The soil nematode Caenorhabdidis elegans is a model system used to study the genetic control of cellular development. The Hall laboratory specializes in ultrastructural studies of the C. elegans. We use serial thin sections, electron microscopy, electron tomography, FIB/SEM and immunocytochemistry as primary tools to follow the development of identified neurons, particularly their axon outgrowth and synaptic connectivity. We also conduct collaborative studies on many other tissues in the embryo, larval, dauer, adult and aging nematode, including many epithelial tissues and the germline.

We host the Center for C. elegans Anatomy, supported by the NIH Office of the Director, and train students in anatomical methods for this system. Members of the lab are authoring the website www.WormAtlas.org. It displays nematode anatomy in great detail through multiple applications including Slidable Worm, a Handbook of all cells and tissues, the WormImage catalogue, a Glossary, and selected html texts of classic papers.

In collaboration with Scott Emmons, we are studying the complete connectome of C. elegans in both sexes and in larval stages to uncover how the nematode wiring diagram develops over time. In collaboration with Maureen Barr (Rutgers) we are studying the “tubulin code” which helps to stabilize ciliary microtubules during development and maintenance of the nematode’s sense endings.

Dimitriadi M, Derdowski A, Kalloo G, Maginnis MS, O'Hern P, Bliska B, Sorkaç A, Nguyen KC, Cook SJ, Poulogiannis G, Atwood WJ, Hall DH, Hart AC (2016) Decreased function of survival motor neuron protein impairs endocytic pathways. Proc Natl Acad Sci U S A. 113(30):E4377-86.

Stavoe AK, Hill SE, Hall DH, Colón-Ramos DA (2016) KIF1A/UNC-104 TransportsATG-9 to Regulate Neurodevelopment and Autophagy at Synapses. Dev. Cell 38(2):171-85.

Grussendorf KA, Trezza CJ, Nichols AL, Meelkop E, Linton C, Giordano-Santini R,Sullivan RK, Donato A, Nolan C, Hall DH, Xue D, Neumann B, Hilliard MA (2016) The Apoptotic Engulfment Machinery Regulates Axonal Degeneration in C. elegans Neurons. Cell Rep. 14(7):1673-83.

Morsci NS, Hall DH, Driscoll M, Sheng ZH (2016) Age-Related Phasic Patterns of Mitochondrial Maintenance in Adult C. elegans Neurons. J Neurosci. 2016 Jan 27;36(4):1373-85.

Nichols AL, Meelkop E, Linton C, Giordano-Santini R, Sullivan RK, Donato A, Nolan C, Hall DH, Xue D, Neumann B, Hilliard MA (2016) The Apoptotic Engulfment Machinery Regulates Axonal Degeneration in C. elegans Neurons. Cell Rep. 2016 Feb 23;14(7):1673-83.

Wang, J, Kaletsky, R, Silva, M, Williams, A, Haas, L, Androwski, R, Landis, J, Patrick, C, Rashid, A, Santiago-Martinez, D, Gravato-Nobre, M, Hodgkin, J, Hall, DH, Murphy, C and Barr, MM (2015) Cell-Specific Transcriptional Profiling of Ciliated Sensory Neurons Reveals Regulators of Behavior and Extracellular Vesicle Biogenesis. Curr Biol. 2015 Dec 21;25(24):3232-8.

Sammut, M, Cook, SJ, Nguyen, K, Felton, T, Hall, DH, Emmons, SW, Poole, RJ and Barrios, A (2015) Glia-derived neurons are required for sex-specific learning in C. elegans. Nature 526:385-90

Maguire, JE, Silva, M, Nguyen, KC, Hellen, AD, Hall, DH and Barr, MM (2015) Myristoylated CIL-7 regulates ciliary extracellular vesicle biogenesis. Mol Biol Cell 26: 2823-32. doi: 10.1091/mbc.

Warburton-Pitt, SR, Silva, M, Nguyen, KC, Hall, DH and Barr, MM (2014) The nphp-2 and arl-13 genetic modules interact to regulate ciliogenesis and ciliary microtubule patterning in C. elegans. PLoS Genet. 10(12)e1004866.

Nguyen, PAT, Liou, W, Hall, DH and Leroux, MR (2014) Ciliopathy proteins establish a bipartite signaling compartment in a C. elegans thermosensory neuron. J. Cell Science 127:5317-30.

Wang, J, Silva M, Haas, LA, Nguyen, KCQ, Hall, DH and Barr, MM. (2014) C. elegans ciliated sensory neurons release extracellular vesicles that function in animal communication. Curr. Biol. 24: 519-25 doi: 10.1016/j.cub.2014.01.002.

Riddle MR, Weintraub A, Nguyen KC, Hall DH, Rothman JH (2013) Transdifferentiation and remodeling of postembryonic C. elegans cells by a single transcription factor. Development. 140: 4844-9.

Zhang, J, Li, X, Jevince, AR, Wang, J, Hall, DH and Ding, M (2013) Neuronal target identification requires AHA-1-mediated fine-tuning of Wnt signaling in C. elegans. PLoS Genet. 9(6):e1003618.

Liu, P, Chen, B, Altun, ZF, Gross, MJ, Shan, A, Schuman, B, Hall, DH and Wang, ZW (2013) Six innexins contribute to electrical coupling of C. elegans bodywall muscle. PLos One 8: e76877.

Jarrell, TA, Wang, Y, Bloniarz, AE, Brittin, CA, Xu, M, Thomson, JN, Albertson, DG, Hall, DH and Emmons, SW (2012) The connectome of a decision making neuronal network. Science 337: 437-444.

Topalidou, I, Keller, C, Kalebic, N, Nguyen, KC, Somhegyi, H, Politi, KA, Heppenstall, P, Hall, DH and Chalfie, M (2012) Both enzymatic and structural activities of the tubulin acetyltransferase MEC-17 are required for microtubule structure and organization in C. elegans. Current Biol. 22: 1057-65.

Toth, M, Melentijevic, I, Shah, L, Bhatia, A, Lu, K, Talwar, A, Naji, H, Ibanez-Ventoso, C, Ghose, P, Jevince, A, Xue, J, Herndon, LA, Bhanot, G, Rongo, C, Hall, DH, and Driscoll, M (2012) Neurite sprouting and synapse deterioration in the aging C. elegans nervous system. J. Neurosci. 32: 8778-90.

O’Hagan, R, Piasecki, B, Silva, M, Phirke, P, Nguyen, KCQ, Hall, DH, Swoboda, P and Barr, M (2011) The tubulin deglutamylase CCPP-1 regulates the function and stability of sensory cilia in C. elegans. Current Biol. 21: 1685-94.

Neumann, B., Nguyen, KCQ, Hall, DH, Ben-Yakar, A and Hilliard, MA (2011) Axonal regeneration proceeds through specific axonal fusion in transected C. elegans neurons. Dev. Dyn. 240: 1365-72.

Varshney, LR, Chen, BL, Paniagua, E, Hall, DH and Chklovskii, DB (2011) Structural properties of the Caenorhabditis elegans neuronal network. PLoS Comp Biol Feb 3;7(2):e1001066.

Albeg, A, Smith, C, Chatzigeorgiou, M, Feitelson, DG, Hall, DH, Schaefer, WR, Miller, DM III, and Treinin, M. (2011) C. elegans multi-dendritic sensory neurons: morphology and function. Mol. Cell. Neurosci 46:308-17.

Oren-Suissa, M, Hall, DH, Treinin, M, Shemer, G, and Podbilewicz, B (2010) The fusogen EFF-1 controls sculpting of mechanosensory dendrites. Science 328: 1285-8.

Govorunova, E, Moussaif, M, Kullyev, A, Nguyen, KCQ, McDonald, T, Hall, DH and Sze, JY (2010) A homolog of FHM2 is involved in modulation of excitatory neurotransmission by serotonin in C. elegans. PLosONE, Apr 28;5(4):e10368.

Altun, ZF, Chen, B, Thomas, JH, Wang, Z-W and Hall, DH (2009) A high-resolution map of C. elegans gap junction proteins. Dev. Dynamics 238: 1936-1950.

Wang, J, Farr, GW, Hall, DH, Furtak, K, Dreier, L and Horwich, AL (2009) An ALS-linked mutant SOD1 produces a locomotor defect associated with aggregate formation and synaptic dysfunction when expressed in neurons of Caenorhabditis elegans. PLoS Genetics Jan;5(1):e1000350.

Jauregui, AR, Nguyen, KCQ, Hall, DH and Barr, MM (2008) C. elegans nephrocystin-1 and nephrocystin-4 modulate cilia development and morphogenesis. J Cell Biol.180: 973-88.

Liu, Q, Chen, B, Hall, DH, and Wang, Z (2007) A quantum of neurotransmitter causes minis in multiple postsynaptic cells at the C. elegans neuromuscular junction. Dev. Neurobiology 67: 123-128.

Gattegno, T, Mittal, A, Valansi, AV, Nguyen, CQ, Hall, DH, Chernomordik, LV and Podbilewicz, B (2007) Genetic control of fusion pore expansion in the epidermis of C. elegans. Mol Biol of the Cell 18: 1153-1166.

Bénard, CY, Boyanov, A, Hall, DH and Hobert O. (2006) DIG-1, a novel giant protein non-autonomously mediates maintenance of nervous system architecture. Development 133: 3329-40.

Rowland, AM, Olsen, JG, Richmond, JE, Hall, DH and Bamber, BA (2006) Presynaptic terminals independently regulate synaptic clustering and autophagy of GABA_A receptors in Caenorhabditis elegans. J. Neuroscience 26: 1711-20.

Chen, B, Hall, DH and Chklovskii, DB (2006) Wiring optimization can relate neuronal structure and function. PNAS 103: 4723-4728.

Shemer, G, Suissa, M, Kolotuev, I, Nguyen, KCQ, Hall, DH, and Podbilewicz, B (2004) EFF-1 is sufficient to initiate and execute tissue-specific cell fusion in C. elegans. Current Biology 14: 1587-91.

Melendez, A, Talloczy, Z, Seaman, M, Eskelinen, E-L, Hall, DH, and Levine, B (2003) Autophagy genes are essential for dauer development and lifespan extension in C. elegans. Science 301: 1387-91.

Huang, C-C, Hall, DH, Hedgecock, EM, Kao, G, Karantza, V, Vogel, B, Hutter, H, Chisholm, AD, Yurchenco, PD, and Wadsworth, WG (2003) Laminin a subunits and their role in C. elegans development. Development 130: 3343-3358.

Starich, T, Miller, A, Nguyen, RL, Hall, DH and Shaw, JE (2003) The C. elegans innexin gene product INX-3 is localized to gap junctions and is essential for embryonic development. Dev. Biol. 256: 403-417.

Herndon, LA, Schmeissner, PJ, Dudaroneck, JM, Brown, PA, Listner, KM, Paupard, MC, Hall, DH, and Driscoll, M (2002) Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 419: 788-794.

Aurelio, O, Hall, DH, and Hobert, O (2002) Immunoglobulin-domain proteins required for maintenance of ventral nerve cord organization. Science 295: 686-690.

Rolls, MM, Hall, DH, Victor, M, Stelzer, EHK, and Rappaport, TA (2002) Targeting of rough endoplasmic reticulum membrane proteins and ribosomes in invertebrate neurons. Mol. Biol. of the Cell 13: 1778-1791.

Nass, R, Hall, DH, Miller, DM and Blakeley, RD (2002) Neurotoxin-induced degeneration of dopamine neurons in C. elegans. PNAS 99: 3264-3269.

Barr, MM, DeModena, J, Braun, D, Nguyen, CQ, Hall, DH, and Sternberg, PW (2001) The Caenorhabditis elegans autosomal dominant polycystic kidney disease homologs lov-1 and pkd-2 act in the same pathway. Current Biology 11:1341-46

Koeppen, M, Simske, J, Sims, P, Firestein, BL, Hall, DH, Radice, A, Rongo, C and Hardin, J (2001) Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia. Nature Cell Biology 3: 983-991.

Licktieg, KM, Duerr, J, Frisby, D, Hall, DH, Rand, J and Miller, DM (2001) Regulation of neurotransmitter vesicles by the homeodomain protein UNC-4 and the co-repressor protein UNC-37/Groucho in Caenorhabditis elegans cholinergic motor neurons. J. Neuroscience 21: 2001-2014.

Yu, RYL, Nguyen, CQ, Hall, DH and Chow, KL (2000) Expression of the ram-5 gene in the structural cell is required for sensory ray morphogenesis in the C. elegans male tail. EMBO J. 19:3542-3555.

Cassata, G, Kagoshima, H, Andachi, Y, Kohara, Y, Durrenburger, MB, Hall, DH and Burglin, TR. (2000) The Lim homeobox gene ceh-14 confers thermosensory function to the AFD neurons in Caenorhabditis elegans. Neuron 25:587-597.

Nguyen, KCQ, Hall, DH, Yang, Y, and Fitch, DHA (1999) Morphogenesis of the C. elegans male tail tip. Dev. Biol. 207:86-106.

Goodman, MB, Hall, DH, Avery, L and Lockery, SR (1998) Intrinsic electrical properties of C. elegans neurons revealed by whole-cell patch-clamp recordings. Neuron 20:763-772.

Hall, DH, Gu, G, Garcia-Anoveros, J, Gong, L, Driscoll, M and Chalfie, M (1997) Neuropathology of degenerative cell death in C. elegans. J. Neurosci. 17:1033-45.

Mitani, S, Du, H, Hall, DH, Driscoll, M and Chalfie, M (1993) Combinatorial control of touch neuron receptor expression in Caenorhabditis elegans. Development 119:773-783.

Hall, DH and Hedgecock, EM (1991) Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans. Cell 65:837-847.

Hall, DH and Russell, RL (1991) The posterior nervous system of the nematode Caenorhabditis elegans: Serial reconstruction of identified neurons and complete pattern of synaptic interactions. J. Neurosci. 11:1-22.

Hedgecock, EM, Culotti, JG and Hall, DH (1990) The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 4:61-85.

Hedgecock, EM, Culotti, JG, Hall, DH and Stern, BG (1987) Genetics of cell and axon migrations in Caenorhabditis elegans. Development 100: 365-382.

Hall, DH, Gilat, E and Bennett, MVL. (1985) Ultrastructure of the rectifying synapses between the giant fibers and the pectoral fin adductor motoneurons in the hatchetfish. J. Neurocytol. 14:825-834.

Hall, DH, Spray, DC and Bennett, MVL (1983) Gap junctions and septate-like junctions in Navanax neurons. J. Neurocytology 12:831-846.

Textbook:

Hall, DH and Altun, Z (2008) C. elegans Atlas. Cold Spring Harbor Laboratory Press, 340 pp.

Published Reviews:

Hall DH (2016) Gap junctions in C. elegans: Their roles in behavior and development. Dev Neurobiol. Jun 13. doi:10.1002/dneu.22408.

Hall, DH and Rice WJ (2015) Electron tomography methods for C. elegans. (invited review). Methods Mol. Biol. 1327:141-58

Hall, DH, Hartwieg, E and Nguyen, KCQ (2012) Modern electron microscopy methods for C. elegans. In Methods in Cell Biology (Eds) Joel Rothman and Andrew Singson. Academic Press, New York, 107:93-149.

Hall, DH and Treinin, M (2011) Form and function of sensory arbors. Trends Neurosci 9:443-51

Altun, Z, Lints, R. and Hall, DH (2006) Nematode neurons. Anatomy and anatomical methods in Caenorhabditis elegans. Int. Rev. Neurobiol. 69: 1-35.