Effect of heat stress on the hypothalamic expression profile of water homeostasis‐associated genes in low‐ and high‐water efficient chicken lines

Abstract With climate change, selection for water efficiency and heat resilience are vitally important. We undertook this study to determine the effect of chronic cyclic heat stress (HS) on the hypothalamic expression profile of water homeostasis‐associated markers in high (HWE)‐ and low (LWE)‐water efficient chicken lines. HS significantly elevated core body temperatures of both lines. However, the amplitude was higher by 0.5–1°C in HWE compared to their LWE counterparts. HWE line drank significantly less water than LWE during both thermoneutral (TN) and HS conditions, and HS increased water intake in both lines with pronounced magnitude in LWE birds. HWE had better feed conversion ratio (FCR), water conversion ratio (WCR), and water to feed intake ratio. At the molecular level, the overall hypothalamic expression of aquaporins (AQP8 and AQP12), arginine vasopressin (AVP) and its related receptor AVP2R, angiotensinogen (AGT), angiotensin II receptor type 1 (AT1), and calbindin 2 (CALB2) were significantly lower; however, CALB1 mRNA and AQP2 protein levels were higher in HWE compared to LWE line. Compared to TN conditions, HS exposure significantly increased mRNA abundances of AQPs (8, 12), AVPR1a, natriuretic peptide A (NPPA), angiotensin I‐converting enzyme (ACE), CALB1 and 2, and transient receptor potential cation channel subfamily V member 1 and 4 (TRPV1 and TRPV4) as well as the protein levels of AQP2, however it decreased that of AQP4 gene expression. A significant line by environment interaction was observed in several hypothalamic genes. Heat stress significantly upregulated AQP2 and SCT at mRNA levels and AQP1 and AQP3 at both mRNA and protein levels, but it downregulated that of AQP4 protein only in LWE birds. In HWE broilers, however, HS upregulated the hypothalamic expression of renin (REN) and AVPR1b genes and AQP5 proteins, but it downregulated that of AQP3 protein. The hypothalamic expression of AQP (5, 7, 10, and 11) genes was increased by HS in both chicken lines. In summary, this is the first report showing improvement of growth performances in HWE birds. The hypothalamic expression of several genes was affected in a line‐ and/or environment‐dependent manner, revealing potential molecular signatures for water efficiency and/or heat tolerance in chickens.

[1]  S. Dridi,et al.  Impact of Phytase Supplementation on Meat Quality of Heat-Stressed Broilers , 2023, Animals : an open access journal from MDPI.

[2]  Zuzanna A. Jagiello,et al.  The effect of climate change on avian offspring production: A global meta-analysis , 2023, Proceedings of the National Academy of Sciences of the United States of America.

[3]  R. Wideman,et al.  Comparative- and network-based proteomic analysis of bacterial chondronecrosis with osteomyelitis lesions in broiler’s proximal tibiae identifies new molecular signatures of lameness , 2023, Scientific Reports.

[4]  P. Marvar,et al.  Central amygdala angiotensin type 1 receptor (Agtr1) expressing neurons contribute to fear extinction , 2023, Neuropharmacology.

[5]  F. Baldi,et al.  Effects of Feeding and Drinking Behavior on Performance and Carcass Traits in Beef Cattle , 2022, Animals : an open access journal from MDPI.

[6]  A. R. Sesay Impact of Heat Stress on Chicken Performance, Welfare, and Probable Mitigation Strategies , 2022, International Journal of Environment and Climate Change.

[7]  K. N. Reddy,et al.  Impact of recent climate change on corn, rice, and wheat in southeastern USA , 2022, Scientific Reports.

[8]  B. Balasubramanian,et al.  Heat Stress Affects Jejunal Immunity of Yellow-Feathered Broilers and Is Potentially Mediated by the Microbiome , 2022, Frontiers in Physiology.

[9]  S. Dridi Nutritional Biochemistry: From the Classroom to the Research Bench , 2022 .

[10]  S. Dridi,et al.  Effects of heat stress on cyto(chemo)kine and inflammasome gene expression and mechanical properties in isolated red and white blood cells from 4 commercial broiler lines and their ancestor jungle fowl , 2022, Poultry science.

[11]  J. Tollefson Climate change is hitting the planet faster than scientists originally thought. , 2022, Nature.

[12]  S. Dridi,et al.  Effect of Cyclic Heat Stress on Feeding-Related Hypothalamic Neuropeptides of Three Broiler Populations and Their Ancestor Jungle Fowl , 2021, Frontiers in Physiology.

[13]  J. Meullenet,et al.  Effects of Herbal Adaptogen Feed-Additive on Growth Performance, Carcass Parameters, and Muscle Amino Acid Profile in Heat-Stressed Modern Broilers , 2021, Frontiers in Physiology.

[14]  Atul K. Jain,et al.  Climate impacts on global agriculture emerge earlier in new generation of climate and crop models , 2021, Nature Food.

[15]  N. Anthony,et al.  Effects of Cyclic Chronic Heat Stress on the Expression of Nutrient Transporters in the Jejunum of Modern Broilers and Their Ancestor Wild Jungle Fowl , 2021, Frontiers in Physiology.

[16]  J. Hansen,et al.  Aquaglyceroporins and orthodox aquaporins in human adipocytes. , 2021, Biochimica et biophysica acta. Biomembranes.

[17]  C. Baes,et al.  Meta-analysis to predict the effects of temperature stress on meat quality of poultry , 2021, Poultry science.

[18]  B. Bryan,et al.  Future global urban water scarcity and potential solutions , 2021, Nature Communications.

[19]  L. Kőrösi,et al.  Effects of heat stress on the immune responses of chickens subjected to thermal manipulation in the pre-hatch period. , 2021, Acta veterinaria Hungarica.

[20]  N. Anthony,et al.  Applied Research Note: Development of a novel low flow water monitoring system in poultry/agriculture systems , 2021, Journal of Applied Poultry Research.

[21]  D. Campos,et al.  Methionine supplementing effects on intestine, liver and uterus morphology, and on positivity and expression of Calbindin-D28k and TRPV6 epithelial calcium carriers in laying quail in thermoneutral conditions and under thermal stress , 2021, PloS one.

[22]  M. Cassandro,et al.  Emerging Genetic Tools to Investigate Molecular Pathways Related to Heat Stress in Chickens: A Review , 2020, Animals : an open access journal from MDPI.

[23]  Yuanchang Jin,et al.  Heat stress impacts on broiler performance: a systematic review and meta-analysis , 2020, Poultry science.

[24]  B. Mishra,et al.  Impact of Heat Stress on Poultry Health and Performances, and Potential Mitigation Strategies , 2020, Animals : an open access journal from MDPI.

[25]  N. Anthony,et al.  Intestinal Barrier Integrity in Heat-Stressed Modern Broilers and Their Ancestor Wild Jungle Fowl , 2020, Frontiers in Veterinary Science.

[26]  Sun-Ok Lee,et al.  Protective effects of the phytogenic feed additive "comfort" on growth performance via modulation of hypothalamic feeding- and drinking-related neuropeptides in cyclic heat-stressed broilers. , 2020, Domestic animal endocrinology.

[27]  N. Anthony,et al.  Processing evaluation of random bred broiler populations and a common ancestor at 55 days under chronic heat stress conditions , 2020, Poultry science.

[28]  C. Krehbiel,et al.  Characterization of Water Intake and Water Efficiency in beef cattle. , 2019, Journal of animal science.

[29]  N. Dingemanse,et al.  Adaptive responses of animals to climate change are most likely insufficient , 2019, Nature Communications.

[30]  Komlavi Akpoti,et al.  Agricultural land suitability analysis: State-of-the-art and outlooks for integration of climate change analysis , 2019, Agricultural Systems.

[31]  D. Ahn,et al.  How can heat stress affect chicken meat quality? ‐ a review , 2019, Poultry science.

[32]  D. Victor,et al.  Global warming will happen faster than we think , 2018, Nature.

[33]  S. Tramberend,et al.  Global assessment of water challenges under uncertainty in water scarcity projections , 2018, Nature Sustainability.

[34]  Lin Zhang,et al.  Effects of chronic heat exposure on growth performance, intestinal epithelial histology, appetite-related hormones and genes expression in broilers. , 2018, Journal of the science of food and agriculture.

[35]  Carl J. Schmidt,et al.  Immunomodulatory effects of heat stress and lipopolysaccharide on the bursal transcriptome in two distinct chicken lines , 2018, BMC Genomics.

[36]  W. Kuenzel,et al.  AMP-Activated Protein Kinase Mediates the Effect of Leptin on Avian Autophagy in a Tissue-Specific Manner , 2018, Front. Physiol..

[37]  T. Hertel,et al.  New science of climate change impacts on agriculture implies higher social cost of carbon , 2017, Nature Communications.

[38]  K. Tsutsui,et al.  Neuropeptide Control of Feeding Behavior in Birds and Its Difference with Mammals , 2016, Front. Neurosci..

[39]  A. Bruce Critical role of animal science research in food security and sustainability , 2016, Food Security.

[40]  M. Hajihosseini,et al.  Hypothalamic tanycytes—masters and servants of metabolic, neuroendocrine, and neurogenic functions , 2015, Front. Neurosci..

[41]  N. Metcalfe,et al.  Variation in the link between oxygen consumption and ATP production, and its relevance for animal performance , 2015, Proceedings of the Royal Society B: Biological Sciences.

[42]  R. Jahanian,et al.  Dietary chromium methionine supplementation could alleviate immunosuppressive effects of heat stress in broiler chicks. , 2015, Journal of animal science.

[43]  N. Metcalfe,et al.  Flexibility in metabolic rate confers a growth advantage under changing food availability , 2015, The Journal of animal ecology.

[44]  S. Shields,et al.  The Impacts of Climate Change Mitigation Strategies on Animal Welfare , 2015, Animals : an open access journal from MDPI.

[45]  F. Langlet,et al.  Tanycytes: A Gateway to the Metabolic Hypothalamus , 2014, Journal of neuroendocrinology.

[46]  J. Pollock,et al.  Water and electrolyte homeostasis brings balance to physiology. , 2014, American journal of physiology. Regulatory, integrative and comparative physiology.

[47]  M. Prager-Khoutorsky,et al.  Unique Interweaved Microtubule Scaffold Mediates Osmosensory Transduction via Physical Interaction with TRPV1 , 2014, Neuron.

[48]  M. Cassell,et al.  Activation of the renin-angiotensin system, specifically in the subfornical organ is sufficient to induce fluid intake. , 2014, American journal of physiology. Regulatory, integrative and comparative physiology.

[49]  K. Ishibashi,et al.  The role of mammalian superaquaporins inside the cell. , 2014, Biochimica et biophysica acta.

[50]  P. Siegel Evolution of the modern broiler and feed efficiency. , 2014, Annual review of animal biosciences.

[51]  Felipe J. Colón-González,et al.  Multimodel assessment of water scarcity under climate change , 2013, Proceedings of the National Academy of Sciences.

[52]  T. Giambelluca,et al.  The projected timing of climate departure from recent variability , 2013, Nature.

[53]  F. Detcheverry,et al.  Optimizing water permeability through the hourglass shape of aquaporins , 2013, Proceedings of the National Academy of Sciences.

[54]  W. Kuenzel,et al.  Neuroendocrine regulation of stress in birds with an emphasis on vasotocin receptors (VTRs). , 2013, General and comparative endocrinology.

[55]  E. Rush,et al.  Water: neglected, unappreciated and under researched , 2013, European Journal of Clinical Nutrition.

[56]  L. J. Lara,et al.  Impact of Heat Stress on Poultry Production , 2013, Animals : an open access journal from MDPI.

[57]  K. Wiedemann,et al.  Effects of natriuretic peptides upon hypothalamo-pituitary-adrenocortical system activity and anxiety behaviour. , 2012, Experimental and clinical endocrinology & diabetes : official journal, German Society of Endocrinology [and] German Diabetes Association.

[58]  T. Ebeid,et al.  High ambient temperature influences eggshell quality and calbindin-D28k localization of eggshell gland and all intestinal segments of laying hens. , 2012, Poultry science.

[59]  W. Hauswirth,et al.  ERK1/2 activation is a therapeutic target in age-related macular degeneration , 2012, Proceedings of the National Academy of Sciences.

[60]  Xinglian Xu,et al.  Effects of dietary glutamine and gamma-aminobutyric acid on meat colour, pH, composition, and water-holding characteristic in broilers under cyclic heat stress , 2012, British poultry science.

[61]  I-Ching Chen,et al.  Rapid Range Shifts of Species Associated with High Levels of Climate Warming , 2011, Science.

[62]  C. Revenga,et al.  Urban growth, climate change, and freshwater availability , 2011, Proceedings of the National Academy of Sciences.

[63]  B. Nilius,et al.  The transient receptor potential family of ion channels , 2011, Genome Biology.

[64]  V. Lee,et al.  Secretin and body fluid homeostasis. , 2011, Kidney international.

[65]  M. Papp,et al.  Alterations in hippocampal calcium-binding neurons induced by stress models of depression: a preliminary assessment , 2010, Pharmacological reports : PR.

[66]  W. Yung,et al.  Secretin as a neurohypophysial factor regulating body water homeostasis , 2009, Proceedings of the National Academy of Sciences.

[67]  S. Dai,et al.  Dietary glutamine supplementation improves growth performance, meat quality and colour stability of broilers under heat stress , 2009, British poultry science.

[68]  A. Patapoutian,et al.  TRPV1 Is Activated by Both Acidic and Basic pH , 2009, The Journal of Neuroscience.

[69]  A. Johnson,et al.  Enhanced water and salt intake in transgenic mice with brain-restricted overexpression of angiotensin (AT1) receptors. , 2008, American journal of physiology. Regulatory, integrative and comparative physiology.

[70]  Thomas D. Schmittgen,et al.  Analyzing real-time PCR data by the comparative CT method , 2008, Nature Protocols.

[71]  C. Bourque,et al.  Contribution of TRPV channels to osmosensory transduction, thirst, and vasopressin release. , 2008, Kidney international.

[72]  M. Papadopoulos,et al.  Water movements in the brain: role of aquaporins , 2008, Trends in Neurosciences.

[73]  J. Jordan,et al.  Water drinking induces thermogenesis through osmosensitive mechanisms. , 2007, The Journal of clinical endocrinology and metabolism.

[74]  M. Cassell,et al.  Local production of angiotensin II in the subfornical organ causes elevated drinking. , 2007, The Journal of clinical investigation.

[75]  M. Flörke,et al.  Future long-term changes in global water resources driven by socio-economic and climatic changes , 2007 .

[76]  E. Mosley‐Thompson,et al.  Abrupt tropical climate change: past and present. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[77]  M. Wechselberger,et al.  Physiology and Pharmacology of Temperature Regulation Ionic channels and conductance-based models for hypothalamic neuronal thermosensitivity , 2006 .

[78]  J. Buyse,et al.  Acute heat stress induces oxidative stress in broiler chickens. , 2006, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[79]  R. Alley,et al.  Ice-Sheet and Sea-Level Changes , 2005, Science.

[80]  G. Manley,et al.  Reduced cerebrospinal fluid production and intracranial pressure in mice lacking choroid plexus water channel Aquaporin‐1 , 2005, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[81]  J. Badaut,et al.  Distribution and possible roles of aquaporin 9 in the brain , 2004, Neuroscience.

[82]  Larry J Young,et al.  Profound Impairment in Social Recognition and Reduction in Anxiety-Like Behavior in Vasopressin V1a Receptor Knockout Mice , 2004, Neuropsychopharmacology.

[83]  A. Johnson,et al.  The physiological regulation of thirst and fluid intake. , 2004, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[84]  F. Edens,et al.  Influence of selenium sources on age-related and mild heat stress-related changes of blood and liver glutathione redox cycle in broiler chickens (Gallus domesticus). , 2003, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[85]  R. Ross Anandamide and vanilloid TRPV1 receptors , 2003, British journal of pharmacology.

[86]  J. Friedman,et al.  Abnormal osmotic regulation in trpv4-/- mice , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[87]  Thomas Walther,et al.  Angiotensin-(1–7) is an endogenous ligand for the G protein-coupled receptor Mas , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[88]  Gary D. Schnitkey,et al.  ECONOMIC LOSSES FROM HEAT STRESS BY US LIVESTOCK INDUSTRIES , 2003 .

[89]  Gary K. Beauchamp,et al.  Food Intake, Water Intake, and Drinking Spout Side Preference of 28 Mouse Strains , 2002, Behavior genetics.

[90]  M. Cassell,et al.  Glia- and Neuron-specific Expression of the Renin-Angiotensin System in Brain Alters Blood Pressure, Water Intake, and Salt Preference* , 2002, The Journal of Biological Chemistry.

[91]  N. Deeb,et al.  Genotype-by-environment interaction with broiler genotypes differing in growth rate. 3. Growth rate and water consumption of broiler progeny from weight-selected versus nonselected parents under normal and high ambient temperatures. , 2002, Poultry science.

[92]  K. Holthoff,et al.  A Novel Role of Vasopressin in the Brain: Modulation of Activity-Dependent Water Flux in the Neocortex , 2001, The Journal of Neuroscience.

[93]  K. Robison,et al.  A Novel Angiotensin-Converting Enzyme–Related Carboxypeptidase (ACE2) Converts Angiotensin I to Angiotensin 1-9 , 2000, Circulation research.

[94]  C. Vörösmarty,et al.  Global water resources: vulnerability from climate change and population growth. , 2000, Science.

[95]  Arai,et al.  Calbindin D28k and calretinin in oxytocin and vasopressin neurons of the rat supraoptic nucleus.A triple-labeling immunofluorescence study , 1999, Cell and tissue research.

[96]  W. Rascher,et al.  Effects of systemic treatment with irbesartan and losartan on central responses to angiotensin II in conscious, normotensive rats. , 1999, European journal of pharmacology.

[97]  P. Agre,et al.  Direct immunogold labeling of aquaporin-4 in square arrays of astrocyte and ependymocyte plasma membranes in rat brain and spinal cord. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[98]  H. Soininen,et al.  Distribution of parvalbumin‐, calretinin‐, and calbindin‐D28k–immunoreactive neurons and fibers in the human entorhinal cortex , 1997, The Journal of comparative neurology.

[99]  D. Julius,et al.  The capsaicin receptor: a heat-activated ion channel in the pain pathway , 1997, Nature.

[100]  P. Agre,et al.  Specialized Membrane Domains for Water Transport in Glial Cells: High-Resolution Immunogold Cytochemistry of Aquaporin-4 in Rat Brain , 1997, The Journal of Neuroscience.

[101]  S. Bhattacharya,et al.  Anxiolytic Activity of Intraventricularly Administered Atrial Natriuretic Peptide in the Rat , 1996, Neuropsychopharmacology.

[102]  D. Bichet Vasopressin receptors in health and disease. , 1996, Kidney international.

[103]  S. Fluharty,et al.  Intracerebroventricular administration of angiotensin type 1 (AT1) receptor antisense oligonucleotides attenuate thirst in the rat , 1995, Regulatory Peptides.

[104]  J. Thaxton,et al.  Daily Feed and Water Consumption of Broiler Chicks From 0 to 21 Days of Age , 1992 .

[105]  P. Baylis,et al.  OSMOREGULATION OF VASOPRESSIN SECRETION AND THIRST IN HEALTH AND DISEASE , 1988, Clinical endocrinology.

[106]  W. Samson,et al.  Atrial natriuretic factor inhibits dehydration- and angiotensin II-induced water intake in the conscious, unrestrained rat. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[107]  G. Pesti,et al.  Water consumption of broiler chickens under commercial conditions. , 1985, Poultry science.

[108]  C. Desplan,et al.  Synthesis, molecular cloning, and restriction analysis of DNA complementary to vitamin D-dependent calcium-binding protein mRNA from rat duodenum. , 1983, The Journal of biological chemistry.

[109]  J. Fuller,et al.  Genetic influence on water and sweetened water consumption in mice , 1976, Physiology & Behavior.

[110]  D. Baker,et al.  Body composition and nutrient utilization of chicks fed amino acid diets containing graded amounts of either isoleucine or lysine. , 1972, The Journal of nutrition.

[111]  V. Prévot,et al.  The special relationship: glia–neuron interactions in the neuroendocrine hypothalamus , 2018, Nature Reviews Endocrinology.

[112]  E. Maier‐Reimer,et al.  The projected timing of climate departure from recent variability , 2016 .

[113]  Sarah S. Simmonds,et al.  Central Control of Fluid and Electrolyte Homeostasis Osmoregulatory thirst in mice lacking the transient receptor potential vanilloid type 1 (TRPV1) and/or type 4 (TRPV4) receptor , 2014 .

[114]  C. Bourque,et al.  Molecular Transient Receptor Potential Vanilloid 1 Is Required for Intrinsic Osmoreception in Organum Vasculosum Lamina Terminalis Neurons and for Normal Thirst Responses to Systemic Hyperosmolality , 2006 .

[115]  R. Mulder Safe poultry meat production in the next century. , 1997, Acta veterinaria Hungarica.

[116]  M. Murphy,et al.  Water metabolism of dairy cattle. , 1992, Journal of dairy science.

[117]  B. W. Bierer,et al.  A comparison of the survival time and gross pathology in producing and nonproducing White Leghorn hens deprived of water. , 1966, Poultry science.