3,369
Views
12
CrossRef citations to date
0
Altmetric
Original Research Article

Astroglial transcriptome dysregulation in early disease of an ALS mutant SOD1 mouse model

, , &
Pages 37-48 | Received 13 Sep 2016, Accepted 09 Nov 2016, Published online: 25 Dec 2016

References

  • Alice, M., & Walsh, M.J.L. (2013). Regulation of EGFR trafficking and cell signaling by Sprouty2 and MIG6 in lung cancer cells. Journal of Cell Science, 126, 4339–4348. doi:10.1242/jcs.123208.
  • Bataveljic, D., Nikolic, L., Milosevic, M., Todorovic, N., & Andjus, P.R. (2012). Changes in the astrocytic aquaporin-4 and inwardly rectifying potassium channel expression in the brain of the amyotrophic lateral sclerosis SOD1(G93A) rat model. Glia, 60, 1991–2003. doi:10.1002/glia.22414.
  • Beck, H., Schwarz, G., Schroter, C.J., Deeg, M., Baier, D., Stevanovic, S., … Kalbacher, H. (2001). Cathepsin S and an asparagine-specific endoprotease dominate the proteolytic processing of human myelin basic protein in vitro. The European Journal of Immunology, 31, 3726–3736. doi:10.1002/1521-4141(200112)31:12<3726::AID-IMMU3726>3.0.CO;2-O.
  • Berjaoui, S., Povedano, M., Garcia-Esparcia, P., Carmona, M., Aso, E., & Ferrer, I. (2015). complex inflammation mRNA-related response in ALS is region dependent. Neural Plasticity, 2015, 573784. doi: 10.1155/2015/573784.
  • Brekken, R.A. (2004). Expression and characterization of murine hevin (SC1), a member of the SPARC family of matricellular proteins. Journal of Histochemistry and Cytochemistry, 52, 735–748. doi:10.1369/jhc.3A6245.2004.
  • Brekken, R.A., & Sage, E.H. (2000). SPARC, a matricellular protein: at the crossroads of cell-matrix. Matrix Biology, 19, 569–580. doi:10.1016/S0945-053X(00)00105-0.
  • Cahoy, J.D., Emery, B., Kaushal, A., Foo, L.C., Zamanian, J.L., Christopherson, K.S., … Barres, B.A. (2008). A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. The Journal of Neuroscience, 28, 264–278. doi:10.1523/jneurosci.4178-07.2008.
  • Casci, T., Vinos, J., & Freeman, M. (1999). Sprouty, an intracellular inhibitor of Ras signaling. Cell, 96, 655–665. doi:10.1016/S0092-8674(00)80576-0.
  • Chiu, I.M., Morimoto, E.T., Goodarzi, H., Liao, J.T., O'keeffe, S., Phatnani, H.P., … Maniatis, T. (2013). A neurodegeneration-specific gene-expression signature of acutely isolated microglia from an amyotrophic lateral sclerosis mouse model. Cell Reports, 4, 385–401. doi:10.1016/j.celrep.2013.06.018.
  • Claeskens, A., Ongenae, N., Neefs, J.M., Cheyns, P., Kaijen, P., Cools, M., & Kutoh, E. (2000). Hevin is down-regulated in many cancers and is a negative regulator of cell growth and proliferation. The British Journal of Cancer, 82, 1123–1130. doi:10.1054/bjoc.1999.1051.
  • Driessen, C., Bryant, R.A., Lennon-Dumenil, A.M., Villadangos, J.A., Bryant, P.W., Shi, G.P., … Ploegh, H.L. (1999). Cathepsin S controls the trafficking and maturation of MHC class II molecules in dendritic cells. Journal of Cell Biology, 147, 775–790.
  • Du, Y., Kiyoshi, C.M., Wang, Q., Wang, W., Ma, B., Alford, C.C., … Zhou, M. (2016). Genetic deletion of TREK-1 or TWIK-1/TREK-1 potassium channels does not alter the basic electrophysiological properties of mature hippocampal astrocytes in situ. Frontiers in Cellular Neuroscience, 10, 13. doi:10.3389/fncel.2016.00013.
  • Egan, J.E., Hall, A.B., Yatsula, B.A., & Bar-Sagi, D. (2002). The bimodal regulation of epidermal growth factor signaling by human Sprouty proteins. Proceedings of the National Academy of the Sciences in the United States of America, 99, 6041–6046. doi:10.1073/pnas.052090899.
  • Enyedi, P., & Czirjak, G. (2010). Molecular background of leak K + currents: two-pore domain potassium channels. Physiological Reviews, 90, 559–605. doi:10.1152/physrev.00029.2009.
  • Eroglu, C. (2009). The role of astrocyte-secreted matricellular proteins in central nervous system development and function. The Journal of Cell Communication and Signaling, 3, 167–176. doi:10.1007/s12079-009-0078-y.
  • Felfly, H., & Klein, O.D. (2013). Sprouty genes regulate proliferation and survival of human embryonic stem cells. Science Reports, 3, 2277. doi:10.1038/srep02277.
  • Feliciangeli, S., Tardy, M.P., Sandoz, G., Chatelain, F.C., Warth, R., Barhanin, J., … Lesage, F. (2010). Potassium channel silencing by constitutive endocytosis and intracellular sequestration. Journal of Biological Chemistry, 285, 4798–4805. doi:10.1074/jbc.M109.078535.
  • Ferguson, A.R., Nielson, J.L., Cragin, M.H., Bandrowski, A.E., & Martone, M.E. (2014). Big data from small data: data-sharing in the ‘long tail’ of neuroscience. Nature Neuroscience, 17, 1442–1447. doi:10.1038/nn.3838.
  • Ferraiuolo, L., Higginbottom, A., Heath, P.R., Barber, S., Greenald, D., Kirby, J., & Shaw, P.J. (2011). Dysregulation of astrocyte-motoneuron cross-talk in mutant superoxide dismutase 1-related amyotrophic lateral sclerosis. Brain, 134, 2627–2641. doi:10.1093/brain/awr193.
  • Foo, L.C. (2013). Purification of astrocytes from transgenic rodents by fluorescence-activated cell sorting. Cold Spring Harbor Protocol, 2013, 551–560. doi:10.1101/pdb.prot074229.
  • Gross, I., Bassit, B., Benezra, M., & Licht, J.D. (2001). Mammalian sprouty proteins inhibit cell growth and differentiation by preventing ras activation. Journal of Biological Chemistry, 276, 46460–46468. doi:10.1074/jbc.M108234200.
  • Guo, Y., Duan, W., Li, Z., Huang, J., Yin, Y., Zhang, K., … Li, C. (2010). Decreased GLT-1 and increased SOD1 and HO-1 expression in astrocytes contribute to lumbar spinal cord vulnerability of SOD1-G93A transgenic mice. FEBS Letters, 584, 1615–1622. doi:10.1016/j.febslet.2010.03.025.
  • Hickman, S.E., Kingery, N.D., Ohsumi, T.K., Borowsky, M.L., Wang, L.C., Means, T.K., & El Khoury, J. (2013). The microglial sensome revealed by direct RNA sequencing. Nature Neuroscience, 16, 1896–1905. doi:10.1038/nn.3554.
  • Holtman, I.R., Noback, M., Bijlsma, M., Duong, K.N., van der Geest, M.A., Ketelaars, P.T., … Boddeke, H.W. (2015). Glia Open Access Database (GOAD): a comprehensive gene expression encyclopedia of glia cells in health and disease. Glia, 63, 1495–1506. doi:10.1002/glia.22810.
  • Hwang, E.M., Kim, E., Yarishkin, O., Woo, D.H., Han, K.S., Park, N., … Park, J.Y. (2014). A disulphide-linked heterodimer of TWIK-1 and TREK-1 mediates passive conductance in astrocytes. Nature Communications, 5, 3227. doi:10.1038/ncomms4227.
  • Johnston, I.G., Paladino, T., Gurd, J.W., & Brown, I.R. (1990). Molecular cloning of SC1: a putative brain extracellular matrix glycoprotein showing partial similarity to osteonectin/BM40/SPARC. Neuron, 4, 165–176. doi:10.1016/0896-6273(90)90452-L.
  • Kaiser, M., Maletzki, I., Hulsmann, S., Holtmann, B., Schulz-Schaeffer, W., Kirchhoff, F., … Neusch, C. (2006). Progressive loss of a glial potassium channel (KCNJ10) in the spinal cord of the SOD1 (G93A) transgenic mouse model of amyotrophic lateral sclerosis. Journal of Neurochemistry, 99, 900–912. doi:10.1111/j.1471-4159.2006.04131.x.
  • Kucukdereli, H., Allen, N.J., Lee, A.T., Feng, A., Ozlu, M.I., Conatser, L.M., … Eroglu, C. (2011). Control of excitatory CNS synaptogenesis by astrocyte-secreted proteins Hevin and SPARC. Proceedindgs of the National Academy of Sciences of the United States of America, 108, E440–E449. doi:10.1073/pnas.1104977108.
  • Kulijewicz-Nawrot, M., Sykova, E., Chvatal, A., Verkhratsky, A., & Rodriguez, J.J. (2013). Astrocytes and glutamate homoeostasis in Alzheimer's disease: a decrease in glutamine synthetase, but not in glutamate transporter-1, in the prefrontal cortex. ASN Neuro, 5, 273–282. doi:10.1042/AN20130017.
  • LaFerla, F.M. (2002). Calcium dyshomeostasis and intracellular signalling in Alzheimer's disease. Nature Reviews Neuroscience, 3, 862–872. doi:10.1038/nrn960.
  • Lemere, C.A., Munger, J.S., Shi, G.P., Natkin, L., Haass, C., Chapman, H.A., & Selkoe, D.J. (1995). The lysosomal cysteine protease, cathepsin S, is increased in Alzheimer's disease and Down syndrome brain. An immunocytochemical study. American Journal of Pathology, 146, 848–860.
  • Lesage, F., Guillemare, E., Fink, M., Duprat, F., Lazdunski, M., Romey, G., & Barhanin, J. (1996). TWIK-1, a ubiquitous human weakly inward rectifying K + channel with a novel structure. EMBO Journal, 15, 1004–1011.
  • Li, P., Qian, J., Yu, G., Chen, Y., Liu, K., Li, J., & Wang, J. (2012). Down-regulated SPARCL1 is associated with clinical significance in human gastric cancer. Journal of Surgical Oncology, 105, 31–37. doi:10.1002/jso.22025.
  • Lim, J., Yusoff, P., Wong, E.S.M., Chandramouli, S., Lao, D.H., Fong, C.W., & Guy, G.R. (2002). The cysteine-rich sprouty translocation domain targets mitogen-activated protein kinase inhibitory proteins to phosphatidylinositol 4,5-bisphosphate in plasma membranes. Molecular and Cellular Biology, 22, 7953–7966. doi:10.1128/mcb.22.22.7953-7966.2002.
  • Lively, S., & Brown, I.R. (2007). Analysis of the extracellular matrix protein SC1 during reactive gliosis in the rat lithium-pilocarpine seizure model. Brain Research, 1163, 1–9. doi:10.1016/j.brainres.2007.05.052.
  • Lively, S., & Brown, I.R. (2008). Extracellular matrix protein SC1/hevin in the hippocampus following pilocarpine-induced status epilepticus. Journal of Neurochemistry, 107, 1335–1346. doi:10.1111/j.1471-4159.2008.05696.x.
  • Lively, S., Moxon-Emre, I., & Schlichter, L.C. (2011). SC1/hevin and reactive gliosis after transient ischemic stroke in young and aged rats. Journal of Neuropathology and Experimental Neurology, 70, 913–929. doi:10.1097/NEN.0b013e318231151e.
  • Lively, S., Ringuette, M.J., & Brown, I.R. (2007). Localization of the extracellular matrix protein SC1 to synapses in the adult rat brain. Neurochemical Research, 32, 65–71. doi:10.1007/s11064-006-9226-4.
  • Mason, J.M., Morrison, D.J., Basson, M.A., & Licht, J.D. (2006). Sprouty proteins: multifaceted negative-feedback regulators of receptor tyrosine kinase signaling. Trends in Cell Biology, 16, 45–54. doi:10.1016/j.tcb.2005.11.004.
  • McKinnon, P.J., & Margolskee, R.F. (1996). SC1: a marker for astrocytes in the adult rodent brain is upregulated during reactive astrocytosis. Brain Research, 709, 27–36. doi:10.1016/0006-8993(95)01224-9.
  • Mendis, D.B., Ivy, G.O., & Brown, I.R. (1996). SC1, a brain extracellular matrix glycoprotein related to SPARC and follistatin, is expressed by rat cerebellar astrocytes following injury and during development. Brain Research, 730, 95–106. doi:10.1016/0006-8993(96)00440-4.
  • Miller, S.J., & Rothstein, J.D. (2016). Astroglia in thick tissue with super resolution and cellular reconstruction. PLoS One, 11, e0160391. doi:10.1371/journal.pone.0160391.
  • Munger, J.S., Haass, C., Lemere, C.A., Shi, G.P., Wong, W.S., Teplow, D.B., … Chapman, H.A. (1995). Lysosomal processing of amyloid precursor protein to A beta peptides: a distinct role for cathepsin S. Biochemical Journal, 311, 299–305.
  • Nowacek, A., Kosloski, L.M., & Gendelman, H.E. (2009). Neurodegenerative disorders and nanoformulated drug development. Nanomedicine (Lond), 4, 541–555. doi:10.2217/nnm.09.37.
  • Oberheim, N.A., Goldman, S.A., & Nedergaard, M. (2012). Heterogeneity of astrocytic form and function. Methods in Molecular Biology, 814, 23–45. doi:10.1007/978-1-61779-452-0_3.
  • Olsen, M.L., Campbell, S.C., McFerrin, M.B., Floyd, C.L., & Sontheimer, H. (2010). Spinal cord injury causes a wide-spread, persistent loss of Kir4.1 and glutamate transporter 1: benefit of 17 beta-oestradiol treatment. Brain, 133, 1013–1025. doi:10.1093/brain/awq049.
  • Petanceska, S., Burke, S., Watson, S.J., & Devi, L. (1994). Differential distribution of messenger RNAs for cathepsins B, L and S in adult rat brain: an in situ hybridization study. Neuroscience, 59, 729–738. doi:10.1016/0306-4522(94)90190-2.
  • Petanceska, S., Canoll, P., & Devi, L.A. (1996). Expression of rat cathepsin S in phagocytic cells. Journal of Biological Chemistry, 271, 4403–4409. doi:10.1074/jbc.271.8.4403.
  • Phatnani, H.P., Guarnieri, P., Friedman, B.A., Carrasco, M.A., Muratet, M., O?Keeffe, S., … Maniatis, T. (2013). Intricate interplay between astrocytes and motor neurons in ALS. Proceedings of the National Academy of Sciences of the United States of America, 110, E756–E765. doi:10.1073/pnas.1222361110.
  • Rajan, S., Plant, L.D., Rabin, M.L., Butler, M.H., & Goldstein, S.A. (2005). Sumoylation silences the plasma membrane leak K + channel K2P1. Cell, 121, 37–47. doi:10.1016/j.cell.2005.01.019.
  • Re, D.B., Le Verche, V., Yu, C., Amoroso, M.W., Politi, K.A., Phani, S., … Przedborski, S. (2014). Necroptosis drives motor neuron death in models of both sporadic and familial ALS. Neuron, 81, 1001–1008. doi:10.1016/j.neuron.2014.01.011.
  • Risher, W.C., Patel, S., Kim, I.H., Uezu, A., Bhagat, S., Wilton, D.K., … Eroglu, C. (2014). Astrocytes refine cortical connectivity at dendritic spines. Elife, 3, doi:10.7554/eLife.04047.
  • Robberecht, W., & Philips, T. (2013). The changing scene of amyotrophic lateral sclerosis. Nature Reviews Neuroscience, 14, 248–264. doi:10.1038/nrn3430.
  • Rothstein, D.W., & Cleveland, J.D. (2001). From charcot to lou gehrig: deciphering selective motor neuron death in als. Nature Reviews Neuroscience, 2, 806–819. doi:10.1038/35097565.
  • Rothstein, J.D., Van Kammen, M., Levey, A.I., Martin, L.J., & Kuncl, R.W. (1995). Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Annals of Neurology, 38, 73–84. doi:10.1002/ana.410380114.
  • Shi, G.P., Webb, A.C., Foster, K.E., Knoll, J.H., Lemere, C.A., Munger, J.S., & Chapman, H.A. (1994). Human cathepsin S: chromosomal localization, gene structure, and tissue distribution. Journal of Biological Chemistry, 269, 11530–11536.
  • Singh, S.K., Stogsdill, J.A., Pulimood, N.S., Dingsdale, H., Kim, Y.H., Pilaz, L.J., … Eroglu, C. (2016). Astrocytes assemble thalamocortical synapses by bridging NRX1α and NL1 via Hevin. Cell, 164, 183–196. doi:10.1016/j.cell.2015.11.034.
  • Sofroniew, M.V., & Vinters, H.V. (2010). Astrocytes: biology and pathology. Acta Neuropathologica, 119, 7–35. doi:10.1007/s00401-009-0619-8.
  • Sultan, S., Li, L., Moss, J., Petrelli, F., Casse, F., Gebara, E., … Toni, N. (2015). Synaptic integration of adult-born hippocampal neurons is locally controlled by astrocytes. Neuron, 88, 957–972. doi:10.1016/j.neuron.2015.10.037.
  • Talley, E.M., Solorzano, G., Lei, Q., Kim, D., & Bayliss, D.A. (2001). Cns distribution of members of the two-pore-domain (KCNK) potassium channel family. Journal of Neuroscience, 21, 7491–7505.
  • Tong, X., Ao, Y., Faas, G.C., Nwaobi, S.E., Xu, J., Haustein, M.D., … Khakh, B.S. (2014). Astrocyte Kir4.1 ion channel deficits contribute to neuronal dysfunction in Huntington’s disease model mice. Nature Neuroscience, 17, 694–703. doi:10.1038/nn.3691.
  • Turtoi, A., Musmeci, D., Naccarato, A.G., Scatena, C., Ortenzi, V., Kiss, R., … Castronovo, V. (2012). Sparc-like protein 1 is a new marker of human glioma progression. Journal of Proteome Research, 11, 5011–5021. doi:10.1021/pr3005698.
  • Vargas, M.R., & Johnson, J.A. (2010). Astrogliosis in amyotrophic lateral sclerosis: role and therapeutic potential of astrocytes. Neurotherapeutics, 7, 471–481. doi:10.1016/j.nurt.2010.05.012.
  • Volterra, A., & Meldolesi, J. (2005). Astrocytes, from brain glue to communication elements: the revolution continues. Nature Reviews Neuroscience, 6, 626–640. doi:10.1038/nrn1722.
  • Walsh, A.M., Kapoor, G.S., Buonato, J.M., Mathew, L.K., Bi, Y., Davuluri, R.V., … Lazzara, M.J. (2015). Sprouty2 drives drug resistance and proliferation in glioblastoma. Molecular Cancer Research, 13, 1227–1237. doi:10.1158/1541-7786.MCR-14-0183-T.
  • Wang, W., Putra, A., Schools, G.P., Ma, B., Chen, H., Kaczmarek, L.K., … Zhou, M. (2013). The contribution of TWIK-1 channels to astrocyte K(+) current is limited by retention in intracellular compartments. Frontiers in Cellular Neuroscience, 7, 246. doi:10.3389/fncel.2013.00246.
  • Wendt, W., Lubbert, H., & Stichel, C.C. (2008). Upregulation of cathepsin S in the aging and pathological nervous system of mice. Brain Research, 1232, 7–20. doi:10.1016/j.brainres.2008.07.067.
  • Weydt, P., Hong, S.Y., Kliot, M., & Moller, T. (2003). Assessing disease onset and progression in the SOD1 mouse model of ALS. Neuroreport, 14, 1051–1054. doi:10.1097/01.wnr.0000073685.00308.89.
  • Wilkinson, R.D., Williams, R., Scott, C.J., & Burden, R.E. (2015). Cathepsin S: therapeutic, diagnostic, and prognostic potential. Biological Chemistry, 396, 867–882. doi:10.1515/hsz-2015-0114.
  • Yamazaki, T., Z, K., Hailey, D., Presley, J., Lippincott-Schwartz, J., & Samelson, L.E. (2002). Role of Grb2 in EGF-stimulated EGFR internalization. Journal of Cell Science, 115, 1791–1802.
  • Yan, Q., & Sage, E.H. (1999). SPARC, a matricellular glycoprotein with important biological functions. Journal of Histochemistry and Cytochemistry, 47, 1495–1506. doi:10.1177/002215549904701201.
  • Yang, Y., Vidensky, S., Jin, L., Jie, C., Lorenzini, I., Frankl, M., & Rothstein, J.D. (2011). Molecular comparison of GLT1+ and ALDH1L1+ astrocytes in vivo in astroglial reporter mice. Glia, 59, 200–207. doi:10.1002/glia.21089.
  • Yusoff, P., Lao, D.H., Ong, S.H., Wong, E.S., Lim, J., Lo, T.L., … Guy, G.R. (2002). Sprouty2 inhibits the Ras/MAP kinase pathway by inhibiting the activation of Raf. Journal of Biological Chemistry, 277, 3195–3201. doi:10.1074/jbc.M108368200.
  • Zhang, Y., & Barres, B.A. (2010). Astrocyte heterogeneity: an underappreciated topic in neurobiology. Current Opinion in Neurobiology, 20, 588–594. doi:10.1016/j.conb.2010.06.005.
  • Zhou, M., Xu, G., Xie, M., Zhang, X., Schools, G.P., Ma, L., … Chen, H. (2009). TWIK-1 and TREK-1 are potassium channels contributing significantly to astrocyte passive conductance in rat hippocampal slices. Journal of Neuroscience, 29, 8551–8564. doi:10.1523/JNEUROSCI.5784-08.2009.