SNA077, an Extract of Marine Streptomyces sp., Inhibits Melanogenesis by Downregulating Melanogenic Proteins via Inactivation of cAMP/PKA/CREB Signaling
Abstract
:1. Introduction
2. Results
2.1. Secondary Metabolite Profiling of SNA077 Extract
2.2. Inhibitory Effect of SNA077 on Melanin Content and Cellular Tyrosinase Activity in B16, Melan-a, and MNT-1 Cells
2.3. Inhibitory Effect of SNA077 on mRNA and Protein Expression Levels of Melanogenesis-Related Genes in B16 and MNT-1 Cells
2.4. Anti-Melanogenic Effect of SNA077 Involves Down-Regulating the Phosphorylation of cAMP/PKA/CREB and MAPK in α-MSH-Stimulated B16 Cells
2.5. Inhibitory Effect of SNA077 on Melanogenesis in a 3D Human Skin Equivalent
3. Discussion
4. Materials and Methods
4.1. General Experiments
4.2. Collection, Phylogenetic Analysis, Cultivation, Extraction, and Fractionation
4.3. Secondary Metabolite Profiling Analysis
4.4. Cell Culture
4.5. Cell Viability Assay
4.6. Measurement of Melanin Content
4.7. Mushroom Tyrosinase Activity Assay
4.8. Cellular Tyrosinase Activity Assay
4.9. Western Blot Analysis
4.10. Real-Time PCR
4.11. Cyclic AMP Assay
4.12. Skin Whitening Test Using a MelanoDerm Skin Equivalent
4.13. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
a-MSH | a-melanocyte-stimulating hormone |
MC1R | melanocortin 1 receptor |
CREB | cAMP response element-binding protein |
Tyrp-1 | tyrosinase-related protein 1 |
MITF | microphthalmia-associated transcription factor |
MAPL | mitogen-activated protein kinase |
F&M | Fontana-Masson |
References
- Bérdy, J. Bioactive Microbial Metabolites. J. Antibiot. 2005, 58, 1–26. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Slominski, A.; Tobin, D.J.; Shibahara, S.; Wortsman, J. Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol. Rev. 2004, 84, 1155–1228. [Google Scholar] [CrossRef] [PubMed]
- Dunbar, J.C.; Lu, H. Leptin-induced increase in sympathetic nervous and cardiovascular tone is mediated by proopiomelanocortin (POMC) products. Brain Res. Bull. 1999, 50, 215–221. [Google Scholar] [CrossRef] [PubMed]
- Lee, C.S.; Jang, W.H.; Park, M.; Jung, K.; Baek, H.S.; Joo, Y.H.; Park, Y.H.; Lim, K.M. A novel adamantyl benzylben-zamide derivative, AP736, suppresses melanogenesis through the inhibition of cAMP-PKA-CREB-activated microph-thalmia-associated transcription factor and tyrosinase expression. Exp. Dermatol. 2013, 22, 762–764. [Google Scholar] [CrossRef] [PubMed]
- Oh, T.-I.; Yun, J.-M.; Park, E.-J.; Kim, Y.-S.; Lee, Y.-M.; Lim, J.-H. Plumbagin Suppresses α-MSH-Induced Melanogenesis in B16F10 Mouse Melanoma Cells by Inhibiting Tyrosinase Activity. Int. J. Mol. Sci. 2017, 18, 320. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Smalley, K.; Eisen, T. The involvement of p38 mitogen-activated protein kinase in the α-melanocyte stimulating hormone (α-MSH)-induced melanogenic and anti-proliferative effects in B16 murine melanoma cells. FEBS Lett. 2000, 476, 198–202. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- D’Mello, S.A.N.; Finlay, G.J.; Baguley, B.C.; Askarian-Amiri, M.E. Signaling Pathways in Melanogenesis. Int. J. Mol. Sci. 2016, 17, 1144. [Google Scholar] [CrossRef] [Green Version]
- Bellei, B.; Maresca, V.; Flori, E.; Pitisci, A.; Larue, L.; Picardo, M. p38 regulates pigmentation via proteasomal degradation of tyrosinase. J. Biol. Chem. 2010, 285, 7288–7299. [Google Scholar] [CrossRef] [Green Version]
- del Marmol, V.; Beermann, F. Tyrosinase and related proteins in mammalian pigmentation. FEBS Lett. 1996, 381, 165–168. [Google Scholar] [CrossRef] [PubMed]
- Sulaimon, S.S.; Kitchell, B.E. The biology of melanocytes. Veter-Dermatol. 2003, 14, 57–65. [Google Scholar] [CrossRef]
- Yokoyama, K.; Yasumoto, K.; Suzuki, H.; Shibahara, S. Cloning of the human DOPAchrome tautomerase/tyrosinase-related protein 2 gene and identification of two regulatory regions required for its pigment cell-specific expression. J. Biol. Chem. 1994, 269, 27080–27087. [Google Scholar] [CrossRef] [PubMed]
- Kobayashi, T.; Urabe, K.; Winder, A.; Jiménez-Cervantes, C.; Imokawa, G.; Brewington, T.; Solano, F.; Garcia-Borron, J.C.; Hearing, V. Tyrosinase related protein 1 (TRP1) functions as a DHICA oxidase in melanin biosynthesis. EMBO J. 1994, 13, 5818–5825. [Google Scholar] [CrossRef]
- Kim, Y.-J.; Uyama, H. Tyrosinase inhibitors from natural and synthetic sources: Structure, inhibition mechanism and perspective for the future. Cell. Mol. Life Sci. 2005, 62, 1707–1723. [Google Scholar] [CrossRef]
- Petersen, F.; Zähner, H.; Metzger, J.W.; Freund, S.; Hummel, R.-P. Germicidin, an autoregulative germination inhibitor of Streptomyces viridochromogenes NRRL B-1551. J. Antibiot. 1993, 46, 1126–1138. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhao, M.; Wang, L.; Ye, W.; Zhang, W.; Zhang, Q.; Ma, L.; Zhang, L.; Zhang, C.; Yang, C. Diversity of actinobacteria from mangrove sediment in Gaoqiao, Zhanjiang and identification of germicidins from one strain of Streptomyces. Acta Microbiol. Sinica. 2022, 62, 1740–1753. [Google Scholar]
- Song, M.-J.; Bae, J.; Lee, D.-S.; Kim, C.-H.; Kim, J.-S.; Kim, S.-W.; Hong, S.-I. Purification and characterization of prodigiosin produced by integrated bioreactor from Serratia sp. KH-95. J. Biosci. Bioeng. 2006, 101, 157–161. [Google Scholar] [CrossRef] [PubMed]
- Georgousaki, K.; Tsafantakis, N.; Gumeni, S.; Gonzalez, I.; Mackenzie, T.A.; Reyes, F.; Lambert, C.; Trougakos, I.P.; Genilloud, O.; Fokialakis, N. Screening for tyrosinase inhibitors from actinomycetes; identification of trichostatin derivatives from Streptomyces sp. CA-129531 and scale up production in bioreactor. Bioorg. Med. Chem. Lett. 2020, 30, 126952. [Google Scholar] [CrossRef] [PubMed]
- Favas, R.; Morone, J.; Martins, R.; Vasconcelos, V.; Lopes, G. Cyanobacteria and microalgae bioactive compounds in skin-ageing: Potential to restore extracellular matrix filling and overcome hyperpigmentation. J. Enzym. Inhib. Med. Chem. 2021, 36, 1829–1838. [Google Scholar] [CrossRef] [PubMed]
- Favas, R.; Morone, J.; Martins, R.; Vasconcelos, V.; Lopes, G. Cyanobacteria secondary metabolites as biotechnological ingredients in natural anti-aging cosmetics: Potential to overcome hyperpigmentation, loss of skin density and UV radiation-deleterious effects. Mar. Drugs. 2022, 20, 183. [Google Scholar] [CrossRef]
- Kalasariya, H.S.; Yadav, V.K.; Yadav, K.K.; Tirth, V.; Algahtani, A.; Islam, S.; Gupta, N.; Jeon, B.H. Seaweed-Based Molecules and Their Potential Biological Activities: An Eco-Sustainable Cosmetics. Molecules 2021, 26, 17. [Google Scholar] [CrossRef] [PubMed]
- Wolf Horrell, E.M.; Boulanger, M.C.; D’Orazio, J.A. Melanocortin 1 receptor: Structure, function, and regulation. Front. Genet. 2016, 7, 95. [Google Scholar] [CrossRef]
- Imokawa, G.; Ishida, K. Inhibitors of intracellular signaling pathways that lead to stimulated epidermal pigmentation: Perspective of anti-pigmenting agents. Int. J. Mol. Sci. 2014, 15, 8293–8315. [Google Scholar] [CrossRef] [Green Version]
- Zhao, L.M.; Han, L.N.; Ren, F.Z.; Chen, S.H.; Liu, L.H.; Wang, M.X.; Sang, M.X.; Shan, B.E. An ester extract of Cochinchina momordica seeds induces differentiation of melanoma B16 F1 cells via MAPKs signaling. Asian. Pac. J. Cancer. Prev. 2012, 13, 3795–3802. [Google Scholar] [CrossRef] [Green Version]
- Peng, H.Y.; Lin, C.C.; Wang, H.Y.; Shih, Y.; Chou, S.T. The melanogenesis alteration effects of Achillea millefolium L. essential oil and linalyl acetate: Involvement of oxidative stress and the JNK and ERK signaling pathways in melanoma cells. PLoS. One 2014, 9, e95186. [Google Scholar] [CrossRef]
- Hirata, N.; Naruto, S.; Ohguchi, K.; Akao, Y.; Nozawa, Y.; Iinuma, M.; Matsuda, H. Mechanism of the melanogenesis stimulation activity of (-)-cubebin in murine B16 melanoma cells. Bioorg. Med. Chem. 2007, 15, 4897–4902. [Google Scholar] [CrossRef] [PubMed]
- Grewal, S.S.; Fass, D.M.; Yao, H.; Ellig, C.L.; Goodman, R.H.; Stork, P.J. Calcium and cAMP signals differentially regulate cAMP-responsive element-binding protein function via a Rap1-extracellular signal-regulated kinase pathway. J. Biol. Chem. 2000, 275, 34433–34441. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Muthusamy, V.; Piva, T.J. The UV response of the skin: A review of the MAPK, NFkappaB and TNFalpha signal trans-duction pathways. Arch. Dermatol. Res. 2010, 302, 5–17. [Google Scholar] [CrossRef]
- Alesiani, D.; Cicconi, R.; Mattei, M.; Bei, R.; Canini, A. Inhibition of Mek 1/2 kinase activity and stimulation of melanogenesis by 5,7-dimethoxycoumarin treatment of melanoma cells. Int. J. Oncol. 2009, 34, 1727–1735. [Google Scholar]
- Baek, S.H.; Lee, S.H. Sesamol decreases melanin biosynthesis in melanocyte cells and zebrafish: Possible involve-ment of MITF via the intracellular cAMP and p38/JNK signalling pathways. Exp. Dermatol. 2015, 24, 761–766. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, C.S.; Park, M.; Han, J.; Lee, J.H.; Bae, I.H.; Choi, H.; Son, E.D.; Park, Y.H.; Lim, K.M. Liver X receptor activa-tion inhibits melanogenesis through the acceleration of ERK-mediated MITF degradation. J. Invest. Dermatol. 2013, 133, 1063–1071. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Lim, S.-J.; Jung, D.-W.; Hillman, P.F.; Nam, S.-J.; Lee, C.-S. SNA077, an Extract of Marine Streptomyces sp., Inhibits Melanogenesis by Downregulating Melanogenic Proteins via Inactivation of cAMP/PKA/CREB Signaling. Int. J. Mol. Sci. 2022, 23, 14922. https://doi.org/10.3390/ijms232314922
Lim S-J, Jung D-W, Hillman PF, Nam S-J, Lee C-S. SNA077, an Extract of Marine Streptomyces sp., Inhibits Melanogenesis by Downregulating Melanogenic Proteins via Inactivation of cAMP/PKA/CREB Signaling. International Journal of Molecular Sciences. 2022; 23(23):14922. https://doi.org/10.3390/ijms232314922
Chicago/Turabian StyleLim, Su-Jin, Da-Won Jung, Prima F. Hillman, Sang-Jip Nam, and Chang-Seok Lee. 2022. "SNA077, an Extract of Marine Streptomyces sp., Inhibits Melanogenesis by Downregulating Melanogenic Proteins via Inactivation of cAMP/PKA/CREB Signaling" International Journal of Molecular Sciences 23, no. 23: 14922. https://doi.org/10.3390/ijms232314922