Peer Review History

Original SubmissionNovember 6, 2019
Decision Letter - Aftab A. Ansari, Editor

PONE-D-19-30903

Evaluation of antiviral T cell responses and TSCM cells in volunteers enrolled in a phase I HIV-1 subtype C prophylactic vaccine trial in India

PLOS ONE

Dear Dr. Luke,

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.

   Both reviewers had concerns that the data do not in fact support the conclusions as stated. Both reviewers also had concerns with regards to the techniques being utilized and the need for some additional studies to confirm the conclusions reached by the authors. This manuscript therefore requires some additional studies and, in addition, a need to address each of the concerns raised by the 2 reviewers.

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Aftab A. Ansari, PhD

Academic Editor

PLOS ONE

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

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Reviewer #1: Yes

Reviewer #2: Partly

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: No

**********

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Reviewer #1: No

Reviewer #2: Yes

**********

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Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Review Comments to the Author

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Reviewer #1: In this manuscript Ponnan et al., aims to evaluate an T cell responses and TSCM cells in volunteers enrolled in a phase I HIV-1 subtype C prophylactic vaccine trial in India during 2009-2010. Ponnan et al, hereby report novel findings where they interrogated vaccine induced responses and stem cell memory responses in volunteers who received an HIV-1 subtype C prophylactic vaccine candidate primed with ADVAX DNA and later followed by MVA boost versus either MVA alone or placebo. The results obtained in this study revealed that priming with ADVAX DNA followed with MVA boost versus MVA alone resulted in increased frequencies of peripheral CD8+ TSCM cells and augmented CD8+ T cell-mediated inhibition of replication of different HIV-1 clades. Even-though the manuscript is well written, and these finding may have have significance in the development of vaccines that are urgently needed by high risk populations. However, as stated, the true role of TSCM and actual changes that occur during HIV-1 infection is yet to be fully understood. Therefore, in this manuscript additional investigation is required to confirm the true functionality of CD8+ TSCM cells generated after successful HIV-1 subtype C prophylactic vaccine candidate + ADVAX DNA + MVA boost. Therefore, the manuscript lacks critical experiment such as by sorting CD8+TSCM (a) could they have superior virus inhibition following co-culture with autologous infected CD4+ T cells? (b) in comparison to more differentiated memory phenotypes, are there any differences in cytokine patterns in response to HIV-1 specific overlapping peptides? to make any conclusions on the role of TSCM cells in this prophylactic vaccine trial.

Reviewer #2: In this manuscript, Ponnan and colleagues characterized the phenotype of total CD4 and CD8 T cells, and the ability of in vitro expanded cells to inhibit HIV replication using cells obtained from a HIV vaccine study that was conducted in India many years ago. The authors conclude that cells from vaccinated individuals exhibit some HIV inhibition activity and vaccination induces Tscm cells. Overall, these results are not conclusive and there are some major issues with the analyses as described below.

1) Need to provide details for CD4 T cell infection assay and indicate the ratio of CD4 and CD8 T cells used for virus inhibition assays.

2) Fig 2 – virus inhibition activity is not conclusive. There are no P values and activity was observed even at prevaccination time point (Fig. 2A).

3) Figs 3-6: The data on characterization of different memory CD4 and CD8 T cells are not conclusive and significant for the following reasons. 1) These should be expressed as a percent of total lymphocytes or converted into absolute number to get some idea about the actual change in the number of these cells over time. Currently, they are presented as a percent of total CD4 or CD8 T cells. This is not appropriate. 2) These are total CD4 or CD8 T cells, not vaccine-specific T cells. 3) Where there is an increase, we don’t know if these are MVA or HIV-specific cells. 4) overall, the observed increases are small considering that these are total cells (not antigen-specific).

4) The authors need to correct for multiple comparisons for P values.

**********

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Reviewer #1: No

Reviewer #2: No

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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 us at figures@plos.org. Please note that Supporting Information files do not need this step.

https://doi.org/10.1371/journal.pone.0229461.r001
Revision 1
Author Response

Reviewer #1: In this manuscript Ponnan et al., aims to evaluate an T cell responses and TSCM cells in volunteers enrolled in a phase I HIV-1 subtype C prophylactic vaccine trial in India during 2009-2010. Ponnan et al, hereby report novel findings where they interrogated vaccine induced responses and stem cell memory responses in volunteers who received an HIV-1 subtype C prophylactic vaccine candidate primed with ADVAX DNA and later followed by MVA boost versus either MVA alone or placebo. The results obtained in this study revealed that priming with ADVAX DNA followed with MVA boost versus MVA alone resulted in increased frequencies of peripheral CD8+ TSCM cells and augmented CD8+ T cell-mediated inhibition of replication of different HIV-1 clades. Even-though the manuscript is well written, and these finding may have have significance in the development of vaccines that are urgently needed by high risk populations.

However, as stated, the true role of TSCM and actual changes that occur during HIV-1 infection is yet to be fully understood. Therefore, in this manuscript additional investigation is required to confirm the true functionality of CD8+ TSCM cells generated after successful HIV-1 subtype C prophylactic vaccine candidate + ADVAX DNA + MVA boost. Therefore, the manuscript lacks critical experiment such as by sorting CD8+TSCM (a) could they have superior virus inhibition following co-culture with autologous infected CD4+ T cells? (b) in comparison to more differentiated memory phenotypes, are there any differences in cytokine patterns in response to HIV-1 specific overlapping peptides? to make any conclusions on the role of TSCM cells in this prophylactic vaccine trial.

• We agree with the reviewer that single cell sorting of CD8+ Tscm cells and their analysis for HIV-1 peptide induced cytokine response as well as virus inhibition activity would be extremely interesting. However, we were not in a position to undertake such experiments due to the limited number of PBMC available for this study. As mentioned in the manuscript, this study has been carried out PBMC stored from volunteers who were vaccinated during the period 2009-2010. Using the limited number of cells that were available we studied several aspects of vaccine-induced cellular and humoral immune responses including polyfunctional T cells, T follicular helper cells, Regulatory T cells, memory T cells, Tscm cells, variable loop antibodies, neutralizing antibodies, virus inhibition activity, etc. We have previously published 2 manuscripts in PLOSone entitled “Induction of circulating T Follicular Helper cells and Regulatory T cells correlating with HIV-1 gp120 variable loop antibodies by a subtype C prophylactic vaccine tested in a Phase I trial in India” (https://doi.org/10.1371/journal.pone.0055831) and “Induction and maintenance of bi-functional (IFN-γ + IL-2+ and IL-2+ TNF-α+) T cell responses by DNA prime MVA boosted subtype C prophylactic vaccine tested in a Phase I trial in India” (https://doi.org/10.1371/journal.pone.0213911).

Reviewer #2: In this manuscript, Ponnan and colleagues characterized the phenotype of total CD4 and CD8 T cells, and the ability of in vitro expanded cells to inhibit HIV replication using cells obtained from a HIV vaccine study that was conducted in India many years ago. The authors conclude that cells from vaccinated individuals exhibit some HIV inhibition activity and vaccination induces Tscm cells. Overall, these results are not conclusive and there are some major issues with the analyses as described below.

1) Need to provide details for CD4 T cell infection assay and indicate the ratio of CD4 and CD8 T cells used for virus inhibition assays.

As suggested by the reviewer, we revisited our description of the VIA assay and the suggested details have been incorporated in the manuscript.

2) Fig 2 – virus inhibition activity is not conclusive. There are no P values and activity was observed even at pre vaccination time point (Fig. 2A).

The mean values of log10 reduction was compared at different time points within the placebo, Group A and Group B vaccinees for the 5 different viral clades, using Kruskal-Wallis test followed by subgroup analysis using Dunn’s multiple comparison test to identify differences between the three groups. For all analyses, differences were considered significant if p value was <0.05. The p values have been incorporated in Fig-2.

3) Figs 3-6: The data on characterization of different memory CD4 and CD8 T cells are not conclusive and significant for the following reasons.

• These should be expressed as a percent of total lymphocytes or converted into absolute number to get some idea about the actual change in the number of these cells over time. Currently, they are presented as a percent of total CD4 or CD8 T cells. This is not appropriate.

According to the reviewer's suggestion, we have reanalysed the FACS data and exported absolute count of different subsets of T cells and incorporated as supplementary tables in addition to the percentage frequency of immune cells.

• These are total CD4 or CD8 T cells, not vaccine-specific T cells.

3) Where there is an increase, we don’t know if these are MVA or HIV-specific cells..

4) overall, the observed increases are small considering that these are total cells (not antigen-specific).

We agree with the reviewer that the CD4 and CD8 T cells are not antigen specific. However, we found the significantly increased frequencies of different memory T cells in the vaccine recipients as compared to the placebo recipients. We therefore assume that the increase in immune cell subsets was vaccine induced.

4) The authors need to correct for multiple comparisons for P values.

As suggested by the reviewer we revisited statistical analysis. Since the study includes three groups of volunteers (Placebo, Group-A and Group-B) and different timepoints of vaccination, we used Kruskal-Wallis test to compare vaccine induced responses at different time points and followed it up with subgroup analysis using Dunn’s multiple comparison test to identify differences between the groups. This has been mentioned in the manuscript.

Attachments
Attachment
Submitted filename: Responce to the reviewers.docx
https://doi.org/10.1371/journal.pone.0229461.r002
Decision Letter - Aftab A. Ansari, Editor

PONE-D-19-30903R1

Evaluation of antiviral T cell responses and TSCM cells in volunteers enrolled in a phase I HIV-1 subtype C prophylactic vaccine trial in India

PLOS ONE

Dear Dr Luke,

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 see the minor comments I have posted in the comments to the authors. I would very much like the authors to address thie minor issue. Otherwise, as I stated, the authors have done the best they can to address the issues raised by the 2 reviewers.

We would appreciate receiving your revised manuscript by Mar 19 2020 11:59PM. When you are 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.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter.

To enhance the reproducibility of your results, we recommend that if applicable you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols

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). This letter should be uploaded as separate file and labeled 'Response to Reviewers'.
  • A marked-up copy of your manuscript that highlights changes made to the original version. This file should be uploaded as separate file and labeled 'Revised Manuscript with Track Changes'.
  • An unmarked version of your revised paper without tracked changes. This file should be uploaded as separate file and labeled 'Manuscript'.

Please note while forming your response, if your article is accepted, you may have the opportunity to make the peer review history publicly available. The record will include editor decision letters (with reviews) and your responses to reviewer comments. If eligible, we will contact you to opt in or out.

We look forward to receiving your revised manuscript.

Kind regards,

Aftab A. Ansari, PhD

Academic Editor

PLOS ONE

Additional Editor Comments (if provided):

The authors I believe have done the best they can to address the issues raised by the 2 reviewers. There is only one remaining isue that the authors need to address. In the revised Fig. 2 that appears to be presented out of order, there are only 2 data sets that show asterisk in Fig. 2C ? Are there no other statistically valid differences in the other data presented ? If so, the authors need to modify their manuscript otherwise please edit the figure.

[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 to be viewed.]

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 us at figures@plos.org. Please note that Supporting Information files do not need this step.

https://doi.org/10.1371/journal.pone.0229461.r003
Revision 2
Author Response

Reviewer #1: In this manuscript Ponnan et al., aims to evaluate an T cell responses and TSCM cells in volunteers enrolled in a phase I HIV-1 subtype C prophylactic vaccine trial in India during 2009-2010. Ponnan et al, hereby report novel findings where they interrogated vaccine induced responses and stem cell memory responses in volunteers who received an HIV-1 subtype C prophylactic vaccine candidate primed with ADVAX DNA and later followed by MVA boost versus either MVA alone or placebo. The results obtained in this study revealed that priming with ADVAX DNA followed with MVA boost versus MVA alone resulted in increased frequencies of peripheral CD8+ TSCM cells and augmented CD8+ T cell-mediated inhibition of replication of different HIV-1 clades. Even-though the manuscript is well written, and these finding may have have significance in the development of vaccines that are urgently needed by high risk populations.

However, as stated, the true role of TSCM and actual changes that occur during HIV-1 infection is yet to be fully understood. Therefore, in this manuscript additional investigation is required to confirm the true functionality of CD8+ TSCM cells generated after successful HIV-1 subtype C prophylactic vaccine candidate + ADVAX DNA + MVA boost. Therefore, the manuscript lacks critical experiment such as by sorting CD8+TSCM (a) could they have superior virus inhibition following co-culture with autologous infected CD4+ T cells? (b) in comparison to more differentiated memory phenotypes, are there any differences in cytokine patterns in response to HIV-1 specific overlapping peptides? to make any conclusions on the role of TSCM cells in this prophylactic vaccine trial.

• We agree with the reviewer that single cell sorting of CD8+ Tscm cells and their analysis for HIV-1 peptide induced cytokine response as well as virus inhibition activity would be extremely interesting. However, we were not in a position to undertake such experiments due to the limited number of PBMC available for this study. As mentioned in the manuscript, this study has been carried out PBMC stored from volunteers who were vaccinated during the period 2009-2010. Using the limited number of cells that were available we studied several aspects of vaccine-induced cellular and humoral immune responses including polyfunctional T cells, T follicular helper cells, Regulatory T cells, memory T cells, Tscm cells, variable loop antibodies, neutralizing antibodies, virus inhibition activity, etc. We have previously published 2 manuscripts in PLOSone entitled “Induction of circulating T Follicular Helper cells and Regulatory T cells correlating with HIV-1 gp120 variable loop antibodies by a subtype C prophylactic vaccine tested in a Phase I trial in India” (https://doi.org/10.1371/journal.pone.0055831) and “Induction and maintenance of bi-functional (IFN-γ + IL-2+ and IL-2+ TNF-α+) T cell responses by DNA prime MVA boosted subtype C prophylactic vaccine tested in a Phase I trial in India” (https://doi.org/10.1371/journal.pone.0213911).

Reviewer #2: In this manuscript, Ponnan and colleagues characterized the phenotype of total CD4 and CD8 T cells, and the ability of in vitro expanded cells to inhibit HIV replication using cells obtained from a HIV vaccine study that was conducted in India many years ago. The authors conclude that cells from vaccinated individuals exhibit some HIV inhibition activity and vaccination induces Tscm cells. Overall, these results are not conclusive and there are some major issues with the analyses as described below.

1) Need to provide details for CD4 T cell infection assay and indicate the ratio of CD4 and CD8 T cells used for virus inhibition assays.

As suggested by the reviewer, we revisited our description of the VIA assay and the suggested details have been incorporated in the manuscript.

2) Fig 2 – virus inhibition activity is not conclusive. There are no P values and activity was observed even at pre vaccination time point (Fig. 2A).

As suggested, addition to the Mann Whitney test, mean values of log10 reduction was compared at different time points within the placebo, Group A and Group B vaccines for the 5 different viral clades by post Hoc analysis by using Kruskal-Wallis test followed by subgroup analysis using Dunn’s multiple comparison test to identify differences between the three groups. For all analyses, differences were considered significant if p value was <0.05. We found Group A & B was statistically significant against the placebo only in " U455 viral inhibition at two week post last vaccination".

3) Figs 3-6: The data on characterization of different memory CD4 and CD8 T cells are not conclusive and significant for the following reasons.

• These should be expressed as a percent of total lymphocytes or converted into absolute number to get some idea about the actual change in the number of these cells over time. Currently, they are presented as a percent of total CD4 or CD8 T cells. This is not appropriate.

According to the reviewer's suggestion, we have reanalysed the FACS data and exported absolute count of different subsets of T cells and incorporated as supplementary tables in addition to the percentage frequency of immune cells.

• These are total CD4 or CD8 T cells, not vaccine-specific T cells.

3) Where there is an increase, we don’t know if these are MVA or HIV-specific cells..

4) overall, the observed increases are small considering that these are total cells (not antigen-specific).

We agree with the reviewer that the CD4 and CD8 T cells are not antigen specific. However, we found the significantly increased frequencies of different memory T cells in the vaccine recipients as compared to the placebo recipients. We therefore assume that the increase in immune cell subsets was vaccine induced.

4) The authors need to correct for multiple comparisons for P values.

As suggested by the reviewer we revisited statistical analysis. Since the study includes three groups of volunteers (Placebo, Group-A and Group-B) and different timepoints of vaccination, we used Kruskal-Wallis test to compare vaccine induced responses at different time points and followed it up with subgroup analysis using Dunn’s multiple comparison test to identify differences between the groups. This has been mentioned in the manuscript.

Additional Editor Comments (if provided):

The authors I believe have done the best they can to address the issues raised by the 2 reviewers. There is only one remaining isue that the authors need to address. In the revised Fig. 2 that appears to be presented out of order, there are only 2 data sets that show asterisk in Fig. 2C ? Are there no other statistically valid differences in the other data presented ? If so, the authors need to modify their manuscript otherwise please edit the figure.

Suggested modification has been carried out.

Attachments
Attachment
Submitted filename: Responce to the reviewers.docx
https://doi.org/10.1371/journal.pone.0229461.r004
Decision Letter - Aftab A. Ansari, Editor

Evaluation of antiviral T cell responses and TSCM cells in volunteers enrolled in a phase I HIV-1 subtype C prophylactic vaccine trial in India

PONE-D-19-30903R2

Dear Dr. Luke,

We are pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it complies with all outstanding technical requirements.

Within one week, you will receive an e-mail containing information on the amendments required prior to publication. When all required modifications have been addressed, you will receive a formal acceptance letter and your manuscript will proceed to our production department and be scheduled for publication.

Shortly after the formal acceptance letter is sent, an invoice for payment will follow. To ensure an efficient production and billing process, please log into Editorial Manager at https://www.editorialmanager.com/pone/, click the "Update My Information" link at the top of the page, and update your user information. 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 enable them to help maximize its impact. If they will be preparing press materials for this manuscript, you must inform our press team as soon as possible and 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.

With kind regards,

Aftab A. Ansari, PhD

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

https://doi.org/10.1371/journal.pone.0229461.r005
Formally Accepted
Acceptance Letter - Aftab A. Ansari, Editor

PONE-D-19-30903R2

Evaluation of antiviral T cell responses and TSCM cells in volunteers enrolled in a phase I HIV-1 subtype C prophylactic vaccine trial in India

Dear Dr. Hanna:

I am 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 notify them about your upcoming paper at this point, to enable them to help maximize its impact. If they will be preparing press materials for this manuscript, 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.

For any other questions or concerns, please email plosone@plos.org.

Thank you for submitting your work to PLOS ONE.

With kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Aftab A. Ansari

Academic Editor

PLOS ONE

https://doi.org/10.1371/journal.pone.0229461.r006

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