Fungal-induced cell cycle impairment, chromosome instability and apoptosis via differential activation of NF-κB

PLoS Pathogens

Volumn 8, Issue 3, 2012, Pages

  Ben Abdallah, Mariem ^a,b   Sturny Leclère, Aude ^a,b   Avé, Patrick ^a   Louise, Anne ^a   Moyrand, Frédérique ^a   Weih, Falk ^c   Janbon, Guilhem ^a   Mémet, Sylvie ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c FRITZ LIPMANN INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ANEUPLOIDY; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL FATE; CELL GROWTH; CELL MUTANT; CELL PROLIFERATION; CELL VIABILITY; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; FUNGAL STRAIN; FUNGUS MUTANT; G2 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; GROWTH INHIBITION; HOST PATHOGEN INTERACTION; IMMUNE RESPONSE; INFLAMMATION; M PHASE CELL CYCLE CHECKPOINT; MACROPHAGE; MOUSE; NONHUMAN; PHAGOCYTOSIS; S PHASE CELL CYCLE CHECKPOINT; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; CELL CYCLE CHECKPOINT; CELL LINE; CELL SURVIVAL; GENE EXPRESSION REGULATION; GENETICS; IMMUNE EVASION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOUSE STRAIN; PATHOGENICITY; PHYSIOLOGY; TRANSGENIC MOUSE;

FILOBASIDIELLA NEOFORMANS;

ANEUPLOIDY; ANIMALS; APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CHROMOSOMAL INSTABILITY; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; IMMUNE EVASION; MACROPHAGES; MICE; MICE, INBRED STRAINS; MICE, TRANSGENIC; NF-KAPPA B; SIGNAL TRANSDUCTION;

EID: 84861209808     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002555     Document Type: Article

References (63)

1. Dromer F, Mathoulin-Pelissier S, Launay O, Lortholary O, Group. FCS (2007) Determinants of disease presentation and outcome during cryptococcosis: the CryptoA/D study. PLOS Med 4: e21.
2. Park BJ, Wannemuehler KA, Marston BJ, Govender N, Pappas PG, et al. (2009) Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 23: 525-530.
3. Idnurm A, Bahn YS, Nielsen K, Lin X, Fraser JA, et al. (2005) Deciphering the model pathogenic fungus Cryptococcus neoformans. Nat Rev Microbiol 3: 753-764.
4. Hohl TM, Rivera A, Pamer EG (2006) Immunity to fungi. Curr Opin Immunol 18: 465-472.
5. Voelz K, May RC (2010) Cryptococcal interactions with the host immune system. Eukaryot Cell 9: 835-846.
6. Botts MR, Hull CM (2010) Dueling in the lung: how Cryptococcus spores race the host for survival. Curr Opin Microbiol 13: 437-442.
7. Grinsell M, Weinhold LC, Cutler JE, Han Y, Kozel TR (2001) In vivo clearance of glucuronoxylomannan, the major capsular polysaccharide of Cryptococcus neoformans: a critical role for tissue macrophages. J Infect Dis 184: 479-487.
8. Levitz SM (2001) Cryptococcus neoformans: intracellular or extracellular? Trends Microbiol 9: 417-418.
9. Shao X, Mednick A, Alvarez M, van Rooijen N, Goldman DL (2005) An innate immune system cell is a major determinant of species-related susceptibility differences to fungal pneumonia. J Immunol 175: 3244-3251.
10. Kechichian TB, Shea J, Del Poeta M (2007) Depletion of alveolar macrophages decreases the dissemination of a glucosylceramide-deficient mutant of Crypto-coccus neoformans in immunodeficient mice. Infect Immun 75: 4792-4798.
11. Osterholzer JJ, Milam JE, Chen GH, Toews GB, Huffnagle GB, et al. (2009) Role of dendritic cells and alveolar macrophages in regulating early host defense against pulmonary infection with Cryptococcus neoformans. Infect Immun 77: 3749-3758.
12. Zaragoza O, Rodrigues ML, De Jesus M, Frases S, Dadachova E, et al. (2009) The capsule of the fungal pathogen Cryptococcus neoformans. Adv Appl Microbiol 68: 133-216.
13. Stano P, Williams V, Villani M, Cymbalyuk ES, Qureshi A, et al. (2009) App1: an antiphagocytic protein that binds to complement receptors 3 and 2. J Immunol 182: 84-91.
14. Chun CD, Brown JC, Madhani HD (2011) A Major Role for Capsule-Independent Phagocytosis-Inhibitory Mechanisms in Mammalian Infection by Cryptococcus neoformans. Cell Host Microbe 9: 243-251.
15. Alvarez M, Casadevall A (2006) Phagosome extrusion and host-cell survival after Cryptococcus neoformans phagocytosis by macrophages. Curr Biol 16: 2161-2165.
16. Ma H, Croudace JE, Lammas DA, May RC (2006) Expulsion of live pathogenic yeast by macrophages. Curr Biol 16: 2156-2160.
17. Tucker SC, Casadevall A (2002) Replication of Cryptococcus neoformans in macrophages is accompanied by phagosomal permeabilization and accumulation of vesicles containing polysaccharide in the cytoplasm. Proc Natl Acad Sci USA 99: 3165-3170.
18. Nussbaum G, Anandasabapathy S, Mukherjee J, Fan M, Casadevall A, et al (1999) Molecular and idiotypic analyses of the antibody response to Cryptococcus neoformans glucuronoxylomannan-protein conjugate vaccine in autoimmune and nonautoimmune mice. Infect Immun 67: 4469-4476.
19. Levitz SM (2002) Receptor-mediated recognition of Cryptococcus neoformans. Nippon Ishinkin Gakkai Zasshi 43: 133-136.
20. Kelly RM, Chen J, Yauch LE, Levitz SM (2005) Opsonic requirements for dendritic cell-mediated responses to Cryptococcus neoformans. Infect Immun 73: 592-598.
21. Pericolini E, Cenci E, Monari C, De Jesus M, Bistoni F, et al. (2006) Cryptococcus neoformans capsular polysaccharide component galactoxylomannan induces apoptosis of human T-cells through activation of caspase-8. Cell Microbiol 8: 267-275.
22. Monari C, Paganelli F, Bistoni F, Kozel TR, Vecchiarelli A (2008) Capsular polysaccharide induction of apoptosis by intrinsic and extrinsic mechanisms. Cell Microbiol 10: 2129-2137.
23. Villena SN, Pinheiro RO, Pinheiro CS, Nunes MP, Takiya CM, et al. (2008) Capsular polysaccharides galactoxylomannan and glucuronoxylomannan from Cryptococcus neoformans induce macrophage apoptosis mediated by Fas ligand. Cell Microbiol 10: 1274-1285.
24. Chiapello LS, Baronetti JL, Garro AP, Spesso MF, Masih DT (2008) Cryptococcus neoformans glucuronoxylomannan induces macrophage apoptosis mediated by nitric oxide in a caspase-independent pathway. Int Immunol 20: 1527-1541.
25. Gilmore TD (2006) Introduction to NF-kappaB: players, pathways, perspectives. Oncogene 25: 6680-6684.
26. Hayden MS, West AP, Ghosh S (2006) NF-kappaB and the immune response. Oncogene 25: 6758-6780.
27. Dutta J, Fan Y, Gupta N, Fan G, Gelinas C (2006) Current insights into the regulation of programmed cell death by NF-kappaB. Oncogene 25: 6800-6816.
28. Hayden MS, Ghosh S (2008) Shared principles in NF-kappaB signaling. Cell 132: 344-362.
29. Lawrence T, Bebien M, Liu GY, Nizet V, Karin M (2005) IKKalpha limits macrophage NF-kappaB activation and contributes to the resolution of inflammation. Nature 434: 1138-1143.
30. Li Q, Lu Q, Bottero V, Estepa G, Morrison L, et al. (2005) Enhanced NF-kappaB activation and cellular function in macrophages lacking IkappaB kinase 1 (IKK1). Proc Natl Acad Sci USA 102: 12425-12430.
31. Bonizzi G, Karin M (2004) The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol 25: 280-288.
32. Vallabhapurapu S, Karin M (2009) Regulation and function of NF-kappaB transcription factors in the immune system. Annu Rev Immunol 27: 693-733.
33. Dejardin E (2006) The alternative NF-kappaB pathway from biochemistry to biology: pitfalls and promises for future drug development. Biochem Pharmacol 72: 1161-1179.
34. Moyrand F, Janbon G (2004) UGD1, encoding the Cryptococcus neoformans UDP-glucose dehydrogenase, is essential for growth at 37 degrees C and for capsule biosynthesis. Eukaryot Cell 3: 1601-1608.
35. Levitz SM, DiBenedetto DJ (1989) Paradoxical role of capsule in murine bronchoalveolar macrophage-mediated killing of Cryptococcus neoformans. J Immunol 142: 659-665.
36. Moyrand F, Fontaine T, Janbon G (2007) Systematic capsule gene disruption reveals the central role of galactose metabolism on Cryptococcus neoformans virulence. Mol Microbiol 64: 771-781.
37. Charlier C, Chretien F, Baudrimont M, Mordelet E, Lortholary O, et al. (2005) Capsule Structure Changes Associated with Cryptococcus neoformans Crossing of the Blood-Brain Barrier. Am J Pathol 166: 421-432.
38. Caamano JH, Rizzo CA, Durham SK, Barton DS, Raventossuarez C, et al. (1998) Nuclear factor (NF)-kappa-B2 (p100/p52) is required for normal splenic microarchitecture and B cell-mediated immune responses. J Exp Med 187: 185-196.
39. Michel LS, Liberal V, Chatterjee A, Kirchwegger R, Pasche B, et al. (2001) MAD2 haplo-insufficiency causes premature anaphase and chromosome instability in mammalian cells. Nature 409: 355-359.
40. Sotillo R, Hernando E, Diaz-Rodriguez E, Teruya-Feldstein J, Cordon-Cardo C, et al. (2007) Mad2 overexpression promotes aneuploidy and tumorigenesis in mice. Cancer Cell 11: 9-23.
41. Fong CH, Bebien M, Didierlaurent A, Nebauer R, Hussell T, et al. (2008) An antiinflammatory role for IKKbeta through the inhibition of "classical" macrophage activation. J Exp Med 205: 1269-1276.
42. Porta C, Rimoldi M, Raes G, Brys L, Ghezzi P, et al. (2009) Tolerance and M2 (alternative) macrophage polarization are related processes orchestrated by p50 nuclear factor kappaB. Proc Natl Acad Sci USA 106: 14978-14983.
43. Labbe K, Saleh M (2008) Cell death in the host response to infection. Cell Death Differ 15: 1339-1349.
44. Lawrence T, Gilroy DW, Colville-Nash PR, Willoughby DA (2001) Possible new role for NF-kappaB in the resolution of inflammation. Nat Med 7: 1291-1297.
45. Pericolini E, Gabrielli E, Cenci E, De Jesus M, Bistoni F, et al. (2009) Involvement of glycoreceptors in galactoxylomannan-induced T cell death. J Immunol 182: 6003-6010.
46. Fan Y, Dutta J, Gupta N, Fan G, Gelinas C (2008) Regulation of programmed cell death by NF-kappaB and its role in tumorigenesis and therapy. Adv Exp Med Biol 615: 223-250.
47. Ouaaz F, Li M, Beg AA (1999) A critical role for the RelA subunit of nuclear factor kappa B in regulation of multiple immune-response genes and in Fasinduced cell death. J Exp Med 189: 999-1004.
48. Nougayrède JP, Taieb F, De Rycke J, Oswald E (2005) Cyclomodulins: bacterial effectors that modulate the eukaryotic cell cycle. Trends Microbiol 13: 103-110.
49. Sieg SF, Harding CV, Lederman MM (2001) HIV-1 infection impairs cell cycle progression of CD4(+) T cells without affecting early activation responses. J Clin Invest 108: 757-764.
50. Stajich JE, Dietrich FS (2006) Evidence of mRNA-mediated intron loss in the human-pathogenic fungus Cryptococcus neoformans. Eukaryot Cell 5: 789-793.
51. Luo Y, Tucker SC, Casadevall A (2005) Fc- and complement-receptor activation stimulates cell cycle progression of macrophage cells from G1 to S. J Immunol 174: 7226-7233.
52. Luo Y, Casadevall A (2010) Intracellular cryptococci suppress Fc-mediated cyclin D1 elevation. Commun Integr Biol 3: 390-391.
53. Goudeau B, Huetz F, Samson S, Di Santo JP, Cumano A, et al. (2003) IkappaBalpha/IkappaBepsilon deficiency reveals that a critical NF-kappaB dosage is required for lymphocyte survival. Proc Natl Acad Sci USA 100: 15800-15805.
54. Barre B, Perkins ND (2007) A cell cycle regulatory network controlling NF-kappaB subunit activity and function. Embo J 26: 4841-4855.
55. Schneider G, Saur D, Siveke JT, Fritsch R, Greten FR, et al. (2006) IKKalpha controls p52/RelB at the skp2 gene promoter to regulate G1- to S-phase progression. Embo J 25: 3801-3812.
56. Hinz M, Krappmann D, Eichten A, Heder A, Scheidereit C, et al. (1999) NF-kappa B function in growth control: Regulation of cyclin D1 expression and G(0)G(1)-to-S-Phase transition. Mol Cell Biol 19: 2690-2698.
57. Bash J, Zong WX, Gelinas C (1997) c-rel arrests the proliferation of HeLa cells and affects critical regulators of the G1/S-phase transition. Mol Cell Biol 17: 6526-6536.
58. Janbandhu VC, Singh AK, Mukherji A, Kumar V (2010) p65 Negatively regulates transcription of the cyclin E gene. J Biol Chem 285: 17453-17464.
59. Bartz SR, Rogel ME, Emerman M (1996) Human immunodeficiency virus type 1 cell cycle control: Vpr is cytostatic and mediates G2 accumulation by a mechanism which differs from DNA damage checkpoint control. J Virol 70: 2324-2331.
60. Machida K, Liu JC, McNamara G, Levine A, Duan L, et al. (2009) Hepatitis C virus causes uncoupling of mitotic checkpoint and chromosomal polyploidy through the Rb pathway. J Virol 83: 12590-12600.
61. Umeda M, Murata-Kamiya N, Saito Y, Ohba Y, Takahashi M, et al. (2009) Helicobacter pylori CagA causes mitotic impairment and induces chromosomal instability. J Biol Chem 284: 22166-22172.
62. Schvartzman JM, Sotillo R, Benezra R (2010) Mitotic chromosomal instability and cancer: mouse modelling of the human disease. Nat Rev Cancer 10: 102-115.
63. Chi YH, Ward JM, Cheng LI, Yasunaga J, Jeang KT (2009) Spindle assembly checkpoint and p53 deficiencies cooperate for tumorigenesis in mice. Int J Cancer 124: 1483-1489.