Antioxidant defense of the midgut epithelium by the peritrophic envelope in caterpillars

Journal of Insect Physiology

Volumn 50, Issue 9, 2004, Pages 783-790

  Barbehenn, Raymond V ^a   Stannard, Jasmine ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Caterpillar; Iron; Lepidoptera; Oxidation; Peritrophic envelope; Reactive oxygen species

Indexed keywords

ANTIOXIDANT; BENZENESULFONIC ACID DERIVATIVE; C.I. FLUORESCENT BRIGHTENING AGENT 28; IRON; PROTEIN; TANNIN DERIVATIVE;

ANTIOXIDANT;

ANIMAL; ARTICLE; CANADA; COMPARATIVE STUDY; EPITHELIUM; EXTRACELLULAR MATRIX; GASTROINTESTINAL TRACT; LARVA; METABOLISM; MOTH; NONPARAMETRIC TEST;

ANIMALS; ANTIOXIDANTS; BENZENESULFONATES; EPITHELIUM; EXTRACELLULAR MATRIX; GASTROINTESTINAL TRACT; IRON; LARVA; MOTHS; ONTARIO; PROTEINS; STATISTICS, NONPARAMETRIC; TANNINS;

ARTHROPODA; LEPIDOPTERA; MALACOSOMA; MALACOSOMA DISSTRIA; ORGYIA; ORGYIA LEUCOSTIGMA; PHACELIA CONGESTA; TRIXIS;

EID: 12344296957     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2004.05.012     Document Type: Article

References (55)

1. Ahmad S. Biochemical defence of pro-oxidant plant allelochemicals by herbivorous insects. Biochemical Ecology and Systematics. 20:1992;269-296
2. Allen S.E. Chemical composition of soils and plant materials. Allen S.E. Analysis of Ecological Materials. 1974;508-509 Blackwell, Oxford
3. Arosio P., Levi S. Ferritin, iron homeostasis, and oxidative damage. Free Radical Biology and Medicine. 33:2002;457-463
4. Baines D.M. Observations on the peritrophic membrane of Locusta migratoria migratorioides (R. and F.) nymphs. Acrida. 7:1978;11-21
5. Barbehenn R. Roles of peritrophic membranes in protecting herbivorous insects from ingested plant allelochemicals. Archives of Insect Biochemistry and Physiology. 47:2001;86-99
6. Barbehenn R.V., Martin M.M. The protective role of the peritrophic membrane in the tannin-tolerant larvae of Orgyia leucostigma (Lepidoptera). Journal of Insect Physiology. 38:1992;973-980
7. Barbehenn R.V., Martin M.M. Tannin sensitivity in Malacosoma disstria: roles of the peritrophic envelope and midgut oxidation. Journal of Chemical Ecology. 20:1994;1985-2001
8. Barbehenn R.V., Martin M.M. Permeability of the peritrophic envelopes of herbivorous insects to dextran sulfate: a test of the polyanion exclusion hypothesis. Journal of Insect Physiology. 43:1997;243-249
9. Barbehenn R.V., Martin M.M. Formation of insoluble and colloidally dispersed tannic acid complexes in the midgut fluid of Manduca sexta (Lepidoptera: Sphingidae): an explanation for the failure of tannic acid to cross the peritrophic envelopes of lepidopteran larvae. Archives of Insect Biochemistry and Physiology. 39:1998;109-117
10. Barbehenn R.V., Bumgarner S.L., Roosen E.F., Martin M.M. Antioxidant defenses in caterpillars: role of the ascorbate-recycling system in the midgut lumen. Journal of Insect Physiology. 47:2001;349-357
11. Barbehenn R.V., Poopat U., Spencer B. Semiquinone and ascorbyl radicals in the gut fluids of caterpillars measured with EPR spectrometry. Insect Biochemistry and Molecular Biology. 33:2002;125-130
12. Bartnicki-Garcia S., Persson J., Chanzy H. An electron microscope and electron diffraction study of the effect of Calcofluor and Congo red on the biosynthesis of chitin in vitro. Archives of Biochemistry and Biophysics. 310:1994;6-15
13. Bernays E.A., Simpson S.J. Nutrition. Chapman R.F., Joern A. Biology of Grasshoppers. 1989;105-128 John Wiley and Sons, New York
14. Broadway R.M., Williams D.L., Kain W.C., Harman G.E., Lorito M., Labeda D.P. Partial purification of chitinolytic enzymes from Streptomyces albidoflavus. Journal of Applied Microbiology. 20:1995;271-276
15. Buettner G. The pecking order of free radicals and antioxidants: lipid peroxidation, α-tocopherol, and ascorbate. Archives of Biochemistry and Biophysics. 300:1993;535-543
16. Cross C.E., Halliwell B., Allen A. Antioxidant protection: a function of tracheobronchial and gastrointestinal mucus. Lancet. 1:1984;1328-1330
17. Davies M.J., Fu S., Wang H., Dean R.T. Stable markers of oxidant damage to proteins and their application in the study of human disease. Free Radical Biology and Medicine. 27:1999;1151-1163
18. Duffey S.S., Stout M.J. Antinutritive and toxic components of plant defense against insects. Archives of Insect Biochemistry and Physiology. 32:1996;3-37
19. Edwards M.J., Jacobs-Lorena M. Permeability and disruption of the peritrophic matrix and caecal membrane from Aedes aegypti and Anopheles gambiae mosquito larvae. Journal of Insect Physiology. 46:2000;1313-1320
20. Felton G.W. Nutritive quality of plant protein: sources of variation and insect herbivore responses. Archives of Insect Biochemistry and Physiology. 32:1996;107-130
21. Felton G.W., Summers C.B. Antioxidant systems in insects. Archives of Insect Biochemistry and Physiology. 29:1995;187-197
22. Gamblin B.E., Stevens J.G., Wilson K.L. Structural investigations of chitin and chitosan complexed with iron or tin. Hyperfine Interactions. 112:1998;117-122
23. Granger D.N., Hernandez L.A., Grisham M.B. Reactive oxygen metabolites: mediators of cell injury in the digestive system. Viewpoints on Digestive Diseases. 18:1986;13-16
24. Grisham M.B. Reactive Metabolites of Oxygen and Nitrogen in Biology and Medicine. 1992;Landes, Austin
25. Grisham M.B., Von Ritter C., Smith B.F., Lamont J.T., Granger D.N. Interaction between oxygen radicals and gastric mucin. American Journal of Physiology. 253:1987;G93-G96
26. Halliwell B., Gutteridge J.M.C. Oxygen free radicals and iron in relation to biology and medicine: some problems and concepts. Archives of Biochemistry and Biophysics. 246:1986;501-514
27. Halliwell B., Gutteridge J.M.C. The antioxidants of human extracellular fluids. Archives of Biochemistry and Biophysics. 280:1990;1-8
28. Halliwell B., Gutteridge J.M.C. Free Radicals in Biology and Medicine. 1999;Oxford University Press, New York
29. Halliwell B., Zhao K., Whiteman M. The gastrointestinal tract: a major site of antioxidant action. Free Radical Research. 33:2000;819-830
30. Hoover K., Washburn J.O., Volkman L.E. Midgut-based resistance of Heliothis virescens to baculovirus infection mediated by phytochemicals in cotton. Journal of Insect Physiology. 49:2000;999-1007
31. Kakhlon O., Cabantchik Z.I. The labile iron pool: characterization, measurement, and participation in cellular processes. Free Radical Biology and Medicine. 33:2002;1037-1046
32. Kim I.G., Park S.Y., Oh T.J. Dithiothreitol induces the sacrificial antioxidant property of human serum albumin in a metal-catalyzed oxidation and γ-irradiation system. Archives of Biochemistry and Biophysics. 388:2001;1-6
33. Koshijima T., Tanaka R., Muraki E., Yamada A., Yaku F. Chelating polymers derived from cellulose and chitin. I. Formation of polymer complexes with metal ions. Cellulose Chemistry and Technology. 7:1973;197-208
34. Krantz-Rulcker C., Frandberg E., Schnurer J. Metal loading and enzymatic degradation of fungal cell walls and chitin. Biometals. 8:1995;12-18
35. Lehane M.J. Peritrophic matrix structure and function. Annual Review of Entomology. 42:1997;525-550
36. McDonald M., Mila I., Scalbert A. Precipitation of metal ions by plant polyphenols: optimal conditions and origin of precipitation. Journal of Agriculture and Food Chemistry. 44:1996;599-606
37. Pascoa V., Oliveira P.L., Dansa-Petretski M., Silva J.R., Alvarenga P.H., Jacobs-Lorena M., Lemos F.J.A. Aedes aegypti peritrophic matrix and its interaction with heme during blood digestion. Insect Biochemistry and Molecular Biology. 32:2002;517-523
38. Peters W. Peritrophic Membranes. 1992;Berlin, Springer-Verlag
39. Quinlan G.J., Gutteridge J.M.C. Carbonyl assay for oxidative damage to proteins. Taniguchi N., Gutteridge J.M.C. Experimental Protocols for Reactive Oxygen and Nitrogen Species. 2000;257-258 Oxford University Press, New York
40. Reznick A.Z., Packer L. Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods in Enzymology. 233:1994;357-371
41. Schneider W. Iron hydrolysis and the biochemistry of iron - the interplay of hydroxide and biogenic ligands. Chimia. 42:1988;9-20
42. Sheppard C.A., Shapiro M. Physiological and nutritional effects of a fluorescent brightener on nuclear polyhedrosis virus-infected Lymantria dispar (L.) larvae (Lepidoptera: Lymantriidae). Biological Control. 4:1994;404-411
43. Stadtman E.R. Metal ion-catalyzed oxidation of proteins: biochemical mechanism and biological consequences. Free Radical Biology and Medicine. 9:1990;315-325
44. Summers C.B., Felton G.W. Prooxidant effects of phenolic acids on the generalist herbivore Helicoverpa zea (Lepidoptera: Noctuidae): potential mode of action for phenolic compounds in plant anti-herbivore chemistry. Insect Biochemistry and Molecular Biology. 24:1994;943-953
45. Summers C.B., Felton G.W. Peritrophic envelope as a functional antioxidant. Archives of Insect Biochemistry and Physiology. 32:1996;131-142
46. Tellam R.L., Eisemann C. Chitin is only a minor component of the peritrophic matrix from larvae of Lucilia cuprina. Insect Biochemistry and Molecular Biology. 30:2000;1189-1201
47. Tellam R.L., Wijffels G., Willadsen P. Peritrophic matrix proteins. Insect Biochemistry and Molecular Biology. 29:1999;87-101
48. Wang P., Granados R.R. An intestinal mucin is the target substrate for a baculovirus enhancin. Proceedings of the National Academy of Sciences USA. 94:1997;6977-6982
49. Wang P., Granados R.R. Calcofluor disrupts the midgut defense system in insects. Insect Biochemistry and Molecular Biology. 30:2000;135-143
50. Wang P., Granados R.R. Molecular structure of the peritrophic membrane (PM): identification of potential PM target sites for insect control. Archives of Insect Biochemistry and Physiology. 47:2001;110-118
51. Washburn J.O., Kirkpatrick B.A., Haas-Stapleton E., Volkman L.E. Evidence that the stilbene-derived optical brightener M2R enhances Autographa californica M nucleopolyhedrovirus infection of Trichoplusia ni and Heliothis virescens by preventing sloughing of infected midgut epithelial cells. Biological Control. 11:1998;58-69
52. Watanabe N., Forman H.J. Autoxidation of extracellular hydroquinones is a causative event for the cytotoxicity of menadione and DMNQ in A549-S cells. Archives of Biochemistry and Biophysics. 411:2003;145-157
53. Welch K.D., Davis T.Z., Van Eden M.E., Aust S.D. Deleterious iron-mediated oxidation of biomolecules. Free Radical Biology and Medicine. 32:2002;577-583
54. Wilkinson L. SYSTAT: The System for Statistics. 2000;SYSTAT Inc, Evanston, IL
55. Zimmerman D., Peters W. Fine structure and permeability of peritrophic membranes of Calliphora erythrocephala (Meigen) (Insecta: Diptera) after inhibition of chitin and protein synthesis. Comparative Biochemistry and Physiology. 86B:1987;353-360