Startseite Lebenswissenschaften Two secreted cystatins of the soft tick Ornithodoros moubata: differential expression pattern and inhibitory specificity
Artikel
Lizenziert
Nicht lizenziert Erfordert eine Authentifizierung

Two secreted cystatins of the soft tick Ornithodoros moubata: differential expression pattern and inhibitory specificity

  • , , , , , und
Veröffentlicht/Copyright: 28. November 2006
Biological Chemistry
Aus der Zeitschrift Band 387 Heft 12

Abstract

Two genes coding for cysteine peptidase inhibitors of the cystatin family (Om-cystatin 1 and 2) were isolated from a gut-specific cDNA library of the soft tick Ornithodoros moubata. Both cystatins were clearly down-regulated after a blood meal. Om-cystatin 1 is mainly expressed in the tick gut, while Om-cystatin 2 mRNA was also found in other tick tissues. Authentic Om-cystatin 2 was significantly more abundant than Om-cystatin 1 in the gut contents of fasting ticks and was associated with hemosome-derived residual bodies accumulated in the gut lumen. Om-cystatin 2 was also expressed by type 2 secretory cells in the salivary glands of unfed ticks. The inhibitory specificity of recombinant Om-cystatins 1 and 2 was tested with mammalian cysteine peptidases, as well as endogenous cysteine peptidases present in the tick gut. Both cystatins efficiently inhibited papain-like peptidases, including cathepsin B and H, but differed significantly in their affinity towards cathepsin C and failed to block asparaginyl endopeptidase. Our results suggest that the secreted cystatin isoinhibitors are involved in the regulation of multiple proteolytic targets in the tick digestive system and tick-host interaction.

:

Corresponding author

References

Abrahamson, M. (1994). Cystatins. Methods Enzymol.244, 685–700.10.1016/0076-6879(94)44051-4Suche in Google Scholar

Adkison, A.M., Raptis, S.Z., Kelley, D.G., and Pham, C.T. (2002). Dipeptidyl peptidase I activates neutrophil-derived serine proteases and regulates the development of acute experimental arthritis. J. Clin. Invest.109, 363–371.10.1172/JCI0213462Suche in Google Scholar

Agarwala, K.L., Kawabata, S., Hirata, M., Miyagi, M., Tsunasawa, S., and Iwanaga, S. (1996). A cysteine protease inhibitor stored in the large granules of horseshoe crab hemocytes: purification, characterization, cDNA cloning and tissue localization. J. Biochem. (Tokyo).119, 85–94.10.1093/oxfordjournals.jbchem.a021220Suche in Google Scholar

Alvarez-Fernandez, M., Barrett, A.J., Gerhartz, B., Dando, P.M., Ni, J., and Abrahamson, M. (1999). Inhibition of mammalian legumain by some cystatins is due to a novel second reactive site. J. Biol. Chem.274, 19195–19203.10.1074/jbc.274.27.19195Suche in Google Scholar

Balashov, I.S. (1979). An Atlas of Electron Microscopical Anatomy of Ixodid Ticks (Leningrad, Russia: USSR Academy of Sciences/Nauka Publishers).Suche in Google Scholar

Barrett, A.J. and Kirschke, H. (1981). Cathepsin B, cathepsin H, and cathepsin L. Methods Enzymol.80, 535–561.10.1016/S0076-6879(81)80043-2Suche in Google Scholar

Barrett, A.J., Rawlings, N.D., Davies, M.E., Machleidt, W., Salvesen, G., and Turk, V. (1986). Cysteine proteinase inhibitors of the cystatin superfamily. In: Proteinase inhibitors. A.J. Barrett and G. Salvesen, eds. (Amsterdam, Netherlands: Elsevier), pp. 515–569.Suche in Google Scholar

Belaaouaj, A. (2002). Neutrophil elastase-mediated killing of bacteria: lessons from targeted mutagenesis. Microbes Infect.4, 1259–1264.10.1016/S1286-4579(02)01654-4Suche in Google Scholar

Bieth, J.G. (1995). Theoretical and practical aspects of proteinase inhibition kinetics. Methods Enzymol.248, 59–84.10.1016/0076-6879(95)48007-2Suche in Google Scholar

Bode, W., Engh, R., Musil, D., Thiele, U., Huber, R., Karshikov, A., Brzin, J., Kos, J., and Turk, V. (1988). The 2.0 Å X-ray crystal structure of chicken egg white cystatin and its possible mode of interaction with cysteine proteinases. EMBO J.7, 2593–2599.Suche in Google Scholar

Boldbaatar, D., Sikalizyo Sikasunge, C., Battsetseg, B., Xuan, X., and Fujisaki, K. (2006). Molecular cloning and functional characterization of an aspartic protease from the hard tick Haemaphysalis longicornis. Insect Biochem. Mol. Biol.36, 25–36.10.1016/j.ibmb.2005.10.003Suche in Google Scholar PubMed

Burg, N.D. and Pillinger, M.H. (2001). The neutrophil: function and regulation in innate and humoral immunity. Clin. Immunol.99, 7–17.10.1006/clim.2001.5007Suche in Google Scholar PubMed

Caffrey, C.R. and Ruppel, A. (1997). Cathepsin B-like activity predominates over cathepsin L-like activity in adult Schistosoma mansoni and S. japonicum. Parasitol. Res.83, 632–635.10.1007/s004360050310Suche in Google Scholar PubMed

Caffrey, C.R., McKerrow, J.H., Salter, J.P., and Sajid, M. (2004). Blood ‘n’ guts: an update on schistosome digestive peptidases. Trends Parasitol.20, 241–248.10.1016/j.pt.2004.03.004Suche in Google Scholar

Colella, R., Sakaguchi, Y., Nagase, H., and Bird, J.W. (1989). Chicken egg white cystatin. Molecular cloning, nucleotide sequence, and tissue distribution. J. Biol. Chem.264, 17164–17169.10.1016/S0021-9258(18)71473-7Suche in Google Scholar

Coons, L.B., Rosell-Davis, R., and Tarnowski, B.I. (1986). Bloodmeal digestion in ticks. In: Morphology, Physiology, and Behavioral Biology of Ticks. J.R. Sauer and J.A. Hair, eds. (Chichester, UK: Ellis Horwood), pp. 248–279.Suche in Google Scholar

Dodt, J. and Reichwein, J. (2003). Human cathepsin H: deletion of the mini-chain switches substrate specificity from aminopeptidase to endopeptidase. Biol. Chem.384, 1327–1332.10.1515/BC.2003.149Suche in Google Scholar

Grandjean, O. (1984). Blood digestion in Ornithodoros moubata Murray sensu stricto Walton (Ixodoidea: Argasidae) females. I. Biochemical changes in the midgut lumen and ultrastructure of the midgut cells, related to intracellular digestion. Acarologia25, 147–165.Suche in Google Scholar

Grunclová, L., Fouquier, H., Hypša, V., and Kopáček, P. (2003). Lysozyme from the gut of the soft tick Ornithodoros moubata: the sequence, phylogeny and post-feeding regulation. Dev. Comp. Immunol.27, 651–660.10.1016/S0145-305X(03)00052-1Suche in Google Scholar

Hartmann, S. and Lucius, R. (2003). Modulation of host immune responses by nematode cystatins. Int. J. Parasitol.33, 1291–1302.10.1016/S0020-7519(03)00163-2Suche in Google Scholar

Hsing, L.C. and Rudensky, A.Y. (2005). The lysosomal cysteine proteases in MHC class II antigen presentation. Immunol. Rev.207, 229–241.10.1111/j.0105-2896.2005.00310.xSuche in Google Scholar

Karim, S., Miller, N.J., Valenzuela, J., Sauer, J.R., and Mather, T.N. (2005). RNAi-mediated gene silencing to assess the role of synaptobrevin and cystatin in tick blood feeding. Biochem. Biophys. Res. Commun.334, 1336–1342.10.1016/j.bbrc.2005.07.036Suche in Google Scholar

Kevil, C.G., Walsh, L., Laroux, F.S., Kalogeris, T., Grisham, M.B., and Alexander, J.S. (1997). An improved, rapid Northern protocol. Biochem. Biophys. Res. Commun.238, 277–279.10.1006/bbrc.1997.7284Suche in Google Scholar

Khaznadji, E., Collins, P., Dalton, J.P., Bigot, Y., and Moire, N. (2005). A new multi-domain member of the cystatin superfamily expressed by Fasciola hepatica. Int. J. Parasitol.35, 1115–1125.10.1016/j.ijpara.2005.05.001Suche in Google Scholar

Kopáček, P., Weise, C., and Götz, P. (1995). The prophenoloxidase from the wax moth Galleria mellonella: purification and characterization of the proenzyme. Insect Biochem. Mol. Biol.25, 1081–1091.10.1016/0965-1748(95)00040-2Suche in Google Scholar

Kopáček, P., Vogt, R., Jindrák, L., Weise, Ch., and Šafařík, I. (1999). Purification and characterization of the lysozyme from the gut of the soft tick Ornithodoros moubata. Insect Biochem. Mol. Biol.29, 989–997.10.1016/S0965-1748(99)00075-2Suche in Google Scholar

Kopáček, P., Ždychová, J., Yoshiga, T., Weise, C., Rudenko, N., and Law, J.H. (2003). Molecular cloning, expression and isolation of ferritins from two tick species Ornithodoros moubata and Ixodes ricinus. Insect Biochem. Mol. Biol.33, 103–113.10.1016/S0965-1748(02)00181-9Suche in Google Scholar

Lara, F.A., Lins, U., Paiva-Silva, G., Almeida, I.C., Braga, C.M., Miguens, F.C., Oliveira, P.L., and Dansa-Petretski, M. (2003). A new intracellular pathway of haem detoxification in the midgut of the cattle tick Boophilus microplus: aggregation inside a specialized organelle, the hemosome. J. Exp. Biol.206, 1707–1715.10.1242/jeb.00334Suche in Google Scholar

Lara, F.A., Lins, U., Bechara, G.H., and Oliveira, P.L. (2005). Tracing heme in a living cell: hemoglobin degradation and heme traffic in digest cells of the cattle tick Boophilus microplus. J. Exp. Biol.208, 3093–3101.10.1242/jeb.01749Suche in Google Scholar

Lustigman, S., Brotman, B., Huima, T., Prince, A.M., and McKerrow, J.H. (1992). Molecular cloning and characterization of onchocystatin, a cysteine proteinase inhibitor of Onchocerca volvulus. Biol. Chem.267, 17339–17346.10.1016/S0021-9258(18)41931-XSuche in Google Scholar

Machleidt, W., Thiele, U., Laber, B., Assfalg-Machleidt, I., Esterl, A., Wiegand, G., Kos, J., Turk, V., and Bode, W. (1989). Mechanism of inhibition of papain by chicken egg white cystatin. Inhibition constants of N-terminally truncated forms and cyanogen bromide fragments of the inhibitor. FEBS Lett.243, 234–238.10.1016/0014-5793(89)80135-8Suche in Google Scholar

Manoury, B., Hewitt, E.W., Morrice, N., Dando, P.M., Barrett, A.J., and Watts, C. (1998). An asparaginyl endopeptidase processes a microbial antigen for class II MHC presentation. Nature396, 695–699.10.1038/25379Suche in Google Scholar

McGuire, M.J., Lipsky, P.E., and Thiele, D.L. (1992). Purification and characterization of dipeptidyl peptidase I from human spleen. Arch. Biochem. Biophys.295, 280–288.10.1016/0003-9861(92)90519-3Suche in Google Scholar

Mendiola, J., Alonso, M., Marquetti, M.C., and Finlay, C. (1996). Boophilus microplus: multiple proteolytic activities in the midgut. Exp. Parasitol.82, 27–33.10.1006/expr.1996.0004Suche in Google Scholar PubMed

Mulenga, A., Sugimoto, C., Ingram, G., Ohashi, K., and Onuma, M. (1999). Molecular cloning of two Haemaphysalis longicornis cathepsin L-like cysteine proteinase genes. J. Vet. Med. Sci.61, 497–502.10.1292/jvms.61.497Suche in Google Scholar PubMed

Nakajima, Y., Ishibashi, J., Yukuhiro, F., Asaoka, A., Taylor, D., and Yamakawa, M. (2003a). Antibacterial activity and mechanism of action of tick defensin against Gram-positive bacteria. Biochim. Biophys. Acta1624, 125–130.10.1016/j.bbagen.2003.10.004Suche in Google Scholar

Nakajima, Y., Ogihara, K., Taylor, D., and Yamakawa, M. (2003b). Antibacterial hemoglobin fragments from the midgut of the soft tick, Ornithodoros moubata (Acari: Argasidae). J. Med. Entomol.40, 78–81.10.1603/0022-2585-40.1.78Suche in Google Scholar

Nelson, P.S., Hawkins, V., Schummer, M., Bumgarner, R., Ng, W.L., Ideker, T., Ferguson, C., and Hood, L. (1999). Negative selection: a method for obtaining low-abundance cDNAs using high-density cDNA clone arrays. Genet. Anal.15, 209–215.10.1016/S1050-3862(99)00006-6Suche in Google Scholar

Nicklin, M.J. and Barrett, A.J. (1984). Inhibition of cysteine proteinases and dipeptidyl peptidase I by egg-white cystatin. Biochem. J.223, 245–253.10.1042/bj2230245Suche in Google Scholar

Pham, C.T. and Ley, T.J. (1999). Dipeptidyl peptidase I is required for the processing and activation of granzymes A and B in vivo. Proc. Natl. Acad. Sci. USA96, 8627–8632.10.1073/pnas.96.15.8627Suche in Google Scholar

Renard, G., Garcia, J.F., Cardoso, F.C., Richter, M.F., Sakanari, J.A., Ozaki, L.S., Termignoni, C., and Masuda, A. (2000). Cloning and functional expression of a Boophilus microplus cathepsin L-like enzyme. Insect Biochem. Mol. Biol.30, 1017–1026.10.1016/S0965-1748(00)00070-9Suche in Google Scholar

Renard, G., Lara, F.A., de Cardoso, F.C., Miguens, F.C., Dansa-Petretski, M., Termignoni, C., and Masuda, A. (2002). Expression and immunolocalization of a Boophilus microplus cathepsin L-like enzyme. Insect Mol. Biol.11, 325–328.10.1046/j.1365-2583.2002.00342.xSuche in Google Scholar PubMed

Ribeiro, J.M., Alarcon-Chaidez, F.B., Francischetti, I.M., Mans, B.J., Mather, T.N., Valenzuela, J.G., and Wikel, S.K. (2006). An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks. Insect Biochem. Mol. Biol.36, 111–129.10.1016/j.ibmb.2005.11.005Suche in Google Scholar PubMed

Rotari, V.I., Dando, P.M., and Barrett, A.J. (2001). Legumain forms from plants and animals differ in their specificity. Biol. Chem.382, 953–959.10.1515/BC.2001.119Suche in Google Scholar PubMed

Schierack, P., Lucius, R., Sonnenburg, B., Schilling, K., and Hartmann, S. (2003). Parasite-specific immunomodulatory functions of filarial cystatin. Infect. Immun.71, 2422–2429.10.1128/IAI.71.5.2422-2429.2003Suche in Google Scholar PubMed PubMed Central

Sonenshine, D.E. (1991). Biology of Ticks, vol. 1 (New York, USA: Oxford University Press).Suche in Google Scholar

Turk, V. and Bode W. (1991). The cystatins: protein inhibitors of cysteine proteinases. FEBS Lett.285, 213–219.10.1016/0014-5793(91)80804-CSuche in Google Scholar

Varma, M.G. (1956). Infections of Ornithodoros ticks with relapsing fever spirochaetes, and the mechanisms of their transmission. Ann. Trop. Med. Parasitol.50, 18–31.10.1080/00034983.1956.11685735Suche in Google Scholar

Wardley, R.C., De M Andrade, C., Black, D.N., De Castro Portugal, F.L., Enjuanes, L., Hess, W.R., Mebus, C., Ordas, A., Rutili, D., Sanches Vizcaino, J., et al. (1983). African Swine Fever virus. Brief Rev. Arch. Virol.76, 73–90.10.1007/BF01311692Suche in Google Scholar

Williamson, A.L., Brindley, P.J., Knox, D.P., Hotez, P.J., and Loukas, A. (2003). Digestive proteases of blood-feeding nematodes. Trends Parasitol.9, 417–423.10.1016/S1471-4922(03)00189-2Suche in Google Scholar

Wolters, P.J., Raymond, W.W., Blount, J.L., and Caughey, G.H. (1998). Regulated expression, processing, and secretion of dog mast cell dipeptidyl peptidase I. J. Biol. Chem.273, 15514–15520.10.1074/jbc.273.25.15514Suche in Google Scholar PubMed

Published Online: 2006-11-28
Published in Print: 2006-12-01

©2006 by Walter de Gruyter Berlin New York

Artikel in diesem Heft

  1. Janus-faced role of endothelial NO synthase in vascular disease: uncoupling of oxygen reduction from NO synthesis and its pharmacological reversal
  2. Leucine aminopeptidases: diversity in structure and function
  3. Endogenous anti-inflammatory substances, inter-α-inhibitor and bikunin
  4. Mitochondrial morphology and distribution in mammalian cells
  5. Heterogeneity in the cysteine protease inhibitor clitocypin gene family
  6. Mutations in the inter-SH2 domain of the regulatory subunit of phosphoinositide 3-kinase: effects on catalytic subunit binding and holoenzyme function
  7. Evaluation of Bacillus anthracis thymidine kinase as a potential target for the development of antibacterial nucleoside analogs
  8. The human malaria parasite Plasmodium falciparum expresses an atypical N-terminally extended pyrophosphokinase with specificity for thiamine
  9. Fes1p acts as a nucleotide exchange factor for the ribosome-associated molecular chaperone Ssb1p
  10. Detailed analysis of MIA protein by mutagenesis
  11. The role of human tissue kallikreins 7 and 8 in intracranial malignancies
  12. Prognostic significance of the expression of SR-A1, encoding a novel SR-related CTD-associated factor, in breast cancer
  13. Suppression of TNF-α production by S-adenosylmethionine in human mononuclear leukocytes is not mediated by polyamines
  14. Topotecan and methotrexate alter expression of the apoptosis-related genes BCL2, FAS and BCL2L12 in leukemic HL-60 cells
  15. Two secreted cystatins of the soft tick Ornithodoros moubata: differential expression pattern and inhibitory specificity
  16. Acknowledgment
  17. Contents Biological Chemistry Volume 387, 2006
  18. Author Index
  19. Subject Index
Heruntergeladen am 2.4.2026 von https://www.degruyterbrill.com/document/doi/10.1515/BC.2006.204/html
Button zum nach oben scrollen