Hyaluronan in tissue injury and repair

Annual Review of Cell and Developmental Biology

Volumn 23, Issue , 2007, Pages 435-461

  Jiang, Dianhua ^a   Liang, Jiurong ^a   Noble, Paul W ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CD44; Extracellular matrix; Inflammation; Lung injury; Toll like receptors

Indexed keywords

CELL SURFACE RECEPTOR; HERMES ANTIGEN; HYALURONIC ACID; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; GLUCURONOSYLTRANSFERASE; HYALURONAN SYNTHASE; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

CELL PROTECTION; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; INFLAMMATION; LUNG INJURY; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; TISSUE REPAIR; ANIMAL; IMMUNITY; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; REGENERATION; WOUND HEALING;

ANIMALS; ANTIGENS, CD44; GLUCURONOSYLTRANSFERASE; HUMANS; HYALURONIC ACID; IMMUNITY; REGENERATION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; WOUND HEALING;

EID: 38049066579     PISSN: 10810706     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.cellbio.23.090506.123337     Document Type: Review

References (155)

1. Adamson IY, Bowden DH. 1974. The pathogenesis of bloemycin-induced pulmonary fibrosis in mice. Am. J. Pathol. 77:185-97
2. Akira S. 2006. TLR signaling. Curr. Top. Microbiol. Immunol. 311:1-16
3. Al'Qteishat A, Gaffney J, Krupinski J, Rubio F, West D, et al. 2006. Changes in hyaluronan production and metabolism following ischaemic stroke in man. Brain 129:2158-76
4. Ariel A, Lider O, Brill A, Cahalon L, Savion N, et al. 2000. Induction of interactions between CD44 and hyaluronic acid by a short exposure of human T cells to diverse proinflammatory mediators. Immunology 100:345-51
5. Aruffo A, Stamenkovic I, Melnick M, Underhill CB, Seed B. 1990. CD44 is the principal cell surface receptor for hyaluronate. Cell 61:1303-13
6. Bai KJ, Spicer AP, Mascarenhas MM, Yu L, Ochoa CD, et al. 2005. The role of hyaluronan synthase 3 in ventilator-induced lung injury. Am. J. Respir. Crit. Care Med. 172:92-98
7. Banerji S, Ni J, Wang SX, Clasper S, Su J, et al. 1999. Lyve-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J. Cell Biol. 144:789-801
8. Barsness KA, Arcaroli J, Harken AH, Abraham E, Banerjee A, et al. 2004. Hemorrhage-induced acute lung injury is TLR-4 dependent. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287:R592-99
9. Barton GM, Medzhitov R. 2003. Toll-like receptor signaling pathways. Science 300:1524-25
10. Bates EJ, Harper GS, Lowther DA, Preston BN. 1984. Effect of oxygen-derived reactive species on cartilage proteoglycan-hyaluronate aggregates. Biochem. Int. 8:629-37
11. Beck-Schimmer B, Oertli B, Pasch T, Wuthrich RP. 1998. Hyaluronan induces monocyte chemoattractant protein-1 expression in renal tubular epithelial cells. J. Am. Soc. Nephrol. 9:2283-90
12. Bensadoun ES, Burke AK, Hogg JC, Roberts CR. 1996. Proteoglycan deposition in pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 154:1819-28
13. Biragyn A, Ruffini PA, Leifer CA, Klyushnenkova E, Shakhov A, et al. 2002. Toll-like receptor 4-dependent activation of dendritic cells by beta-defensin 2. Science 298:1025-29
14. 2+ signaling, and cytoskeleton modification in head and neck squamous cell carcinoma cells. J. Biol. Chem. 281:14026-40
15. Bourguignon LY, Gilad E, Rothman K, Peyrollier K. 2005. Hyaluronan-CD44 interaction with IQGAP1 promotes Cdc42 and ERK signaling, leading to actin binding, Elk-1/estrogen receptor transcriptional activation, and ovarian cancer progression. J. Biol. Chem. 280:11961-72
16. Camenisch TD, Schroeder JA, Bradley J, Klewer SE, McDonald JA. 2002. Heart-valve mesenchyme formation is dependent on hyaluronan-augmented activation of ErbB2-ErbB3 receptors. Nat. Med. 8:850-55
17. Camenisch TD, Spicer AP, Brehm-Gibson T, Biesterfeldt J, Augustine ML, et al. 2000. Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme. J. Clin. Invest. 106:349-60
18. Carter GR. 1972. Improved hemagglutination test for identifying type A strains of Pasteurella multocida. Appl. Microbiol. 24:162-63
19. Chao H, Spicer AP. 2005. Natural antisense mRNAs to hyaluronan synthase 2 inhibit hyaluronan biosynthesis and cell proliferation. J. Biol. Chem. 280:27513-22
20. Cherr GN, Meyers SA, Yudin AI, VandeVoort CA, Myles DG, et al. 1996. The PH-20 protein in cynomolgus macaque spermatozoa: identification of two different forms exhibiting hyaluronidase activity. Dev. Biol. 175:142-53
21. Chesnutt AN, Matthay MA, Tibayan FA, Clark JG. 1997. Early detection of type III procollagen peptide in acute lung injury. Pathogenetic and prognostic significance. Am. J. Respir. Crit. Care Med. 156:840-45
22. Csoka AB, Frost GI, Stern R. 2001. The six hyaluronidase-like genes in the human and mouse genomes. Matrix Biol. 20:499-508
23. Csoka AB, Frost GI, Wong T, Stern R. 1997. Purification and microsequencing of hyaluronidase isozymes from human urine. FEBS Lett. 417:307-10
24. Czipri M, Otto JM, Cs-Szabo G, Kamath RV, Vermes C, et al. 2003. Genetic rescue of chondrodysplasia and the perinatal lethal effect of cartilage link protein deficiency. J. Biol. Chem. 278:39214-23
25. DeGrendele HC, Estess P, Siegelman MH. 1997. Requirement for CD44 in activated T cell extravasation into an inflammatory site. Science 278:672-75
26. Diebold SS, Kaisho T, Hemmi H, Akira S, Reis e Sousa C. 2004. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303:1529-31
27. Do Y, Nagarkatti PS, Nagarkatti M. 2004. Role of CD44 and hyaluronic acid (HA) in activation of alloreactive and antigen-specific T cells by bone marrow-derived dendritic cells. J. Immunother. 27:1-12
28. Elias JA, Krol RC, Freundlich B, Sampson PM. 1988. Regulation of human lung fibroblast glycosaminoglycan production by recombinant interferons, tumor necrosis factor, and lymphotoxin. J. Clin. Invest. 81:325-33
29. Engstrom-Laurent A. 1997. Hyaluronan in joint disease. J. Intern. Med. 242:57-60
30. Esnault S, Malter JS. 2003. Hyaluronic acid or TNF-alpha plus fibronectin triggers granulocyte macrophage-colony-stimulating factor mRNA stabilization in eosinophils yet engages differential intracellular pathways and mRNA binding proteins. J. Immunol. 171:6780-87
31. Fan J, Li Y, Vodovotz Y, Billiar TR, Wilson MA. 2006. Hemorrhagic shock-activated neutrophils augment TLR4 signaling-induced TLR2 upregulation in alveolar macrophages: role in hemorrhage-primed lung inflammation. Am. J. Physiol. Lung Cell Mol. Physiol. 290:L738-46
32. lpr kidney: role of cytokines. Nephron 83:66-73
33. Fieber C, Baumann P, Vallon R, Termeer C, Simon JC, et al. 2004. Hyaluronanoligosaccharide-induced transcription of metalloproteases. J. Cell Sci. 117:359-67
34. Fiszer-Szafarz B, Czartoryska B, Tylki-Szymanska A. 2005. Serum hyaluronidase aberrations in metabolic and morphogenetic disorders. Glycoconj. J. 22:395-400
35. Fitzgerald KA, Bowie AG, Skeffington BS, O'Neill LA. 2000. Ras, protein kinase Cζ, and IκB kinases 1 and 2 are downstream effectors of CD44 during the activation of NF-κB by hyaluronic acid fragments in T-24 carcinoma cells. J. Immunol. 164:2053-63
36. Foell D, Wittkowski H, Vogl T, Roth J. 2007. S100 proteins expressed in phagocytes: a novel group of damage-associated molecular pattern molecules. J. Leukoc. Biol. 81:28-37
37. Fraser JR, Laurent TC, Laurent UB. 1997. Hyaluronan: its nature, distribution, functions and turnover. J. Intern. Med. 242:27-33
38. Gale NW, Prevo R, Fematt JE, Ferguson DJ, Dominguez MG, et al. 2007. Normal lymphatic development and function in mice deficient for the lymphatic hyaluronan receptor LYVE-1. Mol. Cell. Biol. 27:595-604
39. George J, Stern R. 2004. Serum hyaluronan and hyaluronidase: very early markers of toxic liver injury. Clin. Chim. Acta 348:189-97
40. Goetinck PF, Stirpe NS, Tsonis PA, Carlone D. 1987. The tandemly repeated sequences of cartilage link protein contain the sites for interaction with hyaluronic acid. J. Cell Biol. 105:2403-8
41. Hall CL, Yang B, Yang X, Zhang S, Turley M, et al. 1995. Overexpression of the hyaluronan receptor RHAMM is transforming and is also required for H-Ras transformation. Cell 82:19-26
42. Hamann KJ, Dowling TL, Neeley SP, Grant JA, Leff AR. 1995. Hyaluronic acid enhances cell proliferation during eosinopoiesis through the CD44 surface antigen. J. Immunol. 154:4073-80
43. Hance AJ, Crystal RG. 1975. The connective tissue of lung. Am. Rev. Respir. Dis. 112:657-711
44. Hansen B, Longati P, Elvevold K, Nedredal GI, Schledzewski K, et al. 2005. Stabilin-1 and stabilin-2 are both directed into the early endocytic pathway in hepatic sinusoidal endothelium via interactions with clathrin/AP-2, independent of ligand binding. Exp. Cell Res. 303:160-73
45. Hardwick C, Hoare K, Owens R, Hohn HP, Hook M, et al. 1992. Molecular cloning of a novel hyaluronan receptor that mediates tumor cell motility. J. Cell Biol. 117:1343-50
46. Harris EN, Kyosseva SV, Weigel JA, Weigel PH. 2007. Expression, processing, and glycosaminoglycan binding activity of the recombinant human 315-kDa hyaluronic acid receptor for endocytosis (HARE). J. Biol. Chem. 282:2785-97
47. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, et al. 2001. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410:1099-1103
48. Hayer S, Steiner G, Gortz B, Reiter E, Tohidast-Akrad M, et al. 2005. CD44 is a determinant of inflammatory bone loss. J. Exp. Med. 201:903-14
49. Hecht JT, Blanton SH, Wang Y, Daiger SP, Horton WA, et al. 1992. Exclusion of human proteoglycan link protein (CRTL1) and type II collagen (COL2A1) genes in pseudoachondroplasia. Am. J. Med. Genet. 44:420-24
50. Heldin P, Asplund T, Ytterberg D, Thelin S, Laurent TC. 1992. Characterization of the molecular mechanism involved in the activation of hyaluronan synthetase by platelet-derived growth factor in human mesothelial cells. Biochem. J. 283(Pt. 1):165-70
51. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, et al. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408:740-45
52. Henke CA, Roongta U, Mickelson DJ, Knutson JR, McCarthy JB. 1996. CD44-related chondroitin sulfate proteoglycan, a cell surface receptor implicated with tumor cell invasion, mediates endothelial cell migration on fibrinogen and invasion into a fibrin matrix. J. Clin. Invest. 97:2541-52
53. Hershon LE. 1971. Elaboration of hyaluronidase and chondroitin sulfatase by microorganisms inhabiting the gingival sulcus: evaluation of a screening method for periodontal disease. J. Periodontol. 42:34-36
54. Hodge-Dufour J, Noble PW, Horton MR, Bao C, Wysoka M, et al. 1997. Induction of IL-12 and chemokines by hyaluronan requires adhesion-dependent priming of resident but not elicited macrophages. J. Immunol. 159:2492-2500
55. Hofmann M, Assmann V, Fieber C, Sleeman JP, Moll J, et al. 1998. Problems with RHAMM: a new link between surface adhesion and oncogenesis? Cell 95:591-92; author reply 592-93
56. Horton MR, Burdick MD, Strieter RM, Bao C, Noble PW. 1998a. Regulation of hyaluronan-induced chemokine gene expression by IL-10 and IFN-γ in mouse macrophages. J. Immunol. 160:3023-30
57. Horton MR, McKee CM, Bao C, Liao F, Farber JM, et al. 1998b. Hyaluronan fragments synergize with interferon-γ to induce the C-X-C chemokines mig and interferon-inducible protein-10 in mouse macrophages. J. Biol. Chem. 273:35088-94
58. Horton MR, Shapiro S, Bao C, Lowenstein CJ, Noble PW. 1999. Induction and regulation of macrophage metalloelastase by hyaluronan fragments in mouse macrophages. J. Immunol. 162:4171-76
59. Huang SS, Liu IH, Smith T, Shah MR, Johnson FE, Huang JS. 2006. CRSBP-1/LYVE-l-null mice exhibit identifiable morphological and functional alterations of lymphatic capillary vessels. FEBS Lett. 580:6259-68
60. Itano N, Sawai T, Atsumi F, Miyaishi O, Taniguchi S, et al. 2004. Selective expression and functional characteristics of three mammalian hyaluronan synthases in oncogenic malignant transformation. J. Biol. Chem. 279:18679-87
61. Itano N, Sawai T, Yoshida M, Lenas P, Yamada Y, et al. 1999. Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties. J. Biol. Chem. 274:25085-92
62. Jacobson A, Brinck J, Briskin MJ, Spicer AP, Heldin P. 2000. Expression of human hyaluronan synthases in response to external stimuli. Biochem. J. 348(Pt. 1):29-35
63. Jiang D, Liang J, Fan J, Yu S, Chen S, et al. 2005. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat. Med. 11:1173-79
64. Jiang D, Liang J, Li Y, Noble PW. 2006. The role of Toll-like receptors in noninfectious lung injury. Cell Res. 16:693-701
65. Johnson GB, Brunn GJ, Kodaira Y, Platt JL. 2002. Receptor-mediated monitoring of tissue well-being via detection of soluble heparan sulfate by Toll-like receptor 4. J. Immunol. 168:5233-39
66. Karimi K, Sarir H, Mortaz E, Smit JJ, Hosseini H, et al. 2006. Toll-like receptor-4 mediates cigarette smoke-induced cytokine production by human macrophages. Respir. Res. 7:66
67. Katoh S, Matsumoto N, Kawakita K, Tominaga A, Kincade PW, Matsukura S. 2003. A role for CD44 in an antigen-induced murine model of pulmonary eosinophilia. J. Clin. Invest. 111:1563-70
68. Khaldoyanidi S, Moll J, Karakhanova S, Herrlich P, Ponta H. 1999. Hyaluronate-enhanced hematopoiesis: Two different receptors trigger the release of interleukin-1β and interleukin-6 from bone marrow macrophages. Blood 94:940-49
69. Kobayashi H, Terao T. 1997. Hyaluronic acid-specific regulation of cytokines by human uterine fibroblasts. Am. J. Physiol. 273:C1151-59
70. Kohda D, Morton CJ, Parkar AA, Hatanaka H, Inagaki FM, et al. 1996. Solution structure of the link module: a hyaluronan-binding domain involved in extracellular matrix stability and cell migration. Cell 86:767-75
71. Kopp EB, Medzhitov R. 1999. The Toll-receptor family and control of innate immunity. Curr. Opin. Immunol. 11:13-18
72. Kreil G. 1995. Hyaluronidases: a group of neglected enzymes. Protein Sci. 4:1666-69
73. Lathrop WF, Carmichael EP, Myles DG, Primakoff P. 1990. cDNA cloning reveals the molecular structure of a sperm surface protein, PH-20, involved in sperm-egg adhesion and the wide distribution of its gene among mammals. J. Cell Biol. 111:2939-49
74. Lawrence T, Bebien M, Liu GY, Nizet V, Karin M. 2005. IKKα limits macrophage NF-κB activation and contributes to the resolution of inflammation. Nature 434:1138-43
75. Lepperdinger G, Strobl B, Kreil G. 1998. HYAL2, a human gene expressed in many cells, encodes a lysosomal hyaluronidase with a novel type of specificity. J. Biol. Chem. 273:22466-70
76. Lesley J, He Q, Miyake K, Hamann A, Hyman R, Kincade PW. 1992. Requirements for hyaluronic acid binding by CD44: a role for the cytoplasmic domain and activation by antibody. J. Exp. Med. 175:257-66
77. Lesley J, Hyman R, Kincade PW. 1993. CD44 and its interaction with extracellular matrix. Adv. Immunol. 54:271-335
78. Li Y, Rahmanian M, Widstrom C, Lepperdinger G, Frost GI, Heldin P. 2000. Irradiation-induced expression of hyaluronan (HA) synthase 2 and hyaluronidase 2 genes in rat lung tissue accompanies active turnover of HA and induction of types I and III collagen gene expression. Am. J. Respir. Cell Mol. Biol. 23:411-18
79. Lindqvist U. 1997. Is serum hyaluronan a helpful tool in the management of patients with liver diseases? J. Intern. Med. 242:67-71
80. Lokeshwar VB, Selzer MG. 2000. Differences in hyaluronic acid-mediated functions and signaling in arterial, microvessel, and vein-derived human endothelial cells. J. Biol. Chem. 275:27641-49
81. Lowther DA, Rogers HJ. 1955. Biosynthesis of hyaluronate. Nature 175:435
82. Maclennan AP. 1956. The production of capsules, hyaluronic acid and hyaluronidase by 25 strains of group C streptococci. J. Gen. Microbiol. 15:485-91
83. Mascarenhas MM, Day RM, Ochoa CD, Choi WI, Yu L, et al. 2004. Low molecular weight hyaluronan from stretched lung enhances interleukin-8 expression. Am. J. Respir. Cell Mol. Biol. 30:51-60
84. McKee CM, Lowenstein CJ, Horton MR, Wu J, Bao C, et al. 1997. Hyaluronan fragments induce nitric-oxide synthase in murine macrophages through a nuclear factor κB-dependent mechanism. J. Biol. Chem. 272:8013-18
85. McKee CM, Penno MB, Cowman M, Burdick MD, Strieter RM, et al. 1996. Hyaluronan (HA) fragments induce chemokine gene expression in alveolar macrophages. The role of HA size and CD44. J. Clin. Invest. 98:2403-13
86. Meduri GU. 1995. Pulmonary fibroproliferation and death in patients with late ARDS. Chest 107:5-6
87. Medzhitov R, Preston-Hurlburt P, Kopp E, Stadlen A, Chen C, et al. 1998. MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol. Cell 2:253-58
88. Meyer K, Palmer JW. 1934. The polysaccharide of the vitreous humor. J. Biol. Chem. 107:629-34
89. Miggin SM, O'Neill LA. 2006. New insights into the regulation of TLR signaling. J. Leukoc. Biol. 80:220-26
90. Mikecz K, Brennan FR, Kim JH, Glant TT. 1995. Anti-CD44 treatment abrogates tissue oedema and leukocyte infiltration in murine arthritis. Nat. Med. 1:558-63
91. Milinkovic M, Antin JH, Hergrueter CA, Underhill CB, Sackstein R. 2004. CD44-hyaluronic acid interactions mediate shear-resistant binding of lymphocytes to dermal endothelium in acute cutaneous GVHD. Blood 103:740-42
92. Mouta Carreira C, Nasser SM, di Tomaso E, Padera TP, Boucher Y, et al. 2001. LYVE-1 is not restricted to the lymph vessels: expression in normal liver blood sinusoids and down-regulation in human liver cancer and cirrhosis. Cancer. Res. 61:8079-84
93. Mummert ME, Mohamadzadeh M, Mummert DI, Mizumoto N, Takashima A. 2000. Development of a peptide inhibitor of hyaluronan-mediated leukocyte trafficking. J. Exp. Med. 192:769-79
94. Nakamura K, Yokohama S, Yoneda M, Okamoto S, Tamaki Y, et al. 2004. High, but not low, molecular weight hyaluronan prevents T-cell-mediated liver injury by reducing proinflammatory cytokines in mice. J. Gastroenterol. 39:346-54
95. Natowicz MR, Short MP, Wang Y, Dickersin GR, Gebhardt MC, et al. 1996. Clinical and biochemical manifestations of hyaluronidase deficiency. N. Engl. J. Med. 335:1029-33
96. Nettelbladt O, Bergh J, Schenholm M, Tengblad A, Hallgren R. 1989. Accumulation of hyaluronic acid in the alveolar interstitial tissue in bleomycin-induced alveolitis. Am. Rev. Respir. Dis. 139:759-62
97. Neudecker BA, Stern R, Connolly MK. 2004. Aberrant serum hyaluronan and hyaluronidase levels in scleroderma. Br. J. Dermatol. 150:469-76
98. Noble PW, Jiang D. 2006. Matrix regulation of lung injury, inflammation, and repair: the role of innate immunity. Proc. Am. Thorac. Soc. 3:401-4
99. Noble PW, Lake FR, Henson PM, Riches DW. 1993. Hyaluronate activation of CD44 induces insulin-like growth factor-1 expression by a tumor necrosis factor-α-dependent mechanism in murine macrophages. J. Clin. Invest. 91:2368-77
100. Noble PW, McKee CM, Cowman M, Shin HS. 1996. Hyaluronan fragments activate an NF-κB/I-κBα autoregulatory loop in murine macrophages. J. Exp. Med. 183:2373-78
101. O'Neill LA. 2005. TLRs play good cop, bad cop in the lung. Nat. Med. 11:1161-62
102. Oertli B, Beck-Schimmer B, Fan X, Wuthrich RP. 1998. Mechanisms of hyaluronan-induced up-regulation of ICAM-1 and VCAM-1 expression by murine kidney tubular epithelial cells: Hyaluronan triggers cell adhesion molecule expression through a mechanism involving activation of nuclear factor-κB and activating protein-1. J. Immunol. 161:3431-37
103. Ohashi K, Burkart V, Flohe S, Kolb H. 2000. Cutting edge: Heat shock protein 60 is a putative endogenous ligand of the Toll-like receptor-4 complex. J. Immunol. 164:558-61
104. Oliferenko S, Kaverina I, Small JV, Huber LA. 2000. Hyaluronic acid (HA) binding to CD44 activates Rac1 and induces lamellipodia outgrowth. J. Cell Biol. 148:1159-64
105. Olman MA, Simmons WL, Pollman DJ, Loftis AY, Bini A, et al. 1996. Polymerization of fibrinogen in murine bleomycin-induced lung injury. Am. J. Physiol. 271:L519-26
106. Osborne-Lawrence SL, Sinclair AK, Hicks RC, Lacey SW, Eddy RL Jr, et al. 1990. Complete amino acid sequence of human cartilage link protein (CRTl1) deduced from cDNA clones and chromosomal assignment of the gene. Genomics 8:562-67
107. Park JS, Svetkauskaite D, He Q, Kim JY, Strassheim D, et al. 2004. Involvement of Toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J. Biol. Chem. 279:7370-77
108. Pienimaki JP, Rilla K, Fulop C, Sironen RK, Karvinen S, et al. 2001. Epidermal growth factor activates hyaluronan synthase 2 in epidermal keratinocytes and increases pericellular and intracellular hyaluronan. J. Biol. Chem. 276:20428-35
109. Politz O, Gratchev A, McCourt PA, Schledzewski K, Guillot P, et al. 2002. Stabilin-1 and -2 constitute a novel family of fasciclin-like hyaluronan receptor homologues. Biochem. J. 362:155-64
110. Ragan C, Meyer K. 1949. The hyaluronic acid of synovial fluid in rheumatoid arthritis. J. Clin. Invest. 28:56-59
111. Rai SK, Duh FM, Vigdorovich V, Danilkovitch-Miagkova A, Lerman MI, Miller AD. 2001. Candidate tumor suppressor HYAL2 is a glycosylphosphatidylinositol (GPI)-anchored cell-surface receptor for Jaagsiekte sheep retrovirus, the envelope protein of which mediates oncogenic transformation. Proc. Natl. Acad. Sci. USA 98:4443-48
112. Raja RH, McGary CT, Weigel PH. 1988. Affinity and distribution of surface and intracellular hyaluronic acid receptors in isolated rat liver endothelial cells. J. Biol. Chem. 263:16661-68
113. Rakoff-Nahoum S, Hao L, Medzhitov R. 2006. Role of Toll-like receptors in spontaneous commensal-dependent colitis. Immunity 25:319-29
114. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. 2004. Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell 118:229-41
115. Regan C, Meyer K. 1950. Hyaluronic acid-hyaluronidase and the rheumatic diseases. Ann. N.Y. Acad. Sci. 52:1108-11
116. Saari H. 1991. Oxygen derived free radicals and synovial fluid hyaluronate. Ann. Rheum. Dis. 50:389-92
117. Saari H, Konttinen YT. 1989. Determination of synovial fluid hyaluronate concentration and polymerisation by high performance liquid chromatography. Ann. Rheum. Dis. 48:565-70
118. Sampson PM, Rochester CL, Freundlich B, Elias JA. 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
119. Sato H, Takahashi T, Ide H, Fukushima T, Tabata M, et al. 1988. Antioxidant activity of synovial fluid, hyaluronic acid, and two subcomponents of hyaluronic acid. Synovial fluid scavenging effect is enhanced in rheumatoid arthritis patients. Arthritis Rheum. 31:63-71
120. Savani RC, Wang C, Yang B, Zhang S, Kinsella MG, et al. 1995. Migration of bovine aortic smooth muscle cells after wounding injury. The role of hyaluronan and RHAMM. J. Clin. Invest. 95:1158-68
121. Schaefer L, Babelova A, Kiss E, Hausser HJ, Baliova M, et al. 2005. The matrix component biglycan is proinflammatory and signals through Toll-like receptors 4 and 2 in macrophages. J. Clin. Invest. 115:2223-33
122. Scheibner KA, Lutz MA, Boodoo S, Fenton MJ, Powell JD, Horton MR. 2006. Hyaluronan fragments act as an endogenous danger signal by engaging TLR2. J. Immunol. 177:1272-81
123. Schmits R, Filmus J, Gerwin N, Senaldi G, Kiefer F, et al. 1997. CD44 regulates hematopoietic progenitor distribution, granuloma formation, and tumorigenicity. Blood 90:2217-33
124. Sherman L, Sleeman J, Herrlich P, Ponta H. 1994. Hyaluronate receptors: key players in growth, differentiation, migration and tumor progression. Curr. Opin. Cell Biol. 6:726-33
125. Slevin M, Krupinski J, Kumar S, Gaffney J. 1998. Angiogenic oligosaccharides of hyaluronan induce protein tyrosine kinase activity in endothelial cells and activate a cytoplasmic signal transduction pathway resulting in proliferation. Lab. Invest. 78:987-1003
126. Spicer AP, McDonald JA. 1998. Characterization and molecular evolution of a vertebrate hyaluronan synthase gene family. J. Biol. Chem. 273:1923-32
127. Spicer AP, Seldin MF, Olsen AS, Brown N, Wells DE, et al. 1997. Chromosomal localization of the human and mouse hyaluronan synthase genes. Genomics 41:493-97
128. Spicer AP, Tien JY. 2004. Hyaluronan and morphogenesis. Birth Defects Res. C 72:89-108
129. Stuhlmeier KM, Pollaschek C. 2004. Differential effect of transforming growth factor beta (TGF-β) on the genes encoding hyaluronan synthases and utilization of the p38 MAPK pathway in TGF-β-induced hyaluronan synthase 1 activation. J. Biol. Chem. 279:8753-60
130. Sugahara KN, Murai T, Nishinakamura H, Kawashima H, Saya H, Miyasaka M. 2003. Hyaluronan oligosaccharides induce CD44 cleavage and promote cell migration in CD44-expressing tumor cells. J. Biol. Chem. 278:32259-65
131. Takeuchi O, Hoshino K, Kawai T, Sanjo H, Takada H, et al. 1999. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 11:443-51
132. Tammi R, Pasonen-Seppanen S, Kolehmainen E, Tammi M. 2005. Hyaluronan synthase induction and hyaluronan accumulation in mouse epidermis following skin injury. J. Invest. Dermatol. 124:898-905
133. Taylor KR, Trowbridge JM, Rudisill JA, Termeer CC, Simon JC, Gallo RL. 2004. Hyaluronan fragments stimulate endothelial recognition of injury through TLR4. J. Biol. Chem. 279:17079-84
134. Teder P, Vandivier RW, Jiang D, Liang J, Cohn L, et al. 2002. Resolution of lung inflammation by CD44. Science 296:155-58
135. Termeer C, Benedix F, Sleeman J, Fieber C, Voith U, et al. 2002. Oligosaccharides of hyaluronan activate dendritic cells via Toll-like receptor 4. J. Exp. Med. 195:99-111
136. Termeer CC, Hennies J, Voith U, Ahrens T, Weiss JM, et al. 2000. Oligosaccharides of hyaluronan are potent activators of dendritic cells. J. Immunol. 165:1863-70
137. Tesar BM, Jiang D, Liang J, Palmer SM, Noble PW, Goldstein DR. 2006. The role of hyaluronan degradation products as innate alloimmune agonists. Am. J. Transplant. 6:2622-35
138. Toole BP. 1990. Hyaluronan and its binding proteins, the hyaladherins. Curr. Opin. Cell Biol. 2:839-44
139. Tsan MF, Gao B. 2004. Endogenous ligands of Toll-like receptors. J. Leukoc. Biol. 76:514-19
140. Underhill DM, Ozinsky A, Smith KD, Aderem A. 1999. Toll-like receptor-2 mediates mycobacteria-induced proinflammatory signaling in macrophages. Proc. Natl. Acad. Sci. USA 96:14459-63
141. Wang CT, Lin YT, Chiang BL, Lin YH, Hou SM. 2006. High molecular weight hyaluronic acid down-regulates the gene expression of osteoarthritis-associated cytokines and enzymes in fibroblast-like synoviocytes from patients with early osteoarthritis. Osteoarthritis Cartilage 14:1237-47
142. Watanabe H, Yamada Y. 1999. Mice lacking link protein develop dwarfism and craniofacial abnormalities. Nat. Genet. 21:225-29
143. Watanabe K, Yamaguchi Y. 1996. Molecular identification of a putative human hyaluronan synthase. J. Biol. Chem. 271:22945-48
144. Weissman B, Meyer K. 1954. The structure of hyalobiuronic acid and of hyaluronic acid from umbilical cord. J. Am. Chem. Soc. 76:1753-57
145. West DC, Hampson IN, Arnold F, Kumar S. 1985. Angiogenesis induced by degradation products of hyaluronic acid. Science 228:1324-26
146. Wilkinson TS, Potter-Perigo S, Tsoi C, Altman LC, Wight TN. 2004. Pro- and antiinflammatory factors cooperate to control hyaluronan synthesis in lung fibroblasts. Am. J. Respir. Cell Mol. Biol. 31:92-99
147. Wuthrich RP. 1999. The proinflammatory role of hyaluronan-CD44 interactions in renal injury. Nephrol. Dial. Transplant 14:2554-56
148. Yamamoto M, Sato S, Hemmi H, Uematsu S, Hoshino K, et al. 2003. TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nat. Immunol. 4:1144-50
149. Yang B, Yang BL, Savani RC, Turley EA. 1994. Identification of a common hyaluronan binding motif in the hyaluronan binding proteins RHAMM, CD44 and link protein. EMBO J. 13:286-96
150. Yang D, Oppenheim JJ. 2004. Antimicrobial proteins act as "alarmins" in joint immune defense. Arthritis Rheum. 50:3401-3
151. Yung S, Thomas GJ, Davies M. 2000. Induction of hyaluronan metabolism after mechanical injury of human peritoneal mesothelial cells in vitro. Kidney Int. 58:1953-62
152. Zaman A, Cui Z, Foley JP, Zhao H, Grimm PC, et al. 2005. Expression and role of the hyaluronan receptor RHAMM in inflammation after bleomycin injury. Am. J. Respir. Cell Mol. Biol. 33:447-54
153. Zhang X, Shan P, Jiang G, Cohn L, Lee PJ. 2006. Toll-like receptor 4 deficiency causes pulmonary emphysema. J. Clin. Invest. 116:3050-59
154. Zhang X, Shan P, Qureshi S, Homer R, Medzhitov R, et al. 2005. Cutting edge: TLR4 deficiency confers susceptibility to lethal oxidant lung injury. J. Immunol. 175:4834-38
155. Zhou B, Weigel JA, Fauss L, Weigel PH. 2000. Identification of the hyaluronan receptor for endocytosis (HARE). J. Biol. Chem. 275:37733-41