Source: UNIVERSITY OF TENNESSEE submitted to NRP
THE ROLE OF LCORL IN THE EPIGENETIC PROGRAMMING OF ANIMAL GROWTH
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
ACTIVE
Funding Source
Reporting Frequency
Annual
Accession No.
1022854
Grant No.
2020-67015-31342
Cumulative Award Amt.
$499,354.00
Proposal No.
2018-07010
Multistate No.
(N/A)
Project Start Date
Jun 15, 2020
Project End Date
Jun 14, 2025
Grant Year
2020
Program Code
[A1231]- Animal Health and Production and Animal Products: Improved Nutritional Performance, Growth, and Lactation of Animals
Recipient Organization
UNIVERSITY OF TENNESSEE
2621 MORGAN CIR
KNOXVILLE,TN 37996-4540
Performing Department
Department of Animal Science
Non Technical Summary
Understanding of genetic, biochemical, and physiological interrelationships influencing animal growth and development is essential for improving the efficiency of production for our livestock species. The relationship between the deposition of muscle and adipose tissue are at the core of production efficiency of animal protein. Molecular variation within the LCORL gene provides a unique opportunity to potentially define key events during animal development that appear to have continued effects throughout the growth phase of production, especially in muscle and adipose tissue. Characterizing the mechanism by which this genetic variation influences the function of downstream gene networks to modify animal growth will provide insight to both genetic and environmental factors that can be used to improve production efficiency in cattle. However, the significance of understanding this phenomenon extends beyond cattle as there is significant evidence that regulation of these genetic mechanisms are likely conserved among species. Thus, the proposed research will provide fundamental knowledge that has the potential to have a much broader impact on our understanding ofanimal biology as well as improve the production efficiency of livestock species.
Animal Health Component
(N/A)
Research Effort Categories
Basic
80%
Applied
(N/A)
Developmental
20%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
3043310105033%
3033320104033%
3083399108034%
Keywords
Goals / Objectives
Over-Arching Goal.The overall objective of this proposal is to understand how LCORLis able to exert its effects on animal growth and composition. Successful completion of this work will provide insight to both genetic and environmental factors that can be used to improve production efficiency in cattle and provide fundamental knowledge about animal growth that has the potential to increase the efficiency of animal protein production in several species. Furthermore, the fundamental knowledge gained may also provide insight to human health and development.Objective 1. Assess population level variation of LCORL expression in muscle tissue and its association with phenotypic characteristics and predicted molecular signatures.Experimentally, we propose to 1) measure the population variation of LCORL expression in muscle tissue within a large population of cattle, 2) confirm the relationship between LCORL QTN genotype and LCORL expression, 3) evaluate the relationship between growth and carcass phenotypes and the level of LCORL expression, 4) further define the influence of variation in LCORL expression on the muscle transcriptome, and 5) examine the influence of allelic variation at the LCORL locus on the regulation of individual genes and gene networks.Objective 2. Define changes in the epigenome, specifically H3K4 and H3K27 modification, generated by LCORL variation and their relationship to transcriptional changes.Experimentally, we propose to 1) measure changes in H3K4 and H3K27 epigenetic marks using ChIP-seq analysis, 2) determine the relationship between changes in histone modifications and LCORL genotype and level of expression, and 3) link epigenetic modifications with the corresponding changes in the muscle transcriptome. By defining these elements we can better understand the causal relationship between changes in LCORL expression, chromatin structure, and downstream regulation of gene networks.Objective 3. Demonstrate that induction of LCORL expression is causal for the generation of molecular and physical phenotypes we have associated with the genetic and environmental variation in LCORL expression.Experimentally, we propose to 1) develop and characterize a transgenic mouse model capable of inducible expression of LCORL both globally and in a tissue-specific manner, and 2) measure both the molecular and physical phenotypes associated with induction of LCORL expression.
Project Methods
Objective 1Progeny growth and feedlot performance data will be collected on 300 Shorthorn or Simmental-Angus sired animals. Bodyweight will be taken at birth and at weaning. Individual estimates of feed intake will be obtained using the GrowSafe System Ltdfeed monitoring system. Weights being taken on 28d intervals. Ultrasound will be used to determine 12th rib backfat and marblingat successive time points on 28d intervals. Yield and quality grade will be collected on all cattle at harvest, approximately 430 d of age. A total of 200 animals, with equal distribution between sexes, born within a three-week calving window will be selected for whole blood collection and muscle biopsy at ~300d of age. In addition to the calving period, health status will also be assessed prior to biopsy and only animals with positive health status will be considered for biopsy. Whole blood will be collected by jugular venipuncture and used for the isolation of genomic DNA. A biopsy sample of the longissimus dorsi muscle will be taken from each animal for gene expression analyses. Total RNA will be extracted from muscle samples. Quantitative RT-PCR of LCORL will be performed. The calculation of relative expression between individuals will be performed using the relative standard curve method. The relationship between LCORL expression and phenotypic traits will be analyzed. Genotyping, CNV-calling, and RNA-seq analyses will be performed on 48 animals from each tail of the distribution for LCORL expression (n=96 total). Selected animals will be genotyped using the Illumina Bovine HD Beadchip™ containing approximately 777,000 markers. RNA-seq libraries will be constructed. All libraries will be indexed, quantified by qPCR, and pooled. The pool will be sequencedfor a target of >40 million raw reads per sample. Initial quality control, read mapping, normalization, and removal of unknown batch effects will be performed. Samples will be fitted to a negative-binomial general linear model and tested for differential gene expression between the high and low LCORL expression groups. Further analyses to examine the relationship between the expression of individual genes and their networks will also be performed. A phenotype by marker/CNV GWAS will be conducted. Normalized read counts for each transcript meeting a minimal count threshold will be used as molecular phenotypes to conduct an eQTL analysis. All animals will be used in the eQTL analysis as this analysis aims to map genetic variation to changes in gene expression.Objective 2Chromatin immunoprecipitation will be performed using longissimus dorsi muscle tissue collected in Objective 1. A total of 48 animals will be used, 24 animals from both high and low LCORL expression groups. Selection will be based on both LCORL genotype and the relationship between gene expression patterns within each group. Samples with the highest pairwise gene expression correlations will be selected based on cluster analysis. Antibodies directed against H3K4me3 and H3K27me3 will be obtained. Guidelines recommended by ENCODE and FAANG will be followed. ChIP samples and controls will be sequencedto a target depth of >50 million reads for H3K27me3, >25 million for H3K4me3, and >20 million for input DNA controls. Following pruning for quality, reads will be aligned to the appropriate reference genome. Identification of regions containing high read densities, or peak calling, will be performed. Reads from non-immunoprecipitation control libraries are used to assess enrichment of sequences associated with the specific target during analysis. RNA-seq and ChIP-seq data will be analyzed to investigate the relationship between changes in epigenetic marks and gene expression by comparing gene lists generated from each analysis.Objective 3Transgenic mice will be produced with a knock-in of LCORL into the endogenous safe-harbor locus, ROSA26. The general design involves generating a construct that contains the murine LCORL cDNA; isoform 1 of murine LCORL (NM_001163073) will be used. For tissue-specific activation of LCORL designs include reporter/stop cassettes that are flanked by loxP sites. Mating of transgenic mice carrying this LCORL construct with Cre-recombinase expressing transgenic mouse strains removes this upstream cassette and allows expression of the inserted gene via the ROSA26 promoter and/or the exogenous promoter used to drive reporter expression. Therefore, mating mice with muscle-specific Cre-recombinase mice would allow muscle-specific expression. Heterozygous mice for each transgene can be mated to produce pups that have no transgene, either of the transgenes or both transgenes within a single litter. As only mice with both transgenes will respond to doxycycline administration with LCORL overexpression, all other litter mates can be used as controls.Mice will be housed in breeding pairs or groups, and pups will be weaned at 3 weeks of age into individual or group cages. Pups will be genotyped by collecting ear notches or tail clips at weaning. Once validation is complete, heterozygous mice for each transgene will be mated to produce pups; 25% of these pups will carry both transgenes and respond to doxycycline administration with LCORL overexpression. Bodyweight is expected to increase due to LCORL overexpression. To detect a 10% increase in body weight (α=0.05, β=0.80) at 8 weeks of age, 13 mice are needed. Two periods of LCORL induction are planned. Ten litters of mice will be exposed to doxycycline in utero. Pregnant females will be given doxycycline for the final 14d of pregnancy. After giving birth, all dams will be given water without doxycycline, and progeny will be weighed at 5 days of age and weaned at 3 weeks of age into individual cages. Ten litters will be used resulting in 20 mice expected to carry both transgenes. Mice from litters unexposed to doxycycline in utero will be weaned into individual cages and genotyped. A total of 30 mice (15 with both transgenes and 15 without) will be administered doxycycline from 3 to 8 weeks of age. After weaning, all mice will be housed individually and sacrificed at 8 weeks of age. Bodyweight and feed intake of mice will be measured weekly from 3-8 weeks of age. Additionally, body composition will be assessed at 4, 6, and 8 weeks of age using EchoMRI. After sacrifice, weights of liver, heart, muscles (tibialis anterior, biceps femoris, gastrocnemius/soleus, longissimus dorsi, triceps brachii ), and fat pads (inguinal, retroperitoneal, gonadal) will be recorded.Data will be analyzed as two separate experiments based on induction timing. The mouse will serve as the experimental unit and litter serve as a block. This study is designed as a 2x2 factorial of LCORL induction and sex; the interaction of sex and LCORL induction will be considered but sample sizes between sexes may be unequal. The expression of LCORL will be measured in muscle, adipose tissue, heart, and liver of all mice. RNA-seq and ChIP-seq protocols will be conducted as described in Objectives 1 & 2. Provided the expected results are obtained for LCORL overexpression, we will select four mice having both transgenes and four mice having neither transgene from the postnatal induction period for RNA-seq analysis (8 mice total). To determine the effects of in utero induction of LCORL overexpression, 3 additional pregnant mice will be administered doxycycline, and progeny will be sacrificed at birth. Hindlimb and forelimb muscles from individual mice will be combined for RNA isolation and immunoprecipitation in order to generate sufficient RNA and DNA for sequencing. Four mice having both transgenes and four mice having neither transgene will be selected for RNA-seq analysis (8 mice total).

Progress 06/15/23 to 06/14/24

Outputs
Target Audience:Research results have been shared with the scientific body as results have been published on the findings discussed in the last report. Laboratory, computational, and science communication experience for the graduate student assigned to this project. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Laboratory, computational analysis, and science communication experience for the graduate student assigned to this project. The student presented on the findings from the eQTL and haplotype analysis at Plant and Animal Genome (PAG) Conference 31 and completed his master's thesis with the results from this project. How have the results been disseminated to communities of interest?The findings from this project were presented at PAG 31 and the haplotype analysis has been published in Genes. What do you plan to do during the next reporting period to accomplish the goals?Begin collecting growth data and tissue samples from the gene-edited mice. Further explore haplotype diversity in this region using publicly available bovine sequence data.

Impacts
What was accomplished under these goals? An eQTL analysis was conducted with the RNA-seq data generated prior to this project. This, alongside the previous RNA-seq analysis, has identified a network of genes including LCORL itself that are differentially expressed between QQ and qq animals that have the potential to be controlling their differences in size and lean growth. Long read sequencing has indicated that a 388-bp repetitive insertion of As and Ts exists in the intron of NCAPG. This insertion has exclusively been found in Q haplotypes so far, though it is unclear if this variant has any functional impact. No other major structural differences between QQ and qq animals have been found in the long-read data. WGS data from Herefords, Simmentals, along side the Charolais x Sim, Sim x Angus, and Shorthorn x Sim sequences collected for our previous research has been collected to further explore haplotype diversity. Few recombinations closer than what was reported in our recent publication have been found in this dataset of 300+ animals, though this has led to the discovery of similar haplotypes that have some, but not all of the exclusive 'Q' variants. However, it is unclear at this time whether these animals should be considered to be phenotypically 'Q' (increased growth), 'q' (ancestral wild-type), or something else. We have ordered the mouse model for this project. It will be arriving in early December.

Publications

  • Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Majeres, L.E.; Dilger, A.C.; Shike, D.W.; McCann, J.C.; Beever, J.E. Defining a Haplotype Encompassing the LCORL-NCAPG Locus Associated with Increased Lean Growth in Beef Cattle. Genes 2024, 15, 576. https://doi.org/10.3390/genes15050576


Progress 06/15/22 to 06/14/23

Outputs
Target Audience:Laboratory and computational analysis experience for the graduate student assigned to this project. Changes/Problems:Due to issues with RNAseq data that was generated in the previous reporting period (ran out of tissue for many animals with QQ haplotype to extract further RNA from; most remaining tissue samples did not carry the genetic variation responsible for increased body size, and thus we did not have enough QQ samples for RNAseq analysis), a different approach focusing on defining the LCORL-NCAPG haplotype and identifying samples with the appropriate genotype was used. Observation of apparent insertion structural variants in the haplotype led us to conclude that long read sequencing would be necessary to understand the genetic changes occurring at this locus that could be causative for the phenotype. What opportunities for training and professional development has the project provided?Laboratory and computational analysis experience for the graduate student assigned to this project. This includes development and use of PCR-RFLP and 5'-3' exonuclease assays for genotyping samples, processing and analysis of whole genome sequence data using GATK and other software, and statistical analysis using R. 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?Next steps for this project include: eQTL analysis with RNA-seq data generated prior to this project Long read sequencing and analysis to assemble the haplotype around the LCORL-NCAPG locus and investigate for structural variants. Sequencing additional cattle of different breed composition to further refine the Q haplotype. Begin development of a mouse colony

Impacts
What was accomplished under these goals? We identified potential causative variants responsible for the change in body size associated with this locus by using a subtractive approach to find variants exclusive to the Q haplotype. This has deepened our understanding of this haplotype and thus understanding how this region exerts its control over growth and development. While this does not directly address the above listed objectives, it will make carrying them out significantly easier in bovine populations, as it will improve our ability to identify candidate animals that would be appropriate for RNA-seq and ATAC-seq, as we can accurately identify individuals with the haplotype responsible for this region. Further, by deepening our understanding of the potential causative mechanisms in this region, that will inform our decisions for mouse model design.

Publications


    Progress 06/15/21 to 06/14/22

    Outputs
    Target Audience:Preliminary results were shared with Tennessee beef cattle producers and stakeholders at the UT Beef and Forage Center. Additionally, research opportunities for a graduate student, several undergraduate students, and a high school student to gain experience with genetics lab and computational techniques, including DNA and RNA extraction, library preparation, and data analysis. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This project provided educational opportunities for a graduate student, undergraduates, as well as a high school student in the form of hands-on experience working in a genetics lab. In addition to practical lab skills, the graduate student has had opportunities to present his research in the form of a seminar within the department and a poster presentation at the UT Beef and Forage Center Research Report. How have the results been disseminated to communities of interest?Preliminary data was shared with producers during the UT Beef and Forage Center Research Report via a poster presentation. What do you plan to do during the next reporting period to accomplish the goals?Next steps for this project include: Whole genome sequencing the animals used for the RNA-Seq analysis and calling genotypes, which will be used in conjunction with the RNA-Seq data. Finishing analysis of the RNA-Seq data, using R to identify expression patterns associated with LCORL expression and genotype in our dataset. Begin publication of data, in the form of the student's master's thesis, as well as papers in the scientific literature relating to this project, and uploading the RNA-Seq data to GEO. Initiate objectives 2 and 3 including beginning development of a mouse colony and acquiring tissue samples to utilize for ATAC-Seq.

    Impacts
    What was accomplished under these goals? Objective 1: RNA was isolated from muscle tissue samples obtained the year prior, as well as from other tissue samples from 2 previous studies which would be usable for this project. qPCR was performed to determine relative LCORL expression to select individuals to use for RNA-Seq. About 30 animals were selected from each of the three populations, with half being high and low expressors of LCORL identified by the qPCR experiments. The RNA from these animals was used for library preparation and sequenced at an average of 35 million reads each. The sequence data has gone through quality control steps and is currently in the process of being analyzed by the graduate student working on this project. Additionally, DNA has been extracted from blood taken from the animals used for this project and will be used for whole genome sequencing. This genotype data will complement the RNA-seq data collected. Objectives 2 and 3 have not been initiated yet.

    Publications

    • Type: Conference Papers and Presentations Status: Published Year Published: 2021 Citation: L Majeres, S Moisa, A Dilger, J McCann, D Shike, J Beever. The Level of LCORL Expression in Muscle is Associated with Lean Growth Rate in Beef Cattle. University of Tennessee Institute of Agriculture Beef and Forage Center Annual Research Report. 2: 15 (2021). https://doi.org/10.6084/m9.figshare.17208854.v1


    Progress 06/15/20 to 06/14/21

    Outputs
    Target Audience:Members of the scientific community were reached through formal and informal presentations that included the background information forthe project and its implications for the beef and other livestock industries. Preliminary data that supported the project hypotheses and objectives were also presented along with current progress toward project goals. Changes/Problems:The transition between the University of Illinois and the University of Tennessee took longer than expected and there was a delay in hiring the required staff to execute the project. What opportunities for training and professional development has the project provided? Nothing Reported 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?A graduate research assistant was hired on August 15, 2021, to execute the objectives.

    Impacts
    What was accomplished under these goals? The 174 tissue samples were collected to evaluate Objective 1 of the proposed aims. However, the graduate research assistant was not hired until August 15, 2021.

    Publications