Home LiteratureArticle Details
PMID: 15349769 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Positive selection in MAOA gene is human exclusive: determination of the putative amino acid change selected in the human lineage.

Human genetics ·Vol. 115 ·No. 5 ·2004-10-00 ·Pages 377-86

Andrés AM, Soldevila M, Navarro A, Kidd KK, Oliva B, Bertranpetit J

Abstract

Monoamine oxidase A (MAOA) is the X-linked gene responsible for deamination and subsequent degradation of several neurotransmitters and other amines. Among other activities, the gene has been shown to play a role in locomotion, circadian rhythm, and pain sensitivity and to have a critical influence on behavior and cognition. Previous studies have reported a non-neutral evolution of the gene attributable to positive selection in the human lineage. To determine whether this selection was human-exclusive or shared with other species, we performed a population genetic analysis of the pattern of nucleotide variation in non-human species, including bonobo, chimpanzee, gorilla, and orangutan. Footprints of positive selection were absent in all analyzed species, suggesting that positive selection has been recent and unique to humans. To determine which human-unique genetic changes could have been responsible for this differential evolution, the coding region of the gene was compared between human, chimpanzee, and gorilla. Only one human exclusive non-conservative change is present in the gene: Glu151Lys. This human substitution affects protein dimerization according to a three-dimensional structural model that predicts a non-negligible functional shift. This is the only candidate position at present to have been selected to fixation in humans during an episode of positive selection. Divergence analysis among species has shown that, even under positive selection in the human lineage, the MAOA gene did not experience accelerated evolution in any of the analyzed lineages, and that tools such as K(a)/ K(s) would not have detected the selective history of the gene.

MeSH Terms
Amino Acid Sequence Animals Evolution, Molecular Gorilla gorilla Humans Models, Molecular Molecular Sequence Data Monoamine Oxidase/genetics Pan paniscus Pan troglodytes Phylogeny Pongo pygmaeus Population Surveillance Selection, Genetic
Chemicals
Monoamine Oxidase
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Andrés Aida M
Unitat de Biologia Evolutiva, Departament de Ciències Experimentals i de la Salut, Universitat Pompeu Fabra, Barcelona, Catalonia, Spain.
Soldevila Marta
Navarro Arcadi
Kidd Kenneth K
Oliva Baldomero
Bertranpetit Jaume
References (45)
45 references, click to expand
  1. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.
    Genetics. 1989 Nov;123(3):585-95 PMID: 2513255
  2. Adaptive evolution of ASPM, a major determinant of cerebral cortical size in humans.
    Hum Mol Genet. 2004 Mar 1;13(5):489-94 PMID: 14722158
  3. Statistical tests of neutrality of mutations.
    Genetics. 1993 Mar;133(3):693-709 PMID: 8454210
  4. A human genome diversity cell line panel.
    Science. 2002 Apr 12;296(5566):261-2 PMID: 11954565
  5. Biochemical, behavioral, physiologic, and neurodevelopmental changes in mice deficient in monoamine oxidase A or B.
    Brain Res Bull. 2001 Nov 15;56(5):453-62 PMID: 11750790
  6. Extensive nuclear DNA sequence diversity among chimpanzees.
    Science. 1999 Nov 5;286(5442):1159-62 PMID: 10550054
  7. Monoamine oxidase: from genes to behavior.
    Annu Rev Neurosci. 1999;22:197-217 PMID: 10202537
  8. Comparative analysis of Alu insertion sequences in the APP 5' flanking region in humans and other primates.
    J Mol Evol. 2004 Jun;58(6):722-31 PMID: 15461429
  9. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis.
    Bioinformatics. 1999 Feb;15(2):174-5 PMID: 10089204
  10. Adaptive protein evolution at the Adh locus in Drosophila.
    Nature. 1991 Jun 20;351(6328):652-4 PMID: 1904993
  11. Tools for comparative protein structure modeling and analysis.
    Nucleic Acids Res. 2003 Jul 1;31(13):3375-80 PMID: 12824331
  12. Genome sequence comparisons: hurdles in the fast lane to functional genomics.
    Brief Bioinform. 2000 Nov;1(4):381-8 PMID: 11465055
  13. Episodic adaptive evolution of primate lysozymes.
    Nature. 1997 Jan 9;385(6612):151-4 PMID: 8990116
  14. cDNA cloning of human liver monoamine oxidase A and B: molecular basis of differences in enzymatic properties.
    Proc Natl Acad Sci U S A. 1988 Jul;85(13):4934-8 PMID: 3387449
  15. Monoamine oxidase in neuropsychiatry and behavior.
    Am J Hum Genet. 1999 Sep;65(3):593-8 PMID: 10441564
  16. Evolution of the human ASPM gene, a major determinant of brain size.
    Genetics. 2003 Dec;165(4):2063-70 PMID: 14704186
  17. Rapid evolution of male reproductive genes in the descent of man.
    Nature. 2000 Jan 20;403(6767):304-9 PMID: 10659848
  18. Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA.
    Science. 1995 Jun 23;268(5218):1763-6 PMID: 7792602
  19. Phylogenetic shadowing of primate sequences to find functional regions of the human genome.
    Science. 2003 Feb 28;299(5611):1391-4 PMID: 12610304
  20. Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals.
    Proc Natl Acad Sci U S A. 2001 Feb 27;98 (5):2509-14 PMID: 11226269
  21. Genomewide comparison of DNA sequences between humans and chimpanzees.
    Am J Hum Genet. 2002 Jun;70(6):1490-7 PMID: 11992255
  22. The geographic distribution of monoamine oxidase haplotypes supports a bottleneck during the dispersion of modern humans from Africa.
    J Mol Evol. 2001 Feb;52(2):157-63 PMID: 11231895
  23. Isolation of a candidate gene for Norrie disease by positional cloning.
    Nat Genet. 1992 Jun;1(3):199-203 PMID: 1303235
  24. Molecular evolution of FOXP2, a gene involved in speech and language.
    Nature. 2002 Aug 22;418(6900):869-72 PMID: 12192408
  25. Great ape DNA sequences reveal a reduced diversity and an expansion in humans.
    Nat Genet. 2001 Feb;27(2):155-6 PMID: 11175781
  26. Abnormal behavior associated with a point mutation in the structural gene for monoamine oxidase A.
    Science. 1993 Oct 22;262(5133):578-80 PMID: 8211186
  27. Evidence for positive selection and population structure at the human MAO-A gene.
    Proc Natl Acad Sci U S A. 2002 Jan 22;99(2):862-7 PMID: 11805333
  28. Hitchhiking under positive Darwinian selection.
    Genetics. 2000 Jul;155(3):1405-13 PMID: 10880498
  29. Selective enhancement of emotional, but not motor, learning in monoamine oxidase A-deficient mice.
    Proc Natl Acad Sci U S A. 1997 May 27;94(11):5929-33 PMID: 9159177
  30. Low nucleotide diversity in chimpanzees and bonobos.
    Genetics. 2003 Aug;164(4):1511-8 PMID: 12930756
  31. Structure of human monoamine oxidase B, a drug target for the treatment of neurological disorders.
    Nat Struct Biol. 2002 Jan;9(1):22-6 PMID: 11753429
  32. Monoamine oxidase deficiency in males with an X chromosome deletion.
    Neuron. 1989 Jan;2(1):1069-76 PMID: 2483108
  33. Molecular dynamics simulation of highly charged proteins: comparison of the particle-particle particle-mesh and reaction field methods for the calculation of electrostatic interactions.
    Protein Sci. 2003 Oct;12(10):2161-72 PMID: 14500874
  34. PAML: a program package for phylogenetic analysis by maximum likelihood.
    Comput Appl Biosci. 1997 Oct;13(5):555-6 PMID: 9367129
  35. Gene diversity patterns at 10 X-chromosomal loci in humans and chimpanzees.
    Mol Biol Evol. 2003 Aug;20(8):1281-9 PMID: 12777533
  36. Accelerated protein evolution and origins of human-specific features: Foxp2 as an example.
    Genetics. 2002 Dec;162(4):1825-35 PMID: 12524352
  37. Neutral substitutions occur at a faster rate in exons than in noncoding DNA in primate genomes.
    Genome Res. 2003 May;13(5):838-44 PMID: 12727904
  38. The Protein Data Bank and structural genomics.
    Nucleic Acids Res. 2003 Jan 1;31(1):489-91 PMID: 12520059
  39. Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees.
    Am J Hum Genet. 2001 Feb;68(2):444-56 PMID: 11170892
  40. A test of neutral molecular evolution based on nucleotide data.
    Genetics. 1987 May;116(1):153-9 PMID: 3110004
  41. Protein structure modeling for structural genomics.
    Nat Struct Biol. 2000 Nov;7 Suppl:986-90 PMID: 11104007
  42. Multiple protein sequence alignment from tertiary structure comparison: assignment of global and residue confidence levels.
    Proteins. 1992 Oct;14(2):309-23 PMID: 1409577
  43. The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003.
    Nucleic Acids Res. 2003 Jan 1;31(1):365-70 PMID: 12520024
  44. Human monoamine oxidase A and B genes exhibit identical exon-intron organization.
    Proc Natl Acad Sci U S A. 1991 May 1;88(9):3637-41 PMID: 2023912
  45. RRTree: relative-rate tests between groups of sequences on a phylogenetic tree.
    Bioinformatics. 2000 Mar;16(3):296-7 PMID: 10869026
Article Info
Journal
Human genetics
Abbr.
Hum Genet
ISSN
0340-6717
Published
2004-10-00
Epub
2004-00-03
Pages
377-86
Language
English
Region
Germany
NLM ID
7613873
Subset
IM
Databases
GENBANK
AY684851, AY684852, AY684853, AY684854, AY684855, AY684859, AY684860, AY684861, AY684862, AY684863, AY685683, AY685684, AY685686, AY685687, AY685688, AY685689, AY685690, AY685691, AY685692, AY685693, AY685694, AY685695, AY685696, AY685697, AY685698, AY685699, AY685700, AY685701, AY685702, AY685703, AY685704, AY685705
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com