Cytokines and glycosaminoglycans (GAGs)

Advances in Experimental Medicine and Biology

Volumn 535, Issue , 2002, Pages 125-143

  Gibbs, Roslyn V ^a  

^a UNIVERSITY OF PORTSMOUTH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE BINDING PROTEIN; CHEMOKINE; CHONDROITIN; CHONDROITIN SULFATE; COLONY STIMULATING FACTOR; CYTOKINE; DERMATAN SULFATE; DISACCHARIDE; GAMMA INTERFERON; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; HEPARIN; HYALURONIC ACID; INTERFERON; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR; INTERLEUKIN 7; INTERLEUKIN 8; KERATAN SULFATE; N ACETYLGALACTOSAMINE 4 SULFATASE; OLIGOSACCHARIDE; POLYMER; PROTEOGLYCAN; PROTEOHEPARAN SULFATE; TUMOR NECROSIS FACTOR;

ANALYTIC METHOD; ANTIBODY PRODUCTION; ANTIGEN PRESENTING CELL; ANTIMICROBIAL ACTIVITY; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; BINDING SITE; CARBOHYDRATE ANALYSIS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CHEMICAL COMPOSITION; CHEMOTAXIS; CONFERENCE PAPER; CONNECTIVE TISSUE; CORNEA; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ELECTROPHORESIS; EMBRYONAL TISSUE; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX; IMMUNE RESPONSE; IMMUNOREGULATION; IMMUNOSTIMULATION; INFLAMMATION; LEUKOCYTE ADHERENCE; LYMPHOCYTE PROLIFERATION; MACROPHAGE; MAST CELL; NATURAL KILLER CELL; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SURFACE PLASMON RESONANCE; T LYMPHOCYTE ACTIVATION; THYMOCYTE; TISSUE DISTRIBUTION;

ANIMALS; CYTOKINES; GLYCOSAMINOGLYCANS; HUMANS; INTERFERON TYPE II; INTERLEUKINS; PROTEIN BINDING;

EID: 1642481194     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: None     Document Type: Conference Paper

References (101)

1. Appasamy, P., 1999, Biological and clinical implications of interleukin-7 and lymphopoiesis, Cytokines Cell Mol Ther. 5:25-39.
2. Baldwin, E.T., Weber, I.T., St. Charles, R., Xuan, J.-C., Appella, E., Yamada, M., Matsushima, K., Edwards, B.F.P., Clore, G.M., Gronenborn, A.M., and Wlodawer, A., 1991, Crystal structure of interleukin 8: symbiosis of NMR and crystallography, Proc Natl Acad Sci. 88:502-506.
3. Bazan, F.J. and McKay, D.B., 1992, Unraveling the structure of IL-2, Science. 257:410-412.
4. Billips, L.G., Petitte, D., Dorshkind, K., Narayanan, R., Chiu, C., and Landreth, K.S., 1992, Differential roles of stromal cells, interleukin-7 and kit-ligand in the regulation of B lymphopoiesis, Blood. 79:1185-1192.
5. Borghesi, L.A., Yamashita, Y., and Kincade, P.W., 1999, Heparan sulfate proteoglycans mediate interleukin-7-dependent B lymphopoiesis, Blood. 93:140-148.
6. Cardin, A.D. and Weintraub, H.J.R., 1989, Molecular modeling of protein-glycosaminoglycan interactions, Arteriosclerosis. 9:21-32.
7. Casu, B., 1985, Structure and biological activity of heparin, Adv Carbohydr Chem Biochem. 43:51-135.
8. Chazen, G.D., Pereira, G.M.B., LeGros, G., Gillis, S., and Shevach, E.M., 1989, Interleukin-7 is a T cell growth factor, Proc Natl Acad Sci. 86:5923-5927.
9. Clarke, D., Katoh, O., Gibbs, R.V., Griffiths, S.D., and Gordon, M.Y., 1995, Interaction of interleukin 7 (IL-7) with glycosaminoglycans and its biological relevance, Cytokine. 7:325-330.
10. Cosenza, L.L., Sweeney, E.E., and Murphy, J.R., 1997, Disulphide bond assignment in human interleukin-7 by matrix assisted laser desorption/ ionization mass spectroscopy and site-directed cysteine to serine mutational analysis, J Biol Chem. 272:32995-33000.
11. Costello, R., Imbert, J., and Olive, D., 1993, Interleukin-7, a major T-lymphocyte cytokine, Eur Cytokine Netw. 4:253-262.
12. Coutino, A., Lotta, E., Larsson, E., Gronvik, K., and Andersson, J., 1979, Studies on T cell activation II. The targets for concanavalin A-induced growth factors, Eur J Immunol. 9:587-592.
13. Daubener, W., Nockemann, S., Gutsche, M., and Hadding, U., 1995, Heparin inhibits the antiparasitic and immune modulatory effects of human recombinant Interferon-γ, Eur J Immunol. 25:688-692.
14. Dumont, F.J., Palfree, R.G.E., and Fisher, P.A., 1988, The T-cell activating protein (TAP) is up-regulated by endogenous IFN-γ in activated T cells, Immunol. 64:267-271.
15. Ealick, S.E., Cook, W.J., Vijay-Kumar, S., Carson, M., Nagabhushan, T.L., Trotta, P.P., and Bugg, C.E., 1991, Three-dimensional structure of recombinant human interferon-γ, Science. 252:698-702.
16. Farrar, J.J., Benjamin, W.R., Hilfiker, M.L., Howard, M., Farrar, W.L., and Farrar-Fuller, J., 1982, The biochemistry, biology and role of interleukin 2 in the induction of cytotoxic T cell and antibody-forming B cell responses, Immunol Rev. 63:129-166.
17. Fernandez-Botran, R., Yan, J., and Justus, D.E., 1999, Binding of interferon γ by glycosaminoglycans: a strategy for localization and/or inhibition of its activity, Cytokine. 11:313-325.
18. Fritchley, S.J., Kirby, J.A., and Ali, S., 2000, The antagonism of interferon-gamma (IFN-γ) by heparin: examination of the blockade of class II MHC antigen and heat shock protein-70 expression, Clin Exp Immunol. 120:247-252.
19. Fromm, J.R., Hileman, R.E., Caldwell, E.E.O., Weiler, J.M., and Linhardt, R.J., 1997, Pattern and spacing of basic amino acids in heparin binding sites, Arch Biochem Biophys. 343:92-100.
20. Frucht, D.M., Fukao, T., Bogdan, C., Schindler, H., O'Shea, J.J., and Koyasu, S., 2001, IFN-γ production by antigen presenting cells: mechanisms emerge, Trends Immunol. 22:556-560.
21. Funderburgh, J.L., 2000, Keratan sulphate: structure, biosynthesis and function, Glycobiology. 10:951-958.
22. Gallagher, J.F., Lyon, M., and Steward, W.P., 1986, Structure and function of heparan sulphate proteoglycans, Biochem J. 236:313-325.
23. Garnier, P., Gibbs, R.V., and Rider, C.C., 2003, A role for chondroitin sulphate B in the activation of IL-12 in stimulating γ-IFN secretion, Immunol Lett. 85:53-58.
24. Giacomini, P., Tecce, R., Gambari, R., Sacchi, A., Fisher, P.B., and Natali, .PG., 1988, Recombinant human IFN-γ, but not IFN-α or IFN-β, enhances MHC-and non-MHC-encoded glycoproteins by a protein-synthesis-dependent mechanism, J Immunol. 140:3073-3081.
25. Gibbs, R.V. and Gordon, M.Y., 1996, Binding of growth factors to extracellular matrix proteins and glycoproteins, in: Cell and tissue culture: laboratory procedures. Ch 8E 1.I-1.19. eds. J.B. Griffiths, A. Doyle, D.G. Newell, John Wiley and Sons Ltd, W. Sussex, UK.
26. Giovarelli, M., Santoni, A., Jemma, C., Musso, T., Giuffrida, A., Cavallo, G., Landolfo, S., and Forni, G., 1988, Obligatory role of IFN-γ in induction of lymphokine-activated and T lymphocyte killer cell activity, but not in boosting of natural cytotoxicity, J Immunol. 141:2831-2836.
27. Goger, B., Halden, Y., Rek, A., Mosi, R., Pye, D., Gallagher, J., and Kungl, A.J., 2002, Different affinities of glycosaminoglycan oligosaccharides for monomeric and dimeric interleukin-8: a model for chemokine regulation at inflammatory sites, Biochemistry. 41:1640-1646.
28. Gordon, M.Y., Riley, G.P., Watt, S.M., and Greaves, M.F., 1987, Compartmentalization of a growth factor (GM-CSF) by glycosaminoglycans in the bone marrow microenvironment, Nature. 326:403-405.
29. Grimm, E.A., Robb, R.J., Roth, L.M., Neckers, L.M., Lachman, L.B., Wilson, D.J., and Rosenburg, S.A., 1983, Lymphokine-activated killer cell phenomenon. III. Evidence that IL-2 is sufficient for direct activation of peripheral blood lymphocytes, J Exp Med. 158:1356-1361.
30. Guelle, M., Nika, K., Mernagh, D., Mulloy, B., Forster M., and Gibbs, R., 2000, Characterisation of interleukin-7 (IL-7)-glycosaminoglycan interactions, Minerva Biotecnologica. 12:121-122.
31. Hasan, M., Najjam, S., Gordon, M.Y., Gibbs, R.V., and Rider, C.C., 1999, IL-12 is a heparin-binding cytokine, J Immunol. 162:1064-1070.
32. Hascall, V.C., Calabro, A., Midura, R.J., and Yanagishita, M., 1994, Isolation and characterization of proteoglycans, Methods Enzymol. 230:390-417.
33. He, Y.W. and Malek, T.R., 1998, The structure and function of γc-dependent cytokines and receptors: regulation of T lymphocyte development and homeostasis, Crit Rev Immunol. 18:503-524.
34. Hileman, R.E., Fromm, J.R., Weiler, J.M., and Linhardt, R.J., 1998, Glycosaminoglycan-protein interactions: definition of consensus sites in glycosaminoglycan binding proteins, BioEssays. 20:156-167.
35. Heney, C.S., Kuribayashi, K., Kern, D.E., and Gillis, S., 1981, Interleukin-2 augments natural killer cell activity, Nature. 291:335-338.
36. Hoogewerf, A.J., Kuschert, G.S.V., Proudfoot, A.E.I., Borlat, F., Clark-Lewis, I., Power, C.A., and Wells, T.N.C., 1997, Glycosaminoglycans mediate cell surface oligomerization of chemokines, Biochemistry. 36:13570-13578.
37. Kjellen, L. and Lindahl, U., 1991, Proteoglycans: structures and interactions. Annu Rev Biochem. 60:443-475.
38. Kolset, S.O. and Gallagher, J.F., 1990, Proteoglycans in haemopoietic cells, Biochim Biophys Acta. 1032:191-211.
39. Kroemer, R.T., Doughty, S.W., Robinson, A.J., and Richards, W.G., 1996, Prediction of the three-dimensional structure of human interleukin-7 by homology modeling, Prot Engin. 9:493-498.
40. Kuschert, G.S.V., Hoogewerf, A.J., Proudfoot, A.E.I., Chung, C.-W., Coooke, R.M., Hubbard, R.E., Wells, T.N.C., and Sanderson, P.N., 1998, Identification of a glycosaminoglycan binding surface on human interleukin-8, Biochemistry. 37:11193-11201.
41. Laurent, T.C. and Fraser, J.R., 1992, Hyaluronan, FASEB J. 6:2397-2404.
42. Scott, J.E., 1993, The nomenclature of glycosaminoglycans and proteoglycans, Glycoconj J. 10:419-421.
43. Lee, K.K. and Lander, A.D., 1991, Analysis of affinity and structural selectivity in the binding of proteins to glycosaminoglycans: development of a sensitive electrophoretic approach, Proc Natl Acad Sci USA. 88:2768-2772.
44. Lindahl, U., Thunberg, L.L., Backstrom, G., Riesenfeld, J., Nordling, K., and Bjork, I., 1984, Extension and structural variability of the antithrombin-binding sequence in heparin, J Biol Chem. 259:12368-12376.
45. Lipscombe, R.J., Nalchoul, A.M., Sanderson, C.J., and Coombe, D.R., 1998, Interleukin-5 binds to heparin/heparan sulfate. A model for an interaction with extracellular matrix, J Leukoc Biol. 63:342-350.
46. Lortat-Jacob, H., Baltzer, F., and Grimaud, J.-A., 1996a, Heparin decreases the blood clearance of Interferon-γ and increases its activity by limiting the processing of its carboxyl-terminal sequence, J Biol Chem. 271:16139-16143.
47. Lortat-Jacob, H., Brisson, C., Guerret, S., and Morel, G., 1996b, Non-receptor-mediated tissue localization of human interferon-γ: role of heparan sulphate/heparin-like molecules, Cytokine. 8:557-566.
48. Lortat-Jacob, H., Garrone, P., Banchereau, J., and Grimaud, J.-A., 1997, Human interleukin 4 is a glycosaminoglycan-binding protein, Cytokine. 9:101-105.
49. Lortat-Jacob, H. and Grimaud, J.-A., 1991, Interferon-γ binds to heparan sulfate by a cluster of amino acids located in the C-terminal part of the molecule, FEBS Letts. 280:152-154.
50. Lortat-Jacob, H., Kleinman, H.K., and Grimaud, J.-A., 1991, High-affinity binding of interferon-γ to a basement membrane complex (matrigel), J Clin Invest. 87:878-883.
51. Lortat-Jacob, H., Turnbull, J.E., and Grimaud, J.-A., 1995, Molecular organisation of the interferon γ-binding domain in heparan sulphate, Biochem J. 310:497-505.
52. Lustig, F., Hoebeke, J., Olsson, U., and Fager, G.G., 1996, Alternative splicing determines the binding of platelet-derived growth factor to glycosaminoglycans, Biochemistry. 35:12077-12085.
53. Lynch, D.H. and Miller, R.E., 1992, Induction of murine lymphokine-activated killer cells by recombinant IL-7, J Immunol. 145:1983-1990.
54. Mach, H., Volkin, D.B., Burke, C.J., and Middaugh, R.C., 1993, Nature of the interaction of heparin with acidic fibroblast growth factor, Biochemistry. 32:5480-5489.
55. Maimone, M.M. and Tollefsen, D.M., 1990, Structure of a dermatan sulfate hexasaccharide that binds to heparin cofactor II with high affinity, J Biol Chem. 265:18263-18271.
56. Martin, L., Blanpain, C., Garnier, P., Wittamer, V., Parmentier, M., and Vita, C., 2001, Structural and functional analysis of the RANTES- glycosaminoglycans interactions, Biochemistry. 40:6303-6318.
57. McFadden, G. and Kelvin, D., 1997, New strategies for chemokine inhibition and modulation, Biochem Pharmacol. 54:1271-1280.
58. McKay, D.B., 1992, Unraveling the structure of IL-2 Response, Science. 257:412-413.
59. Meager, T., 1998, The Molecular Biology of Cytokines. John Wiley & Sons, West Sussex, UK.
60. Meuer, S.C., Hussey, R.E., Cantrell, D.A., Hodgon, J.C., Schlossman, S.F., Smith, K.A., and Reinherz, E.L., 1984, Triggering of the T3-Ti antigen-receptor complex results in clonal T-cell proliferation through an interleukin-2-dependent autocrine pathway, Proc Natl Acad Sci. 81:1509-1513.
61. Mummery, R.S. and Rider C.C., 2000, Characterization of the heparin-binding properties of IL-6, J Immunol. 165:5671-5679.
62. Najjam, S., Gibbs R.V., Gordon, M.Y., and Rider, C.C., 1997, Characterization of human recombinant interleukin 2 binding to heparin and heparan sulfate using an ELISA approach, Cytokine. 9:1013-1022.
63. Najjam, S., Mulloy, B., Theze, J., Gordon, M., Gibbs, R., and Rider, C.C., 1998, Further characterization of the binding of human recombinant interleukin 2 to heparin and identification of putative binding sites, Glycobiology. 8:509-516.
64. + natural killer cells, J Immunol. 147:2208-2214.
65. Nice, E.G. and Catimel, B., 1999, Instrumental biosensors: new perspectives for the analysis of biomolecular interactions, BioEssays. 21:339-352.
66. Otsu, K., Inoue, H., Tsuzuki, Y., Yonekura, H., Nakanishi, Y., and Suzuki, S., 1985, A distinct terminal structure in newly synthesised chondroitin sulphate chains, Biochem J. 227:37-48.
67. Pace, J.L., Russell, S.W., Torres, B.A., Johnson, H.M., and Gray, P.W., 1983, Recombinant mouse γ interferon induces the priming step in macrophage activation for tumour cell killing, J Immunol. 130:2011-2013.
68. Petroni, K.C., Shen, L., and Guyer, P.M., 1988, Modulation of human polymorphonuclear leucocyte IgG Fc receptors and Fc receptor-mediated functions by IFN-γ and glucocorticoids, J Immunol. 140:3467-3472.
69. Ramsden, L. and Rider, C.C., 1992, Selective and differential binding of interleukin-1α, interleukin-2 and interleukin-6 to glycosaminoglycans, Eur J Immunol. 22:3027-3031.
70. Rich, R.L. and Myszka, D.G., 2000, Advances in surface plasmon resonance biosensor analysis, Curr Opin Biotech. 11:54-61.
71. Rider, C.C., Coombe, D.R., Harrop, H.A., Hounsel, E.F., Bauer, C., Feeney, J., Mulloy, B., Mahmood, N., Hay, A., and Parish, C.R., 1994, Anti-HIV-1 activity of chemically modified heparins: correlation between binding to the V3 loop of gp120 and inhibition of cellular HIV-1 infection in vitro, Biochemistry. 33:6974-6980.
72. Rinderknecht, E., O'Connor, B.H., and Rodriguez, H., 1984, Natural human interferon-γ, J Biol Chem. 259:6790-6797.
73. Robb, R.J. and Smith, C., 1981, Heterogeneity of human T-cell growth factor(s) due to variable glycosylation, Mol Immunol. 18:1087-1094.
74. Roberts, R., Gallagher, J., Spooncer, E., Allen, T.D., Bloomfield, F., and Dexter, T.M., 1988, Heparan sulphate bound growth factors: a mechanism for stromal cell mediated haemopoiesis, Nature. 332:376-378.
75. Rot, A., 1992, Endothelial cell binding of NAP-1/IL-8: role in neutrophil emigration, Immunol Today. 13:291-294.
76. Rot, A., Hub, E., Middleton, J., Pons, F., Rabeck, C., Thierer, K., Wintle, J., Wolff, B., Zsak, M., and Dukor, P., 1996, Some aspects of IL-8 pathophysiology III: chemokine interaction with endothelial cells, J Leukoc Biol. 59:39-44.
77. Sadir, R., Forest, E., and Lortat-Jacob, H., 1998, The heparan sulfate binding sequence of interferon-γ increased the on rate of the interferon-γ-interferon-γ receptor complex formation, J Biol Chem. 273:10919-10925.
78. Salaman, Z., Macleod, A.H., and Tollin, G., 1997, Surface plasmon resonance spectroscopy as a tool for investigating the biochemical and biophysical properties of membrane protein systems. I: Theoretical principles, Biochim Biophys Acta. 1331:117-129.
79. Salek-Ardakani, S., Arrand, J.R., Shaw, D., and Mackett, M., 2000, Heparin and heparan sulphate bind IL-10 and modulate its activity, Blood. 96:1879-1888.
80. San Antonio, J.D., Slover, J., Lawler, J., Karnovsky, M.J., and Lander, A.D., 1993, Specificity in the interactions of extracellular matrix proteins with subpopulations of the glycosaminoglycan heparin, Biochemistry. 32:4746-4755.
81. Scott, J.E., 1993, The nomenclature of glycosaminoglycans and proteoglycans, Glycoconj J. 10:419-421.
82. Solid, L.M., Kvale, D., Brrandtzaeg, P., Markussen, G., and Thorsby, E., 1987, Interferon-γ enhances expression of secretory component, the epithelial receptor for polymeric immunoglobulins, J Immunol. 138:4303-4306.
83. Spillmann, D. and Lindahl, U., 1994, Glycosaminoglycan-protein interactions: a question of specificity, Curr Opin Struc Biol. 4:677-682.
84. Spillmann, D., Witt, D., and Lindahl, U., 1998, Defining the interleukin-8-binding domain of heparan sulfate, J Biol Chem. 273:15487-15493.
85. Stearns, N.A., Prigent-Richard, S., Letourneur, D., and Castellot, J.J., 1997, Synthesis and characterisation of highly sensitive heparin probes for detection of heparin-binding proteins, Anal Biochem. 247:348-356.
86. Tanaka, Y., Adams, D.H., and Shaw, S., 1993, Proteoglycans on endothelial cells present adhesion-inducing cytokines to leucocytes, Immunol Today. 14:111-115.
87. Toida, T., Yoshida, H., Toyoda, H., Koshiishi, I., Imanari, T., Hileman, R.E., Fromm, J.R., and Lindardt, R.J., 1997, Structural differences and the presence of unsubstituted amino groups in heparan sulphates from different tissues and species, Biochem J. 332:499-506.
88. Trinchieri, G., 1995, Interleukin-12: a proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-specific adaptive immunity, Annu Rev Immunol. 13:251-276.
89. Trinchieri, G. and Perussia, B., 1985, Immune interferon: a pleiotropic lymphokine with multiple effects, Immunol Today. 6:131-136.
90. Turnbull, J.E. and Gallagher, J.T., 1990a, Distribution of iduronate 2-sulphate residues in heparan sulphate, Biochem J. 273:553-559.
91. Turnbull, J.E. and Gallagher, J.T., 1990b, Molecular organisation of heparan sulphate from human skin fibroblasts, Biochem J. 265:715-724.
92. Vives, R.R., Pye, D.A., Salmivirta, M., Hopwoods, J.J., Lindahl, U., and Gallagher, J.T., 1999, Sequence analysis of heparan sulphate and heparin oligosaccharides, Biochem J. 339:767-773.
93. Webb, L.M.C., Ehrengruber, M.U., Clark-Lewis, I., Baggiolini, M., and Rot, A., 1993, Binding to heparan sulfate or heparin enhances neutrophil responses to IL-8, Proc Natl Acad Sci USA. 90:7158-7162.
94. Witt, D.P. and Lander, A.D., 1994, Differential binding of chemokine to glycosaminoglycan subpopulations, Curr Biol. 4:394-400.
95. Wolf, S.F., Temple, P.A., Kobayashi, M., Young, D., Dicig, M., Lowe, L., Dzialo, R., Fitz, L., Ferenz, C., Hewick, R.M., Kelleher, K., Herrmann, S.H., Clark, S.C., Azzoni, L., Chan, S.H., Trinchieri, G., and Perussia, B., 1991, Cloning of cDNA for natural killer cell stimulatory factor, a heterodimeric cytokine with multiple effects on T and natural killer cells, J Immunol. 146:3074-3081.
96. Wrenshall, L.E. and Platt, J.L., 1999, Regulation of T cell homeostasis by heparan sulfate-bound IL-2, J Immunol. 163:3793-3800.
97. Yamada, S., Yoshida, K., Sugiura, M., and Sugahara, K., 1992, One-and two-dimensional H-NMR characterization of two series of sulfated oligosaccharides prepared from chondroitin sulfate and heparan sulfate/heparin by bacterial eliminase digestion, J Biochem. 112:440-447.
98. Yanagishita, M., 1994, A brief history of proteoglycans, EXS. 70:3-7.
99. Yanagishita, M. and Hascall, V.C., 1992, Cell surface heparan sulfate proteoglycans, J Biol Chem. 287:9451-9454.
100. Yayon, A., Klagsburn, M., Esko, J.D., Leder, P., and Ornitz, D.M., 1991, Cell surface heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor, Cell. 64:841-848.
101. Yip, Y.K., Barrowclough, B.S., Urban, C., and Vilcek, J., 1982, Purification of two subspecies of human γ (immune) interferon, Proc Natl Acad Sci USA. 79:1820-1824.