Diversification of the insulin receptor family in the helminth parasite Schistosoma mansoni

FEBS Journal

Volumn 274, Issue 3, 2007, Pages 659-676

  Khayath, Naji ^a   Vicogne, Jerome ^a,b   Ahier, Arnaud ^a   BenYounes, Amena ^a   Konrad, Christian ^c   Trolet, Jacques ^a   Viscogliosi, Eric ^a   Brehm, Klaus ^c   Dissous, Colette ^a  

^a INSTITUT PASTEUR DE LILLE   (France)

^b STONY BROOK UNIVERSITY   (United States)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Evolution; Insulin receptor; Platyhelminth; Schistosoma mansoni

Indexed keywords

INSULIN RECEPTOR;

ANIMAL TISSUE; ARTICLE; DEVELOPMENTAL SCREENING; ECHINOCOCCUS MULTILOCULARIS; FEMALE; GENE FUNCTION; GENETIC VARIABILITY; INSULIN BINDING; INSULIN RELEASE; MALE; MOLECULAR CLONING; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; RECEPTOR AFFINITY; RECEPTOR INTRINSIC ACTIVITY; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; STRUCTURAL HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; BLOTTING, WESTERN; CLONING, MOLECULAR; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HELMINTH PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; PROTEIN ISOFORMS; RECEPTOR, INSULIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SCHISTOSOMA MANSONI; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; TWO-HYBRID SYSTEM TECHNIQUES;

ECHINOCOCCUS MULTILOCULARIS; INVERTEBRATA; METAZOA; PLATYHELMINTHES; SCHISTOSOMA MANSONI; TREMATODA; VERMES; VERTEBRATA;

EID: 33846413178     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2006.05610.x     Document Type: Article

References (53)

1. Shilo BZ & Raz E (1991) Developmental control by the Drosophila EGF receptor homolog DER. Trends Genet 7, 388-392.
2. Wiley LM, Adamson ED & Tsark EC (1995) Epidermal growth factor receptor function in early mammalian development. Bioessays 17, 839-846.
3. Conlon I & Raff M (1999) Size control in animal development. Cell 96, 235-244.
4. Singh AB & Harris RC (2005) Autocrine, paracrine and juxtacrine signaling by EGFR ligands. Cell Signal 17, 1183-1193.
5. Popovici C, Roubin R, Coulier F, Pontarotti P & Birnbaum D (1999) The family of Caenorhabditis elegans tyrosine kinase receptors: similarities and differences with mammalian receptors. Genome Res 9, 1026-1039.
6. Reidling JC, Miller MA & Steele RE (2000) Sweet Tooth, a novel receptor protein-tyrosine kinase with C-type lectin-like extracellular domains. J Biol Chem 275, 10323-10330.
7. Vicogne J, Pin JP, Lardans V, Capron M, Noel C & Dissous C (2003) An unusual receptor tyrosine kinase of Schistosoma mansoni contains a Venus Flytrap module. Mol Biochem Parasitol 126, 51-62.
8. Skorokhod A, Gamulin V, Gundacker D, Kavsan V, Muller IM & Muller WE (1999) Origin of insulin receptor-like tyrosine kinases in marine sponges. Biol Bull 197, 198-206.
9. Bravo DA, Gleason JB, Sanchez RI, Roth RA & Fuller RS (1994) Accurate and efficient cleavage of the human insulin proreceptor by the human proprotein-processing protease furin. Characterization and kinetic parameters using the purified, secreted soluble protease expressed by a recombinant baculovirus. J Biol Chem 269, 25830-25837.
10. Bass J, Turck C, Rouard M & Steiner DF (2000) Furin-mediated processing in the early secretory pathway: sequential cleavage and degradation of misfolded insulin receptors. Proc Natl Acad Sci USA 97, 11905-11909.
11. Gustafson TA, He W, Craparo A, Schaub CD & O'Neill TJ (1995) Phosphotyrosine-dependent interaction of SHC and insulin receptor substrate 1 with the NPEY motif of the insulin receptor via a novel non-SH2 domain. Mol Cell Biol 15, 2500-2508.
12. Leevers SJ (2001) Growth control: invertebrate insulin surprises. Curr Biol 11, R209-R212.
13. Kimura KD, Tissenbaum HA, Liu Y & Ruvkun G (1997) daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277, 942-946.
14. Roovers E, Vincent ME, van Kesteren E, Geraerts WP, Planta RJ, Vreugdenhil E & van Heerikhuizen H (1995) Characterization of a putative molluscan insulin-related peptide receptor. Gene 162, 181-188.
15. Pashmforoush M, Chan SJ & Steiner DF (1996) Structure and expression of the insulin-like peptide receptor from amphioxus. Mol Endocrinol 10, 857-866.
16. Leibush BN, Lappova YL, Bondareva VM, Chistyacova OV, Gutierrez J & Plisetskaya EM (1998) Insulin-family peptide-receptor interaction at the early stage of vertebrate evolution. Comp Biochem Physiol B Biochem Mol Biol 121, 57-63.
17. Kim JJ & Accili D (2002) Signalling through IGF-I and insulin receptors: where is the specificity? Growth Horm IGF Res 12, 84-90.
18. Khan AH & Pessin JE (2002) Insulin regulation of glucose uptake: a complex interplay of intracellular signalling pathways. Diabetologia 45, 1475-1483.
19. Kjeldsen T, Andersen AS, Wiberg FC, Rasmussen JS, Schaffer L, Balschmidt P, Moller KB & Moller NP (1991) The ligand specificities of the insulin receptor and the insulin-like growth factor I receptor reside in different regions of a common binding site. Proc Natl Acad Sci USA 88, 4404-4408.
20. Chan SJ, Cao QP & Steiner DF (1990) Evolution of the insulin superfamily: cloning of a hybrid insulin/insulin-like growth factor cDNA from amphioxus. Proc Natl Acad Sci USA 87, 9319-9323.
21. Konrad C, Kroner A, Spiliotis M, Zavala-Gongora R & Brehm K (2003) Identification and molecular characterisation of a gene encoding a member of the insulin receptor family in Echinococcus multilocularis. Int J Parasitol 33, 301-312.
22. Cornford E (1974) Effects of Insulin on Schistosomatium douthitti. Gen Comp Endocrinol 23, 286-293.
23. Levi-Schaffer F & Smolarsky M (1981) Schistosoma mansoni: effect of insulin and a low-molecular-weight fraction of serum on schistosomula in chemically defined media. Exp Parasitol 52, 378-385.
24. Skelly PJ & Shoemaker CB (1996) Rapid appearance and asymmetric distribution of glucose transporter SGTP4 at the apical surface of intramammalian-stage Schistosoma mansoni. Proc Natl Acad Sci USA 93, 3642-3646.
25. Sparrow LG, McKern NM, Gorman JJ, Strike PM, Robinson CP, Bentley JD & Ward CW (1997) The disulfide bonds in the C-terminal domains of the human insulin receptor ectodomain. J Biol Chem 272, 29460-29467.
26. Hanks SK & Hunter T (1995) Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 9, 576-596.
27. Seino S, Seino M, Nishi S & Bell GI (1989) Structure of the human insulin receptor gene and characterization of its promoter. Proc Natl Acad Sci USA 86, 114-118.
28. Abbott AM, Bueno R, Pedrini MT, Murray JM & Smith RJ (1992) Insulin-like growth factor I receptor gene structure. J Biol Chem 267, 10759-10763.
29. Ruan Y, Chen C, Cao Y & Garofalo RS (1995) The Drosophila insulin receptor contains a novel carboxyl-terminal extension likely to play an important role in signal transduction. J Biol Chem 270, 4236-4243.
30. Brehm K, Jensen K, Frosch P & Frosch M (1999) Characterization of the genomic locus expressing the ERM-like protein of Echinococcus multilocularis. Mol Biochem Parasitol 100, 147-152.
31. Khayath N, Mithieux G, Zitoun C, Coustau C, Vicogne J, Tielens AG & Dissous C (2006) Glyceroneogenesis: An unexpected metabolic pathway for glutamine in Schistosoma mansoni sporocysts. Mol Biochem Parasitol 147, 145-153.
32. Dissous C, Khayath N, Vicogne J & Capron M (2006) Growth factor receptors in helminth parasites: Signalling and host-parasite relationships. FEBS Lett 580, 2968-2975.
33. Elleman TC, Frenkel MJ, Hoyne PA, McKern NM, Cosgrove L, Hewish DR, Jachno KM, Bentley JD, Sankovich SE & Ward CW (2000) Mutational analysis of the N-linked glycosylation sites of the human insulin receptor. Biochem J 347 Part 3, 771-779.
34. Ahmed Z, Smith BJ, Kotani K, Wilden P & Pillay TS (1999) APS, an adapter protein with a PH and SH2 domain, is a substrate for the insulin receptor kinase. Biochem J 341, 665-668.
35. Zhu J & Kahn CR (1997) Analysis of a peptide hormone-receptor interaction in the yeast two-hybrid system. Proc Natl Acad Sci USA 94, 13063-13068.
36. Hao C, Whittaker L & Whittaker J (2006) Characterization of a second ligand binding site of the insulin receptor. Biochem Biophys Res Commun 347, 334-339.
37. Lou M, Garrett TP, McKern NM, Hoyne PA, Epa VC, Bentley JD, Lovrecz GO, Cosgrove LJ, Frenkel MJ & Ward CW (2006) The first three domains of the insulin receptor differ structurally from the insulin-like growth factor 1 receptor in the regions governing ligand specificity. Proc Natl Acad Sci USA 103, 12429-12434.
38. Fernandez-Almonacid R & Rosen OM (1987) Structure and ligand specificity of the Drosophila melanogaster insulin receptor. Mol Cell Biol 7, 2718-2727.
39. Steele RE, Lieu P, Mai NH, Shenk MA & Sarras MP (1996) Response to insulin and the expression pattern of a gene encoding an insulin receptor homologue suggest a role for an insulin-like molecule in regulating growth and patterning in Hydra. Dev Genes Evol 206, 247-259.
40. Jonas EA, Knox RJ, Kaczmarek LK, Schwartz JH & Solomon DH (1996) Insulin receptor in Aplysia neurons: characterization, molecular cloning, and modulation of ion currents. J Neurosci 16, 1645-1658.
41. Mynarcik DC, Williams PF, Schaffer L, Yu GQ & Whittaker J (1997) Identification of common ligand binding determinants of the insulin and insulin-like growth factor 1 receptors. Insights into mechanisms of ligand binding. J Biol Chem 272, 18650-18655.
42. Whittaker J & Whittaker L (2005) Characterization of the functional insulin binding epitopes of the full-length insulin receptor. J Biol Chem 280, 20932-20936.
43. Bueding E (1950) Carbohydrate metabolism of Schistosoma mansoni. J Gen Physiol 33, 475-495.
44. Dissous C & Capron A (1981) Isolation and characterization of surface antigens from Schistosoma mansoni schistosomula. Mol Biochem Parasitol 3, 215-225.
45. Schallig H, Sassen MJ & De Jong-Brink M (1990) A simplified medium for the in vitro culture of mother sporocysts of the schistosome Trichobilharzia ocellata. Parasitol Res 76, 278-279.
46. Chirgwin JM, Przybyla AE, MacDonald RJ & Rutter WJ (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18, 5294-5299.
47. Kumar S, Tamura K & Nei M (2004) MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5, 150-163.
48. Huelsenbeck JP & Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754-755.
49. Jones DT, Taylor WR & Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8, 275-282.
50. Abascal F, Zardoya R & Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104-2105.
51. Green PJ (1995) Reversible jump Markov chain Monte Carlo computation and Bayesian model determination. Biometrika 82, 711-732.
52. Livak KJ & Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) Method. Methods 25, 402-408.
53. Gounon P (1999) Low-temperature embedding in acrylic resins. Methods Mol Biol 117, 111-124.