Inhibition of apoptosis signal-regulating kinase 1 enhances endochondral bone formation by increasing chondrocyte survival

Cell Death and Disease

Volumn 5, Issue 11, 2014, Pages

  Eaton, G J ^a   Zhang, Q S ^a,b   Diallo, C ^a   Matsuzawa, A ^c   Ichijo, H ^c   Steinbeck, M J ^d   Freeman, T A ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c UNIVERSITY OF TOKYO   (Japan)

^d DREXEL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS SIGNAL REGULATING KINASE 1 INHIBITOR; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE INHIBITOR; STAUROSPORINE; UNCLASSIFIED DRUG; 2,7-DIOXO-2,7-DIHYDRO-3H-NAPHTHO(1,2,3-DE)QUINOLINE-1-CARBOXYLATE; APOPTOSIS SIGNAL REGULATING KINASE 1; APORPHINE DERIVATIVE; MAP3K5 PROTEIN, MOUSE; PROTEIN KINASE INHIBITOR; QUINOLINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BONE MINERALIZATION; CARTILAGE CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; ENCHONDRAL OSSIFICATION; FIBROBLAST CULTURE; GROWTH PLATE; HYPERTROPHY; LONG BONE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRABECULAR BONE; ANIMAL; ANTAGONISTS AND INHIBITORS; BONE; BONE DEVELOPMENT; CHONDROGENESIS; CYTOLOGY; DRUG EFFECTS; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM;

MUS;

ANIMALS; APOPTOSIS; APORPHINES; BONE AND BONES; CALCIFICATION, PHYSIOLOGIC; CELL DIFFERENTIATION; CELL SURVIVAL; CHONDROCYTES; CHONDROGENESIS; FIBROBLASTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HYDROGEN PEROXIDE; MAP KINASE KINASE KINASE 5; MICE; MICE, KNOCKOUT; OSTEOGENESIS; PROTEIN KINASE INHIBITORS; QUINOLINES; SIGNAL TRANSDUCTION; STAUROSPORINE;

EID: 84927923235     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.480     Document Type: Article

References (46)

1. Du J, Suzuki H, Nagase F, Akhand AA, Ma X, Takagi Y et al. Superoxide-mediated early oxidation and activation of ASK1 are important for initiating methylglyoxal-induced apoptosis process. Free Radic Biol Med 2001; 31: 469-478.
2. Yasinska IM, Kozhukhar AV, Sumbayev VV. S-nitrosation of thioredoxin in the nitrogen monoxide/superoxide system activates apoptosis signal-regulating kinase 1. Arch Biochem Biophys 2004; 428: 198-203.
3. Nishitoh H, Matsuzawa A, Tobiume K, Matsuzawa A, Tobiume K, Saegusa K, Takeda K, Inoue K et al. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev 2002; 16: 1345-1355.
4. Gotoh Y, Cooper JA. Reactive oxygen species-and dimerization-induced activation of apoptosis signal-regulating kinase 1 in tumor necrosis factor-alpha signal transduction. J Biol Chem 1998; 273: 17477-17482.
5. Yoon KW, Cho JH, Lee JK, Chae JS, Kim YM, Kim J et al. CIB1 functions as a ca(2+)-sensitive modulator of stress-induced signaling by targeting ASK1. Proc Natl Acad Sci USA 2009; 106: 17389-17394.
6. Kawarazaki Y, Ichijo H, Naguro I. Apoptosis signal-regulating kinase 1 as a therapeutic target. Expert Opin Ther Targets 2014; 18: 651-664.
7. Soga M, Matsuzawa A, Ichijo H. Oxidative stress-induced diseases via the ASK1 signaling pathway. Int J Cell Biol 2012; 2012: 439587.
8. Sturchler E, Feurstein D, McDonald P, Duckett D. ASK1 and its role in neurodegenerative diseases. In: Chang RC-C (ed). Neurodegenerative Diseases-Processes, Prevention, Protection and Monitoring. InTech, 2011. Available from: http://www.intechopen.com/books/neurodegenerative-diseases-processes-prevention-protection-and-monitoring/ask1-and-its-role-in-neurodegenerative-diseases.
9. Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, Sawada Y et al. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 1998; 17: 2596-2606.
10. Song JJ, Rhee JG, Suntharalingam M, Walsh SA, Spitz DR, Lee YJ. Role of glutaredoxin in metabolic oxidative stress. glutaredoxin as a sensor of oxidative stress mediated by H2O2. J Biol Chem 2002; 277: 46566-46575.
11. Zhang L, Chen J, Fu H. Suppression of apoptosis signal-regulating kinase 1-induced cell death by 14-3-3 proteins. Proc Natl Acad Sci USA 1999; 96: 8511-8515.
12. Alavi AS, Acevedo L, Min W, Cheresh DA. Chemoresistance of endothelial cells induced by basic fibroblast growth factor depends on raf-1-mediated inhibition of the proapoptotic kinase, ASK1. Cancer Res 2007; 67: 2766-2772.
13. Tobiume K, Saitoh M, Ichijo H. Activation of apoptosis signal-regulating kinase 1 by the stress-induced activating phosphorylation of pre-formed oligomer. J Cell Physiol 2002; 191: 95-104.
14. Van Laethem A, Nys K, Van Kelst S, Claerhout S, Ichijo H, Vandenheede JR et al. Apoptosis signal regulating kinase-1 connects reactive oxygen species to p38 MAPK-induced mitochondrial apoptosis in UVB-irradiated human keratinocytes. Free Radic Biol Med 2006; 41: 1361-1371.
15. Takeda K, Hatai T, Hamazaki TS, Nishitoh H, Saitoh M, Ichijo H. Apoptosis signal-regulating kinase 1 (ASK1) induces neuronal differentiation and survival of PC12 cells. J Biol Chem 2000; 275: 9805-9813.
16. Sayama K, Hanakawa Y, Shirakata Y et al. Apoptosis signal-regulating kinase 1 (ASK1) is an intracellular inducer of keratinocyte differentiation. J Biol Chem 2001; 276: 999-1004.
17. Almeida M, Han L, Martin-Millan M, Plotkin LI, Stewart SA, Roberson PK et al. Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids. J Biol Chem 2007; 282: 27285-27297.
18. Jilka RL, Almeida M, Ambrogini E, Han L, Roberson PK, Weinstein RS et al. Decreased oxidative stress and greater bone anabolism in the aged, when compared to the young, murine skeleton with parathyroid hormone administration. Aging Cell 2010; 9: 851-867.
19. Morita K, Miyamoto T, Fujita N, Kubota Y, Ito K, Takubo K et al. Reactive oxygen species induce chondrocyte hypertrophy in endochondral ossification. J Exp Med 2007; 204: 1613-1623.
20. Shalini S, Dorstyn L, Wilson C, Puccini J, Ho L, Kumar S. Impaired antioxidant defence and accumulation of oxidative stress in caspase-2-deficient mice. Cell Death Differ. 2012; 19: 1370-1380.
21. Hatai T, Matsuzawa A, Inoshita S, Mochida Y, Kuroda T, Sakamaki K et al. Execution of apoptosis signal-regulating kinase 1 (ASK1)-induced apoptosis by the mitochondria-dependent caspase activation. J Biol Chem 2000; 275: 26576-26581.
22. Aaron RK, Ciombor DM, Wang S, Simon B. Clinical biophysics: The promotion of skeletal repair by physical forces. Ann N Y Acad Sci 2006; 1068: 513-531.
23. Yosimichi G, Nakanishi T, Nishida T, Hattori T, Takano-Yamamoto T, Takigawa M. CTGF/Hcs24 induces chondrocyte differentiation through a p38 mitogen-activated protein kinase (p38MAPK), and proliferation through a p44/42 MAPK/extracellular-signal regulated kinase (ERK). Eur J Biochem. 2001; 268: 6058-6065.
24. Doan TKP, Park KS, Kim HK, Park DS, Kim JH, Yoon TR. Inhibition of JNK and ERK pathways by SP600125-and U0126-enhanced osteogenic differentiation of bone marrow stromal cells. Tissue Eng Regenerative Med 2012; 9: 283-294.
25. Wei S, Wang MW, Teitelbaum SL, Ross FP. Interleukin-4 reversibly inhibits osteoclastogen-esis via inhibition of NF-kappa B and mitogen-activated protein kinase signaling. J Biol Chem 2002; 277: 6622-6630.
26. Tobiume K, Matsuzawa A, Takahashi T, Nishitoh H, Morita K, Takeda K et al. ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep 2001; 2: 222-228.
27. Tobiume K, Inage T, Takeda K, Enomoto S, Miyazono K, Ichijo H. Molecular cloning and characterization of the mouse apoptosis signal-regulating kinase 1. Biochem Biophys Res Commun 1997; 239: 905-910.
28. Volynets GP, Chekanov MO, Synyugin AR, Golub AG, Kukharenko OP, Bdzhola VG et al. Identification of 3H-naphtho[1, 2, 3-de]quinoline-2, 7-diones as inhibitors of apoptosis signal-regulating kinase 1 (ASK1). J Med Chem 2011; 54: 2680-2686.
29. Sabbagh Y, Carpenter TO, Demay MB. Hypophosphatemia leads to rickets by impairing caspase-mediated apoptosis of hypertrophic chondrocytes. Proc Natl Acad Sci USA 2005; 102: 9637-9642.
30. Vu TH, Shipley JM, Bergers G, Berger JE, Helms JA, Hanahan D et al. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 1998; 93: 411-422.
31. Lukic IK, Grcevic D, Kovacic N, Katavić V, Ivcević S, Kalajzić I et al. Alteration of newly induced endochondral bone formation in adult mice without tumour necrosis factor receptor 1. Clin Exp Immunol 2005; 139: 236-244.
32. Miura M, Chen XD, Allen MR, Bi Y, Gronthos S, Seo BM et al. A crucial role of caspase-3 in osteogenic differentiation of bone marrow stromal stem cells. J Clin Invest 2004; 114: 1704-1713.
33. Szymczyk KH, Freeman TA, Adams CS, Srinivas V, Steinbeck MJ. Active caspase-3 is required for osteoclast differentiation. J Cell Physiol 2006; 209: 836-844.
34. Yamaguchi O, Higuchi Y, Hirotani S, Kashiwase K, Nakayama H, Hikoso S et al. Targeted deletion of apoptosis signal-regulating kinase 1 attenuates left ventricular remodeling. Proc Natl Acad Sci USA 2003; 100: 15883-15888.
35. Cho KJ, Lee BI, Cheon SY, Kim HW, Kim HJ, Kim GW. Inhibition of apoptosis signal-regulating kinase 1 reduces endoplasmic reticulum stress and nuclear huntingtin fragments in a mouse model of huntington disease. Neuroscience 2009; 163: 1128-1134.
36. Matsuzawa A, Saegusa K, Noguchi T, Sadamitsu C, Nishitoh H, Nagai S et al. ROS-dependent activation of the TRAF6-ASK1-p38 pathway is selectively required for TLR4-mediated innate immunity. Nat Immunol 2005; 6: 587-592.
37. Shimono K, Tung WE, Macolino C, Tung WE, Macolino C, Chi AH et al. Potent inhibition of heterotopic ossification by nuclear retinoic acid receptor-gamma agonists. Nat Med 2011; 17: 454-460.
38. Guo X, Harada C, Namekata K, Matsuzawa A, Camps M, Ji H et al. Regulation of the severity of neuroinflammation and demyelination by TLR-ASK1-p38 pathway. EMBO Mol Med 2010; 2: 504-515.
39. Neumann T, Hofbauer LC, Rauner M, Lodes S, Kästner B, Franke S et al. Clinical and endocrine correlates of circulating sclerostin levels in patients with type 1 diabetes mellitus. Clin Endocrinol 2014; 80: 649-655.
40. Johnstone B, Hering TM, Caplan AI, Goldberg VM, Yoo JU. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 1998; 238: 265-272.
41. Taipaleenmaki H, Harkness L, Chen L, Larsen KH, Säämänen AM, Kassem M et al. The crosstalk between transforming growth factor-beta1 and delta like-1 mediates early chondrogenesis during embryonic endochondral ossification. Stem Cells 2012; 30: 304-313.
42. McLeod MJ. Differential staining of cartilage and bone in whole mouse fetuses by alcian blue and alizarin red S. Teratology 1980; 22: 299-301.
43. Klement BJ, Spooner BS. Embryonic mouse pre-metatarsal development in organ culture. J Exp Zool 1993; 265: 285-294.
44. Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Muller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 2010; 25: 1468-1486.
45. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ et al. Bone histomorphometry: Standardization of nomenclature, symbols, and units. report of the ASBMR histomorphometry nomenclature committee. J Bone Miner Res 1987; 2: 595-610.
46. Shimono K, Morrison TN, Tung WE et al. Inhibition of ectopic bone formation by a selective retinoic acid receptor alpha-agonist: A new therapy for heterotopic ossification? J Orthop Res 2010; 28: 271-277.