Molecular Cloning of DNA Encoding a Calmodulin-dependent Phosphodiesterase Enriched in Striatum

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1992 Nov 15

PMID 1332068

Citations 17

Authors

J W Polli

R L Kincaid

Affiliations

Soon will be listed here.

Abstract

A murine cDNA for the 63-kDa calmodulin-dependent phosphodiesterase (CaM-PDE), PDE1B-1, was isolated by using polymerase chain reaction with degenerate primers followed by the cloning of a full-length cDNA from a whole-brain phage library. The nucleotide sequence of 2986 base pairs contains an open reading frame encoding a protein of 535 amino acids (M(r) = 61,231) with a predicted isoelectric point of 5.54. The deduced protein sequence shows approximately 60% identity with that of the 61-kDa isoform (PDE1A2), consistent with the proposal that these proteins arise from two separate genes [Novack, J. P., Charbonneau, H., Bentley, J. K., Walsh, K. A. & Beavo, J. A. (1991) Biochemistry 30, 7940-7947]. Southern blot analysis suggests high nucleotide-sequence conservation of the PDE1B1 gene among mammalian and avian species. A single approximately 3600-nucleotide mRNA transcript was seen in all brain regions, with striatum containing 4- to 30-fold higher levels than other areas. In nonneural tissues, low amounts of PDE1B1 mRNA were detected in lung, spleen, thymus, and testis; hybridization to several larger mRNA species was also seen in thymus and testis. By using nucleic acid probes for PDE1B1, the mechanisms that control its highly selective gene expression can now be studied at the molecular level.

Citing Articles

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References

SANGER F, Nicklen S, Coulson A . DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977; 74(12):5463-7. PMC: 431765. DOI: 10.1073/pnas.74.12.5463. View

Hansen R, Beavo J . Purification of two calcium/calmodulin-dependent forms of cyclic nucleotide phosphodiesterase by using conformation-specific monoclonal antibody chromatography. Proc Natl Acad Sci U S A. 1982; 79(9):2788-92. PMC: 346291. DOI: 10.1073/pnas.79.9.2788. View

Charbonneau H, Kumar S, Novack J, Blumenthal D, Griffin P, Shabanowitz J . Evidence for domain organization within the 61-kDa calmodulin-dependent cyclic nucleotide phosphodiesterase from bovine brain. Biochemistry. 1991; 30(32):7931-40. DOI: 10.1021/bi00246a009. View

Novack J, Charbonneau H, Bentley J, Walsh K, Beavo J . Sequence comparison of the 63-, 61-, and 59-kDa calmodulin-dependent cyclic nucleotide phosphodiesterases. Biochemistry. 1991; 30(32):7940-7. DOI: 10.1021/bi00246a010. View

Ludvig N, Burmeister V, Jobe P, Kincaid R . Electron microscopic immunocytochemical evidence that the calmodulin-dependent cyclic nucleotide phosphodiesterase is localized predominantly at postsynaptic sites in the rat brain. Neuroscience. 1991; 44(2):491-500. DOI: 10.1016/0306-4522(91)90072-v. View

Thompson W . Cyclic nucleotide phosphodiesterases: pharmacology, biochemistry and function. Pharmacol Ther. 1991; 51(1):13-33. DOI: 10.1016/0163-7258(91)90039-o. View

Polli J, Kincaid R, TORRIS J, Billingsley M . Expression of calmodulin-dependent enzymes in developing rat striatum is not affected by perturbation of dopaminergic systems. Synapse. 1991; 9(2):136-43. DOI: 10.1002/syn.890090208. View

Nebert D, Nelson D, Coon M, Estabrook R, Feyereisen R, Fujii-Kuriyama Y . The P450 superfamily: update on new sequences, gene mapping, and recommended nomenclature. DNA Cell Biol. 1991; 10(1):1-14. DOI: 10.1089/dna.1991.10.1. View

Beavo J, Reifsnyder D . Primary sequence of cyclic nucleotide phosphodiesterase isozymes and the design of selective inhibitors. Trends Pharmacol Sci. 1990; 11(4):150-5. DOI: 10.1016/0165-6147(90)90066-H. View

10.

Hurwitz R, Hirsch K, Clark D, Holcombe V, Hurwitz M . Induction of a calcium/calmodulin-dependent phosphodiesterase during phytohemagglutinin-stimulated lymphocyte mitogenesis. J Biol Chem. 1990; 265(15):8901-7. View

11.

Kincaid R, Giri P, Higuchi S, Tamura J, Dixon S, Marietta C . Cloning and characterization of molecular isoforms of the catalytic subunit of calcineurin using nonisotopic methods. J Biol Chem. 1990; 265(19):11312-9. View

12.

Lipkin V, Khramtsov N, Vasilevskaya I, Atabekova N, Muradov K, Gubanov V . Beta-subunit of bovine rod photoreceptor cGMP phosphodiesterase. Comparison with the phosphodiesterase family. J Biol Chem. 1990; 265(22):12955-9. View

13.

Billingsley M, Polli J, Balaban C, Kincaid R . Developmental expression of calmodulin-dependent cyclic nucleotide phosphodiesterase in rat brain. Brain Res Dev Brain Res. 1990; 53(2):253-63. DOI: 10.1016/0165-3806(90)90015-q. View

14.

Davis R, Takayasu H, Eberwine M, Myres J . Cloning and characterization of mammalian homologs of the Drosophila dunce+ gene. Proc Natl Acad Sci U S A. 1989; 86(10):3604-8. PMC: 287186. DOI: 10.1073/pnas.86.10.3604. View

15.

Hashimoto Y, Sharma R, Soderling T . Regulation of Ca2+/calmodulin-dependent cyclic nucleotide phosphodiesterase by the autophosphorylated form of Ca2+/calmodulin-dependent protein kinase II. J Biol Chem. 1989; 264(18):10884-7. View

16.

Swinnen J, Joseph D, Conti M . Molecular cloning of rat homologues of the Drosophila melanogaster dunce cAMP phosphodiesterase: evidence for a family of genes. Proc Natl Acad Sci U S A. 1989; 86(14):5325-9. PMC: 297614. DOI: 10.1073/pnas.86.14.5325. View

17.

Balaban C, Billingsley M, Kincaid R . Evidence for transsynaptic regulation of calmodulin-dependent cyclic nucleotide phosphodiesterase in cerebellar Purkinje cells. J Neurosci. 1989; 9(7):2374-81. PMC: 6569749. View

18.

Epstein P, Moraski Jr S, Hachisu R . Identification and characterization of a Ca2+-calmodulin-sensitive cyclic nucleotide phosphodiesterase in a human lymphoblastoid cell line. Biochem J. 1987; 243(2):533-9. PMC: 1147887. DOI: 10.1042/bj2430533. View

19.

Kincaid R, Balaban C, Billingsley M . Regulated expression of calmodulin-dependent cyclic nucleotide phosphodiesterase in the central nervous system. J Cyclic Nucleotide Protein Phosphor Res. 1986; 11(7):473-86. View

20.

Rossi P, Giorgi M, Geremia R, Kincaid R . Testis-specific calmodulin-dependent phosphodiesterase. A distinct high affinity cAMP isoenzyme immunologically related to brain calmodulin-dependent cGMP phosphodiesterase. J Biol Chem. 1988; 263(30):15521-7. View