Secretory phospholipase A2 promotes MMP-9-mediated cell death by degrading type I collagen via the ERK pathway at an early stage of chondrogenesis

Biology of the Cell

Volumn 102, Issue 2, 2010, Pages 107-119

  Choi, Young Ae ^a   Kim, Dong Kyun ^b   Bang, Ok Sun ^c   Kang, Shin Sung ^a   Jin, Eun Jung ^b  

^a Kyungpook National University   (South Korea)

^b Wonkwang University   (South Korea)

^c Korea Institute of Oriental Medicine (KIOM)   (South Korea)

Author keywords

Apoptosis; Chondrogenesis; Extracellular signal regulated kinase (ERK); Matrix metalloproteinase 9; Secretory phospholipase A2 (sPLA2); Type I collagen

Indexed keywords

4 AMINOPHENYL MANNOPYRANOSIDE; CHICKEN YOLK SAC IMMUNOGLOBULIN Y RECEPTOR; COLLAGEN TYPE 1; GELATINASE B; MANNOSE RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; SECRETORY PHOSPHOLIPASE A2; UNCLASSIFIED DRUG; AVIAN PROTEIN;

ANIMAL CELL; ARTICLE; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; CHICKEN; CHONDROGENESIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; LIMB DEVELOPMENT; MESENCHYME CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; ANIMAL; APOPTOSIS; CARTILAGE CELL; CELL CULTURE; CELL DIFFERENTIATION; CHICK EMBRYO; CYTOLOGY; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SIGNAL TRANSDUCTION; TIME;

MAMMALIA;

ANIMALS; APOPTOSIS; AVIAN PROTEINS; CELL DIFFERENTIATION; CELLS, CULTURED; CHICK EMBRYO; CHONDROCYTES; CHONDROGENESIS; COLLAGEN TYPE I; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MAP KINASE SIGNALING SYSTEM; MATRIX METALLOPROTEINASE 9; PHOSPHOLIPASES A2, SECRETORY; TIME FACTORS;

EID: 70450174242     PISSN: 02484900     EISSN: 1768322X     Source Type: Journal    
DOI: 10.1042/BC20090073     Document Type: Article

References (56)

1. Attiga, F. A., Fernandez, P. M., Weeraratna, A. T., Manyak, M. J. and Patierno, S. R. (2000) Inhibitors of prostaglandin synthesis inhibit human prostate tumor cell invasiveness and reduce the release of matrix metalloproteinases. Cancer Res. 60, 4629-4637
2. Bang, O. S., Kim, E. J., Chung, J. G., Lee, S. R., Park, T. K. and Kang, S. S. (2000) Association of focal adhesion kinase with fibronectin and paxillin is required for precartilage condensation of chick mesenchymal cells. Biochem. Biophys. Res. Commun. 278, 522-529
3. Bigg, H. F., Rowan, A. D., Barker, M. D. and Cawston, T. E. (2007) Activity of matrix metalloproteinase-9 against native collagen types I and III. FEBS J. 274, 1246-1255
4. Choi, Y. A., Lim, H. K., Kim, J. R., Lee, C. H., Kim, Y. J., Kang, S. S. and Baek, S. H. (2004) Group IB secretory phospholipase A2 promotes matrix metalloproteinase-2-mediated cell migration via the phosphatidylinositol 3-kinase and Akt pathway. J. Biol. Chem. 279, 36579-36585
5. Cupillard, L., Mulherkar, R., Gomez, N., Kadam, S., Valentin, E., Lazdunski, M. and Lambeau, G. (1999) Both group IB and group IIA secreted phospholipases A2 are natural ligands of the mouse 180-kDa M-type receptor. J. Biol. Chem. 274, 7043-7051
6. Daniel, B. and DeCoster, M. A. (2004) Quantification of sPLA2-induced early and late apoptosis changes in neuronal cell cultures using combined TUNEL and DAPI staining. Brain Res. Protoc. 13, 144-150
7. DeCoster, M. A. (2003) Group III secreted phospholipase A2 causes apoptosis in rat primary cortical neuronal cultures. Brain Res. 988, 20-28
8. DeLise, A. M., Fischer, L. and Tuan, R. S. (2000) Cellular interactions and signaling in cartilage development. Osteoarthritis Cartilage 8, 309-334
9. Fonteh, A. N., Marion, C. R., Barham, B. J., Edens, M. B., Atsumi, G., Samet, J. M., High, K. P. and Chilton, F. H. (2001) Enhancement of mast cell survival: a novel function of some secretory phospholipase A(2) isotypes. J. Immunol. 167, 4161-4171
10. Gack, S., Vallon, R., Schmidt, J., Grigoriadis, A., Tuckermann, J., Schenkel, J., Weiher, H., Wagner, E. F. and Angel, P. (1995) Expression of interstitial collagenase during skeletal development of the mouse is restricted to osteoblast-like cells and hypertrophic chondrocytes. Cell Growth Differ. 6, 759-767
11. Goldring, M. B., Tsuchimochi, K. and Ijiri, K. (2006) The control of chondrogenesis. J. Cell Biochem. 97, 33-44
12. Gorovetz, M., Schwob, O., Krimsky, M., Yedgar, S. and Reich, R. (2008) MMP production in human fibrosarcoma cells and their invasiveness are regulated by group IB secretory phospholipase A2 receptor-mediated activation of cytosolic phospholipase A2. Front. Biosci. 13, 1917-1925
13. Granata, F., Frattini, A., Loffredo, S., Del Prete, A., Sozzani, S., Marone, G. and Triggiani, M. (2006) Signaling events involved in cytokine and chemokine production induced by secretory phospholipase A2 in human lung macrophages. Eur. J. Immunol. 36, 1938-1950
14. Granata, F., Petraroli, A., Boilard, E., Bezzine, S., Bollinger, J., Del Vecchio, L., Gelb, M.H., Lambeau, G., Marone, G. and Triggiani, M. (2005) Activation of cytokine production by secreted phospholipase A2 in human lung macrophages expressing the M-type receptor. J. Immunol. 174, 464-474
15. Gu, Z., Kaul, M., Yan, B., Kridel, S. J., Cui, J., Strongin, A., Smith, J. W., Liddington, R. C. and Lipton, S. A. (2002) S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 297, 1186-1190
16. Guo, L., Moss, S. E., Alexander, R. A., Ali, R. R., Fitzke, F.W. and Cordeiro, M. F. (2005) Retinal ganglion cell apoptosis in glaucoma is related to intraocular pressure and IOP-induced effects on extracellular matrix. Invest. Ophthalmol. Vis. Sci. 46, 175-182
17. 2+ mobilization in the human astrocytoma cell line 1321N1 by a mechanism independent of its catalytic activity. Biochem. Biophys. Res. Commun. 260, 99-104
18. Hurt-Camejo, E., Camejo, G., Peilot, H., Oörni, K. and Kovanen, P. (2001) Phospholipase A(2) in vascular disease. Circ. Res. 89, 298-304
19. Ikeno, Y., Konno, N., Cheon, S. H., Bolchi, A., Ottonello, S., Kitamoto, K. and Arioka, M. (2005) Secretory phospholipases A2 induce neurite outgrowth in PC12 cells through lysophosphatidylcholine generation and activation of G2A receptor. J. Biol. Chem. 280, 28044-28052
20. Jin, E. J., Park, J. H., Lee, S. Y., Chun, J. S., Bang, O. S. and Kang, S. S. (2006) Wnt-5a is involved in TGF-β3-stimulated chondrogenic differentiation of chick wing bud mesenchymal cells. Int. J. Biochem. Cell Biol. 38, 183-195
21. Jin, E. J., Choi, Y. A., Kyun Park, E., Bang, O.S. and Kang, S.S. (2007) MMP-2 functions as a negative regulator of chondrogenic cell condensation via down-regulation of the FAK-integrin β1 interaction. Dev. Biol. 308, 474-484
22. Johansson, N., Saarialho-Kere, U., Airola, K., Herva, R., Nissinen, L., Westermarck, J., Vuorio, E., Heino, J. and Kahari, VM (1997) Collagenase-3 (MMP-13) is expressed by hypertrophic chondrocytes periosteal cells, and osteoblasts during human fetal bone development. Dev. Dyn. 208, 387-397
23. Kallajoki, M., Alanen, K. A., Nevalainen, M. and Nevalainen, T. J. (1998) Group II phospholipase A2 in human male reproductive organs and genital tumors. Prostate 35, 263-272
24. Kinoshita, E., Handa, N., Hanada, K., Kajiyama, G. and Sugiyama, M. (1997) Activation of MAP kinase cascade induced by human pancreatic phospholipase A2 in a human pancreatic cancer cell line. FEBS Lett. 407, 343-346
25. Knudson, C. B. and Knudson, W. (2001) Cartilage proteoglycans. Semin. Cell Dev. Biol. 12, 69-78
26. Kosher, R. A (1983) The chondroblast and the chondrocyte. In Cartilage, Volume I (Hall, B. K., ed.), pp. 59-85, Academic Press, New York
27. Kramer, R. M., Roberts, E. F., Um, S. L., Börsch-Haubold, A. G., Watson, S. P., Fisher, M. J. and Jakubowski, J. A. (1996a) p38 mitogen-activated protein kinase phosphorylates cytosolic phospholipase A2 (cPLA2) in thrombin-stimulated platelets. Evidence that proline-directed phosphorylation is not required for mobilization of arachidonic acid by cPLA2. J. Biol. Chem. 271, 27723-27729
28. Kramer, R. M., Stephenson, D. T., Roberts, E. F. and Clemens, J. A. (1996b) Cytosolic phospholipase A2 (cPLA2) and lipid mediator release in the brain. J. Lipid Mediat. Cell Signal. 14, 3-7
29. 2. J. Biol. Chem. 269, 1575-1578
30. 2. Trends Pharmacol. Sci. 20, 162-170
31. Lee, W. S., Kim, M. J., Beck, Y. I., Park, Y. D. and Jeong, T. S. (2005) Lp-PLA2 inhibitory activities of fatty acid glycerols isolated from Saururus chinensis roots. Bioorg. Med. Chem. Lett. 15, 3573-3575
32. 2. Chem. Phys. Lipids 146, 54-66
33. Maeda, S., Haneda, M., Guo, B., Koya, D., Hayashi, K., Sugimoto, T., Isshiki, K., Yasuda, H., Kashiwagi, A. and Kikkawa, R. (2001) Dinucleotide repeat polymorphism of matrix metalloproteinase-9 gene is associated with diabetic nephropathy. Kidney Int. 60, 1428-1434
34. Manabe, S., Gu, Z. and Lipton, S. A. (2005) Activation of matrix metalloproteinase-9 via neuronal nitric oxide synthase contributes to NMDA-induced retinal ganglion cell death. Invest. Ophthalmol. Vis. Sci. 46, 4747-4753
35. Mannello, F., Tonti, G. and Papa, S. (2005) Matrix metalloproteinase inhibitors as anticancer therapeutics. Curr. Cancer Drug Targets 5, 285-298
36. Masuda, S., Murakami, M., Matsumoto, S., Eguchi, N., Urade, Y., Lambeau, G., Gelb, M. H., Ishikawa, Y., Ishii, T. and Kudo, I. (2004) Localization of various secretory phospholipase A2 enzymes in male reproductive organs. Biochim. Biophys. Acta 1686, 61-76
37. Mott, J. D. and Werb, Z. (2004) Regulation of matrix biology by matrix metalloproteinases. Curr. Opin. Cell Biol. 16, 558-564
38. 2+ signaling in smooth muscle by cAMP- and cGMP-dependent protein kinases. Inhibitory phosphorylation of PLA2 by cyclic nucleotide-dependent protein kinases. J. Biol. Chem. 273, 34519-34526
39. Nevalainen, T. J., Meri, K. M. and Niemi, M. (1993) Synovial-type (group II) phospholipase A2 human seminal plasma. Andrologia 25, 355-358
40. Oestvang, J. and Johansen, B. (2006) Phospholipase A2: a key regulator of inflammatory signalling and a connector to fibrosis development in atherosclerosis. Biochim. Biophys. Acta 1761, 1309-1316
41. Ohuchi, E., Imai, K., Fujii, Y., Sato, H., Seiki, M. and Okada, Y. (1997) Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J. Biol. Chem. 272, 2446-2451
42. Pogue, R. and Lyons, K. (2006) BMP signaling in the cartilage growth plate. Curr. Top. Dev. Biol. 76, 1-48
43. Putz, T., Ramoner, R., Gander, H., Rahm, A., Bartsch, G., Bernardo, K., Ramsay, S. and Thurnher, M. (2007) Bee venom secretory phospholipase A2 and phosphatidylinositol-homologues cooperatively disrupt membrane integrity, abrogate signal transduction and inhibit proliferation of renal cancer cells. Cancer Immunol. Immunother. 56, 627-640
44. Rao, G. N., Lassègue, B., Alexander, R. W. and Griendling, K. K. (1994) Angiotensin II stimulates phosphorylation of high-molecular-mass cytosolic phospholipase A2 in vascular smooth-muscle cells. Biochem. J. 299, 197-201
45. 2 type II binds to extracellular matrix biglycan: modulation of its activity on LDL by colocalization in glycosaminoglycan matrices. Arterioscler. Thromb. Vasc. Biol. 18, 1934-1941
46. Somerville, R. P., Oblander, S. A. and Apte, S. S. (2003) Matrix metalloproteinases: old dogs with new tricks. Genome Biol. 4, 216
47. Stahle-Backdahl, M., Sandstedt, B., Bruce, K., Lindahl, A., Jimenez, M. G., Vega, J. A. and Lopez-Otin, C. (1997) Collagenase-3 (MMP-13) is expressed during human fetal ossification and reexpressed in postnatal bone remodeling and in rheumatoid arthritis. Lab. Invest. 76, 717-728
48. Takahara, M., Naruse, T., Takagi, M., Orui, H. and Ogino, T. (2004) Matrix metalloproteinase-9 expression, tartrate-resistant acid phosphatase activity, and DNA fragmentation in vascular and cellular invasion into cartilage preceding primary endochondral ossification in long bones. J. Orthop. Res. 22, 1050-1057
49. Tesar, D. B., Cheung, E. J. and Bjorkman, P. J. (2008) The chicken yolk sac IgY receptor, a mammalian mannose receptor family member, transcytoses IgY across polarized epithelial cells. Mol. Biol. Cell 19, 1587-1593
50. van Tienhoven, M., Atkins, J., Li, Y. and Glynn, P. (2002) Human neuropathy target esterase catalyzes hydrolysis of membrane lipids. J. Biol. Chem. 277, 20942-20948
51. von Wnuck, Lipinski, K., Keul, P., Ferri, N., Lucke, S., Heusch, G., Fischer, J.W. and Levkau, B. (2006) Integrin-mediated transcriptional activation of inhibitor of apoptosis proteins protects smooth muscle cells against apoptosis induced by degraded collagen. Circ. Res. 98, 1490-1497
52. Vu, T. H., Shipley, J. M., Bergers, G., Berger, J. E., Helms, J. A., Hanahan, D., Shapiro, S. D., Senior, R. M. and Werb, Z. (1998) MMP-9/ gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93, 411-422
53. Vu, T. H. and Werb, Z. (2000) Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev. 14, 2123-2133
54. 2. Proc. Natl. Acad. Sci. U.S.A. 95, 15345-15350
55. West, Jr, A. P., Herr, A. B. and Bjorkman, P. J. (2004) The chicken yolk sac IgY receptor, a functional equivalent of the mammalian MHC-related Fc receptor, is a phospholipase A2 receptor homolog. Immunity 20, 601-610
56. 2 induces neuronal cell death via apoptosis. J. Neurochem. 81, 449-461