AMPK in regulation of apical junctions and barrier function of intestinal epithelium

References

• Matter K, Balda MS. Signalling to and from tight junctions. Nat Rev Mol Biol. 2003;4(3):225–236. doi: 10.1038/nrm1055.
   PubMed Web of Science ®Google Scholar
• Gumbiner B. Structure, biochemistry, and assembly of epithelial tight junctions. Am J Physiol. 1987;253(6 Pt 1):C749–758. doi: 10.1152/ajpcell.1987.253.6.C749.
   PubMedGoogle Scholar
• Heath JK. Transcriptional networks and signaling pathways that govern vertebrate intestinal development. Curr Top Dev Biol. 2010;90:159–192. doi: 10.1016/S0070-2153(10)90004-5.
   PubMed Web of Science ®Google Scholar
• Tsukita S, Furuse M, Itoh M. Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol. 2001;2(4):285–293. doi: 10.1038/35067088.
   PubMed Web of Science ®Google Scholar
• Zeissig S, Burgel N, Gunzel D, Richter J, Mankertz J, Wahnschaffe U, Kroesen AJ, Zeitz M, Fromm M, Schulzke JD. Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn’s disease. Gut. 2007;56(1):61–72. doi: 10.1136/gut.2006.094375.
   PubMed Web of Science ®Google Scholar
• Laukoetter MG, Nava P, Lee WY, Severson EA, Capaldo CT, Babbin BA, Williams IR, Koval M, Peatman E, Campbell JA, et al. JAM-A regulates permeability and inflammation in the intestine in vivo. J Exp Med. 2007;204(13):3067–3076. doi: 10.1084/jem.20071416.
   PubMed Web of Science ®Google Scholar
• Vetrano S, Rescigno M, Cera MR, Correale C, Rumio C, Doni A, Fantini M, Sturm A, Borroni E, Repici A, et al. Unique role of junctional adhesion molecule-a in maintaining mucosal homeostasis in inflammatory bowel disease. Gastroenterology. 2008;135(1):173–184. doi: 10.1053/j.gastro.2008.04.002.
   PubMed Web of Science ®Google Scholar
• Sun X, Yang Q, Rogers CJ, Du M, Zhu MJ. AMPK improves gut epithelial differentiation and barrier function via regulating Cdx2 expression. Cell Death Differ. 2017;24(5):819–831. doi: 10.1038/cdd.2017.14.
   PubMed Web of Science ®Google Scholar
• Yu TX, Gu BL, Yan JK, Zhu J, Yan WH, Chen J, Qian LX, Cai W. CUGBP1 and HuR regulate E-cadherin translation by altering recruitment of E-cadherin mRNA to processing bodies and modulate epithelial barrier function. Am J Physiol Cell Physiol. 2016;310(1):C54–65. doi: 10.1152/ajpcell.00112.2015.
   PubMed Web of Science ®Google Scholar
• Kiesslich R, Duckworth CA, Moussata D, Gloeckner A, Lim LG, Goetz M, Pritchard DM, Galle PR, Neurath MF, Watson AJ. Local barrier dysfunction identified by confocal laser endomicroscopy predicts relapse in inflammatory bowel disease. Gut. 2012;61(8):1146–1153. doi: 10.1136/gutjnl-2011-300695.
   PubMed Web of Science ®Google Scholar
• Lee SY, Lee SH, Yang EJ, Kim EK, Kim JK, Shin DY, Cho ML. Metformin ameliorates inflammatory bowel disease by suppression of the STAT3 signaling pathway and regulation of the between Th17/Treg Balance. PLoS One. 2015;10(9):e0135858. doi: 10.1371/journal.pone.0135858.
   PubMed Web of Science ®Google Scholar
• Piepenhagen PA, Nelson WJ. Differential expression of cell-cell and cell-substratum adhesion proteins along the kidney nephron. Am J Physiology-Cell Physiol. 1995;269(6):C1433–C1449. doi: 10.1152/ajpcell.1995.269.6.C1433.
   Web of Science ®Google Scholar
• Förster C. Tight junctions and the modulation of barrier function in disease. Histochem Cell Biol. 2008;130(1):55–70. doi: 10.1007/s00418-008-0424-9.
   PubMed Web of Science ®Google Scholar
• Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007;56(7):1761–1772. doi: 10.2337/db06-1491.
   PubMed Web of Science ®Google Scholar
• Clairembault T, Leclair-Visonneau L, Coron E, Bourreille A, Le Dily S, Vavasseur F, Heymann M-F, Neunlist M, Derkinderen P. Structural alterations of the intestinal epithelial barrier in Parkinson’s disease. Acta Neuropathol Commun. 2015;3(1):12. doi: 10.1186/s40478-015-0196-0.
   PubMedGoogle Scholar
• Z Alam M, Alam Q, A Kamal M, M Abuzenadah A, Haque AA. possible link of gut microbiota alteration in type 2 diabetes and Alzheimer’s disease pathogenicity: an update. CNS Neurol Disord Drug Targets (Formerly Current Drug Targets-CNS Neurological Disorders). 2014;13(3):383–390.
   PubMed Web of Science ®Google Scholar
• Buscarinu MC, Cerasoli B, Annibali V, Policano C, Lionetto L, Capi M, Mechelli R, Romano S, Fornasiero A, Mattei G. Altered intestinal permeability in patients with relapsing–remitting multiple sclerosis: A pilot study. Mult Scler J. 2017;23(3):442–446. doi: 10.1177/1352458516652498.
   PubMed Web of Science ®Google Scholar
• Kahn BB, Alquier T, Carling D, Hardie DG. AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab. 2005;1(1):15–25. doi: 10.1016/j.cmet.2004.12.003.
   PubMed Web of Science ®Google Scholar
• Hardie DG. Biochemistry. Balancing cellular energy. Science. 2007;315(5819):1671–1672. doi: 10.1126/science.1140737.
   PubMed Web of Science ®Google Scholar
• Fu X, Zhao JX, Liang J, Zhu MJ, Foretz M, Viollet B, Du M. AMP-activated protein kinase mediates myogenin expression and myogenesis via histone deacetylase 5. Am J Physiol Cell Physiol. 2013;305(8):C887–895. doi: 10.1152/ajpcell.00124.2013.
   PubMed Web of Science ®Google Scholar
• Wang S, Liang X, Yang Q, Fu X, Zhu M, Rodgers BD, Jiang Q, Dodson MV, Du M. Resveratrol enhances brown adipocyte formation and function by activating AMP-activated protein kinase (AMPK) alpha1 in mice fed high-fat diet. Mol Nutr Food Res. 2017;61(4):1600746. doi: 10.1002/mnfr.201600746.
   Web of Science ®Google Scholar
• Dzeja PP, Chung S, Faustino RS, Behfar A, Terzic A. Developmental enhancement of adenylate kinase-AMPK metabolic signaling axis supports stem cell cardiac differentiation. PLoS One. 2011;6(4):e19300. doi: 10.1371/journal.pone.0019300.
   PubMed Web of Science ®Google Scholar
• Sun X, Fu X, Du M, Zhu MJ. Ex vivo gut culture for studying differentiation and migration of small intestinal epithelial cells. Open Biol. 2018;8(4):170256. doi: 10.1098/rsob.170256.
   PubMed Web of Science ®Google Scholar
• Bays JL, Campbell HK, Heidema C, Sebbagh M, DeMali KA. Linking E-cadherin mechanotransduction to cell metabolism through force-mediated activation of AMPK. Nat Cell Biol. 2017;19(6):724–731. doi: 10.1038/ncb3537.
   PubMed Web of Science ®Google Scholar
• 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(9):1619–1625. doi: 10.3945/jn.109.104638.
   PubMed Web of Science ®Google Scholar
• Scharl M, Paul G, Barrett KE, McCole DF. AMP-activated protein kinase mediates the interferon-gamma-induced decrease in intestinal epithelial barrier function. J Biol Chem. 2009;284(41):27952–27963. doi: 10.1074/jbc.M109.046292.
   PubMed Web of Science ®Google Scholar
• Sun X, Du M, Navarre DA, Zhu MJ. Purple potato extract promotes intestinal epithelial differentiation and barrier function by activating AMP-activated protein kinase. Mol Nutr Food Res. 2018;62(4):1700536. doi: 10.1002/mnfr.201700536.
   Web of Science ®Google Scholar
• Wang K, Jin X, Chen Y, Song Z, Jiang X, Hu F, Conlon MA, Topping DL. Polyphenol-rich propolis extracts strengthen intestinal barrier function by activating AMPK and ERK signaling. Nutrients. 2016;8(5):272. doi: 10.3390/nu8050272.
   PubMed Web of Science ®Google Scholar
• Meddings J. The significance of the gut barrier in disease. Gut. 2008;57(4):438–440. doi: 10.1136/gut.2007.143172.
   PubMed Web of Science ®Google Scholar
• Denker BM, Nigam SK. Molecular structure and assembly of the tight junction. Am J Physiol. 1998;274(1 Pt 2):F1–9.
   PubMedGoogle Scholar
• Kimura Y, Shiozaki H, Hirao M, Maeno Y, Doki Y, Inoue M, Monden T, Ando-Akatsuka Y, Furuse M, Tsukita S, et al. Expression of occludin, tight-junction-associated protein, in human digestive tract. Am J Pathol. 1997;151(1):45–54.
   PubMed Web of Science ®Google Scholar
• Mehta S, Nijhuis A, Kumagai T, Lindsay J, Silver A. Defects in the adherens junction complex (E-cadherin/beta-catenin) in inflammatory bowel disease. Cell Tissue Res. 2015;360(3):749–760. doi: 10.1007/s00441-014-1994-6.
   PubMed Web of Science ®Google Scholar
• Burdett ID. Aspects of the structure and assembly of desmosomes. Micron. 1998;29(4):309–328.
   PubMed Web of Science ®Google Scholar
• Garrod D, Chidgey M. Desmosome structure, composition and function. Biochim Biophys Acta. 2008;1778(3):572–587. doi: 10.1016/j.bbamem.2007.07.014.
   PubMed Web of Science ®Google Scholar
• Walko G, Castanon MJ, Wiche G. Molecular architecture and function of the hemidesmosome. Cell Tissue Res. 2015;360(3):529–544. doi: 10.1007/s00441-015-2216-6.
   PubMed Web of Science ®Google Scholar
• Goodenough DA, Paul DL. Gap junctions. Cold Spring Harb Perspect Biol. 2009;1(1):a002576. doi: 10.1101/cshperspect.a002576.
   PubMed Web of Science ®Google Scholar
• Hartsock A, Nelson WJ. Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim Biophys Acta. 2008;1778(3):660–669. doi: 10.1016/j.bbamem.2007.07.012.
   PubMed Web of Science ®Google Scholar
• Furuse M, Hirase T, Itoh M, Nagafuchi A, Yonemura S, Tsukita S, Tsukita S. Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol. 1993;123(6 Pt 2):1777–1788.
   PubMed Web of Science ®Google Scholar
• Suzuki T, Elias BC, Seth A, Shen L, Turner JR, Giorgianni F, Desiderio D, Guntaka R, Rao R. PKC eta regulates occludin phosphorylation and epithelial tight junction integrity. Proc Natl Acad Sci U S A. 2009;106(1):61–66. doi: 10.1073/pnas.0802741106.
   PubMed Web of Science ®Google Scholar
• Chiba H, Osanai M, Murata M, Kojima T, Sawada N. Transmembrane proteins of tight junctions. Biochim Biophys Acta. 2008;1778(3):588–600. doi: 10.1016/j.bbamem.2007.08.017.
   PubMed Web of Science ®Google Scholar
• Raleigh DR, Marchiando AM, Zhang Y, Shen L, Sasaki H, Wang Y, Long M, Turner JR. Tight junction-associated MARVEL proteins marveld3, tricellulin, and occludin have distinct but overlapping functions. Mol Biol Cell. 2010;21(7):1200–1213. doi: 10.1091/mbc.E09-08-0734.
   PubMed Web of Science ®Google Scholar
• Furuse M, Fujita K, Hiiragi T, Fujimoto K, Tsukita S. Claudin-1 and −2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol. 1998;141(7):1539–1550.
   PubMed Web of Science ®Google Scholar
• Itoh M, Furuse M, Morita K, Kubota K, Saitou M, Tsukita S. Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J Cell Biol. 1999;147(6):1351–1363.
   PubMed Web of Science ®Google Scholar
• Mineta K, Yamamoto Y, Yamazaki Y, Tanaka H, Tada Y, Saito K, Tamura A, Igarashi M, Endo T, Takeuchi K, et al. Predicted expansion of the claudin multigene family. FEBS Lett. 2011;585(4):606–612. doi: 10.1016/j.febslet.2011.01.028.
   PubMed Web of Science ®Google Scholar
• Amasheh S, Meiri N, Gitter AH, Schoneberg T, Mankertz J, Schulzke JD, Fromm M. Claudin-2 expression induces cation-selective channels in tight junctions of epithelial cells. J Cell Sci. 2002;115(Pt 24):4969–4976.
   PubMed Web of Science ®Google Scholar
• Rosenthal R, Milatz S, Krug SM, Oelrich B, Schulzke JD, Amasheh S, Gunzel D, Fromm M. Claudin-2, a component of the tight junction, forms a paracellular water channel. J Cell Sci. 2010;123(Pt 11):1913–1921. doi: 10.1242/jcs.060665.
   PubMed Web of Science ®Google Scholar
• Bibi S, Kang Y, Du M, Zhu MJ. Dietary red raspberries attenuate dextran sulfate sodium-induced acute colitis. J Nutr Biochem. 2018;51:40–46. doi: 10.1016/j.jnutbio.2017.08.017.
   PubMed Web of Science ®Google Scholar
• Prasad S, Mingrino R, Kaukinen K, Hayes KL, Powell RM, MacDonald TT, Collins JE. Inflammatory processes have differential effects on claudins 2, 3 and 4 in colonic epithelial cells. Lab Invest. 2005;85(9):1139–1162. doi: 10.1038/labinvest.3700316.
   PubMed Web of Science ®Google Scholar
• Luettig J, Rosenthal R, Barmeyer C, Schulzke JD. Claudin-2 as a mediator of leaky gut barrier during intestinal inflammation. Tissue Barriers. 2015;3(1–2):e977176. doi: 10.4161/21688370.2014.977176.
   PubMed Web of Science ®Google Scholar
• Martin-Padura I, Lostaglio S, Schneemann M, Williams L, Romano M, Fruscella P, Panzeri C, Stoppacciaro A, Ruco L, Villa A, et al. Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol. 1998;142(1):117–127.
   PubMed Web of Science ®Google Scholar
• Ebnet K. Junctional adhesion molecules (JAMs): cell adhesion receptors with pleiotropic functions in cell physiology and development. Physiol Rev. 2017;97(4):1529–1554. doi: 10.1152/physrev.00004.2017.
   PubMed Web of Science ®Google Scholar
• Steinbacher T, Kummer D, Ebnet K. Junctional adhesion molecule-A: functional diversity through molecular promiscuity. Cell Mol Life Sci. 2018;75(8):1393–1409. doi: 10.1007/s00018-017-2729-0.
   PubMed Web of Science ®Google Scholar
• Chopyk DM, Kumar P, Raeman R, Liu Y, Smith T, Anania FA. Dysregulation of junctional adhesion molecule-A contributes to ethanol-induced barrier disruption in intestinal epithelial cell monolayers. Physiol Rep. 2017;5(23):e13541. doi: 10.14814/phy2.13262.
   Web of Science ®Google Scholar
• Ikenouchi J, Furuse M, Furuse K, Sasaki H, Tsukita S, Tsukita S. Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. J Cell Biol. 2005;171(6):939–945. doi: 10.1083/jcb.200510043.
   PubMed Web of Science ®Google Scholar
• Krug SM, Bojarski C, Fromm A, Lee IM, Dames P, Richter JF, Turner JR, Fromm M, Schulzke JD. Tricellulin is regulated via interleukin-13-receptor alpha2, affects macromolecule uptake, and is decreased in ulcerative colitis. Mucosal Immunol. 2018. doi: 10.1038/mi.2017.1052.
   Web of Science ®Google Scholar
• Morampudi V, Graef FA, Stahl M, Dalwadi U, Conlin VS, Huang T, Vallance BA, Yu HB, Jacobson K. Tricellular tight junction protein tricellulin is targeted by the enteropathogenic Escherichia coli effector EspG1, leading to epithelial barrier disruption. Infect Immun. 2017;85(1):e00700–00716. doi: 10.1128/IAI.00700-16.
   PubMed Web of Science ®Google Scholar
• Meng W, Takeichi M. Adherens junction: molecular architecture and regulation. Cold Spring Harb Perspect Biol. 2009;1(6):a002899. doi: 10.1101/cshperspect.a002899.
   PubMed Web of Science ®Google Scholar
• Overduin M, Harvey TS, Bagby S, Tong KI, Yau P, Takeichi M, Ikura M. Solution structure of the epithelial cadherin domain responsible for selective cell adhesion. Science. 1995;267(5196):386–389.
   PubMed Web of Science ®Google Scholar
• Wu Y, Jin X, Harrison O, Shapiro L, Honig BH, Ben-Shaul A. Cooperativity between trans and cis interactions in cadherin-mediated junction formation. Proc Natl Acad Sci U S A. 2010;107(41):17592–17597. doi: 10.1073/pnas.1011247107.
   PubMed Web of Science ®Google Scholar
• Rimm DL, Koslov ER, Kebriaei P, Cianci CD, Morrow JS. Alpha 1(E)-catenin is an actin-binding and -bundling protein mediating the attachment of F-actin to the membrane adhesion complex. Proc Natl Acad Sci U S A. 1995;92(19):8813–8817.
   PubMed Web of Science ®Google Scholar
• Takahashi K, Nakanishi H, Miyahara M, Mandai K, Satoh K, Satoh A, Nishioka H, Aoki J, Nomoto A, Mizoguchi A, et al. Nectin/PRR: an immunoglobulin-like cell adhesion molecule recruited to cadherin-based adherens junctions through interaction with Afadin, a PDZ domain-containing protein. J Cell Biol. 1999;145(3):539–549.
   PubMed Web of Science ®Google Scholar
• Reymond N, Borg JP, Lecocq E, Adelaide J, Campadelli-Fiume G, Dubreuil P, Lopez M. Human nectin3/PRR3: a novel member of the PVR/PRR/nectin family that interacts with afadin. Gene. 2000;255(2):347–355.
   PubMed Web of Science ®Google Scholar
• Itoh M, Nagafuchi A, Moroi S, Tsukita S. Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to alpha catenin and actin filaments. J Cell Biol. 1997;138(1):181–192.
   PubMed Web of Science ®Google Scholar
• Yamamoto T, Harada N, Kano K, Taya S, Canaani E, Matsuura Y, Mizoguchi A, Ide C, Kaibuchi K. The Ras target AF-6 interacts with ZO-1 and serves as a peripheral component of tight junctions in epithelial cells. J Cell Biol. 1997;139(3):785–795.
   PubMed Web of Science ®Google Scholar
• Campbell HK, Maiers JL, DeMali KA. Interplay between tight junctions & adherens junctions. Exp Cell Res. 2017;358(1):39–44. doi: 10.1016/j.yexcr.2017.03.061.
   PubMed Web of Science ®Google Scholar
• Yoshida-Noro C, Suzuki N, Takeichi M. Molecular nature of the calcium-dependent cell-cell adhesion system in mouse teratocarcinoma and embryonic cells studied with a monoclonal antibody. Dev Biol. 1984;101(1):19–27.
   PubMed Web of Science ®Google Scholar
• Oakhill JS, Steel R, Chen ZP, Scott JW, Ling N, Tam S, Kemp BE. AMPK is a direct adenylate charge-regulated protein kinase. Science. 2011;332(6036):1433–1435. doi: 10.1126/science.1200094.
   PubMed Web of Science ®Google Scholar
• Ross FA, Jensen TE, Hardie DG. Differential regulation by AMP and ADP of AMPK complexes containing different gamma subunit isoforms. Biochem J. 2016;473(2):189–199. doi: 10.1042/BJ20150910.
   PubMedGoogle Scholar
• Davies SP, Helps NR, Cohen PT, Hardie DG. 5ʹ-AMP inhibits dephosphorylation, as well as promoting phosphorylation, of the AMP-activated protein kinase. Studies using bacterially expressed human protein phosphatase-2C alpha and native bovine protein phosphatase-2AC. FEBS Lett. 1995;377(3):421–425. doi: 10.1016/0014-5793(95)01368-7.
   PubMed Web of Science ®Google Scholar
• Fujiwara Y, Kawaguchi Y, Fujimoto T, Kanayama N, Magari M, Tokumitsu H. Differential AMP-activated protein kinase (AMPK) recognition mechanism of Ca2+/Calmodulin-dependent protein kinase kinase isoforms. J Biol Chem. 2016;291(26):13802–13808. doi: 10.1074/jbc.M116.727867.
   PubMed Web of Science ®Google Scholar
• Momcilovic M, Hong SP, Carlson M. Mammalian TAK1 activates Snf1 protein kinase in yeast and phosphorylates AMP-activated protein kinase in vitro. J Biol Chem. 2006;281(35):25336–25343. doi: 10.1074/jbc.M604399200.
   PubMed Web of Science ®Google Scholar
• Steinberg GR, Kemp BE. AMPK in health and disease. Physiol Rev. 2009;89(3):1025–1078. doi: 10.1152/physrev.00011.2008.
   PubMed Web of Science ®Google Scholar
• Xue Y, Zhang H, Sun X, Zhu MJ. Metformin improves ileal epithelial barrier function in interleukin-10 deficient mice. PLoS One. 2016;11(12):e0168670. doi: 10.1371/journal.pone.0168670.
   PubMed Web of Science ®Google Scholar
• Zhang L, Li J, Young LH, Caplan MJ. AMP-activated protein kinase regulates the assembly of epithelial tight junctions. Proc Natl Acad Sci U S A. 2006;103(46):17272–17277. doi: 10.1073/pnas.0608531103.
   PubMed Web of Science ®Google Scholar
• Zheng B, Cantley LC. Regulation of epithelial tight junction assembly and disassembly by AMP-activated protein kinase. Proc Natl Acad Sci U S A. 2007;104(3):819–822. doi: 10.1073/pnas.0610157104.
   PubMed Web of Science ®Google Scholar
• Zhang L, Jouret F, Rinehart J, Sfakianos J, Mellman I, Lifton RP, Young LH, Caplan MJ. AMP-activated protein kinase (AMPK) activation and glycogen synthase kinase-3β (GSK-3β) inhibition induce Ca2+-independent deposition of tight junction components at the plasma membrane. J Biol Chem. 2011;286(19):16879–16890. doi: 10.1074/jbc.M110.186932.
   PubMed Web of Science ®Google Scholar
• Rowart P, Erpicum P, Krzesinski JM, Sebbagh M, Jouret F. Mesenchymal stromal cells accelerate epithelial tight junction assembly via the AMP-activated protein kinase pathway, independently of liver kinase B1. Stem Cells Int. 2017;2017:9717353. doi: 10.1155/2017/9717353.
   PubMedGoogle Scholar
• Tang XX, Chen H, Yu S, Zhang L, Caplan MJ, Chan HC. Lymphocytes accelerate epithelial tight junction assembly: role of AMP-activated protein kinase (AMPK). PLoS One. 2010;5(8):e12343. doi: 10.1371/journal.pone.0012343.
   PubMed Web of Science ®Google Scholar
• Muanprasat C, Wongkrasant P, Satitsri S, Moonwiriyakit A, Pongkorpsakol P, Mattaveewong T, Pichyangkura R, Chatsudthipong V. Activation of AMPK by chitosan oligosaccharide in intestinal epithelial cells: mechanism of action and potential applications in intestinal disorders. Biochem Pharmacol. 2015;96(3):225–236. doi: 10.1016/j.bcp.2015.05.016.
   PubMed Web of Science ®Google Scholar
• Pongkorpsakol P, Satitsri S, Wongkrasant P, Chittavanich P, Kittayaruksakul S, Srimanote P, Chatsudthipong V, Muanprasat C. Flufenamic acid protects against intestinal fluid secretion and barrier leakage in a mouse model of Vibrio cholerae infection through NF-kappaB inhibition and AMPK activation. Eur J Pharmacol. 2017;798:94–104. doi: 10.1016/j.ejphar.2017.01.026.
   PubMed Web of Science ®Google Scholar
• Shiomi R, Shigetomi K, Inai T, Sakai M, Ikenouchi J. CaMKII regulates the strength of the epithelial barrier. Sci Rep. 2015;5:13262. doi: 10.1038/srep13262.
   PubMed Web of Science ®Google Scholar
• Xiang RL, Mei M, Cong X, Li J, Zhang Y, Ding C, Wu LL, Yu GY. Claudin-4 is required for AMPK-modulated paracellular permeability in submandibular gland cells. J Mol Cell Biol. 2014;6(6):486–497. doi: 10.1093/jmcb/mju048.
   PubMed Web of Science ®Google Scholar
• Glotfelty LG, Zahs A, Iancu C, Shen L, Hecht GA. Microtubules are required for efficient epithelial tight junction homeostasis and restoration. Am J Physiology-Cell Physiol. 2014;307(3):C245–C254. doi: 10.1152/ajpcell.00336.2013.
   PubMed Web of Science ®Google Scholar
• Yano T, Matsui T, Tamura A, Uji M, Tsukita S. The association of microtubules with tight junctions is promoted by cingulin phosphorylation by AMPK. J Cell Biol. 2013;203(4):605–614. doi: 10.1083/jcb.201304194.
   PubMed Web of Science ®Google Scholar
• Aznar N, Patel A, Rohena CC, Dunkel Y, Joosen LP, Taupin V, Kufareva I, Farquhar MG, Ghosh P. AMP-activated protein kinase fortifies epithelial tight junctions during energetic stress via its effector GIV/Girdin. Elife. 2016;5:e20795. doi: 10.7554/eLife.20795.
   PubMed Web of Science ®Google Scholar
• Park HY, Kunitake Y, Hirasaki N, Tanaka M, Matsui T. Theaflavins enhance intestinal barrier of Caco-2 Cell monolayers through the expression of AMP-activated protein kinase-mediated Occludin, Claudin-1, and ZO-1. Bioscience Biotechnology and Biochemistry. 2015;79(1):130–137. doi: 10.1080/09168451.2014.951027.
   PubMed Web of Science ®Google Scholar
• Wang B, Wu Z, Ji Y, Sun K, Dai Z, Wu G. L-glutamine enhances tight junction integrity by activating CaMK kinase 2-AMP-activated protein kinase signaling in intestinal porcine epithelial cells. J Nutr. 2016;146(3):501–508. doi: 10.3945/jn.115.224857.
   PubMed Web of Science ®Google Scholar
• Akhmanova A, Steinmetz MO. Control of microtubule organization and dynamics: two ends in the limelight. Nat Rev Mol Cell Biol. 2015;16(12):711. doi: 10.1038/nrm4084.
   PubMed Web of Science ®Google Scholar
• Takeichi M. Dynamic contacts: rearranging adherens junctions to drive epithelial remodelling. Nat Rev Mol Cell Biol. 2014;15(6):397. doi: 10.1038/nrm3802.
   PubMed Web of Science ®Google Scholar
• Nakano A, Kato H, Watanabe T, Min K-D, Yamazaki S, Asano Y, Seguchi O, Higo S, Shintani Y, Asanuma H. AMPK controls the speed of microtubule polymerization and directional cell migration through CLIP-170 phosphorylation. Nat Cell Biol. 2010;12(6):583–590. doi: 10.1038/ncb2060.
   PubMed Web of Science ®Google Scholar
• Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol. 2009;10(11):778.
   PubMed Web of Science ®Google Scholar
• Cunningham KE, Turner JR. Myosin light chain kinase: pulling the strings of epithelial tight junction function. Ann N Y Acad Sci. 2012;1258(1):34–42. doi: 10.1111/j.1749-6632.2012.06526.x.
   PubMedGoogle Scholar
• Lee JH, Koh H, Kim M, Kim Y, Lee SY, Karess RE, Lee S-H, Shong M, Kim J-M, Kim J. Energy-dependent regulation of cell structure by AMP-activated protein kinase. Nature. 2007;447(7147):1017–1020. doi: 10.1038/nature05828.
   PubMed Web of Science ®Google Scholar
• Ginzberg RD, Gilula NB. Modulation of cell junctions during differentiation of the chicken otocyst sensory epithelium. Dev Biol. 1979;68(1):110–129.
   PubMed Web of Science ®Google Scholar
• Batts LE, Polk DB, Dubois RN, Kulessa H. Bmp signaling is required for intestinal growth and morphogenesis. Dev Dyn. 2006;235(6):1563–1570. doi: 10.1002/dvdy.20741.
   PubMed Web of Science ®Google Scholar
• Yang G, Wang H, Kang Y, Zhu MJ. Grape seed extract improves epithelial structure and suppresses inflammation in ileum of IL-10-deficient mice. Food Funct. 2014;5(10):2558–2563. doi: 10.1039/c4fo00451e.
   PubMed Web of Science ®Google Scholar
• Di Fusco D, Dinallo V, Monteleone I, Laudisi F, Marafini I, Franze E, Di Grazia A, Dwairi R, Colantoni A, Ortenzi A, et al. Metformin inhibits inflammatory signals in the gut by controlling AMPK and p38 MAP kinase activation. Clin Sci (Lond). 2018. doi: 10.1042/CS20180167.
   PubMed Web of Science ®Google Scholar
• Koh SJ, Kim JM, Kim IK, Ko SH, Kim JS. Anti-inflammatory mechanism of metformin and its effects in intestinal inflammation and colitis-associated colon cancer. J Gastroenterol Hepatol. 2014;29(3):502–510.
   PubMed Web of Science ®Google Scholar
• Jones RG, Plas DR, Kubek S, Buzzai M, Mu J, Xu Y, Birnbaum MJ, Thompson CB. AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol Cell. 2005;18(3):283–293. doi: 10.1016/j.molcel.2005.03.027.
   PubMed Web of Science ®Google Scholar
• Shaw RJ, Bardeesy N, Manning BD, Lopez L, Kosmatka M, DePinho RA, Cantley LC. The LKB1 tumor suppressor negatively regulates mTOR signaling. Cancer Cell. 2004;6(1):91–99. doi: 10.1016/j.ccr.2004.06.007.
   PubMed Web of Science ®Google Scholar
• O’neill LA, Hardie DG. Metabolism of inflammation limited by AMPK and pseudo-starvation. Nature. 2013;493(7432):346–355. doi: 10.1038/nature11862.
   PubMed Web of Science ®Google Scholar
• Bibi S, Kang Y, Du M, Zhu MJ. Maternal high-fat diet consumption enhances offspring susceptibility to DSS-induced colitis in mice. Obesity (Silver Spring). 2017;25(5):901–908. doi: 10.1002/oby.21816.
   PubMed Web of Science ®Google Scholar
• Brusq J-M, Ancellin N, Grondin P, Guillard R, Martin S, Saintillan Y, Issandou M. Inhibition of lipid synthesis through activation of AMP kinase: an additional mechanism for the hypolipidemic effects of berberine. J Lipid Res. 2006;47(6):1281–1288. doi: 10.1194/jlr.M600020-JLR200.
   PubMed Web of Science ®Google Scholar
• Chen MB, McAinch AJ, Macaulay SL, Castelli LA, O’Brien PE, Dixon JB, Cameron-Smith D, Kemp BE, Steinberg GR. Impaired activation of AMP-kinase and fatty acid oxidation by globular adiponectin in cultured human skeletal muscle of obese type 2 diabetics. J Clin Endocrinol Metabolism. 2005;90(6):3665–3672. doi: 10.1210/jc.2004-1980.
   PubMed Web of Science ®Google Scholar
• Group DPPR. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med. 2002;2002(346):393–403.
   Google Scholar
• Spruss A, Kanuri G, Stahl C, Bischoff SC, Bergheim I. Metformin protects against the development of fructose-induced steatosis in mice: role of the intestinal barrier function. Lab Invest. 2012;92(7):1020–1032. doi: 10.1038/labinvest.2012.75.
   PubMed Web of Science ®Google Scholar
• Lee YS, Kim WS, Kim KH, Yoon MJ, Cho HJ, Shen Y, Ye JM, Lee CH, Oh WK, Kim CT, et al. Berberine, a natural plant product, activates AMP-activated protein kinase with beneficial metabolic effects in diabetic and insulin-resistant states. Diabetes. 2006;55(8):2256–2264. doi: 10.2337/db06-0006.
   PubMed Web of Science ®Google Scholar
• Shen L, Xiong Y, Wang DQ, Howles P, Basford JE, Wang J, Xiong YQ, Hui DY, Woods SC, Liu M. Ginsenoside Rb1 reduces fatty liver by activating AMP-activated protein kinase in obese rats. J Lipid Res. 2013;54(5):1430–1438. doi: 10.1194/jlr.M035907.
   PubMed Web of Science ®Google Scholar
• Reiter CE, Kim JA, Quon MJ. Green tea polyphenol epigallocatechin gallate reduces endothelin-1 expression and secretion in vascular endothelial cells: roles for AMP-activated protein kinase, Akt, and FOXO1. Endocrinology. 2010;151(1):103–114. doi: 10.1210/en.2009-0997.
   PubMed Web of Science ®Google Scholar
• Wang S, Liang X, Yang Q, Fu X, Rogers CJ, Zhu M, Rodgers BD, Jiang Q, Dodson MV, Du M. Resveratrol induces brown-like adipocyte formation in white fat through activation of AMP-activated protein kinase (AMPK) alpha1. Int J Obes (Lond). 2015;39(6):967–976. doi: 10.1038/ijo.2015.23.
   PubMed Web of Science ®Google Scholar
• Yang G, Xue Y, Zhang H, Du M, Zhu MJ. Favourable effects of grape seed extract on intestinal epithelial differentiation and barrier function in IL10-deficient mice. Br J Nutr. 2015;114(1):15–23. doi: 10.1017/S0007114515001415.
   PubMed Web of Science ®Google Scholar
• Harikumar KB, Aggarwal BB. Resveratrol: a multitargeted agent for age-associated chronic diseases. Cell Cycle. 2008;7(8):1020–1035. doi: 10.4161/cc.7.8.5740.
   PubMed Web of Science ®Google Scholar
• Tome-Carneiro J, Gonzalvez M, Larrosa M, Yanez-Gascon MJ, Garcia-Almagro FJ, Ruiz-Ros JA, Garcia-Conesa MT, Tomas-Barberan FA, Espin JC. One-year consumption of a grape nutraceutical containing resveratrol improves the inflammatory and fibrinolytic status of patients in primary prevention of cardiovascular disease. Am J Cardiol. 2012;110(3):356–363. doi: 10.1016/j.amjcard.2012.03.030.
   PubMed Web of Science ®Google Scholar
• Robich MP, Osipov RM, Nezafat R, Feng J, Clements RT, Bianchi C, Boodhwani M, Coady MA, Laham RJ, Sellke FW. Resveratrol improves myocardial perfusion in a swine model of hypercholesterolemia and chronic myocardial ischemia. Circulation. 2010;122(11 Suppl):S142–149. doi: 10.1161/CIRCULATIONAHA.109.920132.
   PubMed Web of Science ®Google Scholar
• Ong KW, Hsu A, Tan BK. Anti-diabetic and anti-lipidemic effects of chlorogenic acid are mediated by ampk activation. Biochem Pharmacol. 2013;85(9):1341–1351. doi: 10.1016/j.bcp.2013.02.008.
   PubMed Web of Science ®Google Scholar
• Hashemzehi M, Behnam-Rassouli R, Hassanian SM, Moradi-Binabaj M, Moradi-Marjaneh R, Rahmani F, Fiuji H, Jamili M, Mirahmadi M, Boromand N, et al. Phytosomal-curcumin antagonizes cell growth and migration, induced by thrombin through AMP-Kinase in breast cancer. J Cell Biochem. 2018. doi: 10.1002/jcb.v119.7.
   Web of Science ®Google Scholar
• Liu K, Mei F, Wang Y, Xiao N, Yang L, Wang Y, Li J, Huang F, Kou J, Liu B, et al. Quercetin oppositely regulates insulin-mediated glucose disposal in skeletal muscle under normal and inflammatory conditions: the dual roles of AMPK activation. Mol Nutr Food Res. 2016;60(3):551–565. doi: 10.1002/mnfr.201500509.
   PubMed Web of Science ®Google Scholar