Source: TRUSTEES OF TUFTS COLLEGE submitted to NRP
GUT MICROBIOTA MODULATE THE EFFECT OF DIET ON INFLAMMATION AND TUMORIGENESIS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1022521
Grant No.
2020-67017-30845
Cumulative Award Amt.
$499,669.00
Proposal No.
2019-07690
Multistate No.
(N/A)
Project Start Date
Apr 15, 2020
Project End Date
Apr 14, 2023
Grant Year
2020
Program Code
[A1343]- Food and Human Health
Recipient Organization
TRUSTEES OF TUFTS COLLEGE
136 HARRISON AVE
Boston,MA 021111817
Performing Department
Vitamins & Carcinogenesis
Non Technical Summary
Colorectal cancer (CRC) remains a major public health problem in the US - with approximately 135,000 new cases being diagnosed and 50,000 deaths from this disease each year. Although several agents are reported to reduce cancer formation in laboratory rodents, aspirin remains the only agent with robust evidence in human populations - however its adverse side effects may outweigh its benefits. Thus, there is a clear need to identify new, effective and safe strategies to prevent CRC.Diet is a major determinant of CRC risk - recent estimates indicate that up to 38% of all CRC cases can be attributed to poor diet. The consensus of several human population studies is that consumption of a Mediterranean diet (MD) is associated with a significantly reduced risk for CRC. The MD is characterized by a high intake of vegetables, legumes, fruits, nuts, grains, fish, seafood, olive oil, and moderate intake of red wine.Changes in the composition of the gut bacteria play a role in CRC formation. Moreover, the composition of the gut bacteria is also sensitive to diet. The goal of our current studies is to understand the involvement of gut bacteria in CRC prevention by MD and whether the CRC protective effect of MD can be enhanced by giving specific bacteria with known anti-cancer propertiesWe will achieve this goal by conducting two experiments utilizing a mouse model of CRC. Mice will be fed standard diet or a Mediterranean and undergo various bacteria treatments including depletion, depletion with adding back inflammatory bacteria components and supplementation with protective bacteria.Successful completion of these studies will enhance our understanding of how MD protects against CRC and may outline a novel approach to further enhance the protective effect of MD.
Animal Health Component
(N/A)
Research Effort Categories
Basic
100%
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
70250101010100%
Goals / Objectives
Colorectal cancer (CRC) remains a major public health burden in the US - with approximately 135,000 new cases being diagnosed and 50,000 deaths from this disease each year. Our long-term goal is to create knowledge that will contribute to the development of strategies to reduce the burden of this disease on our society.The Mediterranean diet (MD) is one of the dietary patterns most strongly associated with a reduced risk for CRC. Disturbances in the composition of gut microbial communities are also etiologically involved in CRC. Given that gut microbial populations are sensitive to diet, our lack of understanding of how the MD affects the gut microbiome, and the physiological significance of these effects, is surprising.The major goal of this project is to understand the role of the gut microbiome in the chemopreventive effect of the MDThe specific objectives of this proposal are to:To understand the contribution of gut microbiota to the chemopreventive effect of MD.To determine if the chemopreventive effect of MD is enhanced by Pd.To determine if MD increases the abundance of Pd in the gut.
Project Methods
The objectives of this proposal will be addressed by conducting two mouse experiments, each with a 2 x 3 factorial design. The first experiment will address Aim 1 and will involve randomizing wildtype C57BL6/J mice to receive either of two diets (control, or Mediterranean Diet) and either of three gut microbiota manipulations (control, microbiota depletion or microbiota depletion with restored inflammatory capacity). The second experiment will address Aims 2 and 3 and will involve randomizing wildtype C57BL6/J mice to receive either of two diets (control, or Mediterranean Diet) and either of three gut microbiota manipulations (control, freeze dried Pd or live Pd).Mice will be kept on a 12hr light/dark cycle and food and water provided ad libitum.Experiment 1: Mice will be randomized into one of six experimental groups 1) control diet; 2) control diet with microbiota depletion; 3) control diet with microbiota depletion and restored inflammatory capacity; 4) Mediterranean diet; 5) Mediterranean diet with microbiota depletion; 6) Mediterranean diet with microbiota depletion and restored inflammatory capacity. The groups undergoing gut microbiota depletion will be provided an antibiotic (Abx) cocktail of streptomycin (2 g/l), gentamicin (0.5 g/l), bacitracin (1 g/l) and ciprofloxacin (0.125 g/l) in autoclaved water ad libitum. LPS will be added in drinking water to at a concentration of 60 mg/ml to restore the inflammatory milieu of Abx treat mice in groups 3 and 6.Experiment 2: Mice will be randomized into one of six experimental groups 1) control diet; 2) control diet supplemented with freeze dried Parabacteroides distasonis, 3) control diet and weekly gavage with live Parabacteroides distasonis; 4) Mediterranean diet; 5) Mediterranean diet supplemented with freeze dried Parabacteroides distasonis; 6) Mediterranean diet and weekly gavage with live Parabacteroides distasonis.Four weeks after beginning diets, mice will be given one dose of the colorectal carcinogen azoxymethane (AOM. 10mg/kg IP) to initiate tumorigenesis. On the fifth (days 35-42) and eighth (days 56-63) weeks mice will be given dextran sulfate sodium (DSS. MWt 36-50 kDa) in drinking water (3%) to promote colitis.Mice will be euthanized after 12 weeks, which is 8 weeks after the AOM injection and 3 weeks after the second DSS cycle. To assess gut "leakiness" all mice will be administered 0.6 mg/g FITC-dextran four hours prior to euthanasia by oral gavage. Mice will be weighed weekly throughout the protocol. We will assess body composition by MRI in the 11th week of the protocol. Stool will be collected weekly and stored frozen. Microbiota depletion in Abx treated mice will be confirmed by routine stool culture and PCR with universal primers.Mice will be euthanized by isoflurane anesthesia combined with exsanguination by cardiac puncture (EDTA tubes) and finally cervical dislocation. The abdomen will be opened and liver and spleen weighed, frozen in liquid N2 and stored at -80°C. The large intestine and cecum will be removed, measured and contents removed and stored. The intestines will then be flushed, opened longitudinally and rinsed thoroughly in cold PBS with protease inhibitors.Colons will be scrutinized under a dissecting microscope for the presence of tumors by an observer unaware to the groups. Tumors will be measured, excised and fixed for later confirmation and grading by a rodent histopathologist.A 0.5cm section will be cut from the center of the colon and fixed in formalin for later histologic analyses. The remaining colon will be scraped with glass slides to collect the mucosa which will then be stored frozen for later analysis of inflammatory markers.Total protein will be isolated from colonic mucosal scrapings with RIPA buffer and quantified using the BCA assay. Cytokines (IL-1b, Tnfa, IL-2, IL-6, IL-8, IL-10, Il-17, Tgfb, Ifng) will be measured in mucosa by ELISA. Mediators of pro-inflammatory signaling MyD88 and IkB phosphorylation (ser32) will be measured in mucosa by western blotting with GAPDH as loading control. Tight junction proteins ZO-1 and occludin will be measured in mucosa by western blotting. Active (non-phospho) b-catenin will be also be measured by western blot.Multiple microscope slides will be prepared from the fixed and embedded colon tissue section: H&E stained slides will be evaluated for histologic inflammation and Disease Activity Index calculated according to established criteria. To assess inflammatory signaling nuclear NF-kB (p65) will be measured by immunohistochemistry. Proliferation and apoptosis will be measured by IHC for Ki-67 and cleaved caspase 3.To assess gut leakiness we will measure blood FITC concentrations (from gavage) in serum with a microplate reader at an excitation/emission wavelength of 485/528nm. In addition, serum endotoxin (LPS) will be measured by the Limulus Amebocyte Lysate assay. Fecal calprotectin will also be measured at 0, 4, 9 and 12 weeks as an additional measure of colonic inflammation.Gut microbial composition will be assessed in stool by 16S rRNA sequencing.

Progress 04/15/21 to 04/14/22

Outputs
Target Audience:The target audience for this work includes scientific researchers, medical practitioners, dieticians and individuals with an elevated risk for colorectal cancer such as the elderly, obese, sufferers of inflammatory bowel disease and those with a family history of colorectal cancer. Changes/Problems:1) In April 2021 Meredith Davis, the original postdoc hired to conduct this project, left my lab to go back to her home state. Due to current conditions I was not able to find a replacement postdoc but was fortunate to recruit Lucia Pham, a technician who had recently been let go by a trusted colleague due to funding shortages. 2) We had some problems with the animal intervention study. We utilized an antibiotic cocktail that is published and verified by us to be safe and effective in a pilot study. However, in the current study we observed an unexpected antibiotic x DSS (colitis agent) interaction that resulted in some mortality of mice. Interstingly, mortality appeared to be diet and sex dependent. We reduced the DSS dosage to minimize mortality and reduced the antibiotic dose. Although these changes mitigated the mortality somewhat they resulted in irregular tumor induction. We are currently scrutinizing the data thoroughly and may adjust the diet and mouse model for the second mouse study as appropriate. Despite weak tumor induction we do expect the microbiome analyses, as well as colon gene/protein expression analyses to be informative. What opportunities for training and professional development has the project provided?Lucia Pham was trainined in mouse models of colitis and colon cancer and mouse diet intervention studies. She is currently undertaking an online microbiology course and learning hands-on culture of anaerbic bacteria in the Tufts Anaerobe laboratory. How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals?In the next reporting period we plan to: 1) complete molecular analyses of mouse tissues collected in the previous period 2) complete data analyses of data collected in the previous period 3) complete the second of two mouse studies described in the proposal as well as all tissue analyses and data analyses

Impacts
What was accomplished under these goals? Unfortunately Meredith Davis, the original post-doc hired to conduct this experiment, left my lab in April 2021 for a new opportunity in her home state. Fortunately I was able to hire a technician, Lucia Pham,to take over the running of these studies. After training Lucia we initiated the first of two animal expereiments described in the proposal. The intervention portion of this 16 week, 6 armstudy was now been completed and all tumors and samples have been collected. Fecal microbiome analyses are underway. Ananlysis of body weight, body composition, food intake and tumor data is also underway. As of Feb 7 2022, Lucia and myself will be moving to Boston Univeristy School of Medicine and continuing these studies there. The stored samples have already been transfered to BUSM and are safely stored in a -80C freezer. The second of the twoproposed anaimal studies will be initiated later in 2022 and in the mean time we will continue molecular analyses of collected tissues to assess various markers of inflammation and otehr pro-tumorigenic changes.

Publications


    Progress 04/15/20 to 03/09/22

    Outputs
    Target Audience:The target audience for this work includes scientific researchers, medical practitioners, dieticians and individuals with an elevated risk for colorectal cancer such as the elderly, obese, sufferers of inflammatory bowel disease and those with a family history of colorectal cancer. Changes/Problems:1) In April 2021 Meredith Davis, the original postdoc hired to conduct this project, left my lab to go back to her home state. Due to current conditions I was not able to find a replacement postdoc but was fortunate to recruit Lucia Pham, a technician who had recently been let go by a trusted colleague due to funding shortages. 2) We had some problems with the animal intervention study. We utilized an antibiotic cocktail that is published and verified by us to be safe and effective in a pilot study. However, in the current study we observed an unexpected antibiotic x DSS (colitis agent) interaction that resulted in some mortality of mice. Interstingly, mortality appeared to be diet and sex dependent. We reduced the DSS dosage to minimize mortality and reduced the antibiotic dose. Although these changes mitigated the mortality somewhat they resulted in irregular tumor induction. We are currently scrutinizing the data thoroughly and may adjust the diet and mouse model for the second mouse study as appropriate. Despite weak tumor induction we do expect the microbiome analyses, as well as colon gene/protein expression analyses to be informative. 3) On 2/7/22 my research team moved to Boston University School of Medicine and we hope to continue with our second mouse study in spring 2022. Animal and biosafety protocols have already been submitted for these studies. What opportunities for training and professional development has the project provided?Lucia Pham was trainined in mouse models of colitis and colon cancer and mouse diet intervention studies. She is currently undertaking an online microbiology course and learning hands-on culture of anaerbic bacteria in the Tufts Anaerobe laboratory. How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

    Impacts
    What was accomplished under these goals? The 3 aims of this project will be addressed through 2 mouse intervention expereiment. - The mouse diet intervention of thefirst experiment (Aim 1) has been completed and all tissues have been harvested and stored. Fecal microbiome alalyses have been completed and data analysis is underway. Analyses of colonic gene expression and systemic inflammation are underway. - As of 2/7/22my research team moved to Boston University School of Medicine. We have submitted an animal protocol and associated biosafety protocol for the second mouse experiment (addressing Aims 2 and 3) and plan to initiate these studies in spring 2022.

    Publications


      Progress 04/15/20 to 04/14/21

      Outputs
      Target Audience:Researchers, Physicians, Nutritionists Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Meredith Davis has learned several new techniques including ELISA, animal handling and LPS measurement. How have the results been disseminated to communities of interest?No data has resulted from the project to date. Once data is obtained it will be disseminated using the regular avenues including publication in peer reviewed journals and presentation at national meetings. In addition, data will be presented at various intramural seminar series. Any omics data will be uploaded to appropriate file sharing locations. What do you plan to do during the next reporting period to accomplish the goals?The proposal describes 2 animal studies. By the next project period we will have completed our pilot study to optimize antibiotic treatment and hope to have initiated the first of the two animal studies. A description of any data in hand will be provided.

      Impacts
      What was accomplished under these goals? Current activities mainly pertain to preparing to performing the experiments described in the proposal. Although Covid has been a major impediment we have made the following progress: 1. A highly skilled postdoc was hired. Her name is Meredith Davis PhD. Meredith was trained and cleared for animal use at Tufts University Meredith has familiarized with the animal protocol Meredith has been trained in relevant lab techniques Meredith has familiarized herself with literature on microbiome and colorectal cancer 2. Animal studies have been scheduled with our animal facility 3. We are working with the diet vendor to revise the Mediterranean Diet to include tomato powder. 4. A small pilot study is being performed currently to optimize anti-biotic treatment regimens

      Publications