Cyclic mechanical strain maintains Nanog expression through PI3K/Akt signaling in mouse embryonic stem cells

Experimental Cell Research

Volumn 318, Issue 14, 2012, Pages 1726-1732

  Horiuchi, Rie ^a   Akimoto, Takayuki ^a,b   Hong, Zhang ^b   Ushida, Takashi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b WASEDA UNIVERSITY   (Japan)

Author keywords

Actin; Embryonic germ (EG); Embryonic stem (ES); Focal adhesion kinase (FAK); Mechano transduction; Mechanobiology; Stemness; Stretch

Indexed keywords

CYTOCHALASIN D; LEUKEMIA INHIBITORY FACTOR; MESSENGER RNA; OCTAMER TRANSCRIPTION FACTOR 4; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; WORTMANNIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL RENEWAL; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENZYME PHOSPHORYLATION; GENE EXPRESSION REGULATION; INTRACELLULAR SIGNALING; MECHANICAL STRESS; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; TRANSCRIPTION INITIATION;

EID: 84862892940     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2012.05.021     Document Type: Article

References (36)

1. Evans M.J., Kaufman M.H. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981, 292:154-156.
2. Smith A.G., Heath J.K., Donaldson D.D., Wong G.G., Moreau J., Stahl M., Rogers D. Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature 1988, 336:688-690.
3. Williams R.L., Hilton D.J., Pease S., Willson T.A., Stewart C.L., Gearing D.P., Wagner E.F., Metcalf D., Nicola N.A., Gough N.M. Myeloid leukemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature 1988, 336:684-687.
4. Chambers I., Colby D., Robertson M., Nichols J., Lee S., Tweedie S., Smith A. Functional expression cloning of Nanog pluripotency sustaining factor in embryonic stem cells. Cell 2003, 13:643-655.
5. Mitsui K., Tokuzawa Y., Itoh H., Segawa K., Murakami M., Takahashi K., Maruyama M., Maeda M., Yamanaka S. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003, 113:631-642.
6. Boyer L.A., Lee T.I., Cole M.F., Johnstone S.E., Levine S.S., Zucker J.P., Guenther M.G., Kumar R.M., Murray H.L., Jenner R.G., Gifford D.K., Melton D.A., Jaenisch R., Young R.A. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005, 122:947-956.
7. Rodda D.J., Chew J.L., Lim L.H., Loh Y.H., Wang B., Ng H.H., Robson P. Transcriptional regulation of nanog by OCT4 and SOX2. J. Biol. Chem. 2005, 280:24731-24737.
8. Niwa H., Miyazaki J., Smith A.G. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 2000, 24:372-376.
9. Altman G.H., Horan R.L., Martin I., Farhadi J., Stark P.R., Volloch V., Richmond J.C., Vunjak-Novakovic G., Kaplan D.L. Cell differentiation by mechanical stress. FASEB J. 2002, 16:270-272.
10. Lee D.A., Knight M.M., Campbell J.J., Bader D.L. Stem cell mechanobiology. J. Cell Biochem. 2011, 112:1-9.
11. Saha S., Ji L., de Pablo J.J., Palecek S.P. Inhibition of human embryonic stem cell differentiation by mechanical strain. J. Cell Physiol. 2006, 206:126-137.
12. Akimoto T., Ushida T., Miyaki S., Akaogi H., Tsuchiya K., Yan Z., Williams R.S., Tateishi T. Mechanical stretch inhibits myoblast-to-adipocyte differentiation through Wnt signaling. Biochem. Biophys. Res. Commun. 2005, 329:381-385.
13. Wada S., Kato Y., Okutsu M., Miyaki S., Suzuki K., Yan Z., Schiaffino S., Asahara H., Ushida T., Akimoto T. Translational suppression of atrophic regulators by miR-23a integrates resistance to skeletal muscle atrophy. J. Biol. Chem. 2011, 286:38456-38465.
14. Takahashi K., Murakami M., Yamanaka S. Role of the phosphoinositide3-kinase pathway in mouse embryonic stem (ES) cells. Biochem. Soc. Trans. 2005, 33:1522-1525.
15. Watanabe S., Umehara H., Murayama K., Okabe M., Kimura T., Nakano T. Activation of Akt signaling is sufficient to maintain pluripotency in mouse and primate embryonic stem cells. Oncogene 2006, 25:2697-2707.
16. Chapman G.B., Durante W., Hellums J.D., Schafer A.I. Physiological cyclic stretch causes cell cycle arrest in cultured vascular smooth muscle cells. Am. J. Physiol. Heart Circ. Physiol. 2000, 278:H748-H754.
17. Ghazanfari S., Tafazzoli-Shadpour M., Shokrgozar M.A. Effects of cyclic stretch on proliferation of mesenchymal stem cells and their differentiation to smooth muscle cells. Biochem. Biophys. Res. Commun. 2009, 388:601-605.
18. Liu M., Skinner S.J., Xu J., Han R.N., Tanswell A.K., Post M. Stimulation of fetal rat lung cell proliferation in vitro by mechanical stretch. Am. J. Physiol. 1992, 263:L376-L383.
19. Predel H.G., Yang Z., von Segesser L., Turina M., Bühler F.R., Lüscher T.F. Implications of pulsatile stretch on growth of saphenous vein and mammary artery smooth muscle. Lancet 1992, 340:878-879.
20. Shimizu N., Yamamoto K., Obi S., Kumagaya S., Masumura T., Shimano Y., Naruse K., Yamashita J.K., Igarashi T., Ando J. Cyclic strain induces mouse embryonic stem cell differentiation into vascular smooth muscle cells by activating PDGF receptor beta. J. Appl. Physiol. 2008, 104:766-772.
21. Niwa H., Burdon T., Chambers I., Smith A.G. Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev. 1998, 12:2048-2060.
22. Saha S., Ji L., de Pablo J.J., Palecek S.P. TGFbeta/Activin/Nodal pathway in inhibition of human embryonic stem cell differentiation by mechanical strain. Biophys. J. 2008, 94:4123-4133.
23. Niwa H., Ogawa K., Shimosato D., Adachi K. A parallel circuit of LIF signaling pathways maintains pluripotency of mouse ES cells. Nature 2009, 460:118-122.
24. Potier E., Noailly J., Ito K. Directing bone marrow-derived stromal cell function with mechanics. J. Biomech. 2010, 43:807-817.
25. Park J.S., Chu J.S., Cheng C., Chen F., Chen D., Li S. Differential effects of equiaxial and uniaxial strain on mesenchymal stem cells. Biotechnol. Bioeng. 2004, 88:359-368.
26. Pan G., Thomson J.A. Nanog and transcriptional networks in embryonic stem cell pluripotency. Cell Res. 2007, 17:42-49.
27. Hornberger T.A., Armstrong D.D., Koh T.J., Burkholder T.J., Esser K.A. Intracellular signaling specificity in response to uniaxial vs. multiaxial stretch: implications for mechanotransduction. Am. J. Physiol. Cell Physiol. 2005, 288:C185-C194.
28. Kippenberger S., Loitsch S., Guschel M., Müller J., Knies Y., Kaufmann R., Bernd A. Mechanical stretch stimulates protein kinase B/Akt phosphorylation in epidermal cells via angiotensin II type 1 receptor and epidermal growth factor receptor. J. Biol. Chem. 2005, 280:3060-3067.
29. Sakamoto K., Aschenbach W.G., Hirshman M.F., Goodyear L.J. Akt signaling in skeletal muscle: regulation by exercise and passive stretch. Am. J. Physiol. Endcrinol. Metab. 2003, 285:E1081-E1088.
30. Sasai N., Agata N., Inoue-Miyazu M., Kawakami K., Kobayashi K., Sokabe M., Hayakawa K. Involvement of PI3K/Akt/TOR pathway in stretch-induced hypertrophy of myotubes. Muscle Nerve 2010, 41:100-106.
31. 2+ release via activation of phosphatidylinositol 3-kinase-Akt pathway in smooth muscle. PLoS One 2008, 25:e2526.
32. Pan J., Fukuda K., Saito M., Matsuzaki J., Kodama H., Sano M., Takahashi T., Kato T., Ogawa S. Mechanical stretch activates the JAK/STAT pathway in rat cardiomyocytes. Circ. Res. 1999, 84:1127-1136.
33. Flusberg D.A., Numaguchi Y., Ingber D.E. Cooperative control of Akt phosphorylation, bcl-2 expression, and apoptosis by cytoskeletal microfilaments and microtubules in capillary endothelial cells. Mol. Biol. Cell 2001, 12:3087-3094.
34. Park E.H., Kang S.S., Lee Y.S., Kim E.J., Tak E.N., Sonn J.K. Integrity of the cortical actin ring is required for activation of the PI3K/Akt and p38 MAPK signaling pathways in redifferentiation of chondrocytes on chitosan. Cell Biol. Int. 2008, 32:1272-1278.
35. Peyrollier K., Hajduch E., Gray A., Litherland G.J., Prescott A.R., Leslie N.R., Hundal H.S. A role for the actin cytoskeleton in the hormonal and growth-factor-mediated activation of protein kinase B. Int. J. Biochem. Mol. Biol. 2000, 352:617-622.
36. Wang H.B., Dembo M., Hanks S.K., Wang Y. Focal adhesion kinase is involved in mechanosensing during fibroblast migration. Proc. Natl. Acad. Sci. USA 2001, 98:11295-11300.