Transcriptional profiling of chondrodysplasia growth plate cartilage reveals adaptive ER-stress networks that allow survival but disrupt hypertrophy

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Cameron, Trevor L ^a   Bell, Katrina M ^a   Tatarczuch, Liliana ^b   Mackie, Eleanor J ^b   Rajpar, M Helen ^c   McDermott, Ben T ^c   Boot Handford, Raymond P ^c   Bateman, John F ^a,b  

^a MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA; CHAPERONE; COLLAGEN TYPE 10; ENZYME; FOLDASE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; THYROGLOBULIN; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; CRELD2 PROTEIN, MOUSE; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 21; MANF PROTEIN, MOUSE; MEMBRANE PROTEIN; NERVE GROWTH FACTOR; SCLEROPROTEIN; STEAP PROTEIN, MOUSE; TUMOR ANTIGEN; WOLFRAMIN PROTEIN;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARMET GENE; ARTICLE; CARTILAGE CELL; CELL DIFFERENTIATION; CHONDROCYTE HYPERTROPHY; CHONDRODYSPLASIA; CHONDROPATHY; CONTROLLED STUDY; CRELD2 GENE; ENDOPLASMIC RETICULUM STRESS; ENZYME REGULATION; FGF21 GENE; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE MAPPING; GROWTH PLATE; IN VIVO STUDY; MICRODISSECTION; MOUSE; MOUSE MUTANT; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; STEAP1 GENE; SURVIVAL; SYVN1 GENE; TRANSCRIPTOMICS; UNFOLDED PROTEIN RESPONSE; WFS1 GENE; WILD TYPE; ANIMAL; APOPTOSIS; BIOLOGY; CARTILAGE; CELL HYPOXIA; CYTOLOGY; DNA MICROARRAY; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; METHODOLOGY; NICK END LABELING; PATHOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING;

ANIMALS; ANTIGENS, NEOPLASM; APOPTOSIS; BLOTTING, WESTERN; CARTILAGE; CELL ADHESION MOLECULES; CELL HYPOXIA; CHONDROCYTES; COMPUTATIONAL BIOLOGY; ENDOPLASMIC RETICULUM STRESS; EXTRACELLULAR MATRIX PROTEINS; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION PROFILING; GROWTH PLATE; IN SITU HYBRIDIZATION; IN SITU NICK-END LABELING; MEMBRANE PROTEINS; MICE; MICRODISSECTION; MICROSCOPY, ELECTRON, TRANSMISSION; NERVE GROWTH FACTORS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSTEOCHONDRODYSPLASIAS; POLYMERASE CHAIN REACTION;

EID: 80052842907     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024600     Document Type: Article

References (86)

1. Bateman JF, Boot-Handford RP, Lamande SR, (2009) Genetic diseases of connective tissues: cellular and extracellular effects of ECM mutations. Nat Rev Genet 10: 173-183.
2. Tsang KY, Chan D, Bateman JF, Cheah KS, (2010) In vivo cellular adaptation to ER stress: survival strategies with double-edged consequences. J Cell Sci 123: 2145-2154.
3. Boot-Handford RP, Briggs MD, (2010) The unfolded protein response and its relevance to connective tissue diseases. Cell Tissue Res 339: 197-211.
4. Scheuner D, Kaufman RJ, (2008) The unfolded protein response: a pathway that links insulin demand with beta-cell failure and diabetes. Endocr Rev 29: 317-333.
5. Eizirik DL, Cardozo AK, Cnop M, (2008) The role for endoplasmic reticulum stress in diabetes mellitus. Endocr Rev 29: 42-61.
6. Ji C, (2008) Dissection of endoplasmic reticulum stress signaling in alcoholic and non-alcoholic liver injury. J Gastroenterol Hepatol 23 (Suppl 1): S16-24.
7. Ji C, Kaplowitz N, (2006) ER stress: can the liver cope? J Hepatol 45: 321-333.
8. 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.
9. 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.
10. Malhotra JD, Kaufman RJ, (2007) The endoplasmic reticulum and the unfolded protein response. Semin Cell Dev Biol 18: 716-731.
11. Ron D, Walter P, (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8: 519-529.
12. Kaufman RJ, (1999) Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 13: 1211-1233.
13. Yoshida H, Okada T, Haze K, Yanagi H, Yura T, et al. (2000) ATF6 activated by proteolysis binds in the presence of NF-Y (CBF) directly to the cis-acting element responsible for the mammalian unfolded protein response. Mol Cell Biol 20: 6755-6767.
14. 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.
15. Yoshida H, Oku M, Suzuki M, Mori K, (2006) pXBP1(U) encoded in XBP1 pre-mRNA negatively regulates unfolded protein response activator pXBP1(S) in mammalian ER stress response. J Cell Biol 172: 565-575.
16. Lee K, Tirasophon W, Shen X, Michalak M, Prywes R, et al. (2002) IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev 16: 452-466.
17. 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.
18. Hollien J, Weissman JS, (2006) Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313: 104-107.
19. Han D, Lerner AG, Vande Walle L, Upton JP, Xu W, et al. (2009) IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 138: 562-575.
20. Harding HP, Zhang Y, Ron D, (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271-274.
21. Szegezdi E, Logue SE, Gorman AM, Samali A, (2006) Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep 7: 880-885.
22. Oyadomari S, Mori M, (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11: 381-389.
23. Schroder M, Kaufman RJ, (2005) The mammalian unfolded protein response. Annu Rev Biochem 74: 739-789.
24. 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.
25. Edgar R, Domrachev M, Lash AE, (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210.
26. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
27. Tadimalla A, Belmont PJ, Thuerauf DJ, Glassy MS, Martindale JJ, et al. (2008) Mesencephalic astrocyte-derived neurotrophic factor is an ischemia-inducible secreted endoplasmic reticulum stress response protein in the heart. Circ Res 103: 1249-1258.
28. Kaneko M, Koike H, Saito R, Kitamura Y, Okuma Y, et al. (2010) Loss of HRD1-mediated protein degradation causes amyloid precursor protein accumulation and amyloid-beta generation. J Neurosci 30: 3924-3932.
29. Wang XZ, Harding HP, Zhang Y, Jolicoeur EM, Kuroda M, et al. (1998) Cloning of mammalian Ire1 reveals diversity in the ER stress responses. EMBO J 17: 5708-5717.
30. Lin JH, Li H, Zhang Y, Ron D, Walter P, (2009) Divergent effects of PERK and IRE1 signaling on cell viability. PLoS One 4: e4170.
31. Kaneko M, Yasui S, Niinuma Y, Arai K, Omura T, et al. (2007) A different pathway in the endoplasmic reticulum stress-induced expression of human HRD1 and SEL1 genes. FEBS Lett 581: 5355-5360.
32. Fonseca SG, Fukuma M, Lipson KL, Nguyen LX, Allen JR, et al. (2005) WFS1 is a novel component of the unfolded protein response and maintains homeostasis of the endoplasmic reticulum in pancreatic beta-cells. J Biol Chem 280: 39609-39615.
33. Verfaillie T, Salazar M, Velasco G, Agostinis P, (2010) Linking ER Stress to Autophagy: Potential Implications for Cancer Therapy. Int J Cell Biol 2010: 930509.
34. Belluoccio D, Bernardo BC, Rowley L, Bateman JF, (2008) A microarray approach for comparative expression profiling of the discrete maturation zones of mouse growth plate cartilage. Biochim Biophys Acta 1779: 330-340.
35. Wang Y, Middleton F, Horton JA, Reichel L, Farnum CE, et al. (2004) Microarray analysis of proliferative and hypertrophic growth plate zones identifies differentiation markers and signal pathways. Bone 35: 1273-1293.
36. James CG, Stanton LA, Agoston H, Ulici V, Underhill TM, et al. (2010) Genome-wide analyses of gene expression during mouse endochondral ossification. PLoS One 5: e8693.
37. Lui JC, Andrade AC, Forcinito P, Hegde A, Chen W, et al. (2010) Spatial and temporal regulation of gene expression in the mammalian growth plate. Bone 46: 1380-1390.
38. Pirog-Garcia KA, Meadows RS, Knowles L, Heinegard D, Thornton DJ, et al. (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.
39. Nundlall S, Rajpar MH, Bell PA, Clowes C, Zeeff LA, et al. (2010) An unfolded protein response is the initial cellular response to the expression of mutant matrilin-3 in a mouse model of multiple epiphyseal dysplasia. Cell Stress Chaperones 15: 835-849.
40. Lisse TS, Thiele F, Fuchs H, Hans W, Przemeck GK, et al. (2008) ER stress-mediated apoptosis in a new mouse model of osteogenesis imperfecta. PLoS Genet 4: e7.
41. Lin JH, Li H, Yasumura D, Cohen HR, Zhang C, et al. (2007) IRE1 signaling affects cell fate during the unfolded protein response. Science 318: 944-949.
42. Lu R, Misra V, (2000) Potential role for luman, the cellular homologue of herpes simplex virus VP16 (alpha gene trans-inducing factor), in herpesvirus latency. J Virol 74: 934-943.
43. Raggo C, Rapin N, Stirling J, Gobeil P, Smith-Windsor E, et al. (2002) Luman, the cellular counterpart of herpes simplex virus VP16, is processed by regulated intramembrane proteolysis. Mol Cell Biol 22: 5639-5649.
44. 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.
45. DenBoer LM, Hardy-Smith PW, Hogan MR, Cockram GP, Audas TE, et al. (2005) Luman is capable of binding and activating transcription from the unfolded protein response element. Biochem Biophys Res Commun 331: 113-119.
46. Kondo S, Saito A, Hino S, Murakami T, Ogata M, et al. (2007) BBF2H7, a novel transmembrane bZIP transcription factor, is a new type of endoplasmic reticulum stress transducer. Mol Cell Biol 27: 1716-1729.
47. 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.
48. Liang G, Audas TE, Li Y, Cockram GP, Dean JD, et al. (2006) Luman/CREB3 induces transcription of the endoplasmic reticulum (ER) stress response protein Herp through an ER stress response element. Mol Cell Biol 26: 7999-8010.
49. Stirling J, O'Hare P, (2006) CREB4, a transmembrane bZip transcription factor and potential new substrate for regulation and cleavage by S1P. Mol Biol Cell 17: 413-426.
50. Saito A, Hino S, 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.
51. Vembar SS, Brodsky JL, (2008) One step at a time: endoplasmic reticulum-associated degradation. Nat Rev Mol Cell Biol 9: 944-957.
52. Di Jeso B, Park YN, Ulianich L, Treglia AS, Urbanas ML, et al. (2005) Mixed-disulfide folding intermediates between thyroglobulin and endoplasmic reticulum resident oxidoreductases ERp57 and protein disulfide isomerase. Mol Cell Biol 25: 9793-9805.
53. Pagani M, Fabbri M, Benedetti C, Fassio A, Pilati S, et al. (2000) Endoplasmic reticulum oxidoreductin 1-lbeta (ERO1-Lbeta), a human gene induced in the course of the unfolded protein response. J Biol Chem 275: 23685-23692.
54. Fonseca SG, Ishigaki S, Oslowski CM, Lu S, Lipson KL, et al. (2010) Wolfram syndrome 1 gene negatively regulates ER stress signaling in rodent and human cells. J Clin Invest 120: 744-755.
55. Apte SS, Olsen BR, (1993) Characterization of the mouse type X collagen gene. Matrix 13: 165-179.
56. Apte SS, Seldin MF, Hayashi M, Olsen BR, (1992) Cloning of the human and mouse type X collagen genes and mapping of the mouse type X collagen gene to chromosome 10. Eur J Biochem 206: 217-224.
57. Kielty CM, Grant ME, (2002) The collagen family: structure, assembly, and organization in the extracellular matrix. In: Royce PM, Steinmann B, editors. Connective Tissue and Its Heritable Disorders Molecular, Genetic, and Medical Aspects. 2nd ed Wiley-Liss pp. 159-221.
58. Myllyharju J, Kivirikko KI, (2004) Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20: 33-43.
59. Marriott A, Ayad S, Grant ME, (1991) The synthesis of type X collagen by bovine and human growth-plate chondrocytes. J Cell Sci 99 (Pt 3): 641-649.
60. Deshpande V, Venkatesh SG, (1999) Thyroglobulin, the prothyroid hormone: chemistry, synthesis and degradation. Biochim Biophys Acta 1430: 157-178.
61. Yang SX, Pollock HG, Rawitch AB, (1996) Glycosylation in human thyroglobulin: location of the N-linked oligosaccharide units and comparison with bovine thyroglobulin. Arch Biochem Biophys 327: 61-70.
62. Wilson R, Freddi S, Chan D, Cheah KS, Bateman JF, (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.
63. Mizobuchi N, Hoseki J, Kubota H, Toyokuni S, Nozaki J, et al. (2007) ARMET is a soluble ER protein induced by the unfolded protein response via ERSE-II element. Cell Struct Funct 32: 41-50.
64. Apostolou A, Shen Y, Liang Y, Luo J, Fang S, (2008) Armet, a UPR-upregulated protein, inhibits cell proliferation and ER stress-induced cell death. Exp Cell Res 314: 2454-2467.
65. 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.
66. Yoshida H, (2007) ER stress and diseases. FEBS J 274: 630-658.
67. Voutilainen MH, Back S, Porsti E, Toppinen L, Lindgren L, et al. (2009) Mesencephalic astrocyte-derived neurotrophic factor is neurorestorative in rat model of Parkinson's disease. J Neurosci 29: 9651-9659.
68. Oh-hashi K, Koga H, Ikeda S, Shimada K, Hirata Y, et al. (2009) CRELD2 is a novel endoplasmic reticulum stress-inducible gene. Biochem Biophys Res Commun 387: 504-510.
69. Ortiz JA, Castillo M, del Toro ED, Mulet J, Gerber S, et al. (2005) The cysteine-rich with EGF-like domains 2 (CRELD2) protein interacts with the large cytoplasmic domain of human neuronal nicotinic acetylcholine receptor alpha4 and beta2 subunits. J Neurochem 95: 1585-1596.
70. Hubert RS, Vivanco I, Chen E, Rastegar S, Leong K, et al. (1999) STEAP: a prostate-specific cell-surface antigen highly expressed in human prostate tumors. Proc Natl Acad Sci U S A 96: 14523-14528.
71. Ohgami RS, Campagna DR, McDonald A, Fleming MD, (2006) The Steap proteins are metalloreductases. Blood 108: 1388-1394.
72. Kurosu H, Kuro OM, (2009) The Klotho gene family as a regulator of endocrine fibroblast growth factors. Mol Cell Endocrinol 299: 72-78.
73. Kharitonenkov A, Larsen P, (2011) FGF21 reloaded: challenges of a rapidly growing field. Trends Endocrinol Metab 22: 81-86.
74. Yoshida H, Haze K, Yanagi H, Yura T, Mori K, (1998) Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors. J Biol Chem 273: 33741-33749.
75. Dai J, Rabie AB, (2007) VEGF: an essential mediator of both angiogenesis and endochondral ossification. J Dent Res 86: 937-950.
76. Park JE, Keller GA, Ferrara N, (1993) The vascular endothelial growth factor (VEGF) isoforms: differential deposition into the subepithelial extracellular matrix and bioactivity of extracellular matrix-bound VEGF. Mol Biol Cell 4: 1317-1326.
77. 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.
78. Vu TH, Shipley JM, Bergers G, Berger JE, Helms JA, et al. (1998) MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93: 411-422.
79. Tajiri S, Oyadomari S, Yano S, Morioka M, Gotoh T, et al. (2004) Ischemia-induced neuronal cell death is mediated by the endoplasmic reticulum stress pathway involving CHOP. Cell Death Differ 11: 403-415.
80. Tajiri S, Yano S, Morioka M, Kuratsu J, Mori M, et al. (2006) CHOP is involved in neuronal apoptosis induced by neurotrophic factor deprivation. FEBS Lett 580: 3462-3468.
81. Oyadomari S, Koizumi A, Takeda K, Gotoh T, Akira S, et al. (2002) Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J Clin Invest 109: 525-532.
82. Gow A, Wrabetz L, (2009) CHOP and the endoplasmic reticulum stress response in myelinating glia. Curr Opin Neurobiol 19: 505-510.
83. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
84. Ritchie ME, Silver J, Oshlack A, Holmes M, Diyagama D, et al. (2007) A comparison of background correction methods for two-colour microarrays. Bioinformatics 23: 2700-2707.
85. Schmitz N, Laverty S, Kraus VB, Aigner T, (2010) Basic methods in histopathology of joint tissues. Osteoarthritis Cartilage 18 (Suppl 3): S113-116.
86. Engfeldt B, Reinholt FP, Hultenby K, Widholm SM, Muller M, (1994) Ultrastructure of hypertrophic cartilage: histochemical procedures compared with high pressure freezing and freeze substitution. Calcif Tissue Int 55: 274-280.