Histochemistry and Cell Biology

, Volume 135, Issue 1, pp 21–26 | Cite as

In situ real-time imaging of the satellite cells in rat intact and injured soleus muscles using quantum dots

Original Paper


The recruitment of satellite cells, which are located between the basement membrane and the plasma membrane in myofibers, is required for myofiber repair after muscle injury or disease. In particular, satellite cell migration has been focused on as a satellite cell response to muscle injury because satellite cell motility has been revealed in cell culture. On the other hand, in situ, it is poorly understood how satellite cell migration is involved in muscle regeneration after injury because in situ it has been technically very difficult to visualize living satellite cells localized within skeletal muscle. In the present study, using quantum dots conjugated to anti-M-cadherin antibody, we attempted the visualization of satellite cells in both intact and injured skeletal muscle of rat in situ. As a result, the present study is the first to demonstrate in situ real-time imaging of satellite cells localized within the skeletal muscle. Moreover, it was indicated that satellite cell migration toward an injured site was induced in injured muscle while spatiotemporal change in satellite cells did not occur in intact muscle. Thus, it was suggested that the satellite cell migration may play important roles in the regulation of muscle regeneration after injury. Moreover, the new method used in the present study will be a useful tool to develop satellite cell-based therapies for muscle injury or disease.


Skeletal muscle Quantum dots Satellite cells In situ Real-time imaging 


  1. Allen RE, Sheehan SM, Taylor RG, Kendall TL, Rice GM (1995) Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro. J Cell Physiol 165:307–312CrossRefPubMedGoogle Scholar
  2. Anderson J, Pilipowicz O (2002) Activation of muscle satellite cells in single-fiber cultures. Nitric Oxide 7:36–41CrossRefPubMedGoogle Scholar
  3. Barbero A, Benelli R, Minghelli S, Tosetti F, Dorcaratto A, Ponzetto C, Wernig A, Cullen MJ, Albini A, Noonan DM (2001) Growth factor supplemented matrigel improves ectopic skeletal muscle formation—a cell therapy approach. J Cell Physiol 186:183–192CrossRefPubMedGoogle Scholar
  4. Bassaglia Y, Gautron J (1995) Fast and slow rat muscles degenerate and regenerate differently after whole crush injury. J Muscle Res Cell Motil 16:420–429CrossRefPubMedGoogle Scholar
  5. Bischoff R (1997) Chemotaxis of skeletal muscle satellite cells. Dev Dyn 208:505–515CrossRefPubMedGoogle Scholar
  6. Bornemann A, Schmalbruch H (1994) Immunocytochemistry of M-cadherin in mature and regenerating rat muscle. Anat Rec 239:119–125CrossRefPubMedGoogle Scholar
  7. Chambers RL, McDermott JC (1996) Molecular basis of skeletal muscle regeneration. Can J Appl Physiol 21:155–184PubMedGoogle Scholar
  8. Chen X, Li Y (2009) Role of matrix metalloproteinases in skeletal muscle: migration, differentiation, regeneration and fibrosis. Cell Adh Migr 3:337–341CrossRefPubMedGoogle Scholar
  9. Cornelison DD, Wold BJ (1997) Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191:270–283CrossRefPubMedGoogle Scholar
  10. El Fahime E, Torrente Y, Caron NJ, Bresolin MD, Tremblay JP (2000) In vivo migration of transplanted myoblasts requires matrix metalloproteinase activity. Exp Cell Res 258:279–287CrossRefPubMedGoogle Scholar
  11. Gao X, Yang L, Petros JA, Marshall FF, Simons JW, Nie S (2005) In vivo molecular and cellular imaging with quantum dots. Curr Opin Biotechnol 16:63–72CrossRefPubMedGoogle Scholar
  12. Gonda K, Watanabe TM, Ohuchi N, Higuchi H (2010) In vivo nano-imaging of membrane dynamics in metastatic tumor cells using quantum dots. J Biol Chem 285:2750–2757CrossRefPubMedGoogle Scholar
  13. Hawke TJ, Garry DJ (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91:534–551PubMedGoogle Scholar
  14. Jockusch H, Voigt S (2003) Migration of adult myogenic precursor cells as revealed by GFP/nLacZ labelling of mouse transplantation chimeras. J Cell Sci 116:1611–1616CrossRefPubMedGoogle Scholar
  15. Kawamura K, Takano K, Suetsugu S, Kurisu S, Yamazaki D, Miki H, Takenawa T, Endo T (2004) N-WASP and WAVE2 acting downstream of phosphatidylinositol 3-kinase are required for myogenic cell migration induced by hepatocyte growth factor. J Biol Chem 279:54862–54871CrossRefPubMedGoogle Scholar
  16. Klein-Ogus C, Harris JB (1983) Preliminary observations of satellite cells in undamaged fibres of the rat soleus muscle assaulted by a snake-venom toxin. Cell Tissue Res 230:671–676CrossRefPubMedGoogle Scholar
  17. Kosaka N, Ogawa M, Sato N, Choyke PL, Kobayashi H (2009) In vivo real-time, multicolor, quantum dot lymphatic imaging. J Invest Dermatol 129:2818–2822CrossRefPubMedGoogle Scholar
  18. Maltin CA, Harris JB, Cullen MJ (1983) Regeneration of mammalian skeletal muscle following the injection of the snake-venom toxin, taipoxin. Cell Tissue Res 232:565–577CrossRefPubMedGoogle Scholar
  19. Nelson SR, Ali MY, Trybus KM, Warshaw DM (2009) Random walk of processive, quantum dot-labeled myosin Va molecules within the actin cortex of COS-7 cells. Biophys J 97:509–518CrossRefPubMedGoogle Scholar
  20. Olson EN (1992) Interplay between proliferation and differentiation within the myogenic lineage. Dev Biol 154:261–272CrossRefPubMedGoogle Scholar
  21. Partridge TA, Morgan JE, Coulton GR, Hoffman EP, Kunkel LM (1989) Conversion of mdx myofibres from dystrophin-negative to -positive by injection of normal myoblasts. Nature 337:176–179CrossRefPubMedGoogle Scholar
  22. Pinaud F, Michalet X, Bentolila LA, Tsay JM, Doose S, Li JJ, Iyer G, Weiss S (2006) Advances in fluorescence imaging with quantum dot bio-probes. Biomaterials 27:1679–1687CrossRefPubMedGoogle Scholar
  23. Schultz E, Jaryszak DL, Valliere CR (1985) Response of satellite cells to focal skeletal muscle injury. Muscle Nerve 8:217–222CrossRefPubMedGoogle Scholar
  24. Schultz E, Albright DJ, Jaryszak DL, David TL (1988) Survival of satellite cells in whole muscle transplants. Anat Rec 222:12–17CrossRefPubMedGoogle Scholar
  25. Siegel AL, Atchison K, Fisher KE, Davis GE, Cornelison DDW (2009) 3D timelapse analysis of muscle satellite cell motility. Stem Cells 27:2527–2538CrossRefPubMedGoogle Scholar
  26. Tada H, Higuchi H, Wanatabe TM, Ohuchi N (2007) In vivo real-time tracking of single quantum dots conjugated with monoclonal anti-HER2 antibody in tumors of mice. Cancer Res 67:1138–1144CrossRefPubMedGoogle Scholar
  27. Tatsumi R, Anderson JE, Nevoret CJ, Halevy O, Allen RE (1998) HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev Biol 194:114–128CrossRefPubMedGoogle Scholar
  28. Villena J, Brandan E (2004) Dermatan sulfate exerts an enhanced growth factor response on skeletal muscle satellite cell proliferation and migration. J Cell Physiol 198:169–178CrossRefPubMedGoogle Scholar
  29. Wang W, Pan H, Murray K, Jefferson BS, Li Y (2009) Matrix metalloproteinase-1 promotes muscle cell migration and differentiation. Am J Pathol 174:541–549CrossRefPubMedGoogle Scholar
  30. Watt DJ, Karasinski J, Moss J, England MA (1994) Migration of muscle cells. Nature 368:406–407CrossRefPubMedGoogle Scholar
  31. Yoo J, Kambara T, Gonda K, Higuchi H (2008) Intracellular imaging of targeted proteins labeled with quantum dots. Exp Cell Res 314:3563–3569CrossRefPubMedGoogle Scholar
  32. Zhou H, Wu S, Joo JY, Zhu S, Han DW, Lin T, Trauger S, Bien G, Yao S, Zhu Y, Siuzdak G, Scholer HR, Duan L, Ding S (2009) Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 4:381–384CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Faculty of Education, Creative Arts and SciencesAichi University of EducationKariyaJapan
  2. 2.Department of Physical EducationAichi University of EducationKariyaJapan

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