Nasal immunity is an ancient arm of the mucosal immune system of vertebrates

Abstract

The mucosal surfaces of all vertebrates have been exposed to similar evolutionary pressures for millions of years. In terrestrial vertebrates such as birds and mammals, the nasopharynx-associated lymphoid tissue (NALT) represents a first line of immune defence. Here we propose that NALT is an ancient arm of the mucosal immune system not restricted to terrestrial vertebrates. We find that NALT is present in rainbow trout and that it resembles other teleost mucosa-associated lymphoid tissues. Trout NALT consists of diffuse lymphoid cells and lacks tonsils and adenoids. The predominant B-cell subset found in trout NALT are IgT + B cells, similar to skin and gut. The trout olfactory organ is colonized by abundant symbiotic bacteria, which are coated by trout secretory immunoglobulin. Trout NALT is capable of mounting strong anti-viral immune responses following nasal delivery of a live attenuated viral vaccine. Our results open up a new tool for the control of aquatic infectious diseases via nasal vaccination.

Nasal vaccination of young rainbow trout ( Oncorhynchus mykiss ) against infectious hematopoietic necrosis and enteric red mouth disease

“…Interestingly, the power of diffuse NALT to induce effective immunity following nasal vaccination in the absence of organized NALT was unequivocally demonstrated in newborn mice whose organized NALT had been surgically removed (Sabirov and Metzger, 2008). Recently, we characterized teleost NALT, which consists of diffuse NALT only lacking organized lymphoid structures such as tonsils or adenoids (Tacchi et al, 2014).…”

“…The discovery of nasal immunity in teleosts prompted the first studies concerning nasal vaccines for use in aquaculture (Tacchi et al, 2014;LaPatra et al, 2015). Both ERM and IHNV vaccines are very effective when delivered intranasally to approximately 5 g rainbow trout.…”

“…Duplicate 25-fish groups from each treatment were challenged with either IHNV or Yersinia ruckeri at 28 (400 DD) days postimmunization (dpi) and followed for an additional 28 days as previously described (Tacchi et al, 2014). Kidney, spleen and liver were collected from rainbow trout that died prior to challenge.…”

“…Recently, nasal vaccines were added to this list. Nasal vaccination can be a very effective way to control 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 aquatic infectious diseases in finfish (Tacchi et al, 2014;LaPatra et al, 2015). The use of this delivery route has been tested in small trout but age was not controlled in those studies.…”

Topographical Mapping of the Rainbow Trout (Oncorhynchus mykiss) Microbiome Reveals a Diverse Bacterial Community with Antifungal Properties in the Skin

“…In our trout data set, however, Bacteroidetes and Proteobacteria were the most abundant bacterial groups. The recent discovery of a nasopharynx-associated lymphoid tissue (NALT) in teleosts (62) and the presence of a rich bacterial microbiota in association with this mucosal surface highlights the importance of the cross talk between the nasal microbiota and vertebrate NALT. Our initial pyrosequencing results and the finding that the skin is the most diverse site in trout led us to hypothesize that some of the diversity may be associated with bacterial colonization of the trout skin epidermis.…”