Molecular fractionation and characterization of a Candida albicans fraction that increases tumor cell adhesion to hepatic endothelium

Applied Microbiology and Biotechnology

Volumn 92, Issue 1, 2011, Pages 133-145

  Ramirez Garcia, Andoni ^a   Gallot, Natalia ^b   Abad, Ana ^a   Mendoza, Lorea ^b   Rementeria, Aitor ^a   Hernando, Fernando Luis ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b Pharmakine SL   (Spain)

Author keywords

Cancer; Candida albicans; Endothelium; Mannoproteins; Melanoma

Indexed keywords

CANCER; CANDIDA ALBICANS; ENDOTHELIUM; MANNOPROTEINS; MELANOMA;

ADHESION; AFFINITY CHROMATOGRAPHY; CELL ADHESION; DERMATOLOGY; ELECTROPHORESIS; ENDOTHELIAL CELLS; ONCOLOGY; TUMORS; YEAST;

CANDIDA;

ACTIN; ALCOHOL DEHYDROGENASE; AMINOPEPTIDASE; AMINOPEPTIDASE Y; ELONGATION FACTOR TU; ENOLASE; FRUCTOSE BISPHOSPHATE ALDOLASE; GLUTATHIONE DERIVATIVE; ISOCITRATE DEHYDROGENASE; KETOL ACID REDUCTOISOMERASE; PHOSPHOGLUCONATE DEHYDROGENASE; PHOSPHOGLYCERATE KINASE; PROTEIN DISULFIDE ISOMERASE; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG;

CANCER; CHROMATOGRAPHY; ELECTROKINESIS; FRACTIONATION; FUNGUS; HEMATOLOGY; IMMUNE RESPONSE; MOLECULAR ANALYSIS; PEPTIDE; PROTEIN; TUMOR;

AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGENICITY; ARTICLE; CANDIDA ALBICANS; CELL ADHESION; CONTROLLED STUDY; ELECTROPHORESIS; ENDOTHELIUM CELL; IMMUNOGENICITY; IN VITRO STUDY; ISOELECTRIC POINT; LIVER CELL; MALE; MELANOMA CELL; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PROTEIN ANALYSIS;

CANDIDA ALBICANS; CELL ADHESION; CELL LINE, TUMOR; CHEMICAL FRACTIONATION; CHROMATOGRAPHY, AFFINITY; ELECTROPHORESIS; ENDOTHELIUM; FUNGAL PROTEINS; HUMANS; ISOELECTRIC FOCUSING; ISOELECTRIC POINT; LIVER; MOLECULAR WEIGHT;

CANDIDA ALBICANS;

EID: 82455164174     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-011-3540-8     Document Type: Article

References (57)

1. Anttila VJ, Ruutu P, Bondestam S, Jansson SE, Nordling S, Färkkilä M, Sivonen A, Castren M, Ruutu T (1994) Hepatosplenic yeast infection in patients with acute-leukemia-A diagnostic problem. Clin Infect Dis 18:979-981 (Pubitemid 24171347)
2. Asumendi A, Alvarez A, Martinez I, Smedsrod B, VidalVanaclocha F (1996) Hepatic sinusoidal endothelium heterogeneity with respect to mannose receptor activity is interleukin-1 dependent. Hepatology 23:1521-1529 (Pubitemid 26181236)
3. Bohme A, Ruhnke M, Buchheidt D, Cornely OA, Einsele H, Enzensberger R, Hebart H, Heinz W, Junghanss C, Karthaus M, Krüger W, Krug U, Kubin T, Penack O, Reichert D, Reuter S, Silling G, Südhoff T, Ullmann AJ, Maschmeyer G (2009) Treatment of invasive fungal infections in cancer patients-recommendations of the Infectious Diseases Working Party (AGIHO) of the German Society of Hematology and Oncology (DGHO). Ann Hematol 88:97-110
4. Buckley HR, Richardson MD, Evans EGV, Wheat LJ (1992) Immunodiagnosis of invasive fungal infection. J Med Vet Mycol 30:249-260 (Pubitemid 23055906)
5. Caldas TD, El Yaagoubi A, Richarme G (1998) Chaperone properties of bacterial elongation factor EF-Tu. J Biol Chem 273:11478-11482 (Pubitemid 28272041)
6. Canback B, Andersson SGE, Kurland CG (2002) The global phylogeny of glycolytic enzymes. Proc Natl Acad Sci U S A 99:6097-6102 (Pubitemid 34493271)
7. Chaffin WL, Lopez-Ribot JL, Casanova M, Gozalbo D, Martinez JP (1998) Cell wall and secreted proteins of Candida albicans: Identification, function, and expression. Microbiol Mol Biol Rev 62:130-180 (Pubitemid 28130799)
8. Chung CW, Nickerson WJ (1954) Polysaccharide syntheses in growing yeasts. J Biol Chem 208:395-407
9. Coler RN, Skeiky YAW, Bernards K, Greeson K, Carter D, Cornellison CD, Modabber F, Campos-Neto A, Reed SG (2002) Immunization with a polyprotein vaccine consisting of the T-cell antigens thiol-specific antioxidant, Leishmania major stress-inducible protein 1, and Leishmania elongation initiation factor protects against leishmaniasis. Infect Immun 70:4215-4225 (Pubitemid 34790930)
10. Coussens LM, Werb Z (2002) Inflammation and cancer. Nature 420:860-867 (Pubitemid 36019639)
11. Crowe JD, Sievwright IK, Auld GC, Moore NR, Gow NA, Booth NA (2003) Candida albicans binds human plasminogen: Identification of eight plasminogen-binding proteins. Mol Microbiol 47:1637-1651 (Pubitemid 36363345)
12. de Pauw B (2004) Preventative use of antifungal drugs in patients treated for cancer. J Antimicrob Chemother 53:130-132
13. Derepentigny L, Kaufman L, Cole GT, Kruse D, Latgé JP, Matthews RC (1994) Immunodiagnosis of invasive fungal-infections. J Med Vet Mycol 32:239-252
14. Fernandez-Arenas E, Molero G, Nombela C, Diez-Orejas R, Gil C (2004) Contribution of the antibodies response induced by a low virulent Candida albicans strain in protection against systemic candidiasis. Proteomics 4:1204-1215 (Pubitemid 38445977)
15. Gobom J, Nordhoff E, Mirgorodskaya E, Ekman R, Roepstorff P (1999) Sample purification and preparation technique based on nano-scale reversed-phase columns for the sensitive analysis of complex peptide mixtures by matrix-Assisted laser desorption/ionization mass spectrometry. J Mass Spectrom 34:105-116
16. Gozalbo D, Gil-Navarro I, Azorin I, Renau-Piqueras J, Martínez JP, Gil ML (1998) The cell wall-Associated glyceraldehyde-3-phosphate dehydrogenase of Candida albicans is also a fibronectin and laminin binding protein. Infect Immun 66:2052-2059 (Pubitemid 28194101)
17. Haas G, Karaali G, Ebermayer K, Metzger WG, Lamer S, Zimny-Arndt U, Diescher S, Goebel UB, Vogt K, Roznowski AB, Wiedenmann BJ, Meyer TF, Aebischer T, Jungblut PR (2002) Immunoproteomics of Helicobacter pylori infection and relation to gastric disease. Proteomics 2:313-324 (Pubitemid 34269985)
18. Hernando FL, Calvo E, Abad A, Ramírez A, Rementería A, Sevilla MJ, Pontón J (2007) Identification of protein and mannoprotein antigens of Candida albicans of relevance for the serodiagnosis of invasive candidiasis. Int Microbiol 10:103-108 (Pubitemid 47173981)
19. Iborra S, Soto M, Carrion J, Nieto A, Fernández E, Alonso C, Requena JM (2003) The Leishmania infantum acidic ribosomal protein P0 administered as a DNA vaccine confers protective immunity to Leishmania major infection in BALB/c mice. Infect Immun 71:6562-6572 (Pubitemid 37337716)
20. Jong AY, Chen SHM, Stins MF, Kim KS, Tuan TL, Huang SH (2003) Binding of Candida albicans enolase to plasmin(ogen) results in enhanced invasion of human brain microvascular endothelial cells. J Med Microbiol 52:615-622 (Pubitemid 36981467)
21. Klotz SA, Pendrak ML, Hein RC (2001) Antibodies to alpha(5)beta (1), and alpha(v)beta(3) integrins react with Candida albicans alcohol dehydrogenase. Microbiology 147:3159-3164 (Pubitemid 33077005)
22. Lain A, Moragues MD, Ruiz JC, Mendoza J, Camacho A, Del Palacio A, Pontón J (2007) Evaluation of a novel enzyme-linked immunosorbent assay to detect immunoglobulin G antibody to enolase for serodiagnosis of invasive candidiasis. Clin Vaccine Immunol 14:318-319 (Pubitemid 46570291)
23. Lamaris GA, Esmaeli B, Chamilos G, Desai A, Chemaly RF, Raad II, Safdar A, Lewis RE, Kontoyiannis DP (2008) Fungal endophthalmitis in a tertiary care cancer center: A review of 23 cases. Eur J Clin Microbiol Infect Dis 27:343-347
24. Lim DB, Hains P, Walsh B, Bergquist P, Nevalainen H (2001) Proteins associated with the cell envelope of Trichoderma reesei: A proteomic approach. Proteomics 1:899-909
25. Marques MAM, Chitale S, Brennan PJ, Pessolani MCV (1998) Mapping and identification of the major cell wall-Associated components of Mycobacterium leprae. Infect Immun 66:2625-2631 (Pubitemid 28261762)
26. Martinez JP, Gil ML, Lopez-Ribot JL (1998) Serologic response to cell wall mannoproteins and proteins of Candida albicans. Clin Microbiol Rev 11:121-141 (Pubitemid 28046018)
27. Martínez-López R, Nombela C, Diez-Orejas R, Monteoliva L, Gil C (2008) Immunoproteomic analysis of the protective response obtained from vaccination with Candida albicans ecm33 cell wall mutant in mice. Proteomics 8:2651-2664 (Pubitemid 351988570)
28. Masuoka J, Glee PM, Hazen KC (1998) Preparative isoelectric focusing and preparative electrophoresis of hydrophobic Candida albicans cell wall proteins with in-line transfer to polyvinylidene difluoride membranes for sequencing. Electrophoresis 19:675-678 (Pubitemid 28236665)
29. Matsuda K, Sakaguchi K, Kobayashi S, Tominaga M, Hirayama K, Kadosawa T, Taniyama H (2009) Systemic candidiasis and Mesenteric mast cell tumor with multiple metastases in a dog. J Vet Med Sci 71:229-232
30. Mendoza L, Olaso E, Anasagasti MJ, Fuentes AM, Vidal-Vanaclocha F (1998) Mannose receptor-mediated endothelial cell activation contributes to B16 melanoma cell adhesion and metastasis in liver. J Cell Physiol 174:322-330 (Pubitemid 28068709)
31. Nishizawa M, Yasuhara T, Nakai T, Fujiki Y, Ohashi A (1994) Molecular-cloning of the aminopeptidase Y gene of Saccharomyces cerevisiae-sequence-Analysis and gene disruption of a new aminopeptidase. J Biol Chem 269:13651-13655
32. Oliveira SC, Splitter GA (1996) Immunization of mice with recombinant L7/L12 ribosomal protein confers protection against Brucella abortus infection. Vaccine 14:959-962 (Pubitemid 26271067)
33. Pagano L, Larocca LM, Marra R, Pizzigallo E, Leone G (1992) A leukemic patient with hepatosplenic abscesses due to coagulasenegative staphylococci. Clin Infect Dis 14:364-365
34. Pardo M, Ward M, Pitarch A, Sánchez M, Nombela C, Blackstock W, Gil C (2000) Cross-species identification of novel Candida albicans immunogenic proteins by combination of two-dimensional polyacrylamide gel electrophoresis and mass spectrometry. Electrophoresis 21:2651-2659 (Pubitemid 30646300)
35. Parvez T (2003) Fungal infections in neutropenic cancer patients. J Coll Physicians Surg Pak 13:669-673 (Pubitemid 38029008)
36. Pemán J, Cantón E, Orero A, Viudes A, Frasquet J, Gobernado M (2002) Epidemiology of candidemia in Spain-multicenter study. Rev Iberoam Micol 19:30-35
37. Pitarch A, Diez-Orejas R, Molero G, Pardo M, Sánchez M, Gil C, Nombela C (2001) Analysis of the serologic response to systemic Candida albicans infection in a murine model. Proteomics 1:550-559 (Pubitemid 33588308)
38. Pitarch A, Sanchez M, Nombela C, Gil C (2002) Sequential fractionation and two-dimensional gel analysis unravels the complexity of the dimorphic fungus Candida albicans cell wall proteome. Mol Cell Proteomics 1:967-982
39. Pitarch A, Abian J, Carrascal M, Sánchez M, Nombela C, Gil C (2004) Proteomics-based identification of novel Candida albicans antigens for diagnosis of systemic candidiasis in patients with underlying hematological malignancies. Proteomics 4:3084-3106 (Pubitemid 39372391)
40. Rafailidis PI, Kapaskelis A, Christodoulou C, Galani E, Falagas ME (2008) Concurrent M-Tuberculosis, Klebsiella pneumoniae, and Candida albicans infection in liver metastasis of bowel carcinoma. Eur J Clin Microbiol Infect Dis 27:753-755
41. Ribeiro LA, Azevedo V, Le Loir Y, Oliveira SC, Dieye Y, Piard JC, Gruss A, Langella P (2002) Production and targeting of the Brucella abortus antigen L7/L12 in Lactococcus lactis: A first step towards food-grade live vaccines against brucellosis. Appl Environ Microbiol 68:910-916 (Pubitemid 34113084)
42. Rodrigo L, Gil F, Hernandez AF, Lopez O, Pla A (2003) Identification of paraoxonase 3 in rat liver microsomes: Purification and biochemical properties. Biochem J 376:261-268 (Pubitemid 37487222)
43. Rodriguez-Cuesta J, Vidal-Vanaclocha F, Mendoza L, Valcárcel M, Gallot N, Martínez de Tejada G (2005) Effect of asymptomatic natural infections due to common mouse pathogens on the metastatic progression of B16 murine melanoma in C57BL/6 mice. Clin Exp Metastasis 22:549-558 (Pubitemid 43234639)
44. Rodriguez-Cuesta J, Hernando FL, Mendoza L, Gallot N, de Cerio AA, Martínez-de-Tejada G, Vidal-Vanaclocha F (2010) Candida albicans enhances experimental hepatic melanoma metastasis. Clin Exp Metastasis 27:35-42
45. Ruhnke M, Maschmeyer G (2002) Management of mycoses in patients with hematologic disease and cancer-review of the literature. Eur J Med Res 7:227-235
46. Sanchez-Campillo M, Bini L, Comanducci R, Raggiaschi R, Marzocchi B, Pallini V, Ratti G (1999) Identification of immunoreactive proteins of Chlamydia trachomatis by Western blot analysis of a two-dimensional electrophoresis map with patient sera. Electrophoresis 20:2269-2279 (Pubitemid 29413316)
47. Saxena A, Calderone R (1990) Purification and characterization of the extracellular C3d-binding protein of Candida albicans. Infect Immun 58:309-314 (Pubitemid 20058801)
48. Schlesinger A, Paul M, Gafter-Gvili A, Rubinovitch B, Leibovici L (2009) Infection-control interventions for cancer patients after chemotherapy: A systematic review and meta-Analysis. Lancet Infect Dis 9:97-107
49. Shen HD, Choo KB, Tang RB, Lee CF, Yeh JY, Han SH (1989) Allergenic components of Candida albicans identified by immunoblot analysis. Clin Exp Allergy 19:191-195
50. Sundstrom P, Jensen J, Balish E (1994) Humoral and cellular immuneresponses to enolase after alimentary-Tract colonization or intravenous immunization with Candida albicans. J Infect Dis 170:390-395 (Pubitemid 24226369)
51. Swoboda RK, Bertram G, Hollander H, Greenspan D, Greenspan JS, Gow NA, Gooday GW, Brown AJ (1993) Glycolytic-enzymes of Candida albicans are nonubiquitous immunogens during candidiasis. Infect Immun 61:4263-4271 (Pubitemid 23298583)
52. Urban C, Sohn K, Lottspeich F, Brunner H, Rupp S (2003) Identification of cell surface determinants in Candida albicans reveals Tsa1p, a protein differentially localized in the cell. FEBS Lett 544:228-235 (Pubitemid 36628068)
53. van Deventer H, Goessens W, van Vliet A, Verbrugh H (1996) Anti-enolase antibodies partially protective against systemic candidiasis in mice. Clin Microbiol Infect 2:36-43 (Pubitemid 126682076)
54. Vidal-Vanaclocha F, Rocha M, Asumendi A, Barbera-Guillem E (1993) Isolation and enrichment of two sublobular compartmentspecific endothelial cell subpopulations from liver sinusoids. Hepatology 18:328-339 (Pubitemid 23225104)
55. Vidal-Vanaclocha F, Fantuzzi G, Mendoza L, Fuentes AM, Anasagasti MJ, Martín J, Carrascal T, Walsh P, Reznikov LL, Kim SH, Novick D, Rubinstein M, Dinarello CA (2000) IL-18 regulates IL-1 beta-dependent hepatic melanoma metastasis via vascular cell adhesion molecule-1. Proc Natl Acad Sci U S A 97:734-739 (Pubitemid 30070378)
56. Walsh TJ, Hathorn JW, Sobel JD, Merz WG, Sanchez V, Maret SM, Buckley HR, Pfaller MA, Schaufele R, Sliva C, Navarro E, Lecciones J, Chandrasekar P, Lee J, Pizzo PA (1991) Detection of circulating candida enolase by immunoassay in patients with cancer and invasive candidiasis. N Engl J Med 324:1026-1031
57. Xin H, Dziadek S, Bundle DR, Cutler JE (2008) Synthetic glycopeptide vaccines combining beta-mannan and peptide epitopes induce protection against candidiasis. Proc Natl Acad Sci U S A 105:13526-13531