Bacteriocyte cell death in the pea aphid/Buchnera symbiotic system.

Bacteriocyte cell death in the pea aphid/Buchnera symbiotic system.
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DOI:
10.1073/pnas.1720237115
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发表时间:
2018-02-20
影响因子:
11.1
通讯作者:
Calevro F
Calevro F
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Simonet P;Gaget K;Balmand S;Ribeiro Lopes M;Parisot N;Buhler K;Duport G;Vulsteke V;Febvay G;Heddi A;Charles H;Callaerts P;Calevro F

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Beneficial symbiotic associations, ubiquitously found in nature, have led to the emergence of eukaryotic cells, the bacteriocytes, specialized in harboring microbial partners. One of the most fundamental questions concerning these enigmatic cells is how organismal homeostasis controls their elimination. Here we report that aphid bacteriocytes have evolved a form of cell death distinct from the conserved cell-death mechanisms hitherto characterized. This cell-death mechanism is a nonapoptotic multistep process that starts with the hypervacuolation of the endoplasmic reticulum, followed by a cascade of cellular stress responses. Our findings provide a framework to study biological functioning of bacteriocytes and the cellular mechanisms associated with symbiosis and contribute to the understanding of eukaryotic cell-death diversity. Symbiotic associations play a pivotal role in multicellular life by facilitating acquisition of new traits and expanding the ecological capabilities of organisms. In insects that are obligatorily dependent on intracellular bacterial symbionts, novel host cells (bacteriocytes) or organs (bacteriomes) have evolved for harboring beneficial microbial partners. The processes regulating the cellular life cycle of these endosymbiont-bearing cells, such as the cell-death mechanisms controlling their fate and elimination in response to host physiology, are fundamental questions in the biology of symbiosis. Here we report the discovery of a cell-death process involved in the degeneration of bacteriocytes in the hemipteran insect Acyrthosiphon pisum. This process is activated progressively throughout aphid adulthood and exhibits morphological features distinct from known cell-death pathways. By combining electron microscopy, immunohistochemistry, and molecular analyses, we demonstrated that the initial event of bacteriocyte cell death is the cytoplasmic accumulation of nonautophagic vacuoles, followed by a sequence of cellular stress responses including the formation of autophagosomes in intervacuolar spaces, activation of reactive oxygen species, and Buchnera endosymbiont degradation by the lysosomal system. We showed that this multistep cell-death process originates from the endoplasmic reticulum, an organelle exhibiting a unique reticular network organization spread throughout the entire cytoplasm and surrounding Buchnera aphidicola endosymbionts. Our findings provide insights into the cellular and molecular processes that coordinate eukaryotic host and endosymbiont homeostasis and death in a symbiotic system and shed light on previously unknown aspects of bacteriocyte biological functioning.
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