ZFIN ID: ZDB-LAB-010302-1
Catherina & Thomas Becker Lab
PI/Director: Becker, Catherina G.
Becker, Thomas
Contact Person: Becker, Catherina G.
Email: catherina.becker@ed.ac.uk
URL: http://www.cnr.ed.ac.uk/research/Becker.html
Address: Centre for Neuroregeneration The University of Edinburgh The Chancellor's Building 49 Little France Crescent Edinburgh EH16 4SB United Kingdom
Country: United Kingdom
Phone: +44 131 242 7983
Fax: +44 131 242 7983
Line Designation: ue


GENOMIC FEATURES ORIGINATING FROM THIS LAB
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STATEMENT OF RESEARCH INTERESTS
Zebrafish have an amazing capacity for central nervous system (CNS) regeneration. They regain function after complete lesions of the spinal cord or the optic nerve. Such lesions in mammals are not repaired and functions are permanently lost.

How can zebrafish replace lost neurons from adult stem cells?

How are severed axonal connections repaired?

How are these processes related to developmental neurogenesis and axonal pathfinding?

To address these questions we are focusing on two important cell types, retinal ganglion cells, which convey all visual information form the eye to the brain, and spinal motor neurons, which control muscle contraction during swimming:

Retinal ganglion cell axons navigate to their targets guided by a variety of molecules. We have found that molecules of the extracellular matrix are essential for pathfinding of developing as well as regenerating axons to their termination areas in zebrafish. We are continuing to investigate which molecules are needed for correct guidance and termination of developing and regenerating retinal ganglion cells using a variety of techniques, such as gene knock down, mutant analysis and expression profiling.

Motor neurons are important target cells for axons descending from the brainstem that control swimming movements. We have shown that regeneration of descending axons is necessary for functional recovery after a spinal lesion and are now investigating the signals that lead to the (re-)generation of motor neurons. We have found that in embryonic motor neurons, transcriptional co-factors control expression of specific cell recognition molecules, such as plexins and neuropilins, which in turn are necessary for pathfinding of embryonic motor axons. We are now using small molecule screens and expression profiling on cDNA microarrays to discover new factors that are important for motor neuron differentiation, both during development and adult regeneration.

By analysing development and regeneration of important cell types in the zebrafish we hope to gain insight into fundamental developmental and regenerative mechanisms in the CNS, and to ultimately increase our understanding of human conditions, such as spinal cord injury and motor neuron disease.


LAB MEMBERS
Boyd, Penelope Post-Doc Cardozo, Marcos Post-Doc Caldwell, Lindsey Graduate Student
Davies, Nick O. Graduate Student McCann, Tess Graduate Student Mysiak, Karolina S. Graduate Student
Smith, Hannah Graduate Student Tsarouchas, Themistoklis Graduate Student Yang, Yujie Graduate Student
Michael, Andria Research Staff Santos, Silvère Fish Facility Staff


ZEBRAFISH PUBLICATIONS OF LAB MEMBERS
Oprişoreanu, A.M., Smith, H.L., Arya, S., Webster, R., Zhong, Z., Wehner, D., Cardozo, M.J., Becker, T., Talbot, K., Becker, C.G. (2019) Interaction of Axonal Chondrolectin with Collagen XIXa1 Is Necessary for Precise Neuromuscular Junction Formation. Cell Reports. 29:1082-1098.e10
Arribat, Y., Mysiak, K.S., Lescouzères, L., Boizot, A., Ruiz, M., Rossel, M., Bomont, P. (2019) Sonic Hedgehog repression underlies gigaxonin mutation-induced motor deficits in giant axonal neuropathy. The Journal of Clinical Investigation. 129(12):5312-5326
Caldwell, L.J., Davies, N.O., Cavone, L., Mysiak, K.S., Semenova, S.A., Panula, P., Armstrong, J.D., Becker, C.G., Becker, T. (2019) Regeneration of dopaminergic neurons in adult zebrafish depends on immune system activation and differs for distinct populations. The Journal of neuroscience : the official journal of the Society for Neuroscience. 39(24):4694-4713
Bertolini, J.A., Favaro, R., Zhu, Y., Pagin, M., Ngan, C.Y., Wong, C.H., Tjong, H., Vermunt, M.W., Martynoga, B., Barone, C., Mariani, J., Cardozo, M.J., Tabanera, N., Zambelli, F., Mercurio, S., Ottolenghi, S., Robson, P., Creyghton, M.P., Bovolenta, P., Pavesi, G., Guillemot, F., Nicolis, S.K., Wei, C.L. (2019) Mapping the Global Chromatin Connectivity Network for Sox2 Function in Neural Stem Cell Maintenance. Cell Stem Cell. 24:462-476.e6
Tsarouchas, T.M., Wehner, D., Cavone, L., Munir, T., Keatinge, M., Lambertus, M., Underhill, A., Barrett, T., Kassapis, E., Ogryzko, N., Feng, Y., van Ham, T.J., Becker, T., Becker, C.G. (2018) Dynamic control of proinflammatory cytokines Il-1β and Tnf-α by macrophages in zebrafish spinal cord regeneration. Nature communications. 9:4670
Wehner, D., Becker, T., Becker, C.G. (2017) Restoration of anatomical continuity after spinal cord transection depends on Wnt/β-catenin signaling in larval zebrafish. Data in brief. 16:65-70
Drummond, N.J., Davies, N.O., Lovett, J.E., Miller, M.R., Cook, G., Becker, T., Becker, C.G., McPhail, D.B., Kunath, T. (2017) A synthetic cell permeable antioxidant protects neurons against acute oxidative stress. Scientific Reports. 7:11857
Wehner, D., Tsarouchas, T.M., Michael, A., Haase, C., Weidinger, G., Reimer, M.M., Becker, T., Becker, C.G. (2017) Wnt signaling controls pro-regenerative Collagen XII in functional spinal cord regeneration in zebrafish. Nature communications. 8:126
Cardozo, M.J., Mysiak, K.S., Becker, T., Becker, C.G. (2017) Reduce, Reuse, Recycle - Developmental Signals in Spinal Cord Regeneration. Developmental Biology. 432(1):53-62
Boyd, P.J., Tu, W.Y., Shorrock, H.K., Groen, E.J.N., Carter, R.N., Powis, R.A., Thomson, S.R., Thomson, D., Graham, L.C., Motyl, A.A.L., Wishart, T.M., Highley, J.R., Morton, N.M., Becker, T., Becker, C.G., Heath, P.R., Gillingwater, T.H. (2017) Bioenergetic status modulates motor neuron vulnerability and pathogenesis in a zebrafish model of spinal muscular atrophy. PLoS Genetics. 13:e1006744
Powis, R.A., Karyka, E., Boyd, P., Côme, J., Jones, R.A., Zheng, Y., Szunyogova, E., Groen, E.J., Hunter, G., Thomson, D., Wishart, T.M., Becker, C.G., Parson, S.H., Martinat, C., Azzouz, M., Gillingwater, T.H. (2016) Systemic restoration of UBA1 ameliorates disease in spinal muscular atrophy. JCI insight. 1:e87908
Ohnmacht, J., Yang, Y.J., Maurer, G.W., Barreiro-Iglesias, A., Tsarouchas, T.M., Wehner, D., Sieger, D., Becker, C.G., Becker, T. (2016) Spinal motor neurons are regenerated after mechanical lesion and genetic ablation in larval zebrafish. Development (Cambridge, England). 143(9):1464-74
Mysiak, K.S., Barreiro-Iglesias, A., Reimer, M.M., Scott, A.L., Yang, Y., Becker, T., Becker, C.G. (2015) Serotonin promotes motor neuron development and adult regeneration in zebrafish. International journal of developmental neuroscience : the official journal of the International Society for Developmental Neuroscience. 47:51
Barreiro-Iglesias, A., Mysiak, K.S., Scott, A.L., Reimer, M.M., Yang, Y., Becker, C.G., Becker, T. (2015) Serotonin Promotes Development and Regeneration of Spinal Motor Neurons in Zebrafish. Cell Reports. 13:924-932
Greenlees, R., Mihelec, M., Yousoof, S., Speidel, D., Wu, S.K., Rinkwitz, S., Prokudin, I., Perveen, R., Cheng, A., Ma, A., Nash, B., Gillespie, R., Loebel, D.A., Clayton-Smith, J., Lloyd, I.C., Grigg, J.R., Tam, P.P., Yap, A.S., Becker, T.S., Black, G.C., Semina, E., Jamieson, R.V. (2015) Mutations in SIPA1L3 cause eye defects through disruption of cell polarity and cytoskeleton organization. Human molecular genetics. 24(20):5789-804
Boyd, P.J., Cunliffe, V.T., Roy, S., Wood, J.D. (2015) Sonic hedgehog functions upstream of disrupted-in-schizophrenia 1 (disc1): implications for mental illness. Biology Open. 4(10):1336-43
Becker, T., Becker, C.G. (2014) Axonal regeneration in zebrafish. Current opinion in neurobiology. 27C:186-191
Münzel, E., Becker, C.G., Becker, T., Williams, A. (2014) Zebrafish regenerate full thickness optic nerve myelin after demyelination, but this fails with increasing age. Acta neuropathologica communications. 2:77
Cardozo, M.J., Sánchez-Arrones, L., Sandonis, A., Sánchez-Camacho, C., Gestri, G., Wilson, S.W., Guerrero, I., Bovolenta, P. (2014) Cdon acts as a Hedgehog decoy receptor during proximal-distal patterning of the optic vesicle. Nature communications. 5:4272
Wishart, T.M., Mutsaers, C.A., Riessland, M., Reimer, M.M., Hunter, G., Hannam, M.L., Eaton, S.L., Fuller, H.R., Roche, S.L., Somers, E., Morse, R., Young, P.J., Lamont, D.J., Hammerschmidt, M., Joshi, A., Hohenstein, P., Morris, G.E., Parson, S.H., Skehel, P.A., Becker, T., Robinson, I.M., Becker, C.G., Wirth, B., Gillingwater, T.H. (2014) Dysregulation of ubiquitin homeostasis and beta-catenin signaling promote spinal muscular atrophy. J. Clin. Invest.. 124:1821-34
Sleigh, J.N., Barreiro-Iglesias, A., Oliver, P.L., Biba, A., Becker, T., Davies, K.E., Becker, C.G., and Talbot, K. (2014) Chondrolectin affects cell survival and neuronal outgrowth in in vitro and in vivo models of spinal muscular atrophy. Human molecular genetics. 23(4):855-69
Reimer, M.M., Norris, A., Ohnmacht, J., Patani, R., Zhong, Z., Dias, T.B., Kuscha, V., Scott, A.L., Chen, Y.C., Rozov, S., Frazer, S.L., Wyatt, C., Higashijima, S., Patton, E.E., Panula, P., Chandran, S., Becker, T., and Becker, C.G. (2013) Dopamine from the Brain Promotes Spinal Motor Neuron Generation during Development and Adult Regeneration. Developmental Cell. 25(5):478-491
Barreiro-Iglesias, A., Mysiak, K.S., Adrio, F., Rodicio, M.C., Becker, C.G., Becker, T., and Anadón, R. (2013) Distribution of glycinergic neurons in the brain of glycine transporter-2 Tg(glyt2:gfp) transgenic adult zebrafish: Relation with brain-spinal descending systems. The Journal of comparative neurology. 521(2):389-425
Kuscha, V., Frazer, S.L., Dias, T.B., Hibi, M., Becker, T., and Becker, C.G. (2012) Lesion-induced generation of interneuron cell types in specific dorso-ventral domains in the spinal cord of adult zebrafish. The Journal of comparative neurology. 520(16):3604-3616
Kuscha, V., Barreiro-Iglesias, A., Becker, C.G., and Becker, T. (2012) Plasticity of tyrosine hydroxylase and serotonergic systems in the regenerating spinal cord of adult zebrafish. The Journal of comparative neurology. 520(5):933-951
Zhong, Z., Ohnmacht, J., Reimer, M.M., Bach, I., Becker, T., and Becker, C.G. (2012) Chondrolectin mediates growth cone interactions of motor axons with an intermediate target. The Journal of neuroscience : the official journal of the Society for Neuroscience. 32(13):4426-4439
Dias, T.B., Yang, Y.J., Ogai, K., Becker, T., and Becker, C.G. (2012) Notch signaling controls generation of motor neurons in the lesioned spinal cord of adult zebrafish. The Journal of neuroscience : the official journal of the Society for Neuroscience. 32(9):3245-3252
Münzel, E.J., Schaefer, K., Obirei, B., Kremmer, E., Burton, E.A., Kuscha, V., Becker, C.G., Brösamle, C., Williams, A., and Becker, T. (2012) Claudin k is specifically expressed in cells that form myelin during development of the nervous system and regeneration of the optic nerve in adult zebrafish. Glia. 60(2):253-70
Zhong, Z., Ma, H., Taniguchi-Ishigaki, N., Nagarajan, L., Becker, C.G., Bach, I., and Becker, T. (2011) SSDP cofactors regulate neural patterning and differentiation of specific axonal projections. Developmental Biology. 349(2):213-224
Wyatt, C., Ebert, A., Reimer, M.M., Rasband, K., Hardy, M., Chien, C.B., Becker, T., and Becker, C.G. (2010) Analysis of the astray/robo2 Zebrafish Mutant Reveals that Degenerating Tracts Do Not Provide Strong Guidance Cues for Regenerating Optic Axons. The Journal of neuroscience : the official journal of the Society for Neuroscience. 30(41):13838-13849
O'Brien, G.S., Martin, S.M., Söllner, C., Wright, G.J., Becker, C.G., Portera-Cailliau, C., and Sagasti, A. (2009) Developmentally Regulated Impediments to Skin Reinnervation by Injured Peripheral Sensory Axon Terminals. Current biology : CB. 19(24):2086-2090
Reimer, M.M., Kuscha, V., Wyatt, C., Sörensen, I., Frank, R.E., Knüwer, M., Becker, T., and Becker, C.G. (2009) Sonic hedgehog is a polarized signal for motor neuron regeneration in adult zebrafish. The Journal of neuroscience : the official journal of the Society for Neuroscience. 29(48):15073-15082
Reimer, M.M., Sörensen, I., Kuscha, V., Frank, R.E., Liu, C., Becker, C.G., and Becker, T. (2008) Motor neuron regeneration in adult zebrafish. The Journal of neuroscience : the official journal of the Society for Neuroscience. 28(34):8510-8516
Becker, C.G., and Becker, T. (2008) Adult zebrafish as a model for successful central nervous system regeneration. Restorative neurology and neuroscience. 26(2-3):71-80
Güngör, C., Taniguchi-Ishigaki, N., Ma, H., Drung, A., Tursun, B., Ostendorff, H.P., Bossenz, M., Becker, C.G., Becker, T., and Bach, I. (2007) Proteasomal selection of multiprotein complexes recruited by LIM homeodomain transcription factors. Proceedings of the National Academy of Sciences of the United States of America. 104(38):15000-15005
Wolman, M.A., Regnery, A.M., Becker, T., Becker, C.G., and Halloran, M.C. (2007) Semaphorin3D regulates axon axon interactions by modulating levels of L1 cell adhesion molecule. The Journal of neuroscience : the official journal of the Society for Neuroscience. 27(36):9653-9663
Becker, C.G., and Becker, T. (2007) Growth and pathfinding of regenerating axons in the optic projection of adult fish. Journal of neuroscience research. 85(12):2793-2799
Schweitzer, J., Gimnopoulos, D., Lieberoth, B.C., Pogoda, H.M., Feldner, J., Ebert, A., Schachner, M., Becker, T., and Becker, C.G. (2007) Contactin1a expression is associated with oligodendrocyte differentiation and axonal regeneration in the central nervous system of zebrafish. Molecular and cellular neurosciences. 35(2):194-207
Feldner, J., Reimer, M.M., Schweitzer, J., Wendik, B., Meyer, D., Becker, T., and Becker, C.G. (2007) PlexinA3 restricts spinal exit points and branching of trunk motor nerves in embryonic zebrafish. The Journal of neuroscience : the official journal of the Society for Neuroscience. 27(18):4978-4983
Schweitzer, J., Becker, T., Schachner, M., Nave, K.A., and Werner, H. (2006) Evolution of myelin proteolipid proteins: Gene duplication in teleosts and expression pattern divergence. Molecular and cellular neurosciences. 31(1):161-177
Feldner, J., Becker, T., Goishi, K., Schweitzer, J., Lee, P., Schachner, M., Klagsbrun, M., and Becker, C.G. (2005) Neuropilin-1a is involved in trunk motor axon outgrowth in embryonic zebrafish. Developmental dynamics : an official publication of the American Association of Anatomists. 234(3):535-549
Schweitzer, J., Becker, T., Lefebvre, J., Granato, M., Schachner, M., and Becker, C.G. (2005) Tenascin-C is involved in motor axon outgrowth in the trunk of developing zebrafish. Developmental dynamics : an official publication of the American Association of Anatomists. 234(3):550-566
Becker, T., Lieberoth, B.C., Becker, C.G., and Schachner, M. (2005) Differences in the regenerative response of neuronal cell populations and indications for plasticity in intraspinal neurons after spinal cord transection in adult zebrafish. Molecular and cellular neurosciences. 30(2):265-278
Schweitzer, J., Becker, C.G., Schachner, M., and Becker, T. (2005) Expression of collapsin response mediator proteins in the nervous system of embryonic zebrafish. Gene expression patterns : GEP. 5(6):809-816
Becker, C.G., Lieberoth, B.C., Morellini, F., Feldner, J., Becker, T., and Schachner, M. (2004) L1.1 is involved in spinal cord regeneration in adult zebrafish. The Journal of neuroscience : the official journal of the Society for Neuroscience. 24(36):7837-7842
Becker, C.G., Schweitzer, J., Feldner, J., Schachner, M., and Becker, T. (2004) Tenascin-R as a repellent guidance molecule for newly growing and regenerating optic axons in adult zebrafish. Molecular and cellular neurosciences. 26(3):376-389
Bovenkamp, D.E., Goishi, K., Bahary, N., Davidson, A.J., Zhou, Y., Becker, T., Becker, C.G., Zon, L.I., and Klagsbrun, M. (2004) Expression and mapping of duplicate neuropilin-1 and neuropilin-2 genes in developing zebrafish. Gene expression patterns : GEP. 4(4):361-370
Becker, C.G., Schweitzer, J., Feldner, J., Becker, T., and Schachner, M. (2003) Tenascin-R as a repellent guidance molecule for developing optic axons in zebrafish. The Journal of neuroscience : the official journal of the Society for Neuroscience. 23(15):6232-6237
Becker, T., McLane, M.A., and Becker, C.G. (2003) Integrin antagonists affect growth and pathfinding of ventral motor nerves in the trunk of embryonic zebrafish. Molecular and cellular neurosciences. 23(1):54-68
Schweitzer, J., Becker, T., Becker, C.G., and Schachner, M. (2003) Expression of protein zero is increased in lesioned axon pathways in the central nervous system of adult zebrafish. Glia. 41(3):301-317
Becker, T., Bossenz, M., Tursun, B., Schlüter, A., Peters, M.A., Becker, C.G., Ostendorff, H.P., and Bach, I. (2003) Comparing protein stabilities during zebrafish embryogenesis. Methods in cell science : an official journal of the Society for In Vitro Biology. 25(1-2):85-89
Lieberoth, B.C., Becker, C.G., and Becker, T. (2003) Double labeling of neurons by retrograde axonal tracing and non-radioactive in situ hybridization in the CNS of adult zebrafish. Methods in cell science : an official journal of the Society for In Vitro Biology. 25(1-2):65-70
Gimnopoulos, D., Becker, C.G., Ostendorff, H.P., Bach, I., Schachner, M., and Becker, T. (2002) Expression of the zebrafish recognition molecule F3/F11/contactin in a subset of differentiating neurons is regulated by cofactors associated with LIM domains. Mechanisms of Development. 119:S135-S141
Becker, T., Ostendorff, H., Bossenz, M., Schlüter, A., Becker, C.G., Peirano, R.I., and Bach, I. (2002) Multiple functions of LIM domain-binding CLIM/NLI/Ldb cofactors during zebrafish development. Mechanisms of Development. 117(1-2):75-85
Becker, C.G. and Becker, T. (2002) Repellent guidance of regenerating optic axons by chondroitin sulfate glycosaminoglycans in zebrafish. The Journal of neuroscience : the official journal of the Society for Neuroscience. 22(3):842-853
Vendrell, V., Gimnopoulos, D., Becker, T., and Schimmang, T. (2001) Functional analysis of FGF3 during zebrafish inner ear development. The International journal of developmental biology. :S105-S106
Becker, T., Becker, C.G., Schachner, M., and Bernhardt, R.R. (2001) Antibody to the HNK-1 glycoepitope affects fasciculation and axonal pathfinding in the developing posterior lateral line nerve of embryonic zebrafish. Mechanisms of Development. 109(1):37-49
Becker, T. and Becker, C.G. (2001) Regenerating descending axons preferentially reroute to the gray matter in the presence of a general macrophage/microglial reaction caudal to a spinal transection in adult zebrafish. The Journal of comparative neurology. 433(1):131-147
Becker, C.G., Meyer, R.L., and Becker, T. (2000) Gradients of ephrin-A2 and ephrin-A5b mRNA during retinotopic regeneration of the optic projection in adult zebrafish. The Journal of comparative neurology. 427(3):469-483
Becker, C.G. and Becker, T. (2000) Chondroitinase injection into the brain leads to misrouting of regenerating optic fibers into the posterior pretectal nucleus in adult zebrafish. The European journal of neuroscience. 12:289
Becker, T., R.R. Bernhardt, E. Reinhard, M.F. Wullimann, E. Tongiorgi, and M. Schachner (1998) Readiness of zebrafish brain neurons to regenerate a spinal axon correlates with differential expression of specific cell recognition molecules. The Journal of neuroscience : the official journal of the Society for Neuroscience. 18:5789-5803
Becker, T., Wullimann, M.F., Becker, C.G., Bernhardt, R.R., and Schachner, M. (1997) Axonal regrowth after spinal cord transection in adult zebrafish. The Journal of comparative neurology. 377(4):577-595