Cathepsin B from the white shrimp Litopenaeus vannamei: cDNA sequence analysis, tissues-specific expression and biological activity

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 161, Issue 1, 2012, Pages 32-40

  Stephens, A ^a   Rojo, L ^b   Araujo Bernal, S ^a   Garcia Carreno F ^b   Muhlia Almazan, A ^a  

^a CENTRO DE INVESTIGACIÓN EN ALIMENTACIÓN Y DESARROLLO   (Mexico)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS DEL NOROESTE   (Mexico)

Author keywords

Cathepsin B; Cystein proteinases; Genes expression; Shrimp; Starvation

Indexed keywords

COMPLEMENTARY DNA; CYSTEINE PROTEINASE; LITOPENAEUS VANNAMEI CATHEPSIN B; MESSENGER RNA; PROTEINASE; UNCLASSIFIED DRUG; CATHEPSIN B;

ARTICLE; DNA SEQUENCE; GENE EXPRESSION; LITOPENAEUS VANNAMEI; MIDGUT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STOMACH JUICE; AMINO ACID SEQUENCE; ANIMAL; ANTIBODY SPECIFICITY; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PENAEIDAE; SEQUENCE ALIGNMENT; STARVATION;

CRUSTACEA; DECAPODA (CRUSTACEA); DENDROBRANCHIATA; LITOPENAEUS VANNAMEI; PENAEIDAE; VERTEBRATA;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CATHEPSIN B; DNA, COMPLEMENTARY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; PENAEIDAE; PHYLOGENY; RNA, MESSENGER; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; STARVATION;

EID: 84863741111     PISSN: 10964959     EISSN: 18791107     Source Type: Journal    
DOI: 10.1016/j.cbpb.2011.09.004     Document Type: Article

References (52)

1. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25(17):3389-3402.
2. Aoki H., Ahsan M.N., Watabe S. Molecular cloning and characterization of cathepsin B from the hepatopancreas of northern shrimp Pandalus borealis. Comp. Biochem. Physiol. B 2003, 134:681-694.
3. Baig S., Damian R.T., Peterson D.S. A novel cathepsin B active site motif is shared by helminth bloodfeeders. Exp. Parasitol. 2002, 101:83-89.
4. Barrett A.J., Rawlings N.D., Woessner J.F. The Handbook of Proteolytic Enzymes 2004, Academic Press, London, 1666pp. 2nd ed.
5. Bown D.P., Wilkinson H., Jongsma M.A., Gatehouse J.A. Characterisation of cysteine proteinases responsible for digestive proteolysis in guts of larval western corn rootworm (Diabrotica virgifera) by expression in the yeast Pichia pastoris. Insect Biochem. Mol. Biol. 2004, 34:305-320.
6. Cardenas-Lopez J.L., Haard N. Cystein proteinase activity in jumbo squid (Dosidicus gigas) hepatopancreas extracts. J. Food Biochem. 2005, 29:171-186.
7. Cathers B.E., Barrett C., Palmer J.T., Rydzewski R.M. pH Dependence of inhibitors targeting the occluding loop of cathepsin B. Bioorg. Chem. 2002, 30:264-275.
8. Cho W.L., Tsao S.M., Hays A.R., Walter R., Chen J.S., Snigirevskaya E.S., Raikhel A.S. Mosquito Cathepsin B-like protease latent extraovarian precursor. J. Biol. Chem. 1999, 274(19):13311-13321.
9. Chomczynsky P., Sacchi N. Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987, 162:156-159.
10. Delcroix M., Sajid M., Caffre C., Lim K., Dvorak J., Hsieh I., Bahgat M., Dissous C., McKerrow J.H. A multienzyme network functions in intestinal protein digestion by a Platyhelminth parasite. J. Biol. Chem. 2006, 281(51):39316-39329.
11. Dyrlov B.J., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: signal P 3.0. J. Mol. Biol. 2004, 340:783-795.
12. Ellis, R.C., 2004. Characterization of Cathepsin B mRNA and protein expression, enzymatic activity and cellular localization following contusion spinal cord injury in rats. PhD Thesis. University of Florida. 85 pp.
13. Franta Z., Frantova H., Konvickova J., Horn M., Sojka D., Mares M., Kopacek P. Dynamics of digestive proteolytic system during blood feeding of the hard tick Ixodes ricinus. Parasit. Vectors 2010, 3:119.
14. Griffitt R.J., Chandler G.T., Greig T.W., Quattro J.M. Cathepsin B and glutathione peroxidase show differing transcriptional responses in the grass shrimp, Palaemonetes pugio following exposure to three xenobiotics. Environ. Sci. Technol. 2006, 40(11):3640-3645.
15. Halangk W., Lerch M.M., Brandt-Nedelev B., Roth W., Ruthenbuerger M., Reinheckel T., Domschke W., Lippert H., Peters C., Deussing J. Role of cathepsin B in intracellular trypsinogen activation and the onset of acute pancreatitis. J. Clin. Invest. 2000, 106:773-781.
16. Harrop S.A., Sawangjaroen N., Prociv P., Brindley P.J. Characterization and localization of cathepsin B proteinases expressed by adult Ancylostoma caninum hookworms. Mol. Biochem. Parasitol. 1995, 71:163-171.
17. Hillis D.M., Bull J.J. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst. Biol. 1993, 42:182-192.
18. Hu K.J., Leung P.C. Shrimp cathepsin L encoded by an intronless gene has predominant expression in hepatopancreas, and occurs in the nucleus of oocyte. Comp. Biochem. Physiol. B 2004, 137:21-33.
19. Hu K.J., Leung P.C. Food digestion by cathepsin L and digestion-related rapid cell differentiation in shrimp hepatopancreas. Comp. Biochem. Physiol. B 2007, 146:69-80.
20. Jones D.T., Taylor W.R., Thornton J.M. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 1992, 8:275-282.
21. Kollien A.H., Waniek P.J., Nisbet A.J., Billingsley P.F., Schaub G.A. Activity and sequence characterization of two cysteine proteases in the digestive tract of the reduviid bug Triatoma infestans. Insect Mol. Biol. 2004, 13:569-579.
22. Krupa J.C., Hasnain S., Nagler D.K., Macnard R., Mort J.S. S2' substrate specificity and the role of His110 and His111 in the exopeptidase activity of human cathepsin B. Biochem. J. 2002, 361:613-619.
23. Le Boulay C., van Wormhoudt A., Sellos D. Cloning and expression of cathepsin L-like proteinases in the hepatopancreas of the shrimp Penaeus vannamei during the intermolt cycle. J. Comp. Physiol. B 1996, 166:310-318.
24. Lerch M.M., Halangk W. Human pancreatitis and the role of cathepsin B. Gut 2006, 55(9):1228-1230.
25. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2_δδCT method. Methods 2001, 25:402-408.
26. McGrath M.E. The lysosomal cysteine proteases. Annu. Rev. Biophys. Biomol. Struct. 1999, 28:181-204.
27. Menard R., Carriere J., LaFlamme P., Plouffe C., Khouri H.E., Vernet T., Tessier D.C., Thomas D.Y., Storer A.C. Contribution of the glutamine 19 side chain to transition-state stabilization in the oxyanion hole of papain. Biochemistry 1991, 30:8924-8928.
28. Muhlia-Almazan A., Garcia-Carreño F.L. Influence of molting and starvation on the synthesis of proteolytic enzymes in the midgut gland of the white shrimp Penaeus vannamei. Comp. Biochem. Physiol. B 2002, 133(3):383-394.
29. Muhlia-Almazan A., Sanchez-Paz A., Garcia-Carreño F.L. Invertebrate trypsins: a review. J. Com. Physiol. B 2008, 178(6):655-672.
30. Musil D., Zucic D., Turk D., Engh R.A., Mayr I., Huber R., Popovic T., Turk V., Towatari T., Katunuma N., Bode W. The refined 2.15 Ǻ X-ray crystal structure of human liver cathepsin B: the structural basis for its specificity. EMBO J. 1991, 10(9):2321-2330.
31. Navarrete del Toro M.A., Garcia-Carreño F.L., Cordova-Murueta J.H. Comparison of digestive proteinases in three penaeids. Aquaculture 2011, 317:99-106.
32. Prabhakar S., Chen M.S., Elpidina E.N., Vinokurov K.S., Smith C.M., Marshall J., Oppert B. Sequence analysis and molecular characterization of larval midgut cDNA transcripts encoding peptidases from the yellow mealworm, Tenebrio molitor L. Insect Mol. Biol. 2007, 16:455-468.
33. Ranjit N., Zhan B., Stenzel D.J., Mulvenna J., Fujiwara R., Hotez P.J., Loukas A. A family of cathepsin B cysteine proteases expressed in the gut of the human hookworm, Necator americanus. Mol. Biochem. Parasitol. 2008, 160:90-99.
34. Rehman A., Jasmer D.P. Defined characteristics of cathepsin B-like proteins from nematodes: inferred functional diversity and phylogenetic relationships. Mol. Biochem. Parasitol. 1999, 102:297-310.
35. Ren Q., Zhang X.-W., Sun Y.-D., Sun S.-S., Zhou J., Zhao X.-F., Wang J.-X. Two cysteine proteinases respond to bacterial and WSSV challenge in Chinese white shrimp Fenneropenaeus chinensis. Fish Shellfish Immunol. 2010, 29(4):551-556.
36. Rojo L., Muhlia-Almazan A., Saborowski R., Garcia-Carreño F. Aspartic Cathepsin D endopeptidase contributes to extracellular digestion in clawed lobsters Homarus americanus and Homarus gammarus. Mar. Biotechnol. 2010, 12:696-707.
37. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406-425.
38. 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.H., Caffrey C.R. Functional expression and characterization of Schistosoma mansoni cathepsin B and its trans-activation by an endogenous asparaginyl endopeptidase. Mol. Biochem. Parasitol. 2003, 131:65-75.
39. Sambrook J., Russell D.W. Molecular Cloning: a Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, NY. 3rd ed.
40. Sanchez-Paz A., Garcia-Carreño F.L., Muhlia-Almazan A., Hernandez-Saavedra N., Yepiz-Plascencia G. Differential expression of trypsin mRNA in the white shrimp (Penaeus vannamei) midgut gland under starvation conditions. J. Exp. Mar. Biol. Ecol. 2003, 292:1-17.
41. Sloane B.F. Cathepsin B and cystatins: evidence for a role in cancer progression. Semin. Cancer Biol. 1990, 1(2):137-152.
42. Sojka D., Franta Z., Horn M., Hajdusek O., Caffrey C., Mares M., Kopacek P. Profiling of proteolytic enzymes in the gut of the tick Ixodes ricinus reveals an evolutionarily conserved network of aspartic and cysteine peptidases. Parasit. Vectors 2008, 1:7-21.
43. Tamura K., Dudley J., Nei M., Kumar S. MEGA 4.1: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
44. Teschke M., Saborowski R. Cysteine proteinases substitute for serine proteinases in the midgut glands of Crangon crangon and Crangon allmani (Decapoda: Caridea). J. Exp. Mar. Biol. Ecol. 2004, 316:213-229.
45. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22:4673-4680.
46. Uchida K., Ohmori D., Ueno T., Nishizuka M., Eshita Y., Fukunaga A., Kominami E. Preoviposition activation of cathepsin-like proteinases in degenerating ovarian follicles of the mosquito Culex pipiens pallens. Dev. Biol. 2001, 237(1):68-78.
47. Vernet T., Berti P.J., de Montigny C., Musil R., Tessier D.C., Menard R., Magny M.C., Storer A.C., Thomas D.Y. Processing of the papain precursor. J. Biol. Chem. 1995, 270(18):10838-10846.
48. Wang J., Xiang Y.-F., Lim C. The double catalytic triad, Cys25-His159-Asp158 and Cys25-His159-Asn175, in papain catalysis: role of Asp158 and Asn175. Protein Eng. 1994, 7:75-82.
49. Williamson A.L., Brindley P.J., Knox D.P., Hotez P.J., Loukas A. Digestive proteases of blood-feeding nematodes. Trends Parasitol. 2003, 19:417-423.
50. Wilson L.R., Good R.T., Panaccio M., Wijffels G.L., Sandeman R.M., Spithill T.W. Fasciola hepatica: characterization and cloning of the major cathepsin B protease secreted by newly excysted juvenile liver fluke. Exp. Parasitol. 1998, 88:85-94.
51. Yatsuda A.P., Bakker N., Krijgsveld J., Knox D.P., Heck A.J., de Vries E. Identification of secreted cystein proteases from the parasitic nematode Haemonchus contortus detected by biotinylated inhibitors. Infect. Immun. 2006, 74(3):1989-1993.
52. Zar J.H. Biostatistical Analysis 1984, Prentice-Hall, NJ. 4th ed.