Mechanisms of aberrant organization of growth plates in conditional transgenic mouse model of spondyloepiphyseal dysplasia associated with the R992C substitution in collagen II

American Journal of Pathology

Volumn 185, Issue 1, 2015, Pages 214-229

  Arita, Machiko ^a   Fertala, Jolanta ^a   Hou, Cheryl ^a   Steplewski, Andrzej ^a   Fertala, Andrzej ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 10; COLLAGEN TYPE 2; GLUCOSE REGULATED PROTEIN 78; COL2A1 PROTEIN, MOUSE;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREEDING; CARTILAGE CELL; CELL POLARITY; CELL PROLIFERATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYMATIC DEGRADATION; EUKARYOTIC FLAGELLUM; EXTRACELLULAR SPACE; FEMALE; GENE DOSAGE; GENE EXPRESSION; GENE MUTATION; GENETIC VARIABILITY; GOLGI COMPLEX; GROWTH PLATE; HETEROZYGOTE; HISTOLOGY; IMMUNOHISTOCHEMISTRY; LUMBAR VERTEBRA; MALE; MOUSE; NEWBORN; NONHUMAN; POLYMERASE CHAIN REACTION; PROGENY; SKELETON; SPONDYLOEPIPHYSEAL DYSPLASIA; TISSUE SPECIFICITY; ANIMAL; CARTILAGE; CHONDRODYSPLASIA; CONGENITAL MALFORMATION; CROSS BREEDING; CYTOLOGY; DISEASE MODEL; GENETICS; GENOTYPE; METABOLISM; MUTATION; TRANSGENE; TRANSGENIC MOUSE;

AMINO ACID SUBSTITUTION; ANIMALS; CARTILAGE; CELL PROLIFERATION; CHONDROCYTES; CILIA; COLLAGEN TYPE II; CROSSES, GENETIC; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM STRESS; GENETIC VARIATION; GENOTYPE; GROWTH PLATE; MICE; MICE, TRANSGENIC; MUTATION; OSTEOCHONDRODYSPLASIAS; TRANSGENES;

EID: 84918830147     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2014.09.003     Document Type: Article

References (65)

1. R.T. Ballock, and R.J. O'Keefe The biology of the growth plate J Bone Joint Surg Am 85-A 2003 715 726
2. R.E. Burgeson, and D.W. Hollister Collagen heterogeneity in human cartilage: identification of several new collagen chains Biochem Biophys Res Commun 87 1979 1124 1131
3. D. Eyre Collagen of articular cartilage Arthritis Res 4 2002 30 35
4. U.K. Blaschke, E.F. Eikenberry, D.J. Hulmes, H.J. Galla, and P. Bruckner Collagen XI nucleates self-assembly and limits lateral growth of cartilage fibrils J Biol Chem 275 2000 10370 10378
5. R. Hagg, P. Bruckner, and E. Hedbom Cartilage fibrils of mammals are biochemically heterogeneous: differential distribution of decorin and collagen IX J Cell Biol 142 1998 285 294
6. V. Lefebvre, and P. Bhattaram Vertebrate skeletogenesis Curr Top Dev Biol 90 2010 291 317
7. E.J. Mackie, L. Tatarczuch, and M. Mirams The skeleton: a multi-functional complex organ: the growth plate chondrocyte and endochondral ossification J Endocrinol 211 2011 109 121
8. B. Song, C.J. Haycraft, H.S. Seo, B.K. Yoder, and R. Serra Development of the post-natal growth plate requires intraflagellar transport proteins Dev Biol 305 2007 202 216
9. G.S. Dodds Row formation and other types of arrangement of cartilage cells in endochondral ossification Anat Rec 46 1930 385 399
10. C.A. Poole, M.H. Flint, and B.W. Beaumont Morphology of the pericellular capsule in articular cartilage revealed by hyaluronidase digestion J Ultrastruct Res 91 1985 13 23
11. S.R. McGlashan, C.J. Haycraft, C.G. Jensen, B.K. Yoder, and C.A. Poole Articular cartilage and growth plate defects are associated with chondrocyte cytoskeletal abnormalities in Tg737orpk mice lacking the primary cilia protein polaris Matrix Biol 26 2007 234 246
12. C.A. Poole, C.G. Jensen, J.A. Snyder, C.G. Gray, V.L. Hermanutz, and D.N. Wheatley Confocal analysis of primary cilia structure and colocalization with the Golgi apparatus in chondrocytes and aortic smooth muscle cells Cell Biol Int 21 1997 483 494
13. P. Satir, and S.T. Christensen Overview of structure and function of mammalian cilia Annu Rev Physiol 69 2007 377 400
14. S.R. McGlashan, C.G. Jensen, and C.A. Poole Localization of extracellular matrix receptors on the chondrocyte primary cilium J Histochem Cytochem 54 2006 1005 1014
15. W.V. Arnold, and A. Fertala Skeletal diseases caused by mutations that affect collagen structure and function Int J Biochem Cell Biol 45 2013 1556 1567
16. W. McLean, and B.R. Olsen Mouse models of abnormal skeletal development and homeostasis Trends Genet 17 2001 S38 S43
17. M. Savontaus, M. Metsranta, and E. Vuorio Retarded skeletal development in transgenic mice with a type II collagen mutation Am J Pathol 149 1996 2169 2182
18. K.G. Gaiser, B.K. Maddox, J.G. Bann, B.A. Boswell, D.R. Keene, S. Garofalo, and W.A. Horton Y-position collagen II mutation disrupts cartilage formation and skeletal development in a transgenic mouse model of spondyloepiphyseal dysplasia J Bone Miner Res 17 2002 39 47
19. O. Barbieri, S. Astigiano, M. Morini, S. Tavella, A. Schito, A. Corsi, D. Di Martino, P. Bianco, R. Cancedda, and S. Garofalo Depletion of cartilage collagen fibrils in mice carrying a dominant negative Col2a1 transgene affects chondrocyte differentiation Am J Physiol Cell Physiol 285 2003 C1504 C1512
20. L.R. Donahue, B. Chang, S. Mohan, N. Miyakoshi, J.E. Wergedal, D.J. Baylink, N.L. Hawes, C.J. Rosen, P. Ward-Bailey, Q.Y. Zheng, R.T. Bronson, K.R. Johnson, and M.T. Davisson A missense mutation in the mouse Col2a1 gene causes spondyloepiphyseal dysplasia congenita, hearing loss, and retinoschisis J Bone Miner Res 18 2003 1612 1621
21. H.J. Chung, D.A. Jensen, K. Gawron, A. Steplewski, and A. Fertala R992C (p.R1192C) substitution in collagen II alters the structure of mutant molecules and induces the unfolded protein response J Mol Biol 390 2009 306 318
22. D.A. Jensen, A. Steplewski, K. Gawron, and A. Fertala Persistence of intracellular and extracellular changes after incompletely suppressing expression of the R789C (p.R989C) and R992C (p.R1192C) collagen II mutants Hum Mutat 32 2011 794 805
23. Committee for the Update of the Guide for the Care and Use of Laboratory Animals; National Research Council Guide for the Care and Use of Laboratory Animals: Eighth Edition 2011 National Academies Press Washington, DC
24. V. Hintze, A. Steplewski, H. Ito, D.A. Jensen, U. Rodeck, and A. Fertala Cells expressing partially unfolded R789C/p.R989C type II procollagen mutant associated with spondyloepiphyseal dysplasia undergo apoptosis Hum Mutat 29 2008 841 851
25. H. Ito, E. Rucker, A. Steplewski, E. McAdams, R.J. Brittingham, T. Alabyeva, and A. Fertala Guilty by association: some collagen II mutants alter the formation of ECM as a result of atypical interaction with fibronectin J Mol Biol 352 2005 382 395
26. J.Y. Cho, T.D. Grant, G.P. Lunstrum, and W.A. Horton Col2-GFP reporter mouse - a new tool to study skeletal development Am J Med Genet 106 2001 251 253
27. T.D. Grant, J. Cho, K.S. Ariail, N.B. Weksler, R.W. Smith, and W.A. Horton Col2-GFP reporter marks chondrocyte lineage and chondrogenesis during mouse skeletal development Dev Dyn 218 2000 394 400
28. E.G. Canty-Laird, Y. Lu, and K.E. Kadler Stepwise proteolytic activation of type I procollagen to collagen within the secretory pathway of tendon fibroblasts in situ Biochem J 441 2012 707 717
29. Y. Hojima, M. van der Rest, and D.J. Prockop Type I procollagen carboxyl-terminal proteinase from chick embryo tendons. Purification and characterization J Biol Chem 260 1985 15996 16003
30. L. Li, B. Tasic, K.D. Micheva, V.M. Ivanov, M.L. Spletter, S.J. Smith, and L. Luo Visualizing the distribution of synapses from individual neurons in the mouse brain PLoS One 5 2010 e11503
31. J. Grover, and P.J. Roughley Generation of a transgenic mouse in which Cre recombinase is expressed under control of the type II collagen promoter and doxycycline administration Matrix Biol 25 2006 158 165
32. L.A. Neuhold, L. Killar, W. Zhao, M.L. Sung, L. Warner, J. Kulik, J. Turner, W. Wu, C. Billinghurst, T. Meijers, A.R. Poole, P. Babij, and L.J. DeGennaro Postnatal expression in hyaline cartilage of constitutively active human collagenase-3 (MMP-13) induces osteoarthritis in mice J Clin Invest 107 2001 35 44
33. K.L. Posey, A.C. Veerisetty, P. Liu, H.R. Wang, B.J. Poindexter, R. Bick, J.L. Alcorn, and J.T. Hecht An inducible cartilage oligomeric matrix protein mouse model recapitulates human pseudoachondroplasia phenotype Am J Pathol 175 2009 1555 1563
34. E.N. Blaney Davidson, E.L. Vitters, M.B. Bennink, P.L. van Lent, A.P. van Caam, A.B. Blom, W.B. van den Berg, F.A. van de Loo, and P.M. van der Kraan Inducible chondrocyte-specific overexpression of BMP2 in young mice results in severe aggravation of osteophyte formation in experimental OA without altering cartilage damage Ann Rheum Dis 2014
35. K. Sakai, L. Hiripi, V. Glumoff, O. Brandau, R. Eerola, E. Vuorio, Z. Bosze, R. Fassler, and A. Aszodi Stage-and tissue-specific expression of a Col2a1-Cre fusion gene in transgenic mice Matrix Biol 19 2001 761 767
36. D.A. Ovchinnikov, J.M. Deng, G. Ogunrinu, and R.R. Behringer Col2a1-directed expression of Cre recombinase in differentiating chondrocytes in transgenic mice Genesis 26 2000 145 146
37. H. Akiyama, M.C. Chaboissier, J.F. Martin, A. Schedl, and B. de Crombrugghe The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6 Genes Dev 16 2002 2813 2828
38. M. Gossen, S. Freundlieb, G. Bender, G. Muller, W. Hillen, and H. Bujard Transcriptional activation by tetracyclines in mammalian cells Science 268 1995 1766 1769
39. R. Moutier, F. Tchang, S.M. Caucheteux, and C. Kanellopoulos-Langevin Placental anomalies and fetal loss in mice, after administration of doxycycline in food for tet-system activation Transgenic Res 12 2003 369 373
40. A. Kistner, M. Gossen, F. Zimmermann, J. Jerecic, C. Ullmer, H. Lubbert, and H. Bujard Doxycycline-mediated quantitative and tissue-specific control of gene expression in transgenic mice Proc Natl Acad Sci U S A 93 1996 10933 10938
41. A. Fertala, A.L. Sieron, A. Ganguly, S.W. Li, L. Ala-Kokko, K.R. Anumula, and D.J. Prockop Synthesis of recombinant human procollagen II in a stably transfected tumour cell line (HT1080) Biochem J 298 1994 31 37
42. J.M. Somerville, R.M. Aspden, K.E. Armour, K.J. Armour, and D.M. Reid Growth of C57BL/6 mice and the material and mechanical properties of cortical bone from the tibia Calcif Tissue Int 74 2004 469 475
43. M.D. Brodt, C.B. Ellis, and M.J. Silva Growing C57Bl/6 mice increase whole bone mechanical properties by increasing geometric and material properties J Bone Miner Res 14 1999 2159 2166
44. M.G. Chambers, T. Kuffner, S.K. Cowan, K.S. Cheah, and R.M. Mason Expression of collagen and aggrecan genes in normal and osteoarthritic murine knee joints Osteoarthritis Cartilage 10 2002 51 61
45. M. Kveiborg, R. Albrechtsen, L. Rudkjaer, G. Wen, K. Damgaard-Pedersen, and U.M. Wewer ADAM12-S stimulates bone growth in transgenic mice by modulating chondrocyte proliferation and maturation J Bone Miner Res 21 2006 1288 1296
46. T. Aizawa, S. Kokubun, and Y. Tanaka Apoptosis and proliferation of growth plate chondrocytes in rabbits J Bone Joint Surg Br 79 1997 483 486
47. Y. Tajima, K. Kato, S. Maruyama, and K. Hosoi In vivo modulation of proliferating cell nuclear antigen in growth plate chondrocytes from normal, hypophysectomized, growth hormone-treated hypophysectomized rats: a comparative immunohistochemical study with image analysis J Histochem Cytochem 44 1996 713 720
48. A. Fertala, L. Ala-Kokko, R. Wiaderkiewicz, and D.J. Prockop 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 1997 6457 6464
49. A.L. Sieron, A. Fertala, L. Ala-Kokko, and D.J. Prockop Deletion of a large domain in recombinant human procollagen II does not alter the thermal stability of the triple helix J Biol Chem 268 1993 21232 21237
50. D.R. Keene, J.T. Oxford, and N.P. Morris Ultrastructural localization of collagen types II, IX, and XI in the growth plate of human rib and fetal bovine epiphyseal cartilage: type XI collagen is restricted to thin fibrils J Histochem Cytochem 43 1995 967 979
51. M. Arita, S.W. Li, G. Kopen, E. Adachi, S.A. Jimenez, and A. Fertala Skeletal abnormalities and ultrastructural changes of cartilage in transgenic mice expressing a collagen II gene (COL2A1) with a Cys for Arg-alpha1-519 substitution Osteoarthritis Cartilage 10 2002 808 815
52. J.T. Hecht, E. Hayes, R. Haynes, and W.G. Cole COMP mutations, chondrocyte function and cartilage matrix Matrix Biol 23 2005 525 533
53. M.S. Ho, K.Y. Tsang, R.L. Lo, M. Susic, O. Makitie, T.W. Chan, V.C. Ng, D.O. Sillence, R.P. Boot-Handford, G. Gibson, K.M. Cheung, W.G. Cole, K.S. Cheah, and D. Chan 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 2007 1201 1215
54. D.J. Prockop Osteogenesis imperfecta: phenotypic heterogeneity, protein suicide, short and long collagen Am J Hum Genet 36 1984 499 505
55. D.J. Prockop, and K.I. Kivirikko Collagens: molecular biology, diseases, and potentials for therapy Annu Rev Biochem 64 1995 403 434
56. A. Woods, G. Wang, and F. Beier Regulation of chondrocyte differentiation by the actin cytoskeleton and adhesive interactions J Cell Physiol 213 2007 1 8
57. D.R. Rich, and A.L. Clark Chondrocyte primary cilia shorten in response to osmotic challenge and are sites for endocytosis Osteoarthritis Cartilage 20 2012 923 930
58. K.A. Pirog-Garcia, R.S. Meadows, L. Knowles, D. Heinegard, D.J. Thornton, K.E. Kadler, R.P. Boot-Handford, and M.D. Briggs 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 2007 2072 2088
59. K.Y. Tsang, D. Chan, J.F. Bateman, and K.S. Cheah In vivo cellular adaptation to ER stress: survival strategies with double-edged consequences J Cell Sci 123 2010 2145 2154
60. B. Gualeni, M.H. Rajpar, A. Kellogg, P.A. Bell, P. Arvan, R.P. Boot-Handford, and M.D. Briggs 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 2013 1414 1425
61. K.K. Svoboda Chondrocyte-matrix attachment complexes mediate survival and differentiation Microsc Res Tech 43 1998 111 122
62. C. Grashoff, A. Aszodi, T. Sakai, E.B. Hunziker, and R. Fassler Integrin-linked kinase regulates chondrocyte shape and proliferation EMBO Rep 4 2003 432 438
63. C. Huber, and V. Cormier-Daire Ciliary disorder of the skeleton Am J Med Genet C Semin Med Genet 160C 2012 165 174
64. P. Smits, A.D. Bolton, V. Funari, M. Hong, E.D. Boyden, L. Lu, D.K. Manning, N.D. Dwyer, J.L. Moran, M. Prysak, B. Merriman, S.F. Nelson, L. Bonafe, A. Superti-Furga, S. Ikegawa, D. Krakow, D.H. Cohn, T. Kirchhausen, M.L. Warman, and D.R. Beier Lethal skeletal dysplasia in mice and humans lacking the golgin GMAP-210 N Engl J Med 362 2010 206 216
65. C.J. Haycraft, and R. Serra Cilia involvement in patterning and maintenance of the skeleton Curr Top Dev Biol 85 2008 303 332