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Scientifica
Volume 2014, Article ID 825463, 13 pages
http://dx.doi.org/10.1155/2014/825463
Review Article

Autophagy in Macrophages: Impacting Inflammation and Bacterial Infection

B-Cell Molecular Immunology Section, Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Building 10, Room 11N214, Center Drive, MSC 1876, Bethesda, MD 20892, USA

Received 15 January 2014; Accepted 28 February 2014; Published 9 April 2014

Academic Editor: Patrick Auberger

Copyright © 2014 Ali Vural and John H. Kehrl. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Z. Yang and D. J. Klionsky, “Mammalian autophagy: core molecular machinery and signaling regulation,” Current Opinion in Cell Biology, vol. 22, no. 2, pp. 124–131, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. N. Mizushima, B. Levine, A. M. Cuervo, and D. J. Klionsky, “Autophagy fights disease through cellular self-digestion,” Nature, vol. 451, no. 7182, pp. 1069–1075, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. P. Boya, F. Reggiori, and P. Codogno, “Emerging regulation and functions of autophagy,” Nature Cell Biology, vol. 15, no. 7, pp. 713–720, 2013. View at Google Scholar
  4. C. C. Mihalache and H.-U. Simon, “Autophagy regulation in macrophages and neutrophils,” Experimental Cell Research, vol. 318, no. 11, pp. 1187–1192, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. C. Kraft, M. Peter, and K. Hofmann, “Selective autophagy: ubiquitin-mediated recognition and beyond,” Nature Cell Biology, vol. 12, no. 9, pp. 836–841, 2010. View at Publisher · View at Google Scholar
  6. B. Levine, N. Mizushima, and H. W. Virgin, “Autophagy in immunity and inflammation,” Nature, vol. 469, no. 7330, pp. 323–335, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. B. Levine and V. Deretic, “Unveiling the roles of autophagy in innate and adaptive immunity,” Nature Reviews Immunology, vol. 7, no. 10, pp. 767–777, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. J. D. Mintern and J. A. Villadangos, “Autophagy and mechanisms of effective immunity,” Frontiers in Immunology, vol. 3, article 60, 2012. View at Google Scholar
  9. V. Deretic, T. Saitoh, and S. Akira, “Autophagy in infection, inflammation and immunity,” Nature Reviews Immunology, vol. 13, no. 10, pp. 722–737, 2013. View at Google Scholar
  10. V. Deretic, S. Jiang, and N. Dupont, “Autophagy intersections with conventional and unconventional secretion in tissue development, remodeling and inflammation,” Trends in Cell Biology, vol. 22, no. 8, pp. 397–406, 2012. View at Google Scholar
  11. C. A. Lamb, T. Yoshimori, and S. A. Tooze, “The autophagosome: origins unknown, biogenesis complex,” Nature Reviews Molecular Cell Biology, vol. 14, no. 12, pp. 759–774, 2013. View at Google Scholar
  12. B. Ravikumar, S. Sarkar, J. E. Davies et al., “Regulation of mammalian autophagy in physiology and pathophysiology,” Physiological Reviews, vol. 90, no. 4, pp. 1383–1435, 2010. View at Publisher · View at Google Scholar
  13. C. Behrends, M. E. Sowa, S. P. Gygi, and J. W. Harper, “Network organization of the human autophagy system,” Nature, vol. 466, no. 7302, pp. 68–76, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. C. Settembre, A. Fraldi, D. L. Medina, and A. Ballabio, “Signals from the lysosome: a control centre for cellular clearance and energy metabolism,” Nature Reviews. Molecular Cell Biology, vol. 14, no. 5, pp. 283–296, 2013. View at Publisher · View at Google Scholar
  15. E. Itakura, C. Kishi-Itakura, and N. Mizushima, “The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes,” Cell, vol. 151, no. 6, pp. 1256–1269, 2012. View at Google Scholar
  16. J. E. Oh and H. K. Lee, “Modulation of pathogen recognition by autophagy,” Frontiers in Immunology, vol. 3, article 44, 2012. View at Google Scholar
  17. V. Deretic, “Autophagy as an innate immunity paradigm: expanding the scope and repertoire of pattern recognition receptors,” Current Opinion in Immunology, vol. 24, no. 1, pp. 21–31, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. V. Deretic, “Autophagy: an emerging immunological paradigm,” The Journal of Immunology, vol. 189, no. 1, pp. 15–20, 2012. View at Google Scholar
  19. P. J. Murray and T. A. Wynn, “Protective and pathogenic functions of macrophage subsets,” Nature Reviews Immunology, vol. 11, no. 11, pp. 723–737, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Chow, B. D. Brown, and M. Merad, “Studying the mononuclear phagocyte system in the molecular age,” Nature Reviews Immunology, vol. 11, no. 11, pp. 788–798, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. T. Kawai and S. Akira, “The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors,” Nature Immunology, vol. 11, no. 5, pp. 373–384, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. L. Gong, R. J. Devenish, and M. Prescott, “Autophagy as a macrophage response to bacterial infection,” IUBMB Life, vol. 64, no. 9, pp. 740–747, 2012. View at Publisher · View at Google Scholar
  23. J. M. Blander and L. E. Sander, “Beyond pattern recognition: five immune checkpoints for scaling the microbial threat,” Nature Reviews Immunology, vol. 12, no. 3, pp. 215–225, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. B. Lemaitre, E. Nicolas, L. Michaut, J.-M. Reichhart, and J. A. Hoffmann, “The dorsoventral regulatory gene cassette spatzle/Toll/Cactus controls the potent antifungal response in Drosophila adults,” Cell, vol. 86, no. 6, pp. 973–983, 1996. View at Publisher · View at Google Scholar · View at Scopus
  25. R. Medzhitov, P. Preston-Hurlburt, and C. A. Janeway Jr., “A human homologue of the Drosophila toll protein signals activation of adaptive immunity,” Nature, vol. 388, no. 6640, pp. 394–397, 1997. View at Publisher · View at Google Scholar · View at Scopus
  26. R. Medzhitov, “Approaching the asymptote: 20 years later,” Immunity, vol. 30, no. 6, pp. 766–775, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. T. Kawai and S. Akira, “The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors,” Nature Immunology, vol. 11, no. 5, pp. 373–384, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Into, M. Inomata, E. Takayama, and T. Takigawa, “Autophagy in regulation of Toll-like receptor signaling,” Cellular Signalling, vol. 24, no. 6, pp. 1150–1162, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. C.-S. Shi and J. H. Kehrl, “Traf6 and A20 differentially regulate TLR4-induced autophagy by affecting the ubiquitination of Beclin 1,” Autophagy, vol. 6, no. 7, pp. 986–987, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. C.-S. Shi and J. H. Kehrl, “TRAF6 and A20 regulate lysine 63-linked ubiquitination of Beclin-1 to control TLR4-induced autophagy,” Science Signaling, vol. 3, no. 123, article ra42, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. I. Nakagawa, A. Amano, N. Mizushima et al., “Autophagy defends cells against invading group A Streptococcus,” Science, vol. 306, no. 5698, pp. 1037–1040, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. M. G. Gutierrez, S. S. Master, S. B. Singh, G. A. Taylor, M. I. Colombo, and V. Deretic, “Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages,” Cell, vol. 119, no. 6, pp. 753–766, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. Y. Xu, C. Jagannath, X.-D. Liu, A. Sharafkhaneh, K. E. Kolodziejska, and N. T. Eissa, “Toll-like receptor 4 is a sensor for autophagy associated with innate immunity,” Immunity, vol. 27, no. 1, pp. 135–144, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. C.-S. Shi and J. H. Kehrl, “MyD88 and Trif target Beclin 1 to trigger autophagy in macrophages,” The Journal of Biological Chemistry, vol. 283, no. 48, pp. 33175–33182, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. M. A. Delgado, R. A. Elmaoued, A. S. Davis, G. Kyei, and V. Deretic, “Toll-like receptors control autophagy,” The EMBO Journal, vol. 27, no. 7, pp. 1110–1121, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Shaid, C. H. Brandts, H. Serve, and I. Dikic, “Ubiquitination and selective autophagy,” Cell Death and Differentiation, vol. 20, no. 1, pp. 21–30, 2013. View at Publisher · View at Google Scholar
  37. C.-S. Shi and J. H. Kehrl, “Traf6 and A20 differentially regulate TLR4-induced autophagy by affecting the ubiquitination of Beclin 1,” Autophagy, vol. 6, no. 7, pp. 986–987, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. V. Canadien, T. Tan, R. Zilber, J. Szeto, A. J. Perrin, and J. H. Brumell, “Cutting edge: microbial products elicit formation of dendritic cell aggresome-like induced structures in macrophages,” Journal of Immunology, vol. 174, no. 5, pp. 2471–2475, 2005. View at Google Scholar · View at Scopus
  39. J. Szeto, N. A. Kaniuk, V. Canadien et al., “ALIS are stress-induced protein storage compartments for substrates of the proteasome and autophagy,” Autophagy, vol. 2, no. 3, pp. 189–199, 2006. View at Google Scholar · View at Scopus
  40. K.-I. Fujita and S. M. Srinivasula, “TLR4-mediated autophagy in macrophages is a p62-dependent type of selective autophagy of aggresome-like induced structures (ALIS),” Autophagy, vol. 7, no. 5, pp. 552–554, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. K.-I. Fujita, D. Maeda, Q. Xiao, and S. M. Srinivasula, “Nrf2-mediated induction of p62 controls Toll-like receptor-4-driven aggresome-like induced structure formation and autophagic degradation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 4, pp. 1427–1432, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. X. D. Liu, S. Ko, Y. Xu et al., “Transient aggregation of ubiquitinated proteins is a cytosolic unfolded protein response to inflammation and endoplasmic reticulum stress,” The Journal of Biological Chemistry, vol. 287, no. 23, pp. 19687–19698, 2012. View at Publisher · View at Google Scholar
  43. Y. Nishida, S. Arakawa, K. Fujitani et al., “Discovery of Atg5/Atg7-independent alternative macroautophagy,” Nature, vol. 461, no. 7264, pp. 654–658, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. Y. Zhong, A. Kinio, and M. Saleh, “Functions of NOD-like receptors in human diseases,” Frontiers in Immunology, vol. 4, article 333, 2013. View at Google Scholar
  45. D. Qi and R. W. Innes, “Recent advances in plant NLR structure, function, localization, and signaling,” Frontiers in Immunology, vol. 4, article 348, 2013. View at Google Scholar
  46. M. F. McDermott and J. Tschopp, “From inflammasomes to fevers, crystals and hypertension: how basic research explains inflammatory diseases,” Trends in Molecular Medicine, vol. 13, no. 9, pp. 381–388, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. L. H. Travassos, L. A. M. Carneiro, M. Ramjeet et al., “Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry,” Nature Immunology, vol. 11, no. 1, pp. 55–62, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. R. Cooney, J. Baker, O. Brain et al., “NOD2 stimulation induces autophagy in dendritic cells influencing bacterial handling and antigen presentation,” Nature Medicine, vol. 16, no. 1, pp. 90–97, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Strowig, J. Henao-Mejia, E. Elinav, and R. Flavell, “Inflammasomes in health and disease,” Nature, vol. 481, no. 7381, pp. 278–286, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. V. A. K. Rathinam, S. K. Vanaja, and K. A. Fitzgerald, “Regulation of inflammasome signaling,” Nature Immunology, vol. 13, no. 4, pp. 333–342, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. E. Latz, T. S. Xiao, and A. Stutz, “Activation and regulation of the inflammasomes,” Nature Reviews Immunology, vol. 13, no. 6, pp. 397–411, 2013. View at Google Scholar
  52. L. Franchi, T. Eigenbrod, R. Muñoz-Planillo, and G. Nuñez, “The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis,” Nature Immunology, vol. 10, no. 3, pp. 241–247, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. N. B. Bryan, A. Dorfleutner, Y. Rojanasakul, and C. Stehlik, “Activation of inflammasomes requires intracellular redistribution of the apoptotic speck-like protein containing a caspase recruitment domain,” Journal of Immunology, vol. 182, no. 5, pp. 3173–3182, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. T. Fernandes-Alnemri, J. Wu, J.-W. Yu et al., “The pyroptosome: a supramolecular assembly of ASC dimers mediating inflammatory cell death via caspase-1 activation,” Cell Death and Differentiation, vol. 14, no. 9, pp. 1590–1604, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. O. Groß, “Measuring the inflammasome,” Methods in Molecular Biology, vol. 844, pp. 199–222, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. T. Saitoh, N. Fujita, M. H. Jang et al., “Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1β production,” Nature, vol. 456, no. 7219, pp. 264–268, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. J. Harris, M. Hartman, C. Roche et al., “Autophagy controls IL-1beta secretion by targeting pro-IL-1beta for degradation,” The Journal of Biological Chemistry, vol. 286, no. 11, pp. 9587–9597, 2011. View at Publisher · View at Google Scholar
  58. K. Nakahira, J. A. Haspel, V. A. K. Rathinam et al., “Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome,” Nature Immunology, vol. 12, no. 3, pp. 222–230, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. C.-S. Shi, K. Shenderov, N.-N. Huang et al., “Activation of autophagy by inflammatory signals limits IL-1β production by targeting ubiquitinated inflammasomes for destruction,” Nature Immunology, vol. 13, no. 3, pp. 255–263, 2012. View at Publisher · View at Google Scholar · View at Scopus
  60. B. O. Bodemann, A. Orvedahl, T. Cheng et al., “RalB and the exocyst mediate the cellular starvation response by direct activation of autophagosome assembly,” Cell, vol. 144, no. 2, pp. 253–267, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. J.-C. Farré and S. Subramani, “Rallying the exocyst as an autophagy scaffold,” Cell, vol. 144, no. 2, pp. 172–174, 2011. View at Publisher · View at Google Scholar · View at Scopus
  62. J. M. Yuk and E. K. Jo, “Crosstalk between autophagy and inflammasomes,” Molecules and Cells, vol. 36, no. 5, pp. 393–399, 2013. View at Publisher · View at Google Scholar
  63. Y. Ma, L. Galluzzi, L. Zitvogel, and G. Kroemer, “Autophagy and cellular immune responses,” Immunity, vol. 39, no. 2, pp. 211–227, 2013. View at Google Scholar
  64. W. Nickel and C. Rabouille, “Mechanisms of regulated unconventional protein secretion,” Nature Reviews Molecular Cell Biology, vol. 10, no. 2, pp. 148–155, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. N. Dupont, S. Jiang, M. Pilli, W. Ornatowski, D. Bhattacharya, and V. Deretic, “Autophagy-based unconventional secretory pathway for extracellular delivery of IL-1β,” The EMBO Journal, vol. 30, no. 23, pp. 4701–4711, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. H. Y. Gee, S. H. Noh, B. L. Tang, K. H. Kim, and M. G. Lee, “Rescue of Δf508-CFTR trafficking via a GRASP-dependent unconventional secretion pathway,” Cell, vol. 146, no. 5, pp. 746–760, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. L. Gong, R. J. Devenish, and M. Prescott, “Autophagy as a macrophage response to bacterial infection,” IUBMB Life, vol. 64, no. 9, pp. 740–747, 2012. View at Google Scholar
  68. V. Deretic, “Autophagy as an innate immunity paradigm: expanding the scope and repertoire of pattern recognition receptors,” Current Opinion in Immunology, vol. 24, no. 1, pp. 21–31, 2012. View at Publisher · View at Google Scholar · View at Scopus
  69. S. Manley, J. A. Williams, and W. X. Ding, “Role of p62/SQSTM1 in liver physiology and pathogenesis,” Experimental Biology and Medicine, vol. 238, no. 5, pp. 525–538, 2013. View at Google Scholar
  70. M. Komatsu, S. Kageyama, and Y. Ichimura, “p62/SQSTM1/A170: physiology and pathology,” Pharmacological Research, vol. 66, no. 6, pp. 457–462, 2012. View at Google Scholar
  71. M. Ponpuak, A. S. Davis, E. A. Roberts et al., “Delivery of cytosolic components by autophagic adaptor protein p62 endows autophagosomes with unique antimicrobial properties,” Immunity, vol. 32, no. 3, pp. 329–341, 2010. View at Publisher · View at Google Scholar · View at Scopus
  72. F. Nazio, F. Strappazzon, M. Antonioli et al., “mTOR inhibits autophagy by controlling ULK1 ubiquitylation, self-association and function through AMBRA1 and TRAF6,” Nature Cell Biology, vol. 15, no. 4, pp. 406–416, 2013. View at Publisher · View at Google Scholar
  73. S. Mostowy, V. Sancho-Shimizu, M. A. Hamon et al., “p62 and NDP52 proteins target intracytosolic Shigella and Listeria to different autophagy pathways,” The Journal of Biological Chemistry, vol. 286, no. 30, pp. 26987–26995, 2011. View at Publisher · View at Google Scholar · View at Scopus
  74. Y. T. Zheng, S. Shahnazari, A. Brech, T. Lamark, T. Johansen, and J. H. Brumell, “The adaptor protein p62/SQSTM1 targets invading bacteria to the autophagy pathway,” Journal of Immunology, vol. 183, no. 9, pp. 5909–5916, 2009. View at Publisher · View at Google Scholar · View at Scopus
  75. N. Dupont, S. Lacas-Gervais, J. Bertout et al., “Shigella phagocytic vacuolar membrane remnants participate in the cellular response to pathogen invasion and are regulated by autophagy,” Cell Host & Microbe, vol. 6, no. 2, pp. 137–149, 2009. View at Publisher · View at Google Scholar · View at Scopus
  76. A. Orvedahl, S. MacPherson, R. Sumpter Jr., Z. Tallóczy, Z. Zou, and B. Levine, “Autophagy protects against Sindbis virus infection of the central nervous system,” Cell Host & Microbe, vol. 7, no. 2, pp. 115–127, 2010. View at Publisher · View at Google Scholar · View at Scopus
  77. S. Ivanov and C. R. Roy, “NDP52: the missing link between ubiquitinated bacteria and autophagy,” Nature Immunology, vol. 10, no. 11, pp. 1137–1139, 2009. View at Publisher · View at Google Scholar · View at Scopus
  78. M. Pilli, J. Arko-Mensah, M. Ponpuak et al., “TBK-1 promotes autophagy-mediated antimicrobial defense by controlling autophagosome maturation,” Immunity, vol. 37, no. 2, pp. 223–234, 2012. View at Publisher · View at Google Scholar
  79. T. L. M. Thurston, G. Ryzhakov, S. Bloor, N. von Muhlinen, and F. Randow, “The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria,” Nature Immunology, vol. 10, no. 11, pp. 1215–1221, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. P. Wild, H. Farhan, D. G. McEwan et al., “Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth,” Science, vol. 333, no. 6039, pp. 228–233, 2011. View at Publisher · View at Google Scholar · View at Scopus
  81. G. Matsumoto, K. Wada, M. Okuno, M. Kurosawa, and N. Nukina, “Serine 403 phosphorylation of p62/SQSTM1 regulates selective autophagic clearance of ubiquitinated proteins,” Molecular Cell, vol. 44, no. 2, pp. 279–289, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. B. W. Kim, S. B. Hong, J. H. Kim, H. Kwon do, and H. K. Song, “Structural basis for recognition of autophagic receptor NDP52 by the sugar receptor galectin-8,” Nature Communications, vol. 4, article 1613, 2013. View at Publisher · View at Google Scholar
  83. T. L. M. Thurston, M. P. Wandel, N. von Muhlinen, Á. Foeglein, and F. Randow, “Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion,” Nature, vol. 482, no. 7385, pp. 414–418, 2012. View at Publisher · View at Google Scholar · View at Scopus
  84. S. Li, M. P. Wandel, F. Li et al., “Sterical hindrance promotes selectivity of the autophagy cargo receptor NDP52 for the danger receptor galectin-8 in antibacterial autophagy,” Science Signaling, vol. 6, no. 261, article ra9, 2013. View at Google Scholar
  85. A. Huett, R. J. Heath, J. Begun et al., “The LRR and RING domain protein LRSAM1 is an E3 ligase crucial for ubiquitin-dependent autophagy of intracellular Salmonella Typhimurium,” Cell Host & Microbe, vol. 12, no. 6, pp. 778–790, 2012. View at Publisher · View at Google Scholar
  86. H. Sarantis and S. Grinstein, “Subversion of phagocytosis for pathogen survival,” Cell Host & Microbe, vol. 12, no. 4, pp. 419–431, 2012. View at Google Scholar
  87. E. A. Oczypok, T. D. Oury, and C. T. Chu, “It's a cell-eat-cell world: autophagy and phagocytosis,” The American Journal of Pathology, vol. 182, no. 3, pp. 612–622, 2013. View at Google Scholar
  88. M. A. Sanjuan, C. P. Dillon, S. W. G. Tait et al., “Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis,” Nature, vol. 450, no. 7173, pp. 1253–1257, 2007. View at Publisher · View at Google Scholar · View at Scopus
  89. W. Shui, L. Sheu, J. Liu et al., “Membrane proteomics of phagosomes suggests a connection to autophagy,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 44, pp. 16952–16957, 2008. View at Publisher · View at Google Scholar · View at Scopus
  90. J. Martinez, J. Almendinger, A. Oberst et al., “Microtubule-associated protein 1 light chain 3 alpha (LC3)-associated phagocytosis is required for the efficient clearance of dead cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 42, pp. 17396–17401, 2011. View at Publisher · View at Google Scholar · View at Scopus
  91. D. L. Bonilla, A. Bhattacharya, Y. Sha et al., “Autophagy regulates phagocytosis by modulating the expression of scavenger receptors,” Immunity, vol. 39, no. 3, pp. 537–547, 2013. View at Google Scholar
  92. K. Cadwell and J. A. Philips, “Autophagy meets phagocytosis,” Immunity, vol. 39, no. 3, pp. 425–427, 2013. View at Google Scholar
  93. M. Simicek, S. Lievens, M. Laga et al., “The deubiquitylase USP33 discriminates between RALB functions in autophagy and innate immune response,” Nature Cell Biology, vol. 15, no. 10, pp. 1220–1230, 2013. View at Google Scholar
  94. A. Vural, T. J. McQuiston, J. B. Blumer et al., “Normal autophagic activity in macrophages from mice lacking Gαi3, AGS3, or RGS19,” PLoS ONE, vol. 8, no. 11, Article ID e81886, 2013. View at Google Scholar