Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-22T17:09:53.620Z Has data issue: false hasContentIssue false

A role for antimicrobial peptides in intestinal microsporidiosis

Published online by Cambridge University Press:  12 December 2008

G. J. LEITCH*
Affiliation:
The Whitney Laboratory for Marine Bioscience, University of Florida, St Augustine, Florida, USA
C. CEBALLOS
Affiliation:
The Whitney Laboratory for Marine Bioscience, University of Florida, St Augustine, Florida, USA
*
*Corresponding author: The Whitney Laboratory for Marine Bioscience, University of Florida, 9505 Ocean Shore Blvd., St Augustine, FL 32080, USA. Tel: +904 461 4000. Fax: +904 461 4052. E-mail: [email protected]

Summary

Clinical isolates from 3 microsporidia species, Encephalitozoon intestinalis and Encephalitozoon hellem, and the insect parasite Anncaliia (Brachiola, Nosema) algerae, were used in spore germination and enterocyte-like (C2Bbe1) cell infection assays to determine the effect of a panel of antimicrobial peptides. Spores were incubated with lactoferrin (Lf), lysozyme (Lz), and human beta defensin 2 (HBD2), human alpha defensin 5 (HD5), and human alpha defensin 1 (HNP1), alone and in combination with Lz, prior to germination. Of the Encephalitozoon species only E. hellem spore germination was inhibited by HNP1, while A. algerae spore germination was inhibited by Lf, HBD2, HD5 and HNP1, although HBD2 and HD5 inhibition required the presence of Lz. The effects of HBD2 and HD5 on microsporidia enterocyte infection paralleled their effects on spore germination. Lysozyme alone only inhibited infection with A. algerae, while Lf inhibited infection by E. intestinalis and A. algerae. HNP1 significantly reduced enterocyte infection by all 3 parasite species and a combination of Lf, Lz and HNP1 caused a further reduced infection with A. algerae. These data suggest that intestinal antimicrobial peptides contribute to the defence of the intestine against infection by luminal microsporidia spores and may partially determine which parasite species infects the intestine.

Type
Research Article
Copyright
Copyright © 2008 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abrink, M., Larsson, E., Gobl, A. and Hellman, L. (2000). Expression of lactoferrin in the kidney: Implications for innate immunity and iron metabolism. Kidney International 57, 20042010.Google Scholar
Ayabe, T., Satchell, D. P., Wilson, C. L., Parks, W. C., Selsted, M. E. and Ouellette, A. J. (2000). Secretion of microbicidal α-defensins by intestinal Paneth cells in response to bacteria. Nature Immunology 1, 113118.CrossRefGoogle ScholarPubMed
Bard, E., Laibe, S., Bettinger, D., Riethmuller, D., Buchle, S., Seilles, E. and Meillet, D. (2003). New sensitive method for the measurement of lysozyme and lactoferrin for assessment of innate mucosal immunity. Part II: time-resolved immunofluorometric assay in serum and mucosal secretions. Clinical Chemistry and Laboratory Medicine 41, 127133.Google Scholar
Brogden, K. A. (2005). Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nature Reviews Microbiology 3, 238250.CrossRefGoogle ScholarPubMed
Buccigrossi, V., de Marco, G., Bruzzese, E., Ombrato, L., Bracale, I, Polito, G. and Guarino, A. (2007). Lactoferrin induces concentration-dependent functional modulation of intestinal proliferation and differentiation. Pediatric Research 61, 410414.CrossRefGoogle ScholarPubMed
Cali, A., Weiss, L. M. and Takvorian, P. M. (2002). Brachiola algerae spore membrane systems, their activity during extrusion, and a new structural entity, the multilayered interlaced network, associated with the polar tube and the sporoplasm. Journal of Eukaryotic Microbiology 49, 164174.Google Scholar
Chen, X., Niyonsaba, F., Ushio, H., Okuda, D., Nagaoka, I., Ikeda, S., Okumura, K. and Ogawa, H. (2005). Synergistic effect of antibacterial agents human beta-defensins, cathelicidin LL-37 and lysozyme against Staphylococcus aureus and Escherichia coli. Journal of Dermatological Science 40, 123132.CrossRefGoogle ScholarPubMed
Couzinet, S., Cejas, E., Schittny, J., Deplazes, P., Weber, R. and Zimmerli, S. (2000). Phagocytic uptake of Encephalitozoon cuniculi by nonprofessional phagocytes. Infection and Immunity 68, 69396945.CrossRefGoogle ScholarPubMed
Coyle, C. M., Weiss, L. M., Rhodes, V., Cali, A., Takvorian, P. M., Brown, F., Visvesvara, G. S., Xiao, L., Naktin, J., Young, E., Gareca, M., Colasante, G. and Wittner, M. (2004). Fatal myositis due to the microsporidian Brachiola algerae, a mosquito pathogen. New England Journal of Medicine 351, 4247.CrossRefGoogle Scholar
Cunliffe, R. N. (2003). Alpha-defensins in the gastrointestinal tract. Molecular Immunology 40, 463467.CrossRefGoogle ScholarPubMed
Dann, S. M. and Eckmann, L. (2007). Innate immune defenses in the intestinal tract. Current Opinions in Gastroenterology 23, 115120.CrossRefGoogle ScholarPubMed
De Leeuw, E., Burks, S. R., Li, X., Kao, J. P. and Lu, W. (2007). Structure-dependent functional properties of human defensin 5. FEBS Letters 581, 515520.CrossRefGoogle ScholarPubMed
del Aguila, C., Moura, H., Fenoy, S., Navajas, R., Lopez-Velez, R., Li, L., Xiao, L., Leitch, G. J., da Silva, A., Pieniazek, N. J., Lal, A. A. and Visvesvara, G. S. (2001). In vitro culture, ultrastructure, antigenic and molecular characterization of Encephalitozoon cuniculi isolated from urine and sputum samples from a Spanish patient with AIDS. Journal of Clinical Microbiology 39, 11051108.CrossRefGoogle ScholarPubMed
Didier, E. S. and Weiss, L. M. (2006). Microsporidiosis: current status. Current Opinions in Infectious Diseases 19, 485492.CrossRefGoogle ScholarPubMed
Didier, E. S., Orenstein, J. M., Aldras, A., Bertucci, D., Rogers, L. B. and Janney, F. A. (1995). Comparison of three staining methods for detecting microsporidia in fluids. Journal of Clinical Microbiology 33, 31383145.CrossRefGoogle ScholarPubMed
El Yazidi-Belkoura, I., Legrand, D., Nuijens, J., Slomiany, M.-C., van Berkel, P. and Spik, G. (2001). The binding of lactoferrin to glycosaminoglycans on enterocyte-like HT 29-18-C1 cells is mediated through basic residues located on the N terminus. Biochimica et Biophysica Acta 1568, 197204.CrossRefGoogle Scholar
Franzen, C. (2004). Microsporidia: how can they invade other cells? Trends in Parasitology 20, 275279.CrossRefGoogle ScholarPubMed
Franzen, C., Hosl, M., Salzberger, B. and Hartmann, P. (2005). Uptake of Encephalitozoon spp. and Vittaforma corneae (microsporidia) by different cells. Journal of Parasitology 91, 745749.CrossRefGoogle ScholarPubMed
Frixione, E., Ruiz, L., Cerbon, J. and Undeen, A. H. (1997). Germination of Nosema algerae (Microspora) spores: conditional inhibition by D2O, ethanol and Hg2+ suggests dependence of water influx upon membrane hydration and specific transmembrane pathways. Journal of Eukaryotic Microbiology 44, 109116.CrossRefGoogle Scholar
Ganz, T., Selsted, M. E., Szklarek, D., Harwig, S. S., Daher, K., Bainton, D. F. and Lehrer, R. L. (1985). Defensins. Natural peptide antibiotics of human neutrophils. Journal of Clinical Investigation 76, 14271435.CrossRefGoogle ScholarPubMed
Gifford, J. L., Hunter, H. N. and Vogel, H. J. (2005). Lactoferricin: a lactoferrin-derived peptide with antimicrobial, antiviral, antitumor and immunological properties. Cellular and Molecular Life Sciences 62, 25882598.CrossRefGoogle ScholarPubMed
Hancock, R. E. W. and Scott, M. G. (2000). The role of antimicrobial peptides in animal defenses. Proceedings of the National Academy of Sciences, USA 97, 88568861.CrossRefGoogle ScholarPubMed
Hayman, J. R., Southern, R. and Nash, T. E. (2005). Role of sulfated glycans in adherence of the microsporidian Encephalitozoon intestinalis to host cells in vitro. Infection and Immunity 73, 841848.Google Scholar
Jentsch, H., Sievert, Y. and Gocke, R. (2004). Lactoferrin and other markers from gingival crevicular fluid and saliva before and after periodontal treatment. Journal of Clinical Periodontology 31, 511514.CrossRefGoogle ScholarPubMed
Joly, S., Maze, C., McCray, P. B. Jr. and Guthmiller, J. M. (2004). Human β-defensins 2 and 3 demonstrate strain-selective activity against oral microorganisms. Journal of Clinical Microbiology 42, 10241029.Google Scholar
Jones, B. A. and Gore, G. J. (1997). Physiology and pathophysiology of apoptosis in epithelial cells of the liver, pancreas and intestine. American Journal of Physiology 273, G1174G1188.Google Scholar
Keohane, E. M. and Weiss, L. M. (1999). The structure, function, and composition of the microsporidian polar tube. In The Microsporidia and Microsporidiosis (ed. Whittner, M. and Weiss, L. M.), pp. 196224. American Society for Microbiology Press, Washington, D.C., USA.Google Scholar
Kotler, D. P. and Orenstein, J. M. (1998). Clinical syndromes associated with microsporidiosis. Advances in Parasitology 40, 321341.CrossRefGoogle ScholarPubMed
Kucerova, Z., Moura, H., Visvesvara, G. S. and Leitch, G. J. (2004). Differences between Brachiola (Nosema) algerae isolates of human and insect origin when tested using an in vitro spore germination assay and a cultured cell infection assay. Journal of Eukaryotic Microbiology 51, 339343.CrossRefGoogle Scholar
Leitch, G. J., Visvesvara, G. S. and He, Q. (1993). Inhibition of microsporidian spore germination. Parasitology Today 9, 422424.CrossRefGoogle ScholarPubMed
Leitch, G. J., Ward, T. L., Shaw, A. P. and Newman, G. (2005). Apical spore phagocytosis is not a significant route of infection of differentiated enterocytes by Encephalitozoon intestinalis. Infection and Immunity 73, 76977704.CrossRefGoogle Scholar
Leitch, G. J. and Ceballos, C. (2008). Effects of host temperature, and gastric and duodenal environments on microsporidia spore germination and infectivity of intestinal epithelial cells. Parasitology Research 104, 3542. 10.1007/s00436-008-1156-4.Google Scholar
Levay, P. F. and Viljoen, M. (1995). Lactoferrin: A general review. Haematologica 80, 252267.Google ScholarPubMed
Lievin-Le Moal, V. and Servin, A. L. (2006). The front line of enteric host defense against unwelcome intrusion of harmful microorganisms: mucins, antimicrobial peptides, and microbiota. Clinical Microbiology Reviews 19, 315337.CrossRefGoogle ScholarPubMed
Mathis, A., Weber, R. and Deplazes, P. (2005). Zoonotic potential of the microsporidia. Clinical Microbiology Reviews 18, 423445.Google Scholar
Montagne, P., Cuilliere, M. L., Mole, C., Rene, M. C. and Faure, G. (1998). Microparticle-enhanced nephelometric immunoassay of milk and other human body fluids. Clinical Chemistry 44, 16101615.Google Scholar
Muller, A., Bialek, R., Kamper, A., Fatkenheuer, G., Salzberger, B. and Franzen, C. (2001). Detection of microsporidia in travelers with diarrhea. Journal of Clinical Microbiology 39, 6301632.Google Scholar
Nagaoka, I., Hirota, S., Yamogida, S., Ohwada, A., and Hirata, M. (2000). Synergistic actions of antibacterial neutrophil defensins and cathelicidins. Inflammation Research 49, 7379.CrossRefGoogle ScholarPubMed
Newman, S. L., Gootee, L., Gabay, J. E. and Selsted, M. E. (2000). Identification of constituents of human neutrophil azurophil granules that mediate fungistasis against Histoplasma capsulatum. Infection and Immunity 68, 56685672.Google Scholar
Ouellette, A. J. (2006). Paneth cell alpha-defensin synthesis and function. Current Topics in Microbiology and Immunology 306, 125.Google Scholar
Peeters, T. and Vantrappen, G. (1975). The Paneth cell: a source of intestinal lysozyme. Gut 16, 553558.CrossRefGoogle ScholarPubMed
Pryzwansky, K. B., Rausch, P. G., Spitznagel, J. K. and Herion, J. C. (1979). Immunocytochemical distinction between primary and secondary granule formation in developing human neutrophils: correlations with Romanowsky stains. Blood 53, 179185.CrossRefGoogle ScholarPubMed
Rudney, J. D. and Smith, Q. T. (1985). Relationship between levels of lysozyme, lactoferrin, salivary peroxidase and secretory immunoglobulin A in stimulated parotid saliva. Infection and Immunity 49, 469475.CrossRefGoogle ScholarPubMed
Samaranayke, Y. H., Samaranayake, L. P., Pow, E. H. N., Beena, V. T. and Yeung, K. W. S. (2001). Antifungal effects of lysozyme and lactoferrin against genetically similar, sequential Candida albicans isolates from a human immunodeficiency virus-infected southern Chinese cohort. Journal of Clinical Microbiology 39, 32963302.CrossRefGoogle Scholar
Singh, P. K., Tack, B. F., McCray, P. B. Jr. and Welsh, M. J. (2000). Synergistic and additive killing by antimicrobial factors found in human airway surface liquid. American Journal of Physiology 279, L799L805.Google Scholar
Vavra, J. and Larsson, J. I. R. (1999). Structure of the microsporidia. In The Microsporidia and Microsporidiosis (ed. Whittner, M. and Weiss, L. M.), pp. 784. American Society for Microbiology Press, Washington, D.C., USA.Google Scholar
Visvesvara, G. S., Moura, H., Leitch, G. J. and Schwartz, D. A. (1999). Culture and propagation of microsporidia. In The Microsporidia and Microsporidiosis (ed. Whittner, M. and Weiss, L. M.), pp. 363392. American Society for Microbiology Press, Washington, D.C., USA.Google Scholar
Visvesvara, G. S., Moura, H., Leitch, G. J., Schwartz, D. A. and Xiao, L. X. (2005). Public health importance of Brachiola algerae (Microsporidia) – an emerging pathogen of humans. Folia Parasitologica (Praha) 52, 8394.CrossRefGoogle ScholarPubMed
Vylkova, S., Nayyar, N., Li, W. and Edgerton, M. (2007). Human beta defensins kill Candida albicans in an energy-dependent and salt–sensitive manner without causing membrane disruption. Antimicrobial Agents and Chemotherapy 51, 154161.Google Scholar