Characterization of cyclophilin-encoding genes in Phytophthora

Molecular Genetics and Genomics

Volumn 281, Issue 5, 2009, Pages 565-578

  Gan, Pamela Hui Peng ^a   Shan, Weixing ^a,b   Blackman, Leila M ^a   Hardham, Adrienne R ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b NORTHWEST A F UNIVERSITY   (China)

Author keywords

Cyclophilins; Oomycetes; Peptidyl prolyl isomerases; Phytophthora

Indexed keywords

CYCLOPHILIN; MESSENGER RNA;

ARTICLE; BIOINFORMATICS; CELL NUCLEUS; CYTOPLASM; GENE EXPRESSION; GENE SEQUENCE; IMMUNOCYTOCHEMISTRY; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYTOPHTHORA; PLANT; PLANT DISEASE; PLANT GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; SEXUAL DEVELOPMENT; SPECIES; SYNTENY; ZOOSPORE;

ALGAL PROTEINS; COMPUTATIONAL BIOLOGY; CYCLOPHILINS; EXPRESSED SEQUENCE TAGS; MULTIGENE FAMILY; PHYLOGENY; PHYTOPHTHORA; PHYTOPHTHORA INFESTANS; PLANT DISEASES; PROTEIN STRUCTURE, TERTIARY;

NICOTIANA OBTUSIFOLIA; OOMYCETES; PHYTOPHTHORA; PHYTOPHTHORA INFESTANS; PHYTOPHTHORA NICOTIANAE;

EID: 67349278806     PISSN: 16174615     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00438-009-0431-0     Document Type: Article

References (80)

1. B Adams A Musiyenko R Kumar S Barik 2005 A novel class of dual-family immunophilins J Biol Chem 280 24308 24314 (Pubitemid 40934512)
2. SF Altschul TL Madden AA Schaffer J Zhang Z Zhang W Miller DJ Lipman 1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res 25 3389 3402 (Pubitemid 27359211)
3. L Aravind EV Koonin 2000 The U box is a modified RING finger-a common domain in ubiquitination Curr Biol 10 R132 R134 (Pubitemid 30146770)
4. M Arevalo-Rodriguez J Heitman 2005 Cyclophilin A is localized to the nucleus and controls meiosis in Saccharomyces cerevisiae Eukaryot Cell 4 17 29 (Pubitemid 40234418)
5. EK Baker NJ Colley CS Zuker 1994 The cyclophilin homolog NinaA functions as a chaperone, forming a stable complex in vivo with its protein target rhodopsin EMBO J 13 4886 4895 (Pubitemid 24319372)
6. A Bell P Monaghan AP Page 2006 Peptidyl-prolyl cis-trans isomerases (immunophilins) and their roles in parasite biochemistry, host-parasite interaction and antiparasitic drug action Int J Parasitol 36 261 276 (Pubitemid 43376108)
7. JD Bendtsen H Nielsen Gv Heijne S Brunak 2004 Improved prediction of signal peptides: signal P 3.0 J Mol Biol 340 783 795 (Pubitemid 38829638)
8. E Birney S Kumar AR Krainer 1993 Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors Nucleic Acids Res 21 5803 5816 (Pubitemid 24023691)
9. JR Blankenship FL Wormley MK Boyce WA Schell SG Filler JR Perfect J Heitman 2003 Calcineurin is essential for Candida albicans survival in serum and virulence Eukaryot Cell 2 422 430 (Pubitemid 36774691)
10. KN Brazin RJ Mallis DB Fulton AH Andreotti 2002 Regulation of the tyrosine kinase Itk by the peptidyl-prolyl isomerase cyclophilin A Proc Natl Acad Sci USA 99 1899 1904 (Pubitemid 34168986)
11. J Campanella L Bitincka J Smalley 2003 MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences BMC Bioinformatics 4 29 (Pubitemid 38751241)
12. JM Chesnick M Goff J Graham C Ocampo BF Lang E Seif G Burger 2000 The mitochondrial genome of the stramenopile alga Chrysodidymus synuroideus. Complete sequence, gene content and genome organization Nucleic Acids Res 28 2512 2518 (Pubitemid 30420848)
13. R Chiu O Rey JQ Zheng JL Twiss J Song S Pang KK Yokoyama 2003 Effects of altered expression and localization of cyclophilin A on differentiation of p19 embryonic carcinoma cells Cell Mol Neurobiol 23 929 943 (Pubitemid 38063333)
14. IT Chou CS Gasser 1997 Characterization of the cyclophilin gene family of Arabidopsis thaliana and phylogenetic analysis of known cyclophilin proteins Plant Mol Biol 35 873 892 (Pubitemid 28016946)
15. M Clamp J Cuff SM Searle GJ Barton 2004 The jalview java alignment editor Bioinformatics 20 426 427 (Pubitemid 38262778)
16. G Coaker A Falick B Staskawicz 2005 Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin Science 308 548 550 (Pubitemid 40570584)
17. NJ Colley EK Baker MA Stamnes CS Zuker 1991 The cyclophilin homolog ninaA is required in the secretory pathway Cell 67 255 263
18. M Cope MC Webb ET O' Gara BA Philip AR Hardham 1996 Immunocytochemical comparison of peripheral vesicles in zoospores of Phytophthora and Phytium species Mycologia 88 91 102 (Pubitemid 27004882)
19. MC Cruz M Del Poeta P Wang R Wenger G Zenke VFJ Quesniaux NR Movva JR Perfect ME Cardenas J Heitman 2000 Immunosuppressive and nonimmunosuppressive cyclosporine analogs are toxic to the opportunistic fungal pathogen Cryptococcus neoformans via cyclophilin-dependent inhibition of calcineurin Antimicrob Agents Chemother 44 143 149 (Pubitemid 30010685)
20. O Emanuelsson H Nielsen S Brunak Gv Heijne 2000 Predicting subcellular localization of proteins based on their N-terminal amino acid sequence J Mol Biol 300 1005 1016
21. HC Evans C Prior 1987 Cocoa pod diseases: causal agents and control Outlook Agric 16 13 41
22. J Felsenstein 1989 PHYLIP-phylogeny inference package (version 3.4) Cladistics 5 164 166
23. PA Ferrereira TA Nakayama WL Pak GH Travis 1996 Cyclophilin-related protein RanBP2 acts as a chaperone for red/green opsin Nature 383 637 640 (Pubitemid 26347588)
24. DS Fox J Heitman 2002 Good fungi gone bad: the corruption of calcineurin Bioessays 24 894 903 (Pubitemid 35197585)
25. BC Freeman DO Toft RI Morimoto 1996 Molecular chaperone machines: chaperone activities of the cyclophilin Cyp-40 and the steroid aporeceptor-associated protein p23 Science 274 1718 1720 (Pubitemid 26414905)
26. A Galat 1999 Variations of sequences and amino acid compositions of proteins that sustain their biological functions: an analysis of the cyclophilin family of proteins Arch Biochem Biophys 371 149 162
27. E Gaulin A Jauneau F Villalba M Rickauer M-T Esquerre-Tugaye A Bottin 2002 The CBEL glycoprotein of Phytophthora parasitica var-nicotianae is involved in cell wall deposition and adhesion to cellulosic substrates J Cell Sci 115 4565 4575 (Pubitemid 36004416)
28. LY Geer M Domrachev DJ Lipman SH Bryant 2002 CDART: protein homology by domain architecture Genome Res 12 1619 1623 (Pubitemid 35175101)
29. AV Godoy AS Lazzaro CA Casalongue B San Segundo 2000 Expression of a Solanum tuberosum cyclophilin gene is regulated by fungal infection and abiotic stress conditions Plant Sci 152 123 134 (Pubitemid 30106393)
30. A Götesson JS Marshall DA Jones AR Hardham 2002 Characterization and evolutionary analysis of a large polygalacturonase gene family in the oomycete plant pathogen Phytophthora cinnamomi Mol Plant Microbe Interact 15 907 921 (Pubitemid 35197596)
31. CM Grant 2001 Role of the glutathione/ glutaredoxin and thioredoxin systems in yeast growth and response to stress conditions Mol Microbiol 39 533 541 (Pubitemid 32158135)
32. Gregory PH (1983) Some major epidemics caused by Phytophthora. In: Erwin DC, Bartnicki-Garcia S, Tsao PH (eds) Phytophthora: its biology, taxonomy, ecology, and pathology. American Phytopathological Society, St Paul, pp 271-278
33. F Gubler AR Hardham 1988 Secretion of adhesive material during encystment of Phytophthora cinnamomi zoospores, characterised by immunogold labelling with monoclonal antibodies to components of peripheral vesicles J Cell Sci 90 225 235
34. M Gullerova A Barta ZJ Lorković 2006 AtCyp59 is a multidomain cyclophilin from Arabidopsis thaliana that interacts with SR proteins and the C-terminal domain of the RNA polymerase II RNA 12 631 643
35. TA Hall 1999 BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT Nucleic Acids Symp Ser 41 95 98
36. RE Handschumacher MW Harding J Rice RJ Drugge DW Speicher 1984 Cyclophilin: a specific cytosolic binding protein for cyclosporin A Science 226 544 547 (Pubitemid 14018525)
37. Hardham AR (2001) Investigations of oomycete cell biology. In: Talbot NJ (ed) Molecular and cell biology of filamentous fungi: a practical approach. Oxford University Press, Oxford, pp 127-155
38. AR Hardham 2005 Phytophthora cinnamomi Mol Plant Pathol 6 589 604
39. AR Hardham F Gubler 1990 Polarity of attachment of zoospores of a root pathogen and pre-alignment of the emerging germ tube Cell Biol Int Rep 14 947 956
40. A Harel S Bercovich O Yarden 2006 Calcineurin is required for sclerotial development and pathogenicity of Sclerotinia sclerotiorum in an oxalic acid-independent manner Mol Plant Microbe Interact 19 682 693 (Pubitemid 43787732)
41. Z He L Li S Luan 2004 Immunophilins and parvulins. Superfamily of peptidyl prolyl isomerases in Arabidopsis Plant Physiol 134 1248 1267 (Pubitemid 38527337)
42. D Higgins J Thompson T Gibson 1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighing position-specific gap penalties and weight matrix choice Nucleic Acids Res 22 4673 4680 (Pubitemid 24354800)
43. J Kallen C Spitzfaden MGM Zurini G Wider H Widmer K Wuthrich MD Walkinshaw 1991 Structure of human cyclophilin and its binding site for cyclosporin A determined by X-ray crystallography and NMR spectroscopy Nature 353 276 279
44. S Kamoun 2003 Molecular genetics of pathogenic oomycetes Eukaryot Cell 2 191 199 (Pubitemid 36562358)
45. H Ke L Zydowsky J Liu C Walsh 1991 Crystal structure of recombinant human T-cell cyclophilin A at 2.5 Å resolution Proc Natl Acad Sci USA 88 9483 9487
46. T Kiefhaber R Quaas U Hahn FX Schmid 1990 Folding of ribonuclease T1.2. Kinetic models for the folding and unfolding reactions Biochemistry 29 3061 3070 (Pubitemid 20119304)
47. R Krämer S Freytag E Schmelzer 1997 In vitro formation of infection structures of Phytophthora infestans is associated with synthesis of stage specific polypeptides Eur J Plant Pathol 103 43 53 (Pubitemid 27108749)
48. A Krzywicka J Beisson A-M Keller J Cohen M Jerka-Dziadosz C Klotz 2001 KIN241: a gene involved in cell morphogenesis in Paramecium tetraurelia reveals a novel protein family of cyclophilin-RNA interacting proteins (CRIPs) conserved from fission yeast to man Mol Microbiol 42 257 267 (Pubitemid 34212177)
49. M Latijnhouwers Wit PJGMd F Govers 2003 Oomycetes and fungi: similar weaponry to attack plants Trends Microbiol 11 462 469 (Pubitemid 37214873)
50. M Le Hir Q Su L Weber G Woerly A Granelli-Piperno B Ryffel 1995 In situ detection of cyclosporin A: evidence for nuclear localization of cyclosporine and cyclophilins Lab Investig 73 727 733
51. D Li R Roberts 2001 Human genome and diseases: WD-repeat proteins: structure characteristics, biological function, and their involvement in human diseases Cell Mol Life Sci 58 2085 2097 (Pubitemid 34016977)
52. A Marchler-Bauer JB Anderson PF Cherukuri C DeWeese-Scott LY Geer M Gwadz S He DI Hurwitz JD Jackson Z Ke CJ Lanczycki CA Liebert C Liu F Lu GH Marchler M Mullokandov BA Shoemaker V Simonyan JS Song PA Thiessen RA Yamashita JJ Yin SH Bryant 2005 CDD: a Conserved Domain Database for protein classification Nucleic Acids Res 33 D192 D196 (Pubitemid 40207858)
53. PJ Mark BK Ward P Kumar H Lahooti RF Minchin T Ratajczak 2001 Human cyclophilin 40 is a heat shock protein that exhibits altered intracellular localization following heat shock Cell Stress Chaperones 6 59 70 (Pubitemid 32275330)
54. A McLeod CD Smart WE Fry 2004 Core promoter structure in the oomycete Phytophthora infestans Eukaryot Cell 3 91 99 (Pubitemid 38237301)
55. V Mikol J Kallen G Pflugl MD Walkinshaw 1993 X-ray structure of a monomeric cyclophilin A-cyclosporin A crystal complex at 2.1 Å resolution J Mol Biol 234 1119 1130 (Pubitemid 24027241)
56. HJ Mitchell AR Hardham 1999 Characterization of the water expulsion vacuole in Phytophthora nicotianae zoospores Protoplasma 206 118 130 (Pubitemid 29496731)
57. JW Montague FMJ Hughes JA Cidlowski 1997 Native recombinant cyclophilins A, B and C degrade DNA independently of peptidylprolyl cis-trans-isomerase activity. Potential roles of cyclophilins in apoptosis J Biol Chem 272 6677 6684 (Pubitemid 27118154)
58. A Odom S Muir E Lim DL Toffaletti JR Perfect J Heitman 1997 Calcineurin is required for virulence of Cryptococcus neoformans EMBO J 16 2576 2589 (Pubitemid 27226197)
59. RD Page 1996 TreeView: an application to display phylogenetic trees on personal computers Comput Appl Biosci 12 357 358 (Pubitemid 126760426)
60. TJ Pemberton JE Kay 2005 Identification and comparative analysis of the peptidyl-prolyl cis/trans isomerase repertoires of H. sapiens, D. melanogaster, C. elegans, S. cerevisiae and Sz. pombe Comp Funct Genomics 6 277 300 (Pubitemid 41319900)
61. CJ Penington JR Iser BR Grant KR Gayler 1989 Role of RNA and protein synthesis in stimulated germination of zoospores of the pathogenic fungus Phytophthora palmivora Exp Mycol 13 158 168 (Pubitemid 19153022)
62. K Piotukh W Gu M Kofler D Labudde V Helms C Freund 2005 Cyclophilin A binds to linear peptide motifs containing a consensus that is present in many human proteins J Biol Chem 280 23668 23674 (Pubitemid 40884848)
63. SP Reddy WG Rasmussen JB Baseman 1996 Correlations between Mycoplasma pneumoniae sensitivity to cyclosporin A and cyclophilin-mediated regulation of mycoplasma cytadherence Microb Pathog 20 155 169 (Pubitemid 26132923)
64. DM Rizzo M Garbelotto JM Davidson GW Slaughter ST Koike 2002 Phytophthora ramorum as the cause of extensive mortality of Quercus spp. and Lithocarpus densiflorus in California Plant Dis 86 205 214 (Pubitemid 34191066)
65. AV Robold A Hardham 2005 During attachment Phytophthora spores secrete proteins containing thrombospondin type 1 repeats Curr Genet 47 307 315 (Pubitemid 40723971)
66. AH Sarris MW Harding TR Jiang D Aftab RE Handschumacher 1992 Immunofluorescent localization and immunochemical determination of cyclophilin-A with specific rabbit antisera Transplantation 54 904 910
67. W Shan AR Hardham 2004 Construction of a bacterial artificial chromosome library, determination of genome size, and characterization of an Hsp70 gene family in Phytophthora nicotianae Fungal Genet Biol 41 369 380 (Pubitemid 38169456)
68. W Shan JS Marshall AR Hardham 2004 Gene expression in germinated cysts of Phytophthora nicotianae Mol Plant Pathol 5 317 330 (Pubitemid 38940767)
69. B Sherry N Yarlett A Strupp A Cerami 1992 Identification of cyclophilin as a proinflammatory secretory product of lipopolysaccharide-activated macrophages PNAS 89 3511 3515
70. D Škalamera AP Wasson AR Hardham 2004 Genes expressed in zoospores of Phytophthora nicotianae Mol Gen Genet 270 549 557 (Pubitemid 38200045)
71. J Suzuki Z-G Jin DF Meoli T Matoba BC Berk 2006 Cyclophilin A is secreted by a vesicular pathway in vascular smooth muscle cells Circ Res 98 811 817 (Pubitemid 43755265)
72. BM Tyler S Tripathy X Zhang P Dehal RHY Jiang A Aerts FD Arredondo L Baxter D Bensasson JL Beynon J Chapman CMB Damasceno AE Dorrance D Dou AW Dickerman IL Dubchak M Garbelotto M Gijzen SG Gordon F Govers NJ Grunwald W Huang KL Ivors RW Jones S Kamoun K Krampis KH Lamour M-K Lee WH McDonald M Medina HJG Meijer EK Nordberg DJ Maclean MD Ospina-Giraldo PF Morris V Phuntumart NH Putnam S Rash JKC Rose Y Sakihama AA Salamov A Savidor CF Scheuring BM Smith BWS Sobral A Terry TA Torto-Alalibo J Win Z Xu H Zhang IV Grigoriev DS Rokhsar JL Boore 2006 Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis Science 313 1261 1266 (Pubitemid 44330944)
73. Y Van de Peer G van der Auwera R De Wachter 1996 The evolution or stramenopiles and alveolates as derived by "substitution rate calibration" of small ribosomal subunit RNA J Mol Evol 42 201 210 (Pubitemid 126437669)
74. MC Viaud PV Balhadere NJ Talbot 2002 A Magnaporthe grisea cyclophilin acts as a virulence determinant during plant infection Plant Cell 14 917 930 (Pubitemid 34523036)
75. M Viaud A Brunet-Simon Y Brygoo J-M Pradier C Levis 2003 Cyclophilin A and calcineurin functions investigated by gene inactivation, cyclosporin A inhibition and cDNA arrays approaches in the phytopathogenic fungus Botrytis cinerea Mol Microbiol 50 1451 1465 (Pubitemid 38010444)
76. DH Walter J Haendeler J Galle AM Zeiher S Dimmeler 1998 Cyclosporin A inhibits apoptosis of human endothelial cells by preventing release of cytochrome C from mitochondria Circulation 98 1153 1157 (Pubitemid 28436163)
77. BB Wang KJ Hayeng DG Payan JM Fisher 1996 Identification of a nuclear-specific cyclophilin which interacts with the proteinase inhibitor eglin c Biochem J 314 313 319 (Pubitemid 26063864)
78. J Win T-D Kanneganti T Torto-Alalibo S Kamoun 2006 Computational and comparative analyses of 150 full-length cDNA sequences from the oomycete plant pathogen Phytophthora infestans Fungal Genet Biol 43 20 33 (Pubitemid 43038751)
79. H-Z Yan R-F Liou 2006 Selection of internal control genes for real-time quantitative RT-PCR assays in the oomycete plant pathogen Phytophthora parasitica Fungal Genet Biol 43 430 438 (Pubitemid 43668998)
80. LD Zydowsky FA Etzkorn HY Chang SB Ferguson LA Stolz SI Ho CT Walsh 1992 Active site mutants of human cyclophilin A separate peptidyl-prolyl isomerase activity from cyclosporin A binding and calcineurin inhibition Protein Sci 1 1092 1099 (Pubitemid 23016423)