Rewired glycosylation activity promotes scarless regeneration and functional recovery in spiny mice after complete spinal cord transection

Developmental Cell - Tập 57 - Trang 440-450.e7 - 2022
Joana Nogueira-Rodrigues1,2, Sérgio C. Leite1, Rita Pinto-Costa1, Sara C. Sousa1,2, Liliana L. Luz3, Maria A. Sintra1, Raquel Oliveira4,5,6, Ana C. Monteiro1, Gonçalo G. Pinheiro7,8, Marta Vitorino7,8, Joana A. Silva8, Sónia Simão8,9, Vitor E. Fernandes8,9, Jan Provazník10, Vladimir Benes10, Célia D. Cruz4,5, Boris V. Safronov3, Ana Magalhães11,12, Celso A. Reis11,12,13, Jorge Vieira14
1Nerve Regeneration Group, Instituto de Biologia Molecular e Celular (IBMC), Instituto de Investigação e Inovação em Saúde (i3S), University of Porto, 4200-135 Porto, Portugal
2Graduate Program in Molecular and Cell Biology, Instituto de Ciências Biomédicas Abel Salazar (ICBAS), University of Porto, 4050-313 Porto, Portugal
3Neuronal Networks Group, Instituto de Biologia Molecular e Celular (IBMC), Instituto de Investigação e Inovação em Saúde (i3S), University of Porto, 4200-135 Porto, Portugal
4Translational NeuroUrology Group, Instituto de Biologia Molecular e Celular (IBMC), Instituto de Investigação e Inovação em Saúde (i3S), University of Porto, 4200-135 Porto, Portugal
5Department of Biomedicine, Experimental Biology Unit, Faculty of Medicine of Porto, University of Porto, 4200-319 Porto, Portugal
6Regeneration Group, Wolfson Centre for Age-Related Diseases, Institute of Psychiatry, Psychology and Neuroscience, King’s College London WC2R 2LS, London, UK
7Molecular & Regenerative Medicine Laboratory, Centro de Ciências do Mar (CCMAR), University of Algarve, 8005-139 Faro, Portugal
8Faculty of Medicine and Biomedical Sciences, University of Algarve, 8005-139 Faro, Portugal
9Algarve Biomedical Center Research Institute (ABC-RI), University of Algarve, 8005-139 Faro, Portugal
10Genomics Core Facility, European Molecular Biology Laboratory (EMBL), 69117 Heidelberg, Germany
11Glycobiology in Cancer Group, Institute of Molecular Pathology and Immunology, IPATIMUP), Instituto de Investigação e Inovação em Saúde (i3S), University of Porto, 4200-135 Porto, Portugal
12Department of Molecular Biology, Instituto de Ciências Biomédicas Abel Salazar (ICBAS), University of Porto, 4050-313 Porto, Portugal
13Department of Pathology, Faculty of Medicine of Porto, University of Porto, 4200-319 Porto, Portugal
14Phenotypic Evolution Group, Instituto de Biologia Molecular e Celular (IBMC), Instituto de Investigação e Inovação em Saúde (i3S), University of Porto, 4200-135 Porto, Portugal

Tài liệu tham khảo

Basso, 2006, Basso mouse scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains, J. Neurotrauma, 23, 635, 10.1089/neu.2006.23.635 Brant, 2015, A comparative analysis of gene expression profiles during skin regeneration in Mus and Acomys, PLoS One, 10, e0142931, 10.1371/journal.pone.0142931 Brant, 2016, Cellular events during scar-free skin regeneration in the spiny mouse, Acomys, Wound Repair Regen, 24, 75, 10.1111/wrr.12385 Chen, 2017, Evaluating the voiding spot assay in mice: a simple method with complex environmental interactions, Am. J. Physiol. Renal Physiol., 313, F1274, 10.1152/ajprenal.00318.2017 Cregg, 2014, Functional regeneration beyond the glial scar, Exp. Neurol., 253, 197, 10.1016/j.expneurol.2013.12.024 Cyr, 2019, Regeneration-competent and -incompetent murids differ in neutrophil quantity and function, Integr. Comp. Biol., 59, 1138, 10.1093/icb/icz023 Dent, 1999, Reorganization and movement of microtubules in axonal growth cones and developing interstitial branches, J. Neurosci., 19, 8894, 10.1523/JNEUROSCI.19-20-08894.1999 Dias, 2018, Fibrotic scarring following lesions to the central nervous system, Matrix Biol, 68, 561, 10.1016/j.matbio.2018.02.009 Diaz Quiroz, 2013, Spinal cord regeneration: where fish, frogs and salamanders lead the way, can we follow?, Biochem. J., 451, 353, 10.1042/BJ20121807 Didangelos, 2016, High-throughput proteomics reveal alarmins as amplifiers of tissue pathology and inflammation after spinal cord injury, Sci. Rep., 6, 21607, 10.1038/srep21607 Du, 2015, Pten deletion promotes regrowth of corticospinal tract axons 1 year after spinal cord injury, J. Neurosci., 35, 9754, 10.1523/JNEUROSCI.3637-14.2015 Gawriluk, 2020, Complex tissue regeneration in mammals is associated With reduced inflammatory cytokines and an influx of T cells, Front. Immunol., 11, 1695, 10.3389/fimmu.2020.01695 Gawriluk, 2016, Comparative analysis of ear-hole closure identifies epimorphic regeneration as a discrete trait in mammals, Nat. Commun., 7, 11164, 10.1038/ncomms11164 Giger, 2010, Guidance molecules in axon regeneration, Cold Spring Harb. Perspect. Biol., 2, a001867, 10.1101/cshperspect.a001867 Haas, 2013, De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis, Nat. Protoc., 8, 1494, 10.1038/nprot.2013.084 Hamid, 2018, Epidemiology and pathophysiology of neurogenic bladder after spinal cord injury, World J. Urol., 36, 1517, 10.1007/s00345-018-2301-z Imagama, 2011, Keratan sulfate restricts neural plasticity after spinal cord injury, J. Neurosci., 31, 17091, 10.1523/JNEUROSCI.5120-10.2011 Ishikawa, 2015, A combination of keratan sulfate digestion and rehabilitation promotes anatomical plasticity after rat spinal cord injury, Neurosci. Lett., 593, 13, 10.1016/j.neulet.2015.03.015 Jao, 2016, Alteration of colonic epithelial cell differentiation in mice deficient for glucosaminyl N-deacetylase/N-sulfotransferase 4, Oncotarget, 7, 84938, 10.18632/oncotarget.12915 Jin, 2015, Restoration of skilled locomotion by sprouting corticospinal axons induced by co-deletion of PTEN and SOCS3, Nat. Commun., 6, 8074, 10.1038/ncomms9074 Jones, 2002, Spinal cord injury elicits expression of keratan sulfate proteoglycans by macrophages, reactive microglia, and oligodendrocyte progenitors, J. Neurosci., 22, 4611, 10.1523/JNEUROSCI.22-11-04611.2002 Kakuda, 2017, Deciphering the Fringe-mediated Notch code: identification of activating and inhibiting sites allowing discrimination between ligands, Dev. Cell, 40, 193, 10.1016/j.devcel.2016.12.013 Law, 2014, voom: Precision weights unlock linear model analysis tools for RNA-seq read counts, Genome Biol, 15, R29, 10.1186/gb-2014-15-2-r29 Lee-Liu, 2013, Spinal cord regeneration: lessons for mammals from non-mammalian vertebrates, Genesis, 51, 529, 10.1002/dvg.22406 Leite, 2016, The actin-binding protein alpha-Adducin is required for maintaining axon diameter, Cell Rep, 15, 490, 10.1016/j.celrep.2016.03.047 Liddelow, 2017, Reactive astrocytes: production, function, and therapeutic potential, Immunity, 46, 957, 10.1016/j.immuni.2017.06.006 Liddelow, 2017, Neurotoxic reactive astrocytes are induced by activated microglia, Nature, 541, 481, 10.1038/nature21029 Lin, 2011, 6-sulphated chondroitins have a positive influence on axonal regeneration, PLoS One, 6, e21499, 10.1371/journal.pone.0021499 Lopez-Fernandez, 2020, SEDA: a desktop tool Suite for FASTA files processing, IEEE/ACM Trans. Comput. Biol. Bioinform., 10.1109/TCBB.2020.3040383 Mar, 2016, Myelin lipids inhibit axon regeneration following spinal cord injury: a novel perspective for therapy, Mol. Neurobiol., 53, 1052, 10.1007/s12035-014-9072-3 Martin, 2011, Cutadapt removes adapter sequences from high-throughput sequencing reads, EMBnet. j., 17, 10, 10.14806/ej.17.1.200 Matias Santos, 2016, Ear wound regeneration in the African spiny mouse Acomys cahirinus, Regeneration (Oxf), 3, 52, 10.1002/reg2.50 Miller, 2015, Sugar-dependent modulation of neuronal development, regeneration, and plasticity by chondroitin sulfate proteoglycans, Exp. Neurol., 274, 115, 10.1016/j.expneurol.2015.08.015 Morii, 2006, SCG10, a microtubule destabilizing factor, stimulates the neurite outgrowth by modulating microtubule dynamics in rat hippocampal primary cultured neurons, J. Neurobiol., 66, 1101, 10.1002/neu.20295 Muenks, 2017, Sequence-structure relationships, expression profiles, and disease-associated mutations in the paralogs of phosphoglucomutase 1, PLoS One, 12, e0183563, 10.1371/journal.pone.0183563 Mukhopadhyay, 1994, A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration, Neuron, 13, 757, 10.1016/0896-6273(94)90042-6 Oishi, 2018, Macrophages in inflammation, repair and regeneration, Int. Immunol., 30, 511, 10.1093/intimm/dxy054 Okada, 2018, Astrocyte reactivity and astrogliosis after spinal cord injury, Neurosci. Res., 126, 39, 10.1016/j.neures.2017.10.004 Pallerla, 2008, Altered heparan sulfate structure in mice with deleted NDST3 gene function, J. Biol. Chem., 283, 16885, 10.1074/jbc.M709774200 Randal, 2001, The structure and activity of a monomeric interferon-gamma:alpha-chain receptor signaling complex, Structure, 9, 155, 10.1016/S0969-2126(01)00567-6 Salmela, 2011, Correcting errors in short reads by multiple alignments, Bioinformatics, 27, 1455, 10.1093/bioinformatics/btr170 Schmitz, 2011, Automated analysis of neuronal morphology, synapse number and synaptic recruitment, J. Neurosci. Methods, 195, 185, 10.1016/j.jneumeth.2010.12.011 Seifert, 2012, Skin shedding and tissue regeneration in African spiny mice (Acomys), Nature, 489, 561, 10.1038/nature11499 Simkin, 2017, Macrophages are necessary for epimorphic regeneration in African spiny mice, Elife, 6, 26, 10.7554/eLife.24623 Steppan, 2004, Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes, Syst. Biol., 53, 533, 10.1080/10635150490468701 Streeter, 2020, Molecular and histologic outcomes following spinal cord injury in spiny mice, Acomys cahirinus, J. Comp. Neurol., 528, 1535, 10.1002/cne.24836 Thuret, 2012, Enhanced functional recovery in MRL/MpJ mice after spinal cord dorsal hemisection, PLoS One, 7, e30904, 10.1371/journal.pone.0030904 Tica, 2018, Comparative transcriptomics of rat and axolotl after spinal cord injury dissects differences and similarities in inflammatory and matrix remodeling gene expression patterns, Front. Neurosci., 12, 808, 10.3389/fnins.2018.00808 Tsata, 2021, A switch in pdgfrb+ cell-derived ECM composition prevents inhibitory scarring and promotes axon regeneration in the zebrafish spinal cord, Dev. Cell, 56, 509, 10.1016/j.devcel.2020.12.009 Wang, 2008, Chondroitin-4-sulfation negatively regulates axonal guidance and growth, J. Cell Sci., 121, 3083, 10.1242/jcs.032649 Wu, 2014, IFN-gamma primes macrophage activation by increasing phosphatase and tensin homolog via downregulation of miR-3473b, J. Immunol., 193, 3036, 10.4049/jimmunol.1302379 Yang, 2020, Dissecting the dual role of the glial scar and scar-forming astrocytes in spinal cord injury, Front. Cell. Neurosci., 14, 78, 10.3389/fncel.2020.00078 Zabbarova, 2018, Targeting p75 neurotrophin receptors ameliorates spinal cord injury-induced detrusor sphincter dyssynergia in mice, Neurourol. Urodyn., 37, 2452, 10.1002/nau.23722