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Warning Sines: Alu Elements, Evolution of the Human Brain, and the Spectrum of Neurological Disease

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Warning Sines: Alu Elements, Evolution of the Human Brain, and the Spectrum of Neurological Disease Chromosome Res (2018) 26:93–111 https://doi.org/10.1007/s10577-018-9573-4 ORIGINAL ARTICLE Warning SINEs: Alu elements, evolution of the human brain, and the spectrum of neurological disease Peter A. Larsen & Kelsie E. Hunnicutt & Roxanne J. Larsen & Anne D. Yoder & Ann M. Saunders Received: 6 December 2017 /Revised: 14 January 2018 /Accepted: 15 January 2018 /Published online: 19 February 2018 # The Author(s) 2018. This article is an open access publication Abstract Alu elements are a highly successful family of neurological networks are potentially vulnerable to the primate-specific retrotransposons that have fundamen- epigenetic dysregulation of Alu elements operating tally shaped primate evolution, including the evolution across the suite of nuclear-encoded mitochondrial genes of our own species. Alus play critical roles in the forma- that are critical for both mitochondrial and CNS func- tion of neurological networks and the epigenetic regu- tion. Here, we highlight the beneficial neurological as- lation of biochemical processes throughout the central pects of Alu elements as well as their potential to cause nervous system (CNS), and thus are hypothesized to disease by disrupting key cellular processes across the have contributed to the origin of human cognition. De- CNS. We identify at least 37 neurological and neurode- spite the benefits that Alus provide, deleterious Alu generative disorders wherein deleterious Alu activity has activity is associated with a number of neurological been implicated as a contributing factor for the manifes- and neurodegenerative disorders. In particular, tation of disease, and for many of these disorders, this activity is operating on genes that are essential for proper mitochondrial function. We conclude that the Responsible Editor: Beth Sullivan. epigenetic dysregulation of Alu elements can ultimately disrupt mitochondrial homeostasis within the CNS. This Electronic supplementary material The online version of this article (https://doi.org/10.1007/s10577-018-9573-4) contains mechanism is a plausible source for the incipient neuro- supplementary material, which is available to authorized users. nal stress that is consistently observed across a spectrum : : of sporadic neurological and neurodegenerative P. A. Larsen K. E. Hunnicutt A. D. Yoder disorders. Department of Biology, Duke University, Durham, NC 27708, USA : Keywords A-to-I editing . Alzheimer’sdisease. Brain P. A. Larsen A. D. Yoder . Duke Lemur Center, Duke University, Durham, NC 27708, USA connectome Epigenetics Mitochondria Mosaicbrain Parkinson’s disease P. A. Larsen (*) Department of Biology, Duke University, 130 Science Drive, Box Abbreviations 90338, Durham, NC 27708, USA e-mail: [email protected] A-to-I Adenosine-to-inosine AD Alzheimer’sdisease R. J. Larsen ADAR Adenosine deaminase acting on RNA Duke University School of Medicine, Duke University, Durham, ALS Amyotrophic lateral sclerosis NC 27710, USA AMPA α-Amino-3-hydroxy-5methyl-4-isoxazole A. M. Saunders propionate Zinfandel Pharmaceuticals Inc, Chapel Hill, NC 27709, USA APP Amyloid precursor protein 94 P. A. Larsen et al. circRNAs Circular RNAs Jeck et al. 2013; Töhönen et al. 2015;Luco2016; Chen CNS Central nervous system and Yang 2017). Moreover, Alus fundamentally alter the FLAM Free left Alu monomer three-dimensional architecture and spatial organization LINE Long interspersed element of primate genomes by defining the boundaries of chro- L1 Long interspersed element-1 matin interaction domains (i.e., topologically associat- LTR Long-terminal repeat ing domains (TADs); Dixon et al. 2012). Genome ar- mRNA Messenger RNA chitecture has a direct influence on biological function, PD Parkinson’s disease and the observation that Alus are enriched within both pre- Precursor messenger RNA TADs and super-enhancer domains (SEDs) supports the mRNA hypothesis that Alus directly influence a wide range of SEDs Super-enhancer domains critically important processes within primates across SINE Short interspersed element multiple levels, from overall genome stability to tissue- TADs Topologically associating domains specific gene regulation (Huda et al. 2009; Dixon et al. TOMM Translocase of outer mitochondrial 2012; Soibam 2017; Glinsky 2018). In light of the membrane functional benefits that Alus provide primates, it is in- teresting to note that Alu retrotransposition events oc- curred at an estimated 15-fold higher rate in the human, chimpanzee, and bonobo lineage (as compared to other Introduction great apes) and a 2.2-fold higher rate in humans when compared to chimpanzee and bonobo (Hedges et al. Retrotransposons are mobile genetic elements that uti- 2004; Prüfer et al. 2012; Hormozdiari et al. 2013). These lize an RNA intermediate to copy and paste themselves evolutionary patterns indicate that positive selection is throughout the genome. There are two primary groups acting to maintain Alu elements in primate genomes, of retrotransposons, those having long-terminal repeats especially within humans (Mattick and Mehler 2008; (LTRs) and those without (non-LTR) (Cordaux and Tsirigos and Rigoutsos 2009). Batzer 2009). In the human genome, non-LTR One of the most fascinating and biologically impor- retrotransposons consist of long interspersed elements tant aspects of Alu elements is that they serve an impor- (LINEs) and short interspersed elements (SINEs), and tant role in the formation and function of the brain these collectively account for a remarkable ~ 33% of connectome (Oliver and Greene 2011; Li and Church total genome sequence (Cordaux and Batzer 2009). Alu 2013; Smalheiser 2014; Sakurai et al. 2014; Prendergast elements are primate-specific SINEs that are approxi- et al. 2014; Linker et al. 2017; Bitar and Barry, 2017). mately 300 nucleotides in length and are abundant in the Many lines of evidence connect Alu elements with human genome, with over 1.3 million elements account- neurogenesis and critical neuronal biochemical process- ing for at least 11% of overall DNA sequence es, including somatic retrotransposition in developing (Deininger et al. 2003; Hancks and Kazazian 2016). neurons (in parallel to L1 retrotransposition; Baillie Although once considered to be useless Bjunk DNA,^ et al. 2011;Kurnosovetal.2015), formation of regula- the prevalence, diversity, and non-random distribution tory circRNAs that are enriched in the central nervous of Alu elements across primate genomes are suggestive system (CNS) and concentrated at synapses (Jeck et al. of a functional advantage. Indeed, a large body of evi- 2013; Rybak-Wolf et al. 2015; Chen and Schuman dence documents that Alu elements have directly influ- 2016;Florisetal.2017), regulation of genes that are enced primate evolution by facilitating genome innova- essential for proper neuron function (e.g., ACE, SMN1, tion through novel gene formation, elevated transcrip- SMN2, SLC6A4;Wuetal.2013; Ottesen et al. 2017; tional diversity, long non-coding RNA and microRNA Schneider et al. 2017), and elevated adenosine-to- evolution (including circular RNAs), transcriptional inosine (A-to-I) RNA editing in the brain (Mehler and regulation, and creation of novel response elements Mattick 2007;Kurnosovetal.2015; Behm and Öhman (Vansant and Reynolds 1995;Norrisetal.1995;Britten 2016). In particular, epigenetic A-to-I editing plays a 1997;Lev-Maoretal.2003; Polak and Domany 2006; significant role in mediating neuronal gene expression Laperriere et al. 2007; Lin et al. 2008, 2016;Lehnert pathways (Tariq and Jantsch 2012)withAlus serving as et al. 2009; Cordaux and Batzer 2009;Shenetal.2011; the primary target for RNA editing in primates (Picardi Warning SINEs: Alu elements, evolution of the human brain, and the spectrum of neurological disease 95 et al. 2015; Behm and Öhman 2016). Beyond RNA editing mechanisms, human neuronal gene pathways are regulated by non-coding RNAs originating from Alu elements (e.g., BC200 and NDM29) and specific Alu subfamilies contain retinoic acid response elements which help to regulate neural patterning, differentiation, and axon outgrowth (Vansant and Reynolds 1995; Laperriere et al. 2007;Maden2007; Castelnuovo et al. 2010; Smalheiser 2014). Moreover, recent discoveries indicate that Alu elements underlie the formation of a vast number of human-specific circRNAs that are hy- pothesized to play important roles in neurological gene expression pathways (Jeck et al. 2013; Rybak-Wolf et al. 2015; Chen and Schuman 2016; Dong et al. 2017). There is a deep connection between Alus and the for- mation and function of primate neurological networks, and this has led to the hypothesis that Alu elements were essential for development of the transcriptional diversity and regulation required for the genesis of human cogni- tive function (Mattick and Mehler 2008; Oliver and Greene 2011;LiandChurch2013; Sakurai et al. 2014). Despite the functional benefits that Alus have provided primate genomes, Alu elements can disrupt gene expres- sion and function through many pathways (Fig. 1; Deininger and Batzer 1999; Deininger 2011; Tarallo et al. 2012; Ade et al. 2013; Elbarbary et al. 2016; Varizhuk et al. 2016). For this reason, the genome tightly Fig. 1 Select mechanisms whereby Alu elements can alter gene regulates Alus using both DNA methylation and histone expression and function (also see Elbarbary et al. 2016). a Se- quence homology and orientation of Alu elements contribute to the (H3K9 methylation) modification in order to control their formation of distinct secondary structures in both DNA and RNA. expression
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