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3 pages, 193 KiB

Open AccessEditorial

Ancient Immunity. Phylogenetic Emergence of Recognition-Defense Mechanisms

by Loriano Ballarin, Matteo Cammarata and Pierangelo Luporini

Biology 2021, 10(4), 342; https://doi.org/10.3390/biology10040342 - 19 Apr 2021

Cited by 3 | Viewed by 1983

Abstract

Although still scarcely considered by the majority of the biomedical world, invertebrates have greatly contributed to the elucidation of fundamental biological problems [...] Full article

(This article belongs to the Special Issue Ancient Immunity. Phylogenetic Emergence of Recognition-Defence Mechanisms)

Research

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17 pages, 4286 KiB

Open AccessArticle

The Immune Response of the Invasive Golden Apple Snail to a Nematode-Based Molluscicide Involves Different Organs

by Alice Montanari, Giulia Bergamini, Agnese Ferrari, Anita Ferri, Milena Nasi, Roberto Simonini and Davide Malagoli

Biology 2020, 9(11), 371; https://doi.org/10.3390/biology9110371 - 30 Oct 2020

Cited by 10 | Viewed by 3961

Abstract

The spreading of alien and invasive species poses new challenges for the ecosystem services, the sustainable production of food, and human well-being. Unveiling and targeting the immune system of invasive species can prove helpful for basic and applied research. Here, we present evidence [...] Read more.

The spreading of alien and invasive species poses new challenges for the ecosystem services, the sustainable production of food, and human well-being. Unveiling and targeting the immune system of invasive species can prove helpful for basic and applied research. Here, we present evidence that a nematode (Phasmarhabditis hermaphrodita)-based molluscicide exerts dose-dependent lethal effects on the golden apple snail, Pomacea canaliculata. When used at 1.7 g/L, this biopesticide kills about 30% of snails within one week and promotes a change in the expression of Pc-bpi, an orthologue of mammalian bactericidal/permeability increasing protein (BPI). Changes in Pc-bpi expression, as monitored by quantitative PCR (qPCR), occurred in two immune-related organs, namely the anterior kidney and the gills, after exposure at 18 and 25 °C, respectively. Histological analyses revealed the presence of the nematode in the snail anterior kidney and the gills at both 18 and 25 °C. The mantle and the central nervous system had a stable Pc-bpi expression and seemed not affected by the nematodes. Fluorescence in situ hybridization (FISH) experiments demonstrated the expression of Pc-bpi in circulating hemocytes, nurturing the possibility that increased Pc-bpi expression in the anterior kidney and gills may be due to the hemocytes patrolling the organs. While suggesting that P. hermaphrodita-based biopesticides enable the sustainable control of P. canaliculata spread, our experiments also unveiled an organ-specific and temperature-dependent response in the snails exposed to the nematodes. Overall, our data indicate that, after exposure to a pathogen, the snail P. canaliculata can mount a complex, multi-organ innate immune response. Full article

(This article belongs to the Special Issue Ancient Immunity. Phylogenetic Emergence of Recognition-Defence Mechanisms)

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13 pages, 1856 KiB

Open AccessArticle

Insights into the Complement System of Tunicates: C3a/C5aR of the Colonial Ascidian Botryllus schlosseri

by Anna Peronato, Nicola Franchi and Loriano Ballarin

Biology 2020, 9(9), 263; https://doi.org/10.3390/biology9090263 - 1 Sep 2020

Cited by 6 | Viewed by 2984

Abstract

As an evolutionary ancient component of the metazoan immune defense toolkit, the complement system can modulate cells and humoral responses of both innate and (in jawed vertebrates) adaptive immunity. All the three known complement-activation pathways converge on the cleavage of C3 to C3a [...] Read more.

As an evolutionary ancient component of the metazoan immune defense toolkit, the complement system can modulate cells and humoral responses of both innate and (in jawed vertebrates) adaptive immunity. All the three known complement-activation pathways converge on the cleavage of C3 to C3a and C3b. The anaphylatoxin C3a behaves as a chemokine in inflammatory responses, whereas C3b exerts an opsonic role and, ultimately, can activate the lytic pathway. C3aR, one of the mammalian receptors for C3a, is a member of the G-protein-coupled receptor family sharing seven transmembrane alpha helixes. C3aR can act as a chemokine and recruit neutrophils, triggering degranulation and respiratory burst, which initiates an inflammatory reaction. Mining the transcriptome of the colonial ascidian Botryllus schlosseri, we identified a transcript showing homology with both mammalian C3aR and C5aR. The gene (bsc3/c5ar) is actively transcribed in morula cells, the circulating immunocyte triggering the inflammatory reactions in response to the recognition of nonself. Its transcription is modulated during the recurrent cycles of asexual reproduction known as blastogenetic cycles. Moreover, the treatment of hemocytes with C3aR agonist, induces a significant increase in the transcription of BsC3, revealing the presence of an autocrine feedback system able to modulate the expression of C3 in order to obtain a rapid clearance of potentially dangerous nonself cells or particles. The obtained results support the previously proposed role of complement as one of the main humoral components of the immune response in tunicates and stress the importance of morula cells in botryllid ascidian innate immunity. Full article

(This article belongs to the Special Issue Ancient Immunity. Phylogenetic Emergence of Recognition-Defence Mechanisms)

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Review

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18 pages, 3595 KiB

Open AccessReview

On Origin and Evolution of the Antibody Molecule

by Umberto Oreste, Alessia Ametrano and Maria Rosaria Coscia

Biology 2021, 10(2), 140; https://doi.org/10.3390/biology10020140 - 10 Feb 2021

Cited by 17 | Viewed by 5557

Abstract

The vertebrate immune system provides a powerful defense because of the ability to potentially recognize an unlimited number of pathogens. The antibody molecule, also termed immunoglobulin (Ig) is one of the major mediators of the immune response. It is built up from two [...] Read more.

The vertebrate immune system provides a powerful defense because of the ability to potentially recognize an unlimited number of pathogens. The antibody molecule, also termed immunoglobulin (Ig) is one of the major mediators of the immune response. It is built up from two types of Ig domains: the variable domain, which provides the capability to recognize and bind a potentially infinite range of foreign substances, and the constant domains, which exert the effector functions. In the last 20 years, advances in our understanding of the molecular mechanisms and structural features of antibody in mammals and in a variety of other organisms have uncovered the underlying principles and complexity of this fundamental molecule. One notable evolutionary topic is the origin and evolution of antibody. Many aspects have been clearly stated, but some others remain limited or obscure. By considering a wide range of prokaryotic and eukaryotic organisms through a literature survey about the topic, we have provided an integrated view of the emergence of antibodies in evolution and underlined the very ancient origins. Full article

(This article belongs to the Special Issue Ancient Immunity. Phylogenetic Emergence of Recognition-Defence Mechanisms)

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14 pages, 1307 KiB

Open AccessReview

Allograft Inflammatory Factor-1 in Metazoans: Focus on Invertebrates

by Jacopo Vizioli, Tiziano Verri and Patrizia Pagliara

Biology 2020, 9(11), 355; https://doi.org/10.3390/biology9110355 - 24 Oct 2020

Cited by 11 | Viewed by 2958

Abstract

Allograft inflammatory factor-1 (AIF-1) is a calcium-binding scaffold/adaptor protein often associated with inflammatory diseases. Originally cloned from active macrophages in humans and rats, this gene has also been identified in other vertebrates and in several invertebrate species. Among metazoans, AIF-1 protein sequences remain [...] Read more.

Allograft inflammatory factor-1 (AIF-1) is a calcium-binding scaffold/adaptor protein often associated with inflammatory diseases. Originally cloned from active macrophages in humans and rats, this gene has also been identified in other vertebrates and in several invertebrate species. Among metazoans, AIF-1 protein sequences remain relatively highly conserved. Generally, the highest expression levels of AIF-1 are observed in immunocytes, suggesting that it plays a key role in immunity. In mammals, the expression of AIF-1 has been reported in different cell types such as activated macrophages, microglial cells, and dendritic cells. Its main immunomodulatory role during the inflammatory response has been highlighted. Among invertebrates, AIF-1 is involved in innate immunity, being in many cases upregulated in response to biotic and physical challenges. AIF-1 transcripts result ubiquitously expressed in all examined tissues from invertebrates, suggesting its participation in a variety of biological processes, but its role remains largely unknown. This review aims to present current knowledge on the role and modulation of AIF-1 and to highlight its function along the evolutionary scale. Full article

(This article belongs to the Special Issue Ancient Immunity. Phylogenetic Emergence of Recognition-Defence Mechanisms)

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22 pages, 2988 KiB

Open AccessReview

Nanomaterials and Annelid Immunity: A Comparative Survey to Reveal the Common Stress and Defense Responses of Two Sentinel Species to Nanomaterials in the Environment

by Kornélia Bodó, Nicoló Baranzini, Rossana Girardello, Bohdana Kokhanyuk, Péter Németh, Yuya Hayashi, Annalisa Grimaldi and Péter Engelmann

Biology 2020, 9(10), 307; https://doi.org/10.3390/biology9100307 - 23 Sep 2020

Cited by 11 | Viewed by 4318

Abstract

Earthworms and leeches are sentinel animals that represent the annelid phylum within terrestrial and freshwater ecosystems, respectively. One early stress signal in these organisms is related to innate immunity, but how nanomaterials affect it is poorly characterized. In this survey, we compare the [...] Read more.

Earthworms and leeches are sentinel animals that represent the annelid phylum within terrestrial and freshwater ecosystems, respectively. One early stress signal in these organisms is related to innate immunity, but how nanomaterials affect it is poorly characterized. In this survey, we compare the latest literature on earthworm and leeches with examples of their molecular/cellular responses to inorganic (silver nanoparticles) and organic (carbon nanotubes) nanomaterials. A special focus is placed on the role of annelid immunocytes in the evolutionarily conserved antioxidant and immune mechanisms and protein corona formation and probable endocytosis pathways involved in nanomaterial uptake. Our summary helps to realize why these environmental sentinels are beneficial to study the potential detrimental effects of nanomaterials. Full article

(This article belongs to the Special Issue Ancient Immunity. Phylogenetic Emergence of Recognition-Defence Mechanisms)

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26 pages, 5277 KiB

Open AccessReview

Cnidarian Immunity and the Repertoire of Defense Mechanisms in Anthozoans

by Maria Giovanna Parisi, Daniela Parrinello, Loredana Stabili and Matteo Cammarata

Biology 2020, 9(9), 283; https://doi.org/10.3390/biology9090283 - 11 Sep 2020

Cited by 32 | Viewed by 6591

Abstract

Anthozoa is the most specious class of the phylum Cnidaria that is phylogenetically basal within the Metazoa. It is an interesting group for studying the evolution of mutualisms and immunity, for despite their morphological simplicity, Anthozoans are unexpectedly immunologically complex, with large genomes [...] Read more.

Anthozoa is the most specious class of the phylum Cnidaria that is phylogenetically basal within the Metazoa. It is an interesting group for studying the evolution of mutualisms and immunity, for despite their morphological simplicity, Anthozoans are unexpectedly immunologically complex, with large genomes and gene families similar to those of the Bilateria. Evidence indicates that the Anthozoan innate immune system is not only involved in the disruption of harmful microorganisms, but is also crucial in structuring tissue-associated microbial communities that are essential components of the cnidarian holobiont and useful to the animal’s health for several functions including metabolism, immune defense, development, and behavior. Here, we report on the current state of the art of Anthozoan immunity. Like other invertebrates, Anthozoans possess immune mechanisms based on self/non-self-recognition. Although lacking adaptive immunity, they use a diverse repertoire of immune receptor signaling pathways (PRRs) to recognize a broad array of conserved microorganism-associated molecular patterns (MAMP). The intracellular signaling cascades lead to gene transcription up to endpoints of release of molecules that kill the pathogens, defend the self by maintaining homeostasis, and modulate the wound repair process. The cells play a fundamental role in immunity, as they display phagocytic activities and secrete mucus, which acts as a physicochemical barrier preventing or slowing down the proliferation of potential invaders. Finally, we describe the current state of knowledge of some immune effectors in Anthozoan species, including the potential role of toxins and the inflammatory response in the Mediterranean Anthozoan Anemonia viridis following injection of various foreign particles differing in type and dimensions, including pathogenetic bacteria. Full article

(This article belongs to the Special Issue Ancient Immunity. Phylogenetic Emergence of Recognition-Defence Mechanisms)

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14 pages, 833 KiB

Open AccessEditor’s ChoiceReview

Conservation of Cell Communication Systems in Invertebrate Host–Defence Mechanisms: Possible Role in Immunity and Disease

by Manon Auguste, Teresa Balbi, Caterina Ciacci and Laura Canesi

Biology 2020, 9(8), 234; https://doi.org/10.3390/biology9080234 - 18 Aug 2020

Cited by 21 | Viewed by 3794

Abstract

Innate immunity is continuously revealing multiple and highly conserved host–defence mechanisms. Studies on mammalian immunocytes are showing different communication systems that may play a role in coordinating innate immune responses also in invertebrates. Extracellular traps (ETs) are an immune response by which cells [...] Read more.

Innate immunity is continuously revealing multiple and highly conserved host–defence mechanisms. Studies on mammalian immunocytes are showing different communication systems that may play a role in coordinating innate immune responses also in invertebrates. Extracellular traps (ETs) are an immune response by which cells release net-like material, including DNA, histones and proteins. ETs are thought to immobilise and kill microorganisms, but are also involved in inflammation and autoimmune disease. Immune cells are also known to communicate through extracellular vesicles secreted in the extracellular environment or exosomes, which can carry a variety of different signalling molecules. Tunnelling nanotubes (TNTs) represent a direct cell-to-cell communication over a long distance, that allow for bi- or uni-directional transfer of cellular components between cells. Their functional role in a number of physio-pathological processes, including immune responses and pathogen transfer, has been underlined. Although ETs, exosomes, and TNTs have been described in invertebrate species, their possible role in immune responses is not fully understood. In this work, available data on these communication systems are summarised, in an attempt to provide basic information for further studies on their relevance in invertebrate immunity and disease. Full article

(This article belongs to the Special Issue Ancient Immunity. Phylogenetic Emergence of Recognition-Defence Mechanisms)

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13 pages, 1025 KiB

Open AccessReview

Evolution of Allorecognition in the Tunicata

by Marie L. Nydam

Biology 2020, 9(6), 129; https://doi.org/10.3390/biology9060129 - 16 Jun 2020

Cited by 5 | Viewed by 3744

Abstract

Allorecognition, the ability to distinguish self or kin from unrelated conspecifics, plays several important biological roles in invertebrate animals. Two of these roles include negotiating limited benthic space for colonial invertebrates, and inbreeding avoidance through self-incompatibility systems. Subphylum Tunicata (Phylum Chordata), the sister [...] Read more.

Allorecognition, the ability to distinguish self or kin from unrelated conspecifics, plays several important biological roles in invertebrate animals. Two of these roles include negotiating limited benthic space for colonial invertebrates, and inbreeding avoidance through self-incompatibility systems. Subphylum Tunicata (Phylum Chordata), the sister group to the vertebrates, is a promising group in which to study allorecognition. Coloniality has evolved many times independently in the tunicates, and the best known invertebrate self-incompatibility systems are in tunicates. Recent phylogenomic studies have coalesced around a phylogeny of the Tunicata as well as the Order Stolidobranchia within the Tunicata, providing a path forward for the study of allorecognition in this group. Full article

(This article belongs to the Special Issue Ancient Immunity. Phylogenetic Emergence of Recognition-Defence Mechanisms)

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