Nesprin-3 regulates endothelial cell morphology, perinuclear cytoskeletal architecture, and flow-induced polarization

Molecular Biology of the Cell

Volumn 22, Issue 22, 2011, Pages 4324-4334

  Morgan, Joshua T ^a   Pfeiffer, Emily R ^a   Thirkill, Twanda L ^b   Kumar, Priyadarsini ^b   Peng, Gordon ^a   Fridolfsson, Heidi N ^c   Douglas, Gordon C ^b   Starr, Daniel A ^c   Barakat, Abdul I ^a,d  

^a University of California   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d ECOLE POLYTECHNIQUE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

NESPRIN 3; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BLOOD FLOW; CELL ELONGATION; CELL MEMBRANE; CELL MIGRATION; CELL STRUCTURE; CENTROSOME; CYTOSKELETON; ENDOTHELIUM CELL; GENE MUTATION; HUMAN; HUMAN CELL; NUCLEUS ACCUMBENS; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; VASCULAR ENDOTHELIUM;

AORTA; CELL MOVEMENT; CELL NUCLEUS; CELL POLARITY; CELL SHAPE; CELLS, CULTURED; CENTROSOME; CYTOSKELETON; ENDOTHELIAL CELLS; HUMANS; INTERMEDIATE FILAMENTS; MECHANOTRANSDUCTION, CELLULAR; MEMBRANE PROTEINS; MICROFILAMENT PROTEINS; NERVE TISSUE PROTEINS; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 81755162747     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-04-0287     Document Type: Article

References (64)

1. Ando J, Nomura H, Kamiya A (1987). The effect of fluid shear stress on the migration and proliferation of cultured endothelial cells. Microvasc Res 33, 62-70. (Pubitemid 17006443)
2. Andra K, Lassmann H, Bittner R, Shorny S, Fassler R, Propst F, Wiche G (1997). Targeted inactivation of plectin reveals essential function in maintaining the integrity of skin, muscle, and heart cytoarchitecture. Genes Dev 11, 3143-3156. (Pubitemid 27528055)
3. Apel ED, Lewis RM, Grady RM, Sanes JR (2000). Syne-1, a dystrophin- and Klarsicht-related protein associated with synaptic nuclei at the neuromuscular junction. J Biol Chem 275, 31986-31995.
4. Brosig M, Ferralli J, Gelman L, Chiquet M, Chiquet-Ehrismann R (2010). Interfering with the connection between the nucleus and the cytoskeleton affects nuclear rotation, mechanotransduction and myogenesis. Int J Biochem Cell Biol 42, 1717-1728.
5. Burgstaller G, Gregor M, Winter L, Wiche G (2010). Keeping the vimentin network under control: cell-matrix adhesion-associated plectin 1f affects cell shape and polarity of fibroblasts. Mol Biol Cell 21, 3362-3375.
6. Cao Y, Linden P, Farnebo J, Cao R, Eriksson A, Kumar V, Qi JH, Claesson-Welsh L, Alitalo K (1998). Vascular endothelial growth factor C induces angiogenesis in vivo. Proc Natl Acad Sci USA 95, 14389-14394. (Pubitemid 28549377)
7. Chancellor TJ, Lee J, Thodeti CK, Lele T (2010). Actomyosin tension exerted on the nucleus through nesprin-1 connections influences endothelial cell adhesion, migration, and cyclic strain-induced reorientation. Biophys J 99, 115-123.
8. Chen CS, Alonso JL, Ostuni E, Whitesides GM, Ingber DE (2003). Cell shape provides global control of focal adhesion assembly. Biochem Biophys Res Commun 307, 355-361. (Pubitemid 36818878)
9. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE (1997). Geometric control of cell life and death. Science 276, 1425-1428. (Pubitemid 27235413)
10. Chien S (2007). Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell. Am J Physiol 292, H1209-1224.
11. Crisp M, Liu Q, Roux K, Rattner JB, Shanahan C, Burke B, Stahl PD, Hodzic D (2006). Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Biol 172, 41-53. (Pubitemid 43042628)
12. Dahl KN, Booth-Gauthier EA, Ladoux B (2010). In the middle of it all: mutual mechanical regulation between the nucleus and the cytoskeleton. J Biomech 43, 2-8.
13. Davies PF (1995). Flow-mediated endothelial mechanotransduction. Physiol Rev 75, 519-560.
14. Galbraith CG, Skalak R, Chien S (1998). Shear stress induces spatial reorganization of the endothelial cell cytoskeleton. Cell Motil Cytoskeleton 40, 317-330. (Pubitemid 28364153)
15. Gieni RS, Hendzel MJ (2008). Mechanotransduction from the ECM to the genome: are the pieces now in place? J Cell Biochem 104, 1964-1987.
16. Gojova A, Barakat AI (2005). Vascular endothelial wound closure under shear stress: role of membrane fluidity and flow-sensitive ion channels. J Appl Physiol 98, 2355-2362. (Pubitemid 40726937)
17. Gomes ER, Jani S, Gundersen GG (2005). Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells. Cell 121, 451-463. (Pubitemid 40692304)
18. Grady RM, Starr DA, Ackerman GL, Sanes JR, Han M (2005). Syne proteins anchor muscle nuclei at the neuromuscular junction. Proc Natl Acad Sci USA 102, 4359-4364. (Pubitemid 40397116)
19. Gray BL, Lieu DK, Collins SD, Smith RL, Barakat AI (2002). Microchannel platform for the study of endothelial cell shape and function. Biomed Microdev 4, 9-16. (Pubitemid 34240359)
20. Gros-Louis F, Dupre N, Dion P, Fox MA, Laurent S, Verreault S, Sanes JR, Bouchard JP, Rouleau GA (2007). Mutations in SYNE1 lead to a newly discovered form of autosomal recessive cerebellar ataxia. Nat Genet 39, 80-85. (Pubitemid 46026505)
21. Henrion D et al. (1997). Impaired flow-induced dilation in mesenteric resistance arteries from mice lacking vimentin. J Clin Invest 100, 2909-2914. (Pubitemid 28007562)
22. Hu S, Chen J, Butler JP, Wang N (2005). Prestress mediates force propagation into the nucleus. Biochem Biophys Res Commun 329, 423-428. (Pubitemid 40311763)
23. Huveneers S, Danen EH (2009). Adhesion signaling - crosstalk between integrins, Src and Rho. J Cell Sci 122, 1059-1069.
24. Hynes RO (2002). Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687.
25. Ketema M, Wilhelmsen K, Kuikman I, Janssen H, Hodzic D, Sonnenberg A (2007). Requirements for the localization of nesprin-3 at the nuclear envelope and its interaction with plectin. J Cell Sci 120, 3384-3394. (Pubitemid 350028346)
26. Lee JS, Hale CM, Panorchan P, Khatau SB, George JP, Tseng Y, Stewart CL, Hodzic D, Wirtz D (2007). Nuclear lamin A/C deficiency induces defects in cell mechanics, polarization, and migration. Biophys J 93, 2542-2552. (Pubitemid 47511153)
27. Libotte T et al. (2005). Lamin A/C-dependent localization of Nesprin-2, a giant scaffolder at the nuclear envelope. Mol Biol Cell 16, 3411-3424. (Pubitemid 40962609)
28. Liliensiek SJ, Wood JA, Yong J, Auerbach R, Nealey PF, Murphy CJ (2010). Modulation of human vascular endothelial cell behaviors by nanotopographic cues. Biomaterials 31, 5418-5426.
29. Malech HL, Root RK, Gallin JI (1977). Structural analysis of human neutrophil migration. Centriole, microtubule, and microfilament orientation and function during chemotaxis. J Cell Biol 75, 666-693. (Pubitemid 8239170)
30. Maniotis AJ, Chen CS, Ingber DE (1997). Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc Natl Acad Sci USA 94, 849-854. (Pubitemid 27074410)
31. Masuda M, Fujiwara K (1993). The biased lamellipodium development and microtubule organizing center position in vascular endothelial cells migrating under the influence of fluid flow. Biol Cell 77, 237-245. (Pubitemid 23238635)
32. Mazzag BM, Tamaresis JS, Barakat AI (2003). A model for shear stress sensing and transmission in vascular endothelial cells. Biophys J 84, 4087-4101. (Pubitemid 36637900)
33. McCue S, Dajnowiec D, Xu F, Zhang M, Jackson MR, Langille BL (2006). Shear stress regulates forward and reverse planar cell polarity of vascular endothelium in vivo and in vitro. Circ Res 98, 939-946.
34. McGee MD, Rillo R, Anderson AS, Starr DA (2006). UNC-83 IS a KASH protein required for nuclear migration and is recruited to the outer nuclear membrane by a physical interaction with the SUN protein UNC-84. Mol Biol Cell 17, 1790-1801. (Pubitemid 44011595)
35. Na S, Collin O, Chowdhury F, Tay B, Ouyang M, Wang Y, Wang N (2008). Rapid signal transduction in living cells is a unique feature of mechanotransduction. Proc Natl Acad Sci USA 105, 6626-6631. (Pubitemid 351754557)
36. Neumann S, Schneider M, Daugherty RL, Gottardi CJ, Eming SA, Beijer A, Noegel AA, Karakesisoglou I (2010). Nesprin-2 interacts with alpha-catenin and regulates Wnt signaling at the nuclear envelope. J Biol Chem 285, 34932-34938.
37. Niwa T, Saito H, Imajoh-ohmi S, Kaminishi M, Seto Y, Miki Y, Nakanishi A (2009). BRCA2 interacts with the cytoskeletal linker protein plectin to form a complex controlling centrosome localization. Cancer Sci 100, 2115-2125.
38. Padmakumar VC, Abraham S, Braune S, Noegel AA, Tunggal B, Karakesisoglou I, Korenbaum E (2004). Enaptin, a giant actin-binding protein, is an element of the nuclear membrane and the actin cytoskeleton. Exp Cell Res 295, 330-339. (Pubitemid 38490489)
39. Postel R, Ketema M, Kuikman I, de Pereda JM, Sonnenberg A (2011). Nesprin-3 augments peripheral nuclear localization of intermediate filaments in zebrafish. J Cell Sci 124, 755-764.
40. Puckelwartz MJ et al. (2009). Disruption of nesprin-1 produces an Emery Dreifuss muscular dystrophy-like phenotype in mice. Hum Mol Genet 18, 607-620.
41. Puckelwartz MJ et al. (2010). Nesprin-1 mutations in human and murine cardiomyopathy. J Mol Cell Cardiol 48, 600-608.
42. Razafsky D, Hodzic D (2009). Bringing KASH under the SUN: the many faces of nucleo-cytoskeletal connections. J Cell Biol 186, 461-472.
43. Rogers KA, Kalnins VI (1983). Comparison of the cytoskeleton in aortic endothelial cells in situ and in vitro. Lab 49, 650-654. (Pubitemid 14220330)
44. Rogers KA, McKee NH, Kalnins VI (1985). Preferential orientation of centrioles toward the heart in endothelial cells of major blood vessels is reestablished after reversal of a segment. Proc Natl Acad Sci USA 82, 3272-3276. (Pubitemid 15033165)
45. Roux KJ, Crisp ML, Liu Q, Kim D, Kozlov S, Stewart CL, Burke B (2009). Nesprin 4 is an outer nuclear membrane protein that can induce kinesin-mediated cell polarization. Proc Natl Acad Sci USA 106, 2194-2199.
46. Salpingidou G, Smertenko A, Hausmanowa-Petrucewicz I, Hussey PJ, Hutchison CJ (2007). A novel role for the nuclear membrane protein emerin in association of the centrosome to the outer nuclear membrane. J Cell Biol 178, 897-904. (Pubitemid 47443314)
47. Schneider M, Lu W, Neumann S, Brachner A, Gotzmann J, Noegel AA, Karakesisoglou I (2011). Molecular mechanisms of centrosome and cytoskeleton anchorage at the nuclear envelope. Cell Mol Life Sci 68, 1593-1610.
48. Starr DA (2009). A nuclear-envelope bridge positions nuclei and moves chromosomes. J Cell Sci 122, 577-586.
49. Starr DA, Fridolfsson HN (2010). Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu Rev Cell Dev Biol 26, 421-444.
50. Stewart-Hutchinson PJ, Hale CM, Wirtz D, Hodzic D (2008). Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness. Exp Cell Res 314, 1892-1905.
51. Suvatne J, Barakat AI, O'Donnell ME (2001). Flow-induced expression of endothelial Na-K-Cl cotransport: dependence on K+ and Cl- channels. Am J Physiol 280, C216-C227.
52. Tzima E, Kiosses WB, del Pozo MA, Schwartz MA (2003). Localized cdc42 activation, detected using a novel assay, mediates microtubule organizing center positioning in endothelial cells in response to fluid shear stress. J Biol Chem 278, 31020-31023. (Pubitemid 36994615)
53. Vartanian KB, Berny MA, McCarty OJ, Hanson SR, Hinds MT (2010). Cytoskeletal structure regulates endothelial cell immunogenicity independent of fluid shear stress. Am J Physiol 298, C333-C341.
54. Vartanian KB, Kirkpatrick SJ, Hanson SR, Hinds MT (2008). Endothelial cell cytoskeletal alignment independent of fluid shear stress on micropatterned surfaces. Biochem Biophys Res Commun 371, 787-792.
55. 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.
56. Westwood SM, Gray BL, Grist S, Huffman K, Jaffer S, Kavanagh KL (2008). SU-8 polymer enclosed microchannels with interconnect and nanohole arrays as an optical detection device for biospecies. Proc IEEE Eng Med Biol Soc 2008, 5652-5655.
57. Wheeler MA, Davies JD, Zhang Q, Emerson LJ, Hunt J, Shanahan CM, Ellis JA (2007). Distinct functional domains in nesprin-1alpha and nesprin-2beta bind directly to emerin and both interactions are disrupted in X-linked Emery-Dreifuss muscular dystrophy. Exp Cell Res 313, 2845-2857. (Pubitemid 47126429)
58. Wilhelmsen K, Litjens SH, Kuikman I, Tshimbalanga N, Janssen H, van den Bout I, Raymond K, Sonnenberg A (2005). Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin. J Cell Biol 171, 799-810. (Pubitemid 41746582)
59. Zhang J et al. (2010). Nesprin 1 is critical for nuclear positioning and anchorage. Hum Mol Genet 19, 329-341.
60. Zhang Q et al. (2007a). Nesprin-1 and -2 are involved in the pathogenesis of Emery Dreifuss muscular dystrophy and are critical for nuclear envelope integrity. Hum Mol Genet 16, 2816-2833. (Pubitemid 350048381)
61. Zhang Q, Skepper JN, Yang F, Davies JD, Hegyi L, Roberts RG, Weissberg PL, Ellis JA, Shanahan CM (2001). Nesprins: a novel family of spectrin-repeat-containing proteins that localize to the nuclear membrane in multiple tissues. J Cell Sci 114, 4485-4498. (Pubitemid 34082869)
62. Zhang X, Lei K, Yuan X, Wu X, Zhuang Y, Xu T, Xu R, Han M (2009). SUN1/2 and Syne/Nesprin-1/2 complexes connect centrosome to the nucleus during neurogenesis and neuronal migration in mice. Neuron 64, 173-187.
63. Zhang X, Xu R, Zhu B, Yang X, Ding X, Duan S, Xu T, Zhuang Y, Han M (2007b). Syne-1 and Syne-2 play crucial roles in myonuclear anchorage and motor neuron innervation. Development 134, 901-908. (Pubitemid 46795681)
64. Zhen YY, Libotte T, Munck M, Noegel AA, Korenbaum E (2002). NUANCE, a giant protein connecting the nucleus and actin cytoskeleton. J Cell Sci 115, 3207-3222.