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Per os feeding with antisera specific to peritrophic matrix proteins stimulates larval growth in Mamestra configurata Walker (Lepidoptera: Noctuidae)

Year 2013, Volume: 37 Issue: 2, 203 - 212, 01.04.2013

Abstract

Peritrophic matrix (PM) is an acellular, porous sheath composed of chitin and proteins that lines the midgut epithelial cells. The PM serves as a barrier against food particles, pathogens and toxins. Several studies in dipteran systems revealed that antibodies specific to PM proteins retard insect development by binding to their target antigens in the PM and blocking PM pores. To test whether antisera specific to PM proteins also inhibit larval growth in a lepidopteran system, antisera specific to chitin deacetylase 1, insect intestinal mucin 2, insect intestinal mucin 4 and PM protein 1 were fed to 2nd instar Mamestra configurata Walker (Lepidoptera: Noctuidae) larvae, a major pest of Brassica plants in North America. Interestingly, all larvae feeding on antisera gained more weight than the larvae feeding on the diet containing non-immune sera or no antiserum. The anti-McPM1 and anti-McIIM4 antisera treatments showed the highest larval weight gains, followed by the anti-McCDA1 and anti-McIIM2 antisera treatments. The interaction of treatment with time was found significant by the 6th day and the interaction of concentration with time was found significant only by the 12th day. No difference was found between the larval weights from all treatments at concentrations of 1 or 4%.

References

  • Adang, M. J. & K. D. Spence, 1983. Permeability of the peritrophic membrane of the Douglas fir tussock moth (Orgyia pseudotsugata). Comparative Physiology and Biochemistry 75A(2): 233-238.
  • Allingham, P. G., I. J. East, R. L. Kerlin & D. H. Kemp, 1998. Digestion of host immunoglobulin and activity of midgut proteases in the buffalo fly Haematobia irritans exigua. Journal of Insect Physiology 44(5-6): 445-450. Barbehenn, R. V. & M. M. Martin, 1995. Peritrophic envelope permeability in herbivorous insects. Journal of Insect Physiology 41(4): 303-311.
  • Bradford, M. M, 1976. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248-254.
  • Bucher, G. E. & G. K. Bracken, 1976. The bertha armyworm, Mamestra configurata (Lepidoptera: Noctuidae). Artificial diet and rearing technique. Canadian Entomologist 108(12): 1327-1338.
  • Caldeira, W., A. B. Dias, W. R. Terra & A. F. Ribeiro, 2007. Digestive enzyme compartmentalization and recycling and sites of absorption and secretion along the midgut of Dermestes maculatus (Coleoptera) larvae. Archives of Insect Biochemistry and Physiology 64(1): 1-18.
  • Casu, R., C. Eisemann, R. Pearson, G. Riding, I. East, A. Donaldson, L. Cadogan & R. L. Tellam, 1997. Antibodymediated inhibition of the growth of larvae from an insect causing cutaneous myiasis in a mammalian host. Proceedings of the National Academy of Sciences of the United States of America 94(17): 8939-8944. East, I. J. & C. H. Eisemann, 1993. Vaccination against Lucilia cuprina: the causative agent of sheep blowfly strike. Immunology and Cell Biology 71(5): 453-62.
  • East, I. J., C. J. Eitzgerald, R. D. Pearson, R. A. Donaldson, T. Vuocolo, L. C. Cadogan, C. H. Eisemann & R. L. Tellam, 1993. Lucilia cuprina: Inhibition of larval growth induced by immunisation of host sheep with extracts of larval peritrophic membrane. International Journal for Parasitology 23(2): 221-229.
  • Eisemann, C. H., R. D. Pearson, R. A. Donaldson, L. C. Cadogan & T. Vuocolo, 1993. Uptake and fate of specific antibody in feeding larvae of the sheep blowfly, Lucilia cuprina. Medical and Veterinary Entomology 7(2): 1771
  • Eisemann, C. H. & K. C. Binnington, 1994. The peritrophic membrane: its formation, structure, chemical composition and permeability in relation to vaccination against ectoparasitic arthropods. International Journal for Parasitology 24(1): 15-26.
  • Hegedus, D., D. Baldwin, M. O’Grady, L. Braun, S. Gleddie, A. Sharpe, D. Lydiate & M. Erlandson, 2003. Midgut proteases from Mamestra configurata (Lepidoptera: Noctuidae) larvae: Characterization, cDNA cloning and expressed sequence tag analysis. Archives of Insect Biochemistry and Physiology 53(1): 30-47.
  • Hegedus, D., M. Erlandson, C. Gillott & U. Toprak, 2009. New insights into peritrophic matrix synthesis, architecture, and function. Annual Review of Entomology 54: 285-302.
  • Lehane, M. J., 1997. Peritrophic matrix structure and function. Annual Review of Entomology 42: 525-550.
  • Natalia, D., S. Muharsini, F. F. Masduki, A. H. Wardhana, S. E. Wardani, E. Maria & J. V. D. Heuvel, 2007. Production of recombinant vaccine Cb peritrophin-42 of screwworm fly in Escherichia coli and Saccharomyces cerevisiae. Microbiology Indonesia 1(3): 105-108.
  • Ramasamy, M. S., K. A. Srikrishanraj, S. Wijekoone, L. S. Jesuthasan & R. Ramasamy, 1992. Host immunity to mosquitoes: effect of anti-mosquito antibodies on Anopheles tessellatus and Culex quinquefasciatus (Diptera: Culicidae). Journal of Medical Entomology 29(6): 934-938.
  • Ryerse, J. S., J. P. Purcell, R. D Sammons & P. B. Lavrik, 1992. Peritrophic membrane structure and formation in the larva of a moth, Heliothis. Tissue and Cell 24(5): 751-771.
  • Shi, X., M. Chamankhah, S. Visal-Shah, S. M. Hemmingsen, M. Erlandson, L. Braun, M. Alting-Mees, G. G. Khachatourians, M. O’Grady & D. D. Hegedus , 200 Modeling the structure of the type I peritrophic matrix: Characterization of a Mamestra configurata intestinal mucin and novel peritrophin containing 19 chitin binding domains. Insect Biochemistry and Molecular Biology 34(10): 1101-1115.
  • Sukarsih, S. Partoutomo, E. Satria, G. Wijffels, G. Riding, C. Eisemann & P. Willadsen, 2000a. Vaccination against the old world screwwormy (Chrysomya bezziana). Parasite Immunology 22(11): 545-552.
  • Sukarsih, S. Partoutomo, G. Wijffels, T. Vuocolo & P. Willadsen, 2000b. Vaccination trials in sheep against Chrysomya bezziana larvae using the recombinant peritrophin antigens cb15, cb42 and cb48. Indonesian Journal of Animal and Veterinary Sciences 5(3): 192-196.
  • Suneja, A., M. Gulia & S. K. Gakhar, 2003. Blocking of malaria parasite development in mosquito and fecundity reduction by midgut antibodies in Anopheles stephensi (Diptera: Culicidae). Archives of Insect Biochemistry and Physiology 52(2): 63-70.
  • Tellam, R. L. & C. H. Eisemann, 1998. Inhibition of growth of Lucilia cuprina larvae using serum from sheep vaccinated with first-instar larval antigens. International Journal for Parasitology 28(3): 439-450.
  • Tellam, R. L., C. H. Eisemann, T. Vuocolo, R. Casu, J. Jarmey, V. Bowles & R. Pearson, 2001. Role of oligosaccharides in the immune response of sheep vaccinated with Lucilia cuprina larval glycoprotein, peritrophin-95. International Journal for Parasitology 31(8): 798-809.
  • Terra, W. R., C. Ferreira & A. G. de Bianchi, 1979. Distribution of digestive enzymes among the endo- and ectoperitrophic spaces and midgut cells of Rhynchosciara and its physiological significance. Journal of Insect Physiology 25(6): 487-494.
  • Terra, W. R. & C. Ferreira, 1994. Insect digestive enzymes: Properties, compartmentalization and function. Comparative Physiology and Biochemistry 109B(1): 1-62.
  • Toprak, U., D. Baldwin, M. Erlandson, C. Gillott, X. Hou, C. Coutu & D. Hegedus, 2008. A chitin deacetylase and putative insect intestinal lipases are components of Mamestra configuata peritrophic matrix. Insect Molecular Biology 17(5): 573-585.
  • Toprak, U., D. Baldwin, M. Erlandson, C. Gillott, S. Harris & D. Hegedus, 2010a. Expression patterns of genes encoding proteins with peritrophin A domains and protein localization in Mamestra configurata. Journal of Insect Physiology 56(12): 1711-1720.
  • Toprak, U., D. Baldwin, M. Erlandson, C. Gillott & D. Hegedus, 2010b. Insect intestinal mucins and serine proteases associated with the peritrophic matrix from feeding, starved and molting Mamestra configurata larvae. Insect Molecular Biology 19(2): 163-175.
  • Toprak, U., M. Erlandson & D. Hegedus, 2010c. Peritrophic matrix proteins. Trends in Entomology 6: 23-51. Valentine, R. C. & N. M. Green, 1967. Electron microscopy of an antibody hapten complex. Journal of Molecular Biology 27(3): 615-617.

Peritrofik matriks proteinlerine spesifik antiserumların ağız yoluyla yedirilmesinin Mamestra configurata Walker (Lepidoptera: Noctuidae) larva gelişimine etkisi

Year 2013, Volume: 37 Issue: 2, 203 - 212, 01.04.2013

Abstract

Peritrofik matriks (PM) mide epitel hücreleri boyunca uzanan, kitin ve proteinden oluşan gözenekli ve hücresiz bir yapıdır. PM besin partikülleri, patojenler ve toksinlere karşı bir bariyer görevi görmektedir. Dipter sistemlerdeki çeşitli araştırmalar PM proteinlerine spesifik antibadilerin PM’deki hedef antijenlerine bağlanıp PM gözeneklerini tıkayarak böcek gelişimini geciktirdiğini göstermiştir. PM proteinlerine spesifik antibadilerin lepidopter bir sistemde de larva gelişimini engelleyip engellemediğinin belirlenmesi amacıyla, kitin deasetilaz 1, böcek barsak musini 2, böcek barsak musini 4 ve PM proteini 1 proteinlerine spesifik antiserumlar, Kuzey Amerika’daki Brassica bitkilerinin ana zararlısı durumunda olan Mamestra configurata Walker (Lepidoptera: Noctuidae)’nın 2. dönem larvalarına yedirilmiştir. İlginç olarak bu larvalar, antiserum içermeyen veya normal serum içeren besin üzerinde beslenen larvalara göre daha fazla ağırlık kazanmıştır. Anti-McPM1 and anti-McIIM4 antiserum denemeleri en yüksek larva ağırlık artışına neden olurken, anti-McCDA1 and anti-McIIM2 antiserum denemeleri daha az ağırlık artışına neden olmuştur. Antiserum-zaman ilişkisi 6. günden itibaren önemli bulunurken, konsantrasyon-zaman ilişkisi sadece 12. günde önemli bulunmuştur. Tüm antiserum uygulamalarının % 1 veya % 4’lük konsantrasyonlarındaki larva ağırlık artışları arasındaki fark önemli bulunmamıştır.

References

  • Adang, M. J. & K. D. Spence, 1983. Permeability of the peritrophic membrane of the Douglas fir tussock moth (Orgyia pseudotsugata). Comparative Physiology and Biochemistry 75A(2): 233-238.
  • Allingham, P. G., I. J. East, R. L. Kerlin & D. H. Kemp, 1998. Digestion of host immunoglobulin and activity of midgut proteases in the buffalo fly Haematobia irritans exigua. Journal of Insect Physiology 44(5-6): 445-450. Barbehenn, R. V. & M. M. Martin, 1995. Peritrophic envelope permeability in herbivorous insects. Journal of Insect Physiology 41(4): 303-311.
  • Bradford, M. M, 1976. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248-254.
  • Bucher, G. E. & G. K. Bracken, 1976. The bertha armyworm, Mamestra configurata (Lepidoptera: Noctuidae). Artificial diet and rearing technique. Canadian Entomologist 108(12): 1327-1338.
  • Caldeira, W., A. B. Dias, W. R. Terra & A. F. Ribeiro, 2007. Digestive enzyme compartmentalization and recycling and sites of absorption and secretion along the midgut of Dermestes maculatus (Coleoptera) larvae. Archives of Insect Biochemistry and Physiology 64(1): 1-18.
  • Casu, R., C. Eisemann, R. Pearson, G. Riding, I. East, A. Donaldson, L. Cadogan & R. L. Tellam, 1997. Antibodymediated inhibition of the growth of larvae from an insect causing cutaneous myiasis in a mammalian host. Proceedings of the National Academy of Sciences of the United States of America 94(17): 8939-8944. East, I. J. & C. H. Eisemann, 1993. Vaccination against Lucilia cuprina: the causative agent of sheep blowfly strike. Immunology and Cell Biology 71(5): 453-62.
  • East, I. J., C. J. Eitzgerald, R. D. Pearson, R. A. Donaldson, T. Vuocolo, L. C. Cadogan, C. H. Eisemann & R. L. Tellam, 1993. Lucilia cuprina: Inhibition of larval growth induced by immunisation of host sheep with extracts of larval peritrophic membrane. International Journal for Parasitology 23(2): 221-229.
  • Eisemann, C. H., R. D. Pearson, R. A. Donaldson, L. C. Cadogan & T. Vuocolo, 1993. Uptake and fate of specific antibody in feeding larvae of the sheep blowfly, Lucilia cuprina. Medical and Veterinary Entomology 7(2): 1771
  • Eisemann, C. H. & K. C. Binnington, 1994. The peritrophic membrane: its formation, structure, chemical composition and permeability in relation to vaccination against ectoparasitic arthropods. International Journal for Parasitology 24(1): 15-26.
  • Hegedus, D., D. Baldwin, M. O’Grady, L. Braun, S. Gleddie, A. Sharpe, D. Lydiate & M. Erlandson, 2003. Midgut proteases from Mamestra configurata (Lepidoptera: Noctuidae) larvae: Characterization, cDNA cloning and expressed sequence tag analysis. Archives of Insect Biochemistry and Physiology 53(1): 30-47.
  • Hegedus, D., M. Erlandson, C. Gillott & U. Toprak, 2009. New insights into peritrophic matrix synthesis, architecture, and function. Annual Review of Entomology 54: 285-302.
  • Lehane, M. J., 1997. Peritrophic matrix structure and function. Annual Review of Entomology 42: 525-550.
  • Natalia, D., S. Muharsini, F. F. Masduki, A. H. Wardhana, S. E. Wardani, E. Maria & J. V. D. Heuvel, 2007. Production of recombinant vaccine Cb peritrophin-42 of screwworm fly in Escherichia coli and Saccharomyces cerevisiae. Microbiology Indonesia 1(3): 105-108.
  • Ramasamy, M. S., K. A. Srikrishanraj, S. Wijekoone, L. S. Jesuthasan & R. Ramasamy, 1992. Host immunity to mosquitoes: effect of anti-mosquito antibodies on Anopheles tessellatus and Culex quinquefasciatus (Diptera: Culicidae). Journal of Medical Entomology 29(6): 934-938.
  • Ryerse, J. S., J. P. Purcell, R. D Sammons & P. B. Lavrik, 1992. Peritrophic membrane structure and formation in the larva of a moth, Heliothis. Tissue and Cell 24(5): 751-771.
  • Shi, X., M. Chamankhah, S. Visal-Shah, S. M. Hemmingsen, M. Erlandson, L. Braun, M. Alting-Mees, G. G. Khachatourians, M. O’Grady & D. D. Hegedus , 200 Modeling the structure of the type I peritrophic matrix: Characterization of a Mamestra configurata intestinal mucin and novel peritrophin containing 19 chitin binding domains. Insect Biochemistry and Molecular Biology 34(10): 1101-1115.
  • Sukarsih, S. Partoutomo, E. Satria, G. Wijffels, G. Riding, C. Eisemann & P. Willadsen, 2000a. Vaccination against the old world screwwormy (Chrysomya bezziana). Parasite Immunology 22(11): 545-552.
  • Sukarsih, S. Partoutomo, G. Wijffels, T. Vuocolo & P. Willadsen, 2000b. Vaccination trials in sheep against Chrysomya bezziana larvae using the recombinant peritrophin antigens cb15, cb42 and cb48. Indonesian Journal of Animal and Veterinary Sciences 5(3): 192-196.
  • Suneja, A., M. Gulia & S. K. Gakhar, 2003. Blocking of malaria parasite development in mosquito and fecundity reduction by midgut antibodies in Anopheles stephensi (Diptera: Culicidae). Archives of Insect Biochemistry and Physiology 52(2): 63-70.
  • Tellam, R. L. & C. H. Eisemann, 1998. Inhibition of growth of Lucilia cuprina larvae using serum from sheep vaccinated with first-instar larval antigens. International Journal for Parasitology 28(3): 439-450.
  • Tellam, R. L., C. H. Eisemann, T. Vuocolo, R. Casu, J. Jarmey, V. Bowles & R. Pearson, 2001. Role of oligosaccharides in the immune response of sheep vaccinated with Lucilia cuprina larval glycoprotein, peritrophin-95. International Journal for Parasitology 31(8): 798-809.
  • Terra, W. R., C. Ferreira & A. G. de Bianchi, 1979. Distribution of digestive enzymes among the endo- and ectoperitrophic spaces and midgut cells of Rhynchosciara and its physiological significance. Journal of Insect Physiology 25(6): 487-494.
  • Terra, W. R. & C. Ferreira, 1994. Insect digestive enzymes: Properties, compartmentalization and function. Comparative Physiology and Biochemistry 109B(1): 1-62.
  • Toprak, U., D. Baldwin, M. Erlandson, C. Gillott, X. Hou, C. Coutu & D. Hegedus, 2008. A chitin deacetylase and putative insect intestinal lipases are components of Mamestra configuata peritrophic matrix. Insect Molecular Biology 17(5): 573-585.
  • Toprak, U., D. Baldwin, M. Erlandson, C. Gillott, S. Harris & D. Hegedus, 2010a. Expression patterns of genes encoding proteins with peritrophin A domains and protein localization in Mamestra configurata. Journal of Insect Physiology 56(12): 1711-1720.
  • Toprak, U., D. Baldwin, M. Erlandson, C. Gillott & D. Hegedus, 2010b. Insect intestinal mucins and serine proteases associated with the peritrophic matrix from feeding, starved and molting Mamestra configurata larvae. Insect Molecular Biology 19(2): 163-175.
  • Toprak, U., M. Erlandson & D. Hegedus, 2010c. Peritrophic matrix proteins. Trends in Entomology 6: 23-51. Valentine, R. C. & N. M. Green, 1967. Electron microscopy of an antibody hapten complex. Journal of Molecular Biology 27(3): 615-617.
There are 27 citations in total.

Details

Primary Language Turkish
Journal Section Articles
Authors

Umut Toprak This is me

Doug Baldwın This is me

Dwayne D. Hegedus This is me

Martin Erlandson (203-211) This is me

Publication Date April 1, 2013
Submission Date February 8, 2014
Published in Issue Year 2013 Volume: 37 Issue: 2

Cite

APA Toprak, U. ., Baldwın, D. ., Hegedus, D. D. . . ., (203-211), M. E. . (2013). Peritrofik matriks proteinlerine spesifik antiserumların ağız yoluyla yedirilmesinin Mamestra configurata Walker (Lepidoptera: Noctuidae) larva gelişimine etkisi. Turkish Journal of Entomology, 37(2), 203-212.
AMA Toprak U, Baldwın D, Hegedus DD, (203-211) ME. Peritrofik matriks proteinlerine spesifik antiserumların ağız yoluyla yedirilmesinin Mamestra configurata Walker (Lepidoptera: Noctuidae) larva gelişimine etkisi. TED. April 2013;37(2):203-212.
Chicago Toprak, Umut, Doug Baldwın, Dwayne D. Hegedus, and Martin Erlandson (203-211). “Peritrofik Matriks Proteinlerine Spesifik antiserumların ağız Yoluyla Yedirilmesinin Mamestra Configurata Walker (Lepidoptera: Noctuidae) Larva gelişimine Etkisi”. Turkish Journal of Entomology 37, no. 2 (April 2013): 203-12.
EndNote Toprak U, Baldwın D, Hegedus DD, (203-211) ME (April 1, 2013) Peritrofik matriks proteinlerine spesifik antiserumların ağız yoluyla yedirilmesinin Mamestra configurata Walker (Lepidoptera: Noctuidae) larva gelişimine etkisi. Turkish Journal of Entomology 37 2 203–212.
IEEE U. . Toprak, D. . Baldwın, D. D. . . . Hegedus, and M. E. . (203-211), “Peritrofik matriks proteinlerine spesifik antiserumların ağız yoluyla yedirilmesinin Mamestra configurata Walker (Lepidoptera: Noctuidae) larva gelişimine etkisi”, TED, vol. 37, no. 2, pp. 203–212, 2013.
ISNAD Toprak, Umut et al. “Peritrofik Matriks Proteinlerine Spesifik antiserumların ağız Yoluyla Yedirilmesinin Mamestra Configurata Walker (Lepidoptera: Noctuidae) Larva gelişimine Etkisi”. Turkish Journal of Entomology 37/2 (April 2013), 203-212.
JAMA Toprak U, Baldwın D, Hegedus DD, (203-211) ME. Peritrofik matriks proteinlerine spesifik antiserumların ağız yoluyla yedirilmesinin Mamestra configurata Walker (Lepidoptera: Noctuidae) larva gelişimine etkisi. TED. 2013;37:203–212.
MLA Toprak, Umut et al. “Peritrofik Matriks Proteinlerine Spesifik antiserumların ağız Yoluyla Yedirilmesinin Mamestra Configurata Walker (Lepidoptera: Noctuidae) Larva gelişimine Etkisi”. Turkish Journal of Entomology, vol. 37, no. 2, 2013, pp. 203-12.
Vancouver Toprak U, Baldwın D, Hegedus DD, (203-211) ME. Peritrofik matriks proteinlerine spesifik antiserumların ağız yoluyla yedirilmesinin Mamestra configurata Walker (Lepidoptera: Noctuidae) larva gelişimine etkisi. TED. 2013;37(2):203-12.