Control of IFN-I responses by the aminopeptidase IRAP in neonatal C57BL/6 alveolar macrophages during RSV infection.


Journal

Mucosal immunology
ISSN: 1935-3456
Titre abrégé: Mucosal Immunol
Pays: United States
ID NLM: 101299742

Informations de publication

Date de publication:
07 2021
Historique:
received: 31 07 2020
accepted: 22 03 2021
revised: 03 03 2021
pubmed: 14 4 2021
medline: 28 12 2021
entrez: 13 4 2021
Statut: ppublish

Résumé

Respiratory Syncytial Virus (RSV) is the major cause of lower respiratory tract infection in infants, in whom, the sensing of RSV by innate immune receptors and its regulation are still poorly described. However, the severe bronchiolitis following RSV infection in neonates has been associated with a defect in type I interferons (IFN-I) production, a cytokine produced mainly by alveolar macrophages (AMs) upon RSV infection in adults. In the present study, neonatal C57BL/6 AMs mobilized very weakly the IFN-I pathway upon RSV infection in vitro and failed to restrain virus replication. However, IFN-I productions by neonatal AMs were substantially increased by the deletion of Insulin-Responsive AminoPeptidase (IRAP), a protein previously involved in the regulation of IFN-I production by dendritic cells. Moreover, neonatal IRAP

Identifiants

pubmed: 33846534
doi: 10.1038/s41385-021-00402-w
pii: S1933-0219(22)00192-1
pmc: PMC8221999
doi:

Substances chimiques

Interferon Type I 0
Toll-Like Receptors 0
Cystinyl Aminopeptidase EC 3.4.11.3
leucyl-cystinyl aminopeptidase EC 3.4.11.3

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

949-962

Références

Smyth, R. L. & Openshaw, P. J. Bronchiolitis. Lancet 368, 312–322 (2006).
pubmed: 16860701
Janssen, R. et al. Genetic susceptibility to respiratory syncytial virus bronchiolitis is predominantly associated with innate immune genes. J. Infect. Dis. 196, 826–834 (2007).
pubmed: 17703412
Lambert, L., Sagfors, A. M., Openshaw, P. J. & Culley, F. J. Immunity to RSV in early-life. Front Immunol. 5, 466 (2014).
pubmed: 25324843 pmcid: 4179512
Cormier, S. A., You, D. & Honnegowda, S. The use of a neonatal mouse model to study respiratory syncytial virus infections. Expert Rev. Anti Infect. Ther. 8, 1371–1380 (2010).
pubmed: 21133663 pmcid: 3033119
de Kleer, I. M. et al. Perinatal activation of the interleukin-33 pathway promotes Type 2 immunity in the developing lung. Immunity 45, 1285–1298 (2016).
pubmed: 27939673
Saluzzo, S. et al. First-breath-induced Type 2 pathways shape the lung immune environment. Cell Rep. 18, 1893–1905 (2017).
pubmed: 28228256 pmcid: 5329122
Drajac, C., Laubreton, D., Riffault, S. & Descamps, D. Pulmonary susceptibility of neonates to respiratory syncytial virus infection: a problem of innate immunity? J. Immunol. Res. 2017, 8734504 (2017).
pubmed: 29250560 pmcid: 5700507
Culley, F. J., Pollott, J. & Openshaw, P. J. Age at first viral infection determines the pattern of T cell-mediated disease during reinfection in adulthood. J. Exp. Med. 196, 1381–1386 (2002).
pubmed: 12438429 pmcid: 2193991
Remot, A. et al. Flt3 ligand improves the innate response to respiratory syncytial virus and limits lung disease upon RSV reexposure in neonate mice. Eur. J. Immunol. 46, 874–884 (2016).
pubmed: 26681580
Ruckwardt, T. J., Malloy, A. M., Morabito, K. M. & Graham, B. S. Quantitative and qualitative deficits in neonatal lung-migratory dendritic cells impact the generation of the CD8
pubmed: 24550729 pmcid: 3923758
Stephens, L. M. & Varga, S. M. Function and modulation of type I interferons during respiratory syncytial virus infection. Vaccines 8 (2020).
Hall, C. B., Douglas, R. G. Jr., Simons, R. L. & Geiman, J. M. Interferon production in children with respiratory syncytial, influenza, and parainfluenza virus infections. J. Pediatr. 93, 28–32 (1978).
pubmed: 206677
Cormier, S. A. et al. Limited type I interferons and plasmacytoid dendritic cells during neonatal respiratory syncytial virus infection permit immunopathogenesis upon reinfection. J. Virol. 88, 9350–9360 (2014).
pubmed: 24920801 pmcid: 4136292
Hijano, D. R. et al. Role of Type I Interferon (IFN) in the respiratory syncytial virus (RSV) immune response and disease severity. Front Immunol. 10, 566 (2019).
pubmed: 30972063 pmcid: 6443902
Makris, S., Paulsen, M., Johansson, C. & Type, I. Interferons as regulators of lung inflammation. Front Immunol. 8, 259 (2017).
pubmed: 28344581 pmcid: 5344902
Goritzka, M. et al. Alpha/beta interferon receptor signaling amplifies early proinflammatory cytokine production in the lung during respiratory syncytial virus infection. J. Virol. 88, 6128–6136 (2014).
pubmed: 24648449 pmcid: 4093897
Zeng, R., Cui, Y., Hai, Y. & Liu, Y. Pattern recognition receptors for respiratory syncytial virus infection and design of vaccines. Virus Res. 167, 138–145 (2012).
pubmed: 22698878
Miyake, K. et al. Mechanisms controlling nucleic acid-sensing Toll-like receptors. Int. Immunol. 30, 43–51 (2018).
pubmed: 29452403
Saitoh, S. I. et al. TLR7 mediated viral recognition results in focal type I interferon secretion by dendritic cells. Nat. Commun. 8, 1592 (2017).
pubmed: 29150602 pmcid: 5693993
Liu, Y., Olagnier, D. & Lin, R. Host and viral modulation of RIG-I-mediated antiviral immunity. Front Immunol. 7, 662 (2016).
pubmed: 28096803
Ohman, T., Rintahaka, J., Kalkkinen, N., Matikainen, S. & Nyman, T. A. Actin and RIG-I/MAVS signaling components translocate to mitochondria upon influenza A virus infection of human primary macrophages. J. Immunol. 182, 5682–5692 (2009).
pubmed: 19380815
Saveanu, L. et al. IRAP identifies an endosomal compartment required for MHC class I cross-presentation. Science 325, 213–217 (2009).
pubmed: 19498108
Babdor, J. et al. IRAP+ endosomes restrict TLR9 activation and signaling. Nat. Immunol. 18, 509–518 (2017).
pubmed: 28319098
Goritzka, M. et al. Alveolar macrophage-derived type I interferons orchestrate innate immunity to RSV through recruitment of antiviral monocytes. J. Exp. Med. 212, 699–714 (2015).
pubmed: 25897172 pmcid: 4419339
Laubreton, D. et al. Regulatory B lymphocytes colonize the respiratory tract of neonatal mice and modulate immune responses of alveolar macrophages to RSV Infection in IL-10-dependant manner. Viruses 12, 822 (2020).
Nikolaou, A. et al. Presence and regulation of insulin-regulated aminopeptidase in mouse macrophages. J. Renin Angiotensin Aldosterone Syst. 15, 466–479 (2014).
pubmed: 24532823
Makris, S., Bajorek, M., Culley, F. J., Goritzka, M. & Johansson, C. Alveolar macrophages can control respiratory syncytial virus infection in the absence of Type I interferons. J. Innate Immun. 8, 452–463 (2016).
pubmed: 27423203 pmcid: 5322584
Prince, G. A., Horswood, R. L., Berndt, J., Suffin, S. C. & Chanock, R. M. Respiratory syncytial virus infection in inbred mice. Infect. Immun. 26, 764–766 (1979).
pubmed: 546793 pmcid: 414679
Chavez-Bueno, S. et al. Respiratory syncytial virus-induced acute and chronic airway disease is independent of genetic background: an experimental murine model. Virol. J. 2, 46 (2005).
pubmed: 15916706 pmcid: 1183251
Rameix-Welti, M. A. et al. Visualizing the replication of respiratory syncytial virus in cells and in living mice. Nat. Commun. 5, 5104 (2014).
pubmed: 25277263
Ravi, L. I. et al. A systems-based approach to analyse the host response in murine lung macrophages challenged with respiratory syncytial virus. BMC Genom. 14, 190 (2013).
Schneider, W. M., Chevillotte, M. D. & Rice, C. M. Interferon-stimulated genes: a complex web of host defenses. Annu Rev. Immunol. 32, 513–545 (2014).
pubmed: 24555472 pmcid: 4313732
Howes, A. et al. Differential production of Type I IFN determines the reciprocal levels of IL-10 and proinflammatory cytokines produced by C57BL/6 and BALB/c macrophages. J. Immunol. 197, 2838–2853 (2016).
pubmed: 27549173 pmcid: 5026030
Kenney, A. D. et al. Human genetic determinants of viral diseases. Annu Rev. Genet 51, 241–263 (2017).
pubmed: 28853921 pmcid: 6038703
Malinczak, C. A., Lukacs, N. W. & Fonseca, W. Early-life respiratory syncytial virus infection, trained immunity and subsequent pulmonary diseases. Viruses 12 (2020).
Aksoy, E. et al. Interferon regulatory factor 3-dependent responses to lipopolysaccharide are selectively blunted in cord blood cells. Blood 109, 2887–2893 (2007).
pubmed: 17138826
Danis, B. et al. Interferon regulatory factor 7-mediated responses are defective in cord blood plasmacytoid dendritic cells. Eur. J. Immunol. 38, 507–517 (2008).
pubmed: 18200500
Collins, P. L. & Melero, J. A. Progress in understanding and controlling respiratory syncytial virus: still crazy after all these years. Virus Res. 162, 80–99 (2011).
pubmed: 21963675 pmcid: 3221877
Sedeyn, K., Schepens, B. & Saelens, X. Respiratory syncytial virus nonstructural proteins 1 and 2: exceptional disrupters of innate immune responses. PLoS Pathog. 15, e1007984 (2019).
pubmed: 31622448 pmcid: 6797084
Hillyer, P. et al. Respiratory syncytial virus infection induces a subset of types I and III interferons in human dendritic cells. Virology 504, 63–72 (2017).
pubmed: 28157546
Ling, Z., Tran, K. C. & Teng, M. N. Human respiratory syncytial virus nonstructural protein NS2 antagonizes the activation of beta interferon transcription by interacting with RIG-I. J. Virol. 83, 3734–3742 (2009).
pubmed: 19193793 pmcid: 2663251
Spann, K. M., Tran, K. C. & Collins, P. L. Effects of nonstructural proteins NS1 and NS2 of human respiratory syncytial virus on interferon regulatory factor 3, NF-kappaB, and proinflammatory cytokines. J. Virol. 79, 5353–5362 (2005).
pubmed: 15827150 pmcid: 1082743
Spann, K. M., Tran, K. C., Chi, B., Rabin, R. L. & Collins, P. L. Suppression of the induction of alpha, beta, and lambda interferons by the NS1 and NS2 proteins of human respiratory syncytial virus in human epithelial cells and macrophages [corrected]. J. Virol. 78, 4363–4369 (2004).
pubmed: 15047850 pmcid: 374276
Quicke, K. M., Diamond, M. S. & Suthar, M. S. Negative regulators of the RIG-I-like receptor signaling pathway. Eur. J. Immunol. 47, 615–628 (2017).
pubmed: 28295214 pmcid: 5554756
Si-Tahar, M. et al. Protective role of LGP2 in influenza virus pathogenesis. J. Infect. Dis. 210, 214–223 (2014).
pubmed: 24493823
Evnouchidou, I. et al. IRAP-dependent endosomal T cell receptor signalling is essential for T cell responses. Nat. Commun. 11, 2779 (2020).
pubmed: 32487999 pmcid: 7265453
Weimershaus, M. et al. Conventional dendritic cells require IRAP-Rab14 endosomes for efficient cross-presentation. J. Immunol. 188, 1840–1846 (2012).
pubmed: 22238454
Liegeois, M., Legrand, C., Desmet, C. J., Marichal, T. & Bureau, F. The interstitial macrophage: A long-neglected piece in the puzzle of lung immunity. Cell Immunol. 330, 91–96 (2018).
pubmed: 29458975
Rincheval, V. et al. Functional organization of cytoplasmic inclusion bodies in cells infected by respiratory syncytial virus. Nat. Commun. 8, 563 (2017).
pubmed: 28916773 pmcid: 5601476
Morris, S. et al. Autophagy-mediated dendritic cell activation is essential for innate cytokine production and APC function with respiratory syncytial virus responses. J. Immunol. 187, 3953–3961 (2011).
pubmed: 21911604
Reed, M. et al. Autophagy-inducing protein beclin-1 in dendritic cells regulates CD4 T cell responses and disease severity during respiratory syncytial virus infection. J. Immunol. 191, 2526–2537 (2013).
pubmed: 23894198
Reed, M., Morris, S. H., Owczarczyk, A. B. & Lukacs, N. W. Deficiency of autophagy protein Map1-LC3b mediates IL-17-dependent lung pathology during respiratory viral infection via ER stress-associated IL-1. Mucosal Immunol. 8, 1118–1130 (2015).
pubmed: 25669150 pmcid: 4532659
Pokharel, S. M., Shil, N. K. & Bose, S. Autophagy, TGF-beta, and SMAD-2/3 signaling regulates interferon-beta response in respiratory syncytial virus infected macrophages. Front. Cell. Infect. Microbiol. 6, 174 (2016).
pubmed: 28018859 pmcid: 5149518
Kuma, A. et al. The role of autophagy during the early neonatal starvation period. Nature 432, 1032–1036 (2004).
pubmed: 15525940
Stranks, A. J. et al. Autophagy controls acquisition of aging features in macrophages. J. Innate Immun. 7, 375–391 (2015).
pubmed: 25764971 pmcid: 4386145
Hirata, Y. et al. Vimentin binds IRAP and is involved in GLUT4 vesicle trafficking. Biochem. Biophys. Res. Commun. 405, 96–101 (2011).
pubmed: 21216232
Tojo, H. et al. The Formin family protein, formin homolog overexpressed in spleen, interacts with the insulin-responsive aminopeptidase and profilin IIa. Mol. Endocrinol. 17, 1216–1229 (2003).
pubmed: 12677009
Brock, S. C., Goldenring, J. R. & Crowe, J. E. Jr. Apical recycling systems regulate directional budding of respiratory syncytial virus from polarized epithelial cells. Proc. Natl Acad. Sci. U.S.A. 100, 15143–15148 (2003).
pubmed: 14630951 pmcid: 299925
Larance, M. et al. Characterization of the role of the Rab GTPase-activating protein AS160 in insulin-regulated GLUT4 trafficking. J. Biol. Chem. 280, 37803–37813 (2005).
pubmed: 16154996
Szatmari, Z. & Sass, M. The autophagic roles of Rab small GTPases and their upstream regulators: a review. Autophagy 10, 1154–1166 (2014).
pubmed: 24915298 pmcid: 4203544
Utley, T. J. et al. Respiratory syncytial virus uses a Vps4-independent budding mechanism controlled by Rab11-FIP2. Proc. Natl Acad. Sci. U.S.A. 105, 10209–10214 (2008).
pubmed: 18621683 pmcid: 2481327

Auteurs

Carole Drajac (C)

INRAE, UVSQ, VIM, Université Paris-Saclay, Jouy-en-Josas, France.

Daphné Laubreton (D)

INRAE, UVSQ, VIM, Université Paris-Saclay, Jouy-en-Josas, France.

Quentin Marquant (Q)

INRAE, UVSQ, VIM, Université Paris-Saclay, Jouy-en-Josas, France.

Claire Chottin (C)

INRAE, UVSQ, VIM, Université Paris-Saclay, Jouy-en-Josas, France.

Cécile Ferret (C)

INRAE, UVSQ, VIM, Université Paris-Saclay, Jouy-en-Josas, France.

Edwige Bouguyon (E)

INRAE, UVSQ, VIM, Université Paris-Saclay, Jouy-en-Josas, France.

Isabelle Schwartz-Cornil (I)

INRAE, UVSQ, VIM, Université Paris-Saclay, Jouy-en-Josas, France.

Loredana Saveanu (L)

Institut National de la Santé et de la Recherche Médicale, Unité UMR 1149, Centre de Recherche sur l'Inflammation, Paris, France.
Faculté de Médecine Xavier Bichat, Université Paris Diderot, Paris, France.

Sabine Riffault (S)

INRAE, UVSQ, VIM, Université Paris-Saclay, Jouy-en-Josas, France.

Delphyne Descamps (D)

INRAE, UVSQ, VIM, Université Paris-Saclay, Jouy-en-Josas, France. delphyne.descamps@inrae.fr.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH