CAMP/PKA signaling balances respiratory activity with mitochondria dependent apoptosis via transcriptional regulation

BMC Cell Biology

Volumn 11, Issue , 2010, Pages

  Leadsham, Jane E ^a   Gourlay, Campbell W ^a  

^a UNIVERSITY OF KENT   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; FUNGAL RNA; PROTEIN HAP4; PROTEIN SCO1; PROTEIN SOK2; PROTEIN TPK3P; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; CCAAT BINDING FACTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE CATALYTIC SUBUNIT; HAP4 PROTEIN, S CEREVISIAE; MEMBRANE PROTEIN; MITOCHONDRIAL PROTEIN; REPRESSOR PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SCO1 PROTEIN, S CEREVISIAE; SOK2 PROTEIN, S CEREVISIAE; TPK3 PROTEIN, S CEREVISIAE;

APOPTOSIS; ARTICLE; BIOGENESIS; CELL STRUCTURE; FUNGAL STRAIN; FUNGUS GROWTH; GENE EXPRESSION; MICROARRAY ANALYSIS; MITOCHONDRIAL RESPIRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; RNA ISOLATION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ENZYME ACTIVE SITE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MITOCHONDRION;

EUKARYOTA; MAMMALIA; SACCHAROMYCETALES;

APOPTOSIS; CATALYTIC DOMAIN; CCAAT-BINDING FACTOR; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASE CATALYTIC SUBUNITS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GENE EXPRESSION REGULATION, FUNGAL; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; REACTIVE OXYGEN SPECIES; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 78649332389     PISSN: None     EISSN: 14712121     Source Type: Journal    
DOI: 10.1186/1471-2121-11-92     Document Type: Article

References (58)

1. Butow RA, Avadhani NG. Mitochondrial Signaling: The Retrograde Response. Molecular Cell 2004, 14(1):1-15. 10.1016/S1097-2765(04)00179-0, 15068799.
2. McBride HM, Neuspiel M, Wasiak S. Mitochondria: More Than Just a Powerhouse. Current Biology 2006, 16(14):R551-R560. 10.1016/j.cub.2006.06.054, 16860735.
3. Wang C, Youle RJ. The Role of Mitochondria in Apoptosis. Annual review of genetics 2009,
4. Passos JF, Simillion C, Hallinan J, Wipat A, von Zglinicki T. Cellular senescence: unravelling complexity. Age Dordrecht, Netherlands 2009,
5. Chan SL, Wei Z, Chigurupathi S, Tu W. Compromised respiratory adaptation and thermoregulation in aging and age-related diseases. Ageing research reviews 2009,
6. Turner N, Heilbronn LK. Is mitochondrial dysfunction a cause of insulin resistance?. Trends in endocrinology and metabolism: TEM 2008, 19(9):324-330. 10.1016/j.tem.2008.08.001, 18804383.
7. Gogvadze V, Orrenius S, Zhivotovsky B. Mitochondria as targets for chemotherapy. Apoptosis 2009, 14(4):624-640. 10.1007/s10495-009-0323-0, 19205885.
8. Mahad D, Lassmann H, Turnbull D. Review: Mitochondria and disease progression in multiple sclerosis. Neuropathology and applied neurobiology 2008, 34(6):577-589. 10.1111/j.1365-2990.2008.00987.x, 2981078, 19076696.
9. Gibson GE, Karuppagounder SS, Shi Q. Oxidant-induced changes in mitochondria and calcium dynamics in the pathophysiology of Alzheimer's disease. Annals of the New York Academy of Sciences 2008, 1147:221-232. 10.1196/annals.1427.038, 2744687, 19076444.
10. Henchcliffe C, Beal MF. Mitochondrial biology and oxidative stress in Parkinson disease pathogenesis. Nature clinical practice 2008, 4(11):600-609. 10.1038/ncpneuro0924, 18978800.
11. Boveris A, Navarro A. Brain mitochondrial dysfunction in aging. IUBMB life 2008, 60(5):308-314. 10.1002/iub.46, 18421773.
12. Ishii N. Role of oxidative stress from mitochondria on aging and cancer. Cornea 2007, 26(9 Suppl 1):S3-9. 10.1097/ICO.0b013e31812f6745, 17881913.
13. Orrenius S. Reactive oxygen species in mitochondria-mediated cell death. Drug metabolism reviews 2007, 39(2-3):443-455. 10.1080/03602530701468516, 17786631.
14. Hock MB, Kralli A. Transcriptional control of mitochondrial biogenesis and function. Annual review of physiology 2009, 71:177-203. 10.1146/annurev.physiol.010908.163119, 19575678.
15. Ohlmeier S, Kastaniotis AJ, Hiltunen JK, Bergmann U. The Yeast Mitochondrial Proteome, a Study of Fermentative and Respiratory Growth. J Biol Chem 2004, 279(6):3956-3979. 10.1074/jbc.M310160200, 14597615.
16. Hlavata L, Aguilaniu H, Pichova A, Nystrom T. The oncogenic RAS2val19 mutation locks respiration, independently of PKA, in a mode prone to generate ROS. The EMBO journal 2003, 22(13):3337-3345. 10.1093/emboj/cdg314, 165639, 12839995.
17. Hlavata L, Nachin L, Jezek P, Nystrom T. Elevated Ras/protein kinase A activity in Saccharomyces cerevisiae reduces proliferation rate and lifespan by two different reactive oxygen species-dependent routes. Aging cell 2008, 7(2):148-157. 10.1111/j.1474-9726.2007.00361.x, 18081742.
18. Reinders A, Burckert N, Boller T, Wiemken A, De Virgilio C. Saccharomyces cerevisiae cAMP-dependent protein kinase controls entry into stationary phase through the Rim15p protein kinase. Genes & development 1998, 12(18):2943-2955.
19. Toda T, Cameron S, Sass P, Zoller M, Scott J, McCullen B, Hurwitz M, Krebs E, Wigler M. Cloning and characterisation of BCY1, a locus encoding a regulatory subunit of the cyclic AMP-dependent protein kinase in Saccharomyces cerevisiae. Molecular and cellular biology 1987, 7:1371-1377. 365223, 3037314.
20. Toda T, Cameron S, Sass P, Zoller M, Wigler M. Three different genes in S. cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase. Cell 1987, 50:277-287. 10.1016/0092-8674(87)90223-6, 3036373.
21. Toda T, Uno I, Ishikawa T, Powers S, Kataoka T, Broek D, Cameron S, Broach J, Matsumoto K, Wigler M. In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell 1985, 40(1):27-36. 10.1016/0092-8674(85)90305-8, 2981630.
22. Robertson LS, Causton HC, Young RA, Fink GR. The yeast A kinases differentially regulate iron uptake and respiratory function. Proceedings of the National Academy of Sciences of the United States of America 2000, 97(11):5984-5988. 10.1073/pnas.100113397, 18545, 10811893.
23. Robertson LS, Fink GR. The three yeast A kinases have specific signaling functions in pseudohyphal growth. Proceedings of the National Academy of Sciences of the United States of America 1998, 95(23):13783-13787. 10.1073/pnas.95.23.13783, 24897, 9811878.
24. Akada R, Yamamoto J, Yamashita I. Screening and identification of yeast sequences that cause growth inhibition when overexpressed. Mol Gen Genet 1997, 254:267-274. 10.1007/s004380050415, 9150260.
25. Gerst JE, Ferguson K, Vojtek A, Wigler M, Field J. CAP is a bifunctional component of the Saccharomyces cerevisiae adenylyl cyclase complex. Molecular and cellular biology 1991, 11(3):1248-1257. 369396, 1996090.
26. Mintzer KA, Field J. Interactions between adenylyl cyclase, CAP and RAS from Saccharomyces cerevisiae. Cellular signalling 1994, 6(6):681-694. 10.1016/0898-6568(94)90050-7, 7531994.
27. Gourlay CW, Ayscough KR. Actin-Induced Hyperactivation of the Ras Signalling Pathway Leads to Apoptosis in Saccharomyces cerevisiae. Molecular and cellular biology 2006, 26(17):6487-6501. 10.1128/MCB.00117-06, 1592845, 16914733.
28. Gourlay CW, Carpp LN, Timpson P, Winder SJ, Ayscough KR. A role for the actin cytoskeleton in cell death and aging in yeast. J Cell Biol 2004, 164(6):803-809. 10.1083/jcb.200310148, 15024029.
29. Gourlay CW, Ayscough KR. Identification of an upstream regulatory pathway controlling actin-mediated apoptosis in yeast. J Cell Sci 2005, 118:2119-2132. 10.1242/jcs.02337, 15855235.
30. Leadsham JE, Miller K, Ayscough KR, Colombo S, Martegani E, Sudbery P, Gourlay CW. Whi2p links nutritional sensing to actin-dependent Ras-cAMP-PKA regulation and apoptosis in yeast. J Cell Sci 2009, 122:706-715. 10.1242/jcs.042424, 2720921, 19208759.
31. Chevtzoff C, Vallortigara J, Averet N, Rigoulet M, Devin A. The yeast cAMP protein kinase Tpk3p is involved in the regulation of mitochondrial enzymatic content during growth. Biochem Biophys Acta 2005, 1706:117-125. 10.1016/j.bbabio.2004.10.001, 15620372.
32. Gueldener U, Heinisch J, Koehler GJ, Voss D, Hegemann JH. A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic acids research 2002, 30(6):e23. 10.1093/nar/30.6.e23, 101367, 11884642.
33. Mazon MJ, Behrens MM, Morgado E, Portillo F. Low activity of the yeast cAMP-dependent protein kinase catalytic subunit Tpk3 is due to the poor expression of the TPK3 gene. European journal of biochemistry/FEBS 1993, 213(1):501-506. 10.1111/j.1432-1033.1993.tb17787.x, 8386630.
34. Lascaris R, Bussemaker HJ, Boorsma A, Piper M, van der Spek H, Grivell L, Blom J. Hap4p overexpression in glucose-grown Saccharomyces cerevisiae induces cells to enter a novel metabolic state. Genome biology 2003, 4(1):R3. 10.1186/gb-2002-4-1-r3, 151284, 12537548.
35. von der Haar T. Optimized protein extraction for quantitative proteomics of yeasts. PloS one 2007, 2(10):e1078. 10.1371/journal.pone.0001078, 2031916, 17957260.
36. Gourlay CW, Carpp LN, Timpson P, Winder SJ, Ayscough KR. A role for the actin cytoskeleton in cell death and aging in yeast. J Cell Biol 2004, 164(6):803-809. 10.1083/jcb.200310148, 2172293, 15024029.
37. Westermann B, Neupert W. Mitochondria-targeted green fluorescent proteins: convenient tools for the study of organelle biogenesis in Saccharomyces cerevisiae. Yeast 2000, 16(15):1421-1427. 10.1002/1097-0061(200011)16:15<1421::AID-YEA624>3.0.CO;2-U, 11054823.
38. Wilson RB, Renault G, Jacquet M, Tatchell K. The pde2 gene of Saccharomyces cerevisiae is allelic to rcal and encodes a phosphodiesterase which protects the cell from extracellullar cAMP. FEBS letters 1993, 325(3):191-195. 10.1016/0014-5793(93)81071-7, 8391474.
39. Nagley P, Hall RM, Ooi BG. Amino acid substitutions in mitochondrial ATPase subunit 9 of saccharomyces cerevisiae leading to oligomycin or venturicidin resistance. FEBS letters 1986, 195(1-2):159-163. 10.1016/0014-5793(86)80152-1, 2867935.
40. Cain K, Griffiths DE. Studies of energy-linked reactions. Biochem J 1977, 162:575-580. 1164640, 141273.
41. Vachova L, Devaux F, Kucerova H, Ricicova M, Jacq C, Palkova Z. Sok2p transcription factor is involved in adaptive program relevant for long term survival of Saccharomyces cerevisiae colonies. The Journal of biological chemistry 2004, 279(36):37973-37981. 10.1074/jbc.M404594200, 15229222.
42. Vachova L, Palkova Z. Physiological regulation of yeast cell death in multicellular colonies is triggered by ammonia. The Journal of cell biology 2005, 169(5):711-717. 10.1083/jcb.200410064, 2171614, 15939758.
43. Garcia-Rodriguez LJ, Gay AC, Pon LA. Puf3p, a Pumilio family RNA binding protein, localizes to mitochondria and regulates mitochondrial biogenesis and motility in budding yeast. The Journal of cell biology 2007, 176(2):197-207. 10.1083/jcb.200606054, 2063939, 17210948.
44. Forsburg SL, Guarente L. Identification and characterization of HAP4: a third component of the CCAAT-bound HAP2/HAP3 heteromer. Genes & development 1989, 3(8):1166-1178.
45. Zhang L, Zambon AC, Vranizan K, Pothula K, Conklin BR, Insel PA. Gene expression signatures of cAMP/protein kinase A (PKA)-promoted, mitochondrial-dependent apoptosis. Comparative analysis of wild-type and cAMP-deathless S49 lymphoma cells. The Journal of biological chemistry 2008, 283(7):4304-4313. 10.1074/jbc.M708673200, 18048352.
46. Martinez-Velazquez M, Melendez-Zajgla J, Maldonado V. Apoptosis induced by cAMP requires Smac/DIABLO transcriptional upregulation. Cellular signalling 2007, 19(6):1212-1220. 10.1016/j.cellsig.2007.01.001, 17320350.
47. Pagliarini DJ, Dixon JE. Mitochondrial modulation: reversible phosphorylation takes center stage?. Trends in biochemical sciences 2006, 31(1):26-34. 10.1016/j.tibs.2005.11.005, 16337125.
48. Acin-Perez R, Salazar E, Kamenetsky M, Buck J, Levin LR, Manfredi G. Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation. Cell metabolism 2009, 9(3):265-276. 10.1016/j.cmet.2009.01.012, 2684673, 19254571.
49. Cho JH, Lee YK, Chae CB. The modulation of the biological activities of mitochondrial histone Abf2p by yeast PKA and its possible role in the regulation of mitochondrial DNA content during glucose repression. Biochimica et biophysica acta 2001, 1522(3):175-186.
50. Sickmann A, Reinders J, Wagner Y, Joppich C, Zahedi R, Meyer HE, Schonfisch B, Perschil I, Chacinska A, Guiard B, et al. The proteome of Saccharomyces cerevisiae mitochondria. Proceedings of the National Academy of Sciences of the United States of America 2003, 100(23):13207-13212. 10.1073/pnas.2135385100, 263752, 14576278.
51. Ward MP, Gimeno CJ, Fink GR, Garrett S. SOK2 may regulate cyclic AMP-dependent protein kinase-stimulated growth and pseudohyphal development by repressing transcription. Molecular and cellular biology 1995, 15(12):6854-6863. 230940, 8524252.
52. Rep M, Proft M, Remize F, Tamas M, Serrano R, Thevelein JM, Hohmann S. The Saccharomyces cerevisiae Sko1p transcription factor mediates HOG pathway-dependent osmotic regulation of a set of genes encoding enzymes implicated in protection from oxidative damage. Molecular microbiology 2001, 40(5):1067-1083. 10.1046/j.1365-2958.2001.02384.x, 11401713.
53. Pascual-Ahuir A, Posas F, Serrano R, Proft M. Multiple levels of control regulate the yeast cAMP-response element-binding protein repressor Sko1p in response to stress. The Journal of biological chemistry 2001, 276(40):37373-37378. 10.1074/jbc.M105755200, 11500510.
54. Lascaris R, Piwowarski J, van der Spek H, Teixeira de Mattos J, Grivell L, Blom J. Overexpression of HAP4 in glucose-derepressed yeast cells reveals respiratory control of glucose-regulated genes. Microbiology (Reading, England) 2004, 150(Pt 4):929-934.
55. Nowikovsky K, Reipert S, Devenish RJ, Schweyen RJ. Mdm38 protein depletion causes loss of mitochondrial K+/H+ exchange activity, osmotic swelling and mitophagy. Cell death and differentiation 2007, 14(9):1647-1656. 10.1038/sj.cdd.4402167, 17541427.
56. Barrientos A, Barros MH, Valnot I, Rotig A, Rustin P, Tzagoloff A. Cytochrome oxidase in health and disease. Gene 2002, 286(1):53-63. 10.1016/S0378-1119(01)00803-4, 11943460.
57. Shoubridge EA. Cytochrome c oxidase deficiency. American journal of medical genetics 2001, 106(1):46-52. 10.1002/ajmg.1378, 11579424.
58. Sullivan PG, Brown MR. Mitochondrial aging and dysfunction in Alzheimer's disease. Progress in neuro-psychopharmacology & biological psychiatry 2005, 29(3):407-410.