Home LiteratureArticle Details
PMID: 25497060 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Selective autophagy: xenophagy.

Methods (San Diego, Calif.) ·Vol. 75 ·2015-03-00 ·Pages 120-7

Bauckman KA, Owusu-Boaitey N, Mysorekar IU

Abstract

Xenophagy is an autophagic phenomenon that specifically involves pathogens and other non-host entities. Although the understanding of the relationship between autophagosomes and invading organisms has grown significantly in the past decade, the exact steps to confirm xenophagy has been not been thoroughly defined. Here we describe a methodical approach to confirming autophagy, its interaction with bacterial invasion, as well as the specific type of autophagic formation (i.e. autophagosome, autolysosome, phagolysosome). Further, we argue that xenophagy is not limited to pathogen interaction with autophagosome, but also non-microbial entities such as iron.

Keywords
Ferritinophagy Infection Inflammasome LC3 Associated Phagocytosis Symbiophagy UPEC
MeSH Terms
Autophagy/genetics Brucella/genetics,pathogenicity Host-Pathogen Interactions/genetics Humans Infections/genetics,microbiology Lysosomes/metabolism Molecular Biology/methods Phagosomes/genetics,microbiology,pathology
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Bauckman Kyle A
Department of Obstetrics and Gynecology, Washington University School of Medicine, St. Louis, MO, USA.
Owusu-Boaitey Nana
Department of Obstetrics and Gynecology, Washington University School of Medicine, St. Louis, MO, USA.
Mysorekar Indira U
Department of Obstetrics and Gynecology, Washington University School of Medicine, St. Louis, MO, USA; Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA. Electronic address: indira@wustl.edu.
References (110)
110 references, click to expand
  1. Bacterial autophagy: the trigger, the target and the timing.
    Autophagy. 2012 Dec;8(12):1848-50 PMID: 22932645
  2. The effect of transforming growth factor β1 on the crosstalk between autophagy and apoptosis in the annulus fibrosus cells under serum deprivation.
    Cytokine. 2014 Dec;70(2):87-96 PMID: 25127907
  3. The role of lysosomes in iron metabolism and recycling.
    Int J Biochem Cell Biol. 2011 Dec;43(12):1686-97 PMID: 21907822
  4. Arsenic trioxide induces a beclin-1-independent autophagic pathway via modulation of SnoN/SkiL expression in ovarian carcinoma cells.
    Cell Death Differ. 2010 Dec;17(12):1867-81 PMID: 20508647
  5. Minocycline inhibits the growth of glioma by inducing autophagy.
    Autophagy. 2011 Feb;7(2):166-75 PMID: 21079420
  6. A current perspective of autophagosome biogenesis.
    Cell Res. 2014 Jan;24(1):58-68 PMID: 24296784
  7. Xenophagy.
    Br Dent J. 1981 Mar 3;150(5):136 PMID: 6937205
  8. Quantitative analysis of protein co-localization on B cells opsonized with rituximab and complement using the ImageStream multispectral imaging flow cytometer.
    J Immunol Methods. 2006 Dec 20;317(1-2):90-9 PMID: 17067631
  9. Autophagy variation within a cell population determines cell fate through selective degradation of Fap-1.
    Nat Cell Biol. 2014 Jan;16(1):47-54 PMID: 24316673
  10. Subversion of autophagy in adherent invasive Escherichia coli-infected neutrophils induces inflammation and cell death.
    PLoS One. 2012;7(12):e51727 PMID: 23272151
  11. Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy.
    Mol Cell. 2014 Jan 23;53(2):167-78 PMID: 24462201
  12. A novel image-based cytometry method for autophagy detection in living cells.
    Autophagy. 2012 Sep;8(9):1371-82 PMID: 22895056
  13. Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway.
    Cell. 2012 Aug 17;150(4):803-15 PMID: 22901810
  14. Self and nonself: how autophagy targets mitochondria and bacteria.
    Cell Host Microbe. 2014 Apr 9;15(4):403-11 PMID: 24721569
  15. Atg16l1 is required for autophagy in intestinal epithelial cells and protection of mice from Salmonella infection.
    Gastroenterology. 2013 Dec;145(6):1347-57 PMID: 23973919
  16. Toll-like receptor 4 is a sensor for autophagy associated with innate immunity.
    Immunity. 2007 Jul;27(1):135-44 PMID: 17658277
  17. Eating the strangers within: host control of intracellular bacteria via xenophagy.
    Cell Microbiol. 2011 Sep;13(9):1319-27 PMID: 21740500
  18. Azithromycin blocks autophagy and may predispose cystic fibrosis patients to mycobacterial infection.
    J Clin Invest. 2011 Sep;121(9):3554-63 PMID: 21804191
  19. Identifying specific receptors for cargo-mediated autophagy.
    Cell Res. 2014 Jul;24(7):783-4 PMID: 24797431
  20. Bacterial interactions with the autophagic pathway.
    Cell Microbiol. 2002 Jan;4(1):1-10 PMID: 11856168
  21. Iron modulates cell survival in a Ras- and MAPK-dependent manner in ovarian cells.
    Cell Death Dis. 2013;4:e592 PMID: 23598404
  22. Autophagy as a defence against intracellular pathogens.
    Essays Biochem. 2013;55:153-63 PMID: 24070478
  23. Autophagy in antimicrobial immunity.
    Mol Cell. 2014 Apr 24;54(2):224-33 PMID: 24766886
  24. Molecular basis of canonical and bactericidal autophagy.
    Int Immunol. 2009 Nov;21(11):1199-204 PMID: 19737785
  25. Autophagy stimulation by rapamycin suppresses lung inflammation and infection by Burkholderia cenocepacia in a model of cystic fibrosis.
    Autophagy. 2011 Nov;7(11):1359-70 PMID: 21997369
  26. Atg16L1 T300A variant decreases selective autophagy resulting in altered cytokine signaling and decreased antibacterial defense.
    Proc Natl Acad Sci U S A. 2014 May 27;111(21):7741-6 PMID: 24821797
  27. EGCG stimulates autophagy and reduces cytoplasmic HMGB1 levels in endotoxin-stimulated macrophages.
    Biochem Pharmacol. 2011 May 1;81(9):1152-63 PMID: 21371444
  28. Selective autophagy.
    Essays Biochem. 2013;55:79-92 PMID: 24070473
  29. Symbiophagy as a cellular mechanism for coral bleaching.
    Autophagy. 2009 Feb;5(2):211-6 PMID: 19066451
  30. Listeriolysin O is necessary and sufficient to induce autophagy during Listeria monocytogenes infection.
    PLoS One. 2010;5(1):e8610 PMID: 20062534
  31. Xenophagy in Helicobacter pylori- and Epstein-Barr virus-induced gastric cancer.
    J Pathol. 2014 Jun;233(2):103-12 PMID: 24633785
  32. p62/SQSTM1 is required for Parkin-induced mitochondrial clustering but not mitophagy; VDAC1 is dispensable for both.
    Autophagy. 2010 Nov;6(8):1090-106 PMID: 20890124
  33. Autophagy, ageing and apoptosis: the role of oxidative stress and lysosomal iron.
    Arch Biochem Biophys. 2007 Jun 15;462(2):220-30 PMID: 17306211
  34. The dynamics of autophagy visualized in live cells: from autophagosome formation to fusion with endo/lysosomes.
    Autophagy. 2005 Apr;1(1):23-36 PMID: 16874023
  35. NOD2 is dispensable for ATG16L1 deficiency-mediated resistance to urinary tract infection.
    Autophagy. 2014 Feb;10(2):331-8 PMID: 24384785
  36. Symbiophagy and biomineralization in the "living fossil" Astrosclera willeyana.
    Autophagy. 2014 Mar;10(3):408-15 PMID: 24343243
  37. Quantitative proteomics identifies NCOA4 as the cargo receptor mediating ferritinophagy.
    Nature. 2014 May 1;509(7498):105-9 PMID: 24695223
  38. Selective VPS34 inhibitor blocks autophagy and uncovers a role for NCOA4 in ferritin degradation and iron homeostasis in vivo.
    Nat Cell Biol. 2014 Nov;16(11):1069-79 PMID: 25327288
  39. Autophagy mediates transporter associated with antigen processing-independent presentation of viral epitopes through MHC class I pathway.
    Blood. 2012 Aug 2;120(5):994-1004 PMID: 22723550
  40. A novel method for autophagy detection in primary cells: impaired levels of macroautophagy in immunosenescent T cells.
    Autophagy. 2012 Apr;8(4):677-89 PMID: 22302009
  41. Autophagy and bacterial infectious diseases.
    Exp Mol Med. 2012 Feb 29;44(2):99-108 PMID: 22257885
  42. Etiology of Crohn's disease: many roads lead to autophagy.
    J Mol Med (Berl). 2012 Sep;90(9):987-96 PMID: 22797958
  43. The Burkholderia pseudomallei type III secretion system and BopA are required for evasion of LC3-associated phagocytosis.
    PLoS One. 2011;6(3):e17852 PMID: 21412437
  44. Autophagy as a stress-response and quality-control mechanism: implications for cell injury and human disease.
    Annu Rev Pathol. 2013 Jan 24;8:105-37 PMID: 23072311
  45. Autophagy and viruses: adversaries or allies?
    J Innate Immun. 2013;5(5):480-93 PMID: 23391695
  46. A quantitative assay for the monitoring of autophagosome accumulation in different phases of the cell cycle.
    Autophagy. 2011 Jan;7(1):83-90 PMID: 20980814
  47. IFN-γ elicits macrophage autophagy via the p38 MAPK signaling pathway.
    J Immunol. 2012 Jul 15;189(2):813-8 PMID: 22675202
  48. An IFN-γ-stimulated ATF6-C/EBP-β-signaling pathway critical for the expression of Death Associated Protein Kinase 1 and induction of autophagy.
    Proc Natl Acad Sci U S A. 2012 Jun 26;109(26):10316-21 PMID: 22699507
  49. Autophagic clearance of bacterial pathogens: molecular recognition of intracellular microorganisms.
    Front Cell Infect Microbiol. 2013;3:54 PMID: 24137567
  50. Autophagy in infection, inflammation and immunity.
    Nat Rev Immunol. 2013 Oct;13(10):722-37 PMID: 24064518
  51. ATG16L1 and pathogenesis of urinary tract infections.
    Autophagy. 2012 Nov;8(11):1693-4 PMID: 22874553
  52. A synonymous variant in IRGM alters a binding site for miR-196 and causes deregulation of IRGM-dependent xenophagy in Crohn's disease.
    Nat Genet. 2011 Mar;43(3):242-5 PMID: 21278745
  53. Autophagy regulates phagocytosis by modulating the expression of scavenger receptors.
    Immunity. 2013 Sep 19;39(3):537-47 PMID: 24035364
  54. Beta1 integrin-dependent engulfment of Yersinia enterocolitica by macrophages is coupled to the activation of autophagy and suppressed by type III protein secretion.
    J Immunol. 2009 Nov 1;183(9):5847-60 PMID: 19812190
  55. A novel quantitative flow cytometry-based assay for autophagy.
    Autophagy. 2010 Jul;6(5):634-41 PMID: 20458170
  56. Bacterial toxins can inhibit host cell autophagy through cAMP generation.
    Autophagy. 2011 Sep;7(9):957-65 PMID: 21606683
  57. The LC3 interactome at a glance.
    J Cell Sci. 2014 Jan 1;127(Pt 1):3-9 PMID: 24345374
  58. Autophagy and bacterial clearance: a not so clear picture.
    Cell Microbiol. 2013 Mar;15(3):395-402 PMID: 23121192
  59. Selective subversion of autophagy complexes facilitates completion of the Brucella intracellular cycle.
    Cell Host Microbe. 2012 Jan 19;11(1):33-45 PMID: 22264511
  60. LC3-associated phagocytosis.
    Autophagy. 2014 Mar;10(3):526-8 PMID: 24413059
  61. Mammalian iron metabolism and its control by iron regulatory proteins.
    Biochim Biophys Acta. 2012 Sep;1823(9):1468-83 PMID: 22610083
  62. Autophagy, ferritin and iron chelation.
    Autophagy. 2010 Jan;6(1):157 PMID: 20009528
  63. Analysis of autophagosome formation using lentiviral biosensors for live fluorescent cellular imaging.
    Methods Mol Biol. 2015;1219:157-69 PMID: 25308268
  64. An alteration in ATG16L1 stability in Crohn disease.
    Autophagy. 2014 Oct 1;10(10):1858-60 PMID: 25136803
  65. The autophagosome: origins unknown, biogenesis complex.
    Nat Rev Mol Cell Biol. 2013 Dec;14(12):759-74 PMID: 24201109
  66. LC3-Associated Phagocytosis (LAP): Connections with Host Autophagy.
    Cells. 2012 Jul 30;1(3):396-408 PMID: 24710482
  67. Translocation of iron from lysosomes into mitochondria is a key event during oxidative stress-induced hepatocellular injury.
    Hepatology. 2008 Nov;48(5):1644-54 PMID: 18846543
  68. Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response.
    Proc Natl Acad Sci U S A. 2009 Dec 8;106(49):20842-6 PMID: 19926846
  69. Autophagy subversion by bacteria.
    Curr Top Microbiol Immunol. 2009;335:227-50 PMID: 19802568
  70. Hepcidin and iron homeostasis.
    Biochim Biophys Acta. 2012 Sep;1823(9):1434-43 PMID: 22306005
  71. Mitochondrial calcium uniporter blocker effectively prevents brain mitochondrial dysfunction caused by iron overload.
    Life Sci. 2013 Mar 12;92(4-5):298-304 PMID: 23333832
  72. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome.
    Nat Immunol. 2011 Mar;12(3):222-30 PMID: 21151103
  73. NOD2 stimulation induces autophagy in dendritic cells influencing bacterial handling and antigen presentation.
    Nat Med. 2010 Jan;16(1):90-7 PMID: 19966812
  74. Bacterial autophagy: restriction or promotion of bacterial replication?
    Trends Cell Biol. 2012 Jun;22(6):283-91 PMID: 22555009
  75. p62: a versatile multitasker takes on cancer.
    Trends Biochem Sci. 2012 Jun;37(6):230-6 PMID: 22424619
  76. AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function.
    Genes Dev. 2011 Sep 15;25(18):1895-908 PMID: 21937710
  77. CD40 induces anti-Toxoplasma gondii activity in nonhematopoietic cells dependent on autophagy proteins.
    Infect Immun. 2013 Jun;81(6):2002-11 PMID: 23509150
  78. Autophagy in human health and disease.
    N Engl J Med. 2013 Feb 14;368(7):651-62 PMID: 23406030
  79. Regulation and function of mitophagy in development and cancer.
    Autophagy. 2013 Nov 1;9(11):1720-36 PMID: 24091872
  80. Distinguishing modes of cell death using the ImageStream multispectral imaging flow cytometer.
    Cytometry A. 2004 Jun;59(2):237-45 PMID: 15170603
  81. Guidelines for the use and interpretation of assays for monitoring autophagy.
    Autophagy. 2012 Apr;8(4):445-544 PMID: 22966490
  82. Eat-me: autophagy, phagocytosis, and reactive oxygen species signaling.
    Antioxid Redox Signal. 2013 Feb 20;18(6):677-91 PMID: 22871044
  83. The role of iron and reactive oxygen species in cell death.
    Nat Chem Biol. 2014 Jan;10(1):9-17 PMID: 24346035
  84. Peroxisomes as dynamic organelles: autophagic degradation.
    FEBS J. 2010 Aug;277(16):3289-94 PMID: 20629742
  85. Transient increase of the labile iron pool in HepG2 cells by intravenous iron preparations.
    Eur J Biochem. 2003 Sep;270(18):3731-8 PMID: 12950256
  86. Eating oneself and uninvited guests: autophagy-related pathways in cellular defense.
    Cell. 2005 Jan 28;120(2):159-62 PMID: 15680321
  87. Autophagy controls IL-1beta secretion by targeting pro-IL-1beta for degradation.
    J Biol Chem. 2011 Mar 18;286(11):9587-97 PMID: 21228274
  88. Denatured H-ferritin subunit is a major constituent of haemosiderin in the liver of patients with iron overload.
    Gut. 2002 Mar;50(3):413-9 PMID: 11839724
  89. Xenophagy in herpes simplex virus replication and pathogenesis.
    Autophagy. 2008 Jan;4(1):101-3 PMID: 18000391
  90. Autophagy protects against active tuberculosis by suppressing bacterial burden and inflammation.
    Proc Natl Acad Sci U S A. 2012 Nov 13;109(46):E3168-76 PMID: 23093667
  91. Intracellular innate resistance to bacterial pathogens.
    Cell Microbiol. 2006 Nov;8(11):1720-9 PMID: 16939532
  92. Autophagy, immunity, and microbial adaptations.
    Cell Host Microbe. 2009 Jun 18;5(6):527-49 PMID: 19527881
  93. Activation of autophagy by inflammatory signals limits IL-1β production by targeting ubiquitinated inflammasomes for destruction.
    Nat Immunol. 2012 Mar;13(3):255-63 PMID: 22286270
  94. Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry.
    Nat Immunol. 2010 Jan;11(1):55-62 PMID: 19898471
  95. Roles of autophagy in elimination of intracellular bacterial pathogens.
    Front Immunol. 2013 May 06;4:97 PMID: 23653625
  96. Does the calcein-AM method assay the total cellular 'labile iron pool' or only a fraction of it?
    Biochem J. 2007 Apr 15;403(2):261-6 PMID: 17233627
  97. A deficiency in the autophagy gene Atg16L1 enhances resistance to enteric bacterial infection.
    Cell Host Microbe. 2013 Aug 14;14(2):216-24 PMID: 23954160
  98. Host and bacterial factors that regulate LC3 recruitment to Listeria monocytogenes during the early stages of macrophage infection.
    Autophagy. 2013 Jul;9(7):985-95 PMID: 23584039
  99. Seeing is believing: the impact of electron microscopy on autophagy research.
    Autophagy. 2011 Sep;7(9):935-56 PMID: 21566462
  100. Autophagy in immunity and inflammation.
    Nature. 2011 Jan 20;469(7330):323-35 PMID: 21248839
  101. miRNA-130a targets ATG2B and DICER1 to inhibit autophagy and trigger killing of chronic lymphocytic leukemia cells.
    Cancer Res. 2012 Apr 1;72(7):1763-72 PMID: 22350415
  102. Autophagy in intracellular bacterial infection.
    Biochim Biophys Acta. 2009 Sep;1793(9):1465-77 PMID: 19303905
  103. Autophagosomes, phagosomes, autolysosomes, phagolysosomes, autophagolysosomes... wait, I'm confused.
    Autophagy. 2014 Apr;10(4):549-51 PMID: 24657946
  104. Defects in autophagy favour adherent-invasive Escherichia coli persistence within macrophages leading to increased pro-inflammatory response.
    Cell Microbiol. 2012 Jun;14(6):791-807 PMID: 22309232
  105. A review of recent methods for efficiently quantifying immunogold and other nanoparticles using TEM sections through cells, tissues and organs.
    Ann Anat. 2009 Apr;191(2):153-70 PMID: 19135344
  106. Atg16L1 deficiency confers protection from uropathogenic Escherichia coli infection in vivo.
    Proc Natl Acad Sci U S A. 2012 Jul 3;109(27):11008-13 PMID: 22715292
  107. Iron overload enhances epithelial cell proliferation in endometriotic lesions induced in a murine model.
    Hum Reprod. 2006 Nov;21(11):2810-6 PMID: 16849816
  108. Microtubule-associated protein 1 light chain 3 alpha (LC3)-associated phagocytosis is required for the efficient clearance of dead cells.
    Proc Natl Acad Sci U S A. 2011 Oct 18;108(42):17396-401 PMID: 21969579
  109. Autophagy plays an essential role in the clearance of Pseudomonas aeruginosa by alveolar macrophages.
    J Cell Sci. 2012 Jan 15;125(Pt 2):507-15 PMID: 22302984
  110. Autophagosome maturation and lysosomal fusion.
    Essays Biochem. 2013;55:65-78 PMID: 24070472
Article Info
Journal
Methods (San Diego, Calif.)
Abbr.
Methods
ISSN
1095-9130
Published
2015-03-00
Epub
2014-00-11
Pages
120-7
Language
English
Region
United States
NLM ID
9426302
PMCID
PMC4355331
Subset
IM
Grants
NIDDK NIH HHS · R01 DK100644 · United States
NIAID NIH HHS · T32 AI007172 · United States
NICHD NIH HHS · T32 HD049305 · United States
NIAID NIH HHS · T32 AI 007172-35 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com