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

Volumn 352, Issue 2, 2013, Pages 371-385

  Pradeep, Appukuttan Nair R ^a   Anitha, Jayaram ^a   Awasthi, Arvind K ^a   Babu, Mohd A ^b   Geetha, Murthy N ^a   Arun, Hariharan K ^a   Chandrashekhar, Sagar ^c   Rao, Guruprasad C ^a   Vijayaprakash, Nanjappa B ^a  

^a Seribiotech Research Laboratory   (India)

^b CENTRAL SERICULTURAL RESEARCH AND TRAINING INSTITUTE   (India)

^c NATIONAL INSTITUTE OF MENTAL HEALTH AND NEUROSCIENCES   (India)

Author keywords

Apoptosis; Bombyx mori (Insecta); Host parasite interaction; PPO2 expression; Toll pathway activation

Indexed keywords

CASPASE; CHITINASE; CYTOKINE; DORSAL PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSECT PROTEIN; MELANIN; MONOPHENOL MONOOXYGENASE; N ACETYL BETA GLUCOSAMINIDASE; OXIDOREDUCTASE; PROPHENOL OXIDASE 2; QUINONE DERIVATIVE; SPATZLE PROTEIN; TOLL PROTEIN; TRANSCRIPTION FACTOR REL; TYROSINE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BOMBYX MORI; CASPASE GENE; CELL ACTIVATION; CELL VACUOLE; CONTROLLED STUDY; DNA FRAGMENTATION; DNA SEQUENCE; DOWN REGULATION; ENDOPARASITE; ENZYME ACTIVATION; ENZYME ACTIVITY; EXORISTA BOMBYCIS; FUNCTIONAL PROTEOMICS; GENE EXPRESSION; GENETIC VARIABILITY; HUMORAL IMMUNITY; IMMUNOCOMPETENCE; INNATE IMMUNITY; LAMELLAR BODY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN EPITHELIUM; UPREGULATION;

ANIMALS; APOPTOSIS; BOMBYX; CELL DEATH; DIPTERA; FEMALE; GENE EXPRESSION PROFILING; HOST-PARASITE INTERACTIONS; MALE; SIGNAL TRANSDUCTION;

BOMBYX MORI; CACTACEAE; DIPTERA; EXORISTA BOMBYCIS; HEXAPODA; INSECTA;

EID: 84880571465     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-012-1520-7     Document Type: Article

References (90)

1. Acharya MM, Katyare SS (2004) An improved micromethod for tyrosine estimation. Z Naturforsch 59c:897-900
2. Amaya KE, Asgari S, Jung R, Hongskula M, Beckage NE (2005) Parasitization of Manduca sexta larvae by the parasitoid wasp Cotesia congregata induces an impaired host immune response. J Insect Physiol 51:505-512
3. Ambrose RL, Mackenzie JM (2010) West Nile virus differentially modulates the unfolded protein response to facilitate replication and immune evasion. J Virol 85:2723-2732
4. Asano T, Ashida M (2001) Cuticular pro-phenoloxidase of the silkworm, Bombyx mori: purification and demonstration of its transport from hemolymph. J Biol Chem 276:11100-11112
5. Ashida M, Brey PT (1995) Role of the integument in insect defense: pro-phenol oxidase cascade in the cuticular matrix. Proc Natl Acad Sci USA 92:10698-10702
6. Ashida M, Brey PT (1998) Recent advances in research on the insect prophenoloxidase cascade. In: Brey PT, Hultmark D (eds) Molecular mechanisms of immune responses in insects. Chapman and Hall, London, pp 135-172
7. Biron DG, Ponton F, Marché L, Galeotti N, Renault L, Demey-Thomas E, Poncet J, Brown SP, Jouin P, Thomas F (2006) Suicide of crickets harbouring hairworms: a proteomics investigation. Insect Mol Biol 15:731-742
8. Boltz KA, Carney GE (2008) Loss of p24 function in Drosophila melanogaster causes a stress response and increased levels of NF-κB-regulated gene products. BMC Genomics 9:212
9. Bras M, Queenan B, Susin SA (2005) Programmed cell death via mitochondria: different modes of dying. Biochem Mosc 70:284-293
10. Brey PT, Lee WJ, Yamakawa M, Koizumi Y, Perrot S, Francois M, Ashida M (1993) Role of the integument in insect immunity: epicuticular abrasion and induction of cecropin synthesis in cuticular epithelial cells. Proc Natl Acad Sci USA 90:6275-6279
11. Bruchhaus I, Roeder T, Rennenberg A, Heussler VT (2007) Protozoan parasites: programmed cell death as a mechanism of parasitism. Trends Parasitol 23:376-383
12. Bursch W, Ellinger A, Gerner CH, Fröhwein U, Schulte-Hermann R (2000) Programmed cell death (PCD): apoptosis, autophagic PCD or others? Ann N Y Acad Sci 926:1-12
13. Chan DC (2006) Mitochondria: dynamic organelles in disease, aging, and development. Cell 125:1241-1252
14. Chatterjee SN, Mohandas TP, Taraphdar T (2003) Molecular characterization of the gene pool of Exorista sorbillans (Diptera: Tachinidae) a parasitoid of silkworm, Bombyx mori, in India. Eur J Entomol 100:195-200
15. Cheng TC, Zhang YL, Chun L, Xu PZ, Gao ZH, Xia QY, Xiang ZH (2008) Identification and analysis of toll-related genes in the domesticated silkworm, Bombyx mori. Dev Comp Immunol 32:464-475
16. Christophides GK, Zdobnov E, Barillas-Mury C, Birney E, Blandin S, Blass C, et al (2002) Immunity-related genes and gene families in Anopheles gambiae. Science 298:159-165
17. Clark TM, Hutchinson MJ, Huegel KL, Moffett SB, Moffett DF (2005) Additional morphological and physiological heterogeneity within the midgut of larval Aedes aegypti (Diptera: Culicidae) revealed by histology, electrophysiology and effects of Bacillus thuringiensis endotoxin. Tissue Cell 37:457-468
18. De Gregorio E, Spellman PT, Tzou P, Rubin GM, Lemaitre B (2002) Toll and IMD pathways are the major regulators of the immune response in Drosophila. EMBO J 21:2568-2579
19. Dohke K (1973) Studies on prophenoloxidase-activating enzyme from cuticle of the silkworm. Bombyx mori. II. Purification and characterization of the enzyme. Arch Biochem Biophys 157:210-221
20. DosReis GA, Barcinski MA (2001) Apoptosis and parasitism: from the parasite to the host immune response. Adv Parasitol 49:133-161
21. Etebari K, Palfreyman RW, Schlipalius D, Nielsen LK, Glatz RV, Asgari S (2011) Deep sequencing-based transcriptome analysis of Plutella xylostella larvae parasitized by Diadegma semiclausum. BMC Genomics 12:446
22. Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, Jiang H et al (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol 15:645-656
23. Ferrandon D, Imler JL, Hetru C, Hoffmann JA (2007) The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat Rev Immunol 7:862-874
24. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294-299
25. Gandhe AS, John SH, Nagaraju J (2007) Noduler, a novel immune up-regulated protein mediates nodulation response in insects. J Immunol 179:6943-6951
26. Gillespie JP, Kanost MR, Trenczek T (1997) Biological mediators of insect immunity. Annu Rev Entomol 42:611-643
27. Goldsmith MR, Shimada T, Abe H (2005) The genetics and genomics of the silkworm, Bombyx mori. Ann Rev Entomol 50:71-100
28. Gottlieb E, Armour SM, Harris MH, Thompson CB (2003) Mitochondrial membrane potential regulates matrix configuration and cytochrome c release during apoptosis. Cell Death Diff 10:709-717
29. Hardt N, DeKegel D, Vanheule L, Villani G, Spadari S (1980) DNA polymerase γ, cytochrome c oxidase and mitochondrial integrity in rabbit spleen lymphocytes stimulated with concanavalin A. Exp Cell Res 127:269-276
30. Higes M, García-Palencia P, Martín-Hernández R, Meana A (2007) Experimental infection of Apis mellifera honey bees with Nosema ceranae (Microsporidia). J Invertebr Pathol 94:211-217
31. Hoffmann JA, Kafatos FC, Janeway CA, Ezekowitz RA (1999) Phylogenetic perspectives in innate immunity. Science 284:1313-1318
32. Hurd H, Carter V, Nacer A (2005) Interactions between malaria and mosquitoes: the role of apoptosis in parasite establishment and vector response to infection. Curr Top Microbiol Immunol 289:185-217
33. Ioannou YA, Chen FW (1996) Quantitation of DNA fragmentation in apoptosis. Nucleic Acids Res 24:992-993
34. Ishii K, Hamamoto H, Kamimura M, Nakamura Y, Noda H, Imamura K, Mita K, Sekimizu K (2010) Insect cytokine paralytic peptide (PP) induces cellular and humoral immune responses in the silkworm Bombyx mori. J Biol Chem 285:28635-28642
35. Jiang J, Cai H, Zhou Q, Levine M (1993) Conversion of a dorsal-dependent silencer into an enhancer: evidence for dorsal corepressors. EMBO J 12:3201-3209
36. Kuraishi T, Binggeli O, Opota O, Buchon N, Lemaitre B (2011) Genetic evidence for a protective role of the peritrophic matrix against intestinal bacterial infection in Drosophila melanogaster. Proc Natl Acad Sci USA 108:15966-15971
37. LeBlanc PM, Saleh M (2009) Caspases in inflammation and immunity. eLS, Wiley Online Library
38. Leist M, Jaattela M (2001) Four deaths and a funeral: from caspases to alternative mechanisms. Nature Rev Mol Cell Biol 2:589-598
39. Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA (1996) The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila. EMBO J 14:536-545
40. Liu L, Tang Q, Fu C, Peng J, Yang H, Li Y, Hong H (2007) Influence of glucose starvation on the pathway of death in insect cell line Sl: apoptosis follows autophagy. Cytotechnology 54:97-105
41. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin-phenol reagent. J Biol Chem 193:265-275
42. Martin DN, Baehrecke EH (2004) Caspases function in autophagic programmed cell death in Drosophila. Development 131:275-284
43. Matus S, Lisbona F, Torres M, Leon C, Thielen P, Hetz C (2008) The stress rheostat: an interplay between the unfolded protein response (UPR) and autophagy in neurodegeneration. Curr Mol Med 8:157-172
44. McBride HM, Neuspiel M, Wasiak S (2006) Mitochondria: more than just a powerhouse. Curr Biol 16:R551-R560
45. Meister M, Govind S (2003) Hematopoietic development in Drosophila: a parallel with vertebrates. In: Godin I, Cumano A (eds) Hematopoietic stem cells. Landes Bioscience, Austin
46. Merzendorfer H, Zimoch L (2003) Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases. J Exp Biol 206:4393-4412
47. Mrinal N, Tomar A, Nagaraju J (2011) Role of sequence encoded κB DNA geometry in gene regulation by Dorsal. Nucleic Acids Res 39:9574-9591
48. Nakahara Y, Kanamori Y, Kiuchi M, Kamimura M (2003) Effects of silkworm paralytic peptide on in vitro hematopoiesis and plasmatocyte spreading. Arch Insect Biochem Physiol 52:163-174
49. Nappi AJ, Vass E (1993) Melanogenesis and the generation of cytotoxic molecules during insect cellular immune reactions. Pigment Cell Res 6:117-126
50. Narayanaswamy KC, Devaiah MC (1998) Silkworm uzi fly. Zen Publishers, Bangalore
51. Noguchi H, Tsuzuki S, Tanaka K, Matsumoto H, Hiruma K, Hayakawa Y (2003) Isolation and characterization of a dopa decarboxylase cDNA and the induction of its expression by an insect cytokine, growth-blocking peptide in Pseudaletia separate. Insect Biochem Mol Biol 33:209-217
52. Oeckinghaus A, Hayden MS, Ghosh S (2011) Crosstalk in NF-κB signaling pathways. Nat Immunol 12:695-708
53. Pahl HL, Baeuerle PA (1997) The ER-overload response: activation of NF-κB. Trends Biochem Sci 22:63-67
54. Palmer CA, Wittrock DD, Christensen BM (1986) Ultrastructure of Malpighian tubules of Aedes aegypti infected with Dirofilaria immitis. J Invertebr Pathol 48:310-317
55. Perumalsamy LR, Nagala M, Sarin A (2010) Notch-activated cascade interacts with mitochondrial remodeling proteins to regulate cell survival. Proc Natl Acad Sci USA 107:6882-6887
56. Pinheiro DO, Silva MD, Gregorio EA (2010) Mitochondria in the midgut epithelial cells of sugarcane borer parasitized by Cotesia flavipes (Cameron, 1891). Braz J Biol 70:163-169
57. Pradeep AR, Awasthi AK, Urs RS (2008) Association of A/T rich microsatellites with responses to artificial selection for larval developmental duration in the silkworm Bombyx mori. Mol Cells 25:467-478
58. Pradeep AR, Awasthi AK, Singh CK, Anuradha HJ, Rao CG, Vijayaprakash NB (2011) Genetic evaluation of eri silkworm Samia cynthia ricini: ISSR loci specific to high and low altitude regimes and quantitative attributes. J Appl Genet 52:345-353
59. Prasad MD, Muthulakshmi M, Madhu M, Archak S, Mita K, Nagaraju J (2005) Survey and analysis of microsatellites in the silkworm, Bombyx mori: frequency, distribution, mutations, marker potential and their conservation in heterologous species. Genetics 169:197-214
60. Pye AE (1974) Microbial activation of prophenoloxidase from immune insect larvae. Nature 251:610-613
61. Reddy BK, Rao JVK (2009) Seasonal occurrence and control of silkworm diseases, grasserie, flacherie and muscardine and insect pest, uzi fly in Andhra Pradesh, India. Int J Indust Entomol 18:57-61
62. Rosenfeld J, Capdevielle J, Guillemot C, Ferrara P (1992) In-gel digestion for internal sequence analysis after one- or two-dimensional gel electrophoresis. Anal Biochem 203:173-179
63. Santamaría-Fríes M, Fajardo LF, Sogin ML, Olson PD, Relman DA (1996) Lethal infection by a previously unrecognised metazoan parasite. Lancet 347:1797-1801
64. Sass M (2008) Autophagy research on insects. Autophagy 4:265-267
65. Satake S, Kaya M, Sakurai S (1998) Hemolymph ecdysteroid titer and ecdysteroid-dependent developmental events in the last-larval stadium of the silkworm, Bombyx mori: role of low ecdysteroid titer in larval-pupal metamorphosis and a reappraisal of the head critical period. J Insect Physiol 44:867-881
66. Sathisha GJ, Prakash YKS, Chachadi VB, Nagaraja NN, Inamdar SR, Leonidas DD, Savithri HS, Swamy BM (2008) X-ray sequence ambiguities of Sclerotium rolfsii lectin resolved by mass spectrometry. Amino Acids 35:309-320
67. Schaub GA, Sehnitker A (1988) Influence of Blastocrithidia triatomae (Trypanosomatidae) on the reduviid bug Triatoma infestans: alterations in the Malpighian tubules. Parasitol Res 75:88-97
68. Schlenke TA, Morales J, Govind S, Clark AG (2007) Contrasting infection strategies in generalist and specialist wasp parasitoids of Drosophila melanogaster. PLoS Pathog 3:e158
69. Schluns H, Sadd BM, Schmid-Hempel P, Crozier RH (2010) Infection with the trypanosome Crithidia bombi and expression of immune - related genes in the bumble bee Bombus terrestris. Dev Comp Immunol 34:705-709
70. Schmid-Hempel P (2005) Evolutionary ecology of insect immune defenses. Ann Rev Entomol 50:529-551
71. Schmidt O (2008) Insect immune recognition and suppression. In: Beckage NE (ed) Insect immunology. Elsevier/Academic Press, San Diego, pp 271-294
72. Sengupta K, Kumar P, Baig M, Govindaiah M (1990) Handbook of pest and disease control in mulberry and silkworm. United Nations Economic and Social Commission for Asia and the Pacific, Bangkok
73. Sorrentino RP, Carton Y, Govind S (2002) Cellular immune response to parasite infection in the Drosophila lymph gland is developmentally regulated. Dev Biol 243:65-80
74. Strengerg C, Benchimol M, Linden R (2010) Caspase dependence of the death of neonatal retinal ganglion cells induced by axon damage and induction of autophagy as survival mechanism. Braz J Med Biol Res 43:950-956
75. Suganuma I, Ushiyama T, Yamada H, Iwamoto A, Kobayashi M, Ikeda M (2011) Cloning and characterization of a dronc homologue in the silkworm, Bombyx mori. Insect Biochem Mol Biol 41:909-921
76. Takahashi M, Kiuchi M, Kamimura M (2002) A new chitinase-related gene, BmChiR1, is induced in the Bombyx mori anterior silk gland at molt and metamorphosis by ecdysteroid. Insect Biochem Mol Biol 32:147-151
77. Takayama S, Reed JC, Homma S (2003) Heat-shock proteins as regulators of apoptosis. Oncogene 22:9041-9047
78. Tanaka H, Yamamoto M, Moriyama Y, Yamao M, Furukawa S, Sagisaka A et al (2005) A novel Rel protein and shortened isoform that differentially regulate antibacterial protein genes in the silkworm, Bombyx mori. Biochim Biophys Acta 1730:10-21
79. Tanaka H, Ishibashi J, Fujita K, Nakajima Y, Sagisaka A, Tomimoto K, Suzuki N et al (2008) A genome-wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochem Mol Biol 38:1087-1110
80. Tang H (2009) Regulation and function of the melanization reaction in Drosophila. Fly (Austin) 3:105-111
81. Torres M, Castillo K, Armisén R, Stutzin A, Soto C, Hetz C (2010) Prion protein misfolding affects calcium homeostasis and sensitizes cells to endoplasmic reticulum stress. PLoS One 5:e15658
82. Valanne S, Wang JH, Rämet M (2011) The Drosophila toll signaling pathway. J Immunol 186:649-656
83. Wertheim B, Kraaijeveld AR, Schuster E, Blanc E, Hopkins M, Pletcher SD, Strand MR, Partridge L, Godfray HCJ (2005) Genome-wide gene expression in response to parasitoid attack in Drosophila. Genome Biol 6:R94
84. Wertheim B, Kraaijeveld AR, Hopkins MG, Boer MW, Godfray HCJ (2011) Functional genomics of the evolution of increased resistance to parasitism in Drosophila. Mol Ecol 20:932-949
85. Wirawan E, Berghe TV, Lippens S, Agostinis P, Vandenabeele P (2011) Autophagy: for better or for worse. Cell Res 22:43-61
86. Yano T, Kurata S (2011) Intracellular recognition of pathogens and autophagy as an innate immune host defence. J Biochem 150:143-149
87. Zeiske W, Meyer H, Wheczoreck H (2002) Insect midgut K secretion concerted run-down of apical/basolateral transporters with extra/intracellular acidity. J Exp Biol 205:463-467
88. Zhang YM, Lu XF, Bhavnani BR (2003) Equine estrogens differentially inhibit DNA fragmentation induced by glutamate in neuronal cells by modulation of regulatory proteins involved in programmed cell death. BMC Neurosci 4:32
89. Zhang FX, Shao HL, Wang JX, Zhao XF (2011) β-Thymosin is upregulated by the steroid hormone 20-hydroxyecdysone and microorganisms. Insect Mol Biol 20:519-527
90. Zou Z, Shin SW, Alvarez KS, Bian G, Kokoza V, Raikhel AS (2008) Mosquito RUNX4 in the immune regulation of PPO gene expression and its effect on avian malaria parasite infection. Proc Nat Acad Sci USA 105:18454-18459