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Human Cell

, Volume 30, Issue 3, pp 162–168 | Cite as

In vitro production of insulin-responsive skeletal muscle tissue from mouse embryonic stem cells by spermine-induced differentiation method

  • Mikako SaitoEmail author
  • Ayano Ishida
  • Shota Nakagawa
Rapid Communication

Abstract

The treatment of an embryoid body with spermine for a short duration can trigger the generation of a 3-dimensional multilayer myotube sheet (MMTS) that shows pulsatile activity. MMTS was previously characterized as a model of skeletal muscle tissue. In the present work, the insulin responsiveness of MMTS was investigated because it is an essential function for a model of skeletal muscle. The glucose uptake activity of MMTS was analyzed by confocal microscopy using fluorescent glucose analogs, namely 2-[N-(7-nitrobenz-2-oxa-1,3-diazol-4-yl)amino]-2-deoxy-d-glucose (2-NBDG) and its l-glucose counterpart, 2-NBDLG. The specific uptake rate of glucose was estimated from the difference between the fluorescent signals of 2-NBDG and 2-NBDLG. It was enhanced by insulin stimulation to 3.6 times higher than the control without insulin, and this insulin responsiveness was maintained for 5 days. The advantages of the 3-dimensional structure of MMTS are discussed in the contexts of its potential in vivo and in vitro uses.

Keywords

Fluorescent glucose analog Insulin-stimulated glucose uptake Multilayer myotube sheet Skeletal muscle tissue Spermine 

Notes

Acknowledgements

We thank Prof. Emer. Hideaki Matsuoka of Tokyo University of Agriculture and Technology for his valuable advice in bioimaging. The work was supported in part by the Strategic Research Promotion Program, the Ministry of Education, Culture, Sports, Science, and Technology, on the research subject “Development of Next Generation Bioresources”.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Kido Y, Burks DJ, Withers D, et al. Tissue-specific insulin resistance in mice with mutations in the insulin receptor, IRS-1, and IRS-2. J Clin Invest. 2000;105:199–205.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    González-Rodríguez Á, Mas-Gutierrez JA, Sanz-González S, et al. Inhibition of PTP1B restores IRS1-mediated hepatic insulin signaling in IRS2-deficient mice. Diabetes. 2010;59:588–99.CrossRefPubMedGoogle Scholar
  3. 3.
    Sato H, Kubota N, Kubota T, et al. Anagliptin increases insulin-induced skeletal muscle glucose uptake via an NO-dependent mechanism in mice. Diabetologia. 2016;59:2426–34.CrossRefPubMedGoogle Scholar
  4. 4.
    Al-Bayati A, Lukka D, Brown AE, Walker M. Effects of thrombin on insulin signalling and glucose uptake in cultured human myotubes. J Diabetes Complicat. 2016;30:1209–16.CrossRefPubMedGoogle Scholar
  5. 5.
    Bertuzzi A, Conte F, Mingrone G, Papa F, Salinari S, Sinisgalli C. Insulin signaling in insulin resistance states and cancer: a modeling analysis. PLoS One. 2016;11:e0154415.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Obanda DN, Ribnicky D, Yu Y, Stephens J, Cefalu WT. An extract of Urtica dioica L. mitigates obesity induced insulin resistance in mice skeletal muscle via protein phosphatase 2A (PP2A). Sci Rep. 2016;6:22222.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Sasaki T, Matsuoka H, Saito M. Generation of a multi-layer muscle fiber sheet from mouse ES cells by the spermine action at specific timing and concentration. Differentiation. 2008;76:1023–30.CrossRefPubMedGoogle Scholar
  8. 8.
    Saito M, Abe N, Ishida A, Nakagawa S, Matsuoka H. Concentration dependent effects of spermine on apoptosis and consequent generation of multilayer myotube sheets from mouse embryoid bodies in vitro. In Vitro Dev Biol Anim. 2014;50:973–81.CrossRefGoogle Scholar
  9. 9.
    Yoshioka K, Takahashi H, Homma T, et al. A novel fluorescence derivative of glucose applicable to the assessment of glucose uptake activity of Escherichia coli. Biochim Biophys Acta. 1996;1289:5–9.CrossRefPubMedGoogle Scholar
  10. 10.
    Ball SW, Bailey JR, Stewart JM, Vogels CM, Westcott SA. A fluorescent compound for glucose uptake measurements in isolated rat cardiomyocytes. Can J Physiol Pharmacol. 2002;80:205–9.CrossRefPubMedGoogle Scholar
  11. 11.
    Bernardinelli Y, Magistretti PJ, Chatton JY. Astrocytes generate Na+-mediated metabolic waves. Proc Natl Acad Sci USA. 2004;101:14937–42.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    O’Neil RG, Wu L, Mullani N. Uptake of a fluorescent deoxyglucose analog (2-NBDG) in tumor cells. Mol Imaging Biol. 2005;7:388–92.CrossRefPubMedGoogle Scholar
  13. 13.
    Yamada Y, Saito M, Matsuoka H, Inagaki N. A real-time method of imaging glucose uptake in single, living mammalian cells. Nat Prot. 2007;2:753–62.CrossRefGoogle Scholar
  14. 14.
    Yamamoto T, Nishiuchi Y, Teshima T, Matsuoka H, Yamada K. Synthesis of 2-NBDLG, a fluorescent derivative of l-glucosamine; the antipode of d-glucose tracer 2-NBDG. Tetrahedron Lett. 2008;49:6867–78.Google Scholar
  15. 15.
    Funabashi H, Ogino S, Saito M, Matsuoka H. Utilization of fluorescent glucose analog as a metabolic indicator during differentiation. Electrochemistry. 2012;80:299–301.CrossRefGoogle Scholar
  16. 16.
    Hashimoto H, Tamaki T, Hirata M, Uchiyama Y, Sato M, Mochida J. Reconstitution of the complete rupture in musculotendinous junction using skeletal muscle-derived multipotent stem cell sheet-pellets as a “bio-bond”. Peer J. 2016;4:e2231.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Culberson JW. Clinical aspects of glucose metabolism and chronic disease. Prog Mol Biol Transl Sci. 2017;146:1–11.CrossRefPubMedGoogle Scholar
  18. 18.
    Assi R, Foster TR, He H, et al. Delivery of mesenchymal stem cells in biomimetic engineered scaffolds promotes healing of diabetic ulcers. Regen Med. 2016;11:245–60.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Hall MN, Hall JK, Cadwallader AB, et al. Transplantation of skeletal muscle stem cells. Methods Mol Biol. 2017;1556:237–44.CrossRefPubMedGoogle Scholar
  20. 20.
    Darabi R, Pan W, Bosnakovski D, Baik J, Kyba M, Perlingeiro RCR. Functional myogenic engraftment from mouse iPS cells. Stem Cell Rev Rep. 2011;7:948–57.CrossRefGoogle Scholar
  21. 21.
    Mizuno Y, Chang H, Umeda K, et al. Generation of skeletal muscle stem/progenitor cells from murine induced pluripotent stem cells. FASEB J. 2010;24:2245–53.CrossRefPubMedGoogle Scholar
  22. 22.
    Tierney M, Sacco A. Engraftment of FACS isolated muscle stem cells into injured skeletal muscle. Methods Mol Biol. 2017;1556:223–36.CrossRefPubMedGoogle Scholar
  23. 23.
    Witt R, Weigand A, Boos AM, et al. Mesenchymal stem cells and myoblast differentiation under HGF and IGF-1 stimulation for 3D skeletal muscle tissue engineering. BMC Cell Biol. 2017;18:15(1–16).Google Scholar
  24. 24.
    Haywood NJ, Cordell PA, Tang KY, et al. Insulin-like growth factor binding protein 1 could improve glucose regulation and insulin sensitivity through its RGD domain. Diabetes. 2017;66:287–99.CrossRefPubMedGoogle Scholar
  25. 25.
    Hernández-Mijares A, Bañuls C, Peris JE, et al. A single acute dose of pinitol from a naturally occurring food ingredient decreases hyperglycemia and circulating insulin levels in healthy subjects. Food Chem. 2013;141:1267–72.CrossRefPubMedGoogle Scholar
  26. 26.
    Bañuls C, Rovira-Llopis S, Falcón R, et al. Chronic consumption of an inositol-enriched carob extract improves postprandial glycaemia and insulin sensitivity in healthy subjects: a randomized controlled trial. Clin Nutr. 2016;35:600–7.CrossRefPubMedGoogle Scholar
  27. 27.
    Santos JM, Benite-Ribeiro SA, Queiroz G, Duarte JA. The interrelation between aPKC and glucose uptake in the skeletal muscle during contraction and insulin stimulation. Cell Biochem Funct. 2014;32:621–4.CrossRefPubMedGoogle Scholar
  28. 28.
    Satoh T. Molecular mechanisms for the regulation of insulin-stimulated glucose uptake by small guanosine triphosphatases in skeletal muscle and adipocytes. Int J Mol Sci. 2014;15:18677–92.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Japan Human Cell Society and Springer Japan 2017

Authors and Affiliations

  1. 1.Department of Biotechnology and Life ScienceTokyo University of Agriculture and TechnologyTokyoJapan

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