Table of Contents
ISRN Zoology
Volume 2013 (2013), Article ID 858941, 7 pages
http://dx.doi.org/10.1155/2013/858941
Research Article

Red-Eared Slider Turtles Lack Response to Immunization with Keyhole Limpet Hemocyanin but Have High Levels of Natural Antibodies

School of Biological Sciences, Illinois State University, Campus Box 4120, Normal, IL 61790-4120, USA

Received 24 October 2013; Accepted 28 November 2013

Academic Editors: D. V. Andrade, B. Crother, and C.-F. Weng

Copyright © 2013 Laura M. Zimmerman et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Medzhitov and C. Janeway Jr., “Innate immunity,” The New England Journal of Medicine, vol. 343, no. 5, pp. 338–344, 2000. View at Publisher · View at Google Scholar · View at Scopus
  2. H. B. Oral, C. Özakin, and C. A. Akdiş, “Back to the future: antibody-based strategies for the treatment of infectious diseases,” Molecular Biotechnology, vol. 21, no. 3, pp. 225–239, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. T. Snoeijs, M. Eens, E. van den Steen, and R. Pinxten, “Kinetics of primary antibody responses to sheep red blood cells in birds: a literature review and new data from great tits and European starlings,” Animal Biology, vol. 57, no. 1, pp. 79–95, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. R. D. Jurd, “Reptiles and birds,” in Immunology: A Comparative Approach, R. J. Turner, Ed., pp. 137–172, John Wiley & Sons, West Sussex, UK, 1994. View at Google Scholar
  5. M. Or-Guil, N. Wittenbrink, A. A. Weiser, and J. Schuchhardt, “Recirculation of germinal center B cells: a multilevel selection strategy for antibody maturation,” Immunological Reviews, vol. 216, no. 1, pp. 130–141, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. F. Davison, B. Kaspers, and K. A. Schat, Avian Immunology, Elsevier/Academic Press, Boston, Mass, USA, 2008.
  7. L. M. Zimmerman, L. A. Vogel, and R. M. Bowden, “Understanding the vertebrate immune system: insights from the reptilian perspective,” Journal of Experimental Biology, vol. 213, no. 5, pp. 661–671, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. H. M. Grey, “Phylogeny of the immune response: studies on some physical, chemical, and serologic characteristics of antibody produced in the turtle,” Journal of Immunology, vol. 91, no. 6, pp. 819–825, 1963. View at Google Scholar · View at Scopus
  9. B. M. Longenecker and T. R. Mosmann, “‘Natural’ antibodies to chicken MHC antigens are present in mice, rats, humans, alligators and allogeneic chickens,” Immunogenetics, vol. 11, no. 3, pp. 293–302, 1980. View at Google Scholar · View at Scopus
  10. R. Gonzalez, J. Charlemagne, W. Mahana, and S. Avrameas, “Specificity of natural serum antibodies present in phylogenetically distinct fish species,” Immunology, vol. 63, no. 1, pp. 31–36, 1988. View at Google Scholar · View at Scopus
  11. A. F. Ochsenbein and R. M. Zinkernagel, “Natural antibodies and complement link innate and acquired immunity,” Immunology Today, vol. 21, no. 12, pp. 624–630, 2000. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. Naparstek, J. Andre-Schwartz, T. Manser et al., “A single germline VH gene segment of normal A/J mice encodes autoantibodies characteristic of systemic lupus erythematosus,” Journal of Experimental Medicine, vol. 164, no. 2, pp. 614–626, 1986. View at Google Scholar · View at Scopus
  13. S. Avrameas, “Natural autoantibodies: from “horror autotoxicus” to ‘gnothi seauton’,” Immunology Today, vol. 12, pp. 154–159, 1991. View at Google Scholar
  14. C. J. Binder, M.-Y. Chou, L. Fogelstrand et al., “Natural antibodies in murine atherosclerosis,” Current Drug Targets, vol. 9, no. 3, pp. 190–195, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Boes, A. P. Prodeus, T. Schmidt, M. C. Carroll, and J. Chen, “A critical role of natural immunoglobulin M in immediate defense against systemic bacterial infection,” Journal of Experimental Medicine, vol. 188, no. 12, pp. 2381–2386, 1998. View at Publisher · View at Google Scholar · View at Scopus
  16. A. F. Ochsenbein, T. Fehr, C. Lutz et al., “Control of early viral and bacterial distribution and disease by natural antibodies,” Science, vol. 286, no. 5447, pp. 2156–2159, 1999. View at Publisher · View at Google Scholar · View at Scopus
  17. C. H. Ernst, J. E. Lovich, and R. W. Barbour, Turtles of the United States and Canada, Smithsonian Institution Press, Washington, DC, USA, 1994.
  18. L. M. Zimmerman, R. T. Paitz, L. A. Vogel, and R. M. Bowden, “Variation in the seasonal patterns of innate and adaptive immunity in the red-eared slider (Trachemys scripta),” Journal of Experimental Biology, vol. 213, no. 9, pp. 1477–1483, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. L. M. Zimmerman, S. G. Clairardin, R. T. Paitz et al., “Humoral immune responses are maintained with age in a long-lived ectotherm, the red-eared slider turtle,” Journal of Experimental Biology, vol. 216, pp. 633–640, 2013. View at Google Scholar
  20. H. M. Wilbur, “A growth model for the turtle Chrysemys picta,” Copeia, no. 2, pp. 337–343, 1975. View at Google Scholar
  21. J. W. Gibbons, R. D. Semlitsch, J. L. Greene, and J. P. Schubauer, “Variation in age and size at maturity of the slider turtle (Pseudemys scripta),” The American Naturalist, vol. 117, no. 5, pp. 841–845, 1981. View at Google Scholar
  22. B. Friguet, A. F. Chaffotte, L. Djavadi-Ohaniance, and M. E. Goldberg, “Measurements of the true affinity constant in solution of antigen-antibody complexes by enzyme-linked immunosorbent assay,” Journal of Immunological Methods, vol. 77, no. 2, pp. 305–319, 1985. View at Publisher · View at Google Scholar · View at Scopus
  23. G. A. Ingram and D. H. Molyneux, “The primary humoral immune response of European green lizards (Lacerta viridis) to Leishmania agamae,” Parasite Immunology, vol. 5, no. 1, pp. 95–108, 1983. View at Google Scholar · View at Scopus
  24. G. W. Pye, D. R. Brown, M. F. Nogueira et al., “Experimental inoculation of broad-nosed caimans (Caiman latirostris) and Siamese crocodiles (Crocodylus siamensis) with Mycoplasma alligatoris,” Journal of Zoo and Wildlife Medicine, vol. 32, no. 2, pp. 196–201, 2001. View at Google Scholar · View at Scopus
  25. F. C. Origgi, P. A. Klein, K. Mathes et al., “Enzyme-linked immunosorbent assay for detecting herpesvirus exposure in Mediterranean tortoises (spur-thighed tortoise [Testudo graeca] and Hermann's tortoise [Testudo hermanni]),” Journal of Clinical Microbiology, vol. 39, no. 9, pp. 3156–3163, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. J. J. Marchalonis, E. H. Ealey, and E. Diener, “Immune response of the Tuatara, Sphenodon punctatum,” The Australian Journal of Experimental Biology and Medical Science, vol. 47, no. 3, pp. 367–380, 1969. View at Google Scholar · View at Scopus
  27. T. M. Work, G. H. Balazs, R. A. Rameyer, S. P. Chang, and J. Berestecky, “Assessing humoral and cell-mediated immune response in Hawaiian green turtles, Chelonia mydas,” Veterinary Immunology and Immunopathology, vol. 74, no. 3-4, pp. 179–194, 2000. View at Publisher · View at Google Scholar · View at Scopus
  28. P. Kanakambika and V. Muthukkaruppan, “The immune response to sheep erythrocytes in the lizard Calotes versicolor,” Journal of Immunology, vol. 109, no. 3, pp. 415–419, 1972. View at Google Scholar · View at Scopus
  29. B. Ujvari and T. Madsen, “Age, parasites, and condition affect humoral immune response in tropical pythons,” Behavioral Ecology, vol. 17, no. 1, pp. 20–24, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. T. Madsen, B. Ujvari, K. S. Nandakumar, D. Hasselquist, and R. Holmdahl, “Do “infectious” prey select for high levels of natural antibodies in tropical pythons?” Evolutionary Ecology, vol. 21, no. 2, pp. 271–279, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. F. C. Sandmeier, C. R. Tracy, S. Dupre, and K. Hunter, “A trade-off between natural and acquired antibody production in a reptile: implications for long-term resistance to disease,” Biology Open, vol. 1, no. 11, pp. 1078–1082, 2012. View at Publisher · View at Google Scholar
  32. B. Heyman, “Regulation of antibody responses via antibodies, complement, and Fc receptors,” Annual Review of Immunology, vol. 18, pp. 709–737, 2000. View at Publisher · View at Google Scholar · View at Scopus
  33. R. Brink, T. G. Phan, D. Paus, and T. D. Chan, “Visualizing the effects of antigen affinity on T-dependent B-cell differentiation,” Immunology and Cell Biology, vol. 86, no. 1, pp. 31–39, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. U. Bruderer, S. J. Cryz Jr., U. B. Schaad, M. Deusinger, J. U. Que, and A. B. Lang, “Affinity constants of naturally acquired and vaccine-induced anti-Pseudomonas aeruginosa antibodies in healthy adults and cystic fibrosis patients,” Journal of Infectious Diseases, vol. 166, no. 2, pp. 344–349, 1992. View at Google Scholar · View at Scopus
  35. N. M. Kachamakova, I. Irnazarow, H. K. Parmentier, H. F. J. Savelkoul, A. Pilarczyk, and G. F. Wiegertjes, “Genetic differences in natural antibody levels in common carp (Cyprinus carpio L.),” Fish and Shellfish Immunology, vol. 21, no. 4, pp. 404–413, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. H. K. Parmentier, A. Lammers, J. J. Hoekman, G. de Vries Reilingh, I. T. A. Zaanen, and H. F. J. Savelkoul, “Different levels of natural antibodies in chickens divergently selected for specific antibody responses,” Developmental and Comparative Immunology, vol. 28, no. 1, pp. 39–49, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. L. Benatuil, J. Kaye, N. Cretin et al., “Ig knock-in mice producing anti-carbohydrate antibodies: breakthrough of B cells producing low affinity anti-self antibodies,” Journal of Immunology, vol. 180, no. 6, pp. 3839–3848, 2008. View at Google Scholar · View at Scopus
  38. N. Baumgarth, J. W. Tung, and L. A. Herzenberg, “Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion,” Springer Seminars in Immunopathology, vol. 26, no. 4, pp. 347–362, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. S. A. Johnson, S. J. Rozzo, and J. C. Cambier, “Aging-dependent exclusion of antigen-inexperienced cells from the peripheral B cell repertoire,” Journal of Immunology, vol. 168, no. 10, pp. 5014–5023, 2002. View at Google Scholar · View at Scopus
  40. L. M. Zimmerman, R. T. Paitz, S. G. Clairardin, L. A. Vogel, and R. M. Bowden, “No evidence that estrogens affect the development of the immune system in the red-eared slider turtle, Trachemys scripta,” Hormones and Behavior, vol. 62, no. 3, pp. 331–336, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. T. Koppenheffer, “Ontogeny of antibody production against microbial cell wall constituents in juvenile chickens,” The FASEB Journal, vol. 22, p. 560, 2008. View at Google Scholar
  42. S. L. Klein, “Hormones and mating system affect sex and species differences in immune function among vertebrates,” Behavioural Processes, vol. 51, no. 1–3, pp. 149–166, 2000. View at Publisher · View at Google Scholar · View at Scopus
  43. Z.-H. Zhou, A. G. Tzioufas, and A. L. Notkins, “Properties and function of polyreactive antibodies and polyreactive antigen-binding B cells,” Journal of Autoimmunity, vol. 29, no. 4, pp. 219–228, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. Y. Wang, J. Hong, X. Liu et al., “Snake cathelicidin from Bungarus fasciatus is a potent peptide antibiotics,” PLoS ONE, vol. 3, no. 9, Article ID e3217, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. M. E. Merchant, C. Roche, R. M. Elsey, and J. Prudhomme, “Antibacterial properties of serum from the American alligator (Alligator mississippiensis),” Comparative Biochemistry and Physiology B, vol. 136, no. 3, pp. 505–513, 2003. View at Publisher · View at Google Scholar · View at Scopus