PRP8 intein in Ajellomycetaceae family pathogens: Sequence analysis, splicing evaluation and homing endonuclease activity

Fungal Genetics and Biology

Volumn 48, Issue 2, 2011, Pages 80-91

  Theodoro, Raquel Cordeiro ^a,b   Volkmann, Gerrit ^b   Liu, Xiang Qin ^b   Bagagli, Eduardo ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Ajellomycetaceae; Homing endonuclease; Intein; PRP8; Splicing

Indexed keywords

ENDONUCLEASE; INTEIN; NUCLEAR PROTEIN; PRP8 INTEIN; UNCLASSIFIED DRUG;

AJELLOMYCES; AJELLOMYCETACEAE; ARTICLE; BLASTOMYCES DERMATITIDIS; CONTROLLED STUDY; EMMONSIA PARVA; ENZYME ACTIVITY; ESCHERICHIA COLI; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; BLASTOMYCES; CHRYSOSPORIUM; CLUSTER ANALYSIS; ENDONUCLEASES; ESCHERICHIA COLI; FUNGAL PROTEINS; INTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN SPLICING; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS;

AJELLOMYCES CAPSULATUS; AJELLOMYCES DERMATITIDIS; AJELLOMYCETACEAE; EMMONSIA PARVA; ESCHERICHIA COLI; FUNGI; PARACOCCIDIOIDES BRASILIENSIS;

EID: 78649960166     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2010.07.010     Document Type: Article

References (52)

1. Bagagli E., Franco M., Bosco S.M.G., Hebeler-Barbosa F., Trinca L.A., Montenegro M.R. High frequency of Paracoccidioides brasiliensis infection in armadillos (Dasypus novemcinctus): an ecological study. Med. Mycol. 2003, 41:217-223.
2. Belfort M., Roberts R.J. Homing endonucleases: keeping the house in order. Nucleic Acids Res. 1997, 25:3379-3388.
3. Bokor A.A.M., Kan J.A.L.V., Poulter R.T.M. Sexual mating of Botrytis cinerea illustrates PRP8 intein HEG activity. Fungal Genet. Biol. 2010, 10.1016/j.fgb.2010.01.003.
4. Burt A., Koufopanou V. Homing endonuclease genes: the rise and fall and rise again of a selfish element. Curr. Opin. Gen. Develop. 2004, 14:609-615.
5. Butler M.L., Goodwin T.J.D., Poulter R.T.M. A nuclear-encoded intein in the fungal pathogen Cryptococcus neoformans. Yeast 2001, 18:1365-1370.
6. Butler M.I., Gray J., Goodwin T.J., Poulter R.T.M. The distribution and evolutionary history of the PRP8 intein. BMC Evol. Biol. 2006, 6:1-26.
7. Butler M.I., Poulter R.T. The PRP8 inteins in Cryptococcus are a source of phylogenetic and epidemiological information. Fungal Genet. Biol. 2005, 42:452-463.
8. Carrero L.L., Niño-Vega G., Teixeira M.M., Carvalho M.J.A., Soares C.M.A., Pereira M., Jesuíno R.S.A., McEween J.G., Mendoza L., Taylor J.W., Felipe M.S., San-Blas G. New Paracoccidioides brasiliensis isolate reveals unexpected genomic variability in this human pathogen. Fungal Genet. Biol. 2008, 45:605-612.
9. Chong S., Shao Y., Paulus H., Benner J., Perler F.B., Xu M.Q. Protein splicing involving the Saccharomyces cerevisiae VMA intein. The steps in the splicing pathway, side reactions leading to protein cleavage, and establishment of an in vitro splicing system. J. Biol. Chem. 1996, 271:22159-22168.
10. Cooper A.A., Chen Y.J., Lindorfer M.A., Stevens T.H. Protein splicing of the yeast TFP1 intervening protein sequence: a model for self-excision. EMBO J. 1993, 12:2575-2583.
11. Daugelat S., Jacobs W.R. The Mycobacterium tuberculosis recA intein can be used in an ORFTRAP to select for open reading frames. Protein Sci. 1999, 8:644-653.
12. Davis E.O., Jenner P.J., Brooks P.C., Colston M.J., Sedgwick S.G. Protein splicing in the maturation of M. Tuberculosis recA protein: a mechanism for tolerating a novel class of intervening sequence. Cell 1992, 71:201-210.
13. Derbyshire V., Wood D.W., Wu W., Dansereau J.T., Dalgaard J.Z., Belfort M. Genetic definition of a protein-splicing domain: functional mini-inteins support structure predictions and a model for intein evolution. Proc. Nat. Acad. Sci. USA 1997, 94:11466-11471.
14. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:783-791.
15. Franco M. Host-parasite relationships in paracoccidioidomycosis. J. Med. Vet. Mycol. 1987, 25:5-18.
16. Gangopadhyay J.P., Jiang S.Q., Paulus H. An in vitro screening system for protein splicing inhibitors based on green fluorescent protein as an indicator. Anal. Chem. 2003, 75:2456-2462.
17. Gimble F.S., Thorner J. Homing of a DNA endonuclease gene by meiotic gene conversion in Saccharomyces cerevisiae. Nature 1992, 357:301-306.
18. Gogarten J.P., Hilario E. Inteins, introns, and homing endonucleases: recent revelations about the life cycle of parasitic genetic elements. BMC Evol. Biol. 2006, 6:1-5.
19. Gogarten J.P., Senejani A.G., Zhaxybayeva O., Olendzenski L., Hilario E. Inteins: structure, function, and evolution. Annu. Rev. Microbiol. 2002, 56:263-287.
20. Gonzales M., Dugan J., Shafer R. Synonymous-non-synonymous mutation rates between sequences containing ambiguous nucleotides (Syn-SCAN). Bioinformatics 2002, 18:886-887.
21. Grainger R.J., Beggs J.D. Prp8 protein: at the heart of the spliceosome. RNA 2005, 11:533-557.
22. Guhan N., Muniyappa K. Mycobacterium tuberculosis RecA intein possesses a novel ATP-dependent site-specific double-stranded DNA endonuclease activity. J. Biol. Chem. 2002, 277:16257-16264.
23. Guhan N., Muniyappa K. Structural and functional characteristics of homing endonucleases. Crit. Rev. Biochem. Mol. 2003, 38:199-248.
24. Hebeler-Barbosa F., Morais F.V., Montenegro M.R., Kuramae E.E., Montes B., McEwen J.G., Puccia R., Bagagli E. Sequence comparison of the internal transcribed spacer regions and gp 43 in Paracoccidioides brasiliensis for patients and armadillos Dasypus novemcinctus. J. Clin. Microbiol. 2003, 41:5735-5737.
25. Hoog G.S., Guarro J., Gené J., Figueras M.J. Atlas of Clinical Fungi 2000, Centraalbureau voor Schimmelcultures, Ultrech.
26. Koufopanou V., Burt A. Degeneration and domestication of a selfish gene in yeast: molecular evolution versus site-directed mutagenesis. Mol. Biol. Evol. 2005, 22:1535-1538.
27. Kumar S., Tamura K., Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 2004, 5:150-163.
28. Liu X.Q. Protein-splicing intein: genetic mobility, origin, and evolution. Annu. Rev. Genet. 2000, 34:61-76.
29. Liu X.Q., Yang J. Prp8 intein in fungal pathogens: target for potential antifungal drugs. FEBS Lett. 2004, 572:46-50.
30. Matute D.R., McEwen J.G., Puccia R., Montes B.A., San-Blas G., Bagagli E., Rauscher J.T., Restrepo A., Morais F., Nino-Vega G., et al. Cryptic speciation and recombination in the fungus Paracoccidioides brasiliensis as revealed by gene genealogies. Mol. Biol. Evol. 2006, 23:65-73.
31. Matute D.R., Sepulveda V.E., Quesada L.M., Goldman G.H., Taylor J.W., Restrepo A., McEwen J.G. Microsatellite analysis of three phylogenetic species of Paracoccidioides brasiliensis. J. Clin. Microbiol. 2006, 44:2153-2157.
32. McCullough M.J., DiSalvo A.F., Clemons K.V., Park P., Stevens D.A. Molecular epidemiology of Blastomyces dermatitidis. Clin. Infect. Dis. 2000, 30:328-335.
33. Narmandakh A., Bearne S.L. Purification of recombinant mandelate racemase: improved catalytic activity. Protein Expres. Purif. 2009, 69:39-46.
34. Nei M., Gojobori T. Simple methods for estimating the numbers of synonymous and non-synonymous nucleotide substitutions. Mol. Biol. Evol. 1986, 3:418-426.
35. Okuda Y., Sasaki D., Nogami S., Kaneko Y., Ohya Y., Anraku Y. Occurrence, horizontal transfer and degeneration of VDE intein family in Saccharomycete yeasts. Yeast 2003, 20:563-573.
36. Paulus H. Inteins as targets for potential antimycobacterial drugs. Front. Biosci. 2003, 8:1157-1165.
37. Pearl E.J., Tyndall J.D.A., Poulter R.T.M., Wilbanks S.M. Sequence requirements for splicing by the Cne PRP8 intein. FEBS Lett. 2007, 581:3000-3004.
38. Perler F.B. InBase, the intein database. Nucleic Acids Res. 2000, 28:344-345.
39. Perler F.B., Adam E. Protein splicing and its applications. Curr. Opin. Biotechnol. 2000, 11:377-383.
40. Perler F.B., Davis E.O., Dean G.E., Gimble F.S., Jack W.E., Neff N., Noren C.J., Thorner J., Belfort M. Protein splicing elements: inteins and exteins - a definition of terms and recommended nomenclature. Nucleic Acids Res. 1994, 22:1125-1127.
41. Posey K.L., Koufopanou V., Burt A., Gimble F.S. Evolution of divergent DNA recognition specificities in VDE homing endonucleases from two yeast species. Nucleic Acids Res. 2004, 32:3947-3956.
42. Poulter R.T., Goodwin T.J., Butler M.I. The nuclear-encoded inteins of fungi. Fungal Genet. Biol. 2007, 44:153-179.
43. Taborda P.R., Taborda V.A., McGinnis M.R. Lacazia loboi, the etiologic agent of lobomycosis. J. Clin. Microbiol. 1999, 37:2031-2033.
44. Teixeira M.M., Theodoro R.C., de Carvalho M.J., Fernandes L., Paes H.C., Hahn R.C., Mendoza L., Bagagli E., San-Blas G., Felipe M.S. Phylogenetic analysis reveals a high level of speciation in the Paracoccidioides genus. Mol. Phylogenet. Evol. 2009, 52:273-283.
45. Theodoro R.C., Bagagli E. Inteins in pathogenic fungi: a phylogenetic tool and perspectives for therapeutic applications. Mem. Inst. Oswaldo Cruz 2009, 104:497-504.
46. Theodoro R.C., Bagagli E., Oliveira C. Phylogenetic analysis of PRP8 intein in Paracoccidioides brasiliensis species complex. Fungal Genet. Biol. 2008, 45:1284-1291.
47. Untereiner W.A., Scott J.A., Naveau F.A., Sigler L., Bachewish J., Angus A. The Ajellomycetaceae, a new family of vertebrate-associate Onygenales. Mycology 2004, 96:812-821.
48. Vilela R., Rosa P.S., Belone A.F., Taylor J.W., Diorio S.M., Mendoza L. Molecular phylogeny of animal pathogen Lacazia loboi inferred from rDNA and DNA coding sequences. Mycol. Res. 2009, 113:851-857.
49. Wu H., Hu Z., Liu X.Q. Protein trans-splicing by a split intein encoded in a split DnaE gene of Synechocystis sp. PCC6803. Proc. Nat. Acad. Sci. USA 1998, 95:9226-9231.
50. Wu H., Xu M.Q., Liu X.Q. Protein trans-splicing and functional mini-inteins of a cyanobacterial dnaB intein. Biochim. Biophys. Acta 1998, 1387:422-432.
51. Xu M.Q., Perler F.B. The mechanism of protein splicing and its modulation by mutation. EMBO J. 1996, 15:5146-5153.
52. Zeidler M.P., Tan C., Bellaiche Y., Cherry S., Hader S., Gayko U., Perrimon N. Temperature-sensitive control of protein activity by conditionally splicing inteins. Nat. Biotechnol. 2004, 22:871-876.