The induction of cytokines by polycation containing microspheres by a complement dependent mechanism

Biomaterials

Volumn 34, Issue 3, 2013, Pages 621-630

  Rokstad, Anne Mari ^a   Brekke, Ole Lars ^b   Steinkjer, Bjørg ^a   Ryan, Liv ^a   Kolláriková, Gabriela ^c   Strand, Berit L ^a   Skjåk Bræk, Gudmund ^a   Lambris, John D ^d   Lacík, Igor ^c   Mollnes, Tom Eirik ^b,e   Espevik, Terje ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b NORDLAND HOSPITAL   (Norway)

^c POLYMER INSTITUTE   (Slovakia)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e UNIVERSITY OF OSLO   (Norway)

Author keywords

Alginate; Biocompatibility; Biomaterial; Complement; Inflammation; Microspheres

Indexed keywords

ANTI-INFLAMMATORIES; CHEMOKINES; COMPLEMENT; COMPSTATIN; CYTOKINES; GROWTH FACTOR; INFLAMMATION; INFLAMMATORY CYTOKINES; INFLAMMATORY MEDIATORS; INFLAMMATORY RESPONSE; L-LYSINE; POLYCATIONS; SCREENING ASSAYS; WHOLE BLOOD;

ALGINATE; AMINO ACIDS; BIOCOMPATIBILITY; BIOMATERIALS; BLOOD;

MICROSPHERES;

BIOMATERIAL; COMPLEMENT; COMPLEMENT COMPONENT C3; CYTOKINE; GUANIDINE; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LEPIRUDIN; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MICROSPHERE; MONOCYTE CHEMOTACTIC PROTEIN 1; POLY(METHYLENE CO GUANIDINE); POLYCATION; POLYLYSINE; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; VASCULOTROPIN;

ARTICLE; CELL ENCAPSULATION; COMPLEMENT ACTIVATION; COMPLEMENT DEPOSITION; CONTROLLED STUDY; CYTOKINE PRODUCTION; PRIORITY JOURNAL; SCREENING TEST;

ALGINATES; BIOCOMPATIBLE MATERIALS; CHEMOKINE CCL3; COMPLEMENT ACTIVATION; COMPLEMENT C3; CYTOKINES; GUANIDINES; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-10; INTERLEUKIN-6; INTERLEUKIN-8; MICROSPHERES; PEPTIDES, CYCLIC; POLYAMINES; POLYLYSINE; TUMOR NECROSIS FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84868481408     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2012.10.012     Document Type: Article

References (52)

1. Anderson J.M., Rodriguez A., Chang D.T. Foreign body reaction to biomaterials. Semin Immunol 2008, 20:86-100.
2. Luttikhuizen D.T., van Amerongen M.J., de Feijter P.C., Petersen A.H., Harmsen M.C., van Luyn M.J. The correlation between difference in foreign body reaction between implant locations and cytokine and MMP expression. Biomaterials 2006, 27:5763-5770.
3. Luttikhuizen D.T., Dankers P.Y., Harmsen M.C., van Luyn M.J. Material dependent differences in inflammatory gene expression by giant cells during the foreign body reaction. J Biomed Mater Res A 2007, 83:879-886.
4. Schutte R.J., Xie L., Klitzman B., Reichert W.M. In vivo cytokine-associated responses to biomaterials. Biomaterials 2009, 30:160-168.
5. Brodbeck W.G., Voskerician G., Ziats N.P., Nakayama Y., Matsuda T., Anderson J.M. In vivo leukocyte cytokine mRNA responses to biomaterials are dependent on surface chemistry. J Biomed Mater Res A 2003, 64:320-329.
6. Schutte R.J., Parisi-Amon A., Reichert W.M. Cytokine profiling using monocytes/macrophages cultured on common biomaterials with a range of surface chemistries. J Biomed Mater Res A 2009, 88:128-139.
7. Brodbeck W.G., Nakayama Y., Matsuda T., Colton E., Ziats N.P., Anderson J.M. Biomaterial surface chemistry dictates adherent monocyte/macrophage cytokine expression in vitro. Cytokine 2002, 18:311-319.
8. Jones J.A., Chang D.T., Meyerson H., Colton E., Kwon I.K., Matsuda T., et al. Proteomic analysis and quantification of cytokines and chemokines from biomaterial surface-adherent macrophages and foreign body giant cells. J Biomed Mater Res A 2007, 83:585-596.
9. Holt D.J., Chamberlain L.M., Grainger D.W. Cell-cell signaling in co-cultures of macrophages and fibroblasts. Biomaterials 2010, 31:9382-9394.
10. Nilsson B., Korsgren O., Lambris J.D., Ekdahl K.N. Can cells and biomaterials in therapeutic medicine be shielded from innate immune recognition?. Trends Immunol 2010, 31:32-38.
11. Ekdahl K.N., Lambris J.D., Elwing H., Ricklin D., Nilsson P.H., Teramura Y., et al. Innate immunity activation on biomaterial surfaces: a mechanistic model and coping strategies. Adv Drug Deliv Rev 2011, 63:1042-1050.
12. Babensee J.E., Cornelius R.M., Brash J.L., Sefton M.V. Immunoblot analysis of proteins associated with HEMA-MMA microcapsules: human serum proteins in vitro and rat proteins following implantation. Biomaterials 1998, 19:839-849.
13. Tang L., Ugarova T.P., Plow E.F., Eaton J.W. Molecular determinants of acute inflammatory responses to biomaterials. J Clin Invest 1996, 97:1329-1334.
14. Mollnes T.E., Brekke O.L., Fung M., Fure H., Christiansen D., Bergseth G., et al. Essential role of the C5a receptor in E coli-induced oxidative burst and phagocytosis revealed by a novel lepirudin-based human whole blood model of inflammation. Blood 2002, 100:1869-1877.
15. Bergseth G., Lambris J.D., Mollnes T.E., Lappegard K.T. Artificial surface-induced inflammation relies on complement factor 5: proof from a deficient person. Ann Thorac Surg 2011, 91:527-533.
16. Lappegard K.T., Fung M., Bergseth G., Riesenfeld J., Mollnes T.E. Artificial surface-induced cytokine synthesis: effect of heparin coating and complement inhibition. Ann Thorac Surg 2004, 78:38-44.
17. Lappegard K.T., Bergseth G., Riesenfeld J., Pharo A., Magotti P., Lambris J.D., et al. The artificial surface-induced whole blood inflammatory reaction revealed by increases in a series of chemokines and growth factors is largely complement dependent. J Biomed Mater Res A 2008, 87:129-135.
18. Sokolov A., Hellerud B.C., Lambris J.D., Johannessen E.A., Mollnes T.E. Activation of polymorphonuclear leukocytes by candidate biomaterials for an implantable glucose sensor. J Diabetes Sci Technol 2011, 5:1490-1498.
19. Sokolov A., Hellerud B.C., Johannessen E.A., Mollnes T.E. Inflammatory response induced by candidate biomaterials of an implantable microfabricated sensor. J Biomed Mater Res A 2012, 100:1142-1150.
20. Luttikhuizen D.T., Harmsen M.C., van Luyn M.J. Cytokine and chemokine dynamics differ between rats and mice after collagen implantation. J Tissue Eng Regen Med 2007, 1:398-405.
21. Vaithilingam V., Tuch B.E. Islet transplantation and encapsulation: an update on recent developments. Rev Diabet Stud 2011, 8:51-67.
22. 2+ microbeads: in vitro and in vivo function. Artif Cells Blood Substit Immobil Biotechnol 2008, 36:403-420.
23. Rokstad A.M., Brekke O.L., Steinkjer B., Ryan L., Kollarikova G., Strand B.L., et al. Alginate microbeads are complement compatible, in contrast to polycation containing microcapsules, as revealed in a human whole blood model. Acta Biomater 2011, 7:2566-2578.
24. Qu H., Ricklin D., Bai H., Chen H., Reis E.S., Maciejewski M., et al. New analogs of the clinical complement inhibitor compstatin with subnanomolar affinity and enhanced pharmacokinetic properties. Immunobiology 2012, Available from:. http://www.ncbi.nlm.nih.gov/pubmed/22795972.
25. Mollnes T.E., Redl H., Hogasen K., Bengtsson A., Garred P., Speilberg L., et al. Complement activation in septic baboons detected by neoepitope-specific assays for C3b/iC3b/C3c, C5a and the terminal C5b-9 complement complex (TCC). Clin Exp Immunol 1993, 91:295-300.
26. Strand B.L., Morch Y.A., Espevik T., Skjak-Braek G. Visualization of alginate-poly-L-lysine-alginate microcapsules by confocal laser scanning microscopy. Biotechnol Bioeng 2003, 82:386-394.
27. Lacik I., Brissova M., Anilkumar A.V., Powers A.C., Wang T. New capsule with tailored properties for the encapsulation of living cells. J Biomed Mater Res 1998, 39:52-60.
28. Mollnes T.E., Lea T., Harboe M. Detection and quantification of the terminal C5b-9 complex of human complement by a sensitive enzyme-linked immunosorbent assay. Scand J Immunol 1984, 20:157-166.
29. Brekke O.L., Christiansen D., Fure H., Pharo A., Fung M., Riesenfeld J., et al. Combined inhibition of complement and CD14 abolish E. coli-induced cytokine-, chemokine- and growth factor-synthesis in human whole blood. Mol Immunol 2008, 45:3804-3813.
30. Lappegard K.T., Christiansen D., Pharo A., Thorgersen E.B., Hellerud B.C., Lindstad J., et al. Human genetic deficiencies reveal the roles of complement in the inflammatory network: lessons from nature. Proc Natl Acad Sci U S A 2009, 106:15861-15866.
31. Mangsbo S.M., Sanchez J., Anger K., Lambris J.D., Ekdahl K.N., Loskog A.S., et al. Complement activation by CpG in a human whole blood loop system: mechanisms and immunomodulatory effects. J Immunol 2009, 183:6724-6732.
32. Zhang X., Kimura Y., Fang C., Zhou L., Sfyroera G., Lambris J.D., et al. Regulation of Toll-like receptor-mediated inflammatory response by complement in vivo. Blood 2007, 110:228-236.
33. Hajishengallis G., Lambris J.D. Crosstalk pathways between Toll-like receptors and the complement system. Trends Immunol 2010, 31:154-163.
34. Klos A., Tenner A.J., Johswich K.O., Ager R.R., Reis E.S., Kohl J. The role of the anaphylatoxins in health and disease. Mol Immunol 2009, 46:2753-2766.
35. Strand B.L., Ryan T.L., In't V.P., Kulseng B., Rokstad A.M., Skjak-Brek G., et al. Poly-L-Lysine induces fibrosis on alginate microcapsules via the induction of cytokines. Cell Transplant 2001, 10:263-275.
36. Guo R.F., Ward P.A. Role of C5a in inflammatory responses. Annu Rev Immunol 2005, 23:821-852.
37. Chen N.J., Mirtsos C., Suh D., Lu Y.C., Lin W.J., McKerlie C., et al. C5L2 is critical for the biological activities of the anaphylatoxins C5a and C3a. Nature 2007, 446:203-207.
38. Pan Z.K. Anaphylatoxins C5a and C3a induce nuclear factor kappaB activation in human peripheral blood monocytes. Biochim Biophys Acta 1998, 1443:90-98.
39. Monsinjon T., Gasque P., Chan P., Ischenko A., Brady J.J., Fontaine M.C. Regulation by complement C3a and C5a anaphylatoxins of cytokine production in human umbilical vein endothelial cells. Faseb J 2003, 17:1003-1014.
40. Laudes I.J., Chu J.C., Huber-Lang M., Guo R.F., Riedemann N.C., Sarma J.V., et al. Expression and function of C5a receptor in mouse microvascular endothelial cells. J Immunol 2002, 169:5962-5970.
41. Rittirsch D., Flierl M.A., Nadeau B.A., Day D.E., Huber-Lang M., Mackay C.R., et al. Functional roles for C5a receptors in sepsis. Nat Med 2008, 14:551-557.
42. Riedemann N.C., Guo R.F., Bernacki K.D., Reuben J.S., Laudes I.J., Neff T.A., et al. Regulation by C5a of neutrophil activation during sepsis. Immunity 2003, 19:193-202.
43. Takeda Y., Kaneda K., Jimma F., Shiobara N., Hidaka M., Saniabadi A.R., et al. Inhibition of CXCL10 release by monomeric C3bi and C4b. Clin Exp Immunol 2012, 167:149-157.
44. Shokouhi B., Coban C., Hasirci V., Aydin E., Dhanasingh A., Shi N., et al. The role of multiple toll-like receptor signalling cascades on interactions between biomedical polymers and dendritic cells. Biomaterials 2010, 31:5759-5771.
45. King A., Sandler S., Andersson A. The effect of host factors and capsule composition on the cellular overgrowth on implanted alginate capsules. J Biomed Mater Res 2001, 57:374-383.
46. King A., Strand B., Rokstad A.M., Kulseng B., Andersson A., Skjak-Braek G., et al. Improvement of the biocompatibility of alginate/poly-L-lysine/alginate microcapsules by the use of epimerized alginate as a coating. J Biomed Mater Res A 2003, 64:533-539.
47. Vandenbossche G.M., Bracke M.E., Cuvelier C.A., Bortier H.E., Mareel M.M., Remon J.P. Host reaction against empty alginate-polylysine microcapsules. Influence of preparation procedure. J Pharm Pharmacol 1993, 45:115-120.
48. Safley S.A., Cui H., Cauffiel S., Tucker-Burden C., Weber C.J. Biocompatibility and immune acceptance of adult porcine islets transplanted intraperitoneally in diabetic NOD mice in calcium alginate poly-L-lysine microcapsules versus barium alginate microcapsules without poly-L-lysine. J Diabetes Sci Technol 2008, 2:760-767.
49. Boor P., Konieczny A., Villa L., Schult A.L., Bucher E., Rong S., et al. Complement C5 mediates experimental tubulointerstitial fibrosis. J Am Soc Nephrol 2007, 18:1508-1515.
50. Le Y., Zhou Y., Iribarren P., Wang J.M. Chemokines and chemokine receptors: their manifold roles in homeostais and disease. Cell Mol Imm 2004, 1:95-104.
51. Koch A.E., Polverini P.J., Kunkel S.L., Harlow L.A., DiPietro L.A., Elner V.M., et al. Interleukin-8 as a macrophage-derived mediator of angiogenesis. Science 1992, 258:1798-1801.
52. Belperio J., Keane M.P., Burdick M.D., Gomperts B., Xue Y.Y., Hong K., et al. Role of CXCR2/CXCR2 ligands in vascular remodeling during bronchiolitis obliterans syndrome. J Clin Invest 2005, 115:1150-1162.