Activated human neutrophil response to perfluorocarbon nanobubbles: Oxygen-dependent and -independent cytotoxic responses

Toxicology Letters

Volumn 203, Issue 2, 2011, Pages 172-180

  Hwang, Tsong Long ^a   Fang, Chia Lang ^b   Al Suwayeh, Saleh A ^c   Yang, Li Jia ^a   Fang, Jia You ^a,c,d  

^a CHANG GUNG UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c KING SAUD UNIVERSITY   (Saudi Arabia)

^d CHANG GUNG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

Author keywords

Elastase; Lactate dehydrogenase; Nanobubbles; Neutrophils; Superoxide anion; Toxicity

Indexed keywords

CATIONIC SURFACTANT; COCONUT OIL; ELASTASE; FLUOROCARBON; FORMYLMETHIONYLLEUCYLPHENYLALANINE; LACTATE DEHYDROGENASE; NANOBUBBLE; OCTADECYLAMINE; OXYGEN; PHOSPHATIDYLCHOLINE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE;

ADULT; ARTICLE; CELL ACTIVATION; CELL MEMBRANE; CELLULAR STRESS RESPONSE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG FORMULATION; ENZYME INDUCTION; ENZYME RELEASE; HUMAN; HUMAN CELL; MEMBRANE DAMAGE; NEUTROPHIL; NORMAL HUMAN; PARTICLE SIZE; PRIORITY JOURNAL;

ADULT; CELL SURVIVAL; FLUOROCARBONS; HUMANS; L-LACTATE DEHYDROGENASE; N-FORMYLMETHIONINE LEUCYL-PHENYLALANINE; NANOPARTICLES; NEUTROPHIL ACTIVATION; NEUTROPHILS; PANCREATIC ELASTASE; PHOSPHATIDYLCHOLINES; REACTIVE OXYGEN SPECIES; SUPEROXIDES; YOUNG ADULT;

GLYCINE MAX;

EID: 79955474114     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2011.03.022     Document Type: Article

References (62)

1. Blüml S., Rosc B., Lorincz A., Seyerl M., Kirchberger S., Oskolkova O., Bochkov V.N., Majdic O., Ligeti E., Stöckl J. The oxidation state of phospholipids controls the oxidative burst in neutrophil granulocytes. J. Immunol. 2008, 181:4347-4353.
2. Borden M., Little E., Gillies R., Ferrara K. DNA and polylysine adsorption and multylayer construction onto cationic lipid-coated microbubbles. Langmuir 2007, 23:9401-9408.
3. Boyum A., Lovhaug D., Tresland L., Nordlie E.M. Separation of leucocytes: improved cell purity by fine adjustments of gradient medium density and osmolality. Scand. J. Immunol. 1991, 34:697-712.
4. ®. Eur. J. Pharm. Biopharm. 2000, 49:143-149.
5. Cowburn A.S., Condliffe A.M., Farahi N., Summers C., Chilvers E.R. Advances in neutrophil biology: clinical implications. Chest 2008, 134:606-612.
6. Cury-Boaventura M.F., Gorjão R., de Lima T.M., Piva T.M., Peres C.M., Soriano F.G., Curi R. Toxicity of a soybean oil emulsion on human lymphocytes and neutrophils. J. Parenter. Enteral Nutr. 2006, 30:115-123.
7. Dayton P.A., Chomas J.E., Lum A.F.H., Allen J.S., Lindner J.R., Simon S.I., Ferrara K.W. Optical and acoustical dynamics of microbubble contrast agents inside neutrophils. Biophys. J. 2001, 80:1547-1556.
8. Dias E., Andrade M., Alverca E., Pereira P., Batoréu M.C.C., Jordan P., Silva M.J. Comparative study of the cytotoxic effect of microcistin-LR and purified extracts from Microcystis aeruginosa on a kidney cell line. Toxicon 2009, 53:487-495.
9. 19F-MRI. Pharm. Res. 2010, 27:1-16.
10. Dobrovolskaia M.A., McNeil S.E. Immunological properties of engineered nanomaterials. Nat. Nanotechnol. 2007, 2:469-478.
11. Ehrenberg M.S., Friedman A.E., Finkelstein J.N., Oberdörster G., McGrath J.L. The influence of protein adsorption on nanoparticle association with cultured endothelial cells. Biomaterials 2009, 30:603-610.
12. Fang J.Y., Hung C.F., Hua S.C., Hwang T.L. Acoustically active perfluorocarbon nanoemulsions as drug delivery carriers for camptothecin: drug release and cytotoxicity against cancer cells. Ultrasonics 2009, 49:39-46.
13. Fang J.Y., Hung C.F., Liao M.H., Chien C.C. A study of the formulation design of acoustically active lipospheres as carriers for drug delivery. Eur. J. Pharm. Biopharm. 2007, 67:67-75.
14. Fernandez R., Sarma V., Younkin E., Hirschl R.B., Ward P.A., Younger J.G. Exposure to perflubron is associated with decreased Syk phosphorylation in human neutrophils. J. Appl. Physiol. 2001, 91:1941-1947.
15. Fialkow L., Wang Y., Downey G.P. Reactive oxygen and nitrogen species as signaling molecules regulating neutrophil function. Free Radic. Biol. Med. 2007, 42:153-164.
16. Gonçalves C., Torrado E., Martins T., Pereira P., Pedrosa J., Gama M. Dextrin nanoparticles: studies on the interaction with murine macrophages and blood clearance. Colloid Surf. B - Biointerfaces 2010, 75:483-489.
17. 2) nanoparticles. Toxicol. In Vitro 2010, 24:1002-1008.
18. Goodman C., McCusker C., Yilmaz T., Rotello V. Toxicity of gold nanoparticles functionalized with cationic and anionic side chains. Bioconjugate Chem. 2004, 15:897-900.
19. Hartmann P., Szabó A., Erös G., Gurabi D., Horváth G., Németh I., Ghyczy M., Boros M. Anti-inflammatory effects of phosphatidylcholine in neutrophil leukocyte-dependent acute arthritis in rats. Eur. J. Pharmacol. 2009, 622:58-64.
20. Haslam G., Wyatt D., Kitos P.A. Estimating the number of viable animal cells in multi-well cultures based on their lactate dehydrogenase activities. Cytotechnology 2000, 32:63-75.
21. Hirsch J.G., Cohn Z.A. Degranulation of polymorphonuclear leucocytes following phagocytosis of microorganisms. J. Exp. Med. 1960, 112:1005-1014.
22. Huang C.C., Aronstam R.S., Chen D.R., Huang Y.W. Oxidative stress, calcium homeostasis, and altered gene expression in human lung epithelial cells exposed to ZnO nanoparticles. Toxicol. In Vitro 2009, 24:45-55.
23. Hung C.F., Chen J.K., Liao M.H., Lo H.M., Fang J.Y. Development and evaluation of emulsion-liposome blends for resveratrol delivery. J. Nanosci. Nanotechnol. 2006, 6:2950-2958.
24. Hwang T.L., Leu Y.L., Kao S.H., Tang M.C., Chang H.L. Viscolin, a new chalcone from Viscum coloratum, inhibits human neutrophil superoxide anion and elastase release via a cAMP-dependent pathway. Free Radic. Biol. Med. 2006, 41:1433-1441.
25. Hwang T.L., Lin Y.K., Chi C.H., Huang T.H., Fang J.Y. Development and evaluation of perfluorocarbon nanobubbles for apomorphine delivery. J. Pharm. Sci. 2009, 98:3735-3747.
26. Hwang T.L., Wang C.C., Kuo Y.H., Huang H.C., Wu Y.C., Kuo L.M., Wu Y.H. The hederagenin saponin SMG-1 is a natural FMLP receptor inhibitor that suppresses human neutrophil activation. Biochem. Pharmacol. 2010, 80:1190-1200.
27. Hwang T.L., Yeh S.H., Leu Y.L., Chern C.Y., Hsu H.C. Inhibition of superoxide anion and elastase release in human neutrophils by 3′-isopropoxychalcone via a cAMP-dependent pathway. Br. J. Pharmacol. 2006, 148:78-87.
28. Jing X.X., Wang Z.G., Ran H.T., Li L., Wu X., Li X.D., Peng X.Q., Yang C.J., Li X.S., Zhang Q.X. Evaluation of renal ischemia-reperfusion injury in rabbits using microbubbles targeted to activated neutrophils. Clin. Imaging 2008, 32:178-182.
29. Khatchadourian A., Maysinger D. Lipid droplets: their role in nanoparticle-induced oxidative stress. Mol. Pharm. 2009, 6:1125-1137.
30. Kim J.S., Yoon T.J., Yu K.N., Noh M.S., Woo M., Kim B.G., Lee K.H., Sohn B.H., Park S.B., Lee J.K., Cho M.H. Cellular uptake of magnetic nanoparticle is mediated through energy-dependent endocytosis in A549 cells. J. Vet. Sci. 2006, 7:321-326.
31. Lentacker I., Geers B., Demeester J., De Smedt S.C., Sanders N.N. Design and evaluation of doxorubicin-containing microbubbles for ultrasound-triggered doxorubicin delivery: cytotoxicity and mechanisms involved. Mol. Ther. 2010, 18:101-108.
32. Lewinski N., Colvin V., Drezek R. Cytotoxicity of nanoparticles. Small 2008, 4:26-49.
33. Lindner J.R., Song J., Xu F., Klibanov A.L., Singbartl K., Ley K., Kaul S. Noninvasive ultrasound imaging of inflammation using microbubbles targeted to activated leukocytes. Circulation 2000, 102:2745-2750.
34. Linkov I., Satterstrom F.K., Corey L.M. Nanotoxicology and nanomedicine: making hard decisions. Nanomed. - Nanotechnol. Biol. Med. 2008, 4:167-171.
35. Lin W.S., Huang Y.W., Zhou X.D., Ma Y.F. In vitro toxicity of silica nanoparticles in human lung cancer cells. Toxicol. Appl. Pharmacol. 2006, 217:252-259.
36. Liu Y., Miyoshi H., Nakamura M. Encapsulated ultrasound microbubbles: therapeutic application in drug/gene delivery. J. Control. Release 2006, 114:89-99.
37. Macdowell A.L., Peters S.P. Neutrophils in asthma. Curr. Allergy Asthma Rep. 2007, 7:464-468.
38. Mainardes R.M., Gremião M.P.D., Brunetti I.L., Fonseca L.M., Khalil N.M. Zidovudine-loaded PLA and PLA-PEG blend nanoparticles: influence of polymer type on phagocytic uptake by polymorphonuclear cells. J. Pharm. Sci. 2009, 98:257-267.
39. Medina C., Santos-Martinez M.J., Radomski A., Corrigan O.I., Radomski M.W. Nanoparticles: pharmacological and toxicological significance. Br. J. Pharmacol. 2007, 150:552-558.
40. Müller R.H., Rühl D., Runge S., Schulze-Forster K., Mehnert W. Cytotoxicity of solid lipid nanoparticles as a function of the lipid matrix and the surfactant. Pharm. Res. 1997, 14:458-462.
41. Narayan P., Marchant D., Wheatley M.A. Optimization of spray drying by factorial design for production of hollow microspheres for ultrasound imaging. J. Biomed. Mater. Res. 2001, 56:333-341.
42. Nel A., Xia T., Mädler L., Li N. Toxic potential of materials at the nanolevel. Science 2006, 311:622-627.
43. Owen C.A., Campbell M.A., Sannes P.L., Boukedes S.S., Campbell E.J. Cell surface-bound elastase and cathepsin G on human neutrophils: a novel, non-oxidative mechanism by which neutrophils focus and preserve catalytic activity of serine proteinases. J. Cell Biol. 1995, 131:775-789.
44. Pancholi K.P., Farook U., Moaleji R., Stride E., Edirisinghe M.J. Novel methods for preparing phospholipid coated microbubbles. Eur. Biophys. J. 2008, 37:515-520.
45. Pham C.T. Neutrophil serine proteases: specific regulators of inflammation. Microbes Infect. 2006, 5:1313-1327.
46. Qazi M.R., Bogdanska J., Butenhoff J.L., Nelson B.D., DePierre J.W., Abdel-Valugerdi M. High-dose, short-term exposure of mice to perfluorooctanesulfonate (PFOS) or perfluorooctanoate (PFOA) affects the number of circulating neutrophils differently, but enhances the inflammatory responses of macrophages to lipopolysaccharide (LPS) in a similar fashion. Toxicology 2009, 262:207-214.
47. Rapoport N., Gao Z., Kennedy A. Multifunctional nanoparticles for combining ultrasonic tumor imaging and targeted chemotherapy. J. Natl. Cancer Inst. 2007, 99:1095-1106.
48. Schoof E., von der Hardt K., Kandler M.A., Abendroth F., Papadopoulos T., Rascher W., Dötsch J. Aerosolized perfluorocarbon reduces adhesion molecule gene expression and neutrophil sequestration in acute respiratory distress. Eur. J. Pharmacol. 2002, 457:195-200.
49. Senda C., Nishinaka Y., Arai T., Segawa H., Mori H., Nonogawa M., Endo N., Miyoshi T., Yamashita K., Sasada M. Effects of injectable propofol emulsion on singlet oxygen released from activated human neutrophils and that chemically generated. J. Pharmacol. Sci. 2008, 107:460-464.
50. Service R.F. Nanotechnology grows up. Science 2004, 304:1732-1734.
51. Schöler N., Olbrich C., Tabatt K., Müller R.H., Hahn H., Liesenfeld O. Surfactant, but not the size of solid lipid nanoparticles (SLN) influences viability and cytokine production of macrophages. Int. J. Pharm. 2001, 221:57-67.
52. Shubayev V.I., Pisanic II T.R., Jin S. Magnetic nanoparticles for theragnostics. Adv. Drug Deliv. Rev. 2009, 61:467-477.
53. Tamura D.Y., Moore E.E., Patrick D.A., Johnson J.L., Zallen G., Silliman C.C. Primed neutrophils require phosphatidic acid for maximal receptor-activated elastase release. J. Surg. Res. 1998, 77:71-74.
54. Tan A.S., Berridge M.V. Superoxide produced by activated neutrophils efficiently reduces the tetrazolium salt, WST-1 to produce a soluble formazan: a simple colorimetric assay for measuring respiratory burst activation and for screening anti-inflammatory agents. J. Immunol. Methods 2000, 238:59-68.
55. Tinkov S., Bekeredjian R., Winter G., Loester C. Microbubbles as ultrasound triggered drug carriers. J. Pharm. Sci. 2009, 98:1935-1961.
56. Tronchère H., Planat V., Record M., Tercé F., Ribbes G., Chap H. Phosphatidylcholine turnover in activated human neutrophils. J. Biol. Chem. 1995, 270:13138-13146.
57. Unger E.C., Porter T., Culp W., Labell R., Matsunaga T., Zutshi R. Therapeutic applications of lipid-coated microbubbles. Adv. Drug Deliv. Rev. 2004, 56:1291-1314.
58. Wang F., Gao F., Lan M., Yuan H., Huang Y., Liu J. Oxidative stress contributes to silica nanoparticle-induced cytotoxicity in human embryonic kidney cells. Toxicol. In Vitro 2009, 23:808-815.
59. Wang J.J., Sung K.C., Hu O.Y.P., Yeh C.H., Fang J.Y. Submicron lipid emulsion as a drug delivery system for nalbuphine and its prodrugs. J. Control. Release 2006, 115:140-149.
60. 2+ mobilization by parenteral lipid emulsions in human neutrophils. J. Lipid Res. 2002, 43:550-556.
61. Witko-Sarsat V., Rieu P., Descamps-Latscha B., Lesavre P., Halbwachs-Mecarelli L. Neutrophils: molecules, functions and pathophysiological aspects. Lab. Invest. 2000, 80:617-653.
62. Zhao Y.Z., Liang H.D., Mei X.G., Halliwell M. Preparation, characterization and in vivo observation of phospholipid-based gas-filled microbubbles containing hirudin. Ultrasound Med. Biol. 2005, 31:1237-1243.