Optineurin deficiency in mice contributes to impaired cytokine secretion and neutrophil recruitment in bacteria-driven colitis

DMM Disease Models and Mechanisms

Volumn 8, Issue 8, 2015, Pages 817-829

  Chew, Thean S ^a   O'Shea, Nuala R ^a   Sewell, Gavin W ^a   Oehlers, Stefan H ^b   Mulvey, Claire M ^a,c   Crosier, Philip S ^b   Godovac Zimmermann, Jasminka ^a   Bloom, Stuart L ^d   Smith, Andrew M ^a,e   Segal, Anthony W ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON HOSPITALS   (United Kingdom)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Crohn's disease; Cytokines; Escherichia coli; Macrophages; TNF

Indexed keywords

CELL PROTEIN; CYTOKINE; INTERLEUKIN 6; OPTINEURIN; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; EYE PROTEIN; OPTN PROTEIN, HUMAN; OPTN PROTEIN, MOUSE; TRANSCRIPTION FACTOR IIIA; TUMOR NECROSIS FACTOR;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL INFECTION; BONE MARROW DERIVED MACROPHAGE; CELL FRACTIONATION; CITROBACTER; CLINICAL ARTICLE; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CROHN DISEASE; CYTOKINE RELEASE; ENTAMOEBA COLI; FEMALE; GENETIC TRANSCRIPTION; GOLGI COMPLEX; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INHERITANCE; LIQUID CHROMATOGRAPHY; LYSOSOME; MALE; MIDDLE AGED; MOUSE; NEUTROPHIL; NONHUMAN; PERITONITIS; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SALMONELLOSIS; TANDEM MASS SPECTROMETRY; TRANS GOLGI NETWORK; YOUNG ADULT; ZEBRA FISH; ANIMAL; BACTERIUM; BIOLOGICAL MODEL; BLOOD; CASE CONTROL STUDY; COLITIS; DEFICIENCY; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; GENETICS; MACROPHAGE; METABOLISM; MICROBIOLOGY; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; PHYSIOLOGY; SECRETION (PROCESS); SINGLE NUCLEOTIDE POLYMORPHISM; UPREGULATION;

BACTERIA (MICROORGANISMS); CITROBACTER; DANIO RERIO; ESCHERICHIA COLI; MUS; SALMONELLA;

ADULT; ANIMALS; BACTERIA; CASE-CONTROL STUDIES; CITROBACTER; COLITIS; CROHN DISEASE; CYTOKINES; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; EYE PROTEINS; FEMALE; GOLGI APPARATUS; HUMANS; INFLAMMATION MEDIATORS; INHERITANCE PATTERNS; MACROPHAGES; MALE; MICE; MIDDLE AGED; MODELS, BIOLOGICAL; NEUTROPHIL INFILTRATION; POLYMORPHISM, SINGLE NUCLEOTIDE; TRANSCRIPTION FACTOR TFIIIA; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION; ZEBRAFISH;

EID: 84939478111     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.020362     Document Type: Article

References (65)

1. Albagha, O. M. E. , Visconti, M. R. , Alonso, N. , Langston, A. L. , Cundy, T. , Dargie, R. , Dunlop, M. G. , Fraser, W. D. , Hooper, M. J. , Isaia, G. et al. (2010). Genomewide association study identifies variants at CSF1, OPTN and TNFRSF11A as genetic risk factors for Paget's disease of bone. Nat. Genet. 42, 520-524.
2. Baumgart, D. C. and Sandborn, W. J. (2012). Crohn's disease. Lancet 380, 1590-1605.
3. Bedell, V. M. , Westcot, S. E. and Ekker, S. C. (2011). Lessons from morpholinobased screening in zebrafish. Brief. Funct. Genomics 10, 181-188.
4. Belzil, V. V. , Daoud, H. , Desjarlais, A. , Bouchard, J.-P. , Dupré, N. , Camu, W. , Dion, P. A. and Rouleau, G. A. (2011). Analysis of OPTN as a causative gene for amyotrophic lateral sclerosis. Neurobiol. Aging 32, 555. e13-555. e14.
5. Bond, L. M. , Peden, A. A. , Kendrick-Jones, J. , Sellers, J. R. and Buss, F. (2011). Myosin VI and its binding partner optineurin are involved in secretory vesicle fusion at the plasma membrane. Mol. Biol. Cell 22, 54-65.
6. Bosenko, D. V. , Zinkevich, N. S. , Tyler, R. C. , Link, B. A. and Semina, E. V. (2004). Sequence and expression of zebrafish optineurin gene suggests conserved function in vertebrate eye. Invest. Ophthalmol. Vis. Sci. 45, 4408.
7. Chassaing, B. , Aitken, J. D. , Malleshappa, M. and Vijay-Kumar, M. (2014). Dextran sulfate sodium (DSS)-induced colitis in mice. Curr. Protoc. Immunol. 104, Unit 15 25.
8. Chew, T. , Sewell, G. , O'Shea, N. , Bloom, S. , Segal, A. and Smith, A. (2014). LB-003 the role of optineurin in macrophage cytokine secretion and bowel inflammation. Gut 63 Suppl. 1, e2.
9. Chi, Z.-L. , Akahori, M. , Obazawa, M. , Minami, M. , Noda, T. , Nakaya, N. , Tomarev, S. , Kawase, K. , Yamamoto, T. , Noda, S. et al. (2010). Overexpression of optineurin E50K disrupts Rab8 interaction and leads to a progressive retinal degeneration in mice. Hum. Mol. Genet. 19, 2606-2615.
10. Claes, A.-K. , Steck, N. , Schultz, D. , Zähringer, U. , Lipinski, S. , Rosenstiel, P. , Geddes, K. , Philpott, D. J. , Heine, H. and Grassl, G. A. (2014). Salmonella enterica serovar Typhimurium DeltamsbB triggers exacerbated inflammation in Nod2 deficient mice. PLoS ONE 9, e113645.
11. Collins, J. W. , Keeney, K. M. , Crepin, V. F. , Rathinam, V. A. , Fitzgerald, K. A. , Finlay, B. B. and Frankel, G. (2014). Citrobacter rodentium: Infection, inflammation and the microbiota. Nat. Rev. Microbiol. 12, 612-623.
12. de Bruyn, M. , Machiels, K. , Vandooren, J. , Lemmens, B. , Van Lommel, L. , Breynaert, C. , Van der Goten, J. , Staelens, D. , Billiet, T. , De Hertogh, G. et al. (2014). Infliximab restores the dysfunctional matrix remodeling protein and growth factor gene expression in patients with inflammatory bowel disease. Inflamm. Bowel Dis. 20, 339-352.
13. Del Bo, R. , Tiloca, C. , Pensato, V. , Corrado, L. , Ratti, A. , Ticozzi, N. , Corti, S. , Castellotti, B. , Mazzini, L. , Soraru, G. et al. (2011). Novel optineurin mutations in patients with familial and sporadic amyotrophic lateral sclerosis. J. Neurol. Neurosurg. Psychiatry 82, 1239-1243.
14. del Toro, D. , Alberch, J. , Lazaro-Dieguez, F. , Martin-Ibanez, R. , Xifro, X. , Egea, G. and Canals, J. M. (2009). Mutant huntingtin impairs post-Golgi trafficking to lysosomes by delocalizing optineurin/Rab8 complex from the Golgi apparatus. Mol. Biol. Cell 20, 1478-1492.
15. Dhillon, S. S. , Fattouh, R. , Elkadri, A. , Xu, W. , Murchie, R. , Walters, T. , Guo, C. , Mack, D. , Huynh, H. Q. , Baksh, S. et al. (2014). Variants in NADPH oxidase complex components determine susceptibility to very early onset inflammatory bowel disease. Gastroenterology 147, 680-689. e2.
16. Dippold, H. C. , Ng, M. M. , Farber-Katz, S. E. , Lee, S.-K. , Kerr, M. L. , Peterman, M. C. , Sim, R. , Wiharto, P. A. , Galbraith, K. A. , Madhavarapu, S. et al. (2009). GOLPH3 bridges phosphatidylinositol-4-phosphate and actomyosin to stretch and shape the Golgi to promote budding. Cell 139, 337-351.
17. Dunn, D. L. , Barke, R. A. , Knight, N. B. , Humphrey, E. W. and Simmons, R. L. (1985). Role of resident macrophages, peripheral neutrophils, and translymphatic absorption in bacterial clearance from the peritoneal cavity. Infect. Immun. 49, 257-264.
18. Farthing, M. J. G. (2004). Bugs and the gut: An unstable marriage. Best Pract. Res. Clin. Gastroenterol. 18, 233-239.
19. Franke, A. , McGovern, D. P. B. , Barrett, J. C. , Wang, K. , Radford-Smith, G. L. , Ahmad, T. , Lees, C. W. , Balschun, T. , Lee, J. , Roberts, R. et al. (2010). Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat. Genet. 42, 1118-1125.
20. Ginhoux, F. and Jung, S. (2014). Monocytes and macrophages: Developmental pathways and tissue homeostasis. Nat. Rev. Immunol. 14, 392-404.
21. Gleason, C. E. , Ordureau, A. , Gourlay, R. , Arthur, J. S. C. and Cohen, P. (2011). Polyubiquitin binding to optineurin is required for optimal activation of TANKbinding kinase 1 and production of interferon beta. J. Biol. Chem. 286, 35663-35674.
22. Goncalves, N. S. , Ghaem-Maghami, M. , Monteleone, G. , Frankel, G. , Dougan, G. , Lewis, D. J. M. , Simmons, C. P. and MacDonald, T. T. (2001). Critical role for tumor necrosis factor alpha in controlling thenumber of lumenal pathogenic bacteria and immunopathology in infectious colitis. Infect. Immun. 69, 6651-6659.
23. Hall, L. J. , Faivre, E. , Quinlan, A. , Shanahan, F. , Nally, K. and Melgar, S. (2011). Induction and activation of adaptive immune populations during acute and chronic phases of a murine model of experimental colitis. Dig. Dis. Sci. 56, 79-89.
24. Hugot, J.-P. , Chamaillard, M. , Zouali, H. , Lesage, S. , Cézard, J.-P. , Belaiche, J. , Almer, S. , Tysk, C. , O'Morain, C. A. , Gassull, M. et al. (2001). Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 411, 599-603.
25. Ito, H. , Fujita, K. , Nakamura, M. , Wate, R. , Kaneko, S. , Sasaki, S. , Yamane, K. , Suzuki, N. , Aoki, M. , Shibata, N. et al. (2011). Optineurin is co-localized with FUS in basophilic inclusions of ALS with FUS mutation and in basophilic inclusion body disease. Acta Neuropathol. 121, 555-557.
26. Jostins, L. Ripke, S. Weersma, R. K. Duerr, R. H. McGovern, D. P. Hui, K. Y. Lee, J. C. Schumm, L. P. Sharma, Y. Anderson, C. A. et al. (2012). Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491, 119-124.
27. Khor, B. , Gardet, A. and Xavier, R. J. (2011). Genetics and pathogenesis of inflammatory bowel disease. Nature 474, 307-317.
28. Kim, Y.-G. , Kamada, N. , Shaw, M. H. , Warner, N. , Chen, G. Y. , Franchi, L. and Núñez, G. (2011). The Nod2 sensor promotes intestinal pathogen eradication via the chemokine CCL2-dependent recruitment of inflammatory monocytes. Immunity 34, 769-780.
29. Kobayashi, K. S. , Chamaillard, M. , Ogura, Y. , Henegariu, O. , Inohara, N. , Nuñez, G. and Flavell, R. A. (2005). Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 307, 731-734.
30. Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408.
31. Manderson, A. P. , Kay, J. G. , Hammond, L. A. , Brown, D. L. and Stow, J. L. (2007). Subcompartments of the macrophage recycling endosome direct the differential secretion of IL-6 and TNFalpha. J. Cell Biol. 178, 57-69.
32. Mankouri, J. , Fragkoudis, R. , Richards, K. H. , Wetherill, L. F. , Harris, M. , Kohl, A. , Elliott, R. M. and Macdonald, A. (2010). Optineurin negatively regulates the induction of IFNbeta in response toRNAvirus infection. PLoSPathog. 6, e1000778.
33. Marino, M. W. , Dunn, A. , Grail, D. , Inglese, M. , Noguchi, Y. , Richards, E. , Jungbluth, A. , Wada, H. , Moore, M. , Williamson, B. et al. (1997). Characterization of tumor necrosis factor-deficient mice. Proc. Natl. Acad. Sci. USA 94, 8093-8098.
34. Marks, D. J. B. , Harbord, M. W. N. , MacAllister, R. , Rahman, F. Z. , Young, J. , Al-Lazikani, B. , Lees, W. , Novelli, M. , Bloom, S. and Segal, A. W. (2006). Defective acute inflammation in Crohn's disease: A clinical investigation. Lancet 367, 668-678.
35. Marks, D. J. B. , Miyagi, K. , Rahman, F. Z. , Novelli, M. , Bloom, S. L. and Segal, A. W. (2009). Inflammatory bowel disease in CGD reproduces the clinicopathological features of Crohn's disease. Am. J. Gastroenterol. 104, 117-124.
36. Maruyama, H. , Morino, H. , Ito, H. , Izumi, Y. , Kato, H. , Watanabe, Y. , Kinoshita, Y. , Kamada, M. , Nodera, H. , Suzuki, H. et al. (2010). Mutations of optineurin in amyotrophic lateral sclerosis. Nature 465, 223-226.
37. Medzhitov, R. (2008). Origin and physiological roles of inflammation. Nature 454, 428-435.
38. Millecamps, S. , Boillée, S. , Chabrol, E. , Camu, W. , Cazeneuve, C. , Salachas, F. , Pradat, P.-F. , Danel-Brunaud, V. , Vandenberghe, N. , Corcia, P. et al. (2011). Screening of OPTN in French familial amyotrophic lateral sclerosis. Neurobiol. Aging 32, 557. e11-557. e13.
39. Mulvey, C. M. , Tudzarova, S. , Crawford, M. , Williams, G. H. , Stoeber, K. and Godovac-Zimmermann, J. (2013). Subcellular proteomics reveals a role for nucleo-cytoplasmic trafficking at the DNA replication origin activation checkpoint. J. Proteome Res. 12, 1436-1453.
40. Munitic, I. , Giardino Torchia, M. L. , Meena, N. P. , Zhu, G. , Li, C. C. and Ashwell, J. D. (2013). Optineurin insufficiency impairs IRF3 but not NF-kappaB activation in immune cells. J. Immunol. 191, 6231-6240.
41. Murray, R. Z. , Kay, J. G. , Sangermani, D. G. and Stow, J. L. (2005). A role for the phagosome in cytokine secretion. Science 310, 1492-1495.
42. Murthy, A. , Li, Y. , Peng, I. , Reichelt, M. , Katakam, A. K. , Noubade, R. , Roose-Girma, M. , DeVoss, J. , Diehl, L. , Graham, R. R. et al. (2014). A Crohn's disease variant in Atg16l1 enhances its degradation by caspase 3. Nature 506, 456-462.
43. Naito, Y. , Takagi, T. , Handa, O. , Ishikawa, T. , Nakagawa, S. , Yamaguchi, T. , Yoshida, N. , Minami, M. , Kita, M. , Imanishi, J. et al. (2003). Enhanced intestinal inflammation induced by dextran sulfate sodium in tumor necrosis factor-alpha deficient mice. J. Gastroenterol. Hepatol. 18, 560-569.
44. Nasevicius, A. and Ekker, S. C. (2000). Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 26, 216-220.
45. Oehlers, S. H. , Flores, M. V. , Chen, T. , Hall, C. J. , Crosier, K. E. and Crosier, P. S. (2011). Topographical distribution of antimicrobial genes in the zebrafish intestine. Dev. Comp. Immunol. 35, 385-391.
46. Ogura, Y. , Bonen, D. K. , Inohara, N. , Nicolae, D. L. , Chen, F. F. , Ramos, R. , Britton, H. , Moran, T. , Karaliuskas, R. , Duerr, R. H. et al. (2001). A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411, 603-606.
47. Perse, M. and Cerar, A. (2012). Dextran sodium sulphate colitis mouse model: Traps and tricks. J. Biomed. Biotechnol. 2012, 718617.
48. Prajsnar, T. K. , Cunliffe, V. T. , Foster, S. J. and Renshaw, S. A. (2008). A novel vertebrate model of Staphylococcus aureus infection reveals phagocytedependent resistance of zebrafish to non-host specialized pathogens. Cell Microbiol. 10, 2312-2325.
49. Rahman, F. Z. , Smith, A. M. , Hayee, B. , Marks, D. J. B. , Bloom, S. L. and Segal, A. W. (2010). Delayed resolution of acute inflammation in ulcerative colitis is associated with elevated cytokine release downstream of TLR4. PLoS ONE 5, e9891.
50. Rezaie, T. , Child, A. , Hitchings, R. , Brice, G. , Miller, L. , Coca-Prados, M. , Héon, E. , Krupin, T. , Ritch, R. , Kreutzer, D. et al. (2002). Adult-onset primary openangle glaucoma caused by mutations in optineurin. Science 295, 1077-1079.
51. Sahlender, D. A. , Roberts, R. C. , Arden, S. D. , Spudich, G. , Taylor, M. J. , Luzio, J. P. , Kendrick-Jones, J. and Buss, F. (2005). Optineurin links myosin VI to the Golgi complex and is involved in Golgi organization and exocytosis. J. Cell Biol. 169, 285-295.
52. Schreiber, H. A. , Loschko, J. , Karssemeijer, R. A. , Escolano, A. , Meredith, M. M. , Mucida, D. , Guermonprez, P. and Nussenzweig, M. C. (2013). Intestinal monocytes and macrophages are required for T cell polarization in response to Citrobacter rodentium. J. Exp. Med. 210, 2025-2039.
53. Segal, A. W. and Loewi, G. (1976). Neutrophil dysfunction in Crohn's disease. Lancet 308, 219-221.
54. Sewell, G. W. , Marks, D. J. B. and Segal, A. W. (2009). The immunopathogenesis of Crohn's disease: A three-stage model. Curr. Opin. Immunol. 21, 506-513.
55. Sewell, G. W. , Rahman, F. Z. , Levine, A. P. , Jostins, L. , Smith, P. J. , Walker, A. P. , Bloom, S. L. , Segal, A. W. and Smith, A. M. (2012). Defective tumor necrosis factor release from Crohn's disease macrophages in response to toll-like receptor activation: Relationship to phenotype and genome-wide association susceptibility loci. Inflamm. Bowel Dis. 18, 2120-2127.
56. Shurety, W. , Merino-Trigo, A. , Brown, D. , Hume, D. A. and Stow, J. L. (2000). Localization and post-Golgi trafficking of tumor necrosis factor-alpha in macrophages. J. Interferon Cytokine Res. 20, 427-438.
57. Skarnes, W. C. , Rosen, B. , West, A. P. , Koutsourakis, M. , Bushell, W. , Iyer, V. , Mujica, A. O. , Thomas, M. , Harrow, J. , Cox, T. et al. (2011). A conditional knockout resource for the genome-wide study of mouse gene function. Nature 474, 337-342.
58. Smith, A. M. , Rahman, F. Z. , Hayee, B. , Graham, S. J. , Marks, D. J. B. , Sewell, G. W. , Palmer, C. D. , Wilde, J. , Foxwell, B. M. J. , Gloger, I. S. et al. (2009). Disordered macrophage cytokine secretion underlies impaired acute inflammation and bacterial clearance in Crohn's disease. J. Exp. Med. 206, 1883-1897.
59. Smith, A. M. , Sewell, G. W. , Levine, A. P. , Chew, T. S. , Dunne, J. , O'Shea, N. R. , Smith, P. J. , Harrison, P. J. , Macdonald, C. M. , Bloom, S. L. et al. (2015). Disruption of macrophage pro-inflammatory cytokine release in Crohn's disease is associated with reduced optineurin expression in a subset of patients. Immunology 144, 45-55.
60. Solski, J. A. , Williams, K. L. , Yang, S. , Nicholson, G. A. and Blair, I. P. (2012). Mutation analysis of the optineurin gene in familial amyotrophic lateral sclerosis. Neurobiol. Aging 33, 210. e9-210. e10.
61. Tumer, Z. , Bertelsen, B. , Gredal, O. , Magyari, M. , Nielsen, K. C. , Lucamp, Grønskov, K. and Brøndum-Nielsen, K. (2012). Novel heterozygous nonsense mutation of the OPTN gene segregating in a Danish family with ALS. Neurobiol. Aging 33, 208. e1-208. e5.
62. Wild, P. , Farhan, H. , McEwan, D. G. , Wagner, S. , Rogov, V. V. , Brady, N. R. , Richter, B. , Korac, J. , Waidmann, O. , Choudhary, C. et al. (2011). Phosphorylation of the autophagy receptor optineurin restricts salmonella growth. Science 333, 228-233.
63. Wirtz, S. , Neufert, C. , Weigmann, B. and Neurath, M. F. (2007). Chemically induced mouse models of intestinal inflammation. Nat. Protoc. 2, 541-546.
64. Xu, Y. , Hunt, N. H. and Bao, S. (2007). The correlation between proinflammatory cytokines, MAdCAM-1 and cellular infiltration in the inflamed colon from TNFalpha gene knockout mice. Immunol. Cell Biol. 85, 633-639.
65. Yan, D. , Wang, X. , Luo, L. , Cao, X. and Ge, B. (2012). Inhibition of TLR signaling by a bacterial protein containing immunoreceptor tyrosine-based inhibitory motifs. Nat. Immunol. 13, 1063-1071.