A nitric oxide-dependent cross-talk between class i and III histone deacetylases accelerates skin repair

Journal of Biological Chemistry

Volumn 288, Issue 16, 2013, Pages 11004-11012

  Spallotta, Francesco ^a,i   Cencioni, Chiara ^a,i   Straino, Stefania ^b,j   Nanni, Simona ^c   Rosati, Jessica ^d   Artuso, Simona ^e   Manni, Isabella ^e   Colussi, Claudia ^d   Piaggio, Giulia ^e   Martelli, Fabio ^f   Valente, Sergio ^g   Mai, Antonello ^g   Capogrossi, Maurizio C ^b   Farsetti, Antonella ^h   Gaetano, Carlo ⁱ  

^a CENTRO CARDIOLOGICO MONZINO   (Italy)

^b LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

^c CATHOLIC UNIVERSITY   (Italy)

^d CASA SOLLIEVO DELLA SOFFERENZA HOSPITAL   (Italy)

^e REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^f IRCCS POLICLINICO SAN DONATO   (Italy)

^g SAPIENZA UNIVERSITY OF ROME   (Italy)

^h CNR   (Italy)

ⁱ GOETHE UNIVERSITY   (Germany)

^j Explora Srl   (Italy)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CLASS I; HISTONE DEACETYLASES; NO PRODUCTIONS; WOUND REPAIR;

REPAIR;

NITRIC OXIDE;

3 [4 [3 (3 FLUOROPHENYL) 3 OXO 1 PROPENYL] 1 METHYL 1H PYRROL 2 YL]ACRYLOHYDROXAMIC ACID; CYSTEINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENTINOSTAT; ENZYME ACTIVATOR; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 10; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE INHIBITOR; INHIBITOR OF TRICHOSTATIN A; MC 2562; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; RESVERATROL; SIRTINOL; SIRTUIN; SOMATOMEDIN C; TRICHOSTATIN A; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL STIMULATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DRUG EFFICACY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; KERATINOCYTE; MALE; MOLECULAR INTERACTION; MOUSE; NITROSYLATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; SKIN INJURY; TISSUE REGENERATION; TISSUE REPAIR; WOUND HEALING;

ANIMALS; CELL LINE, TRANSFORMED; ENZYME ACTIVATORS; ENZYME INHIBITORS; FIBROBLAST GROWTH FACTOR 10; GROUP III HISTONE DEACETYLASES; HISTONE DEACETYLASE 2; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MALE; MICE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; SIGNAL TRANSDUCTION; SKIN; WOUND HEALING;

EID: 84876580701     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.441816     Document Type: Article

References (28)

1. Illi, B., Colussi, C., Grasselli, A., Farsetti, A., Capogrossi, M. C., and Gaetano, C. (2009) NO sparks off chromatin. Tales of a multifaceted epigenetic regulator. Pharmacol. Ther. 123, 344-352.
2. Watson, P. M., and Riccio, A. (2009) Nitric oxide and histone deacetylases. A new relationship between old molecules. Commun. Integr. Biol. 2, 11-13.
3. Nott, A., Watson, P. M., Robinson, J. D., Crepaldi, L., and Riccio, A. (2008) S-Nitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature 455, 411-415.
4. Colussi, C., Mozzetta, C., Gurtner, A., Illi, B., Rosati, J., Straino, S., Ragone, G., Pescatori, M., Zaccagnini, G., Antonini, A., Minetti, G., Martelli, F., Piaggio, G., Gallinari, P., Steinkuhler, C., Steinkulher, C., Clementi, E., Dell'Aversana, C., Altucci, L., Mai, A., Capogrossi, M. C., Puri, P. L., and Gaetano, C. (2008) HDAC2 blockade by nitric oxide and histone deacetylase inhibitors reveals a common target in Duchenne muscular dystrophy treatment. Proc. Natl. Acad. Sci. U.S.A. 105, 19183-19187.
5. Illi, B., Dello Russo, C., Colussi, C., Rosati, J., Pallaoro, M., Spallotta, F., Rotili, D., Valente, S., Ragone, G., Martelli, F., Biglioli, P., Steinkuhler, C., Gallinari, P., Mai, A., Capogrossi, M. C., and Gaetano, C. (2008) Nitric oxide modulates chromatin folding in human endothelial cells via protein phosphatase 2A activation and class II histone deacetylases nuclear shuttling. Circ. Res. 102, 51-58.
6. Spallotta, F., Rosati, J., Straino, S., Nanni, S., Grasselli, A., Ambrosino, V., Rotili, D., Valente, S., Farsetti, A., Mai, A., Capogrossi, M. C., Gaetano, C., and Illi, B. (2010) Nitric oxide determines mesodermic differentiation of mouse embryonic stem cells by activating class IIa histone deacetylases. Potential therapeutic implications in a mouse model of hindlimb ischemia. Stem Cells 28, 431-442.
7. Chen, Z., Peng, I. C., Cui, X., Li, Y. S., Chien, S., and Shyy, J. Y. (2010) Shear stress, SIRT1, and vascular homeostasis. Proc. Natl. Acad. Sci. U.S.A. 107, 10268-10273.
8. Mattagajasingh, I., Kim, C. S., Naqvi, A., Yamamori, T., Hoffman, T. A., Jung, S. B., DeRicco, J., Kasuno, K., and Irani, K. (2007) SIRT1 promotes endothelium-dependent vascular relaxation by activating endothelial nitric oxide synthase. Proc. Natl. Acad. Sci. U.S.A. 104, 14855-14860.
9. Broughton, G., 2nd, Janis, J. E., and Attinger, C. E. (2006) The basic science of wound healing. Plast. Reconstr. Surg. 117, 12S-34S.
10. Soneja, A., Drews, M., and Malinski, T. (2005) Role of nitric oxide, nitroxidative and oxidative stress in wound healing. Pharmacol. Rep. 57, 108-119.
11. Isenberg, J. S., Ridnour, L. A., Espey, M. G., Wink, D. A., and Roberts, D. D. (2005) Nitric oxide in wound-healing. Microsurgery 25, 442-451.
12. Luo, J. D., and Chen, A. F. (2005) Nitric oxide.Anewly discovered function on wound healing. Acta Pharmacol. Sin. 26, 259-264.
13. Blander, G., Bhimavarapu, A., Mammone, T., Maes, D., Elliston, K., Reich, C., Matsui, M. S., Guarente, L., and Loureiro, J. J. (2009) SIRT1 promotes differentiation of normal human keratinocytes. J. Invest. Dermatol. 129, 41-49.
14. Dal Farra, C., and Domloge, N. (2006) SIRT1, the human homologue to SIR2, is expressed in human skin and in cultured keratinocytes fibroblasts and HaCaT cells; and its levels is closely related to stress and aging. J. Cosmet. Sci. 57, 187-188.
15. Mai, A., Valente, S., Meade, S., Carafa, V., Tardugno, M., Nebbioso, A., Galmozzi, A., Mitro, N., De Fabiani, E., Altucci, L., and Kazantsev, A. (2009) Study of 1, 4-dihydropyridine structural scaffold. Discovery of novel sirtuin activators and inhibitors. J. Med. Chem. 52, 5496-5504.
16. Bashmakov, Y. K., Assaad-Khalil, S., and Petyaev, I. M. (2011) Resveratrol may be beneficial in treatment of diabetic foot syndrome. Med. Hypotheses 77, 364-367.
17. Khanna, S., Venojarvi, M., Roy, S., Sharma, N., Trikha, P., Bagchi, D., Bagchi, M., and Sen, C. K. (2002) Dermal wound healing properties of redox-active grape seed proanthocyanidins. Free Radic. Biol. Med. 33, 1089-1096.
18. Goeman, F., Manni, I., Artuso, S., Ramachandran, B., Toietta, G., Bossi, G., Rando, G., Cencioni, C., Germoni, S., Straino, S., Capogrossi, M. C., Bacchetti, S., Maggi, A., Sacchi, A., Ciana, P., and Piaggio, G. (2012) Molecular imaging of nuclear factor-Y transcriptional activity maps proliferation sites in live animals. Mol. Biol. Cell 23, 1467-1474.
19. Schoop, V. M., Mirancea, N., and Fusenig, N. E. (1999) Epidermal organization and differentiation of HaCaT keratinocytes in organotypic coculture with human dermal fibroblasts. J. Invest. Dermatol. 112, 343-353.
20. Nanni, S., Benvenuti, V., Grasselli, A., Priolo, C., Aiello, A., Mattiussi, S., Colussi, C., Lirangi, V., Illi, B., D'Eletto, M., Cianciulli, A. M., Gallucci, M., De Carli, P., Sentinelli, S., Mottolese, M., Carlini, P., Strigari, L., Finn, S., Mueller, E., Arcangeli, G., Gaetano, C., Capogrossi, M. C., Donnorso, R. P., Bacchetti, S., Sacchi, A., Pontecorvi, A., Loda, M., and Farsetti, A. (2009) Endothelial NOS, estrogen receptor, and HIFs cooperate in the activation of a prognostic transcriptional pattern in aggressive human prostate cancer. J. Clin. Invest. 119, 1093-1108.
21. Mai, A., Massa, S., Pezzi, R., Simeoni, S., Rotili, D., Nebbioso, A., Scognamiglio, A., Altucci, L., Loidl, P., and Brosch, G. (2005) Class II (IIa)-selective histone deacetylase inhibitors. 1. Synthesis and biological evaluation of novel (aryloxopropenyl)pyrrolyl hydroxyamides. J. Med. Chem. 48, 3344-3353.
22. Vaquero, A., Sternglanz, R., and Reinberg, D. (2007) NAD+-dependent deacetylation of H4 lysine 16 by class III HDACs. Oncogene 26, 5505-5520.
23. Fitzgerald O'Connor, E. J., Badshah, I. I., Addae, L. Y., Kundasamy, P., Thanabalasingam, S., Abioye, D., Soldin, M., and Shaw, T. J. (2012) Histone deacetylase 2 is upregulated in normal and keloid scars. J. Invest. Dermatol. 132, 1293-1296.
24. Marchese, C., Felici, A., Visco, V., Lucania, G., Igarashi, M., Picardo, M., Frati, L., and Torrisi, M. R. (2001) Fibroblast growth factor 10 induces proliferation and differentiation of human primary cultured keratinocytes. J. Invest. Dermatol. 116, 623-628.
25. Rafehi, H., El-Osta, A., and Karagiannis, T. C. (2011) Genetic and epigenetic events in diabetic wound healing. Int. Wound J. 8, 12-21.
26. Shaw, T., and Martin, P. (2009) Epigenetic reprogramming during wound healing. Loss of polycomb-mediated silencing may enable upregulation of repair genes. EMBO Rep. 10, 881-886.
27. Colussi, C., Scopece, A., Vitale, S., Spallotta, F., Mattiussi, S., Rosati, J., Illi, B., Mai, A., Castellano, S., Sbardella, G., Farsetti, A., Capogrossi, M. C., and Gaetano, C. (2012) P300/CBP associated factor regulates nitroglycerindependent arterial relaxation by N(ε)-lysine acetylation of contractile proteins. Arterioscler. Thromb. Vasc. Biol. 32, 2435-2443.
28. Park, S. J., Ahmad, F., Philp, A., Baar, K., Williams, T., Luo, H., Ke, H., Rehmann, H., Taussig, R., Brown, A. L., Kim, M. K., Beaven, M. A., Burgin, A. B., Manganiello, V., and Chung, J. H. (2012) Resveratrol ameliorates aging-related metabolic phenotypes by inhibiting cAMP phosphodiesterases. Cell 148, 421-433.