Phylogenomic analysis of glycogen branching and debranching enzymatic duo

BMC Evolutionary Biology

Volumn 14, Issue 1, 2014, Pages

  Zmasek, Christian M ^a   Godzik, Adam ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

AGL; Branching; Debranching; GBE1; GlgB; GlgX; Glycogen; Glycogen storage disease; Starch; TreX

Indexed keywords

ENZYME ACTIVITY; EUKARYOTE; GENOMICS; PHYLOGENETICS; PHYLOGENY; STARCH; TAXONOMY;

1,4 ALPHA GLUCAN BRANCHING ENZYME; GLYCOGEN; STARCH;

ANIMAL; BACTERIA; CLASSIFICATION; ENZYMOLOGY; EUKARYOTE; GENETICS; GLYCOGEN STORAGE DISEASE; HUMAN; METABOLISM; MOLECULAR EVOLUTION; PHYLOGENY; PLANT;

1,4-ALPHA-GLUCAN BRANCHING ENZYME; ANIMALS; BACTERIA; EUKARYOTA; EVOLUTION, MOLECULAR; GLYCOGEN; GLYCOGEN STORAGE DISEASE; HUMANS; PHYLOGENY; PLANTS; STARCH;

EID: 84910636827     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/s12862-014-0183-2     Document Type: Article

References (69)

1. Voet D, Voet JG: Biochemistry. In 4th edition. New York: Wiley; 2010.
2. Glycogen: a Trojan horse for neurons. PJ Magistretti, I Allaman, Nat Neurosci 2007 10 11 1341 1342 10.1038/nn1107-1341 17965648
3. From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule. SG Ball, MK Morell, Annu Rev Plant Biol 2003 54 207 233 10.1146/annurev.arplant.54.031902.134927 14502990
4. The fractal structure of glycogen: a clever solution to optimize cell metabolism. R Meléndez, E Meléndez-Hevia, EI Canela, Biophys J 1999 77 3 1327 1332 10.1016/S0006-3495(99)76982-1 10465745
5. Glycogen and its metabolism. PJ Roach, Curr Mol Med 2002 2 101 120 10.2174/1566524024605761 11949930
6. Glycogen and its metabolism: some new developments and old themes. PJ Roach, A Depaoli-Roach, TD Hurley, VS Tagliabracci, Biochem J 2012 441 763 787 10.1042/BJ20111416 22248338
7. Regulation of glycogen metabolism in yeast and bacteria. W Wilson, PJ Roach, M Montero, E Baroja-Fernández, FJ Muñoz, G Eydallin, AM Viale, J Pozueta-Romero, FEMS Microbiol Rev 2010 34 952 985 20412306
8. Glycogen branches out: new perspectives on the role of glycogen metabolism in the integration of metabolic pathways. CC Greenberg, MJ Jurczak, AM Danos, MJ Brady, Am J Physiol Endocrinol Metab 2006 291 1 E8 10.1152/ajpendo.00652.2005 16478770
9. Isolation and nucleotide sequence of human liver glycogen debranching enzyme mRNA: identification of multiple tissue-specific isoforms. Y Bao, BZ Yang, TL Dawson, YT Chen, Gene 1997 197 389 398 10.1016/S0378-1119(97)00291-6 9332391
10. Monophyly of Rhizaria and Multigene Phylogeny of unicellular Bikonts. F Burki, J Pawlowski, Mol Biol Evol 2006 23 10 1922 1930 10.1093/molbev/msl055 16829542
11. Evolution: revisiting the root of the eukaryote tree. AJ Roger, AGB Simpson, Curr Biol 2009 19 165 R167 10.1016/j.cub.2008.12.032 19243692
12. Multigene phylogeny of choanozoa and the origin of animals. K Shalchian-Tabrizi, M Minge, M Espelund, R Orr, T Ruden, KS Jakobsen, T Cavalier-Smith, PLoS One 2008 3 2098 10.1371/journal.pone.0002098 18461162
13. Glycogen branching enzyme (GBE1) mutation causing equine glycogen storage disease IV. TL Ward, SJ Valberg, DL Adelson, CA Abbey, MM Binns, JR Mickelson, Mamm Genome 2004 15 7 570 577 10.1007/s00335-004-2369-1 15366377
14. The carbohydrate-active enzymes database (CAZy) in 2013. V Lombard, H Golaconda Ramulu, E Drula, PM Coutinho, B Henrissat, Nucleic Acids Res 2014 42 D1 490 D495 10.1093/nar/gkt1178 24270786
15. Structural basis for branching-enzyme activity of glycoside hydrolase family 57: Structure and stability studies of a novel branching enzyme from the hyperthermophilic archaeon Thermococcus Kodakaraensis KOD1. CR Santos, CCC Tonoli, DM Trindade, C Betzel, H Takata, T Kuriki, T Kanai, T Imanaka, RK Arni, MT Murakami, Proteins 2011 79 2 547 557 10.1002/prot.22902 21104698
16. Thermus thermophilus glycoside hydrolase family 57 branching enzyme. M Palomo, T Pijning, T Booiman, JM Dobruchowska, J van der Vlist, S Kralj, A Planas, K Loos, JP Kamerling, BW Dijkstra, MJ van der Maarel, L Dijkhuizen, H Leemhuis, J Biol Chem 2011 286 5 3520 3530 10.1074/jbc.M110.179515 21097495
17. The Pfam protein families database. M Punta, PC Coggill, RY Eberhardt, J Mistry, J Tate, C Boursnell, N Pang, K Forslund, G Ceric, J Clements, A Heger, L Holm, EL Sonnhammer, SR Eddy, A Bateman, RD Finn, Nucleic Acids Res 2012 40 Database issue 290 D301 10.1093/nar/gkr1065 22127870
18. Three-dimensional structure of Pseudomonas isoamylase at 2.2 Å resolution. Y Katsuya, Y Mezaki, M Kubota, Y Matsuura, J Mol Biol 1998 281 5 885 897 10.1006/jmbi.1998.1992 9719642
19. Refined molecular structure of pig pancreatic α-amylase at 2 · 1 Å resolution. SB Larson, A Greenwood, D Cascio, J Day, A McPherson, J Mol Biol 1994 235 5 1560 1584 10.1006/jmbi.1994.1107 8107092
20. Three orthologs in rice, Arabidopsis, and Populus encoding starch branching enzymes (SBEs) are different from other SBE gene families in plants. Y Han, F-J Sun, S Rosales-Mendoza, SS Korban, Gene 2007 401 123 130 10.1016/j.gene.2007.06.026 17698298
21. Coordinate regulation of glycogen metabolism in the yeast Saccharomyces cerevisiae. Induction of glycogen branching enzyme. VJ Thon, C Vigneron-Lesens, T Marianne-Pepin, J Montreuil, A Decq, C Rachez, SG Ball, JF Cannon, J Biol Chem 1992 267 21 15224 15228 1634552
22. Biosynthesis of bacterial glycogen. Primary structure of Escherichia coli 1,4-alpha-D-glucan:1,4-alpha-D-glucan 6-alpha-D-(1, 4-alpha-D-glucano)-transferase as deduced from the nucleotide sequence of the glg B gene. PA Baecker, E Greenberg, J Preiss, J Biol Chem 1986 261 19 8738 8743 3013861
23. The X-ray crystallographic structure of Escherichia coli branching enzyme. MC Abad, K Binderup, J Rios-Steiner, RK Arni, J Preiss, JH Geiger, J Biol Chem 2002 277 44 42164 42170 10.1074/jbc.M205746200 12196524
24. Crystal structure of full-length Mycobacterium tuberculosis H37Rv glycogen branching enzyme: insights of N-terminal beta-sandwich in substrate specificity and enzymatic activity. K Pal, S Kumar, S Sharma, SK Garg, MS Alam, HE Xu, P Agrawal, K Swaminathan, J Biol Chem 2010 285 27 20897 20903 10.1074/jbc.M110.121707 20444687
25. Crystal structure of the branching enzyme I (BEI) from Oryza sativa L with implications for catalysis and substrate binding. J Noguchi, K Chaen, NT Vu, T Akasaka, H Shimada, T Nakashima, A Nishi, H Satoh, T Omori, Y Kakuta, M Kimura, Glycobiology 2011 21 8 1108 1116 10.1093/glycob/cwr049 21493662
26. Cloning and sequencing of a cluster of genes encoding novel enzymes of trehalose biosynthesis from thermophilic archaebacterium Sulfolobus acidocaldarius. K Maruta, H Mitsuzumi, T Nakada, M Kubota, H Chaen, S Fukuda, T Sugimoto, M Kurimoto, Biochim Biophys Acta 1996 1291 3 177 181 10.1016/S0304-4165(96)00082-7 8980629
27. Reaction kinetics of substrate transglycosylation catalyzed by TreX of sulfolobus solfataricus and effects on glycogen breakdown. DHD Nguyen, J-T Park, J-H Shim, PL Tran, EF Oktavina, TLH Nguyen, S-J Lee, C-S Park, D Li, S-H Park, D Stapleton, JS Lee, KH Park, J Bacteriol 2014 196 11 1941 1949 10.1128/JB.01442-13 24610710
28. TreX from sulfolobus solfataricus ATCC 35092 displays isoamylase and 4-alpha-glucanotransferase activities. H-S Park, J-T Park, H-K Kang, H Cha, D-S Kim, J-W Kim, K-H Park, Biosci Biotechnol Biochem 2007 71 5 1348 1352 10.1271/bbb.70016 17485831
29. Structural insight into the bifunctional mechanism of the glycogen-debranching enzyme TreX from the archaeon sulfolobus solfataricus. E-J Woo, S Lee, H Cha, J-T Park, S-M Yoon, H-N Song, K-H Park, J Biol Chem 2008 283 42 28641 28648 10.1074/jbc.M802560200 18703518
30. Identification of the catalytic residues of bifunctional glycogen debranching enzyme. A Nakayama, K Yamamoto, S Tabata, J Biol Chem 2001 276 31 28824 28828 10.1074/jbc.M102192200 11375985
31. Analysis of the Escherichia coli glycogen gene cluster suggests that catabolic enzymes are encoded among the biosynthetic genes. T Romeo, A Kumar, J Preiss, Gene 1988 70 2 363 376 10.1016/0378-1119(88)90208-9 2975249
32. Structural rationale for the short branched substrate specificity of the glycogen debranching enzyme GlgX. H-N Song, T-Y Jung, J-T Park, B-C Park, PK Myung, W Boos, E-J Woo, K-H Park, Proteins 2010 78 8 1847 1855 20187119
33. Emergence of diverse biochemical activities in evolutionarily conserved structural scaffolds of proteins. V Anantharaman, L Aravind, EV Koonin, Curr Opin Chem Biol 2003 7 12 20 10.1016/S1367-5931(02)00018-2 12547421
34. One fold with many functions: the evolutionary relationships between TIM barrel families based on their sequences, structures and functions. N Nagano, C Orengo, JM Thornton, J Mol Biol 2002 321 741 765 10.1016/S0022-2836(02)00649-6 12206759
35. Coordinate genetic regulation of glycogen catabolism and biosynthesis in Escherichia coli via the CsrA gene product. H Yang, MY Liu, T Romeo, J Bacteriol 1996 178 4 1012 1017 8576033
36. Starch granule biosynthesis in Arabidopsis is abolished by removal of all debranching enzymes but restored by the subsequent removal of an endoamylase. S Streb, T Delatte, M Fau-Umhang, M Umhang, S Fau-Eicke, S Eicke, M Fau-Schorderet, M Schorderet, D Fau-Reinhardt, D Reinhardt, SC Fau-Zeeman, SC Zeeman, Plant Cell 2008 20 1040 4651 10.1105/tpc.108.063487
37. Clinical and genetic variability of glycogen storage disease type IIIa: seven novel AGL gene mutations in the Mediterranean area. S Lucchiari, I Fogh, A Prelle, R Parini, N Bresolin, D Melis, L Fiori, G Scarlato, GP Comi, Am J Med Genet 2002 109 3 183 190 10.1002/ajmg.10347 11977176
38. http://www.ncbi.nlm.nih.gov/books/NBK26372/ Glycogen Storage Disease Type III: Glycogen Storage Disease Type III.
39. Familial cirrhosis of the liver with storage of abnormal glycogen. DH Andersen, Lab Invest 1956 5 1 11 20 13279125
40. http://www.ncbi.nlm.nih.gov/books/NBK115333/ Glycogen Storage Disease Type IV: Glycogen Storage Disease Type IV.
41. The variable presentations of glycogen storage disease type IV: a review of clinical, enzymatic and molecular studies. SW Moses, R Parvari, Curr Mol Med 2002 2 2 177 188 10.2174/1566524024605815 11949934
42. Non-lethal congenital hypotonia due to glycogen storage disease type IV. TA Burrow, RJ Hopkin, KE Bove, L Miles, BL Wong, A Choudhary, D Bali, SC Li, Y-T Chen, Am J Med Genet A 2006 140A 8 878 882 10.1002/ajmg.a.31166
43. Glycogen branching enzyme deficiency in adult polyglucosan body disease. C Bruno, S Servidei, S Shanske, G Karpati, S Carpenter, D McKee, RJ Barohn, M Hirano, Z Rifai, S Dimauro, Ann Neurol 1993 33 1 88 93 10.1002/ana.410330114 8494336
44. A complex rearrangement in GBE1 causes both perinatal hypoglycemic collapse and late-juvenile-onset neuromuscular degeneration in glycogen storage disease type IV of Norwegian forest cats. JC Fyfe, RL Kurzhals, MG Hawkins, P Wang, N Yuhki, U Giger, TJ Van Winkle, ME Haskins, DF Patterson, PS Henthorn, Mol Genet Metab 2007 90 4 383 392 10.1016/j.ymgme.2006.12.003 17257876
45. Comparison of starch-branching enzyme genes reveals evolutionary relationships among isoforms. Characterization of a gene for starch-branching enzyme IIa from the wheat genome donor Aegilops tauschii. S Rahman, A Regina, Z Li, Y Mukai, M Yamamoto, B Kosar-Hashemi, S Abrahams, MK Morell, Plant Physiol 2001 125 3 1314 1324 10.1104/pp.125.3.1314 11244112
46. Molecular evolution accompanying functional divergence of duplicated genes along the plant starch biosynthesis pathway. O Nougue, J Corbi, S Ball, D Manicacci, M Tenaillon, BMC Evol Biol 2014 14 1 103 10.1186/1471-2148-14-103 24884572
47. Starch: its metabolism, evolution, and biotechnological modification in plants. SC Zeeman, J Kossmann, AM Smith, Annu Rev Plant Biol 2010 61 1 209 234 10.1146/annurev-arplant-042809-112301 20192737
48. New knowledge from old: in silico discovery of novel protein domains in Streptomyces coelicolor. C Yeats, S Bentley, A Bateman, BMC Microbiol 2003 3 3 10.1186/1471-2180-3-3 12625841
49. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. F Ronquist, M Teslenko, P van der Mark, DL Ayres, A Darling, S Hohna, B Larget, L Liu, MA Suchard, JP Huelsenbeck, Syst Biol 2012 61 3 539 542 10.1093/sysbio/sys029 22357727
50. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. K Katoh, DM Standley, Mol Biol Evol 2013 30 4 772 780 10.1093/molbev/mst010 23329690
51. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. HA Schmidt, K Strimmer, M Vingron, A von Haeseler, Bioinformatics 2002 18 3 502 504 10.1093/bioinformatics/18.3.502 11934758
52. Fast and accurate phylogeny reconstruction algorithms based on the minimum-evolution principle. R Desper, O Gascuel, J Comput Biol 2002 9 5 687 705 10.1089/106652702761034136 12487758
53. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. S Guindon, O Gascuel, Syst Biol 2003 52 5 696 704 10.1080/10635150390235520 14530136
54. Data from: Phylogenomic Analysis of Glycogen Branching and Debranching Enzymatic Duo. CM Zmasek, A Godzik, Dryad Data Repository 2014
55. RIO: analyzing proteomes by automated phylogenomics using resampled inference of orthologs. CM Zmasek, SR Eddy, BMC Bioinformatics 2002 3 14 10.1186/1471-2105-3-14 12028595
56. https://sites.google.com/site/cmzmasek/home/software/forester forester: software libraries for evolutionary biology and comparative genomics research.
57. A simple algorithm to infer gene duplication and speciation events on a gene tree. CM Zmasek, SR Eddy, Bioinformatics 2001 17 9 821 828 10.1093/bioinformatics/17.9.821 11590098
58. Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. DC Price, CX Chan, HS Yoon, EC Yang, H Qiu, APM Weber, R Schwacke, J Gross, NA Blouin, C Lane, A Reyes-Prieto, DG Durnford, JA Neilson, BF Lang, G Burger, JM Steiner, W Löffelhardt, JE Meuser, MC Posewitz, S Ball, MC Arias, B Henrissat, PM Coutinho, SA Rensing, A Symeonidi, H Doddapaneni, BR Green, VD Rajah, J Boore, D Bhattacharya, Science 2012 335 6070 843 847 10.1126/science.1213561 22344442
59. Diversity and evolutionary history of plastids and their hosts. PJ Keeling, Am J Bot 2004 91 10 1481 1493 10.3732/ajb.91.10.1481 21652304
60. Signal conflicts in the phylogeny of the primary photosynthetic eukaryotes. P Deschamps, D Moreira, Mol Biol Evol 2009 26 12 2745 2753 10.1093/molbev/msp189 19706725
61. Aggregative multicellularity evolved independently in the eukaryotic supergroup Rhizaria. MW Brown, M Kolisko, JD Silberman, AJ Roger, Current Biol: CB 2012 22 12 1123 1127 10.1016/j.cub.2012.04.021
62. Distinct mutations in the glycogen debranching enzyme found in glycogen storage disease type III lead to impairment in diverse cellular functions. A Cheng, M Zhang, M Okubo, K Omichi, AR Saltiel, Hum Mol Genet 2009 18 11 2045 2052 10.1093/hmg/ddp128 19299494
63. Surprising complexity of the ancestral apoptosis network. CM Zmasek, Q Zhang, Y Ye, A Godzik, Genome Biol 2007 8 10 226 10.1186/gb-2007-8-10-r226 17958905
64. Accelerated Profile HMM Searches. SR Eddy, PLoS Comput Biol 2011 7 10 1002195 10.1371/journal.pcbi.1002195 22039361
65. ProbCons: probabilistic consistency-based multiple sequence alignment. CB Do, MS Mahabhashyam, M Brudno, S Batzoglou, Genome Res 2005 15 2 330 340 10.1101/gr.2821705 15687296
66. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. S Whelan, N Goldman, Mol Biol Evol 2001 18 5 691 699 10.1093/oxfordjournals.molbev.a003851 11319253
67. ProtTest: selection of best-fit models of protein evolution. F Abascal, R Zardoya, D Posada, Bioinformatics 2005 21 9 2104 2105 10.1093/bioinformatics/bti263 15647292
68. phyloXML: XML for evolutionary biology and comparative genomics. M Han, CM Zmasek, BMC Bioinformatics 2009 10 1 356 10.1186/1471-2105-10-356 19860910
69. A 100%-complete sequence reveals unusually simple genomic features in the hot-spring red alga Cyanidioschyzon merolae. H Nozaki, H Takano, O Misumi, K Terasawa, M Matsuzaki, S Maruyama, K Nishida, F Yagisawa, Y Yoshida, T Fujiwara, S Takio, K Tamura, SJ Chung, S Nakamura, H Kuroiwa, K Tanaka, N Sato, T Kuroiwa, BMC Biol 2007 5 28 10.1186/1741-7007-5-28 17623057