Crescentin

Last updated
Crescentin
Identifiers
SymbolCrescentin
Pfam PF19220
InterPro IPR043652
Available protein structures:
Pfam   structures / ECOD  
PDB RCSB PDB; PDBe; PDBj
PDBsum structure summary
Intermediate filament-like cell shape determinant CreS
Identifiers
Organism Caulobacter vibrioides
SymbolCreS
Alt. symbolsParA
UniProt Q6IET3
Search for
Structures Swiss-model
Domains InterPro

Crescentin is a protein which is a bacterial relative of the intermediate filaments found in eukaryotic cells. Just as tubulins and actins, the other major cytoskeletal proteins, have prokaryotic homologs in, respectively, the FtsZ and MreB proteins, intermediate filaments are linked to the crescentin protein. Some of its homologs are erroneously labelled Chromosome segregation protein ParA. This protein family is found in Caulobacter and Methylobacterium .

Contents

Role in cell shape

Crescentin was discovered in 2009 by Christine Jacobs-Wagner in Caulobacter crescentus (now vibrioides), an aquatic bacterium which uses its crescent-shaped cells for enhanced motility. [1] The crescentin protein is located on the concave face of these cells and appears to be necessary for their shape, as mutants lacking the protein form rod-shaped cells. [2] To influence the shape of the Caulobacter cells, the helices of crescentin filaments associate with the cytoplasmic side of the cell membrane on one lateral side of the cell. This induces a curved cell shape in younger cells, which are shorter than the helical pitch of crescentin, but induces a spiral shape in older, longer cells. [3]

Protein structure

Like eukaryotic intermediate filaments, crescentin organizes into filaments and is present in a helical structure in the cell. Crescentin is necessary for both shapes of the Caulobacter prokaryote (vibroid/crescent-shape and helical shape, which it may adopt after a long stationary phase). The crescentin protein has 430 residues; its sequence mostly consists of a pattern of 7 repeated residues which form a coiled-coil structure. The DNA sequence of the protein has sections very similar to the eukaryotic keratin and lamin proteins, mostly involving the coiled-coil structure. Ausmees et al. (2003) proved that, like animal intermediate filament proteins, crescentin has a central rod made up of four coiled-coil segments. [4] Both intermediate filament and crescentin proteins have a primary sequence including four α-helical segments along with non-α-helical linker domains. An important difference between crescentin and animal intermediate filament proteins is that crescentin lacks certain consensus sequence elements at the ends of the rod domain which are conserved in animal lamin and keratin proteins. [5]

The protein has been divided into a few subdomains organized similarly to eukaryotic IF proteins. [6] Not every researcher is convinced that it is a homolog of intermediate filaments, suggesting instead that the similarity might have arisen via convergent evolution. [7] (Indeed, the Cryo-EM structure of CreS does not display the proposed eukaryotic-like interruption in the rod; see next paragraph.)

A number of Cryo-EM structures of crescentin were published in late 2023. The researchers used a nanobody that tags onto one specific part of the filament, so that it's easier to tell where each unit of the filament begins and ends. Two chains of the crescentin molecule pair together into a dimeric coil. Two coils come together side-by-side into a strand. Each strand is paired at its head and tail by another strand, so that it continues like a chain. Two chains of strands pair together side-by-side into a filament. Like eukaryotic intermediate filamenets, the CreS filament is octameric and lacks overall polarity. However, CreS does not show a linker domain in the middle but instead presents as a continuous rod. [8]

Assembly of filaments

Eukaryotic intermediate filament proteins assemble into filaments of 8–15 nm within the cell without the need for energy input, that is, no need for ATP or GTP. Ausmees et al. continued their crescentin research by testing whether the protein could assemble into filaments in this manner in vitro . They found that crescentin proteins were indeed able to form filaments about 10 nm wide, and that some of these filaments organized laterally into bundles, just as eukaryotic intermediate filaments do. [4] The similarity of crescentin protein to intermediate filament proteins suggests an evolutionary linkage between these two cytoskeletal proteins.

Like eukaryotic intermediate filaments, the filament built from crescentin is elastic. Individual proteins dissociate slowly, making the structure somewhat stiff and slow to remodel. Strain does not induce hardening of the structure, unlike eukaryotic IFs that do. [9]

Related Research Articles

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The cytoskeleton is a complex, dynamic network of interlinking protein filaments present in the cytoplasm of all cells, including those of bacteria and archaea. In eukaryotes, it extends from the cell nucleus to the cell membrane and is composed of similar proteins in the various organisms. It is composed of three main components: microfilaments, intermediate filaments, and microtubules, and these are all capable of rapid growth and or disassembly depending on the cell's requirements.

<span class="mw-page-title-main">Actin</span> Family of proteins

Actin is a family of globular multi-functional proteins that form microfilaments in the cytoskeleton, and the thin filaments in muscle fibrils. It is found in essentially all eukaryotic cells, where it may be present at a concentration of over 100 μM; its mass is roughly 42 kDa, with a diameter of 4 to 7 nm.

<span class="mw-page-title-main">Intermediate filament</span> Cytoskeletal structure

Intermediate filaments (IFs) are cytoskeletal structural components found in the cells of vertebrates, and many invertebrates. Homologues of the IF protein have been noted in an invertebrate, the cephalochordate Branchiostoma.

<span class="mw-page-title-main">MreB</span>

MreB is a protein found in bacteria that has been identified as a homologue of actin, as indicated by similarities in tertiary structure and conservation of active site peptide sequence. The conservation of protein structure suggests the common ancestry of the cytoskeletal elements formed by actin, found in eukaryotes, and MreB, found in prokaryotes. Indeed, recent studies have found that MreB proteins polymerize to form filaments that are similar to actin microfilaments. It has been shown to form multilayer sheets comprising diagonally interwoven filaments in the presence of ATP or GTP.

<span class="mw-page-title-main">FtsZ</span> Protein encoded by the ftsZ gene

FtsZ is a protein encoded by the ftsZ gene that assembles into a ring at the future site of bacterial cell division. FtsZ is a prokaryotic homologue of the eukaryotic protein tubulin. The initials FtsZ mean "Filamenting temperature-sensitive mutant Z." The hypothesis was that cell division mutants of E. coli would grow as filaments due to the inability of the daughter cells to separate from one another. FtsZ is found in almost all bacteria, many archaea, all chloroplasts and some mitochondria, where it is essential for cell division. FtsZ assembles the cytoskeletal scaffold of the Z ring that, along with additional proteins, constricts to divide the cell in two.

<span class="mw-page-title-main">Tubulin</span> Superfamily of proteins that make up microtubules

Tubulin in molecular biology can refer either to the tubulin protein superfamily of globular proteins, or one of the member proteins of that superfamily. α- and β-tubulins polymerize into microtubules, a major component of the eukaryotic cytoskeleton. It was discovered and named by Hideo Mōri in 1968. Microtubules function in many essential cellular processes, including mitosis. Tubulin-binding drugs kill cancerous cells by inhibiting microtubule dynamics, which are required for DNA segregation and therefore cell division.

<span class="mw-page-title-main">Nuclear lamina</span>

The nuclear lamina is a dense fibrillar network inside the nucleus of eukaryote cells. It is composed of intermediate filaments and membrane associated proteins. Besides providing mechanical support, the nuclear lamina regulates important cellular events such as DNA replication and cell division. Additionally, it participates in chromatin organization and it anchors the nuclear pore complexes embedded in the nuclear envelope.

<i>Caulobacter crescentus</i> Species of bacterium

Caulobacter crescentus is a Gram-negative, oligotrophic bacterium widely distributed in fresh water lakes and streams. The taxon is more properly known as Caulobacter vibrioides.

<span class="mw-page-title-main">Cytokeratin</span> Keratin protein

Cytokeratins are keratin proteins found in the intracytoplasmic cytoskeleton of epithelial tissue. They are an important component of intermediate filaments, which help cells resist mechanical stress. Expression of these cytokeratins within epithelial cells is largely specific to particular organs or tissues. Thus they are used clinically to identify the cell of origin of various human tumors.

<span class="mw-page-title-main">Vimentin</span> Type III intermediate filament protein

Vimentin is a structural protein that in humans is encoded by the VIM gene. Its name comes from the Latin vimentum which refers to an array of flexible rods.

<span class="mw-page-title-main">Peripherin</span> Protein-coding gene in the species Homo sapiens

Peripherin is a type III intermediate filament protein expressed mainly in neurons of the peripheral nervous system. It is also found in neurons of the central nervous system that have projections toward peripheral structures, such as spinal motor neurons. Its size, structure, and sequence/location of protein motifs is similar to other type III intermediate filament proteins such as desmin, vimentin and glial fibrillary acidic protein. Like these proteins, peripherin can self-assemble to form homopolymeric filamentous networks, but it can also heteropolymerize with neurofilaments in several neuronal types. This protein in humans is encoded by the PRPH gene. Peripherin is thought to play a role in neurite elongation during development and axonal regeneration after injury, but its exact function is unknown. It is also associated with some of the major neuropathologies that characterize amyotropic lateral sclerosis (ALS), but despite extensive research into how neurofilaments and peripherin contribute to ALS, their role in this disease is still unidentified.

Neurofilaments (NF) are classed as type IV intermediate filaments found in the cytoplasm of neurons. They are protein polymers measuring 10 nm in diameter and many micrometers in length. Together with microtubules (~25 nm) and microfilaments (7 nm), they form the neuronal cytoskeleton. They are believed to function primarily to provide structural support for axons and to regulate axon diameter, which influences nerve conduction velocity. The proteins that form neurofilaments are members of the intermediate filament protein family, which is divided into six types based on their gene organization and protein structure. Types I and II are the keratins which are expressed in epithelia. Type III contains the proteins vimentin, desmin, peripherin and glial fibrillary acidic protein (GFAP). Type IV consists of the neurofilament proteins NF-L, NF-M, NF-H and α-internexin. Type V consists of the nuclear lamins, and type VI consists of the protein nestin. The type IV intermediate filament genes all share two unique introns not found in other intermediate filament gene sequences, suggesting a common evolutionary origin from one primitive type IV gene.

<span class="mw-page-title-main">Protein filament</span> Long chain of protein monomers

In biology, a protein filament is a long chain of protein monomers, such as those found in hair, muscle, or in flagella. Protein filaments form together to make the cytoskeleton of the cell. They are often bundled together to provide support, strength, and rigidity to the cell. When the filaments are packed up together, they are able to form three different cellular parts. The three major classes of protein filaments that make up the cytoskeleton include: actin filaments, microtubules and intermediate filaments.

Recombinases are genetic recombination enzymes.

<span class="mw-page-title-main">Keratin 5</span>

Keratin 5, also known as KRT5, K5, or CK5, is a protein that is encoded in humans by the KRT5 gene. It dimerizes with keratin 14 and forms the intermediate filaments (IF) that make up the cytoskeleton of basal epithelial cells. This protein is involved in several diseases including epidermolysis bullosa simplex and breast and lung cancers.

<span class="mw-page-title-main">Prokaryotic cytoskeleton</span> Structural filaments in prokaryotes

The prokaryotic cytoskeleton is the collective name for all structural filaments in prokaryotes. It was once thought that prokaryotic cells did not possess cytoskeletons, but advances in visualization technology and structure determination led to the discovery of filaments in these cells in the early 1990s. Not only have analogues for all major cytoskeletal proteins in eukaryotes been found in prokaryotes, cytoskeletal proteins with no known eukaryotic homologues have also been discovered. Cytoskeletal elements play essential roles in cell division, protection, shape determination, and polarity determination in various prokaryotes.

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<span class="mw-page-title-main">IFFO1</span> Protein-coding gene in the species Homo sapiens

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Christine Jacobs-Wagner is a microbial molecular biologist. She is the Dennis Cunningham Professor of Biology and Microbiology and Immunology at Stanford University. Jacobs-Wagner's research has shown that bacterial cells have a great deal of substructure, including analogs of microfilaments, and that proteins are directed by regulatory processes to locate to specific places within the bacterial cell. She was elected to the National Academy of Sciences in 2015 and has received a number of scientific awards.

References

  1. Charbon G, Cabeen MT, Jacobs-Wagner C (May 2009). "Bacterial intermediate filaments: in vivo assembly, organization, and dynamics of crescentin". Genes & Development. 23 (9): 1131–44. doi:10.1101/gad.1795509. PMC   2682956 . PMID   19417107.
  2. Møller-Jensen J, Löwe J (February 2005). "Increasing complexity of the bacterial cytoskeleton". Current Opinion in Cell Biology. 17 (1): 75–81. doi:10.1016/j.ceb.2004.11.002. PMID   15661522.
  3. Margolin W (March 2004). "Bacterial shape: concave coiled coils curve caulobacter". Current Biology. 14 (6): R242-4. Bibcode:2004CBio...14.R242M. doi: 10.1016/j.cub.2004.02.057 . PMID   15043836. S2CID   37470451.
  4. 1 2 Ausmees N, Kuhn JR, Jacobs-Wagner C (December 2003). "The bacterial cytoskeleton: an intermediate filament-like function in cell shape". Cell. 115 (6): 705–13. doi: 10.1016/S0092-8674(03)00935-8 . PMID   14675535. S2CID   14459851.
  5. Herrmann H, Aebi U (2004). "Intermediate filaments: molecular structure, assembly mechanism, and integration into functionally distinct intracellular Scaffolds". Annual Review of Biochemistry. 73: 749–89. doi:10.1146/annurev.biochem.73.011303.073823. PMID   15189158.
  6. Cabeen, MT; Herrmann, H; Jacobs-Wagner, C (April 2011). "The domain organization of the bacterial intermediate filament-like protein crescentin is important for assembly and function". Cytoskeleton. 68 (4): 205–19. doi:10.1002/cm.20505. PMC   3087291 . PMID   21360832.
  7. Kollmar, M (29 May 2015). "Polyphyly of nuclear lamin genes indicates an early eukaryotic origin of the metazoan-type intermediate filament proteins". Scientific Reports. 5: 10652. Bibcode:2015NatSR...510652K. doi:10.1038/srep10652. PMC   4448529 . PMID   26024016.
  8. Liu, Y; van den Ent, F; Löwe, J (13 February 2024). "Filament structure and subcellular organization of the bacterial intermediate filament-like protein crescentin". Proceedings of the National Academy of Sciences of the United States of America. 121 (7): e2309984121. doi:10.1073/pnas.2309984121. PMC   10873595 . PMID   38324567.
  9. Esue O, Rupprecht L, Sun SX, Wirtz D (January 2010). "Dynamics of the bacterial intermediate filament crescentin in vitro and in vivo". PLOS ONE. 5 (1): e8855. Bibcode:2010PLoSO...5.8855E. doi: 10.1371/journal.pone.0008855 . PMC   2816638 . PMID   20140233.