CoChat
Sign Up
Cited by 30

The DOI matches its Crossref record; 26 of the 26 references it cites were found in a registry or an index.

Monitoring autophagy in cancer: From bench to bedside

Long, Maeve, McWilliams, Thomas G.·2020·Seminars in Cancer Biology
DOI 10.1016/j.semcancer.2019.05.016
Open this paper in CoChat — free account

Abstract

Autophagy refers to an essential mechanism that evolved to sustain eukaryotic homeostasis and metabolism during instances of nutrient deprivation. During autophagy, intracellular cargo is encapsulated and delivered to the lysosome for elimination. Loss of basal autophagy in vivo negatively impacts cellular proteostasis, metabolism and tissue integrity. Accordingly, many drug development strategies are focused on modulating autophagic capacity in various pathophysiological states, from cancer to neurodegenerative disease. The role of autophagy in cancer is particularly complicated, as either augmenting or attenuating this process can have variable outcomes on cellular survival, proliferation and transformation. This complexity is compounded by the emergence of several selective autophagy pathways, which act to eliminate damaged or superfluous cellular components in a targeted fashion. The advent of sensitive tools to monitor autophagy pathways in vivo holds promise to clarify their importance in cancer pathophysiology. In this review, we provide an overview of autophagy in cancer biology and outline how the development of tools to study autophagy in vivo could enhance our understanding of its function for translational benefit.

Overview

Integrity signals

Registry

Crossref · 10.1016/j.semcancer.2019.05.016

Cites

26 of 26 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Show all 26 references

Research works printed but not linked: 114

  1. Ktistakis, 2017, In praise of M. Anselmier who first used the term “autophagie” in 1859, Autophagy., 10.1080/15548627.2017.1367473 · DOI
  2. Mizushima, 2018, A brief history of autophagy from cell biology to physiology and disease, Nat. Cell Biol., 10.1038/s41556-018-0092-5 · DOI · Paper page
  3. Hanahan, 2011, Hallmarks of cancer: the next generation, Cell., 144, 646, 10.1016/j.cell.2011.02.013 · DOI · Paper page
  4. Mizushima, 2017, The exponential growth of autophagy-related research: from the humble yeast to the Nobel Prize, FEBS Lett., 10.1002/1873-3468.12594 · DOI
  5. Laplante, 2012, MTOR signaling in growth control and disease, Cell., 10.1016/j.cell.2012.03.017 · DOI · Paper page
  6. Mejlvang, 2018, Starvation induces rapid degradation of selective autophagy receptors by endosomal microautophagy, J. Cell Biol., 10.1083/jcb.201711002 · DOI
  7. Lin, 2012, GSK3-TIP60-ULK1 signaling pathway links growth factor deprivation to autophagy, Science., 10.1126/science.1217032 · DOI · Paper page
  8. Xie, 2007, Autophagosome formation: core machinery and adaptations, Nat. Cell Biol., 10.1038/ncb1007-1102 · DOI
  9. Bissa, 2018, Autophagosome formation: cutting the gordian knot at the ER, Curr. Biol., 10.1016/j.cub.2018.03.015 · DOI
  10. Ge, 2013, The ER–Golgi intermediate compartment is a key membrane source for the LC3 lipidation step of autophagosome biogenesis, Elife., 10.7554/eLife.00947.028 · DOI
  11. Hailey, 2010, Mitochondria supply membranes for autophagosome biogenesis during starvation, Cell., 10.1016/j.cell.2010.04.009 · DOI
  12. Valverde, 2019, ATG2 transports lipids to promote autophagosome biogenesis, J. Cell Biol. jcb, 10.1083/jcb.201811139 · DOI
  13. Zhou, 2019, Rab5-dependent autophagosome closure by ESCRT, J. Cell Biol., 10.1083/jcb.201811173 · DOI
  14. Shima, 2019, COPII vesicles contribute to autophagosomal membranes, J. Cell Biol., 10.1083/jcb.201809032 · DOI
  15. Biazik, 2015, The versatile electron microscope: an ultrastructural overview of autophagy, Methods., 10.1016/j.ymeth.2014.11.013 · DOI
  16. Ganley, 2013, Autophagosome maturation and lysosomal fusion, Essays Biochem.
  17. Klionsky, 2014, Autophagosomes, phagosomes, autolysosomes, phagolysosomes, autophagolysosomes… Wait, I’m confused, Autophagy., 10.4161/auto.28448 · DOI
  18. Matsui, 2018, Autophagosomal YKT6 is required for fusion with lysosomes independently of syntaxin 17, J. Cell Biol., 10.1083/jcb.201712058 · DOI · Paper page
  19. Itakura, 2012, The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes, Cell., 10.1016/j.cell.2012.11.001 · DOI
  20. Lim, 2016, The lysosome as a command-and-control center for cellular metabolism, J. Cell Biol., 10.1083/jcb.201607005 · DOI
  21. Chen, 2013, Autophagic lysosome reformation, Exp. Cell Res., 10.1016/j.yexcr.2012.09.004 · DOI
  22. Munson, 2015, mTOR activates the VPS34-UVRAG complex to regulate autolysosomal tubulation and cell survival, EMBO J., 10.15252/embj.201590992 · DOI
  23. Nishida, 2016, Erratum: corrigendum: discovery of Atg5/Atg7-independent alternative macroautophagy, Nature., 533, 10.1038/nature16538 · DOI
  24. Ra, 2016, TRIM31 promotes Atg5/Atg7-independent autophagy in intestinal cells, Nat. Commun., 7, 11726, 10.1038/ncomms11726 · DOI
  25. Okamoto, 2014, Organellophagy: eliminating cellular building blocks via selective autophagy, J. Cell Biol., 10.1083/jcb.201402054 · DOI
  26. Khaminets, 2016, Ubiquitin-dependent and independent signals in selective autophagy, Trends Cell Biol., 10.1016/j.tcb.2015.08.010 · DOI
  27. Marcassa, 2018, Dual role of USP30 in controlling basal pexophagy and mitophagy, EMBO Rep., 10.15252/embr.201745595 · DOI · Paper page
  28. Rogov, 2014, Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy, Mol. Cell, 10.1016/j.molcel.2013.12.014 · DOI · Paper page
  29. Galluzzi, 2017, Molecular definitions of autophagy and related processes, EMBO J., 10.15252/embj.201796697 · DOI · Paper page
  30. Kaushik, 2018, The coming of age of chaperone-mediated autophagy, Nat. Rev. Mol. Cell Biol., 10.1038/s41580-018-0001-6 · DOI · Paper page
  31. Kaushik, 2012, Chaperone-mediated autophagy: a unique way to enter the lysosome world, Trends Cell Biol., 10.1016/j.tcb.2012.05.006 · DOI
  32. Amaravadi, 2016, Recent insights into the function of autophagy in cancer, Genes Dev., 10.1101/gad.287524.116 · DOI
  33. Mathew, 2009, Autophagy suppresses tumorigenesis through elimination of p62, Cell., 10.1016/j.cell.2009.03.048 · DOI
  34. Jiang, 2014, Autophagy and human diseases, Cell Res., 10.1038/cr.2013.161 · DOI
  35. Liang, 1999, Induction of autophagy and inhibition of tumorigenesis by beclin 1, Nature., 10.1038/45257 · DOI · Paper page
  36. Yue, 2003, Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor, Proc. Natl. Acad. Sci., 10.1073/pnas.2436255100 · DOI · Paper page
  37. Qu, 2003, Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene, J. Clin. Invest., 10.1172/JCI20039 · DOI · Paper page
  38. White, 2015, CCR focus autophagy, metabolism, and Cancer, Clin. Cancer Res., 10.1158/1078-0432.CCR-15-0490 · DOI
  39. Pattingre, 2005, Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy, Cell., 10.1016/j.cell.2005.07.002 · DOI · Paper page
  40. Fernández, 2018, Disruption of the beclin 1-BCL2 autophagy regulatory complex promotes longevity in mice, Nature., 10.1038/s41586-018-0162-7 · DOI · Paper page
  41. Liang, 2006, Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG, Nat. Cell Biol., 10.1038/ncb1426 · DOI · Paper page
  42. Nassour, 2019, Autophagic cell death restricts chromosomal instability during replicative crisis, Nature., 10.1038/s41586-019-0885-0 · DOI · Paper page
  43. Rosenfeldt, 2013, P53 status determines the role of autophagy in pancreatic tumour development, Nature., 10.1038/nature12865 · DOI · Paper page
  44. Wei, 2014, p62/SQSTM1 synergizes with autophagy for tumor growth in vivo, Genes Dev., 10.1101/gad.237354.113 · DOI
  45. Rosenfeldt, 2017, PTEN deficiency permits the formation of pancreatic cancer in the absence of autophagy, Cell Death Differ., 10.1038/cdd.2016.120 · DOI
  46. Mainz, 2018, Autophagy and cancer – insights from mouse models, FEBS J., 10.1111/febs.14274 · DOI
  47. Bryant, 2019, Combination of ERK and autophagy inhibition as a treatment approach for pancreatic cancer, Nat. Med., 10.1038/s41591-019-0368-8 · DOI · Paper page
  48. Kinsey, 2019, Publisher Correction: protective autophagy elicited by RAF→MEK→ERK inhibition suggests a treatment strategy for RAS-driven cancers, Nat. Med., 25
  49. Kauffman, 2014, Molecular genetics and cellular features of TFE3 and TFEB fusion kidney cancers, Nat. Rev. Urol., 10.1038/nrurol.2014.162 · DOI
  50. Perera, 2018, MiT/TFE family of transcription factors, lysosomes, and Cancer, Annu. Rev. Cancer Biol.
  51. Briceño, 2003, Therapy of glioblastoma multiforme improved by the antimutagenic chloroquine, Neurosurg. Focus, 10.3171/foc.2003.14.2.4 · DOI
  52. Briceño, 2007, Institutional experience with chloroquine as an adjuvant to the therapy for glioblastoma multiforme, Surg. Neurol., 10.1016/j.surneu.2006.08.080 · DOI
  53. Sotelo, 2006, Adding chloroquine to conventional treatment for glioblastoma multiforme: a randomized, double-blind, placebo-controlled trial, Ann. Intern. Med., 10.7326/0003-4819-144-5-200603070-00008 · DOI
  54. Rangwala, 2014, Phase I trial of hydroxychloroquine with dose-intense temozolomide in patients with advanced solid tumors and melanoma, Autophagy.
  55. Rangwala, 2014, Combined MTOR and autophagy inhibition: phase I trial of hydroxychloroquine and temsirolimus in patients with advanced solid tumors and melanoma, Autophagy.
  56. Rosenfeld, 2014, A phase I/II trial of hydroxychloroquine in conjunction with radiation therapy and concurrent and adjuvant temozolomide in patients with newly diagnosed glioblastoma multiforme, Autophagy., 10, 1359, 10.4161/auto.28984 · DOI
  57. Goldberg, 2012, A phase i study of erlotinib and hydroxychloroquine in advanced non-small-cell lung cancer, J. Thorac. Oncol., 10.1097/JTO.0b013e318262de4a · DOI
  58. Mahalingam, 2014, Combined autophagy and HDAC inhibition: a phase I safety, tolerability, pharmacokinetic, and pharmacodynamic analysis of hydroxychloroquine in combination with the HDAC inhibitor vorinostat in patients with advanced solid tumors, Autophagy., 10.4161/auto.29231 · DOI
  59. Maycotte, 2012, Chloroquine sensitizes breast cancer cells to chemotherapy independent of autophagy, Autophagy., 10.4161/auto.8.2.18554 · DOI
  60. Jacquin, 2017, Pharmacological modulators of autophagy activate a parallel noncanonical pathway driving unconventional LC3 lipidation, Autophagy., 10.1080/15548627.2017.1287653 · DOI
  61. Limpert, 2018, Autophagy in Cancer: regulation by small molecules, Trends Pharmacol. Sci., 39, 1021, 10.1016/j.tips.2018.10.004 · DOI
  62. Maycotte, 2014, STAT3-Mediated autophagy dependence identifies subtypes of breast cancer where autophagy inhibition can be efficacious, Cancer Res., 10.1158/0008-5472.CAN-13-3470 · DOI
  63. Ma, 2014, Targeting ER stress-induced autophagy overcomes BRAF inhibitor resistance in melanoma, J. Clin. Invest., 10.1172/JCI70454 · DOI · Paper page
  64. Wang, 2017, Targeting autophagy sensitizes BRAF-mutant thyroid cancer to vemurafenib, J. Clin. Endocrinol. Metab., 10.1210/jc.2016-1999 · DOI
  65. Levy, 2017, Autophagy inhibition overcomes multiple mechanisms of resistance to BRAF inhibition in brain tumors, Elife.
  66. Vera-Ramirez, 2018, Autophagy promotes the survival of dormant breast cancer cells and metastatic tumour recurrence, Nat. Commun., 10.1038/s41467-018-04070-6 · DOI
  67. Pagotto, 2017, Autophagy inhibition reduces chemoresistance and tumorigenic potential of human ovarian cancer stem cells, Cell Death Dis., 10.1038/cddis.2017.327 · DOI · Paper page
  68. Ragusa, 2014, PROX1 promotes metabolic adaptation and fuels outgrowth of Wnt high metastatic colon cancer cells, Cell Rep., 10.1016/j.celrep.2014.08.041 · DOI
  69. Kon, 2011, Chaperone-mediated autophagy is required for tumor growth, Sci. Transl. Med., 10.1126/scitranslmed.3003182 · DOI
  70. Thorburn, 2011, Targeting chaperone-mediated autophagy in cancer, Sci. Transl. Med., 10.1126/scitranslmed.3003390 · DOI
  71. Karsli-Uzunbas, 2014, Autophagy is required for glucose homeostasis and lung tumor maintenance, Cancer Discov., 10.1158/2159-8290.CD-14-0363 · DOI · Paper page
  72. Towers, 2016, Therapeutic targeting of autophagy, EBioMedicine., 10.1016/j.ebiom.2016.10.034 · DOI
  73. Madeo, 2014, Caloric restriction mimetics: towards a molecular definition, Nat. Rev. Drug Discov., 10.1038/nrd4391 · DOI · Paper page
  74. Lee, 2012, Fasting cycles retard growth of tumors and sensitize a range of cancer cell types to chemotherapy, Sci. Transl. Med., 10.1126/scitranslmed.3003293 · DOI
  75. Cuyàs, 2019, Metformin induces a fasting- and antifolate-mimicking modification of systemic host metabolism in breast cancer patients, Aging (Albany. NY)., 10.18632/aging.101960 · DOI
  76. Wheaton, 2014, Metformin inhibits mitochondrial complex I of cancer cells to reduce tumorigenesis, Elife., 10.7554/eLife.02242.019 · DOI
  77. Poillet-Perez, 2019, Role of tumor and host autophagy in cancer metabolism, Genes Dev., 33, 610, 10.1101/gad.325514.119 · DOI
  78. Poillet-Perez, 2018, Autophagy maintains tumour growth through circulating arginine, Nature., 10.1038/s41586-018-0697-7 · DOI
  79. Caccialanza, 2019, Fasting in oncology: a word of caution, Nat. Rev. Cancer, 10.1038/s41568-018-0098-0 · DOI
  80. Nencioni, 2019, Reply to ‘Fasting in oncology: a word of caution.’, Nat. Rev. Cancer, 10.1038/s41568-018-0100-x · DOI
  81. McWilliams, 2019, Vol. 1880, 621
  82. Mizushima, 2004, In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker, Mol. Biol. Cell, 15, 1101, 10.1091/mbc.e03-09-0704 · DOI · Paper page
  83. Komatsu, 2006, Loss of autophagy in the central nervous system causes neurodegeneration in mice, Nature., 10.1038/nature04723 · DOI · Paper page
  84. McWilliams, 2018, Phosphorylation of Parkin at serine 65 is essential for its activation in vivo, Open Biol., 10.1098/rsob.180108 · DOI
  85. Kimura, 2007, Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3, Autophagy., 10.4161/auto.4451 · DOI · Paper page
  86. Kaizuka, 2016, An autophagic flux probe that releases an internal control, Mol. Cell, 10.1016/j.molcel.2016.09.037 · DOI
  87. Palikaras, 2018, Mechanisms of mitophagy in cellular homeostasis, physiology and pathology, Nat. Cell Biol., 10.1038/s41556-018-0176-2 · DOI
  88. Rodger, 2018, Mammalian mitophagy – from in vitro molecules to in vivo models, FEBS J., 10.1111/febs.14336 · DOI
  89. Scott, 1998, Delivery of proteins and organelles to the vacuole from the cytoplasm, Curr. Opin. Cell Biol., 10.1016/S0955-0674(98)80068-9 · DOI
  90. Lemasters, 2005, Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging, Rejuvenation Res., 8, 3, 10.1089/rej.2005.8.3 · DOI
  91. Lewis, 1915, Mitochondria (and other cytoplasmic structures) in tissue cultures, Am. J. Anat., 10.1002/aja.1000170304 · DOI
  92. Clark, 1957, Cellular differentiation in the kidneys of newborn mice studied with the electron microscope, J. Biophys. Biochem. Cytol., 10.1083/jcb.3.3.349 · DOI
  93. Novikoff, 1962, Cytolysomes and mitochondrial degeneration, J. Cell Biol., 10.1083/jcb.15.1.140 · DOI
  94. Fletcher, 1961, Turnover of rat-liver mitochondria, BBA - Biochim. Biophys. Acta., 10.1016/0006-3002(61)90177-9 · DOI
  95. Narendra, 2008, Parkin is recruited selectively to impaired mitochondria and promotes their autophagy, J. Cell Biol., 10.1083/jcb.200809125 · DOI · Paper page
  96. McWilliams, 2017, PINK1 and Parkin: emerging themes in mitochondrial homeostasis, Curr. Opin. Cell Biol., 10.1016/j.ceb.2017.03.013 · DOI
  97. McWilliams, 2016, Mito-QC illuminates mitophagy and mitochondrial architecture in vivo, J. Cell Biol., 10.1083/jcb.201603039 · DOI
  98. Sun, 2015, Measuring in vivo mitophagy, Mol. Cell, 10.1016/j.molcel.2015.10.009 · DOI
  99. McWilliams, 2018, Basal mitophagy occurs independently of PINK1 in mouse tissues of high metabolic demand, Cell Metab., 10.1016/j.cmet.2017.12.008 · DOI · Paper page
  100. Yamada, 2018, Mitochondrial stasis reveals p62-Mediated ubiquitination in parkin-independent mitophagy and mitigates nonalcoholic fatty liver disease, Cell Metab., 10.1016/j.cmet.2018.06.014 · DOI
  101. Soutar, 2019, FBS/BSA media concentration determines CCCP’s ability to depolarize mitochondria and activate PINK1-PRKN mitophagy, Autophagy., 10.1080/15548627.2019.1603549 · DOI
  102. Voorde, 2019, Improving the metabolic fidelity of cancer models with a physiological cell culture medium, Sci. Adv.
  103. Bernardini, 2017, Parkin and mitophagy in cancer, Oncogene., 10.1038/onc.2016.302 · DOI
  104. Veeriah, 2010, Somatic mutations of the Parkinson’s disease-associated gene PARK2 in glioblastoma and other human malignancies, Nat. Genet., 10.1038/ng.491 · DOI
  105. Gong, 2014, Pan-cancer genetic analysis identifies PARK2 as a master regulator of G1/S cyclins, Nat. Genet., 10.1038/ng.2981 · DOI
  106. Zhang, 2011, Parkin, a p53 target gene, mediates the role of p53 in glucose metabolism and the Warburg effect, Proc. Natl. Acad. Sci.
  107. Villa, 2017, Parkin-independent mitophagy controls chemotherapeutic response in Cancer cells, Cell Rep., 10.1016/j.celrep.2017.08.087 · DOI
  108. Doménech, 2015, AMPK and PFKFB3 mediate glycolysis and survival in response to mitophagy during mitotic arrest, Nat. Cell Biol., 10.1038/ncb3231 · DOI
  109. Matheoud, 2019, Intestinal infection triggers Parkinson’s disease-like symptoms in Pink1-/- mice, Nature, 10.1038/s41586-019-1405-y · DOI · Paper page
  110. Bajaj, 2010, Parkinson’s disease and cancer risk: a systematic review and meta-analysis, Cancer Causes Control
  111. Bose, 2018, Parkinson’s disease and melanoma: co-occurrence and mechanisms, J. Parkinsons Dis., 8, 385, 10.3233/JPD-171263 · DOI
  112. Ascherio, 2016, The epidemiology of Parkinson’s disease: risk factors and prevention, Lancet Neurol., 15, 1257, 10.1016/S1474-4422(16)30230-7 · DOI
  113. Andreux, 2019, The mitophagy activator urolithin A is safe and induces a molecular signature of improved mitochondrial and cellular health in humans, Nat. Metab., 1, 595, 10.1038/s42255-019-0073-4 · DOI · Paper page
  114. Ryu, 2016, Urolithin A induces mitophagy and prolongs lifespan in C. Elegans and increases muscle function in rodents, Nat. Med., 10.1038/nm.4132 · DOI · Paper page

Cited by

Sorted by citations

Metadata

Authors
Long, M., & McWilliams, T. G.
Venue
Seminars in Cancer Biology
Publisher
Elsevier BV
Published
2020-11
Volume
66
Pages
12-21
ISSN
1044-579X
DOI
10.1016/j.semcancer.2019.05.016
Cited by
30
References
26
Language
en
Licence
Funders
  • Sigrid Juséliuksen Säätiö
  • Novo Nordisk Fonden
  • Helsingin Yliopisto
  • Academy of Finland

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review