Behavioral decay in aging male C. elegans correlates with increased cell excitability

Neurobiology of Aging

Volumn 33, Issue 7, 2012, Pages 1483.e5-1483.e23

  Guo, Xiaoyan ^a   Navetta, Andrew ^a   Gualberto, Daisy G ^a   García, L Rene ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Acetylcholine receptors; Aging; Caloric deprivation; Mating behavior

Indexed keywords

CALCIUM ION; CHOLINERGIC RECEPTOR; POTASSIUM CHANNEL HERG;

ADULTHOOD; AGING; ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; CELL EXCITABILITY; CELL FUNCTION; CONTROLLED STUDY; DETERIORATION; DIET; GENE EXPRESSION; IMAGING; MALE; MATING; MUSCLE CELL; MUSCLE DISEASE; MUSCLE EXCITATION; NERVE CELL STIMULATION; NONHUMAN; PHARMACOLOGICAL PROCEDURES; PRIORITY JOURNAL; PROTEIN FUNCTION; SPERM;

EID: 84861194399     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2011.12.016     Document Type: Article

References (66)

1. Augustin H., Partridge L. Invertebrate models of age-related muscle degeneration. Biochim. Biophys. Acta 2009, 1790:1084-1094.
2. Barr M.M., Garcia L.R. Male Mating Behavior 2006, WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook. 1.7.1. http://www.wormbook.org.
3. Barr M.M., Sternberg P.W. A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans. Nature 1999, 401:386-389.
4. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
5. Chase D.L., Pepper J.S., Koelle M.R. Mechanism of extrasynaptic dopamine signaling in Caenorhabditis elegans. Nat. Neurosci 2004, 7:1096-1103.
6. De Luca A., Mambrini M., Conte Camerino D. Changes in membrane ionic conductances and excitability characteristics of rat skeletal muscle during aging. Pflugers Arch 1990, 415:642-644.
7. Edwards S.L., Charlie N.K., Milfort M.C., Brown B.S., Gravlin C.N., Knecht J.E., Miller K.G. A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans. PLoS Biol 2008, 6:e198.
8. Ernest M.J. Regulation of tyrosine aminotransferase messenger ribonucleic acid in rat liver. Effect of cycloheximide on messenger ribonucleic acid turnover. Biochemistry 1982, 21:6761-6767.
9. Forster M.J., Dubey A., Dawson K.M., Stutts W.A., Lal H., Sohal R.S. Age-related losses of cognitive function and motor skills in mice are associated with oxidative protein damage in the brain. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:4765-4769.
10. Frolkis V.V., Stupina A.S., Martinenko O.A., Tòth S., Timchenko A.I. Aging of neurons in the mollusc Lymnaea stagnalis. Structure, function and sensitivity to transmitters. Mech. Ageing Dev 1984, 25:91-102.
11. Garcia L.R., Mehta P., Sternberg P.W. Regulation of distinct muscle behaviors controls the C. elegans male's copulatory spicules during mating. Cell 2001, 107:777-788.
12. Garcia L.R., Sternberg P.W. Caenorhabditis elegans UNC-103 ERG-like potassium channel regulates contractile behaviors of sex muscles in males before and during mating. J. Neurosci 2003, 23:2696-2705.
13. Gems D., Riddle D.L. Genetic, behavioral and environmental determinants of male longevity in Caenorhabditis elegans. Genetics 2000, 154:1597-1610.
14. Glenn C.F., Chow D.K., David L., Cooke C.A., Gami M.S., Iser W.B., Hanselman K.B., Goldberg I.G., Wolkow C.A. Behavioral deficits during early stages of aging in Caenorhabditis elegans result from locomotory deficits possibly linked to muscle frailty. J. Gerontol. A Biol. Sci. Med. Sci 2004, 59:1251-1260.
15. Goldstein P. The synaptonemal complexes of Caenorhabditis elegans: pachytene karyotype analysis of hermaphrodites from the recessive him-5 and him-7 mutants. J. Cell Sci 1986, 82:119-127.
16. Granato M., Schnabel H., Schnabel R. pha-1, a selectable marker for gene transfer in C. elegans. Nucleic Acids Res 1994, 22:1762-1763.
17. Greer E.L., Brunet A. Different dietary restriction regimens extend lifespan by both independent and overlapping genetic pathways in C. elegans. Aging Cell 2009, 8:113-127.
18. Gruninger T.R., Gualberto D.G., Garcia L.R. Sensory perception of food and insulin-like signals influence seizure susceptibility. PLoS Genet 2008, 4:e1000117.
19. Gruninger T.R., Gualberto D.G., LeBoeuf B., Garcia L.R. Integration of male mating and feeding behaviors in Caenorhabditis elegans. J. Neurosci 2006, 26:169-179.
20. Guarente L., Kenyon C. Genetic pathways that regulate ageing in model organisms. Nature 2000, 408:255-262.
21. Hagiwara S., Byerly L. Membrane biophysics of calcium currents. Fed. Proc 1981, 40:2220-2225.
22. Hansen M., Chandra A., Mitic L.L., Onken B., Driscoll M., Kenyon C. A role for autophagy in the extension of lifespan by dietary restriction in C. elegans. PLoS Genet 2008, 4:e24.
23. Herndon L.A., Schmeissner P.J., Dudaronek J.M., Brown P.A., Listner K.M., Sakano Y., Paupard M.C., Hall D.H., Driscoll M. Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 2002, 419:808-814.
24. Hill K.L., L'Hernault S.W. Analyses of reproductive interactions that occur after heterospecific matings within the genus Caenorhabditis. Dev. Biol 2001, 232:105-114.
25. Hodgkin J., Horvitz H.R., Brenner S. Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics 1979, 91:67-94.
26. Hosono R., Nishimoto S., Kuno S. Alterations of life span in the nematode Caenorhabditis elegans under monoxenic culture conditions. Exp. Gerontol 1989, 24:251-264.
27. Houthoofd K., Gems D., Johnson T.E., Vanfleteren J.R. Dietary restriction in the nematode Caenorhabditis elegans. Interdiscip. Top. Gerontol 2007, 35:98-114.
28. Houthoofd K., Vanfleteren J.R. The longevity effect of dietary restriction in Caenorhabditis elegans. Exp. Gerontol 2006, 41:1026-1031.
29. Hsu A.L., Feng Z., Hsieh M.Y., Xu X.Z. Identification by machine vision of the rate of motor activity decline as a lifespan predictor in C. elegans. Neurobiol. Aging 2009, 30:1498-1503.
30. Huang C., Xiong C., Kornfeld K. Measurements of age-related changes of physiological processes that predict lifespan of Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:8084-8089.
31. Iwasa H., Yu S., Xue J., Driscoll M. Novel EGF pathway regulators modulate C. elegans healthspan and lifespan via EGF receptor, PLC-gamma, and IP3R activation. Aging Cell 2010, 9:490-505.
32. Kaeberlein T.L., Smith E.D., Tsuchiya M., Welton K.L., Thomas J.H., Fields S., Kennedy B.K., Kaeberlein M. Lifespan extension in Caenorhabditis elegans by complete removal of food. Aging Cell 2006, 5:487-494.
33. Karakelides H., Nair K.S. Sarcopenia of aging and its metabolic impact. Curr. Top. Dev. Biol 2005, 68:123-148.
34. Kenyon C. The plasticity of aging: insights from long-lived mutants. Cell 2005, 120:449-460.
35. Kenyon C., Chang J., Gensch E., Rudner A., Tabtiang R. A C. elegans mutant that lives twice as long as wild type. Nature 1993, 366:461-464.
36. Klass M.R. Aging in the nematode Caenorhabditis elegans: major biological and environmental factors influencing life span. Mech. Ageing Dev 1977, 6:413-429.
37. Koo P.K., Bian X., Sherlekar A.L., Bunkers M.R., Lints R. The robustness of Caenorhabditis elegans male mating behavior depends on the distributed properties of ray sensory neurons and their output through core and male-specific targets. J. Neurosci 2011, 31:7497-7510.
38. LeBoeuf B., Gruninger T.R., Garcia L.R. Food deprivation attenuates seizures through CaMKII and EAG K+ channels. PLoS Genet 2007, 3:1622-1632.
39. LeBoeuf B., Guo X., García L.R. The effects of transient starvation persist through direct interactions between CaMKII and ether-a-go-go K+ channels in C. elegans males. Neuroscience 2011, 175:1-17.
40. Lewis J.A., Wu C.H., Berg H., Levine J.H. The genetics of levamisole resistance in the nematode Caenorhabditis elegans. Genetics 1980, 95:905-928.
41. Liu K.S., Sternberg P.W. Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron 1995, 14:79-89.
42. Liu Y., Lebeouf B., Guo X., Correa P.A., Gualberto D.G., Lints R., Garcia L.R. A cholinergic-regulated circuit coordinates the maintenance and bi-stable states of a sensory-motor behavior during Caenorhabditis elegans male copulation. PLoS Genet 2011, 7:e1001326.
43. Liu Y., LeBoeuf B., Garcia L.R. G alpha(q)-coupled muscarinic acetylcholine receptors enhance nicotinic acetylcholine receptor signaling in Caenorhabditis elegans mating behavior. J. Neurosci 2007, 27:1411-1421.
44. Loer C.M., Kenyon C.J. Serotonin-deficient mutants and male mating behavior in the nematode Caenorhabditis elegans. J. Neurosci 1993, 13:5407-5417.
45. Lopes G.S., Smaili S.S., Neto A.C., Vladimirova I., Jurkiewicz A., Jurkiewicz N.H. Aging-induced decrease of cholinergic response and calcium sensitivity on rat jejunum contractions. J. Gerontol. A Biol. Sci. Med. Sci 2007, 62:264-270.
46. Maryon E.B., Saari B., Anderson P. Muscle-specific functions of ryanodine receptor channels in Caenorhabditis elegans. J. Cell Sci 1998, 111:2885-2895.
47. Masoro E.J. Overview of caloric restriction and ageing. Mech. Ageing Dev 2005, 126:913-922.
48. McIntire S.L., Jorgensen E., Kaplan J., Horvitz H.R. The GABAergic nervous system of Caenorhabditis elegans. Nature 1993, 364:337-341.
49. Mello C.C., Kramer J.M., Stinchcomb D., Ambros V. Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 1991, 10:3959-3970.
50. Murakami H., Bessinger K., Hellmann J., Murakami S. Manipulation of serotonin signal suppresses early phase of behavioral aging in Caenorhabditis elegans. Neurobiol. Aging 2008, 29:1093-1100.
51. Murchison D., Griffith W.H. Low-voltage activated calcium currents increase in basal forebrain neurons from aged rats. J. Neurophysiol 1995, 74:876-887.
52. Murchison D., Griffith W.H. High-voltage-activated calcium currents in basal forebrain neurons during aging. J. Neurophysiol 1996, 76:158-174.
53. Murphy G.G., Fedorov N.B., Giese K.P., Ohno M., Friedman E., Chen R., Silva A.J. Increased neuronal excitability, synaptic plasticity, and learning in aged Kvbeta1.1 knockout mice. Curr. Biol 2004, 14:1907-1915.
54. Nakai J., Ohkura M., Imoto K. A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat. Biotechnol 2001, 19:137-141.
55. Park E.C., Horvitz H.R. Mutations with dominant effects on the behavior and morphology of the nematode Caenorhabditis elegans. Genetics 1986, 113:821-852.
56. Pierce-Shimomura J.T., Chen B.L., Mun J.J., Ho R., Sarkis R., McIntire S.L. Genetic analysis of crawling and swimming locomotory patterns in C. elegans. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:20982-20987.
57. Reiner D.J., Weinshenker D., Tian H., Thomas J.H., Nishiwaki K., Miwa J., Gruninger T., Leboeuf B., Garcia L.R. Behavioral genetics of Caenorhabditis elegans unc-103-encoded erg-like K(+) channel. J. Neurogenet 2006, 20:41-66.
58. Salthouse T.A. Memory aging from 18 to 80. Alzheimer Dis. Assoc. Disord 2003, 17:162-167.
59. Sawin E.R., Ranganathan R., Horvitz H.R. C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 2000, 26:619-631.
60. Schnabel R., Schnabel H. Early determination in the C. elegans embryo: a gene, cib-1, required to specify a set of stem-cell-like blastomeres. Development 1990, 108:107-119.
61. Schreiber M.A., Pierce-Shimomura J.T., Chan S., Parry D., McIntire S.L. Manipulation of behavioral decline in Caenorhabditis elegans with the Rag GTPase raga-1. PLoS Genet 2010, 6:e1000972.
62. Simon A.F., Liang D.T., Krantz D.E. Differential decline in behavioral performance of Drosophila melanogaster with age. Mech. Ageing Dev 2006, 127:647-651.
63. Tank E.M., Rodgers K.E., Kenyon C. Spontaneous age-related neurite branching in Caenorhabditis elegans. J. Neurosci 2011, 31:9279-9288.
64. Thibault O., Hadley R., Landfield P.W. Elevated postsynaptic [Ca2+]i and L-type calcium channel activity in aged hippocampal neurons: relationship to impaired synaptic plasticity. J. Neurosci 2001, 21:9744-9756.
65. Thompson L.T., Moyer J.R., Disterhoft J.F. Transient changes in excitability of rabbit CA3 neurons with a time course appropriate to support memory consolidation. J. Neurophysiol 1996, 76:1836-1849.
66. Wu W.W., Oh M.M., Disterhoft J.F. Age-related biophysical alterations of hippocampal pyramidal neurons: implications for learning and memory. Ageing Res. Rev 2002, 1:181-207.