Immune Response: Evolution

Abstract

Innate immune processes arose from specific host–pathogen coevolutive interactions and the ability to recognise self and nonself structures is extremely conserved from invertebrates to vertebrates. In this context, phagocytes represent the most ancient defensive line against foreign materials, already present in earliest protostomes. Moreover, although more complex functions evolved in vertebrates, both cellular and humoral innate immune mechanisms are extremely conserved, leading to identify some forms of innate immune memory also in invertebrates.

Key Concepts

  • Phagocytosis represents the first mechanism of defence in metazoans.
  • Immune system has evolved to discriminate self and nonself structures.
  • Immune mechanisms present a high level of conservation throughout phyla.
  • Vertebrate innate immune memory derives from ancient forms and mechanisms already present in invertebrates.
  • Alternative animal models are crucial for investigating the molecular basis of the immune processes.

Keywords: invertebrate; innate immunity; adaptive immunity; comparative immunology; immune memory

Figure 1. Representation to describe the HvRNASET2 antibacterial role in the medicinal leech. After 30 min, both PAMPs or DAMPs recognition by TLR2 and TLR4 positive cells induces granulocyte activation. These immune cells secrete HvRNASET2, whose primary role is to perform an antibacterial activity against harmful invaders. Moreover, HvRNASET2 allows to recruit numerous macrophages in the stimulated area especially after 6–24 h, and these cells subsequently secrete both AIF‐1 and HvRNASET2, which maintain the inflammatory state by the recruitment of other macrophages. These phagocytic cells not only represent the main defensive line against pathogens but also play a pivotal role in cellular and bacterial debris clearance.
Figure 2. The humoral cytolytic factor presents in the oligochetes coelom (CCF) is involved in peptidoglycan, b‐1,3‐glucan and LPS recognition. These molecules are highly present on bacterial and yeast membranes and once detected induce the prophenoloxidase cascade activation, which in turn leads to melanin production.
Figure 3. (a) Hirudinea immunocytes. TEM images representing a transversal section of LPS stimulated leech and the relative immune cells detected in the stimulated area. Underneath the epithelium (e), numerous vessels (v) are clearly visible after LPS treatment and different types of migrating cells are easily recognizable (arrowheads). NK cells, macrophages and two types of granulocytes are shown in TEM details. A scheme of Hirudinea immunocytes and of their inherent roles is represented below. (b) Schemes of both body wall transversal sections and gut anterior portion of oligochetes. Hyaline (LC) and granular (SC) coelomocytes, shown in TEM details, derive from somatopleure (in yellow) and splanchnopleure (in green) respectively. These cells express specific markers and possess phagocytic and cytotoxic activities. Around the gut, chloragocytes (or eleocytes) play an antibacterial role by releasing several molecules that directly act against pathogens.
close

References

Acquati F, Monti L, Lualdi M, et al. (2011) Molecular signature induced by RNASET2, a tumor antagonizing gene, in ovarian cancer cells. Oncotarget 2 (6): 477–484.

Akira S, Uematsu S and Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124 (4): 783–801.

Baranzini N, De Vito A, Orlandi VT, et al. (2020) Antimicrobial role of RNASET2 protein during innate immune response in the medicinal leech Hirudo verbana. Frontiers in Immunology 11: 370.

Blalock JE (2005) The immune system as the sixth sense. Journal of Internal Medicine 257 (2): 126–138.

Buchmann K (2014) Evolution of innate immunity: clues from invertebrates via fish to mammals. Frontiers in Immunology 5: 459.

Chaplin DD (2010) Overview of the immune response. The Journal of Allergy and Clinical Immunology 125 (2 Suppl 2): S3–S23.

Chou PH, Chang HS, Chen IT, et al. (2009) The putative invertebrate adaptive immune protein Litopenaeus vannamei Dscam (LvDscam) is the first reported Dscam to lack a transmembrane domain and cytoplasmic tail. Developmental and Comparative Immunology 33 (12): 1258–1267.

Cooper EL, Kauschke E and Cossarizza A (2002) Digging for innate immunity since Darwin and Metchikoff. BioEssays 24: 319–333.

Dong Y, Taylo HE and Dimopoulos G (2006) AgDscam, a hypervariable immunoglobulin domain‐containing receptor of the Anopheles gambiae innate immune system. PLoS Biology 4 (7): e229.

Drago F, Sautière PE, Le Marrec‐Croq F, et al. (2014) Microglia of medicinal leech (Hirudo medicinalis) express a specific activation marker homologous to vertebrate ionized calcium‐binding adapter molecule 1 (Iba1/alias aif‐1). Developmental Neurobiology 74 (10): 987–1001.

de Eguileor M, Grimaldi A, Tettamanti G, et al. (2000) Lipopolysaccharide‐dependent induction of leech leukocytes that cross‐react with vertebrate cellular differentiation markers. Tissue and Cell 32 (5): 437–445.

de Eguileor M, Grimaldi A and Tettamanti G (2016) Protective responses in invertebrates. In: Loriano Ballarin and Matteo Cammarata (eds.) Lesson in immunity. From Single‐Cell Organisms to Mammals. Chapter 11, pp 145–157. Academic Press: Cambridge, USA.

Eleftheriadis T, Antoniadi G, Liakopoulos V, et al. (2010) Paricalcitol reduces basal and lipopolysaccharide‐induced (LPS) TNF‐alpha and IL‐8 production by human peripheral blood mononuclear cells. International Urology and Nephrology 42 (1): 181–185.

Engelmann P, Bodó K, Najbauer J, et al. (2018) Annelida: Oligochaetes (segmented worms): earthworm immunity, quo vadis? Advances and new paradigms ín the omics era. In: Cooper E (ed.) Advances in Comparative Immunology, pp 135–191. Springer: Cham.

Girardello R, Baranzini N, Tettamanti G, et al. (2019) The medicinal leech as a valuable model for better understanding the role of a TLR4‐like receptor in the inflammatory process. Cell and Tissue Research 377 (3): 245–257.

Girón‐pérez MI (2010) Relationships between innate immunity in bivalve molluscs and environmental pollution. Invertebrate Survival Journal 7 (2): 149–156.

Gordon S (2016) Elie metchnikoff, the man and the myth. Journal of Innate Immunity 8 (3): 223–227.

Gourbal B, Pinaud S, Beckers GJM, et al. (2018) Innate immune memory: an evolutionary perspective. Immunology Reviews 283 (1): 21–40.

Greco S, Gerdol M, Edomi P, et al. (2020) Molecular diversity of mytilin‐like defense peptides in mytilidae (Mollusca, Bivalvia). Antibiotics 9 (1): 37.

Grimaldi A (2014) Anellidi. In: Ottaviani E (ed.) Compendio di Immunobiologia Comparata, pp 19–33. Piccin: Padova.

Grimaldi A, Tettamanti G, Girardello R, et al. (2014) Functional amyloid formation in LPS activated cells from invertebrates to vertebrates. Invertebrate Survival Journal 11 (1): 286–297.

Hartenstein V and Martinez P (2019) Phagocytosis in cellular defense and nutrition: a food‐centered approach to the evolution of macrophages. Cell and Tissue Research 377 (3): 527–547.

Hildemann WH, Johnson IS and Jokiel PL (1979) Immunocompetence in the lowest metazoan phylum: transplantation immunity in sponges. Science 204: 420–422.

Homa J (2018) Earthworm coelomocyte extracellular traps: structural and functional similarities with neutrophil NETs. Cell and Tissue Research 371 (3): 407–414.

Jin P, Hu J, Qian J, et al. (2012) 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. Fish and Shellfish Immunology 32 (6): 1223–1228.

Kaur H, Jaso‐Friedmann L and Evans DL (2003) Identification of a scavenger receptor homologue on non‐specific cytotoxic cells and evidence for binding to oligodeoxyguanosine. Fish and Shellfish Immunology 15 (3): 169–181.

Kvell K, Cooper EL, Engelmann P, et al. (2007) Blurring borders: innate immunity with adaptive features. Clinical and Developmental Immunology 2007: 83671.

Leor J, Palevski D, Amit U, et al. (2016) Macrophages and regeneration: lessons from the heart. Seminars in Cell and Developmental Biology 58: 26–33.

Li S, Jia Z, Li X, et al. (2014) Identification and expression analysis of lipopolysaccharide‐induced TNF‐alpha factor gene in Chinese mitten crab Eriocheir sinensis. Fish and Shellfish Immunology 38 (1): 190–195.

Liu Y, Zhang P, Wang W, et al. (2018) A DM9‐containing protein from oyster Crassostrea gigas (CgDM9CP‐2) serves as a multipotent pattern recognition receptor. Developmental and Comparative Immunology 84: 315–326.

Liu S, Zheng SC, Li Y, et al. (2020) Hemocyte‐mediated phagocytosis in Crustaceans. Frontiers in Immunology 11: 268.

Malagoli D (2010) Cytokine network in invertebrates: the very next phase of comparative immunology. Invertebrate Survival Journal 7 (2): 146–148.

Metchnikoff E (1901) L'immunité dans les Maladies Infectieuses. Masson: Paries.

Milutinović B and Kurtz J (2016) Immune memory in invertebrates. Seminars in Immunology 28 (4): 328–342.

Ottaviani E (2010) Immunocyte: the invertebrate counterpart of the vertebrate macrophage. Invertebrate Survival Journal 8 (1): 1–4.

Pancer Z, Amemiya CT, Ehrhardt GR, et al. (2004) Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 430 (6996): 174–180.

Parisi MG, Vizzini A, Toubiana M, et al. (2015) Identification, cloning and environmental factors modulation of a αβ defensin from the Lessepsian invasive mussel Brachidontes pharaonis (Bivalvia: Mytilidae). Invertebrate Survival Journal 12 (1): 264–273.

Parrinello N, Vizzini A, Arizza V, et al. (2008) Enhanced expression of a cloned and sequenced Ciona intestinalis TNFalpha‐like (CiTNF alpha) gene during the LPS‐induced inflammatory response. Cell and Tissue Research 334 (2): 305–317.

Passlick B, Flieger D and Ziegler‐Heitbrock HW (1989) Identification and characterization of a novel monocyte subpopulation in human peripheral blood. Blood 74 (7): 2527–2534.

Peskin AV, Labas YA and Tikhonov AN (1998) Superoxide radical production by sponges Sycon sp. FEBS 434: 201–204.

Pozzolini M, Scarfì S, Ghignone S, et al. (2016) Molecular characterization and expression analysis of the first Porifera tumor necrosis factor superfamily member and of its putative receptor in the marine sponge Chondrosia reniformis. Developmental and Comparative Immunology 57: 88–98.

Pradeu T and Du Pasquier L (2018) Immunological memory: what's in a name? Immunological Reviews 283 (1): 7–20.

Prendergast RA and Suzuki M (1970) Invertebrate protein simulating mediators of delayed hypersensitivity. Nature 227 (5255): 277–279.

Ruscitti P, Rago C, Breda L, et al. (2017) Macrophage activation syndrome in still's disease: analysis of clinical characteristics and survival in paediatric and adult patients. Clinical Rheumatology 36 (12): 2839–2845.

Schorn T, Drago F, de Eguileor M, et al. (2015) The allograft inflammatory factor‐1 (AIF‐1) homologous in Hirudo medicinalis (medicinal leech) is involved in immune response during wound healing and graft rejection processes. Invertebrate Survival Journal 12 (1): 129–141.

Tasiemski A, Massol F, Cuvillier‐Hot V, et al. (2015) Reciprocal immune benefit based on complementary production of antibiotics by the leech Hirudo verbana and its gut symbiont Aeromonas veronii. Scientific Reports 5: 17498.

Tettamanti G, Grimaldi A, Ferrarese R, et al. (2003) Leech responses to tissue transplantation. Tissue and Cell 35 (3): 199–212.

Zhang G and Ghosh S (2001) Toll‐like receptor‐mediated NF‐kappaB activation: a phylogenetically conserved paradigm in innate immunity. The Journal of Clinical Investigation 107 (1): 13–19.

Further Reading

Grimaldi A, Tettamanti G and de Eguileor M (2018) Annelida: Hirudinea (Leeches): heterogeneity in leech immune responses. In: Cooper E (ed.) Advances in Comparative Immunology, pp 173–191. Springer: Cham.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Baranzini, Nicolò, Engelmann, Péter, and Grimaldi, Annalisa(Dec 2020) Immune Response: Evolution. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0029225]