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Gene transcription in polar bears (Ursus maritimus) from disparate populations

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Abstract

Polar bears in the Beaufort (SB) and Chukchi (CS) Seas experience different environments due primarily to a longer history of sea ice loss in the Beaufort Sea. Ecological differences have been identified as a possible reason for the generally poorer body condition and reproduction of Beaufort polar bears compared to those from the Chukchi, but the influence of exposure to other stressors remains unknown. We use molecular technology, quantitative PCR, to identify gene transcription differences among polar bears from the Beaufort and Chukchi Seas as well as captive healthy polar bears. We identified significant transcriptional differences among a priori groups (i.e., captive bears, SB 2012, SB 2013, CS 2013) for ten of the 14 genes of interest (i.e., CaM, HSP70, CCR3, TGFβ, COX2, THRα, T-bet, Gata3, CD69, and IL17); transcription levels of DRβ, IL1β, AHR, and Mx1 did not differ among groups. Multivariate analysis also demonstrated separation among the groups of polar bears. Specifically, we detected transcript profiles consistent with immune function impairment in polar bears from the Beaufort Sea, when compared with Chukchi and captive polar bears. Although there is no strong indication of differential exposure to contaminants or pathogens between CS and SB bears, there are clearly differences in important transcriptional responses between populations. Further investigation is warranted to refine interpretation of potential effects of described stress-related conditions for the SB population.

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References

  • Acevedo-Whitehouse K, Duffus ALJ (2009) Effects of environmental change on wildlife health. Phil Trans R Soc Lond B 364:3429–3438

    Article  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Atwood TC, Peacock E, Burek-Huntington K, Shearn-Bochsler V, Bodenstein B, Durner G, Beckmann K (2015) Prevalence and spatio-temporal variation of an alopecia syndrome detected in polar bears in the southern Beaufort Sea. J Wildl Dis 51:48–59. doi:10.7589/2013-11-301

    Article  PubMed  Google Scholar 

  • Bechshoft TO, Sonne C, Dietz R, Born EW, Muir DCG, Letcher RJ, Novak MA, Henchey E, Meyer JS, Jenssen BM, Villanger GD (2012) Associations between complex OHC mixtures and thyroid and cortisol hormone levels in East Greenland polar bears. Environ Res 116:26–35

    Article  CAS  PubMed  Google Scholar 

  • Bowen L, Aldridge B, Miles AK, Stott JL (2006) Expressed MHC class II genes in sea otters (Enhydra lutris) from geographically disparate populations. Tissue Agn 67:402–408

    Article  CAS  Google Scholar 

  • Bowen L, Schwartz J, Aldridge B, Riva F, Miles AK, Mohr FC, Stott JL (2007) Differential gene expression induced by exposure of captive mink to fuel oil: a model for the sea otter. EcoHealth 4:298–309

    Article  Google Scholar 

  • Bowen L, Miles AK, Murray M, Haulena M, Tuttle J, Van Bonn W, Adams L, Bodkin JL, Ballachey BE, Estes JA, Tinker MT, Keister R, Stott JL (2012) Gene transcription in sea otters (Enhydra lutris); emerging diagnostics in marine mammal and ecosystem health. Mol Ecol Resour 12:67–74. doi:10.1111/j.1755-0998.2011.03060.x

    Article  CAS  PubMed  Google Scholar 

  • Bowen L, Miles AK, Kolden CA, Saarinen JA, Bodkin JL, Murray MJ, Tinker MT (2015) Effects of wildfire on sea otter (Enhydra lutris) gene transcription profiles. Mar Mamm Sci 31:191–210. doi:10.1111/mms.12151

    Article  Google Scholar 

  • Braathen M, Derocher AE, Wiig Ø, Sørmo EG, Lie E, Skaare JU, Jenssen BM (2004) Relationships between PCBs and thyroid hormones and retinol in female and male polar bears. Environ Health Perspect 112:826–833

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bromaghin JF, McDonald TL, Stirling I, Derocher AE, Richardson ES, Regehr EV, Douglas DC, Durner GM, Atwood TC, Amstrup SC (2015) Polar bear population dynamics in the southern Beaufort Sea during a period of sea ice decline. Ecol Appl 25:634–651

    Article  PubMed  Google Scholar 

  • Buckman AH, Veldhoen N, Ellis G, Ford JK, Helbing CC, Ross PS (2011) PCB-associated changes in mRNA expression in killer whales (Orcinus orca) from the NE Pacific Ocean. Enviro Sci Technol 45:10194–10202

    Article  CAS  Google Scholar 

  • Burchiel SW, Luster MI (2001) Signaling by environmental polycyclic aromatic hydrocarbons in human lymphocytes. Clin Immunol 98:2–10

    Article  CAS  PubMed  Google Scholar 

  • Calvert W, Ramsay MA (1998) Evaluation of age determination of polar bears by counts of cementum growth layer groups. Ursus 10:449–453

    Google Scholar 

  • Chen Z, Wang H, Matsumura K, Qian P (2012) Expression of calmodulin and myosin light chain kinase during larval settlement of the barnacle Balanus Amphitrite. PLoS ONE 7:e31337

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cherry SG, Derocher AE, Stirling I, Richardson ES (2009) Fasting physiology of polar bears in relation to environmental change and breeding behavior in the Beaufort Sea. Polar Biol 32:383–391

    Article  Google Scholar 

  • De Maio A (1999) Heat shock proteins: facts, thoughts, and dreams. Shock 11:1–12

    Article  PubMed  Google Scholar 

  • Derocher AE, Lunn NJ, Stirling I (2004) Polar bears in a warming climate. Integr Comp Biol 44:163–176

    Article  PubMed  Google Scholar 

  • Dong L, Ma Q, Whitlock JP Jr (1997) Down-regulation of major histocompatibility complex Q1b gene expression by 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin. J Biol Chem 272:29614–29619

    Article  CAS  PubMed  Google Scholar 

  • Ferguson SH, Stirling I, McLoughlin P (2005) Climate change and ringed seal (Phoca hispida) recruitment in western Hudson Bay. Mar Mamm Sci 21:121–135

    Article  Google Scholar 

  • Fonfara S, Siebert U, Prange A, Colijn F (2007) The impact of stress on cytokine and haptoglobin mRNA expression in blood samples from harbour porpoises (Phocoena phocoena ). J Mar Biol Assoc UK 87:305–311

    Article  CAS  Google Scholar 

  • Ghanem MM, Batelli LA, Mercer RR, Scabilloni JF, Kashon ML, Ma JY, Nath J, Hubbs AF (2006) Apoptosis and Bax expression are increased by coal dust in the polycyclic aromatic hydrocarbon-exposed lung. Environ Health Perspect 114:1367–1373

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Goldsby RA, Kindt TJ, Osborne BA, Kuby J (2003) Immunology, 5th edn. WH Freeman and Company, New York

    Google Scholar 

  • Gregory M, Cyr DG (2003) Effects of environmental contaminants on the endocrine system of marine mammals. In: Vos JG, Ross PS, de Swart RL, van Loveren H, Osterhaus AD (eds) Toxicology of marine mammals, volume 3—systems. Taylor and Francis, New York, pp 67–81

    Google Scholar 

  • Gurish MF, Humbles A, Tao H, Finkelstein S, Boyce JA, Gerard C, Friend DS, Austen KF (2002) CCR3 is required for tissue eosinophilia and larval cytotoxicity after infection with Trichinella spiralis. J Immunol 168:5730–5736

    Article  CAS  PubMed  Google Scholar 

  • Harris SG, Padilla J, Koumas L, Ray D, Phipps RP (2002) Prostaglandins as modulators of immunity. Trends Immunol 23:144–150

    Article  CAS  PubMed  Google Scholar 

  • Iwama GK, Mathilakath MV, Forsyth RB, Ackerman PA (1999) Heat shock proteins and physiological stress in fish. Am Zool 39:901–909

    CAS  Google Scholar 

  • Kallenborn R, Halsall C, Dellong M, Carlsson P (2012) The influence of climate change on the global distribution and fate processes of anthropogenic persistent organic pollutants. J Environ Monit 14:2854–2869

    Article  CAS  PubMed  Google Scholar 

  • Kannan K, Yun SH, Evans TJ (2005) Chlorinated, brominated, and perfluorinated contaminants in livers of polar bears from Alaska. Environ Sci Technol 39:9057–9063

    Article  CAS  PubMed  Google Scholar 

  • Kennerly E, Ballmann A, Martin S, Wolfinger R, Gregory S, Stoskopf M, Gibson G (2008) A gene expression signature of confinement in peripheral blood of red wolves (Canis rufus). Mol Ecol 17:2782–2791. doi:10.1111/j.1365294X.2008.03775.x

    Article  PubMed  Google Scholar 

  • Kibenge MJT, Munir K, Kibenge FSB (2005) Constitutive expression of Atlantic salmon Mx1 protein in CHSE-214 cells confers resistance to infectious salmon Anaemia virus. Virol J 2:75

    Article  PubMed Central  PubMed  Google Scholar 

  • Kringel H, Iburg T, Dawson H, Aasted B, Roepstorff A (2006) A time course study of immunological responses in Trichuris suis infected pigs demonstrates induction of a local type 2 response associated with worm burden. Int J Parasitol 36:915–924

    Article  CAS  PubMed  Google Scholar 

  • Letcher RJ, Bustnes JO, Dietz R, Jenssen BM, Jorgensen EH, Sonne C, Verreault J, Vijayan MM, Gabrielsen GW (2010) Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish. Sci Total Environ 408:2995–3043

    Article  CAS  PubMed  Google Scholar 

  • Lie E, Larsen HJS, Larsen S, Johansen GM, Derocher AE, Lunn NJ, Norstrom RJ, Wiig Ø, Skaare JU (2004) Does high organochlorine (OC) exposure impair the resistance to infection in polar bears (Ursus maritimus)? Part I: effect of OCs on the humoral immunity. J Toxicol Environ Health A 67:555–582

    Article  CAS  PubMed  Google Scholar 

  • Lie E, Larsen HJS, Larsen S, Johansen GM, Derocher AE, Lunn NJ, Norstrom RJ, Wiig Ø, Skaare JU (2005) Does high organochlorine (OC) exposure impair the resistance to infection in polar bears (Ursus maritimus)? Part II: possible effects of OCs on mitogen- and antigen-induced lymphocyte proliferation. J Toxicol Environ Health A 68:457–484

    Article  CAS  PubMed  Google Scholar 

  • Lynch M, Kirkwood R, Mitchell A, Duignan P, Arnould JPY (2011) Prevalence and significance of an alopecia syndrome in Australian fur seals (Arctocephalus pusillus doriferus). J Mamm 92:342–351

    Article  Google Scholar 

  • Martin P, Sanchez-Madrid F (2011) CD69: an unexpected regulator of TH17 cell-driven inflammatory responses. Sci Signal 4:pe14. doi:10.1126/scisignal.2001825

  • McKinney MA, Peacock E, Letcher RJ (2009) Sea ice-associated diet change increases the levels of chlorinated and brominated contaminants in polar bears. Environ Sci Technol 43:4334–4336

    Article  CAS  PubMed  Google Scholar 

  • McKinney MA, Iverson SJ, Fisk AT, Sonne C, Riget FF, Letcher RJ, Arts MT, Born EW, Rosing-Asvid A, Dietz R (2013) Global Change effects on the long-term feeding ecology and contaminant exposures of East Greenland polar bears. Glob Chang Biol 19:2360–2372

    Article  PubMed  Google Scholar 

  • McKinney MA, Atwood T, Dietz R, Sonne C, Iverson SJ, Peacock E (2014) Validation of adipose lipid content as a body condition index for polar bears. Ecol Evol 4:516–527

    Article  PubMed Central  PubMed  Google Scholar 

  • McLoughlin K, Turteltaub K, Bankaitis-Davis D, Gerren R, Siconolfi L, Storm K, Cheronis J, Trollinger D, Macejak D, Tryon V, Bevilacqua M (2006) Limited dynamic range of immune response gene expression observed in healthy blood donors using RT-PCR. Mol Med 12:185–195

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • McPhee ME, Carlstead K (2010) The importance of maintaining natural behaviors in captive mammals. In: Kleiman DG, Thompson KV, Baer CK (eds) Wild mammal in captivity: principles and techniques for zoo management. University of Chicago Press, Illinois, pp 303–313

    Google Scholar 

  • Miles AK, Bowen L, Ballachey B, Bodkin JL, Murray M, Keister RA, Stott JL (2012) Variations of transcript profiles between sea otters (Enhydra lutris) from Prince William Sound, Alaska, and clinically normal reference otters. Mar Ecol Prog Ser 451:201–212

    Article  Google Scholar 

  • Moe SJ, De Schamphelaere K, Clements WH, Sorensen MT, Van den Brink PJ, Liess M (2013) Combined and interactive effects of global climate change and toxicants on populations and communities. Environ Toxicol Chem 32:49–61

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • National Oceanic and Atmospheric Administration (NOAA) (2011) 2011 Arctic seal disease outbreak update on investigation and findings. Alaska, U.S. Department of Commerce http://alaskafisheries.noaa.gov/protectedresources/seals/ice/diseased/factsheet112211

  • Oesch-Bartlomowicz B, Oesch F (2005) Phosphorylation of cytochromes P450: first discovery of a posttranslational modification of a drug-metabolizing enzyme. Biochem Biophys Resour Commun 338:446–449

    Article  CAS  Google Scholar 

  • Parham P (2014) The Immune System, 4th edn. Garland Science, Taylor and Francis Group, LLC, New York

    Google Scholar 

  • Pfirman S, Eicken H, Bauch D, Weeks WF (1995) The potential transport of pollutants by Arctic sea ice. Sci Total Environ 159:129–146

    Article  CAS  Google Scholar 

  • Pfirman S, Kogeler JW, Rigor I (1997) Potential for rapid transport of contaminants from the Kara Sea. Sci Total Environ 202:111–122

    Article  CAS  PubMed  Google Scholar 

  • PreAnalytiX (2009) PAXgene blood RNA Kit handbook, 2nd edn. QIAGEN GmbH for PreAnalytix, Switzerland, pp 37–39

    Google Scholar 

  • Quintana FJ, Basso AS, Iglesias AH, Korn T, Farez MF, Bettelli E, Caccamo M, Oukka M, Weiner HL (2008) Control of Treg and TH17 cell differentiation by the aryl hydrocarbon receptor. Nature 453:65–71

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Ramesh A, Walker SA, Hood DB, Guillen MD, Schneider K, Weyand EH (2004) Bioavailability and risk assessment of orally ingested polycyclic aromatic hydrocarbons. Int J Toxicol 23:301–333

    Article  CAS  PubMed  Google Scholar 

  • Ramsay MA, Stirling I (1988) Reproductive biology and ecology of female polar bears (Ursus maritimus). J Zool 214:601–634

    Article  Google Scholar 

  • Regehr EV, Lunn NJ, Amstrup SC, Stirling I (2007) Effects of earlier sea ice breakup on survival and population size of polar bears in Western Hudson Bay. J Wildl Manag 71:2673–2683

    Article  Google Scholar 

  • Robinson J, Waller M, Parham P, Bodmer JG, Marsh SGE (2001) IMGT/HLA Database—a sequence database for the human major histocompatibility complex. Nucl Acids Res 29:210–213

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rode KD, Amstrup SC, Regehr EV (2010) Reduced body size and cub recruitment in polar bears associated with sea ice decline. Ecol Appl 20:768–782

    Article  PubMed  Google Scholar 

  • Rode KD, Regehr EV, Douglas D, Durner G, Derocher AE, Thiemann G, Budge S (2014) Variation in the nutritional and reproductive ecology of two polar bear populations experiencing sea ice loss. Glob Change Biol 20:76–88. doi:10.1111/gcb.12339

    Article  Google Scholar 

  • Sakshaug E (2004) Primary and secondary production in the Arctic Seas. In: Stein R, MacDonald RW (eds) The organic carbon cycle in the Arctic Ocean. Springer, Berlin, pp 57–81

    Chapter  Google Scholar 

  • Schwartz JA, Aldridge BM, Lasley BL, Snyder PW, Stott JL, Mohr FC (2004a) Chronic fuel oil toxicity in American mink (Mustela vison): systemic and hematological effects of ingestion of a low-concentration of bunker C fuel oil. Toxi Appl Pharm 200:146–158

    Article  CAS  Google Scholar 

  • Schwartz JA, Aldridge BM, Lasley BL, Snyder PW, Stott JL, Mohr FC (2004b) Immunophenotypic and functional effects of bunker C fuel oil on the immune system of American mink (Mustela vison). Vet Immunol Immunopathol 101:179–190

    Article  CAS  PubMed  Google Scholar 

  • Sigler MF, Renner M, Danielson SL, Eisner LB, Lauth RR, Kuletz KJ, Logerwell EA, Hunt GL Jr (2011) Fluxes, fins, and feathers: relationships among the Bering, Chukchi, and Beaufort seas in a time of climate change. Oceanography 24:250–265

    Article  Google Scholar 

  • Simon E, Bytingsvik J, Jonker W, Leonards PEG, de Boer J, Jenssen BM, Lie E, Aars J, Hamers T, Lamoree MH (2011) Blood plasma sample preparation method for the assessment of thyroid hormone-disrupting potency in effect-directed analysis. Environ Sci Technol 45:7936–7944

    Article  CAS  PubMed  Google Scholar 

  • Sonne C (2010) Health effects from long-range transported contaminants in Arctic top predators: an integrated review based on studies of polar bears and relevant model species. Environ Int 36:461–491

    Article  CAS  PubMed  Google Scholar 

  • Stirling I, Thiemann GW, Richardson E (2008) Quantitative support for a subjective fatness index for immobilized polar bears. J Wildl Manag 72:568–574

    Article  Google Scholar 

  • Stroeve JC, Markus T, Boisvert L, Miller J, Barrett A (2014) Changes in Arctic melt seasons and implications for sea ice loss. Geophys Res Lett 41:1216–1225. doi:10.1002/2013GL058951

    Article  Google Scholar 

  • Tabuchi M, Veldhoen N, Dangerfield N, Jeffries S, Helbing CC, Ross PS (2006) PCB-related alteration of thyroid hormones and thyroid hormone receptor gene expression in free-ranging harbor seals (Phoca vitulina). Environ Health Perspect 114:1024–1031

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tsai MJ, O’Malley BW (1994) Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu Rev Biochem 63:451–486

    Article  CAS  PubMed  Google Scholar 

  • Tsan MF, Gao B (2004) Cytokine function of heat shock proteins. Am J Physiol-Cell Physiol 286:C739–C744

    Article  CAS  PubMed  Google Scholar 

  • Tumpey TM, Szretter KJ, Hoeven NV, Katz JM, Kochs G, Haller O, García-Sastre A, Staeheli P (2007) The Mx1 gene protects mice against the pandemic 1918 and highly lethal human H5N1 influenza viruses. J Virol 81:10818–10821

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Veldhoen M, Hirota K, Westendorf AM, Buer J, Dumoutier L, Renauld JC, Stockinger B (2008) The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 453:106–109

    Article  CAS  PubMed  Google Scholar 

  • Vijayan MM, Aluru N, Maule AG, Jørgensen EH (2006) Fasting augments PCB impact on liver metabolism in anadromous arctic char. Tox Sci 91:431–439

    Article  CAS  Google Scholar 

  • Vongraven D, Aars J, Amstrup SC, Atkinson SN, Belikov S, Born EW, DeBruyn T, Derocher AE, Gill M, Lunn NJ, Obbard ME, Omelak J, Ovsyanikov NG, Peacock E, Richardson E, Sahanatien V, Stirling I, Wiig Ø (2012) A circumpolar monitoring framework for polar bears. Ursus 23:1–66

    Article  Google Scholar 

  • Wegner KM, Kalbe M, Rauch G, Kurtz J, Schaschl H, Reusch TBH (2006) Genetic variation in MHC class II expression and interactions with MHC sequence polymorphism in three-spined sticklebacks. Mol Ecol 15:1153–1164

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Funding was provided by the U.S. Geological Survey’s Changing Arctic Ecosystems Initiative. We are grateful for the contributions of the veterinarians to the Anchorage Zoo, SeaWorld San Diego, Brookfield Zoo, Cleveland Metroparks Zoo, SeaWorld Orlando, Louisville Zoo, Detroit Zoo, Kansas City Zoo, Omaha Henry Doorly Zoo, Buffalo City Zoo, Toledo Zoo, Columbus Zoo, Oregon Zoo, and Point Defiance Zoo and Aquarium. Samples were provided by the zoos and aquaria under the expressed permission of the US Fish and Wildlife Service, and under the Animal Care Committee protocols established at each of the aquaria. Mention of trade names or organizations does not imply endorsement by the US government.

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Bowen, L., Miles, A.K., Waters, S. et al. Gene transcription in polar bears (Ursus maritimus) from disparate populations. Polar Biol 38, 1413–1427 (2015). https://doi.org/10.1007/s00300-015-1705-0

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