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Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 9703609, 17 pages
https://doi.org/10.1155/2017/9703609
Research Article

Fish Scale Collagen Peptides Protect against CoCl2/TNF-α-Induced Cytotoxicity and Inflammation via Inhibition of ROS, MAPK, and NF-κB Pathways in HaCaT Cells

1Department of Anatomy, Pusan National University School of Medicine, Yangsan, Gyeongsangnam-do 50612, Republic of Korea
2Pioneer Research Center, Suwon 16499, Republic of Korea
3Department of Mechanical Engineering, Korea Polytechnic University, Siheung 15073, Republic of Korea
4Kyungpook National University, Daegu 41566, Republic of Korea
5Department of Pharmacology, Ajou University School of Medicine, Suwon 16499, Republic of Korea

Correspondence should be addressed to Sik Yoon; rk.ca.nasup@nooykis

Received 24 January 2017; Revised 20 March 2017; Accepted 26 April 2017; Published 22 June 2017

Academic Editor: Giuseppe Filomeni

Copyright © 2017 Fazli Subhan et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. Coman, N. R. Blickenstaff, and H. I. Maibach, “Skin and the environment,” Reviews on Environmental Health, vol. 29, no. 3, p. 143, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. J. D. Bos and M. L. Kapsenberg, “The skin immune system: progress in cutaneous biology,” Immunology Today, vol. 14, no. 2, pp. 75–78, 1993. View at Publisher · View at Google Scholar · View at Scopus
  3. J. H. Kim, Z. W. Jin, G. Murakami, and B. H. Cho, “Characterization of mesenchymal cells beneath cornification of the fetal epithelium and epidermis at the face: an immunohistochemical study using human fetal specimens,” Anatomy and Cell Biology, vol. 49, no. 1, pp. 50–60, 2016. View at Publisher · View at Google Scholar · View at Scopus
  4. D. R. Bickers and M. Athar, “Oxidative stress in the pathogenesis of skin disease,” The Journal of Investigative Dermatology, vol. 126, no. 12, pp. 2565–2575, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. R. T. Narendhirakannan and M. A. Hannah, “Oxidative stress and skin cancer: an overview,” Indian Journal of Clinical Biochemistry, vol. 28, no. 2, pp. 110–115, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Y. Kim, Y. Y. Lim, H. M. Kim, Y. M. Park, H. Kang, and B. J. Kim, “Synergistic inhibition of tumor necrosis factor-alpha-stimulated pro-inflammatory cytokine expression in HaCaT cells by a combination of rapamycin and mycophenolic acid,” Annals of Dermatology, vol. 27, no. 1, pp. 32–39, 2015. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Kobielak and K. Boddupally, “Junctions and inflammation in the skin,” Cell Communication & Adhesion, vol. 21, no. 3, pp. 141–147, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. Y. H. Choi, G. H. Yan, O. H. Chai, and C. H. Song, “Inhibitory effects of curcumin on passive cutaneous anaphylactoid response and compound 48/80-induced mast cell activation,” Anatomy and Cell Biology, vol. 43, no. 1, pp. 36–43, 2010. View at Publisher · View at Google Scholar
  9. S. Kumari and M. Pasparakis, “Epithelial cell death and inflammation in skin,” Current Topics in Microbiology and Immunology, vol. 2015, pp. 1–17, 2015. View at Publisher · View at Google Scholar
  10. T. A. Mustoe, K. O’Shaughnessy, and O. Kloeters, “Chronic wound pathogenesis and current treatment strategies: a unifying hypothesis,” Plastic and Reconstructive Surgery, vol. 117, no. 7, pp. 35S–41S, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. C. Yang, H. Ling, M. Zhang et al., “Oxidative stress mediates chemical hypoxia-induced injury and inflammation by activating NF-κb-COX-2 pathway in HaCaT cells,” Molecules and Cells, vol. 6, no. 6, pp. 531–538, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. K. Watanabe, T. Kawamori, S. Nakatsugi, and K. Wakabayashi, “COX-2 and iNOS, good targets for chemoprevention of colon cancer,” Biofactors, vol. 12, no. 1–4, pp. 129–133, 2002. View at Publisher · View at Google Scholar
  13. J. K. Wang, G. M. Xiong, B. Luo et al., “Surface modification of PVDF using non-mammalian sources of collagen for enhancement of endothelial cell functionality,” Journal of Materials Science. Materials in Medicine, vol. 27, no. 3, p. 45, 2016. View at Publisher · View at Google Scholar · View at Scopus
  14. C. Liu, Y. Xue, and J. Sun, “Hydrolyzed fish collagen inhibits inflammatory cytokines secretion in lipopolysaccharide-induced HUVECs,” Advances in Materials Research, vol. 1025-1026, pp. 570–573, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. K. Yamamoto, K. Igawa, K. Sugimoto et al., “Biological safety of fish (tilapia) collagen,” BioMed Research International, vol. 2014, Article ID 630757, 9 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. L. Wang, X. X. An, F. M. Yang, Z. H. Xin, L. Y. Zhao, and Q. H. Hu, “Isolation and characterisation of collagens from the skin, scale and bone of deep-sea redfish (Sebastes mentella),” Food Chemistry, vol. 108, no. 2, pp. 616–623, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. R. C. Cheung, T. B. Ng, and J. H. Wong, “Marine peptides: bioactivities and applications,” Marine Drugs, vol. 13, no. 7, pp. 4006–4043, 2015. View at Publisher · View at Google Scholar · View at Scopus
  18. F. Zhang, Z. Wang, and S. Xu, “Macroporous resin purification of grass carp fish (Ctenopharyngodon idella) scale peptides with in vitro angiotensin-I converting enzyme (ACE) inhibitory ability,” Food Chemistry, vol. 117, no. 3, pp. 387–392, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Asserin, E. Lati, T. Shioya, and J. Prawitt, “The effect of oral collagen peptide supplementation on skin moisture and the dermal collagen network,” Journal of Cosmetic Dermatology, vol. 14, no. 4, pp. 291–301, 2015. View at Publisher · View at Google Scholar · View at Scopus
  20. H. Ohara, H. Iida, K. Ito, Y. Takeuchi, and Y. Nomura, “Effects of pro-Hyp, a collagen hydrolysate-derived peptide, on hyaluronic acid synthesis using in vitro cultured synovium cells and oral ingestion of collagen hydrolysates in a guinea pig model of osteoarthritis,” Bioscience, Biotechnology, and Biochemistry, vol. 74, no. 10, pp. 2096–2099, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. Z. Zhang, J. Wang, Y. Ding, X. Dai, and Y. Li, “Oral administration of marine collagen peptides from chum Salmon skin enhances cutaneous wound healing and angiogenesis in rats,” Journal of the Science of Food and Agriculture, vol. 91, no. 12, pp. 2173–2179, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. C. Liu and J. Sun, “Potential application of hydrolyzed fish collagen for inducing the multidirectional differentiation of rat bone marrow mesenchymal stem cells,” Biomacromolecules, vol. 15, no. 1, pp. 436–443, 2015. View at Publisher · View at Google Scholar · View at Scopus
  23. C. H. Ding, Q. Li, Z. Y. Xiong, A. W. Zhou, G. Jones, and S. Y. Xu, “Oral administration of type II collagen suppresses pro-inflammatory mediator production by synoviocytes in rats with adjuvant arthritis,” Clinical and Experimental Immunology, vol. 132, no. 3, pp. 416–423, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. W. Zou, M. Yan, W. Xu et al., “Cobalt chloride induces PC12 cells apoptosis through reactive oxygen species and accompanied by AP-1 activation,” Journal of Neuroscience Research, vol. 64, no. 6, pp. 646–653, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. G. Schmalz, H. Schweikl, and K. A. Hiller, “Release of prostaglandin E2, IL-6 and IL-8 from human oral epithelial culture models after exposure to compounds of dental materials,” European Journal of Oral Sciences, vol. 108, no. 5, pp. 442–448, 2000. View at Publisher · View at Google Scholar
  26. Y. Okayama, “Oxidative stress in allergic and inflammatory skin diseases,” Current Drug Targets-Inflammation & Allergy, vol. 4, no. 4, pp. 517–519, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Aleman and O. Martinez-Alvarez, “Marine collagen as a source of bioactive molecules. A Review,” Natural Products Journal, vol. 3, no. 2, pp. 105–114, 2013. View at Publisher · View at Google Scholar
  28. E. Mendis, N. Rajapakse, H. G. Byun, and S. K. Kim, “Investigation of jumbo squid (Dosidicus gigas) skin gelatin peptides for their in vitro antioxidant effects,” Life Sciences, vol. 77, no. 17, pp. 2166–2178, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. S. K. Kim, Y. T. Kim, H. G. Byun, K. S. Nam, D. S. Joo, and F. Shahidi, “Isolation and characterization of antioxidative peptides from gelatin hydrolysate of Alaska,” Journal of Agricultural and Food Chemistry, vol. 49, no. 4, pp. 1984–1989, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. D. H. Ngo, B. Ryu, T. S. Vo, S. W. A. Himaya, I. Wijesekara, and S. K. Kim, “Free radical scavenging and angiotensin-I converting enzyme inhibitory peptides from Pacific cod (Gadus macrocephalus) skin gelatin. International Journal of Biological Macromolecules,” International Journal of Biological Macromolecules, vol. 49, no. 5, pp. 1110–1116, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. S. W. A. Himaya, D. H. Ngo, B. Ryu, and S. K. Kim, “An active peptide purified from gastrointestinal enzyme hydrolysate of Pacific cod skin gelatine attenuates angiotensin-1 converting enzyme (ACE)activity and cellular oxidative stress,” Food Chemistry, vol. 132, no. 4, pp. 1872–1882, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. D. P. Mohanty, S. Mohapatra, S. Misra, and P. S. Sahu, “Milk derived bioactive peptides and their impact on human health - a review,” Saudi Journal of Biological Sciences, vol. 23, no. 5, pp. 577–583, 2016. View at Publisher · View at Google Scholar · View at Scopus
  33. N. Ito, S. Fukushima, A. Hasegawa, M. Shibata, and T. Ogiso, “Carcinogenicity of butylated hydroxyanisole in F344 rats,” Journal of the National Cancer Institute, vol. 70, no. 2, pp. 343–347, 1983. View at Publisher · View at Google Scholar
  34. N. Yadav, A. Dwivedi, S. F. Mujtaba et al., “Photosensitized mefloquine induces ROS-mediated DNA damage and apoptosis in keratinocytes under ambient UVB and sunlight exposure,” Cell Biology and Toxicology, vol. 30, no. 5, pp. 253–268, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. J. Jeon, K. S. Song, H. J. Han, S. H. Park, W. Chang, and M. Y. Lee, “Rosmarinic acid inhibits chemical hypoxia-induced cytotoxicity in primary cultured rat hepatocytes,” Archives of Pharmacal Research, vol. 37, no. 7, pp. 907–915, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Yang, H. Ling, M. Zhang et al., “Oxidative stress mediates chemical hypoxia-induced injury and inflammation by activating NF-κb-COX-2 pathway in HaCaT cells,” Molecules and Cells, vol. 31, no. 6, pp. 531–538, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Wang, M. Xu, R. Liang, M. Zhao, Z. Zhang, and Y. Li, “Oral administration of marine collagen peptides prepared from chum salmon (Oncorhynchus keta) improves wound healing following cesarean section in rats,” Food & Nutrition Research, vol. 59, p. 26411, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Xu, W. Dong, J. Zhao, and Y. Xu, “Effect of marine collagen peptides on physiological and neurobehavioral development of male rats with perinatal asphyxia,” Marine Drugs, vol. 13, no. 6, pp. 3653–3671, 2015. View at Publisher · View at Google Scholar · View at Scopus
  39. J. T. Ryan, R. P. Ross, D. Bolton, G. F. Fitzgerald, and C. Stanton, “Bioactive peptides from muscle sources: meat and fish,” Nutrients, vol. 3, no. 9, pp. 765–791, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. N. Muralidharan, R. Jeya Shakila, D. Sukumar, and G. Jeyasekaran, “Skin, bone and muscle collagen extraction from the trash fish, leather jacket (Odonus niger) and their characterization,” Journal of Food Science and Technology, vol. 50, no. 6, pp. 1106–1113, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Yamamoto, Y. Yoshizawa, K. Yanagiguchi, T. Ikeda, S. Yamada, and Y. Hayashi, “The characterization of fish (tilapia) collagen sponge as a biomaterial,” International Journal of Polymer Science, vol. 2015, Article ID 957385, 5 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  42. A. A. Karim and R. Bhat, “Fish gelatin: properties, challenges, and prospects as an alternative to mammalian gelatins,” Food Hydrocolloid, vol. 23, no. 3, pp. 563–576, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. D. J. Choi, S. M. Choi, H. Y. Kang et al., “Bioactive fish collagen/polycaprolactone composite nanofibrous scaffolds fabricated by electrospinning for 3D cell culture,” Journal of Biotechnology, vol. 205, pp. 47–58, 2015. View at Publisher · View at Google Scholar · View at Scopus
  44. J. Liu, B. Zhang, S. Song et al., “Bovine collagen peptides compounds promote the proliferation and differentiation of MC3T3-E1 pre-osteoblasts,” PloS One, vol. 9, no. 6, article e99920, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Coondoo, “Cytokines in dermatology - a basic overview,” Indian Journal of Dermatology, vol. 56, no. 4, pp. 368–374, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. J. J. O'Shea, A. Ma, and P. Lipsky, “Cytokines and autoimmunity,” Nature Reviews. Immunology, vol. 2, no. 1, pp. 37–45, 2002. View at Publisher · View at Google Scholar
  47. Z. Sun, M. A. Mohamed, S. Y. Park, and T. H. Yi, “Fucosterol protects cobalt chloride induced inflammation by the inhibition of hypoxia-inducible factor through PI3K/Akt pathway,” International Immunopharmacology, vol. 2, no. 2, pp. 642–647, 2015. View at Publisher · View at Google Scholar · View at Scopus
  48. H. K. Koul, M. Pal, and S. Koul, “Role of p38 MAP kinase signal transduction in solid tumors,” Genes & Cancer, vol. 4, no. 9-10, pp. 342–359, 2013. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Mavropoulos, T. Orfanidou, C. Liaskos et al., “p38 MAPK signaling in pemphigus: implications for skin autoimmunity,” Autoimmune Diseases, vol. 2013, Article ID 728529, 11 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. L. R. Coulthard, D. E. White, D. L. Jones, M. F. McDermott, and S. A. Burchill, “p38MAPK: stress responses from molecular mechanisms to therapeutics,” Trends in Molecular Medicine, vol. 15, no. 8, pp. 369–379, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. L. Jinlian, Z. Yingbin, and W. Chunbo, “p38 MAPK in regulating cellular responses to ultraviolet radiation,” Journal of Biomedical Science, vol. 4, no. 3, pp. 303–312, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. L. Soegaard-Madsen, C. Johansen, L. Iversen, and K. Kragballe, “Adalimumab therapy rapidly inhibits p38 mitogen-activated protein kinase activity in lesional psoriatic skin preceding clinical improvement,” The British Journal of Dermatology, vol. 162, no. 6, pp. 1216–1223, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Saklatvala, “The p38 MAP kinase pathway as a therapeutic target in inflammatory disease,” Current Opinion in Pharmacology, vol. 4, no. 4, pp. 372–377, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. J. Saldeen and N. Welsh, “p38 MAPK inhibits JNK2 and mediates cytokine-activated iNOS induction and apoptosis independently of NF-KB translocation in insulin-producing cells,” European Cytokine Network, vol. 1, no. 1, pp. 47–52, 2004. View at Google Scholar
  55. A. Lan, W. Xu, H. Zhang et al., “Inhibition of ROS activated p38 MAPK pathway is involved in the protective effect of H2S against chemical hypoxia-induced inflammation in PC12 cells,” Neurochemical Research, vol. 7, no. 7, pp. 1454–1466, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Van Laethem, S. Van Kelst, S. Lippens et al., “Activation of p38 MAPK is required for Bax translocation to mitochondria, cytochrome c release and apoptosis induced by UVB irradiation in human keratinocytes,” The FASEB journal, vol. 18, no. 15, pp. 1946–1948, 2004. View at Publisher · View at Google Scholar · View at Scopus
  57. Z. G. Liu, “Molecular mechanism of TNF signaling and beyond,” Cell Research, vol. 15, no. 1, pp. 24–27, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. B. B. Aggarwal, S. Shishodia, Y. Takada et al., “TNF blockade: an inflammatory issue,” Ernst Schering Research Foundation Workshop, vol. 56, no. 56, pp. 161–186, 2006. View at Publisher · View at Google Scholar
  59. G. Sabio and R. J. Davis, “TNF and MAP kinase signalling pathways,” Seminars in Immunology, vol. 26, no. 3, pp. 237–245, 2014. View at Publisher · View at Google Scholar · View at Scopus
  60. T. Lawrence, “The nuclear factor NF-kappaB pathway in inflammation,” Cold Spring Harbor Perspectives in Biology, vol. 1, no. 6, article a001651, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. O. H. Chai and C. H. Song, “Role of mast cell in the late phase of contact hypersensitivity induced by trimellitic anhydride,” Anatomy & Cell Biology, vol. 48, no. 4, pp. 225–234, 2015. View at Publisher · View at Google Scholar · View at Scopus
  62. L. Guo, P. A. Harnedy, M. B. O'Keeffe et al., “Fractionation and identification of Alaska pollock skin collagen-derived mineral chelating peptides,” Food Chemistry, vol. 173, pp. 536–542, 2015. View at Publisher · View at Google Scholar · View at Scopus
  63. C. Y. Huang, C. H. Wu, J. J. Yang, Y. H. Li, and J. M. Kuo, “Evaluation of iron-binding activity of collagen peptides prepared from the scales of four cultivated fishes in Taiwan,” Journal of Food and Drug Analysis, vol. 23, no. 4, pp. 671–678, 2015. View at Publisher · View at Google Scholar · View at Scopus