Silk gland fi broinase: Case study in Bombyx mori and Samia cynthia ricini
Main Article Content
Abstract
Fibroinase is a cathepsin L-like cysteine proteinase isolated from the silk glands of the silkworm, Bombyx mori, and the Eri silkworm, Samia cynthia ricini, and characterized by our research group. In B. mori, its physiological functions are disclosed as follows. (1) During each molt period in the larva, fi broinase is secreted into the lumen of the silk glands and digests the fi broin and sericin completely to make the lumen empty so that the silk gland cells can start synthesizing fi broin and sericin, and then secrete them into the lumen of the silk glands in the late molt period. (2) In day zero to day one pupa, fi broinase is secreted into the lumen of the silk glands and digests the remaining fi broin and sericin. (3) In the feeding period for each instar of the larva and in the spinning period for the last fi fth instar larva, fi broinase functions as a lysosomal proteinase in lysosomes within the silk gland cells for the digestion of obsolete proteins and organelles, such as mitochondria, endoplasmic reticulum, and ribosomal proteins, transported into the lysosomes for regeneration of the highly effi cient protein synthesis machinery. In S. cynthia ricini, the properties of fi boroinase are different in several points from those of B. mori, such as the N-terminal amino acid sequence, developmental profi le, and maximum activity. Higher maximum activity, 38 times the maximum activity of B. mori per individual insect, is observed at the end of spinning. The silk glands of S. cynthia ricini degenerate just after the end of the spinning and the day zero pupa has no silk glands. Accordingly, the physiological functions of fi broinase in S. cynthia ricini are the fi broinase functions (1) and (3) in B. mori. The purpose of this review article is to encourage researchers of insect science to start studying fi broinase of silk glands in other insect species and to fi nd out the species specifi city for a comprehensive view of silk gland fi broinase of a diverse array of insect species. As a guide for the study, we will present the study path in which knowledge of fi broinase in B. mori, and S. cynthia ricini, was obtained with the logic utilized.
Article Details
This work is licensed under a Creative Commons Attribution-NoDerivatives 4.0 International License.
References
Akai, H. 1965. Studies on the ultrastructure of the silk gland in the silkworm, Bombyx mori L. VI. Bulletin of Sericultural Experiment Station 19, 375-484. (in Japanese)
Akai, H. 1971. An ultrastructural study of changes during molting in the silk gland of larvae of the eri-silkwrom, Philosamia cynthia ricini Boisduval (Lepidoptera: Saturniidae). Applied Entomology and Zoology 66, 27-39.
Akai, H. 2005. Porous cocoon fi laments –Their characteristics and formation. International Journal of Wild Silkmoth & Silk 10, 57-74.
Akai, H. 2007. Why are lysosomes not released into silk gland lumen of Bombyx larvae. International Journal of Wild Silkmoth & Silk 12, 51-58.
Akai, H., Kiuchi, M. and Tamura, T. 1989. Ultrastructures of silk glands and cocoon fi laments of wild silkmoths, Antheraea yamamai and Antheraea pernyi. Wild Silkmoths 88, 9-23.
Akao, A. 1941. Studies on silk spinning by Bombyx mori larvae I. Accumulation of silk proteins in the silk gland of pupae by enforced silk spinning on a fl at surface and biochemical changes in haemolymph components, associated with autolysis of silk gland. Bulletin of the Imperial Sericultural Experiment Station 10, 189-227. (in Japanese with German summary)
Berger, E. and Kafatos, F. C. 1971a. Immunocytochemistry of an insect protease, cocoonase, and its zymogen. Immunochemistry 8, 391-394, 395-403.
Berger, E. and Kafatos, F.C. 1971b. Quantitative studies of prococoonase synthesis and accumulation during development. Developmental Biology 25, 377-397.
Berger, E., Kafatos, F. C., Felsted, R. L. and Law, J. H. 1971. Cocoonase III. Purifi cation, preliminary characterization, and activation of the zymogen of an insect protease. The Journal of Biological Chemistry 246, 4131-4137.
Chaitanya, R. K., Sridevi, P., Senthilkumaran, B. and Gupta A. D. 2011. 20-Hydroxyecdysone regulation of Hfi broin gene in the stored grain pest Corcyra cephalonica, during the last instar larval development. Steroids 76, 125-134.
Cherbas, L., Lee, K. and Cherbas, P. 1991. Identifi cation of ecdysone response elements by analysis of the Drosophila Eip28/29 gene. Genes and Development 5, 120-31.
Craig, C. L. and Riekel, C. 2002. Review Comparative architecture of silks, fi brous proteins and their encoding genes in insects and spiders. Comparative Biochemistry and Physiology 133B, 493-507.
Cristofoletti, P. T., Ribeiro, A. F. and Terra, W. R. 2005. The cathepsin L-like proteinases from the midgut of Tenebrio molitor larvae: Sequence, properties, immunocytochemical localization and function. Insect Biochemistry and Molecular Biology 35, 883-901.
D’Amato, F. 1989. Polyploidy in cell differentiation. Caryologia 42, 183-211.
Eguchi, M. and Iwamoto, A. 1975. Role of the midgut, crop, and maxillae of Bombyx mori in the production of cocoon-digestion enzyme. Journal of Insect Physiology 21, 1365-1372.
Fedic, R., Zurovec, M. and Sehnal, F. 2002. The silk of Lepidoptera. Journal of Insect Biotechnology and Sericology 71, 1-15.
Felsted, R. L., Kramer, K. J., Law, J. H., Berger, E. and Kafatos, F. C. 1973a. Cocoonase IV. Mechanism of activation of procoonase from Antheraea polyphemus. The Journal of Biological Chemistry 248, 3012- 3020.
Felsted, R. L., Law, J. H., Sinha, A. K. and Jolly, M. S. 1973b. Properties of the Antheraea mylitta cocoonase. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 44, 595-598.
Freddi, G., Mossotti, R. and Innocenti, R. 2003. Degumming of silk fabric with several proteases. Journal of Biotechnology 106, 101-112.
Fukumori, H., Teshiba, S., Shigeoka, Y., Yamamoto, K., Banno, Y. and Aso, Y. 2014. Purifi cation and characterization of cocoonase from the silkworm Bombyx mori. Bioscience, Biotechnology, and Biochemistry 78, 202-211.
Geng, P., Lin, L., Li, Y., Fan, Q., Wang, N., Song, L. and Li, W. 2014. A novel fi brin(ogen)olytic trypsin-like protease from Chinese oak silkworm (Antheraea pernyi): Purifi cation and characterization. Biochemical and Biophysical Research Communications 445, 64-70.
Hakim, R. S. and Kafatos, F. C. 1974. The structure and salivary function of the labial gland in adult Manuduca sexta. Tissue and Cell 6, 729-750.
Hruska, J. F., Law, J. H. and Kezdy, F. J. 1969. Differential titration of trypsin-like enzymes. Biochemical and Biophysical Research Communications 36, 272-277.
Hruska, J. F., Felsted, R. L. and Law, J. H. 1973. Cocoonase of silkworm moths: Catalytic properties and biological function. Insect Biochemistry 3, 31-43.
Inoue, S., Tanaka, K., Arisaka, F., Kimura, S., Ohtomo, K. and Mizuno, S. 2000. Silk fi broin of Bombyx mori is secreted, assembling a high molecular mass elementary unit consisting of H-chain, L-chain, and P25, with a 6:6:1 molar ratio. Journal of Biological Chemistry 275, 40517-40528.
Iwanaga, S. 1978. New synthetic peptide substrates for proteinases involved in blood coagulation–Kinin–fi - brinolysis. PRF, Protein Research Foundation Report 4, 1-12. (in Japanese) KAIKObase. http://sgp2010.dna.affrc.go.jp/KAIKObase/
Kafatos, F. C. 1968. The labial gland: a salt-secreting organ of Saturniid moths. Journal of Experimental Biology 48, 435-453.
Kafatos, F. C. 1972. The cocoonase zymogen cells of silk moths: a model of terminal cell differentiation for specifi c protein synthesis. Current Topics in Developmental Biology 7, 125-91.
Kafatos, F. C. and Feder, N. 1968. Cytodifferentiation during insect metamorphosis: The galea of silkmoths. Science 161, 470-472.
Kafatos, F. C. and Kiortsis, V. 1971. The packaging of a secretory protein Kinetics of cocoonase zymogen transport into a storage vacuole. The Journal of Cell Biology 48, 426-431.
Kafatos, F. C. and Reich, J. 1968. Stability of differentiation-specifi c and nonspecifi c messenger RNA in insect cells. Proceedings of the National Academy of Sciences USA 60, 1458-1465.
Kafatos, F. C. and Williams, C. M. 1964. Enzymatic mechanism for the escape of certain moths from cocoons. Science 146, 538-540.
Kafatos, F. C., Tartakoff, A. M. and Law, J. H. 1967a. Cocoonase I. Preliminary characterization of a proteolytic enzyme from silk moths. The Journal of Biological Chemistry 242, 1477-1487.
Kafatos, F. C., Law, J. H. and Tartakoff, A. M. 1967b. Cocoonase II. Substrate specifi city, inhibitors, and classifi cation of the enzyme. The Journal of Biological Chemistry 242, 1488-1494.
Katagata, Y., Kikuchi, A. and Shimura, K. 1984. Characterization of the crystalline-region peptides prepared from the posterior silk gland fi broin. Journal of Sericultural Science, Japan 53, 165-174.
Kiguchi, K. and Agui, N. 1981. Ecdysteroid levels and developmental events during larval molting in the silkworm, Bombyx mori. Journal of Insect Physiology 27, 805-812.
Kramer, K. J., Felsted, R. L. and Law, J. H. 1973. Cocoonase V. Structural studies on an insect serine protease. The Journal of Biological Chemistry 248, 3021- 3028.
Law, J. H. 2015. Breaking good: A chemist wanders into entomology. Annual Review of Entomology 60, 1-15.
Law, J. H., Dunn, P. E. and Kramer, K. J. 1977. Insect proteases and peptidases. Advances in Enzymology and Related Areas of Molecular Biology 45, 389-425.
Matsuura, S., Morimoto, T., Nagata, S. and Tashiro, Y. 1968. Studies on the posterior silk gland of the silkworm, Bombyx mori II. Cytolytic processes in posterior silk gland cells during metamorphosis from larva to pupa. The Journal of Cell Biology 38, 589- 603.
Morimoto T., Matsuura, S., Nagata, S. and Tashiro, Y. 1968. Studies on the posterior silk gland of the silkworm, Bombyx mori III. Ultrastructural changes of posterior silk gland in the fourth larval instar. The Journal of Cell Biology 38, 604-614.
Oda, K. 2012. New families of carboxyl peptidases: serinecarboxyl peptidases and glutamic peptidases. Journal of Biochemistry 151, 13-25.
Ono, M. 1942. Studies on silk spinning by Bombyx mori larvae II. Morphological and physiological changes in pupae and silk proteins remaining in the silk gland by enforced silk spinning on a fl at surface. Bulletin of the Imperial Sericultural Experiment Station 10, 495-542 (in Japanese with German summary).
Oyama, F., Mizuno, S. and Shimura, K. 1984. Predominant synthesis of fi broin heavy and light chains on the membrane-bound polysomes prepared from the posterior silk gland of the silkworm, Bombyx mori. Journal of Biochemistry 96, 1143-1153.
Prasad, B. C., Pandy, J. P. and Sinha, A. K. 2012. Studies on Antheraea mylitta cocoonase and its use in cocoons cooking. American Journal of Food Technology 7, 320-325.
Prasad, S. V., Fernando-Warnakulasuriya, G. J. P., Sumida, M., Law, J. H. and Wells, M. A. 1986. Lipoprotein biosynthesis in the larvae of the tobacco hornworm, Manduca sexta. Journal of Biological Chemistry 261,17174-17176.
Rachner, T. D., Khosla, S. and Hofbauer, L. C. 2011. Osteoporosis: now and the future. The Lancet 377, 1276-1287.
Rawlings, N. D. and Barrett, A. J. 1994. Families of cysteine peptidases. Method in Enzymology 244, 461-486.
Repnik, U., Stoka, V., Turk, V. and Turk, B. 2012. Lysosomes and lysosomal cathepsins in cell death. Biochimica et Biophysica Acta 1824, 22-33.
Rodbumrer, P., Arthan, D., Uyen, U., Yuvaniyama, J., Svasti, J. and Wongsaengchantra, P. Y. 2012. Functional expression of a Bombyx mori cocoonase: potential application for silk degumming. Acta Biochimica et Biophysica Sinica 44, 974-983.
Selman, K. and Kafator, F. C. 1975. Differentiation in the cocoonase producing silkmoth galea: Ultrastructural studies. Developmental Biology 46, 132-150.
Sezutsu, H. and Yukuhiro, K. 2014. The complete nucleotide sequence of the Eri-silkworm (Samia cynthia ricini) fi broin gene. Journal of Insect Biotechnology and Sericology 83, 59-70.
Shirai, H., Kamimura, M., Yamaguchi, J., Imanishi, S., Kojima, T. and Fujiwara, H. 2012. Two adjacent cisregulatory elements are required for ecdysone response of Ecdysone receptor (EcR) B1 transcription. PLOS ONE 7 (11), e49348.
Sumida, M. 2001. Silk gland developmental program in the wild silkmoth, Samia cynthia ricini and the domesticated silkworm, Bombyx mori. International Journal of Wild Silkmoth & Silk 6, 87-90.
Sumida, M. 2010. Fibroinase revisited–How fi broinase was isolated, how its function was revealed, what fi broinase study implicates. International Journal of Wild Silkmoth & Silk 14, 61-76.
Sumida, M. and Sutthikhum, V. 2015. Fibroin and sericinderived bioactive peptides and hydrolysates as alternative sources of food additive for promotion of human health: A review. Research & Knowledge, 1(2), 1-17.
Sumida, M. and Ueda, H. 2007. Dietary sucrose suppresses midgut sucrase activity in germfree, fi fth instar larvae of the silkworm, Bombyx mori. Journal of Insect Biotechnology and Sericology 76, 31-37. (https://www.jstage.jst.go.jp/article/jibs/76/1/76 _1_1_31/_pdf)
Sumida, M. and Yamashita, O. 1983. Purifi cation and some properties of soluble trehalase from midgut of pharate adult of the silkworm, Bombyx mori. Insect Biochemistry 13, 257-265.
Sumida, M., Takimoto, S., Ukai, M. and Matsubara, F. 1993a. Occurrence of fi broinase in degenerating silk gland in the pharate adult of the silkworm, Bombyx mori. Comparative Biochemistry and Physiology 105B, 239-245.
Sumida, M., Takimoto, S. and Matsubara, F. 1993b. Fibroinase from silk gland in the fourth molt stage in the silkworm, Bombyx mori. Comparative Biochemistry and Physiology 105B, 247-251.
Sutthikhum, V., Watanabe, M. and Sumida, M. 2004a. Fibroinase activity in Bomby mori silk gland in the larval-pupal development and its partial purifi cation from spinning larva. Journal of Insect Biotechnology and Sericology 73, 71-79. (https://www.jstage.jst. go.jp/article/jibs/73/2/73_2_71/_pdf)
Sutthikhum, V., Watanabe, M. and Sumida, M. 2004b. Fibroinase, a cathepsin L-like cysteine proteinase from the silk gland of spinning Bombyx mori larva, a counterpart in the silk gland of wild silkmoths, Samia cynthia ricini and Antheraea pernyi: Purifi cation and characterization. International Journal of Wild Silkmoth & Silk, 9, 21-38.
Tagami, K., Kakegawa, H., Kamioka, H., Sumitani, K., Kawata, T., Lenarcic, B., Turk, V. and Katunuma, N. 1994. The mechanisms and regulation of procathepsin L secretion from osteoclast in bone resorption. FEBS Letters 342, 308-312.
Takasu, Y., Yamada, H. and Tsubouchi, K. 2002. Isolation of three main sericin components from the cocoon of the silkworm, Bombyx mori. Bioscience, Biotechnology, and Biochemistry 66, 2715-2718.
Takei, F., Kikuchi, Y., Kikuchi, A., Mizuno, S. and Shimura, K. 1987. Further evidence for importance of the subunit combination of silk fi broin in its effi cient secretion from the posterior silk gland cells. The Journal of Cell Biology 105, 175-180.
Tashiro, Y., Morimoto, T., Matsuura, S. and Nagata, S. 1968. Studies on the posterior silk gland of the silkworm, Bombyx mori I. Growth of posterior silk gland cells and biosynthesis of fi broin during the fi fth larval instar. The Journal of Cell Biology 38, 574- 588.
Tsuda, H., Kurata, K. and Miyazawa, M. 2005. Proteolytic characterization of cocoonase from the domestic silk moth, Bombyx mori. Peptide Science 42, 479-482.
Turk, V., Stoka, V., Vasiljeva, O., Renko, M., Sun, T., Turk, B. and Turk, D. 2012. Cysteine cathepsins: From structure, function and regulation to new frontiers. Biochemica et Biophysica Acta – Proteins and Proteomics 1824, 68-88.
Unajak, S., Arrnluke, S. and Promboon, A. 2014. An active recombinant cocoonase from the silkworm Bombyx mori: bleaching, degumming and sericin degrading activities. Journal of the Science of Food and Agriculture. (DOI: 10.1002/jsfa.6806.)
Watanabe, M. and Sumida, M. 2006. Enzymatic properties of purifi ed fi broinase of Eri-silkworm, Samia cynthia ricini at end of spinning. International Journal of Wild Silkmoth & Silk 11, 60-72.
Watanabe, M., Fujii, S., Miyata, S. and Sumida, M. 2004b. Localization of fi broinase in the silk gland of domesticated silkworm, Bombyx mori, wild silkmoths, Samia cynthia ricini and Antheraea pernyi studied by confocal laser scanning microscopy. International Journal of Wild Silkmoth & Silk 9, 1-14.
Watanabe, M., Fujii, S. and Sumida, M. 2006c. Fibroinase of silk gland of Eri-silkworm, Samia cynthia ricini. Enzymatic properties at the fourth molt period, stage D2, and changes in activity during the fi fth instar. International Journal of Wild Silkmoth & Silk 11, 41-51.
Watanabe, M., Fujii, S., Hinuma, H. and Sumida, M. 2004c. Cathepsin activities in the silk gland of the domesticated silkworm, Bombyx mori, the wild silkmoths, Samia cynthia ricini and Antheraea pernyi during the fi fth instar larval development. International Journal of Wild Silkmoth & Silk 9, 15-20.
Watanabe, M., Kamei, K. and Sumida, M. 2007. Sericin digestion by fi broinase, a cathepsin L-like cysteine proteinase, of Bombyx mori silk gland. Journal of Insect Biotechnology and Sericology 76, 9-15. (https://www.jstage.jst.go.jp/article/jibs/76/1/76_ 1_1_9/_pdf)
Watanabe, M., Kamei, K. and Sumida, M. 2006b. Fibroinase activity of silk gland in larval and early pupal development of the silkworm, Bombyx mori assayed with a fl uorescent quenched peptide substrate. Journal of Insect Biotechnology and Sericology 75, 115- 126. (https://www.jstage.jst.go.jp/article/jibs/75/3/75 _3_115/_pdf)
Watanabe, M., Kotera, T. and Sumida, M. 2006a. Enzymatic properties of fi broinase of silk gland from day one pupa of the silkworm, Bombyx mori. Journal of Insect Biotechnology and Sericology 75, 39-46. (https://www.jstage.jst.go.jp/article/jibs/75/1/75 _1_39/_pdf)
Watanabe, M., Sutthikhum, V., Kotera, T., Okumura, M., Nagaoka, S., Kamei, K., Mori, H. and Sumida, M. 2006d. Bombyx cysteine proteinase of silk gland (BCPSG): Cloning of cDNA and characterization of recombinant enzyme expressed in E. coli. International Journal of Wild Silkmoth & Silk 11, 73-90.
Watanabe, M., Yura, A., Yamanaka, M., Kamei, K. Hara, S. and Sumida, M. 2004a. Purifi cation and characterization of fi broinase, a cathepsin L-like cysteine proteinase, from the silk gland in the fourth instar Bombyx mori larva at the fourth molt period, stage D2 . Journal of Insect Biotechnology and Sericology 73, 61-70. (https://www.jstage.jst.go.jp/article/ jibs/73/2/73_2_61/_pdf)
Wattiaux, R. and Duve, C. de. 1956. Tissue fractionation studies 7. Release of bound hydrolases by means of Triton X-100. Biochemical Journal 63, 606-608.
Yamamoto, Y., Takimoto, K., Izumi, S., Toriyama-Sakurai, M., Kageyama, T. and Takahashi, S.Y. 1994. Molecular cloning and sequencing of cDNA that encodes cysteine proteinase in the egg of the silkmoth, Bombyx mori. Journal of Biochemistry (Tokyo) 116, 1330-1335.
Yamazaki, Y., Ogawa, K. and Kanekatsu, R. 1992. Isolation of cocoonase from the silkworm, Bombyx mori by high performance liquid chromatography and catalytic specifi city. Journal of Sericultural Science, Japan 61, 228-235. (in Japanese with English summary)
Yamazaki, Y., Ogawa, K. and Kanekatsu, R. 1995. N-terminal amino acid sequence of cocoonase in the silkworm, Bombyx mori. Journal of Sericultural Science of Japan 64, 467-468.
Yang, J., Wang, W., Li, B., Wu, Y., Wu, H. and Shen, W. 2009. Expression of cocoonase in silkworm (Bombyx mori) cells by using a recombinant baculovirus and its bioactivity assay. International Journal of Biology 1, 107-112.
Zhou, C. Z., Confalonieri, F., Medina, N., Zivonovic, Y., Esnault, C., Yang, T., Jacquet, M., Janin, J., Duguet, M., Perasso, R. and Li, Z. G. 2000. Fine organization of Bombyx mori fi broin heavy chain gene. Nucleic Acids Research 28, 2413-2419.