Involvement of aquaporin-4 in astroglial cell migration and glial scar formation

Samira Saadoun; Marios C. Papadopoulos; Hiroyuki Watanabe; Donghong Yan; Geoffrey T. Manley; A. S. Verkman

doi:10.1242/jcs.02680

journal article Dec 15, 2005

Involvement of aquaporin-4 in astroglial cell migration and glial scar formation

Samira Saadoun Marios C. Papadopoulos Hiroyuki Watanabe

Donghong Yan Geoffrey T. Manley A. S. Verkman

Journal of Cell Science Vol. 118 No. 24 pp. 5691-5698 · The Company of Biologists

View at Publisher Save 10.1242/jcs.02680

Abstract

Aquaporin-4, the major water-selective channel in astroglia throughout the central nervous system, facilitates water movement into and out of the brain. Here, we identify a novel role for aquaporin-4 in astroglial cell migration, as occurs during glial scar formation. Astroglia cultured from the neocortex of aquaporin-4-null mice had similar morphology, proliferation and adhesion, but markedly impaired migration determined by Transwell migration efficiency (18±2 vs 58±4% of cells migrated towards 10% serum in 8 hours; P&lt;0.001) and wound healing rate (4.6 vs 7.0 μm/hour speed of wound edge; P&lt;0.001) compared with wild-type mice. Transwell migration was similarly impaired (25±4% migrated cells) in wild-type astroglia after ∼90% reduction in aquaporin-4 protein expression by RNA inhibition. Aquaporin-4 was polarized to the leading edge of the plasma membrane in migrating wild-type astroglia, where rapid shape changes were seen by video microscopy. Astroglial cell migration was enhanced by a small extracellular osmotic gradient, suggesting that aquaporin-4 facilitates water influx across the leading edge of a migrating cell. In an in vivo model of reactive gliosis and astroglial cell migration produced by cortical stab injury, glial scar formation was remarkably impaired in aquaporin-4-null mice, with reduced migration of reactive astroglia towards the site of injury. Our findings provide evidence for the involvement of aquaporin-4 in astroglial cell migration, which occurs during glial scar formation in brain injury, stroke, tumor and focal abscess.

Topics

No keywords indexed for this article. Browse by subject →

References

42

[1]

Anderson, J. L. (1983). Movement of a semipermeable vesicle through an osmotic gradient. Phys. Fluids26, 2871-2879. 10.1063/1.864051

[2]

Bloch, O., Papadopoulos, M. C., Manley, G. T. and Verkman, A. S. (2005). Aquaporin-4 gene disruption in mice increases focal edema associated with staphylococcal brain abscess. J. Neurochem.95, 354-262.

[3]

Bush, T. G., Puvanachandra, N., Horner, C. H., Polito, A., Ostenfeld, T., Svendsen, C. N., Mucke, L., Johnson, M. H. and Sofroniew, M. V. (1999). Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron23, 297-308. 10.1016/s0896-6273(00)80781-3

[4]

Localized glucose and water influx facilitatesCryptosporidium parvumcellular invasion by means of modulation of host-cell membrane protrusion

Xian-Ming Chen, Steven P. O'Hara, Bing Q. Huang et al.

Proceedings of the National Academy of Sciences 10.1073/pnas.0408563102

[5]

Condeelis, J., Bresnick, A., Demma, M., Dharmawardhane, S., Eddy, R., Hall, A. L., Sauterer, R. and Warren, V. (1990). Mechanisms of amoeboid chemotaxis: an evaluation of the cortical expansion model. Dev. Genet.11, 333-340. 10.1002/dvg.1020110504

[6]

Eng, L. F., Ghirnikar, R. S. and Lee, Y. L. (2000). Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochem. Res.25, 1439-1451. 10.1023/a:1007677003387

[7]

Reactive Astrocytes Protect Tissue and Preserve Function after Spinal Cord Injury

Jill R. Faulkner, Julia E. Herrmann, Michael J. Woo et al.

The Journal of Neuroscience 10.1523/jneurosci.3547-03.2004

[8]

Fawcett, J. W. and Asher, R. A. (1999). The glial scar and central nervous system repair. Brain Res. Bull.49, 377-391. 10.1016/s0361-9230(99)00072-6

[9]

Hampton, D. W., Rhodes, K. E., Zhao, C., Franklin, R. J. and Fawcett, J. W. (2004). The responses of oligodendrocyte precursor cells, astrocytes and microglia to a cortical stab injury, in the brain. Neuroscience127, 813-820. 10.1016/j.neuroscience.2004.05.028

[10]

Huttenlocher, A. (2005). Cell polarization mechanisms during directed cell migration. Nat. Cell Biol.7, 336-337. 10.1038/ncb0405-336

[11]

Jaeger, M., Carin, M., Medale, M. and Tryggvason, G. (1999). The osmotic migration of cells in a solute gradient. Biophys. J.77, 1257-1267. 10.1016/s0006-3495(99)76977-8

[12]

Kinouchi, R., Takeda, M., Yang, L., Wilhelmsson, U., Lundkvist, A., Pekny, M. and Chen, D. F. (2003). Robust neural integration from retinal transplants in mice deficient in GFAP and vimentin. Nat. Neurosci.6, 863-868. 10.1038/nn1088

[13]

Klein, M., Seeger, P., Schuricht, B., Alper, S. L. and Schwab, A. (2000). Polarization of Na(+)/H(+) and Cl(–)/HCO (3)(–) exchangers in migrating renal epithelial cells. J. Gen. Physiol.115, 599-608. 10.1085/jgp.115.5.599

[14]

Lurie, D. I. and Rubel, E. W. (1994). Astrocyte proliferation in the chick auditory brainstem following cochlea removal. J. Comp. Neurol.346, 276-288. 10.1002/cne.903460207

[15]

Ma, T., Yang, B., Gillespie, A., Carlson, E. J., Epstein, C. J. and Verkman, A. S. (1997). Generation and phenotype of a transgenic knockout mouse lacking the mercurial-insensitive water channel aquaporin-4. J. Clin. Invest.100, 957-962. 10.1172/jci231

[16]

Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke

Geoffrey T. Manley, Miki Fujimura, Tonghui Ma et al.

Nature Medicine 10.1038/72256

[17]

McGraw, J., Hiebert, G. W. and Steeves, J. D. (2001). Modulating astrogliosis after neurotrauma. J. Neurosci. Res.63, 109-115. 10.1002/1097-4547(20010115)63:2<109::aid-jnr1002>3.0.co;2-j

[18]

Nicchia, G. P., Frigeri, A., Liuzzi, G. M., Santacroce, M. P., Nico, B., Procino, G., Quondamatteo, F., Herken, R., Roncali, L. and Svelto, M. (2000). Aquaporin-4-containing astrocytes sustain a temperature- and mercury-insensitive swelling in vitro. Glia31, 29-38. 10.1002/(sici)1098-1136(200007)31:1<29::aid-glia30>3.0.co;2-3

[19]

Nicchia, G. P., Frigeri, A., Liuzzi, G. M. and Svelto, M. (2003). Inhibition of aquaporin-4 expression in astrocytes by RNAi determines alteration in cell morphology, growth, and water transport and induces changes in ischemia-related genes. FASEB J.17, 1508-1510.

[20]

Nielsen, S., Nagelhus, E. A., Amiry-Moghaddam, M., Bourque, C., Agre, P. and Ottersen, O. P. (1997). Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J. Neurosci.17, 171-180. 10.1523/jneurosci.17-01-00171.1997

[21]

Nona, S. N., Duncan, A., Stafford, C. A., Maggs, A., Jeserich, G. and Cronly-Dillon, J. R. (1992). Myelination of regenerated axons in goldfish optic nerve by Schwann cells. J. Neurocytol.21, 391-401. 10.1007/bf01191504

[22]

Oster, G. F. and Perelson, A. S. (1987). The physics of cell motility. J. Cell Sci.8, 35-54. 10.1242/jcs.1987.supplement_8.3

[23]

Papadopoulos, M. C. and Verkman, A. S. (2005). Aquaporin-4 gene disruption in mice reduces brain swelling and mortality in pneumococcal meningitis. J. Biol. Chem.280, 13906-13912. 10.1074/jbc.m413627200

[24]

Papadopoulos, M. C., Manley, G. T., Krishna, S. and Verkman, A. S. (2004). Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J.18, 1291-1293. 10.1096/fj.04-1723fje

[25]

Pekny, M. and Nilsson, M. (2005). Astrocyte activation and reactive gliosis. Glia50, 427-434. 10.1002/glia.20207

[26]

Rhodes, K. E., Moon, L. D. and Fawcett, J. W. (2003). Inhibiting cell proliferation during formation of the glial scar: effects on axon regeneration in the CNS. Neuroscience120, 41-56. 10.1016/s0306-4522(03)00285-9

[27]

Romero-Aleman, M. M., Monzon-Mayor, M., Yanes, C. and Lang, D. (2004). Radial glial cells, proliferating periventricular cells, and microglia might contribute to successful structural repair in the cerebral cortex of the lizard Gallotia galloti. Exp. Neurol.188, 74-85. 10.1016/j.expneurol.2004.03.014

[28]

Saadoun, S., Papadopoulos, M. C., Davies, D. C., Krishna, S. and Bell, B. A. (2002). Aquaporin-4 expression is increased in oedematous human brain tumours. J. Neurol. Neurosurg. Psychiatry72, 262-265. 10.1136/jnnp.72.2.262

[29]

Saadoun, S., Papadopoulos, M. C. and Krishna, S. (2003). Water transport becomes uncoupled from K+ siphoning in brain contusion, bacterial meningitis, and brain tumours: immunohistochemical case review. J. Clin. Pathol.56, 972-975. 10.1136/jcp.56.12.972

[30]

Saadoun, S., Papadopoulos, M. C., Hara-Chikuma, M. and Verkman, A. S. (2005). Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature434, 786-792. 10.1038/nature03460

[31]

Small, J. V., Stradal, T., Vignal, E. and Rottner, K. (2002). The lamellipodium: where motility begins. Trends Cell. Biol.12, 112-120. 10.1016/s0962-8924(01)02237-1

[32]

Smith, P. J., Howes, E. A. and Treherne, J. E. (1987). Mechanisms of glial regeneration in an insect central nervous system. J. Exp. Biol.132, 59-78. 10.1242/jeb.132.1.59

[33]

Smith, T. G., Jr, Lange, G. D. and Marks, W. B. (1996). Fractal methods and results in cellular morphology – dimensions, lacunarity and multifractals. J. Neurosci. Methods69, 123-136. 10.1016/s0165-0270(96)00080-5

[34]

Solenov, E., Watanabe, H., Manley, G. T. and Verkman, A. S. (2004). Sevenfold-reduced osmotic water permeability in primary astrocyte cultures from AQP-4-deficient mice, measured by a fluorescence quenching method. Am. J. Physiol. Cell Physiol.286, C426-C432. 10.1152/ajpcell.00298.2003

[35]

Svitkina, T. M. and Borisy, G. G. (1999). Progress in protrusion: the tell-tale scar. Trends Biochem. Sci.24, 432-436. 10.1016/s0968-0004(99)01461-9

[36]

Tomas-Camardiel, M., Venero, J. L., de Pablos, R. M., Rite, I., Machado, A. and Cano, J. (2004). In vivo expression of aquaporin-4 by reactive microglia. J. Neurochem.91, 891-899. 10.1111/j.1471-4159.2004.02759.x

[37]

Vizuete, M. L., Venero, J. L., Vargas, C., Ilundain, A. A., Echevarria, M., Machado, A. and Cano, J. (1999). Differential upregulation of aquaporin-4 mRNA expression in reactive astrocytes after brain injury: potential role in brain edema. Neurobiol. Dis.6, 245-258. 10.1006/nbdi.1999.0246

[38]

Wang, K., Bekar, L. K., Furber, K. and Walz, W. (2004). Vimentin-expressing proximal reactive astrocytes correlate with migration rather than proliferation following focal brain injury. Brain Res.1024, 193-202. 10.1016/j.brainres.2004.07.086

[39]

Wujek, J. R. and Reier, P. J. (1984). Astrocytic membrane morphology: differences between mammalian and amphibian astrocytes after axotomy. J. Comp. Neurol.222, 607-619. 10.1002/cne.902220411

[40]

Yang, B. and Verkman, A. S. (1997). Water and glycerol permeabilities of aquaporins 1-5 and MIP determined quantitatively by expression of epitope-tagged constructs in Xenopus oocytes. J. Biol. Chem.272, 16140-16146. 10.1074/jbc.272.26.16140

[41]

Zhou, C. F., Lawrence, J. M., Morris, R. J. and Raisman, G. (1986). Migration of host astrocytes into superior cervical sympathetic ganglia autografted into the septal nuclei or choroid fissure of adult rats. Neuroscience17, 815-827. 10.1016/0306-4522(86)90047-3

[42]

Zinemanas, D. and Nir, A. (1995). Osmophoretic motion of deformable particles. Int. J. Multiphase Flow21, 787-800. 10.1016/0301-9322(95)00009-m

Cited By

410

Super-resolution imaging of aquaporin-4 orthogonal arrays of particles in cell membranes

Andrea Rossi, Tobias J. Moritz · 2012

Journal of Cell Science

Metrics

410

Citations

42

References

Details

Published: Dec 15, 2005
Vol/Issue: 118(24)
Pages: 5691-5698

Authors

S

Samira Saadoun

Departments of Medicine and Physiology, Cardiovascular Research Institute, University of California, 505 Parnassus Avenue, San Francisco, CA 94143-0521, USA; Academic Neurosurgery Unit, St George's University of London, Cranmer Terrace, London, SW17 0RE, UK

M

Marios C. Papadopoulos

Departments of Medicine and Physiology, Cardiovascular Research Institute, University of California, 505 Parnassus Avenue, San Francisco, CA 94143-0521, USA; Academic Neurosurgery Unit, St George's University of London, Cranmer Terrace, London, SW17 0RE, UK

H

Hiroyuki Watanabe

Department of Neurological Surgery, University of California, 1001 Potrero Avenue, San Francisco, CA 94110, USA

D

Donghong Yan

Department of Neurological Surgery, University of California, 1001 Potrero Avenue, San Francisco, CA 94110, USA

G

Geoffrey T. Manley

Department of Neurological Surgery, University of California, 1001 Potrero Avenue, San Francisco, CA 94110, USA

A

A. S. Verkman

Departments of Medicine and Physiology, Cardiovascular Research Institute, University of California, 505 Parnassus Avenue, San Francisco, CA 94143-0521, USA

Cite This Article

Samira Saadoun, Marios C. Papadopoulos, Hiroyuki Watanabe, et al. (2005). Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. Journal of Cell Science, 118(24), 5691-5698. https://doi.org/10.1242/jcs.02680

Involvement of aquaporin-4 in astroglial cell migration and glial scar formation

You May Also Like