The LIM Homeobox Gene ceh-14 Confers Thermosensory Function to the AFD Neurons in Caenorhabditis elegans

In Caenorhabditis elegans three pairs of neurons, AFD, AIY, and AIZ, play a key role in thermosensation. The LIM homeobox gene ceh-14 is expressed in the AFD thermosensory neurons. ceh-14 mutant animals display athermotactic behaviors, although the neurons are still present and differentiated. Two other LIM homeobox genes, ttx-3 and lin-11, function in the two interneurons AIY and AIZ, respectively. Thus, the three key thermosensory neurons are specified by three different LIM homeobox genes. ceh-14 ttx-3 lin-11 triple mutant animals have a basic cryophilic thermotaxis behavior indicative of a second thermotaxis pathway. Misexpression of ceh-14 in chemosensory neurons can restore thermotactic behavior without impairing the chemosensory function. Thus, ceh-14 confers thermosensory function to neurons.

[1]  J. N. Thomson,et al.  Mutant sensory cilia in the nematode Caenorhabditis elegans. , 1986, Developmental biology.

[2]  G. Ruvkun,et al.  Regulation of Interneuron Function in the C. elegans Thermoregulatory Pathway by the ttx-3 LIM Homeobox Gene , 1997, Neuron.

[3]  S. Brenner,et al.  The structure of the nervous system of the nematode Caenorhabditis elegans. , 1986, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[4]  M. Rosenfeld,et al.  A family of LIM domain-associated cofactors confer transcriptional synergism between LIM and Otx homeodomain proteins. , 1997, Genes & development.

[5]  Cori Bargmann,et al.  OSM-9, A Novel Protein with Structural Similarity to Channels, Is Required for Olfaction, Mechanosensation, and Olfactory Adaptation inCaenorhabditis elegans , 1997, The Journal of Neuroscience.

[6]  A. Coulson,et al.  Caenorhabditis elegans has scores of homoeobox-containing genes , 1989, Nature.

[7]  S. Pfaff,et al.  LIM Homeodomain Factors Lhx3 and Lhx4 Assign Subtype Identities for Motor Neurons , 1998, Cell.

[8]  J. Eisen,et al.  Motoneuron fate specification revealed by patterned LIM homeobox gene expression in embryonic zebrafish. , 1995, Development.

[9]  G. Ruvkun,et al.  Control of Neural Development and Function in a Thermoregulatory Network by the Lim Homeobox Gene Lin-11 , 2022 .

[10]  J. J. Breen,et al.  LIM domains: multiple roles as adapters and functional modifiers in protein interactions. , 1998, Trends in genetics : TIG.

[11]  J. J. Breen,et al.  Interactions of the LIM-domain-binding factor Ldbl with LIM homeodomain proteins , 1996, Nature.

[12]  John B. Thomas,et al.  The Drosophila islet Gene Governs Axon Pathfinding and Neurotransmitter Identity , 1997, Neuron.

[13]  G. Warren,et al.  A monoclonal antibody against a 135‐K Golgi membrane protein. , 1982, The EMBO journal.

[14]  M. Chalfie,et al.  The mec-3 gene of Caenorhabditis elegans requires its own product for maintained expression and is expressed in three neuronal cell types. , 1989, Genes & development.

[15]  D. Julius,et al.  The capsaicin receptor: a heat-activated ion channel in the pain pathway , 1997, Nature.

[16]  Cornelia I Bargmann,et al.  Reprogramming Chemotaxis Responses: Sensory Neurons Define Olfactory Preferences in C. elegans , 1997, Cell.

[17]  L. Jurata,et al.  Nuclear LIM interactor, a rhombotin and LIM homeodomain interacting protein, is expressed early in neuronal development. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[18]  R. Toyama,et al.  LIM domain proteins. , 1995, Comptes rendus de l'Academie des sciences. Serie III, Sciences de la vie.

[19]  I. Mori,et al.  Neural regulation of thermotaxis in Caenorhabditis elegans , 1995, Nature.

[20]  R. L. Russell,et al.  Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Andrew Smith Genome sequence of the nematode C-elegans: A platform for investigating biology , 1998 .

[22]  G. Niklaus,et al.  Rapid expression screening of Caenorhabditis elegans homeobox open reading frames using a two-step polymerase chain reaction promoter-gfp reporter construction technique. , 1998, Gene.

[23]  Andrew Tomlinson,et al.  A LIM-homeodomain combinatorial code for motor-neuron pathway selection , 1999, Nature.

[24]  P. O’Farrell,et al.  A universal target sequence is bound in vitro by diverse homeodomains , 1993, Mechanisms of Development.

[25]  Gary Ruvkun,et al.  The unc-86 gene product couples cell lineage and cell identity in C. elegans , 1990, Cell.

[26]  A. Varela-Echavarría,et al.  Differential Expression of LIM Homeobox Genes among Motor Neuron Subpopulations in the Developing Chick Brain Stem , 1996, Molecular and Cellular Neuroscience.

[27]  L. Avery,et al.  Guanylyl cyclase expression in specific sensory neurons: a new family of chemosensory receptors. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[28]  R. Plasterk,et al.  Target-selected gene inactivation in Caenorhabditis elegans by using a frozen transposon insertion mutant bank. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Ikue Mori,et al.  Mutations in a Cyclic Nucleotide–Gated Channel Lead to Abnormal Thermosensation and Chemosensation in C. elegans , 1996, Neuron.

[30]  Cori Bargmann,et al.  odr-10 Encodes a Seven Transmembrane Domain Olfactory Receptor Required for Responses to the Odorant Diacetyl , 1996, Cell.

[31]  T. Jessell,et al.  Requirement for LIM Homeobox Gene Isl1 in Motor Neuron Generation Reveals a Motor Neuron– Dependent Step in Interneuron Differentiation , 1996, Cell.

[32]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[33]  V. Ambros,et al.  Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. , 1991, The EMBO journal.

[34]  Steven N. Hird,et al.  Targeted mutations in the Caenorhabditis elegans POU homeo box gene ceh-18 cause defects in oocyte cell cycle arrest, gonad migration, and epidermal differentiation. , 1994, Genes & development.

[35]  M. Chalfie,et al.  mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans , 1988, Cell.

[36]  J. Thomas,et al.  Control of neuronal pathway selection by the Drosophila LIM homeodomain gene apterous. , 1995, Development.

[37]  P. Sternberg,et al.  Analysis of dominant-negative mutations of the Caenorhabditis elegans let-60 ras gene. , 1991, Genes & development.

[38]  D. Julius,et al.  A capsaicin-receptor homologue with a high threshold for noxious heat , 1999, Nature.

[39]  F. Ashton,et al.  Chemo- and thermosensory neurons: structure and function in animal parasitic nematodes. , 1999, Veterinary parasitology.

[40]  Cori Bargmann,et al.  Alternative olfactory neuron fates are specified by the LIM homeobox gene lim-4. , 1999, Genes & development.

[41]  Cori Bargmann,et al.  A Putative Cyclic Nucleotide–Gated Channel Is Required for Sensory Development and Function in C. elegans , 1996, Neuron.

[42]  Cori Bargmann,et al.  A cyclic nucleotide-gated channel inhibits sensory axon outgrowth in larval and adult Caenorhabditis elegans: a distinct pathway for maintenance of sensory axon structure. , 1998, Development.

[43]  Cori Bargmann,et al.  Odorant-selective genes and neurons mediate olfaction in C. elegans , 1993, Cell.

[44]  T. Jessell,et al.  Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes , 1994, Cell.