Effects of combined Actinobacillus pleuropneumoniae challenge and change in environmental temperature on calcitonin receptor expression levels in growing pigs
C. A. Kerr A E , K. O. Mathews A C , L. R. Giles B and M. R. Jones A DA CSIRO Livestock Industries, Queensland Bioscience Precinct, Level 6, 306 Carmody Rd, St Lucia, Qld 4067, Australia.
B NSW Agriculture, Elizabeth Macarthur Agricultural Institute, PMB 8, Camden, NSW 2570, Australia.
C Present address: Faculty of Veterinary Science, The University of Sydney, Camden, NSW 2570, Australia.
D Present address: School of Science, Food and Horticulture, Hawkesbury Campus, Building K12, University of Western Sydney, Locked Bag 1797, South Penrith Distribution Centre, NSW 1797, Australia.
E Corresponding author; email: Caroline.Kerr@csiro.au
Australian Journal of Agricultural Research 55(7) 727-732 https://doi.org/10.1071/AR03249
Submitted: 27 November 2003 Accepted: 28 April 2004 Published: 2 August 2004
Abstract
We have identified through differential gene expression polymerase chain reaction that porcine calcitonin receptor expression levels could be altered in porcine leukocytes in response to Actinobacillus pleuropneumoniae (App) challenge. This study further investigates the effects of mild pleuropneumonia and changes in environmental temperature, singularly and in combination, on leukocyte expression levels of the calcitonin receptor in domestic pigs. Forty entire male pigs were allocated by weight and temperament at a starting liveweight of 33 0± 5 kg to 4 treatments: control (22°C room temperature); A. pleuropneumoniae challenge (Day 1); varied temperature (15°C for 8 h on Days 0, 1, and 2; 30°C for 24 h on Day 6); and the combined A. pleuropneumoniae challenge and varied temperature treatment. The analysis of the leukocyte expression levels of calcitonin receptor using semi-quantitative reverse transcription PCR revealed that calcitonin receptor was up-regulated in response to the A. pleuropneumoniae challenge (P < 0.001) and the temperature treatment (P < 0.001). In addition, up-regulation of the calcitonin receptor correlated with decreased weight gain, feed intake, and plasma IGF-I. Thus, expression levels of the calcitonin receptor reflect changes in growth performance associated with alteration in ambient temperature and App challenge. In addition, this study indicates that calcitonin receptor expression represents a mechanism through which endocrine and immune systems interact to affect growth.
Acknowledgments
This research was partially supported by Australian Pork Limited. We thank Mr Graeme Furley for his skilled technical assistance during the pig experiment, Dr Pat Blackall for supplying the App serovar, and Dr Anthony Reverter for his statistical assistance. Also, we thank our collaborators: Pharmacia Upjohn, QAF Meat Industries, Dr A. Knowles, Dr P. Wynn, and Dr D. Strom.
Aida S,
Shimoji K, Abo T
(1995) Calcitonin affects the expression of adhesion molecules on T-cell receptor (TCR) cells. International Journal of Immunotherapy 11, 107–113.
Amara SG,
Jonas V,
Rosenfeld MG,
Ong ES, Evans RM
(1982) Alternative RNA processing in calcitonin gene expression generates mRNAs encoding different polypeptide products. Nature 298, 240–244.
| Crossref |
PubMed |
Baarsch MJ,
Scamurra RW,
Burger K,
Foss DL,
Maheswaran SK, Murtaugh MP
(1995) Inflammatory cytokine expression in swine experimentally infected with Actinobacillus pleuropneumoniae.
Infection and Immunology 63, 3587–3594.
Benson DA,
Boguski MS,
Lipman DJ, Ostell J
(1997) GenBank. Nucleic Acids Research 25, 1–6.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Besedovsky HO, del Rey A
(2000) The cytokine-HPA axis feed-back circuit. Zeitschrift Für Rheumatologie 59, 26–30.
| Crossref |
Black JL, Davies GT, Bradley LR
(1994) Future needs in swine research. ‘Livestock production for the 21st Century: priorities and research needs’. (Eds PJ Moughan, MWA Verstegen, MI Visser-Reyneveld)
pp. 87–102. (Wageningen Press: Wageningen, The Netherlands)
Black JL, Giles LR, Wynn PC, Knowles AG, Kerr CA, Jones MR, Strom AD, Gallagher NL, Eamens GJ
(2001) A review—factors limiting the performance of growing pigs in commercial environments. ‘Manipulating pig production VIII’. (Ed. PD Cranwell)
pp. 9–36. (Australasian Pig Science Association: Werribee, Vic.)
de Braganca MM,
Mounier AM, Prunier A
(1998) Does feed restriction mimic the effects of increased ambient temperature in lactating sows? Journal of Animal Science 76, 2017–2024.
| PubMed |
Bray GA
(2000) Afferent signals regulating food intake. Proceedings of the Nutrition Society 59, 373–384.
| PubMed |
Buess M,
Moroni C, Hirsch HH
(1997) Direct identification of differentially expressed genes by cycle sequencing and cycle labelling using the differential display PCR primers. Nucleic Acids Research 25, 2233–2235.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Collin A,
van Milgen J,
Dubois S, Noblet J
(2001) Effect of high temperature on feeding behaviour and heat production in group-housed young pigs. The British Journal of Nutrition 8, 63–70.
Gelfand EW,
Cheung RK,
Mills GB, Grinstein S
(1988) The uptake of extracellular Ca2+, and not recruitment from internal stores is essential for T lymphocyte proliferation. European Journal of Immunology 118, 917–922.
Gonyou HW, Stricklin WR
(1998) Effects of floor area allowance and group size on the productivity of growing/finishing pigs. Journal of Animal Science 76, 1326–1330.
| PubMed |
Gouy H,
Cefai D,
Christensen SB,
Debre P, Bismuth G
(1990) Ca2+ influx in human T lymphocytes is induced independently of inositol phosphate production by mobilization of intracellular Ca2+ endoplasmic reticulum-ATPase inhibitor thapsigargin. European Journal of Immunology 20, 2269–2275.
| PubMed |
Herpin P,
Berthon D,
Bertin R,
Demarco F,
Dauncey MJ, Ledividich J
(1995) Cold-induced changes in circulating levels of catecholamines and thyroid-hormones are modulated by energy-intake in newborn pigs. Experimental Physiology 80, 877–880.
| PubMed |
Hyun J,
Ellis M,
Riskowski G, Johnson RW
(1998) Growth performance on pigs subjected to multiple concurrent environmental stressors. Journal of Animal Science 76, 721–727.
| PubMed |
Johnson RW
(1997) Inhibition of growth by pro-inflammatory cytokines: an integrated view. Journal of Animal Science 75, 1244–1255.
| PubMed |
Kawamura N,
Tamura H,
Obana S,
Wenner M,
Ishikawa T,
Nakata A, Yamamoto H
(1998) Differential effects of neuropeptides on cytokine production by mouse helper T cell subsets. Neuroimmunomodulation 5, 9–15.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kerr CA, Eamens GJ, Altman EL, Sheehy PA, Giles LR, Collins DP, Jones MR
(1999) Effect of mild pleuropneumonia on individual feed intake, growth and cortisol in growing pigs. ‘Manipulating pig production VII’. (Ed. PD Cranwell)
p. 253. (Australasian Pig Science Association: Werribee, Vic.)
Kerr CA,
Eamens GJ,
Briegal J,
Sheehy PA,
Giles LR, Jones MR
(2003) Effects of combined Actinobacillus pleuropneumoniae challenge and change in environmental temperature on production, plasma insulin-like growth factor I (IGF-I) and cortisol parameters in growing pigs. Australian Journal of Agricultural Research 54, 1057–1064.
| Crossref | GoogleScholarGoogle Scholar |
Keys JR
(2001) Porcine lymphocytes and stress: adrenergic receptor signal transduction. PhD thesis, The University of Sydney, NSW, Australia.
(
:
)
Knowles AG, Kingsford NM, Seccombe AM, Keys JR, Kerr CA, Jones MR, Husband AJ
(1997) Immunological output and cytokine profile in pigs exposed to high temperatures. ‘Manipulating pig production VI’. (Ed. PD Cranwell)
p. 229. (Australasian Pig Science Association: Werribee, Vic.)
Levite M
(2000) Nerve-driven immunity—the direct effects of neurotransmitters on T-cell function. Neuroimmunomodulation Annals of the New York Academy of Sciences 917, 307–321.
Lopez J,
Jesse GW,
Becker BA, Ellersieck MR
(1991) Effects of temperature on the performance of finishing swine: I. Effects of a hot, diurnal temperature on average daily gain, feed intake and feed efficiency. Journal of Animal Science 69, 1843–1849.
| PubMed |
Nambiar MP,
Enyedy EJ,
Fisher CU,
Warke VG, Tsokos GC
(2001) High dose of dexamethasone upregulates TCR/CD30 induced calcium response independent of the TCRξ chain expression in human T lymphocytes. Journal of Cellular Biochemistry 83, 401–413.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rafai P, Fodor E
(1980) Studies on porcine adrenocortical function. Acta Veterinaria Academiae Scientiarum Hungaricae, Tomus 28, 443–454.
Scherubl H,
Hescheler J,
Schultz G,
Kliemann D,
Zink A,
Ziegler R, Raue F
(1992) Inhibition of Ca2+-induced calcitonin secretion by somatostatin—roles of voltage dependent Ca2+ channels and G-proteins. Cellular Signalling 4, 77–85.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tang YM,
Feng Y, Wang X
(1998) Calcitonin gene-related peptide potentiates LPS-induced IL-6 release from mouse peritoneal macrophages. Journal of Neuroimmunology 84, 207–212.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wallgren P,
Segall T,
Morner AP, Gunnarsson A
(1999) Experimental infections with Actinobacillus pleuropneumoniae in pigs – I. Comparison of five different parenteral antibiotic treatments. Journal of Veterinary Medicine Series B, Infectious Diseases and Veterinary Public Health 46, 249–260.
Wang X,
Fiscus RR,
Tang Z,
Yang LH,
Wu J,
Fan S, Mathews HL
(1994) CGRP in the serum of endoxin-treated rats suppresses lymphoproliferation. Brain, Behavior, and Immunity 8, 282–292.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Whittemore EC,
Kyriazakis I,
Emmans GC, Tolkamp GJ
(2001) Tests of two theories of food intake of foods of differing bulk content. Animal Science 72, 351–360.
