Heparin inhibits melanosome uptake and inflammatory response coupled with phagocytosis through blocking PI3k/Akt and MEK/ERK signaling pathways in human epidermal keratinocytes

Pigment Cell and Melanoma Research

Volumn 27, Issue 6, 2014, Pages 1063-1074

  Makino Okamura, Chieko ^a   Niki, Yoko ^a   Takeuchi, Seiji ^b   Nishigori, Chikako ^b   Declercq, Lieve ^c   Yaroch, Daniel B ^d   Saito, Naoaki ^a  

^a KOBE UNIVERSITY   (Japan)

^b KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c Estée Lauder Companies   (Belgium)

^d Estee Lauder Inc   (United States)

Author keywords

Heparin; Inflammation; Melanosome transfer; Phagocytosis

Indexed keywords

CYCLOOXYGENASE 2; HEPARIN; MITOGEN ACTIVATED PROTEIN KINASE; PROSTAGLANDIN E2; PROTEIN KINASE B; MELANIN; MESSENGER RNA; MICROSPHERE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEINASE ACTIVATED RECEPTOR 2; PTGS2 PROTEIN, HUMAN;

ARTICLE; CELL TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVATION; EPIDERMIS CELL; HUMAN; HUMAN CELL; INFLAMMATION; KERATINOCYTE; MELANOSOME; PHAGOCYTOSIS; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; BIOSYNTHESIS; CYTOLOGY; DRUG EFFECTS; ENZYMOLOGY; EPIDERMIS; FLUORESCENCE; GENETICS; METABOLISM; PATHOLOGY;

CYCLOOXYGENASE 2; DINOPROSTONE; ENZYME ACTIVATION; EPIDERMIS; FLUORESCENCE; HEPARIN; HUMANS; INFLAMMATION; KERATINOCYTES; MAP KINASE SIGNALING SYSTEM; MELANINS; MELANOSOMES; MICROSPHERES; PHAGOCYTOSIS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, PAR-2; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84911394187     PISSN: 17551471     EISSN: 1755148X     Source Type: Journal    
DOI: 10.1111/pcmr.12287     Document Type: Article

References (46)

1. Aderem, A., and Underhill, D.M. (1999). Mechanisms of phagocytosis in macrophages. Annu. Rev. Immunol. 17, 593-623.
2. Ahn, S., Shenoy, S.K., Wei, H., and Lefkowitz, R.J. (2004). Differential kinetic and spatial patterns of beta-arrestin and G protein-mediated ERK activation by the angiotensin II receptor. J. Biol. Chem. 279, 35518-35525.
3. Ando, H., Niki, Y., Yoshida, M., Ito, M., Akiyama, K., Kim, J.H., Yoon, T.J., Lee, J.H., Matsui, M.S., and Ichihashi, M. (2010). Keratinocytes in culture accumulate phagocytosed melanosomes in the perinuclear area. Pigment Cell Melanoma Res. 23, 129-133.
4. Ando, H., Niki, Y., Ito, M., Akiyama, K., Matsui, M.S., Yarosh, D.B., and Ichihashi, M. (2012). Melanosomes are transferred from melanocytes to keratinocytes through the processes of packaging, release, uptake, and dispersion. J. Invest. Dermatol. 132, 1222-1229.
5. Bass, M.D., Williamson, R.C., Nunan, R.D., Humphries, J.D., Byron, A., Morgan, M.R., Martin, P., and Humphries, M.J. (2011). A syndecan-4 hair trigger initiates wound healing through caveolin- and RhoG-regulated integrin endocytosis. Dev. Cell 21, 681-693.
6. Beaumont, K.A., Hamilton, N.A., Moores, M.T. et al. (2011). The recycling endosome protein Rab17 regulates melanocytic filopodia formation and melanosome trafficking. Traffic 12, 627-643.
7. Belleudi, F., Purpura, V., Scrofani, C., Persechino, F., Leone, L., and Torrisi, M.R. (2011). Expression and signaling of the tyrosine kinase FGFR2b/KGFR regulates phagocytosis and melanosome uptake in human keratinocytes. FASEB J. 25, 170-181.
8. Botta, A., Delteil, F., Mettouchi, A., Vieira, A., Estrach, S., Negroni, L., Stefani, C., Lemichez, E., Meneguzzi, G., and Gagnoux-Palacios, L. (2012). Confluence switch signaling regulates ECM composition and the plasmin proteolytic cascade in keratinocytes. J. Cell Sci. 125, 4241-4252.
9. Cardinali, G., Ceccarelli, S., Kovacs, D., Aspite, N., Lotti, L.V., Torrisi, M.R., and Picardo, M. (2005). Keratinocyte growth factor promotes melanosome transfer to keratinocytes. J. Invest. Dermatol. 125, 1190-1199.
10. Cauza, K., Hinterhuber, G., Dingelmaier-Hovorka, R., Brugger, K., Klosner, G., Horvat, R., Wolff, K., and Foedinger, D. (2005). Expression of FcRn, the MHC class I-related receptor for IgG, in human keratinocytes. J. Invest. Dermatol. 124, 132-139.
11. Compton, S.J., Renaux, B., Wijesuriya, S.J., and Hollenberg, M.D. (2001). Glycosylation and the activation of proteinase-activated receptor 2 (PAR(2)) by human mast cell tryptase. Br. J. Pharmacol. 134, 705-718.
12. Cook, P.W., Mattox, P.A., Keeble, W.W., Pittelkow, M.R., Plowman, G.D., Shoyab, M., Adelman, J.P., and Shipley, G.D. (1991). A heparin sulfate-regulated human keratinocyte autocrine factor is similar or identical to amphiregulin. Mol. Cell. Biol. 11, 2547-2557.
13. Cox, D., Tseng, C.C., Bjekic, G., and Greenberg, S. (1999). A requirement for phosphatidylinositol 3-kinase in pseudopod extension. J. Biol. Chem. 274, 1240-1247.
14. Holmes, B.B., Devos, S.L., Kfoury, N. et al. (2013). Heparan sulfate proteoglycans mediate internalization and propagation of specific proteopathic seeds. Proc. Natl Acad. Sci. USA 110, E3138-E3147.
15. Huttunen, M., Hyttinen, M., Nilsson, G., Butterfield, J.H., Horsmanheimo, M., and Harvima, I.T. (2001). Inhibition of keratinocyte growth in cell culture and whole skin culture by mast cell mediators. Exp. Dermatol. 10, 184-192.
16. Kanekiyo, T., and Bu, G. (2009). Receptor-associated protein interacts with amyloid-beta peptide and promotes its cellular uptake. J. Biol. Chem. 284, 33352-33359.
17. Larochelle, W.J., Sakaguchi, K., Atabey, N., Cheon, H.G., Takagi, Y., Kinaia, T., Day, R.M., Miki, T., Burgess, W.H., and Bottaro, D.P. (1999). Heparan sulfate proteoglycan modulates keratinocyte growth factor signaling through interaction with both ligand and receptor. Biochemistry 38, 1765-1771.
18. Leverrier, Y., Okkenhaug, K., Sawyer, C., Bilancio, A., Vanhaesebroeck, B., and Ridley, A.J. (2003). Class I phosphoinositide 3-kinase p110beta is required for apoptotic cell and Fcgamma receptor-mediated phagocytosis by macrophages. J. Biol. Chem. 278, 38437-38442.
19. McDonald, P.C., Fielding, A.B., and Dedhar, S. (2008). Integrin-linked kinase-essential roles in physiology and cancer biology. J. Cell Sci. 121, 3121-3132.
20. Molino, M., Barnathan, E.S., Numerof, R., Clark, J., Dreyer, M., Cumashi, A., Hoxie, J.A., Schechter, N., Woolkalis, M., and Brass, L.F. (1997). Interactions of mast cell tryptase with thrombin receptors and PAR-2. J. Biol. Chem. 272, 4043-4049.
21. Paine, C., Sharlow, E., Liebel, F., Eisinger, M., Shapiro, S., and Seiberg, M. (2001). An alternative approach to depigmentation by soybean extracts via inhibition of the PAR-2 pathway. J. Invest. Dermatol. 116, 587-595.
22. Park, H.Y., Kosmadaki, M., Yaar, M., and Gilchrest, B.A. (2009). Cellular mechanisms regulating human melanogenesis. Cell. Mol. Life Sci. 66, 1493-1506.
23. Pillai, S., Gilliam, L., Conrad, H.E., and Holleran, W.M. (1994). Heparin and its non-anticoagulant analogues inhibit human keratinocyte growth without inducing differentiation. J. Invest. Dermatol. 103, 647-650.
24. Poon, I.K., Parish, C.R., and Hulett, M.D. (2010). Histidine-rich glycoprotein functions cooperatively with cell surface heparan sulfate on phagocytes to promote necrotic cell uptake. J. Leukoc. Biol. 88, 559-569.
25. Sayedyahossein, S., Nini, L., Irvine, T.S., and Dagnino, L. (2012). Essential role of integrin-linked kinase in regulation of phagocytosis in keratinocytes. FASEB J. 26, 4218-4229.
26. Schechter, N.M., Brass, L.F., Lavker, R.M., and Jensen, P.J. (1998). Reaction of mast cell proteases tryptase and chymase with protease activated receptors (PARs) on keratinocytes and fibroblasts. J. Cell. Physiol. 176, 365-373.
27. Schwartz, L.B., and Bradford, T.R. (1986). Regulation of tryptase from human lung mast cells by heparin. Stabilization of the active tetramer. J. Biol. Chem. 261, 7372-7379.
28. Seiberg, M. (2001). Keratinocyte-melanocyte interactions during melanosome transfer. Pigment Cell Res. 14, 236-242.
29. Seiberg, M., Paine, C., Sharlow, E., Andrade-Gordon, P., Costanzo, M., Eisinger, M., and Shapiro, S.S. (2000a). Inhibition of melanosome transfer results in skin lightening. J. Invest. Dermatol. 115, 162-167.
30. Seiberg, M., Paine, C., Sharlow, E., Andrade-Gordon, P., Costanzo, M., Eisinger, M., and Shapiro, S.S. (2000b). The protease-activated receptor 2 regulates pigmentation via keratinocyte-melanocyte interactions. Exp. Cell Res. 254, 25-32.
31. Sharlow, E.R., Paine, C.S., Babiarz, L., Eisinger, M., Shapiro, S., and Seiberg, M. (2000). The protease-activated receptor-2 upregulates keratinocyte phagocytosis. J. Cell Sci. 113(Pt 17), 3093-3101.
32. Sher, I., Zisman-Rozen, S., Eliahu, L. et al. (2006). Targeting perlecan in human keratinocytes reveals novel roles for perlecan in epidermal formation. J. Biol. Chem. 281, 5178-5187.
33. Shipley, G.D., Keeble, W.W., Hendrickson, J.E., Coffey, R.J. JR, and Pittelkow, M.R. (1989). Growth of normal human keratinocytes and fibroblasts in serum-free medium is stimulated by acidic and basic fibroblast growth factor. J. Cell. Physiol. 138, 511-518.
34. 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.
35. 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.
36. Spratte, J., Meyer Zu Schwabedissen, H., Endlich, N., Zygmunt, M., and Fluhr, H. (2013). Heparin inhibits TNF-alpha signaling in human endometrial stromal cells by interaction with NF-kappaB. Mol. Hum. Reprod. 19, 227-236.
37. Steinhoff, M., Corvera, C.U., Thoma, M.S., Kong, W., McAlpine, B.E., Caughey, G.H., Ansel, J.C., and Bunnett, N.W. (1999). Proteinase-activated receptor-2 in human skin: tissue distribution and activation of keratinocytes by mast cell tryptase. Exp. Dermatol. 8, 282-294.
38. Stephens, L., Ellson, C., and Hawkins, P. (2002). Roles of PI3Ks in leukocyte chemotaxis and phagocytosis. Curr. Opin. Cell Biol. 14, 203-213.
39. Tarafder, A.K., Bolasco, G., Correia, M.S. et al. (2014). Rab11b mediates melanin transfer between donor melanocytes and acceptor keratinocytes via coupled exo/endocytosis. J. Invest. Dermatol. 134, 1056-1066.
40. Tumova, S., Woods, A., and Couchman, J.R. (2000). Heparan sulfate proteoglycans on the cell surface: versatile coordinators of cellular functions. Int. J. Biochem. Cell Biol. 32, 269-288.
41. Van Den Bossche, K., Naeyaert, J.M., and Lambert, J. (2006). The quest for the mechanism of melanin transfer. Traffic 7, 769-778.
42. Victor, M., Weiss, J., and Elsbach, P. (1981). Heparin inhibits phagocytosis by polymorphonuclear leukocytes. Infect. Immun. 32, 295-299.
43. Virador, V.M., Muller, J., Wu, X. et al. (2002). Influence of alpha-melanocyte-stimulating hormone and ultraviolet radiation on the transfer of melanosomes to keratinocytes. FASEB J. 16, 105-107.
44. Wu, X.S., Masedunskas, A., Weigert, R., Copeland, N.G., Jenkins, N.A., and Hammer, J.A. (2012). Melanoregulin regulates a shedding mechanism that drives melanosome transfer from melanocytes to keratinocytes. Proc. Natl Acad. Sci. USA 109, E2101-E2109.
45. Yamamoto, O., and Bhawan, J. (1994). Three modes of melanosome transfers in Caucasian facial skin: hypothesis based on an ultrastructural study. Pigment Cell Res. 7, 158-169.
46. Young, E. (2008). The anti-inflammatory effects of heparin and related compounds. Thromb. Res. 122, 743-752.