Respiratory syncytial virus infection and G and/or SH protein expression contribute to substance P, which mediates inflammation and enhanced pulmonary disease in BALB/c mice

Journal of Virology

Volumn 74, Issue 4, 2000, Pages 1614-1622

  Tripp, Ralph A ^a,b   Moore, Deborah ^a   Winter, Jorn ^a   Anderson, Larry J ^a  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN G; RESPIRATORY SYNCYTIAL VIRUS VACCINE; SUBSTANCE P; SUBSTANCE P ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CYTOKINE PRODUCTION; EOSINOPHILIA; INFLAMMATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PATHOGENESIS; PNEUMONIA; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; VERO CELL; VIRUS INFECTION;

ANIMALS; ANTIGENS, CD3; ANTIGENS, VIRAL; BRONCHIOLITIS; BRONCHOALVEOLAR LAVAGE; CERCOPITHECUS AETHIOPS; CYTOKINES; FEMALE; HN PROTEIN; HUMANS; MICE; MICE, INBRED BALB C; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; SUBSTANCE P; T-LYMPHOCYTES; VERO CELLS; VIRAL ENVELOPE PROTEINS; VIRAL PROTEINS;

EID: 0033920379     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.4.1614-1622.2000     Document Type: Article

References (66)

1. Agro, A., and A. M. Stanisz. 1993. Inhibition of murine intestinal inflammation by anti-substance P antibody. Reg. Immunol. 5:120-126.
2. Agro, A., and A. M. Stanisz. 1995. Neuroimmunomodulation: classical and non-classical cellular activation. Adv. Neuroimmunol. 5:311-319.
3. Bai, T. R., D. Zhou, T. Weir, B. Walker, R. Hegele, S. Hayashi, K. McKay, G. P. Bondy, and T. Fong. 1995. Substance P (NK1)-and neurokinin A (NK2)-receptor gene expression in inflammatory airway diseases. Am. J. Physiol. 269:L309-L317.
4. Barnes, P. J. 1991. Neurogenic inflammation in airways. Int. Arch. Allergy Appl. Immunol. 94:303-309.
5. Bembridge, G. P., R. Garcia-Beato, J. A. Lopez, J. A. Melero, and G. Taylor. 1998. Subcellular site of expression and route of vaccination influence pulmonary eosinophilia following respiratory syncytial virus challenge in BALB/c mice sensitized to the attachment G protein. J. Immunol. 161: 2473-2480.
6. Berczi, I., I. M. Chalmers, E. Nagy, and R. J. Warrington. 1996. The immune effects of neuropeptides. Baillieres Clin. Rheumatol. 10:227-257.
7. Berman, A. S., C. Chancellor-Freeland, G. Zhu, and P. H. Black. 1996. Substance P primes murine peritoneal macrophages for an augmented proinflammatory cytokine response to lipopolysaccharide. Neuroimmunomodulation 3:141-149.
8. Boichot, E., V. Lagente, M. Paubert-Braquet, and N. Frossard. 1993. Inhaled substance P induces activation of alveolar macrophages and increases airway responses in the guinea-pig. Neuropeptides 25:307-313.
9. Bowden, J. J., P. Baluk, P. M. Lefevre, S. R. Vigna, and D. M. McDonald. 1996. Substance P (NK1) receptor immunoreactivity on endothelial cells of the rat tracheal mucosa. Am. J. Physiol. 270:L404-L414.
10. Bowden, J. J., A. M. Garland, P. Baluk, P. Lefevre, E. F. Grady, S. R. Vigna, N. W. Bunnett, and D. M. McDonald. 1994. Direct observation of substance P-induced internalization of neurokinin 1 (NK1) receptors at sites of inflammation. Proc. Natl. Acad. Sci. USA 91:8964-8968.
11. Bozic, C. R., B. Lu, U. E. Hopken, C. Gerard, and N. P. Gerard. 1996. Neurogenic amplification of immune complex inflammation. Science 273: 1722-1725.
12. Brandt, C. D., H. W. Kim, J. O. Arrobio, B. C. Jefferies, S. C. Wood, R. M. Chanock, and R. H. Parrott. 1973. Epidemiology of respiratory syncytial virus infection in Washington. D.C. III. Composite analysis of eleven consecutive yearly epidemics. Am. J. Epidemiol. 98:355-364.
13. Brunelleschi, S., D. Colangelo, G. Bordin, and I. Viano. 1998. Tachykinin receptors are present on human monocytes and play a role in rheumatoid arthritis. J. Chemother. 10:150-152.
14. Brunelleschi, S., A. Parenti, E. Ceni, A. Giotti, and R. Fantozzi. 1992. Enhanced responsivencss of ovalbumin-sensitized guinea-pig alveolar macrophages to tachykinins. Br. J. Pharm. 107:964-969.
15. Carolan, E. J., and T. B. Casale. 1993. Effects of neuropeptides on neutrophil migration through noncellular and endothelial barriers. J. Allergy Clin. Immunol. 92:589-598.
16. Cheido, M., and G. Idova. 1997. Neuropeptides in the immunomodulation: substance P-induced stimulation of immune response in mice. Int. J. Immunopharmacol. 19:529-533.
17. Choi, D. C., and O. J. Kwon. 1998. Neuropeptides and asthma. Curr. Opin. Pulm. Med. 4:16-24.
18. Connors, M., N. A. Giese, A. B. Kulkarni, C. Y. Firestone, H. C. Morse III, and B. R. Murphy. 1994. Enhanced pulmonary histopathology induced by respiratory syncytial virus (RSV) challenge of formalin-inactivated RSV-immunized BALB/c mice is abrogated by depletion of interleukin-4 (IL-4) and IL-10. J. Virol. 68:5321-5325.
19. Covas, M. J., L. A. Pinto, and R. M. Victorino. 1994. Disturbed immunoregulatory properties of the neuropeptide substance P on lymphocyte proliferation in HIV infection. Clin. Exp. Immunol. 96:384-388.
20. Dickerson, C., B. Undem, B. Bullock, and R. A. Winchurch. 1998. Neuropeptide regulation of proinflammatory cytokine responses. J. Leukoc. Biol. 63: 602-605.
21. Goetzl, E. J., M. Xia, D. A. Ingram, J. L. Kishiyama, H. B. Kaltreider, P. K. Byrd, S. Ichikawa, and S. P. Sreedharan. 1995. Neuropeptide signaling of lymphocytes in immunological responses. Int. Arch. Allergy Immunol. 107: 202-204.
22. Gordon, D. J., L. S. Ostlere, and C. A. Holden. 1997. Neuropeptide modulation of Th1 and Th2 cytokines in peripheral blood mononuclear leucocytes in atopic dermatitis and non-atopic controls. Br. J. Dermatol. 137:921-927.
23. Graham, B. S., G. S. Henderson, Y. W. Tang, X. Lu, K. M. Neuzil, and D. G. Colley. 1993. Priming immunization determines T helper cytokine mRNA expression patterns in lungs of mice challenged with respiratory syncytial virus. J. Immunol. 151:2032-2040.
24. Groothuis, J. R., E. A. Simoes, and V. G. Hemming. 1995. Respiratory syncytial virus (RSV) infection in preterm infants and the protective effects of RSV immune globulin (RSVIG). Respiratory Syncytial Virus Immune Globulin Study Group. Pediatrics 95:463-467.
25. Halliday, D. A., J. D. McNeil, and R. Scicchitano. 1993. A metabolite of substance P, SP7-11 is involved in the pathogenesis of inflammatory joint disease. Med. Hypotheses 40:227-231.
26. Henderson, F. W., W. A. Clyde, A. M. Collier, F. W. Denny, R. J. Senior, C. I. Sheaffer, W. G. Conley, and R. M. Christian. 1979. The etiologic and epidemiologic spectrum of bronchiolitis in pediatric practice. J. Pediatr. 95: 183-190.
27. Ho, W. Z., J. P. Lai, X. H. Zhu, M. Uvaydova, and S. D. Douglas. 1997. Human monocytes and macrophages express substance P and neurokinin-1 receptor. J. Immunol. 159:5654-5660.
28. Institute of Medicine. 1986. New vaccine development: establishing priorities, diseases of importance in developing countries. National Academy Press, Washington, D.C.
29. Institute of Medicine. 1985. New vaccine development: establishing priorities, diseases of importance in the United States. National Academy Press, Washington, D.C.
30. Johnson, T. R., J. E. Johnson, S. R. Roberts, G. W. Wertz, R. A. Parker, and B. S. Graham. 1998. Priming with secreted glycoprotein G of respiratory syncytial virus (RSV) augments interleukin-5 production and tissue eosinophilia after RSV challenge. J. Virol. 72:2871-2880.
31. Joos, G. F., J. C. Kips, R. A. Peleman, and R. A. Pauwels. 1995. Tachykinin antagonists and the airways. Arch. Int. Pharmacodyn. Ther. 329:205-219.
32. Kaltreider, H. B., S. Ichikawa, P. K. Byrd, D. A. Ingram, J. L. Kishiyama, S. P. Sreedharan, M. L. Warnock, J. M. Beck, and E. J. Goetzl. 1997. Upregulation of neuropeptides and neuropeptide receptors in a murine model of immune inflammation in lung parenchyma. Am. J. Respir. Cell Mol. Biol. 16:133-144.
33. Karron, R. A., D. A. Buonagurio, A. F. Georgiu, S. S. Whitehead, J. E. Adamus, M. L. Clements-Mann, D. O. Harris, V. B. Randolph, S. A. Udem, B. R. Murphy, and M. S. Sidhu. 1997. Respiratory syncytial virus (RSV) SH and G proteins are not essential for viral replication in vitro: clinical evaluation and molecular characterization of a cold-passaged, attenuated RSV subgroup B mutant. Proc. Natl. Acad. Sci. USA 94:13961-13966.
34. Killingsworth, C. R., S. A. Shore, F. Alessandrini, R. D. Dey, and J. D. Paulauskis. 1997. Rat alveolar macrophages express preprotachykinin gene-I mRNA-encoding tachykinins. Am. J. Physiol. 273:L1073-L1081.
35. Kim, H. W., J. O. Arrobio, C. D. Brandt, B. C. Jeffries, G. Pyles, J. L. Reid, R. M. Chanock, and R. H. Parrott. 1973. Epidemiology of respiratory syncytial virus infection in Washington. D.C. I. Importance of the virus in different respiratory tract syndromes and temporal distribution of infection. Am. J. Epidemiol. 98:216-225.
36. Lambert, N., P. L. Lescoulie, B. Yassine-Diab, G. Enault, B. Mazieres, C. De Preval, and A. Cantagrel. 1998. Substance P enhances cytokine-induced vascular cell adhesion molecule-1 (VCAM-1) expression on cultured rheumatoid fibroblast-like synoviocytes. Clin. Exp. Immunol. 113:269-275.
37. Lee, H. R., W. Z. Ho, and S. D. Douglas. 1994. Substance P augments tumor necrosis factor release in human monocyte-derived macrophages. Clin. Diagn. Lab. Immunol. 1:419-423.
38. Lotz, M., J. H. Vaughan, and D. A. Carson. 1988. Effect of neuropeptides on production of inflammatory cytokines by human monocytes. Science 241: 1218-1221.
39. Lucey, D. R., J. M. Novak, V. R. Polonis, Y. Liu, and S. Gartner. 1994. Characterization of substance P binding to human monocytes/macrophages. Clin. Diagn. Lab. Immunol. 1:330-335.
40. Luger, T. A., R. S. Bhardwaj, S. Grabbe, and T. Schwarz. 1996. Regulation of the immune response by epidermal cytokines and neurohormones. J. Dermatol. Sci. 13:5-10.
41. Lundberg, J. M. 1995. Tachykinins, sensory nerves, and asthma - an overview. Can. J. Physiol. Pharmacol. 73:908-914.
42. Maggi, C. A. 1997. The effects of tachykinins on inflammatory and immune cells. Regul. Pept. 70:75-90.
43. Maggi, C. A. 1995. The mammalian tachykinin receptors. Gen. Pharmacol. 26:911-944.
44. Manske, J. M., E. L. Sullivan, and S. M. Andersen. 1995. Substance P mediated stimulation of cytokine levels in cultured murine bone marrow stromal cells. Adv. Exp. Med. Biol. 383:53-64.
45. Mantyh, P. W. 1991. Substance P and the inflammatory and immune response. Ann. N. Y. Acad. Sci. 632:263-271.
46. Martinez, F. D., W. J. Morgan, A. L. Wright, A. L. Holberg, and L. M. Tausig. 1988. Diminished lung function as a predisposing factor for wheezing respiratory illness in patients. N. Engl. J. Med. 319:1112-1117.
47. McGillis, J. P., M. L. Organist, and D. G. Payan. 1987. Substance P and immunoregulation. Fed. Proc. 46:196-199.
48. Nicolai, T., and A. Pohl. 1990. Acute viral bronchiolitis in infancy: epidemiology and management. Lung 168(Suppl.):396-405.
49. Openshaw, P. J. 1995. Immunity and immunopathology to respiratory syncytial virus. The mouse model. Am. J. Respir. Crit. Care Med. 152:S59-S62.
50. Palma, C., and S. Manzini. 1998. Substance P induces secretion of immunomodulatory cytokines by human astrocytoma cells. J. Neuroimmunol. 81: 127-137.
51. Price, J. F. 1990. Acute and long-term effects of viral bronchiolitis in infancy. Lung 168(Suppl.):414-421.
52. Reynolds, P. N., M. D. Holmes, and R. Scicchitano. 1997. Role of tachykinins in bronchial hyper-responsiveness. Clin. Exp. Pharmacol. Physiol. 24:273-280.
53. Sparer, T. E., S. Matthews, T. Hussell, A. J. Rae, B. Garcia-Barreno, J. A. Melero, and P. J. Openshaw. 1998. Eliminating a region of respiratory syncytial virus attachment protein allows induction of protective immunity without vaccine-enhanced lung eosinophilia. J. Exp. Med. 187:1921-1926.
54. Srikiatkhachorn, A., and T. J. Braciale. 1997. Virus-specific CD8+ T lymphocytes downregulate T helper cell type 2 cytokine secretion and pulmonary eosinophilia during experimental murine respiratory syncytial virus infection. J. Exp. Med. 186:421-432.
55. Srikiatkhachorn, A., W. Chang, and T. J. Braciale. 1999. Induction of Th1-and Th2-responses by respiratory syncytial virus attachment glycoprotein is epitope and major histocompatibility complex independent. J. Virol. 73: 6590-6597.
56. Stokes Peebles, R., J. R. Sheller, J. E. Johnson, D. B. Mitchell, and B. S. Graham. 1999. Respiratory syncytial virus infection prolongs methacholine-induced airway hyperresponsiveness in ovalbumin-sensitized mice. J. Med. Virol. 57:186-192.
57. Tanabe, T., H. Otani, K. Mishima, R. Ogawa, and C. Inagaki. 1996. Mechanisms of oxyradical production in substance P stimulated rheumatoid synovial cells. Rheumatol. Int. 16:159-167.
58. Tebbey, P. W., M. Hagem, and G. E. Hancock. 1998. Atypical pulmonary eosinophilia is mediated by a specific amino acid sequence of the attachment (G) protein of respiratory syncytial virus. J. Exp. Med. 188:1967-1972.
59. Tomaki, M., M. Ichinose, M. Miura, Y. Hirayama, H. Yamauchi, N. Nakajima, and K. Shirato. 1995. Elevated substance P content in induced sputum from patients with asthma and patients with chronic bronchitis. Am. J. Respir. Crit. Care Med. 151:613-617.
60. Tripp, R. A., and L. J. Anderson. 1998. Cytotoxic T-lymphocyte precursor frequencies in BALB/c mice after acute respiratory syncytial virus (RSV) infection or immunization with a formalin-inactivated RSV vaccine. J. Virol. 72:8971-8975.
61. Tripp, R. A., D. Moore, L. Jones, W. Sullender, J. Winter, and L. J. Anderson. 1999. Respiratory syncytial virus (RSV) G and/or SH proteins alter Th1 cytokines, natural killer cells and neutrophils responding to pulmonary infection in BALB/c mice. J. Virol. 73:7099-7107.
62. Waris, M. E., C. Tsou, D. D. Erdman, S. R. Zaki, and L. J. Anderson. 1996. Respiratory syncytial virus infection in BALB/c mice previously immunized with formalin-inactivated virus induces enhanced pulmonary inflammatory response with a predominant Th2-like cytokine pattern. J. Virol. 70:2852-2860.
63. Weinstock, J. V., and D. Elliott. 1998. The substance P and somatostatin interferon-gamma immunoregulatory circuit. Ann. N. Y. Acad. Sci. 840: 532-539.
64. Welliver, R. C. 1995. RSV and chronic asthma. Lancet 346:789-790.
65. Welliver, R. C., and L. Duffy. 1993. The relationship of RSV-specific immunoglobulin E antibody responses in infancy, recurrent wheezing, and pulmonary function at age 7-8 years. Pediatr. Pulmonol. 15:19-27.
66. Welliver, R. C., M. R. Gallagher, and P. L. Ogra. 1981. Clinical and laboratory diagnosis of respiratory syncytial virus infection. Crit. Rev. Clin. Lab. Sci. 13:213-239.