Extracellular UDP-glucose activates P2Y14 receptor and induces signal transducer and activator of transcription 3 (STAT3) Tyr705 phosphorylation and binding to Hyaluronan synthase 2 (HAS2) promoter, stimulating Hyaluronan synthesis of keratinocytes

Journal of Biological Chemistry

Volumn 289, Issue 26, 2014, Pages 18569-18581

  Jokela, Tiina A ^a   Kärnä, Riikka ^a   Makkonen, Katri M ^a   Laitinen, Jarmo T ^a   Tammi, Raija H ^a   Tammi, Markku I ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; PHOSPHORYLATION;

COUPLED RECEPTORS; HYALURONAN SYNTHESIS; IMMUNOPRECIPITATIONS; KERATINOCYTE CULTURES; KERATINOCYTE MIGRATION; MATRIX MOLECULES; RESPONSE ELEMENTS; SIGNAL TRANSDUCERS;

HYALURONIC ACID;

G PROTEIN COUPLED RECEPTOR; HYALURONAN SYNTHASE 2; HYALURONIC ACID; INTERLEUKIN 8; JANUS KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PURINERGIC P2Y RECEPTOR; PURINERGIC P2Y14 RECEPTOR; STAT3 PROTEIN; SYNTHETASE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE GLUCOSE;

ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME SPECIFICITY; GENE; GENE EXPRESSION; GENE INDUCTION; GLYCOSAMINOGLYCAN METABOLISM; HAS2 GENE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IL 8 GENE; KERATINOCYTE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; RECEPTOR BLOCKING; TRANSCRIPTION REGULATION; UPREGULATION;

HYALURONAN; HYALURONATE; JANUS KINASE (JAK); KERATINOCYTE; P2Y14; PURINERGIC RECEPTOR; STAT3; UDP-GLC;

AMINO ACID MOTIFS; CELL MOVEMENT; GLUCURONOSYLTRANSFERASE; HUMANS; HYALURONIC ACID; JANUS KINASE 2; KERATINOCYTES; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECEPTORS, PURINERGIC P2; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TYROSINE; UP-REGULATION; URIDINE DIPHOSPHATE GLUCOSE;

EID: 84903534739     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.551804     Document Type: Article

References (60)

1. Tammi, R., Ågren, U. M., Tuhkanen, A. L., and Tammi, M. (1994) Hyaluronan metabolism in skin. Prog. Histochem. Cytochem. 29, 1-81
2. Pienimaki, J. P., Rilla, K., Fulop, C., Sironen, R. K., Karvinen, S., Pasonen, S., Lammi, M. J., Tammi, R., Hascall, V. C., and Tammi, M. I. (2001) Epidermal growth factor activates hyaluronan synthase 2 in epidermal keratinocytes and increases pericellular and intracellular hyaluronan. J. Biol. Chem. 276, 20428-20435
3. Turley, E. A., Noble, P. W., and Bourguignon, L. Y. (2002) Signaling properties of hyaluronan receptors. J. Biol. Chem. 277, 4589-4592
4. Hall, C. L., and Turley, E. A. (1995) Hyaluronan: RHAMM mediated cell locomotion and signaling in tumorigenesis. J. Neurooncol. 26, 221-229
5. Maytin, E. V., Chung, H. H., and Seetharaman, V. M. (2004) Hyaluronan participates in the epidermal response to disruption of the permeability barrier in vivo. Am. J. Pathol. 165, 1331-1341
6. Tammi, R., Pasonen-Seppänen, S., Kolehmainen, E., and Tammi, M. (2005) Hyaluronan synthase induction and hyaluronan accumulation in mouse epidermis following skin injury. J. Invest. Dermatol. 124, 898-905
7. Monslow, J., Sato, N., Mack, J. A., and Maytin, E. V. (2009) Woundinginduced synthesis of hyaluronic acid in organotypic epidermal cultures requires the release of heparin-binding egf and activation of the EGFR. J. Invest. Dermatol. 129, 2046-2058
8. Tammi, R. H., and Tammi, M. I. (2009) Hyaluronan accumulation in wounded epidermis: a mediator of keratinocyte activation. J. Invest. Dermatol. 129, 1858-1860
9. Tammi, R., Ripellino, J. A., Margolis, R. U., and Tammi, M. (1988) Localization of epidermal hyaluronic acid using the hyaluronate binding region of cartilage proteoglycan as a specific probe. J. Invest. Dermatol. 90, 412-414
10. Passi, A., Sadeghi, P., Kawamura, H., Anand, S., Sato, N., White, L. E., Hascall, V. C., and Maytin, E. V. (2004) Hyaluronan suppresses epidermal differentiation in organotypic cultures of rat keratinocytes. Exp. Cell Res. 296, 123-134
11. Pasonen-Seppänen, S., Karvinen, S., Törrönen, K., Hyttinen, J. M., Jokela, T., Lammi, M. J., Tammi, M. I., and Tammi, R. (2003) EGF upregulates, whereas TGF-beta downregulates, the hyaluronan synthases Has2 and Has3 in organotypic keratinocyte cultures: correlations with epidermal proliferation and differentiation. J. Invest. Dermatol. 120, 1038-1044
12. Siiskonen, H., Törrönen, K., Kumlin, T., Rilla, K., Tammi, M. I., and Tammi, R. H. (2011) Chronic UVR causes increased immunostaining of CD44 and accumulation of hyaluronan in mouse epidermis. J. Histochem. Cytochem. 59, 908-917
13. Weigel, P. H., and DeAngelis, P. L. (2007) Hyaluronan synthases: a decadeplus of novel glycosyltransferases. J. Biol. Chem. 282, 36777-36781
14. Prehm, P. (1984) Hyaluronate is synthesized at plasma membranes. Biochem. J. 220, 597-600
15. Hubbard, C., McNamara, J. T., Azumaya, C., Patel, M. S., and Zimmer, J. (2012) The hyaluronan synthase catalyzes the synthesis and membrane translocation of hyaluronan. J. Mol. Biol. 418, 21-31
16. Karvinen, S., Pasonen-Seppänen, S., Hyttinen, J. M., Pienimäki, J. P., Törrönen, K., Jokela, T. A., Tammi, M. I., and Tammi, R. (2003) Keratinocyte growth factor stimulates migration and hyaluronan synthesis in the epidermis by activation of keratinocyte hyaluronan synthases 2 and 3. J. Biol. Chem. 278, 49495-49504
17. Jokela, T. A., Lindgren, A., Rilla, K., Maytin, E., Hascall, V. C., Tammi, R. H., and Tammi, M. I. (2008) Induction of hyaluronan cables and monocyte adherence in epidermal keratinocytes. Connect. Tissue Res. 49, 115-119
18. Sampson, P. M., Rochester, C. L., Freundlich, B., and Elias, J. A. (1992) Cytokine regulation of human lung fibroblast hyaluronan (hyaluronic acid) production. Evidence for cytokine-regulated hyaluronan (hyaluronic acid) degradation and human lung fibroblast-derived hyaluronidase. J. Clin. Invest. 90, 1492-1503
19. Pasonen-Seppänen, S. M., Maytin, E. V., Törrönen, K. J., Hyttinen, J. M., Hascall, V. C., MacCallum, D. K., Kultti, A. H., Jokela, T. A., Tammi, M. I., and Tammi, R. H. (2008) All-trans retinoic acid-induced hyaluronan production and hyperplasia are partly mediated by EGFR signaling in epidermal keratinocytes. J. Invest. Dermatol. 128, 797-807
20. Saavalainen, K., Tammi, M. I., Bowen, T., Schmitz, M. L., and Carlberg, C. (2007) Integration of the activation of the human hyaluronan synthase 2 gene promoter by common cofactors of the transcription factors retinoic acid receptor and nuclear factor kBJ. Biol. Chem. 282, 11530-11539
21. Saavalainen, K., Pasonen-Seppänen, S., Dunlop, T. W., Tammi, R., Tammi, M. I., and Carlberg, C. (2005) The human hyaluronan synthase 2 gene is a primary retinoic acid and epidermal growth factor responding gene. J. Biol. Chem. 280, 14636-14644
22. Jokela, T. A., Makkonen, K. M., Oikari, S., Kärnä, R., Koli, E., Hart, G. W., Tammi, R. H., Carlberg, C, and Tammi, M. I. (2011) Cellular content of UDP-N-acetylhexosamines controls hyaluronan synthase 2 expression and correlates with O-GlcNAc modification of transcription factors YY1 and SP1. J. Biol. Chem. 286, 33632-33640
23. Vigetti, D., Deleonibus, S., Moretto, P., Karousou, E., Viola, M., Bartolini, B., Hascall, V. C, Tammi, M., De Luca, G., and Passi, A. (2012) Role of UDP-N-acetylglucosamine (GlcNAc) and O-GlcNAcylation of hyaluronan synthase 2 in the control of chondroitin sulfate and hyaluronan synthesis. J. Biol. Chem. 287, 35544-35555
24. Kreda, S. M., Seminario-Vidal, L., Heusden, Cv., and Lazarowski, E. R. (2008) Thrombin-promoted release of UDP-glucose from human astrocytoma cells. Br. J. Pharmacol. 153, 1528-1537
25. Sesma, J. I., Esther, C. R., Jr, Kreda, S. M., Jones, L., O'Neal, W., Nishihara, S., Nicholas, R. A., and Lazarowski, E. R. (2009) Endoplasmic reticulum/Golgi nucleotide sugar transporters contribute to the cellular release of UDP-sugar signaling molecules. J. Biol. Chem. 284, 12572-12583
26. Chambers, J. K., Macdonald, L. E., Sarau, H. M., Ames, R. S., Freeman, K., Foley, J. J., Zhu, Y., McLaughlin, M. M., Murdock, P., McMillan, L., Trill, J., Swift, A., Aiyar, N, Taylor, P., Vawter, L., Naheed, S., Szekeres, P., Hervieu, G., Scott, C, Watson, J. M., Murphy, A. J., Duzic, E., Klein, C, Bergsma, D. J., Wilson, S., and Livi, G. P. (2000) A G protein-coupled receptor for UDP-glucose. J. Biol. Chem. 275, 10767-10771
27. 14 receptor of airway epithelial cells: coupling to intracellular Ca2+ and IL-8 secretion. Am. J. Respir. CellMol. Biol. 33, 601-609
28. 14 receptor) adds diversity to the P2Y receptor family. Trends Pharmacol. Sci. 24, 52-55
29. Zippel, N, Limbach, C A., Ratajski, N, Urban, C, Luparello, C, Pansky A., Kassack, M. U., and Tobiasch, E. (2012) Purinergic receptors influence the differentiation of human mesenchymal stem cells. Stem Cells Dev. 21, 884-900
30. 14 receptor in model cell systems. J. Pharmacol. Exp. Ther. 330, 162-168
31. 14 receptors is a mediator of mast cell degranulation. Biochem. Pharmacol. 79, 873-879
32. Burrell, H. E., Bowler, W. B., Gallagher, J. A., and Sharpe, G. R. (2003) Human keratinocytes express multiple P2Y-receptors: evidence for functional P2Y1, P2Y2, and P2Y4 receptors. J. Invest. Dermatol. 120, 440-447
33. Greig, A. V., Linge, C, Cambrey, A., and Burnstock, G. (2003) Purinergic receptors are part of a signaling system for keratinocyte proliferation, differentiation, and apoptosis in human fetal epidermis. J. Invest. Dermatol. 121, 1145-1149
34. Boukamp, P., Petrussevska, R. T., Breitkreutz, D., Hornung, J., Markham, A., and Fusenig, N. E. (1988) Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106, 761-771
35. Jokela, T. A., Jauhiainen, M., Auriola, S., Kauhanen, M., Tiihonen, R., Tammi, M. I., and Tammi, R. H. (2008) Mannose inhibits hyaluronan synthesis by down-regulation of the cellular pool of UDP-N-acetylhexosamines. J. Biol. Chem. 283, 7666-7673
36. Räbinä, J., Mäki, M., Savilahti, E. M., Järvinen, N, Penttilä, L., and Renkonen, R. (2001) Analysis of nucleotide sugars from cell lysates by ion-pair solid-phase extraction and reversed-phase high-performance liquid chromatography. Glycoconj. J. 18, 799-805
37. Rilla, K., Oikari, S., Jokela, T. A., Hyttinen, J. M., Kärnä, R., Tammi, R. H, and Tammi, M. I. (2013) Hyaluronan synthase 1 (HAS1) requires higher cellular UDP-GlcNAc concentration than HAS2 and HAS3. J. Biol. Chem. 288, 5973-5983
38. Tammi, R. H., Passi, A. G., Rilla, K., Karousou, E., Vigetti, D., Makkonen, K., and Tammi, M. I. (2011) Transcriptional and post-translational regulation of hyaluronan synthesis. FEBS J. 278, 1419-1428
39. Harden, T. K., Sesma, J. I., Fricks, I. P., and Lazarowski, E. R. (2010) Signalling and pharmacological properties of the P2Y receptor. Acta Physiol. (Oxf). 199, 149-160
40. Tsukimoto, M., Homma, T., Ohshima, Y., and Kojima, S. (2010) Involvement of purinergic signaling in cellular response to y radiation. Radiat. Res. 173, 298-309
41. Kopf G. S., and Wookalis M. J. (1991) ADP-ribosylation of G proteins with pertussis toxin. Methods Enzymol. 195, 257-266
42. Chung, J., Uchida, E., Grammer, T. C, and Blenis, J. (1997) STAT3 serine phosphorylation by ERK-dependent and -independent pathways negatively modulates its tyrosine phosphorylation. Mol. Cell Biol. 17, 6508-6516
43. Ceresa, B. P., Horvath, C. M., and Pessin, J. E. (1997) Signal transducer and activator of transcription-3 serine phosphorylation by insulin is mediated by a Ras/Raf/MEK-dependent pathway. Endocrinology. 138, 4131-4137
44. Ripple, M. O., Kim, N, and Springett, R. (2013) Acute mitochondrial inhibition by mitogen-activated protein kinase/extracellular signaling-regulated kinase (MEK) 1/2 inhibitors regulates proliferation. J. Biol. Chem. 288, 2933-2940
45. Bromberg, J., and Chen, X. (2001) STAT proteins: signal tranducers and activators of transcription. Methods Enzymol. 333, 138-151
46. Shirakata, Y. (2010) Regulation of epidermal keratinocytes by growth factors. J. Dermatol. Sci. 59, 73-80
47. Rilla, K., Pasonen-Seppänen, S., Rieppo, J., Tammi, M., and Tammi, R. (2004) The hyaluronan synthesis inhibitor 4-methylumbelliferone prevents keratinocyte activation and epidermal hyperproliferation induced by epidermal growth factor. J. Invest. Dermatol. 123, 708-714
48. Ipata, P. L., Balestri, F., Camici, M., and Tozzi, M. G. (2011) Molecular mechanisms of nucleoside recycling in the brain. Int. J. Biochem. Cell Biol. 43, 140-145
49. Tammi, R., Rilla, K., Pienimaki, J. P., MacCallum, D. K., Hogg, M., Luukkonen, M., Hascall, V. C, and Tammi, M. (2001) Hyaluronan enters keratinocytes by a novel endocytic route for catabolism. J. Biol. Chem. 276, 35111-35122
50. Yu, H., Pardoll, D., and Jove, R. (2009) STATs in cancer inflammation and immunity: a leading role for STAT3. Nat. Rev. Cancer. 9, 798-809
51. Washburn, K. B., and Neary, J. T. (2006) P2 purinergic receptors signal to STAT3 in astrocytes: difference in STAT3 responses to P2Y and P2X receptor activation. Neuroscience. 142, 411-423
52. Bromberg, J., and Darnell, J. E., Jr. (2000) The role of STATs in transcriptional control and their impact on cellular function. Oncogene. 19, 2468-2473
53. Bromberg, J. F., Horvath, C. M., Besser, D., Lathem, W. W., and Darnell, J. E., Jr. (1998) Stat3 activation is required for cellular transformation by v-src. Mol. Cell. Biol. 18, 2553-2558
54. Schuringa, J. J., Schepers, H., Vellenga, E., and Kruijer, W. (2001) Ser727-dependent transcriptional activation by association of p300 with STAT3 upon IL-6 stimulation. FEBS Lett. 495, 71-76
55. Lee, H. K., Jung, J., Lee, S. H, Seo, S. Y., Suh, D. J., and Park, H. T. (2009) Extracellular signal-regulated kinase activation is required for serine 727 phosphorylation of STAT3 in Schwann cells in vitro and in vivo. Korean J. Physiol. Pharmacol. 13, 161-168
56. 705 largely through TC45. Genes Cells. 2, 135-145
57. Sandjeu, Y., and Haftek, M. (2009) Desmosealin and other components of the epidermal extracellular matrix. J. Physiol. Pharmacol. 60, 23-30
58. Bianco, F., Fumagalli, M., Pravettoni, E., D'Ambrosi, N., Volonte, C., Matteoli, M., Abbracchio, M. P., and Verderio, C. (2005) Pathophysiological roles of extracellular nucleotides in glial cells: differential expression of purinergic receptors in resting and activated microglia. Brain Res. Brain Res. Rev. 48, 144-156
59. Moore, D. J., Murdock, P. R., Watson, J. M., Faull, R. L., Waldvogel, H. J., Szekeres, P. G., Wilson, S., Freeman, K. B., and Emson, P. C. (2003) GPR105, a novel Gi/o-coupled UDP-glucose receptor expressed on brain glia and peripheral immune cells, is regulated by immunologic challenge: possible role in neuroimmune function. Brain Res. Mol. Brain Res. 118, 10-23
60. Lee, B. C., Cheng, T., Adams, G. B., Attar, E. C., Miura, N., Lee, S. B., Saito, Y., Olszak, I., Dombkowski, D., Olson, D. P., Hancock, J., Choi, P. S., Haber, D. A., Luster, A. D., and Scadden, D. T. (2003) P2Y-like receptor, GPR105 (P2Y14), identifies and mediates chemotaxis of bone-marrow hematopoietic stem cells. Genes Dev. 17, 1592-1604