Functional characterization of transmembrane adenylyl cyclases from the honeybee brain

Insect Biochemistry and Molecular Biology

Volumn 42, Issue 6, 2012, Pages 435-445

  Balfanz, Sabine ^a   Ehling, Petra ^b   Wachten, Sebastian ^c   Jordan, Nadine ^a   Erber, Joachim ^d   Mujagic, Samir ^e   Baumann, Arnd ^a  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^e BIELEFELD UNIVERSITY   (Germany)

Author keywords

Behavior; Cellular signaling; GPCR; Learning and memory; Second messenger

Indexed keywords

ADENYLATE CYCLASE; INSECT PROTEIN;

ANIMAL; ARTICLE; BEE; BRAIN; CHEMICAL STRUCTURE; ENZYMOLOGY; GENETICS; METABOLISM; MULTIGENE FAMILY; SEQUENCE HOMOLOGY;

ADENYLATE CYCLASE; ANIMALS; BEES; BRAIN; INSECT PROTEINS; MOLECULAR STRUCTURE; MULTIGENE FAMILY; SEQUENCE HOMOLOGY, NUCLEIC ACID;

ANIMALIA; APIS MELLIFERA; BASIDIOMYCOTA; BRASSICA NAPUS VAR. NAPOBRASSICA; VERTEBRATA;

EID: 84860239515     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2012.02.005     Document Type: Article

References (58)

1. 2+ release in Drosophila melanogaster. J. Neurochem. 2005, 93:440-451.
2. Cann M.J., Chung E., Levin L.R. A new family of adenylyl cyclase genes in the male germline of Drosophila melanogaster. Dev. Genes Evol. 2000, 210:200-206.
3. Cann M.J., Levin L.R. Restricted expression of a truncated adenylyl cyclase in the cephalic furrow of Drosophila melanogaster. Dev. Genes Evol. 2000, 210:34-40.
4. Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 1987, 7:2745-2752.
5. Chen Y., Cann M.J., Litvin T.N., Iourgenko V., Sinclair M.L., Levin L.R., Buck J. Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 2000, 289:625-628.
6. Cooper D.M.F. Compartmentalization of adenylate cyclase and cAMP signaling. Biochem. Soc. Trans. 2005, 33:1319-1322.
7. Cooper D.M.F., Crossthwaite A.J. Higher-order organization and regulation of adenylyl cyclases. Trends Pharmacol. Sci. 2006, 27:426-431.
8. Davis R.L. Traces of Drosophila memory. Neuron 2011, 70:8-19.
9. Diel S., Beyermann M., Navarro Llorens J.M., Wittig B., Kleuss C. Two interaction sites on mammalian adenylyl cyclase type I and II: modulation by calmodulin and Gβγ. Biochem. J. 2008, 411:449-456.
10. Diel S., Klass K., Wittig B., Kleuss C. Gβγ activation site in adenylyl cyclase type II. J. Biol. Chem. 2006, 281:288-294.
11. Eisenhardt, D., Galizia, G., Giurfa, M., 2011. Honeybee neurobiology and behavior: a tribute to Randolf Menzel. Springer Science & Business Media B.V., Dordrecht.
12. Erber J., Masuhr T., Menzel R. Localization of short-term memory in the brain of the bee, Apis mellifera. Physiol. Entomol. 1980, 5:343-358.
13. Fiala A., Müller U., Menzel R. Reversible downregulation of protein kinase A during olfactory learning using antisense technique impairs long-term memory formation in the honeybee, Apis mellifera. J. Neurosci. 1999, 19:10125-10134.
14. Fuss N., Mujagic S., Erber J., Wachten S., Baumann A. Biochemical properties of heterologously expressed and native adenylyl cyclases from the honeybee brain (Apis mellifera L.). Insect Biochem. Mol. Biol. 2010, 40:573-580.
15. Gervasi N., Tchénio P., Preat T. PKA dynamics in a Drosophila learning center: coincidence detection by rutabaga adenylyl cyclase and spatial regulation by dunce phosphodiesterase. Neuron 2010, 65:516-529.
16. Gross K.L., Lu N.Z., Cidlowski J.A. Molecular mechanisms regulating glucocorticoid sensitivity and resistance. Mol. Cell. Endocrinol. 2009, 300:7-16.
17. Hacker B.M., Tomlinson J.E., Wayman G.A., Sultana R., Chan G., Villacres E., Disteche C., Storm D.R. Cloning, chromosomal mapping, and regulatory properties of the human type 9 adenylyl cyclase (ADCY9). Genomics 1998, 50:97-104.
18. Han K.A., Millar N.S., Davis R.L. A novel octopamine receptor with preferential expression in Drosophila mushroom bodies. J. Neurosci. 1998, 18:3650-3658.
19. Han K.A., Millar N.S., Grotewiel M.S., Davis R.L. DAMB, a novel dopamine receptor expressed specifically in Drosophila mushroom bodies. Neuron 1996, 16:1127-1135.
20. Han P.-L., Levin L.R., Reed R.R., Davis R.L. Preferential expression of the Drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects. Neuron 1992, 9:619-627.
21. Hanoune J., Defer N. Regulation and role of adenylyl cyclase isoforms. Annu. Rev. Pharmacol. Toxicol. 2001, 41:145-174.
22. Heisenberg M. Mushroom body memoir: from maps to models. Nat. Rev. Neurosci. 2003, 4:266-275.
23. Herlitze S., Koenen M. A general and rapid mutagenesis method using polymerase chain reaction. Gene 1990, 91:143-147.
24. 2+ signaling by an octopamine receptor from Drosophila melanogaster. FASEB J. 2011, 25:2484-2491.
25. Iourgenko V., Kliot B., Cann M.J., Levin L.R. Cloning and characterization of a Drosophila adenylyl cyclase homologous to mammalian type IX. FEBS Lett. 1997, 413:104-108.
26. Iourgenko V., Levin L.R. A calcium-inhibited Drosophila adenylyl cyclase. Biochim. Biophys. Acta 2000, 1495:125-139.
27. Kamenetsky M., Middelhaufe S., Bank E.M., Levin L.R., Buck J., Steegborn C. Molecular details of cAMP generation in mammalian cells: a tale of two systems. J. Mol. Biol. 2006, 362:623-639.
28. Kaupp U.B., Seifert R. Cyclic nucleotide-gated ion channels. Physiol. Rev. 2002, 82:769-824.
29. Kozak M. Compilation and analysis of sequences upstream from the translational start site in eukatyotic mRNAs. Nucleic Acids Res. 1984, 12:857-872.
30. Landschulz W.H., Johnson P.F., McKnight S.L. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science 1988, 240:1759-1764.
31. 2+/Calmodulin-responsive adenylyl cyclase. Cell 1992, 68:479-489.
32. Linder J.U. Class III adenylyl cyclases: molecular mechanisms of catalysis and regulation. Cell. Mol. Life Sci. 2006, 63:1736-1751.
33. Livingstone M.S., Sziber P.P., Quinn W.G. Loss of calcium/Calmodulin responsiveness in adenylyl cyclase of rutabaga, a Drosophila learning mutant. Cell 1984, 37:205-215.
34. Ludwig J., Margalit T., Eismann E., Lancet D., Kaupp U.B. Primary structure of cAMP-gated channel from bovine olfactory epithelium. FEBS Lett. 1990, 270:24-29.
35. Mao Z., Roman G., Zong L., Davis R.L. Pharmacogenetic rescue in time and space of the rutabaga memory impairment by using Gene-Switch. Proc. Natl. Acad. Sci. USA 2004, 101:198-203.
36. Menzel R. Searching for the memory trace in a mini-brain, the honeybee. Learn. Mem. 2001, 8:53-62.
37. Menzel R., Leboulle G., Eisenhardt D. Small brains, smart minds. Cell 2006, 124:237-239.
38. Pagano M., Clynes M.A., Masada N., Ciruela A., Ayling L.-J., Wachten S., Cooper D.M.F. Insight into the residence in lipid rafts of adenylyl cyclase AC8 and its regulation by capacitive calcium entry. Am. J. Physiol. Cell. Physiol. 2009, 296:C607-C619.
39. Patel T.B., Du Z., Pierre S., Cartin L., Scholich K. Molecular biological approaches to unravel adenylyl cyclase signaling and function. Gene 2001, 269:13-25.
40. Pidoux G., Tasken K. Specificity and spatial dynamics of protein kinase A signaling organized by A-kinase-anchoring proteins. J. Mol. Endocrinol. 2010, 44:271-284.
41. Poels J., Vanden Broeck J. Insect basic leucine zipper proteins and their role in cyclic AMP-dependent regulation of gene expression. Int. Rev. Cytol. 2004, 241:277-309.
42. Sadana R., Dessauer C.W. Physiological roles of G protein-regulated adenylyl cyclase isoforms: insights from knockout and overexpression studies. Neurosignals 2009, 17:5-22.
43. Sambrook J., Russell D.W. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. third ed.
44. Sanabra C., Mengod G. Neuroanatomical distribution and neurochemical characterization of cells expressing adenylyl cyclase isoforms in mouse and rat brain. J. Chem. Anat. 2011, 41:43-54.
45. Scheiner R., Baumann A., Blenau W. Aminergic control and modulation of honeybee behavior. Curr. Neuropharmacol. 2006, 4:259-276.
46. Scheiner R., Müller U., Heimburger S., Erber J. Activity of protein kinase A and gustatory responsiveness in the honey bee (Apis mellifera L.). J. Comp. Physiol. 2003, 189:427-434.
47. Seebacher T., Linder J.U., Schultz J.E. An isoform-specific interaction of the membrane anchors affects mammalian adenylyl cyclase type V activity. Eur. J. Biochem. 2001, 268:105-110.
48. Sunahara R.K., Taussig R. Isoforms of mammalian adenylyl cyclase: multiplicities of signalling. Mol. Interv. 2002, 2:168-184.
49. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
50. Tang W.J., Krupinski J., Gilman A.G. Expression and characterization of calmodulin-activated (type I) adenylyl cyclase. J. Biol. Chem. 1991, 266:8595-8603.
51. γS. Science 1997, 278:1907-1916.
52. Tomchik S.M., Davis R.L. Dynamics of learning-related cAMP signaling and stimulus integration in the Drosophila olfactory pathway. Neuron 2009, 64:510-521.
53. Wachten S., Schlenstedt J., Gauss R., Baumann A. Molecular identification and functional characterization of an adenylyl cyclase from the honeybee. J. Neurochem. 2006, 96:1580-1590.
54. Wahl-Schott C., Biel M. HCN-channels: structure, cellular regulation and physiological function. Cell. Mol. Life Sci. 2008, 66:470-494.
55. 2+ regulation of adenylyl cyclases in cAMP microdomains. Physiol. Rev. 2007, 87:965-1010.
56. 2+ microdomains associated with different isoforms of adenylyl cyclase. J. Cell Sci. 2010, 123:107-117.
57. Zars T., Wolf R., Davis R., Heisenberg M. Tissue-specific expression of a type I adenylyl cyclase rescues the rutabaga mutant memory defect: in search of the engram. Learn. Mem. 2000, 7:18-31.
58. Zhang G., Liu Y., Ruoho A.E., Hurley J.H. Structure of the adenylyl cyclase catalytic core. Nature 1997, 386:247-253.