Soluble mediators of innate immunity in annelids and bivalve mollusks: A mini-review

. 2022 ; 13 () : 1051155. [epub] 20221202

Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, přehledy, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid36532070

Annelids and mollusks, both in the superphylum of Lophotrochozoa (Bilateria), are important ecological groups, widespread in soil, freshwater, estuarine, and marine ecosystems. Like all invertebrates, they lack adaptive immunity; however, they are endowed with an effective and complex innate immune system (humoral and cellular defenses) similar to vertebrates. The lack of acquired immunity and the capacity to form antibodies does not mean a lack of specificity: invertebrates have evolved genetic mechanisms capable of producing thousands of different proteins from a small number of genes, providing high variability and diversity of immune effector molecules just like their vertebrate counterparts. This diversity allows annelids and mollusks to recognize and eliminate a wide range of pathogens and respond to environmental stressors. Effector molecules can kill invading microbes, reduce their pathogenicity, or regulate the immune response at cellular and systemic levels. Annelids and mollusks are "typical" lophotrochozoan protostome since both groups include aquatic species with trochophore larvae, which unite both taxa in a common ancestry. Moreover, despite their extensive utilization in immunological research, no model systems are available as there are with other invertebrate groups, such as Caenorhabditis elegans or Drosophila melanogaster, and thus, their immune potential is largely unexplored. In this work, we focus on two classes of key soluble mediators of immunity, i.e., antimicrobial peptides (AMPs) and cytokines, in annelids and bivalves, which are the most studied mollusks. The mediators have been of interest from their first identification to recent advances in molecular studies that clarified their role in the immune response.

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Bilej M, Prochazkova P, Silerova M, Joskova R. Earthworm immunity. Adv Exp Med Biol (2010) 708:66–79. doi: 10.1007/978-1-4419-8059-5_4 PubMed DOI

Liebeke M, Strittmatter N, Fearn S, Morgan AJ, Kille P, Fuchser J, et al. . Unique metabolites protect earthworms against plant polyphenols. Nat Commun (2015) 6:7869. doi: 10.1038/ncomms8869 PubMed DOI PMC

Schenk S, Hoeger U. Annelid coelomic fluid proteins. In: Schenk S, Hoeger U, editors. Vertebrate and invertebrate respiratory proteins, lipoproteins and other body fluid proteins subcellular biochemistry, vol. 94 . Cham: Springer; (2020). PubMed

Prochazkova P, Roubalova R, Dvorak J, Navarro Pacheco NI, Bilej M. Pattern recognition receptors in annelids. Dev Comp Immunol (2020) 102:103493. doi: 10.1016/j.dci.2019.103493 PubMed DOI

Cho JH, Park CB, Yoon YG, Kim SC. Lumbricin I, a novel proline-rich antimicrobial peptide from the earthworm: purification, cDNA cloning and molecular characterization. Biochim Biophys Acta (1998) 1408(1):67–76. doi: 10.1016/S0925-4439(98)00058-1 PubMed DOI

Schikorski D, Cuvillier-Hot V, Leippe M, Boidin-Wichlacz C, Slomianny C, Macagno E, et al. . Microbial challenge promotes the regenerative process of the injured central nervous system of the medicinal leech by inducing the synthesis of antimicrobial peptides in neurons and microglia. J Immunol (2008) 181(2):1083–95. doi: 10.4049/jimmunol.181.2.1083 PubMed DOI PMC

Wang X, Wang X, Zhang Y, Qu X, Yang S. An antimicrobial peptide of the earthworm pheretima tschiliensis: cDNA cloning, expression and immunolocalization. Biotechnol Lett (2003) 25(16):1317–23. doi: 10.1023/A:1024999206117 PubMed DOI

Li W, Li S, Zhong J, Zhu Z, Liu J, Wang W. A novel antimicrobial peptide from skin secretions of the earthworm, pheretima guillelmi (Michaelsen). Peptides (2011) 32(6):1146–50. doi: 10.1016/j.peptides.2011.04.015 PubMed DOI

Bodo K, Boros A, Rumpler E, Molnar L, Borocz K, Nemeth P, et al. . Identification of novel lumbricin homologues in eisenia andrei earthworms. Dev Comp Immunol (2019) 90:41–6. doi: 10.1016/j.dci.2018.09.001 PubMed DOI

Tasiemski A, Vandenbulcke F, Mitta G, Lemoine J, Lefebvre C, Sautiere PE, et al. . Molecular characterization of two novel antibacterial peptides inducible upon bacterial challenge in an annelid, the leech theromyzon tessulatum. J Biol Chem (2004) 279(30):30973–82. doi: 10.1074/jbc.M312156200 PubMed DOI

Ovchinnikova TV, Aleshina GM, Balandin SV, Krasnosdembskaya AD, Markelov ML, Frolova EI, et al. . Purification and primary structure of two isoforms of arenicin, a novel antimicrobial peptide from marine polychaeta arenicola marina. FEBS Lett (2004) 577(1-2):209–14. doi: 10.1016/j.febslet.2004.10.012 PubMed DOI

Sandvang D, Kristensen HH, Neve S. Arenicin-3: A novel antimicrobial peptide showing potent in vitro activity against gram-negative multiresistant clinical isolates. Proceedings of the 46th Annual Meeting, Idsa. (2008) Washington, DC, USA. p. F1-3986.

Tasiemski A, Jung S, Boidin-Wichlacz C, Jollivet D, Cuvillier-Hot V, Pradillon F, et al. . Characterization and function of the first antibiotic isolated from a vent organism: the extremophile metazoan alvinella pompejana. PloS One (2014) 9(4):e95737. doi: 10.1074/jbc.M312156200 PubMed DOI PMC

Safronova VN, Panteleev PV, Sukhanov SV, Toropygin IY, Bolosov IA, Ovchinnikova TV. Mechanism of action and therapeutic potential of the beta-hairpin antimicrobial peptide capitellacin from the marine polychaeta capitella teleta. Mar Drugs (2022) 20(3):167. doi: 10.3390/md20030167 PubMed DOI PMC

Panteleev PV, Tsarev AV, Bolosov IA, Paramonov AS, Marggraf MB, Sychev SV, et al. . Novel antimicrobial peptides from the arctic polychaeta nicomache minor provide new molecular insight into biological role of the BRICHOS domain. Mar Drugs (2018) 16(11):401. doi: 10.3390/md16110401 PubMed DOI PMC

Tasiemski A, Schikorski D, Le Marrec-Croq F, Pontoire-Van Camp C, Boidin-Wichlacz C, Sautiere PE. Hedistin: A novel antimicrobial peptide containing bromotryptophan constitutively expressed in the NK cells-like of the marine annelid, nereis diversicolor. Dev Comp Immunol (2007) 31(8):749–62. doi: 10.1016/j.dci.2006.11.003 PubMed DOI

Pan W, Liu X, Ge F, Han J, Zheng T. Perinerin, a novel antimicrobial peptide purified from the clamworm perinereis aibuhitensis grube and its partial characterization. J Biochem (2004) 135(3):297–304. doi: 10.1093/jb/mvh036 PubMed DOI

Seo JK, Nam BH, Go HJ, Jeong M, Lee KY, Cho SM, et al. . Hemerythrin-related antimicrobial peptide, msHemerycin, purified from the body of the lugworm, marphysa sanguinea. Fish Shellfish Immunol (2016) 57:49–59. doi: 10.1016/j.fsi.2016.08.018 PubMed DOI

Jung S, Sonnichsen FD, Hung CW, Tholey A, Boidin-Wichlacz C, Haeusgen W, et al. . Macin family of antimicrobial proteins combines antimicrobial and nerve repair activities. J Biol Chem (2012) 287(17):14246–58. doi: 10.1074/jbc.M111.336495 PubMed DOI PMC

Gharibyan AL, Wasana Jayaweera S, Lehmann M, Anan I, Olofsson A. Endogenous human proteins interfering with amyloid formation. Biomolecules (2022) 12(3):446. doi: 10.3390/biom12030446 PubMed DOI PMC

Edwards IA, Elliott AG, Kavanagh AM, Zuegg J, Blaskovich MA, Cooper MA. Contribution of amphipathicity and hydrophobicity to the antimicrobial activity and cytotoxicity of beta-hairpin peptides. ACS Infect Dis (2016) 2(6):442–50. doi: 10.1021/acsinfecdis.6b00045 PubMed DOI PMC

Cooper E, Franchini A, Ottaviani E. Earthworm coelomocytes possess immunoreactive cytokines and POMC-derived peptides. Anim Biol (1995) 4(1):25–9.

Engelmann P, Pal J, Berki T, Cooper EL, Nemeth P. Earthworm leukocytes react with different mammalian antigen-specific monoclonal antibodies. Zool (Jena) (2002) 105(3):257–65. doi: 10.1078/0944-2006-00068 PubMed DOI

Beschin A, Bilej M, Torreele E, De Baetselier P. On the existence of cytokines in invertebrates. Cell Mol Life Sci (2001) 58(5-6):801–14. doi: 10.1007/PL00000901 PubMed DOI PMC

Silerova M, Prochazkova P, Joskova R, Josens G, Beschin A, De Baetselier P, et al. . Comparative study of the CCF-like pattern recognition protein in different lumbricid species. Dev Comp Immunol (2006) 30(9):765–71. doi: 10.1016/j.dci.2005.11.002 PubMed DOI

Beschin A, Bilej M, Brys L, Torreele E, Lucas R, Magez S, et al. . Convergent evolution of cytokines. Nature (1999) 400(6745):627–8. doi: 10.1038/23164 PubMed DOI

Beschin A, Bilej M, Magez S, Lucas R, De Baetselier P. Functional convergence of invertebrate and vertebrate cytokine-like molecules based on a similar lectin-like activity. Prog Mol Subcell Biol (2004) 34:145–63. doi: 10.1007/978-3-642-18670-7_6 PubMed DOI

Bilej M, Joskova R, Van den Bergh R, Prochazkova P, Silerova M, Ameloot P, et al. . An invertebrate TNF functional analogue activates macrophages via lectin-saccharide interaction with ion channels. Int Immunol (2006) 18(12):1663–70. doi: 10.1093/intimm/dxl100 PubMed DOI

De Zoysa M, Jung S, Lee J. First molluscan TNF-alpha homologue of the TNF superfamily in disk abalone: molecular characterization and expression analysis. Fish Shellfish Immunol (2009) 26(4):625–31. doi: 10.1016/j.fsi.2008.10.004 PubMed DOI

Zheng Y, Liu Z, Wang L, Li M, Zhang Y, Zong Y, et al. . A novel tumor necrosis factor in the pacific oyster crassostrea gigas mediates the antibacterial response by triggering the synthesis of lysozyme and nitric oxide. Fish Shellfish Immunol (2020) 98:334–41. doi: 10.1016/j.fsi.2019.12.073 PubMed DOI

Cao Y, Yang S, Feng C, Zhan W, Zheng Z, Wang Q, et al. . Evolution and function analysis of interleukin-17 gene from pinctada fucata martensii. Fish Shellfish Immunol (2019) 88:102–10. doi: 10.1016/j.fsi.2019.02.044 PubMed DOI

Roberts S, Gueguen Y, de Lorgeril J, Goetz F. Rapid accumulation of an interleukin 17 homolog transcript in crassostrea gigas hemocytes following bacterial exposure. Dev Comp Immunol (2008) 32(9):1099–104. doi: 10.1016/j.dci.2008.02.006 PubMed DOI

Cao W, Wang W, Fan S, Li J, Li Q, Wu S, et al. . The receptor CgIL-17R1 expressed in granulocytes mediates the CgIL-17 induced haemocytes proliferation in crassostrea gigas. Dev Comp Immunol (2022) 131:104376. doi: 10.1016/j.dci.2022.104376 PubMed DOI

Lv X, Sun J, Li Y, Yang W, Wang L, Leng J, et al. . CgIL17-5 regulates the mRNA expressions of immune effectors through inducing the phosphorylation of CgMAPKs and the nuclear translocation of CgRel and CgAP-1 in the pacific oyster crassostrea gigas. Dev Comp Immunol (2022) 127:104263. doi: 10.1016/j.dci.2021.104263 PubMed DOI

Saco A, Rey-Campos M, Rosani U, Novoa B, Figueras A. The evolution and diversity of interleukin-17 highlight an expansion in marine invertebrates and its conserved role in mucosal immunity. Front Immunol (2021) 12:692997. doi: 10.3389/fimmu.2021.692997 PubMed DOI PMC

Schorn T, Drago F, Tettamanti G, Valvassori R, de Eguileor M, Vizioli J, et al. . Homolog of allograft inflammatory factor-1 induces macrophage migration during innate immune response in leech. Cell Tissue Res (2015) 359(3):853–64. doi: 10.1007/s00441-014-2058-7 PubMed DOI

Zhang Y, Li J, Yu F, He X, Yu Z. Allograft inflammatory factor-1 stimulates hemocyte immune activation by enhancing phagocytosis and expression of inflammatory cytokines in crassostrea gigas. Fish Shellfish Immunol (2013) 34(5):1071–7. doi: 10.1016/j.fsi.2013.01.014 PubMed DOI

Parisi MG, Toubiana M, Mangano V, Parrinello N, Cammarata M, Roch P. MIF from mussel: coding sequence, phylogeny, polymorphism, 3D model and regulation of expression. Dev Comp Immunol (2012) 36(4):688–96. doi: 10.1016/j.dci.2011.10.014 PubMed DOI

Li F, Huang S, Wang L, Yang J, Zhang H, Qiu L, et al. . A macrophage migration inhibitory factor like gene from scallop chlamys farreri: Involvement in immune response and wound healing. Dev Comp Immunol (2011) 35(1):62–71. doi: 10.1016/j.dci.2010.08.009 PubMed DOI

Cui S, Zhang D, Jiang S, Pu H, Hu Y, Guo H, et al. . A macrophage migration inhibitory factor like oxidoreductase from pearl oyster pinctada fucata involved in innate immune responses. Fish Shellfish Immunol (2011) 31(2):173–81. doi: 10.1016/j.fsi.2011.03.009 PubMed DOI

Qiao X, Zong Y, Liu Z, Wu Z, Li Y, Wang L, et al. . The cGAS/STING-TBK1-IRF regulatory axis orchestrates a primitive interferon-like antiviral mechanism in oyster. Front Immunol (2021) 12:689783. doi: 10.3389/fimmu.2021.689783 PubMed DOI PMC

Zhang R, Liu R, Wang W, Xin L, Wang L, Li C, et al. . Identification and functional analysis of a novel IFN-like protein (CgIFNLP) in crassostrea gigas. Fish Shellfish Immunol (2015) 44(2):547–54. doi: 10.1016/j.fsi.2015.03.015 PubMed DOI

Zhang R, Liu R, Xin L, Chen H, Li C, Wang L, et al. . A CgIFNLP receptor from crassostrea gigas and its activation of the related genes in human JAK/STAT signaling pathway. Dev Comp Immunol (2016) 65:98–106. doi: 10.1016/j.dci.2016.06.010 PubMed DOI

Qiao X, Wang L, Song L. The primitive interferon-like system and its antiviral function in molluscs. Dev Comp Immunol (2021) 118:103997. doi: 10.1016/j.dci.2021.103997 PubMed DOI

Yang Y, Qiao X, Song X, Zhang D, Yu S, Dong M, et al. . CgATP synthase beta subunit involved in the regulation of haemocytes proliferation as a CgAstakine receptor in crassostrea gigas. Fish Shellfish Immunol (2022) 123:85–93. doi: 10.1016/j.fsi.2022.02.054 PubMed DOI

Schikorski D, Cuvillier-Hot V, Boidin-Wichlacz C, Slomianny C, Salzet M, Tasiemski A. Deciphering the immune function and regulation by a TLR of the cytokine EMAPII in the lesioned central nervous system using a leech model. J Immunol (2009) 183(11):7119–28. doi: 10.4049/jimmunol.0900538 PubMed DOI

Pacheco NIN, Roubalova R, Dvorak J, Benada O, Pinkas D, Kofronova O, et al. . Understanding the toxicity mechanism of CuO nanoparticles: the intracellular view of exposed earthworm cells. Environ Science-Nano (2021) 8(9):2464–77. doi: 10.1039/D1EN00080B DOI

Shalak V, Kaminska M, Mitnacht-Kraus R, Vandenabeele P, Clauss M, Mirande M. The EMAPII cytokine is released from the mammalian multisynthetase complex after cleavage of its p43/proEMAPII component. J Biol Chem (2001) 276(26):23769–76. doi: 10.1074/jbc.M100489200 PubMed DOI

Knies UE, Behrensdorf HA, Mitchell CA, Deutsch U, Risau W, Drexler HC, et al. . Regulation of endothelial monocyte-activating polypeptide II release by apoptosis. Proc Natl Acad Sci USA (1998) 95(21):12322–7. doi: 10.1073/pnas.95.21.12322 PubMed DOI PMC

Prochazkova P, Roubalova R, Skanta F, Dvorak J, Pacheco NIN, Kolarik M, et al. . Developmental and immune role of a novel multiple cysteine cluster TLR from eisenia andrei earthworms. Front Immunol (2019) 10:1277. doi: 10.3389/fimmu.2019.01277 PubMed DOI PMC

Cua DJ, Tato CM. Innate IL-17-producing cells: the sentinels of the immune system. Nat Rev Immunol (2010) 10(7):479–89. doi: 10.1038/nri2800 PubMed DOI

Hernadi SB. Earthworm system immunity and its modulation by nanoparticles. Cardiff: Cardiff University; (2020).

Canesi L, Pruzzo C. Specificity of innate immunity in bivalves: A lesson from bacteria. In: Ballarin L, Cammarata M, editors. Lessons in immunity: from single-cell organisms to mammals. London, UK: Academic Press, Elsevier Inc; (2016).

Gerdol M, Gomez-Chiari M, Castillo MG, Figueras A, Fiorito G, Moreira R, et al. . Immunity in molluscs: recognition and effector mechanisms, with a focus on bivalvia. In: Cooper E, editor. Advances in comparative immunology. Cham, Switzerland: Springer; (2018). p. 225–342.

Hubert F, Noel T, Roch P. A member of the arthropod defensin family from edible Mediterranean mussels (Mytilus galloprovincialis). Eur J Biochem (1996) 240(1):302–6. doi: 10.1111/j.1432-1033.1996.0302h.x PubMed DOI

Figueras A, Moreira R, Sendra M, Novoa B. Genomics and immunity of the Mediterranean mussel mytilus galloprovincialis in a changing environment. Fish Shellfish Immunol (2019) 90:440–5. doi: 10.1016/j.fsi.2019.04.064 PubMed DOI

Zannella C, Mosca F, Mariani F, Franci G, Folliero V, Galdiero M, et al. . Microbial diseases of bivalve mollusks: infections, immunology and antimicrobial defense. Mar Drugs (2017) 15(6):182. doi: 10.3390/md15060182 PubMed DOI PMC

Gerdol M, Moreira R, Cruz F, Gomez-Garrido J, Vlasova A, Rosani U, et al. . Massive gene presence-absence variation shapes an open pan-genome in the Mediterranean mussel. Genome Biol (2020) 21(1):275. doi: 10.1186/s13059-020-02180-3 PubMed DOI PMC

Balseiro P, Falco A, Romero A, Dios S, Martinez-Lopez A, Figueras A, et al. . Mytilus galloprovincialis myticin c: a chemotactic molecule with antiviral activity and immunoregulatory properties. PloS One (2011) 6(8):e23140. doi: 10.1371/journal.pone.0023140 PubMed DOI PMC

Rey-Campos M, Moreira R, Romero A, Medina-Gali RM, Novoa B, Gasset M, et al. . Transcriptomic analysis reveals the wound healing activity of mussel myticin c. Biomolecules (2020) 10(1):133. doi: 10.3390/biom10010133 PubMed DOI PMC

Gerdol M, Schmitt P, Venier P, Rocha G, Rosa RD, Destoumieux-Garzon D. Functional insights from the evolutionary diversification of big defensins. Front Immunol (2020) 11:758. doi: 10.3389/fimmu.2020.00758 PubMed DOI PMC

Loth K, Vergnes A, Barreto C, Voisin SN, Meudal H, Da Silva J, et al. . The ancestral n-terminal domain of big defensins drives bacterially triggered assembly into antimicrobial nanonets. mBio (2019) 10(5):e01821–19. doi: 10.1128/mBio.01821-19 PubMed DOI PMC

Ouellette AJ, Selsted ME. Immunology. HD6 defensin nanonets. Science (2012) 337(6093):420–1. doi: 10.1126/science.1225906 PubMed DOI

Stambuk F, Ojeda C, Machado Matos G, Rosa RD, Mercado L, Schmitt P. Big defensin from the scallop argopecten purpuratus ApBD1 is an antimicrobial peptide which entraps bacteria through nanonets formation. Fish Shellfish Immunol (2021) 119:456–61. doi: 10.1016/j.fsi.2021.10.037 PubMed DOI

Oh R, Lee MJ, Kim YO, Nam BH, Kong HJ, Kim JW, et al. . Myticusin-beta, antimicrobial peptide from the marine bivalve, mytilus coruscus. Fish Shellfish Immunol (2020) 99:342–52. doi: 10.1016/j.fsi.2020.02.020 PubMed DOI

Pacor S, Benincasa M, Musso MV, Krce L, Aviani I, Pallavicini A, et al. . The proline-rich myticalins from mytilus galloprovincialis display a membrane-permeabilizing antimicrobial mode of action. Peptides (2021) 143:170594. doi: 10.1016/j.peptides.2021.170594 PubMed DOI

Zheng X, Yuan C, Zhang Y, Zha S, Mao F, Bao Y. Prediction and characterization of a novel hemoglobin-derived mutant peptide (mTgHbP7) from tegillarca granosa. Fish Shellfish Immunol (2022) 125:84–9. doi: 10.1016/j.fsi.2022.05.007 PubMed DOI

Zhang G, Fang X, Guo X, Li L, Luo R, Xu F, et al. . The oyster genome reveals stress adaptation and complexity of shell formation. Nature (2012) 490(7418):49–54. doi: 10.1038/nature11413 PubMed DOI

Hughes TK, Smith EM, Leung MK, Stefano GB. Immunoreactive cytokines in mytilus edulis nervous and immune interactions. Acta Biol Hung (1992) 43(1-4):269–73. PubMed

Ottaviani E, Franchini A. Immune and neuroendocrine responses in molluscs: the role of cytokines. Acta Biol Hung (1995) 46(2-4):341–9. PubMed

Ottaviani E, Malagoli D, Franchini A. Invertebrate humoral factors: cytokines as mediators of cell survival. Prog Mol Subcell Biol (2004) 34:1–25. doi: 10.1007/978-3-642-18670-7_1 PubMed DOI

Beschin A, Muller WEG. Invertebrate cytokines and the phylogeny of immunity: facts and paradoxes. Berlin Heidelberg New York: Springer-Verlag; (2004).

Betti M, Ciacci C, Lorusso LC, Canonico B, Falcioni T, Gallo G, et al. . Effects of tumour necrosis factor alpha (TNFalpha) on mytilus haemocytes: role of stress-activated mitogen-activated protein kinases (MAPKs). Biol Cell (2006) 98(4):233–44. doi: 10.1042/BC20050049 PubMed DOI

Herpin A, Lelong C, Favrel P. Transforming growth factor-beta-related proteins: an ancestral and widespread superfamily of cytokines in metazoans. Dev Comp Immunol (2004) 28(5):461–85. doi: 10.1016/j.dci.2003.09.007 PubMed DOI

Wu SZ, Huang XD, Li Q, He MX. Interleukin-17 in pearl oyster (Pinctada fucata): molecular cloning and functional characterization. Fish Shellfish Immunol (2013) 34(5):1050–6. doi: 10.1016/j.fsi.2013.01.005 PubMed DOI

Canesi L, Betti M, Ciacci C, Citterio B, Pruzzo C, Gallo G. Tyrosine kinase-mediated cell signalling in the activation of mytilus hemocytes: possible role of STAT-like proteins. Biol Cell (2003) 95(9):603–13. doi: 10.1016/j.biolcel.2003.09.006 PubMed DOI

Balbi T, Auguste M, Ciacci C, Canesi L. Immunological responses of marine bivalves to contaminant exposure: contribution of the -omics approach. Front Immunol (2021) 12:618726. doi: 10.3389/fimmu.2021.618726 PubMed DOI PMC

Han Z, Li J, Wang W, Li J, Zhao Q, Li M, et al. . A calmodulin targeted by miRNA scaffold659_26519 regulates IL-17 expression in the early immune response of oyster crassostrea gigas. Dev Comp Immunol (2021) 124:104180. doi: 10.1016/j.dci.2021.104180 PubMed DOI

Chen H, Zhou Z, Wang H, Wang L, Wang W, Liu R, et al. . An invertebrate-specific and immune-responsive microRNA augments oyster haemocyte phagocytosis by targeting CgIkappaB2. Sci Rep (2016) 6:29591. doi: 10.1038/srep29591 PubMed DOI PMC

Rodriguez-Rojas A, Makarova O, Rolff J. Antimicrobials, stress and mutagenesis. PloS Pathog (2014) 10(10):e1004445. doi: 10.1371/journal.ppat.1004445 PubMed DOI PMC

Kumar P, Kizhakkedathu JN, Straus SK. Antimicrobial peptides: Diversity, mechanism of action and strategies to improve the activity and biocompatibility In vivo . Biomolecules (2018) 8(1):4. doi: 10.3390/biom8010004 PubMed DOI PMC

Elliott AG, Huang JX, Neve S, Zuegg J, Edwards IA, Cain AK, et al. . An amphipathic peptide with antibiotic activity against multidrug-resistant gram-negative bacteria. Nat Commun (2020) 11(1):3184. doi: 10.1038/s41467-020-16950-x PubMed DOI PMC

Abdualkader AM, Ghawi AM, Alaama M, Awang M, Merzouk A. Leech therapeutic applications. Indian J Pharm Sci (2013) 75(2):127–37. PubMed PMC

Markwardt F. Past, present and future of hirudin. Haemostasis (1991) 21 Suppl 1:11–26. doi: 10.1159/000216258 PubMed DOI

Fernandez Robledo JA, Yadavalli R, Allam B, Pales Espinosa E, Gerdol M, Greco S, et al. . From the raw bar to the bench: Bivalves as models for human health. Dev Comp Immunol (2019) 92:260–82. doi: 10.1016/j.dci.2018.11.020 PubMed DOI PMC

Wei D, Zhang X. Biosynthesis, bioactivity, biotoxicity and applications of antimicrobialpeptides for human health. Biosafety Health (2022) 4:118–34. doi: 10.1016/j.bsheal.2022.02.003 DOI

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