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01-07-2009 | Original Article

The effect of downhill running on Notch signaling in regenerating skeletal muscle

Authors: Susan K. Tsivitse, Michael G. Peters, Angel L. Stoy, Jeffrey A. Mundy, Robert S. Bowen

Published in: European Journal of Applied Physiology | Issue 5/2009

Abstract

Notch signaling expression in regenerating muscle following injurious downhill running (DHR) was characterized in male C57BL/J6 mice (3 mo). Hindlimb muscles were harvested from control mice or at 24, 48, 72, 96 or 120 h post-DHR. Muscle injury was observed at 96 h (3.3-fold) and 120 h (3.7-fold) post-DHR (P < 0.01) and elevated MCadherin expression at 72 h (2.7-fold), 96 h (2.4-fold) post-DHR (P < 0.05) and 120 h (3.3-fold) post-DHR (P < 0.01). Desmin increased at 72 h (2.2-fold), 96 h (3-fold) and 120 h (1.8-fold) post-DHR (P < 0.05). Delta1 +/MCadherin + cells increased ~2-fold at 72, 96 (P < 0.01) and 120 h post-DHR (P < 0.05). Isolated muscle-associated cells increased Delta1 (2.6-fold) (P < 0.05) and Notch1 (fourfold) (P < 0.01) expression at 120 h post-DHR. The results of this novel study indicate that DHR up-regulates Notch components within myoblasts and regenerating muscle.

Allbrook D (1981) Skeletal muscle regeneration. Muscle Nerve 4:234–245. doi:10.1002/mus.880040311 PubMedCrossRef

Armand A, Launay T, Gapera BD, Charbonnier F, Gallien CL, Chanoine C (2003) Effects of eccentric treadmill running on mouse soleus: degeneration/regeneration studied with Myf-5 and MyoD probes. Acta Physiol Scand 179:75–84. doi:10.1046/j.1365-201X.2003.01187.x PubMedCrossRef

Artavanis-Tsakonas S, Ran MD, Lake RJ (1999) Notch signaling: cell fate control signal integration in development. Science 284:770–776. doi:10.1126/science.284.5415.770 PubMedCrossRef

Berezovska O, Jack C, McLean P, Aster JC, Hicks C, Xia W, Wolfe MS, Weinmaster G, Selkoe DJ, Hyman BT (2000) Rapid Notch1 nuclear translocation after ligand binding depends on presenilin-associated gamma-secretase activity. Ann N Y Acad Sci 920:223–226PubMedCrossRef

Boppart M, Burkin DJ, Kaufman SJ (2006) Alpha7-beta1-integrin regulates mechanotransduction and prevents skeletal muscle injury. Am J Physiol Cell Physiol 290:C1660–C1665. doi:10.1152/ajpcell.00317.2005 PubMedCrossRef

Carey K, Farnfield MM, Tarquinio SD, Cameron-Smith D (2007) Impaired expression of notch signaling genes in aged human skeletal muscle. J Gerontol Biol Sci A 62A(1):9–17

Charge S, Rudnicki MA (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev 84:209–238. doi:10.1152/physrev.00019.2003 PubMedCrossRef

Chen J, Goldhamer DJ (2003) Skeletal muscle stem cells. Reprod Biol Endocrinol 1:101. doi:10.1186/1477-7827-1-101 PubMedCrossRef

Chiba S (2006) Notch signaling in stem cell systems. Stem Cells 24:2437–2447. doi:10.1634/stemcells.2005-0661 PubMedCrossRef

Conboy I, Rando TA (2002) The regulation of notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell 3:397–409. doi:10.1016/S1534-5807(02)00254-X PubMedCrossRef

Conboy I, Conboy MJ, Smythe GM, Rando TA (2003) Notch-mediated restoration of regenerative potential aged muscle. Science 302:1575–1577. doi:10.1126/science.1087573 PubMedCrossRef

Conboy I, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA (2005) Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433:760–764. doi:10.1038/nature03260 PubMedCrossRef

Cornelison DD, Wold BJ (1997) Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191:270–283. doi:10.1006/dbio.1997.8721 PubMedCrossRef

Cossu G, Biressi S (2005) Satellite cells, myoblasts and other occasional myogenic progenitors: possible origin, phenotypic features and role in muscle regeneration. Semin Cell Dev Biol 16:623–631. doi:10.1016/j.semcdb.2005.07.003 PubMedCrossRef

Dahlqvist C, Blokzijl A, Chapman G, Falk A, Dannaeus K, Ibanez CF, Lendahl U (2003) Functional notch signaling is required for BMP4-induced inhibition of myogenic differentiation. Development 130:6089–6099. doi:10.1242/dev.00834 PubMedCrossRef

Figeac N, Daczewska M, Marcelle C, Kagla K (2007) Muscle stem cells and model systems for their investigation. Dev Dyn 236:3332–3342. doi:10.1002/dvdy.21345 PubMedCrossRef

Hamer P, McGeachie JM, Grounds MD (2002) Evans Blue Dye as an in vivo marker of myofibre damage: optimising parameters for detecting initial myofibre membrane permeability. J Anat 200:69–79. doi:10.1046/j.0021-8782.2001.00008.x PubMedCrossRef

Holterman C, Rudnicki MA (2005) Molecular regulation of satellite cell function. Semin Cell Dev Biol 16:575–584. doi:10.1016/j.semcdb.2005.07.004 PubMedCrossRef

Ishido M, Uda M, Masuhara M, Kami K (2006) Alterations of M-cadherin, neural cell adhesion molecule and β-catenin expression in satellite cells during overload-induced skeletal muscle hypertrophy. Acta Physiol (Oxf) 187:407–418. doi:10.1111/j.1748-1716.2006.01577.x CrossRef

Karlstrom H, Bergman A, Lendahl U, Naslunc J, Lundkvist J (2002) A sensitive and quantitative assay for measuring cleavage of presenilin substrates. J Biol Chem 277(9):6763–6766. doi:10.1074/jbc.C100649200 PubMedCrossRef

Kitzmann M, Bonnieu A, Duret C, Vernus B, Barro M, Laodj-Chevivesse D, Verdi JM, Carnac G (2006) Inhibition of notch signaling induces myotube hypertrophy by recruiting a subpopulation of reserve cells. J Cell Physiol 208:538–548. doi:10.1002/jcp.20688 PubMedCrossRef

Kuroday K, Tani S, Tamura K, Minoguchi S, Kurooka H, Honjo T (1999) Delta-induced notch signaling mediated by RBP-J inhibits MyoD expression and myogenesis. J Biol Chem 274(11):7238–7244. doi:10.1074/jbc.274.11.7238 CrossRef

Nofziger D, Miyamoto A, Lyons KM, Weinmaster G (1999) Notch signaling imposes two distinct blocks in the differentiation of C2C12 myoblasts. Development 126:1689–1702PubMed

Sasamura T, Sasaki N, Miyashita F, Nakao S, Ishikawa HO, Ito M, Kitagawa M, Harigaya K, Spana E, Bilder D, Perrimon N, Matsuno K (2003) Neurotic, a novel maternal neurogenic gene, encodes an O-fucosyltransferase that is essential for Notch–Delta interactions. Development 130(20):4785–4795. doi:10.1242/dev.00679 PubMedCrossRef

Schuster-Gossler K, Cordes R, Gossler A (2007) Premature myogenic differentiation and depletion of progenitor cells cause severe muscle hypotrophy in Delta1 mutants. Proc Natl Acad Sci USA 104:537–542. doi:10.1073/pnas.0608281104 PubMedCrossRef

Shawber C, Nofziger D, Hsieh JJD, Lindsell C, Bogler O, Hayward D, Weinmaster G (1996) Notch signaling inhibits muscle cell differentiation through a CBF1-independent pathway. Development 122:3765–3773PubMed

Shi X, Garry DJ (2006) Muscle stem cells in development, regeneration, and disease. Genes Dev 20:1692–1708. doi:10.1101/gad.1419406 PubMedCrossRef

Smith H, Plyley MJ, Rogers CD, McKee NH (1997) Skeletal muscle damage in the rat hindlimb following single or repeated daily bouts of downhill exercise. Int J Sports Med 18:94–100. doi:10.1055/s-2007-972602 PubMedCrossRef

Tsivitse S, McLoughlin TJ, Peterson JM, Mylona E, McGregor SJ, Pizza FX (2003) Downhill running in rats: influence on neutrophils, macrophages, and MyoD + cells in skeletal muscle. Eur J Physiol Occup Physiol 90:633–638. doi:10.1007/s00421-003-0909-0 CrossRef

Turner M, Kleeberger SR, Lightfoot JT (2005) Influence of genetic background on daily running-wheel activity differs with aging. Physiol Genomics 16(22):76–85. doi:10.1152/physiolgenomics.00243.2004

Title: The effect of downhill running on Notch signaling in regenerating skeletal muscle
Authors: Susan K. Tsivitse
Michael G. Peters
Angel L. Stoy
Jeffrey A. Mundy
Robert S. Bowen
Publication date: 01-07-2009
Publisher: Springer-Verlag
Published in: European Journal of Applied Physiology / Issue 5/2009
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI: https://doi.org/10.1007/s00421-009-1077-7

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The effect of downhill running on Notch signaling in regenerating skeletal muscle

Abstract

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