Material properties in complement activation

Advanced Drug Delivery Reviews

Volumn 63, Issue 12, 2011, Pages 1000-1007

  Moghimi, S Moein ^a   Andersen, Alina J ^a   Ahmadvand, Davoud ^a   Wibroe, Peter P ^a   Andresen, Thomas L ^b   Hunter, A Christy ^c  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c UNIVERSITY OF BRIGHTON   (United Kingdom)

Author keywords

Acute allergic reactions; Liposomes; Nanomedicine; Nanospheres; Nanotoxicology; Polymers

Indexed keywords

ALLERGIC REACTIONS; CLINICAL MEDICINE; COMPLEMENT SYSTEMS; DRUG CARRIER; LIFE THREATENING CONDITIONS; MATERIAL DESIGNS; MATERIAL PROPERTY; MECHANISTIC ASPECTS; NANO PARTICULATES; NANO-ENGINEERING; NANOMEDICINES; NANOSCALE SIZE; NANOTOXICOLOGY; SENSING MOLECULES; SURFACE CHARACTERISTICS;

LIPOSOMES; MATERIALS PROPERTIES; MEDICAL NANOTECHNOLOGY; MEDICINE; NANOSTRUCTURED MATERIALS; PHOSPHOLIPIDS;

POLYMERS;

ANTIHISTAMINIC AGENT; COMPLEMENT COMPONENT C1S INHIBITOR; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C3B; COMPLEMENT COMPONENT C4A; COMPLEMENT COMPONENT C5A; DEXAMETHASONE; DOXORUBICIN; HISTAMINE H2 RECEPTOR ANTAGONIST; LEUKOTRIENE; LIPOSOME; MACROGOL; NANOMATERIAL; NANOPARTICLE; OLIGONUCLEOTIDE PHOSPHOROTHIOATE; PACLITAXEL; PHOSPHOLIPID; POLOXAMER; POLYMER; PROSTAGLANDIN; THROMBOCYTE ACTIVATING FACTOR; THROMBOXANE;

BIOCOMPATIBILITY; BLOOD CLOTTING; COMPLEMENT ACTIVATION; COMPLEMENT CLASSICAL PATHWAY; COMPLEMENT LECTIN PATHWAY; COMPLEMENT SYSTEM; DRUG DELIVERY SYSTEM; DRUG MEGADOSE; EQUIPMENT DESIGN; HUMAN; IMMUNOCOMPETENT CELL; INFLAMMATION; MICELLE; NANOENGINEERING; NANOMEDICINE; NEOPLASM; NONHUMAN; OPSONIZATION; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW; SURFACE PROPERTY; THROMBOGENESIS; TUMOR GROWTH; UNSPECIFIED SIDE EFFECT;

ANIMALS; BIOCOMPATIBLE MATERIALS; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM PROTEINS; HUMANS; NANOMEDICINE; POLYMERS;

EID: 80052154470     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2011.06.002     Document Type: Review

References (78)

1. Szebeni J. Complement activation-related pseudoallergy: a new class of drug-induced acute immune toxicity. Toxicology 2005, 216:106-121.
2. Channan-Khan A., Szebeni J., Savay S., Liebes L., Rafique N.M., Alving C.R., Muggia F.M. Complement activation following first exposure to pegylated liposomal doxorubicin (Doxil): possible role in hypersensitivity reactions. Annal. Oncology 2003, 14:1430-1437.
3. Alberts D.S., Garcia D.J. Safety aspects of pegylated liposomal doxorubicin in patients with cancer. Drugs 1997, 54(Suppl.):30-45.
4. Uziely B., Jeffers S., Isacson R., Kutsch K., Wei-Tsao D., Yehoshua Z., Libson E., Muggia F.M., Gabizon A. Liposomal doxorubicin: activity and unique toxicities during two complementary phase I studies. J. Clin. Oncol. 1995, 13:1777-1785.
5. Szebeni J. Complement activation-related pseudoallergy caused by liposomes, micellar carriers of intravenous drugs, and radiocontrast agents. Crit Rev Ther Drug Carrier Syst 2001, 18:567-606.
6. Moghimi S.M., Andersen A.J., Hashemi S.H., Lettiero B., Ahmadvand D., Hunter A.C., Andresen T.L., Hamad I., Szebeni J. Complement activation cascade triggered by PEG-PL engineered nanomedicines and carbon nanotubes: the challenges ahead. J Control Release 2010, 146:175-181.
7. Szebeni J., Baranyi L., Savay S., Bodo M., Milosevits J., Alving C.R., Bunger R. Complement activation-related cardiac anaphylaxis in pigs: role of C5a anaphylatoxin and adenosine in liposome-induced abnormalities in ECG and heart function. Am J Physiol Heart Circ Physiol 2006, 290:H1050-H1058.
8. Szebeni J., Alving C.R., Rosivall L., Bunger R., Baranyi L., Bedocs P., Toth M., Barenholz Y. Animal models of complement-mediated hypersensitivity reactions to liposomes and other lipid-based nanoparticles. J. Liposome Res. 2007, 17:107-117.
9. Walport M.J. Advances in immunology: complement (first of two parts). N Engl J Med 2001, 344:1058-1066.
10. Walport M.J. Advances in immunology: complement (second of two parts). N Engl J Med 2001, 344:1140-1144.
11. Moghimi S.M., Hamad I. Liposome-mediated triggering of complement cascade. J. Liposome Res. 2008, 18:195-209.
12. Ricklin D., Hajishengallis G., Yang K., Lambris J.D. Complement: a key system for immune surveillance and hemostasis. Nat. Immunol. 2010, 11:785-797.
13. Moghimi S.M., Hunter A.C., Murray J.C. Long-circulating and target-specific nanoparticles: theory to practice. Pharmacol. Rev. 2001, 53:283-318.
14. Moghimi S.M., Hamad I., Andresen T.L., Jørgensen K., Szebeni J. Methylation of the phosphate oxygen moiety of phospholipid-methoxy(polyethylene glycol) conjugate prevents PEGylated liposome-mediated complement activation and anaphylatoxin production. FASEB J. 2006, 20:2591-2593.
15. Dos Santos N., Allen C., Doppen A.M., Cox K.A.K., Galleher R.C., Karlsson G., Edwards K., Kenner G., Samuells L., Webb M.S., Bally M.B. Influence of poly(ethylene glycol) grafting density and polymer length on liposomes: relating plasma circulation lifetimes to protein binding. Biochim. Biophys. Acta Biomembr. 2007, 1768:1367-1377.
16. Andersen A.J., Hashemi A.H., Andresen T.L., Hunter A.C., Moghimi S.M. Complement: alive and kicking nanomedicines. J. Biomed. Nanotechnol. 2009, 5:364-372.
17. Hattori R., Hamilton K.K., McEver R.P., Sims P.J. Complement proteins C5b-9 induce secretion of high molecular-weight multimers of endothelial von Willebrand-factor and translocation of granule membrane-protein GMP-140 to the cell-surface. J. Biol. Chem. 1989, 264:9053-9060.
18. Szebeni J., Muggia F.M., Alving C.R. Complement activation by cremophor EL as a possible contributor to hypersensitivity to paclitaxel: an in vitro study. J. Natl. Cancer Inst. 1998, 90:300-306.
19. Szebeni J., Alving C.R., Savay S., Barenholz Y., Priev A., Dnino D., Talmon Y. Formation of complement-activating particles in aqueous solutions of Taxol: possible role in hypersensitivity. Int. Immunopharmacol. 2001, 1:721-735.
20. Andersson J., Ekdahl K.N., Larsson R., Nilsson U.R., Nilsson B. C3 adsorbed to a polymer surface can form an initiating alternative pathway convertase. J. Immunol. 2002, 168:5786-5791.
21. Moghimi S.M., Hunter A.C., Dadswell C.M., Savey S., Alving C.R., Szebeni J. Causative factors behind poloxamer 188 (Pluronic F68, Flocor™)-induced complement activation in human sera. A protective role against poloxamer-mediated complement activation by elevated levels of lipoproteins. Biochim. Biophys. Acta Mol. Basis Dis. 2004, 1689:103-113.
22. Andersson J., Bexborn F., Klinth J., Nilsson B., Ekdahl K.N. Surface-attached PEO in the form of activated pluronic with immobilized factor H reduces both coagulation and complement activation in a whole-blood model. J. Biomed. Mater. Res. Part A 2005, 76A:25-34.
23. Arima Y., Toda M., Iwata H. Complement activation on surfaces modifies with ethylene glycol units. Biomaterials 2008, 29:551-560.
24. Hamad I., Hunter A.C., Szebeni J., Moghimi S.M. Poly(ethylene glycol)s generate complement activation products in human serum through increased alternative pathway turnover and a MASP-2-dependent process. Mol. Immunol. 2008, 46:225-232.
25. Hamad I., Al-Hanbali O., Hunter A.C., Rutt K.J., Andresen T.L., Moghimi S.M. Distinct polymer architecture mediates switching of complement activation pathways at the nanosphere-serum interface: implications for stealth nanoparticle engineering. ACS Nano 2010, 4:6629-6638.
26. Engberg A.E., Rosengren-Holmberg J.P., Chen H., Nilsson B., Lambris J.D., Nicholls I.A., Ekdahl K.N. Blood protein-polymer adsorption: implications for understanding complement-mediated hemoincompatibility. J Biomed Mater Res A 2011, 97A:74-84.
27. Chonn A., Cullis P., Devine D.A. The role of surface charge in the activation of the classical and alternative pathways of complement by liposomes. J. Immunol. 1991, 146:4234-4241.
28. Bradley A.J., Maurer-Spurej E., Brooks D.E., Devine D.V. Unusual electrostatic effects on binding of C1q to anionic liposomes: role of anionic phospholipids domain and their line tension. Biochemistry 1999, 38:8112-8123.
29. Bradley A.J., Brooks D.E., Norris-Jones R., Devine D.V. C1q binding to liposomes is charge dependent and is inhibited by peptides consisting of residues 14-26 of the human C1qA chain in a sequence independent manner. Biochim. Biophys. Acta 1999, 1418:19-30.
30. Gbadamosi J.K., Hunter A.C., Moghimi S.M. PEGylation of microspheres generates a heterogeneous population of particles with differential surface characteristics and biological performance. FEBS Lett. 2002, 523:338-344.
31. Moghimi S.M., Szebeni J. Stealth liposomes and nanoparticles: critical issues on protein-binding properties, activation of proteolytic blood cascades and intracellular fate. Prog. Lipid Res. 2003, 42:463-478.
32. Moghimi S.M., Hunter A.C., Murray J.C. Nanomedicine: current status and future prospects. FASEB J. 2005, 19:311-330.
33. Salvador-Morales C., Flahaut E., Sim E., Sloan J., Green M.L.H., Sim R.B. Complement activation and protein adsorption by carbon nanotubes. Mol. Immunol. 2006, 43:193-201.
34. Al-Hanbali O., Rutt K.J., Sarker D., Hunter A.C., Moghimi S.M. Concentration dependent structural ordering of poloxamine 908 on polystyrene nanoparticles and their modulatory role on complement consumption. J. Nanosci. Nanotechnol. 2006, 6:3126-3133.
35. Salvador-Morales C., Basiuk E.V., Basiuk V.A., Green H.M.L., Sim R.B. Effects of covalent functionalization on the biocompatibility of multi-walled carbon nanotubes. J. Nanosci. Nanotechnol. 2007, 8:2347-2356.
36. Hamad I., Hunter A.C., Rutt K.J., Liu Z., Dai H., Moghimi S.M. Complement activation by PEGylated single-walled carbon nanotubes is independent of C1q and alternative pathway turnover. Mol. Immunol. 2008, 45:3797-3803.
37. Toda M., Kitazawa T., Hirata I., Hirano Y., Iwata H. Complement activation on surfaces carrying amino groups. Biomaterials 2008, 29:407-417.
38. Lundqvist M., Stigler J., Elia G., Lynch I., Cedervall T., Dawson K.A. Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:14265-14270.
39. Sou K., Tsuchida E. Electrostatic interactions and complement activation on the surface of phospholipid vesicle containing acidic lipids: effect of the structure of acidic groups. Biochim. Biophys. Acta 2008, 1778:1035-1041.
40. Salvador-Morales C., Zhang L.F., Langer R., Farokhzad O.C. Immunocompatibility properties of lipid-polymer hybrid nanoparticles with heterogenous surface functional groups. Biomaterials 2009, 30:2231-2240.
41. Pedersen M.B., Zhou X., Larsen E.K.U., Sørensen U.S., Kjems J., Nygaard J.V., Nyengaard J.R., Meyer R.L., Bosen T., Vorup-Jensen T. Curvature of synthetic and natural surfaces is an important target feature in classical pathway complement activation. J. Immunol. 2010, 184:1931-1945.
42. Moghimi S.M., Hunter A.C. Complement monitoring of carbon nanotubes. Nat. Nanotechnol. 2010, 5:382.
43. Janssen B.J., Christodoulidou A., McCarthy A., Lambris J.D., Gros P. Structure of C3b reveals conformational changes that underlie complement activity. Nature 2006, 444:213-216.
44. Woodburn K., Sykes E., Kessel D. Interactions of Solutol HS15 and Cremophor EL with plasma lipoproteins. Int. J. Biochem. Cell Biol. 1995, 27:693-699.
45. Ingram D.A., Forman M.B., Murray J.J. Activation of complement by Flusol attributes to the Pluronic detergent micelle structure. J. Cardiovasc. Pharmacol. 1993, 22:456-461.
46. Vercellotti G.M., Hammerschmidth D.E., Craddock P.R., Jacob H.S. Activation of plasma complement by perfluorocarbon artificial blood: probable mechanism of adverse pulmonary reactions in treated patients and rationale for corticosteroid prophylaxis. Blood 1982, 59:1299-1304.
47. Kent K.M., Cleman M.W., Cowley M.J., Forman M.B., Jaffe C.C., Kaplan M., King S.B., Krucoff M.W., Lassar T., Mcauley B., Smith R., Wisdom C., Wohlgelernter D. Reduction of myocardial ischemia during percutaneous coronary angioplasty with oxygenated Fluosol. Am. J. Cardiol. 1990, 66:279-284.
48. Hamilton K.K., Zaho J., Sims P.J. Interaction between apolipoproteins A-I and A-II and the membrane attack complex of complement. J. Biol. Chem. 1993, 268:3632-3638.
49. Blunk T., Hochstrasser D.F., Sanchez J.-C., Muller B.W., Muller R.H. Colloidal carriers for intravenous drug targeting: plasma protein adsorption patterns on surface-modified latex particles evaluated by two-dimensional polyacrylamide gel electrophoresis. Electrophoresis 1993, 14:1382-1387.
50. Cedervall T., Lynch I., Foy M., Berggard T., Donnelly S.C., Cagney G., Linse S., Dawson K.A. Detailed identification of plasma proteins adsorbed on copolymer nanoparticles. Angew. Chem. Int. Ed. 2007, 46:5754-5756.
51. Monopoli M.P., Walczyk D., Campbell A., Elia G., Lynch I., Bombelli F.B., Dawson K.A. Physical-chemical aspects of protein corona: relevance to in vitro and in vivo biological impacts of nanoparticles. J. Am. Chem. Soc. 2011, 133:2525-2534.
52. Price M.E., Cornelius R.M., Brash J.L. Protein adsorption to polyethylene glycol modified liposomes from fibrinogen solution and from plasma. Biochim. Biophys. Acta 2001, 1512:191-205.
53. Wu Y.Q., Qu H.C., Sfyroera G., Tzekou A., Kay B.K., Nilsson B., Ekdahl K.N., Ricklin D., Lambris J.D. Protection of nonself surfaces from complement attack by factor H-binding peptides: implications for therapeutic medicine. J. Immunol. 2011, 186:4269-4277.
54. Moghimi S.M., Hunter A.C. Recognition by macrophages and liver cells of opsonised phospholipid vesicles and phospholipid headgroups. Pharm. Res. 2001, 18:1-8.
55. Nilsson U.R., Storm K.E., Elwing H., Nilsson B. Conformational epitopes of C3 reflecting its mode of binding to an artificial polymer surface. Mol. Immunol. 1993, 30:211-219.
56. Lutz H.U., Fumia S., Schurtenberger C., Alaia V. Opinion paper: Stimulation of complement amplification or activation of the alternative pathway of complement?. Mol. Immunol. 2007, 44:3862-3865.
57. Hallstrom T., Blom A.M., Zipfel P.F., Riesbeck K. Nontypeable Haemophilus influenza protein E binds vitronectin and is important for serum resistance. J. Immunol. 2009, 183:2593-2601.
58. Mosqueira V.C.F., Legrand P., Gulik A., Bourdon O., Gref R., Labarre D., Barratt G. Relationship between complement activation, cellular uptake and surface physicochemical aspects of novel PEG-modified nanocapsules. Biomaterials 2001, 22:2967-2979.
59. Peracchia M.T., Harnisch S., Pinto-Alphandary H., Gulik A., Dedieu J.C., Desmaele D., d'Angelo J., Muller R.H., Couvreur P. Visualization of in vitro protein-rejecting properties of PEGylated Stealth® polycyanoacrylate nanoparticles. Biomaterials 1999, 20:1269-1275.
60. Szebeni J., Baranyi L., Savay S., Lutz H.U., Jelezarova E., Bunger R., Alving C.R. The role of complement activation in hypersensitivity to pegylated liposomal doxorubicin (Doxil). J. Liposome Res. 2000, 10:469-481.
61. Ishida T., Wang X., Shimizu T., Nawata K., Kiwada H. PEGylated liposomes elicit an anti-PEG IgM response in a T-cell-independent manner. J Control Release 2007, 122:349-355.
62. Wang X., Ishida T., Kiwada H. Anti-PEG IgM elicited by injection of liposomes is involved in the enhanced blood clearance of a subsequent dose of PEGylated liposome. J Control Release 2007, 119:236-244.
63. Srinivasan S.K., Iversen P. Review of in vivo pharmacokinetics and toxicology of phosphorothioate oligonucleotides. J. Clin. Lab. Anal. 1995, 9:129-137.
64. Sarmiento U.M., Perez J.R., Becker J.M., Narayanan R. In vivo toxicological effects of rel A antisense phosphorotioate in CD-1 mice. Antisense Res. Dev. 1994, 4:99-107.
65. Zhang X., Kimura Y., Fang C., Zhou L., Sfyroera G., Lambris J.D., Westel R.A., Miwa T., Song W.C. Regulation of Toll-like receptor-mediated inflammatory response by complement in vivo. Blood 2007, 110:228-236.
66. Markiewski M.M., DeAngelis R.A., Benencia F., Ricklin-lichtsteiner S.K., Koutoulaki A., Gerard G., Coukos G., Lambris J.D. Modulation of the antitumour immune response by complement. Nat Immunol 2008, 9:1225-1235.
67. Henry S.P., Giclas P.C., Leeds J., Pangburn M., Auletta C., Levin A.A., Kornburst D.J. Activation of the alternative pathway of complement by a phosphorothioate oligonucleotide: potential mechanisms of action. J. Pharmacol. Exp. Ther. 1997, 281:810-816.
68. Mangsbo S.M., Sanchez J., Anger K., Lambris J.D., Ekdahl K.N., Loskog A.S., Nilsson B., Totterman T.H. Complement activation by CpG in ahuman whole blood loop system: mechanisms and immunomodulatory effects. J. Immunol. 2009, 183:6724-6732.
69. Fearon D.T., Carroll M.C. Regulation of B lymphocyte responses to foreign and self-antigens by the CD19/CD21 complex. Ann. Rev. Immunol. 2000, 18:393-422.
70. Reddy S.T., van der Vlies A.J., Simeoni E., Angeli V., Randolph G.J., O'Niell C.P., Lee L.K., Swratz M.A., Hubbell J.A. Exploiting lymphatic transport and complement activation in nanoparticles vaccines. Nat. Biotechnol. 2007, 25:1159-1164.
71. Ricklin D., Lambris J.D. Complement-targeted therapeutics. Nat. Biotechnol. 2007, 25:1265-1275.
72. Rooijakkers S.H.M., van Strijp J.A.G. Bacterial complement evasion. Mol. Immunol. 2007, 44:23-32.
73. Lambris J.D., Ricklin D., Geisbrecht B.V. Complement evasion by human pathogens. Nat. Rev. Microbiol. 2008, 6:132-142.
74. Moghimi S.M., Hamad I., Bunger R., Andresen T.L., Jorgensen K., Hunter A.C., Baranji L., Rosivall L., Szebeni J. Activation of the human complement system by cholesterol-rich and PEGylated liposomes. Modulation of cholesterol-rich liposome-mediated complement activation by elevated serum LDL and HDL levels. J. Liposome Res. 2006, 16:167-174.
75. Moghimi S.M., Andresen T.L. Complement-mediated tumour growth: implications for cancer nanotechnology and nanomedicines. Mol. Immunol. 2009, 46:1571-1572.
76. Emmerling M.R., Watson M.D., Raby C.A., Spiegel K. The role of complement in Alzheimer's disease. Biochim. Biophys. Acta 2000, 1502:158-171.
77. Lyzogubov V.V., Tytarenko R.G., Liu J., Bora N.S., Bora P.S. Polyethylene glycol (PEG)-induced mouse model of choroidal neovascularisation. J. Biol. Chem. 2011, 286:16229-16237.
78. Lenz H.J. Management and preparedness for infusion and hypersensitivity reactions. Oncologist 2007, 12:601-619.