Cathepsin B differential expression and enzyme processing and activity during Fundulus heteroclitus embryogenesis

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 158, Issue 2, 2011, Pages 221-228

  Tingaud Sequeira, Angèle ^a   Carnevali, Oliana ^b   Cerdà, Joan ^a  

^a INSTITUT DE CIÈNCIES DEL MAR   (Spain)

^b UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

Author keywords

Cathepsin; Embryo; Enzyme processing; Gastrulation; Yolk metabolism

Indexed keywords

CATHEPSIN B; CATHEPSIN L;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CATALYSIS; CELLULAR DISTRIBUTION; CYPRINODONTIFORMES; ELECTROPHORESIS; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; FERTILIZATION; GASTRULATION; GENETIC TRANSCRIPTION; NEURULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION;

CYPRINODONTOIDEI; FUNDULUS HETEROCLITUS; TELEOSTEI;

EID: 78650523370     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2010.11.002     Document Type: Article

References (73)

1. Ahn S.J., Kim N.Y., Jeon S.J., Sung J.H., Je J.E., Seo J.S., Kim M.S., Kim J.K., Chung J.K., Lee H.H. Molecular cloning, tissue distribution and enzymatic characterization of cathepsin X from olive flounder (Paralichthys olivaceus). Comp. Biochem. Physiol. B 2008, 151:203-212.
2. Ahn S.J., Kim N.Y., Seo J.S., Je J.E., Sung J.H., Lee S.H., Kim M.S., Kim J.K., Chung J.K., Lee H.H. Molecular cloning, mRNA expression and enzymatic characterization of cathepsin F from olive flounder (Paralichthys olivaceus). Comp. Biochem. Physiol. B 2009, 154:211-220.
3. Alt B., Reibe S., Feitosa N.M., Elsalini O.A., Wendl T., Rohr K.B. Analysis of origin and growth of the thyroid gland in zebrafish. Dev. Dyn. 2006, 235:1872-1883.
4. Amano H., Fujita T., Hiramatsu N., Kagawa H., Matsubara T., Sullivan C.V., Hara A. Multiple vitellogenin-derived yolk proteins in gray mullet (Mugil cephalus): disparate proteolytic patterns associated with ovarian follicle maturation. Mol. Reprod. Dev. 2008, 75:1307-1317.
5. Armstrong P.B., Child J.W. Stages in the normal development of Fundulus heteroclitus. Biol. Bull. 1965, 128:143-168.
6. Authier F., Mort J.S., Bell A.W., Posner B.I., Bergeron J.J. Proteolysis of glucagon within hepatic endosomes by membrane-associated cathepsins B and D. J. Biol. Chem. 1995, 270:15798-15807.
7. Azaryan A.V., Hook V.Y. Unique cleavage specificity of 'prohormone thiol protease' related to proenkephalin processing. FEBS Lett. 1994, 341:197-202.
8. Bechet D.M., Ferrara M.J., Mordier S.B., Roux M.P., Deval C.D., Obled A. Expression of lysosomal cathepsin B during calf myoblast-myotube differentiation. Characterization of a cDNA encoding bovine cathepsin B. J. Biol. Chem. 1991, 266:14104-14112.
9. Blomberg L., Hashizume K., Viebahn C. Blastocyst elongation, trophoblastic differentiation, and embryonic pattern formation. Reproduction 2008, 135:181-195.
10. Britton C., Murray L. Cathepsin L protease (CPL-1) is essential for yolk processing during embryogenesis in Caenorhabditis elegans. J. Cell Sci. 2004, 117:5133-5143.
11. Callegari E.A., Ferguson-Gottschall S., Gibori G. PGF2alpha induced differential expression of genes involved in turnover of extracellular matrix in rat decidual cells. Reprod. Biol. Endocrinol. 2005, 3:3.
12. Campbell C.M., Idler D.R. Characterization of an estradiol-induced protein from rainbow trout serum as vitellogenin by the composition and radioimmunological cross reactivity to ovarian yolk fractions. Biol. Reprod. 1980, 22:605-617.
13. Carnevali O., Centonze F., Brooks S., Marota I., Sumpter J.P. Molecular cloning and expression of ovarian cathepsin D in seabream, Sparus aurata. Biol. Reprod. 1999, 61:785-791.
14. Carnevali O., Carletta R., Cambi A., Vita A., Bromage N. Yolk formation and degradation during oocyte maturation in seabream Sparus aurata Involvement of two lysosomal proteinases. Biol. Reprod. 1999, 60:140-146.
15. Carnevali O., Cionna C., Tosti L., Lubzens E., Maradonna F. Role of cathepsins in ovarian follicle growth and maturation. Gen. Comp. Endocrinol. 2006, 146:195-203.
16. Carnevali O., Cionna C., Tosti L., Cerdà J., Gioacchini G. Changes in cathepsin gene expression and relative enzymatic activity during gilthead sea bream oogenesis. Mol. Reprod. Dev. 2008, 75:97-104.
17. Carnevalli O., Mosconi G., Cambi A., Ridolfi S., Zanuy S., Polzonetti-Magni A.M. Changes of lysosomal enzyme activities in sea bass (Dicentrarchus labrax) eggs and developing embryos. Aquaculture 2001, 202:249-256.
18. Cerdà J., Calman B.G., LaFleur G.J., Limesand S. Pattern of vitellogenesis and follicle maturational competence during the ovarian follicular cycle of Fundulus heteroclitus. Gen. Comp. Endocrinol. 1996, 103:24-35.
19. Cerdà J., Fabra M., Raldúa D. Physiological and molecular basis of fish oocyte hydration. The Fish Oocyte: from Basic Studies to Biotechnological Applications 2007, 349-396. Springer-Verlag, The Netherlands. P. Babin, J. Cerdà, E. Lubzens (Eds.).
20. 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 involved in embryonic degradation of vitellin is produced as a latent extraovarian precursor. J. Biol. Chem. 1999, 274:13311-13321.
21. Devauchelle N., Coves D. The characteristics of sea bass (Dicentrarchus labrax) eggs: description, biochemical composition and hatching performances. Aquat. Liv. Resourc. 1988, 1:223-230.
22. 2+-dependent thiol protease. Eur. J. Biochem. 1986, 155:409-413.
23. Eykelbosh A.J., Van Der Kraak G. A role for the lysosomal protease cathepsin B in zebrafish follicular apoptosis. Comp. Biochem. Physiol. A 2010, 156:218-223.
24. Fabra M., Cerdà J. Ovarian cysteine proteinases in the teleost Fundulus heteroclitus: molecular cloning and gene expression during vitellogenesis and oocyte maturation. Mol. Reprod. Dev. 2004, 67:282-294.
25. Ferrara M., Wojcik F., Rhaissi H., Mordier S., Roux M.-P., Bechet D. Gene structure of mouse cathepsin B. FEBS Lett. 1990, 273:195-199.
26. Finn R.N. The maturational disassembly and differential proteolysis of paralogous vitellogenins in a marine pelagophil teleost: a conserved mechanism of oocyte hydration. Biol. Reprod. 2007, 76:936-948.
27. Finn R.N. Vertebrate yolk complexes and the functional implications of phosvitins and other subdomains in vitellogenins. Biol. Reprod. 2007, 76:936-948.
28. Finn R.N., Fyhn H.J. Requirement for amino acids in ontogeny of fish. Aquac. Res. 2010, 41:684-716.
29. Finn R.N., Kristoffersen B.A. Vertebrate vitellogenin gene duplication in relation to the "3R Hypothesis": correlation to the pelagic egg and the oceanic radiation of teleosts. PLoS ONE 2 2007, e169.
30. Finn R.N., Fyhn H.J., Henderson R.J., Evjen M.S. The sequence of catabolic substrate oxidation and enthalpy balance of developing embryos and yolk-sac larvae of turbot (Scophthalmus maximus L.). Comp. Biochem. Physiol. A 1996, 115:133-151.
31. Finn R.N., Kolarevic J., Kongshaug H., Nilsen F. Evolution and differential expression of a vertebrate vitellogenin gene cluster. BMC Evol. Biol. 2009, 9:2.
32. Greeley M.S., Calder D.R., Wallace R.A. Changes in teleost yolk proteins during oocyte maturation: correlation of yolk proteolysis with oocyte hydration. Comp. Biochem. Physiol. B 1986, 84:1-9.
33. Heming T.A., Buddington R.K. Yolk absorption in embryonic and larval fishes. Fish Physiology 1988, vol 11A:407-446. Academic press, New York.
34. Hiramatsu N., Ichikawa N., Fukada H., Fujita T., Sullivan C.V., Hara A. Identification and characterization of proteases involved in specific proteolysis of vitellogenin and yolk proteins in salmonids. J. Exp. Zool. 2002, 292:11-25.
35. Hoch R.V., Soriano P. Roles of PDGF in animal development. Development 2003, 130:4769-4784.
36. Hsing L.C., Rudensky A.Y. The lysosomal cysteine proteases in MHC class II antigen presentation. Immunol. Rev. 2005, 207:229-241.
37. Ishidoh K., Kominami E. Processing and activation of lysosomal proteinases. Biol. Chem. 2002, 383:1827-1831.
38. Je J.E., Ahn S.J., Kim N.Y., Seo J.S., Kim M.S., Park N.G., Kim J.K., Chung J.K., Lee H.H. Molecular cloning, expression analysis and enzymatic characterization of cathepsin K from olive flounder (Paralichthys olivaceus). Comp. Biochem. Physiol. A 2009, 154:474-485.
39. Jia A., Zhang X.H. Molecular cloning, characterization and expression analysis of cathepsin D gene from turbot Scophthalmus maximus. Fish Shellfish Immunol. 2009, 26:606-613.
40. Kao C.M., Huang F.L. Cloning and expression of carp cathepsin Z: possible involvement in yolk metabolism. Comp Biochem Physiol B 2008, 149:541-551.
41. Kestemont P., Cooremans J., Abi-Ayad A., Mélard C. Cathepsin L in eggs and larvae of perch Perca fluviatilis: variations with developmental stage and spawning period. Fish Physiol. Biochem. 1999, 21:59-64.
42. Kwon J.Y., Prat F., Randall C., Tyler C.R. Molecular characterization of putative yolk processing enzymes and their expression during oogenesis and embryogenesis in rainbow trout (Oncorhynchus mykiss). Biol. Reprod. 2001, 65:1701-1709.
43. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
44. LaFleur G.J., Raldúa D., Fabra M., Carnevali O., Denslow N., Wallace R.A., Cerdà J. Derivation of major yolk proteins from parental vitellogenins and alternative processing during oocyte maturation in Fundulus heteroclitus. Biol. Reprod. 2005, 73:815-824.
45. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
46. Mallya S., Partin J.S., Valdizan M.C., Lennarz W.J. Proteolysis of the major yolk glycoproteins is regulated by acidification of the yolk platelets in sea urchin embryos. J. Cell Biol. 1992, 117:1211-1221.
47. Matsubara T., Sawano K. Proteolytic cleavage of vitellogenin and yolk proteins during vitellogenin uptake and oocyte maturation in barfin flounder (Verasper moseri). J. Exp. Zool. 1995, 272:34-45.
48. Matsubara T., Nagae M., Ohkubo N., Andoh T., Sawaguchi S., Hiramatsu N., Sullivan C.V., Hara A. Multiple vitellogenins and their unique roles in marine teleosts. Fish Physiol. Biochem. 2003, 28:295-299.
49. McPherson R., Greeley M.S., Wallace R.A. The influence of yolk protein proteolysis on hydration in the oocytes of Fundulus heteroclitus. Dev. Growth Differ. 1989, 31:475-483.
50. Meyer A., Van de Peer Y. From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 2005, 27:937-945.
51. Miyata S., Kubo T. Inhibition of gastrulation in Xenopus embryos by an antibody against a cathepsin L-like protease. Dev. Growth Differ. 1997, 39:111-115.
52. Murakami M., Iuchi I., Yamagami K. Yolk phosphoprotein metabolism during early development of the fish Oryzias latipes. Dev. Growth Differ. 1990, 32:619-627.
53. Ohkubo N., Matsubara T. Sequential utilization of free amino acids, yolk proteins and lipids in developing eggs and yolk-sac larvae of barfin flounder Verasper moseri. Mar. Biol. 2002, 140:187-196.
54. Oursler M.J., Riggs B.L., Spelsberg T.C. Glucocorticoid-induced activation of latent transforming growth factor-beta by normal human osteoblast-like cells. Endocrinology 1993, 133:2187-2196.
55. Park E.M., Kim Y.O., Nam B.H., Kong H.J., Kim W.J., Lee S.J., Kim K.K. Cloning and expression analysis of cathepsin D in the olive flounder Paralichthys olivaceus. Biosci. Biotechnol. Biochem. 2009, 73:1856-1859.
56. +-ATPase inhibitor: effects on the hydration mechanism. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 290:R456-R466.
57. Rauch G.J., Lyons D.A., Middendorf I., Friedlander B., Arana N., Reyes T., Talbot W.S. Submission and Curation of Gene Expression Data. ZFIN Direct Data Submission 2003.
58. Roberts R. Lysosomal cysteine proteases: structure, function and inhibition of cathepsins. Drug News Perspect. 2005, 18:605-614.
59. Sire M.F., Babin P.J., Vernier J.M. Involvement of the lysosomal system in yolk protein deposit and degradation during vitellogenesis and embryonic development in trout. J. Exp. Zool. 1994, 269:69-83.
60. Tan Y., Osatomi K., Nozaki Y., Ishihara T., Hara K. Occurrence of two distinct molecular species of cathepsin B in carp. Fish. Sci. 2006, 72:185-194.
61. Thisse B., Pflumio S., Fürthauer M., Loppin B., Heyer V., Degrave A., Woehl R., Lux A., Steffan T., Charbonnier X.Q., Thisse C. Expression of the zebrafish genome during embryogenesis (NIH R01 RR15402). ZFIN Direct Data Submission 2001.
62. Tingaud-Sequeira A., Cerdà J. Phylogenetic relationships and gene expression pattern of three different cathepsin L (Ctsl) isoforms in zebrafish: Ctsla is the putative yolk processing enzyme. Gene 2007, 386:98-106.
63. Tingaud-Sequeira A., Zapater C., Chauvigne F., Otero D., Cerdà J. Adaptive plasticity of killifish (Fundulus heteroclitus) embryos: dehydration-stimulated development and differential aquaporin-3 expression. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 296:R1041-R1052.
64. Tobin D.J., Foitzik K., Reinheckel T., Mecklenburg L., Botchkarev V.A., Peters C., Paus R. The lysosomal protease cathepsin L is an important regulator of keratinocyte and melanocyte differentiation during hair follicle morphogenesis and cycling. Am. J. Pathol. 2002, 160:1807-1821.
65. Wallace R.A., Begovac P. Phosvitins in Fundulus oocytes and eggs. J. Biol. Chem. 1985, 260:11268-11274.
66. Wallace R.A., Selman K. Major proteins changes during vitellogenesis and maturation of Fundulus oocytes. Dev. Biol. 1985, 110:492-498.
67. Walzer C., Schönenberger N. Ultrastructure and cytochemistry study of the yolk syncytial layer in the alevin of trout (Salmo fario trutta L.) after hatching. I. The vitellolysis zone. Cell Tissue Res. 1979, 196:59-73.
68. Walzer C., Schönenberger N. Ultrastructure and cytochemistry of the yolk syncytial layer in the alevin of trout (Salmo fario trutta L. and Salmo gairdneri R.) after hatching. II. The cytoplasmic zone. Cell Tissue Res. 1979, 196:75-93.
69. Yajima Y., Kawashima S. Calpain function in the differentiation of mesenchymal stem cells. Biol. Chem. 2002, 383:757-764.
70. Yasothornsrikul S., Greenbaum D., Medzihradszky K.F., Toneff T., Bundey R., Miller R., Schilling B., Petermann I., Dehnert J., Logvinova A., Goldsmith P., Neveu J.M., Lane W.S., Gibson B., Reinheckel T., Peters C., Bogyo M., Hook V. Cathepsin L in secretory vesicles functions as a prohormone-processing enzyme for production of the enkephalin peptide neurotransmitter. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:9590-9595.
71. Yeh H.Y., Klesius P.H. Molecular cloning, sequencing and characterization of channel catfish (Ictalurus punctatus, Rafinesque 1818) cathepsin S gene. Vet. Immunol. Immunopathol. 2008, 126:382-387.
72. Yeh H.Y., Klesius P.H. Channel catfish, Ictalurus punctatus, cysteine proteinases: cloning, characterisation and expression of cathepsin H and L. Fish Shellfish Immunol. 2009, 26:332-338.
73. Zhang T., Rawson D.M., Tosti L., Carnevali O. Cathepsin activities and membrane integrity of zebrafish (Danio rerio) oocytes after freezing to -196 degrees C using controlled slow cooling. Cryobiology 2008, 56:138-143.