Skip to main content
SpringerLink
Log in

trans-Chalcone, a flavonoid precursor, inhibits UV-induced skin inflammation and oxidative stress in mice by targeting NADPH oxidase and cytokine production

  • Paper
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

trans-Chalcone is a plant flavonoid precursor, which lacks broad investigation on its biological activity in inflammatory processes. In the present study, anti-inflammatory and antioxidant mechanisms of systemic administration with trans-chalcone, a flavonoid precursor, on ultraviolet (UV) irradiation-induced skin inflammation and oxidative stress in hairless mice were investigated by the following parameters: skin edema, myeloperoxidase activity (neutrophil marker), matrix metalloproteinase-9 activity, reduced glutathione levels, catalase activity, lipid peroxidation products, superoxide anion production, gp91phox (NADPH oxidase subunit) mRNA expression by quantitative PCR and cytokine production by ELISA. Systemic treatment with trans-chalcone inhibited skin inflammation by reducing skin edema and neutrophil recruitment, and also inhibited matrix metalloproteinase-9 activity. trans-Chalcone also inhibited oxidative stress, gp91phox mRNA expression, and the production of a wide range of pro-inflammatory cytokines, while it did not affect anti-inflammatory cytokines induced by UV irradiation. However, trans-chalcone did not prevent oxidative stress in vitro, suggesting that its in vivo effect is more related to anti-inflammatory properties rather than a direct antioxidant effect. In conclusion, treatment with trans-chalcone inhibited UV-induced skin inflammation resulting in oxidative stress inhibition in vivo. Therefore, systemic supplementation with this compound may represent an important therapeutic approach in inflammatory skin diseases induced by UV irradiation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. A. Svobodová, J. Psotová and D. Walterová, Biomed. Pap. Med. Fac. Univ. Palacky. Olomouc. Czech. Repub., 2003, 147, 137–145.

    Article  PubMed  Google Scholar 

  2. M. Yaar and B. A. Gilchrest, Br. J. Dermatol., 2007, 157, 874–887.

    Article  CAS  PubMed  Google Scholar 

  3. F. T. Vicentini, T. He, Y. Shao, M. J. Fonseca, W. A. Verri, Jr., G. J. Fisher and Y. Xu, J. Dermatol. Sci., 2011, 61, 162–168.

    Article  CAS  PubMed  Google Scholar 

  4. J. Anrather, G. Racchumi and C. Iadecola, J. Biol. Chem., 2006, 281, 5657–5667.

    Article  CAS  PubMed  Google Scholar 

  5. M. Valko, D. Leibfritz, J. Moncol, M. T. D. Cronin, M. Mazur and J. Telser, Int. J. Biochem. Cell Biol., 2007, 39, 44–84.

    Article  CAS  PubMed  Google Scholar 

  6. G. M. Halliday and J. G. Lyons, Photochem. Photobiol., 2008, 84, 272–283.

    Article  CAS  PubMed  Google Scholar 

  7. W. A. Verri, Jr., F. T. M. C. Vicentini, M. M. Baracat, S. R. Georgetti, R. D. R. Cardoso, T. M. Cunha, S. H. Ferreira, F. Q. Cunha, M. J. V. Fonseca and R. Casagrande, Stud. Nat. Prod. Chem., 2012, 36, 297–330.

    Article  CAS  Google Scholar 

  8. J. A. Nichols and S. K. Katiyar, Arch. Dermatol. Res., 2010, 302, 71–83.

    Article  CAS  PubMed  Google Scholar 

  9. M. Z. Campanini, F. A. Pinho-Ribeiro, A. L. Ivan, V. S. Ferreira, F. M. Vilela, F. T. Vicentini, R. M. Martinez, A. C. Zarpelon, M. J. Fonseca, T. J. Faria, M. M. Baracat, W. A. Verri, Jr., S. R. Georgetti and R. Casagrande, J. Photochem. Photobiol., B, 2013, 127, 153–160.

    Article  CAS  Google Scholar 

  10. R. Casagrande, S. R. Georgetti, W. A. Verri, Jr., D. J. Dorta, A. C. dos Santos and M. J. Fonseca, J. Photochem. Photobiol., B, 2006, 84, 21–27.

    Article  CAS  Google Scholar 

  11. R. M. Martinez, F. A. Pinho-Ribeiro, V. S. Steffen, C. V. Caviglione, J. A. Vignoli, M. M. Baracat, S. R. Georgetti, W. A. Verri, Jr. and R. Casagrande, J. Photochem. Photobiol., B, 2015, 148, 145–153.

    Article  CAS  Google Scholar 

  12. R. M. Martinez, F. A. Pinho-Ribeiro, V. S. Steffen, C. V. Caviglione, J. A. Vignoli, D. S. Barbosa, M. M. Baracat, S. R. Georgetti, W. A. Verri, Jr. and R. Casagrande, J. Nat. Prod., 2015, 78, 1647–1655.

    Article  CAS  PubMed  Google Scholar 

  13. R. M. Martinez, F. A. Pinho-Ribeiro, V. S. Steffen, T. C. C. Silva, C. V. Caviglione, C. Bottura, M. J. V. Fonseca, F. T. M. C. Vicentini, J. A. Vignoli, M. M. Baracat, S. R. Georgetti, W. A. Verri, Jr. and R. Casagrande, PLoS One, 2016, 11, e0146296.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. R. M. Martinez, F. A. Pinho-Ribeiro, V. S. Steffen, C. V. Caviglione, D. Pala, M. M. Baracat, S. R. Georgetti, W. A. Verri, Jr. and R. Casagrande, Photochem. Photobiol. Sci., 2016, 15, 554–563.

    Article  CAS  PubMed  Google Scholar 

  15. A. Filip, S. Clichici, D. Daicoviciu, M. Adriana, I. D. Postescu, M. Perde-Schrepler and D. Olteanu, Exp. Oncol., 2009, 31, 9–15.

    CAS  PubMed  Google Scholar 

  16. A. T. Fujimura, R. M. Martinez, F. A. Pinho-Ribeiro, A. M. Lopes Dias da Silva, M. M. Baracat, S. R. Georgetti, W. A. Verri, Jr., M. Chorilli and R. Casagrande, J. Nat. Prod., 2016, 79, 1329–1338.

    Article  CAS  PubMed  Google Scholar 

  17. P. G. Pietta, J. Nat. Prod., 2000, 63, 1035–1042.

    Article  CAS  PubMed  Google Scholar 

  18. G. Duthie and A. Crozier, Curr. Opin. Clin. Nutr. Metab. Care, 2000, 3, 447–451.

    Article  CAS  PubMed  Google Scholar 

  19. N. K. Sahu, S. S. Balbhadra, J. Choudhary and D. V. Kohli, Curr. Med. Chem., 2012, 19, 209–225.

    Article  CAS  PubMed  Google Scholar 

  20. G. Silva, M. Marins, A. L. Fachin, S.-H. Lee and S. J. Baek, Mol. Carcinog., 2016, 55, 1438–1448.

    Article  CAS  PubMed  Google Scholar 

  21. M. Sikander, S. Malik, D. Yadav, S. Biswas, D. P. Katare and S. K. Jain, Asian Pac. J. Cancer Prev., 2011, 12, 2513–2516.

    PubMed  Google Scholar 

  22. F. Lamoke, M. Labazi, A. Montemari, G. Parisi, M. Varano and M. Bartoli, Exp. Eye Res., 2011, 93, 350–354.

    Article  CAS  PubMed  Google Scholar 

  23. A. L. Ivan, M. Z. Campanini, R. M. Martinez, V. S. Ferreira, V. S. Steffen, F. T. Vicentini, F. M. Vilela, F. S. Martins, A. C. Zarpelon, T. M. Cunha, M. J. Fonseca, M. M. Baracat, S. R. Georgetti, W. A. Verri, Jr. and R. Casagrande, J. Photochem. Photobiol., B, 2014, 138, 124–133.

    Article  CAS  Google Scholar 

  24. R. M. Martinez, A. C. Zarpelon, V. V. M. Zimermann, S. R. Georgetti, M. M. Baracat, M. J. V. Fonseca, F. T. M. C. Vicentini, I. C. Moreira, C. C. Andrei, W. A. Verri, Jr. and R. Casagrande, Rev. Bras. Farmacogn., 2012, 22, 587–597.

    Article  CAS  Google Scholar 

  25. N. A. Maioli, A. C. Zarpelon, S. S. Mizokami, C. Calixto-Campos, C. F. S. Guazelli, M. S. N. Hohmann, F. A. Pinho-Ribeiro, T. T. Carvalho, M. F. Manchope, C. R. Ferraz, R. Casagrande and W. A. Verri, Jr., Braz. J. Med. Biol. Res., 2015, 48, 321–331.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Y. Deng, A. Ediriwickrema, F. Yang, J. Lewis, M. Girardi and W. M. Saltzman, Nat. Mater., 2015, 14, 1278–1285.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. A. Schwarz, R. Bhardwaj, Y. Aragane, K. Mahnke, H. Riemann, D. Metze, T. A. Luger, T. Schwarz, J. Invest. Dermatol., 1995, 104, 922–927.

    Article  CAS  PubMed  Google Scholar 

  28. S. Mouret, J. Wartelle, M. Batal, S. Emorine, M. Bertoni, T. Poyot, C. Clery-Barraud, N. El Bakdouri, A. Peinnequin, T. Douki and I. Boudry, Toxicol. Lett., 2015, 232, 68–78.

    Article  CAS  PubMed  Google Scholar 

  29. R. L. Prior, X. Wu, K. Schaich, J. Agric. Food Chem., 2005, 53, 4290–4302.

    Article  CAS  PubMed  Google Scholar 

  30. C. Oresajo, S. Pillai, M. Manco, M. Yatskayer and D. McDaniel, Dermatol. Ther., 2012, 25, 252–259.

    Article  PubMed  Google Scholar 

  31. R. Casagrande, S. R. Georgetti, W. A. Verri, Jr. and J. R. Jabor, A. C. Santos, M. J. Fonseca, AAPS PharmSciTech, 2006, 7, E10.

    Article  PubMed  Google Scholar 

  32. R. Casagrande, S. R. Georgetti, W. A. Verri, Jr., M. F. Borin, R. F. Lopez and M. J. Fonseca, Int. J. Pharm., 2007, 328, 183–190.

    Article  CAS  PubMed  Google Scholar 

  33. F. Rijken and C. A. Bruijnzeel-Koomen, Clin. Pharmacol. Ther., 2011, 89, 120–124.

    Article  CAS  PubMed  Google Scholar 

  34. V. Fattori, F. A. Amaral and W. A. Verri, Jr., Pharmacol. Res., 2016, 112, 84–98.

    Article  CAS  PubMed  Google Scholar 

  35. H. Singh, S. Sidhu, K. Chopra and M. U. Khan, Can. J. Physiol. Pharmacol., 2016, 1–9.

    Google Scholar 

  36. B. K. Pilcher, M. Wang, X. J. Qin, W. C. Parks, R. M. Senior and H. G. Welgus, Ann. N. Y. Acad. Sci., 1999, 878, 12–24.

    Article  CAS  PubMed  Google Scholar 

  37. A. C. A. Devillers, A. W. van Toorenenbergen, G. J. Klein Heerenbrink, P. G. H. Muldert and A. P. Oranje, Clin. Exp. Dermatol., 2007, 32, 311–313.

    Article  CAS  PubMed  Google Scholar 

  38. A. John and G. Tuszynski, Pathol. Oncol. Res., 2001, 7, 14–23.

    Article  CAS  PubMed  Google Scholar 

  39. H. Y. Song, S. M. Ju, A. R. Goh, D. J. Kwon, S. Y. Choi and J. Park, BMB Rep., 2011, 44, 462–467.

    Article  CAS  PubMed  Google Scholar 

  40. S. H. Lin, Y. W. Shih, Mol. Cell. Biochem., 2014, 391, 47–58.

    Article  CAS  PubMed  Google Scholar 

  41. M. Meloni and J. F. Nicolay, Toxicol. In Vitro, 2003, 17, 609–613.

    Article  CAS  PubMed  Google Scholar 

  42. G. J. Fisher, Z. Q. Wang, S. C. Datta, J. Varani, S. Kang and J. J. Voorhees, N. Engl. J. Med., 1997, 337, 1419–1428.

    Article  CAS  PubMed  Google Scholar 

  43. T. M. Bray and C. G. Taylor, Can. J. Physiol. Pharmacol., 1993, 71, 746–751.

    Article  CAS  PubMed  Google Scholar 

  44. C. F. Ng, F. Q. Schafer, G. R. Buettner and V. G. J. Rodgers, Free Radical Res., 2007, 41, 1201–1211.

    Article  CAS  Google Scholar 

  45. L. Karkhaneh, P. Yaghmaei, K. Parivar, M. Sadeghizadeh and A. Ebrahim-Habibi, Pharmacol. Rep., 2016, 68, 720–727.

    Article  CAS  PubMed  Google Scholar 

  46. B. C. Pence, M. F. Naylor, J. Invest. Dermatol., 1990, 95, 213–216.

    Article  CAS  PubMed  Google Scholar 

  47. N. J. Sullivan, K. L. Tober, E. M. Burns, J. S. Schick, J. A. Riggenbach, T. A. Mace, M. A. Bill, G. S. Young, T. M. Oberyszyn and G. B. Lesinski, J. Invest. Dermatol., 2012, 132, 695–702.

    Article  CAS  PubMed  Google Scholar 

  48. A. Gupta, B. Butts, K. A. Kwei, K. Dvorakova, S. P. Stratton, M. M. Briehl and G. T. Bowden, Cancer Lett., 2001, 173, 115–125.

    Article  CAS  PubMed  Google Scholar 

  49. A. W. Girotti, J. Photochem. Photobiol., B, 2001, 63, 103–113.

    Article  CAS  Google Scholar 

  50. J. M. Gutteridge, FEBS Lett., 1986, 201, 291–295.

    Article  CAS  PubMed  Google Scholar 

  51. Y. Fang, X.-H. Hu, Z.-G. Jia, M.-H. Xu, Z.-Y. Guo and F.-H. Gao, Australas. J. Dermatol., 2012, 53, 172–180.

    Article  PubMed  Google Scholar 

  52. C. Nathan, M. U. Shiloh, Proc. Natl. Acad. Sci. U. S. A., 2000, 97, 8841–8848.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. H. Hattori, K. K. Subramanian, J. Sakai, Y. Jia, Y. Li, T. F. Porter, F. Loison, B. Sarraj, A. Kasorn, H. Jo, C. Blanchard, D. Zirkle, D. McDonald, S. Y. Pai, C. N. Serhan and H. R. Luo, Proc. Natl. Acad. Sci. U. S. A., 2010, 107, 3546–3551.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. K. Schulze-Osthoff, M. K. Bauer, M. Vogt and S. Wesselborg, Int. J. Vitam. Nutr. Res., 1997, 67, 336–342.

    CAS  PubMed  Google Scholar 

  55. Y. Mutou, Y. Ibuki and S. Kojima, Photodermatol., Photoimmunol. Photomed., 2007, 23, 135–144.

    Article  CAS  Google Scholar 

  56. J. S. Lou, X. E. Chen, Y. Zhang, Z. W. Gao, T. P. Chen, G. Q. Zhang and C. Ji, Exp. Ther. Med., 2013, 6, 1022–1028.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. M. Yokogawa, M. Takaishi, K. Nakajima, R. Kamijima and J. Digiovanni, S. Sano, Mol. Carcinog., 2013, 52, 760–769.

    Article  CAS  PubMed  Google Scholar 

  58. Z. W. Sun, E. Hwang, H. J. Lee, T. Y. Lee, H. G. Song, S. Y. Park, H. S. Shin, D. G. Lee and T. H. Yi, J. Nat. Med., 2015, 69, 22–34.

    Article  CAS  PubMed  Google Scholar 

  59. K. Hiramoto, H. Kobayashi, Y. Yamate, M. Ishii and E. F. Sato, Exp. Dermatol., 2012, 21, 911–914.

    Article  CAS  PubMed  Google Scholar 

  60. I. Strickland, L. E. Rhodes, B. F. Flanagan and P. S. Friedmann, J. Invest. Dermatol., 1997, 108, 763–768.

    Article  CAS  PubMed  Google Scholar 

  61. W. W. Lin, M. Karin, J. Clin. Invest., 2007, 117, 1175–1183.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. W. A. Verri, Jr., F. O. Souto, S. M. Vieira, S. C. Almeida, S. Y. Fukada, D. Xu, J. C. Alves-Filho, T. M. Cunha, A. T. Guerrero, R. B. Mattos-Guimaraes, F. R. Oliveira, M. M. Teixeira, J. S. Silva, I. B. McInnes, S. H. Ferreira, P. Louzada-Junior, F. Y. Liew and F. Q. Cunha, Ann. Rheum. Dis., 2010, 69, 1697–1703.

    Article  CAS  PubMed  Google Scholar 

  63. T. T. Carvalho, S. M. Borghi, F. A. Pinho-Ribeiro, S. S. Mizokami, T. M. Cunha, S. H. Ferreira, F. Q. Cunha, R. Casagrande and W. A. Verri, Jr., Eur. J. Pharmacol., 2015, 749, 62–72.

    Article  CAS  PubMed  Google Scholar 

  64. W. A. Verri, Jr., R. O. Molina, I. R. S. Schivo, T. M. Cunha, C. A. Parada, S. Poole, S. H. Ferreira and F. Q. Cunha, J. Pharmacol. Exp. Ther., 2005, 315, 609–615.

    Article  CAS  PubMed  Google Scholar 

  65. A. N. J. McKenzie, H. Spits and G. Eberl, Immunity, 2014, 41, 366–374.

    Article  CAS  PubMed  Google Scholar 

  66. L. Cosmi, L. Maggi, V. Santarlasci, F. Liotta and F. Annunziato, Cytometry, Part A, 2014, 85, 36–42.

    Article  CAS  Google Scholar 

  67. M. Peiser, Clin. Dev. Immunol., 2013, 2013, 261037.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. I. Striz, E. Brabcova, L. Kolesar and A. Sekerkova, Clin. Sci., 2014, 126, 593–612.

    Article  CAS  Google Scholar 

  69. A. M. Lewis, S. Varghese, H. Xu and H. R. Alexander, J. Transl. Med., 2006, 4, 48.

    Article  PubMed  PubMed Central  Google Scholar 

  70. S.-C. Han, D.-H. Koo, N.-J. Kang, W.-J. Yoon, G.-J. Kang, H.-K. Kang and E.-S. Yoo, J. Invest. Dermatol., 2014, 135, 1556–1564.

    Article  PubMed  CAS  Google Scholar 

  71. Y. Yamazaki, Y. Kawano and U. Nagashima, J. Comput. Chem., Jpn, 2012, 11, 159–163.

    Article  CAS  Google Scholar 

  72. T. C. Theoharides, K. D. Alysandratos, A. Angelidou, D. A. Delivanis, N. Sismanopoulos, B. Zhang, S. Asadi, M. Vasiadi, Z. Weng, A. Miniati and D. Kalogeromitros, Biochim. Biophys. Acta, 2012, 1822, 21–33.

    Article  CAS  PubMed  Google Scholar 

  73. V. R. Yadav, S. Prasad, B. Sung and B. B. Aggarwal, Int. Immunopharmacol., 2011, 11, 295–309.

    Article  CAS  PubMed  Google Scholar 

  74. K. Zenger, S. Agnolet, B. Schneider and B. Kraus, J. Agric. Food Chem., 2015, 63, 6376–6385.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departamento de Ciências Farmacêuticas, Universidade Estadual de Londrina-UEL, Avenida Robert Koch, 60, Hospital Universitário, 86038-350, Londrina, Paraná, Brasil

    Renata M. Martinez, Vinicius S. Steffen, Carla V. Caviglione, Carolina Bottura, Marcela M. Baracat, Sandra R. Georgetti & Rubia Casagrande

  2. Departamento de Patologia, Universidade Estadual de Londrina-UEL, Rodovia Celso Garcia Cid, Km 380, PR445, Cx. Postal 10.011, 86057-970, Londrina, Paraná, Brasil

    Felipe A. Pinho-Ribeiro, Victor Fattori, Allan J. C. Bussmann & Waldiceu A. Verri Jr

  3. Departamento de Ciências Farmacêuticas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto-USP, Av. do Café s/n, 14049-903, Ribeirão Preto, São Paulo, Brazil

    Maria J. V. Fonseca

  4. Departamento de Bioquímica e Biotecnologia, Universidade Estadual de Londrina-UEL, Rodovia Celso Garcia Cid, Km 380, PR445, Cx. Postal 10.011, 86057-970, Londrina, Paraná, Brasil

    Josiane A. Vignoli

Authors
  1. Renata M. Martinez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Felipe A. Pinho-Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vinicius S. Steffen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carla V. Caviglione
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Victor Fattori
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Allan J. C. Bussmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Carolina Bottura
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maria J. V. Fonseca
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Josiane A. Vignoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Marcela M. Baracat
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Sandra R. Georgetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Waldiceu A. Verri Jr
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Rubia Casagrande
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rubia Casagrande.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martinez, R.M., Pinho-Ribeiro, F.A., Steffen, V.S. et al. trans-Chalcone, a flavonoid precursor, inhibits UV-induced skin inflammation and oxidative stress in mice by targeting NADPH oxidase and cytokine production. Photochem Photobiol Sci 16, 1162–1173 (2017). https://doi.org/10.1039/c6pp00442c

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c6pp00442c

Search

Navigation