A role for A-to-I RNA editing in temperature adaptation

Physiology

Volumn 27, Issue 6, 2012, Pages 362-369

  Garrett, Sandra C ^a   Rosenthal, Joshua J C ^a  

^a UNIVERSITY OF PUERTO RICO MEDICAL SCIENCES CAMPUS   (Puerto Rico)

Author keywords

[No Author keywords available]

Indexed keywords

ISOPROTEIN; MESSENGER RNA;

ADAPTATION; ANIMAL; GENETICS; HUMAN; REVIEW; RNA EDITING; TEMPERATURE;

ADAPTATION, BIOLOGICAL; ANIMALS; HUMANS; PROTEIN ISOFORMS; RNA EDITING; RNA, MESSENGER; TEMPERATURE;

EID: 84870777288     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00029.2012     Document Type: Review

References (63)

1. Athanasiadis A, Rich A, Maas S. Widespread A-to-I RNA editing of Alu-containing mRNAs in the human transcriptome. PLoS Biol 2: e391, 2004.
2. Basilio C, Wahba AJ, Lengyel P, Speyer JF, Ochoa S. Synthetic polynucleotides and the amino acid code. Proc Natl Acad Sci USA 48: 613-616, 1962.
3. Berezovsky IN, Chen WW, Choi PJ, Shakhnovich EI. Entropic stabilization of proteins and its proteomic consequences. PLoS Comput Biol 1: e47, 2005.
4. Bhalla T, Rosenthal JJ, Holmgren M, Reenan R. Control of human potassium channel inactivation by editing of a small mRNA hairpin. Nat Struct Mol Biol 11: 950-956, 2004.
5. Bjelic S, Brandsdal BO, Aqvist J. Cold adaptation of enzyme reaction rates. Biochemistry 47: 10049-10057, 2008.
6. Blow M, Futreal PA, Wooster R, Stratton MR. A survey of RNA editing in human brain. Genome Res 14: 2379-2387, 2004. 367.
7. Britton KL, Baker PJ, Borges KM, Engel PC, Pasquo A, Rice DW, Robb FT, Scandurra R, Stillman TJ, Yip KS. Insights into thermal stability from a comparison of the glutamate dehydrogenases from Pyrococcus furiosus and Thermococcus litoralis. Eur J Biochem 229: 688-695, 1995.
8. Brouns SJ, Wu H, Akerboom J, Turnbull AP, de Vos WM, van der Oost J. Engineering a selectable marker for hyperthermophiles. J Biol Chem 280: 11422-11431, 2005.
9. Burns CM, Chu H, Rueter SM, Hutchinson LK, Canton H, Sanders-Bush E, Emeson RB. Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature 387: 303-308, 1997.
10. Chen J, Stites WE. Replacement of staphylococcal nuclease hydrophobic core residues with those from thermophilic homologues indicates packing is improved in some thermostable proteins. J Mol Biol 344: 271-280, 2004.
11. Colina C, Palavicini JP, Srikumar D, Holmgren M, Rosenthal JJ. Regulation of Na /K ATPase transport velocity by RNA editing. PLoS Biol 8: e1000540, 2010.
12. Dawson TR, Sansam CL, Emeson RB. Structure and sequence determinants required for the RNA editing of ADAR2 substrates. J Biol Chem 279: 4941-4951, 2004.
13. Desterro JM, Keegan LP, Jaffray E, Hay RT, O'Connell MA, Carmo-Fonseca M. SUMO-1 modification alters ADAR1 editing activity. Mol Biol Cell 16: 5115-5126, 2005.
14. Desterro JM, Keegan LP, Lafarga M, Berciano MT, O'Connell M, Carmo-Fonseca M. Dynamic association of RNA-editing enzymes with the nucleolus. J Cell Sci 116: 1805-1818, 2003.
15. Dong Y, Somero GN. Temperature adaptation of cytosolic malate dehydrogenases of limpets (genus Lottia): differences in stability and function due to minor changes in sequence correlate with biogeographic and vertical distributions. J Exp Biol 212: 169-177, 2009.
16. Eckmann CR, Neunteufl A, Pfaffstetter L, Jantsch MF. The human but not the Xenopus RNA-editing enzyme ADAR1 has an atypical nuclear localization signal and displays the characteristics of a shuttling protein. Mol Biol Cell 12: 1911-1924, 2001.
17. Farias ST, Bonato MC. Preferred amino acids and thermostability. Genet Mol Res 2: 383-393, 2003.
18. Garrett S, Rosenthal JJ. RNA editing underlies temperature adaptation in K channels from polar octopuses. Science 335: 848-851, 2012.
19. Georlette D, Blaise V, Collins T, D'Amico S, Gratia E, Hoyoux A, Marx JC, Sonan G, Feller G, Gerday C. Some like it cold: biocatalysis at low temperatures. FEMS Microbiol Rev 28: 25-42, 2004.
20. Gerber A, O'Connell MA, Keller W. Two forms of human double-stranded RNA-specific editase 1 (hRED1) generated by the insertion of an Alu cassette. RNA 3: 453-463, 1997.
21. V1.1 channel mRNAs disrupts binding of the N-terminus tip at the intracellular cavity. Nat Commun 2: 436, 2011.
22. Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, Yang L, Artieri CG, van Baren MJ, Boley N, Booth BW, Brown JB, Cherbas L, Davis CA, Dobin A, Li R, Lin W, Malone JH, Mattiuzzo NR, Miller D, Sturgill D, Tuch BB, Zaleski C, Zhang D, Blanchette M, Dudoit S, Eads B, Green RE, Hammonds A, Jiang L, Kapranov P, Langton L, Perrimon N, Sandler JE, Wan KH, Willingham A, Zhang Y, Zou Y, Andrews J, Bickel PJ, Brenner SE, Brent MR, Cherbas P, Gingeras TR, Hoskins RA, Kaufman TC, Oliver B, Celniker SE. The developmental transcriptome of Drosophila melanogaster. Nature 471: 473-479, 2011.
23. Hennig M, Darimont B, Sterner R, Kirschner K, Jansonius JN. 2.0. A structure of indole-3-glycerol phosphate synthase from the hyperthermophile Sulfolobus solfataricus: possible determinants of protein stability. Structure 3: 1295-1306, 1995.
24. Huang H, Tan BZ, Shen Y, Tao J, Jiang F, Sung YY, Ng CK, Raida M, Kohr G, Higuchi M, FatemiShariatpanahi H, Harden B, Yue DT, Soong TW. RNA editing of the IQ domain in Ca(v)1.3 channels modulates their Ca(2)-dependent inactivation. Neuron 73: 304-316, 2012.
25. Johns GC, Somero GN. Evolutionary convergence in adaptation of proteins to temperature: A4-lactate dehydrogenases of Pacific damselfishes (Chromis spp.). Mol Biol Evol 21: 314-320, 2004.
26. Jollivet D, Mary J, Gagniere N, Tanguy A, Fontanillas E, Boutet I, Hourdez S, Segurens B, Weissenbach J, Poch O, Lecompte O. Proteome adaptation to high temperatures in the ectothermic hydrothermal vent Pompeii worm. PLos One 7: e31150, 2012.
27. Keegan LP, Brindle J, Gallo A, Leroy A, Reenan RA, O'Connell MA. Tuning of RNA editing by ADAR is required in Drosophila. EMBO J 24: 2183-2193, 2005.
28. Keegan LP, McGurk L, Palavicini JP, Brindle J, Paro S, Li X, Rosenthal JJ, O'Connell MA. Functional conservation in human and Drosophila of Metazoan ADAR2 involved in RNA editing: loss of ADAR1 in insects. Nucleic Acids Res 39: 7249-7262, 2011.
29. Kempf JG, Jung JY, Ragain C, Sampson NS, Loria JP. Dynamic requirements for a functional protein hinge. J Mol Biol 368: 131-149, 2007.
30. Kim DD, Kim TT, Walsh T, Kobayashi Y, Matise TC, Buyske S, Gabriel A. Widespread RNA editing of embedded alu elements in the human transcriptome. Genome Res 14: 1719-1725, 2004.
31. Lai F, Chen CX, Carter KC, Nishikura K. Editing of glutamate receptor B subunit ion channel RNAs by four alternatively spliced DRADA2 doublestranded RNA adenosine deaminases. Mol Cell Biol 17: 2413-2424, 1997.
32. Laurencikiene J, Kallman AM, Fong N, Bentley DL, Ohman M. RNA editing and alternative splicing: the importance of co-transcriptional coordination. EMBO Rep 7: 303-307, 2006.
33. Lehmann KA, Bass BL. The importance of internal loops within RNA substrates of ADAR1. J Mol Biol 291: 1-13, 1999.
34. Li JB, Levanon EY, Yoon JK, Aach J, Xie B, Leproust E, Zhang K, Gao Y, Church GM. Genomewide identification of human RNA editing sites by parallel DNA capturing and sequencing. Science 324: 1210-1213, 2009.
35. Low KH, Lim C, Ko HW, Edery I. Natural variation in the splice site strength of a clock gene and species-specific thermal adaptation. Neuron 60: 1054-1067, 2008.
36. Maas S, Melcher T, Herb A, Seeburg PH, Keller W, Krause S, Higuchi M, O'Connell MA. Structural requirements for RNA editing in glutamate receptor pre-mRNAs by recombinant doublestranded RNA adenosine deaminase. J Biol Chem 271: 12221-12226, 1996.
37. Majercak J, Sidote D, Hardin PE, Edery I. How a circadian clock adapts to seasonal decreases in temperature and day length. Neuron 24: 219-230, 1999.
38. Marcucci R, Brindle J, Paro S, Casadio A, Hempel S, Morrice N, Bisso A, Keegan LP, Del Sal G, O'Connell MA. Pin1 and WWP2 regulate GluR2 Q/R site RNA editing by ADAR2 with opposing effects. EMBO J 30: 4211-4222, 2011.
39. Metpally RP, Reddy BV. Comparative proteome analysis of psychrophilic versus mesophilic bacterial species: insights into the molecular basis of cold adaptation of proteins. BMC Genomics 10: 11, 2009.
40. Moiseev VM, Rodina EV, Kurilova SA, Vorobyeva NN, Nazarova TI, Avaeva SM. Substitutions of glycine residues Gly100 and Gly147 in conservative loops decrease rates of conformational rearrangements of Escherichia coli inorganic pyrophosphatase. Biochemistry (Mosc) 70: 858-866, 2005.
41. Murrell-Lagnado RD, Aldrich RW. Interactions of amino terminal domains of Shaker K channels with a pore blocking site studied with synthetic peptides. J Gen Physiol 102: 949-975, 1993.
42. Narberhaus F. Translational control of bacterial heat shock and virulence genes by temperaturesensing mRNAs. RNA Biol 7: 84-89, 2009.
43. Nimmich ML, Heidelberg LS, Fisher JL. RNA editing of the GABA(A) receptor alpha3 subunit alters the functional properties of recombinant receptors. Neurosci Res 63: 288-293, 2009.
44. Niswender CM, Copeland SC, Herrick-Davis K, Emeson RB, Sanders-Bush E. RNA editing of the human serotonin 5-hydroxytryptamine 2C receptor silences constitutive activity. J Biol Chem 274: 9472-9478, 1999.
45. Palackal N, Brennan Y, Callen WN, Dupree P, Frey G, Goubet F, Hazlewood GP, Healey S, Kang YE, Kretz KA, Lee E, Tan X, Tomlinson GL, Verruto J, Wong VW, Mathur EJ, Short JM, Robertson DE, Steer BA. An evolutionary route to xylanase process fitness. Protein Sci 13: 494-503, 2004.
46. Palavicini JP, O'Connell MA, Rosenthal JJ. An extra double-stranded RNA binding domain confers high activity to a squid RNA editing enzyme. RNA 15: 1208-1218, 2009.
47. Palladino MJ, Keegan LP, O'Connell MA, Reenan RA. dADAR, a Drosophila double-stranded RNA-specific adenosine deaminase is highly developmentally regulated and is itself a target for RNA editing. RNA 6: 1004-1018, 2000.
48. Patton DE, Silva T, Bezanilla F. RNA editing generates a diverse array of transcripts encoding squid Kv2 K channels with altered functional properties. Neuron 19: 711-722, 1997.
49. Peng Z, Cheng Y, Tan BC, Kang L, Tian Z, Zhu Y, Zhang W, Liang Y, Hu X, Tan X, Guo J, Dong Z, Liang Y, Bao L, Wang J. Comprehensive analysis of RNA-Seq data reveals extensive RNA editing in a human transcriptome. Nat Biotechnol 30: 253-260, 2012.
50. Reenan RA. Molecular determinants and guided evolution of species-specific RNA editing. Nature 434: 409-413, 2005.
51. Rosenthal JJ, Bezanilla F. Extensive editing of mRNAs for the squid delayed rectifier K channel regulates subunit tetramerization. Neuron 34: 743-757, 2002.
52. Rula EY, Lagrange AH, Jacobs MM, Hu N, Macdonald RL, Emeson RB. Developmental modulation of GABA(A) receptor function by RNA editing. J Neurosci 28: 6196-6201, 2008.
53. Ryan MY, Maloney R, Reenan RA. Characterization of five RNA editing sites in Shab potassium channels. Channels 2: 202-209, 2008.
54. Sansam CL, Wells KS, Emeson RB. Modulation of RNA editing by functional nucleolar sequestration of ADAR2. Proc Natl Acad Sci USA 100: 14018-14023, 2003.
55. Savva YA, Jepson JE, Sahin A, Sugden AU, Dorsky JS, Alpert L, Lawrence C, Reenan RA. Autoregulatory RNA editing fine-tunes mRNA recoding and complex behaviour in Drosophila. Nat Commun 3: 790, 2012.
56. Shin DS, Didonato M, Barondeau DP, Hura GL, Hitomi C, Berglund JA, Getzoff ED, Cary SC, Tainer JA. Superoxide dismutase from the eukaryotic thermophile Alvinella pompejana: structures, stability, mechanism, and insights into amyotrophic lateral sclerosis. J Mol Biol 385: 1534-1555, 2009.
57. Somero GN. Adaptation of enzymes to temperature: searching for basic "strategies". Comp Biochem Physiol B Biochem Mol Biol 139: 321-333, 2004.
58. Spiller B, Gershenson A, Arnold FH, Stevens RC. A structural view of evolutionary divergence. Proc Natl Acad Sci USA 96: 12305-12310, 1999.
59. Wahlstedt H, Daniel C, Enstero M, Ohman M. Large-scale mRNA sequencing determines global regulation of RNA editing during brain development. Genome Res 19: 978-986, 2009.
60. Wang GZ, Lercher MJ. Amino acid composition in endothermic vertebrates is biased in the same direction as in thermophilic prokaryotes. BMC Evol Biol 10: 263, 2010.
61. Yip KS, Stillman TJ, Britton KL, Artymiuk PJ, Baker PJ, Sedelnikova SE, Engel PC, Pasquo A, Chiaraluce R, Consalvi V, et al. The structure of Pyrococcus furiosus glutamate dehydrogenase reveals a key role for ion-pair networks in maintaining enzyme stability at extreme temperatures. Structure 3: 1147-1158, 1995.
62. Zeldovich KB, Berezovsky IN, Shakhnovich EI. Protein and DNA sequence determinants of thermophilic adaptation. PLoS Comput Biol 3: e5, 2007.
63. Zhu BY, Zhou NE, Kay CM, Hodges RS. Packing and hydrophobicity effects on protein folding and stability: effects of beta-branched amino acids, valine and isoleucine, on the formation and stability of two-stranded alpha-helical coiled coils/leucine zippers. Protein Sci 2: 383-394, 1993.