Attenuation of UV-B exposure-induced inflammation by abalone hypobranchial gland and gill extracts

Kuanpradit,Chitraporn; Jaisin,Yamaratee; Jungudomjaroen,Sumon; Akter Mitu,Shahida; Puttikamonkul,Srisombat; Sobhon,Prasert; Cummins,Scott  F.

doi:10.3892/ijmm.2017.2939

Attenuation of UV-B exposure-induced inflammation by abalone hypobranchial gland and gill extracts

Authors:
- Chitraporn Kuanpradit
- Yamaratee Jaisin
- Sumon Jungudomjaroen
- Shahida Akter Mitu
- Srisombat Puttikamonkul
- Prasert Sobhon
- Scott F. Cummins
View Affiliations

Affiliations: Faculty of Medicine, Srinakharinwirot University, Bangkok 10110, Thailand, Genecology Research Center, Faculty of Science, Health and Education, University of the Sunshine Coast, Maroochydore, DC, QLD 4558, Australia, Faculty of Science, Mahidol University, Bangkok 10400, Thailand
Published online on: March 29, 2017 https://doi.org/10.3892/ijmm.2017.2939
Pages: 1083-1090
Copyright: © Kuanpradit et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Exposure to solar ultraviolet B (UV-B) is a known causative factor for many skin complications such as wrinkles, black spots, shedding and inflammation. Within the wavelengths 280‑320 nm, UV-B can penetrate to the epidermal level. This investigation aimed to test whether extracts from the tropical abalone [Haliotis asinina (H. asinina)] mucus-secreting tissues, the hypobranchial gland (HBG) and gills, were able to attenuate the inflammatory process, using the human keratinocyte HaCaT cell line. Cytotoxicity of abalone tissue extracts was determined using an AlamarBlue viability assay. Results showed that HaCaT cells could survive when incubated in crude HBG and gill extracts at concentrations between <11.8 and <16.9 µg/ml, respectively. Subsequently, cell viability was compared between cultured HaCaT cells exposed to serial doses of UV-B from 1 to 11 (x10) mJ/cm2 and containing 4 different concentrations of abalone extract from both the HBG and gill (0, 0.1, 2.5, 5 µg/ml). A significant increase in cell viability was observed (P<0.001) following treatment with 2.5 and 5 µg/ml extract. Without extract, cell viability was significantly reduced upon exposure to UV-B at 4 mJ/cm2. Three morphological changes were observed in HaCaT cells following UV-B exposure, including i) condensation of cytoplasm; ii) shrunken cells and plasma membrane bubbling; and iii) condensation of chromatin material. A calcein AM‑propidium iodide live‑dead assay showed that cells could survive cytoplasmic condensation, yet cell death occurred when damage also included membrane bubbling and chromatin changes. Western blot analysis of HaCaT cell COX‑2, p38, phospho‑p38, SPK/JNK and phospho‑SPK/JNK following exposure to >2.5 µg/ml extract showed a significant decrease in intensity for COX‑2, phospho‑p38 and phospho‑SPK/JNK. The present study demonstrated that abalone extracts from the HGB and gill can attenuate inflammatory proteins triggered by UV-B. Hence, the contents of abalone extract, including cellmetabolites and peptides, may provide new agents for skin anti‑inflammation, preventing damage due to UV-B.

View Figures

View References

1	de Gruijl FR and Van der Leun JC: Estimate of the wavelength dependency of ultraviolet carcinogenesis in humans and its relevance to the risk assessment of a stratospheric ozone depletion. Health Phys. 67:319–325. 1994. View Article : Google Scholar : PubMed/NCBI
2	Svobodova A, Walterova D and Vostalova J: Ultraviolet light induced alteration to the skin. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 150:25–38. 2006. View Article : Google Scholar : PubMed/NCBI
3	Nichols JA and Katiyar SK: Skin photoprotection by natural polyphenols: Anti-inflammatory, antioxidant and DNA repair mechanisms. Arch Dermatol Res. 302:71–83. 2010. View Article : Google Scholar
4	Afaq F: Natural agents: Cellular and molecular mechanisms of photoprotection. Arch Biochem Biophys. 508:144–151. 2011. View Article : Google Scholar :
5	López-Camarillo C, Ocampo EA, Casamichana ML, Pérez- Plasencia C, Alvarez-Sánchez E and Marchat LA: Protein kinases and transcription factors activation in response to UV-radiation of skin: Implications for carcinogenesis. Int J Mol Sci. 13:142–172. 2012. View Article : Google Scholar : PubMed/NCBI
6	Bender K, Göttlicher M, Whiteside S, Rahmsdorf HJ and Herrlich P: Sequential DNA damage-independent and -dependent activation of NF-kappaB by UV. EMBO J. 17:5170–5181. 1998. View Article : Google Scholar : PubMed/NCBI
7	Hernandez-Pigeon H, Jean C, Charruyer A, Haure MJ, Titeux M, Tonasso L, Quillet-Mary A, Baudouin C, Charveron M and Laurent G: Human keratinocytes acquire cellular cytotoxicity under UV-B irradiation. Implication of granzyme B and perforin. J Biol Chem. 281:13525–13532. 2006. View Article : Google Scholar : PubMed/NCBI
8	Ali D, Verma A, Mujtaba F, Dwivedi A, Hans RK and Ray RS: UV-B-induced apoptosis and DNA damaging potential of chrysene via reactive oxygen species in human keratinocytes. Toxicol Lett. 204:199–207. 2011. View Article : Google Scholar : PubMed/NCBI
9	Wu MS, Sun DS, Lin YC, Cheng CL, Hung SC, Chen PK, Yang JH and Chang HH: Nanodiamonds protect skin from ultraviolet B-induced damage in mice. J Nanobiotechnology. 13:352015. View Article : Google Scholar : PubMed/NCBI
10	Devary Y, Rosette C, DiDonato JA and Karin M: NF-kappa B activation by ultraviolet light not dependent on a nuclear signal. Science. 261:1442–1445. 1993. View Article : Google Scholar : PubMed/NCBI
11	Buckman SY, Gresham A, Hale P, Hruza G, Anast J, Masferrer J and Pentland AP: COX-2 expression is induced by UV-B exposure in human skin: Implications for the development of skin cancer. Carcinogenesis. 19:723–729. 1998. View Article : Google Scholar : PubMed/NCBI
12	Muller-Decker K, Neufang G, Berger I, Neumann M, Marks F and Furstenberger G: Transgenic cyclooxygenase-2 overexpression sensitizes mouse skin for carcinogenesis. Proc Natl Acad Sci USA. 99:12483–12488. 2002. View Article : Google Scholar : PubMed/NCBI
13	Shibata A, Nakagawa K, Yamanoi H, Tsuduki T, Sookwong P, Higuchi O, Kimura F and Miyazawa T: Sulforaphane suppresses ultraviolet B-induced inflammation in HaCaT keratinocytes and HR-1 hairless mice. J Nutr Biochem. 21:702–709. 2010. View Article : Google Scholar
14	Liu S, Mizu H and Yamauchi H: Photoinflammatory responses to UV-irradiated ketoprofen mediated by the induction of ROS generation, enhancement of cyclooxygenase-2 expression, and regulation of multiple signaling pathways. Free Radic Biol Med. 48:772–780. 2010. View Article : Google Scholar
15	Kim JE, Kwon JY, Seo SK, Son JE, Jung SK, Min SY, Hwang MK, Heo YS, Lee KW and Lee HJ: Cyanidin suppresses ultraviolet B-induced COX-2 expression in epidermal cells by targeting MKK4, MEK1, and Raf-1. Biochem Pharmacol. 79:1473–1482. 2010. View Article : Google Scholar : PubMed/NCBI
16	Englaro W, Dérijard B, Ortonne JP and Ballotti R: Solar ultraviolet light activates extracellular signal-regulated kinases and the ternary complex factor in human normal keratinocytes. Oncogene. 16:661–664. 1998. View Article : Google Scholar : PubMed/NCBI
17	Ashida M, Bito T, Budiyanto A, Ichihashi M and Ueda M: Involvement of EGF receptor activation in the induction of cyclooxygenase-2 in HaCaT keratinocytes after UV-B. Exp Dermatol. 12:445–452. 2003. View Article : Google Scholar : PubMed/NCBI
18	El-Abaseri TB, Hammiller B, Repertinger SK and Hansen LA: The epidermal growth factor receptor increases cytokine production and cutaneous inflammation in response to ultraviolet irradiation. ISRN Dermatol. 2013:8487052013. View Article : Google Scholar : PubMed/NCBI
19	Zamzow JP and Losey GS: Ultraviolet radiation absorbance by coral reef fish mucus: Photo-protection and visual communication. Environ Biol Fishes. 63:41–47. 2002. View Article : Google Scholar
20	Jacobson PB and Jacobs RS: Fuscoside: An anti-inflammatory marine natural product which selectively inhibits 5-lipoxygenase Part I: Physiological and biochemical studies in murine inflammatory models. J Pharmacol Exp Ther. 262:866–873. 1992.PubMed/NCBI
21	Ojika M, Kigoshi H, Yoshida Y, Ishigaki T, Nisiwaki M, Tsukada I, Arakawa M, Ekimoto H and Yamada K: Aplyronine A, a potent antitumor macrolide of marine origin, and the congeners aplyronines B and C: Isolation, structures, and bioactivities. Tetrahedron. 63:3138–3167. 2007. View Article : Google Scholar
22	Uddin MH, Otsuka M, Muroi T, Ono A, Hanif N, Matsuda S, Higa T and Tanaka J: Deoxymanoalides from the nudibranch Chromodoris willani. Chem Pharm Bull (Tokyo). 57:885–887. 2009. View Article : Google Scholar
23	Yamada K, Ojika M, Kigoshi H and Suenaga K: Aplyronine A, a potent antitumor macrolide of marine origin, and the congeners aplyronines B-H: Chemistry and biology. Nat Prod Rep. 26:27–43. 2009. View Article : Google Scholar : PubMed/NCBI
24	Adikwu MU and Alozie BU: Application of snail mucin dispersed in detarium gum gel in wound healing. Sci Res Essays. 2:195–198. 2007.
25	Santana WA, Melo CM, Cardoso JC, Pereira-Filho RN, Rabelo AS, Reis FP and Albuquerque-Júnior RLC: Assessment of antimicrobial activity and healing potential of mucous secretion of Achatina fulica. Int J Morphol. 30:365–373. 2012. View Article : Google Scholar
26	Shimidzu N, Goto M and Miki W: Carotenoids as singlet oxygen quenchers in marine organisms. Fish Sci. 62:134–137. 1996.
27	Bonnemain B: Helix and drugs: Snails for western health care from antiquity to the present. Evid Based Complement Alternat Med : eCAM. 2:25–28. 2005. View Article : Google Scholar : PubMed/NCBI
28	D'Orazio N, Gammone MA, Gemello E, De Girolamo M, Cusenza S and Riccioni G: Marine bioactives: Pharmacological properties and potential applications against inflammatory diseases. Mar Drugs. 10:812–833. 2012. View Article : Google Scholar : PubMed/NCBI
29	Cruz MC, Sanz-Rodríguez F, Zamarrón A, Reyes E, Carrasco E, González S and Juarranz A: A secretion of the mollusc Cryptomphalus aspersa promotes proliferation, migration and survival of keratinocytes and dermal fibroblasts in vitro. Int J Cosmet Sci. 34:183–189. 2012. View Article : Google Scholar
30	Chalermwat K, Szuster BW and Flaherty M: Shellfish aquaculture in Thailand. Aquac Econ Manag. 7:249–261. 2003. View Article : Google Scholar
31	Cook PA and Roy Gordon H: World abalone supply, markets, and pricing. J Shellfish Res. 29:569–571. 2010. View Article : Google Scholar
32	Wanichanon C, Laimek P, Linthong V, Sretarugsa P, Kruatrachue M, Upatham ES, Poomtong T and Sobhon P: Histology of hypobranchial glands and gills of Haliotis asinina Linnaeus. J Shellfish Res. 23:1107–1112. 2004.
33	Naegel LCA and Aguilar-Cruz CA: The hypobranchial gland from the purple snail Plicopurpura pansa (Gould, 1853) (Prosobranchia: Muricidae). J Shellfish Res. 25:391–394. 2006. View Article : Google Scholar
34	Laimek P, Clark S, Stewart M, Pfeffer F, Wanichanon C, Hanna P and Sobhon P: The presence of GABA in gastropod mucus and its role in inducing larval settlement. J Exp Mar Biol Ecol. 354:182–191. 2008. View Article : Google Scholar
35	Kuanpradit C, Cummins SF, Degnan BM, Sretarugsa P, Hanna PJ, Sobhon P and Chavadej J: Identification of an attractin-like pheromone in the mucus-secreting hypobranchial gland of the abalone Haliotis asinina linnaeus. J Shellfish Res. 29:699–704. 2010. View Article : Google Scholar
36	Kuanpradit C, Stewart MJ, York PS, Degnan BM, Sobhon P, Hanna PJ, Chavadej J and Cummins SF: Characterization of mucus-associated proteins from abalone (Haliotis) - candidates for chemical signaling. FEBS J. 279:437–450. 2012. View Article : Google Scholar
37	Stewart P, Williams EA, Stewart MJ, Soonklang N, Degnan SM, Cummins SF, Hanna PJ and Sobhon P: Characterization of a GABAA receptor β subunit in the abalone Haliotis asinina that is upregulated during larval development. J Exp Mar Biol Ecol. 410:53–60. 2011. View Article : Google Scholar
38	Seo MD, Kang TJ, Lee CH, Lee AY and Noh M: HaCaT keratinocytes and primary epidermal keratinocytes have different transcriptional profiles of cornified envelope-associated genes to T helper cell cytokines. Biomol Ther (Seoul). 20:171–176. 2012. View Article : Google Scholar
39	Yang YL, Chang CH, Huang CC and Liu HW: Anti- inflammation and anti-apoptosis effects of pearl extract gel on UV-B irradiation HaCaT cells. Biomed Mater Eng. 26(Suppl 1): S139–S145. 2015.
40	Kim SB, Kang OH, Joung DK, Mun SH, Seo YS, Cha MR, Ryu SY, Shin DW and Kwon DY: Anti-inflammatory effects of tectroside on UV-B-induced HaCaT cells. Int J Mol Med. 31:1471–1476. 2013.PubMed/NCBI
41	Al-Nasiry S, Geusens N, Hanssens M, Luyten C and Pijnenborg R: The use of Alamar Blue assay for quantitative analysis of viability, migration and invasion of choriocarcinoma cells. Hum Reprod. 22:1304–1309. 2007. View Article : Google Scholar : PubMed/NCBI
42	Shick JM, Lesser MP, Dunlap WC, Stochaj WR, Chalker BE and Won JW: Depth dependent responses to solar ultraviolet radiation and oxidative stress in the zooxanthellate coral Acropora microphthalma. Mar Biol. 122:41–51. 1995. View Article : Google Scholar
43	Baker KS, Smith RC and Green AES: Middle ultraviolet radiation reaching the ocean surface. Photochem Photobiol. 32:367–374. 1980. View Article : Google Scholar
44	Geiger DL: Distribution and biogeography of the recent Haliotidae (Gastropoda: Vetigastropoda) world-wide. Bollettino Malacologico. 35:57–120. 2000.
45	Benkendorff K, Rudd D, Nongmaithem BD, Liu L, Young F, Edwards V, Avila C and Abbott CA: Are the traditional medical uses of muricidae molluscs substantiated by their pharmacological properties and bioactive compounds? Mar Drugs. 13:5237–5275. 2015. View Article : Google Scholar : PubMed/NCBI
46	Sales-Campos H, de Souza PR, Basso PJ, Ramos AD, Nardini V, Chica JE, Capurro ML, Sá-Nunes A and de Barros Cardoso CR: Aedes aegypti salivary gland extract ameliorates experimental inflammatory bowel disease. Int Immunopharmacol. 26:13–22. 2015. View Article : Google Scholar : PubMed/NCBI
47	Ghosh M, Sangwan N and Sangwan AK: Partial characterization of a novel anti-inflammatory protein from salivary gland extract of Hyalomma anatolicum anatolicum (77Acari: Ixodidae) ticks. Vet World. 8:772–776. 2015. View Article : Google Scholar
48	Wei L, Huang C, Yang H, Li M, Yang J, Qiao X, Mu L, Xiong F, Wu J and Xu W: A potent anti-inflammatory peptide from the salivary glands of horsefly. Parasit Vectors. 8:5562015. View Article : Google Scholar : PubMed/NCBI
49	Cheong SH, Hwang JW, Lee SH, Kim YS, Sim EJ, You BI, Lee SH, Park DJ, Ahn CB, Kim EK, et al: In vitro and in vivo antioxidant and anti-inflammatory activities of abalone (Haliotis discus) water extract. Adv Exp Med Biol. 803:833–849. 2015. View Article : Google Scholar : PubMed/NCBI