Autophagy in airway diseases: A new frontier in human asthma?

Allergy: European Journal of Allergy and Clinical Immunology

Volumn 71, Issue 1, 2016, Pages 5-14

  Zeki, A A ^a   Yeganeh, B ^b   Kenyon, N J ^a   Post, M ^b   Ghavami, S ^c  

^a Center for Comparative Respiratory Biology and Medicine   (United States)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c UNIVERSITY OF MANITOBA   (Canada)

Author keywords

asthma; autophagy; fibrosis; hypotheses; remodeling

Indexed keywords

AUTOPHAGY PROTEIN 5; ANTIASTHMATIC AGENT;

ASTHMA; AUTOPHAGY; CELL FATE; EOSINOPHIL; EXTRACELLULAR MATRIX; GENE; GENETIC ASSOCIATION; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; LUNG DISEASE; LUNG FIBROSIS; LUNG FUNCTION; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY TRACT DISEASE; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; TH2 CELL; AIRWAY REMODELING; ANIMAL; DISEASE MODEL; DRUG EFFECTS; FIBROSIS; GENETIC PREDISPOSITION; GENETICS; IMMUNITY; IMMUNOLOGY; METABOLISM; PATHOLOGY;

AIRWAY REMODELING; ANIMALS; ANTI-ASTHMATIC AGENTS; ASTHMA; AUTOPHAGY; DISEASE MODELS, ANIMAL; EXTRACELLULAR MATRIX; FIBROSIS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; IMMUNITY;

EID: 84956606320     PISSN: 01054538     EISSN: 13989995     Source Type: Journal    
DOI: 10.1111/all.12761     Document Type: Review

References (93)

1. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, et al., Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8: 445-544.
2. Yang F, Yang YP, Mao CJ, Cao BY, Cai ZL, Shi JJ, et al., Role of autophagy and proteasome degradation pathways in apoptosis of PC12 cells overexpressing human alpha-synuclein. Neurosci Lett 2009; 454: 203-208.
3. Ghavami S, Shojaei S, Yeganeh B, Ande SR, Jangamreddy JR, Mehrpour M, et al., Autophagy and apoptosis dysfunction in neurodegenerative disorders. Prog Neurobiol 2014; 112: 24-49.
4. Levine B, Klionsky DJ,. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004; 6: 463-477.
5. Levine B, Yuan J,. Autophagy in cell death: an innocent convict? J Clin Invest 2005; 115: 2679-2688.
6. Ghavami S, Sharma P, Yeganeh B, Ojo OO, Jha A, Mutawe MM, et al., Airway mesenchymal cell death by mevalonate cascade inhibition: integration of autophagy, unfolded protein response and apoptosis focusing on Bcl2 family proteins. Biochim Biophys Acta 2014; 1843: 1259-1271.
7. Morselli E, Galluzzi L, Kepp O, Vicencio JM, Criollo A, Maiuri MC, et al., Anti- and pro-tumor functions of autophagy. Biochim Biophys Acta 2009; 1793: 1524-1532.
8. Ghavami S, Gupta S, Ambrose E, Hnatowich M, Freed DH, et al., Autophagy and heart disease: implications for cardiac ischemia-reperfusion damage. Curr Mol Med 2014; 14: 616-629.
9. Klionsky DJ, Cregg JM, Dunn WA Jr, Emr SD, Sakai Y, Sandoval IV, et al., A unified nomenclature for yeast autophagy-related genes. Dev Cell 2003; 5: 539-545.
10. Huang J, Klionsky DJ,. Autophagy and human disease. Cell Cycle 2007; 6: 1837-1849.
11. Munakata M,. Airway remodeling and airway smooth muscle in asthma. Allergol Int 2006; 55: 235-243.
12. Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y,. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 2009; 10: 458-467.
13. Ghavami S, Cunnington RH, Gupta S, Yeganeh B, Filomeno KL, Freed DH, et al., Autophagy is a regulator of TGF-beta1-induced fibrogenesis in primary human atrial myofibroblasts. Cell Death Dis 2015; 6: e1696.
14. Hutchins MU, Veenhuis M, Klionsky DJ,. Peroxisome degradation in Saccharomyces cerevisiae is dependent on machinery of macroautophagy and the Cvt pathway. J Cell Sci 1999; 112: 4079-4087.
15. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, et al., The role of autophagy during the early neonatal starvation period. Nature 2004; 432: 1032-1036.
16. Komatsu M, Ueno T, Waguri S, Uchiyama Y, Kominami E, Tanaka K,. Constitutive autophagy: vital role in clearance of unfavorable proteins in neurons. Cell Death Differ 2007; 14: 887-894.
17. Yorimitsu T, Klionsky DJ,. Autophagy: molecular machinery for self-eating. Cell Death Differ 2005; 12: 1542-1552.
18. Xie Z, Klionsky DJ,. Autophagosome formation: core machinery and adaptations. Nat Cell Biol 2007; 9: 1102-1109.
19. He C, Klionsky DJ,. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43: 67-93.
20. Mizushima N, Noda T, Yoshimori T, Tanaka Y, Ishii T, George MD, et al., A protein conjugation system essential for autophagy. Nature 1998; 395: 395-398.
21. Tanida I, Tanida-Miyake E, Ueno T, Kominami E,. The human homolog of Saccharomyces cerevisiae Apg7p is a protein-activating enzyme for multiple substrates including human Apg12p, GATE-16, GABARAP, and MAP-LC3. J Biol Chem 2001; 276: 1701-1706.
22. Shintani T, Mizushima N, Ogawa Y, Matsuura A, Noda T, Ohsumi Y,. Apg10p, a novel protein-conjugating enzyme essential for autophagy in yeast. EMBO J 1999; 18: 5234-5241.
23. Mizushima N, Noda T, Ohsumi Y,. Apg16p is required for the function of the Apg12p-Apg5p conjugate in the yeast autophagy pathway. EMBO J 1999; 18: 3888-3896.
24. Mizushima N, Kuma A, Kobayashi Y, Yamamoto A, Matsubae M, Takao T, et al., Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. J Cell Sci 2003; 116: 1679-1688.
25. Kirisako T, Baba M, Ishihara N, Miyazawa K, Ohsumi M, Yoshimori T, et al., Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J Cell Biol 1999; 147: 435-446.
26. Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, et al., A ubiquitin-like system mediates protein lipidation. Nature 2000; 408: 488-492.
27. Ichimura Y, Imamura Y, Emoto K, Umeda M, Noda T, Ohsumi Y,. In vivo and in vitro reconstitution of Atg8 conjugation essential for autophagy. J Biol Chem 2004; 279: 40584-40592.
28. Yoshimori T,. Autophagy: a regulated bulk degradation process inside cells. Biochem Biophys Res Commun 2004; 313: 453-458.
29. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, et al., LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19: 5720-5728.
30. Kabeya Y, Mizushima N, Yamamoto A, Oshitani-Okamoto S, Ohsumi Y, Yoshimori T,. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci 2004; 117: 2805-2812.
31. Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K, et al., Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol 2001; 152: 657-668.
32. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y,. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 2004; 15: 1101-1111.
33. Stromhaug PE, Klionsky DJ,. Approaching the molecular mechanism of autophagy. Traffic 2001; 2: 524-531.
34. Scott SV, Nice DC 3rd, Nau JJ, Weisman LS, Kamada Y, Keizer-Gunnink I, et al., Apg13p and Vac8p are part of a complex of phosphoproteins that are required for cytoplasm to vacuole targeting. J Biol Chem 2000; 275: 25840-25849.
35. Tanaka A, Jin Y, Lee SJ, Zhang M, Kim HP, Stolz DB, et al., Hyperoxia-induced LC3B interacts with the Fas apoptotic pathway in epithelial cell death. Am J Respir Cell Mol Biol 2012; 46: 507-514.
36. Hu Y, Liu J, Wu YF, Lou J, Mao YY, Shen HH, et al., mTOR and autophagy in regulation of acute lung injury: a review and perspective. Microbes Infect 2014; 16: 727-734.
37. Crapo JD,. Morphologic changes in pulmonary oxygen toxicity. Annu Rev Physiol 1986; 48: 721-731.
38. Levine B, Kroemer G,. Autophagy in the pathogenesis of disease. Cell 2008; 132: 27-42.
39. Alavian SM, Ande SR, Coombs KM, Yeganeh B, Davoodpour P, Hashemi M, et al., Virus-triggered autophagy in viral hepatitis-possible novel strategies for drug development. J Viral Hepat 2011; 18: 821-830.
40. Levine B, Mizushima N, Virgin HW,. Autophagy in immunity and inflammation. Nature 2011; 469: 323-335.
41. Yeganeh B, Rezaei Moghadam A, Tran AT, Rahim MN, Ande SR, Hashemi M, et al., Asthma and influenza virus infection: focusing on cell death and stress pathways in influenza virus replication. Iran J Allergy Asthma Immunol 2013; 12: 1-17.
42. Yeganeh B, Ghavami S, Kroeker AL, Mahood TH, Stelmack GL, Klonisch T, et al., Suppression of influenza A virus replication in human lung epithelial cells by noncytotoxic concentrations bafilomycin A1. Am J Physiol Lung Cell Mol Physiol 2015; 308: L270-L286.
43. Lee SJ, Smith A, Guo L, Alastalo TP, Li M, Sawada H, et al., Autophagic protein LC3B confers resistance against hypoxia-induced pulmonary hypertension. Am J Respir Crit Care Med 2011; 183: 649-658.
44. Lahm T, Petrache I,. LC3 as a potential therapeutic target in hypoxia-induced pulmonary hypertension. Autophagy 2012; 8: 1146-1147.
45. Mayer ML, Blohmke CJ, Falsafi R, Fjell CD, Madera L, Turvey SE, et al., Rescue of dysfunctional autophagy attenuates hyperinflammatory responses from cystic fibrosis cells. J Immunol 2013; 190: 1227-1238.
46. Luciani A, Villella VR, Esposito S, Brunetti-Pierri N, Medina D, Settembre C, et al., Defective CFTR induces aggresome formation and lung inflammation in cystic fibrosis through ROS-mediated autophagy inhibition. Nat Cell Biol 2010; 12: 863-875.
47. De Stefano D, Villella VR, Esposito S, Tosco A, Sepe A, De Gregorio F, et al., Restoration of CFTR function in patients with cystic fibrosis carrying the F508del-CFTR mutation. Autophagy 2014; 10: 2053-2074.
48. Lee J, Yeganeh B, Ermini L, Post M,. Sphingolipids as cell fate regulators in lung development and disease. Apoptosis 2015; 20: 740-757.
49. Marzetti E, Csiszar A, Dutta D, Balagopal G, Calvani R, Leeuwenburgh C,. Role of mitochondrial dysfunction and altered autophagy in cardiovascular aging and disease: from mechanisms to therapeutics. Am J Physiol Heart Circ Physiol 2013; 305: H459-H476.
50. Rubinsztein DC, Marino G, Kroemer G,. Autophagy and aging. Cell 2011; 146: 682-695.
51. Ban GY, Pham DL, Trinh HK, Lee SI, Suh DH, Yang EM, et al., Autophagy mechanisms in sputum and peripheral blood cells of patients with severe asthma: a new therapeutic target. Clin Exp Allergy 2015; doi: 10.1111/cea.12585 [Epub ahead of print]
52. Dickinson JD, Alevy Y, Malvin NP, Patel KK, Gunsten SP, Holtzman MJ, et al., IL13 activates autophagy to regulate secretion in airway epithelial cells. Autophagy 2015; DOI:10.1080/15548627.2015.1056967 [Epub ahead of print]
53. Zeki AA, Ott S, Sandhu K, Ghavami S, Kenyon NJ,. The complex roles of endoplasmic reticulum stress and autophagy in modulating Eotaxin-3 production and secretion from human airway epithelial cells. Am J Respir Crit Care Med 2014; 189: A5683.
54. Poon AH, Chouiali F, Tse SM, Litonjua AA, Hussain SN, Baglole CJ, et al., Genetic and histologic evidence for autophagy in asthma pathogenesis. J Allergy Clin Immunol 2012; 129: 569-571.
55. Martin LJ, Gupta J, Jyothula SS, Butsch Kovacic M, Biagini Myers JM, Patterson TL, et al., Functional variant in the autophagy-related 5 gene promotor is associated with childhood asthma. PLoS One 2012; 7: e33454.
56. Ghavami S, Yeganeh B, Serebrin A, Mutawe MM, Sharma P, McNeill KD, et al., Autophagy regulates TGF-beta1 induced fibrosis in human airway smooth muscle cells. Am J Respir Crit Care Med 2011; 183: A2110.
57. Jyothula SS, Eissa NT,. Autophagy and role in asthma. Curr Opin Pulm Med 2013; 19: 30-35.
58. Graham MT, Nadeau KC,. Lessons learned from mice and man: mimicking human allergy through mouse models. Clin Immunol 2014; 155: 1-16.
59. Puleston DJ, Simon AK,. Autophagy in the immune system. Immunology 2014; 141: 1-8.
60. Cao Z, Pan P, Tan H, Tan Q, Wang Z, Su X, et al., Anti-nerve growth factor antibody reduces airway hyperresponsiveness in a mouse model of asthma by down-regulating the level of autophagy in lungs. Zhonghua Jie He He Hu Xi Za Zhi 2014; 37: 507-511.
61. Cho IH, Choi YJ, Gong JH, Shin D, Kang MK, Kang YH,. Astragalin inhibits autophagy-associated airway epithelial fibrosis. Respir Res 2015; 16: 51.
62. Neill T, Schaefer L, Iozzo RV,. Instructive roles of extracellular matrix on autophagy. Am J Pathol 2014 Aug; 184: 2146-2153.
63. Duran JM, Anjard C, Stefan C, Loomis WF, Malhotra V,. Unconventional secretion of Acb1 is mediated by autophagosomes. J Cell Biol 2010; 188: 527-536.
64. Bruns C, McCaffery JM, Curwin AJ, Duran JM, Malhotra V,. Biogenesis of a novel compartment for autophagosome-mediated unconventional protein secretion. J Cell Biol 2011; 195: 979-992.
65. Deretic V, Jiang S, Dupont N,. Autophagy intersections with conventional and unconventional secretion in tissue development, remodeling and inflammation. Trends Cell Biol 2012; 22: 397-406.
66. Jeffery PK, Laitinen A, Venge P,. Biopsy markers of airway inflammation and remodelling. Respir Med 2000; 94: S9-S15.
67. Sumi Y, Hamid Q,. Airway remodeling in asthma. Allergol Int 2007; 56: 341-348.
68. Schaafsma D, McNeill KD, Mutawe MM, Ghavami S, Unruh H, Jacques E, et al., Simvastatin inhibits TGFbeta1-induced fibronectin in human airway fibroblasts. Respir Res 2011; 12: 113.
69. Gerthoffer WT, Schaafsma D, Sharma P, Ghavami S, Halayko AJ,. Motility, survival, and proliferation. Compr Physiol 2012; 2: 255-281.
70. Schaafsma D, Dueck G, Ghavami S, Kroeker A, Mutawe MM, Hauff K, et al., The mevalonate cascade as a target to suppress extracellular matrix synthesis by human airway smooth muscle. Am J Respir Cell Mol Biol 2011; 44: 394-403.
71. Stewart A,. More muscle in asthma, but where did it come from? Am J Respir Crit Care Med 2012; 185: 1035-1037.
72. Yeganeh B, Mukherjee S, Moir LM, Kumawat K, Kashani HH, Bagchi RA, et al., Novel non-canonical TGF-beta signaling networks: emerging roles in airway smooth muscle phenotype and function. Pulm Pharmacol Ther 2013; 26: 50-63.
73. Gifford AH, Matsuoka M, Ghoda LY, Homer RJ, Enelow RI,. Chronic inflammation and lung fibrosis: pleotropic syndromes but limited distinct phenotypes. Mucosal Immunol 2012; 5: 480-484.
74. Sivakumar P, Ntolios P, Jenkins G, Laurent G,. Into the matrix: targeting fibroblasts in pulmonary fibrosis. Curr Opin Pulm Med 2012; 18: 462-469.
75. Camoretti-Mercado B, Solway J,. Transforming growth factor-beta1 and disorders of the lung. Cell Biochem Biophys 2005; 43: 131-148.
76. Mehal WZ, Iredale J, Friedman SL,. Scraping fibrosis: expressway to the core of fibrosis. Nat Med 2011; 17: 552-553.
77. Engelman JA,. Targeting PI3K signalling in cancer: opportunities, challenges and limitations. Nat Rev Cancer 2009; 9: 550-562.
78. Brana I, Siu LL,. Clinical development of phosphatidylinositol 3-kinase inhibitors for cancer treatment. BMC Med 2012; 10: 161.
79. Akinleye A, Avvaru P, Furqan M, Song Y, Liu D,. Phosphatidylinositol 3-kinase (PI3K) inhibitors as cancer therapeutics. J Hematol Oncol 2013; 6: 88.
80. Cleary JM, Shapiro GI,. Development of phosphoinositide-3 kinase pathway inhibitors for advanced cancer. Curr Oncol Rep 2010; 12: 87-94.
81. Falasca M,. Phosphoinositide 3-kinase pathway inhibitors: pharmacology, metabolism & drug development. Curr Med Chem 2011; 18: 2673.
82. McNamara CR, Degterev A,. Small-molecule inhibitors of the PI3K signaling network. Future Med Chem 2011; 3: 549-565.
83. Bago R, Malik N, Munson MJ, Prescott AR, Davies P, Sommer E, et al., Characterization of VPS34-IN1, a selective inhibitor of Vps34, reveals that the phosphatidylinositol 3-phosphate-binding SGK3 protein kinase is a downstream target of class III phosphoinositide 3-kinase. Biochem J 2014; 463: 413-427.
84. Pasquier B, El-Ahmad Y, Filoche-Romme B, Dureuil C, Fassy F, Abecassis PY, et al., Discovery of (2S)-8-[(3R)-3-methylmorpholin-4-yl]-1-(3-methyl-2-oxobutyl)-2-(trifluoromethyl)-3,4-dihydro-2H-pyrimido[1,2-a]pyrimidin-6-one: a novel potent and selective inhibitor of Vps34 for the treatment of solid tumors. J Med Chem 2015; 58: 376-400.
85. Ronan B, Flamand O, Vescovi L, Dureuil C, Durand L, Fassy F, et al., A highly potent and selective Vps34 inhibitor alters vesicle trafficking and autophagy. Nat Chem Biol 2014; 10: 1013-1019.
86. Chan EY,. mTORC1 phosphorylates the ULK1-mAtg13-FIP200 autophagy regulatory complex. Sci Signal 2009; 2: pe51.
87. Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA, Mair W, et al., Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 2011; 331: 456-461.
88. Shu CW, Madiraju C, Zhai D, Welsh K, Diaz P, Sergienko E, et al., High-throughput fluorescence assay for small-molecule inhibitors of autophagins/Atg4. J Biomol Screen 2011; 16: 174-182.
89. Chu PM, Chen LH, Chen MT, Ma HI, Su TL, Hsieh PC, et al., Targeting autophagy enhances BO-1051-induced apoptosis in human malignant glioma cells. Cancer Chemother Pharmacol 2012; 69: 621-633.
90. Hernandez-Gea V, Ghiassi-Nejad Z, Rozenfeld R, Gordon R, Fiel MI, Yue Z, et al., Autophagy releases lipid that promotes fibrogenesis by activated hepatic stellate cells in mice and in human tissues. Gastroenterology 2012; 142: 938-946.
91. Stoppoloni D, Politi L, Dalla Vedova P, Messano M, Koverech A, Scandurra R, et al., L-carnitine enhances extracellular matrix synthesis in human primary chondrocytes. Rheumatol Int 2013; 33: 2399-2403.
92. Cabrera S, Maciel M, Herrera I, Nava T, Vergara F, Gaxiola M, et al., Essential role for the ATG4B protease and autophagy in bleomycin-induced pulmonary fibrosis. Autophagy 2015; 11: 670-684.
93. Araya J, Kojima J, Takasaka N, Ito S, Fujii S, Hara H, et al., Insufficient autophagy in idiopathic pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2013; 304: L56-L69.