Microglia mechanics: Immune activation alters traction forces and durotaxis

Frontiers in Cellular Neuroscience

Volumn 9, Issue September, 2015, Pages 1-16

  Bollmann, Lars ^a,b   Koser, David E ^a,c,f   Shahapure, Rajesh ^a   Gautier, Hélène O B ^a   Holzapfel, Gerhard A ^b   Scarcelli, Giuliano ^d   Gather, Malte C ^e   Ulbricht, Elke ^a,g   Franze, Kristian ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^c UNIVERSITY OF COLOGNE   (Germany)

^d UNIVERSITY OF MARYLAND   (United States)

^e UNIVERSITY OF ST ANDREWS   (United Kingdom)

^f GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^g DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Biased random walk; CNS; Foreign body reaction; Gliosis; LPS; Mechanotaxis; Migration; Random walk

Indexed keywords

LIPOPOLYSACCHARIDE; POLYACRYLAMIDE;

ANIMAL CELL; ARTICLE; CELL TRACKING; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; IMMUNE RESPONSE; MATHEMATICAL MODEL; MICROGLIA; MOUSE; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; POLYMERIZATION; RAT; TIME LAPSE IMAGING;

EID: 84942893035     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2015.00363     Document Type: Article

References (59)

1. abd-el-Basset, E., and Fedoroff, S. (1995). Effect ofbacterial wall lipopolysaccharide (LPS) on morphology, motility, and cytoskeletal organization of microglia in cultures. J. Neurosci. Res. 41, 222-237. doi: 10.1002/jnr.490410210
2. Arani, A., Murphy, M. C., Glaser, K. J., Manduca, A., Lake, D. S., Kruse, S. A., et al. (2015). Measuring the effects of aging and sex on regional brain stiffness with MR elastography in healthy older adults. Neuroimage 111, 59-64. doi: 10.1016/j.neuroimage.2015.02.016
3. Bergert, M., Chandradoss, S. D., Desai, R. A., and Paluch, E. (2012). Cell mechanics control rapid transitions between blebs and lamellipodia during migration. Proc. Natl. Acad. Sci. U.S.A. 109, 14434-14439. doi: 10.1073/pnas.1207968109
4. Betz, T., Koch, D., Lu, Y. B., Franze, K., and Kas, J. A. (2011). Growth cones as soft and weak force generators. Proc. Natl. Acad. Sci. U.S.A. 108, 13420-13425. doi: 10.1073/pnas.1106145108
5. Bischofs, I. B., and Schwarz, U. S. (2003). Cell organization in soft media due to active mechanosensing. Proc. Natl. Acad. Sci. U.S.A. 100, 9274-9279. doi: 10.1073/pnas.1233544100
6. Califano, J. P., and Reinhart-King, C. A. (2010). Substrate stiffness and cell area predict cellular traction stresses in single cells and cells in contact. Cell Mol Bioeng. 3, 68-75. doi: 10.1007/s12195-010-0102-6
7. Chauvet, D., Imbault, M., Capelle, L., Demene, C., Mossad, M., Karachi, C., et al. (2015). In vivo measurement of Brain Tumor elasticity using intraoperative shear wave elastography. Ultraschall Med. doi: 10.1055/s-0034-1399152. [Epub ahead of print].
8. Christ, A. F., Franze, K., Gautier, H., Moshayedi, P., Fawcett, J., Franklin, R. J., et al. (2010). Mechanical difference between white and gray matter in the rat cerebellum measured by scanning force microscopy. J. Biomech. 43,2986-2992. doi: 10.1016/j.jbiomech.2010.07.002
9. Codling, E. A., Plank, M. J., and Benhamou, S. (2008). Random walk models in biology. J. R. Soc. Interface 5, 813-834. doi: 10.1098/rsif.2008.0014
10. Elkin, B. S., Azeloglu, E. U., Costa, K. D., and Morrison, B. III. (2007). Mechanical heterogeneity of the rat hippocampus measured by atomic force microscope indentation. J. Neurotrauma 24, 812-822. doi: 10.1089/neu.2006.0169
11. Engler, A. J., Griffin, M. A., Sen, S., Bonnemann, C. G., Sweeney, H. L., and Discher, D. E. (2004). Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J. Cell Biol. 166, 877-887. doi: 10.1083/jcb.200405004
12. Fournier, M. F., Sauser, R., Ambrosi, D., Meister, J. J., and Verkhovsky, A. B. (2010). Force transmission in migrating cells. J. Cell Biol. 188, 287-297. doi: 10.1083/jcb.200906139
13. Foxman, E. F., Kunkel, E. J., and Butcher, E. C. (1999). Integrating conflicting chemotactic signals. The role of memory in leukocyte navigation. J. Cell Biol. 147, 577-588. doi: 10.1083/jcb.147.3.577
14. Franze, K., Francke, M., Günter, K., Christ, A. F., Korber, N., Reichenbach, A., et al. (2011). Spatial mapping of the mechanical properties of the living retina using scanning force microscopy. Soft. Matter 7, 3147-3154. doi: 10.1039/c0sm01017k
15. Franze, K., Gerdelmann, J., Weick, M., Betz, T., Pawlizak, S., Lakadamyali, M., et al. (2009). Neurite branch retraction is caused by a threshold-dependent mechanical impact. Biophys. J. 97, 1883-1890. doi: 10.1016/j.bpj.2009.07.033
16. Franze, K., Janmey, P. A., and Guck, J. (2013). Mechanics in neuronal development and repair. Annu. Rev. Biomed. Eng. 15,227-251. doi: 10.1146/annurev-bioeng-071811-150045
17. Georges, P. C., Miller, W. J., Meaney, D. F., Sawyer, E. S., and Janmey, P. A. (2006). Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures. Biophys. J. 90, 3012-3018. doi: 10.1529/biophysj.105.073114
18. Ghibaudo, M., Saez, A., Trichet, L., Xayaphoummine, A., Browaeys, J., Silberzan, P., et al. (2008). Traction forces and rigidity sensing regulate cell functions. Soft Matter 4, 1836-1843. doi: 10.1039/b804103b
19. Giulian, D., and Baker, T. J. (1986). Characterization of ameboid microglia isolated from developing mammalian brain. J. Neurosci. 6, 2163-2178.
20. Grevesse, T., Versaevel, M., Circelli, G., Desprez, S., and Gabriele, S. (2013). A simple route to functionalize polyacrylamide hydrogels for the independent tuning of mechanotransduction cues. Lab. Chip. 13, 777-780. doi: 10.1039/c2lc41168g
21. Han, S. J., Bielawski, K. S., Ting, L. H., Rodriguez, M. L., and Sniadecki, N. J. (2012). Decoupling substrate stiffness, spread area, and micropost density: aclose spatial relationship between traction forces and focal adhesions. Biophys. J. 103, 640-648. doi: 10.1016/j.bpj.2012.07.023
22. He, W., and Bellamkonda, R. V. (2008). “A molecular perspective on understanding and modulating the performance of chronic central nervous system (CNS) recording electrodes” in Indwelling Neural Implants: Strategies for Contending with the In Vivo Environment, ed W. M. Reichert (Boca Raton, FL: CRC Press), 151-176.
23. Isenberg, B. C., Dimilla, P. A., Walker, M., Kim, S., and Wong, J. Y. (2009). Vascular smooth muscle cell durotaxis depends on substrate stiffness gradient strength. Biophys. J. 97, 1313-1322. doi: 10.1016/j.bpj.2009.06.021
24. Iwashita, M., Kataoka, N., Toida, K., and Kosodo, Y. (2014). Systematic profiling of spatiotemporal tissue and cellular stiffness in the developing brain. Development 141, 3793-3798. doi: 10.1242/dev.109637
25. Jagielska, A., Norman, A. L., Whyte, G., Vliet, K. J., Guck, J., and Franklin, R. J. (2012). Mechanical environment modulates biological properties of oligodendrocyte progenitor cells. Stem Cells Dev. 21, 2905-2914. doi: 10.1089/scd.2012.0189
26. Kettenmann, H., Hanisch, U. K., Noda, M., and Verkhratsky, A. (2011). Physiology of microglia. Physiol. Rev. 91, 461-553. doi: 10.1152/physrev.00011.2010
27. Kim, S. N., Jeibmann, A., Halama, K., Witte, H. T., Wolte, M., Matzat, T., et al. (2014). ECM stiffness regulates glial migration in Drosophila and mammalian glioma models. Development 141, 3233-3242. doi: 10.1242/dev.106039
28. Koch, D., Rosoff, W. J., Jiang, J., Geller, H. M., and Urbach, J. S. (2012). Strength in the periphery: growth cone biomechanics and substrate rigidity response in peripheral and central nervous system neurons. Biophys. J. 102, 452-460. doi: 10.1016/j.bpj.2011.12.025
29. Koser, D. E., Moeendarbary, E., Hanne, J., Kuerten, S., and Franze, K. (2015). CNS cell distribution and axon orientation determine local spinal cord mechanical properties. Biophys. J. 108, 2137-2147. doi: 10.1016/j.bpj.2015.03.039
30. Kuo, C. H., Xian, J., Brenton, J. D., Franze, K., and Sivaniah, E. (2012). Complex stiffness gradient substrates for studying mechanotactic cell migration. Adv. Mater. 24, 6059-6064. doi: 10.1002/adma.201202520
31. Lazopoulos, K. A., and Stamenovic, D. (2008). Durotaxis as an elastic stability phenomenon. J. Biomech. 41, 1289-1294. doi: 10.1016/j.jbiomech.2008.01.008
32. Liu, Y. J., Le Berre, M., Lautenschlaeger, F., Maiuri, P., Callan-Jones, A., Heuzé, M., et al. (2015). Confinement and low adhesion induce fast amoeboid migration of slow mesenchymal cells. Cell 160, 659-672. doi: 10.1016/j.cell.2015.01.007
33. Lively, S., and Schlichter, L. C. (2013). The microglial activation state regulates migration and roles of matrix-dissolving enzymes for invasion. J. Neuroinflammation 10,75. doi: 10.1186/1742-2094-10-75
34. Lo, C. M., Wang, H. B., Dembo, M., and Wang, Y. L. (2000). Cell movement is guided by the rigidity of the substrate. Biophys. J. 79, 144-152. doi: 10.1016/S0006-3495(00)76279-5
35. Lu, Y. B., Iandiev, I., Hollborn, M., Korber, N., Ulbricht, E., Hirrlinger, P. G., et al. (2011). Reactive glial cells: increased stiffness correlates with increased intermediate filament expression. FASEB J. 25, 624-631. doi: 10.1096/fj.10-163790
36. Marcq, P., Yoshinaga, N., and Prost, J. (2011). Rigidity sensing explained by active matter theory. Biophys. J. 101, L33-35. doi: 10.1016/j.bpj.2011.08.023
37. Mccarthy, K. D., and de Vellis, J. (1980). Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85, 890-902. doi: 10.1083/jcb.85.3.890
38. Mori, H., Takahashi, A., Horimoto, A., and Hara, M. (2013). Migration of glial cells differentiated from neurosphere-forming neural stem/progenitor cells depends on the stiffness of the chemically cross-linked collagen gel substrate. Neurosci. Lett. 555, 1-6. doi: 10.1016/j.neulet.2013.09.012
39. Moshayedi, P., Costa, L. D., Christ, A., Lacour, S. P., Fawcett, J., Guck, J., et al. (2010). Mechanosensitivity of astrocytes on optimized polyacrylamide gels analyzed by quantitative morphometry. J. Phys. Condens. Matter 22:194114. doi: 10.1088/0953-8984/1022/1019/194114
40. Moshayedi, P., Ng, G., Kwok, J. C., Yeo, G. S., Bryant, C. E., Fawcett, J. W., et al. (2014). The relationship between glial cell mechanosensitivity and foreign body reactions in the central nervous system. Biomaterials 35, 3919-3925. doi: 10.1016/j.biomaterials.2014.01.038
41. Murphy, M. C., Huston, J. III., Jack, C. R. Jr., Glaser, K. J., Manduca, A., Felmlee, J. P., et al. (2011). Decreased brain stiffness in Alzheimer’s disease determined by magnetic resonance elastography. J. Magn. Reson. Imaging 34, 494-498. doi: 10.1002/jmri.22707
42. Nakamura, Y. (2002). Regulating factors for microglial activation. Biol. Pharm. Bull. 25, 945-953. doi: 10.1248/bpb.25.945
43. Plotnikov, S. V., Pasapera, A. M., Sabass, B., and Waterman, C. M. (2012). Force fluctuations within focal adhesions mediate ECM-rigidity sensing to guide directed cell migration. Cell 151, 1513-1527. doi: 10.1016/j.cell.2012.11.034
44. Raab, M., Swift, J., Dingal, P. C., Shah, P., Shin, J. W., and Discher, D. E. (2012). Crawling from soft to stiff matrix polarizes the cytoskeleton and phosphoregulates myosin-II heavy chain. J. Cell Biol. 199, 669-683. doi: 10.1083/jcb.201205056
45. Riek, K., Millward, J. M., Hamann, I., Mueller, S., Pfueller, C. F., Paul, F., et al. (2012). Magnetic resonance elastography reveals altered brain viscoelasticity in experimental autoimmune encephalomyelitis. NeuroImage Clin. 1, 81-90. doi: 10.1016/j.nicl.2012.09.003
46. Sabass, B., Gardel, M. L., Waterman, C. M., and Schwarz, U. S. (2008). High resolution traction force microscopy based on experimental and computational advances. Biophys. J. 94, 207-220. doi: 10.1529/biophysj.107.113670
47. Sack, I., Streitberger, K. J., Krefting, D., Paul, F., and Braun, J. (2011). The influence of physiological aging and atrophy on brain viscoelastic properties in humans. PLoS ONE 6:e23451. doi: 10.1371/journal.pone.0023451
48. Schregel, K., Wuerfel, E., Garteiser, P., Gemeinhardt, I., Prozorovski, T., Aktas, O., et al. (2012). Demyelination reduces brain parenchymal stiffness quantified in vivo by magnetic resonance elastography. Proc. Natl. Acad. Sci. U.S.A. 109, 6650-6655. doi: 10.1073/pnas.1200151109
49. Schwarz, U. S., Erdmann, T., and Bischofs, I. B. (2006). Focal adhesions as mechanosensors: the two-spring model. Biosystems 83, 225-232. doi: 10.1016/j.biosystems.2005.05.019
50. Solon, J., Levental, I., Sengupta, K., Georges, P. C., and Janmey, P. A. (2007). Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys. J. 93, 4453-4461. doi: 10.1529/biophysj.106.101386
51. Streitberger, K. J., Sack, I., Krefting, D., Pfüller, C., Braun, J., Paul, F., et al. (2012). Brain viscoelasticity alteration in chronic-progressive multiple sclerosis. PLoS ONE7:e29888. doi: 10.1371/journal.pone.0029888
52. Stricker, J., Falzone, T., and Gardel, M. L. (2010). Mechanics of the F-actin cytoskeleton. J. Biomech. 43, 9-14. doi: 10.1016/j.jbiomech.2009.09.003
53. Style, R. W., Che, Y., Park, S. J., Weon, B. M., Je, J. H., Hyland, C., et al. (2013). Patterning droplets with durotaxis. Proc. Natl. Acad. Sci. U.S.A. 110, 12541-12544. doi: 10.1073/pnas.1307122110
54. Tolic-Norrelykke, I. M., and Wang, N. (2005). Traction in smooth muscle cells varies with cell spreading. J. Biomech. 38, 1405-1412. doi: 10.1016/j.jbiomech.2004.06.027
55. Tresco, P. A., and Winslow, B. D. (2011). The challenge of integrating devices into the central nervous system. Crit. Rev. Biomed. Eng. 39, 29-44. doi: 10.1615/CritRevBiomedEng.v39.i1.30
56. Trichet, L., Le Digabel, J., Hawkins, R. J., Vedula, S. R., Gupta, M., Ribrault, C., et al. (2012). Evidence of a large-scale mechanosensing mechanism for cellular adaptation to substrate stiffness. Proc. Natl. Acad. Sci. U.S.A. 109, 6933-6938. doi: 10.1073/pnas.1117810109
57. Uhlemann, R., Gertz, K., Boehmerle, W., Schwarz, T., Nolte, C., Freyer, D., et al. (2015). Actin dynamics shape microglia effector functions. Brain Struct. Funct. doi: 10.1007/s00429-015-1067-y. [Epub ahead of print]
58. Vincent, L. G., Choi, Y. S., Alonso-Latorre, B., del álamo, J. C., and Engler, A. J. (2013). Mesenchymal stem cell durotaxis depends on substrate stiffness gradient strength. Biotechnol. J. 8, 472-484. doi: 10.1002/biot.201200205
59. Zemel, A., Rehfeldt, F., Brown, A. E., Discher, D. E., and Safran, S. A. (2010). Optimal matrix rigidity for stress-fibre polarization in stem cells. Nat. Phys. 6, 468-473. doi: 10.1038/nphys1613