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Effects of environmental enrichment and regrouping on natural autoantibodies-binding danger and neural antigens in healthy pigs with different individual characteristics

Published online by Cambridge University Press:  06 April 2017

L. Luo ,
R. Geers ,
I. Reimert ,
B. Kemp ,
H. K. Parmentier  and
J. E. Bolhuis
L. Luo
Affiliation:
Adaptation Physiology Group, Department of Animal Sciences, Wageningen University & Research, PO Box 338, 6700 AH, Wageningen, The Netherlands
R. Geers
Affiliation:
Adaptation Physiology Group, Department of Animal Sciences, Wageningen University & Research, PO Box 338, 6700 AH, Wageningen, The Netherlands
I. Reimert
Affiliation:
Adaptation Physiology Group, Department of Animal Sciences, Wageningen University & Research, PO Box 338, 6700 AH, Wageningen, The Netherlands
B. Kemp
Affiliation:
Adaptation Physiology Group, Department of Animal Sciences, Wageningen University & Research, PO Box 338, 6700 AH, Wageningen, The Netherlands
H. K. Parmentier
Affiliation:
Adaptation Physiology Group, Department of Animal Sciences, Wageningen University & Research, PO Box 338, 6700 AH, Wageningen, The Netherlands
J. E. Bolhuis*
Affiliation:
Adaptation Physiology Group, Department of Animal Sciences, Wageningen University & Research, PO Box 338, 6700 AH, Wageningen, The Netherlands
*
†E-mail: liesbeth.bolhuis@wur.nl
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Abstract

Pigs living in commercial husbandry systems may experience both acute stress due to standard management procedures and chronic stress through limitations in their barren housing environment. This might influence their immune status, including antibody responses to neural and danger autoantigens. Levels of natural autoantibody (NAAb)-binding phosphorylcholine-conjugated bovine serum albumin (PC-BSA) and myelin basic protein (MBP) were measured over time in pigs that were kept in environmental enriched v. barren housing, and that underwent a regrouping test. In total, 480 pigs were housed in 80 pens in either barren or straw-enriched pens from 4 through 23 weeks of age. Blood samples were taken from pigs before (week 8), and 3 days after a 24 h regrouping test (week 9), and at 22 weeks of age. Phosphorylcholine-conjugated bovine serum albumin (PC-BSA) and MBP antibody titres in serum were measured using ELISA. Enriched-housed pigs had higher levels of IgM-binding MBP, and tended to have higher levels of IgG-binding MBP and IgA-binding PC-BSA than barren-housed pigs. Each NAAb measured in this study was affected by gender and litter. These results suggest that enriched housing conditions, as well as acute regrouping stress, have an influence on levels of serum NAAb-binding danger and neural antigens in pigs.

Keywords

environmental enrichmentnatural autoantibodypigstressimmunity
Type
Research Article
Information
animal , Volume 11 , Issue 11 , November 2017 , pp. 2019 - 2026
Copyright
© The Animal Consortium 2017 

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References

Abou-Donia, MB, Abou-Donia, MM, ElMasry, EM, Monro, JA and Mulder, MF 2013. Autoantibodies to nervous system-specific proteins are elevated in sera of flight crew members: biomarkers for nervous system injury. Journal of Toxicology and Environmental Health, Part A 76, 363–380.Google Scholar
Andrejević, S, Bukilica, M, Dimitrijević, M, Laban, O, Radulovic, J, Kovacevic-jovanovic, V, Stanojevic, S, Vasiljevic, T and Marković, BM 1997. Stress-induced rise in serum anti-brain autoantibody levels in the rat. International Journal of Neuroscience 89, 153–164.Google Scholar
Bao, M, Bovenhuis, H, Nieuwland, M, Parmentier, H and van der Poel, J 2016. Genetic parameters of IgM and IgG antibodies binding autoantigens in healthy chickens. Poultry Science 95, 458–465.Google Scholar
Bolhuis, JE, Parmentier, HK, Schouten, WG, Schrama, JW and Wiegant, VM 2003. Effects of housing and individual coping characteristics on immune responses of pigs. Physiology & Behavior 79, 289–296.Google Scholar
Bolhuis, JE, Schouten, WG, Schrama, JW and Wiegant, VM 2005. Behavioural development of pigs with different coping characteristics in barren and substrate-enriched housing conditions. Applied Animal Behaviour Science 93, 213–228.CrossRefGoogle Scholar
Bupp, MRG 2015. Sex, the aging immune system, and chronic disease. Cellular Immunology 294, 102–110.Google Scholar
Camerlink, I, Bolhuis, J, Duijvesteijn, N, Van Arendonk, J and Bijma, P 2014. Growth performance and carcass traits in pigs selected for indirect genetic effects on growth rate in two environments. Journal of Animal Science 92, 2612–2619.Google Scholar
Camerlink, I, Turner, SP, Bijma, P and Bolhuis, JE 2013. Indirect genetic effects and housing conditions in relation to aggressive behaviour in pigs. PLoS ONE 8, e65136.CrossRefGoogle ScholarPubMed
Camerlink, I, Ursinus, WW, Bijma, P, Kemp, B and Bolhuis, JE 2015. Indirect genetic effects for growth rate in domestic pigs alter aggressive and manipulative biting behaviour. Behavior Genetics 45, 117–126.Google Scholar
Casali, P and Notkins, AL 1989. Probing the human B-cell repertoire with EBV: polyreactive antibodies and CD5+B lymphocytes. Annual Review of Immunology 7, 513–535.CrossRefGoogle ScholarPubMed
de Jong, IC, Prelle, IT, van de Burgwal, JA, Lambooij, E, Korte, SM, Blokhuis, HJ and Koolhaas, JM 2000. Effects of environmental enrichment on behavioral responses to novelty, learning, and memory, and the circadian rhythm in cortisol in growing pigs. Physiology & Behavior 68, 571–578.Google Scholar
Dhabhar, FS 2014. Effects of stress on immune function: the good, the bad, and the beautiful. Immunologic Research 58, 193–210.Google Scholar
Douglas, C, Bateson, M, Walsh, C, Bédué, A and Edwards, SA 2012. Environmental enrichment induces optimistic cognitive biases in pigs. Applied Animal Behaviour Science 139, 65–73.Google Scholar
Gold, M, Pul, R, Bach, JP, Stangel, M and Dodel, R 2012. Pathogenic and physiological autoantibodies in the central nervous system. Immunological Reviews 248, 68–86.Google Scholar
Grimberg-Henrici, CG, Vermaak, P, Bolhuis, JE, Nordquist, RE and van der Staay, FJ 2016. Effects of environmental enrichment on cognitive performance of pigs in a spatial holeboard discrimination task. Animal Cognition 19, 271–283.Google Scholar
Hedegaard, CJ, Chen, N, Sellebjerg, F, Sørensen, PS, Leslie, RGQ, Bendtzen, K and Nielsen, CH 2009. Autoantibodies to myelin basic protein (MBP) in healthy individuals and in patients with multiple sclerosis: a role in regulating cytokine responses to MBP. Immunology 128, e451–e461.Google Scholar
Kim, SJ, Gershov, D, Ma, X, Brot, N and Elkon, KB 2002. I-PLA2 activation during apoptosis promotes the exposure of membrane lysophosphatidylcholine leading to binding by natural immunoglobulin M antibodies and complement activation. The Journal of Experimental Medicine 196, 655–665.CrossRefGoogle Scholar
Koh, KB 1998. Emotion and immunity. Journal of Psychosomatic Research 45, 107–115.Google Scholar
Lutz, HU, Binder, CJ and Kaveri, S 2009. Naturally occurring auto-antibodies in homeostasis and disease. Trends in Immunology 30, 43–51.Google Scholar
Maier, SF and Watkins, LR 1998. Cytokines for psychologists: implications of bidirectional immune-to-brain communication for understanding behavior, mood, and cognition. Psychological Review 105, 83.Google Scholar
Mayasari, N, de Vries Reilingh, G, Nieuwland, M, Remmelink, G, Parmentier, H, Kemp, B and van Knegsel, A 2015. Effect of maternal dry period length on colostrum immunoglobulin content and on natural and specific antibody titers in calves. Journal of Dairy Science 98, 3969–3979.Google ScholarPubMed
Nagele, EP, Han, M, Acharya, NK, DeMarshall, C, Kosciuk, MC and Nagele, RG 2013. Natural IgG autoantibodies are abundant and ubiquitous in human sera, and their number is influenced by age, gender, and disease. PLoS ONE 8, e60726.Google Scholar
Oster, M, Muráni, E, Ponsuksili, S, Richard, B, Turner, SP, Evans, G, Thölking, L, Kurt, E, Klont, R and Foury, A 2014. Transcriptional responses of PBMC in psychosocially stressed animals indicate an alerting of the immune system in female but not in castrated male pigs. BMC Genomics 15, 967.CrossRefGoogle Scholar
Panda, S and Ding, JL 2015. Natural antibodies bridge innate and adaptive immunity. The Journal of Immunology 194, 13–20.Google Scholar
Postal, M and Appenzeller, S 2015. The importance of cytokines and autoantibodies in depression. Autoimmunity Reviews 14, 30–35.Google Scholar
Reimert, I, Rodenburg, TB, Ursinus, WW, Kemp, B and Bolhuis, JE 2014a. Selection based on indirect genetic effects for growth, environmental enrichment and coping style affect the immune status of pigs. PLoS ONE 9, e108700.Google Scholar
Reimert, I, Rodenburg, TB, Ursinus, WW, Kemp, B and Bolhuis, JE 2014b. Responses to novel situations of female and castrated male pigs with divergent social breeding values and different backtest classifications in barren and straw-enriched housing. Applied Animal Behaviour Science 151, 24–35.CrossRefGoogle Scholar
Rossi, S, Doucelin, A, Le Potier, M-F, Eraud, C and Gilot-Fromont, E 2013. Innate immunity correlates with host fitness in wild boar (Sus scrofa) exposed to classical swine fever. PLoS ONE 8, e79706.CrossRefGoogle ScholarPubMed
Scholz, J, Allemang-Grand, R, Dazai, J and Lerch, JP 2015. Environmental enrichment is associated with rapid volumetric brain changes in adult mice. NeuroImage 109, 190–198.CrossRefGoogle ScholarPubMed
Schrama, J, Schouten, J, Swinkels, J, Gentry, J, de Vries Reilingh, G and Parmentier, H 1997. Effect of hemoglobin status on humoral immune response of weanling pigs differing in coping styles. Journal of Animal Science 75, 2588–2596.CrossRefGoogle ScholarPubMed
Sun, Y, Parmentier, H, Frankena, K and Van der Poel, J 2011. Natural antibody isotypes as predictors of survival in laying hens. Poultry Science 90, 2263–2274.CrossRefGoogle ScholarPubMed
Tuyttens, FAM 2005. The importance of straw for pig and cattle welfare: a review. Applied Animal Behaviour Science 92, 261–282.CrossRefGoogle Scholar
van Dixhoorn, ID, Reimert, I, Middelkoop, J, Bolhuis, JE, Wisselink, HJ, Koerkamp, PWG, Kemp, B and Stockhofe-Zurwieden, N 2016. Enriched housing reduces disease susceptibility to co-infection with porcine reproductive and respiratory virus (PRRSV) and Actinobacillus pleuropneumoniae (A. pleuropneumoniae) in young pigs. PLoS ONE 11, e0161832.Google Scholar
Wijga, S, Bovenhuis, H, Bastiaansen, J, Arendonk, J, Ploegaert, T, Tijhaar, E and Poel, J 2013. Genetic parameters for natural antibody isotype titers in milk of Dutch Holstein‐Friesians. Animal Genetics 44, 485–492.Google Scholar
Zhou, Y, Cheshire, A, Howell, LA, Ryan, DH and Harris, RB 1999. Neuroautoantibody immunoreactivity in relation to aging and stress in apolipoprotein E-deficient mice. Brain Research Bulletin 49, 173–179.Google Scholar