Abstract
After the devastation of genetics in our country, Academician Leon A. Orbeli has provided an opportunity for the studies on evolutionary conservatism of genes controlling the main properties of the higher nervous activity and conditioning. For the last few years, determination and bioinformatic analysis of genome sequences in the plant, worm, Drosophila, and human genome have revealed, indeed, a high interspecies homology of genes. Studies on Drosophila mutants have shown that components of intracellular signalization systems regulating neuronal functions and gene expression are organized in supramolecular complexes. It has become evident that the chromosomal architecture predetermines the appearance of deletions, duplications, insertions, and translocations and, therefore, plays an important role not only in evolution but also in generating human pathological syndromes with multiple manifestations, including cognitive dysfunctions. There appeared a new approach, comparative genomics, that allows revealing functions of human disease genes on the basis of their sequence homology to the known Drosophila gene with various well-studied mutant phenotypes. For this reason, the Drosophila genes should be saturated with mutant phenotypes, and these are to be studied in comparison with the chromosomal architecture. Our complex behavioral and molecular-genetic study of spontaneous, induced, and P-insertional mutations in the Drosophila agnostic locus and the bioinformatic analyses of genomic sequences has allowed us to assign the locus to the Drosophila genomic scaffold AE003489 from the 11AB X-chromosomal region that contains the CG1848 gene coding for LIM-kinase 1. Mutations, insertions, and deletions in the agnostic locus lead to an increased activity of Ca2+/calmodulin-dependent PDE1, resistance to ether, an inactivator of synaptic transmission, impairments of the brain structures, learning and memory defects in conditioned courtship suppression paradigm, alterations in sound production and in structural-functional chromosomal organization. Therefore, the agnostic locus represents a model to study the human Williams syndrome with multiple dysfunctions due to a contiguous deletion in the 7q11.23 spanning 17 genes, among them the gene for LIM-kinase 1 presumed to be responsible for cognitive defects. The Williams syndrome is considered to be a most efficient model to study human cognition, human genome organization, and evolution.
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REFERENCES
Lobashev, M.E., Principle of Conditioning in Behavior of Invertebrates,Usp. Sovr. Biol.,1951, vol.31, pp.13-37.
Lobashev, M.E., On Parallel-Analogous and Homologous Lines of Development of the Basic Properties of the Higher Nervous Activity in Phylogenesis of Animals,Materialy 2-go nauchnogo soveshchaniya, posvyashchennogo pamyati L.A. Orbeli(Proceedings of the 2nd Scientific Meeting Devoted to the Memory of L.A. Orbeli), Moscow-Leningrad, 1960, pp. 16-23.
Ponomarenko, V.V., Lopatina, N.G., Marshin, V.G., Nikitina, I.A., Smirnova, G.P., and Chesnokova, E.G., On Realization of Genetic Information Responsible for the Nervous System Activity and Behavior in Animals of Different Phylogenetic Levels,Aktual'nye problemy genetiki povedeniya(Current Problems of Behavioral Genetics), Leningrad: Nauka, 1975, pp. 195.
Lopatina, N.G., Marshin, V.G., Ponomarenko, V.V., Smirnova, G.P., and Sogrin, B.V., Study of the Neurophysiological Trait, the Rate of Ether Narcosis, in Connection with Behavior of Insects (Drosophila, Bee). I. The Character of Genetical and Ontogenetic Variability of the Ether Narcosis Rate in Drosophila Strains and Bee Races, Selection of Drosophila Strains for this Trait,Genetika,1977, vol. 13, pp. 1767-1777.
Ponomarenko, V.V., and Lopatina, N.G., Mutations of Homologous Genes in Comparative Genetical Studies of Behavior, Voprosy obshchei genetiki (Problems of General Genetics),Moscow: Nauka,1981, pp.313-323.
Lobashev, M.E., Ponomarenko, V.V., Polyanskaya, G.G., Tsapygina, R.I., On the Role of the Nervous System in Regulation of Different Genetical and Cytogenetic Processes,Zh. Evol. Biokhim. Fiziol., 1973, vol.9, pp.396-406.
Benzer, S., From Gene to Behavior,Aktual'nye problemy genetiki povedeniya(Current Problems in Behavioral Genetics),Leningrad: Nauka,1975, pp.5-22.
Heisenberg, M., Central Brain Function in Insects: Genetic Studies on the Mushroom Bodies and Central Complex in Drosophila, Fortschr. Zool.,1994, vol.39, pp. 61-79.
Savvateeva, E.V., and Kamyshev, N.G., Behavioral Effects of Temperature Sensitive Mutations Affecting Metabolism of cAMP in D. melanogaster, Pharm. Biochem. Behav.,1981, vol. 14, pp. 603-611.
Bier, E., Vaessin, H., Shepherd, S., Lee, K., McCall, K., Barbel, S., Ackerman, L., Carretto, L., Uemura, T., Grell, E., Jan, Y., and Jan, Y.N., Searching for Pattern and Mutation in the Drosophila Genome with a P-lacZ Vector,Genes Develop.,1989, vol. 3, pp. 1273-1287.
Spradling, A., Stern, D., Kiss, I., Laverty, T., and Rubin, G., Gene Disruptions Using P Transposable Elements: An Integral Component of the Drosophila Genome Project,Proc. Natl Acad. Sci. USA,1995, vol. 92, pp.10824-10830.
Adams, M.D., Celniker, S.E., Holt, R.A., Evance, C.A., Gocayne, J.D., et al., The Genome Sequence of Drosophila melanogaster,Science,2000, vol.287, pp. 2185-2195.
Venter, J.C., Adams, M.D., Myers, E.W., et al., The Sequence of the Human Genome,Science,2001, vol. 291, pp. 1304-1351.
Rubin, G.M., Yandell, M.D., Wortman, J.R., Gabor, M.G.L., Nelson, C.R., et al.,Comparative Genomics of the Eukaryotes,Science,2000, vol. 287, pp.2204-2215.
Huala, E., Dickerman, A.W., Garcia-Hernandez, M., Weems, D., Reiser, L., et al., The Arabidopsis Information Resource (TAIR): A Comprehensive Database and Web-Based Information Retrieval, Analysis, and Visualization System for a Model Plant,Nucleic Acids Res.,2001, vol.29, pp.102-105.
http://www.ncbi.nlm.nih.gov/BLAST
Hartley, D., Drosophila Inherit Diseases,Nature Genetics, 1996, vol.13, pp. 133-134.
Ji, Y., Eichler, E.E., Schwartz, S., and Nicholls, R.D., Structure of Chromosomal Duplicons and Their Role in Mediating Human Genomic Disorders,Genome Res.,2000, vol. 10, pp.597-610.
Davis, R.L. and Dauwalder, B., The Drosophila dunce Locus: Learning and Memory Genes in the Fly,Trends Genet.,1991, vol.7, pp. 224-229.
Feany, M. and Quinn, W.G., A Neuropeptide Gene Defined by the Drosophila Memory Mutant Amnesiac, Science, 1995, vol. 268, pp.869-873. agnostic locus mutants may be considered as an unique model for Williams syndrome, i.e., for coupling genomic structure and cognition [83]. 730 JOURNAL OF EVOLUTIONARY BIOCHEMISTRY AND PHYSIOLOGY Vol. 38 No. 6 2002 SAVVATEEVA-POPOVA et al.
Bolger, G., Michaeli, T., Martins, T., St. John, T., Steiner, B., Rodgers, L., Riggs, M., Wigler, M., and Ferguson, K., A Family of Human Phosphodiesterases Homologous to the dunce Learning and Memory Gene Product of Drosophila melanogaster are Potential Targets for Antidepressant Drugs,Mol. Cell. Biol., 1993, vol.13, pp. 6558-6571.
Gasic, G., Systems and Molecular Genetic Approaches Converge to Tackle Learning and Memory,Neuron, 1995, vol. 15, pp.507-512.
Kandel, E. and Abel, T., Neuropeptides, Adenylyl Cyclase, and Memory Storage,Science,1995, vol.68, pp.825-826.
West, A.E., Chen, W.G., Dalva, M.B., Dolmetsch, R.E., Kornhauser, J.M., Shaywitz, A., Takasu, M.A., Tao, X., and Greenberg, M.E., Calcium Regulation of Neuronal Gene Expression,Proc. Natl Acad. Sci. USA,2001, vol. 98, pp. 11 024-11 031.
Putney, J.W., Jr., Broad, L.M., Braun, F.J., Lievremont, J.P., and Bird, G.S., Mechanisms of Capacitative Calcium Entry,J. Cell Sci.,2001, vol. 114, pp. 2223-2229.
Rosado, J.A. and Sage, S.O., The Actin Cytoskeleton in Store-Mediated Calcium Entry,J. Physiol.,2000, vol. 526, pp.221-229.
Harria, B.Z. and Lim, W.A., Mechanisms and Role of PDZ Domains in Signaling Complex Assembly,J. Cell Sci., 2001, vol. 114, pp.3219-3231.
Stoerkhul, K.F., Hovemann, B.H., and Carison, J.R., Olfactory Adaptation Depends on the Trp Ca2+ Channel in Drosophila,J. Neurosci.,1999, vol. 19, pp. 4839-4846.
Vaccaro, P., Branetti, B., Montecchi-Palazzi, L., Philipp, S., Citterich, M.H., Cesarini, G., and Dente, L., Distinct Binding Specificity of the Multiple PDZ Domains of INADL, a Human Protein with Homology to INAD from D. melanogaster,J. Biol. Chem., 2001, vol.276, pp. 42 122-42 130.
Savvateeva, E.V., Kamyshev, N.G., and Rosenblyum, S.R., Isolation of Temperature-Sensitive Mutations that Impair Metabolism of Cyclic-3'5'-Adenosine Monophosphate in D. melanogaster,Dokl. Akad. Nauk SSSR, 1978, vol.240, pp. 1443-1445.
Savvateeva, E.V. and Kamyshev, N.G., Effects of Temperature-Sensitive Mutations That Impair Metabolism of Cyclic-3'5'-Adenosine Monophosphate on Locomotor Activity and Learning in D. melanogaster,Dokl. Akad. Nauk SSSR,1978, vol. 243, pp.1564-1567.
Savvateeva, E.V. and Korochkin, L.I., Adenylate Cyclase in ts-Mutants of D. melanogaster,Isozyme Bull., 1982, vol.15, p.21.
Savvateeva, E.V., Lobazova, I.V., and Korochkin, L.I., A Study of Phosphodiesterase of Cyclic-3'5'-Adenosine Monophosphate in Temperature-Sensitive D. melanogaster Mutants,Dokl. Akad. Nauk SSSR,1981, vol.258, pp.748-753.
Savvateeva, E.V. and Korochkin, L.I.,A Study of the cAMP Level Regulation i D. melanogaster,Dokl. Akad. Nauk SSSR,1981. vol. 260, pp.481-484.
Savvateeva, E.V., Peresleni, I.V., and Korochkin, L.I., Ontogenetic Variability in Activities of Adenylyl Cyclase and Phosphodiesterase in Temperature-Sensitive Drosophila Mutants with Impaired cAMP Metabolism, Dokl. Akad. Nauk SSSR,1985, vol. 281, pp.439.
Savvateeva, E.V., Peresleni, I.V., and Korochkin, L.I., Cyclic AMP and Motor Activity in Drosophila,Dokl. Akad. Nauk SSSR,1985, vol. 281, pp.966-970.
Savvateeva, E.V., Peresleni, I.V., and Korochkin, L.I., Temperature-Sensitive Drosophila Mutants with Changed cAMP Phosphodiesterase Activity: Is a Gene for Calmodulin Found?,Dokl. Akad. Nauk SSSR, 1985, vol. 281, pp. 1233-1237.
Savvateeva, E.V., Peresleni, I.V., Ivanushina, V., and Korochkin, L.I., Expression of Adenylate Cyclase and Phosphodiesterase in Development of Temperature-Sensitive Mutants with Impaired Metabolism of cAMP in D. melanogaster,Develop. Genet., 1985, vol.5, pp. 159-172.
Savvateeva, E.V., Korochkina, S.E., Peresleni, I.V., and Kamyshev, N.G., Map Expansion around ts-Mutations in Genes Controlling cAMP Metabolism in D. melanogaster,Dros. Inform. Serv.,1985, vol.61, pp.144-146.
Savvateeva, E.V., Genetic Control of Second Messenger Systems and Their Role in Learning,Usp. Sovr. Genet.,1991, vol. 17, pp.33-99.
Korochkina, S.E., Savvateeva, E.V., Klimenko, V.V., and Ponomarenko, V.V., Spontaneous and Temperature-Induced Recombination in Drosophila Strains with Impaired cAMP Metabolism,Dokl. Akad. Nauk SSSR,1985, vol.285, pp. 1454-1458.
Korochkina, S.E. and Savvateeva, E.V., A Study of Interstrain Gonad Transplantations in D. melanogaster Females,Ontogenez,1985, vol.5, pp. 521-523.
Sharagina, L.M., Savvateeva, E.V., and Atamanenko, A.A., A Study of Cyclic Nucleotide Phosphodiesterase Activity in Mutant Strains of D. melanogaster, Genetika,1997, vol.33, pp.784-787.
Peresleni, A.I., Savvateeva, E.V., Peresleni, I.V., and Sharagina, L.M., Mutational Analysis and Genetic Cloning of the agnostic Locus Which Regulates Learning Ability in Drosophila,Neurosci. Behav. Physiol., 1997, vol.27, pp. 258-263.
Antoni, F.A., Molecular Diversity of Cyclic AMP Signalling, Front. Neuroendocrinol.,2000, vol.21, pp.103-132.
Davis, R.L. and Kiger, J.A.,A Partial Characteriza731 tion of the Cyclic Nucleotide Phosphodiesterases of Drosophila melanogaster,Arch. Biochem. Biophys., 1980, vol.203, pp.412-421.
Davis, R.L. and Kauvar, L.M., Drosophila Cyclic Nucleotide Phosphodiesterases,Adv. Cyclic Nucleot. Protein Phosphoryl. Res.,1984, vol. 16, pp.393-402.
Jackson, S.M. and Berg, C.A., Soma-to-Germline Interactions during Drosophila Oogenesis Are Influenced by Dose-Sensitive Interactions between Cut and the Genes cappuccino, ovarian tumor and agnostic, Genetics,1999, vol. 153, pp.289-303.
Yamakura, T., Bertaccini, E., Trudell, J.R., and Harris, R.A., Anesthetics and Ion Channels: Molecular Models and Sites of Action,Ann. Rev. Pharmacol. Toxicol., 2001, vol.41, pp. 23-51.
Mascia, M.P., Trudell, J.R., and Harris, R.A., Specific Binding Sites for Alcohols and Anesthetics on Ligand-Gated Ion Channels,Proc. Natl Acad. Sci. USA,2000, vol. 97, pp.9305-9310.
Leibovitch, B.A., Campbell, D.B., Krishnan, K.S., and Nash, H.A., Mutations that Affect Ion Channels Change the Sensitivity of Drosophila melanogaster to Volatile Anesthetics,J. Neurogenet.,1995, vol. 10, pp. 1-13.
van Swinderen, B., Saifee, O., Shebester, L., Robertson, R., Nonet, M.L., and Crowsder, M.C., A Neomorphic Syntaxin Mutation Blocks Volatile.Anesthetic Action in Caenorhabditis elegans,Proc. Natl Acad. Sci. USA,1999, vol.96, pp.2479-2484.
Park, S.K., Sedore, S.A., Cronmiller, C., and Hirsh, J., Type II cAMP-Dependent Protein Kinase-Deficient Drosophila Are Viable, but Show Developmental, Circadian, and Drug Response Phenotypes,J. Biol. Chem.,2000, vol.275, pp.20 588-20 596.
Kaech, S., Brinkhaus, H., and Matus, A., Volatile Anesthetics Block Actin-Based Motility in Dendritic Spines,Proc. Natl Acad. Sci. USA,1999, vol.96, pp. 10 433-10 437.
Mattson, M.P., LaFerla, F.M., Chan, S.L., Leissring, M.A., Shepel, P.N., and Geiger, J.D.,Calcium Signaling in the ER: Its Role in Neuronal Plasticity and Neurodegenerative Disorders,Trends Neurosci., 2000, vol.23, pp.222-229.
Tokmacheva, E.V., A Study of Mitotic Activity in Larval Neuronal Ganglion Cells in Drosophila ts-Mutants with Changed Learning Ability and Increased Activation Potency of Calmodulin,Zh. Vyssh. Nervn. Deyat., 1995, vol.45, pp.565-571.
Strauss, R. and Heisenberg, M., A Higher Control Center of Locomotor Behavior in the Drosophila Brain,J. Neurosci.,1993, vol. 13, pp.1852-1861.
Kamyshev, N.G., Iliadi, K.G., and Bragina, Yu.V., Drosophila Conditioned Courtship: Two Ways of Testing Memory,Learn. Mem.,1999, vol.6, pp. 1-20.
Kamyshev, N.G., Iliadi, K.G., Bragina, Yu.V., Savvateeva-Popova, E.V., Tokmacheva, E.V., and Prea, T., Detection of Drosophila Mutants with Defective Memory in Conditioned Courtship Suppression,Sechenov Fiziol. Zh.,1999, vol.85, pp.84-92.
Popov, A.V., Savvateeva-Popova, E.V., and Kamyshev, N.G., Peculiarities of Acoustic Communication in Fruit Flies Drosophila melanogaster,Sensor. Sist., 2000, vol.14, pp. 60-74.
Peixoto, A.A. and Hall, J.C., Analysis of Temperature-Sensitive Mutants Reveals New Genes Involved in the Courtship Song of Drosophila,Genetics,1998, vol.148, pp. 827-838.
Dellinger, B., Felling, R., and Ordway, R.W., Genetic Modifiers of the Drosophila NSF Mutant, Comatose, Include a Temperature-Sensitive Paralytic Allele of the Calcium Channel {alpha}1-Subunit Gene,cacophony, Genetics,2000, vol. 155, pp. 203-211.
Smith, L.A., Peixoto, A.A., Kramer, E.M., Villella, A., and Hall, J.C., Courtship and Visual Defects of cacophony Mutants Reveal Functional Complexity of a Calcium-Channel {alpha}1 Subunit in Drosophila, Genetics,1998, vol. 149, pp.1407-1426.
Zhimulev, I.F., Semeshin, V.F., Kulichkov, V.A., and Belyaeva, E.S., Intercalary Heterochromatin in Drosophila. Localisation and General Characteristics, Chromosoma,1982, vol.87, pp.197-228.
Medvedeva, A.V. and Savvateeva, E.V., The Effects of the agnostic Gene ts-Mutations That Control Calmodulin Functions and Learning Ability on Ectopic Pairing of Drosophila Polytene Chromosomes,Dokl. Akad. Nauk SSSR,1991, vol. 318, pp.733-736.
Medvedeva, A.V. and Savvateeva, E.V., Temperature Effects on Spatial Organization of Polytene Chromosomes in Drosophila Mutants with Changed Calmodulin Functions,Dokl. Akad. Nauk SSSR,1991, vol.318, pp.988-991.
Zhimulev, I.F., Polytene Chromosomes, Heterochromatin, and Position Effect Variegation,Adv. Genet., 1998, vol. 37, pp. 1-566.
Leach, T.J., Chotkowski, H.L., Wotring, M.G., Dilwith R.L., and Glaser, R.L., Replication of Heterochromatin and Structure of Polytene Chromosomes, Mol. Cell Biol.,2000, vol. 20, pp. 6308-6316.
Asztalos, Z., von Wegerer, J., Wustmann, G., Dombradi, V., Gausz, J., Spatz, H.C., and Friedrich, P., Protein Phosphatase 1-Deficient Mutant Drosophila Is Affected in Habituation and Associative Learning, J. Neurosci.,1993, vol. 13, pp. 924-930.
Belyaeva, E.S., Zhimulev, I.F., Volkova, E.I., Alekseenko, A.A., Moshkin, Y.M., and Koryakov, D.E., Su(UR)ES: A Gene Suppressing DNA Underreplication in Intercalary and Pericentric Heterochromatin of Drosophila melanogaster Polytene Chromosomes, Proc. Natl Acad. Sci. USA,1998, vol.95, pp. 7532-7537.
Kafatos, F.C., Loitus, C., Savakis, C., Glover, D., Ashburner, M., Link, A.J., Siden-Kiamos, I., and Saunders, R., Integrated Maps of the Drosophila Genome: Progress and Prospects,Trends Genet.,1991, vol.7, pp. 155-161.
Lozovskaya, E.R., Petrov, D.A., and Hartl, D.L., A Combined Molecular and Cytogenetic Approach to Genome Evolution in Drosophila Using Large-Fragment DNA Cloning,Chromosoma,1993, vol. 102, pp. 253-256.
Lenhoff, H.M., Wang, P.P., Greenberg, F., and Bellugi, U., Williams Syndrome and the Brain, Sci. Amer., 1997, vol. 277, pp.68-73.
Donnai, D. and Karmiloff-Smith, A., Williams Syndrome: From Genotype through to the Cognitive Phenotype, Am. J. Med. Genet.,2000, vol.97, pp.64-71.
Okano, I., Hiraoka, J., Otera H., Nunoue, K., Ohashi, K., Iwashita, S., Hirai, M, and Mizuno, K., Identification and Characterization of a Novel Family of Serine/Threonine Kinases Containing Two N-Terminal LIM Motifs, J. Biol. Chem., 1995, vol. 270, pp. 31 321-31 330.
Ohashi, K., Hosoya, T., Takahashi, K., Hing, H., and Mizuno, K., et al., Drosophila Homolog of LIM-Kinase Phosphorylates Cofilin and Induces Actin Cytoskeletal Reorganization,Biochem. Biophys. Res. Commun., 2000, vol. 276, pp. 1178-1185.
Wang, J.Y., Wigston, D.J., Rees, H.D., Levey, A.I., and Falls, D.L., LIM Kinase 1 Accumulates in Presynaptic Terminals during Synapse Maturation,J. Comp. Neurol., 2000, vol. 416, pp.319-334.
Takahashi, H., Koshimizu, U., and Nakamura, T., A Novel Transcript Encoding Truncated LIM Kinase 2 Is Specifically Expressed in Male Germ Cells Undergoing Meiosis,Biochem. Biophys. Res. Commun.,1998, vol. 249, pp. 138-145.
Erickson, J.W. and Cline, T.W., Key Aspects of the Primary Sex Determination Mechanism Are Conserved across the Genus Drosophila,Development, 1998, vol.125, pp.3259-3268.
Li, C., Geng, C., Leung, H.T., Hong, Y.S., Strong, L.L., Schneuwly, S., and Pak, W.L., INAF, A Protein Required for Transient Receptor Potential Ca(2+) Channel Function,Proc. Natl Acad. Sci. USA,1999, vol. 96, pp. 13 474-13 479.
Hall, J.C., Pleiotropy of Behavioral Genes,Flexibility and Constraint in Behavioral Systems, Greenspan, R.J. and Kyriacou, C.P., Eds., Chichester: John Wiley & Sons,1994, pp. 15-27.
Shaikh, T.H., Kurahashi, H., and Emanuel, B.S., Evolutionarily Conserved Low Copy Repeats (LCRs) in 22q11 Mediate Deletions, Duplications, Translocations, and Genomic Instability: An Update and Literature Review,Genet. Med.,2001, vol. 3, pp. 6-13.
Korenberg, J.R., Chen, X., Hirota, N., Lai, Z., Bellugi, U., Burian, D., Roe, B., and Matsuoka, R., Genome Structure and Cognitive Map of Williams Syndrome, Cogn. Neurosci., 2000, vol.12, pp. S89-S107.
Peoples, R., Franke, Y., Wang, Y.K., Perez-Yurado, L., Paperna, T., Cisco, M., and Francke, U., A Physical Map, Including a BAC/PAC Clone Contig, of the Williams.Beuren Syndrome.Deletion Region at 7q11.23,Am. J. Hum. Genet., 2000, vol.66, pp. 47-68.
Osborne, L.R., Li, M., Pober, B., Chitayat, D., Bodurtha, J., Mandel, A., Costa, T., Grebe, T., Cox, S., Tsui, L.C., and Scherer, S.W., A 1.5 Million-Base Pair Inversion Polymorphism in Families with Williams. Beuren Syndrome,Nat. Genet., 2001, vol. 29, pp. 321.
Xamena, N., Creus, A., and Macros, R., Effect of Intercalating Mutagens on Crossing-Over in D. melanogaster Females,Experientia,1985, vol. 41, pp. 1078-1081.
Kosikov, K.V., A New Duplication in the X-Chromosome of D. melanogaster and Its Evolutionary Significance, Dokl. Akad. Nauk SSSR,1936, vol.3, pp. 297.
Montell, C., Birnbaumer, L., and Flockerzi, V., The TRP Channels, A Remarkably Functional Family, Cell,2002, vol. 108, pp. 595-598.
Zhang, Z., Tang, J., Tikunova, S., Johnson, J.D., Chen, Z., Qin, N., Dietrich, A., Stefani, E., Birnbaumer, L., and Zhu, M.X., Activation of Trp3 by Inositol 1,4,5-Trisphosphate Receptors through Displacement of Inhibitory Calmodulin from a Common Binding Domain,Proc. Natl Acad. Sci. USA,2001, vol.98, pp. 3168-3173.
Saimi, Y. and Kung, C., Calmodulin as an Ion Channel Subunit,Ann. Rev. Physiol., 2002, vol. 64, pp.289.
Krupp, J., Vissel, B., Thomas, C.G., Heinemann, S.F., and Westbrook, G.L., Interactions of Calmodulin and Alpha-Actinin with the NR1 Subunit Modulate Ca2+-Dependent Inactivation of NMDA Receptors,J. Neurosci., 1999, vol.19, pp. 1165-1178.
Bezprozvanny, I. and Maximov, A., PDZ Domains: More Than Just a Glue,Proc. Natl Acad. Sci. USA, 2001, vol. 98, pp. 787-789.
Edwards, D.C. and Gill, G.N., Structural Features of LIM Kinase That Control Effects on the Actin Cytoskeleton, J. Biol. Chem.,1999, vol. 274, pp.11 352-11 361.
Sumi, T., Matsumoto, K., Takai, Y., and Nakamura, T., Cofilin Phosphorylation and Actin Cytoskeletal Dynamics Regulated by Rho and Cdc42-Activated LIM-Kinase 2,J. Cell Biol.1999, vol. 147, pp. 1519-1532.
Toshima, J., Toshima, J.Y., Amano, T., Yang, N., Narumiya, S., and Mizuno, K., Cofilin Phosphorylation by Protein Kinase Testicular Protein Kinase 1 and Its Role in Integrin-Mediated Actin Reorganization and Focal Adhesion Formation,Mol. Biol. Cell.,2001, vol. 12, pp. 1131-1145.
Connolly, J.B. and Tully, T., Integrins: A Role for Adhesion Molecules in Olfactory Memory,Curr. Biol., 1998, vol.8, pp.R386-R389.
http://flybase.bio.indiana.edu
Osborne, L.R., Soder, S., Shi, X.M., Rober, B., Costa, T., Scherer, S.W., and Tsui, L.C., Hemizygous Deletion of the Syntaxin 1A Gene in Individuals with Williams Syndrome,Am. J. Hum. Genet.,1997, vol.61, pp.449-452.
Sumi, T., Matsumoto, K., and Nakamura, T., Mitosis-Dependent Phosphorylation and Activation of LIM-Kinase 1,Biochem. Biophys. Res. Commun., 2002, vol. 290, pp. 1315-1320.
Brown, K., Nuclear Structure, Gene Expression and Development,Crit. Rev. Eukaryot. Gene Expr.,1999, vol. 9, pp. 203-212.
Rando, O.J., Zhao, K., and Crabtree, G.R., Searching for a Function of Nuclear Actin,Trends Cell Biol., 2000, vol. 10, pp. 92-97.
Osborne, L.R., Campbell, T., Daradich, A., Scherer, S.W., and Tsui, L.C., Identification of a Putative Transcription Factor Gene (WBSCR11) That Is Commonly Deleted in Williams.Beuren Syndrome,Genomics, 1999, Apr. 15; vol. 57, no. 2, pp. 279-284.
Lawler, S., The LIM Kinase Connection,Current Biol.,1999, vol. 9, pp. R800-R802.
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Savvateeva-Popova, E.V., Peresleny, A.I., Scharagina, L.M. et al. Complex Study of Drosophila Mutants in the agnostic Locus: A Model for Coupling Chromosomal Architecture and Cognitive Functions. Journal of Evolutionary Biochemistry and Physiology 38, 706–733 (2002). https://doi.org/10.1023/A:1023003625014
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DOI: https://doi.org/10.1023/A:1023003625014