IL-1β induces proMMP-9 expression via c-Src-dependent PDGFR/PI3K/Akt/p300 cascade in rat brain astrocytes

Journal of Neurochemistry

Volumn 105, Issue 4, 2008, Pages 1499-1512

  Wu, Cheng Ying ^a   Hsieh, Hsi Lung ^a   Sun, Chi Chin ^a   Tseng, Ching Ping ^b   Yang, Chuen Mao ^a,c  

^a CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

^c CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

Author keywords

Astrocytes; Interleukin 1 ; Matrix metalloproteinases; p300; Platelet derived growth factor receptor transactivation

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 4 AMINO 7 TERT BUTYL 5 (4 METHYLPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; 6,7 DIMETHOXY 2 PHENYLQUINOXALINE; CURCUMIN; GELATINASE B; GENISTEIN; HISTONE H4; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN KINASE B; PROTEIN P300; PROTEIN TYROSINE KINASE; SHORT HAIRPIN RNA;

ANIMAL CELL; ARTICLE; ASTROCYTE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; NONHUMAN; ONCOGENE SRC; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; UPREGULATION; WESTERN BLOTTING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ASTROCYTES; CELL LINE; CELLS, CULTURED; ENZYME INDUCTION; ENZYME PRECURSORS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENES, SRC; HUMANS; INTERLEUKIN-1BETA; MATRIX METALLOPROTEINASE 9; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RECEPTORS, PLATELET-DERIVED GROWTH FACTOR; SIGNAL TRANSDUCTION;

RATTUS;

EID: 42549152437     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05318.x     Document Type: Article

References (62)

1. Alexander J. P. Acott T. S. (2001) Involvement of protein kinase C in TNFα regulation of trabecular matrix metalloproteinases and TIMPs. Invest. Ophthalmol. Vis. Sci. 42, 2831 2838.
2. Andjelkovic M., Alessi D. R., Meier R., Fernandez A., Lamb N. J., Frech M., Cron P., Cohen P., Lucocq J. M. Hemmings B. A. (1997) Role of translocation in the activation and function of protein kinase B. J. Biol. Chem. 272, 31515 31524.
3. Andreev J., Galisteo M. L., Kranenburg O., Logan S. K., Chiu E. S., Okigaki M., Cary L. A., Moolenaar W. H. Schlessinger J. (2001) Src and PYK2 mediate G-protein-coupled receptor activation of epidermal growth factor receptor (EGFR) but are not required for coupling to the mitogen-activated protein (MAP) kinase signaling cascade. J. Biol. Chem. 276, 20130 20135.
4. Balasubramanyam K., Varier R. A., Altaf M., Swaminathan V., Siddappa N. B., Ranga U. Kundu T. K. (2004) Curcumin, a novel p300/CREB-binding protein-specific inhibitor of acetyltransferase, represses the acetylation of histone/nonhistone proteins and histone acetyltransferase-dependent chromatin transcription. J. Biol. Chem. 279, 51163 51171.
5. Byun H. J., Hong I. K., Kim E., Jin Y. J., Jeoung D. I., Hahn J. H., Kim Y. M., Park S. H. 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.
6. Campbell I. L. Pagenstecher A. (1999) Matrix metalloproteinases and their inhibitors in the nervous system: the good, the bad and the enigmatic. Trends Neurosci. 22, 285 287.
7. Chambaut-Guerin A. M., Herigault S., Rouet-Benzineb P., Rouher C. Lafuma C. (2000) Induction of matrix metalloproteinase MMP-9 (92-kDa gelatinase) by retinoic acid in human neuroblastoma SKNBE cells: relevance to neuronal differentiation. J. Neurochem. 74, 508 517.
8. Cooper K. L., Myers T. A., Rosenberg M., Chavez M. Hudson L. G. (2004) Roles of mitogen activated protein kinases and EGF receptor in arsenite-stimulated matrix metalloproteinase-9 production. Toxicol. Appl. Pharmacol. 200, 177 185.
9. Dikic I., Tokiwa G., Lev S., Courtneidge S. A. Schlessinger J. (1996) A role for PYK2 and Src in linking G-protein-coupled receptors with MAP kinase activation. Nature 383, 547 550.
10. Dinarello C. A. (1997) Interleukin-1. Cytokine Growth Factor Rev. 8, 253 265.
11. Downward J. (1995) Signal transduction. A target for PI(3) kinase. Nature 376, 553 554.
12. 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.
13. Eguchi S., Iwasaki H., Inagami T., Numaguchi K., Yamakawa T., Motley E. D., Owada K. M., Marumo F. Hirata Y. (1999) Involvement of PYK2 in angiotensin II signaling of vascular smooth muscle cells. Hypertension 33, 201 206.
14. Esteve P. O., Chicoine E., Robledo O., Aoudjit F., Descoteaux A., Potworowski E. F. St Pierre Y. (2002) Protein kinase C-ζ regulates transcription of the matrix metalloproteinase-9 gene induced by IL-1 and TNF-alpha in glioma cells via NF-kappa B. J. Biol. Chem. 277, 35150 35155.
15. Fabunmi R. P., Baker A. H., Murray E. J., Booth R. F. Newby A. C. (1996) Divergent regulation by growth factors and cytokines of 95 kDa and 72 kDa gelatinases and tissue inhibitors or metalloproteinases-1, -2, and -3 in rabbit aortic smooth muscle cells. Biochem. J. 315 (Pt. 1 335 342.
16. Franke T. F., Kaplan D. R., Cantley L. C. Toker A. (1997) Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4- bisphosphate. Science 275, 665 668.
17. Galis Z. S., Muszynski M., Sukhova G. K., Simon-Morrissey E., Unemori E. N., Lark M. W., Amento E. Libby P. (1994) Cytokine-stimulated human vascular smooth muscle cells synthesize a complement of enzymes required for extracellular matrix digestion. Circ. Res. 75, 181 189.
18. Gottschall P. E. Deb S. (1996) Regulation of matrix metalloproteinase expressions in astrocytes, microglia and neurons. [Review] [57 refs]. Neuroimmunomodulation 3, 69 75.
19. Gutkind J. S. (1998) Cell growth control by G protein-coupled receptors: from signal transduction to signal integration. Oncogene 17, 1331 1342.
20. Hartung H. P. Kieseier B. C. (2000) The role of matrix metalloproteinases in autoimmune damage to the central and peripheral nervous system. [Review] [60 refs]. J. Neuroimmunol. 107, 140 147.
21. Hemmings B. A. (1997) Akt signaling: linking membrane events to life and death decisions. Science 275, 628 630.
22. Hirota K., Murata M., Itoh T., Yodoi J. Fukuda K. (2001) Redox-sensitive transactivation of epidermal growth factor receptor by tumor necrosis factor confers the NF-κB activation. J. Biol. Chem. 276, 25953 25958.
23. Hsieh H. L., Yen M. H., Jou M. J. Yang C. M. (2004) Intracellular signalings underlying bradykinin-induced matrix metalloproteinase-9 expression in rat brain astrocyte-1. Cell. Signal. 16, 1163 1176.
24. Huang W. C. Chen C. C. (2005) Akt phosphorylation of p300 at Ser-1834 is essential for its histone acetyltransferase and transcriptional activity. Mol. Cell. Biol. 25, 6592 6602.
25. Jou T. C., Jou M. J., Chen J. Y. Lee S. Y. (1985) Properties of rat brain astrocytes in long-term culture. J. Formos. Med. Assoc. 84, 865 881.
26. Koyasu S. (2003) The role of PI3K in immune cells. Nat. Immunol. 4, 313 319.
27. Kraus S., Benard O., Naor Z. Seger R. (2003) c-Src is activated by the epidermal growth factor receptor in a pathway that mediates JNK and ERK activation by gonadotropin-releasing hormone in COS7 cells. J. Biol. Chem. 278, 32618 32630.
28. Lee W. J., Shin C. Y., Yoo B. K., Ryu J. R., Choi E. Y., Cheong J. H., Ryu J. H. Ko K. H. (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.
29. Lee C. W., Lin C. C., Lin W. N., Liang K. C., Luo S. F., Wu C. B., Wang S. W. Yang C. M. (2007) TNF-alpha induces MMP-9 expression via activation of Src/EGFR, PDGFR/PI3K/Akt cascade and promotion of NF-κB/p300 binding in human tracheal smooth muscle cells. Am. J. Physiol. Lung Cell Mol. Physiol. 292, L799 L812.
30. Liang K. C., Lee C. W., Lin W. N., Lin C. C., Wu C. B., Luo S. F. Yang C. M. (2007) Interleukin-1β induces MMP-9 expression via p42/p44 MAPK, p38 MAPK, JNK, and nuclear factor-κB signaling pathways in human tracjeal smooth muscle cells. J. Cell. Physiol. 211, 759 770.
31. Lin C. C., Lee C. W., Chu T. H., Cheng C. Y., Luo S. F., Hsiao L. D. Yang C. M. (2007) Transactivation of Src, PDGF receptor, and Akt is involved in IL-1beta-induced ICAM-1 expression in A549 cells. J. Cell. Physiol. 211, 771 780.
32. Lu Y. Wahl L. M. (2005) Production of matrix metalloproteinase-9 by activated human monocytes involves a phosphatidylinositol-3 kinase/Akt/ IKKα/NF-κB pathway. J. Leukoc. Biol. 78, 259 265.
33. Lukes A., Mun-Bryce S., Lukes M. Rosenberg G. A. (1999) Extracellular matrix degradation by metalloproteinases and central nervous system diseases. Mol. Neurobiol. 19, 267 284.
34. Luttrell L. M., Daaka Y. Lefkowitz R. J. (1999) Regulation of tyrosine kinase cascades by G-protein-coupled receptors. [Review] [56 refs]. Curr. Opin. Cell Biol. 11, 177 183.
35. Ma Z., Chang M. J., Shah R. C. Benveniste E. N. (2005) Interferon-gamma-activated STAT-1α suppresses MMP-9 gene transcription by sequestration of the coactivators CBP/p300. J. Leukoc. Biol. 78, 515 523.
36. Malinin N. L., Boldin M. P., Kovalenko A. V. Wallach D. (1997) MAP3K-related kinase involved in NF-κB induction by TNF, CD95 and IL-1. Nature 385, 540 544.
37. Marcu M. G., Jung Y. J., Lee S., Chung E. J., Lee M. J., Trepel J. Neckers L. (2006) Curcumin is an inhibitor of p300 histone acetylatransferase. Med. Chem. 2, 169 174.
38. 2+-dependent protein kinase C, Raf/MEK/ERK and IKK/IκB/NF-κB signal cascades. Biochem. Pharmacol. 69, 433 449.
39. Moghal N. Sternberg P. W. (1999) Multiple positive and negative regulators of signaling by the EGF-receptor. Curr. Opin. Cell Biol. 11, 190 196.
40. Nie M., Pang L., Inoue H. Knox A. J. (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. Okada Y., Gonoji Y., Naka K., Tomita K., Nakanishi I., Iwata K., Yamashita K. Hayakawa T. (1992) Matrix metalloproteinase 9 (92-kDa gelatinase/type IV collagenase) from HT 1080 human fibrosarcoma cells. Purification and activation of the precursor and enzymic properties. J. Biol. Chem. 267, 21712 21719.
42. Ozes O. N., Mayo L. D., Gustin J. A., Pfeffer S. R., Pfeffer L. M. Donner D. B. (1999) NF-κB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 401, 82 85.
43. Ries C. Petrides P. E. (1995) Cytokine regulation of matrix metalloproteinase activity and its regulatory dysfunction in disease. [Review] [100 refs]. Biol. Chem. Hoppe Seyler 376, 345 355.
44. Roelle S., Grosse R., Aigner A., Krell H. W., Czubayko F. Gudermann T. (2003) Matrix metalloproteinases 2 and 9 mediate epidermal growth factor receptor transactivation by gonadotropin-releasing hormone. J. Biol. Chem. 278, 47307 47318.
45. Romanic A. M. Madri J. A. (1994) Extracellular matrix-degrading proteinases in the nervous system. [Review] [117 refs]. Brain Pathol. 4, 145 156.
46. Romashkova J. A. Makarov S. S. (1999) NF-κB is a target of AKT in anti-apoptotic PDGF signalling. Nature 401, 86 90.
47. Rosenberg G. A., Cunningham L. A., Wallace J., Alexander S., Estrada E. Y., Grossetete M., Razhagi A., Miller K. Gearing A. (2001) Immunohistochemistry of matrix metalloproteinase in reperfusion injury to rat brain: activation of MMP-9 linked to stromelysin-1 and microglia in cell cultures. Brain Res. 893, 104 112.
48. Rosette C. Karin M. (1996) Ultraviolet light and osmotic stress: activation of the JNK cascade through multiple growth factor and cytokine receptors. Science 274, 1194 1197.
49. Rostworowski M., Balasingam V., Chabot S., Owens T. Yong V. W. (1997) Astrogliosis in the neonatal and adult murine brain post-trauma: elevation of inflammatory cytokines and the lack of requirement for endogenous interferon-γ. J. Neurosci. 17, 3664 3674.
50. Rothwell N. (2003) Interleukin-1 and neuronal injury: mechanisms, modification, and therapeutic potential. [Review] [12 refs]. Brain Behav. Immun. 17, 152 157.
51. Sato H. Seiki M. (1993) Regulatory mechanism of 92 kDa type IV collagenase gene expression which is associated with invasiveness of tumor cells. Oncogene 8, 395 405.
52. Sato H., Kita M. Seiki M. (1993) v-Src activates the expression of 92-kDa type IV collagenase gene through the AP-1 site and the GT box homologous to retinoblastoma control elements. A mechanism regulating gene expression independent of that by inflammatory cytokines. J. Biol. Chem. 268, 23460 23468.
53. Senior R. M., Griffin G. L., Fliszar C. J., Shapiro S. D., Goldberg G. I. Welgus H. G. (1991) Human 92- and 72-kilodalton type IV collagenases are elastases. J. Biol. Chem. 266, 7870 7875.
54. Sizemore N., Lerner N., Dombrowski N., Sakurai H. Stark G. R. (2002) Distinct roles of the IκB kinase α and β subunits in liberating nuclear factor-κB (NF-κB) from IκB and in phosphorylating the p65 subunit of NF-κB. J. Biol. Chem. 277, 3863 3869.
55. Tang H., Zhao Z. J., Landon E. J. Inagami T. (2000) Regulation of calcium-sensitive tyrosine kinase PYK2 by angiotensin II in endothelial cells. Roles of yes tyrosine kinase and tyrosine phosphatase SHP-2. J. Biol. Chem. 275, 8389 8396.
56. Tice D. A., Biscardi J. S., Nickles A. L. Parsons S. J. (1999) Mechanism of biological synergy between cellular Src and epidermal growth factor receptor. Proc. Natl Acad. Sci. USA 96, 1415 1420.
57. Vecil G. G., Larsen P. H., Corley S. M., Herx L. M., Besson A., Goodyer C. G. Yong V. W. (2000) Interleukin-1 is a key regulator of matrix metalloproteinase-9 expression in human neurons in culture and following mouse brain trauma in vivo. J. Neurosci. Res. 61, 212 224.
58. Wu C. Y., Hsieh H. L., Jou M. J. Yang C. M. (2004) Involvement of p42/p44 MAPK, p38 MAPK, JNK and nuclear factor-kappa B in interleukin-1β-induced matrix metalloproteinase-9 expression in rat brain astrocytes. J. Neurochem. 90, 1477 1488.
59. Yang C. M., Lin M. I., Hsieh H. L., Sun C. C., Ma Y. H. Hsiao L. D. (2004) Bradykinin-induced p42/p44 MAPK phosphorylation and cell proliferation via Src, EGF receptors, and PI3-K/Akt in vascular smooth muscle cells. J. Cell. Physiol. 203, 538 546.
60. Yao J., Xiong S., Klos K., Nguyen N., Grijalva R., Li P. Yu D. (2001) Multiple signaling pathways involved in activation of matrix metalloproteinase-9 (MMP-9) by heregulin-β1 in human breast cancer cells. Oncogene 20, 8066 8074.
61. Yong V. W., Power C., Forsyth P. Edwards D. R. (2001) Metalloproteinases in biology and pathology of the nervous system. [Review] [100 refs]. Nat. Rev. Neurosci. 2, 502 511.
62. Zwick E., Wallasch C., Daub H. Ullrich A. (1999) Distinct calcium-dependent pathways of epidermal growth factor receptor transactivation and PYK2 tyrosine phosphorylation in PC12 cells. J. Biol. Chem. 274, 20989 20996.