Duodenal Metabolic Profile Changes in Heat-Stressed Broilers
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Ethics Statements
2.2. Birds, Diets, and Heat Stress Challenge
2.3. Sample Collection and Preparation
2.4. Ultra-High Performance Liquid Chromatography—High Resolution Mass Spectrometry (UHPLC–HRMS) Metabolomics Analysis
2.5. Ingenuity Pathway Analysis (IPA)
2.6. RNA Isolation and Quantitative Real-Time PCR
2.7. Immunoblot Analysis
2.8. Data Processing and Statistical Analysis
3. Results
3.1. Global Analysis of the Duodenal Dynamic Metabolic Profiling
3.2. Identification of Potential Metabolic Signatures
3.3. Metabolic Pathway and Network Analysis
3.3.1. Top Canonical Pathways
3.3.2. Top Diseases and Disorders
3.3.3. Top Molecular and Cellular Functions
3.3.4. Top Up- and Downstream Regulators
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Gene | Accession Number a | Primer Sequence (5′→3′) | Orientation | Product Size (bp) |
---|---|---|---|---|
CA9 HDAC11 CPT1 MAPK3 MAPK1 MAPK14 MAPK9 SOD1 SOD2 18S | XM_004937157 NM_001277141 AY675193 NM_204150 AY033635 XM_419263 NM_205095 NM_205064 NM_204211 AF173612 | GGGATGTGCTTGCTGTGCTAT AGGAAAGCCAGCATTGTGATG ACCAGTCCTCTTTCTTCCCAACT GGGTTCGCAGAGGTTTCAAA GCCCTGATGCCTTCATTCAA ATTTTCCCATGTCTCGGTAGTGA CGGACCATGATCACACAGGAT CAGGAGCCCTGTACCAACGT CGGACCATGATCACACAGGAT CAGGAGCCCTGTACCAACGT AGCTGGAGATTGAGGAATGGAA CGGTGGCACAAAGCTGATTA GCCGATGATCAGCCAGGAT GGCCCAATGGAAGCAAGAG TGGCTTCCATGTGCATGAAT AGCACCTGCGCTGGTACAC GCTGGAGCCCCACATCAGT GGTGGCGTGGTGTTTGCT TCCCCTCCCGTTACTTGGAT GCGCTCGTCGGCATGTA | Forward Reverse Forward Reverse Forward Reverse Forward Reverse Forward Reverse Forward Reverse Forward Reverse Forward Reverse Forward Reverse Forward Reverse | 58 63 60 63 63 62 62 58 61 60 |
HMDB ID | PHS | PF | AHS | CHS | |
---|---|---|---|---|---|
Cystathionine | HMDB0000099 | + | - | ||
N-Acetylornithine | HMDB0003357 | + | - | ||
Dihydroorotate | HMDB0003349 | + | - | ||
Allantoate | HMDB0001209 | + | |||
Trehalose | HMDB0000975 | + | |||
Glucosamine | HMDB0001514 | + | + | ||
sn-Glycerol 3-phosphate | HMDB0000126 | + | + | ||
NAD+ | HMDB0000902 | + | + | ||
Cysteate | HMDB0002757 | - | - | + | |
Inosine | HMDB0000195 | - | |||
Acetylphosphate | HMDB0001494 | + | + | ||
Histidine | HMDB0000177 | + | - | - | |
Homocysteic acid | HMDB0002205 | + | |||
3-Phosphoserine | HMDB0000272 | + | |||
N-Acetyl-beta-alanine | HMDB0061880 | + | |||
Cystine | HMDB0000192 | + | - | ||
Methionine sulfoxide | HMDB0002005 | + | |||
Arginine | HMDB0000517 | + | |||
D-glucarate | HMDB0000663 | + | |||
Xylose | HMDB0000098 | + | |||
Glucose phosphate | HMDB0001254 | + | - | ||
Myo-inositol | HMDB0000211 | + | |||
N-Acetylglucosamine 1/6-phosphate | HMDB0002817 | + | |||
3-Phosphoglycerate | HMDB0000807 | + | |||
2-Oxo-4-methylthiobutanoate | HMDB0001553 | + | |||
FAD | HMDB0001248 | + | + | ||
Hypoxanthine | HMDB0000157 | + | |||
Orotate | HMDB0000226 | + | - | ||
Octulose bisphosphate | N/A | + | |||
Allantoin | HMDB0000462 | + | |||
D-gluconate | HMDB0000625 | + | - | ||
Ribose phosphate | HMDB0001548 | + | |||
Sedoheptulose 1/7-phosphate | HMDB0060509 | + | |||
Aconitate | HMDB0000072 | + | - | ||
Pyridoxine | HMDB0000239 | + | |||
AICAR | HMDB0001517 | - | - | ||
Prephenate | HMDB0012283 | + | + | ||
pimelic acid | HMDB0000857 | + | + | ||
2-Isopropylmalate | HMDB0000402 | + | + | ||
3-Hydroxyisovalerate | HMDB0000754 | + | |||
ADP-glucose | HMDB0006557 | + | + | ||
Homocarnosine | HMDB0000745 | - | - | ||
N-Carbamoyl-L-aspartate | HMDB0000828 | - | |||
Homocysteine | HMDB0000742 | - | |||
dAMP | HMDB0000905 | - | |||
dTMP | HMDB0001227 | - | |||
Glycinamide ribotide (GAR) | HMDB0002022 | - | - | ||
S-Adenosyl-L-homocysteine | HMDB0000939 | - | |||
Homocitrulline | HMDB0000679 | - | |||
Citrate/isocitrate | HMDB0000193 | - | |||
Hydroxyphenylacetate | HMDB0000020 | + | |||
Salicylate | HMDB0000500 | + | |||
NADH | HMDB0001487 | + | |||
UDP | HMDB0000295 | + | |||
NADP+ | HMDB0000217 | + | |||
CDP | HMDB0001546 | + | |||
D-Erythrose 4-phosphate | HMDB0001321 | + | |||
Riboflavin | HMDB0000244 | + | |||
N-Acetylputrescine | HMDB0002064 | - | |||
1-Methylhistidine | HMDB0000001 | - | |||
Phosphothreonine | HMDB0011185 | - | |||
Pantothenate | HMDB0000210 | - |
Canonical Pathways | Molecules | Treatments 1 | |||||||
---|---|---|---|---|---|---|---|---|---|
PHS | AHS | CHS | PF | ||||||
p-Value | Ratio | p-Value | Ratio | p-Value | Ratio | p-Value | Ratio | ||
Purine Nucleotides Degradation | Hypoxanthine *, inosine, NAD+, NADH, uric acid, xanthosine, xanthosine monophosphate, adenosine †, GMP † | - | - | 7.7 × 10−8 | 0.412 | 5.0 × 10−7 | 0.412 | - | - |
Urate Biosynthesis/Inosine 5′-phosphate degradation | NAD+, NADH, uric acid, xanthosine, xanthosine monophosphate | - | - | 1.0 × 10−6 | 0.556 | 4.0 × 10−6 | 0.556 | - | - |
Adenosine Nucleotides Degradation | Hypoxanthine, inosine, NAD+, NADH, uric acid | - | - | 3.8 × 10−6 | 0.455 | - | - | - | - |
Dopamine Degradation | 3′,5′-ADP, 3,4-dihydroxyphenylacetic, NAD+, NADH | - | - | 1.5 × 10−5 | 0.357 | - | - | - | - |
Ascorbate Recycling | Ascorbic acid, NAD+, NADH, NADP, glutathione † | - | - | 2.5 × 10−5 | 0.5 | 1.8 × 10−6 | 0.625 | - | - |
UDP-D-xylose and UDP-D-glucuronate Biosynthesis | NAD+, NADH, UDP-D-glucose, UDP-glucuronic acid | - | - | - | - | 5.5 × 10−6 | 0.8 | - | - |
Salvage Pathways of Pyrimidine Deoxyribonucleotides | Deoxyuridine, dTMP, dUMP, thymidine, thymine, deoxycytidine ‡, uracil ‡ | - | - | - | - | 2.3 × 10−5 | 0.417 | 1.6 × 10−6 | 0.583 |
Glycine Betaine Degradation | Dimethylglycine, glycine, L-homocysteine, L-methionine, L-serine, Pyruvic acid, sarcosine | 6.1 × 10−7 | 0.538 | - | - | - | - | 3.3 × 10−6 | 0.538 |
tRNA Charging | Glycine, L-arginine, l-asparagine, L-aspartic acid, L-histidine, L-methionine, L-phenylalanine, L-proline, l-serine, L-tryptophan, L-tyrosine | 2.5 × 10−6 | 0.256 | - | - | - | - | - | - |
Creatine Biosynthesis | Creatine, glycine, glycocyamine, L-arginine, L-ornithine, S-adenosylhomocysteine ‡ | 4.3 × 10−6 | 0.714 | - | - | - | - | 3.0 × 10−7 | 0.857 |
Pyruvate Fermentation to Lactate | L-lactic acid, NAD+, NADH, Pyruvic acid | 4.8 × 10−6 | 1 | - | - | - | - | - | - |
Diseases and Functions | Treatments 1 | |||||||
---|---|---|---|---|---|---|---|---|
PHS | AHS | CHS | PF | |||||
p-Value | # Mol. | p-Value | # Mol. | p-Value | # Mol. | p-Value | # Mol. | |
Cancer | 4.7 × 10−2–8.8 × 10−9 | 36 | - | - | 3.3 × 10−2–2.2 × 10−5 | 22 | 4.9 × 10−2–4.7 × 10−10 | 45 |
Organismal Injury and abnormalities | 4.7 × 10−2–8.8 × 10−9 | 51 | 4.9 × 10−2–6.5 × 10−4 | 23 | 3.3 × 10−2–2.2 × 10−5 | 29 | 4.9 × 10−2–4.7 × 10−10 | 70 |
Hepatic system disease | 4.7 × 10−2–1.7 × 10−5 | 22 | - | - | - | - | - | - |
Hematological disease | 4.7 × 10−2–1.3 × 10−4 | 13 | - | 3.3 × 10−2–2.9 × 10−4 | 8 | - | - | |
Ophthalmic disease | - | - | 2.5 × 10−2–6.5 × 10−4 | 3 | - | - | - | - |
Cardiovascular disease | - | - | 4.8 × 10−2–1.9 × 10−3 | 3 | - | - | - | - |
Developmental disorders | - | - | 4.2 × 10−2–1.9 × 10−3 | 4 | - | - | - | - |
Hereditary disorders | - | - | 4.2 × 10−2–1.9 × 10−3 | 6 | - | - | - | - |
Neurological disease | - | - | - | - | 3.3 × 10−2–1.2 × 10−4 | 21 | - | - |
Psychological disorders | - | - | - | - | 3.3 × 10−2–8.3 × 10−4 | 15 | - | - |
Inflammatory disease | - | - | - | - | - | - | 4.9 × 10−2–1.4 × 10−6 | 21 |
Inflammatory response | - | - | - | - | - | - | 4.7 × 10−2–1.4 × 10−6 | 32 |
Treatments 1 | ||||||||
---|---|---|---|---|---|---|---|---|
PHS | AHS | CHS | PF | |||||
Molecular and Cellular Functions | p-Value | # Mol. | p-Value | # Mol. | p-Value | # Mol. | p-Value | # Mol. |
Amino acid metabolism | 4.7 × 10−2–1.1 × 10−8 | 27 | - | - | - | - | 4.9 × 10−2–8.9 × 10−9 | 31 |
Molecular transport | 4.7 × 10−2–1.1 × 10−8 | 37 | - | - | - | - | 4.9 × 10−2–2.5 × 10−8 | 48 |
Small molecule biochemistry | 4.7 × 10−2–1.1 × 10−8 | 44 | 4.6 × 10−2–8.4 × 10−5 | 28 | - | - | 4.9 × 10−2–2.5 × 10−8 | 58 |
Protein synthesis | 2.6 × 10−2–1.7 × 10−7 | 18 | - | - | 3.3 × 10−2–2.0 × 10−4 | 11 | 1.4 × 10−2–3.6 × 10−7 | 22 |
Cell death and survival | 4.7 × 10−2–7.5 × 10−7 | 36 | - | 3.3 × 10−2–1.2 × 10−4 | 26 | - | - | |
Nucleic acid metabolism | - | - | 4.5 × 10−2–1.8 × 10−5 | 21 | - | - | - | - |
DNA replication, damage, and repair | - | - | 4.2 × 10−2–3.0 × 10−4 | 11 | - | - | - | - |
Energy production | - | - | 4.2 × 10−2–3.0 × 10−4 | 12 | - | - | - | - |
Carbohydrate metabolism | - | - | 4.3 × 10−2–6.5 × 10−4 | 10 | - | - | - | - |
Free radical scavenging | - | - | - | - | 3.3 × 10−2–1.4 × 10−4 | 12 | - | - |
Upstream Regulators 2 | Treatments 1 | |||||||
---|---|---|---|---|---|---|---|---|
PHS | AHS | CHS | PF | |||||
p-Value | Z Score | p-Value | Z Score | p-Value | Z Score | p-Value | Z Score | |
GNMT | 4.1 × 10−4 | −2.23 | - | - | - | - | 8.0 × 10−7 | −2.82 |
CPT1B | 1.9 × 10−9 | −2.49 | 1.3 × 10−4 | −2.44 | 1.1 × 10−5 | −2.82 | 1.9 × 10−17 | −3.71 |
GATA4 | 2.8 × 10−6 | 2.82 | - | - | - | - | 1.8 × 10−4 | 2.64 |
MMP11 | 2.2 × 10−5 | 2.00 | - | - | - | - | - | - |
IL37 | - | - | - | 9.9 × 10−4 | −2.23 | 2.9 × 10−10 | −2.49 | |
CA9 | 1.5 × 10−11 | 3.31 | - | - | 1.6 × 10−3 | 2.00 | 6.9 × 10−9 | 3.16 |
HDAC11 | 2.1 × 10−4 | 2.00 | - | - | - | - | 5.9 × 10−4 | 2.0 |
CTH | 7.9 × 10−5 | −2.0 | - | - | - | - |
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Dridi, J.S.; Greene, E.S.; Maynard, C.W.; Brugaletta, G.; Ramser, A.; Christopher, C.J.; Campagna, S.R.; Castro, H.F.; Dridi, S. Duodenal Metabolic Profile Changes in Heat-Stressed Broilers. Animals 2022, 12, 1337. https://doi.org/10.3390/ani12111337
Dridi JS, Greene ES, Maynard CW, Brugaletta G, Ramser A, Christopher CJ, Campagna SR, Castro HF, Dridi S. Duodenal Metabolic Profile Changes in Heat-Stressed Broilers. Animals. 2022; 12(11):1337. https://doi.org/10.3390/ani12111337
Chicago/Turabian StyleDridi, Jalila S., Elizabeth S. Greene, Craig W. Maynard, Giorgio Brugaletta, Alison Ramser, Courtney J. Christopher, Shawn R. Campagna, Hector F. Castro, and Sami Dridi. 2022. "Duodenal Metabolic Profile Changes in Heat-Stressed Broilers" Animals 12, no. 11: 1337. https://doi.org/10.3390/ani12111337
APA StyleDridi, J. S., Greene, E. S., Maynard, C. W., Brugaletta, G., Ramser, A., Christopher, C. J., Campagna, S. R., Castro, H. F., & Dridi, S. (2022). Duodenal Metabolic Profile Changes in Heat-Stressed Broilers. Animals, 12(11), 1337. https://doi.org/10.3390/ani12111337