Abstract
Background
Experimental and clinical studies have provided knowledge regarding osteogenesis during limb lengthening. However, response of skeletal muscle to limb lengthening is not fully understood, especially as concerns histogenesis. We studied the morphological response of rabbit skeletal muscle to limb lengthening. In this study, we investigated proliferation of satellite cells, responsible for generation of new myonuclei, during limb lengthening.
Methods
Tibialis anterior muscles of young and adult rabbits were subjected to lengthening at a rate of 0.mm twice per day for 20 days. After lengthening, muscle wet weight was measured to assess skeletal muscle growth, then proliferating cell nuclear antigen was measured. Immunostaining was performed to analyze proliferating cells in the proximal, middle, and distal portions of the muscle belly and the musculotendinous junction.
Results
Muscle wet weight increased significantly after lengthening both in adult (0.4g) and young (0.1g) rabbits. Satellite cells showed proliferation in response to lengthening. In adult rabbits, satellite cell proliferation increased along the entire lengthened muscle to a similar degree (from 7.1% in the middle portion to 8.6% in the musculotendinous junction). In young rabbits, proliferation was greater in the musculotendinous junction (4.8%) than that in other muscle portions (2.3% in the middle and distal portions, and 2.4% in the proximal portion). In adult rabbits, the rate of increase in satellite cell proliferation was 1780% in the middle portion to 2860% in the musculotendinous junction, whereas the rate was between 210% in the middle portion and 290% in the distal portion in young rabbit. The rate of increase in cell proliferation by lengthening was higher in adult muscle than that in young muscles as well as satellite cell proliferation.
Conclusion
These findings indicate that limb lengthening promotes muscle growth in both young and adult rabbits.
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References
GA Ilizarov (1990) ArticleTitleClinical application of the tension–stress effect for limb lengthening Clin Orthop 250 8–26 Occurrence Handle2403497
C Sangkaew (2005) ArticleTitleDistraction osteogenesis for the treatment of post traumatic complications using a conventional external fixator. A novel technique Injury 36 185–93 Occurrence Handle15589939
KS Leung WH Cheung HY Yeung KM Lee KP Fung (2004) ArticleTitleEffect of weightbearing on bone formation during distraction osteogenesis Clin Orthop 419 251–7 Occurrence Handle10.1097/00003086-200402000-00041 Occurrence Handle15021163
RH Meffert JE Tis N Inoue EF McCarthy E Brug EYS Chao (2000) ArticleTitlePrimary resective shortening followed by distraction osteogenesis for limb reconstruction: a comparison with simple lengthening J Orthop Res 18 629–36 10.1002/jor.1100180416 Occurrence Handle10.1002/jor.1100180416 Occurrence Handle1:STN:280:DC%2BD3crgtl2msg%3D%3D Occurrence Handle11052500
H Mizuta E Nakamura S Kudo T Maeda K Takagi (2004) ArticleTitleGreater frequency of distraction accelerates bone formation in open-wedge proximal tibial osteotomy with hemicallotasis Acta Orthop Scand 75 588–93 10.1080/00016470410001475 Occurrence Handle15513492 Occurrence Handle10.1080/00016470410001475
B Fink E Neuen-Jacob A Lienert A Francke O Niggemeyer W Rüther (2001) ArticleTitleChanges in canine skeletal muscles during experimental tibial lengthening Clin Orthop 385 207–18 Occurrence Handle10.1097/00003086-200104000-00032 Occurrence Handle11302316
T Nagaoka M Abe H Yoshimoto H Shirai T Onomura (1995) ArticleTitleMorphological study of the elongated muscle in limb lengthening Eur J Exp Musculoskel Res 4 188–94
H Yamazaki M Abe K Kanbara (2003) ArticleTitleChanges of fiber type ratio and diameter in rabbit skeletal muscle during limb lengthening J Orthop Sci 8 75–8 Occurrence Handle10.1007/s007760300012 Occurrence Handle12560890
CA Lindsey MR Makarov S Shoemaker JG Birch PH Buschang AM Cherkashin et al. (2002) ArticleTitleThe effect of the amount of limb lengthening on skeletal muscle Clin Orthop 402 278–87 Occurrence Handle10.1097/00003086-200209000-00028 Occurrence Handle12218494
P Williams P Kyberd H Simpson J Kenwright G Goldspink (1998) ArticleTitleThe morphological basis of increased stiffness of rabbit tibialis anterior muscles during surgical limb-lengthening J Anat 193 131–8 10.1046/j.1469-7580.1998.19310131.x Occurrence Handle10.1046/j.1469-7580.1998.19310131.x Occurrence Handle9758143
T Matano K Tamai T Kurokawa (1994) ArticleTitleAdaptation of skeletal muscle in limb lengthening: a light diffraction study on the sarcomere length in situ J Orthop Res 12 193–6 10.1002/jor.1100120207 Occurrence Handle10.1002/jor.1100120207 Occurrence Handle1:STN:280:DyaK2c3hs12qsA%3D%3D Occurrence Handle8164091
K Tamai T Kurokawa I Matsubara (1989) ArticleTitleIn situ observation of adjustment of sarcomere length in skeletal muscle under sustained stretch J Jpn Orthop Assoc 63 1558–63 Occurrence Handle1:STN:280:DyaK3c7ntFKltA%3D%3D
CS Day MS Moreland SS Floyd SuffixJr J Huard (1997) ArticleTitleLimb lengthening promotes muscle growth J Orthop Res 15 227–34 Occurrence Handle10.1002/jor.1100150211 Occurrence Handle1:STN:280:DyaK2szhtVCmug%3D%3D Occurrence Handle9167625
B Schumacher J Keller I Hvid (1994) ArticleTitleDistraction effects on muscle. Leg lengthening studied in rabbits Acta Orthop Scand 65 647–50 Occurrence Handle1:STN:280:DyaK2M7ktFyisQ%3D%3D Occurrence Handle7839853
T Matsushita K Nakamura T Kurokawa (1999) ArticleTitleTensile force in limb lengthening: histogenesis or only mechanical elongation Orthopedics 22 61–3 Occurrence Handle1:STN:280:DyaK1M7it1GrtA%3D%3D Occurrence Handle9925198
E Schultz KM McCormick (1994) ArticleTitleSkeletal muscle satellite cells Rev Physiol Biochem Pharmacol 123 213–57 Occurrence Handle10.1007/BFb0030904 Occurrence Handle1:STN:280:DyaK2c3mvFGjsA%3D%3D Occurrence Handle8209136
TJ Hawke DJ Garry (2001) ArticleTitleMyogenic satellite cells: physiology to molecular biology J Appl Physiol 91 534–51 Occurrence Handle1:CAS:528:DC%2BD3MXmtVyrurY%3D Occurrence Handle11457764
R Bravo R Frank PA Blundell H Macdonald-Bravo (1987) ArticleTitleCyclin/PCNA is the auxiliary protein of DNA polymerase-delta Nature (Lond) 326 515–7 Occurrence Handle10.1038/326515a0 Occurrence Handle1:CAS:528:DyaL2sXhvFWntr8%3D
B Shpitz Y Bomstein Y Mekori R Cohen Z Kaufman M Grankin et al. (1997) ArticleTitleProliferating cell nuclear antigen as a marker of cell kinetics in aberrant crypt foci, hyperplastic polyps, adenomas, and adenocarcinomas of the human colon Am J Surg 174 425–30 10.1016/S0002-9610(97)00122-0 Occurrence Handle10.1016/S0002-9610(97)00122-0 Occurrence Handle1:STN:280:DyaK2svnslWjtw%3D%3D Occurrence Handle9337168
V Renault LE Thorne PO Eriksson G Butler-Browne V Mouly (2002) ArticleTitleRegenerative potential of human skeletal muscle during aging Aging Cell 1 132–9 10.1046/j.1474-9728.2002.00017.x Occurrence Handle10.1046/j.1474-9728.2002.00017.x Occurrence Handle1:CAS:528:DC%2BD3sXktlSqt7k%3D Occurrence Handle12882343
RN Cooper S Tajbakhsh V Mouly G Cossu M Buckigham GS Butler-Browne (1999) ArticleTitleIn vivo satellite cell activation via Myf5 and MyoD in regenerating mouse skeletal muscle J Cell Sci 112 2895–901 Occurrence Handle1:CAS:528:DyaK1MXmtlWqs7k%3D Occurrence Handle10444384
R Tatsumi SM Sheehan H Iwasaki A Hattori RE Allen (2001) ArticleTitleMechanical stretch induces activation of skeletal muscle satellite cells in vitro Exp Cell Res 267 107–14 10.1006/excr.2001.5252 Occurrence Handle10.1006/excr.2001.5252 Occurrence Handle1:CAS:528:DC%2BD3MXksVWqtLs%3D Occurrence Handle11412043
J Anderson O Pilipowicz (2002) ArticleTitleActivation of muscle satellite cells in single-fiber cultures Nitric Oxide 7 36–41 10.1016/S1089-8603(02)00011-3 Occurrence Handle10.1016/S1089-8603(02)00011-3 Occurrence Handle1:CAS:528:DC%2BD38XmtFSitLY%3D Occurrence Handle12175818
V Jacquemin D Furling A Bigot GS Butler-Browne V Mouly (2004) ArticleTitleIGF-1 induces human myotube hypertrophy by increasing cell recruitment Exp Cell Res 299 148–58 10.1016/j.yexcr.2004.05.023 Occurrence Handle10.1016/j.yexcr.2004.05.023 Occurrence Handle1:CAS:528:DC%2BD2cXmsVKgu74%3D Occurrence Handle15302582
R Tatsumi JE Anderson CJ Nevoret O Halevy RE Allen (1998) ArticleTitleHGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells Dev Biol 194 114–28 10.1006/dbio.1997.8803 Occurrence Handle10.1006/dbio.1997.8803 Occurrence Handle1:CAS:528:DyaK1cXhsVKmsr8%3D Occurrence Handle9473336
B Mackay TJ Harrop AR Muir (1969) ArticleTitleThe fine structure of the muscle tendon junction in the rat Acta Anat (Basel) 73 588–602 Occurrence Handle10.1159/000143318 Occurrence Handle1:STN:280:DyaE3c3gtFOguw%3D%3D
PE Williams G Goldspink (1971) ArticleTitleLongitudinal growth of striated *T*muscle fibers J Cell Sci 9 751–67 Occurrence Handle1:STN:280:DyaE387nvVCltQ%3D%3D Occurrence Handle5148015
N Yasui H Kojimoto H Shimizu Y Shimomura (1991) ArticleTitleThe effect of distraction upon bone, muscle, and periosteum Orthop Clin N Am 22 563–7 Occurrence Handle1:STN:280:DyaK38%2FltVOjug%3D%3D
P Seale A Asakura MA Rudnicki (2001) ArticleTitleThe potential of muscle stem cells Dev Cell 1 333–42 10.1016/S1534-5807(01)00049-1 Occurrence Handle10.1016/S1534-5807(01)00049-1 Occurrence Handle1:CAS:528:DC%2BD3MXntlamtbw%3D Occurrence Handle11702945
HC Olguin BB Olwin (2004) ArticleTitlePax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: a potential mechanism for self-renewal Dev Biol 275 375–88 10.1016/j.ydbio.2004.08.015 Occurrence Handle10.1016/j.ydbio.2004.08.015 Occurrence Handle1:CAS:528:DC%2BD2cXovVKltb0%3D Occurrence Handle15501225
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Tsujimura, T., Kinoshita, M. & Abe, M. Response of rabbit skeletal muscle to tibial lengthening. J Orthop Sci 11, 185–190 (2006). https://doi.org/10.1007/s00776-005-0991-8
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DOI: https://doi.org/10.1007/s00776-005-0991-8