Striving for normality: Whole body regeneration through a series of abnormal generations

Department of Biochemistry, Stanford University, Palo Alto, California, United States
The FASEB Journal (Impact Factor: 5.04). 06/2007; 21(7):1335-44. DOI: 10.1096/fj.06-7337com
Source: PubMed


Embryogenesis and asexual reproduction are commonly considered to be coordinated developmental processes, which depend on accurate progression through a defined sequence of developmental stages. Here we report a peculiar developmental scenario in a simple chordate, Botryllus schlosseri, wherein a normal colony of individuals (zooids and buds) is regenerated from the vasculature (vascular budding) through a sequence of morphologically abnormal developmental stages. Vascular budding was induced by surgically removing buds and zooids from B. schlosseri colonies, leaving only the vasculature and the tunic that connects them. In vivo imaging and histological sections showed that the timing and morphology of developing structures during vascular budding deviated significantly from other asexual reproduction modes (the regular asexual reproduction mode in this organism and vascular budding in other botryllid species). Subsequent asexual reproduction cycles exhibited gradual regaining of normal developmental patterns, eventually leading to regeneration of a normal colony. The conversion into a normal body form suggests the activation of an alternative pathway of asexual reproduction, which involves gradual regaining of normal positional information. It presents a powerful model for studying the specification of the same body plan by different developmental programs.

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Available from: Baruch Rinkevich, Sep 29, 2015
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    • "The entire body can be regenerated even if no pre-existing zooids are present. This suggests that pluripotent and/or multipotent stem and progenitor cells that initiate budding can migrate and that regions within the colony vasculature are suitable niches (Voskoboynik et al. 2007). "
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    ABSTRACT: The decline of tissue regenerative potential with the loss of stem cell function is a hallmark of mammalian aging. We study Botryllus schlosseri, a colonial chordate which exhibits robust stem cell-mediated regeneration capacities throughout life. Larvae, derived by sexual reproduction and chordate development, metamorphose to clonal founders that undergo weekly formation of new individuals by budding from stem cells. Individuals are transient structures which die through massive apoptosis, and successive buds mature to replicate an entire new body. As a result, their stem cells, which are the only self-renewing cells in a tissue, are the only cells which remain through the entire life of the genotype and retain the effects of time. During aging, a significant decrease in the colonies’ regenerative potential is observed and both sexual and asexual reproductions will eventually halt. When a parent colony is experimentally separated into a number of clonal replicates, they frequently undergo senescence simultaneously, suggesting a heritable factor that determines lifespan in these colonies. The availability of the recently published B. schlosseri genome coupled with its unique life cycle features promotes the use of this model organism for the study of the evolution of aging, stem cells, and mechanisms of regeneration.
    Invertebrate Reproduction and Development 01/2015; 59(sup1). DOI:10.1080/07924259.2014.944673 · 0.61 Impact Factor
    • "The situation in animals is quite different. In the case of Botryllus, for example, while the most parsimonious explanation to wholebody regeneration is the existence of stem cells, their exact anatomical location remains controversial, and the possibility of neogenesis (production of stem cells from other differentiated cells, for example) remains a formal possibility (Laird et al., 2005; Laird and Weissman, 2004; Rinkevich et al., 2013; Voskoboynik et al., 2007, 2008). In planarians, the anatomical location of stem cells (neoblasts) has been known for a very long time (Elliott and Sá nchez Alvarado, 2013), and though evidence exists that at least some of these cells are pluripotent (Wagner et al., 2011), it still remains to be determined whether or not there exists discrete heterogeneities of stem cells among the neoblast population and whether such heterogeneities are defined or plastic. "
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    ABSTRACT: Cell differentiation is an essential process for the development, growth, reproduction, and longevity of all multicellular organisms, and its regulation has been the focus of intense investigation for the past four decades. The study of natural and induced stem cells has ushered an age of re-examination of what it means to be a stem or a differentiated cell. Past and recent discoveries in plants and animals, as well as novel experimental manipulations, are beginning to erode many of these established concepts and are forcing a re-evaluation of the experimental systems and paradigms presently being used to explore these and other biological process.
    Cell 03/2014; 157(1):110-119. DOI:10.1016/j.cell.2014.02.041 · 32.24 Impact Factor
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    • "The weekly blastogenic cycle allows botryllid ascidians to execute continuous somatic proliferation throughout their lives, as well as resorption of old zooidal soma through the establishment of new zooids at the take-over phase of the blastogenesis (Rinkevich, 2002). This, in combination with the species-specific high regeneration-power based on totipotent stem cells (Sköld et al., 2009; Voskoboynik et al., 2007) and the evidence for telomerase activity active only in early buds and suppressed in the cells of adult zooids (Laird and Weissman, 2004), cumulatively supports the theory of an evolutionary development strategy that does not benefit efficient DNA repair mechanisms or other costly investments in somatic maintenance for this species. Moreover, in their natural habitat, B. schlosseri colonies are found under rocks or vegetation, areas sheltered from direct sunlight. "
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    ABSTRACT: Ultraviolet radiation (UVR) may cause significant DNA damages when interacting with shallow water organisms, primarily in the tropics. Here we investigate DNA repair kinetics in two shallow water colonial marine invertebrates, the scleractinian coral Seriatopora hystrix and the colonial tunicate Botryllus schlosseri. Cells from both species were irradiated with UVA/UVB in vitro. Using the alkaline (B. schlosseri) and the neutral (S. hystrix) versions of the comet assay, DNA damage and repair were measured. After 24 h, little DNA repair was recorded in the irradiated Botryllus cells for both types of radiation (UVB 3.55 W/s/UVA 8.09 W/s, 15 min radiation each), revealing twice (30%) as much apoptotic cells as controls. Cells of S. hystrix showed a highly efficient DNA repair capacity (i.e. complete DNA repair within 30 min post-irradiation), coincident with their endurance to reactive oxygen species impacts. Therefore, while S. hystrix and likely other shallow water corals use efficient DNA repair mechanisms, B. schlosseri and possibly other similar species are reliant on UVR sheltered sites to maintain DNA integrity. The low repair capacity of B. schlosseri might be explained by the ‘disposable soma’ concept, where zooidal soma in this species is cast off and recycled on a weekly basis. Further research is needed to elucidate the spectrum of responses used by shallow water sedentary marine invertebrates to cope with daily high UVR levels.
    Journal of Experimental Marine Biology and Ecology 03/2014; 452:40–46. DOI:10.1016/j.jembe.2013.12.003 · 1.87 Impact Factor
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