Protein kinase A type i activates a CRE-element more efficiently than protein kinase A type II regardless of C subunit isoform

BMC Biochemistry

Volumn 12, Issue 1, 2011, Pages

  Stakkestad, Oystein ^a,b   Larsen, Anja Cv ^a   Kvissel, Anne Katrine ^a   Eikvar, Sissel ^a   Ørstavik, Sigurd ^a,c   Skålhegg, Bjørn S ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

^c ULLEVÅL UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE 1; CYCLIC AMP DEPENDENT PROTEIN KINASE 2; CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT IALPHA; CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT IIALPHA; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ISOPROTEIN; LUCIFERASE;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; REPORTER GENE; CELL STRAIN HEK293; COMPARATIVE STUDY; DNA RESPONSIVE ELEMENT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROTEIN BINDING;

EUKARYOTA;

CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASE TYPE I; CYCLIC AMP-DEPENDENT PROTEIN KINASE TYPE II; GENE EXPRESSION REGULATION; GENES, REPORTER; HEK293 CELLS; HUMANS; LUCIFERASES; PROTEIN BINDING; PROTEIN ISOFORMS; RESPONSE ELEMENTS;

EID: 79551682944     PISSN: None     EISSN: 14712091     Source Type: Journal    
DOI: 10.1186/1471-2091-12-7     Document Type: Article

References (67)

1. Adenosine 3',5'-monophosphate in biological materials. II. The measurement of adenosine 3',5'-monophosphate in tissues and the role of the cyclic nucleotide in the lipolytic response of fat to epinephrine. RW Butcher RJ Ho HC Meng EW Sutherland, J Biol Chem 1965 240 4515 4523 4378937
2. An adenosine 3',5'-monophosphate-dependant protein kinase from rabbit skeletal muscle. DA Walsh JP Perkins EG Krebs, J Biol Chem 1968 243 3763 3765 4298072
3. Evidence that rabbit muscle protein kinase has two kinetically distinct binding sites for adenosine 3'; 5'-cyclic monophosphate. SO Doskeland, Biochem Biophys Res Commun 1978 83 542 549 10.1016/0006-291X(78)91024-0 212058 (Pubitemid 8391859)
4. The distribution and dissociation of cyclic adenosine 3':5'-monophosphate-dependent protein kinases in adipose, cardiac, and other tissues. JD Corbin SL Keely CR Park, J Biol Chem 1975 250 218 225 166986
5. Separation of regulatory and catalytic subunits of the cyclic 3',5'-adenosine monophosphate-dependent protein kinase(s) of rabbit skeletal muscle. EM Reimann CO Brostrom JD Corbin CA King EG Krebs, Biochem Biophys Res Commun 1971 42 187 194 10.1016/0006-291X(71)90086-6 4322813
6. In vivo phosphorylation of a synthetic peptide substrate of cyclic AMP-dependent protein kinase. JL Maller BE Kemp EG Krebs, Proc Natl Acad Sci USA 1978 75 248 251 10.1073/pnas.75.1.248 203933 (Pubitemid 8290776)
7. Binding of a nuclear protein to the cyclic-AMP response element of the somatostatin gene. MR Montminy LM Bilezikjian, Nature 1987 328 175 178 10.1038/328175a0 2885756 (Pubitemid 17108220)
8. Phosphorylation-induced binding and transcriptional efficacy of nuclear factor CREB. KK Yamamoto GA Gonzalez WH Biggs MR Montminy, Nature 1988 334 494 498 10.1038/334494a0 2900470
9. Specificity in the cAMP/PKA signaling pathway. Differential expression, regulation, and subcellular localization of subunits of PKA. BS Skalhegg K Tasken, Front Biosci 2000 5 678 D693 10.2741/Skalhegg 10922298
10. The human gene for the regulatory subunit RI alpha of cyclic adenosine 3', 5'-monophosphate-dependent protein kinase: two distinct promoters provide differential regulation of alternately spliced messenger ribonucleic acids. R Solberg M Sandberg V Natarajan PA Torjesen V Hansson T Jahnsen K Tasken, Endocrinology 1997 138 169 181 10.1210/en.138.1.169 8977401 (Pubitemid 27009421)
11. Alternative 5'-exons of the mouse cAMP-dependent protein kinase subunit RIalpha gene are conserved and expressed in both a ubiquitous and tissue-restricted fashion. S Barradeau T Imaizumi-Scherrer MC Weiss DM Faust, FEBS Lett 2000 476 272 276 10.1016/S0014-5793(00)01653-7 10913627 (Pubitemid 30410831)
12. Cyclic AMP regulates expression of the RI alpha subunit of cAMP-dependent protein kinase through an alternatively spliced 5' UTR. MK Dahle HK Knutsen KA Tasken R Pilz K Tasken, Eur J Biochem 2001 268 5920 5929 10.1046/j.0014-2956. 2001.02542.x 11722580 (Pubitemid 33079328)
13. A winged helix forkhead (FOXD2) tunes sensitivity to cAMP in T lymphocytes through regulation of cAMP-dependent protein kinase RIalpha. CC Johansson MK Dahle SR Blomqvist LM Gronning EM Aandahl S Enerback K Tasken, J Biol Chem 2003 278 17573 17579 10.1074/jbc.M300311200 12621056 (Pubitemid 36799646)
14. Human testis cDNA for the regulatory subunit RII alpha of cAMP-dependent protein kinase encodes an alternate amino-terminal region. O Oyen F Myklebust JD Scott V Hansson T Jahnsen, FEBS Lett 1989 246 57 64 10.1016/0014-5793(89)80253- 4 2540040 (Pubitemid 19087771)
15. Induction of Cbeta splice variants and formation of novel forms of protein kinase A type II holoenzymes during retinoic acid-induced differentiation of human NT2 cells. AK Kvissel S Orstavik P Oistad T Rootwelt T Jahnsen BS Skalhegg, Cell Signal 2004 16 577 587 10.1016/j.cellsig.2003.08.014 14751543 (Pubitemid 38125144)
16. Identification of novel splice variants of the human catalytic subunit Cbeta of cAMP-dependent protein kinase. S Orstavik N Reinton E Frengen BT Langeland T Jahnsen BS Skalhegg, Eur J Biochem 2001 268 5066 5073 10.1046/j.0014-2956.2001.02429.x 11589697 (Pubitemid 32955557)
17. A novel isoform of human cyclic 3',5'-adenosine monophosphate-dependent protein kinase, c alpha-s, localizes to sperm midpiece. N Reinton S Orstavik TB Haugen T Jahnsen K Tasken BS Skalhegg, Biol Reprod 2000 63 607 611 10.1095/biolreprod63.2.607 10906071 (Pubitemid 30639953)
18. Cloning of cDNA for the catalytic subunit of cAMP-dependent protein kinase. MO Showers RA Maurer, Methods Enzymol 1988 159 311 318 3412179
19. Isolation of cDNA clones coding for the catalytic subunit of mouse cAMP-dependent protein kinase. MD Uhler DF Carmichael DC Lee JC Chrivia EG Krebs GS McKnight, Proc Natl Acad Sci USA 1986 83 1300 1304 10.1073/pnas.83.5.1300 3456589 (Pubitemid 16016116)
20. Isoform C beta 2, an unusual form of the bovine catalytic subunit of cAMP-dependent protein kinase. S Wiemann V Kinzel W Pyerin, J Biol Chem 1991 266 5140 5146 2002051 (Pubitemid 21909470)
21. Expression of a nonmyristylated variant of the catalytic subunit of protein kinase A during male germ-cell development. JL Desseyn KA Burton GS McKnight, Proc Natl Acad Sci USA 2000 97 6433 6438 10.1073/pnas.97.12.6433 10841548 (Pubitemid 30412731)
22. Two novel brain-specific splice variants of the murine Cbeta gene of cAMP-dependent protein kinase. CR Guthrie BS Skalhegg GS McKnight, J Biol Chem 1997 272 29560 29565 10.1074/jbc.272.47.29560 9368018
23. n-Tetradecanoyl is the NH2-terminal blocking group of the catalytic subunit of cyclic AMP-dependent protein kinase from bovine cardiac muscle. SA Carr K Biemann S Shoji DC Parmelee K Titani, Proc Natl Acad Sci USA 1982 79 6128 6131 10.1073/pnas.79.20.6128 6959104 (Pubitemid 13219818)
24. A conserved deamidation site at Asn 2 in the catalytic subunit of mammalian cAMP-dependent protein kinase detected by capillary LC-MS and tandem mass spectrometry. PT Jedrzejewski A Girod A Tholey N Konig S Thullner V Kinzel D Bossemeyer, Protein Sci 1998 7 457 469 10.1002/pro.5560070227 9521123 (Pubitemid 28092868)
25. Expression of the catalytic subunit of cAMP-dependent protein kinase in Escherichia coli: multiple isozymes reflect different phosphorylation states. FW Herberg SM Bell SS Taylor, Protein Eng 1993 6 771 777 10.1093/protein/6.7.771 8248101 (Pubitemid 23293207)
26. Autophosphorylation of the catalytic subunit of cAMP-dependent protein kinase. J Toner-Webb SM van Patten DA Walsh SS Taylor, J Biol Chem 1992 267 25174 25180 1460017
27. Identification of phosphorylation sites in the recombinant catalytic subunit of cAMP-dependent protein kinase. W Yonemoto SM Garrod SM Bell SS Taylor, J Biol Chem 1993 268 18626 18632 8395513 (Pubitemid 23273801)
28. The catalytic subunit of the cAMP-dependent protein kinase of ovine sperm flagella has a unique amino-terminal sequence. JT San Agustin JD Leszyk LM Nuwaysir GB Witman, J Biol Chem 1998 273 24874 24883 10.1074/jbc.273.38.24874 9733793 (Pubitemid 28454994)
29. Identification, cloning and characterization of a novel 47 kDa murine PKA C subunit homologous to human and bovine Cbeta2. A Funderud HH Henanger TT Hafte PS Amieux S Orstavik BS Skalhegg, BMC Biochem 2006 7 20 10.1186/1471-2091-7-20 16889664
30. Identification and characterization of novel PKA holoenzymes in human T lymphocytes. S Orstavik A Funderud TT Hafte S Eikvar T Jahnsen BS Skalhegg, FEBS J 2005 272 1559 1567 10.1111/j.1742-4658.2005.04568.x 15794744 (Pubitemid 40516207)
31. Protein kinases in human renal cell carcinoma and renal cortex. A comparison of isozyme distribution and of responsiveness to adenosine 3':5'-cyclic monophosphate. TM Fossberg SO Doskeland PM Ueland, Arch Biochem Biophys 1978 189 272 281 10.1016/0003-9861(78)90224-2 213022
32. A safety study of a mixed-backbone oligonucleotide (GEM231) targeting the type I regulatory subunit alpha of protein kinase A using a continuous infusion schedule in patients with refractory solid tumors. S Goel K Desai A Bulgaru A Fields G Goldberg S Agrawal R Martin M Grindel S Mani, Clin Cancer Res 2003 9 4069 4076 14519628 (Pubitemid 37204022)
33. Protein kinase A (PK-A) regulatory subunit expression in colorectal cancer and related mucosa. AW Bradbury DC Carter WR Miller YS Cho-Chung T Clair, Br J Cancer 1994 69 738 742 10.1038/bjc.1994.139 8142263 (Pubitemid 24112697)
34. Increased expression of the RIalpha subunit of the cAMP-dependent protein kinase A is associated with advanced stage ovarian cancer. HM McDaid MT Cairns RJ Atkinson S McAleer DP Harkin P Gilmore PG Johnston, Br J Cancer 1999 79 933 939 10.1038/sj.bjc.6690149 10070893 (Pubitemid 29082129)
35. The essential role of RI alpha in the maintenance of regulated PKA activity. PS Amieux GS McKnight, Ann N Y Acad Sci 2002 968 75 95 10.1111/j.1749-6632.2002.tb04328.x 12119269 (Pubitemid 34721873)
36. A mouse model for the Carney complex tumor syndrome develops neoplasia in cyclic AMP-responsive tissues. LS Kirschner DF Kusewitt L Matyakhina WH Towns JA Carney H Westphal CA Stratakis, Cancer Res 2005 65 4506 4514 10.1158/0008-5472.CAN-05-0580 15930266 (Pubitemid 40740784)
37. Mouse models of altered protein kinase A signaling. LS Kirschner Z Yin GN Jones E Mahoney, Endocr Relat Cancer 2009 16 773 793 10.1677/ERC-09-0068 19470615
38. Phosphorylation of a cyclic adenosine 3':5'-monophosphate-dependent protein kinase from bovine cardiac muscle. J Erlichman R Rosenfeld OM Rosen, J Biol Chem 1974 249 5000 5003 4367815
39. PKA type IIalpha holoenzyme reveals a combinatorial strategy for isoform diversity. J Wu SH Brown DS von SS Taylor, Science 2007 318 274 279 10.1126/science.1146447 17932298 (Pubitemid 47574855)
40. A-kinase anchoring proteins take shape. DL Beene JD Scott, Curr Opin Cell Biol 2007 19 192 198 10.1016/j.ceb.2007.02.011 17317140 (Pubitemid 46394601)
41. Localized effects of cAMP mediated by distinct routes of protein kinase A. K Tasken EM Aandahl, Physiol Rev 2004 84 137 167 10.1152/physrev.00021.2003 14715913 (Pubitemid 38049878)
42. Phosphorylation of the cAMP-dependent protein kinase (PKA) regulatory subunit modulates PKA-AKAP interaction, substrate phosphorylation, and calcium signaling in cardiac cells. S Manni JH Mauban CW Ward M Bond, J Biol Chem 2008 283 24145 24154 10.1074/jbc.M802278200 18550536
43. Rapid protein kinase assay using phosphocellulose-paper absorption. JJ Witt R Roskoski Jr, Anal Biochem 1975 66 253 258 10.1016/0003-2697(75)90743-5 1147218
44. Role of multiple basic residues in determining the substrate specificity of cyclic AMP-dependent protein kinase. BE Kemp DJ Graves E Benjamini EG Krebs, J Biol Chem 1977 252 4888 4894 194899 (Pubitemid 8162200)
45. Regulation of transcription by cyclic AMP-dependent protein kinase. PL Mellon CH Clegg LA Correll GS McKnight, Proc Natl Acad Sci USA 1989 86 4887 4891 10.1073/pnas.86.13.4887 2544878 (Pubitemid 19182204)
46. Limited proteolysis of the catalytic subunit of cAMP-dependent protein kinase - a membranal regulatory device? E Alhanaty S Shaltiel, Biochem Biophys Res Commun 1979 89 323 332 10.1016/0006-291X(79)90633-8 226083
47. Isozymes of cyclic AMP-dependent protein kinases (PKA) in human lymphoid cell lines: levels of endogenous cAMP influence levels of PKA subunits and growth in lymphoid cell lines. BS Skalhegg AK Johansen FO Levy KB Andersson EM Aandahl HK Blomhoff V Hansson K Tasken, J Cell Physiol 1998 177 85 93 10.1002/(SICI)1097-4652(199810)177:1<85::AID-JCP9>3.0.CO;2-A 9731748 (Pubitemid 28421524)
48. Movement of the free catalytic subunit of cAMP-dependent protein kinase into and out of the nucleus can be explained by diffusion. AT Harootunian SR Adams W Wen JL Meinkoth SS Taylor RY Tsien, Mol Biol Cell 1993 4 993 1002 8298196 (Pubitemid 23331539)
49. Derivatives of 1-beta-D-ribofuranosylbenzimidazole 3',5'-phosphate that mimic the actions of adenosine 3',5'-phosphate (cAMP) and guanosine 3',5'-phosphate (cGMP). HG Genieser E Winkler E Butt M Zorn S Schulz F Iwitzki R Stormann B Jastorff SO Doskeland D Ogreid,, et al. Carbohydr Res 1992 234 217 235 10.1016/0008-6215(92)85050-A 1334800
50. Involvement of the catalytic subunit of protein kinase A and of HA95 in pre-mRNA splicing. AK Kvissel S Orstavik S Eikvar G Brede T Jahnsen P Collas G Akusjarvi BS Skalhegg, Exp Cell Res 2007 313 2795 2809 10.1016/j.yexcr.2007.05. 014 17594903 (Pubitemid 47126439)
51. Formation of inactive cAMP-saturated holoenzyme of cAMP-dependent protein kinase under physiological conditions. R Kopperud AE Christensen E Kjarland K Viste H Kleivdal SO Doskeland, J Biol Chem 2002 277 13443 13448 10.1074/jbc.M109869200 11834733 (Pubitemid 34967939)
52. Substrate enhances the sensitivity of type I protein kinase a to cAMP. K Viste RK Kopperud AE Christensen SO Doskeland, J Biol Chem 2005 280 13279 13284 10.1074/jbc.M413065200 15691833 (Pubitemid 40517212)
53. Protein kinase A type I and type II define distinct intracellular signaling compartments. BG Di A Zoccarato V Lissandron A Terrin X Li MD Houslay GS Baillie M Zaccolo, Circ Res 2008 103 836 844 10.1161/CIRCRESAHA.108.174813 18757829
54. Regulation of cAMP-dependent protein kinase subunit expression in CATH.a and SH-SY5Y cells. VA Boundy J Chen EJ Nestler, J Pharmacol Exp Ther 1998 286 1058 1065 9694969 (Pubitemid 29003504)
55. Holoenzymes of cAMP-dependent protein kinase containing the neural form of type I regulatory subunit have an increased sensitivity to cyclic nucleotides. GG Cadd MD Uhler GS McKnight, J Biol Chem 1990 265 19502 19506 2174040 (Pubitemid 120013892)
56. Importance of the A-helix of the catalytic subunit of cAMP-dependent protein kinase for stability and for orienting subdomains at the cleft interface. FW Herberg B Zimmermann M McGlone SS Taylor, Protein Sci 1997 6 569 579 10.1002/pro.5560060306 9070439 (Pubitemid 27120053)
57. A-kinase-interacting protein localizes protein kinase A in the nucleus. M Sastri DM Barraclough PT Carmichael SS Taylor, Proc Natl Acad Sci USA 2005 102 349 354 10.1073/pnas.0408608102 15630084 (Pubitemid 40116770)
58. Phosphotransferase and substrate binding mechanism of the cAMP-dependent protein kinase catalytic subunit from porcine heart as deduced from the 2.0 A structure of the complex with Mn2+ adenylyl imidodiphosphate and inhibitor peptide PKI(5-24). D Bossemeyer RA Engh V Kinzel H Ponstingl R Huber, EMBO J 1993 12 849 859 8384554 (Pubitemid 23095833)
59. Crystal structures of the myristylated catalytic subunit of cAMP-dependent protein kinase reveal open and closed conformations. J Zheng DR Knighton NH Xuong SS Taylor JM Sowadski LF Ten Eyck, Protein Sci 1993 2 1559 1573 10.1002/pro.5560021003 8251932 (Pubitemid 23294335)
60. Mobilization of the A-kinase N-myristate through an isoform-specific intermolecular switch. M Gangal T Clifford J Deich X Cheng SS Taylor DA Johnson, Proc Natl Acad Sci USA 1999 96 12394 12399 10.1073/pnas.96.22.12394 10535933 (Pubitemid 29513513)
61. Intracellular distribution of mammalian protein kinase A catalytic subunit altered by conserved Asn2 deamidation. R Pepperkok A Hotz-Wagenblatt N Konig A Girod D Bossemeyer V Kinzel, J Cell Biol 2000 148 715 726 10.1083/jcb.148.4.715 10684253
62. Binding of hisactophilin I and II to lipid membranes is controlled by a pH-dependent myristoyl-histidine switch. F Hanakam G Gerisch S Lotz T Alt A Seelig, Biochemistry 1996 35 11036 11044 10.1021/bi960789j 8780505 (Pubitemid 26301166)
63. Myristoylated and non-myristoylated forms of the pH sensor protein hisactophilin II: intracellular shuttling to plasma membrane and nucleus monitored in real time by a fusion with green fluorescent protein. F Hanakam R Albrecht C Eckerskorn M Matzner G Gerisch, EMBO J 1996 15 2935 2943 8670794
64. The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. S McLaughlin A Aderem, Trends Biochem Sci 1995 20 272 276 10.1016/S0968-0004(00)89042-8 7667880
65. Cyclic AMP-dependent protein kinase type I mediates the inhibitory effects of 3',5'-cyclic adenosine monophosphate on cell replication in human T lymphocytes. BS Skalhegg BF Landmark SO Doskeland V Hansson T Lea T Jahnsen, J Biol Chem 1992 267 15707 15714 1379235
66. Inactive forms of the catalytic subunit of protein kinase A are expressed in the brain of higher primates. ACV Larsen AK Kvissel TT Hafte CIA Avellan S Eikvar T Rootwelt S Orstavik BS Skalhegg, Febs Journal 2008 275 250 262 10.1111/j.1742-4658.2007.06195.x 18070107
67. Involvement of the catalytic subunit of protein kinase A and of HA95 in pre-mRNA splicing. AK Kvissel S Orstavik S Eikvar G Brede T Jahnsen P Collas G Akusjarvi BS Skalhegg, Exp Cell Res 2007 313 2795 2809 10.1016/j.yexcr.2007.05. 014 17594903 (Pubitemid 47126439)