- Short Communication
- Published:
Galectin-1 expression in innervated and denervated skeletal muscle
Cellular & Molecular Biology Letters volume 14, pages 128–138 (2009)
Abstract
Galectin-1 is a soluble carbohydrate-binding protein with a particularly high expression in skeletal muscle. Galectin-1 has been implicated in skeletal muscle development and in adult muscle regeneration, but also in the degeneration of neuronal processes and/or in peripheral nerve regeneration. Exogenously supplied oxidized galectin-1, which lacks carbohydrate-binding properties, has been shown to promote neurite outgrowth after sciatic nerve sectioning. In this study, we compared the expression of galectin-1 mRNA and immunoreactivity in innervated and denervated mouse and rat hind-limb and hemidiaphragm muscles. The results show that galectin-1 mRNA expression and immunoreactivity are up-regulated following denervation. The galectin-1 mRNA is expressed in the extrasynaptic and perisynaptic regions of the muscle, and its immunoreactivity can be detected in both regions by Western blot analysis. The results are compatible with a role for galectin-1 in facilitating reinnervation of denervated skeletal muscle.
Abbreviations
- Gal1:
-
galectin-1
- Inn:
-
innervated
- Den:
-
denervated
- PS:
-
perisynaptic
- ES:
-
extrasynaptic
References
Barondes, S.H., Cooper, D.N., Gitt, M.A. and Leffler, H. Galectins. Structure and function of a large family of animal lectins. J. Biol. Chem. 269 (1994) 20807–20810.
Hsu, D.K. and Liu, F-T. Regulation of cellular homeostasis by galectins. Glycoconj. J. 19 (2004) 507–515.
Cooper, D.N. and Barondes, S.H. Evidence for export of a muscle lectin from cytosol to extracellular matrix and for a novel secretory mechanism. J. Cell. Biol. 110 (1990) 1681–1691.
Cooper, D.N., Massa, S.M. and Barondes, S.H. Endogenous muscle lectin inhibits myoblast adhesion to laminin. J. Cell. Biol. 115 (1991) 1437–1448.
Georgiadis, V., Stewart, H.J., Pollard, H.J., Tavsanoglu, Y., Prasad, R., Horwood, J., Deltour, L., Goldring, K., Poirier, F. and Lawrence-Watt, D.J. Lack of galectin-1 results in defects in myoblast fusion and muscle regeneration. Dev. Dyn. 236 (2007) 1014–1024.
Watt, D.J., Jones, G.E. and Goldring, K. The involvement of galectin-1 in skeletal muscle determination, differentiation and regeneration. Glycoconj. J. 19 (2004) 615–619.
McGraw, J., McPhail, L.T., Oschipok, L.W., Horie, H., Poirier, F., Steeves, J.D., Ramer, M.S. and Tetzlaff, W. Galectin-1 in regenerating motoneurons. Eur. J. Neurosci. 20 (2004) 2872–2880.
Plachta, N., Annaheim, C., Bissière, S., Lin, S., Rüegg, M., Hoving, S., Müller, D., Poirier, F., Bibel, M. and Barde, Y-A. Identification of a lectin causing the degeneration of neuronal processes using engineered embryonic stem cells. Nat. Neurosci. 10 (2007) 712–719.
Akazawa, C., Nakamura, Y., Sango, K., Horie, H. and Kohsaka, S. Distribution of the galectin-1 mRNA in the rat nervous system: its transient upregulation in rat facial motor neurons after facial nerve axotomy. Neurosci. 125 (2004) 171-178.
Whitney, P.L., Powell, J.T. and Sanford, G.L. Oxidation and chemical modification of lung β-galactoside-specific lectin. Biochem. J. 238 (1986) 683–689.
Horie, H., Inagaki, Y., Sohma, Y., Nozawa, R., Okawa, K., Hasegawa, M., Muramatsu, N., Kawano, H., Horie, M., Koyama, H., Sakai, I., Takeshita, K., Kowada, Y., Takano, M. and Kadoya, T. Galectin-1 regulates initial axonal growth in peripheral nerves after axotomy. J. Neurosci. 19 (1999) 9964–9974.
Horie, H., Kadoya, T., Hikawa, N., Sango, K., Inoue, H., Takeshita, K., Asawa, R., Hiroi, T., Sato, M., Yoshioka, T. and Ishikawa, Y. Oxidized galectin-1 stimulates macrophages to promote axonal regeneration in peripheral nerves after axotomy. J. Neurosci. 24 (2004) 1873–1880.
Magnusson, C., Högklint, L., Libelius, R. and Tågerud, S. Expression of mRNA for plasminogen activators and protease nexin-1 in innervated and denervated mouse skeletal muscle. J. Neurosci. Res. 66 (2001) 457–463.
Wilson, T.J., Firth, M.N., Powell, J.T. and Harrison, F.L. The sequence of the mouse 14 kDa β-galactoside-binding lectin and evidence for its synthesis on free cytoplasmic ribosomes. Biochem. J. 261 (1989) 847–852.
Magnusson, C., Libelius, R. and Tågerud, S. Nogo (reticulon 4) expression in innervated and denervated mouse skeletal muscle. Mol. Cell. Neurosci. 22 (2003) 298–307.
Svensson, A., Libelius, R. and Tågerud, S. Semaphorin 6C expression in innervated and denervated skeletal muscle. J. Mol. Histol. 39 (2008) 5–13.
Raz, A., Carmi, P. and Pazerini, G. Expression of two different endogenous galactoside-binding lectins sharing sequence homology. Cancer Res. 48 (1988) 645–649.
Raz, A., Meromsky, L. and Lotan, R. Differential expression of endogenous lectins on the surface of nontumorigenic, tumorigenic, and metastatic cells. Cancer Res. 46 (1986) 3667–3672.
Batt, J., Bain, J., Goncalves, J., Michalski, B., Plant, P., Fahnestock, M. and Woodgett, J. Differential gene expression profiling of short and long term denervated muscle. FASEB J. 20 (2006) 115–117.
Gajendran, N., Frey, J.R., Lefkovits, I., Kuhn, L., Fountoulakis, M., Krapfenbauer, K. and Brenner, H.R. Proteomic analysis of secreted muscle components: Search for factors involved in neuromuscular synapse formation. Proteomics 2 (2002) 1601–1615.
Gonzalez de Aguilar, J-L., Niederhauser-Wiederkehr, C., Halter, B., De Tapia, M., Di Scala, F., Demougin, P., Dupuis, L., Primig, M., Meininger, V. and Loeffler, J-P. Gene profiling of skeletal muscle in an amyotrophic lateral sclerosis mouse model. Physiol. Genomics 32 (2008) 207–218.
Chan, J., O’Donoghue, K., Gavina, M., Torrente, Y., Kennea, N., Mehmet, H., Stewart, H., Watt, D.J., Morgan, J.E. and Fisk, N.M. Galectin-1 induces skeletal muscle differentiation in human fetal mesenchymal stem cells and increases muscle regeneration. Stem Cells 24 (2006) 1879–1891.
Sola, O.M. and Martin, A.W. Denervation hypertrophy and atrophy of the hemidiaphragm of the rat. Am. J. Physiol. 172 (1953) 324–332.
Feng, T-P. and Lu, D-X. New lights on the phenomenon of transient hypertrophy in the denervated hemidiaphragm of the rat. Sci. Sin. 14 (1965) 1772–1784.
Gutmann, E., Haníková, M., Hájek, I., Klicpera, M. and Syrovy, I. The postdenervation hypertrophy of the diaphragm. Physiol. Bohemoslov. 15 (1966) 508–524.
Zhan, W-Z. and Sieck, G.C. Adaptations of diaphragm and medial gastrocnemius muscles to inactivity. J. Appl. Physiol. 72 (1992) 1445–1453.
Zhan, W-Z., Farkas, G.A., Schroeder, M.A., Gosselin, L.E. and Sieck, G.C. Regional adaptations of rabbit diaphragm muscle fibers to unilateral denervation. J. Appl. Physiol. 79 (1995) 941–950.
Rowley, K.L., Mantilla, C.B. and Sieck, G.C. Respiratory muscle plasticity. Respir. Physiol. Neurobiol. 147 (2005) 235–251.
Chang-Hong, R., Wada, M., Koyama, S., Kimura, H., Arawaka, S., Kawanami, T., Kurita, K., Kadoya, T., Aoki, M., Itoyama, Y. and Kato, T. Neuroprotective effect of oxidized galectin-1 in a transgenic mouse model of amyotrophic lateral sclerosis. Exp. Neurol. 194 (2005) 203–211.
Cho, M. and Cummings, R.D. Galectin-1, a β-galactoside-binding lectin in chinese hamster ovary cells. J. Biol. Chem. 270 (1995) 5198–5206.
Adams, L., Scott, G.K. and Weinberg, C.S. Biphasic modulation of cell growth by recombinant human galectin-1. Biochim. Biophys. Acta 1312 (1996) 137–144.
Vas, V., Fajka-Boja, R., Ion, G., Dudics, V., Monostori, É. and Uher, F. Biphasic effect of recombinant galectin-1 on the growth and death of early hematopoietic cells. Stem Cells 23 (2005) 279–287.
Miura, T., Takahashi, M., Horie, H., Kurushima, H., Tsuchimoto, D., Sakumi, K. and Nakabeppu, Y. Galectin-1β, a natural monomeric form of galectin-1 lacking its six amino-terminal residues promotes axonal regeneration but not cell death. Cell Death Differ. 11 (2004) 1076–1083.
Hsieh, S.H., Ying, N.W., Wu, M.H., Chiang C.L., Hsu, C.L., Wong, T.Y., Jin, Y.T., Hong, T.M. and Chen, Y.L. Galectin-1, a novel ligand of neuropilin-1, activates VEGFR-2 signaling and modulates the migration of vascular endothelial cells. Oncogene 27 (2008) 3746–3753.
Pellet-Many, C., Frankel, P., Jia, H. and Zachary, I. Neuropilins: structure, function and role in disease. Biochem. J. 411 (2008) 211–226.
Moret, F., Renaudot, C., Bozon, M. and Castellani, V. Semaphorin and neuropilin co-expression in motoneurons sets axon sensitivity to environmental semaphorin sources during motor axon pathfinding. Development 134 (2007) 4491–4501.
Lambrechts, D. and Carmeliet, P. VEGF at the neurovascular interface: Therapeutic implications for motor neuron disease. Biochim. Biophys. Acta 1762 (2006) 1109–1121.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Svensson, A., Tågerud, S. Galectin-1 expression in innervated and denervated skeletal muscle. Cell Mol Biol Lett 14, 128–138 (2009). https://doi.org/10.2478/s11658-008-0039-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11658-008-0039-0