Increased susceptibility to dextran sulfate sodium-induced colitis in the endoplasmic reticulum stress transducer OASIS deficient mice

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Hino, Kenta ^a   Saito, Atsushi ^a   Asada, Rie ^a   Kanemoto, Soshi ^a   Imaizumi, Kazunori ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; DEXTRAN SULFATE; TAUROURSODEOXYCHOLIC ACID;

ADULT; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BODY WEIGHT; CELL INFILTRATION; COLITIS; CONTROLLED STUDY; DEXTRAN SULFATE SODIUM INDUCED COLITIS; ENDOPLASMIC RETICULUM STRESS; EPITHELIUM CELL; GOBLET CELL; INFLAMMATORY CELL; INTESTINE EPITHELIUM; INTESTINE MUCOSA; LARGE INTESTINE; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN FOLDING; PROTEIN SYNTHESIS; STRESS;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; CELLS, CULTURED; COLITIS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DEXTRAN SULFATE; DISEASE SUSCEPTIBILITY; ENDOPLASMIC RETICULUM STRESS; FEMALE; IMMUNOENZYME TECHNIQUES; IN SITU HYBRIDIZATION; INFLAMMATION; INTESTINES; LUCIFERASES; MALE; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84894628100     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088048     Document Type: Article

References (54)

1. Harding HP, Zhang Y, Ron D (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271-274. (Pubitemid 29051178)
2. Tirasophon W, Welihinda AA, Kaufman RJ (1998) A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells. Genes Dev 12: 1812-1824. (Pubitemid 28304334)
3. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, et al. (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415: 92-96. (Pubitemid 34062456)
4. Shen J, Chen X, Hendershot L, Prywes R (2002) ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 3: 99-111. (Pubitemid 34778399)
5. Ron D (2002) Translational control in the endoplasmic reticulum stress response. J Clin Invest 110: 1383-1388.
6. Kaufman RJ (2002) Orchestrating the unfolded protein response in health and disease. J Clin Invest 101: 1389-1398.
7. Asada R, Kanemoto S, Kondo S, Saito A, Imaizumi K (2011) The signaling from endoplasmic reticulum-resident bZIP transcription factors involved in diverse cellullar physiology. J Biochem 149: 507-518.
8. Honma Y, Kanazawa K, Mori T, Tanno Y, Tojo M, et al. (1999) Identification of a novel gene, OASIS, which encodes for a putative CREB/ATF family transcription factor in the long-term cultured astrocytes and gliotic tissue. Brain Res Mol Brain Res 69: 93-103. (Pubitemid 29238190)
9. Storlazzi CT, Mertens F, Nascimento A, Isaksson M, Wejde J, et al. (2003) Fusion of the FUS and BBF2H7 genes in low grade fibromyxoid sarcoma. Hum Mol Genet 12: 2349-2358. (Pubitemid 37160879)
10. Omori Y, Imai J, Watanabe M, Komatsu T, Suzuki Y, et al. (2001) CREB-H: a novel mammalian transcription factor belonging to the CREB/ATF family and functioning via the box-B element with a liver-specific expression. Nucleic Acids Res 29: 2154-2162. (Pubitemid 32472086)
11. Stelzer G, Don J (2002) Atce1: a novel mouse cyclic adenosine 39,59- monophosphate-responsive element-binding protein-like gene exclusively expressed in postmeiotic spermatids. Endocrinology 143: 1578-1588. (Pubitemid 34415871)
12. Lu R, Yang P, O'Hare P, Misra V (1997) Luman, a new member of the CREB/ATF family, binds to herpes simplex virus VP16-associated host cellular factor. Mol Cell Biol 17: 5117-5126. (Pubitemid 27357610)
13. Ko J, Jang SW, Kim YS, Kim IS, Sung HJ, et al. (2004) Human LZIP binds to CCR1 and differentially affects the chemotactic activities of CCR1-dependent chemokines. FASEBJ 18: 890-892.
14. Saito A, Hino SI, Murakami T, Kanemoto S, Kondo S, et al. (2009) Regulation of endoplasmic reticulum stress response by a BBF2H7-mediated Sec23a pathway is essential for chondrogenesis. Nat Cell Biol 11: 1197-1204.
15. Elveld-Trancikova D, Sanecka A, Van Hout-Kuijer MA, Looman MW, Hendriks IA, et al. (2010) DC-STAMP interacts with ER-resident transcription factor LUMAN which becomes activated during DC maturation. Mol Immunol 47: 1963-1973.
16. Zhang K, Shen X, Wu J, Sakaki K, Saunders T, et al. (2006) Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell 124: 587-599. (Pubitemid 43199443)
17. Vecchi C, Montosi G, Zhang K, Lamberti I, Duncan SA, et al. (2009) ER stress controls iron metabolism through induction of hepcidin. Science 325: 877-880.
18. Nagamori I, Yomogida K, Ikawa M, Okabe M, Yabuta N, et al. (2006) The testes-specific bZip type transcription factor Tisp40 plays a role in ER stress responses and chromatin packaging during spermiogenesis. Genes Cells 11: 1161-1171. (Pubitemid 44426206)
19. Adham IM, Eck TJ, Mierau K, Müller N, Sallam MA, et al. (2005) Reduction of spermatogenesis but not fertility in Creb3l4-deficient mice. Mol Cell Biol 25: 7657-7664. (Pubitemid 41170127)
20. Saito A, Kanemoto S, Kawasaki N, Asada R, Iwamoto H, et al. (2012) Unfolded protein response, activated by OASIS family transcription factors, promotes astrocyte differentiation. Nat Commun 3: 967.
21. Saito A, Kanemoto S, Zhang Y, Asada R, Hino K, et al. (in press) Chondrocyte Proliferation Regulated by Secreted Luminal Domain of ER Stress Transducer BBF2H7/CREB3L2. Mol Cell doi: 10.1016/j.molcel.2013.11.008. In press.
22. Kondo S, Murakami T, Tatsumi K, Ogata M, Kanemoto S, et al. (2005) OASIS, a CREB/ATF-family member, modulates UPR signalling in astrocytes. Nat Cell Biol 7: 186-194. (Pubitemid 40268134)
23. Murakami T, Kondo S, Ogata M, Kanemoto S, Saito A, et al. (2006) Cleavage of the membrane-bound transcription factor OASIS in response to endoplasmic reticulum stress. J Neurochem 96: 1090-1100.
24. Saito A, Hino SI, Murakami T, Kondo S, Imaizumi K (2007) A novel ER stress transducer, OASIS, expressed in astrocytes. Antioxid Redox Signal 9: 563-571. (Pubitemid 46598254)
25. Asada R, Saito A, Kawasaki N, Kanemoto S, Iwamoto H, et al. (2012) The endoplasmic reticulum stress transducer OASIS is involved in the terminal differentiation of goblet cells in the large intestine. J Biol Chem 287: 8144-8153.
26. Sartor RB (2008) Microbial influences in inflammatory bowel diseases. Gastroenterology 134: 577-594.
27. Van der Sluis M, De Koning BA, De Bruijn AC, Velcich A, Meijerink JP, et al. (2006) Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 131: 117-129. (Pubitemid 44015753)
28. Shkoda A, Ruiz PA, Daniel H, Kim SC, Rogler G, et al. (2007) Interleukin-10 blocked endoplasmic reticulum stress in intestinal epithelial cells: impact on chronic inflammation. Gastroenterology 132: 190-207. (Pubitemid 46108743)
29. Hu S, Ciancio MJ, Lahav M, Fujiya M, Lichitenstein L, et al. (2007) Translational inhibition of colonic epithelial heat shock proteins by IFN-gamma and TNF-alpha in intestinal inflammation. Gastroenterology 133: 1893-1904. (Pubitemid 350180816)
30. Heazlewood CK, Cook MC, Eri R, Price GR, Tauro SB, et al. (2008) Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis. PLoS Med 5: e54.
31. Kaser A, Lee AH, Franke A, Glickman JN, Zeissig S, et al. (2008) XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 134: 743-756.
32. McGovern DP, Gardet A, Torkvist L, Goyette P, Essers J, et al. (2010) Genome-wide association identifies multiple ulcerative colitis susceptibility loci. Nat Genet 42: 332-337.
33. Zheng W, Rosenstiel P, Huse K, Sina C, Valentonyte R, et al. (2006) Evaluation of AGR2 and AGR3 as candidate genes for inflammatory bowel disease. Genes Immun 7: 11-18.
34. Park SW, Zhen G, Verhaeghe C, Nakagami Y, Nguyenvu LT, et al. (2009) The protein disulfide isomerase AGR2 is essential for production of intestinal mucus. Proc Natl Acad Sci USA 106: 6950-6955.
35. Zhao F, Edwards R, Dizon D, Afrasiabi K, Mastroianni JR, et al. (2010) Disruption of Paneth and goblet cell homeostasis and increased endoplasmic reticulum stress in Agr2 2/2 mice. Dev Biol 338: 270-279.
36. Bertlotti A, Wang X, Novoa I, Jungreis R, Schlessinger K, et al. (2001) Increased sensitivity to dextran sodium sulfate colitis in IRE1beta-deficient mice. J Clin Invest 107: 585-593. (Pubitemid 32205179)
37. Cao SS, Zimmermann EM, Chuang BM, Song B, Nwokoye A, et al. (2013) The unfolded protein response and chemical chaperones reduce protein misfolding and colitis in mice. Gastroenterology 144: 989-1000.
38. Murakami T, Saito A, Hino SI, Kondo S, Kanemoto S, et al. (2009) Signalling mediated by the endoplasmic reticulum stress transducer OASIS is involved in bone formation. Nat Cell Biol 10: 1205-1211.
39. Berg DJ, Zhang J, Weinstock JV, Ismail HF, Earle KA, et al. (2002) Rapid development of colitis in NSAID-treated IL-10-deficient mice. Gastroenterology 123: 1527-1542. (Pubitemid 35231653)
40. Perse M, Cerar A (2012) Dextran Sodium Sulphate Colitis Mouse Model: Traps and Tricks. J Biomed Biotechnol 2012: 718617.
41. Kitajima S, Takuma S, Morimoto M (1999) Changes in colonic mucosal permeability in mouse colitis induced with dextran sulfate sodium. Exp Anim 48: 137-143. (Pubitemid 129558679)
42. Naito Y, Takagi T, Handa O, Ishikawa T, Nakagawa S, et al. (2003) Enhanced intestinal inflammation induced by dextran sulfate sodium in tumor necrosis factor-alpha deficient mice. J Gastroenterol Hepatol 18: 560-569. (Pubitemid 36645291)
43. Beck PL, Xavier R, Wong J, Ezedi I, Mashimo H, et al. (2004) Paradoxical roles of different nitric oxide synthase isoforms in colonic injury. Am J Physiol 286: G137-147. (Pubitemid 38055847)
44. Beck PL, Li Y, Wong J, Chen CW, Keenan CM, et al. (2007) Inducible nitric oxide synthase from bone marrow-derived cells plays a critical role in regulating colonic inflammation. Gastroenterology 132: 1778-1790. (Pubitemid 46677932)
45. Griendling KK, Sorescu D, Ushio-Fukai M (2000) NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 86: 494-501. (Pubitemid 30165039)
46. Xue X, Piao JH, Nakajima A, Sakon-Komazawa S, Kojima Y, et al. (2005) Tumor necrosis factor alpha (TNFalpha) induces the unfolded protein response (UPR) in a reactive oxygen species (ROS)-dependent fashion, and the UPR counteracts ROS accumulation by TNFalpha. J Biol Chem 280: 33917-33925. (Pubitemid 41443111)
47. Malhotra JD, Kaufman RJ (2007) Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal 9: 2277-2293. (Pubitemid 350059010)
48. Tsujino M, Hirata Y, Imai T, Kanno K, Eguchi S, et al. (1994) Induction of nitric oxide synthase gene by interleukin-1 beta in cultured rat cardiocytes. Circulation 90: 375-383. (Pubitemid 24203702)
49. Li WW, Alexandre S, Cao X, Lee AS (1993) Transactivation of the grp78 promoter by Ca2+ depletion. A comparative analysis with A23187 and the endoplasmic reticulum Ca(2 +)-ATPase inhibitor thapsigargin. J Biol Chem 268: 12003-12009. (Pubitemid 23168163)
50. Hotamisligil GS (2010) Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140: 900-917.
51. Deng J, Lu PD, Zhang Y, Scheuner D, Kaufman RJ, et al. (2004) Translational repression mediates activation of nuclear factor kappa B by phosphorylated translation initiation factor 2. Mol Cell Biol 24: 10161-10168. (Pubitemid 39507856)
52. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, et al. (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287: 664-666. (Pubitemid 30070916)
53. Hu P, Han Z, Couvillon AD, Kaufman RJ, Exton JH (2006) Autocrine tumor necrosis factor alpha links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1alpha-mediated NF-kappaB activation and down-regulation of TRAF2 expression. Mol Cell Biol 26: 3071-3084.
54. Yamazaki H, Hiramatsu N, Hayakawa K, Tagawa Y, Okamura M, et al. (2009) Activation of the Akt-NF-kappaB pathway by subtilase cytotoxin through the ATF6 branch of the unfolded protein response. J Immunol 183: 1480-1487.