Genome-wide association analysis of clinical vs. nonclinical origin provides insights into Saccharomyces cerevisiae pathogenesis

Molecular Ecology

Volumn 20, Issue 19, 2011, Pages 4085-4097

  Muller, L A H ^a,c   Lucas, J E ^b   Georgianna, D R ^a   McCusker, J H ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b DUKE UNIVERSITY   (United States)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

clinical origin; environmental association; genome wide association analysis; pathogenesis; Saccharomyces cerevisiae; tiling array

Indexed keywords

ARTICLE; COMPARATIVE STUDY; FUNGAL GENOME; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENETICS; GENOTYPE; ISOLATION AND PURIFICATION; PATHOGENICITY; SACCHAROMYCES CEREVISIAE;

GENETIC VARIATION; GENOME, FUNGAL; GENOTYPE; POLYMORPHISM, GENETIC; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

EID: 80053267267     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2011.05225.x     Document Type: Article

References (67)

1. Bassetti S, Frei R, Zimmerli W, (1998) Fungemia with Saccharomyces cerevisiae after treatment with Saccharomyces boulardii. American Journal of Medicine, 105, 71-72. (Pubitemid 28346111)
2. Bengtsson H, Simpson K, Bullard J, Hansen K, (2008) Aroma.affymetrix: A Generic Gramework in R for Analyzing Small to Very Large Affymetrix Data Sets in Bounded Memory. Technical Report #745, Department of Statistics, University of California, Berkeley, USA.
3. Bolstad BM, Irizarry RA, Astrand M, Speed TP, (2003) A comparison of normalization methods for high density oligonucleotide array data based on bias and variance. Bioinformatics, 19, 185-193. (Pubitemid 36181903)
4. Borth N, Walther A, Reijnst P, Jorde S, Schaub Y, Wendland J, (2010) Candida albicans Vrp1 is required for polarized morphogenesis and interacts with Wal1 and Myo5. Microbiology, 156, 2962-2969.
5. Clemons KV, McCusker JH, Davis RW, Stevens DA, (1994) Comparative pathogenesis of clinical and nonclinical isolates of Saccharomyces cerevisiae. Journal of Infectious Diseases, 169, 859-867. (Pubitemid 24102121)
6. Coluccio A, Bogengruber E, Conrad MN, Dresser ME, Briza P, Neiman AM, (2004) Morphogenetic pathway of spore wall assembly in Saccharomyces cerevisiae. Eukaryotic Cell, 3, 1464-1475. (Pubitemid 40025105)
7. Coop G, Witonsky D, Di Rienzo A, Pritchard JK, (2010) Using environmental correlations to identify loci underlying local adaptation. Genetics, 185, 1411-1423.
8. Enache-Angoulvant A, Hennequin C, (2005) Invasive Saccharomyces infection: a comprehensive review. Clinical Infectious Diseases, 41, 1559-1568. (Pubitemid 41691593)
9. Ernst R, Klemm R, Schmitt L, Kuchler K, (2005) Yeast ATP-binding cassette transporters: cellular cleaning pumps. Methods in Enzymology, 400, 460-484. (Pubitemid 43052435)
10. Excoffier L, Lischer HEL, (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564-567.
11. Excoffier L, Smouse PE, Quattro JM, (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131, 479-491.
12. Falush D, Stephens M, Pritchard JK, (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics, 164, 1567-1587. (Pubitemid 37102217)
13. Fraley C, Raftery AE, (2002) Model-based clustering, discriminant analysis and density estimation. Journal of the American Statistical Association, 97, 611-631.
14. Fraley C, Raftery AE, (2006) MCLUST version 3 for R: Normal Mixture Modelling and Model-based Clustering. Technical Report #504, Department of Statistics, University of Washington, Seattle, USA.
15. Gancedo JM, (2001) Control of pseudohyphae formation in Saccharomyces cerevisiae. FEMS Microbiology Reviews, 25, 107-123. (Pubitemid 32057198)
16. Goffeau A, Barrell BG, Bussey H, et al. (1996) Life with 6000 genes. Science, 274, 546.
17. Gognies S, Barka EA, Gainvors-Claisse A, Belarbi A, (2006) Interactions between yeasts and grapevines: filamentous growth, endopolygalacturonase and phytopathogenicity of colonizing yeasts. Microbial Ecology, 51, 109-116. (Pubitemid 43213967)
18. Gresham D, Ruderfer DM, Pratt SC, et al. (2006) Genome-wide detection of polymorphisms at nucleotide resolution with a single DNA microarray. Science, 311, 1932-1936.
19. Guslandi M, (2006) Are probiotics effective for treating Clostridium difficile disease and antibiotic-associated diarrhea? Nature Clinical Practice Gastroenterology and Hepatology, 3, 606-607. (Pubitemid 44644765)
20. Hennequin C, Kauffmann-Lacroix C, Jobert A, et al. (2000) Possible role of catheters in Saccharomyces boulardii fungemia. European Journal of Clinical Microbiology & Infectious Diseases, 19, 16-20. (Pubitemid 30093376)
21. de Hoog GS, (1996) Risk assessment of fungi reported from humans and animals. Mycoses, 39, 407-417. (Pubitemid 27166190)
22. Hoyer LL, Green CB, Oh SH, Zhao X, (2008) Discovering the secrets of the Candida albicans agglutinin-like sequence (ALS) gene family-a sticky pursuit. Medical Mycology, 46, 1-15. (Pubitemid 351298235)
23. Hube B, Naglik J, (2002) Extracellular hydrolases. In: Candida and Candidiasi (ed., Calderone RA,). pp. 107-122, ASM Press, Washington, DC.
24. Hubisz MJ, Falush D, Stephens M, Pritchard JK, (2009) Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources, 9, 1322-1332.
25. Imazu H, Sakurai H, (2005) Saccharomyces cerevisiae heat shock transcription factor regulates cell wall remodeling in response to heat shock. Eukaryotic Cell, 4, 1050-1056. (Pubitemid 40817464)
26. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP, (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Research, 31, e15.
27. Jin R, Dobry CJ, McCown PJ, Kumar A, (2008) Large-scale analysis of yeast filamentous growth by systematic gene disruption and overexpression. Molecular Biology of the Cell, 19, 284-296. (Pubitemid 351186153)
28. Kang HM, Zaitlen NA, Wade CM, et al. (2008) Efficient control of population structure in model organism association mapping. Genetics, 178, 1709-1723.
29. Kang HM, Sul JH, Service SK, et al. (2010) Variance component model to account for sample structure in genome-wide association studies. Nature Genetics, 42, 348-354.
30. Klingberg TD, Lesnik U, Arneborg N, Raspor P, Jespersen L, (2008) Comparison of Saccharomyces cerevisiae strains of clinical and nonclinical origin by molecular typing and determination of putative virulence traits. FEMS Yeast Research, 8, 631-640. (Pubitemid 351678647)
31. Kwon-Chung K, Bennett JE, (1992) Saccharomyces Meyen Ex Reess. In: Medical Mycolog (eds, Kwon-Chung JJ, Bennet JE,). pp. 772-773, Lea and Febiger, Philadelphia, PA.
32. Liti G, Carter DM, Moses AM, et al. (2009) Population genomics of domestic and wild yeasts. Nature, 458, 337-341.
33. de Llanos R, Querol A, Planes AM, Fernandez-Espinar MT, (2004) Molecular characterization of clinical Saccharomyces cerevisiae isolates and their association with non-clinical strains. Systematic and Applied Microbiology, 27, 427-435. (Pubitemid 39071017)
34. de Llanos R, Querol A, Peman J, Gobernado M, Fernandez-Espinar MT, (2006a) Food and probiotic strains from the Saccharomyces cerevisiae species as a possible origin of human systemic infections. International Journal of Food Microbiology, 110, 286-290. (Pubitemid 44108263)
35. de Llanos R, Fernández-Espinar MT, Querol A, (2006b) A comparison of clinical and food Saccharomyces cerevisiae isolates on the basis of potential virulence factors. Antonie van Leeuwenhoek, 90, 221-231. (Pubitemid 44314600)
36. Madhani HD, Galitski T, Lander ES, Fink GR, (1999) Effectors of a developmental mitogen-activated protein kinase cascade revealed by expression signatures of signaling mutants. Proceedings of the National Academy of Sciences, USA, 96, 12530-12535. (Pubitemid 29513536)
37. Malgoire JY, Bertout S, Renaud F, Bastide JM, Mallie M, (2005) Typing of Saccharomyces cerevisiae clinical strains by using microsatellite sequence polymorphism. Journal of Clinical Microbiology, 43, 1133-1137. (Pubitemid 40364928)
38. McCusker JH, Clemons KV, Stevens DA, Davis RW, (1994) Saccharomyces cerevisiae virulence phenotype as determined with CD-1 mice is associated with the ability to grow at 42 degrees C and form pseudohyphae. Infection and Immunity, 62, 5447-5455. (Pubitemid 24364986)
39. Mortimer RK, Johnston JR, (1986) Genealogy of principal strains of the yeast genetic stock center. Genetics, 113, 35-43. (Pubitemid 16042668)
40. Muller LAH, McCusker JH, (2009) Microsatellite analysis of genetic diversity among clinical and nonclinical Saccharomyces cerevisiae isolates suggests heterozygote advantage in clinical environments. Molecular Ecology, 18, 2779-2786.
41. Muñoz P, Bouza E, Cuenca-Estrella M, et al. (2005) Saccharomyces cerevisiae fungemia: an emerging infectious disease. Clinical Infectious Diseases, 40, 1625-1634. (Pubitemid 40720813)
42. Nelson B, Kurischko C, Horecka J, et al. (2003) RAM: a conserved signaling network that regulates Ace2p transcriptional activity and polarized morphogenesis. Molecular Biology of the Cell, 14, 3782-3803. (Pubitemid 37151626)
43. Nicholls S, MacCallum DM, Kaffarnik FA, Selway L, Peck SC, Brown AJ, (2011) Activation of the heat shock transcription factor Hsf1 is essential for the full virulence of the fungal pathogen Candida albicans. Fungal Genetics and Biology, 48, 297-305.
44. Noble SM, French S, Kohn LA, Chen V, Johnson AD, (2010) Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity. Nature Genetics, 42, 590-598.
45. Pardini G, De Groot PW, Coste AT, et al. (2006) The CRH family coding for cell wall glycosylphosphatidylinositol proteins with a predicted transglycosidase domain affects cell wall organization and virulence of Candida albicans. Journal of Biological Chemistry, 281, 40399-40411. (Pubitemid 46041843)
46. Phan QT, Myers CL, Fu Y, et al. (2007) Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biology, 5, e64.
47. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959. (Pubitemid 30397141)
48. Purcell S, Neale B, Todd-Brown K, et al. (2007) PLINK: a toolset for whole-genome association and population-based linkage analysis. American Journal of Human Genetics, 81, 559-575. (Pubitemid 47330214)
49. R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0.
50. Reignault P, Valette-Collet O, Boccara M, (2008) The importance of fungal pectinolytic enzymes in plant invasion, host adaptability and symptom type. European Journal of Plant Pathology, 120, 1-11. (Pubitemid 350165654)
51. Rodriguez-Peña JM, Rodriguez C, Alvarez A, Nombela C, Arroyo J, (2002) Mechanisms for targeting of the Saccharomyces cerevisiae GPI-anchored cell wall protein Crh2p to polarised growth sites. Journal of Cell Science, 115, 2549-2558. (Pubitemid 34778072)
52. Salonen JH, Richardson MD, Gallacher K, et al. (2000) Fungal colonization of haematological patients receiving cytotoxic chemotherapy: emergence of azole-resistant Saccharomyces cerevisiae. Journal of Hospital Infection, 45, 293-301. (Pubitemid 30645074)
53. Santos B, Snyder M, (2000) Sbe2p and sbe22p, two homologous Golgi proteins involved in yeast cell wall formation. Molecular Biology of the Cell, 11, 435-452. (Pubitemid 30112156)
54. Schacherer J, Shapiro JA, Ruderfer DM, Kruglyak L, (2009) Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature, 458, 342-345.
55. Sherman F, (1991) Getting started with yeast. In: Methods in Enzymolog (eds, Guthrie C, Fink GR,). pp. 3-21, Academic Press, New York, NY.
56. Shin JH, Blay S, McNeney B, Graham J, (2006) LDheatmap: an R function for graphical display of pairwise linkage disequilibria between single nucleotide polymorphisms. Journal of Statistical Software, 16, Code Snippet 3.
57. Sinha H, David L, Pascon RC, et al. (2008) Sequential elimination of major-effect contributors identifies additional quantitative trait loci conditioning high-temperature growth in yeast. Genetics, 180, 1661-1670.
58. Smith D, Metzgar D, Wills C, Fierer J, (2002) Fatal Saccharomyces cerevisiae aortic graft infection. Journal of Clinical Microbiology, 40, 2691-2692. (Pubitemid 34747394)
59. Sundstrom P, (2006) Candida albicans hypha formation and virulence. In: Molecular Principles of Fungal Pathogenesi (eds, Heitman J, Filler SG, Edwards JE, Mitchell AP,). pp. 45-47, ASM Press, Washington, DC.
60. Tarassov K, Messier V, Landry CR, et al. (2008) An in vivo map of the yeast protein interactome. Science, 320, 1465-1470. (Pubitemid 351929421)
61. Vink E, Vossen JH, Ram AF, et al. (2002) The protein kinase Kic1 affects 1,6-beta-glucan levels in the cell wall of Saccharomyces cerevisiae. Microbiology, 148, 4035-4048. (Pubitemid 36097465)
62. Voorman A, Lumley T, McKnight B, Rice K, (2011) Behavior of QQ-plots and genomic control in studies of gene-environment interaction. PLoS ONE, 6, e19416.
63. Wei W, McCusker JH, Hyman RW, et al. (2007) Genome sequencing and comparative analysis of Saccharomyces cerevisiae strain YJM789. Proceedings of the National Academy of Sciences, USA, 104, 12825-12830. (Pubitemid 47255239)
64. Wheeler RT, Kupiec M, Magnelli P, Abeijon C, Fink GR, (2003) A Saccharomyces cerevisiae mutant with increased virulence. Proceedings of the National Academy of Sciences of the United States of America, 100, 2766-2770. (Pubitemid 36297573)
65. Wong Sak Hoi J, Dumas B, (2010) Ste12 and Ste12-like proteins, fungal transcription factors regulating development and pathogenicity. Eukaryotic Cell, 9, 480-485.
66. Wu X, Jiang YW, (2005) Genetic/genomic evidence for a key role of polarized endocytosis in filamentous differentiation of S. cerevisiae. Yeast, 22, 1143-1153. (Pubitemid 41684145)
67. Yamamoto A, Mizukami Y, Sakurai H, (2005) Identification of a novel class of target genes and a novel type of binding sequence of heat shock transcription factor in Saccharomyces cerevisiae. Journal of Biological Chemistry, 280, 11911-11919. (Pubitemid 40418506)