The Age of Cortical Neural Networks Affects Their Interactions with Magnetic Nanoparticles
Andy Tay
Department of Bioengineering, University of California, Los Angeles, CA, 90095 USA
Department of Biomedical Engineering, National University of Singapore, 4 Engineering Drive 3, Singapore, 117583 Singapore
Search for more papers by this authorAnja Kunze
Department of Bioengineering, University of California, Los Angeles, CA, 90095 USA
Search for more papers by this authorDukwoo Jun
Department of Civil and Environmental Engineering, University of California, Los Angeles, CA, 90095 USA
Search for more papers by this authorEric Hoek
Department of Civil and Environmental Engineering, University of California, Los Angeles, CA, 90095 USA
Search for more papers by this authorCorresponding Author
Dino Di Carlo
Department of Bioengineering, University of California, Los Angeles, CA, 90095 USA
California Nanosystems Institute, University of California, Los Angeles, CA, 90095 USA
Jonsson Comprehensive Cancer Center, University of California, Los Angeles, CA, 90095 USA
E-mail: [email protected]Search for more papers by this authorAndy Tay
Department of Bioengineering, University of California, Los Angeles, CA, 90095 USA
Department of Biomedical Engineering, National University of Singapore, 4 Engineering Drive 3, Singapore, 117583 Singapore
Search for more papers by this authorAnja Kunze
Department of Bioengineering, University of California, Los Angeles, CA, 90095 USA
Search for more papers by this authorDukwoo Jun
Department of Civil and Environmental Engineering, University of California, Los Angeles, CA, 90095 USA
Search for more papers by this authorEric Hoek
Department of Civil and Environmental Engineering, University of California, Los Angeles, CA, 90095 USA
Search for more papers by this authorCorresponding Author
Dino Di Carlo
Department of Bioengineering, University of California, Los Angeles, CA, 90095 USA
California Nanosystems Institute, University of California, Los Angeles, CA, 90095 USA
Jonsson Comprehensive Cancer Center, University of California, Los Angeles, CA, 90095 USA
E-mail: [email protected]Search for more papers by this authorAbstract
Despite increasing use of nanotechnology in neuroscience, the characterization of interactions between magnetic nanoparticles (MNPs) and primary cortical neural networks remains underdeveloped. In particular, how the age of primary neural networks affects MNP uptake and endocytosis is critical when considering MNP-based therapies for age-related diseases. Here, primary cortical neural networks are cultured up to 4 weeks and with CCL11/eotaxin, an age-inducing chemokine, to create aged neural networks. As the neural networks are aged, their association with membrane-bound starch-coated ferromagnetic nanoparticles (fMNPs) increases while their endocytic mechanisms are impaired, resulting in reduced internalization of chitosan-coated fMNPs. The age of the neurons also negates the neuroprotective effects of chitosan coatings on fMNPs, attributing to decreased intracellular trafficking and increased colocalization of MNPs with lysosomes. These findings demonstrate the importance of age and developmental stage of primary neural cells when developing in vitro models for fMNP therapeutics targeting age-related diseases.
Supporting Information
As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer reviewed and may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors.
Filename | Description |
---|---|
smll201600673-sup-0001-S1.pdf572 KB | Supplementary |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1G. A. Silva, Nat. Rev. Neurosci. 2006, 7, 65.
- 2A. Tay, A. Kunze, C. Murray, D. Di Carlo, ACS Nano 2016, 10, 2331.
- 3Y. Wong, K. Markham, Z. P. Xu, M. Chen, G. Q. M. Lu, P. F. Bartlett, H. M. Cooper, Biomaterials 2010, 31, 8770.
- 4L. Hasadsri, J. Kreuter, H. Hattori, T. Iwasaki, J. M. George, J. Biol. Chem. 2009, 284, 6972.
- 5Y. Cho, R. Shi, R. B. Borgens, J. Biol. Eng. 2010, 4, 2.
- 6A. Cardoso, P. Costa, L. De Almeida, S. Simoes, N. Plesnila, C. Culmsee, E. Wagner, M. P. de Lima, J. Controlled Release 2010, 142, 392.
- 7I.-D. Kim, C.-M. Lim, J.-B. Kim, H. Y. Nam, K. Nam, S.-W. Kim, J.-S. Park, J.-K. Lee, J. Controlled Release 2010, 142, 422.
- 8B. D. Chithrani, W. C. Chan, Nano Lett. 2007, 7, 1542.
- 9L. K. Limbach, Y. Li, R. N. Grass, T. J. Brunner, M. A. Hintermann, M. Muller, D. Gunther, J. Stark, Environ. Sci. Technol. 2005, 39, 9370.
- 10K. Zheng, L. Bard, J. P. Reynolds, C. King, T. P. Jensen, A. V. Gourine, D. A. Rusakov, Neuron 2015, 88, 277.
- 11D. E. Berman, Y. Dudai, Science 2001, 291, 2417.
- 12T. Hedden, J. D. Gabrieli, Nat. Rev. Neurosci. 2004, 5, 87.
- 13M. P. Mattson, T. Magnus, Nat. Rev. Neurosci. 2006, 7, 278.
- 14R. Chen, G. Romero, M. G. Christiansen, A. Mohr, P. Anikeeva, Science 2015, 347, 1477.
- 15H. Huang, S. Delikanli, H. Zeng, D. M. Ferkey, A. Pralle, Nat. Nanotechnol. 2010, 5, 602.
- 16J. Dobson, Gene Ther. 2006, 13, 283.
- 17M. Arruebo, R. Fernández- Pacheco, M. R. Ibarra, J. Santamaría, Nano Today 2007, 2, 22.
- 18K. R. Ospina, S. Parada, C. Lapuente, A. E. Céspedes, Rev. Colomb. Cienc. Anim. 2015, 7, 21.
- 19N. M. Porter, O. Thibault, V. Thibault, K.-C. Chen, P. W. Landfield, J. Neurosci. 1997, 17, 5629.
- 20S. A. Villeda, J. Luo, K. I. Mosher, B. Zou, M. Britschgi, G. Bieri, T. M. Stan, N. Fainberg, Z. Ding, A. Eggel, Nature 2011, 477, 90.
- 21M. Z. Adzemovic, J. Ockinger, M. Zeitelhofer, S. Hochmeister, A. D. Beyeen, A. Paulson, A. Gillett, M. Thessen Hedreul, R. Covacu, H. Lassmann, PLoS One 2012, 7, e39794.
- 22A. D. Fryer, L. H. Stein, Z. Nie, D. E. Curtis, C. M. Evans, S. T. Hodgson, P. J. Jose, K. E. Belmonte, E. Fitch, D. B. Jacoby, J. Clin. Invest. 2006, 116, 228.
- 23H. Wang, E. S. Wittchen, Y. Jiang, B. Ambati, H. E. Grossniklaus, M. E. Hartnett, Invest. Ophthalmol. Visual Sci. 2011, 52, 8271.
- 24S. Maysami, D. Nguyen, F. Zobel, S. Heine, M. Höpfner, M. Stangel, J. Neuroimmunol. 2006, 178, 17.
- 25D. A. Wainwright, J. Xin, N. A. Mesnard, T. R. Beahrs, C. M. Politis, V. M. Sanders, K. J. Jones, ASN Neuro 2009, 1, AN20090017.
- 26B. Parajuli, H. Horiuchi, T. Mizuno, H. Takeuchi, A. Suzumura, Glia 2015, 63, 2274.
- 27S. B. Dumanis, J. A. Tesoriero, L. W. Babus, M. T. Nguyen, J. H. Trotter, M. J. Ladu, E. J. Weeber, R. S. Turner, B. Xu, G. W. Rebeck, J. Neurosci. 2009, 29, 15317.
- 28S. Baloyannis, J. Neurol. Sci. 2009, 283, 153.
- 29R. G. Perez, H. Zheng, L. H. Van der Ploeg, E. H. Koo, J. Neurosci. 1997, 17, 9407.
- 30M.Llorens- Martin, A.Fuster- Matanzo, C. Teixeira, J.Jurado- Arjona, F. Ulloa, A. Rábano, F.Herná ndez, E. Soriano, J. Ávila, Mol. Psychiatry 2013, 18, 451.
- 31S. N. Burke, C. A. Barnes, Nat. Rev. Neurosci. 2006, 7, 30.
- 32J. D. Grill, D. R. Riddle, Brain Res. 2002, 937, 8.
- 33J. De Brabander, R. Kramers, H. Uylings, Eur. J. Neurosci. 1998, 10, 1261.
- 34H. B. Uylings, J. De Brabander, Brain Cognit. 2002, 49, 268.
- 35V. A. Alvarez, B. L. Sabatini, Annu. Rev. Neurosci. 2007, 30, 79.
- 36P. Penzes, M. E. Cahill, K. A. Jones, J.-E. VanLeeuwen, K. M. Woolfrey, Nat. Neurosci. 2011, 14, 285.
- 37R. Mostany, J. E. Anstey, K. L. Crump, B. Maco, G. Knott, C. Portera- Cailliau, J. Neurosci. 2013, 33, 4094.
- 38A. Kunze, P. Tseng, C. Godzich, C. Murray, A. Caputo, F. E. Schweizer, D. Di Carlo, ACS Nano 2015, 9, 3664.
- 39T. Linemann, L. B. Thomsen, K. G. d. Jardin, J. C. Laursen, J. B. Jensen, J. Lichota, T. Moos, Pharmaceutics 2013, 5, 246.
- 40A. Obermeier, S. Kuchler, F. Matl, T. Pirzer, A. Stemberger, O. Mykhaylyk, W. Friess, R. Burgkart, J. Biomater. Sci., Polym. Ed. 2012, 23, 2321.
- 41A. Pala, M. Liberatore, P. D' Elia, F. Nepi, V. Megna, M. Mastantuono, A. Al- Nahhas, D. Rubello, M. Barteri, Mol. Imaging Biol. 2012, 14, 593.
- 42C. A. Ruge, U. F. Schaefer, J. Herrmann, J. Kirch, O. Canadas, M. Echaide, J. Pérez-Gil, C. Casals, R. Mü ller, C.-M. Lehr, 2012, PLoS One 7, e40775.
- 43P. Tseng, D. Di Carlo, J. W. Judy, Nano Lett. 2009, 9, 3053.
- 44X. Wang, N. Chi, X. Tang, Eur. J. Pharm. Biopharm. 2008, 70, 735.
- 45M. Malhotra, C. Tomaro- Duchesneau, S. Prakash, Biomaterials 2013, 34, 1270.
- 46D. K. Kim, M. Mikhaylova, F. H. Wang, J. Kehr, B. Bjelke, Y. Zhang, T. Tsakalakos, M. Muhammed, Chem. Mater. 2003, 15, 4343.
- 47A. Lesniak, F. Fenaroli, M. P. Monopoli, C. Åberg, K. A. Dawson, A. Salvati, ACS Nano 2012, 6, 5845.
- 48C. He, Y. Hu, L. Yin, C. Tang, C. Yin, Biomaterials 2010, 31, 3657.
- 49T. Dos Santos, J. Varela, I. Lynch, A. Salvati, K. A. Dawson, Small 2011, 7, 3341.
- 50T. A. Blanpied, D. B. Scott, M. D. Ehlers, Neuron 2002, 36, 435.
- 51J. A. Allen, R. A. Halverson- Tamboli, M. M. Rasenick, Nat. Rev. Neurosci. 2007, 8, 128.
- 52L. M. Bareford, P. W. Swaan, Adv. Drug Delivery Rev. 2007, 59, 748.
- 53P. Dannhauser, M. Platen, H. Böning, I. Schaap, Nat. Nanotechnol. 2015.
- 54O. Harush- Frenkel, E. Rozentur, S. Benita, Y. Altschuler, Biomacromolecules 2008, 9, 435.
- 55K. Shapero, F. Fenaroli, I. Lynch, D. C. Cottell, A. Salvati, K. A. Dawson, Mol. BioSyst. 2011, 7, 371.
- 56A. Salvati, C. Åberg, T. dos Santos, J. Varela, P. Pinto, I. Lynch, K. A. Dawson, Nanomedicine 2011, 7, 818.
- 57S. Gunawardena, Pharm. Res. 2013, 30, 2459.
- 58T. R. Pisanic, J. D. Blackwell, V. I. Shubayev, R. R. Fiñones, S. Jin, Biomaterials 2007, 28, 2572.
- 59P. Thevenaz, U. E. Ruttimann, M. Unser, IEEE Trans. Image Process. 1998, 7, 27.
- 60K. Jaqaman, D. Loerke, M. Mettlen, H. Kuwata, S. Grinstein, S. L. Schmid, G. Danuser, Nat. Methods 2008, 5, 695.
- 61P. H. Reddy, U. P. Shirendeb, Biochim. Biophys. Acta, Mol. Basis Dis. 2012, 1822, 101.