Profiles of carbohydrate ligands associated with adsorbed proteins on self-assembled monolayers of defined chemistries
Sucharita P. Shankar
Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, 313 Ferst Drive, Atlanta, Georgia 30332
Search for more papers by this authorInn Inn Chen
Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, 313 Ferst Drive, Atlanta, Georgia 30332
Search for more papers by this authorBenjamin G. Keselowsky
George W. Woodruff School of Mechanical Engineering, Georgia Institute of Technology, 313 Ferst Drive, Atlanta, Georgia 30332
Present address: J. Crayton Pruitt Family Department of Biomedical Engineering, University of Florida, Gainesville, FL 32611.
Search for more papers by this authorAndrés J. García
George W. Woodruff School of Mechanical Engineering, Georgia Institute of Technology, 313 Ferst Drive, Atlanta, Georgia 30332
Search for more papers by this authorCorresponding Author
Julia E. Babensee
Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, 313 Ferst Drive, Atlanta, Georgia 30332
Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, 313 Ferst Drive, Atlanta, Georgia 30332Search for more papers by this authorSucharita P. Shankar
Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, 313 Ferst Drive, Atlanta, Georgia 30332
Search for more papers by this authorInn Inn Chen
Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, 313 Ferst Drive, Atlanta, Georgia 30332
Search for more papers by this authorBenjamin G. Keselowsky
George W. Woodruff School of Mechanical Engineering, Georgia Institute of Technology, 313 Ferst Drive, Atlanta, Georgia 30332
Present address: J. Crayton Pruitt Family Department of Biomedical Engineering, University of Florida, Gainesville, FL 32611.
Search for more papers by this authorAndrés J. García
George W. Woodruff School of Mechanical Engineering, Georgia Institute of Technology, 313 Ferst Drive, Atlanta, Georgia 30332
Search for more papers by this authorCorresponding Author
Julia E. Babensee
Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, 313 Ferst Drive, Atlanta, Georgia 30332
Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, 313 Ferst Drive, Atlanta, Georgia 30332Search for more papers by this authorAbstract
Conserved protein–carbohydrate–lipid pathogen-associated molecular patterns (PAMPs) interact with cells of the innate immune system to mediate antigen recognition and internalization and activation of immune cells. We examined if analogous “biomaterial-associated molecular patterns” composed of proteins, specifically their carbohydrate modifications, existed on biomaterials, which can play a role in mediating the innate immune response to biomaterials. To probe for these carbohydrates in the adsorbed protein layer, as directed by the underlying biomaterial chemistry, self-assembled monolayers (SAMs) presenting CH3, OH, COOH, or NH2 were preincubated with serum/plasma, and the presence of carbohydrate ligands of C-type lectin receptors (CLRs) was investigated using lectin probes in an enzyme-linked lectin assay (ELLA). Presentation of CLR ligands was detected on control tissue culture polystyrene (TCPS). Absorbances of mannose or N-acetylglucosamine increased with decreasing incubating serum concentration, whereas absorbances of sialylated epitopes or fucose remained unchanged. Absorbances of α-galactose or N-acetylgalactosamine decreased with decreasing incubating serum concentration; β-galactose was undetectable. Among SAM endgroups, preincubation with 10% serum resulted in differential presentation of CLR ligands: higher α-galactose on COOH SAMs than NH2 or CH3 SAMs, highest complex mannose on NH2 SAMs, and higher complex mannose on OH SAMs than CH3 SAMs. Least sialylated groups were detected on CH3 SAMs. In summary, biomaterial chemistry may regulate protein adsorption and hence unique presentation of associated carbohydrates. The ultimate goal is to identify the effects of protein glycosylations associated with biomaterials in stimulating innate immune responses. © 2009 Wiley Periodicals, Inc. J Biomed Mater Res, 2010
References
- 1 Yago T,Leppanen A,Qiu H,Marcus WD,Nollert MU,Zhu C,Cummings RD,McEver RP. Distinct molecular and cellular stabilizing selectin-mediated rolling under flow. J Cell Biol 2002; 158: 787–799.
- 2 Geijtenbeek TBH,Torensma R,van Vliet SJ,van Duijnhoven GCF,Adema GJ,van Kooyk Y,Figdor CG. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 2000; 100: 575–585.
- 3 Engering A,Geijtenbeek TBH,Van Kooyk Y. Immune escape through C-type lectins on dendritic cells. Trends Immunol 2002; 23: 480–485.
- 4 Gringhuis SI,Den Dunnen J,Litjens M,van het Hof B,van Kooyk Y,Geijtenbeek BH. C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-κB. Immunity 2007; 26: 605–616.
- 5 Liu XE,Desmyter L,Gao CF,Laroy W,Dewaele S,Vanhooren V,Wang L,Zhuang H,Callewaert N,Libert C,Contreras R,Chen C. N-Glycomic changes in hepatocellular carcinoma patients with liver cirrhosis induced by hepatitis B virus. Hepatology 2007; 46: 1426–1435.
- 6 Fujimura T,Shinohara Y,Tissot B,Pang PC,Kurogohi M,Saito S,Arai Y,Sadilek M,Murayama K,Dell A,Nishimura S,Hakomori SI. Glycosylation status of haptoglobin in sera of patients with prostate cancer vs. benign prostate disease or normal subjects. Int J Cancer 2008; 122: 39–49.
- 7 Yung S,Chan TM. Peritoneal proteoglycans: Much more than ground substance. Perit Dial Int 2007; 27: 375–390.
- 8 Roughley PJ. The structure and function of cartilage proteoglycans. Eur Cells Mater 2006; 12: 92–101.
- 9 Macri L,Silverstein D,Clark RA. Growth factor binding to the pericellular matrix and its importance in tissue engineering. Adv Drug Deliv Rev 2007; 59: 1366–1381.
- 10 Ferdous Z,Grande-Allen KJ. Utility and control of proteoglycans in tissue engineering. Tissue Eng 2007; 13: 1893–1904.
- 11 Babensee JE,Anderson JM,McIntire LV,Mikos AG. Host response to tissue engineered devices. Adv Drug Deliv Rev 1998; 33: 111–139.
- 12 Babensee JE,Sefton MV. Viability of HEMA-MMA microencapsulated model hepatoma cells in rats and the host response. Tissue Eng 2000; 6: 165–182.
- 13 Rihova B. Immunocompatibility and biocompatibility of cell delivery systems. Adv Drug Deliv Rev 2000; 42: 65–80.
- 14 Tang L,Eaton JW. Inflammatory response to biomaterials. Am J Clin Pathol 1995; 103: 466–471.
- 15 Kyriakides TR,Leach KJ,Hoffman AS,Ratner BD. Mice that lack the angiogenesis inhibitor thrombospondin 2 mount an altered foreign body reaction characterized by increased vascularity. Proc Natl Acad Sci USA 1999; 96: 4449–4454.
- 16
Picha GJ,Drake RF.
Pillard-surface microstructure and soft-tissue implants: Effect of implant site and fixation.
J Biomed Mater Res
1996;
30:
305–312.
10.1002/(SICI)1097-4636(199603)30:3<305::AID-JBM5>3.0.CO;2-U CAS PubMed Web of Science® Google Scholar
- 17 Sanders JE,Baker AB,Golledge SL. Control of in vivo microvessel ingrowth by modulation of biomaterial local architecture and chemistry. J Biomed Mater Res A 2002; 60: 36–43.
- 18 Brauker JH,Carr-Brendel VE,Martinson LA,Crudele J,Johnston WD,Johnson RC. Neovascularization of synthetic membranes directed by membrane microarchitecture. J Biomed Mater Res A 1995; 29: 1517–1524.
- 19
van Luyn MJ,Khouw IM,van Wachem PB,Blaauw EH,Werkmeister JA.
Modulation of the tissue reaction to biomaterials. II. The function of T cells in the inflammatory reaction to crosslinked collagen implanted in T-cell-deficient rats.
J Biomed Mater Res A
1998;
39:
398–406.
10.1002/(SICI)1097-4636(19980305)39:3<398::AID-JBM8>3.0.CO;2-E CAS PubMed Web of Science® Google Scholar
- 20 Ertl HC,Varga I,Xiang ZQ,Kaiser K,Stephens L,Otvos LJ. Poly(DL-lactide-co-glycolide) microspheres as carriers for peptide vaccines. Vaccine 1996; 14: 879–885.
- 21 Walker KB,Xing DKL,Sesardic D,Corbel MJ. Modulation of the immune response to tetanus toxoid by polylactide-polyglycolide microspheres. Dev Biol Stand 1998; 92: 259–267.
- 22 Matzelle MM,Babensee JE. Humoral and T cell immune responses to model antigen delivered with biomaterials used in tissue engineering. Biomaterials 2004; 25: 295–304.
- 23 Bennewitz NL,Babensee JE. The effect of the physical form of poly(lactic-co-glycolic acid) carriers on the humoral immune response to co-delivered antigen. Biomaterials 2005; 26: 2991–2999.
- 24 Cella M,Engering A,Pinet V,Pieters J,Lanzavecchia A. Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature 1997; 388: 782–787.
- 25 Sun H,Pollock KG,Brewer JM. Analysis of the role of vaccine adjuvants in modulating dendritic cell activation and antigen presentation in vitro. Vaccine 2003; 21: 849–855.
- 26 Singh M,O'Hagan D. Advances in vaccine adjuvants. Nat Biotechnol 1999; 17: 1075–1081.
- 27 Yoshida M,Babensee JE. Poly(lactic-co-glycolic acid) enhances maturation of human monocyte-derived dendritic cells. J Biomed Mater Res A 2004; 71: 45–54.
- 28 Babensee JE,Paranjpe A. Differential levels of dendritic cell maturation on different biomaterials used in combination products. J Biomed Mater Res A 2005; 74: 503–10.
- 29 Yoshida M,Babensee JE. Differential effects of agarose and poly(lactic-co-glycolic acid) on dendritic cell maturation. J Biomed Mater Res A 2006; 79: 393–408.
- 30 Yoshida M,Babensee JE. Molecular aspects of microparticle phagocytosis by dendritic cells. J Biomater Sci Polym Ed 2006; 17: 893–907.
- 31 Brown GD,Gordon S. Immune recognition. A new receptor for beta-glucans. Nature 2001; 413: 36–37.
- 32 Bhardwaj N. Influenza virus-infected dendritic cells stimulate strong proliferative and cytolytic responses from human CD8+ T cells. J Clin Invest 1994; 94: 797–807.
- 33 Smiley ST,King JA,Hancock WW. Fibrinogen stimulates macrophage chemokine secretion through Toll-like receptor 4. J Immunol 2001; 167: 2887–2894.
- 34 Okamura Y,Watari M,Jerud ES,Young DW,Ishizaka ST,Rose J,Chow JC,Strauss JFIII. The extra domain of fibronectin activates toll-like receptor 4. J Biol Chem 2001; 276: 10229–10233.
- 35 Akira S,Takeda K,Kaisho T. Toll-like receptors: Critical proteins linking innate and acquired immunity. Nat Immunol 2001; 2: 675–680.
- 36 Medzhitov R,Janeway CAJ. Toll-like receptors and innate immunity. Nat Rev Immunol 2001; 1: 135–145.
- 37 Aderem A,Ulevitch RJ. Toll-like Receptors in the induction of the innate immune response. Nature. 2000; 406: 782–787.
- 38 Gantner BN,Simmons RM,Canavera SJ,Akira S,Underhill DM. Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J Exp Med 2003; 197: 1107–1117.
- 39 Rogers NC,Slack EC,Edwards AD,Nolte MA,Schulz O,Schweighoffer E,Williams DL,Gordon S,Tybulewicz VL,Brown GD,Sousa CRE. Syk-dependent cytokine induction by Dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity 2005; 22: 507–517.
- 40 Dillon S,Agrawal S,Banerjee K,Letterio J,Denning TL,Oswald-Richter O,Kasprowicz DJ,Kellar K,Pare J,van Dyke T,Ziegler S,Unutmaz D,Pulendran B. Yeast zymosan, a stimulus for TLR2 and dectin-1, induces regulatory antigen-presenting cells and immunological tolerance. J Clin Invest 2006; 116: 916–928.
- 41 Geitjenbeek TBH,Engering A,van Kooyk Y. DC-SIGN, a C-type lectin on dendritic cells that unveils many aspects of dendritic cell biology. J Leukoc Biol 2002; 71: 921–931.
- 42 Valladeau J,Duvert-Frances V,Pin JJ,Kleijmeer MJ,Ait-Yahia S,Ravel O,Vincent C,Veha JF,Helms A,Gorman D,Zurawski SM,Zurawski G,Ford J,Saeland S. Immature human dendritic cells express asialoglycoprotein receptor isoforms for efficient receptor-mediated endocytosis. JImmunol 2001; 167: 5767–5774.
- 43 McGreal EP,Martinez-Pomares L,Gordon S. Divergent roles for C-type lectins expressed by cells of the innate immune system. Mol Immunol 2004; 41: 1109–1121.
- 44 Termeer CC,Hennies J,Voith U,Ahrens T,Weiss JM,Prehm P,Simon JC. Oligosaccharides of hyaluronan are potent activators of dendritic cells. J Immunol 2000; 165: 1863–1887.
- 45 Termeer CC,Benedix F,Sleeman J,Fieber C,Voith U,Ahrens T,Miyake F,Freudenberg M,Galanos C,Simon JC. Oligosaccharides of hyaluronan activate dendritc cells via toll-like receptor 4. J Exp Med 2002; 195: 99–111.
- 46 Banchereau J,Steinman RM. Dendritic cells and the control of immunity. Nature 1998; 392: 245–252.
- 47 Banchereau J,Briere F,Caux C,Davoust J,Lebecque S,Liu YJ,Pulendran B,Palucka K. Immunobiology of dendritic cells. Annu Rev Immunol 2000; 18: 767–811.
- 48 Gallucci S,Lolkema M,Matzinger P. Natural adjuvants: Endogenous activators of dendritic cells. Nat Med 1999; 5: 1249–1255.
- 49 Figdor CG,van Kooyk Y,Adema GJ. C-type lectin receptors on dendritic cells and Langerhans cells. Nat Rev Immunol 2002; 2: 77–84.
- 50 van Kooyk Y,Geitjenbeek TBH. DC-SIGN: Escape mechanism for pathogens. Nat Rev Immunol 2003; 3: 697–709.
- 51 Pulendran B. Modulating vaccine responses with dendritic cells and Toll-like receptors. Immunol Rev 2004; 199: 227–250.
- 52 Janeway CAJ,Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002; 20: 197–216.
- 53 Brown GD,Herre J,Williams DL,Willment JA,Marshall AS,Gordon S. Dectin-1 mediates the biological effects of beta glucans. J Exp Med 2003; 197: 1119–1124.
- 54 Brown GD. Dectin-1: A signaling non-TLR pattern recognition receptor. Nat Rev Immunol 2006; 6: 33–43.
- 55 Silverblatt FJ,Ofek I. Interaction of bacterial pili and leukocytes. Infection 1983; 11: 235–238.
- 56 van Vliet SJ,den Dunnen J,Gringhuis SI,Geijtenbeek THB,van Kooyk Y. Innate signaling and regulation of dendritic cell immunity. Curr Opin Immunol 2007; 19: 435–440.
- 57 Spreu J,Kienle EC,Schrage B,Steinle A. CLEC2A: A novel, alternatively spliced and skin-associated member of the NKC-encoded AICL-CD69-LLT1 family. Immunogenetics 2007; 59: 903–912.
- 58 Werling D,Hope JC,Howard CJ,Jungi TW. Differentialproduction of cytokines, reactive oxygen and nitrogen by bovine macrophages and dendritic cells stimulated with Toll-like receptor agonists. Immunology 2004; 111: 41–52.
- 59 Taylor PR,Brown GD,Reid DM,Willmet JA,Martinez-Pomares L,Gordon S,Wong SY. The beta-glucan receptor, dectin-1, is predominantly expressed on the surface of cells of the monocyte/macrophage and neutrophil lineages. J Immunol 2002; 169: 3876–3882.
- 60 van Villet SJ,van Liempt E,Saeland E,Aarnoudse CA,Applemelk B,Irimura T,Geitjenbeek TBH,Blixt O,Alvarez R,van Die I,van Kooyk Y. Carbohydrate profiling reveals a distinctive role for the C-type lectin MGL in the recognition of helminth parasites and tumor Ags by dendritic cells. Int Immunol 2005; 17: 661–669.
- 61 Jiang W,Swiggard WJ,Heufler C,Peng M,Mirza A,Steinman RM,Nussenzweig MC. The receptor DEC-205 expressed by dendritic cells and thymic epithelial cells is involved in antigen processing. Nature 1995; 375: 151–155.
- 62 Mahnke K,Guo M,Lee S,Sepulveda H,Swain SL,Nussenzweig M,Steinman RM. The dendritic cell receptor for endocytosis, DEC-205, can recycle and enhance antigen presentation via major histocompatibility complex class II-positive lysosomal compartments. J Cell Biol 2000; 151: 673–684.
- 63 Cobb BA,Wang Q,Tzianabos AO,Kasper DL. Polysaccharide processing and presentation by the MHCII pathway. Cell 2004; 117: 677–687.
- 64 Kanazawa N,Okazaki T,Nishimura H,Tashiro K,Inaba K,Miyachi Y. DCIR acts as an inhibitory receptor depending on its immunoreceptor tyrosine-based inhibitory motif. J Invest Dermatol 2002; 118: 261–266.
- 65 Mrksich M,Chen CS,Xia Y,Dike LE,Ingber DE,Whitesides GM. Controlling cell attachment on contoured surfaces with self-assembled monolayers of alkanethiolates on gold. Proc Natl Acad Sci USA 1996; 93: 10775–10778.
- 66 Sigal GB,Mrksich M,Whitesides GM. Effect of surface wettability on the adsorption of proteins and detergents. J Am Chem Soc 1998; 120: 3464–3473.
- 67 Michael KE,Vernekar VN,Keselowsky BG,Meredith JC,Latour RA,Garcia AJ. Adsorption-induced conformational changes in fibronectin due to interactions with well-defined surface chemistries. Langmuir 2003; 19: 8033–8040.
- 68 Luk Y,Kato M,Mrksich M. Self-Assembled monolayers of alkanthiolates presenting mannitol groups are inert to protein adsorption and cell attachment. Langmuir 2000; 16: 9604–9608.
- 69 Harder P,Grunze M,Dahint R,Whitesides GM,Laibinis PE. Molecular conformation on oligo (ethylene glycol)-terminated self-assembled monolayers on gold and silver surfaces determines their ability to resist protein adsorption. J Phys Chem B 1998; 102: 426–436.
- 70
McClary KB,Ugarova T,Grainger DW.
Modulating fibroblast adhesion, spreading and proliferation using self-assembled monolayer films of alkylthiolates on gold.
J Biomed Mater Res
2000;
50:
428–439.
10.1002/(SICI)1097-4636(20000605)50:3<428::AID-JBM18>3.0.CO;2-H CAS PubMed Web of Science® Google Scholar
- 71 Keselowsky BG,Collard DM,Garcia AJ. Surface chemistry modulates fibronectin conformation and directs integrin binding and specificity to control cell adhesion. J Biomed Mater Res A 2003; 66: 247–259.
- 72 Barbosa JN,Barbosa MA,Aguas AP. Adhesion of human leukocytes to biomaterials: An in vitro study using alkanethiolate monolayers with different chemically functionalized surfaces. J Biomed Mater Res A 2003; 65: 429–434.
- 73 Schwendel D,Hayashi T,Dahint R,Pertsin A,Grunze M,Steitz R,Schreiber F. Interaction of water with self-assembled monolayers: neutron reflectivity measurements of the water density in the interface region. Langmuir 2003; 19: 2284–2293.
- 74 Lindbald M,Lestelius M,Johansson A,Tengvall P,Thomsen P. Cell and soft tissue interactions with methyl- and hydroxyl-terminated alkane thiols on gold surfaces. Biomaterials 1997; 18: 1059–1068.
- 75
Tegoulia VA,Cooper SL.
Leukocyte adhesion on model surfaces under flow: Effects of surface chemistry, protein adsorption, and shear rate.
J Biomed Mater Res
2000;
50:
291–301.
10.1002/(SICI)1097-4636(20000605)50:3<291::AID-JBM2>3.0.CO;2-1 CAS PubMed Web of Science® Google Scholar
- 76
Shen M,Horbett TA.
The effects of surface chemistry and adsorbed proteins on monocyte/macrophage adhesion to chemically modified polystyrene surfaces.
J Biomed Mater Res
2001;
57:
336–345.
10.1002/1097-4636(20011205)57:3<336::AID-JBM1176>3.0.CO;2-E CAS PubMed Web of Science® Google Scholar
- 77 Kalltorp M,Oblogina S,Jacobsson S,Karlsson A,Tengvall P,Thomsen P. In vivo cell recruitment, cytokine release and chemiluminescence response at gold, and thiol functionalized surfaces. Biomaterials 1999; 20: 2123–2137.
- 78 Dadsetan M,Jones JA,Hiltner A,Anderson JM. Surface chemistry mediates adhesive structure, cytoskeletal organization, and fusion of macrophages. J Biomed Mater Res A 2004; 71: 439–448.
- 79 Shankar SP, Petrie TA, Garcia AJ, Babensee JE. Dendritic cell responses to self-assembled monolayers of defined chemistries. J Biomed Mater Res. 2010; 92: 1487–1499.
- 80 Leriche V,Sibille P,Carpentier B. Use of an enzyme-linked lectinsorbent assay to monitor the shift in polysaccharide composition in bacterial biofilms. Appl Environ Microbiol 2000; 66: 1851–1856.
- 81 van Leuven F,Torrekens S,Van Damme E,Peumans W,Van den Berghe H. Mannose-specific lectins bind alpha-2-macroglobulin and an unknown protein from human plasma. Protein Sci 1993; 2: 255–263.
- 82 Balzarini J,Van Laethem K,Hatse S,Froeyen M,Van Damme E,Bolmstedt A,Peumans W,De Clercq E. Marked depletion of glycosylation sites in HIV-1 gp120 under selection pressure by the mannose-specific plant lectins of Hippeastrum hybrid and Galanthus nivalis. Mol Pharmacol 2005; 67: 1556–1565.
- 83 Shibuya N,Goldstein IJ,Broekaertg WF,Nsimba-Lubaki M,Peetersll P,Peumans WJ. The elderberry (Sambucus nigra L.) bark lectin recognizes the Neu5Ac(alpha 2–6)Gal/GalNAc sequence. J Biol Chem 1987; 262: 1596–1601.
- 84 De Carlos A,Caride-Castro A,Martinez-Zorzano VS,De La Cadena MP,Rodriguez-Berrocal FJ. Lectin isolation and detection of N-glycoproteins bearing sialic acid and L-fucose residues in human colorectal mucosa and in adenocarcinoma biopsies. Int J Oncol 2002; 20: 367–372.
- 85 Chacko BK,Appukuttan PS. Peanut (Arachis hypogaea) lectin recognizes α-linked galactose, but not N-acetyl lactosamine in N-linked oligosaccharide terminals. Int J Biol Macromol 2001; 28: 365–371.
- 86 Balu K,Chacko PS. Peanut (Arachis hypogaea) lectin recognizes α-linked galactose, but not N-acetyl lactosamine in N-linked oligosaccharide terminals. Int J Biol Macromol 2001; 28: 365–371.
- 87 Sueyoshi S,Tsuji T,Osawa T. Carbohydrate-binding specificities of five lectins that bind to O-glycosyl-linked carbohydrate chains: Quantitative analysis by frontal-affinity chromatography. Carbohydr Res 1988; 178: 213–224.
- 88 Roque-Barreira MC,Campos-Neto A. Jacalin: An IgG-binding lectin. J Immunol 1985; 134: 1740–1743.
- 89 van Damme EJM,Peumans WJ,Pusztai A,Bardocz S. Handbook of Plant Lectins: Properties and Biomedical Applications. Chicester: John Wiley & Sons; 1998.
- 90
Tanahashi M,Matsuda T.
Surface functional group dependence on apatite formation on self-assembled monolayers in a simulated body fluid.
J Biomed Mater Res
1997;
34:
305–315.
10.1002/(SICI)1097-4636(19970305)34:3<305::AID-JBM5>3.0.CO;2-O CAS PubMed Web of Science® Google Scholar
- 91 Franco M,Nealey PF,Campbell S,Teixeira AI,Murphy CJ. Adhesion and proliferation of corneal epithelial cells on self assembled monolayers. J Biomed Mater Res 2000; 52: 261–269.
- 92 Capadona J,Collard D,Garcia AJ. Fibronectin adsorption and cell adhesion to mixed monolayers of tri(ethylene glycol)- and methyl-terminated alkanethiols. Langmuir 2003; 19: 1847–1857.
- 93 Silver JH,Hergenrother RW,Lin JC,Lim F,Lin HB,Okada T,Chaudhury MK,Cooper SL. Surface and blood-contacting properties of alkylsiloxane monolayers supported on silicone rubber. J Biomed Mater Res 1995; 29: 535–548.
- 94 Rodrigues SN,Goncalves IC,Martins MC,Barbosa MA,Ratner BD. Fibrinogen adsorption, platelet adhesion and activation on mixed hydroxyl-/methyl-terminated self-assembled monolayers. Biomaterials 2006; 27: 5357–5367.
- 95 Hirata I,Hioki Y,Toda M,Kitazawa T,Murakami Y,Kitano E,Kitamura H,Ikada Y,Iwata H. Deposition of complement protein C3b on mixed self-assembled monolayers carrying surface hydroxyl and methyl groups studied by surface plasmon resonance. J Biomed Mater Res A 2003; 66: 669–676.
- 96 Silin VV,Weetall H,Vanderah DJ. SPR studies of the nonspecific adsorption kinetics of human IgG and BSA on gold surfaces modified by self-assembled monolayers (SAMs). J Colloid Interface Sci 1997; 185: 94–103.
- 97 Martins MC,Fonseca C,Barbosa MA,Ratner BD. Albumin adsorption on alkanethiols self-assembled monolayers on gold electrodes studied by chronopotentiometry. Biomaterials 2003; 24: 3697–3706.
- 98 McNally AK,DeFife KM,Anderson JM. Interleukin-4-induced macrophage fusion is prevented by inhibitors of mannose receptor activity. Am J Clin Pathol 1996; 149: 975–985.
- 99 Chieppa M,Bianchi G,Doni A,Del Prete A,Sironi M,Laskarin G,Monti P,Piemonti L,Biondi A,Mantovani A,Introna M,Allavena P. Cross-linking of the mannose receptor on monocyte-derived dendritic cells activates an anti-inflammatory immunosuppressive program. J Immunol 2003; 171: 4552–4560.
- 100 Patwa TH,Zhao J,Anderson MA,Simeone DM,Lubman DM. Screening of glycosylation patterns in serum using natural glycoprotein microarrays and multi-lectin fluorescence detection. Anal Chem 2006; 78: 6411–6421.
- 101 Kanoh Y,Mashiko T,Danbara M,Takayama Y,Ohtani S,Imasaki T,Abe T,Akahoshi T. Analysis of the oligosaccharide chain of human serum immunoglobulin G in patients with localized or metastatic cancer. Oncology 2004; 66: 365–370.
- 102 Johnson PJ,Poon TCW,Hjelm NM,Ho CS,Blake C,Ho SKW. Structures of disease-specific serum alpha-fetoprotein isoforms. Br J Cancer 2000; 83: 1330–1337.
- 103 Lee RT,Ichikawa Y,Fay M,Drickhamer K,Shao MC,Lee YC. Ligand-binding characteristics of rat serum-type mannose binding protein (MBP-A). Homology of binding site architecture with mammalian and chicken hepatic lectins. J Biol Chem 1991; 266: 4810–4815.
- 104 Tabares G,Radcliffe CM,Barrabes S,Ramirez M,Aleixandre N,Hoesel W,Dwek RA,Rudd PM,Peracaula R,de Llorens R. Different glycan structures in prostrate-specific antigen from prostrate cancer sera in relation to seminal plasma PSA. Glycobiology 2006; 16: 132–145.
- 105 Turner G. N-Glycosylation of serum proteins in disease and its investigation using lectins. Clin Chim Acta 1992; 208: 149–171.
- 106 Brockhausen I. Pathways of O-glycan biosynthesis in cancer cells. Biochim Biophys Acta 1999; 1473: 67–95.
- 107 Elliott MA,Elliott HG,Ghallagher K,McGuire J,Field M,Smith KD. Investigation into the concanavalin A reactivity, fucosylation and oligosaccharide microheterogeneity of alpha-1-acid glycoprotein expressed in the sera of patients with rheumatoid arthritis. J Chromatogr B Biomed Sci Appl 1997; 688: 229–237.
- 108 Havenaar EC,Axford JS,Brinkman-van der Linden EC,Alavi A,Van Ommen EC,van het Hof B,Spector T,Mackiewiczm A,Van Dijk W. Severe rheumatoid arthritis prohibits the pregnancy-induced decrease in alpha-3-fucosylation of alpha-1-acid glycoprotein. Glycoconj J 1998; 15: 723–729.
- 109 van Gisbergen KPJM,Aarnoudse CA,Meijer GA,Geitjenbeek TBH,van Kooyk Y. Dendritic cells recognize tumor-specific glycosylation of carcinoembryonic antigen on colorectal cancer cells through dendritic cell-specific intercellular adhesion molecule-3-grabbing nonintegrin. Cancer Res 2005; 65: 5935–5944.
- 110 Cambi A,Koopman M,Figdor CG. How C-type lectins detect pathogens. Cell Microbiol 2005; 7: 481–488.
- 111
Okuyama T,Maehara Y,Kakeji Y,Tsujitani S,Korenaga D,Sugimachi K.
Interrelation between tumor-associated cell surface glycoprotein and host immune response in gastric carcinoma patients.
Cancer
1998;
82:
1468–1475.
10.1002/(SICI)1097-0142(19980415)82:8<1468::AID-CNCR6>3.0.CO;2-5 CAS PubMed Web of Science® Google Scholar