Differential uptake of nanoparticles by human M1 and M2 polarized macrophages: Protein corona as a critical determinant

Nanomedicine

Volumn 11, Issue 22, 2016, Pages 2889-2902

  Binnemars Postma, Karin A ^a   Ten Hoopen, Hetty Wm ^a   Storm, Gert ^a,b   Prakash, Jai ^a  

^a UNIVERSITY OF TWENTE   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

complement factor; heat inactivated serum; M1 macrophages; M2 macrophages; nanoparticles; opsonization; phagocytosis; protein corona; serum proteins; silica nanoparticles

Indexed keywords

DECTIN 1; INTERLEUKIN 1BETA; PROTEIN CORONA; SILICA NANOPARTICLE; TUMOR NECROSIS FACTOR; LIGAND; NANOPARTICLE; PLASMA PROTEIN; SILICON DIOXIDE;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DC SIGN GENE; DECTIN 1 GENE; GENE; HUMAN; HUMAN CELL; IL 1BETA GENE; MACROPHAGE; MONOCYTE; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RPS18 GENE; TNF ALPHA GENE; CHEMISTRY; DRUG EFFECTS; FLOW CYTOMETRY; METABOLISM;

BLOOD PROTEINS; CELL DIFFERENTIATION; FLOW CYTOMETRY; HUMANS; LIGANDS; MACROPHAGES; NANOPARTICLES; PARTICLE SIZE; PROTEIN CORONA; SILICON DIOXIDE;

EID: 84994607144     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm-2016-0233     Document Type: Article

References (51)

1. Duncan R, Gaspar R. Nanomedicine(s) under the microscope. Mol. Pharmaceutics 8(6), 2101-2141 (2011).
2. Petros RA, Desimone JM. Strategies in the design of nanoparticles for therapeutic applications. Nat. Rev. Drug Discov. 9(8), 615-627 (2010).
3. Waite CL, Roth CM. Nanoscale drug delivery systems for enhanced drug penetration into solid tumors: current progress and opportunities. Crit. Rev. Biomed. Eng. 40(1), 21-41 (2012).
4. Flannagan RS, Jaumouille V, Grinstein S. The cell biology of phagocytosis. Annu. Rev. Pathol. 7, 61-98 (2012).
5. Owens DE 3rd, Peppas NA. Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. Int. J. Pharm. 307(1), 93-102 (2006).
6. Liu T, Choi H, Zhou R, Chen IW. Quantitative evaluation of the reticuloendothelial system function with dynamic MRI. PLoS ONE 9(8), e103576 (2014).
7. Alexis F, Pridgen E, Molnar LK, Farokhzad OC. Factors affecting the clearance and biodistribution of polymeric nanoparticles. Mol. Pharmaceutics 5(4), 505-515 (2008).
8. Haniffa M, Bigley V, Collin M. Human mononuclear phagocyte system reunited. Semin. Cell Dev. Biol. 41, 59-69 (2015).
9. Podila R, Brown JM. Toxicity of engineered nanomaterials: A physicochemical perspective. J. Biochem. Mol. Toxicol. 27(1), 50-55 (2013).
10. Verma A, Stellacci F. Effect of surface properties on nanoparticle-cell interactions. Small 6(1), 12-21 (2010).
11. Lewis JS, Roy K, Keselowsky BG. Materials that harness and modulate the immune system. MRS Bull. 39(1), 25-34 (2014).
12. Edwards DA, Hanes J, Caponetti G et al. Large porous particles for pulmonary drug delivery. Science 276(5320), 1868-1871 (1997).
13. Champion JA, Mitragotri S. Role of target geometry in phagocytosis. Proc. Natl Acad. Sci. USA 103(13), 4930-4934 (2006).
14. Frohlich E. The role of surface charge in cellular uptake and cytotoxicity of medical nanoparticles. Int. J. Nanomed. 7, 5577-5591 (2012).
15. Bhattacharjee S, Ershov D, Fytianos K et al. Cytotoxicity and cellular uptake of tri-block copolymer nanoparticles with different size and surface characteristics. Part. Fibre Toxicol. 9, 11 (2012).
16. Anselmo AC, Zhang M, Kumar S et al. Elasticity of nanoparticles influences their blood circulation, phagocytosis, endocytosis, and targeting. ACS Nano 9(3), 3169-3177 (2015).
17. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5(12), 953-964 (2005).
18. Allavena P, Mantovani A. Immunology in the clinic review series; focus on cancer: Tumour-associated macrophages: undisputed stars of the inflammatory tumour microenvironment. Clin. Exp. Immunol. 167(2), 195-205 (2012).
19. Viola J, Soehnlein O. Atherosclerosis-a matter of unresolved inflammation. Semin. Immunol. 27(3), 184-193 (2015).
20. Bartneck M, Warzecha KT, Tacke F. Therapeutic targeting of liver inflammation and fibrosis by nanomedicine. Hepatobiliary Surg. Nutr. 3(6), 364-376 (2014).
21. Sica A, Larghi P, Mancino A et al. Macrophage polarization in tumour progression. Semin. Cancer Biol. 18(5), 349-355 (2008).
22. Biswas SK, Gangi L, Paul S et al. A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-kappaB and enhanced IRF-3/ STAT1 activation). Blood 107(5), 2112-2122 (2006).
23. Schiffelers RM, Metselaar JM, Fens MH, Janssen AP, Molema G, Storm G. Liposome-encapsulated prednisolone phosphate inhibits growth of established tumors in mice. Neoplasia 7(2), 118-127 (2005).
24. Banciu M, Schiffelers RM, Fens MH, Metselaar JM, Storm G. Anti-angiogenic effects of liposomal prednisolone phosphate on B16 melanoma in mice. J. Control. Release 113(1), 1-8 (2006).
25. Hoppstädter J, Seif M, Dembek A et al. M2 polarization enhances silica nanoparticle uptake by macrophages. Front. Pharmacol. 6, 55 (2015).
26. Krysko O, Holtappels G, Zhang N et al. Alternatively activated macrophages and impaired phagocytosis of S. Aureus in chronic rhinosinusitis. Allergy 66(3), 396-403 (2011).
27. Durafourt BA, Moore CS, Zammit DA et al. Comparison of polarization properties of human adult microglia and bloodderived macrophages. Glia 60(5), 717-727 (2012).
28. Chinetti-Gbaguidi G, Baron M, Bouhlel MA et al. Human atherosclerotic plaque alternative macrophages display low cholesterol handling but high phagocytosis because of distinct activities of the PPARgamma and LXRalpha pathways. Circ. Res. 108(8), 985-995 (2011).
29. Lesniak A, Fenaroli F, Monopoli MP, Aberg C, Dawson KA, Salvati A. Effects of the presence or absence of a protein corona on silica nanoparticle uptake and impact on cells. ACS Nano 6(7), 5845-5857 (2012).
30. Lesniak A, Salvati A, Santos-Martinez MJ, Radomski MW, Dawson KA, Aberg C. Nanoparticle adhesion to the cell membrane and its effect on nanoparticle uptake efficiency. J. Am. Chem. Soc. 135(4), 1438-1444 (2013).
31. Tenzer S, Docter D, Rosfa S et al. Nanoparticle size is a critical physicochemical determinant of the human blood plasma corona: A comprehensive quantitative proteomic analysis. ACS Nano 5(9), 7155-7167 (2011).
32. Shannahan JH, Podila R, Brown JM. A hyperspectral and toxicological analysis of protein corona impact on silver nanoparticle properties, intracellular modifications, and macrophage activation. Int. J. Nanomedicine 10, 6509-6521 (2015).
33. Martinez FO, Gordon S, Locati M, Mantovani A. Transcriptional profiling of the human monocyte-tomacrophage differentiation and polarization: new molecules and patterns of gene expression. J. Immunol. 177(10), 7303-7311 (2006).
34. Relloso M, Puig-Kroger A, Pello OM et al. DC-SIGN (CD209) expression is IL-4 dependent and is negatively regulated by IFN, TGF-beta, and anti-inflammatory agents. J. Immunol. 168(6), 2634-2643 (2002).
35. Willment JA, Marshall AS, Reid DM et al. The human beta-glucan receptor is widely expressed and functionally equivalent to murine Dectin-1 on primary cells. Eur. J. Immunol. 35(5), 1539-1547 (2005).
36. Stöber W, Fink A, Bohn E. Controlled growth of monodisperse silica spheres in the micron size range. J. Colloid Interface Sci. 26(1), 62-69 (1968).
37. Hartlen KD, Athanasopoulos AP, Kitaev V. Facile preparation of highly monodisperse small silica spheres (15 to <200 nm) suitable for colloidal templating and formation of ordered arrays. Langmuir 24(5), 1714-1720 (2008).
38. Scalia S, Young PM, Traini D. Solid lipid microparticles as an approach to drug delivery. Expert Opin. Drug Deliv. 12(4), 583-599 (2015).
39. De Jong WH, Borm PJ. Drug delivery and nanoparticles: Applications and hazards. Int. J. Nanomed. 3(2), 133-149 (2008).
40. Van Lookeren Campagne M, Wiesmann C, Brown EJ. Macrophage complement receptors and pathogen clearance. Cell. Microbiol. 9(9), 2095-2102 (2007).
41. Yang A, Liu W, Li Z, Jiang L, Xu H, Yang X. Influence of polyethyleneglycol modification on phagocytic uptake of polymeric nanoparticles mediated by immunoglobulin G and complement activation. J. Nanosci. Nanotechnol. 10(1), 622-628 (2010).
42. Giard DJ. Routine heat inactivation of serum reduces its capacity to promote cell attachment. In vitro Cell. Dev. Biol. 23(10), 691-697 (1987).
43. Soltis RD, Hasz D, Morris MJ, Wilson ID. The effect of heat inactivation of serum on aggregation of immunoglobulins. Immunology 36(1), 37-45 (1979).
44. Lundqvist M, Stigler J, Elia G, Lynch I, Cedervall T, Dawson KA. Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proc. Natl Acad. Sci. USA 105(38), 14265-14270 (2008).
45. Fedeli C, Segat D, Tavano R et al. The functional dissection of the plasma corona of SiO(2)-NPs spots histidine rich glycoprotein as a major player able to hamper nanoparticle capture by macrophages. Nanoscale 7(42), 17710-17728 (2015).
46. Van Lent P, Nabbe KC, Boross P et al. The inhibitory receptor FcgammaRII reduces joint inflammation and destruction in experimental immune complex-mediated arthritides not only by inhibition of FcgammaRI/III but also by efficient clearance and endocytosis of immune complexes. Am. J. Pathol. 163(5), 1839-1848 (2003).
47. Underhill DM, Ozinsky A. Phagocytosis of microbes: complexity in action. Annu. Rev. Immunol. 20, 825-852 (2002).
48. Su X, Abumrad NA. Cellular fatty acid uptake: A pathway under construction. Trends Endocrinol. Metab. 20(2), 72-77 (2009).
49. Ohtani K, Suzuki Y, Eda S et al. The membrane-type collectin CL-P1 is a scavenger receptor on vascular endothelial cells. J. Biol. Chem. 276(47), 44222-44228 (2001).
50. Berton G, Lowell CA. Integrin signalling in neutrophils and macrophages. Cell. Signal. 11(9), 621-635 (1999).
51. Fuentes AL, Millis L, Vapenik J, Sigola L. Lipopolysaccharide-mediated enhancement of zymosan phagocytosis by RAW 264. 7 macrophages is independent of opsonins, laminarin, mannan, and complement receptor 3. J. Surg. Res. 189(2), 304-312 (2014).