High and Low Molecular Weight Hyaluronic Acid Differentially Influence Macrophage Activation

ACS Biomaterials Science and Engineering

Volumn 1, Issue 7, 2015, Pages 481-493

  Rayahin, Jamie E ^a   Buhrman, Jason S ^a   Zhang, Yu ^a   Koh, Timothy J ^a   Gemeinhart, Richard A ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b University of Illinois at Chicago   (United States)

Author keywords

alternatively activated; classically activated; hyaluronic acid; macrophage; molecular weight; polarization

Indexed keywords

ARGINASE; ARGINASE 1; B7 ANTIGEN; HYALURONIC ACID; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 12P40; LIPOPOLYSACCHARIDE; MANNOSE RECEPTOR; MANNOSE RECEPTOR C TYPE 1; MESSENGER RNA; NITRIC OXIDE; NITRITE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UREA;

ANIMAL CELL; ARTICLE; CELL LEVEL; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; ENZYME ACTIVITY; GENETIC TRANSCRIPTION; IN VITRO STUDY; INFLAMMATION; INTRACELLULAR SIGNALING; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; MOLECULAR WEIGHT; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; UREA CYCLE;

EID: 84969262552     PISSN: None     EISSN: 23739878     Source Type: Journal    
DOI: 10.1021/acsbiomaterials.5b00181     Document Type: Article

References (100)

1. Meyer, K.; Palmer, J. W. The Polysaccharide of the Vitreous Humor J. Biol. Chem. 1934, 107, 629-634
2. Meyer, K. The Biological Significance of Hyaluronic Acid and Hyaluronidase Physiol. Rev. 1947, 27, 335-359
3. Necas, J.; Bartosikova, L.; Brauner, P.; Kolar, J. Hyaluronic Acid (Hyaluronan): A Review Vet. Med. 2008, 53, 397-411
4. Collins, M. N.; Birkinshaw, C. Hyaluronic Acid Based Scaffolds for Tissue Engineering-a Review Carbohydr. Polym. 2013, 92, 1262-1279 10.1016/j.carbpol.2012.10.028
5. Colen, S.; van den Bekerom, M. P. J.; Mulier, M.; Haverkamp, D. Hyaluronic Acid in the Treatment of Knee Osteoarthritis a Systematic Review and Meta-Analysis with Emphasis on the Efficacy of Different Products BioDrugs 2012, 26, 257-268 10.2165/11632580-000000000-00000
6. Beasley, K. L.; Weiss, M. A.; Weiss, R. A. Hyaluronic Acid Fillers: A Comprehensive Review Facial Plast. Surg. 2009, 25, 86-94 10.1055/s-0029-1220647
7. Hascall, V.; Esko, J. D. Hyaluronan. In Essentials of Glycobiology, 2nd ed.; Cummings, V. A., Ed.l Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, 2009; Chapter 15.
8. Stern, R.; Kogan, G.; Jedrzejas, M. J.; Soltes, L. The Many Ways to Cleave Hyaluronan Biotechnol. Adv. 2007, 25, 537-557 10.1016/j.biotechadv.2007.07.001
9. Burdick, J. A.; Prestwich, G. D. Hyaluronic Acid Hydrogels for Biomedical Applications Adv. Mater. 2011, 23, H41-56 10.1002/adma.201003963
10. Kogan, G.; Soltes, L.; Stern, R.; Gemeiner, P. Hyaluronic Acid: A Natural Biopolymer with a Broad Range of Biomedical and Industrial Applications Biotechnol. Lett. 2007, 29, 17-25 10.1007/s10529-006-9219-z
11. Liu, X. M.; Harmon, P. S.; Maziarz, E. P.; Rah, M. J.; Merchea, M. M. Comparative Studies of Hyaluronan in Marketed Ophthalmic Products Optom. Vis. Sci. 2014, 91, 32-38 10.1097/OPX.0000000000000100
12. Balazs, E. A. Hyaluronan as an Ophthalmic Viscoelastic Device Curr. Pharm. Biotechnol. 2008, 9, 236-238
13. Wobig, M.; Bach, G.; Beks, P.; Dickhut, A.; Runzheimer, J.; Schwieger, G.; Vetter, G.; Balazs, E. The Role of Elastoviscosity in the Efficacy of Viscosupplementation for Osteoarthritis of the Knee: A Comparison of Hylan G-F 20 and a Lower-Molecular-Weight Hyaluronan Clin. Ther. 1999, 21, 1549-1562 10.1016/S0149-2918(00)80010-7
14. Pelletier, J. P.; Martel-Pelletier, J. The Pathophysiology of Osteoarthritis and the Implication of the Use of Hyaluronan and Hylan as Therapeutic Agents in Viscosupplementation J. Rheumatol. 1993, 39, S19-S24
15. Guidolin, D.; Franceschi, F. Viscosupplementation with High Molecular Weight Native Hyaluronan. Focus on a 1500-2000 Kda Fraction (Hyalubrix(R) Eur. Rev. Med. Pharmacol. Sci. 2014, 18, 3326-3338
16. Nicoletti, G.; Ghilardi, C. G.; Scevola, S.; Faga, A. Hyaluronan-Induced Cosmetic Reconstruction of the Nostril Facial Plast. Surg. 2014, 30, 81-83 10.1055/s-0033-1363757
17. McCracken, M. S.; Khan, J. A.; Wulc, A. E.; Holds, J. B.; Fante, R. G.; Migliori, M. E.; Ebroon, D. A.; Amato, M. M.; Silkiss, R. Z.; Patel, B. C. Hyaluronic Acid Gel (Restylane) Filler for Facial Rhytids: Lessons Learned from American Society of Ophthalmic Plastic and Reconstructive Surgery Member Treatment of 286 Patients Ophthal. Plast. Reconstr. Surg. 2006, 22, 188-191 10.1097/01.iop.0000217562.64529.ff
18. Remes, A.; Williams, D. F. Immune Response in Biocompatibility Biomaterials 1992, 13, 731-743 10.1016/0142-9612(92)90010-L
19. Ialenti, A.; Di Rosa, M. Hyaluronic Acid Modulates Acute and Chronic Inflammation Agents Actions 1994, 43, 44-47 10.1007/BF02005763
20. He, H.; Zhang, S.; Tighe, S.; Son, J.; Tseng, S. C. Immobilized Heavy Chain-Hyaluronic Acid Polarizes Lipopolysaccharide-Activated Macrophages toward M2 Phenotype J. Biol. Chem. 2013, 288, 25792-25803 10.1074/jbc.M113.479584
21. Kuang, D. M.; Wu, Y.; Chen, N.; Cheng, J.; Zhuang, S. M.; Zheng, L. Tumor-Derived Hyaluronan Induces Formation of Immunosuppressive Macrophages through Transient Early Activation of Monocytes Blood 2007, 110, 587-595 10.1182/blood-2007-01-068031
22. Maharjan, A. S.; Pilling, D.; Gomer, R. H. High and Low Molecular Weight Hyaluronic Acid Differentially Regulate Human Fibrocyte Differentiation PLoS One 2011, 6, e26078 10.1371/journal.pone.0026078
23. Mytar, B.; Woloszyn, M.; Szatanek, R.; Baj-Krzyworzeka, M.; Siedlar, M.; Ruggiero, I.; Wieckiewicz, J.; Zembala, M. Tumor Cell-Induced Deactivation of Human Monocytes J. Leukocyte Biol. 2003, 74, 1094-1101 10.1189/jlb.0403140
24. Sokolowska, M.; Chen, L. Y.; Eberlein, M.; Martinez-Anton, A.; Liu, Y.; Alsaaty, S.; Qi, H. Y.; Logun, C.; Horton, M.; Shelhamer, J. H. Low Molecular Weight Hyaluronan Activates Cytosolic Phospholipase A2alpha and Eicosanoid Production in Monocytes and Macrophages J. Biol. Chem. 2014, 289, 4470-4488 10.1074/jbc.M113.515106
25. Toole, B. P. Hyaluronan: From Extracellular Glue to Pericellular Cue Nat. Rev. Cancer 2004, 4, 528-539 10.1038/nrc1391
26. Black, K. E.; Collins, S. L.; Hagan, R. S.; Hamblin, M. J.; Chan-Li, Y.; Hallowell, R. W.; Powell, J. D.; Horton, M. R. Hyaluronan Fragments Induce Ifnbeta Via a Novel Tlr4-Trif-Tbk1-Irf3-Dependent Pathway J. Inflammation 2013, 10, 23 10.1186/1476-9255-10-23
27. McKee, C. M.; Penno, M. B.; Cowman, M.; Burdick, M. D.; Strieter, R. M.; Bao, C.; Noble, P. W. Hyaluronan (Ha) Fragments Induce Chemokine Gene Expression in Alveolar Macrophages. The Role of Ha Size and Cd44 J. Clin. Invest. 1996, 98, 2403-2413 10.1172/JCI119054
28. Termeer, C.; Benedix, F.; Sleeman, J.; Fieber, C.; Voith, U.; Ahrens, T.; Miyake, K.; Freudenberg, M.; Galanos, C.; Simon, J. C. Oligosaccharides of Hyaluronan Activate Dendritic Cells Via Toll-Like Receptor 4 J. Exp. Med. 2002, 195, 99-111 10.1084/jem.20001858
29. Ghosh, P. The Role of Hyaluronic Acid (Hyaluronan) in Health and Disease: Interactions with Cells, Cartilage and Components of Synovial Fluid Clin. Exp. Rheumatol. 1994, 12, 75-82
30. Garg, H. G.; Hales, C. A. Chemistry and Biology of Hyaluronan, 1st ed.; Elsevier: Boston, 2004.
31. Fraser, J. R.; Laurent, T. C.; Laurent, U. B. Hyaluronan: Its Nature, Distribution, Functions and Turnover J. Intern. Med. 1997, 242, 27-33 10.1046/j.1365-2796.1997.00170.x
32. Mosser, D. M. The Many Faces of Macrophage Activation J. Leukocyte Biol. 2003, 73, 209-212 10.1189/jlb.0602325
33. Martinez, F. O.; Gordon, S. The M1 and M2 Paradigm of Macrophage Activation: Time for Reassessment F1000Prime Rep. 2014, 6, 13 10.12703/P6-13
34. Mosser, D. M.; Edwards, J. P. Exploring the Full Spectrum of Macrophage Activation Nat. Rev. Immunol. 2008, 8, 958-969 10.1038/nri2448
35. Mosser, D. M.; Zhang, X. Activation of Murine Macrophages Curr. Prot. Immunol. 2008, 83, 14.2.1-14.2.8 10.1002/0471142735.im1402s83
36. Martinez, F. O.; Sica, A.; Mantovani, A.; Locati, M. Macrophage Activation and Polarization Front. Biosci., Landmark Ed. 2008, 13, 453-461 10.2741/2692
37. Stein, M.; Keshav, S.; Harris, N.; Gordon, S. Interleukin-4 Potently Enhances Murine Macrophage Mannose Receptor Activity-a Marker of Alternative Immunological Macrophage Activation J. Exp. Med. 1992, 176, 287-292 10.1084/jem.176.1.287
38. Odegaard, J. I.; Chawla, A. Alternative Macrophage Activation and Metabolism Annu. Rev. Pathol.: Mech. Dis. 2011, 6, 275-297 10.1146/annurev-pathol-011110-130138
39. Gordon, S.; Martinez, F. O. Alternative Activation of Macrophages: Mechanism and Functions Immunity 2010, 32, 593-604 10.1016/j.immuni.2010.05.007
40. Gordon, S. Alternative Activation of Macrophages Nat. Rev. Immunol. 2003, 3, 23-35 10.1038/nri978
41. Luo, Y.; Prestwich, G. D. Synthesis and Selective Cytotoxicity of a Hyaluronic Acid-Antitumor Bioconjugate Bioconjugate Chem. 1999, 10, 755-763 10.1021/bc9900338
42. Schiller, J.; Arnhold, J.; Benard, S.; Reichl, S.; Arnold, K. Cartilage Degradation by Hyaluronate Lyase and Chondroitin Abc Lyase: A Maldi-Tof Mass Spectrometric Study Carbohydr. Res. 1999, 318, 116-122 10.1016/S0008-6215(99)00063-4
43. Yeung, B.; Marecak, D. Molecular Weight Determination of Hyaluronic Acid by Gel Filtration Chromatography Coupled to Matrix-Assisted Laser Desorption Ionization Mass Spectrometry J. Chromatogr. A 1999, 852, 573-581 10.1016/S0021-9673(99)00647-0
44. Tezel, A.; Fredrickson, G. H. The Science of Hyaluronic Acid Dermal Fillers J. Cosmet. Laser Ther. 2008, 10, 35-42 10.1080/14764170701774901
45. Bellamy, N.; Campbell, J.; Robinson, V.; Gee, T.; Bourne, R.; Wells, G. Viscosupplementation for the Treatment of Osteoarthritis of the Knee Cochrane Database Syst. Rev. 2006, CD005321
46. Lo, G. H.; LaValley, M.; McAlindon, T.; Felson, D. T. Intra-Articular Hyaluronic Acid in Treatment of Knee Osteoarthritis: A Meta-Analysis JAMA, J. Am. Med. Assoc. 2003, 290, 3115-3121 10.1001/jama.290.23.3115
47. Laurent, T. C.; Fraser, J. R. The Properties and Turnover of Hyaluronan Ciba Found. Symp. 1986, 124, 9-29
48. Laurent, U. B. Hyaluronate in Aqueous Humour Exp. Eye Res. 1981, 33, 147-155 10.1016/S0014-4835(81)80063-2
49. Pettersson, T.; Froseth, B.; Riska, H.; Klockars, M. Concentration of Hyaluronic Acid in Pleural Fluid as a Diagnostic Aid for Malignant Mesothelioma Chest 1988, 94, 1037-1039 10.1378/chest.94.5.1037
50. Balazs, E. A.; Watson, D.; Duff, I. F.; Roseman, S. Hyaluronic Acid in Synovial Fluid. I. Molecular Parameters of Hyaluronic Acid in Normal and Arthritis Human Fluids Arthritis Rheum. 1967, 10, 357-376 10.1002/art.1780100407
51. Ralph, P.; Moore, M. A.; Nilsson, K. Lysozyme Synthesis by Established Human and Murine Histiocytic Lymphoma Cell Lines J. Exp. Med. 1976, 143, 1528-1533 10.1084/jem.143.6.1528
52. Ralph, P.; Nakoinz, I. Antibody-Dependent Killing of Erythrocyte and Tumor Targets by Macrophage-Related Cell Lines: Enhancement by Ppd and Lps J. Immunol. 1977, 119, 950-954
53. Iyamu, E. W.; Asakura, T.; Woods, G. M. A Colorimetric Microplate Assay Method for High-Throughput Analysis of Arginase Activity in Vitro Anal. Biochem. 2008, 383, 332-334 10.1016/j.ab.2008.08.016
54. Morris, S. M.; Kepka-Lenhart, D.; Chen, L. C. Differential Regulation of Arginases and Inducible Nitric Oxide Synthase in Murine Macrophage Cells Am. J. Physiol.: Endocrinol. Metab. 1998, 275, E740-E747
55. Schenborn, E.; Groskreutz, D. Reporter Gene Vectors and Assays Mol. Biotechnol. 1999, 13, 29-44 10.1385/MB:13:1:29
56. Schmittgen, T. D.; Livak, K. J. Analyzing Real-Time Pcr Data by the Comparative C(T) Method Nat. Protoc. 2008, 3, 1101-1108 10.1038/nprot.2008.73
57. Gordon, S. Macrophage Heterogeneity and Tissue Lipids J. Clin. Invest. 2007, 117, 89-93 10.1172/JCI30992
58. Chow, J. C.; Young, D. W.; Golenbock, D. T.; Christ, W. J.; Gusovsky, F. Toll-Like Receptor-4 Mediates Lipopolysaccharide-Induced Signal Transduction J. Biol. Chem. 1999, 274, 10689-10692 10.1074/jbc.274.16.10689
59. Iwamoto, M.; Kurachi, M.; Nakashima, T.; Kim, D.; Yamaguchi, K.; Oda, T.; Iwamoto, Y.; Muramatsu, T. Structure-Activity Relationship of Alginate Oligosaccharides in the Induction of Cytokine Production from Raw264.7 Cells FEBS Lett. 2005, 579, 4423-4429 10.1016/j.febslet.2005.07.007
60. Rogers, T. H.; Babensee, J. E. Altered Adherent Leukocyte Profile on Biornaterials in Toll-Like Receptor 4 Deficient Mice Biomaterials 2010, 31, 594-601 10.1016/j.biomaterials.2009.09.077
61. Grandjean-Laquerriere, A.; Tabary, O.; Jacquot, J.; Richard, D.; Frayssinet, P.; Guenounou, M.; Laurent-Maquin, D.; Laquerriere, P.; Gangloff, S. Involvement of Toll-Like Receptor 4 in the Inflammatory Reaction Induced by Hydroxyapatite Particles Biomaterials 2007, 28, 400-404 10.1016/j.biomaterials.2006.09.015
62. Campo, G. M.; Avenoso, A.; Campo, S.; D'Ascola, A.; Traina, P.; Rugolo, C. A.; Calatroni, A. Differential Effect of Molecular Mass Hyaluronan on Lipopolysaccharide-Induced Damage in Chondrocytes Innate Immun. 2010, 16, 48-63 10.1177/1753425909340419
63. Hu, X.; Ivashkiv, L. B. Cross-Regulation of Signaling Pathways by Interferon-Gamma: Implications for Immune Responses and Autoimmune Diseases Immunity 2009, 31, 539-50 10.1016/j.immuni.2009.09.002
64. Mantovani, A.; Sica, A.; Sozzani, S.; Allavena, P.; Vecchi, A.; Locati, M. The Chemokine System in Diverse Forms of Macrophage Activation and Polarization Trends Immunol. 2004, 25, 677-686 10.1016/j.it.2004.09.015
65. Porcheray, F.; Viaud, S.; Rimaniol, A.-C.; Leone, C.; Samah, B.; Dereuddre-Bosquet, N.; Dormont, D.; Gras, G. Macrophage Activation Switching: An Asset for the Resolution of Inflammation Clin. Exp. Immunol. 2005, 142, 481-489 10.1111/j.1365-2249.2005.02934.x
66. Noble, P. W. Hyaluronan and Its Catabolic Products in Tissue Injury and Repair Matrix Biol. 2002, 21, 25-29 10.1016/S0945-053X(01)00184-6
67. Chen, W. Y. J.; Abatangelo, G. Functions of Hyaluronan in Wound Repair Wound Repair Regen. 1999, 7, 79-89 10.1046/j.1524-475X.1999.00079.x
68. Oksala, O.; Salo, T.; Tammi, R.; Hakkinen, L.; Jalkanen, M.; Inki, P.; Larjava, H. Expression of Proteoglycans and Hyaluronan During Wound-Healing J. Histochem. Cytochem. 1995, 43, 125-135 10.1177/43.2.7529785
69. Ponta, H.; Sherman, L.; Herrlich, P. A. Cd44: From Adhesion Molecules to Signalling Regulators Nat. Rev. Mol. Cell Biol. 2003, 4, 33-45 10.1038/nrm1004
70. Gee, K.; Lim, W.; Ma, W.; Nandan, D.; Diaz-Mitoma, F.; Kozlowski, M.; Kumar, A. Differential Regulation of Cd44 Expression by Lipopolysaccharide (Lps) and Tnf-Alpha in Human Monocytic Cells: Distinct Involvement of C-Jun N-Terminal Kinase in Lps-Induced Cd44 Expression J. Immunol. 2002, 169, 5660-5672 10.4049/jimmunol.169.10.5660
71. Hodge-Dufour, J.; Noble, P. W.; Horton, M. R.; Bao, C.; Wysoka, M.; Burdick, M. D.; Strieter, R. M.; Trinchieri, G.; Pure, E. Induction of Il-12 and Chemokines by Hyaluronan Requires Adhesion-Dependent Priming of Resident but Not Elicited Macrophages J. Immunol. 1997, 159, 2492-2500
72. Levesque, M. C.; Haynes, B. F. Cytokine Induction of the Ability of Human Monocyte Cd44 to Bind Hyaluronan Is Mediated Primarily by Tnf-Alpha and Is Inhibited by Il-4 and Il-13 J. Immunol. 1997, 159, 6184-6194
73. Underhill, C. B.; Nguyen, H. A.; Shizari, M.; Culty, M. Cd44 Positive Macrophages Take up Hyaluronan During Lung Development Dev. Biol. 1993, 155, 324-336 10.1006/dbio.1993.1032
74. Levesque, M. C.; Haynes, B. F. Tnf Alpha and Il-4 Regulation of Hyaluronan Binding to Monocyte Cd44 Involves Posttranslational Modification of Cd44 Cell. Immunol. 1999, 193, 209-218 10.1006/cimm.1999.1456
75. Brown, K. L.; Maiti, A.; Johnson, P. Role of Sulfation in Cd44-Mediated Hyaluronan Binding Induced by Inflammatory Mediators in Human Cd14(+) Peripheral Blood Monocytes J. Immunol. 2001, 167, 5367-5374 10.4049/jimmunol.167.9.5367
76. Pure, E.; Cuff, C. A. A Crucial Role for Cd44 in Inflammation Trends Mol. Med. 2001, 7, 213-221 10.1016/S1471-4914(01)01963-3
77. Bollyky, P. L.; Lord, J. D.; Masewicz, S. A.; Evanko, S. P.; Buckner, J. H.; Wight, T. N.; Nepom, G. T. Cutting Edge: High Molecular Weight Hyaluronan Promotes the Suppressive Effects of Cd4+Cd25+ Regulatory T Cells J. Immunol. 2007, 179, 744-747 10.4049/jimmunol.179.2.744
78. Firan, M.; Dhillon, S.; Estess, P.; Siegelman, M. H. Suppressor Activity and Potency among Regulatory T Cells Is Discriminated by Functionally Active Cd44 Blood 2006, 107, 619-627 10.1182/blood-2005-06-2277
79. Zorro Manrique, S.; Duque Correa, M. A.; Hoelzinger, D. B.; Dominguez, A. L.; Mirza, N.; Lin, H. H.; Stein-Streilein, J.; Gordon, S.; Lustgarten, J. Foxp3-Positive Macrophages Display Immunosuppressive Properties and Promote Tumor Growth J. Exp. Med. 2011, 208, 1485-1499 10.1084/jem.20100730
80. Hart, S. P.; Rossi, A. G.; Haslett, C.; Dransfield, I. Characterization of the Effects of Cross-Linking of Macrophage Cd44 Associated with Increased Phagocytosis of Apoptotic Pmn PLoS One 2012, 7, e33142 10.1371/journal.pone.0033142
81. Vivers, S.; Dransfield, I.; Hart, S. P. Role of Macrophage Cd44 in the Disposal of Inflammatory Cell Corpses Clin. Sci. 2002, 103, 441-449 10.1042/CS20020115
82. Kaisho, T.; Akira, S. Toll-Like Receptors and Their Signaling Mechanism in Innate Immunity Acta Odontol. Scand. 2001, 59, 124-130 10.1080/000163501750266701
83. Medzhitov, R. Toll-Like Receptors and Innate Immunity Nat. Rev. Immunol. 2001, 1, 135-145 10.1038/35100529
84. Akira, S.; Takeda, K. Toll-Like Receptor Signalling Nat. Rev. Immunol. 2004, 4, 499-511 10.1038/nri1391
85. Hume, D. A.; Underhill, D. M.; Sweet, M. J.; Ozinsky, A. O.; Liew, F. Y.; Aderem, A. Macrophages Exposed Continuously to Lipopolysaccharide and Other Agonists That Act Via Toll-Like Receptors Exhibit a Sustained and Additive Activation State BMC Immunol. 2001, 2, 11 10.1186/1471-2172-2-11
86. Campo, G. M.; Avenoso, A.; Campo, S.; D'Ascola, A.; Nastasi, G.; Calatroni, A. Molecular Size Hyaluronan Differently Modulates Toll-Like Receptor-4 in Lps-Induced Inflammation in Mouse Chondrocytes Biochimie 2010, 92, 204-215 10.1016/j.biochi.2009.10.006
87. McWhorter, F. Y.; Wang, T.; Nguyen, P.; Chung, T.; Liu, W. F. Modulation of Macrophage Phenotype by Cell Shape Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 17253-17258 10.1073/pnas.1308887110
88. Matou-Nasri, S.; Gaffney, J.; Kumar, S.; Slevin, M. Oligosaccharides of Hyaluronan Induce Angiogenesis through Distinct Cd44 and Rhamm-Mediated Signalling Pathways Involving Cdc2 and Gamma-Adducin Int. J. Oncol. 2009, 35, 761-773 10.3892/ijo-00000389
89. Hardwick, C.; Hoare, K.; Owens, R.; Hohn, H. P.; Hook, M.; Moore, D.; Cripps, V.; Austen, L.; Nance, D. M.; Turley, E. A. Molecular-Cloning of a Novel Hyaluronan Receptor That Mediates Tumor-Cell Motility J. Cell Biol. 1992, 117, 1343-1350 10.1083/jcb.117.6.1343
90. Hofmann, M.; Fieber, C.; Assmann, V.; Gottlicher, M.; Sleeman, J.; Plug, R.; Howells, N.; von Stein, O.; Ponta, H.; Herrlich, P. Identification of Ihabp, a 95 Kda Intracellular Hyaluronate Binding Protein J. Cell Sci. 1998, 111 (Pt 12) 1673-1684
91. Zhang, S.; Chang, M. C.; Zylka, D.; Turley, S.; Harrison, R.; Turley, E. A. The Hyaluronan Receptor Rhamm Regulates Extracellular-Regulated Kinase J. Biol. Chem. 1998, 273, 11342-11348 10.1074/jbc.273.18.11342
92. Entwistle, J.; Hall, C. L.; Turley, E. A. Receptors: Regulators of Signalling to the Cytoskeleton J. Cell. Biochem. 1996, 61, 569-577 10.1002/(SICI)1097-4644(19960616)61:4<569::AID-JCB10>3.0.CO;2-B
93. Nikitovic, D.; Kouvidi, K.; Karamanos, N. K.; Tzanakakis, G. N. The Roles of Hyaluronan/Rhamm/Cd44 and Their Respective Interactions Along the Insidious Pathways of Fibrosarcoma Progression BioMed Res. Int. 2013, 2013, 929531 10.1155/2013/929531
94. Taylor, K. R.; Yamasaki, K.; Radek, K. A.; Di Nardo, A.; Goodarzi, H.; Golenbock, D.; Beutler, B.; Gallo, R. L. Recognition of Hyaluronan Released in Sterile Injury Involves a Unique Receptor Complex Dependent on Toll-Like Receptor 4, Cd44, and Md-2 J. Biol. Chem. 2007, 282, 18265-18275 10.1074/jbc.M606352200
95. Takahashi, R.; Kubota, K.; Kawada, M.; Okamoto, A. Effect of Molecular Weight Distribution on the Solution Properties of Sodium Hyaluronate in 0.2m Nacl Solution Biopolymers 1999, 50, 87-98 10.1002/(SICI)1097-0282(199907)50:1<87::AID-BIP8>3.0.CO;2-K
96. Gribbon, P.; Heng, B. C.; Hardingham, T. E. The Analysis of Intermolecular Interactions in Concentrated Hyaluronan Solutions Suggest No Evidence for Chain-Chain Association Biochem. J. 2000, 350 (Pt 1) 329-335 10.1042/0264-6021:3500329
97. Shimada, E.; Matsumura, G. Viscosity and Molecular-Weight of Hyaluronic Acids J. Biochem. 1975, 78, 513-517
98. Matsuoka, S.; Cowman, M. K. Equation of State for Polymer Solution Polymer 2002, 43, 3447-3453
99. Mendichi, R.; Soltes, L.; Giacometti Schieroni, A. Evaluation of Radius of Gyration and Intrinsic Viscosity Molar Mass Dependence and Stiffness of Hyaluronan Biomacromolecules 2003, 4, 1805-1810
100. Laurent, T. C.; Fraser, J. R. Hyaluronan FASEB J. 1992, 6, 2397-2404