Impact of an Ectoparasite on the Immunity and Pathology of an Invertebrate: Evidence for Host Immunosuppression and Viral Amplification

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2005 May 18

PMID 15897457

Citations 187

Authors

Xiaolong Yang

Diana L Cox-Foster

Affiliations

Soon will be listed here.

Abstract

Varroa mites (Varroa destructor) are ectoparasites of honey bees (Apis mellifera) and cause serious damage to bee colonies. The mechanism of how varroa mites kill honey bees remains unclear. We have addressed the effects of the mites on bee immunity and the replication of a picorna-like virus, the deformed wing virus (DWV). The expression of genes encoding three antimicrobial peptides (abaecin, defensin, and hymenoptaecin) and four immunity-related enzymes (phenol oxidase, glucose dehydrogenase, glucose oxidase, and lysozyme) were used as markers to measure the difference in the immune response. We have demonstrated an example of an ectoparasite immunosuppressing its invertebrate host with the evidence that parasitization significantly suppressed expression of these immunity-related genes. Given that ticks immunosuppress their vertebrate hosts, our finding indicates that immunosuppression of hosts may be a common phenomenon in the interaction and coevolution between ectoparasites and their vertebrate and invertebrate hosts. DWV viral titers were significantly negatively correlated with the expression levels of the immunity-related enzymes. All bees had detectable DWV. Mite-infested pupae developed into adults with either normal or deformed wings. All of the deformed-wing bees were greatly infected by DWV (approximately 10(6) times higher than varroa-infested but normal-winged bees). Injection with heat-killed bacteria dramatically promoted DWV titers (10(5) times in 10 h) in the mite-infested, normal-winged bees to levels similar to those found in mite-infested, deformed-wing bees. Varroa mites may cause the serious demise of honey bees by suppressing bee immunity and by boosting the amplification of DWV in bees exposed to microbes.

Citing Articles

Avoiding the tragedies of parasite tolerance in Darwinian beekeeping.

Sokolov N, Boots M, Bartlett L Proc Biol Sci. 2025; 292(2040):20242433.

PMID: 39904384 PMC: 11793967. DOI: 10.1098/rspb.2024.2433.

Selection of Honey Bee () Genotypes for Three Generations of Low and High Population Growth of the Mite .

De la Mora A, Goodwin P, Emsen B, Kelly P, Petukhova T, Guzman-Novoa E Animals (Basel). 2024; 14(23).

PMID: 39682502 PMC: 11640491. DOI: 10.3390/ani14233537.

Leveraging Transcriptional Signatures of Diverse Stressors for Bumble Bee Conservation.

Quinlan G, Hines H, Grozinger C Mol Ecol. 2024; 34(3):e17626.

PMID: 39670295 PMC: 11754722. DOI: 10.1111/mec.17626.

Comparative Transcriptome Analysis of Cold Tolerance Mechanism in Honeybees ().

Shan J, Cheng R, Magaoya T, Duan Y, Chen C Insects. 2024; 15(10).

PMID: 39452366 PMC: 11508713. DOI: 10.3390/insects15100790.

and deformed wing virus interaction increases incidence of winter mortality in honey bee colonies.

Claing G, Dubreuil P, Bernier M, Ferland J, LHomme Y, Rodriguez E Can J Vet Res. 2024; 88(3):69-76.

PMID: 38988334 PMC: 11232088.

References

Equils O, Faure E, Thomas L, Bulut Y, Trushin S, Arditi M . Bacterial lipopolysaccharide activates HIV long terminal repeat through Toll-like receptor 4. J Immunol. 2001; 166(4):2342-7. DOI: 10.4049/jimmunol.166.4.2342. View

Schoeler G, Wikel S . Modulation of host immunity by haematophagous arthropods. Ann Trop Med Parasitol. 2002; 95(8):755-71. DOI: 10.1080/0003498012011118. View

Wikel S . Tick modulation of host immunity: an important factor in pathogen transmission. Int J Parasitol. 1999; 29(6):851-9. DOI: 10.1016/s0020-7519(99)00042-9. View

Ohashi K, Natori S, Kubo T . Expression of amylase and glucose oxidase in the hypopharyngeal gland with an age-dependent role change of the worker honeybee (Apis mellifera L.). Eur J Biochem. 1999; 265(1):127-33. DOI: 10.1046/j.1432-1327.1999.00696.x. View

Sulkowski M, Chaisson R, Karp C, Moore R, Margolick J, Quinn T . The effect of acute infectious illnesses on plasma human immunodeficiency virus (HIV) type 1 load and the expression of serologic markers of immune activation among HIV-infected adults. J Infect Dis. 1998; 178(6):1642-8. DOI: 10.1086/314491. View

Rotchford K, Strum A, Wilkinson D . Effect of coinfection with STDs and of STD treatment on HIV shedding in genital-tract secretions: systematic review and data synthesis. Sex Transm Dis. 2000; 27(5):243-8. DOI: 10.1097/00007435-200005000-00001. View

Casteels P, Ampe C, Jacobs F, Vaeck M, Tempst P . Apidaecins: antibacterial peptides from honeybees. EMBO J. 1989; 8(8):2387-91. PMC: 401180. DOI: 10.1002/j.1460-2075.1989.tb08368.x. View

Chen Y, Higgins J, Feldlaufer M . Quantitative real-time reverse transcription-PCR analysis of deformed wing virus infection in the honeybee (Apis mellifera L.). Appl Environ Microbiol. 2005; 71(1):436-41. PMC: 544241. DOI: 10.1128/AEM.71.1.436-441.2005. View

Gillespie J, Kanost M, Trenczek T . Biological mediators of insect immunity. Annu Rev Entomol. 1997; 42:611-43. DOI: 10.1146/annurev.ento.42.1.611. View

10.

Hoffmann J . The immune response of Drosophila. Nature. 2003; 426(6962):33-8. DOI: 10.1038/nature02021. View

11.

Sammataro D, Gerson U, Needham G . Parasitic mites of honey bees: life history, implications, and impact. Annu Rev Entomol. 2000; 45:519-48. DOI: 10.1146/annurev.ento.45.1.519. View

12.

Camazine , Liu . A putative iridovirus from the honey bee mite, varroa jacobsoni oudemans . J Invertebr Pathol. 1998; 71(2):177-8. DOI: 10.1006/jipa.1997.4713. View

13.

Souza Santos K, Santos L, Mendes M, de Souza B, Malaspina O, Palma M . Profiling the proteome complement of the secretion from hypopharyngeal gland of Africanized nurse-honeybees (Apis mellifera L.). Insect Biochem Mol Biol. 2004; 35(1):85-91. DOI: 10.1016/j.ibmb.2004.10.003. View

14.

Sano O, Kunikata T, Kohno K, Iwaki K, Ikeda M, Kurimoto M . Characterization of royal jelly proteins in both Africanized and European honeybees (Apis mellifera) by two-dimensional gel electrophoresis. J Agric Food Chem. 2004; 52(1):15-20. DOI: 10.1021/jf030340e. View

15.

Martin , Gunn . The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite varroa jacobsoni Oud . J Invertebr Pathol. 1999; 73(1):101-6. DOI: 10.1006/jipa.1998.4807. View

16.

De Gregorio E, Spellman P, Tzou P, Rubin G, Lemaitre B . The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO J. 2002; 21(11):2568-79. PMC: 126042. DOI: 10.1093/emboj/21.11.2568. View

17.

Casteels P, Ampe C, Jacobs F, Tempst P . Functional and chemical characterization of Hymenoptaecin, an antibacterial polypeptide that is infection-inducible in the honeybee (Apis mellifera). J Biol Chem. 1993; 268(10):7044-54. View

18.

Wikel S, Alarcon-Chaidez F . Progress toward molecular characterization of ectoparasite modulation of host immunity. Vet Parasitol. 2001; 101(3-4):275-87. DOI: 10.1016/s0304-4017(01)00556-8. View

19.

Ghassemi M, Asadi F, Andersen B, Novak R . Mycobacterium avium induces HIV upregulation through mechanisms independent of cytokine induction. AIDS Res Hum Retroviruses. 2000; 16(5):435-40. DOI: 10.1089/088922200309098. View

20.

Morishima I, Horiba T, Iketani M, Nishioka E, Yamano Y . Parallel induction of cecropin and lysozyme in larvae of the silkworm, Bombyx mori. Dev Comp Immunol. 1995; 19(5):357-63. DOI: 10.1016/0145-305x(95)00019-p. View