Characterization of a truncated metabotropic glutamate receptor in a primitive metazoan, the parasitic flatworm schistosoma mansoni

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Taman, Amira ^a   Ribeiro, Paula ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; COMPLEMENTARY DNA; DIMER; METABOTROPIC RECEPTOR; MONOMER; SCHISTOSOMA MANSONI GLUTAMATE BINDING PROTEIN; SODIUM CHLORIDE; UNCLASSIFIED DRUG; UREA;

ARTICLE; BIOTINYLATION; CONTROLLED STUDY; ESCHERICHIA COLI; IMMUNOLOCALIZATION; MALE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SCHISTOSOMA MANSONI; WESTERN BLOTTING;

ANIMALS; BIOTINYLATION; BLOTTING, WESTERN; CELL MEMBRANE; CLONING, MOLECULAR; DNA, COMPLEMENTARY; FEMALE; GLUTAMIC ACID; HOST-PARASITE INTERACTIONS; IMMUNOGLOBULIN G; IMMUNOPRECIPITATION; MALE; PEPTIDE FRAGMENTS; PHYLOGENY; PROTEIN CONFORMATION; RABBITS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, METABOTROPIC GLUTAMATE; RNA, MESSENGER; SCHISTOSOMA MANSONI; SNAILS;

DIONAEA; METAZOA; PLATYHELMINTHES; SCHISTOSOMA; SCHISTOSOMA MANSONI;

EID: 84858250572     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027119     Document Type: Article

References (57)

1. Gryseels B, Polman K, Clerinx J, Kestens L, (2006) Human schistosomiasis. Lancet 368: 1106-1118.
2. Halton DW, Maule AG, (2004) Flatworm nerve-muscle: structural and functional analysis. Can J Zool 82: 316-333.
3. Ribeiro P, El-Shehabi F, Patocka N, (2005) Classical transmitters and their receptors in flatworms. Parasitol 131: S19-S40.
4. Ribeiro P, Geary T, (2010) Neuronal signaling in schistosomes: current status and prospects for post genomics. Can J Zool 88: 1-22.
5. Brownlee DJ, Fairweather I, (1996) Immunocytochemical localization of glutamate-like immunoreactivity within the nervous system of the cestode Mesocestoides corti and the trematode Fasciola hepatica. Parasitol Res 82: 423-427.
6. Keenan L, Koopowitz H, (1982) Physiology and in situ identification of putative aminergic neurotransmitters in the nervous system of Gyrocotyle fimbriata, a parasitic flatworm. J Neurobiol 13: 9-21.
7. Webb RA, Eklove H, (1989) Demonstration of intense glutamate-like immunoreactivity in the longitudinal nerve cords of the cestode Hymenolepis diminuta. Parasitol Res 75: 545-548.
8. Cebria F, Kudome T, Nakazawa M, Mineta K, Ikeo K, et al. (2002) The expression of neural-specific genes reveals the structural and molecular complexity of the planarian central nervous system. Mech Dev 116: 199-204.
9. Solis-Soto JM, De Jong Brink M, (1994) Immunocytochemical study on biologically active neurosubstances in daughter sporocysts and cercariae of Trichobilharzia ocellata and Schistosoma mansoni. Parasitol 108 (Pt 3): 301-311.
10. Miller CL, Day TA, Bennett JL, Pax RA, (1996) Schistosoma mansoni: L-glutamate-induced contractions in isolated muscle fibers; evidence for a glutamate transporter. Exp Parasitol 84: 410-419.
11. Thompson CS, Mettrick DF, (1989) The effects of 5-hydroxytryptamine and glutamate on muscle contraction in Hymenolepis diminuta (Cestoda). Can J Zool 67: 1257-1262.
12. Mendonça-Silva DL, Pessoa RF, Noel F, (2002) Evidence for the presence of glutamatergic receptors in adult Schistosoma mansoni. Biochem Pharmacol 64: 1337-1344.
13. Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, et al. (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460: 352-358.
14. The Schistosoma japonicum Genome Sequencing and Functional Analysis Consortium (2009) The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460: 345-351.
15. Kew JNC, Kemp JA, (2005) Ionotropic and metabotropic glutamate receptor structure and pharmacology. Psychopharmacol 179: 4-29.
16. Parmentier ML, Pin JP, Bockaert J, Grau Y, (1996) Cloning and Functional Expression of a Drosophila Metabotropic Glutamate Receptor Expressed in the Embryonic CNS. J Neurosc 16: 6687-6694.
17. Dillon J, Hopper NA, Holden-Dye L, O'Connor V, (2006) Molecular characterization of the metabotropic glutamate receptor family in Caenorhabditis elegans. Biochem Soc Trans 34: 942-948.
18. Mitri C, Parmentier ML, Pin JP, Bockaert J, Grau Y, (2004) Divergent evolution in metabotropic glutamate receptors. J Biol Chem 279: 9313-9320.
19. Hampson DR, Rose EM, Antflick JE, (2008) The structures of metabotropic glutamate receptors. In: The Receptors- The Glutamate Receptors. Gereau RW, Swanson GT, editors. Totowa, NJ Humana Press pp. 363-386.
20. O'Hara PJ, Sheppard PO, Thogersen H, Venezia D, Haldeman BA, et al. (1993) The ligand-binding domain in metabotropic glutamate receptors is related to bacterial periplasmic binding proteins. Neuron 11: 41-52.
21. Cao J, Huang S, Qian J, Huang J, Jin L, et al. (2009) Evolution of the class C GPCR Venus flytrap modules involved positive selected functional divergence. BMC Evol Biol 9: 67.
22. Pin JP, Acher F, (2002) The metabotropic glutamate receptors: structure, activation mechanism and pharmacology. Curr Drug Targets CNS Neurol Disord 1: 297-317.
23. Kniazeff J, Bessis AS, Maurel D, Ansanay H, Prezeau L, Pin JP, (2004) Closed state of both binding domains of homodimeric mGlu receptors is required for full activity. Nat Struct Mol Biol 11: 706-713.
24. Kammermeier PJ, Yun J, (2005) Activation of metabotropic glutamate receptor 1 dimers requires glutamate binding in both subunits. J Pharmacol Exp Ther 312: 502-508.
25. Taman A, Ribeiro P, (2011) Glutamate-mediated signaling in Schistosoma mansoni: A novel glutamate receptor is expressed in neurons and the female reproductive tract. Mol Biochem Parasitol 176: 42-50.
26. Robb SMC, Ross E, Sánchez AlvaradoA, (2007) SmedGD: the Schmidtea mediterranea Genome Database. Nucleic Acids Res 36: D599-D606.
27. Lewis F, (2001) Schistosomiasis. Curr Protoc Immunol 19.1.1-19.1.28.
28. El-Shehabi F, Vermeire JJ, Yoshino TP, Ribeiro P, (2009) Developmental expression analysis and immunolocalization of a biogenic amine receptor in Schistosoma mansoni. Exp Parasitol 122: 17-27.
29. Verjovski-Almeida S, DeMarco R, Martins EA, Guimaraes PE, Ojopi EP, et al. (2003) Transcriptome analysis of the acoelomate human parasite Schistosoma mansoni. Nat Genet 35: 148-157.
30. Taman A, Ribeiro P, (2009) Investigation of a dopamine receptor in Schistosoma mansoni: functional studies and immunolocalization. Mol Biochem Parasitol 168: 24-33.
31. Okamoto T, Schwab R, Scherer P, Lisanti M, (2001) Analysis of the association of proteins with membranes. Curr Protoc Cell Biol 5.4.1-5.4.17.
32. Nabhan JF, Ribeiro P, (2006) The 19 S proteasomal subunit POH1 contributes to the regulation of c-Jun ubiquitination, stability, and subcellular localization. J Biol Chem 281: 16099-16107.
33. Braschi S, Wilson RA, (2006) Proteins exposed at the adult schistosome surface revealed by biotinylation. Mol Cell Proteomics 5: 347-356.
34. 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.
35. Bernard A, Payton M, (2001) Selection of Escherichia coli expression systems. Curr Protoc Protein Sci 5.2.1-5.2.18.
36. Suzuki Y, Moriyoshi E, Tsuchiya D, Jingami H, (2004) Negative cooperativity of glutamate binding in the dimeric metabotropic glutamate receptor subtype 1. J Biol Chem 279: 35526-35534.
37. Pieper U, Eswar N, Webb BM, Eramian D, Kelly L, et al. (2009) MODBASE, a database of annotated comparative protein structure models and associated resources. Nucleic Acids Res 37: D347-54.
38. Muto T, Tsuchiya D, Morikawa K, Jingami H, (2007) Structures of the extracellular regions of the group II/III metabotropic glutamate receptors Proc Natl Acad Sci USA 104: 3759-3764.
39. Romano C, Yang WL, O'Malley KL, (1996) Metabotropic glutamate receptor 5 is a disulfide-linked dimer. J Biol Chem 271: 28612-28616.
40. Tsuji Y, Shimada Y, Takeshita T, Kajimura N, Nomura S, et al. (2000) Cryptic dimer interface and domain organization of the extracellular region of metabotropic glutamate receptor subtype 1. J Biol Chem 275: 28144-28151.
41. Ferraguti F, Shigemoto R, (2006) Metabotropic glutamate receptors. Cell Tissue Res 326: 483-504.
42. Sartorius LJ, Nagappan G, Lipska BK, Lu B, Sei Y, et al. (2006) Alternative splicing of human metabotropic glutamate receptor 3. J Neurochem 96: 1139-1148.
43. Tam R, Saier MH Jr, (1993) Structural, functional and evolutionary relationships among extracellular solute-binding receptors in bacteria. Microbiol Rev 57: 320-346.
44. Gilson E, Alloing G, Schmidt T, Claverys JP, Dudler R, Hofnung M, (1988) Evidence for high affinity binding-protein dependent transport systems in Gram-positive bacteria and in Mycoplasm. EMBO J 7: 3971-3974.
45. Felder CB, Graul RC, Lee AY, Merkle HP, Sadee W, (1999) The Venus Flytrap of Periplasmic Binding Proteins: An ancient protein module present in multiple drug receptors.AAPS PharmSci 1: article 2.
46. Romano C, Miller JK, Hyrc K, Dikranian S, Mennerick S, et al. (2001) Covalent and noncovalent interactions mediate metabotropic glutamate receptor mGlu5 dimerization. Mol Pharmacol 59: 46-53.
47. Okamoto T, Sekiyama N, Otsu M, Shimada Y, Sato A, et al. (1998) Expression and purification of the extracellular ligand binding region of metabotropic glutamate receptor subtype 1. J Biol Chem 273: 13089-13096.
48. Han G, Hampson DR, (1999) Ligand binding to the amino-terminal domain of the mGluR4 subtype of metabotropic glutamate receptor. J Biol Chem 274: 10008-10013.
49. Fitzpatrick JM, Peak E, Perally S, Chalmers IW, Barrett B, et al. (2009) Anti-schistosomal intervention targets identified by lifecycle transcriptomic analyses. PLoS Negl Trop Dis 3 (11): e543.
50. Gustafsson MKS, (1987) Immunocytochemical demonstration of neuropeptides and serotonin in the nervous system of adult Schistosoma mansoni. Parasitol Res 74: 168-174.
51. Kohn AB, Moroz LL, LEA JM, Greenberg RM, (2001) Distribution of nitric oxide synthase immunoreactivity in the nervous system and peripheral tissues of Schistosoma mansoni. Parasitol 122: 87-92.
52. Mair GR, Niciu MJ, Stewart MT, Brennan G, Omar H, et al. (2004) A functionally atypical amidating enzyme from the human parasite Schistosoma mansoni. FASEB J 18: 114-121.
53. Bentley GN, Jones AK, Parra WGO, Agnew A, (2004) ShAR1 alpha and ShAR1 beta: novel putative nicotinic acetylcholine receptor subunits from the platyhelminth blood fluke Schistosoma. Gene 329: 27-38.
54. Beqollari D, Kammermeier PJ, (2010) Venus flytrap domain of mGluR1 functions as a dominant negative against Group I mGluR signaling. J Neurophysiol 104: 439-448.
55. Halton DW, (2004) Microscopy and the helminth parasite. Micron 35: 361-390.
56. Forrester SG, Warfel PW, Pearce EJ, (2004) Tegumental expression of a novel type II receptor serine/threonine kinase (SmRK2) in Schistosoma mansoni. Mol Biochem Parasitol 136: 149-156.
57. Waisberg M, Lobo FP, Cerqueira GC, Passos LK, Carvalho OS, et al. (2007) Microarray analysis of gene expression induced by sexual contact in Schistosoma mansoni. BMC Genomics 8: 181.