Predator odor induces genome instability in the mouse bone marrow cells
- Authors: Glinin T.S1, Starshova P.A1, Shubina V.A1, Anisimova M.V2, Bondarenko A.A1, Moshkin M.P2, Daev E.V1
-
Affiliations:
- St Petersburg State University
- Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences
- Issue: Vol 15, No 1 (2017)
- Pages: 4-11
- Section: Articles
- URL: https://journals.rcsi.science/ecolgenet/article/view/6296
- DOI: https://doi.org/10.17816/ecogen1514-11
- ID: 6296
Cite item
Full Text
Abstract
Background. Long coevolution of prey and predator species of mammals creates specific mechanisms of their interaction, e. g. prey’s innate behavior aversive to the predator odor. However, little is known about genetic responses in the prey organism. We assessed genome instability of the bone marrow cells in mice affected by the cat’s odor influence, and proposed pathway of such action.
Materials and methods. CBA mouse males were exposed to volatiles from adult cat urine for 2 or 24 hours. To estimate the genetic effect, ana-telophase method of chromosome aberration analysis and comet assay were used. The level of corticosterone was also measured after the exposure for 30 or 60 minutes.
Results. The exposure to cat’s urine volatiles for 2 hours induced damage of DNA in bone marrow cells of the mouse males as was shown by the DNA comet analysis. The exposure for 24 hours elevated the frequency of chromosome aberrations in mitotically dividing cells at ana-telophase stage. No significant changes were found in the level of corticosterone in the peripheral blood.
Conclusion. We have shown that volatile chemosignals from predator’s urine induce genomic instability in bone marrow cells of a prey. The hormonal pathway of such influence is still unknown. Intraorganismic paths leading to genome damage are discussed as well as far consequences of discovered effects.
Full Text
##article.viewOnOriginalSite##About the authors
Timofey S Glinin
St Petersburg State University
Author for correspondence.
Email: t.glinin@gmail.com
PhD student. Department of Genetics and Biotechnology
Russian Federation, Saint Petersburg, RussiaPolina A Starshova
St Petersburg State University
Email: pstrsh@gmail.com
student. Department of Genetics and Biotechnology
Russian Federation, Saint Petersburg, RussiaVictoria A Shubina
St Petersburg State University
Email: vicktory.shubina@gmail.com
student. Department of Genetics and Biotechnology
Russian Federation, Saint Petersburg, RussiaMargarita V Anisimova
Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences
Email: anisimova@bionet.nsc.ru
PhD student. Department of Genetic Resources of Experimental Animals
Russian Federation, Novosibirsk, RussiaAnton A Bondarenko
St Petersburg State University
Email: emptybox1267@gmail.com
student. Department of Genetics and Biotechnology
Russian Federation, Saint Petersburg, RussiaMikhail P Moshkin
Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences
Email: mmp@bionet.nsc.ru
Dr. of Sci. Department of Genetic Resources of Experimental Animals
Russian Federation, Novosibirsk, RussiaEugene V Daev
St Petersburg State University
Email: mouse_gene@mail.ru
Professor, Department of Genetics and Biotechnology
Russian Federation, Saint Petersburg, RussiaReferences
- Sewards TV, Sewards MA. Innate visual object recognition in vertebrates: Some proposed pathways and mechanisms. Comparative Biochemistry and Physiology. A Molecular and Integrative Physiology. 2002;132(4):861-891. doi: 10.1016/S1095-6433(02)00119-8.
- Banks PB, Norrdahl K, Korpimäki E. Mobility decisions and the predation risks of reintroduction. Biological Conservation. 2002;103(2):133-138. doi: 10.1016/S0006-3207(01)00110-0.
- Apfelbach R, Blanchard CD, Blanchard RJ, et al. The effects of predator odors in mammalian prey species: A review of field and laboratory studies. Neuroscience and Biobehavioral Reviews. 2005;29(8):1123-1144. doi: 10.1016/j.neubiorev.2005.05.005.
- Curio E. The functional organization of anti-predator behaviour in the pied flycatcher: A study of avian visual perception. Animal Behaviour. 1975;32(1):1-12. doi: 10.1016/0003-3472(75)90056-1.
- Hegab IM, Kong S, Yang S, et al. The ethological relevance of predator odors to induce changes in prey species. Acta Ethologica. 2014;18(1):1-9. doi: 10.1007/s10211-014-0187-3.
- Kavaliers M, Choleris E, Colwell DD. Brief exposure to female odors «emboldens» male mice by reducing predator-induced behavioral and hormonal responses. Hormones and behavior. 2001;40(4):497-509. doi: 10.1006/hbeh.2001.1714.
- Munoz-Abellan C, Armario A, Nadal R. Do odors from different cats induce equivalent unconditioned and conditioned responses in rats? Physiology & Behavior. 2010;99(3):388-394. doi: 10.1016/j.physbeh.2009.12.008.
- Voznessenskaya VV, Malanina TV. Effect of chemical signals from a predator (Felis catus) on the reproduction of Mus musculus. Doklady. Biological Sciences. 2013;453(1):362-364. doi: 10.1134/S0012496613060057.
- Vasilieva NY, Cherepanova EV, Von Holst D, Apfelbach R. Predator odour and its impact on male fertility and reproduction in Phodopus campbelli hamsters. Naturwissenschaften. 2000;87(7):312-314. doi: 10.1007/s001140050728.
- Novotny M, Jemiolo B, Harvey S, et al. Adrenal-mediated endogenous metabolites inhibit puberty in female mice. Science. 1986;231(4739):722-725. doi: 10.1126/science.3945805.
- Daev EV, Kazarova VE, Vyborova AM, Dukel’skaya AV. Effects of “Pheromone-Like” pyrazine-containing compounds on stability of genetic apparatus in bone marrow cells of the male house mouse Mus musculus L. Journal of Evolutionary Biochemistry and Physiology. 2009;45(5):589-595. doi: 10.1134/S0022093009050053.
- Daev EV. Genetic consequences of olfactory stresses in mice. St Petersb. Gos. Univ. [dissertation] Saint Petersburg; 2006.
- Sasaki YF, Sekihashi K, Izumiyama F, Nishidate E, et al. The Comet Assay with Multiple Mouse Organs: Comparison of Comet Assay Results and Carcinogenicity with 208 Chemicals Selected from the IARC Monographs and U.S. NTP Carcinogenicity Database. Critical Reviews in Toxicology. 2000;30(6):629-799. doi: 10.1080/10408440008951123.
- Дурнев А.Д., Жанатаев А.К., Анисина Е.А., и др. Применение метода щелочного гель-электрофореза изолированных клеток для оценки генотоксических свойств природных и синтетических соединений: Методические рекомендации. – М., 2006 [Durnev AD, Zhanataev AK, Anisina EA, et al. Primenenie metoda shchelochnogo gel’-elektroforeza izolirovannykh kletok dlya otsenki genotoksicheskikh svoistv prirodnykh i sinteticheskikh soedinenii: Metodicheskie rekomendatsii. Moscow; 2006. (In Russ.)]
- Макаров В.Б., Сафронов В.В. Цитогенетические методы анализа хромосом. – М.: Наука, 1978. – С. 85. [Makarov VB, Safronov VV. Cytogenetic Methods of Chromosome Analysis. Moscow: Nauka; 1978. P. 85. (In Russ.)]
- Глотов Н.В., Животовский Л.А., Хованов Н.В., Хромов-Борисов Н.Н. Биометрия. – Л.: Изд-во ЛГУ, 1982. – С. 264. [Glotov NV, Zhivotovskii LA, Khovanov NV, Khromov-Borisov NN. Biometry. Leningrad: Izdatelstvo LGU; 1982. P. 264. (In Russ.)]
- McGregor IS, Schrama L, Ambermoon P, Dielenberg RA. Not all ‘predator odours’ are equal: cat odour but not 2,4,5 trimethylthiazoline (TMT; fox odour) elicits specific defensive behaviours in rats. Behavioural Brain Research. 2002;129(1-2):1-16. doi: 10.1016/S0166-4328(01)00324-2.
- Bowen MT, Keats K, Kendig MD, et al. Aggregation in quads but not pairs of rats exposed to cat odor or bright light. Behavioural Processes. 2012;90(3):331-336. doi: 10.1016/j.beproc.2012.03.014.
- Xu HY, Liu YJ, Xu MY, et al. Inactivation of the bed nucleus of the stria terminalis suppresses the innate fear responses of rats induced by the odor of cat urine. Neuroscience. 2012;221:21-27. doi: 10.1016/j.neuroscience.2012.06.056.
- Hegab IM, Wang A, Yin B, et al. Behavioral and neuroendocrine response of Brandt’s voles, Lasiopodomys brandtii, to odors of different species. European Journal of Wildlife Research. 2014;60(2):331-340. doi: 10.1007/s10344-013-0790-z.
- De Oliveira Crisanto K, de Andrade Wylqui MG, de Azevedo Silva KD, et al. The differential mice response to cat and snake odor. Physiology and Behavior. 2015;152: 272-279. doi: 10.1016/j.physbeh.2015.10.013.
- Dent CL, Isles AR, Humby T. Measuring risk-taking in mice: Balancing the risk between seeking reward and danger. European Journal of Neuroscience. 2014;39(4):520-530. doi: 10.1111/ejn.12430.
- Hacquemand R, Choffat N, Jacquot L, Brand G. Comparison between low doses of TMT and cat odor exposure in anxiety- and fear-related behaviors in mice. Behavioural Brain Research. 2013;238(1):227-231. doi: 10.1016/j.bbr.2012.10.014.
- Papes F, Logan DW, Stowers L. The Vomeronasal Organ Mediates Interspecies Defensive Behaviors through Detection of Protein Pheromone Homologs. Cell. 2010;141(4):692-703. doi: 10.1016/j.cell.2010.03.037.
- Mikhailov VM, Vezhenkova IV. Double-strand Breaks of DNA of C57BL and mdx Mouse Cardiomyocytes after Dynamic Stress. Cell and Tissue Biology. 2007;1(4): 328-333. doi: 10.1134/S1990519X07040049.
- Aguilera A, García-Muse T. Causes of Genome Instability. Annual Review of Genetics. 2013;47:1-32. doi: 10.1146/annurev-genet-111212-133232.
- Meijer L, Guidet S, Vogel L. Progress in cell cycle research. Springer Science & Bussines Media. 2012:284.
- Roy V, Belzung C, Delarue C, Chapillon P. Environmental enrichment in BALB/c mice: Effects in classical tests of anxiety and exposure to a predatory odor. Physiology and Behavior. 2001;74(3):313-320. doi: 10.1016/S0031-9384(01)00561-3.
- Sotnikov SV, Markt PO, Umriukhin AE, Landgraf R. Genetic predisposition to anxiety-related behavior predicts predator odor response. Behavioural Brain Research. 2011;225(1):230-234. doi: 10.1016/j.bbr.2011.07.022.
- Flint MS, Baum A, Chambers WH, Jenkins FJ. Induction of DNA damage, alteration of DNA repair and transcriptional activation by stress hormones. Psychoneuroendocrinology. 2007;32(5):470-479. doi: 10.1016/j.psyneuen.2007.02.013.
- Munoz-Abellan C, Andero R, Nadal R, Armario A. Marked dissociation between hypothalamic-pituitary-adrenal activation and long-term behavioral effects in rats exposed to immobilization or cat odor. Psychoneuroendocrinology. 2008;33(8):1139-1150. doi: 10.1016/j.psyneuen.2008.06.002.
- File SE, Zangrossi H, Sanders FL, Mabbutt PS. Dissociation between behavioral and corticosterone responses on repeated exposures to cat odor. Physiology and Behavior. 1993;54(6):1109-1111. doi: 10.1016/0031-9384(93)90333-B.
- Munoz-Abellan C, Daviu N, Rabasa C, et al. Cat odor causes long-lasting contextual fear conditioning and increased pituitary-adrenal activation, without modifying anxiety. Hormones and Behavior. 2009;56(4):465-471. doi: 10.1016/j.yhbeh.2009.08.002.
- Hara MR, Kovacs JJ, Whalen EJ, et al. A stress response pathway regulates DNA damage through β2-adrenoreceptors and β-arrestin-1. Nature. 2011; 477(7364):349-353. doi: 10.1038/nature10368.
- Hara MR, Sachs BD, Caron MG, Lefkowitz RJ. Pharmacological blockade of a β2AR-β-arrestin-1 signaling cascade prevents the accumulation of DNA damage in a behavioral stress model. Cell Cycle. 2013;12(2): 219-224. doi: 10.4161/cc.23368.
- Daev EV, Vorob’ev KV, Shustova TI, et al. Genotype-Specific Changes in Functional Parameters of Immunocompetent Cells in Laboratory Male Mice under Conditions of Pheromoneal Stress. Russian Journal of Genetics. 2000;36(8):872-876.
- Daev EV. Stress, chemocommunication, and the physiological hypothesis of mutation. Russian Journal of Genetics. 2000;43(10):1082-0392. doi: 10.1134/S102279540710002X.
- Cha HJ, Yim H. The accumulation of DNA repair defects is the molecular origin of carcinogenesis. Tumor Biology. 2013;34(6):3293-3302. doi: 10.1007/s13277-013-1038-y.
- Moskalev AA, Shaposhnikov MV, Plyusnina EN, et al. The role of DNA damage and repair in aging through the prism of Koch-like criteria. Ageing Research Reviews. 2013;12(2):661-684. doi: 10.1016/j.arr.2012.02.001.
- Flach J, Bakker ST, Mohrin M, et al. Replication stress is a potent driver of functional decline in ageing haematopoietic stem cells. Nature. 2013;512(7513): 198-202. doi: 10.1038/nature13619.
Supplementary files
![](/img/style/loading.gif)