Rescue of the Learning Defect in Dunce, a Drosophila Learning Mutant, by an Allele of Rutabaga, a Second Learning Mutant

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1990 Apr 1

PMID 2157213

Citations 11

Authors

M B Feany

Affiliations

Soon will be listed here.

Abstract

rutabaga1 (rut1), a Drosophila learning mutant, has adenylate cyclase (EC 4.6.1.1) with reduced basal activity and the absence of calcium/calmodulin-stimulated activity. A second learning mutant, dunce, is defective in cyclic AMP degradation due to decreased or absent phosphodiesterase activity. These opposing biochemical defects allow rut1 to partially suppress the female sterility caused by elevated cyclic AMP levels in dunce flies. Selection of mutations that suppress dunce sterility has led to the isolation of two rutabaga alleles. The alleles (rut2 and rut3) decrease basal adenylate cyclase activity [Bellen, H. J., Gregory, B. K., Olsson, C. L. & Kiger, J. A. (1987) Dev. Biol. 121, 432-444] but, unlike the original rutabaga mutation, leave the calcium/calmodulin-stimulated activity intact. Behaviorally, the two alleles also differ from rut1. One of the mutations partially rescues the dunce learning defect, and flies bearing both alleles learn. Calcium responsiveness may thus be the crucial component of adenylate cyclase activity required for associative learning.

Citing Articles

Embryonic cAMP and developmental potential in Drosophila melanogaster.

Whitehouse-Hills S, Bellen H, Kiger Jr J Rouxs Arch Dev Biol. 2017; 201(4):257-264.

PMID: 28305849 DOI: 10.1007/BF00188756.

Cyclic nucleotide signaling is required during synaptic refinement at the Drosophila neuromuscular junction.

Vonhoff F, Keshishian H Dev Neurobiol. 2016; 77(1):39-60.

PMID: 27281494 PMC: 5148738. DOI: 10.1002/dneu.22407.

PKA and cAMP/CNG Channels Independently Regulate the Cholinergic Ca(2+)-Response of Drosophila Mushroom Body Neurons.

Pavot P, Carbognin E, Martin J eNeuro. 2015; 2(2).

PMID: 26464971 PMC: 4596083. DOI: 10.1523/ENEURO.0054-14.2015.

C. elegans positive olfactory associative memory is a molecularly conserved behavioral paradigm.

Stein G, Murphy C Neurobiol Learn Mem. 2014; 115:86-94.

PMID: 25108196 PMC: 4250358. DOI: 10.1016/j.nlm.2014.07.011.

A novel role for ecdysone in Drosophila conditioned behavior: linking GPCR-mediated non-canonical steroid action to cAMP signaling in the adult brain.

Ishimoto H, Wang Z, Rao Y, Wu C, Kitamoto T PLoS Genet. 2013; 9(10):e1003843.

PMID: 24130506 PMC: 3794910. DOI: 10.1371/journal.pgen.1003843.

References

Livingstone M, Tempel B . Genetic dissection of monoamine neurotransmitter synthesis in Drosophila. Nature. 1983; 303(5912):67-70. DOI: 10.1038/303067a0. View

Dudai Y, Zvi S . Adenylate cyclase in the Drosophila memory mutant rutabaga displays an altered Ca2+ sensitivity. Neurosci Lett. 1984; 47(2):119-24. DOI: 10.1016/0304-3940(84)90416-6. View

Kauvar L . Defective cyclic adenosine 3':5'-monophosphate phosphodiesterase in the Drosophila memory mutant dunce. J Neurosci. 1982; 2(10):1347-58. PMC: 6564408. View

Bellen H, Gregory B, Olsson C, Kiger Jr J . Two Drosophila learning mutants, dunce and rutabaga, provide evidence of a maternal role for cAMP on embryogenesis. Dev Biol. 1987; 121(2):432-44. DOI: 10.1016/0012-1606(87)90180-1. View

Krupinski J, Coussen F, Bakalyar H, Tang W, Feinstein P, Orth K . Adenylyl cyclase amino acid sequence: possible channel- or transporter-like structure. Science. 1989; 244(4912):1558-64. DOI: 10.1126/science.2472670. View

Kandel E, Abrams T, Bernier L, Carew T, Hawkins R, Schwartz J . Classical conditioning and sensitization share aspects of the same molecular cascade in Aplysia. Cold Spring Harb Symp Quant Biol. 1983; 48 Pt 2:821-30. DOI: 10.1101/sqb.1983.048.01.085. View

Tempel B, Livingstone M, Quinn W . Mutations in the dopa decarboxylase gene affect learning in Drosophila. Proc Natl Acad Sci U S A. 1984; 81(11):3577-81. PMC: 345552. DOI: 10.1073/pnas.81.11.3577. View

Salomon Y . Adenylate cyclase assay. Adv Cyclic Nucleotide Res. 1979; 10:35-55. View

Tully T, Quinn W . Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A. 1985; 157(2):263-77. DOI: 10.1007/BF01350033. View

10.

Byers D, Davis R, Kiger Jr J . Defect in cyclic AMP phosphodiesterase due to the dunce mutation of learning in Drosophila melanogaster. Nature. 1981; 289(5793):79-81. DOI: 10.1038/289079a0. View

11.

Livingstone M, Sziber P, Quinn W . Loss of calcium/calmodulin responsiveness in adenylate cyclase of rutabaga, a Drosophila learning mutant. Cell. 1984; 37(1):205-15. DOI: 10.1016/0092-8674(84)90316-7. View

12.

Livingstone M . Genetic dissection of Drosophila adenylate cyclase. Proc Natl Acad Sci U S A. 1985; 82(17):5992-6. PMC: 390680. DOI: 10.1073/pnas.82.17.5992. View

13.

Davis R, Kiger Jr J . Dunce mutants of Drosophila melanogaster: mutants defective in the cyclic AMP phosphodiesterase enzyme system. J Cell Biol. 1981; 90(1):101-7. PMC: 2111840. DOI: 10.1083/jcb.90.1.101. View

14.

Dudai Y . Mutations affect storage and use of memory differentially in Drosophila. Proc Natl Acad Sci U S A. 1983; 80(17):5445-8. PMC: 384273. DOI: 10.1073/pnas.80.17.5445. View

15.

Chen C, Denome S, Davis R . Molecular analysis of cDNA clones and the corresponding genomic coding sequences of the Drosophila dunce+ gene, the structural gene for cAMP phosphodiesterase. Proc Natl Acad Sci U S A. 1986; 83(24):9313-7. PMC: 387128. DOI: 10.1073/pnas.83.24.9313. View

16.

Dudai Y, Jan Y, Byers D, Quinn W, Benzer S . dunce, a mutant of Drosophila deficient in learning. Proc Natl Acad Sci U S A. 1976; 73(5):1684-8. PMC: 430364. DOI: 10.1073/pnas.73.5.1684. View

17.

Bradford M . A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976; 72:248-54. DOI: 10.1016/0003-2697(76)90527-3. View

18.

Quinn W, Harris W, Benzer S . Conditioned behavior in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1974; 71(3):708-12. PMC: 388082. DOI: 10.1073/pnas.71.3.708. View