Melanogenesis in uveal melanoma cells: Effect of argan oil Corrigendum in /10.3892/ijmm.2023.5308

Caporarello,Nunzia; Olivieri,Melania; Cristaldi,Martina; Rusciano,Dario; Lupo,Gabriella; Anfuso,Carmelina  Daniela

doi:10.3892/ijmm.2017.3104

Melanogenesis in uveal melanoma cells: Effect of argan oil

Corrigendum in: /10.3892/ijmm.2023.5308

Authors:
- Nunzia Caporarello
- Melania Olivieri
- Martina Cristaldi
- Dario Rusciano
- Gabriella Lupo
- Carmelina Daniela Anfuso
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Affiliations: Department of Biomedical and Biotechnological Sciences, Section of Medical Biochemistry, University of Catania, I-95123 Catania, Italy, Sooft Italia S.p.A., Rome, Italy
Published online on: August 23, 2017 https://doi.org/10.3892/ijmm.2017.3104
Pages: 1277-1284

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Abstract

The mechanisms underlying cutaneous melanogenesis have been widely studied; however, very little is known about uveal melanogenesis. Melanin is normally produced by uveal melanocytes and gives the color to the iris. A derangement from this normal production may occur, for instance, by iatrogenic events, such as glaucoma therapy with prostaglandins that may enhance cutaneous and iris pigmentation. In this study, we investigated the mechanisms that regulate uveal melanogenesis in human uveal melanoma cells (92.1) and murine cutaneous melanoma cells (B16-F1). In the first part of the study, we compared the effects of known cutaneous pigmenting agents on the B16-F1 and 92.1 cells, showing an opposite response of the two cell lines. Subsequently, using argan oil, a known depigmenting agent for murine cutaneous melanoma cells, on 92.1 cells, we found that in these cells, it also functioned as an inhibitor of melanogenesis and tyrosinase expression. From a molecular perspective, treatment of the 92.1 cells with argan oil decreased melanogenesis-associated transcription factor (MITF) gene expression by inducing MITF phosphorylation at Ser73, thus leading to MITF ubiquitination and disposal. It also led to the downregulation of the extracellular signal-regulated kinase (ERK)1/2 and Akt pathways, also known to be involved in cutaneous melanogenesis, although with an opposing function. Taken together, our data indicate that: ⅰ) some differences exist in the regulation of melanogenesis between cutaneous and uveal melanoma cells; and ⅱ) argan oil exerts a depigmenting effect on 92.1 cells through its action on the ERK1/2 and Akt pathways.

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1	Plonka PM, Passeron T, Brenner M, Tobin DJ, Shibahara S, Thomas A, Slominski A, Kadekaro AL, Hershkovitz D, Peters E, et al: What are melanocytes really doing all day long…? Exp Dermatol. 18:799–819. 2009. View Article : Google Scholar : PubMed/NCBI
2	Tachibana M: Sound needs sound melanocytes to be heard. Pigment Cell Res. 12:344–354. 1999. View Article : Google Scholar : PubMed/NCBI
3	Brito FC and Kos L: Timeline and distribution of melanocyte precursors in the mouse heart. Pigment Cell Melanoma Res. 21:464–470. 2008. View Article : Google Scholar : PubMed/NCBI
4	Hu DN, Simon JD and Sarna T: Role of ocular melanin in ophthalmic physiology and pathology. Photochem Photobiol. 84:639–644. 2008. View Article : Google Scholar : PubMed/NCBI
5	Randhawa M, Huff T, Valencia JC, Younossi Z, Chandhoke V, Hearing VJ and Baranova A: Evidence for the ectopic synthesis of melanin in human adipose tissue. FASEB J. 23:835–843. 2009. View Article : Google Scholar :
6	Suzuki I, Cone RD, Im S, Nordlund J and Abdel-Malek ZA: Binding of melanotropic hormones to the melanocortin receptor MC1R on human melanocytes stimulates proliferation and melanogenesis. Endocrinology. 137:1627–1633. 1996. View Article : Google Scholar : PubMed/NCBI
7	Olivares C and Solano F: New insights into the active site structure and catalytic mechanism of tyrosinase and its related proteins. Pigment Cell Melanoma Res. 22:750–760. 2009. View Article : Google Scholar : PubMed/NCBI
8	Costin GE and Hearing VJ: Human skin pigmentation: Melanocytes modulate skin color in response to stress. FASEB J. 21:976–994. 2007. View Article : Google Scholar : PubMed/NCBI
9	Oka M, Kageyama A, Fukunaga M, Bito T, Nagai H and Nishigori C: Phosphatidylinositol 3-kinase/Akt-dependent and -independent protection against apoptosis in normal human melanocytes. J Invest Dermatol. 123:930–936. 2004. View Article : Google Scholar : PubMed/NCBI
10	Hemesath TJ, Price ER, Takemoto C, Badalian T and Fisher DE: MAP kinase links the transcription factor Microphthalmia to c-Kit signalling in melanocytes. Nature. 391:298–301. 1998. View Article : Google Scholar : PubMed/NCBI
11	Slominski A, Tobin DJ, Shibahara S and Wortsman J: Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol Rev. 84:1155–1228. 2004. View Article : Google Scholar : PubMed/NCBI
12	Bae JS, Han M, Yao C and Chung JH: Chaetocin inhibits IBMX-induced melanogenesis in B16F10 mouse melanoma cells through activation of ERK. Chem Biol Interact. 245:66–71. 2016. View Article : Google Scholar : PubMed/NCBI
13	Jeong HS, Gu GE, Jo AR, Bang JS, Yun HY, Baek KJ, Kwon NS, Park KC and Kim DS: Baicalin-induced Akt activation decreases melanogenesis through downregulation of microphthalmia-associated transcription factor and tyrosinase. Eur J Pharmacol. 761:19–27. 2015. View Article : Google Scholar : PubMed/NCBI
14	Li L, Hu DN, Zhao H, McCormick SA, Nordlund JJ and Boissy RE: Uveal melanocytes do not respond to or express receptors for α-melanocyte-stimulating hormone. Invest Ophthalmol Vis Sci. 47:4507–4512. 2006. View Article : Google Scholar : PubMed/NCBI
15	Hu DN, Stjernschantz J and McCormick SA: Effect of prostaglandins A₂, E₁ F_2 α and latanoprost on cultured human iridal melanocytes. Exp Eye Res. 70:113–120. 2000. View Article : Google Scholar : PubMed/NCBI
16	Hamid MA, Sarmidi MR and Park CS: Mangosteen leaf extract increases melanogenesis in B16F1 melanoma cells by stimulating tyrosinase activity in vitro and by up-regulating tyrosinase gene expression. Int J Mol Med. 29:209–217. 2012.
17	Li X, Guo L, Sun Y, Zhou J, Gu Y and Li Y: Baicalein inhibits melanogenesis through activation of the ERK signaling pathway. Int J Mol Med. 25:923–927. 2010. View Article : Google Scholar : PubMed/NCBI
18	Guo H, Yang K, Deng F, Xing Y, Li Y, Lian X and Yang T: Wnt3a inhibits proliferation but promotes melanogenesis of melan-a cells. Int J Mol Med. 30:636–642. 2012. View Article : Google Scholar : PubMed/NCBI
19	Lv N, Koo JH, Yoon HY, Yu J, Kim KA, Choi IW, Kwon KB, Kwon KS, Kim HU, Park JW, et al: Effect of Angelica gigas extract on melanogenesis in B16 melanoma cells. Int J Mol Med. 20:763–767. 2007.PubMed/NCBI
20	Huang HC, Lin H and Huang MC: The lactoferricin B-derived peptide, LfB17-34, induces melanogenesis in B16F10 cells. Int J Mol Med. 39:595–602. 2017. View Article : Google Scholar : PubMed/NCBI
21	Solano F, Briganti S, Picardo M and Ghanem G: Hypopigmenting agents: An updated review on biological, chemical and clinical aspects. Pigment Cell Res. 19:550–571. 2006. View Article : Google Scholar : PubMed/NCBI
22	Villareal MO, Kume S, Bourhim T, Bakhtaoui FZ, Kashiwagi K, Han J, Gadhi C and Isoda H: Activation of MITF by argan oil leads to the inhibition of the tyrosinase and dopachrome tautomerase expressions in B16 murine melanoma cells. Evid Based Complement Alternat Med. 2013:3401072013. View Article : Google Scholar : PubMed/NCBI
23	Anfuso CD, Motta C, Giurdanella G, Arena V, Alberghina M and Lupo G: Endothelial PKCα-MAPK/ERK-phospholipase A₂ pathway activation as a response of glioma in a triple culture model. A new role for pericytes? Biochimie. 99:77–87. 2014. View Article : Google Scholar
24	Anfuso CD, Giurdanella G, Motta C, Muriana S, Lupo G, Ragusa N and Alberghina M: PKCα-MAPK/ERK-phospholipase A₂ signaling is required for human melanoma-enhanced brain endothelial cell proliferation and motility. Microvasc Res. 78:338–357. 2009. View Article : Google Scholar : PubMed/NCBI
25	Rusciano D, Lorenzoni P, Lin S and Burger MM: Hepatocyte growth factor/scatter factor and hepatocytes are potent downregulators of tyrosinase expression in B16 melanoma cells. J Cell Biochem. 71:264–276. 1998. View Article : Google Scholar : PubMed/NCBI
26	Lupo G, Anfuso CD, Ragusa N, Tirolo C, Marchetti B, Gili E, La Rosa C and Vancheri C: Activation of cytosolic phospholipase A₂ and 15-lipoxygenase by oxidized low-density lipoproteins in cultured human lung fibroblasts. Biochim Biophys Acta. 1771:522–532. 2007. View Article : Google Scholar : PubMed/NCBI
27	Giurdanella G, Anfuso CD, Olivieri M, Lupo G, Caporarello N, Eandi CM, Drago F, Bucolo C and Salomone S: Aflibercept, bevacizumab and ranibizumab prevent glucose-induced damage in human retinal pericytes in vitro, through a PLA₂/COX-2/VEGF-A pathway. Biochem Pharmacol. 96:278–287. 2015. View Article : Google Scholar : PubMed/NCBI
28	Scuderi MR, Anfuso CD, Lupo G, Motta C, Romeo L, Guerra L, Cappellani A, Ragusa N, Cantarella G and Alberghina M: Expression of Ca²⁺ -independent and Ca²⁺ -dependent phospholipases A₂ and cyclooxygenases in human melanocytes and malignant melanoma cell lines. Biochim Biophys Acta. 1781:635–642. 2008. View Article : Google Scholar : PubMed/NCBI
29	Cheli Y, Luciani F, Khaled M, Beuret L, Bille K, Gounon P, Ortonne JP, Bertolotto C and Ballotti R: αMSH and cyclic AMP elevating agents control melanosome pH through a protein kinase A-independent mechanism. J Biol Chem. 284:18699–18706. 2009. View Article : Google Scholar : PubMed/NCBI
30	Englaro W, Bertolotto C, Buscà R, Brunet A, Pagès G, Ortonne JP and Ballotti R: Inhibition of the mitogen-activated protein kinase pathway triggers B16 melanoma cell differentiation. J Biol Chem. 273:9966–9970. 1998. View Article : Google Scholar : PubMed/NCBI
31	Hah YS, Cho HY, Lim TY, Park DH, Kim HM, Yoon J, Kim JG, Kim CY and Yoon TJ: Induction of melanogenesis by rapamycin in human MNT-1 melanoma cells. Ann Dermatol. 24:151–157. 2012. View Article : Google Scholar : PubMed/NCBI
32	Hu DN, Ritch R, McCormick SA and Pelton-Henrion K: Isolation and cultivation of human iris pigment epithelium. Invest Ophthalmol Vis Sci. 33:2443–2453. 1992.PubMed/NCBI
33	Eagle RC Jr: Iris pigmentation and pigmented lesions: An ultrastructural study. Trans Am Ophthalmol Soc. 86:581–687. 1988.PubMed/NCBI
34	Imesch PD, Bindley CD, Khademian Z, Ladd B, Gangnon R, Albert DM and Wallow IH: Melanocytes and iris color. Electron microscopic findings. Arch Ophthalmol. 114:443–447. 1996. View Article : Google Scholar : PubMed/NCBI
35	Wilkerson CL, Syed NA, Fisher MR, Robinson NL, Wallow IH and Albert DM: Melanocytes and iris color. Light microscopic findings. Arch Ophthalmol. 114:437–442. 1996. View Article : Google Scholar : PubMed/NCBI
36	Hu DN: Regulation of growth and melanogenesis of uveal melanocytes. Pigment Cell Res. 13(Suppl 8): 81–86. 2000. View Article : Google Scholar : PubMed/NCBI
37	Bito LZ, Matheny A, Cruickshanks KJ, Nondahl DM and Carino OB: Eye color changes past early childhood. The Louisville Twin Study. Arch Ophthalmol. 115:659–663. 1997. View Article : Google Scholar : PubMed/NCBI
38	Wistrand PJ, Stjernschantz J and Olsson K: The incidence and time-course of latanoprost-induced iridial pigmentation as a function of eye color. Surv Ophthalmol. 41(Suppl 2): S129–S138. 1997. View Article : Google Scholar : PubMed/NCBI
39	Seiberg M: Keratinocyte-melanocyte interactions during melanosome transfer. Pigment Cell Res. 14:236–242. 2001. View Article : Google Scholar : PubMed/NCBI
40	Hu DN, McCormick SA, Seedor JA, Ritterband DC and Shah MK: Isolation, purification and cultivation of conjunctival melanocytes. Exp Eye Res. 84:655–662. 2007. View Article : Google Scholar : PubMed/NCBI
41	Bassi MT, Schiaffino MV, Renieri A, De Nigris F, Galli L, Bruttini M, Gebbia M, Bergen AA, Lewis RA and Ballabio A: Cloning of the gene for ocular albinism type 1 from the distal short arm of the X chromosome. Nat Genet. 10:13–19. 1995. View Article : Google Scholar : PubMed/NCBI
42	Kim HJ, Kim IS, Dong Y, Lee IS, Kim JS, Kim JS, Woo JT and Cha BY: Melanogenesis-inducing effect of cirsimaritin through increases in microphthalmia-associated transcription factor and tyrosinase expression. Int J Mol Sci. 16:8772–8788. 2015. View Article : Google Scholar : PubMed/NCBI
43	Onken MD, Li J and Cooper JA: Uveal melanoma cells utilize a novel route for transendothelial migration. PLoS One. 9:e1154722014. View Article : Google Scholar : PubMed/NCBI
44	Samane S, Noël J, Charrouf Z, Amarouch H and Haddad PS: Insulin-sensitizing and anti-proliferative effects of Argania spinosa seed extracts. Evid Based Complement Alternat Med. 3:317–327. 2006. View Article : Google Scholar : PubMed/NCBI
45	Mitchell P, Smith W and Wang JJ: Iris color, skin sun sensitivity, and age-related maculopathy. The Blue Mountains Eye Study. Ophthalmology. 105:1359–1363. 1998. View Article : Google Scholar : PubMed/NCBI