Molecular cloning and DNA binding characterization of DAF-16 orthologs from Ancylostoma hookworms

International Journal for Parasitology

Volumn 39, Issue 4, 2009, Pages 407-415

  Gao, Xin ^a   Frank, Daniel ^a   Hawdon, John M ^a  

^a GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Ancylostoma caninum; Dauer; Forkhead; Hookworm; Insulin signaling; Transition to parasitism

Indexed keywords

CLONE; GENE EXPRESSION; HOST SPECIFICITY; MOLECULAR ANALYSIS; NEMATODE; SIGNALING;

AMINO ACID SEQUENCE; ANCYLOSTOMA; ANIMALS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CLONING, MOLECULAR; FORKHEAD TRANSCRIPTION FACTORS; GENES, REPORTER; MOLECULAR SEQUENCE DATA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 58849167647     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2008.09.005     Document Type: Article

References (62)

1. Alessi D.R., Barry Caudwell F., Andjelkovic M., Hemmings B.A., and Cohen P. Molecular basis for the substrate specificity of protein kinase B; comparison with MAPKAP kinase-1 and p70 S6 kinase. FEBS Lett. 399 (1996) 333-338
2. Alessi D.R. Discovery of PDK1, one of the missing links in insulin signal transduction. Colworth Medal Lecture. Biochem. Soc. Trans. 29 (2001) 1-14
3. Altschul S.F., Gish W., Miller W., Myers E.W., and Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215 (1990) 403-410
4. Altschul S.F., Madden T.L., Schaeffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
5. Bektesh S., Van Doren K., and Hirsh D. Presence of the Caenorhabditis elegans spliced leader on different mRNAs and in different genera of nematodes. Genes Dev. 2 (1988) 1277-1283
6. Bektesh S.L., and Hirsh D.I. C. elegans mRNAs acquire a spliced leader through a trans-splicing mechanism. Nucleic Acids Res. 16 (1988) 5692
7. Bendtsen J.D., Nielsen H., von Heijne G., and Brunak S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340 (2004) 783-795
8. Bethony J., Chen J., Lin S., Xiao S., Zhan B., Li S., Xue H., Xing F., Humphries D., Yan W., Chen G., Foster V., Hawdon J.M., and Hotez P.J. Emerging patterns of hookworm infection: influence of aging on the intensity of Necator infection in Hainan Province, People's Republic of China. Clin. Infect. Dis. 35 (2002) 1336-1344
9. Bethony J., Brooker S., Albonico M., Geiger S.M., Loukas A., Diemert D., and Hotez P.J. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367 (2006) 1521-1532
10. Bird D.M., and Riddle D.L. A genetic nomenclature for parasitic nematodes. J. Nematol. 26 (1994) 138-143
11. Blumenthal T., and Steward K. RNA processing and gene structure. In: Riddle D.L., Blumenthal T., Meyer B.J., and Priess J.R. (Eds). C. elegans II, Cold Spring Harbor Monograph Series Vol. 33 (1997), Cold Spring Harbor Laboratory Press, Plainview, New York, USA 117-145
12. Brand A., and Hawdon J.M. Phosphoinositide-3-OH-kinase inhibitor LY294002 prevents activation of Ancylostoma caninum and Ancylostoma ceylanicum third-stage infective larvae. Int. J. Parasitol. 34 (2004) 909-914
13. Brownawell A.M., Kops G.J., Macara I.G., and Burgering B.M. Inhibition of nuclear import by protein kinase B (Akt) regulates the subcellular distribution and activity of the forkhead transcription factor AFX. Mol. Cell. Biol. 21 (2001) 3534-3546
14. Brunet A., Bonni A., Zigmond M.J., Lin M.Z., Juo P., Hu L.S., Anderson M.J., Arden K.C., Blenis J., and Greenberg M.E. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96 (1999) 857-868
15. Bundy D.A.P., Chan M.S., and Savioli L. Hookworm infection in pregnancy. Trans. R. Soc. Trop. Med. Hyg. 89 (1995) 521-522
16. Cahill C.M., Tzivion G., Nasrin N., Ogg S., Dore J., Ruvkun G., and Alexander-Bridges M. Phosphatidylinositol 3-kinase signaling inhibits DAF-16 DNA binding and function via 14-3-3-dependent and 14-3-3-independent pathways. J. Biol. Chem. 276 (2001) 13402-13410
17. Cassada R.C., and Russell R.L. The dauer larva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Dev. Biol. 46 (1975) 326-342
18. Dreyfuss M.L., Stoltzfus R.J., Shrestha J.B., Pradhan E.K., LeClerq S.C., Khatry S.K., Shrestha S.R., Katz J., Albonico M., and West Jr. K.P. Hookworms, malaria and vitamin A deficiency contribute to anemia and iron deficiency among pregnant women in the plains of Nepal. J. Nutr. 130 (2000) 2527-2536
19. Estevez A.O., Cowie R.H., Gardner K.L., and Estevez M. Both insulin and calcium channel signaling are required for developmental regulation of serotonin synthesis in the chemosensory ADF neurons of Caenorhabditis elegans. Dev. Biol. 298 (2006) 32-44
20. Furuyama T., Nakazawa T., Nakano I., and Mori N. Identification of the differential distribution patterns of mRNAs and consensus binding sequences for mouse DAF-16 homologues. Biochem. J. 349 (2000) 629-634
21. Garside P., and Behnke J.M. Ancylostoma ceylanicum in the hamster: observations on the host-parasite relationship during primary infection. Parasitology 98 (1989) 283-289
22. Gottlieb S., and Ruvkun G. Daf-2, daf-16 and daf-23: genetically interacting genes controlling Dauer formation in Caenorhabditis elegans. Genetics 137 (1994) 107-120
23. Hacker U., Grossniklaus U., Gehring W., and Jackle H. Developmentally regulated Drosophila gene family encoding the fork head domain. PNAS 89 (1992) 8754-8758
24. Hajarnavis A., Korf I., and Durbin R. A probabilistic model of 3' end formation in Caenorhabditis elegans. Nucleic Acids Res. 32 (2004) 3392-3399
25. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 41 (1999) 95-98
26. Hawdon J.M., and Schad G.A. Serum stimulated feeding in vitro by third stage infective larvae of the canine hookworm Ancylostoma caninum. J. Parasitol. 76 (1990) 394-398
27. Hawdon J.M., and Schad G.A. Developmental Adaptations in Nematodes. In: Toft C.A., Aeschlimann A., and Bolis L. (Eds). Parasitism: Coexistence or Conflict? (1991), Oxford University Press, Oxford 274-298
28. Hawdon J.M., and Schad G.A. Long-term storage of hookworm infective larvae in buffered saline solution maintains larval responsiveness to host signals. J. Helm. Soc. Wash. 58 (1991) 140-142
29. Hawdon J.M., Jones B.F., and Hotez P.J. Cloning and characterization of a cDNA encoding the catalytic subunit of a cAMP-dependent protein kinase from Ancylostoma caninum third-stage infective larvae. Mol. Biochem. Parasitol. 69 (1995) 127-130
30. Hawdon J.M., Jones B.F., Perregaux M.A., and Hotez P.J. Ancylostoma caninum: metalloprotease release coincides with activation of infective larvae in vitro. Exp. Parasitol. 80 (1995) 205-211
31. Hawdon J.M., and Hotez P.J. Hookworm: developmental biology of the infectious process. Curr. Opin. Gen. Dev. 6 (1996) 618-623
32. Hawdon J.M., Jones B.F., Hoffman D.R., and Hotez P.J. Cloning and characterization of Ancylostoma-secreted protein. A novel protein associated with the transition to parasitism by infective hookworm larvae. J. Biol. Chem. 271 (1996) 6672-6678
33. Hawdon J.M., Narasimhan S., and Hotez P.J. Ancylostoma secreted protein 2: cloning and characterization of a second member of a family of nematode secreted proteins from Ancylostoma caninum. Mol. Biochem. Parasitol. 99 (1999) 149-165
34. Hawdon J.M., and Datu B. The second messenger cyclic GMP mediates activation in Ancylostoma caninum infective larvae. Int. J. Parasitol. 33 (2003) 787-793
35. Hawdon J.M., Datu B., and Crowell M. Molecular cloning of a novel multidomain Kunitz-type proteinase inhibitor from the hookworm Ancylostoma caninum. J. Parasitol. 89 (2003) 402-407
36. Henderson S.T., and Johnson T.E. Daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr. Biol. 11 (2001) 1975-1980
37. Hotez P.J., Hawdon J.M., and Schad G.A. Hookworm larval infectivity, arrest, and amphiparatenesis: the Caenorhabditis elegans daf-c paradigm. Parasitol. Today 9 (1993) 23-26
38. Kimura K.D., Tissenbaum H.A., Liu Y., and Ruvkun G. Daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277 (1997) 942-946
39. Kumar S., Tamura K., and Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5 (2004) 150-163
40. la Cour T., Kiemer L., Molgaard A., Gupta R., Skriver K., and Brunak S. Analysis and prediction of leucine-rich nuclear export signals. Protein Eng. Des. Sel. 17 (2004) 527-536
41. Lee R.Y., Hench J., and Ruvkun G. Regulation of C. elegans DAF-16 and its human ortholog FKHRL1 by the daf-2 insulin-like signaling pathway. Curr. Biol. 11 (2001) 1950-1957
42. Li J., Tewari M., Vidal M., and Lee S.S. The 14-3-3 protein FTT-2 regulates DAF-16 in Caenorhabditis elegans. Dev. Biol. 301 (2007) 82-91
43. Lin K., Dorman J.B., Rodan A., and Kenyon C. Daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278 (1997) 1319-1322
44. Lozoff B., Jimenez E., and Wolf A.W. Long-term developmental outcome of infants with iron deficiency. N. Engl. J. Med. 235 (1991) 687-694
45. Massey Jr. H.C., Nishi M., Chaudhary K., Pakpour N., and Lok J.B. Structure and developmental expression of Strongyloides stercoralis fktf-1, a proposed ortholog of daf-16 in Caenorhabditis elegans. Int. J. Parasitol. 33 (2003) 1537-1544
46. Massey J.H.C., Bhopale M.K., Li X., Castelletto M., and Lok J.B. The fork head transcription factor FKTF-1b from Strongyloides stercoralis restores DAF-16 developmental function to mutant Caenorhabditis elegans. Int. J. Parasitol. 36 (2006) 347-352
47. Mitreva M., McCarter J.P., Arasu P., Hawdon J., Martin J., Dante M., Wylie T., Xu J., Stajich J.E., Kapulkin W., Clifton S.W., Waterston R.H., and Wilson R.K. Investigating hookworm genomes by comparative analysis of two Ancylostoma species. BMC Genomics 6 (2005) 58
48. Morris J.Z., Tissenbaum H.A., and Ruvkun G. A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 382 (1996) 536-539
49. Muslin A.J., Tanner J.W., Allen P.M., and Shaw A.S. Interaction of 14-3-3 with signaling proteins Is mediated by the recognition of phosphoserine. Cell 84 (1996) 889-897
50. Nolan T.J., Bhopale V., Megyeri Z., and Schad G.A. Cryopreservation of human hookworms. J. Parasitol. 80 (1994) 648-650
51. Obenauer J.C., Cantley L.C., and Yaffe M.B. Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31 (2003) 3635-3641
52. Ogg S., Paradis S., Gottlieb S., Patterson G.I., Lee L., Tissenbaum H.A., and Ruvkun G. The fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389 (1997) 994-999
53. Ogg S., and Ruvkun G. The C. elegans PTEN homolog, DAF-18, acts in the insulin receptor-like metabolic signaling pathway. Mol. Cell. 2 (1998) 887-893
54. Paradis S., and Ruvkun G. Caenorhabditis elegans Akt/PKB transduces insulin receptor-like signals from AGE-1 PI3 kinase to the DAF-16 transcription factor. Genes Dev. 12 (1998) 2488-2498
55. Paradis S., Ailion M., Toker A., Thomas J.H., and Ruvkun G. A PDK1 homolog is necessary and sufficient to transduce AGE-1 PI3 kinase signals that regulate diapause in Caenorhabditis elegans. Genes Dev. 13 (1999) 1438-1452
56. Rogers W.P., and Sommerville R.I. The infective stage of nematode parasites and its significance in parasitism. Adv. Parasitol. 1 (1963) 109-177
57. Rogers W.P., and Petronijevic T. The infective stage and the development of nematodes. In: Symons L.E.A., Donald A.D., and Dineen J.K. (Eds). Biology and Control of Endoparasites (1982), Academic Press, Australia 3-28
58. Schad G.A., and Page M.R. Ancylostoma caninum: adult worm removal, corticosteroid treatment, and resumed development of arrested larvae in dogs. Exp. Parasitol. 54 (1982) 303-309
59. Sulston J., and Hodgkin J. Methods. In: Wood W.B. (Ed). The Nematode Caenorhabditis elegans (1988), Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 587-606
60. Tissenbaum H.A., Hawdon J., Perregaux M., Hotez P., Guarente L., and Ruvkun G. A common muscarinic pathway for diapause recovery in the distantly related nematode species Caenorhabditis elegans and Ancylostoma caninum. Proc. Natl. Acad. Sci. USA 97 (2000) 460-465
61. Van Der Heide L.P., Hoekman M.F., and Smidt M.P. The ins and outs of FoxO shuttling: mechanisms of FoxO translocation and transcriptional regulation. Biochem. J. 380 (2004) 297-309
62. Vlahos C., Matter W., Hui K., and Brown R. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269 (1994) 5241-5248