Hemocyte Density Increases with Developmental Stage in an Immune-Challenged Forest Caterpillar

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Stoepler, Teresa M ^a,b   Castillo, Julio C ^a   Lill, John T ^a   Eleftherianos, Ioannis ^a  

^a GEORGE WASHINGTON UNIVERSITY   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD CELL; BODY SIZE; CATERPILLAR; CELL DENSITY; CELLULAR IMMUNITY; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENOCYTOID; ESCHERICHIA COLI; EUCLEA DELPHINII; GRANULOCYTE; HEMATOPOIESIS; LITHACODES FASCIOLA; NONHUMAN; PHAGOCYTOSIS; PLASMA CELL; SPHERULOCYTE;

ANIMALS; BLOOD CELL COUNT; BODY SIZE; BUTTERFLIES; CELL COUNT; CELL SIZE; HEMOCYTES; LARVA; LIFE CYCLE STAGES; PHAGOCYTOSIS; TREES;

EID: 84881184735     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070978     Document Type: Article

References (47)

1. Tsakas S, Marmaras VJ, (2010) Insect immunity and its signalling: an overview. Invertebrate Survival Journal 7: 228-238.
2. Davis MM, Engstrom Y, (2012) Immune response in the barrier epithelia: Lessons from the fruit fly Drosophila melanogaster. Journal of Innate Immunity 4: 273-283.
3. Ganesan S, Aggarwal K, Paquette N, Silverman N, (2011) NF-kappa B/Rel proteins and the humoral immune responses of Drosophila melanogaster. Current topics in Microbiology and Immunology 349: 25-60.
4. Eleftherianos I, Revenis C, (2011) Role and importance of phenoloxidase in insect hemostasis. Journal of Innate Immunity 3: 28-33.
5. Loof TG, Schmidt O, Herwald H, Theopold U, (2011) Coagulation systems of invertebrates and vertebrates and their roles in innate immunity: The same side of two coins? Journal of Innate Immunity 3: 34-40.
6. Royet J, (2011) Epithelial homeostasis and the underlying molecular mechanisms in the gut of the insect model Drosophila melanogaster. Cellular and Molecular Life Sciences 68: 3651-3660.
7. Ryu JH, Ha EM, Lee WJ, (2010) Innate immunity and gut-microbe mutualism in Drosophila. Developmental and Comparative Immunology 34: 369-376.
8. Marmaras VJ, Lampropoulou M, (2009) Regulators and signalling in insect haemocyte immunity. Cellular Signalling 21: 186-195.
9. Crozatier M, Meister M, (2007) Drosophila haematopoiesis. Cellular Microbiology 9: 1117-1126.
10. Williams MJ, (2007) Drosophila hemopoiesis and cellular immunity. Journal of Immunology 178: 4711-4716.
11. Ribeiro C, Brehelin M, (2006) Insect haemocytes: What type of cell is that? Journal of Insect Physiology 52: 417-429.
12. Strand MR, (2008) The insect cellular immune response. Insect Science 15: 1-14.
13. Jiang H, Vilcinskas A, Kanost MR, (2010) Immunity in lepidopteran insects. Invertebrate Immunity 708: 181-204.
14. Wood W, Jacinto A, (2007) Drosophila melanogaster embryonic haemocytes: masters of multitasking. Nature Reviews Molecular Cell Biology 8: 542-551.
15. Hillyer JF, (2010) Mosquito immunity. Invertebrate Immunity 708: 218-238.
16. Gupta AP, Sutherland DJ, (1967) Phase contrast and histochemical studies of Spherule cells in cockroaches (Dictyoptera). Annals of the Entomological Society of America 60: 557-565.
17. Gupta AP, Han SS, (1988) Arthropod immune system. III. Septate junctions in the hemocytic capsule of the german cockroach, Blattella germanica. Tissue & Cell 20: 629-634.
18. Sait SM, Begon M, Thompson DJ, (1994) The influence of larval age on the response of Plodia interpunctella to a granulosis virus. Journal of Invertebrate Pathology 63: 107-110.
19. Tate AT, Rudolf VHW, (2012) Impact of life stage specific immune priming on invertebrate disease dynamics. Oikos 121: 1083-1092.
20. Kirkpatrick BA, Washburn JO, Volkman LE, (1998) AcMNPV pathogenesis and developmental resistance in fifth instar Heliothis virescens. Journal of Invertebrate Pathology 72: 63-72.
21. Sandland GJ, Minchella DJ, (2003) Costs of immune defense: an enigma wrapped in an environmental cloak? Trends in Parasitology 19: 571-574.
22. Kraaijeveld AR, Limentani EC, Godfray HCJ, (2001) Basis of the trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Proceedings of the Royal Society B-Biological Sciences 268: 259-261.
23. Bradley JE, Jackson JA, (2008) Measuring immune system variation to help understand host-pathogen community dynamics. Parasitology 135: 807-823.
24. Poulin R, (2007) Are there general laws in parasite ecology? Parasitology 134: 763-776.
25. Murphy SM, Lill JT, Epstein ME, (2011) Natural history of limacodid moths (Zygaenoidea) in the environs of Washington, D.C. Journal of the Lepidopterists' Society. 65: 137-152.
26. Lill JT, Marquis RJ, Forkner RE, Le Corff J, Holmberg N, et al. (2006) Leaf pubescence affects distribution and abundance of generalist slug caterpillars (Lepidoptera: Limacodidae). Environmental Entomology 35: 797-806.
27. Stoepler TM (2012) Bottom-up effects of habitat, host plant and herbivore quality on parasitoid host use. Ph.D. dissertation, George Washington University. 243 p.
28. Gates MW, Lill JT, Kula RR, O'Hara JE, Wahl DB, et al. (2012) Review of parasitoid wasps and flies (Hymenoptera, Diptera) associated with Limacodidae (Lepidoptera) in North America, with a key to genera. Proceedings of the Entomological Society of Washington 114: 24-110.
29. Stoepler TM, Lill JT, Murphy SM, (2011) Cascading effects of host size and host plant species on parasitoid resource allocation. Ecological Entomology 36: 724-735.
30. Strand MR, Pech LL, (1995) Immunological basis for compatability in parasitoid-host relationships. Annual Review of Entomology 40: 31-56.
31. Brodeur J, Vet LEM, (1995) Relationships between parasitoid host-range and host-defense- A comparative study of egg encapsulation in two related parasitoid species. Physiological Entomology 20: 7-12.
32. Vinson SB, (1990) How parasitoids deal with the immune system of their host: An overview. Archives of Insect Biochemistry and Physiology 13: 3-27.
33. Stireman JO, O'Hara JE, Wood DM, (2006) Tachinidae: Evolution, behavior, and ecology. Annual Review of Entomology 51: 525-555.
34. Laughton AM, Boots M, Siva-Jothy MT, (2011) Overview of parasitism associated effects on host haemocytes in larval parasitoids and comparison with effects of the egg-larval parasitoid Chelonus inanitus on its host Spodoptera littoralis. Journal of Insect Physiology 57: 1023-1032.
35. Gardiner EMM, Strand MR, (2000) Hematopoiesis in larval Pseudoplusia includens and Spodoptera frugiperda. Archives of Insect Biochemistry and Physiology 43: 147-164.
36. Wilson-Rich N, Dres ST, Starks PT, (2008) The ontogeny of immunity: Development of innate immune strength in the honey bee (Apis mellifera). Journal of Insect Physiology 54: 1392-1399.
37. Kacsoh BZ, Schlenke TA, (2012) High hemocyte load is associated with increased resistance against parasitoids in Drosophila suzukii, a relative of D. melanogaster. PloS One 7: e34721.
38. Stoepler TM, Castillo JC, Lill JT, Eleftherianos I, (2012) A simple protocol for extracting hemocytes from wild caterpillars. Journal of Visualized Experiments 69: e4173.
39. Kanost MR, Jiang HB, Yu XQ (2004) Innate immune responses of a lepidopteran insect, Manduca sexta. Immunological Reviews 198.
40. Beetz S, Holthusen TK, Koolman J, Trenczek T, (2008) Correlation of hemocyte counts with different developmental parameters during the last larval instar of the tobacco hornworm, Manduca sexta. Archives of Insect Biochemistry and Physiology 67: 63-75.
41. Nakahara Y, Kanamori Y, Kiuchi M, Kamimura M, (2010) Two hemocyte lineages exist in silkworm larval hematopoietic organ. Plos One 5: e11816.
42. Nakahara Y, Shimura S, Ueno C, Kanamori Y, Mita K, et al. (2009) Purification and characterization of silkworm hemocytes by flow cytometry. Developmental and Comparative Immunology 33: 439-448.
43. Regier JC, Zwick A, Cummings MP, Kawahara AY, Cho S, et al. (2009) Toward reconstructing the evolution of advanced moths and butterflies (Lepidoptera: Ditrysia): an initial molecular study. BMC Evolutionary Biology 280.
44. Lavine MD, Strand MR, (2002) Insect hemocytes and their role in immunity. Insect Biochemistry and Molecular Biology 32: 1295-1309.
45. Pech LL, Strand MR, (1995) Encapsulation of foreign targets by hemocytes of the moth Pseudoplusia includens (Lepidoptera: Noctuidae) involves an RGD-dependent cell adhesion mechanism. Journal of Insect Physiology 41: 481-488.
46. Vallet-Gely I, Lemaitre B, Boccard F, (2008) Bacterial strategies to overcome insect defences. Nature Reviews Microbiology 6: 302-313.
47. Asgari S, Rivers DB, (2011) Venom proteins from endoparasitoid wasps and their role in host-parasite interactions. Annual Review of Entomology 56: 313-335.