Biochemical Genetics

, Volume 47, Issue 9–10, pp 609–624 | Cite as

Opossum Aldehyde Dehydrogenases: Evidence for Four ALDH1A1-like Genes on Chromosome 6 and ALDH1A2 and ALDH1A3 Genes on Chromosome 1

Article

Abstract

Evidence is presented for six opossum ALDH1A genes, including four ALDH1A1-like genes on chromosome 6 and ALDH1A2- and ALDH1A3-like genes on chromosome 1. Predicted structures for the opossum aldehyde dehydrogenase (ALDH) subunits and the intron–exon boundaries for opossum ALDH genes showed a high degree of similarity with other mammalian ALDHs. Phylogenetic analyses supported the proposed designation of these opossum class 1 ALDHs as ALDH1A-like, ALDH1A2-like, and ALDH1A3-like and are therefore likely to play important roles in retinal and peroxidic aldehyde metabolism. Alignments of predicted opossum ALDH1A amino acid sequences with sheep ALDH1A1 and rat ALDH1A2 sequences demonstrated conservation of key residues previously shown to participate in catalysis and coenzyme binding. Amino acid substitution rates observed for family 1A ALDHs during vertebrate evolution indicated that ALDH1A2-like genes are evolving slower than ALDH1A1- and ALDH1A3-like genes. It is proposed that the common ancestor for ALDH1A genes predates the appearance of birds during vertebrate evolution.

Keywords

Aldehyde dehydrogenase Opossum Genetics Evolution 

Notes

Acknowledgments

I am grateful to Dr. Laura Cox and Dr. John VandeBerg of the Southwest Foundation for Biomedical Research in San Antonio, Texas, for helpful discussions and advice.

References

  1. Abedinia M, Pain T, Algar EM, Holmes RS (1990) Bovine corneal aldehyde dehydrogenase: the major soluble protein with a possible dual protective role for the eye. Exp Eye Res 51:419PubMedCrossRefGoogle Scholar
  2. Algar EM, Holmes RS (1989) Kinetic properties of murine liver aldehyde dehydrogenases. In: Weiner H, Flynn TG (eds) Enzymology and molecular biology of carbonyl metabolism. Alan R. Liss Inc, New YorkGoogle Scholar
  3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403PubMedGoogle Scholar
  4. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497PubMedCrossRefGoogle Scholar
  5. Dockham PA, Lee MO, Sladek NE (1992) Identification of human liver aldehyde dehydrogenases that catalyze the oxidation of aldophosphamide and retinaldehyde. Biochem Pharmacol 43:2453–2469PubMedCrossRefGoogle Scholar
  6. Duester G, Deltour HL, Ang HL (1997) Evidence that class IV alcohol dehydrogenase may function in embryonic retinoic acid synthesis. Adv Exp Med Biol 414:357PubMedGoogle Scholar
  7. Duester G, Molotkova N, Molotkov A (2006) Aldehyde dehydrogenase gene knockouts provide insight into role of retinoic acid during eye development. In: Weiner H, Plapp B, Lindahl R, Maser E (eds) Enzymology and molecular biology of carbonyl metabolism, vol 12. Purdue University Press, Indiana, p 56Google Scholar
  8. Gägnon I, Duester G, Bhat PV (2002) Kinetic analysis of mouse retinal dehydrogenase type-2 (RALDH2) for retinal substrates. Biochim Biophys Acta 1596:156PubMedGoogle Scholar
  9. Goedde HW, Agarwal DP, Harada S, Meier-Tackmann D, Ruofo D, Bienzle U, Kroeger A, Hussein L (1983) Population genetic studies of aldehyde dehydrogenase deficiency and alcohol sensitivity. Am J Hum Genet 35:769PubMedGoogle Scholar
  10. Grün F, Hirose Y, Kawauchi S, Ogura T, Umesono K (2000) Aldehyde dehydrogenase 6, a cytosolic retinaldehyde dehydrogenase prominently expressed in sensory neuroepithelia during development. J Biol Chem 275:41210PubMedCrossRefGoogle Scholar
  11. Harada S, Misawa S, Agarwal DP, Goedde HW (1980) Liver alcohol dehydrogenase and aldehyde dehydrogenase in the Japanese: isozyme variation and its possible role in alcohol intoxication. Am J Hum Genet 32:8PubMedGoogle Scholar
  12. Hempel J, von Bahr-Lindtröm H, Jornvall J (1984) Aldehyde dehydrogenase from human liver. Primary structure of the cytoplasmic isoenzyme. Eur J Biochem 141:21PubMedCrossRefGoogle Scholar
  13. Hjelle JJ, Petersen DR (1983) Hepatic aldehyde dehydrogenases and lipid peroxidation. Pharmcol Biochem Behav 18(Suppl 1):155CrossRefGoogle Scholar
  14. Holmes RS (1978) Genetics and ontogeny of aldehyde dehydrogenase isozymes in the mouseL localization of Ahd-1 encoding the mitochondrial isozyme on chromosome 4. Biochem Genet 16:1207PubMedCrossRefGoogle Scholar
  15. Holmes RS (2009) Opossum alcohol dehydrogenases: sequences, structures, phylogeny and evolution: evidence for the tandem location of ADH genes on opossum chromosome 5. Chem Biol Inter 178:8CrossRefGoogle Scholar
  16. Holmes RS, van Oorschot RAH, VandeBerg JL (1991) Aldehyde dehydrogenase isozymes in the gray short-tailed opossum (Monodelphis domestica): tissue and subcellular distribution and biochemical genetics of ALDH3. Biochem Genet 29:163PubMedGoogle Scholar
  17. Hsu L, Bendel RE, Akira Yoshida A (1988) Genomic structure of the human mitochondrial aldehyde dehydrogenase gene. Genomics 2:57PubMedCrossRefGoogle Scholar
  18. Hsu L, Chang W-C, Yoshida A (1989) Genomic structure of the human cytosolic aldehyde dehydrogenase gene. Genomics 5:857PubMedCrossRefGoogle Scholar
  19. Hsu LC, Chang WC, Hiraoka L, Hsieh CL (1994) Molecular cloning, genomic organization and chromosomal localization of an additional human aldehyde dehydrogenase, ALDH6. Genomics 24:333PubMedCrossRefGoogle Scholar
  20. Hsu L, Chang W-C, Yoshida A (1997) Human aldehyde dehydrogenase genes, ALDH7 and ALDH8: Genomic organization and gene structure comparison. Gene 189:89PubMedCrossRefGoogle Scholar
  21. Hsu LC, Chang WC, Hoffmann I, Duester G (1999) Molecular analysis of two closely related aldehyde dehydrogenases: identification of a role for ALDH1 but not for ALDH-pb in the biosynthesis of retinoic acid. Biochem J 339:387PubMedCrossRefGoogle Scholar
  22. Hsu LC, Chang W-C, Yoshida A (2000) Mouse type-2 retinaldehyde dehydrogenase (RALDH2): genomic organization, tissue-dependent expression, chromosome assignment and comparison to other types. Biochim Biophys Acta 1492:289PubMedGoogle Scholar
  23. Kays WT, Piatigorsky J (1997) Aldehyde dehydrogenase class 3 expression: identification of a cornea-preferred gene promoter in transgenic mice. Proc Natl Acad Sci USA 94:13594PubMedCrossRefGoogle Scholar
  24. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D (2002) The human genome browser at UCSC. Genome Res 12:994Google Scholar
  25. King G, Holmes RS (1998) Human ocular aldehyde dehydrogenase isozymes: distribution and properties as major soluble proteins in cornea and lens. J Exp Zool 282:12PubMedCrossRefGoogle Scholar
  26. Kumar S, Hedges SB (1998) A molecular timescale for vertebrate evolution. Nature 392:917PubMedCrossRefGoogle Scholar
  27. Labrecque J, Dumas F, Lacroix A, Bhat PV (1995) A novel isoenzyme of aldehyde dehydrogenase specifically involved in the biosynthesis of 9-cis and all-trans retinoic acid. Biochem J 305:681PubMedGoogle Scholar
  28. Lamb AL, Newcomer ME (1999) The structure of retinal dehydrogenase type II at 2.7 Å resolution: implications for retinal specificity. Biochem 38:6003CrossRefGoogle Scholar
  29. Lee MO, Manthey CL, Sladek NE (1991) Identification of mouse liver aldehyde dehydrogenases that catalyze the oxidation of retinaldehyde to retinoic acid. Biochem Pharmacol 42:1279PubMedCrossRefGoogle Scholar
  30. Manzer R, Qamar L, Estey T, Pappa A, Petersen DR, Vasiliou V (2003) Molecular cloning and baculovirus expression of the rabbit corneal aldehyde dehydrogenase (ALDH1A1) cDNA. DNA Cell Biol 22:329PubMedCrossRefGoogle Scholar
  31. McCaffrey P, Posch KC, Napoli JL, Gudas L, Dräger UC (1993) Changing patterns of the retinoic acid system in the developing retina. Dev Biol 158:390CrossRefGoogle Scholar
  32. McGuffin LJ, Bryson K, Jones DT (2000) The PSIPRED protein structure prediction server. Bioinformatics 16:404PubMedCrossRefGoogle Scholar
  33. Mikkelsen TS, Wakefield MJ, Aken B, Amemiya CT, Chang JL, Duke S, Garber M, Gentles AJ, Goodstadt L, Heger A, Jurka J, Kamal M, Mauceli E, Searle SMJ, Sharpe T, Baker ML, Batzer MA, Benos PV, Belov K, Clamp M, Cook A, Cuff J, Das R, Davidow L, Deakin JE, Fazzari MJ, Glass JL, Grabherr M, Greally JM, Gu W, Hore TA, Huttley GA, Kleber M, Jirtle RL, Koin E, Lee JT, Mahony S, Marra MA, Miller RD, Nicholls RD, Oda M, Papenfuss AT, Parra ZE, Pollock DD, Ray DA, Schein JE, Speed TP, Thompson K, VandeBerg JL, Wade CM, Walker JA, Waters PD, Webber C, Weidman JR, Xie X, Zody MC, Marshall Graves JA, Ponting CP, Breen M, Samollow PB, Lander ES, Lindblad-Toh J (2007) Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences. Nature 447:167PubMedCrossRefGoogle Scholar
  34. Moore SA, Baker HM, Blythe TJ, Kitson KE, Kitson TM, Baker EN (1998) Sheep liver cytosolic aldehyde dehydrogenase: the structure reveals the basis for the retinal specificity of class 1 aldehyde dehydrogenases. Structure 6:1541PubMedCrossRefGoogle Scholar
  35. Niederreither K, Subbarayan V, Dollé P, Chambon P (1999) Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat Genet 21:444PubMedCrossRefGoogle Scholar
  36. Nilsson MA, Arnason U, Spencer PB, Janke A (2004) Marsupial relationships and a timeline for marsupial radiation in South Gondwana. Gene 340:1189CrossRefGoogle Scholar
  37. Pappa A, Estey T, Manzer R, Brown D, Vasiliou V (2003) Human aldehyde dehydrogenase 3A1 (ALDH3A1): biochemical characterization and immunohistochemical localization in the cornea. Biochem J 376:615PubMedCrossRefGoogle Scholar
  38. Parés X, Cederlund E, Moreno A, Hjelmqvist L, Farrés J, Jörnvall H (1994) Mammalian class IV alcohol dehydrogenase (stomach alcohol dehydrogenase): structure, origin and correlation with enzymology. Proc Natl Acad Sci USA 91:1893PubMedCrossRefGoogle Scholar
  39. Rainwater DL, Kammerer CM, Singh ATK, Moore PM, Pousesh M, Shelledy WR, Vandeberg JL, Robinson ES (2001) Genetic control of lipoprotein phenotypes in the laboratory opossum. Genescreen 1:117CrossRefGoogle Scholar
  40. Schwede T, Kopp J, Guex N, Peitsch MC (2003) Swiss-Model: an automated protein homology-modelling server. Nucleic Acids Res 31:3383CrossRefGoogle Scholar
  41. Sophos NA, Black WJ, Vasiliou V (2006) An update of the ALDH gene family. In: Weiner H, Plapp B, Lindahl R, Maser E (eds) Enzymology and molecular biology of carbonyl metabolism. Pursue University Press, Indiana, 12: 3Google Scholar
  42. Steinmetz CG, Xie P, Weiner H, Hurley TD (1997) Structure of mitochondrial aldehyde dehydrogenase: the genetic component of ethanol aversion. Structures 5:701CrossRefGoogle Scholar
  43. Thierry-Mieg D, Thierry-Mieg J (2006) AceView: a comprehensive cDNA-supported gene and transcripts annotation. Genome Biol 7:S12PubMedCrossRefGoogle Scholar
  44. Timms GP, Holmes RS (1981) Genetics of aldehyde dehydrogenase isozymes in the mouse; evidence for multiple loci and localization of Ahd-2 on chromosome 19. Genetics 97:327PubMedGoogle Scholar
  45. VandeBerg JL (1990) The gray short-tailed opossum (Monodelphis domestica) as a model didephid species for marsupial genetic research. Aust J Zool 37:235CrossRefGoogle Scholar
  46. VandeBerg JL, Williams-Blangero S, Hubbard GB, Robinson ES (1994) Susceptibility to ultra-violet indiced corneal sarcomas is highly heritable in a laboratory opossum model. Int J Cancer 56:119PubMedCrossRefGoogle Scholar
  47. Vasiliou V, Nebert DW (2005) Analysis and update of the human aldehyde dehydrogenase (ALDH) gene family. Hum Genomics 2:138PubMedGoogle Scholar
  48. Vasiliou V, Bairoch A, Tipton KF, Nebert DW (1999) Eukaryotic aldehyde dehydrogenase (ALDH) genes: human polymorphisms and recommended nomenclature based on divergent evolution and chromosomal mapping. Pharmacogenetics 9:421PubMedCrossRefGoogle Scholar
  49. Wang X, Penzes P, Naploi JL (1996) Cloning of a cDNA encoding an aldehyde dehydrogenase and its expression in Escherichia coli. J Biol Chem 271:16288PubMedCrossRefGoogle Scholar
  50. Woodburne MO, Rich TH, Springer MS (2003) The evolution of tribospheny and the antiquity of mammalian clades. Mol Phylogenet Evol 28:360PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.School of Biomolecular and Physical SciencesGriffith UniversityBrisbaneAustralia

Personalised recommendations