Calmodulin kinase II-dependent transactivation of PDGF receptors mediates astrocytic MMP-9 expression and cell motility induced by lipoteichoic acid

Journal of Neuroinflammation

Volumn 7, Issue , 2010, Pages

  Wang, Hui Hsin ^a   Hsieh, Hsi Lung ^b   Yang, Chuen Mao ^a  

^a CHANG GUNG UNIVERSITY   (Taiwan)

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

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; GELATINASE B; LIPOTEICHOIC ACID; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN C JUN; PROTEIN KINASE B; SHORT HAIRPIN RNA; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; CALCIUM; LIPOPOLYSACCHARIDE; TEICHOIC ACID;

ANIMAL CELL; ARTICLE; ASTROCYTE; BINDING SITE; CALCIUM SIGNALING; CELL FUNCTION; CELL MIGRATION; CELL MOTILITY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENETIC TRANSFECTION; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LIPID INTERACTION; RAT; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING; ZYMOGRAPHY; ANIMAL; CELL LINE; CELL MOTION; CYTOLOGY; DRUG EFFECT; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ANIMALS; ASTROCYTES; CALCIUM; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL LINE; CELL MOVEMENT; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIPOPOLYSACCHARIDES; MATRIX METALLOPROTEINASE 9; PHOSPHATIDYLINOSITOL 3-KINASES; RATS; RECEPTORS, PLATELET-DERIVED GROWTH FACTOR; SIGNAL TRANSDUCTION; TEICHOIC ACIDS; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTIONAL ACTIVATION;

EID: 78549251420     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-7-84     Document Type: Article

References (58)

1. Lee SJ, Lee S. Toll-like receptors and inflammation in the CNS. Curr Drug Targets Inflamm Allergy 2002, 1:181-191. 10.2174/1568010023344698, 14561199.
2. Konat GW, Kielian T, Marriott I. The role of Toll-like receptors in CNS response to microbial challenge. J Neurochem 2006, 99:1-12. 10.1111/j.1471-4159.2006.04076.x, 2423668, 16899072.
3. Sutcliffe IC, Shaw N. Atypical lipoteichoic acids of gram-positive bacteria. J Bacteriol 1991, 173:7065-7069. 209210, 1938910.
4. Neher JJ, Brown GC. Neurodegeneration in models of Gram-positive bacterial infections of the central nervous system. Biochem Soc Trans 2007, 35:1166-1167. 10.1042/BST0351166, 17956303.
5. Schroder NW, Morath S, Alexander C, Hamann L, Hartung T, Zahringer U, Gobel UB, Weber JR, Schumann RR. Lipoteichoic acid (LTA) of Streptococcus pneumoniae and Staphylococcus aureus activates immune cells via Toll-like receptor (TLR)-2, lipopolysaccharide-binding protein (LBP), and CD14, whereas TLR-4 and MD-2 are not involved. J Biol Chem 2003, 278:15587-15594. 10.1074/jbc.M212829200, 12594207.
6. Mullaly SC, Kubes P. The role of TLR2 in vivo following challenge with Staphylococcus aureus and prototypic ligands. J Immunol 2006, 177:8154-8163.
7. Liew FY, Xu D, Brint EK, O'Neill LA. Negative regulation of toll-like receptor-mediated immune responses. Nat Rev Immunol 2005, 5:446-458. 10.1038/nri1630, 15928677.
8. Mitchell JA, Paul-Clark MJ, Clarke GW, McMaster SK, Cartwright N. Critical role of toll-like receptors and nucleotide oligomerisation domain in the regulation of health and disease. J Endocrinol 2007, 193:323-330. 10.1677/JOE-07-0067, 17535871.
9. Kinsner A, Pilotto V, Deininger S, Brown GC, Coecke S, Hartung T, Bal-Price A. Inflammatory neurodegeneration induced by lipoteichoic acid from Staphylococcus aureus is mediated by glia activation, nitrosative and oxidative stress, and caspase activation. J Neurochem 2005, 95:1132-1143. 10.1111/j.1471-4159.2005.03422.x, 16144539.
10. Lehnardt S, Henneke P, Lien E, Kasper DL, Volpe JJ, Bechmann I, Nitsch R, Weber JR, Golenbock DT, Vartanian T. A mechanism for neurodegeneration induced by group B streptococci through activation of the TLR2/MyD88 pathway in microglia. J Immunol 2006, 177:583-592.
11. Ziegler G, Harhausen D, Schepers C, Hoffmann O, Rohr C, Prinz V, Konig J, Lehrach H, Nietfeld W, Trendelenburg G. TLR2 has a detrimental role in mouse transient focal cerebral ischemia. Biochem Biophys Res Commun 2007, 359:574-579. 10.1016/j.bbrc.2007.05.157, 17548055.
12. Carpentier PA, Duncan DS, Miller SD. Glial toll-like receptor signaling in central nervous system infection and autoimmunity. Brain Behav Immun 2008, 22:140-147. 10.1016/j.bbi.2007.08.011, 2231624, 17920811.
13. Bowman CC, Rasley A, Tranguch SL, Marriott I. Cultured astrocytes express toll-like receptors for bacterial products. Glia 2003, 43:281-291. 10.1002/glia.10256, 12898707.
14. Bsibsi M, Bajramovic JJ, Van Duijvenvoorden E, Persoon C, Ravid R, Van Noort JM, Vogt MH. Identification of soluble CD14 as an endogenous agonist for Toll-like receptor 2 on human astrocytes by genome-scale functional screening of glial cell derived proteins. Glia 2007, 55:473-482. 10.1002/glia.20473, 17205552.
15. Jack CS, Arbour N, Manusow J, Montgrain V, Blain M, McCrea E, Shapiro A, Antel JP. TLR signaling tailors innate immune responses in human microglia and astrocytes. J Immunol 2005, 175:4320-4330.
16. Krasowska-Zoladek A, Banaszewska M, Kraszpulski M, Konat GW. Kinetics of inflammatory response of astrocytes induced by TLR 3 and TLR4 ligation. J Neurosci Res 2007, 85:205-212. 10.1002/jnr.21088, 17061254.
17. De Keyser J, Mostert JP, Koch MW. Dysfunctional astrocytes as key players in the pathogenesis of central nervous system disorders. J Neurol Sci 2008, 267:3-16. 10.1016/j.jns.2007.08.044, 17935736.
18. Aoki T, Sumii T, Mori T, Wang X, Lo EH. Blood-brain barrier disruption and matrix metalloproteinase-9 expression during reperfusion injury: mechanical versus embolic focal ischemia in spontaneously hypertensive rats. Stroke 2002, 33:2711-2717. 10.1161/01.STR.0000033932.34467.97, 12411666.
19. Harris JE, Nuttall RK, Elkington PT, Green JA, Horncastle DE, Graeber MB, Edwards DR, Friedland JS. Monocyte-astrocyte networks regulate matrix metalloproteinase gene expression and secretion in central nervous system tuberculosis in vitro and in vivo. J Immunol 2007, 178:1199-1207.
20. Wu CY, Hsieh HL, Jou MJ, Yang CM. Involvement of p42/p44 MAPK, p38 MAPK, JNK and nuclear factor-κB in interleukin-1beta-induced matrix metalloproteinase-9 expression in rat brain astrocytes. J Neurochem 2004, 90:1477-1488. 10.1111/j.1471-4159.2004.02682.x, 15341531.
21. Lee WJ, Shin CY, Yoo BK, Ryu JR, Choi EY, Cheong JH, Ryu JH, Ko KH. 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 2003, 41:15-24. 10.1002/glia.10131, 12465042.
22. Rosenberg GA. Matrix metalloproteinases in neuroinflammation. Glia 2002, 39:279-291. 10.1002/glia.10108, 12203394.
23. Souza LF, Jardim FR, Sauter IP, Souza MM, Barreto F, Margis R, Bernard EA. Lipoteichoic acid from Staphylococcus aureus increases matrix metalloproteinase 9 expression in RAW 264.7 macrophages: modulation by A2A and A2B adenosine receptors. Mol Immunol 2009, 46:937-942. 10.1016/j.molimm.2008.09.012, 18950865.
24. Hsieh HL, Wu CY, Yang CM. Bradykinin induces matrix metalloproteinase-9 expression and cell migration through a PKC-δ-dependent ERK/Elk-1 pathway in astrocytes. Glia 2008, 56:619-632. 10.1002/glia.20637, 18240315.
25. Wang HH, Hsieh HL, Wu CY, Sun CC, Yang CM. Oxidized low-density lipoprotein induces matrix metalloproteinase-9 expression via a p42/p44 and JNK-dependent AP-1 pathway in brain astrocytes. Glia 2009, 57:24-38. 10.1002/glia.20732, 18661553.
26. Cario E, Gerken G, Podolsky DK. Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function. Gastroenterolog 2007, 132:1359-1374.
27. O'Neill LA. Primer: Toll-like receptor signaling pathways--what do rheumatologists need to know?. Nat Clin Pract Rheumatol 2008, 4:319-327. 10.1038/ncprheum0802, 18446139.
28. Sadik CD, Hunfeld KP, Bachmann M, Kraiczy P, Eberhardt W, Brade V, Pfeilschifter J, Muhl H. Systematic analysis highlights the key role of TLR2/NF-κB/MAP kinase signaling for IL-8 induction by macrophage-like THP-1 cells under influence of Borrelia burgdorferi lysates. Int J Biochem Cell Biol 2008, 40:2508-2521. 10.1016/j.biocel.2008.04.014, 18571457.
29. Wu CY, Hsieh HL, Sun CC, Tseng CP, Yang CM. IL-1β induces proMMP-9 expression via c-Src-dependent PDGFR/PI3K/Akt/p300 cascade in rat brain astrocytes. J Neurochem 2008, 105:1499-1512. 10.1111/j.1471-4159.2008.05318.x, 18315570.
30. Hsieh HL, Wang HH, Wu CY, Tung WH, Yang CM. Lipoteichoic acid induces matrix metalloproteinase-9 expression via transactivation of PDGF receptors and NF-κB activation in rat brain astrocytes. Neurotox Res 2010, 17:344-359. 10.1007/s12640-009-9111-4, 19763735.
31. Jou TC, Jou MJ, Chen JY, Lee SY. Properties of rat brain astrocytes in long-term culture. Taiwan Yi Xue Hui Za Zhi 1985, 84:865-881.
32. Hsieh HL, Yen MH, Jou MJ, Yang CM. Intracellular signalings underlying bradykinin-induced matrix metalloproteinase-9 expression in rat brain astrocyte-1. Cell Signal 2004, 16:1163-1176. 10.1016/j.cellsig.2004.03.021, 15240011.
33. Grynkiewicz G, Poenie M, Tsien RY. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 1985, 260:3440-3450.
34. Han S, Ritzenthaler JD, Sitaraman SV, Roman J. 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 2006, 281:29614-26924. 10.1074/jbc.M604013200, 16882662.
35. Wu CY, Hsieh HL, Sun CC, Yang CM. IL-1β induces MMP-9 expression via a Ca2+-dependent CaMKII/JNK/c-JUN cascade in rat brain astrocytes. Glia 2009, 57:1775-1789. 10.1002/glia.20890, 19455716.
36. Wang W, Hou XY, Gao C, Liu Y, Zong YY, Zhang GY. Regulation of c-Jun N-terminal kinase activation in hydrogen peroxide induced neurotoxicity. J Neurocytol 2003, 32:143-151. 10.1023/B:NEUR.0000005599.10952.33, 14707549.
37. Hahm ER, Gho YS, Park S, Park C, Kim KW, Yang CH. Synthetic curcumin analogs inhibit activator protein-1 transcription and tumor-induced angiogenesis. Biochem Biophys Res Commun 2004, 321:337-344. 10.1016/j.bbrc.2004.06.119, 15358181.
38. Xu J, Kim GM, Ahmed SH, Xu J, Yan P, Xu XM, Hsu CY. Glucocorticoid receptor-mediated suppression of activator protein-1 activation and matrix metalloproteinase expression after spinal cord injury. J Neurosci 2001, 21:92-97.
39. Saez-Llorens X, McCracken GH. Bacterial meningitis in children. Lancet 2003, 361:2139-2148. 10.1016/S0140-6736(03)13693-8, 12826449.
40. Scarborough M, Thwaites GE. The diagnosis and management of acute bacterial meningitis in resource-poor settings. Lancet Neurol 2008, 7:637-648. 10.1016/S1474-4422(08)70139-X, 18565457.
41. Doran KS, Engelson EJ, Khosravi A, Maisey HC, Fedtke I, Equils O, Michelsen KS, Arditi M, Peschel A, Nizet V. Blood-brain barrier invasion by group B Streptococcus depends upon proper cell-surface anchoring of lipoteichoic acid. J Clin Invest 2005, 115:2499-2507. 10.1172/JCI23829, 1193870, 16138192.
42. Svedin P, Hagberg H, Savman K, Zhu C, Mallard C. Matrix metalloproteinase-9 gene knock-out protects the immature brain after cerebral hypoxia-ischemia. J Neurosci 2007, 27:1511-1518. 10.1523/JNEUROSCI.4391-06.2007, 17301159.
43. McColl BW, Rothwell NJ, Allan SM. Systemic inflammation alters the kinetics of cerebrovascular tight junction disruption after experimental stroke in mice. J Neurosci 2008, 28:9451-9462. 10.1523/JNEUROSCI.2674-08.2008, 18799677.
44. Tarsi-Tsuk D, Levy R. Stimulation of the respiratory burst in peripheral blood monocytes by lipoteichoic acid. The involvement of calcium ions and phospholipase A2. J Immunol 1990, 144:2665-2670.
45. Beskina O, Miller A, Mazzocco-Spezzia A, Pulina MV, Golovina VA. Mechanisms of interleukin-1beta-induced Ca2+ signals in mouse cortical astrocytes: roles of store- and receptor-operated Ca2+ entry. Am J Physiol Cell Physiol 2007, 293:C1103-1111. 10.1152/ajpcell.00249.2007, 17670890.
46. Pita I, Jelaso AM, Ide CF. IL-1β increases intracellular calcium through an IL-1 type 1 receptor mediated mechanism in C6 astrocytic cells. Int J Dev Neurosci 1999, 17:813-820. 10.1016/S0736-5748(99)00063-5, 10593617.
47. Lee CW, Chien CS, Yang CM. Lipoteichoic acid-stimulated p42/p44 MAPK activation via Toll-like receptor 2 in tracheal smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2004, 286:L921-930. 10.1152/ajplung.00124.2003, 15064239.
48. Bayer KU, Schulman H. Regulation of signal transduction by protein targeting: the case for CaMKII. Biochem Biophys Res Commun 2001, 289:917-923. 10.1006/bbrc.2001.6063, 11741277.
49. Quinn CO, Rajakumar RA, Agapova OA. Parathyroid hormone induces rat interstitial collagenase mRNA through Ets-1 facilitated by cyclic AMP response element-binding protein and Ca2+/calmodulin-dependent protein kinase II in osteoblastic cells. J Mol Endocrinol 2000, 25:73-84. 10.1677/jme.0.0250073, 10915220.
50. Hsieh HL, Tung WH, Wu CY, Wang HH, Lin CC, Wang TS, Yang CM. Thrombin induces EGF receptor expression and cell proliferation via a PKC(δ)/c-Src-dependent pathway in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 2009, 29:1594-1601. 10.1161/ATVBAHA.109.185801, 19628787.
51. Belcheva MM, Szùcs M, Wang D, Sadee W, Coscia CJ. μ-Opioid receptor-mediated ERK activation involves calmodulin-dependent epidermal growth factor receptor transactivation. J Biol Chem 2001, 276:33847-33853. 10.1074/jbc.M101535200, 11457825.
52. Byun HJ, Hong IK, Kim E, Jin YJ, Jeoung DI, Hahn JH, Kim YM, Park SH, Lee H. 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 2006, 281:34833-34847. 10.1074/jbc.M605483200, 16984917.
53. Woo CH, Lim JH, Kim JH. 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 2004, 173:6973-6980.
54. Shaulian E, Karin M. AP-1 in cell proliferation and survival. Oncogene 2001, 20:2390-2400. 10.1038/sj.onc.1204383, 11402335.
55. Eberhardt W, Schulze M, Engels C, Klasmeier E, Pfeilschifter J. 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 2002, 16:1752-1766. 10.1210/me.2001-0278, 12145332.
56. Raivich G, Behrens A. Role of the AP-1 transcription factor c-Jun in developing, adult and injured brain. Prog Neurobiol 2006, 78:347-363. 10.1016/j.pneurobio.2006.03.006, 16716487.
57. Lauffenburger DA, Horwitz AF. Cell migration: a physically integrated molecular process. Cell 1996, 84:359-369. 10.1016/S0092-8674(00)81280-5, 8608589.
58. Huang C, Jacobson K, Schaller MD. MAP kinases and cell migration. J Cell Sci 2004, 117:4619-4628. 10.1242/jcs.01481, 15371522.