Abstract
In the present chapter, we will emphasize the immune response in two compartments (Central nervous system and peripheral system) in two blood sucking leeches i.e., the medicinal leech and the bird leech Theromyzon tessulatum. In the medicinal leech, the neuroimmune response has been described in the context of septic trauma at the cellular and humoral levels through microglia, Toll-like, cannabinoids and chemoattractant factors activation and modulation. In the bird leech, the antimicrobial responses have been dissected at the cellular and molecular levels. Altogether, this chapter presents a complete integrate immune response from the brain and the systemic compartments with high similarity to the vertebrates one. These points that the neuroimmune and immune responses evolved sooner than can be expected.
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References
Bely AE, Weisblat DA. Lessons from leeches: a call for DNA barcoding in the lab. Evol Dev 2006; 8(6):491–501.
Borda E, Siddall ME. Arhynchobdellida (Annelida: Oligochaeta: Hirudinida): phylogenetic relationships and evolution. Mol Phylogenet Evol 2004; 30(1):213–225.
Kaigorodova IA, Shcherbakov D. [Molecular phylogenetic study of the systematic position of Baikalian oligochaetes in the system Clitellata]. Genetika 2006; 42(12): 1647–1655.
McDougall C, Hui JH, Monteiro A et al. Annelids in evolutionary developmental biology and comparative genomics. Parasite 2008; 15(3):321–328.
Pfeiffer I, Brenig B, Kutschera U. Molecular phylogeny of selected predaceous leeches with reference to the evolution of body size and terrestrialism. Theory Biosci 2005; 124(1):55–64.
Utevsky SY, Trontelj P. A new species of the medicinal leech (Oligochaeta, Hirudinida, Hirudo) from Transcaucasia and an identification key for the genus Hirudo. Parasitol Res 2005; 98(1):61–66.
Trontelj P, Utevsky SY. Celebrity with a neglected taxonomy: molecular systematics of the medicinal leech (genus Hirudo). Mol Phylogenet Evol 2005; 34(3):616–624.
Macagno ERGTE L, Bafna V, Soares MB et al. Construction of a medicinal leech transcriptome database and its application to the identification of leech homologs of neural and innate immune genes. BMC Genomics 2010; In press.
Salzet M, Capron A, Stefano GB. Molecular crosstalk in host-parasite relationships: schistosome-and leech-host interactions. Parasitol Today 2000; 16(12):536–540.
Macagno ER. Number and distribution of neurons in leech segmental ganglia. J Comp Neurol 1980; 190(2):283–302.
Sawyer RT. Leech biology and behaviour. Clarendon Press, Oxford, England 1986; I, II, III.
Nicholls JG, Hernandez UG. Growth and synapse formation by identified leech neurones in culture: a review. Q J Exp Physiol 1989; 74(7):965–973.
McGlade-McCulloh E, Morrissey AM, Norona F et al. Individual microglia move rapidly and directly to nerve lesions in the leech central nervous system. Proc Natl Acad Sci USA 1989; 86(3): 1093–1097.
Shafer OT, Chen A, Kumar SM et al. Injury-induced expression of endothelial nitric oxide synthase by glial and microglial cells in the leech central nervous system within minutes after injury. Proc Biol Sci 1998;265(1411):2171–2175.
Chen A, Kumar SM, Sahley CL et al. Nitric oxide influences injury-induced microglial migration and accumulation in the leech CNS. J Neurosci 2000; 20(3):1036–1043.
Arafah K, Desmons A, Vizioli J et al. Crosstalk between the CB2-like receptor and nitric oxide systems in the injured leech brain: involvement of the endocannabinoid 2AG in microglia recruitment at the injured site. J Neurosci 2010; Submitted.
Lipitz JB, Arafah K, Zhou X et al. Cannabinoid control of microglia migration to lesions in the leech CNS. J Neurosci 2010; Submitted.
Raborn ES, Marciano-Cabral F, Buckley NE et al. The cannabinoid delta-9-tetrahydrocannabinol mediates inhibition of macrophage chemotaxis to RANTES/CCL5: linkage to the CB2 receptor. J Neuroimmune Pharmacol 2008; 3(2):117–129.
Vannacci A, Giannini L, Passani MB et al. The endocannabinoid 2-arachidonylglycerol decreases the immunological activation of Guinea pig mast cells: involvement of nitric oxide and eicosanoids. J Pharmacol Exp Ther 2004; 311(1):256–264.
Cabrai GA, Marciano-Cabral F. Cannabinoid receptors in microglia of the central nervous system: immune functional relevance. J Leukoc Biol 2005; 78(6): 1192–1197.
Walter L, Neumann H. Role of microglia in neuronal degeneration and regeneration. Semin Immunopathol 2009;31(4):513–525.
Salzet M, Breton C, Bisogno T et al. Comparative biology of the endocannabinoid system possible role in the immune response. Eur J Biochem 2000; 267(16):4917–4927.
Ehrhart J, Obregon D, Mori T et al. Stimulation of cannabinoid receptor 2 (CB2) suppresses microglial activation. J Neuroinflammation 2005; 2:29.
Xu Y, Bolton B, Zipser B et al. Gliarin and macrolin, two novel intermediate filament proteins specifically expressed in sets and subsets of glial cells in leech central nervous system. J Neurobiol 1999; 40(2):244–253.
Vergote D, Sautiere PE, Vandenbulcke F et al. Up-regulation of neurohemerythrin expression in the central nervous system of the medicinal leech, Hirudo medicinalis, following septic injury. J Biol Chem 2004; 279(42):43828–43837.
Vergote D, Macagno ER, Salzet M et al. Proteome modifications of the medicinal leech nervous system under bacterial challenge. Proteomics 2006; 6(17):4817–4825.
Morgese VJ, Elliott EJ, Muller KJ. Microglial movement to sites of nerve lesion in the leech CNS. Brain Res 1983; 272(1):166–170.
Deloffre L, Salzet B, Vieau D et al. Antibacterial properties of hemerythrin of the sand worm Nereis diversicolor. Neuro Endocrinol Lett 2003; 24(1–2):39–45.
Lefebvre C, Salzet M. Annelid neuroimmune system. Curr Pharm Des 2003; 9(2):149–158.
Lefebvre C, Vandenbulcke F, Bocquet B et al. Cathepsin L and cystatin B gene expression discriminates immune coelomic cells in the leech Theromyzon tessulatum. Dev Comp Immunol 2008; 32(7):795–807.
Blackshaw SE, Babington EJ, Emes RD et al. Identifying genes for neuron survival and axon outgrowth in Hirudo medicinalis. J Anat 2004; 204(1): 13–24.
Perlson E, Medzihradszky KF, Darula Z et al. Differential proteomics reveals multiple components in retrogradely transported axoplasm after nerve injury. Mol Cell Proteomics 2004; 3(5):510–520.
Matias I, Bisogno T, Melck D et al. Evidence for an endocannabinoid system in the central nervous system of the leech Hirudo medicinalis. Brain Res Mol Brain Res 2001; 87(2):145–159.
Stefano GB, Rialas CM, Deutsch DG et al. Anandamide amidase inhibition enhances anandamide-stimulated nitric oxide release in invertebrate neural tissues. Brain Res 1998; 793(1–2):341–345.
Stefano GB, Salzet B, Rialas CM et al. Morphine-and anandamide-stimulated nitric oxide production inhibits presynaptic dopamine release. Brain Res 1997; 763(1):63–68.
Stefano GB, Salzet B, Salzet M. Identification and characterization of the leech CNS cannabinoid receptor: coupling to nitric oxide release. Brain Res 1997; 753(2):219–224.
Schikorski D, Cuvillier-Hot V, Leippe M 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): 1083–1095.
Nagao S, Tanaka A, Onozaki K et al. Differences betweenmacrophage migration inhibitions by lymphokines and muramyl dipeptide (MDP) or lipopolysaccharide (LPS): migration enhancement by lymphokines. Cell Immunol 1982; 71(1):1–11.
Fukuyama R, Takeda H, Fushiki S et al. Muramyl dipeptide injected into crushed sciatic nerve, activates macrophages and promotes recovery of walking locomotion in rats. Restor Neurol Neurosci 1998; 13(3–4):213–219.
Schikorski D, Cuvillier-Hot V, Boidin-Wichlacz C et al. 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):7119–7128.
Denes AS, Jekely G, Steinmetz PR et al. Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell 2007; 129(2):277–288.
Hui JH, Raible F, Korchagina N et al. Features of the ancestral bilaterian inferred from Platynereis dumerilii ParaHox genes. BMC Biol 2009; 7:43.
Raible F, Tessmar-Raible K, Osoegawa K et al. Vertebrate-type intron-rich genes in the marine annelid Platynereis dumerilii. Science 2005; 310 (5752):1325–1326.
Tasiemski A, Vandenbulcke F, Mitta G 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):30973–30982.
Tasiemski A, Verger-Bocquet M, Cadet M et al. Proenkephalin A-derived peptides in invertebrate innate immune processes. Brain Res Mol Brain Res 2000; 76(2):237–252.
Levy F, Bulet P, Ehret-Sabatier L. Proteomic analysis of the systemic immune response of Drosophila. Mol Cell Proteomics 2004; 3(2):156–166.
Brogden KA, Ackermann M, Huttner KM. Detection of anionic antimicrobial peptides in ovine bronchoalveolar lavage fluid and respiratory epithelium. Infect Immun 1998; 66(12):5948–5954.
Melino S, Rufini S, Sette M et al. Zn(2+) ions selectively induce antimicrobial salivary peptide histatin-5 to fuse negatively charged vesicles. Identification and characterization of a zinc-binding motif present in the functional domain. Biochemistry 1999; 38(30):9626–9633.
Brewer D, Lajoie G. Evaluation of the metal binding properties of the histidine-rich antimicrobial peptides histatin 3 and 5 by electrospray ionization mass spectrometry. Rapid Commun Mass Spectrom 2000; 14(19):1736–1745.
Hoffmann JA. The immune response of Drosophila. Nature 2003; 426(6962):33–38.
Baert JL, Britel M, Slomianny MC et al. Yolkprotein in leech. Identification, purification and characterization of vitellin and vitellogenin. Eur J Biochem 1991; 201(1):191–198.
Lemaitre B, Reichhart JM, Hoffmann JA. Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc Natl Acad Sci USA 1997; 94(26):14614–14619.
Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 2002; 415(6870):389–395.
Zasloff M. Antibiotic peptides as mediators of innate immunity. Curr Opin Immunol 1992; 4(1):3–7.
Meister M, Richards G. Ecdysone and insect immunity: the maturation of the inducibility of the diptericin gene in Drosophila larvae. Insect Biochem Mol Biol 1996; 26(2):155–160.
Tasiemski A, Salzet M, Benson H et al. The presence of antibacterial and opioid peptides in human plasma during coronary artery bypass surgery. J Neuroimmunol 2000; 109(2):228–235.
Salzet M, Tasiemski A, Cooper E. Innate immunity in lophotrochozoans: the annelids. Curr Pharm Des 2006; 12(24):3043–3050.
Tettamanti G, Malagoli D, Benelli R et al. Growth factors and chemokines: a comparative functional approach between invertebrates and vertebrates. Curr Med Chem 2006; 13(23):2737–2850
Linthicum DS, Stein EA, Marks DH et al. Electron-microscopic observations of normal coelomocytes from the earthworm, Lumbricus terrestris. Cell Tissue Res 1977; 185(3):315–330.
Engelmann P, Pal J, Berki T et al. Earthworm leukocytes react with different mammalian antigen-specific monoclonal antibodies. Zoology (Jena) 2002; 105(3):257–265.
Verger-Bocquet M, Wattez C, Salzet M et al. Immunohistochemical identification of peptidergic neurons in compartment 4 of the supracesophageal ganglion of the leech Theromyzon tessulatum (O.F.M). Can J Zool 1993; 70:856–865.
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Tasiemski, A., Salzet, M. (2010). Leech Immunity: From Brain to Peripheral Responses. In: Söderhäll, K. (eds) Invertebrate Immunity. Advances in Experimental Medicine and Biology, vol 708. Springer, Boston, MA. https://doi.org/10.1007/978-1-4419-8059-5_5
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DOI: https://doi.org/10.1007/978-1-4419-8059-5_5
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