Skip to main content
SpringerLink
Log in

Allograft rejection in the mixed cell reaction system of the demosponge Suberites domuncula is controlled by differential expression of apoptotic genes

  • Original Paper
  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

Until recently, the lack of molecular probes hampered the determination of the expression of pro-apoptotic and anti-apoptotic genes in sponge. In an approach to solve this problem, the present study describes a variety of cDNAs from the demosponge Suberites domuncula, coding for proteins that are characteristic for the initiation of apoptosis (caspase, MA3, ALG-2 protein), for the prevention of programmed cells death (2 Bcl-2 homology proteins, FAIM-related polypeptide, and DAD-1-related protein), and for morphogenetic processes (retinoid X receptor). They were used as probes to monitor the expression levels in vitro in the allogeneic mixed sponge cell reaction (MSCR) system. In the allogeneic MSCR, two-cell aggregates (primmorphs) from genetically different animals of the same species were positioned next to each other. After approximately 8 days in culture, one of the primmorphs underwent apoptotic death, while the second remained alive. The expression levels of the aforementioned genes were determined by Northern blotting and by in situ hybridization. These experiments revealed that in the apoptotic primmorph, the characteristic apoptotic genes were expressed, while in the non-apoptotic aggregates the cell-survival genes are highly upregulated. Interestingly, the transcript levels of retinoid X receptor were higher in apoptotic primmorphs than in the non-apoptotic aggregate in the assay. Our data show for the first time that in the in vitro MSCR system, allogeneic recognition led to apoptotic cell death in one partner, while the other one survived. We suggest that this process is controlled by a differential expression of the pro-apoptotic and pro-survival genes studied here.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Adams JM, Cory S (1998) The Bcl-2 protein family: arbiters of cell survival. Science 281:1322–1326

    Article  CAS  PubMed  Google Scholar 

  • Adell T, Nefkens I, Müller WEG (2003) Polarity factor “Frizzled” in the demosponge Suberites domuncula: identification, expression and localization of the receptor in the epithelium/pinacoderm. FEBS Lett 554:363–368

    Article  CAS  PubMed  Google Scholar 

  • Adell T, Wiens M, Korzhev M, Perović-Ottstadt S, Gamulin V, Müller WEG (2004) Evolution of metazoan tight junction proteins: the scaffold protein MAGI and the transmembrane receptor tetraspanin in the demosponge Suberites domuncula. J Mol Evol 59:41–50

    Article  CAS  PubMed  Google Scholar 

  • Aubry L, Mattei S, Blot B, Sadoul R, Satre M, Klein G (2002) Biochemical characterization of two analogues of the apoptosis-linked gene 2 protein in Dictyostelium discoideum and interaction with a physiological partner in mammals, murine Ali. J Biol Chem 277:21947–21954

    Article  CAS  PubMed  Google Scholar 

  • Ausubel FM, Brent R, Kingston RE, Moore DD, Smith JA, Seidmann JG, Struhl K (1995) Current protocols in molecular biology. Wiley, New York

    Google Scholar 

  • Blumbach B, Diehl-Seifert B, Seack J, Steffen R, Müller IM, Müller WEG (1999) Cloning and expression of new receptors belonging to the immunoglobulin superfamily from the marine sponge Geodia cydonium. Immunogenetics 49:751–763

    Article  CAS  PubMed  Google Scholar 

  • Clem RJ et al (1998) Modulation of cell death by Bcl-XL through caspase interaction. Proc Natl Acad Sci USA 95:554–559

    Article  CAS  PubMed  Google Scholar 

  • Coligan JE, Dunn BM, Ploegh HL, Speicher DW, Wingfield PT (2000) Current protocols in protein science. Wiley, Chichester, pp 2.0.1–2.8.17

    Google Scholar 

  • Custodio MR, Prokic I, Steffen R, Koziol C, Borojevic R, Brümmer F, Nickel M, Müller WEG (1998) Primmorphs generated from dissociated cells of the sponge Suberites domuncula: a model system for studies of cell proliferation and cell death. Mech Ageing Develop 105:45–59

    Article  CAS  Google Scholar 

  • Dayhoff MO, Schwartz RM, Orcutt BC (1978) A model of evolutionary change in protein. In: Dayhoff MO (ed) Atlas of protein sequence and structure. National Biomedical Research Foundation, Washington, pp 345–352

    Google Scholar 

  • Earnshaw WC, Martins LM, Kaufmann SH (1999) Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 68:383–424

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1993) PHYLIP, ver. 3.5. University of Washington, Seattle

    Google Scholar 

  • Fernandez-Busquets X, Kammerer RA, Burger MM (1996) A 25 kDa protein is the basic unit of the core from the 2×104-kDa aggregation factor responsible for species-specific cell adhesion in the marine sponge Microciona prolifera. J Biol Chem 271:23558–23565

    Article  CAS  PubMed  Google Scholar 

  • Gallois P, Makishima T, Hechtt V, Despres B, Laudie M, Nishimoto T, Cooke R (1997) An Arabidopsis thaliana cDNA complementing a hamster suppressor mutant. Plant J 11:1325–1331

    Article  CAS  PubMed  Google Scholar 

  • Gamulin V, Müller IM, Müller WEG (2000) Sponge proteins are more similar to those of Homo sapiens than to Caenorhabditis elegans. Biol J Linn Soc 71:821–828

    Article  Google Scholar 

  • Grant RE (1826) Beobachtungen und Versuche über die Bildung und die Funktion des See-Schwammes (Spongia). Notizen aus dem Gebiete der Natur- und Heilkunde 13:226–231

    Google Scholar 

  • Gross A, McDonnell JM, Korsmeyer SJ (1999) Bcl-2 family members and their mitochondria in apoptosis. Genes Dev 13:1899–1911

    CAS  PubMed  Google Scholar 

  • Hwang IS, Jung YS, Kim E (2002) Interaction of ALG-2 with ASK1 influences ASK1 localization and subsequent JNK activation. FEBS Lett 529:183–187

    Article  CAS  PubMed  Google Scholar 

  • Jung YS, Kim KS, Kim KD, Lim JS, Kim JW, Kim E (2001) Apoptosis-linked gene 2 binds to the death domain of Fas and dissociates from Fas during Fas-mediated apoptosis in Jurkat cells. Biochem Biophys Res Commun 288:420–426

    Article  CAS  PubMed  Google Scholar 

  • Kissane JM, Robins E (1958) The fluorimetric measurement of deoxyribonucleic acid in animal tissue with special reference to the central nervous system. J Biol Chem 233:184–188

    CAS  PubMed  Google Scholar 

  • Krasko A, Batel R, Schröder HC, Müller IM, Müller WEG (2000) Expression of silicatein and collagen genes in the marine sponge Suberites domuncula is controlled by silicate and myotrophin. Eur J Biochem 267:4878–4887

    Article  CAS  PubMed  Google Scholar 

  • Krebs J, Saremaslani P, Caduff R (2002) ALG-2: a Ca2+-binding modulator protein involved in cell proliferation and in cell death. Biochim Biophys Acta 1600:68–73

    Article  CAS  PubMed  Google Scholar 

  • Kruse M, Müller IM, Müller WEG (1997) Early evolution of metazoan serine/threonine- and tyrosine kinases: identification of selected kinases in marine sponges. Mol Biol Evol 14:1326–1334

    Google Scholar 

  • Kruse M, Steffen R, Batel R, Müller IM, Müller WEG (1999) Differential expression of allograft inflammatory factor 1 and of glutathione peroxidase during auto- and allograft response in marine sponges. J Cell Sci 112:4305–4313

    CAS  PubMed  Google Scholar 

  • Lee KS, Chung EH, Han JH, Sohn HD, Jin BR (2003) cDNA cloning of a defender against apoptotic cell death 1 (DAD1) homologue, responsible to external temperature stimulus from the spider, Araneus ventricosus, part B. Comp Biochem Physiol 135:117–123

    Google Scholar 

  • Martin SJ, Green DR (1995) Protease activation during apoptosis: death by a thousand cuts? Cell 82:349–352

    Article  CAS  PubMed  Google Scholar 

  • Martin SJ, Bradley JG, Cotter TG (1990) HL-60 cells induced to differentiate towards neutrophils subsequently die via apoptosis. Clin Exp Immunol 79:448–451

    CAS  PubMed  Google Scholar 

  • Moscona AA (1973) Cell aggregation. In: Bittar EE (ed) Cell biology in medicine. Wiley, New York

    Google Scholar 

  • Müller WEG (2003) The origin of metazoan complexity: Porifera as integrated animals. Integr Comp Biol 43:3–10

    Google Scholar 

  • Müller WEG, Müller IM (2003) Origin of the metazoan immune system: identification of the molecules and their functions in sponges. Integr Comp Biol 43:281–292

    Google Scholar 

  • Müller WEG, Blumbach B, Müller IM (1999a) Evolution of the innate and adaptive immune systems: relationships between potential immune molecules in the lowest metazoan phylum [Porifera] and those in vertebrates. Transplantation 68:1215–1227

    PubMed  Google Scholar 

  • Müller WEG, Wiens M, Batel R, Steffen R, Borojevic R, Custodio RM (1999b) Establishment of a primary cell culture from a sponge: primmorphs from Suberites domuncula. Mar Ecol Progr Ser 178:205–219

    Google Scholar 

  • Müller WEG, Krasko A, Skorokhod A, Bünz C, Grebenjuk VA, Steffen R, Batel R, Müller IM, Schröder HC (2002) Histocompatibility reaction in the sponge Suberites domuncula on tissue and cellular level: central role of the allograft inflammatory factor 1. Immunogenetics 54:48–58

    Article  PubMed  Google Scholar 

  • Müller WEG, Wiens M, Adell T, Gamulin V, Schröder HC, Müller IM (2004) The bauplan of the Urmetazoa: the basis of the genetic complexity of Metazoa using the siliceous sponges [Porifera] as living fossils. Int Rev Cytol 235:53–92

    PubMed  Google Scholar 

  • Nakashima T, Sekiguchi T, Kuraoka A, Fukushima K, Shibata Y, Komiyama S, Nishimoto T (1993) Molecular cloning of a human cDNA encoding a novel protein, DAD1, whose defect causes apoptotic cell death in hamster BHK21 cells. Mol Cell Biol 13:6367–6374

    CAS  PubMed  Google Scholar 

  • Nicholas KB, Nicholas HB Jr (1997) GeneDoc: a tool for editing and annotating multiple sequence alignments, version 1.1.004. Distributed by the author: cris.com/~ketchup/genedoc.shtml

  • Pechenik JA (2000) Biology of the invertebrates. McGraw Hill, Boston

    Google Scholar 

  • Perović S, Schröder HC, Sudek S, Grebenjuk VA, Batel R, Štifanić M, Müller IM, Müller WEG (2003) Expression of one sponge Iroquois homeobox gene in primmorphs from Suberites domuncula during canal formation. Evol Develop 5:240–250

    Google Scholar 

  • Polak JM, McGee JD (1998) In situ hybridization. Oxford University Press, Oxford

    Google Scholar 

  • Rao J, Argos P (1986) A conformational preference parameter to predict helices in integral membrane proteins. Biochim Biophys Acta 869:197–214

    CAS  PubMed  Google Scholar 

  • Rothstein TL (2000) Inducible resistance to Fas-mediated apoptosis in B cells. Cell Res 10:245–266

    CAS  PubMed  Google Scholar 

  • Rottmann M, Schröder HC, Gramzow M, Renneisen K, Kurelec B, Dorn A, Friese U, Müller WEG (1987) Specific phosphorylation of proteins in pore complex-laminae from the sponge Geodia cydonium by the homologous aggregation factor and phorbol ester. Role of protein kinase C in the phosphorylation of DNA topoisomerase II. EMBO J 6:3939–3944

    CAS  PubMed  Google Scholar 

  • Sato A, Imaizumi M, Saito T, Yoshinari M, Suzuki H, Hayashi Y, Iinuma K (1999) Detection of apoptosis in acute promyelocytic leukemia cells in vivo during differentiation-induction with all-trans retinoic acid in combination with chemotherapy. Leuk Res 23:827–832

    Article  CAS  PubMed  Google Scholar 

  • Satoh H, Nakano Y, Shibata H, Maki M (2002) The penta-EF-hand domain of ALG-2 interacts with amino-terminal domains of both annexin VII and annexin XI in a Ca2+-dependent manner. Biochim Biophys Acta 1600:61–67

    Article  CAS  PubMed  Google Scholar 

  • Schäcke H, Müller WEG, Gamulin V, Rinkevich B (1994) The Ig superfamily includes members from the lowest invertebrates to the highest vertebrates. Immunol Today 15:497–498

    Article  PubMed  Google Scholar 

  • Schneider TJ, Fischer GM, Donohoe TJ, Colarusso TP, Rothstein TL (1999) A novel gene coding for a Fas apoptosis inhibitory molecule (FAIM) isolated from inducibly Fas-resistant B lymphocytes. J Exp Med 189:949–956

    Article  CAS  PubMed  Google Scholar 

  • Schröder HC, Grebenjuk VA, Binder M, Skorokhod A, Batel R, Hassanein H, Müller WEG (2004a) Functional molecular biodiversity: assessing the immune status of two sponge populations (Suberites domuncula) on the molecular level. Mar Ecol 25(2):93–108

    Article  Google Scholar 

  • Schröder HC, Perović-Ottstadt S, Wiens M, Batel R, Müller IM, Müller WEG (2004b) Differentiation capacity of epithelial cells in the sponge Suberites domuncula. Cell Tissue Res 316:271–280

    Google Scholar 

  • Schütze J, Skorokhod A, Pahler S, Müller IM, Müller WEG (2001) Molecular evolution of metazoan extracellular matrix: cloning and expression of structural proteins from the demosponges Suberites domuncula and Geodia cydonium. J Mol Evol 53:402–415

    Article  PubMed  Google Scholar 

  • Schwarz C, Oberbauer R (2003) The influence of organ donor on early allograft function. Curr Opin Urol 13:99–104

    Article  PubMed  Google Scholar 

  • Scopa CD, Tsamandas AC, Zolota V, Kalofonos HP, Batistatou A, Vagianos C (2003) Potential role of bcl-2 and ki-67 expression and apoptosis in colorectal carcinoma: a clinicopathologic study. Dig Dis Sci 48:1990–1997

    Article  PubMed  Google Scholar 

  • Shibahara K, Asano M, Ishida Y, Aoki T, Koike T, Honjo T (1995) Isolation of a novel gene MA-3 that is induced upon programmed cell death. Gene 166:297–301

    Article  CAS  PubMed  Google Scholar 

  • Silberstein S, Collins PG, Kelleher DJ, Gilmore R (1995) The essential OST2 gene encodes the 16-kD subunit of the yeast oligosaccharyltransferase, a highly conserved protein expressed in diverse eukaryotic organisms. J Cell Biol 131:371–383

    Article  CAS  PubMed  Google Scholar 

  • Spencer H (1867) The principles of biology. Williams and Norgate, London

    Google Scholar 

  • Sugimoto A, Hozak RR, Nakashima T, Nishimoto T, Rothman JH (1995) Dad-1, an endogenous programmed cell death suppressor in Caenorhabditis elegans and vertebrates. EMBO J 14:4434–4441

    CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    CAS  PubMed  Google Scholar 

  • Wagner C, Steffen R, Koziol C, Batel R, Lacorn M, Steinhart H, Simat T, Müller WEG (1998) Apoptosis in marine sponges: a biomarker for environmental stress (cadmium and bacteria). Mar Biol 131:411–421

    Article  CAS  Google Scholar 

  • White E (1996) Life, death, and the pursuit of apoptosis. Genes Dev 10:1–15

    CAS  PubMed  Google Scholar 

  • Wiens M, Koziol C, Hassanein HMA, Batel R, Müller WEG (1998) Expression of the chaperones 14-3-3 and HSP70 induced by PCB 118 (2,3′,4,4′,5-pentachlorobiphenyl) in the marine sponge Geodia cydonium. Mar Ecol Progr Ser 165:247–257

    CAS  Google Scholar 

  • Wiens M, Krasko A, Müller CI, Müller WEG (2000a) Molecular evolution of apoptotic pathways: cloning of key domains from sponges (Bcl-2 homology domains and death domains) and their phylogenetic relationships. J Mol Evol 50:520–531

    CAS  PubMed  Google Scholar 

  • Wiens M, Krasko A, Müller IM, Müller WEG (2000b). Increased expression of the potential proapoptotic molecule DD2 and increased synthesis of leukotriene B4 during allograft rejection in a marine sponge. Cell Death Differ 7:461–469

    Article  CAS  PubMed  Google Scholar 

  • Wiens M, Diehl-Seifert B, Müller WEG (2001) Sponge Bcl-2 homologous protein (BHP2-GC) confers selected stress resistance to human HEK-293 cells. Cell Death Differ 8:887–898

    Article  CAS  PubMed  Google Scholar 

  • Wiens M, Luckas B, Brümmer F, Ammar MSA, Steffen R, Batel R, Diehl-Seifert B, Schröder HC, Müller WEG (2002) Okadaic acid: a potential defense molecule for the sponge Suberites domuncula. Mar Biol 142:213–223

    Google Scholar 

  • Wiens M, Krasko A, Perovic S, Müller WEG (2003a) Caspase-mediated apoptosis in sponges: cloning and function of the phylogenetic oldest apoptotic proteases from Metazoa. Biochim Biophys Acta 1593:179–189

    Article  CAS  PubMed  Google Scholar 

  • Wiens M, Batel R, Korzhev M, Müller WEG (2003b) Retinoid X receptor and retinoic acid response in the marine sponge Suberites domuncula. J Exp Biol 206:3261–3271

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the Deutsche Forschungsgemeinschaft (Mü 348/14-1), the Bundesministerium für Bildung und Forschung (project: Center of Excellence BIOTECmarin), and the International Human Frontier Science Program (RG-333/96-M).

Author information

Authors and Affiliations

  1. Institut für Physiologische Chemie, Abteilung Angewandte Molekularbiologie, Universität Mainz, Duesbergweg 6, 55099, Mainz, Germany

    Matthias Wiens, Sanja Perović-Ottstadt, Isabel M. Müller & Werner E. G. Müller

Authors
  1. Matthias Wiens
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sanja Perović-Ottstadt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Isabel M. Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Werner E. G. Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Werner E. G. Müller.

Additional information

The sequences reported have been deposited in the EMBL database: Suberites domuncula cDNAs coding for Fas apoptotic inhibitory-related molecule FAIM-l_SUBDO (SDFAIM-l) under the accession number AJ632072, the apoptosis-linked gene 2 protein ALG-2l_SUBDO (SDALG-2l) under AJ632071, the Bcl-2 homology protein BHP2_SUBDO (SDBHP2) under AJ632074, and the defender against apoptotic cell death 1-like molecule DAD-1l_SUBDO (SDDAD-1l) under AJ632073

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wiens, M., Perović-Ottstadt, S., Müller, I.M. et al. Allograft rejection in the mixed cell reaction system of the demosponge Suberites domuncula is controlled by differential expression of apoptotic genes. Immunogenetics 56, 597–610 (2004). https://doi.org/10.1007/s00251-004-0718-6

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-004-0718-6

Keywords

Search

Navigation