Skip to main content
SpringerLink
Log in

Nitric oxide participates at the first steps of Apis mellifera cellular immune activation in response to non-self recognition

  • Original article
  • Published:
Apidologie Aims and scope Submit manuscript

Abstract

The honey bee Apis mellifera (Hymenoptera) is being affected by many diseases. The elimination of organisms in the insect hemocoel requires hemocytes recognition and response to the invader. After recognizing a surface as “foreign,” hemocytes “spread.” Spreading on glass surfaces by insect hemocytes is used as a measure of immune activation. Nitric oxide (NO) is a signaling and immune effector molecule in response to microbial infection that has been proposed as a key molecule in invertebrate immunity. The participation of NO in the hemocytic response of A. mellifera upon recognition of non-self is herein analyzed. Glass-adherent hemocytes produce large amounts of NO. Treatment with NO donor sodium nitroprusside enhanced hemocyte spreading, while NO scavenger carboxyPTIO reduced hemocyte immune activation. These results are indicative of NO participation at the beginning of A. mellifera immune response to non-self.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.

Similar content being viewed by others

References

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Davies, S., Dow, J. (2009) Modulation of epithelial innate immunity by autocrine production of nitric oxide. Gen. Comp. Endocrinol. 162, 113–121

    Article  PubMed  CAS  Google Scholar 

  • Dean, P., Richards, E.H., Edwards, J.P., Reynolds, S.E., Charnley, K. (2004) Microbial infection causes the appearance of hemocytes with extreme spreading ability in monolayers of the tobacco hornworm Manduca sexta. Dev. Comp. Immunol. 28, 689–700

    Article  PubMed  CAS  Google Scholar 

  • Dietemann, V., Pflugfelder, J., Anderson, D., Charrière, J.D., Chejanovsky, N., et al. (2012) Varroa destructor: research avenues towards sustainable control. J Apic Res 51, 125–132

    Article  Google Scholar 

  • Eleftherianos, I., Xu, M., Yadi, H., Ffrench-Constant, R.H., Reynolds, S.E. (2009) Plasmatocyte-spreading peptide (PSP) plays a central role in insect cellular immune defences against bacterial infection. J. Exp. Biol. 212, 1840–1848

    Article  PubMed  CAS  Google Scholar 

  • Hendriksma, H.P., Hartel, S., Steffan-Dewenter, I. (2011) Honey bee risk assessment: new approaches for in vitro larvae rearing and data analyses. Met. Ecol. Evol.. doi:10.1111/j.2041-210X.2011.00099.x

    Google Scholar 

  • Hillyer, J., Estévez-Lao, T. (2010) Nitric oxide is an essential component of the hemocyte-mediated mosquito immune response against bacteria. Dev. Comp. Immunol. 34, 141–149

    Article  PubMed  CAS  Google Scholar 

  • Gillespie, J.P., Kanost, M.R. (1997) Biological mediators of insect immunity. Annu. Rev. Entomol. 42, 611–643

    Article  PubMed  CAS  Google Scholar 

  • Levy, S. (2012) What’s best for bees. Nature 479, 164–165

    Article  Google Scholar 

  • Ling, E., Yu, X. (2005) Prophenoloxidase binds to the surface of hemocytes and is involved in hemocyte melanization in Manduca sexta. Insect Biochem. Mol. Biol. 35, 1356–1366

    Article  PubMed  CAS  Google Scholar 

  • Mandato, C.A., Diehl-Jones, W., Moore, S.J., Downer, R.G.H. (1996) The effects of eicosanoid biosynthesis inhibitors on prophenoloxidase activation. phagocytosis and cell spreading in Galleria mellonella. J. Insect Physiol. 43, 1–8

    Article  Google Scholar 

  • Marmaras, V.J., Lampropoulou, M. (2009) Regulators and signalling in insect haemocyte immunity. Cell. Signal. 21, 186–195

    Article  PubMed  CAS  Google Scholar 

  • Martin, S.J., Highfield, A.C., Brettell, L., Villalobos, E.M., Budge, G.E., Powell, M., Nikaido, S., Schroeder, D.C. (2012) Global honey bee viral landscape altered by a parasitic mite. Science 336, 1304

    Article  PubMed  CAS  Google Scholar 

  • Müller, U., Hildebrandt, H. (1995) The nitric oxide cGMP system in the antennal lobe of Apis mellifera is implicated in integrative processing of chemosensory stimuli. Europ. J. Neurosci 7, 2240–2248

    Article  Google Scholar 

  • Müller, U. (1996) Inhibition of nitric oxide synthase impairs a distinct form of long-term memory in the honeybee, Apis mellifera. Neuron 16, 541–549

    Article  PubMed  Google Scholar 

  • Müller, U., Hildebrandt, H. (2002) Nitric oxide/cGMP-mediated protein kinase A activation in the antennal lobes plays an important role in appetitive reflex habituation in the honeybee. J. Neurosci. 22, 8739–8747

    PubMed  Google Scholar 

  • Nardi, J.B., Pilas, B., Bee, M.C., Zhuang, S., Garsha, K., Kanost, M.R. (2006) Neuroglian-positive plasmatocytes of Manduca sexta and the initiation of hemocyte attachment to foreign surfaces. Dev. Comp. Immunol. 30, 47–462

    Article  Google Scholar 

  • Negri P., Maggi D., Lamattina L., Eguaras M. J. (2012a) Nitric oxide participation in Apis mellifera hemocytic immune activation upon recognition of non-self and encapsulation. 2012 International Congress on Invertebrate Pathology and Microbial Control and 45th Annual Meeting of the Society for Invertebrate Pathology, August 9, Buenos Aires, Argentina.

  • Negri P., Maggi M. D., Fernandez N., Lamattina L., Eguaras M. J. (2012b) Apis mellifera cellular immune responses in-vitro: qualitative differences before and after the puppae metamorphosis black box. 2012 International Congress on Invertebrate Pathology and Microbial Control and 45th Annual Meeting of the Society for Invertebrate Pathology, August 9, Buenos Aires, Argentina, DBI-06, page 57

  • Pech, L.L., Strand, M.R. (1995) Encapsulation of foreign targets by hemocytes of the moth Pseudoplusia inchdens (Lepidoptera: Noctuidae) involves an RGD-dependent cell adhesion mechanism. J. Insect Physiol. 41, 481–488

    Article  CAS  Google Scholar 

  • Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O., Kunin, W.E. (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 26, 345–353

    Article  Google Scholar 

  • Rivero, A. (2006) Nitric oxide: an antiparasitic molecule of invertebrates. Trends Parasitol. 22, 219–225

    Article  PubMed  CAS  Google Scholar 

  • Rosenkranz, P., Aumeier, P., Ziegelmann, B. (2010) Biology and control of Varroa destructor. J. Invertebr. Pathol. 103, 96–119

    Article  Google Scholar 

  • Strand, M.R. (2008) The insect cellular immune response. Insect Sci 15, 1–14

    Article  CAS  Google Scholar 

  • Tojo, S., Naganuma, F., Arakawa, K., Yokoo, S. (2000) Involvement of both granular cells and plasmatocytes in phagocytic reactions in the greater wax moth, Galleria mellonella. J. Insect Physiol 46, 1129–1135

    Article  PubMed  CAS  Google Scholar 

  • Whitten, M.M.A., Tew, I.F., Lee, B.L., Ratcliffe, N.A. (2004) A novel role for an insect apolipoprotein (apolipophorin III) in β-1,3-glucan pattern recognition and cellular encapsulation reactions. J. Immunol. 172, 2177–2185

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by “ANPCyT,” Argentina (PICT Redes 2006 no. 00890 Nodo 01 and PICT 2011 2383). The authors would like to thank CONICET and the UNMdP. Pedro Negri is a doctoral fellow from CONICET, Argentina. The authors are very grateful to Dr. Claudia Studdert for E. coli strain and to Lic. Leonardo De Feudis for beekeeping support.

Author information

Authors and Affiliations

  1. Laboratorio de Artrópodos, Universidad Nacional de Mar del Plata (UNMdP), Mar del Plata, Argentina

    Pedro Negri, Matías Maggi, Constanza Brasesco & Martín Eguaras

  2. Instituto de Investigaciones Biológicas-CONICET, Universidad Nacional de Mar del Plata, Mar del Plata, Argentina

    Natalia Correa-Aragunde & Lorenzo Lamattina

  3. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

    Pedro Negri, Matías Maggi, Natalia Correa-Aragunde, Martín Eguaras & Lorenzo Lamattina

  4. Facultad de Cs Exactas y Naturales, nivel 0, Funes 3350, Mar del Plata, 7600, Argentina

    Pedro Negri

Authors
  1. Pedro Negri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matías Maggi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natalia Correa-Aragunde
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Constanza Brasesco
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Martín Eguaras
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lorenzo Lamattina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pedro Negri.

Additional information

Manuscript editor: Klaus Hartfelder

L’oxyde nitrique intervient dans les premières étapes de la réponse immunitaire cellulaire d’ Apis mellifera à la reconnaissance du non-soi

Apidae/ immunité / oxyde nitrique/ infection

Stickstoffmonoxid spielt eine Rolle in den ersten Schritten der Aktivierung der zellulären Immunantwort bei Apis mellifera

Apis mellifera / Immunität/ Stickstoffmonoxid

M. Eguaras and L. Lamattina contributed equally as senior authors.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Negri, P., Maggi, M., Correa-Aragunde, N. et al. Nitric oxide participates at the first steps of Apis mellifera cellular immune activation in response to non-self recognition. Apidologie 44, 575–585 (2013). https://doi.org/10.1007/s13592-013-0207-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-013-0207-8

Keywords

Search

Navigation