Type I interferons control proliferation and function of the intestinal epithelium

Molecular and Cellular Biology

Volumn 36, Issue 7, 2016, Pages 1124-1135

  Katlinskaya, Yuliya V ^a   Katlinski, Kanstantsin V ^a   Lasri, Audrey ^b   Li, Ning ^a   Beiting, Daniel P ^a   Durham, Amy C ^a   Yang, Ting ^c   Pikarsky, Eli ^d   Lengner, Christopher J ^a   Johnson, F Brad ^c   Ben Neriah, Yinon ^b   Fuchs, Serge Y ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ASCL2 PROTEIN; AXIN2 PROTEIN; BETA CATENIN; BETA GALACTOSIDASE; BETA INTERFERON; CASEIN KINASE IALPHA; CASPASE 3; CND1 PROTEIN; DEXTRAN; HERMES ANTIGEN; HISTONE H2AX; IFNAR1 PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 7; MESSENGER RNA; PROTEIN; PROTEIN P53; PROTEIN ZO1; TAMOXIFEN; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG; UVOMORULIN; ALPHA BETA INTERFERON RECEPTOR; IFNAR1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIVISION; CELL FUNCTION; CELL INFILTRATION; CELL PROLIFERATION; CELL VIABILITY; COLON POLYPOSIS; COMPARATIVE STUDY; CONTROLLED STUDY; DNA DAMAGE; EX VIVO STUDY; GENE EXPRESSION PROFILING; GENOTYPE; IMMUNOFLUORESCENCE TEST; INFLAMMATION; INTESTINE EPITHELIUM CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; TRANSCRIPTION INITIATION; UBIQUITINATION; UPREGULATION; WNT SIGNALING PATHWAY; ANIMAL; C57BL MOUSE; CYTOLOGY; GENETICS; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CASEIN KINASE IALPHA; CELL PROLIFERATION; DNA DAMAGE; INTERFERON TYPE I; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTOR, INTERFERON ALPHA-BETA; SIGNAL TRANSDUCTION; UBIQUITINATION;

EID: 84962162241     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00988-15     Document Type: Article

References (55)

1. Heath JP. 1996. Epithelial cell migration in the intestine. Cell Biol Int 20:139-146. http://dx.doi.org/10.1006/cbir.1996.0018.
2. Clevers H. 2006. Wnt/beta-catenin signaling in development and disease. Cell 127:469-480. http://dx.doi.org/10.1016/j.cell.2006.10.018.
3. Pinto D, Clevers H. 2005. Wnt control of stem cells and differentiation in the intestinal epithelium. Exp Cell Res 306:357-363. http://dx.doi.org/10.1016/j.yexcr.2005.02.022.
4. Grivennikov SI, Greten FR, Karin M. 2010. Immunity, inflammation, and cancer. Cell 140:883-899. http://dx.doi.org/10.1016/j.cell.2010.01.025.
5. Terzic J, Grivennikov S, Karin E, Karin M. 2010. Inflammation and colon cancer. Gastroenterology 138:2101-2114. http://dx.doi.org/10.1053/j.gastro.2010.01.058.
6. Abt MC, Osborne LC, Monticelli LA, Doering TA, Alenghat T, Sonnenberg GF, Paley MA, Antenus M, Williams KL, Erikson J, Wherry EJ, Artis D. 2012. Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity 37:158-170. http://dx.doi.org/10.1016/j.immuni.2012.04.011.
7. McAleer JP, Kolls JK. 2012. Maintaining poise: commensal microbiota calibrate interferon responses. Immunity 37:10-12. http://dx.doi.org/10.1016/j.immuni.2012.07.001.
8. Santaolalla R, Abreu MT. 2012. Innate immunity in the small intestine. Curr Opin Gastroenterol 28:124-129. http://dx.doi.org/10.1097/MOG.0b013e3283506559.
9. Santos RL, Raffatellu M, Bevins CL, Adams LG, Tukel C, Tsolis RM, Baumler AJ. 2009. Life in the inflamed intestine, Salmonella style. Trends Microbiol 17:498-506. http://dx.doi.org/10.1016/j.tim.2009.08.008.
10. Platanias LC. 2005. Mechanisms of type-I-and type-II-interferonmediated signalling. Nat Rev Immunol 5:375-386. http://dx.doi.org/10.1038/nri1604.
11. Kole A, He J, Rivollier A, Silveira DD, Kitamura K, Maloy KJ, Kelsall BL. 2013. Type I IFNs regulate effector and regulatory T cell accumulation and anti-inflammatory cytokine production during T cellmediated colitis. J Immunol 191:2771-2779. http://dx.doi.org/10.4049/jimmunol.1301093.
12. Lienenklaus S, Cornitescu M, Zietara N, Lyszkiewicz M, Gekara N, Jablonska J, Edenhofer F, Rajewsky K, Bruder D, Hafner M, Staeheli P, Weiss S. 2009. Novel reporter mouse reveals constitutive and inflammatory expression of IFN-beta in vivo. J Immunol 183:3229-3236. http://dx.doi.org/10.4049/jimmunol.0804277.
13. Fuchs SY. 2013. Hope and fear for interferon: the receptor-centric outlook on the future of interferon therapy. J Interferon Cytokine Res 33:211-225. http://dx.doi.org/10.1089/jir.2012.0117.
14. Piehler J, Thomas C, Garcia KC, Schreiber G. 2012. Structural and dynamic determinants of type I interferon receptor assembly and their functional interpretation. Immunol Rev 250:317-334. http://dx.doi.org/10.1111/imr.12001.
15. Uze G, Schreiber G, Piehler J, Pellegrini S. 2007. The receptor of the type I interferon family. Curr Top Microbiol Immunol 316:71-95.
16. Tschurtschenthaler M, Wang J, Fricke C, Fritz TM, Niederreiter L, Adolph TE, Sarcevic E, Kunzel S, Offner FA, Kalinke U, Baines JF, Tilg H, Kaser A. 2014. Type I interferon signalling in the intestinal epithelium affects Paneth cells, microbial ecology and epithelial regeneration. Gut 63:1921-1931. http://dx.doi.org/10.1136/gutjnl-2013-305863.
17. Rauch I, Hainzl E, Rosebrock F, Heider S, Schwab C, Berry D, Stoiber D, Wagner M, Schleper C, Loy A, Urich T, Muller M, Strobl B, Kenner L, Decker T. 2014. Type I interferons have opposing effects during the emergence and recovery phases of colitis. Eur J Immunol 44:2749-2760. http://dx.doi.org/10.1002/eji.201344401.
18. Sun L, Miyoshi H, Origanti S, Nice TJ, Barger AC, Manieri NA, Fogel LA, French AR, Piwnica-Worms D, Piwnica-Worms H, Virgin HW, Lenschow DJ, Stappenbeck TS. 2015. Type I interferons link viral infection to enhanced epithelial turnover and repair. Cell Host Microbe 17:85-97. http://dx.doi.org/10.1016/j.chom.2014.11.004.
19. Levin D, Harari D, Schreiber G. 2011. Stochastic receptor expression determines cell fate upon interferon treatment. Mol Cell Biol 31:3252-3266 http://dx.doi.org/10.1128/MCB.05251-11.
20. Kumar KG, Barriere H, Carbone CJ, Liu J, Swaminathan G, Xu P, Li Y, Baker DP, Peng J, Lukacs GL, Fuchs SY. 2007. Site-specific ubiquitination exposes a linear motif to promote interferon-alpha receptor endocytosis. J Cell Biol 179:935-950. http://dx.doi.org/10.1083/jcb.200706034.
21. Kumar KG, Krolewski JJ, Fuchs SY. 2004. Phosphorylation and specific ubiquitin acceptor sites are required for ubiquitination and degradation of the IFNAR1 subunit of type I interferon receptor. J Biol Chem 279:46614-46620 http://dx.doi.org/10.1074/jbc.M407082200.
22. Kumar KG, Tang W, Ravindranath AK, Clark WA, Croze E, Fuchs SY.2003 SCF(HOS) ubiquitin ligase mediates the ligand-induced downregulation of the interferon-alpha receptor. EMBO J 22:5480-5490. http://dx.doi.org/10.1093/emboj/cdg524.
23. Liu J, Plotnikov A, Banerjee A, Suresh Kumar KG, Ragimbeau J, Marijanovic Z, Baker DP, Pellegrini S, Fuchs SY. 2008. Ligandindependent pathway that controls stability of interferon alpha receptor. Biochem Biophys Res Commun 367:388-393. http://dx.doi.org/10.1016/j.bbrc.2007.12.137.
24. Zheng H, Qian J, Baker DP, Fuchs SY. 2011. Tyrosine phosphorylation of protein kinase D2 mediates ligand-inducible elimination of the type 1 interferon receptor. J Biol Chem 286:35733-35741. http://dx.doi.org/10.1074/jbc.M111.263608.
25. Zheng H, Qian J, Varghese B, Baker DP, Fuchs S. 2011. Ligandstimulated downregulation of the alpha interferon receptor: role of protein kinase D2. Mol Cell Biol 31:710-720. http://dx.doi.org/10.1128/MCB.01154-10.
26. Liu J, HuangFu WC, Kumar KG, Qian J, Casey JP, Hamanaka RB, Grigoriadou C, Aldabe R, Diehl JA, Fuchs SY. 2009. Virus-induced unfolded protein response attenuates antiviral defenses via phosphorylation-dependent degradation of the type I interferon receptor. Cell Host Microbe 5:72-83. http://dx.doi.org/10.1016/j.chom.2008.11.008.
27. Huangfu WC, Qian J, Liu C, Liu J, Lokshin AE, Baker DP, Rui H, Fuchs SY. 2012. Inflammatory signaling compromises cell responses to interferon alpha. Oncogene 31:161-172. http://dx.doi.org/10.1038/onc.2011.221.
28. Bhattacharya S, Katlinski KV, Reichert M, Takano S, Brice A, Zhao B, Yu Q, Zheng H, Carbone CJ, Katlinskaya YV, Leu NA, McCorkell KA, Srinivasan S, Girondo M, Rui H, May MJ, Avadhani NG, Rustgi AK, Fuchs SY. 2014. Triggering ubiquitination of IFNAR1 protects tissues from inflammatory injury. EMBO Mol Med 6:384-397. http://dx.doi.org/10.1002/emmm.201303236.
29. Liu J, Carvalho LP, Bhattacharya S, Carbone CJ, Kumar KG, Leu NA, Yau PM, Donald RG, Weiss MJ, Baker DP, McLaughlin KJ, Scott P, Fuchs SY. 2009. Mammalian casein kinase 1alpha and its leishmanial ortholog regulate stability of IFNAR1 and type I interferon signaling. Mol Cell Biol 29:6401-6412. http://dx.doi.org/10.1128/MCB.00478-09.
30. Amit S, Hatzubai A, Birman Y, Andersen JS, Ben-Shushan E, Mann M, Ben-Neriah Y, Alkalay I. 2002. Axin-mediated CKI phosphorylation of beta-catenin at Ser 45: a molecular switch for the Wnt pathway. Genes Dev 16:1066-1076. http://dx.doi.org/10.1101/gad.230302.
31. Liu C, Li Y, Semenov M, Han C, Baeg GH, Tan Y, Zhang Z, Lin X, He X. 2002. Control of beta-catenin phosphorylation/degradation by a dualkinase mechanism. Cell 108:837-847. http://dx.doi.org/10.1016/S0092-8674(02)00685-2.
32. Fuchs SY, Chen A, Xiong Y, Pan ZQ, Ronai Z. 1999. HOS, a human homolog of Slimb, forms an SCF complex with Skp1 and Cullin1 and targets the phosphorylation-dependent degradation of IkappaB and beta-catenin. Oncogene 18:2039-2046. http://dx.doi.org/10.1038/sj.onc.1202760.
33. Hart M, Concordet JP, Lassot I, Albert I, del los Santos R, Durand H, Perret C, Rubinfeld B, Margottin F, Benarous R, Polakis P. 1999. The F-box protein beta-TrCP associates with phosphorylated beta-catenin and regulates its activity in the cell. Curr Biol 9:207-210. http://dx.doi.org/10.1016/S0960-9822(99)80091-8.
34. Kitagawa M, Hatakeyama S, Shirane M, Matsumoto M, Ishida N, Hattori K, Nakamichi I, Kikuchi A, Nakayama K, Nakayama K. 1999. An F-box protein, FWD1, mediates ubiquitin-dependent proteolysis of beta-catenin.EMBOJ 18:2401-2410. http://dx.doi.org/10.1093/emboj/18.9.2401.
35. Latres E, Chiaur DS, Pagano M. 1999. The human F box protein beta-Trcp associates with the Cul1/Skp1 complex and regulates the stability of beta-catenin. Oncogene 18:849-854. http://dx.doi.org/10.1038/sj.onc.1202653.
36. Winston JT, Strack P, Beer-Romero P, Chu CY, Elledge SJ, Harper JW.1999 The SCFbeta-TRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IkappaBalpha and betacatenin and stimulates IkappaBalpha ubiquitination in vitro. Genes Dev 13:270-283. http://dx.doi.org/10.1101/gad.13.3.270.
37. Elyada E, Pribluda A, Goldstein RE, Morgenstern Y, Brachya G, Cojocaru G, Snir-Alkalay I, Burstain I, Haffner-Krausz R, Jung S, Wiener Z, Alitalo K, Oren M, Pikarsky E, Ben-Neriah Y. 2011. CKIalpha ablation highlights a critical role for p53 in invasiveness control. Nature 470:409-413. http://dx.doi.org/10.1038/nature09673.
38. Pribluda A, Elyada E, Wiener Z, Hamza H, Goldstein RE, Biton M, Burstain I, Morgenstern Y, Brachya G, Billauer H, Biton S, Snir-Alkalay I, Vucic D, Schlereth K, Mernberger M, Stiewe T, Oren M, Alitalo K, Pikarsky E, Ben-Neriah Y. 2013. A senescence-inflammatory switch from cancer-inhibitory to cancer-promoting mechanism. Cancer Cell 24:242-256. http://dx.doi.org/10.1016/j.ccr.2013.06.005.
39. Greten FR, Eckmann L, Greten TF, Park JM, Li ZW, Egan LJ, Kagnoff MF, Karin M. 2004. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 118:285-296. http://dx.doi.org/10.1016/j.cell.2004.07.013.
40. Katlinskaya YV, Carbone CJ, Yu Q, Fuchs SY. 2015. Type 1 interferons contribute to the clearance of senescent cell. Cancer Biol Ther 16:1214-1219 http://dx.doi.org/10.1080/15384047.2015.1056419.
41. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, van Es JH, Abo A, Kujala P, Peters PJ, Clevers H. 2009. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459:262-265. http://dx.doi.org/10.1038/nature07935.
42. Yu Q, Carbone CJ, Katlinskaya YV, Zheng H, Zheng K, Luo M, Wang PJ, Greenberg RA, Fuchs SY. 2015. Type I interferon controls propagation of long interspersed element-1. J Biol Chem 290:10191-10199. http://dx.doi.org/10.1074/jbc.M114.612374.
43. Yu Q, Katlinskaya YV, Carbone CJ, Zhao B, Katlinski KV, Zheng H, Guha M, Li N, Chen Q, Yang T, Lengner CJ, Greenberg RA, Johnson FB, Fuchs SY. 2015. DNA-damage-induced type I interferon promotes senescence and inhibits stem cell function. Cell Rep 11:785-797. http://dx.doi.org/10.1016/j.celrep.2015.03.069.
44. Moiseeva O, Mallette FA, Mukhopadhyay UK, Moores A, Ferbeyre G.2006 DNA damage signaling and p53-dependent senescence after prolonged beta-interferon stimulation. Mol Biol Cell 17:1583-1592. http://dx.doi.org/10.1091/mbc.E05-09-0858.
45. 2-terminal truncated beta-catenin on mouse intestinal epithelial homeostasis. J Cell Biol 141:765-777. http://dx.doi.org/10.1083/jcb.141.3.765.
46. Sansom OJ, Reed KR, Hayes AJ, Ireland H, Brinkmann H, Newton IP, Batlle E, Simon-Assmann P, Clevers H, Nathke IS, Clarke AR, Winton DJ. 2004. Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev 18:1385-1390. http://dx.doi.org/10.1101/gad.287404.
47. Mangan NE, Fung KY. 2012. Type I interferons in regulation of mucosal immunity. Immunol Cell Biol 90:510-519. http://dx.doi.org/10.1038/icb.2012.13.
48. Knippschild U, Gocht A, Wolff S, Huber N, Lohler J, Stoter M. 2005. The casein kinase 1 family: participation in multiple cellular processes in eukaryotes. Cell Signal 17:675-689. http://dx.doi.org/10.1016/j.cellsig.2004.12.011.
49. Takaoka A, Hayakawa S, Yanai H, Stoiber D, Negishi H, Kikuchi H, Sasaki S, Imai K, Shibue T, Honda K, Taniguchi T. 2003. Integration of interferon-alpha/beta signalling to p53 responses in tumour suppression and antiviral defence. Nature 424:516-523. http://dx.doi.org/10.1038/nature01850.
50. Preitner N, Quan J, Nowakowski DW, Hancock ML, Shi J, Tcherkezian J, Young-Pearse TL, Flanagan JG. 2014. APC is an RNA-binding protein, and its interactome provides a link to neural development and microtubule assembly. Cell 158:368-382. http://dx.doi.org/10.1016/j.cell.2014.05.042.
51. Valvezan AJ, Huang J, Lengner CJ, Pack M, Klein PS. 2014. Oncogenic mutations in adenomatous polyposis coli (Apc) activate mechanistic target of rapamycin complex 1 (mTORC1) in mice and zebrafish. Dis Model Mech 7:63-71. http://dx.doi.org/10.1242/dmm.012625.
52. Wang S, Li N, Yousefi M, Nakauka-Ddamba A, Li F, Parada K, Rao S, Minuesa G, Katz Y, Gregory BD, Kharas MG, Yu Z, Lengner CJ. 2015. Transformation of the intestinal epithelium by the MSI2 RNA-binding protein. Nat Commun 6:6517. http://dx.doi.org/10.1038/ncomms7517.
53. Katakura K, Lee J, Rachmilewitz D, Li G, Eckmann L, Raz E. 2005. Toll-like receptor 9-induced type I IFN protects mice from experimental colitis. J Clin Invest 115:695-702. http://dx.doi.org/10.1172/JCI22996.
54. Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY, Lee JC, Schumm LP, Sharma Y, Anderson CA, Essers J, Mitrovic M, Ning K, Cleynen I, Theatre E, Spain SL, Raychaudhuri S, Goyette P, Wei Z, Abraham C, Achkar JP, Ahmad T, Amininejad L, Ananthakrishnan AN, Andersen V, Andrews JM, Baidoo L, Balschun T, Bampton PA, Bitton A, Boucher G, Brand S, Buning C, Cohain A, Cichon S, D'Amato M, De Jong D, Devaney KL, Dubinsky M, Edwards C, Ellinghaus D, Ferguson LR, Franchimont D, Fransen K, Gearry R, Georges M, Gieger C, Glas J, Haritunians T, Hart A, et al. 2012. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491:119-124. http://dx.doi.org/10.1038/nature11582.
55. Gonzalez-Navajas JM, Lee J, David M, Raz E. 2012. Immunomodulatory functions of type I interferons. Nat Rev Immunol 12:125-135. http://dx.doi.org/10.1038/nri3133.