Skip to main content
SpringerLink
Log in

Effects of heat stress on the gene expression of nutrient transporters in the jejunum of broiler chickens (Gallus gallus domesticus)

  • Original Paper
  • Published:
International Journal of Biometeorology Aims and scope Submit manuscript

An Erratum to this article was published on 09 May 2015

Abstract

In broiler chickens, heat stress disrupts nutrient digestion and absorption. However, the underlying molecular mechanism is not clearly understood. Hence, to investigate the effects of high ambient temperatures on the expression levels of nutrient transporters in the jejunum of broiler chickens, seventy-two 35-day-old male broiler chickens with similar body weights were randomly allocated into two groups: control (24 ± 1 °C) and heat-stressed (32 ± 1 °C). The chickens in the heat-stressed group were exposed to 10 h of heat daily from 08:00 to 18:00 and then raised at 24 ± 1 °C. The rectal temperature and feed intake of the chickens were recorded daily. After 7 days, nine chickens per group were sacrificed by exsanguination, and the jejunum was collected. The results show that heat exposure significantly decreased the feed intake and increased the rectal temperature of the broiler chickens. The plasma concentrations of uric acid and triglyceride significantly increased and decreased, respectively, in the heat-stressed group. No significant differences in the levels of plasma glucose, total amino acids, and very low-density lipoprotein were observed between the heat-stressed and control groups. However, the plasma concentration of glucose tended to be higher (P = 0.09) in the heat-stressed group than in the control group. Heat exposure did not significantly affect the mRNA levels of Na+-dependent glucose transporter 1 and amino acid transporters y + LAT1, CAT1, r-BAT, and PePT-1. However, the expression levels of GLUT-2, FABP1, and CD36 were significantly decreased by heat exposure. The results of this study provide new insights into the mechanisms by which heat stress affects nutrient absorption in broiler chickens. Our findings suggest that periodic heat exposure might alter the jejunal glucose and lipid transport rather than amino acid transport. However, intestinal epithelial damage and cell loss should be considered when interpreting the effects of heat stress on the expression of intestinal transporters.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adibi SA, Gray SJ, Menden E (1967) The kinetics of amino acid absorption and alteration of plasma composition of free amino acids after intestinal perfusion of amino acid mixtures. Am J Clin Nutr 20:24–33

    CAS  Google Scholar 

  • Banaszak L, Winter N, Xu Z, Bernlohr DA, Cowan S, Jones TA (1994) Lipid-binding protein: a family of fatty acid and retinoid transport protein. Adv Protein Chem 45:89–151

    Article  CAS  Google Scholar 

  • Bröer S (2008) Amino acid transport across mammalian intestinal and renal epithelia. Physiol Rev 88:249–286

    Article  Google Scholar 

  • Chrousos GP, Kino T (2005) Intracellular glucocorticoid signaling: a formerly simple system turns stochastic. Sci STKE 304:pe48

    Google Scholar 

  • Daniel H (2004) Molecular and integrative physiology of intestinal peptide transport. Annu Rev Physiol 66:361–384

    Article  CAS  Google Scholar 

  • Ferrer C, Pedragosa E, Torras-Llort M, Parcerisa X, Rafecas M, Ferrer R, Amat C, Moretó M (2003) Dietary lipids modify brush border membrane composition and nutrient transport in chicken small intestine. J Nutr 133:1147–1153

    CAS  Google Scholar 

  • Furuhashi M, Hotamisligil GS (2008) Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets. Nat Rev Drug Discov 7:489–503

    Article  CAS  Google Scholar 

  • Garriga C, Hunter RR, Amat C, Planas JM, Mitchell MA, Moreto M (2006) Heat stress increases apical glucose transport in the chicken jejunum. Am J Physiol Regul Integr Comp Physiol 290:R195–201

    Article  CAS  Google Scholar 

  • Gilbert ER, Li H, Emmerson DA, Webb KE, Wong EA (2007) Developmental regulation of nutrient transporter and enzyme mRNA abundance in the small intestine of broilers. Poult Sci 86:1739–1753

    Article  CAS  Google Scholar 

  • Griffin HD, Whitehead CC (1982) Plasma lipoprotein concentration as an indicator of fatness in broilers: development and use of a simple assay for plasma very low density lipoproteins. Br Poult Sci 23:307–313

    Article  CAS  Google Scholar 

  • Hsu SC, DeFranco DB (1995) Selectivity of cell cycle regulation of glucocorticoid receptor function. J Biol Chem 270:3359–3364

    Article  CAS  Google Scholar 

  • Hu XF, Guo YM, Huang BY, Bun S, Zhang LB, Li JH, Liu D, Long FY, Yang X, Jiao P (2010a) The effect of glucagon-like peptide 2 injection on performance, small intestinal morphology, and nutrient transporter expression of stressed broiler chickens. Poult Sci 89:1967–1974

    Article  CAS  Google Scholar 

  • Hu XF, Guo YM, Huang BY, Zhang LB, Bun S, Liu D, Long FY, Li JH, Yang X, Jiao P (2010b) Effect of corticosterone administration on small intestinal weight and expression of small intestinal nutrient transporter mRNA of broiler chickens. Asian-australasian J Anim Sci 23:175–181

    Article  CAS  Google Scholar 

  • Hurwitz S, Weiselberg M, Eisner M, Bartov I, Riesenfeld G, Sharvit M, Niv A, Bornstein S (1980) The energy requirements and performance of growing chickens and turkeys as affected by environmental temperature. Poult Sci 59:2209–2299

    Google Scholar 

  • Jane D, Steven V, Timothy P, King SP, Shirazi Z (2003) Glucose sensing in the intestinal epithelium. Eur J Biochem 270:3377–3388

    Article  Google Scholar 

  • Kellett GL (2001) The facilitated component of intestinal glucose absorption. J Physiol 531:585–595

    Article  CAS  Google Scholar 

  • Kellett GL, Helliwell PA (2000) The diffusive component of intestinal glucose absorption is mediated by the glucose-induced recruitment of GLUT2 to the brush-border membrane. Biochem J 1:155–162

    Article  Google Scholar 

  • Kellett GL, Brot-Laroche E, Mace OJ, Leturque A (2008) Sugar absorption in the intestine: the role of GLUT2. Annu Rev Nutr 28:35–54

    Article  CAS  Google Scholar 

  • Koelkebeck KW, Parsons CM, Wang X (1998) Effect of acute heat stress on amino acid digestibility in laying hens. Poult Sci 77:1393–1396

    Article  CAS  Google Scholar 

  • Lei L, Xianlei L, Hepeng L, Hongchao J, Hai L, Sheikhahmadi A, Zhigang S (2013) Acute heat stress alters gene expression of brain-gut appetite regulatory neuropeptides in broiler chickens (Gallus gallus domesticus). J Anim Sci 91:5194–5201

    Article  CAS  Google Scholar 

  • Lin H, Buyse J, Du R, Gu XH, Zhang ZY (2004a) Response of rectal temperature of broiler chickens to thermal environment factors. Archiv fur Geflugelkunde 68:126–131

    Google Scholar 

  • Lin H, Decuypere E, Buyse J (2004b) Oxidative stress induced by corticosterone administration in broiler chickens (Gallus gallus domesticus) 1 chronic exposure. Comp Biochem Physiol B 139:737–744

    Article  CAS  Google Scholar 

  • Lin H, Zhang HF, Jiao HC, Zhao T, Sui SJ, Gu XH, Zhang ZY, Buyse J, Decuypere E (2005) Thermoregulation responses of broiler chickens to humidity at different ambient temperatures I One week of age. Poult Sci 84:1166–1172

    Article  CAS  Google Scholar 

  • Liu F, Yin J, Du M, Yan P, Xu J, Zhu X, Yu J (2009) Heat-stress-induced damage to porcine small intestinal epithelium associated with downregulation of epithelial growth factor signaling. J Anim Sci 87:1941–1949

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)) method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • McDowell RE, Hooven NW, Camoens JK (1976) Effects of climate on performance of Holsteins in first lactation. J Dairy Sci 59:965–971

    Article  Google Scholar 

  • Moraes VMB, Malheiros RD, Bruggeman V, Collin A, Tona K, Van PAS, Onagbesan OM, Buyse J, Decuypere E, Macari M (2003) Effect of thermal conditioning during embryonic development on aspects of physiological responses of broilers to heat stress. J Therm Biol 28:133–140

    Article  Google Scholar 

  • Nathana DB, Hellera ED, Pereka M (1976) The effect of short heat stress upon leucocyte count, plasma corticosterone level, plasma and leucocyte ascorbic acid content. Br Poult Sci 17:481–486

    Article  Google Scholar 

  • Nicol C (2011) Management and welfare of farm animals: The UFAW farm handbook: UFAW farm handbook. Editor, John Webster, 5th ed. John Wiley -Blackwell, West Sussex, UK, pp 25

  • Palacin M, Kanai Y (2004) The ancillary proteins of HATs: SLC3 family of amino acid transporters. Pflugers Arch 447:490–494

    Article  CAS  Google Scholar 

  • Prows DR, Murphy EJ, Schroeder F (1995) Intestinal and liver fatty acid-binding proteins differentially affect fatty acid uptake and esterification in L-cell. Lipids 30:907–910

    Article  CAS  Google Scholar 

  • Quinteiro-Filho WM, Ribeiro A, Ferra de Paula V, Pinheiro ML, Sakai M, Sá LRM, Perreira AJP, Palermo-Neto J (2010) Heat stress impairs performance parameters, induces intestinal injury, and decreases macrophage activity in broiler chickens. Poult Sci 89:1905–1914

    Article  CAS  Google Scholar 

  • Rezaei M, Hajati H (2010) Effect of diet dilution at early age on performance, carcass characteristics and blood parameters of broiler chicks. Italian J Anim Sci 9:e19. doi:10.4081/ijas.2010.e19

    Article  Google Scholar 

  • Rodriguez SM, Guimaraes KC, Matthews JC, McLeod KR, Baldwin RL, Harmon DL (2004) Influence of abomasal carbohydrates on small intestinal sodium-dependent glucose cotransporter activity and abundance in steers. J Anim Sci 82:3015–3023

    CAS  Google Scholar 

  • Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment, 5th edn. Cambridge University Press, UK, p 383

    Google Scholar 

  • Shepherd EJ, Helliwell PA, Mace OJ, Morgan EL, Patel N, Kellett GL (2004) Stress and glucocorticoid inhibit apical GLUT-2-trafficking and intestinal glucose absorption in rat small intestine. J Physiol 560:281–290

    Article  CAS  Google Scholar 

  • Shim KS, Hwang KT, Son MW, Park GH (2006) Lipid metabolisms and peroxidation in broiler chicks under chronic heat stress. Asian-australasian J Anim Sci 19:1206–1211

    Article  CAS  Google Scholar 

  • Sinha RK (2007) Study of changes in some pathophysiological stress markers in different age groups of an animal model of acute and chronic heat stress. Iran Biom J 11:101–111

    Google Scholar 

  • Sklan D, Geyra A, Tako E, Gal-Gerber O, Uni Z (2003) Ontogeny of brush border carbohydrate digestion and uptake in the chick. Br J Nutr 89:747–753

    Article  CAS  Google Scholar 

  • Song Z, Liu L, Sheikhahmadi A, Jiao H, Lin H (2012) Effect of heat exposure on gene expression of feed intake regulatory peptides in laying hens. J Biomed Biotechnol. doi:10.1155/2012/484869

    Google Scholar 

  • Song J, Jiao LF, Xiao K, Luan ZS, Hu CH, Shi B, Zhan XA (2013) Cello-oligosaccharide ameliorates heat stress-induced impairment of intestinal microflora, morphology and barrier integrity in broilers. Anim Feed Sci Tech 185:175–181

    Article  CAS  Google Scholar 

  • Sylvia S, Mader W (1998) Biology, 6th edn. McGraw-Hill, New York, p 185

    Google Scholar 

  • Takahashi K, Jensen LS, Bolden SL (1983) Diet composition, environmental temperature, and exogenous estradiol effects on hepatic lipid deposition in growing chicks. Poult Sci 63:524–531

    Article  Google Scholar 

  • Temim S, Chagneau AM, Peresson R, Tesseraud S (2000) Chronic heat exposure alters protein turnover of three different skeletal muscles in finishing broiler chickens fed 20 or 25% protein diets. J Nutr 130:813–819

    CAS  Google Scholar 

  • Thorens B (1996) Glucose transporters in the regulation of intestinal, renal, and liver glucose fluxes. Am J Physiol 270:G541–553

    CAS  Google Scholar 

  • Verrey F, Meier C, Rossier G, Kühn LC (2000) Glycoprotein-associated amino acid exchangers: broadening the range of transport specificity. Pflugers Arch 440:503–512

    Article  CAS  Google Scholar 

  • Wallis IR, Balnave D (1984) The influence of environmental temperature, age and sex on the digestibility of amino acids in growing broiler chickens. Br Poult Sci 25:401–407

    Article  CAS  Google Scholar 

  • Wolfenson D, Bachrach D, Maman M, Graber Y, Rozenboim I (2001) Evaporative cooling of ventral regions of the skin in heat-stressed laying hens. Poult Sci 80:958–964

    Article  CAS  Google Scholar 

  • Wright EM, Turk E (2004) The sodium/glucose cotransport family SLC5. Pflugers Arch 447:510–518

    Article  CAS  Google Scholar 

  • Yaman MA, Kita K, Okumura J (2000) Different responses of protein synthesis to refeeding in various muscles of fasted chicks. Br Poult Sci 41:224–228

    Article  CAS  Google Scholar 

  • Zhan XA, Wang M, Ren H, Zhao RQ, Li JX, Tan ZL (2007) Effect of early feed restriction on metabolic programming and compensatory growth in broiler chickens. Poult Sci 86:654–660

    Article  CAS  Google Scholar 

  • Zhao JP, Jiang YB, Jiao HC, Song ZG, Wang XJ, Lin H (2012) Cool perch availability improves the performance and welfare status of broiler chickens in hot weather. Poult Sci 91:1775–1784

    Article  CAS  Google Scholar 

Download references

Acknowledgment

This work was funded by Shandong Modern Agricultural Technology and Industry System (SDAIT-13-011-08).

Author information

Authors and Affiliations

  1. Department of Animal Science and Technology, Shandong Agricultural University, Taian, Shandong, 271018, China

    Xiaolei Sun, Haichao Zhang, Hongchao Jiao, Hai Lin & Zhigang Song

  2. Department of Animal Science, Faculty of Agriculture, University of Kurdistan, Sanandaj, 66177-15175, Iran

    Ardashir Sheikhahmadi

  3. Laboratory of Livestock Physiology, Department of Biosystems, KU Leuven, Kasteelpark Arenberg 30, 3001, Leuven, Belgium

    Yufeng Wang

Authors
  1. Xiaolei Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Haichao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ardashir Sheikhahmadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yufeng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hongchao Jiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hai Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhigang Song
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhigang Song.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, X., Zhang, H., Sheikhahmadi, A. et al. Effects of heat stress on the gene expression of nutrient transporters in the jejunum of broiler chickens (Gallus gallus domesticus). Int J Biometeorol 59, 127–135 (2015). https://doi.org/10.1007/s00484-014-0829-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00484-014-0829-1

Keywords

Search

Navigation