DOI QR코드

DOI QR Code

Asterias pectinifera-Derived Collagen Peptides Mixed with Halocynthia roretzi Extracts Exhibit Anti-Photoaging Activities during Exposure to UV Irradiation, and Antibacterial Properties

  • Soo-Jin Oh (BK21 Graduate Program, Department of Biomedical Sciences, College of Medicine, Korea University Guro Hospital) ;
  • Ji-Ye Park (BK21 Graduate Program, Department of Biomedical Sciences, College of Medicine, Korea University Guro Hospital) ;
  • Bada Won (R&D Center, Star's Tech Co., Ltd.) ;
  • Yong-Taek Oh (R&D Center, Star's Tech Co., Ltd.) ;
  • Seung-Chan Yang (R&D Center, Star's Tech Co., Ltd.) ;
  • Ok Sarah Shin (BK21 Graduate Program, Department of Biomedical Sciences, College of Medicine, Korea University Guro Hospital)
  • Received : 2022.07.08
  • Accepted : 2022.09.30
  • Published : 2022.11.28

Abstract

Asterias pectinifera, a species of starfish and cause of concern in the aquaculture industry, was recently identified as a source of non-toxic and highly water-soluble collagen peptides. In this study, we investigated the antioxidant and anti-photoaging functions of compounds formulated using collagen peptides from extracts of Asterias pectinifera and Halocynthia roretzi (AH). Our results showed that AH compounds have various skin protective functions, including antioxidant effects, determined by measuring the scavenging activity of 2,2-diphenyl-1-picrylhydrazyl radicals, as well as anti-melanogenic effects, determined by measuring tyrosinase inhibition activity. To determine whether ethosome-encapsulated AH compounds (E(AH)) exert ultraviolet (UV)-protective effects, human dermal fibroblasts or keratinocytes were incubated with E(AH) before and after exposure to UVA or UVB. E(AH) treatment led to inhibition of photoaging-induced secretion of matrix metalloproteinase-1 and interleukin-6 and -8, which are associated with inflammatory responses during UV irradiation. Finally, the antibacterial effects of AH and E(AH) were confirmed against both gram-negative and gram-positive bacteria. Our results indicate that E(AH) has the potential for use in the development of cosmetics with a range of skin protective functions.

Keywords

Acknowledgement

This research was supported by the Korea Institute of Marine Science & Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries (20210276).

References

  1. Monmai C, Go SH, Shin IS, You S, Kim D-O, Kang S, et al. 2018. Anti-inflammatory effect of asterias amurensis fatty acids through NF-kB and MAPK pathways against LPS-stimulated RAW264.7 cells. J. Microbiol. Biotechnol. 28: 1635-1644. https://doi.org/10.4014/jmb.1802.03044
  2. Lee CC, Hsieh HJ, Hsieh C-H, Hwang DF. 2014. Antioxidative and anticancer activities of various ethanolic extract fractions from crown-of-thorns starfish (Acanthaster planci). Environ. Toxicol. Pharmacol. 38: 761-73. https://doi.org/10.1016/j.etap.2014.08.021
  3. Zhang W, Wang J, Jin W, Zhang Q. 2013. The antioxidant activities and neuroprotective effect of polyAHccharides from the starfish Asterias rollestoni. Carbohydr. Polym. 95: 9-15. https://doi.org/10.1016/j.carbpol.2013.02.035
  4. Jeong MH, Yang KM, Kim JK, Nam BH, Kim GY, Lee SW, et al. 2013. Inhibitory effects of Asterina pectinifera extracts on melanin biosynthesis through tyrosinase activity. Int. J. Mol. Med. 31: 205-212. https://doi.org/10.3892/ijmm.2012.1181
  5. Thao NP, Cuong NX, Luyen BTT, Quang TH, Hanh TTH, Kim S, et al. 2013. Anti-inflammatory components of the starfish Astropecten polyacanthus. Mar. Drugs 11: 2917-2926. https://doi.org/10.3390/md11082917
  6. Han SB, Won B, Yang SC, Kim DH. 2021. Asterias pectinifera derived collagen peptide-encapsulating elastic nanoliposomes for the cosmetic application. J. Ind. Eng. Chem. 98: 289-297. https://doi.org/10.1016/j.jiec.2021.03.039
  7. Cuadrado A, Garcia-Fernandez L, Gonzalez L, Suarez Y, Losada A, Alcaide V, et al. 2003. AplidinTM induces apoptosis in human cancer cells via glutathione depletion and sustained activation of the epidermal growth factor receptor, Src, JNK, and p38 MAPK. J. Biol. Chem. 278: 241-250. https://doi.org/10.1074/jbc.M201010200
  8. Gunasinghe MA, AT Kim, SM Kim. 2019. Inhibitory effects of vanadium-binding proteins purified from the sea squirt Halocynthia roretzi on adipogenesis in 3T3-L1 adipocytes. Appl. Biochem. Biotechnol. 189: 49-64. https://doi.org/10.1007/s12010-019-02982-7
  9. Gunasinghe M. and SM Kim. 2018. Antioxidant and antidiabetic activities of vanadium binding proteins purified from the Halocynthia roretzi. J. Food Sci. Technol. 55: 1840-1849. https://doi.org/10.1007/s13197-018-3099-9
  10. Kim AT and Kim DO. 2019. Anti-inflammatory effects of vanadium-binding protein from Halocynthia roretzi in LPS-stimulated RAW264. 7 macrophages through NF-κB and MAPK pathways. Int. J. Biol. Macromol. 133: 732-738. https://doi.org/10.1016/j.ijbiomac.2019.04.106
  11. Oh Y, Shim KB, Ahn CB, Kim SS, Je JY. 2019. Halocynthia roretzi (Halocynthia roretzi) hydrolyAHtes induce apoptosis in human colon cancer HT-29 cells through activation of reactive oxygen species. Nutr. Cancer 71: 118-127. https://doi.org/10.1080/01635581.2018.1540717
  12. Park JH, Seo BY, Lee SC, Park E. 2010. Effects of ethanol extracts from stalked Halocynthia roretzi (Styela clava) on antioxidant potential, oxidative DNA damage and DNA repair. Food Sci. Biotechnol. 19: 1035-1040. https://doi.org/10.1007/s10068-010-0145-4
  13. White KM, Rosales R, Yildiz S, Kehrer T, Miorin L, Moreno E, et al. 2021. Plitidepsin has potent preclinical efficacy against AHRSCoV-2 by targeting the host protein eEF1A. Science 371: 926-931. https://doi.org/10.1126/science.abf4058
  14. Jang WS, Kim KN, Lee YS, Nam MH, Lee IH. 2002. Halocidin: a new antimicrobial peptide from hemocytes of the solitary tunicate, Halocynthia aurantium. FEBS Lett. 521: 81-86. https://doi.org/10.1016/S0014-5793(02)02827-2
  15. Oh S-J, JK Lee, OS Shin. 2019. Aging and the immune system: the impact of immunosenescence on viral infection, immunity and vaccine immunogenicity. Immune Netw. 19: e37.
  16. Lee JK, Oh SJ, Gim JA, Shin OS. 2022. miR-10a, miR-30c, and miR-451a encapsulated in small extracellular vesicles are pro-senescence factors in human dermal fibroblasts. J. Invest. Dermatol. 142: 2570-2579.e6. https://doi.org/10.1016/j.jid.2022.03.032
  17. Seo SW, Park SK, Oh SJ, Shin OS. 2018. TLR4-mediated activation of the ERK pathway following UVA irradiation contributes to increased cytokine and MMP expression in senescent human dermal fibroblasts. PLoS One 13: e0202323.
  18. Gilchrest BA. 2013. Photoaging. J. Investig. Dermatol. 133: E2-6. https://doi.org/10.1038/skinbio.2013.176
  19. Collado M, Blasco MA, Serrano M. 2007. Cellular senescence in cancer and aging. Cell 130: 223-233. https://doi.org/10.1016/j.cell.2007.07.003
  20. Ghosh K, BC Capell. 2016. The senescence-associated secretory phenotype: critical effector in skin cancer and aging. J. Investig. Dermatol. 136: 2133-2139. https://doi.org/10.1016/j.jid.2016.06.621
  21. Wikler M, F Cockerill, W Craig. 2006. Performance standards for antimicrobial disc susceptibility tests; Standards.
  22. D'Mello SAN, Finlay GJ, Baguley BC, Askarian-Amiri ME. 2016. Signaling pathways in melanogenesis. Int. J. Mol. Sci. 17: 1144.
  23. Slominski A, Tobin DJ, Shibahara S, Wortsman J. 2004. Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol. Rev. 84: 1155-1228. https://doi.org/10.1152/physrev.00044.2003
  24. Qian W, Liu W, Zhu D, Cao Y, Tang A, Gong G, et al. 2020. Natural skin-whitening compounds for the treatment of melanogenesis. Exp. Ther. Med. 20: 173-185. https://doi.org/10.3892/etm.2020.8687
  25. Pillaiyar T, Namasivayam V, Manickam M, Jung SH. 2018. Inhibitors of melanogenesis: an updated review. J. Med. Chem. 61: 7395-7418. https://doi.org/10.1021/acs.jmedchem.7b00967
  26. Lambert JD, Elias RJ. T 2010. he antioxidant and pro-oxidant activities of green tea polyphenols: a role in cancer prevention. Arch. Biochem. Biophys. 501: 65-72. https://doi.org/10.1016/j.abb.2010.06.013
  27. Bigelow R, Cardelli J. 2006. The green tea catechins,(-)-Epigallocatechin-3-gallate (EGCG) and (-)-Epicatechin-3-gallate (ECG), inhibit HGF/Met signaling in immortalized and tumorigenic breast epithelial cells. Oncogene 25: 1922-1930. https://doi.org/10.1038/sj.onc.1209227
  28. Singh D, Srivastava Sk, Chaudhuri Tk, Upadhyay G. 2015. Multifaceted role of matrix metalloproteinases (MMPs). Front. Mol. Biosci. 2: 19.
  29. Burrage PS, Mix KS, Brinckerhoff CE. 2006. Matrix metalloproteinases: role in arthritis. Front. Biosci. 11: 529-543. https://doi.org/10.2741/1817
  30. Catho G, Martischang R, Boroli F, Chraiti MN, Martin Y, Tomsuk ZK, et al. 2021. Outbreak of Pseudomonas aerugino producing VIM carbapenemase in an intensive care unit and its termination by implementation of waterless patient care. Crit. Care 25: 301.
  31. Enright MC, Robinson DA, Randle G, Feil EJ, Grundmann H, Spratt B. 2002. The evolutionary history of methicillin-resistant Staphylococcus aureus (MRAH). Proc. Natl. Acad. Sci. USA 99: 7687-7692. https://doi.org/10.1073/pnas.122108599
  32. Monmai C, Go SH, Shin I-S, You SG, Lee H, Kang SB, et al. 2018. Immune-enhancement and anti-inflammatory activities of fatty acids extracted from Halocynthia aurantium tunic in RAW264. 7 cells. Mar. Drugs 16: 309.
  33. Kim SS, Ahn CB, Moon SE, Je JY. 2018. Purification and antioxidant activities of peptides from Halocynthia roretzi (Halocynthia roretzi) protein hydrolyAHtes using pepsin hydrolysis. Food Biosci. 25: 128-133. https://doi.org/10.1016/j.fbio.2018.08.010
  34. Delgado-Calle J, Kurihara N, Atkinson EG, Nelson J, Miyagawa K, Galmarini CM, et al. 2019. Aplidin (plitidepsin) is a novel anti-myeloma agent with potent anti-resorptive activity mediated by direct effects on osteoclasts. Oncotarget 10: 2709-2721. https://doi.org/10.18632/oncotarget.26831
  35. Gomes NGM, Valentao PB, Pereira RB. 2020. Plitidepsin to treat multiple myeloma. Drugs Today (Barc) 56: 337-347. https://doi.org/10.1358/dot.2020.56.5.3135886
  36. LoAHda A, Munoz-Alonso MJ, Garcia C, Sanchez-Murcia PA, Martinzw-L JF, Dominguez JM, et al. 2016. Translation elongation factor eEF1A2 is a novel anticancer target for the marine natural product plitidepsin. Sci. Rep. 6: 35100.
  37. Blowes LM, Egertova M, Liu Y, Davis GR, Terrill NJ, Gupta HS, et al. 2017. Body wall structure in the starfish Asteriasrubens. J. Anat. 231: 325-341. https://doi.org/10.1111/joa.12646
  38. O'Neill P. 1989. Structure and mechanics of starfish body wall. J. Exp. Biol. 147: 53-89. https://doi.org/10.1242/jeb.147.1.53
  39. Eylers JP. 1976. Aspects of skeletal mechanics of the starfish Asterias forbesii. J. Morphol. 149: 353-367. https://doi.org/10.1002/jmor.1051490305
  40. Park S.-H, Song T, Bae TS, Khang G, Choi BH, Park SR, et al. 2012. Comparative analysis of collagens extracted from different animal sources for application of cartilage tissue engineering. Int. J. Precis. Eng. Manufact. 13: 2059-2066. https://doi.org/10.1007/s12541-012-0271-4
  41. Ikoma T, Kobayashi H, Tanaka J, Walsh D, Mann S. 2003. Physical properties of type I collagen extracted from fish scales of Pagrus major and Oreochromis niloticas. Int. J. Biol. Macromol. 32: 199-204. https://doi.org/10.1016/S0141-8130(03)00054-0
  42. Sun L, Hou H, Li B, Zhang Y. 2017. Characterization of acid-and pepsin-soluble collagen extracted from the skin of Nile tilapia (Oreochromis niloticus). Int. J. Biol. Macromol. 99: 8-14. https://doi.org/10.1016/j.ijbiomac.2017.02.057
  43. Sercombe L, Veerati T, Moheimani F, Wu SY, Sood AK, Hua S. 2015. Advances and challenges of liposome assisted drug delivery. Front. Pharmacol. 6: 286.
  44. Akbarzadeh A, Rezaei-Sadabady R, Davaran S, Joo SW, Zarghami N, Hanifehpour Y, et al. 2013. Liposome: classification, preparation, and applications. Nanoscale Res. Lett. 8: 102.
  45. Zylberberg C, S Matosevic. 2016. Pharmaceutical liposomal drug delivery: a review of new delivery systems and a look at the regulatory landscape. Drug Deliv. 23: 3319-3329. https://doi.org/10.1080/10717544.2016.1177136
  46. Paiva-AHntos AC, Silva AL, Guerra C, Peixoto D, Pereira-Silva M, Zeinali M, et al. 2021. Ethosomes as nanocarriers for the development of skin delivery formulations. Pharm. Res. 38: 947-970. https://doi.org/10.1007/s11095-021-03053-5
  47. Nasr S, Rady M, Gomaa I, Syrovets T, Simmet T, Fayad W, et al. 2019. Ethosomes and lipid-coated chitoAHn nanocarriers for skin delivery of a chlorophyll derivative: a potential treatment of squamous cell carcinoma by photodynamic therapy. Int. J. Pharm. 568: 118528.
  48. ElAHyed MM, Abdallah OY, Naggar VF, Khalafallah NM. 2006. Deformable liposomes and ethosomes: mechanism of enhanced skin delivery. Int. J. Pharm. 322: 60-66. https://doi.org/10.1016/j.ijpharm.2006.05.027
  49. Bellefroid C, Lechanteur A, Evrard B, Mottet D, Debacq-Chainiaux F, Piei G. 2019. In vitro skin penetration enhancement techniques: a combined approach of ethosomes and microneedles. Int. J. Pharm. 572: 118793.
  50. Shen LN, Zhang YT, Wang Q, Xu L, Feng NP. 2014. Enhanced in vitro and in vivo skin deposition of apigenin delivered using ethosomes. Int. J. Pharm. 460: 280-288. https://doi.org/10.1016/j.ijpharm.2013.11.017
  51. Van Tran V, JY Moon, YC Lee. 2019. Liposomes for delivery of antioxidants in cosmeceuticals: challenges and development strategies. J. Control. Release 300: 114-140. https://doi.org/10.1016/j.jconrel.2019.03.003
  52. Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler JR VG. 2015. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin. Microbiol. Rev. 28: 603-661. https://doi.org/10.1128/CMR.00134-14
  53. Dayan GH, Mohamed N, Scully IL, Cooper D, Begier E, Eiden J, et al. 2016. Staphylococcus aureus: the current state of disease, pathophysiology and strategies for prevention. Expert Rev. Vccines 15: 1373-1392. https://doi.org/10.1080/14760584.2016.1179583
  54. Peterson LR, DM Schora. 2016. Methicillin-resistant Staphylococcus aureus control in the 21st century: laboratory involvement affecting disease impact and economic benefit from large population studies. J. Clin. Microbiol. 54: 2647-2654. https://doi.org/10.1128/JCM.00698-16
  55. Choi EJ, Kim HI, Kim JA, Jun SY, Kang SH, Park DJ, et al. 2015. The herbal-derived honokiol and magnolol enhances immune response to infection with methicillin-sensitive Staphylococcus aureus (MSAH) and methicillin-resistant S. aureus (MRAH). Appl. Microbiol. Biotechnol. 99: 4387-4396. https://doi.org/10.1007/s00253-015-6382-y