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5. Activation of Autophagy by Metals in Chlamydomonas reinhardtii

Author

Pérez-Martín, Marta, Blaby-Haas, Crysten E, Pérez-Pérez, María Esther, Andrés-Garrido, Ascensión, Blaby, Ian K, Merchant, Sabeeha S, and Crespo, José L

Subjects
Microbiology, Biological Sciences, Generic health relevance, Autophagy, Cation Transport Proteins, Chlamydomonas reinhardtii, Metals, Heavy, Oxidative Stress, Plant Proteins, Transcriptome, Immunology
Abstract

Autophagy is an intracellular self-degradation pathway by which eukaryotic cells recycle their own material in response to specific stress conditions. Exposure to high concentrations of metals causes cell damage, although the effect of metal stress on autophagy has not been explored in photosynthetic organisms. In this study, we investigated the effect of metal excess on autophagy in the model unicellular green alga Chlamydomonas reinhardtii. We show in cells treated with nickel an upregulation of ATG8 that is independent of CRR1, a global regulator of copper signaling in Chlamydomonas. A similar effect on ATG8 was observed with copper and cobalt but not with cadmium or mercury ions. Transcriptome sequencing data revealed an increase in the abundance of the protein degradation machinery, including that responsible for autophagy, and a substantial overlap of that increased abundance with the hydrogen peroxide response in cells treated with nickel ions. Thus, our results indicate that metal stress triggers autophagy in Chlamydomonas and suggest that excess nickel may cause oxidative damage, which in turn activates degradative pathways, including autophagy, to clear impaired components and recover cellular homeostasis.

Published
2015

6. Insularity determines nestling sex ratio variation in Egyptian vulture populations [Dataset]

Author

Sanz-Aguilar, Ana [0000-0002-4177-9749], Crespo, José L. [0000-0003-3514-1025], Gómez-López, Guillermo, Sanz-Aguilar, Ana, Carrete, Martina, Arrondo, Eneko, Benítez, José Ramón, Ceballos, Olga, Cortés-Avizanda, Ainara, Pablo, Félix de, Donázar, José Antonio, Frías, Óscar, Gangoso, Laura, García-Alfonso, Marina, Crespo, José L., Grande, Juan Manuel, Serrano, David, Tella, José Luis, Blanco, Guillermo, Sanz-Aguilar, Ana [0000-0002-4177-9749], Crespo, José L. [0000-0003-3514-1025], Gómez-López, Guillermo, Sanz-Aguilar, Ana, Carrete, Martina, Arrondo, Eneko, Benítez, José Ramón, Ceballos, Olga, Cortés-Avizanda, Ainara, Pablo, Félix de, Donázar, José Antonio, Frías, Óscar, Gangoso, Laura, García-Alfonso, Marina, Crespo, José L., Grande, Juan Manuel, Serrano, David, Tella, José Luis, and Blanco, Guillermo

Published
2023

15. Insularity determines nestling sex ratio variation in Egyptian vulture populations

Author

Ministerio de Economía y Competitividad (España), Agencia Estatal de Investigación (España), Junta de Andalucía, Diputación General de Aragón, European Commission, Govern de les Illes Balears, Gobierno de Canarias, Cabildo de Fuerteventura, Junta de Castilla y León, Bárdenas Reales de Navarra, Generalitat Valenciana, Ministerio de Educación, Cultura y Deporte (España), Gómez-López, Guillermo, Sanz-Aguilar, Ana, Carrete, Martina, Arrondo, Eneko, Benítez, José Ramón, Ceballos, Olga, Cortés-Avizanda, Ainara, Pablo, Félix de, Donázar, José Antonio, Frías, Óscar, Gangoso, Laura, García-Alfonso, Marina, Crespo, José L., Grande, Juan Manuel, Serrano, David, Tella, José Luis, Blanco, Guillermo, Ministerio de Economía y Competitividad (España), Agencia Estatal de Investigación (España), Junta de Andalucía, Diputación General de Aragón, European Commission, Govern de les Illes Balears, Gobierno de Canarias, Cabildo de Fuerteventura, Junta de Castilla y León, Bárdenas Reales de Navarra, Generalitat Valenciana, Ministerio de Educación, Cultura y Deporte (España), Gómez-López, Guillermo, Sanz-Aguilar, Ana, Carrete, Martina, Arrondo, Eneko, Benítez, José Ramón, Ceballos, Olga, Cortés-Avizanda, Ainara, Pablo, Félix de, Donázar, José Antonio, Frías, Óscar, Gangoso, Laura, García-Alfonso, Marina, Crespo, José L., Grande, Juan Manuel, Serrano, David, Tella, José Luis, and Blanco, Guillermo

Abstract

Variation in offspring sex ratio, particularly in birds, has been frequently studied over the last century, although seldom using long-term monitoring data. In raptors, the cost of raising males and females is not equal, and several variables have been found to have significant effects on sex ratio, including food availability, parental age, and hatching order. Sex ratio differences between island populations and their mainland counterparts have been poorly documented, despite broad scientific literature on the island syndrome reporting substantial differences in population demography and ecology. Here, we assessed individual and environmental factors potentially affecting the secondary sex ratio of the long-lived Egyptian vulture Neophron percnopterus. We used data collected from Spanish mainland and island populations over a ca. 30-year period (1995-2021) to assess the effects of insularity, parental age, breeding phenology, brood size, hatching order, type of breeding unit (pairs vs. trios), and spatial and temporal variability on offspring sex ratio. No sex bias was found at the population level, but two opposite trends were observed between mainland and island populations consistent with the island syndrome. Offspring sex ratio was nonsignificantly female-biased in mainland Spain (0.47, n = 1112) but significantly male-biased in the Canary Islands (0.55, n = 499), where a male-biased mortality among immatures could be compensating for offspring biases and maintaining a paired adult sex ratio. Temporal and spatial variation in food availability might also have some influence on sex ratio, although the difficulties in quantifying them preclude us from determining the magnitude of such influence. This study shows that insularity influences the offspring sex ratio of the Egyptian vulture through several processes that can affect island and mainland populations differentially. Our research contributes to improving our understanding of sex allocation theory by invest

Published
2023

16. Monitoring Autophagic Flux in the Model Single-Celled Microalga Chlamydomonas reinhardtii

Author

Ministerio de Ciencia, Innovación y Universidades (España), Agencia Estatal de Investigación (España), Junta de Andalucía, Crespo, José L., Pérez-Pérez, María Esther, Ministerio de Ciencia, Innovación y Universidades (España), Agencia Estatal de Investigación (España), Junta de Andalucía, Crespo, José L., and Pérez-Pérez, María Esther

Abstract

Autophagy is a catabolic process by which eukaryotic cells degrade and recycle unnecessary or damaged intracellular components to maintain cellular homeostasis and to cope with stress. The development of specific tools to monitor autophagy in microalgae and plants has been fundamental to investigate this catabolic pathway in photosynthetic organisms. The protein ATG8 is a widely used molecular marker of autophagy in all eukaryotes, including the model microalga Chlamydomonas reinhardtii. The drug concanamycin A, a specific inhibitor of vacuolar ATPase, has also been extensively used to block autophagic flux in the green lineage. In Chlamydomonas, inhibition of autophagic flux by concanamycin A has been shown to prevent the degradation of ribosomal proteins and the formation of lipid bodies under nitrogen or phosphorous starvation. Here, we detail how the abundance and lipidation state of ATG8 can be used to monitor autophagic flux in Chlamydomonas by western blot analysis.

Published
2023

17. Adaptation, Performance and Vapnik-Chervonenkis Dimension of Straight Line Programs

Author

Montaña, José L., Alonso, César L., Borges, Cruz E., Crespo, José L., Hutchison, David, Series editor, Kanade, Takeo, Series editor, Kittler, Josef, Series editor, Kleinberg, Jon M., Series editor, Mattern, Friedemann, Series editor, Mitchell, John C., Series editor, Naor, Moni, Series editor, Nierstrasz, Oscar, Series editor, Pandu Rangan, C., Series editor, Steffen, Bernhard, Series editor, Sudan, Madhu, Series editor, Terzopoulos, Demetri, Series editor, Tygar, Doug, Series editor, Vardi, Moshe Y., Series editor, Weikum, Gerhard, Series editor, Vanneschi, Leonardo, editor, Gustafson, Steven, editor, Moraglio, Alberto, editor, De Falco, Ivanoe, editor, and Ebner, Marc, editor

Published
2009
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19. Deciphering the role of autophagy in the extremophilic microalga Chlamydomonas urium

Author

Odriozola-Gil, Yosu, Pérez-Pérez, María Esther, Mallén-Ponce, Manuel J., Rubio, Alejandro, Martínez-Force, Enrique, Salas, Joaquín J., Pérez-Pulido, Antonio J., Crespo, José L., and Junta de Andalucía

Abstract

Extremophilic microalgae have the ability to grow and adapt their metabolism to extreme conditions including acidic pH, high or very low temperature, or the presence of high concentrations of heavy metals. In addition to their ecological importance as primary producers in extreme environments, these organisms also have biotechnological potential since they produce several beneficial compounds as metabolism side-products including lipids or carbohydrates. Autophagy is a degradative process by which eukaryotic cells eliminate toxic or superfluous cellular components in order to cope with stress or unfavorable conditions and maintain cellular homeostasis. We have demonstrated that autophagy is a pro-survival mechanism that is upregulated by a wide range of stress conditions such as nutrient starvation or metal toxicity in the model microalga Chlamydomonas reinhardtii. However, autophagy has never been investigated in extremophiles and it is currently unknown whether this catabolic process play a role in the adaptation of these organisms to adverse environments. To address this question, we have isolated a new microalga, Chlamydomonas urium, from the Tinto River (Nerva, Spain), a well-characterized extremely acidic river with a high content of heavy metals. Genome sequencing and annotation revealed that core ATG genes are conserved in C. urium, indicating that autophagy must be conserved in extremophilic organisms. Our studies by western blot analysis, ultrastructural microscopy and metabolomics showed that autophagy is a highly dynamic process in C. urium. Interestingly, the inhibition of autophagic flux results in a large increase of triacylglycerols and starch, the two main carbon storage molecules. Thus, our results pinpoint autophagy as a central process regulating carbon storage in the new extremophilic microalga C. urium., This work was supported in part by Junta de Andalucía (Grant P20_00057)

Published
2022

20. Tudor staphylococcal nuclease is a docking platform for stress granule components and is essential for SnRK1 activation in Arabidopsis

Author

Ministerio de Economía y Competitividad (España), Gutiérrez-Beltrán, Emilio [0000-0001-7978-3164], Dalman, Kerstin [0000-0002-9919-9149], Moschou, Panagiotis N. [0000-0001-7212-0595], Uversky, Vladimir [0000-0002-4037-5857], Crespo, José L. [0000-0003-3514-1025], Bozhkov, Peter V. [/0000-0002-8819-3884], Gutiérrez-Beltrán, Emilio, Elander, Pernilla H., Dalman, Kerstin, Dayhoff II, Guy W., Moschou, Panagiotis N., Crespo, José L., Bozhkov, Peter V., Uversky, Vladimir, Ministerio de Economía y Competitividad (España), Gutiérrez-Beltrán, Emilio [0000-0001-7978-3164], Dalman, Kerstin [0000-0002-9919-9149], Moschou, Panagiotis N. [0000-0001-7212-0595], Uversky, Vladimir [0000-0002-4037-5857], Crespo, José L. [0000-0003-3514-1025], Bozhkov, Peter V. [/0000-0002-8819-3884], Gutiérrez-Beltrán, Emilio, Elander, Pernilla H., Dalman, Kerstin, Dayhoff II, Guy W., Moschou, Panagiotis N., Crespo, José L., Bozhkov, Peter V., and Uversky, Vladimir

Abstract

Tudor staphylococcal nuclease (TSN; also known as Tudor-SN, p100, or SND1) is a multifunctional, evolutionarily conserved regulator of gene expression, exhibiting cytoprotective activity in animals and plants and oncogenic activity in mammals. During stress, TSN stably associates with stress granules (SGs), in a poorly understood process. Here, we show that in the model plant Arabidopsis thaliana, TSN is an intrinsically disordered protein (IDP) acting as a scaffold for a large pool of other IDPs, enriched for conserved stress granule components as well as novel or plantspecific SG-localized proteins. While approximately 30% of TSN interactors are recruited to stress granules de novo upon stress perception, 70% form a protein–protein interaction network present before the onset of stress. Finally, we demonstrate that TSN and stress granule formation promote heat-induced activation of the evolutionarily conserved energy-sensing SNF1-related protein kinase 1 (SnRK1), the plant orthologue of mammalian AMP-activated protein kinase (AMPK). Our results establish TSN as a docking platform for stress granule proteins, with an important role in stress signalling

Published
2021

30. Compartmentalization, a key mechanism controlling the multi-tasking role of SnRK1 complex

Author

Universidad de Sevilla. Departamento de Bioquímica Vegetal y Biología Molecular, Ministerio de Ciencia e Innovación (MICIN). España, Agencia Estatal de Investigación. España, Ministerio de Economía y Competitividad (MINECO). España, Gutiérrez Beltrán, Emilio, Crespo, José L., Universidad de Sevilla. Departamento de Bioquímica Vegetal y Biología Molecular, Ministerio de Ciencia e Innovación (MICIN). España, Agencia Estatal de Investigación. España, Ministerio de Economía y Competitividad (MINECO). España, Gutiérrez Beltrán, Emilio, and Crespo, José L.

Published
2022

31. Deciphering the role of autophagy in the extremophilic microalga Chlamydomonas urium

Author

Junta de Andalucía, Odriozola-Gil, Yosu, Pérez-Pérez, María Esther, Mallén-Ponce, Manuel J., Rubio, Alejandro, Martínez-Force, Enrique, Salas, Joaquín J., Pérez-Pulido, Antonio J., Crespo, José L., Junta de Andalucía, Odriozola-Gil, Yosu, Pérez-Pérez, María Esther, Mallén-Ponce, Manuel J., Rubio, Alejandro, Martínez-Force, Enrique, Salas, Joaquín J., Pérez-Pulido, Antonio J., and Crespo, José L.

Abstract

Extremophilic microalgae have the ability to grow and adapt their metabolism to extreme conditions including acidic pH, high or very low temperature, or the presence of high concentrations of heavy metals. In addition to their ecological importance as primary producers in extreme environments, these organisms also have biotechnological potential since they produce several beneficial compounds as metabolism side-products including lipids or carbohydrates. Autophagy is a degradative process by which eukaryotic cells eliminate toxic or superfluous cellular components in order to cope with stress or unfavorable conditions and maintain cellular homeostasis. We have demonstrated that autophagy is a pro-survival mechanism that is upregulated by a wide range of stress conditions such as nutrient starvation or metal toxicity in the model microalga Chlamydomonas reinhardtii. However, autophagy has never been investigated in extremophiles and it is currently unknown whether this catabolic process play a role in the adaptation of these organisms to adverse environments. To address this question, we have isolated a new microalga, Chlamydomonas urium, from the Tinto River (Nerva, Spain), a well-characterized extremely acidic river with a high content of heavy metals. Genome sequencing and annotation revealed that core ATG genes are conserved in C. urium, indicating that autophagy must be conserved in extremophilic organisms. Our studies by western blot analysis, ultrastructural microscopy and metabolomics showed that autophagy is a highly dynamic process in C. urium. Interestingly, the inhibition of autophagic flux results in a large increase of triacylglycerols and starch, the two main carbon storage molecules. Thus, our results pinpoint autophagy as a central process regulating carbon storage in the new extremophilic microalga C. urium.

Published
2022

32. Photosynthetic assimilation of CO2 regulates TOR activity

Author

Ministerio de Ciencia y Tecnología (España), Mallén-Ponce, Manuel J., Pérez-Pérez, María Esther, Crespo, José L., Ministerio de Ciencia y Tecnología (España), Mallén-Ponce, Manuel J., Pérez-Pérez, María Esther, and Crespo, José L.

Abstract

The target of rapamycin (TOR) kinase is a master regulator that integrates nutrient signals to promote cell growth in all eukaryotes. It is well established that amino acids and glucose are major regulators of TOR signaling in yeast and metazoan, but whether and how TOR responds to carbon availability in photosynthetic organisms is less understood. In this study, we showed that photosynthetic assimilation of CO2 by the Calvin–Benson–Bassham (CBB) cycle regulates TOR activity in the model single-celled microalga Chlamydomonas reinhardtii. Stimulation of CO2 fixation boosted TOR activity, whereas inhibition of the CBB cycle and photosynthesis down-regulated TOR. We uncovered a tight link between TOR activity and the endogenous level of a set of amino acids including Ala, Glu, Gln, Leu, and Val through the modulation of CO2 fixation and the use of amino acid synthesis inhibitors. Moreover, the finding that the Chlamydomonas starch-deficient mutant sta6 displayed disproportionate TOR activity and high levels of most amino acids, particularly Gln, further connected carbon assimilation and amino acids to TOR signaling. Thus, our results showed that CO2 fixation regulates TOR signaling, likely through the synthesis of key amino acids.

Published
2022

34. Compartmentalization, a key mechanism controlling the multi-tasking role of SnRK1 complex

Author

Gutiérrez Beltrán, Emilio, Crespo, José L., Universidad de Sevilla. Departamento de Bioquímica Vegetal y Biología Molecular, Ministerio de Ciencia e Innovación (MICIN). España, Agencia Estatal de Investigación. España, and Ministerio de Economía y Competitividad (MINECO). España

Subjects
stress granules, SnRK1/TOR signaling, Autophagy, SnRK1 compartmentalization, SnRK1-interacting proteins, plant cell
Abstract

SNF1-related protein kinase 1 (SnRK1), the plant ortholog of mammalian AMP-activated protein kinase/fungal (yeast) Sucrose Non-Fermenting 1 (AMPK/SNF1), plays a central role in metabolic responses to reduced energy levels in response to nutritional and environmental stresses. SnRK1 functions as a heterotrimeric complex composed of a catalytic α- and regulatory β- and βγ-subunits. SnRK1 is a multitasking protein involved in regulating various cellular functions, including growth, autophagy, stress response, stomatal development, pollen maturation, hormone signaling, and gene expression. However, little is known about the mechanism whereby SnRK1 ensures differential execution of downstream functions. Compartmentalization has been recently proposed as a new key mechanism for regulating SnRK1 signaling in response to stimuli. In this review, we discuss the multitasking role of SnRK1 signaling associated with different subcellular compartments. Ministerio de Ciencia e Innovación y Agencia Estatal de Investigación, de España (MCIN/AEI) PID2020-119737GA-I00 Ministerio de Economía y Competitividad de España - PGC2018-099048-B-100

Published
2022

38. Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition)

Author

Klionsky, Daniel J., Alonso, Alicia, Hervás, Javier H., Arévalo, María Ángeles, García-Sanz, Patricia, Belló Pérez, Melissa, García del Portillo, Francisco, Boya, Patricia, Pinar, Mario, Testillano, P. S., Casas, Josefina, Colell Riera, Anna, Fernández-Checa, José C., Moles, Anna, Coll, Núria S., Crespo, José L., Ruano, Diego, Lastres-Becker, Isabel, Vincent, Olivier, Martín-Sanz, Paloma, Valverde, Ángela M., Varela-Nieto, Isabel, Gargini, Ricardo, Izquierdo, José M., López-Guerrero, José Antonio, Wandosell, Francisco G., Romero, Luis C., Sanz, Pascual, Vilar, Marçal, Pimentel-Muiños, Felipe X., Sánchez-Alcázar, José Antonio, and National Institute of General Medical Sciences (US)

Abstract

Klionsky, Daniel J. et al., In 2008, we published the first set of guidelines for standardizing research in autophagy. Since then, this topic has received increasing attention, and many scientists have entered the field. Our knowledge base and relevant new technologies have also been expanding. Thus, it is important to formulate on a regular basis updated guidelines for monitoring autophagy in different organisms. Despite numerous reviews, there continues to be confusion regarding acceptable methods to evaluate autophagy, especially in multicellular eukaryotes. Here, we present a set of guidelines for investigators to select and interpret methods to examine autophagy and related processes, and for reviewers to provide realistic and reasonable critiques of reports that are focused on these processes. These guidelines are not meant to be a dogmatic set of rules, because the appropriateness of any assay largely depends on the question being asked and the system being used. Moreover, no individual assay is perfect for every situation, calling for the use of multiple techniques to properly monitor autophagy in each experimental setting. Finally, several core components of the autophagy machinery have been implicated in distinct autophagic processes (canonical and noncanonical autophagy), implying that genetic approaches to block autophagy should rely on targeting two or more autophagy-related genes that ideally participate in distinct steps of the pathway. Along similar lines, because multiple proteins involved in autophagy also regulate other cellular pathways including apoptosis, not all of them can be used as a specific marker for bona fide autophagic responses. Here, we critically discuss current methods of assessing autophagy and the information they can, or cannot, provide. Our ultimate goal is to encourage intellectual and technical innovation in the field., This work was supported by the National Institute of General Medical Sciences [GM131919].

Published
2021

39. Biotechnology and Plant Breeding

Author

Barro Losada, Francisco, Sánchez-Pérez, Raquel, Crespo, José L., Fernández-Muñoz, Rafael, Igartua Arregui, Ernesto, Lois, L. María, Malvar Pintos, Rosa Ana, Orzáez Calatayud, Diego, and Prieto, Pilar

Subjects
Phenotyping, food and beverages, Climate change, Population growth, Biodiversity, Genome-editing, Omic technologies, Synthetic biology
Abstract

The challenge “Biotechnology and Plant Breeding” aims to understand how ‘omics information translates into phenotypes in photosynthetic organisms, to turn plant breeding into a predictive science. In scenarios of population growth and climate change, this knowledge will predict the agronomic value of natural variation and spontaneous or induced genetic changes, thus enabling the development of new crops with enhanced features that contribute to increase food security and the sustainability of primary production.

Published
2021

40. Tudor staphylococcal nuclease is a docking platform for stress granule components and is essential for SnRK1 activation in Arabidopsis

Author

Universidad de Sevilla. Departamento de Bioquímica Vegetal y Biología Molecular, Gutiérrez Beltrán, Emilio, Elander, Pernilla H., Dalman, Kerstin, Dayhoff, Guy W. II, Moschou, Panagiotis N., Uversky, Vladimir N., Crespo, José L., Bozhkov, Peter V., Universidad de Sevilla. Departamento de Bioquímica Vegetal y Biología Molecular, Gutiérrez Beltrán, Emilio, Elander, Pernilla H., Dalman, Kerstin, Dayhoff, Guy W. II, Moschou, Panagiotis N., Uversky, Vladimir N., Crespo, José L., and Bozhkov, Peter V.

Abstract

Tudor staphylococcal nuclease (TSN; also known as Tudor-SN, p100, or SND1) is a multifunctional, evolutionarily conserved regulator of gene expression, exhibiting cytoprotective activity in animals and plants and oncogenic activity in mammals. During stress, TSN stably associates with stress granules (SGs), in a poorly understood process. Here, we show that in the model plant Arabidopsis thaliana, TSN is an intrinsically disordered protein (IDP) acting as a scaffold for a large pool of other IDPs, enriched for conserved stress granule components as well as novel or plant-specific SG-localized proteins. While approximately 30% of TSN interactors are recruited to stress granules de novo upon stress perception, 70% form a protein–protein interaction network present before the onset of stress. Finally, we demonstrate that TSN and stress granule formation promote heat-induced activation of the evolutionarily conserved energy-sensing SNF1-related protein kinase 1 (SnRK1), the plant orthologue of mammalian AMP-activated protein kinase (AMPK). Our results establish TSN as a docking platform for stress granule proteins, with an important role in stress signalling.

Published
2021

41. Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition)

Author

National Institute of General Medical Sciences (US), Klionsky, Daniel J., Alonso, Alicia, Hervás, Javier H., Arévalo, María Ángeles, García-Sanz, Patricia, Belló Pérez, Melissa, García del Portillo, Francisco, Boya, Patricia, Pinar, Mario, Testillano, P. S., Casas, Josefina, Colell Riera, Anna, Fernández-Checa, José C., Moles, Anna, Coll, Núria S., Crespo, José L., Ruano, Diego, Lastres-Becker, Isabel, Vincent, Olivier, Martín-Sanz, Paloma, Valverde, Ángela M., Varela-Nieto, Isabel, Gargini, Ricardo, Izquierdo, José M., López-Guerrero, José Antonio, Wandosell, Francisco G., Romero, Luis C., Sanz, Pascual, Vilar, Marçal, Pimentel-Muiños, Felipe X., Sánchez-Alcázar, José Antonio, National Institute of General Medical Sciences (US), Klionsky, Daniel J., Alonso, Alicia, Hervás, Javier H., Arévalo, María Ángeles, García-Sanz, Patricia, Belló Pérez, Melissa, García del Portillo, Francisco, Boya, Patricia, Pinar, Mario, Testillano, P. S., Casas, Josefina, Colell Riera, Anna, Fernández-Checa, José C., Moles, Anna, Coll, Núria S., Crespo, José L., Ruano, Diego, Lastres-Becker, Isabel, Vincent, Olivier, Martín-Sanz, Paloma, Valverde, Ángela M., Varela-Nieto, Isabel, Gargini, Ricardo, Izquierdo, José M., López-Guerrero, José Antonio, Wandosell, Francisco G., Romero, Luis C., Sanz, Pascual, Vilar, Marçal, Pimentel-Muiños, Felipe X., and Sánchez-Alcázar, José Antonio

Abstract

In 2008, we published the first set of guidelines for standardizing research in autophagy. Since then, this topic has received increasing attention, and many scientists have entered the field. Our knowledge base and relevant new technologies have also been expanding. Thus, it is important to formulate on a regular basis updated guidelines for monitoring autophagy in different organisms. Despite numerous reviews, there continues to be confusion regarding acceptable methods to evaluate autophagy, especially in multicellular eukaryotes. Here, we present a set of guidelines for investigators to select and interpret methods to examine autophagy and related processes, and for reviewers to provide realistic and reasonable critiques of reports that are focused on these processes. These guidelines are not meant to be a dogmatic set of rules, because the appropriateness of any assay largely depends on the question being asked and the system being used. Moreover, no individual assay is perfect for every situation, calling for the use of multiple techniques to properly monitor autophagy in each experimental setting. Finally, several core components of the autophagy machinery have been implicated in distinct autophagic processes (canonical and noncanonical autophagy), implying that genetic approaches to block autophagy should rely on targeting two or more autophagy-related genes that ideally participate in distinct steps of the pathway. Along similar lines, because multiple proteins involved in autophagy also regulate other cellular pathways including apoptosis, not all of them can be used as a specific marker for bona fide autophagic responses. Here, we critically discuss current methods of assessing autophagy and the information they can, or cannot, provide. Our ultimate goal is to encourage intellectual and technical innovation in the field.

Published
2021

42. Inositol polyphosphates and target of rapamycin kinase signalling govern photosystem II protein phosphorylation and photosynthetic function under light stress in Chlamydomonas

Author

Ministerio de Economía y Competitividad (España), European Commission, Couso, Inmaculada, Smythers, Amanda L., Ford, Megan M., Umen, James G., Crespo, José L., Hicks, Leslie M., Ministerio de Economía y Competitividad (España), European Commission, Couso, Inmaculada, Smythers, Amanda L., Ford, Megan M., Umen, James G., Crespo, José L., and Hicks, Leslie M.

Abstract

Stress and nutrient availability influence cell proliferation through complex intracellular signalling networks. In a previous study it was found that pyro-inositol polyphosphates (InsP7 and InsP8) produced by VIP1 kinase, and target of rapamycin (TOR) kinase signalling interacted synergistically to control cell growth and lipid metabolism in the green alga Chlamydomonas reinhardtii. However, the relationship between InsPs and TOR was not completely elucidated. We used an in vivo assay for TOR activity together with global proteomic and phosphoproteomic analyses to assess differences between wild-type and vip1-1 in the presence and absence of rapamycin. We found that TOR signalling is more severely affected by the inhibitor rapamycin in a vip1-1 mutant compared with wild-type, indicating that InsP7 and InsP8 produced by VIP1 act independently but also coordinately with TOR. Additionally, among hundreds of differentially phosphorylated peptides detected, an enrichment for photosynthesis-related proteins was observed, particularly photosystem II proteins. The significance of these results was underscored by the finding that vip1-1 strains show multiple defects in photosynthetic physiology that were exacerbated under high light conditions. These results suggest a novel role for inositol pyrophosphates and TOR signalling in coordinating photosystem phosphorylation patterns in Chlamydomonas cells in response to light stress and possibly other stresses.

Published
2021

49. Contributors

Author

Abrams, John M., primary, Adelman, John P., additional, Alcorn, Joseph L., additional, Alessi, Dario R., additional, Alexov, Emil, additional, Alford, Simon, additional, Alitalo, Kari, additional, Allison, James P., additional, Almo, Steven C., additional, Alory, Christelle, additional, Al-Shamkhani, Aymen, additional, Amundson, Sally A., additional, Anderson, Carl W., additional, Andersen, Jannik N., additional, Angel, Peter, additional, Appella, Ettore, additional, Arendshorst, William J., additional, Arkinstall, Steve, additional, Audhya, Anjon, additional, Avruch, Joseph, additional, Bader, Gary D., additional, Bagala, Cinzia, additional, Balch, William E., additional, Balsinde, Jesus, additional, Banerjee, Utpal, additional, Barford, David, additional, Bar-Sagi, Dafna, additional, Bartlett, Perry F., additional, Bastiaens, Philippe I.H., additional, Battelli, Chiara, additional, Baudhuin, Linnea M., additional, Beavil, Andrew J., additional, Beavil, Rebecca L., additional, Beavo, Joseph A., additional, Bello-Reuss, Elsa, additional, Bellum, Stephen, additional, Belmonte, Juan Carlos Izpisúa, additional, Bennett, Craig B., additional, Benovic, Jeffrey L., additional, Berridge, Michael J., additional, Beuning, Penny J., additional, Bhandari, Rashna, additional, Bhattacharya, Ananya, additional, Biel, Martin, additional, Bielinski, Vincent A., additional, Bilak, Hana, additional, Birnbaumer, Lutz, additional, Birrell, Geoff, additional, Bishop, Gail A., additional, Blackmer, Trillium, additional, Blackshear, Perry J., additional, Blattner, Christine, additional, Blaustein, Mordecai P., additional, Bokoch, Gary M., additional, Bonewald, Lynda F., additional, Bonomi, Marco, additional, Booden, Michelle A., additional, Boone, Charles, additional, Bootman, Martin D., additional, Bos, Johannes L., additional, Bradbury, Jane M., additional, Bradshaw, Ralph A., additional, Bresnick, Anne R., additional, Brevnova, Lena, additional, Brinkworth, Ross I., additional, Brown, Michael S., additional, Brown, Steven A., additional, Brunet, Anne, additional, Bucki, Robert, additional, Burgoyne, Robert D., additional, Buss, Janice E., additional, Butow, Ronald A., additional, Capdevila, Javier, additional, Carafoli, Ernesto, additional, Carlson, Cathrine R., additional, Carpenter, Graham, additional, Carrillo, Juan J., additional, Casey, Patrick J., additional, Catterall, William A., additional, Cerione, Richard A., additional, Cesareni, Gianni, additional, Chan, Andrew C., additional, Chang, Geoffrey, additional, Chao, Moses V., additional, Charbonneau, Harry, additional, Chen, Philip, additional, Cheng, Alan, additional, Chiu, Chris, additional, Chow, Dar-chone, additional, Chrisman, Ted D., additional, Christensen, Anne Elisabeth, additional, Chung, Jee Y., additional, Churchill, Grant C., additional, Ciechanover, Aaron, additional, Cingolani, Gino, additional, Claeysen, Sylvie, additional, Closset, Jean, additional, Cockcroft, Shamshad, additional, Cohen, Patricia T.W., additional, Cohen, Philip, additional, Colbran, Roger J., additional, Comstock, Clay E.S., additional, Conti, Marco, additional, Corbin, Jackie D., additional, Corda, Daniela, additional, Costagliola, Sabine, additional, Cote, Rick H., additional, Coughlin, Shaun R., additional, Cowart, L. Ashley, additional, Cox, Adrienne D., additional, Cragg, Mark S., additional, Crespo, José L., additional, Crosio, Claudia, additional, Daly, Christopher, additional, Damak, Sami, additional, Dasso, Mary, additional, David, Michael, additional, Davis, Anthony J., additional, Davis, Roger J., additional, Day, Richard N., additional, Degerman, Eva, additional, DeLano, Warren L., additional, Dell'Acqua, Mark L., additional, Délot, Emmanuèle, additional, Demple, Bruce, additional, Dennis, Edward A., additional, Denu, John M., additional, DePaoli-Roach, Anna A., additional, Der, Channing J., additional, de Rooij, Johan, additional, de Sauvage, Frederic, additional, Devreotes, Peter N., additional, Dewaste, Valérie, additional, Dickson, Robert B., additional, Diebold, Becky A., additional, Fiori, Pier Paolo Di, additional, Girolamo, Maria Di, additional, Diplexcito, Julie, additional, Dixon, Jack E., additional, Doms, Robert W., additional, Donoghue, Daniel J., additional, Doolittle, Russell F., additional, Døskeland, Stein Ove, additional, Dostmann, Wolfgang R.G., additional, Dreyer, Matthias K., additional, Du, Guo Guang, additional, Du, Keyong, additional, Duchen, Michael R., additional, Dunphy, William G., additional, Durgan, Joanne, additional, Dustin, Michael L., additional, Edwards, Peter A., additional, Egen, Jackson G., additional, Eiden, Lee E., additional, Elion, Elaine A., additional, Emr, Scott, additional, Engelhardt, Othmar G., additional, Erneux, Christophe, additional, Espenshade, Peter J., additional, Esplin, Edward D., additional, Evers, B. Mark, additional, Eyles, Joanne L., additional, Fame, Sheelagh, additional, Farquhar, Marilyn, additional, Feil, Robert, additional, Feng, Gui-Jie, additional, Fields, Stanley, additional, Fiordalisi, James J., additional, Firtel, Richard A., additional, Fitzgerald, Garret A., additional, Flint, Andrew, additional, Foiani, Marco, additional, Forman, Barry Marc, additional, Fornace, Albert J., additional, Francis, Sharron H., additional, Fritz, Günter, additional, Fruman, David A., additional, Galione, Antony, additional, Gandhi, Chris S., additional, Garbers, David L., additional, Garcia, K. Christopher, additional, Geiger, Benjamin, additional, Gerace, Larry, additional, Gerstner, Andrea, additional, Giaccia, Amato J., additional, Giannattasio, Michele, additional, Giguère, Vincent, additional, Glass, Christopher K., additional, Glennie, Martin J., additional, Glick, Jennifer L., additional, Goldstein, Joseph L., additional, Gopal, Venkatesh, additional, Gorospe, Myriam, additional, Govaerts, Cedric, additional, Graves, Paul R., additional, Gray, Patrick W., additional, Graziani, Irene, additional, Green, Douglas R., additional, Greenberg, Michael E., additional, Greenwald, Iva, additional, Gu, Haihua, additional, Gueven, Nuri, additional, Gutkind, J. Silvio, additional, Haeggström, Jesper Z., additional, Hall, Alan, additional, Hall, Michael N., additional, Haller, Otto, additional, Hamm, Heidi E., additional, Hannun, Yusef A., additional, Hansen, Carl A., additional, Harden, T. Kendall, additional, Hardie, D. Grahame, additional, Hasegawa, Kiminori, additional, Hawkins, Phillip T., additional, Haystead, Timothy A.J., additional, He, Xiao-lin, additional, Heizmann, Claus W., additional, Heldin, Carl-Henrik, additional, Hermiston, Michelle L., additional, Herrlich, Peter, additional, Hewat, Elizabeth A., additional, Hille, Bertil, additional, Hilton, Douglas J., additional, Hinchliffe, K.A., additional, Ho, Steffan N., additional, Ho, Su-Chin, additional, Hochstrasser, Mark, additional, Hofmann, Franz, additional, Hogue, Christopher W., additional, Hol, Wim G.J., additional, Holash, Jocelyn, additional, Holmgren, Robert A., additional, Honig, Barry, additional, Hostager, Bruce S., additional, Hubbard, Stevan R., additional, Huber, Michael, additional, Hunter, Tony, additional, Huttenlocher, Anna, additional, Hymowitz, Sarah G., additional, Ihle, James N., additional, Imler, Jean-Luc, additional, Irvine, R.F., additional, Isacoff, Ehud Y., additional, Iturrioz, Xavier, additional, Iversen, Lars F., additional, Iyengar, Ravi, additional, Jackson, Stephen P., additional, Jan, Lily Yeh, additional, Janiak-Spens, Fabiola, additional, Janmey, Paul A., additional, Jansen, Peter Gildsig, additional, Jarriault, Sophie, additional, Javitch, Jonathan A., additional, Jensen, Elwood V., additional, Jepsen, Kristen, additional, Jones, E. Yvonne, additional, Jones, Katherine A., additional, Jordan, J. Dedrick, additional, Joseph, Jomon, additional, Justement, Louis B., additional, Kafri, Yariv, additional, Kahn, Richard A., additional, Kang, Shin W., additional, Karlin, Arthur, additional, Kast-Woelbern, Heidi R., additional, Kaufman, Randal J., additional, Kazlauskas, Andrius, additional, Keen, James H., additional, Kemler, Rolf, additional, Kemp, Bruce E., additional, Kennedy, Mary B., additional, Kennedy, Matthew A., additional, Kikkawa, Ushio, additional, Kim, Albert H., additional, Kim, Soo-A, additional, Kim, Sung-Hou, additional, Kim, Youngjoo, additional, King-Jones, Kirst, additional, Kintner, Chris, additional, Kivimäe, Saul, additional, Klee, Claude B., additional, Klein, Rüdiger, additional, Kleppisch, Thomas, additional, Kliewer, Steven A., additional, Klinghoffer, Richard A., additional, Knoblich, Juergen A., additional, Kobe, Bostjan, additional, Kochs, George, additional, Kong-Beltran, Monica, additional, König, Rolf, additional, Koong, Albert C., additional, Korc, Murray, additional, Kornitzer, Daniel, additional, Kossiakoff, Anthony A., additional, Kotera, Jun, additional, Kovalenko, M.V., additional, Kozasa, Tohru, additional, Kozlov, Sergei, additional, Kozminski, Keith G., additional, Krugmann, Sonja, additional, Kuriyan, John, additional, Kurokawa, Riki, additional, Kwong, Peter D., additional, Lai, Wi S., additional, Lamar, Elise, additional, Lambert, Millard H., additional, Lambright, David G., additional, Lancet, Doron, additional, Landry, Reiko, additional, Langdon, Wallace Y., additional, Langeberg, Lorene K., additional, Lasko, Paul, additional, Latham, Vaughn, additional, Lavin, Martin F., additional, Lease, Kevin A., additional, Leffler, Hakon, additional, Lemmon, Mark A., additional, Leonard, Ann E., additional, Levitzki, Alexander, additional, Liao, Hong-Jun, additional, Liaw, Lucy, additional, Liberi, Giordano, additional, Lickert, Heiko, additional, Liddington, Robert C., additional, Lincoln, Thomas M., additional, Linder, Jürgen U., additional, Linder, Maurine E., additional, Liu, Hui, additional, Liu, Zhengchang, additional, Lohela, Marja K., additional, Louie, Sarah H., additional, Luttrell, Deirdre K., additional, Luttrell, Louis M., additional, Lyons, Karen M., additional, Macaulay, S. Lance, additional, Maceyka, Michael, additional, Maciag, Thomas, additional, Macian, Fernando, additional, MacKintosh, Carol, additional, MacLennan, David H., additional, Mahmood, Nadir A., additional, Malbon, Craig C., additional, Malik, Sohail, additional, Man, Orna, additional, Manahan, Carol L., additional, Mandinova, Anna, additional, Manganiello, Vincent C., additional, Manley, James L., additional, Mann, Matthias, additional, Manning, Gerald, additional, Manser, Ed, additional, Margeta-Mitrovic, Marta, additional, Margolskee, Robert F., additional, Marinissen, Julia, additional, Mariuzza, Roy A., additional, Marmor, Mina D., additional, Martin, G. Steven, additional, Martin, Karen H., additional, Martinez, Sergio E., additional, Mathews, Michael B., additional, Mayer, Bruce J., additional, Mayer, Mark L., additional, Mazzoni, Maria R., additional, McCormick, Frank, additional, McGowan, Clare H., additional, McKay, Melissa M., additional, McKeehan, Wallace L., additional, McLean, Alison J., additional, Means, Anthony R., additional, Meili, Ruedi, additional, Meng, Jingwei, additional, Merchant, Mark, additional, Mercurio, Frank, additional, Milligan, Graeme, additional, Ming, Guo-Li, additional, Minor, Daniel L., additional, Moghal, Nadeem, additional, Møller, Neils Peter H., additional, Mongillo, Marco, additional, Montminy, Marc, additional, Moon, Randall T., additional, Morimoto, Richard I., additional, Moss, Stephen E., additional, Mott, Helen R., additional, Mouta, Carla, additional, Muda, Marco, additional, Mumby, Marc C., additional, Murphy, Gretchen A., additional, Muzi-Falconi, Marco, additional, Nagaraj, Raghavendra, additional, Nahorski, Stefan R., additional, Nairn, Angus C., additional, Nash, Piers, additional, Neel, Benjamin G., additional, Newton, Alexandra C., additional, Nishizuka, Yasutomi, additional, Noel, Joseph P., additional, Nollen, Ellen A.A., additional, Nooren, Irene M.A., additional, O'Connor, Rodney, additional, Offermanns, Stefan, additional, Olender, Tsviya, additional, Ong, Shao-En, additional, Owen, Darerca, additional, Pagliari, Lisa J., additional, Pao, Lily, additional, Papaconstantinou, John, additional, Pardo, Leonardo, additional, Park, Hay-Oak, additional, Park, Young Chul, additional, Parker, Peter J., additional, Parsons, J. Thomas, additional, Passner, J.M., additional, Pawson, Tony, additional, Pelliccioli, Achille, additional, Perez-Polo, J. Regino, additional, Perrimon, Norbert, additional, Petite, Fabrice G., additional, Petroulakis, Emmanuel, additional, Pfaff, Samuel L., additional, Piehler, Jacob, additional, Pike, Linda J., additional, Pinkoski, Michael J., additional, Pixley, Fiona J., additional, Plevani, Paolo, additional, Poo, Mu-ming, additional, Pozzan, Tullioi, additional, Prescott, Stephen M., additional, Prudovsky, Igor, additional, Putney, James W., additional, Radimerski, Thomas, additional, Radzio-Andzelm, Elzbieta, additional, Ram, Prahlad T., additional, Rameh, Lucia, additional, Ramljak, Danica, additional, Ranscht, Barbara, additional, Rao, Anjana, additional, Raport, Carol J., additional, Reeves, Jacqueline D., additional, Rehman, Holger, additional, Reichman, Trevor W., additional, Reiter, Eric, additional, Resnick, Michael A., additional, Reth, Michael, additional, Rhee, Sue Goo, additional, Richter, Joel D., additional, Rietze, Rodney L., additional, Rini, James M., additional, Ripperger, Jürgen A., additional, Rizo, Josep, additional, Robishaw, Janet D., additional, Roderick, H. Llewelyn, additional, Roeder, Robert G., additional, Rohrschneider, Larry R., additional, Ron, David, additional, Rosenfeld, Michael G., additional, Rosenfeldt, Hans, additional, Rossman, Kent L., additional, Roth, Christopher B., additional, Rudolph, Markus G., additional, Ruppelt, Anja, additional, Saez, Lino, additional, Sakmar, Thomas P., additional, Salvesen, Guy S., additional, Sassone-Corsi, Paolo, additional, Saxe, Charles L., additional, Schäfer, Beat W., additional, Schibler, Ueli, additional, Schindler, Christian W., additional, Schmelzle, Tobias, additional, Schmid, Sandra L., additional, Schmidt, Anja, additional, Schmidt, Eric F., additional, Schreiber, Gideon, additional, Schultz, Joachim E., additional, Schwaller, Beat, additional, Schwamborn, Klaus, additional, Schwartz, Thue, additional, Schwindinger, William F., additional, Scita, Giorgio, additional, Scott, John D., additional, Scott, Shaun, additional, Seebeck, Thomas, additional, Serhan, Charles N., additional, Shabb, John B., additional, Shaw, Andrey S., additional, Shears, Stephen B., additional, Shenolikar, Shirish, additional, Shi, Lei, additional, Shin, Chanseok, additional, Shiozaki, Kazuhiro, additional, Shokat, Kevan M., additional, Shuttleworth, Trevor J., additional, Siderovski, David P., additional, Siegelbaum, Steven A., additional, Silverstein, Adam M., additional, Singer, Robert H., additional, Skinner, Michael K., additional, Slack-Davis, Jill K., additional, Smerdon, Stephen J., additional, Smith, Graeme C.M., additional, Smits, Guillaume, additional, Smolik, Sarah M., additional, Smotrys, Jessica E., additional, Smyth, Emer M., additional, Snyder, Jason T., additional, Sogame, Naoko, additional, Soldi, Raffaella, additional, Sondek, John, additional, Sonenberg, Nahum, additional, Sonneberg, Erica Dutil, additional, Sparrow, Lindsay G., additional, Spiegel, Sarah, additional, Sprang, Stephen R., additional, Srivastava, Deepak, additional, Stanfield, Robyn L., additional, Stanley, E. Richard, additional, Stauber, Deborah J., additional, Stefan, Christopher, additional, Stenson-Holst, Lena, additional, Stephens, Len, additional, Sternberg, Paul W., additional, Sternweis, Paul C., additional, Steward, Ruth, additional, Stickney, John T., additional, Stoker, Andrew W., additional, Strittmatter, Stephen M., additional, Stronach, Beth E., additional, Strong, Roland K., additional, Stroud, Robert M., additional, Südhof, Thomas C., additional, Sunahara, Roger K., additional, Sutton, Brian J., additional, Szabolcs, Sipeki, additional, Tang, Xiao-Bo, additional, Taskén, Kjetil, additional, Tatebe, Hisashi, additional, Tauszig-Delamasure, Servane, additional, Taylor, Colin W., additional, Taylor, Garry L., additional, Taylor, Laura J., additional, Taylor, Susan S., additional, Thomas, George, additional, Thomas, Robert P., additional, Thompson, E. Brad, additional, Thompson, Michael J., additional, Thornton, Janet M., additional, Thummel, Carl S., additional, Togashi, Hideaki, additional, Tong, Amy Hin Yan, additional, Tonks, Nicholas K., additional, Tontonoz, Peter, additional, Topham, M.K., additional, Torgersen, Knut Martin, additional, Tran, Hien, additional, Tremblay, Michel L., additional, Tsai, Ming-Jer, additional, Tsai, Sophia Y., additional, Tsunoda, Susan, additional, Turley, Stewart, additional, Tyson, Darren, additional, Van Etten, Robert L., additional, Vassart, Gilbert, additional, Verveer, Peter J., additional, Vlaeminck, Virginie, additional, de Vos, Abraham M., additional, Voss, Ty C., additional, Walczak, Robert, additional, Walker, Graham C., additional, Walker, John C., additional, Walter, Gernot, additional, Walter, Mark R., additional, Wang, Fen, additional, Wang, Jean Y.J., additional, Wang, Weiru, additional, Ward, Richard J., additional, Wedegaertner, Philip, additional, Wehrle, Christian, additional, Weiss, Arthur, additional, Weiss, Jamie L., additional, Wells, Alan, additional, Werner, Claudia, additional, West, Ann H., additional, Weston, Marie C., additional, Westwick, John K., additional, Wetterholm, Anders, additional, White, Morris F., additional, Whitman, Malcolm, additional, Whorton, Matt R., additional, Wiesmann, Christian, additional, Williams, Roger L., additional, Willis, William D., additional, Willson, Timothy M., additional, Wilson, Ian A., additional, Wiser, Ofer, additional, Wishart, Matthew J., additional, Wittinghofer, Alfred, additional, Woodgett, James R., additional, Worthylake, David K., additional, Wrana, Jeffrey L., additional, Wu, Hao, additional, Xiao, Yijin, additional, Xu, H. Eric, additional, Xu, Yan, additional, Xu, Zheng, additional, Yaffe, Michael B., additional, Yamada, Kenneth M., additional, Yang, Seun-Ah, additional, Yang, Wannian, additional, Yarden, Yosef, additional, Ye, Hong, additional, Ye, Weilan, additional, Yeates, Todd O., additional, Yin, Helen L., additional, York, John D., additional, Young, Edgar C., additional, Young, Kenneth W., additional, Young, Matthew A., additional, Young, Michael W., additional, Yu, Minmin, additional, Zaccai, Nathan R., additional, Zaccolo, Manuela, additional, Zamir, Eli, additional, von Zastrow, Mark, additional, Zhang, Chao, additional, Zhang, Xuewu, additional, Zhang, Zhong-Yin, additional, Zhou, Wenhong, additional, and Zoraghi, Roya, additional

Published
2003
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50. Abscisic Acid-Triggered Persulfidation of Cysteine Protease ATG4 Mediates Regulation of Autophagy by Sulfide

Author

European Commission, Ministerio de Economía y Competitividad (España), Agencia Estatal de Investigación (España), Junta de Andalucía, Gobierno de Aragón, Yruela Guerrero, Inmaculada [0000-0003-3608-4720], Laureano-Marín, Ana M., Aroca, Ángeles, Pérez-Pérez, M. Esther, Yruela Guerrero, Inmaculada, Jurado-Flores, Ana, Moreno, Inmaculada, Crespo, José L., Romero, Luis C., Gotor, Cecilia, European Commission, Ministerio de Economía y Competitividad (España), Agencia Estatal de Investigación (España), Junta de Andalucía, Gobierno de Aragón, Yruela Guerrero, Inmaculada [0000-0003-3608-4720], Laureano-Marín, Ana M., Aroca, Ángeles, Pérez-Pérez, M. Esther, Yruela Guerrero, Inmaculada, Jurado-Flores, Ana, Moreno, Inmaculada, Crespo, José L., Romero, Luis C., and Gotor, Cecilia

Abstract

Hydrogen sulfide is a signaling molecule that regulates essential processes in plants, such as autophagy. In Arabidopsis (Arabidopsis thaliana), hydrogen sulfide negatively regulates autophagy independently of reactive oxygen species via an unknown mechanism. Comparative and quantitative proteomic analysis was used to detect abscisic acid-triggered persulfidation that reveals a main role in the control of autophagy mediated by the autophagy-related (ATG) Cys protease AtATG4a. This protease undergoes specific persulfidation of Cys170 that is a part of the characteristic catalytic Cys-His-Asp triad of Cys proteases. Regulation of the ATG4 activity by persulfidation was tested in a heterologous assay using the Chlamydomonas reinhardtii CrATG8 protein as a substrate. Sulfide significantly and reversibly inactivates AtATG4a. The biological significance of the reversible inhibition of the ATG4 by sulfide is supported by the results obtained in Arabidopsis leaves under basal and autophagy-activating conditions. A significant increase in the overall ATG4 proteolytic activity in Arabidopsis was detected under nitrogen starvation and osmotic stress and can be inhibited by sulfide. Therefore, the data strongly suggest that the negative regulation of autophagy by sulfide is mediated by specific persulfidation of the ATG4 protease.

Published
2020

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