Matrix metalloproteinase-9 mediates RSV infection in vitro and in vivo

Viruses

Volumn 7, Issue 8, 2015, Pages 4230-4253

  Kong, Michele Y F ^a   Whitley, Richard J ^a   Peng, Ning ^a   Oster, Robert ^b   Schoeb, Trenton R ^a   Sullender, Wayne ^c   Ambalavanan, Namasivayam ^a   Clancy, John Paul ^d   Gaggar, Amit ^b   Blalock, J Edwin ^b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

^c Global Health and Health Disparities   (United States)

^d CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Cell; Matrix metalloproteinase; Murine model; Respiratory syncytial virus

Indexed keywords

GELATINASE B; SMALL INTERFERING RNA; TISSUE INHIBITOR OF METALLOPROTEINASE;

AIRWAY RESISTANCE; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE SILENCING; HISTOLOGY; HUMAN; HUMAN CELL; LUNG FUNCTION TEST; MOUSE; NONHUMAN; PNEUMONIA; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN SECRETION; RESPIRATORY SYNCYTIAL VIRUS INFECTION; VIRUS LOAD; VIRUS REPLICATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL CULTURE; EPITHELIUM CELL; GENETICS; HOST PATHOGEN INTERACTION; HUMAN RESPIRATORY SYNCYTIAL VIRUS; KNOCKOUT MOUSE; LUNG; METABOLISM; PATHOLOGY; PHYSIOLOGY; VIROLOGY;

MURINAE; MUS; RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

ANIMALS; CELLS, CULTURED; EPITHELIAL CELLS; GENE SILENCING; HOST-PATHOGEN INTERACTIONS; HUMANS; LUNG; MATRIX METALLOPROTEINASE 9; MICE, INBRED C57BL; MICE, KNOCKOUT; RESPIRATORY SYNCYTIAL VIRUSES; RNA, SMALL INTERFERING; VIRAL LOAD;

EID: 84938303975     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7082817     Document Type: Article

References (55)

1. Blanken, M.O.; Rovers, M.M.; Molenaar, J.M.; Winkler-Seinstra, P.L.; Meijer, A.; Kimpen, J.L.; Bont, L. Dutch RSV Neonatal Network. Respiratory syncytial virus and recurrent wheeze in healthy preterm infants. N. Engl. J. Med. 2013, 368, 1791-1799. [CrossRef] [PubMed]
2. Stretton, M.; Ajizian, S.J.; Mitchell, I.; Newth, C.J. Intensive care course and outcome of patients infected with respiratory syncytial virus. Pediatr. Pulmonol. 1992,13,143-150. [CrossRef][PubMed]
3. Buckingham, S.C.; Quasney, M.W.; Bush, A.J.; DeVincenzo, J.P. Respiratory syncytial virus infection in the pediatric intensive care unit: Clinical characteristics and risk factors for adverse outcomes. Pediatr. Crit. Care Med. 2001, 2, 318-323. [CrossRef] [PubMed]
4. Nair, H.; Nokes, D.J.; Gessner, B.D.; Dherani, M.; Madhi, S.A.; Singleton, R.J.; O’Brien, K.L.; Roca, A.; Wright, P.F.; Bruce, N., et al. Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: A systematic review and meta-analysis. Lancet 2010, 375,1545-1555. [CrossRef]
5. Purcell, K.; Fergie, J. Driscoll Children’s Hospital respiratory syncytial virus database: Risk factors, treatment and hospital course in 3308 infants and young children, 1991 to 2002. Pediatr. Infect. Dis. J. 2004, 23, 418-423. [CrossRef] [PubMed]
6. Yuksel, B.; Greenough, A. Birthweight and hospital readmission in infants born prematurely. Arch. Pediatr. Adolesc. Med. 1994, 148, 384-388. [CrossRef] [PubMed]
7. Hall, C.B.; Weinberg, G.A.; Iwane, M.K.; Blumkin, A.K.; Edwards, K.M.; Staat, M.A.; Auinger, P.; Griffin, M.R.; Poehling, K.A.; Erdman, D., et al. The burden of respiratory syncytial virus infection in young children. N. Engl. J. Med. 2009, 360, 588-598. [CrossRef] [PubMed]
8. Stevens, T.P.; Sinkin, R.A.; Hall, C.B.; Maniscalco, W.M.; McConnochie, K.M. Respiratory syncytial virus and premature infants born at 32 weeks’ gestation or earlier: Hospitalization and economic implications of prophylaxis. Arch. Pediatr. Adolesc. Med. 2000, 154, 55-61. [PubMed]
9. McCormick, J.; Tubman, R. Readmission with respiratory syncytial virus (RSV) infection among graduates from a neonatal intensive care unit. Pediatr. Pulmonol. 2002, 34, 262-266. [CrossRef] [PubMed]
10. Vogel, A.M.; Lennon, D.R.; Broadbent, R.; Byrnes, C.A.; Grimwood, K.; Mildenhall, L.; Richardson, V.; Rowley, S. Palivizumab prophylaxis of respiratory syncytial virus infection in high-risk infants. J. Paediatr. Child Health 2002, 38, 550-554. [CrossRef] [PubMed]
11. Johnson, S.; Oliver, C.; Prince, G.A.; Hemming, V.G.; Pfarr, D.S.; Wang, S.C.; Dormitzer, M.; O’Grady, J.; Koenig, S.; Tamura, J.K., et al. Development of a humanized monoclonal antibody [MEDI-493] with potent in vitro and in vivo activity against Respiratory Syncytial Virus. J. Infect. Dis. 1997, 176, 1215-1224. [CrossRef] [PubMed]
12. Prais, D.; Danino, D.; Schonfeld, T.; Amir, J. Impact of palivizumab on admission to the ICU for respiratory syncytial virus bronchiolitis: A national survey. Chest 2005, 128, 2765-2771. [CrossRef] [PubMed]
13. Homaira, N.; Rawlinson, W.; Snelling, T.L.; Jaffe, A. Effectiveness of Palivizumab in Preventing RSV Hospitalization in High Risk Children: A Real-World Perspective. Int. J. Pediatr. 2014, 2014, 571609. [CrossRef] [PubMed]
14. Smith, D.W.; Frankel, L.R.; Mathers, L.H.; Tang, A.T.; Ariagno, R.L.; Prober, C.G. A Controlled Trial of Aerosolized Ribavirin in Infants Receiving Mechanical Ventilation for Severe Respiratory Syncytial Virus Infection. N. Engl. J. Med. 1991, 325, 24-29. [CrossRef] [PubMed]
15. Krilov, L.R. Safety issues related to the administration of ribavirin. Pediatr. Infect. Dis. J. 2002, 21,479-481. [CrossRef] [PubMed]
16. Devereux, G.; Steele, S.; Jagelman, T.; Fielding, S.; Muirhead, R.; Brady, J.; Grierson, C.; Brooker, R.; Winter, J.; Fardon, T., et al. An observational study of matrix metalloproteinase (MMP)-9 in cystic fibrosis. J. Cyst. Fibros. 2014, 13, 557-563. [CrossRef] [PubMed]
17. Ma, H.P.; Li, W.; Liu, X.M. Matrix metalloproteinase 9 is involved in airway inflammation in cough variant asthma. Exp. Ther. Med. 2014, 8, 1197-1200. [CrossRef] [PubMed]
18. Kong, M.; Gaggar, A.; Li, Y.; Winkler, M.; Blalock, J.E.; Clancy, J.P. Matrix metalloproteinase activity in pediatric acute lung injury. Int. J. Med. Sci. 2009, 6, 9-17. [CrossRef] [PubMed]
19. Kong, M.; Clancy, J.P.; Peng, N.; Li, Y.; Szul, T.J.; Xu, X.; Oster, R.; Sullender, W.; Ambalavanan, N.; Blalock, J.E., et al. Pulmonary matrix metalloproteinase-9 activity in mechanically ventilated children with respiratory syncytial virus. Eur. Respir. J. 2014, 43, 1086-1096. [CrossRef] [PubMed]
20. American Academy of Pediatrics Subcommittee on Diagnosis and Management of Bronchiolitis. Diagnosis and management of bronchiolitis. Pediatrics 2006, 118, 1774-1793.
21. American Academy of Pediatrics Committee on Infectious Diseases; American Academy of Pediatrics Bronchiolitis Guidelines Committee. Updated guidance for palivizumab prophylaxis among infants and young children at increased risk of hospitalization for respiratory syncytial virus infection. Pediatrics 2014, 134, e620-e638.
22. Ventre, K.; Randolph, A.G. Ribavirin for respiratory syncytial virus infection of the lower respiratory tract in infants and young children. Cochrane Database Syst. Rev. 2007, 1, CD000181. [PubMed]
23. DeVincenzo, J.P.; Whitley, R.J.; Mackman, R.L.; Scaglioni-Weinlich, C.; Harrison, L.; Farrell, E.; McBride, S.; Lambkin-Williams, R.; Jordan, R.; Xin, Y., et al. Oral GS-5806 activity in a respiratory syncytial virus challenge study. N. Engl. J. Med. 2014,371,711-722. [CrossRef] [PubMed]
24. Cataldo, D.D.; Bettiol, J.; Noël, A.; Bartsch, P.; Foidart, J.M.; Louis, R. Matrix metalloproteinase-9, but not tissue inhibitor of matrix metalloproteinase-1, increases in the sputum from allergic asthmatic patients after allergen challenge. Chest 2002, 122, 1553-1559. [CrossRef] [PubMed]
25. Culpitt, S.V.; Rogers, D.F.; Traves, S.L.; Barnes, P.J.; Donnelly, L.E. Sputum matrix metalloproteinases: Comparison between chronic obstructive pulmonary disease and asthma. Respir. Med. 2005, 99, 703-710. [CrossRef] [PubMed]
26. Cederqvist, K.; Sorsa, T.; Tervahartiala, T.; Maisi, P.; Reunanen, K.; Lassus, P.; Andersson, S. Matrix metalloproteinases-2, -8, and -9 and TIMP-2 in tracheal aspirates from preterm infants with respiratory distress. Pediatrics 2001, 108, 686-692. [CrossRef] [PubMed]
27. Gaggar, A.; Li, Y.; Weathington, N.; Kong, M.; Jackson, P.; Blalock, J.E.; Clancy, J.P. Matrix metalloprotease-9 dysregulation in lower airway secretions of cystic fibrosis patients. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007, 293, 96-104. [CrossRef] [PubMed]
28. Zheng, T.; Zhu, Z.; Wang, Z.; Homer, R.J.; Ma, B.; Riese, R.J.; Chapman, H.A., Jr.; Shapiro, S.D.; Elias, J.A. Inducible targeting of IL-13 to the adult lung causes matrix metalloproteinase- and cathepsin-dependent emphysema. J. Clin. Investig. 2000, 106, 1081-1093. [CrossRef] [PubMed]
29. Jung, Y.W.; Zindl, C.L.; Lai, J.F.; Weaver, C.T.; Chaplin, D.D. MMP induced by Gr-1+ cells are crucial for recruitment of Th cells into the airways. Eur. J. Immunol. 2009,39,2281-2292.[CrossRef] [PubMed]
30. Malik, M.; Bakshi, C.S.; McCabe, K.; Catlett, S.V.; Shah, A.; Singh, R.; Jackson, P.L.; Gaggar, A.; Metzger, D.W.; Melendez, J.A., et al. Matrix metalloproteinase 9 activity enhances host susceptibility to pulmonary infection with type A and B strains of Francisella tularensis. J. Immunol. 2007, 178, 1013-1020. [CrossRef] [PubMed]
31. Churg, A.; Wang, R.; Wang, X.; Onnervik, P.O.; Thim, K.; Wright, J.L. Effect of an MMP-9/MMP-12 inhibitor on smoke-induced emphysema and airway remodelling in guinea pigs. Thorax 2007, 62, 706-713. [CrossRef] [PubMed]
32. Kim, J.H.; Suk, M.H.; Yoon, D.W.; Lee, S.H.; Hur, G.Y.; Jung, K.H.; Jeong, H.C.; Lee, S.Y.; Lee, S.Y.; Suh, I.B., et al. Inhibition of matrix metalloproteinase-9 prevents neutrophilic inflammation in ventilator-induced lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 2006, 291, L580-L587. [CrossRef] [PubMed]
33. Sochor, M.; Richter, S.; Schmidt, A.; Hempel, S.; Hopt, U.T.; Keck, T. Inhibition of matrix metalloproteinase-9 with doxycycline reduces pancreatitis-associated lung injury. Digestion 2009, 80,65-73. [CrossRef] [PubMed]
34. Cataldo, D.D.; Tournoy, K.G.; Vermaelen, K.; Munaut, C.; Foidart, J.M.; Louis, R.; Noël, A.; Pauwels, R.A. Matrix metalloproteinase-9 deficiency impairs cellular infiltration and bronchial hyperresponsiveness during allergen-induced airway inflammation. Am. J. Pathol. 2002,161, 491-498. [CrossRef]
35. Warner, R.L.; Beltran, L.; Younkin, E.M.; Lewis, C.S.; Weiss, S.J.; Varani, J.; Johnson, K.J. Role of stromelysin 1 and gelatinase B in experimental acute lung injury. Am. J. Respir. Cell Mol. Biol. 2001,24,537-544. [CrossRef] [PubMed]
36. Fernández, F.G.; Campbell, L.G.; Liu, W.; Shipley, J.M.; Itohara, S.; Patterson, G.A.; Senior, R.M.; Mohanakumar, T.; Jaramillo, A. Inhibition of obliterative airway disease development in murine tracheal allografts by matrix metalloproteinase-9 deficiency. Am. J. Transplant. 2005, 5, 671-683. [CrossRef] [PubMed]
37. Stark, J.M.; McDowell, S.A.; Koenigsknecht, V.; Prows, D.R.; Leikauf, J.E.; le Vine, A.M.; Leikauf, G.D. Genetic susceptibility to respiratory syncytial virus infection in inbred mice. J. Med. Virol. 2002, 67, 92-100. [CrossRef] [PubMed]
38. Jafri, H.S.; Chavez-Bueno, S.; Mejias, A.; Gomez, A.M.; Rios, A.M.; Nassi, S.S.; Yusuf, M.; Kapur, P.; Hardy, R.D.; Hatfield, J., et al. Respiratory syncytial virus induces pneumonia, cytokine response, airway obstruction, and chronic inflammatory infiltrates associated with long-term airway hyperresponsiveness in mice. J. Infect. Dis. 2004, 189, 1856-1865. [CrossRef] [PubMed]
39. Chávez-Bueno, S.; Mejías, A.; Gómez, A.M.; Olsen, K.D.; Ríos, A.M.; Fonseca-Aten, M.; Ramilo, O.; Jafri, H.S. Respiratory syncytial virus-induced acute and chronic airway disease is independent of genetic background: An experimental murine model. Virol. J. 2005, 2, e46. [CrossRef] [PubMed]
40. Horsfall, F.L.J.; Hahn, R.G. A latent virus in normal mice capable of producing pneumonia in its natural host. J. Exp. Med. 1940, 71, 391-408. [CrossRef] [PubMed]
41. Domachowske, J.B.; Bonville, C.A.; Dyer, K.D.; Easton, A.J.; Rosenberg, H.F. Pulmonary eosinophilia and production of MIP-1alpha are prominent responses to infection with pneumonia virus of mice. Cell. Immunol. 2000, 200, 98-104. [CrossRef] [PubMed]
42. Domachowske, J.B.; Bonville, C.A.; Easton, A.J.; Rosenberg, H.F. Differential expression of proiflammatory cytokine genes in vivo in response to pathogenic and nonpathogenic pneumovirus infections. J. Infect. Dis. 2002, 186, 8-14. [CrossRef] [PubMed]
43. Lukacs, N.W.; Moore, M.L.; Rudd, B.D.; Berlin, A.A.; Collins, R.D.; Olson, S.J.; Ho, S.B.; Peebles, R.S. Differential immune responses and pulmonary pathophysiology are induced by two different strains of respiratory syncytial virus. Am. J. Pathol. 2006, 169, 977-986. [CrossRef] [PubMed]
44. Moore, M.L.; Chi, M.H.; Luongo, C.; Lukacs, N.W.; Polosukhin, V.V.; Huckabee, M.M.; Newcomb, D.C.; Buchholz, U.J.; Crowe, J.E., Jr.; Goleniewska, K., et al. A chimeric A2 strain of respiratory syncytial virus (RSV) with the fusion protein of RSV strain line 19 exhibits enhanced viral load, mucus, and airway dysfunction. J. Virol. 2009, 83, 4185-4194. [CrossRef] [PubMed]
45. Dey, N.; Liu, T.; Garofalo, R.P.; Casola, A. TAK1 regulates NF-KB and AP-1 activation in airway epithelial cells following RSV infection. Virology 2011, 418, 93-101. [CrossRef] [PubMed]
46. Benbow, U.; Brinckerhoff, C.E. The AP-1 site and MMP gene regulation: What is all the fuss about? Matrix Biol. 1997, 15, 519-526. [CrossRef]
47. Cozens, A.L.; Yezzi, M.J.; Kunzelmann, K.; Ohrui, T.; Chin, L.; Eng, K.; Finkbeiner, W.E.; Widdicombe, J.H.; Gruenert, D.C. CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 1994,10,38-47. [CrossRef] [PubMed]
48. Mbiguino, A.; Menezes, J. Purification of human respiratory syncytial virus: Superiority of sucrose gradient over percoll, renografin, and metrizamide gradients. J. Virol. Methods 1991, 31, 161-170. [CrossRef]
49. Sullender, W.M.; Anderson, K.; Wertz, G.W. The respiratory syncytial virus subgroup B attachment glycoprotein: Analysis of sequence, expression from a recombinant vector, and evaluation as an immunogen against homologous and heterologous subgroup virus challenge. Virology 1990, 178, 195-203. [CrossRef]
50. Jaovisidha, P.; Peeples, M.E.; Brees, A.A.; Carpenter, L.R.; Moy, J.N. Respiratory syncytial virus stimulates neutrophil degranulation and chemokine release. J. Immunol. 1999, 163, 2816-2820. [PubMed]
51. Grumbach, Y.; Quynh, N.V.; Chiron, R.; Urbach, V. LXA4 stimulates ZO-1 expression and transepithelial electrical resistance in human airway epithelial (16HBE14o-) cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009, 296, L101-L108. [CrossRef] [PubMed]
52. LeSimple, P.; Liao, J.; Robert, R.; Gruenert, D.C.; Hanrahan, J.W. Cystic fibrosis transmembrane conductance regulator trafficking modulates the barrier function of airway epithelial cell monolayers. J. Physiol. 2010, 588, 1195-1209. [CrossRef] [PubMed]
53. Ambalavanan, N.; Nicola, T.; Li, P.; Bulger, A.; Murphy-Ullrich, J.; Oparil, S.; Chen, Y.F. Role of matrix metalloproteinase-2 in newborn mouse lungs under hypoxic conditions. Pediatr. Res. 2008, 63,26-32. [CrossRef] [PubMed]
54. Davis, I.C.; Sullender, W.M.; Hickman-Davis, J.M.; Lindsey, J.R.; Matalon, S. Nucleotide-mediated inhibition of alveolar fluid clearance in BALB/c mice after respiratory syncytial virus infection. Am. J. Physiol. Lung Cell. Mol. Physiol. 2004,286,112-120.[CrossRef] [PubMed]
55. Nicola, T.; Hagood, J.S.; James, M.L.; Macewen, M.W.; Williams, T.A.; Hewitt, M.M.; Schwiebert, L.; Bulger, A.; Oparil, S.; Chen, Y.F., et al. Loss of Thy-1 inhibits alveolar development in the newborn mouse lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009, 296, L738-L750. [CrossRef] [PubMed]