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Molecular analysis of glyceraldehyde-3-phosphate dehydrogenase in Trypanoplasma borelli: an evolutionary scenario of subcellular compartmentation in kinetoplastida.

Bibliographic reference Wiemer, E A ; Hannaert, Véronique ; van den IJssel, P R ; Van Roy, Joris ; Opperdoes, Frederik ; et. al. Molecular analysis of glyceraldehyde-3-phosphate dehydrogenase in Trypanoplasma borelli: an evolutionary scenario of subcellular compartmentation in kinetoplastida.. In: Journal of molecular evolution, Vol. 40, no. 4, p. 443-54 (1995)
Permanent URL http://hdl.handle.net/2078.1/26849
  1. Alefounder PR, Perham RN (1989) Identification, molecular cloning and sequence analysis of a gene cluster encoding the Class II fructose 1,6-bisphosphate aldolase, 3-phosphoglycerate kinase and a putative second glyceraldehyde 3-phosphate dehydrogenase of Escherichia coli. Mol Microbiol 3:723?732
  2. Alexander K, Parsons M (1991) A phosphoglycerate kinase-like molecule localized to glycosomal microbodies: evidence that the topogenic signal is not at the C-terminus. Mol Biochem Parasitol 46: 1?10
  3. Blattner J, Swinkels BW, Dorsam H, Prospero T, Subramani S, Clayton C (1992) Glycosome assembly in trypanosomes: variations in the acceptable degeneracy of a COOH-terminal microbody targeting signal. J Cell Biol 119:1129?1136
  4. Borst P, Swinkels BW (1989) The evolutionary origin of glycosomes; how glycolysis moved from cytosol to organelle. In: Grunberg-Manago M, Clark BFC, Zachau HG (eds) Evolutionary tinkering in gene expression. Plenum Publishing Corporation, pp 163?174
  5. Branlant G, Branlant C (1985) Nucleotide sequence of the Escherichia coli gap gene. Different evolutionary behaviour of the NAD+-binding domain and of the catalytic domain of D-glyceraldehyde-3-phosphate dehydrogenase. Eur J Biochem 150:61?66
  6. Brun R, Schönenberger M (1979) Cultivation and in vitro cloning of procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Acta Trop (Basel) 36:289?292
  7. Callens M, Kuntz DA, Opperdoes FR (1991) Characterization of pyruvate kinase from Trypanosoma brucei and its role in the regulation of carbohydrate metabolism. Mol Biochem Parasitol 47:19?30
  8. Cavalier-Smith T (1990) Symbiotic origin of peroxisomes. In: Nardon P, Gianinazii-Pecurson V, Grenier AM, Margulis L, Smith DC (eds) Endocytobiology IV. pp 515?520
  9. Chen J-H, Gibson JL, McCue LA, Tabita FR (1991) Identification, expression, and deduced primary structure of transketolase and other enzymes encoded within the form II carbon dioxide fixation operon of Rhodobacter sphaeroides. J Biol Chem 266: 20447?20452
  10. Conway T, Sewell GW, Ingram LO (1987) Glyceraldehyde-3-phosphate dehydrogenase gene from Zymomonas mobilis: cloning, sequencing, and identification of promoter region. J Bacteriol 169: 5653?5662
  11. Doolittle RF, Feng DF, Anderson KL, Alberro MR (1990) A naturally occurring horizontal gene transfer from a eukaryote to a prokaryote. J Mol Evol 31:383?388
  12. Efron B (1982) The jack-knife, the bootstrap and other resampling plans. Society for Industrial and Applied Mathematics, Philadelphia
  13. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783?791
  14. Felsenstein J (1993) PHYLIP manual, version 3.5
  15. Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279?284
  16. Fernandez AP, Nelson K, Beverley SM (1993) Evolution of nuclear ribosomal RNAs in kinetoplastid protozoa: perspectives on the age and origins of parasitism. Proc Natl Acad Sci USA 90:11608?11612
  17. Fothergill-Gilmore LA, Michels PAM (1993) Evolution of glycolysis. Progr Biophys Mol Biol 59:105?235
  18. Gilbert DG (1993) ReadSeq manual
  19. Goudot-Crozel V, Caillol D, Djabali M, Dessein AJ (1989) The major parasite surface antigen associated with human resistance to schistosomiasis is a 37 kD glyceraldehyde-3P-dehydrogenase. J Exp Med 170:2065?2080
  20. Gould SJ, Keller GA, Hosken N, Wilkinson J, Subramani S (1989) A conserved tripeptide sorts proteins to peroxisomes. J Cell Biol 108: 1657?1664
  21. Harris JI, Perham RN (1968) Glyceraldehyde 3-phosphate dehydrogenase from pig muscle. Nature 219:1025?1028
  22. Hannaert V, Blaauw M, Kohl L, Allert S, Opperdoes FR, Michels PAM (1992) Molecular analysis of the cytosolic and glycosomal glyceraldehyde-3-phosphate dehydrogenase in Leishmania mexicana. Mol Biochem Parasitol 55:115?126
  23. Hannaert V, Michels PAM (1994) Structure, function and biogenesis of glycosomes in Kinetoplastida. J Bioenerg Biomembr 20:205?212
  24. Hart DT, Opperdoes FR (1984) The occurrence of glycosomes (microbodies) in the promastigote stage of four major Leishmania species. Mol Biochem Parasitol 13:159?172
  25. Hasegawa M, Fujiwara M (1993) Relative efficiencies of the maximum likelihood, maximum parsimony, and neighbor-joining methods for estimating protein phylogeny. Mol Phylogenet Evol 2:1?5
  26. Hecht RM, Garza A, Lee Y-H, Miller MD, Pisegna MA (1989) Nucleotide sequence of the glyceraldehyde-3-phosphate dehydrogenase gene from Thermus aquaticus YT1. Nucleic Acids Res 17:10?23
  27. Holland JP, Holland MJ (1979) The primary structure of a glyceraldehyde-3-phosphate dehydrogenase gene from Saccharomyces cerevisiae. J Biol Chem 254:9839?9845
  28. Keegan FP, Blum JJ (1993) Incorporation of label from acetate and laurate into mannan of Leishmania donovani via the glyoxylate cycle. J Euk Microbiol 40:730?732
  29. Kendall G, Wilderspin AWF, Ashall F, Miles MA, Kelly JM (1990) Trypanosoma cruzi glycosomal glyceraldehyde-3-phosphate dehydrogenase does not conform to the ?hotspot? model of topogenesis. EMBO J 9:2751?2758
  30. Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge.
  31. Kohl L, Callens M, Wierenga RK, Opperdoes FR, Michels PAM (1994) Triosephosphate isomerase of Leishmania mexicana mexicana. Cloning and characterization of the gene, overexpression in Escherichia coli and analysis of the protein. Eur J Biochem 220: 331?338
  32. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680?685
  33. Lambeir A-M, Loiseau AM, Kuntz DA, Vellieux FM, Michels PAM, Opperdoes FR (1991) The cytosolic and glycosomal glyceraldehyde-3-phosphate dehydrogenase from T. brucei: kinetic properties and comparison with homologous enzymes. Eur J Biochem 198: 429?435
  34. Le Blancq SM, Swinkels BW, Gibson WC, Borst P (1988) Evidence for gene conversion between the phosphoglycerate kinase genes of Trypanosoma brucei. J Mol Biol 200:439?447
  35. Marchand M, Kooystra U, Wierenga RK, Lambeir A-M, Van Beeumen J, Opperdoes FR, Michels PAM (1989) Glucosephosphate isomerase from Trypanosoma brucei. Cloning and characterization of the gene and analysis of the enzyme. Eur J Biochem 184:455?464
  36. Markos A, Miretsky A, Müller M (1993) A glyceraldehyde-3-phosphate dehydrogenase with eubacterial features in the amitochondriate eukaryote Trichomonas vaginalis. J Mol Evol 37:631?643
  37. Martin W, Cerff R (1986) Prokaryotic features of a nucleus-encoded enzyme. cDNA sequences for chloroplast and cytosolic glyceraldehyde-3-phosphate dehydrogenases from mustard (Sinapis alba). Eur J Biochem 159:323?331
  38. Martin W, Brinkmann H, Savona C, Cerff R (1993) Evidence for a chimaeric nature of nuclear genomes: eubacterial origin of eukaryotic glyceraldehyde-3-phosphate dehydrogenase genes. Proc Natl Acad Sci USA 90:8692?8696
  39. Martinez P, Martin W, Cerff R (1989) Structure, evolution and anaerobic regulation of a nuclear gene encoding cytosolic glyceraldehyde-3-phosphate dehydrogenase from maize. J Mol Biol 208:551?565
  40. McLaughlin PJ, Dayhoff MO (1973) Eukaryotic evolution: a view based on cyrochrome C sequence data. J Mol Evol 2:99?116
  41. Michels PAM, Poliszczak A, Osinga KA, Misset O, Van Beeumen J, Wieringa RK, Borst P, Opperdoes FR (1986) Two tandemly linked genes code for the glycosomal glyceraldehyde-phosphate dehydrogenase in Trypanosoma brucei. EMBO J 5:1049?1056
  42. Michels PAM, Marchand M, Kohl L, Allert S, Wierenga RK, Opperdoes FR (1991) The cytosolic and glycosomal isoenzymes of glyceraldehyde-3-phosphate dehydrogenase in Trypanosoma brucei have a distant evolutionary relationship. Eur J Biochem 198:421?428
  43. Michels PAM, Opperdoes FR (1991) The evolutionary origin of glycosomes. Parasitol Today 7:105?109
  44. Michels PAM, Hannaert V (1994) The evolution of kinetoplastid glycosomes. J Bioenerg Biomembr 26:213?219
  45. Misset O, Opperdoes FR (1984) Simultaneous purification of hexokinase, class-I fructose-bisphosphate aldolase, triosephosphate isomerase and phosphoglycerate kinase from Trypanosoma brucei. Eur J Biochem 144:475?483
  46. Misset O, Van Beeumen J, Lambeir AM, Van Der Meer R, Opperdoes FR (1987) Glyceraldehyde-phosphate dehydrogenase from Trypanosoma brucei: comparison of the glycosomal and cytosolic isoenzymes. Eur J Biochem 162:501?507
  47. Opperdoes FR, Borst P (1977) Localization of nine glycolytic enzymes in a microbody-like organelle in Trypanosoma brucei: the glycosome. FEBS Lett 80:360?364
  48. Opperdoes FR (1987) Compartmentation of carbohydrate metabolism in trypanosomes. Ann Rev Microbiol 41:127?151
  49. Opperdoes FR, Nohynkova E, Van Schaftingen E, Lambeir A-M, Veenhuis M, Van Roy J (1988) Demonstration of glycosomes (microbodies) in the Bodonid flagellate Trypanoplasma borelli (Protozoa, Kinetoplastida). Mol Biochem Parasitol 30:155?164
  50. Osinga KA, Swinkels BW, Gibson WC, Borst P, Veeneman GH, Van Boom JH, Michels PAM, Opperdoes FR (1985) Topogenesis of microbody enzymes: a sequence comparison of the genes for the glycosomal (microbody) and cytosolic phosphoglycerate kinases of Trypanosoma brucei. EMBO J 4:3811?3817
  51. Punt P, Dingemanse MA, Jacobs-Meijsing BJM, Pouwels PH, Van den Hondel CAMJJ (1988) Isolation and characterization of the glyceraldehyde-3-phosphate dehydrogenase gene of Aspergillus nidulans. Gene 69:49?57
  52. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406?425
  53. Schultes V, Deutzmann R, Jaenicke R (1990) Complete amino-acid sequence of glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic eubacterium Thermotoga maritima. Eur J Biochem 192:25?31
  54. Shih M-C, Heinrich PC, Goodman HM (1991) Cloning and chromosomal mapping of nuclear genes encoding chloroplast and cytosolic glyceraldehyde-3-phosphate dehydrogenase from Arabidopsis thaliana. Gene 104:133?138
  55. Sogin ML, Elwood HJ, Gunderson JH (1986) Evolutionary diversity of eukaryotic small-subunit rRNA genes. Proc Natl Acad Sci USA 83:1383?1387
  56. Sommer JM, Cheng Q-L, Keller GA, Wang CC (1992) In vivo import of firefly luciferase into the glycosomes of Trypanosoma brucei and mutational analysis of the C-terminal targeting signal. Mol Biol Cell 3:749?759
  57. Stein S, Bohlen P, Stone J, Dairman W, Udenfriend S (1973) Amino-acid analysis with fluorescamine at the picomole level. Arch Biochem Biophys 155:203?212
  58. Stone EM, Rothblum KN, Alevy MC, Koo TM, Schwartz RJ (1985) Complete sequence of the chicken glyceraldehyde-3-phosphate dehydrogenase gene. Proc Natl Acad Sci USA 82:1628?1642
  59. Swinkels BW, Evers R, Borst P (1988) The topogenic signal of the glycosomal (microbody) phosphoglycerate kinase of Crithidia fasciculata resides in a carboxy-terminal extension. EMBO J 7:1159?1165
  60. Swinkels BW, Loiseau A, Opperdoes FR, Borst P (1992) A phosphoglycerate kinase-related gene conserved between Trypanosoma brucei and Crithidia fasciculata. Mol Biochem Parasitol 50:69?78
  61. Tso JY, Sun X-H, Kao T-H, Reece KS, Wu R (1985) Isolation and characterization of rat and human glyceraldehyde-3-phosphate dehydrogenase cDNAs: genomic complexity and molecular evolution of the gene. Nucleic Acids Res 13:2485?2502
  62. Van der Ploeg LHT, Bernards A, Rijsewijk FAM, Borst P (1982) Characterization of the DNA duplication-transposition that controls the expression of two genes for variant surface glycoproteins in Trypanosoma brucei. Nucleic Acids Res 10:539?609
  63. Vellieux FMD, Hajdu J, Verlinde CLMJ, Groendijk H, Read RJ, Greenhough TJ, Campbell JW, Kalk KH, Littlechild JA, Watson HC, Hol WGJ (1993) Structure of glycosomal glyceraldehyde-3-phosphate dehydrogenase from Trypanosoma brucei determined from Laue data. Proc Natl Acad Sci USA 90:2355?2359
  64. Viaene A, Dhaese P (1989) Sequence of the glyceraldehyde-3-phosphate dehydrogenase gene from Bacillus subtilis. Nucleic Acids Res 17:12?51
  65. Visser N, Opperdoes FR (1980) Glycolysis in Trypanosoma brucei. Eur J Biochem 103:623?632
  66. Wierenga RK, Swinkels B, Michels PAM, Osinga K, Misset O, Van Beeumen J, Gibson WC, Postma JPM, Borst P, Opperdoes FR, Hol WGJ (1987) Common elements on the surface of glycolytic enzymes from Trypanosoma brucei may serve as topogenic signals for import into glycosomes. EMBO J 6:215?221