Ameliorative effects of Penthorum chinense Pursh on insulin resistance and oxidative stress in diabetic obesity db/db mice

Jilei Hu; Leyu Zheng; Xi Fan; Hongmei Lang; Huibo Xie; Ning Lin

doi:10.1371/journal.pone.0311502

Peer Review History

Original SubmissionMay 10, 2024
28 Jun 2024 Decision Letter - Mehran Rahimlou, Editor PONE-D-24-18781Ameliorative Effects of Penthorum chinense Pursh on Insulin Resistance and Oxidative Stress in diabetic obesity db/db micePLOS ONE Dear Dr. Hu, 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 10 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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Comments from PLOS Editorial Office: We note that one or more reviewers has recommended that you cite specific previously published works. As always, we recommend that you please review and evaluate the requested works to determine whether they are relevant and should be cited. It is not a requirement to cite these works. We appreciate your attention to this request. Additional Editor Comments: Dear Dr. Jilei Hu Based on the comments received from the reviewers regarding this manuscript, we request you to revise your manuscript based on the comments raised by the reviewers. Many thans [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 ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: Yes Reviewer #3: 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 Reviewer #3: 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 Reviewer #3: 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.A few grammatical and typographical errors noted. For instance, ANIMALS EXPERIMENT, instead of ANIMAL EXPERIMENTS 2. De Ritis ratio and Ferritin could have been included 3. The authors are advised to compute lipid ratios, in view of their link with both diabetes mellitus and steatosis 4. Was the ELISA kit for HbA1c ,a high sensitivity and specificity one with minimal cross reactivity?? Why did the authors not use HPLC ??? Reviewer #2: 1. Language should be improved and spelling mistakes should be corrected. 2. Please abbreviate the text at first instance. 3. Give 2-3 lines about current status of diabetes at global level. Brauer, Michael, Roth, Gregory A., Aravkin, Aleksandr Y., Zheng, Peng, Abate, Kalkidan Hassen, Abate, Yohannes Habtegiorgis, Abbafati, Cristiana, Kavita Munjal et al., 2024. Global burden and strength of evidence for 88 risk factors in 204 countries and 811 subnational locations, 1990–2021: a systematic analysis for the Global Burden of Disease Study 2021. The Lancet. 403, 2162-2203. https://doi.org/10.1016/S0140-6736 (24)00933-4. Gauttam, V., Munjal, K., Mujwar, S., Sawale, J., Rohilla, M., Gupta, S. 2022. Comparative Study of Developed Formulation and Market Formulation for Antidiabetic Potential in Alloxan Induced Diabetic Wistar Rats. Journal of Young Pharmacists. 2022; 14(4), 387-393. Reviewer #3: In this manuscript, the authors demonstrated that PCP significantly alleviated hyperglycemia, hyperinsulinemia, hyperlipidemia, and obesity, inhibited hepatic oxidative stress, and enhanced hepatic glucose transport in T2DM mice. Generally, the paper is well written and the results are of some scientific significance. I recommend this paper to be accepted after minor revision. Minor points: 1. The inter-group significance shown in the picture is inconsistent with the description in the text. For example, in the result section ‘PCP improved parameters related to hyperglycemia and IR in db/db mice’ (Line 186), according to the figure, it should be ‘P<0.01’? 2. In Fig5-B, the significance may be wrong, especially HPCP Group. Please check through the manuscript to avoid these errors.”. ****** 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: A.R.SRINIVASAN Reviewer #2: Yes: Dr. Kavita Munjal 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. Attachments Attachment Submitted filename: Accept after minor revision.docx https://doi.org/10.1371/journal.pone.0311502.r001
Revision 1
3 Aug 2024 Author Response Dear Editor and Reviewers, We sincerely thank you for your valuable feedback which helped to improve the quality of our manuscript entitled “Ameliorative Effects of Penthorum chinense Pursh on Insulin Resistance and Oxidative Stress in diabetic obesity db/db mice” (Manuscript ID: PONE-D-24-18781). We have considered your comments word by word and have made revisions based on your suggestions question by question. We have amended the format according to the Journal Requirements, and the details can be found in the flie of Point-by-point response to reviewers and editors.The reviewers’ comments are listed in blue italics and specific concerns have been numbered. Our response is given in normal font and changes/additions to the manuscript are marked in red. The main amendments in the paper and the responses to your comments are listed as follows: For reviewer 1# 1. A few grammatical and typographical errors were noted. For instance, ANIMALS EXPERIMENT, instead of ANIMAL EXPERIMENTS. Response: Thank you for your meticulousness. We felt sorry about this low-grade mistake and the amendment is in red. 2. De Ritis ratio and Ferritin could have been included. Response: Thank you for your advice. Penthorum chinense Pursh (PCP) is widely utilized in China to treat a variety of liver diseases. Previous studies have demonstrated that the levels of aspartate aminotransferase (AST) and alanine aminotransferase (ALT) were ameliorated in a dose-dependent manner by PCP [1-4]. Therefore, we did not measure liver function-related indicators in this study and unfortunately, we were unable to calculate the De Ritis ratio either. As for ferritin, there is no published literature report on the effect of PCP on it. However, our team's ongoing but unpublished study suggests that total flavonoids of PCP were able to significantly attenuate liver injury of iron-overloaded rats by up-regulating the expression of divalent metal ion transporter protein 1 and transferrin receptor 1. Of course, if we can get new funds, we shall carry out more experiments to dig into the effect of PCP on ferritin. 3. The authors are advised to compute lipid ratios, because of their link with both diabetes mellitus and steatosis. Response: Thank you for your advice. T2DM patients often present with characteristic plasma lipid and lipoprotein abnormalities, including low HDL-C, high LDL-C, and elevated TC and TG levels [5], which is consistent with our findings. Considering the reviewer’s suggestion, we further analyzed the lipid ratio parameters, including TC/HDL-C, TG/HDL-C, and LDL-C/HDL-C, that considered could predict the risk of T2DM complications by prior studies [6], especially for coronary heart disease. The results of lipid ratio parameters are shown in Fig 2G-I. Those in the NC, including TC/HDL-C, TG/HDL-C, and LDL-C/HDL-C were significantly higher than those in the db/db mice (P<0.01). The values of TG/HDL-C in the MPCP and HPCP were significantly lower than those in the MC (P<0.05), while those of LPCP were not significantly different from those of the MC. However, the values of TG/HDL-C in the LPCP were significantly higher than those in the HPCP (P<0.05). All doses of PCP treatment decreased the values of LDL-C/HDL-C in a dose-response relationship (P<0.05), demonstrated by significantly lower values of LDL-C/HDL-C in the HPCP than those in the LPCP and MPCP (P<0.01). 4. Was the ELISA kit for HbA1c, a high-sensitivity and specificity one with minimal cross-reactivity? Why did the authors not use HPLC? Response: Thank you for your question. According to the literature, various methods developed for HbA1c examination include immunoassay, boronated affinity, enzymatic, capillary electrophoresis, and Ion-Exchange High-Performance Liquid Chromatography (IE-HPLC) [7], and each has its advantages and limitations. Currently, the two most used methods for HbA1c detection are IE-HPLC and immunoassay, and the results of them are in strong agreement in most cases. In addition to its advantages in detecting HbA1c, IE-HPLC methods can also detect other types of hemoglobin and the presence of hemoglobin variants, which are widely used in clinical practice. However, we did not choose IE-HPLC due to its high price. ELISA kits working on the principle of immunoassay, are one of the methods with high sensitivity, stable efficacy, and low price for the determination of HbA1c, which are widely used in animal experiments [8]. In summary, we finally chose the ELISA kits to measure the HbA1c levels of db/db mice. For reviewer 2#: 1. Language should be improved and spelling mistakes should be corrected. Response: Thank you for your suggestion. We have invited a native English speaker to help polish our manuscript, and we hope the revised manuscript will be acceptable to you. 2. Please abbreviate the text at the first instance. Response: Thank you for your suggestion. We felt sorry about this low-grade mistake and now all full names with their abbreviations have been added when they first appear. The amendment is in red. 3. Give 2-3 lines about the status of diabetes at the global level. Response: Thank you for providing valuable references. We have checked the literature carefully and added more description about the status of diabetes at the global level in the INTRODUCTION part of the revised manuscript (Lines 57-60). For reviewer 3#: 1. The inter-group significance shown in the picture is inconsistent with the description in the text. For example, in the result section ‘PCP improved parameters related to hyperglycemia and IR in db/db mice’ (Line 186), according to the figure, it should be ‘P<0.01’. Response: Thank you for your meticulousness. We felt sorry about this low-grade mistake and the amendment is in red. 2. In Fig5B, the significance may be wrong, especially HPCP Group. Please check through the manuscript to avoid these errors. Response: Thank you for your meticulousness. We have checked and reanalyzed the raw data and unfortunately, the results and significance were real. As shown in Fig 5B, when compared to the MC, the relative expression of GCK protein increased in the LPCP, HPCP (P < 0.05), and MPCP (P < 0.01), respectively. However, there was no significant difference in multiple comparisons between the three PCP-treatment groups. We considered the following two possible reasons. Firstly, a smaller p-value does not mean that the difference is larger, only that more reason to think that there is a difference between the two groups. In this study, the relative expression of GCK protein in the MPCP and HPCP was significantly higher than the MC, but the p-value was smaller in the MPCP, which only means that there was more reason to think that the MPCP is different from the MC. Secondly, the above results may be due to the relatively small sample size of the experiment. Finally, we would like to express our thanks again for your reviews and guidance on our manuscript. We sincerely hope that with the help of your knowledge, we can complete an excellent paper and we also hope our paper can be published in your journal. Thank you and best regards. Yours Sincerely, Ning Lin Clinical Nutrition, The General Hospital of Western Theater Command, Sichuan, Chengdu 610083, China. Email: helenmedic@yeah.net August 3, 2024 Reference 1. Du YC, Lai L, Zhang H, Zhong FR, Cheng HL, Qian BL, et al. Kaempferol from Penthorum chinense Pursh suppresses HMGB1/TLR4/NF-κB signaling and NLRP3 inflammasome activation in acetaminophen-induced hepatotoxicity. Food & function. 2020;11(9):7925-34. 2. Jiang Y, Zhong M, Zhan H, Tao X, Zhang Y, Mao J, et al. Integrated strategy of network pharmacology, molecular docking, HPLC-DAD and mice model for exploring active ingredients and pharmacological mechanisms of Penthorum chinense Pursh against alcoholic liver injury. Journal of ethnopharmacology. 2022;298:115589. 3. Wang S, Li W, Liu W, Yu L, Peng F, Qin J, et al. Total flavonoids extracted from Penthorum chinense Pursh mitigates CCl(4)-induced hepatic fibrosis in rats via inactivation of TLR4-MyD88-mediated NF-κB pathways and regulation of liver metabolism. Frontiers in pharmacology. 2023;14:1253013. 4. Zhang H, Cui X, Liu W, Xiang Z, Ye JF. Regulation of intestinal microflora and metabolites of Penthorum chinense Pursh on alcoholic liver disease. Frontiers in pharmacology. 2023;14:1331956. 5. Bahiru E, Hsiao R, Phillipson D, Watson KE. Mechanisms and Treatment of Dyslipidemia in Diabetes. Current cardiology reports. 2021;23(4):26. 6. Gu X, Yang X, Li Y, Cao J, Li J, Liu X, et al. Usefulness of Low-Density Lipoprotein Cholesterol and Non-High-Density Lipoprotein Cholesterol as Predictors of Cardiovascular Disease in Chinese. The American journal of cardiology. 2015;116(7):1063-70. 7. Rhea JM, Molinaro R. Pathology consultation on HbA(1c) methods and interferences. American journal of clinical pathology. 2014;141(1):5-16. 8. Huang D, Jiang Y, Chen W, Yao F, Huang G, Sun L. Evaluation of hypoglycemic effects of polyphenols and extracts from Penthorum chinense. Journal of ethnopharmacology. 2015;163:256-63. Attachments Attachment Submitted filename: Point-by-point response to reviewers and editors.docx https://doi.org/10.1371/journal.pone.0311502.r002
20 Sep 2024 Decision Letter - Mehran Rahimlou, Editor Ameliorative Effects of Penthorum chinense Pursh on Insulin Resistance and Oxidative Stress in diabetic obesity db/db mice PONE-D-24-18781R1 Dear Dr. Jilei Hu , 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. 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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 #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 #1: Yes Reviewer #3: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes 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 #1: Yes 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 #1: Yes 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 #1: Ameliorative Effects of Penthorum chinense Pursh on Insulin Resistance and Oxidative Stress in diabetic obesity db/db mice is a sound attempt. More light can be thrown by associating the markers of oxidative stress with the available and objective indicators of insulin sensitivity/insulin resistance, both dependent and independent of lipid status Reviewer #3: The authors have made enough revisions and responses. The manuscript can be accepted in present form. ****** 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: Yes: A.R.Srinivasan @ Vellore A.R.Srinivasan Reviewer #3: No ******** https://doi.org/10.1371/journal.pone.0311502.r003
Formally Accepted
27 Sep 2024 Acceptance Letter - Mehran Rahimlou, Editor PONE-D-24-18781R1 PLOS ONE Dear Dr. Hu, 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. Mehran Rahimlou Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0311502.r004

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