The evolution of cell death programs as prerequisites of multicellularity

Huettenbrenner, S; Maier, Susanne; Leisser, Christina; Polgar, Doris; Strasser, Stephen; Grusch, Michael; Krupitza, Georg

doi:10.1016/s1383-5742(02)00110-2

Cited by 75 publications

(60 citation statements)

References 124 publications

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“…However, apoptosis rapidly evolved a new, co-opted function in our multicellular yeast with no obvious parallel in the unicellular ancestor. Similarly, the existence of apoptosis-like cellular suicide in the unicellular ancestors of metazoans (38) may be an important preadaptation, facilitating the evolution of complex multicellularity (39). Apoptotic cells, like nonreproductive somatic tissue, leave no direct descendants once they differentiate.…”

Section: Discussionmentioning

confidence: 99%

Experimental evolution of multicellularity

Ratcliff

Denison²,

Borrello³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

469

619

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Multicellularity was one of the most significant innovations in the history of life, but its initial evolution remains poorly understood. Using experimental evolution, we show that key steps in this transition could have occurred quickly. We subjected the unicellular yeast Saccharomyces cerevisiae to an environment in which we expected multicellularity to be adaptive. We observed the rapid evolution of clustering genotypes that display a novel multicellular life history characterized by reproduction via multicellular propagules, a juvenile phase, and determinate growth. The multicellular clusters are uniclonal, minimizing within-cluster genetic conflicts of interest. Simple among-cell division of labor rapidly evolved. Early multicellular strains were composed of physiologically similar cells, but these subsequently evolved higher rates of programmed cell death (apoptosis), an adaptation that increases propagule production. These results show that key aspects of multicellular complexity, a subject of central importance to biology, can readily evolve from unicellular eukaryotes.T he evolution of multicellularity was transformative for life on earth (1). In addition to larger size, multicellularity increased biological complexity through the formation of new biological structures. For example, multicellular organisms have evolved sophisticated, higher-level functionality via cooperation among component cells with complementary behaviors (2, 3). However, dissolution and death of multicellular individuals occurs when cooperation breaks down, cancer being a prime example (4). There are multiple mechanisms to help ensure cooperation of component cells in most extant multicellular species (5-8), but the origin and the maintenance of multicellularity are two distinct evolutionary problems. Component cells in a nascent multicellular organism would appear to have frequent opportunities to pursue noncooperative reproductive strategies at a cost to the reproduction of the multicellular individual. How, then, does the transition to multicellularity occur?Understanding the evolution of complex multicellular individuals from unicellular ancestors has been extremely challenging, largely because the first steps in this process occurred in the deep past (>200 million years ago) (9, 10). As a result, transitional forms have been lost to extinction, and little is known about the physiology, ecology, and evolutionary processes of incipient multicellularity (11). Nonetheless, several key steps have been identified for this transition. Because multicellular organisms are composed of multiple cells, the first step in this transition was likely the evolution of genotypes that form simple cellular clusters (1, 3, 12-16). It is not known whether this occurs more readily through aggregation of genetically distinct cells, as in biofilms, or by mother-daughter cell adhesion after division. Once simple clusters have evolved, selection among multicelled clusters must predominate over selection among single cells within clusters (1,15,17,18). T...

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Section: Discussionmentioning

confidence: 99%

Experimental evolution of multicellularity

Ratcliff

Denison²,

Borrello³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

469

619

View full text Add to dashboard Cite

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“…9 Alternatively, zooxanthellae PCD may be a 'pseudo-altruistic' mechanism by which dysfunctional symbionts initiate cell suicide in order to protect the host and thereby promote survival of the zooxanthellae clone population. 40,41 Clearly, the operation of different cell death pathways in symbiosis in response to stress warrants further study and it is important that we understand the triggers of PCD and necrosis in the two components of the symbiosis during bleaching. The adaptive and evolutionary significance of the cell death process is critical to understanding of coral bleaching, a serious ecological phenomenon that is threatening the existence of coral reef ecosystems.…”

Section: Discussionmentioning

confidence: 99%

Heat stress induces different forms of cell death in sea anemones and their endosymbiotic algae depending on temperature and duration

et al. 2004

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Bleaching of reef building corals and other symbiotic cnidarians due to the loss of their dinoflagellate algal symbionts ( ¼ zooxanthellae), and/or their photosynthetic pigments, is a common sign of environmental stress. Mass bleaching events are becoming an increasingly important cause of mortality and reef degradation on a global scale, linked by many to global climate change. However, the cellular mechanisms of stress-induced bleaching remain largely unresolved. In this study, the frequency of apoptosislike and necrosis-like cell death was determined in the symbiotic sea anemone Aiptasia sp. using criteria that had previously been validated for this symbiosis as indicators of programmed cell death (PCD) and necrosis. Results indicate that PCD and necrosis occur simultaneously in both host tissues and zooxanthellae subject to environmentally relevant doses of heat stress. Frequency of PCD in the anemone endoderm increased within minutes of treatment. Peak rates of apoptosis-like cell death in the host were coincident with the timing of loss of zooxanthellae during bleaching. The proportion of apoptosis-like host cells subsequently declined while cell necrosis increased. In the zooxanthellae, both apoptosis-like and necrosis-like activity increased throughout the duration of the experiment (6 days), dependent on temperature dose. A stress-mediated PCD pathway is an important part of the thermal stress response in the sea anemone symbiosis and this study suggests that PCD may play different roles in different components of the symbiosis during bleaching.

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“…After 60 min of incubation at 37˚C cells were examined on a Zeiss Axiovert fluorescence microscope (Zeiss) equipped with a DAPI filter. Cells were photographed and analysed by visual examination to distinguish between apoptosis and necrosis (22). Cells were judged according to their morphology and the integrity of their cell membranes by propidium iodide staining.…”

Section: Reagentsmentioning

confidence: 99%

Effects of Scrophularia extracts on tumor cell proliferation, death and intravasation through lymphoendothelial cell barriers

et al. 2012

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Abstract. Different studies describe the anti-inflammatory effects of Scrophularia species, a medicinal plant widely used in folk medicine since ancient times. As knowledge regarding the anti-neoplastic properties of this species is rather limited, we investigated the influence of methanol extracts of different Scrophularia species on cell proliferation, cell death, and tumour cell intravasation through the lymph endothelial barrier. HL-60 leukaemia cells were treated with methanol extracts of different Scrophularia species leading to strong growth inhibition and high cell death rates. The expression of cell cycle regulators, oncogenes and cell death inducers was determined by Western blot analysis. Furthermore the effect of S. lucida was studied in an NF-κB reporter assay, and in a novel assay measuring 'circular chemo-repellent-induced defects' (CCID) in lymph endothelial monolayers that were induced by MCF-7 breast cancer spheroids. Methanol extracts of Scrophularia species exhibited strong anti-proliferative properties. S. floribunda extract inhibited G2/M-and later on S-phase and S. lucida inhibited S-phase and in both cases this was associated with the down-regulation of c-Myc expression. Extracts of S. floribunda and S. lucida led to necrosis and apoptosis, respectively. Furthermore, S. lucida, but not S. floribunda, effectively attenuated tumour cell intravasation through lymph endothelial cell monolayers, which correlated with the inhibition of NF-κB. S. lucida exhibited promising anti-neoplastic effects and this was most likely due to the downregulation of various cell cycle regulators, proto-oncogenes and NF-κB and the activation of caspase-3.

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The evolution of cell death programs as prerequisites of multicellularity

Cited by 75 publications

References 124 publications

Experimental evolution of multicellularity

Experimental evolution of multicellularity

Heat stress induces different forms of cell death in sea anemones and their endosymbiotic algae depending on temperature and duration

Effects of Scrophularia extracts on tumor cell proliferation, death and intravasation through lymphoendothelial cell barriers

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