Plasticity of primary microglia on micropatterned geometries and spontaneous long-distance migration in microfluidic channels

BMC Neuroscience

Volumn 14, Issue , 2013, Pages

  Amadio, Susanna ^a   De Ninno, Adele ^b,c   Montilli, Cinzia ^a   Businaro, Luca ^b   Gerardino, Annamaria ^b   Volonté, Cinzia ^a  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c CNR   (Italy)

Author keywords

Confocal analysis; Long distance migration; Microfabrication; Microglia plasticity; Time lapse microscopy

Indexed keywords

DIMETICONE;

ANIMAL CELL; ARTICLE; BIOMIMETICS; CYTOPLASM; FILOPODIUM; GEOMETRY; MICROFLUIDICS; MICROGLIA; MORPHOLOGY; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; RAT; VELOCITY;

ANIMALS; CELL MOVEMENT; FLUORESCENT ANTIBODY TECHNIQUE; MICE; MICROFLUIDICS; MICROGLIA; MICROSCOPY, CONFOCAL; RATS;

EID: 84885368501     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-14-121     Document Type: Article

References (45)

1. del Rio-Hortega P. Microglia. Cytology and Cellular Pathology of the Nervous System 1932, 482-534. New York: Hoeber, Penfield W.
2. Nimmerjahn A, Kirchhoff F, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005, 308:1314-1318. 10.1126/science.1110647, 15831717.
3. Rezaie P, Male D. Colonisation of the developing human brain and spinal cord by microglia: a review. Microsc Res Tech 1999, 45:359-382. 10.1002/(SICI)1097-0029(19990615)45:6<359::AID-JEMT4>3.0.CO;2-D, 10402264.
4. Wake H, Moorhouse AJ, Nabekura J. Functions of microglia in the central nervous system-beyond the immune response. Neuron Glia Biol 2011, 7:47-53. 10.1017/S1740925X12000063, 22613055.
5. Ransohoff RM, Brown MA. Innate immunity in the central nervous system. J Clin Invest 2012, 122:1164-1171. 10.1172/JCI58644, 3314450, 22466658.
6. Greter M, Merad M. Regulation of microglia development and homeostasis. Glia 2013, 61:121-127. 10.1002/glia.22408, 22927325.
7. Hickey WF. Basic principles of immunological surveillance of the normal central nervous system. Glia 2001, 36:118-124. 10.1002/glia.1101, 11596120.
8. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB. ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 2005, 8:752-758. 10.1038/nn1472, 15895084.
9. 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.
10. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A. Physiology of microglia. Physiol Rev 2011, 91:461-553. 10.1152/physrev.00011.2010, 21527731.
11. Tremblay M, Stevens B, Sierra A, Wake H, Bessis A, Nimmerjahn A. The role of microglia in the healthy brain. J Neurosci 2011, 31:16064-16069. 10.1523/JNEUROSCI.4158-11.2011, 22072657.
12. Saijo K, Crotti A, Glass CK. Regulation of microglia activation and deactivation by nuclear receptors. Glia 2013, 61:104-111. 10.1002/glia.22423, 22987512.
13. El-Ali J, Sorger PK, Jensen KF. Cells on chips. Nature 2006, 442:403-411. 10.1038/nature05063, 16871208.
14. Zervantonakis IK, Hughes-Alford SK, Charest JL, Condeelis JS, Gertler FB, Kamm RD. Three-dimensional microfluidic model for tumor cell intravasation and endothelial barrier function. Proc Natl Acad Sci U S A 2012, 109:13515-13520. 10.1073/pnas.1210182109, 3427099, 22869695.
15. Kim BJ, Wu M. Microfluidics for mammalian cell chemotaxis. Ann Biomed Eng 2012, 40:1316-1327. 10.1007/s10439-011-0489-9, 3424276, 22189490.
16. Businaro L, De Ninno A, Schiavoni G, Lucarini V, Ciasca G, Gerardino A, Belardelli F, Gabriele L, Mattei F. Cross talk between cancer and immune cells: exploring complex dynamics in a microfluidic environment. Lab Chip 2013, 13:229-239. 10.1039/c2lc40887b, 23108434.
17. Taylor AM, Jeon NL. Microfluidic and compartmentalized platforms for neurobiological research. Crit Rev Biomed Eng 2011, 39:185-200. 10.1615/CritRevBiomedEng.v39.i3.20, 21967302.
18. Kim HJ, Park JW, Byun JH, Vahidi B, Rhee SW, Jeon NL. Integrated microfluidics platforms for investigating injury and regeneration of CNS axons. Ann Biomed Eng 2012, 40:1268-1276. 10.1007/s10439-012-0515-6, 22302320.
19. Persheyev S, Fan Y, Irving A, Rose MJ. BV-2 microglial cells sense micro-nanotextured silicon surface topology. J Biomed Mater Res A 2011, 99:135-140.
20. Hosmane S, Tegenge MA, Rajbhandari L, Uapinyoying P, Kumar NG, Thakor N, Venkatesan A. Toll/interleukin-1 receptor domain-containing adapter inducing interferon-β mediates microglial phagocytosis of degenerating axons. J Neurosci 2012, 32:7745-7757. 10.1523/JNEUROSCI.0203-12.2012, 3398425, 22649252.
21. Ransohoff RM, Perry VH. Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol 2009, 27:119-145. 10.1146/annurev.immunol.021908.132528, 19302036.
22. Tambuyzer BR, Ponsaerts P, Nouwen EJ. Microglia: gatekeepers of central nervous system immunology. J Leukocyte Biol 2009, 85:352-370.
23. Kreutzberg GW. Microglia: a sensor for pathological events in the CNS. Trends Neurosci 1996, 19:312-318. 10.1016/0166-2236(96)10049-7, 8843599.
24. D'Ambrosi N, Finocchi P, Apolloni S, Cozzolino M, Ferri A, Padovano V, Pietrini G, Carrì MT, Volonté C. The proinflammatory action of microglial P2 receptors is enhanced in SOD1 models for amyotrophic lateral sclerosis. J Immunol 2009, 183:4648-4656. 10.4049/jimmunol.0901212, 19734218.
25. Sasaki Y, Hoshi M, Akazawa C, Nakamura Y, Tsuzuki H, Inoue K, Kohsaka S. Selective expression of Gi/o-coupled ATP receptor P2Y12 in microglia in rat brain. Glia 2003, 44:242-250. 10.1002/glia.10293, 14603465.
26. Marín-Teva JL, Almendros A, Calvente R, Cuadros MA, Navascués J. Tangential migration of ameboid microglia in the developing quail retina: mechanism of migration and migratory behavior. Glia 1998, 22:31-52. 10.1002/(SICI)1098-1136(199801)22:1<31::AID-GLIA4>3.0.CO;2-B, 9436786.
27. Khatau SB, Hale CM, Stewart-Hutchinson PJ, Patel MS, Stewart CL, Searson PC, Hodzic D, Wirtz D. A perinuclear actin cap regulates nuclear shape. Proc Natl Acad Sci U S A 2009, 106:19017-19022. 10.1073/pnas.0908686106, 2776434, 19850871.
28. Ristanović D, Milosević NT, Stefanović BD, Marić DL, Rajković K. Morphology and classification of large neurons in the adult human dentate nucleus: a qualitative and quantitative analysis of 2D images. Neurosci Res 2010, 67:1-7. 10.1016/j.neures.2010.01.002, 20079774.
29. Ferrari D, Villalba M, Chiozzi P, Falzoni S, Ricciardi-Castagnoli P, Di Virgilio F. Mouse microglial cells express a plasma membrane pore gated by extracellular ATP. J Immunol 1996, 156:1531-1539.
30. Zhang J, Geula C, Lu C, Koziel H, Hatcher LM, Roisen FJ. Neurotrophins regulate proliferation and survival of two microglial cell lines in vitro. Exp Neurol 2003, 183:469-481. 10.1016/S0014-4886(03)00222-X, 14552887.
31. Ohsawa K, Imai Y, Nakajima K, Kohsaka S. Generation and characterization of a microglial cell line, MG5, derived from a p53-deficient mouse. Glia 1997, 21:285-298. 10.1002/(SICI)1098-1136(199711)21:3<285::AID-GLIA4>3.0.CO;2-4, 9383038.
32. Prinz M, Mildner A. Microglia in the CNS: immigrants from another world. Glia 2011, 59:177-187. 10.1002/glia.21104, 21125659.
33. Ousman SS, Kubes P. Immune surveillance in the central nervous system. Nat Neurosci 2012, 15:1096-1101. 10.1038/nn.3161, 22837040.
34. Carbonell WS, Murase SI, Horwitz AF, Mandell JW. Infiltrative microgliosis: activation and long-distance migration of subependymal microglia following periventricular insults. J Neuroinflammation 2005, 2:5. 10.1186/1742-2094-2-5, 548677, 15679892.
35. Lee S, Chung CY. Role of VASP phosphorylation for the regulation of microglia chemotaxis via the regulation of focal adhesion formation/maturation. Mol Cell Neurosci 2009, 42:382-390. 10.1016/j.mcn.2009.08.010, 19733667.
36. Karlstetter M, Lippe E, Walczak Y, Moehle C, Aslanidis A, Mirza M, Langmann T. Curcumin is a potent modulator of microglial gene expression and migration. J Neuroinflammation 2011, 8:125. 10.1186/1742-2094-8-125, 3192695, 21958395.
37. Honda S, Sasaki Y, Ohsawa K, Imai Y, Nakamura Y, Inoue K, Kohsaka S. Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J Neurosci 2001, 21:1975-1982.
38. Nasu-Tada K, Koizumi S, Inoue K. Involvement of beta1 integrin in microglial chemotaxis and proliferation on fibronectin: different regulations by ADP through PKA. Glia 2005, 52:98-107. 10.1002/glia.20224, 15920726.
39. Haynes SE, Hollopeter G, Yang G, Kurpius D, Dailey ME, Gan WB, Julius D. The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat Neurosci 2006, 9:1512-1519. 10.1038/nn1805, 17115040.
40. Whitesides GM. The origins and the future of microfluidics. Nature 2006, 442:368-373. 10.1038/nature05058, 16871203.
41. Qin D, Xia Y, Whitesides GM. Soft lithography for micro- and nanoscale patterning. Nat Protoc 2010, 5:491-502. 10.1038/nprot.2009.234, 20203666.
42. Hosmane S, Yang IH, Ruffin A, Thakor N, Venkatesan A. Circular compartmentalized microfluidic platform: Study of axon-glia interactions. Lab Chip 2010, 10:741-747. 10.1039/b918640a, 20221562.
43. Park JW, Vahidi B, Taylor AM, Rhee SW, Jeon NL. Microfluidic culture platform for neuroscience research. Nat Protoc 2006, 1:2128-2136. 10.1038/nprot.2006.316, 17487204.
44. Chen Y, Balasubramaniyan V, Peng J, Hurlock EC, Tallquist M, Li J, Lu QR. Isolation and culture of rat and mouse oligodendrocyte precursor cells. Nat Protoc 2007, 2:1044-1051. 10.1038/nprot.2007.149, 17546009.
45. Kozlowski C, Weimer RM. An automated method to quantify microglia morphology and application to monitor activation state longitudinally in vivo. PLoS One 2012, 7:e31814. 10.1371/journal.pone.0031814, 3294422, 22457705.