Altered glycosylation of recombinant NKp30 hampers binding to heparan sulfate: A lesson for the use of recombinant immunoreceptors as an immunological tool

Glycobiology

Volumn 18, Issue 1, 2008, Pages 28-41

  Hershkovitz, Oren ^a   Jarahian, Mostafa ^a   Zilka, Alon ^a   Bar Ilan, Ahuva ^a   Landau, Guy ^a   Jivov, Sergey ^a   Tekoah, Yoram ^a   Glicklis, Rachel ^a   Gallagher, John T ^c   Hoffmann, Sabrina C ^b   Zer, Hagit ^d   Mandelboim, Ofer ^e   Watzl, Carsten ^b   Momburg, Frank ^a   Porgador, Angel ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d Institute of Life Sciences   (Israel)

^e HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Glycosylation; Heparan sulfate; Natural killer; NCR; NKp30

Indexed keywords

GAMMA INTERFERON; GLYCAN; HEPARAN SULFATE; PROTEIN NKP30; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; GLYCOSYLATION; HELA CELL; HUMAN; HUMAN CELL; LIGAND BINDING; LYMPHOCYTE ACTIVATION; NATURAL KILLER CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; TUMOR CELL;

ANIMALS; BINDING SITES; CELL LINE, TUMOR; CHO CELLS; CRICETINAE; CRICETULUS; GLYCOSYLATION; HELA CELLS; HEPARITIN SULFATE; HUMANS; PEPTIDE-N4-(N-ACETYL-BETA-GLUCOSAMINYL) ASPARAGINE AMIDASE; POLYSACCHARIDES; RECEPTORS, IMMUNOLOGIC; RECOMBINANT PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 37549028403     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwm125     Document Type: Article

References (46)

1. Achdout H, Arnon TI, Markel G, Gonen-Gross T, Katz G, Lieberman N, Gazit R, Joseph A, Kedar E, Mandelboim O. 2003. Enhanced recognition of human NK receptors after influenza virus infection. J Immunol. 171:915-923.
2. Amon TI, Achdout H, Levi O, Markel G, Saleh N, Katz G, Gazit R, Gonen-Gross T, Hanna J, Nahari E et al. 2005. Inhibition of the NKp30 activating receptor by pp65 of human cytomegalovirus. Nat Immunol. 6:515-523.
3. Amon TI, Achdout H, Lieberman N, Gazit R, Gonen-Gross T, Katz G, Bar-Ilan A, Bloushtain N, Lev M, Joseph A et al. 2004. The mechanisms controlling the recognition of tumor and virus infected cells by NKp46. Blood. 103:664-672.
4. Amon TI, Lev M, Katz G, Chemobrov Y, Porgador A, Mandelboim O. 2001. Recognition of viral hemagglutinins by NKp44 but not by NKp30. Eur J Immunol. 31:2680-2689.
5. Baker KN, Rendall MH, Hills AE, Hoare M, Freedman RB, James DC. 2001. Metabolic control of recombinant protein N-glycan processing in NSO and CHO cells.Biotechnol Bioeng. 73:188-202.
6. Bloushtain N, Qimron U, Bar-Ilan A, Hershkovitz O, Gazit R, Fima E, Korc M, Vlodavsky I, Bovin NV, Porgador A. 2004. Membrane-associated heparan sulfate proteoglycans are involved in the recognition of cellular targets by NKp30 and NKp46. J Immumol. 173:2392-2401.
7. Capila I, Linhardt RJ. 2002. Heparin-protein interactions. Angew Chem Int Ed Engl. 41:391-412.
8. Cerwenka A, Lanier LL. 2003. NKG2D ligands: Unconventional MHC class I-like molecules exploited by viruses and cancer. Tissue Antigens. 61:335-343.
9. Dennissen MA, Jenniskens GJ, Pieffers M, Versteeg EM, Petitou M, Veerkamp JH, van Kuppevelt TH. 2002. Large, tissue-regulated domain diversity of heparan sulfates demonstrated by phage display antibodies. J Biol Chem. 277:10982-10986.
10. Draghi M, Pashine A, Sanjanwala B, Gendzekhadze K, Cantoni C, Cosman D, Moretta. A, Valiante NM, Parham P. 2007. NKp46 and NKG2D recognition of infected dendritic cells is necessary for NK cell activation in the human response to influenza infection. J Immunol. 178:2688-2698.
11. Esko JD. 1991. Genetic analysis of proteoglycan structure, function and metabolism. Curr Opin Cell Biol. 3:805-816.
12. Gabius HJ. 2006. Cell surface glycans: The why and how of their functionality as biochemical signals in lectin-mediated information transfer. Crit Rev Immunol. 26:43-79.
13. Galfre G, Milstein C. 1982. Chemical typing of human kappa light chain subgroups expressed by human hybrid myelomas. Immunology. 45:125-128.
14. Goger B, Halden Y, Rek A, Mosl R, Pye D, Gallagher J, Kungl AJ. 2002. Different affinities of glycosaminoglycan oligosaccharides for monomeric and dimeric interleukin-8: A model for chemokine regulation at inflammatory sites. Biochemistry. 41:1640-1646.
15. Hershkovitz O, Jivov S, Bloushtain N, Zilka A, Landau G, Bar-Ilan A, Lichtenstein RG, Campbell KS, Kuppevelt TH, Porgador A. 2007. Characterization of the recognition of tumor cells by the natural cytotoxicity receptor, NKp44. Biochemistry. 46:7426-7436.
16. Hileman RE, Fromm JR, Weiler JM, Linhardt RJ. 1998. Glycosaminoglycan-protein interactions: Definition of consensus sites in glycosaminoglycan binding proteins. Bioessays. 20:156-167.
17. Ibrahimi OA, Zhang F, Hrstka FC, Mohammadi M, Linhardt RJ. 2004. Kinetic model for FGF, FGFR, and proteoglycan signal transduction complex assembly. Biochemistry. 43:4724-4730.
18. Jang JH, Hwang JH, Chung CP, Choung PH. 2004. Identification and kinetics analysis of a novel heparin-binding site (KEDK) in human tenascin-C. J Biol Chem. 279:25562-25566.
19. Jenkins N, Parekh RB, James DC. 1996. Getting the glycosylation right: Implications for the biotechnology industry. Nat Biotechnol. 14:75-981.
20. Kaneko Y, Nimmerjahn F, Ravetch JV. 2006. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science. 313:670-673.
21. Krapp S, Mimura Y, Jefferis R, Huber R, Sondermann P. 2003. Structural analysis of human IgG-Fc glycoforms reveals a correlation between glycosylation and structural integrity. J Mol Biol. 325:979-989.
22. Kuster B, Wheeler SF, Hunter AP, Dwek RA, Harvey DJ. 1997. Sequencing of N-linked oligosaccharides directly from protein gels: In-gel deglycosylation followed by matrix-assisted laser desorption/ionization mass spectrometry and normal-phase high-performance liquid chromatography. Anal Biochem. 250:82-101.
23. Lai J, Chien J, Staub J, Avula R, Greene EL, Matthews TA, Smith DI, Kaufmann SH, Roberts LR, Shridhar V. 2003. Loss of HSulf-1 up-regulates heparin-binding growth factor signaling in cancer. J Biol Chem. 278:23107-23117.
24. Lewis JA, Brown EL, Duncan PA. 2006. Approaches to the release of a master cell bank of PER.C6 cells; a novel cell substrate for the manufacture of human vaccines. Dev Biol (Basel). 123:165-176; discussion 183-197.
25. Linsley PS, Brady W, Grosmaire L, Aruffo A, Damle NK, Ledbetter JA. 1991. Binding of the B cell activation antigen B7 to CD28 costimulates T cell proliferation and interleukin 2 mRNA accumulation. J Exp Med. 173:721-730.
26. Linsley PS, Brady W, Urnes M, Grosmaire LS, Damle NK, Ledbetter JA. 1991. CTLA-4 is a second receptor for the B cell activation antigen B7. J Exp Med. 174:561-569.
27. Mandelboim OP, Malik DM, Davis CH, Jo J, Boyson E, Strominger JL. 1999. Human CD16 as a lysis receptor mediating direct natural killer cell cytotoxicity. Proc Natl Acad Sci USA. 96:5640-5644.
28. Molinari M. 2007. N-glycan structure dictates extension of protein folding or onset of disposal. Nat Chem Biol. 3:313-320.
29. Momburg F, Armandola EA, Post M, Hammerling GJ. 1996. Residues in TAP2 peptide transporters controlling substrate specificity. J Immunol. 156:1756-1763.
30. Moretta A, Biassoni R, Bottino C, Mingari MC, Moretta L. 2000. Natural cytotoxicity receptors that trigger human NK-cell-mediated cytolysis. Immunol Today. 21:228-234.
31. Moretta L, Bottino C, Cantoni C, Mingari MC, Moretta A. 2001. Human natural killer cell function and receptors. Curr Opin Pharmacol. 1:387-391.
32. Moretta L, Moretta A. 2004. Unravelling natural killer cell function: Triggering and inhibitory human NK receptors. Embo J. 23:255-259.
33. Omitz DM, Itoh N. 2001. Fibroblast growth factors. Genome Biol. 2:1-12.
34. Pende D, Parolini S, Pessino A, Sivori S, Augugliaro R, Morelli L, Marcenaro E, Accame L, Malaspina A, Biassoni R et al. 1999. Identification and molecular characterization of NKp30, a novel triggering receptor involved in natural cytotoxicity mediated by human natural killer cells. J Exp Med. 190:1505-1516.
35. Rauchenberger R, Borges E, Thomassen-Wolf E, Rom E, Adar R, Yaniv Y, Malka M, Chumakov I, Kotzer S, Resnitzky D et al. 2003. Human combinatorial Fab library yielding specific and functional antibodies against the human fibroblast growth factor receptor 3. J Biol Chem. 278:38194-38205.
36. Ricard-Blum S, Feraud O, Lortat-Jacob H, Rencurosi A, Fukul N, Dkhissi F, Vittet D, Imberty A, Olsen BR, Van Der Rest M. 2004. Characterization of endostatin binding to heparin and heparan sulfate by surface plasmon resonance and molecular modeling: Role of divalent cations. J Biol Chem. 279:2927-2936.
37. Rio DC, Clark SG, Tjian R. 1985. A mammalian host-vector system that regulates expression and amplification of transfected genes by temperature induction. Science. 227:23-28.
38. Rudd PM, Colominas C, Royle L, Murphy N, Hart E, Merry AH, Hebestreit HF, Dwek RA. 2001. A high-performance liquid chromatography based strategy for rapid, sensitive sequencing of N-linked oligosaccharide modifications to proteins in sodium dodecyl sulphate polyacrylamide electrophoresis gel bands. Proteomics. 1:285-294.
39. Rudd PM, Dwek RA. 1997. Glycosylation: Heterogeneity and the 3D structure of proteins. Crit Rev Biochem Mol Biol. 32:1-100.
40. Rudd PM, Elliott T, Cresswell P, Wilson IA, Dwek RA. 2001. Glycosylation and the immune system. Science. 291:2370-2376.
41. Sasisekharan R, Venkataraman G. 2000. Heparin and heparan sulfate: Biosynthesis, structure and function. Curr Opin Chem Biol. 4:626-631.
42. Stark S, Flaig RM, Sandusky M, Watzl C. 2005. The use of trimeric isoleucine-zipper fusion proteins to study surface-receptor-ligand interactions in natural killer cells. J Inummol Methods. 296:149-158.
43. Warren HS, Jones AL, Freeman C, Bettadapura J, Parish CR. 2005. Evidence that the cellular ligand for the human NK cell activation receptor NKp30 is not a heparan sulfate glycosaminoglycan.J Immunol. 175:207-212.
44. Werner RG, Noe W, Kopp K, Schluter M. 1998. Appropriate mammalian expression systems for biopharmaccuticals. Arzneimittelforschung. 48:870-880.
45. Winter CC, Long EO. 2000. Binding of soluble KIR-Fc fusion proteins to HLA class I. Methods Mol Biol. 121:239-250.
46. Zilka A, Landau G, Hershkovitz O, Bloushtain N, Bar-Ilan A, Benchetrit F, Fima E, van Kuppevelt TH, Gallagher JT, Elgavish S et al. 2005. Characterization of the heparin/heparan sulfate binding site of the natural cytotoxicity receptor NKp46. Biochemistry. 44:14477-14485.