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Spatio-Temporal Expression Profile of Sirtuins During Aging of the Annual Gene Expression Patterns 33 (2019) 11–19 Contents lists available at ScienceDirect Gene Expression Patterns journal homepage: www.elsevier.com/locate/gep Spatio-temporal expression profile of sirtuins during aging of the annual fish Nothobranchius furzeri T ∗ Julijan Kabiljo, Christina Murko, Oliver Pusch, Gordin Zupkovitz Center for Anatomy and Cell Biology, Medical University of Vienna, Vienna, 1090, Austria ARTICLE INFO ABSTRACT Keywords: The founding member of the sirtuin family, yeast Sir2, was the first evolutionarily conserved gene to be iden- Sirtuins tified as a regulator of longevity. Sirtuins constitute a protein family of metabolic sensors, translating changes in Histone deacetylases NAD + levels into adaptive responses, thereby acting as crucial regulators of the network that controls energy Nothobranchius furzeri, epigenetics homeostasis and as such determines healthspan. In mammals the sirtuin family comprises seven proteins, SIRT1- Aging SIRT7, which vary in tissue specificity, subcellular localization, enzymatic activity and targets. Here, we report the identification and a detailed spatio-temporal expression profile of sirtuin genes in the short-lived fish Nothobranchius furzeri, from embryogenesis to late adulthood, mapping its entire life cycle. Database exploration of the recently published N. furzeri genome revealed eight orthologues corresponding to the seven known mammalian sirtuins, including two copies of the sirt5 gene. Phylogenetic analysis showed high cross species similarity of individual sirtuins in both their overall amino acid sequence and catalytic domain, suggesting a high degree of functional conservation. Moreover, we show that N. furzeri sirtuins exhibit ubiquitous and wide tissue distribution with a unique spatial expression pattern for each individual member of this enzyme family. Specifically, we observed a transcriptional down-regulation of several sirtuin genes with age, most significantly sirt1, sirt5a, sirt6 and sirt7 in a wide range of functionally distinct tissues. Overall, this spatio-temporal expression analysis provides the foundation for future research, both into genetic and pharmacological manipulation of this important group of enzymes in Nothobranchius furzeri, an emerging model organism for aging research. 1. Introduction demalonylase and desuccinylase activity and only weak deacetylase activity (Michishita et al., 2005). Together, they regulate crucial cel- Ever since their characterization as direct regulators of life span in lular and biological functions with highly divergent as well as con- yeast and fruitfly(Kaeberlein et al., 1999; Rogina and Helfand, 2004) vergent roles in maintaining metabolic homeostasis thereby de- the NAD+-dependent class III histone deacetylases, the so called sir- termining healthspan. Each sirtuin is regulated individually in a tissue tuins, continue to be at the center of interest in aging research. Sirtuins and cell specific manner. With the exception of ubiquitous Sirt6 and are homologues of the yeast silent information regulator Sir2 and are brain specific Sirt1, gain of sirtuin function in mammals failed to extend comprised of seven members, SIRT1-7. Based on phylogenetic analysis lifespan, (Kanfi et al., 2012; Satoh et al., 2013), although their in- sirtuins have been divided into four classes (Frye, 2000). Class one volvement in many age associated physiological processes in verte- consists of SIRT1, SIRT2 and SIRT3. Class II and III have one member brates is well documented (for reviews see Finkel et al., 2009; each, SIRT4 and SIRT5, respectively, while SIRT6 and SIRT7 constitute Houtkooper et al., 2012; O'Callaghan and Vassilopoulos, 2017). Calorie class IV. Moreover, vertebrate sirtuins display distinct patterns of sub- restriction, which can delay the onset of age-dependent diseases such as cellular localization with a subset of sirtuins residing in predominantly diabetes, cardiovascular disease and cancer in rodents, and results in nuclear (SIRT1, SIRT6, and SIRT7), cytosolic (SIRT2), or mitochondrial prolonged healthy lifespan, was directly linked to the activity of SIRT1 (SIRT3, SIRT4, and SIRT5) compartments (Houtkooper et al., 2012). and SIRT6 proteins (Cohen et al., 2004; Zhang et al., 2016). Recent Regarding their enzymatic activity most sirtuins display protein dea- screenings of chemical libraries have revealed new activators of SIRT1, cetylase activity. Exceptions include SIRT4, which is known only for including resveratrol, a substance known to prolong lifespan in multiple ADP-ribosyltransferase activity, and SIRT5, which has very effective organisms due to its ability to mimic aspects of calorie restriction (Baur ∗ Corresponding author. Center for Anatomy and Cell Biology, Medical University of Vienna Schwarzspanierstr. 17, 1090, Vienna, Austria. E-mail addresses: [email protected] (J. Kabiljo), [email protected] (C. Murko), [email protected] (O. Pusch), [email protected] (G. Zupkovitz). https://doi.org/10.1016/j.gep.2019.05.001 Received 29 January 2019; Received in revised form 24 April 2019; Accepted 6 May 2019 Available online 07 May 2019 1567-133X/ © 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/). J. Kabiljo, et al. Gene Expression Patterns 33 (2019) 11–19 et al., 2006; Howitz et al., 2003). Furthermore, sirtuin deficiency stu- comparison of sirtuin catalytic domains between these two species re- dies in mice, particularly knockout of Sirt1, Sirt6 and Sirt7, have ad- sulted in an even higher degree of similarity (Supplementary Table 2) ditionally demonstrated the significance of these enzymes regarding emphasizing the conservation of class III HDACs throughout evolution. promotion of healthy life and longevity (Cheng et al., 2003; McBurney et al., 2003; Mostoslavsky et al., 2006; Vakhrusheva et al., 2008). 2.2. Expression of sirtuins throughout the N. furzeri life cycle The African turquoise killifish, Nothobranchius furzeri, is an exciting new model organism for aging research. N. furzeri is a naturally short Studies conducted in invertebrate species such as S. cerevisiae, C. lived vertebrate that inhabits ephemeral ponds in South-East Africa and elegans and D. melanogaster have identified the sirtuin class of HDACs as was first collected and identified as a new species in 1969 (Furzer, one of the key regulators of lifespan (Kaeberlein et al., 1999; Rogina 1969; Jubb, 1971; Parle, 1970). Its habitat is characterized by a short and Helfand, 2004; Tissenbaum and Guarente, 2001). To assess the rainy season followed by a long dry season. The turquoise killifish has potential change in expression levels of sirtuins in N. furzeri throughout adapted to this extreme environment by undergoing a unique annual life we analyzed five different time points broadly spanning from em- life cycle composed of two distinct phases with opposite features, a bryogenesis to late adulthood. The first time point (E14) chosen was 14 compressed lifespan specified by rapid growth, early sexual maturation days post fertilization when N. furzeri reaches the black eye stage and and fast aging followed by a long-term diapause state in the dry season has completed embryogenesis. The day of hatching (D01) was selected (Blažek et al., 2013; Reichard et al., 2009). With a lifespan of 4–6 as second time point. For determination of further time points, we months (which is 6–10 times shorter than the lifespan of mice and generated a survival curve of the GRZ strain of N. furzeri maintained in zebrafish, respectively) N. furzeri is currently the shortest-lived verte- our lab from 5 weeks post hatching onwards (Fig. 2A). The survival brate that can be bred in captivity (Genade et al., 2005; Terzibasi et al., curve obtained is comparable to those published for other N. furzeri 2007). Despite its short lifespan, the fish shows typical aging related facilities (Hartmann et al., 2009; Smith et al., 2017). Five weeks post phenotypes with substantial parallels to mammalian aging, such as hatching represents the age when the fish reaches sexual maturity and decline in fertility, degenerative loss of skeletal muscle mass, reduced was taken as our third time point (W05). At the fourth time-point, week ability to learn and development of tumors (Kim et al., 2016). More- 11 (W11), the fish start showing first aging related characteristics. over, it was demonstrated that calorie restriction, a resveratrol-rich diet Obvious macroscopic aging phenotypes include progressive loss of body and temperature reduction have a positive impact on N. furzeri lifespan and tail colouration in males. At a behavioral level, older fish exhibit (Terzibasi et al., 2009; Valenzano et al., 2006a, 2006b). Recently, two decreased spontaneous locomotion activity (Genade et al., 2005). At independent groups, (Reichwald et al., 2015; Valenzano et al., 2015), week 13 (W13), the last time-point in our analysis, which corresponds reported the successful completion of a reference genome for the short- to approximately 10% survivorship, most fish show a drastic decline in lived turquoise killifish. In addition, methods for transgenesis (Allard their performance and display severe aging related features, such as et al., 2013; Hartmann and Englert, 2012; Valenzano et al., 2011) and a abnormal spine curvature, loss of muscle mass and emaciation. Inter- toolbox for precise genome-editing (Harel et al., 2015) were success- estingly, a specific outward aging trait
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