FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / J Anim Sci / Dietary tributyrin supplementation and submaximal exercise p...
Journal of animal science2019; 97(12); 4951-4956; doi: 10.1093/jas/skz330

Dietary tributyrin supplementation and submaximal exercise promote activation of equine satellite cells.

Abstract: Postexercise skeletal muscle repair is dependent on the actions of satellite cells (SCs). The signal(s) responsible for activation of these normally quiescent cells in the horse remain unknown. The objective of the experiment was to determine whether submaximal exercise or tributyrin (TB) supplementation is sufficient to stimulate SC activation. Adult geldings were fed a control diet (n = 6) or a diet containing 0.45% TB (n = 6). After 30 d, the geldings performed a single bout of submaximal exercise. Middle gluteal muscle biopsies and blood were collected on days -1, 1, 3, and 5 relative to exercise. Diet had no effect on any parameter of physical performance. Total RNA isolated from the gluteal muscle of TB fed geldings contained greater (P < 0.05) amounts of myogenin mRNA than controls. Satellite cell isolates from TB supplemented horses had a greater (P = 0.02) percentage of proliferating cell nuclear antigen immunopositive (PCNA+) SC than controls after 48 h in culture. Submaximal exercise was sufficient to increase (P < 0.05) the percentage of PCNA(+) cells in all isolates obtained during recovery period. No change in the amount of gluteal muscle Pax7 mRNA, a lineage marker of SCs, occurred in response to either diet or exercise. Our results indicate that both submaximal exercise and TB prime SCs for activation and cell cycle reentry but are insufficient to cause an increase in Pax7 expression during the recovery period.
© The Author(s) 2019. Published by Oxford University Press on behalf of the American Society of Animal Science. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
Get Full Text
Publication Date: 2019-10-21 PubMed ID: 31630180PubMed Central: PMC6915229DOI: 10.1093/jas/skz330Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article explores how a dietary additive, Tributyrin (TB), and submaximal exercise severity can influence the activation of satellite cells (SCs) – crucial entities in skeletal muscle repair – in horses.

Objective and Methodology

The research was aimed to investigate if submaximal exercise and TB supplementation can stimulate the activation of SCs, which are typically inactive in horses. In the matter of methodology, adult geldings (male horses) were divided into two groups. One group was fed a control diet whereas the other received a diet containing 0.45% TB. After a period of 30 days, the horses performed a single bout of submaximal exercise. Muscle biopsies and blood samples were collected from the horses on day -1, 1, 3, and 5 relative to exercise.

  • A total RNA was isolated from the gluteal muscle of horses supplemented with TB.
  • SC isolates from horses supplemented with TB were tested for percentage of proliferating cell nuclear antigen immunopositive (PCNA+),a marker of dividing cells.
  • Submaximal exercise’s effects on the percentage of PCNA(+) cells were evaluated.
  • They also checked for any changes in the quantity of Pax7 mRNA, an identifier of SCs, in response to diet or exercise.

Findings

The research discovered that feeding horses with a diet supplemented with TB or exposing them to submaximal exercise does not impact their physical performance parameters. However, there were significantly higher levels of myogenin mRNA in the total RNA isolated from the gluteal muscle of TB-fed horses compared to the control group.

  • The SC isolates obtained from TB-supplemented horses displayed a greater percentage of PCNA+ SCs after 48 hours in culture when compared to those from control diet-fed horses.
  • Submaximal exercise was sufficient to augment the percentage of PCNA(+) cells in all the isolates obtained during the recovery phase.
  • Neither the TB dietary supplement nor the submaximal exercise resulted in any change in the levels of Pax7 mRNA, which is a lineage marker of SCs.

Conclusion

In conclusion, both submaximal exercise and a diet supplemented with TB were found to facilitate the activation and cell cycle re-entry of SCs, though these interventions were not sufficient to cause an increase in Pax7 expression during the recovery period.

Cite This Article

APA
Gonzalez ML, Jacobs RD, Ely KM, Johnson SE. (2019). Dietary tributyrin supplementation and submaximal exercise promote activation of equine satellite cells. J Anim Sci, 97(12), 4951-4956. https://doi.org/10.1093/jas/skz330

Publication

Journal of animal science
ISSN: 1525-3163
NlmUniqueID: 8003002
Country: United States
Language: English
Volume: 97
Issue: 12
Pages: 4951-4956

Researcher Affiliations

Gonzalez, Madison L
  • Department of Animal and Poultry Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA.
Jacobs, Robert D
  • Purina Animal Nutrition, Gray Summit, MO.
Ely, Kristine M
  • Department of Animal and Poultry Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA.
Johnson, Sally E
  • Department of Animal and Poultry Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA.

MeSH Terms

  • Animal Feed
  • Animal Nutritional Physiological Phenomena
  • Animals
  • Diet / veterinary
  • Dietary Supplements
  • Horses / physiology
  • Male
  • Muscle, Skeletal / physiology
  • Myogenin
  • PAX7 Transcription Factor / genetics
  • PAX7 Transcription Factor / metabolism
  • Physical Conditioning, Animal / physiology
  • Proliferating Cell Nuclear Antigen / metabolism
  • RNA, Messenger / metabolism
  • Satellite Cells, Skeletal Muscle / physiology
  • Triglycerides / administration & dosage
  • Triglycerides / pharmacology

References

This article includes 43 references
  1. Allen RE, Sheehan SM, Taylor RG, Kendall TL, Rice GM. Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro.. J Cell Physiol 1995 Nov;165(2):307-12.
    pubmed: 7593208doi: 10.1002/jcp.1041650211google scholar: lookup
  2. Anderson JE. Hepatocyte Growth Factor and Satellite Cell Activation.. Adv Exp Med Biol 2016;900:1-25.
    doi: 10.1007/978-3-319-27511-6_1pubmed: 27003394google scholar: lookup
  3. Avila F, Mickelson JR, Schaefer RJ, McCue ME. Genome-Wide Signatures of Selection Reveal Genes Associated With Performance in American Quarter Horse Subpopulations.. Front Genet 2018;9:249.
    doi: 10.3389/fgene.2018.00249pmc: PMC6060370pubmed: 30105047google scholar: lookup
  4. Bedford A, Yu H, Squires EJ, Leeson S, Gong J. Effects of supplementation level and feeding schedule of butyrate glycerides on the growth performance and carcass composition of broiler chickens.. Poult Sci 2017 Sep 1;96(9):3221-3228.
    doi: 10.3382/ps/pex098pubmed: 28431158google scholar: lookup
  5. Biondo LA, Teixeira AAS, Silveira LS, Souza CO, Costa RGF, Diniz TA, Mosele FC, Rosa Neto JC. Tributyrin in Inflammation: Does White Adipose Tissue Affect Colorectal Cancer?. Nutrients 2019 Jan 8;11(1).
    pmc: PMC6357117pubmed: 30626010doi: 10.3390/nᄁ0110google scholar: lookup
  6. Brandt AM, Kania JM, Gonzalez ML, Johnson SE. Hepatocyte growth factor acts as a mitogen for equine satellite cells via protein kinase C δ-directed signaling.. J Anim Sci 2018 Sep 7;96(9):3645-3656.
    pmc: PMC6127786pubmed: 29917108doi: 10.1093/jas/sky234google scholar: lookup
  7. Chan JK, Sun L, Yang XJ, Zhu G, Wu Z. Functional characterization of an amino-terminal region of HDAC4 that possesses MEF2 binding and transcriptional repressive activity.. J Biol Chem 2003 Jun 27;278(26):23515-21.
    doi: 10.1074/jbc.M301922200pubmed: 12709441google scholar: lookup
  8. Conley BA, Egorin MJ, Tait N, Rosen DM, Sausville EA, Dover G, Fram RJ, Van Echo DA. Phase I study of the orally administered butyrate prodrug, tributyrin, in patients with solid tumors.. Clin Cancer Res 1998 Mar;4(3):629-34.
    pubmed: 9533530
  9. Dong L, Zhong X, He J, Zhang L, Bai K, Xu W, Wang T, Huang X. Supplementation of tributyrin improves the growth and intestinal digestive and barrier functions in intrauterine growth-restricted piglets.. Clin Nutr 2016 Apr;35(2):399-407.
    doi: 10.1016/j.clnu.2015.03.002pubmed: 26112894google scholar: lookup
  10. Dressel U, Bailey PJ, Wang SC, Downes M, Evans RM, Muscat GE. A dynamic role for HDAC7 in MEF2-mediated muscle differentiation.. J Biol Chem 2001 May 18;276(20):17007-13.
    doi: 10.1074/jbc.M101508200pubmed: 11279209google scholar: lookup
  11. Eivers SS, McGivney BA, Fonseca RG, MacHugh DE, Menson K, Park SD, Rivero JL, Taylor CT, Katz LM, Hill EW. Alterations in oxidative gene expression in equine skeletal muscle following exercise and training.. Physiol Genomics 2010 Jan 8;40(2):83-93.
    doi: 10.1152/physiolgenomics.00041.2009pubmed: 19861432google scholar: lookup
  12. Eivers SS, McGivney BA, Gu J, MacHugh DE, Katz LM, Hill EW. PGC-1α encoded by the PPARGC1A gene regulates oxidative energy metabolism in equine skeletal muscle during exercise.. Anim Genet 2012 Apr;43(2):153-62.
    doi: 10.1111/j.1365-2052.2011.02238.xpubmed: 22404351google scholar: lookup
  13. Fridén J, Lieber RL. Eccentric exercise-induced injuries to contractile and cytoskeletal muscle fibre components.. Acta Physiol Scand 2001 Mar;171(3):321-6.
    doi: 10.1046/j.1365-201x.2001.00834.xpubmed: 11412144google scholar: lookup
  14. Galatioto J, Mascareno E, Siddiqui MA. CLP-1 associates with MyoD and HDAC to restore skeletal muscle cell regeneration.. J Cell Sci 2010 Nov 1;123(Pt 21):3789-95.
    pmc: PMC2964110pubmed: 20940258doi: 10.1242/jcs.073387google scholar: lookup
  15. Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre M, Cefalu WT, Ye J. Butyrate improves insulin sensitivity and increases energy expenditure in mice.. Diabetes 2009 Jul;58(7):1509-17.
    doi: 10.2337/db08-1637pmc: PMC2699871pubmed: 19366864google scholar: lookup
  16. Gu Y, Song Y, Yin H, Lin S, Zhang X, Che L, Lin Y, Xu S, Feng B, Wu D, Fang Z. Dietary supplementation with tributyrin prevented weaned pigs from growth retardation and lethal infection via modulation of inflammatory cytokines production, ileal expression, and intestinal acetate fermentation.. J Anim Sci 2017 Jan;95(1):226-238.
    doi: 10.2527/jas.2016.0911pubmed: 28177354google scholar: lookup
  17. Hughes SM, Chi MM, Lowry OH, Gundersen K. Myogenin induces a shift of enzyme activity from glycolytic to oxidative metabolism in muscles of transgenic mice.. J Cell Biol 1999 May 3;145(3):633-42.
    doi: 10.1083/jcb.145.3.633pmc: PMC2185087pubmed: 10225962google scholar: lookup
  18. Hyldahl RD, Hubal MJ. Lengthening our perspective: morphological, cellular, and molecular responses to eccentric exercise.. Muscle Nerve 2014 Feb;49(2):155-70.
    doi: 10.1002/mus.24077pubmed: 24030935google scholar: lookup
  19. Iezzi S, Di Padova M, Serra C, Caretti G, Simone C, Maklan E, Minetti G, Zhao P, Hoffman EP, Puri PL, Sartorelli V. Deacetylase inhibitors increase muscle cell size by promoting myoblast recruitment and fusion through induction of follistatin.. Dev Cell 2004 May;6(5):673-84.
    pubmed: 15130492doi: 10.1016/s1534-5807(04)00107-8google scholar: lookup
  20. Joanisse S, Snijders T, Nederveen JP, Parise G. The Impact of Aerobic Exercise on the Muscle Stem Cell Response.. Exerc Sport Sci Rev 2018 Jul;46(3):180-187.
    doi: 10.1249/JES.0000000000000153pubmed: 29664744google scholar: lookup
  21. Kawai M, Aida H, Hiraga A, Miyata H. Muscle satellite cells are activated after exercise to exhaustion in Thoroughbred horses.. Equine Vet J 2013 Jul;45(4):512-7.
    doi: 10.1111/evj.12010pubmed: 23206314google scholar: lookup
  22. Leonel AJ, Teixeira LG, Oliveira RP, Santiago AF, Batista NV, Ferreira TR, Santos RC, Cardoso VN, Cara DC, Faria AM, Alvarez-Leite J. Antioxidative and immunomodulatory effects of tributyrin supplementation on experimental colitis.. Br J Nutr 2013 Apr 28;109(8):1396-407.
    doi: 10.1017/S000711451200342Xpubmed: 22906779google scholar: lookup
  23. Mal A, Harter ML. MyoD is functionally linked to the silencing of a muscle-specific regulatory gene prior to skeletal myogenesis.. Proc Natl Acad Sci U S A 2003 Feb 18;100(4):1735-9.
    doi: 10.1073/pnas.0437843100pmc: PMC149902pubmed: 12578986google scholar: lookup
  24. McGivney BA, Browne JA, Fonseca RG, Katz LM, Machugh DE, Whiston R, Hill EW. MSTN genotypes in Thoroughbred horses influence skeletal muscle gene expression and racetrack performance.. Anim Genet 2012 Dec;43(6):810-2.
    doi: 10.1111/j.1365-2052.2012.02329.xpubmed: 22497477google scholar: lookup
  25. Miyoshi M, Sakaki H, Usami M, Iizuka N, Shuno K, Aoyama M, Usami Y. Oral administration of tributyrin increases concentration of butyrate in the portal vein and prevents lipopolysaccharide-induced liver injury in rats.. Clin Nutr 2011 Apr;30(2):252-8.
    doi: 10.1016/j.clnu.2010.09.012pubmed: 21051124google scholar: lookup
  26. Murray RL, Zhang W, Iwaniuk M, Grilli E, Stahl CH. Dietary tributyrin, an HDAC inhibitor, promotes muscle growth through enhanced terminal differentiation of satellite cells.. Physiol Rep 2018 May;6(10):e13706.
    doi: 10.14814/phy2.13706pmc: PMC5974723pubmed: 29845774google scholar: lookup
  27. Nguyen TD, Prykhodko O, Fåk Hållenius F, Nyman M. Effects of monobutyrin and tributyrin on liver lipid profile, caecal microbiota composition and SCFA in high-fat diet-fed rats.. J Nutr Sci 2017;6:e51.
    doi: 10.1017/jns.2017.54pmc: PMC5672331pubmed: 29152255google scholar: lookup
  28. Nout YS, Hinchcliff KW, Jose-Cunilleras E, Dearth LR, Sivko GS, DeWille JW. Effect of moderate exercise immediately followed by induced hyperglycemia on gene expression and content of the glucose transporter-4 protein in skeletal muscles of horses.. Am J Vet Res 2003 Nov;64(11):1401-8.
    doi: 10.2460/ajvr.2003.64.1401pubmed: 14620777google scholar: lookup
  29. Peake JM, Neubauer O, Della Gatta PA, Nosaka K. Muscle damage and inflammation during recovery from exercise.. J Appl Physiol (1985) 2017 Mar 1;122(3):559-570.
    doi: 10.1152/japplphysiol.00971.2016pubmed: 28035017google scholar: lookup
  30. Rivero JL, Hill EW. Skeletal muscle adaptations and muscle genomics of performance horses.. Vet J 2016 Mar;209:5-13.
    doi: 10.1016/j.tvjl.2015.11.019pubmed: 26831154google scholar: lookup
  31. Rodgers JT, King KY, Brett JO, Cromie MJ, Charville GW, Maguire KK, Brunson C, Mastey N, Liu L, Tsai CR, Goodell MA, Rando TA. mTORC1 controls the adaptive transition of quiescent stem cells from G0 to G(Alert).. Nature 2014 Jun 19;510(7505):393-6.
    doi: 10.1038/nature13255pmc: PMC4065227pubmed: 24870234google scholar: lookup
  32. Rodgers JT, Schroeder MD, Ma C, Rando TA. HGFA Is an Injury-Regulated Systemic Factor that Induces the Transition of Stem Cells into G(Alert).. Cell Rep 2017 Apr 18;19(3):479-486.
    doi: 10.1016/j.celrep.2017.03.066pmc: PMC5468096pubmed: 28423312google scholar: lookup
  33. Rooney MF, Porter RK, Katz LM, Hill EW. Skeletal muscle mitochondrial bioenergetics and associations with myostatin genotypes in the Thoroughbred horse.. PLoS One 2017;12(11):e0186247.
    doi: 10.1371/journal.pone.0186247pmc: PMC5708611pubmed: 29190290google scholar: lookup
  34. Rosset R, Lecoultre V, Egli L, Cros J, Dokumaci AS, Zwygart K, Boesch C, Kreis R, Schneiter P, Tappy L. Postexercise repletion of muscle energy stores with fructose or glucose in mixed meals.. Am J Clin Nutr 2017 Mar;105(3):609-617.
    doi: 10.3945/ajcn.116.138214pubmed: 28100512google scholar: lookup
  35. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA. Pax7 is required for the specification of myogenic satellite cells.. Cell 2000 Sep 15;102(6):777-86.
    doi: 10.1016/s0092-8674(00)00066-0pubmed: 11030621google scholar: lookup
  36. Sheehan SM, Tatsumi R, Temm-Grove CJ, Allen RE. HGF is an autocrine growth factor for skeletal muscle satellite cells in vitro.. Muscle Nerve 2000 Feb;23(2):239-45.
    pubmed: 10639617doi: 10.1002/(sici)1097-4598(200002)23:2<239::aid-mus15>3.0.co;2-ugoogle scholar: lookup
  37. Snijders T, Nederveen JP, McKay BR, Joanisse S, Verdijk LB, van Loon LJ, Parise G. Satellite cells in human skeletal muscle plasticity.. Front Physiol 2015;6:283.
    doi: 10.3389/fphys.2015.00283pmc: PMC4617172pubmed: 26557092google scholar: lookup
  38. Tang H, Macpherson P, Marvin M, Meadows E, Klein WH, Yang XJ, Goldman D. A histone deacetylase 4/myogenin positive feedback loop coordinates denervation-dependent gene induction and suppression.. Mol Biol Cell 2009 Feb;20(4):1120-31.
    doi: 10.1091/mbc.e08-07-0759pmc: PMC2642751pubmed: 19109424google scholar: lookup
  39. Tatsumi R, Anderson JE, Nevoret CJ, Halevy O, Allen RE. HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells.. Dev Biol 1998 Feb 1;194(1):114-28.
    doi: 10.1006/dbio.1997.8803pubmed: 9473336google scholar: lookup
  40. Valberg SJ, Perumbakkam S, McKenzie EC, Finno CJ. Proteome and transcriptome profiling of equine myofibrillar myopathy identifies diminished peroxiredoxin 6 and altered cysteine metabolic pathways.. Physiol Genomics 2018 Dec 1;50(12):1036-1050.
    doi: 10.1152/physiolgenomics.00044.2018pmc: PMC6337024pubmed: 30289745google scholar: lookup
  41. von Maltzahn J, Jones AE, Parks RJ, Rudnicki MA. Pax7 is critical for the normal function of satellite cells in adult skeletal muscle.. Proc Natl Acad Sci U S A 2013 Oct 8;110(41):16474-9.
    doi: 10.1073/pnas.1307680110pmc: PMC3799311pubmed: 24065826google scholar: lookup
  42. Walsh ME, Bhattacharya A, Sataranatarajan K, Qaisar R, Sloane L, Rahman MM, Kinter M, Van Remmen H. The histone deacetylase inhibitor butyrate improves metabolism and reduces muscle atrophy during aging.. Aging Cell 2015 Dec;14(6):957-70.
    doi: 10.1111/acel.12387pmc: PMC4693467pubmed: 26290460google scholar: lookup
  43. Zhang Y, Yu B, Yu J, Zheng P, Huang Z, Luo Y, Luo J, Mao X, Yan H, He J, Chen D. Butyrate promotes slow-twitch myofiber formation and mitochondrial biogenesis in finishing pigs via inducing specific microRNAs and PGC-1α expression1.. J Anim Sci 2019 Jul 30;97(8):3180-3192.
    doi: 10.1093/jas/skz187pmc: PMC6667260pubmed: 31228349google scholar: lookup

Citations

This article has been cited 2 times.
  1. Dang X, Lee H, Lee SJ, Song JH, Mun S, Lee KY, Han K, Kim IH. Tributyrin and anise mixture supplementation improves growth performance, nutrient digestibility, jejunal villus height, and fecal microbiota in weaned pigs.. Front Vet Sci 2023;10:1107149.
    doi: 10.3389/fvets.2023.1107149pubmed: 36777676google scholar: lookup
  2. Busse NI, Gonzalez ML, Wagner AL, Johnson SE. Short Communication: Supplementation with calcium butyrate causes an increase in the percentage of oxidative fibers in equine gluteus medius muscle.. J Anim Sci 2022 Aug 1;100(8).
    doi: 10.1093/jas/skac108pubmed: 35908781google scholar: lookup
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.