Journal of Comparative Physiology B

, Volume 185, Issue 1, pp 17–35 | Cite as

Trypsin isozymes in the lobster Panulirus argus (Latreille, 1804): from molecules to physiology

  • Erick Perera
  • Leandro Rodríguez-Viera
  • Rolando Perdomo-Morales
  • Vivian Montero-Alejo
  • Francisco Javier Moyano
  • Gonzalo Martínez-Rodríguez
  • Juan Miguel Mancera


Trypsin enzymes have been studied in a wide variety of animal taxa due to their central role in protein digestion as well as in other important physiological and biotechnological processes. Crustacean trypsins exhibit a high number of isoforms. However, while differences in properties of isoenzymes are known to play important roles in regulating different physiological processes, there is little information on this aspect for decapod trypsins. The aim of this review is to integrate recent findings at the molecular level on trypsin enzymes of the spiny lobster Panulirus argus, into higher levels of organization (biochemical, organism) and to interpret those findings in relation to the feeding ecology of these crustaceans. Trypsin in lobster is a polymorphic enzyme, showing isoforms that differ in their biochemical features and catalytic efficiencies. Molecular studies suggest that polymorphism in lobster trypsins may be non-neutral. Trypsin isoenzymes are differentially regulated by dietary proteins, and it seems that some isoenzymes have undergone adaptive evolution coupled with a divergence in expression rate to increase fitness. This review highlights important but poorly studied issues in crustaceans in general, such as the relation among trypsin polymorphism, phenotypic (digestive) flexibility, digestion efficiency, and feeding ecology.


Digestion biochemistry Ecological physiology Panulirus argus Protein digestion Trypsin polymorphism Spiny lobster 



Most of the work outlined on this topic was supported by the International Foundation for Science (No. A/4306-1 and No. A/4306-2) granted to EP, the Agencia Española de Cooperación Internacional/Asociación Universitaria Iberoamericana de Postgrado (AUIP/AECI) from Spain, and the Program ʻDoctorado Iberoamericano en Ciencias’ at the University of Cadiz, Spain.


  1. Aguila J, Cuzon G, Pascual C, Domingues PM, Gaxiola G, Sánchez A, Maldonado T, Rosas C (2007) The effects of fish hydrolysate (CPSP) level on Octopus maya (Voss and Solis) diet: digestive enzyme activity, blood metabolites, and energy balance. Aquaculture 273:641–655Google Scholar
  2. Ahsan MM, Watabe S (2001) Kinetic and structural properties of two isoforms of trypsin isolated from the viscera of Japanese anchovy, Engraulis japonicus. J Protein Chem 20:49–58PubMedGoogle Scholar
  3. Anheller JE, Hellgren L, Karlstam B, Vincent J (1989) Biochemical and biological profile of a new enzyme preparation from Antarctic krill (E. superba) suitable for debridement of ulcerative lesions. Arch Dermatol Res 281:105–110PubMedGoogle Scholar
  4. Barclay MC, Irvin SJ, Williams KC, Smith DM (2006) Comparison of diets for the tropical spiny lobster Panulirus ornatus: astaxanthin-supplemented feeds and mussel flesh. Aquacult Nutr 12:117–125Google Scholar
  5. Barret A, Rawlings N, Woessner J (1998) Handbook of proteolytic enzymes, 2nd edn. Academic Press, San Diego, p 1666Google Scholar
  6. Bassompierre M, Ostenfeld TH, McLean E, Rungruangsak-Torrissen K (1998) In vitro protein digestion and growth of Atlantic salmon with different trypsin isozymes. Aquac Int 6:47–56Google Scholar
  7. Blakemore D, Williams S, Lehane MJ (1995) Protein stimulation of trypsin secretion from the opaque zone midgut cells of Stomoxys calcitrans. Comp Biochem Physiol 110B:301–307Google Scholar
  8. Borovsky D (2003) Biosynthesis and control of mosquito gut proteases. IUBMB Life 55:435–441PubMedGoogle Scholar
  9. Bougatef A (2013) Trypsins from fish processing waste: characteristics and biotechnological applications––comprehensive review. J Clean Prod 57:257–265Google Scholar
  10. Bragado MJ, Groblewski GE, Williams JA (1998) Regulation of protein synthesis by cholecystokinin in rat pancreatic acini involves PHAS-I and the p70 S6 kinase pathway. Gastroenterology 115:733–742PubMedGoogle Scholar
  11. Brandon MC, Pennington JE, Isoe J, Zamora J, Schillinger AS, Miesfeld RL (2008) TOR signaling is required for amino acid stimulation of early trypsin protein synthesis in the midgut of Aedes aegypti mosquitoes. Insect Biochem Mol Biol 38:916–922PubMedCentralPubMedGoogle Scholar
  12. Brivanlou AH, Darnell JE (2002) Signal transduction and the control of gene expression. Science 295:813–818PubMedGoogle Scholar
  13. Brockeroff H, Hoyle RJ, Hwang PC (1970) Digestive enzymes of the American lobster (Homarus americanus). J Fish Res Board Can 27:1357–1370Google Scholar
  14. Buddington RK, Krogdahl Å (2004) Hormonal regulation of the fish gastrointestinal tract. Comp Biochem Physiol 139A:261–271Google Scholar
  15. Cahu CL, Rønnestad I, Grangiera V, Zambonino-Infante JL (2004) Expression and activities of pancreatic enzymes in developing sea bass larvae (Dicentrarchus labrax) in relation to intact and hydrolyzed dietary protein; involvement of cholecystokinin. Aquaculture 238:295–308Google Scholar
  16. Carrillo O, Forrellat-Barrios A, Guerrero-Galván S, Vega-Villasante F (2007) A review of digestive enzyme activity in penaeid shrimps. Crustaceana 80:257–275Google Scholar
  17. Celis-Gerrero LE, García-Carreño FL, Navarrete del Toro MA (2004) Characterization of proteases in the digestive system of spiny lobster (Panulirus interruptus). Mar Biotechnol 6:262–269Google Scholar
  18. Chen H, Zhu YC, Whitworth RJ, Reese JC, Chen MS (2013) Serine and cysteine protease-like genes in the genome of a gall midge and their interactions with host plant genotypes. Insect Biochem Mol Biol 43:701–711PubMedGoogle Scholar
  19. Chow S, Suzuki S, Matsunaga T, Lavery S, Jeffs A, Takeyama H (2011) Investigation on natural diets of larval marine animals using peptide nucleic acid-directed polymerase chain reaction clamping. Mar Biotechnol 13:305–313PubMedGoogle Scholar
  20. Colinas-Sánchez F, Briones-Foorzan P (1990) Feeding of the spiny lobsters Panulirus guttatus and P. argus in the Mexican Caribbean. Inst Cienc Limnol Univ Nac Auton Mex 17:89–106Google Scholar
  21. Comeau SR, Gatchell DW, Vajda S, Camacho CJ (2004a) ClusPro: an automated docking and discrimination method for the prediction of protein complexes. Bioinformatics 20:45–50PubMedGoogle Scholar
  22. Comeau SR, Gatchell DW, Vajda S, Camacho CJ (2004b) ClusPro: a fully automated algorithm for protein–protein docking. Nucleic Acids Res 32:W96–W99PubMedCentralPubMedGoogle Scholar
  23. Córdova-Murueta JH, García-Carreño F (2002) Nutritive value of squid and hydrolyzed protein supplement in shrimp feed. Aquaculture 210:371–384Google Scholar
  24. Cox C, Hunt JH, Lyons WG, Davis GE (1997) Nocturnal foraging of the Caribbean spiny lobster, Panulirus argus on off shore reef of Florida, USA. Mar Freshw Res 48:671–679Google Scholar
  25. de Albuquerquee-Cavalcanti C, García-Carreño FL, Navarrete del Toro MA (2002) Trypsin and trypsin inhibitors from penaeid shrimp. J Food Biochem 26:233–251Google Scholar
  26. Díaz-Mendoza M, Ortego F, García de Lacoba M, Magaña C, de la Poza M, Farinós GP, Castañera P, Hernández-Crespo P (2005) Diversity of trypsins in the Mediterranean corn borer Sesamia nonagrioides (Lepidoptera: Noctuidae), revealed by nucleic acid sequences and enzyme purification. Insect Biochem Mol Biol 35:1005–1020PubMedGoogle Scholar
  27. Drummond DA, Bloom JD, Adami C, Wilke CO, Arnold FH (2005) Why highly expressed proteins evolve slowly. Proc Natl Acad Sci USA 102:14338–14343PubMedCentralPubMedGoogle Scholar
  28. Einarsson S, Davies PS, Talbot C (1997) Effect of exogenous cholecystokinin on the discharge of the gallbladder and the secretion of trypsin and chymotrypsin from the pancreas of the Atlantic salmon, Salmo salar L. Comp Biochem Physiol 117C:63–67Google Scholar
  29. Favrel P, Kegel G, Sedlmeier D, Keller R, van Wormhoudt A (1991) Structure and biological activity of crustacean gastrointestinal peptides identified with antibodies to gastrin/cholecystokinin. Biochimie 73:1233–1239PubMedGoogle Scholar
  30. Fernández I, Oliva M, Carrillo O, VanWormhoudt A (1997) Digestive enzyme activities of Penaeus notialis during reproduction and molting cycle. Comp Biochem Physiol 118A:1267–1271Google Scholar
  31. Fernández-Gimenez AV, García-Carreño FL, Navarrete del Toro MA, Fenucci JL (2001) Digestive proteinases of red shrimp Pleoticus muelleri (Decapoda, Penaeoidea): partial characterization and relationship with molting. Comp Biochem Physiol 130B:331–338Google Scholar
  32. Fernández-Gimenez AV, García-Carreño FL, Navarrete del Toro MA, Fenucci JL (2002) Digestive proteinases of Artemesia longinaris (Decapoda, Penaeidae) and relationship with molting. Comp Biochem Physiol 132B:593–598Google Scholar
  33. Figarella C, Negri GA, Guy O (1975) The two human trypsinogens. Inhibition spectra of the two human trypsins derived from their purified zymogens. Eur J Biochem 53:457–463PubMedGoogle Scholar
  34. Fodor K, Harmat V, Hetényi C, Kardos J, Antal J, Perczel A, Patthy A, Katona G, Gráf L (2005) Extended intermolecular interactions in a serine protease-canonical inhibitor complex account for strong and highly specific inhibition. J Mol Biol 350:156–169PubMedGoogle Scholar
  35. Galgani F, Nagayama F (1987) Digestive proteinases in the Japanese spiny lobster Panulirus japonicus. Comp Biochem Physiol 87B:889–893Google Scholar
  36. German DP, Nagle BC, Villeda JM, Ruiz AM, Thomson AW, Contreras-Balderas S, Evans DH (2010) Evolution of herbivory in a carnivorous clade of minnows (Teleostei: Cyprinidae): effects on gut size and digestive physiology. Physiol Biochem Zool 83:1–18PubMedGoogle Scholar
  37. Graf R, Lea AO, Briegel H (1998) A temporal profile of the endocrine control of trypsin synthesis in the yellow fever mosquito, Aedes aegypti. J Insect Physiol 44:451–454PubMedGoogle Scholar
  38. Green GM, Miyasaka K (1983) Rat pancreatic response to intestinal infusion of intact and hydrolyzed protein. Am J Physiol Gastrointest Liver Physiol 245:G394–G398Google Scholar
  39. Hara H, Hashimoto N, Akatsuka N, Kasai T (2000) Induction of pancreatic trypsin by dietary amino acids in rats: four trypsinogen isozymes and cholecystokinin messenger RNA. J Nutr Biochem 11:52–59PubMedGoogle Scholar
  40. Hedstrom L (1996) Trypsin: a case study in the structural determinants of enzyme specificity. Biol Chem 377:465–470PubMedGoogle Scholar
  41. Hehemann JH, Redecke L, Murugaiyan J, von Bergen M, Betzel C, Saborowski R (2008) Autoproteolytic stability of a trypsin from the marine crab Cancer pagurus. Biochem Bioph Res Commun 370:566–571Google Scholar
  42. Herrera A, Díaz-Iglesias E, Brito R, Gonzáles G, Gotera G, Espinosa J, Ibarzábal D (1991) Alimentación natural de la langosta Panulirus argus en la región de los Indios (Plataforma SW de Cuba) y su relación con el bentos. Rev Invest Mar 12:172–182Google Scholar
  43. Hickman RW, Illingworth J (1980) Condition cycle of the green-lipped mussel Perna canaliculus in New Zealand. Mar Biol 60:27–38Google Scholar
  44. Hira T, Hara H, Kasai T (1997) Stimulation of exocrine pancreatic secretion by soybean trypsin inhibitor does not depend on the masking of luminal trypsin activity in rats that have bile-pancreatic juice diverted into the ileum. Pancreas 15:285–290PubMedGoogle Scholar
  45. Hirota M, Ohmuraya M, Baba H (2006) The role of trypsin, trypsin inhibitor, and trypsin receptor in the onset and aggravation of pancreatitis. J Gastroenterol 41:832–836PubMedGoogle Scholar
  46. Holloway AK, Lawniczak MKN, Mezey JG, Begun DJ, Jones CD (2007) Adaptive gene expression divergence inferred from population genomics. PLoS Genet 3:2007–2013PubMedGoogle Scholar
  47. Huber R, Kukla D, Bode W, Schwager P, Bartels K, Deisenhofer J, Steigemann W (1974) Structure of the complex formed by bovine trypsin and bovine pancreatic trypsin inhibitor II. Crystallographic refinement at 1.9 Å resolution. J Mol Biol 89:73–101PubMedGoogle Scholar
  48. Hughes BL, Suniga RG, Yardley DG (1994) Influence of amylase genotypes on growth rate and feed conversion of chickens. Poultry Sci 73:953–957Google Scholar
  49. Hurst LD (2002) The Ka/Ks ratio: diagnosing the form of sequence evolution. Trends Genet 18:486–487PubMedGoogle Scholar
  50. Huvet A, Daniel JY, Quéré C, Dubois S, Prudence M, Van Wormhoudt A, Sellos D, Samain JF, Moal J (2003) Tissue expression of two α-amylase genes in the Pacific oyster Crassostrea gigas. Effects of two different food rations. Aquaculture 228:321–333Google Scholar
  51. Huvet A, Jeffroy F, Fabioux C, Daniel JY, Quillien V, Van Wormhoudt A, Moal J, Samain JF, Boudry P, Pouvreau S (2008) Association among growth, food consumption-related traits and amylase gene polymorphism in the Pacific oyster Crassostrea gigas. Anim Genet 39:662–665PubMedGoogle Scholar
  52. Inomata N, Nakashima S (2008) Short 5′-flanking regions of the Amy gene of Drosophila kikkawai affect amylase gene expression and respond to food environments. Gene 412:102–109PubMedGoogle Scholar
  53. Johnson SC, Ewart KV, Osborne JA, Delage D, Ross NW, Murray HM (2002) Molecular cloning of trypsin cDNAs and trypsin gene expression in the salmon louse Lepeophtheirus salmonis (Copepoda: Caligidae). Parasitol Res 88:789–796PubMedGoogle Scholar
  54. Johnston DJ (2003) Ontogenetic changes in digestive enzyme activity of the spiny lobster, Jasus edwardsii (Decapoda; Palinuridae). Mar Biol 143:1071–1082Google Scholar
  55. Johnston D, Freeman J (2005) Dietary preference and digestive enzyme activities as indicators of trophic resource utilization by six species of crab. Biol Bull 208:36–46PubMedGoogle Scholar
  56. Johnston D, Hermans JM, Yellowlees D (1995) Isolation and characterization of a trypsin from the slipper lobster, Thenus orientalis (Lund). Arch Biochem Biophys 324:35–40PubMedGoogle Scholar
  57. Johnston D, Ritar A, Thomas C, Jeffs A (2004) Digestive enzyme profiles of spiny lobster Jasus edwardsii phyllosoma larvae. Mar Ecol Prog Ser 275:219–230Google Scholar
  58. Jones DA, Kumlu M, Le Vay L, Fletcher DJ (1997) The digestive physiology of herbivorous, omnivorous and carnivorous crustacean larvae: a review. Aquaculture 155:285–295Google Scholar
  59. Jongsma MA, Bolter C (1997) The adaptation of insects to plant protease inhibitors. J Insect Physiol 43:885–895PubMedGoogle Scholar
  60. Jönsson E, Forsman A, Einarsdottir IE, Egnér E, Ruohonen K, Björnsson BT (2006) Circulating levels of cholecystokinin and gastrin-releasing peptide in rainbow trout fed different diets. Gen Comp Endocr 148:187–194PubMedGoogle Scholar
  61. Karasov WH, Martínez del Rio C, Caviedes-Vidal E (2011) Ecological physiology of diet and digestive systems. Annu Rev Physiol 73:69–93PubMedGoogle Scholar
  62. Kim HR, Meyers SP, Godber JS (1992) Purification and characterization of anionic trypsins from the hepatopancreas of crayfish Procambarus clarkii. Comp Biochem Physiol 103B:391–398Google Scholar
  63. Kirpichnikov VS, Muske GA (1980) The adaptative value of biochemical polymorphism in animal and plant populations. Genetica 52(53):183–193Google Scholar
  64. Kittaka J (1997) Culture of larval spiny lobsters: a review of work done in northern Japan. Mar Freshw Res 48:923–930Google Scholar
  65. Klein B, Le Moullac G, Sellos D, Van Wormhoudt A (1996) Molecular cloning and sequencing of trypsin cDNA from Penaeus vannamei (Crustacea, Decapoda): use in assessing gene expression during the moult cycle. Int J Biochem Cell Biol 28:551–563PubMedGoogle Scholar
  66. Klein B, Sellos D, Van Wormhoudt A (1998) Genomic organization and polymorphism of a Crustacean trypsin multi-gene family. Gene 216:123–129PubMedGoogle Scholar
  67. Kofuji PYM, Murashita K, Hosokawa H, Masumoto T (2007) Effects of exogenous cholecystokinin and gastrin on the secretion of trypsin and chymotrypsin from yellowtail (Seriola quinqueradiata) isolated pyloric caeca. Comp Biochem Physiol 146A:124–130Google Scholar
  68. Konturek SJ, Zabielski R, Konturek JW, Czarnecki J (2003) Neuroendocrinology of the pancreas: role of brain–gut axis in pancreatic secretion. Eur J Pharmacol 481:1–14PubMedGoogle Scholar
  69. Kossiakoff AA, Chambers JL, Kay LM, Stroud RM (1977) Structure of bovine trypsinogen at 1.9 Å resolutions. Biochemistry 16:654–664PubMedGoogle Scholar
  70. Koven W, Rojas-García CR, Finn RN, Tandler A, Rønnestad I (2002) Stimulatory effect of ingested protein and/or free amino acids on the secretion of the gastro-endocrine hormone cholecystokinin and on tryptic activity, in early-feeding herring larvae, Clupea harengus. Mar Biol 140:1241–1247Google Scholar
  71. Kozakov D, Brenke R, Comeau SR, Vajda S (2006) PIPER: an FFT-based protein docking program with pairwise potentials. Proteins 65:392–406PubMedGoogle Scholar
  72. Kozakov D, Beglov D, Bohnuud T, Mottarella S, Xia B, Hall DR, Vajda S (2013) How good is automated protein docking? Proteins 81:2159–2216PubMedCentralPubMedGoogle Scholar
  73. Kvamme BO, Kongshaug H, Organisation FN (2005) Organization of trypsin genes in the salmon louse (Lepeophtheirus salmonis, Crustacea, copepoda) genome. Gene 352:63–74PubMedGoogle Scholar
  74. Lalana R, Ortiz M (1991) Contenido estomacal de puérulos y post-puérulos de la langosta Panulirus argus en el Archipiélago de los Canarreos, Cuba. Rev Invest Mar 12:107–116Google Scholar
  75. Larracuente AM, Sackton TB, Greenberg AJ, Wong A, Singh ND, Sturgill D, Zhang Y, Oliver B, Clark AG (2008) Evolution of protein-coding genes in Drosophila. Trends Genet 24:114–123PubMedGoogle Scholar
  76. Le Moullac G, Klein B, Sellos D, Van Wormhoudt A (1996) Adaptation of trypsin, chymotrypsin and amylase to casein level and protein source in Penaeus vannamei (Crustacea, Decapoda). J Exp Mar Biol Ecol 208:107–125Google Scholar
  77. Le Vay L, Jones DA, Puello-Cruz AC, Sangha RS, Ngamphongsai C (2001) Digestion in relation to feeding strategies exhibited by crustacean larvae. Comp Biochem Physiol 128A:623–630Google Scholar
  78. Lehane MJ, Blakemore D, Williams S, Moffatt MR (1995) Regulation of digestive enzyme levels in insects. Comp Biochem Physiol 110B:285–289Google Scholar
  79. Liao D (1999) Concerted evolution: molecular mechanism and biological implications. Am J Hum Genet 64:24–30PubMedCentralPubMedGoogle Scholar
  80. Lipcius RN, Herrnkind WF (1982) Molt cycle alterations in behavior, feeding and diel rhythms of a decapod crustacean, the spiny lobster Panulirus argus. Mar Biol 68:241–252Google Scholar
  81. Lopes AR, Juliano MA, Juliano L, Terra WR (2004) Coevolution of insect trypsins and inhibitors. Arch Insect Biochem 55:140–152Google Scholar
  82. Ma M, Wang J, Chen R, Li L (2009) Expanding the crustacean neuropeptidome using a multifaceted mass spectrometric approach. J Proteome Res 8:2426–2437PubMedCentralPubMedGoogle Scholar
  83. Marana SR, Lopes AR, Juliano L, Juliano MA, Fer-reira C, Terra WR (2002) Subsites of trypsin active site favor catalysis or substrate binding. Biochem Biophys Res Commun 290:494–497PubMedGoogle Scholar
  84. Marx JM, Herrnkind WF (1985) Macroalgae (Rhodophyta: Laurecia spp.) as habitat for young juvenile spiny lobsters Panulirus argus B. Mar Sci 36:423–431Google Scholar
  85. Mazumdar-Leighton S, Broadway RM (2001) Transcriptional induction of diverse midgut trypsins in larval Agrotis ipsilon and Helicoverpa zea feeding on the soybean trypsin Inhibitor. Insect Biochem Mol Biol 31:645–657PubMedGoogle Scholar
  86. Meyer JH, Kelly GA (1976) Canine pancreatic responses to intestinally perfused proteins and protein digests. Am J Physiol 231:682–691PubMedGoogle Scholar
  87. Moffatt M, Blakemore D, Lehane MJ (1995) Studies on the synthesis and secretion of trypsin in the midgut of Stomoxys calcitrans. Comp Bioehem Physiol 110B:291–300Google Scholar
  88. Molnár T, Vörös J, Szeder B, Takáts K, Kardos J, Katona G, Gráf L (2013) Comparison of complexes formed by a crustacean and a vertebrate trypsin with bovine pancreatic trypsin inhibitor––the key to achieving extreme stability? FEBS J 280:5750–5763PubMedGoogle Scholar
  89. Muhlia-Almazán A, García-Carreño FL, Sánchez-Paz JA, Yepiz-Plascencia G, Peregrino-Uriarte AB (2003) Effects of dietary protein on the activity and mRNA level of trypsin in the midgut gland of the white shrimp Penaeus vannamei. Comp Biochem Physiol 135B:373–383Google Scholar
  90. Muhlia-Almazán A, Sánchez-Paz A, García-Carreño FL (2008) Invertebrate trypsins: a review. J Comp Physiol 178B:655–672Google Scholar
  91. Nègre N, Brown CD, Ma L, Bristow CA, Miller SW, Wagner U, Kheradpour P, Eaton ML, Loriaux P, Sealfon R, Li Z, Ishii H, Spokony RF, Chen J, Hwang L, Cheng C, Auburn RP, Davis MB, Domanus M, Shah PK, Morrison CA, Zieba J, Suchy S, Senderowicz L, Victorsen A, Bild NA, Grundstad AJ, Hanley D, MacAlpine DM, Mannervik M, Venken K, Bellen H, White R, Gerstein M, Russell S, Grossman RL, Ren B, Posakony JW, Kellis M, White KP (2011) A cis-regulatory map of the Drosophila genome. Nature 471:527–531PubMedCentralPubMedGoogle Scholar
  92. Nelson K, Hedgecock D (1980) Enzyme polymorphism and adaptive strategy in the decapod crustacea. Am Nat 116:238–280Google Scholar
  93. Noriega FG, Wells MA (1999) A molecular view of trypsin synthesis in the midgut of Aedes aegypti. J Insect Physiol 45:613–620PubMedGoogle Scholar
  94. Noriega FG, Colonna AE, Wells MA (1999) Increase in the size of the amino acid pool is sufficient to activate translation of early trypsin mRNA in Aedes aegypti midgut. Insect Biochem Mol Biol 29:243–247PubMedGoogle Scholar
  95. Northrup JH, Kunitz M (1931) Isolation of protein crystals possessing tryptic activity. Science 73:262–263Google Scholar
  96. Northrup JH, Kunitz M, Herriott RM (1948) Crystalline enzymes, 2nd edn. Columbia University Press, New YorkGoogle Scholar
  97. Nyberg P, Ylipalosaari M, Sorsa T, Salo T (2006) Trypsins and their role in carcinoma growth. Exp Cell Res 312:1219–1228PubMedGoogle Scholar
  98. Ohlsson K, Tegner H (1973) Anionic and cationic dog trypsin: isolation and partial characterization. Biochim Biophys Acta 317:328–337PubMedGoogle Scholar
  99. Owyang C (1994) Negative feedback control of exocrine pancreatic secretion: role of cholecystokinin and cholinergic pathway. J Nutr 124:1321S–1326SPubMedGoogle Scholar
  100. Page MJ, Di Cera E (2008) Serine peptidases: classification, structure and function. Cell Mol Life Sci 65:1220–1236PubMedGoogle Scholar
  101. Patthy L (1999) Genome evolution and the evolution of exon shuffling: a review. Gene 238:103–114PubMedGoogle Scholar
  102. Pavasovic A, Anderson AJ, Mather PB, Richardson NA (2007) Effect of a variety of animal, plant and single cell-based feed ingredients on diet digestibility and digestive enzyme activity in redclaw crayfish, Cherax quadricarinatus (Von Martens 1868). Aquaculture 272:564–572Google Scholar
  103. Perera E, Fraga I, Carrillo O, Díaz-Iglesias E, Cruz R, Báez M, Galich G (2005) Evaluation of practical diets for the Caribbean spiny lobster Panulirus argus (Latreille, 1804): effects of protein sources on substrate metabolism and digestive proteases. Aquaculture 244:251–262Google Scholar
  104. Perera E, Moyano FJ, Díaz M, Perdomo-Morales R, Montero-Alejo V, Alonso-Jiménez E, Carrillo O, Galich G (2008a) Polymorphism and partial characterization of digestive enzymes in the spiny lobster Panulirus argus. Comp Biochem Physiol 150B:247–254Google Scholar
  105. Perera E, Moyano FJ, Díaz M, Perdomo-Morales R, Montero V, Rodríguez-Viera L, Alonso E, Carrillo O, Galich G (2008b) Changes in digestive enzymes through developmental and molt stages in the spiny lobster, Panulirus argus. Comp Biochem Physiol 151B:250–256Google Scholar
  106. Perera E, Moyano FJ, Rodríguez-Viera L, Cervantes A, Martínez-Rodríguez G, Mancera JM (2010a) In vitro digestion of protein sources by crude enzyme extracts of the spiny lobster Panulirus argus (Latreille, 1804) hepatopancreas with different trypsin isoenzyme patterns. Aquaculture 310:178–185Google Scholar
  107. Perera E, Pons T, Hernández D, Moyano FJ, Martínez-Rodríguez G, Mancera JM (2010b) New members of the brachyurins family in lobster include a trypsin-like enzyme with amino acid substitutions in the substrate-binding pocket. FEBS J 277:3489–3501PubMedGoogle Scholar
  108. Perera E, Rodríguez-Casariego J, Rodríguez-Viera L, Calero J, Perdomo-Morales R, Mancera JM (2012a) Lobster (Panulirus argus) hepatopancreatic trypsin isoforms and their digestion efficiency. Biol Bull 222:158–170PubMedGoogle Scholar
  109. Perera E, Rodríguez-Viera L, Rodríguez-Casariego J, Fraga I, Carrillo O, Martínez-Rodríguez G, Mancera JM (2012b) Dietary protein quality differentially regulates trypsin enzymes at the secretion and transcription levels in the lobster (Panulirus argus) by distinct signaling pathways. J Exp Biol 215:853–862PubMedGoogle Scholar
  110. Perona JJ, Craik CS (1995) Structural basis of substrate specificity in the serine proteases. Protein Sci 4:337–360PubMedCentralPubMedGoogle Scholar
  111. Perona JP, Craik CS (1997) Evolutionary divergence of substrate specificity within the chymotrypsin-like serine protease fold. J Biol Chem 272:29987–29990PubMedGoogle Scholar
  112. Perona JJ, Tsu CA, Craik CS, Fletterick RJ (1997) Crystal structure of an ecotincollagenase complex suggests a model for recognition and cleavage of the collagen triple helix. Biochemistry 36:5381–5392PubMedGoogle Scholar
  113. Perry GH, Dominy NJ, Claw KG, Lee AS, Fiegler H, Redon R, Werner J, Villanea FA, Mountain JL, Misra R, Carter NP, Lee C, Stone AC (2007) Diet and the evolution of human amylase gene copy number variation. Nat Genet 39:1256–1260PubMedCentralPubMedGoogle Scholar
  114. Phillips B, Matsuda H (2011) A global review of spiny lobster aquaculture. In: Fotedar RK, Phillips BF (eds) Recent advances and new species in aquaculture. Blackwell Publishing Ltd, Oxford, pp 22–84Google Scholar
  115. Prudence M, Moal J, Boudry P, Daniel JY, Quéré C, Jeffroy F, Mingant C, Ropert M, Bédier E, Van Wormhoudt A, Samain JF, Huvet A (2006) An amylase gene polymorphism is associated with growth differences in the Pacific cupped oyster Crassostrea gigas. Anim Genet 37:348–351PubMedGoogle Scholar
  116. Psochiou E, Sarropoulou E, Mamuris Z, Moutou KA (2007) Sequence analysis and tissue expression pattern of Sparus aurata chymotrypsinogens and trypsinogen. Comp Biochem Physiol 147B:367–377Google Scholar
  117. Puigserver A, Desnuelle P (1971) Identification of an anionic trypsinogen in bovine pancreas. Biochim Biophys Acta 236:499–502PubMedGoogle Scholar
  118. Rascón AA, Gearin J, Isoe J, Miesfeld RL (2011) In vitro activation and enzyme kinetic analysis of recombinant midgut serine proteases from the dengue vector mosquito Aedes aegypti. BMC Biochem 12:43PubMedCentralPubMedGoogle Scholar
  119. Ravallec-Plé R, van Wormhoudt A (2003) Secretagogue activities in cod (Gadus morhua) and shrimp (Penaeus aztecus) extracts and alcalase hydrolysates determined in AR4-2J pancreatic tumour cells. Comp Biochem Physiol 134B:669–679Google Scholar
  120. Resch-Sedlmeier G, Sedlmeier D (1999) Release of digestive enzymes from the crustacean hepatopancreas: effect of vertebrate gastrointestinal hormones. Comp Biochem Physiol 123B:187–192Google Scholar
  121. Rungruangsak-Torrissen K (2012) Trypsin and its implementation for growth, maturation, and dietary quality assessment. In: Weaver K, Kelley C (eds) Trypsin: structure, biosynthesis and functions. Nova Science Publishers, Inc., New York, pp 1–59Google Scholar
  122. Rungruangsak-Torrissen K, Male R (2000) Trypsin isozymes: development, digestion and structure. In: Haard NF, Simpson BK (eds) Seafood Enzymes, utilization and influence on post-harvest seafood quality. Marcel Dekker Inc, New York, pp 215–269Google Scholar
  123. Rungruangsak-Torrissen K, Pringle GM, Moss R, Houlihan DF (1998) Effects of varying rearing temperatures on expression of different trypsin isoenzymes, feed conversion efficiency and growth in Atlantic salmon (Salmo salar L.). Fish Physiol Biochem 19:247–255Google Scholar
  124. Rungruangsak-Torrissen K, Carter CG, Sundby A, Berg A, Houlihan DF (1999) Maintenance ration, protein synthesis capacity, plasma insulin and growth of Atlantic salmon (Salmo salar L.) with genetically different trypsin isoenzymes. Fish Physiol Biochem 21:223–233Google Scholar
  125. Rypniewski WR, Perrakis A, Vorgias CE, Wilson KS (1994) Evolutionary divergence and conservation of trypsin. Protein Eng 7:57–64PubMedGoogle Scholar
  126. Saborowski R, Schatte J, Gimenez L (2012) Catalytic properties and polymorphism of serine endopeptidases from the midgut gland of the brown shrimp Crangon crangon (Decapoda, Caridea). Mar Biol 159:1107–1118Google Scholar
  127. Sainz JC, Córdova-Murueta JH (2009) Activity of trypsin from Litopenaeus vannamei. Aquaculture 290:190–195Google Scholar
  128. Sainz JC, García-Carreño FL, Hernández-Cortés P (2004a) Penaeus vannamei isotrypsins: purification and characterization. Comp Biochem Physiol 138B:155–162Google Scholar
  129. Sainz JC, García-Carreño FL, Sierra-Beltrán A, Hernández-Cortés P (2004b) Trypsin synthesis and storage as zymogen in the midgut gland of the shrimp Litopenaeus vannamei. J Crustac Biol 24:266–273Google Scholar
  130. Sainz JC, García-Carreño FL, Córdova-Murueta JH, Cruz-Hernández P (2005) Penaeus vannamei (Boone, 1931) isotrypsins, genotype and modulation. J Exp Mar Biol Ecol 326:105–113Google Scholar
  131. Sans MD, Williams JA (2002) Translational control of protein synthesis in pancreatic acinar cells. Int J Gastrointest Cancer 31:107–115PubMedGoogle Scholar
  132. Sans MD, Tashiro M, Vogel NL, Kimball SR, D’Alecy LG, Williams JA (2006) Leucine activates pancreatic translational machinery in rats and mice through mTOR independently of CCK and insulin. J Nutr 136:1792–1799PubMedGoogle Scholar
  133. Saunders MI, Thompson PA, Jeffs AG, Säwström C, Sachlikidis N, Beckley LE, Waite AM (2012) Fussy feeders: phyllosoma larvae of the Western rock lobster (Panulirus cygnus) demonstrate prey preference. PLoS One 7:1–9Google Scholar
  134. Savoie A, Le François NR, Lamarre SG, Blier PU, Beaulieu L, Cahu C (2011) Dietary protein hydrolysate and trypsin inhibitor effects on digestive capacities and performances during early-stages of spotted wolffish: suggested mechanisms. Comp Biochem Physiol 158A:525–530Google Scholar
  135. Schwarzenberger A, Zitt A, Kroth P, Mueller S, Von Elert E (2010) Gene expression and activity of digestive proteases in Daphnia: effects of cyanobacterial protease inhibitors. BMC Physiol 10:6PubMedCentralPubMedGoogle Scholar
  136. Shahidi F, Kamil YVAJ (2001) Enzymes from fish and aquatic invertebrates and their application in the food industry. Trends Food Sci Tech 12:435–464Google Scholar
  137. Simon CJ (2009) Digestive enzyme response to natural and formulated diets in cultured juvenile spiny lobster, Jasus edwardsii. Aquaculture 294:271–281Google Scholar
  138. Simon CJ, Jeffs A (2008) Feeding and gut evacuation of cultured juvenile spiny lobsters, Jasus edwardsii. Aquaculture 280:211–219Google Scholar
  139. Simon CJ, Jeffs A (2011) The effect of dietary carbohydrates on the growth response, digestive gland glycogen and digestive enzyme activities of early spiny lobster juveniles, Jasus edwardsii. Aquacult Nutr 17:613–626Google Scholar
  140. Singer MV (1987) Pancreatic secretory response to intestinal stimulants: a review. Scand J Gastroenterol Suppl 139:1–13PubMedGoogle Scholar
  141. Smith DM, Williams KC, Irvin SJ (2005) Response of the tropical spiny lobster Panulirus ornatus to protein content of pelleted feed and to a diet of mussel flesh. Aquacult Nutr 11:209–217Google Scholar
  142. Soares TS, Watanabe RMO, Lemos FJA, Tanaka AS (2011) Molecular characterization of genes encoding trypsin-like enzymes from Aedes aegypti larvae and identification of digestive enzymes. Gene 489:70–75PubMedGoogle Scholar
  143. Spit J, Zels S, Dillen S, Holtof M, Wynant N, Broeck JV (2014) Effects of different dietary conditions on the expression of trypsin- and chymotrypsin-like protease genes in the digestive system of the migratory locust, Locusta migratoria. Insect Biochem Mol Biol 48:100–109PubMedGoogle Scholar
  144. Srinivasan A, Giri AP, Gupta VS (2006) Structural and functional diversities in lepidopteran serine proteases. Cell Mol Biol Lett 11:132–154PubMedGoogle Scholar
  145. Staljanssens D, Azari EK, Christiaens O, Beaufays J, Lins L, Camp JV, Smagghe G (2011) The CCK(-like) receptor in the animal kingdom: functions, evolution and structures. Peptides 32:607–619PubMedGoogle Scholar
  146. Stryer L (1988) Biochemistry, 3rd edition. WH Freeman, New York, p 1136Google Scholar
  147. Sweet RM, Wright HT, Janin J, Chothia CH, Blow DM (1974) Crystal structure of the complex of porcine trypsin with soybean trypsin inhibitor (Kunitz) at 2.6-Å resolution. Biochemistry 13:4212–4228PubMedGoogle Scholar
  148. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedGoogle Scholar
  149. Taylor JS, Raes J (2004) Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet 38:615–643PubMedGoogle Scholar
  150. Teschke M, Saborowski R (2005) Cysteine proteinases substitute for serine proteinases in the midgut glands of Crangon crangon and Crangon allmani (Decapoda: Caridea). J Exp Mar Biol Ecol 316:213–229Google Scholar
  151. Thimister PWL, Hopman WPM, Sloots CEJ, Rosenbusch G, Willems HL, Trijbels FJM, Jansen JBMJ (1996) Role of intraduodenal proteases in plasma cholecystokinin and pancreaticobiliary responses to protein and amino acids. Gastroenterology 110:567–575PubMedGoogle Scholar
  152. Tillner R, Rønnestad I, Harboe T, Ueberschär B (2013) Hormonal control of tryptic enzyme activity in Atlantic cod larvae (Gadus morhua): involvement of cholecystokinin during ontogeny and diurnal rhythm. Aquaculture 402–403:133–140Google Scholar
  153. Torrissen KR (1987) Genetic variation of trypsin-like isozymes correlated to fish size of Atlantic salmon (Salmo salar). Aquaculture 62:1–10Google Scholar
  154. Torrissen KR (1991) Genetic variation in growth rate of Atlantic salmon with different trypsin-like isozyme patterns. Aquaculture 93:299–312Google Scholar
  155. Torrissen KR, Shearer KD (1992) Protein digestion, growth and food conversion in Atlantic salmon and Arctic charr with different trypsin-like isozyme patterns. J Fish Biol 41:409–415Google Scholar
  156. Torrissen KR, Male R, Naevdal G (1993) Trypsin isozymes in Atlantic salmon, Salmo salar L.: studies of heredity, egg quality and effect on growth of three deferent populations. Aquac Fish Manag 24:407–415Google Scholar
  157. Torrissen KR, Lied E, Espe M (1994) Differences in digestion and absorption of dietary protein in Atlantic salmon (Salmo salar) with genetically different trypsin isoenzymes. J Fish Biol 45:1087–1104Google Scholar
  158. Toyota E, Iyaguchi D, Sekizaki H, Itoh K, Tanizawa K (2007) Kinetic properties of three isoforms of trypsin isolated from the pyloric caeca of chum salmon (Oncorhynchus keta). Biol Pharm Bull 30:1648–1652PubMedGoogle Scholar
  159. Tsu CA, Craik CS (1998) Brachyurins. In: Barrett AJ, Rawlings ND, Woessner JF (eds) Handbook of proteolytic enzymes. Academic Press, San Diego, pp 25–30Google Scholar
  160. Tsu CA, Perona JJ, Fletterick RJ, Craik CS (1997) Structural basis for the broad substrate specificity of fiddler crab collagenolytic serine protease. Biochemistry 36:5393–5401PubMedGoogle Scholar
  161. Unajak S, Meesawat P, Paemanee A, Areechon N, Engkagul A, Kovitvadhi U, Kovitvadhi S, Rungruangsak-Torrissen K, Choowongkomon K (2012) Characterisation of thermostable trypsin and determination of trypsin isozymes from intestine of Nile tilapia (Oreochromis niloticus L.). Food Chem 134:1533–1541Google Scholar
  162. van Acker GJD, Perides G, Steer ML (2006) Co-localization hypothesis: a mechanism for the intrapancreatic activation of digestive enzymes during the early phases of acute pancreatitis. World J Gastroenterol 12:1985–1990PubMedCentralPubMedGoogle Scholar
  163. van Hoef V, Breugelmans B, Spit J, Simonet G, Zels S, Billen J, Broeck JV (2011) Functional analysis of a pancreatic secretory trypsin inhibitor-like protein in insects: silencing effects resemble the human pancreatic autodigestión phenotype. Insect Biochem Mol Biol 41:688–695PubMedGoogle Scholar
  164. van Wormhoudt A (1974) Variations of the level of the digestive enzymes during the intermolt cycle of Palaemon serratus: influence of the season and effect of the eyestalk ablation. Comp Biochem Physiol 49A:707–715Google Scholar
  165. van Wormhoudt A, Favrel P, Guillaume J (1989) Gastrin/cholecystokinin-like post-prandial variations: quantitative and qualitative changes in the haemolymph of penaeids (Crustacea; Decapoda). J Comp Physiol 159:213–269Google Scholar
  166. Vogt G, Stfcker W, Storeh V, Zwilling R (1989) Biosynthesis of Astacus protease, a digestive enzyme from crayfish. Histochemistry 91:373–381PubMedGoogle Scholar
  167. Voytek P, Gjessing EC (1971) Studies of an anionic trypsinogen and its active enzyme from porcine pancreas. J Biol Chem 246:508–516PubMedGoogle Scholar
  168. Walsh KA, Wilcox PE (1970) Serine proteinases. Method Enzymol 19:31–41Google Scholar
  169. Walsh KA, Kauffman DL, Sampath-Kumar KSV, Neurath H (1964) On the structure and function of bovine trypsinogen and trypsin. Proc Natl Acad Sci USA 51:301–308PubMedCentralPubMedGoogle Scholar
  170. Wang S, Magoulas C, Hickey D (1999) Concerted evolution within a trypsin gene cluster in Drosophila. Mol Biol Evol 16:1117–1124PubMedGoogle Scholar
  171. Williams KC (2007) Nutritional requirements and feeds development for post-larval spiny lobster: a review. Aquaculture 263:1–14Google Scholar
  172. Woodring J, Diersch S, Lwalaba D, Hoffmann KH, Meyering-Vos M (2009) Control of the release of digestive enzymes in the caeca of the cricket Gryllus bimaculatus. Physiol Entomol 34:144–151Google Scholar
  173. Wray GA, Hahn MW, Abouheif E, Balhoff JP, Pizer M (2003) The evolution of transcriptional regulation in eukaryotes. Mol Biol Evol 20:1377–1419PubMedGoogle Scholar
  174. Wu Z, Jiang G, Xiang P, Xu H (2008) Anionic trypsin from North Pacific krill (Euphausia pacifica): purification and characterization. Int J Pept Res Ther 14:113–120Google Scholar
  175. Wu DD, Wang GD, Irwin DM, Zhang YP (2009) A profound role for the expansion of trypsin-like serine protease family in the evolution of hematophagy in mosquito. Mol Biol Evol 26:2333–2341PubMedGoogle Scholar
  176. Xiong B, Jacobs-Lorena M (1995) The black fly Simulium vittatum trypsin gene: characterization of the 5′-upstream region and induction by the blood meal. Exp Parasitol 81:363–370PubMedGoogle Scholar
  177. Zambonino-Infante JL, Cahu C (2007) Dietary modulation of some digestive enzymes and metabolic processes in developing marine fish: applications to diet formulation. Aquaculture 268:98–105Google Scholar
  178. Zlatanos S, Laskaridis K, Sagredos A (2009) Determination of proximate composition, fatty acid content and amino acid profile of five lesser-common sea organisms from the Mediterranean Sea. Int J Food Sci Tech 44:1590–1594Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Erick Perera
    • 1
    • 4
  • Leandro Rodríguez-Viera
    • 1
  • Rolando Perdomo-Morales
    • 2
  • Vivian Montero-Alejo
    • 2
  • Francisco Javier Moyano
    • 3
  • Gonzalo Martínez-Rodríguez
    • 4
  • Juan Miguel Mancera
    • 5
  1. 1.Center for Marine ResearchUniversity of HavanaHavanaCuba
  2. 2.Biochemistry DepartmentCenter for Pharmaceuticals Research and DevelopmentHavanaCuba
  3. 3.Department of Applied BiologyUniversity of AlmeriaAlmeríaSpain
  4. 4.ICMAN-CSIC, Apartado OficialPuerto RealSpain
  5. 5.Department of Biology, Faculty of Marine and Environmental ScienceUniversity of CadizCádizSpain

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