The calcium transporter Pmc1 provides Ca2+ tolerance and influences the progression of murine cryptococcal infection

FEBS Journal

Volumn 280, Issue 19, 2013, Pages 4853-4864

  Kmetzsch, Livia ^a   Staats, Charley C ^a   Cupertino, Julia B ^a   Fonseca, Fernanda L ^b   Rodrigues, Marcio L ^b,c   Schrank, Augusto ^a   Vainstein, Marilene H ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

calcium transport; cryptococcosis; Cryptococcus neoformans; vacuolar calcium storage; virulence

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); ADENOSINE TRIPHOSPHATASE (CALCIUM) PMC1; CALCIUM ION; GLUCURONOXYLOMANNAN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TOLERANCE; CALCIUM TRANSPORT; COMPUTER MODEL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CRYPTOCOCCAL MENINGITIS; CRYPTOCOCCUS NEOFORMANS; DISEASE ASSOCIATION; FEMALE; FUNGAL CAPSULE; FUNGAL COLONIZATION; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS GROWTH; GENE; GENE INACTIVATION; IN VITRO STUDY; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGEN LOAD; PATHOGENESIS; PHENOTYPE; PHYLOGENETIC TREE; PHYSICAL TOLERANCE; PMC1 GENE; PRIORITY JOURNAL; PROTEIN FUNCTION; PULMONARY CRYPTOCOCCOSIS; SENSITIVITY ANALYSIS; SEQUENCE HOMOLOGY; VCX1 GENE;

CALCIUM TRANSPORT; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; VACUOLAR CALCIUM STORAGE; VIRULENCE;

ANIMALS; CALCIUM; CALCIUM-TRANSPORTING ATPASES; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; FUNGAL PROTEINS; MICE; PHYLOGENY; VACUOLES; VIRULENCE;

FILOBASIDIELLA NEOFORMANS; MURINAE; MUS;

EID: 84884597229     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12458     Document Type: Article

References (38)

1. Berridge MJ, Lipp P, &, Bootman MD, (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1, 11-21.
2. Kraus PR, &, Heitman J, (2003) Coping with stress: calmodulin and calcineurin in model and pathogenic fungi. Biochem Biophys Res Commun 311, 1151-1157.
3. Yoshimoto H, Saltsman K, Gasch AP, Li HX, Ogawa N, Botstein D, Brown PO, &, Cyert MS, (2002) Genome-wide analysis of gene expression regulated by the calcineurin/Crz1p signaling pathway in Saccharomyces cerevisiae. J Biol Chem 277, 31079-31088.
4. Stathopoulos-Gerontides A, Guo JJ, &, Cyert MS, (1999) Yeast calcineurin regulates nuclear localization of the Crz1p transcription factor through dephosphorylation. Genes Dev 13, 798-803.
5. Reedy JL, Filler SG, &, Heitman J, (2010) Elucidating the Candida albicans calcineurin signaling cascade controlling stress response and virulence. Fungal Genet Biol 47, 107-116.
6. Steinbach WJ, Cramer RA Jr, Perfect BZ, Asfaw YG, Sauer TC, Najvar LK, Kirkpatrick WR, Patterson TF, Benjamin DK Jr, Heitman J, et al,. (2006) Calcineurin controls growth, morphology, and pathogenicity in Aspergillus fumigatus. Eukaryot Cell 5, 1091-1103.
7. Odom A, Muir S, Lim E, Toffaletti DL, Perfect J, &, Heitman J, (1997) Calcineurin is required for virulence of Cryptococcus neoformans. EMBO J 16, 2576-2589.
8. Chen YL, Lehman VN, Lewit Y, Averette AF, &, Heitman J, (2013) Calcineurin governs thermotolerance and virulence of Cryptococcus gattii. G3 (Bethesda) 3, 52, 7-539.
9. Kozubowski L, Lee SC, &, Heitman J, (2009) Signalling pathways in the pathogenesis of Cryptococcus. Cell Microbiol 11, 370-380.
10. Kozubowski L, Aboobakar EF, Cardenas ME, &, Heitman J, (2011) Calcineurin colocalizes with P-bodies and stress granules during thermal stress in Cryptococcus neoformans. Eukaryot Cell 10, 1396-1402.
11. Kraus PR, Fox DS, Cox GM, &, Heitman J, (2003) The Cryptococcus neoformans MAP kinase Mpk1 regulates cell integrity in response to antifungal drugs and loss of calcineurin function. Mol Microbiol 48, 1377-1387.
12. Fox DS, Cruz MC, Sia RA, Ke H, Cox GM, Cardenas ME, &, Heitman J, (2001) Calcineurin regulatory subunit is essential for virulence and mediates interactions with FKBP12-FK506 in Cryptococcus neoformans. Mol Microbiol 39, 835-849.
13. Cruz MC, Fox DS, &, Heitman J, (2001) Calcineurin is required for hyphal elongation during mating and haploid fruiting in Cryptococcus neoformans. EMBO J 20, 1020-1032.
14. Lev S, Desmarini D, Chayakulkeeree M, Sorrell TC, &, Djordjevic JT, (2012) The Crz1/Sp1 transcription factor of Cryptococcus neoformans is activated by calcineurin and regulates cell wall integrity. PLoS ONE 7, e51403.
15. Kraus PR, Nichols CB, &, Heitman J, (2005) Calcium- and calcineurin-independent roles for calmodulin in Cryptococcus neoformans morphogenesis and high-temperature growth. Eukaryot Cell 4, 1079-1087.
16. Liu M, Du P, Heinrich G, Cox GM, &, Gelli A, (2006) Cch1 mediates calcium entry in Cryptococcus neoformans and is essential in low-calcium environments. Eukaryot Cell 5, 1788-1796.
17. 2+ATPase, is involved in stress tolerance and virulence in Cryptococcus neoformans. Infect Immun 75, 3394-3405.
18. 2+ tolerance and virulence in Cryptococcus neoformans. Eukaryot Cell 9, 1798-1805.
19. 2+ uptake. Cell Calcium 50, 139-146.
20. 2+ ATPases. J Cell Biol 124, 351-363.
21. Ma H, &, May RC, (2009) Virulence in Cryptococcus species. Adv Appl Microbiol 67, 131-190.
22. 2+-ATPases that contribute to cadmium tolerance in yeast. Toxicol Lett 207, 104-111.
23. O'Meara TR, &, Alspaugh JA, (2012) The Cryptococcus neoformans capsule: a sword and a shield. Clin Microbiol Rev 25, 387-408.
24. Chun CD, &, Madhani HD, (2010) Ctr2 links copper homeostasis to polysaccharide capsule formation and phagocytosis inhibition in the human fungal pathogen Cryptococcus neoformans. PLoS ONE 5, e12503.
25. Kmetzsch L, Joffe LS, Staats CC, de Oliveira DL, Fonseca FL, Cordero RJ, Casadevall A, Nimrichter L, Schrank A, Vainstein MH, et al,. (2011) Role for Golgi reassembly and stacking protein (GRASP) in polysaccharide secretion and fungal virulence. Mol Microbiol 81, 206-218.
26. 2+ ATPases in Saccharomyces cerevisiae. Mol Cell Biol 16, 2226-2237.
27. Griffiths EJ, Kretschmer M, &, Kronstad JW, (2012) Aimless mutants of Cryptococcus neoformans: failure to disseminate. Fungal Biol Rev 26, 61-72.
28. Dinamarco TM, Freitas FZ, Almeida RS, Brown NA, dos Reis TF, Ramalho LN, Savoldi M, Goldman MH, Bertolini MC, &, Goldman GH, (2012) Functional characterization of an Aspergillus fumigatus calcium transporter (PmcA) that is essential for fungal infection. PLoS ONE 7, e37591.
29. Nguyen QB, Kadotani N, Kasahara S, Tosa Y, Mayama S, &, Nakayashiki H, (2008) Systematic functional analysis of calcium-signalling proteins in the genome of the rice-blast fungus, Magnaporthe oryzae, using a high-throughput RNA-silencing system. Mol Microbiol 68, 1348-1365.
30. Fraser JA, Subaran RL, Nichols CB, &, Heitman J, (2003) Recapitulation of the sexual cycle of the primary fungal pathogen Cryptococcus neoformans var. gattii: implications for an outbreak on Vancouver Island Canada. Eukaryot Cell 2, 1036-1045.
31. Idnurm A, Reedy JL, Nussbaum JC, &, Heitman J, (2004) Cryptococcus neoformans virulence gene discovery through insertional mutagenesis. Eukaryot Cell 3, 420-429.
32. Schneider Rde O, Fogaca Nde S, Kmetzsch L, Schrank A, Vainstein MH, &, Staats CC, (2012) Zap1 regulates zinc homeostasis and modulates virulence in Cryptococcus gattii. PLoS ONE 7, e43773.
33. Toffaletti DL, Rude TH, Johnston SA, Durack DT, &, Perfect JR, (1993) Gene transfer in Cryptococcus neoformans by use of biolistic delivery of DNA. J Bacteriol 175, 1405-1411.
34. Baker LG, Specht CA, Donlin MJ, &, Lodge JK, (2007) Chitosan, the deacetylated form of chitin, is necessary for cell wall integrity in Cryptococcus neoformans. Eukaryot Cell 6, 855-867.
35. Casadevall A, Mukherjee J, &, Scharff MD, (1992) Monoclonal antibody based ELISAs for cryptococcal polysaccharide. J Immunol Methods 154, 27-35.
36. Casadevall A, Cleare W, Feldmesser M, Glatman-Freedman A, Goldman DL, Kozel TR, Lendvai N, Mukherjee J, Pirofski LA, Rivera J, 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.
37. Fonseca FL, Nimrichter L, Cordero RJ, Frases S, Rodrigues J, Goldman DL, Andruszkiewicz R, Milewski S, Travassos LR, Casadevall A, et al,. (2009) Role for chitin and chitooligomers in the capsular architecture of Cryptococcus neoformans. Eukaryot Cell 8, 1543-1553.
38. Livak KJ, &, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25, 402-408.