Evolution and divergence of the mammalian SAMD9/SAMD9L gene family

BMC Evolutionary Biology

Pedro J Esteves¹  Grant McFadden²  Jia Liu²  Ana Lemos de Matos² 

[1] Centro de Investigação em Tecnologias da Saúde, IPSN, CESPU, 4585-116 Gandra, Portugal;Department of Molecular Genetics and Microbiology, University of Florida College of Medicine, Gainesville, Florida 32610, USA

关键词: Positive selection;    Evolutionary history;    Mammals;    SAMD9-like;    SAMD9;   

Others  :  1087099
DOI  :  10.1186/1471-2148-13-121

 received in 2013-02-06, accepted in 2013-06-06,  发布年份 2013

【 摘 要 】

Background

The physiological functions of the human Sterile Alpha Motif Domain-containing 9 (SAMD9) gene and its chromosomally adjacent paralogue, SAMD9-like (SAMD9L), currently remain unknown. However, the direct links between the deleterious mutations or deletions in these two genes and several human disorders, such as inherited inflammatory calcified tumors and acute myeloid leukemia, suggest their biological importance. SAMD9 and SAMD9L have also recently been shown to play key roles in the innate immune responses to stimuli such as viral infection. We were particularly interested in understanding the mammalian evolutionary history of these two genes. The phylogeny of SAMD9 and SAMD9L genes was reconstructed using the Maximum Likelihood method. Furthermore, six different methods were applied to detect SAMD9 and SAMD9L codons under selective pressure: the site-specific model M8 implemented in the codeml program in PAML software and five methods available on the Datamonkey web server, including the Single Likelihood Ancestor Counting method, the Fixed Effect Likelihood method, the Random Effect Likelihood method, the Mixed Effects Model of Evolution method and the Fast Unbiased Bayesian AppRoximation method. Additionally, the house mouse (Mus musculus) genome has lost the SAMD9 gene, while keeping SAMD9L intact, prompting us to investigate whether this loss is a unique event during evolution.

Results

Our evolutionary analyses suggest that SAMD9 and SAMD9L arose through an ancestral gene duplication event after the divergence of Marsupialia from Placentalia. Additionally, selection analyses demonstrated that both genes have been subjected to positive evolutionary selection. The absence of either SAMD9 or SAMD9L genes from some mammalian species supports a partial functional redundancy between the two genes.

Conclusions

To the best of our knowledge, this work is the first study on the evolutionary history of mammalian SAMD9 and SAMD9L genes. We conclude that evolutionary selective pressure has acted on both of these two genes since their divergence, suggesting their importance in multiple cellular processes, such as the immune responses to viral pathogens.

【 授权许可】

   
2013 Lemos de Matos et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Li CF, MacDonald JR, Wei RY, Ray J, Lau K, Kandel C, Koffman R, Bell S, Scherer SW, Alman BA: Human sterile alpha motif domain 9, a novel gene identified as down-regulated in aggressive fibromatosis, is absent in the mouse. BMC Genomics 2007, 8:92. BioMed Central Full Text
• [2]Asou H, Matsui H, Ozaki Y, Nagamachi A, Nakamura M, Aki D, Inaba T: Identification of a common microdeletion cluster in 7q21.3 subband among patients with myeloid leukemia and myelodysplastic syndrome. Biochem Biophys Res Commun 2009, 383:245-251.
• [3]Topaz O, Indelman M, Chefetz I, Geiger D, Metzker A, Altschuler Y, Choder M, Bercovich D, Uitto J, Bergman R, et al.: A deleterious mutation in SAMD9 causes normophosphatemic familial tumoral calcinosis. Am J Hum Genet 2006, 79:759-764.
• [4]Chefetz I, Ben Amitai D, Browning S, Skorecki K, Adir N, Thomas MG, Kogleck L, Topaz O, Indelman M, Uitto J, et al.: Normophosphatemic familial tumoral calcinosis is caused by deleterious mutations in SAMD9, encoding a TNF-alpha responsive protein. J Invest Dermatol 2008, 128:1423-1429.
• [5]Tanaka M, Shimbo T, Kikuchi Y, Matsuda M, Kaneda Y: Sterile alpha motif containing domain 9 is involved in death signaling of malignant glioma treated with inactivated Sendai virus particle (HVJ-E) or type I interferon. Int J Cancer 2010, 126:1982-1991.
• [6]Hershkovitz D, Gross Y, Nahum S, Yehezkel S, Sarig O, Uitto J, Sprecher E: Functional characterization of SAMD9, a protein deficient in normophosphatemic familial tumoral calcinosis. J Invest Dermatol 2011, 131:662-669.
• [7]Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, Rice CM: A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 2011, 472:481-485.
• [8]Liu J, Wennier S, Zhang L, McFadden G: M062 is a host range factor essential for myxoma virus pathogenesis and functions as an antagonist of host SAMD9 in human cells. J Virol 2011, 85:3270-3282.
• [9]Zhang LK, Chai F, Li HY, Xiao G, Guo L: Identification of Host Proteins Involved in Japanese Encephalitis Virus Infection by Quantitative Proteomics Analysis. J Proteome Res 2013, 12(6):2666-2678. Epub 2013 May 21
• [10]Pappas DJ, Coppola G, Gabatto PA, Gao F, Geschwind DH, Oksenberg JR, Baranzini SE: Longitudinal system-based analysis of transcriptional responses to type I interferons. Physiol Genomics 2009, 38:362-371.
• [11]Jiang Q, Quaynor B, Sun A, Li Q, Matsui H, Honda H, Inaba T, Sprecher E, Uitto J: The Samd9L gene: transcriptional regulation and tissue-specific expression in mouse development. J Invest Dermatol 2011, 131:1428-1434.
• [12]Critchley-Thorne RJ, Yan N, Nacu S, Weber J, Holmes SP, Lee PP: Down-regulation of the interferon signaling pathway in T lymphocytes from patients with metastatic melanoma. PLoS Med 2007, 4:e176.
• [13]Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SD: GARD: a genetic algorithm for recombination detection. Bioinformatics 2006, 22:3096-3098.
• [14]Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SD: Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol 2006, 23:1891-1901.
• [15]Song S, Liu L, Edwards SV, Wu S: Resolving conflict in eutherian mammal phylogeny using phylogenomics and the multispecies coalescent model. Proc Natl Acad Sci USA 2012, 109:14942-14947.
• [16]Yang Z: PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 1997, 13:555-556.
• [17]Yang Z: PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24:1586-1591.
• [18]Scheffler K, Martin DP, Seoighe C: Robust inference of positive selection from recombining coding sequences. Bioinformatics 2006, 22:2493-2499.
• [19]Wlasiuk G, Nachman MW: Adaptation and constraint at Toll-like receptors in primates. Mol Biol Evol 2010, 27:2172-2186.
• [20]Areal H, Abrantes J, Esteves PJ: Signatures of positive selection in Toll-like receptor (TLR) genes in mammals. BMC Evol Biol 2011, 11:368. BioMed Central Full Text
• [21]Zhang J: Rates of conservative and radical nonsynonymous nucleotide substitutions in mammalian nuclear genes. J Mol Evol 2000, 50:56-68.
• [22]Woolley S, Johnson J, Smith MJ, Crandall KA, McClellan DA: TreeSAAP: selection on amino acid properties using phylogenetic trees. Bioinformatics 2003, 19:671-672.
• [23]Adkins RM, Gelke EL, Rowe D, Honeycutt RL: Molecular phylogeny and divergence time estimates for major rodent groups: evidence from multiple genes. Mol Biol Evol 2001, 18:777-791.
• [24]Churakov G, Sadasivuni MK, Rosenbloom KR, Huchon D, Brosius J, Schmitz J: Rodent evolution: back to the root. Mol Biol Evol 2010, 27:1315-1326.
• [25]Bininda-Emonds OR, Cardillo M, Jones KE, MacPhee RD, Beck RM, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A: The delayed rise of present-day mammals. Nature 2007, 446:507-512.
• [26]Hughes AL, Ota T, Nei M: Positive Darwinian selection promotes charge profile diversity in the antigen-binding cleft of class I major-histocompatibility-complex molecules. Mol Biol Evol 1990, 7:515-524.
• [27]Zhang J, Webb DM: Rapid evolution of primate antiviral enzyme APOBEC3G. Hum Mol Genet 2004, 13:1785-1791.
• [28]Ponting CP: SAM: a novel motif in yeast sterile and Drosophila polyhomeotic proteins. Protein Sci 1995, 4:1928-1930.
• [29]Qiao F, Bowie JU: The many faces of SAM. Sci STKE 2005, 2005:re7.
• [30]Meruelo AD, Bowie JU: Identifying polymer-forming SAM domains. Proteins 2009, 74:1-5.
• [31]Knight MJ, Leettola C, Gingery M, Li H, Bowie JU: A human sterile alpha motif domain polymerizome. Protein Sci 2011, 20:1697-1706.
• [32]Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680.
• [33]Hall T: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 1999, 41:95-98.
• [34]Xia X, Xie Z: DAMBE: software package for data analysis in molecular biology and evolution. J Hered 2001, 92:371-373.
• [35]Posada D, Crandall KA: The effect of recombination on the accuracy of phylogeny estimation. J Mol Evol 2002, 54:396-402.
• [36]Pond SL, Frost SD: Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 2005, 21:2531-2533.
• [37]Posada D: jModelTest: phylogenetic model averaging. Mol Biol Evol 2008, 25:1253-1256.
• [38]Zwickl DJ: Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. University of Texas: PhD Thesis; 2006.
• [39]Miyata T, Yasunaga T: Molecular evolution of mRNA: a method for estimating evolutionary rates of synonymous and amino acid substitutions from homologous nucleotide sequences and its application. J Mol Evol 1980, 16:23-36.
• [40]Nei M, Gojobori T: Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 1986, 3:418-426.
• [41]Crandall KA, Kelsey CR, Imamichi H, Lane HC, Salzman NP: Parallel evolution of drug resistance in HIV: failure of nonsynonymous/synonymous substitution rate ratio to detect selection. Mol Biol Evol 1999, 16:372-382.
• [42]Nielsen R, Yang Z: Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 1998, 148:929-936.
• [43]Yang Z, Nielsen R, Goldman N, Pedersen AM: Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 2000, 155:431-449.
• [44]Yang Z, Wong WS, Nielsen R: Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 2005, 22:1107-1118.
• [45]Kosakovsky Pond SL, Frost SD: Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 2005, 22:1208-1222.
• [46]Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL: Detecting individual sites subject to episodic diversifying selection. PLoS Genet 2012, 8:e1002764.
• [47]Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, Scheffler K: FUBAR: A Fast, Unconstrained Bayesian AppRoximation for Inferring Selection. Mol Biol Evol 2013, 30:1196-1205.