Cyclic stretch-induced apoptosis in rat annulus fibrosus cells is mediated in part by endoplasmic reticulum stress through nitric oxide production

European Spine Journal

Volumn 20, Issue 8, 2011, Pages 1233-1243

  Zhang, Yue Hui ^a   Zhao, Chang Qing ^a   Jiang, Lei Sheng ^a   Dai, Li Yang ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Apoptosis; Cyclic stretch; Endoplasmic reticulum stress; Intervertebral disc; Nitric oxide

Indexed keywords

BENZYLOXYCARBONYLLEUCYLGLUTAMYLHISTIDYLASPARTYL FLUOROMETHYL KETONE; CALCITONIN GENE RELATED PEPTIDE; CALCITONIN GENE RELATED PEPTIDE 78; CASPASE 12; CASPASE 8; CASPASE 9; CASPASE INHIBITOR; HOE 33342; NITRIC OXIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANNULUS FIBROSUS CELL; APOPTOSIS; ARTICLE; BONE CELL; CELL STRUCTURE; CYCLIC STRETCH; DRUG ACTIVITY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; FEMALE; FLOW CYTOMETRY; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STAINING; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; ENDOPLASMIC RETICULUM STRESS; FEMALE; FIBROCARTILAGE; INTERVERTEBRAL DISC; NITRIC OXIDE; PRIMARY CELL CULTURE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 83255161985     PISSN: 09406719     EISSN: 14320932     Source Type: Journal    
DOI: 10.1007/s00586-011-1718-5     Document Type: Article

References (43)

1. Ariga K, Yonenobu K, Nakase T, Hosono N, Okuda S, Meng W, Tamura Y, Yoshikawa H (2003) Mechanical stress-induced apoptosis of endplate chondrocytes in organ-cultured mouse intervertebral discs: an ex vivo study. Spine 28:1528-1533 (Pubitemid 36877085)
2. Benallaoua M, Richette P, Francois M, Tsagris L, Revel M, Corvol M, Poiraudeau S, Savouret JF, Rannou F (2006) Modulation of proteoglycan production by cyclic tensile stretch in intervertebral disc cells through a post-translational mechanism. Biorheology 43:303-310 (Pubitemid 44221912)
3. Broberg KB (1983) On the mechanical behaviour of intervertebral discs. Spine 8:151-165 (Pubitemid 13089567)
4. Chen J, Yan W, Setton LA (2004) Tensile stretch alters metalloproteinase activity and gene expression in anulus fibrosus cells. Trans Orthop Res Soc 29:834
5. Chen J, Baer AE, Paik PY, Yan W, Setton LA (2002) Matrix protein gene expression in intervertebral disc cells subjected to altered osmolarity. Biochem Biophys Res Commun 293:932-938 (Pubitemid 34694130)
6. Chen J, Qin J, Liu X, Han Y, Yang Z, Chang X, Ji X (2008) Nitric oxide-mediated neuronal apoptosis in rats with recurrent febrile seizures through endoplasmic reticulum stress pathway. Neurosci Lett 443:134-139
7. Cheng WP, Hung HF, Wang BW, Shyu KG (2008) The molecular regulation of GADD153 in apoptosis of cultured vascular smooth muscle cells by cyclic mechanical stretch. Cardiovasc Res 77:551-559
8. Ching CT, Chow DH, Yao FY, Holmes AD (2003) The effect of cyclic compression on the mechanical properties of the intervertebral disc: an in vivo study in a rat tail model. Clin Biomech 18:182-189 (Pubitemid 36298623)
9. Clancy RM, Amin AR, Abramson SB (1998) The role of nitric oxide in inflammation and immunity. Arthritis Rheum 41:1141-1151 (Pubitemid 28313414)
10. Court C, Colliou OK, Chin JR, Liebenberg E, Bradford DS, Lotz JC (2001) The effect of static in vivo bending on the murine intervertebral disc. Spine J 1:239-245 (Pubitemid 33634221)
11. Evans CH, Watkins SC, Stefanovic-Racic M (1996) Nitric oxide and cartilage metabolism. Methods Enzymol 269:75-88 (Pubitemid 26295698)
12. Fribley A, Zhang K, Kaufman RJ (2009) Regulation of apoptosis by the unfolded protein response. Methods Mol Biol 559: 191-204
13. Friederich M, Hansell P, Palm F (2009) Diabetes, oxidative stress, nitric oxide and mitochondria function. Curr Diabetes Rev 5:120-144
14. Gotoh T, Mori M (2006) Nitric oxide and endoplasmic reticulum stress. Arterioscler Thromb Vasc Biol 26:1439-1446 (Pubitemid 44288967)
15. Huang J, Ballou LR, Hasty KA (2007) Cyclic equibiaxial tensile strain induces both anabolic and catabolic responses in articular chondrocytes. Gene 404:101-109 (Pubitemid 47562648)
16. Hutton WC, Yoon ST, Elmer WA, Li J, Murakami H, Minamide A, Akamaru T (2002) Effect of tail suspension (or simulated weightlessness) on the lumbar intervertebral disc: study of proteoglycans and collagen. Spine 27:1286-1290 (Pubitemid 34655133)
17. Kawahara K, Oyadomari S, Gotoh T, Kohsaka S, Nakayama H, Mori M (2001) Induction of CHOP and apoptosis by nitric oxide in p53-deficient microglial cells. FEBS Lett 506:135-139 (Pubitemid 32925215)
18. Kosuge Y, Imai T, Kawaguchi M, Kihara T, Ishige K, Ito Y (2008) Subregion-specific vulnerability to endoplasmic reticulum stress-induced neurotoxicity in rat hippocampal neurons. Neurochem Int 52:1204-1211
19. Kuhn K, D'Lima DD, Hashimoto S, Lotz M (2004) Cell death in cartilage. Osteoarthritis Cartil 12:1-16 (Pubitemid 38111546)
20. Lee JR, Kim JK, Lee SJ, Kim KP (2009) Role of protein tyrosine nitration in neurodegenerative diseases and atherosclerosis. Arch Pharm Res 32:1109-1118
21. Lotz M (1999) The role of nitric oxide in articular cartilage damage. Rheum Dis Clin North Am 25:269-282 (Pubitemid 29267883)
22. Lotz JC, Chin JR (2000) Intervertebral disc cell death is dependent on the magnitude and duration of spinal loading. Spine 25:1477-1483 (Pubitemid 30418460)
23. Luthra S, Dong J, Gramajo AL, Chwa M, Kim DW, Neekhra A, Kuppermann BD, Kenney MC (2008) 7-Ketocholesterol activates caspases-3/7, -8, and -12 in human microvascular endothelial cells in vitro. Microvasc Res 75:343-350
24. Mao W, Iwai C, Keng PC, Vulapalli R, Liang CS (2006) Norepinephrine- induced oxidative stress causes PC-12 cell apoptosis by both endoplasmic reticulum stress and mitochondrial intrinsic pathway: inhibition of phosphatidylinositol 3-kinase survival pathway. Am J Physiol Cell Physiol 290:C1373-C1384
25. Matsumoto T, Kawakami M, Kuribayashi K, Takenaka T, Tamaki T (1999) Cyclic mechanical stretch stress increases the growth rate and collagen synthesis of nucleus pulposus cells in vitro. Spine 24:315-319 (Pubitemid 29101939)
26. Miyamoto H, Doita M, Nishida K, Yamamoto T, Sumi M, Kurosaka M (2006) Effects of cyclic mechanical stress on the production of inflammatory agents by nucleus pulposus and anulus fibrosus derived cells in vitro. Spine 31:4-9 (Pubitemid 43348186)
27. Nakagawa T, Yuan J (2000) Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J Cell Biol 150:887-894 (Pubitemid 30663424)
28. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J (2000) Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-b. Nature 403:98-103 (Pubitemid 30038529)
29. Oyadomari S, Mori M (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11:381-389 (Pubitemid 38489416)
30. Park JB, Lee JK, Park SJ, Kim KW, Riew KD (2005) Mitochondrial involvement in fas-mediated apoptosis of human lumbar disc cells. J Bone Joint Surg Am 87:1338-1342 (Pubitemid 40756637)
31. Park JB, Park IC, Park SJ, Jin HO, Lee JK, Riew KD (2006) Antiapoptotic effects of caspase inhibitors on rat intervertebral disc cells. J Bone Joint Surg Am 88:771-779
32. Rannou F, Poiraudeau S, Foltz V, Boiteux M, Corvol M, Revel M (2000) Monolayer anulus fibrosus cell cultures in a mechanically active environment: local culture condition adaptations and cell phenotype study. J Lab Clin Med 136:412-421
33. Rannou F, Richette P, Benallaoua M, Francois M, Genries V, Korwin-Zmijowska C, Revel M, Corvol M, Poiraudeau S (2003) Cyclic tensile stretch modulates proteoglycan production by intervertebral disc annulus fibrosus cells through production of nitrite oxide. J Cell Biochem 90:148-157 (Pubitemid 37052317)
34. Rannou F, Lee TS, Zhou RH, Chin J, Lotz JC, Mayoux-Benhamou MA, Barbet JP, Chevrot A, Shyy JY (2004) Intervertebral disc degeneration: the role of the mitochondrial pathway in annulus fibrosus cell apoptosis induced by overload. Am J Pathol 164:915-924 (Pubitemid 38235473)
35. Rasheva VI, Domingos PM (2009) Cellular responses to endoplasmic reticulum stress and apoptosis. Apoptosis 14:996-1007
36. Rodella LF, Ricci F, Borsani E, Stacchiotti A, Foglio E, Favero G, Rezzani R, Mariani C, Bianchi R (2008) Aluminium exposure induces Alzheimer's disease-like histopathological alterations in mouse brain. Histol Histopathol 23:433-439 (Pubitemid 351552328)
37. Sowa G, Agarwal S (2008) Cyclic tensile stress exerts a protective effect on intervertebral disc cells. Am J Phys Med Rehabil 87:537-544
38. Wang HQ, Takahashi R (2007) Expanding insights on the involvement of endoplasmic reticulum stress in Parkinson's disease. Antioxid Redox Signal 9:553-561 (Pubitemid 46598253)
39. Wang XZ, Lawson B, Brewer JW, Zinszner H, Sanjay A, Mi LJ, Boorstein R, Kreibich G, Hendershot LM, Ron D (1996) Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol Cell Biol 16:4273-4280 (Pubitemid 26251229)
40. Xu W, Liu L, Charles IG, Moncada S (2004) Nitric oxide induces coupling of mitochondrial signalling with the endoplasmic reticulum stress response. Nat Cell Biol 6:1129-1134 (Pubitemid 39468015)
41. Yamaguchi M, Kasai K (2005) Inflammation in periodontal tissues in response to mechanical forces. Arch Immunol Ther Exp 53:388-398 (Pubitemid 43116639)
42. Zhao CQ, Jiang LS, Dai LY (2006) Programmed cell death in intervertebral disc degeneration. Apoptosis 11:2079-2088
43. Zhao CQ, Wang LM, Jiang LS, Dai LY (2007) The cell biology of intervertebral disc aging and degeneration. Ageing Res Rev 6:247-261