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Evaluation of the role of the endocytic receptor L-SIGN for cytoadhesion of Plasmodium falciparum-infected erythrocytes

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Abstract

Hepatic cell populations play an important role during the malaria life cycle. L-SIGN, a homologue of DC-SIGN, mediating leukocyte and pathogen binding, is selectively expressed on liver endothelial cells. Here, we present evidence that L-SIGN acts as an endocytic cell surface receptor. However, P. falciparum-infected erythrocytes did not cytoadhere to L-SIGN. Thus, L-SIGN contributes to elimination of mannosylated ligands but does not participate in hepatic clearance of P. falciparum-infected erythrocytes.

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References

  • Aikawa M, Iseki M, Barnwell JW, Taylor D, Oo MM, Howard RJ (1990) The pathology of human cerebral malaria. Am J Trop Med Hyg 43(2Pt2):30–37

    CAS  PubMed  Google Scholar 

  • Andrews KT, Pirrit LA, Przyborski JM, Sanchez CP, Sterkers Y, Ricken S, Wickert H, Lepolard C, Avril M, Scherf A, Gysin J, Lanzer M (2003a) Recovery of adhesion to chondroitin-4-sulphate in Plasmodium falciparum var CSA disruption mutants by antigenically similar PfEMP1 variants. Mol Microbiol 49(3):655–669

    Article  CAS  PubMed  Google Scholar 

  • Andrews KT, Viebig NK, Wissing F, Klatt N, Oster N, Wickert H, Knolle P, Lanzer M (2003b) A human schwannoma cell line supports the in vitro adhesion of Plasmodium falciparum infected erythrocytes to chondroitin-4-sulfate. Parasitol Res 89(3):188–193

    CAS  PubMed  Google Scholar 

  • Baruch DI, Pasloske BL, Singh HB, Bi X, Ma XC, Feldman M, Taraschi TF, Howard RJ (1995) Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell 82(1):77–87

    Article  CAS  PubMed  Google Scholar 

  • Bashirova AA, Geijtenbeek TB, van Duijnhoven GC, van Vliet SJ, Eilering JB, Martin MP, Wu L, Martin TD, Viebig N, Knolle PA, KewalRamani VN, van Kooyk Y, Carrington M (2001) A dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin (DC-SIGN)-related protein is highly expressed on human liver sinusoidal endothelial cells and promotes HIV-1 infection. J Exp Med 193(6):671–678

    Article  CAS  PubMed  Google Scholar 

  • Berendt AR, Ferguson DJ, Gardner J, Turner G, Rowe A, McCormick C, Roberts D, Craig A, Pinches R, Elford BC et al (1994) Molecular mechanisms of sequestration in malaria. Parasitology 108(Suppl):S19–S28

    PubMed  Google Scholar 

  • Breiner KM, Schaller H, Knolle PA (2001) Endothelial cell-mediated uptake of a hepatitis B virus: a new concept of liver targeting of hepatotropic microorganisms. Hepatology 34(4Pt1):803–808

    Article  CAS  PubMed  Google Scholar 

  • Cormier EG, Durso RJ, Tsamis F, Boussemart L, Manix C, Olson WC, Gardner JP, Dragic T (2004) L-SIGN (CD209L) and DC-SIGN (CD209) mediate transinfection of liver cells by hepatitis C virus. Proc Natl Acad Sci U S A 101(39):14067–14072

    Article  CAS  PubMed  Google Scholar 

  • Craig A, Scherf A (2001) Molecules on the surface of the Plasmodium falciparum infected erythrocyte and their role in malaria pathogenesis and immune evasion. Mol Biochem Parasitol 115(2):129–143

    Article  CAS  PubMed  Google Scholar 

  • Engering A, Geijtenbeek TB, van Vliet SJ, Wijers M, van Liempt E, Demaurex N, Lanzavecchia A, Fransen J, Figdor CG, Piguet V, van Kooyk Y (2002) The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J Immunol 168(5):2118–2126

    CAS  PubMed  Google Scholar 

  • Feinberg H, Mitchell DA, Drickamer K, Weis WI (2001) Structural basis for selective recognition of oligosaccharides by DC- SIGN and DC-SIGNR. Science 294(5549):2163–2166

    Article  CAS  PubMed  Google Scholar 

  • Gardner MJ, Shallom SJ, Carlton JM, Salzberg SL, Nene V, Shoaibi A, Ciecko A, Lynn J, Rizzo M, Weaver B, Jarrahi B, Brenner M, Parvizi B, Tallon L, Moazzez A, Granger D, Fujii C, Hansen C, Pederson J, Feldblyum T, Peterson J, Suh B, Angiuoli S, Pertea M, Allen J, Selengut J, White O, Cummings LM, Smith HO, Adams MD, Venter JC, Carucci DJ, Hoffman SL, Fraser CM (2002) Sequence of Plasmodium falciparum chromosomes 2, 10, 11 and 14. Nature 419(6906):531–534

    Article  CAS  PubMed  Google Scholar 

  • Gardner JP, Durso RJ, Arrigale RR, Donovan GP, Maddon PJ, Dragic T, Olson WC (2003) L-SIGN (CD 209L) is a liver-specific capture receptor for hepatitis C virus. Proc Natl Acad Sci U S A 100(8):4498–4503

    Article  CAS  PubMed  Google Scholar 

  • Geijtenbeek TB, Krooshoop DJ, Bleijs DA, van Vliet SJ, van Duijnhoven GC, Grabovsky V, Alon R, Figdor CG, van Kooyk Y (2000a) DC-SIGN-ICAM-2 interaction mediates dendritic cell trafficking. Nat Immunol 1(4):353–357

    Article  CAS  PubMed  Google Scholar 

  • Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, Middel J, Cornelissen IL, Nottet HS, KewalRamani VN, Littman DR, Figdor CG, van Kooyk Y (2000b) DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100(5):587–597

    Article  CAS  PubMed  Google Scholar 

  • Geijtenbeek TB, Torensma R, van Vliet SJ, van Duijnhoven GC, Adema GJ, van Kooyk Y, Figdor CG (2000c) Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100(5):575–585

    Article  CAS  PubMed  Google Scholar 

  • Geijtenbeek TB, Van Vliet SJ, Koppel EA, Sanchez-Hernandez M, Vandenbroucke-Grauls CM, Appelmelk B, Van Kooyk Y (2003) Mycobacteria target DC-SIGN to suppress dendritic cell function. J Exp Med 197(1):7–17

    Article  CAS  PubMed  Google Scholar 

  • Good MF, Kaslow DC, Miller LH (1998) Pathways and strategies for developing a malaria blood-stage vaccine. Annu Rev Immunol 16:57–87

    Article  CAS  PubMed  Google Scholar 

  • Gowda DC, Davidson EA (1999) Protein glycosylation in the malaria parasite. Parasitol Today 15(4):147–152

    Article  CAS  PubMed  Google Scholar 

  • Halary F, Amara A, Lortat-Jacob H, Messerle M, Delaunay T, Houles C, Fieschi F, Arenzana-Seisdedos F, Moreau JF, Dechanet-Merville J (2002) Human cytomegalovirus binding to DC-SIGN is required for dendritic cell infection and target cell trans-infection. Immunity 17(5):653–664

    Article  CAS  PubMed  Google Scholar 

  • Jensen JB (1978) Concentration from continuous culture of erythrocytes infected with trophozoites and schizonts of Plasmodium falciparum. Am J Trop Med Hyg 27(6):1274–1276

    CAS  PubMed  Google Scholar 

  • Knolle PA, Limmer A (2001) Neighborhood politics: the immunoregulatory function of organ-resident liver endothelial cells. Trends Immunol 22(8):432–437

    Article  CAS  PubMed  Google Scholar 

  • Lambros C, Vanderberg JP (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65(3):418–420

    CAS  PubMed  Google Scholar 

  • Limmer A, Ohl J, Kurts C, Ljunggren HG, Reiss Y, Groettrup M, Momburg F, Arnold B, Knolle PA (2000) Efficient presentation of exogenous antigen by liver endothelial cells to CD8+ T cells results in antigen-specific T-cell tolerance. Nat Med 6(12):1348–1354

    Article  CAS  PubMed  Google Scholar 

  • Lozach PY, Lortat-Jacob H, De Lacroix De Lavalette A, Staropoli I, Foung S, Amara A, Houles C, Fieschi F, Schwartz Virelizier JL, Arenzana-Seisdedos F, Altmeyer R (2003) DC-SIGN and L-SIGN are high-affinity binding receptors for hepatitis C Virus glycoprotein E2. J Biol Chem 27:27

    Google Scholar 

  • Menendez C (1995) Malaria during pregnancy: a priority area of malaria research and control. Parasitol Today 11(5):178–183

    Article  CAS  PubMed  Google Scholar 

  • Miller LH, Smith JD (1998) Motherhood and malaria. Nat Med 4(11):1244–1245

    Article  CAS  PubMed  Google Scholar 

  • Morgenstern JP, Land H (1990) Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res 18(12):3587–3596

    CAS  PubMed  Google Scholar 

  • Mota MM, Jarra W, Hirst E, Patnaik PK, Holder AA (2000) Plasmodium chabaudi-infected erythrocytes adhere to CD36 and bind to microvascular endothelial cells in an organ-specific way. Infect Immun 68(7):4135–4144

    Article  CAS  PubMed  Google Scholar 

  • Renia L, Miltgen F, Charoenvit Y, Ponnudurai T, Verhave JP, Collins WE, Mazier D (1988) Malaria sporozoite penetration. A new approach by double staining. J Immunol Methods 112(2):201–205

    Article  CAS  PubMed  Google Scholar 

  • Rowe A, Obeiro J, Newbold CI, Marsh K (1995) Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infect Immun 63(6):2323–2326

    CAS  PubMed  Google Scholar 

  • Scherf A, Hernandez-Rivas R, Buffet P, Bottius E, Benatar C, Pouvelle B, Gysin J, Lanzer M (1998) Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. Embo J 17(18):5418–5426

    Article  CAS  PubMed  Google Scholar 

  • Schroit AJ, Madsen JW, Tanaka Y (1985) In vivo recognition and clearance of red blood cells containing phosphatidylserine in their plasma membranes. J Biol Chem 260(8):5131–5138

    CAS  PubMed  Google Scholar 

  • Smith JD, Chitnis CE, Craig AG, Roberts DJ, Hudson-Taylor DE, Peterson DS, Pinches R, Newbold CI, Miller LH (1995) Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82(1):101–110

    Article  CAS  PubMed  Google Scholar 

  • Su XZ, Heatwole VM, Wertheimer SP, Guinet F, Herrfeldt JA, Peterson DS, Ravetch JA, Wellems TE (1995) The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 82(1):89–100

    Article  CAS  PubMed  Google Scholar 

  • Trager W, Jensen JB (1976) Human malaria parasites in continuous culture. Science 193(4254):673–675

    CAS  PubMed  Google Scholar 

  • Urban BC, Ferguson DJ, Pain A, Willcox N, Plebanski M, Austyn JM, Roberts DJ (1999) Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature 400(6739):73–77

    Article  CAS  PubMed  Google Scholar 

  • Yamada M, Steketee R, Abramowsky C, Kida M, Wirima J, Heymann D, Rabbege J, Breman J, Aikawa M (1989) Plasmodium falciparum associated placental pathology: a light and electron microscopic and immunohistologic study. Am J Trop Med Hyg 41(2):161–168

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant from the European Commission (QLRT-PL-1999-30109). The authors would like to thank Blanche Schwappach and Angelika Kehlenbach (ZMBH) for their help with retroviral expression vectors and FACSorting and Mary Carrington for their antibodies. All experiments were performed in agreement with current German laws.

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Authors and Affiliations

  1. Hygiene Institut, Abteilung Parasitologie, Universität Heidelberg, Im Neuenheimer Feld 324, 69120, Heidelberg, Germany

    Nicola K. Viebig, Katherine T. Andrews & Michael Lanzer

  2. Zentrum für Molekulare Biologie Heidelberg (ZMBH), Im Neuenheimer Feld 282, 69120, Heidelberg, Germany

    Nicola K. Viebig & Percy A. Knolle

  3. Departement of Molecular Cell Biology, Vrije Universiteit Medical Center Amsterdam, 1081, Amsterdam, Netherlands

    Yvette van Kooyk

  4. Institut für Molekulare Medizin und Experimentelle Immunologie, Friedrich-Wilhelms-Universität Bonn, Sigmund-Freud-Str. 25, 53105, Bonn, Germany

    Percy A. Knolle

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  1. Nicola K. Viebig
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  2. Katherine T. Andrews
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  5. Percy A. Knolle
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Correspondence to Percy A. Knolle.

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Viebig, N.K., Andrews, K.T., Kooyk, Y.v. et al. Evaluation of the role of the endocytic receptor L-SIGN for cytoadhesion of Plasmodium falciparum-infected erythrocytes. Parasitol Res 96, 247–252 (2005). https://doi.org/10.1007/s00436-005-1360-4

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  • DOI: https://doi.org/10.1007/s00436-005-1360-4

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