Magnetic nanoparticles in primary neural cell cultures are mainly taken up by microglia

BMC Neuroscience

Volumn 13, Issue 1, 2012, Pages

  Pinkernelle, Josephine ^a   Calatayud, Pilar ^b   Goya, Gerado F ^b   Fansa, Hisham ^c   Keilhoff, Gerburg ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b UNIVERSITY OF ZARAGOZA   (Spain)

^c Klinikum Bielefeld   (Germany)

Author keywords

Magnetic nanoparticles; Microglia; Organotypic spinal cord; Primary neuronal cells

Indexed keywords

NANOPARTICLE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CELL COUNT; CELL LINE; CELL STRAIN; CELL TYPE; COCULTURE; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; ENDOCYTOSIS; IMMUNE SYSTEM; MACROGLIA; MICROGLIA; NERVE CELL CULTURE; NERVE GRAFT; NONHUMAN; PHAGOCYTOSIS; RAT; SCHWANN CELL; SPINAL CORD; ANIMAL; CELL CULTURE; CYTOLOGY; MAGNETISM; NERVE CELL;

ANIMALS; CELLS, CULTURED; COCULTURE TECHNIQUES; MAGNETICS; MICROGLIA; MICROSCOPY, CONFOCAL; NANOPARTICLES; NEURONS; PC12 CELLS; RATS;

EID: 84858732725     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-13-32     Document Type: Article

References (60)

1. Li W, Chen C, Ye C, Wei T, Zhao Y, Lao F, Chen Z, Meng H, Gao Y, Yuan H, Xing G, Zhao F, Chai Z, Zhang X, Yang F, Han D, Tang X, Zhang Y. The translocation of fullerenic nanoparticles into lysosome via the pathway of clathrin-mediated endocytosis. Nanotechnol 2008, 19:145102.
2. Shi H, He X, Yuan Y, Wang K, Liu D. Nanoparticle-based biocompatible and long-life marker for lysosome labelling and tracking. Anal Chem 2010, 82:2213-2220. 10.1021/ac902417s, 20155925.
3. Pankhurst QA, Connolly J, Jones SK, Dobson J. Applications of magnetic nanoparticles in biomedicine. J Phys D-Appl Phys 2003, 36:R167-R181.
4. Gupta AK, Gupta M. Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials 2005, 26:3995-4021. 10.1016/j.biomaterials.2004.10.012, 15626447.
5. Suh WH, Suslick KS, Stucky GD, Suh Y-H. Nanotechnology, nanotoxicology, and neuroscience. Prog Neurobiol 2009, 87:133-170. 10.1016/j.pneurobio.2008.09.009, 2728462, 18926873.
6. Sudimack J, Lee RJ. Targeted drug delivery via the folate receptor. Adv Drug Deliv Rev 2000, 41:147-162. 10.1016/S0169-409X(99)00062-9, 10699311.
7. Darius J, Meyer FP, Sabel BA, Schroeder U. Influence of nanoparticles on the brain-to-serum distribution and the metabolism of valproic acid in mice. J Pharm Pharmacol 2000, 52:1043-1047.
8. Chertok B, Moffat BA, David AE, Yu F, Bergemann C, Ross BD, Yang VC. Iron oxide nanoparticles as a drug delivery vehicle for MRI monitored magnetic targeting of brain. Biomaterials 2008, 29:487-496. 10.1016/j.biomaterials.2007.08.050, 2761681, 17964647.
9. Thiesen B, Jordan A. Clinical applications of magnetic nanoparticles for hyperthermia. Int J Hyperthermia 2008, 24:467-474. 10.1080/02656730802104757, 18608593.
10. Scherer F, Anton M, Schillinger U, Henke J, Bergemann C, Krüger A, Gänsbacher B, Plank C. Magnetofection: enhancing and targeting gene delivery by magnetic force in vitro and in vivo. Gene Ther 2002, 9:102-109. 10.1038/sj.gt.3301624, 11857068.
11. Cooper DR, Nadau JL. Nanotechnology for in vitro neuroscience. Nanoscale 2009, 1:183-200. 10.1039/b9nr00132h, 20644838.
12. McDonald JW, Sadowsky C. Spinal-cord injury. Lancet 2002, 359:417-425. 10.1016/S0140-6736(02)07603-1, 11844532.
13. Yegiyants S, Dayicioglu D, Kardashian G, Panthaki ZJ. Traumatic peripheral nerve injury: a wartime review. J Craniofac Surg 2010, 21:998-1001. 10.1097/SCS.0b013e3181e17aef, 20613581.
14. Stoll G, Griffin JW, Li CY, Trapp BD. Wallerian degeneration in the peripheral nervous system: participation of both Schwann cells and macrophages in myelin degradation. J Neurocytol 1989, 18:671-683. 10.1007/BF01187086, 2614485.
15. Vargas ME, Barres BA. Why is Wallerian degeneration in the CNS so slow?. Annu Rev Neurosci 2007, 30:153-179. 10.1146/annurev.neuro.30.051606.094354, 17506644.
16. Mittnacht U, Hartmann H, Hein S, Oliveira H, Dong M, Pêgo AP, Kjems J, Howard KA, Schlosshauer B. Chitosan/siRNA nanoparticles biofunctionalize nerve implants and enable neurite outgrowth. Nano Lett 2010, 10:3933-3939. 10.1021/nl1016909, 20795625.
17. Hamasaki T, Tanaka N, Kamei N, Ishida O, Yanada S, Nakanishi K, Nishida K, Oishi Y, Kawamata S, Sakai N, Ochi M. Magnetically labelled neural progenitor cells, which are localized by magnetic force, promote axon growth in organotypic cocultures. Spine 2007, 32:2300-2305. 10.1097/BRS.0b013e318154c651, 17906569.
18. Pisanic TR, Blackwell JD, Shubayev VI, Finones RR, Jin S. Nanotoxicity of iron oxide nanoparticle internalization in growing neurons. Biomaterials 2007, 28:2572-2581. 10.1016/j.biomaterials.2007.01.043, 17320946.
19. Häfeli UO, Riffle JS, Harris-Shekhawat L, Carmichael-Baranauskas A, Mark F, Dailey JP, Bardenstein D. Cell uptake and in vitro toxicity of magnetic nanoparticles suitable for drug delivery. Mol Pharm 2009, 6:1417-1428. 10.1021/mp900083m, 19445482.
20. Gupta AK, Curtis ASG. Surface modified superparamagnetic nanoparticles for drug delivery: Interaction studies with human fibroblasts in culture. J Mater Sci Mater Med 2004, 15:493-496.
21. Wilkening S, Stahl F, Bader A. Comparison of primary human hepatocytes and hepatoma cell line HEPG2 with regard to their biotransformation properties. Drug Metab Dispos 2003, 31:1035-1042. 10.1124/dmd.31.8.1035, 12867492.
22. Pan C, Kumar C, Bohl S, Klingmueller U, Mann M. Comparative proteomic phenotyping of cell lines and primary cells to assess preservation of cell type-specific functions. Mol Cell Proteomics 2009, 8:443-450. 10.1074/mcp.M800258-MCP200, 2649808, 18952599.
23. Thangnipon W, Kingsbury A, Webb M, Balazs R. Observations on rat cerebellar cells in vitro: influence of substratum, potassium concentration and relationship between neurones and astrocytes. Dev Brain Res 1983, 11:177-189.
24. Polazzi E, Gianni T, Contestabile A. Microglial cells protect cerebellar granule neurons from apoptosis: evidence for reciprocal signaling. Glia 2001, 36:271-280. 10.1002/glia.1115, 11746765.
25. Levi G, Aloisi F, Wilkin GP. Differentiation of cerebellar bipotential glial precursors into oligodendrocytes in primary culture: developmental profile of surface antigens and mitotic activity. J Neurosci Res 1987, 18:407-417. 10.1002/jnr.490180305, 3437464.
26. Aloisi F, Agresti C, D'Urso D, Levi G. Differentiation of bipotential glial precursors into oligodendrocytes is promoted by interaction with type-1 astrocytes in cerebellar cultures. Proc Natl Acad Sci 1988, 85:6167-6171. 10.1073/pnas.85.16.6167, 281926, 3413085.
27. Bernstein H-G, Keilhoff G, Bukowska A, Ziegeler A, Funke S, Dobrowolny H, Kanakis D, Bogerts B, Lendeckel U. ADAM (a disintegrin and metalloprotease) 12 is expressed in rat and human brain and localized to oligodendrocytes. J Neurosci Res 2004, 75:353-360. 10.1002/jnr.10858, 14743448.
28. Vyas A, Li Z, Aspalter M, Feiner J, Hoke A, Zhou C, O'Daly A, Abdullah M, Rohde C, Brushart TM. An in vitro model of adult mammalian nerve repair. Exp Neurol 2010, 223:112-118. 10.1016/j.expneurol.2009.05.022, 2849894, 19464291.
29. Kroll A, Pillukat MH, Hahn D, Schnekenburger J. Current in vitro methods in nanoparticle risk assessment: Limitations and challenges. Eur J Pharm Biopharm 2009, 72:370-377. 10.1016/j.ejpb.2008.08.009, 18775492.
30. Mailänder V, Landfester K. Interaction of nanoparticles with cells. Biomacromolecules 2009, 10:2379-2400. 10.1021/bm900266r, 19637907.
31. Roy S, Johnston AH, Newman TA, Glueckert R, Dudas J, Bitsche M, Corbacell E, Rieger G, Martini A, Schrott-Fischer A. Cell-specific targeting in the mouse inner ear using nanoparticles conjugated with a neurotropin-derived peptide ligand: Potential tool for drug delivery. Int J Pharm 2010, 390:214-224. 10.1016/j.ijpharm.2010.02.003, 20153412.
32. Hussain SM, Javorina AK, Schrand AM, Duhart HM, Ali SF, Schlager JJ. The interaction of manganese nanoparticles with PC-12 cells induces dopamine depletion. Toxicol Sci 2006, 92:456-463. 10.1093/toxsci/kfl020, 16714391.
33. Pickard MR, Chari DM. Robust uptake of Magnetic Nanoparticles (MNPs) by Central Nervous System (CNS) microglia: Implications for particle uptake in mixed neural cell populations. Int J Mol Sci 2010, 11:967-981. 10.3390/ijms11030967, 2869227, 20479995.
34. Geppert M, Hohnholt MC, Thiel K, Nürnberger S, Grunwald I, Rezwan K, Dringen R. Uptake of dimercaptosuccinate-coated magnetic iron oxide nanoparticles by cultured brain astrocytes. Nanotechnology 2011, 22:145101-145111. 10.1088/0957-4484/22/14/145101, 21346306.
35. Jenkins SI, Pickard MR, Granger N, Chari DM. Magnetic nanoparticle-mediated gene transfer to oligodendrocyte precursor cell transplant populations is enhanced by magnetofection strategies. ACS Nano 2011, 8:6527-6538.
36. Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 2007, 10:1387-1394. 10.1038/nn1997, 17965659.
37. Ponomarev ED, Shriver LP, Maresz K, Dittel BN. Microglial cell activation and proliferation precedes the onset of CNS autoimmunity. J Neurosci Res 2005, 81:374-389. 10.1002/jnr.20488, 15959904.
38. Baloui H, Stettler O, Weiss S, Nothias F, Boxberg Y. Upregulation in rat spinal cord microglia of the nonintegrin laminin receptor 37 kDa-LRP following activation by a traumatic lesion or peripheral injury. J Neurotrauma 2009, 26:195-207. 10.1089/neu.2008.0677, 19196078.
39. 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. PNAS 2008, 105:14265-14270. 10.1073/pnas.0805135105, 2567179, 18809927.
40. Owens DE, Peppas NA. Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. Int J Pharm 2006, 307:93-102. 10.1016/j.ijpharm.2005.10.010, 16303268.
41. Nel AE, Mädler L, Velegol D, Xia T, Hoek EMV, Somasundaran P, Klaessig F, Castranova V, Thompson M. Understanding biophysicochemical interactions at the nano-bio interface. Nat Mater 2009, 8:543-557. 10.1038/nmat2442, 19525947.
42. Suzumura A, Marunouchi T, Yamamoto H. Morphological transformation of microglia in vitro. Brain Res 1991, 545:301-306. 10.1016/0006-8993(91)91302-H, 1907214.
43. Aloisi F, de Simone R, Columba-Cabezas S, Levi G. Opposite effects of Interferon-γ and Prostaglandin E2 on Tumor Necrosis Factor and Interleukin-10 production in microglia: A regulatory loop controlling microglia pro-and anti-inflammatory activities. J Neurosci Res 1999, 56:571-580. 10.1002/(SICI)1097-4547(19990615)56:6<571::AID-JNR3>3.0.CO;2-P, 10374812.
44. Noske W, Lentzen H, Lange K, Keller K. Phagocytotic activity of glial cells in culture. Exp Cell Res 1982, 142:437-445. 10.1016/0014-4827(82)90385-8, 6293852.
45. Triarhou LC, Del Cerro M, Herndon RM. Ultrastructural evidence for phagocytosis by oligodendroglia. Neurosci Lett 1985, 53:185-189. 10.1016/0304-3940(85)90183-1, 3982706.
46. Saito H, Tomioka H, Sato K, Watanabe T. Abilities of human oligodendroglial cells and mouse Schwann cells to phagocytose Mycobacterium leprae and other mycobacteria. Infect Immun 1986, 51:157-162. 261079, 3510165.
47. Tansey FA, Cammer W. Differential uptake of dextran beads by astrocytes, macrophages and oligodendrocytes in mixed glial-cell cultures from brains of neonatal rats. Neurosci Lett 1998, 248:159-162. 10.1016/S0304-3940(98)00373-5, 9654333.
48. Unfried K, Albrecht C, Klotz L-O, Mikecz A, Grether-Beck S, Schins RPF. Cellular responses to nanoparticles: Target structures and mechanisms. Nanotoxicology 2007, 1:52-71.
49. Chen Z-L, Yu W-M, Strickland S. Peripheral regeneration. Annu Rev Neurosci 2007, 30:209-233. 10.1146/annurev.neuro.30.051606.094337, 17341159.
50. Bigbee JW, Yoshino JE, DeVries GH. Morphological and proliferative responses of cultured Schwann cells following rapid phagocytosis of a myelin-enriched fraction. J Neurocytol 1987, 16:487-496. 10.1007/BF01668503, 3681350.
51. Arlein WJ, Shearer JD, Caldwell MD. Continuity between wound macrophage and fibroblast phenotype: analysis of wound fibroblast phagocytosis. Am J Physiol Regul Integr Comp Physiol 1998, 275:R1041-R1048.
52. Abraham LC, Dice JF, Lee K, Kaplan DL. Phagocytosis and remodelling of collagen matrices. Exp Cell Res 2007, 313:1045-1055. 10.1016/j.yexcr.2006.12.019, 2700050, 17276428.
53. Berry CC, Wells S, Charles S, Curtis ASG. Dextran and albumin derivatised iron oxide nanoparticles: influence on fibroblasts in vitro. Biomaterials 2003, 24:4551-4557. 10.1016/S0142-9612(03)00237-0, 12950997.
54. Dunning MD, Lakatos A, Loizou L, Kettunen M, ffrench-Constant C, Brindle KM, Franklin RJM. Superparamagnetic iron oxide-labeled Schwann cells and olfactory ensheating cells can be traced in vivo by magnetic resonance imaging and retain functional properties after transplantation into the CNS. J Neurosci 2004, 24:9799-9810. 10.1523/JNEUROSCI.3126-04.2004, 15525765.
55. Luciani N, Gazeau F, Wilhelm C. Reactivity of the monocyte/macrophage system to superparamagnetic anionic nanoparticles. J Mater Chem 2009, 19:6373-6380.
56. Gupta AK, Gupta M. Cytotoxicity suppression and cellular uptake enhancement of surface modified magnetic nanoparticles. Biomaterials 2005, 26:1565-1573. 10.1016/j.biomaterials.2004.05.022, 15522758.
57. Karlsson HL, Gustafsson J, Cronholm P, Möller L. Size-dependent toxicity of metal oxide particles - A comparison between nano- and micrometer size. Toxicol Lett 2009, 188:112-118. 10.1016/j.toxlet.2009.03.014, 19446243.
58. Patel PC, Giljohann DA, Daniel WL, Zheng D, Prigodich AE, Mirkin CA. Scavenger receptors mediate cellular uptake of polyvalent oligonucleotide-functionalized gold nanoparticles. Bioconjug Chem 2010, 21:2250-2256. 10.1021/bc1002423, 3241523, 21070003.
59. Nativo P, Prior IA, Brust M. Uptake and intracellular fate of surface-modified gold nanoparticles. ACS Nano 2008, 2:1639-1644. 10.1021/nn800330a, 19206367.
60. Fansa H, Schneider W, Wolf G, Keilhoff G. Influence of insulin-like growth factor-I (IGF-I) on nerve autografts and tissue-engineered nerve grafts. Muscle Nerve 2002, 26:87-93. 10.1002/mus.10165, 12115953.