Antimicrobial Peptides: Principal Defense Constituents of Silk Worms - A Review

Authors

  • Jakrimchi A Sangma Department of Zoology, Assam Don Bosco University, Tapesia Gardens, Kamrup 782403, Assam
  • Bhavna P Baroowa Department of Zoology, North Guwahati College, North Guwahati 781030, Assam
  • Yungkham Rajeevkumar Singh Department of Zoology, North Guwahati College, North Guwahati 781030, Assam
  • Prasanta Choudhury Department of Zoology, Assam Don Bosco University, Tapesia Gardens, Kamrup 782403, Assam

DOI:

https://doi.org/10.55446/IJE.2023.951

Keywords:

Antimicrobial peptides, silk worm, Philosamia ricini, insects’ immunity, cecropin, lebocin, moricin, attacin, defensin, gloverin, enbocin, isolation, characterization, microbes, multiple drug resistance

Abstract

Insect has a highly developed innate immune system consisting of cellular and humoral responses. Antimicrobial peptides (AMPs) are the important components of the insect’s humoral defense system and were first purified from the giant silk moth, Hyalophora cecropia L (Boman et al., 1980). For a variety of infections, they serve as the initial line of defense. AMPS are low molecular weight peptides and generally cationic in nature. Off late, the resistance of the pathogenic microbes towards established antibiotics have become a serious threat to global health. Over the years, an array of AMPs from natural sources has served as potent candidate against various infective agents viz. bacteria, fungi and viruses. These insect peptides not only exhibit antibacterial action by rupturing the microbial membrane but also prevent the development of drug resistance by microbes. Studies have shown AMPS to have synergistic effects with traditional antibiotics, providing an opportunity for combined therapy. Defensin, cecropins, drosocin, attacins, diptericins, ponericins, metchnikowins and melittin are a few classes of AMPs from insects that are currently isolated. However, the possibility of discovering new AMPs cannot be fully ruled out. Currently, 33 peptides are undergoing clinical trials, and 43% of the 77 AMPs are still in the preclinical stage (Makwana et al., 2023). Daptomycin and ovitavancin are two antibacterial lipopeptides that Food and Drug Administration has recently approved that are used for skin infection caused by bacteria. The present paper is an attempt to provide a comprehensive insight on antimicrobial peptides isolated from silk worm with reference to their structures, functions and possible mechanism of action.

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Published

2023-09-01

How to Cite

Sangma, J. A., Baroowa, B. P., Singh, Y. R., & Choudhury, P. (2023). Antimicrobial Peptides: Principal Defense Constituents of Silk Worms - A Review. Indian Journal of Entomology, 85(3), 808–819. https://doi.org/10.55446/IJE.2023.951

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Section

Review Articles

References

Abdel-latief M, Hilker M. 2008. Innate immunity: eggs of Manduca sexta are able to respond to parasitism by Trichogramma evanescens. Insect Biochemistry and Molecular Biology 38(2): 136–145.

Aley S B, Zimmerman M, Hetsko M, Selsted M E, Gillin F D. 1994. Killing of Giardia lamblia by cryptdins and cationic neutrophil peptides. Infection and Immunity 62(12): 5397- 403.

Andrä J, Berninghausen O, Leippe M. 2001. Cecropins, antibacterial peptides from insects and mammals, are potently fungicidal against Candida albicans. Medical Microbiology and Immunology 189: 169–173.

Al Souhail Q, Hiromasa Y, Rahnamaeian M, Giraldo M C, Takahashi D, Valent B, Vilcinskas A, Kanost M R. 2016. Characterization and regulation of expression of an antifungal peptide from hemolymph of an insect, Manduca sexta. Developmental and Comparative Immunology 61: 258–268.

Arrowood M J, Jaynes J M, Healey M C. 1991. In vitro activities of lytic peptides against the sporozoites of Cryptosporidium parvum. Antimicrobial Agents and Chemotheraphy 35(2): 224-227.

Axén A, Carlsson A, Engström A, Bennich H. 1997. Gloverin an antibacterial protein from the immune hemolymph of Hyalophora pupae. European Journal of Biochemistry 247(2): 614-619.

Barr S C, Rose D, Jaynes J M. 1995. Activity of lytic peptides against intracellular Trypanosoma cruzi amastigotes in vitro and parasitemias in mice. Journal of Parasitology 81(6): 974-978.

Barbault F, Landon C, Guenneugues M, Meyer J P, Schott V, Dimarcq J L, Vovelle F. 2003. Solution structure of Alo-3: a new knottin-type antifungal peptide from the insect Acrocinus longimanus. Biochemistry 42(49): 14434-14442.

Boisbouvier J, Prochnicka-Chalufour A, Nieto A R, Torres J A, Nanard N, Rodriguez M H, Possani D L, Delepierre M. 1998. Structural information on a cecropin-like synthetic peptide, Shiva-3 toxic to the sporogonic development of Plasmodium berghei. European Journal of Biochemistry 257(1): 263-273.

Boman H G, Hultmark D. 1987. Cell-free immunity in insects. Annual Review of Microbiology 41(1): 103–126.

Boulanger N, Brun R, Ehret-Sabatier L, Kunz C, Bulet P. 2002. Immunopeptides in the defense reactions of Glossina morsitans to bacterial and Trypanosoma brucei brucei infections. Insect Biochemistry and Molecular Biology 32(4): 369–375.

Brown S E, Howard A, Kasprzak A B, Gordon K H, East P D. 2008. The discovery and analysis of a diverged family of novel antifungal moricin-like peptides in the wax moth Galleria mellonella. Insect Biochemistry and Molecular Biology 38(2): 201-212.

Brey P T, Hultmark D. 1998. Molecular Mechanisms of Immune Responses in Insects. (Eds), Chapman & Hall, London/New York, 1998. Bulet P, Hetru C, Dimarcq J L, Hoffmann D. 1999. Abtimicrobial peptides in insects; structure and function. Developmental and Comparative Immunology 23(4-5): 329–344.

Bulet P, Stöcklin R, Menin L. 2004. Anti-microbial peptides: from invertebrates to vertebrates. Immunological Review 198(1): 169–184.

Buhroo Z I, Bhat M A, Bali G K, Kamili A S, Ganai N A. 2018. Antimicrobial peptides from insects with special reference to silkworm Bombyx mori L.: A review. Journal of Entomology and Zoology Studies 6: 752-759.

Buonocore F, Fausto A M, Pelle G D, Roncevic T, Gerdol M, Picchietti S. 2021. Attacins: A Promising Class of Insect Antimicrobial Peptides. Antibiotics 10(2): 212.

Casteels P, Ampe C, Riviere L, Van Damme J, Elicone C, Fleming M, Jacobs F, Tempst P. 1990. Isolation and characterization of abaecin, a major antibacterial response peptide in the honeybee (Apis mellifera). European Journal of Biochemistry 187(2): 381–386.

Carlsson A, Nyström T, de Cock H, Bennich H. 1998. Attacin—An insect immune protein—Binds LPS and triggers the specific inhibition of bacterial outer-membrane protein synthesis. Microbiology 144(8): 2179-2188.

Chalk R, Townson H, Ham P J. 1995. Brugia pahangi: the effects of cecropins on microfilariae in vitro and in Aedes aegypti. Experimental Parasitology 80(3): 401–406.

Chadwick J S, Aston W P. 1991. Antibacterial immunity in Lepidoptera. In: Gupta AP, editor. Immunology of insects and other arthropods. Boca Raton: CRC Press; 1991, 347-370.

Cheng T, Zhao P, Liu C, Xu P, Gao Z, Xia Q, Xiang Z. 2006. Structures, regulatory regions, and inductive expression patterns of antimicrobial peptide genes in the silkworm Bombyx mori. Genomics 87(3): 356-365.

Cheng T C, Zhang Y L, Liu C, Xu P Z, Gao Z H, Xia Q Y, Xiang Z H. 2008. Identification and analysis of Toll-related genes in the domesticated silkworm, Bombyx mori. Developmental and Comparative Immunology 32(5): 464-475.

Chen H M, Wang W, Smith D, Chan S C. 1997. Effects of the antibacterial peptide cecropin B and its analogs, cecropins B-1 and B-2, on liposomes, bacteria, and cancer cells. Biochimica et Biophysica Acta (BBA)-General subjects 1336(2): 171-179.

Chen C H, Lu T K. 2020. Development and challenges of antimicrobial peptides for therapeutic applications. Antibiotics 9(1):24.

Chowdhury S, Taniai K, Hara S, Kadonookuda K, Kato Y, Yamamoto M, Xu J, Choi S K, Debnath N C, Choi H K, Miyanoshita A, Sugiyama M, Asaoka A, Yamakawa M. 1995. cDNA cloning and gene expression of lebocin, a novel member of antibacterial peptides from the silkworm, Bombyx mori. Biochemical and Biophysical Research Communications 214(1): 271–278.

Christensen B C, Fink J, Merrifield R B, Mauzerall D. 1988. Channel-forming properties of cecropins and related model compounds incorporated into planar lipid membranes. Proceedings of the National Academy of Science 85(14): 5072–5076.

Cociancich S, Bulet P, Hetru C, Hoffmann J A. 1994. The inducible antibacterial peptides of insects. Parasitol Today 10(4): 132-139.

Dai H, Rayaprolu S, Gong Y, Huang R, Prakash O, Jiang H. 2008. Solution structure, antibacterial activity, and expression profile of Manduca sexta moricin. Journal of Peptide Science: An Official European Peptide Society14: 855–863.

Dini I, De Biasi M G, Mancusi A. 2022. An overview of the potentialities of antimicrobial peptides derived from natural sources. Antibiotics 11(11): 1483.

Dubovskiy I M, Kryukova N A, Glupov V V, Ratcliffe N A. 2016. Encapsulation and nodulation in insects. Invertebrate Survival Journal 13(1): 229-46.

Dularay B, Lackie A M. 1985. Haemocytic encapsulation and prophenoloxidase activation pathway in the locust Schisocerca gregaria. Forsk. Insects Biochemistry 15(6): 827-834.

Dunn P E. 1986. Biochemical aspects of insect immunology. Annual Review of Entomology 31(1): 321-339.

Durell S R, Raghunathan G, Guy H R. 1992. Modeling the ion channel structure of cecropin. Biophysical Journal 63(6): 1623–1631.

Dutta D, Kumar N, Willcox M D P. 2016. Antimicrobial activity of four cationic peptides immobilized to poly-hydroxyethylmethacrylate. Biofouling 32(4): 429-438.

Erdem Büyükkiraz, M.; Kesmen, Z. 2022. Antimicrobial peptides (AMPs): A promising class of antimicrobial compounds. J. Appl. Microbiol. 132: 1573–1596.

Fu H, Björstad A, Dahlgren C, Bylund J. 2004. A bactericidal cecropin-A peptide with a stabilized α-helical structure possess an increased killing capacity but no proinflammatory activity. Inflammation 28(6): 337–343.

Fujiwara S, Imai J, Fujiwara M, Yaeshima T, Kawashima T, Kobayashi K. 1990. A potent antibacterial protein in royal jelly. Purification and determination of the primary structure of royalisin. Journal of Biological Chemistry 265(19): 11333-11337.

Gabay J E. 1994. Ubiquitous Natural science. Science 264(5157): 373–374.

Gandhe A S, Arunkumar K P, John S H, Nagaraju J. 2006. Analysis of bacteria-challenged wild silkmoth, Antheraea mylitta (lepidoptera) transcriptome reveals potential immune genes.BMC Genomics 7(1): 1-10.

Ganz T. 2003. Defensins: antimicrobial peptides of innate immunity. Nature reviews immunology 3(9): 710–720.

Giacometti A, Cirioni O, Ghiselli R, Viticchi C, Mocchegiani F, Riva A, Saba V, Scalise G. 2001. Effect of mono-dose intraperitoneal cecropins in experimental septic shock. Critical care medicine 29(9): 1666–1669.

Goldsmith M R, Shimada T, Abe H. 2005. The genetics and genomics of the silkworm, Bombyx mori. Annual review entomology 50: 71-100.

Gudmundsson G H, Lidholm D A, Asling B, Gan R, Boman H G. 1991. The cecropin locus. Cloning and expression of a gene cluster encoding three antibacterial peptides in Hyalophora cecropia. Journal of Biological Chemistry 266(18): 11510–11517.

Guo C, Huang Y, Zheng H, Tang L, He J, Xiao L, Liu D, Jiang H. 2012. Secretion and activity of antimicrobial peptide cecropin D expressed in Pichia pastoris. Experimental and therapeutic Medicine 4(6): 1063–1068.

Gupta A P. 1986. Hemocytic and Humorul Immunity in Arthropods. Wiley, New York, 1986

Gupta A P. 1991. Immunology of insects and other arthropods. CRC press.

Hancock R E, Lehrer R. 1998. Cationic peptides: a new source of antibiotics. Trends in Biotechnology 16(2): 82-88.

Hara S, Yamakawa M. 1995. Moricin, a novel type of antibacterial peptide isolated from the silkworm, Bombyx mori (*). Journal of Biological Chemistry 270(50): 29923-29927.

Hara S, Yamakawa M. 1995. A novel antibacterial peptide family isolated from the silkworm, Bombyx mori. Biochemical Journal 310(2): 651–656.

Hetru C, Troxler L, Hoffmann J A. 2003. Drosophiola melanogaster antimicrobial defense. Journal of Infectious Diseases 187(Supplement_2): 327–S343.

Hoffmann J A, Hetru C. 1992. Insect defensins: Inducible antibacterial peptides. Immunology today 13(10): 411–415.

Hoffmann J A, Kafatos C F, Jr Janeway A C, Ezekowitz B A R. 1999. Phylogenetic perspective in innate immunity. Science 284(5418): 1313-1318.

Huan Y, Kong Q, Mou H, Yi H. 2020. Antimicrobial peptides: classification, design, application and research progress in multiple fields. Frontiers in microbiology p2559.

Hultmark D, Steiner H, Rasmuson T, Boman H G. 1980. Insect immunity. Purification and properties of three inducible bactericidal proteins from hemolymph of immunized pupae of Hyalophora cecropia. European Journal of Biochemistry106(1): 7-16.

Hultmark D, Engström A, Bennich H, Kapur R, Boman H G. 1982. Insect immunity. Isolation and structure of cecropin D and four minor antibacterial components from cecropia pupae. European Journal of Biochemistry 127(1): 207–217.

Hultmark D, Engström A, Andersson K, Steiner H, Bennich H, Boman H G. 1983. Insect immunity. Attacins, a family of antibacterial proteins from Hyalophora cecropia. The EMBO Journal 2(4): 571–576.

Hultmark D. 1993. Immune reactions in Drosophila and other insects: a model for innate immunity. Trends in Genetics 9(5): 178-183.

Hu H, Wang C, Guo X, Li W, Wang Y, He Q. 2013. Broad activity against porcine bacterial pathogens displayed by two insect antimicrobial peptides moricin and cecropin B. Molecules and Cells 35: 106–114.

Imura Y, Nishida M, Matsuzaki K. 2007. Action mechanism of PEGylated magainin 2 analogue peptides. Biochimica et Biophysica Acta (BBA) – Biomembranes 1768(10): 2578-2585.

Irving P, Troxler L, Heuer T S, Belvin M, Kopczynski C, Reichhart J M, Hoffmann J A, Hetru C. 2001. A genome-wide analysis of immune responses in Drosophila. Immunology 98(26): 15119-15124.

Islam J S, Bezbaruah S and Kalita J. 2016. A review on antimicrobial peptides from Bombyx mori L and their application in plant and animal disease control. Journal of Advances in Biology & Biotechnology 9(3): 1-15.

Ishii K, Hamamoto H, Sekimizu K. 2015. Studies of host-pathogen interactions and immune-related drug development using the silkworm: interdisciplinary immunology, microbiology, and pharmacology studies. Drug discoveries and Therapeutics 9(4): 238-246.

Jaynes J M, Burton C A, Barr S B, Jeffers G W, Julian G R, White K L, Enright F M, Klei T R, Laine R A. 1998. In vitro cytocidal effect of novel lytic peptides on Plasmodium falciparum and Trypanosoma cruzi. The FASEB Journal 2(13): 2878-2883.

Jayaram A, Pradeep A N R, Awasthi A K, Murthy G N, Ponnuvel K M, Sasibhushan S, Rao G C. 2014. Coregulation of host–response genes in integument: switchover of gene expression correlation pattern and impaired immune responses induced by dipteran parasite infection in the silkworm, Bombyx mori.Journal of Applied Genetics 55: 209–221.

Jin G, Weinberg A. 2018. Human antimicrobial peptides and cancer. In Seminars in Cell and Developmental Biology 88: 156-162.

Kaito C, Sekimizu K. 2007. A silkworm model of pathogenic bacterial infection. Drug Discovery and Therapeutics 1(2): 89-93.

Kaneko Y, Furukawa S, Tanaka H, Yamakawa M. 2007. Expression of antimicrobial peptide genes encoding Enbocin and Gloverin isoforms in the silkworm, Bombyx mori. Bioscience, Biotechnology and Biochemistry 71(9): 2233-2241.

Kaneko Yoichi, Tanaka Hiromitsu, Ishibashi J, Wasaki T, Yamakawa M. 2008. Gene expression of a novel defensin antimicrobial peptide in the silkworm, Bombyx mori. Bioscience, Biotechnology and Biochemistry 72(9): 2353–2361.

Kawaoka S, Katsuma S, Daimon T, Isono R, Omuro N, Mita K, Shimada T. 2008. Functional analysis of four Gloverin-like genes in the silkworm, Bombyx mori. Archives of Insect Biochemistry and Physiology: Published in collaboration with Entomological society of America 67(2): 87-96.

Kim S H, Park B S, Yun F Y, Je Y H, Woo S D, Kang S W, Kim K Y, Kang S K. 1998. Cloning and expression of a novel gene encoding a new antibacterial peptide from silkworm, Bombyx mori. Biochemical and Biophysical Research Communications 246(2): 388-392.

Kim S R, Hong M Y, Park S W, Choi K H, Yun E Y, Goo T W, Kang S W, Suh H J, Kim I, Hwang J S. 2010. Characterization and cDNA cloning of a cecropin-like antimicrobial peptide, papiliocin, from the swallowtail butterfly, Papilio xuthus. Molecules and Cells 29: 419-423.

Kockum K, Faye I, Hofsten P V, Lee J Y, Xanthopoulos K G, Boman H G. 1984. Insect immunity, Isolation and sequence of two cDNA clones corresponding to acidic and basic attacins from Hyalophora cecropia. The EMBO Journal 3(9): 2071–2075.

Kreil, G. 1994. In Antimicrobial Peptides (Ciba Foundation Symposium 186), pp.77–90, John Wiley & Sons, Inc., Chichester.

Lambert J, Keppi E, Dimarcq J L, Wicker C, Reichhart J M, Dunbar B, Lepages P, Van Dorsselaer A, Hoffmann J, Forthergill J, Hoffmann D. 1989. Insect immunity: isolation from immune blood of the dipteran Phormia terranovae of two insect antibacterial peptides with sequence homology to rabbit lung macrophage bactericidal peptides. Proceedings of National Academy of Sciences 86(1): 262–266.

Lamberty M, Ades S, Uttenweiler-Joseph S, Brookhart G, Bushey D, Hoffmann J A, Bulet P. 1999. Insect immunity: Isolation from the lepidopteran Heliothisvirescens of a novel insect defensin with potent antifungal activity. Journal of Biological Chemistry 274(14): 9320-9326.

Lamberty M, Caille A, Landon C, Tassin-Moindrot S, Hetru C, Bulet P, Vovelle F. 2001. Solution structures of the antifungal heliomicin and a selected variant with both antibacterial and antifungal activities. Biochemistry 40(40): 11995–12003.

Lavine M D, Strand M R. 2002. Insect hemocytes and their role in immunity. Insect biochemistry and molecular biology 32(10): 1295-309.

Lekha G, Vijayagwori E, Sirigineedi S, Sivaprasad V, Ponnuvel K M. 2014. Differential level of host gene expression associated with nucleopolyhedrovirus infection in silkworm races of Bombyx mori. International Journal of Industrial Entomology 29: 145–152.

Lekha G, Gupta T, Awasthi A K, Murthy G N, Trivedy K, Ponnuvel K M. 2015. Genome wide microarray-based expression profiles associated with BmNPV resistance and susceptibility in Indian silkworm races of Bombyx mori. Genomics 106: 393–403.

Lemaitre B, Hoffmann J. 2007. The host defense of Drosophila melanogaster. Annual review of Immunology 25: 697-743.

Li Z, Ma Y, Liu X, Li Y, Dai F. 2019. Antimicrobial peptides in silkworm. Animal Biology 69(4): 391-410.

Liu X, Guo C, Huang Y, Zhang X, Chen Y. 2015. Inhibition of porcine reproductive and respiratory syndrome virus by Cecropin D in vitro. Infection, Genetics and Evolution 34: 7–16.

Lundstrom A, Liu G, Kang D, Berzins K, Steiner H. 2002. Trichoplusia ni gloverin, an inducible immune gene encoding an antibacterial insect protein. Insect Biochemistry and Molecular Biology 32(7): 795-801.

Lu D, Geng T, Hou C, Huang Y, Qin G, Guo X. 2016. Bombyx mori cecropin A has a high antifungal activity to entomopathogenic fungus Beauveria bassiana. Gene 583(1): 29–35.

Mackintosh J A, Gooley A A, Karuso P H, Beattie A J, Jardine D R, Veal D A. 1998a. A gloverin-like antibacterial protein is synthesized in Helicoverpa armigera following bacterial challenge. Developmental and Comparative Immunology 22(4): 387–399.

Mahlapuu M, Björn C, Ekblom J. 2020. Antimicrobial peptides as therapeutic agents: Opportunities and challenges. Critical reviews in biotechnology 40(7): 978-92.

Manniello M D, Moretta A, Salvia R, Scieuzo C, Lucchetti D, Vogel H, Sgambato A, Falabella P. 2021. Insect antimicrobial peptides: Potential weapons to counteract the antibiotic resistance. Cellular and Molecular Life Science 78: 4259–4282.

Makwana P, Dubey H, Pradeep A N R, Sivaprasad V, Ponnuvel K M, Mishra R K. 2021. Dipteran endo parasitoid infestation actively suppressed host defense components in hemocytes of silkwormBombyx morifor successful parasitism. Animal Gene 22: 200118.

Makwana P, Kamisi R, Katsuhiko I, Bindu S. 2023. Diversity of antimicrobial peptides in silkworm. Life 13(5): 1161.

Mastore M, Quadroni S, Caramella S, Brivio M F. 2021. The Silkworm as a Source of Natural Antimicrobial Preparations: Efficacy on Various Bacterial Strains. Antibiotics 10(11):1339.

Matsuyama K, Natori S. 1998. Purification of three antibacterial proteins from the culture medium of NIH-Sape-4, an embryonic cell line of Sarcophega peregrina. Journal of Biological Chemistry 263(32): 17112– 17116.

Meng X, Zhu F, Chen K. 2017. Silkworm: A Promising Model Organism in Life Science. Journal of Insect Science 17(5): 97.

Minakhina S, Steward R. 2010. Hematopoietic stem cells in Drosophila. Development 137(1):27-31.

Moore A J, Beazley W D, Bibby M C, Devine D A. 1996. Antimicrobial activity of cecropins. Journal of Antimicrobial and Chemotherapy 37(6): 1077-1089.

Montano A M, Tsujino F, Takahata N, Satta Y. 2011. Evolutionary of peptidoglycan recognition proteins in vertebrate innate immune system. BMC Evolutionary Biology 11(1): 1-10.

Moretta A, Scieuzo C, Petrone A M, Salvia R, Manniello M D, Franco A, Lucchetti D, Vassallo A, Vogel H, Sgambato A, Falabella P. 2021. Antimicrobial peptides: A new hope in biomedical and pharmaceutical fields. Frontiers in Cellular and Infection Microbiology p 453.

Mrinal N, Nagaraju J. 2008. Intron loss is associated with gain of function in the evolution of the gloverin family of antibacterial genes in Bombyx mori. Journal of Biological Chemistry 283(34): 23376–23387.

Nakajima Y, Qu X M, Natori S. 1987. Interaction between liposomes and sarcotoxin IA, a potent antibacterial protein of Sarcophaga peregrina (flesh fly). Journal of Biological Chemistry 262(4): 1665-1669.

Nayak T, Mandal S M, Neog K, Ghosh A K. 2017. Characterization of a gloverin-like antimicrobial peptide isolated from muga silkworm, Antheraea assamensis. International journal of Peptides Research and Therapeutics 24: 337-346.

Nesa J, Sadat A, Buccini D F, Kati A, Manda A K, Franco O L. 2020. Antimicrobial peptides from Bombyx mori: a splendid immune defense response in silkworms. Royal Society of Chemistry Advances 10(1): 512-523.

Noorwala M, Mohammad F V, Ahmad V U, Sener B. 1994. A bidesmosidic triterpene glycoside from the roots of Symphytum officinale. Phytochemistry 36(2): 439-443.

Oizumi Y, Hemmi H, Minami M, Asaoka A, Yamakawa M. 2005. Isolation, gene expression and solution structure of a novel moricin analogue, antibacterial peptide from a lepidopteran insect, Spodoptera litura. Biochimica et Biophysica Acta (BBA)-proteins and Proteomics 1752(1): 83-92.

Ouyang, L.; Xu, X.; Freed, S.; Gao, Y.; Yu, J.; Wang, S.; Ju, W.; Zhang, Y.; Jin, F. Cecropins from Plutella xylostella and Their Interaction with Metarhizium anisopliae. PLoS ONE 10: e0142451.

Okada M, Natori S. 1985. Primary structure of sarcotoxin I, an antibacterial protein induced in the hemolymph of Sarcophaga peregrina (flesh fly) larvae. Journal of Biological Chemistry 260(12): 7174–7177.

Park S I, An H S, Chang B S, Yoe S M. 2013. Expression, cDNA cloning, and characterization of the antibacterial peptide cecropin D from Agrius convolvuli. Animal Cells and System 17(1): 23–30.

Pillai A, Ueno S, Zhang H, Lee J M, Kato Y. 2005. Cecropin P1 and novel nematode cecropins: a bacteria-inducible antimicrobial peptide family in the nematode Ascaris suum. Biochemical Journal 390(1): 207–214.

Ponnuvel K M, Yamakawa M. 2002. Immune responses against bacterial infection in Bombyx mori and regulation of host gene expression. Current Science 83: 447-454.

Pradeep A N R, Anita J, Awasthi A K, Babu M A, Geetha M N, Arun H K, Chandrashekhar S, Rao G C. 2013. Activation of autophagic programmed cell death and innate immune gene expression reveals immuno-competence of integumental epithelium in Bombyx mori infected by a dipteran parasitoid. Cell and Tissue Research 352: 371–385.

Ramzah N H, Yenn T W, Lee W H, Loo C Y, Tan W N, Ring L C. 2023. Antimicrobial peptides, an alternative antimicrobial agent against multi-drug-resistant microbes: Source, application, and potential. In Advancements in Materials Science and Technology Led by Women 9: 235-259.

Ravindar G, Ragamalika G and Nagaraja Rao P. 2015. Analysis of proteins profile and antibacterial activity in haemolymph of Eri silkworm, Samia cynthia ricini after bacterial inoculation. International Journal of Advanced Research 3(1): 186-192.

Ravi C, Jeyashree A, Devi K R. 2011. Antimicrobial Peptides from insects: an overview. Research in Biotechnology 2(5).

Ratcliffe N A. 1985. Invertebrate immunity- a primer for the non-specialist. Immunology Letters 10(5): 253-270.

Ribeiro C, Brehélin M. 2006. Insect haemocytes: what type of cell is that?. Journal of insect physiology 52(5): 417-29.

Rizki T M, Rizki R M. 1984. The cellular defense system of Drosophila melanogaster. Insect ultrastructure 2: 579-604.

Russell V W, Dunn P E. 1996. Antibacterial proteins in the midgut of Manduca sexta during metamorphosis. Journal Insect Physiology 42(1): 65-71.

Saviane A, Romoli O, Bozzato A, Freddi G, Cappelletti C, Rosini E, Cappellozza S, Tettamanti G, Sandrelli F. 2018. Intrinsic antimicrobial properties of silk spun by genetically modified silkworm strains. Transgenic Research 27: 87-101.

Schmid-Hempel, P. 2005. Evolutionary ecology of insect’s immune defenses. Annual Review of Entomology 50: 529-551.

Silvestro L, Axelsen P H. 2000. Membrane-induced folding of cecropin A. Biophysical Journal 79(3): 1465–1477.

Song L, Wang F, Dong S, Hu C, Hua X, Xia Q. 2015. Paralytic peptide activates insect humoral immune response via epidermal growth factor receptor. Peptide, 71: 20–27.

Strand M R. 2008. The insect cellular immune response. Insect science 15(1): 1-4.

Srisailam S, Arunkumar A I, Wang W, Yu C, Chen H M. 2000. Conformational study of a custom antibacterial peptide cecropin B1: implications of the lytic activity. Biochimica et Biophysica Acta (BBA)-Protein Structure and Molecular Enzymology 1479(1-2): 275–285.

Srisailam S, Kumar T K, Arunkumar A I, Leung K W, Yu C, Chen H M. 2001. Crumpled structure of the custom hydrophobic lytic peptide cecropin B3. European Journal of Biochemistry 268(15): 4278–4284.

Steiner H, Hultmark D, Engstrom A, Bennich H, Boman H G. 1981. Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature 292(5820): 246-248.

Suttmann H, Retz M, Paulsen F, Harder J, Zwergel U, Kamradt J, Wullich B, Unteregger G, Stockie M, Lehmann J. 2008. Antimicrobial peptides of the Cecropin-family show potent antitumor activity against bladder cancer cells. BMC Urology 8(1): 1-7.

Tan J, Xu M, Zhang K, Wang X, Chen S, Li T, Xiang Z, Cui H. 2013. Characterization of hemocytes proliferation in larval silkworm, Bombyx mori. Journal of insect physiology 59(6): 595-603.

Tanaka H, Ishibashi J, Fujita K, Nakajima Y, Sagisaka A, Tomimoto K, Suzuki N, Yoshiyama M, Kaneko Y, Iwasaki T, Sunagwa T, Yamaji K, Asaoka A, Mita K, Yamakawa M. 2008. A genome-wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochemistry and Molecular Biology 38(12): 1087-1110.

Uddin S J, Shilpi J A, Nahar L, Sarker S D, Göransson U. 2021. Natural antimicrobial peptides: Hope for new antibiotic lead molecules. Frontiers in Pharmacology 12: 640938.

Vanzolini T, Bruschi M, Rinaldi A C, Magnani M, Fraternale A. 2022. Multitalented synthetic antimicrobial peptides and their antibacterial, antifungal and antiviral mechanisms. Int. J. Mol. Sci. 23: 545.

Volkoff A N, Rocher J, d’Alencon E, Bouton M, Landais I, QuesadaMoraga E, Vey A, Fournier P, Mita K, Devauchelle G. 2003. Characterization and transcriptional profiles of three Spodoptera frugiperda genes encoding cysteine-rich peptides: A new class of defensin-like genes from lepidopteran insects? Gene 319: 43–53.

Wang M, Zhou Z, Li S, Zhu W, Hu X. 2021. Identification and characterization of antimicrobial peptides from butterflies: an integrated bioinformatics and experimental study. Frontiers in microbiology 12: 720381.

Wang Y P, Lai R. 2010. Insect antimicrobial peptides: structures, properties and gene regulation. Zoological research 31(1): 27-34. DOI:10.3724/SP.J.1141.2010.01027.

Wang D, Qiu X, Wang H. Qiao K, wang K. 2010. Reduced fitness associated with spinosad resistance in Helicoverpa armigera. Phytoparasitica 38: 103–110.

Wan J, Zhou X, Zhou X. 2012. A review of innate immunity of silkworm, Bombyx mori. African Journal of Agricultural Research 8(20): 2319-2325.

Wen H, Lan X, Cheng T, He N, Shiomi K, Kajiura Z, Zhou Z, Xia Q, Xiang Z, Nakagaki M. 2009. Sequence structure and expression pattern of a novel anionic defensin-like gene from silkworm (Bombyx mori). Molecular Biology reports 36: 711-716.

Wu Qinghua, Patoˇcka Jiˇrí, Kuˇca Kamil Kuˇca. 2018. Insect antimicrobial peptides, a mini review. Toxins 10(11): 461.

Xiao Y, Hughes A L, Ando J, Mastuda Y, Cheng J F, Skinner-Noble D, Zhang G. 2004. A genome-wide screen identifies a single β-defensin gene cluster in the chicken: implications for the origin and evolution of mammalian defensins. BMC Genomics 5: 1-11.

Xu X X, Zhong X, Yi H Y, Yu X Q. 2012. Manduca sexta gloverin binds microbial components and is active against bacteria and fungi. Developmental and Comparative Immunology 38(2): 275–284.

Yamano Y, Matsumoto M, Sasahara K, Sakamoto E, Morishima I. 1998. Structure of genes for cecropin A and an inducible nuclear protein that binds to the promoter region of the genes from the silkworm, Bombyx mori. Bioscience, biotechnology and biochemistry 62(2): 237-241.

Yamakawa M, Tanaka H. 1999. Immune proteins and their gene expression in the silkworm, Bombyx mori. Developmental & Comparative Immunology 23(4-5): 281-289.

Yang W, Cheng T, Ye M, Deng X, Yi H, Huang Y, Tan X, Han D, Wang B, Xiang Z, Cao Y, Xia Q. 2011. Functional divergence among silkworm antimicrobial peptide paralogs by the activities of recombinant proteins and the induced expression profiles. PLOS ONE 6(3): e18109.

Yi H Y, Chowdhury M, Huang Y D, Yu X Q. 2014. Insect antimicrobial peptides and their applications. Applied microbiology and biotechnology 98: 5807–5822.

Yoe S M, Kang C S, Han S S, Bang I S. 2006. Characterization and cDNA cloning of hinnavin II, a cecropin family antibacterial peptide from the cabbage butterfly, Artogeia rapae. Comparative Biochemistry and Physiology- Biochemistry and Molecular Biology 144(2): 199-205.

Yun J, Lee D G. 2016. Cecropin A-induced apoptosis is regulated by ion balance and glutathione antioxidant system in Candida albicans. IUBMB Life 68(8): 652–662.

Zhao W Y, Dong B R, Zhou Y. 2005. In vitro antimicrobial activity of defensins from rabbit neutrophils against Pseudomonas aeruginosa and its multiple-drug-resistance strains. Sichuan da xue xue bao. Yi xue ban 36(1): 83–85.

Zhu Y, Johnson T J, Myers A A, Kanost M R. 2003. Identification by subtractive suppression hybridization of bacteria-induced genes expressed in Manduca sexta fat body. Insect biochemistry and molecular biology 33(5): 541–559.