Korean journal of applied entomology (한국응용곤충학회지)

Korean Society of Applied Entomology (한국응용곤충학회)
권호 표지
DOI QR코드

DOI QR Code

Change in Hemocyte Populations of the Beet Armyworm, Spodoptera exigua, in Response to Bacterial Infection and Eicosanoid Mediation

세균 감염에 따른 파밤나방 혈구 밀도 변화와 아이코사노이드 중개 역할

  • Park, Jiyeong (Department of Bioresource Sciences, Andong National University) ;
  • Kim, Yonggyun (Department of Bioresource Sciences, Andong National University)
  • 박지영 (안동대학교 자연과학대학 생명자원과학과) ;
  • 김용균 (안동대학교 자연과학대학 생명자원과학과)
  • Received : 2012.06.15
  • Accepted : 2012.09.16
  • Published : 2012.12.01
Download PDF
⟨ Previous Next ⟩

Abstract

Eicosanoid mediates various cellular immune responses in insects. This study aimed to discover its novel action on the modulation of hemocyte populations in response to an immune challenge. Upon bacterial challenge, the last instar larvae of the beet armyworm, Spodoptera exigua, increased their total hemocyte density in 2 h, and then decreased it to a basal hemocyte density level. This rapid increase in total hemocyte density was explained by an increase of plasmatocyte and spherulocyte densities. When larvae were treated with dexamethasone (a specific phospholipase $A_2$ ($PLA_2$) inhibitor), they did not show any increase in hemocyte density in response to bacterial challenge. However, the addition of arachidonic acid (a catalytic product of $PLA_2$) to larvae treated with dexamethasone recovered the up-regulation of hemocyte density in response to bacterial infection. Among eicosanoid, cyclooxygenase (COX), but not lipoxygenase (LOX), products seemed to mediate the increase of hemocyte density in response to bacterial infection because naproxene (a COX inhibitor) inhibited the hemocyte density increase, though esculetin (a LOX inhibitor) did not. Prostaglandin $E_2$, a COX product, significantly increased the hemocyte density even without bacterial infection. These results suggest that eicosaniod mediates a rapid increase in total hemocyte density in response to immune challenge.

아이코사노이드는 곤충의 다양한 세포성 면역 반응을 중개한다. 본 연구는 면역반응에 따라 혈구세포 밀도 변화에 대한 아이코사노이드의 새로운 중개 기능을 밝히기 위해 수행되었다. 파밤나방(Spodoptera exigua) 5령충은 세균 감염에 따라 2 시간이 지나면 총혈구수의 현격한 증가를 보였다. 이 총혈구수 증가는 주로 부정형혈구와 소구형혈구 밀도의 증가로 해석되었다. 파밤나방 유충에 phospholipase $A_2$ ($PLA_2$) 억제자인 dexamethasone을 처리하면 세균 처리에 의한 총혈구수 변화가 일어나지 않았다. 하지만 dexamethasone을 처리한 유충에 $PLA_2$의 촉매산물인 arachidonic acid를 첨가하면 총혈구수 증가가 회복되었다. 이러한 혈구 밀도 변화에 원인으로서 아이코사노이드 종류를 추적하기 위해 cyclooxygenase (COX)의 억제자인 naproxene을 처리한 결과 총혈구수 증가가 억제되고, lipoxygenase (LOX)의 억제자인 esculetin을 처리하면 총혈구수 증가가 유지되어 COX 산물이 세균 침입에 따른 총혈구수 증가에 관여하는 것으로 나타났다. COX의 생산물인 prostaglandin $E_2$ ($PGE_2$)를 세균 없이 단독으로 처리할 때도 총혈구수의 뚜렷한 증가를 나타냈다. 이러한 결과는 파밤나방의 세포성 면역반응 과정에서 총혈구수 증가를 중개하는 아이코사노이드의 새로운 기능을 제시하고 있다.

Keywords

References

  1. Baines, D., Downer, R.G., 1994. Octopamine enhances phagocytosis in cockroach hemocytes: involvement of inositol triphosphate. Arch. Insect Biochem. Physiol. 26, 249-261. https://doi.org/10.1002/arch.940260402
  2. Beckage, N.E., 2008. Insect immunology. Academic Press, New York.
  3. Beetz, S., Holthusen, T.K., Koolman, J., Trenczek, T., 2008. Correlation of hemocyte counts with different developmental parameters during the last larval instar of the tobacco hornworm, Manduca sexta. Arch. Insect Biochem. Physiol. 67, 63-75. https://doi.org/10.1002/arch.20221
  4. Burke, J.E., Dennis, E.A., 2009. Phospholipase $A_{2}$ structure /function, mechanism and signaling. J. Lipid Res. 50, S237-S242.
  5. Buyukguzel, E., Tunaz, H., Stanley D., Buyukguzel, K., 2007. Eicosanoids mediate Galleria mellonella cellular immune response to viral infection. J. Insect Physiol. 53, 99-105. https://doi.org/10.1016/j.jinsphys.2006.10.012
  6. Clark, K.D., Pech, L.L., Strand, M.R., 1997. Isolation and identification of a plasmatocyte-spreading peptide from the hemolymph of the lepidopteran insect Pseudoplusia includens. J. Biol. Chem. 272, 23440-23447. https://doi.org/10.1074/jbc.272.37.23440
  7. Gardiner, E.M.M., Strand, M.R., 2000. Hematopoiesis in larval Pseudoplusia includens and Spodoptera frugiperda. Arch. Insect Biochem. Physiol. 43, 147-164. https://doi.org/10.1002/(SICI)1520-6327(200004)43:4<147::AID-ARCH1>3.0.CO;2-J
  8. Gillespie, J.P., Kanost, M.R., Trenczek, T., 1997. Biological mediators of insect immunity. Annu. Rev. Entomol. 42, 611-643. https://doi.org/10.1146/annurev.ento.42.1.611
  9. Goh, H.G., Lee, S.G., Lee, B.P., Choi, G.M., Kim, J.H., 1990. Simple mass-rearing of beet armyworm, Spodoptera exigua. Kor. J. Appl. Entomol. 29, 180-183.
  10. Huang, F., Yang, Y.Y., Shi, M., Li, J.Y., Chen, Z.Q., Chen, F.S., Chen, X.X., 2010. Ultrastructural and functional characterization of circulating hemocytes from Plutella xylostella larva: cell types and their role in phagocytosis. Tissue Cell 42, 360-364. https://doi.org/10.1016/j.tice.2010.07.012
  11. Jurenka, R.A., Pedibhotla, V.K., Stanley, D.W., 1999. Prostaglandin production in response to bacterial infection in true armyworm larvae. Arch. Insect Biochem. Physiol. 41, 225-232. https://doi.org/10.1002/(SICI)1520-6327(1999)41:4<225::AID-ARCH6>3.0.CO;2-0
  12. Kim, G., Kim, Y., 2010. Up-regulation of circulating hemocyte population in response to bacterial challenge is mediated by octopamine and 5-hydroxytryptamine via Rac1 signal in Spodoptera exigua. J. Insect Physiol. 56, 559-566. https://doi.org/10.1016/j.jinsphys.2009.11.022
  13. Kim, K., Madanagopal, N., Lee, D., Kim, Y., 2009. Octopamine and 5-hydroxytryptamine mediate hemocytic phagocytosis and nodule formation via eicosanoids in the beet armyworm, Spodoptera exigua. Arch. Insect Biochem. Physiol. 70, 162-176. https://doi.org/10.1002/arch.20286
  14. Kim, J., Nalini, M., Kim, Y., 2008. Immunosuppressive activity of cultured broth of entomopathogenic bacteria on the beet armyworm, Spodoptera exigua, and their mixture effects with BT biopesticide on insecticidal pathogenicity. Kor. J. Pestic. Sci. 12, 184-191.
  15. Lavine, M.D., Strand, M.R., 2002. Insect hemocytes and their role in cellular immune responses. Insect Biochem. Mol. Biol. 32, 1237-1242.
  16. Lord, J.C., Anderson, S., Stanley, D.W., 2002. Eicosanoids mediate Manduca sexta cellular response to the fungal pathogen Beauveria bassiana: a role for the lipoxygenase pathway. Arch. Insect Biochem. Physiol. 51, 46-54. https://doi.org/10.1002/arch.10049
  17. Markus, R., Laurinyecz, B., Kurucz, E., Honti, V., Bajusz, I., Sipos, B., Somogyi, K., Kronhamn, K., Hultmark, J., Ando, D.I., 2009. Sessile hemocytes and hematopoietic compartment in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 106, 4805-4809. https://doi.org/10.1073/pnas.0801766106
  18. Merchant, D., Ertl, R., Rennard, S.I., Stanley, D.W., Miller, J.S., 2008. Eicosanoids mediate insect hemocyte migration. J. Insect Physiol. 54, 215-221. https://doi.org/10.1016/j.jinsphys.2007.09.004
  19. Miller, J.S., Nguyen, T., Stanley-Samuelson, D.W., 1994. Eicosanoids mediate insect nodulation responses to bacterial infections. Proc. Natl. Acad. Sci. USA 91, 12418-12422. https://doi.org/10.1073/pnas.91.26.12418
  20. Morishima, I., Yamano, Y., Inoue, K., Matsu, N., 1997. Eicosanoid mediate induction of immune genes in the fat body of the silkworm, Bombyx mori. FEBS Lett. 419, 83-86. https://doi.org/10.1016/S0014-5793(97)01418-X
  21. Park, J., Kim, Y., 2012. Eicosanoid biosynthesis is activated via Toll, but not Imd signal pathway. J. Invertebr. Pathol. 110, 382-388. https://doi.org/10.1016/j.jip.2012.04.015
  22. Riddiford, L.M., 1991. Hormonal control of sequential gene expression in insect epidermis, in: Binnington, K., Retnakaran, A. (Eds.), Physiology of the insect epidermis. CSIRO, Melbourne, Australia, pp. 46-54.
  23. SAS Institute, Inc., 1989. SAS/STAT user's guide, Release 6.03, Ed. Cary, N.C.
  24. Shrestha, S., Kim, Y., 2007. An entomopathogenic bacterium, Xenorhabdus nematophila, inhibits hemocyte phagocytosis of Spodoptera exigua by inhibiting phospholipase $A_{2}$. J. Invertebr. Pathol. 96, 64-70. https://doi.org/10.1016/j.jip.2007.02.009
  25. Shrestha, S., Kim, Y., 2008. Eicosanoids mediate prophenoloxidase release from oenocytoids in the beet armyworm, Spodoptera exigua. Insect Biochem. Mol. Biol. 38, 99-112. https://doi.org/10.1016/j.ibmb.2007.09.013
  26. Shrestha, S., Stanley, D., Kim, Y., 2011. PGE2 induces oenocytoid cell lysis via a G protein-coupled receptor in the beet armyworm, Spodoptera exigua. J. Insect Physiol. 57, 1568-1576. https://doi.org/10.1016/j.jinsphys.2011.08.010
  27. Stanley, D.W., 2005. Eicosanoids. in: Gilbert, L.L., Iatrou, K., Gill, S.S. (Eds.), Comprehensive insect molecular science. Vol. 4. Elsevier, Amsterdam, The Netherlands, pp. 307-339.
  28. Stanley, D.W., 2006. Prostaglandins and other eicosanoids in insects: biological significance. Annu. Rev. Entomol. 51, 25-44. https://doi.org/10.1146/annurev.ento.51.110104.151021
  29. Stanley, D.W., 2011. Eicosanoids: progress towards manipulating insect immunity. J. Appl. Entomol. 135, 534-545. https://doi.org/10.1111/j.1439-0418.2010.01612.x
  30. Stanley, D., Kim, Y., 2011. Prostaglandins and their receptors in insect biology. Front. Endocrinol. 2, 1-11.
  31. Tunaz, H., Park, Y., Buyukguzel, K., Bedick, J.C., Nor Aliza, A.R., Stanley, D.W., 2003. Eicosanoids in insect immunity: bacterial infection stimulates hemocytic phospholipase A2 activity in tobacco hornworms. Arch. Insect Biochem. Physiol. 52, 1-6. https://doi.org/10.1002/arch.10056
  32. Wolfgang, W.J., Riddiford, L.M., 1986. Larval cuticular morphogenesis in the tobacco hornworm, Manduca sexta, and its hormonal regulation. Dev. Biol. 113, 305-316. https://doi.org/10.1016/0012-1606(86)90166-1
  33. Yajima, M., Takada, M., Takahashi, N., Kikuchi, H., Natori, S., Oshima, Y., Kurata, S., 2003. A newly established in vitro culture using transgenic Drosophila reveals functional coupling between the phospholipase $A_{2}$-generated activation of the immune deficiency (imd) pathway in insect immunity. Biochem. J. 371, 205-210. https://doi.org/10.1042/BJ20021603
  34. Yu, X.Q., Zhu, Y.F., Ma, C., Fabrick, J.A., Kanost, M.R., 2002. Pattern recognition proteins in Manduca sexta plasma. Insect Biochem. Mol. Biol. 32, 1287-1293. https://doi.org/10.1016/S0965-1748(02)00091-7

Cited by

  1. Cellular Immune Response of the Legume Pod Borer, Maruca vitrata, and its Suppression by BtPlus to Enhance Bacillus thuringiensis Pathogenicity vol.21, pp.2, 2017, https://doi.org/10.7585/kjps.2017.21.2.150
  2. An entomopathogenic bacterium, Xenorhabdus hominickii ANU101, produces oxindole and suppresses host insect immune response by inhibiting eicosanoid biosynthesis vol.145, 2017, https://doi.org/10.1016/j.jip.2017.03.004
  3. Specific inhibition of Xenorhabdus hominickii , an entomopathogenic bacterium, against different types of host insect phospholipase A 2 vol.149, 2017, https://doi.org/10.1016/j.jip.2017.08.009
  4. A novel calcium-independent phospholipase A 2 and its physiological roles in development and immunity of a lepidopteran insect, Spodoptera exigua vol.77, 2017, https://doi.org/10.1016/j.dci.2017.08.014
  5. PROSTAGLANDIN MEDIATES DOWN-REGULATION OF PHENOLOXIDASE ACTIVATION OFSpodoptera exiguaVIA PLASMATOCYTE-SPREADING PEPTIDE-BINDING PROTEIN vol.85, pp.4, 2014, https://doi.org/10.1002/arch.21156
  6. Nitric oxide mediates antimicrobial peptide gene expression by activating eicosanoid signaling vol.13, pp.2, 2018, https://doi.org/10.1371/journal.pone.0193282