1,289
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

ROS-mediated lysosomal membrane permeabilization and autophagy inhibition regulate bleomycin-induced cellular senescence

, , , , , , , , , , , , , ORCID Icon & show all
Received 06 Jun 2023, Accepted 06 May 2024, Published online: 18 May 2024

References

  • Watson RA, De La Peña H, Tsakok MT, et al. Development of a best-practice clinical guideline for the use of bleomycin in the treatment of germ cell tumours in the UK. Br J Cancer. 2018;119(9):1044–1051. doi: 10.1038/s41416-018-0300-x
  • Della Latta V, Cecchettini A, Del Ry S, et al. Bleomycin in the setting of lung fibrosis induction: from biological mechanisms to counteractions. Pharmacological Research. 2015 Jul;97:122–130. doi: 10.1016/j.phrs.2015.04.012
  • Sleijfer S. Bleomycin-induced pneumonitis. Chest. 2001 Aug;120(2):617–624. doi: 10.1378/chest.120.2.617
  • Cheng T, Liu Q, Zhang R, et al. Lysyl oxidase promotes bleomycin-induced lung fibrosis through modulating inflammation. J Mol Cell Biol. 2014 Dec;6(6):506–515. doi: 10.1093/jmcb/mju039
  • Sawada H, Ibi M, Kihara T, et al. Mechanisms of antiapoptotic effects of estrogens in nigral dopaminergic neurons. Faseb J. 2000;14(9):1202–1214. doi: 10.1096/fasebj.14.9.1202
  • Getsy PM, Mayer CA, MacFarlane PM, et al. Acute lung injury in neonatal rats causes postsynaptic depression in nucleus tractus solitarii second-order neurons. Respir Physiol Neurobiol. 2019;269:103250. doi: 10.1016/j.resp.2019.103250
  • Linge A, Weinhold K, Bläsche R, et al. Downregulation of caveolin-1 affects bleomycin-induced growth arrest and cellular senescence in A549 cells. Int J Biochem Cell Biol. 2007;39(10):1964–1974. doi: 10.1016/j.biocel.2007.05.018
  • Kasper M, Barth K. Bleomycin and its role in inducing apoptosis and senescence in lung cells - modulating effects of caveolin-1. Curr Cancer Drug Targets. 2009;9(3):341–353. doi: 10.2174/156800909788166501
  • Hemnes AR, Zaiman A, Champion HC. PDE5A inhibition attenuates bleomycin-induced pulmonary fibrosis and pulmonary hypertension through inhibition of ROS generation and RhoA/Rho kinase activation. Am J Physiol Lung Cell Mol Physiol. 2008;294(1):L24–L33. doi: 10.1152/ajplung.00245.2007
  • Zhou Z, Yin Y, Chang Q, et al. Downregulation of B-myb promotes senescence via the ROS-mediated p53/p21 pathway, in vascular endothelial cells. Cell Prolif. 2017;50(2). doi: 10.1111/cpr.12319
  • Hernandez-Segura A, Nehme J, Demaria M. Hallmarks of cellular senescence. Trends Cell Biol. 2018 Jun;28(6):436–453. doi: 10.1016/j.tcb.2018.02.001
  • Di Micco R, Krizhanovsky V, Baker D, et al. Cellular senescence in ageing: from mechanisms to therapeutic opportunities. Nat Rev Mol Cell Biol. 2021 Feb;22(2):75–95. doi: 10.1038/s41580-020-00314-w
  • Guo J, Huang X, Dou L, et al. Aging and aging-related diseases: from molecular mechanisms to interventions and treatments. Signal Transduct Target Ther. [2022 Dec 16];7(1):391. doi: 10.1038/s41392-022-01251-0
  • Aoshiba K, Tsuji T, Nagai A. Bleomycin induces cellular senescence in alveolar epithelial cells. Eur Respir J. 2003;22(3):436–443. doi: 10.1183/09031936.03.00011903
  • Huang P, Zhou Y, Li X-H, et al. N-methyl-D-aspartate receptor blockers attenuate bleomycin-induced pulmonary fibrosis by inhibiting endogenous mesenchymal stem cells senescence. Ann Transl Med. 2022;10(11):642. doi: 10.21037/atm-22-2507
  • Zhang Y, Liang Q, Zhang Y, et al. Olmesartan alleviates bleomycin-mediated vascular smooth muscle cell senescence via the miR-665/SDC1 axis. Am J Transl Res. 2020;12(9):5205–5220.
  • Nie D, Zhang J, Zhou Y, et al. Rapamycin treatment of tendon stem/progenitor cells reduces cellular senescence by upregulating autophagy. Stem Cells Int. 2021;2021:1–10. doi: 10.1155/2021/6638249
  • Dikic I, Elazar Z. Mechanism and medical implications of mammalian autophagy. Nat Rev Mol Cell Biol. 2018;19(6):349–364. doi: 10.1038/s41580-018-0003-4
  • Serrano-Puebla A, Boya P. Lysosomal membrane permeabilization in cell death: new evidence and implications for health and disease. Ann N Y Acad Sci. 2016;1371(1):30–44. doi: 10.1111/nyas.12966
  • Tan JX, Finkel T. A phosphoinositide signalling pathway mediates rapid lysosomal repair. Nature. 2022 Sep;609(7928):815–821. doi: 10.1038/s41586-022-05164-4
  • Korolchuk VI, Saiki S, Lichtenberg M, et al. Lysosomal positioning coordinates cellular nutrient responses. Nat Cell Biol. 2011;13(4):453–460. doi: 10.1038/ncb2204
  • Jia R, Guardia CM, Pu J, et al. BORC coordinates encounter and fusion of lysosomes with autophagosomes. Autophagy. 2017;13(10):1648–1663. doi: 10.1080/15548627.2017.1343768
  • Rabanal-Ruiz Y, Otten EG, Korolchuk VI, et al. mTORC1 as the main gateway to autophagy. Essays Biochem. 2017;61(6):565–584. doi: 10.1042/EBC20170027
  • Chen X, Yu C, Kang R, et al. Cellular degradation systems in ferroptosis. Cell Death Differ. 2021 Apr;28(4):1135–1148. doi: 10.1038/s41418-020-00728-1
  • Su S, Shi Y-T, Chu Y, et al. Sec62 promotes gastric cancer metastasis through mediating UPR-induced autophagy activation. Cell Mol Life Sci. 2022;79(2):133. doi: 10.1007/s00018-022-04143-2
  • Choi GE, Lee HJ, Chae CW, et al. BNIP3L/NIX-mediated mitophagy protects against glucocorticoid-induced synapse defects. Nat Commun. 2021;12(1):487. doi: 10.1038/s41467-020-20679-y
  • Krobitsch S, Lindquist S. Aggregation of huntingtin in yeast varies with the length of the polyglutamine expansion and the expression of chaperone proteins. Proc Natl Acad Sci USA. 2000;97(4):1589–1594. doi: 10.1073/pnas.97.4.1589
  • Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy. 2007;3(5):452–460. doi: 10.4161/auto.4451
  • Itakura E, Kishi-Itakura C, Mizushima N. The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell. 2012;151(6):1256–1269. doi: 10.1016/j.cell.2012.11.001
  • Sardiello M, Palmieri M, di Ronza A, et al. A gene network regulating lysosomal biogenesis and function. Science. 2009;325(5939):473–477. doi: 10.1126/science.1174447
  • Sankaranarayanan S, De Angelis D, Rothman JE, et al. The use of pHluorins for optical measurements of presynaptic activity. Biophys J. 2000;79(4):2199–2208. doi: 10.1016/S0006-3495(00)76468-X
  • Aits S, Kricker J, Liu B, et al. Sensitive detection of lysosomal membrane permeabilization by lysosomal galectin puncta assay. Autophagy. 2015;11(8):1408–1424. doi: 10.1080/15548627.2015.1063871
  • Ishida Y, Kuninaka Y, Mukaida N, et al. Immune mechanisms of pulmonary fibrosis with Bleomycin. Int J Mol Sci. [2023 Feb 5];24(4):3149. doi: 10.3390/ijms24043149
  • Tai H, Wang Z, Gong H, et al. Autophagy impairment with lysosomal and mitochondrial dysfunction is an important characteristic of oxidative stress-induced senescence. Autophagy. 2017;13(1):99–113. doi: 10.1080/15548627.2016.1247143
  • Wu R, Wyatt E, Chawla K, et al. Hexokinase II knockdown results in exaggerated cardiac hypertrophy via increased ROS production. EMBO Mol Med. 2012;4(7):633–646. doi: 10.1002/emmm.201200240
  • Tyagi M, Bauri AK, Chattopadhyay S, et al. Thiol antioxidants sensitize malabaricone C induced cancer cell death via reprogramming redox sensitive p53 and NF-κB proteins in vitro and in vivo. Free Radic Biol Med. 2020;148:182–199. doi: 10.1016/j.freeradbiomed.2020.01.011
  • Wang K, Zhang T, Lei Y, et al. Identification of ANXA2 (annexin A2) as a specific bleomycin target to induce pulmonary fibrosis by impeding TFEB-mediated autophagic flux. Autophagy. 2018;14(2):269–282. doi: 10.1080/15548627.2017.1409405
  • Herranz N, Gallage S, Mellone M, et al. mTOR regulates MAPKAPK2 translation to control the senescence-associated secretory phenotype. Nat Cell Biol. 2015 Sep;17(9):1205–1217. doi: 10.1038/ncb3225
  • Chung CL, Lawrence I, Hoffman M, et al. Topical rapamycin reduces markers of senescence and aging in human skin: an exploratory, prospective, randomized trial. Geroscience. 2019 Dec;41(6):861–869. doi: 10.1007/s11357-019-00113-y
  • Zhang S, Cai G, Fu B, et al. SIRT1 is required for the effects of rapamycin on high glucose-inducing mesangial cells senescence. Mech Ageing Dev. 2012 Jun;133(6):387–400. doi: 10.1016/j.mad.2012.04.005
  • Iglesias-Bartolome R, Patel V, Cotrim A, et al. mTOR inhibition prevents epithelial stem cell senescence and protects from radiation-induced mucositis. Cell Stem Cell. [2012 Sep 7];11(3):401–414. doi: 10.1016/j.stem.2012.06.007
  • Vats TS, Morantz RA, Wood GW, et al. Study of effectiveness of bleomycin in rat brain tumor model intravenously and intracerebrally. Int J Radiat Oncol Biol Phys. 1979 Sep;5(9):1527–1529. doi: 10.1016/0360-3016(79)90764-8
  • Linnert M, Gehl J. Bleomycin treatment of brain tumors: an evaluation. Anticancer Drugs. 2009 Mar;20(3):157–164. doi: 10.1097/CAD.0b013e328325465e
  • Steighner RJ, Povirk LF. Bleomycin-induced DNA lesions at mutational hot spots: implications for the mechanism of double-strand cleavage. Proc Natl Acad Sci USA. 1990;87(21):8350–8354. doi: 10.1073/pnas.87.21.8350
  • Bolzán AD, Bianchi MS. DNA and chromosome damage induced by bleomycin in mammalian cells: an update. Mutat Res Rev Mutat Res. 2018;775:51–62. doi: 10.1016/j.mrrev.2018.02.003
  • Cabrera S, Maciel M, Herrera I, et al. Essential role for the ATG4B protease and autophagy in bleomycin-induced pulmonary fibrosis. Autophagy. 2015;11(4):670–684. doi: 10.1080/15548627.2015.1034409
  • Sai X, Qin C, Wu Y, et al. Downregulation of PTEN mediates bleomycin-induced premature senescence in lung cancer cells by suppressing autophagy. J Int Med Res. 2020;48(5):300060520923522. doi: 10.1177/0300060520923522
  • Gui Y-S, Wang L, Tian X, et al. mTOR overactivation and compromised autophagy in the pathogenesis of pulmonary fibrosis. PLOS ONE. 2015;10(9):e0138625. doi: 10.1371/journal.pone.0138625
  • Zhang X, Mao Y, Peng W, et al. Autophagy-related protein EI24 delays the development of pulmonary fibrosis by promoting autophagy. Life Sci. 2021;264:118664. doi: 10.1016/j.lfs.2020.118664
  • Baek AR, Hong J, Song KS, et al. Spermidine attenuates bleomycin-induced lung fibrosis by inducing autophagy and inhibiting endoplasmic reticulum stress (ERS)-induced cell death in mice. Exp Mol Med. 2020;52(12):2034–2045. doi: 10.1038/s12276-020-00545-z
  • Zhou J, Li X-Y, Liu Y-J, et al. Full-coverage regulations of autophagy by ROS: from induction to maturation. Autophagy. 2022;18(6):1240–1255. doi: 10.1080/15548627.2021.1984656
  • Wang H, Wang N, Xu D, et al. Oxidation of multiple MiT/TFE transcription factors links oxidative stress to transcriptional control of autophagy and lysosome biogenesis. Autophagy. 2020;16(9):1683–1696. doi: 10.1080/15548627.2019.1704104
  • Zhang X, Cheng X, Yu L, et al. MCOLN1 is a ROS sensor in lysosomes that regulates autophagy. Nat Commun. 2016;7(1):12109. doi: 10.1038/ncomms12109
  • Wan X, Dennis AT, Obejero-Paz C, et al. Oxidative inactivation of the lipid phosphatase phosphatase and tensin homolog on chromosome ten (PTEN) as a novel mechanism of acquired long QT syndrome. J Biol Chem. 2011;286(4):2843–2852. doi: 10.1074/jbc.M110.125526
  • Alexander A, Cai S-L, Kim J, et al. ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc Natl Acad Sci USA. 2010;107(9):4153–4158. doi: 10.1073/pnas.0913860107
  • Scherz-Shouval R, Shvets E, Fass E, et al. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. Embo J. 2007;26(7):1749–1760. doi: 10.1038/sj.emboj.7601623
  • Frudd K, Burgoyne T, Burgoyne JR. Oxidation of Atg3 and Atg7 mediates inhibition of autophagy. Nat Commun. 2018;9(1):95. doi: 10.1038/s41467-017-02352-z
  • Shen Y, Zhang B, Su Y, et al. Iron promotes dihydroartemisinin cytotoxicity via ROS production and blockade of autophagic Flux via Lysosomal Damage in Osteosarcoma. Front Pharmacol. 2020;11:444. doi: 10.3389/fphar.2020.00444
  • Huang W, Hickson LJ, Eirin A, et al. Cellular senescence: the good, the bad and the unknown. Nat Rev Nephrol. 2022;18(10):611–627. doi: 10.1038/s41581-022-00601-z
  • Hao X, Shiromoto Y, Sakurai M, et al. ADAR1 downregulation by autophagy drives senescence independently of RNA editing by enhancing p16INK4a levels. Nat Cell Biol. 2022;24(8):1202–1210. doi: 10.1038/s41556-022-00959-z
  • Carosi JM, Fourrier C, Bensalem J, et al. The mTOR–lysosome axis at the centre of ageing. FEBS Open Bio. 2022;12(4):739–757. doi: 10.1002/2211-5463.13347
  • Zhang W, Bai J, Hang K, et al. Role of lysosomal acidification dysfunction in mesenchymal stem cell senescence. Front Cell Dev Biol. 2022;10:817877. doi: 10.3389/fcell.2022.817877
  • Colacurcio DJ, Nixon RA. Disorders of lysosomal acidification-the emerging role of v-ATPase in aging and neurodegenerative disease. Ageing Res Rev. 2016;32:75–88. doi: 10.1016/j.arr.2016.05.004
  • López-Otín C, Blasco MA, Partridge L, et al. Hallmarks of aging: an expanding universe. Cell. 2023;186(2):243–278. doi: 10.1016/j.cell.2022.11.001
  • Narita M, Young ARJ, Arakawa S, et al. Spatial coupling of mTOR and autophagy augments secretory phenotypes. Science. 2011;332(6032):966–970. doi: 10.1126/science.1205407
  • Lee BY, Han JA, Im JS, et al. Senescence-associated β-galactosidase is lysosomal β-galactosidase. Aging Cell. 2006;5(2):187–195. doi: 10.1111/j.1474-9726.2006.00199.x
  • Farífarías GG, Guardia CM, De Pace R, et al. Borc/kinesin-1 ensemble drives polarized transport of lysosomes into the axon. Proc Natl Acad Sci USA. 2017;114(14):E2955–E2964. doi: 10.1073/pnas.1616363114
  • Labun K, Montague TG, Krause M, et al. CHOPCHOP v3: expanding the CRISPR web toolbox beyond genome editing. Nucleic Acids Res. 2019;47(W1):W171–W174. doi: 10.1093/nar/gkz365

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.