Upregulated expression of inducible nitric oxide synthase plays a key role in early apoptosis after anterior cruciate ligament injury

Journal of Orthopaedic Research

Volumn 24, Issue 7, 2006, Pages 1521-1534

  Murakami, Hideaki ^a   Shinomiya, Nariyoshi ^a   Kikuchi, Toshiyuki ^a   Yoshihara, Yasuo ^a   Nemoto, Koichi ^a  

^a NATIONAL DEFENSE MEDICAL COLLEGE   (Japan)

Author keywords

Anterior cruciate ligament (ACL); Apoptosis; Inflammatory cytokines; Nitric oxide synthase (NOS); P38 MAPK

Indexed keywords

AGAROSE; CYTOKINE; DNA FRAGMENT; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; NITRIC OXIDE;

AGAR GEL ELECTROPHORESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR CRUCIATE LIGAMENT INJURY; APOPTOSIS; ARTICLE; CELL CULTURE; CELL ISOLATION; CONTROLLED STUDY; DOWNSTREAM PROCESSING; ELECTRON MICROSCOPY; HEALING; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LIGAMENT; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RABBIT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STATISTICAL ANALYSIS; UPREGULATION;

ANIMALS; ANTERIOR CRUCIATE LIGAMENT; APOPTOSIS; DISEASE MODELS, ANIMAL; FIBROBLASTS; HUMANS; INTERLEUKIN-1; KNEE INJURIES; MEDIAL COLLATERAL LIGAMENT, KNEE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RABBITS; UP-REGULATION;

EID: 33746176555     PISSN: 07360266     EISSN: None     Source Type: Journal    
DOI: 10.1002/jor.20151     Document Type: Article

References (41)

1. Fetto JF, Marshall JL. 1980. The natural history and diagnosis of anterior cruciate ligament insufficiency. Clin Orthop 147:29-38.
2. Amiel D, Scotto K, Akeson WH. 1990. Cruciate Ligaments, response to injury. In: Daniel DM, Akeson WH, O'Connor JJ, editors. Knee ligaments: structure, function, injury, and repair. New York: Raven Press; p 365-377.
3. Hefti FL, Kress A, Fasel J, et al. 1991. Healing of the transected anterior cruciate ligament in the rabbit. J Bone joint Surg Am 73:373-383.
4. O'Donoghue DH, Rockwood CA Jr, Frank GR, et al. 1966. Repair of the anterior cruciate ligament in dogs. J Bone Joint Surg Am 1966; 48:503-519.
5. Amiel D, Billings F, Akeson WH. 1990. Ligament structure, chemistry, and physiology. In: Daniel DM, Akeson WH, O'Connor JJ, editors. Knee ligaments: structure, function, injury, and repair. New York: Raven Press; p 86-91.
6. Nagineni CN, Amiel D, Green MH, et al. 1992. Characterization of intrinsic properties of anterior cruciate and medial collateral ligament cells: an in vitro cell culture study. J Orthop Res 10:465-475.
7. Schmit CC, Georgescu HI, Kwoh CK, et al. 1995. Effect of growth factors on proliferation of fibroblasts from the medial collateral and anterior cruciate ligaments. J Orthop Res 13:184-190.
8. Nishida K, Doi T, Inoue H. 2000. The role of nitric oxide in arthritis joints: a therapeutic target? Mod Rheumatol 10:63-67.
9. Yuan J, Murrel GAC, Wei A, et al. 2002. Apoptosis in rotator cuff tendonopathy. J Orthop Res 20:1372-1379.
10. Borderie D, Hillquin P, Hernvann A, et al. 1999. Apoptosis induced by nitric oxide is associated with nuclear p53 protein expression in cultured osteoarthritic synoviocytes. Osteoarthr Cartilage 7:203-213.
11. Hashimoto S, Takahashi K, Amiel D, et al. 1998. Chondrocyte apoptosis and nitric oxide production during experimentally induced osteoarthritis. Arthritis Rheum 41:1226-1274.
12. Hashimoto S, Takahashi K, Ochs RL, et al. 1999. Nitric oxide production and apoptosis in cells of the meniscus during experimental osteoarthritis. Arthritis Rheum 42:2123-2131.
13. Jilka RL, Weinstein RS, Bellido T, et al. 1998. Osteoblast programmed cell death (apoptosis): modulation by growth factors and cytokines. J Bone Miner Res 13:793-802.
14. Nathan C, Xie Q-W. 1994. Regulation of biosynthesis of nitric oxide. J Biol Chem 269:13725-13728.
15. Goodstone NJ, Hardingham TE. 2002. Tumor necrosis factor α stimulates nitric oxide production more potently than interleukin-1β in porcine articular chondrocytes. Rheumatology 41:883-891.
16. McInnes IB, Leung BP, Field M, et al. 1996. Production of nitric oxide in the synovial membrane of rheumatoid and osteoarthritis patients. J Exp Med 184:1519-1524.
17. Cipolletta C, Jouzeau J-Y, Gegout-Pottie P, et al. 1998. Modulation of IL-1-induced cartilage injury by NO synthase inhibitors: a comparative with rat chondrocytes and cartilage entities. Br J Phalmacol 124:1719-1727.
18. Pelletier JP, Jovanovic D, Fernandes JC, et al. 1998. Reduced progression of experimental osteoarthritis in vivo by selective inhibition of inducible nitric oxide synthase. Arthritis Rheum 41:1275-1286.
19. Hellio MP, Reno C, Hart DA. 1998. Influence of pregnancy on gene expression in rabbit articular cartilage. Osteoarthr Cartilage 6:341-350.
20. Vindelov LL, Christensen IJ, Nissen NI. 1983. A detergent-trypsin method for the preparation of nuclei for flow cytometric DNA analysis. Cytometry 3:323-327.
21. Blanco FJ, Ochs RL, Schwarz H, et al. 1995. Chondrocyte apoptosis induced by nitric oxide. Am J Pathol 146:75-85.
22. Farrell AJ, Blake DR, Palmer RMJ, et al. 1992. Increased concentrations of nitrite in synovial fluid and serum samples suggest increased nitric oxide synthesis in rheumatic diseases. Ann Rheum Dis 51:1219-1222.
23. Amiel D, Ishizue KK, Harwood FL, et al. 1989. Injury of anterior cruciate ligament: the role of collagenase in ligament degeneration. J Orthop Res 7:486-493.
24. Neurath MF, Printz H, Stofft E. 1994. Cellular ultra-structure of the ruptured anterior cruciate ligament: a transmission electron microscopic and immunohistochemical study in 55 cases. Acta Orthop Scand 65:71-76.
25. Abe S, Kurosawa M, Iguchi T, et al. 1993. Light and electron microscopic study of remodeling and maturation process in autogenous graft anterior cruciate ligament reconstruction. Arthroscopy 9:394-405.
26. Toyoda T, Matsumoto H, Fujikawa K, et al. 1998. Tensile load and the metabolism of anterior cruciate ligament cells. Clin Orthop Relat Res 353:247-255.
27. Kim YM, Kim TH, Seol DW, et al. 1998. Nitric oxide suppression of apoptosis occurs in association with an inhibition of bcl-2 cleavage and cytochrome c release. J Biol Chem 273:31437-31441.
28. Rossig L, Fichtlscherer B, Breitschopf K, et al. 1999. Nitric oxide inhibits caspase-3 by S-nitrosation in vivo. J Biol Chem 274:6823-6826.
29. Fischer BA, Mundle S, Cole AA. 2000. Tumor necrosis factor-alpha induced DNA cleavage in human articular chondrocytes may involve multiple endonucleolytic activities during apoptosis. Microsc Res Tech 50:236-242.
30. Maneiro E, Lopez-Armada MJ, deAndres MC, et al. 2005. Effect of nitric oxide on mitochondrial respiratory activity of human articular chondrocytes. Ann Rheum Dis 64:388-395.
31. Presle N, Cipolletta C, Jouzeau JY, et al. 1999. Cartilage protection by nitrite oxide synthase inhibitors after intraarticular injection of interleukin-1β in rats. Arthritis Rheum 42:2094-2102.
32. Murakami H, Shinomiya N, Kikuchi T, et al. 2005. Differential sensitivity to NO-induced apoptosis between anterior cruciate and medial collateral ligament cells. J Orthop Sci 10:84-90.
33. Chun JS. 2004. Expression, activity, and regulation of MAP kinases in cultured chondrocytes. Methods Mol Med 100:291-306.
34. Malemud CJ. 2004. Protein kinases in chondrocytes signaling and osteoarthritis. Clin Orthop Relat Res 427:145-151.
35. Cheng A, Chan SL, Milhavet O, et al. 2001. p38 MAP kinase mediates nitric oxide-induced apoptosis of neural progenitor cells. J Biol Chem 276:43320-43327.
36. Han OJ, Joe KH, Kim SW, et al. 2001. Involvement of p38 mitogen-activated protein kinase and apoptosis signal-regulating kinase-1 in nitric oxide-induced cell death in PC12 cells. Neurochem Res 26:525-532.
37. Kim SJ, Hwang SG, Shin DY, et al. 2002. p38 kinase regulates nitric oxide-induced apoptosis of articular chondrocytes by accumulating p53 via NFkappa B-dependent transcription and stabilization by serine 15 phosphorylation. J Biol Chem 277:33501-33508.
38. Oh-Hashi K, Maruyama W, Isobe K. 2001. Peroxynitrite induces GADD34, 45, and 153 VIA p38 MAPK in human neuroblastoma SH-SY5Y cells. Free Radic Biol Med 30:213-221.
39. Pelletier JP, Fernandes JC, Jovanovic DV, et al. 2001. Chondrocyte death in experimental osteoarthritis is mediated by MEK 1/2 and p38 pathway: role of cyclooxygenase-2 and inducible nitric oxide synthase. J Rheumatol 28:2509-2519.
40. Kim SJ, Ju JW, Oh CD, et al. 2002. ERK-1/2 and p38 kinase oppositely regulate nitric oxide-induced apoptosis of chondrocytes in association with p53, caspase-3, and differentiation status. J Biol Chem 277:1332-1339.
41. Saldeen J, Lee JC, Welsh N. 2001. Role of p38 mitogen-activated protein kinase (p38 MAPK) in cytokine-induced rat islet cell apoptosis. Biochem Pharmacol 61:1561-1569.