Establishment of a synchronized tyrosinase transport system revealed a role of Tyrp1 in efficient melanogenesis by promoting tyrosinase targeting to melanosomes.

Journal

Scientific reports

ISSN: 2045-2322

Titre abrégé: Sci Rep

Pays: England

ID NLM: 101563288

Informations de publication

Date de publication:
30 Jan 2024

Historique:

received: 28 11 2023

accepted: 27 01 2024

medline: 31 1 2024

pubmed: 31 1 2024

entrez: 30 1 2024

Statut: epublish

Résumé

Tyrosinase (Tyr) is a key enzyme in the process of melanin synthesis that occurs exclusively within specialized organelles called melanosomes in melanocytes. Tyr is synthesized and post-translationally modified independently of the formation of melanosome precursors and then transported to immature melanosomes by a series of membrane trafficking events that includes endoplasmic reticulum (ER)-to-Golgi transport, post-Golgi trafficking, and endosomal transport. Although several important regulators of Tyr transport have been identified, their precise role in each Tyr transport event is not fully understood, because Tyr is present in several melanocyte organelles under steady-state conditions, thereby precluding the possibility of determining where Tyr is being transported at any given moment. In this study, we established a novel synchronized Tyr transport system in Tyr-knockout B16-F1 cells by using Tyr tagged with an artificial oligomerization domain FM4 (named Tyr-EGFP-FM4). Tyr-EGFP-FM4 was initially trapped at the ER under oligomerized conditions, but at 30 min after chemical dissociation into monomers, it was transported to the Golgi and at 9 h reached immature melanosomes. Melanin was then detected at 12 h after the ER exit of Tyr-EGFP-FM4. By using this synchronized Tyr transport system, we were able to demonstrate that Tyr-related protein 1 (Tyrp1), another melanogenic enzyme, is a positive regulator of efficient Tyr targeting to immature melanosomes. Thus, the synchronized Tyr transport system should serve as a useful tool for analyzing the molecular mechanism of each Tyr transport event in melanocytes as well as in the search for new drugs or cosmetics that artificially regulate Tyr transport.

Identifiants

DOI: 10.1038/s41598-024-53072-6 PMID: 38291221

pubmed: 38291221

doi: 10.1038/s41598-024-53072-6

pii: 10.1038/s41598-024-53072-6

doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

Pagination

2529

Subventions

Organisme : Ministry of Education, Culture, Sports, Science and Technology

ID : 22H02613

Organisme : Japan Science and Technology Agency

ID : JPMJCR17H4

Informations de copyright

Références

Shibahara, S. et al. Cloning and expression of cDNA encoding mouse tyrosinase. Nucleic Acids Res. 14, 2413–2427. https://doi.org/10.1093/nar/14.6.2413 (1986).

doi: 10.1093/nar/14.6.2413 pubmed: 3008090 pmcid: 339673

Hearing, V. J. Determination of melanin synthetic pathways. J. Invest. Dermatol. 131, E8–E11. https://doi.org/10.1038/skinbio.2011.4 (2011).

doi: 10.1038/skinbio.2011.4 pubmed: 22094404 pmcid: 6944209

Tomita, Y. & Suzuki, T. Genetics of pigmentary disorders. Am. J. Med. Genet. C (Semin. Md. Genet.) 131, 75–81. https://doi.org/10.1002/ajmg.c.30036 (2004).

doi: 10.1002/ajmg.c.30036

Fitzpatrick, T. B. & Breathnach, A. S. The epidermal melanin unit system. Dermatol. Wochenschr. 147, 481–489 (1963).

pubmed: 14172128

Byers, H. Melanosome processing in keratinocytes. In The Pigmentary System: Physiology and Pathophysiology 2nd edn (eds Nordlund, J. J. et al.) 181–190 (Wiley, 2007).

Fernandes, B., Cavaco-Paulo, A. & Matamá, T. A comprehensive review of mammalian pigmentation: Paving the way for innovative hair colour-changing cosmetics. Biology 12, 290. https://doi.org/10.3390/biology12020290 (2023).

doi: 10.3390/biology12020290 pubmed: 36829566 pmcid: 9953601

Marks, M. S. & Seabra, M. C. The melanosome: Membrane dynamics in black and white. Nat. Rev. Mol. Cell Biol. 2, 738–748. https://doi.org/10.1038/35096009 (2001).

doi: 10.1038/35096009 pubmed: 11584301

Raposo, G. & Marks, M. S. Melanosomes–dark organelles enlighten endosomal membrane transport. Nat. Rev. Mol. Cell Biol. 8, 786–797. https://doi.org/10.1038/nrm2258 (2007).

doi: 10.1038/nrm2258 pubmed: 17878918 pmcid: 2786984

Bowman, S. L., Bi-Karchin, J., Le, L. & Marks, M. S. The road to lysosome-related organelles: Insights from Hermansky-Pudlak syndrome and other rare diseases. Traffic 20, 404–435. https://doi.org/10.1111/tra.12646 (2019).

doi: 10.1111/tra.12646 pubmed: 30945407 pmcid: 6541516

Delevoye, C., Marks, M. S. & Raposo, G. Lysosome-related organelles as functional adaptations of the endolysosomal system. Curr. Opin. Cell Biol. 59, 147–158. https://doi.org/10.1016/j.ceb.2019.05.003 (2019).

doi: 10.1016/j.ceb.2019.05.003 pubmed: 31234051 pmcid: 6726539

Fukuda, M. Rab GTPases: Key players in melanosome biogenesis, transport, and transfer. Pigment Cell Melanoma Res. 34, 222–235. https://doi.org/10.1111/pcmr.12931 (2021).

doi: 10.1111/pcmr.12931 pubmed: 32997883

Wei, A. H. & Li, W. Hermansky-Pudlak syndrome: Pigmentary and non-pigmentary defects and their pathogenesis. Pigment Cell Melanoma Res. 26, 176–192. https://doi.org/10.1111/pcmr.12051 (2013).

doi: 10.1111/pcmr.12051 pubmed: 23171219

Gerondopoulos, A., Langemeyer, L., Liang, J. R., Linford, A. & Barr, F. A. BLOC-3 mutated in Hermansky-Pudlak syndrome is a Rab32/38 guanine nucleotide exchange factor. Curr. Biol. 22, 2135–2139. https://doi.org/10.1016/j.cub.2012.09.020 (2012).

doi: 10.1016/j.cub.2012.09.020 pubmed: 23084991 pmcid: 3502862

Loftus, S. K. et al. Mutation of melanosome protein RAB38 in chocolate mice. Proc. Natl. Acad. Sci. U. S. A. 99, 4471–4476. https://doi.org/10.1073/pnas.072087599 (2002).

doi: 10.1073/pnas.072087599 pubmed: 11917121 pmcid: 123672

Wasmeier, C. et al. Rab38 and Rab32 control post-Golgi trafficking of melanogenic enzymes. J. Cell Biol. 175, 271–281. https://doi.org/10.1083/jcb.200606050 (2006).

doi: 10.1083/jcb.200606050 pubmed: 17043139 pmcid: 2064568

Ohishi, Y., Kinoshita, R., Marubashi, S., Ishida, M. & Fukuda, M. The BLOC-3 subunit HPS4 is required for activation of Rab32/38 GTPases in melanogenesis, but its Rab9 activity is dispensable for melanogenesis. J. Biol. Chem. 294, 6912–6922. https://doi.org/10.1074/jbc.RA119.007345 (2019).

doi: 10.1074/jbc.RA119.007345 pubmed: 30837268 pmcid: 6497944

Dennis, M. K. et al. BLOC-1 and BLOC-3 regulate VAMP7 cycling to and from melanosomes via distinct tubular transport carriers. J. Cell Biol. 214, 293–308. https://doi.org/10.1083/jcb.201605090 (2016).

doi: 10.1083/jcb.201605090 pubmed: 27482051 pmcid: 4970331

Yu, J. et al. HPS1 regulates the maturation of large dense core vesicles and lysozyme secretion in Paneth cells. Front. Immunol. 11, 560110. https://doi.org/10.3389/fimmu.2020.560110 (2020).

doi: 10.3389/fimmu.2020.560110 pubmed: 33224134 pmcid: 7674556

Rivera, V. M. et al. Regulation of protein secretion through controlled aggregation in the endoplasmic reticulum. Science 287, 826–830. https://doi.org/10.1126/science.287.5454.826 (2000).

doi: 10.1126/science.287.5454.826 pubmed: 10657290

Ishida, M., Marubashi, S. & Fukuda, M. M-INK, a novel tool for visualizing melanosomes and melanocores. J. Biochem. 161, 323–326. https://doi.org/10.1093/jb/mvw100 (2017).

doi: 10.1093/jb/mvw100 pubmed: 28096452

Nishizawa, A., Maruta, Y. & Fukuda, M. Rab32/38-dependent and -independent transport of tyrosinase to melanosomes in B16–F1 melanoma cells. Int. J. Mol. Sci. 23, 14144. https://doi.org/10.3390/ijms232214144 (2022).

doi: 10.3390/ijms232214144 pubmed: 36430618 pmcid: 9695596

Hirschberg, K. et al. Kinetic analysis of secretory protein traffic and characterization of Golgi to plasma membrane transport intermediates in living cells. J. Cell Biol. 143, 1485–1503. https://doi.org/10.1083/jcb.143.6.1485 (1998).

doi: 10.1083/jcb.143.6.1485 pubmed: 9852146 pmcid: 2132993

Hatoyama, Y., Homma, Y., Hiragi, S. & Fukuda, M. Establishment and analysis of conditional Rab1- and Rab5-knockout cells using the auxin-inducible degron system. J. Cell Sci. 134, cs259184. https://doi.org/10.1242/jcs.259184 (2021).

doi: 10.1242/jcs.259184

Bissig, C., Rochin, L. & van Niel, G. PMEL Amyloid fibril formation: The bright steps of pigmentation. Int. J. Mol. Sci. 17, 1438. https://doi.org/10.3390/ijms17091438 (2016).

doi: 10.3390/ijms17091438 pubmed: 27589732 pmcid: 5037717

Kobayashi, T. et al. DHICA oxidase activity of TRP1 and interactions with other melanogenic enzymes. Pigment Cell Res. 7, 227–234. https://doi.org/10.1111/j.1600-0749.1994.tb00054.x (1994).

doi: 10.1111/j.1600-0749.1994.tb00054.x pubmed: 7855068

Kobayashi, T., Imokawa, G., Bennett, D. C. & Hearing, V. J. Tyrosinase stabilization by Tyrp1 (the brown locus protein). J. Biol. Chem. 273, 31801–31805. https://doi.org/10.1074/jbc.273.48.31801 (1998).

doi: 10.1074/jbc.273.48.31801 pubmed: 9822646

Lavinda, O., Manga, P., Orlow, J. & Cardozo, T. Biophysical compatibility of a heterotrimeric tyrosinase-TYRP1-TYRP2 metalloenzyme complex. Front. Pharmacol. 12, 602206. https://doi.org/10.3389/fphar.2021.602206 (2021).

doi: 10.3389/fphar.2021.602206 pubmed: 33995009 pmcid: 8114058

Jiménez-Cervantes, C., Martínez-Esparza, M., Solano, F., Lozano, J. A. & García-Borrón, J. C. Molecular interactions within the melanogenic complex: Formation of heterodimers of tyrosinase and TRP1 from B16 mouse melanoma. Biochem. Biophys. Res. Commun. 253, 761–767. https://doi.org/10.1006/bbrc.1998.9817 (1998).

doi: 10.1006/bbrc.1998.9817 pubmed: 9918801

Huizing, M. et al. AP-3 mediates tyrosinase but not TRP-1 trafficking in human melanocytes. Mol. Biol. Cell 12, 2075–2085. https://doi.org/10.1091/mbc.12.7.2075 (2001).

doi: 10.1091/mbc.12.7.2075 pubmed: 11452004 pmcid: 55657

Chapuy, B. et al. AP-1 and AP-3 mediate sorting of melanosomal and lysosomal membrane proteins into distinct post-Golgi trafficking pathways. Traffic 9, 1157–1172. https://doi.org/10.1111/j.1600-0854.2008.00745.x (2008).

doi: 10.1111/j.1600-0854.2008.00745.x pubmed: 18410487

Tamura, K. et al. Varp is a novel Rab32/38-binding protein that regulates Tyrp1 trafficking in melanocytes. Mol. Biol. Cell 20, 2900–2908. https://doi.org/10.1091/mbc.e08-12-1161 (2009).

doi: 10.1091/mbc.e08-12-1161 pubmed: 19403694 pmcid: 2695797

Yatsu, A., Ohbayashi, N., Tamura, K. & Fukuda, M. Syntaxin-3 is required for melanosomal localization of Tyrp1 in melanocytes. J. Invest. Dermatol. 133, 2237–2246. https://doi.org/10.1038/jid.2013.156 (2013).

doi: 10.1038/jid.2013.156 pubmed: 23549422

Jani, R. A., Purushothaman, L. K., Rani, S., Bergam, P. & Setty, S. R. G. STX13 regulates cargo delivery from recycling endosomes during melanosome biogenesis. J. Cell Sci. 128, 3263–3276. https://doi.org/10.1242/jcs.171165 (2015).

doi: 10.1242/jcs.171165 pubmed: 26208634 pmcid: 4582192

Niki, Y. et al. S-palmitoylation of tyrosinase at cysteine

doi: 10.1016/j.jid.2022.08.040 pubmed: 36063887

Ando, H. et al. Fatty acids regulate pigmentation via proteasomal degradation of tyrosinase: A new aspect of ubiquitin-proteasome function. J. Biol. Chem. 279, 15427–15433. https://doi.org/10.1074/jbc.M313701200 (2004).

doi: 10.1074/jbc.M313701200 pubmed: 14739285

Ando, H., Kondoh, H., Ichihashi, M. & Hearing, V. J. Approaches to identify inhibitors of melanin biosynthesis via the quality control of tyrosinase. J. Invest. Dermatol. 127, 751–761. https://doi.org/10.1038/sj.jid.5700683 (2007).

doi: 10.1038/sj.jid.5700683 pubmed: 17218941

Homma, Y. et al. Comprehensive knockout analysis of the Rab family GTPases in epithelial cells. J. Cell Biol. 218, 2035–2050. https://doi.org/10.1083/jcb.201810134 (2019).

doi: 10.1083/jcb.201810134 pubmed: 31072826 pmcid: 6548125

Katoh, Y., Nozaki, S., Hartanto, D., Miyano, R. & Nakayama, K. Architectures of multisubunit complexes revealed by a visible immuno-precipitation assay using fluorescent fusion proteins. J. Cell Sci. 128, 2351–2362. https://doi.org/10.1242/jcs.168740 (2015).

doi: 10.1242/jcs.168740 pubmed: 25964651