Transcriptomic analysis in the leech Theromyzon tessulatum: Involvement of cystatin B in innate immunity

Biochemical Journal

Volumn 380, Issue 3, 2004, Pages 617-625

  Lefebvre, Christophe ^a   Cocquerelle, Claude ^a   Vandenbulcke, Franck ^a   Hot, David ^b   Huot, Ludovic ^b   Lemoine, Yves ^a,b   Salzet, Michel ^a  

^a CNRS   (France)

^b INSTITUT PASTEUR DE LILLE   (France)

Author keywords

cDNA microarray; Cystatin B; Differential display reverse transcriptase (RT) PCR; Innate immunity; Leech; Theromyzon tessulatum

Indexed keywords

AMINO ACIDS; BACTERIOLOGY; CELLS; CLONING; CORROSION INHIBITORS; DNA; GENES; PROTEINS;

INVERTEBRATE GROUPS; MICROARRAYS; REVERSE TRANSCRIPTASE (RT); TRANSCRIPTOMIC ANALYSIS;

GENETIC ENGINEERING;

ALPHA TUBULIN; CYSTATIN B; CYSTEINE PROTEINASE; GLUTAMINE; GLYCINE; MALATE DEHYDROGENASE; POLYADENYLIC ACID BINDING PROTEIN; THREONINE DEHYDRATASE; VALINE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CAENORHABDITIS ELEGANS; DIFFERENTIAL DISPLAY; DNA MICROARRAY; DROSOPHILA MELANOGASTER; GENE IDENTIFICATION; GENE STRUCTURE; GENETIC ANALYSIS; HUMORAL IMMUNITY; IMMUNOCYTOCHEMISTRY; IMMUNOMODULATION; IMMUNOSTIMULATION; IN SITU HYBRIDIZATION; LEECH; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROVOCATION TEST; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CYSTATINS; CYSTEINE PROTEINASE INHIBITORS; ESCHERICHIA COLI; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, NATURAL; LEECHES; MICE; MICROCOCCUS LUTEUS; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION, GENETIC; UP-REGULATION;

ANNELIDA; BACTERIA (MICROORGANISMS); CAENORHABDITIS; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; ECDYSOZOA; HEXAPODA; HIRUDINIDA; INVERTEBRATA; MELANOGASTER; THEROMYZON; THEROMYZON TESSULATUM; VERTEBRATA;

EID: 3042704064     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20040478     Document Type: Article

References (56)

1. Lemaitre, B., Kromer-Metzger, E., Michaut, L., Nicolas, E., Meister, M., Georgel, P., Reichhart, J. M. and Hoffmann, J. A. (1995) A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense. Proc. Natl. Acad. Sci. U.S.A. 92, 9465-9469
2. Lemaitre, B., Nicolas, E., Michaut, L., Reichhart, J. M. and Hoffmann, J. A. (1996) The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86, 973-983
3. Medzhitov, R. and Janeway, Jr, C. A. (1997) Innate immunity: impact on the adaptive immune response. Curr. Opin. Immunol. 9, 4-9
4. Hoffmann, J. A. and Reichhart, J. M. (2002) Drosophila innate immunity: an evolutionary perspective. Nat. Immunol. 3, 121-126
5. Salzet, M. (2001) Vertebrate innate immunity resembles a mosaic of invertebrate immune responses. Trends Immunol. 22, 285-288
6. De Gregorio, E., Spellman, P. T., Rubin, G. M. and Lemaitre, B. (2001) Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc. Natl. Acad. Sci. U.S.A. 98, 12590-12595
7. Irving, P, Troxler, L., Heuer, T. S., Belvin, M., Kopczynski, C., Reichhart, J. M., Hoffmann, J. A. and Hetru, C. (2001) A genome-wide analysis of immune responses in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 98, 15119-15124
8. Levy, F., Bulet, P. and Ehret-Sabatier, L. (2004) Proteomic analysis of the systemic immune response of Drosophila. Mol. Cell. Proteomics 3, 156-166
9. Vierstraete, E., Verleyen, P., Baggerman, G., D'Hertog, W., Van den Bergh, G., Arckens, L., De Loof, A. and Schoofs, L. (2004) A proteomic approach for the analysis of instantly released wound and immune proteins in Drosophila melanogaster hemolymph. Proc. Natl. Acad. Sci. U.S.A. 101, 470-475
10. Hoffmann, J. A. (2003) The immune response of Drosophila. Nature (London) 426, 33-38
11. Malecha, J., Verger-Bocquet, M. and Tramu, G. (1989) Mise en évidence et évolution, au cours du cycle biologique, de neurones producteurs d'une substance apparentèe à la motiline porcine dans le ganglion supraoesophagien de la sangsue Theromyzon tessulatum. Can. J. Zool. 67, 636-640
12. Liang, P. and Pardee, A. B. (1992) Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257, 967-971
13. Frohman, M. A., Dush, M. K. and Martin, G. R. (1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc. Natl. Acad. Sci. U.S.A. 85, 8998-9002
14. Karlin, S. and Altschul, S. F. (1990) Methods for assessing the statistical significance of molecular sequence features by using general scoring schemes. Proc. Natl. Acad. Sci. U.S.A. 87, 2264-2268
15. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402
16. Schena, M., Shalon, D., Davis, R. W. and Brown, P. O. (1995) Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270, 467-470
17. Mitta, G., Vandenbulcke, F., Noel, T., Romestand, B., Beauvillain, J. C., Salzet, M. and Roch, P. (2000) Differential distribution and defence involvement of antimicrobial peptides in mussel. J. Cell Sci. 113, 2759-2769
18. Munoz, M., Vandenbulcke, F., Saulnier, D. and Bachere, E. (2002) Expression and distribution of penaeidin antimicrobial peptides are regulated by haemocyte reactions in microbial challenged shrimp. Eur. J. Biochem. 269, 2678-2689
19. Ali, M., Markham, A. F. and Isaacs, J. D. (2001) Application of differential display to immunological research. J. Immunol. Methods 250, 29-43
20. Tasiemski, A., Vandenbulcke, F., Mitta, G., Lemoine, J., Lefebvre, C., Sautiere, P. E. and Salzet, M. (2003) Molecular characterization of two novel antibacterial peptides inducible upon bacterial challenge in an annelid: the leech Theromyzon tessulatum. J. Biol. Chem. (2004) DOI 10.1074/jbc.M312156200
21. Anastasi, A., Brown, M. A., Kembhavi, A. A., Nicklin, M. J., Sayers, C. A., Sunter, D. C. and Barrett, A. J. (1983) Cystatin, a protein inhibitor of cysteine proteinases. Improved purification from egg white, characterization, and detection in chicken serum. Biochem. J. 211, 129-138
22. Barrera, C., Ye, G., Espejo, R., Gunasena, S., Almanza, R., Leary, J., Crowe, S., Ernst, P. and Reyes, V. E. (2001) Expression of cathepsins B, L, S, and D by gastric epithelial cells implicates them as antigen presenting cells in local immune responses. Hum. Immunol. 62, 1081-1091
23. Riese, R. J. and Chapman, H. A. (2000) Cathepsins and compartmentalization in antigen presentation. Curr. Opin. Immunol. 12, 107-113
24. Tryselius, Y. and Hultmark, D. (1997) Cysteine proteinase 1 (CP1), acathepsin L-like enzyme expressed in the Drosophila melanogaster haemocyte cell line mbn-2. Insect Mol. Biol. 6, 173-181
25. Reverter, D., Sorimachi, H. and Bode, W. (2001) The structure of calcium-free human m-calpain: implications for calcium activation and function. Trends Cardiovasc. Med. 11, 222-229
26. Pol, E. and Bjork, I. (2001) Role of the single cysteine residue, Cys 3, of human and bovine cystatin B (stefin B) in the inhibition of cysteine proteinases. Protein Sci. 10, 1729-1738
27. Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16, 10881-10890
28. Takeuchi, H., Fujiyuki, T., Shirai, K., Matsuo, Y., Kamikouchi, A., Fujinawa, Y., Kato, A., Tsujimoto, A. and Kubo, T. (2002) Identification of genes expressed preferentially in the honeybee mushroom bodies by combination of differential display and cDNA microarray. FEBS Lett. 513, 230-234
29. Green, C. D., Simons, J. F., Taillon, B. E. and Lewin, D. A. (2001) Open systems: panoramic views of gene expression. J. Immunol. Methods 250, 67-79
30. Crawford, D. L. (2001) Functional genomics does not have to be limited to a few select organisms. Genome Biol. 2, interactions 1001.1-1001.2
31. Samach, A., Broday, L., Hareven, D. and Lifschitz, E. (1995) Expression of an amino acid biosynthesis gene in tomato flowers: developmental upregulation and MeJa response are parenchyma-specific and mutually compatible. Plant J. 8, 391-406
32. Hildmann, T., Ebneth, M., Pena-Cortes, H., Sanchez-Serrano, J. J., Willmitzer, L. and Prat, S. (1992) General roles of abscisic and jasmonic acids in gene activation as a result of mechanical wounding. Plant Cell 4, 1157-1170
33. Thomma, B. P., Eggermont, K., Tierens, K. F. and Broekaert, W. F. (1999) Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiol. 121, 1093-1102
34. Feys, B. J. and Parker, J. E. (2000) Interplay of signaling pathways in plant disease resistance. Trends Genet. 16, 449-455
35. Suzuki, T., Hashimoto, S., Toyoda, N., Nagai, S., Yamazaki, N., Dong, H. Y., Sakai, J., Yamashita, T., Nukiwa, T. and Matsushima, K. (2000) Comprehensive gene expression profile of LPS-stimulated human monocytes by SAGE. Blood 96, 2584-2591
36. Hashimoto, S., Suzuki, T., Dong, H. Y., Yamazaki, N. and Matsushima, K. (1999) Serial analysis of gene expression in human monocytes and macrophages. Blood 94, 837-844
37. Lee, D. G., Park, Y., Kim, H. N., Kim, H. K., Kim, P. I., Choi, B. H. and Hahm, K. S. (2002) Antifimgal mechanism of an antimicrobial peptide, HP (2-20), derived from N-terminus of Helicobacter pylori ribosomal protein L1 against Candida albicans. Biochem. Biophys. Res. Commun. 291, 1006-1013
38. Putsep, K., Branden, C. I., Boman, H. G. and Normark, S. (1999) Antibacterial peptide from H. pylori. Nature (London) 398, 671-672
39. Putsep, K., Normark, S. and Boman, H. G. (1999) The origin of cecropins; implications from synthetic peptides derived from ribosomal protein L1. FEBS Lett. 451, 249-252
40. Yang, H., Duckett, C. S. and Lindsten, T. (1995) iPABP, an inducible poly(A)-binding protein defected in activated human T cells. Mol. Cell. Biol. 15, 6770-6776
41. Miller, R. A., Garcia, G., Kirk, C. J. and Witkowski, J. M. (1997) Early activation defects in T lymphocytes from aged mice. Immunol. Rev. 160, 79-90
42. Krasnow, S, W., Zhang, L. Q., Leung, K. Y., Osborn, L., Kunkel, S. and Nabel, G. J. (1991) Tumor necrosis factor-alpha, interleukin 1, and phorbol myristate acetate are independent activators of NF-kappa B which differentially activate T cells. Cytokine 3, 372-379
43. Sachs, A. B. and Oeardorff, J. A. (1992) Translation initiation requires the PAB-dependent poly(A) ribonuclease in yeast. Cell 70, 961-973
44. Rawlings, N. D. and Barrett, A. J. (1990) Evolution of proteins of the cystatin superfamily. J. Mol. Evol. 30, 60-71
45. Barrett, A. J., Fritz, H., Grubb, A., Isemura, S., Jarvinen, M., Katunuma, N., Machleidt, W., Muller-Esterl, W., Sasaki, M. and Turk, V. (1986) Nomenclature and classification of the proteins homologous with the cysteine-proteinase inhibitor chicken cystatin. Biochem. J. 236, 312
46. Thiele, U., Auerswald, E. A., Gebhard, W., Assfalg-Machleidt, I., Popovic, T. and Machleidt, W. (1988) Inhibitorily active recombinant human stefin B. Gene synthesis, expression and isolation of an inhibitory active MS-2 pol-stefin B fusion protein and preparation of Des[Met1,2(2)]stefin B. Biol. Chem. Hoppe Seyler 369, 1167-1178
47. Turk, B., Colic, A., Stoka, V. and Turk, V. (1994) Kinetics of inhibition of bovine cathepsin S by bovine stefin B. FEBS Lett. 339, 155-159
48. Cimerman, N., Mesko Brguljan, P., Krasovec, M., Suskovic, S. and Kos, J. (2001) Serum concentration and circadian profiles of cathepsins B, H and L, and their inhibitors, stefins A and B, in asthma. Clin. Chim. Acta 310, 113-122
49. Kos, J. and Lan, T. T. (1998) Cysteine proteinases and their endogenous inhibitors: target proteins for prognosis, diagnosis and therapy in cancer. Oncol. Rep. 5, 1349-1361
50. Pennacchio, L. A., Lehesjoki, A. E., Stone, N. E., Willour, V. L., Virtaneva, K., Miao, J., O'Amato, E., Ramirez, L., Faham, M., Koskiniemi, M. et al. (1996) Mutations in the gene encoding cystatin B in progressive myoclonus epilepsy (EPM1). Science 271, 1731-1734
51. Pennacchio, L. A., Bouley, D. M., Higgins, K. M., Scott, M. P., Noebels, J. L. and Myers, R. M. (1998) Progressive ataxia, myoclonic epilepsy and cerebellar apoptosis in cystatin B-deficient mice. Nat. Genet. 20, 251-258
52. Riccio, M., Di Giaimo, R., Pianetti, S., Palmieri, P. P., Melli, M. and Santi, S. (2001) Nuclear localization of cystatin B, the cathepsin inhibitor implicated in myoclonus epilepsy (EPM1). Exp. Cell. Res. 262, 84-94
53. Houseweart, M. K., Pennacchio, L. A., Vilaythong, A., Peters, C., Noebels, J. L. and Myers, R. M. (2003) Cathepsin B but not cathepsins L or S contributes to the pathogenesis of Unverricht-Lundborg progressive myoclonus epilepsy (EPM1). J. Neurobiol. 56, 315-327
54. Lieuallen, K., Pennacchio, L. A., Park, M., Myers, R. M. and Lennon, G. G. (2001) Cystatin B-deficient mice have increased expression of apoptosis and glial activation genes. Hum. Mol. Genet. 10, 1867-1871
55. Muno, D., Kominami, E. and Mizuochi, T. (2000) Generation of both MHC class I- and class II-restricted antigenic peptides from exogenously added ovalbumin in murine phagosomes. FEBS Lett. 478, 178-182
56. Schierack, P., Lucius, R., Sonnenburg, B., Schilling, K. and Hartmann, S. (2003) Parasite-specific immunomodulatory functions of filarial cystatin. Infect. Immun. 71, 2422-2429