Aspergillus Collagen-like genes (acl): Identification, sequence polymorphism, and assessment for PCR-based pathogen detection

Applied and Environmental Microbiology

Volumn 79, Issue 24, 2013, Pages 7882-7895

  Tuntevski, Kiril ^a   Durney, Brandon C ^a   Snyder, Anna K ^a   Rocco LaSala, P ^a   Nayak, Ajay P ^b   Green, Brett J ^b   Beezhold, Donald H ^b   Rio, Rita V M ^a   Holland, Lisa A ^a   Lukomski, Slawomir ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

^b NATIONAL INSTITUTE FOR OCCUPATIONAL SAFETY AND HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPERGILLUS FUMIGATUS; ASPERGILLUS GENERA; GENETIC POLYMORPHISMS; INVASIVE ASPERGILLOSIS; MICRO FLUIDIC APPLICATIONS; MORPHOLOGICAL CHARACTERIZATION; PHYLOGENETIC ANALYSIS; SENSITIVITY AND SPECIFICITY;

ASSAYS; CAPILLARY ELECTROPHORESIS; COLLAGEN; CONSERVATION; GENES; PUBLIC HEALTH;

ASPERGILLUS;

BIOASSAY; COLLAGEN; GENE EXPRESSION; INFECTIOUS DISEASE; MICROBIAL ACTIVITY; PATHOGEN; POLYMERASE CHAIN REACTION; POLYMORPHISM; PUBLIC HEALTH; SAMPLING;

COLLAGEN; FUNGAL DNA; FUNGAL PROTEIN;

ARTICLE; ASPERGILLOSIS; ASPERGILLUS; CHEMISTRY; CLUSTER ANALYSIS; DNA SEQUENCE; GENETIC POLYMORPHISM; GENETICS; HUMAN; ISOLATION AND PURIFICATION; LUNG LAVAGE; METHODOLOGY; MICROBIOLOGY; MOLECULAR DIAGNOSIS; MOLECULAR GENETICS; MYCOLOGY; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION; SPUTUM; VALIDATION STUDY;

ASPERGILLOSIS; ASPERGILLUS; BRONCHOALVEOLAR LAVAGE FLUID; CLUSTER ANALYSIS; COLLAGEN; DNA, FUNGAL; FUNGAL PROTEINS; HUMANS; MOLECULAR DIAGNOSTIC TECHNIQUES; MOLECULAR SEQUENCE DATA; MYCOLOGY; PHYLOGENY; POLYMERASE CHAIN REACTION; POLYMORPHISM, GENETIC; SEQUENCE ANALYSIS, DNA; SPUTUM;

EID: 84888232280     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02835-13     Document Type: Article

References (80)

1. Eduard W. 2009. Fungal spores: a critical review of the toxicological and epidemiological evidence as a basis for occupational exposure limit setting. Crit. Rev. Toxicol. 39:799-864.
2. Machida M, Yamada O, Gomi K. 2008. Genomics of Aspergillus oryzae: learning from the history of Koji mold and exploration of its future. DNA Res. 15:173-183.
3. Jahromi MF, Liang JB, Ho YW, Mohamad R, Goh YM, Shokryazdan P. 2012. Lovastatin production by Aspergillus terreus using agro-biomass as substrate in solid state fermentation. J. Biomed. Biotechnol. 2012:196264.
4. Yu J, Chang PK, Cary JW, Wright M, Bhatnagar D, Cleveland TE, Payne GA, Linz JE. 1995. Comparative mapping of aflatoxin pathway gene clusters in Aspergillus parasiticus and Aspergillus flavus. Appl. Environ. Microbiol. 61:2365-2371.
5. Zmeili OS, Soubani AO. 2007. Pulmonary aspergillosis: a clinical update. QJM 100:317-334.
6. Latgé JP. 1999. Aspergillus fumigatus and aspergillosis. Clin. Microbiol. Rev. 12:310-350.
7. Groll AH, Kurz M, Schneider W, Witt V, Schmidt H, Schneider M, Schwabe D. 1999. Five-year-survey of invasive aspergillosis in a paediatric cancer centre. Epidemiology, management and long-term survival. Mycoses 42:431-442.
8. Dimopoulos G, Frantzeskaki F, Poulakou G, Armaganidis A. 2012. Invasive aspergillosis in the intensive care unit. Ann. N. Y. Acad. Sci. 1272:31-39.
9. Hsieh KH, Shen JJ. 1988. Prevalence of childhood asthma in Taipei, Taiwan, and other Asian Pacific countries. J. Asthma 25:73-82.
10. Chaudhary N, Marr KA. 2011. Impact of Aspergillus fumigatus in allergic airway diseases. Clin. Transl. Allergy 1:4. doi:10.1186/2045-7022-1-4.
11. Patterson K, Strek ME. 2010. Allergic bronchopulmonary aspergillosis. Proc. Am. Thorac. Soc. 7:237-244.
12. Simon-Nobbe B, Denk U, Poll V, Rid R, Breitenbach M. 2008. The spectrum of fungal allergy. Int. Arch. Allergy Immunol. 145:58-86.
13. Tong KB, Lau CJ, Murtagh K, Layton AJ, Seifeldin R. 2009. The economic impact of aspergillosis: analysis of hospital expenditures across patient subgroups. Int. J. Infect. Dis. 13:24-36.
14. Pingleton WW, Hiller FC, Bone RC, Kerby GR, Ruth WE. 1977. Treatment of allergic aspergillosis with triamcinolone acetonide aerosol. Chest 71:782-784.
15. FDA. 2013. Multistate outbreak of fungal meningitis and other infections. U.S. Food and Drug Administration, Silver Spring, MD. http://www.fda.gov/Drugs/DrugSafety/FungalMeningitis/default.htm.
16. Denning DW. 2000. Aspergillus species, p 2306-2310. In Mandell GL, Bennett JE, Dolin R (ed), Principles and practices of infectious diseases, part III-infectious diseases and their etiologic agents. Churchill Livingstone, Philadelphia, PA.
17. Hachem RY, Kontoyiannis DP, Chemaly RF, Jiang Y, Reitzel R, Raad I. 2009. Utility of galactomannan enzyme immunoassay and (1,3) β-Dglucan in diagnosis of invasive fungal infections: low sensitivity for Aspergillus fumigatus infection in hematologic malignancy patients. J. Clin. Microbiol. 47:129-133.
18. Kourkoumpetis TK, Fuchs BB, Coleman JJ, Desalermos A, Mylonakis E. 2012. Polymerase chain reaction-based assays for the diagnosis of invasive fungal infections. Clin. Infect. Dis. 54:1322-1331.
19. Hope WW, Walsh TJ, Denning DW. 2005. Laboratory diagnosis of invasive aspergillosis. Lancet Infect. Dis. 5:609-622.
20. Loeffler J, Barnes R, Donnelly JP. 2012. Standardization of Aspergillus PCR diagnosis. Bone Marrow Transplant. 47:299-300.
21. White PL, Bretagne S, Klingspor L, Melchers WJ, McCulloch E, Schulz B, Finnstrom N, Mengoli C, Barnes RA, Donnelly JP, Loeffler J. 2010. Aspergillus PCR: one step closer to standardization. J. Clin. Microbiol. 48:1231-1240.
22. Leski TA, Caswell CC, Pawlowski M, Klinke DJ, Bujnicki JM, Hart SJ, Lukomski S. 2009. Identification and classification of bcl genes and proteins of Bacillus cereus group organisms and their application in Bacillus anthracis detection and fingerprinting. Appl. Environ. Microbiol. 75: 7163-7172.
23. Castanha ER, Swiger RR, Senior B, Fox A, Waller LN, Fox KF. 2006. Strain discrimination among B. anthracis and related organisms by characterization of bclA polymorphisms using PCR coupled with agarose gel or microchannel fluidics electrophoresis. J. Microbiol. Methods 64:27-45.
24. Sylvestre P, Couture-Tosi E, Mock M. 2002. A collagen-like surface glycoprotein is a structural component of the Bacillus anthracis exosporium. Mol. Microbiol. 45:169-178.
25. Bateman A, Birney E, Durbin R, Eddy SR, Howe KL, Sonnhammer EL. 2000. The Pfam protein families database. Nucleic Acids Res. 28:263-266.
26. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
27. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8:785-786.
28. Eisenhaber B, Bork P, Eisenhaber F. 1999. Prediction of potential GPImodification sites in proprotein sequences. J. Mol. Biol. 292:741-758.
29. Edgar RC. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113. doi:10.1186/1471-2105-5-113.
30. Swofford DL. 2002. PAUP 4.0-phylogenetic analysis using parsimony, version 4. Sinauer Associates, Sunderland, MA.
31. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:539-542.
32. Felsenstein J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17:368-376.
33. Nylander JAA. 2004. MrModeltest v2. Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.
34. Chow TY-K, Käfer E. 1993. A rapid method for isolation of total nucleic acids from Aspergillus nidulans. Fungal Genet. Newslett. 40:25-27.
35. Archer-Hartmann SA, Sargent LM, Lowry DT, Holland LA. 2011. Microscale exoglycosidase processing and lectin capture of glycans with phospholipid assisted capillary electrophoresis separations. Anal. Chem. 83:2740-2747.
36. Durney BC, Lounsbury JA, Poe BL, Landers JP, Holland LA. 2013. A thermally responsive phospholipid pseudogel: tunable DNA sieving with capillary electrophoresis. Anal. Chem. 85:6617-6625.
37. White CM, Luo R, Archer-Hartmann SA, Holland LA. 2007. Electrophoretic screening of ligands under suppressed EOF with an inert phospholipid coating. Electrophoresis 28:3049-3055.
38. Luo R, Archer-Hartmann SA, Holland LA. 2010. Transformable capillary electrophoresis for oligosaccharide separations using phospholipid additives. Anal. Chem. 82:1228-1233.
39. Henry T, Iwen PC, Hinrichs SH. 2000. Identification of Aspergillus species using internal transcribed spacer regions 1 and 2. J. Clin. Microbiol. 38:1510-1515.
40. White TB, Lee TJS, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Academic Press, Inc., New York, NY.
41. Kurtzman CP, Robnett CJ. 1997. Identification of clinically important ascomycetous yeasts based on nucleotide divergence in the 5' end of the large-subunit (26S) ribosomal DNA gene. J. Clin. Microbiol. 35:1216-1223.
42. Hogaboam CM, Carpenter KJ, Schuh JM, Buckland KF. 2005. Aspergillus and asthma-any link? Med. Mycol. 43(Suppl 1):S197-S1202.
43. Torres HA, Rivero GA, Lewis RE, Hachem R, Raad II, Kontoyiannis DP. 2003. Aspergillosis caused by non-fumigatus Aspergillus species: risk factors and in vitro susceptibility compared with Aspergillus fumigatus. Diagn. Microbiol. Infect. Dis. 46:25-28.
44. Berisio R, Vitagliano L, Mazzarella L, Zagari A. 2002. Crystal structure of the collagen triple helix model [(Pro-Pro-Gly)10]3. Protein Sci. 11:262-270.
45. Hulmes DJ. 1992. The collagen superfamily-diverse structures and assemblies. Essays Biochem. 27:49-67.
46. Engel J. 1997. Versatile collagens in invertebrates. Science 277:1785-1786.
47. Rasmussen M, Jacobsson M, Bjorck L. 2003. Genome-based identification and analysis of collagen-related structural motifs in bacterial and viral proteins. J. Biol. Chem. 278:32313-32316.
48. Munk R, Ghosh P, Ghosh MC, Saito T, Xu M, Carter A, Indig F, Taub DD, Longo DL. 2011. Involvement of mTOR in CXCL12 mediated T cell signaling and migration. PLoS One 6:e24667. doi:10.1371/journal.pone.0024667.
49. Celerin M, Ray JM, Schisler NJ, Day AW, Stetler-Stevenson WG, Laudenbach DE. 1996. Fungal fimbriae are composed of collagen. EMBO J. 15:4445-4453.
50. Celerin M, Day AW, Smith RJ, Laudenbach DE. 1997. Immunolocalization of fimbrial epitopes in thin sections of Microbotryum violaceum. Can. J. Microbiol. 43:136-142.
51. Wang C, St Leger RJ. 2006. A collagenous protective coat enables Metarhizium anisopliae to evade insect immune responses. Proc. Natl. Acad. Sci. U.S.A. 103:6647-6652.
52. Håkansson K, Reid KB. 2000. Collectin structure: a review. Protein Sci. 9:1607-1617.
53. van de Wetering JK, van Golde LM, Batenburg JJ. 2004. Collectins: players of the innate immune system. Eur. J. Biochem. 271:1229-1249.
54. Kilchherr E, Hofmann H, Steigemann W, Engel J. 1985. Structural model of the collagen-like region of C1q comprising the kink region and the fibre-like packing of the six triple helices. J. Mol. Biol. 186:403-415.
55. Haagsman HP. 1994. Surfactant proteins A and D. Biochem. Soc. Trans. 22:100-106.
56. Persikov AV, Ramshaw JA, Kirkpatrick A, Brodsky B. 2003. Triple-helix propensity of hydroxyproline and fluoroproline: comparison of hostguest and repeating tripeptide collagen models. J. Am. Chem. Soc. 125: 11500-11501.
57. Vitagliano L, Berisio R, Mazzarella L, Zagari A. 2001. Structural bases of collagen stabilization induced by proline hydroxylation. Biopolymers 58: 459-464.
58. Holmgren SK, Taylor KM, Bretscher LE, Raines RT. 1998. Code for collagen's stability deciphered. Nature 392:666-667.
59. Levdansky E, Romano J, Shadkchan Y, Sharon H, Verstrepen KJ, Fink GR, Osherov N. 2007. Coding tandem repeats generate diversity in Aspergillus fumigatus genes. Eukaryot. Cell 6:1380-1391.
60. Sabino R, Sampaio P, Rosado L, Stevens DA, Clemons KV, Pais C. 2010. New polymorphic microsatellite markers able to distinguish among Candida parapsilosis sensu stricto isolates. J. Clin. Microbiol. 48:1677-1682.
61. Torelli R, Sanguinetti M, Moody A, Pagano L, Caira M, De Carolis E, Fuso L, De Pascale G, Bello G, Antonelli M, Fadda G, Posteraro B. 2011. Diagnosis of invasive aspergillosis by a commercial real-time PCR assay for Aspergillus DNA in bronchoalveolar lavage fluid samples from highrisk patients compared to a galactomannan enzyme immunoassay. J. Clin. Microbiol. 49:4273-4278.
62. Lass-Flörl C, Follett SA, Moody A, Denning DW. 2011. Detection of Aspergillus in lung and other tissue samples using the MycAssay Aspergillus real-time PCR kit. Can. J. Microbiol. 57:765-768.
63. Arendrup MC, Jensen RH, Grif K, Skov M, Pressler T, Johansen HK, Lass-Florl C. 2012. In vivo emergence of Aspergillus terreus with reduced azole susceptibility and a Cyp51a M217I alteration. J. Infect. Dis. 206:981-985.
64. Blum G, Hortnagl C, Jukic E, Erbeznik T, Pumpel T, Dietrich H, Nagl M, Speth C, Rambach G, Lass-Florl C. 2013. New insight into amphotericin B resistance in Aspergillus terreus. Antimicrob. Agents Chemother. 57:1583-1588.
65. Georgiadou SP, Kontoyiannis DP. 2012. The impact of azole resistance on aspergillosis guidelines. Ann. N. Y. Acad. Sci. 1272:15-22.
66. Hadrich I, Makni F, Neji S, Cheikhrouhou F, Bellaaj H, Elloumi M, Ayadi A, Ranque S. 2012. Amphotericin B in vitro resistance is associated with fatal Aspergillus flavus infection. Med. Mycol. 50:829-834.
67. Walsh TJ, Wissel MC, Grantham KJ, Petraitiene R, Petraitis V, Kasai M, Francesconi A, Cotton MP, Hughes JE, Greene L, Bacher JD, Manna P, Salomoni M, Kleiboeker SB, Reddy SK. 2011. Molecular detection and species-specific identification of medically important Aspergillus species by real-time PCR in experimental invasive pulmonary aspergillosis. J. Clin. Microbiol. 49:4150-4157.
68. Balajee SA, Gribskov J, Brandt M, Ito J, Fothergill A, Marr KA. 2005. Mistaken identity: Neosartorya pseudofischeri and its anamorph masquerading as Aspergillus fumigatus. J. Clin. Microbiol. 43:5996-5999.
69. Klich MA, Cary JW, Beltz SB, Bennett CA. 2003. Phylogenetic and morphological analysis of Aspergillus ochraceoroseus. Mycologia 95:1252-1260.
70. El Khoury A, Atoui A, Rizk T, Lteif R, Kallassy M, Lebrihi A. 2011. Differentiation between Aspergillus flavus and Aspergillus parasiticus from pure culture and aflatoxin-contaminated grapes using PCR-RFLP analysis of aflR-aflJ intergenic spacer. J. Food. Sci. 76:M247-M253.
71. Horn BW, Moore GG, Carbone I. 2009. Sexual reproduction in Aspergillus flavus. Mycologia 101:423-429.
72. Guttman A. 1993. Separation of DNA by capillary electrophoresis, p 129-143. In Landers J (ed), Handbook of capillary and microchip electrophoresis and associated microtechniques, 3 ed. Taylor & Francis, Boca Raton, FL.
73. Tian H, Landers JP. 2002. Hydroxyethylcellulose as an effective polymer network forDNAanalysis in uncoated glass microchips: optimization and application to mutation detection via heteroduplex analysis. Anal. Biochem. 309:212-223.
74. Barron AE, Soane DS, Blanch HW. 1993. Capillary electrophoresis of DNA in uncross-linked polymer solutions. J. Chromatogr. A 652:3-16.
75. Ruiz-Martinez MC, Berka J, Belenkii A, Foret F, Miller AW, Karger BL. 1993. DNAs equencing by capillary electrophoresis with replaceable linear polyacrylamide and laser-induced fluorescence detection. Anal. Chem. 65:2851-2858.
76. Buchholz BA, Shi W, Barron AE. 2002. Microchannel DNA sequencing matrices with switchable viscosities. Electrophoresis 23:1398-1409.
77. Case WS, Glinert KD, LaBarge S, McGown LB. 2007. Guanosine gel for sequence-dependent separation of polymorphic ssDNA. Electrophoresis 28:3008-3016.
78. Yu Y, Nakamura D, DeBoyace K, Neisius AW, McGown LB. 2008. Tunable thermoassociation of binary guanosine gels. J. Phys. Chem. B 112:1130-1134.
79. Wu X, Langan TJ, Durney BC, Holland LA. 2012. Thermally responsive phospholipid preparations for fluid steering and separation in microfluidics. Electrophoresis 33:2674-2681.
80. Kwon-Chung KJ. 1975. A new pathogenic species of Aspergillus in the Aspergillus fumigatus series. Mycologia 67:770-779.