Publications

1. Peer reviewed primary publications:

1) Ivica J, Kejzar N, Ho H, Stockwell I, Kuchtiak V, Scrutton AM, Nakagawa T#, Greger IH#. Proton-triggered rearrangement of the AMPA receptor N-terminal domains impacts receptor kinetics and synaptic localization. Nat Struct Mol Biol. 2024 Oct;31(10):1601-1613. doi: 10.1038/s41594-024-01369-5. Epub 2024 Aug 13. PMID: 39138332; PMCID: PMC11479944. #Corresponding authors.

2) Nakagawa T#, Wang XT, Miguez-Cabello FJ, Bowie D. The open gate of the AMPA receptor forms a Ca2+ binding site critical in regulating ion transport. Nat Struct Mol Biol. 2024 Apr;31(4):688-700. doi: 10.1038/s41594-024-01228-3. Epub 2024 Feb 26. PMID: 38409505; PMCID: PMC11536930. #Corresponding author.

•Highlighted in Greger IH. Regulating calcium flux through AMPA glutamate receptors. Cell Calcium. 2024 Nov;123:102934. doi: 10.1016/j.ceca.2024.102934. Epub 2024 Jul 30. PMID: 39096546.

3) Perozzo AM, Schwenk J, Kamalova A, Nakagawa T, Fakler B, Bowie D. GSG1L-containing AMPA receptor complexes are defined by their spatiotemporal expression, native interactome and allosteric sites. Nat Commun. 2023 Oct 26;14(1):6799. doi: 10.1038/s41467-023-42517-7. PMID: 37884493; PMCID: PMC10603098.

4) Singh PK, Cecchini G, Nakagawa T, Iverson TM. CryoEM structure of a post-assembly MS-ring reveals plasticity in stoichiometry and conformation. PLoS One. 2023 May 19;18(5):e0285343. doi: 10.1371/journal.pone.0285343. PMID: 37205674; PMCID: PMC10198558.

5) Zhang D, Lape R, Shaikh S, Kohegyi B, Watson JF, Cais O, Nakagawa T, Greger IH Modulatory mechanisms of TARPγ8-selective AMPA receptor therapeutics. Nature Commun. (2023) Mar 25;14(1):1659. doi: 10.1038/s41467-023-37259-5. PMID: 36966141; PMCID: PMC10039940.

6) Kamalova A, Futai K, Delpire E, and Nakagawa T. AMPA receptor auxiliary subunit GSG1L suppresses short-term facilitation in corticothalamic synapses and determines seizure susceptibility. Cell Rep. (2020) July 21;32(3):107921. PMID: 32697982. PMCID: PMC7425083.
Erratum: Cell Rep. 2021 Feb 16;34(7):108732. doi: 10.1016/j.celrep.2021.108732. Erratum for: Cell Rep. 2020 Jul 21;32(3):107921. PMID: 33596427; PMCID: PMC7982905.

7) Perfitt TL, Wang X, Dickerson MT, Stephenson JR, Nakagawa T, Jacobson DA, Colbran RJ. Neuronal L-Type Calcium Channel Signaling to the Nucleus Requires a Novel CaMKIIα-Shank3 Interaction. J Neurosci. (2020) Mar 4;40(10):2000-2014. Epub 2020 Feb 4. PMID: 32019829; PMCID: PMC7055140.

8) Kendall AK, Xie B, Xu P , Wang J, Burcham R, Frazier MN, Binshtein E, Wei H, Graham TR, Nakagawa T, and Jackson LP. Mammalian retromer is an adaptable scaffold for cargo sorting from endosomes. Structure (2020); 28(4):393-405.e4. PMID: 32027819 PMCID: PMC7145723

9) Azumaya CM, Linton EA, Risener CJ, Nakagawa T, Karakas E. Cryo-EM structure of human type-3 inositol triphosphate receptor reveals the presence of a self-binding peptide that acts as an antagonist. J Biol Chem. (2020) Feb 7;295(6):1743-1753. Epub 2020 Jan 8. PMID: 31915246; PMCID: PMC7008357.

10) Nakagawa T. Structures of the AMPA receptor in complex with its auxiliary subunit cornichon. Science. 2019 Dec 6;366(6470):1259-1263. doi: 10.1126/science.aay2783. PMID: 31806817; PMCID: PMC11533862.

• A perspective in the same issue highlighting the report:
Schwenk J, Fakler B. Folding unpredicted. Science. 2019 Dec 6;366(6470):1194-1195. doi: 10.1126/science.aaz8642. PubMed PMID: 31806799.
•The report was recommended in F1000Prime as being of special significance in its field by F1000 Faculty Member Johannes Hell (also recommended by Ryan Hibbs).

11) Sierra-Valdez F, Azumaya CM, Romero LO, Nakagawa T*, Cordero-Morales JF*. (*equal contribution)
 Structure-function analyses of the ion channel TRPC3 reveal that its cytoplasmic domain allosterically modulates channel gating. J. Biol. Chem. (2018); PubMed [journal] PMID: 30139744

12) Azumaya CM, Sierra-Valdez F, Cordero-Morales JF*, Nakagawa T*. (*equal contribution)
 Cryo-EM structure of the cytoplasmic domain of murine transient receptor potential cation channel subfamily C member 6 (TRPC6). J. Biol. Chem. (2018) May 11. PubMed PMID: 29752403. PMCID: PMC6028952.

13) Savas JN, Wang YZ, DeNardo LA, Martinez-Bartolome S, McClatchy DB, Hark TJ, Shanks NF, Cozzolino KA, Lavallée-Adam M, Smukowski SN, Park SK, Kelly JW, Koo EH, Nakagawa T, Masliah E, Ghosh A, Yates JR 3rd. Amyloid Accumulation Drives Proteome-wide Alterations in Mouse Models of Alzheimer’s Disease-like Pathology. Cell Reports. (2017); 21(9):2614-2627. NIHMSID: NIHMS919653 PubMed [journal] PMID: 29186695, PMCID: PMC5726791

14) Wang, X., Marks C.R., Perfitt, T.L., Nakagawa, T., Lee A., David A. Jacobson, D.A., Colbran, R.J. A novel mechanism for Ca2+ calmodulin-dependent protein kinase II targeting to L-type Ca2+ channels that initiates long-range signaling to the nucleus J. Biol. Chem. (2017) 292(42):17324-17336. PubMed [journal] PMID: 28916724, PMCID: PMC5655510

15) Hawken NM, Zaika EI, Nakagawa T. Engineering defined membrane-embedded elements of AMPA receptor induces opposing gating modulation by cornichon 3 and stargazin. The Journal of physiology. (2017); 595(20):6517-6539. PubMed [journal] PMID: 28815591, PMCID: PMC5638889

16) Stephenson, J.R., Wang, X., Perfitt, T.L., Parrish, W.P., Shonesy, B.C., Marks, C.R., Mortlock, D.P., Nakagawa, T., Sutcliffe, J.S., Colbran, R.J. A Novel Human CAMK2A Mutation Disrupts Dendritic Morphology and Synaptic Transmission, and Causes ASD-Related Behaviors. J. Neurosci. (2017); 37(8):2216-2233. PubMed PMID: 28130356, PMCID:PMC5338762

17) Azumaya, C.M., Days, E.L., Vinson, P.N., Stauffer, S., Sulikowski, G., Weaver, C.D., Nakagawa, T. Screening for AMPA receptor auxiliary subunit specific modulators. PLOS one. (2017); 12(3):e0174742. PubMed PMID: 28358902, PMCID: PMC5373622

18) Elegheert, J., Kakegawa, W., Clay, J., Shanks, N., Behiels, E., Matsuda, K., Kohda, K., Miura, E., Rossmann, M., Mitakidis, N., Motohashi, J., Chang, V., Siebold, C., Greger, I., Nakagawa, T., Yuzaki, M, Aricescu, A.R. (2016) Structural basis for integration of GluD receptors within synaptic organizer complexes. Science. 2016 Jul 15;353(6296):295-9 PMID: 27418511

19) Coles, C.H., Mitakidis, N., Zhang, P., Elegheert, J., Lu, W., Stoker, A.W., Nakagawa, T., Craig, A.M., Jones, E.Y., Aricescu, A.R. (2014) Structural basis for extracellular cis and trans RPTPσ signal competition in synaptogenesis. Nat Commun. Nov 11;5:5209. doi:10.1038/ncomms6209. PubMed PMID: 25385546; PubMed Central PMCID: PMC4239663.

20) Shanks NF, Cais O, Maruo T, Savas JN, Zaika EI, Azumaya CM, Yates JR 3rd, Greger I, Nakagawa T. Molecular dissection of the interaction between the AMPA receptor and cornichon homolog-3. J Neurosci. 2014 Sep 3;34(36):12104-20. doi: 10.1523/JNEUROSCI.0595-14.2014. PMID: 25186755; PMCID: PMC4152608.

21) Shanks, N. F., Savas, J. N., Maruo, T., Cais, O., Hirao, A., Oe, S., Ghosh, A., Noda, Y., Greger, I. H., Yates III, J. R., Nakagawa, T. (2012) Differences of AMPA and kainate receptor interactomes facilitate identification of AMPA receptor auxiliary subunit, GSG1L. Cell Reports 1: 590-598. PMID: 22813734 PMCID: PMC3401968.

22) Farina, A. N., Blain, K. Y., Maruo, T., Kwiatkowski, W., Choe, S., and Nakagawa, T. (2011) Separation of domain contacts is required for heteromeric assembly of functional NMDA receptors. J. Neurosci. 31: 3565-3579. PMID: 21389213 PMCID: PMC3063151.

23) Comoletti, D., Miller, M., Jeffries, C. M., Wilson, J., Demeler, B., Taylor, P., Trewhella, J., and Nakagawa, T. (2010) The macromolecular architecture of the extracellular domain of a-neurexin-1: domain organization, flexibility and insights into trans-synaptic association. Structure 18: 1044-1053. PMID: 20696403 PMCID: PMC2948785.

24) Shanks, N. F., Maruo, T., Farina, A. N., Ellisman, M. H., and Nakagawa, T. (2010) Contribution of the global subunit structure and stargazin on the maturation of AMPA receptors. J. Neurosci. 30: 2728-2740. PMID: 20164357 PMCID: PMC2842908.

25) Fischer, A., Garcia-Rodriguez, C., Geren, I., Lou, J., Marks, J. D., Nakagawa, T.*, and Montal, M.* (*equal contribution)
 (2008) Molecular architecture of Botulinum neurotoxin E revealed by single particle electron microscopy.
 J. Biol. Chem. 283: 3997-4003.

26) Cheng, D., Hoogenraad, C. C., Rush, J., Ramm, E., Schlager, M. A., Duong, D. M., Xu, P., Wijayawardana, S. R., Hanfelt, J., Nakagawa, T., Sheng, M., and Peng, J. (2006) Relative and absolute quantification of postsynaptic density proteome isolated from rat forebrain and cerebellum. Mol. Cell. Proteomics 5: 1158-1170.

27) Nakagawa, T., Cheng, Y., Sheng, M., and Walz, T. (2006) Three-dimensional structure of an AMPA receptor without associated stargazin/TARP proteins. Biol. Chem. 387: 179-187. PMID: 16497150.

28) Chen, X., Vinade, L., Leapman, R. D., Petersen, J.D., Nakagawa, T., Phillips, T. M., Sheng, M., and Rees, T. S. (2005) Mass of the post synaptic density and enumeration of three key molecules. Proc. Natl. Acad. Sci. USA 102: 11551-11556.

29) Nakagawa, T., Feliu-Mojer, M. I., Wulf, P., Lois, C., Sheng, M., and Hoogenraad, C. C. (2006) Generation of lentiviral transgenic rats expressing glutamate receptor binding protein 1 (GRIP1) in brain, spinal cord, and testis. J. Neurosci. Methods 152: 1-9.

30) Takao, K., Okamoto, K., Nakagawa, T., Neve, R. L., Nagai, T., Miyawaki, A., Hashikawa, T., Kobayashi, S., and Hayashi, Y. (2005) Visualization of synaptic Ca2+ /calmodulin-dependent protein kinase II activity in living neurons. J. Neurosci. 25: 3107-3112.

31) Nakagawa T, Cheng Y, Ramm E, Sheng M, Walz T. Structure and different conformational states of native AMPA receptor complexes. Nature. 2005 Feb 3;433(7025):545-9. doi: 10.1038/nature03328. PMID: 15690046.

• Highlighted in the News & Views:
Mayer, M. Some assembly required. Nat Struct Mol Biol 12, 208–209 (2005). https://doi.org/10.1038/nsmb0305-208

32) Nakagawa, T., Futai, K., Lashuel, H. A., Lo, I., Okamoto, K., Walz, T., Hayashi, Y., and Sheng, M. (2004) Quaternary structure, protein dynamics and synaptic function of SAP97 controlled by L27 domain interactions. Neuron 44: 453-467. PMID: 15504326.

33) Schulz, T. W., Nakagawa, T., Licznerski, P., Pawlak, V., Kolleker, A., Rozov, A., Kim, J., Dittgen, T., Köhr, G., Sheng, M., Seeburg, P. H., and Osten, P. (2004) Actin/-actinin-dependent transport of AMPA receptors in dendritic spines: role of the PDZ-LIM protein RIL. J. Neurosci. 24: 8584-8594.

34) Nakagawa, T., Engler, J. A., and Sheng, M. (2004) The dynamic turnover and functional roles of -actinin in dendritic spines. Neuropharmacology. 47: 734-745.

35) Passafaro, M., Nakagawa, T., Sala, C., and Sheng, M. (2003) Induction of dendritic spines by an extracellular domain of AMPA receptor subunit GluR2. Nature. 424: 677-681.

36) Nakajima, K., Takei, Y., Tanaka, Y., Nakagawa, T., Nakata, T., Noda, Y., Setou, M., and Hirokawa, N. (2002) Molecular motor KIF1C is not essential for mouse survival and motor-dependent retrograde Golgi apparatus-to-endoplasmic reticulum transport. Mol. Cell Biol. 22: 866-873.

37) Zhao, C., Takita, J., Tanaka, Y., Setou, M., Nakagawa, T., Takeda, S., Yang, H. W., Terada, S., Nakata, T., Takei, Y., Saito, M., Tsuji, S., Hayashi, Y., and Hirokawa, N. (2001) Charcot-Marie-Tooth disease type 2A caused by mutation in a microtubule motor KIF1B. Cell. 105: 587-597.

38) Nakagawa, T., Setou, M., Seog, D.–H., Ogasawara, K., Dohmae, N., Takio, K., and Hirokawa, N. (2000) A novel motor, KIF13A, transports mannose-6-phosphate receptor to plasma membrane through direct interaction with AP-1 complex. Cell. 103: 569-581.

39) Setou, M., Nakagawa, T., Seog. D.–H., and Hirokawa, N. (2000) Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science. 288: 1796-1802.

40) Nakagawa, T., Tanaka, Y., Matsuoka, E., Kondo, S., Okada, Y., Noda, Y., Kanai, Y., and Hirokawa, N. (1997) Identification and classification of sixteen new kinesin superfamily (KIF) proteins in mouse genome. Proc. Natl. Acad. Sci. USA. 94: 9654-9659.

41) Nakagawa, T., Chen, J., Zang, Z., Kanai, Y., and Hirokawa, N. (1995) Two distinct functions of the carboxyl-terminal tail domain of NF-M upon neurofilament assembly: cross-bridge formation and longitudinal elongation of filaments. J. Cell. Biol. 129: 411-429.

Other publications:

1) Hansen, KB., Wollmuth, L.P., Bowie, D., Furukawa, H., Menniti, F.S., Sobolevsky, A.I., Swanson, G.T., Swanger, S.A., Greger, I.H., Nakagawa, T., McBain, C.J., Jayaraman, V., Low, C-M., Dell’Acqua, M.L., Diamond, J., Perszyk, R.E., Camp, C.R., Yuan, H., and Traynelis, S.F. Structure, Function, and Pharmacology of Glutamate Receptor Ion Channels. Pharmacol Rev. (2021) Oct;73(4):298-487. doi: 10.1124/pharmrev.120.000131. PMID: 34753794; PMCID: PMC8626789.

2) Kamalova A, and Nakagawa T. AMPA receptor structure and auxiliary subunits [published online ahead of print, 2020 Jan 31]. J Physiol. (2020);10.1113/JP278701. PMID: 32004381.

3) Nakagawa, T., Hoogenraad, C. C. (2011) Lentiviral transgenesis. Methods Mol. Biol. 693: 117-142. In Transgenic Mouse Methods and Protocols. 2nd Edition. Chapter 8. (Editors Hofker, M., van Deursen, J.).

4) Nakagawa, T. (2010) The biochemistry, ultrastructure, and subunit assembly mechanism of AMPA receptors. Mol. Neurobiol. 42: 161-184.

5) Sheng, M., and Nakagawa, T. (2002) Neurobiology: glutamate receptors on the move. Nature 417: 601-602.

6) Nakagawa, T., and Sheng, M. (2000) A stargazer fortells the way to the synapse. Science 290: 2270-2271.