Effects of Vertebrate Insulin Hormone on Major Hemolymph Proteins and Ovarium Development in The Silkworm Bombyx mori Pupal Stage

Tugce Ordu; Kübra Yılmaz; Ebru Göncü

doi:10.18016/ksutarimdoga.vi.1627726

EN TR

Effects of Vertebrate Insulin Hormone on Major Hemolymph Proteins and Ovarium Development in The Silkworm Bombyx mori Pupal Stage

Abstract

Insulin, released from the islets of Langerhans in the pancreas, regulates sugar metabolism and plays a key role in growth, differentiation, metabolism, and apoptosis in both vertebrates and invertebrates. Vertebrate insulin affects anabolic metabolism by activating glucose uptake and conversion while inhibiting glycogen degradation. The first insulin-like peptide (ILP) identified in invertebrates was bombyxin from Bombyx mori, which regulates growth, metabolism, and egg development, and is homologous to mammalian insulin. In insects, hemolymph consists of plasma and hemocytes, which are essential for defense against microorganisms and antigens. All events, such as the transportation of hormones and nutrients to target cells and the sending of waste to excretory organs, occur through hemolymph. The key organs that play a role in reproductive physiology in female insects are the fat body and the ovary. Some proteins synthesized by fat body cells are transported to the ovary via hemolymph during the pupal period and play a role in egg development. Due to different physiological processes, the content and amount of hemolymph proteins change in larval, pupal, and adult stages. In this study, vertebrate insulin was injected into B. mori female pupae on different days, and its effects on ovarian development and major hemolymph proteins were investigated. For this purpose, histological and electrophoretic methods were used. Findings showed that the vertebrate hormone insulin causes changes in the relative abundance of essential proteins in the ovary and hemolymph of female B. mori pupae.

Keywords

İpek Böceği Bombyx mori Pupal Döneminde Omurgalı İnsülin Hormonunun Temel Hemolenf Proteinleri ve Ovaryum Gelişimi Üzerine Etkileri

Öz

Omurgalı canlılarda pankreasın Langerhans adacıklarından salınan insülin, vücudun şeker metabolizmasının düzenlenmesinde önemli hormonlardan biridir. Omurgalı ve omurgasız hayvanlarda insülin ve insülin ilişkili peptidlerin büyüme, farklılaşma, metabolizma ve apoptozis gibi hücresel süreçlerin düzenlenmesinde önemli bir rol oynadığı bilinmektedir. Omurgalı insülini, glikojen yıkımını inhibe ederken glikoz alımını ve dönüştürmeyi aktive ederek anabolik metabolizmayı etkiler. Omurgasız hayvanlardaki insülin benzeri peptid olarak belirlenen ilk molekül Bombyx mori’ de belirlenmiş ve bombyxin adını almıştır. Bombyxinler, böcek büyümesini, karbonhidrat metabolizmasını ve yumurta gelişimini düzenler. Böceklerdeki insülin benzeri peptidler moleküler formda memelilerin insülinlerine homologdurlar, ayrıca işlevsel olarak eşdeğerdirler. Hemolenf, hayvanın vücudunu mikroorganizmalardan ve antijenlerden koruyan hemositlerden ve plazmadan oluşur. Hormonların ve besin maddelerinin hedef hücrelere taşınımı ve atıkların boşaltım organlarına gönderilmesi gibi tüm olaylar hemolenf aracılığıyla olur. Dişi böceklerdeki üreme fizyolojisinde rol oynayan anahtar organlar yağ doku ve ovaryumdur. Yağ doku hücreleri tarafından sentezlenen bazı proteinler pupal dönem boyunca hemolenf aracılığıyla ovaryuma taşınır ve yumurta gelişiminde rol alır. Farklı fizyolojik süreçlerden dolayı hemolenf proteinlerin içeriği ve miktarı larval, pupal ve ergin evrelerde değişmektedir. Bu çalışmada pupal evrenin farklı günlerinde Bombyx mori dişi pupalarına omurgalı insülini enjekte edilmiş, ovaryum gelişimine ve temel hemolenf proteinleri üzerindeki etkileri araştırılmıştır. Bu amaçla histolojik ve elektroforetik yöntemler kullanılmıştır. Elde edilen bulgular omurgalı hormonu olan insülinin, dişi Bombyx mori pupalarının ovaryum ve hemolenfinde bulunan temel proteinlerin nispi yoğunluklarında değişimler meydana getirdiğini göstermiştir.

Anahtar Kelimeler

Kaynakça

Babila Jasmine, J., Annalakshmi, T., & Syed Ali Fathima, K. M. (2024). Studies on the effects of Insect Growth Regulators on Haemolymph Proteins in Relation to Morbidity in Silkworm of Bombyx mori. L. Advance Research Trends in Biology, 366.
Batcha, M. M., Ahamed, A. S., Rahman, M. A. U., Janarthanan, S., & Krishnan, M. (2023). The in-vitro and in-vivo radio labeling unfolds the vitellogenin protein expression site of Bombyx mori L as the ventral perivisceral fat body. Journal of Asia-Pacific Entomology, 26(2), 102087.
Biolo, G., & Wolfe, R. R. (1993). Insulin action on protein metabolism. Bailliere's clinical endocrinology and metabolism, 7(4), 989-1005.
Bradford, M.M., (1976). A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Analytical Biochemistry, 72: 248-254 pp.
Brogiolo, W., Stocker, H., Ikeya, T., Rintelen, F., Fernandez, R., & Hafen, E. (2001). An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Current biology, 11(4), 213-221.
Engelmann, F. (2013). The Physiology of Insect Reproduction: International Series of Monographs in Pure and Applied Biology: Zoology. Elsevier.
Gamo, T. (1978). Low molecular weight lipoproteins in the haemolymph of the silkworm, Bombyx mori: inheritance, isolation and some properties. Insect Biochemistry, 8, 457-470
Gu, S. H., & Lin, P. L. (2024). Upregulation of Insulin and Ecdysone Signaling in Relation to Diapause Termination in Bombyx mori Eggs Exposed to 5° C. Insects, 15(12), 989.

Gu, S. H., Chang, C. H., & Lin, P. L. (2022). Bombyxin-stimulated ecdysteroidogenesis in relation to sugar transporter/trehalase expressions in Bombyx prothoracic glands. Insect Biochemistry and Molecular Biology, 151, 103864.
Gültekin, S. (2024). The Therapeutic Potential of Berberine and Resveratrol in Type 2 Diabetes Treatment: Pharmacokinetic and Bioactivity Properties, and Molecular Docking Analysis. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 27(Ek Sayı 2 (Suppl 2)), 333-350.
Hyršl, P., & Šimek, V. (2005). An analysis of hemolymph protein profiles during the finalinstar, prepupa and pupa of the silkworm, Bombyx mori(Lepidoptera: Bombycidae). Biologia, 60.
Izumi, S., & Tomino, S. (1976). Protein metabolism during insect metamorphosis. I. Translation of the silkworm mRNA in wheat embryo cell-free system. Zool. Mag, 85(406), 100-113.
Izumi, S., Tomino, S., & Chino, H. (1980). Purification and molecular properties of vitellin from the silkworm, Bombyx mori. Insect Biochemistry, 10(2), 199-208.
Jouni, Z. E., Takada, N., Gazard, J., Maekawa, H., Wells, M. A., & Tsuchida, K. (2003). Transfer of cholesterol and diacylglycerol from lipophorin to Bombyx mori ovarioles in vitro: role of the lipid transfer particle. Insect biochemistry and molecular biology, 33(2), 145-153.
Kawooya, J. K., & Law, J. H. (1988). Role of lipophorin in lipid transport to the insect egg. Journal of Biological Chemistry, 263(18), 8748-8753 pp.
Keleş, İ., Bayrakdar, A., & Olgun, N. (2024). Investigation of The Efficacy of Plantago Major Flavonoids in The Healing of Diabetic Foot Wound in Silico Analysis. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 27(5), 1032-1041.
Kim, E.J., Park, H.I. and Park, T.H. (2003). Inhibition of apoptosis by recombinant 30K protein originating from silkworm hemolymph. Biochemical and Biophysical Research Communications 308: 523-528.
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685 pp.
Liu, W., Gray, S., Huo, Y., Li, L., Wei, T., & Wang, X. (2015). Proteomic analysis of interaction between a plant virus and its vector insect reveals new functions of hemipteran cuticular protein. Molecular & Cellular Proteomics, 14(8), 2229-2242.
Manière, G., Rondot, I., Bullesbach, E. E., Gautron, F., Vanhems, E., & Delbecque, J. P. (2004). Control of ovarian steroidogenesis by insulin-like peptides in the blowfly (Phormia regina). Journal of Endocrinology, 181(1), 147-156.
Nagasawa, H., Kataoka, H., Isogai, A., Tamura, S., Suzuki, A., Ishizaki, H., … & Suzuki, A. (1984). Amino-terminal amino acid sequence of the silkworm prothoracicotropic hormone: homology with insulin. Science, 226(4680), 1344-1345.
Nagasawa, H., Kataoka, H., Isogai, A., Tamura, S., Suzuki, A., Mizoguchi, A., ... & Ishizaki, H. (1986). Amino acid sequence of a prothoracicotropic hormone of the silkworm Bombyx mori. Proceedings of the National Academy of Sciences, 83(16), 5840-5843.
Ogawa, K. I., & TOJo, S. (1981). Quantitative changes of storage proteins and vitellogenin during the pupal-adult development in the silkworm, Bombyx mori (Lepidoptera: Bombycidae). Applied Entomology and Zoology, 16(3), 288-296.
Palli, S. R. (2016). Hormonal regulation of development and reproduction. Management of Insect Pests to Agriculture: Lessons Learned from Deciphering their Genome, Transcriptome and Proteome, 97-114.
Riehle, M. A., & Brown, M. R. (1999). Insulin stimulates ecdysteroid production through a conserved signaling cascade in the mosquito Aedes aegypti. Insect biochemistry and molecular biology, 29(10), 855-860.
Semaniuk, U., Piskovatska, V., Strilbytska, O., Strutynska, T., Burdyliuk, N., Vaiserman, A., ... & Lushchak, O. (2021). Drosophila insulin‐like peptides: from expression to functions–a review. Entomologia Experimentalis et Applicata, 169(2), 195-208.
Shi, X. F., Li, Y. N., Yi, Y. Z., Xiao, X. G., & Zhang, Z. F. (2015). Identification and characterization of 30 K protein genes found in Bombyx mori (Lepidoptera: Bombycidae) transcriptome. Journal of Insect Science, 15(1), 71.
Sun, Q., Zhao, P., Lin, Y., Hou, Y., XIA, Q. Y., & XIANG, Z. H. (2007). Analysis of the structure and expression of the 30K protein genes in silkworm, Bombyx mori. Insect Science, 14(1), 5-14.
Swevers L., Raikhel, A. S., Sappington, T. W., Shirk P., Iatrou K. (2005). Vitellogenesis and Post-Vitellogenic Maturation of the Insect Ovarian Follicle, Comprehensive Molecular Insect Science, Elsevier, 1(3), 87-155.
Thangaraj, P., Neelamegam, R., Nagaraj, K., & Muthukalingan, K. (2017). Lipophorin uptake into developing ovariole in Bombyx mori (Bombycidae: Lepidoptera). Journal of Insect Biotechnology and Sericology, 86(3), 3_059-3_065.
Tojo, S., Nagata, M., & Kobayashi, M. (1980). Storage proteins in the silkworm, Bombyx mori. Insect Biochemistry, 10(3), 289-303.
Tsuchida, K., Nagata, M., & Suzuki, A. (1987). Hormonal control of ovarian development in the silkworm, Bombyx mori. Archives of insect biochemistry and physiology, 5(3), 167-177.
Ujita, M., Katsuno, Y., Kawachi, I., Ueno, Y., Banno, Y., Fujii, H. And Hara, A. (2005). Glucan-binding activity of silkworm 30-kDa apolipoprotein and its involvement in defense against fungal infection. Bioscience Biotechnology and Biochemistry 69: 1178-1185.
Uranlı, R. (2008). İpekböceğinde (Bombyx mori) 5.larval Evrenin 0.gününden İtibaren Kontrol ve Jüvenil Hormon Analoğu Fenoxycarb Uygulanan Gruplarda Hemolenf Proteinlerinin SDS-PAGE ile Belirlenmesi (Tez no 224160). [Yüksek Lisans Tezi, Ege Üniversitesi Fen Bilimleri Enstitüsü Biyoloji Anabilim Dalı]. Yükseköğretim Kurulu Ulusal Tez Merkezi.
Winther-Sørensen, M., Galsgaard, K. D., Santos, A., Tramm ell, S. A., Sulek, K., Kuhre, R. E., ... & Albrechtsen, N. J. W. (2020). Glucagon acutely regulates hepatic amino acid catabolism and the effect may be disturbed by steatosis. Molecular metabolism, 42, 101080.
Wyatt, G. R., & Pan, M. L. (1978). Insect plasma proteins. Annual Review of Biochemistry, 47(1), 779-817. Yamauchi H. and Yoshitake N. (1984). Developmental stages of ovarian follicles of the silkworm, Bombyx mori L., Journal of Morphology 179: 21- 31.
Yan, J., Xue, Z., Dong, H., Pang, J., Liu, H., Gong, J., ... & Hou, Y. (2022). Nutrition regulates the expression of storage proteins in Bombyx mori via insulin-like/FoxO signaling pathway. Insect Biochemistry and Molecular Biology, 149, 103847.
Yang, C., Lin, Y., Shen, G., Chen, E., Wang, Y., Luo, J., ... & Xia, Q. (2014). Female qualities in males: Vitellogenin synthesis induced by ovary transplants into the male silkworm, Bombyx mori. Biochemical and Biophysical Research Communications, 453(1), 31-36.
Yang, H., Li, H., Song, Y., Sui, Y., Du, Z., & Zhang, G. (2021). Bombyxin II Regulates Glucose Absorption and Glycogen Synthesis through the PI3K Signaling Pathway in HepG2 Cells. BioMed Research International, 2021(1), 6639232.
Ye, L., Zhang, Y., Dong, Z., Guo, P., Zhao, D., Li, H., ... & Zhao, P. (2021). Five silkworm 30K proteins are involved in the cellular immunity against fungi. Insects, 12(2), 107.
Zhang, Q., Sun, W., Sun, B. Y., Xiao, Y., & Zhang, Z. (2017). The dynamic landscape of gene regulation during Bombyx mori oogenesis. BMC genomics, 18, 1-13.
Ziegler, R., & Van Antwerpen, R. (2006). Lipid uptake by insect oocytes. Insect biochemistry and molecular biology, 36(4), 264-272.

Ayrıntılar

Birincil Dil

İngilizce

Konular

Hayvan Fizyolojisi - Hücre

Bölüm

Araştırma Makalesi

Yazarlar

Tugce Ordu ^*
0000-0001-7578-3917
Türkiye

Kübra Yılmaz
0009-0005-1559-4715
Türkiye

Ebru Göncü
0000-0002-0191-4141
Türkiye

Erken Görünüm Tarihi

28 Temmuz 2025

Yayımlanma Tarihi

11 Eylül 2025

Gönderilme Tarihi

27 Ocak 2025

Kabul Tarihi

2 Haziran 2025

Yayımlandığı Sayı

Yıl 2025 Cilt: 28 Sayı: 5

DOI

https://doi.org/10.18016/ksutarimdoga.vi.1627726

IZ

https://izlik.org/JA56AE54DB

Kaynak Göster

RIS / Bibtex

APA

Ordu, T., Yılmaz, K., & Göncü, E. (2025). Effects of Vertebrate Insulin Hormone on Major Hemolymph Proteins and Ovarium Development in The Silkworm Bombyx mori Pupal Stage. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 28(5), 1357-1370. https://doi.org/10.18016/ksutarimdoga.vi.1627726

Effects of Vertebrate Insulin Hormone on Major Hemolymph Proteins and Ovarium Development in The Silkworm Bombyx mori Pupal Stage

Abstract

Keywords

İpek Böceği Bombyx mori Pupal Döneminde Omurgalı İnsülin Hormonunun Temel Hemolenf Proteinleri ve Ovaryum Gelişimi Üzerine Etkileri

Öz

Anahtar Kelimeler

Kaynakça

Ayrıntılar

Birincil Dil

Konular

Bölüm

Yazarlar

Erken Görünüm Tarihi

Yayımlanma Tarihi

Gönderilme Tarihi

Kabul Tarihi

Yayımlandığı Sayı

DOI

IZ

Kaynak Göster

e-ISSN: 2619-9149