Inhibition of HSP27 blocks fibrosis development and EMT features by promoting snail degradation

FASEB Journal

Volumn 27, Issue 4, 2013, Pages 1549-1560

  Wettstein, Guillaume ^a,b   Bellaye, Pierre Simon ^a,b   Kolb, Martin ^c,d   Hammann, Arlette ^a,b   Crestani, Bruno ^e,f,g   Soler, Paul ^e,f,g   Marchal Somme, Joëlle ^e,f,g   Hazoume, Adonis ^a,b   Gauldie, Jack ^c,d   Gunther, Andreas ^h   Micheau, Olivier ^a,b   Gleave, Martin ⁱ   Camus, Philippe ^a,b,j   Garrido, Carmen ^a,b   Bonniaud, Philippe ^a,b,j  

^a Chu   (France)

^b UNIVERSITÉ DE BOURGOGNE   (France)

^c MCMASTER UNIVERSITY   (Canada)

^d MCMASTER UNIVERSITY   (Canada)

^e INSERM   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

^g BICHAT HOSPITAL   (France)

^h JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

ⁱ UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^j DIJON UNIVERSITY HOSPITAL   (France)

more..

Author keywords

Epithelial to mesenchymal transition; Mesothelial; Pleura; Transforming growth factor

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; HEAT SHOCK PROTEIN 27; OGX 427; PROTEASOME; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; FEMALE; FIBROGENESIS; FIBROSING ALVEOLITIS; GENE SILENCING; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MESOTHELIUM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RAT;

ANIMALS; CADHERINS; CELL LINE; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FIBROSIS; HSP27 HEAT-SHOCK PROTEINS; HUMANS; OLIGONUCLEOTIDES, ANTISENSE; RATS; RATS, SPRAGUE-DAWLEY; SNAILS; THIONUCLEOTIDES; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA1;

ADENOVIRIDAE; GASTROPODA; RATTUS;

EID: 84875729306     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-220053     Document Type: Article

References (53)

1. Libby, P. (2002) Inflammation in atherosclerosis. Nature 420, 868-874.
2. Hansson, G. K., and Libby, P. (2006) The immune response in atherosclerosis: a double-edged sword. Nat. Rev. Immunol. 6, 508-519.
3. Hansson, G. K., and Hermansson, A. The immune system in atherosclerosis. Nat. Immunol. 12, 204-212.
4. Taleb, S., Tedgui, A., and Mallat, Z. Adaptive T cell immune responses and atherogenesis. Curr. Opin. Pharmacol. 10, 197-202.
5. Packard, R. R., Lichtman, A. H., and Libby, P. (2009) Innate and adaptive immunity in atherosclerosis. Semin. Immunopathol. 31, 5-22.
6. Galkina, E., and Ley, K. (2009) Immune and inflammatory mechanisms of atherosclerosis. Annu. Rev. Immunol. 27, 165-197.
7. Alevizaki, M., Cimponeriu, A., Lekakis, J., Papamichael, C., and Chrousos, G. P. (2007) High anticipatory stress plasma cortisol levels and sensitivity to glucocorticoids predict severity of coronary artery disease in subjects undergoing coronary angiography. Metabolism 56, 222-226.
8. Souverein, P. C., Berard, A., Van Staa, T. P., Cooper, C., Egberts, A. C., Leufkens, H. G., and Walker, B. R. (2004) Use of oral glucocorticoids and risk of cardiovascular and cerebrovascular disease in a population based case-control study. Heart 90, 859-865.
9. Etxabe, J., and Vazquez, J. A. (1994) Morbidity and mortality in Cushing's disease: an epidemiological approach. Clin. Endocrinol. (Oxf.) 40, 479-484.
10. Faggiano, A., Pivonello, R., Spiezia, S., De Martino, M. C., Filippella, M., Di Somma, C., Lombardi, G., and Colao, A. (2003) Cardiovascular risk factors and common carotid artery caliber and stiffness in patients with Cushing's disease during active disease and 1 year after disease remission. J. Clin. Endocrinol. Metab. 88, 2527-2533.
11. Rask, E., Olsson, T., Soderberg, S., Andrew, R., Livingstone, D. E., Johnson, O., and Walker, B. R. (2001) Tissue-specific dysregulation of cortisol metabolism in human obesity. J. Clin. Endocrinol. Metab. 86, 1418-1421.
12. Livingstone, D. E., Jones, G. C., Smith, K., Jamieson, P. M., Andrew, R., Kenyon, C. J., and Walker, B. R. (2000) Understanding the role of glucocorticoids in obesity: tissue-specific alterations of corticosterone metabolism in obese Zucker rats. Endocrinology 141, 560-563.
13. Masuzaki, H., Paterson, J., Shinyama, H., Morton, N. M., Mullins, J. J., Seckl, J. R., and Flier, J. S. (2001) A transgenic model of visceral obesity and the metabolic syndrome. Science 294, 2166-2170.
14. Kotelevtsev, Y., Holmes, M. C., Burchell, A., Houston, P. M., Schmoll, D., Jamieson, P., Best, R., Brown, R., Edwards, C. R., Seckl, J. R., and Mullins, J. J. (1997) 11β-hydroxysteroid dehydrogenase type 1 knockout mice show attenuated glucocorticoid- inducible responses and resist hyperglycemia on obesity or stress. Proc. Natl. Acad. Sci. USA. 94, 14924-14929.
15. Morton, N. M., Holmes, M. C., Fievet, C., Staels, B., Tailleux, A., Mullins, J. J., and Seckl, J. R. (2001) Improved lipid and lipoprotein profile, hepatic insulin sensitivity, and glucose tolerance in 11-hydroxysteroid dehydrogenase type 1 null mice. J. Biol. Chem. 276, 41293-41300.
16. Morton, N. M., Paterson, J. M., Masuzaki, H., Holmes, M. C., Staels, B., Fievet, C., Walker, B. R., Flier, J. S., Mullins, J. J., and Seckl, J. R. (2004) Novel adipose tissue-mediated resistance to diet-induced visceral obesity in 11β-hydroxysteroid dehydrogenase type 1-deficient mice. Diabetes 53, 931-938.
17. Rosenstock, J., Banarer, S., Fonseca, V. A., Inzucchi, S. E., Sun, W., Yao, W., Hollis, G., Flores, R., Levy, R., Williams, W. V., Seckl, J. R., and Huber, R. The 11β-hydroxysteroid dehydrogenase type 1 inhibitor INCB13739 improves hyperglycemia in patients with type 2 diabetes inadequately controlled by metformin monotherapy. Diabetes Care 33, 1516-1522.
18. Hermanowski-Vosatka, A., Balkovec, J. M., Cheng, K., Chen, H. Y., Hernandez, M., Koo, G. C., Le Grand, C. B., Li, Z., Metzger, J. M., Mundt, S. S., Noonan, H., Nunes, C. N., Olson, S. H., Pikounis, B., Ren, N., Robertson, N., Schaeffer, J. M., Shah, K., Springer, M. S., Strack, A. M., Strowski, M., Wu, K., Wu, T., Xiao, J., Zhang, B. B., Wright, S. D., and Thieringer, R. (2005) 11β-HSD1 inhibition ameliorates metabolic syndrome and prevents progression of atherosclerosis in mice. J. Exp. Med. 202, 517-527.
19. Lloyd, D. J., Helmering, J., Cordover, D., Bowsman, M., Chen, M., Hale, C., Fordstrom, P., Zhou, M., Wang, M., Kaufman, S. A., and Veniant, M. M. (2009) Antidiabetic effects of 11-HSD1 inhibition in a mouse model of combined diabetes, dyslipidaemia and atherosclerosis. Diabetes Obes. Metab. 11, 688-699
20. Thieringer, R., Le, Grand, C. B., Carbin, L. Cai, T. Q., Wong, B., Wright, S. D. and Hermanowski-Vosatka, A. (2001) 11βhydroxysteroid dehydrogenase type 1 is induced in human monocytes upon differentiation to macrophages. J. Immunol. 167, 30-35.
21. Gilmour, J. S., Coutinho, A. E., Cailhier, J. F., Man, T. Y., Clay, M., Thomas, G., Harris, H. J., Mullins, J. J., Seckl, J. R., Savill, J. S., and Chapman, K. E. (2006) Local amplification of glucocorticoids by 11β-hydroxysteroid dehydrogenase type 1 promotes macrophage phagocytosis of apoptotic leukocytes. J. Immunol. 176, 7605-7611.
22. Zhang, T. Y., Ding, X., and Daynes, R. A. (2005) The expression of 11β-hydroxysteroid dehydrogenase type I by lymphocytes provides a novel means for intracrine regulation of glucocorticoid activities. J. Immunol. 174, 879-889.
23. Liu, Y., Cousin, J. M., Hughes, J., Van Damme, J., Seckl, J. R., Haslett, C., Dransfield, I., Savill, J., and Rossi, A. G. (1999) Glucocorticoids promote nonphlogistic phagocytosis of apoptotic leukocytes. J. Immunol. 162, 3639-3646.
24. Chapman, K. E., Coutinho, A. E., Gray, M., Gilmour, J. S., Savill, J. S., and Seckl, J. R. (2009) The role and regulation of 11β-hydroxysteroid dehydrogenase type 1 in the inflammatory response. Mol. Cell. Endocrinol. 301, 123-131.
25. Coutinho, A. E., Gray, M., Seckl, J. R., and Chapman, K. E. (2012) 11β-hydroxysteroid dehydrogenase type 1, but not type2, deficiency worsens acute inflammation and experimental arthritis in mice. Endocrinology 153, 234-240.
26. Poon, M., Gertz, S. D., Fallon, J. T., Wiegman, P., Berman, J. W., Sarembock, I. J., and Taubman, M. B. (2001) Dexamethasone inhibits macrophage accumulation after balloon arterial injury in cholesterol fed rabbits. Atherosclerosis 155, 371-380.
27. Goncharova, E. A., Billington, C. K. Irani, C., Vorotnikov, A. V., Tkachuk, V. A., Penn, R. B., Krymskaya, V. P., and Panettieri, R. A., Jr. (2003) Cyclic AMP-mobilizing agents and glucocorticoids modulate human smooth muscle cell migration. Am. J. Respir. Cell Mol. Biol. 29, 19-27.
28. Longenecker, J. P., Kilty, L. A., and Johnson, L. K. (1984) Glucocorticoid inhibition of vascular smooth muscle cell proliferation: influence of homologous extracellular matrix and serum mitogens. J. Cell Biol. 98, 534-540.
29. Hadoke, P. W., Christy, C., Kotelevtsev, Y. V., Williams, B. C., Kenyon, C. J., Seckl, J. R., Mullins, J. J., and Walker, B. R. (2001) Endothelial cell dysfunction in mice after transgenic knockout of type 2, but not type 1, 11β-hydroxysteroid dehydrogenase. Circulation 104, 2832-2837.
30. Small, G. R., Hadoke, P. W., Sharif, I., Dover, A. R., Armour, D., Kenyon, C. J., Gray, G. A., and Walker, B. R. (2005) Preventing local regeneration of glucocorticoids by 11-hydroxysteroid dehydrogenase type 1 enhances angiogenesis. Proc. Natl. Acad. Sci. USA. 102, 12165-12170.
31. Ayaori, M., Sawada, S., Yonemura, A., Iwamoto, N., Ogura, M., Tanaka, N., Nakaya, K., Kusuhara, M., Nakamura, H., and Ohsuzu, F. (2006) Glucocorticoid receptor regulates ATP-binding cassette transporter-A1 expression and apolipoprotein-mediated cholesterol efflux from macrophages. Arterioscler. Thromb. Vasc. Biol. 26, 163-168.
32. Canalis, E. (1983) Effect of glucocorticoids on type I collagen synthesis, alkaline phosphatase activity, and deoxyribonucleic acid content in cultured rat calvariae. Endocrinology 112, 931-939.
33. Cutroneo, K. R., and Counts, D. F. (1975) Anti-inflammatory steroids and collagen metabolism: glucocorticoid-mediated alterations of prolyl hydroxylase activity and collagen synthesis. Mol. Pharmacol. 11, 632-639.
34. Holman, R. L., Mc, G. H. Jr., Strong, J. P., and Geer, J. C. (1958) Technics for studying atherosclerotic lesions. Lab. Invest. 7, 42-47.
35. Hadoke, P., Wainwright, C. L., Wadsworth, R. M., Butler, K., and Giddings, M. J. (1995) Characterization of the morphological and functional alterations in rabbit subclavian artery subjected to balloon angioplasty. Coron. Artery Dis. 6, 403-415.
36. Shiomi, M., Ito, T., Tsukada, T., Yata, T., Watanabe, Y., Tsujita, Y., Fukami, M., Fukushige, J., Hosokawa, T., and Tamura, A. (1995) Reduction of serum cholesterol levels alters lesional composition of atherosclerotic plaques. Effect of pravastatin sodium on atherosclerosis in mature WHHL rabbits. Arterioscler. Thromb. Vasc. Biol. 15, 1938-1944.
37. Williams, H., Johnson, J. L., Carson, K. G., and Jackson, C. L. (2002) Characteristics of intact and ruptured atherosclerotic plaques in brachiocephalic arteries of apolipoprotein E knockout mice. Arterioscler. Thromb. Vasc. Biol. 22, 788-792.
38. Kirkby, N. S., Low, L., Seckl, J. R., Walker, B. R., Webb, D. J., and Hadoke, P. W. Quantitative 3-dimensional imaging of murine neointimal and atherosclerotic lesions by optical projection tomography. PLoS One 6, e16906.
39. De Sousa Peixoto, R. A., Turban, S., Battle, J. H., Chapman, K. E., Seckl, J. R., and Morton, N. M. (2008) Preadipocyte 11β-hydroxysteroid dehydrogenase type 1 is a keto-reductase and contributes to diet-induced visceral obesity in vivo. Endocrinology 149, 1861-1868.
40. Harris, H. J., Kotelevtsev, Y., Mullins, J. J., Seckl, J. R., and Holmes, M. C. (2001) Intracellular regeneration of glucocorticoids by 11-hydroxysteroid dehydrogenase (11-HSD)-1 plays a key role in regulation of the hypothalamic-pituitary-adrenal axis: analysis of 11-HSD-1-deficient mice. Endocrinology 142, 114-120.
41. Rigamonti, E., Helin, L., Lestavel, S., Mutka, A. L., Lepore, M., Fontaine, C., Bouhlel, M. A., Bultel, S., Fruchart, J. C., Ikonen, E., Clavey, V., Staels, B., and Chinetti-Gbaguidi, G. (2005) Liver X receptor activation controls intracellular cholesterol trafficking and esterification in human macrophages. Circ. Res. 97, 682-689.
42. Combadiere, C., Potteaux, S., Rodero, M., Simon, T., Pezard, A., Esposito, B., Merval, R., Proudfoot, A., Tedgui, A., and Mallat, Z. (2008) Combined inhibition of CCL2, CX3CR1, and CCR5 abrogates Ly6C(hi) and Ly6C(lo) monocytosis and almost abolishes atherosclerosis in hypercholesterolemic mice. Circulation 117, 1649-1657.
43. Weber, C., Zernecke, A., and Libby, P. (2008) The multifaceted contributions of leukocyte subsets to atherosclerosis: lessons from mouse models. Nat. Rev. Immunol. 8, 802-815.
44. Tacke, F., Alvarez, D., Kaplan, T. J., Jakubzick, C., Spanbroek, R., Llodra, J., Garin, A., Liu, J., Mack, M., van Rooijen, N., Lira, S. A., Habenicht, A. J., and Randolph, G. J. (2007) Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J. Clin. Invest. 117, 185-194.
45. Swirski, F. K., Libby, P., Aikawa, E., Alcaide, P., Luscinskas, F. W., Weissleder, R., and Pittet, M. J. (2007) Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J. Clin. Invest. 117, 195-205.
46. Charo, I. F., and Taubman, M. B. (2004) Chemokines in the pathogenesis of vascular disease. Circ. Res. 95, 858-866.
47. Blankenberg, S., Barbaux, S., and Tiret, L. (2003) Adhesion molecules and atherosclerosis. Atherosclerosis 170, 191-203.
48. Meisler, N., Shull, S., Xie, R., Long, G. L., Absher, M., Connolly, J. P., and Cutroneo, K. R. (1995) Glucocorticoids coordinately regulate type I collagen pro alpha 1 promoter activity through both the glucocorticoid and transforming growth factor beta response elements: a novel mechanism of glucocorticoid regulation of eukaryotic genes. J. Cell. Biochem. 59, 376-388.
49. Deuchar, G. A., McLean, D., Hadoke, P. W., Brownstein, D. G., Webb, D. J., Mullins, J. J., Chapman, K., Seckl, J. R., and Kotelevtsev, Y. V. 11β-hydroxysteroid dehydrogenase type 2 deficiency accelerates atherogenesis and causes proinflammatory changes in the endothelium in apoe-/- mice. Endocrinology 152, 236-246.
50. Simoncini, T., Maffei, S., Basta, G., Barsacchi, G., Genazzani, A. R., Liao, J. K., and De Caterina, R. (2000) Estrogens and glucocorticoids inhibit endothelial vascular cell adhesion molecule- 1 expression by different transcriptional mechanisms. Circ. Res. 87, 19-25.
51. Cavalcanti, D. M., Lotufo, C. M., Borelli, P., Ferreira, Z. S., Markus, R. P., and Farsky, S. H. (2007) Endogenous glucocorticoids control neutrophil mobilization from bone marrow to blood and tissues in non-inflammatory conditions. Br. J. Pharmacol. 152, 1291-1300.
52. Curtiss, L. K. (2000) ApoE in atherosclerosis: a protein with multiple hats. Arterioscler. Thromb. Vasc. Biol. 20, 1852-1853.
53. Zhu, Y., Kodvawala, A., and Hui, D. Y. Apolipoprotein E inhibits Toll-like receptor (TLR)-3- and TLR-4-mediated macrophage activation through distinct mechanisms. Biochem. J. 428, 47-54.