Skip to main content

Advertisement

Log in

Inflamed adult pharynx tissues and swimming larva of Ciona intestinalis share CiTNFα-producing cells

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

In situ hybridisation and immunohistochemistry analyses have shown that the Ciona intestinalis tumour necrosis factor alpha gene (CiTNFα), which has been previously cloned and sequenced, is expressed either during the inflammatory pharynx response to lipopolysaccharide (LPS) or during the swimming larval phase of development. Granulocytes with large granules and compartment/morula cells are CiTNFα-producing cells in both inflamed pharynx and larvae. Pharynx vessel endothelium also takes part in the inflammatory response. Haemocyte nodules in the vessel lumen or associated with the endothelium suggest the involvement of CiTNFα in recruiting lymphocyte-like cells and promoting the differentiation of inflammatory haemocytes. Specific antibodies against a CiTNFα peptide have identified a 43-kDa cell-bound form of the protein. Observations of pharynx histological sections (at 4 and 8 h post-LPS inoculation) from naive and medium-inoculated ascidians have confirmed the CiTNFα-positive tissue response. Larval histological sections and whole-mount preparations have revealed that CiTNFα is expressed by trunk mesenchyme, preoral lobe and tunic cells, indicating CiTNFα-expressing cell immigration events and an ontogenetic role.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Akira S, Hirano T, Taga T, Kishimoto T (1990) Biology of multifunctional cytokines: IL 6 and related molecules (IL 1 and TNF). FASEB J 4:2860–2867

    CAS  PubMed  Google Scholar 

  • Arch RH, Gedrich RW, Thompson CB (1998) Tumour necrosis factor receptors-associated factors (TRAFs)—a family of adapter proteins that regulates life and death. Genes Dev 12:2821–2830

    Article  Google Scholar 

  • Arizza V, Parrinello D (2009) Inflammatory hemocytes in Ciona intestinalis innate immune response. Invertebr Survival J 6:S58–S66

    Google Scholar 

  • Baghdiguian S, Martinand-Mari C, Mangeat P (2007) Using Ciona to study developmental programmed cell death. Semin Cancer Biol 17:147–153

    Article  CAS  PubMed  Google Scholar 

  • Bodmer JL, Schneider P, Tschopp J (2002) The molecular architecture of the TNF superfamily. Trends Biochem Sci 27:19–26

    Article  CAS  PubMed  Google Scholar 

  • Bourlat SJ, Juliusdottir T, Lowe CJ, Freeman R, Aronowicz J, Kirschner M, Lander ES, Thorndyke M, Nakano H, Kohn AB, Heyland A, Moroz LL, Copley RR, Telford MJ (2006) Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 444:85–88

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of proteins utilizing the principles of protein–dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Cammarata M, Arizza V, Cianciolo C, Parrinello D, Vazzana M, Vizzini A, Salerno G, Parrinello N (2008) The prophenoloxidase system is activated during the tunic inflammatory reaction of Ciona intestinalis. Cell Tissue Res 333:481–492

    Article  CAS  PubMed  Google Scholar 

  • Chambon JP, Soule J, Pomies P, Fort P, Sahuquet A, Alexandre D, Mangeat PH, Baghdiguian S (2002) Tail regression in Ciona intestinalis (Prochordate) involves a caspase-dependent apoptosis event associated with ERK activation. Development 129:3105–3114

    CAS  PubMed  Google Scholar 

  • Chambon JP, Nakayama A, Takamura K, McDougall A, Satoh N (2007) ERK-and JNK-signalling regulate gene networks that stimulate metamorphosis and apoptosis in tail tissues of ascidian tadpoles. Development 134:1203–1219

    Article  CAS  PubMed  Google Scholar 

  • Chiba S, Sasaki A, Nakayama A, Takamura K, Satoh N (2004) Development of Ciona intestinalis juveniles (through 2nd ascidian stage). Zool Sci 21:285–298

    Article  PubMed  Google Scholar 

  • Cloney RA (1982) Ascidian larvae and the events of metamorphosis. Am Zool 22:817–826

    Google Scholar 

  • Davidson B, Swalla BJ (2002) A molecular analysis of ascidian metamorphosis reveals activation of an innate immune response. Development 129:4739–4751

    Article  CAS  PubMed  Google Scholar 

  • Davidson B, Smith Wallace SE, Howsmon RA, Swalla BJ (2003) A morphological and genetic characterization of metamorphosis in the ascidian Boltenia villosa. Dev Genes Evol 213:601–611

    Article  CAS  PubMed  Google Scholar 

  • De Leo G (1992) Ascidian hemocytes and their involvement in defence reactions. Boll Zool 59:195–213

    Google Scholar 

  • De Leo G, Parrinello N, Di Bella MA (1987) Fine structure of blood system in Ciona intestinalis (Tunicata). Vessel and hemocytes in pharyngeal wall. Arch Biol 98:35–52

    Google Scholar 

  • De Leo G, Parrinello N, Parrinello D, Cassara' G, Russo D, Di Bella MA (1997) Encapsulation response of Ciona intestinalis (Ascidiacea) to intratunical erythrocyte injection. J Invertebr Pathol 69:14–23

    Article  PubMed  Google Scholar 

  • Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:923–924

    Article  Google Scholar 

  • Di Bella MA, De Leo G (2000) Hemocyte migration during inflammatory-like reaction of Ciona intestinalis (Tunicata, ascidiacea). J Invertebr Pathol 76:105–111

    Article  PubMed  Google Scholar 

  • Ermak TH (1982) The renewing cell populations of ascidians. Am Zool 22:795–805

    Google Scholar 

  • Gallucci S, Matzinger P (2001) Danger signals: SOS to the immune system. Curr Opin Immunol 13:114–119

    Article  CAS  PubMed  Google Scholar 

  • Goetz FW, Planas JV, MacKenzie S (2004) Tumor necrosis factors. Dev Comp Immunol 28:487–497

    Article  CAS  PubMed  Google Scholar 

  • Hirano T, Nishida H (1997) Developmental fates of larval tissues after metamorphosis in ascidian Halocynthia roretzi. I. Origin of mesodermal tissues of the juvenile. Dev Biol 192:199–210

    Article  CAS  PubMed  Google Scholar 

  • Idriss TH, Naismith JH (2000) TNF alpha and the TNF receptor superfamily: structure function relationship(s). Microsc Res Tech 1:184–195

    Article  Google Scholar 

  • Jeffery WR, Chiba T, Krajka FR, Deyts C, Satoh N, Joly JS (2008) Trunk lateral cells are neural crest-like cells in the ascidian Ciona intestinalis: insights into the ancestry and evolution of the neural crest. Dev Biol 324:152–160

    Article  CAS  PubMed  Google Scholar 

  • Kimura Y, Yoshida M, Morisawa M (2003) Interaction between noradrenaline or adrenaline and the beta 1-adrenergic receptor in the nervous system triggers early metamorphosis of larvae in the ascidian, Ciona savignyi. Dev Biol 258:129–140

    Article  CAS  PubMed  Google Scholar 

  • Kohchi C, Mizuno D, Soma G (1991) Expression of tumor necrosis factor-alpha and -beta transcripts in embryonal carcinoma and trophoblast cell lines: inflammation-like state as possible regulatory mechanism for ontogenesis. Eur Cytokine Net 2:245–255

    CAS  Google Scholar 

  • Kohchi C, Noguchi K, Tanabe Y, Mizuno D, Soma G (1994) Constitutive expression of TNF-alpha and -beta genes in mouse embryo: roles of cytokines as regulator and effector on development. Int J Biochem 26:111–119

    Article  CAS  PubMed  Google Scholar 

  • Kusakabe T, Yoshida R, Kawakami I, Kusakabe R, Mochizuki Y, Yamada L, Shin-i T, Kohara Y, Satoh N, Tsuda M, Satou Y (2002) Gene expression profiles in tadpole larvae of Ciona intestinalis. Dev Biol 242:188–203

    Article  PubMed  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural protein during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

  • Magor BJ, Magor KE (2001) Evolution of effectors and receptors of innate immunity. Dev Comp Immunol 25:651–682

    Article  CAS  PubMed  Google Scholar 

  • Marino R, Kimura Y, De Santis R, Lambris JD, Pinto MR (2002) Complement in urochordates: cloning and characterization of two C3-like genes in the ascidian Ciona intestinalis. Immunogenetics 53:1055–1064

    Article  CAS  PubMed  Google Scholar 

  • Matzinger P (2002) An innate sense of danger. Ann N Y Acad Sci 961:341–342

    Article  PubMed  Google Scholar 

  • Melillo D, Sfyroera G, De Santis R, Graziano R, Marino R, Lambris JD, Pinto MR (2006) First identification of a chemotactic receptor in an invertebrate species: structural and functional characterization of Ciona intestinalis C3a receptor. J Immunol 177:4132–4140

    CAS  PubMed  Google Scholar 

  • Nakayama A, Satou Y, Satoh N (2002) Further characterization of genes expressed during Ciona intestinalis metamorphosis. Differentiation 70:429–437

    Article  CAS  PubMed  Google Scholar 

  • Nakayama A, Satoh N, Sasakura Y (2005) Tissue profile of DNA replication in the swimming larvae of Ciona intestinalis. Zool Sci 22:301–309

    Article  CAS  PubMed  Google Scholar 

  • Nakayama-Ishimura A, Chambon J-P, Horie T, Satoh N, Sasakura Y (2009) Delineating metamorphic pathways in the ascidian Ciona intestinalis. Dev Biol 326:357–367

    Article  CAS  PubMed  Google Scholar 

  • Nishide K, Nishikata T, Satoh N (1989) A monoclonal antibody specific to embryonic trunk-lateral cells of the ascidian Halocynthia roretzi stains coelomic cells of juvenile and adult basophilic blood cells. Dev Growth Differ 31:595–600

    Article  Google Scholar 

  • Ordás MC, Costa MM, Roca FJ, López-Castejón G, Mulero V, Meseguer J, Figueras A, Novoa B (2007) Turbot TNFalpha gene: molecular characterization and biological activity of the recombinant protein. Mol Immunol 44:389–400

    Article  PubMed  Google Scholar 

  • Parrinello N (1981) The reaction of Ciona intestinalis L. to subcuticular erythrocyte and protein injection. Dev Comp Immunol 5:105–110

    Article  Google Scholar 

  • Parrinello N, Patricolo E (1984) Inflammatory-like reaction in the tunic of Ciona intestinalis (Tunicata). II. Capsule components. Biol Bull 167:238–250

    Article  Google Scholar 

  • Parrinello N, Patricolo E, Canicattı C (1984) Inflammatory-like reaction in the tunic of Ciona intestinalis (Tunicata). I. Encapsulation and tissue injury. Biol Bull 167:229–237

    Article  Google Scholar 

  • Parrinello N, De Leo G, Di Bella MA (1990) Fine structural observations of the granulocytes involved in the tunic inflammatory-like reaction of Ciona intestinalis (Tunicata). J Invertebr Pathol 56:181–189

    Article  CAS  PubMed  Google Scholar 

  • Parrinello N, Arizza V, Cammarata M, Giaramita FT, Pergolizzi M, Vazzana M, Vizzini A, Parrinello D (2007) Inducible lectins with galectin properties and human IL1alpha epitopes opsonize yeast during the inflammatory response of the ascidian Ciona intestinalis. Cell Tissue Res 329:379–390

    Article  CAS  PubMed  Google Scholar 

  • Parrinello N, Vizzini A, Arizza V, Salerno G, Parrinello D, Cammarata M, Giaramita FT, Vazzana M (2008) Enhanced expression of a cloned and sequenced Ciona intestinalis TNFalpha-like (CiTNF alpha) gene during the LPS-induced inflammatory response. Cell Tissue Res 334:305–317

    Article  CAS  PubMed  Google Scholar 

  • Passamaneck YJ, Di Gregorio A (2005) Ciona intestinalis: cordate development made simple. Dev Dyn 233:1–19

    Article  CAS  PubMed  Google Scholar 

  • Peddie CM, Smith VJ (1995) “Lymphocyte-like” cells in ascidians: precursors for vertebrate lymphocytes? Fish Shellfish Immunol 5:613–629

    Article  Google Scholar 

  • Peddie CM, Riches AC, Smith VJ (1995) Proliferation of undifferentiated blood cells from the solitary ascidian, Ciona intestinalis in vitro. Dev Comp Immunol 19:377–387

    Article  CAS  PubMed  Google Scholar 

  • Pinto MR, Chinnici CM, Kimura Y, Melillo D, Marino R, Spruce LA, De Santis R, Parrinello N, Lambris JD (2003) CiC3–1a mediated chemotaxis in the deuterostome invertebrate Ciona intestinalis (Urochordata). J Immunol 171:5521–5528

    CAS  PubMed  Google Scholar 

  • Plagemann PG (2005) Epitope specificity of monoclonal antibodies to the N-protein of porcine reproductive and respiratory syndrome virus by ELISA with synthetic peptides. Vet Immunol Immunopathol 104:50–68

    Article  Google Scholar 

  • Roberts B, Davidson B, MacMaster G, Lockhart V, Ma E, Wallace SS, Swalla BJ (2007) A complement response may activate metamorphosis in the ascidian Boltenia villosa. Dev Genes Evol 217:449–458

    Article  CAS  PubMed  Google Scholar 

  • Satou Y, Imai KS, Satoh N (2001) Early embryonic expression of a LIM-homeobox gene Cs-lhx3 is downstream of beta-catenin and responsible for the endoderm differentiation in Ciona savignyi embryos. Development 128:3559–3570

    CAS  PubMed  Google Scholar 

  • Sawada T, Zhang J, Cooper EL (1994) Sustained viability and profileration of hemocytes from the cultured pharynx of Styela clava. Mar Biol 119:597–603

    Article  Google Scholar 

  • Tarallo R, Sordino P (2004) Time course of programmed cell death in Ciona intestinalis in relation to mitotic activity and MAPK signalling. Dev Dyn 230:251–262

    Article  CAS  PubMed  Google Scholar 

  • Terajima D, Shida K, Takada N, Kasuya A, Rokhsar D, Satoh N, Satake M, Wang HG (2003) Identification of candidate genes encoding the core components of the cell death machinery in the Ciona intestinalis genome. Cell Death Differ 10:749–753

    Article  CAS  PubMed  Google Scholar 

  • Vaux DL, Korsmeyer SJ (1999) Cell death in development. Cell 96:245–254

    Article  CAS  PubMed  Google Scholar 

  • Vienne A, Pontarotti P (2006) Metaphylogeny of 82 gene families sheds a new light on chordate evolution. Int J Biol Sci 2:32–37

    CAS  PubMed  Google Scholar 

  • Vizzini A, Pergolizzi M, Vazzana M, Salerno G, Di Sano C, Macaluso P, Arizza V, Parrinello D, Cammarata M, Parrinello N (2008) FACIT collagen (1alpha-chain) is expressed by hemocytes and epidermis during the inflammatory response of the ascidian Ciona intestinalis. Dev Comp Immunol 32:682–692

    Article  CAS  PubMed  Google Scholar 

  • Wride MA, Sanders EJ (1995) Potential roles for tumour necrosis factor alpha during embryonic development. Anat Embryol 191:1–10

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Luan W, Jin S, Xiang J (2008) A novel tumor necrosis factor ligand superfamily member (CsTL) from Ciona savignyi: molecular identification and expression analysis. Dev Comp Immunol 32:1362–1373

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nicolò Parrinello.

Additional information

This work was supported by a research grant from the Italian Ministry of University and Scientific Research (PRIN 2006 to N. Parrinello).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Parrinello, N., Vizzini, A., Salerno, G. et al. Inflamed adult pharynx tissues and swimming larva of Ciona intestinalis share CiTNFα-producing cells. Cell Tissue Res 341, 299–311 (2010). https://doi.org/10.1007/s00441-010-0993-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-010-0993-5

Keywords

Navigation