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Adrenocortical Expression Profiling of Cattle with Distinct Juvenile Temperament Types

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Abstract

Temperament affects ease of handling, animal welfare, and economically important production traits in cattle. The use of gene expression profiles as molecular traits provides a novel means of gaining insight into behavioural genetics. In this study, differences in adrenocortical expression profiles between 60 F2 cows (Charolais × German Holstein) of distinct temperament types were analysed. The cows were assessed in a novel-human test at an age of 90 days. Most of the adrenal cortex transcripts which were differentially expressed (FDR <0.05) were found between temperament types of ‘fearful/neophobic-alert’ and all other temperament types. These transcripts belong to several biological functions like NRF2-mediated oxidative stress response, Glucocorticoid Receptor Signalling and Complement System. Overall, the present study provides new insight into transcriptional differences in the adrenal cortex between cows of distinct temperament types. Genetic regulations of such molecular traits facilitate uncovering positional and functional gene candidates for temperament type in cattle.

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References

  • Adamczyk K, Pokorska J, Makulska J, Earley B, Mazurek M (2013) Genetic analysis and evaluation of behavioural traits in cattle. Livest Sci 154:1–12

    Article  Google Scholar 

  • Affymetrix (2007) Quality assessment of exon and gene arrays. (Affymetrix GeneChip® Gene and Exon Array Whitepaper Collection):1–18

  • Bamberger CM, Schulte HM, Chrousos GP (1996) Molecular determinants of glucocorticoid receptor function and tissue sensitivity to glucocorticoids. Endocr Rev 17(3):245–261

    Article  PubMed  Google Scholar 

  • Brain PF (1972) Mammalian behavior and the adrenal cortex—a review. Behav Biol 7(4):453–477

    Article  PubMed  Google Scholar 

  • Brand B, Hadlich F, Brandt B, Schauer N, Graunke KL, Langbein J, Repsilber D, Ponsuksili S, Schwerin M (2015) Temperament type specific metabolite profiles of the prefrontal cortex and serum in cattle. PLoS ONE 10(4):e0125044

    Article  PubMed  PubMed Central  Google Scholar 

  • Briassoulis G, Damjanovic S, Xekouki P, Lefebvre H, Stratakis CA (2011) The glucocorticoid receptor and its expression in the anterior pituitary and the adrenal cortex: a source of variation in hypothalamic-pituitary-adrenal axis function; implications for pituitary and adrenal tumors. Endocr Pract 17(6):941–948

    Article  PubMed  PubMed Central  Google Scholar 

  • Burdick NC, Carroll JA, Hulbert LE, Dailey JW, Willard ST, Vann RC, Welsh TH Jr, Randel RD (2010) Relationships between temperament and transportation with rectal temperature and serum concentrations of cortisol and epinephrine in bulls. Livest Sci 129:166–172

    Article  Google Scholar 

  • Burdick NC, Carroll JA, Randel RD, Willard ST, Vann RC, Chase CC Jr, Lawhon SD, Hulbert LE, Welsh TH Jr (2011a) Influence of temperament and transportation on physiological and endocrinological parameters in bulls. Livest Sci 139:213–221

    Article  Google Scholar 

  • Burdick NC, Randel RD, Carroll JA, Welsh TH Jr (2011b) Interactions between temperament, stress, and immune funtion in cattle. Int J Zool 2011:1–9

    Article  Google Scholar 

  • Bureau C, Hennequet-Antier C, Couty M, Guemene D (2009) Gene array analysis of adrenal glands in broiler chickens following ACTH treatment. BMC Genom 10:430

    Article  Google Scholar 

  • Cafe LM, Robinson DL, Ferguson DM, Geesink GH, Greenwood PL (2011) Temperament and hypothalamic-pituitary-adrenal axis function are related and combine to affect growth, efficiency, carcass, and meat quality traits in Brahman steers. Domest Anim Endocrinol 40(4):230–240

    Article  PubMed  Google Scholar 

  • Charmandari E, Tsigos C, Chrousos G (2005) Endocrinology of the stress response. Annu Rev Physiol 67:259–284

    Article  PubMed  Google Scholar 

  • Curley KO Jr, Neuendorff DA, Lewis AW, Cleere JJ, Welsh TH Jr, Randel RD (2008) Functional characteristics of the bovine hypothalamic-pituitary-adrenal axis vary with temperament. Horm Behav 53(1):20–27

    Article  PubMed  Google Scholar 

  • Dewing P, Ching ST, Zhang YH, Huang BL, Peirce RM, McCabe ER, Vilain E (2000) Midkine is expressed early in rat fetal adrenal development. Mol Genet Metab 71(4):616–622

    Article  PubMed  Google Scholar 

  • Eadie BD, Zhang WN, Boehme F, Gil-Mohapel J, Kainer L, Simpson JM, Christie BR (2009) Fmr1 knockout mice show reduced anxiety and alterations in neurogenesis that are specific to the ventral dentate gyrus. Neurobiol Dis 36(2):361–373

    Article  PubMed  Google Scholar 

  • Filiou MD, Zhang Y, Teplytska L, Reckow S, Gormanns P, Maccarrone G, Frank E, Kessler MS, Hambsch B, Nussbaumer M, Bunck M, Ludwig T, Yassouridis A, Holsboer F, Landgraf R, Turck CW (2011) Proteomics and metabolomics analysis of a trait anxiety mouse model reveals divergent mitochondrial pathways. Biol Psychiatr 70(11):1074–1082

    Article  Google Scholar 

  • Filiou MD, Asara JM, Nussbaumer M, Teplytska L, Landgraf R, Turck CW (2014) Behavioral extremes of trait anxiety in mice are characterized by distinct metabolic profiles. J Psychiatr Res 58:115–122

    Article  PubMed  Google Scholar 

  • Friedrich J, Brand B, Ponsuksili S, Graunke KL, Langbein J, Knaust J, Kuehn C, Schwerin M (2016) Detection of genetic variants affecting cattle behaviour and their impact on milk production: a genome-wide association study. Anim Genet 47(1):12–18

    Article  PubMed  Google Scholar 

  • Graunke KL, Nuernberg G, Repsilber D, Puppe B, Langbein J (2013) Describing temperament in an ungulate: a multidimensional approach. PLoS ONE 8(9):e74579

    Article  PubMed  PubMed Central  Google Scholar 

  • Grignard L, Boivin X, Boissy A, Le Neindre P (2001) Do beef cattle react consistently to different handling situations? Appl Anim Behav Sci 71:263–276

    Article  PubMed  Google Scholar 

  • Hall NL, Buchanan DS, Anderson VL, Ilse BR, Carlin KR, Berg EP (2011) Working chute behavior of feedlot cattle can be an indication of cattle temperament and beef carcass composition and quality. Meat Sci 89(1):52–57

    Article  PubMed  Google Scholar 

  • Hammon HM, Bellmann O, Voigt J, Schneider F, Kühn C (2007) Glucose-dependent insulin response and milk production in heifers within a segregating resource family population. J Dairy Sci 90(7):3247–3254

    Article  PubMed  Google Scholar 

  • Hammon HM, Metges CC, Schulz A, Junghans P, Schneider F, Pfuhl R, Bruckmaier RM, Weikard R, Kühn C (2010) Differences in milk production, glucose metabolism, and carcass composition of 2 Charolais × Holstein F2 families derived from reciprocal paternal and maternal grandsire crosses. J Dairy Sci 93:3007–3018

    Article  PubMed  Google Scholar 

  • Hazard D, Liaubet L, Sancristobal M, Mormede P (2008) Gene array and real time PCR analysis of the adrenal sensitivity to adrenocorticotropic hormone in pig. BMC Genom 9:101

    Article  Google Scholar 

  • Hemsworth PH, Coleman GJ, Barnett JL, Borg S (2000) Relationships between human–animal interactions and productivity of commercial dairy cows. J Anim Sci 78(11):2821–2831

    Article  PubMed  Google Scholar 

  • Hoppe S, Brandt HR, König S, Erhardt G, Gauly M (2010) Temperament traits of beef calves measured under field conditions and their relationships to performance. J Anim Sci 88(6):1982–1989

    Article  PubMed  Google Scholar 

  • Hughes HD, Carroll JA, Burdick Sanchez NC, Richeson JT (2014) Natural variations in the stress and acute phase responses of cattle. Innate Immun 20(8):888–896

    Article  PubMed  Google Scholar 

  • Ishimoto H, Muench MO, Higuchi T, Minegishi K, Tanaka M, Yoshimura Y, Jaffe RB (2006) Midkine, a heparin-binding growth factor, selectively stimulates proliferation of definitive zone cells of the human fetal adrenal gland. J Clin Endocrinol Metab 91(10):4050–4056

    Article  PubMed  Google Scholar 

  • Johnston TD, Edwards L (2002) Genes, interactions, and the development of behavior. Psychol Rev 109(1):26–34

    Article  PubMed  Google Scholar 

  • Joyce AR, Palsson BO (2006) The model organism as a system: integrating ‘omics’ data sets. Nat Rev Mol Cell Biol 7(3):198–210

    Article  PubMed  Google Scholar 

  • King DA, Schuehle Pfeiffer CE, Randel RD, Welsh TH Jr, Oliphint RA, Baird BE, Curley KO Jr, Vann RC, Hale DS, Savell JW (2006) Influence of animal temperament and stress responsiveness on the carcass quality and beef tenderness of feedlot cattle. Meat Sci 74(3):546–556

    Article  PubMed  Google Scholar 

  • Koolhaas JM, de Boer SF, Coppens CM, Buwalda B (2010) Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Front Neuroendocrinol 31(3):307–321

    Article  PubMed  Google Scholar 

  • Kühn C, Bellmann O, Voigt J, Wegner J, Guiard V, Ender K (2002) An experimental approach for studying the genetic and physiological background of nutrient transformation in cattle with respect to nutrient secretion and accretion type. Arch Tierz 45:317–330

    Google Scholar 

  • Mackay JR, Haskell MJ (2015) Consistent individual behavioral variation: the difference between temperament, personality and behavioral syndromes. Animals 5(3):455–478

    Article  PubMed  PubMed Central  Google Scholar 

  • Mazurek M, McGee M, Crowe MA, Prendiville DJ, Boivin X, Earley B (2011) Consistency and stability of behavioural fear responses of heifers to different fear-eliciting situations involving humans. Appl Anim Behav Sci 131:21–28

    Article  Google Scholar 

  • McClintick JN, Edenberg HJ (2006) Effects of filtering by present call on analysis of microarray experiments. BMC Bioinform 7:49

    Article  Google Scholar 

  • Müller R, Schrader L (2005) Behavioural consistency during social separation and personality in dairy cows. Behaviour 142:1289–1306

    Article  Google Scholar 

  • Muráni E, Ponsuksili S, D’Eath RB, Turner SP, Evans G, Tholking L, Kurt E, Klont R, Foury A, Mormede P, Wimmers K (2011) Differential mRNA expression of genes in the porcine adrenal gland associated with psychosocial stress. J Mol Endocrinol 46(3):165–174

    Article  PubMed  Google Scholar 

  • Nakamura E, Kadomatsu K, Yuasa S, Muramatsu H, Mamiya T, Nabeshima T, Fan QW, Ishiguro K, Igakura T, Matsubara S, Kaname T, Horiba M, Saito H, Muramatsu T (1998) Disruption of the midkine gene (Mdk) resulted in altered expression of a calcium binding protein in the hippocampus of infant mice and their abnormal behaviour. Genes Cells 3(12):811–822

    Article  PubMed  Google Scholar 

  • Nkrumah JD, Crews DH Jr, Basarab JA, Price MA, Okine EK, Wang Z, Li C, Moore SS (2007) Genetic and phenotypic relationships of feeding behavior and temperament with performance, feed efficiency, ultrasound, and carcass merit of beef cattle. J Anim Sci 85:2382–2390

    Article  PubMed  Google Scholar 

  • O’Loughlin A, Lynn DJ, McGee M, Doyle S, McCabe M, Earley B (2012) Transcriptomic analysis of the stress response to weaning at housing in bovine leukocytes using RNA-seq technology. BMC Genom 13:250

    Article  Google Scholar 

  • Ponsuksili S, Zebunke M, Murani E, Trakooljul N, Krieter J, Puppe B, Schwerin M, Wimmers K (2015) Integrated Genome-wide association and hypothalamus eQTL studies indicate a link between the circadian rhythm-related gene PER1 and coping behavior. Sci Rep 5:16264

    Article  PubMed  PubMed Central  Google Scholar 

  • Prasad R, Kowalczyk JC, Meimaridou E, Storr HL, Metherell LA (2014) Oxidative stress and adrenocortical insufficiency. J Endocrinol 221(3):R63–R73

    Article  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2014) R: A language and environment for statistical computing

  • Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82(2):291–318

    Article  PubMed  Google Scholar 

  • Reimert I, Bolhuis JE, Kemp B, Rodenburg TB (2014) Social support in pigs with different coping styles. Physiol Behav 129:221–229

    Article  PubMed  Google Scholar 

  • Salak-Johnson JL, McGlone JJ (2007) Making sense of apparently conflicting data: stress and immunity in swine and cattle. J Dairy Sci 85(13 Suppl):E81–E88

    Google Scholar 

  • Sewalem A, Miglior F, Kistemaker GJ (2011) Genetic parameters of milking temperament and milking speed in Canadian Holsteins. J Dairy Sci 94(1):512–516

    Article  PubMed  Google Scholar 

  • Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Rev Biol 79(3):241–277

    Article  Google Scholar 

  • Spiers JG, Chen HJ, Sernia C, Lavidis NA (2014) Activation of the hypothalamic-pituitary-adrenal stress axis induces cellular oxidative stress. Front Neurosci 8:456

    PubMed  Google Scholar 

  • Sutherland MA, Rogers AR, Verkerk GA (2012) The effect of temperament and responsiveness towards humans on the behavior, physiology and milk production of multi-parous dairy cows in a familiar and novel milking environment. Physiol Behav 107(3):329–337

    Article  PubMed  Google Scholar 

  • Terlouw EMC, Bourguet C, Deiss V (2012) Stress at slaughter in cattle: role of reactivity profile and environmental factors. Anim Welf 21(S2):43–49

    Article  Google Scholar 

  • van Reenen CG, Van der Werf JTN, O’Connell NE, Heutinck LFM, Spoolder HAM, Jones RB, Koolhaas JM, Blokhuis HJ (2013) Behavioural and physiological responses of heifer calves to acute stressors: long-term consistency and relationship with adult reactivity to milking. Appl Anim Behav Sci 147:55–68

    Article  Google Scholar 

  • Vetters MDD, Engle TE, Ahola JK, Grandin T (2013) Comparison of flight speed and exit score as measurements of temperament in beef cattle. J Anim Sci 91:374–381

    Article  PubMed  Google Scholar 

  • Whistler T, Chiang C, Lin J, Lonergan W, Reeves WC (2010) The comparison of different pre- and post-analysis filters for determination of exon-level alternative splicing events using affymetrixs arrays. J Biomol Tech 21(1):44–53

    PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work is part of the project “PHENOMICS—a system biological approach of genotype-phenotype-distinction in the context of farm animal performance, health and welfare in cattle and pig” (0315536A) (http://www.phaenomics.auf.uni-rostock.de/en-home.html) funded by the German Federal Ministry of Education and Research (BMBF). The funders had no role in study design, data collection, analysis and interpretation, preparation of the manuscript or decision to publish. The authors want to thank all colleagues at the FBN Dummerstorf involved in rearing and investigating the SEGFAM population.

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Authors and Affiliations

  1. Institute for Farm Animal Research and Technology, University of Rostock, Rostock, Germany

    Juliane Friedrich & Manfred Schwerin

  2. Institute for Genome Biology, Leibniz Institute for Farm Animal Biology, Wilhelm-Stahl-Allee 2, 18196, Dummerstorf, Germany

    Bodo Brand, Manfred Schwerin & Siriluck Ponsuksili

  3. Institute for Behavioural Physiology, Leibniz Institute for Farm Animal Biology, Dummerstorf, Germany

    Katharina Luise Graunke & Jan Langbein

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  1. Juliane Friedrich
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  3. Katharina Luise Graunke
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Correspondence to Siriluck Ponsuksili.

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Conflict of interest

Juliane Friedrich, Bodo Brand, Katharina Luise Graunke, Jan Langbein, Manfred Schwerin, Siriluck Ponsuksili declare that they have no conflict of interest.

Human and animals rights and informed consent

The experimental procedures were carried out according to the animal care guidelines of the State Mecklenburg-Vorpommern, Germany and were approved by the Landesamt für Landwirtschaft, Lebensmittelsicherheit und Fischerei Mecklenburg-Vorpommern (Reference Number: LVL M-V/310-4/7221.3-2.1-017/03).

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Friedrich, J., Brand, B., Graunke, K.L. et al. Adrenocortical Expression Profiling of Cattle with Distinct Juvenile Temperament Types. Behav Genet 47, 102–113 (2017). https://doi.org/10.1007/s10519-016-9816-0

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  • DOI: https://doi.org/10.1007/s10519-016-9816-0

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