The CD44/integrins interplay and the significance of receptor binding and re-presentation in the uptake of RGD-functionalized hyaluronic acid

Biomaterials

Volumn 33, Issue 4, 2012, Pages 1120-1134

  Ouasti, Sihem ^a   Kingham, Paul J ^a,b   Terenghi, Giorgio ^a   Tirelli, Nicola ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

CD44; Hyaluronic acid; Integrin; Macrophages; RGD

Indexed keywords

ANCILLARY LIGANDS; CD44; CELL SURFACES; FUNCTIONALIZED; HYALURONIC ACIDS; INTEGRINS; MECHANISM AND KINETICS; MULTIPLE LIGANDS; MURINE MACROPHAGES; PHAGOCYTIC CELLS; PRE-CONCENTRATION; RATE DETERMINING STEP; RECEPTOR BINDING; RGD;

CELL MEMBRANES; GLYCOPROTEINS; MACROMOLECULES; MACROPHAGES; ORGANIC ACIDS;

LIGANDS;

ALPHA5 INTEGRIN; ARGINYLGLYCYLASPARTIC ACID; HERMES ANTIGEN; HYALURONIC ACID;

ANIMAL CELL; ARTICLE; CELL INTERACTION; CELL KINETICS; CELLULAR DISTRIBUTION; CHEMICAL STRUCTURE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; INTERNALIZATION; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN BINDING; RECEPTOR BINDING;

ANIMALS; ANTIGENS, CD44; CELL LINE; DRUG CARRIERS; ENDOCYTOSIS; HYALURONIC ACID; INTEGRINS; MACROPHAGES; MICE; OLIGOPEPTIDES; PROTEIN BINDING;

MURINAE;

EID: 81355147866     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2011.10.009     Document Type: Article

References (83)

1. Balazs E.A., Denlinger J.L. Viscosupplementation. A new concept in the treatment of osteoarthritis. J Rheumatol 1993, 20:3-9.
2. Divine J.G., Zazulak B.T., Hewett T.E. Viscosupplementation for knee osteoarthritis - a systematic review. Clin Orthop Relat R 2007, 113-122.
3. Brown T.J. The development of hyaluronan as a drug transporter and excipient for chemotherapeutic drugs. Curr Pharm Biotechno 2008, 9:253-260.
4. Luo Y., Prestwich G.D. Synthesis and selective cytotoxicity of a hyaluronic acid-antitumor bioconjugate. Bioconjug Chem 1999, 10:755-763.
5. Campoccia D., Doherty P., Radice M., Brun P., Abatangelo G., Williams D.F. Semisynthetic resorbable materials from hyaluronan esterification. Biomaterials 1998, 19:2101-2127.
6. Park Y.D., Tirelli N., Hubbell J.A. Photopolymerized hyaluronic acid-based hydrogels and interpenetrating networks. Biomaterials 2003, 24:893-900.
7. Lee H., Mok H., Lee S., Oh Y.K., Park T.G. Target-specific intracellular delivery of siRNA using degradable hyaluronic acid nanogels. J Control Release 2007, 119:245-252.
8. Nasti A., Zaki N.M., de Leonardis P., Ungphaiboon S., Sansongsak P., Rimoli M.G., et al. Chitosan/tpp and chitosan/tpp-hyaluronic acid nanoparticles: systematic optimisation of the preparative process and preliminary biological evaluation. Pharm Res 2009, 26:1918-1930.
9. Lee J.Y., Spicer A.P. Hyaluronan: a multifunctional, megadalton, stealth molecule. Curr Opin Cell Biol 2000, 12:581-586.
10. Taglienti A., Cellesi F., Crescenzi V., Sequi P., Valentini M., Tirelli N. Investigating the interactions of hyaluronan derivatives with biomolecules. The use of diffusional nmr techniques. Macromol Biosci 2006, 6:611-622.
11. Day A.J., Prestwich G.D. Hyaluronan-binding proteins: tying up the giant. J Biol Chem 2002, 277:4585-4588.
12. Harris E.N., Kyosseva S.V., Weigel J.A., Weigel P.H. Expression, processing, and glycosaminoglycan binding activity of the recombinant human 315 kDa hyaluronic acid receptor for endocytosis (HARE). J Biol Chem 2007, 282:2785-2797.
13. Harris E.N., Weigel J.A., Weigel P.H. Endocytic function, glycosaminoglycan specificity, and antibody sensitivity of the recombinant human 190 kDa hyaluronan receptor for endocytosis (HARE). J Biol Chem 2004, 279:36201-36209.
14. Mochizuki S., Kano A., Shimada N., Maruyama A. Uptake of enzymatically-digested hyaluronan by liver endothelial cells in vivo and in vitro. J Biomat Sci-Polym E 2009, 20:83-97.
15. Prevo R., Banerji S., Ferguson D.J.P., Clasper S., Jackson D.G. Mouse LYVE-1 is an endocytic receptor for hyaluronan in lymphatic endothelium. J Biol Chem 2001, 276:19420-19430.
16. Arimoto J., Ikura Y., Suekane T., Nakagawa M., Kitabayashi C., Iwasa Y., et al. Expression of LYVE-1 in sinusoidal endothelium is reduced in chronically inflamed human livers. J Gastroenterol 2010, 45:317-325.
17. Gordon E.J., Gale N.W., Harvey N.L. Expression of the hyaluronan receptor LYVE-1 is not restricted to the lymphatic vasculature; lyve-1 is also expressed on embryonic blood vessels. Dev Dynam 2008, 237:1901-1909.
18. Johnson L.A., Prevo R., Clasper S., Jackson D.G. Inflammation-induced uptake and degradation of the lymphatic endothelial hyaluronan receptor LYVE-1. J Biol Chem 2007, 282.
19. Milner C.M., Day A.J. TSG-6: a multifunctional protein associated with inflammation. J Cell Sci 2003, 116:1863-1873.
20. Baranova N.S., Nilebäck E., Briggs D.C., Michael Haller F., Svedhem S., Day A.J., et al. The inflammation-associated protein TSG-6 cross-links hyaluronan via hyaluronan-induced TSG-6 oligomers. J Biol Chem 2011, 286:25675-25686.
21. Lesley J., Gál I., Mahoney D.J., Cordell M.R., Rugg M.S., Hyman R., et al. TSG-6 modulates the interaction between hyaluronan and cell surface cd44. J Biol Chem 2004, 279:25745-25754.
22. Turley E.A. Purification of a hyaluronate-binding protein-fraction that modifies cell social behaviour. Biochem Bioph Res Co 1982, 108:1016-1024.
23. Giannopoulos K., Schmitt M. Targets and strategies for T-cell based vaccines in patients with b-cell chronic lymphocytic leukemia. Leuk Lymphoma 2006, 47:2028-2036.
24. Tolg C., Hamilton S.R., Nakrieko K.A., Kooshesh F., Walton P., McCarthy J.B., et al. Rhamm(-/-) fibroblasts are defective in CD44-mediated ERK1,2 motogenic signaling, leading to defective skin wound repair. J Cell Biol 2006, 175:1017-1028.
25. Yang B.H., Yang B.L., Savani R.C., Turley E.A. Identification of a common hyaluronan-binding motif in the hyaluronan-binding proteins rhamm, Cd44 and Link protein. Embo J 1994, 13:286-296.
26. Gares S.L., Pilarski L.M. Beta(1)-integrins control spontaneous adhesion and motility of human progenitor thymocytes and regulate differentiation-dependent expression of the receptor for hyaluronan-mediated motility. Scand J Immunol 1999, 50:626-634.
27. Maxwell C.A., McCarthy J., Turley E. Cell-surface and mitotic-spindle rhamm: moonlighting or dual oncogenic functions?. J Cell Sci 2008, 121:925-932.
28. Witkin S.S., Babayan A., Neuer A., Dieterle S., Bongiovanni A.M. Hyaluronan in follicular fluid and embryo implantation following in vitro fertilization and embryo transfer. J Assist Reprod Gen 2008, 25:473-476.
29. Travis J.A., Hughes M.G., Wong J.M., Wagner W.D., Geary R.L. Hyaluronan enhances contraction of collagen by smooth muscle cells and adventitial fibroblasts - role of CD44 and implications for constrictive remodeling. Circ Res 2001, 88:77-83.
30. Day A.J., de la Motte C.A. Hyaluronan cross-linking: a protective mechanism in inflammation?. Trends Immunol 2005, 26:637-643.
31. McDonald B., McAvoy E.F., Lam F., Gill V., de la Motte C., Savani R.C., et al. Interaction of CD44 and hyaluronan is the dominant mechanism for neutrophil sequestration in inflamed liver sinusoids. J Exp Med 2008, 205:915-927.
32. Kaya G., Rodriguez I., Jorcano J.L., Vassalli P., Stamenkovic I. Selective suppression of CD44 in keratinocytes of mice bearing an antisense cd44 transgene driven by a tissue-specific promoter disrupts hyaluronate metabolism in the skin and impairs keratinocyte proliferation. Gene Dev 1997, 11:996-1007.
33. Kaya G., Augsburger E., Stamenkovic I., Saurat J.H. Decrease in epidermal CD44 expression as a potential mechanism for abnormal hyaluronate accumulation in superficial dermis in lichen sclerosus et atrophicus. J Invest Dermatol 2000, 115:1054-1058.
34. Faassen A.E., Schrager J.A., Klein D.J., Oegema T.R., Couchman J.R., Mccarthy J.B. A cell-surface chondroitin sulfate proteoglycan, immunologically related to Cd44, is involved in type-1 collagen-mediated melanoma cell motility and invasion. J Cell Biol 1992, 116:521-531.
35. Faassen A.E., Mooradian D.L., Tranquillo R.T., Dickinson R.B., Letourneau P.C., Oegema T.R., et al. Cell-surface Cd44-related chondroitin sulfate proteoglycan is required for transforming growth factor-beta-stimulated mouse melanoma cell motility and invasive behavior on type-i1collagen. J Cell Sci 1993, 105:501-511.
36. Ishii S., Ford R., Thomas P., Nachman A., Steele G., Jessup J.M. Cd44 participates in the adhesion of human colorectal-carcinoma cells to laminin and type-iv collagen. Surg Oncol 1993, 2:255-264.
37. Jalkanen S., Jalkanen M. Lymphocyte Cd44 binds the COOH-terminal heparin-binding domain of fibronectin. J Cell Biol 1992, 116:817-825.
38. Clark R.A.F., Lin F.B., Greiling D., An J.Q., Couchman J.R. Fibroblast invasive migration into fibronectin/fibrin gels requires a previously uncharacterized dermatan sulfate-CD44 proteoglycan. J Invest Dermatol 2004, 122:266-277.
39. Naujokas M.F., Morin M., Anderson M.S., Peterson M., Miller J. The chondroitin sulfate form of invariant chain can enhance stimulation of t-cell responses through interaction with Cd44. Cell 1993, 74:257-268.
40. Greenfield B., Wang W.C., Marquardt H., Piepkorn M., Wolff E.A., Aruffo A., et al. Characterization of the heparan sulfate and chondroitin sulfate assembly sites in CD44. J Biol Chem 1999, 274:2511-2517.
41. Suzuki K., Zhu B., Rittling S.R., Denhardt D.T., Pilkington M.F., Dixon S.J., et al. Association of intracellular osteopontin with the CD44 receptor complex in osteoclasts. J Bone Miner Res 2000, 15:S219.
42. Katoh S., Zheng Z., Oritani K., Shimozato T., Kincade P.W. Glycosylation of CD44 negatively regulates its recognition of hyaluronan. J Exp Med 1995, 182:419-429.
43. DeGrendele H.C., Estess P., Siegelman M.H. Requirement for CD44 in activated T cell extravasation into an inflammatory site. Science 1997, 278:672-675.
44. Esford L.E., Maiti A., Badar S.A., Tufaro F., Johnson P. Analysis of CD44 interactions with hyaluronan in murine L cell fibroblasts deficient in glycosaminoglycan synthesis: a role for chondroitin sulfate. J Cell Sci 1998, 111:1021-1029.
45. 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.
46. Cichy J., Pure E. Oncostatin M and transforming growth factor-Beta 1 induce post-translational modification and hyaluronan binding to CD44 in lung-derived epithelial tumor cells. J Biol Chem 2000, 275:18061-18069.
47. Culty M., Omara T.E., Underhill C.B., Yeager H., Swartz R.P. Hyaluronan receptor (Cd44) expression and function in human peripheral-blood monocytes and alveolar macrophages. J Leukoc Biol 1994, 56:605-611.
48. Liu D.C., Zhang D.X., Mori H., Sy M.S. Binding of CD44 to hyaluronic acid can be induced by multiple signals and requires the CD44 cytoplasmic domain. Cell Immunol 1996, 174:73-83.
49. Liu D.C., Liu T., Sy M.S. 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 1998, 190:132-140.
50. Jiang H., Peterson R.S., Wang W.H., Bartnik E., Knudson C.B., Knudson W. A requirement for the CD44 cytoplasmic domain for hyaluronan binding, pericellular matrix assembly, and receptor-mediated endocytosis in cos-7 cells. J Biol Chem 2002, 277:10531-10538.
51. Knudson W., Chow G., Knudson C.B. CD44-mediated uptake and degradation of hyaluronan. Matrix Biol 2002, 21:15-23.
52. Tammi R., Rilla K., Pienimaki J.P., MacCallum D.K., Hogg M., Luukkonen M., et al. Hyaluronan enters keratinocytes by a novel endocytic route catabolism. J Biol Chem 2001, 276:35111-35122.
53. Thankamony S.P., Knudson W. Acylation of CD44 and its association with lipid rafts are required for receptor and hyaluronan endocytosis. J Biol Chem 2006, 281:34601-34609.
54. Lee J.L., Wang M.J., Sudhir P.R., Chen J.Y. CD44 engagement promotes matrix-derived survival through the CD44-Src-integrin axis in lipid rafts. Mol Cell Biol 2008, 28:5710-5723.
55. Lokeshwar V.B., Fregien N., Bourguignon L.Y.W. Ankyrin-binding domain of Cd44(Gp85) is required for the expression of hyaluronic acid-mediated adhesion function. J Cell Biol 1994, 126:1099-1109.
56. Lee J.L., Wang M.J., Sudhir P.R., Chen G.D., Chi C.W., Chen J.Y. Osteopontin promotes integrin activation through outside-in and inside-out mechanisms: OPN-CD44(v) interaction enhances survival in gastrointestinal cancer cells. Cancer Res 2007, 67:2089-2097.
57. Lundell B.I., McCarthy J.B., Kovach N.L., Verfaillie C.M. Activation of beta 1 integrins on CML progenitors reveals cooperation between beta 1 integrins and CD44 in the regulation of adhesion and proliferation. Leukemia 1997, 11:822-829.
58. Nandi A., Estess P., Siegelman M. Bimolecular complex between rolling and firm adhesion receptors required for cell arrest: CD44 association with VLA-4 in t cell extravasation. Immunity 2004, 20:455-465.
59. Misra S., Heldin P., Hascall V.C., Karamanos N.K., Skandalis S.S., Markwald R.R., et al. Hyaluronan-CD44 interactions as potential targets for cancer therapy. Febs J 2011, 278:1429-1443.
60. Aguiar D.J., Knudson W., Knudson C.B. Internalization of the hyaluronan receptor cd44 by chondrocytes. Exp Cell Res 1999, 252:292-302.
61. Caswell P.T., Vadrevu S., Norman J.C. Integrins: masters and slaves of endocytic transport. Nat Rev Mol Cell Bio 2009, 10:843-853.
62. Takada Y., Ye X.J., Simon S. The integrins. Genome Biol 2007, 8. Art. No 15.
63. Lutolf M.P., Raeber G.P., Zisch A.H., Tirelli N., Hubbell J.A. Cell-responsive synthetic hydrogels. Adv Mater 2003, 15:888-892.
64. Massia S.P., Hubbell J.A. An RGD spacing of 440 nm is sufficient for integrin alpha-v-beta-3-mediated fibroblast spreading and 140 nm for focal contact and stress fiber formation. J Cell Biol 1991, 114:1089-1100.
65. Kuo J.W., Swann D.A., Prestwich G.D. Chemical modification of hyaluronic-acid by carbodiimides. Bioconjug Chem 1991, 2:232-241.
66. Tomihata K., Ikada Y. Crosslinking of hyaluronic acid with water-soluble carbodiimide. J Biomed Mater Res 1997, 37:243-251.
67. Debelder A.N., Wik K.O. Preparation and properties of fluorescein-labeled hyaluronate. Carbohyd Res 1975, 44:251-257.
68. Vretblad P., Axen R. Preparation and properties of an immobilized barley beta-amylase. Biotechnol Bioeng 1973, 15:783-794.
69. Choi E.T., Engel L., Callow A.D., Sun S.P., Trachtenberg J., Santoro S., et al. Inhibition of neointimal hyperplasia by blocking alpha(v)beta(3), integrin with a small peptide antagonist gpengrgdspca. J Vasc Surg 1994, 19:125-134.
70. Crow A.R., Song S., Suppa S.J., Ma S.H., Reilly M.P., Andre P., et al. Amelioration of murine immune thrombocytopenia by CD44 antibodies: a potential therapy for ITP?. Blood 2011, 117:971-974.
71. Zaki N.M., Tirelli N. Gateways for the intracellular access of nanocarriers: a review of receptor-mediated endocytosis mechanisms and of strategies in receptor targeting. Expert Opin Drug Del 2010, 7:895-913.
72. Culty M., Nguyen H.A., Underhill C.B. The hyaluronan receptor (Cd44) participates in the uptake and degradation of hyaluronan. J Cell Biol 1992, 116:1055-1062.
73. Mcguire P.G., Castellot J.J., Orkin R.W. Size-dependent hyaluronate degradation by cultured-cells. J Cell Physiol 1987, 133:267-276.
74. Zaki N.M., Nasti A., Tirelli N. Nano-carriers for cytoplasmic delivery: cellular uptake and intracellular fate of chitosan and hyaluronic acid-coated chitosan nanoparticles in a phagocytic cell model. Macromol Biosci 2011, 11. 10.1002/mabi.201100156.
75. Wolny P.M., Banerji S., Gounon C., Brisson A.R., Day A.J., Jackson D.G., et al. 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 2010, 285:30170-30180.
76. Harada H., Takahashi M. CD44-dependent intracellular and extracellular catabolism of hyaluronic acid by hyaluronidase-1 and-2. J Biol Chem 2007, 282:5597-5607.
77. Bourguignon L.Y.W., Singleton P.A., Diedrich F., Stern R., Gilad E. CD44 interaction with Na+-H+ exchanger (NHE1) creates acidic microenvironments leading to hyaluronidase-2 and cathepsin B activation and breast tumor cell invasion. J Biol Chem 2004, 279:26991-27007.
78. Jones M.C., Caswell P.T., Norman J.C. Endocytic recycling pathways: emerging regulators of cell migration. Curr Opin Cell Biol 2006, 18:549-557.
79. Roberts M., Barry S., Woods A., van der Sluijs P., Norman J. PDGF-regulated rab4-dependent recycling of alphavbeta3 integrin from early endosomes is necessary for cell adhesion and spreading. Curr Biol 2001, 11:1392-1402.
80. Woods A.J., White D.P., Caswell P.T., Norman J.C. PKD1/PKC mu promotes alpha v beta 3 integrin recycling and delivery to nascent focal adhesions. Embo J 2004, 23:2531-2543.
81. Reynolds A.R., Hart I.R., Watson A.R., Welti J.C., Silva R.G., Robinson S.D., et al. Stimulation of tumor growth and angiogenesis by low concentrations of RGD-mimetic integrin inhibitors. Nat Med 2009, 15:392-400.
82. Contreras-Ruiz L., de la Fuente M., Parraga J.E., Lopez-Garcia A., Fernandez I., Seijo B., et al. Intracellular trafficking of hyaluronic acid-chitosan oligomer-based nanoparticles in cultured human ocular surface cells. Mol Vis 2011, 17:279-290.
83. Vidricaire G., Tremblay M.J. A clathrin, caveolae, and dynamin-independent endocytic pathway requiring free membrane cholesterol drives HIV-1 internalization and infection in polarized trophoblastic cells. J Mol Biol 2007, 368:1267-1283.