Abstract
Mucosal surfaces are the main points of contact between animal bodies and the external environment. The olfactory system of vertebrates is one of the most ancient and conserved sensory systems and is responsible for the rapid detection of chemical stimuli. Apart from chemosensory functions, olfactory systems have evolved to defend animal hosts from invading pathogens. Although we know very little about the biological principles that govern nasal immune responses in nonmammalian vertebrates, our knowledge has increased over the past few years. This chapter reviews the phylogeny of olfactory systems and their associated lymphoid tissue, the nasopharynx-associated lymphoid tissue, and highlights how nasal vaccination studies have illuminated some of the immunological aspects of nasal immune systems from teleost fish to mammals.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Allison AC (1953) The morphology of the olfactory system in the vertebrates. Biol Rev 2:195–244
Amemiya CT et al (2013) The African coelacanth genome provides insights into tetrapod evolution. Nature 496:311–316
Asanuma H et al (1997) Isolation and characterization of mouse nasal-associated lymphoid tissue. J Immunol Methods 202:123–131
Atta KI (2013) Morphological, anatomical and histological studies on the olfactory organs and eyes of teleost fish: Anguilla anguilla in relation to its feeding habits. J Basic Appl Zool 66:101–108
Brandtzaeg P, Kiyono H, Pabst R, Russel MW (2008) Terminology: nomenclature of mucosa-associated lymphoid tissue. Mucosal Immunol 1:31–37
Brykczynska U, Tzika AC, Rodriguez I, Milinkovitch MC (2013) Contrasted evolution of the vomeronasal receptor repertoires in mammals and squamate reptiles. Genome Biol Evol 5:389–401
Cesta MF (2006) Normal structure, function, and histology of mucosa-associated lymphoid tissue. Toxicol Pathol 34:599–608
Chang S et al (2013) The sea lamprey has a primordial accessory olfactory system. BMC Evol Biol 13:172
Davis SS (2001) Nasal vaccines. Adv Drug Deliv Rev 51:21–42
Debertin AS, Tschernig T, Tönjes H, Kleemann WJ, Tröger HD, Pabst R (2003) Nasal-associated lymphoid tissue (NALT): frequency and localization in young children. Clin Exp Immunol 134:503–507
Døving KB, Trotier D (1998) Structure and function of the vomeronasal organs. J Exp Biol 201:2913–2925
Feng B, Bulchand S, Yaksi E, Friedrich RW, Jesuthasan S (2005) The recombination activation gene I (RagI) is expressed in a subset of zebrafish olfactory neurons but is not essential for axon targeting or amino acid detection. BMC Neurosci 6:46
Forero A et al (2017) Evaluation of the innate immune responses to influenza and live-attenuated influenza vaccine infection in primary differentiated human nasal epithelial cells. Vaccine 35:6112–6121
Galli SJ, Tsai M (2013) IgE and mast cells in allergic disease. Nat Med 18:693–704
Goldstine SN, Manickavel V, Choen N (1975) Phylogeny of gut-associated lymphoid tissue. Am Zool 15:107–118
Gomez G, Celii A (2008) The peripheral olfactory system of the domestic chicken: physiology and development. Brian Res Bull 76:208–216
González A, Morona R, López JM, Moreno N, Northcutt RG (2010) Lungfishes, like tetrapods, possess a vomeronasal system. Front Neuroanat 4:130
Guo P, Hirano M, Herrin BR, Li J, You C, Sadlonova A, Cooper MD (2009) Dual nature of the adaptive immune system in lampreys. Nature 459:796–801
Haley PJ (2003) Species differences in the structure and function of the immune system. Toxicology 188:49–71
Hamdani EH, Døving KB (2007) The functional organization of the fish olfactory system. Prog Neurobiol 82:80–86
Hathaway LJ, Kraehenbuhl JP (2000) The role of M cells in mucosal immunity. Cell Mol Life Sci 57:323–332
Heritage PL, Underdown BJ, Arsenault AL, Snider DP, McDermott MR (1997) Comparison of murine nasal-associated lymphoid tissue and Peyer’s patches. Am J Respir Crit Care Med 156:1256–1262
Jacobson ER et al (2014) Mycoplasmosis and upper respiratory tract disease of tortoises: a review and update. Vet J 201:257–264
Kang H, Wang H, Yu Q, Yang Q (2012) Effect of intranasal immunization with inactivated avian influenza virus on local and systemic immune responses in ducks. Poult Sci 91:1074–1080
Kang H, Yan M, Yu Q, Yang Q (2013) Characteristics of nasal-associated lymphoid tissue (NALT) and nasal absorption capacity in chicken. PLoS One 8:e84097
Kang H, Yan M, Yu Q, Yang Q (2014) Characterization of nasal cavity-associated lymphoid tissue in ducks. Anat Rec 297:916–924
Kermen F, Franco LM, Wyatt C, Yaksi E (2013) Neural circuits mediating olfactory-driven behavior in fish. Front Neural Circuits 7:62
Kiyono H, Fukuyama S (2004) NALT- versus Peyer’s-patch-mediated mucosal immunity. Nat Rev Immunol 4:699–710
Lacalli TC (2004) Sensory systems in amphioxus: a window on the ancestral chordate condition. Brain Behav Evol 64:148–162
Larragoite ET, Tacchi L, LaPatra SE, Salinas I (2016) An attenuated virus vaccine appears safe to the central nervous system of rainbow trout (Oncorhynchus mykiss) after intranasal delivery. Fish Shellfish Immunol 49:351–354
Malnic B, Godfrey PA, Buck LB (2003) The human olfactory receptor gene family. Proc Natl Acad Sci 101:2584–2589
Marschang RE (2011) Viruses infecting reptiles. Virus 3:2087–2126
Meredith TL, Kajiura SM (2010) Olfactory morphology and physiology of elasmobranchs. J Exp Biol 213:3449–3456
Nakamuta S, Nakamuta N, Taniguchi K, Taniguchi K (2012) Histological and ultrastructural characteristics of the primordial vomeronasal organ in lungfish. Anat Rec 295:481–491
Nei M, Niimura Y, Nozawa M (2008) The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity. Nat Rev Genet 9:951–963
Niimura Y (2009a) Evolutionary dynamics of olfactory receptor genes in chordates: interaction between environments and genomic contents. Hum Genomics 4:107–118
Niimura Y (2009b) On the origin and evolution of vertebrate olfactory receptor genes: comparative genome analysis among 23 chordate species. Genome Biol Evol 1:34–44
Niimura Y, Nei M (2003) Evolution of olfactory receptor genes in the human genome. Proc Natl Acad Sci 100:12235–12240
Ohshima K, Hiramatsu K (2000) Distribution of T-cell subsets and immunoglobulin-containing cells in nasal-associated lymphoid tissue (NALT) of chickens. Histol Histopathol 15:713–720
Oikawa T, Suzuki K, Saito TR, Takahashi KW, Taniguchi K (1998) Fine structure of three types of olfactory organs in Xenopus laevis. Anat Rec 252:301–310
Olender T, Lancet D, Nebert DW (2008) Update on the olfactory receptor (OR) gene superfamily. Hum Genomics 3:87–97
Pancer Z, Amemiya CT, Ehrhardt GRA, Ceitlin J, Gartland GL, Cooper MD (2004) Somatic diversification of variable lymphocyte receptors in the agnathans sea lamprey. Nature 430:174–180
Perry M, Whyte A (1998) Immunology of the tonsils. Immunol Today 19:414–421
Saraiva LR, Ahuja G, Ivandic I, Syed AS, Marioni JC, Korsching SI, Logan DW (2015) Molecular and neuronal homology between the olfactory systems of zebrafish and mouse. Sci Rep 5:11487
Satoh G (2005) Characterization of novel GPCR gene coding locus in amphioxus genome: gene structure, expression, and phylogenetic analysis with implications for its involvement in chemoreception. Genesis 41:47–57
Schumacher J (2003) Reptile respiratory medicine. Vet Clin Exot Anim 6:213–231
Sepahi A, Salinas I (2016) The evolution of nasal immune systems in vertebrates. Mol Immunol 69:131–138
Sepahi A, Casadei E, Tacchi L, Muñoz P, LaPatra SE, Salinas I (2016) Tissue microenvironments in the nasal epithelium of rainbow trout (Oncorhynchus mykiss) define two distinct CD8α+ cell populations and establish regional immunity. J Immunol 197:4453–4463
Sepahi A, Tacchi L, Casadei E, Takizawa F, LaPatra SE, Salinas I (2017) CK12a, a CCL19-like chemokine that orchestrates both nasal and systemic antiviral immune responses in rainbow trout. J Immunol 199:3900–3913
Śmiałek M, Tykałowski B, Stenzel T, Koncicki A (2011) Local immunity of the respiratory mucosal system in chickens and turkeys. Pol J Vet Sci 14:291–297
Tacchi L, Musharrafieh R, Larragoite ET, Crossey K, Erhardt EB, Martion SAM, LaPatra SE, Salinas I (2014) Nasal immunity is an ancient arm of the mucosal immune system of vertebrates. Nat Commun 5:5205
Tacchi L, Larragoite ET, Muñoz P, Amemiya CT, Salinas I (2015) African lungfish reveal the evolutionary origins of organized mucosal lymphoid tissue in vertebrates. Curr Biol 25:2417–2424
Taniguchi K, Taniguchi K (2014) Phylogenic studies on the olfactory system in vertebrates. J Vet Med Sci 76:781–788
Taniguchi K, Saito S, Taniguchi K (2010) Phylogenic outline of the olfactory system in vertebrates. J Vet Med Sci 73:139–147
Volff JN (2005) Genome evolution and biodiversity in teleost fish. Heredity 94:280–294
Yoplak KE, Lisney TJ, Collin SP (2015) Not all sharks are “swimming noses”: variation in olfactory bulb size in cartilaginous fishes. Brain Struct Funct 2203:1127–1143
Zardoya R, Meyer A (1996) Evolutionary relationships of the coelacanth, lungfishes, and tetrapods based on the 28S ribosomal RNA gene. Proc Natl Acad Sci 93:5449–5454
Zhao K et al (2016) IgA response and protection following nasal vaccination of chickens with Newcastle disease virus DNA vaccine nanoencapsulated with Ag@SiO2 hollow nanoparticles. Sci Rep 6:25720
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer International Publishing AG, part of Springer Nature
About this chapter
Cite this chapter
Heimroth, R.D., Salinas, I. (2018). Comparative Phylogeny of the Nasopharynx-Associated Lymphoid Tissue. In: Cooper, E. (eds) Advances in Comparative Immunology. Springer, Cham. https://doi.org/10.1007/978-3-319-76768-0_25
Download citation
DOI: https://doi.org/10.1007/978-3-319-76768-0_25
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-76767-3
Online ISBN: 978-3-319-76768-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)