Biophysical regulation of chromatin architecture instills a mechanical memory in mesenchymal stem cells

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Heo, Su Jin ^a,b   Thorpe, Stephen D ^c   Driscoll, Tristan P ^a,b,d   Duncan, Randall L ^e   Lee, David A ^c   Mauck, Robert L ^a,b,d  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

^e UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM; CHROMATIN; HISTONE LYSINE METHYLTRANSFERASE; MYOSIN ADENOSINE TRIPHOSPHATASE;

ANIMAL; BIOMECHANICS; BOVINE; CALCIUM SIGNALING; CELL LINEAGE; CELL NUCLEUS; CHEMISTRY; CHROMATIN; CYTOLOGY; CYTOSKELETON; GENE EXPRESSION REGULATION; GENETICS; MECHANICAL STRESS; MECHANOTRANSDUCTION; MESENCHYMAL STROMA CELL; METABOLISM; SECRETION (PROCESS); STIFLE; ULTRASTRUCTURE;

ACTOMYOSIN; ADENOSINE TRIPHOSPHATE; ANIMALS; BIOMECHANICAL PHENOMENA; CALCIUM; CALCIUM SIGNALING; CATTLE; CELL LINEAGE; CELL NUCLEUS; CHROMATIN; CYTOSKELETON; GENE EXPRESSION REGULATION; HISTONE-LYSINE N-METHYLTRANSFERASE; MECHANOTRANSDUCTION, CELLULAR; MESENCHYMAL STROMAL CELLS; STIFLE; STRESS, MECHANICAL;

EID: 84947904482     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep16895     Document Type: Article

References (54)

1. Bianco, P., et al. The meaning, the sense and the significance: translating the science of mesenchymal stem cells into medicine. Nat Med. 19, 35-42 (2013
2. Pittenger, M. F., et al. Multilineage potential of adult human mesenchymal stem cells. Science. 284, 143-147 (1999
3. Engler, A. J., Sen, S., Sweeney, H. L., & Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell. 126, 677-689 (2006
4. Downing, T. L., et al. Biophysical regulation of epigenetic state and cell reprogramming. Nat Mater. 12, 1154-1162 (2013
5. Baker, B. M., Shah, R. P., Huang, A. H., & Mauck, R. L. Dynamic tensile loading improves the functional properties of mesenchymal stem cell-laden nanofiber-based fibrocartilage. Tissue Eng Part A. 17, 1445-1455 (2011
6. Huang, A. H., Baker, B. M., Ateshian, G. A., & Mauck, R. L. Sliding contact loading enhances the tensile properties of mesenchymal stem cell-seeded hydrogels. Eur Cell Mater. 24, 29-45 (2012
7. Arnsdorf, E. J., Tummala, P., Kwon, R. Y., & Jacobs, C. R. Mechanically induced osteogenic differentiation-The role of RhoA, ROCKII and cytoskeletal dynamics. J Cell Sci. 122, 546-553 (2009
8. Deguchi, S., Maeda, K., Ohashi, T., & Sato, M. Flow-induced hardening of endothelial nucleus as an intracellular stress-bearing organelle. J Biomech. 38, 1751-1759 (2005
9. Iyer, K. V., Pulford, S., Mogilner, A., & Shivashankar, G. V. Mechanical activation of cells induces chromatin remodeling preceding MKL nuclear transport. Biophys J. 103, 1416-1428 (2012
10. Provenzano, P. P., & Keely, P. J. Mechanical signaling through the cytoskeleton regulates cell proliferation by coordinated focal adhesion and Rho GTPase signaling. J Cell Sci. 124, 1195-1205 (2011
11. Driscoll, T. P., Cosgrove, B. D., Heo, S. J., Shurden, Z. E., & Mauck, R. L. Cytoskeletal to Nuclear Strain Transfer Regulates YAP Signaling in Mesenchymal Stem Cells. Biophys J. 108, 2783-2793 (2015
12. Kutscheidt, S., et al. FHOD1 interaction with nesprin-2G mediates TAN line formation and nuclear movement. Nat Cell Biol. 16, 708-715 (2014
13. Constantinescu, D., Gray, H. L., Sammak, P. J., Schatten, G. P., & Csoka, A. B. Lamin A/C expression is a marker of mouse and human embryonic stem cell differentiation. Stem Cells. 24, 177-185 (2006
14. Pajerowski, J. D., Dahl, K. N., Zhong, F. L., Sammak, P. J., & Discher, D. E. Physical plasticity of the nucleus in stem cell differentiation. Proc Natl Acad Sci USA. 104, 15619-15624 (2007
15. Swift, J., et al. Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science. 341, 1240104 (2013
16. Arnsdorf, E. J., Tummala, P., Castillo, A. B., Zhang, F., & Jacobs, C. R. The epigenetic mechanism of mechanically induced osteogenic differentiation. J Biomech. 43, 2881-2886 (2010
17. Fullgrabe, J., Hajji, N., & Joseph, B. Cracking the death code: apoptosis-related histone modifications. Cell Death Differ. 17, 1238-1243 (2010
18. Zullo, J. M., et al. DNA sequence-dependent compartmentalization and silencing of chromatin at the nuclear lamina. Cell. 149, 1474-1487 (2012
19. Gaspar-Maia, A., Alajem, A., Meshorer, E., & Ramalho-Santos, M. Open chromatin in pluripotency and reprogramming. Nat Rev Mol Cell Biol. 12, 36-47 (2011
20. Schneider, R., & Grosschedl, R. Dynamics and interplay of nuclear architecture, genome organization, and gene expression. Genes Dev. 21, 3027-3043 (2007
21. Bannister, A. J., & Kouzarides, T. Regulation of chromatin by histone modifications. Cell Res. 21, 381-395 (2011
22. Wang, N., Tytell, J. D., & Ingber, D. E. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol. 10, 75-82 (2009
23. Guilluy, C., et al. Isolated nuclei adapt to force and reveal a mechanotransduction pathway in the nucleus. Nat Cell Biol. 16, 376-381 (2014
24. Campbell, J. J., Bader, D. L., & Lee, D. A. Mechanical loading modulates intracellular calcium signaling in human mesenchymal stem cells. J Appl Biomater Biomech. 6, 9-15 (2008
25. Gardinier, J., et al. P2Y2 receptors regulate osteoblast mechanosensitivity during fluid flow. Am J Physiol Cell Physiol. 306, C1058-1067 (2014
26. Gardinier, J. D., Majumdar, S., Duncan, R. L., & Wang, L. Cyclic Hydraulic Pressure and Fluid Flow Differentially Modulate Cytoskeleton Re-Organization in MC3T3 Osteoblasts. Cell Mol Bioeng. 2, 133-143 (2009
27. Genetos, D. C., Geist, D. J., Liu, D., Donahue, H. J., & Duncan, R. L. Fluid shear-induced ATP secretion mediates prostaglandin release in MC3T3-E1 osteoblasts. J Bone Miner Res. 20, 41-49 (2005
28. Balestrini, J. L., Chaudhry, S., Sarrazy, V., Koehler, A., & Hinz, B. The mechanical memory of lung myofibroblasts. Integr Biol (Camb) 4, 410-421 (2012
29. Yang, C., Tibbitt, M. W., Basta, L., & Anseth, K. S. Mechanical memory and dosing influence stem cell fate. Nat Mater. 13, 645-652 (2014
30. Irianto, J., et al. Osmotic challenge drives rapid and reversible chromatin condensation in chondrocytes. Biophys J. 104, 759-769 (2013
31. Hemming, S., et al. EZH2 and KDM6A act as an epigenetic switch to regulate mesenchymal stem cell lineage specification. Stem Cells. 32, 802-815 (2014
32. Verma, S. K., et Al. Identification of Potent, Selective, Cell-Active Inhibitors of the Histone Lysine Methyltransferase EZH2. ACS Med Chem Lett. 3, 1091-1096 (2012
33. Dupont, S., et al. Role of YAP/TAZ in mechanotransduction. Nature. 474, 179-183 (2011
34. Azorin, N., et al. ATP signalling is crucial for the response of human keratinocytes to mechanical stimulation by hypo-osmotic shock. Exp Dermatol. 20, 401-407 (2011
35. Jain, N., Iyer, K. V., Kumar, A., & Shivashankar, G. V. Cell geometric constraints induce modular gene-expression patterns via redistribution of HDAC3 regulated by actomyosin contractility. Proc Natl Acad Sci USA. 110, 11349-11354 (2013
36. Poh, Y. C., et al. Dynamic force-induced direct dissociation of protein complexes in a nuclear body in living cells. Nat Commun. 3, 866 (2012
37. Gavara, N., Roca-Cusachs, P., Sunyer, R., Farre, R., & Navajas, D. Mapping cell-matrix stresses during stretch reveals inelastic reorganization of the cytoskeleton. Biophys J. 95, 464-471 (2008
38. Vignali, M., Hassan, A. H., Neely, K. E., & Workman, J. L. ATP-dependent chromatin-remodeling complexes. Mol Cell Biol. 20, 1899-1910 (2000
39. Bertrand, A. T., et al. Cellular microenvironments reveal defective mechanosensing responses and elevated YAP signaling in LMNA-mutated muscle precursors. J Cell Sci. 127, 2873-2884 (2014
40. Yu, F. X., et al. Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell. 150, 780-791 (2012
41. Coste, B., et al. Piezo proteins are pore-forming subunits of mechanically activated channels. Nature. 483, 176-181 (2012
42. Lee, W., et al. Synergy between Piezo1 and Piezo2 channels confers high-strain mechanosensitivity to articular cartilage. Proc Natl Acad Sci USA. 111, E5114-5122 (2014
43. Mauck, R. L., Yuan, X., & Tuan, R. S. Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-Term agarose culture. Osteoarthritis Cartilage. 14, 179-189 (2006
44. Chalut, K. J., et al. Chromatin decondensation and nuclear softening accompany Nanog downregulation in embryonic stem cells. Biophys J. 103, 2060-2070 (2012
45. Solon, J., Levental, I., Sengupta, K., Georges, P. C., & Janmey, P. A. Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys J. 93, 4453-4461 (2007
46. Garcia, M., & Knight, M. M. Cyclic loading opens hemichannels to release ATP as part of a chondrocyte mechanotransduction pathway. J Orthop Res. 28, 510-515 (2010
47. Han, W. M., et al. Impact of cellular microenvironment and mechanical perturbation on calcium signalling in meniscus fibrochondrocytes. Eur Cell Mater. 27, 321-331 (2014
48. Reiter, B., et al. TRPV4-mediated regulation of epithelial permeability. FASEB J. 20, 1802-1812 (2006
49. O'Conor, C. J., Leddy, H. A., Benefield, H. C., Liedtke, W. B., & Guilak, F. TRPV4-mediated mechanotransduction regulates the metabolic response of chondrocytes to dynamic loading. Proc Natl Acad Sci USA. 111, 1316-1321 (2014
50. Pingguan-Murphy, B., El-Azzeh, M., Bader, D. L., & Knight, M. M. Cyclic compression of chondrocytes modulates a purinergic calcium signalling pathway in a strain rate- And frequency-dependent manner. J Cell Physiol. 209, 389-397 (2006
51. Houtman, R., et al. Attenuation of very late antigen-5-mediated adhesion of bone marrow-derived mast cells to fibronectin by peptides with inverted hydropathy to EF-hands. J Immunol. 166, 861-867 (2001
52. Bae, C., Sachs, F., & Gottlieb, P. A. The mechanosensitive ion channel Piezo1 is inhibited by the peptide GsMTx4. Biochemistry. 50, 6295-6300 (2011
53. Gooch, J. L., Tang, Y., Ricono, J. M., & Abboud, H. E. Insulin-like growth factor-I induces renal cell hypertrophy via a calcineurindependent mechanism. J Biol Chem. 276, 42492-42500 (2001
54. Cui, Z. J., Hidaka, H., & Dannies, P. S. KN-62, a calcium/calmodulin-dependent protein kinase II inhibitor, inhibits high potassium-stimulated prolactin secretion and intracellular calcium increases in anterior pituitary cells. Biochim Biophys Acta. 1310, 343-347 (1996