Effects of Supplementation With Iron, Selenium and Magnesium on Galleria mellonella Cell-Mediated Immune Responses
Yıl 2021,
Cilt: 8 Sayı: 3, 605 - 614, 26.07.2021
Serhat Kaya
,
Bülent Gündüz
Öz
Immune responses play a key role in the survival of all living things. Intake of inorganic materials is of critical importance in living organisms because of their participation in metabolism and some component of cells. Iron (Fe), magnesium (Mg) and selenium (Se) were selected for this study because of their participation in critical constituents of cells, such as nucleic acids and enzymes in living organisms, and their indirect and direct effects on immunity. Although the separate effects of these inorganic materials are known, there is no study on their combined effects. Galleria mellonella, which is used as a model organism, is frequently used in evaluating of effects of human pathogens due to its various properties. Total hemocyte counts and encapsulation-melanization responses are the most commonly observed parameters when examining the immune responses of this model organism. In our study, the effects of the selected inorganic materials added in the ratio of 0.1%, 0.25%, 0.5% and 1% in the nutrient content of Galleria mellonella on the immune responses of this organism were investigated. As a result of the study, it was found that only 0.25% of the doses increased the hemocyte count and that the other doses significantly decreased compared to the control group. However, it was determined that 0.5% and 1% feeding caused a significant decrease in both hemocyte count and encapsulation-melanization responses. According to our findings, the nutrients which have over a certain dose by inorganic substances have negative effects on immunity.
Destekleyen Kurum
Çanakkale Onsekiz Mart Üniversitesi BAP birimi
Proje Numarası
FBA-2018-2521
Teşekkür
This work was supported by The Scientific Research Coordination Unit of Çanakkale Onsekiz Mart University, Turkey (Project number: FBA-2018-2521).
Kaynakça
- Altuntaş, H., Kılıç, A. Y., Uçkan, F. and Ergin, E. 2012. Effects of gibberellic acid on hemocytes of Galleria mellonella L. (Lepidoptera: Pyralidae). Environmental Entomology, 41(3): 688-696.
- Anastassopoulou J. and Theophanides T. 1995. The Role of Metal Ions in Biological Systems and Medicine. Pp 209-218. In: Kessissoglou D.P. (eds) Bioinorganic Chemistry. NATO ASI Series (Series C: Mathematical and Physical Sciences), vol 459. Springer, Dordrecht. pp415.
- Arthur, J. R., McKenzie, R. C. and Beckett, G. J. 2003. Selenium in the immune system. The Journal of Nutrition, 133(5): 1457-1459.
- Avery, J. C. and Hoffmann, P. R. 2018. Selenium, selenoproteins, and immunity. Nutrients, 10(9): 1203.
- Barbagallo, M., Belvedere, M. and Dominguez, L. J. 2009. Magnesium homeostasis and aging. Magnesium Research, 22(4): 235-246.
- Brandao, K., Deason-Towne, F., Perraud, A. L. and Schmitz, C. 2013. The role of Mg 2+ in immune cells. Immunologic Research, 55(1-3): 261-269.
- Cook S. M. and McArthur J. D. 2013. Developing Galleria mellonella as a model host for human pathogens. Virulence, 4: 350-353.
- Coskun, M., Kayis, T., Gulsu, E., and Alp, E. (2020). Effects of Selenium and Vitamin E on Enzymatic, Biochemical, and Immunological Biomarkers in Galleria mellonella L. Scientific Reports, 10(1), 1-7.
- Cutuli, M. A., Petronio Petronio, G., Vergalito, F., Magnifico, I., Pietrangelo, L., Venditti, N., and Di Marco, R. 2019. Galleria mellonella as a consolidated in vivo model hosts: New developments in antibacterial strategies and novel drug testing. Virulence, 10(1): 527-541.
- Dias, F. A., Gandara, A. C., Perdomo, H. D., Gonçalves, R. S., Oliveira, C. R., Oliveira, R. L., Citelli, M., Polycarpo, C. R., Santesmasses D., Mariotti, M., Guigó, R., Braz, G. R., Missirlis, F. and Oliveira, P. L 2016. Identification of a selenium-dependent glutathione peroxidase in the blood-sucking insect Rhodnius prolixus. Insect Biochemistry and Molecular Biology, 69: 105-114.
- Dixon, S. J., Lemberg, K. M., Lamprecht, M. R., Skouta, R., Zaitsev, E. M., Gleason, C. E., Patel, D. N., Bauer, A. j., Cantley, A. M., Yang, W. S., Morrison, B. and Stockwell, B. R. 2012. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell, 149(5), 1060-1072.
- Dubovskiy, I. M., Kryukova, N. A., Glupov, V. V. and Ratcliffe, N. A. 2016. Encapsulation and nodulation in insects. Invertebrate Survival Journal, 13(1), 229-246.
- Dunphy, G. B., Niven, D. F. and Chadwick, J. S. 2002. Iron contributes to the antibacterial functions of the haemolymph of Galleria mellonella. Journal of Insect Physiology, 48(9): 903-914.
- Eguchi D. and Iwabuchi K. 2006. A new cell line from the wax moth Galleria mellonella Linne (Lepidoptera: Pyralididae). In Vitro Cellular and Developmental Biology-Animal, 42: 1-3.
- Er, A. and Keskin, M. 2015. Influence of abscisic acid on the biology and hemocytes of the model insect Galleria mellonella (Lepidoptera: Pyralidae). Annals of the Entomological Society of America, 109(2): 244-251.
- Er, A., Uçkan, F., Rivers, D. B., Ergin, E. and Sak, O. 2010. Effects of parasitization and envenomation by the endoparasitic wasp Pimpla turionellae (Hymenoptera: Ichneumonidae) on hemocyte numbers, morphology, and viability of its host Galleria mellonella (Lepidoptera: Pyralidae). Annals of the Entomological Society of America, 103(2): 273-282.
- Feng, H., Guo, L., Gao, H. and Li, X. A. 2011. Deficiency of calcium and magnesium induces apoptosis via scavenger receptor BI. Life sciences, 88(13-14): 606–612.
- Golubkina, N., Sheshnitsan, S. and Kapitalchuk, M. 2014. Ecological importance of insects in selenium biogenic cycling. International Journal of Ecology, Article ID 835636
- Gwokyalya, R. and Altuntaş, H. 2019. Boric acid‐induced immunotoxicity and genotoxicity in model insect Galleria mellonella L. (Lepidoptera: Pyralidae). Archives of Insect Biochemistry and Physiology, e21588.
- Hillyer, J. F. 2016. Insect immunology and hematopoiesis. Developmental and Comparative Immunology, 58: 102-118.
- Hoffmann, P. R. and Berry, M. J. 2008. The influence of selenium on immune responses. Molecular Nutrition and Food Research, 52(11): 1273-1280.
- Huebers, H. A., Huebers, E., Finch, C. A., Webb, B. A., Truman, J. W., Riddiford, L. M., Martin, A.V. and Massover, W. H. 1988. Iron binding proteins and their roles in the tobacco hornworm, Manduca sexta (L.). Journal of Comparative Physiology B, 158(3): 291-300.
- Jiang, L., Peng, L. L., Cao, Y. Y., Thakur, K., Hu, F., Tang, S. M. and Wei, Z. J. 2020. Effect of Dietary Selenium Supplementation on Growth and Reproduction of Silkworm Bombyx mori L. Biological Trace Element Research, 193(1): 271-281.
- Kaya, S., Akkuş, G., Türkdoğan, S., and Gündüz, B. 2021a. Influence of Helichrysum arenarium on hemocyte-mediated immune responses and phenoloxidase enzyme activity of model organism Galleria mellonella (L.). International Journal of Tropical Insect Science, 1-8. Doi: 10.1007/s42690-021-00432-8
- Kaya, S., Uçkan, F. and Er, A. 2021b. Influence of Indole-3-Acetic Acid on Cellular Immune Responses of Galleria mellonella L.(Lepidoptera: Pyralidae) and Pimpla turionellae L. (Hymenoptera: Ichneumonidae) in a host-parasitoid system. International Journal of Tropical Insect Science, 41(1): 169-179.
- Krautz, R., Arefin, B. and Theopold, U. 2014. Damage signals in the insect immune response. Frontiers in Plant Science, 5: 342.
- Kurt, D. and Kayış, T. 2015. Effects of the pyrethroid insecticide deltamethrin on the hemocytes of Galleria mellonella. Turkish Journal of Zoology, 39(3): 452-457.
- Lavine M.D. and Strand M.R. 2002. Insect hemocytes and their role in immunity, Insect Biochemistry and Molecular Biology, 32: 1295–1309.
- Lee, M. J. and Anstee, J. H. 1995. Phenoloxidase and its zymogen from the haemolymph of larvae of the lepidopteran Spodoptera littoralis (Lepidoptera: Noctuidae). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 110(2): 379-384.
- Locke, M. and Nichol, H. 1992. Iron economy in insects: transport, metabolism, and storage. Annual Review of Entomology, 37(1): 195-215.
- Lynch, S. R. 2000. The effect of calcium on iron absorption. Nutrition Research Reviews, 13(2): 141-158.
- Martin-Romero, F. J., Kryukov, G. V., Lobanov, A. V., Carlson, B. A., Lee, B. J., Gladyshev, V. N. and Hatfield, D. L. 2001. Selenium metabolism in Drosophila: selenoproteins, selenoprotein mRNA expression, fertility, and mortality. Journal of Biological Chemistry, 276(32): 29798-29804.
- Mukherjee, K., Altincicek, B., Hain, T., Domann, E., Vilcinskas, A. and Chakraborty, T. 2010. Galleria mellonella as a Model System for Studying Listeria Pathogenesis. Applied and Environmental Microbiology, 76 (1): 310–317.
- Nappi, A. J. and Christensen, B. M. 2005. Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochemistry and Molecular Biology, 35(5): 443-459.
- Qiao, B., He, B., Cai, J., Lam, A. K. Y. and He, W. 2017. Induction of oxidative stress and cell apoptosis by selenium: the cure against oral carcinoma. Oncotarget, 8(69): 113614.
- Pech, L. L. and Strand, M. R. 1996. Granular cells are required for encapsulation of foreign targets by insect haemocytes. Journal of Cell Science, 109(8): 2053-2060.
- Piatek, M., Sheehan, G. and Kavanagh, K. 2020. Utilising Galleria mellonella larvae for studying in vivo activity of conventional and novel antimicrobial agents. Pathogens and Disease, 78(8): ftaa059.
- Popham, H. J., Shelby, K. S., and Popham, T. W. 2005. Effect of dietary selenium supplementation on resistance to baculovirus infection. Biological Control, 32(3): 419-426.
- Reeves, M. A., Bellinger, F. P. and Berry, M. J. 2010. The neuroprotective functions of selenoprotein M and its role in cytosolic calcium regulation. Antioxidants and Redox Signaling, 12(7): 809–818.
- Richards E. H. and Dani M. P. 2008. Biochemical isolation of an insect haemocyte anti-aggregation protein from the venom of the endoparasitic wasp, Pimpla hypochondriaca, and identification of its gene, Journal of Insect Physiology, 54: 1041-1049.
- Sak O., Uçkan F. and Ergin E. 2006. Effects of cypermethrin on total body weight, glycogen, protein, and lipid contents of Pimpla turionellae (L.) (Hymenoptera: Ichneumonidae), Belgian Journal of Zoology., 136: 53-58.
- Senior, N. J. and Titball, R. W. 2020. Isolation and primary culture of Galleria mellonella hemocytes for infection studies. F1000Research, 9: 1392.
- Sheehan, G., Garvey, A., Croke, M. and Kavanagh, K. 2018. Innate humoral immune defences in mammals and insects: The same, with differences?. Virulence, 9(1): 1625-1639.
- Shelby, K. S. and Popham, H. J. 2007. Increased plasma selenium levels correlate with elevated resistance of Heliothis virescens larvae against baculovirus infection. Journal of Invertebrate Pathology, 95(2): 77-83.
- Son, E. W., Lee, S. R., Choi, H. S., Koo, H. J., Huh, J. E., Kim, M. H. and Pyo, S. 2007. Effects of supplementation with higher levels of manganese and magnesium on immune function. Archives of Pharmacal Research, 30(6): 743-749.
- Sorvari, J., Hakkarainen, H. and Rantala, M. J. 2014. Immune defense of ants is associated with changes in habitat characteristics. Environmental Entomology, 37(1), 51-56.
- Tam, M., Gomez, S., Gonzalez-Gross, M. and Marcos, A. 2003. Possible roles of magnesium on the immune system. European Journal of Clinical Nutrition, 57(10): 1193.
- Tang, X. and Zhou, B. 2013. Iron homeostasis in insects: Insights from Drosophila studies. IUBMB Life, 65(10): 863-872.
- Tassetto, M., Kunitomi, M. and Andino R. 2017. Circulating immune cells mediate a systemic RNAi based adaptive antiviral response in Drosophila. Cell, 169 (2): 314–325.
- Trapani, V., Mastrototaro, L. and Wolf, F. I. 2011. Magnesium and the Yin-‐Yang interplay in apoptosis. pp. 85-98. In: Nechifor M. and Vink R (Eds). Magnesium in the Central Nervous System vol 85. University of Adelaide Press. xxx+ 356 pp.
- Toru, A. 1994. Superoxide generation in vitro in lepidopteran larval haemolymph. Journal of Insect Physiology, 40(2): 165-171.
- Yalçıntepe, L. and Halis, E. 2016. Modulation of iron metabolism by iron chelation regulates intracellular calcium and increases sensitivity to doxorubicin. Bosnian Journal of Basic Medical Sciences, 16(1): 14.
Demir, Selenyum ve Magnezyum ile Takviyenin Galleria mellonella Hücre Aracılı Bağışıklık Tepkileri Üzerindeki Etkileri
Yıl 2021,
Cilt: 8 Sayı: 3, 605 - 614, 26.07.2021
Serhat Kaya
,
Bülent Gündüz
Öz
Bağışıklık tepkileri, tüm canlıların hayatta kalmasında önemli bir rol oynar. İnorganik materyallerin bünyeye alımı; canlı organizmalarda metabolizmaya ve bazı hücrelerin bileşenlerine katılımları nedeniyle kritik öneme sahiptir. Bu çalışmada demir (Fe), magnezyum (Mg) ve selenyum (Se) canlı organizmalardaki nükleik asitler ve enzimler gibi hücrelerin kritik bileşenlerine katılımları ve bağışıklık üzerindeki dolaylı ve doğrudan etkileri nedeniyle seçilmiştir. Bu inorganik maddelerin ayrı ayrı etkileri bilinmesine rağmen, bunların birleşik etkileri üzerine bir çalışma bulunmamaktadır. Model organizma olarak kullanılan Galleria mellonella, çeşitli özelliklerinden dolayı insan patojenlerinin etkilerinin değerlendirilmesinde sıklıkla kullanılmaktadır. Toplam hemosit sayımları, kapsülleme-melanizasyon tepkileri, bu model organizmanın bağışıklık tepkilerini incelerken en sık gözlemlenen parametrelerdir. Çalışmamızda; Galleria mellonella'nın besin içeriğine% 0.1,% 0.25,% 0.5 ve% 1 oranında eklenen seçilmiş inorganik maddelerin bu organizmanın immün yanıtları üzerindeki etkileri araştırılmıştır. Çalışma sonucunda kontrol grubuna göre dozların sadece% 0.25'inin hemosit sayısını artırdığı, diğer dozların ise önemli ölçüde azaldığı tespit edildi. Bununla birlikte,% 0.5 ve% 1 beslemenin hem hemosit sayısında hem de kapsülleme-melanizasyon yanıtlarında önemli bir düşüşe neden olduğu belirlendi. Bu çalışmanın sonuçlarından biri, bu inorganik maddelerin besin içeriğinin% 2'sinin üzerine eklendiğinde gelişimini durdurması ve daha yüksek dozların larvaların ölümüne neden olmasıdır. Bulgularımıza göre inorganik maddeler tarafından belirli bir dozun üzerinde bulunan besinler bağışıklık üzerinde olumsuz etkilere sahiptir.
Proje Numarası
FBA-2018-2521
Kaynakça
- Altuntaş, H., Kılıç, A. Y., Uçkan, F. and Ergin, E. 2012. Effects of gibberellic acid on hemocytes of Galleria mellonella L. (Lepidoptera: Pyralidae). Environmental Entomology, 41(3): 688-696.
- Anastassopoulou J. and Theophanides T. 1995. The Role of Metal Ions in Biological Systems and Medicine. Pp 209-218. In: Kessissoglou D.P. (eds) Bioinorganic Chemistry. NATO ASI Series (Series C: Mathematical and Physical Sciences), vol 459. Springer, Dordrecht. pp415.
- Arthur, J. R., McKenzie, R. C. and Beckett, G. J. 2003. Selenium in the immune system. The Journal of Nutrition, 133(5): 1457-1459.
- Avery, J. C. and Hoffmann, P. R. 2018. Selenium, selenoproteins, and immunity. Nutrients, 10(9): 1203.
- Barbagallo, M., Belvedere, M. and Dominguez, L. J. 2009. Magnesium homeostasis and aging. Magnesium Research, 22(4): 235-246.
- Brandao, K., Deason-Towne, F., Perraud, A. L. and Schmitz, C. 2013. The role of Mg 2+ in immune cells. Immunologic Research, 55(1-3): 261-269.
- Cook S. M. and McArthur J. D. 2013. Developing Galleria mellonella as a model host for human pathogens. Virulence, 4: 350-353.
- Coskun, M., Kayis, T., Gulsu, E., and Alp, E. (2020). Effects of Selenium and Vitamin E on Enzymatic, Biochemical, and Immunological Biomarkers in Galleria mellonella L. Scientific Reports, 10(1), 1-7.
- Cutuli, M. A., Petronio Petronio, G., Vergalito, F., Magnifico, I., Pietrangelo, L., Venditti, N., and Di Marco, R. 2019. Galleria mellonella as a consolidated in vivo model hosts: New developments in antibacterial strategies and novel drug testing. Virulence, 10(1): 527-541.
- Dias, F. A., Gandara, A. C., Perdomo, H. D., Gonçalves, R. S., Oliveira, C. R., Oliveira, R. L., Citelli, M., Polycarpo, C. R., Santesmasses D., Mariotti, M., Guigó, R., Braz, G. R., Missirlis, F. and Oliveira, P. L 2016. Identification of a selenium-dependent glutathione peroxidase in the blood-sucking insect Rhodnius prolixus. Insect Biochemistry and Molecular Biology, 69: 105-114.
- Dixon, S. J., Lemberg, K. M., Lamprecht, M. R., Skouta, R., Zaitsev, E. M., Gleason, C. E., Patel, D. N., Bauer, A. j., Cantley, A. M., Yang, W. S., Morrison, B. and Stockwell, B. R. 2012. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell, 149(5), 1060-1072.
- Dubovskiy, I. M., Kryukova, N. A., Glupov, V. V. and Ratcliffe, N. A. 2016. Encapsulation and nodulation in insects. Invertebrate Survival Journal, 13(1), 229-246.
- Dunphy, G. B., Niven, D. F. and Chadwick, J. S. 2002. Iron contributes to the antibacterial functions of the haemolymph of Galleria mellonella. Journal of Insect Physiology, 48(9): 903-914.
- Eguchi D. and Iwabuchi K. 2006. A new cell line from the wax moth Galleria mellonella Linne (Lepidoptera: Pyralididae). In Vitro Cellular and Developmental Biology-Animal, 42: 1-3.
- Er, A. and Keskin, M. 2015. Influence of abscisic acid on the biology and hemocytes of the model insect Galleria mellonella (Lepidoptera: Pyralidae). Annals of the Entomological Society of America, 109(2): 244-251.
- Er, A., Uçkan, F., Rivers, D. B., Ergin, E. and Sak, O. 2010. Effects of parasitization and envenomation by the endoparasitic wasp Pimpla turionellae (Hymenoptera: Ichneumonidae) on hemocyte numbers, morphology, and viability of its host Galleria mellonella (Lepidoptera: Pyralidae). Annals of the Entomological Society of America, 103(2): 273-282.
- Feng, H., Guo, L., Gao, H. and Li, X. A. 2011. Deficiency of calcium and magnesium induces apoptosis via scavenger receptor BI. Life sciences, 88(13-14): 606–612.
- Golubkina, N., Sheshnitsan, S. and Kapitalchuk, M. 2014. Ecological importance of insects in selenium biogenic cycling. International Journal of Ecology, Article ID 835636
- Gwokyalya, R. and Altuntaş, H. 2019. Boric acid‐induced immunotoxicity and genotoxicity in model insect Galleria mellonella L. (Lepidoptera: Pyralidae). Archives of Insect Biochemistry and Physiology, e21588.
- Hillyer, J. F. 2016. Insect immunology and hematopoiesis. Developmental and Comparative Immunology, 58: 102-118.
- Hoffmann, P. R. and Berry, M. J. 2008. The influence of selenium on immune responses. Molecular Nutrition and Food Research, 52(11): 1273-1280.
- Huebers, H. A., Huebers, E., Finch, C. A., Webb, B. A., Truman, J. W., Riddiford, L. M., Martin, A.V. and Massover, W. H. 1988. Iron binding proteins and their roles in the tobacco hornworm, Manduca sexta (L.). Journal of Comparative Physiology B, 158(3): 291-300.
- Jiang, L., Peng, L. L., Cao, Y. Y., Thakur, K., Hu, F., Tang, S. M. and Wei, Z. J. 2020. Effect of Dietary Selenium Supplementation on Growth and Reproduction of Silkworm Bombyx mori L. Biological Trace Element Research, 193(1): 271-281.
- Kaya, S., Akkuş, G., Türkdoğan, S., and Gündüz, B. 2021a. Influence of Helichrysum arenarium on hemocyte-mediated immune responses and phenoloxidase enzyme activity of model organism Galleria mellonella (L.). International Journal of Tropical Insect Science, 1-8. Doi: 10.1007/s42690-021-00432-8
- Kaya, S., Uçkan, F. and Er, A. 2021b. Influence of Indole-3-Acetic Acid on Cellular Immune Responses of Galleria mellonella L.(Lepidoptera: Pyralidae) and Pimpla turionellae L. (Hymenoptera: Ichneumonidae) in a host-parasitoid system. International Journal of Tropical Insect Science, 41(1): 169-179.
- Krautz, R., Arefin, B. and Theopold, U. 2014. Damage signals in the insect immune response. Frontiers in Plant Science, 5: 342.
- Kurt, D. and Kayış, T. 2015. Effects of the pyrethroid insecticide deltamethrin on the hemocytes of Galleria mellonella. Turkish Journal of Zoology, 39(3): 452-457.
- Lavine M.D. and Strand M.R. 2002. Insect hemocytes and their role in immunity, Insect Biochemistry and Molecular Biology, 32: 1295–1309.
- Lee, M. J. and Anstee, J. H. 1995. Phenoloxidase and its zymogen from the haemolymph of larvae of the lepidopteran Spodoptera littoralis (Lepidoptera: Noctuidae). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 110(2): 379-384.
- Locke, M. and Nichol, H. 1992. Iron economy in insects: transport, metabolism, and storage. Annual Review of Entomology, 37(1): 195-215.
- Lynch, S. R. 2000. The effect of calcium on iron absorption. Nutrition Research Reviews, 13(2): 141-158.
- Martin-Romero, F. J., Kryukov, G. V., Lobanov, A. V., Carlson, B. A., Lee, B. J., Gladyshev, V. N. and Hatfield, D. L. 2001. Selenium metabolism in Drosophila: selenoproteins, selenoprotein mRNA expression, fertility, and mortality. Journal of Biological Chemistry, 276(32): 29798-29804.
- Mukherjee, K., Altincicek, B., Hain, T., Domann, E., Vilcinskas, A. and Chakraborty, T. 2010. Galleria mellonella as a Model System for Studying Listeria Pathogenesis. Applied and Environmental Microbiology, 76 (1): 310–317.
- Nappi, A. J. and Christensen, B. M. 2005. Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochemistry and Molecular Biology, 35(5): 443-459.
- Qiao, B., He, B., Cai, J., Lam, A. K. Y. and He, W. 2017. Induction of oxidative stress and cell apoptosis by selenium: the cure against oral carcinoma. Oncotarget, 8(69): 113614.
- Pech, L. L. and Strand, M. R. 1996. Granular cells are required for encapsulation of foreign targets by insect haemocytes. Journal of Cell Science, 109(8): 2053-2060.
- Piatek, M., Sheehan, G. and Kavanagh, K. 2020. Utilising Galleria mellonella larvae for studying in vivo activity of conventional and novel antimicrobial agents. Pathogens and Disease, 78(8): ftaa059.
- Popham, H. J., Shelby, K. S., and Popham, T. W. 2005. Effect of dietary selenium supplementation on resistance to baculovirus infection. Biological Control, 32(3): 419-426.
- Reeves, M. A., Bellinger, F. P. and Berry, M. J. 2010. The neuroprotective functions of selenoprotein M and its role in cytosolic calcium regulation. Antioxidants and Redox Signaling, 12(7): 809–818.
- Richards E. H. and Dani M. P. 2008. Biochemical isolation of an insect haemocyte anti-aggregation protein from the venom of the endoparasitic wasp, Pimpla hypochondriaca, and identification of its gene, Journal of Insect Physiology, 54: 1041-1049.
- Sak O., Uçkan F. and Ergin E. 2006. Effects of cypermethrin on total body weight, glycogen, protein, and lipid contents of Pimpla turionellae (L.) (Hymenoptera: Ichneumonidae), Belgian Journal of Zoology., 136: 53-58.
- Senior, N. J. and Titball, R. W. 2020. Isolation and primary culture of Galleria mellonella hemocytes for infection studies. F1000Research, 9: 1392.
- Sheehan, G., Garvey, A., Croke, M. and Kavanagh, K. 2018. Innate humoral immune defences in mammals and insects: The same, with differences?. Virulence, 9(1): 1625-1639.
- Shelby, K. S. and Popham, H. J. 2007. Increased plasma selenium levels correlate with elevated resistance of Heliothis virescens larvae against baculovirus infection. Journal of Invertebrate Pathology, 95(2): 77-83.
- Son, E. W., Lee, S. R., Choi, H. S., Koo, H. J., Huh, J. E., Kim, M. H. and Pyo, S. 2007. Effects of supplementation with higher levels of manganese and magnesium on immune function. Archives of Pharmacal Research, 30(6): 743-749.
- Sorvari, J., Hakkarainen, H. and Rantala, M. J. 2014. Immune defense of ants is associated with changes in habitat characteristics. Environmental Entomology, 37(1), 51-56.
- Tam, M., Gomez, S., Gonzalez-Gross, M. and Marcos, A. 2003. Possible roles of magnesium on the immune system. European Journal of Clinical Nutrition, 57(10): 1193.
- Tang, X. and Zhou, B. 2013. Iron homeostasis in insects: Insights from Drosophila studies. IUBMB Life, 65(10): 863-872.
- Tassetto, M., Kunitomi, M. and Andino R. 2017. Circulating immune cells mediate a systemic RNAi based adaptive antiviral response in Drosophila. Cell, 169 (2): 314–325.
- Trapani, V., Mastrototaro, L. and Wolf, F. I. 2011. Magnesium and the Yin-‐Yang interplay in apoptosis. pp. 85-98. In: Nechifor M. and Vink R (Eds). Magnesium in the Central Nervous System vol 85. University of Adelaide Press. xxx+ 356 pp.
- Toru, A. 1994. Superoxide generation in vitro in lepidopteran larval haemolymph. Journal of Insect Physiology, 40(2): 165-171.
- Yalçıntepe, L. and Halis, E. 2016. Modulation of iron metabolism by iron chelation regulates intracellular calcium and increases sensitivity to doxorubicin. Bosnian Journal of Basic Medical Sciences, 16(1): 14.