Skip to main content

Advertisement

SpringerLink
Log in

Investigation of differentially expressed proteins in rat gastrocnemius muscle during denervation–reinnervation

  • Original Paper
  • Published:
Journal of Muscle Research & Cell Motility Aims and scope Submit manuscript

Abstract

To have a better insight into the molecular events involved in denervation-induced atrophy and reinnervation-induced regeneration of skeletal muscles, it is important to investigate the changes in expression levels of a great multitude of muscle proteins during the process of denervation–reinnervation. In this study, we employed an experimental model of rat sciatic nerve crush to examine the differentially expressed proteins in the rat gastrocnemius muscle at different time points (0, 1, 2, 3, 4 weeks) after sciatic␣nerve crush by using two-dimensional gel electrophoresis (2-DE) followed by matrix-assisted laser desorption/ionization-time-of-flight mass spectrometry (MALDI-TOF-MS), collectively referred to as the modern proteomic analysis. The results showed that 16 proteins in the rat gastrocnemius muscle exhibited two distinct types of change pattern in their relative abundance: (1) The relative expression levels of 11 proteins (including alpha actin, myosin heavy chain, etc.)were decreased either within 1 or 2 weeks post-sciatic nerve injury, followed by restoration during the ensuing days until 4 weeks. (2) The other 5 proteins (including alpha enolase, beta enolase, signal peptide peptidase-like 3, etc.) displayed an up-regulation in their relative expression levels within 1 week following sciatic nerve injury, and a subsequent gradual decrease in their relative expression levels until 4 weeks. Moreover, the significance of the changes in expression levels of the 16 proteins during denervation–reinnervation has been selectively discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alway SE, Degens H, Krishnamurthy G, Chaudhrai A (2003) Denervation stimulates apoptosis but not Id2 expression in hindlimb muscles of aged rats. J Gerontol A Biol Sci Med Sci 58:687–697

    PubMed  Google Scholar 

  • Atomi Y, Yamada S, Nishida T (1991) Early changes of alpha B-crystallin mRNA in rat skeletal muscle to mechanical tension and denervation. Biochem Biophys Res Commun 181:1323–1330

    Article  PubMed  CAS  Google Scholar 

  • Bain JR, Mackinnon SE, Hunter DA (1989) Functional evaluation of complete sciatic, peroneal, and posterior tibial nerve lesions in the rat. Plast Reconstr Surg 83:129–138

    Article  PubMed  CAS  Google Scholar 

  • Baumann AP, Ibebunjo C, Grasser WA, Paralkar VM (2003) Myostatin expression in age and denervation-induced skeletal muscle atrophy. J Musculoskelet Neuronal Interact 3:8–16

    PubMed  CAS  Google Scholar 

  • Boissonneault G, Tremblay RR (1989) Effect of denervation on the androgen-induced expression of actin and CPK mRNAs in the levator ani muscle of the rat. FEBS Lett 257:329–332

    Article  PubMed  CAS  Google Scholar 

  • Booth FW, Criswell DS (1997) Molecular events underlying skeletal muscle atrophy and the development of effective countermeasures. Int J Sports Med 18 (Suppl 4):S265–S269

    Google Scholar 

  • Borisov AB, Carlson BM (2000) Cell death in denervated skeletal muscle is distinct from classical apoptosis. Anat Rec 258:305–318

    Article  PubMed  CAS  Google Scholar 

  • Clark JI, Muchowski PJ (2000) Small heat-shock proteins and their potential role in human disease. Curr Opin Struct Biol 10:52–59

    Article  PubMed  CAS  Google Scholar 

  • Davis HL, Kiernan JA, Goldspink DF, Goldspink DF, McGrath JA, Venter JC, Kidd GL, Williams RG, Maier A, Crockett JL, Simpson DR, Saubert CI, Edgerton VR, Edgerton VR, Barnard RJ, Peter JB, Maier PA, Simpson DR, Fudema JJ, Fizzell JA, Nelson EM (1981) Effect of nerve extract of atrophy of denervated or immobilized muscles. Exp Neurol 72:582–591

    Article  PubMed  CAS  Google Scholar 

  • Donoghue P, Ribaric S, Moran B, Cebasek V, Erzen I, Ohlendieck K (2004) Early effects of denervation on Ca(2+)-handling proteins in skeletal muscle. Int J Mol Med 13:767–772

    PubMed  CAS  Google Scholar 

  • DuBois DC, Max SR (1983) Effect of denervation and reinnervation on oxidation of [6–14C]glucose by rat skeletal muscle homogenates. J Neurochem 40:727–733

    PubMed  CAS  Google Scholar 

  • Eisenberg HA, Hood DA (1994) Blood flow, mitochondria, and performance in skeletal muscle after denervation and reinnervation. J Appl Physiol 76:859–866

    PubMed  CAS  Google Scholar 

  • Engel WK (1970) Selective and nonselective susceptibility of muscle fiber types. A new approach to human neuromuscular diseases. Arch Neurol 22:97–117

    PubMed  CAS  Google Scholar 

  • Furuno K, Goodman MN, Goldberg AL (1990) Role of different proteolytic systems in the degradation of muscle proteins during denervation atrophy. J Biol Chem 265:8550–8557

    PubMed  CAS  Google Scholar 

  • Gamble SC, Dunn MJ, Wheeler CH, Joiner MC, Adu-Poku A, Arrand JE (2000) Expression of proteins coincident with inducible radioprotection in human lung epithelial cells. Cancer Res 60:2146–2151

    PubMed  CAS  Google Scholar 

  • Geiger PC, Bailey JP, Zhan WZ, Mantilla CB, Sieck GC (2003) Denervation-induced changes in myosin heavy chain expression in the rat diaphragm muscle. J Appl Physiol 95:611–619

    PubMed  CAS  Google Scholar 

  • Glazner GW, Ishii DN (1995) Insulinlike growth factor gene expression in rat muscle during reinnervation. Muscle Nerve 18:1433–1442

    Article  PubMed  CAS  Google Scholar 

  • Goldspink DF, Morton AJ, Loughna P, Goldspink G (1986) The effect of hypokinesia and hypodynamia on protein turnover and the growth of four skeletal muscles of the rat. Pflugers Arch 407:333–340

    Article  PubMed  CAS  Google Scholar 

  • Grigorenko AP, Moliaka YK, Korovaitseva GI, Rogaev EI (2002) Novel class of polytopic proteins with domains associated with putative protease activity. Biochemistry (Mosc) 67:826–835

    Article  CAS  Google Scholar 

  • Haftek J, Thomas PK (1968) Electron-microscope observations on the effects of localized crush injuries on the connective tissues of peripheral nerve. J Anat 103:233–243

    PubMed  CAS  Google Scholar 

  • Hantai D, Rao JS, Festoff BW (1990) Rapid neural regulation of muscle urokinase-like plasminogen activator as defined by nerve crush. Proc Natl Acad Sci USA 87:2926–2930

    Article  PubMed  CAS  Google Scholar 

  • Helfman DM, Cheley S, Kuismanen E, Finn LA, Yamawaki-Kataoka Y (1986) Nonmuscle and muscle tropomyosin isoforms are expressed from a single gene by alternative RNA splicing and polyadenylation. Mol Cell Biol 6:3582–3595

    PubMed  CAS  Google Scholar 

  • Herbison GJ, Jaweed MM, Ditunno JF (1979) Muscle atrophy in␣rats following denervation, casting, inflammation, and tenotomy. Arch Phys Med Rehabil 60:401–404

    PubMed  CAS  Google Scholar 

  • Horwitz J (1992) Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci USA 89:10449–10453

    Article  PubMed  CAS  Google Scholar 

  • Horwitz J (2003) Alpha-crystallin. Exp Eye Res 76:145–153

    Article  PubMed  CAS  Google Scholar 

  • Inaguma Y, Goto S, Shinohara H, Hasegawa K, Ohshima K, Kato K (1993) Physiological and pathological changes in levels of the two small stress proteins, HSP27 and alpha B crystallin, in rat hindlimb muscles. J Biochem (Tokyo) 114:378–384

    CAS  Google Scholar 

  • Isfort RJ (2002) Proteomic analysis of striated muscle. J Chromatogr B Analyt Technol Biomed Life Sci 771:155–165

    Article  PubMed  CAS  Google Scholar 

  • Isfort RJ, Hinkle RT, Jones MB, Wang F, Greis KD, Sun Y, Keough TW, Anderson NL, Sheldon RJ (2000) Proteomic analysis of the atrophying rat soleus muscle following denervation. Electrophoresis 21:2228–2234

    Article  PubMed  CAS  Google Scholar 

  • Isfort RJ, Wang F, Greis KD, Sun Y, Keough TW, Bodine SC, Anderson NL (2002a) Proteomic analysis of rat soleus and tibialis anterior muscle following immobilization. J Chromatogr B Analyt Technol Biomed Life Sci 769:323–332

    CAS  Google Scholar 

  • Isfort RJ, Wang F, Greis KD, Sun Y, Keough TW, Farrar RP, Bodine SC, Anderson NL (2002b) Proteomic analysis of␣rat soleus muscle undergoing hindlimb suspension-induced atrophy and reweighting hypertrophy. Proteomics 2:543–550

    Article  CAS  Google Scholar 

  • Jackman RW, Kandarian SC (2004) The molecular basis of skeletal muscle atrophy. Am J Physiol Cell Physiol 287:C834–C843

    Article  PubMed  CAS  Google Scholar 

  • Jakubiec-Puka A, Kordowska J, Catani C, Carraro U (1990) Myosin heavy chain isoform composition in striated muscle after denervation and self-reinnervation. Eur J Biochem 193:623–628

    Google Scholar 

  • Jejurikar SS, Marcelo CL, Kuzon WM, Jr. (2002) Skeletal muscle denervation increases satellite cell susceptibility to apoptosis. Plast Reconstr Surg 110:160–168

    Article  PubMed  Google Scholar 

  • Jia L, Xu L, Jiang M, Gu Y, Zhang Z (2005) Protein abnormality in denervated skeletal muscles from patients with brachial injury. Microsurgery 25:316–321

    Article  PubMed  CAS  Google Scholar 

  • Kamradt MC, Chen F, Cryns VL (2001) The small heat shock protein alpha B-crystallin negatively regulates cytochrome c- and caspase−8-dependent activation of caspase−3 by inhibiting its autoproteolytic maturation. J Biol Chem 276:16059–16063

    Article  PubMed  CAS  Google Scholar 

  • Kamradt MC, Chen F, Sam S, Cryns VL (2002) The small heat shock protein alpha B-crystallin negatively regulates apoptosis during myogenic differentiation by inhibiting caspase−3 activation. J Biol Chem 277:38731–38736

    Article  PubMed  CAS  Google Scholar 

  • Kato K, Shimizu A, Semba R, Satoh T (1985) Tissue distribution, developmental profiles and effect of denervation of enolase isozymes in rat muscles. Biochim Biophys Acta 841:50–58

    PubMed  CAS  Google Scholar 

  • Lai KS, Jaweed MM, Seestead R, Herbison GJ, Ditunno JF Jr, McCully K, Chance B (1992) Changes in nerve conduction and Pi/PCr ratio during denervation–reinnervation of the gastrocsoleus muscles of rats. Arch Phys Med Rehabil 73:1155–1159

    PubMed  CAS  Google Scholar 

  • Lemberg MK, Martoglio B (2002) Requirements for signal peptide peptidase-catalyzed intramembrane proteolysis. Mol Cell 10:735–744

    Article  PubMed  CAS  Google Scholar 

  • Loughna P, Goldspink G, Goldspink DF (1986) Effect of inactivity and passive stretch on protein turnover in phasic and postural rat muscles. J Appl Physiol 61:173–179

    PubMed  CAS  Google Scholar 

  • Mao YW, Liu JP, Xiang H, Li DW (2004) Human alphaA- and alphaB-crystallins bind to Bax and Bcl-X(S) to sequester their translocation during staurosporine-induced apoptosis. Cell Death Differ 11:512–526

    Article  PubMed  CAS  Google Scholar 

  • Mao YW, Xiang H, Wang J, Korsmeyer S, Reddan J, Li DW (2001) Human Bcl−2 gene attenuates the ability of rabbit lens epithelial cells against H2O2-induced apoptosis through down-regulation of the alpha B-crystallin gene. J Biol Chem 276:43435–43445

    Article  PubMed  CAS  Google Scholar 

  • Migheli A, Mongini T, Doriguzzi C, Chiado-Piat L, Piva R, Ugo I, Palmucci L (1997) Muscle apoptosis in humans occurs in normal and denervated muscle, but not in myotonic dystrophy, dystrophinopathies or inflammatory disease. Neurogenetics 1:81–87

    Article  PubMed  CAS  Google Scholar 

  • Moir RD, Spann TP, Lopez-Soler RI, Yoon M, Goldman AE, Khuon S, Goldman RD (2000) Review: the dynamics of the nuclear lamins during the cell cycle––relationship between structure and function. J Struct Biol 129:324–334

    Article  PubMed  CAS  Google Scholar 

  • Ngai SM, Pearlstone JR, Farah CS, Reinach FC, Smillie LB, Hodges RS (2001) Structural and functional studies on Troponin I and Troponin C interactions. J Cell Biochem 83:33–46

    Article  PubMed  CAS  Google Scholar 

  • Nihei T, Monckton G (1980) A study of protein metabolism in denervation and reinnervation following sciatic nerve crush. FEBS Lett 119:275–278

    Article  PubMed  CAS  Google Scholar 

  • Sakimura K, Kushiya E, Ohshima-Ichimura Y, Mitsui H, Takahashi Y (1990) Structure and expression of rat muscle-specific enolase gene. FEBS Lett 277:78–82

    Article  PubMed  CAS  Google Scholar 

  • Simon M, Porter R, Brown R, Coulton GR, Terenghi G (2003) Effect of NT−4 and BDNF delivery to damaged sciatic nerves on phenotypic recovery of fast and slow muscles fibres. Eur J Neurosci 18:2460–2466

    Article  PubMed  Google Scholar 

  • Simon M, Terenghi G, Green CJ, Coulton GR (2000) Differential effects of NT−3 on reinnervation of the fast extensor digitorum longus (EDL) and the slow soleus muscle of rat. Eur J Neurosci 12:863–871

    Article  PubMed  CAS  Google Scholar 

  • Taillandier D, Aurousseau E, Meynial-Denis D, Bechet D, Ferrara M, Cottin P, Ducastaing A, Bigard X, Guezennec CY, Schmid HP et al (1996) Coordinate activation of lysosomal, Ca 2+-activated and ATP-ubiquitin-dependent proteinases in the unweighted rat soleus muscle. Biochem J␣316(Pt 1):65–72

    PubMed  CAS  Google Scholar 

  • Tang H, Cheung WM, Ip FC, Ip NY (2000) Identification and characterization of differentially expressed genes in denervated muscle. Mol Cell Neurosci 16:127–140

    Article  PubMed  CAS  Google Scholar 

  • Tews DS, Behrhof W, Schindler S (2005) Expression patterns of initiator and effector caspases in denervated human skeletal muscle. Muscle Nerve 31:175–181

    Article  PubMed  CAS  Google Scholar 

  • Tews DS, Goebel HH, Schneider I, Gunkel A, Stennert E, Neiss WF (1997) DNA-fragmentation and expression of apoptosis-related proteins in experimentally denervated and reinnervated rat facial muscle. Neuropathol Appl Neurobiol 23:141–149

    Article  PubMed  CAS  Google Scholar 

  • Thomason DB, Booth FW (1989) Influence of performance on gene expression in skeletal muscle: effects of forced inactivity. Adv Myochem 2:79–82

    PubMed  CAS  Google Scholar 

  • Wang X, Hu W, Cao Y, Yao J, Wu J, Gu XS (2005) Dog sciatic nerve regeneration across a 30-mm defect bridged by a chitosan/PGA artificial nerve graft. Brain 128:1897–1910

    Article  PubMed  Google Scholar 

  • Washabaugh CH, Ontell M (2001) Effect of chronic denervation and denervation–reinnervation on cytoplasmic creatine kinase transcript accumulation. J Neurobiol 47:194–206

    Article  PubMed  CAS  Google Scholar 

  • Weihofen A, Binns K, Lemberg MK, Ashman K, Martoglio B␣(2002) Identification of signal peptide peptidase, a presenilin-type aspartic protease. Science 296:2215–2218

    Article  PubMed  CAS  Google Scholar 

  • White KK, Vaughan DW (1991) Age effects on cytochrome oxidase activities during denervation and recovery of three muscle fiber types. Anat Rec 230:460–467

    Article  PubMed  CAS  Google Scholar 

  • Wu Z, Ji H, Gu Y (2002) Changes of gene expression in atrophic muscle induced by brachial plexus injury in rats. Chin J␣Traumatol 18:357–360

    Google Scholar 

Download references

Acknowledgment

This study was supported by Hi-Tech Research and Development Program of China (863 Program, Grant No. 2003AA205030) National Natural Science Foundation of China (Grant No. 30270427) and Jiangsu Province Natural Science Foundation of China (Grant No. BK 200236)

Author information

Authors and Affiliations

  1. The Jiangsu Key Laboratory of Neuroregeneration, Nantong University, 19 Qi-Xiu Road, Nantong, Jiangsu Province, 226001, P.R. China

    Hualin Sun, Jie Liu, Fei Ding, Xiaodong Wang, Mei Liu & Xiaosong Gu

Authors
  1. Hualin Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jie Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fei Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaodong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mei Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaosong Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiaosong Gu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sun, H., Liu, J., Ding, F. et al. Investigation of differentially expressed proteins in rat gastrocnemius muscle during denervation–reinnervation. J Muscle Res Cell Motil 27, 241–250 (2006). https://doi.org/10.1007/s10974-006-9067-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10974-006-9067-4

Keywords

Search

Navigation