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Elly Tanaka

Our group seeks to understand the cellular mechanisms underlying salamander limb and spinal cord regeneration as a model for how successful regeneration occurs in a vertebrate. This model acts as a starting point to rigorously investigate how mammals such as mice have lost regeneration capabilities over evolution. In addition, these studies act as a springboard to design novel strategies for regenerating or replacing mammalian tissues. Toward that end we have engineered three-dimensional spinal cord tissue from mouse embryonic stem cells and retinal pigment epithelia from human embryonic stem cells.

Publications

Nowoshilow, S., Schloissnig, S., Fei, JF., Dahl, A., Pang, AWC., Pippel, M., Winkler, S., Hastie, AR., Young, G., Roscito, JG., Falcon, F., Knapp, D., Powell, S., Cruz, A., Cao, H., Habermann, B., Hiller, M., Tanaka, EM., Myers, EW. (2018) The axolotl genome and the evolution of key tissue formation regulators. Nature. 554(7690):50-55
Oliveira, CR., Lemaitre, R., Murawala, P., Tazaki, A., Drechsel, DN., Tanaka, EM. (2018) Pseudotyped baculovirus is an effective gene expression tool for studying molecular function during axolotl limb regeneration. Dev Biol. 433(2):262-275
Fei, JF., Schuez, M., Knapp, D., Taniguchi, Y., Drechsel, DN., Tanaka, EM. (2017) Efficient gene knockin in axolotl and its use to test the role of satellite cells in limb regeneration. Proc Natl Acad Sci U S A.
Ishihara, K., Ranga, A., Lutolf, MP., Tanaka, EM., Meinhardt, A. (2017) Reconstitution of a Patterned Neural Tube from Single Mouse Embryonic Stem Cells. Methods Mol Biol. 1597:43-55
Kaucka, M., Zikmund, T., Tesarova, M., Gyllborg, D., Hellander, A., Jaros, J., Kaiser, J., Petersen, J., Szarowska, B., Newton, PT., Dyachuk, V., Li, L., Qian, H., Johansson, AS., Mishina, Y., Currie, J., Tanaka, EM., Erickson, A., Dudley, A., Brismar, H., Southam, P., Coen, E., Chen, M., Weinstein, LS., Hampl, A., Arenas, E., Chagin, AS., Fried, K., Adameyko, I. (2017) Oriented clonal cell dynamics enables accurate growth and shaping of vertebrate cartilage. Elife. 6
Ocaña, OH., Coskun, H., Minguillón, C., Murawala, P., Tanaka, EM., Galcerán, J., Muñoz-Chápuli, R., Nieto, MA. (2017) A right-handed signalling pathway drives heart looping in vertebrates. Nature. 549(7670):86-90
Russell, JJ., Theriot, JA., Sood, P., Marshall, WF., Landweber, LF., Fritz-Laylin, L., Polka, JK., Oliferenko, S., Gerbich, T., Gladfelter, A., Umen, J., Bezanilla, M., Lancaster, MA., He, S., Gibson, MC., Goldstein, B., Tanaka, EM., Hu, CK., Brunet, A. (2017) Non-model model organisms. BMC Biol. 15(1):55
Wagner, I., Wang, H., Weissert, PM., Straube, WL., Shevchenko, A., Gentzel, M., Brito, G., Tazaki, A., Oliveira, C., Sugiura, T., Shevchenko, A., Simon, A., Drechsel, DN., Tanaka, EM. (2017) Serum Proteases Potentiate BMP-Induced Cell Cycle Re-entry of Dedifferentiating Muscle Cells during Newt Limb Regeneration. Dev Cell. 40(6):608-617.e6
Currie, JD., Kawaguchi, A., Traspas, RM., Schuez, M., Chara, O., Tanaka, EM. (2016) Live Imaging of Axolotl Digit Regeneration Reveals Spatiotemporal Choreography of Diverse Connective Tissue Progenitor Pools. Dev Cell. 39(4):411-423
Nacu, E., Gromberg, E., Oliveira, CR., Drechsel, D., Tanaka, EM. (2016) FGF8 and SHH substitute for anterior-posterior tissue interactions to induce limb regeneration. Nature. 533(7603):407-10
Ranga, A., Girgin, M., Meinhardt, A., Eberle, D., Caiazzo, M., Tanaka, EM., Lutolf, MP. (2016) Neural tube morphogenesis in synthetic 3D microenvironments. Proc Natl Acad Sci U S A. 113(44):E6831-E6839
Reddien, PW., Tanaka, EM. (2016) Editorial overview: Cell reprogramming, regeneration and repair. Curr Opin Genet Dev. 40:iv-vi
Rost, F., Albors, AR., Mazurov, V., Brusch, L., Deutsch, A., Tanaka, EM., Chara, O. (2016) Accelerated cell divisions drive the outgrowth of the regenerating spinal cord in axolotls. Elife. 5
Sugiura, T., Wang, H., Barsacchi, R., Simon, A., Tanaka, EM. (2016) MARCKS-like protein is an initiating molecule in axolotl appendage regeneration. Nature. 531(7593):237-40
Khattak, S., Tanaka, EM. (2015) Transgenesis in axolotl (Ambystoma mexicanum). Methods Mol Biol. 1290:269-77
Rodrigo Albors, A., Tanaka, EM. (2015) High-efficiency electroporation of the spinal cord in larval axolotl. Methods Mol Biol. 1290:115-25
Rodrigo Albors, A., Tazaki, A., Rost, F., Nowoshilow, S., Chara, O., Tanaka, EM. (2015) Planar cell polarity-mediated induction of neural stem cell expansion during axolotl spinal cord regeneration. Elife. 4:e10230
Vincent, CD., Rost, F., Masselink, W., Brusch, L., Tanaka, EM. (2015) Cellular dynamics underlying regeneration of appropriate segment number during axolotl tail regeneration. BMC Dev Biol. 15:48
Ader, M., Tanaka, EM. (2014) Modeling human development in 3D culture. Curr Opin Cell Biol. 31:23-8
Carido, M., Zhu, Y., Postel, K., Benkner, B., Cimalla, P., Karl, MO., Kurth, T., Paquet-Durand, F., Koch, E., Münch, TA., Tanaka, EM., Ader, M. (2014) Characterization of a mouse model with complete RPE loss and its use for RPE cell transplantation. Invest Ophthalmol Vis Sci. 55(8):5431-44
Chara, O., Tanaka, EM., Brusch, L. (2014) Mathematical modeling of regenerative processes. Curr Top Dev Biol. 108:283-317
Fei, JF., Schuez, M., Tazaki, A., Taniguchi, Y., Roensch, K., Tanaka, EM. (2014) CRISPR-mediated genomic deletion of Sox2 in the axolotl shows a requirement in spinal cord neural stem cell amplification during tail regeneration. Stem Cell Reports. 3(3):444-59
Khattak, S., Murawala, P., Andreas, H., Kappert, V., Schuez, M., Sandoval-Guzmán, T., Crawford, K., Tanaka, EM. (2014) Optimized axolotl (Ambystoma mexicanum) husbandry, breeding, metamorphosis, transgenesis and tamoxifen-mediated recombination. Nat Protoc. 9(3):529-40
Khattak, S., Schuez, M., Richter, T., Knapp, D., Haigo, SL., Sandoval-Guzmán, T., Hradlikova, K., Duemmler, A., Kerney, R., Tanaka, EM. (2014) Germline Transgenic Methods for Tracking Cells and Testing Gene Function during Regeneration in the Axolotl. Stem Cell Reports. 2(2):243
Meinhardt, A., Eberle, D., Tazaki, A., Ranga, A., Niesche, M., Wilsch-Bräuninger, M., Stec, A., Schackert, G., Lutolf, M., Tanaka, EM. (2014) 3D reconstitution of the patterned neural tube from embryonic stem cells. Stem Cell Reports. 3(6):987-99
Sandoval-Guzmán, T., Wang, H., Khattak, S., Schuez, M., Roensch, K., Nacu, E., Tazaki, A., Joven, A., Tanaka, EM., Simon, A. (2014) Fundamental differences in dedifferentiation and stem cell recruitment during skeletal muscle regeneration in two salamander species. Cell Stem Cell. 14(2):174-87
Jászai, J., Graupner, S., Tanaka, EM., Funk, RH., Huttner, WB., Brand, M., Corbeil, D. (2013) Spatial distribution of prominin-1 (CD133)-positive cells within germinative zones of the vertebrate brain. PLoS One. 8(5):e63457
Khattak, S., Sandoval-Guzmán, T., Stanke, N., Protze, S., Tanaka, EM., Lindemann, D. (2013) Foamy virus for efficient gene transfer in regeneration studies. BMC Dev Biol. 13:17
Knapp, D., Schulz, H., Rascon, CA., Volkmer, M., Scholz, J., Nacu, E., Le, M., Novozhilov, S., Tazaki, A., Protze, S., Jacob, T., Hubner, N., Habermann, B., Tanaka, EM. (2013) Comparative transcriptional profiling of the axolotl limb identifies a tripartite regeneration-specific gene program. PLoS One. 8(5):e61352
Kragl, M., Roensch, K., Nüsslein, I., Tazaki, A., Taniguchi, Y., Tarui, H., Hayashi, T., Agata, K., Tanaka, EM. (2013) Muscle and connective tissue progenitor populations show distinct Twist1 and Twist3 expression profiles during axolotl limb regeneration. Dev Biol. 373(1):196-204
Nacu, E., Glausch, M., Le, HQ., Damanik, FF., Schuez, M., Knapp, D., Khattak, S., Richter, T., Tanaka, EM. (2013) Connective tissue cells, but not muscle cells, are involved in establishing the proximo-distal outcome of limb regeneration in the axolotl. Development. 140(3):513-8
Roensch, K., Tazaki, A., Chara, O., Tanaka, EM. (2013) Progressive specification rather than intercalation of segments during limb regeneration. Science. 342(6164):1375-9
Simon, A., Tanaka, EM. (2013) Limb regeneration. Wiley Interdiscip Rev Dev Biol. 2(2):291-300
Stewart, R., Rascón, CA., Tian, S., Nie, J., Barry, C., Chu, LF., Ardalani, H., Wagner, RJ., Probasco, MD., Bolin, JM., Leng, N., Sengupta, S., Volkmer, M., Habermann, B., Tanaka, EM., Thomson, JA., Dewey, CN. (2013) Comparative RNA-seq analysis in the unsequenced axolotl: the oncogene burst highlights early gene expression in the blastema. PLoS Comput Biol. 9(3):e1002936
Zhu, Y., Carido, M., Meinhardt, A., Kurth, T., Karl, MO., Ader, M., Tanaka, EM. (2013) Three-dimensional neuroepithelial culture from human embryonic stem cells and its use for quantitative conversion to retinal pigment epithelium. PLoS One. 8(1):e54552
Epperlein, HH., Khattak, S., Knapp, D., Tanaka, EM., Malashichev, YB. (2012) Neural crest does not contribute to the neck and shoulder in the axolotl (Ambystoma mexicanum). PLoS One. 7(12):e52244
Knapp, D., Tanaka, EM. (2012) Regeneration and reprogramming. Curr Opin Genet Dev. 22(5):485-93
McHedlishvili, L., Mazurov, V., Grassme, KS., Goehler, K., Robl, B., Tazaki, A., Roensch, K., Duemmler, A., Tanaka, EM. (2012) Reconstitution of the central and peripheral nervous system during salamander tail regeneration. Proc Natl Acad Sci U S A. 109(34):E2258-66
McHedlishvili, L., Mazurov, V., Tanaka, EM. (2012) Reconstitution of the central nervous system during salamander tail regeneration from the implanted neurospheres. Methods Mol Biol. 916:197-202
Murawala, P., Tanaka, EM., Currie, JD. (2012) Regeneration: the ultimate example of wound healing. Semin Cell Dev Biol. 23(9):954-62
Plath, K., Srivastava, D., Alvarez-Buylla, A., Tanaka, EM., Kriegstein, AR. (2012) Stem cells in the land of the rising sun: ISSCR 2012. Cell Stem Cell. 11(5):607-14
Protze, S., Khattak, S., Poulet, C., Lindemann, D., Tanaka, EM., Ravens, U. (2012) A new approach to transcription factor screening for reprogramming of fibroblasts to cardiomyocyte-like cells. J Mol Cell Cardiol. 53(3):323-32
Tanaka, EM. (2012) Regenerative biology: Skin, heal thyself. Nature. 489(7417):508-10
Tapia, N., Reinhardt, P., Duemmler, A., Wu, G., Araúzo-Bravo, MJ., Esch, D., Greber, B., Cojocaru, V., Rascon, CA., Tazaki, A., Kump, K., Voss, R., Tanaka, EM., Schöler, HR. (2012) Reprogramming to pluripotency is an ancient trait of vertebrate Oct4 and Pou2 proteins. Nat Commun. 3:1279
Campbell, LJ., Suárez-Castillo, EC., Ortiz-Zuazaga, H., Knapp, D., Tanaka, EM., Crews, CM. (2011) Gene expression profile of the regeneration epithelium during axolotl limb regeneration. Dev Dyn. 240(7):1826-40
Jászai, J., Fargeas, CA., Graupner, S., Tanaka, EM., Brand, M., Huttner, WB., Corbeil, D. (2011) Distinct and conserved prominin-1/CD133-positive retinal cell populations identified across species. PLoS One. 6(3):e17590
Nacu, E., Tanaka, EM. (2011) Limb regeneration: a new development? Annu Rev Cell Dev Biol. 27:409-40
Tanaka, EM., Reddien, PW. (2011) The cellular basis for animal regeneration. Dev Cell. 21(1):172-85
Antos, CL., Tanaka, EM. (2010) Vertebrates that regenerate as models for guiding stem cels. Adv Exp Med Biol. 695:184-214
Berg, DA., Kirkham, M., Beljajeva, A., Knapp, D., Habermann, B., Ryge, J., Tanaka, EM., Simon, A. (2010) Efficient regeneration by activation of neurogenesis in homeostatically quiescent regions of the adult vertebrate brain. Development. 137(24):4127-34
Gin, E., Tanaka, EM., Brusch, L. (2010) A model for cyst lumen expansion and size regulation via fluid secretion. J Theor Biol. 264(3):1077-88
Ishizaki, K., Suzuki, K., Mito, T., Tanaka, EM., Sato, S. (2010) Morphologic, functional, and occlusal characterization of mandibular lateral displacement malocclusion. Am J Orthod Dentofacial Orthop. 137(4):454.e1-9; discussion 454-5
Khattak, S., Richter, T., Tanaka, EM. (2009) Generation of transgenic axolotls (Ambystoma mexicanum). Cold Spring Harb Protoc. 2009(8):pdb.prot5264
Khattak, S., Tanaka, EM. (2009) Axolotl (Ambystoma mexicanum) in vitro fertilization. Cold Spring Harb Protoc. 2009(8):pdb.prot5263
Kragl, M., Tanaka, EM. (2009) Axolotl (Ambystoma mexicanum) limb and tail amputation. Cold Spring Harb Protoc. 2009(8):pdb.prot5267
Kragl, M., Tanaka, EM. (2009) Grafting axolotl (Ambystoma mexicanum) limb skin and cartilage from GFP+ donors to normal hosts. Cold Spring Harb Protoc. 2009(8):pdb.prot5266
Nacu, E., Knapp, D., Tanaka, EM., Epperlein, HH. (2009) Axolotl (Ambystoma mexicanum) embryonic transplantation methods. Cold Spring Harb Protoc. 2009(8):pdb.prot5265
Sasaguri, K., Ishizaki-Takeuchi, R., Kuramae, S., Tanaka, EM., Sakurai, T., Sato, S. (2009) The temporomandibular joint in a rheumatoid arthritis patient after orthodontic treatment. Angle Orthod. 79(4):804-11
Tanaka, EM., Ferretti, P. (2009) Considering the evolution of regeneration in the central nervous system. Nat Rev Neurosci. 10(10):713-23
Voss, SR., Epperlein, HH., Tanaka, EM. (2009) Ambystoma mexicanum, the axolotl: a versatile amphibian model for regeneration, development, and evolution studies. Cold Spring Harb Protoc. 2009(8):pdb.emo128
Kragl, M., Knapp, D., Nacu, E., Khattak, S., Schnapp, E., Epperlein, HH., Tanaka, EM. (2008) Novel insights into the flexibility of cell and positional identity during urodele limb regeneration. Cold Spring Harb Symp Quant Biol. 73:583-92
Lynch, SL., Boon, AJ., Smith, J., Harper, CM., Tanaka, EM. (2008) Complications of needle electromyography: hematoma risk and correlation with anticoagulation and antiplatelet therapy. Muscle Nerve. 38(4):1225-30
Tanaka, EM., Sato, S. (2008) Longitudinal alteration of the occlusal plane and development of different dentoskeletal frames during growth. Am J Orthod Dentofacial Orthop. 134(5):602.e1-11; discussion 602-3
Tanaka, EM., Weidinger, G. (2008) Micromanaging regeneration. Genes Dev. 22(6):700-5
Tanaka, EM., Weidinger, G. (2008) Heads or tails: can Wnt tell which one is up? Nat Cell Biol. 10(2):122-4
Lööf, S., Straube, WL., Drechsel, D., Tanaka, EM., Simon, A. (2007) Plasticity of mammalian myotubes upon stimulation with a thrombin-activated serum factor. Cell Cycle. 6(9):1096-101
Straube, WL., Tanaka, EM. (2006) Reversibility of the differentiated state: regeneration in amphibians. Artif Organs. 30(10):743-55
da Silva, AV., Pezerico, SB., de Lima, VY., d'Arc Moretti, L., Pinheiro, JP., Tanaka, EM., Ribeiro, MG., Langoni, H. (2005) Genotyping of Toxoplasma gondii strains isolated from dogs with neurological signs. Vet Parasitol. 127(1):23-7
Echeverri, K., Tanaka, EM. (2005) Proximodistal patterning during limb regeneration. Dev Biol. 279(2):391-401
Mercader, N., Tanaka, EM., Torres, M. (2005) Proximodistal identity during vertebrate limb regeneration is regulated by Meis homeodomain proteins. Development. 132(18):4131-42
Habermann, B., Bebin, AG., Herklotz, S., Volkmer, M., Eckelt, K., Pehlke, K., Epperlein, HH., Schackert, HK., Wiebe, G., Tanaka, EM. (2004) An Ambystoma mexicanum EST sequencing project: analysis of 17,352 expressed sequence tags from embryonic and regenerating blastema cDNA libraries. Genome Biol. 5(9):R67
Echeverri, K., Tanaka, EM. (2003) Electroporation as a tool to study in vivo spinal cord regeneration. Dev Dyn. 226(2):418-25
Tanaka, EM. (2003) Cell differentiation and cell fate during urodele tail and limb regeneration. Curr Opin Genet Dev. 13(5):497-501
Tanaka, EM. (2003) Regeneration: if they can do it, why can't we? Cell. 113(5):559-62
Echeverri, K., Tanaka, EM. (2002) Ectoderm to mesoderm lineage switching during axolotl tail regeneration. Science. 298(5600):1993-6
Echeverri, K., Tanaka, EM. (2002) Mechanisms of muscle dedifferentiation during regeneration. Semin Cell Dev Biol. 13(5):353-60
Velloso, CP., Kumar, A., Tanaka, EM., Brockes, JP. (2000) Generation of mononucleate cells from post-mitotic myotubes proceeds in the absence of cell cycle progression. Differentiation. 66(4-5):239-46
Tanaka, EM., Drechsel, DN., Brockes, JP. (1999) Thrombin regulates S-phase re-entry by cultured newt myotubes. Curr Biol. 9(15):792-9
Tanaka, EM., Brockes, JP. (1998) A target of thrombin activation promotes cell cycle re-entry by urodele muscle cells. Wound Repair Regen. 6(4):371-81
Tanaka, EM., Gann, AA., Gates, PB., Brockes, JP. (1997) Newt myotubes reenter the cell cycle by phosphorylation of the retinoblastoma protein. J Cell Biol. 136(1):155-65
Odde, DJ., Tanaka, EM., Hawkins, SS., Buettner, HM. (1996) Stochastic dynamics of the nerve growth cone and its microtubules during neurite outgrowth. Biotechnol Bioeng. 50(4):452-61
Tanaka, EM., Gann, AF. (1995) Limb development. The budding role of FGF. Curr Biol. 5(6):594-7
Tanaka, EM., Kirschner, MW. (1991) Microtubule behavior in the growth cones of living neurons during axon elongation. J Cell Biol. 115(2):345-63