Characterization of asparaginyl endopeptidase, legumain induced by blood feeding in the ixodid tick Haemaphysalis longicornis

Insect Biochemistry and Molecular Biology

Volumn 37, Issue 9, 2007, Pages 911-922

  Abdul Alim, M ^a   Tsuji, Naotoshi ^a   Miyoshi, Takeharu ^a   Khyrul Islam, M ^a   Huang, Xiaohong ^a   Motobu, Maki ^a   Fujisaki, Kozo ^b,c  

^a NATIONAL INSTITUTE OF ANIMAL HEALTH   (Japan)

^b OBIHIRO UNIVERSITY OF AGRICULTURE AND VETERINARY MEDICINE   (Japan)

^c KAGOSHIMA UNIVERSITY   (Japan)

Author keywords

Asparaginyl endopeptidase; Blood meal digestion; Haemaphysalis longicornis; Hydrolysis activity; Ixodid tick; Legumain

Indexed keywords

ANTIGEN; CYSTEINE PROTEINASE; LEGUMAIN; MESSENGER RNA; PRIMER DNA; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CLASSIFICATION; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION PROFILING; GENETICS; JAPAN; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; TICK;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS; CLONING, MOLECULAR; CONSERVED SEQUENCE; CYSTEINE ENDOPEPTIDASES; DNA PRIMERS; ESCHERICHIA COLI; GENE EXPRESSION PROFILING; IXODIDAE; JAPAN; MOLECULAR SEQUENCE DATA; PHYLOGENY; RECOMBINANT PROTEINS; RNA, MESSENGER; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

BOVINAE; ESCHERICHIA COLI; HAEMAPHYSALIS LONGICORNIS; IXODIDA;

EID: 34547532754     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2007.04.010     Document Type: Article

References (55)

1. Abe Y., Shirane K., Yokasawa H., Matsushita H., Mitta M., Kato I., and Ishii S.I. Asparaginyl endopeptidase of jack bean seeds: purification, characterization, and high utility in protein sequence analysis. J. Biol. Chem. 268 (1993) 3525-3529
2. Agyei A.D., and Runham N.W. Studies on the morphological changes in the midguts of two ixodid tick species Boophilus microplus and Rhipucephalus appendiculatus during digestion of the blood meal. Int. J. Parasitol. 25 (1995) 55-62
3. Akov S. Blood digestion in ticks. In: Obenchain F., and Galun R. (Eds). Physiology of Ticks (1982), Pergamon Press, Oxford 197-211
4. Alonso J.M., and Granell A. A putative vacuolar processing protease is regulated by ethylene and also during fruit ripening in citrus fruit. Plant Physiol. 109 (1995) 541-547
5. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSIBLAST a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
6. Antoniou A.N., Blackwood S.L., Mazzeo D., and Watts C. Control of antigen presentation by a single protease cleavage site. Immunity 12 (2000) 391-398
7. Benson D.A., Karsch-Mizrachi I., Lipman D.J., Ostell J., Rapp B.A., and Wheeler D.L. GenBank. Nucleic Acids Res. 30 (2002) 17-20
8. Bogin E., and Hadani A. Proteolytic enzyme activity in the gut of Hyalomma excavatum female ticks. Z. Parasitenkd. 41 (1973) 139-146
9. Boldbaatar D., Sikasunge C.S., Battsetseg B., Xuan X., and Fujisaki K. Molecular cloning and functional characterization of an aspartic protease from the hard tick Haemaphysalis longicornis. Insect Biochem. Mol. Biol. 36 (2006) 25-36
10. Brindley P.J., Kalinna B.H., Dalton J.P., Day S.R., Wong J.Y., Smythe M.L., and McManus D.P. Proteolytic degradation of host hemoglobin by schistosomes. Mol. Biochem. Parasitol. 89 (1997) 1-9
11. Chen J.M., Dando P.M., Rawlings N.D., Brown M.A., Young N.E., Stevens R.A., Hewitt E., Watts C., and Barrett A.J. Cloning, isolation and characterization of mammalian legumain, an asparaginyl endopeptidase. J. Biol. Chem. 272 (1997) 8090-8098
12. Chen J.M., Dando P.M., Stevens R.A.E., Fortunato M., and Barrett A.J. Cloning and expression of mouse legumain, a lysosomal endopeptidase. Biochem. J. 335 (1998) 111-117
13. Chen J.M., Rawlings N.D., Stevens R.A.E., and Barrett A.J. Identification of the active site of legumain links it to caspases, clostripain and gingipains in a new clan of cysteine endopeptidases. FEBS Lett. 441 (1998) 361-365
14. Choi J.S., Reddy V.S., Devlin D.R., Menna C., Chung H., Boyce B.F., and Roodman D.G. Identification of human asparaginyl endopeptidase (legumain) as an inhibitor of osteoclast formation and bone resorption. J. Biol. Chem. 274 (1999) 27747-27753
15. Coons L.B., Rosell-Davis R., and Tarnowski B.I. Blood meal digestion in ticks. In: Sauer J.R., and Hair J.A. (Eds). Morphology, Physiology and Behavioural Biology of Ticks (1986), Ellis Harwood, Wiley, New York 248-279
16. Dalton J.P., and Brindley P.J. Schistosome asparaginyl endopeptidase Sm32 in hemoglobin digestion. Parasitol. Today 12 (1996) 125
17. Dalton J.P., Hola-Jamriska L., and Brindley P.J. Asparaginyl endopeptidase activity in adult Schistosoma mansoni. Parasitology 111 (1995) 575-580
18. Dando P.M., Fortunato M., Smith L., Knight C.G., McKendrick J.E., and Barrett A.J. Pig kidney legumain: an asparaginyl endopeptidase with restricted specificity. Biochem. J. 339 (1999) 743-749
19. Davis A.H., Nanduri J., and Watson D.C. Cloning and gene expression of Schistosoma mansoni protease. J. Biol. Chem. 262 (1987) 12851-12855
20. D'Souza S.E., Ginsberg M.H., and Plow E.F. Arginyl-glycyl-aspartic acid (RGD): a cell adhesion motif. Trends Biochem. Sci. 16 (1991) 246-250
21. Eggleson K.K., Duffin K.L., and Goldberg D.E. Identification and characterization of falcilysin, a metallopeptidase involved in hemoglobin catabolism within the malaria parasite Plasmodium falciparum. J. Biol. Chem. 274 (1999) 32411-32417
22. El Meanawy M.A., Aji T., Phillips N.F.B., Davis R.E., Salata R.A., Malhotra I., McClain D., Aikawa M., and Davis A.H. Definition of the complete Schistosoma mansoni hemoglobinase mRNA sequence and gene expression in developing parasites. Am. J. Trop. Med. Hyg. 43 (1990) 67-78
23. Fujisaki K. Development of acquired resistance and precipitating antibody in rabbits experimentally infested with females of Haemaphysalis longicornis (Ixodoidea: Ixodidae). Natl. Inst. Anim. Health Q. (Tokyo) 18 (1978) 27-83
24. Fujisaki K., Kawazu S., and Kamio T. The taxonomy of the bovine Theileria spp. Parasitol. Today 10 (1994) 31-33
25. Furuse M., Fujita K., Hiiragi T., Fujimoto K., and Tsukita S. Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J. Cell Biol. 141 (1998) 1539-1550
26. Gould R.J., Polokoff M.A., Friedman P.A., Huang T.F., Holt J.C., Cook J.J., and Niewiarowski S. Disintegrins: a family of integrin inhibitory proteins from viper venoms. Proc. Soc. Exp. Biol. Med. 195 (1990) 168-171
27. Hara-Nishimura I., Inoue K., and Nishimura M. A unique vacuolar processing enzyme responsible for conversion of several proprotein precursors into the mature forms. FEBS Lett. 294 (1991) 89-93
28. Hara-Nishimura I., Takeuchi Y., and Nishimura M. Molecular characterization of a vacuolar processing enzyme related to a putative cystyeine proteinase of Schistosoma mansoni. Plant cell 5 (1993) 1651-1659
29. Hara-Nishimura I., Shimada T., Hiraiwa N., and Nishimura M. Vacuolar processing enzyme responsible for maturation of seed protein. J. Plant Physiol. 145 (1995) 6412-6417
30. Hatta T., Kazama K., Miyoshi T., Umemiya R., Liao M., Inoue N., Xuan X., Tsuji N., and Fujisaki K. Identification and characterization of a leucine aminopeptidase from the hard tick Haemaphysalis longicornis. Int. J. Parasitol. 36 (2006) 1123-1132
31. Ho T., Htwe K.K., Yamasaki N., Zhang G.Q., Ogawa M., Yamaguchi T., Fukushi H., and Hirai K. Isolation of Coxiella burnetii from dairy cattle and ticks, and some characteristics of the isolates in Japan. Microbiol. Immunol. 39 (1995) 663-671
32. Hoogstraal H., Roberts F.H., Kohls G.M., and Tipton V.J. Review of Haemaphysalis (Kaiseriana) longicornis Neumann (resurrected) of Australia, New Zealand, New Caledonia, Fiji, Japan, Korea, and northeastern China and USSR, and its parthenogenetic and bisexual populations (Ixodoidea, Ixodidae). J. Parasitol. 54 (1968) 1197-1213
33. Ishii S. Legumain: asparaginyl endopeptidase. Methods Enzymol 244 (1994) 604-625
34. Kembhavi A.A., Buttle D.J., Knight C.G., and Barrett A.J. The two cysteine endopeptidases of legume seeds: purification and characterization by use of specific fluorometric assays. Arch. Biochem. Biophys. 303 (1993) 208-213
35. Koh K., Mori T., Shiraishi S., and Uchida T.A. Ultrastructural changes of the midgut epithelial cells in feeding and moulting nymphs of the tick Haemaphysalis longicornis. Int. J. Parasitol. 21 (1991) 23-36
36. Kyte J., and Doolittle R.F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157 (1982) 105-132
37. Majima E., Koike H., Hong Y.M., Shinohara Y., and Terada H. Characterization of cysteine residues mitochondrial ADP/ATP carrier with the SH-reagents cosin 5-maleimide and N-ethylmaleimide. J. Biol. Chem. 286 (1993) 22181-22187
38. Manoury B., Hewitt W.E., Morrice N., Dando P.M., Barrett A.J., and Watts C. An asparaginyl endopeptidase processes a microbial antigen for class II MHC presentation. Nature 396 (1998) 695-699
39. Miyoshi T., Tsuji N., Islam M.K., Kamio T., and Fujisaki K. Cloning and molecular characterization of a cubilin-related serine proteinase from the hard tick Haemaphysalis longicornis. Insect Biochem. Mol. Biol. 34 (2004) 799-808
40. Needham G.R., and Teel P.D. Off-host physiological ecology of ixodid ticks. Annu. Rev. Entomol. 36 (1991) 659-681
41. Nielsen H., Engelbrecht J., Brunak S., and Heijne G. Identification of prokaryotic and eukaryotic signal peptides and predictions of their cleavage sites. Protein Eng. Des. Sel. 10 (1997) 1-6
42. Oliver E.M., Skuce P.J., McNair C.M., and Knox D.P. Identification and characterization of an asparaginyl proteinase (Legumain) from the parasitic nematode, Haemonchus contortus. Parasitology 133 (2006) 237-244
43. Ruoslahti E., and Pierschbacher M.D. Arg-Gly-Asp: a versatile cell recognition signal. Cell 44 (1986) 517-518
44. Sajid M., Mckerrow J.H., Hansell E., Mathieu M.A., Lucas K.D., Hsieh I., Greenbaum D., Bogyo M., Salter J.P., Lim K.C., Franklin C., Kim J., and Caffrey C.R. Functional expression and characterization of Schistosoma mansoni cathepsin B and its trans-activation by an endogenous asparaginyl endopeptidase. Mol. Biochem. Parasitol. 131 (2003) 65-75
45. Shutov A.D., and Vaintraub I.A. Degradation of storage proteins in germinating seeds. Phytochemistry 26 (1987) 1557-1566
46. Sojka D., Hajdusek O., Dvorak J., Sajid M., Franta Z., Schneider E.L., Craik C.S., Vancova M., Buresova V., Bogyo M., Sexton K.B., McKerrow J.H., Caffrey C.R., and Kopacek P. IrAE-An asparaginyl endopeptidase (legumain) in the gut of the hard tick Ixodes ricinus. Int. J. Parasitol. 37 (2007) 713-724 10.1016/j.ijpara.2006.12.020
47. Tarnowski B.I., and Coons L.B. Ultrastructure of the midgut and blood meal digestion in the adult tick Dermacentor variabilis. Exp. Appl. Acarol. 6 (1989) 263-289
48. Terra W.R., and Ferreira C. Insect digestive enzymes: properties, compartmentalization and function. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 109 (1994) 1-62
49. Tsuji N., Kamio T., Isobe T., and Fujisaki K. Molecular characterization of a peroxiredoxin from the hard tick Haemaphysalis longicornis. Insect Mol. Biol. 10 (2001) 121-129
50. Wilkins M.R., Lindskog I., Gasteiger E., Bairoch A., Sanchez J.C., Hochstrasser D.F., and Appel R.D. Detailed peptide characterization using PEPTIDE MASS-a World Wide Web accessible tool. Electrophoresis 18 (1997) 403-408
51. Williamson A.L., Lecchi P., Turk B.E., Choe Y., Hotez P.J., McKerrow J.H., Cantley L.C., Sajid M., Craik C.S., and Loukas A. A multi-enzyme cascade of hemoglobin proteolysis in the intestine of blood-feeding hookworms. J. Biol. Chem. 279 (2004) 35950-35957
52. Yamane T., Takeuchi K., Yamamoto Y., Li Y.-H., Fujiwara M., Nishi K., Takahashi S., and Ohkubo I. Legumain from bovine kidney: its purification, molecular cloning, immunohistochemical localization and degradation of annexin II and vitamin D-binding protein. Biochim. Biophys. Acta 1596 (2002) 108-120
53. You M., Xuan X., Tsuji N., Kamio T., Igarashi I., Nagasawa H., Mikami T., and Fujisaki K. Molecular characterization of a troponin I-like protein from the hard tick Haemaphysalis longicornis. Insect Biochem. Mol. Biol. 32 (2001) 67-73
54. You M., Xuan X., Tsuji N., Kamio T., Taylor D., Suzuki N., and Fujisaki K. Identification and molecular characterization of a chitinase from the hard tick Haemaphysalis longicornis. J. Biol. Chem. 278 (2003) 8556-8563
55. Zaim M., and Guillet P. Alternative insecticides: an urgent need. Trends Parasitol. 18 (2002) 161-163