Identification of a new pharyngeal mucosal lymphoid organ in zebrafish and other teleosts: tonsils in fish?
Science Advances(2023)
Abstract
The constant exposure of the fish branchial cavity to aquatic pathogens must have driven local mucosal immune responses to be extremely important for their survival. In this study, we used a universal marker for T lymphocytes/natural killer cells (ZAP70) and advanced imaging techniques to investigate the lymphoid architecture of the zebrafish branchial cavity. We identified a new lymphoid organ, which we tentatively named “Nemausean Lymphoid Organ” (NEMO), situated below the pharynx, and closely associated with gill lymphoid tissues. Besides T/NK cells, NEMO is enriched in plasma/B cells and antigen-presenting cells embedded in a network of reticulated epithelial cells. Presence of activated T cells and lymphocyte proliferation but not V(D)J recombination or hematopoiesis, suggests a function as secondary lymphoid organ. In response to infection, NEMO displays structural changes including the formation of T/NK cells clusters. NEMO and gill lymphoid aggregates form a cohesive unit within a lymphoid network that extends throughout the pharyngo-respiratory area. Collectively, our findings reveal a new mucosal lymphoid organ reminiscent of mammalian tonsils that evolved in fish. Importantly, NEMO could clearly be identified in multiple teleost fish families.
One sentence summary A previously unreported lymphoid organ has been identified within the pharyngo-respiratory tract of the zebrafish, and other teleost fish, providing new insights into the immune system of teleost fish and the evolution of vertebrate immunology.
### Competing Interest Statement
The authors have declared no competing interest.
* Aa
: Afferent artery
Aaa
: Afferent arch artery
ALT
: Amphibranchial Lymphoid Tissue
B
: Bone
Bc
: Branchial cavity
Bm
: Basement membrane
BTK
: Bruton Tyrosine Kinase
Bv
: Blood vessel
C
: Cartilage
Cbe
: Cavo-branchial epithelium
Ct
: Connective tissue
Cvs
: Central venous sinus
d-ILT
: distal Interbranchial Lymphoid Tissue
Dpi
: Day post-infection
Ea
: Efferent artery
Eaa
: Efferent arch artery
Eav
: Endothelial anastomotic vessels
Ec
: Endothelial cell
EM
: Electron Microscopy
Ft
: Fat tissue
Ga
: Gill arch
GALT
: Gut-Associated Lymphoid Tissue
Gi
: Gills
GIALT
: Gill-Associated Lymphoid Tissue
H&E
: Hematoxylin and Eosin
HK
: Head-Kidney
ILT
: Interbranchial Lymphoid Tissue
IHNV
: Infectious Hematopoietic Necrosis Virus
La
: Lamellae
Lu
: Lumen
M
: Muscles
MALT
: Mucosa-Associated Lymphoid Tissue
NALT
: Nasal-Associated Lymphoid Tissue
NEMO
: Nemausean lymphoid Organ
NK
: cell Natural Killer cell
Op
: Operculum
PCNA
: Proliferating Cell Nuclear Antigen
p-ILT
: proximal Interbranchial Lymphoid Tissue
Rbc
: Red blood cell
S
: Septum
SALT
: Skin Associated Lymphoid Tissue
Sk
: Skin
Spi
: Sub-pharyngeal isthmus
SVCV
: Spring Viremia of Carp Virus
Tc
: Thymus cortex
Td
: tendon
TEM
: Transmission Electron Microscopy
Tf
: Thyroid follicle
Tm
: Thymus medulla
Tu
: Tubule
Uh
: Urohyal bone
Um
: Urohyal marrow
Va
: Ventral aorta
Wpf
: week post-fertilization
ZAP70
: Zeta-chain-Associated Protein kinase 70.
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