Anti- and pro-tumor functions of autophagy

doi:10.1016/J.BBAMCR.2009.01.006

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Anti- and pro-tumor functions of autophagy

Journal Article•DOI•

Anti- and pro-tumor functions of autophagy

Eugenia Morselli¹, Lorenzo Galluzzi¹, Lorenzo Galluzzi², Lorenzo Galluzzi³, Oliver Kepp¹, Oliver Kepp², Oliver Kepp³, José-Miguel Vicencio¹, José-Miguel Vicencio², José-Miguel Vicencio³, Alfredo Criollo³, Alfredo Criollo¹, Alfredo Criollo², Maria Chiara Maiuri, Guido Kroemer³, Guido Kroemer², Guido Kroemer¹ - Show less +13 more•Institutions (3)

French Institute of Health and Medical Research¹, Institut Gustave Roussy², University of Paris-Sud³

01 Sep 2009-Biochimica et Biophysica Acta (Elsevier)-Vol. 1793, Iss: 9, pp 1524-1532

TL;DR: Current knowledge is reviewed on the dual role of autophagy as an anti- and pro-tumor mechanism, which would represent a major therapeutic target for chemosensitization.

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About: This article is published in Biochimica et Biophysica Acta.The article was published on 2009-09-01 and is currently open access. It has received 354 citations till now. The article focuses on the topics: BAG3 & Autophagy.

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Journal Article•DOI•

Regulation of Mammalian Autophagy in Physiology and Pathophysiology

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Brinda Ravikumar¹, Sovan Sarkar¹, Janet E. Davies¹, Marie Futter¹, Moisés García-Arencibia¹, Zeyn W. Green-Thompson¹, Maria Jimenez-Sanchez¹, Viktor I. Korolchuk¹, Maike Lichtenberg¹, Shouqing Luo¹, Dunecan Massey¹, Fiona M. Menzies¹, Kevin Moreau¹, Usha Narayanan¹, Maurizio Renna¹, Farah H. Siddiqi¹, Benjamin R. Underwood¹, Ashley R. Winslow¹, David C. Rubinsztein¹ - Show less +15 more•Institutions (1)

University of Cambridge¹

01 Oct 2010-Physiological Reviews

TL;DR: This review focuses on mammalian autophagy, and an overview of the understanding of its machinery and the signaling cascades that regulate it is given, and the possibility of autophagic upregulation as a therapeutic approach for various conditions is considered.

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Abstract: (Macro)autophagy is a bulk degradation process that mediates the clearance of long-lived proteins and organelles. Autophagy is initiated by double-membraned structures, which engulf portions of cytoplasm. The resulting autophagosomes ultimately fuse with lysosomes, where their contents are degraded. Although the term autophagy was first used in 1963, the field has witnessed dramatic growth in the last 5 years, partly as a consequence of the discovery of key components of its cellular machinery. In this review we focus on mammalian autophagy, and we give an overview of the understanding of its machinery and the signaling cascades that regulate it. As recent studies have also shown that autophagy is critical in a range of normal human physiological processes, and defective autophagy is associated with diverse diseases, including neurodegeneration, lysosomal storage diseases, cancers, and Crohn's disease, we discuss the roles of autophagy in health and disease, while trying to critically evaluate if the coincidence between autophagy and these conditions is causal or an epiphenomenon. Finally, we consider the possibility of autophagy upregulation as a therapeutic approach for various conditions.

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1,616 citations

Journal Article•DOI•

Programmed cell death pathways in cancer: a review of apoptosis, autophagy and programmed necrosis

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Liang Ouyang¹, Ziyan Shi², Ziyan Shi¹, S. Zhao¹, Fang Wang¹, T.-T. Zhou³, Bo Liu¹, Jinku Bao¹ - Show less +4 more•Institutions (3)

Sichuan University¹, Guizhou Normal University², Second Military Medical University³

01 Dec 2012-Cell Proliferation

TL;DR: Understanding PCD and the complex interplay between apoptosis, autophagy and programmed necrosis pathways and apoptosis‐related microRNA regulation, in cancer may ultimately allow scientists and clinicians to harness the three types of PCD for discovery of further novel drug targets, in the future cancer treatment.

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Abstract: Programmed cell death (PCD), referring to apoptosis, autophagy and programmed necrosis, is proposed to be death of a cell in any pathological format, when mediated by an intracellular program. These three forms of PCD may jointly decide the fate of cells of malignant neoplasms; apoptosis and programmed necrosis invariably contribute to cell death, whereas autophagy can play either pro-survival or pro-death roles. Recent bulk of accumulating evidence has contributed to a wealth of knowledge facilitating better understanding of cancer initiation and progression with the three distinctive types of cell death. To be able to decipher PCD signalling pathways may aid development of new targeted anti-cancer therapeutic strategies. Thus in this review, we present a brief outline of apoptosis, autophagy and programmed necrosis pathways and apoptosis-related microRNA regulation, in cancer. Taken together, understanding PCD and the complex interplay between apoptosis, autophagy and programmed necrosis may ultimately allow scientists and clinicians to harness the three types of PCD for discovery of further novel drug targets, in the future cancer treatment.

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1,197 citations

Journal Article•DOI•

Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice.

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Mickaël Michaud¹, Mickaël Michaud², Mickaël Michaud³, Isabelle Martins², Isabelle Martins¹, Isabelle Martins³, Abdul Qader Sukkurwala², Abdul Qader Sukkurwala³, Abdul Qader Sukkurwala¹, Sandy Adjemian¹, Sandy Adjemian³, Sandy Adjemian², Yuting Ma, Patrizia Pellegatti⁴, Shensi Shen¹, Shensi Shen³, Shensi Shen², Oliver Kepp³, Oliver Kepp², Oliver Kepp¹, Marie Scoazec², Grégoire Mignot⁵, Santiago Rello-Varona³, Santiago Rello-Varona¹, Santiago Rello-Varona², Maximilien Tailler³, Maximilien Tailler¹, Maximilien Tailler², Laurie Menger¹, Laurie Menger³, Laurie Menger², Erika Vacchelli², Erika Vacchelli¹, Erika Vacchelli³, Lorenzo Galluzzi³, Lorenzo Galluzzi¹, Lorenzo Galluzzi², François Ghiringhelli⁵, Francesco Di Virgilio⁴, Laurence Zitvogel, Guido Kroemer - Show less +37 more•Institutions (5)

University of Paris-Sud¹, Institut Gustave Roussy², French Institute of Health and Medical Research³, University of Ferrara⁴, University of Burgundy⁵

16 Dec 2011-Science

TL;DR: It is demonstrated that autophagy, which is often disabled in cancer, is dispensable for chemotherapy-induced cell death but required for its immunogenicity, and increased extracellular ATP concentrations improve the efficacy of antineoplastic chemotherapies when Autophagy is disabled.

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Abstract: Antineoplastic chemotherapies are particularly efficient when they elicit immunogenic cell death, thus provoking an anticancer immune response. Here we demonstrate that autophagy, which is often disabled in cancer, is dispensable for chemotherapy-induced cell death but required for its immunogenicity. In response to chemotherapy, autophagy-competent, but not autophagy-deficient, cancers attracted dendritic cells and T lymphocytes into the tumor bed. Suppression of autophagy inhibited the release of adenosine triphosphate (ATP) from dying tumor cells. Conversely, inhibition of extracellular ATP-degrading enzymes increased pericellular ATP in autophagy-deficient tumors, reestablished the recruitment of immune cells, and restored chemotherapeutic responses but only in immunocompetent hosts. Thus, autophagy is essential for the immunogenic release of ATP from dying cells, and increased extracellular ATP concentrations improve the efficacy of antineoplastic chemotherapies when autophagy is disabled.

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1,139 citations

Journal Article•DOI•

ROS signalling in the biology of cancer.

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Jennifer N. Moloney¹, Thomas G. Cotter¹•Institutions (1)

University College Cork¹

03 Jun 2017-Seminars in Cell & Developmental Biology

TL;DR: The generation and sources of ROS within tumour cells, the regulation of ROS by antioxidant defence systems, as well as the effect of elevated ROS production on their signalling targets in cancer are discussed.

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1,100 citations

Journal Article•DOI•

Structure and dynamics of molecular networks: A novel paradigm of drug discovery: A comprehensive review

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Peter Csermely¹, Tamas Korcsmaros², Tamas Korcsmaros¹, Huba Kiss¹, Gábor London³, Ruth Nussinov⁴, Ruth Nussinov⁵ - Show less +3 more•Institutions (5)

Semmelweis University¹, Eötvös Loránd University², École Polytechnique Fédérale de Lausanne³, Science Applications International Corporation⁴, Tel Aviv University⁵

01 Jun 2013-Pharmacology & Therapeutics

TL;DR: It is shown how network techniques can help in the identification of single-target, edgetic, multi-target and allo-network drug target candidates and an optimized protocol of network-aided drug development is suggested, and a list of systems-level hallmarks of drug quality is provided.

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806 citations

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References

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Open Access

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Journal Article•DOI•

The hallmarks of cancer.

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Douglas Hanahan¹, Robert A. Weinberg²•Institutions (2)

University of California, San Francisco¹, Massachusetts Institute of Technology²

07 Jan 2000-Cell

TL;DR: This work has been supported by the Department of the Army and the National Institutes of Health, and the author acknowledges the support and encouragement of the National Cancer Institute.

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28,811 citations

"Anti- and pro-tumor functions of au..." refers background in this paper

...Thus, disabled autophagy might constitute a common feature of cancer that adds to the hallmarks originally formulated in 2000 by Hanahan and Weinberg [108] and more recently integrated by other authors [109,110], namely provision of autonomous growth stimuli, insensitivity to antiproliferative signals, disabled apoptosis, limitless replication, production of angiogenic factors, tissue invasion with metastasis [108], avoidance of the immune response [110], and enhanced anabolic metabolism [109]....
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...In 2000, Hanahan andWeinberg [108] enum growth signals, insensitivity to antiproliferative signals, unlimited replicative potential, pro Subsequently, escape from immune surveillance and enhanced anabolism have been prop suppressor mechanism by (at least) three distinct means, namely by preserving genome s inflammation....
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Journal Article•DOI•

Surfing the p53 network

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Bert Vogelstein¹, David P. Lane², Arnold J. Levine³•Institutions (3)

Howard Hughes Medical Institute¹, University of Dundee², Rockefeller University³

16 Nov 2000-Nature

TL;DR: The p53 tumour-suppressor gene integrates numerous signals that control cell life and death, and the disruption of p53 has severe consequences when a highly connected node in the Internet breaks down.

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Abstract: The p53 tumour-suppressor gene integrates numerous signals that control cell life and death. As when a highly connected node in the Internet breaks down, the disruption of p53 has severe consequences.

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6,605 citations

"Anti- and pro-tumor functions of au..." refers background in this paper

..., ATM, Chk1), following the amplification-dependent overexpression of MDM2, the E3 ubiquitin ligase that directs p53 to proteasomemediated degradation, or as a result of the loss of p14 function [72,73]....
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...p53 was initially described as a transcription factor that transactivates pro-apoptotic and cell cycle arresting programs [72], therefore inducing apoptosis and/or senescence of cancer cells characterized by irreparable genomic alterations, either in the context of tumor progression or following chemo- and/or radiotherapy [73]....
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Journal Article•DOI•

Autophagy in the Pathogenesis of Disease

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Beth Levine¹, Guido Kroemer², Guido Kroemer³, Guido Kroemer⁴•Institutions (4)

University of Texas Southwestern Medical Center¹, University of Paris-Sud², French Institute of Health and Medical Research³, Institut Gustave Roussy⁴

11 Jan 2008-Cell

TL;DR: This Review summarizes recent advances in understanding the physiological functions of autophagy and its possible roles in the causation and prevention of human diseases.

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6,301 citations

"Anti- and pro-tumor functions of au..." refers background in this paper

...Autophagic vacuolization has been observed in numerous pathophysiological scenarios [5,6], and the term “autophagic cell death” has been extensively employed to indicate a cell death subroutine lacking themorphological features of classical apoptosis and rathermanifesting with the cytoplasmic accumulation of autophagosomes [7]....
[...]

Journal Article•DOI•

Development by Self-Digestion: Molecular Mechanisms and Biological Functions of Autophagy

[...]

Beth Levine¹, Daniel J. Klionsky²•Institutions (2)

Columbia University¹, University of Michigan²

01 Apr 2004-Developmental Cell

TL;DR: This review summarizes the current knowledge about the molecular machinery of autophagy and the role of the autophagic machinery in eukaryotic development and identifies a set of evolutionarily conserved genes that are essential forAutophagy.

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3,721 citations

"Anti- and pro-tumor functions of au..." refers background in this paper

...Autophagic vacuolization has been observed in numerous pathophysiological scenarios [5,6], and the term “autophagic cell death” has been extensively employed to indicate a cell death subroutine lacking themorphological features of classical apoptosis and rathermanifesting with the cytoplasmic accumulation of autophagosomes [7]....
[...]

Journal Article•DOI•

Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy.

[...]

Sophie Pattingre¹, Sophie Pattingre², Amina T. Tassa², Xueping Qu¹, Xueping Qu², Rita Garuti², Xiao Huan Liang¹, Noboru Mizushima³, Milton Packer², Michael D. Schneider⁴, Beth Levine¹, Beth Levine² - Show less +8 more•Institutions (4)

Columbia University¹, University of Texas Southwestern Medical Center², Institute of Medical Science³, Baylor College of Medicine⁴

23 Sep 2005-Cell

TL;DR: Bcl-2 not only functions as an antiapoptotic protein, but also as an antiautophagy protein via its inhibitory interaction with Beclin 1, which may help maintain autophagy at levels that are compatible with cell survival, rather than cell death.

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3,384 citations

"Anti- and pro-tumor functions of au..." refers background in this paper

...In particular, anti-apoptotic factors like Bcl-2 [41], Bcl-XL [42], Bcl-w [43] and Mcl-1 [42] suppress autophagy, mainly by interacting with and therefore inhibiting Bec-1....
[...]