Forces and dynamics of glucose and inhibitor binding to sodium glucose co-transporter SGLT1 studied by single molecule force spectroscopy

Journal of Biological Chemistry

Volumn 289, Issue 31, 2014, Pages 21673-21683

  Neundlinger, Isabel ^a   Puntheeranurak, Theeraporn ^a,b   Wildling, Linda ^a   Rankl, Christian ^c   Wang, Lai Xi ^d   Gruber, Hermann J ^a   Kinne, Rolf K H ^e   Hinterdorfer, Peter ^a  

^a JOHANNES KEPLER UNIVERSITY LINZ   (Austria)

^b Mahidol University   (Thailand)

^c Agilent Technologies Osterrreich GmbH   (Austria)

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

^e MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMIC FORCE MICROSCOPY; CONFORMATIONS; ENERGY BARRIERS; GLUCOSE; MOLECULAR PHYSICS; POLYETHYLENE GLYCOLS; RATE CONSTANTS; SODIUM;

ATOMIC FORCE MICROSCOPY TIPS; CONFORMATIONAL STATE; INCREASING TEMPERATURES; SINGLE MOLECULE FORCE SPECTROSCOPY; SINGLE MOLECULE LEVEL; TEMPERATURE SENSITIVITY; TEMPERATURE-SENSITIVE; TRANSPORT INHIBITORS;

LOADING;

2' AMINOETHYL BETA DEXTRO GLUCOPYRANOSIDE; AMINOPHLORIZIN; GLUCOPYRANOSIDE; GLUCOSE; LIGAND; MACROGOL; PHLORIZIN; SODIUM GLUCOSE COTRANSPORTER 1; THIOGLUCOSE; UNCLASSIFIED DRUG; PROTEIN BINDING;

ARTICLE; ATOMIC FORCE MICROSCOPY; AVERAGE LIFE TIME; BINDING AFFINITY; BINDING PROBABILITY; BINDING SITE; CARBOHYDRATE TRANSPORT; CHO CELL LINE; CONTROLLED STUDY; DYNAMICS; HIGH TEMPERATURE; HUMAN; HUMAN CELL; LOW TEMPERATURE; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN CONFORMATION; RETRACTION VELOCITY; SINGLE MOLECULE FORCE SPECTROSCOPY; SPECTROSCOPY; TEMPERATURE DEPENDENCE; TEMPERATURE SENSITIVITY; WIDTH OF ENERGY BARRIER; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; CRICETULUS; HAMSTER; METABOLISM;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; MICROSCOPY, ATOMIC FORCE; PROTEIN BINDING; SODIUM-GLUCOSE TRANSPORTER 1;

EID: 84905400374     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.529875     Document Type: Article

References (65)

1. Crane, R. K. (1977) The gradient hypothesis and other models of carrier-mediated active transport. Rev. Physiol. Biochem. Pharmacol. 78, 99-159
2. Wright, E. M., Loo, D. D., and Hirayama, B. A. (2011) Biology of human sodium glucose transporters. Physiol. Rev. 91, 733-794
3. +/D-glucose cotransporters SGLT1 and SGLT2. Am. J. Physiol. Cell Physiol. 300, C14-C21
4. Wright, E. M. (1998) I. Glucose galactose malabsorption. Am. J. Physiol. 275, G879-G882
5. Castaneda, F., Burse, A., Boland, W., and Kinne, R. K. (2007) Thioglycosides as inhibitors of hSGLT1 and hSGLT2: potential therapeutic agents for the control of hyperglycemia in diabetes. Int. J. Med. Sci. 4, 131-139 (Pubitemid 46710987)
6. Kinne, R. K., and Castaneda, F. (2011) SGLT inhibitors as new therapeutic tools in the treatment of diabetes. Handb. Exp. Pharmacol. 203, 105-126
7. Castaneda, F., and Kinne, R. K. (2005) A 96-well automated method to study inhibitors of human sodium-dependent D-glucose transport. Mol. Cell Biochem. 280, 91-98 (Pubitemid 41829804)
8. -/GABA (hGAT1) cotransporters. Br. J. Pharmacol. 134, 484-495
9. Tyagi, N. K., Kumar, A., Goyal, P., Pandey, D., Siess, W., and Kinne, R. K. (2007) D-Glucose recognition and phlorizin-binding sites in human sodium/ D-glucose cotransporter 1 (hSGLT1): a tryptophan scanning study. Biochemistry 46, 13616-13628 (Pubitemid 350209957)
10. Raja, M. M., Tyagi, N. K., and Kinne, R. K. (2003) Phlorizin recognition in a C-terminal fragment of SGLT1 studied by tryptophan scanning and affinity labeling. J. Biol. Chem. 278, 49154-49163
11. Wright, E. M., Hirayama, B. A., and Loo, D. F. (2007) Active sugar transport in health and disease. J. Intern. Med. 261, 32-43 (Pubitemid 46046470)
12. Lin, J., Kormanec, J., Homerová, D., and Kinne, R. K. (1999) Probing transmembrane topology of the high-affinity sodium/glucose cotransporter (SGLT1) with histidine-tagged mutants. J. Membr. Biol. 170, 243-252 (Pubitemid 29382905)
13. Watanabe, A., Choe, S., Chaptal, V., Rosenberg, J. M., Wright, E. M., Grabe, M., and Abramson, J. (2010) The mechanism of sodium and substrate release from the binding pocket of vSGLT. Nature 468, 988-991
14. +/glucose cotransporter 1 contains both stereospecific and non-stereospecific sugar interaction sites. J. Biol. Chem. 284, 983-991
15. Sala-Rabanal, M., Hirayama, B. A., Loo, D. D., Chaptal, V., Abramson, J., and Wright, E. M. (2012) Bridging the gap between structure and kinetics of human SGLT1. Am. J. Physiol. Cell Physiol. 302, C1293-C1305
16. Hinterdorfer, P., Baumgartner, W., Gruber, H. J., Schilcher, K., and Schindler, H. (1996) Detection and localization of individual antibody-antigen recognition events by atomic force microscopy. Proc. Natl. Acad. Sci. U.S.A. 93, 3477-3481 (Pubitemid 26125645)
17. Hinterdorfer, P., and Dufrêne, Y. F. (2006) Detection and localization of single molecular recognition events using atomic force microscopy. Nat. Methods 3, 347-355
18. Wildling, L., Rankl, C., Haselgrübler, T., Gruber, H. J., Holy, M., Newman, A. H., Zou, M. F., Zhu, R., Freissmuth, M., Sitte, H. H., and Hinterdorfer, P. (2012) Probing binding pocket of serotonin transporter by single molecular force spectroscopy on living cells. J. Biol. Chem. 287, 105-113
19. +-glucose cotransporter SGLT1 in living cells. J. Cell Sci. 119, 2960-2967
20. Puntheeranurak, T., Wimmer, B., Castaneda, F., Gruber, H. J., Hinterdorfer, P., and Kinne, R. K. (2007) Substrate specificity of sugar transport by rabbit SGLT1: single-molecule atomic force microscopy versus transport studies. Biochemistry 46, 2797-2804 (Pubitemid 46417918)
21. +/glucose cotransporter SGLT1. J. Biol. Chem. 282, 25222-25230
22. Diedrich, D. F. (1966) Competitive inhibition of intestinal glucose transport by phlorizin analogs. Arch. Biochem. Biophys. 117, 248-256
23. Kumar, A., Tyagi, N. K., and Kinne, R. K. (2007) Ligand-mediated conformational changes and positioning of tryptophans in reconstituted human sodium/D-glucose cotransporter1 (hSGLT1) probed by tryptophan fluorescence. Biophys. Chem. 127, 69-77
24. Loo, D. D., Hirayama, B. A., Cha, A., Bezanilla, F., and Wright, E. M. (2005) Perturbation analysis of the voltage-sensitive conformational changes of the Na+/glucose cotransporter. J. Gen. Physiol. 125, 13-36 (Pubitemid 40130095)
25. Oulianova, N., Falk, S., and Berteloot, A. (2001) Two-step mechanism of phlorizin binding to the SGLT1 protein in the kidney. J. Membr. Biol. 179, 223-242 (Pubitemid 32165797)
26. Kipp, H., Lin, J. T., and Kinne, R. K. (1996) Interactions of alkylglucosides with the renal sodium/D-glucose cotransporter. Biochim. Biophys. Acta 1282, 125-130
27. + glucose cotransporter SGLT1 contains a binding site for alkyl glucosides. Biochemistry 43, 10944-10951
28. Lee, G. U., Chrisey, L. A., and Colton, R. J. (1994) Direct measurement of the forces between complementary strands of DNA. Science 266, 771-773 (Pubitemid 24359278)
29. Florin, E. L., Moy, V. T., and Gaub, H. E. (1994) Adhesion forces between individual ligand-receptor pairs. Science 264, 415-417 (Pubitemid 24179839)
30. Rico, F., and Moy, V. T. (2007) Energy landscape roughness of the streptavidin-biotin interaction. J. Mol. Recognit. 20, 495-501
31. De Smedt, H., and Kinne, R. (1981) Temperature dependence of solute transport and enzyme activities in hog renal brush border membrane vesicles. Biochim. Biophys. Acta 648, 247-253
32. Ni, J., Singh, S., and Wang, L. X. (2003) Synthesis of maleimide-activated carbohydrates as chemoselective tags for site-specific glycosylation of peptides and proteins. Bioconjug. Chem. 14, 232-238 (Pubitemid 36169037)
33. Wruss, J., Pollheimer, P. D., Meindl, I., Reichel, A., Schulze, K., Schöfberger, W., Piehler, J., Tampé, R., Blaas, D., and Gruber, H. J. (2009) Conformation of receptor adopted upon interaction with virus revealed by site-specific fluorescence quenchers and FRET Analysis. J. Am. Chem. Soc. 131, 5478-5482
34. Kamruzzahan, A. S., Ebner, A., Wildling, L., Kienberger, F., Riener, C. K., Hahn, C. D., Pollheimer, P. D., Winklehner, P., Hölzl, M., Lackner, B., Schörkl, D. M., Hinterdorfer, P., and Gruber, H. J. (2006) Antibody linking to atomic force microscope tips via disulfide bond formation. Bioconjug. Chem. 17, 1473-1481 (Pubitemid 44851492)
35. Lin, J. T., Hahn, K. D., and Kinne, R. (1982) Synthesis of phlorizin derivatives and their inhibitory effect on the renal sodium/D-glucose cotransport system. Biochim. Biophys. Acta 693, 379-388 (Pubitemid 13144678)
36. Wildling, L. (2008) Biofunktionalisierung von Atomkraftmikroskopiespitzen mit einem breit anwendbaren, modularen Linkersystem. Ph.D. thesis. The Johannes Kepler University, Linz, Austria
37. Wildling, L. (2005) Biofunktionalisierung von Messspitzen für die Rastersondenmikroskopie. Diploma thesis. The Johannes Kepler University, Linz, Austria
38. Ebner, A., Hinterdorfer, P., and Gruber, H. J. (2007) Comparison of different aminofunctionalization strategies for attachment of single antibodies to AFM cantilevers. Ultramicroscopy 107, 922-927 (Pubitemid 47095101)
39. Riener, C. K., Stroh, C. M., Ebner, A., Klampfl, C., Hall, A. A., Romanin, C., Lyubchenko, Y. L., Hinterdorfer, P., and Gruber, H. J. (2003) Simple test system for single molecule recognition force microscopy. Anal. Chim. Acta 479, 59-75 (Pubitemid 36173935)
40. Strunz, T., Oroszlan, K., Schäfer, R., and Güntherodt, H. J. (1999) Dynamic force spectroscopy of single DNA molecules. Proc. Natl. Acad. Sci. U.S.A. 96, 11277-11282 (Pubitemid 29487371)
41. +/D-glucose cotransporter (SGLT1) in a stably transfected Chinese hamster ovary cell line. Biochim. Biophys. Acta 1373, 309-320
42. Butt, H. J., and Jaschke, M. (1995) Calculation of thermal noise in atomic force microscopy. Nanotechnology 6, 1-7
43. Hutter, J. L., and Bechhoefer, J. (1993) Calibration of atomic-force microscope tips. Rev. Sci. Instrum. 64, 1868-1873
44. Baumgartner, W., Hinterdorfer, P., and Schindler, H. (2000) Data analysis of interaction forces measured with the atomic force microscope. Ultramicroscopy 82, 85-95 (Pubitemid 30070088)
45. Evans, E., and Ritchie, K. (1999) Strength of a weak bond connecting flexible polymer chains. Biophys. J. 76, 2439-2447 (Pubitemid 29264606)
46. Bell, G. I. (1978) Models for the specific adhesion of cells to cells. Science 200, 618-627
47. Evans, E., and Ritchie, K. (1997) Dynamic strength of molecular adhesion bonds. Biophys. J. 72, 1541-1555 (Pubitemid 27133095)
48. Wielert-Badt, S., Hinterdorfer, P., Gruber, H. J., Lin, J. T., Badt, D., Wimmer, B., Schindler, H., and Kinne, R. K. (2002) Single molecule recognition of protein binding epitopes in brush border membranes by force microscopy. Biophys. J. 82, 2767-2774 (Pubitemid 34441313)
49. Wielert-Badt, S., Lin, J. T., Lorenz, M., Fritz, S., and Kinne, R. K. (2000) Probing the conformation of the sugar transport inhibitor phlorizin by 2D-NMR, molecular dynamics studies, and pharmacophore analysis. J. Med. Chem. 43, 1692-1698 (Pubitemid 30305002)
50. Panayotova-Heiermann, M., Loo, D. D., Lostao, M. P., and Wright, E. M. (1994) Sodium/D-glucose cotransporter charge movements involve polar residues. J. Biol. Chem. 269, 21016-21020
51. +/glucose cotransporter. J. Biol. Chem. 272, 20324-20327
52. +/glucose cotransporter (SGLT1) expressed in E. coli. FEBS Lett. 459, 386-390
53. +/glucose cotransporters is determined by the carboxyl-terminal half of the protein. J. Biol. Chem. 271, 10029-10034
54. Da Cruz, M. E., Kinne, R., and Lin, J. T. (1983) Temperature dependence of D-glucose transport in reconstituted liposomes. Biochim. Biophys. Acta 732, 691-698
55. Zaccai, G. (2000) How soft is a protein?Aprotein dynamics force constant measured by neutron scattering. Science 288, 1604-1607
56. Nestorovich, E. M., Karginov, V. A., Berezhkovskii, A. M., Parsegian, V. A., and Bezrukov, S. M. (2012) Kinetics and thermodynamics of binding reactions as exemplified by anthrax toxin channel blockage with a cationic cyclodextrin derivative. Proc. Natl. Acad. Sci. U.S.A. 109, 18453-18458
57. Tyagi, N. K., Puntheeranurak, T., Raja, M., Kumar, A., Wimmer, B., Neundlinger, I., Gruber, H., Hinterdorfer, P., and Kinne, R. K. (2011) A biophysical glance at the outer surface of the membrane transporter SGLT1. Biochim. Biophys. Acta 1808, 1-18
58. Puntheeranurak, T., Kinne, R. K., Gruber, H. J., and Hinterdorfer, P. (2008) Single-molecule AFM studies of substrate transport by using the sodiumglucose cotransporter SGLT1. J. Korean Phys. Soc. 52, 1336-1340
59. + gradient the sugar transport. J. Membr. Biol. 42, 81-98
60. Hirayama, B. A., Loo, D. D., Díez-Sampedro, A., Leung, D. W., Meinild, A. K., Lai-Bing, M., Turk, E., and Wright, E. M. (2007) Sodium-dependent reorganization of the sugar-binding site of SGLT1. Biochemistry 46, 13391-13406 (Pubitemid 350136378)
61. Restrepo, D., and Kimmich, G. A. (1986) Phlorizin binding to isolated enterocytes: membrane potential and sodium dependence. J. Membr. Biol. 89, 269-280 (Pubitemid 16163300)
62. Kienberger, F., Pastushenko, V. P., Kada, G., Gruber, H. J., Riener, C., Schindler, H., and Hinterdorfer, P. (2000) Static and dynamical properties of single poly(ethylene glycol) molecules investigated by force spectroscopy. Single Molecules 1, 123-128
63. Maitra, A., and Arya, G. (2011) Influence of pulling handles and device stiffness in single-molecule force spectroscopy. Phys. Chem. Chem. Phys. 13, 1836-1842
64. Novakova, R., Homerova, D., Kinne, R. K., Kinne-Saffran, E., and Lin, J. T. (2001) Identification of a region critically involved in the interaction of phlorizin with the rabbit sodium-D-glucose cotransporter SGLT1. J. Membr. Biol. 184, 55-60 (Pubitemid 33016171)
65. Raja, M. M., and Kinne, R. K. (2005) Interaction of C-terminal loop 13 of sodium-glucose cotransporter SGLT1 with lipid bilayers. Biochemistry 44, 9123-9129 (Pubitemid 40943227)