Histochemical and ultrastructural analysis of macromolecules in trophocytes of the Oriental cockroach, Blatta orientalis (L., 1758) (Blattodea: Blattidae)

Year 2023, Volume: 47 Issue: 1, 87 - 100, 25.04.2023

Tuğba Zülfikaroğlu , Gamze Turgay İzzetoğlu , Mehmet Salih Yıkılmaz , Savaş İzzetoğlu

https://doi.org/10.16970/entoted.1118639

Abstract

The fat body is a major storage area for glycogen, lipid and protein. The trophocyte is the main cell of fat body and stores these macromolecules. The fat body consists of two parts; peripheral and perivisceral. Peripheral fat body is located below the integument while perivisceral fat body is around the digestive tract. The study was conducted in EGEMIKAL Analysis Laboratory and Histology Laboratory of Ege University between 2018 and 2020. The fat body contents of insects at all stages were examined comparatively in three selected sections through histochemical and ultrastructural studies. We identified macromolecules stored in the trophocytes. Both the granular form of proteins and asterisk structure of glycogen localized around the lipid droplets were observed clearly. It was found that accumulation of protein continued in the trophocytes, but glycogen accumulation decreased considerably in adults compared to all nymphal stages. We also found that larger lipid droplets were stored in the PF fat body, while glycogen and protein accumulation was much higher in the PV fat body. These results may contribute to understanding of the mechanisms underlying activities such as amino acid, nitrogen, lipid and carbohydrate metabolism and protein synthesis in insects.

Keywords

Blatta orientalis, fat body, histochemistry, TEM, trophocyte

Supporting Institution

Ege University Scientific Research Fund

Project Number

FYL-2018-20133

Thanks

This work was supported by the Ege University Scientific Research Fund (FYL-2018-20133). Also, we are sincerely grateful to PhD Student Dirim Şendoğan for proofreading and Dr. Agâh Kozan for helping the statistical analyses.

Doğu hamam böceği Blatta orientalis (L., 1758) (Blattodea: Blattidae)’in trofositlerindeki makromoleküllerin histokimyasal ve ince yapı analizi

Abstract

Böcek yağ dokusu glikojen, lipid ve protein için başlıca depolama alanıdır. Trofosit yağ dokusunun temel hücresidir ve bu makro molekülleri depolamaktadır. Yağ dokusu integümentin hemen altında yer alan periferal ve sindirim kanalının etrafında yer alan perivisseral yağ dokusu olmak üzere iki kısımdan oluşmaktadır. Bu çalışma 2018-2020 yılları arasında Ege Üniversitesi EGEMİKAL Analiz Laboratuvarı ve Histoloji Laboratuvarı’nda yürütülmüştür. Böceklerin tüm dönemlerine ait seçilen üç bölgesindeki yağ dokusu karşılaştırmalı olarak histokimyasal ve ince yapı çalışmalarıyla incelenmiştir. Trofositlerde depolanan makromoleküller belirlenmiştir. Hem granüler protein hem de lipid damlalarının etrafında yerleşim gösteren yıldız şeklindeki glikojen yapıları net bir şekilde gözlenmiştir. Tüm nimfal evrelerle erginler karşılaştırıldığında trofositlerde protein birikiminin devam ettiği, ancak glikojen birikiminin önemli ölçüde azaldığı belirlenmiştir. Ayrıca, periferal yağ dokusunda daha iri lipid damlaları depo edilirken, perivisseral yağ dokusunda ise daha fazla glikojen ve protein birikiminin olduğu tespit edilmiştir. Bu bulgular, böceklerde amino asit, nitrojen, lipid ve karbonhidrat metabolizmaları ve protein sentezi gibi faaliyetlerin altında yatan mekanizmaların anlaşılmasına katkı sağlayabilecektir.

Keywords

Blatta orientalis, böcek yağ dokusu, histokimya, TEM, trofosit

Project Number

FYL-2018-20133

References

• Arrese, E. L. & J. L. Soulages, 2010. Insect fat body: Energy, metabolism, and regulation. Annual Review Entomology, 55 (1): 207-225.
• Assis, W. A., J. Malta, P. F. P. Pimenta, J. M. Ramalho-Ortigao & G. F. Martins, 2014. The characterization of the fat bodies and oenocytes in the adult females of the sand fly vectors (Lutzomyia longipalpis and Phlebotomus papatasi). Arthropod Structure & Development, 43 (5): 501-509.
• Azeez, O., R. Meintjes & J. Chamunorwa, 2014. Fat body, fat pad and adipose tissues in invertebrates and vertebrates: The nexus. Lipids in Health and Disease, 13 (1): 71-84.
• Bassirpour, G. & E. Zoratti, 2014. Cockroach allergy and allergen-specific immunotherapy in Asthma. Current Opinion in Allergy and Clinical Immunology, 14 (6): 535-541.
• Carvalho, R. B. R., F. G. Andrade, S. H. Levy, F. Moscardi & A. M. F. Falleiros, 2013. Histology and ultrastructure of the fat body of Anticarsia gemmatalis (Hübner, 1818) (Lepidoptera: Noctuidae). Brazilian Archives of Biology and Technology, 56 (2): 303-310.
• Chowanski, S., J. Lubawy, E. Paluch-Lubawa, M. Spochacz, G. Rosinski & M. Slocinska, 2017. The physiological role of fat body and muscle tissues in response to cold stress in the tropical cockroach Gromphadorhina coquereliana. Plos One, 12 (3): e0173100.
• Cornwell, P. B., 1968. The Cockroach. Vol. 1, Hutchinson, London, 391 pp.
• Corsaro, D., V. Thomas, G. Goy, D. Venditti, R. Radek & G. Greub, 2007. 'Candidatus Rhabdochlamydia crassificans', an intracellular bacterial pathogen of the cockroach Blatta orientalis (Insecta: Blattodea). Systematic and Applied Microbiology, 30 (3): 221-228.
• Dean, R. L., M. Locke & J. V. Collins, 1985. “Structure of Fat Body, 155-210”. In: Comprehensive Insect Physiology, Vol 3. Biochemistry and Pharmacology, (Eds. G. A. Kerkut & L. A. Gilbert), Oxford, UK, 625 pp.
• Dehkordi, A. S., Y. Salim Abadi, H. Nasirian, T. Hazratian, M. A. Gorouhi, S. Yousefi, & A. Paksa. 2017. Synergists action of piperonyl butoxide and S,S,S-tributyl phosphorotrithioate on toxicity of carbamate insecticides against Blattella germanica. Asian Pacific Journal of Tropical Medicine, 10 (1): 981-986.
• Furtado, W. C. A., D. O. Azevedo, G. F. Martins, J. C. Zanuncio & J. E. Serrao, 2013. Histochemistry and ultrastructure of urocytes in the pupae of the stingless bee Melipona quadrifasciata (Hymenoptera: Meliponini). Microscopy and Microanalysis, 19 (6): 1502-1510.
• Grdiša, M. & K. Gršić, 2013. Botanical insecticides in plant protection. Agriculturae Conspectus Scientificus, 78 (2): 85-93.
• Gullan, P. J. & P. S. Cransto, 2014. The Insects: An Outline of Entomology. John Wiley & Sons. Ltd, UK, 624 pp.
• Haunerland, N. H. & P. D. Shirk, 1995. Regional and functional differentiation in the insect fact body. Annual Review Entomology, 40 (1): 121-145.
• Hoshizaki, D. K., 2005. “Fat-Cell Development, 315-345”. In: Comprehensive Molecular Insect Science. Vol. 2 (Eds. L. I. Gilbert, K. Iatrou & S. Gill) Elsevier B, Oxford, England, 384 pp.
• Humason, G. L., 1962. Animal Tissue Techniques. W. H. Freeman and Company, USA, 468 pp.
• Karnovsky, M. J., 1965. A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. The Journal of Cell Biology, 27 (2): 137A-138A.
• Klowden, M. J., 2007. Physiological Systems in Insects. Elsevier, Second Edition, Moscow, Idaho, 661 pp.
• Li, S., X. Yu & Q. Feng, 2019. Fat body biology in the last decade. Annual Review of Entomology, 64 (1): 315-333.
• Lipovsek, S. & T. Novak, 2016. Autophagy in the fat body cells of the cave cricket Troglophilus neglectus Krauss, 1878 (Rhaphidophoridae, Saltatoria) during overwintering. Protoplasma, 253 (2): 457-466.
• Lipovsek, S., T. Novak, F. Janžekovič & M. A. Pabst, 2011. Role of the fat body in the cave crickets Troglophilus cavicola and Troglophilus neglectus (Rhaphidophoridae, Saltatoria) during overwintering. Arthropod Structure & Development, 40 (1): 54-63.
• Liu, Y., H. Liu, S. Liu, S. Wang, R. J. Jiang & S. Li, 2009. Hormonal and nutritional regulation of insect fat body development and function. Archives of Insect Biochemistry and Physiology, 71 (1): 16-30.
• Locke, M., 1984. “The Structure and Development of The Vacuolar System in The Fat Body of Insects, 151-197”. In: Insect Ultrastructure: Vol. 2, (Eds. R. C. King & H. Akai). Plenum Press., New York, 650 pp.
• Makki, R., E. Cinnamon & P. Gould, 2014. The development and functions of oenocytes. Annual Review of Entomology, 59 (1): 405-425.
• Martins, G. F. & J. M. Ramalho-Ortigao, 2012. Oenocytes in insects. Invertebrate Survival Journal, 9 (2): 139-152.
• Millonig, G., 1961. Advantages of a phosphate buffer for OsO4 solution in fixation. Journal of Applied Physiology, 32 (2): 1637-1639.
• Nasirian, H. & A. Salehzadeh, 2019. Control of cockroaches (Blattaria) in sewers: A practical approach systematic review. Journal of Medical Entomology, 56 (1): 181-191.
• Paes-de-Oliveira, V. T. & C. Cruz-Landim, 2003. Morphology and function of insect fat body cells. Biociencias, 11 (2): 195-205.
• Park, M. S., P. Park & M. Takeda, 2013. Roles of fat body trophocytes, mycetocytes and urocytes in the American cockroach, Periplaneta americana under starvation conditions: An ultrastructural study. Arthropod Structure & Development, 42 (4): 287-295.
• Patino-Navarrete, R., M. D. Piulachs, X. Belles, A. Moya, A. Latorre & J. Pereto, 2014. The cockroach Blattella germanica obtains nitrogen from uric acid through a metabolic pathway shared with its bacterial endosymbiont. Biology Letters, 10 (7): 20140407.
• Pavela, R., 2007. Possibilities of botanical insecticide exploitation in plant protection. Pest Technology, 1 (1): 47-52. Presnell, J. K. & M. P. Schreibman, 1997. Humason’s Animal Tissue Techniques. The Johns Hopkins University Press Ltd, London, 572 pp.
• Resh, V. H. & R. T. Carde, 2003. Encyclopedia of Insect. Elsevier Science, USA, 1266 pp.
• Roma, G. C., O. C. Bueno & M. I. Camargo-Mathias, 2010. Morpho-physiological analysis of the insect fat body: A review. Micron, 41 (5): 395-401.
• Sobotnik, J., F. Weyda, R. Hanus, J. Cvačka & J. Nebesářová, 2006. Fat body of Prorhinotermes simplex (Isoptera: Rhinotermitidae): Ultrastructure, inter-caste differences and lipid composition. Micron, 37 (7): 648-656.
• Sohn, M. H. & K. E. Kim, 2012. The Cockroach and Allergic Diseases. Allergy, Asthma & Immunolology Research, 4 (5): 264-269.
• Stankus, R. P., W. E. Horner & S. B. Lehrer, 1990. Identification and characterization of important cockroach allergengs. Journal of Allergy and Clinical Immunology, 86 (5): 781-787.
• Thompson, M., J. C. Steichen & R. H. Ffrench-Constant, 1993. Conservation of cyclodiene insecticide resistance-associated mutations in insects. Insect Molecular Biology, 2 (1): 149-154.
• Toprak, U., D. Hegedus, C. Doğan & G. Güney, 2020. A journey into the world of insect lipid metabolism. Archives of Insect Biochemistry and Physiology, 104 (2): e21682.
• Vaca, G. V., A. A. Michel & F. J. P. Alcaide, 2019. Histology and histochemistry of Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) fat body during the post embrionary development. Revista Chilena de Entomología, 45 (4): 521-532.
• Zara, F. J. & F. H. Caetano, 2004. Ultramorphology and histochemistry of fat body cells from last instar larval of the Pachycondyla (=Neoponera) villosa (Fabricius) (Formicidae: Ponerinae). Brazilian Journal of Biology, 64 (3b): 725-735.
• Zülfikaroğlu, T., G. Turgay-İzzetoğlu, M. S. Yıkılmaz & S. İzzetoğlu, 2022. Demonstrating the general structure and cell types of the fat body in Blatta orientalis (Oriental Cockroach). Anatomia, Histologia, Embryologia, 51 (1): 23-35.