Structural shifts of aldehyde dehydrogenase enzymes were instrumental for the early evolution of retinoid-dependent axial patterning in metazoans

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 1, 2011, Pages 226-231

  Sobreira, Tiago J P ^a   Marlétaz, Ferdinand ^b   Simões Costa, Marcos ^a,c   Schechtman, Deborah ^a   Pereira, Alexandre C ^a   Brunet, Frédéric ^b   Sweeney, Sarah ^d   Pani, Ariel ^e,f   Aronowicz, Jochanan ^f   Lowe, Christopher J ^f   Davidson, Bradley ^d   Laudet, Vincent ^b   Bronner, Marianne ^g   De Oliveira, Paulo S L ^a   Schubert, Michael ^b   Xavier Neto, José ^c  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITÉ DE LYON   (France)

^c LABORATÓRIO NACIONAL DE LUZ SÍNCROTRON   (Brazil)

^d University of Arizona   (United States)

^e UNIVERSITY OF CHICAGO   (United States)

^f STANFORD UNIVERSITY   (United States)

^g CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Aldehyde dehydrogenase phylogeny; Branchiostoma floridae; Ciona intestinalis versus Ciona savignyi; Evolution of retinoic acid signaling; Origins of morphogen dependent signaling

Indexed keywords

ACETALDEHYDE; ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE ISOENZYME 2; RETINAL; RETINOIC ACID;

ARTICLE; ASCIDIACEA; BRANCHIOSTOMA; EUKARYOTE; EVOLUTION; GENE DUPLICATION; GENE EXPRESSION; GENOMICS; METAZOON; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS;

ASCIDIA; BRANCHIOSTOMA FLORIDAE; BRANCHIOSTOMA LANCEOLATUM; CHORDATA; CIONA INTESTINALIS; CIONA SAVIGNYI; EUKARYOTA; INVERTEBRATA; METAZOA; UROCHORDATA;

EID: 78651095017     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1011223108     Document Type: Article

References (37)

1. Seiler N, Eichentopf B (1975) 4-aminobutyrate in mammalian putrescine catabolism. Biochem J 152:201-210.
2. Kikonyogo A, Pietruszko R (1996) Aldehyde dehydrogenase from adult human brain that dehydrogenates gamma-aminobutyraldehyde: Purification, characterization, cloning and distribution. Biochem J 316:317-324.
3. Yoshida A, Rzhetsky A, Hsu LC, Chang C (1998) Human aldehyde dehydrogenase gene family. Eur J Biochem 251:549-557.
4. Campo-Paysaa F, Marlétaz F, Laudet V, Schubert M (2008) Retinoic acid signaling in development: Tissue-specific functions and evolutionary origins. Genesis 46:640-656.
5. Marlétaz F, Holland LZ, Laudet V, Schubert M (2006) Retinoic acid signaling and the evolution of chordates. Int J Biol Sci 2:38-47.
6. Duester G (2008) Retinoic acid synthesis and signaling during early organogenesis. Cell 134:921-931.
7. Simões-Costa MS, Azambuja AP, Xavier-Neto J (2008) The search for non-chordate retinoic acid signaling: Lessons from chordates. J Exp Zoolog B Mol Dev Evol 310:54-72.
8. Theodosiou M, Laudet V, Schubert M (2010) From carrot to clinic: An overview of the retinoic acid signaling pathway. Cell Mol Life Sci 67:1423-1445.
9. Lamb AL, Newcomer ME (1999) The structure of retinal dehydrogenase type II at 2.7 Å resolution: Implications for retinal specificity. Biochemistry 38:6003-6011.
10. Dräger UC, Wagner E, McCaffery P (1998) Aldehyde dehydrogenases in the generation of retinoic acid in the developing vertebrate: A central role of the eye. J Nutr 128(Suppl):4635-4665.
11. Graham CE, Brocklehurst K, Pickersgill RW, Warren MJ (2006) Characterization of retinaldehyde dehydrogenase 3. Biochem J 394:67-75.
12. Lin M, Zhang M, Abraham M, Smith SM, Napoli JL (2003) Mouse retinal dehydrogenase 4 (RALDH4), molecular cloning, cellular expression, and activity in 9-cis-retinoic acid biosynthesis in intact cells. J Biol Chem 278:9856-9861.
13. Niederreither K, Subbarayan V, Dollé P, Chambon P (1999) Embryonic retinoic acid synthesis is essential for earlymouse post-implantation development. Nat Genet 21:444-448.
14. Wang X, Penzes P, Napoli JL (1996) Cloning of a cDNA encoding an aldehyde dehydrogenase and its expression in Escherichia coli. Recognition of retinal as substrate. J Biol Chem 271:16288-16293.
15. Zhao D, et al. (1996) Molecular identification of a major retinoic-acid-synthesizing enzyme, a retinaldehyde-specific dehydrogenase. Eur J Biochem 240:15-22.
16. Klyosov AA (1996) Kinetics and specificity of human liver aldehyde dehydrogenases toward aliphatic, aromatic, and fused polycyclic aldehydes. Biochemistry 35:4457-4467.
17. Moore SA, et al. (1998) Sheep liver cytosolic aldehyde dehydrogenase: The structure reveals the basis for the retinal specificity of class 1 aldehyde dehydrogenases. Structure 6:1541-1551.
18. Steinmetz CG, Xie P, Weiner H, Hurley TD (1997) Structure of mitochondrial aldehyde dehydrogenase: The genetic component of ethanol aversion. Structure 5:701-711.
19. Yoshida A, Hsu LC, Davé V (1992) Retinal oxidation activity and biological role of human cytosolic aldehyde dehydrogenase. Enzyme 46:239-244.
20. Yoshida A, Hsu LC, Yanagawa Y (1993) Biological role of human cytosolic aldehyde dehydrogenase 1: Hormonal response, retinal oxidation and implication in testicular feminization. Adv Exp Med Biol 328:37-44.
21. Duester G (2001) Genetic dissection of retinoid dehydrogenases. Chem Biol Interact 130-132:469-480.
22. Klyosov AA, Rashkovetsky LG, Tahir MK, Keung WM (1996) Possible role of liver cytosolic and mitochondrial aldehyde dehydrogenases in acetaldehyde metabolism. Biochemistry 35:4445-4456.
23. Holland LZ, et al. (2008) The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res 18:1100-1111.
24. Cañestro C, Yokoi H, Postlethwait JH (2007) Evolutionary developmental biology and genomics. Nat Rev Genet 8:932-942.
25. Schubert M, Escriva H, Xavier-Neto J, Laudet V (2006) Amphioxus and tunicates as evolutionary model systems. Trends Ecol Evol 21:269-277.
26. Putnam NH, et al. (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453:1064-1071.
27. Cañestro C, Postlethwait JH, Gonzàlez-Duarte R, Albalat R (2006) Is retinoic acid genetic machinery a chordate innovation? Evol Dev 8:394-406.
28. Skibbe DS, et al. (2002) Characterization of the aldehyde dehydrogenase gene families of Zea mays and Arabidopsis. Plant Mol Biol 48:751-764.
29. Perozich J, Nicholas H, Wang BC, Lindahl R, Hempel J (1999) Relationships within the aldehyde dehydrogenase extended family. Protein Sci 8:137-146.
30. Fujiwara S, Kawamura K (2003) Acquisition of retinoic acid signaling pathway and innovation of the chordate body plan. Zoolog Sci 20:809-818.
31. Niederreither K, McCaffery P, Dräger UC, Chambon P, Dollé P (1997) Restricted expression and retinoic acid-induced downregulation of the retinaldehyde dehydrogenase type 2 (RALDH-2) gene duringmouse development. Mech Dev 62:67-78.
32. Bridgham JT, Ortlund EA, Thornton JW (2009) An epistatic ratchet constrains the direction of glucocorticoid receptor evolution. Nature 461:515-519.
33. Chen C-H, et al. (2008) Activation of aldehyde dehydrogenase-2 reduces ischemic damage to the heart. Science 321:1493-1495.
34. Carroll SB (2008) Evo-devo and an expanding evolutionary synthesis: A genetic theory of morphological evolution. Cell 134:25-36.
35. Hoekstra HE, Coyne JA (2007) The locus of evolution: Evo devo and the genetics of adaptation. Evolution 61:995-1016.
36. Yu J-K, et al. (2007) Axial patterning in cephalochordates and the evolution of the organizer. Nature 445:613-617.
37. Satou Y, et al. (2002) A cDNA resource from the basal chordate Ciona intestinalis. Genesis 33:153-154. (Pubitemid 34966835)