Sphingosine-1-phosphate regulates the expression of adherens junction protein E-cadherin and enhances intestinal epithelial cell barrier function

Digestive Diseases and Sciences

Volumn 56, Issue 5, 2011, Pages 1342-1353

  Greenspon, Jose ^b   Li, Ruiyun ^a,b   Xiao, Lan ^a,b   Rao, Jaladanki N ^a,b   Sun, Rex ^b   Strauch, Eric D ^b   Shea Donohue, Terez ^b   Wang, Jian Ying ^a,b   Turner, Douglas J ^a  

^a BALTIMORE VA MEDICAL CENTER   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Ca2+ signaling; Intestinal barrier; Intestinal epithelium; Sphingosine

Indexed keywords

MESSENGER RNA; SPHINGOSINE 1 PHOSPHATE; UVOMORULIN;

ARTICLE; CELL ADHESION; CELL JUNCTION; CELL MEMBRANE PERMEABILITY; ELECTRIC RESISTANCE; IN VITRO STUDY; INTESTINE EPITHELIUM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSEPITHELIAL ELECTRICAL RESISTANCE;

ADHERENS JUNCTIONS; ANIMALS; BETA CATENIN; CADHERINS; CALCIUM; CELL ADHESION MOLECULES; CELLS, CULTURED; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; INTESTINAL MUCOSA; LYSOPHOSPHOLIPIDS; RNA INTERFERENCE; SPHINGOSINE;

EID: 79955610423     PISSN: 01632116     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10620-010-1421-0     Document Type: Article

References (68)

1. Carneiro-Filho BA, Lima IP, Araujo DH, et al. Intestinal barrier function and secretion in methotrexate-induced rat intestinal mucositis. Dig Dis Sci. 2004;49:65-72. (Pubitemid 38183747)
2. Lima AA, Silva TM, Gifoni AM, et al. Mucosal injury and disruption of intestinal barrier function in HIV-infected individuals with and without diarrhea and cryptosporidiosis in northeast Brazil. Am J Gastroenterol. 1997;92:1861-1866.
3. Cereijido M, Shoshani L, Contreras RG. Molecular physiology and pathophysiology of tight junctions. I. Biogenesis of tight junctions and epithelial polarity. Am J Physiol Gastrointest Liver Physiol. 2000;279:G477-G482.
4. 2+ in cultured epithelia. Biochim Biophys Acta. 1222;147-158:1994.
5. Gumbiner BM. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell. 1996;84:345-357. (Pubitemid 26058560)
6. Mitic LL, Anderson JM. Molecular architecture of tight junctions. Annu Rev Physiol. 1998;60:121-142. (Pubitemid 28157867)
7. Takeichi M. Cadherins: a molecular family important in selective cell - cell adhesion. Annu Rev Biochem. 1990;59:237-252.
8. Yap AS, Brieher WM, Gumbiner BM. Molecular and functional analysis of cadherin-based adherens junctions. Annu Rev Cell Dev Biol. 1997;13:119-146. (Pubitemid 28034522)
9. Cereijido M, Valdés J, Shoshani L, et al. Role of tight junctions in establishing and maintaining cell polarity. Annu Rev Physiol. 1998;60:161-177. (Pubitemid 28157869)
10. Gumbiner B, Stevenson B, Grimaldi A. The role of the cell adhesion molecule uvomorulin in the formation and maintenance of the epithelial junctional complex. J Cell Biol. 1988;107:1575-1587.
11. Madara JL. Regulation of the movement of solutes across tight junctions. Annu Rev Physiol. 1998;60:143-159. (Pubitemid 28157868)
12. Nusrat A, Parkos CA, Verkade P, et al. Tight junctions are membrane microdomains. J Cell Sci. 2000;113(Pt 10):1771-1781. (Pubitemid 30333126)
13. Adams CL, Nelson WJ, Smith SJ. Quantitative analysis of cadherin - catenin - actin reorganization during development of cell- cell adhesion. J Cell Biol. 1996;135:1899-1911. (Pubitemid 27036450)
14. Angres B, Barth A, Nelson WJ. Mechanism for transition from initial to stable cell - cell adhesion: kinetic analysis of E-cadherin-mediated adhesion using a quantitative adhesion assay. J Cell Biol. 1996;134:549-557. (Pubitemid 26250720)
15. Hanby AM, Chinery R, Poulsom R, et al. Downregulation of Ecadherin in the reparative epithelium of the human gastrointestinal tract. Am J Pathol. 1996;148:723-729. (Pubitemid 126660665)
16. Shore EM, Nelson WJ. Biosynthesis of the cell adhesion molecule uvomorulin (E-cadherin) in Madin - Darby canine kidney epithelial cells. J Biol Chem. 1991;266:19672-19680. (Pubitemid 21908280)
17. Angst BD, Marcozzi C, Magee AI. The cadherin superfamily. J Cell Sci. 2001;114:625-626. (Pubitemid 32237134)
18. Rimm DL, Koslov ER, Kebriaei P, et al. 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 USA. 1995;92:8813-8817.
19. Troxell ML, Chen YT, Cobb N, et al. Cadherin function in junctional complex rearrangement and posttranslational control of cadherin expression. Am J Physiol. 1999;276:C404-C418. (Pubitemid 29100564)
20. Weiss EE, Kroemker M, Rüdiger AH, et al. Vinculin is part of the cadherin - catenin junctional complex: complex formation between alpha-catenin and vinculin. J Cell Biol. 1998;141:755-764. (Pubitemid 28217919)
21. Dudek SM, Jacobson JR, Chiang ET, et al. Pulmonary endothelial cell barrier enhancement by sphingosine 1-phosphate: roles for cortactin and myosin light chain kinase. J Biol Chem. 2004;279:24692-24700. (Pubitemid 38725337)
22. English D, Kovala AT, Welch Z, et al. Induction of endothelial cell chemotaxis by sphingosine 1-phosphate and stabilization of endothelial monolayer barrier function by lysophosphatidic acid, potential mediators of hematopoietic angiogenesis. J Hematother Stem Cell Res. 1999;8:627-634. (Pubitemid 30041245)
23. Feistritzer C, Riewald M. Endothelial barrier protection by activated protein C through PAR1-dependent sphingosine 1-phosphate receptor-1 crossactivation. Blood. 2005;105:3178-3184.
24. McVerry BJ, Garcia JG. Endothelial cell barrier regulation by sphingosine 1-phosphate. J Cell Biochem. 2004;92:1075-1085. (Pubitemid 44264219)
25. Siess W. Athero- and thrombogenic actions of lysophosphatidic acid and sphingosine-1-phosphate. Biochim Biophys Acta. 2002;1582:204-215. (Pubitemid 34634131)
26. Singleton PA, Dudek SM, Chiang ET, et al. Regulation of sphingosine 1-phosphate-induced endothelial cytoskeletal rearrangement and barrier enhancement by S1P1 receptor, PI3 kinase, Tiam1/Rac1, and alpha-actinin. FASEB J. 2005;19:1646-1656. (Pubitemid 41429522)
27. Singleton PA, Dudek SM, Ma SF, et al. Transactivation of sphingosine 1-phosphate receptors is essential for vascular barrier regulation: novel role for hyaluronan and cd44 receptor family. J Biol Chem. 2006;281:34381-34393. (Pubitemid 46036646)
28. English D, Welch Z, Kovala AT, et al. Sphingosine 1-phosphate released from platelets during clotting accounts for the potent endothelial cell chemotactic activity of blood serum and provides a novel link between hemostasis and angiogenesis. FASEB J. 2000;14:2255-2265.
29. Nugent D, Xu Y. Sphingosine-1-phosphate: characterization of its inhibition of platelet aggregation. Platelets. 2000;11:226-232. (Pubitemid 30479683)
30. Ryu Y, Takuwa N, Sugimoto N, et al. Sphingosine-1-phosphate, a platelet-derived lysophospholipid mediator, negatively regulates cellular Rac activity and cell migration in vascular smooth muscle cells. Circ Res. 2002;90:325-332. (Pubitemid 34633934)
31. Schaphorst KL, Chiang E, Jacobs KN, et al. Role of sphingosine- 1 phosphate in the enhancement of endothelial barrier integrity by platelet-released products. Am J Physiol Lung Cell Mol Physiol. 2003;285:L258-L267. (Pubitemid 36736489)
32. Björklund S, Palmberg S, Rask S, et al. Effects of sphingosine 1-phosphate on calcium signaling, proliferation and S1P2 receptor expression in PC Cl3 rat thyroid cells. Mol Cell Endocrinol. 2005;231:65-74. (Pubitemid 40248817)
33. 2+ signaling induced by sphingosylphosphorylcholine and sphingosine 1-phosphate via distinct mechanisms in rat glomerular mesangial cells. Kidney Int. 1998;54:1470-1483.
34. Dahm F, Nocito A, Bielawska A, et al. Distribution and dynamic changes of sphingolipids in blood in response to platelet activation. J Thromb Haemost. 2006;4:2704-2709. (Pubitemid 44741568)
35. Davaille J, Li L, Mallat A, et al. Sphingosine 1-phosphate triggers both apoptotic and survival signals for human hepatic myofibroblasts. J Biol Chem. 2002;277:37323-37330.
36. Kaneko T, Murakami T, Kawana H, et al. Sphingosine-1-phosphate receptor agonists suppress concanavalin A-induced hepatic injury in mice. Biochem Biophys Res Commun. 2006;345:85-92.
37. Karliner JS, Honbo N, Summers K, et al. The lysophospholipids sphingosine-1-phosphate and lysophosphatidic acid enhance survival during hypoxia in neonatal rat cardiac myocytes. J Mol Cell Cardiol. 2001;33:1713-1717. (Pubitemid 32844228)
38. Laychock SG, Sessanna SM, Lin MH, et al. Sphingosine 1- phosphate affects cytokine-induced apoptosis in rat pancreatic islet beta-cells. Endocrinology. 2006;147:4705-4712. (Pubitemid 44402178)
39. Peng X, Hassoun PM, Sammani S, et al. Protective effects of sphingosine 1-phosphate in murine endotoxin-induced inflammatory lung injury. Am J Respir Crit Care Med. 2004;169:1245-1251. (Pubitemid 38680403)
40. Finigan JH, Dudek SM, Singleton PA, et al. Activated protein C mediates novel lung endothelial barrier enhancement: role of sphingosine 1-phosphate receptor transactivation. J Biol Chem. 2005;280:17286-17293. (Pubitemid 41389197)
41. McVerry BJ, Garcia JG. In vitro and in vivo modulation of vascular barrier integrity by sphingosine 1-phosphate: mechanistic insights. Cell Signal. 2005;17:131-139.
42. 2+ mediates rac activation and adherens junction assembly in endothelial cells. J Biol Chem. 2005;280:17320-17328.
43. Shikata Y, Birukov KG, Garcia JG. S1P induces FA remodeling in human pulmonary endothelial cells: role of Rac, GIT1, FAK, and paxillin. J Appl Physiol. 2003;94:1193-1203. (Pubitemid 36232038)
44. Lee M-J, Thangada S, Claffey KP, et al. Vascular endothelial cell adherens junction assembly and morphogenesis induced by sphingosine-1-phosphate. Cell. 1999;99:301-312. (Pubitemid 29519909)
45. Lee M-J, Van Brocklyn JR, Thangada S, et al. Sphingosine-1-phosphate as a ligand for the G protein-coupled receptor EDG-1. Science. 1998;279:1552-1555. (Pubitemid 28217081)
46. Thamilselvan V, Li W, Sumpio BE, et al. Sphingosine-1-phosphate stimulates human Caco-2 intestinal epithelial proliferation via p38 activation and activates ERK by an independent mechanism. In Vitro Cell Dev Biol Anim. 2002;38:246-253. (Pubitemid 34975850)
47. Yatomi Y, Welch RJ, Igarashi Y. Distribution of sphingosine 1-phosphate, a bioactive sphingolipid, in rat tissues. FEBS Lett. 1997;404:173-174. (Pubitemid 27113447)
48. Kohno M, Momoi M, Oo ML, et al. Intracellular role for sphingosine kinase 1 in intestinal adenoma cell proliferation. Mol Cell Biol. 2006;26:7211-7223. (Pubitemid 44477697)
49. Suh E, Traber PG. An intestine-specific homeobox gene regulates proliferation and differentiation. Mol Cell Biol. 1996;16:619-625. (Pubitemid 26029101)
50. Guo X, Rao JN, Liu L, et al. Polyamines are necessary for synthesis and stability of occludin protein in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2005;288:G1159-G1169. (Pubitemid 40741068)
51. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-254.
52. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680-685.
53. Vielkind U, Swierenga SH. A simple fixation procedure for immunofluorescent detection of different cytoskeletal components within the same cell. Histochemistry. 1989;91:81-88. (Pubitemid 19051630)
54. 2+) during intestinal epithelial cell migration. Am J Physiol Cell Physiol. 2002;283:C722-C734.
55. Wang JY, McCormack SA, Johnson LR. Role of nonmuscle myosin II in polyamine-dependent intestinal epithelial cell migration. Am J Physiol. 1996;270:G355-G362.
56. 2+-RhoA signaling pathway required for polyamine-dependent intestinal epithelial cell migration. Am J Physiol Cell Physiol. 2001;280:C993-C1007.
57. Wang JY, Wang J, Golovina VA, et al. Role of K(+) channel expression in polyamine-dependent intestinal epithelial cell migration. Am J Physiol Cell Physiol. 2000;278:C303-C314. (Pubitemid 30131147)
58. Parekh AB, Penner R. Store depletion and calcium influx. Physiol Rev. 1997;77:901-930. (Pubitemid 27459576)
59. Wong V, Gumbiner BM. A synthetic peptide corresponding to the extracellular domain of occludin perturbs the tight junction permeability barrier. J Cell Biol. 1997;136:399-409. (Pubitemid 27063089)
60. Balda MS, Whitney JA, Flores C, et al. Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical - basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein. J Cell Biol. 1996;134:1031-1049. (Pubitemid 26278226)
61. Liu TS, Musch MW, Sugi K, et al. Protective role of HSP72 against Clostridium difficile toxin A-induced intestinal epithelial cell dysfunction. Am J Physiol Cell Physiol. 2003;284:C1073-C1082. (Pubitemid 36336964)
62. Guo X, Rao JN, Liu L, et al. Regulation of adherens junctions and epithelial paracellular permeability: a novel function for polyamines. Am J Physiol Cell Physiol. 2003;285:C1174-C1187. (Pubitemid 37296294)
63. Dudek SM, Garcia JG. Cytoskeletal regulation of pulmonary vascular permeability. J Appl Physiol. 2001;91:1487-1500. (Pubitemid 32900340)
64. Liu Y, Wada R, Yamashita T, et al. Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation. J Clin Investig. 2000;106:951-961.
65. Greenspon J, Li R, Xiao L, et al. Sphingosine-1-phosphate protects intestinal epithelial cells from apoptosis through the Akt signaling pathway. Dig Dis Sci. 2008;54:499-510.
66. CoradaM,Liao F, LindgrenM, et al.Monoclonal antibodies directed to different regions of vascular endothelial cadherin extracellular domain affect adhesion and clustering of the protein and modulate endothelial permeability. Blood. 2001;97:1679-1684.
67. Corada M, Mariotti M, Thurston G, et al. Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo. Proc Natl Acad Sci USA. 1999;96:9815-9820. (Pubitemid 29398815)
68. Yang Z, Zhang H, Kumar R. Regulation of E-cadherin. Breast Cancer Online. 2005;8:e15.