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Research Article | DOI: https://doi.org/10.31579/IJBR-2021/047
Department of Health Sciences, Division of Science, Technology, Engineering, and Math, Friends University, USA.
*Corresponding Author: Prince N. Agbedanu, Department of Health Sciences, Division of Science, Technology, Engineering, and Math, Friends University
Citation: Tristan A. Sprague, Prince N. Agbedanu (2021). Visualizing Antineoplastic Activity with a Whole Organism Drosophila Melanogaster Screen. International J. of Biomed Research. 1(8): DOI: 10.31579/IJBR-2021/047
Copyright: ©2021, Prince N. Agbedanu, This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Received: 19 October 2021 | Accepted: 27 November 2021 | Published: 09 November 2021
Keywords: antineoplastics; drug screen; drosophila; whole organism; RNAseq; toxicity
Cancer is a disease characterized by high mitosis rates with a loss of regulation. Many antineoplastics, those drugs used to treat cancer, act by slowing or halting mitosis. We are developing a whole-organism screening protocol to identify novel antineoplastic or their off-target effects. After exposing Drosophila melanogaster eggs and larva to an antineoplastic compound, their growth rate and population decrease. We screened several compounds from the National Cancer Institute’s (NCI) Developmental Therapeutics Program (DTP). Our screen successfully identified two compounds, toyocamycin and stictic acid, previously identified as possible antineoplastics. Toyocamycin killed a fraction of the population proportional to the dose concentration resulting in full mortality at 100 and 200 µM. At low doses, toyocamycin also slowed larval development by a mean of one day. RNAseq seemed to show that no genes were differentially expressed in mature flies after toyocamycin exposure was halted. Stictic acid delayed larval growth by an equal or greater margin compared to toyocamycin. Decreases in Drosophila growth or population may predict a compound’s antineoplastic activity and toxicity.
NCI, National Cancer Institute;
DTP, Developmental Therapeutics Program;
RNAseq, RNA sequencing;
µM, micromolar;
DMSO, dimethyl sulfoxide;
ELISA, enzyme-linked immunosorbent assay;
PBS, phosphate-buffered saline;
A plethora of screens for drug discovery, design, and toxicity exist, especially for novel antineoplastics. In silico and most in vitro screens require prior knowledge of a potential drug target, typically a protein or genetic sequence. Many diseases, including some cancers, are poorly characterized at the molecular level, rendering in silico methods and most in vitro methods less tractable [1]. In vivo screens look for phenotype production or rescue making them ideal for drug discovery for less-
understood diseases. Additionally, in vitro assays cannot recreate the cellular microenvironments present in an organism while whole-organism screens more accurately portray a compound’s biological activity and toxicity [1]. For example, Marstein at al [2] discovered that class II chemotherapeutics may fuel tumor reoccurrence, a potential side effect only uncovered because both cancerous and wild-type intestinal stem cells were present in the Drosophila model .While Drosophila cancer models have been used [2-5] to discover successful antineoplastics in the past, we have developed a screen that does not require generation of a cancer-related genotype. This screen is an inexpensive, widely accessible technique enabling compound characterization in physiological context.
The purpose of antineoplastics is to stop the rampant cell division characterizing cancer tumors. By testing chemical libraries in whole organisms for an ability to produce slow growth or lethality these inhibitors of cell division can be identified [6], although morphology can be an important indicator [7]. Cell division inhibition will be most noticeable where swift growth is ordinarily expected. Thus, screens using organisms in rapid stages of growth will detect such compounds with greater sensitivity than if organisms in slower stages of growth (i.e., adult Drosophila) were used. Our assay exposes Drosophila larva to potential drug candidates directly after emergence from the egg stage.
Many antineoplastics work by altering gene expression, either indirectly (e.g., through transcription factors phosphorylation) or by directly interrupting nucleic acid synthesis. For example, COX inhibitors are known to alter expression of many proteins in addition to their anti-inflammatory effects [8]. 5-fluoroacil, a thymine antimetabolite, has been shown to suppress miR-200b expression in tumors [9]. Such changes in gene expression should be quantifiable by differential [removed]DE) analysis of RNA sequencing data. Here, we investigate possible gene expression effects of the top hit found by our screen.
We were especially interested in gene expression effects long after drug exposure was terminated. The altered gene expression inherent to many antineoplastics could be detrimental to normal physiology if it persists long after treatment has ended. For example, Kurikara et al [10] discovered that toyocamycin strongly increases p16/INK4a expression, thereby inhibiting cell cycle progression. While this contributes to toyocamycin’s antitumor capability, cell senescence can also delay growth. Here, we demonstrate that low-concentration toyocamycin does delay growth, but the effect is short-lived once exposure terminates.
Our protocol correctly identified toyocamycin, a nucleoside isolated from Streptomyces [11], and stictic acid, a β-orcinol depsidone isolated from the lichen Usnea articulata [12], as positive hits out of a panel provided by the NCI Developmental Therapeutics Program (DTP). Toyocamycin is a pyrrolo[2,3‐d]pyrimidine (7‐deazapurine), which are known to have antitumor and antiviral properties [13] in addition to its antibiotic properties [11]. Nishioka et al [14] recorded phosphatidyl kinase inhibition by toyocamycin. Through these mechanisms, toyocamycin perturbs nucleic acid synthesis and translation.
Stictic acid has been shown to inhibit growth in MCF-7 breast cancer and HT29 colon cancer cell lines compared to MRC-5 normal cells [15]. Wassmen et al [16] discovered stictic acid reactivates mutant p53. Stictic acid derivatives also have antioxidant activity against ROS [12]. We report similar growth inhibition in Drosophila in both stictic acid and toyocamycin treatments. In general, we believe this work will be useful for studying antineoplastic strength and toxicity in vivo.
Drosophila Genetics and Maintenance; Chemical Library
Wild-type strain 25210 DGRP 859 flies were used from the Bloomington Drosophila Stock Center (Illinois, USA). Stocks were maintained on commercial media (Formula 424, Carolina Biological, North Carolina, USA) in clear plastic vials 1 1/4" diam × 4" height. Flies were moved to new vials every 30 days.
All compounds were sourced through the Drug Synthesis and Chemistry Branch, Developmental Therapeutics Program, Division of Cancer Treatment and Diagnosis, National Cancer Institute (Maryland, USA). Compounds were stored in crystalline form at -70°C until just prior to use.
In Vivo Drug Screening
15 adult male and 15 adult females were added to each vial and treatment groups consisted of three vials each. All compounds were dissolved in DMSO (HPLC grade; ThermoFisher, Massachusetts, USA) and diluted to 200 µM, unless otherwise specified. In each vial, 15mL of dry media was reconstituted with 13 mL of 200 µM drug solution. Control vials were prepared with 15 mL of dry media and 13 mL of vehicle control. Adult flies were introduced to media for 24 hrs and then removed. Vials were maintained at 21°C with 12 hours lighting per day. 200 µM drug solutions were stored at -20°C.
An additional 2 mL of drug solution or DI water was added to each vial at 24, 48, and 72 hrs from addition of adults. Each vial was observed and the number of pupae and adult offspring recorded daily. Flies were examined for abnormal phenotypes. After emergence of all pupae, the adult vial populations were sexed and counted.
To quantify when flies pupated on average, cumulative pupation was plotted as a function of time in days and fitted with a 4-parameter logistic regression. The inflection point, tmid, was used as a measure of pupation time; the mean and standard deviations are reported in Table 1. See Supplemental Information for further explanation of the logistic regression.
RNAseq and Differential Expression Analysis
Specimens were randomly selected from each vial population and frozen in 1 mL RNAlater (ThermoFisher). Preliminary RNAseq specimens contained one fly per 1 ml RNAlater; triplicates were combined due to low RNA yield. Followup RNAseq specimens were allocated three flies with 1 mL RNAlater per replicate to ensure adequate yield. Specimens were stored at -70°C and shipped overnight on dry ice.
RNAseq was performed by Omega Bioservices (Georgia, USA) using Illumina sequencers at a 10M read sequencing depth. DESeq2 was utilized for differential expression analyses. DESeq2 analysis was performed using the Illumina BaseSpace platform by Omega Bioservices staff.
Apc11 protein ELISA
To verify upregulation of lmgA past the transcription stage, ELISA of the protein Apc11 was undertaken. ELISA was performed according to the kit manufacturer’s instructions (MyBioSource, California, USA). Briefly, samples were prepared by grinding single whole flies (n=6 with equal numbers of each sex flies per treatment.) into 500 µL PBS each using glass tissue grinders in a wet ice bath. Each sample was subjected to three freeze-thaw cycles in liquid N2 at room temperature. All samples were centrifugated at 5000 rpm for 15 minutes. Samples were assayed in triplicate technical replications on a single competitive human ANAPC11 ELISA plate (MyBioSource, California, USA) to avoid interassay variability. Six standards ranging from 100 ng/mL to 0 ng/mL were run in triplicate. 5-parameter logistic regression calibration curves were generated using the nplr package [17] in R.
Statistical Analysis
All statistical analysis and data visualization was done using R v4.0.3 [18] using packages ggplot2 [19], dplyr [20], and nplr, except for DESeq2 analyses. Unless otherwise noted, unpaired two sample t-tests were used to calculate p-values. Confidence levels were set at 0.95.
Toyocamycin results in death or delayed growth of Drosophila from the larval to adult stages. 200 and 100 µM toyocamycin resulted in 100% larval mortality; 50 µM resulted in a nonsignificant decrease (P = 0.1233, Fig. 1). Toyocamycin at 25 µM showed a slight reduction in time to pupation and time to emergence (Fig. 2-3). Additionally, a non-significant decrease in mean population (P>.05) was observed (Fig. 1).
Time to half-pupation is summarized in Table 1. Toyocamycin and stictic groups showed a mean delay of 1 day in pupation (Fig. 2-5); some stictic acid trials showed a delay of 3 days before pupation (individual data not shown). There was no significant difference in the mean population gender proportion between the treatment and control groups (P = 1) in either stictic acid or toyocamycin groups.
Flies exposed to > 100 µM toyocamycin at the egg and larval stage saw complete mortality. Flies exposed to 25 µM toyocamycin saw a nonsignificant level of mortality.
95% CI given for treatments where all 3 replicates could be fit with the model. See Supplementary Information for regression details.
The cumulative number of pupae visible in each vial, averaged over treatments. Toyocamycin slows the appearance of pupae.
The cumulative number of adults visible in each vial, averaged over treatments. Toyocamycin slows the emergence of adults.
The cumulative number of pupae visible in each vial, averaged over treatments. Stictic acid slows the appearance of pupae.
The cumulative number of adults visible in each vial, averaged over treatments. Stictic acid slows the emergence of adults.
Preliminary RNAseq data showed 5 genes were differentially expressed significantly; CG14042, CG14933, Fbp2, and lmgA were upregulated (p = 0.0474, p = 0.0181, p = 0.0012, p = 0.0017 respectively) and snRNA:U1:95Ca was downregulated (p = 0.023) (Fig. 6). lmgA had the highest log2-fold change as calculated by DESeq2, 8.065 (Fig. 6).
Competitive ELISA demonstrated that lmgA was not significantly DE in the toyocamycin group compared to control (Fig. 7, n = 6 flies per group, p = 0.1075). Specimens used in ELISA assay were from trials independent of those used for preliminary RNAseq. Thus, another set of toyocamycin and control trials was run with a greater number of specimens sent for RNAseq.
RNAseq performed on male and female from both control and toyocamycin groups, (n = 3 flies per sex, with RNA combined before sequencing).
Competitive ELISA of Apc11 encoded by lmgA. Apc11 was not upregulated as preliminary RNAseq suggests.
Follow-up RNAseq with greater replicates (n = 6 per group) indicated no significant DE in toyocamycin treated flies at maturity. However, when flies in the toyocamycin group were compared to control flies of the same sex, 4 genes were significantly DE in males and none in females (Fig. 8). However, there are only three replicates per group when sex is considered, which does not meet Schurch et al’s [21] suggested number of biological replicates for RNAseq studies. More extensive study with greater read depth is needed to determine if sex-related differences in gene expression occur after toyocamycin exposure. It is likely that the effect we observed is due to small sampling size and interindividual variability.
Further RNAseq, showing DE between males in control and toyocamycin treatments (n = 3 flies per biological replicates, n = 3 biological replicates). When sex is ignored, no DE genes were found.
Due to the distinct response in Drosophila, our results show toyocamycin and stictic acid are potent inhibitors of actively growing tissues. Toyocamycin is clearly toxic to larva in Drosophila melanogaster, as demonstrated by mortality and the increased time by larva to reach milestones like pupation and emergence. The inhibitory effect quickly becomes toxic as concentration increases beyond 25 µM. Moreover, toyocamycin appears to affect male and female organisms equally, though further gene expression profiling could be warranted. Stictic acid delayed pupation by the same margin as toyocamycin (Fig. 4-5). This agrees with Pejin et al’s [15] observations in cell lines, where clear growth inhibition was noted. These results show that our screening protocol can identify growth inhibitors by observable effects on a developing Drosophila population.
While a preliminary RNAseq experiment suggested some differences in expression in mature flies after toyocamycin exposure, further analysis showed no difference. In turn, this suggest that toyocamycin ceases to affect gene expression relatively quickly when exposure stops. The RNAseq dataset, when specimens were separated by sex and compared, suggested differential expression of four genes; this analysis is inconclusive due to only three biological replicates of each sex per treatment. Furthermore, pupation did not lag far behind controls in the toyocamycin exposed flies. These flies typically pupated only one day after those in the control, while as flies in some stictic acid trials saw a delay of 3 days. Our results suggest toyocamycin’s affect fades rapidly after discontinuation. For patients undergoing chemotherapy, new drugs without long-lasting side effects once treatment is stopped are desirable. Further study of toyocamycin analogues at various time points after exposure is needed. Additionally, RNAseq with greater read depth may reveal more DE genes.
Our screen successfully identified two known antineoplastics. Additionally, potential gene expression changes related to toyocamycin exposure were recorded. This was achieved without the time-consuming and expensive genetic manipulation needed to produce a cancerous genotype or patient avatar in the flies as in Markstein et al [2] or Levine & Cagan’s [3] work. Our screen represents a low-cost platform for studying antineoplastics in vivo. This technique may be used as an initial screen for suspected antineoplastics, to elucidate the mechanism of known antineoplastics in a whole organism, or to study their off-target affects. Furthermore, our gene expression experiments imply that toyocamycin-based antineoplastics may have little long-term toxicity in that regard. In the future, we hope to correlate pupation delay with inhibition of cell division in cancer lines.
This work was partly supported by the Kansas Academy of Science through the Student Research Grant Program; we thank their Undergraduate Scholarship Committee.
We extend our deep gratitude to Dr. Chunyang Li and the other staff at Omega Bioservices for their expertise in RNAseq, useful discussion, and collaboration. We are indebted to Dr. Mostafa Zamanian of the University of Wisconsin-Madison for timely guidance on RNAseq and analysis. Stocks obtained from the Bloomington Drosophila Stock Center (NIH P40OD018537) were used in this study. Also, we thank Sarah Bottorff of Carolina Biological for suggestions on controlling Drosophila bacterial infections.
We wish to thank the Friends University Division of Science, Technology, Engineering, and Math, especially Dr. Nora Strasser (Chair), Amy Morgan (Admin), and Celia Milam (Drosophila stockkeeper). Additionally, we are grateful to Ramon Emmart, Jessica Boone, Erin E. McCoskey (PA-S), and Abbey L. Fischer (CMA) for their scrutiny of our grant proposal.
P.N.A. conceived the project. P.N.A. and T.A.S. designed the experiments. T.A.S. performed all experiments. T.A.S. analyzed the data. T.A.S wrote the manuscript. P.N.A. and T.A.S. edited and proofread the manuscript. P.N.A. and T.A.S procured funding.
Supplementary Information for “Visualizing Antineoplastic Activity with a Whole Organism Drosophila melanogaster Screen”
Nonlinear Regression of Pupation Data.
The cumulative number of Drosophila pupae in a vial as time increases (if the initial number of eggs is fixed) will follow a sigmoidal pattern (Fig. 2, 4). This is also true for cumulative number of adults emerging from a fixed number of pupae. Given that a vial will first have 0 pupae/adults, and will have T number of eggs present, the number of pupae y as time t increases,
where tmid is the time at which half of all flies have pupated and b is the Hill slope. Note the similarity to dose-response curves. Conceptually, tmid is equivalent to an EC50. This is an ideal case, since 100 % and 0 % response are strictly defined; that is, 0% response is 0 pupae and 100% is the maximum number of pupae for that vial. The maximum number of pupae is determined by how many eggs were laid in the vial before the parental generation has been removed and thus cannot change over the course of the experiment. Thus, relative and absolute “EC50” are equivalent in this situation (each replicate could be transformed into % pupa by dividing the cumulative number of pupae on each day by the eventually maximum number of pupae,
tmid will be determined by environmental factors, the presence of a drug, and the specific properties of the drug. By comparing tmid between trials, the pupation delay caused by a drug can be determined. The Hill slope, b, is related to the timespan over which the eggs were laid. If the eggs were laid within a short time span of each other, the slope will be steeper. Eggs laid over a greater timespan will result in a smaller slope. This slope could also be related to the flies’ rate of development during the larval stage.
The 4-parameter logistic regression model explained above can be fitted to the data with the R package “nplr” (R package nplr: n-parameter logistic regressions, Commo & Bott, 2016). For example:
Suppl. Fig. 1-3: 4-parameter nonlinear regression of cumulative pupation vs. time in days. Error bars represent one standard error. Note only one replicate of stictic acid was able to be fit.
nplr calculates “IC50” (actually tmid in this case) from the fitted regression line and the 95% confidence interval. The above regressions were performed on experiments in triplicate. Fitting this model makes it easy to tell that toyocamycin delays the tmid by 1.1 days.
Distributions of ELISA data.
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Dear Editorial Coordinator of the Journal of Nutrition and Food Processing! "I would like to thank the Journal of Nutrition and Food Processing for including and publishing my article. The peer review process was very quick, movement and precise. The Editorial Board has done an extremely conscientious job with much help, valuable comments and advices. I find the journal very valuable from a professional point of view, thank you very much for allowing me to be part of it and I would like to participate in the future!”
Dealing with The Journal of Neurology and Neurological Surgery was very smooth and comprehensive. The office staff took time to address my needs and the response from editors and the office was prompt and fair. I certainly hope to publish with this journal again.Their professionalism is apparent and more than satisfactory. Susan Weiner
My Testimonial Covering as fellowing: Lin-Show Chin. The peer reviewers process is quick and effective, the supports from editorial office is excellent, the quality of journal is high. I would like to collabroate with Internatioanl journal of Clinical Case Reports and Reviews.
My experience publishing in Psychology and Mental Health Care was exceptional. The peer review process was rigorous and constructive, with reviewers providing valuable insights that helped enhance the quality of our work. The editorial team was highly supportive and responsive, making the submission process smooth and efficient. The journal's commitment to high standards and academic rigor makes it a respected platform for quality research. I am grateful for the opportunity to publish in such a reputable journal.
My experience publishing in International Journal of Clinical Case Reports and Reviews was exceptional. I Come forth to Provide a Testimonial Covering the Peer Review Process and the editorial office for the Professional and Impartial Evaluation of the Manuscript.
I would like to offer my testimony in the support. I have received through the peer review process and support the editorial office where they are to support young authors like me, encourage them to publish their work in your esteemed journals, and globalize and share knowledge globally. I really appreciate your journal, peer review, and editorial office.
Dear Agrippa Hilda- Editorial Coordinator of Journal of Neuroscience and Neurological Surgery, "The peer review process was very quick and of high quality, which can also be seen in the articles in the journal. The collaboration with the editorial office was very good."
I would like to express my sincere gratitude for the support and efficiency provided by the editorial office throughout the publication process of my article, “Delayed Vulvar Metastases from Rectal Carcinoma: A Case Report.” I greatly appreciate the assistance and guidance I received from your team, which made the entire process smooth and efficient. The peer review process was thorough and constructive, contributing to the overall quality of the final article. I am very grateful for the high level of professionalism and commitment shown by the editorial staff, and I look forward to maintaining a long-term collaboration with the International Journal of Clinical Case Reports and Reviews.
To Dear Erin Aust, I would like to express my heartfelt appreciation for the opportunity to have my work published in this esteemed journal. The entire publication process was smooth and well-organized, and I am extremely satisfied with the final result. The Editorial Team demonstrated the utmost professionalism, providing prompt and insightful feedback throughout the review process. Their clear communication and constructive suggestions were invaluable in enhancing my manuscript, and their meticulous attention to detail and dedication to quality are truly commendable. Additionally, the support from the Editorial Office was exceptional. From the initial submission to the final publication, I was guided through every step of the process with great care and professionalism. The team's responsiveness and assistance made the entire experience both easy and stress-free. I am also deeply impressed by the quality and reputation of the journal. It is an honor to have my research featured in such a respected publication, and I am confident that it will make a meaningful contribution to the field.
"I am grateful for the opportunity of contributing to [International Journal of Clinical Case Reports and Reviews] and for the rigorous review process that enhances the quality of research published in your esteemed journal. I sincerely appreciate the time and effort of your team who have dedicatedly helped me in improvising changes and modifying my manuscript. The insightful comments and constructive feedback provided have been invaluable in refining and strengthening my work".
I thank the ‘Journal of Clinical Research and Reports’ for accepting this article for publication. This is a rigorously peer reviewed journal which is on all major global scientific data bases. I note the review process was prompt, thorough and professionally critical. It gave us an insight into a number of important scientific/statistical issues. The review prompted us to review the relevant literature again and look at the limitations of the study. The peer reviewers were open, clear in the instructions and the editorial team was very prompt in their communication. This journal certainly publishes quality research articles. I would recommend the journal for any future publications.
Dear Jessica Magne, with gratitude for the joint work. Fast process of receiving and processing the submitted scientific materials in “Clinical Cardiology and Cardiovascular Interventions”. High level of competence of the editors with clear and correct recommendations and ideas for enriching the article.
We found the peer review process quick and positive in its input. The support from the editorial officer has been very agile, always with the intention of improving the article and taking into account our subsequent corrections.
My article, titled 'No Way Out of the Smartphone Epidemic Without Considering the Insights of Brain Research,' has been republished in the International Journal of Clinical Case Reports and Reviews. The review process was seamless and professional, with the editors being both friendly and supportive. I am deeply grateful for their efforts.
To Dear Erin Aust – Editorial Coordinator of Journal of General Medicine and Clinical Practice! I declare that I am absolutely satisfied with your work carried out with great competence in following the manuscript during the various stages from its receipt, during the revision process to the final acceptance for publication. Thank Prof. Elvira Farina
Dear Jessica, and the super professional team of the ‘Clinical Cardiology and Cardiovascular Interventions’ I am sincerely grateful to the coordinated work of the journal team for the no problem with the submission of my manuscript: “Cardiometabolic Disorders in A Pregnant Woman with Severe Preeclampsia on the Background of Morbid Obesity (Case Report).” The review process by 5 experts was fast, and the comments were professional, which made it more specific and academic, and the process of publication and presentation of the article was excellent. I recommend that my colleagues publish articles in this journal, and I am interested in further scientific cooperation. Sincerely and best wishes, Dr. Oleg Golyanovskiy.
Dear Ashley Rosa, Editorial Coordinator of the journal - Psychology and Mental Health Care. " The process of obtaining publication of my article in the Psychology and Mental Health Journal was positive in all areas. The peer review process resulted in a number of valuable comments, the editorial process was collaborative and timely, and the quality of this journal has been quickly noticed, resulting in alternative journals contacting me to publish with them." Warm regards, Susan Anne Smith, PhD. Australian Breastfeeding Association.
Dear Jessica Magne, Editorial Coordinator, Clinical Cardiology and Cardiovascular Interventions, Auctores Publishing LLC. I appreciate the journal (JCCI) editorial office support, the entire team leads were always ready to help, not only on technical front but also on thorough process. Also, I should thank dear reviewers’ attention to detail and creative approach to teach me and bring new insights by their comments. Surely, more discussions and introduction of other hemodynamic devices would provide better prevention and management of shock states. Your efforts and dedication in presenting educational materials in this journal are commendable. Best wishes from, Farahnaz Fallahian.
Dear Maria Emerson, Editorial Coordinator, International Journal of Clinical Case Reports and Reviews, Auctores Publishing LLC. I am delighted to have published our manuscript, "Acute Colonic Pseudo-Obstruction (ACPO): A rare but serious complication following caesarean section." I want to thank the editorial team, especially Maria Emerson, for their prompt review of the manuscript, quick responses to queries, and overall support. Yours sincerely Dr. Victor Olagundoye.
Dear Ashley Rosa, Editorial Coordinator, International Journal of Clinical Case Reports and Reviews. Many thanks for publishing this manuscript after I lost confidence the editors were most helpful, more than other journals Best wishes from, Susan Anne Smith, PhD. Australian Breastfeeding Association.
Dear Agrippa Hilda, Editorial Coordinator, Journal of Neuroscience and Neurological Surgery. The entire process including article submission, review, revision, and publication was extremely easy. The journal editor was prompt and helpful, and the reviewers contributed to the quality of the paper. Thank you so much! Eric Nussbaum, MD
Dr Hala Al Shaikh This is to acknowledge that the peer review process for the article ’ A Novel Gnrh1 Gene Mutation in Four Omani Male Siblings, Presentation and Management ’ sent to the International Journal of Clinical Case Reports and Reviews was quick and smooth. The editorial office was prompt with easy communication.
Dear Erin Aust, Editorial Coordinator, Journal of General Medicine and Clinical Practice. We are pleased to share our experience with the “Journal of General Medicine and Clinical Practice”, following the successful publication of our article. The peer review process was thorough and constructive, helping to improve the clarity and quality of the manuscript. We are especially thankful to Ms. Erin Aust, the Editorial Coordinator, for her prompt communication and continuous support throughout the process. Her professionalism ensured a smooth and efficient publication experience. The journal upholds high editorial standards, and we highly recommend it to fellow researchers seeking a credible platform for their work. Best wishes By, Dr. Rakhi Mishra.
Dear Jessica Magne, Editorial Coordinator, Clinical Cardiology and Cardiovascular Interventions, Auctores Publishing LLC. The peer review process of the journal of Clinical Cardiology and Cardiovascular Interventions was excellent and fast, as was the support of the editorial office and the quality of the journal. Kind regards Walter F. Riesen Prof. Dr. Dr. h.c. Walter F. Riesen.
Dear Ashley Rosa, Editorial Coordinator, International Journal of Clinical Case Reports and Reviews, Auctores Publishing LLC. Thank you for publishing our article, Exploring Clozapine's Efficacy in Managing Aggression: A Multiple Single-Case Study in Forensic Psychiatry in the international journal of clinical case reports and reviews. We found the peer review process very professional and efficient. The comments were constructive, and the whole process was efficient. On behalf of the co-authors, I would like to thank you for publishing this article. With regards, Dr. Jelle R. Lettinga.
Dear Clarissa Eric, Editorial Coordinator, Journal of Clinical Case Reports and Studies, I would like to express my deep admiration for the exceptional professionalism demonstrated by your journal. I am thoroughly impressed by the speed of the editorial process, the substantive and insightful reviews, and the meticulous preparation of the manuscript for publication. Additionally, I greatly appreciate the courteous and immediate responses from your editorial office to all my inquiries. Best Regards, Dariusz Ziora
Dear Chrystine Mejia, Editorial Coordinator, Journal of Neurodegeneration and Neurorehabilitation, Auctores Publishing LLC, We would like to thank the editorial team for the smooth and high-quality communication leading up to the publication of our article in the Journal of Neurodegeneration and Neurorehabilitation. The reviewers have extensive knowledge in the field, and their relevant questions helped to add value to our publication. Kind regards, Dr. Ravi Shrivastava.
Dear Clarissa Eric, Editorial Coordinator, Journal of Clinical Case Reports and Studies, Auctores Publishing LLC, USA Office: +1-(302)-520-2644. I would like to express my sincere appreciation for the efficient and professional handling of my case report by the ‘Journal of Clinical Case Reports and Studies’. The peer review process was not only fast but also highly constructive—the reviewers’ comments were clear, relevant, and greatly helped me improve the quality and clarity of my manuscript. I also received excellent support from the editorial office throughout the process. Communication was smooth and timely, and I felt well guided at every stage, from submission to publication. The overall quality and rigor of the journal are truly commendable. I am pleased to have published my work with Journal of Clinical Case Reports and Studies, and I look forward to future opportunities for collaboration. Sincerely, Aline Tollet, UCLouvain.
Dear Ms. Mayra Duenas, Editorial Coordinator, International Journal of Clinical Case Reports and Reviews. “The International Journal of Clinical Case Reports and Reviews represented the “ideal house” to share with the research community a first experience with the use of the Simeox device for speech rehabilitation. High scientific reputation and attractive website communication were first determinants for the selection of this Journal, and the following submission process exceeded expectations: fast but highly professional peer review, great support by the editorial office, elegant graphic layout. Exactly what a dynamic research team - also composed by allied professionals - needs!" From, Chiara Beccaluva, PT - Italy.
Dear Maria Emerson, Editorial Coordinator, we have deeply appreciated the professionalism demonstrated by the International Journal of Clinical Case Reports and Reviews. The reviewers have extensive knowledge of our field and have been very efficient and fast in supporting the process. I am really looking forward to further collaboration. Thanks. Best regards, Dr. Claudio Ligresti
Dear Chrystine Mejia, Editorial Coordinator, Journal of Neurodegeneration and Neurorehabilitation. “The peer review process was efficient and constructive, and the editorial office provided excellent communication and support throughout. The journal ensures scientific rigor and high editorial standards, while also offering a smooth and timely publication process. We sincerely appreciate the work of the editorial team in facilitating the dissemination of innovative approaches such as the Bonori Method.” Best regards, Dr. Matteo Bonori.
I recommend without hesitation submitting relevant papers on medical decision making to the International Journal of Clinical Case Reports and Reviews. I am very grateful to the editorial staff. Maria Emerson was a pleasure to communicate with. The time from submission to publication was an extremely short 3 weeks. The editorial staff submitted the paper to three reviewers. Two of the reviewers commented positively on the value of publishing the paper. The editorial staff quickly recognized the third reviewer’s comments as an unjust attempt to reject the paper. I revised the paper as recommended by the first two reviewers.
Dear Maria Emerson, Editorial Coordinator, Journal of Clinical Research and Reports. Thank you for publishing our case report: "Clinical Case of Effective Fetal Stem Cells Treatment in a Patient with Autism Spectrum Disorder" within the "Journal of Clinical Research and Reports" being submitted by the team of EmCell doctors from Kyiv, Ukraine. We much appreciate a professional and transparent peer-review process from Auctores. All research Doctors are so grateful to your Editorial Office and Auctores Publishing support! I amiably wish our article publication maintained a top quality of your International Scientific Journal. My best wishes for a prosperity of the Journal of Clinical Research and Reports. Hope our scientific relationship and cooperation will remain long lasting. Thank you very much indeed. Kind regards, Dr. Andriy Sinelnyk Cell Therapy Center EmCell
Dear Editorial Team, Clinical Cardiology and Cardiovascular Interventions. It was truly a rewarding experience to work with the journal “Clinical Cardiology and Cardiovascular Interventions”. The peer review process was insightful and encouraging, helping us refine our work to a higher standard. The editorial office offered exceptional support with prompt and thoughtful communication. I highly value the journal’s role in promoting scientific advancement and am honored to be part of it. Best regards, Meng-Jou Lee, MD, Department of Anesthesiology, National Taiwan University Hospital.
Dear Editorial Team, Journal-Clinical Cardiology and Cardiovascular Interventions, “Publishing my article with Clinical Cardiology and Cardiovascular Interventions has been a highly positive experience. The peer-review process was rigorous yet supportive, offering valuable feedback that strengthened my work. The editorial team demonstrated exceptional professionalism, prompt communication, and a genuine commitment to maintaining the highest scientific standards. I am very pleased with the publication quality and proud to be associated with such a reputable journal.” Warm regards, Dr. Mahmoud Kamal Moustafa Ahmed
Dear Maria Emerson, Editorial Coordinator of ‘International Journal of Clinical Case Reports and Reviews’, I appreciate the opportunity to publish my article with your journal. The editorial office provided clear communication during the submission and review process, and I found the overall experience professional and constructive. Best regards, Elena Salvatore.
Dear Mayra Duenas, Editorial Coordinator of ‘International Journal of Clinical Case Reports and Reviews Herewith I confirm an optimal peer review process and a great support of the editorial office of the present journal
Dear Editorial Team, Clinical Cardiology and Cardiovascular Interventions. I am really grateful for the peers review; their feedback gave me the opportunity to reflect on the message and impact of my work and to ameliorate the article. The editors did a great job in addition by encouraging me to continue with the process of publishing.
Dear Cecilia Lilly, Editorial Coordinator, Endocrinology and Disorders, Thank you so much for your quick response regarding reviewing and all process till publishing our manuscript entitled: Prevalence of Pre-Diabetes and its Associated Risk Factors Among Nile College Students, Sudan. Best regards, Dr Mamoun Magzoub.
International Journal of Clinical Case Reports and Reviews is a high quality journal that has a clear and concise submission process. The peer review process was comprehensive and constructive. Support from the editorial office was excellent, since the administrative staff were responsive. The journal provides a fast and timely publication timeline.
Dear Maria Emerson, Editorial Coordinator of International Journal of Clinical Case Reports and Reviews, What distinguishes International Journal of Clinical Case Report and Review is not only the scientific rigor of its publications, but the intellectual climate in which research is evaluated. The submission process is refreshingly free of unnecessary formal barriers and bureaucratic rituals that often complicate academic publishing without adding real value. The peer-review system is demanding yet constructive, guided by genuine scientific dialogue rather than hierarchical or authoritarian attitudes. Reviewers act as collaborators in improving the manuscript, not as gatekeepers imposing arbitrary standards. This journal offers a rare balance: high methodological standards combined with a respectful, transparent, and supportive editorial approach. In an era where publishing can feel more burdensome than research itself, this platform restores the original purpose of peer review — to refine ideas, not to obstruct them Prof. Perlat Kapisyzi, FCCP PULMONOLOGIST AND THORACIC IMAGING.
Dear Mayra Duenas, Editorial Coordinator of the journal IJCCR, I write here a little on my experience as an author submitting to the International Journal of Clinical Case Reports and Reviews (IJCCR). This was my first submission to IJCCR and my manuscript was inherently an outsider’s effort. It attempted to broadly identify and then make some sense of life’s under-appreciated mysteries. I initially had responded to a request for possible submissions. I then contacted IJCCR with a tentative topic for a manuscript. They quickly got back with an approval for the submission, but with a particular requirement that it be medically relevant. I then put together a manuscript and submitted it. After the usual back-and-forth over forms and formality, the manuscript was sent off for reviews. Within 2 weeks I got back 4 reviews which were both helpful and also surprising. Surprising in that the topic was somewhat foreign to medical literature. My subsequent updates in response to the reviewer comments went smoothly and in short order I had a series of proofs to evaluate. All in all, the whole publication process seemed outstanding. It was both helpful in terms of the paper’s content and also in terms of its efficient and friendly communications. Thank you all very much. Sincerely, Ted Christopher, Rochester, NY.
Dear Grace Pierce, Editorial Coordinator of the journal IJCCR, I had a very positive experience with Auctores - Journal throughout the publication process. The Editorial Team was highly responsive, professional, and supportive at every stage. I would like to extend my sincere thanks to the Editor: Grace Pierce, for her guidance and assistance. The peer-review process was smooth and constructive, helping improve the quality of my work. I would gladly recommend Auctores Journal to fellow researchers and authors. Dr. SABITA SINHA, Medical Oncologist, MD (Electro Homeopathy).
Dear Maria Emerson, Editorial Coordinator of - Journal of Clinical Research and Reports. ''I am pleased to provide this testimonial following the publication of our recent case report in this journal. The peer review process was rigorous, constructive, thorough, and conducted in a timely manner. The reviewers’ comments were thoughtful, detailed, and highly constructive, contributing substantially to the refinement, clarity, and scientific robustness of our manuscript. The process was conducted with professionalism and academic integrity throughout. The support provided by the editorial office was exemplary. Communication was consistently prompt, clear, and courteous at all stages of the submission and publication process. The editorial team demonstrated a high level of organization and responsiveness, ensuring that all queries were addressed efficiently and that the process remained transparent and well-coordinated. The overall quality of the journal is reflected in its strong editorial standards, commitment to scientific excellence, and dedication to publishing clinically meaningful research. It has been a privilege to publish our work in this journal, and we would welcome the opportunity to contribute further in the future.'' Best wishes from, Dr. Efstratios Trogkanis, Cardiologist.
Dear Reader: We have published several articles in the Auctores Publishing, LLC, journal, Clinical Medical Reviews and Reports in recent years (CMRR). This is an ‘open access’ journal and the following are our observations. From the initial invitation to submit an article, to the final edits of galley proofs, we have found CMRR personnel to be professional, responsive, rapid and thorough. This entire process begins with Catherine Mitchell, Editorial Coordinator. She is simply outstanding, and, I believe, unparalleled in her capacity. I cannot imagine a more responsive and dedicated Editorial Coordinator. As I read the dates and timing of her correspondence with us, it seems that she never sleeps. I hope Auctores Publishing, LLC, appreciates her efforts as much as these authors do. Thank you to Auctores Publishing, LLC, to the Editorial Staff/Board, and to Catherine Mitchell from a grateful author(s).
