Mitophagy in tumorigenesis and metastasis

Cells use mitophagy to remove dysfunctional or excess mitochondria, frequently in response to imposed stresses, such as hypoxia and nutrient deprivation. Mitochondrial cargo receptors (MCR) induced by these stresses target mitochondria to autophagosomes through interaction with members of the LC3/GA...

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Published inCellular and molecular life sciences : CMLS Vol. 78; no. 8; pp. 3817 - 3851
Main Authors Poole, Logan P., Macleod, Kay F.
Format Journal Article
LanguageEnglish
Published Cham Springer International Publishing 01.04.2021
Springer Nature B.V
Subjects
Animals
Atrophy
autophagosomes
Biochemistry
Biomedical and Life Sciences
Biomedicine
BNIP3 protein
Cachexia
Cancer
carcinogenesis
Carcinogenesis - metabolism
Carcinogenesis - pathology
Cardiolipin
cardiolipins
Cell Biology
Cell cycle
Cell migration
cell movement
Cell survival
Ceramide
ceramides
Deprivation
Extracellular matrix
family
GABARAP protein
Humans
Hypoxia
Life Sciences
Lipids
Metastases
Metastasis
Mitochondria
Mitochondria - metabolism
Mitochondria - pathology
Mitochondrial Damage Control
Mitochondrial DNA
Mitochondrial Dynamics
mitochondrial proteins
Mitophagy
Modulators
Neoplasm Metastasis - pathology
Neoplasms - metabolism
Neoplasms - pathology
Parkin protein
Phagosomes
Prohibitin
PTEN-induced putative kinase
Review
Signal transduction
Signaling
Sirtuins
Sphingosine 1-phosphate
Stresses
therapeutics
Tumorigenesis
Ubiquitination
Sirtuins
Mitohormesis
BNIP3/BNIP3L
LC3/GABARAP
PARP
Cachexia
Metastasis
Mitophagy
Metabolism
Autophagy
Fission
DRP1
Electron transport chain
NAD
Mitochondria
PINK1/Parkin
BCL2-L-13
FUNDC1
UPR
ROS
AMPK
Respiration
FoxOs
ATF4
UPRmt
Online AccessGet full text
ISSN1420-682X
1420-9071
1420-9071
DOI10.1007/s00018-021-03774-1

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Abstract Cells use mitophagy to remove dysfunctional or excess mitochondria, frequently in response to imposed stresses, such as hypoxia and nutrient deprivation. Mitochondrial cargo receptors (MCR) induced by these stresses target mitochondria to autophagosomes through interaction with members of the LC3/GABARAP family. There are a growing number of these MCRs, including BNIP3, BNIP3L, FUNDC1, Bcl2-L-13, FKBP8, Prohibitin-2, and others, in addition to mitochondrial protein targets of PINK1/Parkin phospho-ubiquitination. There is also an emerging link between mitochondrial lipid signaling and mitophagy where ceramide, sphingosine-1-phosphate, and cardiolipin have all been shown to promote mitophagy. Here, we review the upstream signaling mechanisms that regulate mitophagy, including components of the mitochondrial fission machinery, AMPK, ATF4, FoxOs, Sirtuins, and mtDNA release, and address the significance of these pathways for stress responses in tumorigenesis and metastasis. In particular, we focus on how mitophagy modulators intersect with cell cycle control and survival pathways in cancer, including following ECM detachment and during cell migration and metastasis. Finally, we interrogate how mitophagy affects tissue atrophy during cancer cachexia and therapy responses in the clinic.
AbstractList Cells use mitophagy to remove dysfunctional or excess mitochondria, frequently in response to imposed stresses, such as hypoxia and nutrient deprivation. Mitochondrial cargo receptors (MCR) induced by these stresses target mitochondria to autophagosomes through interaction with members of the LC3/GABARAP family. There are a growing number of these MCRs, including BNIP3, BNIP3L, FUNDC1, Bcl2-L-13, FKBP8, Prohibitin-2, and others, in addition to mitochondrial protein targets of PINK1/Parkin phospho-ubiquitination. There is also an emerging link between mitochondrial lipid signaling and mitophagy where ceramide, sphingosine-1-phosphate, and cardiolipin have all been shown to promote mitophagy. Here, we review the upstream signaling mechanisms that regulate mitophagy, including components of the mitochondrial fission machinery, AMPK, ATF4, FoxOs, Sirtuins, and mtDNA release, and address the significance of these pathways for stress responses in tumorigenesis and metastasis. In particular, we focus on how mitophagy modulators intersect with cell cycle control and survival pathways in cancer, including following ECM detachment and during cell migration and metastasis. Finally, we interrogate how mitophagy affects tissue atrophy during cancer cachexia and therapy responses in the clinic.
Cells use mitophagy to remove dysfunctional or excess mitochondria, frequently in response to imposed stresses, such as hypoxia and nutrient deprivation. Mitochondrial cargo receptors (MCR) induced by these stresses target mitochondria to autophagosomes through interaction with members of the LC3/GABARAP family. There are a growing number of these MCRs, including BNIP3, BNIP3L, FUNDC1, Bcl2-L-13, FKBP8, Prohibitin-2, and others, in addition to mitochondrial protein targets of PINK1/Parkin phospho-ubiquitination. There is also an emerging link between mitochondrial lipid signaling and mitophagy where ceramide, sphingosine-1-phosphate, and cardiolipin have all been shown to promote mitophagy. Here, we review the upstream signaling mechanisms that regulate mitophagy, including components of the mitochondrial fission machinery, AMPK, ATF4, FoxOs, Sirtuins, and mtDNA release, and address the significance of these pathways for stress responses in tumorigenesis and metastasis. In particular, we focus on how mitophagy modulators intersect with cell cycle control and survival pathways in cancer, including following ECM detachment and during cell migration and metastasis. Finally, we interrogate how mitophagy affects tissue atrophy during cancer cachexia and therapy responses in the clinic.Cells use mitophagy to remove dysfunctional or excess mitochondria, frequently in response to imposed stresses, such as hypoxia and nutrient deprivation. Mitochondrial cargo receptors (MCR) induced by these stresses target mitochondria to autophagosomes through interaction with members of the LC3/GABARAP family. There are a growing number of these MCRs, including BNIP3, BNIP3L, FUNDC1, Bcl2-L-13, FKBP8, Prohibitin-2, and others, in addition to mitochondrial protein targets of PINK1/Parkin phospho-ubiquitination. There is also an emerging link between mitochondrial lipid signaling and mitophagy where ceramide, sphingosine-1-phosphate, and cardiolipin have all been shown to promote mitophagy. Here, we review the upstream signaling mechanisms that regulate mitophagy, including components of the mitochondrial fission machinery, AMPK, ATF4, FoxOs, Sirtuins, and mtDNA release, and address the significance of these pathways for stress responses in tumorigenesis and metastasis. In particular, we focus on how mitophagy modulators intersect with cell cycle control and survival pathways in cancer, including following ECM detachment and during cell migration and metastasis. Finally, we interrogate how mitophagy affects tissue atrophy during cancer cachexia and therapy responses in the clinic.
Author Poole, Logan P.
Macleod, Kay F.
AuthorAffiliation 1 The Ben May Department for Cancer Research, The Gordon Center for Integrative Sciences, W-338, The University of Chicago, 929 E 57th Street, Chicago, IL 60637, USA
2 The Committee on Cancer Biology, The University of Chicago, Chicago, USA
AuthorAffiliation_xml – name: 1 The Ben May Department for Cancer Research, The Gordon Center for Integrative Sciences, W-338, The University of Chicago, 929 E 57th Street, Chicago, IL 60637, USA
– name: 2 The Committee on Cancer Biology, The University of Chicago, Chicago, USA
Author_xml – sequence: 1
  givenname: Logan P.
  surname: Poole
  fullname: Poole, Logan P.
  organization: The Ben May Department for Cancer Research, The Gordon Center for Integrative Sciences, W-338, The University of Chicago, The Committee on Cancer Biology, The University of Chicago
– sequence: 2
  givenname: Kay F.
  surname: Macleod
  fullname: Macleod, Kay F.
  email: kmacleod@uchicago.edu
  organization: The Ben May Department for Cancer Research, The Gordon Center for Integrative Sciences, W-338, The University of Chicago, The Committee on Cancer Biology, The University of Chicago
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33580835$$D View this record in MEDLINE/PubMed
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Mitohormesis
BNIP3/BNIP3L
LC3/GABARAP
PARP
Cachexia
Metastasis
Mitophagy
Metabolism
Autophagy
Fission
DRP1
Electron transport chain
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SubjectTerms Animals
Atrophy
autophagosomes
Biochemistry
Biomedical and Life Sciences
Biomedicine
BNIP3 protein
Cachexia
Cancer
carcinogenesis
Carcinogenesis - metabolism
Carcinogenesis - pathology
Cardiolipin
cardiolipins
Cell Biology
Cell cycle
Cell migration
cell movement
Cell survival
Ceramide
ceramides
Deprivation
Extracellular matrix
family
GABARAP protein
Humans
Hypoxia
Life Sciences
Lipids
Metastases
Metastasis
Mitochondria
Mitochondria - metabolism
Mitochondria - pathology
Mitochondrial Damage Control
Mitochondrial DNA
Mitochondrial Dynamics
mitochondrial proteins
Mitophagy
Modulators
Neoplasm Metastasis - pathology
Neoplasms - metabolism
Neoplasms - pathology
Parkin protein
Phagosomes
Prohibitin
PTEN-induced putative kinase
Review
Signal transduction
Signaling
Sirtuins
Sphingosine 1-phosphate
Stresses
therapeutics
Tumorigenesis
Ubiquitination
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Title Mitophagy in tumorigenesis and metastasis
URI https://link.springer.com/article/10.1007/s00018-021-03774-1
https://www.ncbi.nlm.nih.gov/pubmed/33580835
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