Antibody binding to porcine sialoadhesin reduces phagocytic capacity without affecting other macrophage effector functions

Cellular Immunology

Volumn 271, Issue 2, 2011, Pages 462-473

  De Baere, Miet I ^a   Van Gorp, Hanne ^a   Nauwynck, Hans J ^a   Delputte, Peter L ^b  

^a GHENT UNIVERSITY   (Belgium)

^b GHENT UNIVERSITY HOSPITAL   (Belgium)

Author keywords

Cytokine production; Immunotherapy; MHC expression; Phagocytosis; Primary alveolar macrophage; Reactive oxygen nitrogen species production; Sialoadhesin; Siglec; Soluble antigen uptake and processing; Viability

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MICROSPHERE; MONOCLONAL ANTIBODY; REACTIVE OXYGEN METABOLITE; SIALOADHESIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANTIGEN BINDING; ANTIGEN EXPRESSION; ARTICLE; CELL SURFACE; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; LUNG ALVEOLUS MACROPHAGE; MACROPHAGE FUNCTION; NONHUMAN; OXIDATIVE STRESS; PHAGOCYTOSIS; PRIORITY JOURNAL;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGEN PRESENTATION; CELL MEMBRANE; CYTOKINES; HISTOCOMPATIBILITY ANTIGENS CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS II; LIGANDS; MACROPHAGES, ALVEOLAR; MEMBRANE GLYCOPROTEINS; PHAGOCYTOSIS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; RECEPTORS, IMMUNOLOGIC; SWINE;

SUS;

EID: 80054016622     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2011.08.016     Document Type: Article

References (77)

1. Gordon S., Taylor P.R. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 2005, 5:953-964.
2. Robbins C.S., Swirski F.K. The multiple roles of monocyte subsets in steady state and inflammation. Cell. Mol. Life Sci. 2010, 67:2685-2693.
3. Aderem A., Ulevitch R.J. Toll-like receptors in the induction of the innate immune response. Nature 2000, 406:782-787.
4. Aderem A. Phagocytosis and the inflammatory response. J. Infect. Dis. 2003, 187:S340-S345.
5. Fang F.C. Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J. Clin. Invest. 1997, 99:2818-2825.
6. Gordon S. Alternative activation of macrophages. Nat. Rev. Immunol. 2003, 3:23-35.
7. Iles K.E., Forman H.J. Macrophage signaling and respiratory burst. Immunol. Res. 2002, 26:95-105.
8. Zhang X., Mosser D.M. Macrophage activation by endogenous danger signals. J. Pathol. 2008, 214:161-178.
9. Varin A., Gordon S. Alternative activation of macrophages: immune function and cellular biology. Immunobiology 2009, 214:630-641.
10. Barral P., Polzella P., Bruckbauer A., van Rooijen N., Besra G.S., Cerundolo V., Batista F.D. CD169+ macrophages present lipid antigens to mediate early activation of iNKT cells in lymph nodes. Nat. Immunol. 2010, 11:U303-U348.
11. Jutras I., Desjardins M. Phagocytosis: at the crossroads of innate and adaptive immunity. Annu. Rev. Cell Dev. Biol. 2005, 21:511-527.
12. Ramachandra L., Simmons D., Harding C.V. MHC molecules and microbial antigen processing in phagosomes. Curr. Opin. Immunol. 2009, 21:98-104.
13. Batista F.D., Harwood N.E. The who, how and where of antigen presentation to B cells. Nat. Rev. Immunol. 2009, 9:15-27.
14. Martinez-Pomares L., Gordon S. Antigen presentation the macrophage way. Cell 2007, 131:641-643.
15. Taylor P.R., Martinez-Pomares L., Stacey M., Lin H.H., Brown G.D., Gordon S. Macrophage receptors and immune recognition. Annu. Rev. Immunol. 2005, 23:901-944.
16. Crocker P.R., Gordon S. Properties and distribution of a lectin-like hemagglutinin differentially expressed by murine stromal tissue macrophages. J. Exp. Med. 1986, 164:1862-1875.
17. Crocker P.R., Gordon S. Mouse macrophage hemagglutinin (sheep erythrocyte receptor) with specificity for sialylated glycoconjugates characterized by a monoclonal antibody. J. Exp. Med. 1989, 169:1333-1346.
18. van den Berg T.K., Breve J.J.P., Damoiseaux J., Dopp E.A., Kelm S., Crocker P.R., Dijkstra C.D., Kraal G. Sialoadhesin on macrophages: its identification as a lymphocyte adhesion molecule. J. Exp. Med. 1992, 176:647-655.
19. Crocker P.R., Clark E.A., Filbin M., Gordon S., Jones Y., Kehrl J.H., Kelm S., Le Douarin N., Powell L., Roder J., Schnaar R.L., Sgroi D.C., Stamenkovic K., Schauer R., Schachner M., Van den Berg T.K., van der Merwe P.A., Watt S.M., Varki A. Siglecs: a family of sialic-acid binding lectins. Glycobiology 1998, 8:v.
20. Crocker P.R., Paulson J.C., Varki A. Siglecs and their roles in the immune system. Nat. Rev. Immunol. 2007, 7:255-266.
21. Quarles R.H. Myelin-associated glycoprotein (MAG): past present and beyond. J. Neurochem. 2007, 100:1431-1448.
22. Patel N., Brinkman-Van der Linden E.C.M., Altmann S.W., Gish K., Balasubramanian S., Timans J.C., Peterson D., Bell M.P., Bazan J.F., Varki A., Kastelein R.A. OB-BP1/Siglec-6 - a leptin- and sialic acid-binding protein of the immunoglobulin superfamily. J. Biol. Chem. 1999, 274:22729-22738.
23. Munday J., Floyd H., Crocker P.R. Sialic acid binding receptors (siglecs) expressed by macrophages. J. Leukoc. Biol. 1999, 66:705-711.
24. Hartnell A., Steel J., Turley H., Jones M., Jackson D.G., Crocker P.R. Characterization of human sialoadhesin, a sialic acid binding receptor expressed by resident and inflammatory macrophage populations. Blood 2001, 97:288-296.
25. Gijbels M.J.J., van der Cammen M., van der Laan L.J.W., Emeis J.J., Havekes L.M., Hofker M.H., Kraal G. Progression and regression of atherosclerosis in APOE3-Leiden transgenic mice: an immunohistochemical study. Atherosclerosis 1999, 143:15-25.
26. Nath D., Hartnell A., Happerfield L., Miles D.W., Burchell J., Taylor-Papadimitriou J., Crocker P.R. Macrophage-tumour cell interactions: identification of MUC1 on breast cancer cells as a potential counter-receptor for the macrophage-restricted receptor sialoadhesin. Immunology 1999, 98:213-219.
27. Crocker P.R., Mucklow S., Bouckson V., McWilliam A., Willis A.C., Gordon S., Milon G., Kelm S., Bradfield P. Sialoadhesin, a macrophage sialic acid binding receptor for hematopoietic cells with 17 immunoglobulin-like domains. EMBO J. 1994, 13:4490-4503.
28. Crocker P.R., Redelinghuys P. Siglecs as positive and negative regulators of the immune system. Biochem. Soc. Trans. 2008, 36:1467-1471.
29. Crocker P.R., Kelm S., Dubois C., Martin B., McWilliam A.S., Shotton D.M., Paulson J.C., Gordon S. Purification and properties of sialoadhesin, a sialic acid-binding receptor of murine tissue macrophages. EMBO J. 1991, 10:1661-1669.
30. Nath D., Vandermerwe P.A., Kelm S., Bradfield P., Crocker P.R. The amino-terminal immunoglobulin-like domain of sialoadhesin contains the sialic acid binding site. Comparison with CD22. J. Biol. Chem. 1995, 270:26184-26191.
31. Kumamoto Y., Higashi N., Denda-Nagai K., Tsuiji M., Sato K., Crocker P.R., Irimura T. Identification of sialoadhesin as a dominant lymph node counter-receptor for mouse macrophage galactose-type C-type lectin 1. J. Biol. Chem. 2004, 279:49274-49280.
32. Martinez-Pomares L., Crocker P.R., Da Silva R., Holmes N., Colominas C., Rudd P., Dwek R., Gordon S. Cell-specific glycoforms of sialoadhesin and CD45 are counter-receptors for the cysteine-rich domain of the mannose receptor. J. Biol. Chem. 1999, 274:35211-35218.
33. Seyerl M., Kirchberger S., Majdic O., Seipelt J., Jindra C., Schrauf C., Stöckl J. Human rhinoviruses induce IL-35-producing Treg via induction of B7-H1 (CD274) and sialoadhesin (CD169) on DC. Eur. J. Immunol. 2010, 40:321-329.
34. Van Breedam W., Delputte P.L., Van Gorp H., Misinzo G., Vanderheijden N., Duan X.B., Nauwynck H.J. Porcine reproductive and respiratory syndrome virus entry into the porcine macrophage. J. Gen. Virol. 2010, 91:1659-1667.
35. Rempel H., Calosing C., Sun B., Pulliam L. Sialoadhesin expressed on IFN-induced monocytes binds HIV-1 and enhances infectivity. PLoS One 2008, 3:9.
36. Jones C., Virji M., Crocker P.R. Recognition of sialylated meningococcal lipopolysaccharide by siglecs expressed on myeloid cells leads to enhanced bacterial uptake. Mol. Microbiol. 2003, 49:1213-1225.
37. Heikema A.P., Bergman M.P., Richards H., Crocker P.R., Gilbert M., Samsom J.N., van Wamel W.J.B., Endtz H.P., van Belkum A. Characterization of the specific interaction between sialoadhesin and sialylated Campylobacter jejuni lipooligosaccharides. Infect. Immun. 2010, 78:3237-3246.
38. Monteiro V.G., Lobato C.S.S., Silva A.R., Medina D.V., de Oliveira M.A., Seabra S.H., de Souza W., DaMatta R.A. Increased association of Trypanosoma cruzi with sialoadhesin positive mice macrophages. Parasitol. Res. 2005, 97:380-385.
39. Vanderheijden N., Delputte P.L., Favoreel H.W., Vandekerckhove J., Van Damme J., van Woensel P.A., Nauwynck H.J. Involvement of sialoadhesin in entry of porcine reproductive and respiratory syndrome virus into porcine alveolar macrophages. J. Virol. 2003, 77:8207-8215.
40. Revilla C., Poderoso T., Martinez P., Alvarez B., Lopez-Fuertes L., Alonso F., Ezquerra A., Dominguez J. Targeting to porcine sialoadhesin receptor improves antigen presentation to T cells. Vet. Res. 2009, 40:15.
41. Delputte P.L., Van Gorp H., Favoreel H.W., Hoebeke I., Delrue I., Dewerchin H., Verdonck F., Verhasselt B., Cox E., Nauwynck H.J. Porcine sialoadhesin (CD169/Siglec-1) is an endocytic receptor that allows targeted delivery of toxins and antigens to macrophages. PLoS One 2011, 6:e16827.
42. Backer R., Schwandt T., Greuter M., Oosting M., Jungerkes F., Tuting T., Boon L., O'Toole T., Kraal G., Limmer A., den Haan J.M.M. Effective collaboration between marginal metallophilic macrophages and CD8+ dendritic cells in the generation of cytotoxic T cells. Proc. Natl. Acad. Sci. USA 2010, 107:216-221.
43. Ducreux J., Tyteca D., Ucakar B., Medts T., Crocker P.R., Courtroy P.J., Vanbever R. PEGylation of anti-sialoadhesin monoclonal antibodies enhances their inhibitory potencies without impairing endocytosis in mouse peritoneal macrophages. Bioconjug. Chem. 2009, 20:295-303.
44. Ducreux J., Vanbever R., Crocker P.R. The inhibitory potencies of monoclonal antibodies to the macrophage adhesion molecule sialoadhesin are greatly increased following PEGylation. Bioconjug. Chem. 2008, 19:2088-2094.
45. Kratzer R., Mauvais F.X., Burgevin A., Barilleau E., van Endert P. Fusion proteins for versatile antigen targeting to cell surface receptors reveal differential capacity to prime immune responses. J. Immunol. 2010, 184:6855-6864.
46. O'Reilly M.K., Paulson J.C. Siglecs as targets for therapy in immune-cell-mediated disease. Trends Pharmacol. Sci. 2009, 30:240-248.
47. Genini S., Malinverni R., Delputte P.L., Fiorentini S., Stella A., Botti S., Nauwynck H.J., Giuffra E. Gene expression profiling of porcine alveolar macrophages after antibody-mediated cross-linking of sialoadhesin (SnSiglec-1). J. Recept. Signal Transduct. 2008, 28:185-243.
48. Wensvoort G., Terpstra C., Pol J.M.A., Terlaak E.A., Bloemraad M., Dekluyver E.P., Kragten C., Vanbuiten L., Denbesten A., Wagenaar F., Broekhuijsen J.M., Moonen P., Zetstra T., Deboer E.A., Tibben H.J., Dejong M.F., Vantveld P., Groenland G.J.R., Vangennep J.A., Voets M.T., Verheijden J.H.M., Braamskamp J. Mystery swine disease in the Netherlands: the isolation of Lelystad virus. Vet. Q. 1991, 13:121-130.
49. Duan X.B., Nauwynck H.J., Favoreel H.W., Pensaert M.B. Identification of a putative receptor for porcine reproductive and respiratory syndrome virus on porcine alveolar macrophages. J. Virol. 1998, 72:4520-4523.
50. Nauwynck H.J., Pensaert M.B. Effect of specific antibodies on the cell-associated spread of pseudorabies virus in monolayers of different cell types. Arch. Virol. 1995, 140:1137-1146.
51. Hammerberg C., Schurig G.G. Characterization of monoclonal antibodies directed against swine leukocytes. Vet. Immunol. Immunopathol. 1986, 11:107-121.
52. Lefebvre D.J., Costers S., Van Doorsselaere J., Misinzo G., Delputte P.L., Nauwynck H.J. Antigenic differences among porcine circovirus type 2 strains, as demonstrated by the use of monoclonal antibodies. J. Gen. Virol. 2008, 89:177-187.
53. Boyen F., Pasmans F., Donne E., Van Immerseel F., Adriaensen C., Hernalsteens J.P., Ducatelle R., Haesebrouck F. Role of SPI-1 in the interactions of Salmonella typhimurium with porcine macrophages. Vet. Microbiol. 2006, 113:35-44.
54. Van Reeth K., Van Gucht S., Pensaert M. Correlations between lung proinflammatory cytokine levels virus replication and disease after swine influenza virus challenge of vaccination-immune pigs. Viral Immunol. 2002, 15:583-594.
55. Pesanti E.L. Kinetics of phagocytosis of Staphylococcus aureus by alveolar and peritoneal macrophages. Infect. Immun. 1979, 26:479-486.
56. Malek T.R., Castro I. Interleukin-2 receptor signaling: at the interface between tolerance and immunity. Immunity 2010, 33:153-165.
57. Miller L.C., Lager K.M., Kehrli M.E. Role of toll-like receptors in activation of porcine alveolar macrophages by porcine reproductive and respiratory syndrome virus. Clin. Vaccine Immunol. 2009, 16:360-365.
58. Ahsan F.L., Rivas I.P., Khan M.A., Suarez A.I.T. Targeting to macrophages: role of physicochemical properties of particulate carriers-liposomes and microspheres-on the phagocytosis by macrophages. J. Control. Release 2002, 79:29-40.
59. Burke B. Macrophages as novel cellular vehicles for gene therapy. Expert Opin. Biol. Ther. 2003, 3:919-924.
60. Chellat F., Merhi Y., Moreau A., Yahia L. Therapeutic potential of nanoparticulate systems for macrophage targeting. Biomaterials 2005, 26:7260-7275.
61. Keler T., He L., Ramakrishna V., Champion B. Antibody-targeted vaccines. Oncogene 2007, 26:3758-3767.
62. Tacken P.J., de Vries I.J.M., Torensma R., Figdor C.G. Dendritic-cell immunotherapy: from ex vivo loading to in vivo targeting. Nat. Rev. Immunol. 2007, 7:790-802.
63. Zelnickova P., Matiasovic J., Pavlova B., Kudlackova H., Kovaru F., Faldyna M. Quantitative nitric oxide production by rat, bovine and porcine macrophages. Nitric Oxide Biol. Chem. 2008, 19:36-41.
64. Pampusch M.S., Bennaars A.M., Harsch S., Murtaugh M.P. Inducible nitric oxide synthase expression in porcine immune cells. Vet. Immunol. Immunopathol. 1998, 61:279-289.
65. Luo Y., Pollard J.W., Casadevall A. Fc gamma receptor cross-linking stimulates cell proliferation of macrophages via the ERK pathway. J. Biol. Chem. 2010, 285:4232-4242.
66. May R.C., Machesky L.M. Phagocytosis and the actin cytoskeleton. J. Cell Sci. 2001, 114:1061-1077.
67. Rapoport E.M., Sapot'ko Y.B., Pazynina G.V., Bojenko V.K., Bovin N.V. Sialoside-binding macrophage lectins in phagocytosis of apoptotic bodies. Biochem. Moscow 2005, 70:330-338.
68. Wang Y., Neumann H. Alleviation of neurotoxicity by microglial human Siglec-11. J. Neurosci. 2010, 30:3482-3488.
69. Ziegenfuss J.S., Biswas R., Avery M.A., Hong K., Sheehan A.E., Yeung Y.G., Stanley E.R., Freeman M.R. Draper-dependent glial phagocytic activity is mediated by Src and Syk family kinase signalling. Nature 2008, 453:U935-U968.
70. Schneberger D., Aharonson-Raz K., Singh B. Monocyte and macrophage heterogeneity and toll-like receptors in the lung. Cell Tissue Res. 2011, 343:97-106.
71. Brockmeier S.L., Halbur P.G., Thacker E.L. Porcine respiratory disease complex. Polymicrobial Diseases 2002, 231-258. ASM Press, Washington, DC. K.A. Brogden, J.M. Guthmiller (Eds.).
72. Krysko O., Vandenabeele P., Krysko D.V., Bachert C. Impairment of phagocytosis of apoptotic cells and its role in chronic airway diseases. Apoptosis 2010, 15:1137-1146.
73. Bautista E.M., Gregg D., Golde W.T. Characterization and functional analysis of skin-derived dendritic cells from swine without a requirement for in vitro propagation. Vet. Immunol. Immunopathol. 2002, 88:131-148.
74. Janicka M., Chindemi P.A., Hu W.L., Regoeczi E. Effect of transferrin on the degradation of glycoproteins bearing a hybrid or high-mannose glycan by alveolar macrophages. Exp. Cell Res. 1994, 215:17-22.
75. Basta S., Carrasco C.P., Knoetig S.M., Rigden R.C., Gerber H., Summerfield A., McCullough K.C. Porcine alveolar macrophages: poor accessory or effective suppressor cells for T-lymphocytes. Vet. Immunol. Immunopathol. 2000, 77:177-190.
76. Henry F., Bretaudeau L., Hequet A., Barbieux I., Lieubeau B., Meflah K., Gregoire M. Role of antigen-presenting cells in long-term antitumor response based on tumor-derived apoptotic body vaccination. Pathobiology 1999, 67:306-310.
77. Schmid J.P., de Saint Basile G. Inherited hemophagocytic lymphohistiocytosis (HLH). Klinische Padiatr. 2010, 222:345-350.