A PAL for Schistosoma mansoni PHM

Molecular and Biochemical Parasitology

Volumn 173, Issue 2, 2010, Pages 97-106

  Atkinson, Louise E ^a   McVeigh, Paul ^a   Kimber, Michael J ^b   Marks, Nikki J ^a   Eipper, Betty A ^c   Mains, Richard E ^c   Day, Tim A ^b   Maule, Aaron G ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b IOWA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

In situ hybridisation; Neuropeptide amidation; Peptidylglycine amidating lyase; RNA interference; Schistosoma mansoni

Indexed keywords

LYASE; MESSENGER RNA; NEUROPEPTIDE; PEPTIDYLGLYCINE ALPHA AMIDATING LYASE; PEPTIDYLGLYCINE ALPHA HYDROXYLATING MONOOXYGENASE; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE; COMPLEMENTARY DNA; HELMINTH DNA; HELMINTH PROTEIN; MIXED FUNCTION OXIDASE; MULTIENZYME COMPLEX; PEPTIDYLGLYCINE MONOOXYGENASE;

ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; GENE FUNCTION; GENETIC TRANSCRIPTION; IN SITU HYBRIDIZATION; NERVE CELL; NEUROMUSCULAR FUNCTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; SCHISTOSOMA MANSONI; AMINO ACID SEQUENCE; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DNA SEQUENCE; ENZYME ACTIVE SITE; ENZYME STABILITY; ENZYMOLOGY; FEMALE; GENE EXPRESSION PROFILING; GENE SILENCING; GENETICS; MALE; METABOLISM; MOLECULAR GENETICS; MOUSE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY;

SCHISTOSOMA; SCHISTOSOMA MANSONI; SCHISTOSOMATIDAE; VERMES;

AMINO ACID SEQUENCE; ANIMALS; CATALYTIC DOMAIN; DNA, COMPLEMENTARY; DNA, HELMINTH; ENZYME STABILITY; FEMALE; GENE EXPRESSION PROFILING; GENE SILENCING; HELMINTH PROTEINS; HYDROGEN-ION CONCENTRATION; IN SITU HYBRIDIZATION; LYASES; MALE; MICE; MIXED FUNCTION OXYGENASES; MOLECULAR SEQUENCE DATA; MULTIENZYME COMPLEXES; RNA INTERFERENCE; SCHISTOSOMA MANSONI; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 77954700797     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2010.05.009     Document Type: Article

References (65)

1. Hotez P.J., Brindley P.J., Bethony J.M., et al. Helminth infections: the great neglected tropical diseases. J Clin Invest 2008, 118:1311-1321.
2. Fallon P.G., Doenhoff M.J. Drug-resistant schistosomiasis: resistance to praziquantel and oxamniquine induced in Schistosoma mansoni in mice is drug specific. Am J Trop Med Hyg 1994, 51:83-88.
3. Geerts S., Gryseels B. Anthelmintic resistance in human helminths: a review. Trop Med Int Health 2001, 6:915-921.
4. Botros S., Sayed H., Amer N., et al. Current status of sensitivity to praziquantel in a focus of potential drug resistance in Egypt. Int J Parasitol 2005, 35:787-791.
5. Caffrey C.R., Rohwer A., Oellien F., et al. A comparative chemogenomics strategy to predict potential drug targets in the metazoan pathogen, Schistosoma mansoni. PLoS One 2009, 4:e4413.
6. Halton D.W., Gustafsson M.K. Functional morphology of the platyhelminth nervous system. Parasitology 1996, 113:S47.
7. Gustafsson M.K., Halton D.W., Kreshchenko N.D., et al. Neuropeptides in flatworms. Peptides 2002, 23:2053-2061.
8. Maule A.G., Mousley A., Marks N.J., et al. Neuropeptide signaling systems-potential drug targets for parasite and pest control. Curr Top Med Chem 2002, 2:733-758.
9. Mousley A., Marks N.J., Halton D.W., et al. Arthropod FMRFamide-related peptides modulate muscle activity in helminths. Int J Parasitol 2004, 34:755-768.
10. Mousley A., Marks N.J., Maule A.G. Neuropeptide signalling: a repository of targets for novel endectocides?. Trends Parasitol 2004, 20:482-487.
11. Kreshchenko N.D. Functions of flatworm neuropeptides NPF, GYIRF and FMRF in course of pharyngeal regeneration of anterior body fragments of planarian, Girardia tigrina. Acta Biol Hung 2008, 59 Suppl.:199-207.
12. Humphries J.E., Kimber M.J., Barton Y.W., et al. Structure and bioactivity of neuropeptide F from the human parasites Schistosoma mansoni and Schistosoma japonicum. J Biol Chem 2004, 279:39880-39885.
13. McVeigh P., Mair G.R., Atkinson L., et al. Discovery of multiple neuropeptide families in the phylum Platyhelminthes. Int J Parasitol 2009, 39:1243-1252.
14. Skuce P.J., Johnston C.F., Fairweather I., et al. A confocal scanning laser microscope study of the peptidergic and serotoninergic components of the nervous system in larval Schistosoma mansoni. Parasitology 1990, 101(Pt 2):227-234.
15. Skuce P.J., Johnston C.F., Fairweather I., et al. Immunoreactivity to the pancreatic polypeptide family in the nervous system of the adult human blood fluke, Schistosoma mansoni. Cell Tissue Res 1990, 261:573-581.
16. Solis-Soto J.M., De Jong Brink M. Immunocytochemical study on biologically active neurosubstances in daughter sporocysts and cercariae of Trichobilharzia ocellata and Schistosoma mansoni. Parasitology 1994, 108(Pt 3):301-311.
17. Fairweather I., Skuce P.O., Brownlee D.J., et al. Light and electron microscopic immunocytochemistry of FMRFamide and neuropeptide F immunoreactivities in the human blood fluke, Schistosoma mansoni. Acta Biol Hung 1995, 46:211-220.
18. Marks N.J., Halton D.W., Maule A.G., et al. Comparative analyses of the neuropeptide F (NPF)- and FMRFamide-related peptide (FaRP)-immunoreactivities in Fasciola hepatica and Schistosoma spp. Parasitology 1995, 110(Pt. 4):371-381.
19. Mair G.R., Maule A.G., Shaw C., et al. Muscling in on parasitic flatworms. Parasitol Today 1998, 14:73-76.
20. Day T.A., Maule A.G., Shaw C., et al. Platyhelminth FMRFamide-related peptides (FaRPs) contract Schistosoma mansoni (Trematoda: Digenea) muscle fibres in vitro. Parasitology 1994, 109(Pt 4):455-459.
21. Eipper B.A., Stoffers D.A., Mains R.E. The biosynthesis of neuropeptides: peptide alpha-amidation. Annu Rev Neurosci 1992, 15:57-85.
22. Bolkenius F.N., Ganzhorn A.J. Peptidylglycine alpha-amidating mono-oxygenase: neuropeptide amidation as a target for drug design. Gen Pharmacol 1998, 31:655-659.
23. Kulathila R., Merkler K.A., Merkler D.J. Enzymatic formation of C-terminal amides. Nat Prod Rep 1999, 16:145-154.
24. Prigge S.T., Mains R.E., Eipper B.A., et al. New insights into copper monooxygenases and peptide amidation: structure, mechanism and function. Cell Mol Life Sci 2000, 57:1236-1259.
25. Kolhekar A.S., Roberts M.S., Jiang N., et al. Neuropeptide amidation in Drosophila: separate genes encode the two enzymes catalyzing amidation. J Neurosci 1997, 17:1363-1376.
26. Asada A., Orii H., Watanabe K., et al. Planarian peptidylglycine-hydroxylating monooxygenase, a neuropeptide processing enzyme, colocalizes with cytochrome b561 along the central nervous system. FEBS J 2005, 272:942-955.
27. Eipper B.A., Milgram S.L., Husten E.J., et al. Peptidylglycine alpha-amidating monooxygenase: a multifunctional protein with catalytic, processing, and routing domains. Protein Sci 1993, 2:489-497.
28. Mair G.R., Niciu M.J., Stewart M.T., et al. A functionally atypical amidating enzyme from the human parasite Schistosoma mansoni. FASEB J 2004, 18:114-121.
29. Berriman M., Haas B.J., LoVerde P.T., et al. The genome of the blood fluke Schistosoma mansoni. Nature 2009, 460:352-358.
30. Dillon G.P., Illes J.C., Isaacs H.V., et al. Patterns of gene expression in schistosomes: localization by whole mount in situ hybridization. Parasitology 2007, 134:1589-1597.
31. Ndegwa D., Krautz-Peterson G., Skelly P.J. Protocols for gene silencing in schistosomes. Exp. Parasitol. 2007, 117:284-291.
32. Altschul S.F., Gish W., Miller W., et al. Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
33. Zdobnov E.M., Apweiler R. InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 2001, 17:847-848.
34. Emanuelsson O., Brunak S., von Heijne G., et al. Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2007, 2:953-971.
35. Han M., Park D., Vanderzalm P.J., et al. Drosophila uses two distinct neuropeptide amidating enzymes, dPAL1 and dPAL2. J Neurochem 2004, 90:129-141.
36. Pownall M.E., Tucker A.S., Slack J.M., et al. eFGF, Xcad3 and Hox genes form a molecular pathway that establishes the anteroposterior axis in Xenopus. Development 1996, 122:3881-3892.
37. Correnti J.M., Brindley P.J., Pearce E.J. Long-term suppression of cathepsin B levels by RNA interference retards schistosome growth. Mol Biochem Parasitol 2005, 143:209-215.
38. Nielsen H., Engelbrecht J., Brunak S., et al. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 1997, 10:1-6.
39. Kolhekar A.S., Bell J., Shiozaki E.N., et al. Essential features of the catalytic core of peptidyl-alpha-hydroxyglycine alpha-amidating lyase. Biochemistry 2002, 41:12384-12394.
40. De M., Bell J., Blackburn N.J., et al. Role for an essential tyrosine in peptide amidation. J Biol Chem 2006, 281:20873-20882.
41. Chufan E.E., De M., Eipper B.A., et al. Amidation of bioactive peptides: the structure of the lyase domain of the amidating enzyme. Structure 2009, 17:965-973.
42. Ouafik L.H., Stoffers D.A., Campbell T.A., et al. The multifunctional peptidylglycine alpha-amidating monooxygenase gene: exon/intron organization of catalytic, processing, and routing domains. Mol Endocrinol 1992, 6:1571-1584.
43. Iwasaki Y., Shimoi H., Saiki H., et al. Tissue-specific molecular diversity of amidating enzymes (peptidylglycine alpha-hydroxylating monooxygenase and peptidylhydroxyglycine N-C lyase) in Xenopus laevis. Eur J Biochem 1993, 214:811-818.
44. Spijker S., Smit A.B., Eipper B.A., et al. A molluscan peptide alpha-amidating enzyme precursor that generates five distinct enzymes. FASEB J 1999, 13:735-748.
45. Fan X., Spijker S., Akalal D.B., et al. Neuropeptide amidation: cloning of a bifunctional alpha-amidating enzyme from Aplysia. Brain Res Mol Brain Res 2000, 82:25-34.
46. Williamson M., Hauser F., Grimmelikhuijzen C.J. Genomic organization and splicing variants of a peptidylglycine alpha-hydroxylating monooxygenase from sea anemones. Biochem Biophys Res Commun 2000, 277:7-12.
47. Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 1998, 282:2012-2018. C. elegans Sequencing Consortium.
48. Yun H.Y., Johnson R.C., Mains R.E., et al. Topological switching of the COOH-terminal domain of peptidylglycine alpha-amidating monooxygenase by alternative RNA splicing. Arch Biochem Biophys 1993, 301:77-84.
49. Kolhekar A.S., Quon A.S., Berard C.A., et al. Post-translational N-glycosylation of a truncated form of a peptide processing enzyme. J Biol Chem 1998, 273:23012-23018.
50. Eipper B.A., Perkins S.N., Husten E.J., et al. Peptidyl-alpha-hydroxyglycine alpha-amidating lyase. Purification, characterization, and expression. J Biol Chem 1991, 266:7827-7833.
51. Husten E.J., Eipper B.A. Purification and characterization of PAM-1, an integral membrane protein involved in peptide processing. Arch Biochem Biophys 1994, 312:487-492.
52. Boyle J.P., Wu X.J., Shoemaker C.B., et al. Using RNA interference to manipulate endogenous gene expression in Schistosoma mansoni sporocysts. Mol Biochem Parasitol 2003, 128:205-215.
53. Skelly P.J., Da'dara A., Harn D.A. Suppression of cathepsin B expression in Schistosoma mansoni by RNA interference. Int J Parasitol 2003, 33:363-369.
54. Correnti J.M., Pearce E.J. Transgene expression in Schistosoma mansoni: introduction of RNA into schistosomula by electroporation. Mol Biochem Parasitol 2004, 137:75-79.
55. Cheng G.F., Lin J.J., Shi Y., et al. Dose-dependent inhibition of gynecophoral canal protein gene expression in vitro in the schistosome (Schistosoma japonicum) by RNA interference. Acta Biochim Biophys Sin (Shanghai) 2005, 37:386-390.
56. Dinguirard N., Yoshino T.P. Potential role of a CD36-like class B scavenger receptor in the binding of modified low-density lipoprotein (acLDL) to the tegumental surface of Schistosoma mansoni sporocysts. Mol Biochem Parasitol 2006, 146:219-230.
57. Krautz-Peterson G., Radwanska M., Ndegwa D., et al. Optimizing gene suppression in schistosomes using RNA interference. Mol Biochem Parasitol 2007, 153:194-202.
58. Nabhan J.F., El-Shehabi F., Patocka N., et al. The 26S proteasome in Schistosoma mansoni: bioinformatics analysis, developmental expression, and RNA interference (RNAi) studies. Exp Parasitol 2007, 117:337-347.
59. Krautz-Peterson G., Skelly P.J. Schistosome asparaginyl endopeptidase (legumain) is not essential for cathepsin B1 activation in vivo. Mol Biochem Parasitol 2008, 159:54-58.
60. Morales M.E., Rinaldi G., Gobert G.N., et al. RNA interference of Schistosoma mansoni cathepsin D, the apical enzyme of the hemoglobin proteolysis cascade. Mol Biochem Parasitol 2008, 157:160-168.
61. Zhao Z.R., Lei L., Liu M., et al. Schistosoma japonicum: inhibition of Mago nashi gene expression by shRNA-mediated RNA interference. Exp Parasitol 2008, 119:379-384.
62. de Moraes Mourao M., Dinguirard N., Franco G.R., et al. Phenotypic screen of early-developing larvae of the blood fluke, Schistosoma mansoni, using RNA interference. PLoS Negl Trop Dis 2009, 3:e502.
63. Rinaldi G., Morales M.E., Alrefaei Y.N., et al. RNA interference targeting leucine aminopeptidase blocks hatching of Schistosoma mansoni eggs. Mol Biochem Parasitol 2009, 167:118-126.
64. Beckmann S., Buro C., Dissous C., et al. The Syk kinase SmTK4 of Schistosoma mansoni is involved in the regulation of spermatogenesis and oogenesis. PLoS Pathog 2010, 6.
65. Timmons L., Court D.L., Fire A. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 2001, 263:103-112.