The unfolded protein response and its relevance to connective tissue diseases

Cell and Tissue Research

Volumn 339, Issue 1, 2010, Pages 197-211

  Boot Handford, Raymond P ^a   Briggs, Michael D ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Cartilage; Chondrodysplasia; Connective tissue diseases; Endoplasmic reticulum stress; Unfolded protein response

Indexed keywords

COLLAGEN TYPE 4; FIBRILLAR COLLAGEN; MATRILIN 3;

BONE DEVELOPMENT; CHONDRODYSPLASIA; CONNECTIVE TISSUE DISEASE; ENDOPLASMIC RETICULUM STRESS; GENE MUTATION; HUMAN; MISSENSE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; REVIEW;

ACTIVATING TRANSCRIPTION FACTOR 6; ANIMALS; APOPTOSIS; CHONDROCYTES; CONNECTIVE TISSUE DISEASES; EIF-2 KINASE; ENDOPLASMIC RETICULUM; ENDORIBONUCLEASES; FIBROBLASTS; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; MEMBRANE PROTEINS; OSTEOBLASTS; PROTEIN-SERINE-THREONINE KINASES; UNFOLDED PROTEIN RESPONSE;

EID: 72449160579     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-009-0877-8     Document Type: Review

References (108)

1. Y Adachi K Yamamoto T Okada H Yoshida A Harada K Mori 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
2. T Anelli R Sitia 2008 Protein quality control in the early secretory pathway EMBO J 27 315 327 1:CAS:528:DC%2BD1cXhtVKktL4%3D 18216874
3. JF Bateman R Wilson S Freddi SR Lamandé R Savarirayan 2005 Mutations of COL10A1 in Schmid metaphyseal chondrodysplasia Hum Mutat 25 525 534 1:CAS:528:DC%2BD2MXpslSksb8%3D 15880705
4. Bateman JF, Boot-Handford RP, Lamandé SR (2009) Genetic diseases of connective tissues: cellular and extracellular effects of ECM mutations. Nat Genet 10:173-183
5. S Bernales FR Papa P Walter 2006 Intracellular signaling by the unfolded protein response Annu Rev Cell Dev Biol 22 487 508 1:CAS:528:DC%2BD28Xht1yjs7jK 16822172
6. S Bernales S Schuck P Walter 2007 ER-phagy: selective autophagy of the endoplasmic reticulum Autophagy 3 285 287 17351330
7. A Bertolotti Y Zhang LM Hendershot HP Harding D Ron 2000 Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response Nat Cell Biol 2 326 332 1:CAS:528:DC%2BD3cXlt1Sls7o%3D 10854322
8. A Bertolotti X Wang I Novoa R Jungreis K Schlessinger JH Cho AB West D Ron 2001 Increased sensitivity to dextran sodium sulfate colitis in IRE1 β-deficient mice J Clin Invest 107 585 593 1:CAS:528:DC%2BD3MXhs12ns7k%3D 11238559
9. O Bogin M Kvansakul E Rom J Singer A Yayon E Hohenester 2000 Insight into Schmid metaphyseal chondrodysplasia from the crystal structure of the collagen X NC1 domain trimer Structure 10 165 173
10. MD Briggs KL Chapman 2002 Pseudoachondroplasia and multiple epiphyseal dysplasia: mutation review, molecular interactions, and genotype to phenotype correlations Hum Mutat 19 465 478 1:CAS:528:DC%2BD38Xkt1eiu78%3D 11968079
11. MD Briggs SM Hoffman LM King AS Olsen H Mohrenweiser JG Leroy GR Mortier DL Rimoin RS Lachman ES Gaines JA Cekleniak RG Knowlton DH Cohn 1995 Pseudoachondroplasia and multiple epiphyseal dysplasia due to mutations in the cartilage oligomeric matrix protein gene Nat Genet 10 330 336 1:CAS:528:DyaK2MXms1Kjur8%3D 7670472
12. JL Brodsky 2007 The protective and destructive roles played by molecular chaperones during ERAD (endoplasmic-reticulum-associated degradation) Biochem J 404 352 362
13. B Bukau J Weissman A Horwich 2006 Molecular chaperones and protein folding Cell 125 443 451 1:CAS:528:DC%2BD28XkslCjtLw%3D 16678092
14. D Chan YM Weng AM Hocking S Golub DJ McQuillan JF Bateman 1996 Site-directed mutagenesis of human type X collagen. Expression of alpha1(X) NC1, NC2, and helical mutations in vitro and in transfected cells J Biol Chem 271 13566 13572 1:CAS:528:DyaK28XjsVKqurw%3D 8662807
15. D Chan MS Ho KS Cheah 2001 Aberrant signal peptide cleavage of collagen X in Schmid metaphyseal chondrodysplasia. Implications for the molecular basis of the disease J Biol Chem 276 7992 7997 1:CAS:528:DC%2BD3MXitFKgsr4%3D 11115494
16. KL Chapman GR Mortier K Chapman J Loughlin ME Grant MD Briggs 2001 Mutations in the region encoding the von Willebrand factor A domain of matrilin-3 are associated with multiple epiphyseal dysplasia Nat Genet 28 393 396 1:CAS:528:DC%2BD3MXlslelu7w%3D 11479597
17. SD Chessler PH Byers 1993 BiP binds type I procollagen proα chains with mutations in the carboxyl-terminal propeptide synthesized by cells from patients with osteogenesis imperfecta J Biol Chem 268 18226 18233 1:CAS:528:DyaK3sXlsFOmtLY%3D 8349698
18. SL Cotterill GC Jackson MP Leighton R Wagener O Makitie WG Cole MD Briggs 2005 Multiple epiphyseal dysplasia mutations in MATN3 cause misfolding of the A-domain and prevent secretion of mutant matrilin-3 Hum Mutat 26 557 565 1:CAS:528:DC%2BD28Xjs1Cqtg%3D%3D 16287128
19. JJ Credle JS Finer-Moore FR Papa RM Stroud P Walter 2005 On the mechanism of sensing unfolded protein in the endoplasmic reticulum Proc Natl Acad Sci USA 102 18773 18784 1:CAS:528:DC%2BD28XivVyktQ%3D%3D 16365312
20. E Delot SG Brodie LM King WR Wilcox DH Cohn 1998 Physiological and pathological secretion of cartilage oligomeric matrix protein by cells in culture J Biol Chem 273 26692 26697 1:CAS:528:DyaK1cXmslajurk%3D 9756911
21. E Delot LM King MD Briggs WR Wilcox DH Cohn 1999 Trinucleotide expansion mutations in the cartilage oligomeric matrix protein (COMP) gene Hum Mol Genet 8 123 128 1:CAS:528:DyaK1MXoslClsg%3D%3D 9887340
22. J Duke D Montufar-Solis S Underwood Z Lalani JT Hecht 2003 Apoptosis staining in cultured pseudoachondroplasia chondrocytes Apoptosis 8 191 197 1:CAS:528:DC%2BD3sXit12ksbk%3D 12766479
23. DL Eizirik AK Cardozo M Cnop 2008 The role of endoplasmic reticulum stress in diabetes mellitus Endocr Rev 29 42 61 1:CAS:528:DC%2BD1cXivFGqs7s%3D 18048764
24. J Finkelstein EK Doege Y Yamada RE Pyeritz JM Graham JR Moeschler Jr RM Pauli JT Hecht CA Francomano 1991 Analysis of the chondroitin sulfate proteoglycan core protein (CSPGCP) gene in achondroplasia and pseudoachondroplasia Am J Hum Genet 48 97 102 1:CAS:528:DyaK3MXitVGjsrs%3D 1670752
25. J Fitzgerald SR Lamandé JF Bateman 1999 Proteasomal degradation of unassembled mutant type I collagen pro-alpha1(I) chains J Biol Chem 274 27392 27398 1:CAS:528:DyaK1MXmtlOlu70%3D 10488070
26. A Forlino C Tani A Rossi A Lupi E Campari B Gualeni L Bianchi A Armini G Cetta L Bini JC Marini 2007 Differential expression of both extracellular and intracellular proteins is involved in the lethal or nonlethal phenotypic variation of BrtllV, a murine model for osteogenesis imperfecta Proteomics 7 1877 1891 1:CAS:528:DC%2BD2sXntVSisbw%3D 17520686
27. MG Fresquet C Jackson J Loughlin MD Briggs 2008 Novel mutations in exon 2 of MATN3 affect residues within the alpha-helices of the A-domain and can result in the intracellular retention of mutant matrilin-3 Hum Mutat 29 330 18205203
28. DB Gould FC Phalan GJ Breedveld SE van Mil RS Smith JC Schimenti U Aguglia MS van der Knaap P Heutink SWM John 2005 Mutations in Col4a1 cause perinatal cerebral hemorrhage and porencephaly Science 308 1167 1171 1:CAS:528:DC%2BD2MXkt1Slsbs%3D 15905400
29. DB Gould JK Marchant OV Savinova RS Smith SWM John 2007 Col4a1 mutation causes endoplasmic reticulum stress and genetically modifiable ocular dysgenesis Hum Mol Genet 16 797 807
30. K Hamamura Y Liu H Yokota 2008 Microarray analysis of thapsigargin-induced stress to the endoplasmic reticulum of mouse osteoblasts J Bone Miner Metab 26 231 240 1:CAS:528:DC%2BD1cXls1Kntro%3D 18470663
31. K Hamamura MB Goldring H Yokota 2009 Involvement of p38 MAPK in regulation of MMP13 mRNA in chondrocytes in response to surviving stress to endoplasmic reticulum Arch Oral Biol 54 279 286 1:CAS:528:DC%2BD1MXhtlSltbg%3D 19100962
32. HP Harding Y Zhang H Zeng I Novoa PD Lu M Calfon N Sadri C Yun B Popko R Paules DF Stojdl JC Bell T Hettmann JM Leiden D Ron 2003 An integrated stress response regulates amino acid metabolism and resistance to oxidative stress Mol Cell 11 619 633 1:CAS:528:DC%2BD3sXjtVWkt74%3D 12667446
33. Y Hashimoto T Tomiyama Y Yamano H Mori 2003 Mutation (D472Y) in the type 3 repeat domain of cartilage oligomeric matrix protein affects its early vesicle trafficking in endoplasmic reticulum and induces apoptosis Am J Pathol 163 101 110 1:CAS:528:DC%2BD3sXmtVWrtLw%3D 12819015
34. JT Hecht SH Blanton Y Wang SP Daiger WA Horton C Rhodes Y Yamada CA Francomano 1992 Exclusion of human proteoglycan link protein (CRTL1) and type II collagen (COL2A1) genes in pseudoachondroplasia Am J Med Genet 44 420 424 1:STN:280:DyaK3s%2Fnt1Snug%3D%3D 1442879
35. JT Hecht LD Nelson E Crowder Y Wang FF Elder WR Harrison CA Francomano CK Prange GG Lennon M Deere J Lawler 1995 Mutations in exon 17B of cartilage oligomeric matrix protein (COMP) cause pseudoachondroplasia Nat Genet 10 325 329 1:CAS:528:DyaK2MXms1Kjur4%3D 7670471
36. JT Hecht D Montufar-Solis G Decker J Lawler K Daniels PJ Duke 1998 Retention of cartilage oligomeric matrix protein (COMP) and cell death in redifferentiated pseudoachondroplasia chondrocytes Matrix Biol 17 625 633 1:CAS:528:DyaK1MXjslaqtg%3D%3D 9923655 (Pubitemid 29017229)
37. JT Hecht M Deere E Putnam W Cole B Vertel H Chen J Lawler 1998 Characterization of cartilage oligomeric matrix protein (COMP) in human normal and pseudoachondroplasia musculoskeletal tissues Matrix Biol 17 269 278 1:CAS:528:DyaK1cXlsFClsrc%3D 9749943 (Pubitemid 28403341)
38. JT Hecht E Hayes M Snuggs G Decker D Montufar-Solis K Doege F Mwalle R Poole J Stevens PJ Duke 2001 Calreticulin, PDI, Grp94 and BiP chaperone proteins are associated with retained COMP in pseudoachondroplasia chondrocytes Matrix Biol 20 251 262 1:CAS:528:DC%2BD3MXltlOgsLY%3D 11470401
39. C Hetz L Glimcher 2008 The daily job of night killers: althernative roles of the BCL-2 family in organelle physiology Trends Cell Biol 18 38 44 1:CAS:528:DC%2BD1cXlvVyhug%3D%3D 18077169
40. MS Ho KY Tsang RL Lo M Susic O Mäkitie TW Chan VC Ng DO Sillence RP Boot-Handford G Gibson KM Cheung WG Cole KS Cheah D Chan 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 1:CAS:528:DC%2BD2sXntVKqsbY%3D 17403716
41. J Hollien JS Weissman 2006 Decay of endoplasmic reticulum localized mRNAs during the unfolded protein response Science 313 104 107 1:CAS:528: DC%2BD28XmsFWjurc%3D 16825573
42. J Iqbal K Dai T Seimon R Jungreis M Oyadomari G Kuriakose D Ron I Tabas MM Hussain 2008 IRE1beta inhibits chylomicron production by selectively degrading MTP mRNA Cell Metab 7 445 455 1:CAS:528:DC%2BD1cXmtFeiurs%3D 18460335
43. Y Ishida A Yamamoto A Kitamura SR Lamandé Y Yoshimori JF Bateman H Kubota K Nagata 2009 Autophagic elimination of misfolded procollagen aggregates in the endoplasmic reticulum as a means of cell protection Mol Cell Biol 20 2744 2754 1:CAS:528:DC%2BD1MXotVyqu7o%3D
44. GC Jackson FS Barker E Jakkula M Czarny-Ratajczak O Makitie WG Cole MJ Wright SF Smithson M Suri P Rogala GR Mortier C Baldock A Wallace R Elles L Ala-Kokko MD Briggs 2004 Missense mutations in the beta strands of the single A-domain of matrilin-3 result in multiple epiphyseal dysplasia J Med Genet 41 52 59 1:CAS:528:DC%2BD2cXhs1KhsLY%3D 14729835
45. H Kawaguchi 2008 Endochondral ossification signals in cartilage degradation during osteoarthritis progression in experimental mouse models Mol Cells 25 1 6 1:CAS:528:DC%2BD1cXjt1GhsL4%3D 18319608
46. T Kawai J Fan K Mazan-Mamczarz M Gorospe 2004 Global mRNA stabilization preferentially linked to translational repression during the endoplasmic reticulum stress response Mol Cell Biol 24 6773 6787 1:CAS:528: DC%2BD2cXmtlKluro%3D 15254244
47. PS Kim O-Y Kwon P Arvan 1996 An endoplasmic reticulum storage disease causing congenital goiter with hypothyroidism J Cell Biol 133 517 527 1:CAS:528:DyaK28XivVKnt7o%3D 8636228
48. T Kudo S Kanemoto H Hara N Morimoto T Morihara R Kimura T Tabira K Imaizumi M Takeda 2008 A molecular chaperone inducer protects neurons from ER stress Cell Death Differ 15 364 375 1:CAS:528:DC%2BD1cXmsVOksw%3D%3D 18049481
49. SR Lamandé SD Chessler SB Golub PH Byers D Chan WG Cole DO Sillence JF Bateman 1995 Endoplasmic reticulum-mediated quality control of type I collagen production by cells from osteogenesis imperfecta patients with mutations in the pro alpha 1 (I) chain carboxyl-terminal propeptide which impair subunit assembly J Biol Chem 270 8642 8649 7721766
50. MP Leighton S Nundlall T Starborg RS Meadows F Suleman L Knowles R Wagener DJ Thornton KE Kadler RP Boot-Handford MD Briggs 2007 Decreased chondrocyte proliferation and dysregulated apoptosis in the cartilage growth plate are key features of a murine model of epiphyseal dysplasia caused by a matn3 mutation Hum Mol Genet 16 1728 1741 1:CAS:528:DC%2BD2sXosFektb0%3D 17517694
51. JH Lin P Walter TS Yen 2008 Endoplasmic reticulum stress in disease pathogenesis Annu Rev Pathol 3 399 425 1:CAS:528:DC%2BD1cXjsFersLg%3D 18039139
52. F Lisbona D Rojas-Rivera P Thielen S Zamorano D Todd F Martinon A Glavic C Kress JH Lin P Walter JC Reed LH Glimcher C Hetz 2009 BAX inhibitor-1 is a negative regulator of the ER stress sensor IRE1alpha Mol Cell 33 679 691 1:CAS:528:DC%2BD1MXltFSms7k%3D 19328063
53. TS Lisse F Thiele H Fuchs W Hans GKH Przemeck K Abe B Rathkolb L Quintanilla-Martinez G Hoelzlwimmer M Helfrich E Wolf SH Ralston MH de Angelis 2008 ERstress-mediated apoptosis in a new mouse model of osteogenesis imperfecta PLoS Genet 4 e7 18248096
54. PD Lu HP Harding D Ron 2004 Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response J Cell Biol 167 27 33 1:CAS:528:DC%2BD2cXosVOiurc%3D 15479734
55. BK Maddox DR Keene LY Sakai NL Charbonneau NP Morris CC Ridgway BA Boswell MD Sussman WA Horton HP Bachinger JT Hecht 1997 The fate of cartilage oligomeric matrix protein is determined by the cell type in the case of a novel mutation in pseudoachondroplasia J Biol Chem 272 30993 30997 1:CAS:528:DyaK2sXnvFSktr4%3D 9388247
56. JD Malhotra RJ Kaufman 2007 The endoplasmic reticulum and the unfolded protein response Semin Cell Dev Biol 18 716 731 1:CAS:528:DC%2BD2sXhtlGjtrrN 18023214
57. DS Marks CA Gregory GA Wallis A Brass KE Kadler RP Boot-Handford 1999 Metaphyseal chondrodysplasia type Schmid mutations are predicted to occur in two distinct three-dimensional clusters within type X collagen NC1 domains that retain the ability to trimerize J Biol Chem 274 3632 3641 1:CAS:528: DyaK1MXhtVemtr8%3D 9920912
58. JA Maynard RR Cooper IV Ponseti 1972 A unique rough surfaced endoplasmic reticulum inclusion in pseudoachondroplasia Lab Invest 26 40 44 1:STN:280:DyaE38%2FpsV2jtw%3D%3D 4333078
59. M Molinari 2007 N-glycan structure dictates extension of protein folding or onset of disposal Nat Chem Biol 3 313 320 1:CAS:528:DC%2BD2sXltlOjurs%3D 17510649
60. AK Mostert PF Dijkstra BR Jansen JR Van Horn B De Graaf P Heutink D Lindhout 2003 Familial multiple epiphyseal dysplasia due to a matrilin-3 mutation: further delineation of the phenotype including 40 years follow-up Am J Med Genet 120A 490 497 1:STN:280:DC%2BD3szltVegsA%3D%3D 12884427
61. VH Nielsen C Bendixen J Arnbjerg CM Sorensen HE Jensen NM Shukri B Thomsen 2000 Abnormal growth plate function in pigs carrying a dominant mutation in type X collagen Mamm Genome 11 1087 1092 1:CAS:528:DC%2BD3MXovVSm 11130976
62. M Ogata S Hino A Saito K Morikawa S Kondo S Kanemoto T Murakami M Taniguchi I Tanii K Yoshinaga S Shiosaka JA Hammarback F Urano K Imaizumi 2006 Autophagy is activated for cell survival after endoplasmic reticulum stress Mol Cell Biol 26 9220 9231 1:CAS:528:DC%2BD28XhtlemsLvI 17030611
63. SH Oh SC Lim 2009 Endoplasmic reticulum stress-mediated autophagy/apoptosis induced by capsaicin (8-methyl-N-vanillyl-6-nonenamide) and dihydrocapsaicin is regulated by the extent of c-Jun NH2-terminal kinase/extracellular signal-regulated kinase activation in WI38 lung epithelial fibroblast cells Pharmacol Exp Ther 329 112 122 1:CAS:528:DC%2BD1MXksVKnur4%3D
64. U Ozcan Q Cao E Yilmaz AH Lee NN Iwakoshi E Ozdelen G Tuncman C Görgün LH Glimcher GS Hotamisligil 2004 Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes Science 306 457 461 15486293
65. U Ozcan E Yilmaz L Ozcan M Furuhashi E Vaillancourt RO Smith CZ Gorgun GS Hotamisligil 2006 Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes Science 313 1137 1140 16931765
66. E Papp P Csermely 2006 Chemical chaperones: mechanisms of action and potential use Handb Exp Pharmacol 172 405 416 1:CAS:528:DC%2BD2MXhtlWqsbvL 16610368
67. Y-N Park P Arvan 2004 The acetylcholinesterase homology region is essential for normal conformational maturation and secretion of thyroglobulin J Biol Chem 279 17085 17089 1:CAS:528:DC%2BD2cXjt1Ggt7c%3D 14764582
68. D Patra X Xing S Davies J Byran C Franz EB Hunziker LJ Sandell 2007 Site-1 protease is essential for endochondral bone formation in mice J Cell Biol 179 687 700 1:CAS:528:DC%2BD2sXhtlOgu7bO 18025304
69. GD Pearson R Devereux B Loeys C Maslen D Milewicz R Pyeritz F Ramirez D Rifkin L Sakai L Svensson A Wessels J Van Eyk HC Dietz National Heart, Lung, and Blood Institute and National Marfan Foundation Working Group 2008 Report of the National Heart, Lung, and Blood Institute and National Marfan Foundation Working Group on research in Marfan syndrome and related disorders Circulation 118 785 791 18695204
70. DL Perlmutter 2002 Chemical chaperones: a pharmacological strategy for disorders of protein folding and trafficking Pediatric Res 52 832 836
71. KA Pirog-Garcia RS Meadows L Knowles D Heinegard DJ Thornton KE Kadler RP Boot-Handford MD Briggs 2007 Reduced cell proliferation and increased apoptosis are significant pathological mechanisms in a murine model of mild pseudoachondroplasia resulting from a mutation in the C-terminal domain of COMP Hum Mol Genet 16 2072 2088 1:CAS:528:DC%2BD2sXpvVWqt78%3D 17588960
72. DJ Prockop 1984 Osteogenesis imperfecta: phenotypic heterogeneity, protein suicide, short and long collagen Am J Hum Genet 36 449 505
73. X Qi T Hosoi Y Okuma M Kaneko Y Nomura 2004 Sodium 4-phenylbutyrate protects against cerebral ischemic injury Mol Pharmacol 66 899 908 1:CAS:528:DC%2BD2cXotlGmtLY%3D 15226415
74. Rajpar HM, McDermott B, Kung L, Eardley R, Knowles L, Heeran M, Thornton DJ, Wilson R, Bateman JF, Poulom R, Arvan P, Kadler KE, Briggs MD, Boot-Handford RP (2009) Targeted induction of endoplasmic reticulum stress induces cartilage pathology. PloS Genet (in press)
75. DL Rimoin IM Rasmussen MD Briggs PJ Roughley HE Gruber ML Warman BR Olsen YE Hsia J Yuen K Reinker, et al. 1994 A large family with features of pseudoachondroplasia and multiple epiphyseal dysplasia: exclusion of seven candidate gene loci that encode proteins of the cartilage extracellular matrix Hum Genet 93 236 242 1:STN:280:DyaK2c7ntFahsg%3D%3D 7907311
76. JC Rochet 2007 Novel therapeutic strategies for the treatment of protein-misfolding diseases Expert Rev Mol Med 9 1 34 17597554
77. D Ron P Walter 2007 Signal transduction in the endoplasmic reticulum unfolded protein response Nat Rev Mol Cell Biol 8 519 529 1:CAS:528: DC%2BD2sXmvVaktLY%3D 17565364
78. DC Rubinsztein JE Gestwickl LO Murphy D Klionsky 2007 Potential therapeutic applications of autophagy Nat Rev Drug Discov 6 304 312 1:CAS:528:DC%2BD2sXjs1SisLo%3D 17396135
79. C Ruiz-Romero V Carreira I Rego S Remeseiro MJ López-Armada FJ Blanco 2008 Proteomic analysis of human osteoarthritic chondrocytes reveals protein changes in stress and glycolysis Proteomics 8 495 507 1:CAS:528:DC%2BD1cXit1ygs7Y%3D 18186017
80. DT Rutkowski RJ Kaufman 2004 A trip to the ER: coping with stress Trends Cell Biol 14 20 28 1:CAS:528:DC%2BD2cXjtFegsw%3D%3D 14729177
81. DT Rutkowski J Wu SH Back MU Callaghan SP Ferris J Iqbal R Clark H Miao JR Hassler J Fornek MG Katze MM Hussain B Song J Swathirajan J Wang GD Yau RJ Kaufman 2008 UPR pathways combine to prevent hepatic steatosis caused by ER stress-mediated suppression of transcriptional master regulators Dev Cell 15 829 840 1:CAS:528:DC%2BD1cXhsFWgsbjP 19081072
82. M Schmitz A Niehoff N Miosge N Smyth M Paulsson F Zaucke 2008 Transgenic mice expressing D469Delta mutated cartilage oligomeric matrix protein (COMP) show growth plate abnormalities and sternal malformations Matrix Biol 27 67 85 1:CAS:528:DC%2BD1cXhvVWitb0%3D 17889519
83. M Schröder 2008 Endoplasmic reticulum stress responses Cell Mol Life Sci 65 862 894 18038217
84. J Shen X Chen L Hendershot R Prywes 2002 ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals Dev Cell 3 99 111 1:CAS:528:DC%2BD38XlsFSmsL8%3D 12110171
85. X Shen RE Ellis K Sakaki RJ Kaufman 2005 Genetic interactions due to constitutive and inducible gene regulation mediated by the unfolded protein response in C. elegans PLoS Genet 1 e37 16184190
86. V Srinivas J Bohensky AM Zahm IM Shapiro 2009 Autophagy in mineralizing tissues. Microenvironmental perspectives Cell Cycle 8 391 393 1:CAS:528:DC%2BD1MXlvFWjsb8%3D 19177014
87. R Stanescu V Stanescu MP Muriel P Maroteaux 1993 Multiple epiphyseal dysplasia, Fairbank type: morphologic and biochemical study of cartilage Am J Med Genet 45 501 507 1:STN:280:DyaK3s3itVOhsg%3D%3D 8465858
88. V Stanescu P Maroteaux R Stanescu 1982 The biochemical defect of pseudoachondroplasia Eur J Pediatr 138 221 225 1:STN:280:DyaL3s%2FgtlOitQ%3D%3D 7117284
89. E Szegezdi SE Logue AM Gorman A Samali 2006 Mediators of endoplasmic stress-induced apoptosis EMBO Rep 7 880 885 1:CAS:528:DC%2BD28XptVSlsLo%3D 16953201
90. JT Tan F Kremer S Freddi KM Bell NL Baker SR Lamandé JF Bateman 2008 Competency for nonsense-mediated reduction in collagen X mRNA is specified by the 3' UTR and corresponds to the position of mutations in Schmid metaphyseal chondrodysplasia Am J Hum Genet 82 786 793 1:CAS:528:DC%2BD1cXksVGru74%3D 18304492
91. DJ Todd A-H Lee LH Glimcher 2008 The endoplasmic reticulum stress response in immunity and autoimmunity Nat Rev Immunol 8 663 674 1:CAS:528:DC%2BD1cXhtVamu7nP 18670423
92. KY Tsang D Chan D Cheslett WCW Chan CL So IG Melhado TWY Chan KM Kwan EB Hunziker Y Yamada JF Bateman KMC Cheung KSE Cheah 2007 Surviving endoplasmic reticulum stress is coupled to altered chondrocyte differentiation and function PLoS Biology 5 e44 17298185
93. F Urano X Wang A Bertolotti Y Zhang P Chung HP Harding D Ron 2000 Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1 Science 287 664 666 1:CAS:528: DC%2BD3cXovVyhuw%3D%3D 10650002
94. J Vranka A Mokashi DR Keene S Tufa G Corson M Sussman WA Horton K Maddox L Sakai HP Bachinger 2001 Selective intracellular retention of extracellular matrix proteins and chaperones associated with pseudoachondroplasia Matrix Biol 20 439 450 1:CAS:528:DC%2BD3MXnvFGjtb8%3D 11691584
95. GA Wallis B Rash WA Sweetman JT Thomas M Super G Evans ME Grant RP Boot-Handford 1994 Amino acid substitutions of conserved residues in the carboxyl-terminal domain of the α1 chain of type X collagen occur in two unrelated families with metaphyseal chondrodysplasia type Schmid Am J Hum Genet 54 169 178 1:CAS:528:DyaK2cXmt1Cntrc%3D 8304336
96. ML Warman M Abbott SS Apte T Hefferon I McIntosh DH Cohn JT Hecht BR Olsen CA Francomano 1993 A type X collagen mutation causes Schmid metaphyseal chondrodysplasia Nat Genet 5 79 82 1:CAS:528:DyaK3sXmtVWitrg%3D 8220429
97. EJ Weaver GP Summerville G Yeh M Hervada-Page R Oehlmann R Rothman SA Jimenez RG Knowlton 1993 Exclusion of type II and type VI procollagen gene mutations in a five-generation family with multiple epiphyseal dysplasia Am J Med Genet 45 345 352 1:STN:280:DyaK3s7msleiug%3D%3D 8094597
98. J Wei X Sheng D Feng B McGrath DR Cavener 2008 PERK is essential for neonatal skeletal development to regulate osteoblast proliferation and differentiation J Cell Physiol 217 693 707 1:CAS:528:DC%2BD1cXhtlOqt7rM 18683826
99. A Williams S Sarkar P Cuddon EK Ttofi S Saiki FH Siddiqi L Jahreiss A Fleming D Pask P Goldsmith CJ O'Kane RA Floto DC Rubinsztein 2008 Novel targets for Huntington's disease in an mTOR-independent autophagy pathway Nat Chem Biol 4 295 305 1:CAS:528:DC%2BD1cXkvVSmt7c%3D 18391949
100. R Wilson S Freddi JF Bateman 2002 Collagen X chains harboring Schmid metaphyseal chondrodysplasia NC1 domain mutations are selectively retained and degraded in stably transfected cells J Biol Chem 277 12516 12524 1:CAS:528:DC%2BD38XivV2qur4%3D 11805116
101. R Wilson S Freddi D Chan KSE Cheah JF Bateman 2005 Misfolding of collagen X chains harboring Schmid metaphyseal chondrodysplasia mutations results in aberrant disulfide bond formation intracellular retention and activation of the unfolded protein response J Biol Chem 280 15544 15552 1:CAS:528: DC%2BD2MXjtleju78%3D 15695517
102. P Wordsworth D Ogilvie L Priestley R Smith R Wynne-Davies B Sykes 1988 Structural and segregation analysis of the type II collagen gene (COL2A1) in some heritable chondrodysplasias J Med Genet 25 521 527 1:STN:280: DyaL1M%2FhtFyhuw%3D%3D 2902229
103. X Yang K Matsuda P Bialek S Jacquot HC Masuoka T Schinke L Li S Brancorsini P Sassone-Corsi TM Townes A Hanauer G Karsenty 2004 ATF4 is a substrate of RSK2 and essential regulator of osteoblast biology: implication for Coffin-Lowry syndrome Cell 117 387 398 1:CAS:528:DC%2BD2cXjvFemtro%3D 15109498
104. J Ye RB Rawson R Komuro X Chen UP Davé R Prywes MS Brown JL Goldstein 2000 ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs Mol Cell 6 1355 1364 1:CAS:528: DC%2BD3MXlvFahtQ%3D%3D 11163209
105. E Zelzer BR Olsen 2005 Multiple roles of vascular endothelial growth factor (VEGF) in skeletal development, growth, and repair Curr Top Dev Biol 65 169 187 1:CAS:528:DC%2BD2MXltVKlurw%3D 15642383
106. K Zhang RJ Kaufman 2008 From endoplasmic-reticulum stress to the inflammatory response Nature 454 455 462 1:CAS:528:DC%2BD1cXovV2mtbo%3D 18650916
107. P Zhang B McGrath S Li A Frank F Zambito J Reinert M Gannon K Ma K McNaughton DR Cavener 2002 The PERK eukaryotic initiation factor 2 alpha kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas Mol Cell Biol 22 3864 3874 1:CAS:528:DC%2BD38XjslWlt7s%3D 11997520
108. H Zinszner M Kuroda X Wang N Batchvarova RT Lightfoot H Remotti JL Stevens D Ron 1998 CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum Genes Dev 12 982 995 1:CAS:528:DyaK1cXisl2gsr4%3D 9531536