Enhanced chondrogenesis of induced pluripotent stem cells from patients with neonatal-onset multisystem inflammatory disease occurs via the caspase 1-independent cAMP/protein kinase A/CREB pathway

Arthritis and Rheumatology

Volumn 67, Issue 1, 2015, Pages 302-314

  Yokoyama, Koji ^a   Ikeya, Makoto ^a   Umeda, Katsutsugu ^a   Oda, Hirotsugu ^a,b   Nodomi, Seishiro ^a   Nasu, Akira ^a   Matsumoto, Yoshihisa ^a,c   Izawa, Kazushi ^a   Horigome, Kazuhiko ^a,d   Kusaka, Toshimasa ^a   Tanaka, Takayuki ^a   Saito, Megumu K ^a   Yasumi, Takahiro ^a   Nishikomori, Ryuta ^a   Ohara, Osamu ^b,f   Nakayama, Naoki ^g   Nakahata, Tatsutoshi ^a   Heike, Toshio ^a   Toguchida, Junya ^a,e  

^a KYOTO UNIVERSITY   (Japan)

^b RIKEN Center for Integrative Medical Sciences   (Japan)

^c NAGOYA CITY UNIVERSITY   (Japan)

^d DAINIPPON SUMITOMO PHARMA CO LTD   (Japan)

^e KYOTO UNIVERSITY   (Japan)

^f KAZUSA DNA RESEARCH INSTITUTE   (Japan)

^g UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLYCOSAMINOGLYCAN; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; PLATELET DERIVED GROWTH FACTOR BB; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA3; CARRIER PROTEIN; CREB1 PROTEIN, HUMAN; INFLAMMASOME; NLRP3 PROTEIN, HUMAN; SOX9 PROTEIN, HUMAN;

ARTICLE; BINDING SITE; CARTILAGE CELL; CELL CULTURE; CELL SUSPENSION; CHONDROGENESIS; CINCA SYNDROME; CONTROLLED STUDY; ENCHONDRAL OSSIFICATION; HUMAN; HUMAN CELL; IN VITRO STUDY; PATHOPHYSIOLOGY; PHENOTYPE; PLURIPOTENT STEM CELL; PROMOTER REGION; WILD TYPE; CELL DIFFERENTIATION; CHEMISTRY; GENETICS; METABOLISM; MUTATION; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

CARRIER PROTEINS; CASPASE 1; CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROCYTES; CHONDROGENESIS; CRYOPYRIN-ASSOCIATED PERIODIC SYNDROMES; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GLYCOSAMINOGLYCANS; HUMANS; IN VITRO TECHNIQUES; INFLAMMASOMES; MUTATION; PHENOTYPE; PLURIPOTENT STEM CELLS; SIGNAL TRANSDUCTION; SOX9 TRANSCRIPTION FACTOR;

EID: 84919913243     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.38912     Document Type: Article

References (42)

1. Kufer TA, Sansonetti PJ,. NLR functions beyond pathogen recognition. Nat Immunol 2011; 12: 121-8.
2. Hoffman HM, Mueller JL, Broide DH, Wanderer AA, Kolodner RD,. Mutation of a new gene encoding a putative pyrin-like protein causes familial cold autoinflammatory syndrome and Muckle-Wells syndrome. Nat Genet 2001; 29: 301-5.
3. Tanaka N, Izawa K, Saito MK, Sakuma M, Oshima K, Ohara O, et al. High incidence of NLRP3 somatic mosaicism in patients with chronic infantile neurologic, cutaneous, articular syndrome: results of an international multicenter collaborative study. Arthritis Rheum 2011; 63: 3625-32.
4. Feldmann J, Prieur AM, Quartier P, Berquin P, Certain S, Cortis E, et al. Chronic infantile neurological cutaneous and articular syndrome is caused by mutations in CIAS1, a gene highly expressed in polymorphonuclear cells and chondrocytes. Am J Hum Genet 2002; 71: 198-203.
5. Latz E, Xiao TS, Stutz A,. Activation and regulation of the inflammasomes. Nat Rev Immunol 2013; 13: 397-411.
6. Gattorno M, Martini A,. Beyond the NLRP3 inflammasome: autoinflammatory diseases reach adolescence [review]. Arthritis Rheum 2013; 65: 1137-47.
7. Bauernfeind FG, Horvath G, Stutz A, Alnemri ES, MacDonald K, Speert D, et al. NF-κB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J Immunol 2009; 183: 787-91.
8. Mariathasan S, Weiss DS, Newton K, McBride J, O'Rourke K, Roose-Girma M, et al. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 2006; 440: 228-32.
9. Hoffman HM, Rosengren S, Boyle DL, Cho JY, Nayar J, Mueller JL, et al. Prevention of cold-associated acute inflammation in familial cold autoinflammatory syndrome by interleukin-1 receptor antagonist. Lancet 2004; 364: 1779-85.
10. Hawkins PN, Lachmann HJ, McDermott MF,. Interleukin-1-receptor antagonist in the Muckle-Wells syndrome. N Engl J Med 2003; 348: 2583-4.
11. Lachmann HJ, Kone-Paut I, Kuemmerle-Deschner JB, Leslie KS, Hachulla E, Quartier P, et al. Use of canakinumab in the cryopyrin-associated periodic syndrome. N Engl J Med 2009; 360: 2416-25.
12. Arostegui JI, Lopez Saldana MD, Pascal M, Clemente D, Aymerich M, Balaguer F, et al. A somatic NLRP3 mutation as a cause of a sporadic case of chronic infantile neurologic, cutaneous, articular syndrome/neonatal-onset multisystem inflammatory disease: novel evidence of the role of low-level mosaicism as the pathophysiologic mechanism underlying Mendelian inherited diseases. Arthritis Rheum 2010; 62: 1158-66.
13. Hill SC, Namde M, Dwyer A, Poznanski A, Canna S, Goldbach-Mansky R,. Arthropathy of neonatal onset multisystem inflammatory disease (NOMID/CINCA). Pediatr Radiol 2007; 37: 145-52.
14. Mackie EJ, Tatarczuch L, Mirams M,. The skeleton: a multi-functional complex organ. The growth plate chondrocyte and endochondral ossification. J Endocrinol 2011; 211: 109-21.
15. Goldring MB, Tsuchimochi K, Ijiri K,. The control of chondrogenesis. J Cell Biochem 2006; 97: 33-44.
16. Bonar SL, Brydges SD, Mueller JL, McGeough MD, Pena C, Chen D, et al. Constitutively activated NLRP3 inflammasome causes inflammation and abnormal skeletal development in mice. PloS One 2012; 7: e35979.
17. Tanaka T, Takahashi K, Yamane M, Tomida S, Nakamura S, Oshima K, et al. Induced pluripotent stem cells from CINCA syndrome patients as a model for dissecting somatic mosaicism and drug discovery. Blood 2012; 120: 1299-308.
18. Umeda K, Zhao J, Simmons P, Stanley E, Elefanty A, Nakayama N,. Human chondrogenic paraxial mesoderm, directed specification and prospective isolation from pluripotent stem cells. Sci Rep 2012; 2: 455.
19. Nasu A, Ikeya M, Yamamoto T, Watanabe A, Jin Y, Matsumoto Y, et al. Genetically matched human iPS cells reveal that propensity for cartilage and bone differentiation differs with clones, not cell type of origin. PloS One 2013; 8: e53771.
20. Sakai H, Okafuji I, Nishikomori R, Abe J, Izawa K, Kambe N, et al. The CD40-CD40L axis and IFN-γ play critical roles in Langhans giant cell formation. Int Immunol 2012; 24: 5-15.
21. Aoyama T, Okamoto T, Nagayama S, Nishijo K, Ishibe T, Yasura K, et al. Methylation in the core-promoter region of the chondromodulin-I gene determines the cell-specific expression by regulating the binding of transcriptional activator Sp3. J Biol Chem 2004; 279: 28789-97.
22. Ushita M, Saito T, Ikeda T, Yano F, Higashikawa A, Ogata N, et al. Transcriptional induction of SOX9 by NF-κB family member RelA in chondrogenic cells. Osteoarthritis Cartilage 2009; 17: 1065-75.
23. Kajita Y, Kato T Jr, Tamaki S, Furu M, Takahashi R, Nagayama S, et al. The transcription factor Sp3 regulates the expression of a metastasis-related marker of sarcoma, actin filament-associated protein 1-like 1 (AFAP1L1). PloS One 2013; 8: e49709.
24. Sandelin A, Alkema W, Engstrom P, Wasserman WW, Lenhard B,. JASPAR: an open-access database for eukaryotic transcription factor binding profiles. Nucleic Acids Res 2004; 32: D91-4.
25. Saito M, Fujisawa A, Nishikomori R, Kambe N, Nakata-Hizume M, Yoshimoto M, et al. Somatic mosaicism of CIAS1 in a patient with chronic infantile neurologic, cutaneous, articular syndrome. Arthritis Rheum 2005; 52: 3579-85.
26. Saito M, Nishikomori R, Kambe N, Fujisawa A, Tanizaki H, Takeichi K, et al. Disease-associated CIAS1 mutations induce monocyte death, revealing low-level mosaicism in mutation-negative cryopyrin-associated periodic syndrome patients. Blood 2008; 111: 2132-41.
27. Aksentijevich I, Nowak M, Mallah M, Chae JJ, Watford WT, Hofmann SR, et al. De novo CIAS1 mutations, cytokine activation, and evidence for genetic heterogeneity in patients with neonatal-onset multisystem inflammatory disease (NOMID): a new member of the expanding family of pyrin-associated autoinflammatory diseases. Arthritis Rheum 2002; 46: 3340-8.
28. Akiyama H, Lefebvre V,. Unraveling the transcriptional regulatory machinery in chondrogenesis. J Bone Miner Metab 2011; 29: 390-5.
29. Kim Y, Murao H, Yamamoto K, Deng JM, Behringer RR, Nakamura T, et al. Generation of transgenic mice for conditional overexpression of Sox9. J Bone Miner Metab 2011; 29: 123-9.
30. Cucchiarini M, Orth P, Madry H,. Direct rAAV SOX9 administration for durable articular cartilage repair with delayed terminal differentiation and hypertrophy in vivo. J Mol Med (Berlin) 2013; 91: 625-36.
31. Cucchiarini M, Thurn T, Weimer A, Kohn D, Terwilliger EF, Madry H,. Restoration of the extracellular matrix in human osteoarthritic articular cartilage by overexpression of the transcription factor SOX9. Arthritis Rheum 2007; 56: 158-67.
32. Tew SR, Li Y, Pothacharoen P, Tweats LM, Hawkins RE, Hardingham TE,. Retroviral transduction with SOX9 enhances re-expression of the chondrocyte phenotype in passaged osteoarthritic human articular chondrocytes. Osteoarthritis Cartilage 2005; 13: 80-9.
33. Carroll SH, Ravid K,. Differentiation of mesenchymal stem cells to osteoblasts and chondrocytes: a focus on adenosine receptors. Expert Rev Mol Med 2013; 15: e1.
34. Huang W, Zhou X, Lefebvre V, de Crombrugghe B,. Phosphorylation of SOX9 by cyclic AMP-dependent protein kinase A enhances SOX9's ability to transactivate a Col2a1 chondrocyte-specific enhancer. Mol Cell Biol 2000; 20: 4149-58.
35. Tsuda M, Takahashi S, Takahashi Y, Asahara H,. Transcriptional co-activators CREB-binding protein and p300 regulate chondrocyte-specific gene expression via association with Sox9. J Biol Chem 2003; 278: 27224-9.
36. Yoon YM, Oh CD, Kang SS, Chun JS,. Protein kinase A regulates chondrogenesis of mesenchymal cells at the post-precartilage condensation stage via protein kinase C-α signaling. J Bone Miner Res 2000; 15: 2197-205.
37. Almeida MQ, Tsang KM, Cheadle C, Watkins T, Grivel JC, Nesterova M, et al. Protein kinase A regulates caspase-1 via Ets-1 in bone stromal cell-derived lesions: a link between cyclic AMP and pro-inflammatory pathways in osteoblast progenitors. Hum Mol Genet 2011; 20: 165-75.
38. 2+ and cAMP. Nature 2012; 492: 123-7.
39. 2+ is a danger signal activating the NLRP3 inflammasome through G protein-coupled calcium sensing receptors. Nat Commun 2012; 3: 1329.
40. Barberi T, Willis LM, Socci ND, Studer L,. Derivation of multipotent mesenchymal precursors from human embryonic stem cells. PLoS Med 2005; 2: e161.
41. Kawaguchi J, Mee PJ, Smith AG,. Osteogenic and chondrogenic differentiation of embryonic stem cells in response to specific growth factors. Bone 2005; 36: 758-69.
42. Zur Nieden NI, Kempka G, Rancourt DE, Ahr HJ,. Induction of chondro-, osteo- and adipogenesis in embryonic stem cells by bone morphogenetic protein-2: effect of cofactors on differentiating lineages. BMC Dev Biol 2005; 5: 1.