Human PDE4A8, a novel brain-expressed PDE4 cAMP-specific phosphodiesterase that has undergone rapid evolutionary change

Biochemical Journal

Volumn 411, Issue 2, 2008, Pages 361-369

  Mackenzie, Kirsty F ^a   Topping, Emma C ^a   Bugaj Gaweda, Bozena ^b   Deng, Chengjun ^b   Cheung, York Fong ^a   Olsen, Aileen E ^c   Stockard, Cecil R ^d   High Mitchell, Lisa ^e   Baillie, George S ^a   Grizzle, William E ^d,f   De Vivo, Michael ^b   Houslay, Miles D ^a   Wang, Daguang ^b   Bolger, Graeme B ^c,e,f  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b Memory Pharmaceuticals Corporation   (United States)

^c UNIVERSITY OF UTAH HEALTH SCIENCES CENTER   (United States)

^d University of Alabama at Birmingham   (United States)

^e University of Alabama at Birmingham   (United States)

^f UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Alternative mRNA splicing; cAMP; Cilomilast; Phosphodiesterase 4 isoform A (PDE4A); Phosphoric diester hydrolyase; Rolipram

Indexed keywords

ALTERNATIVE MRNA SPLICING; CILOMILAST; PHOSPHODIESTERASE 4 ISOFORM A (PDE4A); PHOSPHORIC DIESTER HYDROLYASE;

ENZYME INHIBITION; GENE EXPRESSION; MAMMALS; RNA;

BRAIN;

CILOMILAST; PHOSPHODIESTERASE IV; PHOSPHODIESTERASE IV A8; ROLIPRAM; UNCLASSIFIED DRUG; COMPLEMENTARY DNA; CYCLIC AMP DEPENDENT PROTEIN KINASE; MESSENGER RNA; NUCLEOTIDE; PDE4A PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL LYSATE; CONTROLLED STUDY; DNA ISOLATION; DRUG INHIBITION; GENE SEQUENCE; GENETIC ANALYSIS; GENOME; HUMAN; HUMAN CELL; IC 50; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA SPLICING; SKELETAL MUSCLE; AMINO ACID SEQUENCE; ANIMAL; ANTIBODY SPECIFICITY; BRAIN; CELL STRAIN COS1; CERCOPITHECUS; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; RAT; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; TIME;

MAMMALIA; RATTUS;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BRAIN; CERCOPITHECUS AETHIOPS; COS CELLS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 4; DNA, COMPLEMENTARY; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENOME, HUMAN; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEOTIDES; ORGAN SPECIFICITY; PHOSPHORYLATION; RATS; RNA, MESSENGER; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; TIME FACTORS;

EID: 42449099614     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20071251     Document Type: Article

References (50)

1. Beavo, J. A. and Brunton, L. L. (2002) Cyclic nucleotide research: still expanding after half a century. Nat. Rev. Mol. Cell Biol. 3, 710-718
2. Conti, M., Richter, W., Mehats, C., Livera, G., Park, J. Y. and Jin, C. (2003) Cyclic AMP-specific PDE4 phosphodiesterases as critical components of cyclic AMP signaling. J. Biol.Chem. 278, 5493-5496
3. Houslay, M. D. and Adams, D. R. (2003) PDE4 cAMP phosphodiesterases: modular enzymes that orchestrate signalling cross-talk, desensitization and compartmentalization. Biochem. J. 370, 1-18
4. Bolger, G. B., Conti, M. and Houslay, M. D. (2007) in Cyclic Nucleotide Phosphodiesterases in Health and Disease (Beavo, J.A., Francis, S.H, and Houslay, M.D., eds), pp. 99-129, Taylor and Francis, Boca Raton
5. Houslay, M. D., Sullivan, M. and Bolger, G. B. (1998) The multienzyme PDE4 cyclic adenosine monophosphate-specific phosphodiesterase family: intracellular targeting, regulation, and selective inhibition by compounds exerting anti-inflammatory and antidepressant actions. Adv. Pharmacol. 44, 225-342
6. Torphy, T. J. and Page, C. (2000) Phosphodiesterases: the journey towards therapeutics. Trends Pharmacol. Sci. 21, 157-159
7. Bach, M. E., Barad, M., Son, H., Zhuo, M., Lu, Y. F., Shih, R., Mansuy, I., Hawkins, R. D. and Kandel, E. R. (1999) Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 96, 5280-5285
8. Barad, M., Bourtchouladze, R., Winder, D. G., Golan, H. and Kandel, E. (1998) Rolipram, a type IV-specific phosphodiesterase inhibitor, facilitates the establishment of long-lasting long-term potentiation and improves memory. Proc. Natl. Acad. Sci. U.S.A. 95, 15020-15025
9. Zhang, H. T., Huang, Y., Jin, S. L., Frith, S. A., Suvarna, N., Conti, M. and O'Donnell, J. M. (2002) Antidepressant-like profile and reduced sensitivity to rolipram in mice deficient in the PDE4D phosphodiesterase enzyme. Neuropsychopharmacology 27, 587-595
10. Bolger, G., Michaeli, T., Martins, T., St. John, T., Steiner, B., Rodgers, L., Riggs, M., Wigler, M. and Ferguson, K. (1993) 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. 13, 6558-6571
11. Beard, M. B., Olsen, A. E., Jones, R. E., Erdogan, S., Houslay, M. D. and Bolger, G. B. (2000) UCR1 and UCR2 domains unique to the cAMP-specific phosphodiesterase family form a discrete module via electrostatic interactions. J. Biol. Chem. 275, 10349-10358
12. Bolger, G. B., Rodgers, L. and Riggs, M. (1994) Differential CNS expression of alternative mRNA isoforms of the mammalian genes encoding cAMP-specific phosphodiesterases. Gene 149, 237-244
13. Bolger, G. B., McPhee, I. and Houslay, M. D. (1996) Alternative splicing of cAMP-specific phosphodiesterase mRNA transcripts: characterization of a novel tissue-specific isoform, RNPDE4A8. J. Biol. Chem. 271, 1065-1071
14. Rena, G., Begg, F., Ross, A., MacKenzie, C., McPhee, I., Campbell, L., Huston, E., Sullivan, M. and Houslay, M. D. (2001) Molecular cloning, genomic positioning, promoter identification, and characterization of the novel cyclic AMP-specific phosphodiesterase PDE4A10. Mol. Pharmacol. 59, 996-1011
15. Wallace, D. A., Johnston, L. A., Huston, E., MacMaster, D., Houslay, T. M., Cheung, Y. F., Campbell, L., Milien, J. E., Smith, R. A., Gall, I. et al. (2005) Identification and characterization of PDE4A11, a novel, widely expressed long isoform encoded by the human PDE4A cAMP phosphodiesterase gene. Mol. Pharmacol. 67, 1920-1934
16. McPhee, I., Cochran, S. and Houslay, M. D. (2001) The novel long PDE4A10 cyclic AMP phosphodiesterase shows a pattern of expression within brain that is distinct from the long PDE4A5 and short PDE4A1 isoforms. Cell. Signalling 13, 911-918
17. Sullivan, M., Rena, G., Begg, F., Gordon, L., Olsen, A. S. and Houslay, M. D. (1998) Identification and characterization of the human homologue of the short PDE4A cAMP-specific phosphodiesterase RD1 (PDE4A1) by analysis of the human HSPDE4A gene locus located at chromosome 19p13.2. Biochem. J. 333, 693-703
18. Davis, R. L., Takayasu, H., Eberwine, M. and Myres, J. (1989) Cloning and characterization of mammalian homologs of the Drosophila dunce + gene. Proc. Natl. Acad. Sci. U.S.A. 86, 3604-3608
19. Shakur, Y., Pryde, J. G. and Houslay, M. D. (1993) Engineered deletion of the unique N-terminal domain of the cyclic AMP-specific phosphodiesterase RD1 prevents plasma membrane association and the attainment of enhanced thermostability without altering its sensitivity to inhibition by rolipram. Biochem. J. 292, 677-686
20. Shakur, Y., Wilson, M., Pooley, L., Lobban, M., Griffiths, S. L., Campbell, A. M., Beattie, J., Daly, C. and Houslay, M. D. (1995) Identification and characterization of the type-IVA cyclic AMP-specific phosphodiesterase RD1 as a membrane-bound protein expressed in cerebellum. Biochem. J. 306, 801-809
21. 2+. J. Cell Sci. 119, 3799-3810
22. Sambrook, J. and Russell, D. W. (2001) Molecular Cloning: a Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor
23. Gluzman, Y. (1981) SV40-transformed simian cells support the replication of early SV40 mutants. Cell 23, 175-182
24. Huston, E., Pooley, L., Julien, P., Scotland, G., McPhee, I., Sullivan, M., Bolger, G. and Houslay, M. (1996) The human cyclic AMP-specific phosphodiesterase PDE-46 (HSPDE4A4B) expressed in transfected COS7 cells occurs as both particulate and cytosolic species which exhibit distinct kinetics of inhibition by the anti-depressant rolipram. J. Biol. Chem. 271, 31334-31344
25. Bolger, G. B., Erdogan, S., Jones, R. E., Loughney, K., Scotland, G., Hoffmann, R., Wilkinson, I., Farrell, C. and Houslay, M. D. (1997) Characterization of five different proteins produced by alternatively spliced mRNAs from the human cAMP-specific phosphodiesterase PDE4D gene. Biochem. J. 328, 539-548
26. McPhee, I., Pooley, L., Lobban, M., Bolger, G. and Houslay, M. D. (1995) Identification, characterization and regional distribution in brain of RPDE-6 (RNPDE4A5), a novel splice variant of the PDE4A cyclic AMP phosphodiesterase family. Biochem. J. 310, 965-974
27. MacKenzie, S. J., Baillie, G. S., McPhee, I., MacKenzie, C., Seamons, R., McSorley, T., Millen, J., Beard, M. B., Van Heeke, G. and Houslay, M. D. (2002) Long PDE4 cAMP specific phosphodiesterases are activated by protein kinase A-mediated phosphorylation of a single serine residue in upstream conserved region 1 (UCR1). Br. J. Pharmacol. 136, 421-433
28. Kreis, T. E. (1986) Microinjected antibodies against the cytoplasmic domain of vesicular stomatitis virus glycoprotein block its transport to the cell surface. EMBO J. 5, 931-941
29. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
30. Marchmont, R. J. and Houslay, M. D. (1980) A peripheral and an intrinsic enzyme constitute the cyclic AMP phosphodiesterase activity of rat liver plasma membranes. Biochem. J. 187, 381-392
31. Beavo, J. A. (1995) Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms. Physiol. Rev. 75, 725-748
32. Olsen, A. E. and Bolger, G. B. (2000) Physical mapping and promoter structure of the murine cAMP-specific phosphodiesterase pde4a gene. Mamm. Genome 11, 41-45
33. McPhee, I., Yarwood, S. J., Scotland, G., Huston, E., Beard, M. B., Ross, A. H., Houslay, E. S. and Houslay, M. D. (1999) Association with the SRC family tyrosyl kinase LYN triggers a conformational change in the catalytic region of human cAMP-specific phosphodiesterase HSPDE4A4B: consequences for rolipram inhibition. J. Biol. Chem. 274, 11796-11810
34. Barnette, M. S., Christensen, S. B., Essayan, D. M., Grous, M., Prabhakar, U., Rush, J. A., Kagey, S. A. and Torphy, T. J. (1998) SB 207499 (Ariflo), a potent and selective second-generation phosphodiesterase 4 inhibitor: in vitro anti-inflammatory actions. J. Pharmacol. Exp. Ther. 284, 420-426
35. Torphy, T. J., Bamette, M. S., Underwood, D. C., Griswold, D. E., Christensen, S. B., Murdoch, R. D., Nieman, R. B. and Compton, C. H. (1999) Ariflo™ (SB 207499), a second generation phosphodiesterase 4 inhibitor for the treatment of asthma and COPD: from concept to clinic. Pulm. Pharmacol. Ther. 12, 131-135
36. Giembycz, M. A. (2001) Cilomilast: a second generation phosphodiesterase 4 inhibitor for asthma and chronic obstructive pulmonary disease. Expert Opin. Invest. Drugs 10, 1361-1379
37. Houslay, M. D. (2001) PDE4 cAMP-specific phosphodiesterases. Prog. Nucleic Acid Res. Mol. Biol. 69, 249-315
38. Richter, W. and Conti, M. (2004) The oligomerization tate determines regulatory properties and inhibitor sensitivity of type 4 cAMP-specific phosphodiesterases. J. Biol. Chem. 279, 30338-30348
39. Rocque, W. J., Tian, G., Wiseman, J. S., Holmes, W. D., Zajac, T. I., Willard, D. H., Patel, I. R., Wisely, G. B., Clay, W. C., Kadwell, S. H. et al. (1997) Human recombinant phosphodiesterase 4B2B binds (R)-rolipram at a single site with two affinities. Biochemistry 36, 14250-14261
40. Bolger, G. B. (2007) Phosphodiesterase isotorms: an annotated list. In Cyclic Nucleotide Phosphodiesterases in Health and Disease (Beavo, J. A., Francis, S. H. and Houslay, M. D., eds), pp. 19-31, CRC Press, Boca Raton
41. Cheung, Y. F., Kan, Z., Garrett-Engele, P., Gall, I., Murdoch, H., Baillie, G. S., Camargo, L. M., Johnson, J. M., Houslay, M. D. and Castle, J. C. (2007) PDE4B5, a novel, super-short, brain-specific cAMP phosphodiesterase-4 variant whose isotorm-specilying N-terminal region is identical to that of cAMP phosphodiesterase-4D6 (PDE4D6). J. Pharmacol. Exp. Ther. 322, 600-609
42. Qiu, Y. H., Chen, C. N., Malone, T., Richter, L., Beckendorf, S. K. and Davis, R. L. (1991) Characterization of the memory gene dunce of Drosophila melanogaster. J. Mol. Biol. 222, 553-565
43. Shepherd, M., McSorley, T., Olsen, A. E., Johnston, L. A., Thomson, N. C., Baillie, G. S., Houslay, M. D. and Bolger, G. B. (2003) Molecular cloning and subcellular distribution of the novel PDE4B4 cAMP-specific phosphodiesterase isoform. Biochem. J. 370, 429-438
44. Farooqui, S. M., Al Bagdadi, F., Houslay, M. D., Bolger, G. B., Stout, R., Specian, R. D., Cherry, J. A., Conti, M. and O'Donnell, J. M. (2001) Surgically induced cryptorchidism-related degenerative changes in spermatogonia are associated with loss of cyclic adenosine monophosphate-dependent phosphodiesterases type 4 in abdominal testes of rats. Biol. Reprod. 64, 1583-1589
45. Cherry, J. A. and Davis, R. L. (1999) Cyclic AMP phosphodiesterases are localized in regions ot the mouse brain associated with reinforcement, movement, and affect. J. Comp. Neurol. 407, 287-301
46. Michaeli, T., Bloom, T. J., Martins, T., Loughney, K., Ferguson, K., Riggs, M., Rodgers, L., Beavo, J. A. and Wigler, M. (1993) Isolation and characterization of a previously undetected human cAMP phosphodiesterase by complementation of cAMP phosphodiesterase-deficient Saccharomyces cerevisiae. J. Biol. Chem. 268, 12925-12932
47. D'Sa, C., Eisch, A. J., Bolger, G. B. and Duman, R. S. (2005) Differential expression and regulation of the cAMP-selective phosphodiesterase type 4A splice variants in rat brain by chronic antidepressant administration. Eur. J. Neurosci. 22, 1463-1475
48. Sullivan, M., Olsen, A. S. and Houslay, M. D. (1999) Genomic organisation of the human cyclic AMP-specific phosphodiesterase PDE4C gene and its chromosomal localisation to 19p13.1, between RAB3A and JUND. Cell. Signalling 11, 735-742
49. Gretarsdottir, S., Thorleifsson, G., Reynisdottir, S. T., Manolescu, A., Jonsdottir, S., Jonsdottir, T., Gudmundsdottir, T., Bjarnadottir, S. M., Einarsson, O. B., Gudjonsdottir, H. M. et al. (2003) The gene encoding phosphodiesterase 4D confers risk of ischemic stroke. Nat. Genet. 35, 131-138
50. Johnston, L. A., Erdogan, S., Cheung, Y. F., Sullivan, M., Barber, R., Lynch, M. J., Baillie, G. S., Van Heeke, G., Adams, D. R., Huston, E. and Houslay, M. D. (2004) Expression, intracellular distribution and basis for lack of catalytic activity of the PDE4A7 isoform encoded by the human PDE4A cAMP-specific phosphodiesterase gene. Biochem. J. 380, 371-384