Table of Contents Author Guidelines Submit a Manuscript
Interdisciplinary Perspectives on Infectious Diseases
Volume 2014, Article ID 412827, 12 pages
http://dx.doi.org/10.1155/2014/412827
Research Article

Identification of Sphingomyelinase on the Surface of Chlamydia pneumoniae: Possible Role in the Entry into Its Host Cells

1Helsinki Biophysics & Biomembrane Group, Medical Biochemistry, Institute of Biomedicine, University of Helsinki, 00014 Helsinki, Finland
2Molecular Imaging North Competence Center (MOIN CC), Christian-Albrechts Universität zu Kiel, AmBotanischen Garten 14, 24118 Kiel, Germany
3Turku Centre for Biotechnology, 20520 Turku, Finland
4HUSLAB, Department of Virology, Haartman Institute, University of Helsinki, 00014 Helsinki, Finland
5Helsinki Biophysics & Biomembrane Group, Department of Biomedical Engineering and Computational Science, P.O. Box 12200, Rakentajanaukio 3, 00076 Aalto, Finland

Received 12 November 2013; Accepted 19 January 2014; Published 13 March 2014

Academic Editor: Mary E. Marquart

Copyright © 2014 Tuula A. Peñate Medina et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. H. Grassmé, E. Gulbins, B. Brenner et al., “Acidic sphingomyelinase mediates entry of N. gonorrhoeae into Nonphagocytic cells,” Cell, vol. 91, no. 5, pp. 605–615, 1997. View at Google Scholar · View at Scopus
  2. H. Grassmé, V. Jendrossek, A. Riehle et al., “Host defense against Pseudomonas aeruginosa requires ceramide-rich membrane rafts,” Nature Medicine, vol. 9, no. 3, pp. 322–330, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Esen, B. Schreiner, V. Jendrossek et al., “Mechanisms of Staphylococcus aureus induced apoptosis of human endothelial cells,” Apoptosis, vol. 6, no. 6, pp. 431–439, 2001. View at Publisher · View at Google Scholar · View at Scopus
  4. J. L. Nieva, R. Bron, J. Corver, and J. Wilschut, “Membrane fusion of Semliki Forest virus requires sphingolipids in the target membrane,” EMBO Journal, vol. 13, no. 12, pp. 2797–2804, 1994. View at Google Scholar · View at Scopus
  5. J.-T. Jan, S. Chatterjee, and D. E. Griffin, “Sindbis virus entry into cells triggers apoptosis by activating sphingomyelinase, leading to the release of ceramide,” Journal of Virology, vol. 74, no. 14, pp. 6425–6432, 2000. View at Publisher · View at Google Scholar · View at Scopus
  6. H. Grassmé, A. Riehle, B. Wilker, and E. Gulbins, “Rhinoviruses infect human epithelial cells via ceramide-enriched membrane platforms,” The Journal of Biological Chemistry, vol. 280, no. 28, pp. 26256–26262, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. K. Hanada, N. M. Q. Palacpac, P. A. Magistrado et al., “Plasmodium falciparum phospholipase C hydrolyzing sphingomyelin and lysocholinephospholipids is a possible target for malaria chemotherapy,” Journal of Experimental Medicine, vol. 195, no. 1, pp. 23–34, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. K. A. Johansen, R. E. Gill, and M. L. Vasil, “Biochemical and molecular analysis of phospholipase C and phospholipase D activity in mycobacteria,” Infection and Immunity, vol. 64, no. 8, pp. 3259–3266, 1996. View at Google Scholar · View at Scopus
  9. A. Alape-Girón, M. Flores-Díaz, I. Guillouard et al., “Identification of residues critical for toxicity in Clostridium perfringens phospholipase C, the key toxin in gas gangrene,” European Journal of Biochemistry, vol. 267, no. 16, pp. 5191–5197, 2000. View at Publisher · View at Google Scholar · View at Scopus
  10. P. H. Guddal, T. Johansen, K. Schulstad, and C. Little, “Apparent phosphate retrieval system in Bacillus cereus,” Journal of Bacteriology, vol. 171, no. 10, pp. 5702–5706, 1989. View at Google Scholar · View at Scopus
  11. C. Geoffroy, J. Raveneau, J.-L. Beretti et al., “Purification and characterization of an extracellular 29-kilodalton phospholipase C from Listeria monocytogenes,” Infection and Immunity, vol. 59, no. 7, pp. 2382–2388, 1991. View at Google Scholar · View at Scopus
  12. Y.-L. Lin, J.-S. Liu, K.-T. Chen, C.-T. Chen, and E.-C. Chan, “Identification of neutral and acidic sphingomyelinases in Helicobacter pylori,” FEBS Letters, vol. 423, no. 2, pp. 249–253, 1998. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Artiushin, J. F. Timoney, J. Nally, and A. Verma, “Host-inducible immunogenic sphingomyelinase-like protein, Lk73.5, of Leptospira interrogans,” Infection and Immunity, vol. 72, no. 2, pp. 742–749, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. J. M. Holopainen, M. I. Angelova, and P. K. J. Kinnunen, “Vectorial budding of vesicles by asymmetrical enzymatic formation of ceramide in giant liposomes,” Biophysical Journal, vol. 78, no. 2, pp. 830–838, 2000. View at Google Scholar · View at Scopus
  15. X. Zha, L. M. Pierini, P. L. Leopold, P. J. Skiba, I. Tabas, and F. R. Maxfield, “Sphingomyelinase treatment induces ATP-independent endocytosis,” Journal of Cell Biology, vol. 140, no. 1, pp. 39–47, 1998. View at Publisher · View at Google Scholar · View at Scopus
  16. L. V. Chernomordik, M. M. Kozlov, and J. Zimmerberg, “Lipids in biological membrane fusion,” Journal of Membrane Biology, vol. 146, no. 1, pp. 1–14, 1995. View at Google Scholar · View at Scopus
  17. J. M. Holopainen, J. Y. A. Lehtonen, and P. K. J. Kinnunen, “Lipid microdomains in dimyristoylphosphatidylcholine—ceramide liposomes,” Chemistry and Physics of Lipids, vol. 88, no. 1, pp. 1–13, 1997. View at Publisher · View at Google Scholar · View at Scopus
  18. H. W. Huang, E. M. Goldberg, and R. Zidovetzki, “Ceramide induces structural defects into phosphatidylcholine bilayers and activates phospholipase A2,” Biochemical and Biophysical Research Communications, vol. 220, no. 3, pp. 834–838, 1996. View at Publisher · View at Google Scholar · View at Scopus
  19. J. M. Holopainen, M. Subramanian, and P. K. J. Kinnunen, “Sphingomyelinase induces lipid microdomain formation in a fluid phosphatidylcholine/sphingomyelin membrane,” Biochemistry, vol. 37, no. 50, pp. 17562–17570, 1998. View at Publisher · View at Google Scholar · View at Scopus
  20. J. M. Holopainen, J. Lemmich, F. Richter, O. G. Mouritsen, G. Rapp, and P. K. J. Kinnunen, “Dimyristoylphosphatidylcholine/C16:0-ceramide binary liposomes studied by differential scanning calorimetry and wide- and small-angle X-ray scattering,” Biophysical Journal, vol. 78, no. 5, pp. 2459–2469, 2000. View at Google Scholar · View at Scopus
  21. J. M. Holopainen, H. L. Brockman, R. E. Brown, and P. K. J. Kinnunen, “Interfacial interactions of ceramide with dimyristoylphosphatidylcholine: impact of the N-acyl chain,” Biophysical Journal, vol. 80, no. 2, pp. 765–775, 2001. View at Google Scholar · View at Scopus
  22. P. K. J. Kinnunen, “On the principles of functional ordering in biological membranes,” Chemistry and Physics of Lipids, vol. 57, no. 2-3, pp. 375–399, 1991. View at Google Scholar · View at Scopus
  23. I. Pascher, “Molecular arrangements in sphingolipids. Conformation and hydrogen bonding of ceramide and their implication on membrane stability and permeability,” Biochimica et Biophysica Acta, vol. 455, no. 2, pp. 433–451, 1976. View at Google Scholar · View at Scopus
  24. M. B. Ruiz-Argüello, G. Basáñez, F. M. Goñi, and A. Alonso, “Different effects of enzyme-generated ceramides and diacylglycerols in phospholipid membrane fusion and leakage,” The Journal of Biological Chemistry, vol. 271, no. 43, pp. 26616–26621, 1996. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Shah, J. M. Atienza, A. V. Rawlings, and G. G. Shipley, “Physical properties of ceramides: effect of fatty acid hydroxylation,” Journal of Lipid Research, vol. 36, no. 9, pp. 1945–1955, 1995. View at Google Scholar · View at Scopus
  26. T. A. Nurminen, J. M. Holopainen, H. Zhao, and P. K. J. Kinnunen, “Observation of topical catalysis by sphingomyelinase coupled to microspheres,” Journal of the American Chemical Society, vol. 124, no. 41, pp. 12129–12134, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Dautry-Varsat, M. E. Balañá, and B. Wyplosz, “Chlamydia-host cell interactions: recent advances on bacterial entry and intracellular development,” Traffic, vol. 5, no. 8, pp. 561–570, 2004. View at Publisher · View at Google Scholar
  28. A. Subtil and A. Dautry-Varsat, “Chlamydia: five years A.G. (after genome),” Current Opinion in Microbiology, vol. 7, no. 1, pp. 85–92, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. D. R. Clifton, K. A. Fields, S. S. Grieshaber et al., “A chlamydial type III translocated protein is tyrosine-phosphorylated at the site of entry and associated with recruitment of actin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 27, pp. 10166–10171, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. C.-C. Kuo, M. Puolakkainen, T.-M. Lin, M. Witte, and L. A. Campbell, “Mannose-receptor positive and negative mouse macrophages differ in their susceptibility to infection by Chlamydia species,” Microbial Pathogenesis, vol. 32, no. 1, pp. 43–48, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Puolakkainen, C.-C. Kuo, and L. A. Campbell, “Chlamydia pneumoniae uses the mannose 6-phosphate/insulin-like growth factor 2 receptor for infection of endothelial cells,” Infection and Immunity, vol. 73, no. 8, pp. 4620–4625, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Scidmore-Carlson and T. Hackstadt, “Chlamydia internalization and intracellular fate,” Sub-Cellular Biochemistry, vol. 33, pp. 459–478, 2000. View at Google Scholar · View at Scopus
  33. R. S. Stephens, K. Koshiyama, E. Lewis, and A. Kubo, “Heparin-binding outer membrane protein of Chlamydiae,” Molecular Microbiology, vol. 40, no. 3, pp. 691–699, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Montigiani, F. Falugi, M. Scarselli et al., “Genomic approach for analysis of surface proteins in Chlamydia pneumoniae,” Infection and Immunity, vol. 70, no. 1, pp. 368–379, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. C. Notredame, D. G. Higgins, and J. Heringa, “T-coffee: a novel method for fast and accurate multiple sequence alignment,” Journal of Molecular Biology, vol. 302, no. 1, pp. 205–217, 2000. View at Publisher · View at Google Scholar · View at Scopus
  36. L. Falquet, M. Pagni, P. Bucher et al., “The PROSITE database, its status in 2002,” Nucleic Acids Research, vol. 30, no. 1, pp. 235–238, 2002. View at Google Scholar · View at Scopus
  37. M. R. Ekman, J. T. Grayston, R. Visakorpi, M. Kleemola, C.-C. Kuo, and P. Saikku, “An epidemic of infections due to Chlamydia pneumoniae in military conscripts,” Clinical Infectious Diseases, vol. 17, no. 3, pp. 420–425, 1993. View at Google Scholar · View at Scopus
  38. H. D. Caldwell, J. Kromhout, and J. Schachter, “Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis,” Infection and Immunity, vol. 31, no. 3, pp. 1161–1176, 1981. View at Google Scholar · View at Scopus
  39. M. P. Melgosa, C.-C. Kuo, and L. A. Campbell, “Outer membrane complex proteins of Chlamydia pneumoniae,” FEMS Microbiology Letters, vol. 112, no. 2, pp. 199–204, 1993. View at Publisher · View at Google Scholar · View at Scopus
  40. G. L. Byrne, “Kinetics of phagocytosis of Chlamydia psittaci by mouse fibroblasts (L cells) separation of the attachment and ingestion stages,” Infection and Immunity, vol. 19, no. 2, pp. 607–612, 1978. View at Google Scholar · View at Scopus
  41. F. N. Wuppermann, J. H. Hegemann, and C. A. Jantos, “Heparan sulfate-like glycosaminoglycan is a cellular receptor for Chlamydia pneumoniae,” Journal of Infectious Diseases, vol. 184, no. 2, pp. 181–187, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. S. A. Weston, A. Lahm, and D. Suck, “X-ray structure of the DNase I-d(GGTATACC)2 complex at 2.3 Å resolution,” Journal of Molecular Biology, vol. 226, no. 4, pp. 1237–1256, 1992. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Matsuo, A. Yamada, K. Tsukamoto et al., “A distant evolutionary relationship between bacterial sphingomyelinase and mammalian DNase I,” Protein Science, vol. 5, no. 12, pp. 2459–2467, 1996. View at Google Scholar · View at Scopus
  44. K. Hofmann, S. Tomiuk, G. Wolff, and W. Stoffel, “Cloning and characterization of the mammalian brain-specific, Mg2+-dependent neutral sphingomyelinase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 11, pp. 5895–5900, 2000. View at Google Scholar · View at Scopus
  45. D. Allan and P. Quinn, “Resynthesis of sphingomyelin from plasma-membrane phosphatidylcholine in BHK cells treated with Staphylococcus aureus sphingomyelinase,” Biochemical Journal, vol. 254, no. 3, pp. 765–771, 1988. View at Google Scholar · View at Scopus
  46. K. L. Godzik, E. R. O'Brien, S. K. Wang, and C.-C. Kuo, “In vitro susceptibility of human vascular wall cells to infection with Chlamydia pneumoniae,” Journal of Clinical Microbiology, vol. 33, no. 9, pp. 2411–2414, 1995. View at Google Scholar · View at Scopus
  47. D. Corsaro and D. Venditti, “Emerging chlamydial infections,” Critical Reviews in Microbiology, vol. 30, no. 2, pp. 75–106, 2004. View at Publisher · View at Google Scholar
  48. L. A. Campbell and C. Kuo, “Chlamydia pneumoniae—an infectious risk factor for atherosclerosis?” Nature Reviews Microbiology, vol. 2, no. 1, pp. 23–32, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. P. Saikku, M. Leinonen, K. Mattila et al., “Serological evidence of an association of a novel Chlamydia, TWAR, with chronic coronary heart disease and acute myocardial infarction,” The Lancet, vol. 2, no. 8618, pp. 983–986, 1988. View at Google Scholar · View at Scopus
  50. M. Weinberger, “Respiratory infections and asthma: current treatment strategies,” Drug Discovery Today, vol. 9, no. 19, pp. 831–837, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. F. Blasi, S. Damato, R. Cosentini et al., “Chlamydia pneumoniae and chronic bronchitis: association with severity and bacterial clearance following treatment,” Thorax, vol. 57, no. 8, pp. 672–676, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. O. Moling, S. Pegoretti, M. Rielli et al., “Chlamydia pneumoniae—reactive arthritis and persistent infection,” The British Journal of Rheumatology, vol. 35, no. 11, pp. 1189–1190, 1996. View at Google Scholar · View at Scopus
  53. B. J. Balin, H. C. Gérard, E. J. Arking et al., “Identification and localization of Chlamydia pneumoniae in the Alzheimer's brain,” Medical Microbiology and Immunology, vol. 187, no. 1, pp. 23–42, 1998. View at Publisher · View at Google Scholar · View at Scopus
  54. C.-C. Kuo and T. Grayston, “Interaction of Chlamydia trachomatis organisms and HeLa 229 cells,” Infection and Immunity, vol. 13, no. 4, pp. 1103–1109, 1976. View at Google Scholar · View at Scopus
  55. G. I. Byrne, “Requirements for ingestion of Chlamydia psittaci by mouse fibroblasts (L cells),” Infection and Immunity, vol. 14, no. 3, pp. 645–651, 1976. View at Google Scholar · View at Scopus
  56. J. E. Rothman and J. Lenard, “Membrane asymmetry,” Science, vol. 195, no. 4286, pp. 743–753, 1977. View at Google Scholar · View at Scopus
  57. S. R. Goth and R. S. Stephens, “Rapid, transient phosphatidylserine externalization induced in host cells by infection with Chlamydia spp.,” Infection and Immunity, vol. 69, no. 2, pp. 1109–1119, 2001. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Eda and I. W. Sherman, “Cytoadherence of malaria-infected red blood cells involves exposure of phosphatidylserine,” Cellular Physiology and Biochemistry, vol. 12, no. 5-6, pp. 373–384, 2002. View at Publisher · View at Google Scholar · View at Scopus
  59. Y. A. Hannun and L. M. Obeid, “Ceramide: an intracellular signal for apoptosis,” Trends in Biochemical Sciences, vol. 20, no. 2, pp. 73–77, 1995. View at Publisher · View at Google Scholar · View at Scopus
  60. K. Wolf and T. Hackstadt, “Sphingomyelin trafficking in Chlamydia pneumoniae-infected cells,” Cellular Microbiology, vol. 3, no. 3, pp. 145–152, 2001. View at Publisher · View at Google Scholar · View at Scopus
  61. N. Nagano, E. G. Hutchinson, and J. M. Thornton, “Barrel structures in proteins: automatic identification and classification including a sequence analysis of TIM barrels,” Protein Science, vol. 8, no. 10, pp. 2072–2084, 1999. View at Google Scholar · View at Scopus
  62. R. S. Stephens and C. J. Lammel, “Chlamydia outer membrane protein discovery using genomics,” Current Opinion in Microbiology, vol. 4, no. 1, pp. 16–20, 2001. View at Publisher · View at Google Scholar · View at Scopus
  63. M. Shirai, H. Hirakawa, K. Ouchi et al., “Comparison of outer membrane protein genes omp and pmp in the whole genome sequences of Chlamydia pneumoniae isolates from Japan and the United States,” Journal of Infectious Diseases, vol. 181, supplement 3, pp. S524–S527, 2000. View at Google Scholar · View at Scopus
  64. W. T. Doerrler and R. H. Raetz, “Loss of outer membrane proteins without inhibition of lipid export in an Eschericia coli YaeT mutant,” The Journal of Biological Chemistry, vol. 280, no. 30, pp. 27679–27687, 2005. View at Publisher · View at Google Scholar
  65. A. Kubo and R. S. Stephens, “Characterization and functional analysis of PorB, a Chlamydia porin and neutralizing target,” Molecular Microbiology, vol. 38, no. 4, pp. 772–780, 2000. View at Publisher · View at Google Scholar · View at Scopus
  66. G. M. Wiseman, “The hemolysins of Staphylococcus aureus,” Bacteriological Reviews, vol. 39, no. 4, pp. 317–344, 1975. View at Google Scholar · View at Scopus