Eur. J. Entomol. 111 (4): 457-468, 2014 | DOI: 10.14411/eje.2014.064

Identifications of cytochrome c and Apaf-1 and their mRNA expressions under heat stress in insecticide-susceptible and -resistant Plutella xylostella (Lepidoptera: Plutellidae)

Lin Jie ZHANG1,2, Jing Fei HUANG1,2, Feng CHEN1,2, Zhen Yang YU1,2, Zhao Li WU1,2, Gang WU1,*
1 Key Laboratory of Biopesticide and Chemical Biology (Ministry of Education), Fujian Agriculture and Forestry University, 350002 Fuzhou, China; e-mails: newugan@163.com; zljmeimei6@163.com
2 Key Laboratory of Integrated Pest Management for Fujian-Taiwan Crops, Ministry of Agriculture

To study the component and gene expressions of apoptosome in the mitochondrial-associated apoptotic pathway, cytochrome c and Apaf-1 were identified in the diamondback moth (DBM), Plutella xylostella, collected from Fuzhou, China. The full-length cDNA of cytochrome c comprised 873 bp, including a 327 bp ORF encoding a putative protein of 108 amino acids. Two full-length cDNAs of Apaf-1, Apaf-1a and Apaf-1b, were identified. Apaf-1a shared the same region of 5'-UTR (5'-untranslated region) (172 bp) and ORF (4,647 bp) of cDNA, but was 73 bp longer than Apaf-1b in the region of 3'-UTR of the cDNA. The ORF of Apaf-1a and Apaf-1b encoded a putative protein of 1,548 amino acids and shared 100% identity. No significant up-regulation of cytochrome c mRNA expression was found in both the chlorpyrifos-resistant (RR) and chlorpyrifos-susceptible (SS) DBM. Compared with the control (at 25°C for 3 h), mRNA transcript levels of Apaf-1a and Apaf-1b increased with the increase of temperature and were significantly higher at 37, 42, 47 and 50°C than at 25 and 33.5°C in RR DBM. However, the extent of up-regulation expression of Apaf-1a and Apaf-1b in SS DBM was slight under heat stress except at 42°C. In general, significantly higher increase in the mRNA transcript level of Apaf-1a and Apaf-1b was found in RR DBM than in SS DBM. It has been suggested that significantly higher expression of caspase-7 and lower biological fitness occurs in RR DBM under heat stress, a suggestion confirmed in our previous publications, and a result which might be associated with their higher up-regulation expression of Apaf-1a and Apaf-1b.

Keywords: Lepidoptera, Plutellidae, Plutella xylostella, diamondback moth, chlorpyrifos-resistant and -susceptible, cytochrome c, Apaf-1, fitness

Received: November 25, 2013; Accepted: April 25, 2014; Revised: April 25, 2014; Prepublished online: August 15, 2014; Published: October 1, 2014Show citation

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ZHANG, L.J., HUANG, J.F., CHEN, F., Yang YU, Z., Li WU, Z., & WU, G. (2014). Identifications of cytochrome c and Apaf-1 and their mRNA expressions under heat stress in insecticide-susceptible and -resistant Plutella xylostella (Lepidoptera: Plutellidae). Eur. J. Entomol.111(4), 457-468. doi: 10.14411/eje.2014.064.
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References

  1. Arnoult D., Parone P., Martinou J.C., Antonsson B., Estaquier J. & Ameisen J.C. 2002: Mitochondrial release of apoptosis-inducing factor occurs downstream of cytochrome c release in response to several proapoptotic stimuli. - J. Cell Biol. 159: 923-929 Go to original source...
  2. Barrett L.W., Fletcher S. & Wilton S.D. 2012: Regulation of eukaryotic gene expression by the untranslated gene regions and other non-coding elements. - Cell. Mol. Life Sci. 69: 3613-3634 Go to original source...
  3. Beumer T.L., Roepers-Gajadien H.L., Gademan L.S., Rutgers D.H. & De Rooij D.G. 1997: P21 (Cip1/WAF1) expression in the mouse testis before and after X irradiation. - Mol. Reprod. Devel. 47: 240-247 Go to original source...
  4. Cooper D.M. & Granville D.J. 2009: The insect caspases. - Apoptosis 14: 247-256 Go to original source...
  5. Cullen S.P. & Martin S.J. 2009: Caspase activation pathways: some recent progress. - Cell Death Differ. 16: 935-938 Go to original source...
  6. Di Giammartino D.C., Nishida K. & Manley J.L. 2011: Mechanisms and consequences of alternative polyadenylation. - Mol. Cell 43: 853-866 Go to original source...
  7. Dickson A.M. & Wilusz J. 2010: Polyadenylation: alternative lifestyles of the A-rich (and famous?). - EMBO J. 29: 1473-1474 Go to original source...
  8. Dorstyn L. & Kumar S. 2008: A biochemical analysis of the activation of the Drosophila caspase DRONC. - Cell Death Differ. 15: 461-470 Go to original source...
  9. Dorstyn L., Colussi P.A., Quinn L.M., Richardson H. & Kumar S. 1999: DRONC, an ecdysone-inducible Drosophila caspase. - Proc. Nat. Acad. Sci. U. S. A. 96: 4307-4312 Go to original source...
  10. Dorstyn L., Mills K., Lazebnik Y. & Kumar S. 2004: The two cytochrome c species, DC3 and DC4, are not required for caspase activation and apoptosis in Drosophila cells. - J. Cell Biol. 167: 405-410 Go to original source...
  11. Ellis H.M. & Horvitz H.R. 1986: Genetic control of programmed cell death in the nematode C. elegans. - Cell 44: 817-829 Go to original source...
  12. Facey C.O. & Lockshin R.A. 2010: The execution phase of autophagy associated PCD during insect metamorphosis. - Apoptosis 15: 639-652 Go to original source...
  13. Fadeel B., Ottosson A. & Pervaiz S. 2008: Big wheel keeps on turning: apoptosome regulation and its role in chemoresistance. - Cell Death Differ. 15: 443-452 Go to original source...
  14. Gu J., Huang L.X., Shen Y., Huang L.H. & Feng Q.L. 2012: Hsp70 and small Hsps are the major heat shock protein members involved in midgut metamorphosis in the common cutworm, Spodoptera litura. - Insect Mol. Biol. 21: 535-543 Go to original source...
  15. Hu Y., Benedict M.A., Wu D., Inohara N. & Nunez G. 1998: Bcl-XL interacts with Apaf-1 and inhibits Apaf-1-dependent caspase-9 activation. - Proc. Nat. Acad. Sci. U.S.A. 95: 4386-4391 Go to original source...
  16. Kanuka H., Sawamoto K., Inohara N., Matsuno K., Okano H. & Miura M. 1999: Control of the cell death pathway by Dapaf-1, a Drosophila Apaf-1/CED-4-related caspase activator. - Mol. Cell 4: 757-769 Go to original source...
  17. Kumar S. 2007: Caspase function in programmed cell death. - Cell Death Differ. 14: 32-43 Go to original source...
  18. Larionov A., Krause A. & Miller W. 2005: A standard curve based method for relative real time PCR data processing. - BMC Bioinform. 6: 62 Go to original source...
  19. Lee U., Rioflorido I., Hong S.W., Larkindale J., Waters E.R. & Vierling E. 2007: The Arabidopsis ClpB/Hsp100 family of proteins: chaperones for stress and chloroplast development. - Plant J. 49: 115-127 Go to original source...
  20. Liu L.J., Peng J.X., Liu K.Y., Yang H., Li Y. & Hong H.Z. 2007: Influence of cytochrome c on apoptosis induced by Anagrapha (Syngrapha) falcifera multiple nuclear polyhedrosis virus (AfMNPV) in insect Spodoptera litura cells. - Cell Biol. Int. 31: 996-1001 Go to original source...
  21. Liu F., Miyata T., Wu Z.J., Li C.W., Wu G., Zhao S.X. & Xie L.H. 2008: Effects of temperature on fitness costs, insecticide susceptibility and heat shock protein in insecticide-resistant and-susceptible Plutella xylostella. - Pestic. Biochem. Physiol. 91: 45-52 Go to original source...
  22. Liu K.Y., Shu D.Y., Song N., Gai Z.C., Yuan Y., Li J., Li M., Guo S.Y., Peng J.X. & Hong H.Z. 2012a: The role of cytochrome c on apoptosis induced by Anagrapha falcifera multiple nuclear polyhedrosis virus in insect Spodoptera litura cells. - PloS One 7: e40877 Go to original source...
  23. Liu K.Y., Yang H., Peng J.X. & Hong H.Z. 2012b: Cytochrome c and insect cell apoptosis. - Insect Sci. 19: 30-40 Go to original source...
  24. Lue Y.H., Hikim A.P., Swerdloff R.S., Im P., Taing K.S., Bui T., Leung A. & Wang C. 1999: Single exposure to heat induces stage-specific germ cell apoptosis in rats: role of intratesticular testosterone on stage specificity. - Endocrinology 140: 1709-1717 Go to original source...
  25. Malagoli D., Iacconi I., Marchesini E. & Ottaviani E. 2005: Cell-death mechanisms in the IPLB-LdFB insect cell line: a nuclear located Bcl-2-like molecule as a possible controller of 2-deoxy-D-ribose-mediated DNA fragmentation. - Cell Tiss. Res. 320: 337-343 Go to original source...
  26. Marek L. 2013: The role of the apoptosome in the activation of procaspase-9. - Postepy Hig. Med. Dosw. 67: 54-64 Go to original source...
  27. Mills K., Daish T., Harvey K.F., Pfleger C.M., Hariharan I.K. & Kumar S. 2006: The Drosophila melanogaster Apaf-1 homologue ARK is required for most, but not all, programmed cell death. - J. Cell Biol. 172: 809-815 Go to original source...
  28. Mohan M., Taneja T.K., Sahdev S., Mohareer K., Begum R., Athar M., Sah N.K. & Hasnain S.E. 2003: Antioxidants prevent UV-induced apoptosis by inhibiting mitochondrial cytochrome c release and caspase activation in Spodoptera frugiperda (Sf9) cells. - Cell Biol. Int. 27: 483-490 Go to original source...
  29. Proudfoot N.J. 2011: Ending the message: poly(A) signals then and now. - Genes Devel. 25: 1770-1782 Go to original source...
  30. Qi X., Wang L. & Du F.H. 2010: Novel small molecules relieve prothymosin alpha-mediated inhibition of apoptosome formation by blocking its interaction with Apaf-1. - Biochemistry 49: 1923-1930 Go to original source...
  31. Reubold T.F. & Eschenburg S. 2012: A molecular view on signal transduction by the apoptosome. - Cell. Signal. 24: 1420-1425 Go to original source...
  32. Reubold T.F., Wohlgemuth S. & Eschenburg S. 2011: Crystal structure of full-length Apaf-1: how the death signal is relayed in the mitochondrial pathway of apoptosis. - Structure 19: 1074-1083 Go to original source...
  33. Richburg J.H. 2000: The relevance of spontaneous- and chemically-induced alterations in testicular germ cell apoptosis to toxicology. - Toxicol. Lett. 112-113: 79-86 Go to original source...
  34. Riedl S.J. & Salvesen G.S. 2007: The apoptosome: signalling platform of cell death. - Nature Rev. Mol. Cell Biol. 8: 405-413 Go to original source...
  35. Rodriguez A., Oliver H., Zou H., Chen P., Wang X. & Abrams J.M. 1999: Dark is a Drosophila homologue of Apaf-1/CED-4 and functions in an evolutionarily conserved death pathway. - Nature Cell Biol. 1: 272-279
  36. Sahdev S., Taneja T.K., Mohan M., Sah N.K., Khar A.K., Hasnain S.E. & Athar M. 2003: Baculoviral p35 inhibits oxidant-induced activation of mitochondrial apoptotic pathway. - Biochem. Biophys. Res. Commun. 307: 483-490 Go to original source...
  37. Sandberg R., Neilson J.R., Sarma A., Sharp P.A. & Burge C.B. 2008: Proliferating cells express mRNAs with shortened 3' untranslated regions and fewer microRNA target sites. - Science 320: 1643-1647 Go to original source...
  38. Shan S.G., Liu K.Y., Peng J.X., Yao H.C., Li Y. & Hong H.Z. 2009: Mitochondria are involved in apoptosis induced by ultraviolet radiation in lepidopteran Spodoptera litura cell line. - Insect Sci. 16: 485-491 Go to original source...
  39. Srinivasula S.M., Ahmad M., Fernandes-Alnemri T. & Alnemri E.S. 1998: Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. - Mol. Cell 1: 949-957 Go to original source...
  40. Swanson M.S., Zieminn S.M., Miller D.D., Garber E.A.E. & Margoliash E. 1984: Developmental expression of nuclear genes that encode mitochondrial protiens: insect cytochromes c. - Proc. Nat. Acad. Sci. U.S.A. 82: 1964-1968 Go to original source...
  41. Tanaka S., Yoshizawa Y. & Sato R. 2012: Response of midgut epithelial cells to Cry1Aa is toxin-dependent and depends on the interplay between toxic action and the host apoptotic response. - FEBS J. 279: 1071-1079 Go to original source...
  42. Torkzadeh-Mahani M., Ataei F., Nikkhah M. & Hosseinkhani S. 2012: Design and development of a whole-cell luminescent biosensor for detection of early-stage of apoptosis. - Biosensors Bioelectr. 38: 362-368 Go to original source...
  43. Ujfaludi Z., Boros I.M. & Balint E. 2007: Different sets of genes are activated by p53 upon UV or ionizing radiation in Drosophila melanogaster. - Acta Biol. Hungar. 58: 65-79 Go to original source...
  44. Vera Y., Diaz-Romero M., Rodriguez S., Lue Y., Wang C., Swerdloff R.S. & Sinha Hikim A.P. 2004: Mitochondria-dependent pathway is involved in heat-induced male germ cell death: lessons from mutant mice. - Biol. Reprod. 70: 1534-1540 Go to original source...
  45. Vera Y., Erkkila K., Wang C., Nunez C., Kyttanen S., Lue Y., Dunkel L., Swerdloff R.S. & Sinha Hikim A.P. 2006: Involvement of p38 mitogen-activated protein kinase and inducible nitric oxide synthase in apoptotic signaling of murine and human male germ cells after hormone deprivation. - Mol. Endocrinol. 20: 1597-1609 Go to original source...
  46. Wang D.H., Hu J.R., Wang L.Y., Hu Y.J., Tan F.Q., Zhou H., Shao J.Z. & Yang W.X. 2012: The apoptotic function analysis of p53, Apaf1, Caspase3 and Caspase7 during the spermatogenesis of the Chinese fire-bellied newt Cynops orientalis. - PloS One 7: e39920 Go to original source...
  47. Wu G. & Jiang S.R. 2002: Field monitor of insecticide resistance and toxicological mechanism in Plutella xylostella. - Acta Phytophyl. Sin. 29: 351-355
  48. Xu J., Xu Z., Jiang Y., Qian X. & Huang Y. 2000: Cryptorchidism induces mouse testicular germ cell apoptosis and changes in bcl-2 and bax protein expression. - J. Environ. Pathol. Toxicol. Oncol. 19: 25-33
  49. Xu X.H., Hua Y.N., Zhang H.L., Wu J.C., Miao Y.Z., Han R., Gu Z.L. & Qin Z.H. 2007: Greater stress protein expression enhanced by combined prostaglandin A1 and lithium in a rat model of focal ischemia. - Acta Pharmacol. Sin. 28: 1097-1104 Go to original source...
  50. Yang X., Chang H.Y. & Baltimore D. 1998: Essential role of CED-4 oligomerization in CED-3 activation and apoptosis. - Science 281: 1355-1357 Go to original source...
  51. Yu X.C., Wang L., Acehan D., Wang X.D. & Akey C.W. 2006: Three-dimensional structure of a double apoptosome formed by the Drosophila Apaf-1 related killer. - J. Mol. Biol. 355: 577-589 Go to original source...
  52. Zhan S., Merlin C., Boore J.L. & Reppert S.M. 2011: The monarch butterfly genome yields insights into long-distance migration. - Cell 147: 1171-1185 Go to original source...
  53. Zhang J.Y., Pan M.H., Sun Z.Y., Huang S.J., Yu Z.S., Liu D., Zhao D.H. & Lu C. 2010: The genomic underpinnings of apoptosis in the silkworm, Bombyx mori. - BMC Genomics 11: 611 Go to original source...
  54. Zhou L., Song Z.W., Tittel J. & Steller H. 1999: HAC-1, a Drosophila homolog of APAF-1 and CED-4 functions in developmental and radiation-induced apoptosis. - Mol. Cell 4: 745-755 Go to original source...
  55. Zhuang H.M., Wang K.F., Liu Q., Liu F., Sun Z.Y., Zhou F., Wu G. & Zhao S.X. 2010: Effects of high temperature on life table parameters and the susceptibility to avermectin of progenies in insecticide-resistant and -susceptible of Plutella xylostella L. (Lepidoptera: Yponomeutidae). - Acta Entomol. Sin. 53: 741-747
  56. Zhuang H.M., Wang K.F., Miyata T., Wu Z.J., Wu G. & Xie L.H. 2011: Identification and expression of caspase-1 gene under heat stress in insecticide-susceptible and -resistant Plutella xylostella (Lepidoptera: Plutellidae). - Mol. Biol. Rep. 38: 2529-2539 Go to original source...
  57. Zimmermann K.C., Ricci J.E., Droin N.M. & Green D.R. 2002: The role of ARK in stress-induced apoptosis in Drosophila cells. - J. Cell Biol. 156: 1077-1087 Go to original source...
  58. Zou H., Henzel W.J., Liu X., Lutschg A. & Wang X. 1997: Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. - Cell 90: 405-413 Go to original source...

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