Globin gene family evolution and functional diversification in annelids

FEBS Journal

Volumn 274, Issue 10, 2007, Pages 2641-2652

  Bailly, Xavier ^a,b   Chabasse, Christine ^a   Hourdez, Stéphane ^a   Dewilde, Sylvia ^c   Martial, Sophie ^a   Moens, Luc ^c   Zal, Franck ^a  

^a STATION BIOLOGIQUE DE ROSCOFF   (France)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Annelid; Dehaloperoxidase; Extracellular globin; Intracellular globin; Myoglobin

Indexed keywords

HEMOGLOBIN;

AMINO ACID SEQUENCE; ANNELID WORM; ARTHROPOD; ARTICLE; GENE FUNCTION; GENE STRUCTURE; GENETIC VARIABILITY; MOLECULAR EVOLUTION; MOLLUSC; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; SEQUENCE HOMOLOGY;

ALVINELLA POMPEJANA; AMPHITRITE ORNATA; ANNELIDA; ARENICOLA MARINA; ARTHROPODA; GLYCERA DIBRANCHIATA; MOLLUSCA;

EID: 34247576294     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.05799.x     Document Type: Article

References (52)

1. Hardison R (1998) Hemoglobins from bacteria to man: evolution of different patterns of gene expression. J Exp Biol 201, 1099 1117.
2. Vinogradov SN. et al. (2005) Three globin lineages belonging to two structural classes in genomes from the three kingdoms of life. Proc Natl Acad Sci USA 102, 11385 11389.
3. Goodman M. et al. (1988) An evolutionary tree for invertebrate globin sequences. J Mol Evol 27, 236 249.
4. Moens L. et al. (1996) Globins in nonvertebrate species: dispersal by horizontal gene transfer and evolution of the structure-function relationships. Mol Biol Evol 13, 324 333.
5. Suzuki T Imai K (1998) Evolution of myoglobin. Cell Mol Life Sci 54, 979 1004.
6. Wittenberg JB (1970) Myoglobin-facilitated oxygen diffusion: role of myoglobin in oxygen entry into muscle. Physiol Rev 50, 559 636.
7. Vinogradov SN, Walz DA, Pohajdak B, Moens L, Kapp OH, Suzuki T Trotman CN (1993) Adventitious variability? The amino acid sequences of nonvertebrate globins. Comp Biochem Physiol B 106, 1 26.
8. Weber RE Vinogradov SN (2001) Nonvertebrate hemoglobins: functions and molecular adaptations. Physiol Rev 81, 569 628.
9. Wittenberg BA, Briehl RW Wittenberg JB (1965) Haemoglobins of invertebrate tissues. Nerve haemoglobins of Aphrodite, Aplysia and Halosydna. Biochem J 96, 363 371.
10. Terwilliger RC, Garlick RL Terwilliger NB (1980) Characterization of hemoglobins and myoglobin of Travisia foetida. Comp Biochem Physiol 66B, 261 266.
11. Kleinschmidt T Weber RE (1998) Primary structures of Arenicola marina isomyoglobins: molecular basis for functional heterogeneity. Biochim Biophys Acta 1383, 55 62.
12. Zafar RS, Chow LH, Stern MS, Scully JS, Sharma PR, Vinogradov SN Walz DA (1990) The cDNA sequences encoding two components of the polymeric fraction of the intracellular hemoglobin of Glycera dibranchiata. J Biol Chem 265, 21843 21851.
13. Zafar RS, Chow LH, Stern MS, Vinogradov SN Walz DA (1990) The heterogeneity of the polymeric intracellular hemoglobin of Glycera dibranchiata and the cDNA-derived amino acid sequence of one component. Biochim Biophys Acta 1041, 117 122.
14. Seamonds B, Forster RE Gottlieb AJ (1971) Heterogeneity of the hemoglobin from the common bloodworm Glycera dibranchiata. J Biol Chem 246, 1700 1705.
15. Gotoh T, Shishikura F, Snow JW, Ereifej KI, Vinogradov SN Walz DA (1987) Two globin strains in the giant annelid extracellular haemoglobins. Biochem J 241, 441 445.
16. Bailly X, Jollivet D, Vanin S, Deutsch J, Zal F, Lallier F Toulmond A (2002) Evolution of the sulfide-binding function within the globin multigenic family of the deep-sea hydrothermal vent tubeworm Riftia pachyptila. Mol Biol Evol 19, 1421 1433.
17. Weber RE (1978) Respiratory pigments. In Physiology of Annelids (Mill PJ, ed), pp. 393 446. Academic Press Inc, New York, NY.
18. Hourdez S, Lallier FH, De Cian MC, Green BN, Weber RE Toulmond A (2000) Gas transfer system in Alvinella pompejana (Annelida polychaeta, Terebellida): functional properties of intracellular and extracellular hemoglobins. Physiol Biochem Zool 73, 365 373.
19. Negrisolo E, Pallavicini A, Barbato R, Dewilde S, Ghiretti-Magaldi A, Moens L Lanfranchi G (2001) The evolution of extracellular hemoglobins of annelids, vestimentiferans, and pogonophorans. J Biol Chem 276, 26391 26397.
20. Gotoh O Suzuki T (1990) Molecular assembly and evolution of multi-subunit extracellular annelid hemoglobins. Zool Sci 7, 1 16.
21. Jhiang SM Riggs AF (1989) The structure of the gene encoding chain c of the hemoglobin of the earthworm, Lumbricus terrestris. J Biol Chem 264, 19003 19008.
22. Dewilde S, Van Hauwaert ML, Vinogradov S, Vierstraete A, Vanfleteren J Moens L (2001) Protein and gene structure of a chlorocruorin chain of Eudistylia vancouverii. Biochem Biophys Res Commun 281, 18 24.
23. Bailly X (2003) Evolution de la fonction de liaison du sulfure d'hydrogène par les hémoglobines de Riftia pachyptila, annélide tubicole des sources hydrothermales profondes. Thèse de doctorat, École Pratique des Hautes Etudes et Université Pierre et Marie Curie, Paris VI, France.
24. Dewilde S, Blaxter M, Van Hauwaert ML, Vanfleteren J, Esmans EL, Marden M, Griffon N Moens L (1996) Globin and globin gene structure of the nerve myoglobin of Aphrodite aculeata. J Biol Chem 271, 19865 19870.
25. Chen YP, Woodin SA, Lincoln DE Lovell CR (1996) An unusual dehalogenating peroxidase from the marine terebellid polychaete Amphitrite ornata. J Biol Chem 271, 4609 4612.
26. Roach MP, Chen YP, Woodin SA, Lincoln DE, Lovell CR Dawson JH (1997) Notomastus lobatus chloroperoxidase and Amphitrite ornata dehaloperoxidase both contain histidine as their proximal heme iron ligand. Biochemistry 36, 2197 2202.
27. LaCount MW, Zhang E, Chen YP, Han K, Whitton MM, Lincoln DE, Woodin SA Lebioda L (2000) The crystal structure and amino acid sequence of dehaloperoxidase from Amphitrite ornata indicate common ancestry with globins. J Biol Chem 275, 18712 18716.
28. Strand K, Knapp JE, Bhyravbhatla B Royer WE Jr. (2004) Crystal structure of the hemoglobin dodecamer from Lumbricus erythrocruorin: allosteric core of giant annelid respiratory complexes. J Mol Biol 344, 119 134.
29. Fushitani K, Matsuura MS Riggs AF (1988) The amino acid sequences of chains a, b, and c that form the trimer subunit of the extracellular hemoglobin from Lumbricus terrestris. J Biol Chem 263, 6502 6517.
30. Suzuki T, Kapp OH Gotoh T (1988) Novel S-S loops in the giant hemoglobin of Tylorrhynchus heterochaetus. J Biol Chem 263, 18524 18529.
31. Suzuki T, Takagi T Ohta S (1993) N-terminal amino acid sequences of 440 kDa hemoglobins of the deep-sea tube worms, Lamellibrachia sp.1, Lamellibrachia sp.2 and slender vestimentifera gen. sp. 1 evolutionary relationship with annelid hemoglobins. Zool Sci 10, 141 146.
32. Jhiang SM, Garey JR Riggs AF (1988) Exon-intron organization in genes of earthworm and vertebrate globins. Science 240, 334 336.
33. Keller EB Noon WA (1984) Intron splicing: a conserved internal signal in introns of animal pre-mRNAs. Proc Natl Acad Sci USA 81, 7417 7420.
34. Harris NL Senapathy P (1990) Distribution and consensus of branch point signals in eukaryotic genes: a computerized statistical analysis. Nucleic Acids Res 18, 3015 3019.
35. Dewilde S, Van Hauwaert M-L, Peeters K, Vanfleteren J Moens L (1999) Daphnia pulex didomain hemoglobin: structure and evolution of polymeric hemoglobins and their coding genes. Mol Biol Evol 16, 1208 1218.
36. Manwell C Baker CMA (1988) Magelona haemerythrin: tissue specificity, molecular weights and oxygen equilibria. Comp Biochem Physiol 89B, 453 463.
37. Fushitani K, Ochi O Morimoto H (1982) Purification, characterization, and comparison of extracellular hemoglobins in coelomic fluid and blood vessel plasma of Travisia japonica (Polychaeta, Annelid). Comp Biochem Physiol B 72, 267 273.
38. Freitas TA, Hou S, Dioum EM, Saito JA, Newhouse J, Gonzalez G, Gilles-Gonzalez MA Alam M (2004) Ancestral hemoglobins in Archaea. Proc Natl Acad Sci USA 101, 6675 6680.
39. Zhu H Riggs AF (1992) Yeast flavohemoglobin is an ancient protein related to globins and a reductase family. Proc Natl Acad Sci USA 89, 5015 5019.
40. Andersson JO, Sjogren AM, Davis LA, Embley TM Roger AJ (2003) Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Curr Biol 13, 94 104.
41. Riggs AF (1991) Aspects of the origin and evolution of non-vertebrate hemoglobins. Am Zool 31, 535 545.
42. Williams EJ, Pal C Hurst LD (2000) The molecular evolution of signal peptides. Gene 253, 313 322.
43. Toulmond A 1992) Properties and functions of extracellular heme pigments. In Advances in Comparative and Environmental Physiology (Mangum CP, ed.), Vol. 13, pp 231 256. Springer, New York.
44. Weber RE, Mangum C, Steinman H, Bonaventura C, Sullivan B Bonaventura J (1977) Hemoglobins of two terebellid polychaetes: Enoplobranchus sanguineus and Amphitrite ornata. Comp Biochem Physiol A 56, 179 187.
45. Mangum CP, Woodin BR, Bonaventura C, Sullivan B Bonaventura J (1975) The role of coelomic and vascular hemoglobin in the annelid family terebellidae. Comp Biochem Physiol A 51, 281 294.
46. Allen G (1989) Sequencing of proteins and peptides. In Laboratory Techniques in Biochemistry and Molecular Biology (Burdon RH, Van Knippenberg PH, eds), Vol. 9, pp. 73 104. Elsevier North Holland, Amsterdam.
47. Swank RT Munkres KD (1971) Molecular weight analysis of oligopeptides by electrophoresis in polyacrylamide gel with sodium dodecyl sulfate. Anal Biochem 39, 462 477.
48. Bendtsen JD, Nielsen H, von Heijne G Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340, 783 795.
49. 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.
50. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792 1797.
51. Jones DT, Taylor WR Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8, 275 282.
52. Mount SM (1982) A catalogue of splice junction sequences. Nucleic Acids Res 10, 459 472.