Autophagy induction can regulate skin pigmentation by causing melanosome degradation in keratinocytes and melanocytes.
Administration, Topical
Autophagosomes
/ drug effects
Autophagy
/ drug effects
Autophagy-Related Protein-1 Homolog
/ metabolism
Beclin-1
/ metabolism
Dipeptides
/ administration & dosage
Epidermis
/ drug effects
Humans
Intracellular Signaling Peptides and Proteins
/ metabolism
Keratinocytes
/ metabolism
Melanins
/ biosynthesis
Melanocytes
/ metabolism
Melanosomes
/ metabolism
Phosphorylation
/ drug effects
Skin Pigmentation
/ drug effects
autophagy
melanocyte
melanogenesis
melanosome degradation
skin pigmentation
Journal
Pigment cell & melanoma research
ISSN: 1755-148X
Titre abrégé: Pigment Cell Melanoma Res
Pays: England
ID NLM: 101318927
Informations de publication
Date de publication:
05 2020
05 2020
Historique:
received:
25
02
2019
revised:
07
10
2019
accepted:
24
10
2019
pubmed:
30
10
2019
medline:
5
2
2021
entrez:
30
10
2019
Statut:
ppublish
Résumé
Autophagy regulates cellular turnover by disassembling unnecessary or dysfunctional constituents. Recent studies demonstrated that autophagy and its regulators play a wide variety of roles in melanocyte biology. Activation of autophagy is known to induce melanogenesis and regulate melanosome biogenesis in melanocytes. Also, autophagy induction was reported to regulate physiologic skin color via melanosome degradation, although the downstream effectors are not yet clarified. To determine the role of autophagy as a melanosome degradation machinery, we administered several autophagy inducers in human keratinocytes and melanocytes. Our results showed that the synthetic autophagy inducer PTPD-12 stimulated autophagic flux in human melanocytes and in keratinocytes containing transferred melanosomes. Increased autophagic flux led to melanosome degradation without affecting the expression of MITF. Furthermore, the color of cell pellets of both melanocytes and keratinocytes was visibly lightened. Inhibition of autophagic flux by chloroquine resulted in marked attenuation of PTPD-12-induced melanosome degradation, whereas the expression of melanogenesis pathway genes and proteins remained unaffected. Taken together, our results suggest that the modulation of autophagy can contribute to the regulation of melanocyte biology and skin pigmentation.
Substances chimiques
Beclin-1
0
Dipeptides
0
Intracellular Signaling Peptides and Proteins
0
Melanins
0
PTPD-12
0
Autophagy-Related Protein-1 Homolog
EC 2.7.11.1
ULK1 protein, human
EC 2.7.11.1
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
403-415Informations de copyright
© 2019 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
Références
Ando, H., Kondoh, H., Ichihashi, M., & Hearing, V. J. (2007). Approaches to identify inhibitors of melanin biosynthesis via the quality control of tyrosinase. Journal of Investigative Dermatology, 127(4), 751-761. https://doi.org/10.1038/sj.jid.5700683
Babiarz-Magee, L., Chen, N., Seiberg, M., & Lin, C. B. (2004). The expression and activation of protease-activated receptor-2 correlate with skin color. Pigment Cell Research, 17(3), 241-251. https://doi.org/10.1111/j.1600-0749.2004.00133.x
Boissy, R. E., Liu, Y. Y., Medrano, E. E., & Nordlund, J. J. (1991). Structural-aberration of the rough endoplasmic-reticulum and melanosome compartmentalization in long-term cultures of melanocytes from vitiligo patients. Journal of Investigative Dermatology, 97(3), 395-404. https://doi.org/10.1111/1523-1747.ep12480976
Correia, M. S., Moreiras, H., Pereira, F. J. C., Neto, M. V., Festas, T. C., Tarafder, A. K., … Barral, D. C. (2018). Melanin transferred to keratinocytes resides in nondegradative endocytic compartments. Journal of Investigative Dermatology, 138(3), 637-646. https://doi.org/10.1016/j.jid.2017.09.042
Ebanks, J. P., Koshoffer, A., Wickett, R. R., Schwemberger, S., Babcock, G., Hakozaki, T., & Boissy, R. E. (2011). Epidermal keratinocytes from light vs. dark skin exhibit differential degradation of melanosomes. Journal of Investigative Dermatology, 131(6), 1226-1233.
Funderburk, S. F., Wang, Q. J., & Yue, Z. (2010). The Beclin 1-VPS34 complex - at the crossroads of autophagy and beyond. Trends in Cell Biology, 20(6), 355-362. https://doi.org/10.1016/j.tcb.2010.03.002
Ganesan, A. K., Ho, H., Bodemann, B., Petersen, S., Aruri, J., Koshy, S., … White, M. A. (2008). Genome-wide siRNA-based functional genomics of pigmentation identifies novel genes and pathways that impact melanogenesis in human cells. Plos Genetics, 4(12), e1000298. https://doi.org/10.1371/journal.pgen.1000298
Grill, C., Bergsteinsdóttir, K., Ögmundsdóttir, M. H., Pogenberg, V., Schepsky, A., Wilmanns, M., … Steingrímsson, E. (2013). MITF mutations associated with pigment deficiency syndromes and melanoma have different effects on protein function. Human Molecular Genetics, 22(21), 4357-4367. https://doi.org/10.1093/hmg/ddt285
Grimes, P., Nordlund, J. J., Pandya, A. G., Taylor, S., Rendon, M., & Ortonne, J. P. (2006). Increasing our understanding of pigmentary disorders. Journal of the American Academy of Dermatology, 54(5), S255-S261. https://doi.org/10.1016/j.jaad.2005.12.042
Hah, Y.-S., Cho, H. Y., Lim, T.-Y., Park, D. H., Kim, H. M., Yoon, J., … Yoon, T.-J. (2012). Induction of melanogenesis by rapamycin in human MNT-1 melanoma cells. Annals of Dermatology, 24(2), 151-157. https://doi.org/10.5021/ad.2012.24.2.151
Ho, H., & Ganesan, A. K. (2011). The pleiotropic roles of autophagy regulators in melanogenesis. Pigment Cell & Melanoma Research, 24(4), 595-604. https://doi.org/10.1111/j.1755-148X.2011.00889.x
Ho, H., Kapadia, R., Al-Tahan, S., Ahmad, S., & Ganesan, A. (2011a). WIPI1 coordinates melanogenic gene transcription and melanosome formation via TORC1 inhibition. Journal of Investigative Dermatology, 131, S121-S121. https://doi.org/10.1074/jbc.M110.200543
Ho, H., Kapadia, R., Al-Tahan, S., Ahmad, S., & Ganesan, A. K. (2011b). WIPI1 coordinates melanogenic gene transcription and melanosome formation via TORC1 inhibition. Journal of Biological Chemistry, 286(14), 12509-12523. https://doi.org/10.1074/jbc.M110.200543
Hou, L., & Pavan, W. J. (2008). Transcriptional and signaling regulation in neural crest stem cell-derived melanocyte development: Do all roads lead to Mitf? Cell Research, 18(12), 1163-1176. https://doi.org/10.1038/cr.2008.303
Hsu, K.-F., Wu, C.-L., Huang, S.-C., Wu, C.-M., Hsiao, J.-R., Yo, Y.-T., … Chou, C.-Y. (2009). Cathepsin L mediates resveratrol-induced autophagy and apoptotic cell death in cervical cancer cells. Autophagy, 5(4), 451-460. https://doi.org/10.4161/auto.5.4.7666
Hurbain, I., Romao, M., Sextius, P., Bourreau, E., Marchal, C., Bernerd, F., … Raposo, G. (2018). Melanosome distribution in keratinocytes in different skin types: Melanosome clusters are not degradative organelles. Journal of Investigative Dermatology, 138(3), 647-656. https://doi.org/10.1016/j.jid.2017.09.039
Jain, A., Lamark, T., Sjottem, E., Larsen, K. B., Awuh, J. A., Overvatn, A., … Johansen, T. (2010). p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. Journal of Biological Chemistry, 285(29), 22576-22591.
Joseph, P., Klein-Szanto, A. J., & Jaiswal, A. K. (1998). Hydroquinones cause specific mutations and lead to cellular transformation and in vivo tumorigenesis. British Journal of Cancer, 78(3), 312-320. https://doi.org/10.1038/bjc.1998.492
Kalie, E., Razi, M., & Tooze, S. A. (2013). ULK1 regulates melanin levels in MNT-1 cells independently of mTORC1. PLoS ONE, 8(9), e75313. https://doi.org/10.1371/journal.pone.0075313
Katsuyama, Y., Taira, N., Yoshioka, M., Okano, Y., & Masaki, H. (2018). 3-O-Glyceryl-2-O-hexyl ascorbate suppresses melanogenesis through activation of the autophagy system. Biological & Pharmaceutical Bulletin, 41(5), 824-827.
Kim, N. H., Choi, S. H., Yi, N., Lee, T. R., & Lee, A. Y. (2017). Arginase-2, a miR-1299 target, enhances pigmentation in melasma by reducing melanosome degradation via senescence-induced autophagy inhibition. Pigment Cell & Melanoma Research, 30(6), 521-530. https://doi.org/10.1111/pcmr.12605
Kimura, S., Noda, T., & Yoshimori, T. (2007). Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy, 3(5), 452-460. https://doi.org/10.4161/auto.4451
Komatsu, M., Kurokawa, H., Waguri, S., Taguchi, K., Kobayashi, A., Ichimura, Y., … Yamamoto, M. (2010). The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nature Cell Biology, 12(3), 213-223. https://doi.org/10.1038/ncb2021
Kwon, S. H., Lim, C. J., Jung, J., Kim, H. J., Park, K., Shin, J. W., … Na, J. I. (2018). The effect autophagy-enhancing peptide in moisturizer on atopic dermatitis: A randomized controlled trial. Journal of Dermatological Treatment, 30(6), 558-564.
Lim, C. J., Lee, Y.-M., Kang, S. G., Lim, H. W., Shin, K.-O., Jeong, S. K., … Park, K. (2017). Aquatide activation of SIRT1 reduces cellular senescence through a SIRT1-FOXO1-autophagy axis. Biomolecules & Therapeutics, 25(5), 511-518. https://doi.org/10.4062/biomolther.2017.119
Liu, C. C., Lin, Y. C., Chen, Y. H., Chen, C. M., Pang, L. Y., Chen, H. A., … Chen, R. H. (2016). Cul3-KLHL20 ubiquitin ligase governs the turnover of ULK1 and VPS34 complexes to control autophagy termination. Molecular Cell, 61(1), 84-97.
Lo Cicero, A. L., Delevoye, C., Gilles-Marsens, F., Loew, D., Dingli, F., Guéré, C., … Raposo, G. (2015). Exosomes released by keratinocytes modulate melanocyte pigmentation. Nature Communications, 6, 7506. https://doi.org/10.1038/ncomms8506
Marks, M. S., & Seabra, M. C. (2001). The melanosome: Membrane dynamics in black and white. Nature Reviews Molecular Cell Biology, 2(10), 738-748. https://doi.org/10.1038/35096009
Matias, A. R., Ferreira, M., Costa, P., & Neto, P. (2015). Skin colour, skin redness and melanin biometric measurements: Comparison study between Antera((R)) 3D, Mexameter((R)) and Colorimeter((R)). Skin Research and Technology, 21(3), 346-362.
McEwan, D. G., & Dikic, I. (2011). The three musketeers of autophagy: Phosphorylation, ubiquitylation and acetylation. Trends in Cell Biology, 21(4), 195-201. https://doi.org/10.1016/j.tcb.2010.12.006
Miracco, C., Cevenini, G., Franchi, A., Luzi, P., Cosci, E., Mourmouras, V., … Massi, D. (2010). Beclin 1 and LC3 autophagic gene expression in cutaneous melanocytic lesions. Human Pathology, 41(4), 503-512. https://doi.org/10.1016/j.humpath.2009.09.004
Mizushima, N., & Komatsu, M. (2011). Autophagy: Renovation of cells and tissues. Cell, 147(4), 728-741. https://doi.org/10.1016/j.cell.2011.10.026
Mizushima, N., Yoshimori, T., & Levine, B. (2010). Methods in mammalian autophagy research. Cell, 140(3), 313-326. https://doi.org/10.1016/j.cell.2010.01.028
Moscat, J., & Diaz-Meco, M. T. (2009). p62 at the crossroads of autophagy, apoptosis, and cancer. Cell, 137(6), 1001-1004. https://doi.org/10.1016/j.cell.2009.05.023
Murase, D., Hachiya, A., Takano, K., Hicks, R., Visscher, M. O., Kitahara, T., … Yoshimori, T. (2013). Autophagy has a significant role in determining skin color by regulating melanosome degradation in keratinocytes. Journal of Investigative Dermatology, 133(10), 2416-2424. https://doi.org/10.1038/jid.2013.165
Nazarko, V. Y., & Zhong, Q. (2013). ULK1 targets Beclin-1 in autophagy. Nature Cell Biology, 15(7), 727-728. https://doi.org/10.1038/ncb2797
Orlow, S. J., Moran, D., & Boissy, R. E. (1992). Biogenesis of melanosomes - molecular evidence for a melanosomal-lysosomal relationship. Journal of Investigative Dermatology, 98(4), 566-566.
Proikas-Cezanne, T., Waddell, S., Gaugel, A., Frickey, T., Lupas, A., & Nordheim, A. (2004). WIPI-1 alpha (WIPI49), a member of the novel 7-bladed WIPI protein family, is aberrantly expressed in human cancer and is linked to starvation-induced autophagy. Oncogene, 23(58), 9314-9325.
Puissant, A., Fenouille, N., & Auberger, P. (2012). When autophagy meets cancer through p62/SQSTM1. American Journal of Cancer Research, 2(4), 397-413.
Puissant, A., Robert, G., Fenouille, N., Luciano, F., Cassuto, J. P., Raynaud, S., & Auberger, P. (2010). Resveratrol promotes autophagic cell death in chronic myelogenous leukemia cells via JNK-mediated p62/SQSTM1 expression and AMPK activation. Cancer Research, 70(3), 1042-1052. https://doi.org/10.1158/0008-5472.CAN-09-3537
Raposo, G., & Marks, M. S. (2007). Melanosomes-dark organelles enlighten endosomal membrane transport. Nature Reviews Molecular Cell Biology, 8(10), 786-797. https://doi.org/10.1038/nrm2258
Rubinsztein, D. C., Gestwicki, J. E., Murphy, L. O., & Klionsky, D. J. (2007). Potential therapeutic applications of autophagy. Nature Reviews Drug Discovery, 6(4), 304-312. https://doi.org/10.1038/nrd2272
Russell, R. C., Tian, Y. E., Yuan, H., Park, H. W., Chang, Y.-Y., Kim, J., … Guan, K.-L. (2013). ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase. Nature Cell Biology, 15(7), 741-750. https://doi.org/10.1038/ncb2757
Seibenhener, M. L., Geetha, T., & Wooten, M. W. (2007). Sequestosome 1/p62 - more than just a scaffold. FEBS Letters, 581(2), 175-179. https://doi.org/10.1016/j.febslet.2006.12.027
Takizawa, T., Imai, T., Onose, J., Ueda, M., Tamura, T., Mitsumori, K., … Hirose, M. (2004). Enhancement of hepatocarcinogenesis by kojic acid in rat two-stage models after initiation with N-bis(2-hydroxypropyl)nitrosamine or N-diethylnitrosamine. Toxicological Sciences, 81(1), 43-49. https://doi.org/10.1093/toxsci/kfh195
Wataya-Kaneda, M., Tanaka, M., Yang, L., Yang, F., Tsuruta, D., Nakamura, A., … Katayama, I. (2015). Clinical and histologic analysis of the efficacy of topical rapamycin therapy against hypomelanotic macules in tuberous sclerosis complex. JAMA Dermatology, 151(7), 722-730. https://doi.org/10.1001/jamadermatol.2014.4298
Yun, W. J., Kim, E. Y., Park, J. E., Jo, S. Y., Bang, S. H., Chang, E. J., & Chang, S. E. (2016). Microtubule-associated protein light chain 3 is involved in melanogenesis via regulation of MITF expression in melanocytes. Scientific Reports, 6, 19914. https://doi.org/10.1038/srep19914
Zhong, Y., Wang, Q. J., Li, X., Yan, Y., Backer, J. M., Chait, B. T., … Yue, Z. (2009). Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nature Cell Biology, 11(4), 468-476. https://doi.org/10.1038/ncb1854