CAT-1 as a novel CAM stabilizes endothelial integrity and mediates the protective actions of l-Arg via a NO-independent mechanism

Journal of Molecular and Cellular Cardiology

Volumn 87, Issue , 2015, Pages 180-191

  Guo, Lu ^a   Tian, Shuang ^a   Chen, Yuguo ^a   Mao, Yun ^a   Cui, Sumei ^a   Hu, Aihua ^b   Zhang, Jianliang ^c   Xia, Shen Ling ^c   Su, Yunchao ^c   Du, Jie ^d   Block, Edward R ^c   Wang, Xing Li ^a,e   Cui, Zhaoqiang ^a  

^a SHANDONG UNIVERSITY   (China)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

^d CAPITAL MEDICAL UNIVERSITY   (China)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

CAT 1; Cell adhesion molecule; L arginine paradox; Trans stimulation; Vascular permeability

Indexed keywords

ALBUMIN; AMINO ACID TRANSPORTER; ARGININE; BETA CATENIN; CALCIUM ION; CELL ADHESION MOLECULE; LYSINE; NITRIC OXIDE; VASCULAR ENDOTHELIAL CADHERIN; SLC7A1 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL AGGREGATION; CELL DENSITY; CELL JUNCTION; CELLULAR DISTRIBUTION; CIS TRANS ISOMERISM; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DIMERIZATION; ENDOTHELIUM; FLUORESCENCE ANALYSIS; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INTERNALIZATION; MEMBRANE PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; CAPILLARY PERMEABILITY; GAP JUNCTION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; PATHOLOGY; PIG; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; ARGININE; BETA CATENIN; CAPILLARY PERMEABILITY; CATIONIC AMINO ACID TRANSPORTER 1; CELL ADHESION; GAP JUNCTIONS; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; NITRIC OXIDE; SWINE;

EID: 84940366373     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2015.08.011     Document Type: Article

References (75)

1. Bazzoni G., Dejana E. Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol. Rev. 2004, 84:869-901.
2. Huttner I., More R.H., Rona G. Fine structural evidence of specific mechanism for increased endothelial permeability in experimental hypertension. Am. J. Pathol. 1970, 61:395-412.
3. Tracey K.J., Lowry S.F., Cerami A. Cachetin/TNF-alpha in septic shock and septic adult respiratory distress syndrome. Am. Rev. Respir. Dis. 1988, 138:1377-1379.
4. Mehta D., Malik A.B. Signaling mechanisms regulating endothelial permeability. Physiol. Rev. 2006, 86:279-367.
5. Wojciak-Stothard B., Potempa S., Eichholtz T., Ridley A.J. Rho and Rac but not Cdc42 regulate endothelial cell permeability. J. Cell Sci. 2001, 114:1343-1355.
6. Ogita H., Takai Y. Nectins and nectin-like molecules: roles in cell adhesion, polarization, movement, and proliferation. IUBMB Life 2006, 58:334-343.
7. Lal B.K., Varma S., Pappas P.J., Hobson R.W., Duran W.N. VEGF increases permeability of the endothelial cell monolayer by activation of PKB/akt, endothelial nitric-oxide synthase, and MAP kinase pathways. Microvasc. Res. 2001, 62:252-262.
8. Hood J.D., Meininger C.J., Ziche M., Granger H.J. VEGF upregulates ecNOS message, protein, and NO production in human endothelial cells. Am. J. Physiol. 1998, 274:H1054-H1058.
9. Ramirez M.M., Quardt S.M., Kim D., Oshiro H., Minnicozzi M., Duran W.N. Platelet activating factor modulates microvascular permeability through nitric oxide synthesis. Microvasc. Res. 1995, 50:223-234.
10. Yuan Y., Granger H.J., Zawieja D.C., DeFily D.V., Chilian W.M. Histamine increases venular permeability via a phospholipase C-NO synthase-guanylate cyclase cascade. Am. J. Physiol. 1993, 264:H1734-H1739.
11. Lum H., Malik A.B. Regulation of vascular endothelial barrier function. Am. J. Physiol. 1994, 267:L223-L241.
12. Garcia J.G., Schaphorst K.L. Regulation of endothelial cell gap formation and paracellular permeability. J. Investig. Med. 1995, 43:117-126.
13. Tsukahara H., Noiri E., Jiang M.Z., Hiraoka M., Mayumi M. Role of nitric oxide in human pulmonary microvascular endothelial cell adhesion. Life Sci. 2000, 67:1-11.
14. Kim J.W., Closs E.I., Albritton L.M., Cunningham J.M. Transport of cationic amino acids by the mouse ecotropic retrovirus receptor. Nature 1991, 352:725-728.
15. Baydoun A.R., Emery P.W., Pearson J.D., Mann G.E. Substrate-dependent regulation of intracellular amino acid concentrations in cultured bovine aortic endothelial cells. Biochem. Biophys. Res. Commun. 1990, 173:940-948.
16. Hecker M., Mitchell J.A., Harris H.J., Katsura M., Thiemermann C., Vane J.R. Endothelial cells metabolize NG-monomethyl-l-arginine to l-citrulline and subsequently to l-arginine. Biochem. Biophys. Res. Commun. 1990, 167:1037-1043.
17. Aisaka K., Gross S.S., Griffith O.W., Levi R. l-arginine availability determines the duration of acetylcholine-induced systemic vasodilation in vivo. Biochem. Biophys. Res. Commun. 1989, 163:710-717.
18. Cooke J.P., Andon N.A., Girerd X.J., Hirsch A.T., Creager M.A. Arginine restores cholinergic relaxation of hypercholesterolemic rabbit thoracic aorta. Circulation 1991, 83:1057-1062.
19. Taylor P.D., Poston L. The effect of hyperglycaemia on function of rat isolated mesenteric resistance artery. Br. J. Pharmacol. 1994, 113:801-808.
20. Rossitch E., Alexander E., Black P.M., Cooke J.P. l-arginine normalizes endothelial function in cerebral vessels from hypercholesterolemic rabbits. J. Clin. Invest. 1991, 87:1295-1299.
21. Creager M.A., Gallagher S.J., Girerd X.J., Coleman S.M., Dzau V.J., Cooke J.P. l-arginine improves endothelium-dependent vasodilation in hypercholesterolemic humans. J. Clin. Invest. 1992, 90:1248-1253.
22. Greene B., Pacitti A.J., Souba W.W. Characterization of l-arginine transport by pulmonary artery endothelial cells. Am. J. Physiol. 1993, 264:L351-L356.
23. Woodard M., Dunn W., Laine R., Malandro M., McMahon R., Simell O., et al. Plasma membrane clustering of system y+(CAT-1) amino acid transporter as detected by immunohistochemistry. Am. J. Physiol. Endocrinol. Metab. 1994, 266:E817-E824.
24. Zharikov S.I., Block E.R. Characterization of l-arginine uptake by plasma membrane vesicles isolated from cultured pulmonary artery endothelial cells. Biochim. Biophys. Acta 1998, 1369:173-183.
25. Zharikov S.I., Herrera H., Block E.R. Role of membrane potential in hypoxic inhibition of l-arginine uptake by lung endothelial cells. Am. J. Physiol. 1997, 272:L78-L84.
26. Cui H., Chen B., Chicoine L.G., Nelin L.D. Overexpression of cationic amino acid transporter-1 increases nitric oxide production in hypoxic human pulmonary microvascular endothelial cells. Clin. Exp. Pharmacol. Physiol. 2011, 38:796-803.
27. Cui Z., Zharikov S., Xia S.-L., Anderson S.I., Law A.S., Archibald A.L., et al. Molecular cloning, characterization, and chromosomal assignment of porcine cationic amino acid transporter-1. Genomics 2005, 85:352-359.
28. Cui Z., Tuladhar R., Hart S.L., Marber M.S., Pearson J.D., Baydoun A.R. Rate of transport of l-arginine is independent of the expression of inducible nitric oxide synthase in HEK 293 cells. Nitric Oxide Biol. Chem. 2005, 12:21-30.
29. Cui Z., Han Z., Li Z., Hu H., Patel J.M., Antony V., et al. Involvement of calpain-calpastatin in cigarette smoke-induced inhibition of lung endothelial nitric oxide synthase. Am. J. Respir. Cell Mol. Biol. 2005, 33:513-520.
30. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
31. McDonald K.K., Zharikov S., Block E.R., Kilberg M.S. A caveolar complex between the cationic amino acid transporter 1 and endothelial nitric-oxide synthase may explain the "arginine paradox". J. Biol. Chem. 1997, 272:31213-31216.
32. Takahashi K., Nakanishi H., Miyahara M., Mandai K., Satoh K., Satoh 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, 145:539-549.
33. Aoki J., Koike S., Asou H., Ise I., Suwa H., Tanaka T., et al. Mouse homolog of poliovirus receptor-related gene 2 product, mPRR2, mediates homophilic cell aggregation. Exp. Cell Res. 1997, 235:374-384.
34. Satoh-Horikawa K., Nakanishi H., Takahashi K., Miyahara M., Nishimura M., Tachibana K., et al. Nectin-3, a new member of immunoglobulin-like cell adhesion molecules that shows homophilic and heterophilic cell-cell adhesion activities. J. Biol. Chem. 2000, 275:10291-10299.
35. Miyahara M., Nakanishi H., Takahashi K., Satoh-Horikawa K., Tachibana K., Takai Y. Interaction of nectin with afadin is necessary for its clustering at cell-cell contact sites but not for its cis dimerization or trans interaction. J. Biol. Chem. 2000, 275:613-618.
36. Patterson C.E., Rhoades R.A., Garcia J.G. Evans blue dye as a marker of albumin clearance in cultured endothelial monolayer and isolated lung. J. Appl. Physiol. 1992, 72:865-873.
37. Paunescu T.G., Russo L.M., Da Silva N., Kovacikova J., Mohebbi N., Van Hoek A.N., et al. Compensatory membrane expression of the V-ATPase B2 subunit isoform in renal medullary intercalated cells of B1-deficient mice. Am. J. Physiol. Ren. Physiol. 2007, 293:F1915-F1926.
38. Pastor-Soler N.M., Hallows K.R., Smolak C., Gong F., Brown D., Breton S. Alkaline pH- and cAMP-induced V-ATPase membrane accumulation is mediated by protein kinase A in epididymal clear cells. Am. J. Physiol. Cell Physiol. 2008, 294:C488-C494.
39. Gong F., Alzamora R., Smolak C., Li H., Naveed S., Neumann D., et al. Vacuolar H+-ATPase apical accumulation in kidney intercalated cells is regulated by PKA and AMP-activated protein kinase. Am. J. Physiol. Ren. Physiol. 2010, 298:F1162-F1169.
40. Rotmann A., Strand D., Martiné U., Closs E.I. Protein Kinase C Activation Promotes the Internalization of the Human Cationic Amino Acid Transporter hCAT-1 A NEW REGULATORY MECHANISM FOR hCAT-1 ACTIVITY. J. Biol. Chem. 2004, 279:54185-54192.
41. Takeichi M. Functional correlation between cell adhesive properties and some cell surface proteins. J. Cell Biol. 1977, 75:464-474.
42. Asou H., Miura M., Kobayashi M., Uyemura K., Itoh K. Cell adhesion molecule L1 guides cell migration in primary reaggregation cultures of mouse cerebellar cells. Neurosci. Lett. 1992, 144:221-224.
43. Wolf S., Janzen A., Vékony N., Martiné U., Strand D., Closs E. Expression of solute carrier 7A4 (SLC7A4) in the plasma membrane is not sufficient to mediate amino acid transport activity. Biochem. J. 2002, 364:767-775.
44. Lopez M., Aoubala M., Jordier F., Isnardon D., Gomez S., Dubreuil P. The human poliovirus receptor related 2 protein is a new hematopoietic/endothelial homophilic adhesion molecule. Blood 1998, 92:4602-4611.
45. Reymond N., Fabre S., Lecocq E., Adelaide J., Dubreuil P., Lopez M. Nectin4/PRR4, a new afadin-associated member of the nectin family that trans-interacts with nectin1/PRR1 through V domain interaction. J. Biol. Chem. 2001, 276:43205-43215.
46. Bode-Böger SM B.R., Creutzig A., et al. l-arginine infusion decreases peripheral arterial resistance and inhibits platelet aggregation in healthy subjects. Clin. Sci. (Lond.) 1994, 87:303-310.
47. Bode-Boger S.M., Boger R.H., Alfke H., Heinzel D., Tsikas D., Creutzig A., et al. l-arginine induces nitric oxide-dependent vasodilation in patients with critical limb ischemia. A randomized, controlled study. Circulation 1996, 93:85-90.
48. Bode-Boger S.M., Boger R.H., Galland A., Tsikas D., Frolich J.C. l-arginine-induced vasodilation in healthy humans: pharmacokinetic-pharmacodynamic relationship. Br. J. Clin. Pharmacol. 1998, 46:489-497.
49. Boger R.H., Bode-Boger S.M. The clinical pharmacology of l-arginine. Annu. Rev. Pharmacol. Toxicol. 2001, 41:79-99.
50. Patzke C., Max K.E., Behlke J., Schreiber J., Schmidt H., Dorner A.A., et al. The coxsackievirus-adenovirus receptor reveals complex homophilic and heterophilic interactions on neural cells. J. Neurosci. 2010, 30:2897-2910.
51. Mengaud J., Ohayon H., Gounon P., Mège R.-M., Cossart P. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 1996, 84:923-932.
52. Closs E. CATs, a family of three distinct mammalian cationic amino acid transporters. Amino Acids 1996, 11:193-208.
53. Closs E., Boissel J.-P., Habermeier A., Rotmann A. Structure and function of cationic amino acid transporters (CATs). J. Membr. Biol. 2006, 213:67-77.
54. Sharawy N. Vasoplegia in septic shock: do we really fight the right enemy?. J. Crit. Care 2014, 29:83-87.
55. Lundy D.J., Trzeciak S. Microcirculatory dysfunction in sepsis. Crit. Care Clin. 2009, 25:721-731.
56. Downing S.W., Edmunds L.H. Release of vasoactive substances during cardiopulmonary bypass. Ann. Thorac. Surg. 1992, 54:1236-1243.
57. Boyle M., Edward M., Pohlman M., Timothy H., Johnson M., Marion C., et al. Endothelial cell injury in cardiovascular surgery: the systemic inflammatory response. Ann. Thorac. Surg. 1997, 63:277-284.
58. Moncada S., Palmer R., Higgs E. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 1991, 43:109-142.
59. Wright C.E., Rees D.D., Moncada S. Protective and pathological roles of nitric oxide in endotoxin shock. Cardiovasc. Res. 1992, 26:48-57.
60. Pedoto A., Tassiopoulos A.K., Oler A., McGraw D.J., Hoffmann S.P., Camporesi E.M., et al. Treatment of septic shock in rats with nitric oxide synthase inhibitors and inhaled nitric oxide. Crit. Care Med. 1998, 26:2021-2028.
61. Szabó C., Wu C.-C., Gross S.S., Thiemermann C., Vane J.R. Interleukin-1 contributes to the induction of nitric oxide synthase by endotoxin in vivo. Eur. J. Pharmacol. 1993, 250:157-160.
62. Wu C.-C., Szabo C., Chen S.-J., Thiemermann C., Vane J.R. Activation of soluble guanylyl cyclase by a factor other than nitric oxide or carbon monoxide contributes to the vascular hyporeactivity to vasoconstrictor agents in the aorta of rats treated with endotoxin. Biochem. Biophys. Res. Commun. 1994, 201:436-442.
63. Dubin A. Tetrahydrobiopterin (BH4) in septic shock: a key to solving the nitric oxide puzzle and opening the microcirculation?. Crit. Care Med. 2012, 40:2912-2914.
64. Liu J., Garcia-Cardena G., Sessa W.C. Palmitoylation of endothelial nitric oxide synthase is necessary for optimal stimulated release of nitric oxide: implications for caveolae localization. Biochemistry 1996, 35:13277-13281.
65. Palmer R.M., Moncada S. A novel citrulline-forming enzyme implicated in the formation of nitric oxide by vascular endothelial cells. Biochem. Biophys. Res. Commun. 1989, 158:348-352.
66. Pollock J.S., Forstermann U., Mitchell J.A., Warner T.D., Schmidt H.H., Nakane M., et al. Purification and characterization of particulate endothelium-derived relaxing factor synthase from cultured and native bovine aortic endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:10480-10484.
67. Block E.R., Herrera H., Couch M. Hypoxia inhibits l-arginine uptake by pulmonary artery endothelial cells. Am. J. Physiol. 1995, 269:L574-L580.
68. Hecker M., Sessa W.C., Harris H.J., Anggard E.E., Vane J.R. The metabolism of l-arginine and its significance for the biosynthesis of endothelium-derived relaxing factor: cultured endothelial cells recycle l-citrulline to l-arginine. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:8612-8616.
69. Mitchell J.A., Hecker M., Anggard E.E., Vane J.R. Cultured endothelial cells maintain their l-arginine level despite the continuous release of EDRF. Eur. J. Pharmacol. 1990, 182:573-576.
70. Gold M.E., Bush P.A., Ignarro L.J. Depletion of arterial l-arginine causes reversible tolerance to endothelium-dependent relaxation. Biochem. Biophys. Res. Commun. 1989, 164:714-721.
71. Arnal J.F., Munzel T., Venema R.C., James N.L., Bai C.L., Mitch W.E., et al. Interactions between l-arginine and l-glutamine change endothelial NO production. An effect independent of NO synthase substrate availability. J. Clin. Invest. 1995, 95:2565-2572.
72. Eddahibi S., Adnot S., Carville C., Blouquit Y., Raffestin B. l-arginine restores endothelium-dependent relaxation in pulmonary circulation of chronically hypoxic rats. Am. J. Physiol. 1992, 263:L194-L200.
73. Closs E.I., Lyons C.R., Kelly C., Cunningham J.M. Characterization of the third member of the MCAT family of cationic amino acid transporters. Identification of a domain that determines the transport properties of the MCAT proteins. J. Biol. Chem. 1993, 268:20796-20800.
74. Kavanaugh M.P. Voltage dependence of facilitated arginine flux mediated by the system y+basic amino acid transporter. Biochemistry 1993, 32:5781-5785.
75. Christensen H.N. Kinetics in transport. Biological Transport 1975, 107-165. Benjamin, Reading, Mass. 2nd ed.