Identification of caspases and apoptosis in the simple metazoan Hydra

Abstract

Apoptosis is a normal process by which cells die and are eliminated from tissue by phagocytosis [1]. It is involved in regulating cell numbers in adult tissues and in eliminating 'excess' cells during embryogenesis and development. Apoptosis is mediated by activation of caspases, which then cleave a variety of cellular substrates and thereby cause the characteristic morphology of apoptotic cells (rounded cells, condensed chromatin, susceptibility to phagocytosis) [2]. Although apoptosis has been well documented in nematodes, insects and mammals, it is not yet clear how early in evolution apoptosis or its component enzymes arose. In the simple metazoan Hydra vulgaris, cell death regulates cell numbers [3] [4] [5]. In starved animals, for example, epithelial cell proliferation continues at a nearly normal rate although the tissue does not increase in size; the excess cells produced are eliminated by phagocytosis. Cell death can also be induced in wild-type hydra by treatment with colchicine [6] or in a mutant strain (sf-1) by temperature shock [7]. Here, we show that cell death in hydra is morphologically indistinguishable from apoptosis in higher animals, that hydra polyps express two genes with strong homology to members of the caspase 3 family, and that caspase-3-specific enzyme activity accompanies apoptosis in hydra. The occurrence of apoptosis and caspases in a member of the ancient metazoan phylum Cnidaria supports the idea that the invention of apoptosis was an essential feature of the evolution of multicellular animals.

Isolation of AmphiCASP-3/7, an ancestral caspase from amphioxus (Branchiostoma floridae). Evolutionary considerations for vertebrate caspases

“…The isolation of Hv Casp3A and Hv Casp3B in Hydra vulgaris, 28 and detection of apoptosis tightly linked with morphogenesis in Hydractina echinata metamorphosis 29 supports the idea that the advent of the apoptosis was instrumental for the evolution of metazoans. Although three novel caspases have been cloned in the nematode Caenorhabditis elegans, 30 only ced-3 is necessary to promote all the developmental programmed cell death in the worm.…”

Apoptosis of tail muscle during amphibian metamorphosis involves a caspase 9-dependent mechanism

“…Caspase activation is a conserved feature of death processes across invertebrate and vertebrates (Cikala et al, 1999). The implication of caspases in tail muscle elimination was underlined by their strong expression in this organ during metamorphosis in Xenopus (Nakajima et al, 2000).…”

On the origin, evolution, and nature of programmed cell death: a timeline of four billion years

“…61,62 On the conserved nature of programmed cell death in multicellular animals Programmed cell death has been found to operate in all multicellular animals studied so far, including cnidaria, nematodes, insects, amphibians, birds and mammals. 16,18,20,24,25,63,64 The evolutionary conservation of programmed cell death in the animal kingdom does not only involve its existence and role, but extends to some central aspects of its genetic control, and to important aspects of its most frequent phenotype, apoptosis. 5,16,18,20,24,25,63,64 In all cases that have been studied to date, programmed cell death is regulated by signals provided by other cells, either in the form of cell-lineage information, of soluble mediators, or of cell-to-cell contacts.…”