw data (if I'm not mistaken, this file can be observed after the figures in the Metadata Journal file). 5. In Figure legends, more details on sample sizes and exact statistical tests used for each comparison would help clarify the results. R = The statistical test and the sample size are indicated in the Figure legends. Reviewer #4: What is conclusion of that study?? R = Thanks for your observation. We added a conclusion at the end of the Discussion. To do this, we had to modify a little bit the first lines of the previous paragraph (lines 7-8, page 18). Elaborate the statistical model used? R = In the Statistical Analysis section, we are mentioning the adequate central and dispersion values according to the distribution of data, as verified with two normality tests (Shapiro–Wilk and Kolmogorov-Smirnov tests). We then applied parametric and non-parametric statistical tests/models, as required. Moreover, the sample size and the specific statistical test used are indicated in the Figure legends. There is need to define the study design briefly? R = Part of the study is descriptive and the part of the agonist’s effect is experimental. However, due to the basic nature/profile of the study, we judge that is not really necessary to mention this issue in the MS. We hope that there is no problem about it. Image J is used where it is impleneted in fig ….? R = ImageJ was used for the analysis of all images, as commented in Methods. Go through these articles to support the manuscript and further understanding https://www.pvj.com.pk/pdf-files/23-430.pdf https://www.pvj.com.pk/pdf-files/24-471.pdf https://pvj.com.pk/pdf-files/23-052.pdf https://www.ijvets.com/pdf-files/24-427.pdf R = Dear Reviewer, with all due respect, we tried hard to include the findings of the papers you suggest. Despite these references deal with potential anti-tumoral agents for breast cancers, unfortunately, we could not find a direct relationship with the core topics of our work: TNBC, cannabinoid receptors and nucleolar sequestration. Attachments Attachment Submitted filename: Responses to Reviewers R2.docx https://doi.org/10.1371/journal.pone.0323554.r003
12 Mar 2025 Decision Letter - Muhammad Ahmad, Editor PONE-D-24-47936R1Nlucleolar Sequestration of Cannabinoid Type-2 Receptor in Triple-Negative Breast Cancer CellsPLOS ONE Dear Dr. Navarro-Polanco, 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 Apr 26 2025 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, Muhammad Ahmad 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 #2: (No Response) Reviewer #3: 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 #2: (No Response) Reviewer #3: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #2: (No Response) Reviewer #3: 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 #2: (No Response) Reviewer #3: 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 #2: (No Response) Reviewer #3: 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 #2: The authors of the paper have fully addressed all the concerns of the previous round, I do not have any further comments. Reviewer #3: Thank you for your revisions. I appreciate the efforts made to address the comments. 1-I understand your reasoning regarding the mechanism of CB2R nucleolar sequestration and agree that acknowledging this limitation in the discussion is a reasonable approach. 2-The additional discussion on the differential response of the cells provide valuable context. 3-The expanded discussion on the potential clinical implications strengthens the relevance of the findings. 4-Data has already been provided in the supplementary data. The statement is also helpful. With these revisions, I find the manuscript suitable for publication. I have no further concerns. Best regards, ****** 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 #2: No Reviewer #3: 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.0323554.r004
Revision 2
27 Mar 2025 Author Response We thank to the editor for his comments on our study and the suggestions to improve our MS. As in the preceding resubmission, changes in the MS are shown in red font, while responses (R) to your specific comments are denoted in blue font. 1) The keywords should not be included in the title. Please revise accordingly. R. Done 2) The beginning of the second paragraph of introduction is not appropriate. Consider rewording for better clarity and coherence. R. Done 3) Improve the overall English language and revise for better readability. R. Done 4) Check for any grammatical mistakes and correct them. R. We have already revised and corrected the grammar of the manuscript in more detail. Attachments Attachment Submitted filename: Response to Editor.docx https://doi.org/10.1371/journal.pone.0323554.r005
10 Apr 2025 Decision Letter - Muhammad Ahmad, Editor Nucleolar sequestration of cannabinoid type-2 receptor in triple-negative breast cancer cells PONE-D-24-47936R2 Dear Dr. Navarro-Polanco, 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, Muhammad Ahmad Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: https://doi.org/10.1371/journal.pone.0323554.r006
Formally Accepted
Acceptance Letter - Muhammad Ahmad, Editor PONE-D-24-47936R2 PLOS ONE Dear Dr. Navarro-Polanco, 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 You will receive further instructions from the production team, including instructions on how to review your proof when it is ready. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few days 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 Mr. Muhammad Ahmad Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0323554.r007

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