Endothelial nuclear lamina is not required for glucocorticoid receptor nuclear import but does affect receptor-mediated transcription activation

American Journal of Physiology - Cell Physiology

Volumn 305, Issue 3, 2013, Pages

  Nayebosadri, Arman ^a   Ji, Julie Y ^a  

^a Indiana University Purdue University Indianapolis   (United States)

Author keywords

Dexamethasone; Endothelial cells; Glucocorticoid receptor; Nuclear lamina; Shear stress

Indexed keywords

DEXAMETHASONE; DUAL SPECIFICITY PHOSPHATASE; GLUCOCORTICOID RECEPTOR; HISTONE; HISTONE DEACETYLASE; I KAPPA B KINASE ALPHA; LAMIN A; LAMIN C; LUCIFERASE;

ALGORITHM; ANIMAL CELL; ARTICLE; BAYES THEOREM; CELL NUCLEUS; CELL TRANSPORT; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IMAGE ANALYSIS; NONHUMAN; NUCLEAR LAMINA; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; SHEAR STRESS; TRANSCRIPTION INITIATION;

EID: 84881019507     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00293.2012     Document Type: Article

References (67)

1. Adcock IM. Glucocorticoid-regulated transcription factors. Pulm Pharmacol Ther 14: 211-219, 2001.
2. Adcock IM, Caramori G. Cross-talk between pro-inflammatory transcription factors and glucocorticoids. Immunol Cell Biol 79: 376-384, 2001.
3. Adenuga D, Rahman I. Oxidative stress, histone deacetylase and corticosteroid resistance in severe asthma and COPD. Curr Resp Med Rev 3: 57-68, 2007.
4. Al-Shali KZ, Hegele RA. Laminopathies and atherosclerosis. Arterioscler Thromb Vasc Biol 24: 1591-1595, 2004.
5. Almawi WY, Melemedjian OK. Molecular mechanisms of glucocorticoid antiproliferative effects: antagonism of transcription factor activity by glucocorticoid receptor. J Leukoc Biol 71: 9-15, 2002.
6. Avenant C, Kotitschke A, Hapgood JP. Glucocorticoid receptor phosphorylation modulates transcription efficacy through GRIP-1 recruitment. Biochemistry 49: 972-985, 2010.
7. Barnes PJ. Anti-inflammatory actions of glucocorticoids: molecular mechanisms. Clin Sci (Lond) 94: 557-572, 1998.
8. Beck IM, Vanden Berghe W, Vermeulen L, Yamamoto KR, Haegeman G, De Bosscher K. Crosstalk in inflammation: the interplay of glucocorticoid receptor-based mechanisms and kinases and phosphatases. Endocr Rev 30: 830-882, 2009.
9. Bione S, Maestrini E, Rivella S, Mancini M, Regis S, Romeo G, Toniolo D. Identification of a novel X-linked gene responsible for Emery- Dreifuss muscular dystrophy. Nat Genet 8: 323-327, 1994.
10. Blake G, Ridker P. Inflammatory bio-markers and cardiovascular risk prediction. J Intern Med 252: 283-294, 2002.
11. Bonne G, Di Barletta MR, Varnous S, Becane HM, Hammouda EH, Merlini L, Muntoni F, Greenberg CR, Gary F, Urtizberea JA, Duboc D, Fardeau M, Toniolo D, Schwartz K. Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat Genet 21: 285-288, 1999.
12. Braddock M, Schwachtgen JL, Houston P, Dickson MC, Lee MJ, Campbell CJ. Fluid shear stress modulation of gene expression in endothelial cells. News Physiol Sci 13: 241-246, 1998.
13. Burke B, Stewart CL. Life at the edge: the nuclear envelope and human disease. Nat Rev Mol Cell Biol 3: 575-585, 2002.
14. Butin-Israeli V, Adam SA, Goldman AE, Goldman RD. Nuclear lamin functions and disease. Trends Genet 28: 464-471, 2012.
15. Cao H, Hegele RA. Nuclear lamin A/C R482Q mutation in canadian kindreds with Dunnigan-type familial partial lipodystrophy. Hum Mol Genet 9: 109-112, 2000.
16. Chien S. Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell. Am J Physiol Heart Circ Physiol 292: H1209-H1224, 2007.
17. Clark AR. Anti-inflammatory functions of glucocorticoid-induced genes. Mol Cell Endocrinol 275: 79-97, 2007.
18. Crisp M, Liu Q, Roux K, Rattner JB, Shanahan C, Burke B, Stahl PD, Hodzic D. Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Biol 172: 41-53, 2006.
19. Dahl KN, Ribeiro AJ, Lammerding J. Nuclear shape, mechanics, mechanotransduction. Circ Res 102: 1307-1318, 2008.
20. Davignon J, Ganz P. Role of endothelial dysfunction in atherosclerosis. Circulation 109: page typefirstIII27/pagex-/xpage typelast32/page, 2004.
21. De Sandre-Giovannoli A, Chaouch M, Kozlov S, Vallat JM, Tazir M, Kassouri N, Szepetowski P, Hammadouche T, Vandenberghe A, Stewart CL, Grid D, Levy N. Homozygous defects in LMNA, encoding lamin A/C nuclear-envelope proteins, cause autosomal recessive axonal neuropathy in human (Charcot-Marie-Tooth disorder type 2) and mouse. Am J Hum Genet 70: 726-736, 2002.
22. De Vos WH, Houben F, Kamps M, Malhas A, Verheyen F, Cox J, Manders EM, Verstraeten VL, van Steensel MA, Marcelis CL, van den Wijngaard A, Vaux DJ, Ramaekers FC, Broers JL. Repetitive disruptions of the nuclear envelope invoke temporary loss of cellular compartmentalization in laminopathies. Hum Mol Genet 20: 4175-4186, 2011.
23. Dechat T, Pfleghaar K, Sengupta K, Shimi T, Shumaker DK, Solimando L, Goldman RD. Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev 22: 832-853, 2008.
24. Demmerle J, Koch AJ, Holaska JM. The nuclear envelope protein emerin binds directly to histone deacetylase 3 (HDAC3) and activates HDAC3 activity. J Biol Chem 287: 22080-22088, 2012.
25. Deroo BJ, Archer TK. Glucocorticoid receptor activation of the I kappa B alpha promoter within chromatin. Mol Biol Cell 12: 3365-3374, 2001.
26. Dewey CF Jr, Bussolari SR, Gimbrone MA Jr, Davies PF. The dynamic response of vascular endothelial cells to fluid shear stress. J Biomech Eng 103: 177-185, 1981.
27. Diamond MI, Miner JN, Yoshinaga SK, Yamamoto KR. Transcription factor interactions: selectors of positive or negative regulation from a single DNA element. Science 249: 1266-1272, 1990.
28. Eickelberg O, Roth M, Lorx R, Bruce V, Rudiger J, Johnson M, Block LH. Ligand-independent activation of the glucocorticoid receptor by beta2-adrenergic receptor agonists in primary human lung fibroblasts and vascular smooth muscle cells. J Biol Chem 274: 1005-1010, 1999.
29. Eriksson M, Brown WT, Gordon LB, Glynn MW, Singer J, Scott L, Erdos MR, Robbins CM, Moses TY, Berglund P, Dutra A, Pak E, Durkin S, Csoka AB, Boehnke M, Glover TW, Collins FS. Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 423: 293-298, 2003.
30. Fatkin D, MacRae C, Sasaki T, Wolff MR, Porcu M, Frenneaux M, Atherton J, Vidaillet HJ Jr, Spudich S, De Girolami U, Seidman JG, Seidman C, Muntoni F, Muehle G, Johnson W, McDonough B. Missense mutations in the rod domain of the lamin A/C gene as causes of dilated cardiomyopathy and conduction-system disease. N Engl J Med 341: 1715-1724, 1999.
31. Fish JE, Matouk CC, Rachlis A, Lin S, Tai SC, D'Abreo C, Marsden PA. The expression of endothelial nitric-oxide synthase is controlled by a cell-specific histone code. J Biol Chem 280: 24824-24838, 2005.
32. Frangos JA, McIntire LV, Eskin SG. Shear stress induced stimulation of mammalian cell metabolism. Biotechnol Bioeng 32: 1053-1060, 1988.
33. Furst R, Schroeder T, Eilken HM, Bubik MF, Kiemer AK, Zahler S, Vollmar AM. MAPK phosphatase-1 represents a novel anti-inflammatory target of glucocorticoids in the human endothelium. FASEB J 21: 74-80, 2007.
34. Galiova G, Bartova E, Raska I, Krejci J, Kozubek S. Chromatin changes induced by lamin A/C deficiency and the histone deacetylase inhibitor trichostatin A. Eur J Cell Biol 87: 291-303, 2008.
35. Galliher-Beckley AJ, Williams JG, Cidlowski JA. Ligand-independent phosphorylation of the glucocorticoid receptor integrates cellular stress pathways with nuclear receptor signaling. Mol Cell Biol 31: 4663-4675, 2011.
36. Goldman RD, Gruenbaum Y, Moir RD, Shumaker DK, Spann TP. Nuclear lamins: building blocks of nuclear architecture. Genes Dev 16: 533-547, 2002.
37. Gruenbaum Y, Margalit A, Goldman RD, Shumaker DK, Wilson KL. The nuclear lamina comes of age. Nat Rev Mol Cell Biol 6: 21-31, 2005.
38. Gupta V, Awasthi N, Wagner BJ. Specific activation of the glucocorticoid receptor and modulation of signal transduction pathways in human lens epithelial cells. Invest Ophthalmol Vis Sci 48: 1724-1734, 2007.
39. Ho CY, Lammerding J. Lamins at a glance. J Cell Sci 125: 2087-2093, 2012.
40. Htun H, Barsony J, Renyi I, Gould DL, Hager GL. Visualization of glucocorticoid receptor translocation and intranuclear organization in living cells with a green fluorescent protein chimera. Proc Natl Acad Sci USA 93: 4845-4850, 1996.
41. Hu JM, Bodwell JE, Munck A. Cell cycle-dependent glucocorticoid receptor phosphorylation and activity. Mol Endocrinol 8: 1709-1713, 1994.
42. Hutchison CJ. Lamins: building blocks or regulators of gene expression? Nat Rev Mol Cell Biol 3: 848-858, 2002.
43. Hutchison CJ, Worman HJ. A-type lamins: guardians of the soma? Nat Cell Biol 6: 1062-1067, 2004.
44. Illi B, Nanni S, Scopece A, Farsetti A, Biglioli P, Capogrossi MC, Gaetano C. Shear stress-mediated chromatin remodeling provides molecular basis for flow-dependent regulation of gene expression. Circ Res 93: 155-161, 2003.
45. Ishida T, Peterson T, Kovach N, Berk B. MAP kinase activation by flow in endothelial cells. Role of beta 1 integrins and tyrosine kinases. Circ Res 79: 310-316, 1996.
46. Itoh M, Adachi M, Yasui H, Takekawa M, Tanaka H, Imai K. Nuclear export of glucocorticoid receptor is enhanced by c-Jun N-terminal kinasemediated phosphorylation. Mol Endocrinol 16: 2382-2392, 2002.
47. Ji JY, Jing H, Diamond SL. Shear stress causes nuclear localization of endothelial glucocorticoid receptor and expression from the GRE promoter. Circ Res 92: 279-285, 2003.
48. Ku D, Giddens D, Zarins C, Glagov S. Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis 5: 293-302, 1985.
49. Kuchan M, Frangos J. Role of calcium and calmodulin in flow-induced nitric oxide production in endothelial cells. Am J Physiol Cell Physiol 266: C628-C636, 1994.
50. Lammerding J, Schulze PC, Takahashi T, Kozlov S, Sullivan T, Kamm RD, Stewart CL, Lee RT. Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J Clin Invest 113: 370-378, 2004.
51. Libby P, DiCarli M, Weissleder R. The vascular biology of atherosclerosis and imaging targets. J Nucl Med 51, Suppl 1: 33S-37S, 2010.
52. Lloyd DJ, Trembath RC, Shackleton S. A novel interaction between lamin A and SREBP1: implications for partial lipodystrophy and other laminopathies. Hum Mol Genet 11: 769-777, 2002.
53. Luo Y, Jian W, Stavreva D, Fu X, Hager G, Bungert J, Huang S, Qiu Y. Trans-regulation of histone deacetylase activities through acetylation. J Biol Chem 284: 34901-34910, 2009.
54. Malhas AN, Lee CF, Vaux DJ. Lamin B1 controls oxidative stress responses via Oct-1. J Cell Biol 184: 45-55, 2009.
55. Matthews L, Johnson J, Berry A, Trebble P, Cookson A, Spiller D, Rivers C, Norman M, White M, Ray D. Cell cycle phase regulates glucocorticoid receptor function. PloS One 6: e22289, 2011.
56. Muchir A, Pavlidis P, Decostre V, Herron AJ, Arimura T, Bonne G, Worman HJ. Activation of MAPK pathways links LMNA mutations to cardiomyopathy in Emery-Dreifuss muscular dystrophy. J Clin Invest 117: 1282-1293, 2007.
57. Nayebosadri A, Christopher L, Ji JY. Bayesian image analysis of dexamethasone and shear stress-induced glucocorticoid receptor intracellular movement. Ann Biomed Eng 40: 1508-1519, 2012.
58. Pavalko FM, Gerard RL, Ponik SM, Gallagher PJ, Jin Y, Norvell SM. Fluid shear stress inhibits TNF-alpha-induced apoptosis in osteoblasts: a role for fluid shear stress-induced activation of PI3-kinase and inhibition of caspase-3. J Cell Physiol 194: 194-205, 2003.
59. Qiu Y, Zhao Y, Becker M, John S, Parekh BS, Huang S, Hendarwanto A, Martinez ED, Chen Y, Lu H, Adkins NL, Stavreva DA, Wiench M, Georgel PT, Schiltz RL, Hager GL. HDAC1 acetylation is linked to progressive modulation of steroid receptor-induced gene transcription. Mol Cell 22: 669-679, 2006.
60. Reddy TE, Pauli F, Sprouse RO, Neff NF, Newberry KM, Garabedian MJ, Myers RM. Genomic determination of the glucocorticoid response reveals unexpected mechanisms of gene regulation. Genome Res 19: 2163-2171, 2009.
61. Shevelyov YY, Nurminsky DI. The nuclear lamina as a gene-silencing hub. Curr Issues Mol Biol 14: 27-38, 2012.
62. Sieprath T, Darwiche R, De Vos WH. Lamins as mediators of oxidative stress. Biochem Biophys Res Commun 421: 635-639, 2012.
63. Tseng H, Peterson T, Berk B. Fluid shear stress stimulates mitogenactivated protein kinase in endothelial cells. Circ Res 77: 869-878, 1995.
64. Wilson KL, Berk JM. The nuclear envelope at a glance. J Cell Sci 123: 1973-1978, 2010.
65. Zakkar M, Chaudhury H, Sandvik G, Enesa K, Luong le A, Cuhlmann S, Mason JC, Krams R, Clark AR, Haskard DO, Evans PC. Increased endothelial mitogen-activated protein kinase phosphatase-1 expression suppresses proinflammatory activation at sites that are resistant to atherosclerosis. Circ Res 103: 726-732, 2008.
66. Zarins C, Giddens D, Bharadvaj B, Sottiurai V, Mabon R, Glagov S. Carotid bifurcation atherosclerosis. Quantitative correlation of plaque localization with flow velocity profiles and wall shear stress. Circ Res 53: 502-514, 1983.
67. Zwerger M, Jaalouk DE, Lombardi ML, Isermann P, Mauermann M, Dialynas G, Herrmann H, Wallrath LL, Lammerding J. Myopathic lamin mutations impair nuclear stability in cells and tissue and disrupt nucleo-cytoskeletal coupling. Hum Mol Genet 22: 2335-2349, 2013.