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Anthranilate fluorescence marks a calcium-propagated necrotic wave that promotes organismal death in C. elegans

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Anthranilate fluorescence marks a calcium-propagated necrotic wave that promotes organismal death in C. elegans. / Coburn, Cassandra; Allman, Erik; Mahanti, Parag; Benedetto, Alexandre; Cabreiro, Filipe; Pincus, Zachary; Matthijssens, Filip; Araiz, Caroline; Mandel, Abraham; Vlachos, Manolis; Edwards, Sally-Anne; Fischer, Grahame; Davidson, Alexander; Pryor, Rosina E; Stevens, Ailsa; Slack, Frank J; Tavernarakis, Nektarios; Braeckman, Bart P; Schroeder, Frank C; Nehrke, Keith; Gems, David.

In: Plos Biology, Vol. 11, No. 7, e1001613, 23.07.2013.

Research output: Contribution to journalJournal articlepeer-review

Harvard

Coburn, C, Allman, E, Mahanti, P, Benedetto, A, Cabreiro, F, Pincus, Z, Matthijssens, F, Araiz, C, Mandel, A, Vlachos, M, Edwards, S-A, Fischer, G, Davidson, A, Pryor, RE, Stevens, A, Slack, FJ, Tavernarakis, N, Braeckman, BP, Schroeder, FC, Nehrke, K & Gems, D 2013, 'Anthranilate fluorescence marks a calcium-propagated necrotic wave that promotes organismal death in C. elegans', Plos Biology, vol. 11, no. 7, e1001613. https://doi.org/10.1371/journal.pbio.1001613

APA

Coburn, C., Allman, E., Mahanti, P., Benedetto, A., Cabreiro, F., Pincus, Z., Matthijssens, F., Araiz, C., Mandel, A., Vlachos, M., Edwards, S-A., Fischer, G., Davidson, A., Pryor, R. E., Stevens, A., Slack, F. J., Tavernarakis, N., Braeckman, B. P., Schroeder, F. C., ... Gems, D. (2013). Anthranilate fluorescence marks a calcium-propagated necrotic wave that promotes organismal death in C. elegans. Plos Biology, 11(7), [e1001613]. https://doi.org/10.1371/journal.pbio.1001613

Vancouver

Author

Coburn, Cassandra ; Allman, Erik ; Mahanti, Parag ; Benedetto, Alexandre ; Cabreiro, Filipe ; Pincus, Zachary ; Matthijssens, Filip ; Araiz, Caroline ; Mandel, Abraham ; Vlachos, Manolis ; Edwards, Sally-Anne ; Fischer, Grahame ; Davidson, Alexander ; Pryor, Rosina E ; Stevens, Ailsa ; Slack, Frank J ; Tavernarakis, Nektarios ; Braeckman, Bart P ; Schroeder, Frank C ; Nehrke, Keith ; Gems, David. / Anthranilate fluorescence marks a calcium-propagated necrotic wave that promotes organismal death in C. elegans. In: Plos Biology. 2013 ; Vol. 11, No. 7.

Bibtex

@article{64604ce7979a443885e6ed4aac7ac40a,
title = "Anthranilate fluorescence marks a calcium-propagated necrotic wave that promotes organismal death in C. elegans",
abstract = "For cells the passage from life to death can involve a regulated, programmed transition. In contrast to cell death, the mechanisms of systemic collapse underlying organismal death remain poorly understood. Here we present evidence of a cascade of cell death involving the calpain-cathepsin necrosis pathway that can drive organismal death in Caenorhabditis elegans. We report that organismal death is accompanied by a burst of intense blue fluorescence, generated within intestinal cells by the necrotic cell death pathway. Such death fluorescence marks an anterior to posterior wave of intestinal cell death that is accompanied by cytosolic acidosis. This wave is propagated via the innexin INX-16, likely by calcium influx. Notably, inhibition of systemic necrosis can delay stress-induced death. We also identify the source of the blue fluorescence, initially present in intestinal lysosome-related organelles (gut granules), as anthranilic acid glucosyl esters--not, as previously surmised, the damage product lipofuscin. Anthranilic acid is derived from tryptophan by action of the kynurenine pathway. These findings reveal a central mechanism of organismal death in C. elegans that is related to necrotic propagation in mammals--e.g., in excitotoxicity and ischemia-induced neurodegeneration. Endogenous anthranilate fluorescence renders visible the spatio-temporal dynamics of C. elegans organismal death.",
keywords = "Animals, Caenorhabditis elegans, Esters, Fluorescence, Oxidative Stress, ortho-Aminobenzoates, Journal Article, Research Support, N.I.H., Extramural, Research Support, Non-U.S. Gov't, Research Support, U.S. Gov't, Non-P.H.S.",
author = "Cassandra Coburn and Erik Allman and Parag Mahanti and Alexandre Benedetto and Filipe Cabreiro and Zachary Pincus and Filip Matthijssens and Caroline Araiz and Abraham Mandel and Manolis Vlachos and Sally-Anne Edwards and Grahame Fischer and Alexander Davidson and Pryor, {Rosina E} and Ailsa Stevens and Slack, {Frank J} and Nektarios Tavernarakis and Braeckman, {Bart P} and Schroeder, {Frank C} and Keith Nehrke and David Gems",
year = "2013",
month = jul,
day = "23",
doi = "10.1371/journal.pbio.1001613",
language = "English",
volume = "11",
journal = "Plos Biology",
issn = "1544-9173",
publisher = "Public Library of Science",
number = "7",

}

RIS

TY - JOUR

T1 - Anthranilate fluorescence marks a calcium-propagated necrotic wave that promotes organismal death in C. elegans

AU - Coburn, Cassandra

AU - Allman, Erik

AU - Mahanti, Parag

AU - Benedetto, Alexandre

AU - Cabreiro, Filipe

AU - Pincus, Zachary

AU - Matthijssens, Filip

AU - Araiz, Caroline

AU - Mandel, Abraham

AU - Vlachos, Manolis

AU - Edwards, Sally-Anne

AU - Fischer, Grahame

AU - Davidson, Alexander

AU - Pryor, Rosina E

AU - Stevens, Ailsa

AU - Slack, Frank J

AU - Tavernarakis, Nektarios

AU - Braeckman, Bart P

AU - Schroeder, Frank C

AU - Nehrke, Keith

AU - Gems, David

PY - 2013/7/23

Y1 - 2013/7/23

N2 - For cells the passage from life to death can involve a regulated, programmed transition. In contrast to cell death, the mechanisms of systemic collapse underlying organismal death remain poorly understood. Here we present evidence of a cascade of cell death involving the calpain-cathepsin necrosis pathway that can drive organismal death in Caenorhabditis elegans. We report that organismal death is accompanied by a burst of intense blue fluorescence, generated within intestinal cells by the necrotic cell death pathway. Such death fluorescence marks an anterior to posterior wave of intestinal cell death that is accompanied by cytosolic acidosis. This wave is propagated via the innexin INX-16, likely by calcium influx. Notably, inhibition of systemic necrosis can delay stress-induced death. We also identify the source of the blue fluorescence, initially present in intestinal lysosome-related organelles (gut granules), as anthranilic acid glucosyl esters--not, as previously surmised, the damage product lipofuscin. Anthranilic acid is derived from tryptophan by action of the kynurenine pathway. These findings reveal a central mechanism of organismal death in C. elegans that is related to necrotic propagation in mammals--e.g., in excitotoxicity and ischemia-induced neurodegeneration. Endogenous anthranilate fluorescence renders visible the spatio-temporal dynamics of C. elegans organismal death.

AB - For cells the passage from life to death can involve a regulated, programmed transition. In contrast to cell death, the mechanisms of systemic collapse underlying organismal death remain poorly understood. Here we present evidence of a cascade of cell death involving the calpain-cathepsin necrosis pathway that can drive organismal death in Caenorhabditis elegans. We report that organismal death is accompanied by a burst of intense blue fluorescence, generated within intestinal cells by the necrotic cell death pathway. Such death fluorescence marks an anterior to posterior wave of intestinal cell death that is accompanied by cytosolic acidosis. This wave is propagated via the innexin INX-16, likely by calcium influx. Notably, inhibition of systemic necrosis can delay stress-induced death. We also identify the source of the blue fluorescence, initially present in intestinal lysosome-related organelles (gut granules), as anthranilic acid glucosyl esters--not, as previously surmised, the damage product lipofuscin. Anthranilic acid is derived from tryptophan by action of the kynurenine pathway. These findings reveal a central mechanism of organismal death in C. elegans that is related to necrotic propagation in mammals--e.g., in excitotoxicity and ischemia-induced neurodegeneration. Endogenous anthranilate fluorescence renders visible the spatio-temporal dynamics of C. elegans organismal death.

KW - Animals

KW - Caenorhabditis elegans

KW - Esters

KW - Fluorescence

KW - Oxidative Stress

KW - ortho-Aminobenzoates

KW - Journal Article

KW - Research Support, N.I.H., Extramural

KW - Research Support, Non-U.S. Gov't

KW - Research Support, U.S. Gov't, Non-P.H.S.

U2 - 10.1371/journal.pbio.1001613

DO - 10.1371/journal.pbio.1001613

M3 - Journal article

C2 - 23935448

VL - 11

JO - Plos Biology

JF - Plos Biology

SN - 1544-9173

IS - 7

M1 - e1001613

ER -