Ryanodine receptor calcium release channels: An evolutionary perspective

Advances in Experimental Medicine and Biology

Volumn 740, Issue , 2012, Pages 159-182

  MacKrill, John J ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Calcium; Calcium release channel; Evolution; Inositol 1,4,5 trisphosphate receptor; Protein domains; Ryanodine receptor

Indexed keywords

MANNOSYLTRANSFERASE; RYANODINE RECEPTOR;

ARTICLE; CALCIUM TRANSPORT; EUKARYOTE EVOLUTION; HUMAN; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS;

ANIMALS; CALCIUM; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; HUMANS; PROTEIN STRUCTURE, TERTIARY; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA; VERTEBRATA;

EID: 84859917357     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-94-007-2888-2_7     Document Type: Article

References (107)

1. Case RM, Eisner D, Gurney A, Jones O, Muallem S, Verkhratsky A (2007) Evolution of calcium homeostasis: from birth of the fi rst cell to an omnipresent signalling system. Cell Calcium 42:345-350
2. Dominguez DC (2004) Calcium signalling in bacteria. Mol Microbiol 54:291-297
3. Norris V, Grant S, Freestone P, Canvin J, Sheikh FN, Toth I, Trinei M, Modha K, Norman RI (1996) Calcium signalling in bacteria. J Bacteriol 178:3677-3682
4. Naseem R, Davies SR, Jones H, Wann KT, Holland IB, Campbell AK (2007) Cytosolic Ca2+ regulates protein expression in E. coli through release from inclusion bodies. Biochem Biophys Res Commun 360:33-39
5. Gray MW, Doolittle WF (1982) Has the endosymbiont hypothesis been proven? Microbiol Rev 46:1-42
6. Roger AJ (1999) Reconstructing early events in eukaryotic evolution. Am Nat 154:S146-S163
7. Cavalier-Smith T (1975) The origin of nuclei and of eukaryotic cells. Nature 256:463-468
8. Negulescu PA, Machen TE (1993) Ca transport by plasma membrane and intracellular stores of gastric cells. Am J Physiol 264:C843-C851
9. Endo M (2006) Calcium ion as a second messenger with special reference to excitationcontraction coupling. J Pharmacol Sci 100:519-524
10. Wu X, Zhang T, Bossuyt J, Li X, McKinsey TA, Dedman JR, Olson EN, Chen J, Brown JH, Bers DM (2006) Local InsP3-dependent perinuclear Ca2+ signaling in cardiac myocyte excitation-transcription coupling. J Clin Invest 116:675-682
11. Liang W, Buluc M, van Breemen C, Wang X (2004) Vectorial Ca2+ release via ryanodine receptors contributes to Ca2+ extrusion from freshly isolated rabbit aortic endothelial cells. Cell Calcium 36:431-443
12. Berkelman T, Garret-Engele P, Hoffman NE (1994) The pacL gene of Synechococcus sp. strain PCC 7942 encodes a Ca(2+)-transporting ATPase. J Bacteriol 176:4430-4436
13. Shigaki T, Rees I, Nakhleh L, Hirschi KD (2006) Identification of three distinct phylogenetic groups of CAX cation/proton antiporters. J Mol Evol 63:815-825
14. Kung C, Blount P (2004) Channels in microbes: so many holes to fi ll. Mol Microbiol 53:373-380
15. Jegla TJ, Zmasek CM, Batalov S, Nayak SK (2009) Evolution of the human ion channel set. Comb Chem High Throughput Screen 12:2-23
16. Dolphin AC (2009) Calcium channel diversity: multiple roles of calcium channel subunits. Curr Opin Neurobiol 19:237-244
17. Flucher BE, Takekura H, Franzini-Armstrong C (1993) Development of the excitationcontraction coupling apparatus in skeletal muscle: association of sarcoplasmic reticulum and transverse tubules with myofi brils. Dev Biol 160:135-147
18. Franzini-Armstrong C, Protasi F, Tijskens P (2005) The assembly of calcium release units in cardiac muscle. Ann NY Acad Sci 1047:76-85
19. Meissner G (2002) Regulation of mammalian ryanodine receptors. Front Biosci 7:d2072-d2080
20. Franzini-Armstrong C (1970) STUDIES OF THE TRIAD: I. Structure of the junction in frog twitch fibers. J Cell Biol 47:488-499
21. Di Biase V, Franzini-Armstrong C (2005) Evolution of skeletal type e-c coupling: a novel means of controlling calcium delivery. J Cell Biol 171:695-704
22. Rogers EF, Koniuszy FR et al (1948) Plant insecticides; ryanodine, a new alkaloid from Ryania speciosa Vahl. J Am Chem Soc 70:3086-3088
23. West DJ, Williams AJ (2007) Pharmacological regulators of intracellular calcium release channels. Curr Pharm Des 13:2428-2442
24. Lai FA, Erickson HP, Rousseau E, Liu QY, Meissner G (1988) Purification and reconstitution of the calcium release channel from skeletal muscle. Nature 331:315-319
25. Campbell KP, Knudson CM, Imagawa T, Leung AT, Sutko JL, Kahl SD, Raab CR, Madson L (1987) Identification and characterization of the high affi nity [3H]ryanodine receptor of the junctional sarcoplasmic reticulum Ca2+ release channel. J Biol Chem 262:6460-6463
26. Inui M, Saito A, Fleischer S (1987) Purification of the ryanodine receptor and identity with feet structures of junctional terminal cisternae of sarcoplasmic reticulum from fast skeletal muscle. J Biol Chem 262:1740-1747
27. Lai FA, Misra M, Xu L, Smith HA, Meissner G (1989) The ryanodine receptor-Ca2+ release channel complex of skeletal muscle sarcoplasmic reticulum. Evidence for a cooperatively coupled, negatively charged homotetramer. J Biol Chem 264:16776-16785
28. Takeshima H, Nishimura S, Matsumoto T, Ishida H, Kangawa K, Minamino N, Matsuo H, Ueda M, Hanaoka M, Hirose T et al (1989) Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature 339:439-445
29. Mignery GA, Sudhof TC, Takei K, De Camilli P (1989) Putative receptor for inositol 1,4,5-trisphosphate similar to ryanodine receptor. Nature 342:192-195
30. Furuichi T, Yoshikawa S, Miyawaki A, Wada K, Maeda N, Mikoshiba K (1989) Primary structure and functional expression of the inositol 1,4,5-trisphosphate- binding protein P400. Nature 342:32-38
31. Coussin F, Macrez N, Morel JL, Mironneau J (2000) Requirement of ryanodine receptor subtypes 1 and 2 for Ca(2+)-induced Ca(2+) release in vascular myocytes. J Biol Chem 275:9596-9603
32. Sei Y, Gallagher KL, Basile AS (1999) Skeletal muscle type ryanodine receptor is involved in calcium signaling in human B lymphocytes. J Biol Chem 274:5995-6002
33. O'Connell PJ, Klyachko VA, Ahern GP (2002) Identification of functional type 1 ryanodine receptors in mouse dendritic cells. FEBS Lett 512:67-70
34. Giannini G, Conti A, Mammarella S, Scrobogna M, Sorrentino V (1995) The ryanodine receptor/calcium channel genes are widely and differentially expressed in murine brain and peripheral tissues. J Cell Biol 128:893-904
35. Giannini G, Clementi E, Ceci R, Marziali G, Sorrentino V (1992) Expression of a ryanodine receptor-Ca2+ channel that is regulated by TGF-beta. Science 257:91-94
36. Olivares EB, Tanksley SJ, Airey JA, Beck CF, Ouyang Y, Deerinck TJ, Ellisman MH, Sutko JL (1991) Nonmammalian vertebrate skeletal muscles express two triad junctional foot protein isoforms. Biophys J 59:1153-1163
37. Airey JA, Grinsell MM, Jones LR, Sutko JL, Witcher D (1993) Three ryanodine receptor isoforms exist in avian striated muscles. Biochemistry 32:5739-5745
38. Ottini L, Marziali G, Conti A, Charlesworth A, Sorrentino V (1996) Alpha and beta isoforms of ryanodine receptor from chicken skeletal muscle are the homologues of mammalian RyR1 and RyR3. Biochem J 315(Pt 1):207-216
39. Darbandi S, Franck JP (2009) A comparative study of ryanodine receptor (RyR) gene expression levels in a basal ray-fi nned fish, bichir (Polypterus ornatipinnis) and the derived euteleost zebrafish (Danio rerio). Comp Biochem Physiol B Biochem Mol Biol 154:443-448
40. Schredelseker J, Shrivastav M, Dayal A, Grabner M (2010) Non-Ca2+ -conducting Ca2+ channels in fish skeletal muscle excitation-contraction coupling. Proc Natl Acad Sci USA 107:5658-5663
41. Hasan G, Rosbash M (1992) Drosophila homologs of two mammalian intracellular Ca(2+)-release channels: Identification and expression patterns of the inositol 1,4,5-triphosphate and the ryanodine receptor genes. Development 116:967-975
42. Takeshima H, Nishi M, Iwabe N, Miyata T, Hosoya T, Masai I, Hotta Y (1994) Isolation and characterization of a gene for a ryanodine receptor/calcium release channel in Drosophila melanogaster. FEBS Lett 337:81-87
43. Sullivan KM, Scott K, Zuker CS, Rubin GM (2000) The ryanodine receptor is essential for larval development in Drosophila melanogaster. Proc Natl Acad Sci USA 97:5942-5947
44. Formelova J, Hurnak O, Novotova M, Zachar J (1990) Ryanodine receptor purifi ed from crayfish skeletal muscle. Gen Physiol Biophys 9:445-453
45. Seok JH, Xu L, Kramarcy NR, Sealock R, Meissner G (1992) The 30S lobster skeletal muscle Ca2+ release channel (ryanodine receptor) has functional properties distinct from the mammalian channel proteins. J Biol Chem 267:15893-15901
46. Sakube Y, Ando H, Kagawa H (1993) Cloning and mapping of a ryanodine receptor homolog gene of Caenorhabditis elegans. Ann NY Acad Sci 707:540-545
47. Maryon EB, Coronado R, Anderson P (1996) unc-68 encodes a ryanodine receptor involved in regulating C. elegans body-wall muscle contraction. J Cell Biol 134:885-893
48. Quinn KE, Castellani L, Ondrias K, Ehrlich BE (1998) Characterization of the ryanodine receptor/channel of invertebrate muscle. Am J Physiol 274:R494-R502
49. Silva CL, Cunha VM, Mendonca-Silva DL, Noel F (1998) Evidence for ryanodine receptors in Schistosoma mansoni. Biochem Pharmacol 56:997-1003
50. Lovett JL, Marchesini N, Moreno SN, Sibley LD (2002) Toxoplasma gondii microneme secretion involves intracellular Ca(2+) release from inositol 1,4,5-triphosphate (IP(3))/ryanodine-sensitive stores. J Biol Chem 277:25870-25876
51. Muir SR, Sanders D (1996) Pharmacology of Ca2+ release from red beet microsomes suggests the presence of ryanodine receptor homologs in higher plants. FEBS Lett 395:39-42
52. Meimoun P, Vidal G, Bohrer AS, Lehner A, Tran D, Briand J, Bouteau F, Rona JP (2009) Intracellular Ca2+ stores could participate to abscisic acid-induced depolarization and stomatal closure in Arabidopsis thaliana. Plant Signal Behav 4:830-835
53. Sorrentino V, Barone V, Rossi D (2000) Intracellular Ca(2+) release channels in evolution. Curr Opin Genet Dev 10:662-667
54. Mackrill JJ (1999) Protein-protein interactions in intracellular Ca2+ -release channel function. Biochem J 337(Pt 3):345-361
55. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389-3402
56. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275-282
57. Felsenstein J (1985) Confi dence-limits on phylogenies -an approach using the bootstrap. Evolution 39:783-791
58. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739
59. Benterbusch R, Herberg FW, Melzer W, Thieleczek R (1992) Excitation-contraction coupling in a pre-vertebrate twitch muscle: the myotomes of Branchiostoma lanceolatum. J Membr Biol 129:237-252
60. Seo HC, Kube M, Edvardsen RB, Jensen MF, Beck A, Spriet E, Gorsky G, Thompson EM, Lehrach H, Reinhardt R, Chourrout D (2001) Miniature genome in the marine chordate Oikopleura dioica. Science 294:2506
61. Nagata T, Iizumi S, Satoh K, Ooka H, Kawai J, Carninci P, Hayashizaki Y, Otomo Y, Murakami K, Matsubara K, Kikuchi S (2004) Comparative analysis of plant and animal calcium signal transduction element using plant full-length cDNA data. Mol Biol Evol 21:1855-1870
62. Krinke O, Novotna Z, Valentova O, Martinec J (2007) Inositol trisphosphate receptor in higher plants: is it real? J Exp Bot 58:361-376
63. Dasgupta S, Dasgupta D, Sen M, Biswas S, Biswas BB (1996) Interaction of myoinositoltrisphosphate-phytase complex with the receptor for intercellular Ca2+ mobilization in plants. Biochemistry 35:4994-5001
64. Verret F, Wheeler G, Taylor AR, Farnham G, Brownlee C (2010) Calcium channels in photosynthetic eukaryotes: implications for evolution of calcium-based signalling. New Phytol 187:23-43
65. Wheeler GL, Brownlee C (2008) Ca2+ signalling in plants and green algae -changing channels. Trends Plant Sci 13:506-514
66. Zelter A, Bencina M, Bowman BJ, Yarden O, Read ND (2004) A comparative genomic analysis of the calcium signaling machinery in Neurospora crassa, Magnaporthe grisea, and Saccharomyces cerevisiae. Fungal Genet Biol 41:827-841
67. Mack MM, Molinski TF, Buck ED, Pessah IN (1994) Novel modulators of skeletal muscle FKBP12/calcium channel complex from Ianthella basta. Role of FKBP12 in channel gating. J Biol Chem 269:23236-23249
68. Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, Kuo A, Mitros T, Salamov A, Carpenter ML, Signorovitch AY, Moreno MA, Kamm K, Grimwood J, Schmutz J, Shapiro H, Grigoriev IV, Buss LW, Schierwater B, Dellaporta SL, Rokhsar DS (2008) The Trichoplax genome and the nature of placozoans. Nature 454:955-960
69. Schierwater B (2005) My favorite animal, Trichoplax adhaerens. Bioessays 27:1294-1302
70. Philippe H, Derelle R, Lopez P, Pick K, Borchiellini C, Boury-Esnault N, Vacelet J, Renard E, Houliston E, Queinnec E, Da Silva C, Wincker P, Le Guyader H, Leys S, Jackson DJ, Schreiber F, Erpenbeck D, Morgenstern B, Worheide G, Manuel M (2009) Phylogenomics revives traditional views on deep animal relationships. Curr Biol 19:706-712
71. Moreira D, von der Heyden S, Bass D, Lopez-Garcia P, Chao E, Cavalier-Smith T (2007) Global eukaryote phylogeny: combined small-and large-subunit ribosomal DNA trees support monophyly of Rhizaria, Retaria and Excavata. Mol Phylogenet Evol 44:255-266
72. King N (2005) Choanofl agellates. Curr Biol 15:R113-R114
73. Cai X (2008) Unicellular Ca2+ signaling toolkit' at the origin of metazoa. Mol Biol Evol 25:1357-1361
74. Ruiz-Trillo I, Inagaki Y, Davis LA, Sperstad S, Landfald B, Roger AJ (2004) Capsaspora owczarzaki is an independent opisthokont lineage. Curr Biol 14:R946-R947
75. Sebe-Pedros A, de Mendoza A, Lang BF, Degnan BM, Ruiz-Trillo I (2011) Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Mol Biol Evol 28:1241-1254
76. Ladenburger EM, Sehring IM, Korn I, Plattner H (2009) Novel types of Ca2+ release channels participate in the secretory cycle of Paramecium cells. Mol Cell Biol 29:3605-3622
77. Ladenburger EM, Korn I, Kasielke N, Wassmer T, Plattner H (2006) An Ins(1,4,5)P3 receptor in Paramecium is associated with the osmoregulatory system. J Cell Sci 119:3705-3717
78. Eisen JA, Coyne RS, Wu M, Wu D, Thiagarajan M, Wortman JR, Badger JH, Ren Q, Amedeo P, Jones KM, Tallon LJ, Delcher AL, Salzberg SL, Silva JC, Haas BJ, Majoros WH, Farzad M, Carlton JM, Smith RK Jr, Garg J, Pearlman RE, Karrer KM, Sun L, Manning G, Elde NC, Turkewitz AP, Asai DJ, Wilkes DE, Wang Y, Cai H, Collins K, Stewart BA, Lee SR, Wilamowska K, Weinberg Z, Ruzzo WL, Wloga D, Gaertig J, Frankel J, Tsao CC, Gorovsky MA, Keeling PJ, Waller RF, Patron NJ, Cherry JM, Stover NA, Krieger CJ, del Toro C, Ryder HF, Williamson SC, Barbeau RA, Hamilton EP, Orias E (2006) Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol 4:e286
79. Cock JM, Sterck L, Rouze P, Scornet D, Allen AE, Amoutzias G, Anthouard V, Artiguenave F, Aury JM, Badger JH, Beszteri B, Billiau K, Bonnet E, Bothwell JH, Bowler C, Boyen C, Brownlee C, Carrano CJ, Charrier B, Cho GY, Coelho SM, Collen J, Corre E, Da Silva C, Delage L, Delaroque N, Dittami SM, Doulbeau S, Elias M, Farnham G, Gachon CM, Gschloessl B, Heesch S, Jabbari K, Jubin C, Kawai H, Kimura K, Kloareg B, Kupper FC, Lang D, Le Bail A, Leblanc C, Lerouge P, Lohr M, Lopez PJ, Martens C, Maumus F, Michel G, Miranda-Saavedra D, Morales J, Moreau H, Motomura T, Nagasato C, Napoli CA, Nelson DR, Nyvall-Collen P, Peters AF, Pommier C, Potin P, Poulain J, Quesneville H, Read B, Rensing SA, Ritter A, Rousvoal S, Samanta M, Samson G, Schroeder DC, Segurens B, Strittmatter M, Tonon T, Tregear JW, Valentin K, von Dassow P, Yamagishi T, Van de Peer Y, Wincker P (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465:617-621
80. Mackrill JJ (2010) Ryanodine receptor calcium channels and their partners as drug targets. Biochem Pharmacol 79:1535-1543
81. Tani S, Yatzkan E, Judelson HS (2004) Multiple pathways regulate the induction of genes during zoosporogenesis in Phytophthora infestans. Mol Plant Microbe Interact 17:330-337
82. Basu MK, Poliakov E, Rogozin IB (2009) Domain mobility in proteins: functional and evolutionary implications. Brief Bioinform 10:205-216
83. Long M, Betran E, Thornton K, Wang W (2003) The origin of new genes: glimpses from the young and old. Nat Rev Genet 4:865-875
84. Valas RE, Yang S, Bourne PE (2009) Nothing about protein structure classifi cation makes sense except in the light of evolution. Curr Opin Struct Biol 19:329-334
85. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang D, Zhang N, Zheng C, Bryant SH (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39:D225-D229
86. Welch W, Rheault S, West DJ, Williams AJ (2004) A model of the putative pore region of the cardiac ryanodine receptor channel. Biophys J 87:2335-2351
87. Ponting CP (2000) Novel repeats in ryanodine and IP3 receptors and protein O-mannosyltransferases. Trends Biochem Sci 25:48-50
88. Kiselyov K, Mignery GA, Zhu MX, Muallem S (1999) The N-terminal domain of the IP3 receptor gates store-operated hTrp3 channels. Mol Cell 4:423-429
89. Kiselyov KI, Shin DM, Wang Y, Pessah IN, Allen PD, Muallem S (2000) Gating of storeoperated channels by conformational coupling to ryanodine receptors. Mol Cell 6:421-431
90. Schug ZT, da Fonseca PC, Bhanumathy CD, Wagner L 2nd, Zhang X, Bailey B, Morris EP, Yule DI, Joseph SK (2008) Molecular characterization of the inositol 1,4,5-trisphosphate receptor pore-forming segment. J Biol Chem 283:2939-2948
91. Mead-Savery FC, Wang R, Tanna-Topan B, Chen SR, Welch W, Williams AJ (2009) Changes in negative charge at the luminal mouth of the pore alter ion handling and gating in the cardiac ryanodine-receptor. Biophys J 96:1374-1387
92. Montell C (2001) Physiology, phylogeny, and functions of the TRP superfamily of cation channels. Sci STKE 2001:re1
93. Ponting C, Schultz J, Bork P (1997) SPRY domains in ryanodine receptors (Ca(2+)-release channels). Trends Biochem Sci 22:193-194
94. Tae H, Casarotto MG, Dulhunty AF (2009) Ubiquitous SPRY domains and their role in the skeletal type ryanodine receptor. Eur Biophys J 39:51-59
95. van de Graaf SF, van der Kemp AW, van den Berg D, van Oorschot M, Hoenderop JG, Bindels RJ (2006) Identification of BSPRY as a novel auxiliary protein inhibiting TRPV5 activity. J Am Soc Nephrol 17:26-30
96. Cui Y, Tae HS, Norris NC, Karunasekara Y, Pouliquin P, Board PG, Dulhunty AF, Casarotto MG (2009) A dihydropyridine receptor alpha1s loop region critical for skeletal muscle contraction is intrinsically unstructured and binds to a SPRY domain of the type 1 ryanodine receptor. Int J Biochem Cell Biol 41:677-686
97. Otsu K, Willard HF, Khanna VK, Zorzato F, Green NM, MacLennan DH (1990) Molecular cloning of cDNA encoding the Ca2+ release channel (ryanodine receptor) of rabbit cardiac muscle sarcoplasmic reticulum. J Biol Chem 265:13472-13483
98. Zorzato F, Fujii J, Otsu K, Phillips M, Green NM, Lai FA, Meissner G, MacLennan DH (1990) Molecular cloning of cDNA encoding human and rabbit forms of the Ca2+ release channel (ryanodine receptor) of skeletal muscle sarcoplasmic reticulum. J Biol Chem 265:2244-2256
99. Durell SR, Hao Y, Nakamura T, Bakker EP, Guy HR (1999) Evolutionary relationship between K(+) channels and symporters. Biophys J 77:775-788
100. Aravind L, Koonin EV (1998) A novel family of predicted phosphoesterases includes Drosophila prune protein and bacterial RecJ exonuclease. Trends Biochem Sci 23:17-19
101. Anantharaman V, Koonin EV, Aravind L (2001) Regulatory potential, phyletic distribution and evolution of ancient, intracellular small-molecule-binding domains. J Mol Biol 307:1271-1292
102. Andersson JO (2005) Lateral gene transfer in eukaryotes. Cell Mol Life Sci 62:1182-1197
103. Hehemann JH, Correc G, Barbeyron T, Helbert W, Czjzek M, Michel G (2010) Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464:908-912
104. Whitaker JW, McConkey GA, Westhead DR (2009) The transferome of metabolic genes explored: analysis of the horizontal transfer of enzyme encoding genes in unicellular eukaryotes. Genome Biol 10:R36
105. Torruella G, Suga H, Riutort M, Pereto J, Ruiz-Trillo I (2009) The evolutionary history of lysine biosynthesis pathways within eukaryotes. J Mol Evol 69:240-248
106. Richards TA, Soanes DM, Foster PG, Leonard G, Thornton CR, Talbot NJ (2009) Phylogenomic analysis demonstrates a pattern of rare and ancient horizontal gene transfer between plants and fungi. Plant Cell 21:1897-1911
107. Goulas T, Arolas JL, Gomis-Ruth FX (2011) Structure, function and latency regulation of a bacterial enterotoxin potentially derived from a mammalian adamalysin/ADAM xenolog. Proc Natl Acad Sci USA 108:1856-1861