Cell geometric constraints induce modular gene-expression patterns via redistribution of HDAC3 regulated by actomyosin contractility

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 28, 2013, Pages 11349-11354

  Jain, Nikhil ^a,b   Iyer, K Venkatesan ^a   Kumar, Abhishek ^a   Shivashankar, G V ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Cell matrix interaction; Chromatin remodelling; MRTF A signaling; Substrate geometry; Transcription control

Indexed keywords

HISTONE; HISTONE DEACETYLASE 3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MYOCARDIN; MYOSIN ADENOSINE TRIPHOSPHATASE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL SHAPE; CELL SIZE; CELL STRUCTURE; CONTROLLED STUDY; DIFFUSION; ENZYME ACTIVITY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GEOMETRY; HISTONE ACETYLATION; HOMEOSTASIS; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SERUM RESPONSIVE ELEMENT; UPREGULATION;

CELL MATRIX INTERACTION; CHROMATIN REMODELLING; MRTF-A SIGNALING; SUBSTRATE GEOMETRY; TRANSCRIPTION CONTROL;

3T3 CELLS; ACETYLATION; ACTOMYOSIN; ANIMALS; GENE EXPRESSION REGULATION; HISTONE DEACETYLASES; HISTONES; MICE; TRANSCRIPTION, GENETIC;

EID: 84879936773     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1300801110     Document Type: Article

References (43)

1. Jean RP, Gray DS, Spector AA, Chen CS (2004) Characterization of the nuclear deformation caused by changes in endothelial cell shape. J Biomech Eng 126(5):552-558. (Pubitemid 40019142)
2. Versaevel M, Grevesse T, Gabriele S (2012) Spatial coordination between cell and nuclear shape within micropatterned endothelial cells. Nat Commun 3:671.
3. Théry M, Pépin A, Dressaire E, Chen Y, Bornens M (2006) Cell distribution of stress fibres in response to the geometry of the adhesive environment. Cell Motil Cytoskeleton 63(6):341-355. (Pubitemid 43787719)
4. Le Beyec J, et al. (2007) Cell shape regulates global histone acetylation in human mammary epithelial cells. Exp Cell Res 313(14):3066-3075. (Pubitemid 47125878)
5. Vergani L, Grattarola M, Nicolini C (2004) Modifications of chromatin structure and gene expression following induced alterations of cellular shape. Int J Biochem Cell Biol 36(8):1447-1461. (Pubitemid 38625825)
6. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE (1997) Geometric control of cell life and death. Science 276(5317):1425-1428. (Pubitemid 27235413)
7. Théry M, Bornens M (2006) Cell shape and cell division. Curr Opin Cell Biol 18(6):648-657. (Pubitemid 44692475)
8. Li Y, et al. (2011) Biophysical regulation of histone acetylation in mesenchymal stem cells. Biophys J 100(8):1902-1909.
9. Dekker RJ, et al. (2002) Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Krüppel-like factor (KLF2). Blood 100(5):1689-1698. (Pubitemid 34925146)
10. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126(4):677-689. (Pubitemid 44233625)
11. McNamara LE, et al. (2012) The role of microtopography in cellular mechanotransduction. Biomaterials 33(10):2835-2847.
12. Cheung P, Allis CD, Sassone-Corsi P (2000) Signaling to chromatin through histone modifications. Cell 103(2):263-271.
13. Nightingale KP, Wellinger RE, Sogo JM, Becker PB (1998) Histone acetylation facilitates RNA polymerase II transcription of the Drosophila hsp26 gene in chromatin. EMBO J 17(10):2865-2876. (Pubitemid 28227133)
14. Birbach A, et al. (2002) Signaling molecules of the NF-kappa B pathway shuttle constitutively between cytoplasm and nucleus. J Biol Chem 277(13):10842-10851. (Pubitemid 34952838)
15. Meyer T, Vinkemeier U (2004) Nucleocytoplasmic shuttling of STAT transcription factors. Eur J Biochem 271(23-24):4606-4612. (Pubitemid 40065563)
16. Miralles F, Posern G, Zaromytidou AI, Treisman R (2003) Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 113(3):329-342. (Pubitemid 36556115)
17. Dupont S, et al. (2011) Role of YAP/TAZ in mechanotransduction. Nature 474(7350):179-183.
18. McGee KM, Vartiainen MK, Khaw PT, Treisman R, Bailly M (2011) Nuclear transport of the serum response factor coactivator MRTF-A is downregulated at tensional homeostasis. EMBO Rep 12(9):963-970.
19. Connelly JT, et al. (2010) Actin and serum response factor transduce physical cues from the microenvironment to regulate epidermal stem cell fate decisions. Nat Cell Biol 12(7):711-718.
20. Kilian KA, Bugarija B, Lahn BT, Mrksich M (2010) Geometric cues for directing the differentiation of mesenchymal stem cells. Proc Natl Acad Sci USA 107(11):4872-4877.
21. Selvaraj A, Prywes R (2004) Expression profiling of serum inducible genes identifies a subset of SRF target genes that are MKL dependent. BMC Mol Biol 5:13.
22. Posern G, Miralles F, Guettler S, Treisman R (2004) Mutant actins that stabilise F-actin use distinct mechanisms to activate the SRF coactivator MAL. EMBO J 23(20):3973-3983. (Pubitemid 39472419)
23. Posern G, Sotiropoulos A, Treisman R (2002) Mutant actins demonstrate a role for unpolymerized actin in control of transcription by serum response factor. Mol Biol Cell 13(12):4167-4178. (Pubitemid 35471176)
24. Roca-Cusachs P, et al. (2008) Micropatterning of single endothelial cell shape reveals a tight coupling between nuclear volume in G1 and proliferation. Biophys J 94(12):4984-4995.
25. Rao J, Bhattacharya D, Banerjee B, Sarin A, Shivashankar GV (2007) Trichostatin-A induces differential changes in histone protein dynamics and expression in HeLa cells. Biochem Biophys Res Commun 363(2):263-268. (Pubitemid 47484325)
26. Mazumder A, Shivashankar GV (2010) Emergence of a prestressed eukaryotic nucleus during cellular differentiation and development. J R Soc Interface 7(Suppl 3):S321-S330.
27. Mascetti G, Carrara S, Vergani L (2001) Relationship between chromatin compactness and dye uptake for in situ chromatin stained with DAPI. Cytometry 44(2):113-119.
28. Bhaskara S, et al. (2008) Deletion of histone deacetylase 3 reveals critical roles in S phase progression and DNA damage control. Mol Cell 30(1):61-72. (Pubitemid 351470157)
29. Bhaskara S, et al. (2010) Hdac3 is essential for the maintenance of chromatin structure and genome stability. Cancer Cell 18(5):436-447.
30. Gao Z, He Q, Peng B, Chiao PJ, Ye J (2006) Regulation of nuclear translocation of HDAC3 by IkappaBalpha is required for tumor necrosis factor inhibition of peroxisome proliferator-activated receptor gamma function. J Biol Chem 281(7):4540-4547. (Pubitemid 43847886)
31. Cai S, et al. (1998) Regulation of cytoskeletal mechanics and cell growth by myosin light chain phosphorylation. Am J Physiol 275(5 Pt 1):C1349-C1356.
32. Bhadriraju K, Elliott JT, Nguyen M, Plant AL (2007) Quantifying myosin light chain phosphorylation in single adherent cells with automated fluorescence microscopy. BMC Cell Biol 8:43.
33. Tang RH, et al. (2008) Myocardin inhibits cellular proliferation by inhibiting NF-kappaB (p65)-dependent cell cycle progression. Proc Natl Acad Sci USA 105(9):3362-3367.
34. Khatau SB, et al. (2009) A perinuclear actin cap regulates nuclear shape. Proc Natl Acad Sci USA 106(45):19017-19022.
35. Thomas CH, Collier JH, Sfeir CS, Healy KE (2002) Engineering gene expression and protein synthesis by modulation of nuclear shape. Proc Natl Acad Sci USA 99(4):1972-1977. (Pubitemid 34168999)
36. Webster M, Witkin KL, Cohen-Fix O (2009) Sizing up the nucleus: Nuclear shape, size and nuclear-envelope assembly. J Cell Sci 122(Pt 10):1477-1486.
37. Shivashankar GV (2010) Nuclear mechanics and genome regulation. Methods Cell Biol 98:xiii.
38. Shivashankar GV (2011) Mechanosignaling to the cell nucleus and gene regulation. Annu Rev Biophys 40:361-378.
39. Bui HT, et al. (2010) Effect of trichostatin A on chromatin remodeling, histone modifications, DNA replication, and transcriptional activity in cloned mouse embryos. Biol Reprod 83(3):454-463.
40. Sato S, Burgess SB, McIlwain DL (1994) Transcription and motoneuron size. J Neurochem 63(5):1609-1615. (Pubitemid 24326201)
41. Schmidt EE, Schibler U (1995) Cell size regulation, a mechanism that controls cellular RNA accumulation: Consequences on regulation of the ubiquitous transcription factors Oct1 and NF-Y and the liver-enriched transcription factor DBP. J Cell Biol 128(4):467-483.
42. Chrzanowska-Wodnicka M, Burridge K (1996) Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J Cell Biol 133(6):1403-1415. (Pubitemid 26192339)
43. Olson EN, Nordheim A (2010) Linking actin dynamics and gene transcription to drive cellular motile functions. Nat Rev Mol Cell Biol 11(5):353-365.