Inner mitochondrial membrane protein Prohibitin 1 mediates Nix-induced, Parkin-independent mitophagy.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
02 01 2023
02 01 2023
Historique:
received:
04
09
2022
accepted:
20
12
2022
entrez:
2
1
2023
pubmed:
3
1
2023
medline:
5
1
2023
Statut:
epublish
Résumé
Autophagy of damaged mitochondria, called mitophagy, is an important organelle quality control process involved in the pathogenesis of inflammation, cancer, aging, and age-associated diseases. Many of these disorders are associated with altered expression of the inner mitochondrial membrane (IMM) protein Prohibitin 1. The mechanisms whereby dysfunction occurring internally at the IMM and matrix activate events at the outer mitochondrial membrane (OMM) to induce mitophagy are not fully elucidated. Using the gastrointestinal epithelium as a model system highly susceptible to autophagy inhibition, we reveal a specific role of Prohibitin-induced mitophagy in maintaining intestinal homeostasis. We demonstrate that Prohibitin 1 induces mitophagy in response to increased mitochondrial reactive oxygen species (ROS) through binding to mitophagy receptor Nix/Bnip3L and independently of Parkin. Prohibitin 1 is required for ROS-induced Nix localization to mitochondria and maintaining homeostasis of epithelial cells highly susceptible to mitochondrial dysfunction.
Identifiants
pubmed: 36593241
doi: 10.1038/s41598-022-26775-x
pii: 10.1038/s41598-022-26775-x
pmc: PMC9807637
doi:
Substances chimiques
Prohibitins
0
Reactive Oxygen Species
0
Membrane Proteins
0
Ubiquitin-Protein Ligases
EC 2.3.2.27
Mitochondrial Proteins
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
18Subventions
Organisme : NIDDK NIH HHS
ID : P30 DK048520
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK117001
Pays : United States
Informations de copyright
© 2023. The Author(s).
Références
Komatsu, M. et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol. 169(3), 425–434 (2005).
doi: 10.1083/jcb.200412022
Mizushima, N. et al. Autophagy fights disease through cellular self-digestion. Nature 451(7182), 1069–1075 (2008).
doi: 10.1038/nature06639
Iida, T. et al. Impact of autophagy of innate immune cells on inflammatory bowel disease. Cells 8(1), 7 (2018).
doi: 10.3390/cells8010007
Wu, Y. et al. The role of autophagy in maintaining intestinal mucosal barrier. J. Cell Physiol. 234(11), 19406–19419 (2019).
doi: 10.1002/jcp.28722
Nguyen, H. T. et al. Autophagy and Crohn’s disease. J. Innate Immun. 5(5), 434–443 (2013).
doi: 10.1159/000345129
Clevers, H. C. & Bevins, C. L. Paneth cells: Maestros of the small intestinal crypts. Annu. Rev. Physiol. 75, 289–311 (2013).
doi: 10.1146/annurev-physiol-030212-183744
Cadwell, K. et al. A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 456(7219), 259–263 (2008).
doi: 10.1038/nature07416
Patel, K. K. et al. Autophagy proteins control goblet cell function by potentiating reactive oxygen species production. EMBO J. 32(24), 3130–3144 (2013).
doi: 10.1038/emboj.2013.233
Kim, S., Eun, H. S. & Jo, E. K. Roles of autophagy-related genes in the pathogenesis of inflammatory bowel disease. Cells 8(1), 77 (2019).
doi: 10.3390/cells8010077
Cadwell, K. et al. A common role for Atg16L1, Atg5 and Atg7 in small intestinal Paneth cells and Crohn disease. Autophagy 5(2), 250–252 (2009).
doi: 10.4161/auto.5.2.7560
Liu, T. C. et al. Interaction between smoking and ATG16L1T300A triggers Paneth cell defects in Crohn’s disease. J. Clin. Investig. 128(11), 5110–5122 (2018).
doi: 10.1172/JCI120453
Ding, W. X. & Yin, X. M. Mitophagy: Mechanisms, pathophysiological roles, and analysis. Biol. Chem. 393(7), 547–564 (2012).
doi: 10.1515/hsz-2012-0119
Geisler, S. et al. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 12(2), 119–131 (2010).
doi: 10.1038/ncb2012
Lazarou, M. et al. The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature 524(7565), 309–314 (2015).
doi: 10.1038/nature14893
Hamacher-Brady, A. & Brady, N. R. Mitophagy programs: Mechanisms and physiological implications of mitochondrial targeting by autophagy. Cell Mol. Life Sci. 73(4), 775–795 (2016).
doi: 10.1007/s00018-015-2087-8
Jin, S. M. & Youle, R. J. The accumulation of misfolded proteins in the mitochondrial matrix is sensed by PINK1 to induce PARK2/Parkin-mediated mitophagy of polarized mitochondria. Autophagy 9(11), 1750–1757 (2013).
doi: 10.4161/auto.26122
Wang, Y. et al. ROS-induced mitochondrial depolarization initiates PARK2/PARKIN-dependent mitochondrial degradation by autophagy. Autophagy 8(10), 1462–1476 (2012).
doi: 10.4161/auto.21211
Li, X. et al. Targeting mitochondrial reactive oxygen species as novel therapy for inflammatory diseases and cancers. J. Hematol. Oncol. 6, 19 (2013).
doi: 10.1186/1756-8722-6-19
Back, J. W. et al. A structure for the yeast prohibitin complex: Structure prediction and evidence from chemical crosslinking and mass spectrometry. Protein Sci. 11(10), 2471–2478 (2002).
doi: 10.1110/ps.0212602
Merkwirth, C. & Langer, T. Prohibitin function within mitochondria: Essential roles for cell proliferation and cristae morphogenesis. Biochim. Biophys. Acta. 1793(1), 27–32 (2009).
doi: 10.1016/j.bbamcr.2008.05.013
Tatsuta, T., Model, K. & Langer, T. Formation of membrane-bound ring complexes by prohibitins in mitochondria. Mol. Biol. Cell. 16(1), 248–259 (2005).
doi: 10.1091/mbc.e04-09-0807
Xu, Y. et al. Prohibitin 1 regulates tumor cell apoptosis via the interaction with X-linked inhibitor of apoptosis protein. J. Mol. Cell Biol. 8(3), 282–285 (2016).
doi: 10.1093/jmcb/mjw018
Bourges, I. et al. Structural organization of mitochondrial human complex I: Role of the ND4 and ND5 mitochondria-encoded subunits and interaction with prohibitin. Biochem. J. 383(Pt. 3), 491–499 (2004).
doi: 10.1042/BJ20040256
Nijtmans, L. G. et al. Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. Embo J. 19(11), 2444–2451 (2000).
doi: 10.1093/emboj/19.11.2444
Barbier-Torres, L. & Lu, S. C. Prohibitin 1 in liver injury and cancer. Exp. Biol. Med. 245(5), 385–394 (2020).
doi: 10.1177/1535370220908257
Signorile, A. et al. Prohibitins: A critical role in mitochondrial functions and implication in diseases. Cells 8(1), 71 (2019).
doi: 10.3390/cells8010071
Theiss, A. L. et al. Prohibitin protects against oxidative stress in intestinal epithelial cells. FASEB J. 21(1), 197–206 (2007).
doi: 10.1096/fj.06-6801com
Wei, Y. et al. Prohibitin 2 is an inner mitochondrial membrane mitophagy receptor. Cell 168(1–2), 224-238.e10 (2017).
doi: 10.1016/j.cell.2016.11.042
Jackson, D. N. et al. Mitochondrial dysfunction during loss of prohibitin 1 triggers Paneth cell defects and ileitis. Gut 69(11), 1928–1938 (2020).
doi: 10.1136/gutjnl-2019-319523
Merkwirth, C. et al. Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria. Genes Dev. 22(4), 476–488 (2008).
doi: 10.1101/gad.460708
Kim, S. J. et al. Hepatitis B virus disrupts mitochondrial dynamics: Induces fission and mitophagy to attenuate apoptosis. PLoS Pathog. 9(12), e1003722 (2013).
doi: 10.1371/journal.ppat.1003722
Koopman, W. J. et al. Mammalian mitochondrial complex I: Biogenesis, regulation, and reactive oxygen species generation. Antioxid. Redox Signal. 12(12), 1431–1470 (2010).
doi: 10.1089/ars.2009.2743
Wang, D. et al. Prohibitin ligands: A growing armamentarium to tackle cancers, osteoporosis, inflammatory, cardiac and neurological diseases. Cell Mol. Life Sci. 77(18), 3525–3546 (2020).
doi: 10.1007/s00018-020-03475-1
Petit, P. X. et al. Disruption of the outer mitochondrial membrane as a result of large amplitude swelling: The impact of irreversible permeability transition. FEBS Lett. 426(1), 111–116 (1998).
doi: 10.1016/S0014-5793(98)00318-4
Ding, W. X. et al. Nix is critical to two distinct phases of mitophagy, reactive oxygen species-mediated autophagy induction and Parkin-ubiquitin-p62-mediated mitochondrial priming. J. Biol. Chem. 285(36), 27879–27890 (2010).
doi: 10.1074/jbc.M110.119537
Ho, G. T. & Theiss, A. L. Mitochondria and inflammatory bowel diseases: Toward a stratified therapeutic intervention. Annu. Rev. Physiol. 84, 435–459 (2022).
doi: 10.1146/annurev-physiol-060821-083306
Schweers, R. L. et al. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc. Natl. Acad. Sci. USA. 104(49), 19500–19505 (2007).
doi: 10.1073/pnas.0708818104
Maejima, I. et al. Autophagy sequesters damaged lysosomes to control lysosomal biogenesis and kidney injury. EMBO J. 32(17), 2336–2347 (2013).
doi: 10.1038/emboj.2013.171
Shibutani, S. T. & Yoshimori, T. Autophagosome formation in response to intracellular bacterial invasion. Cell Microbiol. 16(11), 1619–1626 (2014).
doi: 10.1111/cmi.12357
Chen, Y. et al. Dual autonomous mitochondrial cell death pathways are activated by Nix/BNip3L and induce cardiomyopathy. Proc. Natl. Acad. Sci. USA. 107(20), 9035–9042 (2010).
doi: 10.1073/pnas.0914013107
Sandoval, H. et al. Essential role for Nix in autophagic maturation of erythroid cells. Nature 454(7201), 232–235 (2008).
doi: 10.1038/nature07006
Yussman, M. G. et al. Mitochondrial death protein Nix is induced in cardiac hypertrophy and triggers apoptotic cardiomyopathy. Nat. Med. 8(7), 725–730 (2002).
doi: 10.1038/nm719
Zhang, W. et al. Nix-mediated mitophagy regulates platelet activation and life span. Blood Adv. 3(15), 2342–2354 (2019).
doi: 10.1182/bloodadvances.2019032334
Sowter, H. M. et al. HIF-1-dependent regulation of hypoxic induction of the cell death factors BNIP3 and NIX in human tumors. Cancer Res. 61(18), 6669–6673 (2001).
Vincent, G. et al. Nix-mediated mitophagy modulates mitochondrial damage during intestinal inflammation. Antioxid. Redox Signal. 33(1), 1–19 (2020).
doi: 10.1089/ars.2018.7702
Zhao, J. F. et al. HIF1alpha-dependent mitophagy facilitates cardiomyoblast differentiation. Cell Stress. 4(5), 99–113 (2020).
doi: 10.15698/cst2020.05.220
Jayatunga, D. P. W. et al. Therapeutic potential of mitophagy-inducing microflora metabolite, urolithin a for Alzheimer’s disease. Nutrients 13(11), 3744 (2021).
doi: 10.3390/nu13113744
Marinkovic, M., Sprung, M. & Novak, I. Dimerization of mitophagy receptor BNIP3L/NIX is essential for recruitment of autophagic machinery. Autophagy 17(5), 1232–1243 (2021).
doi: 10.1080/15548627.2020.1755120
Cho, S. G. et al. Bif-1 interacts with prohibitin-2 to regulate mitochondrial inner membrane during cell stress and apoptosis. J. Am. Soc. Nephrol. 30(7), 1174–1191 (2019).
doi: 10.1681/ASN.2018111117
Mannella, C. A. Consequences of folding the mitochondrial inner membrane. Front. Physiol. 11, 536 (2020).
doi: 10.3389/fphys.2020.00536
Rogov, V. V. et al. Phosphorylation of the mitochondrial autophagy receptor Nix enhances its interaction with LC3 proteins. Sci. Rep. 7(1), 1131 (2017).
doi: 10.1038/s41598-017-01258-6
McClung, J. K. et al. Prohibitin: Potential role in senescence, development, and tumor suppression. Exp. Gerontol. 30(2), 99–124 (1995).
doi: 10.1016/0531-5565(94)00069-7
Park, S. E. et al. Genetic deletion of the repressor of estrogen receptor activity (REA) enhances the response to estrogen in target tissues in vivo. Mol. Cell Biol. 25(5), 1989–1999 (2005).
doi: 10.1128/MCB.25.5.1989-1999.2005
Chen, G., Kroemer, G. & Kepp, O. Mitophagy: An emerging role in aging and age-associated diseases. Front. Cell Dev. Biol. 8, 200 (2020).
doi: 10.3389/fcell.2020.00200
Lachen-Montes, M. et al. Olfactory bulb neuroproteomics reveals a chronological perturbation of survival routes and a disruption of prohibitin complex during Alzheimer’s disease progression. Sci. Rep. 7(1), 9115 (2017).
doi: 10.1038/s41598-017-09481-x
Merkwirth, C. et al. Loss of prohibitin membrane scaffolds impairs mitochondrial architecture and leads to tau hyperphosphorylation and neurodegeneration. PLoS Genet. 8(11), e1003021 (2012).
doi: 10.1371/journal.pgen.1003021
Yang, J., Li, B. & He, Q. Y. Significance of prohibitin domain family in tumorigenesis and its implication in cancer diagnosis and treatment. Cell Death Dis. 9(6), 580 (2018).
doi: 10.1038/s41419-018-0661-3
Vara-Perez, M., Felipe-Abrio, B. & Agostinis, P. Mitophagy in cancer: A tale of adaptation. Cells 8(5), 493 (2019).
doi: 10.3390/cells8050493
Kathiria, A. S. et al. Prohibitin 1 modulates mitochondrial stress-related autophagy in human colonic epithelial cells. PLoS ONE 7(2), e31231 (2012).
doi: 10.1371/journal.pone.0031231
Agrawal, T., Gupta, G. K. & Agrawal, D. K. Vitamin D deficiency decreases the expression of VDR and prohibitin in the lungs of mice with allergic airway inflammation. Exp. Mol. Pathol. 93(1), 74–81 (2012).
doi: 10.1016/j.yexmp.2012.04.004
Guyot, A. C. et al. A small compound targeting prohibitin with potential interest for cognitive deficit rescue in aging mice and tau pathology treatment. Sci. Rep. 10(1), 1143 (2020).
doi: 10.1038/s41598-020-57560-3
Theiss, A. L. & Sitaraman, S. V. The role and therapeutic potential of prohibitin in disease. Biochim. Biophys. Acta. 1813(6), 1137–1143 (2011).
doi: 10.1016/j.bbamcr.2011.01.033
He, B. et al. Estrogen-regulated prohibitin is required for mouse uterine development and adult function. Endocrinology 152(3), 1047–1056 (2011).
doi: 10.1210/en.2010-0732
el Marjou, F. et al. Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 39(3), 186–193 (2004).
doi: 10.1002/gene.20042
Galvez, A. S. et al. Distinct pathways regulate proapoptotic Nix and BNip3 in cardiac stress. J. Biol. Chem. 281(3), 1442–1448 (2006).
doi: 10.1074/jbc.M509056200
Nenci, A. et al. Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature 446(7135), 557–561 (2007).
doi: 10.1038/nature05698
Moslehi, J. et al. Loss of hypoxia-inducible factor prolyl hydroxylase activity in cardiomyocytes phenocopies ischemic cardiomyopathy. Circulation 122(10), 1004–1016 (2010).
doi: 10.1161/CIRCULATIONAHA.109.922427
Theiss, A. L. et al. Prohibitin is a novel regulator of antioxidant response that attenuates colonic inflammation in mice. Gastroenterology 137(1), 199-208.e1-e6 (2009).
doi: 10.1053/j.gastro.2009.03.033