The effects of transient starvation persist through direct interactions between CaMKII and ether-a-go-go K+ channels in C. elegans males

Neuroscience

Volumn 175, Issue , 2011, Pages 1-17

  LeBoeuf, B ^a,b   Guo, X ^b   Garcia L R ^a,b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

C. elegans; CaMKII; Cholinergic signaling; Ether a go go K+ channels; Mating behavior; Starvation

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; POTASSIUM CHANNEL; POTASSIUM CHANNEL HERG; PROTEIN UNC 103; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CAENORHABDITIS ELEGANS; CARBOXY TERMINAL SEQUENCE; CHOLINERGIC ACTIVITY; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; LIFESPAN; MALE; MATING; MUSCLE CONTRACTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROGENY; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; SEIZURE; SEXUAL BEHAVIOR; SIGNAL TRANSDUCTION; STARVATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; ETHER-A-GO-GO POTASSIUM CHANNELS; FEMALE; FOOD DEPRIVATION; MALE; MUTATION; POTASSIUM CHANNELS; SEX CHARACTERISTICS; SEXUAL BEHAVIOR, ANIMAL; STARVATION;

EID: 78951469665     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.12.002     Document Type: Article

References (77)

1. Barriere A., Felix M.A. Natural variation and population genetics of Caenorhabditis elegans. WormBook 2005, 1-19.
2. Bastiani C.A., Gharib S., Simon M.I., Sternberg P.W. Caenorhabditis elegans Galphaq regulates egg-laying behavior via a PLCbeta-independent and serotonin-dependent signaling pathway and likely functions both in the nervous system and in muscle. Genetics 2003, 165:1805-1822.
3. Bayer K.U., De Koninck P., Leonard A.S., Hell J.W., Schulman H. Interaction with the NMDA receptor locks CaMKII in an active conformation. Nature 2001, 411:801-805.
4. Beelman C.A., Parker R. Differential effects of translational inhibition in cis and in trans on the decay of the unstable yeast MFA2 mRNA. J Biol Chem 1994, 269:9687-9692.
5. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
6. Burger J.M., Hwangbo D.S., Corby-Harris V., Promislow D.E. The functional costs and benefits of dietary restriction in Drosophila. Aging Cell 2007, 6:63-71.
7. Colbert H.A., Bargmann C.I. Environmental signals modulate olfactory acuity, discrimination, and memory in Caenorhabditis elegans. Learn Mem 1997, 4:179-191.
8. Colbran R.J. Targeting of calcium/calmodulin-dependent protein kinase II. Biochem J 2004, 378:1-16.
9. Colman R.J., Anderson R.M., Johnson S.C., Kastman E.K., Kosmatka K.J., Beasley T.M., Allison D.B., Cruzen C., Simmons H.A., Kemnitz J.W., Weindruch R. Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 2009, 325:201-204.
10. Croll N.A. Components and patterns in the behavior of the nematode Caenorhabditis elegans. J Zool 1975, 176:159-176.
11. Dani C., Blanchard J.M., Piechaczyk M., El Sabouty S., Marty L., Jeanteur P. Extreme instability of myc mRNA in normal and transformed human cells. Proc Natl Acad Sci U S A 1984, 81:7046-7050.
12. Dhahbi J.M., Kim H.J., Mote P.L., Beaver R.J., Spindler S.R. Temporal linkage between the phenotypic and genomic responses to caloric restriction. Proc Natl Acad Sci U S A 2004, 101:5524-5529.
13. 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.
14. Faumont S., Miller A.C., Lockery S.R. Chemosensory behavior of semi-restrained Caenorhabditis elegans. J Neurobiol 2005, 65:171-178.
15. Fontana L., Meyer T.E., Klein S., Holloszy J.O. Long-term calorie restriction is highly effective in reducing the risk for atherosclerosis in humans. Proc Natl Acad Sci U S A 2004, 101:6659-6663.
16. Ganetzky B., Robertson G.A., Wilson G.F., Trudeau M.C., Titus S.A. The eag family of K+ channels in Drosophila and mammals. Ann N Y Acad Sci 1999, 868:356-369.
17. Ganetzky B., Wu C.F. Neurogenetic analysis of potassium currents in Drosophila: synergistic effects on neuromuscular transmission in double mutants. J Neurogenet 1983, 1:17-28.
18. Garcia L.R., LeBoeuf B., Koo P. Diversity in mating behavior of hermaphroditic and male-female Caenorhabditis nematodes. Genetics 2007, 175:1761-1771.
19. Garcia L.R., Mehta P., Sternberg P.W. Regulation of distinct muscle behaviors controls the Celegans male's copulatory spicules during mating. Cell 2001, 107:777-788.
20. 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.
21. Granato M., Schnabel H., Schnabel R. pha-1, a selectable marker for gene transfer in C. elegans. Nucleic Acids Res 1994, 22:1762-1763.
22. 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.
23. 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.
24. Hodgkin J.A., Horvitz H.R., Brenner S. Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics 1979, 91:67-94.
25. Horvitz H.R., Chalfie M., Trent C., Sulston J.E., Evans P.D. Serotonin and octopamine in the nematode Caenorhabditis elegans. Science 1982, 216:1012-1014.
26. Hulshoff Pol H.E., Hoek H.W., Susser E., Brown A.S., Dingemans A., Schnack H.G., van Haren N.E., Pereira Ramos L.M., Gispen-de Wied C.C., Kahn R.S. Prenatal exposure to famine and brain morphology in schizophrenia. Am J Psychiatry 2000, 157:1170-1172.
27. Jenkins D.E., Schultz J.E., Matin A. Starvation-induced cross protection against heat or H2O2 challenge in Escherichia coli. J Bacteriol 1988, 170:3910-3914.
28. Jiang J.C., Jaruga E., Repnevskaya M.V., Jazwinski S.M. An intervention resembling caloric restriction prolongs life span and retards aging in yeast. FASEB J 2000, 14:2135-2137.
29. Jones D., Dixon D.K., Graham R.W., Candido E.P. Differential regulation of closely related members of the hsp16 gene family in Caenorhabditis elegans. DNA 1989, 8:481-490.
30. Ju M., Wray D. Molecular identification and characterisation of the human eag2 potassium channel. FEBS Lett 2002, 524:204-210.
31. Kaplan W.D., Trout W.E. The behavior of four neurological mutants of Drosophila. Genetics 1969, 61:399-409.
32. Kolodziej S.J., Hudmon A., Waxham M.N., Stoops J.K. Three-dimensional reconstructions of calcium/calmodulin-dependent (CaM) kinase IIalpha and truncated CaM kinase IIalpha reveal a unique organization for its structural core and functional domains. J Biol Chem 2000, 275:14354-14359.
33. Laird-Offringa I.A., de Wit C.L., Elfferich P., van der Eb A.J. Poly(A) tail shortening is the translation-dependent step in c-myc mRNA degradation. Mol Cell Biol 1990, 10:6132-6140.
34. LeBoeuf B., Gruninger T.R., Garcia L.R. Food deprivation attenuates seizures through CaMKII and EAG K+ channels. PLoS Genet 2007, 3:1622-1632.
35. Lee B.H., Ashrafi K. A TRPV channel modulates C. elegans neurosecretion, larval starvation survival, and adult lifespan. PLoS Genet 2008, 4:e1000213.
36. Lin S.J., Defossez P.A., Guarente L. Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae. Science 2000, 289:2126-2128.
37. Lipton J., Kleemann G., Ghosh R., Lints R., Emmons S.W. Mate searching in Caenorhabditis elegans: a genetic model for sex drive in a simple invertebrate. J Neurosci 2004, 24:7427-7434.
38. Liu K.S., Sternberg P.W. Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron 1995, 14:79-89.
39. Loer C.M., Kenyon C.J. Serotonin-deficient mutants and male mating behavior in the nematode Caenorhabditis elegans. J Neurosci 1993, 13:5407-5417.
40. Mair W., Goymer P., Pletcher S.D., Partridge L. Demography of dietary restriction and death in Drosophila. Science 2003, 301:1731-1733.
41. Marble D.D., Hegle A.P., Snyder E.D., Dimitratos S., Bryant P.J., Wilson G.F. Camguk/CASK enhances Ether-a-go-go potassium current by a phosphorylation-dependent mechanism. J Neurosci 2005, 25:4898-4907.
42. Mohri A., Kodama E., Kimura K.D., Koike M., Mizuno T., Mori I. Genetic control of temperature preference in the nematode Caenorhabditis elegans. Genetics 2005, 169:1437-1450.
43. Morris E.P., Torok K. Oligomeric structure of alpha-calmodulin-dependent protein kinase II. J Mol Biol 2001, 308:1-8.
44. Occhiodoro T., Bernheim L., Liu J.H., Bijlenga P., Sinnreich M., Bader C.R., Fischer-Lougheed J. Cloning of a human ether-a-go-go potassium channel expressed in myoblasts at the onset of fusion. FEBS Lett 1998, 434:177-182.
45. Pardo L.A., del Camino D., Sanchez A., Alves F., Bruggemann A., Beckh S., Stuhmer W. Oncogenic potential of EAG K(+) channels. EMBO J 1999, 18:5540-5547.
46. 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.
47. Pearson R.B., Woodgett J.R., Cohen P., Kemp B.E. Substrate specificity of a multifunctional calmodulin-dependent protein kinase. J Biol Chem 1985, 260:14471-14476.
48. Polivy J., Herman P., Coelho J.S. Caloric restriction in the presence of attractive food cues: external cues, eating, and weight. Physiol Behav 2008, 94:729-733.
49. Pradeep K.K., Cheriyan J., Suma Priya S.D., Rajeevkumar R., Mayadevi M., Praseeda M., Omkumar R.V. Regulation of Ca2+/calmodulin-dependent protein kinase II catalysis by N-methyl-d-aspartate receptor subunit 2B. Biochem J 2009, 419:123-132. 4 p following 132.
50. Reiner D.J., Newton E.M., Tian H., Thomas J.H. Diverse behavioral defects caused by mutations in Caenorhabditis elegans unc-43 CaM kinase II. Nature 1999, 402:199-203.
51. Reiner D.J., Weinshenker D., Thomas J.H. Analysis of dominant mutations affecting muscle excitation in Caenorhabditis elegans. Genetics 1995, 141:961-976.
52. 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.
53. Reser J.E. Schizophrenia and phenotypic plasticity: schizophrenia may represent a predictive, adaptive response to severe environmental adversity that allows both bioenergetic thrift and a defensive behavioral strategy. Med Hypotheses 2007, 69:383-394.
54. Rosenberg O.S., Deindl S., Sung R.J., Nairn A.C., Kuriyan J. Structure of the autoinhibited kinase domain of CaMKII and SAXS analysis of the holoenzyme. Cell 2005, 123:849-860.
55. 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.
56. Schedl T., Kimble J. fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics 1988, 119:43-61.
57. Schnabel H., Schnabel R. An organ-specific differentiation gene, pha-1, from Caenorhabditis elegans. Science 1990, 250:686-688.
58. Selesniemi K., Lee H.J., Tilly J.L. Moderate caloric restriction initiated in rodents during adulthood sustains function of the female reproductive axis into advanced chronological age. Aging Cell 2008, 7:622-629.
59. Smith E.D., Kaeberlein T.L., Lydum B.T., Sager J., Welton K.L., Kennedy B.K., Kaeberlein M. Age- and calorie-independent life span extension from dietary restriction by bacterial deprivation in Caenorhabditis elegans. BMC Dev Biol 2008, 8:49.
60. Strack S., McNeill R.B., Colbran R.J. Mechanism and regulation of calcium/calmodulin-dependent protein kinase II targeting to the NR2B subunit of the N-methyl-d-aspartate receptor. J Biol Chem 2000, 275:23798-23806.
61. Stringham E.G., Dixon D.K., Jones D., Candido E.P. Temporal and spatial expression patterns of the small heat shock (hsp16) genes in transgenic Caenorhabditis elegans. Mol Biol Cell 1992, 3:221-233.
62. Sulston J.E., Albertson D.G., Thomas J.N. The Caenorhabditis elegans male: postembryonic development of nongonadal structures. Dev Biol 1980, 78:542-576.
63. Sun X.X., Hodge J.J.L., Zhou Y., Nguyen M., Griffith L.C. The eag potassium channel binds and locally activates calcium/calmodulin-dependent protein kinase II. J Biol Chem 2004, 279:10206-10214.
64. Susser E., Neugebauer R., Hoek H.W., Brown A.S., Lin S., Labovitz D., Gorman J.M. Schizophrenia after prenatal famine. Further evidence. Arch Gen Psychiatry 1996, 53:25-31.
65. Sze J.Y., Victor M., Loer C., Shi Y., Ruvkun G. Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 2000, 403:560-564.
66. Terskikh A., Fradkov A., Ermakova G., Zaraisky A., Tan P., Kajava A.V., Zhao X., Lukyanov S., Matz M., Kim S., Weissman I., Siebert P. "Fluorescent timer": protein that changes color with time. Science 2000, 290:1585-1588.
67. Trent C., Tsung N., Horvitz H.R. Egg-laying defective mutants of the nematode Caenorhabditis elegans. Genetics 1983, 104:619-647.
68. Tsui J., Inagaki M., Schulman H. Calcium/calmodulin-dependent protein kinase II (CaMKII) localization acts in concert with substrate targeting to create spatial restriction for phosphorylation. J Biol Chem 2005, 280:9210-9216.
69. Victora C.G., Adair L., Fall C., Hallal P.C., Martorell R., Richter L., Sachdev H.S. Maternal and child undernutrition: consequences for adult health and human capital. Lancet 2008, 371:340-357.
70. Vitousek K.M., Manke F.P., Gray J.A., Vitousek M.N. Caloric restriction for longevity: II. The systematic neglect of behavioral and psychological outcomes in animal research. Eur Eat Disord Rev 2004, 12:338-360.
71. Wahlbeck K., Forsen T., Osmond C., Barker D.J., Eriksson J.G. Association of schizophrenia with low maternal body mass index, small size at birth, and thinness during childhood. Arch Gen Psychiatry 2001, 58:48-52.
72. Wang Z., Wilson G.F., Griffith L.C. Calcium/calmodulin-dependent protein kinase II phosphorylates and regulates the Drosophila eag potassium channel. J Biol Chem 2002, 277:24022-24029.
73. Ward S., Carrel J.S. Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol 1979, 73:304-321.
74. Warmke J., Drysdale R., Ganetzky B. A distinct potassium channel polypeptide encoded by the Drosophila eag locus. Science 1991, 252:1560-1562.
75. Weinshenker D., Wei A., Salkoff L., Thomas J.H. Block of an ether-a-go-go-like K(+) channel by imipramine rescues egl-2 excitation defects in Caenorhabditis elegans. J Neurosci 1999, 19:9831-9840.
76. Wilson G.F., Wang Z., Chouinard S.W., Griffith L.C., Ganetzky B. Interaction of the K channel beta subunit, hyperkinetic, with eag family members. J Biol Chem 1998, 273:6389-6394.
77. Wu Q., Zhang Y., Xu J., Shen P. Regulation of hunger-driven behaviors by neural ribosomal S6 kinase in Drosophila. Proc Natl Acad Sci U S A 2005, 102:13289-13294.