Mechanisms and models of endoplasmic reticulum stress in chondrodysplasia

Developmental Dynamics

Volumn 243, Issue 7, 2014, Pages 875-893

  Patterson, Sara E ^a   Dealy, Caroline N ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Extracellular matrix (ECM) mutations; Genetic cartilage disorders; Human dwarfism; IPSC models; Unfolded protein response (UPR)

Indexed keywords

MUTANT PROTEIN; SCLEROPROTEIN;

ARTICLE; CHONDRODYSPLASIA; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; GENE MUTATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; UNFOLDED PROTEIN RESPONSE; CHONDRODYSPLASIA PUNCTATA; GENETICS; METABOLISM; MUTATION; PHYSIOLOGY;

CHONDRODYSPLASIA PUNCTATA; ENDOPLASMIC RETICULUM STRESS; EXTRACELLULAR MATRIX PROTEINS; HUMANS; MUTATION; UNFOLDED PROTEIN RESPONSE;

EID: 84902546397     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.24131     Document Type: Article

References (239)

1. Adams SL, Cohen AJ, Lassova L. 2007. Integration of signaling pathways regulating chondrocyte differentiation during endochondral bone formation. J Cell Physiol 213:635-641.
2. Akiyama H. 2008. Control of chondrogenesis by the transcription factor Sox9. Mod Rheumatol 18:213-219.
3. Alvarez-Garcia O, Carbajo-Perez E, Garcia E, Gil H, Molinos I, Rodriguez J, Ordonez FA, Santos F. 2007. Rapamycin retards growth and causes marked alterations in the growth plate of young rats. Pediatr Nephrol 22:954-961.
4. Alvarez-Garcia O, Garcia-Lopez E, Loredo V, Gil-Pena H, Mejia-Gaviria N, Rodriguez-Suarez J, Ordonez FA, Santos F. 2012. Growth hormone improves growth retardation induced by rapamycin without blocking its antiproliferative and antiangiogenic effects on rat growth plate. PLoS One 7:e34788.
5. Anderson IJ, Goldberg RB, Marion RW, Upholt WB, Tsipouras P. 1990. Spondyloepiphyseal dysplasia congenita: genetic linkage to type II collagen (COL2AI). Am J Hum Genet 46:896-901.
6. 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.
7. Appenzeller-Herzog C, Hall MN. 2012. Bidirectional crosstalk between endoplasmic reticulum stress and mTOR signaling. Trends Cell Biol 22:274-282.
8. Arnold WV, Fertala A. 2013. Skeletal diseases caused by mutations that affect collagen structure and function. Int J Biochem Cell Biol 45:1556-1567.
9. Bachar-Wikstrom E, Wikstrom JD, Kaiser N, Cerasi E, Leibowitz G. 2013. Improvement of ER stress-induced diabetes by stimulating autophagy. Autophagy 9:626-628.
10. Barbieri O, Astigiano S, Morini M, Tavella S, Schito A, Corsi A, Di Martino D, Bianco P, Cancedda R, Garofalo S. 2003. Depletion of cartilage collagen fibrils in mice carrying a dominant negative Col2a1 transgene affects chondrocyte differentiation. Am J Physiol Cell Physiol 285:C1504-C1512.
11. Bartoszewska S, Kochan K, Madanecki P, Piotrowski A, Ochocka R, Collawn JF, Bartoszewski R. 2013. Regulation of the unfolded protein response by microRNAs. Cell Mol Biol Lett 18:555-578.
12. Bateman JF, Wilson R, Freddi S, Lamande SR, Savarirayan R. 2005. Mutations of COL10A1 in Schmid metaphyseal chondrodysplasia. Hum Mutat 25:525-534.
13. Bell PA, Wagener R, Zaucke F, Koch M, Selley J, Warwood S, Knight D, Boot-Handford RP, Thornton DJ, Briggs MD. 2013. Analysis of the cartilage proteome from three different mouse models of genetic skeletal diseases reveals common and discrete disease signatures. Biol Open 2:802-811.
14. Blais JD, Chin KT, Zito E, Zhang Y, Heldman N, Harding HP, Fass D, Thorpe C, Ron D. 2010. A small molecule inhibitor of endoplasmic reticulum oxidation 1 (ERO1) with selectively reversible thiol reactivity. J Biol Chem 285:20993-21003.
15. Bogaert R, Tiller GE, Weis MA, Gruber HE, Rimoin DL, Cohn DH, Eyre DR. 1992. An amino acid substitution (Gly853->Glu) in the collagen alpha 1(II) chain produces hypochondrogenesis. J Biol Chem 267:22522-22526.
16. Bomsta BD, Bridgewater LC, Seegmiller RE. 2006. Premature osteoarthritis in the Disproportionate micromelia (Dmm) mouse. Osteoarthritis Cartilage 14:477-485.
17. Boot-Handford RP, Briggs MD. 2010. The unfolded protein response and its relevance to connective tissue diseases. Cell Tissue Res 339:197-211.
18. Braakman I, Bulleid NJ. 2011. Protein folding and modification in the mammalian endoplasmic reticulum. Annu Rev Biochem 80:71-99.
19. Brachvogel B, Zaucke F, Dave K, Norris EL, Stermann J, Dayakli M, Koch M, Gorman JJ, Bateman JF, Wilson R. 2013. Comparative proteomic analysis of normal and collagen IX null mouse cartilage reveals altered extracellular matrix composition and novel components of the collagen IX interactome. J Biol Chem 288:13481-13492.
20. Briggs MD, Brock J, Ramsden SC, Bell PA. 2014. Genotype to phenotype correlations in cartilage oligomeric matrix protein associated chondrodysplasias. Eur J Hum Genet. 2014. March 5. doi: 10.1038/ejhg.2014.30.
21. Briggs MD, Chapman KL. 2002. Pseudoachondroplasia and multiple epiphyseal dysplasia: mutation review, molecular interactions, and genotype to phenotype correlations. Hum Mutat 19:465-478.
22. Briggs MD, Hoffman SM, King LM, Olsen AS, Mohrenweiser H, Leroy JG, Mortier GR, Rimoin DL, Lachman RS, Gaines ES, et al. 1995. Pseudoachondroplasia and multiple epiphyseal dysplasia due to mutations in the cartilage oligomeric matrix protein gene. Nat Genet 10:330-336.
23. Briggs MD, Mortier GR, Cole WG, King LM, Golik SS, Bonaventure J, Nuytinck L, De Paepe A, Leroy JG, Biesecker L, Lipson M, Wilcox WR, Lachman RS, Rimoin DL, Knowlton RG, Cohn DH. 1998. Diverse mutations in the gene for cartilage oligomeric matrix protein in the pseudoachondroplasia-multiple epiphyseal dysplasia disease spectrum. Am J Hum Genet 62:311-319.
24. Brodsky JL. 2012. Cleaning up: ER-associated degradation to the rescue. Cell 151:1163-1167.
25. Brown KS, Cranley RE, Greene R, Kleinman HK, Pennypacker JP. 1981. Disproportionate micromelia (Dmm): an incomplete dominant mouse dwarfism with abnormal cartilage matrix. J Embryol Exp Morphol 62:165-182.
26. Cameron TL, Bell KM, Tatarczuch L, Mackie EJ, Rajpar MH, McDermott BT, Boot-Handford RP, Bateman JF. 2011. Transcriptional profiling of chondrodysplasia growth plate cartilage reveals adaptive ER-stress networks that allow survival but disrupt hypertrophy. PLoS One 6:e24600.
27. Cao SS, Kaufman RJ. 2013. Targeting endoplasmic reticulum stress in metabolic disease. Expert Opin Ther Targets 17:437-448.
28. Carames B, Hasegawa A, Taniguchi N, Miyaki S, Blanco FJ, Lotz M. 2012. Autophagy activation by rapamycin reduces severity of experimental osteoarthritis. Ann Rheum Dis 71:575-581.
29. Chakrabarti A, Chen AW, Varner JD. 2011. A review of the mammalian unfolded protein response. Biotechnol Bioeng 108:2777-2793.
30. Chan D, Taylor TK, Cole WG. 1993. Characterization of an arginine 789 to cysteine substitution in alpha 1 (II) collagen chains of a patient with spondyloepiphyseal dysplasia. J Biol Chem 268:15238-15245.
31. Chan D, Weng YM, Graham HK, Sillence DO, Bateman JF. 1998. A nonsense mutation in the carboxyl-terminal domain of type X collagen causes haploinsufficiency in schmid metaphyseal chondrodysplasia. J Clin Invest 101:1490-1499.
32. Chang J, Wang W, Zhang H, Hu Y, Wang M, Yin Z. 2013. The dual role of autophagy in chondrocyte responses in the pathogenesis of articular cartilage degeneration in osteoarthritis. Int J Mol Med 32:1311-1318.
33. Chapman KL, Mortier GR, Chapman K, Loughlin J, Grant ME, Briggs MD. 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.
34. Chen IP, Fukuda K, Fusaki N, Iida A, Hasegawa M, Lichtler A, Reichenberger EJ. 2013. Induced pluripotent stem cell reprogramming by integration-free sendai virus vectors from peripheral blood of patients with craniometaphyseal dysplasia. Cell Reprogram 15:503-513.
35. Chen Y, Brandizzi F. 2013. IRE1: ER stress sensor and cell fate executor. Trends Cell Biol 23:547-555.
36. Chessler SD, Byers PH. 1993. BiP binds type I procollagen pro alpha chains with mutations in the carboxyl-terminal propeptide synthesized by cells from patients with osteogenesis imperfecta. J Biol Chem 268:18226-18233.
37. Chessler SD, Wallis GA, Byers PH. 1993. Mutations in the carboxyl-terminal propeptide of the pro alpha 1(I) chain of type I collagen result in defective chain association and produce lethal osteogenesis imperfecta. J Biol Chem 268:18218-18225.
38. Chun JS, Oh H, Yang S, Park M. 2008. Wnt signaling in cartilage development and degeneration. BMB Rep 41:485-494.
39. Chung HJ, Jensen DA, Gawron K, Steplewski A, Fertala A. 2009. R992C (p.R1192C) Substitution in collagen II alters the structure of mutant molecules and induces the unfolded protein response. J Mol Biol 390:306-318.
40. Cole WG, Hall RK, Rogers JG. 1993. The clinical features of spondyloepiphyseal dysplasia congenita resulting from the substitution of glycine 997 by serine in the alpha 1(II) chain of type II collagen. J Med Genet 30:27-35.
41. Cornejo VH, Hetz C. 2013. The unfolded protein response in Alzheimer's disease. Semin Immunopathol 35:277-292.
42. Correll J. 1991. Surgical correction of short stature in skeletal dysplasias. Acta Paediatr Scand Suppl 377:143-148.
43. Cotterill SL, Jackson GC, Leighton MP, Wagener R, Makitie O, Cole WG, Briggs MD. 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.
44. Coustry F, Posey KL, Liu P, Alcorn JL, Hecht JT. 2012. D469del-COMP retention in chondrocytes stimulates caspase-independent necroptosis. Am J Pathol 180:738-748.
45. Cooper KL, Oh S, Sung Y, Dasari RR, Kirschner MW, Tabin CJ. 2013. Multiple phases of chondrocyte enlargement underlie differences in skeletal proportions. Nature 495:375-378.
46. Csete M. 2010. Translational prospects for human induced pluripotent stem cells. Regen Med 5:509-519.
47. Daniels K, Reiter R, Solursh M. 1996. Micromass cultures of limb and other mesenchyme. Methods Cell Biol 51:237-247.
48. de Crombrugghe B, Lefebvre V, Nakashima K. 2001. Regulatory mechanisms in the pathways of cartilage and bone formation. Curr Opin Cell Biol 13:721-727.
49. DeLise AM, Fischer L, Tuan RS. 2000. Cellular interactions and signaling in cartilage development. Osteoarthritis Cartilage 8:309-334.
50. Deyle DR, Khan IF, Ren G, Wang PR, Kho J, Schwarze U, Russell DW. 2012. Normal collagen and bone production by gene-targeted human osteogenesis imperfecta iPSCs. Mol Ther 20:204-213.
51. Diekman BO, Christoforou N, Willard VP, Sun H, Sanchez-Adams J, Leong KW, Guilak F. 2012. Cartilage tissue engineering using differentiated and purified induced pluripotent stem cells. Proc Natl Acad Sci U S A 109:19172-19177.
52. Ding Q, Lee YK, Schaefer EA, Peters DT, Veres A, Kim K, Kuperwasser N, Motola DL, Meissner TB, Hendriks WT, Trevisan M, Gupta RM, Moisan A, Banks E, Friesen M, Schinzel RT, Xia F, Tang A, Xia Y, Figueroa E, Wann A, Ahfeldt T, Daheron L, Zhang F, Rubin LL, Peng LF, Chung RT, Musunuru K, Cowan CA. 2013. A TALEN genome-editing system for generating human stem cell-based disease models. Cell Stem Cell 12:238-251.
53. Dinser R, Zaucke F, Kreppel F, Hultenby K, Kochanek S, Paulsson M, Maurer P. 2002. Pseudoachondroplasia is caused through both intra- and extracellular pathogenic pathways. J Clin Invest 110:505-513.
54. Donahue LR, Chang B, Mohan S, Miyakoshi N, Wergedal JE, Baylink DJ, Hawes NL, Rosen CJ, Ward-Bailey P, Zheng QY, Bronson RT, Johnson KR, Davisson MT. 2003. A missense mutation in the mouse Col2a1 gene causes spondyloepiphyseal dysplasia congenita, hearing loss, and retinoschisis. J Bone Miner Res 18:1612-1621.
55. Donnelly N, Gorman AM, Gupta S, Samali A. 2013. The eIF2alpha kinases: their structures and functions. Cell Mol Life Sci 70:3493-3511.
56. Egashira T, Yuasa S, Fukuda K. 2013. Novel insights into disease modeling using induced pluripotent stem cells. Biol Pharm Bull 36:182-188.
57. Esapa CT, Hough TA, Testori S, Head RA, Crane EA, Chan CP, Evans H, Bassett JH, Tylzanowski P, McNally EG, Carr AJ, Boyde A, Howell PG, Clark A, Williams GR, Brown MA, Croucher PI, Nesbit MA, Brown SD, Cox RD, Cheeseman MT, Thakker RV. 2012. A mouse model for spondyloepiphyseal dysplasia congenita with secondary osteoarthritis due to a Col2a1 mutation. J Bone Miner Res 27:413-428.
58. Eyre DR, Weis MA, Moskowitz RW. 1991. Cartilage expression of a type II collagen mutation in an inherited form of osteoarthritis associated with a mild chondrodysplasia. J Clin Invest 87:357-361.
59. Fang C, Carlson CS, Leslie MP, Tulli H, Stolerman E, Perris R, Ni L, Di Cesare PE. 2000. Molecular cloning, sequencing, and tissue and developmental expression of mouse cartilage oligomeric matrix protein (COMP). J Orthop Res 18:593-603.
60. Fernandes RJ, Seegmiller RE, Nelson WR, Eyre DR. 2003. Protein consequences of the Col2a1 C-propeptide mutation in the chondrodysplastic Dmm mouse. Matrix Biol 22:449-453.
61. Ferrari D, Gong G, Kosher RA, Dealy CN. 2011. Chondrogenic Differentiation of hESC in Micromass Culture. In: Ye K, Jin S, editors. Springer protocols handbooks. New York: Springer Press. p 359-367.
62. Ferrari DM, Soling HD. 1999. The protein disulphide-isomerase family: unravelling a string of folds. Biochem J 339(Pt 1):1-10.
63. Fertala A, Ala-Kokko L, Wiaderkiewicz R, Prockop DJ. 1997. Collagen II containing a Cys substitution for arg-alpha1-519. Homotrimeric monomers containing the mutation do not assemble into fibrils but alter the self-assembly of the normal protein. J Biol Chem 272:6457-6464.
64. Fitzgerald J, Lamande SR, Bateman JF. 1999. Proteasomal degradation of unassembled mutant type I collagen pro-alpha1(I) chains. J Biol Chem 274:27392-27398.
65. Fresquet M, Jackson GC, Loughlin J, Briggs MD. 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.
66. Gaiser KG, Maddox BK, Bann JG, Boswell BA, Keene DR, Garofalo S, Horton WA. 2002. Y-position collagen II mutation disrupts cartilage formation and skeletal development in a transgenic mouse model of spondyloepiphyseal dysplasia. J Bone Miner Res 17:39-47.
67. Galligan JJ, Petersen DR. 2012. The human protein disulfide isomerase gene family. Hum Genomics 6:6.
68. Gardner BM, Pincus D, Gotthardt K, Gallagher CM, Walter P. 2013. Endoplasmic reticulum stress sensing in the unfolded protein response. Cold Spring Harb Perspect Biol 5:a013169.
69. Garofalo S, Vuorio E, Metsaranta M, Rosati R, Toman D, Vaughan J, Lozano G, Mayne R, Ellard J, Horton W, et al. 1991. Reduced amounts of cartilage collagen fibrils and growth plate anomalies in transgenic mice harboring a glycine-to-cysteine mutation in the mouse type II procollagen alpha 1-chain gene. Proc Natl Acad Sci U S A 88:9648-9652.
70. Gawron K, Jensen DA, Steplewski A, Fertala A. 2010. Reducing the effects of intracellular accumulation of thermolabile collagen II mutants by increasing their thermostability in cell culture conditions. Biochem Biophys Res Commun 396:213-218.
71. Gay SW, Kosher RA. 1984. Uniform cartilage differentiation in micromass cultures prepared from a relatively homogeneous population of chondrogenic progenitor cells of the chick limb bud: effect of prostaglandins. J Exp Zool 232:317-326.
72. Gong G, Ferrari D, Dealy CN, Kosher RA. 2010. Direct and progressive differentiation of human embryonic stem cells into the chondrogenic lineage. J Cell Physiol 224:664-671.
73. Gorbatyuk M, Gorbatyuk O. 2013a. Review: retinal degeneration: focus on the unfolded protein response. Mol Vis 19:1985-1998.
74. Gorbatyuk MS, Gorbatyuk OS. 2013b. The molecular chaperone GRP78/BiP as a therapeutic target for neurodegenerative disorders: a mini review. J Genet Syndr Gene Ther 4:pii128.
75. Groenendyk J, Sreenivasaiah PK, Kim do H, Agellon LB, Michalak M. 2010. Biology of endoplasmic reticulum stress in the heart. Circ Res 107:1185-1197.
76. Gualeni B, Rajpar MH, Kellogg A, Bell PA, Arvan P, Boot-Handford RP, Briggs MD. 2013. A novel transgenic mouse model of growth plate dysplasia reveals that decreased chondrocyte proliferation due to chronic ER stress is a key factor in reduced bone growth. Dis Model Mech 6:1414-1425.
77. Guo FJ, Xiong Z, Luo X, Ye M, Han X, Jiang R. 2013. ATF6 upregulates XBP1S and inhibits ER stress-mediated apoptosis in osteoarthritis cartilage. Cell Signal 26:332-342.
78. Guzzo RM, Gibson J, Xu RH, Lee FY, Drissi H. 2013. Efficient differentiation of human iPSC-derived mesenchymal stem cells to chondroprogenitor cells. J Cell Biochem 114:480-490.
79. Hagiwara M, Maegawa K, Suzuki M, Ushioda R, Araki K, Matsumoto Y, Hoseki J, Nagata K, Inaba K. 2011. Structural basis of an ERAD pathway mediated by the ER-resident protein disulfide reductase ERdj5. Mol Cell 41:432-444.
80. Halasz K, Kassner A, Morgelin M, Heinegard D. 2007. COMP acts as a catalyst in collagen fibrillogenesis. J Biol Chem 282:31166-31173.
81. Hale AN, Ledbetter DJ, Gawriluk TR, Rucker EB III. 2013. Autophagy: regulation and role in development. Autophagy 9:951-972.
82. Hall-Glenn F, Aivazi A, Akopyan L, Ong JR, Baxter RR, Benya PD, Goldschmeding R, van Nieuwenhoven FA, Hunziker EB, Lyons KM. 2013. CCN2/CTGF is required for matrix organization and to protect growth plate chondrocytes from cellular stress. J Cell Commun Signal 7:219-230.
83. Hamamura K, Lin CC, Yokota H. 2013. Salubrinal reduces expression and activity of MMP13 in chondrocytes. Osteoarthritis Cartilage 21:764-772.
84. Han X, Zhou J, Zhang P, Song F, Jiang R, Li M, Xia F, Guo FJ. 2013. IRE1alpha dissociates with BiP and inhibits ER stress-mediated apoptosis in cartilage development. Cell Signal 25:2136-2146.
85. Hartley CL, Edwards S, Mullan L, Bell PA, Fresquet M, Boot-Handford RP, Briggs MD. 2013. Armet/Manf and Creld2 are components of a specialized ER stress response provoked by inappropriate formation of disulphide bonds: implications for genetic skeletal diseases. Hum Mol Genet 22:5262-5275.
86. Hartmann C. 2009. Transcriptional networks controlling skeletal development. Curr Opin Genet Dev 19:437-443.
87. Hasnain SZ, Lourie R, Das I, Chen AC, McGuckin MA. 2012. The interplay between endoplasmic reticulum stress and inflammation. Immunol Cell Biol 90:260-270.
88. Hecht JT, Hayes E, Haynes R, Cole WG. 2005. COMP mutations, chondrocyte function and cartilage matrix. Matrix Biol 23:525-533.
89. Hecht JT, Makitie O, Hayes E, Haynes R, Susic M, Montufar-Solis D, Duke PJ, Cole WG. 2004. Chondrocyte cell death and intracellular distribution of COMP and type IX collagen in the pseudoachondroplasia growth plate. J Orthop Res 22:759-767.
90. Hecht JT, Nelson LD, Crowder E, Wang Y, Elder FF, Harrison WR, Francomano CA, Prange CK, Lennon GG, Deere M, et al. 1995. Mutations in exon 17B of cartilage oligomeric matrix protein (COMP) cause pseudoachondroplasia. Nat Genet 10:325-329.
91. Hintze V, Steplewski A, Ito H, Jensen DA, Rodeck U, Fertala A. 2008. Cells expressing partially unfolded R789C/p.R989C type II procollagen mutant associated with spondyloepiphyseal dysplasia undergo apoptosis. Hum Mutat 29:841-851.
92. Ho MS, Tsang KY, Lo RL, Susic M, Makitie O, Chan TW, Ng VC, Sillence DO, Boot-Handford RP, Gibson G, Cheung KM, Cole WG, Cheah KS, Chan D. 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.
93. Hockemeyer D, Wang H, Kiani S, Lai CS, Gao Q, Cassady JP, Cost GJ, Zhang L, Santiago Y, Miller JC, Zeitler B, Cherone JM, Meng X, Hinkley SJ, Rebar EJ, Gregory PD, Urnov FD, Jaenisch R. 2011. Genetic engineering of human pluripotent cells using TALE nucleases. Nat Biotechnol 29:731-734.
94. Hollien J. 2013. Evolution of the unfolded protein response. Biochim Biophys Acta 1833:2458-2463.
95. Holt DW, Henderson ML, Stockdale CE, Farrell JT, Kooyman DL, Bridgewater LC, Seegmiller RE. 2012. Osteoarthritis-like changes in the heterozygous sedc mouse associated with the HtrA1-Ddr2-Mmp-13 degradative pathway: a new model of osteoarthritis. Osteoarthritis Cartilage 20:430-439.
96. Hoornaert KP, Dewinter C, Vereecke I, Beemer FA, Courtens W, Fryer A, Fryssira H, Lees M, Mullner-Eidenbock A, Rimoin DL, Siderius L, Superti-Furga A, Temple K, Willems PJ, Zankl A, Zweier C, De Paepe A, Coucke P, Mortier GR. 2006. The phenotypic spectrum in patients with arginine to cysteine mutations in the COL2A1 gene. J Med Genet 43:406-413.
97. Hua H, Shang L, Martinez H, Freeby M, Gallagher MP, Ludwig T, Deng L, Greenberg E, Leduc C, Chung WK, Goland R, Leibel RL, Egli D. 2013. iPSC-derived beta cells model diabetes due to glucokinase deficiency. J Clin Invest 123:3146-3153.
98. Hunziker EB. 1994. Mechanism of longitudinal bone growth and its regulation by growth plate chondrocytes. Microsc Res Tech 28:505-519.
99. Ikegawa S, Ohashi H, Nishimura G, Kim KC, Sannohe A, Kimizuka M, Fukushima Y, Nagai T, Nakamura Y. 1998. Novel and recurrent COMP (cartilage oligomeric matrix protein) mutations in pseudoachondroplasia and multiple epiphyseal dysplasia. Hum Genet 103:633-638.
100. Ishida Y, Nagata K. 2009. Autophagy eliminates a specific species of misfolded procollagen and plays a protective role in cell survival against ER stress. Autophagy 5:1217-1219.
101. Ito H, Rucker E, Steplewski A, McAdams E, Brittingham RJ, Alabyeva T, Fertala A. 2005. Guilty by association: some collagen II mutants alter the formation of ECM as a result of atypical interaction with fibronectin. J Mol Biol 352:382-395.
102. Iwawaki T, Oikawa D. 2013. The role of the unfolded protein response in diabetes mellitus. Semin Immunopathol 35:333-350.
103. Izumi S, Saito A, Kanemoto S, Kawasaki N, Asada R, Iwamoto H, Oki M, Miyagi H, Ochi M, Imaizumi K. 2012. The endoplasmic reticulum stress transducer BBF2H7 suppresses apoptosis by activating the ATF5-MCL1 pathway in growth plate cartilage. J Biol Chem 287:36190-36200.
104. Jackson GC, Mittaz-Crettol L, Taylor JA, Mortier GR, Spranger J, Zabel B, Le Merrer M, Cormier-Daire V, Hall CM, Offiah A, Wright MJ, Savarirayan R, Nishimura G, Ramsden SC, Elles R, Bonafe L, Superti-Furga A, Unger S, Zankl A, Briggs MD. 2012. Pseudoachondroplasia and multiple epiphyseal dysplasia: a 7-year comprehensive analysis of the known disease genes identify novel and recurrent mutations and provides an accurate assessment of their relative contribution. Hum Mutat 33:144-157.
105. Joshi M, Kulkarni A, Pal JK. 2013. Small molecule modulators of eukaryotic initiation factor 2alpha kinases, the key regulators of protein synthesis. Biochimie 95:1980-1990.
106. Jung CH, Ro SH, Cao J, Otto NM, Kim DH. 2010. mTOR regulation of autophagy. FEBS Lett 584:1287-1295.
107. Kanazawa H, Tanaka H, Inoue M, Yamanaka Y, Namba N, Seino Y. 2003. Efficacy of growth hormone therapy for patients with skeletal dysplasia. J Bone Miner Metab 21:307-310.
108. Kanbe K, Yang X, Wei L, Sun C, Chen Q. 2007. Pericellular matrilins regulate activation of chondrocytes by cyclic load-induced matrix deformation. J Bone Miner Res 22:318-328.
109. Kang R, Zeh HJ, Lotze MT, Tang D. 2011. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 18:571-580.
110. Kannu P, Bateman JF, Belluoccio D, Fosang AJ, Savarirayan R. 2009. Employing molecular genetics of chondrodysplasias to inform the study of osteoarthritis. Arthritis Rheum 60:325-334.
111. Kaser A, Adolph TE, Blumberg RS. 2013. The unfolded protein response and gastrointestinal disease. Semin Immunopathol 35:307-319.
112. Kaye JA, Finkbeiner S. 2013. Modeling Huntington's disease with induced pluripotent stem cells. Mol Cell Neurosci 56:50-64.
113. Kennedy J, Jackson GC, Barker FS, Nundlall S, Bella J, Wright MJ, Mortier GR, Neas K, Thompson E, Elles R, Briggs MD. 2005. Novel and recurrent mutations in the C-terminal domain of COMP cluster in two distinct regions and result in a spectrum of phenotypes within the pseudoachondroplasia - multiple epiphyseal dysplasia disease group. Hum Mutat 25:593-594.
114. Kim I, Xu W, Reed JC. 2008. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 7:1013-1030.
115. Kincaid MM, Cooper AA. 2007. ERADicate ER stress or die trying. Antioxid Redox Signal 9:2373-2387.
116. Kiskinis E, Eggan K. 2010. Progress toward the clinical application of patient-specific pluripotent stem cells. J Clin Invest 120:51-59.
117. Klatt AR, Becker AK, Neacsu CD, Paulsson M, Wagener R. 2011. The matrilins: modulators of extracellular matrix assembly. Int J Biochem Cell Biol 43:320-330.
118. Klatt AR, Paulsson M, Wagener R. 2002. Expression of matrilins during maturation of mouse skeletal tissues. Matrix Biol 21:289-296.
119. Krakow D, Rimoin DL. 2010. The skeletal dysplasias. Genet Med 12:327-341.
120. Kroemer G, Marino G, Levine B. 2010. Autophagy and the integrated stress response. Mol Cell 40:280-293.
121. Kronenberg HM. 2003. Developmental regulation of the growth plate. Nature 423:332-336.
122. Lamande SR, Chessler SD, Golub SB, Byers PH, Chan D, Cole WG, Sillence DO, Bateman JF. 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.
123. Laustriat D, Gide J, Peschanski M. 2010. Human pluripotent stem cells in drug discovery and predictive toxicology. Biochem Soc Trans 38:1051-1057.
124. Lee B, Vissing H, Ramirez F, Rogers D, Rimoin D. 1989. Identification of the molecular defect in a family with spondyloepiphyseal dysplasia. Science 244:978-980.
125. Leighton MP, Nundlall S, Starborg T, Meadows RS, Suleman F, Knowles L, Wagener R, Thornton DJ, Kadler KE, Boot-Handford RP, Briggs MD. 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.
126. Levine B, Klionsky DJ. 2004. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 6:463-477.
127. Li H, Zhang XY, Wu TJ, Cheng W, Liu X, Jiang TT, Wen J, Li J, Ma QL, Hua ZC. 2013. Endoplasmic reticulum stress regulates rat mandibular cartilage thinning under compressive mechanical stress. J Biol Chem 288:18172-18183.
128. Li SW, Prockop DJ, Helminen H, Fassler R, Lapvetelainen T, Kiraly K, Peltarri A, Arokoski J, Lui H, Arita M, et al. 1995. Transgenic mice with targeted inactivation of the Col2 alpha 1 gene for collagen II develop a skeleton with membranous and periosteal bone but no endochondral bone. Genes Dev 9:2821-2830.
129. Lie CW, Chow W. 2009. Limb lengthening in short-stature patients using monolateral and circular external fixators. Hong Kong Med J 15:280-284.
130. Lisse TS, Thiele F, Fuchs H, Hans W, Przemeck GK, Abe K, Rathkolb B, Quintanilla-Martinez L, Hoelzlwimmer G, Helfrich M, Wolf E, Ralston SH, Hrabe de Angelis M. 2008. ER stress-mediated apoptosis in a new mouse model of osteogenesis imperfecta. PLoS Genet 4:e7.
131. Liu Y, Zhou J, Zhao W, Li X, Jiang R, Liu C, Guo FJ. 2012. XBP1S associates with RUNX2 and regulates chondrocyte hypertrophy. J Biol Chem 287:34500-34513.
132. Lomas C, Tang XD, Chanalaris A, Saklatvala J, Vincent TL. 2011. Cyclic mechanical load causes global translational arrest in articular chondrocytes: a process which is partially dependent upon PKR phosphorylation. Eur Cell Mater 22:178-189.
133. Long F, Ornitz DM. 2013. Development of the endochondral skeleton. Cold Spring Harb Perspect Biol 5:a008334.
134. Lorget F, Kaci N, Peng J, Benoist-Lasselin C, Mugniery E, Oppeneer T, Wendt DJ, Bell SM, Bullens S, Bunting S, Tsuruda LS, O'Neill CA, Di Rocco F, Munnich A, Legeai-Mallet L. 2012. Evaluation of the therapeutic potential of a CNP analog in a Fgfr3 mouse model recapitulating achondroplasia. Am J Hum Genet 91:1108-1114.
135. Lotz MK, Carames B. 2011. Autophagy and cartilage homeostasis mechanisms in joint health, aging and OA. Nat Rev Rheumatol 7:579-587.
136. Luo Y, Fan Y, Chen X, Yue L, Yu B, Li Q, Chen Y, Sun X. 2014. Modeling induced pluripotent stem cells from fibroblasts of Duchenne muscular dystrophy patients. Int J Neurosci 124:12-21.
137. LuValle P, Hayashi M, Olsen BR. 1989. Transcriptional regulation of type X collagen during chondrocyte maturation. Dev Biol 133:613-616.
138. Maattanen P, Gehring K, Bergeron JJ, Thomas DY. 2010. Protein quality control in the ER: the recognition of misfolded proteins. Semin Cell Dev Biol 21:500-511.
139. Macdonald DW, Squires RS, Avery SA, Adams J, Baker M, Cunningham CR, Heimann NB, Kooyman DL, Seegmiller RE. 2013. Structural variations in articular cartilage matrix are associated with early-onset osteoarthritis in the spondyloepiphyseal dysplasia congenita (sedc) mouse. Int J Mol Sci 14:16515-16531.
140. Mackie EJ, Tatarczuch L, Mirams M. 2011. The skeleton: a multi-functional complex organ: the growth plate chondrocyte and endochondral ossification. J Endocrinol 211:109-121.
141. Maes C. 2013. Role and regulation of vascularization processes in endochondral bones. Calcif Tissue Int 92:307-323.
142. Makitie O, Susic M, Ward L, Barclay C, Glorieux FH, Cole WG. 2005. Schmid type of metaphyseal chondrodysplasia and COL10A1 mutations-findings in 10 patients. Am J Med Genet A 137A:241-248.
143. Malemud CJ. 2006. Matrix metalloproteinases: role in skeletal development and growth plate disorders. Front Biosci 11:1702-1715.
144. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM. 2013. RNA-guided human genome engineering via Cas9. Science 339:823-826.
145. Merritt TM, Bick R, Poindexter BJ, Alcorn JL, Hecht JT. 2007. Unique matrix structure in the rough endoplasmic reticulum cisternae of pseudoachondroplasia chondrocytes. Am J Pathol 170:293-300.
146. Metsaranta M, Garofalo S, Decker G, Rintala M, de Crombrugghe B, Vuorio E. 1992. Chondrodysplasia in transgenic mice harboring a 15-amino acid deletion in the triple helical domain of pro alpha 1(II) collagen chain. J Cell Biol 118:203-212.
147. Mier RJ, Holderbaum D, Ferguson R, Moskowitz R. 2001. Osteoarthritis in children associated with a mutation in the type II procollagen gene (COL2A1). Mol Genet Metab 74:338-341.
148. Moreno JA, Halliday M, Molloy C, Radford H, Verity N, Axten JM, Ortori CA, Willis AE, Fischer PM, Barrett DA, Mallucci GR. 2013. Oral treatment targeting the unfolded protein response prevents neurodegeneration and clinical disease in prion-infected mice. Sci Transl Med 5:206ra138.
149. Mori K. 2009. Signalling pathways in the unfolded protein response: development from yeast to mammals. J Biochem 146:743-750.
150. Mortier GR, Weis M, Nuytinck L, King LM, Wilkin DJ, De Paepe A, Lachman RS, Rimoin DL, Eyre DR, Cohn DH. 2000. Report of five novel and one recurrent COL2A1 mutations with analysis of genotype-phenotype correlation in patients with a lethal type II collagen disorder. J Med Genet 37:263-271.
151. Mou X, Wu Y, Cao H, Meng Q, Wang Q, Sun C, Hu S, Ma Y, Zhang H. 2012. Generation of disease-specific induced pluripotent stem cells from patients with different karyotypes of Down syndrome. Stem Cell Res Ther 3:14.
152. Neacsu CD, Ko YP, Tagariello A, Rokenes Karlsen K, Neiss WF, Paulsson M, Wagener R. 2014. Matrilin-1 is essential for zebrafish development by facilitating collagen II secretion. J Biol Chem 289:1505-1518.
153. Ni M, Lee AS. 2007. ER chaperones in mammalian development and human diseases. FEBS Lett 581:3641-3651.
154. Nsair A, MacLellan WR. 2011. Induced pluripotent stem cells for regenerative cardiovascular therapies and biomedical discovery. Adv Drug Deliv Rev 63:324-330.
155. Nugent AE, Speicher DM, Gradisar I, McBurney DL, Baraga A, Doane KJ, Horton WE Jr. 2009. Advanced osteoarthritis in humans is associated with altered collagen VI expression and upregulation of ER-stress markers Grp78 and bag-1. J Histochem Cytochem 57:923-931.
156. Nundlall S, Rajpar MH, Bell PA, Clowes C, Zeeff LA, Gardner B, Thornton DJ, Boot-Handford RP, Briggs MD. 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.
157. O'Neill AC, Ricardo SD. 2013. Human kidney cell reprogramming: applications for disease modeling and personalized medicine. J Am Soc Nephrol 24:1347-1356.
158. Oda Y, Okada T, Yoshida H, Kaufman RJ, Nagata K, Mori K. 2006. Derlin-2 and Derlin-3 are regulated by the mammalian unfolded protein response and are required for ER-associated degradation. J Cell Biol 172:383-393.
159. Okita K, Yamakawa T, Matsumura Y, Sato Y, Amano N, Watanabe A, Goshima N, Yamanaka S. 2013. An efficient nonviral method to generate integration-free human-induced pluripotent stem cells from cord blood and peripheral blood cells. Stem Cells 31:458-466.
160. Olsen BR. 1995. Mutations in collagen genes resulting in metaphyseal and epiphyseal dysplasias. Bone 17:45S-49S.
161. Ornitz DM. 2005. FGF signaling in the developing endochondral skeleton. Cytokine Growth Factor Rev 16:205-213.
162. Osorio F, Lambrecht B, Janssens S. 2013. The UPR and lung disease. Semin Immunopathol 35:293-306.
163. Otten C, Hansen U, Talke A, Wagener R, Paulsson M, Zaucke F. 2010. A matrilin-3 mutation associated with osteoarthritis does not affect collagen affinity but promotes the formation of wider cartilage collagen fibrils. Hum Mutat 31:254-263.
164. Otten C, Wagener R, Paulsson M, Zaucke F. 2005. Matrilin-3 mutations that cause chondrodysplasias interfere with protein trafficking while a mutation associated with hand osteoarthritis does not. J Med Genet 42:774-779.
165. Pace JM, Li Y, Seegmiller RE, Teuscher C, Taylor BA, Olsen BR. 1997. Disproportionate micromelia (Dmm) in mice caused by a mutation in the C-propeptide coding region of Col2a1. Dev Dyn 208:25-33.
166. Papa FR. 2012. Endoplasmic reticulum stress, pancreatic beta-cell degeneration, and diabetes. Cold Spring Harb Perspect Med 2:a007666.
167. Patra D, Xing X, Davies S, Bryan J, Franz C, Hunziker EB, Sandell LJ. 2007. Site-1 protease is essential for endochondral bone formation in mice. J Cell Biol 179:687-700.
168. Pirog-Garcia KA, Meadows RS, Knowles L, Heinegard D, Thornton DJ, Kadler KE, Boot-Handford RP, Briggs MD. 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.
169. Pirog KA, Irman A, Young S, Halai P, Bell PA, Boot-Handford RP, Briggs MD. 2014. Abnormal Chondrocyte Apoptosis in the Cartilage Growth Plate is Influenced by Genetic Background and Deletion of CHOP in a Targeted Mouse Model of Pseudoachondroplasia. PLoS One 9:e85145.
170. Pogue R, Lyons K. 2006. BMP signaling in the cartilage growth plate. Curr Top Dev Biol 76:1-48.
171. Posey KL, Coustry F, Veerisetty AC, Liu P, Alcorn JL, Hecht JT. 2012. Chop (Ddit3) is essential for D469del-COMP retention and cell death in chondrocytes in an inducible transgenic mouse model of pseudoachondroplasia. Am J Pathol 180:727-737.
172. Posey KL, Coustry F, Veerisetty AC, Liu P, Alcorn JL, Hecht JT. 2013. Chondrocyte-specific pathology during skeletal growth and therapeutics in a murine model of pseudoachondroplasia. J Bone Miner Res [Epub ahead of print].
173. Posey KL, Veerisetty AC, Liu P, Wang HR, Poindexter BJ, Bick R, Alcorn JL, Hecht JT. 2009. An inducible cartilage oligomeric matrix protein mouse model recapitulates human pseudoachondroplasia phenotype. Am J Pathol 175:1555-1563.
174. Posey KL, Yang Y, Veerisetty AC, Sharan SK, Hecht JT. 2008. Model systems for studying skeletal dysplasias caused by TSP-5/COMP mutations. Cell Mol Life Sci 65:687-699.
175. Price J, Zaidi AK, Bohensky J, Srinivas V, Shapiro IM, Ali H. 2010. Akt-1 mediates survival of chondrocytes from endoplasmic reticulum-induced stress. J Cell Physiol 222:502-508.
176. Prockop DJ. 1984. Osteogenesis imperfecta: phenotypic heterogeneity, protein suicide, short and long collagen. Am J Hum Genet 36:499-505.
177. Provot S, Schipani E. 2005. Molecular mechanisms of endochondral bone development. Biochem Biophys Res Commun 328:658-665.
178. Rajpar MH, McDermott B, Kung L, Eardley R, Knowles L, Heeran M, Thornton DJ, Wilson R, Bateman JF, Poulsom R, Arvan P, Kadler KE, Briggs MD, Boot-Handford RP. 2009. Targeted induction of endoplasmic reticulum stress induces cartilage pathology. PLoS Genet 5:e1000691.
179. Ribeiro CM, O'Neal WK. 2012. Endoplasmic reticulum stress in chronic obstructive lung diseases. Curr Mol Med 12:872-882.
180. Ricard-Blum S, Dublet B, Van der Rest M. 2000. Unconventional collagens: types VI, VII, VIII, IX, X, XII, XIV, XVI, and XIX. New York: Oxford University Press. xv, 155 p.
181. Richards AJ, Morgan J, Bearcroft PW, Pickering E, Owen MJ, Holmans P, Williams N, Tysoe C, Pope FM, Snead MP, Hughes H. 2002. Vitreoretinopathy with phalangeal epiphyseal dysplasia, a type II collagenopathy resulting from a novel mutation in the C-propeptide region of the molecule. J Med Genet 39:661-665.
182. Ricks ML, Farrell JT, Falk DJ, Holt DW, Rees M, Carr J, Williams T, Nichols BA, Bridgewater LC, Reynolds PR, Kooyman DL, Seegmiller RE. 2013. Osteoarthritis in temporomandibular joint of Col2a1 mutant mice. Arch Oral Biol 58:1092-1099.
183. Rimoin DL, Rasmussen IM, Briggs MD, Roughley PJ, Gruber HE, Warman ML, Olsen BR, Hsia YE, Yuen J, Reinker K, 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.
184. Ritvaniemi P, Korkko J, Bonaventure J, Vikkula M, Hyland J, Paassilta P, Kaitila I, Kaariainen H, Sokolov BP, Hakala M, et al. 1995. Identification of COL2A1 gene mutations in patients with chondrodysplasias and familial osteoarthritis. Arthritis Rheum 38:999-1004.
185. Rochet JC. 2007. Novel therapeutic strategies for the treatment of protein-misfolding diseases. Expert Rev Mol Med 9:1-34.
186. Rock MJ, Holden P, Horton WA, Cohn DH. 2010. Cartilage oligomeric matrix protein promotes cell attachment via two independent mechanisms involving CD47 and alphaVbeta3 integrin. Mol Cell Biochem 338:215-224.
187. Rodriguez D, Rojas-Rivera D, Hetz C. 2011. Integrating stress signals at the endoplasmic reticulum: the BCL-2 protein family rheostat. Biochim Biophys Acta 1813:564-574.
188. Rosati R, Horan GS, Pinero GJ, Garofalo S, Keene DR, Horton WA, Vuorio E, de Crombrugghe B, Behringer RR. 1994. Normal long bone growth and development in type X collagen-null mice. Nat Genet 8:129-135.
189. Rubinsztein DC, Codogno P, Levine B. 2012. Autophagy modulation as a potential therapeutic target for diverse diseases. Nat Rev Drug Discov 11:709-730.
190. Sahlman J, Pitkanen MT, Prockop DJ, Arita M, Li SW, Helminen HJ, Langsjo TK, Puustjarvi K, Lammi MJ. 2004. A human COL2A1 gene with an Arg519Cys mutation causes osteochondrodysplasia in transgenic mice. Arthritis Rheum 50:3153-3160.
191. Saito A, Kanemoto S, Zhang Y, Asada R, Hino K, Imaizumi K. 2014. Chondrocyte proliferation regulated by secreted luminal domain of ER stress transducer BBF2H7/CREB3L2. Mol Cell 53:127-139.
192. Saitta B, Passarini J, Sareen D, Ornelas L, Sahabian A, Argade S, Krakow D, Cohn DH, Svendsen CN, Rimoin DL. 2014. Patient-derived skeletal dysplasia iPSCs display abnormal chondrogenic marker expression and regulation by BMP2 and TGFbeta1. Stem Cells Dev [Epub ahead of print].
193. Sanchez-Danes A, Benzoni P, Memo M, Dell'era P, Raya A, Consiglio A. 2013. Induced pluripotent stem cell-based studies of Parkinson's disease: challenges and promises. CNS Neurol Disord Drug Targets 12:1114-1127.
194. Savendahl L. 2005. Hormonal regulation of growth plate cartilage. Horm Res 64(suppl 2):94-97.
195. Schmitz M, Niehoff A, Miosge N, Smyth N, Paulsson M, Zaucke F. 2008. Transgenic mice expressing D469Delta mutated cartilage oligomeric matrix protein (COMP) show growth plate abnormalities and sternal malformations. Matrix Biol 27:67-85.
196. Scotti C, Piccinini E, Takizawa H, Todorov A, Bourgine P, Papadimitropoulos A, Barbero A, Manz MG, Martin I. 2013. Engineering of a functional bone organ through endochondral ossification. Proc Natl Acad Sci U S A 110:3997-4002.
197. Scotti C, Tonnarelli B, Papadimitropoulos A, Scherberich A, Schaeren S, Schauerte A, Lopez-Rios J, Zeller R, Barbero A, Martin I. 2010. Recapitulation of endochondral bone formation using human adult mesenchymal stem cells as a paradigm for developmental engineering. Proc Natl Acad Sci U S A 107:7251-7256.
198. Seegmiller RE, Bomsta BD, Bridgewater LC, Niederhauser CM, Montano C, Sudweeks S, Eyre DR, Fernandes RJ. 2008. The heterozygous disproportionate micromelia (dmm) mouse: morphological changes in fetal cartilage precede postnatal dwarfism and compared with lethal homozygotes can explain the mild phenotype. J Histochem Cytochem 56:1003-1011.
199. Serra R, Chang C. 2003. TGF-beta signaling in human skeletal and patterning disorders. Birth Defects Res C Embryo Today 69:333-351.
200. Settembre C, Arteaga-Solis E, McKee MD, de Pablo R, Al Awqati Q, Ballabio A, Karsenty G. 2008. Proteoglycan desulfation determines the efficiency of chondrocyte autophagy and the extent of FGF signaling during endochondral ossification. Genes Dev 22:2645-2650.
201. Smits P, Bolton AD, Funari V, Hong M, Boyden ED, Lu L, Manning DK, Dwyer ND, Moran JL, Prysak M, Merriman B, Nelson SF, Bonafe L, Superti-Furga A, Ikegawa S, Krakow D, Cohn DH, Kirchhausen T, Warman ML, Beier DR. 2010. Lethal skeletal dysplasia in mice and humans lacking the golgin GMAP-210. N Engl J Med 362:206-216.
202. So CL, Kaluarachchi K, Tam PP, Cheah KS. 2001. Impact of mutations of cartilage matrix genes on matrix structure, gene activity and chondrogenesis. Osteoarthritis Cartilage 9(suppl A):S160-S173.
203. Sovolyova N, Healy S, Samali A, Logue SE. 2014. Stressed to death - mechanisms of ER stress-induced cell death. Biol Chem 395:1-13.
204. Srinivas V, Bohensky J, Shapiro IM. 2009. Autophagy: a new phase in the maturation of growth plate chondrocytes is regulated by HIF, mTOR and AMP kinase. Cells Tissues Organs 189:88-92.
205. St-Jacques B, Hammerschmidt M, McMahon AP. 1999. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev 13:2072-2086.
206. Sternberg H, Murai JT, Erickson IE, Funk WD, Das S, Wang Q, Snyder E, Chapman KB, Vangsness CT Jr, West MD. 2012. A human embryonic stem cell-derived clonal progenitor cell line with chondrogenic potential and markers of craniofacial mesenchyme. Regen Med 7:481-501.
207. Suh DH, Kim MK, Kim HS, Chung HH, Song YS. 2012. Unfolded protein response to autophagy as a promising druggable target for anticancer therapy. Ann N Y Acad Sci 1271:20-32.
208. Suleman F, Gualeni B, Gregson HJ, Leighton MP, Pirog KA, Edwards S, Holden P, Boot-Handford RP, Briggs MD. 2012. A novel form of chondrocyte stress is triggered by a COMP mutation causing pseudoachondroplasia. Hum Mutat 33:218-231.
209. Sulko J, Czarny-Ratajczak M, Wozniak A, Latos-Bielenska A, Kozlowski K. 2005. Novel amino acid substitution in the Y-position of collagen type II causes spondyloepimetaphyseal dysplasia congenita. Am J Med Genet A 137A:292-297.
210. Szabat M, Kalynyak TB, Lim GE, Chu KY, Yang YH, Asadi A, Gage BK, Ao Z, Warnock GL, Piret JM, Kieffer TJ, Johnson JD. 2011. Musashi expression in beta-cells coordinates insulin expression, apoptosis and proliferation in response to endoplasmic reticulum stress in diabetes. Cell Death Dis 2:e232.
211. Takada K, Hirose J, Senba K, Yamabe S, Oike Y, Gotoh T, Mizuta H. 2011. Enhanced apoptotic and reduced protective response in chondrocytes following endoplasmic reticulum stress in osteoarthritic cartilage. Int J Exp Pathol 92:232-242.
212. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. 2007. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861-872.
213. Tiller GE, Weis MA, Polumbo PA, Gruber HE, Rimoin DL, Cohn DH, Eyre DR. 1995. An RNA-splicing mutation (G+5IVS20) in the type II collagen gene (COL2A1) in a family with spondyloepiphyseal dysplasia congenita. Am J Hum Genet 56:388-395.
214. Tomasio SM, Harding HP, Ron D, Cross BC, Bond PJ. 2013. Selective inhibition of the unfolded protein response: targeting catalytic sites for Schiff base modification. Mol Biosyst 9:2408-2416.
215. Treble NJ, Jensen FO, Bankier A, Rogers JG, Cole WG. 1990. Development of the hip in multiple epiphyseal dysplasia. Natural history and susceptibility to premature osteoarthritis. J Bone Joint Surg Br 72:1061-1064.
216. 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.
217. Tsang KY, Chan D, Cheslett D, Chan WC, So CL, Melhado IG, Chan TW, Kwan KM, Hunziker EB, Yamada Y, Bateman JF, Cheung KM, Cheah KS. 2007. Surviving endoplasmic reticulum stress is coupled to altered chondrocyte differentiation and function. PLoS Biol 5:e44.
218. Unger S, Korkko J, Krakow D, Lachman RS, Rimoin DL, Cohn DH. 2001. Double heterozygosity for pseudoachondroplasia and spondyloepiphyseal dysplasia congenita. Am J Med Genet 104:140-146.
219. Vortkamp A, Lee K, Lanske B, Segre GV, Kronenberg HM, Tabin CJ. 1996. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 273:613-622.
220. Vranka J, Mokashi A, Keene DR, Tufa S, Corson G, Sussman M, Horton WA, Maddox K, Sakai L, Bachinger HP. 2001. Selective intracellular retention of extracellular matrix proteins and chaperones associated with pseudoachondroplasia. Matrix Biol 20:439-450.
221. Walter P, Ron D. 2011. The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:1081-1086.
222. Warman ML, Abbott M, Apte SS, Hefferon T, McIntosh I, Cohn DH, Hecht JT, Olsen BR, Francomano CA. 1993. A type X collagen mutation causes Schmid metaphyseal chondrodysplasia. Nat Genet 5:79-82.
223. Warman ML, Cormier-Daire V, Hall C, Krakow D, Lachman R, LeMerrer M, Mortier G, Mundlos S, Nishimura G, Rimoin DL, Robertson S, Savarirayan R, Sillence D, Spranger J, Unger S, Zabel B, Superti-Furga A. 2011. Nosology and classification of genetic skeletal disorders: 2010 revision. Am J Med Genet A 155A:943-968.
224. Williams CJ, Considine EL, Knowlton RG, Reginato A, Neumann G, Harrison D, Buxton P, Jimenez S, Prockop DJ. 1993. Spondyloepiphyseal dysplasia and precocious osteoarthritis in a family with an Arg75->Cys mutation in the procollagen type II gene (COL2A1). Hum Genet 92:499-505.
225. 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.
226. Wouters BG, Koritzinsky M. 2008. Hypoxia signalling through mTOR and the unfolded protein response in cancer. Nat Rev Cancer 8:851-864.
227. Xia X, Cui Y, Huang Y, Pan L, Wu Y, Zhang P, Jin B. 2007. A first familial G504S mutation of COL2A1 gene results in distinctive spondyloepiphyseal dysplasia congenita. Clin Chim Acta 382:148-150.
228. Xu XH, Zhong Z. 2013. Disease modeling and drug screening for neurological diseases using human induced pluripotent stem cells. Acta Pharmacol Sin 34:755-764.
229. Yagi T, Ito D, Okada Y, Akamatsu W, Nihei Y, Yoshizaki T, Yamanaka S, Okano H, Suzuki N. 2011. Modeling familial Alzheimer's disease with induced pluripotent stem cells. Hum Mol Genet 20:4530-4539.
230. Yang SL, Harnish E, Leeuw T, Dietz U, Batchelder E, Wright PS, Peppard J, August P, Volle-Challier C, Bono F, Herbert JM, Izpisua Belmonte JC. 2012. Compound screening platform using human induced pluripotent stem cells to identify small molecules that promote chondrogenesis. Protein Cell 3:934-942.
231. Yi F, Liu GH, Izpisua Belmonte JC. 2012. Human induced pluripotent stem cells derived hepatocytes: rising promise for disease modeling, drug development and cell therapy. Protein Cell 3:246-250.
232. Yoshida CA, Komori T. 2005. Role of Runx proteins in chondrogenesis. Crit Rev Eukaryot Gene Expr 15:243-254.
233. Yoshida H, Okada T, Haze K, Yanagi H, Yura T, Negishi M, Mori K. 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.
234. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin, II, Thomson JA. 2007. Induced pluripotent stem cell lines derived from human somatic cells. Science 318:1917-1920.
235. Yu SJ, Yoon JH, Yang JI, Cho EJ, Kwak MS, Jang ES, Lee JH, Kim YJ, Lee HS, Kim CY. 2012. Enhancement of hexokinase II inhibitor-induced apoptosis in hepatocellular carcinoma cells via augmenting ER stress and anti-angiogenesis by protein disulfide isomerase inhibition. J Bioenerg Biomembr 44:101-115.
236. Yu YQ, Liu LC, Wang FC, Liang Y, Cha DQ, Zhang JJ, Shen YJ, Wang HP, Fang S, Shen YX. 2010. Induction profile of MANF/ARMET by cerebral ischemia and its implication for neuron protection. J Cereb Blood Flow Metab 30:79-91.
237. Zabel B, Hilbert K, Stoss H, Superti-Furga A, Spranger J, Winterpacht A. 1996. A specific collagen type II gene (COL2A1) mutation presenting as spondyloperipheral dysplasia. Am J Med Genet 63:123-128.
238. Zankl A, Zabel B, Hilbert K, Wildhardt G, Cuenot S, Xavier B, Ha-Vinh R, Bonafe L, Spranger J, Superti-Furga A. 2004. Spondyloperipheral dysplasia is caused by truncating mutations in the C-propeptide of COL2A1. Am J Med Genet A 129A:144-148.
239. Zhou T, Benda C, Dunzinger S, Huang Y, Ho JC, Yang J, Wang Y, Zhang Y, Zhuang Q, Li Y, Bao X, Tse HF, Grillari J, Grillari-Voglauer R, Pei D, Esteban MA. 2012. Generation of human induced pluripotent stem cells from urine samples. Nat Protoc 7:2080-2089.