Mechanical stimulation induces formin-dependent assembly of a perinuclear actin rim

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

Volumn 112, Issue 20, 2015, Pages E2595-E2601

  Shao, Xiaowei ^a   Li, Qingsen ^a   Mogilner, Alex ^b   Bershadsky, Alexander D ^a,c   Shivashankar, G V ^a,d,e  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NEW YORK UNIVERSITY   (United States)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

Author keywords

Calcium; Force; Formin; Mechanotransduction; Perinuclear actin rim

Indexed keywords

ACTIN; CALCIMYCIN; CALCIUM ION; INVERTED FORMIN 2; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; CALCIUM; INF2 PROTEIN, MOUSE;

ACTIN POLYMERIZATION; ARTICLE; CELL NUCLEUS MEMBRANE; CELL STIMULATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FORCE; MECHANICAL STIMULATION; MECHANOTRANSDUCTION; PRIORITY JOURNAL; 3T3 CELL LINE; ACTIN FILAMENT; ANIMAL; ATOMIC FORCE MICROSCOPY; BIOMECHANICS; CELL NUCLEUS; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOBLOTTING; METABOLISM; MOUSE; PHYSICAL STIMULATION; PHYSIOLOGY; ULTRASTRUCTURE;

ACTIN CYTOSKELETON; ANIMALS; BIOMECHANICAL PHENOMENA; CALCIUM; CELL NUCLEUS; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOBLOTTING; MECHANOTRANSDUCTION, CELLULAR; MICE; MICROFILAMENT PROTEINS; MICROSCOPY, ATOMIC FORCE; NIH 3T3 CELLS; PHYSICAL STIMULATION;

EID: 84929493224     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1504837112     Document Type: Article

References (53)

1. Franke RP, et al. (1984) Induction of human vascular endothelial stress fibres by fluid shear stress. Nature 307(5952):648-649.
2. Chen NX, et al. (2000) Ca(2+) regulates fluid shear-induced cytoskeletal reorganization and gene expression in osteoblasts. Am J Physiol Cell Physiol 278(5):C989-C997.
3. Tzima E, et al. (2005) A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437(7057):426-431.
4. Zaidel-Bar R, Kam Z, Geiger B (2005) Polarized downregulation of the paxillin-p130CAS-Rac1 pathway induced by shear flow. J Cell Sci 118(Pt 17):3997-4007.
5. Livne A, Bouchbinder E, Geiger B (2014) Cell reorientation under cyclic stretching. Nat Commun 5:3938.
6. Yoshigi M, Hoffman LM, Jensen CC, Yost HJ, Beckerle MC (2005) Mechanical force mobilizes zyxin from focal adhesions to actin filaments and regulates cytoskeletal reinforcement. J Cell Biol 171(2):209-215.
7. Kaunas R, Nguyen P, Usami S, Chien S (2005) Cooperative effects of Rho and mechanical stretch on stress fiber organization. Proc Natl Acad Sci USA 102(44):15895-15900.
8. Greiner AM, Chen H, Spatz JP, Kemkemer R (2013) Cyclic tensile strain controls cell shape and directs actin stress fiber formation and focal adhesion alignment in spreading cells. PLoS ONE 8(10):e77328.
9. Riveline D, et al. (2001) Focal contacts as mechanosensors: Externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J Cell Biol 153(6):1175-1186.
10. Higashida C, et al. (2013) F- and G-actin homeostasis regulates mechanosensitive actin nucleation by formins. Nat Cell Biol 15(4):395-405.
11. Choquet D, Felsenfeld DP, Sheetz MP (1997) Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell 88(1):39-48.
12. Galbraith CG, Yamada KM, Sheetz MP (2002) The relationship between force and focal complex development. J Cell Biol 159(4):695-705.
13. Wang Y, et al. (2005) Visualizing the mechanical activation of Src. Nature 434(7036):1040-1045.
14. Glogauer M, et al. (1997) Calcium ions and tyrosine phosphorylation interact coordinately with actin to regulate cytoprotective responses to stretching. J Cell Sci 110(Pt 1):11-21.
15. Collins C, et al. (2012) Localized tensional forces on PECAM-1 elicit a global mechanotransduction response via the integrin-RhoA pathway. Curr Biol 22(22):2087-2094.
16. Iyer KV, Pulford S, Mogilner A, Shivashankar GV (2012) Mechanical activation of cells induces chromatin remodeling preceding MKL nuclear transport. Biophys J 103(7):1416-1428.
17. Chan MW, Chaudary F, Lee W, Copeland JW, McCulloch CA (2010) Force-induced myofibroblast differentiation through collagen receptors is dependent on mammalian diaphanous (mDia). J Biol Chem 285(12):9273-9281.
18. Shivashankar GV (2011) Mechanosignaling to the cell nucleus and gene regulation. Annu Rev Biophys 40:361-378.
19. Yip AK, et al. (2013) Cellular response to substrate rigidity is governed by either stress or strain. Biophys J 104(1):19-29.
20. Riedl J, et al. (2008) Lifeact: A versatile marker to visualize F-actin. Nat Methods 5(7):605-607.
21. Roberts WG, et al. (2008) Antitumor activity and pharmacology of a selective focal adhesion kinase inhibitor, PF-562,271. Cancer Res 68(6):1935-1944.
22. Ruder WC, et al. (2012) Calcium signaling is gated by a mechanical threshold in three-dimensional environments. Sci Rep 2(2012):554.
23. Glogauer M, Ferrier J, McCulloch CA (1995) Magnetic fields applied to collagen-coated ferric oxide beads induce stretch-activated Ca2+ flux in fibroblasts. Am J Physiol 269(5 Pt 1):C1093-C1104.
24. Munevar S, Wang YL, Dembo M (2004) Regulation of mechanical interactions between fibroblasts and the substratum by stretch-activated Ca2+ entry. J Cell Sci1 17(Pt 1):85-92.
25. Nakai J, Ohkura M, Imoto K (2001) A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat Biotechnol 19(2):137-141.
26. Thastrup O, Cullen PJ, Drøbak BK, Hanley MR, Dawson AP (1990) Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc Natl Acad Sci USA 87(7):2466-2470.
27. Chao TS, Byron KL, Lee KM, Villereal M, Rosner MR (1992) Activation of MAP kinases by calcium-dependent and calcium-independent pathways. Stimulation by thapsigargin and epidermal growth factor. J Biol Chem 267(28):19876-19883.
28. Hirata H, Tatsumi H, Sokabe M (2008) Mechanical forces facilitate actin polymerization at focal adhesions in a zyxin-dependent manner. J Cell Sci 121(Pt 17):2795-2804.
29. Hotulainen P, Paunola E, Vartiainen MK, Lappalainen P (2005) Actin-depolymerizing factor and cofilin-1 play overlapping roles in promoting rapid F-actin depolymerization in mammalian nonmuscle cells. Mol Biol Cell 16(2):649-664.
30. Crisp M, et al. (2006) Coupling of the nucleus and cytoplasm: Role of the LINC complex. J Cell Biol 172(1):41-53.
31. Lombardi ML, et al. (2011) The interaction between nesprins and sun proteins at the nuclear envelope is critical for force transmission between the nucleus and cytoskeleton. J Biol Chem 286(30):26743-26753.
32. Gay O, et al. (2011) RefilinB (FAM101B) targets filamin A to organize perinuclear actin networks and regulates nuclear shape. Proc Natl Acad Sci USA 108(28):11464-11469.
33. Lynch CD, et al. (2011) Filamin depletion blocks endoplasmic spreading and destabilizes force-bearing adhesions. Mol Biol Cell 22(8):1263-1273.
34. Chhabra ES, Ramabhadran V, Gerber SA, Higgs HN (2009) INF2 is an endoplasmic reticulum-associated formin protein. J Cell Sci 122(Pt 9):1430-1440.
35. Ramabhadran V, Hatch AL, Higgs HN (2013) Actin monomers activate inverted formin 2 by competing with its autoinhibitory interaction. J Biol Chem 288(37):26847-26855.
36. Woo SH, et al. (2014) Piezo2 is required for Merkel-cell mechanotransduction. Nature 509(7502):622-626.
37. Coste B, et al. (2012) Piezo proteins are pore-forming subunits of mechanically activated channels. Nature 483(7388):176-181.
38. Idone V, Tam C, Andrews NW (2008) Two-way traffic on the road to plasma membrane repair. Trends Cell Biol 18(11):552-559.
39. Wang Y, Shibasaki F, Mizuno K (2005) Calcium signal-induced cofilin dephosphorylation is mediated by Slingshot via calcineurin. J Biol Chem 280(13):12683-12689.
40. Robinson RC, et al. (1999) Domain movement in gelsolin: A calcium-activated switch. Science 286(5446):1939-1942.
41. Higashida C, et al. (2008) G-actin regulates rapid induction of actin nucleation by mDia1 to restore cellular actin polymers. J Cell Sci 121(Pt 20):3403-3412.
42. Gurel PS, et al. (2014) INF2-mediated severing through actin filament encirclement and disruption. Curr Biol 24(2):156-164.
43. Madrid R, et al. (2010) The formin INF2 regulates basolateral-to-apical transcytosis and lumen formation in association with Cdc42 and MAL2. Dev Cell 18(5):814-827.
44. Buxboim A, et al. (2014) Matrix elasticity regulates lamin-A,C phosphorylation and turnover with feedback to actomyosin. Curr Biol 24(16):1909-1917.
45. Rivas FV, O'Keefe JP, Alegre ML, Gajewski TF (2004) Actin cytoskeleton regulates calcium dynamics and NFAT nuclear duration. Mol Cell Biol 24(4):1628-1639.
46. Hogan PG, Chen L, Nardone J, Rao A (2003) Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev 17(18):2205-2232.
47. Dupont S, et al. (2011) Role of YAP/TAZ in mechanotransduction. Nature 474(7350):179-183.
48. Aragona M, et al. (2013) A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 154(5):1047-1059.
49. Brown EJ, et al. (2010) Mutations in the formin gene INF2 cause focal segmental glomerulosclerosis. Nat Genet 42(1):72-76.
50. Boyer O, et al. (2011) INF2 mutations in Charcot-Marie-Tooth disease with glomerulopathy. N Engl J Med 365(25):2377-2388.
51. Giannone G, et al. (2007) Lamellipodial actin mechanically links myosin activity with adhesion-site formation. Cell 128(3):561-575.
52. Luo W, et al. (2013) Analysis of the local organization and dynamics of cellular actin networks. J Cell Biol 202(7):1057-1073.
53. Zilberman Y, et al. (2011) Involvement of the Rho-mDia1 pathway in the regulation of Golgi complex architecture and dynamics. Mol Biol Cell 22(16):2900-2911.