Oxidized low-density lipoprotein induces matrix metalloproteinase-9 expression via a p42/p44 and JNK-dependent AP-1 pathway in brain astrocytes

GLIA

Volumn 57, Issue 1, 2009, Pages 24-38

  Wang, Hui Hsin ^a   Hsieh, Hsi Lung ^b   Wu, Cheng Ying ^a   Sun, Chi Chin ^c   Yang, Chuen Mao ^a  

^a CHANG GUNG UNIVERSITY   (Taiwan)

^b CHANG GUNG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^c CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

Author keywords

ERK1 2; JNK1 2; MMP 9; OxLDL; PI3K Akt

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; GELATINASE B; LUCIFERASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OXIDIZED LOW DENSITY LIPOPROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN C FOS; PROTEIN C JUN; PROTEIN KINASE B; SHORT HAIRPIN RNA; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1;

ANIMAL CELL; ARTICLE; ASTROCYTE; BINDING SITE; BRAIN DISEASE; BRAIN INJURY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENETIC TRANSFECTION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RAT; TRANSCRIPTION REGULATION;

ANIMALS; ASTROCYTES; BRAIN; CELL LINE; ENZYME ACTIVATION; ENZYME PRECURSORS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; LIPOPROTEINS, LDL; MAP KINASE KINASE 4; MAP KINASE SIGNALING SYSTEM; MATRIX METALLOPROTEINASE 9; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; OXIDATION-REDUCTION; RATS; TRANSCRIPTION FACTOR AP-1;

EID: 61449218138     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20732     Document Type: Article

References (59)

1. Akaji K, Suga S, Fujino T, Mayanagi K, Inamasu J, Horiguchi T, Sato S, Kawase T. 2003. Effect of intra-ischemic hypothermia on the expression of c-Fos and c-Jun, and DNA binding activity of AP-1 after focal cerebral ischemia in rat brain. Brain Res 975:149-157.
2. Anwar AA, Li FY, Leake DS, Ishii T, Mann GE, Siow RC. 2005. Induction of heme oxygenase 1 by moderately oxidized low-density lipoproteins in human vascular smooth muscle cells: Role of mitogen-activated protein kinases and Nrf2. Free Radic Biol Med 39:227-236.
3. Aoki T, Sumii T, Mori T, Wang X, Lo EH. 2002. Blood-brain barrier disruption and matrix metalloproteinase-9 expression during reperfusion injury mechanical versus embolic focal ischemia in spontaneously hypertensive rats. Stroke 33:2711-2717.
4. Auge N, Garcia V, Maupas-Schwalm F, Levade T, Salvayre R, Negre-Salvayre A. 2002. Oxidized LDL-induced smooth muscle cell proliferation involves the EGF receptor/PI-3 kinase/Akt and the sphingolipid signaling pathways. Arterioscler Thromb Vasc Biol 22:1990-1995.
5. Bogoyevitch MA, Kobe B. 2006. Uses for JNK: The many and varied substrates of the c-Jun N-terminal kinases. Microbiol Mol Biol Rev 70:1061-1095.
6. Boullier A, Li Y, Quehenberger O, Palinski W, Tabas I, Witztum JL, Miller YI. 2006. Minimally oxidized LDL offsets the apoptotic effects of extensively oxidized LDL, free cholesterol in macrophages. Arterioscler Thromb Vasc Biol 26:1169-1176.
7. Byun HJ, Hong IK, Kim E, Jin YJ, Jeoung DI, Hahn JH, Kim YM, Park SH, Lee H. 2006. A splice variant of CD99 increases motility and MMP-9 expression of human breast cancer cells through the AKT-, ERK-, and JNK-dependent AP-1 activation signaling pathways J Biol Chem 281:34833-34847.
8. Carr AC, McCall MR, Frei B. 2000. Oxidation of LDL by myeloperoxidase and reactive nitrogen species: Reaction pathways and antioxidant protection. Arterioscler Thromb Vasc Biol 20:1716-1723.
9. Chatterjee S, Bhunia AK, Snowden A, Han H. 1997. Oxidized low density lipoproteins stimulate galactosyltransferase activity, ras activation, p44 mitogen activated protein kinase and c-fos expression in aortic smooth muscle cells. Glycobiology 7:703-710.
10. Chien MW, Chien CS, Hsiao LD, Lin CH, Yang CM. 2003. OxLDL induces mitogen-activated protein kinase activation mediated via PI3-kinase/Akt in vascular smooth muscle cells. J Lipid Res 44:1667-1675.
11. Dérijard B, Hibi M, Wu IH, Barrett T, Su B, Deng T, Karin M, Davis RJ. 1994. JNK1: A protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 76:1025-1037.
12. Dudley DT, Pang L, Decker SJ, Bridges AJ, Saltiel AR. 1995. A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc Natl Acad Sci USA 92:7686-7689.
13. Eberhardt W, Schulze M, Engels C, Klasmeier E, Pfeilschifter J. 2002. Glucocorticoid-mediated suppression of cytokine-induced matrix metalloproteinase-9 expression in rat mesangial cells: Involvement of nuclear factor-κB and Ets transcription factors. Mol Endocrinol 16: 1752-1766.
14. Eng LF, Ghirnikar RS. 1994. GFAP and astrogliosis. Brain Pathol 4:229-237.
15. Gottschall PE, Yu X. 1995. Cytokines regulate gelatinase A, B (matrix metalloproteinase 2 and 9) activity in cultured rat astrocytes. J Neurochem 64:1513-1520.
16. Griffin RJ, Moloney A, Kelliher M, Johnston JA, Ravid R, Dockery P, O'Connor R, O'Neill C. 2005. Activation of Akt/PKB, increased phosphorylation of Akt substrates and loss and altered distribution of Akt and PTEN are features of Alzheimer's disease pathology. J Neurochem 93:105-117.
17. Gum R, Wang H, Lengyel E, Juarez J, Boyd D. 1997. Regulation of 92 kDa type IV collagenase expression by the jun aminoterminal kinase-and the extracellular signal-regulated kinase-dependent signaling cascades. Oncogene 14:1481-1493.
18. Hahm ER, Gho YS, Park S, Park C, Kim KW, Yang CH. 2004. Synthetic curcumin analogs inhibit activator protein-1 transcription and tumor-induced angiogenesis. Biochem Biophys Res Commun 321: 337-344.
19. Halliwell B. 1992. Oxygen radicals as key mediators in neurological disease: Fact or fiction? Ann Neurol 32 (Suppl):S10-S15.
20. Han S, Ritzenthaler JD, Sitaraman SV, Roman J. 2006. Fibronectin increases matrix metalloproteinase 9 expression through activation of c-Fos via extracellular-regulated kinase and phosphatidylinositol 3-kinase pathways in human lung carcinoma cells. J Biol Chem 281: 29614-29624.
21. Harris JE, Nuttall RK, Elkington PT, Green JA, Horncastle DE, Graeber MB, Edwards DR, Friedland JS. 2007. Monocyte-astrocyte networks regulate matrix metalloproteinase gene expression and secretion in central nervous system tuberculosis in vitro and in vivo. J Immunol 178:1199-1207.
22. Hartmann W, Digon-Sontgerath B, Koch A, Waha A, Endl E, Dani I, Denkhaus D, Goodyer CG, Sorensen N, Wiestler OD, Pietsch T. 2006. Phosphatidylinositol 3′-kinase/AKT signaling is activated in medulloblastoma cell proliferation and is associated with reduced expression of PTEN. Clin Cancer Res 12:3019-3027.
23. Hsieh HL, Wang HH, Wu CY, Jou MJ, Yen MH, Parker P, Yang CM. 2007. BK-induced COX-2 expression via PKC-δ-dependent activation of p42/ p44 MAPK and NF-κB in astrocytes. Cell Signal 19:330-340.
24. 2 expression via sequential PKC-delta, p42/p44 MAPK, and NF-κB activation in rat brain astrocytes. J Cell Physiol 206:246-254.
25. Hsieh HL, Yen MH, Jou MJ, Yang CM. 2004. Intracellular signalings underlying bradykinin-induced matrix metalloproteinase-9 expression in rat brain astrocyte-1. Cell Signal 16:1163-1176.
26. Jou TC, Jou MJ, Chen JY, Lee SY. 1985. Properties of rat brain astrocytes in long-term culture. J Formos Med Assoc 84:865-881.
27. Kang JH, Kim JK, Park WH, Park KK, Lee TS, Magae J, Nakajima H, Kim CH, Chang YC. 2007. Ascochlorin suppresses oxLDL-induced MMP-9 expression by inhibiting the MEK/ERK signaling pathway in human THP-1 macrophages. J Cell Biochem 102:506-14.
28. Keller JN, Hanni KB, Markesbery WR. 1999. Oxidized low-density lipoprotein induces neuronal death: Implications for calcium, reactive oxygen species, and caspases. J Neurochem 72:2601-2609.
29. Kim JA, Tran ND, Berliner JA, Fisher MJ. 2004. Minimally oxidized low-density lipoprotein regulates hemostasis factors of brain capillary endothelial cells. J Neurol Sci 217:135-141.
30. Korzus E, Nagase H, Rydell R, Travis J. 1997. The mitogen-activated protein kinase and JAK-STAT signaling pathways are required for an oncostatin M-responsive element-mediated activation of matrix metalloproteinase 1 gene expression. J Biol Chem 272:1188-1196.
31. Lavery W, Hall V, Yager JC, Rottgers A, Wells MC, Stern M. 2007. Phosphatidylinositol 3-kinase and Akt nonautonomously promote perineurial glial growth in Drosophila peripheral nerves. J Neurosci 27:279-288.
32. Lee WJ, Shin CY, Yoo BK, Ryu JR, Choi EY, Cheong JH, Ryu JH, Ko KH. 2003. Induction of matrix metalloproteinase-9 (MMP-9) in lipopolysaccharide- stimulated primary astrocytes is mediated by extracellular signal-regulated protein kinase 1/2 (Erk1/2). Glia 41:15-24.
33. Liberto CM, Albrecht PJ, Herx LM, Yong VW, Levison SW. 2004. Proregenerative properties of cytokine-activated astrocytes. J Neurochem 89:1092-1100.
34. Lin SJ, Shyue SK, Liu PL, Chen YH, Ku HH, Chen JW, Tam KB, Chen YL. 2004. Adenovirus-mediated overexpression of catalase attenuates oxLDL-induced apoptosis in human aortic endothelial cells via AP-1 and c-Jun N-terminal kinase/extracellular signal-regulated kinase mitogen-activated protein kinase pathways. J Mol Cell Cardiol 36:129-139.
35. Lupo G, Nicotra A, Giurdanella G, Anfuso CD, Romeo L, Biondi G, Tirolo C, Marchetti B, Ragusa N, Alberghina M. 2005. Activation of phospholipase A2 and MAP kinases by oxidized low-density lipoproteins in immortalized GP8.39 endothelial cells. Biochim Biophys Acta 1735:135-150.
36. McGraw J, Hiebert GW, Steeves JD. 2001. Modulating astrogliosis after neurotrauma. J Neurosci Res 63:109-115.
37. McNally AK, Chisolm GM, Morel DW, Cathcart MK. 1990. Activated human monocytes oxidize low-density lipoprotein by a lipoxygenasedependent pathway. J Immunol 145:254-259.
38. Miller YI, Viriyakosol S, Worrall DS, Boullier A, Butler S, Witztum JL. 2005. Toll-like receptor 4-dependent and -independent cytokine secretion induced by minimally oxidized low-density lipoprotein in macrophages. Arterioscler Thromb Vasc Biol 25:1213-1219.
39. Montine TJ, Montine KS, Swift LL. 1997. Central nervous system lipoproteins in Alzheimer's disease. Am J Pathol 151:1571-1575.
40. Nie M, Pang L, Inoue H, Knox AJ. 2003. Transcriptional regulation of cyclooxygenase 2 by bradykinin and interleukin-1β in human airway smooth muscle cells: Involvement of different promoter elements, transcription factors, and histone H4 acetylation. Mol Cell Biol 23:9233-9244.
41. Parthasarathy S, Wieland E, Steinberg D. 1989. A role for endothelial cell lipoxygenase in the oxidative modification of low density lipoprotein. Proc Natl Acad Sci USA 86:1046-1050.
42. Pennypacker KR, Kassed CA, Eidizadeh S, O'Callaghan JP. 2000. Brain injury: Prolonged induction of transcription factors. Acta Neurobiol Exp (Wars) 60:515-530.
43. Pulverer BJ, Kyriakis JM, Avruch J, Nikolakaki E, Woodgett JR. 1991. Phosphorylation of c-jun mediated by MAP kinases. Nature 353:670-674.
44. Rangaswami H, Bulbule A, Kundu GC. 2005. JNK1 differentially regulates osteopontin-induced nuclear factor-inducing kinase/MEKK1-dependent activating protein-1-mediated promatrix metalloproteinase-9 activation. J Biol Chem 280:19381-19392.
45. Rosenberg GA. 2002. Matrix metalloproteinases in neuroinflammation. Glia 39:279-291.
46. Shaulian E, Karin M. 2001. AP-1 in cell proliferation and survival. Oncogene 20:2390-2400.
47. Shie FS, Neely MD, Maezawa I, Wu H, Olson SJ, Jurgens G, Montine KS, Montine TJ. 2004. Oxidized low-density lipoprotein is present in astrocytes surrounding cerebral infarcts and stimulates astrocyte interleukin-6 secretion. Am J Pathol 164:1173-1181.
48. Sparkman NL, Buchanan JB, Heyen JR, Chen J, Beverly JL, Johnson RW. 2006. Interleukin-6 facilitates lipopolysaccharide-induced disruption in working memory and expression of other proinflammatory cytokines in hippocampal neuronal cell layers. J Neurosci 26:10709-10716.
49. Svedin P, Hagberg H, Savman K, Zhu C, Mallard C. 2007. Matrix metalloproteinase- 9 gene knock-out protects the immature brain after cerebral hypoxia-ischemia. J Neurosci 27:1511-1518.
50. Uno M, Harada M, Takimoto O, Kitazato KT, Suzue A, Yoneda K, Morita N, Itabe H, Nagahiro S. 2005. Elevation of plasma oxidized LDL in acute stroke patients is associated with ischemic lesions depicted by DWI, predictive of infarct enlargement. Neurol Res 27:94-102.
51. Wang X, Mori T, Jung JC, Fini ME, Lo EH. 2002. Secretion of matrix metalloproteinase-2 and -9 after mechanical trauma injury in rat cortical cultures and involvement of MAP kinase. J Neurotrauma 19:615-625.
52. Woo CH, Lim JH, Kim JH. 2004. Lipopolysaccharide induces matrix metalloproteinase-9 expression via a mitochondrial reactive oxygen species-p38 kinase-activator protein-1 pathway in Raw 264.7 cells. J Immunol 173:6973-6980.
53. Wu CY, Hsieh HL, Jou MJ, Yang CM. 2004. Involvement of p42/p44 MAPK, p38 MAPK, JNK and nuclear factor-κB in interleukin-1βinduced matrix metalloproteinase-9 expression in rat brain astrocytes. J Neurochem 90:1477-1488.
54. Wu CY, Hsieh HL, Sun CC, Tseng CP, Yang CM. 2008. IL-1β induces proMMP-9 expression via c-Src-dependent PDGFR/PI3K/Akt/p300 cascade in rat brain astrocytes. J Neurochem 105:1499-1512.
55. Wu ZL, Wang YC, Zhou Q, Ge YQ, Lan Y. 2003. Oxidized LDL induces transcription factor activator protein-1 in rat mesangial cells. Cell Biochem Funct 21:249-256.
56. Xu J, Kim GM, Ahmed SH, Xu J, Yan P, Xu XM, Hsu CY. 2001. Glucocorticoid receptor-mediated suppression of activator protein-1 activation and matrix metalloproteinase expression after spinal cord injury. J Neurosci 21:92-97.
57. Yatsushige H, Ostrowski RP, Tsubokawa T, Colohan A, Zhang JH. 2007. Role of c-Jun N-terminal kinase in early brain injury after subarachnoid hemorrhage. J Neurosci Res 85:1436-1448.
58. Yong VW, Krekoski CA, Forsyth PA, Bell R, Edwards DR. 1998. Matrix metalloproteinases and diseases of the CNS. Trends Neurosci 21:75-80.
59. Yong VW, Power C, Forsyth P, Edwards DR. 2001. Metalloproteinases in biology and pathology of the nervous system. Nature Rev Neurosci 2:502-511.