Complementary Proteomic and Biochemical Analysis of Peptidases in Lobster Gastric Juice Uncovers the Functional Role of Individual Enzymes in Food Digestion

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• 作者：Betsaida Bibo-Verdugo ; Anthony J. O'Donoghue ; Liliana Rojo-Arreola…
• 关键词：Homarus americanus ; Peptidase ; Substrate specificity ; Cold ; adapted enzyme
• 刊名：Marine Biotechnology
• 出版年：2016
• 出版时间：April 2016
• 年：2016
• 卷：18
• 期：2
• 页码：201-214
• 全文大小：1,863 KB
• 参考文献：Agren MS, Taplin CJ, Woessner JF, Eaglstein WH, Mertz PM (1992) Collagenase in wound healing: effect of wound age and type. J Investig Dermatol 99:709–714CrossRef PubMed
  Anisimova VE, Shcheglov AS, Bogdanova EA, Rebrikov DV, Nekrasov AN, Barsova EV, Shagin DA, Lukyanov SA (2008) Is crab duplex-specific nuclease a member of the Serratia family of non-specific nucleases? Gene 418:41–48CrossRef PubMed
  Arunachalam B, Phan UT, Geuze HJ, Cresswell P (2000) Enzymatic reduction of disulfide bonds in lysosomes: characterization of a gamma-interferon-inducible lysosomal thiol reductase (GILT). Proc Natl Acad Sci U S A 97:745–750CrossRef PubMed PubMedCentral
  Bibo-Verdugo B, Rojo-Arreola L, Navarrete-Del-Toro MA, García-Carreño F (2015) A chymotrypsin from the digestive tract of California spiny lobster, Panulirus interruptus: purification and biochemical characterization. Mar Biotechnol 17:416–427
  Biggar KK, Dawson NJ, Storey KB (2012) Real-time protein unfolding: a method for determining the kinetics of native protein denaturation using a quantitative real-time thermocycler. Biotechniques 53:231–238CrossRef PubMed
  Brockerhoff H, Hoyle RJ, Hwang PC (1970) Digestive enzymes of the American lobster Homarus americanus. J Fish Res Board Can 27:1357–1370CrossRef
  Burridge LE, Haya K, Zitko V, Waddy S (1999) The lethality of Salmosan (Azamethiphos) to American lobster (Homarus americanus) larvae, postlarvae, and adults. Ecotoxicol Environ Saf 43:165–169CrossRef PubMed
  Chen Y (1991) Characterization of semi-purified collagenase fraction from lobster (Homarus americanus). Master of Science Thesis, McGill University
  Clark KF, Greenwood SJ, Acorn AR, Byrne PJ (2013) Molecular immune response of the American lobster (Homarus americanus) to the white spot syndrome virus. J Invertebr Pathol 114:298–308CrossRef PubMed
  Cobb JS, Phillips BF (1980) The biology and management of lobsters. Academic, New York
  Corvo I, O’Donoghue AJ, Pastro L, Pi-Denis N, Eroy-Reveles A, Roche L, McKerrow JH, Dalton JP, Craik CS (2013) Dissecting the active site of the collagenolytic cathepsin L3 protease of the invasive stage of Fasciola hepatica. PLoS Negl Trop Dis 7:e2269CrossRef PubMed PubMedCentral
  Delcroix M, Sajid M, Caffrey CR, Lim KC, Dvořák J, Hsieh I, Bahgat M, Dissous C, McKerrow JH (2006) A multienzyme network functions in intestinal protein digestion by a platyhelminth parasite. J Biol Chem 281:39316–39329CrossRef PubMed
  Feller G (1996) Enzymes from psychrophilic organisms. FEMS Microbiol Rev 18:189–202CrossRef
  Feller G (2003) Molecular adaptations to cold in psychrophilic enzymes. Cell Mol Life Sci 60:648–662CrossRef PubMed
  Feller G, Gerday C (2003) Psychrophilic enzymes: hot topics in cold adaptation. Nat Rev Microbiol 1:200–208CrossRef PubMed
  Gerday C, Aittaleb M, Bentahir M, Chessa JP, Claverie P, Collins T, D’Amico S, Dumont J, Garsoux G, Georlette D, Hoyoux A, Lonhienne T, Meuwis MA, Feller G (2000) Cold-adapted enzymes: from fundamentals to biotechnology. Trends Biotechnol 18:103–107CrossRef PubMed
  Gillmor SA, Craik CS, Fletterick RJ (1997) Structural determinants of specificity in the cysteine protease cruzain. Protein Sci 6:1603–1611CrossRef PubMed PubMedCentral
  Honig SC (2014) Intralesional collagenase in the treatment of Peyronie’s disease. Ther Adv Urol 6:47–53CrossRef PubMed PubMedCentral
  Hu KJ, Leung PC (2007) Food digestion by cathepsin L and digestion-related rapid cell differentiation in shrimp hepatopancreas. Comp Biochem Physiol B Biochem Mol Biol 146:69–80CrossRef PubMed
  Hurst LC, Badalamente MA, Hentz VR, Hotchkiss RN, Kaplan FT, Meals RA, Smith TM, Rodzvilla J (2009) Injectable collagenase Clostridium histolyticum for Dupuytren’s contracture. N Engl J Med 361:968–979CrossRef PubMed
  Knight CG (1995) Active-site tirtration of peptidases. Methods Enzymol 248:85–101CrossRef PubMed
  Komai T, Kawabata C, Amano M, Lee BR, Ichishima E (2004) Todarepsin, a new cathepsin D from hepatopancreas of Japanese common squid (Todarodes pacificus). Comp Biochem Physiol B Biochem Mol Biol 137:373–382CrossRef PubMed
  Kongsuwan K, Josh P, Zhu Y, Pearson R, Gough J, Colgrave ML (2010) Exploring the midgut proteome of partially fed female cattle tick (Rhipicephalus (Boophilus) microplus). J Insect Physiol 56:212–226CrossRef PubMed
  Laycock MV, Hirama T, Hasnain S, Watson D, Storer AC (1989) Purification and characterization of a digestive cysteine proteinase from the American lobster (Homarus americanus). Biochem J 263:439–444CrossRef PubMed PubMedCentral
  Laycock MV, MacKay RM, Di Fruscio M, Gallant JW (1991) Molecular cloning of three cDNAs that encode cysteine proteinases in the digestive gland of the American lobster (Homarus americanus). FEBS Lett 292:115–120CrossRef PubMed
  Le Chevalier P, Van Wormhoudt A (1998) Alpha-glucosidase from the hepatopancreas of the shrimp, Penaus vannamei (Crustacea-Decapoda). J Exp Zool 280:384–394CrossRef PubMed
  Lonhienne T, Gerday C, Feller G (2000) Psychrophilic enzymes: revisiting the thermodynamic parameters of activation may explain local flexibility. Biochim Biophys Acta Protein Struct Mol Enzymol 1543:1–10CrossRef
  Lynn KR (1990) Chitinases and chitobiases from the American lobster (Homarus americanus). Comp Biochem Physiol B 96:761–766
  McGrath ME, Eakin AE, Engel JC, Yang AS, Honig B, Fletterick RJ (1995) The crystal structure of cruzain: a therapeutic target for Chagas’ disease. J Mol Biol 247:251–259CrossRef PubMed
  Nilsen IW, Øverbø K, Havdalen LJ et al (2010) The enzyme and the cDNA sequence of a thermo labile and double-strand specific DNase from northern shrimps (Pandalus borealis). PLoS One 5:e10295CrossRef PubMed PubMedCentral
  O’Donoghue AJ, Eroy-Reveles AA, Knudsen GM, Ingram J, Zhou M, Statnekov JB, Greninger AL, Hostetter DR, Qu G, Maltby DA, Anderson MO, DeRisi JL, McKerrow JH, Burlingame AL, Craik CS (2012) Global identification of peptidase specificity by multiplex substrate profiling. Nat Methods 9:1095–1103CrossRef PubMed PubMedCentral
  O’Donoghue A, Jin Y, Knudsen G, Perera NC, Jenne DE, Murphy JE, Craik CS, Hermiston TW (2013) Global substrate profiling of proteases in human neutrophil extracellular traps reveals consensus motif predominantly contributed by elastase. PLoS One 8:e75141CrossRef PubMed PubMedCentral
  O’Donoghue AJ, Knudsen GM, Beekman C, Perry JA, Johnson AD, DeRisi JL, Craik CS, Bennett RJ (2015) Destructin-1 is a collagen-degrading endopeptidase secreted by Pseudogymnoascus destructans, the causative agent of white-nose syndrome. Proc Natl Acad Sci USA 112:7478–7483
  Page MJ, Craik CS (2013) In: Rawlings N, Salvesen G (eds) Handbook of proteolytic enzymes, 3rd edn. Elsevier, London, pp 3049–3052CrossRef
  Rivera-Perez C, Garcia-Carreño FL, Saborowski R (2011) Purification and biochemical characterization of digestive lipase in whiteleg shrimp. Mar Biotechnol 13:284–295CrossRef PubMed
  Rojo L, Muhlia-Almazan A, Saborowski R, García-Carreño F (2010a) Aspartic cathepsin D endopeptidase contributes to extracellular digestion in clawed lobsters Homarus americanus and Homarus gammarus. Mar Biotechnol 12:696–707CrossRef PubMed
  Rojo L, Sotelo-Mundo R, García-Carreño F, Gráf L (2010b) Isolation, biochemical characterization, and molecular modeling of American lobster digestive cathepsin D1. Comp Biochem Physiol B Biochem Mol Biol 157:394–400CrossRef PubMed
  Rojo L, García-Carreño F, de los Angeles Navarrete del Toro M (2013) Cold-adapted digestive aspartic protease of the clawed lobsters Homarus americanus and Homarus gammarus: biochemical characterization. Mar Biotechnol 15:87–96CrossRef PubMed
  Schulze WX, Sanggaard KW, Kreuzer I, Knudsen AD, Bemm F, Thogersen IB, Brautigam A, Thomsen LR, Schliesky S, Dyrlund TF, Escalante-Perez M, Becker D, Schultz J, Karring H, Weber A, Hojrup P, Hedrich R, Enghild JJ (2012) The protein composition of the digestive fluid from the Venus flytrap sheds light on prey digestion mechanisms. Mol Cell Proteomics 11:1306–1319CrossRef PubMed PubMedCentral
  Sojka D, Franta Z, Frantova H, Bartosová P, Horn M, Váchová J, O’Donoghue AJ, Eroy-Reveles AA, Craik CS, Knudsen GM, Caffrey CR, McKerrow JH, Mares M, Kopácek P (2012) Characterization of gut-associated cathepsin D hemoglobinase from tick Ixodes ricinus (IrCD1). J Biol Chem 287:21152–21163CrossRef PubMed PubMedCentral
  Stefansson B, Helgadóttir L, Olafsdottir S et al (2010) Characterization of cold-adapted Atlantic cod (Gadus morhua) trypsin I-kinetic parameters, autolysis and thermal stability. Comp Biochem Physiol B Biochem Mol Biol 155:186–194CrossRef PubMed
  Struvay C, Feller G (2012) Optimization to low temperature activity in psychrophilic enzymes. Int J Mol Sci 13:11643–11665CrossRef PubMed PubMedCentral
  Towle DW, Smith CM (2006) Gene discovery in Carcinus maenas and Homarus americanus via expressed sequence tags. Integr Comp Biol 46:912–918CrossRef PubMed
  Turk B, Turk D, Turk V (2000) Lysosomal cysteine proteases: more than scavengers. Biochim Biophys Acta Protein Struct Mol Enzymol 1477:98–111CrossRef
  Wojtowicz MB, Brockerhoff H (1972) Isolation and some properties of the digestive amylase of the American lobster (Homarus americanus). Comp Biochem Physiol 42:295–302
  Yasuda Y, Kageyama T, Akamine A, Shibata M, Kominami E, Uchiyama Y, Yamamoto K (1999) Characterization of new fluorogenic substrates for the rapid and sensitive assay of cathepsin E and cathepsin D. J Biochem 125:1137–1143CrossRef PubMed
  Zaidi N, Maurer A, Nieke S, Kalbacher H (2008) Cathepsin D: a cellular roadmap. Biochem Biophys Res Commun 376:5–9CrossRef PubMed
  Zhu X, Zhou Y, Feng J (2007) Analysis of both chitinase and chitosanase produced by Sphingomonas sp. CJ-5. J Zhejiang Univ Sci B 8(11):831–838
  
• 作者单位：Betsaida Bibo-Verdugo (1)
  Anthony J. O’Donoghue (2)
  Liliana Rojo-Arreola (1) (3)
  Charles S. Craik (2)
  Fernando García-Carreño (1)
  
  1. Centro de Investigaciones Biológicas del Noroeste (CIBNOR), Calle IPN 195, Col. Playa Palo de Santa Rita, La Paz, B.C.S., 23096, Mexico
  2. Department of Pharmaceutical Chemistry, University of California San Francisco, 600 16th Street, San Francisco, CA, 94158, USA
  3. Center for Discovery and Innovation in Parasitic Diseases, University of California San Francisco, 1700 4th Street, San Francisco, CA, 94158, USA
  
• 刊物类别：Earth and Environmental Science
• 刊物主题：Earth sciences
  Oceanography
  
• 出版者：Springer New York
• ISSN：1436-2236

文摘

Crustaceans are a diverse group, distributed in widely variable environmental conditions for which they show an equally extensive range of biochemical adaptations. Some digestive enzymes have been studied by purification/characterization approaches. However, global analysis is crucial to understand how digestive enzymes interplay. Here, we present the first proteomic analysis of the digestive fluid from a crustacean (Homarus americanus) and identify glycosidases and peptidases as the most abundant classes of hydrolytic enzymes. The digestion pathway of complex carbohydrates was predicted by comparing the lobster enzymes to similar enzymes from other crustaceans. A novel and unbiased substrate profiling approach was used to uncover the global proteolytic specificity of gastric juice and determine the contribution of cysteine and aspartic acid peptidases. These enzymes were separated by gel electrophoresis and their individual substrate specificities uncovered from the resulting gel bands. This new technique is called zymoMSP. Each cysteine peptidase cleaves a set of unique peptide bonds and the S2 pocket determines their substrate specificity. Finally, affinity chromatography was used to enrich for a digestive cathepsin D1 to compare its substrate specificity and cold-adapted enzymatic properties to mammalian enzymes. We conclude that the H. americanus digestive peptidases may have useful therapeutic applications, due to their cold-adaptation properties and ability to hydrolyze collagen.