Display options
Cite
Ullah MA, Rittchen S, Li J, et al. DP1 prostanoid receptor activation increases the severity of an acute lower respiratory viral infection in mice via TNF-α-induced immunopathology. Mucosal Immunol. 2021;14(4):963-972doi: 10.1038/s41385-021-00405-7.
Ullah, M. A., Rittchen, S., Li, J., Hasnain, S. Z., & Phipps, S. (2021). DP1 prostanoid receptor activation increases the severity of an acute lower respiratory viral infection in mice via TNF-α-induced immunopathology. Mucosal immunology, 14(4), 963-972. https://doi.org/10.1038/s41385-021-00405-7
Ullah, Md Ashik, et al. "DP1 prostanoid receptor activation increases the severity of an acute lower respiratory viral infection in mice via TNF-α-induced immunopathology." Mucosal immunology vol. 14,4 (2021): 963-972. doi: https://doi.org/10.1038/s41385-021-00405-7
Ullah MA, Rittchen S, Li J, Hasnain SZ, Phipps S. DP1 prostanoid receptor activation increases the severity of an acute lower respiratory viral infection in mice via TNF-α-induced immunopathology. Mucosal Immunol. 2021 Jul;14(4):963-972. doi: 10.1038/s41385-021-00405-7. Epub 2021 Apr 20. PMID: 33879829; PMCID: PMC8057290.
Copy Download .nbib Format: NLM
Share it on

Mucosal Immunol. 2021 Jul;14(4):963-972. doi: 10.1038/s41385-021-00405-7. Epub 2021 Apr 20.

DP1 prostanoid receptor activation increases the severity of an acute lower respiratory viral infection in mice via TNF-α-induced immunopathology.

Mucosal immunology

Md Ashik Ullah, Sonja Rittchen, Jia Li, Sumaira Z Hasnain, Simon Phipps

Affiliations

  1. Respiratory Immunology Laboratory, QIMR Berghofer Medical Research Institute, Herston, QLD, Australia.
  2. Otto Loewi Research Center for Vascular Biology, Immunology and Inflammation, Division of Pharmacology, Medical University of Graz, Graz, Austria.
  3. Department of Laboratory Medicine, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
  4. Australian Infectious Diseases Research Centre, The University of Queensland, Brisbane, QLD, Australia.
  5. Immunopathology Group, Mater Research Institute - The University of Queensland, Translational Research Institute, Brisbane, QLD, Australia.
  6. Respiratory Immunology Laboratory, QIMR Berghofer Medical Research Institute, Herston, QLD, Australia. [email protected].
  7. Australian Infectious Diseases Research Centre, The University of Queensland, Brisbane, QLD, Australia. [email protected].

PMID: 33879829 PMCID: PMC8057290 DOI: 10.1038/s41385-021-00405-7

Abstract

Respiratory syncytial virus (RSV) bronchiolitis is a leading cause of infant hospitalization and mortality. We previously identified that prostaglandin D2 (PGD2), released following RSV infection of primary human airway epithelial cells or pneumonia virus of mice (PVM) infection of neonatal mice, elicits pro- or antiviral innate immune responses as a consequence of D-type prostanoid receptor 2 (DP2) or DP1 activation, respectively. Here, we sought to determine whether treatment with the DP1 agonist BW245c decreases the severity of bronchiolitis in PVM-infected neonatal mice. Consistent with previous findings, BW245c treatment increased IFN-λ production and decreased viral load in week 1 of the infection. However, unexpectedly, BW245c treatment increased mortality in week 2 of the infection. This increased morbidity was associated with viral spread to the parenchyma, an increased cellular infiltrate of TNF-α-producing cells (neutrophils, monocytes, and CD4

References

  1. Global Burden of Disease Pediatrics Collaboration, Kyu, H. H. et al. Global and national burden of diseases and injuries among children and adolescents between 1990 and 2013: findings from the global burden of disease 2013 study. JAMA Pediatr. 170, 267–287 (2016). - PubMed
  2. Florin, T. A., Plint, A. C. & Zorc, J. J. Viral bronchiolitis. Lancet 389, 211–224 (2017). - PubMed
  3. Everard, M. L. et al. Analysis of cells obtained by bronchial lavage of infants with respiratory syncytial virus infection. Arch. Dis. Child. 71, 428–432 (1994). - PubMed
  4. Levy, O. Innate immunity of the newborn: basic mechanisms and clinical correlates. Nat. Rev. Immunol. 7, 379–390 (2007). - PubMed
  5. Holt, P. G. & Sly, P. D. Viral infections and atopy in asthma pathogenesis: new rationales for asthma prevention and treatment. Nat. Med. 18, 726–735 (2012). - PubMed
  6. Lynch, J. P. et al. The influence of the microbiome on early-life severe viral lower respiratory infections and asthma-food for thought? Front. Immunol. 8, 156 (2017). - PubMed
  7. Carroll, K. N. et al. Increasing burden and risk factors for bronchiolitis-related medical visits in infants enrolled in a state health care insurance plan. Pediatrics 122, 58–64 (2008). - PubMed
  8. Makris, S., Paulsen, M. & Johansson, C. Type I interferons as regulators of lung inflammation. Front. Immunol. 8, 259 (2017). - PubMed
  9. Johnson, J. E., Gonzales, R. A., Olson, S. J., Wright, P. F. & Graham, B. S. The histopathology of fatal untreated human respiratory syncytial virus infection. Mod. Pathol. 20, 108–119 (2007). - PubMed
  10. Pickles, R. J. & DeVincenzo, J. P. Respiratory syncytial virus (RSV) and its propensity for causing bronchiolitis. J. Pathol. 235, 266–276 (2015). - PubMed
  11. Pettipher, R., Hansel, T. T. & Armer, R. Antagonism of the prostaglandin D2 receptors DP1 and CRTH2 as an approach to treat allergic diseases. Nat. Rev. Drug Disco. 6, 313–325 (2007). - PubMed
  12. Rittchen S. & Heinemann, A. Therapeutic potential of hematopoietic prostaglandin D2 synthase in allergic inflammation. Cells 8, 619 (2019). - PubMed
  13. Hardy, C. C., Robinson, C., Tattersfield, A. E. & Holgate, S. T. The bronchoconstrictor effect of inhaled prostaglandin D2 in normal and asthmatic men. N. Engl. J. Med. 311, 209–213 (1984). - PubMed
  14. Van Ly, D. et al. Characterising the mechanism of airway smooth muscle β2 adrenoceptor desensitization by rhinovirus infected bronchial epithelial cells. PLoS ONE 8, e56058 (2013). - PubMed
  15. Hammad, H. et al. Activation of the D prostanoid 1 receptor suppresses asthma by modulation of lung dendritic cell function and induction of regulatory T cells. J. Exp. Med. 204, 357–367 (2007). - PubMed
  16. Kupczyk, M. & Kuna, P. Targeting the PGD2/CRTH2/DP1 signaling pathway in asthma and allergic disease: current status and future perspectives. Drugs 77, 1281–1294 (2017). - PubMed
  17. Jandl, K. et al. Activated prostaglandin D2 receptors on macrophages enhance neutrophil recruitment into the lung. J. Allergy Clin. Immunol. 137, 833–843 (2016). - PubMed
  18. Vijay, R. et al. Virus-induced inflammasome activation is suppressed by prostaglandin D2/DP1 signaling. Proc. Natl Acad. Sci. USA 114, E5444–e5453 (2017). - PubMed
  19. Werder, R. B. et al. PGD2/DP2 receptor activation promotes severe viral bronchiolitis by suppressing IFN-lambda production. Sci. Transl. Med. 10, eaao0052 (2018). - PubMed
  20. Lynch, J. P. et al. Aeroallergen-induced IL-33 predisposes to respiratory virus-induced asthma by dampening antiviral immunity. J. Allergy Clin. Immunol. 138, 1326–1337 (2016). - PubMed
  21. Simpson, J. et al. The absence of interferon-beta promotor stimulator-1 (IPS-1) predisposes to bronchiolitis and asthma-like pathology in response to pneumoviral infection in mice. Sci. Rep. 7, 2353 (2017). - PubMed
  22. Simpson, J. et al. Respiratory Syncytial Virus infection promotes necroptosis and HMGB1 release by airway epithelial cells. Am. J. Respir. Crit. Care Med. 201, 1358–1371 (2020). - PubMed
  23. Peters, M., Müller, A. M. & Rose-John, S. Interleukin-6 and soluble interleukin-6 receptor: direct stimulation of gp130 and hematopoiesis. Blood 92, 3495–3504 (1998). - PubMed
  24. Ullah, M. A. et al. Allergen-induced IL-6 trans-signaling activates gammadelta T cells to promote type 2 and type 17 airway inflammation. J. Allergy Clin. Immunol. 136, 1065–1073 (2015). - PubMed
  25. Heinonen, S. et al. Immune profiles provide insights into respiratory syncytial virus disease severity in young children. Sci. Transl. Med. 12, eaaw0268 (2020). - PubMed
  26. McNamara, P. S., Ritson, P., Selby, A., Hart, C. A. & Smyth, R. L. Bronchoalveolar lavage cellularity in infants with severe respiratory syncytial virus bronchiolitis. Arch. Dis. Child. 88, 922–926 (2003). - PubMed
  27. Murata, T. et al. Anti-inflammatory role of PGD2 in acute lung inflammation and therapeutic application of its signal enhancement. Proc. Natl Acad. Sci. USA 110, 5205 (2013). - PubMed
  28. Tumala, B., Phelps, K. R., Zhang, S., Bhattacharya, S. & Shornick, L. P. Prostaglandin D2 levels regulate CD103(+) conventional dendritic cell activation in neonates during respiratory viral infection. Viral Immunol. 31, 658–667 (2018). - PubMed
  29. Zhao, J., Zhao, J., Legge, K. & Perlman, S. Age-related increases in PGD(2) expression impair respiratory DC migration, resulting in diminished T cell responses upon respiratory virus infection in mice. J. Clin. Invest. 121, 4921–4930 (2011). - PubMed
  30. Angeli, V. et al. Activation of the D prostanoid receptor 1 regulates immune and skin allergic responses. J. Immunol. 172, 3822–3829 (2004). - PubMed
  31. Giamarellos-Bourboulis, E. J. et al. Complex immune dysregulation in COVID-19 patients with severe respiratory failure. Cell Host Microbe 27, 992–1000.e1003 (2020). - PubMed
  32. Zarogoulidis, P. et al. Macrolides: from in vitro anti-inflammatory and immunomodulatory properties to clinical practice in respiratory diseases. Eur. J. Clin. Pharm. 68, 479–503 (2012). - PubMed
  33. Chua, R. L. et al. COVID-19 severity correlates with airway epithelium-immune cell interactions identified by single-cell analysis. Nat. Biotechnol. 38, 970–979 (2020). - PubMed
  34. Del Valle, D. M. et al. An inflammatory cytokine signature predicts COVID-19 severity and survival. Nat. Med. 26, 1636–1643 (2020). - PubMed
  35. Mehta, P. et al. COVID-19: consider cytokine storm syndromes and immunosuppression. Lancet 395, 1033–1034 (2020). - PubMed
  36. Bohmwald, K. et al. Contribution of cytokines to tissue damage during human respiratory syncytial virus infection. Front. Immunol. 10, 452 (2019). - PubMed
  37. Medzhitov, R. Recognition of microorganisms and activation of the immune response. Nature 449, 819–826 (2007). - PubMed
  38. Gupta, A. & Chander Chiang, K. Prostaglandin D2 as a mediator of lymphopenia and a therapeutic target in COVID-19 disease. Med. Hypotheses 143, 110122 (2020). - PubMed
  39. Rizk, J. G. et al. Pharmaco-immunomodulatory therapy in COVID-19. Drugs 80, 1267–1292 (2020). - PubMed
  40. Dannappel, M. et al. RIPK1 maintains epithelial homeostasis by inhibiting apoptosis and necroptosis. Nature 513, 90–94 (2014). - PubMed
  41. Muraro, S. P. et al. Respiratory syncytial virus induces the classical ROS-dependent NETosis through PAD-4 and necroptosis pathways activation. Sci. Rep. 8, 14166 (2018). - PubMed
  42. Sebina, I. & Phipps, S. The contribution of neutrophils to the pathogenesis of RSV bronchiolitis. Viruses 12, 808 (2020). - PubMed
  43. Loh, Z. et al. HMGB1 amplifies ILC2-induced type-2 inflammation and airway smooth muscle remodelling. PLoS Pathog. 16, e1008651 (2020). - PubMed
  44. Ullah, M. A. et al. PAG1 limits allergen-induced type 2 inflammation in the murine lung. Allergy 75, 336–345 (2020). - PubMed
  45. Chong, L. et al. Protective effect of curcumin on acute airway inflammation of allergic asthma in mice through Notch1-GATA3 signaling pathway. Inflammation 37, 1476–1485 (2014). - PubMed
  46. Lynch, J. P. et al. Plasmacytoid dendritic cells protect from viral bronchiolitis and asthma through semaphorin 4a-mediated T reg expansion. J. Exp. Med. 215, 537–557 (2018). - PubMed
  47. Spann, K. M. et al. IRF-3, IRF-7, and IPS-1 promote host defense against acute human metapneumovirus infection in neonatal mice. Am. J. Pathol. 184, 1795–1806 (2014). - PubMed

Publication Types