The formin-homology protein SmDia interacts with the Src kinase SmTK and the GTPase SmRho1 in the gonads of Schistosoma mansoni

PLoS ONE

Volumn 4, Issue 9, 2009, Pages

  Quack, Thomas ^a   Knobloch, Jürgen ^b,e   Beckmann, Svenja ^a   Vicogne, Jérome ^c   Dissous, Colette ^d   Grevelding, Christoph G ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c INSTITUT DE BIOLOGIE DE LILLE   (France)

^d UNIV LILLE   (France)

^e UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DIAPHANOUS RELATED FORMIN; METHENAMINE; MICROORGANISM PROTEIN; PROTEIN KINASE FER; PROTEIN SH3; RHO FACTOR; RHO1 FACTOR; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; CARRIER PROTEIN; FETOPROTEIN; FORMIN 1; GUANOSINE TRIPHOSPHATASE; NUCLEAR PROTEIN; PROTEIN TYROSINE KINASE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; DNA LIBRARY; FEMALE; GENETIC TRANSCRIPTION; GONAD; IN SITU HYBRIDIZATION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; SCHISTOSOMA MANSONI; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN; STRUCTURAL HOMOLOGY; TWO HYBRID SYSTEM; ANIMAL; CHEMISTRY; CYTOSKELETON; ENZYMOLOGY; GENE EXPRESSION REGULATION; METABOLISM; MOLECULAR CLONING; OPEN READING FRAME; PROTEIN TERTIARY STRUCTURE;

ANIMALIA; EUKARYOTA; SCHISTOSOMA; SCHISTOSOMA MANSONI;

ANIMALS; BINDING SITES; CARRIER PROTEINS; CLONING, MOLECULAR; CYTOSKELETON; FEMALE; FETAL PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GONADS; GTP PHOSPHOHYDROLASES; MALE; MICROFILAMENT PROTEINS; NUCLEAR PROTEINS; OPEN READING FRAMES; PROTEIN STRUCTURE, TERTIARY; PROTEIN-TYROSINE KINASES; RHO GTP-BINDING PROTEINS; SCHISTOSOMA MANSONI; SRC-FAMILY KINASES; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 70349171810     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006998     Document Type: Article

References (62)

1. Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J (2006) Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 6: 411-425.
2. Ross AG, Bartley PB, Sleigh AC, Olds GR, Li Y, et al. (2002) Schistosomiasis. N Engl J Med 346: 1212-1220.
3. Quack T, Beckmann S, Grevelding CG (2006) Schistosomiasis and the molecular biology of the male-female interaction of S. mansoni. BMTW 119: 365-372.
4. Chitsulo L, LoVerde P, Engels D (2004) Schistosomiasis. Nature Rev Microbiol 2: 12-13.
5. Botros S, Sayed H, Amer N, El-Ghannam M, Bennett JL, et al. (2005) Current status of sensitivity to praziquantel in a focus of potential drug resistance in Egypt. Int J Parasitol 35: 787-791.
6. McManus DP, Loukas A (2008) Current status of vaccines for Schistosomiasis. Clin Microbiol Rev 21: 225-242.
7. Grevelding CG (2004) Schistosoma. Curr Biol 14: R545.
8. Hoffmann K (2004) A historical and genomic view of schistosome conjugal biology with emphasis on sex-specific gene expression. Parasitol 128 (Suppl.): 11-22.
9. Kunz W (2001) Schistosome male-female interaction: induction of germ-cell differentiation. Trends Parasitol 17: 227-231.
10. LoVerde PT, Niles EG, Osman A, Wu W (2004) Schistosoma mansoni male-female interactions. Can J Zool 82: 357-374.
11. LoVerde PT, Osman A, Hinck A (2007) Schistosoma mansoni: TGF-β signaling pathways. Exp Parasitol 117: 304-317.
12. Knobloch J, Beckmann S, Burmeister C, Quack T, Grevelding CG (2007) Tyrosine kinase and cooperative TGFβ signaling in the reproductive organs of Schistosoma mansoni. Exp Parasitol 117: 318-336.
13. Kapp K, Knobloch J, Schussler P, Sroka S, Lammers R, et al. (2004) The Schistosoma mansoni Src kinase TK3 is expressed in the gonads and likely involved in cytoskeletal organization. Mol Biochem Parasitol 138: 171-182.
14. Kapp K, Schussler P, Kunz W, Grevelding CG (2001) Identification, isolation and characterization of a Fyn-like tyrosine kinase from Schistosoma mansoni. Parasitol 122: 317-327.
15. Knobloch J, Kunz W, Grevelding CG (2006) Herbimycin A suppresses mitotic activity and egg production of female Schistosoma mansoni. Int J Parasitol 36: 1261-1272.
16. Faix J, Grosse R (2006) Staying in shape with formins. Dev Cell 10: 693-706.
17. Wallar BJ, Alberts AS (2003) The formins: active scaffolds that remodel the cytoskeleton. Trends Cell Biol 13: 435-446.
18. Young KG, Copeland JW (2008) Formins in cell signaling. Biochim Biophys Acta. (doi: 10.1016/j.bbamcr.2008.09.017).
19. Wennerberg K, Der CJ (2004) Rho-family GTPases: it's not only Rac and Rho (and I like it). J Cell Sci 117: 1301-1312.
20. Krebs A, Rothkegel M, Klar M, Jockusch BM (2002) Characterization of functional domains of mDia1, a link between the small GTPase Rho and the actin cytoskeleton. J Cell Sci 114: 3663-3672.
21. Tominaga T, Sahai E, Chardin P, McCormick F, Courtneidge SA, et al. (2000) Diaphanous-related formins bridge Rho GTPase and Src tyrosine kinase signaling. Mol Cell 5: 13-25.
22. Vermeire JJ, Osman A, LoVerde PT, Williams DL (2003) Characterisation of a Rho homologue of Schistosoma mansoni. Int J Parasitol 33: 721-731.
23. Santos TM, Machado CR, Franco GR, Pena SD (2002) Characterization and comparative functional analysis in yeast of a Schistosoma mansoni Rho1 GTPase gene. Mol Biochem Parasitol 125: 103-112.
24. Belsches AP, Haskell MD, Parsons SJ (1997) Role of c-Src tyrosine kinase in EGF-induced mitogenesis. Front Biosci 2: 501-518.
25. Engena JR, Walesa TE, Hochrein JM, Meyn MA, Ozkand B, et al. (2008) Structure and dynamic regulation of Src-family kinases. Cell Mol Life Sci 65: 3058-3073.
26. Jia CY, Nie J, Wu C, Li C, Li SS (2005) Novel Src homology 3 domain-binding motifs identified from proteomic screen of a Pro-rich region. Mol Cell Proteom 4.8: 1155-1166.
27. Thomas SM, Brugge JS (1997) Cellular functions regulated by Src family kinases. Ann Rev Cell Dev Biol 13: 513-609.
28. Jeffrey R, Gingrich JR, Pelkey KA, Fam SR, Huang Y, et al. (2004) Unique domain anchoring of Src to synaptic NMDA receptors via the mitochondrial protein NADH dehydrogenase subunit 2. PNAS 101: 6237-6242.
29. Grevelding CG (1995) The female specific W1 sequence of the Puerto Rico strain of Schistosoma mansoni occurs in both genders of a Liberian strain. Mol Biochem Parasitol 71: 269-273.
30. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning. A Laboratory Manual. 2nd. edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
31. Robzyk K, Kassir Y (1992) A simple and highly efficient procedure for rescuing autonomous plasmids from yeast. Nucleic Acids Res 20: 3790.
32. Kyhse-Andersen J (1984) Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J Biochem Biophys Methods 10: 203-209.
33. Finken M, Sobek A, Symmons P, Kunz W (1994) Characterization of the complete protein disulfide isomerase gene of Schistosoma mansoni and identification of the tissues of its expression. Mol Biochem Parasitol 640: 135-144.
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. El-Sayed NM, Bartholomeu D, Ivens A, Johnston DA, LoVerde PT (2004) Advances in schistosome genomics. Trends Parasitol 20: 154-157.
36. Kay BK, Williamson MP, Sudol M (2000) The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J 14: 231-241.
37. Kozak M (1989) The scanning model for translation: an update. J Cell Biol 108: 229-241.
38. Haas BJ, Berriman M, Hirai H, Cerqueira GG, LoVerde PT, et al. (2007) Schistosoma mansoni genome: closing in on a final gene set. Exp Parasitol 117: 225-228.
39. Grosse R, Copeland JW, Newsome TP, Way M, Treisman R (2003) A role for VASP in RhoA-Diaphanous signalling to actin dynamics and SRF activity. EMBO 22: 3050-3061.
40. Heasman SJ, Ridley AJ (2008) Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 9: 690-701.
41. Tatosyan AG, Mizenina OA (2000) Kinases of the Src family: structure and functions. Biochem (Moscow) 65: 49-58.
42. Kaneko T, Li C, Li SS (2008) The SH3 domain - a family of versatile peptide- and protein-recognition module. Front Biosci 13: 4938-4952.
43. Ou Y, Rattner JB (2004) The centrosome in higher organisms: structure, composition, and duplication. Int Rev Cytol 238: 119-182.
44. Weiler MC, Smith JL, Masters JN (1996) CR16, a novel proline-rich protein expressed in rat brain neurons, binds to SH3 domains and is a MAP kinase substrate. J Mol Neurosci Fall 7: 203-215.
45. Aspenström P (2005) The verprolin family of proteins: regulators of cell morphogenesis and endocytosis. FEBS Lett 579: 5253-5259.
46. Foster AC, Schwarcz R (1985) Characterization of quinolinic acid phosphoribosyltransferase in human blood and observations in Huntington's disease. J Neurochem 45: 199-205.
47. Cimato TR, Tang J, Xu Y, Guarnaccia C, Herschman HR, et al. (2002) Nerve growth factor-mediated increases in protein methylation occur predominantly at type I arginine methylation sites and involve protein arginine methyltransferase 1. J Neurosci Res 67: 435-442.
48. Leonhard K, Stiegler A, Neupert W, Langer T (1999) Chaperone-like activity of the AAA domain of the yeast Yme1 AAA protease. Nature 398: 348-351.
49. Kang Q, Cao Y, Zolkiewska A (2000) Metalloprotease-disintegrin ADAM 12 binds to the SH3 domain of Src and activates Src tyrosine kinase in C2C12 cells. Biochem J 352: 883-892.
50. Mohrmann L, Verrijzer CP (2005) Composition and functional specificity of SWI2/SNF2 class chromatin remodeling complexes. Biochim Biophys Acta 1681: 59-73.
51. Chai B, Huang J, Cairns B R, Laurent BC (2005) Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev 19: 1656-1661.
52. Downs JA, Nussenzweig MC, Nussenzweig A (2007) Chromatin dynamics and the preservation of genetic information. Nature 447: 951-958.
53. Simone C (2006) SWI/SNF: The crossroad where extracellular signaling pathways meet chromatin. J Cell Physiol 207: 309-314.
54. Takahashi A, Obata Y, Fukumoto Y, Nakayama Y, Kasahara K, et al. (2009) Nuclear Localization of Src-family tyrosine kinases is required for growth factor-induced euchromatinization. Exp Cell Res 2009: (doi: 10.1016/j.yexcr.2009.02.010).
55. Ramirez-Valle F, Braunstein S, Zavadil J, Formenti SC, Schneider RJ (2008) eIF4GI links nutrient sensing by mTOR to cell proliferation and inhibition of autophagy. J Cell Biol 181: 293-307.
56. Liu R, Linardopoulou EV, Osborn GE, Parkhurst SM (2008) Formins in development: orchestrating body plan origami. Biochim Biophys Acta. (doi: 10.1016/j.bbamcr.2008.09.016).
57. Aspenström P, Richnau N, Johansson AS (2006) The diaphanous-related formin DAAM1 collaborates with the Rho GTPases RhoA and Cdc42, CIP4 and Src in regulating cell morphogenesis and actin dynamics. Exp Cell Res 312: 2180-2194.
58. Gasman S, Kalaidzidis Y, Zerial M (2003) RhoD regulates endosome dynamics through Diaphanous-related Formin and Src tyrosine kinase. Nat Cell Biol 5: 195-204.
59. Sandilands E, Frame MC (2008) Endosomal trafficking of Src tyrosine kinase. Trends Cell Biol 18: 322-329.
60. Bahia D, Andrade LF, Ludolf F, Mortara RA, Oliveira G (2006) Protein tyrosine kinases in Schistosoma mansoni. Mem Inst Oswaldo Cruz 101 Suppl 1: 137-143.
61. Ludolf F, Bahia D, Andrade LF, Cousin A, Capron M (2007) Molecular analysis of SmFes, a tyrosine kinase of Schistosoma mansoni orthologous to the members of the Fes/Fps/Fer family. Biochem Biophys Res Commun 360: 163-172.
62. Dissous C, Ahier A, Khayath N (2007) Protein tyrosine kinases as new potential targets against human schistosomiasis. Bioessays 29: 1281-1288.