NC1184: Molecular Mechanisms Regulating Skeletal Muscle Growth and Differentiation

(Multistate Research Project)

Status: Active

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SAES-422 Reports

Annual/Termination Reports:

[12/04/2020] [11/29/2021] [11/18/2022] [11/26/2023]

Date of Annual Report: 12/04/2020

Report Information

Annual Meeting Dates: 10/22/2020 - 10/23/2020
Period the Report Covers: 10/01/2019 - 09/30/2020

Participants

Brief Summary of Minutes

Minutes Attachment:

NC1184 2020 Multistate Research Activity Accomplishments Report-Final.docx

Accomplishments

Publications

Impact Statements

Date of Annual Report: 11/29/2021

Report Information

Annual Meeting Dates: 10/28/2021 - 10/29/2021
Period the Report Covers: 10/01/2020 - 09/30/2021

Participants

Anthony, Tracy (tracy.anthony@rutgers.edu) – Rutgers University
Awada, Tala (tawada2@unl.edu) – University of Nebraska
Burnett, Derris (ddb362@msstate.edu) – Mississippi State University
Dilger, Anna (adilger2@illinois.edu) – University of Illinois
El-Kadi, Samer (elkadi@vt.edu) – Virginia Tech University
Fu, Xing (xfu1@agcenter.lsu.edu) – Louisiana State University
Geisbrecht, Erika (geisbrechte@ksu.edu) – Kansas State University
Gerrard, David (dgerrard@vt.edu) – Virginia Tech
Gonzalez, John (jgonz@uga.edu) – University of Georgia
Guo, Wei (wguo@wisc.edu) – University of Wisconsin
Harsh, Bailey (bharsh2@illinois.edu) – University of Illinois
Huang, Yan (yxh010@uark.edu) – University of Arkansas
Kuang, Shihuan (skuang@purdue.edu) – Purdue University
Matarneh, Sulaiman (sulaiman.matarneh@usu.edu) – Utah State University
Reed, Sarah (sarah.reed@uconn.edu) – University of Connecticut (host)
Rhoads, Rob (rhoadsr@vt.edu) – Virginia Tech University
Selsby, Joshua (jselsby@iastate.edu) – Iowa State University
Strasburg, Gale (stragale@msu.edu) – Michigan State University
Thornton, Kara (kara.thornton@usu.edu) – Utah State University
Velleman, Sandy (velleman.1@osu.edu) – Ohio State University
White, Sarah (shwhite@tamu.edu) – Texas A&M University
Yates, Dustin (dustin.yates@unl.edu) – University of Nebraska
Zhou, Huaijun (hzhou@ucdavis.edu) – University of California Davis
Mozdziak Paul (pemozdzi@ncsu.edu)- North Carolina State University
Smith Zachary (zachary.smith@sdstate.edu) -South Dakota State University
Starkey Jessica (jds0073@auburn.edu) -Auburn University
Starkey Charles (cstarkey@auburn.edu) - Auburn University
Kim Yong-soo (ykim@hawaii.edu) -University of Hawaii
Du Min (min.du@wsu.edu) -Washington State University
Baun Jamie (baum@uark.edu) - University of Arkansas

Brief Summary of Minutes

Brief Summary of Minutes of Annual Meeting:

The annual NC1184 technical committee meeting was held in mixed mode both in-person and virtually on October 28 and 29, 2021. The meeting was hosted by Dr. John Gonzalez of the Department of Animal Science, University of Georgia. On October 28^th, the group was welcomed by Dr. Gonzalez, who shared information about the area, college, and department. The group then began with oral station reports.

On October 28^th at 2 PM, the group had a conference call with Drs. Mark Mirando and Steven Smith, USDA/NIFA, who outlined current funding opportunities, the USDA NIFA budget, statistics on the number of proposals submitted annually and funding rates, and an update on NIFA’s move from Washington, D.C. to Kansas City. A question and answer session followed Drs. Mirando and Smith’s update. Dr. Sally Johnson updated the special issues of JAS. After the call with Drs. Mirando, Smith and Johnson, the groups continued with station reports.

The group voted to hold the 2023 meeting at the Washington State University, to be hosted by Dr. Min Du.

The 2022 meeting will be held at the University of Wisconsin-Madison, to be hosted by Dr. Wei Guo.

Minutes Attachment:

NC1184 2021 Multistate Research Activity Accomplishments Report-Final.docx

Accomplishments

Objective 1: Characterize the signal transduction pathway that regulates skeletal muscle growth and metabolism including the influence of endogenous growth factors and various production practices.   Alabama Station: <ol> <li>Effect of maternal and post-hatch dietary inclusion of 25-hydroxycholecalciferal (25OHD3) on broiler chicken muscle growth characteristics and in vivo satellite cell activity</li> </ol> <ol start="2"> <li>Determining the effects of dietary inclusion of the vitamin D metabolite, 25-hydroxycholecalciferol in commercial broiler production systems will positively impact the way the poultry industry feeds broiler breeder hens and their offspring to improve feed efficiency and meat yield.</li> </ol>   Connecticut Station: <ol> <li>PCR arrays testing the effects of maternal diet on inflammatory factors have been completed, demonstrating sex by treatment and treatment effects on gene expression, including GATA3 and Toll-like receptor 1.</li> <li>LPS challenge completed in 6-month-old offspring of over-, restricted-, and control fed ewes. Cytokine assays in progress as of fall 2021.</li> <li>LD samples from 10-month-old offspring of over-, restricted- and control-fed rams sent to JMG at UGA for shear force testing.</li> <li>Heart samples sent to W. Guo at UW Madison for analysis of autophagy associated pathways.</li> </ol>   Wisconsin Station: <ol> <li>In collaboration with Dr. Reed (Connecticut Station), we found that overfeeding during gestation impacts autophagy signaling at late gestation and neonatal after birth in heart muscle. Cortisol level had no change at early and late gestation stages as well as neonatal. Overfeeding during gestation had significant interactions of maternal diet by developmental stages in male and female sheep. This work led to a manuscript that is under revision.</li> </ol>   Illinois Station: <ol> <li>To determine the effect of maternal inflammation on offspring muscle and immune system development, pregnant sows were inoculated with lipopolysaccharide during mid-gestation. Work is ongoing to determine offspring muscle development, immune system programming, and lifetime productivity.</li> <li>To determine the effects of myostatin on pig muscle growth, gene-editing was used to mutate myostatin in commercial pigs. To date, 77 pigs lacking functional myostatin have been produced but only 2 have survived beyond weaning. These animals do not display an increase in growth. Instead, they appear to be stunted in growth. Work is ongoing to determine the mechanism by which the loss of myostatin has different effects in pigs than in other species.</li> </ol>   Iowa Station: <ol> <li>In collaboration with Dr. Rhoads (Virginia Tech) and Dr. White (TAMU), we are working to better understand metabolic dysregulation and muscle injury caused by heat stress. We are currently exploring the role of a mitochondrially target antioxidant as a countermeasure to heat stress-mediated dysfunction.</li> <li>In conjunction with Dr. Rhoads (Virginia Tech) and Dr. White (TAMU), we have made further inroads into the role of biological sex on the muscular response to heat stress. We have completed an in vivo heat stress experiment and are working through analysis of phenotypical outcomes and will soon begin our biochemical and histological measures.  We have also expanded our complement of tissues to include heart, which may provide novel insight as it is metabolically more oxidative than is oxidative skeletal muscle.  Further, this may provide an opportunity to contribute to human health.  Finally, we have recently generated some interesting data regarding whole-body metabolism/injury during the recovery from heat stress that suggests persistent changes as well as differences impacted by biological sex.</li> <li>We initiated a new collaboration with an expert in proteomics technologies to more holistically capture changes to the proteome caused by muscle injury.</li> </ol>    Kansas Station: <ol> <li>Overall energy production (mitochondrial respiratory chain and ATP synthase complexes) are up regulated during developmental muscle atrophy</li> </ol>   South Dakota Station: <ol> <li>Evaluated the influence of feeding ractopamine HCl (400 mg/daily) to finsihing Holstein steers (Hergenreder et al., 2021b).</li> </ol> <ol> <li>Evaluated the influence of recombinant bovine somatotropin on growth performance, skeletal muscle biological activity, and beta-adrenergic receptor expression in finishing heifers (Hergenreder et al., 2021a).</li> <li>Evaluated the use of coated steroidal combination implants on feedlot performance and carcass traits of beef heifers fed for constant or varying days on feed (Ohnoutka et al., 2021).</li> <li>Evaluated the effects of laidlomycin propionate and bacitracin zinc on digestibility coefficients and ruminal fermentation parameters using a continuous culture model (Thompson et al., 2021).</li> <li>A review over the effects of dust on feedlot cattle was also conducted (Urso et al., 2021).</li> <li>Evaluated the influence of vitamin A status in finishing steers on myogenic gene expression and skeletal muscle fiber characteristics (Wellmann et al., 2021).</li> <li>Investigated the influence that cane molasses supplementation has on gene expression and protein abundance of ruminal epithelial tissue in transition dairy-cow diets (Miller et al., 2021).</li> <li>Finally, a study to determine the effects that encapsulated methionine fed during the growing period has on skeletal muscle growth and finishing phase performance and carcass characteristics (Baggerman et al., 2021).    </li> </ol>   Utah Station: <ol> <li>Demonstrated that implanting cattle with anabolic hormones impacts liver mineral concentrations.</li> <li>Improved understanding of how cattle of different breed types respond to different anabolic implant procedures.</li> <li>Learned about the pathways through which anabolic hormones (estradiol and trenbolone acetate) improve skeletal muscle growth in both the longissimus lumborum of beef steers and primary bovine satellite cells.</li> </ol>   Virginia Station: <ol> <li>O-GlcNAcylation is a post-translational modification considered to be a nutrient sensor that reports nutrient scarcity or surplus. Although O-GlcNAcylation exists in a wide range of cells and/or tissues, its functional role in muscle satellite cells (SCs) remains largely unknown. Using a genetic approach, we ablated O-GlcNAc transferase (OGT), and thus O-GlcNAcylation, in SCs. We first evaluated SC function in vivo using a muscle injury model and found that OGT deficient SCs had compromised capacity to repair muscle after an acute injury compared to the wild-type SCs. We generated muscle specific OGT and interleukin-15 receptor alpha subunit (IL-15ra) double knockout mice (mDKO).  Deletion of IL-15ra in skeletal muscle impaired IL-15 secretion. When fed a high-fat diet, mDKO mice were no longer protected against HFD-induced obesity compared to wild-type mice.</li> <li>OGT leads to a lean phenotype through enhanced interleukin-15 (IL-15) expression though only an association.</li> <li>Postnatal muscle growth is accompanied by increases in fast fiber type compositions raising the possibility that a slow to fast transition may be partially requisite for increases in muscle mass. We ablated the mouse Myh4 gene (myosin heavy chain IIB) and examined its consequence on postnatal muscle growth using chemical and genetic modifiers of muscle fiber type composition.</li> <li>Pork quality is a product of the rate and extent of muscle pH decline paced by carbohydrate metabolism postmortem. Beta-adrenergic agonist ractopamine alters muscle metabolism but has little impact on pork quality.  We fed pigs over a four week period and determined glycolytic metabolites during the postmortem period.</li> <li>Chronic heat stress causes several metabolic adaptations, which limit animal growth and performance. Our lab has demonstrated that HS has negative impacts on substrate metabolism by reducing fat oxidation and metabolic flexibility, which reduces overall ATP production. Data collected from chronic HS studies (3-weeks) demonstrates that pigs with greater metabolic flexibility at the conclusion of HS experienced lower core temperatures throughout the event.</li> </ol>   Indiana Station: <ol> <li>Activities: Used cell and molecular biology techniques, animal models and production animals to study molecular regulation of muscle growth and metabolism.</li> <li>Short-term outcomes: Trained 3 postdoctoral fellows (two landed faculty jobs), currently training 11 graduate students and 6 undergraduate students in various research projects; developed new research techniques and methods; used state-of-art single cell RNA sequencing to illustrate cell dynamics and reveal novel subpopulations in murine and porcine skeletal muscles.</li> <li>Outputs: Presented 4 seminars to the general publics and research communities; Published 11 peer-reviewed papers; Carried out 4 funded projects.</li> </ol>   Texas Station: <ol> <li>Found conjugated linoleic acid supplementation increased skeletal muscle mitochondrial function in young horses while decreasing antioxidant enzyme activity with no change in oxidative stress. Therefore, CLA may be decreasing oxidative load in skeletal muscle, minimizing the need for traditional antioxidant enzyme pathways (superoxide dismutase/glutathione peroxidase).</li> <li>Found that complexed trace mineral supplementation to young, exercising horses increased skeletal muscle antioxidant activity, both at rest and following a trailering stressor.</li> <li>Found that supplementation of a postbiotic modulated cellular stress and inflammation favorably following a submaximal exercise stressor in young horses.</li> <li>Found impaired mitochondrial function but greater mitochondrial capacities, greater type IIx fibers, lesser type IIa/x hybrid fibers, and greater satellite cells/muscle fiber in aged compared to young horses. Submaximal exercise training improved skeletal muscle mitochondrial capacities in both age groups of horses.</li> <li>Found increased mitochondrial function in Brahman calves that had been stressed in utero. May have implications for future growth potential and efficiency of production.</li> <li>Continue identification of impacts of temperament and breed on skeletal muscle mitochondrial energetics and relationships to meat product quality in beef cattle.</li> </ol>   Arkansas Station: <ol> <li>DHA is a potent adipogenic and lipogenic factor that can change the metabolic profile of muscle cells by increasing myocellular fat.</li> <li>Higher dietary crude protein (CP) levels promote growth performance for finishing lambs, whereas lower dietary CP levels are beneficial for meat quality, especially when evaluating color characteristics in the final product.</li> <li>Black pigs (BP) have superior intramuscular fat content to cross-bred commercial pigs (CP), while the growth performance of CP was better, and the transcriptomic differences between these two groups of pigs may cause the meat quality and growth performance variance</li> <li>Heat stress and feed restriction distinctly affect performance, carcass and meat yield, intestinal integrity, and inflammatory (chemo)cytokines in broiler chickens.</li> <li>Neuropeptide Y and its receptors are expressed in chicken skeletal muscle and regulate mitochondrial function.</li> <li>Phytogenic feed additives improve broiler feed efficiency via modulation of intermediary lipid and protein metabolism-regulated signaling pathways.</li> </ol>     Objective 2: Characterize the cellular and molecular basis of myogenesis   Alabama Station: <ol> <li>Ongoing work is being conducted regarding the in vitro differentiation capacity of muscle satellite cells from affected and unaffected broilers</li> </ol> <ol> <li>Effect of early and late-stage incubation temperature variation on broiler chicken muscle satellite cell activity and incidence and severity of Wooden Breast myopathy at processing</li> </ol>   Georgia Station: <ol> <li>In ovo feeding of high-yield broiler embryos with 2.5 mM of NR increased pectoralis major weight and length by 12 and 7%, respectively.</li> <li>Increased pectoralis major morphometrics was accompanied by a 21% decreased in muscle fiber cross-sectional area and 35% increase in muscle fiber density.</li> <li>Fiber morphometric results were associated with increased mRNA expression of SIRT-1, Cyclin D1, D2, and D3 at embryonic day 15, 18, and hatching.</li> </ol>   Kansas Station: <ol> <li>Human pathogenic alleles of TRIM32 expressed in Drosophila muscle tissue result in progressive muscle degeneration.</li> </ol> <ol> <li>The protein kinase NUAK (mammalian ARK5) coordinates with the insulin signaling pathway to control organismal size and sarcomere remodeling.</li> </ol>   Wisconsin Station: <ol> <li>RNA splicing factor RBM20 is differentially expressed in different muscle types and regulates myogenesis and muscle hypertrophy in a muscle type dependent manner.</li> </ol>   Utah Station: <ol> <li>Gained insight into how ultrasonication impacts mitochondrial function leading to development of tenderness in beef animals.</li> <li>Developed a model to study dark cutting beef in cattle</li> </ol>   Virginia Station: <ol> <li>IR, IRS-1, PDK1, mTORC2, pan-Akt, Akt1, and Akt2, play an important role in the activation of translation initiation in response to the insulin surge after an intermittent bolus meal.</li> <li>We also identified the amino acid sensors Sestrin1 and 2, and Rag A/C and Rheb as being sensitive to amino acid pulse after a meal.</li> <li>Our work also suggest that skeletal muscle protein synthesis is differentially regulated compared to other organs in the body.</li> </ol>   Hawaii Station: <ol> <li>Hawaii station continued to produce recombinant proteins suppressing the bioactivity of myostatin (MSTN), a negative regulator of muscle growth.</li> <li>MSTN propeptide (MSTNpro) is a strong negative regulator of MSTN, thus a study was developed to produce recombinant mouse MSTN fragment containing amino acid sequences 1-218 (mMSTNpro218) fused to mouse IgG Fc domain (mMSTNpro218-mFc).</li> <li>mMSTNpro218-mFc cDNA was synthesized and ligated into the pcDNA-3.1+ plasmid (mMSTNpro218-mFc-pcDNA-3.1) commercially. A large scale of mMSTNpro218-mFc-pcDNA-3.1 plasmid was produced from transformed coli cells.</li> <li>The Expi293™ Expression System (ThermoFisher Scientific, MA, USA) was used to express mMSTNpro218-mFc proteins following the protocol described by the manufacture.</li> <li>The expression of the mMSTNpro218-mFc protein was confirmed by SDS-PAGE and Western blot analyses.</li> <li>mMSTNpro218-mFc was purified by Protein A affinity chromatography but a large portion of mMSTNpro218-mFc in the cell culture did not bind to Protein A. SDS-PAGE in non-reduced condition showed that the protein aggregated in non-reduced condition, suggesting that the low affinity of the protein to the protein A column was probably due to the aggregation.</li> <li>When bioactivity of the mMSTNpro218-mFc was measured using the (CAGA)12-luciferase reporter gene assay, the MSTN-inhibitory capacity of the protein was extremely low. The aggregation of mMSTNpro218-mFc is likely associated with the low MSTN-inhibitory potency of recombinant mMSTNpro218-mFc. Thus, future studies need to find a way to minimize the aggregation of the expressed protein.</li> </ol>   Washington Station: <ol> <li>The Washington State Station is continuing to define the impacts of maternal nutrition on early skeletal muscle development, and found that obesity during the early development attenuates myogenic differentiation.</li> <li>The Washington State Station continues to define the molecular mechanisms regulating early formation of muscle cells and test the role of retinoic acid signaling in embryonic development.</li> </ol>   Arkansas Station: <ol> <li>Hypoxia further exacerbates woody breast myopathy in broilers via alteration of satellite cell fate.</li> </ol>   Ohio Station: Effect of Thermal Stress on Pectoralis Major Satellite Cells (with Michigan Station) <ol> <li>Poultry selected for growth have an inefficient thermoregulatory system and are more sensitive to temperature extremes</li> <li>Cold temperatures inhibited rates of proliferation and differentiation of p. major muscle satellite cells.</li> <li>If the hot temperature was applied during p. major muscle satellite cell proliferation, it resulted in greater stimulatory effects on differentiation than if the hot temperature was administered only during differentiation. Similarly, cold temperature administered during proliferation tended to have more suppressive effects on differentiation than if the cold temperature was applied only during differentiation.</li> <li>Growth selection has resulted in the p. major muscle satellite cells from the faster-growing commercial turkeys to be more sensitive to hot temperature during both proliferation and differentiation. The increased rates of proliferation and differentiation in vivo may result in a greater potential to accrete more satellite cells to drive myofiber hypertrophy, which could impact post-hatch breast muscle growth and structure.</li> <li>Adipogenic gene expression is more responsive to thermal challenge in proliferating satellite cells than in differentiating satellite cells, and that growth-selection has increased temperature sensitivity of satellite cells.</li> </ol>   Objective 3: Characterize mechanism of protein assembly and degradation in skeletal muscle   California Station <ol> <li>Tracked white striping, gross muscle pathology, and histological evidence of muscle</li> </ol> pathology. With these findings we have developed linear regression models that show a positive correlation between white striping, gross pathology, and histopathology relative to weight and age.   Kansas Station: <ol> <li>The E3 ubiquitin ligase TRIM32 is required to maintain protein levels of the costamere components βPS integrin and Sarcoglycan δ.</li> <li>Proteasome and peptidase proteins are selectively upregulated during developmental muscle atrophy. Thin filament-associated proteins are preferentially degraded before thick filament proteins.</li> </ol>   Virginia Station: <ol> <li>We set out to determine how the frequency of nutrient delivery controls protein deposition in neonatal muscles. Our studies indicated that despite receiving the same amount of diet per unit of body weight, the efficiency of protein deposition was greater in pigs fed intermittently compared to those fed continuously.  This increase is ascribed to a greater stimulation of protein synthetic pathways by intermittent feeding and occurred in response to a rise in insulin and amino acids.  However, the relative contributions of the insulin- and amino acid-signaling pathways that mediate the effects of these different feeding modalities on protein synthesis and degradation have not been fully elucidated.</li> </ol>   New Jersey Station: <ol> <li>The NJ Station is developing the necessary methodology to study the transcriptome and translatome in skeletal muscle. Development of RNA sequencing and ribosomal profile in mouse tissues as well as measurement of protein synthesis using deuterium oxide will provide new technical platforms to investigate skeletal muscle protein homeostasis in response to nutrients and activity.</li> </ol>   Texas Station: <ol> <li>Found that susceptibility to occurrence of dark cutting carcasses is genetically influenced by sire. This finding will aid selection efforts for reducing incidence.</li> <li>Identified specific microRNAs expressed at harvest that are associated with dark cutting incidence – a first step in understanding genetic triggers that participate in the stress-associated physiological mechanisms that result in dark cutting carcasses.</li> </ol>

Publications

See attached document for complete list   Moyorga EJ, Horst EA, Goetz B, Abeyta M, Al-Qaisi MA, Lei S, Rhoads R, Selsby JT, and Baumgard LH. Rapamycin administration during an acute heat stress challenge in growing pigs.  Journal of Animal Science.  In Press, 2021. Rudolph TE, Mayorga EJ, Rhoads RP, Baumgard L, and Selsby JT.  The effect of MitoQ on heat stressed skeletal muscle, and the potential confounding effect of biological sex. Journal of Thermal Biology.  In Press.  2021 Fausnacht DW, Kroscher KA, McMillan R, Davy DP, Baumgard LH, Selsby JT, Hulver MW, and Rhoads RP.  Heat Stress Reduces Metabolic Rate While Increasing Respiratory Exchange Ratio in Swine.  Animals.  In Press. 2021 Qiyue Ding, Yang Liu, Steven J. Halderson, Sebastian I. Arriola Apelo, Amanda K. Jones, Sambhu M. Pillai, Maria L. Hoffman, Sarah A. Reed, Kristen E. Govoni, Steven A. Zinn, Wei Guo. Maternal overnutrition during gestation in sheep alters autophagy associated pathways in offspring heart. Frontiers in Genetics. Under Review. 2021. Baggerman, J. O., A. J. Thompson, M. A. Jennings, J. E. Hergenreder, W. Rounds, Z. K. Smith, and B. J. Johnson. 2021. Effects of Encapsulated Methionine on Skeletal Muscle Growth and Development and Subsequent Feedlot Performance and Carcass Characteristics in Beef Steers. Animals 11(6):1627. Hergenreder, J. E., J. O. Baggerman, T. L. Harris, A. J. Thompson, K. S. Spivey, P. R. Broadway, G. J. Vogel, Z. K. Smith, and B. J. Johnson. 2021a. Bovine Somatotropin Alters Myosin Heavy Chains and Beta Receptors in Skeletal Muscle of Feedlot Heifers with Little Impact on Live or Carcass Performance. Meat and Muscle Biology 5(1):1-16. doi: <a href="https://doi.org/10.22175/mmb.11137">https://doi.org/10.22175/mmb.11137</a> Hergenreder, J. E., J. L. Beckett, Z. K. Smith, and B. J. Johnson. 2021b. A Greater dose of Ractopamine Hydrochloride Enhances Feedlot Performance and Impacts Carcass Characteristics of Calf-Fed Holstein Steers. Am J Anim Vet Sci 16(1)doi: 10.3844/ajavsp.2021.99.104 Miller, W. F., E. C. Titgemeyer, T. G. Nagaraja, D. H. M. Watanabe, L. D. Felizari, D. D. Millen, Z. K. Smith, and B. J. Johnson. 2021. Influence of Cane Molasses Inclusion to Dairy Cow Diets during the Transition Period on Rumen Epithelial Development. Animals 11(5):1230. Ohnoutka, C. A., R. G. Bondurant, B. M. Boyd, F. H. Hilscher, B. L. Nuttelman, G. I. Crawford, M. N. Streeter, M. K. Luebbe, J. C. MacDonald, Z. K. Smith, B. J. Johnson, and G. E. Erickson. 2021. Evaluation of coated steroidal combination implants on feedlot performance and carcass characteristics of beef heifers fed for constant or varying days on feed. Applied Animal Science 37(1):41-51. doi: 10.15232/aas.2020-02013 Thompson, A. J., Z. K. Smith, J. O. Sarturi, and B. J. Johnson. 2021. Antimicrobial supplementation alters digestibility and ruminal fermentation in a continuous culture model. J Appl Anim Res 49(1):23-29. doi: 10.1080/09712119.2021.1876704 Urso, P., A. Turgeon, F. Ribeiro, Z. Smith, and B. Johnson. 2021. Review: The Effects of Dust on Feedlot Health and Production of Beef Cattle. J Appl Anim Res doi: 10.1080/09712119.2021.1903476 Wellmann, K. B., J. Kim, P. M. Urso, Z. K. Smith, and B. J. Johnson. 2021. Evaluation of vitamin A status on myogenic gene expression and muscle fiber characteristics. J Anim Sci doi: 10.1093/jas/skab075 C.C. Reichhardt, L.L. Okamoto, L.A. Motsinger, B.P. Griffin, G.K. Murdoch, K.J. Thornton. 2021. The impacts of polyamine precursors, polyamines, and steroid hormones on temporal messenger rna abundance in bovine satellite cells induced to differentiate. Animals. 11(3), 764. Doi: 10.3390/ani11030764 Zumbaugh, M.D., A.E. Geiger, J. Luo, Z. Shen, H. Shi and D.E. Gerrard. 2021. O-GlucNAc transferase is required to maintain satellite cell function.  Stem Cells <a href="https://doi.org/10.1002/stem.3361">https://doi.org/10.1002/stem.3361</a> Matarneh, S.K., S.L. Silva and D.E. Gerrard. 2021. New Insights in Muscle Biology that Alter Meat Quality. Annual Review of Animal Biosciences 9:1, 355-377. Wang, C., S.K. Matarneh, D.E. Gerrard and J. Tan.  2021. Modeling of energy metabolism and analysis of pH variations in postmortem muscle. Meat Science, 182, 108634. <a href="https://doi.org/10.1016/j.meatsci.2021.108634">https://doi.org/10.1016/j.meatsci.2021.108634</a>. Zumbaugh, M.D., C-N Yen, J.S. Bodmer, H. Shi and D.E. Gerrard. 2021. Skeletal muscle O-GlcNAc transferase action on global metabolism is partially mediated through interleukin-15, Front Physiol. 12:682052. doi: 10.3389/fphys.2021.682052.  Cônsolo, N.R.B., J. Silva, V.M. Buarque, L.M. Samuelsson, P. Miller, P. Maclean, T.B. Moraes, L.C.G.S. Brabosa, A. Higuera-Padilla, L.A. Colnago, A.S. Netto, D.E. Gerrard and  S.L. Silva. 2021.  Using TD-NMR relaxometry and 1D 1H NMR spectroscopy to evaluate aging of Nellore beef.  Meat Science, 181, 108606. https://doi.org/10.1016/j.meatsci.2021.108606. Cônsolo, N.R.B, J. Silva, V.M. Buarque, L.C. Barbosa, A.H. Padilla, L.A. Colnago, A.S. Netto, D.E. Gerrard and S.L. Silva. 2021. <a href="https://www.tandfonline.com/doi/abs/10.1080/10495398.2021.1894164">Metabolomic signature of genetic potential for muscularity in beef cattle</a> Animal Biotechnology, 1–10. Advance online publication. https://doi.org/10.1080/10495398.2021.1894164. Consolo, NRB, V.L.M Buarque, J. Silva, M.D. Poleti, L.C.G.S. Barbosa, A. Higuera-Padilla, J.F.M. Gómez, L.A. Colnago, D.E. Gerrard, A. Saran Netto, S.L. Silva. 2021. <a href="https://www.sciencedirect.com/science/article/pii/S0377840120306623">Muscle and liver metabolomic signatures associated with residual feed intake in Nellore cattle</a>. Animal Feed Science and Technology, 271:114757 Fausnacht DW, KA Kroscher, RP McMillan, LS Martello, LH Baumgard, JT Selsby, MW Hulver and RP Rhoads. 2021. Heat Stress Reduces Metabolic Rate While Increasing Respiratory Exchange Ratio in Growing Pigs. Animals (Basel). 11(1):215. doi: 10.3390/ani11010215 Rudolph TE, EJ Mayorga, M Roths, RP Rhoads, LH Baumgard and JT Selsby. 2021. The effect of Mitoquinol (MitoQ) on heat stressed skeletal muscle from pigs, and a potential confounding effect of biological sex. J Therm Biol. 97:102900. doi: 10.1016/j.jtherbio.2021.102900 Mayorga EJ, Horst EA, Goetz BM, Rodríguez-Jiménez S, Abeyta MA, Al-Qaisi M, Lei S, Rhoads RP, Selsby JT and Baumgard LH. 2021. Rapamycin administration during an acute heat stress challenge in growing pigs. J Anim Sci. 99(5):skab145. doi: 10.1093/jas/skab145. PMID: 33950189; PMCID: PMC8160530 Guo, Q., J.C. Wicks, C.N. Yen, T.L. Scheffler, B.T. Richert, A.P. Schinckel, A.L. Grant, and D.E. Gerrard. 2021. Ractopamine changes in pork quality are not mediated by changes in muscle glycogen or lactate accumulation postmortem. Meat Science, 174, 108418. https://doi.org/10.1016/j.meatsci.2020.108418 Suryawan A, El-Kadi SW, Nguyen HV, Fiorotto ML, Davis TA. Intermittent bolus compared with continuous feeding enhances insulin and amino acid signaling to translation initiation in skeletal muscle of neonatal pigs. The Journal of Nutrition. 2021; 151:2636-2645. Matarneh, SK, Yen CN, Bodmer J, El-Kadi SW, Gerrard DE. Mitochondria influence glycolytic and tricarboxylic acid cycle metabolism under postmortem simulating conditions. Meat Science. 2021: 172. doi: 10.1016/j.meatsci.2020.108316. El-Kadi SW, Boutry-Regard C, Suryawan A, Nguyen HV, Kimball SR, Fiorotto ML, Davis TA. Intermittent bolus feeding enhances organ growth more than continuous feeding in a neonatal piglet model. Current Developments in Nutrition. 2020: Doi: 10.1093/cdn/nzaa170 Snyder MM, Yue F, Zhang L, Shang R, Qiu J, Chen J, Kim KH, Peng Y, Oprescu SN, Donkin SS, Bi P, Kuang S*. 2021. LETMD1 is required for mitochondrial structure and thermogenic function of brown adipocytes. FASEB J. 35:e21965. <a href="https://doi.org/10.1096/fj.202100597R">https://doi.org/10.1096/fj.202100597R</a>. (Donkin SS is at Oregon State University, Bi P is a University of Georgia). Huang X, Kuang S, Applegate TJ, Lin TL, Cheng HW. 2021. Prenatal Serotonin Fluctuation Affects Serotoninergic Development and Related Neural Circuits in Chicken Embryos. Neuroscience 473, 66-80. <a href="https://doi.org/10.1016/j.neuroscience.2021.08.011">https://doi.org/10.1016/j.neuroscience.2021.08.011</a> (Applegate TJ is at University of Georgia Athens, Cheng HW is at USDA animal behavioral center) Xu, J., Strasburg, G.M., Reed, K.M., and Velleman, S.G. 2021. Response of Turkey Pectoralis Major Muscle Satellite Cells to Hot and Cold Thermal Stress: Effect of Growth Selection on Satellite Cell Proliferation and Differentiation. Comparative Biochemistry and Physiology Pt. A. 252:110823. <a href="https://doi.org/10.1016/j.cbpa.2020.110823">https://doi.org/10.1016/j.cbpa.2020.110823</a> Aljarbou , W.A. England , E.M., Velleman, S.G., Reed, K.M., and Strasburg., G.M.  2021. Phosphorylation state of pyruvate dehydrogenase and metabolite levels in turkey skeletal muscle in normal and pale, soft, exudative meats. Br. Poult. Sci. 62:379-386. https://doi.org/10.1080/00071668.2020.1855629  Xu, J., Strasburg, G.M., Reed, K.M., and Velleman, S.G. 2021. Effect of temperature and growth selection on intracellular lipid accumulation and adipogenic gene expression in turkey pectoralis major muscle satellite cells. Front. Physiol. 12:667814. <a href="https://doi.org/10.3389/fphys.2021.667814">https://doi.org/10.3389/fphys.2021.667814</a>. Reed, K.M., Mendoza, K.M., Abrahante, J.E., Velleman, S.G., and Strasburg, G.M. 2021. Data Mining Identifies Differentially Expressed Circular RNAs in Skeletal Muscle of Thermally Challenged Turkey Poults. Front. Physiol. https://doi.org/10.3389/fphys.2021.732208.

Impact Statements

See attached document

Date of Annual Report: 11/18/2022

Report Information

Annual Meeting Dates: 09/29/2022 - 09/30/2022
Period the Report Covers: 10/01/2021 - 09/30/2022

Participants

Anthony, Tracy (tracy.anthony@rutgers.edu) – Rutgers University
Baum, Jamie (baum@uark.edu) – University of Arkansas
Bohrer, Benjamin (bohrer.13@osu.edu) – Ohio State University
Burnett, Derris (ddb362@msstate.edu) – Mississippi State University
Carlin, Kasey R (kasey.maddockcarlin@ndsu.edu) – North Dakota State University
Dilger, Anna (adilger2@illinois.edu) – University of Illinois
Du Min (min.du@wsu.edu) -Washington State University
El-Kadi, Samer (elkadi@vt.edu) – Virginia Tech University
Ernst, Catherine (ernstc@msu.edu) – Michigan State University
Fallini, Claudia (cfallini@uri.edu) – University of Rhode Island
Fu, Xing (xfu1@agcenter.lsu.edu) – Louisiana State University
Geisbrecht, Erika (geisbrechte@ksu.edu) – Kansas State University
Gerrard, David (dgerrard@vt.edu) – Virginia Tech
Gonzalez, John (jgonz@uga.edu) – University of Georgia
Guo, Wei (wguo@wisc.edu) – University of Wisconsin
Harsh, Bailey (bharsh2@illinois.edu) – University of Illinois
Huang, Yan (yxh010@uark.edu) – University of Arkansas
Johnson, Sally E (sealy@vt.edu) – Virginia Polytechnic Institute and State University
Kim, Jongkyoo (kimjon48@msu.edu) – Michigan State University
Kim Yong-soo (ykim@hawaii.edu) – University of Hawaii
King, Annie (ajking@ucdavis.edu) – University of California Davis
Kuang, Shihuan (skuang@purdue.edu) – Purdue University
Liao, Shengfa (sliao@ads.msstate.edu) – Mississippi State University
Markworth, James (jmarkwor@purdue.edu) – Purdue University
Matarneh, Sulaiman (sulaiman.matarneh@usu.edu) – Utah State University
Mienaltowski, Michael (mjmienaltowski@ucdavis.edu) – University of California Davis
Mozdziak Paul (pemozdzi@ncsu.edu) – North Carolina State University
Petersen, Jessica (jessica.petersen@unl.edu) – University of Nebraska
Reed, Sarah (sarah.reed@uconn.edu) – University of Connecticut (host)
Rhoads, Rob (rhoadsr@vt.edu) – Virginia Tech University
Reed, Sarah (sarah.reed@uconn.edu) – University of Connecticut
Selsby, Joshua (jselsby@iastate.edu) – Iowa State University
Starkey, Jessica (jessica.starkey@auburn.edu) – Auburn University
Strasburg, Gale (stragale@msu.edu) – Michigan State University
Thornton, Kara (kara.thornton@usu.edu) – Utah State University
Velleman, Sandy (velleman.1@osu.edu) – Ohio State University
White, Sarah (shwhite@tamu.edu) – Texas A&M University
YAO, YAO (YAO.YAO@UGA.EDU) – University of Georgia
Yates, Dustin (dustin.yates@unl.edu) – University of Nebraska
Zhou, Huaijun (hzhou@ucdavis.edu) – University of California Davis
Zumbaugh, Morgan (mdzumbaugh@ksu.edu) – Kansas State University

Participants Attachment:

NC1184 2022 Multistate Research Activity Accomplishments Report-Final.docx

Brief Summary of Minutes

The annual NC1184 technical committee meeting was held mainly in-person, but also had several members attended virtually on Sept 29 and 30, 2022. The meeting was hosted by Dr. Wei Guo of the Department of Animal Science, University of Wisconsin. On Sept 29, the group was welcomed by Dr. Kent Weigel, Chair of the Department of Animal & Dairy Sciences, who shared information about the area, college, and department. The group then began with oral station reports.

On Sept 30 morning, the group had a conference call with Dr. Mark Mirando, USDA/NIFA, who outlined current funding opportunities, the USDA NIFA budget, statistics on the number of proposals submitted annually and funding rates, and the new grant opportunity with NIH: Dual Purpose with Dual Benefit. After the call with Dr. Mirando, the groups continued with station reports.

The group voted to hold the 2024 meeting at the Louisiana State University, to be hosted by Dr. Xing Fu.

The 2023 meeting will be held at the Washington State University, to be hosted by Dr. Min Du.

Accomplishments

See attached file

Publications

see attached report

Impact Statements

see attached report

Date of Annual Report: 11/26/2023

Report Information

Annual Meeting Dates: 10/05/2023 - 10/07/2023
Period the Report Covers: 10/01/2022 - 09/20/2023

Participants

Anthony, Tracy (tracy.anthony@rutgers.edu) – Rutgers University
Baum, Jamie (baum@uark.edu) – University of Arkansas
Bohrer, Benjamin (bohrer.13@osu.edu) – Ohio State University
Burnett, Derris (ddb362@msstate.edu) – Mississippi State University
Collins, Galen (gac263@msstate.edu) – Mississippi State University
Dilger, Anna (adilger2@illinois.edu) – University of Illinois
Du Min (min.du@wsu.edu) -Washington State University
El-Kadi, Samer (elkadi@vt.edu) – Virginia Tech University
Ernst, Catherine (ernstc@msu.edu) – Michigan State University
Fallini, Claudia (cfallini@uri.edu) – University of Rhode Island
Fu, Xing (xfu1@agcenter.lsu.edu) – Louisiana State University
Geisbrecht, Erika (geisbrechte@ksu.edu) – Kansas State University
Gerrard, David (dgerrard@vt.edu) – Virginia Tech
Gonzalez, John (jgonz@uga.edu) – University of Georgia
Guo, Wei (wguo@wisc.edu) – University of Wisconsin
Harsh, Bailey (bharsh2@illinois.edu) – University of Illinois
Johnson, Sally E (sealy@vt.edu) – Virginia Polytechnic Institute and State University
Kim, Jongkyoo (kimjon48@msu.edu) – Michigan State University
Kim Yong-soo (ykim@hawaii.edu) – University of Hawaii
Kuang, Shihuan (skuang@purdue.edu) – Purdue University
Liao, Shengfa (sliao@ads.msstate.edu) – Mississippi State University
Markworth, James (jmarkwor@purdue.edu) – Purdue University
Matarneh, Sulaiman (sulaiman.matarneh@usu.edu) – Utah State University
Mienaltowski, Michael (mjmienaltowski@ucdavis.edu) – University of California Davis
Mozdziak Paul (pemozdzi@ncsu.edu) – North Carolina State University
Petersen, Jessica (jessica.petersen@unl.edu) – University of Nebraska
Reed, Sarah (sarah.reed@uconn.edu) – University of Connecticut
Reichhardt, Caleb (ccreichh@hawaii.edu) – University of Hawaii
Rhoads, Robert (rhoadsr@vt.edu) – Virginia Tech University
Riggs, Penny (riggs@tamu.edu) - Texas AgriLife Research
Ro, Seung-Hyun (shro@unl.edu) - University of Nebraska
Rosa, Guilherme (grosa@wisc.edu) - University of Wisconsin
Scheffler, Tracy (tscheffler@ufl.edu) - University of Florida
Schmidt, Ty (tschmidt4@unl.edu) - University of Nebraska
Selsby, Joshua (jselsby@iastate.edu) – Iowa State University
Starkey, Jessica (jessica.starkey@auburn.edu) – Auburn University
Starkey, Charles (cws0031@auburn.edu) - Auburn University
Strasburg, Gale (stragale@msu.edu) – Michigan State University
Thornton, Kara (kara.thornton@usu.edu) – Utah State University
Velleman, Sandra (velleman.1@osu.edu) – Ohio State University
White, Sarah (shwhite@tamu.edu) – Texas A&M University
YAO, YAO (YAO.YAO@UGA.EDU) – University of Georgia
Yates, Dustin (dustin.yates@unl.edu) – University of Nebraska
Zhou, Huaijun (hzhou@ucdavis.edu) – University of California Davis
Zumbaugh, Morgan (mdzumbaugh@ksu.edu) – Kansas State University

Participants Attachment:

NC1184 Annual Station Reports 2023_final[65].docx

Brief Summary of Minutes

Accomplishments

See attached file

Publications

Collaborative Publications <ol> <li>Xu J, Strasburg GM, Reed KM, Bello NM, Velleman SG. Differential effects of temperature and mTOR and Wnt-planar cell polarity pathways on syndecan-4 and CD44 expression in growth-selected turkey satellite cell populations. PLoS One. 2023;18(2):e0281350.</li> <li>Reed KM, Mendoza KM, Xu J, Strasburg GM, Velleman SG. Transcriptome Response of Differentiating Muscle Satellite Cells to Thermal Challenge in Commercial Turkey. Genes (Basel). 2022;13(10). Epub 20221014. doi: 10.3390/genes13101857. PubMed PMID: 36292741; PMCID: PMC9601516.</li> <li>Kim KH, Oprescu SN, Snyder MM, Kim A, Jia Z, Yue F, Kuang S. PRMT5 mediates FoxO1 methylation and subcellular localization to regulate lipophagy in myogenic progenitors. Cell Rep. 2023;42(11):113329. Epub 20231024. doi: 10.1016/j.celrep.2023.113329. PubMed PMID: 37883229.</li> <li>Qiu J, Yue F, Zhu P, Chen J, Xu F, Zhang L, Kim KH, Snyder MM, Luo N, Xu HW, Huang F, Tao WA, Kuang S. FAM210A is essential for cold-induced mitochondrial remodeling in brown adipocytes. Nat Commun. 2023;14(1):6344. Epub 20231010. doi: 10.1038/s41467-023-41988-y. PubMed PMID: 37816711; PMCID: PMC10564795.</li> <li>Oprescu SN, Baumann N, Chen X, Sun Q, Zhao Y, Yue F, Wang H, Kuang S. Sox11 is enriched in myogenic progenitors but dispensable for development and regeneration of the skeletal muscle. Skelet Muscle. 2023;13(1):15. Epub 20230913. doi: 10.1186/s13395-023-00324-0. PubMed PMID: 37705115; PMCID: PMC10498607.</li> <li>Kim KH, Jia Z, Snyder M, Chen J, Qiu J, Oprescu SN, Chen X, Syed SA, Yue F, Roseguini BT, Imbalzano AN, Hu C, Kuang S. PRMT5 links lipid metabolism to contractile function of skeletal muscles. EMBO Rep. 2023;24(8):e57306. Epub 20230619. doi: 10.15252/embr.202357306. PubMed PMID: 37334900; PMCID: PMC10398672.</li> <li>Wang L, Gao P, Li C, Liu Q, Yao Z, Li Y, Zhang X, Sun J, Simintiras C, Welborn M, McMillin K, Oprescu S, Kuang S, Fu X. A single-cell atlas of bovine skeletal muscle reveals mechanisms regulating intramuscular adipogenesis and fibrogenesis. J Cachexia Sarcopenia Muscle. 2023;14(5):2152-67. Epub 20230712. doi: 10.1002/jcsm.13292. PubMed PMID: 37439037; PMCID: PMC10570087.</li> <li>Unsihuay D, Hu H, Qiu J, Latorre-Palomino A, Yang M, Yue F, Yin R, Kuang S, Laskin J. Multimodal high-resolution nano-DESI MSI and immunofluorescence imaging reveal molecular signatures of skeletal muscle fiber types. Chem Sci. 2023;14(15):4070-82. Epub 20230323. doi: 10.1039/d2sc06020e. PubMed PMID: 37063787; PMCID: PMC10094364.</li> <li>Chen J, Yue F, Kuang S. Labeling and analyzing lipid droplets in mouse muscle stem cells. STAR Protoc. 2022;3(4):101849. Epub 20221119. doi: 10.1016/j.xpro.2022.101849. PubMed PMID: 36595920; PMCID: PMC9679676.</li> <li>Wang Y, Troughton LD, Xu F, Chatterjee A, Ding C, Zhao H, Cifuentes LP, Wagner RB, Wang T, Tan S, Chen J, Li L, Umulis D, Kuang S, Suter DM, Yuan C, Chan D, Huang F, Oakes PW, Deng Q. Atypical peripheral actin band formation via overactivation of RhoA and nonmuscle myosin II in mitofusin 2-deficient cells. Elife. 2023;12. Epub 20230919. doi: 10.7554/eLife.88828. PubMed PMID: 37724949; PMCID: PMC10550287.</li> <li>Roths M, Abeyta MA, Wilson B, Rudolph TE, Hudson MB, Rhoads RP, Baumgard LH, Selsby JT. Effects of heat stress on markers of skeletal muscle proteolysis in dairy cattle. J Dairy Sci. 2023;106(8):5825-34. Epub 20230620. doi: 10.3168/jds.2022-22678. PubMed PMID: 37349209.</li> </ol> Other publications: <ol> <li>Ma Z, Huang Z, Zhang C, Liu X, Zhang J, Shu H, Ma Y, Liu Z, Feng Y, Chen X, Kuang S, Zhang Y, Jia Z. Hepatic Acat2 overexpression promotes systemic cholesterol metabolism and adipose lipid metabolism in mice. Diabetologia. 2023;66(2):390-405. Epub 20221115. doi: 10.1007/s00125-022-05829-9. PubMed PMID: 36378328; PMCID: PMC9665029.</li> <li>Kargl CK, Sullivan BP, Middleton D, York A, Burton LC, Brault JJ, Kuang S, Gavin TP. Peroxisome proliferator-activated receptor γ coactivator 1-α overexpression improves angiogenic signalling potential of skeletal muscle-derived extracellular vesicles. Exp Physiol. 2023;108(2):240-52. Epub 20221201. doi: 10.1113/ep090874. PubMed PMID: 36454193; PMCID: PMC9949767.</li> <li>Chen X, Ferreira CR, Kuang S. Targeted Lipidomics Analysis of Adipose and Skeletal Muscle Tissues by Multiple Reaction Monitoring Profiling. Methods Mol Biol. 2023;2640:351-68. doi: 10.1007/978-1-0716-3036-5_25. PubMed PMID: 36995607.</li> <li>Tien PC, Chen X, Elzey BD, Pollock RE, Kuang S. Notch signaling regulates a metabolic switch through inhibiting PGC-1α and mitochondrial biogenesis in dedifferentiated liposarcoma. Oncogene. 2023;42(34):2521-35. Epub 20230711. doi: 10.1038/s41388-023-02768-6. PubMed PMID: 37433985; PMCID: PMC10575759.</li> <li>D'Souza RF, Figueiredo VC, Markworth JF, Zeng N, Hedges CP, Roberts LA, Raastad T, Coombes JS, Peake JM, Mitchell CJ, Cameron-Smith D. Cold water immersion in recovery following a single bout resistance exercise suppresses mechanisms of miRNA nuclear export and maturation. Physiol Rep. 2023;11(15):e15784. doi: 10.14814/phy2.15784. PubMed PMID: 37549955; PMCID: PMC10406566.</li> <li>Liu Q, Li C, Deng B, Gao P, Wang L, Li Y, Shiri M, Alkaifi F, Zhao J, Stephens JM, Simintiras CA, Francis J, Sun J, Fu X. Tcf21 marks visceral adipose mesenchymal progenitors and functions as a rate-limiting factor during visceral adipose tissue development. Cell Rep. 2023;42(3):112166. Epub 20230228. doi: 10.1016/j.celrep.2023.112166. PubMed PMID: 36857185; PMCID: PMC10208561.</li> <li>Ford H, Liu Q, Fu X, Strieder-Barboza C. White Adipose Tissue Heterogeneity in the Single-Cell Era: From Mice and Humans to Cattle. Biology (Basel). 2023;12(10). Epub 20230927. doi: 10.3390/biology12101289. PubMed PMID: 37886999; PMCID: PMC10604679.</li> <li>Liu Q, Li C, Li Y, Wang L, Zhang X, Deng B, Gao P, Shiri M, Alkaifi F, Zhao J, Stephens JM, Simintiras CA, Francis J, Sun J, Fu X. Progenitor cell isolation from mouse epididymal adipose tissue and sequencing library construction. STAR Protoc. 2023;4(4):102703. Epub 20231109. doi: 10.1016/j.xpro.2023.102703. PubMed PMID: 37948186.</li> </ol>

Impact Statements

See attached file