Differential expression of vitellogenin in honey bees (Apis mellifera) with different degrees of Nosema ceranae infection

Journal of Apicultural Research

Volumn 52, Issue 5, 2013, Pages 227-234

  Antúnez, Karina ^a   Mendoza, Yamandú ^b   Santos, Estela ^c   Invernizzi, Ciro ^c  

^a INSTITUTO DE INVESTIGACIONES BIOLÓGICAS CLEMENTE ESTABLE   (Uruguay)

^b INSTITUTO NACIONAL DE INVESTIGACIÓN AGROPECUARIA INIA   (Uruguay)

^c FACULTAD DE CIENCIAS   (Uruguay)

Author keywords

Apis mellifera; Immune response; Nosema ceranae; Real time PCR; Vitellogenin

Indexed keywords

EID: 84892778613     PISSN: 00218839     EISSN: 20786913     Source Type: Journal    
DOI: 10.3896/IBRA.1.52.5.09     Document Type: Article

References (45)

1. AMDAM, G V; OMHOLT, W (2003) The hive bee to forager transition in honey bee colonies: the double repressor hypothesis. Journal of Theoretical Biology 223: 451-464. http://dx.doi.org/10.1016/S0022-5193(03)00121-8
2. AMDAM, G V; NILSEN, K A; NORBERG, K; FONDRK, M K; HARTFELDER, K (2007) Variation in endocrine signaling underlies variation in social life history. The American Naturalist 170: 37-46. http://dx.doi.org/10.1086/518183
3. ANTUNEZ, K; MARTIN-HERNANDEZ, R; PRIETO, L; MEANA, A.; ZUNINO, P; HIGES, M (2009) Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environmental Microbiology 11: 2284-2290. http://dx.doi.org/10.1111/j.1462-2920.2009.01953.x
4. CASTEELS-JOSSON, K; ZHANG, W; CAPACI, T; CASTEELS, P; TEMPST, P; (1994) Acute transcriptional response of the honey bee peptide-antibiotics gene repertoire and required post-translational conversion of the precursor structures. The Journal of Biological Chemistry 269: 28569-28575.
5. CASTEELS, P; AMPE, C; JACOBS, F; TEMPST, P (1993) Functional and chemical characterization of Hymenoptaecin, an antibacterial poly-peptide that is infection-inducible in the honey bee (Apis me lifera). The Journal of Biological Chemistry 268: 7044-7054.
6. CASTEELS, P; AMPE, C; JACOBS, F; VAECK, M; TEMPST, P (1989) Apidaecins: antibacterial peptides from honey bees. The EMBO Journal 8: 2387-2391.
7. CASTEELS, P; AMPE, C; RIVIERE, L; VAN DAMME, J; ELICONE, C; FLEMING, M; JACOBS, F; TEMPST, P (1990) Isolation and characterization of abaecin, a major antibacterial response peptide in the honey bee (Apis mellifera). European Journal of Biochemistry 187: 381-386. http://dx.doi.org/10.1111/j.1432-1033. 1990.tb15315.x
8. CHAIMANEE, V; CHANTAWANNAKUL, P; CHEN, Y; EVANS, J D; PETTIS, J S (2012) Differential expression of immune genes of adult honey bee (Apis mellifera) after inoculated by Nosema ceranae. Journal of Insect Physiology 58 (8): 1090-1095. http://dx.doi.org/10.1016/j.jinsphys.2012.04.016
9. CHAIMANEE, V; PETTIS, J S; CHEN, Y; EVANS, J D; KHONGPHINITBUNJONG, K; CHANTAWANNAKUL, P (2013) Susceptibility of four different honey bee species to Nosema ceranae. Veterinary Parasitology 193(1-3): 260-265. http://dx.doi.org/10. 1016/j.vetpar.2012.12.004.
10. CHEN, Y P; HIGGINS, J A; FELDLAUFER, M F (2005) Quantitative Real-Time Reverse Transcription-PCR analysis of deformed wing virus infection in the honey bee (Apis mellifera L.) Applied and Environmental Microbiology 71: 436-441. http://dx.doi.org/10.1128/AEM.71.1.436-441.2005
11. CORONA, M; VELARDE, R; REMOLINA, S; MORAN-LAUTER, A; WANG, Y; HUGHES, K A; ROBINSON, G E (2007) Vitellogenin, juvenile hormone, insulin signalling, and queen honey bee longevity. Proceedings of the National Academy for Science 104: 7128-7133. http://dx.doi.org/10.1073/pnas.0701909104
12. COX-FOSTER, D L; CONLAN, S; HOLMES, E C; PALACIOS, G; EVANS, J D; MORAN, N A; QUAN, P L; BRIESE, T; HORNIG, M; GEISER, D M; MARTINSON, V; VANENGELSDORP, D; KALKSTEIN, A L; DRYSDALE, A; HUI, J; ZHAI, J; CUI, L; HUTCHISON, S K; SIMONS, J F; EGHOLM, M; PETTIS, J S; LIPKIN, W I (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318: 283-287. http://dx.doi.org/10.1126/science.1146498
13. DAFFRE, S; KLYSTEN, P; SAMAKOVLIS, C; HULTMARK, D (1994). The lysozyme locus in Drosophila melanogaster: an expanded gene family adapted for expression in the digestive tract. Molecular and General Genetics 194: 152-162.
14. EVANS, J D (2006) Beepath: an ordered quantitative-PCR array for exploring honey bee immunity and disease. Journal of Invertebrate Pathology 93: 135-139. http://dx.doi.org/10.1016/j.jip.2006.04.004
15. FORSGREN, E; FRIES, I (2010). Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Veterinary Parasitology 170: 212-217. http://dx.doi.org/10.1016/j.vetpar.2010.02.010
16. FRIES, I (2010) Nosema ceranae in European honey bees (Apis mellifera). Journal of Invertebrate Pathology 103: Suppl 1, S73-79. http://dx.doi.org/10. 1016/j.jip.2009.06.017
17. GILLESPIE, J P; KANOST, M R; TRENCZECK, T (1997) Biological mediators of insect immunity. Annual Review of Entomology 42: 611-643. http://dx.doi.org/10. 1146/annurev.ento.42.1.611
18. GUIDUGLI, K R; NASCIMENTO, A M; AMDAM, G V; BARCHUK, A R; OMHOLT, S W (2005) Vitellogenin regulates hormonal dynamics in the worker caste of a eusocial insect. FEBS Letters 579:4961-4965. http://dx.doi.org/10.1016/j. febslet.2005.07.085
19. HIGES, M; MARTIN-HERNÁNDEZ, R; MEANA, A (2006) Nosema ceranae, a new microsporidian parasite in honey bees in Europe. Journal of Invertebrate Pathology 92: 93-95. http://dx.doi.org/10.1016/j.jip.2006.02.005
20. HIGES, M; MARTIN-HERNÁNDEZ, R; MEANA, A (2010) Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie 41: 375-392. http://dx.doi.org/10.1051/apido/2010019
21. HIGES, M; MARTIN-HERNANDEZ, R; BOTIAS, C; BAILON, E G; GONZALEZ-PORTO, A V; BARRIOS, L; DEL NOZAL, M J; BERNAL, J L; JIMÉNEZ, J J; PALENCIA, P G; MEANA, A (2008) How natural infection by Nosema ceranae causes honey bee colony collapse. Environmental Microbiology 10: 2659-2669. http://dx.doi.org/10.1111/j. 1462-2920.2008.01687.x
22. INVERNIZZI, C; ANTÚNEZ, K; CAMPA, J P; HARRIET, J; MENDOZA, Y; SANTOS, E; ZUNINO, P (2011a). Sanitary situation of the Uruguayan honey bees. Veterinaria 181: 15-27.
23. INVERNIZZI, C; SANTOS, E; GARCÍA, E; DANERS, G; DI LANDRO, R; SAADOUN, A; CABRERA, C (2011b) Sanitary and nutritional characterization of honey bee colonies in Eucalyptus grandis plantations. Archivos de Zootecnia 60: 1303-1314.
24. INVERNIZZI, C; ABUD, C; TOMASCO, I H; HARRIET, J; RAMALLO, G; CAMPA, J; KATZ, H; GARDIOL, G; MENDOZA, Y (2009). Presence of Nosema ceranae in honey bees (Apis mellifera) in Uruguay. Journal of Invertebrate Pathology 101: 150-153. http://dx.doi.org/10.1016/j.jip.2009.03.006
25. KLEE, J; BESANA, A M; GENERSCH, E; GISDER, S; NANETTI, A; TAM, D Q; CHINH, T X; PUERTA, F; RUZ, J M; KRYGER, P; MESSAGE, D; HATJINA, F; KORPELA, S; FRIES, I; PAXTON, R J (2007) Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. Journal of Invertebrate Pathology 96: 1-10. http://dx.doi.org/10.1016/j.jip.2007.02.014
26. LAVINE, M D; STRAND, M R (2002) Insect haemocytes and their role in immunity. Insect Biochemistry and Molecular Biology 32: 1295-1309. http://dx.doi.org/10.1016/S0965-1748(02)00092-9
27. LOVALLO, N C; COX-FOSTER, D L (1999) Alteration in FAD glucose dehydrogenase activity and hemocyte behaviour contribute to initial disruption of Manduca sexta immune response to Cotesia congregata parasitoids. Journal of Insect Physiology 45: 1037-1048. http://dx.doi.org/10.1016/S0022-1910(99)00086-4
28. MARTIN-HERNANDEZ, R; MEANA, A; PRIETO, L; SALVADOR, A M; GARRIDO-BAILON, E; HIGES, M (2007) Outcome of colonization of Apis mellifera by Nosema ceranae. Applied and Environmental Microbiology 73: 6331-6338. http://dx.doi.org/10.1128/ AEM.00270-07
29. MARTIN-HERNANDEZ, R; BOTIAS, C; BARRIOS, L; MARTINEZ-SALVADOR, A; MEANA, A; MAYACK, C; HIGES, M (2011) Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honey bees (Apis mellifera). Parasitology Research 109: 605-612. http://dx.doi.org/10.1007/ s00436-011-2292-9
30. MAYACK, C; NAUG, D (2009) Energetic stress in the honey bee Apis mellifera from Nosema ceranae infection. Journal of Invertebrate Pathology 100: 185-188. http://dx.doi.org/10.1016/j.jip.2008.12.001
31. MENDOZA, Y; ANTÚNEZ, K; BRANCHICCELA, B; ANIDO, M; SANTOS, E; INVERNIZZI, C (2013) Nosema ceranae and RNA viruses in European and Africanized honeybee colonies (Apis mellifera) in Uruguay. Apidologie [In press].
32. MENDOZA, Y; HARRIET, J; CAMPA, J; KATZ, H; RAMALLO, G; DIAZ-CETTI, S; INVERNIZZI, C (2012) Control de Nosema ceranae en colonias de abejas (Apis mellifera) en forestaciones de Eucalyptus grandis. Agrociencia Uruguay 17(1): 108-113.
33. MGAP (2010) Decreto presidencial 14-6-2010. Oxitetraciclina y Fumagilina - Retiro y/o limitación uso en Uruguay. Available at: www.mgap.gub.uy.
34. NELSON, C M; IHLE, K E; FONDRK, M K; PAGE, R E; AMDAM, G V (2007) The gene vitellogenin has multiple coordinating effects on social organization. PloS Biology 5: 673-677. http://dx.doi.org/10.1371/journal.pbio.0050062
35. PAXTON, R J (2010) Does infection by Nosema ceranae cause "Colony Collapse Disorder," in honey bees (Apis mellifera). Journal of Apicultural Research 49: 80-84. http://dx.doi.org/10.3896/IBRA.1.49.1.11
36. PICKARD, R S; EL-SHEMY, A A M (1989) Seasonal variation in the infection of honey bee colonies with Nosema apis Zander. Journal of Apicultural Research 28: 93-100.
37. PORRINI, M; FERNÁNDEZ, N J; GARRIDO, P M; GENDE, L B; MEDICI, S K; EGUARAS, M J (2011) In vivo evaluation of antiparasitic activity of plant extracts on Nosema ceranae (Microsporidia). Apidologie 42: 700-707.
38. R DEVELOPMENT CORE TEAM (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.
39. PRISCO, G D; ZHANG, X; PENNACCHIO, F; CAPRIO, E; LI, J; EVANS, J D; DEGRANDI-HOFFMAN, G; HAMILTON, M; CHEN, Y P (2011) Dynamics of persistent and acute deformed wing virus infections in honey bees, Apis mellifera. Viruses 3: 2425-2441. http://dx.doi.org/10.3390/v3122425
40. REMOLINA, S C; HAFEZ, D M; ROBINSON, G E; HUGHES, K A (2007) Senescence in the worker honey bee Apis mellifera. Journal of Insect Physiology. 53: 1027-1033. http://dx.doi.org/10.1016/j.jinsphys.2007.05.015
41. RINDERER, T E (1976) Honey bees: individual feeding of large numbers of adults workers. Journal of Economic Entomology 69: 489-491.
42. SEEHUUS, S C; NORBERG, K; GIMSA, U; KREKLING, T; AMDAM, G V (2006) Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proceedings of the National Academy of Sciences 103: 962-967. http://dx.doi.org/10.1073/pnas.0502681103
43. WHEELER, D E; KAWOOYA, J K (1990) Purification and characterization of honey bee vitellogenin. Archives of Insect Biochemistry and Physiology 14: 73-79. http://dx.doi.org/10.1002/arch.940140405
44. WILLIAMS, G R; SAMPSON, M A; SHUTLER, D; ROGERS, R E (2008) Does fumagillin control the recently detected invasive parasite Nosema ceranae in western honey bees (Apis mellifera)? Journal of Invertebrate Pathology 99: 342-344. http://dx.doi.org/10.1016/j.jip.2008.04.005
45. YANG, X; COX-FOSTER, D (2007) Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge. Parasitology 134: 405-412. http://dx.doi.org/10.1017/S0031182006000710