Structure and Function of the Nuclear Pore Complex

The nuclear pore complex (NPC) is a supramolecular protein structure in the nuclear envelope that creates a forty-nanometer channel connecting the cytoplasm and nucleoplasm of eukaryotic cells. Its main function is to regulate the vital flow of proteins and RNA between these two major compartments. Small metabolites diffuse freely across the NPC, but the flow of most proteins and RNA is selective and requires specific transit signals. The signals are recognized by mobile receptors termed karyopherins (also called importins, exportins and transportins), which interact with proteins of the NPC (nucleoporins; Nups) to shuttle cargo across the NPC. The process requires thermal energy to operate the NPC machinery, and chemical energy to impart directionality to the transport process via the Ran GTPase.

Research in my lab focuses on two fundamental aspects of nucleocytoplasmic transport:

I. The mechanics of karyopherin movement across the NPC

II. The structure of the NPC transport conduit

We are addressing these topics using a combination of cell biological, biochemical, biophysical, structural, genetic, and molecular modeling techniques in the model eukaryote S. cerevisiae.

I. Mechanics of karyopherin transport across the nuclear pore complex

Many karyopherins and their cargo have been identified but a mechanistic description of how they are mobilized within the NPC is lacking. Each NPC contains more than 200 potential docking sites for karyopherins (provided by nucleoporins that contain FG repeats), so movement of karyopherin-cargo complexes across the NPC is envisioned to be a stochastic process that operates via repeated association-dissociation reactions of karyopherins with FG nucleoporins. Currently, we are charting the path of transport used by karyopherins within the NPC through the identification of nucleoporins that physically contact them in situ within the NPC transport conduit. We are also addressing the kinetics of karyopherin transport across the NPC by characterizing the dynamics of association and dissociation between karyopherins, cargos and nucleoporins, and by identifying factors (KaRFs) that function to accelerate the dissociation rate of the most stable, long-lived intermediate complexes in the transport processes.

II. Architecture of the NPC transport conduit

Although the mechanics of karyopherin-mediated transport across the NPC are still poorly understood, it is clear that interactions between karyopherins and FG Nups are central to the translocation process. Thus, knowledge of the structural characteristics of FG nucleoporins may explain how karyopherin-cargo complexes of different shapes and sizes can translocate across the NPC while its permeability barrier remains intact. We are characterizing the structure of individual FG nucleoporins using biophysical, structural and molecular modeling techniques. We find that FG repeat regions of Nups are largely devoid of secondary structure and are mostly random coils 200-700 amino acids in length. Thus, the ~200 FG Nups present in each NPC likely form a flexible and highly amorphous meshwork of filaments at its center, which captures and engulfs karyopherin-cargo complexes of different shapes and sizes as they move across the NPC. We are currently testing the notion that FG Nups self-assemble into a meshwork of filaments held together by weak hydrophobic interactions between FG repeats.

References:

Intramolecular cohesion of coils mediated by phenylalanine--glycine motifs in the natively unfolded domain of a nucleoporin
  Krishnan VV, Lau EY, Yamada J, Denning DP, Patel SS, Colvin ME, Rexach MF.
  PLoS Comput Biol.  2008 Aug 8;  4(8):e1000145.
     PDF     Table  1  2  3     Figure  1  2  3  4  5
Discovering novel interactions at the nuclear pore complex using bead halo: a rapid method for detecting molecular interactions of high and low affinity at equilibrium.
  Patel SS, Rexach MF.
  Mol Cell Proteomics. 2008 Jan;7(1):121-31. Epub 2007 Sep 26.
     PDF   Supplemental Data
Natively Unfolded Nucleoporins Gate Protein Diffusion across the Nuclear Pore Complex
  Patel S.S., Belmont, B.J., Sante, J.M. and Rexach, M. (2007)
  Cell 129(1):83-96.
     PDF   Supplemental Data
Rapid evolution exposes the boundaries of domain structure and function in natively unfolded FG nucleoporins
  Denning D,. and Rexach, M. (2007)
  Mol Cell Proteomics 6(2):272-82.
     PDF   Supplemental Data
A sorting importin on Sec61
  Rexach, M. (2006)
  Nat Struct Mol Biol 13(6):476-8.
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Increased nuclear envelope permeability and Pep4p-dependent degradation of nucleoporins during hydrogen peroxide-induced cell death
  Mason, D.A., Shulga, N., Undavai, S., Ferrando-May, E., Rexach, M.F., Goldfarb. D.S. (2005)
  FEMS Yeast Res 5(12):1237-51. 
     PDF
Comprehensive analysis of a multidimensional liquid chromatography mass spectrometry dataset acquired on a quadrupole selecting, quadrupole collision cell, time-of-flight mass spectrometer: II. New developments in Protein Prospector allow for reliable and comprehensive automatic analysis of large datasets
  Chalkley, R.J., Baker, P.R., Huang, L., Hansen, K.C., Allen, N.P., Rexach, M., Burlingame, A.L. (2005)
  Mol Cell Proteomics 4(8):1194-204.
     PDF   Supplemental Data   More Supplemental Data
Comprehensive analysis of a multidimensional liquid chromatography mass spectrometry dataset acquired on a quadrupole selecting, quadrupole collision cell, time-of-flight mass spectrometer: I.How much of the data is theoretically interpretable by search engines?
  Chalkley, R.J., Baker, P.R., Hansen, K.C., Medzihradszky, K.F., Allen, N.P., Rexach, M., Burlingame, A.L. (2005)
 
Mol Cell Proteomics 4(8):1189-93.
     PDF   Supplemental Data   More Supplemental Data   Broad Institute Proteomics Mass Spectral Repository
Molecular basis for the rapid dissociation of nuclear localization signals from karyopherin alpha in the nucleoplasm.
  Gilchrist D,. and Rexach, M. (2003)
  Journal of Biological Chemistry 278 (51): 51937-49.
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A gradient of affinity for the karyopherin Kap95p along the yeast nuclear pore complex.
  Pyhtila, B., and Rexach, M.(2003)
  Journal of Biological Chemistry
278(43):42699-709.
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Disorder in the Nuclear Pore Complex: The FG repeat regions of nucleoporins are natively unfolded.
  Denning, D.P., Patel, S.S., Uversky, V., Fink, A.L., and Rexach, M. (2003)
  Proc Natl Acad Sci, USA 100, 2450-2455.
      PDF Supplemental Data
Deciphering networks of protein interactions at the nuclear pore complex.
   Allen, N.P., Patel, S.S., Huang, L., Chalkley, R.J., Burlingame, A., Lutzmann, M., Hurt, E.C., and Rexach, M. (2002)
   Molecular and Cellular Proteomics 1, 930-46.
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The identification of protein-protein interactions of the nuclear pore complex of Saccharomyces cerevisiae using high throughput matrix-assisted laser desorption ionization time-of-flight tandem mass spectrometry.
  Huang, L., Baldwin, M.A., Maltby, D.A., Medzihradszky, K.F., Baker, P.R., Allen, N., Rexach, M., Edmondson, R.D., Campbell, J., Juhasz, P.,
  Martin, S.A., Vestal, M.L., Burlingame, A.L. (2002)
  Mol Cell Proteomics 1(6):434-50.
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The S. cerevisiae nucleoporin Nup2p is a natively unfolded protein.
  Denning, D.P., Uversky, V., Patel, S.S., Fink, A.L, and Rexach, M. (2002)
  Journal of Biological Chemistry 277, 33447-55.
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Accelerating the rate of disassembly of karyopherin·cargo complexes.
  Gilchrist, D., Mykytka, B., and Rexach, M. (2002)
  Journal of Biological Chemistry 277, 18161-18172.
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The nucleoporin Nup60p functions as a Gsp1p-GTP sensitive tether for Nup2 at the nuclear pore complex.
  Denning, D., Mykytka, B., Allen, N.P.C., Huang, L., Burlingame, A., and Rexach, M. (2001)
  Journal of Cell Biology 154, 937-950.
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Proteomic analysis of nucleoporin-interacting proteins.
  Allen, N., Huang, L., Burlingame, A., and Rexach, M. (2001)
  Journal of Biological Chemistry 276, 29268-29274.
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Disassembly of RanGTP-karyopherin b complex: an intermediate in nuclear protein import.
  Floer, M., Blobel, G., and Rexach M. (1997).
  Journal of Biological Chemistry, 272, 19538-19546.
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Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins.
  Rexach, M. and Blobel, G. (1995).
  Cell 83, 683-692.
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Identification of a yeast karyopherin heterodimer that targets import substrate to mammalian nuclear pore complexes.
  Enenkel, C., Blobel, G., and Rexach, M. (1995).
 
Journal of Biological Chemistry 270, 16499-16502.
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