Skip to main content

Effect of Bacterial Infection on Stem Cell Pattern in Porifera

  • Chapter
  • First Online:

Abstract

Multicellular organisms derived from one common ancestor, the Urmetazoa. The only living fossils, which can testify about the earliest evolutionary processes in Metazoa on the molecular level are sponges (phylum: Porifera). The present study outlines that stem cells may play essential roles in cellular specialization, embryogenesis and sponge Bauplan formation, using the demosponge Suberites domuncula as a model. Data indicate that the archaeocytes represent, besides the germ/embryonic cells, totipotent stem cells. First marker genes have been identified, which are expressed in totipotent stem cells and in cells from gemmules. Furthermore, genes have been described that are characteristic for the three main cell lineages in sponges; they all originate from archaeocytes and are involved in the differentiation of skeletal cells, epithelial cells and contractile cells. Finally it is shown that after exposure to the endotoxin LPS (lipopolysaccharide) a differential gene expression occurs, leading to an upregulation of the gene encoding perforin and a concomitant down-regulation of noggin, a stem cell marker. In parallel with this process an increased phosphorylation of the mitogen-activating protein kinase p38 occurs. This modification of the p38 kinase has been quantified with a novel ELISA assay. Our data suggest that in response to bacterial infection the number of stem cells in sponges decreases.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Adell T, Grebenjuk VA, Wiens M, Müller WEG (2003a) Isolation and characterization of two T-box genes from sponges, the phylogenetically oldest metazoan taxon. Dev Genes Evol 213:421–434

    Article  CAS  Google Scholar 

  • Adell T, Nefkens I, Müller WEG (2003b) 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  Google Scholar 

  • Adell T, Thakur AN, Müller WEG (2007) Isolation and characterization of Wnt pathway-related genes from Porifera. Cell Biol Int 31:939–949

    Article  CAS  Google Scholar 

  • Althoff K, Schütt C, Steffen R, Batel R, Müller WEG (1998) Evidence for a symbiosis between bacteria of the genus Rhodobacter and the marine sponge Halichondria panicea: Harbor also for putatively-toxic bacteria? Mar Biol 130:529–536

    Article  Google Scholar 

  • Beisswenger C, Coyne CB, Shchepetov M, Weiser JN (2007) Role of p38 MAP kinase and transforming growth factor-ß signaling in transepithelial migration of invasive bacterial pathogens. J Biol Chem 282:28700–28708

    Article  CAS  Google Scholar 

  • Bergquist PR (1978) Sponges. University of California Press, Berkeley

    Google Scholar 

  • Böhm M, Schröder HC, Müller IM, Müller WEG, Gamulin V (2000) The mitogen-activated protein kinase p38 pathway is conserved in metazoans: Cloning and activation of p38 of the SAPK2 subfamily from the sponge Suberites domuncula. Biol Cell 92:95–104

    Article  Google Scholar 

  • Böhm M, Hentschel U, Friedrich A, Fieseler L, Steffen R, Gamulin V, Müller IM, Müller WEG (2001) Molecular response of the sponge Suberites domuncula to bacterial infection. Mar Biol 139:1037–1045

    Article  CAS  Google Scholar 

  • Böhm M, Gamulin V, Schröder HC, Müller WEG (2002) Evolution of osmosensing signal transduction in metazoa: Stress activated protein kinases p38 and JNK. Cell Tissue Res 308:431–438

    Article  CAS  Google Scholar 

  • Borojevic R (1966) Étude expérimentale de la différentiation des cellules de l’ éponge au cours de son développement. Dev Biol 14:130–153

    Article  CAS  Google Scholar 

  • Borojevic R (1970) Différenciation cellulaire dans l’embryogenèse et la morphogenèse chez les spongiaires. Symp Zool Soc Lond 25:467–490

    Google Scholar 

  • Borojevic R (1971) Le comportement des cellules d’ éponge lors de processus morphogénétique. Ann Biol 10:533–545

    Google Scholar 

  • Brusca RC, Brusca GJ (1990) Invertebrates. Sunderland, Mass, Sinauer

    Google Scholar 

  • Cai JC, Weiss ML, Rao MS (2004) In search of “stemness”. Exp Hematol 32:585–598

    Article  Google Scholar 

  • Cho HH, Bae YC, Jung JS (2006) Role of Toll-like receptors on human adipose-derived stromal cells. Stem Cells 24:2744–2752

    Article  CAS  Google Scholar 

  • Cory S, Adams JM (1998) Matters of life and death: Programmed cell death at Cold Spring Harbor. Biochim Biophys Acta 1377:R25-R44

    CAS  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 Dev 105:45–59

    Article  CAS  Google Scholar 

  • Davletov BA, Suedhof TC (1993) A single C2 domain from synaptotagmin I is sufficient for high affinity Ca2+/phospholipid binding. J Biol Chem 268:26386–26390

    CAS  Google Scholar 

  • Diaz JP (1977) Transformation histologiques et cytologiques post-traumatiques chez la demosponge Suberites massa Nardo. Bull Museum Natural History Nature (Paris) 445:375–396

    Google Scholar 

  • Diaz JP (1979) Variations, differenciations et functions des categories cellulaires de la demosponge d’eaux saumatres, Suberites massa, Nardo, au cours du cycle biologique annuel et dans des conditions experimentales. Thèse, Université des Sciences et techniques du Languedoc, Montpellier

    Google Scholar 

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

    Google Scholar 

  • Friedrich AB, Merkert H, Fendert T, Hacker J, Proksch P, Hentschel U (1999) Microbial diversity in the marine sponge Aplysina cavernicola (formerly Verongia cavernicola) analyzed by fluorescence in situ hybridisation (FISH). Mar Biol 134:461–470

    Article  Google Scholar 

  • Galliot B, Miller D (2000) Origin of anterior patterning – how old is our head? Trends Genetics 16:1–5

    Article  CAS  Google Scholar 

  • Garrone R (1978) Phylogenesis of Connective Tissue. Morphological Aspects and Biosynthesis of Sponge Intercellular Matrix. Karger S, Basel

    Google Scholar 

  • Grunz H (ed) (2004) The Vertebrate Organizer. Springer Verlag, Berlin, Heidelberg, New York

    Google Scholar 

  • Hoshiyama D, Suga H, Iwabe Y, Koyanagi M, Nikoh N, Kuma K, Matsuda F, Honjo T, Miyata T (1998) Sponge Pax cDNA related to Pax-2/5/8 and ancient gene duplications in the Pax family. J Mol Evol 47:640–648

    Article  CAS  Google Scholar 

  • Jiang Q, Akashi S, Miyake K, Petty HR (2000) Cutting edge: Lipopolysaccharide induces physical proximity between CD14 and Toll-like receptor 4 (TLR4) prior to nuclear translocation of NF-κB. J Immunol 165:3541–3544

    CAS  Google Scholar 

  • Jones L (2001) Stem cells: So what’s in a niche? Curr Biol 11:R484–R486

    Article  CAS  Google Scholar 

  • Krasko A, Schröder HC, Batel R, Grebenjuk VA, Steffen R, Müller IM, Müller WEG (2002) Iron induces proliferation and morphogenesis in primmorphs from the marine sponge Suberites domuncula. DNA Cell Biol 21:67–80

    Article  CAS  Google Scholar 

  • Laurent L (1842) Recherches sur l’hydre et l’éponge d’eau douce. Arthus Bertrand, Paris

    Google Scholar 

  • Lee MS, Kim YJ (2007) Pattern-recognition receptor signaling initiated from extracellular, membrane, and cytoplasmic space. Mol Cells 23:1–10

    CAS  Google Scholar 

  • Müller WEG (2001) How was metazoan threshold crossed: The hypothetical Urmetazoa. Comp Biochem Physiol [A] 129:433–460

    Google Scholar 

  • Müller WEG (2005) Spatial and temporal expression patterns in animals. In: Meyers RA (ed) Encyclopedia of Molecular Cell Biology and Molecular Medicine, vol 13. WILEY-VCH Press, Weinheim. pp 269–309

    Google Scholar 

  • Müller WEG (2006) The stem cell concept in sponges (Porifera): Metazoan traits. Semin Cell Dev Biol 17:481–491

    Article  Google Scholar 

  • Müller WEG, Schäcke H (1996) Characterization of the receptor proteintyrosine kinase gene from–the marine sponge Geodia cydonium. Progr Molec Subcell Biol 17:183–208

    Google Scholar 

  • Müller WEG, Blumbach B, Wagner-Hülsmann C, Lessel U (1997) Galectins in the phylogenetically oldest metazoa, the sponges [Porifera]. Trends Glycosci Glycotechnol 9:123–130

    Google Scholar 

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

    Article  Google Scholar 

  • Müller WEG, Blumbach B, Müller IM (1999b) 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

    Article  Google Scholar 

  • Müller WEG, Perovic S, Wilkesman J, Kruse M, Müller IM, Batel R (1999c) Increased gene expression of a cytokine-related molecule and profilin after activation of Suberites domuncula cells with xenogeneic sponge molecule(s). DNA Cell Biol 18:885–893

    Article  Google Scholar 

  • Müller WEG, Schröder HC, Skorokhod A, Bünz C, Müller IM, Grebenjuk VA (2001) Contribution of sponge genes to unravel the genome of the hypothetical ancestor of Metazoa (Urmetazoa). Gene 276:161–173

    Article  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  CAS  Google Scholar 

  • Müller WEG, Wiens M, Müller IM, Schröder HC (2003a) The chemokine networks in sponges: Potential roles in morphogenesis, immunity and stem cell formation. Prog Mol Subcell Biol 34:103–143

    Google Scholar 

  • Müller WEG, Korzhev M, Le Pennec G, Müller IM, Schröder HC (2003b) Origin of metazoan stem cell system in sponges: First approach to establish the model (Suberites domuncula). Biomol Eng 20:369–379

    Article  CAS  Google Scholar 

  • Müller WEG, Wiens M, Adell T, Gamulin V, Schröder HC, Müller IM (2004) Bauplan of Urmetazoa: Basis for Genetic Complexity of Metazoa. Int Rev Cytol 235:53–92

    Article  Google Scholar 

  • Noll FC (1888) Beiträge zur Naturgeschichte der Kieselschwämme. Abhandlungen Senckenbergische Naturforscher Gesellschaft Frankfurt 2:1–58

    Google Scholar 

  • Nüsslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287:795–801

    Article  Google Scholar 

  • Ogawa K, Ishihara S, Saito Y, Mineta K, Nakazawa M, Ikeo K, Gojobori T, Watanabe K, Agata K (2002) Induction of a noggin-like gene by ectopic DV interaction during planarian regeneration. Dev Biol 250:59–70

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Perović-Ottstadt S, Adell T, Proksch P, Wiens M, Korzhev M, Gamulin V, Müller IM, Müller WEG (2004a) A (1→3)-ß-D-glucan recognition protein from the sponge Suberites domuncula: Mediated activation of fibrinogen-like protein and epidermal growth factor gene expression. Eur J Biochem 271:1924–1937

    Article  CAS  Google Scholar 

  • Perović-Ottstadt S, Ćetković H, Gamulin V, Schröder HC, Kropf K, Moss C, Korzhev M, Diehl-Seifert B, Müller IM, Müller WEG (2004b) Molecular markers for germ cell differentiation in the demosponge Suberites domuncula. Int J Dev Biol 48:293–305

    Article  Google Scholar 

  • Pfeifer K, Haasemann M, Gamulin V, Bretting H, Fahrenholz F, Müller WEG (1993) S-type lectins occur also in invertebrates: High conservation of the carbohydrate recognition domain in the lectin genes from the marine sponge Geodia cydonium. Glycobiology 3:179–184

    Article  CAS  Google Scholar 

  • Pilcher H (2005) Back to our roots. Nature 435:1022–1023

    Article  CAS  Google Scholar 

  • Saitou N, Nei M (1987) Neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  Google Scholar 

  • Schmidt EW, Obraztsova AY, Davidson SK, Faulkner DJ, Haygood MG (2000) Identification of the antifungal peptide-containing symbiont of the marine sponge Theonella swinhoei as a novel delta-proteobacterium, ‘Candidatus Entotheonella palauensis’. Mar Biol 136:969–977

    Article  CAS  Google Scholar 

  • Schmidt O (1862) Die Spongien des Adriatischen Meeres. Engelmann W, Leipzig

    Google Scholar 

  • Schröder HC, Krasko A, Batel R, Skorokhod A, Pahler S, Kruse M, Müller IM, Müller WEG (2000) Stimulation of protein (collagen) synthesis in sponge cells by a cardiac myotrophin-related molecule from Suberites domuncula. FASEB J 14:2022–2031

    Article  Google Scholar 

  • Schröder HC, Krasko A, Le Pennec G, Adell T, Hassanein H, Müller IM, Müller WEG (2003) Silicase, an enzyme which degrades biogenous amorphous silica: Contribution to the metabolism of silica deposition in the demosponge Suberites domuncula. Prog Mol Subcell Biol 33:249–268

    Google Scholar 

  • Schröder HC, Natalio F, Wiens M, Tahir MN, Shukoor MI, Tremel W, Belikov SI, Krasko A, Müller WEG (2008) The 2’-5’-oligoadenylate synthetase in the lowest Metazoa: Isolation, cloning, expression and functional activity in the sponge Lubomirskia baicalensis. Mol Immunol 45:945–953

    Article  CAS  Google Scholar 

  • Schulze FE (1904) Hexactinellida. Wissenschaftliche Ergebnisse der Deutschen Tiefsee-Expedition, vol 4. Fischer-Verlag, Jena

    Google Scholar 

  • Scott MG, Vreugdenhil AC, Buurman WA, Hancock RE, Gold MR (2000) Cutting edge: Cationic antimicrobial peptides block the binding of lipopolysaccharide (LPS) to LPS-binding protein. J Immunol 164:549–553

    CAS  Google Scholar 

  • Seger R, Krebs EG (1995) The MAPK signaling cascade. FASEB J 9:726–735

    CAS  Google Scholar 

  • Segura-Pena D, Lutz S, Monnerjahn C, Konrad M, Lavie A (2007) Binding of ATP to TK1-like enzymes is associated with a conformational change in the quaternary structure. J Mol Biol 369:129–141

    Article  CAS  Google Scholar 

  • Sen S, Kundu G, Mekhail N, Castel J, Misono K, Healy B (1990) Myotrophin: Purification of a novel peptide from spontaneously hypertensive rat heart that influences myocardial growth. J Biol Chem 265:16635–16643

    CAS  Google Scholar 

  • Sewalt RGAB, Vlag J, Gunster MJ, Hamer KM, Blaauwen JL, Satijn DPE, Hendrix T, Driel R, Otte AP (1998) Characterization of interactions between mammalian Polycomb-group proteins Enx/EZH2 and EED suggests the existence of different mammalian Polycomb-group protein complexes. Mol Cell Biol 18:3586–3595

    CAS  Google Scholar 

  • Sil P, Kandaswamy V, Sen S (1998) Increased protein kinase C activity in myotrophin-induced myocyte growth. Circ Res 82:1173–1188

    CAS  Google Scholar 

  • Simpson TL (1984) The cell biology of sponges. Springer-Verlag, New York

    Google Scholar 

  • Smith WC, Harland RM (1992) Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 70:829–840

    Article  CAS  Google Scholar 

  • Smith WC, Knecht AK, Wu M, Harland RM (1993) Secreted noggin protein mimics the Spemann organizer in dorsalizing mesoderm. Nature 361:547–549

    Article  CAS  Google Scholar 

  • Sollas WJ (1888) Tetractinellida. In: Wyville Thomson C (ed) Report on the scientific results of the voyage of HMS Challenger. Eyre & Spottiswoode, London, pp 1–453

    Google Scholar 

  • Thakur NL, Hentschel U, Krasko A, Pabel CT, Anil AC, Müller WEG (2003) Antibacterial activity of the sponge Suberites domuncula and its primmorphs: Potential basis for the defense. Aquat Microb Ecol 31:77–83

    Article  Google Scholar 

  • Ulevitch RJ, Tobias PS (1994) Recognition of endotoxin by cells leading to transmembrane signaling. Curr Opin Immunol 6:125–130

    Article  CAS  Google Scholar 

  • Vacelet J, Vacelet E, Gaino E, Gallissian MF (1994) Bacterial attack of spongin skeleton during the 1986–1990 Mediterranean sponge disease. In Van Soest RWM, Van Kempen TMG, Braekman JC (eds) Sponges in time and space. Balkema, Rotterdam, pp 355–362

    Google Scholar 

  • Valenzuela DM, Economides AN, Rojas E, Lamb TM, Nunez L, Jones P, Ip NY, Espinosa R, Brannan CI, Gilbert DJ, Copeland NG, Jenkins NA, LeBeau MM, Harland RM, Yancopoulos GD (1995) Identification of mammalian noggin and its expression in the adult nervous system. J Neurosci 15:6077–6084

    CAS  Google Scholar 

  • Wagner AJ, Weissman IL (2004) Plasticity of adult stem cells. Cell 116:639–648

    Article  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 

  • Wiens M, Mangoni A, D’Esposito M, Fattorusso E, Korchagina N, Schröder HC, Grebenjuk VA, Krasko A, Batel R, Müller IM, Müller WEG (2003) The molecular basis for the evolution of the metazoan bodyplan: Extracellular matrix-mediated morphogenesis in marine demosponges. J Mol Evol 57:S60-S75

    Article  CAS  Google Scholar 

  • Wiens M, Perović-Ottstadt S, Müller IM, Müller WEG (2004) 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

    Article  CAS  Google Scholar 

  • Wiens M, Korzhev M, Krasko A, Thakur NL, Perović-Ottstadt S, Breter HJ, Ushijima H, Diehl-Seifert B, Müller IM, Müller WEG (2005) Innate immune defense of the sponge Suberites domuncula against bacteria involves a MyD88-dependent signaling pathway: Induction of a perforin-like molecule. J Biol Chem 280:27949–27959

    Article  CAS  Google Scholar 

  • Wiens M, Belikov SI, Kaluzhnaya OV, Krasko A, Schröder HC, Perovic-Ottstadt S, Müller WEG (2006) Molecular control of serial module formation along the apical-basal axis in the sponge Lubomirskia baicalensis: Silicateins, mannose-binding lectin and Mago Nashi. Dev Genes Evol 216:229–242

    Article  CAS  Google Scholar 

  • Wilkinson CR, Garrone R, Vacelet J (1984) Marine sponges discriminate between food bacteria and bacterial symbionts: Electron microscope radioautography and in situ evidence. Proc R Soc Lond B 220:519–528

    Article  Google Scholar 

  • Wilson HV (1907) On some phenomena of coalescence and regeneration in sponges. J Exp Zool 5:245–258

    Article  Google Scholar 

  • Wimmer W, Blumbach B, Diehl-Seifert B, Koziol C, Batel R, Steffen R, Müller IM, Müller WEG (1999a) Increased expression of integrin and receptor tyrosine kinase genes during autograft fusion in the sponge Geodia cydonium. Cell Adhes Commun 7:111–124

    Article  CAS  Google Scholar 

  • Wimmer W, Perovic S, Kruse M, Krasko A, Batel R, Müller WEG (1999b) Origin of the integrin-mediated signal transduction: Functional studies with cell cultures from the sponge Suberites domuncula. Eur J Biochem 178:156–165

    Article  Google Scholar 

  • Wolpert L (1998) Principles of development. Oxford University Press, Oxford

    Google Scholar 

  • Yang H, Young DW, Gusovsky F, Chow JC (2000) Cellular events mediated by bipopolysaccharide-stimulated toll-like receptor 4. MD-2 is required for activation of mitogen-activated protein kinases and Elk-1. J Biol Chem 275:20861–20866.

    Google Scholar 

  • Yoshikawa T, Nagasugi Y, Azuma T, Kato M, Sugano S, Hashimoto K, Masuho Y, Muramatsu M, Seki N (2000) Isolation of novel mouse genes differentially expressed in brain using cDNA microarray. Biochem Biophys Res Comm 275:532–537

    Article  CAS  Google Scholar 

  • Zou GM, Reznikoff-Etiénat MF, Milliez J, Léon W, Hirsch F (2000) Fas-mediated apoptosis of mouse embryo stem cells: Its role during embryonic development. Am J Reprod Immunol 43:240–248

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the Deutsche Forschungsgemeinschaft (WI 2116/2-2), the Bundesministerium für Bildung und Forschung (project C1 20 20: cooperation project WTZ BRA – Health of marine ecosystems (03F0451A), and Center of Excellence BIOTECmarin) and the International Human Frontier Science Program (RG-333/ 96-M).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Werner E.G. Müller .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Müller, W.E. et al. (2009). Effect of Bacterial Infection on Stem Cell Pattern in Porifera. In: Rinkevich, B., Matranga, V. (eds) Stem Cells in Marine Organisms. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-2767-2_13

Download citation

Publish with us

Policies and ethics