Invited Mini Review : Loss of gene function and evolution of human phenotypes = Invited Mini Review : Loss of gene function and evolution of human phenotypes

다국어 초록 (Multilingual Abstract)

Humans have acquired many distinct evolutionary traits after the human-chimpanzee divergence. These phenotypes have resulted from genetic changes that occurred in the human genome and were retained by natural selection. Comparative primate genome analyses reveal that loss-of-function mutations are common in the human genome. Some of these gene inactivation events were revealed to be associated with the emergence of advantageous phenotypes and were therefore positively selected and fixed in modern humans (the “less-ismore” hypothesis). Representative cases of human gene inactivation and their functional implications are presented in this review. Functional studies of additional inactive genes will provide insight into the molecular mechanisms underlying acquisition of various human-specific traits. [BMB Reports 2015; 48(7): 373-379]

참고문헌 (Reference)

• 1 Kim U, "Worldwide haplotype diversity and coding sequence variation at human bitter taste receptor loci" Hum Mutat 26 : 199 ~ 204, 2005
• 2 Olson MV, "When less is more: gene loss as an engine of evolutionary change" Am J Hum Genet 64 : 18 ~ 23, 1999
• 3 McGowen MR, "The vestigial olfactory receptor subgenome of odontocete whales:phylogenetic congruence between gene-tree reconciliation and supermatrix methods" Syst Biol 57 : 574 ~ 590, 2008
• 4 Rich SM, "The origin of malignant malaria" Proc Natl Acad Sci U S A 106 : 14902 ~ 14907, 2009
• 5 Kaiser J, "The hunt for missing genes" Science 344 : 687 ~ 689, 2014
• 6 Lin YL, "The evolution and functional impact of human deletion variants shared with archaic hominin genomes" Mol Biol Evol 32 : 1008 ~ 1019, 2015
• 7 Combarros O, "The dopamine β-hydroxylase -1021C/T polymorphism is associated with the risk of Alzheimer's disease in the Epistasis Project" BMC Med Genet 11 : 162 ~, 1021
• 8 Wroe S, "The craniomandibular mechanics of being human" Proc Biol Sci 277 : 3579 ~ 3586, 2010
• 9 Sabeti PC, "The case for selection at CCR5-D32" PLoS Biol 3 : e378 ~, 2005
• 10 Kim DS, "The acquisition of novel N-glycosylation sites in conserved proteins during human evolution" BMC Bioinformatics 16 : 29 ~, 2015
• 11 Roth SM, "The ACTN3 R577X nonsense allele is under-represented in elite-level strength athletes" Eur J Hum Genet 16 : 391 ~ 394, 2008
• 12 Bachmanov AA, "Taste receptor genes" Annu Rev Nutr 27 : 389 ~ 414, 2007
• 13 Kiselyov K, "TRPC channels in pheromone sensing" Vitam Horm 83 : 197 ~ 213, 2010
• 14 Xue Y, "Spread of an inactive form of caspase-12 in humans is due to recent positive selection" Am J Hum Genet 78 : 659 ~ 670, 2006
• 15 Pronin AN, "Specific alleles of bitter receptor genes influence human sensitivity to the bitterness of aloin and saccharin" Curr Biol 17 : 1403 ~ 1408, 2007
• 16 Innan, H.,Liman ER, "Relaxed selective pressure on an essential component of pheromone transduction in primate evolution" National Academy of Sciences; 1999 Proc Natl Acad Sci U S A 100 : 3328 ~ 3332, 2003
• 17 Wang X, "Relaxation of selective constraint and loss of function in the evolution of human bitter taste receptor genes" Hum Mol Genet 13 : 2671 ~ 2678, 2004
• 18 Zhao H, "Pseudogenization of the umami taste receptor gene Tas1r1 in the giant panda coincided with its dietary switch to bamboo" Mol Biol Evol 27 : 2669 ~ 2673, 2010
• 19 Li X, "Pseudogenization of a sweet-receptor gene accounts for cats' indifference toward sugar" PLoS Genet 1 : 27 ~ 35, 2005
• 20 Liu W, "Origin of the human malaria parasite Plasmodium falciparum in gorillas" Nature 467 : 420 ~ 425, 2010
• 21 Niimura Y, "Olfactory receptor multigene family in vertebrates: from the viewpoint of evolutionary genomics" Curr Genomics 13 : 103 ~ 114, 2012
• 22 Barton RA, "Olfactory evolution and behavioral ecology in primates" Am J Primatol 68 : 545 ~ 558, 2006
• 23 McCollum MA, "Of muscle-bound crania and human brain evolution: the story behind the MYH16 headlines" J Hum Evol 50 : 232 ~ 236, 2006
• 24 Takahashi T, "N-glycolylneuraminic acid on human epithelial cells prevents entry of influenza A viruses that possess N-glycolylneuraminic acid binding ability" J Virol 88 : 8445 ~ 8456, 2014
• 25 Stedman HH, "Myosin gene mutation correlates with anatomical changes in the human lineage" Nature 428 : 415 ~ 418, 2004
• 26 Vannier B, "Mouse trp2, the homologue of the human trpc2 pseudogene, encodes mTrp2, a store depletion-activated capacitative Ca2+ entry channel" Proc Natl Acad Sci U S A 96 : 2060 ~ 2064, 1999
• 27 Enard W, "Molecular evolution of FOXP2, a gene involved in speech and language" Nature 418 : 869 ~ 872, 2002
• 28 Samson M, "Molecular cloning and functional expression of a new human CC-chemokine receptor gene" Biochemistry 35 : 3362 ~ 3367, 1996
• 29 Niemi AK, "Mitochondrial DNA and ACTN3genotypes in finnish elite endurance and sprint athletes" Eur J Hum Genet 13 : 965 ~ 969, 2005
• 30 Yim HS, "Minke whale genome and aquatic adaptation in cetaceans" Nat Genet 46 : 88 ~ 92, 2014
• 31 Smith TD, "Microsmatic primates:reconsidering how and when size matters" Anat Rec B New Anat 279 : 24 ~ 31, 2004
• 32 Bergfeld AK, "Metabolism of vertebrate amino sugars with N-glycolyl groups: elucidating the intracellular fate of the non-human sialic acid N-glycolylneuraminic acid" J Biol Chem 287 : 28865 ~ 28881, 2012
• 33 Beauchamp, G.K.,Brand, J.G.,Glaser, D.,Jiang P,Josue, J.,Li, W.,Li, X.,Margolskee, R.F.,Reed, D.R., "Major taste loss in carnivorous mammals" National Academy of Sciences; 1999 Proc Natl Acad Sci U S A 109 : 4956 ~ 4961, 2012
• 34 MacArthur DG, "Loss-of-function variants in the genomes of healthy humans" Hum Mol Genet 19 : 125 ~ 130, 2010
• 35 Sumiyama K, "Loss-of-function mutation in a repressor module of human-specifically activated enhancer HACNS1" Mol Biol Evol 28 : 3005 ~ 3007, 2011
• 36 MacArthur DG, "Loss of ACTN3 gene function alters mouse muscle metabolism and shows evidence of positive selection in humans" Nat Genet 39 : 1261 ~ 1265, 2007
• 37 Hutter G, "Long-term control of HIV by CCR5 Delta32/Delta32 stem-cell transplantation" N Engl J Med 360 : 692 ~ 698, 2009
• 38 Cubells JF, "Linkage analysis of plasma dopamine β-hydroxylase activity in families of patients with schizophrenia" Hum Genet 130 : 635 ~ 643, 2011
• 39 Go Y, "Lineage-specific loss of function of bitter taste receptor genes in humans and nonhuman primates" Genetics 170 : 313 ~ 326, 2005
• 40 Perry GH, "Insights into hominin phenotypic and dietary evolution from ancient DNA sequence data" J Hum Evol 79 : 55 ~ 63, 2015
• 41 Hahn Y, "Inactivation of MOXD2 and S100A15A by exon deletion during human evolution" Mol Biol Evol 24 : 2203 ~ 2212, 2007
• 42 Chou HH,Diaz, S.,Hayakawa, T.,Indriati, E.,Krings, M.,Leakey, M.,Paabo, S.,Satta, Y.,Takahata, N.,Varki A, "Inactivation of CMP-N-acetylneuraminic acid hydroxylase occurred prior to brain expansion during human evolution" National Academy of Sciences; 1999 Proc Natl Acad Sci U S A 99 : 11736 ~ 11741, 2002
• 43 Kim DS, "Identification of novel phosphorylation modification sites in human proteins that originated after the human-chimpanzee divergence" Bioinformatics 27 : 2494 ~ 2501, 2011
• 44 Hahn Y, "Identification of nine humanspecific frameshift mutations by comparative analysis of the human and the chimpanzee genome sequences" Bioinformatics 21 (1) : 186 ~ 194, 2005
• 45 Kim DS, "Identification of human-specific transcript variants induced by DNA insertions in the human genome" Bioinformatics 27 : 14 ~ 21, 2011
• 46 Deng H, "Identification of a major co-receptor for primary isolates of HIV-1" Nature 381 : 661 ~ 666, 1996
• 47 Sulem P, "Identification of a large set of rare complete human knockouts" Nat Genet 47 : 448 ~ 452, 2015
• 48 Konopka G, "Humanspecific transcriptional regulation of CNS development genes by FOXP2" Nature 462 : 213 ~ 217, 2009
• 49 McLean CY, "Humanspecific loss of regulatory DNA and the evolution of human-specific traits" Nature 471 : 216 ~ 219, 2011
• 50 Prabhakar S, "Humanspecific gain of function in a developmental enhancer" Science 321 : 1346 ~ 1350, 2008
• 51 Gerkin RC, "Humans can discriminate trillions of olfactory stimuli, or more, or fewer" arXiv 1502 : 05120 ~, 2015
• 52 Bushdid C, "Humans can discriminate more than 1 trillion olfactory stimuli" Science 343 : 1370 ~ 1372, 2014
• 53 Kim DS, "Human-specific protein isoforms produced by novel splice sites in the human genome after the human-chimpanzee divergence" BMC Bioinformatics 13 : 299 ~, 2012
• 54 Hahn Y, "Human-specific nonsense mutations identified by genome sequence comparisons" Hum Genet 119 : 169 ~ 178, 2006
• 55 Varki A, "Human-specific evolution of sialic acid targets: explaining the malignant malaria mystery?" Proc Natl Acad Sci U S A 106 : 14739 ~ 14740, 2009
• 56 Alkuraya FS, "Human knockout research: new horizons and opportunities" Trends Genet 31 : 108 ~ 115, 2015
• 57 Currie P, "Human genetics: muscling in on hominid evolution" Nature 428 : 373 ~ 374, 2004
• 58 Pennisi E, "Human evolution. The primate bite:brawn versus brain?" Science 303 : 1957 ~, 2004
• 59 Fischer H, "Human caspase 12 has acquired deleterious mutations" Biochem Biophys Res Commun 293 : 722 ~ 726, 2002
• 60 Alnemri ES, "Human ICE/CED-3 protease nomenclature" Cell 87 : 171 ~, 1996
• 61 Deng L, "Host adaptation of a bacterial toxin from the human pathogen Salmonella Typhi" Cell 159 : 1290 ~ 1299, 2014
• 62 Liu R, "Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection" Cell 86 : 367 ~ 377, 1996
• 63 Dragic T, "HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5" Nature 381 : 667 ~ 673, 1996
• 64 Roudnitzky N, "Genomic, genetic and functional dissection of bitter taste responses to artificial sweeteners" Hum Mol Genet 20 : 3437 ~ 3449, 2011
• 65 Chen FC, "Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees" Am J Hum Genet 68 : 444 ~ 456, 2001
• 66 Patterson N, "Genetic evidence for complex speciation of humans and chimpanzees" Nature 441 : 1103 ~ 1108, 2006
• 67 Wang X, "Gene losses during human origins" PLoS Biol 4 : e52 ~, 2006
• 68 Tebas P, "Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV" N Engl J Med 370 : 901 ~ 910, 2014
• 69 Kim DS, "Gains of ubiquitylation sites in highly conserved proteins in the human lineage" BMC Bioinformatics 13 : 306 ~, 2012
• 70 Kim DS, "Frequent loss and alteration of the MOXD2 gene in catarrhines and whales: a possible connection with the evolution of olfaction" PLoS One 9 : e104085 ~, 2014
• 71 Hayakawa T, "Frequent expansions of the bitter taste receptor gene repertoire during evolution of mammals in the Euarchontoglires clade" Mol Biol Evol 31 : 2018 ~ 2031, 2014
• 72 Hayakawa T, "Fixation of the human-specific CMP-N-acetylneuraminic acid hydroxylase pseudogene and implications of haplotype diversity for human evolution" Genetics 172 : 1139 ~ 1146, 2006
• 73 Desjardins PR, "Evolutionary implications of three novel members of the human sarcomeric myosin heavy chain gene family" Mol Biol Evol 19 : 375 ~ 393, 2002
• 74 Dong D, "Evolution of olfactory receptor genes in primates dominated by birth-and-death process" Genome Biol Evol 1 : 258 ~ 264, 2009
• 75 Barnwell, J. W.,Gagneux, P.,Martin MJ,Rayner, J. C.,Varki A, "Evolution of human-chimpanzee differences in malaria susceptibility: relationship to human genetic loss of N-glycolylneuraminic acid" National Academy of Sciences; 1999 Proc Natl Acad Sci U S A 102 : 12819 ~ 12824, 2005
• 76 Bramble DM, "Endurance running and the evolution of Homo" Nature 432 : 345 ~ 352, 2004
• 77 Ruxton GD, "Endurance running and its relevance to scavenging by early hominins" Evolution 67 : 861 ~ 867, 2013
• 78 Erkner, A.,Parry CM,le Coutre, J., "Divergence of T2R chemosensory receptor families in humans, bonobos, and chimpanzees" National Academy of Sciences; 1999 Proc Natl Acad Sci U S A 101 : 14830 ~ 14834, 2004
• 79 Beniaminov A, "Distinctive structures between chimpanzee and human in a brain noncoding RNA" RNA 14 : 1270 ~ 1275, 2008
• 80 Saleh M, "Differential modulation of endotoxin responsiveness by human caspase-12 polymorphisms" Nature 429 : 75 ~ 79, 2004
• 81 Mills M, "Differential expression of the actin-binding proteins, α-actinin-2 and -3, in different species: implications for the evolution of functional redundancy" Hum Mol Genet 10 : 1335 ~ 1346, 2001
• 82 Matsui A, "Degeneration of olfactory receptor gene repertories in primates: no direct link to full trichromatic vision" Mol Biol Evol 27 : 1192 ~ 1200, 2010
• 83 Stephens JC, "Dating the origin of the CCR5-D32 AIDS-resistance allele by the coalescence of haplotypes" Am J Hum Genet 62 : 1507 ~ 1515, 1998
• 84 Timmers HJ, "Congenital dopamine-β-hydroxylase deficiency in humans" Ann N Y Acad Sci 1018 : 520 ~ 523, 2004
• 85 Varki A, "Comparing the human and chimpanzee genomes: searching for needles in a haystack" Genome Res 15 : 1746 ~ 1758, 2005
• 86 Rogers J, "Comparative primate genomics:emerging patterns of genome content and dynamics" Nat Rev Genet 15 : 347 ~ 359, 2014
• 87 Zhu J, "Comparative genomics search for losses of long-established genes on the human lineage" PLoS Comput Biol 3 : e247 ~, 2007
• 88 Perry GH, "Comparative analyses reveal a complex history of molecular evolution for human MYH16" Mol Biol Evol 22 : 379 ~ 382, 2005
• 89 Beggs AH, "Cloning and characterization of two human skeletal muscle alpha-actinin genes located on chromosomes 1 and 11" J Biol Chem 267 : 9281 ~ 9288, 1992
• 90 Yu L, "Characterization of TRPC2, an essential genetic component of VNS chemoreception, provides insights into the evolution of pheromonal olfaction in secondary-adapted marine mammals" Mol Biol Evol 27 : 1467 ~ 1477, 2010
• 91 Varki NM, "Biomedical differences between human and nonhuman hominids: potential roles for uniquely human aspects of sialic acid biology" Annu Rev Pathol 6 : 365 ~ 393, 2011
• 92 Dawkins R, "Arms races between and within species" Proc R Soc Lond B Biol Sci 205 : 489 ~ 511, 1979
• 93 Pollard KS, "An RNA gene expressed during cortical development evolved rapidly in humans" Nature 443 : 167 ~ 172, 2006
• 94 Lubke KT, "Always follow your nose: the functional significance of social chemosignals in human reproduction and survival" Horm Behav 68 : 134 ~ 144, 2015
• 95 Gagneux, P., Satta, Y., Takahata, N.,Hayakawa T,Varki A, "Alu-mediated inactivation of the human CMP N-acetylneuraminic acid hydroxylase gene" National Academy of Sciences; 1999 Proc Natl Acad Sci U S A 98 : 11399 ~ 11404, 2001
• 96 Yang N, "ACTN3 genotype is associated with human elite athletic performance" Am J Hum Genet 73 : 627 ~ 631, 2003
• 97 Buck L, "A novel multigene family may encode odorant receptors: a molecular basis for odor recognition" Cell 65 : 175 ~ 187, 1991
• 98 Chou HH, "A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence" Proc Natl Acad Sci U S A 95 : 11751 ~ 11756, 1998
• 99 Yngvadottir B, "A genome-wide survey of the prevalence and evolutionary forces acting on human nonsense SNPs" Am J Hum Genet 84 : 224 ~ 234, 2009
• 100 Su AI, "A gene atlas of the mouse and human protein-encoding transcriptomes" Proc Natl Acad Sci U S A 101 : 6062 ~ 6067, 2004
• 101 North KN, "A common nonsense mutation results in a-actinin-3 deficiency in the general population" Nat Genet 21 : 353 ~ 354, 1999
• 102 Hoh JF, "'Superfast' or masticatory myosin and the evolution of jaw-closing muscles of vertebrates" J Exp Biol 205 : 2203 ~ 2210, 2002