2q72 › Citations

Antidepressant binding site in a bacterial homologue of neurotransmitter transporters.

Singh SK, Yamashita A, Gouaux E
Nature 448 952-6 (2007)
Related entries: 2q6h, 2qb4, 2qei

Cited: 278 times
EuropePMC logo PMID:
doi logo

Abstract

Sodium-coupled transporters are ubiquitous pumps that harness pre-existing sodium gradients to catalyse the thermodynamically unfavourable uptake of essential nutrients, neurotransmitters and inorganic ions across the lipid bilayer. Dysfunction of these integral membrane proteins has been implicated in glucose/galactose malabsorption, congenital hypothyroidism, Bartter's syndrome, epilepsy, depression, autism and obsessive-compulsive disorder. Sodium-coupled transporters are blocked by a number of therapeutically important compounds, including diuretics, anticonvulsants and antidepressants, many of which have also become indispensable tools in biochemical experiments designed to probe antagonist binding sites and to elucidate transport mechanisms. Steady-state kinetic data have revealed that both competitive and noncompetitive modes of inhibition exist. Antagonist dissociation experiments on the serotonin transporter (SERT) have also unveiled the existence of a low-affinity allosteric site that slows the dissociation of inhibitors from a separate high-affinity site. Despite these strides, atomic-level insights into inhibitor action have remained elusive. Here we screen a panel of molecules for their ability to inhibit LeuT, a prokaryotic homologue of mammalian neurotransmitter sodium symporters, and show that the tricyclic antidepressant (TCA) clomipramine noncompetitively inhibits substrate uptake. Cocrystal structures show that clomipramine, along with two other TCAs, binds in an extracellular-facing vestibule about 11 A above the substrate and two sodium ions, apparently stabilizing the extracellular gate in a closed conformation. Off-rate assays establish that clomipramine reduces the rate at which leucine dissociates from LeuT and reinforce our contention that this TCA inhibits LeuT by slowing substrate release. Our results represent a molecular view into noncompetitive inhibition of a sodium-coupled transporter and define principles for the rational design of new inhibitors.

Reviews - 2q72 mentioned but not cited (2)

  1. Lieberman RL, Culver JA, Entzminger KC, Pai JC, Maynard JA. Methods 55 293-302 (2011)
  2. Zafar S, Jabeen I. Front Chem 6 397 (2018)

Articles - 2q72 mentioned but not cited (10)

  1. Andersen J, Taboureau O, Hansen KB, Olsen L, Egebjerg J, Str酶mgaard K, Kristensen AS. J Biol Chem 284 10276-10284 (2009)
  2. Sinning S, Musgaard M, Jensen M, Severinsen K, Celik L, Kolds酶 H, Meyer T, Bols M, Jensen HH, Schi酶tt B, Wiborg O. J Biol Chem 285 8363-8374 (2010)
  3. Sarker S, Weissensteiner R, Steiner I, Sitte HH, Ecker GF, Freissmuth M, Sucic S. Mol Pharmacol 78 1026-1035 (2010)
  4. Caplan DA, Subbotina JO, Noskov SY. Biophys J 95 4613-4621 (2008)
  5. Sun J, Aluvila S, Kotaria R, Mayor JA, Walters DE, Kaplan RS. Mol Cell Pharmacol 2 101-110 (2010)
  6. Campbell NG, Shekar A, Aguilar JI, Peng D, Navratna V, Yang D, Morley AN, Duran AM, Galli G, O'Grady B, Ramachandran R, Sutcliffe JS, Sitte HH, Erreger K, Meiler J, Stockner T, Bellan LM, Matthies HJG, Gouaux E, Mchaourab HS, Galli A. Proc Natl Acad Sci U S A 116 3853-3862 (2019)
  7. Andersen J, Ringsted KB, Bang-Andersen B, Str酶mgaard K, Kristensen AS, Kristensen AS. Sci Rep 5 15650 (2015)
  8. Gabrielsen M, Kurczab R, Ravna AW, Kufareva I, Abagyan R, Chilmonczyk Z, Bojarski AJ, Sylte I. Eur J Med Chem 47 24-37 (2012)
  9. Indarte M, Liu Y, Madura JD, Surratt CK. ACS Chem Neurosci 1 223-233 (2010)
  10. Jaro艅czyk M, Wo艂osewicz K, Gabrielsen M, Nowak G, Kufareva I, Mazurek AP, Ravna AW, Abagyan R, Bojarski AJ, Sylte I, Chilmonczyk Z. Eur J Med Chem 49 200-210 (2012)


Reviews citing this publication (60)

  1. Kristensen AS, Andersen J, J酶rgensen TN, S酶rensen L, Eriksen J, Loland CJ, Str酶mgaard K, Gether U. Pharmacol Rev 63 585-640 (2011)
  2. Lin L, Yee SW, Kim RB, Giacomini KM. Nat Rev Drug Discov 14 543-560 (2015)
  3. Murphy DL, Lesch KP. Nat Rev Neurosci 9 85-96 (2008)
  4. Hediger MA, Cl茅men莽on B, Burrier RE, Bruford EA. Mol Aspects Med 34 95-107 (2013)
  5. Kennedy PJ, Cryan JF, Dinan TG, Clarke G. Neuropharmacology 112 399-412 (2017)
  6. Krishnamurthy H, Piscitelli CL, Gouaux E. Nature 459 347-355 (2009)
  7. Forrest LR, Rudnick G. Physiology (Bethesda) 24 377-386 (2009)
  8. Shi Y. Annu Rev Biophys 42 51-72 (2013)
  9. Portulano C, Paroder-Belenitsky M, Carrasco N. Endocr Rev 35 106-149 (2014)
  10. Abramson J, Wright EM. Curr Opin Struct Biol 19 425-432 (2009)
  11. Pramod AB, Foster J, Carvelli L, Henry LK. Mol Aspects Med 34 197-219 (2013)
  12. Br枚er S, Gether U. Br J Pharmacol 167 256-278 (2012)
  13. Ziegler C, Bremer E, Kr盲mer R. Mol Microbiol 78 13-34 (2010)
  14. Boudker O, Verdon G. Trends Pharmacol Sci 31 418-426 (2010)
  15. Reith ME, Blough BE, Hong WC, Jones KT, Schmitt KC, Baumann MH, Partilla JS, Rothman RB, Katz JL. Drug Alcohol Depend 147 1-19 (2015)
  16. Penmatsa A, Gouaux E. J Physiol 592 863-869 (2014)
  17. Vinothkumar KR, Henderson R. Q Rev Biophys 43 65-158 (2010)
  18. Andersen J, Kristensen AS, Bang-Andersen B, Str酶mgaard K. Chem Commun (Camb) 3677-3692 (2009)
  19. Zhong H, Haddjeri N, S谩nchez C. Psychopharmacology (Berl) 219 1-13 (2012)
  20. Padan E. Biochim Biophys Acta 1837 1047-1062 (2014)
  21. Connor M, Vaughan CW, Vandenberg RJ. Br J Pharmacol 160 1857-1871 (2010)
  22. Cheng MH, Bahar I. Nat Struct Mol Biol 26 545-556 (2019)
  23. Boudko DY. J Insect Physiol 58 433-449 (2012)
  24. Kazmier K, Claxton DP, Mchaourab HS. Curr Opin Struct Biol 45 100-108 (2017)
  25. Focke PJ, Wang X, Larsson HP. Structure 21 694-705 (2013)
  26. Gouaux E. Philos Trans R Soc Lond B Biol Sci 364 149-154 (2009)
  27. Grouleff J, Ladefoged LK, Kolds酶 H, Schi酶tt B. Front Pharmacol 6 235 (2015)
  28. Nyola A, Karpowich NK, Zhen J, Marden J, Reith ME, Wang DN. Curr Opin Struct Biol 20 415-422 (2010)
  29. Manepalli S, Surratt CK, Madura JD, Nolan TL. AAPS J 14 820-831 (2012)
  30. Salatino-Oliveira A, Rohde LA, Hutz MH. Am J Med Genet B Neuropsychiatr Genet 177 211-231 (2018)
  31. Rives ML, Javitch JA, Wickenden AD. Biochem Pharmacol 135 1-11 (2017)
  32. Shaikh SA, Li J, Enkavi G, Wen PC, Huang Z, Tajkhorshid E. Biochemistry 52 569-587 (2013)
  33. Loland CJ. Biochim Biophys Acta 1850 500-510 (2015)
  34. Joseph D, Pidathala S, Mallela AK, Penmatsa A. Front Mol Biosci 6 80 (2019)
  35. Li F, Egea PF, Vecchio AJ, Asial I, Gupta M, Paulino J, Bajaj R, Dickinson MS, Ferguson-Miller S, Monk BC, Stroud RM. J Biol Chem 296 100557 (2021)
  36. Fairweather SJ, Shah N, Br缨er S. Adv Exp Med Biol 21 13-127 (2021)
  37. Sharma H, Santra S, Dutta A. Future Med Chem 7 2385-2406 (2015)
  38. Khelashvili G, Weinstein H. Biochim Biophys Acta 1848 1765-1774 (2015)
  39. Skonieczna-呕ydecka K, Jakubczyk K, Maciejewska-Markiewicz D, Janda K, Ka藕mierczak-Siedlecka K, Kaczmarczyk M, 艁oniewski I, Marlicz W. Nutrients 12 E3369 (2020)
  40. McLuskey K, Roszak AW, Zhu Y, Isaacs NW. Eur Biophys J 39 723-755 (2010)
  41. Kolds酶 H, Grouleff J, Schi酶tt B. Front Pharmacol 6 208 (2015)
  42. Aggarwal S, Mortensen OV. Curr Protoc Pharmacol 79 12.16.1-12.16.17 (2017)
  43. Skowron K, Kurnik-艁ucka M, Dada艅ski E, B臋tkowska-Korpa艂a B, Gil K. Nutrients 12 E2604 (2020)
  44. Wang CI, Lewis RJ. Biochem Pharmacol 79 1083-1091 (2010)
  45. Mortensen OV, Kortagere S. Front Pharmacol 6 223 (2015)
  46. Combs S, Kaufmann K, Field JR, Blakely RD, Meiler J. ACS Chem Neurosci 2 75-81 (2011)
  47. De Felice LJ. Pflugers Arch 468 503-511 (2016)
  48. Nolan TL, Geffert LM, Kolber BJ, Madura JD, Surratt CK. ACS Chem Neurosci 5 784-792 (2014)
  49. Iyalomhe O, Khantwal CM, Kang DC. J Membr Biol 248 641-650 (2015)
  50. Shiref H, Bergman S, Clivio S, Sahai MA. Methods 185 3-14 (2021)
  51. Bhatt M, Gauthier-Manuel L, Lazzarin E, Zerlotti R, Ziegler C, Bazzone A, Stockner T, Bossi E. Front Physiol 14 1145973 (2023)
  52. Kasarello K, Cudnoch-Jedrzejewska A, Czarzasta K. Front Microbiol 14 1118529 (2023)
  53. Frangos ZJ, Cantwell Chater RP, Vandenberg RJ. Front Mol Biosci 8 734427 (2021)
  54. Aggarwal S, Mortensen OV. Adv Neurobiol 30 101-129 (2023)
  55. Sauve S, Williamson J, Polasa A, Moradi M. Membranes (Basel) 13 462 (2023)
  56. Jaro艅czyk M, Walory J. Molecules 27 533 (2022)
  57. Nepal B, Das S, Reith ME, Kortagere S. Front Physiol 14 1150355 (2023)
  58. Stary D, Bajda M. Int J Mol Sci 24 3788 (2023)
  59. Yamashita A. Nihon Yakurigaku Zasshi 141 235-239 (2013)
  60. Zettl H, Schubert-Zsilavecz M, Siebert CD. Pharm Unserer Zeit 37 206-213 (2008)

Articles citing this publication (206)

  1. Penmatsa A, Wang KH, Gouaux E. Nature 503 85-90 (2013)
  2. Krishnamurthy H, Gouaux E. Nature 481 469-474 (2012)
  3. Singh SK, Piscitelli CL, Yamashita A, Gouaux E. Science 322 1655-1661 (2008)
  4. Coleman JA, Green EM, Gouaux E. Nature 532 334-339 (2016)
  5. Shi L, Quick M, Zhao Y, Weinstein H, Javitch JA. Mol Cell 30 667-677 (2008)
  6. Asano Y, Hiramoto T, Nishino R, Aiba Y, Kimura T, Yoshihara K, Koga Y, Sudo N. Am J Physiol Gastrointest Liver Physiol 303 G1288-95 (2012)
  7. Forrest LR, Zhang YW, Jacobs MT, Gesmonde J, Xie L, Honig BH, Rudnick G. Proc Natl Acad Sci U S A 105 10338-10343 (2008)
  8. Beuming T, Kniazeff J, Bergmann ML, Shi L, Gracia L, Raniszewska K, Newman AH, Javitch JA, Weinstein H, Gether U, Loland CJ. Nat Neurosci 11 780-789 (2008)
  9. Weyand S, Shimamura T, Yajima S, Suzuki S, Mirza O, Krusong K, Carpenter EP, Rutherford NG, Hadden JM, O'Reilly J, Ma P, Saidijam M, Patching SG, Hope RJ, Norbertczak HT, Roach PC, Iwata S, Henderson PJ, Cameron AD. Science 322 709-713 (2008)
  10. Wyant GA, Abu-Remaileh M, Wolfson RL, Chen WW, Freinkman E, Danai LV, Vander Heiden MG, Sabatini DM. Cell 171 642-654.e12 (2017)
  11. Zhao Y, Terry DS, Shi L, Quick M, Weinstein H, Blanchard SC, Javitch JA. Nature 474 109-113 (2011)
  12. Zhao Y, Terry D, Shi L, Weinstein H, Blanchard SC, Javitch JA. Nature 465 188-193 (2010)
  13. Zhou Z, Zhen J, Karpowich NK, Law CJ, Reith ME, Wang DN. Nat Struct Mol Biol 16 652-657 (2009)
  14. Quick M, Winther AM, Shi L, Nissen P, Weinstein H, Javitch JA. Proc Natl Acad Sci U S A 106 5563-5568 (2009)
  15. Kurian MA, Zhen J, Cheng SY, Li Y, Mordekar SR, Jardine P, Morgan NV, Meyer E, Tee L, Pasha S, Wassmer E, Heales SJ, Gissen P, Reith ME, Maher ER. J Clin Invest 119 1595-1603 (2009)
  16. Claxton DP, Quick M, Shi L, de Carvalho FD, Weinstein H, Javitch JA, McHaourab HS. Nat Struct Mol Biol 17 822-829 (2010)
  17. Gao X, Zhou L, Jiao X, Lu F, Yan C, Zeng X, Wang J, Shi Y. Nature 463 828-832 (2010)
  18. Alexander SP, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, Peters JA, Harmar AJ, CGTP Collaborators. Br J Pharmacol 170 1706-1796 (2013)
  19. Kniazeff J, Shi L, Loland CJ, Javitch JA, Weinstein H, Gether U. J Biol Chem 283 17691-17701 (2008)
  20. Piscitelli CL, Krishnamurthy H, Gouaux E. Nature 468 1129-1132 (2010)
  21. Penmatsa A, Wang KH, Gouaux E. Nat Struct Mol Biol 22 506-508 (2015)
  22. Wang H, Goehring A, Wang KH, Penmatsa A, Ressler R, Gouaux E. Nature 503 141-145 (2013)
  23. Shan J, Javitch JA, Shi L, Weinstein H. PLoS One 6 e16350 (2011)
  24. Ng J, Zhen J, Meyer E, Erreger K, Li Y, Kakar N, Ahmad J, Thiele H, Kubisch C, Rider NL, Morton DH, Strauss KA, Puffenberger EG, D'Agnano D, Anikster Y, Carducci C, Hyland K, Rotstein M, Leuzzi V, Borck G, Reith ME, Kurian MA. Brain 137 1107-1119 (2014)
  25. Spurny R, Ramerstorfer J, Price K, Brams M, Ernst M, Nury H, Verheij M, Legrand P, Bertrand D, Bertrand S, Dougherty DA, de Esch IJ, Corringer PJ, Sieghart W, Lummis SC, Ulens C. Proc Natl Acad Sci U S A 109 E3028-34 (2012)
  26. Bulling S, Schicker K, Zhang YW, Steinkellner T, Stockner T, Gruber CW, Boehm S, Freissmuth M, Rudnick G, Sitte HH, Sandtner W. J Biol Chem 287 18524-18534 (2012)
  27. Wang H, Elferich J, Gouaux E. Nat Struct Mol Biol 19 212-219 (2012)
  28. Quick M, Shi L, Zehnpfennig B, Weinstein H, Javitch JA. Nat Struct Mol Biol 19 207-211 (2012)
  29. Khelashvili G, Stanley N, Sahai MA, Medina J, LeVine MV, Shi L, De Fabritiis G, Weinstein H. ACS Chem Neurosci 6 1825-1837 (2015)
  30. Schmitt KC, Reith ME. PLoS One 6 e25790 (2011)
  31. Tavoulari S, Forrest LR, Rudnick G. J Neurosci 29 9635-9643 (2009)
  32. Andersen J, Olsen L, Hansen KB, Taboureau O, J酶rgensen FS, J酶rgensen AM, Bang-Andersen B, Egebjerg J, Str酶mgaard K, Kristensen AS. J Biol Chem 285 2051-2063 (2010)
  33. Celik L, Schi酶tt B, Tajkhorshid E. Biophys J 94 1600-1612 (2008)
  34. Schlessinger A, Matsson P, Shima JE, Pieper U, Yee SW, Kelly L, Apeltsin L, Stroud RM, Ferrin TE, Giacomini KM, Sali A. Protein Sci 19 412-428 (2010)
  35. Bai X, Moraes TF, Reithmeier RAF. Mol Membr Biol 34 1-32 (2017)
  36. Plenge P, Shi L, Beuming T, Te J, Newman AH, Weinstein H, Gether U, Loland CJ. J Biol Chem 287 39316-39326 (2012)
  37. Kantcheva AK, Quick M, Shi L, Winther AM, Stolzenberg S, Weinstein H, Javitch JA, Nissen P. Proc Natl Acad Sci U S A 110 8489-8494 (2013)
  38. Perc谩stegui EG, Ronson TK, Nitschke JR. Chem Rev 120 13480-13544 (2020)
  39. Li J, Shaikh SA, Enkavi G, Wen PC, Huang Z, Tajkhorshid E. Proc Natl Acad Sci U S A 110 7696-7701 (2013)
  40. LeVine MV, Weinstein H. PLoS Comput Biol 10 e1003603 (2014)
  41. Huang X, Gu HH, Zhan CG. J Phys Chem B 113 15057-15066 (2009)
  42. S酶rensen L, Andersen J, Thomsen M, Hansen SM, Zhao X, Sandelin A, Str酶mgaard K, Kristensen AS. J Biol Chem 287 43694-43707 (2012)
  43. Apparsundaram S, Stockdale DJ, Henningsen RA, Milla ME, Martin RS. J Pharmacol Exp Ther 327 982-990 (2008)
  44. Schmitt KC, Zhen J, Kharkar P, Mishra M, Chen N, Dutta AK, Reith ME. J Neurochem 107 928-940 (2008)
  45. Bisgaard H, Larsen MA, Mazier S, Beuming T, Newman AH, Weinstein H, Shi L, Loland CJ, Gether U. Neuropharmacology 60 182-190 (2011)
  46. Tavoulari S, Margheritis E, Nagarajan A, DeWitt DC, Zhang YW, Rosado E, Ravera S, Rhoades E, Forrest LR, Rudnick G. J Biol Chem 291 1456-1471 (2016)
  47. Andersen J, Stuhr-Hansen N, Zachariassen L, Toubro S, Hansen SM, Eildal JN, Bond AD, B酶ges酶 KP, Bang-Andersen B, Kristensen AS, Str酶mgaard K. Proc Natl Acad Sci U S A 108 12137-12142 (2011)
  48. Wildling L, Rankl C, Haselgr眉bler T, Gruber HJ, Holy M, Newman AH, Zou MF, Zhu R, Freissmuth M, Sitte HH, Hinterdorfer P. J Biol Chem 287 105-113 (2012)
  49. Piscitelli CL, Gouaux E. EMBO J 31 228-235 (2012)
  50. Shaikh SA, Tajkhorshid E. PLoS Comput Biol 6 e1000905 (2010)
  51. Andersen J, Stuhr-Hansen N, Zachariassen LG, Kolds酶 H, Schi酶tt B, Str酶mgaard K, Kristensen AS. Mol Pharmacol 85 703-714 (2014)
  52. de Carvalho FD, Quick M. J Biol Chem 286 131-137 (2011)
  53. Barelier S, Sterling T, O'Meara MJ, Shoichet BK. ACS Chem Biol 10 2772-2784 (2015)
  54. Kolds酶 H, Christiansen AB, Sinning S, Schi酶tt B. ACS Chem Neurosci 4 295-309 (2013)
  55. Paroder-Belenitsky M, Maestas MJ, Doh谩n O, Nicola JP, Reyna-Neyra A, Follenzi A, Dadachova E, Eskandari S, Amzel LM, Carrasco N. Proc Natl Acad Sci U S A 108 17933-17938 (2011)
  56. Malinauskaite L, Said S, Sahin C, Grouleff J, Shahsavar A, Bjerregaard H, Noer P, Severinsen K, Boesen T, Schi酶tt B, Sinning S, Nissen P. Nat Commun 7 11673 (2016)
  57. Sudo N. Front Endocrinol (Lausanne) 10 504 (2019)
  58. M枚ller IR, Slivacka M, Nielsen AK, Rasmussen SGF, Gether U, Loland CJ, Rand KD. Nat Commun 10 1687 (2019)
  59. Kolds酶 H, Noer P, Grouleff J, Autzen HE, Sinning S, Schi酶tt B. PLoS Comput Biol 7 e1002246 (2011)
  60. Sandtner W, Stockner T, Hasenhuetl PS, Partilla JS, Seddik A, Zhang YW, Cao J, Holy M, Steinkellner T, Rudnick G, Baumann MH, Ecker GF, Newman AH, Sitte HH. Mol Pharmacol 89 165-175 (2016)
  61. Kolds酶 H, Autzen HE, Grouleff J, Schi酶tt B. PLoS One 8 e63635 (2013)
  62. Shahsavar A, Stohler P, Bourenkov G, Zimmermann I, Siegrist M, Guba W, Pinard E, Sinning S, Seeger MA, Schneider TR, Dawson RJP, Nissen P. Nature 591 677-681 (2021)
  63. Mondal S, Khelashvili G, Shi L, Weinstein H. Chem Phys Lipids 169 27-38 (2013)
  64. Zomot E, Gur M, Bahar I. J Biol Chem 290 544-555 (2015)
  65. Johnson ZL, Lee JH, Lee K, Lee M, Kwon DY, Hong J, Lee SY. Elife 3 e03604 (2014)
  66. Wang H, Gouaux E. EMBO Rep 13 861-866 (2012)
  67. Khelashvili G, Doktorova M, Sahai MA, Johner N, Shi L, Weinstein H. Proteins 83 952-969 (2015)
  68. Skovstrup S, Taboureau O, Br盲uner-Osborne H, J酶rgensen FS. ChemMedChem 5 986-1000 (2010)
  69. Yuan Y, Huang X, Midde NM, Quizon PM, Sun WL, Zhu J, Zhan CG. ACS Chem Neurosci 6 658-665 (2015)
  70. DeChancie J, Shrivastava IH, Bahar I. Mol Biosyst 7 832-842 (2011)
  71. Zhao C, Noskov SY. PLoS Comput Biol 9 e1003296 (2013)
  72. Solis E, Zdravkovic I, Tomlinson ID, Noskov SY, Rosenthal SJ, De Felice LJ. J Biol Chem 287 8852-8863 (2012)
  73. Lin FY, MacKerell AD. J Phys Chem B 121 6813-6821 (2017)
  74. V盲stermark 脜, Saier MH. Proteins 82 336-346 (2014)
  75. Perez C, Faust B, Mehdipour AR, Francesconi KA, Forrest LR, Ziegler C. Nat Commun 5 4231 (2014)
  76. Hilger D, Polyhach Y, Jung H, Jeschke G. Biophys J 96 217-225 (2009)
  77. Cheng Q, Shah N, Br枚er A, Fairweather S, Jiang Y, Schmoll D, Corry B, Br枚er S. Br J Pharmacol 174 468-482 (2017)
  78. Merkle PS, Gotfryd K, Cuendet MA, Leth-Espensen KZ, Gether U, Loland CJ, Rand KD. Sci Adv 4 eaar6179 (2018)
  79. Schmitt KC, Mamidyala S, Biswas S, Dutta AK, Reith ME. J Neurochem 112 1605-1618 (2010)
  80. Rannversson H, Andersen J, S酶rensen L, Bang-Andersen B, Park M, Huber T, Sakmar TP, Str酶mgaard K. Nat Commun 7 11261 (2016)
  81. Parnas ML, Gaffaney JD, Zou MF, Lever JR, Newman AH, Vaughan RA. Mol Pharmacol 73 1141-1150 (2008)
  82. Gedeon PC, Indarte M, Surratt CK, Madura JD. Proteins 78 797-811 (2010)
  83. Kortagere S, Fontana AC, Rose DR, Mortensen OV, Mortensen OV. Neuropharmacology 72 282-290 (2013)
  84. Tavoulari S, Rizwan AN, Forrest LR, Rudnick G. J Biol Chem 286 2834-2842 (2011)
  85. Field JR, Henry LK, Blakely RD. J Biol Chem 285 11270-11280 (2010)
  86. Noskov SY. Proteins 73 851-863 (2008)
  87. Billesb酶lle CB, Kr眉ger MB, Shi L, Quick M, Li Z, Stolzenberg S, Kniazeff J, Gotfryd K, Mortensen JS, Javitch JA, Weinstein H, Loland CJ, Gether U. J Biol Chem 290 26725-26738 (2015)
  88. Gabrielsen M, Kurczab R, Siwek A, Wolak M, Ravna AW, Kristiansen K, Kufareva I, Abagyan R, Nowak G, Chilmonczyk Z, Sylte I, Bojarski AJ. J Chem Inf Model 54 933-943 (2014)
  89. Liang YJ, Zhen J, Chen N, Reith ME. J Neurochem 109 981-994 (2009)
  90. Khelashvili G, LeVine MV, Shi L, Quick M, Javitch JA, Weinstein H. J Am Chem Soc 135 14266-14275 (2013)
  91. Zhong H, Hansen KB, Boyle NJ, Han K, Muske G, Huang X, Egebjerg J, S谩nchez C. Neurosci Lett 462 207-212 (2009)
  92. J酶rgensen AM, Topiol S. Chem Biol Drug Des 72 265-272 (2008)
  93. Gur M, Zomot E, Cheng MH, Bahar I. J Chem Phys 143 243134 (2015)
  94. Edington AR, McKinzie AA, Reynolds AJ, Kassiou M, Ryan RM, Vandenberg RJ. J Biol Chem 284 36424-36430 (2009)
  95. Thomas JR, Gedeon PC, Grant BJ, Madura JD. Biophys J 103 L1-3 (2012)
  96. Lin FY, MacKerell AD. J Chem Theory Comput 14 1083-1098 (2018)
  97. Hasenhuetl PS, Schicker K, Koenig X, Li Y, Sarker S, Stockner T, Sucic S, Sitte HH, Freissmuth M, Sandtner W. Mol Pharmacol 88 12-18 (2015)
  98. Davis BA, Nagarajan A, Forrest LR, Singh SK. Sci Rep 6 23789 (2016)
  99. Ravna AW, Sylte I, Dahl SG. J Mol Model 15 1155-1164 (2009)
  100. Lee J, Chen J, Brooks CL, Im W. J Magn Reson 193 68-76 (2008)
  101. Dahal RA, Pramod AB, Sharma B, Krout D, Foster JD, Cha JH, Cao J, Newman AH, Lever JR, Vaughan RA, Henry LK. J Biol Chem 289 29712-29727 (2014)
  102. Zheng G, Xue W, Wang P, Yang F, Li B, Li X, Li Y, Yao X, Zhu F. Sci Rep 6 26883 (2016)
  103. Tsuruda PR, Yung J, Martin WJ, Chang R, Mai N, Smith JA. J Pharmacol Toxicol Methods 61 192-204 (2010)
  104. Zhang P, Cyriac G, Kopajtic T, Zhao Y, Javitch JA, Katz JL, Newman AH. J Med Chem 53 6112-6121 (2010)
  105. Thompson AJ, Alqazzaz M, Ulens C, Lummis SC. Neuropharmacology 63 761-767 (2012)
  106. Carland JE, Mansfield RE, Ryan RM, Vandenberg RJ. Br J Pharmacol 168 891-902 (2013)
  107. Guptaroy B, Fraser R, Desai A, Zhang M, Gnegy ME. Mol Pharmacol 79 520-532 (2011)
  108. Zhang YW, Tavoulari S, Sinning S, Aleksandrova AA, Forrest LR, Rudnick G. Proc Natl Acad Sci U S A 115 E8854-E8862 (2018)
  109. Plenge P, Yang D, Salomon K, Laursen L, Kalenderoglou IE, Newman AH, Newman AH, Gouaux E, Coleman JA, Loland CJ. Nat Commun 12 5063 (2021)
  110. Plenge P, Abramyan AM, S酶rensen G, M酶rk A, Weikop P, Gether U, Bang-Andersen B, Shi L, Loland CJ. Nat Commun 11 1491 (2020)
  111. Abdul-Hussein S, Andr茅ll J, Tate CG. J Mol Biol 425 2198-2207 (2013)
  112. Bjerregaard H, Severinsen K, Said S, Wiborg O, Sinning S. J Biol Chem 290 7747-7755 (2015)
  113. Skovstrup S, David L, Taboureau O, J酶rgensen FS. PLoS One 7 e39360 (2012)
  114. Walline CC, Nichols DE, Carroll FI, Barker EL. J Pharmacol Exp Ther 325 791-800 (2008)
  115. Stolzenberg S, Li Z, Quick M, Malinauskaite L, Nissen P, Weinstein H, Javitch JA, Shi L. J Biol Chem 292 7372-7384 (2017)
  116. Gros Y, Schuldiner S. J Biol Chem 285 5076-5084 (2010)
  117. Manepalli S, Geffert LM, Surratt CK, Madura JD. J Chem Inf Model 51 2417-2426 (2011)
  118. Meinild AK, Loo DDF, Skovstrup S, Gether U, MacAulay N. J Biol Chem 284 16226-16235 (2009)
  119. Li Z, Lee AS, Bracher S, Jung H, Paz A, Kumar JP, Abramson J, Quick M, Shi L. J Biol Chem 290 127-141 (2015)
  120. Tao Z, Zhang YW, Agyiri A, Rudnick G. J Biol Chem 284 33807-33814 (2009)
  121. Ye R, Blakely RD. Neuroscience 197 28-36 (2011)
  122. Gabrielsen M, Ravna AW, Kristiansen K, Sylte I. J Mol Model 18 1073-1085 (2012)
  123. Navratna V, Tosh DK, Jacobson KA, Gouaux E. PLoS One 13 e0200085 (2018)
  124. Meinild AK, Forster IC. Am J Physiol Cell Physiol 302 C1661-75 (2012)
  125. Khelashvili G, Schmidt SG, Shi L, Javitch JA, Gether U, Loland CJ, Weinstein H. J Biol Chem 291 19786-19799 (2016)
  126. Merchant BA, Madura JD. J Mol Graph Model 38 1-12 (2012)
  127. Severinsen K, Sinning S, M眉ller HK, Wiborg O. J Neurochem 105 1794-1805 (2008)
  128. Zhu J, Yuan Y, Midde NM, Gomez AM, Sun WL, Quizon PM, Zhan CG. J Neurovirol 22 282-292 (2016)
  129. Ramond E, Gesbert G, Guerrera IC, Chhuon C, Dupuis M, Rigard M, Henry T, Barel M, Charbit A. Mol Cell Proteomics 14 870-881 (2015)
  130. Singla RK, Scotti L, Dubey AK. Curr Neuropharmacol 15 1100-1106 (2017)
  131. Naftalin RJ. J Membr Biol 234 75-112 (2010)
  132. Quick M, Abramyan AM, Wiriyasermkul P, Weinstein H, Shi L, Javitch JA. Proc Natl Acad Sci U S A 115 E7924-E7931 (2018)
  133. Wang CI, Shaikh NH, Ramu S, Lewis RJ. Mol Pharmacol 82 898-909 (2012)
  134. Hellsberg E, Ecker GF, Stary-Weinzinger A, Forrest LR. PLoS One 14 e0217377 (2019)
  135. Rudnick G. Mol Membr Biol 30 355-359 (2013)
  136. Hill ER, Huang X, Zhan CG, Ivy Carroll F, Gu HH. Neuropharmacology 61 112-120 (2011)
  137. Karpowich NK, Wang DN. Science 321 781-782 (2008)
  138. Gournas C, Evangelidis T, Athanasopoulos A, Mikros E, Sophianopoulou V. J Biol Chem 290 6141-6155 (2015)
  139. Sotomayor-Z谩rate R, Quiroz G, Araya KA, Abarca J, Ib谩帽ez MR, Montecinos A, Guajardo C, N煤帽ez G, Fierro A, Moya PR, Iturriaga-V谩squez P, G贸mez-Molina C, Gysling K, Reyes-Parada M. Basic Clin Pharmacol Toxicol 111 371-379 (2012)
  140. Dehnes Y, Shan J, Beuming T, Shi L, Weinstein H, Javitch JA. Neurochem Int 73 4-15 (2014)
  141. Banala AK, Zhang P, Plenge P, Cyriac G, Kopajtic T, Katz JL, Loland CJ, Newman AH. J Med Chem 56 9709-9724 (2013)
  142. Lin FY, MacKerell AD. Methods Mol Biol 2022 21-54 (2019)
  143. Martin RS, Henningsen RA, Suen A, Apparsundaram S, Leung B, Jia Z, Kondru RK, Milla ME. J Pharmacol Exp Ther 327 991-1000 (2008)
  144. Larsen MA, Plenge P, Andersen J, Eildal JN, Kristensen AS, B酶ges酶 KP, Gether U, Str酶mgaard K, Bang-Andersen B, Loland CJ. Br J Pharmacol 173 925-936 (2016)
  145. Hess M, H枚fner G, Wanner KT. ChemMedChem 6 1900-1908 (2011)
  146. Focht D, Neumann C, Lyons J, Eguskiza Bilbao A, Blunck R, Malinauskaite L, Schwarz IO, Javitch JA, Quick M, Nissen P. EMBO J 40 e105164 (2021)
  147. Singh SK, Pal A. Methods Enzymol 557 167-198 (2015)
  148. Nolan TL, Lapinsky DJ, Talbot JN, Indarte M, Liu Y, Manepalli S, Geffert LM, Amos ME, Taylor PN, Madura JD, Surratt CK. ACS Chem Neurosci 2 544-552 (2011)
  149. Green EM, Coleman JA, Gouaux E. PLoS One 10 e0145688 (2015)
  150. Reyes N, Tavoulari S. J Gen Physiol 138 467-471 (2011)
  151. Pattison LP, McIntosh S, Sexton T, Childers SR, Hemby SE. Synapse 68 437-444 (2014)
  152. Wein T, Petrera M, Allmendinger L, H枚fner G, Pabel J, Wanner KT. ChemMedChem 11 509-518 (2016)
  153. Erlendsson S, Gotfryd K, Larsen FH, Mortensen JS, Geiger MA, van Rossum BJ, Oschkinat H, Gether U, Teilum K, Loland CJ. Elife 6 e19314 (2017)
  154. Parvaiz N, Ahmad F, Yu W, MacKerell AD, Azam SS. PLoS One 16 e0244967 (2021)
  155. Anderson CM, Kidd PD, Eskandari S. Database (Oxford) 2010 baq028 (2010)
  156. Xu L, Chen LY. J Chem Inf Model 60 3958-3968 (2020)
  157. Motiwala Z, Aduri NG, Shaye H, Han GW, Lam JH, Katritch V, Cherezov V, Gati C. Nature 606 820-826 (2022)
  158. Aree T. Pharmaceuticals (Basel) 13 E278 (2020)
  159. Nielsen S, Pedersen CM, Hansen SG, Petersen MD, Sinning S, Wiborg O, Jensen HH, Bols M. Bioorg Med Chem 17 4900-4909 (2009)
  160. Gaffaney JD, Shetty M, Felts B, Pramod AB, Foster JD, Henry LK, Vaughan RA. Neurochem Int 73 16-26 (2014)
  161. Ma J, Lei HT, Reyes FE, Sanchez-Martinez S, Sarhan MF, Hattne J, Gonen T. Proc Natl Acad Sci U S A 116 2086-2090 (2019)
  162. G贸ral I, 艁膮tka K, Bajda M. Biomolecules 10 E102 (2020)
  163. Pall贸 A, Simon A, Bencsura A, H茅ja L, Kardos J. Biochem Biophys Res Commun 385 210-214 (2009)
  164. Jaro艅czyk M, Chilmonczyk Z, Mazurek AP, Nowak G, Ravna AW, Kristiansen K, Sylte I. Bioorg Med Chem 16 9283-9294 (2008)
  165. Wenge B, B枚nisch H. Neurochem Res 38 1303-1314 (2013)
  166. N煤帽ez-Vivanco G, Fierro A, Moya P, Iturriaga-V谩squez P, Reyes-Parada M. PLoS One 13 e0200637 (2018)
  167. Kirmeier T, Gopalakrishnan R, Gormanns V, Werner AM, Cuboni S, Rudolf GC, H枚fner G, Wanner KT, Sieber SA, Schmidt U, Holsboer F, Rein T, Hausch F. PLoS One 11 e0148608 (2016)
  168. Zhou ZL, Liu HL, Wu JW, Tsao CW, Chen WH, Liu KT, Ho Y. Chem Biol Drug Des 82 705-717 (2013)
  169. Topiol S, Bang-Andersen B, Sanchez C, B酶ges酶 KP. Bioorg Med Chem Lett 26 5058-5064 (2016)
  170. Cherubino F, Miszner A, Renna MD, Sangaletti R, Giovannardi S, Bossi E. Cell Mol Life Sci 66 3797-3808 (2009)
  171. Rannversson H, Wilson P, Kristensen KB, Sinning S, Kristensen AS, Str酶mgaard K, Andersen J. J Biol Chem 290 14582-14594 (2015)
  172. Gerile, Sogawa C, Ohyama K, Masuko T, Kusama T, Morita K, Sogawa N, Kitayama S. Int J Mol Sci 13 2578-2589 (2012)
  173. Goodsell DS. Biochem Mol Biol Educ 37 204-210 (2009)
  174. Christensen H, Schj酶th-Eskesen C, Jensen M, Sinning S, Jensen HH. Chemistry 17 10618-10627 (2011)
  175. Erickson SL, Gandhi AR, Asafu-Adjei JK, Sampson AR, Miner L, Blakely RD, Sesack SR. Int J Neuropsychopharmacol 14 1219-1232 (2011)
  176. Yonar D, Pakta艧 DD, Horasan N, Strancar J, Sentjurc M, S眉nnet莽io臒lu MM. J Liposome Res 21 194-202 (2011)
  177. Aggarwal S, Cheng MH, Salvino JM, Bahar I, Mortensen OV. Biomedicines 9 634 (2021)
  178. Comment Lim HH, Miller C. Nat Struct Mol Biol 19 129-130 (2012)
  179. Wenge B, B枚nisch H. Naunyn Schmiedebergs Arch Pharmacol 377 255-265 (2008)
  180. Cuboni S, Hausch F. Angew Chem Int Ed Engl 53 5008-5009 (2014)
  181. Beckman ML, Pramod AB, Perley D, Henry LK. Neurochem Int 73 98-106 (2014)
  182. Pessoa-Mahana H, Gonz谩lez-Lira C, Fierro A, Zapata-Torres G, Pessoa-Mahana CD, Ortiz-Severin J, Iturriaga-V谩squez P, Reyes-Parada M, Silva-Matus P, Saitz-Barr铆a C, Araya-Maturana R. Bioorg Med Chem 21 7604-7611 (2013)
  183. N煤帽ez-Vivanco G, Vald茅s-Jim茅nez A, Besoa铆n F, Reyes-Parada M. J Cheminform 8 19 (2016)
  184. News Kanner BI. Nature 454 593-594 (2008)
  185. Thomas JR, Gedeon PC, Madura JD. Proteins 82 2289-2302 (2014)
  186. Park JE, Song C, Choi K, Sim T, Moon B, Roh EJ. Bioorg Med Chem Lett 23 5515-5518 (2013)
  187. Castagna M, Cinquetti R, Verri T, Vacca F, Giovanola M, Barca A, Romanazzi T, Roseti C, Galli A, Bossi E. Neurochem Res 47 111-126 (2022)
  188. News Amara SG. Nat Struct Mol Biol 14 792-794 (2007)
  189. Abramyan AM, Quick M, Xue C, Javitch JA, Shi L. J Chem Inf Model 58 1244-1252 (2018)
  190. Yuan Y, Zhu J, Zhan CG. ACS Chem Neurosci 9 1426-1431 (2018)
  191. Reith MEA, Jones KT, Zhen J, Topiol S. Bioorg Med Chem Lett 28 470-475 (2018)
  192. Asciutto EK, Gedeon PC, General IJ, Madura JD. J Phys Chem B 120 8361-8368 (2016)
  193. Khan JA, Sohail A, Jayaraman K, Sz枚ll艖si D, Sandtner W, Sitte HH, Stockner T. Neurochem Res 45 1387-1398 (2020)
  194. Topiol S, Bang-Andersen B, Sanchez C, Plenge P, Loland CJ, Juhl K, Larsen K, Bregnedal P, B酶ges酶 KP. Bioorg Med Chem Lett 27 470-478 (2017)
  195. Lynagh T, Khamu TS, Bryan-Lluka LJ. Naunyn Schmiedebergs Arch Pharmacol 387 95-107 (2014)
  196. Krout D, Pramod AB, Dahal RA, Tomlinson MJ, Sharma B, Foster JD, Zou MF, Boatang C, Newman AH, Lever JR, Vaughan RA, Henry LK. Biochem Pharmacol 142 204-215 (2017)
  197. Amador MHB, McDonald MD. J Exp Biol 221 jeb170928 (2018)
  198. Thompson AJ, Alqazzaz M, Price KL, Weston DA, Lummis SC. Biochemistry 53 6183-6188 (2014)
  199. Topiol S, Sabio M. Bioorg Med Chem Lett 26 484-494 (2016)
  200. Simmons KJ, Gotfryd K, Billesb酶lle CB, Loland CJ, Gether U, Fishwick CW, Johnson AP. Mol Membr Biol 30 184-194 (2013)
  201. Zhu C, Liang X, Chen X, Liang M, Zheng J, Wan B, Luo S. Int J Mol Sci 24 2561 (2023)
  202. Tomlinson MJ, Krout D, Pramod AB, Lever JR, Newman AH, Henry LK, Vaughan RA. Neurochem Int 123 34-45 (2019)
  203. Ahn H, Park K, Kim D, Chi SG, Choi KH, Han SJ, Song C. Biomedicines 11 2846 (2023)
  204. Zhu A, Huang J, Kong F, Tan J, Lei J, Yuan Y, Yan C. Nat Struct Mol Biol 30 1012-1022 (2023)
  205. Reith ME. Neurochem Res 38 1301-1302 (2013)
  206. Introductory Journal Article Kitayama S, Dohi T. Nihon Yakurigaku Zasshi 130 443 (2007)


Related citations provided by authors (1)

  1. . Yamashita A, Singh SK, Kawate T, Jin Y, Gouaux E Nature 437 215-223 (2005)

Quick links