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The African Turquoise Killifish: a Research Organism to Study Vertebrate Aging and Diapause

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The African Turquoise Killifish: a Research Organism to Study Vertebrate Aging and Diapause Accepted: 27 February 2018 DOI: 10.1111/acel.12757 REVIEW ARTICLE The African turquoise killifish: A research organism to study vertebrate aging and diapause Chi-Kuo Hu1 | Anne Brunet1,2 1Department of Genetics, Stanford University, Stanford, CA, USA Summary 2Glenn Laboratories for the Biology of The African turquoise killifish has recently gained significant traction as a new Aging, Stanford, CA, USA research organism in the aging field. Our understanding of aging has strongly bene- Correspondence fited from canonical research organisms—yeast, C. elegans, Drosophila, zebrafish, and Anne Brunet, Department of Genetics, mice. Many characteristics that are essential to understand aging—for example, the Stanford University, Stanford, CA, USA. Email: [email protected] adaptive immune system or the hypothalamo-pituitary axis—are only present in ver- tebrates (zebrafish and mice). However, zebrafish and mice live more than 3 years Funding information National Institutes of Health (NIH), Grant/ and their relatively long lifespans are not compatible with high-throughput studies. Award Number: DP1AG044848; Glenn Therefore, the turquoise killifish, a vertebrate with a naturally compressed lifespan Laboratories for the Biology of Aging (A.B.); NIH T32 Cancer Biology Training, Grant/ of only 4–6 months, fills an essential gap to understand aging. With a recently Award Number: 5 T32 CA 9302-35; Life developed genomic and genetic toolkit, the turquoise killifish not only provides Science Research Foundation fellowships practical advantages for lifespan and longitudinal experiments, but also allows more systematic characterizations of the interplay between genetics and environment during vertebrate aging. Interestingly, the turquoise killifish can also enter a long- term dormant state during development called diapause. Killifish embryos in dia- pause already have some organs and tissues, and they can last in this state for years, exhibiting exceptional resistance to stress and to damages due to the passage of time. Understanding the diapause state could give new insights into strategies to prevent the damage caused by aging and to better preserve organs, tissues, and cells. Thus, the African turquoise killifish brings two interesting aspects to the aging field—a compressed lifespan and a long-term resistant diapause state, both of which should spark new discoveries in the field. KEYWORDS accelerated aging, aging, anti-aging, diapause, killifish, rejuvenation 1 | RESEARCH ORGANISMS FOR AGING first long-lived mutants in Caenorhabditis elegans and Saccharomyces cerevisiae more than two decades ago (Kaeberlein, McVey & Guar- Aging is one of the greatest risk factors for many diseases, and it ente, 1999; Kenyon, Chang, Gensch, Rudner & Tabtiang, 1993; Mor- ultimately restricts the lifespan of organisms by increasing the proba- ris, Tissenbaum & Ruvkun, 1996; Ogg et al., 1997; Wang et al., bility of death (Dillin, Gottschling & Nystrom, 2014; Guarente, Ruv- 1993), the concept that aging is a malleable biological process has kun & Amasino, 1998; Kennedy et al., 2014; Kenyon, 2005; Niccoli been well embraced (Finch & Ruvkun, 2001; Gems & Partridge, & Partridge, 2012). Since the discovery and characterization of the 2013; Kennedy, 2008; Kenyon, 2005, 2010). ---------------------------------------------------------------------------------------------------------------------------------------------------------------------- This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2018 The Authors. Aging Cell published by the Anatomical Society and John Wiley & Sons Ltd. | Aging Cell. 2018;e12757. wileyonlinelibrary.com/journal/acel 1of15 https://doi.org/10.1111/acel.12757 2of15 | HU AND BRUNET However, many mysteries about aging remain. While virtually all process is considerably more complex in vertebrates. While some species experience aging, organismal lifespan is an amazingly diverse key aging genes and pathways are evolutionarily conserved, many trait in nature. For example, the documented maximal lifespans range systems are vertebrate-specific (Figure 2). For example, vertebrates from days in the medfly to over 500 years in clams, comprising all have a more specialized nervous system which is divided into a dis- intermediaries including ~4 months in fruit flies, ~4 years in mice, tinct central nervous system that consists of a segmented brain and ~120 years in humans, ~150 years in giant tortoises, and ~400 years spinal cord, and a peripheral nervous system that contains ganglia in Greenland sharks (Butler, Wanamaker, Scourse, Richardson & Rey- and nerves. These two systems are targeted by different age-related nolds, 2013; Castanet, 1994; Karney et al., 2011; Luckinbill & Clare, neural degenerative diseases (e.g., Alzheimer’s disease in the central 1985; Miller, Harper, Dysko, Durkee & Austad, 2002; Nielsen et al., nervous system versus amyotrophic lateral sclerosis in the peripheral 2016). The extraordinary diversity of lifespan and life history of vari- nervous system) (Niccoli, Partridge & Isaacs, 2017; Wenk, 2003; ous organisms raises many exciting possibilities for modeling and Zarei et al., 2015). Vertebrates also have a hypothalamo-pituitary understanding the aging process. The lowering costs of genome axis, which is critical for neuro-endocrine signaling during aging sequencing and the emergence of cutting-edge genome-editing tech- (Veldhuis, 2008). Unlike invertebrates, which rely on an innate nologies such as CRISPR/Cas9 have enabled the development of vir- immune system, vertebrates have also evolved an adaptive immune tually any organism into a tractable research system (Sanchez system, which plays roles in vertebrate aging in many aspects such Alvarado, 2018). This development will allow the aging field not to as “immunosenescence” (gradual deterioration of the immune system be limited by the specific features of canonical research organisms during aging; Weng, 2006; Weyand & Goronzy, 2016) and “inflam- (yeast, C. elegans, Drosophila, zebrafish and mice) and to exploit the maging” (chronic inflammation that occurs during aging; Monti, amazing diversity of aging and lifespan traits in nature. Ostan, Borelli, Castellani & Franceschi, 2016). Furthermore, aging in As the number of species with emerging interest for research vertebrates is often accompanied by the development of cancers increases (Russell et al., 2017; Sanchez Alvarado, 2018), identifying a (Campisi, 2013), perhaps due to the presence of tissue-specific stem system advantageous to answer specific questions is more critical cells which are more at risk for tumor-inducing mutation (Batlle & than ever. As laid out by Steve Austad in 1997, choosing a research Clevers, 2017). For example, more than half of the newly diagnosed organism involves tradeoffs between factors such as realism, repeata- cancers in humans are found in individuals over 65 years of age bility of results, and feasibility (Austad, 1997; Figure 1). For years, the (Tariman, 2009). This is not the case in worms and flies, which are aging field has greatly benefited from using short-lived unicellular mostly composed of postmitotic cells. Therefore, studying aging organisms (e.g., S. cerevisiae) and invertebrates (e.g., C. elegans and solely in invertebrates does not faithfully reflect all aspects of verte- Drosophila) to understand the biological mechanism of aging (Fabrizio brate aging, and this lack of “realism” is a tradeoff that hampers our & Longo, 2003; Helfand & Rogina, 2003; Kaeberlein, Burtner & Ken- complete understanding of aging. On the other hand, canonical ver- nedy, 2007; Laun, Rinnerthaler, Bogengruber, Heeren & Breitenbach, tebrate research organisms have significantly longer lifespans com- 2006; Olsen, Vantipalli & Lithgow, 2006). However, the aging pared to their invertebrate counterparts. For example, mice and Budding yeast (S. cerevisiae) Unicellular Median lifespan Round worm (C. elegans) Maximal lifespan Fruit fly (D. melanogaster) Invertebrate Turquoise killifish (N. furzeri) Zebrafish (D. rerio) House mouse (M. musculus) Vertebrate 01 2 34 5 6 Resemblance to human aging Lifespan (years) Repeatability and feasibility of experiments FIGURE 1 The turquoise killifish is one of the shortest lived, if not the shortest lived, vertebrate. The turquoise killifish is a vertebrate organism with a lifespan closer to that of unicellular and invertebrate canonical research organisms (yeast, round worm, and fruit fly) than vertebrate canonical research organisms (house mouse and zebrafish). The lifespan of each organism is shown with both median (closed circles) and maximal lifespan (open circles). The turquoise killifish, as one of the shortest lived if not the shortest lived vertebrate, is in the unique position to recapitulate some human aging traits and to allow high repeatability and feasibility for experiments HU AND BRUNET | 3of15 (a) Round worm Fruit fly Killifish/Zebrafish House mouse Human C. elegans D. melanogaster N. furzeri /D. rerio M. musculus H. sapiens Central nervous system and peripheral nervous system Nervous system Fore-, mid-, and hind-brain Hypothalamo-pituitary axis Innate immunity Immune system Adaptive immunity Circulatory system Open circulation Close circulation Respiratory system Tracheae Gills Lungs Skeletal system Bone and cartilage Skeletal-like muscles Skeletal, cardiac, and smooth muscles Muscular system No
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