Hypertrophic Chondrocytes Have a Limited Capacity to Cope with Increases in Endoplasmic Reticulum Stress without Triggering the Unfolded Protein Response

Journal of Histochemistry and Cytochemistry

Volumn 60, Issue 10, 2012, Pages 734-748

  Kung, Louise H W ^a   Rajpar, M Helen ^b   Briggs, Michael D ^c   Boot Handford, Raymond P ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

BiP (Grp78); cartilage; chondrodysplasia; collagen X; endoplasmic reticulum stress; growth plate; hypertrophic chondrocyte; unfolded protein response

Indexed keywords

COLLAGEN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CHONDRODYSPLASIA; EMBRYO; ENDOPLASMIC RETICULUM STRESS; GENE MUTATION; HETEROZYGOTE; MOUSE; MUTANT; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL; UNFOLDED PROTEIN RESPONSE;

ANIMALS; CELL SIZE; CHONDROCYTES; COLLAGEN TYPE X; EMBRYO, MAMMALIAN; ENDOPLASMIC RETICULUM STRESS; GENE DOSAGE; GROWTH PLATE; HEMIZYGOTE; HOMOZYGOTE; MICE; MICE, MUTANT STRAINS; MUTATION; OSTEOCHONDRODYSPLASIAS; OSTEOCLASTS; OSTEOGENESIS; TRANSGENES; UNFOLDED PROTEIN RESPONSE;

EID: 84869819771     PISSN: 00221554     EISSN: None     Source Type: Journal    
DOI: 10.1369/0022155412458436     Document Type: Article

References (31)

1. Bateman JF,Wilson R,Freddi S,Lamande SR,Savarirayan R.Mutations of COL10A1 in Schmid metaphyseal chondrodysplasia.Hum Mutat. 2005;25 (6): 525-534.
2. Boot-Handford RP,Briggs MD.The unfolded protein response and its relevance to connective tissue diseases.Cell Tissue Res. 2010;339:197-211.
3. Cameron TL,Bell KM,Tatarczuch L,Mackie EJ,Rajpar MH,McDermott BT,Boot-Handford RP,Bateman JF.Transcriptional profiling of chondrodysplasia growth plate cartilage reveals adaptive ER-stress networks that allow survival but disrupt hypertrophy.PLoS ONE. 2011;6 (9): e24600.
4. Engin F,Hotamisligil GS.Restoring endoplasmic reticulum function by chemical chaperones: an emerging therapeutic approach for metabolic diseases.Diabetes Obes Metab. 2010;12:108-115.
5. Ho MSP,Tsang KY,Lo RL,Susic M,Makitie O,Chan TW,Ng VC,Sillence DO,Boot-Handford RP,Gibson G, et al.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. 2007;16 (10): 1201-1215.
6. Karsenty G.The complexities of skeletal biology.Nature. 2003;423 (6937): 316-318.
7. Karsenty G.Transcriptional control of skeletogenesis.Annu Rev Genomics Hum Genet. 2008;9:183-196.
8. Karsenty G,Kronenberg HM,Settembre C.Genetic control of bone formation.Ann Rev Cell Dev Biol. 2009;25:629-648.
9. Kronenberg HM.Developmental regulation of the growth plate.Nature. 2003;423 (6937): 332-336.
10. Lee AS.The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress.Methods. 2005;35:373-381.
11. Lin JH,Walter P,Yen TB.Endoplasmic reticulum stress in disease pathogenesis.Annu Rev Pathol-Mech. 2008;3 (1): 399-425.
12. Mackie EJ,Ahmed YA,Tatarczuch L,Chen KS,Mirams M.Endochondral ossification: how cartilage is converted into bone in the developing skeleton.Int J Biochem Cell Biol. 2008;40 (1): 46-62.
13. Malhotra JD,Kaufman RJ.The endoplasmic reticulum and the unfolded protein response.Semin Cell Dev Biol. 2007;18 (6): 716-731.
14. McLaughlin SH,Conn SN,Bulleid NJ.Folding and assembly of type X collagen mutants that cause metaphyseal chondrodysplasia-type Schmid: evidence for co-assembly of the mutant and wild-type chains and binding to molecular chaperones.J Biol Chem. 1999;274:7570-7575.
15. Newman B,Wallis GA.Skeletal dysplasias caused by a disruption of skeletal patterning and endochondral ossification.Clin Genet. 2003;63 (4): 241-251.
16. Papp E,Csermely P.Chemical chaperones: mechanisms of action and potential use.Handb Exp Pharmacol. 2006;172:405-416.
17. Patra D,Xing X,Davies S,Bryan J,Franz C,Hunziker EB,Sandell LJ.Site-1 protease is essential for endochondral bone formation in mice.J Cell Biol. 2007;179 (4): 687-700.
18. Provot S,Schipani E.Molecular mechanisms of endochondral bone development.Biochem Biophys Res Commun. 2005;328 (3): 658-665.
19. Provot S,Schipani E.Fetal growth plate: a developmental model of cellular adaptation to hypoxia.Ann N Y Acad Sci. 2007;1117:26-39.
20. Rajpar MH,McDermott B,Kung L,Eardley R,Knowles L,Heeran M,Thornton DJ,Wilson R,Bateman JF,Poulsom R, et al.Targeted induction of endoplasmic reticulum stress induces cartilage pathology.PLoS Genet. 2009;5 (10): e1000691.
21. Ron D,Walter P.Signal integration in the endoplasmic reticulum unfolded protein response.Nat Rev Mol Cell Biol. 2007;8 (7): 519-529.
22. Saito A,Hino S,Murakami T,Kanemoto S,Kondo S,Saitoh M,Nishimura R,Yoneda T,Furuichi T,Ikegawa S, et al.Regulation of endoplasmic reticulum stress response by a BBF2H7-mediated Sec23a pathway is essential for chondrogenesis.Nat Cell Biol. 2009;11:1197-1204.
23. Samali A,FitzGerald U,Deegan S,Gupta S.Methods for monitoring endoplasmic reticulum stress and the unfolded protein response.Int J Cell Biol. 2010;2010:830307.
24. Schmid TM,Linsenmayer TF.Immunohistochemical localization of short chain cartilage collagen (type X) in avian tissues.J Cell Biol. 1985;100 (2): 598-605.
25. Tabas I,Ron D.Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress.Nat Cell Biol. 2011;13:184-190.
26. Tsang KY,Chan D,Cheslett D,Chan WCW,So CL,Melhado IG,Chan TWY,Kwan KM,Hunziker EB,Yamada Y, et al.Surviving endoplasmic reticulum stress is coupled to altered chondrocyte differentiation and function.PLoS Biol. 2007;5 (3): e44.
27. Wallis GA,Rash B,Sweetman WA,Thomas JT,Super M,Evans G,Grant ME,Boot-Handford RP.Amino acid substitutions of conserved residues in the carboxyl-terminal domain of the a1 chain of type X collagen occur in two unrelated families with metaphyseal chondrodysplasia type Schmid.Am J Hum Genet. 1994;54:169-178.
28. Warman ML,Abbott M,Apte SS,Hefferon T,McIntosh I,Cohn DH,Hecht JT,Olsen BR,Francomano CA.A type X collagen mutation causes Schmid metaphyseal chondrodysplasia.Nat Genet. 1993;5:79-82.
29. Warman ML,Cormier-Daire V,Hall C,Krakow D,Lachman R,LeMerrer M,Mortier G,Mundlos S,Nishimura G,Rimoin DL, et al.Nosology and classification of genetic skeletal disorders: 2010 revision.Am J Med Genet. 2011;155A:943-968.
30. Wilson R,Freddi S,Bateman JF.Collagen X chains harboring Schmid metaphyseal chondrodysplasia NC1 domain mutations are selectively retained and degraded in stably transfected cells.J Biol Chem. 2002;277:12516-12524.
31. Wilson R,Freddi S,Chan D,Cheah KS,Bateman JF.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. 2005;280:15544-15552.