Alternative splicing: A novel mechanism of regulation identified in the chorismate mutase gene of the potato cyst nematode Globodera rostochiensis

Molecular and Biochemical Parasitology

Volumn 162, Issue 1, 2008, Pages 1-15

  Lu, Shun Wen ^a   Tian, Duanhua ^a   Borchardt Wier, Harmony B ^b   Wang, Xiaohong ^a,b  

^a Department of Obstetrics Gynecology   (United States)

^b ROBERT W HOLLEY CENTER FOR AGRICULTURE AND HEALTH   (United States)

Author keywords

Alternative splicing; Chorismate mutase; Dominant negative isoform; Globodera rostochiensis; Intron retention; Plant parasitic nematode

Indexed keywords

CHORISMATE MUTASE; HOMODIMER; MESSENGER RNA; PROTEIN GR CM 1 T; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DIMERIZATION; DOWN REGULATION; ENZYME ACTIVITY; ESCHERICHIA COLI; ESOPHAGUS; GENE FREQUENCY; GENOME; GLOBODERA ROSTOCHIENSIS; IN SITU HYBRIDIZATION; JUVENILE; LOW TEMPERATURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE DEVELOPMENT; POLYACRYLAMIDE GEL ELECTROPHORESIS; POTATO CYST NEMATODE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SPLICING; YEAST;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CHORISMATE MUTASE; DIMERIZATION; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOST-PARASITE INTERACTIONS; INTRONS; MOLECULAR SEQUENCE DATA; PLANT DISEASES; PROTEIN ISOFORMS; SEQUENCE ANALYSIS, DNA; SOLANUM TUBEROSUM; TWO-HYBRID SYSTEM TECHNIQUES; TYLENCHOIDEA;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; GLOBODERA ROSTOCHIENSIS; NEMATODA; SOLANUM TUBEROSUM;

EID: 52049104487     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2008.06.002     Document Type: Article

References (61)

1. Blencowe B.J. Alternative splicing: new insights from global analyses. Cell 126 (2006) 37-47
2. Johnson J.M., Castle J., Garrett-Engele P., et al. Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 302 (2003) 2141-2144
3. Moroy T., and Heyd F. The impact of alternative splicing in vivo: mouse models show the way. RNA 13 (2007) 1155-1171
4. Lee Y., Lee Y., Kim B., et al. ECgene: an alternative splicing database update. Nucleic Acids Res 35 (2007) D99-103
5. Iida K., Seki M., Sakurai T., et al. Genome-wide analysis of alternative pre-mRNA splicing in Arabidopsis thaliana based on full-length cDNA sequences. Nucleic Acids Res 32 (2004) 5096-5103
6. Zahler AM. Alternative splicing in C. elegans. WormBook. The C. elegans Research Community, doi:10.1895/wormbook.1.31.1, http//www.wormbook.org. 2005
7. Jin J., Poole C.B., Slatko B.E., and McReynolds L.A. Alternative splicing creates sex-specific transcripts and truncated forms of the furin protease in the parasite Dirofilaria immitis. Gene 237 (1999) 161-175
8. Kampkotter A., Volkmann T.E., de Castro S.H., et al. Functional analysis of the glutathione S-transferase 3 from Onchocerca volvulus (Ov-GST-3): a parasite GST confers increased resistance to oxidative stress in Caenorhabditis elegans. J Mol Biol 325 (2003) 25-37
9. Herrmann K.M. The shikimate pathway as an entry to aromatic secondary metabolism. Plant Physiol 107 (1995) 7-12
10. Dewick P.M. The biosynthesis of shikimate metabolites. Natual Prod Rep 15 (1998) 17-58
11. Herrmann K.M., and Weaver L.M. The shikimate pathway. Annu Rev Plant Physiol Plant Mol Biol 50 (1999) 473-503
12. Lambert K.N., Allen K.D., and Sussex I.M. Cloning and characterization of an esophageal-gland-specific chorismate mutase from the phytoparasitic nematode Meloidogyne javanica. Mol Plant Microbe Interact 12 (1999) 328-336
13. Bekal S., Niblack T.L., and Lambert K.N. A chorismate mutase from the soybean cyst nematode Heterodera glycines shows polymorphisms that correlate with virulence. Mol Plant Microbe Interact 16 (2003) 439-446
14. Jones J.T., Furlanetto C., Bakker E., et al. Characterization of a chorismate mutase from the potato cyst nematode Globodera pallida. Mol Plant Pathol 4 (2003) 43-50
15. Huang G., Dong R., Allen R., Davis E.L., Baum T.J., and Hussey R.S. Two chorismate mutase genes from the root-knot nematode Meloidogyne incognita. Mol Plant Pathol 6 (2005) 23-30
16. Long H., Wang X., and Xu J. Molecular cloning and life-stage expression pattern of a new chorismate mutase gene from the root-knot nematode Meloidogyne arenaria. Plant Pathol 55 (2006) 559-563
17. Long H., Wang X., Xu J.H., and Hu Y.J. Isolation and characterization of another cDNA encoding a chorismate mutase from the phytoparasitic nematode Meloidogyne arenaria. Exp Parasitol 113 (2006) 106-111
18. Haslam E. Shikimic acid: metabolism and metabolites (1993), John Wiley & Sons, New York
19. Weaver L.M., and Herrmann K.M. Dynamics of the shikimate pathway in plants. Trends Plant Sci 2 (1997) 346-351
20. Hussey R.S. Disease-inducing secretions of plant-parasitic nematodes. Annu Rev Phytopathol 27 (1989) 123-141
21. Davis E.L., Hussey R.S., Baum T.J., et al. Nematode parasitism genes. Annu Rev Phytopathol 38 (2000) 365-396
22. Davis E.L., Hussey R.S., and Baum T.J. Getting to the roots of parasitism by nematodes. Trends Parasitol 20 (2004) 134-141
23. Doyle E.A., and Lambert K.N. Meloidogyne javanica chorismate mutase 1 alters plant cell development. Mol Plant Microbe Interact 16 (2003) 123-131
24. Bakhetia M., Urwin P.E., and Atkinson H.J. qPCR analysis and RNAi define pharyngeal gland cell-expressed genes of Heterodera glycines required for initial interactions with the host. Mol Plant Microbe Interact 20 (2007) 306-312
25. Brodie B.B. Classical and molecular approaches for managing nematodes affecting potato. Can J Plant Pathol 21 (1999) 222-230
26. Skantar A.M., Handoo Z.A., Carta L.K., and Chitwood D.J. Morphological and molecular identification of Globodera pallida associated with potato in Idaho. J Nematol 39 (2007) 133-144
27. Sun F., Miller S., Wood S., and Cote M.-J. Occurrence of potato cyst nematode, Globodera rostochiensis, on potato in the Saint-Amable region, Quebec, Canada. Plant Dis 91 (2007) 908
28. Brodie B.B., Plaisted R.L., and de Scurrah M.M. The incorporation of resistance to Globodera pallida into Solanum tuberosum germplasm adapted to North America. Am Potato J 68 (1991) 1-11
29. Brodie B.B. Effect of initial nematode density on managing Globodera rostochiensis with resistant cultivars and nonhosts. J Nematol 28 (1996) 510-519
30. Clarke A.J., and Perry R.N. Hatching of cyst-nematodes. Nematologica 23 (1977) 350-368
31. Edwards K., Johnstone C., and Thompson C. A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res 19 (1991) 1349
32. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual. 2nd ed. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press; 1989.
33. Wang X., Allen R., Ding X., et al. Signal peptide-selection of cDNA cloned directly from the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol Plant-Microbe Interact 14 (2001) 536-544
34. De Boer J.M., Yan Y., Smant G., Davis E.L., and Baum T.J. In-situ hybridization to messenger RNA of Heterodera glycines. J Nematol 30 (1998) 309-312
35. Baldwin G.S., and Davidson B.E. A kinetic and structural comparison of chorismate mutase/prephenate dehydratase from mutant strains of Escherichia coli K 12 defective in the PheA gene. Arch Biochem Biophys 211 (1981) 66-75
36. Venema R.C., Ju H., Zou R., Ryan J.W., and Venema V.J. Subunit interactions of endothelial nitric-oxide synthase. Comparisons to the neuronal and inducible nitric-oxide synthase isoforms. J Biol Chem 272 (1997) 1276-1282
37. Lorenz M., Hewing B., Hui J., et al. Alternative splicing in intron 13 of the human eNOS gene: a potential mechanism for regulating eNOS activity. FASEB J 21 (2007) 1556-1564
38. Altschul S.F., Madden T.L., Schaffer A.A., et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 (1997) 3389-3402
39. Marchler-Bauer A., and Bryant S.H. CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32 (2004) W327-W331
40. Nielsen H., Engelbrecht J., Brunak S., and von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10 (1997) 1-6
41. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25 (1997) 4876-4882
42. Qamra R., Prakash P., Aruna B., Hasnain S.E., and Mande S.C. The 2.15 Å crystal structure of Mycobacterium tuberculosis chorismate mutase reveals an unexpected gene duplication and suggests a role in host-pathogen interactions. Biochemistry 45 (2006) 6997-7005
43. Felsenstein J. PHYLIP-Phylogeny Inference Package (Version 3.2). Cladistics 5 (1989) 164-166
44. Lee A.Y., Karplus P.A., Ganem B., and Clardy J. Atomic structure of the buried catalytic pocket of Escherichia coli chorismate mutase. J Am Chem Soc 117 (1995) 3627-3628
45. Blumenthal T, Steward K. RNA processing and gene structure. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR, editors, C. elegans II. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press; 1997. p. 117-46.
46. Hastings M.L., Wilson C.M., and Munroe S.H. A purine-rich intronic element enhances alternative splicing of thyroid hormone receptor mRNA. RNA 7 (2001) 859-874
47. Mercado P.A., Ayala Y.M., Romano M., Buratti E., and Baralle F.E. Depletion of TDP 43 overrides the need for exonic and intronic splicing enhancers in the human apoA-II gene. Nucleic Acids Res 33 (2005) 6000-6010
48. Xia T., Song J., Zhao G., Aldrich H., and Jensen R.A. The AroQ-encoded monofunctional chorismate mutase (CM-F) protein is a periplasmic enzyme in Erwinia herbicola. J Bacteriol 175 (1993) 4729-4737
49. Calhoun D.H., Bonner C.A., Gu W., Xie G., and Jensen R.A. The emerging periplasm-localized subclass of AroQ chorismate mutases, exemplified by those from Salmonella typhimurium and Pseudomonas aeruginosa. Genome Biol 2 (2001) 1-16
50. Sasso S., Ramakrishnan C., Gamper M., Hilvert D., and Kast P. Characterization of the secreted chorismate mutase from the pathogen Mycobacterium tuberculosis. FEBS J 272 (2005) 375-389
51. Takai S., Hines S.A., Sekizaki T., et al. DNA sequence and comparison of virulence plasmids from Rhodococcus equi ATCC 33701 and 103. Infect Immun 68 (2000) 6840-6847
52. Bumann D. Examination of Salmonella gene expression in an infected mammalian host using the green fluorescent protein and two-colour flow cytometry. Mol Microbiol 43 (2002) 1269-1283
53. Xue Y., Lipscomb W.N., Graf R., Schnappauf G., and Braus G. The crystal structure of allosteric chorismate mutase at 2.2-Å resolution. Proc Natl Acad Sci U S A 91 (1994) 10814-10818
54. Strater N., Schnappauf G., Braus G., and Lipscomb W.N. Mechanisms of catalysis and allosteric regulation of yeast chorismate mutase from crystal structures. Structure 5 (1997) 1437-1452
55. Okvist M., Dey R., Sasso S., Grahn E., Kast P., and Krengel U. 1.6 Å crystal structure of the secreted chorismate mutase from Mycobacterium tuberculosis: novel fold topology revealed. J Mol Biol 357 (2006) 1483-1499
56. Crossgrove K., Laudet V., and Maina C.V. Dirofilaria immitis encodes Di-nhr-7, a putative orthologue of the Drosophila ecdysone-regulated E78 gene. Mol Biochem Parasitol 119 (2002) 169-177
57. Michael I.P., Kurlender L., Memari N., et al. Intron retention: a common splicing event within the human kallikrein gene family. Clin Chem 51 (2005) 506-515
58. Miyaso H., Okumura M., Kondo S., Higashide S., Miyajima H., and Imaizumi K. An intronic splicing enhancer element in survival motor neuron (SMN) pre-mRNA. J Biol Chem 278 (2003) 15825-15831
59. Lambert K.N., Bekal S., Domier L.L., Niblack T.L., Noel G.R., and Smyth C.A. Selection of Heterodera glycines chorismate mutase-1 alleles on nematode-resistant soybean. Mol Plant Microbe Interact 18 (2005) 593-601
60. Chavez-Gutierrez L., Bourdais J., Aranda G., et al. A truncated isoform of pyroglutamyl aminopeptidase II produced by exon extension has dominant-negative activity. J Neurochem 92 (2005) 807-817
61. 2 subunit of soluble guanylyl cyclase contains an insert homologous to a region within adenylyl cyclases and functions as a dominant negative protein. J Biol Chem 270 (1995) 21109-21113