Interleukin-1β-induced reduction of CD44 Ser-325 phosphorylation in human epidermal keratinocytes promotes CD44 homomeric complexes, binding to ezrin, and extended, monocyte-adhesive hyaluronan coats

Journal of Biological Chemistry

Volumn 290, Issue 19, 2015, Pages 12379-12393

  Jokela, Tiina ^a   Oikari, Sanna ^a   Takabe, Piia ^a   Rilla, Kirsi ^a   Kärnä, Riikka ^a   Tammi, Markku ^a   Tammi, Raija ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BODY FLUIDS; CALMODULIN; CELL CULTURE; ENDOTHELIAL CELLS; PHOSPHORYLATION;

COMPLEX FORMATIONS; HUMAN EPIDERMAL KERATINOCYTES; HUMAN KERATINOCYTES; HYALURONAN SYNTHESIS; KERATINOCYTE CULTURES; POST-TRANSLATIONAL MODIFICATIONS; PROINFLAMMATORY CYTOKINES; RECRUITMENT MECHANISM;

HYALURONIC ACID;

EZRIN; HERMES ANTIGEN; HYALURONIC ACID; INTERLEUKIN 1BETA; MULTIPROTEIN COMPLEX; N [2 [[N [3 (4 CHLOROPHENYL) 2 PROPENYL] N METHYLAMINO]METHYL]PHENYL] N (2 HYDROXYETHYL) 4 METHOXYBENZENESULFONAMIDE; SERINE; CYTOSKELETON PROTEIN;

ARTICLE; CELL ADHESION; COMPLEX FORMATION; CONTROLLED STUDY; CYTOSKELETON; HUMAN; HUMAN CELL; HYALURONAN COAT; INTRACELLULAR SIGNALING; KERATINOCYTE; MONOCYTE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HOMOMERIZATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; CELL MEMBRANE; CELL MOTION; CHEMISTRY; CONFOCAL MICROSCOPY; CYTOLOGY; EPIDERMIS; EXON; FLUORESCENCE MICROSCOPY; INFLAMMATION; LEUKOCYTE; METABOLISM; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; TUMOR CELL LINE;

ANTIGENS, CD44; CELL LINE, TUMOR; CELL MEMBRANE; CELL MOVEMENT; CYTOSKELETAL PROTEINS; CYTOSKELETON; EPIDERMIS; EXONS; HUMANS; HYALURONIC ACID; INFLAMMATION; INTERLEUKIN-1BETA; KERATINOCYTES; LEUKOCYTES; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MONOCYTES; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SERINE;

EID: 84929190622     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.620864     Document Type: Article

References (106)

1. Thorne, R. F., Legg, J. W., and Isacke, C. M. (2004) The role of the CD44 transmembrane and cytoplasmic domains in co-ordinating adhesive and signalling events. J. Cell Sci. 117, 373-380
2. Toole, B. P. (2009) Hyaluronan-CD44 interactions in cancer: paradoxes and possibilities. Clin. Cancer Res. 15, 7462-7468
3. Tuhkanen, A. L., Tammi, M., and Tammi, R. (1997) CD44 substituted with heparan sulfate and endo-beta-galactosidase-sensitive oligosaccharides: a major proteoglycan in adult human epidermis. J. Invest. Dermatol. 109, 213-218
4. Teriete, P., Banerji, S., Noble, M., Blundell, C. D., Wright, A. J., Pickford, A. R., Lowe, E., Mahoney, D. J., Tammi, M. I., Kahmann, J. D., Campbell, I. D., Day, A. J., and Jackson, D. G. (2004) Structure of the regulatory hyaluronan binding domain in the inflammatory leukocyte homing receptor CD44. Mol. Cell 13, 483-496
5. Jiang, H., Knudson, C. B., and Knudson, W. (2001) Antisense inhibition of CD44 tailless splice variant in human articular chondrocytes promotes hyaluronan internalization. Arthritis Rheum. 44, 2599-2610
6. Knudson, W., Aguiar, D. J., Hua, Q., and Knudson, C. B. (1996) CD44-anchored hyaluronan-rich pericellular matrices: an ultrastructural and biochemical analysis. Exp. Cell Res. 228, 216-228
7. Pasonen-Seppänen, S., Hyttinen, J. M., Rilla, K., Jokela, T., Noble, P. W., Tammi, M., and Tammi, R. (2012) Role of CD44 in the organization of keratinocyte pericellular hyaluronan. Histochem. Cell Biol. 137, 107-120
8. Tammi, R., MacCallum, D., Hascall, V. C., Pienimäki, J. P., Hyttinen, M., and Tammi, M. (1998) Hyaluronan bound to CD44 on keratinocytes is displaced by hyaluronan decasaccharides and not hexasaccharides. J. Biol. Chem. 273, 28878-28888
9. Culty, M., Shizari, M., Thompson, E. W., and Underhill, C. B. (1994) Binding and degradation of hyaluronan by human breast cancer cell lines expressing different forms of CD44: correlation with invasive potential. J. Cell Physiol. 160, 275-286
10. Hua, Q., Knudson, C. B., and Knudson, W. (1993) Internalization of hyaluronan by chondrocytes occurs via receptor-mediated endocytosis. J. Cell Sci. 106, 365-375
11. Knudson, C. B., and Knudson, W. (2004) Hyaluronan and CD44: modulators of chondrocyte metabolism. Clin. Orthop. Relat. Res. 427, S152-S162
12. 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
13. Thankamony, S. P., and Knudson, W. (2006) Acylation of CD44 and its association with lipid rafts are required for receptor and hyaluronan endocytosis. J. Biol. Chem. 281, 34601-34609
14. Toole, B. P. (2004) Hyaluronan: from extracellular glue to pericellular cue. Nat. Rev. Cancer 4, 528-539
15. Tzircotis, G., Thorne, R. F., and Isacke, C. M. (2005) Chemotaxis towards hyaluronan is dependent on CD44 expression and modulated by cell type variation in CD44-hyaluronan binding. J. Cell Sci. 118, 5119-5128
16. Lesley, J., Hascall, V. C., Tammi, M., and Hyman, R. (2000) Hyaluronan binding by cell surface CD44. J. Biol. Chem. 275, 26967-26975
17. Duterme, C., Mertens-Strijthagen, J., Tammi, M., and Flamion, B. (2009) Two novel functions of hyaluronidase-2 (Hyal2) are formation of the glycocalyx and control of CD44-ERM interactions. J. Biol. Chem. 284, 33495-33508
18. Jensen, P. V., and Larsson, L. I. (2004) Actin microdomains on endothelial cells: association with CD44, ERM proteins, and signaling molecules during quiescence and wound healing. Histochem. Cell Biol. 121, 361-369
19. Liu, Y. Y., Lee, C. H., Dedaj, R., Zhao, H., Mrabat, H., Sheidlin, A., Syrkina, O., Huang, P. M., Garg, H. G., Hales, C. A., and Quinn, D. A. (2008) High-molecular-weight hyaluronan: a possible new treatment for sepsis-induced lung injury: a preclinical study in mechanically ventilated rats. Crit. Care 12, R102
20. Heldin, P., Karousou, E., Bernert, B., Porsch, H., Nishitsuka, K., and Skandalis, S. S. (2008) Importance of hyaluronan-CD44 interactions in inflammation and tumorigenesis. Connect. Tissue Res. 49, 215-218
21. Johnson, P., and Ruffell, B. (2009) CD44 and its role in inflammation and inflammatory diseases. Inflamm. Allergy Drug Targets 8, 208-220
22. Jiang, D., Liang, J., and Noble, P. W. (2011) Hyaluronan as an immune regulator in human diseases. Physiol. Rev. 91, 221-264
23. Oikari, S., Jokela, T. A., Tammi, R. H., and Tammi, M. I. (2012) in Extracellular Matrix: Pathobiology and Signaling (Karamanos, N., ed) pp. 39-65, Walter de Gruyter, Berlin
24. Day, A. J., and de la Motte, C. A. (2005) Hyaluronan cross-linking: a protective mechanism in inflammation?. Trends Immunol. 26, 637-643
25. Petrey, A. C., and de la Motte, C. A. (2014) Hyaluronan, a crucial regulator of inflammation. Front. Immunol. 5, 101
26. 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
27. Selbi, W., de la Motte, C., Hascall, V., and Phillips, A. (2004) BMP-7 modulates hyaluronan-mediated proximal tubular cell-monocyte interaction. J. Am. Soc. Nephrol. 15, 1199-1211
28. Campo, G. M., Avenoso, A., D'Ascola, A., Scuruchi, M., Prestipino, V., Calatroni, A., and Campo, S. (2012) Hyaluronan in part mediates IL-1β-induced inflammation in mouse chondrocytes by up-regulating CD44 receptors. Gene 494, 24-35
29. Ibrahim, E. M., Stewart, R. L., Corke, K., Blackett, A. D., Tidy, J. A., and Wells, M. (2006) Upregulation of CD44 expression by interleukins 1, 4, and 13, transforming growth factor-β1, estrogen, and progestogen in human cervical adenocarcinoma cell lines. Int. J. Gynecol. Cancer 16, 1631-1642
30. Meran, S., Martin, J., Luo, D. D., Steadman, R., and Phillips, A. (2013) Interleukin-1β induces hyaluronan and CD44-dependent cell protrusions that facilitate fibroblast-monocyte binding. Am. J. Pathol. 182, 2223-2240
31. Tsubaki, H., Ogawa, M., Hosoya, N., Shimizu, D., Obara, M., Hirano, H., and Tanaka, T. (2005) Expression of CD44 mRNA induced by interleukin-1β in human cultured uterine cervical fibroblasts. Eur. J. Obstet. Gynecol. Reprod. Biol. 122, 156-161
32. Vigetti, D., Genasetti, A., Karousou, E., Viola, M., Moretto, P., Clerici, M., Deleonibus, S., De Luca, G., Hascall, V. C., and Passi, A. (2010) Proinflammatory cytokines induce hyaluronan synthesis and monocyte adhesion in human endothelial cells through hyaluronan synthase 2 (HAS2) and the nuclear factor-κB (NF-κB) pathway. J. Biol. Chem. 285, 24639-24645
33. Jokela, T. A., Kuokkanen, J., Kärnä, R., Pasonen-Seppänen, S., Rilla, K., Kössi, J., Laato, M., Tammi, R. H., and Tammi, M. I. (2013) Mannose reduces hyaluronan and leukocytes in wound granulation tissue and inhibits migration and hyaluronan-dependent monocyte binding. Wound Repair Regen. 21, 247-255
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. Breitkreutz, D., Schoop, V. M., Mirancea, N., Baur, M., Stark, H. J., and Fusenig, N. E. (1998) Epidermal differentiation and basement membrane formation by HaCaT cells in surface transplants. Eur. J. Cell Biol. 75, 273-286
36. Neame, S. J., and Isacke, C. M. (1992) Phosphorylation of CD44 in vivo requires both Ser323 and Ser325, but does not regulate membrane localization or cytoskeletal interaction in epithelial cells. EMBO J. 11, 4733-4738
37. Hiltunen, E. L., Anttila, M., Kultti, A., Ropponen, K., Penttinen, J., Yliskoski, M., Kuronen, A. T., Juhola, M., Tammi, R., Tammi, M., and Kosma, V. M. (2002) Elevated hyaluronan concentration without hyaluronidase activation in malignant epithelial ovarian tumors. Cancer Res. 62, 6410-6413
38. Tammi, R., Ågren, U. M., Tuhkanen, A. L., and Tammi, M. (1994) Hyaluronan metabolism in skin. Prog. Histochem. Cytochem. 29, 1-81
39. Okamoto, I., Tsuiki, H., Kenyon, L. C., Godwin, A. K., Emlet, D. R., Holgado-Madruga, M., Lanham, I. S., Joynes, C. J., Vo, K. T., Guha, A., Matsumoto, M., Ushio, Y., Saya, H., and Wong, A. J. (2002) Proteolytic cleavage of the CD44 adhesion molecule in multiple human tumors. Am. J. Pathol. 160, 441-447
40. 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
41. Kugelman, L. C., Ganguly, S., Haggerty, J. G., Weissman, S. M., and Milstone, L. M. (1992) The core protein of epican, a heparan sulfate proteoglycan on keratinocytes, is an alternative form of CD44. J. Invest. Dermatol. 99, 886-891
42. Lewis, C.A., Townsend, P.A., and Isacke, C.M.(2001) Ca2+/calmodulin-dependent protein kinase mediates the phosphorylation of CD44 required for cell migration on hyaluronan. Biochem. J. 357, 843-850
43. Söderberg, O., Gullberg, M., Jarvius, M., Ridderstråle, K., Leuchowius, K. J., Jarvius, J., Wester, K., Hydbring, P., Bahram, F., Larsson, L. G., and Landegren, U. (2006) Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995-1000
44. Siiskonen, H., Kärnä, R., Hyttinen, J. M., Tammi, R. H., Tammi, M. I., and Rilla, K. (2014) Hyaluronan synthase 1 (HAS1) produces a cytokine-and glucose-inducible, CD44-dependent cell surface coat. Exp. Cell Res. 320, 153-163
45. Desai, B., Ma, T., Zhu, J., and Chellaiah, M. A. (2009) Characterization of the expression of variant and standard CD44 in prostate cancer cells: identification of the possible molecular mechanism of CD44/MMP9 complex formation on the cell surface. J. Cell Biochem. 108, 272-284
46. Kozlova, I., Ruusala, A., Voytyuk, O., Skandalis, S. S., and Heldin, P. (2012) IQGAP1 regulates hyaluronan-mediated fibroblast motility and proliferation. Cell. Signal. 24, 1856-1862
47. Legg, J. W., Lewis, C. A., Parsons, M., Ng, T., and Isacke, C. M. (2002) A novel PKC-regulated mechanism controls CD44 ezrin association and directional cell motility. Nat. Cell Biol. 4, 399-407
48. Peck, D., and Isacke, C. M. (1998) Hyaluronan-dependent cell migration can be blocked by a CD44 cytoplasmic domain peptide containing a phosphoserine at position 325. J. Cell Sci. 111, 1595-1601
49. 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
50. 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-β downregulates, the hyaluronan synthases Has2 and Has3 in organotypic keratinocyte cultures: correlations with epidermal proliferation and differentiation. J. Invest. Dermatol. 120, 1038-1044
51. Kim, J. H., Glant, T. T., Lesley, J., Hyman, R., and Mikecz, K. (2000) Adhesion of lymphoid cells to CD44-specific substrata: the consequences of attachment depend on the ligand. Exp. Cell Res. 256, 445-453
52. Wu, Y., Zhao, Q., Peng, C., Sun, L., Li, X. F., and Kuang, D. M. (2011) Neutrophils promote motility of cancer cells via a hyaluronan-mediated TLR4/PI3K activation loop. J. Pathol. 225, 438-447
53. Erickson, J. R., Pereira, L., Wang, L., Han, G., Ferguson, A., Dao, K., Copeland, R. J., Despa, F., Hart, G. W., Ripplinger, C. M., and Bers, D. M. (2013) Diabetic hyperglycaemia activates CaMKII and arrhythmias by O-linked glycosylation. Nature 502, 372-376
54. Tsui, J., Inagaki, M., and Schulman, H. (2005) Calcium/calmodulin-dependent protein kinase II (CaMKII) localization acts in concert with substrate targeting to create spatial restriction for phosphorylation. J. Biol. Chem. 280, 9210-9216
55. Wagner, S., Rokita, A. G., Anderson, M. E., and Maier, L. S. (2013) Redox regulation of sodium and calcium handling. Antioxid. Redox Signal. 18, 1063-1077
56. Li, L., Heldin, C. H., and Heldin, P. (2006) Inhibition of platelet-derived growth factor-BB-induced receptor activation and fibroblast migration by hyaluronan activation of CD44. J. Biol. Chem. 281, 26512-26519
57. Wong, N. K., Lai, J. C., Maeshima, N., and Johnson, P. (2011) CD44-mediated elongated T cell spreading requires Pyk2 activation by Src family kinases, extracellular calcium, phospholipase C and phosphatidyli-nositol-3 kinase. Cell. Signal. 23, 812-819
58. Bourguignon, L. Y., Zhu, H., Shao, L., and Chen, Y. W. (2000) Ankyrin-Tiam1 interaction promotes Rac1 signaling and metastatic breast tumor cell invasion and migration. J. Cell Biol. 150, 177-191
59. Brown, K. L., Birkenhead, D., Lai, J. C., Li, L., Li, R., and Johnson, P. (2005) Regulation of hyaluronan binding by F-actin and colocalization of CD44 and phosphorylated ezrin/radixin/moesin (ERM) proteins in myeloid cells. Exp. Cell Res. 303, 400-414
60. Camp, R. L., Kraus, T. A., and Puré, E. (1991) Variations in the cytoskeletal interaction and posttranslational modification of the CD44 homing receptor in macrophages. J. Cell Biol. 115, 1283-1292
61. Takahashi, E., Nagano, O., Ishimoto, T., Yae, T., Suzuki, Y., Shinoda, T., Nakamura, S., Niwa, S., Ikeda, S., Koga, H., Tanihara, H., and Saya, H. (2010) Tumor necrosis factor-α regulates transforming growth factor-β-dependent epithelial-mesenchymal transition by promoting hyaluronan-CD44-moesin interaction. J. Biol. Chem. 285, 4060-4073
62. Legg, J. W., and Isacke, C. M. (1998) Identification and functional analysis of the ezrin-binding site in the hyaluronan receptor, CD44. Curr. Biol. 8, 705-708
63. Matsui, T., Maeda, M., Doi, Y., Yonemura, S., Amano, M., Kaibuchi, K., Tsukita, S., and Tsukita, S. (1998) Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J. Cell Biol. 140, 647-657
64. Mellor, L., Knudson, C. B., Hida, D., Askew, E. B., and Knudson, W. (2013) Intracellular domain fragment of CD44 alters CD44 function in chondrocytes. J. Biol. Chem. 288, 25838-25850
65. Skandalis, S. S., Kozlova, I., Engström, U., Hellman, U., and Heldin, P. (2010) Proteomic identification of CD44 interacting proteins. IUBMB Life 62, 833-840
66. Buckley, S. T., Medina, C., Kasper, M., and Ehrhardt, C. (2011) Interplay between RAGE, CD44, and focal adhesion molecules in epithelial-mesenchymal transition of alveolar epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 300, L548-L559
67. John, G. R., Chen, L., Rivieccio, M. A., Melendez-Vasquez, C. V., Hartley, A., and Brosnan, C. F. (2004) Interleukin-1β induces a reactive astroglial phenotype via deactivation of the Rho GTPase-Rock axis. J. Neurosci. 24, 2837-2845
68. Xiao, Y., Sun, M., Zhan, Z., Ye, Y., Huang, M., Zou, Y., Liang, L., Yang, X., and Xu, H. (2014) Increased phosphorylation of ezrin is associated with the migration and invasion of fibroblast-like synoviocytes from patients with rheumatoid arthritis. Rheumatology 53, 1291-1300
69. Donatello, S., Babina, I. S., Hazelwood, L. D., Hill, A. D., Nabi, I. R., and Hopkins, A. M. (2012) Lipid raft association restricts CD44-ezrin interaction and promotion of breast cancer cell migration. Am. J. Pathol. 181, 2172-2187
70. Mori, T., Kitano, K., Terawaki, S., Maesaki, R., Fukami, Y., and Hakoshima, T. (2008) Structural basis for CD44 recognition by ERM proteins. J. Biol. Chem. 283, 29602-29612
71. Yonemura, S., Tsukita, S., and Tsukita, S. (1999) Direct involvement of ezrin/radixin/moesin (ERM)-binding membrane proteins in the organization of microvilli in collaboration with activated ERM proteins. J. Cell Biol. 145, 1497-1509
72. Díaz-Perales, A., Quesada, V., Peinado, J. R., Ugalde, A. P., Alvarez, J., Suárez, M. F., Gomis-Rüth, F. X., and López-Otín, C. (2005) Identification and characterization of human archaemetzincin-1 and -2, two novel members of a family of metalloproteases widely distributed in Archaea. J. Biol. Chem. 280, 30367-30375
73. Nunomura, W., Takakuwa, Y., Tokimitsu, R., Krauss, S. W., Kawashima, M., and Mohandas, N. (1997) Regulation of CD44-protein 4.1 interaction by Ca2+ and calmodulin. Implications for modulation of CD44-ankyrin interaction. J. Biol. Chem. 272, 30322-30328
74. Terawaki, S., Kitano, K., Mori, T., Zhai, Y., Higuchi, Y., Itoh, N., Watanabe, T., Kaibuchi, K., and Hakoshima, T. (2010) The PHCCEx domain of Tiam1/2 is a novel protein- and membrane-binding module. EMBO J. 29, 236-250
75. Lefebvre, D. C., Lai, J. C., Maeshima, N., Ford, J. L., Wong, A. S., Cross, J. L., and Johnson, P. (2010) CD44 interacts directly with Lck in a zinc-dependent manner. Mol. Immunol. 47, 1882-1889
76. Yang, C., Cao, M., Liu, H., He, Y., Xu, J., Du, Y., Liu, Y., Wang, W., Cui, L., Hu, J., and Gao, F. (2012) The high and low molecular weight forms of hyaluronan have distinct effects on CD44 clustering. J. Biol. Chem. 287, 43094-43107
77. Tammi, R., Säämänen, A. M., Maibach, H. I., and Tammi, M. (1991) Degradation of newly synthesized high molecular mass hyaluronan in the epidermal and dermal compartments of human skin in organ culture. J. Invest. Dermatol. 97, 126-130
78. Wolny, P. M., Banerji, S., Gounou, C., Brisson, A. R., Day, A. J., Jackson, D. G., and Richter, R. P. (2010) Analysis of CD44-hyaluronan interactions in an artificial membrane system: insights into the distinct binding properties of high and low molecular weight hyaluronan. J. Biol. Chem. 285, 30170-30180
79. Kothapalli, D., Flowers, J., Xu, T., Puré, E., and Assoian, R. K. (2008) Differential activation of ERK and Rac mediates the proliferative and anti-proliferative effects of hyaluronan and CD44. J. Biol. Chem. 283, 31823-31829
80. Evanko, S. P., Potter-Perigo, S., Johnson, P. Y., and Wight, T. N. (2009) Organization of hyaluronan and versican in the extracellular matrix of human fibroblasts treated with the viral mimetic poly I:C. J. Histochem. Cytochem. 57, 1041-1060
81. de La Motte, C. A., Hascall, V. C., Calabro, A., Yen-Lieberman, B., and Strong, S. A. (1999) Mononuclear leukocytes preferentially bind via CD44 to hyaluronan on human intestinal mucosal smooth muscle cells after virus infection or treatment with poly(I·C). J. Biol. Chem. 274, 30747-30755
82. Majors, A. K., Austin, R. C., de la Motte, C. A., Pyeritz, R. E., Hascall, V. C., Kessler, S. P., Sen, G., and Strong, S. A. (2003) Endoplasmic reticulum stress induces hyaluronan deposition and leukocyte adhesion. J. Biol. Chem. 278, 47223-47231
83. Selbi, W., de la Motte, C. A., Hascall, V. C., Day, A. J., Bowen, T., and Phillips, A. O. (2006) Characterization of hyaluronan cable structure and function in renal proximal tubular epithelial cells. Kidney Int. 70, 1287-1295
84. Simpson, R. M., Meran, S., Thomas, D., Stephens, P., Bowen, T., Steadman, R., and Phillips, A. (2009) Age-related changes in pericellular hyaluronan organization leads to impaired dermal fibroblast to myofibroblast differentiation. Am. J. Pathol. 175, 1915-1928
85. Wang, A., and Hascall, V. C. (2004) Hyaluronan structures synthesized by rat mesangial cells in response to hyperglycemia induce monocyte adhesion. J. Biol. Chem. 279, 10279-10285
86. Webber, J., Meran, S., Steadman, R., and Phillips, A. (2009) Hyaluronan orchestrates transforming growth factor-β1-dependent maintenance of myofibroblast phenotype. J. Biol. Chem. 284, 9083-9092
87. Rauhala, L., Hämäläinen, L., Salonen, P., Bart, G., Tammi, M., Pasonen-Seppänen, S., and Tammi, R. (2013) Low dose ultraviolet B irradiation increases hyaluronan synthesis in epidermal keratinocytes via sequential induction of hyaluronan synthases Has1-3 mediated by p38 and Ca2+/calmodulin-dependent protein kinase II (CaMKII) signaling. J. Biol. Chem. 288, 17999-18012
88. Lesley, J., English, N., Charles, C., and Hyman, R. (2000) The role of the CD44 cytoplasmic and transmembrane domains in constitutive and inducible hyaluronan binding. Eur. J. Immunol. 30, 245-253
89. Perschl, A., Lesley, J., English, N., Trowbridge, I., and Hyman, R. (1995) Role of CD44 cytoplasmic domain in hyaluronan binding. Eur. J. Immunol. 25, 495-501
90. Sleeman, J., Rudy, W., Hofmann, M., Moll, J., Herrlich, P., and Ponta, H. (1996) Regulated clustering of variant CD44 proteins increases their hyaluronate binding capacity. J. Cell Biol. 135, 1139-1150
91. Liu, D., Liu, T., and Sy, M. S. (1998) Identification of two regions in the cytoplasmic domain of CD44 through which PMA, calcium, and foskolin differentially regulate the binding of CD44 to hyaluronic acid. Cell Immunol. 190, 132-140
92. Kultti, A., Rilla, K., Tiihonen, R., Spicer, A. P., Tammi, R. H., and Tammi, M. I. (2006) Hyaluronan synthesis induces microvillus-like cell surface protrusions. J. Biol. Chem. 281, 15821-15828
93. Rilla, K., Tiihonen, R., Kultti, A., Tammi, M., and Tammi, R. (2008) Peri-cellular hyaluronan coat visualized in live cells with a fluorescent probe is scaffolded by plasma membrane protrusions. J. Histochem. Cytochem. 56, 901-910
94. Nasti, T. H., and Timares, L. (2012) Inflammasome activation of IL-1 family mediators in response to cutaneous photodamage. Photochem. Photobiol. 88, 1111-1125
95. Jensen, L. E. (2010) Targeting the IL-1 family members in skin inflammation. Curr. Opin. Investig. Drugs 11, 1211-1220
96. Groves, R. W., Sherman, L., Mizutani, H., Dower, S. K., and Kupper, T. S. (1994) Detection of interleukin-1 receptors in human epidermis: induction of the type II receptor after organ culture and in psoriasis. Am. J. Pathol. 145, 1048-1056
97. Mee, J. B., Johnson, C. M., Morar, N., Burslem, F., and Groves, R. W. (2007) The psoriatic transcriptome closely resembles that induced by interleukin-1 in cultured keratinocytes: dominance of innate immune responses in psoriasis. Am. J. Pathol. 171, 32-42
98. Dai, X., Okazaki, H., Hanakawa, Y., Murakami, M., Tohyama, M., Shirakata, Y., and Sayama, K. (2013) Eccrine sweat contains IL-1β, IL-1β and IL-31 and activates epidermal keratinocytes as a danger signal. PLoS One 8, e67666
99. Bourguignon, L. Y., Wong, G., Earle, C. A., and Xia, W. (2011) Interaction of low molecular weight hyaluronan with CD44 and toll-like receptors promotes the actin filament-associated protein 110-actin binding and MyD88-NFκB signaling leading to proinflammatory cytokine/chemokine production and breast tumor invasion. Cytoskeleton 68, 671-693
100. Yamasaki, K., Muto, J., Taylor, K. R., Cogen, A. L., Audish, D., Bertin, J., Grant, E. P., Coyle, A. J., Misaghi, A., Hoffman, H. M., and Gallo, R. L. (2009) NLRP3/cryopyrin is necessary for interleukin-1β (IL-1β) release in response to hyaluronan, an endogenous trigger of inflammation in response to injury. J. Biol. Chem. 284, 12762-12771
101. Huang, Z., Zhao, C., Chen, Y., Cowell, J. A., Wei, G., Kultti, A., Huang, L., Thompson, C. B., Rosengren, S., Frost, G. I., and Shepard, H. M. (2014) Recombinant human hyaluronidase PH20 does not stimulate an acute inflammatory response and inhibits lipopolysaccharide-induced neutrophil recruitment in the air pouch model of inflammation. J. Immunol. 192, 5285-5295
102. Tammi, R., Paukkonen, K., Wang, C., Horsmanheimo, M., and Tammi, M. (1994) Hyaluronan and CD44 in psoriatic skin. Intense staining for hyaluronan on dermal capillary loops and reduced expression of CD44 and hyaluronan in keratinocyte-leukocyte interfaces. Arch. Dermatol. Res. 286, 21-29
103. Buerger, C., Richter, B., Woth, K., Salgo, R., Malisiewicz, B., Diehl, S., Hardt, K., Boehncke, S., and Boehncke, W. H. (2012) Interleukin-1β interferes with epidermal homeostasis through induction of insulin resistance: implications for psoriasis pathogenesis. J. Invest. Dermatol. 132, 2206-2214
104. Kaneko, F., Itoh, N., Yoshida, H., Suzuki, M., and Ono, I. (1991) The cell-components and cytokines in the subcorneal microabscess of psoriasis. Fukushima J. Med. Sci. 37, 103-112
105. Jameson, J. M., Cauvi, G., Sharp, L. L., Witherden, D. A., and Havran, W. L. (2005) Gammadelta T cell-induced hyaluronan production by epithelial cells regulates inflammation. J. Exp. Med. 201, 1269-1279
106. Yonemura, S., Hirao, M., Doi, Y., Takahashi, N., Kondo, T., Tsukita, S., and Tsukita, S. (1998) Ezrin/radixin/moesin (ERM) proteins bind to a positively charged amino acid cluster in the juxta-membrane cytoplasmic domain of CD44, CD43, and ICAM-2. J. Cell Biol. 140, 885-895