Source: TEXAS A&M UNIVERSITY submitted to NRP
PROMOTION OF LIPID ACCUMULATION IN ADIPOSE TISSUE BY GPR43 AND OLEIC ACID
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1018749
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Feb 23, 2019
Project End Date
Feb 23, 2024
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
TEXAS A&M UNIVERSITY
750 AGRONOMY RD STE 2701
COLLEGE STATION,TX 77843-0001
Performing Department
Animal Science
Non Technical Summary
Beef cattle deposit large quantities of lipids within their adipose tissue depots even following the age-related decline in lipogenic enzyme activities and expression of genes associated with adipogenesis and de novo fatty acid biosynthesis. We hypothesize that in beef cattle, subcutaneous (s.c.) adipose tissue continues to accumulate lipid by depressing lipolysis via activation of the G-coupled protein receptor 43 (GPR43) by volatile fatty acids (VFA) and oleic acid. Conversely, acetate and potentially other VFA may promote lipolysis in intramuscular (i.m.) adipose, which is strongly antagonized by oleic acid, thereby promoting i.m. adipose tissue development. Oleic acid can be produced either by neighboring adipocytes or by adjacent muscle fibers.Oleic acid appears to act as an autocrine/paracrine factor to promote lipid filling of i.m. adipose tissue. Thus, grain-based diets increase oleic acid in bovine tissues, which in turn may promote additional lipid filling in i.m. adipose tissue. We believe the studies outlined in this proposal will not only provide information on the expression and activation of GPR43 receptors in bovine adipose tissues but also will elucidate a novel mechanism by which GPR43 affects i.m. adipose tissue growth (and thereby increase carcass quality). If GPR43 truly antagonizes the lipolytic effects of acetate in i.m. adipose tissue, then this research could lead to different nutritional strategies that would increase oleic acid intake and/or endogenous synthesis of oleic acid. Alternatively, it may be possible to identify ligands (natural or synthetic) that promote GPR43 activity in i.m. adipose tissue. Thus, an increased understanding of key differences between i.m. and s.c. adipose tissues could allow for specific technologies to be developed that would increase marbling, concomitantly increasing carcass quality and healthfulness of beef and beef products. If we can confirm that i.m. adipose tissue has different responses to VFA and oleic acid than s.c. adipose tissue, then this will allow producers for the first time to specifically target increases in marbling while not exacerbating carcass fatness in beef cattle.
Animal Health Component
20%
Research Effort Categories
Basic
80%
Applied
20%
Developmental
0%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
30233101030100%
Knowledge Area
302 - Nutrient Utilization in Animals;

Subject Of Investigation
3310 - Beef cattle, live animal;

Field Of Science
1030 - Cellular biology;
Goals / Objectives
1. Establish the interactions among individual VFA (acetate, propionate, and butyrate) and between VFA and the LCFA stearic acid (18:0) and oleic acid for the GPR43 receptor in short-term (1 h) ex vivo incubations of bovine i.m. and s.c. adipose tissues.2. Document the interactions among VFA and the LCFA on GPR mRNA and protein expression in a long-term (48 h) bovine i.m. and s.c. ex vivo adipose tissue explant system.3. Establish the effects of VFA and LCFA on AMPKa mRNA and protein expression to provide additional mechanisms by which ligands for the GPR receptors promote TAG accumulation in long-term (48 h) bovine i.m. and s.c. adipose tissue explant cultures.4. Document the effects of VFA and LCFA on cAMP concentrations and lipolysis (glycerol release), lipogenesis (short-term incubations), adipogenic/lipogenic gene expression, and GPR and AMPKa gene and protein expression (long-term incubations) in i.m. and s.c. adipose tissues taken from Angus steers at 12, 16, and 20 mo of age. These ages represent lean, normally-fattened, and overly-fattened beef cattle.
Project Methods
Interactions among VFA and LCFA - Initial Studies. During the first years of the project, we will establish interactions among VFA (acetate, propionate, and butyrate) in the absence and presence of LCFA (oleic and stearic acid) on the depression or stimulation of cAMP production and glycerol release. Adipose tissue samples will be taken from the 5th-8th longissumus thoracis muscle rib section (described below) and used in preliminary experiments to determine interactions among VFA and LCFA on cAMP production and media glycerol. Once dose-response curves have been established for each of the VFA and LCFA independently, experiments will be designed to document the interactions among VFA and LCFA.Source and Production of Steers (Objective 3). Steers for the proposed experiments will be obtained from the TAMU McGregor Research Center. Calves will be weaned at 6 mo of age and will be allowed to forage free choice on native pastures. At 8 mo of age, the steers will be adapted gradually to a corn/milo-based finishing diet (Smith et al., 2012). Steers will be slaughtered at 12, 16, and 20 mo of age (8 for each age group); we estimate the cattle will grade USDA Select, low Choice, and high Choice at 12, 16, and 20 mo of age, respectively. All calves will be adapted to Calan gates and individually fed until their respective sampling time. With this design, animal will be the experimental unit.Obtaining Adipose Tissues from Cattle. Steers will be transported to the TAMU Rosenthal Meat Science and Technology Center and fasted overnight with free access to fresh water. Cattle will be slaughtered by standard industry practices. The 5th-8th longissimus thoracis rib muscle section will be removed immediately following exsanguination by cutting through the hide (approximately 10 min post-exsanguination) (Miller et al., 1989; May et a., 1994).Short-term Incubations. Fresh adipose tissue pieces (estimated to be 50-100 mg) will be transferred immediately to 6-well culture plates containing 3 mL of the KHB/Hepes/5 mM glucose media. Samples will be pre-incubated with 0.5 mM theophylline plus 10 µM forskolin for 30 min in a CO2­ incubator, after which increasing concentrations of acetate, propionate, or butyrate in the absence and presence of increasing concentrations stearic or oleic acid will be added to the incubation media. Following an additional 30 min incubation, adipose tissue samples will be transferred to pre-tared tubes containing lysis buffer.Explant Cultures. Fresh i.m. and s.c. adipose tissue explants will be cultured as described previously (Miller et al., 1989; May et al., 1994). Treatment medium will be without or with addition of the optimal concentrations of VFA and LCFA. Adipose tissues will be incubated for 48 h, which we have demonstrated to be sufficient time to elicit changes in GPR expression (Table 1). Adipose tissue pieces will be removed after 48 h and frozen at -80°C until mRNA are extracted for the measurement of gene expression.Measurement of Tissue cAMP and Media Glyerol. Tissue cAMP concentrations in adipose tissue samples will be measured using the Cyclic AMP XP Assay Kit (Cell Signaling Technologies, Danvers, MA). Media glycerol will be measured with the Glycerol Assay Kit (Sigma-Aldrich, St. Louis, MO).RNA Extraction of Adipose Tissues. Total RNA will be extracted with Tri Reagent (Sigma Chemicals, St. Louis, MO), as reported previously (Brooks et al., 2011a). Complementary DNA (cDNA) will be produced from 1 μg RNA using TaqMan Reverse Transcriptase Reagents (Applied Biosystems, Foster City, CA) The cDNA samples produced at TAMU will be shipped on dry ice to TTU for quantitative real-time PCR (qRT-PCR).qRT-PCR. Quantitative RT-PCR will be used to analyze the expression of AMPKa, C/EBPβ, FASN, PPARg, SCD, and GPRs 40, 41, 43, and 120 (Chung et al., 2016). The 40S ribosomal protein S9 (RPS9) will be used as an endogenous gene expression control. The ABI Prism 7000 detection system (Applied Biosystems) will be used to perform the assay utilizing the thermal cycling variables recommended by the manufacturer (50 cycles of 15 s at 95°C and 1 min at 60°C).AMPK expression. Phosphorylation of AMPK will be analyzed from short- and long-term incubations of s.c and i.m. adipose tissues treated with VFA and LCFA. Total protein will be extracted and immunoblotted with anti-phosph-AMP-activated protein kinase (pAMPK) and anti-AMPK.

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

Outputs
Target Audience: Nothing Reported Changes/Problems:The COVID-19 pandemic delayed the progress on this project approximately three months. Otherwise, there is nothing to report. What opportunities for training and professional development has the project provided?During this reporting year, one Master of Agriculture student, one Doctor of Philosophy student, and one postdoctoral student were trained in obtaining viable adipose tissue from carcasses and all of the laboratory techniques necessary to accomplish the stated goals of this project. How have the results been disseminated to communities of interest?A manuscript describing the results from the cattle sampled at 14 months of age has been submitted to the Journal of Animal Science. What do you plan to do during the next reporting period to accomplish the goals?1. We will complete the measurement of AMPKa gene and protein expression in tissues from long-term i.m. and s.c. adipose tissue explant cultures. 2. We will complete the measurement of gene expression in adipose tissues from long-term expression. 3. We will submit an abstract to the 2021 annual meeting of the American Society of Animal Science. 4. We will submit a second manuscript describing the results of our additional measurements to the Journal of Animal Science.

Impacts
What was accomplished under these goals? 1. We established that acetate and propionate differently affect cAMP production in ex vivo explants of bovine i.m. and s.c. adipose tissue. Acetate is more effective depressing cAMP in i.m. adipose tissue than in s.c. adipose tissue, indicating a greater abundance of GPR43 receptors in i.m. adipose tissue. Propionate had no effect on cAMP production in either adipose tissue, and oleic acid attenuated the effects of acetate in i.m. adipose tissue only. Conversely, palmitic acid strongly depressed cAMP production in s.c. adipose tissue, but not in i.m. adipose tissue. These results provide strong evidence for different populations of GPR receptors in i.m. and s.c. adipose tissue. 2. Work in still in progress to measure AMPKa gene and protein expression in tissues from long-term i.m. and s.c. adipose tissue explant cultures. 3. Due to the COVID-19 pandemic, cattle were processed 2 mo later than proposed, i.e., they were processed at 14, 18, and 22 mo of age. Work is in progress to measure gene expression in adipose tissues from long-term expression, but cAMP, glycerol, and nonesterified fatty acids have been measured in adipose tissues from short-term incubations.

Publications

  • Type: Journal Articles Status: Submitted Year Published: 2021 Citation: Evidence for functional G-coupled protein receptor 43 in subcutaneous adipose tissue and intramuscular adipose tissue of Angus crossbred steers. Journal of Animal Science


Progress 02/23/19 to 09/30/19

Outputs
Target Audience: Nothing Reported Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?One doctoral student and one postdoctoral student have been trained by the PI (Smith) in the procedures of sample collection, in vitro incubations, and measurement of metabolites. 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?We will establish the interactions among stearate and oleate and the volative fatty acids butyrate and propionate in intramuscular and subcutaneous adipose tissue (Objective 1). We will complete Objective 3 in the next fiscal year and Objective 4 in the subsequent fiscal year. We have the necessary cattle for Objective 4 on feed and the first cattle will be sampled May 2020. Objective 2 (cell culture studies) is ongoing.

Impacts
What was accomplished under these goals? We have initiated studies to establish interactions among VFA (acetate, propionate, and butyrate) in the absence and presence of LCFA (oleic and stearic acid) on the depression or stimulation of cAMP production, PKA activity, and glycerol release. We have obtained intramuscular and subcutaneous adipose tissue samples from 4 steers processed from another study conducted at the TAMU Rosenthal Meat Science and Technology Center. Adipose tissue samples were taken from the 5th-8th longissumus thoracis muscle rib section (described below). These samples were used in preliminary experiments to determine interactions among VFA and LCFA on cAMP production, media glycerol, and tissue PKA activity. We were able to demonstrate that oleic acid, in combination with acetate, depresses PKA activity in both intramuscular and subcutaneous adipose tissue in the explant culture system (Objective 1).

Publications