1887

Abstract

Upregulation of matrix metalloproteinase (MMP)−14, a major driven force of extracellular-matrix (ECM) remodelling and cell migration, correlates with ECM breakdown and pathologic manifestation of genotype VII Newcastle disease virus (NDV) in chickens. However, the functional relevance between MMP-14 and pathogenesis of genotype VII NDV remains to be investigated. In this study, expression, biofunction and regulation of MMP-14 induced by genotype VII NDV were analysed in chicken peripheral blood mononuclear cells (PBMCs). The results showed that JS5/05 significantly increased expression and membrane accumulation of MMP-14 in PBMCs, correlating to enhanced collagen degradation and cell migration. Specific MMP-14 inhibition significantly impaired collagen degradation and migration of JS5/05-infected cells, suggesting dependence of these features on MMP-14. In addition, MMP-14 upregulation correlated with activation of the extracellular signal-regulated kinase (ERK) pathway upon JS5/05 infection, and blockage of the ERK signalling significantly suppressed MMP-14-mediated collagen degradation and migration of JS5/05-infected cells. Using a panel of chimeric NDVs derived from gene exchange between genotype VII and IV NDV, the fusion and haemagglutinin-neuraminidase genes were identified as the major viral determinants for MMP-14 expression and activity. In conclusion, MMP-14 was defined as a critical regulator of collagen degradation and cell migration of chicken PBMCs infected with genotype VII NDV, which may contribute to pathology of the virus. Our findings add novel information to the body of knowledge regarding virus–host biology and NDV pathogenesis.

Funding
This study was supported by the:
  • Priority Academic Program Development of Jiangsu Higher Education Institutions (Award PAPD)
    • Principle Award Recipient: Xiufan Liu
  • Earmarked Fund for China Agriculture Research System (Award CARS-40)
    • Principle Award Recipient: Xiufan Liu
  • Young Scientists Fund (Award 31702243)
    • Principle Award Recipient: Zenglei Hu
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001505
2020-10-22
2024-05-10
Loading full text...

Full text loading...

/deliver/fulltext/jgv/102/1/vir001505.html?itemId=/content/journal/jgv/10.1099/jgv.0.001505&mimeType=html&fmt=ahah

References

  1. Miller PJ, Decanini EL, Afonso CL. Newcastle disease: evolution of genotypes and the related diagnostic challenges. Infect Genet Evol 2010; 10:26–35 [View Article] [PubMed]
    [Google Scholar]
  2. Hu Z, Hu J, Hu S, Song Q, Ding P et al. High levels of virus replication and an intense inflammatory response contribute to the severe pathology in lymphoid tissues caused by Newcastle disease virus genotype VIId. Arch Virol 2015; 160:639–648 [View Article] [PubMed]
    [Google Scholar]
  3. Susta L, Miller PJ, Afonso CL, Brown CC. Clinicopathological characterization in poultry of three strains of Newcastle disease virus isolated from recent outbreaks. Vet Pathol 2011; 48:349–360 [View Article] [PubMed]
    [Google Scholar]
  4. Wang Y, Duan Z, Hu S, Kai Y, Wang X et al. Lack of detection of host associated differences in Newcastle disease viruses of genotype VIId isolated from chickens and geese. Virol J 2012; 9:197 [View Article] [PubMed]
    [Google Scholar]
  5. Ecco R, Brown C, Susta L, Cagle C, Cornax I et al. In vivo transcriptional cytokine responses and association with clinical and pathological outcomes in chickens infected with different Newcastle disease virus isolates using formalin-fixed paraffin-embedded samples. Vet Immunol Immunopathol 2011; 141:221–229 [View Article] [PubMed]
    [Google Scholar]
  6. Hu Z, Gu H, Hu J, Hu S, Wang X et al. Quantitative proteomics identify an association between extracellular matrix degradation and immunopathology of genotype VII Newcastle disease virus in the spleen in chickens. J Proteomics 2018; 181:201–212 [View Article] [PubMed]
    [Google Scholar]
  7. Marchesin V, Castro-Castro A, Lodillinsky C, Castagnino A, Cyrta J et al. ARF6-JIP3/4 regulate endosomal tubules for MT1-MMP exocytosis in cancer invasion. J Cell Biol 2015; 211:339–358 [View Article] [PubMed]
    [Google Scholar]
  8. Wiesner C, Faix J, Himmel M, Bentzien F, Linder S. KIF5B and KIF3A/KIF3B kinesins drive MT1-MMP surface exposure, CD44 shedding, and extracellular matrix degradation in primary macrophages. Blood 2010; 116:1559–1569 [View Article] [PubMed]
    [Google Scholar]
  9. Ayala-Nunez NV, Follain G, Delalande F, Hirschler A, Partiot E et al. Zika virus enhances monocyte adhesion and transmigration favoring viral dissemination to neural cells. Nat Commun 2019; 10:4430 [View Article] [PubMed]
    [Google Scholar]
  10. Sathyamoorthy T, Tezera LB, Walker NF, Brilha S, Saraiva L et al. Membrane type 1 matrix metalloproteinase regulates monocyte migration and collagen destruction in tuberculosis. J Immunol 2015; 195:882–891 [View Article] [PubMed]
    [Google Scholar]
  11. Reddy VRAP, Trus I, Desmarets LMB, Li Y, Theuns S et al. Productive replication of nephropathogenic infectious bronchitis virus in peripheral blood monocytic cells, a strategy for viral dissemination and kidney infection in chickens. Vet Res 2016; 47:70 [View Article] [PubMed]
    [Google Scholar]
  12. Niranjan R, Sumitha MK, Sankari T, Muthukumaravel S, Jambulingam P. Nonstructural protein-1 (NS1) of dengue virus type-2 differentially stimulate expressions of matrix metalloproteinases in monocytes: protective effect of paracetamol. Int Immunopharmacol 2019; 73:270–279 [View Article] [PubMed]
    [Google Scholar]
  13. Al Shammari B, Shiomi T, Tezera L, Bielecka MK, Workman V et al. The extracellular matrix regulates granuloma necrosis in tuberculosis. J Infect Dis 2015; 212:463–473 [View Article] [PubMed]
    [Google Scholar]
  14. Shields MA, Dangi-Garimella S, Krantz SB, Bentrem DJ, Munshi HG. Pancreatic cancer cells respond to type I collagen by inducing snail expression to promote membrane type 1 matrix metalloproteinase-dependent collagen invasion. J Biol Chem 2011; 286:10495–10504 [View Article] [PubMed]
    [Google Scholar]
  15. Hu Z, Hu S, Meng C, Wang X, Zhu J et al. Generation of a genotype VII Newcastle disease virus vaccine candidate with high yield in embryonated chicken eggs. Avian Dis 2011; 55:391–397 [View Article] [PubMed]
    [Google Scholar]
  16. Hu S, Ma H, Wu Y, Liu W, Wang X et al. A vaccine candidate of attenuated genotype VII Newcastle disease virus generated by reverse genetics. Vaccine 2009; 27:904–910 [View Article] [PubMed]
    [Google Scholar]
  17. Kai Y, Hu Z, Xu H, Hu S, Zhu J et al. The M, F and HN genes of genotype VIId Newcastle disease virus are associated with the severe pathological changes in the spleen of chickens. Virol J 2015; 12:133 [View Article] [PubMed]
    [Google Scholar]
  18. Justus CR, Leffler N, Ruiz-Echevarria M, Yang LV. In vitro cell migration and invasion assays. J Vis Exp 2014 [Epub ahead of print 01 Jun 2014] [View Article] [PubMed]
    [Google Scholar]
  19. Deng X, Cong Y, Yin R, Yang G, Ding C et al. Proteomic analysis of chicken peripheral blood mononuclear cells after infection by Newcastle disease virus. J Vet Sci 2014; 15:511–517 [View Article] [PubMed]
    [Google Scholar]
  20. Liu W-Q, Tian M-X, Wang Y-P, Zhao Y, Zou N-L et al. The different expression of immune-related cytokine genes in response to velogenic and lentogenic Newcastle disease viruses infection in chicken peripheral blood. Mol Biol Rep 2012; 39:3611–3618 [View Article] [PubMed]
    [Google Scholar]
  21. Itoh Y. Membrane-Type matrix metalloproteinases: their functions and regulations. Matrix Biol 2015; 44-46:207–223 [View Article] [PubMed]
    [Google Scholar]
  22. Cepeda MA, Pelling JJH, Evered CL, Williams KC, Freedman Z et al. Less is more: low expression of MT1-MMP is optimal to promote migration and tumourigenesis of breast cancer cells. Mol Cancer 2016; 15:65 [View Article] [PubMed]
    [Google Scholar]
  23. Meisel JE, Chang M. Selective small-molecule inhibitors as chemical tools to define the roles of matrix metalloproteinases in disease. Bba-Mol Cell Res 2017; 1864:2001–2014 [View Article]
    [Google Scholar]
  24. Remacle AG, Golubkov VS, Shiryaev SA, Dahl R, Stebbins JL et al. Novel MT1-MMP small-molecule inhibitors based on insights into hemopexin domain function in tumor growth. Cancer Res 2012; 72:2339–2349 [View Article] [PubMed]
    [Google Scholar]
  25. Udi Y, Grossman M, Solomonov I, Dym O, Rozenberg H et al. Inhibition mechanism of membrane metalloprotease by an exosite-swiveling conformational antibody. Structure 2015; 23:104–115 [View Article] [PubMed]
    [Google Scholar]
  26. Talmi-Frank D, Altboum Z, Solomonov I, Udi Y, Jaitin DA et al. Extracellular matrix proteolysis by MT1-MMP contributes to influenza-related tissue damage and mortality. Cell Host Microbe 2016; 20:458–470 [View Article] [PubMed]
    [Google Scholar]
  27. Castro-Castro A, Marchesin V, Monteiro P, Lodillinsky C, Rossé C et al. Cellular and molecular mechanisms of MT1-MMP-dependent cancer cell invasion. Annu Rev Cell Dev Biol 2016; 32:555–576 [View Article] [PubMed]
    [Google Scholar]
  28. Planchon D, Rios Morris E, Genest M, Comunale F, Vacher S et al. Mt1-Mmp targeting to endolysosomes is mediated by upregulation of flotillins. J Cell Sci 2018; 131:jcs218925 [View Article] [PubMed]
    [Google Scholar]
  29. Röhl J, West ZE, Rudolph M, Zaharia A, Van Lonkhuyzen D et al. Invasion by activated macrophages requires delivery of nascent membrane-type-1 matrix metalloproteinase through late endosomes/lysosomes to the cell surface. Traffic 2019; 20:661–673 [View Article] [PubMed]
    [Google Scholar]
  30. Linder S, Wiesner C. Tools of the trade: podosomes as multipurpose organelles of monocytic cells. Cell Mol Life Sci 2015; 72:121–135 [View Article] [PubMed]
    [Google Scholar]
  31. Zhao Y, Zhang ZY. The mechanism of dephosphorylation of extracellular signal-regulated kinase 2 by mitogen-activated protein kinase phosphatase 3. J Biol Chem 2001; 276:32382–32391 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001505
Loading
/content/journal/jgv/10.1099/jgv.0.001505
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error