Nuclear envelope proteins Nesprin2 and LaminA regulate proliferation and apoptosis of vascular endothelial cells in response to shear stress

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1853, Issue 5, 2015, Pages 1165-1173

  Han, Yue ^a   Wang, Lu ^a   Yao, Qing Ping ^a   Zhang, Ping ^a   Liu, Bo ^a   Wang, Guo Liang ^a   Shen, Bao Rong ^a   Cheng, Binbin ^b   Wang, Yingxiao ^a,b   Jiang, Zong Lai ^a   Qi, Ying Xin ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dysfunction; Endothelial cells; Nuclear envelope proteins; Shear stress; Transcription factor; Vascular remodeling

Indexed keywords

LAMIN A; NESPRIN 2; NUCLEAR PROTEIN; SMALL INTERFERING RNA; STAT1 PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN; STAT6 PROTEIN; UNCLASSIFIED DRUG; NERVE PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL NUCLEUS MEMBRANE; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FLOW CYTOMETRY; GENE OVEREXPRESSION; GENE TARGETING; IMMUNOFLUORESCENCE TEST; MECHANOTRANSDUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN EXPRESSION; PROTEIN HOMEOSTASIS; REAL TIME POLYMERASE CHAIN REACTION; SHEAR STRESS; VASCULAR ENDOTHELIUM; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; CYTOLOGY; GENE REGULATORY NETWORK; MECHANICAL STRESS; METABOLISM; PHOSPHORYLATION; RAT; RNA INTERFERENCE; SHEAR STRENGTH; ULTRASTRUCTURE;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL CELLS; GENE REGULATORY NETWORKS; LAMIN TYPE A; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; NUCLEAR ENVELOPE; PHOSPHORYLATION; RATS; RNA INTERFERENCE; SHEAR STRENGTH; STRESS, MECHANICAL; TRANSCRIPTION FACTORS;

EID: 84924060890     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2015.02.013     Document Type: Article

References (45)

1. Chien S. Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell. Am. J. Physiol. Heart Circ. Physiol. 2007, 292:H1209-H1224.
2. Zhou J., Li Y.S., Chien S. Shear stress-initiated signaling and its regulation of endothelial function. Arterioscler. Thromb. Vasc. Biol. 2014, 34:2191-2198.
3. Weinbaum S., Zhang X., Han Y., Vink H., Cowin S.C. Mechanotrasduction and flow across the endothelial glycocalyx. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:7988-7995.
4. Liu Y., Chen B.P., Lu M., Zhu Y., Stemerman M.B., Chien S., Shyy J.Y. Shear stress activation of SREBP1 in endothelial cells is mediated by integrins. Arterioscler. Thromb. Vasc. Biol. 2002, 22:76-81.
5. Traub O., Ishida T., Ishida M., Tupper J.C., Berk B.C. Shear stress-mediated extracellular signal-regulated kinase activation is regulated by sodium in endothelial cells. Potential role for a voltage-dependent sodium channel. J. Biol. Chem. 1999, 274:20144-20150.
6. Chen K.D., Li Y.S., Kim M., Li S., Yuan S., Chien S., Shyy J.Y. Mechanotransduction in response to shear stress. Roles of receptor tyrosine kinases, integrins, and Shc. J. Biol. Chem. 1999, 274:18393-18400.
7. Yamamoto K., Sokabe T., Matsumoto T., Yoshimura K., Shibata M., Ohura N., Fukuda T., Sato T., Sekine K., Kato S., Isshiki M., Fujita T., Kobayashi M., Kawamura K., Masuda H., Kamiya A., Ando J. Impaired flow-dependent control of vascular tone and remodeling in P2X4-deficient mice. Nat. Med. 2006, 12:133-137.
8. Houben F., Ramaekers F.C., Snoeckx L.H., Broers J.L. Role of nuclear lamina-cytoskeleton interactions in the maintenance of cellular strength. Biochim. Biophys. Acta 2007, 1773:675-686.
9. Qi Y.X., Jiang J., Jiang X.H., Wang X.D., Ji S.Y., Han Y., Long D.K., Shen B.R., Yan Z.Q., Chien S., Jiang Z.L. PDGF-BB and TGF-β1 on cross-talk between endothelial and smooth muscle cells in vascular remodeling induced by low shear stress. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:1908-1913.
10. Caille N., Thoumine O., Tardy Y., Meister J.J. Contribution of the nucleus to the mechanical properties of endothelial cells. J. Biomech. 2002, 35:177-187.
11. Kris N.D., Ribeiro A.J., Lammerding J. Nuclear shape, mechanics, and mechanotransduction. Circ. Res. 2008, 102:1307-1318.
12. Crisp M., Liu Q., Roux K., Rattner J.B., Shanahan C., Burke B., Stahl P.D., Hodzic D. Coupling of the nucleus and cytoplasm: role of the LINC complex. J. Cell Biol. 2006, 172:41-53.
13. Holaska J.M. Emerin and the nuclear lamina in muscle and cardiac disease. Circ. Res. 2008, 103:16-23.
14. Isermann P., Lammerding J. Nuclear mechanics and mechanotransduction in health and disease. Curr. Biol. 2013, 23:R1113-R1121.
15. Kwan H.Y., Leung P.C., Huang Y., Yao X. Depletion of intracellular Ca2+ stores sensitizes the flow-induced Ca2+ influx in rat endothelial cells. Circ. Res. 2003, 92:286-292.
16. Schena M., Shalon D., Davis R.W., Brown P.O. Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 1995, 270:467-470.
17. Zeng Q., Zhang P., Wu Z., Xue P., Lu D., Ye Z., Zhang X., Huang Z., Feng J., Song L., Yang D., Jiang T., Yan X. Quantitative proteomics reveals ER-α involvement in CD146-induced epithelial-mesenchymal transition in breast cancer cells. J. Proteome 2014, 155-159. (pii: S1874-3919).
18. Liu Y.Y., Wong-Riley M.T., Liu J.P., Jia Y., Liu H.L., Jiao X.Y., Ju G. GABAergic and glycinergic synapses onto neurokinin-1 receptor-immunoreactive neurons in the pre-Bötzinger complex of rats: light and electron microscopic studies. Eur. J. Neurosci. 2002, 16:1058-1066.
19. Andrés V., González J.M. Role of A-type lamins in signaling, transcription, and chromatin organization. J. Cell Biol. 2009, 187:945-957.
20. Cecchi E., Giglioli C., Valente S., Lazzeri C., Gensini G.F., Abbate R., Mannini L. Role of hemodynamic shear stress in cardiovascular disease. Atherosclerosis 2011, 214:249-256.
21. Zhang Q., Skepper J.N., Yang F., Davies J.D., Hegyi L., Roberts R.G., Weissberg P.L., Ellis J.A., Shanahan C.M. Nesprins: a novel family of spectrin-repeat-containing proteins that localize to the nuclear membrane in multiple tissues. J. Cell Sci. 2001, 114:4485-4498.
22. Yu J., Lei K., Zhou M., Craft C.M., Xu G., Xu T., Zhuang Y., Xu R., Han M. KASH protein Syne-2/Nesprin-2 and SUN proteins SUN1/2 mediate nuclear migration during mammalian retinal development. Hum. Mol. Genet. 2011, 20:1061-1073.
23. Hutchison C.J., Worman H.J. A-type lamins: guardians of the soma?. Nat. Cell Biol. 2004, 6:1062-1067.
24. Lammerding J., Lee R.T. Torn apart: membrane rupture in muscular dystrophies and associated cardiomyopathies. J. Clin. Invest. 2007, 117:1749-1752.
25. Gonzalez J.M., Pla D., Perez-Sala D., Andres V. A-type lamins and Hutchinson-Gilford progeria syndrome: pathogenesis and therapy. Front. Biosci. 2011, 3:1133-1146.
26. Muchir A., Wu W., Worman H.J. Mitogen-activated protein kinase inhibitor regulation of heart function and fibrosis in cardiomyopathy caused by lamin A/C gene mutation. Trends Cardiovasc. Med. 2010, 20:217-221.
27. Yang L., Munck M., Swaminathan K., Kapinos L.E., Noegel A.A., Neumann S. Mutations in LMNA modulate the lamin A-Nesprin-2 interaction and cause LINC complex alterations. PLoS One 2013, 8:e71850.
28. Libotte T., Zaim H., Abraham S., Padmakumar V.C., Schneider M., Lu W., Munck M., Hutchison C., Wehnert M., Fahrenkrog B., Sauder U., Aebi U., Noegel A.A., Karakesisoglou I. Lamin A/C-dependent localization of Nesprin-2, a giant scaffolder at the nuclear envelope. Mol. Biol. Cell 2005, 16:3411-3424.
29. Chiu J.J., Chen L.J., Lee C.I., Lee P.L., Lee D.Y., Tsai M.C., Lin C.W., Usami S., Chien S. Mechanisms of induction of endothelial cell E-selectin expression by smooth muscle cells and its inhibition by shear stress. Blood 2007, 110:519-528.
30. Wang H.Q., Huang L.X., Qu M.J., Yan Z.Q., Liu B., Shen B.R., Jiang Z.L. Shear stress protects against endothelial regulation of vascular smooth muscle cell migration in a coculture system. Endothelium 2006, 13:171-180.
31. Davidson I., Kobi D., Fadloun A., Mengus G. New insights into TAFs as regulators of cell cycle and signaling pathways. Cell Cycle 2005, 4:1486-1490.
32. Fadloun A., Kobi D., Pointud J.C., Indra A.K., Teletin M., Bole-Feysot C., Testoni B., Mantovani R., Metzger D., Mengus G., Davidson I. The TFIID subunit TAF4 regulates keratinocyte proliferation and has cell-autonomous and non-cell-autonomous tumour suppressor activity in mouse epidermis. Development 2007, 134:2947-2958.
33. Mohan W.S., Scheer E., Wendling O., Metzger D., Tora L. TAF10 (TAF(II)30) is necessary for TFIID stability and early embryogenesis in mice. Mol. Cell. Biol. 2003, 23:4307-4318.
34. Heimberger A.B., McGary E.C., Suki D., Ruiz M., Wang H., Fuller G.N., Bar-Eli M. Loss of the AP-2alpha transcription factor is associated with the grade of human gliomas. Clin. Cancer Res. 2005, 11:267-272.
35. Darnell J.E., Jr Kerr I.M., Stark G.R. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 1994, 264:1415-1421.
36. Rawlings J.S., Rosler K.M., Harrison D.A. The JAK/STAT signaling pathway. J. Cell Sci. 2004, 117:1281-1283.
37. Ji Y.Q., Zhang Y.Q., Li M.Q., Du M.R., Wei W.W., Li D.J. EPO improves the proliferation and inhibits apoptosis of trophoblast and decidual stromal cells through activating STAT-5 and inactivating p38 signal in human early pregnancy. Int. J. Clin. Exp. Pathol. 2011, 4:765-774.
38. Kelly K. The RGK family: a regulatory tail of small GTP-binding proteins. Trends Cell Biol. 2005, 15:640-643.
39. Correll R.N., Pang C., Niedowicz D.M., Finlin B.S., Andres D.A. The RGK family of GTP-binding proteins: regulators of voltage-dependent calcium channels and cytoskeleton remodeling. Cell. Signal. 2008, 20:292-300.
40. Pan J.Y., Fieles W.E., White A.M., Egerton M.M., Silberstein Ges D.S. A human GTPase of the Rad/Gem/Kir family, promotes endothelial cell sprouting and cytoskeleton reorganization. J. Cell Biol. 2000, 149:1107-1116.
41. Ray S., Zhao Y., Jamaluddin M., Edeh C.B., Lee C., Brasier A.R. Inducible STAT3 NH2 terminal mono-ubiquitination promotes BRD4 complex formation to regulate apoptosis. Cell. Signal. 2014, 26:1445-1455.
42. Labeur M., Refojo D., Wölfel B., Stalla J., Vargas V., Theodoropoulou M., Buchfelder M., Paez-Pereda M., Arzt E., Stalla G.K. Interferon-gamma inhibits cellular proliferation and ACTH production in corticotroph tumor cells through a novel janus kinases-signal transducer and activator of transcription 1/nuclear factor-kappa B inhibitory signaling pathway. J. Endocrinol. 2008, 199:177-189.
43. Busk P.K., Hinrichsen R., Bartkova J., Hansen A.H., Christoffersen T.E., Bartek J., Haunsø S. Cyclin D2 induces proliferation of cardiac myocytes and represses hypertrophy. Exp. Cell Res. 2005, 304:149-161.
44. Hay D.C., Beers C., Cameron V., Thomson L., Flitney F.W., Hay R.T. Activation of NF-kappaB nuclear transcription factor by flow in human endothelial cells. Biochim. Biophys. Acta 2003, 1642:33-44.
45. Brosig M., Ferralli J., Gelman L., Chiquet M., Chiquet-Ehrismann R. Interfering with the connection between the nucleus and the cytoskeleton affects nuclear rotation mechanotransduction and myogenesis. Int. J. Biochem. Cell Biol. 2010, 42:1717-1728.