Source: UNIV OF MARYLAND submitted to
ROLE OF THE GUT MICROBIOTA ON THE BENEFICIAL EFFECTS OF THE VEGETABLE URTICA DIOICA AS A FUNCTIONAL FOOD
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
ACTIVE
Funding Source
Reporting Frequency
Annual
Accession No.
1025387
Grant No.
2021-67017-34025
Cumulative Award Amt.
$431,407.00
Proposal No.
2020-04436
Multistate No.
(N/A)
Project Start Date
Jan 1, 2021
Project End Date
Dec 31, 2024
Grant Year
2021
Program Code
[A1343]- Food and Human Health
Project Director
Obanda, D.
Recipient Organization
UNIV OF MARYLAND
(N/A)
COLLEGE PARK,MD 20742
Performing Department
Nutrition & Food Science
Non Technical Summary
The gut microbiota is a community of different bacteriagroups that live in our guts and have a large impact on our health. It is linked to several health conditions. Changes in microbiota composition can result in disease. Obesity is an example of a disease that can precipitate from a changed microbiota. A high fat (HF) or high calorie diet can negatively change the gut microbiota composition and reduce the number of different groups of bacteria present in the microbiota. When the microbiota is composed of many different bacterial groups it means the diversity is high and it is healthy. When the number of different bacterial groups decrease, then it means diversity is lowered and this is not associated with good health.Urtica dioica L (UT) grows widely in North America and is used in different international cultures as a vegetable. In our preliminary study, UT vegetable prevented high fat diet induced fat accumulation and insulin resistance. Furthermore, it prevented HF diet induced reduction in health and diversity of gut bacteria and enhanced the proliferation of bacterial species that are associated with health, particularly weight reduction and gut health. The vegetable also induced changes in the immune system. About 80% of our immune system is located in the gut. The bacteria affect how this immune system works to protect us against various diseases.We hypothesize that the effects of UT on the microbiota influences the absorption of dietary fat in the small intestines and therefore the amount of fat that accumulates in fat tissue and liver. We further hypothesize that the effects of UT on the composition of bacterial groups in the gut are behind its impact on fat accumulation i.e reduction in obesity. To test these hypotheses, in Aim 1, we will feed mice diets with or without UT. We will analyze the composition and diversity of gut microbiota in the small intestine and amount of fat absorbed. In Aim 2 we shall study the effect of UT on the immune system and how this is connected to shaping the bacteria composition. The primary outcome of this project is generating new knowledge on how UT benefits the host in terms of a healthier gut bacteria community, a healthier immune system and prevention of obesity.We will disseminatethis information to health scientists, nutrition scientists, the food industry and the agricultural sector with the aim of promoting UT or introducing it as a speciality agricultural crop and vegetable with significant health benefits.
Animal Health Component
0%
Research Effort Categories
Basic
80%
Applied
0%
Developmental
20%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
70214301010100%
Goals / Objectives
GOAL: The goal of this project is to determine the effect of Urtica dioica (UT) vegetable on gut microbiota health, intestinal immune cell phenotype and how these relate to fat absorptionand inflammation. There are two objectives.Objective 1: Determine the effects of UT vegetable on small intestine microbiota composition and diversity and how this relates to fat absorption and accumulation. We hypothesize that UT components attenuate high fat diet induced loss in bacterial diversity, increase the proliferation of specific beneficial species and reduce the amount of dietary fat absorbed and/or assimilated.To test this hypothesis, we will feed mice isocaloric diets with or without UT vegetable and analyze the small intestinal microbiota composition by sequencing the 16S rRNA gene and by targeted nonculture qPCR. We will quantify triglycerides in fecal samples and gene and protein expression or activity of proteins involved in fat absorption, fat transport, lipogenesis, lipolysis and fatty acid oxidation in intestinal tissue, adipose and liver. After identifying bacterial species whose proliferation is enhanced or inhibited by UT vegetable, we will test the effect of these bacterial species on fat absorption using in vitro mouse enteroid cultures. We will aim at completing the work described in this objective within the first two years of the project (First 24 months) Objective 2: Determine the effects of UT vegetable on the intestinal Treg cell-IgA axis and ultimate impact on bacterial diversity and intestinal inflammation. We hypothesize that the changes observed in the microbiota composition and diversity are induced by effects of UT vegetable on the phenotype of intestinal regulatory T cells (Tregs) and on immunoglobulin A (IgA) antibody secretion and actions of IgA.To test this hypothesis, we will obtain fresh intestinal contents and intestinal tissues from mice fed diets with or without UT vegetable. We will quantify IgA coated and uncoated bacteria using flow cytometry. We will separate IgA coated and uncoated bacteria and identify taxa in each fraction by 16s sequencing. From isolated single-cell suspensions of lamina propria immune cells we will quantify IgA+ cell populations and T cells that express the biomarkers CD4, FOXP3 and CD25. CD4+CD25+FOXP3+Tregs play an essential role in intestinal homeostasis and inflammation. We will aim at completing the work described in this objective within the next 1.5 years of the project (month 25-42).Between months 43-48 we shall be working on reports, publications and conference presentations that involve this work. We anticipate to generate 4 publications that we will send to Nutrition journals.We will also seek collaborators for a further project aimed at testing the vegetable in a human clinical setting, i.e translate the findings in a clinical study.
Project Methods
Objective 1 will be divided into 3 parts (1.1, 1.2, 1.3) for methodsObjective 1.1. Determine the effect of UT vegetable on SI microbiome communityAnimal studyWe will use eight-week-old age matched 45 male and 45 female C57BL/6J mice (Jackson labs). Males and females will be separately randomised to 5 groups of 9. Each experimental group will have 9 males and 9 females. All diets will be formulated to be isocaloric. Group 1: Low fat (LF) diet control Group 2: Low fat (LF) diet plus UT (LFUT)Group 3: High fat (HF) diet controlGroup 4: HF diet plus UT (HFUT)Group 5: HF diet plus UT and AVNM antibiotic regimeLF=10 % fat, HF =45% fatSamples collected, variables monitored and determinedFood intake, body weight, insulin resistance, glucose metabolism and fat accumulation will be determined by standard tests.Bacterial DNA will be isolated from the duodenum and jejunum contents. Microbiota membership will be analyzed by 16S rRNA sequencing and Bioinformatics. To identify organisms that correlate with and account for the major differences between microbiota communities, we will perform a random forest analysis of the 16SrRNA data.Objective 1.2. Determine the effect of UT vegetable on tissue markers of fat absorption, lipolysis, fat oxidation and lipogenesis.Tissues collected and analyzed for objective 1.2 will be serum, colon fecal samples, cecal contents, small intestine (SI) tissue, epididymal fat, skeletal muscle and liver. We shall determine:Triglyceride (TAG) content in the fecal and cecal contents to determine the extent of intestinal fat absorption.TAG and free fatty acid content in serum, small intesrtine tissue,liver and muscle.Gene expression and protein expression of proteins involved in lipid transport, TAG formation/lipogenesis, lipolysis, fatty acid oxidation in SI tissue, liver, adipose and skeletal muscle.Objective 1.3. Determine the effect of UT extract on fat absorption in vitro assays using small intestine enteroids16S sequencing will reveal species whose proliferation is enhanced by UT and species whose proliferation is inhibited by UT. We will culture 2 species whose proliferation is most highly increased and two species whose proliferation is inhibited by UT vegetable. From these four cultures we will obtain 'conditioned media' for subsequent experiments below.Intestinal crypts will be isolated (at euthanasia of animal study) and duodenum enteroids cultured and differentiated and used to create 2D monolayers in Trans well plates with 0.4 μm pore polycarbonate membrane inserts. Confluent monolayers will be used to study absorption of lipids.Bacteria will be grown in media with or without the ethanolic/water extract of UT under anaerobic conditions for 48 hours after which filtered conditioned media which we presume contains bioactive metabolites from the bacteria and UT vegetable, will be collected and pooled. Control media will have no bacteria seeded in it.The conditioned media will be divided into 2: one part will be supplemented with 300uM final free fatty acids (FFAs/palmitic acid) bound to BSA to mimic a HF dietary conditions in vitro. Enteroids not receiving FFAs will be treated with BSA only. The conditioned media will be added to enteroid monolayers for 24 hours. In summary, the enteroids will be exposed to: control media with no bacterial metabolites and no excess FFAs, control media with no bacterial metabolites but with excess FFAs, media with bacterial metabolites but no excess FFAs, media with bacterial metabolites and excess FFAs. About 50ul of conditioned or control media will be added to 450ul of enteroid growth media (10% final concentration). This treatment will be separately done with 2 bacterial species whose abundance is identified to be most highly increased by UT in the small intestine and 2 species whose abundance is most highly decreased.After 48 hours, enteroids will be harvested and analyzed for gene and protein expression for:Enzymes that catalyze uptake of fatty acids and the re-synthesis of TAG in enterocytes.Proteins that stimulate secretion of pancreatic enzymes in response to nutrients.Proteins that influence lipoprotein formation, chylomicron formation, regulate fatty acid β oxidation and fatty acid oxidation in intestine.Enteroid monolayers will enable measurement of fats in both the apical compartment and the basolateral compartments. Lipids in the media from each compartment will be extracted by the Folch partition and amounts of FFAs and triglycerides quantified by gas chromatography and colorometric kits. TAGs in the enteroid monolayer cells will be extracted and quantified similarly.Objective 2 will be divided into 2 parts (2.1, 2.2).Objective 2.1. Determine the effect of UT on proportions and taxa of immunoglobulin+ (IgA+) bacteriaWe will obtain fresh small intestine contents and scrapings from mice fed isocaloric diets with or without UT from the same animals used in objective 1 and perform the following tests:Quantify IgA levels- secretoryIgA (sIgA) in the intestinal contents and fecal contents will be quantified using an IgA-specific mouse ELISA kit.Flow cytometric quantification of IgA-bound bacteria-small intetinal contents will be processed to isolate the bacterial pellets. Pellets will be stained with anti-mouse IgA fluorophore-conjugated antibody and then SYBR green before analysis by flow cytometryto quantify IgA coated bacteria.Small intestinal contents will be processed to separate bacteria. The supernatant (with bacteria) will be centrifuged, washed with 0.1% (v/v) BSA. Streptavidin magnetic beads will be used to coat the samples with biotinylated anti-mouse IgA. Using a magnet, IgA bound bacteria will be separated from the unbound bacteria.Samples with IgA-bound and IgA unbound bacteria will be separately processed for DNA extraction and 16S rRNA sequencing and bioinformatics to identify bacterialtaxa targeted for IgA coating and those not coated byIgA.From the 16S rRNA data, we will use a random forest analysis to identify species or taxa whose IgA binding status is changed by UT diet and account for the major differences between HF and HFUT microbiota communities.Objective 2.2. Determine the effect of UT vegetable on intestinal immune cell phenotype and intestinal inflammationWe will obtain primary intestinal tissues, small intestinal mucosal scrapings and fresh fecal samples from mice fed isocaloric diets as shown in Objective 1. The small intestinal lamina propria cells will be isolated and processed to separate the epithelial cell fraction. The cell suspension will be filltered to obtain single-cell suspensions for use in flow cytometry as shown next:Identify and quantify IgA+ cells-using fluorophore-conjugated antibodies we will determine if UT induces changes in intestinal B cell populations. Isolated single-cell suspensions of intestinal lamina propria immune cells will be sorted to quantify frequency and absolute numbers of IgA producing B (IgA+ B220+) and plasma (IgA+ B220−) cells.Identify and quantify Treg cells-we will quantify markers of natural Treg cells and adaptive/induced Treg cells. This will include Foxp3+, CD25+, CD4+ cells.Protein and gene expression of inflammatory and anti-inflammatory cytokines-we will determine the expression of IL-10, ICOS, TGF-β in the mucosal scrapings and in LP cells.Foxp3+ immunohistochemistry- small intestinal tissue will be fixed in formalin, embedded in paraffin and autostained with Foxp3+ polyclonal antibody.Slides will be counterstained with haematoxylin and evaluated to enumerate Foxp3+ cells.

Progress 01/01/23 to 12/31/23

Outputs
Target Audience:1. Nutrition Scientists who are my peers-I presented information about the Project findings at a Scientific conference: American society of Nutrition. 2. Young persons (middle school) -I participated in a career day at an Middle school where my son goes to school(6th graders). Imade a presentation about careers in the field of 'Nutrition'. As an example of a functional food I talked about Nettle (UT) as a food that is eaten in several international cultures but is not widely known In the USA. I talked about what it contains and how it prevents disease. The goal was to inspire the next generation of researchers and encourage young people to enter the field of Nutrition, with the goal of preventing common diseases impacting society or communities today. 3. Local Community: I participated in a community event in my local county where I live (Laurel, MD)and promoted the concept of Food for prevention of disease. I gave a lay presentation of my findings after researching Nettle (UT) as a food. I encouraged participants to try nettle as a Tea or vegetable. Changes/Problems:No problems were encountred with this project. Everything is on schedule. However the collaboration established under the NIFA-BARD Cooperation has not yielded much fruit yet becuse a war broke out in Israel/Palestine right after we worked out all the logistics. As a result, research work in Israel came to a standstill. The Israeliscientists and I hope to pursue this further once the situation improves in that part of the world. What opportunities for training and professional development has the project provided?One undergraduate student and two graduate students have been trained and mentored in research skills, writting skills and research presentation skills.This work has contributed to training of the next generation of scientists in the Nutrition Field. Skills learned include (i) the culture and maintenance of intestinal 3D cells (enteroids) and using them in nutrition research, (ii) use of Flow Cytometry to study the role of food components on the immune system (iii) use of OMICs technologies to study the composition and function of the gut microbiota; particularly metagenomics and transcriptomics (on bacterial RNA and host RNA). How have the results been disseminated to communities of interest?I have presented the research at twonational meetings to Scientists who are peers. I participated in a community event in the county where I live and gave lay presentation to the general population on the role of Food in prevention of disease. Ithen gave UT vegetable as an example of a healthy food that is not well known and can protect against many diseases impacting society today. I edited the Education/Teaching material that Iprepared (reported in 2022) and aimed at Dieticians and young people (high school age). This material aimsto educate them about Nutrition as a career and then used UT vegetable as an example of a healthy food that canbe taken as a Tea or a new vegetable. What do you plan to do during the next reporting period to accomplish the goals?Complete pending laboratory experiments /analysis of tissues collected from the animal studies. Write up a 3rd manuscript from the work and submit to a peer review Journal. Present the workat aconferance in July 2024. Follow-up on the target audience for the education material I prepared in 2022. Basically reinforcing importance of Food in prevention or protection from disease. Further pursue the collaboration with Hebrew University (NIFA-BARD Cooperation) to test other types of Nettle in Prevention of disease.

Impacts
What was accomplished under these goals? Objective 1: We have completed Objective 1. The animal study is complete and we have profiled the gut microbiota composition. We have tested the impact of specific bacteria on fat absorption when study subjects (mice or intestinal 3D cells) are exposed to excess fatty acids (to miminc excess dietary intake of fat). We have shown that some bacterial species whose outgrowth is promoted by UT vegetable do attenuate the amount of fat absorbed and hence reduce obesity. A manuscript with this findings has just been accepted by the Journal of Nutritional Biochemistry and we presented findings at the American Society of Nutrition (ASN) meeting held in July 2023 in Boston, MA. Objective 2:Most of the tissue analysis has been completed. We have shown that UT promotes intestinal immune function. Enhances the representation of IL-10 and TGF-B producing CD4+ Foxp3+ T cells while downregulating the representatioion of IFN-gsecreting cells.Amanuscript with this findings has just been accepted by the Journal of Nutritional Biochemistry and we are preparing to present new findings at the American Society of Nutrition (ASN) meeting which will be held in Chicago, IL in2024.

Publications

  • Type: Journal Articles Status: Awaiting Publication Year Published: 2024 Citation: Impacts of the vegetable Urtica dioica on the intestinal T and B cell phenotype and macronutrient absorption in C57BL/6J mice with diet-induced obesity. The Journal of Nutritional Biochemistry. In press
  • Type: Conference Papers and Presentations Status: Published Year Published: 2023 Citation: Urtica dioica whole vegetable attenuates diet-induced obesity via mechanisms involving nutrient absorption and immune cell function in the small intestines.


Progress 01/01/22 to 12/31/22

Outputs
Target Audience:Nutrition Scientists who are my peers. I presented information about the Project findings at two scientific conferences: (i). Obesity Society (ii) American society of Nutrition. I participated in career day at an Elementary school (5th graders) and made apresentation about careers in the field of 'Nutrition'. As an exampleof a functional food I talked about Nettle (UT) as a food that is not widely known and how beneficial it is to prevent disease. The goal was to inspire the next generation of researchers and encourage young people to enter the field of Nutrition, with the goal of preventing common diseases impacting society or communities today. I prepared a career guidance document targeting Dieticians and High school students on the benefits of Nettlle (UT) as a Food. The Document was shared with educators in the USA and in Britain. It is on various media outlets and social networks such as Linkedin, Facebook, Pinterest and Twitter. It can be found here:https://www.tes.com/teaching-resource/resource-12827490 Changes/Problems:No major changes were made. What opportunities for training and professional development has the project provided?Two students and one postdoctoral fellow have been trained and mentored in the researchskills, laboratory methods required to complete this work. This work has contributed to training of the next generation of scientists in the Nutrition Field. Skills learned include (i) the culture and manitenance of intestinal 3D cells (enteroids) and using them in Nutrition research, (ii) use of Flow Cytometry to study the role of food componentson the immune system (iii) use of OMICs technologies to study the composition and function of the gut microbiota; particularly metagenomics and transcriptomics (on bacterial RNA and host RNA). How have the results been disseminated to communities of interest?I have presented the research at a national meeting to Scientists who are peers. I have prepared an Education/Teaching material aimed at Dieticians and young people (high school age) to educate them about Nutrition as a career and then used UT vegetable as an example of a healthy food that is not well known and can protect against many diseases impacting society today. What do you plan to do during the next reporting period to accomplish the goals?Complete pendinglaboratory experiments /analysis of tissues collected from the animal studies. Write up a second manuscript from the work and submit to a peer review Journal. Follow-up on the target audience forthe education material Iprepared. Basically reinforcing importance of Food in prevention or protection from disease.

Impacts
What was accomplished under these goals? Objective 1: Determine the effects of UT vegetable on small intestine microbiota composition and diversity and how this relates to fat absorption and accumulation. We have completed Objective 1. The animal study is complete and we have profiled the gut microbiota composition. We have tested the impact of specific bacteria on fat absorbtion when study subjects (mice or intestinal 3D cells) are exposed to excess fatty acids (to miminc excess dietary intake of fat). Wehave shown that some bacterial species whose outgrowth is promoted by UT vegetable do attenuate the amount of fat absorbed and hence reduce obesity. A manuscript is under preparation and we are preparing to present the data at the American Society of Nutrition (ASN) meeting to be held in July 2023 Objective 2: Determine the effects of UT vegetable on the intestinal Treg cell-IgA axis and ultimate impact on bacterial diversity and intestinal inflammation. We are currently working on Objective 2. Animal study has been completed but we are analysisng the Tisssues collected and compling data.

Publications

  • Type: Other Status: Published Year Published: 2022 Citation: https://futurumcareers.com/could-a-nettle-a-day-keep-the-doctor-away
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Metagenomic insights into the effects of Urtica dioica vegetable on the gut microbiota of C57BL/6J obese mice, particularly the composition of Clostridia


Progress 01/01/21 to 12/31/21

Outputs
Target Audience: Scientists in the field of Agriculture -the goal is to educate them on the benefits of this vegetable as a functional food. To promote, introduce and/or expand the cultivation of UT which is currently considered just a weed and nuisance crop. The Food industry - educate industry about the health benefits of UT as a vegetable. The aim is to promote manufacture of prebiotics food products based on UT vegetable or products that contain UT vegetable as part of the formulation. Nutrition Scientists-These scientific findings will be published in top Nutrition journals such as 'Molecular Nutrition & Food Research' and 'Nutrients' which possess a large number of readers from academia and industry. These journal publications will inform the scientific community of the potential health benefits associated with UT vegetable as well as inspire additional investigations on this vegetable. Particularly scientists involved in clinical studies involving interventions for metabolic health Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Two graduate students have been trained and mentored in the research skills required toaccomplish this work. This workhas contributed to training of the next generation of scientists in the nutrition field. How have the results been disseminated to communities of interest?We are preparing a manuscript to submit to a Nutrition Journal that has a wide redaership: Molecular Nutrition Food research What do you plan to do during the next reporting period to accomplish the goals?We will be working to complete Aim 1 by performing the following experiments: Gene and protein expression and activity proteins involved in fat absorption, fat transport, lipogenesis, lipolysis and fatty acid oxidation in intestinal tissue, adipose and liver. Gene and protein expression and activity proteins involved in fat absorption, fat transport, lipogenesis, lipolysis and fatty acid oxidation in enteroids treated with UT extract or Clostridium media as source of metabolites. QPCR quantification on specific bacterial taxa or species of interest identified by 16S sequencing to complement the 16S sequencing data. Bioinformatics using Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUST) to make inferences of the functional profile of the microbial communities to determine differences that are responsible for phenotypic changes among the animals fed different diets. Preparation of a manuscript to submit by June 2022.

Impacts
What was accomplished under these goals? We worked out the logistics of carrying out this project particularly Objective 1 and have almost completed it. So far we have performed experiments under Objective 1 to test the hypothesis. Because our preliminary study (as shown in the grant application) utilized 9% UT, before performing the experiments described under objective 1, we performed a dose response study to determine whether a lower amount of dietary UT has equivalent effects. We established that a lower dose of UT (4%) imparts beneficial effects (lower body weight and prevention of insulin resistance). In a second animal study using the lower dose, we determined intestinal microbiota composition by sequencing the 16S rRNA gene, targeted nonculture qPCR and bioinformatics. We showed that UT increased the abundance of class Clostridia while lowering class Bacilli. Particularly UT changed the composition of Clostridia by enhancing the abundance of species among genus Clostridium in both the small intestine and cecum contents. Using intestinal (jejunum) mouse enteroids we studied how phytochemicals of UT and bioactive compounds produced by Clostridium impact fat and glucose absorption. We showed that the phytochemicals in UT do not reduce fat or glucose absorption in the small intestines but, the bioactive compounds produced by Clostridium do so. Thus we elucidated a mechanism by which dietary UT attenuates diet induced obesity; it elicits an increase in Clostridium and this results in less absorption of the excess nutrients provided in a high fat diet.

Publications