Skip to main content

Advertisement

Log in

Sendai virus infection up-regulates trypsin I and matrix metalloproteinase-9, triggering viral multiplication and matrix degradation in rat lungs and lung L2 cells

  • Brief Report
  • Published:
Archives of Virology Aims and scope Submit manuscript

Summary.

To elucidate the virus-host cell interaction, we analyzed quantitatively the expression of various cellular proteases and tumor necrosis factor-α (TNF-α) after Sendai virus infection in rat lungs and lung L2 cells. After infection, TNF-α mRNA levels increased rapidly to a peak on day one, and then trypsin I and matrix metalloproteinase (MMP)-9, but not MMP-2, were significantly up-regulated with a peak on day 2 in vivo. These up-regulations were confirmed in L2 cells. Up-regulation of proMMP-9 and its active convertase trypsin I seems to synergistically enhance virus multiplication and the destruction of lung matrix, resulting in the progression of pneumonia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

References

  • TS Ahuja A Gopalani P Davies H Ahuja (2003) ArticleTitleMatrix metalloproteinase-9 expression in renal biopsies of patients with HIV-associated nephropathy Nephron Clin Pract 95 c100–c104 Occurrence Handle14646370 Occurrence Handle1:CAS:528:DC%2BD3sXpsVKrtbo%3D Occurrence Handle10.1159/000074323

    Article  PubMed  CAS  Google Scholar 

  • T Carne G Scheele (1982) ArticleTitleAmino acid sequences of transport peptides associated with canine exocrine pancreatic proteins J Biol Chem 257 4133–4140 Occurrence Handle6175639 Occurrence Handle1:CAS:528:DyaL38XktF2kurY%3D

    PubMed  CAS  Google Scholar 

  • Y Chen M Shiota M Ohuchi T Towatari J Tashiro M Murakami M Yano B Yang H Kido (2000) ArticleTitleMast cell tryptase from pig lungs triggers infection by pneumotropic Sendai and influenza A viruses. Purification and characterization Eur J Biochem 267 3189–3197 Occurrence Handle10824103 Occurrence Handle1:CAS:528:DC%2BD3cXjvFymtrg%3D Occurrence Handle10.1046/j.1432-1327.2000.01346.x

    Article  PubMed  CAS  Google Scholar 

  • TW Chung SK Moon YC Lee JG Kim JH Ko CH Kim (2002) ArticleTitleEnhanced expression of matrix metalloproteinase-9 by hepatitis B virus infection in liver cells Arch Biochem Biophys 408 147–154 Occurrence Handle12464265 Occurrence Handle1:CAS:528:DC%2BD38XpsF2lu78%3D Occurrence Handle10.1016/S0003-9861(02)00522-2

    Article  PubMed  CAS  Google Scholar 

  • TW Chung YC Lee CH Kim (2004) ArticleTitleHepatitis B viral HBx induces matrix metalloproteinase-9 gene expression through activation of ERK and PI-3K/AKT pathways: involvement of invasive potential FASEB J 18 1123–1125 Occurrence Handle15132991 Occurrence Handle1:CAS:528:DC%2BD2cXpslGrsrw%3D Occurrence Handle10.1096/fj.04-2126com

    Article  PubMed  CAS  Google Scholar 

  • P Cui S Sharmin Y Okumura H Yamada M Yano D Mizuno H Kido (2004) ArticleTitleEndothelin-1 peptides and IL-5 synergistically increase the expression of IL23 in eosinophils Biochem Biophys Res Commun 315 782–787 Occurrence Handle14985080 Occurrence Handle1:CAS:528:DC%2BD2cXhsFWmsLY%3D Occurrence Handle10.1016/j.bbrc.2004.01.168

    Article  PubMed  CAS  Google Scholar 

  • FJ Descamps E Martens F Ballaux K Geboes G Opdenakker (2004) ArticleTitleIn vivo activation of gelatinase B/MMP-9 by trypsin in acute pancreatitis is a permissive factor in streptozotocin-induced diabetes J Pathol 204 555–561 Occurrence Handle15538738 Occurrence Handle1:CAS:528:DC%2BD2MXhsVymsA%3D%3D Occurrence Handle10.1002/path.1669

    Article  PubMed  CAS  Google Scholar 

  • A Devillers-Thiery T Kindt G Scheele G Blobel (1975) ArticleTitleHomology in amino-terminal sequence of precursors to pancreatic secretory proteins Proc Natl Acad Sci USA 72 5016–5020 Occurrence Handle1061088 Occurrence Handle1:CAS:528:DyaE28XlsFGguw%3D%3D Occurrence Handle10.1073/pnas.72.12.5016

    Article  PubMed  CAS  Google Scholar 

  • ME Duncan JP Richardson GI Murray WT Melvin JE Fothergill (1998) ArticleTitleHuman matrix metalloproteinase-9: activation by limited trypsin treatment and generation of monoclonal antibodies specific for the activated form Eur J Biochem 258 37–43 Occurrence Handle9851689 Occurrence Handle1:CAS:528:DyaK1cXnsFCns7o%3D Occurrence Handle10.1046/j.1432-1327.1998.2580037.x

    Article  PubMed  CAS  Google Scholar 

  • B Gotoh T Ogasawara T Toyoda NM Inocencio M Hamaguchi Y Nagai (1990) ArticleTitleAn endoprotease homologous to the blood clotting factor X as a determinant of viral tropism in chick embryo EMBO J 9 4189–4195 Occurrence Handle2174359 Occurrence Handle1:CAS:528:DyaK3MXnslCmuw%3D%3D

    PubMed  CAS  Google Scholar 

  • N Ishida M Homma (1978) ArticleTitleSendai virus Adv Virus Res 23 349–383 Occurrence Handle219669 Occurrence Handle1:STN:280:CSaC283is10%3D Occurrence Handle10.1016/S0065-3527(08)60103-7

    Article  PubMed  CAS  Google Scholar 

  • H Kido Y Yokogoshi K Sakai M Tashiro Y Kishino A Fukutomi N Katunuma (1992) ArticleTitleIsolation and characterization of a novel trypsin-like protease found in rat bronchiolar epithelial Clara cells. A possible activator of the viral fusion glycoprotein J Biol Chem 267 13573–13579 Occurrence Handle1618859 Occurrence Handle1:CAS:528:DyaK38Xls1Kgsb8%3D

    PubMed  CAS  Google Scholar 

  • H Kido M Murakami K Oba Y Chen T Towatari (1999) ArticleTitleCellular proteinases trigger the infectivity of the influenza A and Sendai viruses Mol Cell 9 235–244 Occurrence Handle1:CAS:528:DyaK1MXksVKiu7c%3D

    CAS  Google Scholar 

  • HD Klenk R Rott (1988) ArticleTitleThe molecular biology of influenza virus pathogenicity Adv Virus Res 34 247–281 Occurrence Handle3046255 Occurrence Handle1:CAS:528:DyaL1cXlvVKrsbc%3D

    PubMed  CAS  Google Scholar 

  • HD Klenk W Garten (1994) ArticleTitleHost cell proteases controlling virus pathogenicity Trends Microbiol 2 39–43 Occurrence Handle8162439 Occurrence Handle1:STN:280:ByuB3MvpvFE%3D Occurrence Handle10.1016/0966-842X(94)90123-6

    Article  PubMed  CAS  Google Scholar 

  • N Koshikawa Y Nagashima Y Miyagi H Mizushima S Yanoma H Yasumitsu K Miyazaki (1997) ArticleTitleExpression of trypsin in vascular endothelial cells FEBS Lett 409 442–448 Occurrence Handle9224706 Occurrence Handle1:CAS:528:DyaK2sXjslKls7s%3D Occurrence Handle10.1016/S0014-5793(97)00565-6

    Article  PubMed  CAS  Google Scholar 

  • N Koshikawa S Hasegawa Y Nagashima K Mitsuhashi Y Tsubota S Miyata Y Miyagi H Yasumitsu K Miyazaki (1998) ArticleTitleExpression of trypsin by epithelial cells of various tissues, leukocytes, and neurons in human and mouse Am J Pathol 253 937–944

    Google Scholar 

  • S Maroux J Baratti P Desnuelle (1971) ArticleTitlePurification and specificity of porcine enterokinase J Biol Chem 246 5031–5039 Occurrence Handle5570436 Occurrence Handle1:CAS:528:DyaE3MXltVGguro%3D

    PubMed  CAS  Google Scholar 

  • M Murakami T Towatari M Ohuchi M Shiota M Akao Y Okumura MA Parry H Kido (2001) ArticleTitleMini-plasmin found in the epithelial cells of bronchioles triggers infection by broad-spectrum influenza A viruses and Sendai virus Eur J Biochem 268 2847–2855 Occurrence Handle11358500 Occurrence Handle1:CAS:528:DC%2BD3MXktVSkt78%3D Occurrence Handle10.1046/j.1432-1327.2001.02166.x

    Article  PubMed  CAS  Google Scholar 

  • CM O’Connor MX FitzGerald (1994) ArticleTitleMatrix metalloproteases and lung disease Thorax 49 602–609 Occurrence Handle8016800 Occurrence Handle1:STN:280:ByuB1cjjsFA%3D Occurrence Handle10.1136/thx.49.6.602

    Article  PubMed  CAS  Google Scholar 

  • M Ohuchi M Homma (1976) ArticleTitleTrypsin action on the growth of Sendai virus in tissue culture cells. IV. Evidence for activation of Sendai virus by cleavage of a glycoprotein J Virol 28 1147–1150

    Google Scholar 

  • CA Partridge JJ Jeffrey AB Malik (1993) ArticleTitleA 96-kDa gelatinase induced by TNF-alpha contributes to increased microvascular endothelial permeability Am J Physiol 265 L438–L447 Occurrence Handle8238531 Occurrence Handle1:CAS:528:DyaK2cXlt1ektQ%3D%3D

    PubMed  CAS  Google Scholar 

  • C Ries H Kolb PE Petrides (1994) ArticleTitleRegulation of 92-kD gelatinase release in HL-60 leukemia cells: tumor necrosis factor-alpha as an autocrine stimulus for basal- and phorbol ester-induced secretion Blood 83 3638–3646 Occurrence Handle8204888 Occurrence Handle1:CAS:528:DyaK2cXltVGnt7g%3D

    PubMed  CAS  Google Scholar 

  • HS Rosario SW Waldo SA Becker GW Schmid-Schonbein (2004) ArticleTitlePancreatic trypsin increases matrix metalloproteinase-9 accumulation and activation during acute intestinal ischemia-reperfusion in the rat Am J Pathol 264 1707–1716

    Google Scholar 

  • H Sato M Seiki (1993) ArticleTitleRegulatory mechanism of 92 kDa type IV collagenase gene expression which is associated with invasiveness of tumor cells Oncogene 8 395–405 Occurrence Handle8426746 Occurrence Handle1:CAS:528:DyaK3sXhtF2rur4%3D

    PubMed  CAS  Google Scholar 

  • M Sato S Yoshida K Iida T Tomozawa H Kido M Yamashita (2003) ArticleTitleA novel influenza A virus activating enzyme from porcine lung: purification and characterization Biol Chem 384 219–227 Occurrence Handle12675514 Occurrence Handle1:CAS:528:DC%2BD3sXjt12rsro%3D Occurrence Handle10.1515/BC.2003.024

    Article  PubMed  CAS  Google Scholar 

  • T Sato A Ito Y Ogata H Nagase Y Mori (1996) ArticleTitleTumor necrosis factor alpha (TNFalpha) induces pro-matrix metalloproteinase 9 production in human uterine cervical fibroblasts but interleukin 1alpha antagonizes the inductive effect of TNFalpha FEBS Lett 392 175–178 Occurrence Handle8772198 Occurrence Handle1:CAS:528:DyaK28Xlt1Kitr8%3D Occurrence Handle10.1016/0014-5793(96)00808-3

    Article  PubMed  CAS  Google Scholar 

  • A Scheid PW Choppin (1974) ArticleTitleIdentification of biological activities of paramyxovirus glycoproteins. Activation of cell fusion, hemolysis, and infectivity of proteolytic cleavage of an inactive precursor protein of Sendai virus Virology 57 475–490 Occurrence Handle4361457 Occurrence Handle1:CAS:528:DyaE2cXhtlShsL0%3D Occurrence Handle10.1016/0042-6822(74)90187-1

    Article  PubMed  CAS  Google Scholar 

  • C Stratowa WJ Rutter (1986) ArticleTitleSelective regulation of trypsin gene expression by calcium and by glucose starvation in a rat exocrine pancreas cell line Proc Natl Acad Sci USA 83 4292–4296 Occurrence Handle3086879 Occurrence Handle1:CAS:528:DyaL28Xkslels7g%3D Occurrence Handle10.1073/pnas.83.12.4292

    Article  PubMed  CAS  Google Scholar 

  • M Tashiro E Pritzer MA Khoshnan M Yamakawa K Kuroda HD Klenk R Rott JT Seto (1988) ArticleTitleCharacterization of a pantropic variant of Sendai virus derived from a host range mutant Virology 165 577–583 Occurrence Handle2841801 Occurrence Handle1:CAS:528:DyaL1cXlsVKhs7s%3D Occurrence Handle10.1016/0042-6822(88)90601-0

    Article  PubMed  CAS  Google Scholar 

  • M Tashiro Y Yokogoshi K Tobita JT Seto R Rott H Kido (1992) ArticleTitleTryptase Clara, an activating protease for Sendai virus in rat lungs, is involved in pneumopathogenicity J Virol 66 7211–7216 Occurrence Handle1331518 Occurrence Handle1:CAS:528:DyaK3sXitVajug%3D%3D

    PubMed  CAS  Google Scholar 

  • T Towatari M Ide K Ohba Y Chiba M Murakami M Shiota M Kawachi H Yamada H Kido (2002) ArticleTitleIdentification of ectopic anionic trypsin I in rat lungs potentiating pneumotropic virus infectivity and increased enzyme level after virus infection Eur J Biochem 269 2613–2621 Occurrence Handle12027901 Occurrence Handle1:CAS:528:DC%2BD38XksVWrs7c%3D Occurrence Handle10.1046/j.1432-1033.2002.02937.x

    Article  PubMed  CAS  Google Scholar 

  • DA Tyrrell CR Coid (1970) ArticleTitleSendai virus infection of rats as a convenient model of acute respiratory infection Vet Rec 86 164–165 Occurrence Handle4313635 Occurrence Handle1:STN:280:CS%2BC38bgtFY%3D

    PubMed  CAS  Google Scholar 

  • SJ Yeo SJ Kim JH Kim HJ Lee YH Kook (1999) ArticleTitleInfluenza A virus infection modulates the expression of type IV collagenase in epithelial cells Arch Virol 244 1361–1370 Occurrence Handle10.1007/s007050050592

    Article  Google Scholar 

  • SJ Yeo YJ Yun MA Lyu SY Woo ER Woo SJ Kim HJ Lee HK Park YH Kook (2002) ArticleTitleRespiratory syncytial virus infection induces matrix metalloproteinase-9 expression in epithelial cells Arch Virol 247 229–242 Occurrence Handle10.1007/s705-002-8316-1

    Article  Google Scholar 

  • S Zidovec R Mazuran (1999) ArticleTitleSendai virus induces various cytokines in human peripheral blood leukocytes: different susceptibility of cytokine molecules to low pH Cytokine 11 140–143 Occurrence Handle10089135 Occurrence Handle1:CAS:528:DyaK1MXhvFCltL8%3D Occurrence Handle10.1006/cyto.1998.0411

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yamada, H., Le, Q., Kousaka, A. et al. Sendai virus infection up-regulates trypsin I and matrix metalloproteinase-9, triggering viral multiplication and matrix degradation in rat lungs and lung L2 cells. Arch Virol 151, 2529–2537 (2006). https://doi.org/10.1007/s00705-006-0807-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-006-0807-y

Keywords

Navigation