XBP1-Independent UPR Pathways Suppress C/EBP-β Mediated Chondrocyte Differentiation in ER-Stress Related Skeletal Disease

PLoS Genetics

Volumn 11, Issue 9, 2015, Pages

  Cameron, Trevor L ^a   Bell, Katrina M ^a   Gresshoff, Irma L ^a   Sampurno, Lisa ^a   Mullan, Lorna ^b   Ermann, Joerg ^c   Glimcher, Laurie H ^d   Boot Handford, Raymond P ^b   Bateman, John F ^a,e  

^a MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

^e UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA; TRANSCRIPTOME; X BOX BINDING PROTEIN 1; DNA BINDING PROTEIN; REGULATORY FACTOR X TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; XBP1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARTILAGE CELL; CELL DIFFERENTIATION; CHONDRODYSPLASIA; CONTROLLED STUDY; DISEASE SEVERITY; ENDOPLASMIC RETICULUM STRESS; METAPHYSEAL CHONDRODYSPLASIA; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; UNFOLDED PROTEIN RESPONSE; ANIMAL; ANTAGONISTS AND INHIBITORS; BONE DISEASE; CHONDROCYTE; GENE EXPRESSION PROFILING; GENETICS; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; BONE DISEASES; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELL DIFFERENTIATION; CHONDROCYTES; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION PROFILING; MICE; MICE, TRANSGENIC; REGULATORY FACTOR X TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS; UNFOLDED PROTEIN RESPONSE; X-BOX BINDING PROTEIN 1;

EID: 84943541584     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005505     Document Type: Article

References (40)

1. Mackie EJ, Ahmed YA, Tatarczuch L, Chen KS, Mirams M, (2008) Endochondral ossification: how cartilage is converted into bone in the developing skeleton. Int J Biochem Cell Biol 40: 46–62. 17659995
2. Asada R, Kanemoto S, Kondo S, Saito A, Imaizumi K, (2011) The signalling from endoplasmic reticulum-resident bZIP transcription factors involved in diverse cellular physiology. J Biochem 149: 507–518. doi: 10.1093/jb/mvr041 21454302
3. Hetz C, (2012) The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 13: 89–102. doi: 10.1038/nrm3270 22251901
4. Ron D, Walter P, (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8: 519–529. 17565364
5. Schroder M, Kaufman RJ, (2005) The mammalian unfolded protein response. Annu Rev Biochem 74: 739–789. 15952902
6. Haze K, Yoshida H, Yanagi H, Yura T, Mori K, (1999) Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell 10: 3787–3799. 10564271
7. Harding HP, Zhang Y, Ron D, (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271–274. 9930704
8. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, et al. (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6: 1099–1108. 11106749
9. Lu PD, Harding HP, Ron D, (2004) Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J Cell Biol 167: 27–33. 15479734
10. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K, (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107: 881–891. 11779464
11. Rajpar MH, McDermott B, Kung L, Eardley R, Knowles L, et al. (2009) Targeted induction of endoplasmic reticulum stress induces cartilage pathology. PLoS Genet 5: e1000691. doi: 10.1371/journal.pgen.1000691 19834559
12. Cameron TL, Bell KM, Tatarczuch L, Mackie EJ, Rajpar MH, et al. (2011) Transcriptional profiling of chondrodysplasia growth plate cartilage reveals adaptive ER-stress networks that allow survival but disrupt hypertrophy. PLoS One 6: e24600. doi: 10.1371/journal.pone.0024600 21935428
13. He Y, Sun S, Sha H, Liu Z, Yang L, et al. (2010) Emerging roles for XBP1, a sUPeR transcription factor. Gene Expr 15: 13–25. 21061914
14. Cameron TL, Gresshoff IL, Bell KM, Pirog KA, Sampurno L, et al. (2015) Cartilage-Specific Ablation of XBP1 Signaling in Mouse Results in a Chondrodysplasia Characterized by Reduced Chondrocyte Proliferation and Delayed Cartilage Maturation and Mineralization. Osteoarthritis Cartilage 23: 661–670. doi: 10.1016/j.joca.2015.01.001 25600960
15. Oyadomari S, Mori M, (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11: 381–389. 14685163
16. Hirata M, Kugimiya F, Fukai A, Ohba S, Kawamura N, et al. (2009) C/EBPbeta Promotes transition from proliferation to hypertrophic differentiation of chondrocytes through transactivation of p57. PLoS One 4: e4543. doi: 10.1371/journal.pone.0004543 19229324
17. Hirata M, Kugimiya F, Fukai A, Saito T, Yano F, et al. (2012) C/EBPbeta and RUNX2 cooperate to degrade cartilage with MMP-13 as the target and HIF-2alpha as the inducer in chondrocytes. Hum Mol Genet 21: 1111–1123. doi: 10.1093/hmg/ddr540 22095691
18. Ushijima T, Okazaki K, Tsushima H, Iwamoto Y, (2014) CCAAT/enhancer-binding protein beta regulates the repression of type II collagen expression during the differentiation from proliferative to hypertrophic chondrocytes. J Biol Chem 289: 2852–2863. doi: 10.1074/jbc.M113.492843 24344131
19. Lee AH, Iwakoshi NN, Glimcher LH, (2003) XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 23: 7448–7459. 14559994
20. Tsuchimochi K, Otero M, Dragomir CL, Plumb DA, Zerbini LF, et al. (2010) GADD45beta enhances Col10a1 transcription via the MTK1/MKK3/6/p38 axis and activation of C/EBPbeta-TAD4 in terminally differentiating chondrocytes. J Biol Chem 285: 8395–8407. doi: 10.1074/jbc.M109.038638 20048163
21. Ijiri K, Zerbini LF, Peng H, Correa RG, Lu B, et al. (2005) A novel role for GADD45beta as a mediator of MMP-13 gene expression during chondrocyte terminal differentiation. J Biol Chem 280: 38544–38555. 16144844
22. Ron D, Habener JF, (1992) CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes Dev 6: 439–453. 1547942
23. Wu J, Rutkowski DT, Dubois M, Swathirajan J, Saunders T, et al. (2007) ATF6alpha optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev Cell 13: 351–364. 17765679
24. Okada T, Yoshida H, Akazawa R, Negishi M, Mori K, (2002) Distinct roles of activating transcription factor 6 (ATF6) and double-stranded RNA-activated protein kinase-like endoplasmic reticulum kinase (PERK) in transcription during the mammalian unfolded protein response. Biochem J 366: 585–594. 12014989
25. Maurel M, Chevet E, Tavernier J, Gerlo S, (2014) Getting RIDD of RNA: IRE1 in cell fate regulation. Trends Biochem Sci 39: 245–254. doi: 10.1016/j.tibs.2014.02.008 24657016
26. Chen Y, Brandizzi F, (2013) IRE1: ER stress sensor and cell fate executor. Trends Cell Biol 23: 547–555. doi: 10.1016/j.tcb.2013.06.005 23880584
27. Tsang KY, Chan D, Cheslett D, Chan WC, So CL, et al. (2007) Surviving endoplasmic reticulum stress is coupled to altered chondrocyte differentiation and function. PLoS Biol 5: e44. 17298185
28. Ho MS, Tsang KY, Lo RL, Susic M, Makitie O, et al. (2007) COL10A1 nonsense and frame-shift mutations have a gain-of-function effect on the growth plate in human and mouse metaphyseal chondrodysplasia type Schmid. Hum Mol Genet 16: 1201–1215. 17403716
29. Kung LH, Rajpar MH, Briggs MD, Boot-Handford RP, (2012) Hypertrophic chondrocytes have a limited capacity to cope with increases in endoplasmic reticulum stress without triggering the unfolded protein response. J Histochem Cytochem 60: 734–748. 22859705
30. Adachi Y, Yamamoto K, Okada T, Yoshida H, Harada A, et al. (2008) ATF6 is a transcription factor specializing in the regulation of quality control proteins in the endoplasmic reticulum. Cell Struct Funct 33: 75–89. 18360008
31. Han J, Back SH, Hur J, Lin YH, Gildersleeve R, et al. (2013) ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat Cell Biol 15: 481–490. doi: 10.1038/ncb2738 23624402
32. Arensdorf AM, Rutkowski DT, (2013) Endoplasmic reticulum stress impairs IL-4/IL-13 signaling through C/EBPbeta-mediated transcriptional suppression. J Cell Sci 126: 4026–4036. doi: 10.1242/jcs.130757 23813955
33. Chikka MR, McCabe DD, Tyra HM, Rutkowski DT, (2013) C/EBP homologous protein (CHOP) contributes to suppression of metabolic genes during endoplasmic reticulum stress in the liver. J Biol Chem 288: 4405–4415. doi: 10.1074/jbc.M112.432344 23281479
34. Rutkowski DT, Wu J, Back SH, Callaghan MU, Ferris SP, et al. (2008) UPR pathways combine to prevent hepatic steatosis caused by ER stress-mediated suppression of transcriptional master regulators. Dev Cell 15: 829–840. doi: 10.1016/j.devcel.2008.10.015 19081072
35. Zhang P, Liegeois NJ, Wong C, Finegold M, Hou H, et al. (1997) Altered cell differentiation and proliferation in mice lacking p57KIP2 indicates a role in Beckwith-Wiedemann syndrome. Nature 387: 151–158. 9144284
36. Inada M, Wang Y, Byrne MH, Rahman MU, Miyaura C, et al. (2004) Critical roles for collagenase-3 (Mmp13) in development of growth plate cartilage and in endochondral ossification. Proc Natl Acad Sci U S A 101: 17192–17197. 15563592
37. Woehlbier U, Hetz C, (2011) Modulating stress responses by the UPRosome: a matter of life and death. Trends Biochem Sci 36: 329–337. doi: 10.1016/j.tibs.2011.03.001 21482118
38. Smyth GK, Gentleman R, Carey V., Dudoit S., Irizarry R., Huber W., (2005) Limma: linear models for microarray data. In: Bioinformatics and Computational Biology Solutions using R and Bioconductor: Springer, New York. pp. 397–420.
39. Dunning M, Lynch A., Eldridge M, . (2014) illuminaMousev2.db: Illumina MouseWG6v2 annotation data (chip illuminaMousev2). R package version 1.22.1.
40. Wu D, Lim E, Vaillant F, Asselin-Labat ML, Visvader JE, et al. (2010) ROAST: rotation gene set tests for complex microarray experiments. Bioinformatics 26: 2176–2182. doi: 10.1093/bioinformatics/btq401 20610611