Interaction of reactive astrocytes with type I collagen induces astrocytic scar formation through the integrin–N-cadherin pathway after spinal cord injury (original) (raw)

• McDonald, J.W. & Sadowsky, C. Spinal-cord injury. Lancet 359, 417–425 (2002).
  Article PubMed Google Scholar
• Okada, S. et al. Conditional ablation of Stat3 or Socs3 discloses a dual role for reactive astrocytes after spinal cord injury. Nat. Med. 12, 829–834 (2006).
  Article CAS PubMed Google Scholar
• Silver, J. & Miller, J.H. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 5, 146–156 (2004).
  Article CAS PubMed Google Scholar
• Karimi-Abdolrezaee, S. & Billakanti, R. Reactive astrogliosis after spinal cord injury—beneficial and detrimental effects. Mol. Neurobiol. 46, 251–264 (2012).
  Article CAS PubMed Google Scholar
• Ridet, J.L., Malhotra, S.K., Privat, A. & Gage, F.H. Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci. 20, 570–577 (1997).
  Article CAS PubMed Google Scholar
• Buss, A. et al. Gradual loss of myelin and formation of an astrocytic scar during Wallerian degeneration in the human spinal cord. Brain 127, 34–44 (2004).
  Article CAS PubMed Google Scholar
• Anderson, M.A. et al. Astrocyte scar formation aids central nervous system axon regeneration. Nature 532, 195–200 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Liddelow, S.A. & Barres, B.A. Regeneration: not everything is scary about a glial scar. Nature 532, 182–183 (2016).
  Article CAS PubMed Google Scholar
• Windle, W.F., Clemente, C.D. & Chambers, W.W. Inhibition of formation of a glial barrier as a means of permitting a peripheral nerve to grow into the brain. J. Comp. Neurol. 96, 359–369 (1952).
  Article CAS PubMed Google Scholar
• Freeman, L.W. Return of spinal cord function in mammals after transecting lesions. Ann. NY Acad. Sci. 58, 564–569 (1954).
  Article Google Scholar
• Sofroniew, M.V. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 32, 638–647 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Cregg, J.M. et al. Functional regeneration beyond the glial scar. Exp. Neurol. 253, 197–207 (2014).
  Article PubMed Google Scholar
• Courtine, G. et al. Can experiments in nonhuman primates expedite the translation of treatments for spinal cord injury in humans? Nat. Med. 13, 561–566 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Renault-Mihara, F. et al. Beneficial compaction of spinal cord lesion by migrating astrocytes through glycogen synthase kinase-3 inhibition. EMBO Mol. Med. 3, 682–696 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Vázquez-Chona, F. & Geisert, E.E.J. Jr. N-cadherin at the glial scar in the rat. Brain Res. 838, 45–50 (1999).
  Article PubMed Google Scholar
• McKillop, W.M., Dragan, M., Schedl, A. & Brown, A. Conditional Sox9 ablation reduces chondroitin sulfate proteoglycan levels and improves motor function following spinal cord injury. Glia 61, 164–177 (2013).
  Article PubMed Google Scholar
• Mann, B. et al. Target genes of β-catenin-T cell-factor/lymphoid-enhancer-factor signaling in human colorectal carcinomas. Proc. Natl. Acad. Sci. USA 96, 1603–1608 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Blasi, F. & Carmeliet, P. uPAR: a versatile signalling orchestrator. Nat. Rev. Mol. Cell Biol. 3, 932–943 (2002).
  Article CAS PubMed Google Scholar
• Takeuchi, K. et al. Chondroitin sulphate _N_-acetylgalactosaminyl-transferase-1 inhibits recovery from neural injury. Nat. Commun. 4, 2740 (2013).
  Article PubMed CAS Google Scholar
• Hagino, S. et al. Slit and glypican-1 mRNAs are coexpressed in the reactive astrocytes of the injured adult brain. Glia 42, 130–138 (2003).
  Article PubMed Google Scholar
• Ilieva, H., Polymenidou, M. & Cleveland, D.W. Non–cell autonomous toxicity in neurodegenerative disorders: ALS and beyond. J. Cell Biol. 187, 761–772 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• von Karstedt, S. et al. Cancer cell–autonomous TRAIL-R signaling promotes KRAS-driven cancer progression, invasion, and metastasis. Cancer Cell 27, 561–573 (2015).
  Article CAS PubMed PubMed Central Google Scholar
• Kumamaru, H. et al. Direct isolation and RNA–seq reveal environment-dependent properties of engrafted neural stem/progenitor cells. Nat. Commun. 3, 1140 (2012).
  Article PubMed CAS Google Scholar
• Kumamaru, H. et al. Therapeutic activities of engrafted neural stem/precursor cells are not dormant in the chronically injured spinal cord. Stem Cells 31, 1535–1547 (2013).
  Article CAS PubMed Google Scholar
• Takeichi, M. The cadherin superfamily in neuronal connections and interactions. Nat. Rev. Neurosci. 8, 11–20 (2007).
  Article CAS PubMed Google Scholar
• Tran, M.D., Wanner, I.B. & Neary, J.T. Purinergic receptor signaling regulates N-cadherin expression in primary astrocyte cultures. J. Neurochem. 105, 272–286 (2008).
  Article CAS PubMed Google Scholar
• Hynes, R.O. Integrins: bidirectional, allosteric signaling machines. Cell 110, 673–687 (2002).
  Article CAS PubMed Google Scholar
• Previtali, S.C., Archelos, J.J. & Hartung, H.P. Modulation of the expression of integrins on glial cells during experimental autoimmune encephalomyelitis. A central role for TNF-α. Am. J. Pathol. 151, 1425–1435 (1997).
  CAS PubMed PubMed Central Google Scholar
• Yonezawa, T. et al. Type IV collagen induces expression of thrombospondin-1 that is mediated by integrin α1β1 in astrocytes. Glia 58, 755–767 (2010).
  PubMed Google Scholar
• Doyle, J.P. et al. Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 135, 749–762 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Garg, A. et al. Non-enzymatic dissociation of human mesenchymal stromal cells improves chemokine-dependent migration and maintains immunosuppressive function. Cytotherapy 16, 545–559 (2014).
  Article CAS PubMed Google Scholar
• Yokota, K. et al. Engrafted neural stem/progenitor cells promote functional recovery through synapse reorganization with spared host neurons after spinal cord injury. Stem Cell Rep. 5, 264–277 (2015).
  Article CAS Google Scholar
• Faulkner, J.R. et al. Reactive astrocytes protect tissue and preserve function after spinal cord injury. J. Neurosci. 24, 2143–2155 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Rolls, A. et al. Two faces of chondroitin sulfate proteoglycan in spinal cord repair: a role in microglia/macrophage activation. PLoS Med. 5, e171 (2008).
  Article PubMed PubMed Central Google Scholar
• Rolls, A., Shechter, R. & Schwartz, M. The bright side of the glial scar in CNS repair. Nat. Rev. Neurosci. 10, 235–241 (2009).
  Article CAS PubMed Google Scholar
• Shechter, R., Raposo, C., London, A., Sagi, I. & Schwartz, M. The glial scar–monocyte interplay: a pivotal resolution phase in spinal cord repair. PLoS One 6, e27969 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Brionne, T.C., Tesseur, I., Masliah, E. & Wyss-Coray, T. Loss of TGF-β1 leads to increased neuronal cell death and microgliosis in mouse brain. Neuron 40, 1133–1145 (2003).
  Article CAS PubMed Google Scholar
• Abe, K., Chu, P.J., Ishihara, A. & Saito, H. Transforming growth factor-β1 promotes re-elongation of injured axons of cultured rat hippocampal neurons. Brain Res. 723, 206–209 (1996).
  Article CAS PubMed Google Scholar
• Lutton, C. et al. Combined VEGF and PDGF treatment reduces secondary degeneration after spinal cord injury. J. Neurotrauma 29, 957–970 (2012).
  Article PubMed Google Scholar
• DePaul, M.A., Lin, C.Y., Silver, J. & Lee, Y.S. Peripheral nerve transplantation combined with acidic fibroblast growth factor and chondroitinase induces regeneration and improves urinary function in complete spinal cord transected adult mice. PLoS One 10, e0139335 (2015).
  Article PubMed PubMed Central CAS Google Scholar
• Göritz, C. et al. A pericyte origin of spinal cord scar tissue. Science 333, 238–242 (2011).
  Article PubMed CAS Google Scholar
• Shintani, Y., Wheelock, M.J. & Johnson, K.R. Phosphoinositide-3 kinase–Rac1–c-Jun NH2-terminal kinase signaling mediates collagen I–induced cell scattering and up-regulation of N-cadherin expression in mouse mammary epithelial cells. Mol. Biol. Cell 17, 2963–2975 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Shintani, Y., Hollingsworth, M.A., Wheelock, M.J. & Johnson, K.R. Collagen I promotes metastasis in pancreatic cancer by activating c-Jun NH2-terminal kinase 1 and up-regulating N-cadherin expression. Cancer Res. 66, 11745–11753 (2006).
  Article CAS PubMed Google Scholar
• Le Dréau, G. et al. NOV/CCN3 upregulates CCL2 and CXCL1 expression in astrocytes through β1 and β5 integrins. Glia 58, 1510–1521 (2010).
  Article PubMed Google Scholar
• Cao, J., Wang, J.S., Ren, X.H. & Zang, W.D. Spinal sample showing p-JNK and p38 associated with the pain signaling transduction of glial cell in neuropathic pain. Spinal Cord 53, 92–97 (2015).
  Article CAS PubMed Google Scholar
• Gao, K. et al. Traumatic scratch injury in astrocytes triggers calcium influx to activate the JNK/c-Jun/AP-1 pathway and switch on GFAP expression. Glia 61, 2063–2077 (2013).
  Article PubMed Google Scholar
• Repici, M. et al. Specific inhibition of the JNK pathway promotes locomotor recovery and neuroprotection after mouse spinal cord injury. Neurobiol. Dis. 46, 710–721 (2012).
  Article CAS PubMed Google Scholar
• Kanemaru, K. et al. Calcium-dependent N-cadherin up-regulation mediates reactive astrogliosis and neuroprotection after brain injury. Proc. Natl. Acad. Sci. USA 110, 11612–11617 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Péglion, F. & Etienne-Manneville, S. N-cadherin expression level as a critical indicator of invasion in non-epithelial tumors. Cell Adh Migr. 6, 327–332 (2012).
  Article PubMed PubMed Central Google Scholar
• Bush, T.G. et al. Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron 23, 297–308 (1999).
  Article CAS PubMed Google Scholar
• Silver, J. The glial scar is more than just astrocytes. Exp. Neurol. 286, 147–149 (2016).
  Article PubMed Google Scholar
• Okabe, M., Ikawa, M., Kominami, K., Nakanishi, T. & Nishimune, Y. 'Green mice' as a source of ubiquitous green cells. FEBS Lett. 407, 313–319 (1997).
  Article CAS PubMed Google Scholar
• Sanai, N. et al. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427, 740–744 (2004).
  Article CAS PubMed Google Scholar
• Takahashi, S. et al. C-type lectin–like domain and fibronectin-like type II domain of phospholipase A2 receptor 1 modulate binding and migratory responses to collagen. FEBS Lett. 589, 829–835 (2015).
  Article CAS PubMed Google Scholar
• Hayashi, M. et al. Chd5 regulates MuERV-L/MERVL expression in mouse embryonic stem cells via H3K27me3 modification and histone H3.1/H3.2. J. Cell. Biochem. 117, 780–792 (2016).
  Article CAS PubMed Google Scholar
• Harada, A. et al. Incorporation of histone H3.1 suppresses the lineage potential of skeletal muscle. Nucleic Acids Res. 43, 775–786 (2015).
  Article CAS PubMed Google Scholar
• Trapnell, C. et al. Differential gene and transcript expression analysis of RNA–seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562–578 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Dennis, G. Jr. et al. DAVID: Database for Annotation, Visualization, and integrated Discovery. Genome Biol. 4, P3 (2003).
  Article PubMed Google Scholar
• Hashimshony, T. et al. CEL-Seq2: sensitive highly-multiplexed single-cell RNA-Seq. Genome Biol. 17, 77 (2016).
  Article PubMed PubMed Central CAS Google Scholar
• Langmead, B. & Salzberg, S.L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
  CAS PubMed PubMed Central Google Scholar
• Love, M.I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA–seq data with DESeq2. Genome Biol. 15, 550 (2014).
  Article PubMed PubMed Central CAS Google Scholar