Source: OKLAHOMA STATE UNIVERSITY submitted to NRP
ROLE OF THE ANTI-INFLAMMATORY INTERLEUKIN-10 IN ATTENUATING OBESITY AND INSULIN RESISTANCE
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1016774
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Oct 1, 2018
Project End Date
Sep 30, 2023
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
OKLAHOMA STATE UNIVERSITY
(N/A)
STILLWATER,OK 74078
Performing Department
Human Sciences
Non Technical Summary
Chronic inflammation and the corresponding pro-oxidative state produced by activated immune cells damage many tissues that can lead to the development of numerous chronic conditions including insulin resistance (IR), obesity, and type 2 diabetes (T2D). Obesity and T2D are all major health issues in the US particularly in Oklahoma. More than one-third (36.5%) of US adults are obese and Oklahoma was the seventh worst state in the prevalence of obesity. The rise in obesity leads to the development of many chronic conditions including IR, heart disease and T2D. In 2015, 30.3 million Americans (9.4%) had diabetes and another 84.1 million had pre-diabetes. Based on these alarming statistics, it is apparent that obesity and T2D are having a significant impact on the quality of life of many Americans along with the economic burden it represent to our healthcare system. Therefore, it is imperative to understand factors that contribute to obesity and T2D and develop effective prevention and treatment strategies to reduce the impact of these conditions, particularly in Oklahoma. This study will investigate the role of the anti-inflammatory molecule interleukin (IL)-10 in the development of IR.
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
7011549101080%
7021540109020%
Goals / Objectives
Recent findings demonstrate the importance of IL-10 in reducing inflammation in the gut and the skeletal muscle. However, to our knowledge there are limited studies that examined the effects of IL-10 on other tissues important in glucose homeostasis such as the liver and adipose tissue. In addition to IL-10, the western diet (WD, high fat and high sugar)) increases inflammation through its effects on the immune cells particularly T cells and the gut bacterial population. A distinct intestinal microbial population which subsequently alters short chain fatty acid (SCFAs) levels is linked to the development of obesity and T2D. The aims of this proposed study are:Aim 1: To investigate the effects of IL-10 on: a) glucose homeostasis and if the anti-inflammatory effects of IL-10 protect tissues important in glucose homeostasis (e.g. small intestine, liver, adipose tissue, and muscle); and b) the gut bacterial population and SCFAs production and if these changes alter T cell populations within the gut and leads to systemic and tissue inflammation.Aim 2: To identify intervention strategies (e.g. wheat germ (WG) supplementation) that can positively affect the gut microbiome, SCFAs production, and T cell populations which can subsequently attenuate obesity and markers of IR in the context of Western diet and absence of IL-10.These effects will be investigated in wild type and IL-10 knock-out (KO) mouse models under conditions consistent with the normal and Western diet. The approach of using natural products such as WG or their bioactive components to reduce or prevent chronic disorders particularly obesity, IR and T2D has been the long-term goal of our laboratory.
Project Methods
We have designed a series of animal experiments that will enable us to gain an understanding as to how IL-10 protects against obesity and IR. These experiments will also allow us to investigate how the changes in the gut microbiome and subsequent SCFAs production alter T cell populations (e.g. Th17 and T regulatory cells) and if their activation within the gut contributes to systemic and inflammation in tissues vital to glucose homeostasis. Additionally, whether these changes are attenuated by dietary manipulations and its relationship to IR will also be explored. In terms of the dietary factors that will be manipulated, we will investigate the extent to which the Western diet exacerbates or supplementation with WG improves the aforementioned parameters in the absence of IL-10. These experiments will require that we maintain a mouse colony of IL-10 KO mice. Initial breeding pairs of the IL-10 KO mice will be purchased from Jackson Laboratories (Bar Harbor, ME) as well as age- and gender-matched C57BL/6 mice for each experiment.Due to scope of the proposed work and the number of animals required, we have developed our experiments in three phases. In Phase I, we will investigate the effects of IL-10 on glucose homeostasis and the corresponding shifts in T cell population over time under normal dietary conditions. Male IL-10 KO and wild-type (WT) mice will be maintained on a control diet (AIN-93)46 with study end-points at 3 and 6 mos. The earliest time point that demonstrates significant alterations in glucose homeostasis and an inflammatory response will be designated as the single study end-point for all subsequent experiments. In Phase II, a similar experiment will be designed to determine whether the Western diet exacerbates the inflammatory response in IL-10 KO mice. The control or AIN-93 diet will be formulated to provide 10% kcal from fat compared to the Western diet which will provide 45% kcal from fat and be high in refined sugars.46-47 Finally, in Phase III, we will investigate how supplementing the diet with WG will affect the microbiome, increase luminal SCFA, alter T cell population and subsequent alterations in markers of IR.Throughout all experiments, mice will be housed in groups (n=3-4/cage), have free access to deionized water, and will be matched-fed to control for food intake in each mouse strain. Body weights will be recorded on a weekly basis. At the end of each experiment, mice will be anesthetized, undergo a whole body dual-energy x-ray absorptiometry (DXA) scan to assess body composition, and then bled from the carotid artery. An aliquot of whole blood will be used to determine a complete blood count (i.e., total white cell counts and differentials). Serum and tissues important in glucose homeostasis (e.g. muscle, liver, adipose tissue, and gut samples) will be collected. All procedures will strictly adhere to the guidelines set forth by the Oklahoma State University Animal Care and Use Committee. All the methodology proposed in our study will be conducted to accomplish each of the proposed aims listed below.Aim 1:A. To investigate the effects of IL-10 on glucose homeostasis and if the anti-inflammatory effects of IL-10 protect tissues important in glucose homeostasis (e.g. small intestine, liver, adipose tissue, and muscle).B. To investigate the effects of IL-10 on the gut microbiome and SCFAs production and if these changes alter T cell populations (e.g. Th17 and T regulatory cells) within the gut and leads to systemic and tissue inflammation.Aim 2. To identify intervention strategies (e.g. wheat germ supplementation) that can positively affect the gut microbiome, SCFAs production, T cell populations which can subsequently attenuate obesity and markers of IR in the context of Western diet and absence of IL-10.

Progress 10/01/19 to 09/30/20

Outputs
Target Audience:For this reporting period, our activities are mostly training students- graduate (two Ph.D. and one MS) students and two undergraduate students. This project helped train these students in the area of gut microbiome, immunomodulation, and bioactive food components. It also made them understand the research process, get familiar with animal care and different laboratory techniques, read and interpret scientific publications, and present research findings. Changes/Problems:The first yearof the study was focused on the generation of the mice for the study as well as characterization and dietary treatments. We have also conducted various dietary treatment experiments with our mice colonyand started on the analyses of collected samples. However, we had a setback on laboratory analyses due to the university shut down associated with the COVID-19 pandemic. What opportunities for training and professional development has the project provided?This project provided ample opportunities to train both graduate and undergraduate students.Threegraduate and two undergraduate students were involved in the project and exposed to do basic research in the field of nutritional sciences especially those related to immunomodulation by bioactive foods. Students were involved in all aspects of the study including animal care and maintenance of mouse colony, preparation of dietary treatments, necropsy and sample collection, laboratory analyses including clinical chemistry and hormone analyses, gene and protein expression assay, histological analyses, short-chain fatty acid analyses, and statistical analyses. Students were also involved in reading and interpreting related research articles as well as trained to present the research findings. One of the senior graduate students was able to use this project to do an oral presentation. How have the results been disseminated to communities of interest?During this reporting period, we have mostly done data collection. We have not disseminated our findings exccept for one student presentation. What do you plan to do during the next reporting period to accomplish the goals?We will continue with the laboratory analyses of tissue samples obtained from all the experiments that have been conducted. Statistical analyses will also be conducted as soon as the laboratory analyses have been done. Writing the manuscript of our findings as well as presenting our findings to appropriate audiences will also be done.

Impacts
What was accomplished under these goals? Theobjectivesof this research project are to investigate the effects of IL-10 on (1) the maintenance of bacteria-immune homeostasis in the gut, and in the reduction of gut leakiness and bacteremia, (2) modulation of glucose homeostasis and insulin sensitivity, (3) markers of energy metabolism, and (4) maintenance of normal body composition in mice that are fed a high-fat diet. These objectives were investigated using two mouse strains, the wildtype (C57B/L6, WT) and the IL-10 gene knockout (IL-10KO) from the same background. Several experiments and dietary supplementation were conducted during this reporting period: 1. Characterization of the two mouse strains for both genders fed standard rodent diet (AIN-93M) for 3 and 6 months 2. Investigatingthe effects of western diet feeding for three months on these two strains of mice (male mice only) 3. Examining the effects of wheat germ and the role of the gut microbiome in modulating metabolic outcomes in these two strains of mice (female mice only), and 4. An experiment investigating the effects of three months wheat germ supplementation with high-cholesterol containing high-fat diet on both strains of mice (female only) Because of the COVID-19 pandemic, we got behind with our laboratory analyses.We will continue all laboratory analysesand will be seeking opportunities to present our findings at the various professional organizations.

Publications


    Progress 10/01/18 to 09/30/19

    Outputs
    Target Audience:For this reporting period, our efforts are directed toward the training of graduate and undergraduate students in different laboratory techniques as well as reading and interpreting scientific publications. Changes/Problems:Initially, we had a problem starting our mouse colony. We are now able to generate sufficient quantities of mice for our experiments. However, animal housing cost is very expensive and so we have to be strategic on when we breed our mice. What opportunities for training and professional development has the project provided?We have trained two new graduate students, three undergraduate students, and a visiting scholar about working with research animals, establishing a mouse colony, animal diet preparation, understanding basic laboratory techniques, as well as reading and interpreting scientific publications. A Ph.D. student is also benefiting from this project because he is involved in training new students about basic research. How have the results been disseminated to communities of interest?During this reporting period, we have only done data collection. We have not disseminated our findings. What do you plan to do during the next reporting period to accomplish the goals?We will continue with the analysis of tissue samples obtained from the characterization experiments for both males and females, wild type and IL-10 knock-out as well as the two-time points (i.e. 3 and 6 months). We will also start the experiments investigating dietary approaches that can improve or aggravate obesity and insulin resistance. The role of interleukin-10 in obesity and insulin resistance under these various dietary conditions will be examined.

    Impacts
    What was accomplished under these goals? During this reporting period, we have obtained approval to conduct the animal study and started our mouse colony for both the wild-type and IL-10 knock-out mice. After obtaining adequate mice from the breeding colony, we started and finished the 3 months and 6 months characterization experiment comparing male and female as well as wild type and IL-KO mice. Food intake, weekly body weight, body composition, glucose tolerance tests, and tissue weights were obtained from these experiments. Laboratory analyses are currently being conducted.

    Publications