Skip to main content
SpringerLink
Log in

Bacterial Epithelial Cell Cross Talk

  • Chapter
Defense of Mucosal Surfaces: Pathogenesis, Immunity and Vaccines

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 236))

Abstract

The ability to bind to epithelial cells is an important determinant of virulence for many pathogenic bacteria. The interaction of enteropathogens with host cells of the intestinal epithelia can lead to either extracellular adhesion or internalization of the microorganisms. Generally, binding to intestinal host cells is essential for the bacteria to resist the fluid flow of the luminal contents. Once bound to the epithelial surface, the bacteria may flourish and establish a micro-colony. However, adhesion also serves as a prerequisite for subsequent invasion. Increasingly, evidence suggests that many enteropathogenic bacteria target specialized antigentransporting membraneous cells (M cells) within the follicle-associated epithelium (FAE) of the Peyer’s patches (Siebers and Finlay 1996). This is a remarkable and somewhat ironical adaptation by the pathogens, because not only are M cells a minority in the epithelial population within the intestine, but they also represent a key element of the gastrointestinal immune system. M cells serve as samplers of the intestinal content by constantly transporting potential antigens from the gut lumen to the underlying lymph tissues. Therefore, it is surprising that several enteropathogens have chosen M cells as their conduit to deeper tissues.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight 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

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Adam T, Arpin M, Prevost MC, Gounon P, Sansonetti PJ (1995) Cytoskeletal rearrangements and the functional role of T-plastin during entry of Shigella flexneri into HeLa cells. J Cell Biol 129:367–81

    Article  PubMed  CAS  Google Scholar 

  • Adam T, Giry M, Boquet P, Sansonetti P (1996) Rho-dependent membrane folding causes Shigella entry into epithelial cells. EMBO J 15:3315–3321

    PubMed  CAS  Google Scholar 

  • Alpuche-Aranda CM, Racoosin EL, Swanson JA, Miller SI (1994) Salmonella stimulate macrophage macropinocytosis and persist within spacious phagosomes. J Exp Med 179:601–8

    Article  PubMed  CAS  Google Scholar 

  • Baumler AJ, Tsolis RM, Heffron F (1996) The lpf fimbrial operon mediates adhesion of Salmonella typhimurium to murine Peyer’s patches. Proc Natl Acad Sci USA 93:279–83

    Article  PubMed  CAS  Google Scholar 

  • Baumler AJ, Tsolis RM, Valentine PJ, Ficht TA, Heffron F (1997) Synergistic effect of mutations in invA and lpfC on the ability of Salmonella typhimurium to cause murine typhoid. Infect Immun 65:2254–9

    PubMed  CAS  Google Scholar 

  • Berendson R, Cheney CP, Schad PA, Boedeker EC (1983) Species-specific binding of purified pili (AF/Rl) from the Escherichia coli RDEC-l to rabbit intestinal mucosa. Gastroenterology 85:837–45

    PubMed  CAS  Google Scholar 

  • Black DS, Bliska JB (1997) Identification of p130Cas as a substrate of Yersinia YopH (Yop51), a bacterial protein tyrosine phosphatase that translocates into mammalian cells and targets focal adhesions. EMBO J 16:2730–44

    Article  PubMed  CAS  Google Scholar 

  • Bliska JB, Falkow S (1992) Bacterial resistance to complement killing mediated by the Ail protein of Yersinia enterocolitica. Proc Natl Acad Sci USA 89:3561–5

    Article  PubMed  CAS  Google Scholar 

  • Carter PB,Collins FM (1974) The route of enteric infection in normal mice. J Exp Med 139:1189–203

    Article  PubMed  CAS  Google Scholar 

  • Chen L-M, Hobbie S, Galan JE (1996) Requirement of CDC42 for Salmonella-induced cytoskeletal and nuclear responses. Science 274:2115–2118

    Article  PubMed  CAS  Google Scholar 

  • Clark MA, Jepson MA, Simmons NL, Hirst BH (1994) Preferential interaction of Salmonella typhimurium with mouse Peyer’s patch M cells. Res Microbiol 145:543–52

    Article  PubMed  CAS  Google Scholar 

  • Clerc P, Sansonetti PJ (1987) Entry of Shigella flexneri into HeLa cells: evidence for directed phagocytosis involving actin polymerization and myosin accumulation. Infect Immun 55:2681–8

    PubMed  CAS  Google Scholar 

  • Collazo CM, Galan JE (1997) The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host cell. Mol Microbiol 24:747–56

    Article  PubMed  CAS  Google Scholar 

  • Cornelis GR, Wolfwatz H (1997) The Yersinia Yop virulon — a bacterial system for subvertin eukaryotic cells. Mol Microbiol 23:861–867

    Article  PubMed  CAS  Google Scholar 

  • Dehio C, Prevost MC, Sansonetti PJ (1995) Invasion of epithelial cells by Shigella flexneri induces tyrosine phosphorylation of cortactin by a pp60c-src-mediated signalling pathway. EMBO J 14:2471–82

    PubMed  CAS  Google Scholar 

  • Donnenberg MS, Kaper JB, Finlay BB (1997) Interactions between enteropathogenic Escherichia coli and host epithelial cells. Trends Microbiol 5:109–114

    Article  PubMed  CAS  Google Scholar 

  • Dytoc M, Fedorko L, Sherman PM (1994) Signal transduction in human epithelial cells infected with attaching and effacing Escherichia coli in vitro. Gastroenterology 106:1150–61

    PubMed  CAS  Google Scholar 

  • Fiederling F, Boury M, Petit C, Milon A (1997) Adhesive factor/rabbit 2, a new fimbrial adhesion and a virulence factor from Escherichia coli 0103, a serogroup enteropathogenic for rabbits. Infect Immun 65:847–51

    PubMed  CAS  Google Scholar 

  • Finlay BB (1994) Molecular and cellular mechanisms of Salmonella pathogenesis. Curr Top Micrbiol Immunol 192:163–85

    CAS  Google Scholar 

  • Finlay BB, Falkow S (1990) Salmonella interactions with polarized human intestinal Caco-2 epithelial cells. J Infect Dis 162:1096–106

    Article  PubMed  CAS  Google Scholar 

  • Finlay BB, Gumbiner B, Falkow S (1988) Penetration of Salmonella through a polarized Madin-Darby canine kidney epithelial cell monolayer. J Cell Biol 107:221–30

    Article  PubMed  CAS  Google Scholar 

  • Finlay BB, Ruschkowski S, Dedhar S (1991) Cytoskeletal rearrangements accompanying Salmonella entry into epithelial cells. J Cell Sci 99:283–96

    PubMed  Google Scholar 

  • Finlay BB, Rosenshine I, Donnenberg MS, Kaper JB (1992) Cytoskeletal composition of attaching and effacing lesions associated with enteropathogenic Escherichia coli adherence to HeLa cells. Infect Immun 60:2541–3

    PubMed  CAS  Google Scholar 

  • Foubister V, Rosenshine I, Finlay BB (1994) A diarrheal pathogen, enteropathogenic Escherichia coli (EPEC), triggers a flux of inositol phosphates in infected epithelial cells. J Exp Med 179:993–8

    Article  PubMed  CAS  Google Scholar 

  • Francis CL, Ryan TA, Jones BD, Smith SJ, Falkow S (1993) Ruffles induced by Sahnonella and other stimuli direct macropinocytosis of bacteria. Nature 364:639–42

    Article  PubMed  CAS  Google Scholar 

  • Galan JE (1996) Molecular genetic bases of Salmonella entry into host cells. Mol Microbiol 20:263–271

    Article  PubMed  CAS  Google Scholar 

  • Galan JE, Pace J, Hayman MJ (1992) Involvement of the epidermal growth factor receptor in the invasion of cultured mammalian cells by Salmonella typhimurium. Nature 357:588–9

    Article  PubMed  CAS  Google Scholar 

  • Galyov EE, Hakansson S, Forsberg A, Wolf-Watz H (1993) A secreted protein kinase of Yersinia pseudotuberculosis is an indispensable virulence determinant. Nature 361:730–2

    Article  PubMed  CAS  Google Scholar 

  • Garcia-del Portillo F, Finlay BB (1994) Salmonella invasion of nonphagocytic cells induces formation of macropinosomes in the host cell. Infect Immun 62:4641–5

    PubMed  CAS  Google Scholar 

  • Ginocchio CC, Galan JE (1995) Functional conservation among members of the Salmonella typhimurium InvA family of proteins. Infect Immun 63:729–32

    PubMed  CAS  Google Scholar 

  • Ginocchio CC, Olmsted SB, Wells CL, Galan JE (1994) Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium. Cell 76:717–24

    Article  PubMed  CAS  Google Scholar 

  • Hermant D, Menard R, Arricau N, Parsot C, Popoff MY (1995) Functional conservation of the Salmonella and Shigella effectors of entry into epithelial cells. Mol Microbiol 17:781–789

    Article  PubMed  CAS  Google Scholar 

  • Hueck CJ, Hantman MJ, Bajaj V, Johnston C, Lee CA, Miller SI (1995) Salmonella typhimurium secreted invasion determinants are homologous to Shigella Ipa proteins. Mol Microbiol 18:479–90

    Article  PubMed  CAS  Google Scholar 

  • Isberg RR, Falkow S (1985) A single genetic locus encoded by Yersinia pseudotuberculosis permits invasion of cultured animal cells by Escherichia coli K-12. Nature 317:262–4

    Article  PubMed  CAS  Google Scholar 

  • Isberg RR, Leong JM (1990) Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60:861–71

    Article  PubMed  CAS  Google Scholar 

  • Isberg RR, Voorhis DL, Fa1kow S (1987) Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell 50:769–78

    Article  PubMed  CAS  Google Scholar 

  • Jerse AE, Yu J, Tall BD, Kaper JB (1990) A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc Natl Acad Sci USA 87:7839–43

    Article  PubMed  CAS  Google Scholar 

  • Jones BD, Paterson HF, Hall A, Falkow S (1993) Salmonella typhimurium induces membrane ruffling by a growth factor-receptor-independent mechanism. Proc Natl Acad Sci USA 90:10390–4

    Article  PubMed  CAS  Google Scholar 

  • Jones BD, Ghori N, Falkow S (1994) Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer’s patches. J Exp Med 180:15–23

    Article  PubMed  CAS  Google Scholar 

  • Kaniga K, Trollinger D, Galan JE (1995a) Identification of two targets of the type III protein secretion system encoded by the inv and spa loci of Salmonella typhimurium that have homology to the Shigella IpaD and IpaA proteins. J Bacteriol 177:7078–85

    PubMed  CAS  Google Scholar 

  • Kaniga K, Tucker S, Trollinger D, Galan JE (1995b) Homologs of the Shigella IpaB and IpaC invasins are required for Salmonella typhimurium entry into cultured epithelial cells. J Bacteriol 177:3965–71

    PubMed  CAS  Google Scholar 

  • Kenny B, Devinney R, Stein M, Reinscheid DJ, Frey EA, Finlay BB (1997) Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91:511–520

    Article  PubMed  CAS  Google Scholar 

  • Kenny B, Finlay BB (1998) Intimin-dependent binding of enteropathogenic Escherichia coli to host cells triggers novel signaling events, including tyrosine phosphorylation of phospholipase C gamma. Infection and Immunity 65:2528–2536

    Google Scholar 

  • Kerneis S, Bogdanova A, Kraehenbuhl JP, Pringault E (1997) Conversion by Peyer’s patch lymphocytes of human enterocytes into M cells that transport bacteria [see comments]. Science 277:949–52

    Article  PubMed  CAS  Google Scholar 

  • Kohbata S, Yokoyama H, Yabuuchi E (1986) Cytopathogenic effect of Salmonella typhi GIFU 10007 on M cells of murine ileal Peyer’s patches in ligated ileal loops: an ultrastructural study. Micrbiol Immunol 30:1225–37

    CAS  Google Scholar 

  • Lee CA (1996) Pathogenicity islands and the evolution of bacterial pathogens. Infectious Agents Dis 5:1–7

    CAS  Google Scholar 

  • Leong JM, Morrissey PE, Marra A, Isberg RR (1995) An aspartate residue of the Yersinia pseudotuberculosis invasin protein that is critical for integrin binding. EMBO J 14:422–31

    PubMed  CAS  Google Scholar 

  • Leung KY, Straley SC (1989) The yopM gene of Yersinia pestis encodes a released protein having homology with the human platelet surface protein GPIb alpha. J Bacteriol 171:4623–32

    PubMed  CAS  Google Scholar 

  • Lockman HA, Curtiss R (1992) Isolation and characterization of conditional adherent and non-type 1 fimbriated Salmonella typhimurium mutants. Mol Microbiol 6:933–45

    Article  PubMed  CAS  Google Scholar 

  • Marra A, Isberg RR (1997) Invasin-dependent and invasin-independent pathways for translocation of Yersinia pseudotuberculosis across the Peyer’s patch intestinal epithelium. Infect Immun 65:3412–21

    PubMed  CAS  Google Scholar 

  • McDaniel TK, Jarvis KG, Donnenberg MS, Kaper JB (1995) A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci USA 92:1664–8

    Article  PubMed  CAS  Google Scholar 

  • McNeil A, Dunstan SJ, Clark S, Strugnell RA (1995) Salmonella typhimurium displays normal invasion of mice with defective epidermal growth factor receptors. Infect Immun 63:2770–2

    PubMed  CAS  Google Scholar 

  • Menard R, Dehio C, Sansonetti PJ (1996a) Bacterial entry into epithelial cells: the paradigm of Shigella. Trends Microbiol 4:220–225

    Article  PubMed  CAS  Google Scholar 

  • Menard R, Prevost MC, Gounon P, Sansonetti P, Dehio C (l996b) The secreted Ipa complex of Shigella flexneri promotes entry into mammalian cells. Proc Natl Acad Sci USA 93:1254–8

    Article  Google Scholar 

  • Miller VL, Falkow S (1988) Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells. Infect Immun 56:1242–8

    PubMed  CAS  Google Scholar 

  • Mills SD, Bolan A, Sory MP, Vandersmissen P, Kerbourch C, Finlay BB, Cornelis GR (1997) Yersinia enterocolitica induces apoptosis in macrophages by a process requiring functional type III secretion and translocation mechanisms and involving YopP, presumably acting as an effector protein. Proc Natl Acad Sci USA 94:12638–12643

    Article  PubMed  CAS  Google Scholar 

  • Monack DM, Mecsas J, Ghori N, Falkow S (1997) Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death. Proc Natl Acad Sci USA 94:10385–90

    Article  PubMed  CAS  Google Scholar 

  • Mounier J, Vasselon T, Hellio R, Lesourd M, Sansonetti PJ (1992) Shigella flexneri enters human colonic Caco-2 epithelial cells through the basolateral pole. Infect Immun 60:237–48

    PubMed  CAS  Google Scholar 

  • Pace J, Hayman MJ, Galan JE (1993) Signal transduction and invasion of epithelial cells by S. typhimurium. Cell 72:505–14

    Article  PubMed  CAS  Google Scholar 

  • Penheiter KL, Mathur N, Giles D, Fahlen T, Jones BD (1997) Non-invasive Salmonella typhimurium mutants are avirulent because of an inability to enter and destroy M cells of ileal Peyer’s patches. Mol Microbiol 24:697–709

    Article  PubMed  CAS  Google Scholar 

  • Pepe JC, Wachtel MR, Wagar E, Miller VL (1995) Pathogenesis of defined invasion mutants of Yersinia enterocolitica in a BALB/c mouse model of infection. Infect Immun 63:4837–48

    PubMed  CAS  Google Scholar 

  • Perdomo JJ, Gounon P, Sansonetti PJ (1994a) Polymorphonuclear leukocyte transmigration promotes invasion of colonic epithelial monolayer by Shigella flexneri. J Clin Invest 93:633–43

    Article  PubMed  CAS  Google Scholar 

  • Perdomo OJ, Cavaillon JM, Huerre M, Ohayon H, Gounon P, Sansonetti PJ (1994b) Acute inflammation causes epithelial invasion and mucosal destruction in experimental shigellosis. J Exp Med 180:130719

    Article  Google Scholar 

  • Persson C, Carballeira N, Wolf-Watz H, Fallman M (1997) The PTPase YopH inhibits uptake of Yersinia, tyrosine phosphorylation of p130Cas and FAK, and the associated accumulation of these proteins in peripheral focal adhesions. EMBO J 16:2307–18

    Article  PubMed  CAS  Google Scholar 

  • Rosenshine I, Donnenberg MS, Kaper JB, Finlay BB (1992) Signal transduction between enteropathogenic Escherichia coli (EPEC) and epithelial cells: EPEC induces tyrosine phosphorylation of host cell proteins to initiate cytoskeletal rearrangement and bacterial uptake. EMBO J 11:3551–60

    PubMed  CAS  Google Scholar 

  • Rosenshine I, Ruschkowski S, Foubister V, Finlay BB (1994) Salmonella typhimurium invasion of epithelial cells: role of induced host cell tyrosine protein phosphorylation. Infect Immun 62:4969–74

    PubMed  CAS  Google Scholar 

  • Rosenshine I, Ruschkowski S, Stein M, Reinscheid DJ, Mills SD, Finlay BB (1996) A pathogenic bacterium triggers epithelial signals to form a functional bacterial receptor that mediates actin pseudopod formation. EMBO J 15:2613–2624

    PubMed  CAS  Google Scholar 

  • Rosqvist R, Forsberg A, Rimpilainen M, Bergman T, Wolf-Watz H (1990) The cytotoxic protein YopE of Yersinia obstructs the primary host defence. Mol Microbiol 4:657–67

    Article  PubMed  CAS  Google Scholar 

  • Rosqvist R, Forsberg A, Wolf-Watz H (1991) Intracellular targeting of the Yersinia YopE cytotoxin in mammalian cells induces actin micro filament disruption. Infect Immun 59:4562–9

    PubMed  CAS  Google Scholar 

  • Rosqvist R, Skurnik M, Wolf-Watz H (1988) Increased virulence of Yersinia pseudotuberculosis by two independent mutations. Nature 334:522–4

    Article  PubMed  CAS  Google Scholar 

  • Ruschkowski S, Rosenshine I, Finlay BB (1992) Salmonella typhimurium induces an inositol phosphate flux in infected epithelial cells. FEMS Microbiol Lett 74:121–6

    Article  PubMed  CAS  Google Scholar 

  • Schulze-Koops H, Burkhardt H, Heesemann J, Kirsch T, Swoboda B, Bull C, Goodman S, Emmrich F (1993) Outer membrane protein YadA of enteropathogenic yersiniae mediates specific binding to cellular but not plasma fibronectin. Infect Immun 61:2513–9

    PubMed  CAS  Google Scholar 

  • Schulze-Koops H, Burkhardt H, Heesemann J, von der Mark K, Emmrich F (1992) Plasmid-encoded outer membrane protein YadA mediates specific binding of enteropathogenic yersiniae to various types of collagen. Infect Immun 60:2153–9

    PubMed  CAS  Google Scholar 

  • Siebers A, Finlay BB (1996) M cells and the pathogenesis of mucosal and systemic infections. Trends Microbiol 4:22–9

    Article  PubMed  CAS  Google Scholar 

  • Simonet M, Falkow S (1992) Invasin expression in Yersinia pseudotuberculosis. Infect Immun 60:4414–7

    PubMed  CAS  Google Scholar 

  • Straley SC, Plano GV, Skrzypek E, Haddix PL, Fields KA (1993) Regulation by Ca2+ in the Yersinia low-Ca2+ response. [Review] Mol Microbiol 8:1005–10

    Article  PubMed  CAS  Google Scholar 

  • Tran Van Nhieu G, Ben-Ze’ev A, Sansonetti PJ (1997) Modulation of bacterial entry into epithelial cells by association between vinculin and the Shigella IpaA invasin. EMBO J 16:2717–29

    Article  PubMed  CAS  Google Scholar 

  • Watarai M, Funato S, Sasakawa C (1996) Interaction of ipa proteins of Shigella flexneri with alpha(5)beta(1) integrin promotes entry of the bacteria into mammalian cells. J Exp Med 183:991–999

    Article  PubMed  CAS  Google Scholar 

  • Watarai M, Kamata Y, Kozaki S, Sasakawa C (1997) Rho, a small gtp-binding protein, is essential for shigella invasion of epithelial cells. J Exp Med 185:281–292

    Article  PubMed  CAS  Google Scholar 

  • Wood MW, Rosqvist R, Mullan PB, Edwards MH, Galyov EE (1996) SopE, a secreted protein of Salmonella dublin, is translocated into the target eukaryotic cell via a sip-dependent mechanism and promotes bacterial entry. Mol Microbiol 22:327–38

    Article  PubMed  CAS  Google Scholar 

  • Yang Y, Isberg RR (1993) Cellular internalization in the absence of invasin expression is promoted by the Yersinia pseudotuberculosis yadA product. Infect Immun 61:3907–13

    PubMed  CAS  Google Scholar 

  • Zhang QY, DeRyckere D, Lauer P, Koomey M (1992) Gene conversion in Neisseria gonorrhoeae: evidence for its role in pilus antigenic variation. Proc Natl Acad Sci USA 89:5366–70

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology and Immunology, Stanford University, Stanford, CA, 94305, USA

    B. Raupach, J. Mecsas & S. Falkow

  2. Department of Immunology, Max-Planck Institut für Infektionsbiologie, 10117, Berlin, Germany

    B. Raupach

  3. Biotechnology Laboratory, University of British Columbia, #237-6174 University Blvd, V6T-1Z3, Vancouver, BC, Canada

    U. Heczko & B. B. Finlay

  4. Rocky Mountain Laboratory, Hamilton, MT, 59840, USA

    S. Falkow

Authors
  1. B. Raupach
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Mecsas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. U. Heczko
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. Falkow
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. B. B. Finlay
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Swiss Institute for Experimental Cancer Research Institute of Biochemistry, University of Lausanne, Ch. des Boveresses 155, CH-1066, Epalinges, Switzerland

    Jean-Pierre Kraehenbuhl

  2. GI Cell Biology Laboratory, Children’s Hospital and Harvard Medical School, 300 Longwood Ave., Boston, MA, 02115, USA

    Marian R. Neutra

Rights and permissions

Reprints and permissions

Copyright information

© 1999 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Raupach, B., Mecsas, J., Heczko, U., Falkow, S., Finlay, B.B. (1999). Bacterial Epithelial Cell Cross Talk. In: Kraehenbuhl, JP., Neutra, M.R. (eds) Defense of Mucosal Surfaces: Pathogenesis, Immunity and Vaccines. Current Topics in Microbiology and Immunology, vol 236. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-59951-4_8

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-59951-4_8

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-64194-7

  • Online ISBN: 978-3-642-59951-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation