journal article Open Access Aug 28, 2012

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 · The Company of Biologists
View at Publisher Save 10.1242/bio.20122527
Abstract
Summary
Vertebrate immune systems are understood to be complex and dynamic, with trade-offs among different physiological components (e.g., innate and adaptive immunity) within individuals and among taxonomic lineages. Desert tortoises (Gopherus agassizii) immunised with ovalbumin (OVA) showed a clear trade-off between levels of natural antibodies (NAbs; innate immune function) and the production of acquired antibodies (adaptive immune function). Once initiated, acquired antibody responses included a long-term elevation in antibodies persisting for more than one year. The occurrence of either (a) high levels of NAbs or (b) long-term elevations of acquired antibodies in individual tortoises suggests that long-term humoral resistance to pathogens may be especially important in this species, as well as in other vertebrates with slow metabolic rates, concomitantly slow primary adaptive immune responses, and long life-spans.
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References
54
[1]
Ambrosius "Immunoglobulins and antibody production in reptiles." (1976)
[2]
Baccala "Two murine natural polyreactive autoantibodies are encoded by nonmutated germ-line genes." Proc. Natl. Acad. Sci. USA (1989) 10.1073/pnas.86.12.4624
[3]
Baumgarth "B-1 and B-2 cell-derived immunoglobulin M antibodies are nonredundant components of the protective response to influenza virus infection." J. Exp. Med. (2000) 10.1084/jem.192.2.271
[4]
Baumgarth "Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion." Springer Semin. Immunopathol. (2005) 10.1007/s00281-004-0182-2
[5]
Bayne "The acute phase response and innate immunity of fish." Dev. Comp. Immunol. (2001) 10.1016/s0145-305x(01)00033-7
[6]
Ben–Aissa–Fennira "IgM antibodies to P1 cytoadhesin of Mycoplasma pneumoniae are part of the natural antibody repertoire expressed early in life." Immunol. Lett. (1998) 10.1016/s0165-2478(98)00053-4
[7]
Boes "Role of natural and immune IgM antibodies in immune responses." Mol. Immunol. (2000) 10.1016/s0161-5890(01)00025-6
[8]
Antiphosphocholine antibodies found in normal mouse serum are protective against intravenous infection with type 3 streptococcus pneumoniae.

D E Briles, M Nahm, K Schroer et al.

Journal of Experimental Medicine 1981 10.1084/jem.153.3.694
[9]
Bromage "Plasmablast and plasma cell production and distribution in trout immune tissues." J. Immunol. (2004) 10.4049/jimmunol.173.12.7317
[10]
Brown "Mycoplasma agassizii causes upper respiratory tract disease in the desert tortoise." Infect. Immun. (1994) 10.1128/iai.62.10.4580-4586.1994
[11]
Cartner "Roles of innate and adaptive immunity in respiratory mycoplasmosis." Infect. Immun. (1998) 10.1128/iai.66.8.3485-3491.1998
[12]
Casali "CD5+ B lymphocytes, polyreactive antibodies and the human B-cell repertoire." Immunol. Today (1989) 10.1016/0167-5699(89)90268-5
[13]
Casali "Structure and function of natural antibodies." Curr. Top. Microbiol. Immunol. (1996) 10.1007/978-3-642-85226-8_17
[14]
Chen "Effects of stocking density on growth and non-specific immune responses in juvenile soft-shelled turtle Pelodiscus sinensis." Aquaculture Research (2007) 10.1111/j.1365-2109.2007.01813.x
[15]
Coberley "Survey of Florida green turtles for exposure to a disease-associated herpesvirus." Dis. Aquat. Organ. (2001) 10.3354/dao047159
[16]
Cooper "Description of Xerobates agassizii." Proc. Calif. Acad. Sci. (1863)
[17]
Ehrenstein "Targeted gene disruption reveals a role for natural secretory IgM in the maturation of the primary immune response." Proc. Natl. Acad. Sci. USA (1998) 10.1073/pnas.95.17.10089
[18]
Flajnik "Early and natural antibodies in non-mammalian vertebrates." Curr. Top. Microbiol. Immunol. (2000) 10.1007/978-3-642-57284-5_24
[19]
Gonzalez "Specificity of natural serum antibodies present in phylogenetically distinct fish species." Immunology (1988)
[20]
Herbst "Serological association between spirorchidiasis, herpesvirus infection, and fibropapillomatosis in green turtles from Florida." J. Wildl. Dis. (1998) 10.7589/0090-3558-34.3.496
[21]
Herbst "Use of baculovirus-expressed glycoprotein H in an enzyme-linked immunosorbent assay developed to assess exposure to chelonid fibropapillomatosis-associated herpesvirus and its relationship to the prevalence of fibropapillomatosis in sea turtles." Clin. Vaccine Immunol. (2008) 10.1128/cvi.00438-07
[22]
Hernandez–Divers "Angiographic, anatomic and clinical technique descriptions of a subcarapacial venipuncture site for chelonians." Journal of Herpetological Medicine and Surgery (2002) 10.5818/1529-9651.12.2.32
[23]
Hsu "Mutation, selection, and memory in B lymphocytes of exothermic vertebrates." Immunol. Rev. (1998) 10.1111/j.1600-065x.1998.tb01426.x
[24]
Hunter "Western blot can distinguish natural and acquired antibodies to Mycoplasma agassizii in the desert tortoise (Gopherus agassizii)." J. Microbiol. Methods (2008) 10.1016/j.mimet.2008.07.022
[25]
Jacobson "Serodiagnostics." (2007) 10.1201/9781420004038.ch8
[26]
Janeway (2005)
[27]
Kaattari "Analysis of long-lived plasma cell production and regulation: implications for vaccine design for aquaculture." Aquaculture (2005) 10.1016/j.aquaculture.2004.12.024
[28]
Kachamakova "Genetic differences in natural antibody levels in common carp (Cyprinus carpio L.)." Fish Shellfish Immunol. (2006) 10.1016/j.fsi.2006.01.005
[29]
Origin of Murine B Cell Lineages

A B Kantor, L A Herzenberg

Annual Review of Immunology 1993 10.1146/annurev.iy.11.040193.002441
[30]
Leishman "Immunological consequences of intervention in established immune responses by feeding protein antigens." Cell. Immunol. (1998) 10.1006/cimm.1998.1242
[31]
Madsen "Do “infectious” prey select for high levels of natural antibodies in tropical python?" Evol. Ecol. (2007) 10.1007/s10682-006-9004-4
[32]
Manz "Survival of long-lived plasma cells is independent of antigen." Int. Immunol. (1998) 10.1093/intimm/10.11.1703
[33]
Martin "Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs." Phil. Trans. R. Soc. B (2008) 10.1098/rstb.2007.2142
[34]
Matson "Are there differences in immune function between continental and insular birds?" Proc. Biol. Sci. (2006) 10.1098/rspb.2006.3590
[35]
Matson "No simple answers for ecological immunology: relationships among immune indices at the individual level break down at the species level in waterfowl." Proc. Biol. Sci. (2006) 10.1098/rspb.2005.3376
[36]
Ecological immunology: life history trade-offs and immune defense in birds

K. Norris

Behavioral Ecology 2000 10.1093/beheco/11.1.19
[37]
Ochsenbein "Natural antibodies and complement link innate and acquired immunity." Immunol. Today (2000) 10.1016/s0167-5699(00)01754-0
[38]
Ochsenbein "Control of early viral and bacterial distribution and disease by natural antibodies." Science (1999) 10.1126/science.286.5447.2156
[39]
Origgi "Reptile immunology." (2007) 10.1201/9781420004038.ch2
[40]
Packard "The use of percentages and size-specific indices to normalize physiological data for variation in body size: wasted time, wasted effort?" Comp. Biochem. Physiol. A (1999) 10.1016/s1095-6433(98)10170-8
[41]
Parmentier "Different levels of natural antibodies in chickens divergently selected for specific antibody responses." Dev. Comp. Immunol. (2004) 10.1016/s0145-305x(03)00087-9
[42]
Parmentier "Decreased specific antibody responses to α-Gal-conjugated antigen in animals with preexisting high levels of natural antibodies binding α-Gal residues." Poult. Sci. (2008) 10.3382/ps.2007-00487
[43]
Parslow "Immunogens, antigens, and vaccines." (2001)
[44]
Salvante "Techniques for studying integrated immune function in birds." Auk (2006) 10.1642/0004-8038(2006)123[575:tfsiif]2.0.co;2
[45]
Sandmeier "Upper respiratory tract disease (URTD) as a threat to desert tortoise populations: a reevaluation." Biol. Conserv. (2009) 10.1016/j.biocon.2009.02.001
[46]
Schumacher "Detection of antibodies to a pathogenic mycoplasma in desert tortoises (Gopherus agassizii) with upper respiratory tract disease." J. Clin. Microbiol. (1993) 10.1128/jcm.31.6.1454-1460.1993
[47]
Sinyakov "Vaccines and natural antibodies: a link to be considered." Vaccine (2009) 10.1016/j.vaccine.2009.01.121
[48]
Sinyakov "Natural antibodies and their significance in active immunization and protection against a defined pathogen in fish." Vaccine (2002) 10.1016/s0264-410x(02)00379-1
[49]
Sinyakov "Nano- and microparticles as adjuvants in vaccine design: success and failure is related to host natural antibodies." Vaccine (2006) 10.1016/j.vaccine.2006.06.021
[50]
Slifka "Long-term humoral immunity against viruses: revisiting the issue of plasma cell longevity." Trends Microbiol. (1996) 10.1016/0966-842x(96)10059-7

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Published
Aug 28, 2012
Vol/Issue
1(11)
Pages
1078-1082
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Franziska C. Sandmeier, C. Richard Tracy, Sally Dupré, et al. (2012). A trade-off between natural and acquired antibody production in a reptile: implications for long-term resistance to disease. Biology Open, 1(11), 1078-1082. https://doi.org/10.1242/bio.20122527