Mechanical activation of mammalian target of rapamycin pathway is required for cartilage development

FASEB Journal

Volumn 28, Issue 10, 2014, Pages 4470-4481

  Guan, Yingjie ^a   Yang, Xu ^a,b   Yang, Wentian ^a   Charbonneau, Cherie ^a   Chen, Qian ^a  

^a BROWN UNIVERSITY   (United States)

^b QINGDAO UNIVERSITY   (China)

Author keywords

Chondrocyte; Mechanotransduction; MTOR; Shp2

Indexed keywords

COLLAGEN; GROWTH FACTOR; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN TYROSINE PHOSPHATASE SHP 2; SONIC HEDGEHOG PROTEIN; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CARTILAGE; CARTILAGE CELL; CELL GROWTH; CELL MATURATION; CELL PROLIFERATION; CHICKEN; CHONDROGENESIS; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; GROWTH PLATE; MECHANICAL STIMULATION; MECHANOTRANSDUCTION; MUSCLE CONTRACTION; NONHUMAN; TISSUE GROWTH; ANIMAL; CHICK EMBRYO; CYTOLOGY; EMBRYOLOGY; GENETICS; MECHANICAL STRESS; METABOLISM; PHYSIOLOGY;

ANIMALS; CARTILAGE; CELL PROLIFERATION; CHICK EMBRYO; CHONDROCYTES; CHONDROGENESIS; HEDGEHOG PROTEINS; MECHANOTRANSDUCTION, CELLULAR; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11; STRESS, MECHANICAL; TOR SERINE-THREONINE KINASES;

EID: 84907707647     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-252783     Document Type: Article

References (51)

1. Kim, Y. J., Sah, R. L., Grodzinsky, A. J., Plaas, A. H., and Sandy, J. D. (1994) Mechanical regulation of cartilage biosynthetic behavior: physical stimuli. Arch. Biochem. Biophys. 311, 1-12
2. Carter, D. R., Orr, T. E., Fyhrie, D. P., and Schurman, D. J. (1987) Influences of mechanical stress on prenatal and postnatal skeletal development. Clin. Orthop. Relat. Res. 237-250
3. Schneiderman, R., Keret, D., and Maroudas, A. (1986) Effects of mechanical and osmotic pressure on the rate of glycosaminoglycan synthesis in the human adult femoral head cartilage: an in vitro study. J. Orthop. Res. 4, 393-408
4. Sibonga, J. D., Zhang, M., Evans, G. L., Westerlind, K. C., Cavolina, J. M., Morey-Holton, E., and Turner, R. T. (2000) Effects of spaceflight and simulated weightlessness on longitudinal bone growth. Bone 27, 535-540
5. Wong, M., Siegrist, M., and Goodwin, K. (2003) Cyclic tensile strain and cyclic hydrostatic pressure differentially regulate expression of hypertrophic markers in primary chondrocytes. Bone 33, 685-693
6. Wu, Q. Q., and Chen, Q. (2000) Mechanoregulation of chondrocyte proliferation, maturation, and hypertrophy: ion-channel dependent transduction of matrix deformation signals. Exp. Cell Res. 256, 383-391
7. Ueki, M., Tanaka, N., Tanimoto, K., Nishio, C., Honda, K., Lin, Y. Y., Tanne, Y., Ohkuma, S., Kamiya, T., Tanaka, E., and Tanne, K. (2008) The effect of mechanical loading on the metabolism of growth plate chondrocytes. Ann. Biomed. Eng. 36, 793-800
8. Alvarez-Garcia, O., Carbajo-Perez, E., Garcia, E., Gil, H., Molinos, I., Rodriguez, J., Ordonez, F. A., and Santos, F. (2007) Rapamycin retards growth and causes marked alterations in the growth plate of young rats. Pediatr. Nephrol. 22, 954-961
9. Ramage, L., Nuki, G., and Salter, D. M. (2009) Signalling cascades in mechanotransduction: cell-matrix interactions and mechanical loading. Scand. J. Med. Sci. Sports 19, 457-469
10. Wu, Q., Zhang, Y., and Chen, Q. (2001) Indian hedgehog is an essential component of mechanotransduction complex to stimulate chondrocyte proliferation. J. Biol. Chem. 276, 35290-35296
11. Nowlan, N. C., Prendergast, P. J., and Murphy, P. (2008) Identification of mechanosensitive genes during embryonic bone formation. PLoS Comput. Biol. 4, e1000250
12. Wullschleger, S., Loewith, R., and Hall, M. N. (2006) TOR signaling in growth and metabolism. Cell 124, 471-484
13. Yang, Q., and Guan, K. L. (2007) Expanding mTOR signaling. Cell Res. 17, 666-681
14. Loewith, R., Jacinto, E., Wullschleger, S., Lorberg, A., Crespo, J. L., Bonenfant, D., Oppliger, W., Jenoe, P., and Hall, M. N. (2002) Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol. Cell 10, 457-468
15. Sarbassov, D. D., Ali, S. M., Kim, D. H., Guertin, D. A., Latek, R. R., Erdjument-Bromage, H., Tempst, P., and Sabatini, D. M. (2004) Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr. Biol. 14, 1296-1302
16. Sparks, C. A., and Guertin, D. A. Targeting mTOR: prospects for mTOR complex 2 inhibitors in cancer therapy. Oncogene 29, 3733-3744
17. Soulard, A., Cohen, A., and Hall, M. N. (2009) TOR signaling in invertebrates. Curr. Opin. Cell Biol. 21, 825-836
18. Phornphutkul, C., Lee, M., Voigt, C., Wu, K. Y., Ehrlich, M. G., Gruppuso, P. A., and Chen, Q. (2009) The effect of rapamycin on bone growth in rabbits. J. Orthop. Res. 27, 1157-1161
19. Holstein, J. H., Klein, M., Garcia, P., Histing, T., Culemann, U., Pizanis, A., Laschke, M. W., Scheuer, C., Meier, C., Schorr, H., Pohlemann, T., and Menger, M. D. (2008) Rapamycin affects early fracture healing in mice. Br. J. Pharmacol. 154, 1055-1062
20. Zito, C. I., Qin, H., Blenis, J., and Bennett, A. M. (2007) SHP-2 regulates cell growth by controlling the mTOR/S6 kinase 1 pathway. J. Biol. Chem. 282, 6946-6953
21. Dance, M., Montagner, A., Salles, J. P., Yart, A., and Raynal, P. (2008) The molecular functions of Shp2 in the Ras/Mitogenactivated protein kinase (ERK1/2) pathway. Cell. Signal. 20, 453-459
22. Yang, W., Wang, J., Moore, D. C., Liang, H., Dooner, M., Wu, Q., Terek, R., Chen, Q., Ehrlich, M. G., Quesenberry, P. J., and Neel, B. G. (2013) Ptpn11 deletion in a novel progenitor causes metachondromatosis by inducing hedgehog signalling. Nature 499, 491-495
23. Guan, Y. J., Yang, X., Wei, L., and Chen, Q. (2011) MiR-365: a mechanosensitive microRNA stimulates chondrocyte differentiation through targeting histone deacetylase 4. FASEB J. 25, 4457-4466
24. Chen, Q., Johnson, D. M., Haudenschild, D. R., and Goetinck, P. F. (1995) Progression and recapitulation of the chondrocyte differentiation program: cartilage matrix protein is a marker for cartilage maturation. Dev. Biol. 172, 293-306
25. Phornphutkul, C., Wu, K. Y., Auyeung, V., Chen, Q., and Gruppuso, P. A. (2008) mTOR signaling contributes to chondrocyte differentiation. Dev. Dyn. 237, 702-712
26. Stuermer, A., Hoehn, K., Faul, T., Auth, T., Brand, N., Kneissl, M., Putter, V., and Grummt, F. (2007) Mouse pre-replicative complex proteins colocalise and interact with the centrosome. Eur. J. Cell Biol. 86, 37-50
27. Spankuch, B., Heim, S., Kurunci-Csacsko, E., Lindenau, C., Yuan, J., Kaufmann, M., and Strebhardt, K. (2006) Downregulation of Polo-like kinase 1 elevates drug sensitivity of breast cancer cells in vitro and in vivo. Cancer Res. 66, 5836-5846
28. Robling, A. G. (2009) Is bone's response to mechanical signals dominated by muscle forces? Med. Sci. Sports Exerc. 41, 2044-2049
29. Forwood, M. R. (2001) Mechanical effects on the skeleton: are there clinical implications? Osteoporos. Int. 12, 77-83
30. Ji, B., Jiang, G., Fu, J., Long, J., and Wang, H. (2010) Why high frequency of distraction improved the bone formation in distraction osteogenesis? Med. Hypotheses 74, 871-873
31. Moore, D. C., Leblanc, C. W., Muller, R., Crisco, J. J., 3rd, and Ehrlich, M. G. (2003) Physiologic weight-bearing increases new vessel formation during distraction osteogenesis: a micro-tomographic imaging study. J. Orthop. Res. 21, 489-496
32. Dane, B., Dane, C., Aksoy, F., Cetin, A., and Yayla, M. (2009) Arthrogryposis multiplex congenita: analysis of twelve cases. Clin. Exp. Obstet. Gynecol. 36, 259-262
33. Hall, B. K., and Herring, S. W. (1990) Paralysis and growth of the musculoskeletal system in the embryonic chick. J. Morphol. 206, 45-56
34. Sengupta, S., Peterson, T. R., and Sabatini, D. M. (2010) Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol. Cell 40, 310-322
35. Godin, L. M., Suzuki, S., Jacobs, C. R., Donahue, H. J., and Donahue, S. W. (2007) Mechanically induced intracellular calcium waves in osteoblasts demonstrate calcium fingerprints in bone cell mechanotransduction. Biomech. Model Mechanobiol. 6, 391-398
36. Donahue, S. W., Jacobs, C. R., and Donahue, H. J. (2001) Flow-induced calcium oscillations in rat osteoblasts are age, loading frequency, and shear stress dependent. Am. J. Physiol. Cell Physiol. 281, C1635-C1641
37. You, J., Yellowley, C. E., Donahue, H. J., Zhang, Y., Chen, Q., and Jacobs, C. R. (2000) Substrate deformation levels associated with routine physical activity are less stimulatory to bone cells relative to loading-induced oscillatory fluid flow. J. Biomech. Eng. 122, 387-393
38. Lee, D. Y., Li, Y. S., Chang, S. F., Zhou, J., Ho, H. M., Chiu, J. J., and Chien, S. (2010) Oscillatory flow-induced proliferation of osteoblast-like cells is mediated by alphavbeta3 and beta1 integrins through synergistic interactions of focal adhesion kinase and Shc with phosphatidylinositol 3-kinase and the Akt/ mTOR/p70S6K pathway. J. Biol. Chem. 285, 30-42
39. Kanbe, K., Yang, X., Wei, L., Sun, C., and Chen, Q. (2007) Pericellular matrilins regulate activation of chondrocytes by cyclic load-induced matrix deformation. J. Bone Miner. Res. 22, 318-328
40. Pitsillides, A. A. (2006) Early effects of embryonic movement: 'a shot out of the dark.' J. Anat. 208, 417-431
41. Germiller, J. A., and Goldstein, S. A. (1997) Structure and function of embryonic growth plate in the absence of functioning skeletal muscle. J. Orthop. Res. 15, 362-370
42. Lamb, K. J., Lewthwaite, J. C., Lin, J. P., Simon, D., Kavanagh, E., Wheeler-Jones, C. P., and Pitsillides, A. A. (2003) Diverse range of fixed positional deformities and bone growth restraint provoked by flaccid paralysis in embryonic chicks. Int. J. Exp. Pathol. 84, 191-199
43. Provine, R. R. (1980) Development of between-limb movement synchronization in the chick embryo. Dev. Psychobiol. 13, 151-163
44. Mackie, E. J., Tatarczuch, L., and Mirams, M. (2011) The skeleton: a multi-functional complex organ: the growth plate chondrocyte and endochondral ossification. J. Endocrinol. 211, 109-121
45. Pines, M., and Hurwitz, S. (1991) The role of the growth plate in longitudinal bone growth. Poult. Sci. 70, 1806-1814
46. Villemure, I., and Stokes, I. A. (2009) Growth plate mechanics and mechanobiology: a survey of present understanding. J. Biomech. 42, 1793-1803
47. Studer, D., Millan, C., Ozturk, E., Maniura-Weber, K., and Zenobi-Wong, M. (2012) Molecular and biophysical mechanisms regulating hypertrophic differentiation in chondrocytes and mesenchymal stem cells. Eur. Cell Mater. 24, 118-135; discussion, 135
48. Forriol, F., and Shapiro, F. (2005) Bone development: interaction of molecular components and biophysical forces. Clin Orthop. Relat. Res. 14-33
49. Duke, P. J., and Montufar-Solis, D. (1999) Exposure to altered gravity affects all stages of endochondral cartilage differentiation. Adv. Space Res. 24, 821-827
50. Henderson, J. H., and Carter, D. R. (2002) Mechanical induction in limb morphogenesis: the role of growth-generated strains and pressures. Bone 31, 645-653
51. Krejci, P., Masri, B., Salazar, L., Farrington-Rock, C., Prats, H., Thompson, L. M., and Wilcox, W. R. (2007) Bisindolylmaleimide I suppresses fibroblast growth factor-mediated activation of Erk MAP kinase in chondrocytes by preventing Shp2 association with the Frs2 and Gab1 adaptor proteins. J. Biol. Chem. 282, 2929-2936