Click
here to close Hello! We notice that
you are using Internet Explorer, which is not supported by Echinobase
and may cause the site to display incorrectly. We suggest using a
current version of Chrome,
FireFox,
or Safari.
Front Immunol
2014 Sep 23;5:459. doi: 10.3389/fimmu.2014.00459.
Show Gene links
Show Anatomy links
Evolution of Innate Immunity: Clues from Invertebrates via Fish to Mammals.
Buchmann K
.
???displayArticle.abstract???
Host responses against invading pathogens are basic physiological reactions of all living organisms. Since the appearance of the first eukaryotic cells, a series of defense mechanisms have evolved in order to secure cellular integrity, homeostasis, and survival of the host. Invertebrates, ranging from protozoans to metazoans, possess cellular receptors, which bind to foreign elements and differentiate self from non-self. This ability is in multicellular animals associated with presence of phagocytes, bearing different names (amebocytes, hemocytes, coelomocytes) in various groups including animal sponges, worms, cnidarians, mollusks, crustaceans, chelicerates, insects, and echinoderms (sea stars and urchins). Basically, these cells have a macrophage-like appearance and function and the repair and/or fight functions associated with these cells are prominent even at the earliest evolutionary stage. The cells possess pathogen recognition receptors recognizing pathogen-associated molecular patterns, which are well-conserved molecular structures expressed by various pathogens (virus, bacteria, fungi, protozoans, helminths). Scavenger receptors, Toll-like receptors, and Nod-like receptors (NLRs) are prominent representatives within this group of host receptors. Following receptor-ligand binding, signal transduction initiates a complex cascade of cellular reactions, which lead to production of one or more of a wide array of effector molecules. Cytokines take part in this orchestration of responses even in lower invertebrates, which eventually may result in elimination or inactivation of the intruder. Important innate effector molecules are oxygen and nitrogen species, antimicrobial peptides, lectins, fibrinogen-related peptides, leucine rich repeats (LRRs), pentraxins, and complement-related proteins. Echinoderms represent the most developed invertebrates and the bridge leading to the primitive chordates, cephalochordates, and urochordates, in which many autologous genes and functions from their ancestors can be found. They exhibit numerous variants of innate recognition and effector molecules, which allow fast and innate responses toward diverse pathogens despite lack of adaptive responses. The primitive vertebrates (agnathans also termed jawless fish) were the first to supplement innate responses with adaptive elements. Thus hagfish and lampreys use LRRs as variable lymphocyte receptors, whereas higher vertebrates [cartilaginous and bony fishes (jawed fish), amphibians, reptiles, birds, and mammals] developed the major histocompatibility complex, T-cell receptors, and B-cell receptors (immunoglobulins) as additional adaptive weaponry to assist innate responses. Extensive cytokine networks are recognized in fish, but related signal molecules can be traced among invertebrates. The high specificity, antibody maturation, immunological memory, and secondary responses of adaptive immunity were so successful that it allowed higher vertebrates to reduce the number of variants of the innate molecules originating from both invertebrates and lower vertebrates. Nonetheless, vertebrates combine the two arms in an intricate inter-dependent network. Organisms at all developmental stages have, in order to survive, applied available genes and functions of which some may have been lost or may have changed function through evolution. The molecular mechanisms involved in evolution of immune molecules, might apart from simple base substitutions be as diverse as gene duplication, deletions, alternative splicing, gene recombination, domain shuffling, retrotransposition, and gene conversion. Further, variable regulation of gene expression may have played a role.
Figure 1. Evolution of the immune system is shown. Immune cells and molecules from early invertebrates to vertebrates are shown. Geological periods and time periods (million years ago, mya) are shown with extant representatives of animal groups appearing at different time during evolution.
Baeza Garcia,
Involvement of the cytokine MIF in the snail host immune response to the parasite Schistosoma mansoni.
2010, Pubmed
Baeza Garcia,
Involvement of the cytokine MIF in the snail host immune response to the parasite Schistosoma mansoni.
2010,
Pubmed
Betti,
Effects of tumour necrosis factor alpha (TNFalpha) on Mytilus haemocytes: role of stress-activated mitogen-activated protein kinases (MAPKs).
2006,
Pubmed
Bilej,
Antimicrobial defense of the earthworm.
2000,
Pubmed
Boudinot,
A tetrapod-like repertoire of innate immune receptors and effectors for coelacanths.
2014,
Pubmed
Buchmann,
Interactions between monogenean parasites and their fish hosts.
2002,
Pubmed
Buchmann,
Fish immune responses against endoparasitic nematodes - experimental models.
2012,
Pubmed
Chettri,
PAMP induced expression of immune relevant genes in head kidney leukocytes of rainbow trout (Oncorhynchus mykiss).
2011,
Pubmed
Chettri,
Epidermal response of rainbow trout to Ichthyobodo necator: immunohistochemical and gene expression studies indicate a Th1-/Th2-like switch.
2014,
Pubmed
Clark,
Evasion of killing by human antibody and complement through multiple variations in the surface oligosaccharide of Haemophilus influenzae.
2013,
Pubmed
Cooper,
Evolution of immune systems from self/not self to danger to artificial immune systems (AIS).
2010,
Pubmed
Crivellato,
The mast cell: an evolutionary perspective.
2010,
Pubmed
Cupit,
Ikaros family members from the agnathan Myxine glutinosa and the urochordate Oikopleura dioica: emergence of an essential transcription factor for adaptive immunity.
2003,
Pubmed
Desjardins,
Phagocytosis: the convoluted way from nutrition to adaptive immunity.
2005,
Pubmed
Detournay,
Regulation of cnidarian-dinoflagellate mutualisms: Evidence that activation of a host TGFβ innate immune pathway promotes tolerance of the symbiont.
2012,
Pubmed
Dishaw,
Invertebrate allorecognition: the origins of histocompatibility.
2009,
Pubmed
Dunin-Horkawicz,
Prokaryotic ancestry of eukaryotic protein networks mediating innate immunity and apoptosis.
2014,
Pubmed
Dzik,
The ancestry and cumulative evolution of immune reactions.
2010,
Pubmed
Elvitigala,
Molecular insights of the first gastropod TLR counterpart from disk abalone (Haliotis discus discus), revealing its transcriptional modulation under pathogenic stress.
2013,
Pubmed
Franzenburg,
MyD88-deficient Hydra reveal an ancient function of TLR signaling in sensing bacterial colonizers.
2012,
Pubmed
Fujito,
Evolution of thioester-containing proteins revealed by cloning and characterization of their genes from a cnidarian sea anemone, Haliplanella lineate.
2010,
Pubmed
Fuller-Espie,
Vertebrate cytokines interleukin 12 and gamma interferon, but not interleukin 10, enhance phagocytosis in the annelid Eisenia hortensis.
2010,
Pubmed
Ghosh,
Invertebrate immune diversity.
2011,
Pubmed
,
Echinobase
Hahn,
Involvement of nitric oxide in killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata.
2001,
Pubmed
Hahn,
Production of reactive oxygen species by hemocytes of Biomphalaria glabrata: carbohydrate-specific stimulation.
2000,
Pubmed
Hauton,
The scope of the crustacean immune system for disease control.
2012,
Pubmed
Heinecke,
Adaptive and innate immune molecules in developing rainbow trout, Oncorhynchus mykiss eggs and larvae: expression of genes and occurrence of effector molecules.
2014,
Pubmed
Higa,
Lose the battle to win the war: bacterial strategies for evading host inflammasome activation.
2013,
Pubmed
Jin,
Identification and characterization of a putative lipopolysaccharide-induced TNF-α factor (LITAF) gene from Amphioxus (Branchiostoma belcheri): an insight into the innate immunity of Amphioxus and the evolution of LITAF.
2012,
Pubmed
Kaiser,
Advances in avian immunology--prospects for disease control: a review.
2010,
Pubmed
Kasahara,
On the origins of the adaptive immune system: novel insights from invertebrates and cold-blooded vertebrates.
2004,
Pubmed
Kaur,
Identification of a scavenger receptor homologue on nonspecific cytotoxic cells and evidence for binding to oligodeoxyguanosine.
2003,
Pubmed
Kishishita,
Evolution of adaptive immunity: implications of a third lymphocyte lineage in lampreys.
2014,
Pubmed
Lin,
Crustacean hematopoiesis and the astakine cytokines.
2011,
Pubmed
Lin,
Ancient cytokines, the role of astakines as hematopoietic growth factors.
2010,
Pubmed
Litman,
The origins of vertebrate adaptive immunity.
2010,
Pubmed
Maizels,
Toxocara canis: molecular basis of immune recognition and evasion.
2013,
Pubmed
Malagoli,
unpaired (upd)-3 expression and other immune-related functions are stimulated by interleukin-8 in Drosophila melanogaster SL2 cell line.
2008,
Pubmed
Mills,
M1 and M2 Macrophages: Oracles of Health and Disease.
2012,
Pubmed
Mukherjee,
Ancient origins of vertebrate-specific innate antiviral immunity.
2014,
Pubmed
Nonaka,
Primitive complement system of invertebrates.
2004,
Pubmed
Nydam,
Molecular evolution of a polymorphic HSP40-like protein encoded in the histocompatibility locus of an invertebrate chordate.
2013,
Pubmed
Peiser,
Scavenger receptors in innate immunity.
2002,
Pubmed
Perović-Ottstadt,
A (1-->3)-beta-D-glucan recognition protein from the sponge Suberites domuncula. Mediated activation of fibrinogen-like protein and epidermal growth factor gene expression.
2004,
Pubmed
Reite,
Inflammatory cells of teleostean fish: a review focusing on mast cells/eosinophilic granule cells and rodlet cells.
2006,
Pubmed
Rhodes,
Presence of coelomocytes in the primitive chordate amphioxus (Branchiostoma lanceolatum).
1982,
Pubmed
Roberts,
Rapid accumulation of an interleukin 17 homolog transcript in Crassostrea gigas hemocytes following bacterial exposure.
2008,
Pubmed
,
Echinobase
Ryzhakov,
Evolution of vertebrate immunity: sequence and functional analysis of the SEFIR domain family member Act1.
2011,
Pubmed
Salazar-Jaramillo,
Evolution of a cellular immune response in Drosophila: a phenotypic and genomic comparative analysis.
2014,
Pubmed
Schmid-Hempel,
Immune defence, parasite evasion strategies and their relevance for 'macroscopic phenomena' such as virulence.
2009,
Pubmed
Severin,
Expression of immune-regulatory genes, arginase-2 and inducible nitric oxide synthase (iNOS), in two rainbow trout (Oncorhynchus mykiss) strains following exposure to Myxobolus cerebralis.
2010,
Pubmed
Sigh,
The parasitic ciliate Ichthyophthirius multifiliis induces expression of immune relevant genes in rainbow trout, Oncorhynchus mykiss (Walbaum).
2004,
Pubmed
Skugor,
Local and systemic gene expression responses of Atlantic salmon (Salmo salar L.) to infection with the salmon louse (Lepeophtheirus salmonis).
2008,
Pubmed
Song,
Identification and evolution of an NFAT gene involving Branchiostoma belcheri innate immunity.
2013,
Pubmed
,
Echinobase
Srivastava,
Does fish represent an intermediate stage in the evolution of ureotelic cytosolic arginase I?
2010,
Pubmed
Sun,
Novel translationally controlled tumor protein homologue in the buccal gland secretion of Lampetra japonica.
2008,
Pubmed
Venkatesh,
Elephant shark genome provides unique insights into gnathostome evolution.
2014,
Pubmed
Wang,
The cytokine networks of adaptive immunity in fish.
2013,
Pubmed
Watthanasurorot,
An ancient cytokine, astakine, mediates circadian regulation of invertebrate hematopoiesis.
2011,
Pubmed
Wittamer,
Characterization of the mononuclear phagocyte system in zebrafish.
2011,
Pubmed
Yuen,
The characterization of sponge NLRs provides insight into the origin and evolution of this innate immune gene family in animals.
2014,
Pubmed
Zeng,
Cloning, characterization, and expression of the macrophage migration inhibitory factor gene from the Pacific white shrimp Litopenaeus vannamei (Penaeidae).
2013,
Pubmed
Zhang,
IgT, a primitive immunoglobulin class specialized in mucosal immunity.
2010,
Pubmed
Zhang,
The involvement of suppressors of cytokine signaling 2 (SOCS2) in immune defense responses of Chinese mitten crab Eriocheir sinensis.
2010,
Pubmed
Zhang,
An amphioxus RAG1-like DNA fragment encodes a functional central domain of vertebrate core RAG1.
2014,
Pubmed
Zhang,
Allograft inflammatory factor-1 stimulates hemocyte immune activation by enhancing phagocytosis and expression of inflammatory cytokines in Crassostrea gigas.
2013,
Pubmed
Zimmerman,
Understanding the vertebrate immune system: insights from the reptilian perspective.
2010,
Pubmed
Škanta,
Molecular cloning and expression of TLR in the Eisenia andrei earthworm.
2013,
Pubmed