Chapter 11 : A Host View of the Fungal Cell Wall

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The fungal cell wall surface, which represents the interface between the host and the infective microbe, emerges as the complex structure that harbors many of the relevant components that interact with the host tissues and defenses. Knowledge of cell wall biogenesis and the functions that control dynamics of this interface may provide significant clues for the development of novel therapeutic strategies. This chapter summarizes some structural and functional aspects of the cell wall of the fungal pathogen Candida albicans. It also highlights recent findings that indicate its relevance in the interaction with the host immune cells, as this process is essential to prime and develop a protective immune response and contributes significantly to the control and pathology of the infection. The cell wall is an external structure that confers the typical morphology to almost all microbes. As the most external cellular structure, it mediates adhesion to the host tissues, being crucial to initiate colonization and, therefore, causes disease. Phagocytosis of C. albicans is carried out by different types of cells, mainly neutrophils and macrophages. This process occurs presumably by the action of complement and antibody receptors, following the routes of microbial ingestion after opsonization by either the complement, antibodies, or both. The identification of permanent dialog among the microbe and the host cells at the molecular level (signals, mechanisms, and responses) will have important consequences from which both basic and applied research may benefit in the near future.

Citation: Alonso-Monge R, Román E, Pla J, Nombela C. 2008. A Host View of the Fungal Cell Wall, p 105-112. In Baquero F, Nombela C, Cassell G, Gutiérrez-Fuentes J (ed), Evolutionary Biology of Bacterial and Fungal Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815639.ch11
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1. Akins, R. A. 2005. An update on antifungal targets and mechanisms of resistance in Candida albicans. Med. Mycol. 43: 285318.
2. Alonso-Monge, R.,, F. Navarro-García,, G. Molero,, R. Diez-Orejas,, M. Gustin,, J. Pla,, M. Sánchez, and, C. Nombela. 1999. Role of the mitogen-activated protein kinase Hog1p in morphogenesis and virulence of Candida albicans. J. Bacteriol. 181: 30583068.
3. Anderson, J. B. 2005. Evolution of antifungal-drug resistance: mechanisms and pathogen fitness. Nat. Rev. Microbiol. 3: 547556.
4. Bates, S.,, H. B. Hughes,, C. A. Munro,, W. P. Thomas,, D. M. MacCallum,, G. Bertram, et al. 2006. Outer chain N-glycans are required for cell wall integrity and virulence of Candida albicans. J. Biol. Chem. 281: 9098.
5. Bates, S.,, D. M. MacCallum,, G. Bertram,, C. A. Munro,, H. B. Hughes,, E. T. Buurman, et al. 2005. Candida albicans Pmr1p, a secretory pathway P-type Ca2+/Mn2+-ATPase, is required for glycosylation and virulence. J. Biol. Chem. 280: 2340823415.
6. Braun, B. R., and, A. D. Johnson. 1997. Control of filament formation in Candida albicans by the transcriptional repressor TUP1. Science 277: 105109.
7. Brown, G. D., and, S. Gordon. 2001. Immune recognition. A new receptor for beta-glucans. Nature 413: 3637.
8. Brown, G. D.,, J. Herre,, D. L. Williams,, J. A. Willment,, A. S. Marshall, and, S. Gordon. 2003. Dectin-1 mediates the biological effects of beta-glucans. J. Exp. Med. 197: 11191124.
9. Burnie, J., and, R. Matthews. 2003. The role of antibodies against hsp90 in the treatment of fungal infections. Drug News Perspect. 16: 205210.
10. Calderone, R. A., and, Fonzi, W. A. 2001. Virulence factors of Candida albicans. Trends Microbiol. 9: 327335.
11. Cambi, A.,, K. Gijzen,, J. M. de Vries,, R. Torensma,, B. Joosten,, G. J. Adema, et al. 2003. The C-type lectin DC-SIGN (CD209) is an antigen-uptake receptor for Candida albicans on dendritic cells. Eur. J. Immunol. 33: 532538.
12. Casadevall, A., and, L. Pirofski. 2001. Host-pathogen interactions: the attributes of virulence. J. Infect. Dis. 184: 337344.
13. Casadevall, A., and, L. A. Pirofski. 1999. Host-pathogen interactions: redefining the basic concepts of virulence and pathogenicity. Infect. Immun. 67: 37033713.
14. Chaffin, W. L.,, J. L. Lopez-Ribot,, M. Casanova,, D. Gozalbo, and, J. P. Martinez. 1998. Cell wall and secreted proteins of Candida albicans: identification, function, and expression. Microbiol. Mol. Biol. Rev. 62: 130180.
15. Cutler, J. E. 2001. N-glycosylation of yeast, with emphasis on Candida albicans. Med. Mycol. 39 (Suppl 1): 7586.
16. d’Ostiani, C. F.,, G. Del Sero,, A. Bacci,, C. Montagnoli,, A. Spreca,, A. Mencacci, et al. 2000. Dendritic cells discriminate between yeasts and hyphae of the fungus Candida albicans. Implications for initiation of T helper cell immunity in vitro and in vivo. J. Exp. Med. 191: 16611674.
17. Dromer, F.,, R. Chevalier,, B. Sendid,, L. Improvisi,, T. Jouault,, R. Robert, et al. 2002. Synthetic analogues of beta-1,2 oligomannosides prevent intestinal colonization by the pathogenic yeast Candida albicans. Antimicrob. Agents Chemother. 46: 38693876.
18. East, L., and, C. M. Isacke. 2002. The mannose receptor family. Biochim. Biophys. Acta. 1572 (2–3) : 364386.
19. Ernst, J. F., and, S. K. Prill. 2001. O-glycosylation. Med. Mycol. 39 (Suppl 1): 6774.
20. Ezekowitz, R. A.,, K. Sastry,, P. Bailly, and, A. Warner. 1990. Molecular characterization of the human macrophage mannose receptor: demonstration of multiple carbohydrate recognition-like domains and phagocytosis of yeasts in Cos-1 cells. J. Exp. Med. 172: 17851794.
21. Ezekowitz, R. A.,, D. J. Williams,, H. Koziel,, M. Y. Armstrong,, A. Warner,, F. F. Richards, et al. 1991. Uptake of Pneumocystis carinii mediated by the macrophage mannose receptor. Nature 351: 155158.
22. Fernandez-Arenas, E.,, G. Molero,, C. Nombela,, R. Diez-Orejas, and, C. Gil. 2004a. Contribution of the antibodies response induced by a low virulent Candida albicans strain in protection against systemic candidiasis. Proteomics 4: 12041215.
23. Fernandez-Arenas, E.,, G. Molero,, C. Nombela,, R. Diez-Orejas, and, C. Gil. 2004b. Low virulent strains of Candida albicans: unravelling the antigens for a future vaccine. Proteomics 4: 30073020.
24. Fradin, C.,, D. Poulain, and, T. Jouault. 2000. beta-1,2-linked oligomannosides from Candida albicans bind to a 32-kilodalton macrophage membrane protein homologous to the mammalian lectin galectin-3. Infect. Immun. 68: 43914398.
25. Gantner, B. N.,, R. M. Simmons,, S. J. Canavera,, S. Akira, and, D. M. Underhill. 2003. Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J. Exp. Med. 197: 11071117.
26. Gantner, B. N.,, R. M. Simmons, and, D. M. Underhill. 2005. Dectin-1 mediates macrophage recognition of Candida albicans yeast but not filaments. EMBO. J. 24: 12771286.
27. Geijtenbeek, T. B.,, D. J. Krooshoop,, D. A. Bleijs,, S. J. van Vliet,, G. C. van Duijnhoven,, V. Grabovsky, et al. 2000a. DC-SIGN-ICAM-2 interaction mediates dendritic cell trafficking. Nat. Immunol. 1: 353357.
28. Geijtenbeek, T. B.,, D. S. Kwon,, R. Torensma,, S. J. van Vliet,, G. C. van Duijnhoven,, J. Middel, et al. 2000b. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell. 100: 587597.
29. Geijtenbeek, T. B.,, R. Torensma,, S. J. van Vliet,, G. C. van Duijnhoven,, G. J. Adema,, Y. van Kooyk, et al. 2000c. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell. 100: 575585.
30. Gersuk, G. M.,, D. M. Underhill,, L. Zhu, and, K. A. Marr. 2006. Dectin-1 and TLRs permit macrophages to distinguish between different Aspergillus fumigatus cellular states. J. Immunol. 176: 37173724.
31. Hazen, K. C. 2004. New and emerging yeast pathogens. Clin. Microbiol. Rev. 8: 462478.
32. Herre, J.,, J. A. Willment,, S. Gordon, and, G. D. Brown. 2004. The role of Dectin-1 in antifungal immunity. Crit. Rev. Immunol. 24: 193203.
33. Hoyer L. L. 2001. The ALS gene family of Candida albicans. Trends Microbiol. 9: 176180.
34. Kapteyn, J. C.,, H. van den Ende, and, F. M. Klis. 1999. The contribution of cell wall proteins to the organization of the yeast cell wall. Biochim. Biophys. Acta. 1426: 373383.
35. Karbassi A,, J. M. Becker,, J. S. Foster, and, R. N. Moore. 1987. Enhanced killing of Candida albicans by murine macrophages treated with macrophage colony-stimulating factor: evidence for augmented expression of mannose receptors. J. Immunol. 139: 417421.
36. Kobayashi, G. S., and, J. E. Cutler. 1998. Candida albicans hyphal formation and virulence: is there a clearly defined role? Trends Microbiol. 6: 9294.
37. Kobayashi, H.,, H. Oyamada,, N. Iwadate,, H. Suzuki,, H. Mitobe,, K. Takahashi, et al. 1998. Structural and immunochemical characterization of beta-1,2-linked mannobiosyl phosphate residue in the cell wall mannan of Candida glabrata. Arch. Microbiol. 169: 188194.
38. Lagorce, A.,, N. C. Hauser,, D. Labourdette,, C. Rodriguez,, H. Martin-Yken,, J. Arroyo, et al. ( 2003). Genome-wide analysis of the response to cell wall mutations in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 278: 2034520357.
39. Latge, J. P. 1999. Aspergillus fumigatus and aspergillosis. Clin. Microbiol. Rev. 12: 310350.
40. Lee, S. J.,, N. Y. Zheng,, M. Clavijo, and, M. C. Nussenzweig. 2003. Normal host defense during systemic candidiasis in mannose receptor-deficient mice. Infect. Immun. 71: 437445.
41. Lemaitre, B.,, E. Nicolas,, L. Michaut,, J. M. Reichhart, and, J. A. Hoffmann. 1996. The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell. 86: 973983.
42. Lo, H. J.,, J. R. Kohler,, B. DiDomenico,, D. Loebenberg,, A. Cacciapuoti, and, G. R. Fink. 1997. Nonfilamentous C. albicans mutants are avirulent. Cell. 90: 939949.
43. Lopez-Villar, E.,, L. Monteoliva,, M. R. Larsen,, E. Sachon,, M. Shabaz,, M. Pardo, et al. 2005. Genetic and proteomic evidences support the localization of yeast enolase in the cell wall. Proteomics 6: S107S118.
44. Marodi, L.,, H. M. Korchak, and, R. B. Johnston, Jr. 1991. Mechanisms of host defense against Candida species. I. Phagocytosis by monocytes and monocyte-derived macrophages. J. Immunol. 146: 27832789.
45. Marodi, L.,, S. Schreiber,, D. C. Anderson,, R. P. MacDermott,, H. M. Korchak, and, R. B. Johnston, Jr. 1993. Enhancement of macrophage candidacidal activity by interferon-gamma. Increased phagocytosis, killing, and calcium signal mediated by a decreased number of mannose receptors. J. Clin. Invest. 91: 25962601.
46. Martinez-Pomares, L.,, S. A. Linehan,, P. R. Taylor, and, S. Gordon. 2001. Binding properties of the mannose receptor. Immunobiology 204: 527535.
47. Monge, R. A.,, E. Román,, C. Nombela, and, J. Pla. 2006. The MAP kinase signal transduction network in Candida albicans. Microbiology 152: 905912.
48. Munro, C. A.,, S. Bates,, E. T. Buurman,, H. B. Hughes,, D. M. MacCallum,, G. Bertram, et al. 2005. Mnt1p and Mnt2p of Candida albicans are partially redundant alpha-1,2-mannosyltransferases that participate in O-linked mannosylation and are required for adhesion and virulence. J. Biol. Chem. 280: 10511060.
49. Netea, M. G.,, N. A. Gow,, C. A. Munro,, S. Bates,, C. Collins,, G. Ferwerda, et al. 2006. Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J. Clin. Invest. 116: 16421650.
50. Netea, M. G.,, C. Van der Graaf,, J. W. Van der Meer, and, B. J. Kullberg. 2004. Recognition of fungal pathogens by Toll-like receptors. Eur. J. Clin. Microbiol. Infect. Dis. 23: 672676.
51. Netea, M. G.,, C. A. Van der Graaf,, A. G. Vonk,, I. Verschueren,, J. W. Van der Meer, and, B. J. Kullberg. 2002. The role of toll-like receptor (TLR) 2 and TLR4 in the host defense against disseminated candidiasis. J. Infect. Dis. 185: 14831489.
52. Nombela, C.,, C. Gil, and, W. L. Chaffin. 2006. Non-conventional protein secretion in yeast. Trends Microbiol. 14: 1521.
53. Odds, F. C.,, R. Calderone,, B. Hube, and, C. Nombela. 2003. Candida albicans: views and suggestions from a peer-group workshop. ASM News 69: 5455.
54. Odds, F. C. 1994. Candida species and virulence. ASM News 60: 313318.
55. Pardo, M.,, L. Monteoliva,, L. S. Bains,, M. Ward,, W. Blackstock,, J. Pla, et al. 1999a. Analysis and identification of proteins secreted by Saccharomyces cerevisiae regenerating protoplasts. Curr. Genet. 35: 1219.
56. Pardo, M.,, L. Monteoliva,, J. Pla,, M. Sanchez,, C. Gil, and, C. Nombela. 1999b. Two-dimensional analysis of proteins secreted by Saccharomyces cerevisiae regenerating protoplasts: a novel approach to study the cell wall. Yeast 15: 459472.
57. Perfect, J. R. 2004. Antifungal resistance: the clinical front. Oncology 18 (Suppl 13): 1522.
58. Pitarch, A.,, J. Abian,, M. Carrascal,, M. Sanchez,, C. Nombela, and, C. Gil. 2004. Proteomics-based identification of novel Candida albicans antigens for diagnosis of systemic candidiasis in patients with underlying hematological malignancies. Proteomics 4: 30843106.
59. Pitarch, A.,, A. Jimenez,, C. Nombela, and, C. Gil. 2006. Decoding serological response to Candida cell wall immunome into novel diagnostic, prognostic, and therapeutic candidates for systemic candidiasis by proteomic and bioinformatic analyses. Mol. Cell. Proteomics 5: 7996.
60. Pitarch, A.,, M. Sanchez,, C. Nombela, and, C. Gil. 2002. Sequential fractionation and two-dimensional gel analysis unravels the complexity of the dimorphic fungus Candida albicans cell wall proteome. Mol. Cell. Proteomics 1: 967982.
61. Prill, S. K.,, B. Klinkert,, C. Timpel,, C. A. Gale,, K. Schroppel, and, J. F. Ernst. 2000. PMT family of Candida albicans: five protein mannosyltransferase isoforms affect growth, morphogenesis and antifungal resistance. Mol. Microbiol. 55: 546560.
62. Ram, A. F.,, J. C. Kapteyn,, R. C. Montijn,, L. H. Caro,, J. E. Douwes,, W. Baginsky, et al. 1998. Loss of the plasma membrane-bound protein Gas1p in Saccharomyces cerevisiae results in the release of β-1,3-glucan into the medium and induces a compensation mechanism to ensure cell wall integrity. J. Bacteriol. 180: 14181424.
63. Romani, L. 2004. Immunity to fungal infections. Nat. Rev. Immunol. 4: 123.
64. Rooney, P. J., and, B. S. Klein. 2002. Linking fungal morphogenesis with virulence. Cell. Microbiol. 4: 127137.
65. Rouabhia, M.,, M. Schaller,, C. Corbucci,, A. Vecchiarelli,, S. K. Prill,, L. Giasson, et al. 2005. Virulence of the fungal pathogen Candida albicans requires the five isoforms of protein mannosyltransferases. Infect. Immun. 73: 45714580.
66. Ryley, J. F., and, N. G. Ryley. 1990. Candida albicans: do mycelia matter? J. Med. Vet. Mycol. 28: 225239.
67. Sano, H.,, D. K. Hsu,, J. R. Apgar,, L. Yu,, B. B. Sharma,, I. Kuwabara, et al. 2003. Critical role of galectin-3 in phagocytosis by macrophages. J. Clin. Invest. 112: 389397.
68. Saville, S. P.,, A. L. Lazzell,, C. Monteagudo, and, J. L. Lopez-Ribot. 2003. Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot Cell 2: 10531060.
69. Serrano-Gomez, D.,, A. Dominguez-Soto,, J. Ancochea,, J. A. Jimenez-Heffernan,, J. A. Leal, and, A. L. Corbi. 2004. Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin mediates binding and internalization of Aspergillus fumigatus conidia by dendritic cells and macrophages. J. Immunol. 173: 56355643.
70. Serrano-Gomez, D.,, J. A. Leal, and, A. L. Corbi. 2005. DC-SIGN mediates the binding of Aspergillus fumigatus and keratinophylic fungi by human dendritic cells. Immunobiology 210: 175183.
71. Sharkey, L. L.,, M. D. McNemar,, S. M. Saporito-Irwin,, P. S. Sypherd, and, W. A. Fonzi. 1999. HWP1 functions in the morphological development of Candida albicans downstream of EFG1, TUP1, and RBF1. J. Bacteriol. 181: 52735279.
72. Shibata, N.,, H. Kobayashi,, Y. Okawa, and, S. Suzuki. 2003. Existence of novel beta-1,2 linkage-containing side chain in the mannan of Candida lusitaniae, antigenically related to Candida albicans serotype A. Eur. J. Biochem. 270: 25652575.
73. Sohn, K.,, J. Schwenk,, C. Urban,, J. Lechner,, M. Schweikert, and, S. Rupp. 2006. Getting in touch with Candida albicans: the cell wall of a fungal pathogen. Curr. Drug Targets 7: 505512.
74. Staab, J. F.,, S. D. Bradway,, P. L. Fidel, and, P. Sundstrom. 1999. Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 283: 15351538.
75. Staab, J. F., and, P. Sundstrom. 1998. Genetic organization and sequence analysis of the hypha-specific cell wall protein gene HWP1 of Candida albicans. Yeast 14: 681686.
76. Stahl, P. D., and, R. A. Ezekowitz. 1998. The mannose receptor is a pattern recognition receptor involved in host defense. Curr. Opin. Immunol. 10: 5055.
77. Sternberg, S. 1994. The emerging fungal threat. Science 266: 16321634.
78. Sundstrom, P. 2002. Adhesion in Candida spp. Cell. Microbiol. 4: 461469.
79. Suzuki, A.,, Y. Takata,, A. Oshie,, A. Tezuka,, N. Shibata,, H. Kobayashi, et al. 1995. Detection of beta-1,2-mannosyltransferase in Candida albicans cells. FEBS Lett. 373: 275279.
80. Swain, S. D.,, S. J. Lee,, M. C. Nussenzweig, and, A. G. Harmsen. 2003. Absence of the macrophage mannose receptor in mice does not increase susceptibility to Pneumocystis carinii infection in vivo. Infect. Immun. 71: 62136221.
81. Tada, H.,, E. Nemoto,, H. Shimauchi,, T. Watanabe,, T. Mikami,, T. Matsumoto, et al. 2002. Saccharomyces cerevisiae - and Candida albicans-derived mannan induced production of tumor necrosis factor alpha by human monocytes in a CD14- and Toll-like receptor 4-dependent manner. Microbiol. Immunol. 46: 503512.
82. Taylor, M. E.,, K. Bezouska, and, K. Drickamer. 1992. Contribution to ligand binding by multiple carbohydrate-recognition domains in the macrophage mannose receptor. J. Biol. Chem. 267: 17191726.
83. Taylor, P. R.,, G. D. Brown,, D. M. Reid,, J. A. Willment,, L. Martinez-Pomares,, S. Gordon, et al. 2002. The beta-glucan receptor, dectin-1, is predominantly expressed on the surface of cells of the monocyte/macrophage and neutrophil lineages. J. Immunol. 169: 38763882.
84. Trinel, P. A.,, T. Jouault,, J. E. Cutler, and, D. Poulain. 2002. Beta-1,2-mannosylation of Candida albicans mannoproteins and glycolipids differs with growth temperature and serotype. Infect. Immun. 70: 52745278.
85. Tsuchimori, N.,, L. L. Sharkey,, W. A. Fonzi,, S. W. French,, J. E. Edwards, Jr., and, S. G. Filler. 2000. Reduced virulence of HWP1- deficient mutants of Candida albicans and their interactions with host cells. Infect. Immun. 68: 19972002.
86. Underhill, D. M.,, A. Ozinsky,, A. M. Hajjar,, A. Stevens,, C. B. Wilson,, M. Bassetti, et al. 1999. The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature 401: 811815.
87. Underhill, D. M., and, A. Ozinsky. 2002. Toll-like receptors: key mediators of microbe detection. Curr. Opin. Immunol. 14: 103110.
88. Underhill, D. M.,, E. Rossnagle,, C. A. Lowell, and, R. M. Simmons. 2005. Dectin-1 activates Syk tyrosine kinase in a dynamic subset of macrophages for reactive oxygen production. Blood 106: 25432550.
89. Underhill, D. M. 2004. Toll-like receptors and microbes take aim at each other. Curr. Opin. Immunol. 16: 483487.
90. Urban, C.,, K. Sohn,, F. Lottspeich,, H. Brunner, and, S. Rupp. 2003. Identification of cell surface determinants in Candida albicans reveals Tsa1p, a protein differentially localized in the cell. FEBS Lett. 544: 228235.
91. Urban, C.,, X. Xiong,, K. Sohn,, K. Schroppel,, H. Brunner, and, S. Rupp. 2005. The moonlighting protein Tsa1p is implicated in oxidative stress response and in cell wall biogenesis in Candida albicans. Mol. Microbiol. 57: 13181341.
92. van Deventer, H. J.,, W. H. Goessens,, A. J. van Vliet, and, H. A. Verbrugh. 1996. Antienolase antibodies partially protective against systemic candidiasis in mice. Clin. Microbiol. Infect. 2: 3643.
93. Villamon, E.,, D. Gozalbo,, P. Roig,, J. E. O’Connor,, M. L. Ferrandiz,, D. Fradelizi, et al. 2004. Toll-like receptor 2 is dispensable for acquired host immune resistance to Candida albicans in a murine model of disseminated candidiasis. Microbes Infect. 6: 542548.
94. Villamon, E.,, P. Roig,, M. L. Gil, and, D. Gozalbo. 2005. Toll-like receptor 2 mediates prostaglandin E(2) production in murine peritoneal macrophages and splenocytes in response to Candida albicans. Res. Microbiol. 156: 115118.
95. Wheeler, R. T., and, G. R. Fink. 2006. A drug-sensitive genetic network masks fungi from the immune system. PLoS Pathog. 2: e35.
96. Yamamoto, Y.,, T. W. Klein, and, H. Friedman. 1997. Involvement of mannose receptor in cytokine interleukin-1beta (IL-1beta), IL-6, and granulocyte-macrophage colony-stimulating factor responses, but not in chemokine macrophage inflammatory protein 1beta (MIP-1beta), MIP-2, and KC responses, caused by attachment of Candida albicans to macrophages. Infect. Immun. 65: 10771082.

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