Antibody binding to Cryptococcus neoformans impairs budding by altering capsular mechanical properties

Journal of Immunology

Volumn 190, Issue 1, 2013, Pages 317-323

  Cordero, Radames J B ^a   Pontes, Bruno ^b   Frases, Susana ^b   Nakouzi, Antonio S ^a   Nimrichter, Leonardo ^b   Rodrigues, Marcio L ^b,c   Viana, Nathan B ^b   Casadevall, Arturo ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL POLYSACCHARIDE; GLUCURONOXYLOMANNAN; MONOCLONAL ANTIBODY;

ANTIGEN BINDING; ARTICLE; CELL BUDDING; CONCENTRATION RESPONSE; CONTROLLED STUDY; CROSS LINKING; CRYPTOCOCCUS NEOFORMANS; FUNGAL CAPSULE; NONHUMAN; OPTICAL TWEEZERS; PRIORITY JOURNAL; YOUNG MODULUS;

ANTIBODIES, FUNGAL; ANTIGENS, FUNGAL; BINDING SITES, ANTIBODY; CELL DIVISION; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; FUNGAL CAPSULES; HYDRODYNAMICS; OPTICAL TWEEZERS; POLYSACCHARIDES; STRESS, MECHANICAL;

EID: 84871840392     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202324     Document Type: Article

References (60)

1. Casadevall, A., and L. A. Pirofski. 2012. A new synthesis for antibody-mediated immunity. Nat. Immunol. 13: 21-28.
2. McClelland, E. E., A. M. Nicola, R. Prados-Rosales, and A. Casadevall. 2010. Ab binding alters gene expression in Cryptococcus neoformans and directly modulates fungal metabolism. J. Clin. Invest. 120: 1355-1361.
3. Yano, M., S. Gohil, J. R. Coleman, C. Manix, and L. A. Pirofski. 2011. Antibodies to Streptococcus pneumoniae capsular polysaccharide enhance pneumococcal quorum sensing. MBio. 2: pii. .
4. McClelland, E. E., P. Bernhardt, and A. Casadevall. 2005. Coping with multiple virulence factors: which is most important? PLoS Pathog. 1: e40.
5. Chang, Y. C., and K. J. Kwon-Chung. 1994. Complementation of a capsule-deficient mutation of Cryptococcus neoformans restores its virulence. Mol. Cell. Biol. 14: 4912-4919. (Pubitemid 24196840)
6. Kozel, T. R., G. S. Pfrommer, A. S. Guerlain, B. A. Highison, and G. J. Highison. 1988. Role of the capsule in phagocytosis of Cryptococcus neoformans. Rev. Infect. Dis. 10(Suppl 2): S436-S439.
7. Kozel, T. R., and E. C. Gotschlich. 1982. The capsule of Cryptococcus neoformans passively inhibits phagocytosis of the yeast by macrophages. J. Immunol. 129: 1675-1680. (Pubitemid 12031112)
8. Zaragoza, O., M. L. Rodrigues, M. De Jesus, S. Frases, E. Dadachova, and A. Casadevall. 2009. The capsule of the fungal pathogen Cryptococcus neoformans. Adv. Appl. Microbiol. 68: 133-216.
9. Cordero, R. J., B. Pontes, A. J. Guimarães, L. R. Martinez, J. Rivera, B. C. Fries, L. Nimrichter, M. L. Rodrigues, N. B. Viana, and A. Casadevall. 2011. Chronological aging is associated with biophysical and chemical changes in the capsule of Cryptococcus neoformans. Infect. Immun. 79: 4990-5000.
10. Cordero, R. J., S. Frases, A. J. Guimaräes, J. Rivera, and A. Casadevall. 2011. Evidence for branching in cryptococcal capsular polysaccharides and consequences on its biological activity. Mol. Microbiol. 79: 1101-1117.
11. Frases, S., B. Pontes, L. Nimrichter, N. B. Viana, M. L. Rodrigues, and A. Casadevall. 2009. Capsule of Cryptococcus neoformans grows by enlargement of polysaccharide molecules. Proc. Natl. Acad. Sci. U S A 106: 1228-1233.
12. Casadevall, A., and L. A. Pirofski. 2012. Immunoglobulins in defense, pathogenesis, and therapy of fungal diseases. Cell Host Microbe 11: 447-456.
13. Sanford, J. E., D. M. Lupan, A. M. Schlageter, and T. R. Kozel. 1990. Passive immunization against Cryptococcus neoformans with an isotype-switch family of monoclonal antibodies reactive with cryptococcal polysaccharide. Infect. Immun. 58: 1919-1923. (Pubitemid 20176392)
14. Mukherjee, J., M. D. Scharff, and A. Casadevall. 1992. Protective murine monoclonal antibodies to Cryptococcus neoformans. Infect. Immun. 60: 4534-4541.
15. Fleuridor, R., Z. Zhong, and L. Pirofski. 1998. A human IgM monoclonal antibody prolongs survival of mice with lethal cryptococcosis. J. Infect. Dis. 178: 1213-1216. (Pubitemid 28452228)
16. Dromer, F., J. Charreire, A. Contrepois, C. Carbon, and P. Yeni. 1987. Protection of mice against experimental cryptococcosis by anti-Cryptococcus neoformans monoclonal antibody. Infect. Immun. 55: 749-752. (Pubitemid 17021971)
17. Larsen, R. A., P. G. Pappas, J. Perfect, J. A. Aberg, A. Casadevall, G. A. Cloud, R. James, S. Filler, and W. E. Dismukes. 2005. Phase I evaluation of the safety and pharmacokinetics of murine-derived anticryptococcal antibody 18B7 in subjects with treated cryptococcal meningitis. Antimicrob. Agents Chemother. 49: 952-958. (Pubitemid 40327709)
18. Casadevall, A., W. Cleare, M. Feldmesser, A. Glatman-Freedman, D. L. Goldman, T. R. Kozel, N. Lendvai, J. Mukherjee, L. A. Pirofski, J. Rivera, et al. 1998. Characterization of a murine monoclonal antibody to Cryptococcus neoformans polysaccharide that is a candidate for human therapeutic studies. Antimicrob. Agents Chemother. 42: 1437-1446. (Pubitemid 28257647)
19. Yuan, R. R., G. Spira, J. Oh, M. Paizi, A. Casadevall, and M. D. Scharff. 1998. Isotype switching increases efficacy of antibody protection against Cryptococcus neoformans infection in mice. Infect. Immun. 66: 1057-1062. (Pubitemid 28101146)
20. Taborda, C. P., J. Rivera, O. Zaragoza, and A. Casadevall. 2003. More is not necessarily better: prozone-like effects in passive immunization with IgG. J. Immunol. 170: 3621-3630. (Pubitemid 36359231)
21. Taborda, C. P., and A. Casadevall. 2001. Immunoglobulin M efficacy against Cryptococcus neoformans: mechanism, dose dependence, and prozone-like effects in passive protection experiments. J. Immunol. 166: 2100-2107. (Pubitemid 32114700)
22. Nussbaum, G., W. Cleare, A. Casadevall, M. D. Scharff, and P. Valadon. 1997. Epitope location in the Cryptococcus neoformans capsule is a determinant of antibody efficacy. J. Exp. Med. 185: 685-694. (Pubitemid 27098153)
23. Martinez, L. R., D. Moussai, and A. Casadevall. 2004. Antibody to Cryptococcus neoformans glucuronoxylomannan inhibits the release of capsular antigen. Infect. Immun. 72: 3674-3679. (Pubitemid 38697802)
24. Martinez, L. R., and A. Casadevall. 2005. Specific antibody can prevent fungal biofilm formation and this effect correlates with protective efficacy. Infect. Immun. 73: 6350-6362. (Pubitemid 41368796)
25. McClelland, E. E., and A. Casadevall. 2012. Strain-related differences in antibody-mediated changes in gene expression are associated with differences in capsule and location of binding. Fungal Genet. Biol. 49: 227-234.
26. MacGill, T. C., R. S. MacGill, A. Casadevall, and T. R. Kozel. 2000. Biological correlates of capsular (quellung) reactions of Cryptococcus neoformans. J. Immunol. 164: 4835-4842. (Pubitemid 30238087)
27. Mukherjee, J., W. Cleare, and A. Casadevall. 1995. Monoclonal antibody mediated capsular reactions (Quellung) in Cryptococcus neoformans. J. Immunol. Methods 184: 139-143.
28. Cleare, W., M. E. Brandt, and A. Casadevall. 1999. Monoclonal antibody 13F1 produces annular immunofluorescence patterns on Cryptococcus neoformans serotype AD isolates. J. Clin. Microbiol. 37: 3080. (Pubitemid 29391951)
29. Yuan, R., A. Casadevall, G. Spira, and M. D. Scharff. 1995. Isotype switching from IgG3 to IgG1 converts a nonprotective murine antibody to Cryptococcus neoformans into a protective antibody. J. Immunol. 154: 1810-1816.
30. Mukherjee, J., A. Casadevall, and M. D. Scharff. 1993. Molecular characterization of the humoral responses to Cryptococcus neoformans infection and glucuronoxylomannan-tetanus toxoid conjugate immunization. J. Exp. Med. 177: 1105-1116. (Pubitemid 23097399)
31. Spira, G., M. Paizi, S. Mazar, G. Nussbaum, S. Mukherjee, and A. Casadevall. 1996. Generation of biologically active anti-Cryptococcus neoformans IgG, IgE and IgA isotype switch variant antibodies by acridine orange mutagenesis. Clin. Exp. Immunol. 105: 436-442. (Pubitemid 26297887)
32. Frases, S., B. Pontes, L. Nimrichter, M. L. Rodrigues, N. B. Viana, and A. Casadevall. 2009. The elastic properties of the Cryptococcus neoformans capsule. Biophys. J. 97: 937-945.
33. Nicola, A. M., S. Frases, and A. Casadevall. 2009. Lipophilic dye staining of Cryptococcus neoformans extracellular vesicles and capsule. Eukaryot. Cell 8: 1373-1380.
34. Araujo, Gde. S., F. L. Fonseca, B. Pontes, A. Torres, R. J. Cordero, R. M. Zancopé-Oliveira, A. Casadevall, N. B. Viana, L. Nimrichter, M. L. Rodrigues, et al. 2012. Capsules from pathogenic and non-pathogenic Cryptococcus spp. manifest significant differences in structure and ability to protect against phagocytic cells. PLoS ONE 7: e29561.
35. Teraoka, I. 2002. Polymer Solutions: An Introduction to Physical Properties. Wiley, New York.
36. Jain, N., E. Cook, I. Xess, F. Hasan, D. Fries, and B. C. Fries. 2009. Isolation and characterization of senescent Cryptococcus neoformans and implications for phenotypic switching and pathogenesis in chronic cryptococcosis. Eukaryot. Cell 8: 858-866.
37. Mukherjee, J., G. Nussbaum, M. D. Scharff, and A. Casadevall. 1995. Protective and nonprotective monoclonal antibodies to Cryptococcus neoformans originating from one B cell. J. Exp. Med. 181: 405-409.
38. Rivera, J., and A. Casadevall. 2005. Mouse genetic background is a major determinant of isotype-related differences for antibody-mediated protective efficacy against Cryptococcus neoformans. J. Immunol. 174: 8017-8026. (Pubitemid 40806313)
39. Torres, M., R. May, M. D. Scharff, and A. Casadevall. 2005. Variable-region-identical antibodies differing in isotype demonstrate differences in fine specificity and idiotype. J. Immunol. 174: 2132-2142. (Pubitemid 40223957)
40. Murphy, D. B. 2001. Fundamentals of Light Microscopy and Electronic Imaging. Wiley-Liss, New York.
41. Neufeld, F. 1902. Über die Agglutination der Pneumokokken und über die Theorieen der Agglutination. Z. Hyg. Infektionskr. 40.
42. Mukherjee, J., M. Feldmesser, M. D. Scharff, and A. Casadevall. 1995. Monoclonal antibodies to Cryptococcus neoformans glucuronoxylomannan enhance fluconazole efficacy. Antimicrob. Agents Chemother. 39: 1398-1405.
43. Dromer, F., C. Perronne, J. Barge, J. L. Vilde, and P. Yeni. 1989. Role of IgG and complement component C5 in the initial course of experimental cryptococcosis. Clin. Exp. Immunol. 78: 412-417. (Pubitemid 20009077)
44. Diamond, R. D., R. K. Root, and J. E. Bennett. 1972. Factors influencing killing of Cryptococcus neoformans by human leukocytes in vitro. J. Infect. Dis. 125: 367-376.
45. Campbell, N. A., and J. B. Reece. 2009. Biology. Pearson Benjamin Cummings, San Francisco.
46. Torres, M., N. Fernández-Fuentes, A. Fiser, and A. Casadevall. 2007. The immunoglobulin heavy chain constant region affects kinetic and thermodynamic parameters of antibody variable region interactions with antigen. J. Biol. Chem. 282: 13917-13927. (Pubitemid 47100519)
47. Roux, K. H., L. Strelets, and T. E. Michaelsen. 1997. Flexibility of human IgG subclasses. J. Immunol. 159: 3372-3382. (Pubitemid 127482096)
48. Abdelmoula, M., F. Spertini, T. Shibata, Y. Gyotoku, S. Luzuy, P. H. Lambert, and S. Izui. 1989. IgG3 is the major source of cryoglobulins in mice. J. Immunol. 143: 526-532. (Pubitemid 19191547)
49. Gavin, A. L., N. Barnes, H. M. Dijstelbloem, and P. M. Hogarth. 1998. Identification of the mouse IgG3 receptor: implications for antibody effector function at the interface between innate and adaptive immunity. J. Immunol. 160: 20-23. (Pubitemid 28116709)
50. Greenspan, N. S., and L. J. Cooper. 1992. Intermolecular cooperativity: a clue to why mice have IgG3? Immunol. Today 13: 164-168.
51. Siira, L., T. Kaijalainen, L. Lambertsen, M. H. Nahm, M. Toropainen, and A. Virolainen. 2012. From Quellung to multiplex PCR, and back when needed, in pneumococcal serotyping. J. Clin. Microbiol. 50: 2727-2731.
52. Evans, E. E. 1960. Capsular reactions of Cryptococcus neoformans. Ann. N. Y. Acad. Sci. 89: 184-192.
53. Aspnes, D. E. 1982. Local-field effects and effective-medium theory - a microscopic perspective. Am. J. Phys. 50: 704-709.
54. Gates, M. A., P. Thorkildson, and T. R. Kozel. 2004. Molecular architecture of the Cryptococcus neoformans capsule. Mol. Microbiol. 52: 13-24. (Pubitemid 38519618)
55. Levin, D. E. 2005. Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69: 262-291. (Pubitemid 40847940)
56. McLean, G. R., M. Torres, N. Elguezabal, A. Nakouzi, and A. Casadevall. 2002. Isotype can affect the fine specificity of an antibody for a polysaccharide antigen. J. Immunol. 169: 1379-1386. (Pubitemid 34809182)
57. Beningo, K. A., and Y. L. Wang. 2002. Fc-receptor-mediated phagocytosis is regulated by mechanical properties of the target. J. Cell Sci. 115: 849-856. (Pubitemid 34196344)
58. Underhill, D. M., and H. S. Goodridge. 2012. Information processing during phagocytosis. Nat. Rev. Immunol. 12: 492-502.
59. Alvarez, M., C. Saylor, and A. Casadevall. 2008. Antibody action after phagocytosis promotes Cryptococcus neoformans and Cryptococcus gattii macrophage exocytosis with biofilm-like microcolony formation. Cell. Microbiol. 10: 1622-1633. (Pubitemid 352006146)
60. Alexander, H. E. 1943. Treatment of Haemophilus influenzae infections and of meningococcic and pneumococcic meningitis. Am. J. Dis. Child. 66: 172-187.