Low Concentrations of Hydrogen Peroxide or Nitrite Induced of Paracoccidioides brasiliensis Cell Proliferation in a Ras-Dependent Manner

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Haniu, Ana Eliza Coronel Janu ^a   Maricato, Juliana Terzi ^a   Mathias, Pedro Paulo Moraes ^a   Castilho, Daniele Gonçalves ^a   Miguel, Rodrigo Bernardi ^a   Monteiro, Hugo Pequeno ^a   Puccia, Rosana ^a   Batista, Wagner Luiz ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; HYDROGEN PEROXIDE; NITRITE; PROTEIN FARNESYLTRANSFERASE INHIBITOR; RAS PROTEIN; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE;

ARTICLE; CELL PROLIFERATION; CONCENTRATION RESPONSE; ENZYME ACTIVATION; FUNGAL CELL; IN VITRO STUDY; NITROSYLATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PARACOCCIDIOIDES BRASILIENSIS; PLASMID; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROCESSING;

CELL PROLIFERATION; HYDROGEN PEROXIDE; NITRITES; PARACOCCIDIOIDES; RAS PROTEINS;

EID: 84880794994     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069590     Document Type: Article

References (69)

1. Brummer E, Hanson LH, Restrepo A, Stevens DA, (1989) Intracellular multiplication of Paracoccidioides brasiliensis in macrophages - killing and restriction of multiplication by activated macrophages. Infection and Immunity 57: 2289-2294.
2. Calvi SA, Peracoli MT, Mendes RP, Marcondes-Machado J, Fecchio D, et al. (2003) Effect of cytokines on the in vitro fungicidal activity of monocytes from paracoccidioidomycosis patients. Microbes Infect 5: 107-113.
3. Romani L, (2004) Immunity to fungal infections. Nature Review Immunology 4: 1-23.
4. Nathan C, (2006) Neutrophilis and immunity: challenges and opportunities. Nature Review Immunology 6: 173-182.
5. Tavares AH, Simoneide SS, Dantas A, Campos EG, Andrade RV, et al. (2007) Early transcriptional response of Paracoccidioides brasiliensis upon internalization by murine macrophages. Microbes and Infection 9: 583-590.
6. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS, (2005) Protein S-nitrosylation: Purview and parameters. Nature Rev Mol Cell Biol 6: 150-166.
7. Monteiro HP, Arai RJ, Travassos LR, (2008) Protein tyrosine phosphorylation and protein tyrosine nitration in redox signaling. Antioxidant Redox Signal 10 (5):: 843-889.
8. Lengeler KB, Davidson RC, D'souza C, Harashima T, Shen WC, et al. (2000) Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 64 (4):: 746-785.
9. Cano E, Mahadevan LC, (1995) Parallel signal processing among mammalian MAPKs. Trends Biochem Sci 20 (3):: 117-122.
10. Dérijard B, Hibi M, Wu IH, Barrett T, Su B, et al. (1994) JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 76 (6):: 1025-1037.
11. Elion EA, Satterberg B, Kranz JE, (1993) FUS3 phosphorylates multiple components of the mating signal transduction cascade: evidence for STE12 and FAR1. Mol Biol Cell 4 (5):: 495-510.
12. Takai Y, Sasaki T, Matozaki T, (2001) Small GTP-binding proteins. Physiol Rev 81: 153-208.
13. Karnoub AE, Weinberg RA, (2008) Ras oncogene: split personalities. Nature Rev Mol Cell Biol 9: 517-531.
14. Waugh MS, Nichols CB, De Cesare CM, Cox GM, Heitman J, et al. (2002) Ras1 and Ras2 contribute shared and unique roles in physiology and virulence of Cryptococcus neoformans. Microbiology 148 (Pt 1):: 191-201.
15. Zhang J, Zhang Y, Zhong Y, Qu Y, Wang T, (2012) Ras GTPases modulate morphogenesis, sporulation and cellulase gene expression in the cellulolytic fungus Trichoderma reesei. PLoS One 7 (11):: e48786.
16. Xie XQ, Guan Y, Ying SH, Feng MG, (2013) Differentiated functions of Ras1 and Ras2 proteins in regulating the germination, growth, conidiation, multi-stress tolerance and virulence of Beauveria bassiana. Environ Microbiol 15 (2):: 447-462.
17. Tamanoi F, Ras signaling in yeast. (2011) Genes Cancer 2 (3):: 210-215.
18. Onken B, Wiener H, Philips MR, Chang EC, (2006) Compartmentalized signaling of Ras in fission yeast. Proc Natl Acad Sci 103 (24):: 9045-9050.
19. Fehrenbacher N, Bar-Sagi D, Philips M, (2009) Ras/MAPK signaling from endomembranes. Mol Oncol 3 (4):: 297-307.
20. Chang EC, Philips MR, (2006) Spatial segregation of Ras signaling: new evidence from fission yeast. Cell Cycle 5 (17):: 1936-1939.
21. Fernandes L, Paes HC, Tavares AH, Silva SS, Dantas A, et al. (2008) Transcriptional profile of ras1 and ras2 and the potential role of farnesylation in the dimorphism of the human pathogen Paracoccidioides brasiliensis. FEMS Yeast Res 8 (2):: 300-310.
22. Schnappinger D, Ehrt S, Voskuil MI, Liu Y, Mangan JA, et al. (2003) Transcriptional Adaptation of Mycobacterium tuberculosis within Macrophages: Insights into the Phagosomal Environment. J Exp Med 198 (5):: 693-704.
23. Rhee KY, Erdjument-Bromage H, Tempst P, Nathan CF, (2005) S-nitroso proteome of Mycobacterium tuberculosis: Enzymes of intermediary metabolism and antioxidant defense. Proc Natl Acad Sci U S A 102 (2):: 467-472.
24. Nathan C, Shiloh MU, (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci U S A 97 (16):: 8841-8848.
25. Batista WL, Matsuo AL, Ganiko L, Barros TF, Veiga TR, et al. (2006) The PbMDJ1 gene belongs to a conserved MDJ1/LON locus in thermodimorphic pathogenic fungi and encodes a heat shock protein that localizes to both the mitochondria and cell wall of Paracoccidioides brasiliensis. Eukaryot Cell 5 (2):: 379-390.
26. van Triest M, de Rooij J, Bos JL, (2001) Measurement of GTP-bound Ras-like GTPases by activation-specific probes. Methods Enzymol 333: 343-348.
27. Colombo S, Ronchetti D, Thevelein JM, Winderickx J, Martegani E, (2004) Activation state of the Ras2 protein and glucose-induced signaling in Saccharomyces cerevisiae. J Biol Chem 279 (45):: 46715-46722.
28. Forrester MT, Foster MW, Benhar M, Stamler JS, (2011) Detection of Protein S-Nitrosylation with the Biotin Switch Technique. Free Radic Biol Med 46 (2):: 119-126.
29. Thomas DD, Ridnour LA, Isenberg JS, Flores-Santana W, Switzer CH, et al. (2008) The chemical biology of nitric oxide: implications in cellular signaling. Free Radic Biol. Med 45: 18-31.
30. Quinn J, Findlay VJ, Dawson K, Millar JB, Jones N, et al. (2002) Distinct regulatory proteins control the graded transcriptional response to increasing H(2)O(2) levels in fission yeast Schizosaccharomyces pombe. Mol Biol Cell 13 (3):: 805-816.
31. Vivancos AP, Castillo EA, Jones N, Ayte J, Hidalgo E, (2004) Activation of the redox sensor Pap1 by hydrogen peroxide requires modulation of the intracellular oxidant concentration. Mol Microbiol 52: 1427-1435.
32. Villalobo A, (2006) Nitric oxide and cell proliferation. FEBS J 273 (11):: 2329-2344.
33. Oliveira CJ, Curcio MF, Moraes MS, Tsujita M, Travassos LR, et al. (2008) The low molecular weight S-nitrosothiol, S-nitroso-N-acetylpenicillamine, promotes cell cycle progression in rabbit aortic endothelial cells. Nitric Oxide 18 (4):: 241-255.
34. Takai Y, Sasaki T, Matozaki T, (2001) Small GTP-binding proteins. Physiol Rev 81 (1):: 153-208.
35. Reuter CW, Morgan MA, Bergmann L, (2000) Targeting the Ras signaling pathway: a rational, mechanism-based treatment for hematologic malignancies? Blood 96 (5):: 1655-1669.
36. Scheffzek K, Grünewald P, Wohlgemuth S, Kabsch W, Tu H, et al. (2001) The Ras-Byr2RBD complex: structural basis for Ras effector recognition in yeast. Structure 9 (11):: 1043-1050.
37. Randhawa PK, Rylova S, Heinz JY, Kiser S, Fried JH, et al. (2011) The Ras activator RasGRP3 mediates diabetes-induced embryonic defects and affects endothelial cell migration. Circ Res 108 (10):: 1199-1208.
38. Santibanez JF, Pérez-Gómez E, Fernandez-L A, Garrido-Martin EM, Carnero A, et al. (2010) The TGF-beta co-receptor endoglin modulates the expression and transforming potential of H-Ras. Carcinogenesis 31 (12):: 2145-2154.
39. Rudoni S, Colombo S, Coccetti P, Martegani E, (2001) Role of guanine nucleotides in the regulation of the Ras/cAMP pathway in Saccharomyces cerevisiae. Biochim Biophys Acta 1538 (2-3):: 181-189.
40. Lander HM, Hajjar DP, Hempstead BL, Mirza UA, Chait BT, et al. (1997) A molecular redox switch on p21(ras)- Structural basis for the nitric oxide-p21(ras) interaction. J Biol Chem 272: 4323-4326.
41. Lee TY, Chen YJ, Lu CT, Ching WC, Teng YC, et al. (2012) dbSNO: a database of cysteine S-nitrosylation. Bioinformatics 28 (17):: 2293-2295.
42. Matute DR, Sepulveda VE, Quesada LM, Goldman GH, Taylor JW, et al. (2006) Microsatellite Analysis of Three Phylogenetic Species of Paracoccidioides brasiliensis. J Clin Microbiol 44 (6):: 2153-2157.
43. Teixeira MM, Theodoro RC, Carvalho MJ, Fernandes L, Paes HC, et al. (2009) Phylogenetic analysis reveals a high level of speciation in the Paracoccidioides genus. Mol Phylogenet Evol 52: 273-283.
44. Calich VL, da Costa TA, Felonato M, Arruda C, Bernardino S, et al. (2008) Innate immunity to Paracoccidioides brasiliensis infection. Mycopathologia 165 (4-5):: 223-236.
45. Snelgrove RJ, Edwards L, Willians AE, Rae AJ, Hussell T, (2006) In the absence of reactive oxygen species, T cells default to a Th1 phenotype and mediate protection against pulmonary Cryptococcus neofomans infection. J immunol 177: 5509-5516.
46. Batista WL, Ogata FT, Curcio MF, Miguel RB, Arai RJ, et al. (2013) S-Nitrosoglutathione and Endothelial Nitric Oxide Synthase-Derived Nitric Oxide Regulate Compartmentalized Ras S-Nitrosylation and Stimulate Cell Proliferation. Antioxid Redox Signal 18 (3):: 221-238.
47. Srinivasa K, Kim J, Yee S, Kim W, Choi W, (2012) A MAP kinase pathway is implicated in the pseudohyphal induction by hydrogen peroxide in Candica albicans. Mol Cells 33 (2):: 183-193.
48. Pina A, Bernardino S, Calich VL, (2008) Alveolar macrophages from susceptible mice are more competent than those of resistant mice to control initial Paracoccidioides brasiliensis infection. J Leukoc Biol 83 (5):: 1088-1099.
49. Nascimento FR, Calich VL, Rodríguez D, Russo M, (2002) Dual role for nitric oxide in paracoccidioidomycosis: essential for resistance, but overproduction associated with susceptibility. J Immunol 168 (9):: 4593-4600.
50. Caponigro F, Casale M, Bryce J, (2003) Farnesyl transferase inhibitors in clinical development. Expert Opin Investig Drugs 12 (6):: 943-954.
51. Cullen PJ, Sprague GF Jr, (2012) The regulation of filamentous growth in yeast. Genetics 190 (1):: 23-49.
52. Belden WJ, Larrondo LF, Froehlich AC, Shi M, Chen CH, et al. (2007) The band mutation in Neurospora crassa is a dominant allele of ras-1 implicating RAS signaling in circadian output. Genes Dev 21 (12):: 1494-1505.
53. Pervin S, Singh R, Hernandez E, Wu G, Chaudhuri G, (2007) Nitric oxide in physiologic concentrations targets the translational machinery to increase the proliferation of human breast cancer cells: involvement of mammalian target of rapamycin/eIF4E pathway. Cancer Res 67 (1):: 289-299.
54. Fortwendel JR, Zhao W, Bhabhra R, Park S, Perlin DS, et al. (2005) A fungus-specific ras homolog contributes to the hyphal growth and virulence of Aspergillus fumigatus. Eukaryot Cell 4 (12):: 1982-1989.
55. Leberer E, Harcus D, Dignard D, Johnson L, Ushinsky S, et al. (2001) Ras links cellular morphogenesis to virulence by regulation of the MAP kinase and cAMP signaling pathways in the pathogenic fungus Candida albicans. Mol Microbiol 42: 673-687.
56. Nichols CB, Ferreyra J, Ballou ER, Alspaugh JA, (2009) Subcellular localization directs signaling specificity of the Cryptococcus neoformans Ras1 protein. Eukaryot Cell 8 (2):: 181-189.
57. Monteiro HP, Stern A, (1996) Redox modulation of tyrosine phosphorylation-dependent signal transduction pathways. Free Rad Biol & Med 21: 323-333.
58. Evangelista AM, Kohr MJ, Murphy E, (2013) S-Nitrosylation: Specificity, Occupancy, and Interaction with Other Post-Translational Modifications. Antioxid Redox Signal (in press).
59. Mitchell L, Hobbs GA, Aghajanian A, Campbell SL, (2013) Redox Regulation of Ras and Rho GTPases: Mechanism and Function. Antioxid Redox Signal 18 (3):: 250-258.
60. Davis MF, Vigil D, Campbell SL, Regulation of Ras proteins by reactive nitrogen species. Free radical biology & medicine 51: 565-75, 2011.
61. Raines KW, Bonini MG, Campbell SL, Nitric oxide cell signaling: S-nitrosation of Ras superfamily GTPases. (2007) Cardiovasc Res 75 (2):: 229-239.
62. Heo J, Prutzman KC, Mocanu V, Campbell SL, (2005) Mechanism of free radical nitric oxide-mediated Ras guanine nucleotide dissociation. J Mol Biol 346: 1423-1440.
63. Lander HM, Jacovina AT, Davis RJ, Tauras JM, (1996) Differential activation of mitogen-induced protein kinases by nitric-oxide-related species. J Biol Chem 271: 19705-19709.
64. Seth D, Hausladen A, Wang YJ, Stamler JS, (2012) Endogenous protein S-Nitrosylation in E. coli: regulation by OxyR. Science 336 (6080):: 470-473.
65. Lander HM, Ogiste JS, Pearce SF, Levi R, Novogrodsky A, (1995) Nitric oxide-stimulated guanine nucleotide exchange on p21ras. J Biol Chem 270: 7017-7020.
66. Adachi T, Pimentel DR, Heibeck T, Hou X, Lee YJ, et al. (2004) S-glutathiolation of Ras mediates redox-sensitive signaling by angiotensin II in vascular smooth muscle cells. J Biol Chem 279: 29857-29862.
67. Bhunia AK, Han H, Snowden A, Chatterjee S, (1997) Redox-regulated signaling by lactosylceramide in the proliferation of human aortic smooth muscle cells. J Biol Chem 272: 15642-15649.
68. Tu H, Barr M, Dong DL, Wigler M, (1997) Multiple regulatory domains on the Byr2 protein kinase. Mol Cell Biol 17 (10):: 5876-5887.
69. Feldmesser M, Kress Y, Casadevall A, (2001) Dynamic changes in the morphology of Cryptococcus neoformans during murine pulmonary infection. Microbiology 147 (8):: 2355-2365.