publication . Other literature type . Article . 2018

Inhibiting the integrated stress response pathway prevents aberrant chondrocyte differentiation thereby alleviating chondrodysplasia.

Cheng Wang; Zhijia Tan; Ben Niu; Kwok Yeung Tsang; Andrew Tai; Wilson C W Chan; Rebecca L K Lo; Keith K H Leung; Nelson W F Dung; Nobuyuki Itoh; ...
  • Published: 19 Jul 2018
  • Publisher: eLife Sciences Publications, Ltd
Abstract
<jats:p>The integrated stress response (ISR) is activated by diverse forms of cellular stress, including endoplasmic reticulum (ER) stress, and is associated with diseases. However, the molecular mechanism(s) whereby the ISR impacts on differentiation is incompletely understood. Here, we exploited a mouse model of Metaphyseal Chondrodysplasia type Schmid (MCDS) to provide insight into the impact of the ISR on cell fate. We show the protein kinase RNA-like ER kinase (PERK) pathway that mediates preferential synthesis of ATF4 and CHOP, dominates in causing dysplasia by reverting chondrocyte differentiation via ATF4-directed transactivation of Sox9. Chondrocyte sur...
Subjects
free text keywords: Signal transduction, Cell biology, Fibroblast growth factor, Integrated stress response, EIF-2 kinase, biology.protein, biology, Unfolded protein response, Cellular differentiation, Chondrogenesis, Chondrocyte, medicine.anatomical_structure, medicine, Research Article, Developmental Biology, endoplasmic reticulum stress, chondrodysplasia, protein kinase RNA-like ER kinase pathway, ATF4, ISRIB, Mouse
Related Organizations
124 references, page 1 of 9

Akiyama, H, Chaboissier, MC, Martin, JF, Schedl, A, de Crombrugghe, B. 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 & Development. 2002; 16: 2813-2828 [OpenAIRE] [PubMed] [DOI]

Arnold, WV, Fertala, A. Skeletal diseases caused by mutations that affect collagen structure and function. The International Journal of Biochemistry & Cell Biology. 2013; 45: 1556-1567 [OpenAIRE] [PubMed] [DOI]

Ashburner, M, Ball, CA, Blake, JA, Botstein, D, Butler, H, Cherry, JM, Davis, AP, Dolinski, K, Dwight, SS, Eppig, JT, Harris, MA, Hill, DP, Issel-Tarver, L, Kasarskis, A, Lewis, S, Matese, JC, Richardson, JE, Ringwald, M, Rubin, GM, Sherlock, G. Gene ontology: tool for the unification of biology. the gene ontology consortium. Nature Genetics. 2000; 25: 25-29 [OpenAIRE] [PubMed] [DOI]

Athwal, VS, Pritchett, J, Llewellyn, J, Martin, K, Camacho, E, Raza, SM, Phythian-Adams, A, Birchall, LJ, Mullan, AF, Su, K, Pearmain, L, Dolman, G, Zaitoun, AM, Friedman, SL, MacDonald, A, Irving, WL, Guha, IN, Hanley, NA, Piper Hanley, K, Athwal Varinder, S, Raza Sayyid, MA. SOX9 predicts progression toward cirrhosis in patients while its loss protects against liver fibrosis. EMBO Molecular Medicine. 2017; 9: 1696-1710 [OpenAIRE] [PubMed] [DOI]

Balwierz, PJ, Pachkov, M, Arnold, P, Gruber, AJ, Zavolan, M, van Nimwegen, E. ISMARA: automated modeling of genomic signals as a democracy of regulatory motifs. Genome Research. 2014; 24: 869-884 [OpenAIRE] [PubMed] [DOI]

Bell, DM, Leung, KK, Wheatley, SC, Ng, LJ, Zhou, S, Ling, KW, Sham, MH, Koopman, P, Tam, PP, Cheah, KS. SOX9 directly regulates the type-II collagen gene. Nature Genetics. 1997; 16: 174-178 [OpenAIRE] [PubMed] [DOI]

Bonafe, L, Cormier-Daire, V, Hall, C, Lachman, R, Mortier, G, Mundlos, S, Nishimura, G, Sangiorgi, L, Savarirayan, R, Sillence, D, Spranger, J, Superti-Furga, A, Warman, M, Unger, S. Nosology and classification of genetic skeletal disorders: 2015 revision. American Journal of Medical Genetics Part A. 2015; 167: 2869-2892 [OpenAIRE] [DOI]

Boot-Handford, RP, Briggs, MD. The unfolded protein response and its relevance to connective tissue diseases. Cell and Tissue Research. 2010; 339: 197-211 [OpenAIRE] [PubMed] [DOI]

Briggs, MD, Chapman, KL. Pseudoachondroplasia and multiple epiphyseal dysplasia: mutation review, molecular interactions, and genotype to phenotype correlations. Human Mutation. 2002; 19: 465-478 [OpenAIRE] [PubMed] [DOI]

Brostrom, CO, Prostko, CR, Kaufman, RJ, Brostrom, MA. Inhibition of translational initiation by activators of the glucose-regulated stress protein and heat shock protein stress response systems. role of the interferon-inducible double-stranded RNA-activated eukaryotic initiation factor 2alpha kinase. The Journal of Biological Chemistry. 1996; 271: 24995-25002 [OpenAIRE] [PubMed] [DOI]

Cameron, TL, Bell, KM, Gresshoff, IL, Sampurno, L, Mullan, L, Ermann, J, Glimcher, LH, Boot-Handford, RP, Bateman, JF. XBP1-Independent UPR pathways suppress C/EBP-β mediated chondrocyte differentiation in ER-Stress related skeletal disease. PLOS Genetics. 2015b; 11 [OpenAIRE] [PubMed] [DOI]

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 [OpenAIRE] [PubMed] [DOI]

Cameron, TL, Gresshoff, IL, Bell, KM, Piróg, KA, Sampurno, L, Hartley, CL, Sanford, EM, Wilson, R, Ermann, J, Boot-Handford, RP, Glimcher, LH, Briggs, MD, Bateman, JF. Cartilage-specific ablation of XBP1 signaling in mouse results in a chondrodysplasia characterized by reduced chondrocyte proliferation and delayed cartilage maturation and mineralization. Osteoarthritis and Cartilage. 2015; 23: 661-670 [OpenAIRE] [PubMed] [DOI]

Chou, A, Krukowski, K, Jopson, T, Zhu, PJ, Costa-Mattioli, M, Walter, P, Rosi, S. Inhibition of the integrated stress response reverses cognitive deficits after traumatic brain injury. PNAS. 2017; 114: E6420-E6426 [OpenAIRE] [PubMed] [DOI]

De Sousa-Coelho, AL, Marrero, PF, Haro, D. Activating transcription factor 4-dependent induction of FGF21 during amino acid deprivation. Biochemical Journal. 2012; 443: 165-171 [PubMed] [DOI]

124 references, page 1 of 9
Abstract
<jats:p>The integrated stress response (ISR) is activated by diverse forms of cellular stress, including endoplasmic reticulum (ER) stress, and is associated with diseases. However, the molecular mechanism(s) whereby the ISR impacts on differentiation is incompletely understood. Here, we exploited a mouse model of Metaphyseal Chondrodysplasia type Schmid (MCDS) to provide insight into the impact of the ISR on cell fate. We show the protein kinase RNA-like ER kinase (PERK) pathway that mediates preferential synthesis of ATF4 and CHOP, dominates in causing dysplasia by reverting chondrocyte differentiation via ATF4-directed transactivation of Sox9. Chondrocyte sur...
Subjects
free text keywords: Signal transduction, Cell biology, Fibroblast growth factor, Integrated stress response, EIF-2 kinase, biology.protein, biology, Unfolded protein response, Cellular differentiation, Chondrogenesis, Chondrocyte, medicine.anatomical_structure, medicine, Research Article, Developmental Biology, endoplasmic reticulum stress, chondrodysplasia, protein kinase RNA-like ER kinase pathway, ATF4, ISRIB, Mouse
Related Organizations
124 references, page 1 of 9

Akiyama, H, Chaboissier, MC, Martin, JF, Schedl, A, de Crombrugghe, B. 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 & Development. 2002; 16: 2813-2828 [OpenAIRE] [PubMed] [DOI]

Arnold, WV, Fertala, A. Skeletal diseases caused by mutations that affect collagen structure and function. The International Journal of Biochemistry & Cell Biology. 2013; 45: 1556-1567 [OpenAIRE] [PubMed] [DOI]

Ashburner, M, Ball, CA, Blake, JA, Botstein, D, Butler, H, Cherry, JM, Davis, AP, Dolinski, K, Dwight, SS, Eppig, JT, Harris, MA, Hill, DP, Issel-Tarver, L, Kasarskis, A, Lewis, S, Matese, JC, Richardson, JE, Ringwald, M, Rubin, GM, Sherlock, G. Gene ontology: tool for the unification of biology. the gene ontology consortium. Nature Genetics. 2000; 25: 25-29 [OpenAIRE] [PubMed] [DOI]

Athwal, VS, Pritchett, J, Llewellyn, J, Martin, K, Camacho, E, Raza, SM, Phythian-Adams, A, Birchall, LJ, Mullan, AF, Su, K, Pearmain, L, Dolman, G, Zaitoun, AM, Friedman, SL, MacDonald, A, Irving, WL, Guha, IN, Hanley, NA, Piper Hanley, K, Athwal Varinder, S, Raza Sayyid, MA. SOX9 predicts progression toward cirrhosis in patients while its loss protects against liver fibrosis. EMBO Molecular Medicine. 2017; 9: 1696-1710 [OpenAIRE] [PubMed] [DOI]

Balwierz, PJ, Pachkov, M, Arnold, P, Gruber, AJ, Zavolan, M, van Nimwegen, E. ISMARA: automated modeling of genomic signals as a democracy of regulatory motifs. Genome Research. 2014; 24: 869-884 [OpenAIRE] [PubMed] [DOI]

Bell, DM, Leung, KK, Wheatley, SC, Ng, LJ, Zhou, S, Ling, KW, Sham, MH, Koopman, P, Tam, PP, Cheah, KS. SOX9 directly regulates the type-II collagen gene. Nature Genetics. 1997; 16: 174-178 [OpenAIRE] [PubMed] [DOI]

Bonafe, L, Cormier-Daire, V, Hall, C, Lachman, R, Mortier, G, Mundlos, S, Nishimura, G, Sangiorgi, L, Savarirayan, R, Sillence, D, Spranger, J, Superti-Furga, A, Warman, M, Unger, S. Nosology and classification of genetic skeletal disorders: 2015 revision. American Journal of Medical Genetics Part A. 2015; 167: 2869-2892 [OpenAIRE] [DOI]

Boot-Handford, RP, Briggs, MD. The unfolded protein response and its relevance to connective tissue diseases. Cell and Tissue Research. 2010; 339: 197-211 [OpenAIRE] [PubMed] [DOI]

Briggs, MD, Chapman, KL. Pseudoachondroplasia and multiple epiphyseal dysplasia: mutation review, molecular interactions, and genotype to phenotype correlations. Human Mutation. 2002; 19: 465-478 [OpenAIRE] [PubMed] [DOI]

Brostrom, CO, Prostko, CR, Kaufman, RJ, Brostrom, MA. Inhibition of translational initiation by activators of the glucose-regulated stress protein and heat shock protein stress response systems. role of the interferon-inducible double-stranded RNA-activated eukaryotic initiation factor 2alpha kinase. The Journal of Biological Chemistry. 1996; 271: 24995-25002 [OpenAIRE] [PubMed] [DOI]

Cameron, TL, Bell, KM, Gresshoff, IL, Sampurno, L, Mullan, L, Ermann, J, Glimcher, LH, Boot-Handford, RP, Bateman, JF. XBP1-Independent UPR pathways suppress C/EBP-β mediated chondrocyte differentiation in ER-Stress related skeletal disease. PLOS Genetics. 2015b; 11 [OpenAIRE] [PubMed] [DOI]

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 [OpenAIRE] [PubMed] [DOI]

Cameron, TL, Gresshoff, IL, Bell, KM, Piróg, KA, Sampurno, L, Hartley, CL, Sanford, EM, Wilson, R, Ermann, J, Boot-Handford, RP, Glimcher, LH, Briggs, MD, Bateman, JF. Cartilage-specific ablation of XBP1 signaling in mouse results in a chondrodysplasia characterized by reduced chondrocyte proliferation and delayed cartilage maturation and mineralization. Osteoarthritis and Cartilage. 2015; 23: 661-670 [OpenAIRE] [PubMed] [DOI]

Chou, A, Krukowski, K, Jopson, T, Zhu, PJ, Costa-Mattioli, M, Walter, P, Rosi, S. Inhibition of the integrated stress response reverses cognitive deficits after traumatic brain injury. PNAS. 2017; 114: E6420-E6426 [OpenAIRE] [PubMed] [DOI]

De Sousa-Coelho, AL, Marrero, PF, Haro, D. Activating transcription factor 4-dependent induction of FGF21 during amino acid deprivation. Biochemical Journal. 2012; 443: 165-171 [PubMed] [DOI]

124 references, page 1 of 9
Powered by OpenAIRE Open Research Graph
Any information missing or wrong?Report an Issue
publication . Other literature type . Article . 2018

Inhibiting the integrated stress response pathway prevents aberrant chondrocyte differentiation thereby alleviating chondrodysplasia.

Cheng Wang; Zhijia Tan; Ben Niu; Kwok Yeung Tsang; Andrew Tai; Wilson C W Chan; Rebecca L K Lo; Keith K H Leung; Nelson W F Dung; Nobuyuki Itoh; ...