GRK 1104:  From Cells to Organs: Molecular Mechanisms of Organogenesis

• Subject Area: Basic Research in Biology and Medicine
• Term: from 2005 to 2014
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 455540

• Final Report Year: 2015

Final Report Abstract

The control of tissue regeneration from endogenous cells as well as application of stem cells in regenerative medicine requires a detailed knowledge of the molecular mechanisms that regulate differentiation of pluripotent cells into specific cell types and govern their organization into tissues and organs. In the Research Training Group 1104 (GRK 1104), basic scientists from the Faculty of Biology of the University of Freiburg and the Max Planck Institute of Immunobiology and Epigenetics have joined forces with biomedical scientists from the preclinical and clinical departments of Freiburg University Hospital to establish a research program addressing questions related to patterning, cell specification, cell commitment, cell differentiation and the regulation of morphogenesis in a wide spectrum of organs. Using different model organisms including mouse, zebrafish, chick, Xenopus, C. elegans and Drosophila, a broad spectrum of methods including genetic, biochemical, molecular, cell biology and large scale „omics“ approaches was applied. The results of this research program have significantly improved our mechanistic insight into the development of several organs and tissues including the urogenital system, neuronal tissues, lymphoid follicles and innate lymphocyte populations and interactions of the latter with the intestinal system. In addition important regulatory principles were elucidated. Research in Drosophila, for example, revealed a mechanism how the formation of signaling gradients is coupled to the interpretation of such gradient to equip organ formation with robustness and scaling properties. To optimally prepare Ph.D. student for a career in research a qualification program was established that offered students a broad interdisciplinary training in up to date methods and concepts of modern biomedical research with a focus on developmental biology, cell differentiation and organogenesis. The qualification program combined seminars, lectures and retreats with practical training modules. All students participated in a weekly seminar that served as a central platform of the program for the presentation and discussion of the progress of the Ph.D. projects and for exchanging experience with experimental approaches, experimental protocols and reagents. The students also participate in a guest speaker seminar series and in the program retreats. The rest of the study program was flexible and tailored to the individual training needs. Each student was supervised by a “Thesis Advisory Committee” consisting of the direct thesis supervisor and two other group leaders who attend the student’s progress reports and provided advice on future directions and decisions.

Publications

• (2006) Genetic analysis of dopaminergic system development in zebrafish, J Neural Transm Suppl 2006:61-6
  Ryu S., Holzschuh J., Mahler J., and Driever W
  
• (2006) Identification of a ‘genuine’ mammalian homolog of nematodal CED-4: is the hunt over or do we need better guns? Cell Death and Differentiation; 13 1310-1317
  Manoharan, A., Kiefer T., Leist, S., Schrader, K., Urban, C., Walter, D., Maurer, U. and Borner, C.
  
• (2006). Axonemal localization of the dynein component DNAH5 is not altered in secondary ciliary dyskinesia. Pediatr. Res. 59, 418-422
  Olbrich, H., Horváth, J., Fekete, A., Loges, N.T., Storm van's Gravesande, K., Blum, A., Hörmann, K., Omran, H.
  
• (2006). DNAH5 mutations are a common cause of primary ciliary dyskinesia with outer dynein arm defects. Am. J. Respir. Crit. Care Med. 15; 120-126
  Hornef, N., Olbrich, H., Horvath, J., Zariwala, M.A., Fliegauf, M., Loges, N.T., Wildhaber, J., Noone, P.G., Kennedy, M., Antonarakis, S.E., Blouin, J.L., Bartoloni, L., Nüsslein, T., Ahrens, P., Griese, M., Kuhl, H., Sudbrak, R., Knowles, M.R., Reinhardt, R., Omran, H.
  
• (2006). Expression of the avian gene cNOC2 encoding nucleolar complex associated protein 2 during embryonic development. Anat Embryol (Berl) 211, 649-657
  Zhang, X., Dai, F., Weise, C., Yusuf, F., Bonafede, A., Morosan-Puopolo, G., Rehimi, R., Wang, J., and Brand-Saberi, B.
  
• (2006). Inhibitors of CXCR4 affect the migration and fate of CXCR4+ progenitors in the developing limb of chick embryos. Dev Dyn 235, 3007-3015
  Yusuf, F., Rehimi, R., Morosan-Puopolo, G., Dai, F., Zhang, X., and Brand-Saberi, B.
  
• (2006). Mutations in ACY1, the gene encoding aminoacylase 1, cause a novel inborn error of metabolism. Am. J. Hum. Genet. 78, 401-409
  Sass, J.O., Mohr, V., Olbrich, H., Engelke, U., Horvath, J., Fliegauf, M., Loges, N.T., Schweitzer-Krantz, S., Moebus, R., Weiler, P., Kispert, A., Superti-Furga, A., Wevers, R.A., Omran, H.
  
• (2006). Mutations of DNAI1 in primary ciliary dyskinesia: evidence of founder effect in a common mutation. Am. J. Respir. Crit. Care Med. 174, 858-866
  Zariwala, M.A., Leigh, M.W., Ceppa, F., Kennedy, M.P., Noone, P.G., Carson, J.L., Hazucha, M.J., Lori, A., Horvath, J., Olbrich, H., Loges, N.T., Bridoux, A.M., Pennarun, G., Duriez, B., Escudier, E., Mitchison, H.M., Chodhari, R., Chung, E.M., Morgan, L.C., de Iongh, R.U., Rutland, J., Pradal, U., Omran, H., Amselem, S., Knowles, M.R.
  
• (2006). Somite compartments in anamniotes. Anatomy and embryology 211 Suppl 1, 9-19
  Scaal, M., and Wiegreffe, C.
  
• (2007) Expression of the zebrafish intermediate neurofilament Nestin in the developing nervous system and in neural proliferation zones at postembryonic stages. BMC Developmental Biology, 7:89
  Mahler, J., Driever, W.
  
• (2007) Orthopedia Homedomain Protein is Essential for Diencephalic Dopaminergic Neuron Development, Current Biology 17,1-8
  Ryu S., Mahler J., Acampora D., Holzschuh J., Erhardt S., Omodei D., Simeone A., and Driever W.
  
• (2007). A mutation in CHN-1/CHIP suppresses muscle degeneration in Caenorhabditis elegans. Dev. Biol. 312, 193-202
  Nyamsuren O, Faggionato D, Loch W, Schulze E, Baumeister R
  
• (2007). Further evidence for a somatic KRAS mutation in a pilocytic astrocytoma., Neuropediatrics. 38, 61-63
  Janzarik, W.G., Kratz, C.P., Loges, N.T., Olbrich, H., Klein, C., Schäfer, T., Scheurlen, W., Roggendorf, W., Weiller, C., Niemeyer, C., Korinthenberg, R., Pfister, S., Omran, H.
  
• (2007). Sclerotomal origin of smooth muscle cells in the wall of the avian dorsal aorta. Dev Dyn 236, 2578-2585
  Wiegreffe, C., Christ, B., Huang, R., and Scaal, M.
  
• (2008). Direct inhibition of the longevitypromoting factor SKN-1 by insulin-like signaling in C. elegans. Cell 132,1025-38
  Tullet, J.M., Hertweck, M., An, J.H., Baker, J., Hwang, J.Y., Liu, S., Oliveira, R.P., Baumeister, R., Blackwell, T.K.
  
• (2008). DNAI2 Mutations Cause Primary Ciliary Dyskinesia with Defects in the Outer Dynein Arm. Am J Hum Genet 83, 1-12
  Niki T Loges; Heike Olbrich; Lale Fenske; Huda Mussaffi; Judit Horvath; Manfred Fliegauf; Heiner Kuhl; Gyorgy Baktai; Erzsebet Peterffy; Rahul Chodhari; Eddie Chung; Andrew Rutman; Christopher O'Callaghan; Hannah Blau; Laszlo Tiszlavicz; Katarzyna Voelkel; Michal Witt; Ewa Zietkiewicz; Juergen Neesen; Richard Reinhardt; Hannah M Mitchison; Heymut Omran
  
• (2008). Genetic and physical interaction between the NPHP5 and NPHP6 gene products. Hum Mol Genet 17(23): 3655–3662
  Schäfer, T., Pütz, M., Lienkamp, S., Ganner, A., Bergbreiter, A., Ramachandran, H., Gieloff, V., Gerner, M., Mattonet, C., Czarnecki, P.G., Sayer, J.A., Otto, E.A., Hildebrandt, F., Kramer-Zucker, A., Walz, G.
  
• (2008). Ktu/PF13 is required for cytoplasmic pre-assembly of axonemal dyneins. Nature 456 (7222):611-6
  Omran, H., Kobayashi, D., Olbrich, H., Tsukahara, T., Loges, N.T., Hagiwara, H., Zhang, Q., Leblond, G., O’Toole, E., Hara, C., Mizuno, H., Kawano, H., Fliegauf, M., Yagi, T., Koshida, S., Miyawaki, A., Zentgraf, H.W., Seithe, H., Reinhardt, R., Watanabe, Y., Kamiya, R., Mitchell, D.R., Takeda, H.
  
• (2008). Primary ciliary dyskinesia associated with normal axoneme ultrastructure is caused by DNAH11 mutations. Hum. Mutat. 29, 289- 298
  Schwabe, G.C., Hoffmann, K., Loges, N.T., Birker, D., Rossier, C., de Santi, M.M., Olbrich, H., Fliegauf, M., Failly, M., Liebers, U., Collura, M., Gaedicke, G., Mundlos, S., Wahn, U., Blouin, J.L., Niggemann, B., Omran, H., Antonarakis, S.E., Bartoloni, L.
  
• (2008). Stromal-derived factor-1 (SDF-1) expression during early chick development. Int J Dev Biol 52, 87-92
  Rehimi, R., Khalida, N., Yusuf, F., Dai, F., Morosan-Puopolo, G., and Brand- Saberi, B.
  
• (2009). Deletions and point mutations of LRRC50 cause primary ciliary dyskinesia due to dynein arm defects. Am J Hum Genet. 85(6):883-9
  Loges NT, Olbrich H, Becker-Heck A, Häffner K, Heer A, Reinhard C, Schmidts M, Kispert A, Zariwala MA, Leigh MW, Knowles MR, Zentgraf H, Seithe H, Nürnberg G, Nürnberg P, Reinhardt R, Omran H
  
• (2009). Remodeling of aortic smooth muscle cells in the wall of the avian dorsal aorta. Dev. Dyn 236, 2578-2585
  Wiegreffe, C., Christ, B., Huang, R., Scaal, M.
  
• (2009). RORγt and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nat Immunol 10:83-91
  Sanos, S.L., Bui, V.L., Mortha, A., Oberle, K., Heners, C., Johner, C., and Diefenbach, A.
  
• (2009). Scribble participates in Hippo signaling and is required for normal zebrafish pronephros development. Proc Natl Acad Sci USA. 106 (21):8579-84
  Skouloudaki K, Puetz M, Simons M, Courbard JR, Boehlke C, Hartleben B, Engel C, Moeller MJ, Englert C, Bollig F, Schäfer T, Ramachandran H, Mlodzik M, Huber TB, Kuehn EW, Kim E, Kramer-Zucker A, Walz G
  
• (2009). Testis cord differentiation after the sex determination stage is independent of Sox9 but fail in the combined absence of Sox9 and Sox8. Dev Biol 327(2):301-12
  Barrionuevo F, Georg I, Scherthan H, Lécureuil C, Guillou F, Wegner M and Scherer G
  
• (2009). The biology of cytotoxic cell granule exocytosis pathway: granzymes have evolved to induce cell death and inflammation. Microbes Infect. 11(4):452-9
  Pardo J1, Aguilo JI, Anel A, Martin P, Joeckel L, Borner C, Wallich R, Müllbacher A, Froelich CJ, Simon MM
  
• (2009). The PGD2 pathway, independently of FGF9, amplifies SOX9 activity in Sertoli cells during male sexual differentiation. Development 135, 1813-1821
  Moniot B, Declosmenil F, Barrionuevo F, Scherer G, Aritake K, Malki Safia, Marzi L, Cohen-Solal A, Georg I, Klattig J, Englert C, Kim Y, Capel B, Eguchi N, Urade Y, Boizet-Bonhoure B, Poulat F
  
• (2009). The planar cell polarity (PCP) protein Diversin translocates to the nucleus to interact with the transcription factor AF9. Biochem Biophys Res Commun. 387(1):212-7
  Haribaskar R, Putz M, Schupp B, Skouloudaki K, Bietenbeck A, Walz G, Schäfer T
  
• (2009): Modeling system states in livercells: survival, apoptosis and their modifications in response to viral infection. BMC Syst Biol 3, 97
  Philippi N, Walter D, Schlatter R, Ferreira K, Ederer M, Sawodny O, Timmer J, Borner C, Dandekar T
  
• Immunofluorescence staining of ciliated respiratory epithelial cells. (2009) Methods Cell Biol 91:123-33
  Omran H, Loges NT
  
• (2010) DeltaA/DeltaD regulate multiple and temporally distinct phases of notch signalling during dopaminergic neurogenesis in zebrafish. J Neurosci. 30(49):16621-35
  Mahler, J., Filippi, A., Driever, W.
  
• (2010) Expression of the paralogous tyrosine hydroxylase encoding genes th1 and th2 reveals the full complement of dopaminergic and noradrenergic neurons in zebrafish larval and juvenile brain. J Comp Neurol. 518(4):423-38
  Filippi, A., Mahler, J., Schweitzer, J., Driever, W.
  
• (2010). A novel role of CXCR4 and SDF-1 during migration of cloacal muscle precursors. Dev Dyn. 239(6):1622-31
  Rehimi R, Khalida N, Yusuf F, Morosan-Puopolo G, Brand-Saberi B
  
• (2010). CCDC39 is required for assembly of inner dynein arms and the dynein regulatory complex and for normal ciliary motility in humans and dogs. Nat Genet. 43(1):72-8
  Merveille AC, Davis EE, Becker-Heck A, Legendre M, Amirav I, Bataille G, Belmont J, Beydon N, Billen F, Clément A, Clercx C, Coste A, Crosbie R, de Blic J, Deleuze S, Duquesnoy P, Escalier D, Escudier E, Fliegauf M, Horvath J, Hill K, Jorissen M, Just J, Kispert A, Lathrop M, Loges NT, Marthin JK, Momozawa Y, Montantin G, Nielsen KG, Olbrich H, Papon JF, Rayet I, Roger G, Schmidts M, Tenreiro H, Towbin JA, Zelenika D, Zentgraf H, Georges M, Lequarré AS, Katsanis N, Omran H, Amselem S
  
• (2010). Control of Dpp morphogen signalling by a secreted feedback regulator. Nat Cell Biol. 12(6):611-7
  Vuilleumier R, Springhorn A, Patterson L, Koidl S, Hammerschmidt M, Affolter M, Pyrowolakis G
  
• (2010). Dicer is required for Sertoli cell function and survival. Int J Dev Biol, 54(5), 867
  Kim GJ, Georg I, Scherthan H, Merkenschlager M, Guillou F, Scherer G & Barrionuevo F
  
• (2010). Expression and Regulation of AMNTXR1 in the Chick Embryo, Dev Dyn. 239(2):680-7
  Herrmann D, Ferrer-Vaquer A, Lahsnig C, Firnberg N, Leibgrandt A, Neubüser A
  
• (2010). Integration of human model neurons (NT2) into embryonic chick nervous system. Dev. Dyn. 239, 496-504
  Podrygajlo, G., Wiegreffe, C., Scaal, M., and Bicker, G.
  
• (2010). Molecular cloning of chicken Cecr2 and its expression during chicken embryo development. Int J Dev Biol. 54(5):925-9
  Chen J, Morosan-Puopolo G, Dai F, Wang J, Brand-Saberi B
  
• (2010). Mutations of the SRY-Responsive Enhancer of SOX9 Are Uncommon in XY Gonadal Dysgenesis. Sex Dev 4:321-325
  Georg I, Bagheri-Fam S, Knower KC, Wieacker P, Scherer G, Harley VR
  
• (2010). Non-caspase proteases: triggers or amplifiers of apoptosis? Cell. Mol. Life Sci. 67(10):1607–18
  Schrader K, Huai J, Jöckel L, Oberle C, Borner C
  
• (2010). PRKCSH/80K-H, the protein mutated in polycystic liver disease, protects polycystin-2/TRPP2 against HERP-mediated degradation. Hum Mol Genet. 19(1):16-24
  Gao H, Wang Y, Wegierski T, Skouloudaki K, Putz M, Fu X, Engel C, Boehlke C, Peng H, Kuehn EW, Kim E, Kramer-Zucker A, Walz G
  
• (2010). Regulated expression of nuclear receptor RORgt confers distinct funktional fates to NK cell receptor-expressing RORgt+ innate lymphocytes. Immunity, 33:736-751
  Vonarbourg C, Mortha A, Bui VL, Hernandez PP, Kiss EA, Hoyler T, Flach M, Bengsch B, Thimme R, Hölscher C, Hönig M, Pannicke U, Schwarz K, Ware CF, Finke D, Diefenbach A
  
• (2010). Regulation of Tbx22 during facial and palatal development, Dev Dyn. 239(11):2860-74
  Fuchs A, Inthal A, Herrmann D, Cheng S, Nakatomi M, Peters H, Neubüser A
  
• (2010). Role of caspases and non-caspase proteases in cell death. F1000 Biol Rep. 2, 48
  Huai J, Jöckel L, Schrader K, Borner C
  (See online at https://doi.org/10.3410/B2-48)
• (2010). The retinitis pigmentosa GTPase regulator interacting protein 1 (RPGRIP1) links RPGR to the nephronophthisis protein network. Kidney Int. 77(10):891-6
  Gerner M, Haribaskar R, Pütz M, Czerwitzki J, Walz G, Schäfer T
  
• (2011). Comprehensive catecholaminergic projectome analysis reveals single-neuron integration of zebrafish ascending and descending dopaminergic sytems. Nat Commun, 2:171
  Tay, T.L., Ronneberger, O., Ryu, S., Nitschke, R., Driever, W.
  
• (2011). Control of epithelial cell function by interleukin-22-producing RORγt+ innate lymphoid cells. Immunology 132(4):453-65
  Sanos SL, Vonarbourg C, Mortha A, Diefenbach A
  
• (2011). Diversification and molecular evolution of ATOH8, a gene encoding a bHLH transcription factor. PLoS One. 6(8):e23005
  Chen J, Dai F, Balakrishnan-Renuka A, Leese F, Schempp W, Schaller F, Hoffmann MM, Morosan-Puopolo G, Yusuf F, Bisschoff IJ, Chankiewitz V, Xue J, Chen J, Ying K, Brand-Saberi B
  
• (2011). Ephrin/ephrin receptor expression during early stages of mouse inner ear development. Dev Dyn. 240(6):1578-85
  Saeger BM, Suhm M, Neubüser A
  
• (2011). Mouse granzyme K has proinflammatory potential. Cell Death and Differentiation 18(7):1112–9
  Joeckel LT, Wallich R, Martin P, Sanchez-Martinez D, Weber FC, Martin SF, Borner C, Pardo J, Froelich C, Simon MM
  
• (2011). Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 334(6062):1561-5
  Kiss EA, Vonarbourg C, Kopfmann S, Hobeika E, Finke D, Esser C, Diefenbach A
  
• (2011). Natural killer cell receptor-expressing innate lymphocytes: more than just NK cells. Cell Mol Life Sci. 68(21):3541-55
  Mortha A, Diefenbach A
  
• (2011). The coiled-coil domain containing protein CCDC40 is essential for motile cilia function and left-right axis formation. Nat Genet. 43(1):79-84
  Becker-Heck A, Zohn IE, Okabe N, Pollock A, Lenhart KB, Sullivan-Brown J, McSheene J, Loges NT, Olbrich H, Haeffner K, Fliegauf M, Horvath J, Reinhardt R, Nielsen KG, Marthin JK, Baktai G, Anderson KV, Geisler R, Niswander L, Omran H, Burdine RD
  
• (2011): Tumor necrosis factor sensitizes primary murine hepatocytes to FasCD95-induced apoptosis in a Bim- and Bid-dependent manner. Hepatology 53 (1), 282-292
  Schmich K, Schlatter R, Corazza N, Sa Ferreira K, Ederer M, Brunner T, Borner C, Merfort I
  
• (2012) Low perforin expression of early differentiated HCV-specific CD8+ T cells limits their hepatotoxic potential. J Hepatol. 57(1), 9-16
  Jo J, Bengsch B, Seigel B, Rau SJ, Schmidt J, Bisse E, Aichele P, Aichele U, Joeckel L, Royer C, Ferreira KS, Borner C, Baumert TF, Blum HE, Lohmann V, Fischer R, Thimme R
  (See online at https://doi.org/10.1016/j.jhep.2012.02.030)
• (2012). Caspase-3 feeds back on caspase-8, Bid and XIAP in type I Fas signaling in primary mouse hepatocytes. Apoptosis, 17(5), 503-515
  Ferreira K, Kreutz C, Macnelly S, Neubert K, Haber A, Bogyo M, Timmer J, Borner C
  (See online at https://doi.org/10.1007/s10495-011-0691-0)
• (2012). CCDC103 mutations cause primary ciliary dyskinesia by disrupting assembly of ciliary dynein arms. Nat Genet. 44(6):714-9
  Panizzi JR, Becker-Heck A, Castleman VH, Al-Mutairi DA, Liu Y, Loges NT, Pathak N, Austin-Tse C, Sheridan E, Schmidts M, Olbrich H, Werner C, Häffner K, Hellman N, Chodhari R, Gupta A, Kramer-Zucker A, Olale F, Burdine RD, Schier AF, O'Callaghan C, Chung EM, Reinhardt R, Mitchison HM, King SM, Omran H, Drummond IA
  (See online at https://doi.org/10.1038/ng.2277)
• (2012). Fluorescence-Activated Cell Sorting (FACS) of Fluorescently Tagged Cells from Zebrafish Larvae for RNA Isolation. Cold Spring Harb Protoc. 2012 Aug 1;2012(8)
  Manoli M. and Driever W.
  (See online at https://doi.org/10.1101/pdb.prot069633)
• (2012). Interleukin-1R signaling is essential for induction of proapoptotic CD8 T cells, viral clearance, and pathology during lymphocytic choriomeningitis virus infection in mice. J. Virol. 86(16):8713–9
  Joeckel LT, Wallich R, Metkar SS, Froelich CJ, Simon MM, Borner C
  (See online at https://doi.org/10.1128/JVI.00682-12)
• (2012). Mutations in axonemal dynein assembly factor DNAAF3 cause primary ciliary dyskinesia. Nat Genet. 44(4):381-9
  Mitchison HM, Schmidts M, Loges NT, Freshour J, Dritsoula A, Hirst RA, O'Callaghan C, Blau H, Al Dabbagh M, Olbrich H, Beales PL, Yagi T, Mussaffi H, Chung EM, Omran H, Mitchell DR
  (See online at https://doi.org/10.1038/ng.1106)
• (2012). Recessive HYDIN mutations cause primary ciliary dyskinesia without randomization of left-right body asymmetry. Am J Hum Genet. 91(4):672-84
  Olbrich H, Schmidts M, Werner C, Onoufriadis A, Loges NT, Raidt J, Banki NF, Shoemark A, Burgoyne T, Al Turki S, Hurles ME; UK10K Consortium, Köhler G, Schroeder J, Nürnberg G, Nürnberg P, Chung EM, Reinhardt R, Marthin JK, Nielsen KG, Mitchison HM, Omran H
  (See online at https://doi.org/10.1016/j.ajhg.2013.06.009)
• (2012). Role of the Aryl Hydrocarbon Receptor in Controlling Maintenance and Functional Programs of RORγt(+) Innate Lymphoid Cells and Intraepithelial Lymphocytes. Front Immunol. 31;3:124
  Kiss EA, Diefenbach A
  (See online at https://doi.org/10.3389/fimmu.2012.00124)
• (2012). Shroom3 is required downstream of FGF signalling to mediate proneuromast assembly in zebrafish. Development. 139(24); 4571-81
  Ernst S, Liu K, Agarwala S, Moratscheck N, Avici ME, Nogare DD, Chitnis AB, Ronneberger O and Lecaudey V
  (See online at https://doi.org/10.1242/dev.083253)
• (2012). Sox9 and Sox8 are required for basal lamina integrity of testis cords and for suppression of FOXL2 during embryonic testis development in mice. Biol Reprod. 87(4):99
  Georg I, Barrionuevo F, Wiech T, Scherer G
  (See online at https://doi.org/10.1095/biolreprod.112.101907)
• (2012). Temperature- and Touch-Sensitive Neurons Couple CNG and TRPV Channel Activities to Control Heat Avoidance in Caenorhabditis elegans. PLoS One. 2012; 7(3): e32360
  Liu S., Schulze E., Baumeister R.
  (See online at https://doi.org/10.1371/journal.pone.0032360)
• (2012). The Transcription Factor GATA-3 Controls Cell Fate and Maintenance of Type 2 Innate Lymphoid Cells. Immunity 37:634-648
  Hoyler T, Klose CS, Souabni A, Turqueti-neves A, Pfeifer D, Rawlins EL, Voehringer D, Busslinger M, Diefenbach A
  (See online at https://doi.org/10.1016/j.immuni.2012.06.020)
• (2012). Thymosin β4 induces folding of the developing optic tectum in the chicken (Gallus domesticus). J Comp Neurol. 520(8):1650-62
  Wirsching HG, Kretz O, Morosan-Puopolo G, Chernogorova P, Theiss C, Brand-Saberi B
  (See online at https://doi.org/10.1002/cne.23004)
• (2012). Transcriptional control of innate lymphocyte fate decisions. Curr Opin Immunol. 24(3):290-6
  Klose CS, Hoyler T, Kiss EA, Tanriver Y, Diefenbach A
  (See online at https://doi.org/10.1016/j.coi.2012.04.004)
• (2012). Transcriptional interpretation of the EGF receptor signaling gradient. Proc Natl Acad Sci USA. 109(5):1572-7
  Fuchs A, Cheung LC, Charbonnier E1, Shvartsman SY, Pyrowolakis G
  (See online at https://doi.org/10.1073/pnas.1115190109)
• (2012). YAP1 recruits c-Abl to protect angiomotin-like 1 from Nedd4-mediated degradation. PloS one. 7(4):e35735
  Skouloudaki, K., Walz, G.
  (See online at https://doi.org/10.1371/journal.pone.0035735)
• Genetic Disorders of Mucociliary Clearance Consortium. (2012). Mutations of DNAH11 in patients with primary ciliary dyskinesia with normal ciliary ultrastructure. Thorax. 67(5):433-41
  Knowles MR, Leigh MW, Carson JL, Davis SD, Dell SD, Ferkol TW, Olivier KN, Sagel SD, Rosenfeld M, Burns KA, Minnix SL, Armstrong MC, Lori A, Hazucha MJ, Loges NT, Olbrich H, Becker-Heck A, Schmidts M, Werner C, Omran H, Zariwala MA
  (See online at https://doi.org/10.1136/thoraxjnl-2011-200301)
• (2013). A t-bet gradient controls the fate and function of CCR6-RORγt+ innate lymphoid cells. Nature 494:261-265
  Klose CS, Kiss EA, Schwierzeck V, Ebert K, Hoyler T, D’Hargues Y, Göppert N, Croxford AL, Waisman A, Tanriver Y, Diefenbach A
  
• (2013). aPKCλ/ι and aPKCζ contribute to podocyte differentiation and glomerular maturation. J Am Soc Nephrol. 24(2):253-67
  Hartleben B, Widmeier E, Suhm M, Worthmann K, Schell C, Helmstädter M, Wiech T, Walz G, Leitges M, Schiffer M, Huber TB
  
• (2013). Drosophila ATP6Ap2/VhaPRR functions both as a novel planar cell polarity core protein and a regulator of endosomal trafficking. EMBO Journal 32(2): 245-59
  Hermle T, Guida MC, Beck S., Helmstädter S, Simons M
  (See online at https://doi.org/10.1038/emboj.2012.323)
• (2013). Fast impact of progesterone on the neuronal growth cone. Endocrinology. 154(10):16210-26221
  Olbrich L, Wessel L, Balakrishnan-Renuka A, Brand-Saberi B, Theiss C
  (See online at https://doi.org/10.1210/en.2013-1175)
• (2013). Genome-wide identification of Sox8-, and Sox9-dependent genes during early post-natal testis development in the mouse. Andrology, 1, 281-292
  Chalmel F, Lardenois, A, Georg I, Barrionuevo F, Demougin P, Jégou B, Scherer G, Primig M
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