Olfactory Immunology: the Missing Piece in Airway and CNS Defence

Overview

Journal Nat Rev Immunol

Specialty Allergy & Immunology

Date 2023 Dec 14

PMID 38097777

Authors

Sebastian A Wellford

E Ashley Moseman

Affiliations

Soon will be listed here.

Abstract

The olfactory mucosa is a component of the nasal airway that mediates the sense of smell. Recent studies point to an important role for the olfactory mucosa as a barrier to both respiratory pathogens and to neuroinvasive pathogens that hijack the olfactory nerve and invade the CNS. In particular, the COVID-19 pandemic has demonstrated that the olfactory mucosa is an integral part of a heterogeneous nasal mucosal barrier critical to upper airway immunity. However, our insufficient knowledge of olfactory mucosal immunity hinders attempts to protect this tissue from infection and other diseases. This Review summarizes the state of olfactory immunology by highlighting the unique immunologically relevant anatomy of the olfactory mucosa, describing what is known of olfactory immune cells, and considering the impact of common infectious diseases and inflammatory disorders at this site. We will offer our perspective on the future of the field and the many unresolved questions pertaining to olfactory immunity.

Citing Articles

Transcriptomic profiling of "brain-eating amoeba" infection in mice: the host and the protozoa perspectives.

Guerlais V, Allouch N, Moseman E, Wojciechowska A, Wojciechowski J, Marcelino I Front Cell Infect Microbiol. 2024; 14:1490280.

PMID: 39735262 PMC: 11682717. DOI: 10.3389/fcimb.2024.1490280.

Regional specialization within the mammalian respiratory immune system.

Hoytema van Konijnenburg D, Nigrovic P, Zanoni I Trends Immunol. 2024; 45(11):871-891.

PMID: 39438172 PMC: 11560516. DOI: 10.1016/j.it.2024.09.011.

Why do central nervous system barriers host a diverse immune landscape?.

Zanluqui N, McGavern D Trends Immunol. 2024; 45(10):738-749.

PMID: 39299888 PMC: 11471389. DOI: 10.1016/j.it.2024.08.009.

Therapeutic glycan-specific antibody binding mediates protection during primary amoebic meningoencephalitis.

Moseman A, Chen C, Liang X, Liao D, Kuraoka M, Moseman E Infect Immun. 2024; 92(10):e0018324.

PMID: 39235225 PMC: 11475618. DOI: 10.1128/iai.00183-24.

Distinct olfactory mucosal macrophage populations mediate neuronal maintenance and pathogen defense.

Wellford S, Chen C, Vukovic M, Batich K, Lin E, Shalek A Mucosal Immunol. 2024; 17(5):1102-1113.

PMID: 39074615 PMC: 11483463. DOI: 10.1016/j.mucimm.2024.07.009.

References

Williams J, Long S, Zeng X, Kuehl K, Babka A, Davis N . Eastern equine encephalitis virus rapidly infects and disseminates in the brain and spinal cord of cynomolgus macaques following aerosol challenge. PLoS Negl Trop Dis. 2022; 16(5):e0010081. PMC: 9084534. DOI: 10.1371/journal.pntd.0010081. View

Podlesnaja M, Pilmane M, Sumeraga G . Cytokines, Proliferation Markers, Antimicrobial Factors and Neuropeptide-Containing Innervation in Human Nasal Mucosa after Rhinoseptoplasty Procedure. Med Sci (Basel). 2021; 9(2). PMC: 8167725. DOI: 10.3390/medsci9020025. View

Milinski M . A Review of Suggested Mechanisms of MHC Odor Signaling. Biology (Basel). 2022; 11(8). PMC: 9405088. DOI: 10.3390/biology11081187. View

Gomes S, Delemarre T, Holtappels G, Van Zele T, Derycke L, Bonne E . Olfaction in nasal polyp patients after Reboot surgery: an endotype-based prospective study. Eur Arch Otorhinolaryngol. 2022; 280(6):2821-2830. PMC: 9791624. DOI: 10.1007/s00405-022-07813-w. View

Giacomelli A, Pezzati L, Conti F, Bernacchia D, Siano M, Oreni L . Self-reported Olfactory and Taste Disorders in Patients With Severe Acute Respiratory Coronavirus 2 Infection: A Cross-sectional Study. Clin Infect Dis. 2020; 71(15):889-890. PMC: 7184514. DOI: 10.1093/cid/ciaa330. View

Shirai T, Takase D, Yokoyama J, Nakanishi K, Uehara C, Saito N . Functions of human olfactory mucus and age-dependent changes. Sci Rep. 2023; 13(1):971. PMC: 9846672. DOI: 10.1038/s41598-023-27937-1. View

Mazanec M, Nedrud J, Liang X, Lamm M . Transport of serum IgA into murine respiratory secretions and its implications for immunization strategies. J Immunol. 1989; 142(12):4275-81. View

Yu Y, Kong W, Yin Y, Dong F, Huang Z, Yin G . Mucosal immunoglobulins protect the olfactory organ of teleost fish against parasitic infection. PLoS Pathog. 2018; 14(11):e1007251. PMC: 6237424. DOI: 10.1371/journal.ppat.1007251. View

Lechien J, Vaira L, Saussez S . Prevalence and 24-month recovery of olfactory dysfunction in COVID-19 patients: A multicentre prospective study. J Intern Med. 2022; 293(1):82-90. PMC: 9538281. DOI: 10.1111/joim.13564. View

10.

Murphy C . Olfactory and other sensory impairments in Alzheimer disease. Nat Rev Neurol. 2018; 15(1):11-24. DOI: 10.1038/s41582-018-0097-5. View

11.

Rojas-Hernandez S, Jarillo-Luna A, Rodriguez-Monroy M, Moreno-Fierros L, Campos-Rodriguez R . Immunohistochemical characterization of the initial stages of Naegleria fowleri meningoencephalitis in mice. Parasitol Res. 2004; 94(1):31-6. DOI: 10.1007/s00436-004-1177-6. View

12.

Brown A, Kent K, Bennett C, Bernard K . Tissue tropism and neuroinvasion of West Nile virus do not differ for two mouse strains with different survival rates. Virology. 2007; 368(2):422-30. PMC: 2814419. DOI: 10.1016/j.virol.2007.06.033. View

13.

Hsu M, Rayasam A, Kijak J, Choi Y, Harding J, Marcus S . Neuroinflammation-induced lymphangiogenesis near the cribriform plate contributes to drainage of CNS-derived antigens and immune cells. Nat Commun. 2019; 10(1):229. PMC: 6335416. DOI: 10.1038/s41467-018-08163-0. View

14.

Premraj L, Kannapadi N, Briggs J, Seal S, Battaglini D, Fanning J . Mid and long-term neurological and neuropsychiatric manifestations of post-COVID-19 syndrome: A meta-analysis. J Neurol Sci. 2022; 434:120162. PMC: 8798975. DOI: 10.1016/j.jns.2022.120162. View

15.

Lan Y, Yang P, Zeng Z, Yadav N, Zhang L, Wang L . Gene and protein expression profiles of olfactory ensheathing cells from olfactory bulb olfactory mucosa. Neural Regen Res. 2021; 17(2):440-449. PMC: 8463967. DOI: 10.4103/1673-5374.317986. View

16.

Kumari P, Rothan H, Natekar J, Stone S, Pathak H, Strate P . Neuroinvasion and Encephalitis Following Intranasal Inoculation of SARS-CoV-2 in K18-hACE2 Mice. Viruses. 2021; 13(1). PMC: 7832889. DOI: 10.3390/v13010132. View

17.

Martini V, Paudyal B, Chrun T, McNee A, Edmans M, Atangana Maze E . Simultaneous Aerosol and Intramuscular Immunization with Influenza Vaccine Induces Powerful Protective Local T Cell and Systemic Antibody Immune Responses in Pigs. J Immunol. 2020; 206(3):652-663. PMC: 7812058. DOI: 10.4049/jimmunol.2001086. View

18.

Getchell M, Getchell T . Immunohistochemical localization of components of the immune barrier in the olfactory mucosae of salamanders and rats. Anat Rec. 1991; 231(3):358-74. PMC: 7159625. DOI: 10.1002/ar.1092310310. View

19.

Chen M, Reed R, Lane A . Acute inflammation regulates neuroregeneration through the NF-κB pathway in olfactory epithelium. Proc Natl Acad Sci U S A. 2017; 114(30):8089-8094. PMC: 5544262. DOI: 10.1073/pnas.1620664114. View

20.

Palominos M, Calfun C, Nardocci G, Candia D, Torres-Paz J, Whitlock K . The Olfactory Organ Is a Unique Site for Neutrophils in the Brain. Front Immunol. 2022; 13:881702. PMC: 9186071. DOI: 10.3389/fimmu.2022.881702. View