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[1]Traber PG, Gumucio DL and Wang W: Isolation of intestinal epithelial cells for the study of differential gene expression along the crypt-villus axis. Am J Physiol Gastrointest Liver Physiol 260(6), G895-G903 (1991)
[2]Yang H, Xiong X and Yin Y: Development and renewal of intestinal villi in pigs. In: Nutritional and physiological functions of amino acids in pigs. Ed F. Blachier, G. Wu&Y. Yin. Springer, New York (2013)
[3]Gordon JI and Hermiston ML: Differentiation and self-renewal in the mouse gastrointestinal epithelium. Curr Opin Cell Biol 6, 795-803 (1994)
[4]Fan MZ, Stoll B, Jiang R and Burrin DG: Enterocyte digestive enzyme activity along the crypt-villus and longitudinal axes in the neonatal pig small intestine. J Anim Sci 79, 371-381 (2001)
[5]Fan MZ, Matthews JC, Etienne NMP, Stoll B, Lackeyram D and Burrin DG: Expression of apical membrane L-glutamate transporters in neonatal porcine epithelial cells along the small intestinal crypt-villus axis. Am J Physiol Gastrointest Liver Physiol 287(2), G385-G398 (2004)
[6]Yang C: Expression of porcine intestinal nutrient transporters along crypt-villus axis and during postnatal development. In: University of Guelph, (2011)
[7]Mariadason JM, Nicholas C, L'Italien KE, Zhuang M, Smartt HJM, Heerdt BG, Yang WC, Corner GA, Wilson AJ, Klampfer L, Arango D and Augenlicht LH: Gene expression profiling of intestinal epithelial cell maturation along the crypt-villus axis. Gastroenterology 128(4), 1081-1088 (2005)
[8]Skrzypek T, Valverde Piedra JL, Skrzypek H, Wolinski J, Kazimierczak W, Szymanczyk S, Pawlowska M and Zabielski R: Light and scanning electron microscopy evaluation of the postnatal small intestinal mucosa development in pigs. J Physiol Pharmacol 56, 71-87 (2005)
[9]Skrzypek T, Piedra JLV, Skrzypek H, Kazimierczak W, Szymanczyk S, Pawlowska M and Zabielski R: Intestinal villi structure during the development of pig and wild boar crossbreed neonates. Livest Sci 109(1-3), 38-41 (2007)
[10]Heo JM, Opapeju FO, Pluske JR, Kim JC, Hampson DJ and Nyachoti CM: Gastrointestinal health and function in weaned pigs: a review of feeding strategies to control post-weaning diarrhoea without using in-feed antimicrobial compounds. J Anim Physiol Anim Nutr (Berl) 97(2), 207-237 (2013)
[11]Spreeuwenberg MAM, Verdonk JMAJ, Gaskins HR and Verstegen MWA: Small intestine epithelial barrier function is compromised in pigs with low feed intake at weaning. J Nutr 131(5), 1520-1527 (2001)
[12]Hansson J, Panchaud A, Favre L, Bosco N, Mansourian R, Benyacoub J, Blum S, Jensen ON and Kussmann M: Time-resolved quantitative proteome analysis of in vivo intestinal development. Mol Cell Proteomics 10(3), M110.005231 (2011)
[13]Xiong X, Yang HS, Tan B, Yang CB, Wu MM, Liu G, Kim SW, Li TJ, Li L, Wang JJ, Wu G and Yin YL: Differential expression of proteins involved in energy production along the crypt-villus axis in early-weaning pig small intestine. Am J Physiol Gastrointest Liver Physiol 309(4), G229-G237 (2015)
[14]National ResearchCouncil: Nutrient requirements of swine (9th ed). National Academic Press, Washington, DC (1998)
[15]Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M and Robles M: Blast2 GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18), 3674-3676 (2005)
[16]KEGG: http: //www.genome.jp/kegg/(2014)
[17]Ye J, Fang L, Zheng HK, Zhang Y, Chen J, Zhang ZJ, Wang J, Li ST, Li RQ, Bolund L and Wang J: WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34, W293-W297 (2006)
[18]de Hoon MJL, Imoto S, Nolan J and Miyano S: Open source clustering software. Bioinformatics 20(9), 1453-1454 (2004)
[19]Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, Ching KA, Antosiewicz-Bourget JE, Liu H, Zhang XM, Green RD, Lobanenkov VV, Stewart R, Thomson JA, Crawford GE, Kellis M and Ren B: Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459(7243), 108-112 (2009)
[20]Moeser AJ, Ryan KA, Nighot PK and Blikslager AT: Gastrointestinal dysfunction induced by early weaning is attenuated by delayed weaning and mast cell blockade in pigs. Am J Physiol Gastrointest Liver Physiol 293(2), G413-G421 (2007)
[21]Moeser AJ, Vander Klok C, Ryan KA, Wooten JG, Little D, Cook VL and Blikslager AT: Stress signaling pathways activated by weaning mediate intestinal dysfunction in the pig. Am J Physiol Gastrointest Liver Physiol 292(1), G173-G181 (2007)
[22]Zhu LH, Xu JX, Zhu SW, Cai X, Yang SF, Chen XL and Guo Q: Gene expression profiling analysis reveals weaning-induced cell cycle arrest and apoptosis in the small intestine of pigs. J Anim Sci 92(3), 996-1006 (2014)
[23]Alpers DH: Protein synthesis in intestinal mucosa: the effect of route of administration of precursor amino acids. J Clin Invest 51(1), 167-173 (1972)
[24]Perez-Vilar J and Hill RL: The structure and assembly of secreted mucins. J Biol Chem 274(45), 31751-31754 (1999)
[25]Deplancke B and Gaskins HR: Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. Am J Clin Nutr 73(6), 1131s-1141s (2001)
[26]Dawson PA, Huxley S, Gardiner B, Tran T, McAuley JL, Grimmond S, McGuckin MA and Markovich D: Reduced mucin sulfonation and impaired intestinal barrier function in the hyposulfataemic NaS1 null mouse. Gut 58(7), 910-919 (2009)
[27]Boudry G, Peron V, Le Huerou-Luron I, Lalles JP and Seve B: Weaning induces both transient and long-lasting modifications of absorptive, secretory, and barrier properties of piglet intestine. J Nutr 134(9), 2256-2262 (2004)
[28]Lalles JP, Boudry G, Favier C, Le Floc'h N, Lurona I, Montagne L, Oswald IP, Pie S, Piel C and Seve B: Gut function and dysfunction in young pigs: physiology. Animal Research 53(4), 301-316 (2004)
[29]Pacha J: Development of intestinal transport function in mammals. Physiol Rev 80(4), 1633-1667 (2000)
[30]Jacob R, Alfalah M, Grunberg J, Obendorf M and Naim HY: Structural determinants required for apical sorting of an intestinal brush-border membrane protein. J Biol Chem 275(9), 6566-6572 (2000)
[31]Martel F, Monteiro R and Lemos C: Uptake of serotonin at the apical and basolateral membranes of human intestinal epithelial (Caco-2) cells occurs through the neuronal serotonin transporter (SERT). J Pharmacol Exp Ther 306(1), 355-362 (2003)
[32]Louvard D, Kedinger M and Hauri HP: The differentiating intestinal epithelial-cell - establishment and maintenance of functions through interactions between cellular structures. Annu Rev Cell Biol 8, 157-195 (1992)
[33]Simons K and Vaz WLC: Model systems, lipid rafts, and cell membranes. Annu Rev Biophys Biomol Struct 33, 269-295 (2004)
[34]van der Flier LG and Clevers H: Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 71, 241-260 (2009)
[35]Yang HS, Li FN, Kong XF, Yuan XX, Lian GQ, Geng MM, Li TJ, Yin JD and Yin YL: Molecular cloning, tissue distribution and ontogenetic expression of Xiang pig Chemerin and its involvement in regulating energy metabolism through Akt and ERK1/2 signaling pathways. Mol Biol Rep 39(2), 1887-1894 (2012)
[36]van der Schoor SRD, Reeds PJ, Stoll B, Henry JF, Rosenberger JR, Burrin DG and van Goudoever JB: The high metabolic cost of a functional gut. Gastroenterology 123(6), 1931-1940 (2002)
[37]Wu G: Intestinal mucosal amino acid catabolism. J Nutr 128, 1249-1252 (1998)
[38]Hou YQ, Wang L, Yi D and Wu G: N-acetylcysteine and intestinal health: a focus on mechanisms of its actions. Front Biosci 20, 872-891 (2015)
[39]Wu G, Meier SA and Knabe DA: Dietary glutamine supplementation prevents jejunal atrophy in weaned pigs. J Nutr 126, 2578-2584 (1996)
[40]Wu G, Wu ZL, Dai ZL, Yang Y, Wang WW, Liu C, Wang B, Wang JJ, Yin YL: Dietary requirements of “nutritionally nonessential amino acids“by animals and humans. Amino Acids 44, 1107-1113 (2013)
[41]Wu G, Bazer FW, Dai ZL, Li DF, Wang JJ and Wu ZL: Amino acid nutrition in animals: protein synthesis and beyond. Annu Rev Anim Biosci 2, 387-417 (2014)
[42]Wu G: Dietary requirements of synthesizable amino acids by animals: A paradigm shift in protein nutrition. J Anim Sci Biotechnol 5, 34 (2014)
[43]Hou YQ, Yin YL and Wu G: Dietary essentiality of “nutritionally nonessential amino acids“for animals and humans. Exp Biol Med 240, 997-1007 (2015)
[44]Jiao N, Wu ZL, Ji Y, Wang B,Dai ZL and Wu G: L-Glutamate enhances barrier and anti-oxidative functions in intestinal porcine epithelial cells. J Nutr 145, 2258-2264 (2015)
[45]Duan JL, Yin J, Ren WK, Liu T, Cui ZJ, Huang XG, Wu L, Kim SW, Liu G, Wu X, Wu G, Li TJ and Yin YL: Dietary supplementation with L-glutamate and L-aspartate alleviates oxidative stress in weaned piglets challenged with hydrogen peroxide. Amino Acids 48, 53-64 (2016)
[46]Yi D, Hou YQ, Wang L, Ouyang WJ, Long MH, Zhao D, Ding BY, Liu YL and Wu G: L-Glutamine enhances enterocyte growth via activation of the mTOR signaling pathway independently of AMPK. Amino Acids 47, 65-78 (2015)
[47]Wang B, Wu G,Zhou ZG, Dai ZL, Sun YL, Zhang C, Jiao N, Ji Y, Li W, Wang WW and Wu ZL: Glutamine and intestinal barrier function. Amino Acids 47, 2143-2154 (2015)
[48]Wang L, Hou YQ, Yi D, Li YT, Ding BY, Zhu HL, Liu J, Xiao H and Wu G: Dietary supplementation with glutamate precursor alpha-ketoglutarate attenuates lipopolysaccharide-induced liver injury in young pigs. Amino Acids 47, 1309-1318 (2015)
[49]Flynn NE, Meininger CJ, Kelly K, Ing NH, Morris SM Jr and Wu G: Glucocorticoids mediate the enhanced expression of intestinal type II arginase and argininosuccinate synthase in postweaning pigs. J Nutr 129, 799-803 (1999)
[50]Wu G, Meininger CJ, Kelly K, Watford M and Morris SM Jr: A cortisol surge mediates the enhanced expression of pig intestinal pyrroline-5-carboxylate synthase during weaning. J Nutr 130, 1914-1919 (2000)
[51]Wang WW, Dai ZL, Wu ZL, Lin G, Jia SC, Hu SD, Dahanayaka S and Wu G: Glycine is a nutritionally essential amino acid for maximal growth of milk-fed young pigs. Amino Acids 46: 2037-2045 (2014)
[52]Sun YL, Wu ZL, Li W, Zhang C, Sun KJ, Ji Y, Wang B, Jiao N, He BB, Wang WW, Dai ZL and Wu G: Dietary L-leucine supplementation enhances intestinal development in suckling piglets. Amino Acids 47, 1517-1525 (2015)
[53]Wang L, Hou YQ, Yi D, Ding BY, Zhao D, Wang ZX, Zhu HL, Liu YL, Gong J, Assaad H and Wu G: Dietary oleum cinnamomialleviates intestinal injury. Front Biosci 20: 814-828 (2015)
[54]Yi D, Hou YQ, Wang L, Zhao D, Ding BY, Wu T, Chen HB, Liu YL, Kang P and Wu G: Gene expression profiles in the intestine of lipopolysaccharide-challenged piglets. Front Biosci 21: 487-501 (2016)
[55]Wang JJ, Chen LX, Li P, Li XL, Zhou HJ, Wang FL, Li DF, Yin YL and Wu G: Gene expression is altered in piglet small intestine by weaning and dietary glutamine supplementation. J Nutr 138, 1025-1032 (2008)
[56]Meyuhas O: Synthesis of the translational apparatus is regulated at the translational level. Eur J Biochem 267(21), 6321-6330 (2000)
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Frontiers in Bioscience-Landmark (FBL) is published by IMR Press from Volume 26 Issue 5 (2021). Previous articles were published by another publisher on a subscription basis, and they are hosted by IMR Press on imrpress.com as a courtesy and upon agreement with Frontiers in Bioscience.
Expression of proteins in intestinal middle villus epithelial cells of weaning piglets
1 Chinese Academy of Science, Institute of Subtropical Agriculture, Research Center for Healthy Breeding Livestock and Poultry, Hunan Engineering and Research Center for Animal and Poultry Science, Key Laboratory of Agroecology in Subtropical Region, Scientific Observing and Experimental Station of Animal Nutrition and Feed Science in South-Central China, Ministry of Agriculture, Changsha 410125, Hunan, China
2 University of Chinese Academy of Sciences, Beijing 100039, China
3 School of Life Sciences, Hunan Normal University, Changsha, China
4 Fujian Aonong Biotechnology Corporation, Xiamen, Fujian, China
5 Hunan Collaborative Innovation Center for Utilization of Botanical Functional Ingredients, Hunan Collaborative Innovation Center of Animal Production Safety, Changsha 410128, China
6 Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University, Wuhan 430023, China
7 Department of Animal Science, Texas A and M University, College Station, TX 77843, USA
Abstract
Weaning affects intestinal development in mammals, and pigs are often used as an animal model for analyzing the metabolism and physiology of differentiating middle villus intestinal epithelial cells (DIECs). To assess the impact of weaning on the proteomes of DIECs, we weaned piglets on day 14 and collected their jejunum on days 0, 1, 3, 5, and 7 after weaning. Levels of proteins associated with (a) Golgi vesicle transport and protein glycosylation; (b) monosaccharide, lipid, phospholipid, and nucleotide metabolism; and (c) Krebs cycle and respiratory electron transport chain were decreased in DIECs after weaning. These results indicate that weaning decreases nutrient metabolism in DIECs. Moreover, these results suggest that dietary interventions (e.g.,supplementation with functional amino acids) are required to counter these changes.
Keywords
- Weaning
- Middle Villi
- Epithelial Cells
- Piglet
- Jejunum
- Review
References
- [1] Traber PG, Gumucio DL and Wang W: Isolation of intestinal epithelial cells for the study of differential gene expression along the crypt-villus axis. Am J Physiol Gastrointest Liver Physiol 260(6), G895-G903 (1991)
- [2] Yang H, Xiong X and Yin Y: Development and renewal of intestinal villi in pigs. In: Nutritional and physiological functions of amino acids in pigs. Ed F. Blachier, G. Wu&Y. Yin. Springer, New York (2013)Cited within: 0Google Scholar
- [3] Gordon JI and Hermiston ML: Differentiation and self-renewal in the mouse gastrointestinal epithelium. Curr Opin Cell Biol 6, 795-803 (1994)
- [4] Fan MZ, Stoll B, Jiang R and Burrin DG: Enterocyte digestive enzyme activity along the crypt-villus and longitudinal axes in the neonatal pig small intestine. J Anim Sci 79, 371-381 (2001)
- [5] Fan MZ, Matthews JC, Etienne NMP, Stoll B, Lackeyram D and Burrin DG: Expression of apical membrane L-glutamate transporters in neonatal porcine epithelial cells along the small intestinal crypt-villus axis. Am J Physiol Gastrointest Liver Physiol 287(2), G385-G398 (2004)
- [6] Yang C: Expression of porcine intestinal nutrient transporters along crypt-villus axis and during postnatal development. In: University of Guelph, (2011)
- [7] Mariadason JM, Nicholas C, L'Italien KE, Zhuang M, Smartt HJM, Heerdt BG, Yang WC, Corner GA, Wilson AJ, Klampfer L, Arango D and Augenlicht LH: Gene expression profiling of intestinal epithelial cell maturation along the crypt-villus axis. Gastroenterology 128(4), 1081-1088 (2005)
- [8] Skrzypek T, Valverde Piedra JL, Skrzypek H, Wolinski J, Kazimierczak W, Szymanczyk S, Pawlowska M and Zabielski R: Light and scanning electron microscopy evaluation of the postnatal small intestinal mucosa development in pigs. J Physiol Pharmacol 56, 71-87 (2005)
- [9] Skrzypek T, Piedra JLV, Skrzypek H, Kazimierczak W, Szymanczyk S, Pawlowska M and Zabielski R: Intestinal villi structure during the development of pig and wild boar crossbreed neonates. Livest Sci 109(1-3), 38-41 (2007)
- [10] Heo JM, Opapeju FO, Pluske JR, Kim JC, Hampson DJ and Nyachoti CM: Gastrointestinal health and function in weaned pigs: a review of feeding strategies to control post-weaning diarrhoea without using in-feed antimicrobial compounds. J Anim Physiol Anim Nutr (Berl) 97(2), 207-237 (2013)
- [11] Spreeuwenberg MAM, Verdonk JMAJ, Gaskins HR and Verstegen MWA: Small intestine epithelial barrier function is compromised in pigs with low feed intake at weaning. J Nutr 131(5), 1520-1527 (2001)
- [12] Hansson J, Panchaud A, Favre L, Bosco N, Mansourian R, Benyacoub J, Blum S, Jensen ON and Kussmann M: Time-resolved quantitative proteome analysis of in vivo intestinal development. Mol Cell Proteomics 10(3), M110.005231 (2011)
- [13] Xiong X, Yang HS, Tan B, Yang CB, Wu MM, Liu G, Kim SW, Li TJ, Li L, Wang JJ, Wu G and Yin YL: Differential expression of proteins involved in energy production along the crypt-villus axis in early-weaning pig small intestine. Am J Physiol Gastrointest Liver Physiol 309(4), G229-G237 (2015)
- [14] National ResearchCouncil: Nutrient requirements of swine (9th ed). National Academic Press, Washington, DC (1998)
- [15] Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M and Robles M: Blast2 GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18), 3674-3676 (2005)
- [16] KEGG: http: //www.genome.jp/kegg/(2014)
- [17] Ye J, Fang L, Zheng HK, Zhang Y, Chen J, Zhang ZJ, Wang J, Li ST, Li RQ, Bolund L and Wang J: WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34, W293-W297 (2006)
- [18] de Hoon MJL, Imoto S, Nolan J and Miyano S: Open source clustering software. Bioinformatics 20(9), 1453-1454 (2004)
- [19] Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, Ching KA, Antosiewicz-Bourget JE, Liu H, Zhang XM, Green RD, Lobanenkov VV, Stewart R, Thomson JA, Crawford GE, Kellis M and Ren B: Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459(7243), 108-112 (2009)
- [20] Moeser AJ, Ryan KA, Nighot PK and Blikslager AT: Gastrointestinal dysfunction induced by early weaning is attenuated by delayed weaning and mast cell blockade in pigs. Am J Physiol Gastrointest Liver Physiol 293(2), G413-G421 (2007)
- [21] Moeser AJ, Vander Klok C, Ryan KA, Wooten JG, Little D, Cook VL and Blikslager AT: Stress signaling pathways activated by weaning mediate intestinal dysfunction in the pig. Am J Physiol Gastrointest Liver Physiol 292(1), G173-G181 (2007)
- [22] Zhu LH, Xu JX, Zhu SW, Cai X, Yang SF, Chen XL and Guo Q: Gene expression profiling analysis reveals weaning-induced cell cycle arrest and apoptosis in the small intestine of pigs. J Anim Sci 92(3), 996-1006 (2014)
- [23] Alpers DH: Protein synthesis in intestinal mucosa: the effect of route of administration of precursor amino acids. J Clin Invest 51(1), 167-173 (1972)
- [24] Perez-Vilar J and Hill RL: The structure and assembly of secreted mucins. J Biol Chem 274(45), 31751-31754 (1999)
- [25] Deplancke B and Gaskins HR: Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. Am J Clin Nutr 73(6), 1131s-1141s (2001)
- [26] Dawson PA, Huxley S, Gardiner B, Tran T, McAuley JL, Grimmond S, McGuckin MA and Markovich D: Reduced mucin sulfonation and impaired intestinal barrier function in the hyposulfataemic NaS1 null mouse. Gut 58(7), 910-919 (2009)
- [27] Boudry G, Peron V, Le Huerou-Luron I, Lalles JP and Seve B: Weaning induces both transient and long-lasting modifications of absorptive, secretory, and barrier properties of piglet intestine. J Nutr 134(9), 2256-2262 (2004)
- [28] Lalles JP, Boudry G, Favier C, Le Floc'h N, Lurona I, Montagne L, Oswald IP, Pie S, Piel C and Seve B: Gut function and dysfunction in young pigs: physiology. Animal Research 53(4), 301-316 (2004)
- [29] Pacha J: Development of intestinal transport function in mammals. Physiol Rev 80(4), 1633-1667 (2000)
- [30] Jacob R, Alfalah M, Grunberg J, Obendorf M and Naim HY: Structural determinants required for apical sorting of an intestinal brush-border membrane protein. J Biol Chem 275(9), 6566-6572 (2000)
- [31] Martel F, Monteiro R and Lemos C: Uptake of serotonin at the apical and basolateral membranes of human intestinal epithelial (Caco-2) cells occurs through the neuronal serotonin transporter (SERT). J Pharmacol Exp Ther 306(1), 355-362 (2003)
- [32] Louvard D, Kedinger M and Hauri HP: The differentiating intestinal epithelial-cell - establishment and maintenance of functions through interactions between cellular structures. Annu Rev Cell Biol 8, 157-195 (1992)
- [33] Simons K and Vaz WLC: Model systems, lipid rafts, and cell membranes. Annu Rev Biophys Biomol Struct 33, 269-295 (2004)
- [34] van der Flier LG and Clevers H: Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 71, 241-260 (2009)
- [35] Yang HS, Li FN, Kong XF, Yuan XX, Lian GQ, Geng MM, Li TJ, Yin JD and Yin YL: Molecular cloning, tissue distribution and ontogenetic expression of Xiang pig Chemerin and its involvement in regulating energy metabolism through Akt and ERK1/2 signaling pathways. Mol Biol Rep 39(2), 1887-1894 (2012)
- [36] van der Schoor SRD, Reeds PJ, Stoll B, Henry JF, Rosenberger JR, Burrin DG and van Goudoever JB: The high metabolic cost of a functional gut. Gastroenterology 123(6), 1931-1940 (2002)
- [37] Wu G: Intestinal mucosal amino acid catabolism. J Nutr 128, 1249-1252 (1998)
- [38] Hou YQ, Wang L, Yi D and Wu G: N-acetylcysteine and intestinal health: a focus on mechanisms of its actions. Front Biosci 20, 872-891 (2015)
- [39] Wu G, Meier SA and Knabe DA: Dietary glutamine supplementation prevents jejunal atrophy in weaned pigs. J Nutr 126, 2578-2584 (1996)
- [40] Wu G, Wu ZL, Dai ZL, Yang Y, Wang WW, Liu C, Wang B, Wang JJ, Yin YL: Dietary requirements of “nutritionally nonessential amino acids“by animals and humans. Amino Acids 44, 1107-1113 (2013)
- [41] Wu G, Bazer FW, Dai ZL, Li DF, Wang JJ and Wu ZL: Amino acid nutrition in animals: protein synthesis and beyond. Annu Rev Anim Biosci 2, 387-417 (2014)
- [42] Wu G: Dietary requirements of synthesizable amino acids by animals: A paradigm shift in protein nutrition. J Anim Sci Biotechnol 5, 34 (2014)
- [43] Hou YQ, Yin YL and Wu G: Dietary essentiality of “nutritionally nonessential amino acids“for animals and humans. Exp Biol Med 240, 997-1007 (2015)
- [44] Jiao N, Wu ZL, Ji Y, Wang B,Dai ZL and Wu G: L-Glutamate enhances barrier and anti-oxidative functions in intestinal porcine epithelial cells. J Nutr 145, 2258-2264 (2015)
- [45] Duan JL, Yin J, Ren WK, Liu T, Cui ZJ, Huang XG, Wu L, Kim SW, Liu G, Wu X, Wu G, Li TJ and Yin YL: Dietary supplementation with L-glutamate and L-aspartate alleviates oxidative stress in weaned piglets challenged with hydrogen peroxide. Amino Acids 48, 53-64 (2016)
- [46] Yi D, Hou YQ, Wang L, Ouyang WJ, Long MH, Zhao D, Ding BY, Liu YL and Wu G: L-Glutamine enhances enterocyte growth via activation of the mTOR signaling pathway independently of AMPK. Amino Acids 47, 65-78 (2015)
- [47] Wang B, Wu G,Zhou ZG, Dai ZL, Sun YL, Zhang C, Jiao N, Ji Y, Li W, Wang WW and Wu ZL: Glutamine and intestinal barrier function. Amino Acids 47, 2143-2154 (2015)
- [48] Wang L, Hou YQ, Yi D, Li YT, Ding BY, Zhu HL, Liu J, Xiao H and Wu G: Dietary supplementation with glutamate precursor alpha-ketoglutarate attenuates lipopolysaccharide-induced liver injury in young pigs. Amino Acids 47, 1309-1318 (2015)
- [49] Flynn NE, Meininger CJ, Kelly K, Ing NH, Morris SM Jr and Wu G: Glucocorticoids mediate the enhanced expression of intestinal type II arginase and argininosuccinate synthase in postweaning pigs. J Nutr 129, 799-803 (1999)
- [50] Wu G, Meininger CJ, Kelly K, Watford M and Morris SM Jr: A cortisol surge mediates the enhanced expression of pig intestinal pyrroline-5-carboxylate synthase during weaning. J Nutr 130, 1914-1919 (2000)
- [51] Wang WW, Dai ZL, Wu ZL, Lin G, Jia SC, Hu SD, Dahanayaka S and Wu G: Glycine is a nutritionally essential amino acid for maximal growth of milk-fed young pigs. Amino Acids 46: 2037-2045 (2014)
- [52] Sun YL, Wu ZL, Li W, Zhang C, Sun KJ, Ji Y, Wang B, Jiao N, He BB, Wang WW, Dai ZL and Wu G: Dietary L-leucine supplementation enhances intestinal development in suckling piglets. Amino Acids 47, 1517-1525 (2015)
- [53] Wang L, Hou YQ, Yi D, Ding BY, Zhao D, Wang ZX, Zhu HL, Liu YL, Gong J, Assaad H and Wu G: Dietary oleum cinnamomialleviates intestinal injury. Front Biosci 20: 814-828 (2015)
- [54] Yi D, Hou YQ, Wang L, Zhao D, Ding BY, Wu T, Chen HB, Liu YL, Kang P and Wu G: Gene expression profiles in the intestine of lipopolysaccharide-challenged piglets. Front Biosci 21: 487-501 (2016)
- [55] Wang JJ, Chen LX, Li P, Li XL, Zhou HJ, Wang FL, Li DF, Yin YL and Wu G: Gene expression is altered in piglet small intestine by weaning and dietary glutamine supplementation. J Nutr 138, 1025-1032 (2008)
- [56] Meyuhas O: Synthesis of the translational apparatus is regulated at the translational level. Eur J Biochem 267(21), 6321-6330 (2000)
