Skip to main content
SpringerLink
Log in

Humoral Immune Function in Long-Lived Ectotherms, the Reptiles

  • Living reference work entry
  • First Online:
Handbook of Immunosenescence

Abstract

Traditional biomedical models have provided important insights to the impact of aging on overall health and fitness of organisms. However, many nonmodel organisms may be underrated in their value to studying senescence, particularly the effects of age on immune system function. This review first discusses the current understanding of humoral immunity in reptiles then presents evidence for the potential of reptiles to serve as models for the apparent lack (or reduced intensity) of immunosenescence that they experience on immune function. This review also highlights the necessity for the development of basic tools and reagents to elucidate immune cell subsets and function in these taxa.

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

Access this chapter

Log in via an institution

Institutional subscriptions

References

  • Ademokun A, Wu YC, Dunn-Walters D (2010) The ageing B cell population: composition and function. Biogerontology 11:125–137

    Article  PubMed  Google Scholar 

  • Adeoye GO, Ogunbanwo OO (2007) Helminth parasites of the African lizard Agama agama (Squamata : Agamidae), in Lagos, Nigeria. Rev Biol Trop 55:417–425

    Article  CAS  PubMed  Google Scholar 

  • Amo L, Fargallo JA, Martinez-Padilla J, Millan J, Lopez P, Martin J (2005) Prevalence and intensity of blood and intestinal parasites in a field population of a Mediterranean lizard, Lacerta lepida. Parasitol Res 96:413–417

    Article  CAS  PubMed  Google Scholar 

  • Baumgarth N (2011) The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nat Rev Immunol 11:34–46

    Article  CAS  PubMed  Google Scholar 

  • Benatuil L, Kaye J, Cretin N, Godwin JG, Cariappa A, Pillai S, Iacomini J (2008) Ig knock-in mice producing anti-carbohydrate antibodies: breakthrough of B cells producing low affinity anti-self antibodies. J Immunol 180:3839–3848

    Article  CAS  PubMed  Google Scholar 

  • Ben-Yehuda A, Szabo P, LeMaoult J, Manavalan JS, Weksler ME (1998) Increased VH 11 and VH Q52 gene use by splenic B cells in old mice associated with oligoclonal expansions of CD5 + B cells. Mech Ageing Dev 103:111–121

    Article  CAS  PubMed  Google Scholar 

  • Blaeser T, Panwar A, Vogel LA (2008) Humoral immunity and aging: intrinsic B cell defects. Curr Trends Immunol 8:61–67

    Google Scholar 

  • Bockman D (1970) The thymus. Academy Press, New York

    Google Scholar 

  • Boehm T, Bleul CC (2007) The evolutionary history of lymphoid organs. Nat Immunol 8:131–135

    Article  CAS  PubMed  Google Scholar 

  • Boes M, Prodeus AP, Schmidt T, Carroll MC, Chen J (1998) A critical role of natural immunoglobulin M in immediate defense against systemic bacterial infection. J Exp Med 188: 2381–2386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borysenko M, Lewis S (1979) The effect of malnutrition on immunocompetence and whole body resistance to infection in Chelydra serpentina. Dev Comp Immunol 3:89–100

    Article  CAS  PubMed  Google Scholar 

  • Britton A (2016) Crocodilians: natural history and conservation [Internet]. [cited 15 June 2016]. Available from http://crocodilian.com/cnhc/csp_tsch.htm

  • Brown DR (2002) Mycoplasmosis and immunity of fish and reptiles. Front Biosci 7:d1338–d1346

    Article  CAS  PubMed  Google Scholar 

  • Brown DS, Symondson WO (2014) Sex and age-biased nematode prevalence in reptiles. Mol Ecol 23:3890–3899

    Article  PubMed  Google Scholar 

  • Burnham DK, Keall SN, Nelson NJ, Daugherty CH (2005) T cell function in tuatara (Sphenodon punctatus). Comp Immunol Microbiol Infect Dis 28:213–222

    Article  PubMed  Google Scholar 

  • Chen KS, Quinnan JV Jr (1989) Secretory immunoglobulin A antibody response is conserved in aged mice following oral immunization with influenza virus vaccine. J Gen Virol 70:3291–3296

    Article  PubMed  Google Scholar 

  • Chen SN, Huang B, Zhang XW, Li Y, Zhao LJ, Li N, Gao Q, Nie P (2013) IFN-gamma and its receptors in a reptile reveal the evolutionary conservation of type II IFNs in vertebrates. Dev Comp Immunol 41:587–596

    Article  CAS  PubMed  Google Scholar 

  • Congdon JD, Nagle RD, Kinney OM, van Loben Sels RC (2001) Hypotheses of aging in a long-lived vertebrate, Blanding’s turtle (Emydoidea blandingii). Exp Gerontol 36:813–827

    Article  CAS  PubMed  Google Scholar 

  • Congdon JD, Nagle RD, Kinney OM, van Loben Sels RC, Quinter T, Tinkle DW (2003) Testing hypotheses of aging in long-lived painted turtles (Chrysemys picta). Exp Gerontol 38:765–772

    Article  PubMed  Google Scholar 

  • Cumano AC, Paige J, Iscove NN, Brady G (1992) Bipotential precursors of B cells and macrophages in murine fetal liver. Nature 356:612–615

    Article  CAS  PubMed  Google Scholar 

  • Dabrowski Z, Sano Martins IS, Tabarowski Z, Witkowska-Pelc E, Spadacci Morena DD, Spodaryk K, Podkowa D (2007) Haematopoiesis in snakes (Ophidia) in early postnatal development. Cell Tissue Res 328:291–299

    Article  CAS  PubMed  Google Scholar 

  • de Magalhaes JP, Toussaint O (2002) The evolution of mammalian aging. Exp Gerontol 37:769–775

    Article  PubMed  Google Scholar 

  • Deza FG, Espinel CS, Beneitez JV (2007) A novel IgA-like immunoglobulin in the reptile Eublepharis macularius. Dev Comp Immunol 31:596–605

    Article  PubMed  CAS  Google Scholar 

  • Eberl G, Lochner M (2009) The development of intestinal lymphoid tissues at the interface of self and microbiota. Mucosal Immunol 2:478–485

    Article  CAS  PubMed  Google Scholar 

  • El Deeb S, Zada S, El Ridi R (1985) Ontogeny of hemopoietic and lymphopoietic tissues in the lizard Chalcides ocellatus (Reptilia, Sauna, Scincidae). J Morphol 185:241–253

    Article  Google Scholar 

  • el Masri M, Saad AH, Mansour MH, Badir N (1995) Seasonal distribution and hormonal modulation of reptilian T cells. Immunobiology 193:15–41

    Article  PubMed  Google Scholar 

  • Frasca D, Landin AM, Riley RL, Blomberg BB (2008) Mechanisms for decreased function of B cells in aged mice and humans. J Immunol 180:2741–2746

    Article  CAS  PubMed  Google Scholar 

  • Gambon-Deza F, Espinel CS (2008) IgD in the reptile leopard gecko. Mol Immunol 45:3470–3476

    Article  CAS  PubMed  Google Scholar 

  • Gambon-Deza F, Sanchez-Espinel C, Mirete-Bachiller S, Magadan-Mompo S (2012) Snakes antibodies. Dev Comp Immunol 38:1–9

    Article  CAS  PubMed  Google Scholar 

  • Gibbons JW, Scott DE, Ryan TJ, Buhlmann KA, Tuberville TD, Metts BS, Greene JL, Mills T, Leiden Y, Poppy S, Winne CT (2000) The global decline of reptiles, Deja Vu amphibians. Bioscience 50:653–666

    Article  Google Scholar 

  • Hakim FT, Flomerfelt FA, Boyiadzis M, Gress RE (2004) Aging, immunity and cancer. Curr Opin Immunol 16:151–156

    Article  CAS  PubMed  Google Scholar 

  • Hardy RR (2006) B-1 B cells: development, selection, natural autoantibody and leukemia. Curr Opin Immunol 18:547–555

    Article  CAS  PubMed  Google Scholar 

  • Hareramadas B, Rai U (2005) Mechanism of androgen-induced thymic atrophy in the wall lizard, Hemidactylus flaviviridis: an in vitro study. Gen Comp Endocrinol 144:10–19

    Article  CAS  PubMed  Google Scholar 

  • Hareramadas B, Rai U (2006) Cellular mechanism of estrogen-induced thymic involution in wall lizard: caspase-dependent action. J Exp Zool A Comp Exp Biol 305:396–409

    Article  PubMed  CAS  Google Scholar 

  • Herbst LH, Klein PA (1995) Monoclonal antibodies for the measurement of class-specific antibody responses in the green turtle, Chelonia mydas. Vet Immunol Immunopathol 46:317–335

    Article  CAS  PubMed  Google Scholar 

  • Hsu E (1998) Mutation, selection, and memory in B lymphocytes of exothermic vertebrates. Immunol Rev 162:25–36

    Article  CAS  PubMed  Google Scholar 

  • Hu A, Ehleiter D, Ben Yehuda A, Schwab R, Russo C, Szabo P, Weksler ME (1993) Effect of age on the expressed B cell repertoire: role of B cell subsets. Int Immunol 5:1035–1039

    Article  CAS  PubMed  Google Scholar 

  • Hussein MF, Badir N, el-Ridi R, Akef M (1978) Effect of seasonal variation on lymphoid tissues of the lizards, Mabuya quinquetaeniata Licht. and Uromastyx aegyptia Forsk. Dev Comp Immunol 2:469–478

    Article  CAS  PubMed  Google Scholar 

  • Kaetzel C (2014) Coevolution of mucosal immunoglobulins and the polymeric immunoglobulin receptor: evidence that the commensal microbiota provided the driving force. ISRN Immunol 2014:20

    Article  CAS  Google Scholar 

  • Katsura Y (2002) Redefinition of lymphoid progenitors. Nat Rev Immunol 2:127–132

    Article  CAS  PubMed  Google Scholar 

  • Kawanishi H, Kiely J (1989) Immune-related alterations in aged gut-associated lymphoid tissues in mice. Dig Dis Sci 34:175–184

    Article  CAS  PubMed  Google Scholar 

  • Kroese FG, Ammerlaan WA, Kantor AB (1993) Evidence that intestinal IgA plasma cells in mu, kappa transgenic mice are derived from B-1 (Ly-1 B) cells. Int Immunol 5:1317–1327

    Article  CAS  PubMed  Google Scholar 

  • Kurtz CC, Carey HV (2007) Seasonal changes in the intestinal immune system of hibernating ground squirrels. Dev Comp Immunol 31:415–428

    Article  CAS  PubMed  Google Scholar 

  • Kvell K, Cooper EL, Engelmann P, Bovari J, Nemeth P (2007) Blurring borders: innate immunity with adaptive features. Clin Dev Immunol 2007:83671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leceta J, Zapata A (1985) Seasonal changes in the thymus and spleen of the turtle, Mauremys caspica. A morphometrical, light microscopical study. Dev Comp Immunol 9:653–668

    Article  CAS  PubMed  Google Scholar 

  • Leceta J, Garrido E, Torroba M, Zapata AG (1989) Ultrastructural changes in the thymus of the turtle Mauremys caspica in relation to the seasonal cycle. Cell Tissue Res 256:213–219

    Article  CAS  PubMed  Google Scholar 

  • Li J, Barreda DR, Zhang YA, Boshra H, Gelman AE, Lapatra S, Tort L, Sunyer JO (2006) B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat Immunol 7:1116–1124

    Article  CAS  PubMed  Google Scholar 

  • Li L, Wang T, Sun Y, Cheng G, Yang H, Wei Z, Wang P, Hu X, Ren L, Meng Q, Zhang R, Guo Y, Hammarstrom L, Li N, Zhao Y (2012) Extensive diversification of IgD-, IgY-, and truncated IgY(deltaFc)-encoding genes in the red-eared turtle (Trachemys scripta elegans). J Immunol 189:3995–4004

    Article  CAS  PubMed  Google Scholar 

  • Longenecker BM, Mosmann TR (1980) “Natural” antibodies to chicken MHC antigens are present in mice, rats, humans, alligators and allogeneic chickens. Immunogenetics 11:293–302

    Article  CAS  PubMed  Google Scholar 

  • Macpherson AJ, Gatto D, Sainsbury E, Harriman GR, Hengartner H, Zinkernagel RM (2000) A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 288:2222–2226

    Article  CAS  PubMed  Google Scholar 

  • Magnadottir B, Gudmundsdottir S, Gudmundsdottir BK, Helgason S (2009) Natural antibodies of cod (Gadus morhua L.): specificity, activity and affinity. Comp Biochem Physiol B Biochem Mol Biol 154:309–316

    Article  PubMed  CAS  Google Scholar 

  • Martin LB, Han P, Lewittes J, Kuhlman JR, Klasing KC, Wikelski M (2006) Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Funct Ecol 20:290–299

    Article  Google Scholar 

  • Massot M, Clobert J, Montes-Poloni L, Haussy C, Cubo J, Meylan S (2011) An integrative study of ageing in a wild population of common lizards. Funct Ecol 25:848–858

    Article  Google Scholar 

  • McClellan JS, Dove C, Gentles AJ, Ryan CE, Majeti R (2015) Reprogramming of primary human Philadelphia chromosome-positive B cell acute lymphoblastic leukemia cells into nonleukemic macrophages. Proc Natl Acad Sci USA 112:4074–4079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McDonald KG, Leach MR, Huang C, Wang C, Newberry RD (2011) Aging impacts isolated lymphoid follicle development and function. Immun Ageing 8:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller JK (2001) Escaping senescence: demographic data from the three-toed box turtle (Terrapene carolina triunguis). Exp Gerontol 36:829–832

    Article  CAS  PubMed  Google Scholar 

  • Montecino-Rodriguez E, Leathers H, Dorshkind K (2001) Bipotential B-macrophage progenitors are present in adult bone marrow. Nat Immunol 2:83–88

    Article  CAS  PubMed  Google Scholar 

  • Munoz FA, Estrada-Parra S, Romero-Rojas A, Work TM, Gonzalez-Ballesteros E, Estrada-Garcia I (2009) Identification of CD3+ T lymphocytes in the green turtle Chelonia mydas. Vet Immunol Immunopathol 131:211–217

    Article  CAS  PubMed  Google Scholar 

  • Munoz FA, Franco-Noguez SY, Gonzalez-Ballesteros E, Negrete-Philippe AC, Flores-Romo L (2014) Characterisation of the green turtle’s leukocyte subpopulations by flow cytometry and evaluation of their phagocytic activity. Vet Res Commun 38:123–128

    Article  CAS  PubMed  Google Scholar 

  • Nagler-Anderson C (2001) Man the barrier! Strategic defences in the intestinal mucosa. Nat Rev Immunol 1:59–67

    Article  CAS  PubMed  Google Scholar 

  • Nakashima M, Kinoshita M, Nakashima H, Habu Y, Miyazaki H, Shono S, Hiroi S, Shinomiya N, Nakanishi K, Seki S (2012) Pivotal advance: characterization of mouse liver phagocytic B cells in innate immunity. J Leukoc Biol 91:537–546

    Article  CAS  PubMed  Google Scholar 

  • Natarajan K, Muthukkaruppan VR (1985) Distribution and ontogeny of B cells in the garden lizard, Calotes versicolor. Dev Comp Immunol 9:301–310

    Article  CAS  PubMed  Google Scholar 

  • Nikolich-Zugich J (2014) Aging of the T cell compartment in mice and humans: from no naive expectations to foggy memories. J Immunol 193:2622–2629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ochsenbein AF, Zinkernagel RM (2000) Natural antibodies and complement link innate and acquired immunity. Immunol Today 21:624–630

    Article  CAS  PubMed  Google Scholar 

  • Origgi FC, Klein PA, Mathes K, Blahak S, Marschang RE, Tucker SJ, Jacobson ER (2001) Enzyme-linked immunosorbent assay for detecting herpesvirus exposure in Mediterranean tortoises (spur-thighed tortoise [Testudo graeca] and Hermann’s tortoise [Testudo hermanni]). J Clin Microbiol 39:3156–3163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Overland HS, Pettersen EF, Ronneseth A, Wergeland HI (2010) Phagocytosis by B-cells and neutrophils in Atlantic salmon (Salmo salar L.) and Atlantic cod (Gadus morhua L.) Fish Shellfish Immunol 28:193–204

    Article  CAS  PubMed  Google Scholar 

  • Parra D, Rieger AM, Li J, Zhang YA, Randall LM, Hunter CA, Barreda DR, Sunyer JO (2012) Pivotal advance: peritoneal cavity B-1 B cells have phagocytic and microbicidal capacities and present phagocytosed antigen to CD4+ T cells. J Leukoc Biol 91:525–536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parra D, Takizawa F, Sunyer JO (2013) Evolution of B cell immunity. Annu Rev Anim Biosci 1:65–97

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pata S, Yaraksa N, Daduang S, Temsiripong Y, Svasti J, Araki T, Thammasirirakv S (2011) Characterization of the novel antibacterial peptide Leucrocin from crocodile (Crocodylus siamensis) white blood cell extracts. Dev Comp Immunol 35:545–553

    Article  CAS  PubMed  Google Scholar 

  • Patnaik BK (1994) Ageing in reptiles. Gerontology 40:200–220

    Article  CAS  PubMed  Google Scholar 

  • Pitchappan R, Muthukkaruppan V (1977) Role of the thymus in the immune response to sheep erythrocytes in the lizard Calotes versicolor. Proc Indiana Acad Sci B 85:25–33

    Google Scholar 

  • Preecharram S, Jearranaiprepame P, Daduang S, Temsiripong Y, Somdee T, Fukamizo T, Svasti J, Araki T, Thammasirirak S (2010) Isolation and characterisation of crocosin, an antibacterial compound from crocodile (Crocodylus siamensis) plasma. Anim Sci J 81:393–401

    Article  CAS  PubMed  Google Scholar 

  • Pye GW, Brown DR, Nogueira MF, Vliet KA, Schoeb TR, Jacobson ER, Bennett RA (2001) Experimental inoculation of broad-nosed caimans (Caiman latirostris) and Siamese crocodiles (Crocodylus siamensis) with Mycoplasma alligatoris. J Zoo Wildl Med 32:196–201

    Article  CAS  PubMed  Google Scholar 

  • Rothstein TL (2016) Natural antibodies as rheostats for susceptibility to chronic diseases in the aged. Front Immunol 7:127

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Saad AH, El Ridi R (1984) Mixed leukocyte reaction, graft-versus-host reaction, and skin allograft rejection in the lizard, Chalcides ocellatus. Immunobiology 166:484–493

    Article  CAS  PubMed  Google Scholar 

  • Saad AH, Torroba M, Varas A, Zapata A (1991) Testosterone induces lymphopenia in turtles. Vet Immunol Immunopathol 28:173–180

    Article  CAS  PubMed  Google Scholar 

  • Sacchi R, Capelli E, Scali S, Pellitteri-Rosa D, Ghitti M, Acerbi E, Pingitore E (2014) In vitro temperature dependent activation of T-lymphocytes in common wall lizards (Podarcis muralis) in response to PHA stimulation. Acta Herpetologica 9:131–138

    Google Scholar 

  • Salkeld DJ, Schwarzkopf L (2005) Epizootiology of blood parasites in an Australian lizard: a mark-recapture study of a natural population. Int J Parasitol 35:11–18

    Article  PubMed  Google Scholar 

  • Sandmeier FC, Tracy CR, Dupre S, Hunter K (2012) A trade-off between natural and acquired antibody production in a reptile: implications for long-term resistance to disease. Biol Open 1:1078–1082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scholz JL, Diaz A, Riley RL, Cancro MP, Frasca D (2013) A comparative review of aging and B cell function in mice and humans. Curr Opin Immunol 25:504–510

    Article  CAS  PubMed  Google Scholar 

  • Schwanz L, Warner DA, McGaugh S, Di Terlizzi R, Bronikowski A (2011) State-dependent physiological maintenance in a long-lived ectotherm, the painted turtle (Chrysemys picta). J Exp Biol 214:88–97

    Article  PubMed  Google Scholar 

  • Shaffer HB, Minx P, Warren DE, Shedlock AM, Thomson RC, Valenzuela N, Abramyan J, Amemiya CT, Badenhorst D, Biggar KK, Borchert GM, Botka CW, Bowden RM, Braun EL, Bronikowski AM, Bruneau BG, Buck LT, Capel B, Castoe TA, Czerwinski M, Delehaunty KD, Edwards SV, Fronick CC, Fujita MK, Fulton L, Graves TA, Green RE, Haerty W, Hariharan R, Hernandez O, Hillier LW, Holloway AK, Janes D, Janzen FJ, Kandoth C, Kong L, de Koning AP, Li Y, Literman R, McGaugh SE, Mork LE, O’Laughlin M, Paitz RT, Pollock DD, Ponting CP, Radhakrishnan S, Raney BJ, Richman JM, St John J, Schwartz T, Sethuraman A, Spinks PQ, Storey KB, Thane N, Vinar T, Zimmerman LM, Warren WC, Mardis ER, Wilson RK (2013) The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage. Genome Biol 14:R28

    Article  PubMed  CAS  Google Scholar 

  • Sparkman AM, Palacios MG (2009) A test of life-history theories of immune defence in two ecotypes of the garter snake, Thamnophis elegans. J Anim Ecol 78:1242–1248

    Article  PubMed  Google Scholar 

  • Sun Y, Wei Z, Li N, Zhao Y (2013) A comparative overview of immunoglobulin genes and the generation of their diversity in tetrapods. Dev Comp Immunol 39:103–109

    Article  PubMed  CAS  Google Scholar 

  • Terebey N (1972) A light microscopic study of the mononuclear cells infiltrating skin homografts in the garter snake, Thamnophis sirtalis (Reptilia: Colubridae). J Morphol 137:149–159

    Article  CAS  PubMed  Google Scholar 

  • Turchin A, Hsu E (1996) The generation of antibody diversity in the turtle. J Immunol 156:3797–3805

    CAS  PubMed  Google Scholar 

  • Ujvari B, Madsen T (2006) Age, parasites, and condition affect humoral immune response in tropical pythons. Behav Ecol 17:20–24

    Article  Google Scholar 

  • Ujvari B, Madsen T (2011) Do natural antibodies compensate for humoral immunosenescence in tropical pythons? Funct Ecol 25:813–817

    Article  Google Scholar 

  • Vidard L, Kovacsovics-Bankowski M, Kraeft SK, Chen LB, Benacerraf B, Rock KL (1996) Analysis of MHC class II presentation of particulate antigens of B lymphocytes. J Immunol 156:2809–2818

    CAS  PubMed  Google Scholar 

  • Warner DA, Miller DA, Bronikowski AM, Janzen FJ (2016) Decades of field data reveal that turtles senesce in the wild. Proc Natl Acad Sci USA 113:6502–6507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warr GW, Magor KE, Higgins DA (1995) IgY: clues to the origins of modern antibodies. Immunol Today 16:392–398

    Article  CAS  PubMed  Google Scholar 

  • Wei Z, Wu Q, Ren L, Hu S, Guo Y, Warr GW, Hammarstrom L, Li N, Zhao Y (2009) Expression of IgM, IgD, and IgY in a reptile, Anolis carolinensis. J Immunol 183:3858–3864

    Article  CAS  PubMed  Google Scholar 

  • Weksler ME, Szabo P (2000) The effect of age on the B-cell repertoire. J Clin Immunol 20:240–249

    Article  CAS  PubMed  Google Scholar 

  • Work TM, Balazs GH, Rameyer RA, Chang SP, Berestecky J (2000) Assessing humoral and cell-mediated immune response in Hawaiian green turtles, Chelonia mydas. Vet Immunol Immunopathol 74:179–194

    Article  CAS  PubMed  Google Scholar 

  • Wu Q, Wei Z, Yang Z, Wang T, Ren L, Hu X, Meng Q, Guo Y, Zhu Q, Robert J, Hammarstrom L, Li N, Zhao Y (2010) Phylogeny, genomic organization and expression of lambda and kappa immunoglobulin light chain genes in a reptile, Anolis carolinensis. Dev Comp Immunol 34:579–589

    Article  CAS  PubMed  Google Scholar 

  • Zhu LY, Lin AF, Shao T, Nie L, Dong WR, Xiang LX, Shao JZ (2014) B cells in teleost fish act as pivotal initiating APCs in priming adaptive immunity: an evolutionary perspective on the origin of the B-1 cell subset and B7 molecules. J Immunol 192:2699–2714

    Article  CAS  PubMed  Google Scholar 

  • Zhu Q, Zhang M, Shi M, Liu Y, Zhao Q, Wang W, Zhang G, Yang L, Zhi J, Zhang L, Hu G, Chen P, Yang Y, Dai W, Liu T, He Y, Feng G, Zhao G (2016) Human B cells have an active phagocytic capability and undergo immune activation upon phagocytosis of Mycobacterium tuberculosis. Immunobiology 221:558–567

    Article  CAS  PubMed  Google Scholar 

  • Zimmerman LM, Vogel LA, Bowden RM (2010a) Understanding the vertebrate immune system: insights from the reptilian perspective. J Exp Biol 213:661–671

    Article  CAS  PubMed  Google Scholar 

  • Zimmerman LM, Vogel LA, Edwards KA, Bowden RM (2010b) Phagocytic B cells in a reptile. Biol Lett 6:270–273

    Article  PubMed  Google Scholar 

  • Zimmerman LM, Bowden RM, Vogel LA (2013a) Red-eared slider turtles lack response to immunization with keyhole limpet hemocyanin but have high levels of natural antibodies. ISRN Zool 2013:1–7

    Article  Google Scholar 

  • Zimmerman LM, Clairardin SG, Paitz RT, Hicke JW, LaMagdeleine KA, Vogel LA, Bowden RM (2013b) Humoral immune responses are maintained with age in a long-lived ectotherm, the red-eared slider turtle. J Exp Biol 216:633–640

    Article  CAS  PubMed  Google Scholar 

  • Zimmerman LM, Bowden RM, Vogel LA (2014) A vertebrate cytokine primer for eco-immunologists. Funct Ecol 28:1061–1073

    Article  Google Scholar 

  • Zimmerman LM, Carter AW, Bowden RM, Vogel LA (2017) Immmunocompetence in a long-lived ectothermic vertebrate is temperature dependent but shows no decline in older adults. Functl Ecol 31:1383–1389

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Biological Sciences, Illinois State University, Normal, IL, USA

    Laura A. Vogel, Sarah Palackdharry & Rachel M. Bowden

  2. Biology Department, Millikin University, Decatur, IL, USA

    Laura M. Zimmerman

Authors
  1. Laura A. Vogel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sarah Palackdharry
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laura M. Zimmerman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rachel M. Bowden
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laura A. Vogel .

Editor information

Editors and Affiliations

  1. Division of Geriatrics Research Center on Aging, University of Sherbrooke Dept. of Medicine, Sherbrooke, Québec, Canada

    Tamas Fulop

  2. Dept of Experimental Pathology, University of Bologna, Bologna, Italy

    Claudio Franceschi

  3. Institute for Health and Life Sciences, Tokyo, Japan

    Katsuiku Hirokawa

  4. Center for Medical Research, University of Tübingen, Tübingen, Germany

    Graham Pawelec

Section Editor information

  1. Research Center on Aging, Department of Medicine, Immunology Graduate Programme, Faculty of Medicine, University of Sherbrooke, Sherbrooke, Quebec, Canada

    Tamas Fulop

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG

About this entry

Cite this entry

Vogel, L.A., Palackdharry, S., Zimmerman, L.M., Bowden, R.M. (2018). Humoral Immune Function in Long-Lived Ectotherms, the Reptiles. In: Fulop, T., Franceschi, C., Hirokawa, K., Pawelec, G. (eds) Handbook of Immunosenescence. Springer, Cham. https://doi.org/10.1007/978-3-319-64597-1_84-1

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-64597-1_84-1

  • Received:

  • Accepted:

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-64597-1

  • Online ISBN: 978-3-319-64597-1

  • eBook Packages: Springer Reference Biomedicine and Life SciencesReference Module Biomedical and Life Sciences

Publish with us

Policies and ethics

Search

Navigation