Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1997 Jan;65(1):78–88. doi: 10.1128/iai.65.1.78-88.1997

Host cell heparan sulfate proteoglycans mediate attachment and entry of Listeria monocytogenes, and the listerial surface protein ActA is involved in heparan sulfate receptor recognition.

C Alvarez-Domínguez 1, J A Vázquez-Boland 1, E Carrasco-Marín 1, P López-Mato 1, F Leyva-Cobián 1
PMCID: PMC174559  PMID: 8975895

Abstract

The mechanisms by which the intracellular pathogen Listeria monocytogenes interacts with the host cell surface remain largely unknown. In this study, we investigated the role of heparan sulfate proteoglycans (HSPG) in listerial infection. Pretreatment of bacteria with heparin or heparan sulfate (HS), but not with other glycosaminoglycans, inhibited attachment and subsequent uptake by IC-21 murine macrophages and CHO epithelial-like cells. Specific removal of HS from target cells with heparinase III significantly impaired listerial adhesion and invasion. Mutant CHO cells deficient in HS synthesis bound and internalized significantly fewer bacteria than wild-type cells did. Pretreatment of target cells with the HS-binding proteins fibronectin and platelet factor 4, or with heparinase III, impaired listerial infectivity only in those cells expressing HS. Moreover, a synthetic peptide corresponding to the HS-binding ligand in Plasmodium falciparum circumsporozoite protein (pepPf1) inhibited listerial attachment to IC-21 and CHO cells. A motif very similar to the HS-binding site of pepPf1 was found in the N-terminal region of ActA, the L. monocytogenes surface protein responsible for actin-based bacterial motility and cell-to-cell spread. In the same region of ActA, several clusters of positively charged amino acids which could function as HS-binding domains were identified. An ActA-deficient mutant was significantly impaired in attachment and entry due to altered HS recognition functions. This work shows that specific interaction with an HSPG receptor present on the surface of both professional and nonprofessional phagocytes is involved in L. monocytogenes cytoadhesion and invasion and strongly suggests that the bacterial surface protein ActA may be a ligand mediating HSPG receptor recognition.

Full Text

The Full Text of this article is available as a PDF (310.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alvarez-Dominguez C., Carrasco-Marin E., Leyva-Cobian F. Role of complement component C1q in phagocytosis of Listeria monocytogenes by murine macrophage-like cell lines. Infect Immun. 1993 Sep;61(9):3664–3672. doi: 10.1128/iai.61.9.3664-3672.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bernfield M., Kokenyesi R., Kato M., Hinkes M. T., Spring J., Gallo R. L., Lose E. J. Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu Rev Cell Biol. 1992;8:365–393. doi: 10.1146/annurev.cb.08.110192.002053. [DOI] [PubMed] [Google Scholar]
  3. Cerami C., Frevert U., Sinnis P., Takacs B., Clavijo P., Santos M. J., Nussenzweig V. The basolateral domain of the hepatocyte plasma membrane bears receptors for the circumsporozoite protein of Plasmodium falciparum sporozoites. Cell. 1992 Sep 18;70(6):1021–1033. doi: 10.1016/0092-8674(92)90251-7. [DOI] [PubMed] [Google Scholar]
  4. Cerami C., Frevert U., Sinnis P., Takacs B., Nussenzweig V. Rapid clearance of malaria circumsporozoite protein (CS) by hepatocytes. J Exp Med. 1994 Feb 1;179(2):695–701. doi: 10.1084/jem.179.2.695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Conlan J. W., North R. J. Early pathogenesis of infection in the liver with the facultative intracellular bacteria Listeria monocytogenes, Francisella tularensis, and Salmonella typhimurium involves lysis of infected hepatocytes by leukocytes. Infect Immun. 1992 Dec;60(12):5164–5171. doi: 10.1128/iai.60.12.5164-5171.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cossart P., Mengaud J. Listeria monocytogenes. A model system for the molecular study of intracellular parasitism. Mol Biol Med. 1989 Oct;6(5):463–474. [PubMed] [Google Scholar]
  7. Cottin J., Loiseau O., Robert R., Mahaza C., Carbonnelle B., Senet J. M. Surface Listeria monocytogenes carbohydrate-binding components revealed by agglutination with neoglycoproteins. FEMS Microbiol Lett. 1990 Mar 15;56(3):301–305. doi: 10.1016/s0378-1097(05)80058-8. [DOI] [PubMed] [Google Scholar]
  8. David G. Integral membrane heparan sulfate proteoglycans. FASEB J. 1993 Aug;7(11):1023–1030. doi: 10.1096/fasebj.7.11.8370471. [DOI] [PubMed] [Google Scholar]
  9. Dietrich C. P., Nader H. B., Straus A. H. Structural differences of heparan sulfates according to the tissue and species of origin. Biochem Biophys Res Commun. 1983 Mar 29;111(3):865–871. doi: 10.1016/0006-291x(83)91379-7. [DOI] [PubMed] [Google Scholar]
  10. Domann E., Wehland J., Rohde M., Pistor S., Hartl M., Goebel W., Leimeister-Wächter M., Wuenscher M., Chakraborty T. A novel bacterial virulence gene in Listeria monocytogenes required for host cell microfilament interaction with homology to the proline-rich region of vinculin. EMBO J. 1992 May;11(5):1981–1990. doi: 10.1002/j.1460-2075.1992.tb05252.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dramsi S., Biswas I., Maguin E., Braun L., Mastroeni P., Cossart P. Entry of Listeria monocytogenes into hepatocytes requires expression of inIB, a surface protein of the internalin multigene family. Mol Microbiol. 1995 Apr;16(2):251–261. doi: 10.1111/j.1365-2958.1995.tb02297.x. [DOI] [PubMed] [Google Scholar]
  12. Dramsi S., Lebrun M., Cossart P. Molecular and genetic determinants involved in invasion of mammalian cells by Listeria monocytogenes. Curr Top Microbiol Immunol. 1996;209:61–77. doi: 10.1007/978-3-642-85216-9_4. [DOI] [PubMed] [Google Scholar]
  13. Drevets D. A., Campbell P. A. Roles of complement and complement receptor type 3 in phagocytosis of Listeria monocytogenes by inflammatory mouse peritoneal macrophages. Infect Immun. 1991 Aug;59(8):2645–2652. doi: 10.1128/iai.59.8.2645-2652.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Drevets D. A., Sawyer R. T., Potter T. A., Campbell P. A. Listeria monocytogenes infects human endothelial cells by two distinct mechanisms. Infect Immun. 1995 Nov;63(11):4268–4276. doi: 10.1128/iai.63.11.4268-4276.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Esko J. D., Rostand K. S., Weinke J. L. Tumor formation dependent on proteoglycan biosynthesis. Science. 1988 Aug 26;241(4869):1092–1096. doi: 10.1126/science.3137658. [DOI] [PubMed] [Google Scholar]
  16. Falkow S. Bacterial entry into eukaryotic cells. Cell. 1991 Jun 28;65(7):1099–1102. doi: 10.1016/0092-8674(91)90003-h. [DOI] [PubMed] [Google Scholar]
  17. Falkow S., Isberg R. R., Portnoy D. A. The interaction of bacteria with mammalian cells. Annu Rev Cell Biol. 1992;8:333–363. doi: 10.1146/annurev.cb.08.110192.002001. [DOI] [PubMed] [Google Scholar]
  18. Farber J. M., Peterkin P. I. Listeria monocytogenes, a food-borne pathogen. Microbiol Rev. 1991 Sep;55(3):476–511. doi: 10.1128/mr.55.3.476-511.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Finlay B. B. Cell adhesion and invasion mechanisms in microbial pathogenesis. Curr Opin Cell Biol. 1990 Oct;2(5):815–820. doi: 10.1016/0955-0674(90)90078-s. [DOI] [PubMed] [Google Scholar]
  20. Finlay B. B., Falkow S. Common themes in microbial pathogenicity. Microbiol Rev. 1989 Jun;53(2):210–230. doi: 10.1128/mr.53.2.210-230.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Frevert U., Sinnis P., Cerami C., Shreffler W., Takacs B., Nussenzweig V. Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. J Exp Med. 1993 May 1;177(5):1287–1298. doi: 10.1084/jem.177.5.1287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Friederich E., Gouin E., Hellio R., Kocks C., Cossart P., Louvard D. Targeting of Listeria monocytogenes ActA protein to the plasma membrane as a tool to dissect both actin-based cell morphogenesis and ActA function. EMBO J. 1995 Jun 15;14(12):2731–2744. doi: 10.1002/j.1460-2075.1995.tb07274.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Friederich E., Vancompernolle K., Huet C., Goethals M., Finidori J., Vandekerckhove J., Louvard D. An actin-binding site containing a conserved motif of charged amino acid residues is essential for the morphogenic effect of villin. Cell. 1992 Jul 10;70(1):81–92. doi: 10.1016/0092-8674(92)90535-k. [DOI] [PubMed] [Google Scholar]
  24. Gaillard J. L., Berche P., Frehel C., Gouin E., Cossart P. Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell. 1991 Jun 28;65(7):1127–1141. doi: 10.1016/0092-8674(91)90009-n. [DOI] [PubMed] [Google Scholar]
  25. Gaillard J. L., Berche P., Mounier J., Richard S., Sansonetti P. In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2. Infect Immun. 1987 Nov;55(11):2822–2829. doi: 10.1128/iai.55.11.2822-2829.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Gaillard J. L., Finlay B. B. Effect of cell polarization and differentiation on entry of Listeria monocytogenes into the enterocyte-like Caco-2 cell line. Infect Immun. 1996 Apr;64(4):1299–1308. doi: 10.1128/iai.64.4.1299-1308.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Gaillard J. L., Jaubert F., Berche P. The inlAB locus mediates the entry of Listeria monocytogenes into hepatocytes in vivo. J Exp Med. 1996 Feb 1;183(2):359–369. doi: 10.1084/jem.183.2.359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Goldfine H., Knob C. Purification and characterization of Listeria monocytogenes phosphatidylinositol-specific phospholipase C. Infect Immun. 1992 Oct;60(10):4059–4067. doi: 10.1128/iai.60.10.4059-4067.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Gouin E., Dehoux P., Mengaud J., Kocks C., Cossart P. iactA of Listeria ivanovii, although distantly related to Listeria monocytogenes actA, restores actin tail formation in an L. monocytogenes actA mutant. Infect Immun. 1995 Jul;63(7):2729–2737. doi: 10.1128/iai.63.7.2729-2737.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Goundis D., Reid K. B. Properdin, the terminal complement components, thrombospondin and the circumsporozoite protein of malaria parasites contain similar sequence motifs. Nature. 1988 Sep 1;335(6185):82–85. doi: 10.1038/335082a0. [DOI] [PubMed] [Google Scholar]
  31. Guzman C. A., Rohde M., Chakraborty T., Domann E., Hudel M., Wehland J., Timmis K. N. Interaction of Listeria monocytogenes with mouse dendritic cells. Infect Immun. 1995 Sep;63(9):3665–3673. doi: 10.1128/iai.63.9.3665-3673.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hannah J. H., Menozzi F. D., Renauld G., Locht C., Brennan M. J. Sulfated glycoconjugate receptors for the Bordetella pertussis adhesin filamentous hemagglutinin (FHA) and mapping of the heparin-binding domain on FHA. Infect Immun. 1994 Nov;62(11):5010–5019. doi: 10.1128/iai.62.11.5010-5019.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hardingham T. E., Fosang A. J. Proteoglycans: many forms and many functions. FASEB J. 1992 Feb 1;6(3):861–870. [PubMed] [Google Scholar]
  34. Higashiyama S., Abraham J. A., Klagsbrun M. Heparin-binding EGF-like growth factor stimulation of smooth muscle cell migration: dependence on interactions with cell surface heparan sulfate. J Cell Biol. 1993 Aug;122(4):933–940. doi: 10.1083/jcb.122.4.933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Holt G. D., Pangburn M. K., Ginsburg V. Properdin binds to sulfatide [Gal(3-SO4)beta 1-1 Cer] and has a sequence homology with other proteins that bind sulfated glycoconjugates. J Biol Chem. 1990 Feb 15;265(5):2852–2855. [PubMed] [Google Scholar]
  36. Isaacs R. D. Borrelia burgdorferi bind to epithelial cell proteoglycans. J Clin Invest. 1994 Feb;93(2):809–819. doi: 10.1172/JCI117035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Jackson R. L., Busch S. J., Cardin A. D. Glycosaminoglycans: molecular properties, protein interactions, and role in physiological processes. Physiol Rev. 1991 Apr;71(2):481–539. doi: 10.1152/physrev.1991.71.2.481. [DOI] [PubMed] [Google Scholar]
  38. Kaufmann S. H. Immunity to intracellular bacteria. Annu Rev Immunol. 1993;11:129–163. doi: 10.1146/annurev.iy.11.040193.001021. [DOI] [PubMed] [Google Scholar]
  39. Klagsbrun M., Baird A. A dual receptor system is required for basic fibroblast growth factor activity. Cell. 1991 Oct 18;67(2):229–231. doi: 10.1016/0092-8674(91)90173-v. [DOI] [PubMed] [Google Scholar]
  40. Kocks C., Gouin E., Tabouret M., Berche P., Ohayon H., Cossart P. L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell. 1992 Feb 7;68(3):521–531. doi: 10.1016/0092-8674(92)90188-i. [DOI] [PubMed] [Google Scholar]
  41. Kreft J., Dumbsky M., Theiss S. The actin-polymerization protein from Listeria ivanovii is a large repeat protein which shows only limited amino acid sequence homology to ActA from Listeria monocytogenes. FEMS Microbiol Lett. 1995 Feb 15;126(2):113–121. doi: 10.1111/j.1574-6968.1995.tb07403.x. [DOI] [PubMed] [Google Scholar]
  42. Kuhn M., Goebel W. Identification of an extracellular protein of Listeria monocytogenes possibly involved in intracellular uptake by mammalian cells. Infect Immun. 1989 Jan;57(1):55–61. doi: 10.1128/iai.57.1.55-61.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Lasa I., Cossart P. Actin-based bacterial motility: towards a definition of the minimal requirements. Trends Cell Biol. 1996 Mar;6(3):109–114. doi: 10.1016/0962-8924(96)81001-4. [DOI] [PubMed] [Google Scholar]
  44. Lasa I., David V., Gouin E., Marchand J. B., Cossart P. The amino-terminal part of ActA is critical for the actin-based motility of Listeria monocytogenes; the central proline-rich region acts as a stimulator. Mol Microbiol. 1995 Nov;18(3):425–436. doi: 10.1111/j.1365-2958.1995.mmi_18030425.x. [DOI] [PubMed] [Google Scholar]
  45. Locht C., Bertin P., Menozzi F. D., Renauld G. The filamentous haemagglutinin, a multifaceted adhesion produced by virulent Bordetella spp. Mol Microbiol. 1993 Aug;9(4):653–660. doi: 10.1111/j.1365-2958.1993.tb01725.x. [DOI] [PubMed] [Google Scholar]
  46. Love D. C., Esko J. D., Mosser D. M. A heparin-binding activity on Leishmania amastigotes which mediates adhesion to cellular proteoglycans. J Cell Biol. 1993 Nov;123(3):759–766. doi: 10.1083/jcb.123.3.759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Mengaud J., Braun-Breton C., Cossart P. Identification of phosphatidylinositol-specific phospholipase C activity in Listeria monocytogenes: a novel type of virulence factor? Mol Microbiol. 1991 Feb;5(2):367–372. doi: 10.1111/j.1365-2958.1991.tb02118.x. [DOI] [PubMed] [Google Scholar]
  48. Mengaud J., Ohayon H., Gounon P., Mege R-M, Cossart P. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell. 1996 Mar 22;84(6):923–932. doi: 10.1016/s0092-8674(00)81070-3. [DOI] [PubMed] [Google Scholar]
  49. Mettenleiter T. C., Zsak L., Zuckermann F., Sugg N., Kern H., Ben-Porat T. Interaction of glycoprotein gIII with a cellular heparinlike substance mediates adsorption of pseudorabies virus. J Virol. 1990 Jan;64(1):278–286. doi: 10.1128/jvi.64.1.278-286.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Niebuhr K., Chakraborty T., Rohde M., Gazlig T., Jansen B., Köllner P., Wehland J. Localization of the ActA polypeptide of Listeria monocytogenes in infected tissue culture cell lines: ActA is not associated with actin "comets". Infect Immun. 1993 Jul;61(7):2793–2802. doi: 10.1128/iai.61.7.2793-2802.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Ortega-Barria E., Pereira M. E. A novel T. cruzi heparin-binding protein promotes fibroblast adhesion and penetration of engineered bacteria and trypanosomes into mammalian cells. Cell. 1991 Oct 18;67(2):411–421. doi: 10.1016/0092-8674(91)90192-2. [DOI] [PubMed] [Google Scholar]
  52. Pancake S. J., Holt G. D., Mellouk S., Hoffman S. L. Malaria sporozoites and circumsporozoite proteins bind specifically to sulfated glycoconjugates. J Cell Biol. 1992 Jun;117(6):1351–1357. doi: 10.1083/jcb.117.6.1351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Pistor S., Chakraborty T., Walter U., Wehland J. The bacterial actin nucleator protein ActA of Listeria monocytogenes contains multiple binding sites for host microfilament proteins. Curr Biol. 1995 May 1;5(5):517–525. doi: 10.1016/s0960-9822(95)00104-7. [DOI] [PubMed] [Google Scholar]
  54. Portnoy D. A., Chakraborty T., Goebel W., Cossart P. Molecular determinants of Listeria monocytogenes pathogenesis. Infect Immun. 1992 Apr;60(4):1263–1267. doi: 10.1128/iai.60.4.1263-1267.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Rapraeger A. C. The coordinated regulation of heparan sulfate, syndecans and cell behavior. Curr Opin Cell Biol. 1993 Oct;5(5):844–853. doi: 10.1016/0955-0674(93)90034-n. [DOI] [PubMed] [Google Scholar]
  56. Robson K. J., Hall J. R., Jennings M. W., Harris T. J., Marsh K., Newbold C. I., Tate V. E., Weatherall D. J. A highly conserved amino-acid sequence in thrombospondin, properdin and in proteins from sporozoites and blood stages of a human malaria parasite. Nature. 1988 Sep 1;335(6185):79–82. doi: 10.1038/335079a0. [DOI] [PubMed] [Google Scholar]
  57. Rácz P., Tenner K., Mérö E. Experimental Listeria enteritis. I. An electron microscopic study of the epithelial phase in experimental listeria infection. Lab Invest. 1972 Jun;26(6):694–700. [PubMed] [Google Scholar]
  58. Sandros J., Tuomanen E. Attachment factors of Bordetella pertussis: mimicry of eukaryotic cell recognition molecules. Trends Microbiol. 1993 Aug;1(5):192–196. doi: 10.1016/0966-842x(93)90090-e. [DOI] [PubMed] [Google Scholar]
  59. Schlessinger J., Lax I., Lemmon M. Regulation of growth factor activation by proteoglycans: what is the role of the low affinity receptors? Cell. 1995 Nov 3;83(3):357–360. doi: 10.1016/0092-8674(95)90112-4. [DOI] [PubMed] [Google Scholar]
  60. Schuchat A., Swaminathan B., Broome C. V. Epidemiology of human listeriosis. Clin Microbiol Rev. 1991 Apr;4(2):169–183. doi: 10.1128/cmr.4.2.169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sheehan B., Kocks C., Dramsi S., Gouin E., Klarsfeld A. D., Mengaud J., Cossart P. Molecular and genetic determinants of the Listeria monocytogenes infectious process. Curr Top Microbiol Immunol. 1994;192:187–216. doi: 10.1007/978-3-642-78624-2_9. [DOI] [PubMed] [Google Scholar]
  62. Shieh M. T., WuDunn D., Montgomery R. I., Esko J. D., Spear P. G. Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans. J Cell Biol. 1992 Mar;116(5):1273–1281. doi: 10.1083/jcb.116.5.1273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Sinnis P., Clavijo P., Fenyö D., Chait B. T., Cerami C., Nussenzweig V. Structural and functional properties of region II-plus of the malaria circumsporozoite protein. J Exp Med. 1994 Jul 1;180(1):297–306. doi: 10.1084/jem.180.1.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Smith G. A., Marquis H., Jones S., Johnston N. C., Portnoy D. A., Goldfine H. The two distinct phospholipases C of Listeria monocytogenes have overlapping roles in escape from a vacuole and cell-to-cell spread. Infect Immun. 1995 Nov;63(11):4231–4237. doi: 10.1128/iai.63.11.4231-4237.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Sobel M., Soler D. F., Kermode J. C., Harris R. B. Localization and characterization of a heparin binding domain peptide of human von Willebrand factor. J Biol Chem. 1992 May 5;267(13):8857–8862. [PubMed] [Google Scholar]
  66. Soroka C. J., Farquhar M. G. Characterization of a novel heparan sulfate proteoglycan found in the extracellular matrix of liver sinusoids and basement membranes. J Cell Biol. 1991 Jun;113(5):1231–1241. doi: 10.1083/jcb.113.5.1231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Temm-Grove C. J., Jockusch B. M., Rohde M., Niebuhr K., Chakraborty T., Wehland J. Exploitation of microfilament proteins by Listeria monocytogenes: microvillus-like composition of the comet tails and vectorial spreading in polarized epithelial sheets. J Cell Sci. 1994 Oct;107(Pt 10):2951–2960. doi: 10.1242/jcs.107.10.2951. [DOI] [PubMed] [Google Scholar]
  68. Tilney L. G., Tilney M. S. The wily ways of a parasite: induction of actin assembly by Listeria. Trends Microbiol. 1993 Apr;1(1):25–31. doi: 10.1016/0966-842x(93)90021-i. [DOI] [PubMed] [Google Scholar]
  69. Vancompernolle K., Goethals M., Huet C., Louvard D., Vandekerckhove J. G- to F-actin modulation by a single amino acid substitution in the actin binding site of actobindin and thymosin beta 4. EMBO J. 1992 Dec;11(13):4739–4746. doi: 10.1002/j.1460-2075.1992.tb05579.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Vazquez-Boland J. A., Kocks C., Dramsi S., Ohayon H., Geoffroy C., Mengaud J., Cossart P. Nucleotide sequence of the lecithinase operon of Listeria monocytogenes and possible role of lecithinase in cell-to-cell spread. Infect Immun. 1992 Jan;60(1):219–230. doi: 10.1128/iai.60.1.219-230.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Wang C. L., Wang L. W., Xu S. A., Lu R. C., Saavedra-Alanis V., Bryan J. Localization of the calmodulin- and the actin-binding sites of caldesmon. J Biol Chem. 1991 May 15;266(14):9166–9172. [PubMed] [Google Scholar]
  72. Westerlund B., Korhonen T. K. Bacterial proteins binding to the mammalian extracellular matrix. Mol Microbiol. 1993 Aug;9(4):687–694. doi: 10.1111/j.1365-2958.1993.tb01729.x. [DOI] [PubMed] [Google Scholar]
  73. Wood S., Maroushek N., Czuprynski C. J. Multiplication of Listeria monocytogenes in a murine hepatocyte cell line. Infect Immun. 1993 Jul;61(7):3068–3072. doi: 10.1128/iai.61.7.3068-3072.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Yanagishita M., Hascall V. C. Cell surface heparan sulfate proteoglycans. J Biol Chem. 1992 May 15;267(14):9451–9454. [PubMed] [Google Scholar]
  75. van Putten J. P., Paul S. M. Binding of syndecan-like cell surface proteoglycan receptors is required for Neisseria gonorrhoeae entry into human mucosal cells. EMBO J. 1995 May 15;14(10):2144–2154. doi: 10.1002/j.1460-2075.1995.tb07208.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES