L-glutamine enhances tight junction integrity by activating CaMK kinase 2-AMP-activated protein kinase signaling in intestinal porcine epithelial cells

Journal of Nutrition

Volumn 146, Issue 3, 2016, Pages 501-508

  Wang, Bin ^a   Wu, Zhenlong ^a   Ji, Yun ^a   Sun, Kaiji ^a   Dai, Zhaolai ^a   Wu, Guoyao ^a,b  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

AMPK; CaMKK2; Intestinal epithelial cells; L glutamine; Tight junction

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CLAUDIN 4; GLUTAMINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; JUNCTIONAL ADHESION MOLECULE A; OCCLUDIN; ZONULA OCCLUDENS PROTEIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE KINASE; JUNCTIONAL ADHESION MOLECULE; PROTEIN ZO1; PROTEIN ZO2;

ANIMAL CELL; ARTICLE; CALCIUM DEPLETION; CELL COUNT; CELL GROWTH; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DIET SUPPLEMENTATION; ENZYME ACTIVATION; INTESTINE EPITHELIUM CELL; INTRACELLULAR SIGNALING; NEWBORN; NONHUMAN; PIGLET; PORCINE MODEL; SMALL INTESTINE; TIGHT JUNCTION; TRANSEPITHELIAL RESISTANCE; ANIMAL; CELL MEMBRANE; CYTOLOGY; DRUG EFFECTS; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; INTESTINE; INTESTINE CELL; INTESTINE MUCOSA; METABOLISM; PHOSPHORYLATION; PIG; SIGNAL TRANSDUCTION;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANIMALS, NEWBORN; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE KINASE; CELL MEMBRANE; CELL PROLIFERATION; CLAUDIN-4; ENTEROCYTES; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; GLUTAMINE; INTESTINAL MUCOSA; INTESTINES; JUNCTIONAL ADHESION MOLECULES; OCCLUDIN; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SWINE; TIGHT JUNCTIONS; ZONULA OCCLUDENS-1 PROTEIN; ZONULA OCCLUDENS-2 PROTEIN;

EID: 84960441074     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.115.224857     Document Type: Article

References (42)

1. Ballard ST, Hunter JH, Taylor AE. Regulation of tight-junction permeability during nutrient absorption across the intestinal epithelium. Annu Rev Nutr 1995;15:35-55.
2. Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 2009;9:799-809.
3. Suzuki T. Regulation of intestinal epithelial permeability by tight junctions. Cell Mol Life Sci 2013;70:631-59.
4. Wang B, Wu G, Zhou Z, Dai Z, Sun Y, Ji Y, Li W, Wang W, Liu C, Han F, et al. Glutamine and intestinal barrier function. Amino Acids 2015;47:2143-54.
5. Turner JR, Buschmann MM, Romero-Calvo I, Sailer A, Shen L. The role of molecular remodeling in differential regulation of tight junction permeability. Semin Cell Dev Biol 2014;36:204-12.
6. Fakhoury M, Negrulj R, Mooranian A, Al-Salami H. Inflammatory bowel disease: clinical aspects and treatments. J Inflamm Res 2014;7: 113-20.
7. Marchiando AM, Graham WV, Turner JR. Epithelial barriers in homeostasis and disease. Annu Rev Pathol 2010;5:119-44.
8. Ulluwishewa D, Anderson RC, McNabb WC, Moughan PJ, Wells JM, Roy NC. Regulation of tight junction permeability by intestinal bacteria and dietary components. J Nutr 2011;141:769-76.
9. Wu G, Wu Z, Dai Z, Yang Y, Wang W, Liu C, Wang B, Wang J, Yin Y. Dietary requirements of ''nutritionally non-essential amino acids'' by animals and humans. Amino Acids 2013;44:1107-13.
10. Wu G. Functional amino acids in growth, reproduction, and health. Adv Nutr 2010;1:31-7.
11. Li N, Lewis P, Samuelson D, Liboni K, Neu J. Glutamine regulates Caco-2 cell tight junction proteins. Am J Physiol Gastrointest Liver Physiol 2004;287:G726-33.
12. Wu G, Meier SA, Knabe DA. Dietary glutamine supplementation prevents jejunal atrophy in weaned pigs. J Nutr 1996;126:2578-84.
13. Li N, DeMarco VG, West CM, Neu J. Glutamine supports recovery from loss of transepithelial resistance and increase of permeability induced by media change in Caco-2 cells. J Nutr Biochem 2003;14:401-8.
14. Zhou Q, Souba WW, Croce CM, Verne GN. MicroRNA-29a regulates intestinal membrane permeability in patients with irritable bowel syndrome. Gut 2010;59:775-84.
15. Chaudhry KK, Shukla PK, Mir H, Manda B, Gangwar R, Yadav N, McMullen M, Nagy LE, Rao R. Glutamine supplementation attenuates ethanol-induced disruption of apical junctional complexes in colonic epithelium and ameliorates gut barrier dysfunction and fatty liver in mice. J Nutr Biochem 2016;27:16-26.
16. Bertrand J, Ghouzali I, Guerin C, Bole-Feysot C, Gouteux M, Dechelotte P, Ducrotte P, Coeffier M. Glutamine restores tight junction protein claudin-1 expression in colonic mucosa of patients with diarrheapredominant irritable bowel syndrome. JPEN J Parenter Enteral Nutr 2015 May 13 (Epub ahead of print; pii: 0148607115587330).
17. Wang H, Zhang C, Wu G, Sun Y, Wang B, He B, Dai Z, Wu Z. Glutamine enhances tight junction protein expression and modulates corticotropin-releasing factor signaling in the jejunum of weanling piglets. J Nutr 2015;145:25-31.
18. Li N, Neu J. Glutamine deprivation alters intestinal tight junctions via a PI3-K/Akt mediated pathway in Caco-2 cells. J Nutr 2009;139:710-4.
19. Deli MA. Potential use of tight junction modulators to reversibly open membranous barriers and improve drug delivery. Biochim Biophys Acta 2009;1788:892-910.
20. Bleich M, Shan Q, Himmerkus N. Calcium regulation of tight junction permeability. Ann N Y Acad Sci 2012;1258:93-9.
21. Ma TY, Tran D, Hoa N, Nguyen D, Merryfield M, Tarnawski A. Mechanism of extracellular calcium regulation of intestinal epithelial tight junction permeability: role of cytoskeletal involvement. Microsc Res Tech 2000;51:156-68.
22. Woods A, Dickerson K, Heath R, Hong SP, Momcilovic M, Johnstone SR, Carlson M, Carling D. Ca2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab 2005;2:21-33.
23. Haynes TE, Li P, Li X, Shimotori K, Sato H, Flynn NE, Wang J, Knabe DA, Wu G. L-Glutamine or L-alanyl-L-glutamine prevents oxidant-or endotoxin-induced death of neonatal enterocytes. Amino Acids 2009;37: 131-42.
24. Tafazoli F, Zeng CQ, Estes MK, Magnusson KE, Svensson L. NSP4 enterotoxin of rotavirus induces paracellular leakage in polarized epithelial cells. J Virol 2001;75:1540-6.
25. Jiao N, Wu Z, Ji Y, Wang B, Dai Z, Wu G. L-glutamate enhances barrier and antioxidative functions in intestinal porcine epithelial cells. J Nutr 2015;145:2258-64.
26. Wang H, Ji Y, Wu G, Sun K, Sun Y, Li W, Wang B, He B, Zhang Q, Dai Z, et al. l-tryptophan activates mammalian target of rapamycin and enhances expression of tight junction proteins in intestinal porcine epithelial cells. J Nutr 2015;145:1156-62.
27. Zhang L, Li J, Young LH, Caplan MJ. AMP-activated protein kinase regulates the assembly of epithelial tight junctions. Proc Natl Acad Sci USA 2006;103:17272-7.
28. Tokumitsu H, Inuzuka H, Ishikawa Y, Ikeda M, Saji I, Kobayashi R. STO-609, a specific inhibitor of the Ca(2+)/calmodulin-dependent protein kinase kinase. J Biol Chem 2002;277:15813-8.
29. Racioppi L, Means AR. Calcium/calmodulin-dependent protein kinase kinase 2: roles in signaling and pathophysiology. J Biol Chem 2012;287: 31658-65.
30. Peng L, Li ZR, Green RS, Holzman IR, Lin J. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J Nutr 2009;139:1619-25.
31. Amasheh M, Andres S, Amasheh S, Fromm M, Schulzke JD. Barrier effects of nutritional factors. Ann N Y Acad Sci 2009;1165:267-73.
32. Wu G, Fang YZ, Yang S, Lupton JR, Turner ND. Glutathione metabolism and its implications for health. J Nutr 2004;134:489-92.
33. Wang J, Chen L, Li P, Li X, Zhou H, Wang F, Li D, Yin Y, Wu G. Gene expression is altered in piglet small intestine by weaning and dietary glutamine supplementation. J Nutr 2008;138:1025-32.
34. Chow A, Zhang R. Glutamine reduces heat shock-induced cell death in rat intestinal epithelial cells. J Nutr 1998;128:1296-301.
35. Shen L, Black ED, Witkowski ED, Lencer WI, Guerriero V, Schneeberger EE, Turner JR. Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. J Cell Sci 2006;119: 2095-106.
36. Elamin EE, Masclee AA, Dekker J, Pieters HJ, Jonkers DM. Short-chain fatty acids activate AMP-activated protein kinase and ameliorate ethanol-induced intestinal barrier dysfunction in Caco-2 cell monolayers. J Nutr 2013;143:1872-81.
37. Hamada K, Shitara Y, Sekine S, Horie T. Zonula occludens-1 alterations and enhanced intestinal permeability in methotrexate-treated rats. Cancer Chemother Pharmacol 2010;66:1031-8.
38. Li Q, Zhang Q, Wang C, Liu X, Qu L, Gu L, Li N, Li J. Altered distribution of tight junction proteins after intestinal ischaemia/reperfusion injury in rats. J Cell Mol Med 2009;13:4061-76.
39. Umeda K, Matsui T, Nakayama M, Furuse K, Sasaki H, Furuse M, Tsukita S. Establishment and characterization of cultured epithelial cells lacking expression of ZO-1. J Biol Chem 2004;279:44785-94.
40. Jouret F, Wu J, Hull M, Rajendran V, Mayr B, SchoflC, Geibel J, Caplan MJ. Activation of the Ca(2)+-sensing receptor induces deposition of tight junction components to the epithelial cell plasma membrane. J Cell Sci 2013;126:5132-42.
41. Fanning AS, Ma TY, Anderson JM. Isolation and functional characterization of the actin binding region in the tight junction protein ZO-1. FASEB J 2002;16:1835-7.
42. Rhoads JM, Argenzio RA, Chen W, Rippe RA, Westwick JK, Cox AD, Berschneider HM, Brenner DA. L-glutamine stimulates intestinal cell proliferation and activates mitogen-activated protein kinases. Am J Physiol 1997;272:G943-53.