Annelida: Oligochaetes (Segmented Worms): Earthworm Immunity, Quo Vadis? Advances and New Paradigms in the Omics Era

  • Péter EngelmannEmail author
  • Kornélia Bodó
  • József Najbauer
  • Péter Németh


In the last few decades the field of comparative immunology has undergone an enormous amount of progress due to the novel research tools introduced and the expanding amount of transcriptomic information. Recently, the various “omics” approaches have covered every scientific field of biomedical research.

Earthworms as ecologically prominent organisms are used in different research areas of biological and environmental sciences. In-depth research on the immune components of earthworms is now showing rapid progress, but the precise molecular data on this “non-classical” model organism are still relatively limited compared to those from “classical” invertebrate model (e.g., Drosophila, Caenorhabditis elegans) species. In fact, earthworm immunity possesses many common characteristics with other invertebrate organisms but also harbors some unique features.

In this chapter we briefly summarize our recent findings, concentrating on the cellular components of earthworm immunity applying inhouse-developed monoclonal antibodies. Furthermore, we discuss several fast-advancing scientific fields that rely on different omics data (e.g., transcriptome, epigenome, microbiome, and regenerative biology) and those that are relatively under-represented in invertebrate (earthworm) immunity.


Annelids Innate immunity Coelomocytes Cytotoxicity Monoclonal antibodies Genomics Transcriptomics Epigenetics Microbiome Regeneration 



We acknowledge the financial support of Medical School Research Foundation, University of Pécs (PTE-ÁOK-KA 2017/04), the János Bolyai Research Scholarship of the Hungarian Academy of Sciences (PE). We are grateful to Krisztina Kovács (Department of Medical Microbiology and Immunology, University of Pécs, Hungary) for providing her skill and expertise in identification of the isolated microorganisms. The present scientific contribution is dedicated to the 650th anniversary of the foundation of the University of Pécs, Hungary.


  1. Arrowsmith CH, Bountra C, Fish PV et al (2012) Epigenetic protein families: a new frontier for drug discovery. Nat Rev Drug Discov 11:384–400PubMedGoogle Scholar
  2. Belkaid Y, Hand TW (2014) Role of the microbiota in immunity and inflammation. Cell 157:121–141PubMedPubMedCentralGoogle Scholar
  3. Bely AE (2006) Distribution of segment regeneration ability in the Annelida. Integr Comp Biol 46:508–518PubMedGoogle Scholar
  4. Berrill NJ (1952) Regeneration and budding in worms. Biol Rev 27:401–438Google Scholar
  5. Beschin A, Bilej M, Brys L et al (1999) Convergent evolution of cytokines. Nature 400:627–628PubMedPubMedCentralGoogle Scholar
  6. Bilej M, Procházková P, Silerová M et al (2010) Earthworm immunity. Adv Exp Med Biol 708:66–79PubMedGoogle Scholar
  7. Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16:6–21PubMedGoogle Scholar
  8. Bosch TC (2013) Cnidarian-microbe interactions and the origin of innate immunity in metazoans. Annu Rev Microbiol 67:499–518PubMedGoogle Scholar
  9. Bosch TC (2014) Rethinking the role of immunity: lessons from Hydra. Trends Immunol 35:495–502PubMedGoogle Scholar
  10. Brulle F, Mitta G, Cocquerelle C et al (2006) Cloning and real time PCR testing of 14 potential biomarkers in Eisenia fetida following cadmium exposure. Env. Sci Technol 40:2844–2850Google Scholar
  11. Brulle F, Morgan AJ, Cocquerelle C et al (2010) Transcriptomic underpinning of toxicant-mediated physiological function alterations in three terrestrial invertebrate taxa: a review. Environ Pollut 158:2793–2808PubMedGoogle Scholar
  12. Campos EI, Reinberg D (2009) Histones: annotating chromatin. Annu Rev Genet 43:559–599PubMedPubMedCentralGoogle Scholar
  13. Castanotto D, Rossi JJ (2009) The promises and pitfalls of RNA-interference-based therapeutics. Nature 457:426–433PubMedPubMedCentralGoogle Scholar
  14. Chaves da Silva PG, Corrêa CL, de Carvalho SL et al (2013) The crustacean central nervous system in focus: subacute neurodegeneration induces a specific innate immune response. PLoS One 8:e80896PubMedPubMedCentralGoogle Scholar
  15. Cooper EL, Balamurugan M (2010) Unearthing a source of medicinal molecules. Drug Discov Today 15:966–972PubMedGoogle Scholar
  16. Cooper EL, Hirabayashi K (2013) Origin of innate immune responses: revelation of food and medicinal applications. J Tradit Complement Med 3:204–212PubMedPubMedCentralGoogle Scholar
  17. Cooper EL, Roch P (1984) Earthworm leukocyte interactions during early stages of graft rejection. J Exp Zool 232:67–72PubMedGoogle Scholar
  18. Cooper EL, Kauschke E, Cossarizza A (2002) Digging for innate immunity since Darwin and Metchnikoff. BioEssays 24:319–333PubMedGoogle Scholar
  19. Cooper EL, Kvell K, Engelmann P et al (2006) Still waiting for the Toll? Immunol Lett 104:16–28Google Scholar
  20. Cossarizza A, Cooper EL, Suzuki MM et al (1996) Earthworm leukocytes that are not phagocytic and cross-react with several human epitopes can kill human tumor cell lines. Exp Cell Res 224:174–182PubMedGoogle Scholar
  21. Darwin CR (1881) The formation of vegetable mould, through the action of worms. Murray J, LondonGoogle Scholar
  22. 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 Cell 32:437–445PubMedGoogle Scholar
  23. Dinsmore CE (2001) Regeneration: principles. In: Encyclopedia of life sciences (ELS). Wiley, Chichester. CrossRefGoogle Scholar
  24. Douglas AE (2015) Multiorganismal insects: diversity and function of resident microorganisms. Annu Rev Entomol 60:17–34PubMedGoogle Scholar
  25. Dvořák J, Mančíková V, Pižl V et al (2013) Microbial environment affects innate immunity in two closely related earthworm species Eisenia andrei and Eisenia fetida. PLoS One 8:e79257PubMedPubMedCentralGoogle Scholar
  26. Dvořák J, Roubalová R, Procházková P et al (2016) Sensing microorganisms in the gut triggers the immune response in Eisenia andrei earthworms. Dev Comp Immunol 57:67–74PubMedGoogle Scholar
  27. Elsworth B, Jones M, Blaxter M (2013) Badger--an accessible genome exploration environment. Bioinformatics 29:2788–2789PubMedPubMedCentralGoogle Scholar
  28. Eming SA, Krieg T, Davidson JM (2007) Inflammation in wound repair: molecular and cellular mechanisms. J Invest Dermatol 127:514–525PubMedGoogle Scholar
  29. Engelmann P, Pál J, Berki T et al (2002) Earthworm leukocytes reacted with different mammalian antigen specific monoclonal antibodies. Zoology 105:257–265PubMedGoogle Scholar
  30. Engelmann P, Kiss J, Csöngei V et al (2004) Earthworm leukocytes kill HeLa, HEp-2, PC-12 and PA317 cells in vitro. J Biochem Biophys Methods 61:215–227PubMedGoogle Scholar
  31. Engelmann P, Cooper EL, Németh P (2005a) Anticipating innate immunity without a Toll. Mol Immunol 42:931–942PubMedGoogle Scholar
  32. Engelmann P, Pálinkás L, Cooper EL et al (2005b) Monoclonal antibodies identify four distinct annelid leukocyte markers. Dev Comp Immunol 29:599–614PubMedGoogle Scholar
  33. Engelmann P, Cooper EL, Opper B, Németh P (2011) Earthworm innate immune system. In: Karaca A (ed) Biology of earthworms. Soil Biology 24. Springer, Berlin/Heidelberg, pp 229–245Google Scholar
  34. Engelmann P, Hayashi Y, Bodó K et al (2016a) New aspects of earthworm innate immunity: novel molecules and old proteins with unexpected functions. In: Ballarin L, Cammarata M (eds) Lessons in immunity: from single cell organisms to mammals. Elsevier-Academic Press, New York/Amsterdam, pp 53–66Google Scholar
  35. Engelmann P, Hayashi Y, Bodó K et al (2016b) Phenotypic and functional characterization of earthworm coelomocytes: linking light scatter-based cell typing and imaging of the sorted populations. Dev Comp Immunol 65:41–52PubMedGoogle Scholar
  36. Fischer E (1977) The function of chloragosomes, the specific age-pigment granules of annelids – a review. Exp Gerontol 12:69–74PubMedGoogle Scholar
  37. Fischer E, Molnár L (1992) Environmental aspects of the chloragogenous tissue of earthworms. Soil Biol Biochem 24:1723–1727Google Scholar
  38. Follert P, Cremer H, Béclin C (2014) MicroRNAs in brain development and function: a matter of flexibility and stability. Front Mol Neurosci 7:5PubMedPubMedCentralGoogle Scholar
  39. Fuller-Espie SL (2010) Using flow cytometry to measure phagocytic uptake in earthworms. J Microbiol Biol Educ 11:144–151PubMedPubMedCentralGoogle Scholar
  40. Gaspar-Maia A, Alajem A, Meshorer E et al (2011) Open chromatin in pluripotency and reprogramming. Nat Rev Mol Cell Biol 12:36–47PubMedPubMedCentralGoogle Scholar
  41. Gilbert SF, Bosch TC, Ledón-Rettig C (2015) Eco-Evo-Devo: developmental symbiosis and developmental plasticity as evolutionary agents. Nat Rev Genet 16:611–622PubMedGoogle Scholar
  42. Godwin JW, Brockes JP (2006) Regeneration, tissue injury and the immune response. J Anat 209:423–432PubMedPubMedCentralGoogle Scholar
  43. Godwin JW, Pinto AR, Rosenthal NA (2013) Macrophages are required for adult salamander limb regeneration. Proc Natl Acad Sci U S A 110:9415–9420PubMedPubMedCentralGoogle Scholar
  44. Gomes AQ, Nolasco S, Soares H (2013) Non-coding RNAs: multi-tasking molecules in the cell. Int J Mol Sci 14:16010–16039PubMedPubMedCentralGoogle Scholar
  45. Gong P, Perkins EJ (2016) Earthworm toxicogenomics: a renewed genome-wide quest for novel biomarkers and mechanistic insights. Appl Soil Ecol 104:12–24Google Scholar
  46. Gong P, Guan X, Inouye LS et al (2008) Transcriptomic analysis of RDX and TNT interactive sublethal effects in the earthworm Eisenia fetida. BMC Genomics 9:S15PubMedPubMedCentralGoogle Scholar
  47. Gong P, Xie F, Zhang B et al (2010) In silico identification of conserved microRNAs and their target transcripts from expressed sequence tags of three earthworm species. Comput Biol Chem 34:313–319PubMedGoogle Scholar
  48. Greer EL, Shi Y (2012) Histone methylation: a dynamic mark in health, disease and inheritance. Nat Rev Genet 13:343–357PubMedPubMedCentralGoogle Scholar
  49. Hauton C, Smith VJ (2007) Adaptive immunity in invertebrate: a straw house without a mechanistic foundation. BioEssays 29:1138–1146PubMedGoogle Scholar
  50. Hayashi Y, Engelmann P (2013) Earthworm’s immunity in the nanomaterial world: new room, future challenges. Invertebr Surv J 10:69–76Google Scholar
  51. Hayashi Y, Engelmann P, Foldbjerg R et al (2012) Earthworms and humans in vitro: characterizing evolutionarily conserved stress and immune responses to silver nanoparticles. Environ Sci Technol 46:4166–4173PubMedGoogle Scholar
  52. Hayashi Y, Miclaus T, Scavenius C et al (2013) Species differences take shape at nanoparticles protein corona made of native repertoire assists cellular interaction. Environ Sci Technol 47:14367–14375PubMedGoogle Scholar
  53. Hayashi Y, Miclaus T, Engelmann P et al (2016) Nanosilver pathophysiology in earthworms: transcriptional profiling of secretory proteins and the implication for the protein corona. Nanotoxicology 10:303–311PubMedGoogle Scholar
  54. Hennessy C, McKernan DP (2016) Epigenetics and innate immunity: the ‘unTolld’ story. Immunol Cell Biol 94:631–639PubMedGoogle Scholar
  55. Homa J, Zorksa A, Wesolovski D, Chadzinska M (2013) Dermal exposure to immunostimulants induces changes in activity and proliferation of coelomocytes of Eisenia andrei. J Comp Physiol B 183:313–322PubMedGoogle Scholar
  56. Huang XM, Tian QN, Bao ZX et al (2012) Cloning and identification of microRNAs in earthworm (Eisenia fetida). Biochem Genet 50:1–11PubMedGoogle Scholar
  57. Jamieson BGM (1981) Chloragocytes. In: Jamieson BGM (ed) The ultrastructure of the oligochaete. Academic Press, New York, pp 96–118Google Scholar
  58. Jupatanakul N, Sim S, Dimopoulos G (2014) The insect microbiome modulates vector competence for arboviruses. Virus 6:4294–4313Google Scholar
  59. Kauschke E, Komiyama K, Moro I et al (2001) Evidence for perforin-like activity associated with earthworm leukocytes. Zoology 104:13–24PubMedGoogle Scholar
  60. Kobayashi H, Ohta N, Umeda M (2004) Biology of lysenin, a protein in the coelomic fluid of the earthworm Eisenia foetida. Int Rev Cytol 236:45–99PubMedGoogle Scholar
  61. Kosik KS (2009) MicroRNAs tell an evo-devo story. Nat Rev Neurosci 10:754–759PubMedGoogle Scholar
  62. Kvell K, Cooper EL, Engelmann P et al (2007) Blurring borders: innate immunity with adaptive features. Clin Dev Immunol 2007:83671PubMedPubMedCentralGoogle Scholar
  63. Kwong WK, Moran NA (2016) Gut microbial communities of social bees. Nat Rev Microbiol 14:374–384PubMedPubMedCentralGoogle Scholar
  64. Lassegues M, Milochau A, Doignon F et al (1997) Sequence and expression of an Eisenia fetida-derived cDNA clone that encodes the 40 kDa fetidin antibacterial protein. Eur J Biochem 246:756–762PubMedGoogle Scholar
  65. Layeghifard M, Hwang DM, Guttman DS (2017) Disentangling interactions in the microbiome: a network perspective. Trends Microbiol 25:217–228PubMedGoogle Scholar
  66. Liebmann E (1942) The coelomocytes of Lumbricidae. J Morphol 71:221–249Google Scholar
  67. Liebmann E (1943) New light on regeneration of Eisenia foetida (SAV.). J Morphol 73:583–610Google Scholar
  68. Liu D, Lian B, Wu C et al (2017) A comparative study of gut microbiota profiles of earthworms fed in three different substrates. Symbiosis 74:21–29Google Scholar
  69. Logie C, Stunnenberg HG (2016) Epigenetic memory: a macrophage perspective. Semin Immunol 28:359–367PubMedGoogle Scholar
  70. Luo GZ, He C (2017) DNA N(6)-methyladenine in metazoans: functional epigenetic mark or bystander? Nat Struct Mol Biol 24:503–506PubMedGoogle Scholar
  71. Mácsik LL, Somogyi I, Opper B et al (2015) Induction of apoptosis-like cell death by coelomocyte extracts from Eisenia andrei earthworms. Mol Immunol 67:213–222PubMedGoogle Scholar
  72. Mainschein J (2011) Regenerative medicine’s historical roots in regeneration, transplantation and translation. Dev Biol 358:278–284Google Scholar
  73. Mathew LK, Sengupta S, Kawakami A et al (2007) Unraveling tissue regeneration pathways using chemical genetics. J Biol Chem 282:35202–35210Google Scholar
  74. McFall-Ngai M, Hadfield MG, Bosch TC et al (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci U S A 110:3229–3236PubMedPubMedCentralGoogle Scholar
  75. Mehta A, Baltimore D (2016) MicroRNAs as regulatory elements in immune system logic. Nat Rev Immunol l16:279–294Google Scholar
  76. Mikami Y, Fukushima A, Kuwada-Kusunose T et al (2015) Whole transcriptome analysis using next-generation sequencing of sterile-cultured Eisenia andrei for immune system research. PLoS One 10:e0118587PubMedPubMedCentralGoogle Scholar
  77. Mill PJ (1978) Physiology of annelids. Academic Press, LondonGoogle Scholar
  78. Milutinović B, Kurtz J (2016) Immune memory in invertebrates. Semin Immunol 28:328–342PubMedGoogle Scholar
  79. Molnar L, Pollak E, Skopek Z et al (2015) Immune system participates in brain regeneration and restoration of reproduction in the earthworm Dendrobaena veneta. Dev Comp Immunol 52:269–279PubMedGoogle Scholar
  80. Moment GB (1974) The possible roles of coelomic cells and their yellow pigment in annelid regeneration and aging. Growth 38:209–218PubMedGoogle Scholar
  81. Morgan TH (1901) Regeneration. Macmillan, New YorkGoogle Scholar
  82. Myohara M (2004) Differential tissue development during embryogenesis and regeneration in an annelid. Dev Dyn 231:349–358PubMedGoogle Scholar
  83. Nyberg KG, Conte MA, Kostyun JL et al (2012) Transcriptome characterization via 454 pyrosequencing of the annelid Pristina leidyi, an emerging model for studying the evolution of regeneration. BMC Genomics 13:287PubMedPubMedCentralGoogle Scholar
  84. OECD (1984) Guideline for testing chemicals. OECD, ParisGoogle Scholar
  85. OECD (2004) Earthworm reproduction test (Eisenia fetida/Eisenia andrei). OECD, ParisGoogle Scholar
  86. Okrzesik J, Kachamakova-Trojanowska N, Jozkowicz A et al (2013) Reversible inhibition of reproduction during regeneration of cerebral ganglia and celomocytes in the earthworm Dendrobaena veneta. Invertebr Surv J 10:151–161Google Scholar
  87. Opper B, Bognár A, Heidt D et al (2013) Revising lysenin expression of earthworm coelomocytes. Dev Comp Immunol 39:214–218PubMedGoogle Scholar
  88. Parrinello N, Vizzini A, Arizza V et al (2008) Enhanced expression of a cloned and sequenced Ciona intestinalis TNF alpha-like (CiTNF alpha) gene during the LPS-induced inflammatory response. Cell Tissue Res 334:305–317PubMedGoogle Scholar
  89. Pecot CV, Calin GA, Coleman RL et al (2011) RNA interference in the clinic: challenges and future directions. Nat Rev Cancer 11:59–67PubMedGoogle Scholar
  90. Pirooznia M, Gong P, Guan X et al (2007) Cloning, analysis and functional annotation of expressed sequence tags from the earthworm Eisenia fetida. BMC Bioinformatics 8:S7PubMedPubMedCentralGoogle Scholar
  91. Plytycz B, Kielbasa E, Grebosz A et al (2010) Riboflavin mobilization from eleocyte stores in the earthworm Dendrodrilus rubidus inhabiting aerially-contaminated Ni smelter soil. Chemosphere 81:199–205PubMedGoogle Scholar
  92. Procházková P, Šustr V, Dvořák J et al (2013) Correlation between the activity of digestive enzymes and nonself recognition in the gut of Eisenia andrei earthworms. J Invertebr Pathol 114:217–221PubMedGoogle Scholar
  93. Quintin J, Saeed S, Martens JHA et al (2012) Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe 12:223–232PubMedGoogle Scholar
  94. Roch P (1979) Leukocyte DNA synthesis in grafted Lumbricids: and approach to study histocompatibility in invertebrates. Dev Comp Immunol 3:417–428PubMedGoogle Scholar
  95. Rosa D (1896) I Linfociti degli Oljgocheti. Mem R Ace Tor 46:149–172Google Scholar
  96. Rudi K, Strætkvern KO (2012) Correlations between Lumbricus terrestris survival and gut microbiota. Microb Ecol Health Dis 23:17316Google Scholar
  97. Santoyo MM, Flores CR, Torres AL et al (2011) Global DNA methylation in earthworms: a candidate biomarker of epigenetic risks related to the presence of metals/metalloids in terrestrial environments. Environ Pollut 159:2387–2392PubMedGoogle Scholar
  98. Schikorski D, Cuvillier-Hot V, Leippe M et al (2008) 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 181:1083–1095PubMedPubMedCentralGoogle Scholar
  99. Schröder K, Bosch TC (2016) The origin of mucosal immunity: lessons from the holobiont Hydra. MBio 7:e01184-16Google Scholar
  100. Self-Fordham JB, Naqvi AR, Uttamani JR et al (2017) MicroRNA: dynamic regulators of macrophage polarization and plasticity. Front Immunol 8:1062PubMedPubMedCentralGoogle Scholar
  101. Selosse MA, Bessis A, Pozo MJ (2014) Microbial priming of plant and animal immunity: symbionts as developmental signals. Trends Microbiol 22:607–613PubMedGoogle Scholar
  102. Silverstein AM (2001) History of immunology. In: Encyclopedia of life sciences (ELS). Wiley, Chichester. CrossRefGoogle Scholar
  103. Somogyi I, Boros A, Engelmann P et al (2009) Pituitary adenylate cyclase-activating polypeptide-like compounds could modulate the activity of coelomocytes in the earthworm. Ann N Y Acad Sci 1163:521–523PubMedGoogle Scholar
  104. Šrut M, Drechsel V, Höckner M (2017) Low levels of Cd induce persisting epigenetic modifications and acclimation mechanisms in the earthworm Lumbricus terrestris. PLoS One 12:e0176047PubMedPubMedCentralGoogle Scholar
  105. Stein EA, Avtalion RR, Cooper EL (1977) The coelomocytes of the earthworm Lumbricus terrestris: morphology and phagocytic properties. J Morphol 153:467–477PubMedGoogle Scholar
  106. Stürzenbaum SR, Georgiev O, Morgan AJ et al (2004) Cadmium detoxification in earthworms: from genes to cells. Env. Sci Technol 38:6283–6289Google Scholar
  107. Stürzenbaum SR, Andre J, Kille P et al (2009) Earthworm genome, genes and proteins: the (re)discovery of Darwin’s worms. Proc R Soc B 276:789–797PubMedGoogle Scholar
  108. Sun Y, Zhou Z, Wang L et al (2014) The immunomodulation of a novel tumor necrosis factor (CgTNF-1) in oyster Crassotrea gigas. Fish Shellfish Immunol 45:291–299Google Scholar
  109. Tak ES, Cho SJ, Park SC (2015) Gene expression profiling of coelomic cells anddiscovery of immune-related genes in the earthworm, Eisenia andrei, using expressed sequence tags. Biosci Biotechnol Biochem 79:367–373PubMedGoogle Scholar
  110. Tessmar-Raible K, Arendt D (2003) Emerging systems: between vertebrates and arthropods, the Lophotrochozoa. Curr Opin Genet Dev 13:331–340PubMedGoogle Scholar
  111. Thunders M, Cavanagh J, Li Y (2017) De novo transcriptome assembly, functional annotation and differential gene expression analysis of juvenile and adult E. fetida, a model oligochaete used in ecotoxicological studies. Biol Res 50:7PubMedPubMedCentralGoogle Scholar
  112. Valembois P, Roch P, Lasségues M et al (1982) Antibacterial activity of the haemolytic system from the earthworm Eisenia fetida andrei. J Invertebr Pathol 40:21–27Google Scholar
  113. van der Meer JW, Joosten LAB, Riksen N et al (2015) Trained immunity: a smart way to enhance innate immune defence. Mol Immunol 68:40–44PubMedGoogle Scholar
  114. Van Straalen NM, Roelofs D (2008) Genomics technology for assessing soil pollution. J. Biology 7:19Google Scholar
  115. Vandegehuchte MB, Janssen CR (2014) Epigenetics in an ecotoxicological context. Mutat Res Genet Toxicol Environ Mutagen 764-765:36–45PubMedGoogle Scholar
  116. Velki M, Ečimović S (2017) Important isssues in ecotoxicological investigations using earthworms. Rev Environ Contam Toxicol 239:157–184PubMedGoogle Scholar
  117. Vilcinskas A (2016) The role of epigenetics in host-parasite coevolution: lessons from the model insects Galleria mellonella and Tribolium castaneum. Zoology 119:273–280PubMedGoogle Scholar
  118. Vitulo N, Dalla Valle L et al (2017) Downregulation of lizard immuno-genes in the regenerating tail and myogenes in the scarring limb suggests that tail regeneration occurs in an immuno-privileged organ. Protoplasma 254:2127–2141PubMedGoogle Scholar
  119. Weaver H, Wood W (2016) Creating a buzz about macrophages: the fly as an vivo model for studying immune cell behaviour. Dev Cell 38:129–132Google Scholar
  120. Wiens GD, Glenney GW (2011) Origin and evolution of TNF and TNF receptor superfamilies. Dev Comp Immunol 35:1324–1335PubMedGoogle Scholar
  121. Wilhelm M, Koza A, Engelmann P et al (2006) Evidence for the presence of thyroid-stimulating hormone, thyroglobulin and their receptors in Eisenia fetida: a multilevel hormonal interface between the nervous system and the peripherial tissues. Cell Tissue Res 324:535–546PubMedGoogle Scholar
  122. Xiao N, Ge F, Edwards CA (2011) The regeneration capacity of an earthworms Eisenia fetida, in relation to the site of amputation along the body. Acta Ecol Sin 31:197–204Google Scholar
  123. Zattara EE, Bely AE (2011) Evolution and novel developmental trajectory: fission is distinct from regeneration in the annelid Pristina leidyi. Evol Dev 13:80–95PubMedGoogle Scholar
  124. Zoran MJ (2010) Regeneration in Annelids. In: Encyclopedia of life sciences (ELS). Wiley, Chichester. CrossRefGoogle Scholar
  125. Zwarycz AS, Nossa CW, Putnam NH et al (2015) Timing and scope of genomic expansion within annelida: evidence from homeoboxes in the genome of the earthworm Eisenia fetida. Genome Biol Evol 8:271–281PubMedPubMedCentralGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Péter Engelmann
    • 1
    Email author
  • Kornélia Bodó
  • József Najbauer
  • Péter Németh
  1. 1.Department of Immunology and BiotechnologyClinical Center, University of PécsPécsHungary

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