Skip to main content
SpringerLink
Log in

Apis mellifera hemocytes generate increased amounts of nitric oxide in response to wounding/encapsulation

Apidologie Aims and scope Submit manuscript

Cite this article

A Correction to this article was published on 16 July 2019

This article has been updated

Abstract

Apis mellifera populations are being threatened by several pathogens and parasitosis. Several authors have proposed that honey bee colonies may suffer from a compromised immune system leading to colony loss. This is why the study of A. mellifera immune system has become a topic of pressing concern. Nitric oxide (NO) is a signaling and immune effector molecule that has been proposed as a key molecule in invertebrate immunity, and that plays a part in A. mellifera cellular defenses. This paper deals with NO participation in the response to wounding/encapsulation challenge in A. mellifera fifth instar (L5) larvae. Challenging A. mellifera L5 larvae with nylon implants enhanced NO production and spreading in granulocyte-like hemocytes and increased the number of this NO-producing hemocyte type. However, AmNOS expression levels were not influenced by the insult. These results reveal that NO participates in the wound healing/encapsulation response as a signal molecule, possibly by the activation of a constitutively expressed AmNOS in honey bees.

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.

Change history

  • 16 July 2019

    This correction stands to correct the last sentence found in the caption of Figure 2 where it reads, ���Three independent experiments were performed and a total of 18 larvae per treatment were analyzed.���

  • 16 July 2019

    This correction stands to correct the last sentence found in the caption of Figure 2 where it reads, ���Three independent experiments were performed and a total of 18 larvae per treatment were analyzed.���

References

  • Alaux, C., Ducloz, F., Crauser, D., Le Conte, Y. (2010) Diet effects on honey bee immunocompetence. Biol. Lett. 6, 562–565. doi:10.1098/rsbl.2009.0986

    Article  PubMed Central  PubMed  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  CAS  PubMed  Google Scholar 

  • Frank, S., Kämpfer, H., Wetzler, C., Pfeilschifter, J. (2002) Nitric oxide drives skin repair: novel functions of an established mediator. Kidney Int. 61, 882–888

    Article  CAS  PubMed  Google Scholar 

  • Gätschenberger, H., Azzami, K., Tautz, J., Beier, H. (2013) Antibacterial immune competence of honey bees (Apis mellifera) is adapted to different life stages and environmental risks. PLoS ONE 8(6), e66415. doi:10.1371/journal.pone.0066415

    Article  PubMed Central  PubMed  Google Scholar 

  • Gregorc, A., Evans, J.D., Scharf, M., James, D., Ellis, J.D. (2012) Gene expression in honey bee (Apis mellifera) larvae exposed to pesticides and Varroa mites (Varroa destructor). J. Insect Physiol. 58, 1042–1049

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Jefferson, J., Dolstad, H., Sivalingam, M., Snow, J. (2013) Barrier immune effectors are maintained during transition from nurse to forager in the honey bee. PLoS ONE 8(1), e54097. doi:10.1371/journal.pone.0054097

    Article  CAS  PubMed Central  PubMed  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  CAS  PubMed  Google Scholar 

  • Moreno-García, M., Córdoba-Aguilar, A., Condé, R., Lanz-Mendoza, H. (2013) Current immunity markers in insect ecological immunology: assumed trade-offs and methodological issues. Bull. Entomol. Res. 103, 127–139

    Article  PubMed  Google Scholar 

  • Nappi, A., Christensen, B. (2005) Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochem. Mol. Biol. 35, 443–459

    Article  CAS  PubMed  Google Scholar 

  • Negri, P., Maggi, M., Correa-Aragunde, N., Brasesco, C., Eguaras, M., Lamattina, L. (2013) Nitric oxide participates at the first steps of Apis mellifera cellular immune activation in response to non-self recognition. Apidologie . doi:10.1007/s13592-013-0207-8

    Google Scholar 

  • Park, J.W., Piknova, B., Huang, P.L., Noguchi, C.T., Schechter, A.N. (2013) Effect of blood nitrite and nitrate levels on murine platelet function. PLoS ONE 8(2), e55699. doi:10.1371/journal.pone.0055699

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Richards, E., Jones, B., Bowman, A. (2011) Salivary secretions from the honey bee mite, Varroa destructor: effects on insect hemocytes and preliminary biochemical characterization. Parasitology 138, 602–608. doi:10.1017/S0031182011000072

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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 science 15, 1–14

    Article  CAS  Google Scholar 

  • Wagoner, K., Boncristiani, H., Rueppell, O. (2013) Multifaceted responses to two major parasites in the honey bee (Apis mellifera). BMC Ecology 13, 26

    Article  PubMed Central  PubMed  Google Scholar 

  • Wilson-Rich, N., Dres, D., Starks, P. (2008) The ontogeny of immunity: development of innate immune strength in the honey bee (Apis mellifera). J. Insect Physiol. 54, 1392–1399

    Article  CAS  PubMed  Google Scholar 

  • Yang, X., Cox-Foster, D.L. (2005) Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. PNAS 21, 7470–7475

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by PICT-2012-0594 granted by the “Agencia Nacional de Promoción Científica y Tecnológica” to M.E. The authors would like to thank CONICET and the UNMdP. Pedro Negri is a doctoral fellow from CONICET, Argentina.

Author information

Authors and Affiliations

  1. Laboratorio de Artrópodos, Facultad de Cs Exactas y Naturales, Universidad Nacional de Mar del Plata (UNMdP), Mar del Plata, Argentina

    Pedro Negri, Matias Maggi, Nicolas Szawarski & Martin Eguaras

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

    Lorenzo Lamattina

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

    Pedro Negri, Matias Maggi, Lorenzo Lamattina & Martin Eguaras

  4. Laboratorio de Biología Molecular, Fares Taie Instituto de Análisis, Mar del Plata, Argentina

    Silvina Quintana

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

    Pedro Negri

Authors
  1. Pedro Negri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Silvina Quintana
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matias Maggi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nicolas Szawarski
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lorenzo Lamattina
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Martin Eguaras
    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

Les hémocytes d’Apis mellifera produisent des quantités accrues d’oxyde nitrique en réponse à une blessure/encapsulation

Abeille domestique/larve/défense immunitaire/réaction de défense

Als Antwort auf eine Verwundungs/Einschlussreaktion produzieren die Hämozyten von Apis mellifera erhöhte Mengen an Stickoxid

Apis mellifera/Stickoxid/Verwundung/Einschlussreaktion

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

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Negri, P., Quintana, S., Maggi, M. et al. Apis mellifera hemocytes generate increased amounts of nitric oxide in response to wounding/encapsulation. Apidologie 45, 610–617 (2014). https://doi.org/10.1007/s13592-014-0279-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-014-0279-0

Keywords

search

Navigation