Abstract
The Shaker complex (ShC) spans over 350 kb in the 16F region of the X chromosome. It can be dissected by means of aneuploids into three main sections: the maternal effect (ME), the viable (V) and the haplolethal (HL) regions. The mutational analysis of ShC shows a high density of antimorphic mutations among 12 lethal complementation groups in addition to 14 viable alleles. The complex is the structural locus of a family of potassium channels as well as a number of functions relevant to the biology of the nervous system. The constituents of ShC seem to be linked by functional relationships in view of the similarity of the phenotypes, antimorphic nature of their mutations and the behavior in transheterozygotes. We discuss the relationship between the genetic organization of ShC and the functional coupling of potassium currents with the other functions encoded in the complex.
Full Text
The Full Text of this article is available as a PDF (2.6 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- AUERBACH C., MOSER H. An analysis of the mutagenic action of formaldehyde-food. I. Sensitivity of Drosophila germ cells. Z Indukt Abstamm Vererbungsl. 1953;85(4):479–504. doi: 10.1007/BF00308298. [DOI] [PubMed] [Google Scholar]
- Barbas J. A., Rubio N., Pedroso E., Pongs O., Ferrús A. Antibodies against Drosophila potassium channels identify membrane proteins across species. Brain Res Mol Brain Res. 1989 Mar;5(2):171–176. doi: 10.1016/0169-328x(89)90008-9. [DOI] [PubMed] [Google Scholar]
- Baumann A., Grupe A., Ackermann A., Pongs O. Structure of the voltage-dependent potassium channel is highly conserved from Drosophila to vertebrate central nervous systems. EMBO J. 1988 Aug;7(8):2457–2463. doi: 10.1002/j.1460-2075.1988.tb03092.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baumann A., Krah-Jentgens I., Müller R., Müller-Holtkamp F., Seidel R., Kecskemethy N., Casal J., Ferrus A., Pongs O. Molecular organization of the maternal effect region of the Shaker complex of Drosophila: characterization of an I(A) channel transcript with homology to vertebrate Na channel. EMBO J. 1987 Nov;6(11):3419–3429. doi: 10.1002/j.1460-2075.1987.tb02665.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Beall C. J., Sepanski M. A., Fyrberg E. A. Genetic dissection of Drosophila myofibril formation: effects of actin and myosin heavy chain null alleles. Genes Dev. 1989 Feb;3(2):131–140. doi: 10.1101/gad.3.2.131. [DOI] [PubMed] [Google Scholar]
- Bryant P. J., Zornetzer M. Mosaic analysis of lethal mutations in Drosophila. Genetics. 1973 Dec;75(4):623–637. doi: 10.1093/genetics/75.4.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Byrne J. H. Cellular analysis of associative learning. Physiol Rev. 1987 Apr;67(2):329–439. doi: 10.1152/physrev.1987.67.2.329. [DOI] [PubMed] [Google Scholar]
- Gisselmann G., Sewing S., Madsen B. W., Mallart A., Angaut-Petit D., Müller-Holtkamp F., Ferrus A., Pongs O. The interference of truncated with normal potassium channel subunits leads to abnormal behaviour in transgenic Drosophila melanogaster. EMBO J. 1989 Aug;8(8):2359–2364. doi: 10.1002/j.1460-2075.1989.tb08364.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Homyk T., Jr, Emerson C. P., Jr Functional interactions between unlinked muscle genes within haploinsufficient regions of the Drosophila genome. Genetics. 1988 May;119(1):105–121. doi: 10.1093/genetics/119.1.105. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hotta Y., Benzer S. Mapping of behaviour in Drosophila mosaics. Nature. 1972 Dec 29;240(5383):527–535. doi: 10.1038/240527a0. [DOI] [PubMed] [Google Scholar]
- Jaffe L. F. Control of development by ionic currents. Soc Gen Physiol Ser. 1979;33:199–231. [PubMed] [Google Scholar]
- Kamb A., Iverson L. E., Tanouye M. A. Molecular characterization of Shaker, a Drosophila gene that encodes a potassium channel. Cell. 1987 Jul 31;50(3):405–413. doi: 10.1016/0092-8674(87)90494-6. [DOI] [PubMed] [Google Scholar]
- Kamb A., Tseng-Crank J., Tanouye M. A. Multiple products of the Drosophila Shaker gene may contribute to potassium channel diversity. Neuron. 1988 Jul;1(5):421–430. doi: 10.1016/0896-6273(88)90192-4. [DOI] [PubMed] [Google Scholar]
- Kandel E. R., Schwartz J. H. Molecular biology of learning: modulation of transmitter release. Science. 1982 Oct 29;218(4571):433–443. doi: 10.1126/science.6289442. [DOI] [PubMed] [Google Scholar]
- Karlik C. C., Mahaffey J. W., Coutu M. D., Fyrberg E. A. Organization of contractile protein genes within the 88F subdivision of the D. melanogaster third chromosome. Cell. 1984 Jun;37(2):469–481. doi: 10.1016/0092-8674(84)90377-5. [DOI] [PubMed] [Google Scholar]
- Kline D., Robinson K. R., Nuccitelli R. Ion currents and membrane domains in the cleaving Xenopus egg. J Cell Biol. 1983 Dec;97(6):1753–1761. doi: 10.1083/jcb.97.6.1753. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Koto M., Tanouye M. A., Ferrus A., Thomas J. B., Wyman R. J. The morphology of the cervical giant fiber neuron of Drosophila. Brain Res. 1981 Sep 28;221(2):213–217. doi: 10.1016/0006-8993(81)90772-1. [DOI] [PubMed] [Google Scholar]
- Landel C. P., Krause M., Waterston R. H., Hirsh D. DNA rearrangements of the actin gene cluster in Caenorhabditis elegans accompany reversion of three muscle mutants. J Mol Biol. 1984 Dec 15;180(3):497–513. doi: 10.1016/0022-2836(84)90024-x. [DOI] [PubMed] [Google Scholar]
- Levitan I. B. Modulation of ion channels in neurons and other cells. Annu Rev Neurosci. 1988;11:119–136. doi: 10.1146/annurev.ne.11.030188.001003. [DOI] [PubMed] [Google Scholar]
- Logothetis D. E., Kurachi Y., Galper J., Neer E. J., Clapham D. E. The beta gamma subunits of GTP-binding proteins activate the muscarinic K+ channel in heart. Nature. 1987 Jan 22;325(6102):321–326. doi: 10.1038/325321a0. [DOI] [PubMed] [Google Scholar]
- Orgad S., Llamazares S., Dudai Y., Ferrús A. The Drosophila Mutant tetanic Interacts with a Gene Complex Including the Structural Locus of K+ Channels and Shows Altered Dephosphorylation and Learning. Eur J Neurosci. 1989 Jul;1(4):367–373. doi: 10.1111/j.1460-9568.1989.tb00801.x. [DOI] [PubMed] [Google Scholar]
- Pentz E. S., Black B. C., Wright T. R. A diphenol oxidase gene is part of a cluster of genes involved in catecholamine metabolism and sclerotization in drosophila. I. Identification of the biochemical defect in Dox-A2 [l(2)37Bf] mutants. Genetics. 1986 Apr;112(4):823–841. doi: 10.1093/genetics/112.4.823. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ripoll P. Behavior of somatic cells homozygous for zygotic lethals in Drosophila melanogaster. Genetics. 1977 Jun;86(2 Pt 1):357–376. [PMC free article] [PubMed] [Google Scholar]
- Roehrdanz R. L., Lucchesi J. C. Mutational Events in the Triplo- and Haplo-Lethal Region (83de) of the DROSOPHILA MELANOGASTER Genome. Genetics. 1980 Jun;95(2):355–366. doi: 10.1093/genetics/95.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rudy B. Diversity and ubiquity of K channels. Neuroscience. 1988 Jun;25(3):729–749. doi: 10.1016/0306-4522(88)90033-4. [DOI] [PubMed] [Google Scholar]
- Salkoff L., Wyman R. Genetic modification of potassium channels in Drosophila Shaker mutants. Nature. 1981 Sep 17;293(5829):228–230. doi: 10.1038/293228a0. [DOI] [PubMed] [Google Scholar]
- Schwarz T. L., Tempel B. L., Papazian D. M., Jan Y. N., Jan L. Y. Multiple potassium-channel components are produced by alternative splicing at the Shaker locus in Drosophila. Nature. 1988 Jan 14;331(6152):137–142. doi: 10.1038/331137a0. [DOI] [PubMed] [Google Scholar]
- Solc C. K., Zagotta W. N., Aldrich R. W. Single-channel and genetic analyses reveal two distinct A-type potassium channels in Drosophila. Science. 1987 May 29;236(4805):1094–1098. doi: 10.1126/science.2437657. [DOI] [PubMed] [Google Scholar]
- Stühmer W., Stocker M., Sakmann B., Seeburg P., Baumann A., Grupe A., Pongs O. Potassium channels expressed from rat brain cDNA have delayed rectifier properties. FEBS Lett. 1988 Dec 19;242(1):199–206. doi: 10.1016/0014-5793(88)81015-9. [DOI] [PubMed] [Google Scholar]
- Tanouye M. A., Ferrus A. Action potentials in normal and Shaker mutant Drosophila. J Neurogenet. 1985 Sep;2(4):253–271. doi: 10.3109/01677068509102322. [DOI] [PubMed] [Google Scholar]
- Tanouye M. A., Ferrus A., Fujita S. C. Abnormal action potentials associated with the Shaker complex locus of Drosophila. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6548–6552. doi: 10.1073/pnas.78.10.6548. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tansey T., Mikus M. D., Dumoulin M., Storti R. V. Transformation and rescue of a flightless Drosophila tropomyosin mutant. EMBO J. 1987 May;6(5):1375–1385. doi: 10.1002/j.1460-2075.1987.tb02378.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tempel B. L., Jan Y. N., Jan L. Y. Cloning of a probable potassium channel gene from mouse brain. Nature. 1988 Apr 28;332(6167):837–839. doi: 10.1038/332837a0. [DOI] [PubMed] [Google Scholar]
- Tempel B. L., Papazian D. M., Schwarz T. L., Jan Y. N., Jan L. Y. Sequence of a probable potassium channel component encoded at Shaker locus of Drosophila. Science. 1987 Aug 14;237(4816):770–775. doi: 10.1126/science.2441471. [DOI] [PubMed] [Google Scholar]
- Timpe L. C., Schwarz T. L., Tempel B. L., Papazian D. M., Jan Y. N., Jan L. Y. Expression of functional potassium channels from Shaker cDNA in Xenopus oocytes. Nature. 1988 Jan 14;331(6152):143–145. doi: 10.1038/331143a0. [DOI] [PubMed] [Google Scholar]
- Walters E. T., Byrne J. H. Associative conditioning of single sensory neurons suggests a cellular mechanism for learning. Science. 1983 Jan 28;219(4583):405–408. doi: 10.1126/science.6294834. [DOI] [PubMed] [Google Scholar]
- Weydert A., Daubas P., Lazaridis I., Barton P., Garner I., Leader D. P., Bonhomme F., Catalan J., Simon D., Guénet J. L. Genes for skeletal muscle myosin heavy chains are clustered and are not located on the same mouse chromosome as a cardiac myosin heavy chain gene. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7183–7187. doi: 10.1073/pnas.82.21.7183. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wieschaus E. A combined genetic and mosaic approach to the study of oogenesis in Drosophila. Basic Life Sci. 1980;16:85–94. doi: 10.1007/978-1-4684-7968-3_7. [DOI] [PubMed] [Google Scholar]
- Wu C. F., Haugland F. N. Voltage clamp analysis of membrane currents in larval muscle fibers of Drosophila: alteration of potassium currents in Shaker mutants. J Neurosci. 1985 Oct;5(10):2626–2640. doi: 10.1523/JNEUROSCI.05-10-02626.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zabin I., Villarejo M. R. Protein complementation. Annu Rev Biochem. 1975;44:295–313. doi: 10.1146/annurev.bi.44.070175.001455. [DOI] [PubMed] [Google Scholar]
- de la Pompa J. L., Garcia J. R., Ferrús A. Genetic analysis of muscle development in Drosophila melanogaster. Dev Biol. 1989 Feb;131(2):439–454. doi: 10.1016/s0012-1606(89)80016-8. [DOI] [PubMed] [Google Scholar]