Autophagy proteins control goblet cell function by potentiating reactive oxygen species production

EMBO Journal

Volumn 32, Issue 24, 2013, Pages 3130-3144

  Patel, Khushbu K ^a   Miyoshi, Hiroyuki ^a   Beatty, Wandy L ^a   Head, Richard D ^a   Malvin, Nicole P ^a   Cadwell, Ken ^b   Guan, Jun Lin ^c   Saitoh, Tatsuya ^d   Akira, Shizuo ^d   Seglen, Per O ^e   Dinauer, Mary C ^a   Virgin, Herbert W ^a   Stappenbeck, Thaddeus S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d OSAKA UNIVERSITY   (Japan)

^e OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

Autophagy; Epithelium; Goblet cell; Intestine; NADPH oxidase

Indexed keywords

AUTOPHAGY PROTEIN 5; AUTOPHAGY PROTEIN LC3 BETA; MESSENGER RNA; MUCIN 2; PEPTIDES AND PROTEINS; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL DIFFERENTIATION; CELL FUNCTION; CELL MEMBRANE; CELL VACUOLE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; EXOCYTOSIS; GOBLET CELL; INTESTINE EPITHELIUM CELL; LOSS OF FUNCTION MUTATION; MOUSE; MUCUS SECRETION; MULTIVESICULAR BODY; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ANIMALS; AUTOPHAGY; CELLS, CULTURED; COLON; ENDOCYTOSIS; EPITHELIAL CELLS; GOBLET CELLS; MICE; MICE, MUTANT STRAINS; MICROTUBULE-ASSOCIATED PROTEINS; MUCINS; MUTATION; NADPH OXIDASE; PHAGOSOMES; REACTIVE OXYGEN SPECIES; VESICULAR TRANSPORT PROTEINS;

EID: 84890555657     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.233     Document Type: Article

References (65)

1. Abdullah LH, Conway JD, Cohn JA, Davis CW (1997) Protein kinase C and Ca2+ activation of mucin secretion in airway goblet cells. Am J Physiol 273: L201-L210
2. Anderson CA, Boucher G, Lees CW, Franke A, D'Amato M, Taylor KD, Lee JC, Goyette P, Imielinski M, Latiano A, Lagace C, Scott R, Amininejad L, Bumpstead S, Baidoo L, Baldassano RN, Barclay M, Bayless TM, Brand S, Buning C et al (2011) Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nat Genet 43: 246-252
3. Artis D, Grencis RK (2008) The intestinal epithelium: sensors to effectors in nematode infection. Mucosal Immunol 1: 252-264
4. Bedard K, Krause KH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87: 245-313
5. Berg TO, Fengsrud M, Stromhaug PE, Berg T, Seglen PO (1998) Isolation and characterization of rat liver amphisomes. Evidence for fusion of autophagosomes with both early and late endosomes. J Biol Chem 273: 21883-21892
6. Cadwell K, Liu JY, Brown SL, Miyoshi H, Loh J, Lennerz JK, Kishi C, Kc W, Carrero JA, Hunt S, Stone CD, Brunt EM, Xavier RJ, Sleckman BP, Li E, Mizushima N, Stappenbeck TS, Virgin 4th HW (2008) A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 456: 259-263
7. Cadwell K, Patel KK, Komatsu M, Virgin 4th HW, Stappenbeck TS (2009) A common role for Atg16L1, Atg5 and Atg7 in small intestinal Paneth cells and Crohn disease. Autophagy 5: 250-252
8. Cadwell K, Patel KK, Maloney NS, Liu TC, Ng AC, Storer CE, Head RD, Xavier R, Stappenbeck TS, Virgin HW (2010) Virus-plussusceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine. Cell 141: 1135-1145
9. Cann GM, Guignabert C, Ying L, Deshpande N, Bekker JM, Wang L, Zhou B, Rabinovitch M (2008) Developmental expression of LC3alpha and beta: absence of fibronectin or autophagy phenotype in LC3beta knockout mice. Dev Dyn 237: 187-195
10. Casbon AJ, Allen LA, Dunn KW, Dinauer MC (2009) Macrophage NADPH oxidase flavocytochrome B localizes to the plasma membrane and Rab11-positive recycling endosomes. J Immunol 182: 2325-2339
11. Chang WW, Leblond CP (1971) Renewal of the epithelium in the descending colon of the mouse. I. Presence of three cell populations: vacuolated-columnar, mucous and argentaffin. Am J Anat 131: 73-99
12. Cheranov SY, Jaggar JH (2006) TNF-alpha dilates cerebral arteries via NAD(P)H oxidase-dependent Ca2+ spark activation. Am J Physiol Cell Physiol 290: C964-C971
13. Conway JD, Bartolotta T, Abdullah LH, Davis CW (2003) Regulation of mucin secretion from human bronchial epithelial cells grown in murine hosted xenografts. Am J Physiol Lung Cell Mol Physiol 284: L945-L954
14. Crutzen R, Shlyonsky V, Louchami K, Virreira M, Hupkens E, Boom A, Sener A, Malaisse WJ, Beauwens R (2012) Does NAD(P)H oxidase-derived H2O2 participate in hypotonicity-induced insulin release by activating VRAC in beta-cells? Pflugers Arch 463: 377-390
15. Davis CW, Dickey BF (2008) Regulated airway goblet cell mucin secretion. Annu Rev Physiol 70: 487-512
16. DeSelm CJ, Miller BC, Zou W, Beatty WL, van Meel E, Takahata Y, Klumperman J, Tooze SA, Teitelbaum SL, Virgin HW (2011) Autophagy proteins regulate the secretory component of osteoclastic bone resorption. Dev Cell 21: 966-974
17. Ebato C, Uchida T, Arakawa M, Komatsu M, Ueno T, Komiya K, Azuma K, Hirose T, Tanaka K, Kominami E, Kawamori R, Fujitani Y, Watada H (2008) Autophagy is important in islet homeostasis and compensatory increase of beta cell mass in response to high-fat diet. Cell Metab 8: 325-332
18. Falk P, Roth KA, Gordon JI (1994) Lectins are sensitive tools for defining the differentiation programs of mouse gut epithelial cell lineages. Am J Physiol 266: G987-G1003
19. Florey O, Kim SE, Sandoval CP, Haynes CM, Overholtzer M (2011) Autophagy machinery mediates macroendocytic processing and entotic cell death by targeting single membranes. Nat Cell Biol 13: 1335-1343
20. Franke A, McGovern DP, Barrett JC, Wang K, Radford-Smith GL, Ahmad T, Lees CW, Balschun T, Lee J, Roberts R, Anderson CA, Bis JC, Bumpstead S, Ellinghaus D, Festen EM, Georges M, Green T, Haritunians T, Jostins L, Latiano A et al (2010) Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat Genet 42: 1118-1125
21. Gan B, Peng X, Nagy T, Alcaraz A, Gu H, Guan JL (2006) Role of FIP200 in cardiac and liver development and its regulation of TNFalpha and TSC-mTOR signaling pathways. J Cell Biol 175: 121-133
22. Gordon PB, Hoyvik H, Seglen PO (1992) Prelysosomal and lysosomal connections between autophagy and endocytosis. Biochem J 283: 361-369
23. Gordon PB, Seglen PO (1988) Prelysosomal convergence of autophagic and endocytic pathways. Biochem Biophys Res Commun 151: 40-47
24. Granados MP, Salido GM, Gonzalez A, Pariente JA (2006) Dosedependent effect of hydrogen peroxide on calcium mobilization in mouse pancreatic acinar cells. Biochem Cell Biol 84: 39-48
25. Gundelfinger ED, Kessels MM, Qualmann B (2003) Temporal and spatial coordination of exocytosis and endocytosis. Nat Rev Mol Cell Biol 4: 127-139
26. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki- Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, Mizushima N (2006) Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441: 885-889
27. Henault J, Martinez J, Riggs JM, Tian J, Mehta P, Clarke L, Sasai M, Latz E, Brinkmann MM, Iwasaki A, Coyle AJ, Kolbeck R, Green DR, Sanjuan MA (2012) Noncanonical autophagy is required for type I interferon secretion in response to DNA-immune complexes. Immunity 37: 986-997
28. Hidalgo C, Sanchez G, Barrientos G, Aracena-Parks P (2006) A transverse tubule NADPH oxidase activity stimulates calcium release from isolated triads via ryanodine receptor type 1 S - glutathionylation. J Biol Chem 281: 26473-26482
29. Huang J, Canadien V, Lam GY, Steinberg BE, Dinauer MC, Magalhaes MA, Glogauer M, Grinstein S, Brumell JH (2009) Activation of antibacterial autophagy by NADPH oxidases. Proc Natl Acad Sci USA 106: 6226-6231
30. Huang da W, Sherman BT, Lempicki RA (2009a) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1-13
31. Huang da W, Sherman BT, Lempicki RA (2009b) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57
32. Jackson SH, Gallin JI, Holland SM (1995) The p47phox mouse knock-out model of chronic granulomatous disease. J Exp Med 182: 751-758
33. Johansson ME, Larsson JM, Hansson GC (2011) The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc Natl Acad Sci USA 108(Suppl 1): 4659-4665
34. Jung HS, Chung KW, Won Kim J, Kim J, Komatsu M, Tanaka K, Nguyen YH, Kang TM, Yoon KH, Kim JW, Jeong YT, Han MS, Lee MK, Kim KW, Shin J, Lee MS (2008) Loss of autophagy diminishes pancreatic beta cell mass and function with resultant hyperglycemia. Cell Metab 8: 318-324
35. Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y, Kominami E, Tanaka K, Chiba T (2005) Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 169: 425-434
36. Lam GY, Fattouh R, Muise AM, Grinstein S, Higgins DE, Brumell JH (2011) Listeriolysin O suppresses phospholipase C-mediated activation of the microbicidal NADPH oxidase to promote Listeria monocytogenes infection. Cell Host Microbe 10: 627-634
37. Lam GY, Huang J, Brumell JH (2010) The many roles of NOX2 NADPH oxidase-derived ROS in immunity. Semin Immunopathol 32: 415-430
38. Lamb FS, Hook JS, Hilkin BM, Huber JN, Volk AP, Moreland JG (2012) Endotoxin priming of neutrophils requires endocytosis and NADPH oxidase-dependent endosomal reactive oxygen species. J Biol Chem 287: 12395-12404
39. Levine B, Mizushima N, Virgin HW (2011) Autophagy in immunity and inflammation. Nature 469: 323-335
40. Li N, Li B, Brun T, Deffert-Delbouille C, Mahiout Z, Daali Y, Ma XJ, Krause KH, Maechler P (2012) NADPH oxidase NOX2 defines a new antagonistic role for reactive oxygen species and cAMP/PKA in the regulation of insulin secretion. Diabetes 61: 2842-2850
41. Longatti A, Lamb CA, Razi M, Yoshimura S, Barr FA, Tooze SA (2012) TBC1D14 regulates autophagosome formation via Rab11- and ULK1-positive recycling endosomes. J Cell Biol 197: 659-675
42. Madison BB, Dunbar L, Qiao XT, Braunstein K, Braunstein E, Gumucio DL (2002) Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J Biol Chem 277: 33275-33283
43. Marino G, Fernandez AF, Cabrera S, Lundberg YW, Cabanillas R, Rodriguez F, Salvador-Montoliu N, Vega JA, Germana A, Fueyo A, Freije JM, Lopez-Otin C (2010) Autophagy is essential for mouse sense of balance. J Clin Invest 120: 2331-2344
44. Martinez J, Almendinger J, Oberst A, Ness R, Dillon CP, Fitzgerald P, Hengartner MO, Green DR (2011) Microtubule-associated protein 1 light chain 3 alpha (LC3)-associated phagocytosis is required for the efficient clearance of dead cells. Proc Natl Acad Sci USA 108: 17396-17401
45. Matsunaga K, Saitoh T, Tabata K, Omori H, Satoh T, Kurotori N, Maejima I, Shirahama-Noda K, Ichimura T, Isobe T,Akira S, Noda T, Yoshimori T (2009) Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat Cell Biol 11: 385-396
46. McGuckin MA, Linden SK, Sutton P, Florin TH (2011) Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9: 265-278
47. Miyoshi H, Ajima R, Luo CT, Yamaguchi TP, Stappenbeck TS (2012) Wnt5a potentiates TGF-beta signaling to promote colonic crypt regeneration after tissue injury. Science 338: 108-113
48. Morimoto M, Liu Z, Cheng HT, Winters N, Bader D, Kopan R (2010) Canonical Notch signaling in the developing lung is required for determination of arterial smooth muscle cells and selection of Clara versus ciliated cell fate. J Cell Sci 123: 213-224
49. Nakano Y, Longo-Guess CM, Bergstrom DE, Nauseef WM, Jones SM, Banfi B (2008) Mutation of the Cyba gene encoding p22phox causes vestibular and immune defects in mice. J Clin Invest 118: 1176-1185
50. Pellegrinet L, Rodilla V, Liu Z, Chen S, Koch U, Espinosa L, Kaestner KH, Kopan R, Lewis J, Radtke F (2011) Dll1- and dll4- mediated notch signaling are required for homeostasis of intestinal stem cells. Gastroenterology 140: 1230-1240 e1231-1237
51. Pull SL, Doherty JM, Mills JC, Gordon JI, Stappenbeck TS (2005) Activated macrophages are an adaptive element of the colonic epithelial progenitor niche necessary for regenerative responses to injury. Proc Natl Acad Sci USA 102: 99-104
52. Ravikumar B, Moreau K, Jahreiss L, Puri C, Rubinsztein DC (2010) Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat Cell Biol 12: 747-757
53. Razi M, Chan EY, Tooze SA (2009) Early endosomes and endosomal coatomer are required for autophagy. J Cell Biol 185: 305-321
54. Sanjuan MA, Dillon CP, Tait SW, Moshiach S, Dorsey F, Connell S, Komatsu M, Tanaka K, Cleveland JL, Withoff S, Green DR (2007) Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450: 1253-1257
55. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z (2007) Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 26: 1749-1760
56. Seglen PO (2008) Where endocytosis and autophagy meet: The amphisome. In Hepatic Endocytosis, Sporstol Fonhus M, Mousavi SA, Berg T (eds), pp 61-100. Trivandrum (Kerala): Transworld Research Network
57. Shaw PA, Catchpole IR, Goddard CA, Colledge WH (2008) Comparison of protein transduction domains in mediating cell delivery of a secreted CRE protein. Biochemistry 47: 1157-1166
58. Snippert HJ, van der Flier LG, Sato T, van Es JH, van den Born M, Kroon-Veenboer C, Barker N, Klein AM, van Rheenen J, Simons BD, Clevers H (2010) Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143: 134-144
59. Specian RD, Oliver MG (1991) Functional biology of intestinal goblet cells. Am J Physiol 260: C183-C193
60. Stappenbeck TS, Mills JC, Gordon JI (2003) Molecular features of adult mouse small intestinal epithelial progenitors. Proc Natl Acad Sci USA 100: 1004-1009
61. Ushio H, Ueno T, Kojima Y, Komatsu M, Tanaka S, Yamamoto A, Ichimura Y, Ezaki J, Nishida K, Komazawa-Sakon S, Niyonsaba F, Ishii T, Yanagawa T, Kominami E, OgawaH, Okumura K, Nakano H (2011) Crucial role for autophagy in degranulation of mast cells. J Allergy Clin Immunol 127: 1267-1276 e1266
62. Vazquez-Torres A, Xu Y, Jones-Carson J, Holden DW, Lucia SM, Dinauer MC, Mastroeni P, Fang FC (2000) Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 287: 1655-1658
63. Wang X, Takeda S, Mochizuki S, Jindal R, Dhalla NS (1999) Mechanisms of hydrogen peroxide-induced increase in intracellular calcium in cardiomyocytes. J Cardiovasc Pharmacol Ther 4: 41-48
64. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30: e15
65. Zhu Y, Ehre C, Abdullah LH, Sheehan JK, Roy M, Evans CM, Dickey BF, Davis CW (2008) Munc13-2-/- baseline secretion defect reveals source of oligomeric mucins in mouse airways. J Physiol 586: 1977-1992