دورية أكاديمية

Conservation of a Chromosome 8 Inversion and Exon Mutations Confirm Common Gulonolactone Oxidase Gene Evolution Among Primates, Including H. Neanderthalensis.

التفاصيل البيبلوغرافية
العنوان: Conservation of a Chromosome 8 Inversion and Exon Mutations Confirm Common Gulonolactone Oxidase Gene Evolution Among Primates, Including H. Neanderthalensis.
المؤلفون: Mansueto A; Department of Human Nutrition, Foods, and Exercise, Virginia Tech, Blacksburg, VA, USA.; Department of Biological Sciences, Vanderbilt University, Nashvile, TN, USA., Good DJ; Department of Human Nutrition, Foods, and Exercise, Virginia Tech, Blacksburg, VA, USA. goodd@vt.edu.; Department of Human Nutrition, Foods, and Exercise, Virginia Tech, 1981 Kraft Drive (0913), ILSB Room 1020, Blacksburg, VA, 24060, USA. goodd@vt.edu.
المصدر: Journal of molecular evolution [J Mol Evol] 2024 Jun; Vol. 92 (3), pp. 266-277. Date of Electronic Publication: 2024 Apr 29.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Springer-Verlag Country of Publication: Germany NLM ID: 0360051 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1432-1432 (Electronic) Linking ISSN: 00222844 NLM ISO Abbreviation: J Mol Evol Subsets: MEDLINE
أسماء مطبوعة: Original Publication: Berlin, New York, Springer-Verlag.
مواضيع طبية MeSH: Evolution, Molecular* , Exons*/genetics , Phylogeny* , Primates*/genetics , Mutation*/genetics , L-Gulonolactone Oxidase*/genetics , Chromosome Inversion*/genetics, Animals ; Humans ; Pseudogenes/genetics ; Conserved Sequence/genetics
مستخلص: Ascorbic acid functions as an antioxidant and facilitates other biochemical processes such as collagen triple helix formation, and iron uptake by cells. Animals which endogenously produce ascorbic acid have a functional gulonolactone oxidase gene (GULO); however, humans have a GULO pseudogene (GULOP) and depend on dietary ascorbic acid. In this study, the conservation of GULOP sequences in the primate haplorhini suborder were investigated and compared to the GULO sequences belonging to the primates strepsirrhini suborder. Phylogenetic analysis suggested that the conserved GULOP exons in the haplorhini primates experienced a high rate of mutations following the haplorhini/strepsirrhini divergence. This high mutation rate has decreased during the evolution of the haplorhini primates. Additionally, indels of the haplorhini GULOP sequences were conserved across the suborder. A separate analysis for GULO sequences and well-conserved GULOP sequences focusing on placental mammals identified an in-frame GULO sequence in the Brazilian guinea pig, and a potential GULOP sequence in the pika. Similar to haplorhini primates, the guinea pig and lagomorph species have experienced a high substitution rate when compared to the mammals used in this study. A shared synteny to examine the conservation of local genes near GULO/GULOP identified a conserved inversion around the GULO/GULOP locus between the haplorhini and strepsirrhini primates. Fischer's exact test did not support an association between GULOP and the chromosomal inversion. Mauve alignment showed that the inversion of the length of the syntenic block that the GULO/GULOP genes belonged to was variable. However, there were frequent rearrangements around ~ 2 million base pairs adjacent to GULOP involving the KIF13B and MSRA genes. These data may suggest that genes acquiring deleterious mutations in the coding sequence may respond to these deleterious mutations with rapid substitution rates.
(© 2024. The Author(s).)
References: Altekar G, Dwarkadas S, Huelsenbeck JP, Ronquist F (2004) Parallel metropolis coupled markov chain monte carlo for bayesian phylogenetic inference. Bioinformatics 20:407. (PMID: 10.1093/bioinformatics/btg42714960467)
(2015) A high-quality Neandertal genome sequence https://www.eva.mpg.de/genetics/genome-projects/neandertal/ . Ancient Genome Browser. Ancient Genome Browser.
Birney EC, Jenness R, Ayaz KM (1976) Inability of bats to synthesise L-ascorbic acid. Nature 260:626. (PMID: 10.1038/260626a01264230)
Chatterjee IB, Chatterjee GC, Ghosh NC, Ghosh JJ, Guha BC (1960) Biological synthesis of L-ascorbic acid in animal tissues: conversion of D-glucuronolactone and L-gulonolactone into L-ascorbic acid. Biochem J 76:279. (PMID: 10.1042/bj0760279136926101204705)
Cui J, Pan YH, Zhang Y, Jones G, Zhang S (2011a) Progressive pseudogenization: vitamin C synthesis and its loss in bats. Mol Biol Evol 28:1025. (PMID: 10.1093/molbev/msq28621037206)
Cui J, Yuan X, Wang L, Jones G, Zhang S (2011b) Recent loss of vitamin C biosynthesis ability in bats. PLoS One 6:e27114. (PMID: 10.1371/journal.pone.0027114220694933206078)
Darling AE, Mau B, Perna NT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5:e11147. (PMID: 10.1371/journal.pone.0011147205930222892488)
Devor EJ (2006) Primate microRNAs miR-220 and miR-492 lie within processed pseudogenes. J Hered 97:186. (PMID: 10.1093/jhered/esj02216489141)
Drouin G, Godin JR, Page B (2011) The genetics of vitamin C loss in vertebrates. Curr Genomics 12:371. (PMID: 10.2174/138920211796429736222948793145266)
Gaudry MJ, Campbell KL (2017) Evolution of UCP1 transcriptional regulatory elements across the mammalian phylogeny. Front Physiol 8:670. (PMID: 10.3389/fphys.2017.00670289792095611445)
Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai W, Fritz MH, Hansen NF, Durand EY, Malaspinas AS, Jensen JD, Marques-Bonet T, Alkan C, Prufer K, Meyer M, Burbano HA, Good JM, Schultz R, Aximu-Petri A, Butthof A, Hober B, Hoffner B, Siegemund M, Weihmann A, Nusbaum C, Lander ES, Russ C, Novod N, Affourtit J, Egholm M, Verna C, Rudan P, Brajkovic D, Kucan Z, Gusic I, Doronichev VB, Golovanova LV, Lalueza-Fox C, de la Rasilla M, Fortea J, Rosas A, Schmitz RW, Johnson PLF, Eichler EE, Falush D, Birney E, Mullikin JC, Slatkin M, Nielsen R, Kelso J, Lachmann M, Reich D, Paabo S (2010) A draft sequence of the Neandertal genome. Science 328:710. (PMID: 10.1126/science.1188021204481785100745)
Grollman AP, Lehninger AL (1957) Enzymic synthesis of L-ascorbic acid in different animal species. Arch Biochem Biophys 69:458. (PMID: 10.1016/0003-9861(57)90510-613445217)
Harrison FE, Meredith ME, Dawes SM, Saskowski JL, May JM (2010) Low ascorbic acid and increased oxidative stress in gulo(-/-) mice during development. Brain Res 1349:143. (PMID: 10.1016/j.brainres.2010.06.037205998292914834)
Kent WJ (2002) BLAT–the BLAST-like alignment tool. Genome Res 12:656. (PMID: 11932250187518)
Kleinjan DJ, van Heyningen V (1998) Position effect in human genetic disease. Hum Mol Genet 7:1611. (PMID: 10.1093/hmg/7.10.16119735382)
Lachapelle MY, Drouin G (2011) Inactivation dates of the human and guinea pig vitamin C genes. Genetica 139:199. (PMID: 10.1007/s10709-010-9537-x21140195)
Laukens D, Waeytens A, De Bleser P, Cuvelier C, De Vos M (2009) Human metallothionein expression under normal and pathological conditions: mechanisms of gene regulation based on in silico promoter analysis. Crit Rev Eukaryot Gene Expr 19:301. (PMID: 10.1615/CritRevEukarGeneExpr.v19.i4.4019817707)
Lind J (1753) Treatise of the Scurvy in Three Parts.
Linster CL, Van Schaftingen E (2007) Vitamin C. Biosynthesis, recycling and degradation in mammals. FEBS 274:1. (PMID: 10.1111/j.1742-4658.2006.05607.x)
Maeda N, Hagihara H, Nakata Y, Hiller S, Wilder J, Reddick R (2000) Aortic wall damage in mice unable to synthesize ascorbic acid. Proc Natl Acad Sci USA 97:841. (PMID: 10.1073/pnas.97.2.8411063916715418)
Nishikimi M, Yagi K (1991) Molecular basis for the deficiency in humans of gulonolactone oxidase, a key enzyme for ascorbic acid biosynthesis. Am J Clin Nutr 54:1203S. (PMID: 10.1093/ajcn/54.6.1203s1962571)
Nishikimi M, Koshizaka T, Ozawa T, Yagi K (1988) Occurrence in humans and guinea pigs of the gene related to their missing enzyme L-gulono-gamma-lactone oxidase. Arch Biochem Biophys 267:842. (PMID: 10.1016/0003-9861(88)90093-83214183)
Nishikimi M, Kawai T, Yagi K (1992) Guinea pigs possess a highly mutated gene for L-gulono-gamma-lactone oxidase, the key enzyme for L-ascorbic acid biosynthesis missing in this species. J Biol Chem 267:21967. (PMID: 10.1016/S0021-9258(19)36707-91400507)
Noonan JP, Coop G, Kudaravalli S, Smith D, Krause J, Alessi J, Chen F, Platt D, Paabo S, Pritchard JK, Rubin EM (2006) Sequencing and analysis of Neanderthal genomic DNA. Science 314:1113. (PMID: 10.1126/science.1131412171105692583069)
Ohta Y, Nishikimi M (1999) Random nucleotide substitutions in primate nonfunctional gene for L-gulono-gamma-lactone oxidase, the missing enzyme in L-ascorbic acid biosynthesis. Biochim Biophys Acta 1472:408. (PMID: 10.1016/S0304-4165(99)00123-310572964)
Petrov DA, Hartl DL (2000) Pseudogene evolution and natural selection for a compact genome. J Hered 91:221. (PMID: 10.1093/jhered/91.3.22110833048)
Pink RC, Wicks K, Caley DP, Punch EK, Jacobs L, Carter DR (2011) Pseudogenes: pseudo-functional or key regulators in health and disease? RNA 17:792. (PMID: 10.1261/rna.2658311213984013078729)
Pozzi L, Hodgson JA, Burrell AS, Sterner KN, Raaum RL, Disotell TR (2014) Primate phylogenetic relationships and divergence dates inferred from complete mitochondrial genomes. Mol Phylogenet Evol 75:165. (PMID: 10.1016/j.ympev.2014.02.023245832914059600)
Prufer K, Racimo F, Patterson N, Jay F, Sankararaman S, Sawyer S, Heinze A, Renaud G, Sudmant PH, de Filippo C, Li H, Mallick S, Dannemann M, Fu Q, Kircher M, Kuhlwilm M, Lachmann M, Meyer M, Ongyerth M, Siebauer M, Theunert C, Tandon A, Moorjani P, Pickrell J, Mullikin JC, Vohr SH, Green RE, Hellmann I, Johnson PL, Blanche H, Cann H, Kitzman JO, Shendure J, Eichler EE, Lein ES, Bakken TE, Golovanova LV, Doronichev VB, Shunkov MV, Derevianko AP, Viola B, Slatkin M, Reich D, Kelso J, Paabo S (2014) The complete genome sequence of a Neanderthal from the Altai Mountains. Nature 505:43. (PMID: 10.1038/nature1288624352235)
Robinson JT, Thorvaldsdottir H, Wenger AM, Zehir A, Mesirov JP (2017) Variant review with the integrative genomics viewer. Cancer Res 77:e31. (PMID: 10.1158/0008-5472.CAN-17-0337290929345678989)
Tabula Muris C, Overall c, Logistical c, Organ c, processing, Library p, sequencing, Computational data a, Cell type a, Writing g, Supplemental text writing g, Principal i (2018) Single-cell transcriptomics of 20 mouse organs creates a Tabula Muris. Nature 562:367. (PMID: 10.1038/s41586-018-0590-4)
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512. (PMID: 8336541)
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022. (PMID: 10.1093/molbev/msab120338924918233496)
Villa P, Roebroeks W (2014) Neandertal demise: an archaeological analysis of the modern human superiority complex. PLoS One 9:e96424. (PMID: 10.1371/journal.pone.0096424247890394005592)
Weissbach H, Resnick L, Brot N (2005) Methionine sulfoxide reductases: history and cellular role in protecting against oxidative damage. Biochim Biophys Acta 1703:203. (PMID: 10.1016/j.bbapap.2004.10.00415680228)
Westram AM, Faria R, Johannesson K, Butlin R, Barton N (2022) Inversions and parallel evolution. Philos Trans R Soc Lond B Biol Sci 377:20210203. (PMID: 10.1098/rstb.2021.0203356947479189493)
Yang H (2013) Conserved or lost: molecular evolution of the key gene GULO in vertebrate vitamin C biosynthesis. Biochem Genet 51:413. (PMID: 10.1007/s10528-013-9574-023404229)
Zerbino DR, Achuthan P, Akanni W, Amode MR, Barrell D, Bhai J, Billis K, Cummins C, Gall A, Giron CG, Gil L, Gordon L, Haggerty L, Haskell E, Hourlier T, Izuogu OG, Janacek SH, Juettemann T, To JK, Laird MR, Lavidas I, Liu Z, Loveland JE, Maurel T, McLaren W, Moore B, Mudge J, Murphy DN, Newman V, Nuhn M, Ogeh D, Ong CK, Parker A, Patricio M, Riat HS, Schuilenburg H, Sheppard D, Sparrow H, Taylor K, Thormann A, Vullo A, Walts B, Zadissa A, Frankish A, Hut SE, Kostadima M, Langridge N, Martin FJ, Muffato M, Perry E, Ruffier M, Staines DM, Trevanion SJ, Aken BL, Cunningham F, Yates A, Flicek P (2018) Ensembl 2018. Nucleic Acids Res 46:D754. (PMID: 10.1093/nar/gkx109829155950)
Zody MC, Jiang Z, Fung HC, Antonacci F, Hillier LW, Cardone MF, Graves TA, Kidd JM, Cheng Z, Abouelleil A, Chen L, Wallis J, Glasscock J, Wilson RK, Reily AD, Duckworth J, Ventura M, Hardy J, Warren WC, Eichler EE (2008) Evolutionary toggling of the MAPT 17q21.31 inversion region. Nat Genet 40:1076. (PMID: 10.1038/ng.193191659222684794)
فهرسة مساهمة: Keywords: Ascorbic acid; GULO; GULOP; Neanderthal; Phylogeny; Primates; Vitamin C
المشرفين على المادة: EC 1.1.3.8 (L-Gulonolactone Oxidase)
تواريخ الأحداث: Date Created: 20240429 Date Completed: 20240612 Latest Revision: 20240620
رمز التحديث: 20240621
مُعرف محوري في PubMed: PMC11169010
DOI: 10.1007/s00239-024-10165-0
PMID: 38683367
قاعدة البيانات: MEDLINE
الوصف
تدمد:1432-1432
DOI:10.1007/s00239-024-10165-0