Bone morphogenetic proteins differentially regulate pigmentation in human skin cells

Journal of Cell Science

Volumn 125, Issue 18, 2012, Pages 4306-4319

  Singh, Suman K ^a   Abbas, Waqas A ^a   Tobin, Desmond J ^a  

^a UNIVERSITY OF BRADFORD   (United Kingdom)

Author keywords

Melanin transfer; Noggin; Pigmentation; Sclerostin; UV radiation

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN RECEPTOR 1A; MELANIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOPHENOL MONOOXYGENASE; MYOSIN; MYOSIN X; NOGGIN; PHOSPHATIDYLINOSITOL 3 KINASE; SCLEROSTIN; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN;

ARTICLE; CELL FUNCTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; KERATINOCYTE; MELANOCYTE; MELANOGENESIS; MELANOSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SKIN CELL; SKIN PIGMENTATION; UPREGULATION;

ADULT; AGED; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN RECEPTORS; COCULTURE TECHNIQUES; EPIDERMIS; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; KERATINOCYTES; MELANINS; MELANOCYTES; MIDDLE AGED; MODELS, BIOLOGICAL; MONOPHENOL MONOOXYGENASE; MYOSINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PIGMENTATION; PSEUDOPODIA; SIGNAL TRANSDUCTION; SKIN; SMAD PROTEINS; ULTRAVIOLET RAYS; UP-REGULATION;

EID: 84872201612     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.102038     Document Type: Article

References (57)

1. Adam, L., Vadlamudi, R., Kondapaka, S. B., Chernoff, J., Mendelsohn, J. and Kumar, R. (1998). Heregulin regulates cytoskeletal reorganization and cell migration through the p21-activated kinase-1 via phosphatidylinositol-3 kinase. J. Biol. Chem. 273, 28238-28246.
2. Balemans, W. and Van Hul, W. (2002). Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev. Biol. 250, 231-250.
3. Beaumont, K. A., Hamilton, N. A., Moores, M. T., Brown, D. L., Ohbayashi, N., Cairncross, O., Cook, A. L., Smith, A. G., Misaki, R., Fukuda, M. et al. (2011). The recycling endosome protein Rab17 regulates melanocytic filopodia formation and melanosome trafficking. Traffic 12, 627-643.
4. Bohil, A. B., Robertson, B. W. and Cheney, R. E. (2006). Myosin-X is a molecular motor that functions in filopodia formation. Proc. Natl. Acad. Sci. USA 103, 12411-12416.
5. Botchkarev, V. A. (2003). Bone morphogenetic proteins and their antagonists in skin and hair follicle biology. J. Invest. Dermatol. 120, 36-47.
6. Botchkarev, V. A. and Sharov, A. A. (2004). BMP signaling in the control of skin development and hair follicle growth. Differentiation 72, 512-526.
7. Botchkarev, V. A., Botchkareva, N. V., Roth, W., Nakamura, M., Chen, L. H., Herzog, W., Lindner, G., McMahon, J. A., Peters, C., Lauster, R. et al. (1999). Noggin is a mesenchymally derived stimulator of hair-follicle induction. Nat. Cell Biol. 1, 158-164.
8. Botchkarev, V. A., Botchkareva, N. V., Nakamura, M., Huber, O., Funa, K., Lauster, R., Paus, R. and Gilchrest, B. A. (2001). Noggin is required for induction of the hair follicle growth phase in postnatal skin. FASEB J. 15, 2205-2214.
9. Byers, H. R., Yaar, M., Eller, M. S., Jalbert, N. L. and Gilchrest, B. A. (2000). Role of cytoplasmic dynein in melanosome transport in human melanocytes. J. Invest. Dermatol. 114, 990-997.
10. Cox, D., Berg, J. S., Cammer, M., Chinegwundoh, J. O., Dale, B. M., Cheney, R. E. and Greenberg, S. (2002). Myosin X is a downstream effector of PI(3)K during phagocytosis. Nat. Cell Biol. 4, 469-477.
11. Eller, M. S. and Gilchrest, B. A. (2000). Tanning as part of the eukaryotic SOS response. Pigment Cell Res. 13 Suppl. 8, 94-97.
12. Friedmann, P. S. and Gilchrest, B. A. (1987). Ultraviolet radiation directly induces pigment production by cultured human melanocytes. J. Cell. Physiol. 133, 88-94.
13. Gadea, G., Roger, L., Anguille, C., de Toledo, M., Gire, V. and Roux, P. (2004). TNFalpha induces sequential activation of Cdc42- and p38/p53-dependent pathways that antagonistically regulate filopodia formation. J. Cell Sci. 117, 6355-6364.
14. Galibert, M. D., Carreira, S. and Goding, C. R. (2001). The Usf-1 transcription factor is a novel target for the stress-responsive p38 kinase and mediates UV-induced Tyrosinase expression. EMBO J. 20, 5022-5031.
15. Gilboa, L., Nohe, A., Geissendörfer, T., Sebald, W., Henis, Y. I. and Knaus, P. (2000). Bone morphogenetic protein receptor complexes on the surface of live cells: a new oligomerization mode for serine/threonine kinase receptors. Mol. Biol. Cell 11, 1023-1035.
16. Goto, K., Kamiya, Y., Imamura, T., Miyazono, K. and Miyazawa, K. (2007). Selective inhibitory effects of Smad6 on bone morphogenetic protein type I receptors. J. Biol. Chem. 282, 20603-20611.
17. Herpin, A. and Cunningham, C. (2007). Cross-talk between the bone morphogenetic protein pathway and other major signaling pathways results in tightly regulated cellspecific outcomes. FEBS J. 274, 2977-2985.
18. Hruska, K. A., Mathew, S. and Saab, G. (2005). Bone morphogenetic proteins in vascular calcification. Circ. Res. 97, 105-114.
19. Javelaud, D. and Mauviel, A. (2005). Crosstalk mechanisms between the mitogenactivated protein kinase pathways and Smad signaling downstream of TGF-beta: implications for carcinogenesis. Oncogene 24, 5742-5750.
20. Kauser, S., Schallreuter, K. U., Thody, A. J., Gummer, C. and Tobin, D. J. (2003). Regulation of human epidermal melanocyte biology by beta-endorphin. J. Invest. Dermatol. 120, 1073-1080.
21. Lavery, K., Swain, P., Falb, D. and Alaoui-Ismaili, M. H. (2008). BMP-2/4 and BMP-6/7 differentially utilize cell surface receptors to induce osteoblastic differentiation of human bone marrow-derived mesenchymal stem cells. J. Biol. Chem. 283, 20948-20958.
22. Mansky, K. C., Sankar, U., Han, J. and Ostrowski, M. C. (2002). Microphthalmia transcription factor is a target of the p38 MAPK pathway in response to receptor activator of NF-kappa B ligand signaling. J. Biol. Chem. 277, 11077-11083.
23. Marks, M. S. and Seabra, M. C. (2001). The melanosome: membrane dynamics in black and white. Nat. Rev. Mol. Cell Biol. 2, 738-748.
24. Menna, E., Disanza, A., Cagnoli, C., Schenk, U., Gelsomino, G., Frittoli, E., Hertzog, M., Offenhauser, N., Sawallisch, C., Kreienkamp, H. J. et al. (2009). Eps8 regulates axonal filopodia in hippocampal neurons in response to brain-derived neurotrophic factor (BDNF). PLoS Biol. 7, e1000138.
25. Miyazono, K. (2008). Regulation of TGF-b family signaling by inhibitory Smads. In The TGF-b Family (ed. R. Derynck and K. Miyazono), pp. 363-388. New York: Cold Spring Harbor Laboratory Press.
26. Miyazono, K., Maeda, S. and Imamura, T. (2005). BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. Cytokine Growth Factor Rev. 16, 251-263.
27. Miyazono, K., Kamiya, Y. and Morikawa, M. (2010). Bone morphogenetic protein receptors and signal transduction. J. Biochem. 147, 35-51.
28. Müller, F., Rohrer, H. and Vogel-Höpker, A. (2007). Bone morphogenetic proteins specify the retinal pigment epithelium in the chick embryo. Development 134, 3483-3493.
29. Nohe, A., Hassel, S., Ehrlich, M., Neubauer, F., Sebald, W., Henis, Y. I. and Knaus, P. (2002). The mode of bone morphogenetic protein (BMP) receptor oligomerization determines different BMP-2 signaling pathways. J. Biol. Chem. 277, 5330-5338.
30. Nohe, A., Keating, E., Knaus, P. and Petersen, N. O. (2004). Signal transduction of bone morphogenetic protein receptors. Cell. Signal. 16, 291-299.
31. Osyczka, A. M. and Leboy, P. S. (2005). Bone morphogenetic protein regulation of early osteoblast genes in human marrow stromal cells is mediated by extracellular signal-regulated kinase and phosphatidylinositol 3-kinase signaling. Endocrinology 146, 3428-3437.
32. Park, H. Y., Wu, C., Yaar, M., Stachur, C. M., Kosmadaki, M. and Gilchrest, B. A. (2009a). Role of BMP-4 and Its Signaling Pathways in Cultured Human Melanocytes. Int. J. Cell Biol. 2009, 750482.
33. Park, H. Y., Kosmadaki, M., Yaar, M. and Gilchrest, B. A. (2009b). Cellular mechanisms regulating human melanogenesis. Cell. Mol. Life Sci. 66, 1493-1506.
34. Pi, X., Ren, R., Kelley, R., Zhang, C., Moser, M., Bohil, A. B., Divito, M., Cheney, R. E. and Patterson, C. (2007). Sequential roles for myosin-X in BMP6-dependent filopodial extension, migration, and activation of BMP receptors. J. Cell Biol. 179, 1569-1582.
35. Plonka, P. M., Passeron, T., Brenner, M., Tobin, D. J., Shibahara, S., Thomas, A., Slominski, A., Kadekaro, A. L., Hershkovitz, D., Peters, E. et al. (2009). What are melanocytes really doing all day long...? Exp. Dermatol. 18, 799-819.
36. Rustom, A., Saffrich, R., Markovic, I., Walther, P. and Gerdes, H. H. (2004). Nanotubular highways for intercellular organelle transport. Science 303, 1007-1010.
37. Saha, B., Singh, S. K., Sarkar, C., Bera, R., Ratha, J., Tobin, D. J. and Bhadra, R. (2006). Activation of the Mitf promoter by lipid-stimulated activation of p38-stress signalling to CREB. Pigment Cell Res. 19, 595-605.
38. Scott, G., Leopardi, S., Printup, S. and Madden, B. C. (2002). Filopodia are conduits for melanosome transfer to keratinocytes. J. Cell Sci. 115, 1441-1451.
39. Seiberg, M., Paine, C., Sharlow, E., Andrade-Gordon, P., Costanzo, M., Eisinger, M. and Shapiro, S. S. (2000). The protease-activated receptor 2 regulates pigmentation via keratinocyte-melanocyte interactions. Exp. Cell Res. 254, 25-32.
40. Sharov, A. A., Fessing, M., Atoyan, R., Sharova, T. Y., Haskell-Luevano, C., Weiner, L., Funa, K., Brissette, J. L., Gilchrest, B. A. and Botchkarev, V. A. (2005). Bone morphogenetic protein (BMP) signaling controls hair pigmentation by means of cross-talk with the melanocortin receptor-1 pathway. Proc. Natl. Acad. Sci. USA 102, 93-98.
41. Sharov, A. A., Sharova, T. Y., Mardaryev, A. N., Tommasi di Vignano, A., Atoyan, R., Weiner, L., Yang, S., Brissette, J. L., Dotto, G. P. and Botchkarev, V. A. (2006). Bone morphogenetic protein signaling regulates the size of hair follicles and modulates the expression of cell cycle-associated genes. Proc. Natl. Acad. Sci. USA 103, 18166-18171.
42. Shibahara, S., Takeda, K., Yasumoto, K., Udono, T., Watanabe, K., Saito, H. and Takahashi, K. (2001). Microphthalmia-associated transcription factor (MITF): multiplicity in structure, function, and regulation. J. Investig. Dermatol. Symp. Proc. 6, 99-104.
43. Singh, S. K., Sarkar, C., Mallick, S., Saha, B., Bera, R. and Bhadra, R. (2005). Human placental lipid induces melanogenesis through p38 MAPK in B16F10 mouse melanoma. Pigment Cell Res. 18, 113-121.
44. Singh, S. K., Nizard, C., Kurfurst, R., Bonte, F., Schnebert, S. and Tobin, D. J. (2008). The silver locus product (Silv/gp100/Pmel17) as a new tool for the analysis of melanosome transfer in human melanocyte-keratinocyte co-culture. Exp. Dermatol. 17, 418-426.
45. Singh, S. K., Kurfurst, R., Nizard, C., Schnebert, S., Perrier, E. and Tobin, D. J. (2010). Melanin transfer in human skin cells is mediated by filopodia-a model for homotypic and heterotypic lysosome-related organelle transfer. FASEB J. 24, 3756-3769.
46. ten Dijke, P., Miyazono, K. and Heldin, C. H. (1996). Signaling via hetero-oligomeric complexes of type I and type II serine/threonine kinase receptors. Curr. Opin. Cell Biol. 8, 139-145.
47. Tobin, D. J. (2008). Human hair pigmentation-biological aspects. Int. J. Cosmet. Sci. 30, 233-257.
48. Tokuo, H., Mabuchi, K. and Ikebe, M. (2007). The motor activity of myosin-X promotes actin fiber convergence at the cell periphery to initiate filopodia formation. J. Cell Biol. 179, 229-238.
49. Trichet, L., Sykes, C. and Plastino, J. (2008). Relaxing the actin cytoskeleton for adhesion and movement with Ena/VASP. J. Cell Biol. 181, 19-25.
50. Vadlamudi, R., Adam, L., Talukder, A., Mendelsohn, J. and Kumar, R. (1999). Serine phosphorylation of paxillin by heregulin-b1: role of p38 mitogen activated protein kinase. Oncogene 18, 7253-7264.
51. Van Den Bossche, K., Naeyaert, J. M. and Lambert, J. (2006). The quest for the mechanism of melanin transfer. Traffic 7, 769-778.
52. Vance, K. W. and Goding, C. R. (2004). The transcription network regulating melanocyte development and melanoma. Pigment Cell Res. 17, 318-325.
53. Vancoillie, G., Lambert, J., Mulder, A., Koerten, H. K., Mommaas, A. M., Van Oostveldt, P. and Naeyaert, J. M. (2000). Kinesin and kinectin can associate with the melanosomal surface and form a link with microtubules in normal human melanocytes. J. Invest. Dermatol. 114, 421-429.
54. Vidulescu, C., Clejan, S. and O'connor, K. C. (2004). Vesicle traffic through intercellular bridges in DU 145 human prostate cancer cells. J. Cell. Mol. Med. 8, 388-396.
55. Virador, V. M., Muller, J., Wu, X., Abdel-Malek, Z. A., Yu, Z. X., Ferrans, V. J., Kobayashi, N., Wakamatsu, K., Ito, S., Hammer, J. A. et al. (2002). Influence of alpha-melanocyte-stimulating hormone and ultraviolet radiation on the transfer of melanosomes to keratinocytes. FASEB J. 16, 105-107.
56. Yaar, M., Wu, C., Park, H. Y., Panova, I., Schutz, G. and Gilchrest, B. A. (2006). Bone morphogenetic protein-4, a novel modulator of melanogenesis. J. Biol. Chem. 281, 25307-25314.
57. Zhang, R. Z., Zhu, W. Y., Xia, M. Y. and Feng, Y. (2004). Morphology of cultured human epidermal melanocytes observed by atomic force microscopy. Pigment Cell Res. 17, 62-65.