Microglial migration and interactions with dendrimer nanoparticles are altered in the presence of neuroinflammation

Journal of Neuroinflammation

Volumn 13, Issue 1, 2016, Pages

  Zhang, Fan ^a,b   Nance, Elizabeth ^a,d   Alnasser, Yossef ^a   Kannan, Rangaramanujam ^a,c   Kannan, Sujatha ^a,c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Johns Hopkins University   (United States)

^c KENNEDY KRIEGER INSTITUTE   (United States)

^d University of Washington   (United States)

Author keywords

Cell migration; Dendrimer; Inflammation; Microglia; Morphology

Indexed keywords

DENDRIMER; NANOPARTICLE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INTERACTION; CELL MIGRATION; CELL STRUCTURE; CELL TRANSPORT; CEREBRAL PALSY; CONTROLLED STUDY; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NEWBORN; NONHUMAN; PRENATAL PERIOD; VELOCITY; ANIMAL; BRAIN; CELL MOTION; CHEMICALLY INDUCED; CYTOLOGY; DRUG EFFECTS; FEMALE; INFLAMMATION; ORGAN CULTURE TECHNIQUE; PATHOLOGY; PREGNANCY; RABBIT; ULTRASTRUCTURE;

ANIMALS; ANIMALS, NEWBORN; BRAIN; CELL MOVEMENT; DENDRIMERS; FEMALE; INFLAMMATION; MICROGLIA; NANOPARTICLES; ORGAN CULTURE TECHNIQUES; PREGNANCY; RABBITS;

EID: 84977495378     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-016-0529-3     Document Type: Article

References (49)

1. Kreutzberg GW. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 1996;19(8):312-8. doi: 10.1016/0166-2236(96)10049-7.
2. Stoll G, Jander S. The role of microglia and macrophages in the pathophysiology of the CNS. Prog Neurobiol. 1999;58(3):233-47. doi: 10.1016/S0301-0082(98)00083-5.
3. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A. Physiology of microglia. Physiol Rev. 2011;91(2):461-553. doi: 10.1152/physrev.00011.2010.
4. Nimmerjahn A, Kirchhoff F, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science. 2005;308(5726):1314-8. doi: 10.1126/science.1110647.
5. Stence N, Waite M, Dailey ME. Dynamics of microglial activation: a confocal time-lapse analysis in hippocampal slices. Glia. 2001;33(3):256-66.
6. Nolte C, Moller T, Walter T, Kettenmann H. Complement 5a controls motility of murine microglial cells in vitro via activation of an inhibitory G-protein and the rearrangement of the actin cytoskeleton. Neuroscience. 1996;73(4):1091-107. doi: 1016/0306-4522(96)00106-6.
7. Loane DJ, Byrnes KR. Role of microglia in neurotrauma. Neurotherapeutics. 2010;7(4):366-77. doi: 10.1016/j.nurt.2010.07.002.
8. Mannix RC, Whalen MJ. Traumatic brain injury, microglia, and beta amyloid. Int J Alzheimers Dis. 2012;2012:608732. doi: 10.1155/2012/608732.
9. Lively S, Schlichter LC. The microglial activation state regulates migration and roles of matrix-dissolving enzymes for invasion. J Neuroinflammation. 2013;10:75. doi: 10.1186/1742-2094-10-75.
10. Orr AG, Orr AL, Li XJ, Gross RE, Traynelis SF. Adenosine A(2A) receptor mediates microglial process retraction. Nat Neurosci. 2009;12(7):872-U84. doi: 10.1038/Nn.2341.
11. De Simone R, Niturad CE, De Nuccio C, Ajmone-Cat MA, Visentin S, Minghetti L. TGF-beta and LPS modulate ADP-induced migration of microglial cells through P2Y1 and P2Y12 receptor expression. J Neurochem. 2010;115(2):450-9. doi: 10.1111/J.1471-4159.2010.06937.X.
12. Brown GC, Neher JJ. Microglial phagocytosis of live neurons. Nat Rev Neurosci. 2014;15(4):209-16. doi: 10.1038/nrn3710.
13. Biber K, Owens T, Boddeke E. What is microglia neurotoxicity (not)? Glia. 2014;62(6):841-54. doi: 10.1002/Glia.22654.
14. Hellwig S, Heinrich A, Biber K. The brain's best friend: microglial neurotoxicity revisited. Front. Cell Neurosci. 2013;16(7):71.
15. Indaram M, Ma W, Zhao L, Fariss RN, Rodriguez IR, Wong WT. 7-Ketocholesterol increases retinal microglial migration, activation, and angiogenicity: a potential pathogenic mechanism underlying age-related macular degeneration. Sci Rep. 2015;5:9144. doi: 10.1038/srep09144.
16. Kannan S, Dai H, Navath RS, Balakrishnan B, Jyoti A, Janisse J, et al. Dendrimer-based postnatal therapy for neuroinflammation and cerebral palsy in a rabbit model. Sci Transl Med. 2012;4(130):130ra46. doi: 10.1126/scitranslmed.3003162.
17. Lesniak WG, Mishra MK, Jyoti A, Balakrishnan B, Zhang F, Nance E, et al. Biodistribution of fluorescently labeled PAMAM dendrimers in neonatal rabbits: effect of neuroinflammation. Mol Pharm. 2013;10(12):4560-71. doi: 10.1021/mp400371r.
18. Saadani-Makki F, Kannan S, Lu X, Janisse J, Dawe E, Edwin S, et al. Intrauterine administration of endotoxin leads to motor deficits in a rabbit model: a link between prenatal infection and cerebral palsy. Am J Obstet Gynecol. 2008;199(6):Artn 651.E1. doi: 10.1016/J.Ajog.2008.06.090.
19. Kannan S, Saadani-Makki F, Balakrishnan B, Chakraborty P, Janisse J, Lu X, et al. Magnitude of [C-11]PK11195 binding is related to severity of motor deficits in a rabbit model of cerebral palsy induced by intrauterine endotoxin exposure. Dev Neurosci-Basel. 2011;33(3-4):231-40. doi: 10.1159/000328125.
20. Nance EA, Woodworth GF, Sailor KA, Shih TY, Xu QG, Swaminathan G, et al. A dense poly(ethylene glycol) coating improves penetration of large polymeric nanoparticles within brain tissue. Sci Transl Med. 2012;4(149):ARTN 149ra119. doi: 10.1126/scitranslmed.3003594.
21. Rao SM, Lin ZL, Drobyshevsky A, Chen LN, Ji XH, Ji HT, et al. Involvement of neuronal nitric oxide synthase in ongoing fetal brain injury following near-term rabbit hypoxia-ischemia. Dev Neurosci. 2011;33(3-4):288-98. doi: 10.1159/000327241.
22. Su T, Paradiso B, Long YS, Liao WP, Simonato M. Evaluation of cell damage in organotypic hippocampal slice culture from adult mouse: a potential model system to study neuroprotection. Brain Res. 2011;1385:68-76. doi: 10.1016/j.brainres.2011.01.115.
23. Kannan S, Saadani-Makki F, Muzik O, Chakraborty P, Mangner TJ, Janisse J, et al. Microglial activation in perinatal rabbit brain induced by intrauterine inflammation: detection with 11C-(R)-PK11195 and small-animal PET. Journal of nuclear medicine. 2007;48(6):946-54. doi: 10.2967/jnumed.106.038539.
24. Fraley SI, Feng Y, Krishnamurthy R, Kim DH, Celedon A, Longmore GD, et al. A distinctive role for focal adhesion proteins in three-dimensional cell motility. Nat Cell Biol. 2010;12(6):598-604. doi: 10.1038/ncb2062.
25. Noraberg J, Kristensen BW, Zimmer J. Markers for neuronal degeneration in organotypic slice cultures. Brain Res Protoc. 1999;3:278-290.
26. Tamashiro TT, Dalgard CL, Byrnes KR. Primary microglia isolation from mixed glial cell cultures of neonatal rat brain tissue. Journal of visualized experiments. 2012;66:e3814. doi: 10.3791/3814.
27. Smithpeter CL, Dunn AK, Welch AJ, Richards-Kortum R. Penetration depth limits of in vivo confocal reflectance imaging. Appl Optics. 1998;37(13):2749-54.
28. Dailey ME, Eyo U, Fuller L, Hass J, Kurpius D. Imaging microglia in brain slices and slice cultures. Cold Spring Harb Protoc. 2013;2013(12):1142-8. doi: 10.1101/pdb.prot079483.
29. Dailey ME, Waite M. Confocal imaging of microglial cell dynamics in hippocampal slice cultures. Methods. 1999;18(2):222-30. doi: 10.1006/meth.1999.0775. 177.
30. Cho S, Wood A, Bowby MR. Brain slices as models for neurodegenerative disease and screening platforms to identify novel therapeutics. Current neuropharmacology. 2007;5(1):19-33. doi: 10.2174/157015907780077105.
31. van Rossum D, Hanisch UK. Microglia. Metab Brain Dis. 2004;19(3-4):393-411.
32. Carbonell WS, Murase S, Horwitz AF, Mandell JW. Migration of perilesional microglia after focal brain injury and modulation by CC chemokine receptor 5: an in situ time-lapse confocal imaging study. Journal of neuroscience. 2005;25(30):7040-7. doi: 10.1523/JNEUROSCI.5171-04.2005.
33. Sieger D, Moritz C, Ziegenhals T, Prykhozhij S, Peri F. Long-range Ca2+ waves transmit brain-damage signals to microglia. Dev Cell. 2012;22(6):1138-48. doi: 10.1016/j.devcel.2012.04.012.
34. Dibaj P, Nadrigny F, Steffens H, Scheller A, Hirrlinger J, Schomburg ED, et al. NO mediates microglial response to acute spinal cord injury under ATP control in vivo. Glia. 2010;58(9):1133-44. doi: 10.1002/Glia.20993.
35. Petersen MA, Dailey ME. Diverse microglial motility behaviors during clearance of dead cells in hippocampal slices. Glia. 2004;46(2):195-206. doi: 10.1002/glia.10362.
36. Liu HC, Zheng MH, Du YL, Wang L, Kuang F, Qin HY, et al. N9 microglial cells polarized by LPS and IL4 show differential responses to secondary environmental stimuli. Cell Immunol. 2012;278(1-2):84-90. doi: 10.1016/J.Cellimm.2012.06.001.
37. Chhor V, Le Charpentier T, Lebon S, Ore MV, Celador IL, Josserand J, et al. Characterization of phenotype markers and neuronotoxic potential of polarised primary microglia in vitro. Brain Behav Immun. 2013;32:70-85. doi: 10.1016/j.bbi.2013.02.005.
38. Block ML, Zecca L, Hong JS. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci. 2007;8(1):57-69. doi: 10.1038/nrn2038.
39. Chang WK, Carmona-Fontaine C, Xavier JB. Tumour-stromal interactions generate emergent persistence in collective cancer cell migration. Interface focus. 2013;3(4):20130017. doi: 10.1098/rsfs.2013.0017.
40. Dujardin DL, Barnhart LE, Stehman SA, Gomes ER, Gundersen GG, Vallee RB. A role for cytoplasmic dynein and LIS1 in directed cell movement. J Cell Biol. 2003;163(6):1205-11. doi: 10.1083/jcb.200310097.
41. Danen EHJ, van Rheenen J, Franken W, Huveneers S, Sonneveld P, Jalink K, et al. Integrins control motile strategy through a Rho-cofilin pathway. Journal of Cell Biology. 2005;169(3):515-26. doi: 10.1083/jcb.200412081.
42. Weiner OD. Regulation of cell polarity during eukaryotic chemotaxis: the chemotactic compass. Curr Opin Cell Biol. 2002;14(2):196-202. doi: 10.1016/S0955-0674(02)00310-1.
43. Milner R, Campbell IL. The integrin family of cell adhesion molecules has multiple functions within the CNS. J Neurosci Res. 2002;69(3):286-91. doi: 10.1002/Jnr.10321.
44. Milner R, Campbell IL. The extracellular matrix and cytokines regulate microglial integrin expression and activation. J Immunol. 2003;170(7):3850-8.
45. 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(3):967-81. doi: 10.3390/ijms11030967.
46. Kambhampati SP, Clunies-Ross AJ, Bhutto I, Mishra MK, Edwards M, McLeod DS, et al. Systemic and intravitreal delivery of dendrimers to activated microglia/macrophage in ischemia/reperfusion mouse retina. Invest Ophthalmol Vis Sci. 2015;56(8):4413-24. doi: 10.1167/iovs.14-16250.
47. Zhang F, Mastorakos P, Mishra MK, Mangraviti A, Hwang L, Zhou J, et al. Uniform brain tumor distribution and tumor associated macrophage targeting of systemically administered dendrimers. Biomaterials. 2015;52:507-16. doi: 10.1016/j.biomaterials.2015.02.053.
48. Hayder M, Varilh M, Turrin CO, Saoudi A, Caminade AM, Poupot R, et al. Phosphorus-based dendrimer ABP treats neuroinflammation by promoting IL-10-producing CD4 T cells. Biomacromolecules. 2015. doi:10.1021/acs.biomac.5b00643
49. Boridy S, Soliman GM, Maysinger D. Modulation of inflammatory signaling and cytokine release from microglia by celastrol incorporated into dendrimer nanocarriers. Nanomedicine (Lond). 2012;7(8):1149-65. doi: 10.2217/nnm.12.16.