Cell geometry dictates TNFα-induced genome response

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

Volumn 114, Issue 20, 2017, Pages E3882-E3891

  Mitra, Aninda ^a,b   Venkatachalapathy, Saradha ^a   Ratna, Prasuna ^a,b   Wang, Yejun ^a   Jokhun, Doorgesh Sharma ^a   Shivashankar, G V ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

Author keywords

Cell geometry; Gene expression; NF B; TNF

Indexed keywords

I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; RNA POLYMERASE II; TUMOR NECROSIS FACTOR; MKL1 PROTEIN, HUMAN; RELA PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR RELA;

ANISOTROPY; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; FIBROBLAST; GENE EXPRESSION; GENOME; GEOMETRY; INTRACELLULAR SIGNALING; NIH 3T3 CELL LINE; PRIORITY JOURNAL; PROTEIN DEGRADATION; ANIMAL; CELL NUCLEUS; CELL SHAPE; CELL SIZE; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; MOUSE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELL NUCLEUS; CELL SHAPE; CELL SIZE; FIBROBLASTS; GENE EXPRESSION; HUMANS; I-KAPPA B PROTEINS; MICE; NIH 3T3 CELLS; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85019841216     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1618007114     Document Type: Article

References (44)

1. Wang N, Tytell JD, Ingber DE (2009) Mechanotransduction at a distance: Mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 10:75-82.
2. Humphrey JD, Dufresne ER, Schwartz MA (2014) Mechanotransduction and extracellular matrix homeostasis. Nat Rev Mol Cell Biol 15:802-812.
3. Jain N, Iyer KV, Kumar A, Shivashankar GV (2013) Cell geometric constraints induce modular gene-expression patterns via redistribution of HDAC3 regulated by actomyosin contractility. Proc Natl Acad Sci USA 110:11349-11354.
4. Dupont S, et al. (2011) Role of YAP/TAZ in mechanotransduction. Nature 474:179-183.
5. Iyer KV, Pulford S, Mogilner A, Shivashankar GV (2012) Mechanical activation of cells induces chromatin remodeling preceding MKL nuclear transport. Biophys J 103:1416-1428.
6. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677-689.
7. Kilian KA, Bugarija B, Lahn BT, Mrksich M (2010) Geometric cues for directing the differentiation of mesenchymal stem cells. Proc Natl Acad Sci USA 107:4872-4877.
8. Desprat N, Supatto W, Pouille PA, Beaurepaire E, Farge E (2008) Tissue deformation modulates twist expression to determine anterior midgut differentiation in Drosophila embryos. Dev Cell 15:470-477.
9. Butcher DT, Alliston T, Weaver VM (2009) A tense situation: Forcing tumour progression. Nat Rev Cancer 9:108-122.
10. Li Q, Kumar A, Makhija E, Shivashankar GV (2014) The regulation of dynamic mechanical coupling between actin cytoskeleton and nucleus by matrix geometry. Biomaterials 35:961-969.
11. Wajant H, Pfizenmaier K, Scheurich P (2003) Tumor necrosis factor signaling. Cell Death Differ 10:45-65.
12. N-meth ZH, et al. (2004) Disruption of the actin cytoskeleton results in nuclear factorkappaB activation and inflammatory mediator production in cultured human intestinal epithelial cells. J Cell Physiol 200:71-81.
13. Goldblum SE, Ding X, Campbell-Washington J (1993) TNF-alpha induces endothelial cell F-actin depolymerization, new actin synthesis, and barrier dysfunction. Am J Physiol 264:C894-C905.
14. Barkett M, Gilmore TD (1999) Control of apoptosis by Rel/NF-kappaB transcription factors. Oncogene 18:6910-6924.
15. Karin M, Lin A (2002) NF-kappaB at the crossroads of life and death. Nat Immunol 3: 221-227.
16. Micheau O, Tschopp J (2003) Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114:181-190.
17. Aggarwal BB (2003) Signalling pathways of the TNF superfamily: A double-edged sword. Nat Rev Immunol 3:745-756.
18. Li YP, Schwartz RJ (2001) TNF-alpha regulates early differentiation of C2C12 myoblasts in an autocrine fashion. FASEB J 15:1413-1415.
19. Sero JE, et al. (2015) Cell shape and the microenvironment regulate nuclear translocation of NF-B in breast epithelial and tumor cells. Mol Syst Biol 11:790.
20. Iskratsch T, Wolfenson H, Sheetz MP (2014) Appreciating force and shape-the rise of mechanotransduction in cell biology. Nat Rev Mol Cell Biol 15:825-833.
21. Shivashankar GV (2010) Nuclear mechanics and genome regulation. Methods Cell Biol 98:xiii.
22. Oeckinghaus A, Ghosh S (2009) The NF-kappaB family of transcription factors and its regulation. Cold Spring Harb Perspect Biol 1:a000034.
23. Sit ST, Manser E (2011) Rho GTPases and their role in organizing the actin cytoskeleton. J Cell Sci 124:679-683.
24. Sumi T, Matsumoto K, Nakamura T (2001) Specific activation of LIM kinase 2 via phosphorylation of threonine 505 by ROCK, a Rho-dependent protein kinase. J Biol Chem 276:670-676.
25. Scott RW, Olson MF (2007) LIM kinases: Function, regulation and association with human disease. J Mol Med (Berl) 85:555-568.
26. Mizuno K (2013) Signaling mechanisms and functional roles of cofilin phosphorylation and dephosphorylation. Cell Signal 25:457-469.
27. Luo W, et al. (2013) Analysis of the local organization and dynamics of cellular actin networks. J Cell Biol 202:1057-1073.
28. Miralles F, Posern G, Zaromytidou AI, Treisman R (2003) Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 113:329-342.
29. Cisse II, et al. (2013) Real-time dynamics of RNA polymerase II clustering in live human cells. Science 341:664-667.
30. Crider BJ, Risinger GM, Jr, Haaksma CJ, Howard EW, Tomasek JJ (2011) Myocardinrelated transcription factors A and B are key regulators of TGF-1-induced fibroblast to myofibroblast differentiation. J Invest Dermatol 131:2378-2385.
31. W-jciak-Stothard B, Entwistle A, Garg R, Ridley AJ (1998) Regulation of TNF-alpha-induced reorganization of the actin cytoskeleton and cell-cell junctions by Rho, Rac, and Cdc42 in human endothelial cells. J Cell Physiol 176:150-165.
32. Esnault C, et al. (2014) Rho-actin signaling to the MRTF coactivators dominates the immediate transcriptional response to serum in fibroblasts. Genes Dev 28:943-958.
33. 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.
34. Gosselin K, Touzet H, Abbadie C (2004) Rel/NF-kappaB target genes. Available at bioinfo.lifl.fr/NF-KB/. Accessed January 19, 2017.
35. Baud V, Karin M (2001) Signal transduction by tumor necrosis factor and its relatives. Trends Cell Biol 11:372-377.
36. Salic A, Mitchison TJ (2008) A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc Natl Acad Sci USA 105:2415-2420.
37. Makhija E, Jokhun DS, Shivashankar GV (2016) Nuclear deformability and telomere dynamics are regulated by cell geometric constraints. Proc Natl Acad Sci USA 113:E32-E40.
38. Mong PY, Petrulio C, Kaufman HL, Wang Q (2008) Activation of Rho kinase by TNFalpha is required for JNK activation in human pulmonary microvascular endothelial cells. J Immunol 180:550-558.
39. Olson EN, Nordheim A (2010) Linking actin dynamics and gene transcription to drive cellular motile functions. Nat Rev Mol Cell Biol 11:353-365.
40. Verrecchia F, Mauviel A (2004) TGF-beta and TNF-alpha: Antagonistic cytokines controlling type I collagen gene expression. Cell Signal 16:873-880.
41. Distler JH, Schett G, Gay S, Distler O (2008) The controversial role of tumor necrosis factor alpha in fibrotic diseases. Arthritis Rheum 58:2228-2235.
42. Tang RH, et al. (2008) Myocardin inhibits cellular proliferation by inhibiting NFkappaB( p65)-dependent cell cycle progression. Proc Natl Acad Sci USA 105:3362-3367.
43. Maharana S, et al. (2016) Chromosome intermingling-the physical basis of chromosome organization in differentiated cells. Nucleic Acids Res 44:5148-5160.
44. Toh KC, Ramdas NM, Shivashankar GV (2015) Actin cytoskeleton differentially alters the dynamics of lamin A, HP1alpha and H2B core histone proteins to remodel chromatin condensation state in living cells. Integr Biol 7:1309-1317.