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New activity of yamamarin, an insect pentapeptide, on immune system of mealworm, Tenebrio molitor

Published online by Cambridge University Press:  12 September 2017

K. Walkowiak-Nowicka ,
G. Nowicki ,
M. Kuczer  and
G. Rosiński
K. Walkowiak-Nowicka*
Affiliation:
Department of Animal Physiology and Development, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznań, Poland
G. Nowicki
Affiliation:
Department of Molecular Virology, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznań, Poland
M. Kuczer
Affiliation:
Faculty of Chemistry, University of Wroclaw, Joliot-Curie 14, 50-383 Wrocław, Poland
G. Rosiński
Affiliation:
Department of Animal Physiology and Development, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznań, Poland
*
*Author for correspondence Tel: +48 (61) 829 59 26 Fax: +48 (61) 829 55 90 E-mail: [email protected]
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Abstract

In insects, two types of the immune responses, cellular and humoral, constitute a defensive barrier against various parasites and pathogens. In response to pathogens, insects produce a wide range of immune agents that act on pathogens directly, such as cecropins or lysozyme, or indirectly by the stimulation of hemocyte migration or by increasing phenoloxidase (PO) activity. Recently, many new immunologically active substances from insects, such as peptides and polypeptides, have been identified. Nevertheless, in the most cases, their physiological functions are not fully known. One such substance is yamamarin – a pentapeptide isolated from the silk moth Antheraea yamamai. This yamamarin possesses strong antiproliferative properties and is probably involved in diapause regulation. Here, we examined the immunotropic activity of yamamarin by testing its impact on selected functions of the immune system in heterologous bioassays with the beetle Tenebrio molitor, commonly known as a stored grains pest. Our results indicate that the pentapeptide affects the activity of immune processes in the beetle. We show that yamamarin induces changes in both humoral and cellular responses. The yamamarin increases the activity of PO, as well as causes changes in the hemocyte cytoskeleton and stimulates phagocytic activity. We detected an increased number of apoptotic hemocytes, however after the yamamarin injection, no significant variations in the antibacterial activity in the hemolymph were observed. The obtained data suggest that yamamarin could be an important controller of the immune system in T. molitor.

Keywords

Immunologyany-GSbeetlepest
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 3 , June 2018 , pp. 351 - 359
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Copyright
Copyright © Cambridge University Press 2017 

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References

Boman, H.G. & Hultmark, D. (1987) Cell-free immunity in insects. Annual Review of Microbiology 41, 103–126.CrossRefGoogle ScholarPubMed
Borovsky, D., Rabindran, S., Dawson, W.O., Powell, C.A., Iannotti, D.A., Morris, T.J., Shabanowitz, J., Hunt, D.F., DeBondt, H.L. & DeLoof, A. (2006) Expression of Aedes trypsin-modulating oostatic factor on the virion of TMV: a potential larvicide. Proceedings of the National Academy of Sciences of the United States of America 103(50), 18963–18968.CrossRefGoogle ScholarPubMed
Chan, W.C. & White, P.J. (2000) Fmoc Solid Phase Peptide Synthesis: Practical Approach. New York, Oxford University Press Inc.Google Scholar
Charles, H.M. & Killian, K.A. (2015) Response of the insect immune system to three different immune challenges. Journal of Insect Physiology 81, 97–108.CrossRefGoogle ScholarPubMed
Chernysh, S., Irina, K. & Irina, A. (2012) Anti-tumor activity of immunomodulatory peptide alloferon-1 in mouse tumor transplantation model. International Immunopharmacology 12(1), 312–314.CrossRefGoogle ScholarPubMed
Chowański, S., Kudlewska, M., Marciniak, P. & Rosiński, G. (2014) Synthetic insecticides – is there an alternative? Polish Journal of Environmental Studies 23(2), 291–302.Google Scholar
Chowański, S., Adamski, Z., Lubawy, J., Marciniak, P., Pacholska-Bogalska, J., Słocińska, M., Spochacz, M., Szymczak, M., Urbański, A., Walkowiak-Nowicka, K. & Rosiński, G. (2017) Insect peptides – perspectives in human diseases treatment. Current Medicinal Chemistry 24, 3116–3152.CrossRefGoogle ScholarPubMed
Czarniewska, E., Mrówczynska, L., Kuczer, M. & Rosiński, G. (2012) The pro-apoptotic action of the peptide hormone Neb-colloostatin on insect haemocytes. Journal of Experimental Biology 215(24), 4308–4313.Google ScholarPubMed
Goldsworthy, G., Mullen, L., Opoku-Ware, K. & Chandrakant, S. (2003) Interactions between the endocrine and immune systems in locusts. Physiological Entomology 28(1), 54–61.CrossRefGoogle Scholar
Gonzalez-Santoyo, I. & Cordoba-Aguilar, A. (2012) Phenoloxidase: a key component of the insect immune system. Entomologia Experimentalis et Applicata 142, 1–16.CrossRefGoogle Scholar
Jupatanakul, N., Sim, S., Angleró-Rodríguez, Y.I., Souza-Neto, J., Dasm, S., Potim, K.E., Rossi, S.L., Bergren, N., Vasilakis, N. & Dimopoulos, G. (2017) Engineered Aedes aegypti JAK/STAT pathway-mediated immunity to Dengue virus. PLoS Neglected Tropical Diseases 11(1), e0005187.CrossRefGoogle ScholarPubMed
Kamiya, M.O., Sato, K., Yokoyama, Y., Wang, T., Aizawa, M., Kumaki, T., Mizuguchi, Y., Imai, M., Demura, K., Suzuki, M. & Kawano, K. (2010) Structure-activity relationship of a novel pentapeptide with cancer cell growth-inhibitory activity. Journal of Peptide Science 16(5), 242–248.CrossRefGoogle ScholarPubMed
Kuczer, M., Dziubasik, K., Midak-Siewirska, A., Zahorska, R., Luczak, M. & Konopinska, D. (2010) Studies of insect peptides alloferon, any-GS and their analogues. Synthesis and antiherpes activity. Journal of Peptide Science 16(4), 186–189.CrossRefGoogle ScholarPubMed
Lauwers, A., Twyffels, L., Soin, R., Wauquier, C., Kruys, V. & Gueydan, C. (2009) Post-transcriptional regulation of genes encoding anti-microbial peptides in Drosophila. The Journal of Biological Chemistry 284(13), 8973–8983.CrossRefGoogle ScholarPubMed
Ludwig, D. & Fiore, C. (1960) Further studies on the relationship between parental age and life cycle of the mealworm. Annals of the Entomological Society of America 53, 595–600.CrossRefGoogle Scholar
Mahy, B.W.J. (2004) Vector-Borne Diseases. Cambridge, UK, Cambridge University Press.Google Scholar
Mai, S., Mauger, M.T., Niu, L.N., Barnes, J.B., Kao, S., Bergeron, B.E., Ling, J.Q. & Tay, F.R. (2017) Potential applications of antimicrobial peptides and their mimics in combating caries and pulpal infections. Acta Biomaterialia 49, 16–35.CrossRefGoogle ScholarPubMed
Marmaras, V.J., Charalambidis, N.D. & Zervas, C.G. (1996) Immune response in insects: the role of phenoloxidase in defense reactions in relation to melanization and sclerotization. Archives of Insect Biochemistry and Physiology 31(2), 119–133.3.0.CO;2-V>CrossRefGoogle ScholarPubMed
Mavrouli, M.D., Tsakas, S., Theodorou, G.L., Lampropoulou, M. & Marmaras, V.J. (2005) MAP kinases mediate phagocytosis and melanization via prophenoloxidase activation in medfly hemocytes. Biochemica et Biophysica Acta 1744(2), 145–156.CrossRefGoogle ScholarPubMed
Muturi, E.J., Blackshear, M. Jr. & Montgomery, A. (2012) Temperature and density-dependent effects of larval environment on Aedes aegypti competence for an alphavirus. Journal of Vector Ecology 37(1), 154–161.CrossRefGoogle ScholarPubMed
Pennacchio, F.S. & Strand, M.R. (2006) Evolution of developmental strategies in parasitic hymenoptera. Annual Review of Entomology 51, 233–258.CrossRefGoogle ScholarPubMed
Rolff, J. & Siva-Jothy, M.T. (2004) Selection on insect immunity in the wild. Proceedings of the Royal Society B: Biological Sciences 271(1553), 2157–2160.CrossRefGoogle ScholarPubMed
Rosiński, G. (1995) Metabolic and Myotropic Neuropeptides of Insects. Zoological Series 22. Poznań, Adam Mickiewicz University Press, p. 148.Google Scholar
Rosiński, G., Wrzeszcz, A. & Obuchowicz, L. (1979) Differences in trehalase activity in the intestine of fed and starved larvae of Tenebrio molitor L. Insect Biochemistry 9(5), 485–488.CrossRefGoogle Scholar
Sato, Y., Yang, P., An, Y., Matsukawa, K., Ito, K., Imanishi, S., Matsuda, H., Uchiyama, Y., Imai, K., Ito, S., Ishida, Y. & Suzuki, K. (2010) A palmitoyl conjugate of insect pentapeptide Yamamarin arrests cell proliferation and respiration. Peptides 31(5), 827–833.CrossRefGoogle ScholarPubMed
Satyavathi, V.V., Minz, A. & Nagaraju, J. (2014) Nodulation: an unexplored cellular defense mechanism in insects. Cellular Signalling 26(8), 1753–1763.CrossRefGoogle ScholarPubMed
Siva-Jothy, M.T., Moret, Y. & Rolff, J. (2005) Insect immunity: an evolutionary ecology perspective. Advances in Insect Physiology 32, 1–48.CrossRefGoogle Scholar
Sorrentino, R.P., Small, C.N. & Govind, S. (2002) Quantitative analysis of phenol oxidase activity in insect hemolymph. BioTechniques 32(4), 815–816, 818, 820, 822–813.CrossRefGoogle ScholarPubMed
Strand, M.R. (2008) The insect immune response. Insect Science 15, 1–14.CrossRefGoogle Scholar
Szymanowska-Dziubasik, K., Marciniak, P., Rosinski, G. & Konopinska, D. (2008) Synthesis, cardiostimulatory, and cardioinhibitory effects of selected insect peptides on Tenebrio molitor. Journal of Peptide Science 14(6), 708–713.CrossRefGoogle ScholarPubMed
Tonk, M., Vilcinskas, A. & Rahnamaeian, M. (2016) Insect antimicrobial peptides: potential tools for the prevention of skin cancer. Applied Microbiology and Biotechnology 100(17), 7397–7405.CrossRefGoogle ScholarPubMed
Tsakas, S. & Marmaras, V.J. (2010) Insect immunity and its signalling: an overview. Invertebrate Survival Journal 7, 228–238.Google Scholar
Urbański, A., Czarniewska, E., Baraniak, E. & Rosinski, G. (2014) Developmental changes in cellular and humoral responses of the burying beetle Nicrophorus vespilloides (Coleoptera, Silphidae). Journal of Insect Physiology 60, 98–103.CrossRefGoogle ScholarPubMed
Vaidyanathan, R. & Scott, T.W. (2006) Apoptosis in mosquito midgut epithelia associated with West Nile virus infection. Apoptosis 11(9), 1643–1651.CrossRefGoogle ScholarPubMed
Vega, F.E., Kaya, H.K. & Tanada, Y. (2012) Insect Pathology. Amsterdam, Boston, Elsevier/Academic Press.Google Scholar
Yang, P., Abe, S., Zhao, Y., An, Y. & Suzuki, K. (2004) Growth suppression of rat hepatoma cells by a pentapeptide from Antheraea yamamai. Journal of Insect Biotechnology and Sericology 73(1), 7–13.Google Scholar
Yang, P., Abe, S., Sato, Y., Yamashita, T., Matsuda, F., Hamayasu, T., Imai, K. & Suzuki, K. (2007) A palmitoyl conjugate of an insect pentapeptide causes growth arrest in mammalian cells and mimics the action of diapause hormone. Journal of Insect Biotechnology and Sericology 76, 63–69.Google Scholar