Discovery of Platyhelminth-Specific α/β-Integrin Families and Evidence for Their Role in Reproduction in Schistosoma mansoni

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Beckmann, Svenja ^a   Quack, Thomas ^a   Dissous, Colette ^b   Cailliau, Katia ^b   Lang, Gabriele ^a   Grevelding, Christoph G ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b UNIV LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTEGRIN; BETA INTEGRIN; PROTEIN KINASE SYK;

AMINO ACID SEQUENCE; ARTICLE; CLADISTICS; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; IMMUNOPRECIPITATION; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; PHENOTYPE; PHYLOGENY; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REPRODUCTION; RNA INTERFERENCE; SCHISTOSOMA MANSONI; SEQUENCE ANALYSIS; SEXUAL BEHAVIOR; UNINDEXED SEQUENCE;

ANIMALS; CLONING, MOLECULAR; FEMALE; INTEGRIN ALPHA CHAINS; INTEGRIN BETA CHAINS; MALE; OOGENESIS; OVARY; PROTEIN-TYROSINE KINASES; RNA, SMALL INTERFERING; SCHISTOSOMA MANSONI; SEQUENCE ANALYSIS; SPECIES SPECIFICITY; TESTIS; TRANSCRIPTION, GENETIC;

METAZOA; PLATYHELMINTHES; SCHISTOSOMA; SCHISTOSOMA MANSONI; TREMATODA;

EID: 84871646029     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052519     Document Type: Article

References (78)

1. Fu G, Wang W, Luo BH, (2012) Overview: structural biology of integrins. Methods Mol Biol 757: 81-99.
2. Anthis NJ, Campbell ID, (2011) The tail of integrin activation. Trends Biochem Sci 36: 191-198.
3. Kim C, Ye F, Ginsberg MH, (2011) Regulation of integrin activation. Annu Rev Cell Dev Biol 27: 321-345.
4. Campbell ID, Humphries MJ (2011) Integrin structure, activation, and interactions. Cold Spring Harb Perspect Biol 3: pii, a004994.
5. Guo W, Giancotti FG, (2004) Integrin signalling during tumour progression. Nat Rev Mol Cell Biol 5: 816-826.
6. Hynes RO, (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110: 673-687.
7. Jakus Z, Fodor S, Abram CL, Lowell CA, Mocsai A, (2007) Immunoreceptor-like signaling by beta 2 and beta 3 integrins. Trends Cell Biol 17: 493-501.
8. Obergfell A, Eto K, Mocsai A, Buensuceso C, Moores SL, et al. (2002) Coordinate interactions of Csk, Src, and Syk kinases with [alpha]IIb[beta]3 initiate integrin signaling to the cytoskeleton. J Cell Biol 157: 265-275.
9. Soung YH, Clifford JL, Chung J, (2010) Crosstalk between integrin and receptor tyrosine kinase signaling in breast carcinoma progression. BMB Rep 43: 311-318.
10. Mitra SK, Schlaepfer DD, (2006) Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr Opin Cell Biol 18: 516-523.
11. Woodside DG, Obergfell A, Talapatra A, Calderwood DA, Shattil SJ, et al. (2002) The N-terminal SH2 domains of Syk and ZAP-70 mediate phosphotyrosine-independent binding to integrin beta cytoplasmic domains. J Biol Chem 277: 39401-39408.
12. Ivaska J, Heino J, (2011) Cooperation between integrins and growth factor receptors in signaling and endocytosis. Annu Rev Cell Dev Biol 27: 291-320.
13. Chitsulo L, LoVerde P, Engels D, (2004) Schistosomiasis. Nat Rev Microbiol 2: 12-13.
14. Engels D, Chitsulo L, Montresor A, Savioli L, (2002) The global epidemiological situation of schistosomiasis and new approaches to control and research. Acta Trop 82: 139-146.
15. Quack T, Beckmann S, Grevelding CG, (2006) Schistosomiasis and the molecular biology of the male-female interaction of S. mansoni. Berl Munch Tierarztl Wochenschr 119: 365-372.
16. Ross AG, Bartley PB, Sleigh AC, Olds GR, Li Y, et al. (2002) Schistosomiasis. N Engl J Med 346: 1212-1220.
17. Erasmus DA, (1973) A comparative study of the reproductive system of mature, immature and "unisexual" female Schistosoma mansoni. Parasitology 67: 165-183.
18. Grevelding CG, (2004) Schistosoma. Curr Biol 14: R545.
19. Knobloch J, Kunz W, Grevelding CG, (2002) Quantification of DNA synthesis in multicellular organisms by a combined DAPI and BrdU technique. Dev Growth Differ 44: 559-563.
20. Kunz W, (2001) Schistosome male-female interaction: induction of germ-cell differentiation. Trends Parasitol 17: 227-231.
21. LoVerde PT, Niles EG, Osman A, Wu W, (2004) Schistosoma mansoni male-female interactions. Can J Zool 82: 357-374.
22. Popiel I, (1986) Male-stimulated female maturation in Schistosoma: a review. J Chem Ecol 12: 1745-1754.
23. Beckmann S, Quack T, Burmeister C, Buro C, Long T, et al. (2010) Schistosoma mansoni: signal transduction processes during the development of the reproductive organs. Parasitology 139: 651-668.
24. Knobloch J, Beckmann S, Burmeister C, Quack T, Grevelding CG, (2007) Tyrosine kinase and cooperative TGFbeta signaling in the reproductive organs of Schistosoma mansoni. Exp Parasitol 117: 318-336.
25. LoVerde PT, Osman A, Hinck A, (2007) Schistosoma mansoni: TGF-beta signaling pathways. Exp Parasitol 117: 304-317.
26. 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.
27. Beckmann S, Hahnel S, Cailliau K, Vanderstraete M, Browaeys E, et al. (2011) Characterization of the SRC/ABl hybrid-kinase SMTK6 of Schistosoma mansoni. J Biol Chem 286: 42325-42336.
28. Beckmann S, Grevelding CG, (2010) Imatinib has a fatal impact on morphology, pairing stability and survival of adult Schistosoma mansoni in vitro. Int J Parasitol 40: 521-526.
29. Beckmann S, Buro C, Dissous C, Hirzmann J, Grevelding CG, (2010) The Syk Kinase SmTK4 of Schistosoma mansoni Is Involved in the Regulation of Spermatogenesis and Oogenesis. PLoS Pathog 6: e1000769.
30. Knobloch J, Winnen R, Quack M, Kunz W, Grevelding CG, (2002) A novel Syk-family tyrosine kinase from Schistosoma mansoni which is preferentially transcribed in reproductive organs. Gene 294: 87-97.
31. Vicogne J, Pin JP, Lardans V, Capron M, Noel C, et al. (2003) An unusual receptor tyrosine kinase of Schistosoma mansoni contains a Venus Flytrap module. Mol Biochem Parasitol 126: 51-62.
32. Arias-Salgado EG, Lizano S, Sarkar S, Brugge JS, Ginsberg MH, et al. (2003) Src kinase activation by direct interaction with the integrin beta cytoplasmic domain. Proc Natl Acad Sci USA 100: 13298-13302.
33. Kato A, Oshimi K, (2009) Ancient ubiquitous protein 1 and Syk link cytoplasmic tails of the integrin alpha(IIb)beta(3). Platelets 20: 105-110.
34. Lowell CA, (2011) Src-family and Syk kinases in activating and inhibitory pathways in innate immune cells: signaling cross talk. Cold Spring Harb Perspect Biol 3(3): a002352.
35. Piccardoni P, Manarini S, Federico L, Bagoly Z, Pecce R, et al. (2004) SRC-dependent outside-in signalling is a key step in the process of autoregulation of beta2 integrins in polymorphonuclear cells. Biochem J 380: 57-65.
36. Totani L, Piccoli A, Manarini S, Federico L, Pecce R, et al. (2006) Src-family kinases mediate an outside-in signal necessary for beta2 integrins to achieve full activation and sustain firm adhesion of polymorphonuclear leucocytes tethered on E-selectin. Biochem J 396: 89-98.
37. 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.
38. Wang X, Chen W, Huang Y, Sun J, Men J, et al. (2011) The draft genome of the carcinogenic human liver fluke Clonorchis sinensis. Genome Biol 12: R107.
39. Bork P, Doerks T, Springer TA, Snel B, (1999) Domains in plexins: links to integrins and transcription factors. Trends Biochem Sci 24: 261-263.
40. Takagi J, Springer TA, (2002) Integrin activation and structural rearrangement. Immunol Rev 186: 141-163.
41. Calvete JJ, Henschen A, Gonzalez-Rodriguez J, (1991) Assignment of disulphide bonds in human platelet GPIIIa. A disulphide pattern for the beta-subunits of the integrin family. Biochem J 274: 63-71.
42. Zang Q, Springer TA, (2001) Amino acid residues in the PSI domain and cysteine-rich repeats of the integrin beta2 subunit that restrain activation of the integrin alpha(X)beta(2). J Biol Chem 276: 6922-6929.
43. Bajt ML, Loftus JC, (1994) Mutation of a ligand binding domain of beta 3 integrin. Integral role of oxygenated residues in alpha IIb beta 3 (GPIIb-IIIa) receptor function. J Biol Chem 269: 20913-20919.
44. Young ND, Jex AR, Li B, Liu S, Yang L, et al. (2012) Whole-genome sequence of Schistosoma haematobium. Nat Genet 44: 221-225.
45. Schistosoma japonicum Genome Sequencing, Functional Analysis Consortium, (2009) The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460: 345-351.
46. Robb SM, Ross E, Sanchez AA, (2008) SmedGD: the Schmidtea mediterranea genome database. Nucleic Acids Res 36: D599-D606.
47. Hughes AL, (2001) Evolution of the integrin alpha and beta protein families. J Mol Evol 52: 63-72.
48. Neves RH, de Lamare BC, Machado-Silva JR, Carvalho JJ, Branquinho TB, et al. (2005) A new description of the reproductive system of Schistosoma mansoni (Trematoda: Schistosomatidae) analyzed by confocal laser scanning microscopy. Parasitol Res 95: 43-49.
49. Leutner S, Beckmann S, Grevelding CG, (2011) Characterization of the cGMP-dependent protein kinase SmcGK1 of Schistosoma mansoni. An Acad Bras Cienc 83: 637-648.
50. Verjovski-Almeida S, Venancio TM, Oliveira KC, Almeida GT, DeMarco R, (2007) Use of a 44k oligoarray to explore the transcriptome of Schistosoma mansoni adult worms. Exp Parasitol 117: 236-245.
51. Zou W, Kitaura H, Reeve J, Long F, Tybulewicz VL, et al. (2007) Syk, c-Src, the alphavbeta3 integrin, and ITAM immunoreceptors, in concert, regulate osteoclastic bone resorption. J Cell Biol 176: 877-888.
52. Gould RJ, Polokoff MA, Friedman PA, Huang TF, Holt JC, et al. (1990) Disintegrins: a family of integrin inhibitory proteins from viper venoms. Proc Soc Exp Biol Med 195: 168-171.
53. Kumar CC, Nie H, Rogers CP, Malkowski M, Maxwell E, et al. (1997) Biochemical characterization of the binding of echistatin to integrin alphavbeta3 receptor. J Pharmacol Exp Ther 283: 843-853.
54. Musial J, Niewiarowski S, Rucinski B, Stewart GJ, Cook JJ, et al. (1990) Inhibition of platelet adhesion to surfaces of extracorporeal circuits by disintegrins. RGD-containing peptides from viper venoms. Circulation 82: 261-273.
55. Sato M, Sardana MK, Grasser WA, Garsky VM, Murray JM, et al. (1990) Echistatin is a potent inhibitor of bone resorption in culture. J Cell Biol 111: 1713-1723.
56. Krautz-Peterson G, Bhardwaj R, Faghiri Z, Tararam CA, Skelly PJ, (2010) RNA interference in schistosomes: machinery and methodology. Parasitology 137: 485-495.
57. Ewan R, Huxley-Jones J, Mould AP, Humphries MJ, Robertson DL, et al. (2005) The integrins of the urochordate Ciona intestinalis provide novel insights into the molecular evolution of the vertebrate integrin family. BMC Evol Biol 5: 31.
58. Brower DL, Brower SM, Hayward DC, Ball EE, (1997) Molecular evolution of integrins: genes encoding integrin beta subunits from a coral and a sponge. Proc Natl Acad Sci USA 94: 9182-9187.
59. Wimmer W, Perovic S, Kruse M, Schroder HC, Krasko A, et al. (1999) Origin of the integrin-mediated signal transduction. Functional studies with cell cultures from the sponge Suberites domuncula. Eur J Biochem 260: 156-165.
60. Burke RD, (1999) Invertebrate integrins: structure, function, and evolution. Int Rev Cytol 191: 257-284.
61. Oliveira KC, Carvalho ML, Maracaja-Coutinho V, Kitajima JP, Verjovski-Almeida S, (2011) Non-coding RNAs in schistosomes: an unexplored world. An Acad Bras Cienc 83: 673-694.
62. Arnaout MA, Goodman SL, Xiong JP, (2007) Structure and mechanics of integrin-based cell adhesion. Curr Opin Cell Biol 19: 495-507.
63. Alam N, Goel HL, Zarif MJ, Butterfield JE, Perkins HM, et al. (2007) The integrin-growth factor receptor duet. J Cell Physiol 213: 649-653.
64. Hubbard SR, Till JH, (2000) Protein tyrosine kinase structure and function. Annu Rev Biochem 69: 373-398.
65. van der Flier A, Sonnenberg A, (2001) Function and interactions of integrins. Cell Tissue Res 305: 285-298.
66. Ndegwa D, Krautz-Peterson G, Skelly PJ, (2007) Protocols for gene silencing in schistosomes. Exp Parasitol 117: 284-291.
67. LaFlamme SE, Nieves B, Colello D, Reverte CG, (2008) Integrins as regulators of the mitotic machinery. Curr Opin Cell Biol 20: 576-582.
68. Aszodi A, Hunziker EB, Brakebusch C, Fassler R, (2003) Beta1 integrins regulate chondrocyte rotation, G1 progression, and cytokinesis. Genes Dev 17: 2465-2479.
69. 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.
70. Zou W, Teitelbaum SL, (2010) Integrins, growth factors, and the osteoclast cytoskeleton. Ann NY Acad Sci 1192: 27-31.
71. Quack T, Knobloch J, Beckmann S, Vicogne J, Dissous C, et al. (2009) The formin-homology protein SmDia interacts with the Src kinase SmTK and the GTPase SmRho1 in the gonads of Schistosoma mansoni. PloS One 4: e6998.
72. 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 J 22: 3050-3061.
73. 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.
74. Huveneers S, Danen EH, (2009) Adhesion signaling- crosstalk between integrins, Src and Rho. J Cell Sci 122: 1059-1069.
75. Lee M, Shen B, Schwarzbauer JE, Ahn J, Kwon J, (2005) Connections between integrins and Rac GTPase pathways control gonad formation and function in C. elegans. Biochim Biophys Acta 1723: 248-255.
76. Grevelding CG, (1995) The female-specific W1 sequence of the Puerto Rican strain of Schistosoma mansoni occurs in both genders of a Liberian strain. Mol Biochem Parasitol 71: 269-272.
77. Vicogne J, Cailliau K, Tulasne D, Browaeys E, Yan YT, et al. (2004) Conservation of epidermal growth factor receptor function in the human parasitic helminth Schistosoma mansoni. J Biol Chem 279: 37407-37414.
78. 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 64: 135-144.