Comprehensive Notes on the Nucleus, Nuclear Transport, and Chromatin

Nuclear Pore Complexes and Nucleo-Cytoplasmic Transport

  • Nuclear pore complexes (NPCs) perforate the nuclear envelope (NE) to mediate bi-directional, controlled exchange of molecules between the cytoplasm and the nucleus.

    • Proteins are imported into the nucleus.

    • Proteins, RNAs, and RNPs are exported out.

  • NPCs anchor chromatin and are involved in RNA metabolism (e.g., splicing).

  • Nucleoporins are located on the kinetochore during mitosis.

  • NPCs are large multimeric protein complexes.

    • Up to 500 proteins.

    • Up to 125 MDa in size.

  • There are approximately 3000-4000 NPCs in each nucleus, depending on cell type and cell cycle stage.

  • NPC protein components are called nucleoporins (Nups).

    • Approximately 30 different types, highly conserved in eukaryotes.

    • Multiple copies of each nucleoporin.

  • Nup subcomplexes are present.

    • Cytoplasmic ring with cytosolic fibrils on the cytoplasmic face.

    • Nuclear basket on the nuclear side; the main Nup is Tpr.

  • Membrane Nups (GP210, NDC1, Poms) anchor the NPC into the membrane.

  • Scaffold Nups bend the membrane and stabilize membrane deformation, allowing them to slide against each other for flexibility (e.g., Nup145/46).

  • Channel/central pore Nups contain repeat FG (phenylalanine, glycine) sequences, which fill the pore, restricting the size of molecules that can pass through (FG barrier).

  • NPCs have a huge transport capacity, approximately 1000 molecules/sec/NPC in both directions simultaneously.

    • Molecules require regulated import and/or export, some up to 200 KDa.

    • The pore diameter is approximately 40 nm.

  • Key parts of nucleo-cytoplasmic transport include:

    • Nuclear localization signals (NLS) and nuclear export signals (NES).

    • Transport proteins/karyopherins (importins and exportins).

    • The Ran cycle determines directionality.

Import of Proteins

  • Various nuclear localization signals (NLS) are rich in lysine and basic amino acid residues (e.g., arginine).

    • Classical NLS:

      • Monopartite (PKKKRKV in NLS of SV40 virus T-antigen from polyomavirus).

      • Bipartite NLS (KR[PAATKKAGQA]KKKK is NLS of nucleoplasmin).

    • Non-classical NLS.

  • NLS forms a binding domain for importin (a type of transport protein/karyopherin).

  • Once cargo is bound, importins traverse the pore by interacting with FG repeats in the pore.

  • In the nucleoplasm, RanGTP binds the complex, cargo dissociates, and importins+RanGTP are shuttled back outside.

  • Import adaptor protein = importin-α, which binds to classical NLS; then importin-β binds, forming a trimeric import complex.

  • Importin-β = transport protein (karyopherin).

  • Non-classical NLS binds importin-β directly.

Export of Proteins and RNAs

  • Variety of nuclear export signals on proteins and RNAs, which bind to exportins (karyopherin).

  • Exportins also interact with FG repeats; the export complex dissociates in the cytoplasm, and exportins are shuttled back in.

  • Regulation is by Ran GTPase.

  • The export complex consists of a cargo protein, exportin, and Ran-GTP.

  • Exportins and importins are related.

  • tRNAs and snRNAs are exported like proteins, using exportins and RanGTPase, and have specific karyopherins.

    • tRNAs use exportin-t.

    • snRNAs use Crm1.

  • Ribosomal subunits are also facilitated by RanGTPase and karyopherin-like proteins.

  • mRNA is exported as messenger ribonucleoprotein (mRNP), including mRNA processing enzymes (over 100).

    • Export uses Nxf1-Nxt dimers, not related to karyopherins.

    • Uses ATP to drive export.

    • The nuclear basket and cytosolic fibrils are involved.

The Ran Cycle

  • Ran is a monomeric GTPase regulated by RanGAP (GTPase activating protein) and RanGEF (Guanine exchange factor).

  • In the cytoplasm, there is a large concentration of Ran-GDP; cytoplasmic RanGAP is anchored to the NPC.

  • In the nucleoplasm, there is a large concentration of Ran-GTP; nucleoplasmic RanGEF is bound to chromatin.

  • Ran-GDP is imported again.

  • The Ran cycle drives transport through the pore and determines directionality.

  • Only RanGTP can bind to the transport receptor.

  • RanGTP binding to the import complex causes dissociation of the complex.

  • RanGTP binding to exportin promotes cargo binding and export of the export complex.

  • In the cytoplasm, the export complex dissociates because of RanGTP hydrolysis.

  • Ran-GDP is imported again.

  • Transport through the NPC is controlled by signaling to allow access to the transport machinery.

    • For example, NLS is not accessible in a protein before a signal; a transcription factor is tethered to the cytoskeleton or organelle away from the NPC and released upon a signal.

Summary of NPCs and Nucleo-Cytoplasmic Transport

  • NPCs are large complexes consisting of nucleoporins arranged into subcomplexes.

  • NPCs facilitate the import and export of proteins, RNAs, and RNPs.

  • Import and export are regulated by NLS/NES, karyopherins, and the Ran cycle (except mRNPs).

The Nuclear Envelope and Nuclear Periphery

  • The nuclear envelope (NE) is a barrier separating the nucleoplasm and chromatin from the cytoplasm, controlling nuclear processes and organization.

  • The NE consists of a double membrane: the outer nuclear membrane (ONM) and the inner nuclear membrane (INM).

  • The NE is continuous with the ER and has ribosomes, perforated by nuclear pore complexes (NPCs).

  • The NE is a permeable barrier.

  • Chromatin is in the nucleoplasm.

  • Nuclear structures include the nucleolus.

  • The NE forms invaginations called intranuclear strands.

  • The nucleus has a complex organization, including the peripheral nucleoskeleton (lamina), nuclear structures, and chromatin organization.

  • The nucleus is malleable and mobile.

  • Neutrophils migrate from the bloodstream.

  • Nuclear shape is dependent on cell type (e.g., Arabidopsis root hair and root tip).

  • Nuclei movement responds to stimuli, important in development, cellular function, and stress responses such as mycorrhizal symbiotic signaling.

  • The ONM and perinuclear space have ER functions due to continuity; however, the ONM also has specific proteins linked to INM proteins.

  • The INM and ONM are continuous but also have specific protein composition.

  • The perinuclear space exists between the ONM and INM.

  • Over 100 specific INM (and ONM) proteins exist, with some being tissue-specific NET (nuclear envelope transmembrane) proteins.

  • Most NETs are lamin-associated proteins (LAPs), which are metazoan-specific (animals); SUN and KASH proteins are the only ones conserved in animals, fungi, and plants.

  • Some INM proteins tether silenced chromatin to the NE, thus the NE is involved in chromatin organization and gene regulation.

  • Function and binding of INM proteins are regulated by phosphorylation.

  • The NE itself is involved in signaling by being a Ca^{2+} store, with Ca^{2+} pumps and ion channels in the INM and ONM.

  • In mitosis, the NE breaks down and re-assembles in telophase, with INM proteins and lamins responsible for this process.

  • One class of ONM-specific proteins is Klarsich/Anc1/Syne1 homology (KASH) proteins.

  • KASH proteins are anchored to the ONM by binding to INM proteins called Sad1/Unc84 (SUN) domain proteins.

  • KASH-SUN interactions form physical bridges across the NE, creating nucleo-cytoskeletal bridging complexes = Linker of Nucleoskeleton and Cytoskeleton (LINC) complex.

  • KASH proteins are poorly conserved, but SUN proteins are highly conserved in eukaryotes.

  • 3 SUN proteins anchor three KASH proteins.

  • KASH proteins bind to cytoskeletal components: microtubules, actin, and intermediate filaments.

  • SUN proteins bind to the nucleoskeleton - lamina.

Functions of LINC Complexes

  • Distance maintenance between INM and ONM.

  • Force transmission leading to mechanotransduction.

  • Movement and shape control of nuclei.

  • Movement of chromosomes.

  • Anchorage of RanGAP in plants.

The Lamina

  • The lamina is a nucleoskeletal structure underneath the INM.

  • Lamins in animals include lamin A/C and lamin B.

  • Lamin-like proteins CRWN/NMCP are found in plants.

  • They separately evolved but have similar structure and function.

  • Lamin-binding proteins are in the INM, keeping them in the INM; some lamins are nucleoplasmic.

  • Long coiled-coil domain for dimerization; short N-terminal head and longer C-terminal tail domain for interactions and filament formation.

  • Farnesylation and isoprenylation attach lamin A/C and lamin B to the INM; lamin A/C is cleaved, while lamin B remains attached.

  • Various INM lamin-binding proteins include SUN proteins and (Lap, Emerin, Man) LEM domain proteins, and soluble proteins like histones and transcription factors.

  • Lamins directly (Lamin associated domains [LAPs]) and indirectly associate with chromatin, influencing chromatin organization, gene expression, and DNA repair.

  • They maintain the structure of the nucleus by shaping it and bearing force, and anchoring NPCs.

  • Cell and tissue-specific expression and interactions occur.

  • Laminopathies are mutations in lamins and lamin-binding INM proteins, causing dystrophies and early-onset aging (progeria).

  • Lamin A has over 400 mutations, making it the most mutated gene known, leading to cancer and aging.

Summary of the Nuclear Envelope and Lamina

  • The NE consists of the INM and ONM, separating chromatin and involved in nuclear processes and nucleic acid metabolism.

  • Nucleo-cytoskeletal bridging complexes, composed of SUN and KASH proteins, transmit mechanical forces.

  • The lamina is a nucleoskeletal layer at the NE periphery, consisting of filamentous proteins, with structural functions and involvement in nuclear processes.

The Nucleolus and Other Nuclear Bodies

  • Sub-nuclear, non-membrane-bound organelles.

  • Distinct foci (light and electron microscope); dynamic hubs/reaction sites/modification sites containing core protein components specific to their functions.

  • Nuclear bodies are steady-state structures, kept together by protein-protein and protein-RNA interactions.

  • The nucleolus contains rDNA involved in the transcription of ribosomal RNA (rRNA) and assembly of ribosomal subunits.

  • It’s the accumulation site of various rRNAs, processing enzymes, and ribosomal proteins and particles.

  • Functions include:

    • RNA processing (precursor v mature RNA, including rRNA, snRNA, snoRNA and tRNA

    • Assembly of ribonucleoproteins (RNPs; e.g., signal recognition particle RNA, telomerase, splicing factor U6 snRNP).

  • Lamin B1 scaffolds the nucleolus externally in animals.

  • Cajal Bodies (CBs) are involved in the final assembly and modification of small nuclear and small nucleolar ribonucleoproteins (snRNPs and snoRNPs), and RNA recycling.

  • Nuclear speckles are storage and modification sites of mRNA splicing factors; e.g., snRNPs, kinases & phosphatase regulating splicing factors; hubs for gene activation/transcription and RNA maturation.

  • Polycomb bodies are hubs for gene repression/silencing and consist of Polycomb group (PcG) proteins.

Chromatin Structure, Function, and Epigenetics

  • DNA in a human cell is 2 meters long but needs to fit into a sphere of 6µm – packaging of DNA → organisation of DNA into chromatin.

  • Chromatin = DNA plus protein; proteins are either histones or non-histone chromosomal proteins.

  • Non-histone chromosomal proteins are involved in DNA repair, replication, transcription, and chromatin modifications.

  • Histones organize the basic structure of eukaryotic chromatin, forming the nucleosome.

  • The nucleosome contains 8 core histones: 2 of each H2A, H2B, H3, and H4; H3-H4 dimerize and then tetramerize, H2A-H2B dimerize, and come together as an octamer with 1.7 turns.

  • Negatively charged DNA backbone associates with positively charged histones - approx. 142 hydrogen bonds.

  • 1 nucleosome approx. every 200 nt (147nt on 1 nucleosome + linker DNA)

  • N-terminals tail for modifications

  • Histone variants

  • Chromatin organisation

  • Partial or complete removal and replacement of histone core; approx. ever 1-2h (e.g. histone variant).

  • Nucleosomes stacked on top of each other to compact DNA further into 30nm chromatin fiber.

  • Core histone tails and linker histone H1 involved in compacting.

  • Histone – DNA association dynamic – DNA unwraps approx. 4 times a second – important for access to DNA.

  • ATP-dependent chromatin remodeling complexes associate with histones and DNA of nucleosome and lead to temporary structural change → weaken DNA-histone binding.

  • Complexes at least 10 subunits; many different types.

  • Access to DNA; with chaperons replacement of histones.

  • Two types of chromatin:

    • Heterochromatin (highly condensed, repressed, gene-poor).

    • Euchromatin (less condensed, active, gene-rich).

  • Heterochromatin includes centromeres and telomeres; some of it located at the nuclear periphery; few genes or inactive genes.

  • Position effect – euchromatin next to hetero- chromatin can be silenced (translocation).

  • Some heterochromatin is present for the life of the cell, while some is only present for short periods depending on development and cell type.

  • Chromatin changes (heterochromatin ↔ euchromatin) occur through histone modifications, histone variants, Reader-Writer complexes, and barrier action; specialised chromatin structures.

  • Chromatin changes and structures can be inherited → epigenetics.

Histone Modifications

  • Common histone modifications are methylation, phosphorylation, and acetylation.

  • Modifications are commonly on arginine, serine, and lysine.

  • Specific enzymes add (writer enzymes) and remove modifications (eraser enzyme) (e.g., histone acetyl transferase and histone deacetylase).

  • Recruitment is dependent on transcription factors; the modification can stay in place and be inherited.

  • Modification either changes the DNA-histone interaction in the nucleosome or recruits proteins to alter chromatin structure or effect transcription.

  • For example, trimethylation of H3 lysine recruits H1 → further compaction of DNA and spread of heterochromatin.

  • Protein complexes recognizing specific markings are reader complexes.

  • Writer enzymes that add modifications can interact with reader complexes in the same protein complex, forming reader-writer complexes → spreading of the mark.

  • Multiple readers and writers exist for multiple markings; they can interact with each other.

  • ATP-dependent chromatin remodeling complexes are often associated.

  • They can either decondense (make DNA/genes accessible → gene activation or DNA repair) or condense (silencing, heterochromatin).

  • Eraser enzymes can also be part of reader complexes.

  • Barrier sequences stop the spread of heterochromatin markings.

  • Linked to barrier proteins; prevent access of reader- writer to nucleosome; can be linked to physical features (NPC, INM proteins, and lamins).

  • Barrier proteins can also be writer complexes that add strong markings opposing the spread or contain eraser complexes that delete signals for spread.

Examples of Writer and Eraser Enzymes
  • Writer enzymes:

    • Kinase

    • Histone Acetyltransferase

    • Histone methyltransferase

  • Eraser enzymes:

    • Phosphatase

    • Histone Deacetylase

    • Histone Demethylase

  • Histone variants and modifications act together, forming a highly diverse system for “marking” DNA → histone code.

  • Specific markings elicit specific responses, e.g., newly replicated DNA, damaged DNA, change in transcription.

  • Alternative splicing leads to histone variants; there are no variants for H4; variants are less well conserved and fewer are present than core histones; modifications on variants can be long-lasting.

  • Centromeres are an example of specialized chromatin structures.

  • They have a repeat sequence-rich DNA.

  • Histone H3 variant CENP-A is present.

  • In yeast, there is just one nucleosome and 125nt to make a centromere; in animals and plants, it is much larger (thousands of nts and nucleosomes).

  • A chromosome is one chromatin fiber; it is present in a highly condensed form during cell division and a relaxed state in interphase.

  • In interphase, chromosomes are folded into chromatin loops.

  • In interphase, chromosomes occupy chromosome territories but are dynamic.

  • Interphase chromatin folding into loops and coils is dynamic/changing.

  • Molecular mechanisms are unclear, but nuclear matrix proteins are involved that form a scaffold.

  • Loops decondense to allow access to DNA → transcription.

  • Heterochromatin is at the periphery, and active genes are more central.

  • Structural features of nuclei are involved in spatial chromosome organisation (NE, NPC, nucleolus), creating distinct biochemical environments by concentrating proteins/enzymes.

  • Repair factories and replication factories are organised by soluble lamins.

Summary of Chromatin

  • NE delineates the nucleus and is a permeable barrier; NPC mediate exchange of molecules.

  • Active transport requires RanGTPase, karyopherins, and NLS/NES.

  • The NE contains nucleo-cytoskeletal bridging complexes, involved in nuclei shape, movement, chromosome movement; the lamina is a structural feature associated with the NE.

  • Sub-nuclear organelles of various sizes, numbers, and functions are involved in RNA and DNA metabolism.

  • Nuclear structures (NE, NPC, lamina, nuclear organelles) are involved in chromatin organisation.

  • Chromatin = DNA+protein; histones package DNA into nucleosomes, histone code effects chromatin structure and gene expression.

  • Chromatin is packaged into chromosomes, organised into loops in interphase, occupies territories and is dynamic.

  • Histone code/chromatin structures can be inherited.

  • H3-H4 tetramere passed on to sister DNA helices in replication fork.

  • Markings are retained and spread by reader-writer complexes.