SAC as a model for understanding the impact of endosymbiosis on cell signaling

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1842, Issue 12, 2014, Pages 2548-2554

  Blackstone, Neil W ^a  

^a NORTHERN ILLINOIS UNIVERSITY   (United States)

Author keywords

Adenylyl cyclases; Evolution; History of life; Phylogeny; STAT; VEGF

Indexed keywords

ADENYLATE CYCLASE; STAT PROTEIN; VASCULOTROPIN; ADCY10 PROTEIN, HUMAN;

ALPHAPROTEOBACTERIA; BACTERIAL GENOME; ENDOSYMBIOSIS; EUKARYOTE; HOMEOSTASIS; HYPOTHESIS; METABOLISM; MITOCHONDRION; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; EVOLUTION; HUMAN; SYMBIOSIS;

ALPHAPROTEOBACTERIA; EUKARYOTA;

ADENYLATE CYCLASE; BIOLOGICAL EVOLUTION; HUMANS; SIGNAL TRANSDUCTION; SYMBIOSIS;

EID: 84919391833     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2014.05.037     Document Type: Review

References (72)

1. Maynard Smith J., Szathmáry E. The Major Transitions in Evolution 1995, Oxford University Press, Oxford.
2. Maynard Smith J., Szathmáry E. The Origins of Life 1999, Oxford University Press, Oxford.
3. Okasha S. Evolution and the Levels of Selection 2006, Oxford University Press, Oxford.
4. 2+ signaling systems. Trends Cell Biol. 2011, 21:202-211.
5. Friedman J.R., Nunnari J. Mitochondrial form and function. Nature 2014, 505:335-343.
6. Blackstone N.W. Why did eukaryotes evolve only once? Genetic and energetic aspects of conflict and conflict mediation. Phil. Trans. R. Soc. B 2013, 368:20120266.
7. Blackstone N.W. Evolution and cell physiology. 2. The evolution of cell signaling from mitochondria to Metazoa. Am. J. Physiol. Cell Physiol. 2013, 305:C909-C915.
8. Wilson D.S., Wilson E.O. Rethinking the theoretical foundation of sociobiology. Q. Rev. Biol. 2007, 82:327-348.
9. Lewontin R.C. The units of selection. Annu. Rev. Ecol. Syst. 1970, 1:1-18.
10. Darwin C. The Descent of Man 2004, Penguin, London, (first published 1871).
11. Buss L.W. The Evolution of Individuality 1987, Princeton University Press, Princeton, NJ.
12. Michod R.E. Cooperation and conflict mediation during the origin of multicellularity. Genetic and Cultural Evolution of Cooperation 2003, MIT Press, Cambridge, MA. P. Hammerstein (Ed.).
13. Bonner J.T. The Evolution of Complexity 1988, Princeton University Press, Princeton, NJ.
14. Lane N., Martin W. The energetics of genome complexity. Nature 2010, 467:929-934.
15. Bonner J.T. The origins of multicellularity. Integr. Biol. 1998, 1:27-36.
16. Rokas A. Multicellularity and the early history of the genetic toolkit for animal development. Annu. Rev. Genet. 2008, 42:235-251.
17. Lachmann M., Blackstone N.W., Haig D., Kowald A., Michod R.E., Szathmáry E., Werren J.H., Wolpert L. Group 3: cooperation and conflict in the evolution of genomes, cells, and multicellular organisms. Genetic and Cultural Evolution of Cooperation 2003, MIT Press, Cambridge, MA. P. Hammerstein (Ed.).
18. Minelli A. Perspectives in Animal Phylogeny and Evolution 2009, Oxford University Press, Oxford.
19. Chance B., Williams G.R. The respiratory chain and oxidative phosphorylation. Adv. Enzymol. Relat. Subj. Biochem. 1956, 17:65-134.
20. Kamenentsky 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.
21. Linder J.U., Schulz J.E. The class III adenylyl cyclases: multi-purpose signaling modules. Cell. Signal. 2003, 15:1081-1089.
22. Cann M.J., Hammer A., Zhou J., Kanacher T. A defined subset of adenylyl cyclases is regulated by bicarbonate ion. J. Biol. Chem. 2003, 278:35033-35038.
23. 2. Biochem. J. 2006, 396:215-218.
24. Tresguerres M., Buck J., Levin L.R. Physiological carbon dioxide, bicarbonate, and pH sensing. Pflugers Arch. - Eur. J. Physiol. 2010, 460:953-964.
25. Danchin A. Phylogeny of adenylyl cyclases. Adv. Second Messenger Phosphoprotein Res. 1993, 27:109-162.
26. Sismeiro O., Trotot P., Biville F., Vivares C., Danchin A. Aeromonas hydrophila adenylyl cyclase 2: a new class of adenylyl cyclases with thermophilic properties and sequence similarities to proteins and hyperthermophilic archaebacteria. J. Bacteriol. 1998, 180:3339-3344.
27. Danchin A. Reference classification of adenylate cyclases: adenylyl cyclases and guanylyl cyclases: role and classification http://www.normalesup.org/~adanchin/science/adenylyl_cyclases.html.
28. Gilbert W. Origin of life: the RNA world. Nature 1986, 319:618.
29. +, and early evolution. Orig. Life Evol. Biosph. 2011, 41:483-493.
30. Lane N. Life Ascending: The Ten Great Inventions of Evolution 2009, Norton, New York.
31. Smith E., Morowitz H.J. Universality in intermediary metabolism. Proc. Natl. Acad. Sci. 2004, 101:13168-13173.
32. Gray M.W., Burger G., Lang B.F. The origin and early evolution of mitochondria. Genome Biol. 2001, 2:1018.1-1018.5.
33. Williams T.A., Foster P.G., Nye T.M.W., Cox C.J., Embley T.M. A congruent phylogenomic signal places eukaryotes within the Archaea. Proc. R. Soc. Lond. B 2012, 279:4870-4879.
34. Martin W.F. Early evolution without a tree of life. Biol. Direct 2011, 6:36.
35. Ramulu H.G., Groussin M., Talla E., Planel R., Daubin V., Brochier-Armanet C. Ribosomal proteins: toward a next generation standard for prokaryotic systematic?. Mol. Phylogenet. Evol. 2014, 75:103-117.
36. Yurkov V.V., Beatty J.T. Aerobic anoxygenic phototrophic bacteria. Microbiol. Mol. Biol. Rev. 1998, 62:695-724.
37. Ohmori K., Hirose M., Ohmori M. Function of cAMP as a mat-forming factor in the cyanobacterium Spirulina platensis. Plant Cell Physiol. 1992, 33:21-25.
38. 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.
39. Dutton P.L., Wilson D.F. Redox potentiometry in mitochondrial and photosynthetic bioenergetics. Biochim. Biophys. Acta 1974, 346:165-212.
40. Baltscheffsky H., Baltscheffsky M. Mitochondrial ancestor models: Paracoccus, Rhizobium, and Rhodospirillum. Mitochondria and Microsomes in honor of Lars Ernster 1981, Addison-Wesley, Boston. C.P. Lee, G. Schartz, G. Dallner (Eds.).
41. Acin-Perez R., Salazar E., Kamenetsky M., Buck J., Levin L.R., Manfredi G. Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation. Cell Metab. 2009, 9:265-276.
42. Acin-Perez R., Russwurm M., Günnewig K., Gertz M., Zoidl G., Ramos L., Buck J., Levin L.R., Rassow J., Manfredi G., Steegborn C. A phosphodiesterase 2A isoform localized to mitochondria regulates respiration. J. Biol. Chem. 2011, 286:30423-30432.
43. Lefkimmiatis K., Leronni D., Hofer A.M. The inner and outer compartments of mitochondria are sites of distinct cAMP/PKA signaling dynamics. J. Cell Biol. 2013, 202:453-462.
44. Lefkimmiatis K. cAMP signaling meets mitochondrial compartments. Biochem. Soc. Trans. 2014, 42:265-269.
45. Tresguerres M., Barott K.L. Helman Y, M.E. Barron, Hess KC, J.N. Roa, Established and potential physiological roles of bicarbonate-sensing soluble adenylyl cyclase (sAC) in aquatic animals. J. Exp. Biol. 2014, 217:663-672.
46. Warren C.M., Ziyad S., Briot A., Der A., Iruela-Arispe M.L. A ligand-independent VEGFR2 signaling pathway limits angiogenic responses in diabetes. Sci. Signal. 2014, 7:1-12. (307, ra1).
47. Henze K., Martin W. How do mitochondrial genes get into the nucleus?. Trends Genet. 2001, 17:383-387.
48. Nomura M., Beltrán C., Darszon A., Vacquier V.D. A soluble adenylyl cyclase from sea urchin spermatozoa. Gene 2005, 353:231-238.
49. Wertheimer E., Krapf D., de la Vega-Beltran J.L., Sánchez-Cárdenas C., Navarrete F., Haddad D., Escoffier J., Salicioni A.M., Levin L.R., Buck J., Mager J., Darszon A., Visconti P.E. Compartmentalization of distinct cAMP signaling pathways in mammalian sperm. J. Biol. Chem. 2013, 49:35307-35320.
50. Klengel T., Liang W.-J., Chaloupka J., Ruoff C., Schröppel K., Naglik J.R., Eckert S.E., Mogensen E.G., Haynes K., Tuite M.F., Levin L.R., Buck J., Mühischlegel F.A. Fungal adenylyl cyclase integrates CO2 sensing with cAMP signaling and virulence. Curr. Biol. 2005, 15:2021-2016.
51. Saran S., Meima M.E., Alvarez-Curto E., Weening K.E., Rozen D.E., Schaap P. cAMP signaling in Dictyostelium. J. Muscle Res. Cell Motil. 2002, 23:793-802.
52. Blackstone N.W. A food's-eye view of the transition from basal metazoans to bilaterians. Integr. Comp. Biol. 2007, 47:724-733.
53. Weis V.M. Commentary: Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J. Exp. Biol. 2008, 211:3059-3066.
54. Barott K.L., Helman Y., Haramaty L., Barron M.E., Hess K.C., Buck J., Levin L.R., Tresguerres M. High adenylyl cyclase activity and in vivo cAMP fluctuations in corals suggest central physiological role. Sci. Rep. 2013, 3:1-7.
55. Netherton S.E., Scheer D.M., Morrison P.R., Parrin A.P., Blackstone N.W. Physiological correlates of symbiont migration during bleaching of two octocoral species. J. Exp. Biol. 2014, 217:1469-1477.
56. Levy D.E., Lee C.-K. What does Stat3 do?. J. Clin. Investig. 2002, 109:1143-1148.
57. Gough D.J., Corlett A., Schlessinger K., Wegrzyn J., Larner A.C., Levy D.E. Mitochondrial STAT3 supports Ras-dependent oncogenic transformation. Science 2009, 324:1713-1716.
58. Wegrzyn J., Potla R., Chwae Y.-J., Sepuri N.B.V., Zhang Q., Koeck T., Derecka M., Szczepanek K., Szelag M., Gornicka A., Moh A., Moghaddas S., Chen Q., Bobbili S., Cichy J., Dulak J., Baker D.P., Wolfman A., Stuehr D., Hassan M.O., Fu X.-Y., Avadhani N., Drake J.L., Fawcett P., Lesnefsky E.J., Larner A.C. Function of mitochondrial Stat3 in cellular respiration. Science 2009, 323:793-797.
59. Blackstone N.W. Is evolutionary theory central to molecular cell biology?. Evol J. 2009, 1:34-43.
60. Liongue C., O'Sullivan L.A., Trengove M.C., Ward A.C. Evolution of JAK-STAT pathway components: mechanisms and role in immune system development. PLoS One 2012, 7(3):e32777.
61. Bakal C.J., Vujaklija D., Davies J. Immunochemical indentification of a Stat3 analogue in Streptomycetes. Food Technol. Biotechnol. 2001, 39:313-317.
62. Kawashima T., Kawashima S., Tanaka C., Murai M., Yoneda M., Putnam N.H., Rokhsar D.S., Kanehisa M., Satoh N., Wada H. Domain shuffling and the evolution of vertebrates. Genome Res. 2009, 19:1393-1403.
63. Hagberg C.E., Falkevall A., Wang X., Larsson E., Huusko J., Nilsson I., van Meeteren L.A., Samen E., Lu L., Vanwildemeersch M., Klar J., Genove G., Pietras K., Stone-Elander S., Claesson-Welsh L., Yiä-Herttuala S., Lindahl P., Eriksson U. Vascular endothelial growth factor B controls endothelial fatty acid uptake. Nature 2010, 464:917-921.
64. Andrae J., Gallini R., Betsholtz C. Role of platelet-derived growth factors in physiology and medicine. Genes Dev. 2008, 22:1276-1312.
65. Grassot J., Gouy M., Perrière G., Mouchiroud G. Origin and molecular evolution of receptory tyrosine kinases with immunoglobulin-like domains. Mol. Biol. Evol. 2006, 23:1232-1241.
66. Mylne J.S., Chan L.Y., Chanson A.H., Daly N.L., Schaefer H., Bailey T.L., Nguyencong P., Cascales L., Craik D.J. Cyclic peptides arising by evolutionary parallelism via asparaginyl-endopeptidase-mediated biosynthesis. Plant Cell 2012, 24:2765-2778.
67. Vitt U.A., Hsu S.Y., Hsueh A.J.W. Evolution and classification of cystine knot-containing hormones and related extracellular signaling molecules. Mol. Endocrinol. 2001, 15:681-694.
68. Filomeni G., Rotilio G., Ciriolo M.R. Disulfide relays and phorphorylation cascades: partners in redox-mediated signaling pathways. Cell Death Differ. 2005, 12:1555-1563.
69. Grosberg R.K., Strathmann R.R. The evolution of multicellularity: a minor major transition?. Annu. Rev. Ecol. Evol. Syst. 2007, 38:621-654.
70. Lane N. Energetics and genetics across the prokaryote-eukaryote divide. Biol. Direct 2011, 6:35.
71. Nedelcu A.M. Comparative genomics of phylogenetically diverse unicellular eukaryotes provide new insights into the genetic basis for the evolution of the programmed cell death machinery. J. Mol. Evol. 2009, 68:256-268.
72. Pennisi E. Green genomes. Science 2011, 332:1372-1375.