Advertisement

Archives of Virology

, Volume 158, Issue 12, pp 2561–2575 | Cite as

Matrix metalloproteinases and their tissue inhibitors in serum and cerebrospinal fluid of children with Japanese encephalitis virus infection

  • Vibha Shukla
  • Akhalesh Kumar Shakya
  • T. N. Dhole
  • Usha Kant Misra
Original Article

Abstract

The expression of matrix metalloproteinases (MMPs) is tightly regulated at the level of gene transcription, conversion of pro-enzyme to active MMPs, and the action of tissue inhibitors of metalloproteinases (TIMPs). The present study aimed to investigate the expression of some specific MMPs (2, 7, 9) and TIMPs (1, 2, 3) in serum and cerebrospinal fluid (CSF) of children with Japanese encephalitis virus (JEV) infection. Serum and CSF levels of MMPs and TIMPs in children with JEV infection and disease control (DC) were compared. The CSF and serum concentrations of MMP-2, TIMP-2 and TIMP-3 were significantly higher in children with JEV infection compared to DC. The concentration of MMP-9 in serum was significantly higher in children with JEV infection than in the DC and healthy control (HC), while in the CSF, no significant difference was observed compared to DC. The MMP-7 serum concentration was significantly higher in children with JEV infection compared to HC, but no significant difference was observed compared to DC. MMP-7 concentration was undetectable in CSF in both groups. The TIMP-1 CSF concentration was significantly higher, while the serum concentration was significantly lower, in children with JEV infection compared to DC. No correlation was found between the levels of each biomolecule measured in CSF and serum, suggesting that the levels in CSF represent local production within the CNS rather than production in the periphery. We also observed leucocytosis, mononuclear pleocytosis and elevated protein concentrations in the CSF of children with JEV infection compared to DC.

Keywords

Japanese Encephalitis Virus Amyotrophic Lateral Sclerosis Patient Japanese Encephalitis Virus Japanese Encephalitis Virus Infection ELISA Unit 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We wish to thank Dr. Sudhanshu Vrati for giving us Japanese encephalitis virus strain GP-78. We thank Dr. S.K. Mandal for his assistance in statistical analysis. AK and VS carried out all experiments and analysis and drafted the manuscript. TND and UKM participated in the design of the study and helped to draft the manuscript. All of the authors have read and approved the final manuscript. This work was supported by a grant (No. Immuno/18/11/13/2008-ECD-I) from the Indian Council of Medical Research, New Delhi, India.

Conflict of interest

The authors have no commercial affiliations or conflict of interest to declare.

References

  1. 1.
    Amour A, Knight CG, Webster A, Slocombe PM, Stephens PE, Knäuper V, Docherty AJP, Murphy G (2000) The in vitro activity of ADAM-10 is inhibited by TIMP-1 and TIMP-3. FEBS Lett 473:275–279PubMedCrossRefGoogle Scholar
  2. 2.
    Anthony DC, Ferguson B, Matyzak MK, Miller KM, Esiri MM, Perry VH (1997) Differential matrix metalloproteinase expression in cases of multiple sclerosis and stroke. Neuropathol Appl Neurobiol 23:406–415PubMedCrossRefGoogle Scholar
  3. 3.
    Apostolski S, Nikolić J, Bugarski-Prokopljević C, Miletić V, Pavlović S, Filipović S (1991) Serum and CSF immunological findings in ALS. Acta neurologica scandinavica 83:96–98PubMedCrossRefGoogle Scholar
  4. 4.
    Avolio C, Ruggieri M, Giuliani F, Liuzzi GM, Leante R, Riccio P, Livrea P, Trojano M (2003) Serum MMP-2 and MMP-9 are elevated in different multiple sclerosis subtypes. J Neuroimmunol 136:46–53PubMedCrossRefGoogle Scholar
  5. 5.
    Avolio C, Filippi M, Tortorella C, Rocca MA, Ruggieri M, Agosta F, Tomassini V, Pozzilli C, Stecchi S, Giaquinto P (2005) Serum MMP-9/TIMP-1 and MMP-2/TIMP-2 ratios in multiple sclerosis: relationships with different magnetic resonance imaging measures of disease activity during IFN-beta-1a treatment. Mult Scler 11:441–446PubMedCrossRefGoogle Scholar
  6. 6.
    Azeh I, Mäder M, Smirnov A, Beuche W, Nau R, Weber F (1998) Experimental pneumococcal meningitis in rabbits: the increase of matrix metalloproteinase-9 in cerebrospinal fluid correlates with leucocyte invasion. Neurosci Lett 256:127–130PubMedCrossRefGoogle Scholar
  7. 7.
    Banati RB, Gehrmann J, Schubert P, Kreutzberg GW (1993) Cytotoxicity of microglia. Glia 7:111–118PubMedCrossRefGoogle Scholar
  8. 8.
    Bar-Or A, Nuttall RK, Duddy M, Alter A, Kim HJ, Ifergan I, Pennington CJ, Bourgoin P, Edwards DR, Yong VW (2003) Analyses of all matrix metalloproteinase members in leukocytes emphasize monocytes as major inflammatory mediators in multiple sclerosis. Brain 126:2738–2749PubMedCrossRefGoogle Scholar
  9. 9.
    BenesovA Y, Vasku A, Novotna H, Litzman J, Stourac P, Beranek M, Kadanka Z, Bednarik J (2009) Matrix metalloproteinase-9 and matrix metalloproteinase-2 as biomarkers of various courses in multiple sclerosis. Mult Scler 15:316–322PubMedCrossRefGoogle Scholar
  10. 10.
    Chaudhuri A, Yang B, Gendelman HE, Persidsky Y, Kanmogne GD (2008) STAT1 signaling modulates HIV-1 induced inflammatory responses and leukocyte transmigration across the blood-brain barrier. Blood 111:2062–2072PubMedCrossRefGoogle Scholar
  11. 11.
    Cheung C, Luo H, Yanagawa B, Leong HS, Samarasekera D, Lai JCK, Suarez A, Zhang J, McManus BM (2006) Matrix metalloproteinases and tissue inhibitors of metalloproteinases in coxsackievirus-induced myocarditis. Cardiovasc Pathol 15:63–74PubMedCrossRefGoogle Scholar
  12. 12.
    Colton CA, Gilbert DL (1987) Production of superoxide anions by a CNS macrophage, the microglia. FEBS Lett 223:284–288PubMedCrossRefGoogle Scholar
  13. 13.
    Conant K, McArthur JC, Griffin DE, Sjulson L, Wahl LM, Irani DN (1999) Cerebrospinal fluid levels of MMP-2, 7, and 9 are elevated in association with human immunodeficiency virus dementia. Ann Neurol 46:391–398PubMedCrossRefGoogle Scholar
  14. 14.
    Cossins JA, Clements JM, Ford J, Miller KM, Pigott R, Vos W, Van Der Valk P, De Groot CJA (1997) Enhanced expression of MMP-7 and MMP-9 in demyelinating multiple sclerosis lesions. Acta neuropathologica 94:590–598PubMedCrossRefGoogle Scholar
  15. 15.
    Crocker SJ, Pagenstecher A, Campbell IL (2004) The TIMPs tango with MMPs and more in the central nervous system. J Neurosci Res 75:1–11PubMedCrossRefGoogle Scholar
  16. 16.
    Cunningham LA, Wetzel M, Rosenberg GA (2005) Multiple roles for MMPs and TIMPs in cerebral ischemia. Glia 50:329–339PubMedCrossRefGoogle Scholar
  17. 17.
    Dutta K, Mishra MK, Nazmi A, Kumawat KL, Basu A (2010) Minocycline differentially modulates macrophage mediated peripheral immune response following Japanese encephalitis virus infection. Immunobiology 215:884–893PubMedCrossRefGoogle Scholar
  18. 18.
    Fainardi E, Castellazzi M, Bellini T, Manfrinato MC, Baldi E, Casetta I, Paolino E, Granieri E, Dallocchio F (2006) Cerebrospinal fluid and serum levels and intrathecal production of active matrix metalloproteinase-9 (MMP-9) as markers of disease activity in patients with multiple sclerosis. Mult Scler 12:294–301PubMedCrossRefGoogle Scholar
  19. 19.
    Foerster C, Kahles T, Kietz S, Drenckhahn D (2007) Dexamethasone induces the expression of metalloproteinase inhibitor TIMP-1 in the murine cerebral vascular endothelial cell line cEND. J Physiol 580:937–949CrossRefGoogle Scholar
  20. 20.
    Gehrmann J, Matsumoto Y, Kreutzberg GW (1995) Microglia: intrinsic immuneffector cell of the brain. Brain Res Rev 20:269–287PubMedCrossRefGoogle Scholar
  21. 21.
    Gerlach RF, Tanus-Santos JE (2005) Circulating matrix metalloproteinase-9 levels as a biomarker of disease. Clin Cancer Res 11:8887–8888PubMedCrossRefGoogle Scholar
  22. 22.
    Ghoshal A, Das S, Ghosh S, Mishra MK, Sharma V, Koli P, Sen E, Basu A (2007) Proinflammatory mediators released by activated microglia induces neuronal death in Japanese encephalitis. Glia 55:483–496PubMedCrossRefGoogle Scholar
  23. 23.
    Gijbels K, Masure S, Carton H, Opdenakker G (1992) Gelatinase in the cerebrospinal fluid of patients with multiple sclerosis and other inflammatory neurological disorders. J Neuroimmunol 41:29–34PubMedCrossRefGoogle Scholar
  24. 24.
    Gijbels K, Galardy RE, Steinman L (1994) Reversal of experimental autoimmune encephalomyelitis with a hydroxamate inhibitor of matrix metalloproteases. J Clin Invest 94:2177PubMedCrossRefGoogle Scholar
  25. 25.
    Gottschall PE, Deb S (1996) Regulation of matrix metalloproteinase expression in astrocytes, microglia and neurons. Neuroimmunomodulation 3:69–75PubMedCrossRefGoogle Scholar
  26. 26.
    Harkness K, Adamson P, Sussman J, Davies-Jones G, Greenwood J, Woodroofe M (2000) Dexamethasone regulation of matrix metalloproteinase expression in CNS vascular endothelium. Brain 123:698–709PubMedCrossRefGoogle Scholar
  27. 27.
    Herron G, Banda M, Clark E, Gavrilovic J, Werb Z (1986) Secretion of metalloproteinases by stimulated capillary endothelial cells. II. Expression of collagenase and stromelysin activities is regulated by endogenous inhibitors. J Biol Chem 261:2814PubMedGoogle Scholar
  28. 28.
    Jacobson JA, Hills SL, Winkler JL, Mammen M, Thaisomboonsuk B, Marfin AA, Gibbons RV (2007) Evaluation of three immunoglobulin M antibody capture enzyme-linked immunosorbent assays for diagnosis of Japanese encephalitis. Am J Trop Med Hyg 77:164–168PubMedGoogle Scholar
  29. 29.
    Jaworski DM, Fager N (2000) Regulation of tissue inhibitor of metalloproteinase-3 (Timp-3) mRNA expression during rat CNS development. J Neurosci Res 61:396–408PubMedCrossRefGoogle Scholar
  30. 30.
    Kanoh Y, Ohara T, Kanoh M, Akahoshi T (2008) Serum matrix metalloproteinase-2 levels indicate blood–CSF barrier damage in patients with infectious meningitis. Inflammation 31:99–104PubMedCrossRefGoogle Scholar
  31. 31.
    Kettlun AM, Cartier L, García L, Collados L, Vásquez F, Ramírez E, Valenzuela MA (2003) TIMPs and MMPs expression in CSF from patients with TSP/HAM. Life Sci 72:2863–2876PubMedCrossRefGoogle Scholar
  32. 32.
    Khanna N, Agnihotri M, Mathur A, Chaturvedi UC (1991) Neutrophil chemotactic factor produced by Japanese encephalitis virus stimulated macrophages. Clin Exp Immunol 86:299–303PubMedCrossRefGoogle Scholar
  33. 33.
    Khrestchatisky M, Jourquin J, Ogier C, Charton G, Bernard A, Tremblay E, Rivera S (2003) Matrix metalloproteinases and their inhibitors, modulators of neuro-immune interactions and of pathophysiological processes in the nervous system. J Soc Biol 197:133–144PubMedGoogle Scholar
  34. 34.
    Khuth ST, Akaoka H, Pagenstecher A, Verlaeten O, Belin MF, Giraudon P, Bernard A (2001) Morbillivirus infection of the mouse central nervous system induces region-specific upregulation of MMPs and TIMPs correlated to inflammatory cytokine expression. J Virol 75:8268–8282PubMedCrossRefGoogle Scholar
  35. 35.
    Latronico T, Liuzzi GM, Riccio P, Lichtner M, Mengoni F, D’Agostino C, Vullo V, Mastroianni CM (2007) Antiretroviral therapy inhibits matrix metalloproteinase-9 from blood mononuclear cells of HIV-infected patients. Aids 21:677PubMedCrossRefGoogle Scholar
  36. 36.
    Lee KY, Kim EH, Yang WS, Ryu H, Cho SN, Lee BI, Heo JH (2004) Persistent increase of matrix metalloproteinases in cerebrospinal fluid of tuberculous meningitis. J Neurol Sci 220:73–78PubMedCrossRefGoogle Scholar
  37. 37.
    Lee MA, Palace J, Stabler G, Ford J, Gearing A, Miller K (1999) Serum gelatinase B, TIMP-1 and TIMP-2 levels in multiple sclerosis. A longitudinal clinical and MRI study. Brain 122:191–197PubMedCrossRefGoogle Scholar
  38. 38.
    Leib SL, Leppert D, Clements J, Täuber MG (2000) Matrix metalloproteinases contribute to brain damage in experimental pneumococcal meningitis. Infection Immun 68:615–620CrossRefGoogle Scholar
  39. 39.
    Leonardi A, Abbruzzese G, Arata L, Cocito L, Vische M (1984) Cerebrospinal fluid (CSF) findings in amyotrophic lateral sclerosis. J Neurol 231:75–78PubMedCrossRefGoogle Scholar
  40. 40.
    Leppert D, Hughes P, Huber S, Erne B, Grygar C, Said G, Miller K, Steck A, Probst A, Fuhr P (1999) Matrix metalloproteinase upregulation in chronic inflammatory demyelinating polyneuropathy and nonsystemic vasculitic neuropathy. Neurology 53:62–70PubMedCrossRefGoogle Scholar
  41. 41.
    Lindberg RLP, De Groot CJA, Montagne L, Freitag P, van der Valk P, Kappos L, Leppert D (2001) The expression profile of matrix metalloproteinases (MMPs) and their inhibitors (TIMPs) in lesions and normal appearing white matter of multiple sclerosis. Brain 124:1743–1753PubMedCrossRefGoogle Scholar
  42. 42.
    Lorenzl S, Albers DS, LeWitt PA, Chirichigno JW, Hilgenberg SL, Cudkowicz ME, Beal MF (2003) Tissue inhibitors of matrix metalloproteinases are elevated in cerebrospinal fluid of neurodegenerative diseases. J Neurol Sci 207:71–76PubMedCrossRefGoogle Scholar
  43. 43.
    Mandler RN, Dencoff JD, Midani F, Ford CC, Ahmed W, Rosenberg GA (2001) Matrix metalloproteinases and tissue inhibitors of metalloproteinases in cerebrospinal fluid differ in multiple sclerosis and Devic’s neuromyelitis optica. Brain 124:493–498PubMedCrossRefGoogle Scholar
  44. 44.
    Mathur A, Khanna N, Chaturvedi UC (1992) Breakdown of blood-brain barrier by virus-induced cytokine during Japanese encephalitis virus infection. International J Exp Pathol 73:603Google Scholar
  45. 45.
    Matsuura E, Umehara F, Hashiguchi T, Fujimoto N, Okada Y, Osame M (2000) Marked increase of matrix metalloproteinase 9 in cerebrospinal fluid of patients with fungal or tuberculous meningoencephalitis. J Neurol Sci 173:45–52PubMedCrossRefGoogle Scholar
  46. 46.
    Mishra MK, Dutta K, Saheb SK, Basu A (2009) Understanding the molecular mechanism of blood-brain barrier damage in an experimental model of Japanese encephalitis: correlation with minocycline administration as a therapeutic agent. Neurochem Int 55:717–723PubMedCrossRefGoogle Scholar
  47. 47.
    Moore CS, Crocker SJ (2012) An Alternate Perspective on the Roles of TIMPs and MMPs in Pathology. Am J Pathol 180(1):12–16PubMedCrossRefGoogle Scholar
  48. 48.
    Niebroj-Dobosz I, Janik P, Sokołowska B, Kwiecinski H (2010) Matrix metalloproteinases and their tissue inhibitors in serum and cerebrospinal fluid of patients with amyotrophic lateral sclerosis. Eur J Neurol 17:226–231PubMedCrossRefGoogle Scholar
  49. 49.
    Opdenakker G, Van den Steen PE, Van Damme J (2001) Gelatinase B: a tuner and amplifier of immune functions. Trends immunol 22:571–579PubMedCrossRefGoogle Scholar
  50. 50.
    Ottino P, Finley J, Rojo E, Ottlecz A, Lambrou GN, Bazan HE, Bazan NG (2004) Hypoxia activates matrix metalloproteinase expression and the VEGF system in monkey choroid-retinal endothelial cells: involvement of cytosolic phospholipase A2 activity. Mol Vis 10:341–350PubMedGoogle Scholar
  51. 51.
    Paemen L, Olsson T, Soderstrom M, Damme J, Opdenakker G (1994) Evaluation of gelatinases and IL-6 in the cerebrospinal fluid of patients with optic neuritis, multiple sclerosis and other inflammatory neurological diseases. Eur J Neurol 1:55–63CrossRefGoogle Scholar
  52. 52.
    Pagenstecher A, Stalder AK, Kincaid CL, Shapiro SD, Campbell IL (1998) Differential expression of matrix metalloproteinase and tissue inhibitor of matrix metalloproteinase genes in the mouse central nervous system in normal and inflammatory states. Am J Pathol 152:729PubMedGoogle Scholar
  53. 53.
    Paul R, Lorenzl S, Koedel U, Sporer B, Vogel U, Frosch M, Pfister HW (1998) Matrix metalloproteinases contribute to the blood—brain barrier disruption during bacterial meningitis. Ann Neurol 44:592–600PubMedCrossRefGoogle Scholar
  54. 54.
    Perry V, Anthony D, Bolton S, Brown H (1997) The blood-brain barrier and the inflammatory response. Mol Med Today 3:335–341PubMedCrossRefGoogle Scholar
  55. 55.
    Qi JH, Ebrahem Q, Moore N, Murphy G, Claesson-Welsh L, Bond M, Baker A, Anand-Apte B (2003) A novel function for tissue inhibitor of metalloproteinases-3 (TIMP3): inhibition of angiogenesis by blockage of VEGF binding to VEGF receptor-2. Nat Med 9:407–415PubMedCrossRefGoogle Scholar
  56. 56.
    Ragin AB, Wu Y, Ochs R, Scheidegger R, Cohen BA, McArthur JC, Epstein LG, Conant K (2009) Serum matrix metalloproteinase levels correlate with brain injury in human immunodeficiency virus infection. J Neurovirol 15:275–281PubMedCrossRefGoogle Scholar
  57. 57.
    Ragin AB, Wu Y, Ochs R, Du H, Epstein LG, Conant K, McArthur JC (2011) Marked relationship between matrix metalloproteinase 7 and brain atrophy in HIV infection. J Neurovirol 17:153–158PubMedCrossRefGoogle Scholar
  58. 58.
    Ravi V, Parida S, Desai A, Chandramuki A, Gourie-Devi M, Grau GE (1997) Correlation of tumor necrosis factor levels in the serum and cerebrospinal fluid with clinical outcome in Japanese encephalitis patients. J Med Virol 51:132–136PubMedCrossRefGoogle Scholar
  59. 59.
    Ravi V, Desai A, Balaji M, Apte MP, Lakshman L, Subbakrishna D, Sridharan G, Dhole T, Ravikumar B (2006) Development and evaluation of a rapid IgM capture ELISA (JEV-Chex) for the diagnosis of Japanese encephalitis. J Clin Virol 35:429–434PubMedCrossRefGoogle Scholar
  60. 60.
    Ravi V, Robinson JS, Russell BJ, Desai A, Ramamurty N, Featherstone D, Johnson BW (2009) Evaluation of IgM antibody capture enzyme-linked immunosorbent assay kits for detection of IgM against Japanese encephalitis virus in cerebrospinal fluid samples. Am J Trop Med Hyg 81:1144–1150PubMedCrossRefGoogle Scholar
  61. 61.
    Robak E, Wierzbowska A, Chmiela M, Kulczycka L, Sysa-Jedrejowska A, Robak T (2006) Circulating Total and Active Metalloproteinase-9 and Tissue Inhibitor of Metalloproteinases-1 in Patients With Systemic Lupus Erythomatosus (Research Communication). Mediat Inflamm 1:17898Google Scholar
  62. 62.
    Robinson JS, Featherstone D, Vasanthapuram R, Biggerstaff BJ, Desai A, Ramamurty N, Chowdhury AH, Sandhu HS, Cavallaro KF, Johnson BW (2010) Evaluation of three commercially available Japanese encephalitis virus IgM enzyme-linked immunosorbent assays. Am J Trop Med Hyg 83:1146–1155PubMedCrossRefGoogle Scholar
  63. 63.
    Rosenberg GA (2002) Matrix metalloproteinases in neuroinflammation. Glia 39:279–291PubMedCrossRefGoogle Scholar
  64. 64.
    Rosenberg GA (2005) Matrix metalloproteinases biomarkers in multiple sclerosis. Lancet 365:1291–1293PubMedCrossRefGoogle Scholar
  65. 65.
    Rosenberg GA, Yang Y (2007) Vasogenic edema due to tight junction disruption by matrix metalloproteinases in cerebral ischemia. Neurosurg Focus 22:1–9CrossRefGoogle Scholar
  66. 66.
    Sellner J, Simon F, Meyding-Lamade U, Leib SL (2006) Herpes-simplex virus encephalitis is characterized by an early MMP-9 increase and collagen type IV degradation. Brain Res 1125:155–162PubMedCrossRefGoogle Scholar
  67. 67.
    Seo D-W, Li H, Guedez L, Wingfield PT, Diaz T, Salloum R, Wei B-y, Stetler-Stevenson WG (2003) TIMP-2 mediated inhibition of angiogenesis: an MMP-independent mechanism. Cell 114:171–180PubMedCrossRefGoogle Scholar
  68. 68.
    Shigemori Y, Katayama Y, Mori T, Maeda T, Kawamata T (2006) Matrix metalloproteinase-9 is associated with blood-brain barrier opening and brain edema formation after cortical contusion in rats. Brain Edema XIII. Springer, Berlin, pp 130–133Google Scholar
  69. 69.
    Shima DT, Adamis AP, Ferrara N, Yeo KT, Yeo TK, Allende R, Folkman J, D’Amore PA (1995) Hypoxic induction of endothelial cell growth factors in retinal cells: identification and characterization of vascular endothelial growth factor (VEGF) as the mitogen. Mol Med 1:182PubMedGoogle Scholar
  70. 70.
    Shukla V, Kumar Shakya A, Dhole T, Misra UK (2012) Upregulated expression of matrix metalloproteinases and tissue inhibitors of matrix metalloproteinases in BALB/c mouse brain challenged with Japanese encephalitis virus. Neuroimmunomodulation 19:241–254PubMedCrossRefGoogle Scholar
  71. 71.
    Singh A, Kulshreshtha R, Mathur A (2000) Secretion of the chemokine interleukin-8 during Japanese encephalitis virus infection. J Med Microbiol 49:607–612PubMedGoogle Scholar
  72. 72.
    Sulik A, Chyczewski L (2008) Immunohistochemical analysis of MMP-9, MMP-2 and TIMP-1, TIMP-2 expression in the central nervous system following infection with viral and bacterial meningitis. Folia Histochemica et Cytobiologica 46:437–442PubMedGoogle Scholar
  73. 73.
    Swarup V, Ghosh J, Duseja R, Ghosh S, Basu A (2007) Japanese encephalitis virus infection decrease endogenous IL-10 production: correlation with microglial activation and neuronal death. Neurosci Lett 420:144–149PubMedCrossRefGoogle Scholar
  74. 74.
    Tsai HC, Chung LY, Chen ER, Liu YC, Lee SSJ, Chen YS, Sy CL, Wann SR, Yen CM (2008) Association of matrix metalloproteinase-9 and tissue inhibitors of metalloproteinase-4 in cerebrospinal fluid with blood-brain barrier dysfunction in patients with eosinophilic meningitis caused by Angiostrongylus cantonensis. Am J Trop Med Hyg 78:20–27PubMedGoogle Scholar
  75. 75.
    Tsai HC, Liu SF, Wu KS, Liu YC, Shi MH, Chen ER, Yen CM, Lee SSJ, Huang YL, Chen YS (2008) Dynamic changes of matrix metalloproteinase-9 in patients with Klebsiella pneumoniae meningitis. Inflammation 31:247–253PubMedCrossRefGoogle Scholar
  76. 76.
    Tsai HC, Shi MH, Lee SSJ, Wann SR, Tai MH, Chen YS (2011) Expression of matrix metalloproteinases and their tissue inhibitors in the serum and cerebrospinal fluid of patients with meningitis. Clin Microbiol Infection 17:780–784CrossRefGoogle Scholar
  77. 77.
    Tsai HC, Ye SY, Kunin CM, Lee SSJ, Wann SR, Tai MH, Shi MH, Liu YC, Chen YS (2011) Expression of matrix metalloproteinases and their tissue inhibitors in the serum and cerebrospinal fluid of patients with HIV-1 infection and syphilis or neurosyphilis. CytokineGoogle Scholar
  78. 78.
    Tung WH, Tsai HW, Lee I, Hsieh HL, Chen WJ, Chen YL, Yang CM (2010) Japanese encephalitis virus induces matrix metalloproteinase-9 in rat brain astrocytes via NF-κB signalling dependent on MAPKs and reactive oxygen species. Br J Pharmacol 161:1566–1583PubMedCrossRefGoogle Scholar
  79. 79.
    Vaillant C, Didier-Bazès M, Hutter A, Belin MF, Thomasset N (1999) Spatiotemporal expression patterns of metalloproteinases and their inhibitors in the postnatal developing rat cerebellum. J Neurosci 19:4994–5004PubMedGoogle Scholar
  80. 80.
    Van den Steen PE, Dubois B, Nelissen I, Rudd PM, Dwek RA, Opdenakker G (2002) Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9). Crit Rev Biochem Mol Biol 37:375–536PubMedCrossRefGoogle Scholar
  81. 81.
    Wang P, Dai J, Bai F, Kong KF, Wong SJ, Montgomery RR, Madri JA, Fikrig E (2008) Matrix metalloproteinase 9 facilitates West Nile virus entry into the brain. J Virol 82:8978–8985PubMedCrossRefGoogle Scholar
  82. 82.
    Waubant E, Goodkin D, Gee L, Bacchetti P, Sloan R, Stewart T, Andersson PB, Stabler G, Miller K (1999) Serum MMP-9 and TIMP-1 levels are related to MRI activity in relapsing multiple sclerosis. Neurology 53:1397–1401PubMedCrossRefGoogle Scholar
  83. 83.
    Yang CM, Lin CC, Lee IT, Lin YH, Chen WJ, Jou MJ, Hsiao LD (2012) Japanese encephalitis virus induces matrix metalloproteinase-9 expression via a ROS/c-Src/PDGFR/PI3K/Akt/MAPKs-dependent AP-1 pathway in rat brain astrocytes. J Neuroinflamm 9:12CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2013

Authors and Affiliations

  • Vibha Shukla
    • 1
  • Akhalesh Kumar Shakya
    • 1
  • T. N. Dhole
    • 1
  • Usha Kant Misra
    • 2
  1. 1.Department of MicrobiologySanjay Gandhi Postgraduate Institute of Medical SciencesLucknowIndia
  2. 2.Department of NeurologySanjay Gandhi Postgraduate Institute of Medical SciencesLucknowIndia

Personalised recommendations