Toward Understanding the Functional Role of Ss-riok-1, a RIO Protein Kinase-Encoding Gene of Strongyloides stercoralis

PLoS Neglected Tropical Diseases

Volumn 8, Issue 8, 2014, Pages

  Yuan, Wang ^a   Lok, James B ^b   Stoltzfus, Jonathan D ^b   Gasser, Robin B ^c   Fang, Fang ^a   Lei, Wei Qiang ^a   Fang, Rui ^a   Zhou, Yan Qin ^a   Zhao, Jun Long ^a   Hu, Min ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; MEMBRANE PROTEIN; SS RIOK 1 GENE ENCODING PROTEIN; UNCLASSIFIED DRUG; PROTEIN SERINE THREONINE KINASE;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ADULT; AFFINITY CHROMATOGRAPHY; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DNA EXTRACTION; DNA ISOLATION; DNA STRUCTURE; DNA TRANSCRIPTION; E BOX ELEMENT; ENZYME ASSAY; EXON; FEMALE; GATA BOX; GENE; GENE SEQUENCE; GENETIC TRANSFORMATION; HAEMONCHUS CONTORTUS; INTRON; LARVA; NONHUMAN; OPEN READING FRAME; ORTHOLOGY; PHYLOGENY; POLYMERASE CHAIN REACTION; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; SS RIOK 1 GENE; STRONGYLOIDES STERCORALIS; TATA BOX; ANIMAL; DOG; ENZYMOLOGY; GENETIC TRANSCRIPTION; GENETICS; HUMAN; PHYSIOLOGY;

ANIMALS; DOGS; HUMANS; PROMOTER REGIONS, GENETIC; PROTEIN-SERINE-THREONINE KINASES; STRONGYLOIDES STERCORALIS; TRANSCRIPTION, GENETIC;

EID: 84955612553     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003062     Document Type: Article

References (86)

1. Igra-Siegman Y, Kapila R, Sen P, Kaminski ZC, Louria DB, (1981) Syndrome of hyperinfection with Strongyloides stercoralis. Rev Infect Dis 3: 397–407.
2. Viney ME, Lok JB, (2007) Strongyloides spp. WormBook 10.1895/wormbook.1.141.1: 1–15.
3. Schad G, (1989) Morphology and life history of Strongyloides stercoralis. Strongyloidiasis: a major roundworm infection of man. Philadelphia: Taylor & Francis 85–104.
4. Hanks SK, Quinn AM, Hunter T, (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241: 42–52.
5. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S, (2002) The protein kinase complement of the human genome. Science 298: 1912–1934.
6. LaRonde-LeBlanc N, Wlodawer A, (2005) The RIO kinases: an atypical protein kinase family required for ribosome biogenesis and cell cycle progression. Biochim Biophys Acta 1754: 14–24.
7. LaRonde-LeBlanc N, Wlodawer A, (2005) A family portrait of the RIO kinases. J Biol Chem 280: 37297–37300.
8. Vanrobays E, Gleizes PE, Bousquet-Antonelli C, Noaillac-Depeyre J, Caizergues-Ferrer M, et al. (2001) Processing of 20S pre-rRNA to 18S ribosomal RNA in yeast requires Rrp10p, an essential non-ribosomal cytoplasmic protein. EMBO J 20: 4204–4213.
9. Angermayr M, Roidl A, Bandlow W, (2002) Yeast Rio1p is the founding member of a novel subfamily of protein serine kinases involved in the control of cell cycle progression. Mol Microbiol 44: 309–324.
10. Vanrobays E, Gelugne JP, Gleizes PE, Caizergues-Ferrer M, (2003) Late cytoplasmic maturation of the small ribosomal subunit requires RIO proteins in Saccharomyces cerevisiae. Mol Cell Biol 23: 2083–2095.
11. Widmann B, Wandrey F, Badertscher L, Wyler E, Pfannstiel J, et al. (2012) The kinase activity of human Rio1 is required for final steps of cytoplasmic maturation of 40S subunits. Mol Biol Cell 23: 22–35.
12. Manning G, (2005) Genomic overview of protein kinases. WormBook 10.1895/wormbook.1.60.1: 1–19.
13. Fraser AG, Kamath RS, Zipperlen P, Martinez-Campos M, Sohrmann M, et al. (2000) Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408: 325–330.
14. Ashrafi K, Chang FY, Watts JL, Fraser AG, Kamath RS, et al. (2003) Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 421: 268–272.
15. Simmer F, Moorman C, van der Linden AM, Kuijk E, van den Berghe PV, et al. (2003) Genome-wide RNAi of C. elegans using the hypersensitive rrf-3 strain reveals novel gene functions. PLoS Biol 1: E12.
16. Rual JF, Ceron J, Koreth J, Hao T, Nicot AS, et al. (2004) Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res 14: 2162–2168.
17. Sonnichsen B, Koski LB, Walsh A, Marschall P, Neumann B, et al. (2005) Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434: 462–469.
18. Hu M, Laronde-Leblanc N, Sternberg PW, Gasser RB, (2008) Tv-RIO1 - an atypical protein kinase from the parasitic nematode Trichostrongylus vitrinus. Parasit Vectors 1: 34.
19. Campbell BE, Boag PR, Hofmann A, Cantacessi C, Wang CK, et al. (2011) Atypical (RIO) protein kinases from Haemonchus contortus–promise as new targets for nematocidal drugs. Biotechnol Adv 29: 338–350.
20. Mello C, Fire A, (1995) DNA transformation. Methods Cell Biol 48: 451–482.
21. Lok JB, Massey HC, Jr (2002) Transgene expression in Strongyloides stercoralis following gonadal microinjection of DNA constructs. Mol Biochem Parasitol 119: 279–284.
22. Li X, Massey HC, JrNolan TJ, Schad GA, Kraus K, et al. (2006) Successful transgenesis of the parasitic nematode Strongyloides stercoralis requires endogenous non-coding control elements. Int J Parasitol 36: 671–679.
23. Castelletto ML, Massey HC, JrLok JB, (2009) Morphogenesis of Strongyloides stercoralis infective larvae requires the DAF-16 ortholog FKTF-1. PLoS Pathog 5: e1000370.
24. Lok JB, (2007) Strongyloides stercoralis: a model for translational research on parasitic nematode biology. WormBook 10.1895/wormbook.1.134.1: 1–18.
25. Schad GA, Hellman ME, Muncey DW, (1984) Strongyloides stercoralis: hyperinfection in immunosuppressed dogs. Exp Parasitol 57: 287–296.
26. Bowman DD, Lynn RC (1995) Georgi's Parasitology for Veterinarians. WB Saunders Company. Saint Louis, Missouri, U.S.A.: W B Saunders Co.
27. Hawdon J, Schad G, (1991) Long term storage of hookworm infective larvae in buffered saline solution maintains larval responsiveness to host signals. J Helm Soc Wash 58: 140–142.
28. Gasser RB, Chilton NB, Hoste H, Beveridge I, (1993) Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Res 21: 2525–2526.
29. Junio AB, Li X, Massey HC, JrNolan TJ, Todd Lamitina S, et al. (2008) Strongyloides stercoralis: cell- and tissue-specific transgene expression and co-transformation with vector constructs incorporating a common multifunctional 3′ UTR. Exp Parasitol 118: 253–265.
30. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402.
31. Bairoch A, (1993) The PROSITE dictionary of sites and patterns in proteins, its current status. Nucleic Acids Res 21: 3097–3103.
32. Bateman A, Birney E, Durbin R, Eddy SR, Howe KL, et al. (2000) The Pfam protein families database. Nucleic Acids Res 28: 263–266.
33. Katoh K, Standley DM, (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772–780.
34. Deyneko IV, Kel AE, Kel-Margoulis OV, Deineko EV, Wingender E, et al. (2013) MatrixCatch–a novel tool for the recognition of composite regulatory elements in promoters. BMC Bioinformatics 14: 241.
35. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948.
36. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739.
37. Stoltzfus JD, Massey HC, JrNolan TJ, Griffith SD, Lok JB, (2012) Strongyloides stercoralis age-1: a potential regulator of infective larval development in a parasitic nematode. PLoS One 7: e38587.
38. Nolan TJ, Megyeri Z, Bhopale VM, Schad GA, (1993) Strongyloides stercoralis: the first rodent model for uncomplicated and hyperinfective strongyloidiasis, the Mongolian gerbil (Meriones unguiculatus). J Infect Dis 168: 1479–1484.
39. Stoltzfus JD, Minot S, Berriman M, Nolan TJ, Lok JB, (2012) RNAseq analysis of the parasitic nematode Strongyloides stercoralis reveals divergent regulation of canonical dauer pathways. PLoS Negl Trop Dis 6: e1854.
40. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, et al. (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14: R36.
41. Langmead B, Salzberg SL, (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357–359.
42. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621–628.
43. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, et al. (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7: 562–578.
44. Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, et al. (2013) Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 31: 46–53.
45. Liu T, Deng M, Li J, Tong X, Wei Q, et al. (2011) Phosphorylation of right open reading frame 2 (Rio2) protein kinase by polo-like kinase 1 regulates mitotic progression. J Biol Chem 286: 36352–36360.
46. LaRonde-LeBlanc N, Guszczynski T, Copeland T, Wlodawer A, (2005) Structure and activity of the atypical serine kinase Rio1. FEBS J 272: 3698–3713.
47. Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P, et al. (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392: 71–75.
48. Blumenthal T, Steward K (1997) RNA Processing and Gene Structure. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR, editors. C. elegans II. 2nd ed. Cold Spring Harbor (NY).
49. Angermayr M, Bandlow W, (2002) RIO1, an extraordinary novel protein kinase. FEBS Lett 524: 31–36.
50. White JG, Southgate E, Thomson JN, Brenner S, (1976) The structure of the ventral nerve cord of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 275: 327–348.
51. White JG, Southgate E, Thomson JN, Brenner S, (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314: 1–340.
52. LaRonde-LeBlanc N, Wlodawer A, (2004) Crystal structure of A. fulgidus Rio2 defines a new family of serine protein kinases. Structure 12: 1585–1594.
53. Meharena HS, Chang P, Keshwani MM, Oruganty K, Nene AK, et al. (2013) Deciphering the structural basis of eukaryotic protein kinase regulation. PLoS Biol 11: e1001680.
54. Guderian G, Peter C, Wiesner J, Sickmann A, Schulze-Osthoff K, et al. (2011) RioK1, a new interactor of protein arginine methyltransferase 5 (PRMT5), competes with pICln for binding and modulates PRMT5 complex composition and substrate specificity. J Biol Chem 286: 1976–1986.
55. Ginisty H, Amalric F, Bouvet P, (1998) Nucleolin functions in the first step of ribosomal RNA processing. EMBO J 17: 1476–1486.
56. Allain FH, Bouvet P, Dieckmann T, Feigon J, (2000) Molecular basis of sequence-specific recognition of pre-ribosomal RNA by nucleolin. EMBO J 19: 6870–6881.
57. Ginisty H, Serin G, Ghisolfi-Nieto L, Roger B, Libante V, et al. (2000) Interaction of nucleolin with an evolutionarily conserved pre-ribosomal RNA sequence is required for the assembly of the primary processing complex. J Biol Chem 275: 18845–18850.
58. Raman B, Guarnaccia C, Nadassy K, Zakhariev S, Pintar A, et al. (2001) N(omega)-arginine dimethylation modulates the interaction between a Gly/Arg-rich peptide from human nucleolin and nucleic acids. Nucleic Acids Res 29: 3377–3384.
59. Angermayr M, Hochleitner E, Lottspeich F, Bandlow W, (2007) Protein kinase CK2 activates the atypical Rio1p kinase and promotes its cell-cycle phase-dependent degradation in yeast. FEBS J 274: 4654–4667.
60. Massey HC, JrNishi M, Chaudhary K, Pakpour N, Lok JB, (2003) Structure and developmental expression of Strongyloides stercoralis fktf-1, a proposed ortholog of daf-16 in Caenorhabditis elegans. Int J Parasitol 33: 1537–1544.
61. Massey HC, JrRanjit N, Stoltzfus JD, Lok JB, (2013) Strongyloides stercoralis daf-2 encodes a divergent ortholog of Caenorhabditis elegans DAF-2. Int J Parasitol 43: 515–520.
62. Bucher P, (1990) Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J Mol Biol 212: 563–578.
63. Lowry JA, Atchley WR, (2000) Molecular evolution of the GATA family of transcription factors: conservation within the DNA-binding domain. J Mol Evol 50: 103–115.
64. LaVoie HA, (2003) The role of GATA in mammalian reproduction. Exp Biol Med (Maywood) 228: 1282–1290.
65. Pikkarainen S, Tokola H, Kerkela R, Ruskoaho H, (2004) GATA transcription factors in the developing and adult heart. Cardiovasc Res 63: 196–207.
66. Bresnick EH, Martowicz ML, Pal S, Johnson KD, (2005) Developmental control via GATA factor interplay at chromatin domains. J Cell Physiol 205: 1–9.
67. Murakami R, Okumura T, Uchiyama H, (2005) GATA factors as key regulatory molecules in the development of Drosophila endoderm. Dev Growth Differ 47: 581–589.
68. Atchley WR, Fitch WM, (1997) A natural classification of the basic helix-loop-helix class of transcription factors. Proc Natl Acad Sci U S A 94: 5172–5176.
69. Massari ME, Murre C, (2000) Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol 20: 429–440.
70. Kageyama R, Ohtsuka T, Hatakeyama J, Ohsawa R, (2005) Roles of bHLH genes in neural stem cell differentiation. Exp Cell Res 306: 343–348.
71. Zhao J, Wang P, Corsi AK, (2007) The C. elegans Twist target gene, arg-1, is regulated by distinct E box promoter elements. Mech Dev 124: 377–389.
72. McMiller TL, Johnson CM, (2005) Molecular characterization of HLH-17, a C. elegans bHLH protein required for normal larval development. Gene 356: 1–10.
73. Britton C, Redmond DL, Knox DP, McKerrow JH, Barry JD, (1999) Identification of promoter elements of parasite nematode genes in transgenic Caenorhabditis elegans. Mol Biochem Parasitol 103: 171–181.
74. Levin M, Hashimshony T, Wagner F, Yanai I, (2012) Developmental milestones punctuate gene expression in the Caenorhabditis embryo. Dev Cell 22: 1101–1108.
75. Ashton FT, Bhopale VM, Fine AE, Schad GA, (1995) Sensory neuroanatomy of a skin-penetrating nematode parasite: Strongyloides stercoralis. I. Amphidial neurons. J Comp Neurol 357: 281–295.
76. Fine AE, Ashton FT, Bhopale VM, Schad GA, (1997) Sensory neuroanatomy of a skin-penetrating nematode parasite Strongyloides stercoralis. II. Labial and cephalic neurons. J Comp Neurol 389: 212–223.
77. Ward S, Thomson N, White JG, Brenner S, (1975) Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J Comp Neurol 160: 313–337.
78. Sulston JE, Horvitz HR, (1977) Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 56: 110–156.
79. Sulston JE, Schierenberg E, White JG, Thomson JN, (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100: 64–119.
80. Steward O, Reeves TM, (1988) Protein-synthetic machinery beneath postsynaptic sites on CNS neurons: association between polyribosomes and other organelles at the synaptic site. J Neurosci 8: 176–184.
81. Steward O, (1983) Polyribosomes at the base of dendritic spines of central nervous system neurons–their possible role in synapse construction and modification. Cold Spring Harb Symp Quant Biol 48 Pt 2: 745–759.
82. Steward O, Falk PM, (1985) Polyribosomes under developing spine synapses: growth specializations of dendrites at sites of synaptogenesis. J Neurosci Res 13: 75–88.
83. Steward O, Falk PM, (1986) Protein-synthetic machinery at postsynaptic sites during synaptogenesis: a quantitative study of the association between polyribosomes and developing synapses. J Neurosci 6: 412–423.
84. Garriga G, Desai C, Horvitz HR, (1993) Cell interactions control the direction of outgrowth, branching and fasciculation of the HSN axons of Caenorhabditis elegans. Development 117: 1071–1087.
85. White JG, Southgate E, Thomson JN, Brenner S, (1983) Factors that determine connectivity in the nervous system of Caenorhabditis elegans. Cold Spring Harb Symp Quant Biol 48 Pt 2: 633–640.
86. Steward O, Davis L, Dotti C, Phillips LL, Rao A, et al. (1988) Protein synthesis and processing in cytoplasmic microdomains beneath postsynaptic sites on CNS neurons. A mechanism for establishing and maintaining a mosaic postsynaptic receptive surface. Mol Neurobiol 2: 227–261.