Abstract
The reasons why certain domains evolve much slower than others is unclear. The notion that functionally more important genes evolve more slowly than less important genes is one of the few commonly believed principles of molecular evolution. The macro-domain (also known as the X domain) is an ancient, slowly evolving and highly conserved structural domain found in proteins throughout all of the kingdoms and was first discovered nearly two decades ago with the isolation and cloning of macroH2A1. Macrodomains, which are functionally promiscuous, have been studied intensively for the past decade due to their importance in the regulation of cellular responses to DNA damage, chromatin remodeling, transcription and tumorigenesis. Recent structural, phylogenetic and biological analyses, however, suggest the need for some reconsideration of the evolutionary advantage of concentrating such a plethora of diverse functions into the macrodomain and of how macrodomains could perform so many functions. In this article, we focus on macrodomains that are evolving slowly and broadly discuss the potential relationship between the biological evolution and functional diversity of macrodomains.
Keywords: macrodomain family, environmental stress, biological evolution, functional diversity
Footnotes
This article is published with open access at Springerlink.com
References
- 1.Pehrson J R, Fried V A. MacroH2A, a core histone containing a large nonhistone region. Science. 1992;257:1398–1400. doi: 10.1126/science.1529340. [DOI] [PubMed] [Google Scholar]
- 2.Kustatscher G, Hothorn M, Pugieux C, et al. Splicing regulates nad metabolite binding to histone MacroH2A. Nat Struct Mol Biol. 2005;12:624–625. doi: 10.1038/nsmb956. [DOI] [PubMed] [Google Scholar]
- 3.Han W D, Li X L, Fu X B. The macro domain protein family: Structure, functions, and their potential therapeutic implications. Mutat Res. 2011;727:86–103. doi: 10.1016/j.mrrev.2011.03.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Letunic I, Copley R R, Schmidt S, et al. Smart 4.0: Towards genomic data integration. Nucleic Acids Res. 2004;32:D142–144. doi: 10.1093/nar/gkh088. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Kraus W L. New functions for an ancient domain. Nat Struct Mol Biol. 2009;16:904–907. doi: 10.1038/nsmb0909-904. [DOI] [PubMed] [Google Scholar]
- 6.Karras G I, Kustatscher G, Buhecha H R, et al. The macro domain is an adp-ribose binding module. EMBO J. 2005;24:1911–1920. doi: 10.1038/sj.emboj.7600664. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Zeldovich K B, Shakhnovich E I. Understanding protein evolution: From protein physics to darwinian selection. Annu Rev Phys Chem. 2008;59:105–127. doi: 10.1146/annurev.physchem.58.032806.104449. [DOI] [PubMed] [Google Scholar]
- 8.Heinen T J, Staubach F, Haming D, et al. Emergence of a new gene from an intergenic region. Curr Biol. 2009;19:1527–1531. doi: 10.1016/j.cub.2009.07.049. [DOI] [PubMed] [Google Scholar]
- 9.Knowles D G, McLysaght A. Recent de novo origin of human protein-coding genes. Genome Res. 2009;19:1752–1759. doi: 10.1101/gr.095026.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Cai J, Zhao R, Jiang H, et al. De novo origination of a new protein-coding gene in Saccharomyces cerevisiae. Genetics. 2008;179:487–496. doi: 10.1534/genetics.107.084491. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Murzin A G, Brenner S E, Hubbard T, et al. Scop: A structural classification of proteins database for the investigation of sequences and structures. J Mol Biol. 1995;247:536–540. doi: 10.1006/jmbi.1995.0159. [DOI] [PubMed] [Google Scholar]
- 12.Kaessmann H. Origins, evolution, and phenotypic impact of new genes. Genome Res. 2010;20:1313–1326. doi: 10.1101/gr.101386.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Moore A D, Bjorklund A K, Ekman D, et al. Arrangements in the modular evolution of proteins. Trends Biochem Sci. 2008;33:444–451. doi: 10.1016/j.tibs.2008.05.008. [DOI] [PubMed] [Google Scholar]
- 14.Babushok D V, Ostertag E M, Kazazian H H., Jr. Current topics in genome evolution: Molecular mechanisms of new gene formation. Cell Mol Life Sci. 2007;64:542–554. doi: 10.1007/s00018-006-6453-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Patthy L. Genome evolution and the evolution of exon-shuffling—A review. Gene. 1999;238:103–114. doi: 10.1016/S0378-1119(99)00228-0. [DOI] [PubMed] [Google Scholar]
- 16.Enright A J, Iliopoulos I, Kyrpides N C, et al. Protein interaction maps for complete genomes based on gene fusion events. Nature. 1999;402:86–90. doi: 10.1038/47056. [DOI] [PubMed] [Google Scholar]
- 17.Holm L, Sander C. Parser for protein folding units. Proteins. 1994;19:256–268. doi: 10.1002/prot.340190309. [DOI] [PubMed] [Google Scholar]
- 18.Changolkar L N, Costanzi C, Leu N A, et al. Developmental changes in histone MacroH2A1-mediated gene regulation. Mol Cell Biol. 2007;27:2758–2764. doi: 10.1128/MCB.02334-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Buschbeck M, Uribesalgo I, Wibowo I, et al. The histone variant macroH2A is an epigenetic regulator of key developmental genes. Nat Struct Mol Biol. 2009;16:1074–1079. doi: 10.1038/nsmb.1665. [DOI] [PubMed] [Google Scholar]
- 20.Araya I, Nardocci G, Morales J, et al. MacroH2A subtypes contribute antagonistically to the transcriptional regulation of the ribosomal cistron during seasonal acclimatization of the carp fish. Epigenetics Chromatin. 2010;3:14. doi: 10.1186/1756-8935-3-14. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Chen L, Hu L, Chan T H, et al. Chromodomain helicase/adenosine triphosphatase DNA binding protein 1-like (CHD1L) gene suppresses the nucleus-to-mitochondria translocation of NUR77 to sustain hepatocellular carcinoma cell survival. Hepatology. 2009;50:122–129. doi: 10.1002/hep.22933. [DOI] [PubMed] [Google Scholar]
- 22.Ahel D, Horejsi Z, Wiechens N, et al. Poly(adp-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science. 2009;325:1240–1243. doi: 10.1126/science.1177321. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Wu Z Q, Li Y Z, Li X L, et al. LRP16 integrates into NF-kappaB transcriptional complex and is required for its functional activation. PLoS One. 2011;6:e18157. doi: 10.1371/journal.pone.0018157. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Friedberg E C. DNA damage and repair. Nature. 2003;421:436–440. doi: 10.1038/nature01408. [DOI] [PubMed] [Google Scholar]
- 25.Timinszky G, Till S, Hassa P O, et al. A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat Struct Mol Biol. 2009;16:923–929. doi: 10.1038/nsmb.1664. [DOI] [PubMed] [Google Scholar]
- 26.Lobell D B, Schlenker W, Costa-Roberts J. Climate trends and global crop production since 1980. Science. 2011;333:616–620. doi: 10.1126/science.1204531. [DOI] [PubMed] [Google Scholar]
- 27.Umina P A, Weeks A R, Kearney M R, et al. A rapid shift in a classic clinal pattern in Drosophila reflecting climate change. Science. 2005;308:691–693. doi: 10.1126/science.1109523. [DOI] [PubMed] [Google Scholar]
- 28.Ettensohn C A. Lessons from a gene regulatory network: Echinoderm skeletogenesis provides insights into evolution, plasticity and morphogenesis. Development. 2009;136:11–21. doi: 10.1242/dev.023564. [DOI] [PubMed] [Google Scholar]
- 29.Pinto R, Ivaldi C, Reyes M, et al. Seasonal environmental changes regulate the expression of the histone variant macroH2A in an eurythermal fish. FEBS Lett. 2005;579:5553–5558. doi: 10.1016/j.febslet.2005.09.019. [DOI] [PubMed] [Google Scholar]
- 30.Ladurner A G. Inactivating chromosomes: A macro domain that minimizes transcription. Mol Cell. 2003;12:1–3. doi: 10.1016/S1097-2765(03)00284-3. [DOI] [PubMed] [Google Scholar]
- 31.Maynard-Smith J, Harper D. Animal Signals. Oxford: Oxford University Press; 2003. [Google Scholar]
- 32.Mehrotra P, Riley J P, Patel R, et al. PARP-14 functions as a transcriptional switch for stat6-dependent gene activation. J Biol Chem. 2011;286:1767–1776. doi: 10.1074/jbc.M110.157768. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Goenka S, Boothby M. Selective potentiation of stat-dependent gene expression by collaborator of Stat6 (Coast6), a transcriptional cofactor. Proc Natl Acad Sci USA. 2006;103:4210–4215. doi: 10.1073/pnas.0506981103. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Han W D, Zhao Y L, Meng Y G, et al. Estrogenically regulated LRP16 interacts with estrogen receptor alpha and enhances the receptor’s transcriptional activity. Endocr Relat Cancer. 2007;14:741–753. doi: 10.1677/ERC-06-0082. [DOI] [PubMed] [Google Scholar]
- 35.Yang J, Zhao Y L, Wu Z Q, et al. The single-macro domain protein LRP16 is an essential cofactor of androgen receptor. Endocr Relat Cancer. 2009;16:139–153. doi: 10.1677/ERC-08-0150. [DOI] [PubMed] [Google Scholar]
- 36.Han W D, Mu Y M, Lu X C, et al. Up-regulation of LRP 16 mrna by 17 beta-estradiol through activation of estrogen receptor alpha (ER alpha), but not ER beta, and promotion of human breast cancer MCF-7 cell proliferation: A preliminary report. Endocr Relat Cancer. 2003;10:217–224. doi: 10.1677/erc.0.0100217. [DOI] [PubMed] [Google Scholar]
- 37.Roth J, LeRoith D, Shiloach J, et al. The evolutionary origins of hormones, neurotransmitters, and other extracellular chemical messengers: Implications for mammalian biology. N Engl J Med. 1982;306:523–527. doi: 10.1056/NEJM198203043060907. [DOI] [PubMed] [Google Scholar]
- 38.Kimura M. Cambridge: Cambridge University Press. 1983. The Neutral Theory of Molecular Evolution. [Google Scholar]
- 39.Hasegawa M, Cao Y, Yang Z. Preponderance of slightly deleterious polymorphism in mitochondrial DNA: Nonsynonymous/synonymous rate ratio is much higher within species than between species. Mol Biol Evol. 1998;15:1499–1505. doi: 10.1093/oxfordjournals.molbev.a025877. [DOI] [PubMed] [Google Scholar]
