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The jelly roll or Swiss roll fold is a
protein fold A protein superfamily is the largest grouping (clade) of proteins for which common ancestry can be inferred (see homology). Usually this common ancestry is inferred from structural alignment and mechanistic similarity, even if no sequence similari ...
or
supersecondary structure A supersecondary structure is a compact three-dimensional protein structure of several adjacent elements of a secondary structure that is smaller than a protein domain or a subunit. Supersecondary structures can act as nucleations in the process ...
composed of eight
beta strand The beta sheet, (β-sheet) (also β-pleated sheet) is a common motif of the regular protein secondary structure. Beta sheets consist of beta strands (β-strands) connected laterally by at least two or three backbone hydrogen bonds, forming a gen ...
s arranged in two four-stranded sheets. The name of the structure was introduced by
Jane S. Richardson Jane Shelby Richardson (born January 25, 1941) is an American biophysicist best known for developing the Richardson diagram, or ribbon diagram, a method of representing the 3D structure of proteins. Ribbon diagrams have become a standard repr ...
in 1981, reflecting its resemblance to the jelly or
Swiss roll A Swiss roll, jelly roll (United States), roll cake, cream roll, roulade or Swiss log is a type of rolled sponge cake filled with whipped cream, jam, or icing. The origins of the term are unclear; in spite of the name "Swiss roll", the cake i ...
cake. The fold is an elaboration on the Greek key motif and is sometimes considered a form of
beta barrel In protein structures, a beta barrel is a beta sheet composed of tandem repeats that twists and coils to form a closed toroidal structure in which the first strand is bonded to the last strand (hydrogen bond). Beta-strands in many beta-barrels are ...
. It is very common in
viral protein A viral protein is both a component and a product of a virus. Viral proteins are grouped according to their functions, and groups of viral proteins include structural proteins, nonstructural proteins, regulatory proteins, and accessory proteins. Vi ...
s, particularly
viral capsid A capsid is the protein shell of a virus, enclosing its genetic material. It consists of several oligomeric (repeating) structural subunits made of protein called protomers. The observable 3-dimensional morphological subunits, which may or ma ...
proteins. Taken together, the jelly roll and Greek key structures comprise around 30% of the all-beta proteins annotated in the Structural Classification of Proteins (SCOP) database.


Structure

The basic jelly roll structure consists of eight
beta strand The beta sheet, (β-sheet) (also β-pleated sheet) is a common motif of the regular protein secondary structure. Beta sheets consist of beta strands (β-strands) connected laterally by at least two or three backbone hydrogen bonds, forming a gen ...
s arranged in two four-stranded antiparallel beta sheets which pack together across a
hydrophobic In chemistry, hydrophobicity is the physical property of a molecule that is seemingly repelled from a mass of water (known as a hydrophobe). In contrast, hydrophiles are attracted to water. Hydrophobic molecules tend to be nonpolar and, th ...
interface here citation... uniprot The strands are traditionally labeled B through I for the historical reason that the first solved structure, of a jelly roll capsid protein from the
tomato bushy stunt virus Tomato bushy stunt virus (TBSV) is a virus of the tombusvirus family. It was first reported in tomatoes in 1935 and primarily affects vegetable crops, though it is not generally considered an economically significant plant pathogen. Depending up ...
, had an additional strand A outside the fold's common core. The sheets are composed of strands BIDG and CHEF, folded such that strand B packs opposite strand C, I opposite H, etc.


Viral proteins

A large number of
virus A virus is a submicroscopic infectious agent that replicates only inside the living cells of an organism. Viruses infect all life forms, from animals and plants to microorganisms, including bacteria and archaea. Since Dmitri Ivanovsky's 1 ...
es build their exterior
capsid A capsid is the protein shell of a virus, enclosing its genetic material. It consists of several oligomeric (repeating) structural subunits made of protein called protomers. The observable 3-dimensional morphological subunits, which may or may ...
s from proteins containing either a single or a double jelly roll fold. This shared capsid architecture is thought to reflect ancient evolutionary relationships, possibly dating to before the
last universal common ancestor The last universal common ancestor (LUCA) is the most recent population from which all organisms now living on Earth share common descent—the most recent common ancestor of all current life on Earth. This includes all cellular organisms; t ...
(LUCA) of cellular life. Other viral lineages use evolutionarily unrelated proteins to build their enclosed capsids, which likely evolved independently at least twice and possibly many times, with links to proteins of cellular origin.


Single jelly roll capsid proteins

Single jelly roll capsid (JRC) proteins are found in at least sixteen distinct viral
families Family (from la, familia) is a group of people related either by consanguinity (by recognized birth) or affinity (by marriage or other relationship). The purpose of the family is to maintain the well-being of its members and of society. Ideall ...
, mostly with
icosahedral In geometry, an icosahedron ( or ) is a polyhedron with 20 faces. The name comes and . The plural can be either "icosahedra" () or "icosahedrons". There are infinitely many non- similar shapes of icosahedra, some of them being more symmetrica ...
capsid structures and including both
RNA virus An RNA virus is a virusother than a retrovirusthat has ribonucleic acid (RNA) as its genetic material. The nucleic acid is usually single-stranded RNA ( ssRNA) but it may be double-stranded (dsRNA). Notable human diseases caused by RNA viruses ...
es and
DNA virus A DNA virus is a virus that has a genome made of deoxyribonucleic acid (DNA) that is replicated by a DNA polymerase. They can be divided between those that have two strands of DNA in their genome, called double-stranded DNA (dsDNA) viruses, and ...
es. Many viruses with single jelly roll capsids are
positive-sense single-stranded RNA virus Positive-strand RNA viruses (+ssRNA viruses) are a group of related viruses that have positive-sense, single-stranded genomes made of ribonucleic acid. The positive-sense genome can act as messenger RNA (mRNA) and can be directly translated into ...
es. Two groups of
double-stranded DNA virus A DNA virus is a virus that has a genome made of deoxyribonucleic acid (DNA) that is replicated by a DNA polymerase. They can be divided between those that have two strands of DNA in their genome, called double-stranded DNA (dsDNA) viruses, and ...
es with single-JRC capsids are the ''
Papillomaviridae ''Papillomaviridae'' is a family of non- enveloped DNA viruses whose members are known as papillomaviruses. Several hundred species of papillomaviruses, traditionally referred to as "types", have been identified infecting all carefully inspected ...
'' and ''
Polyomaviridae ''Polyomaviridae'' is a family of viruses whose natural host (biology), hosts are primarily mammals and birds. As of 2020, there are six recognized genera and 117 species, five of which are unassigned to a genus. 14 species are known to infect hu ...
'', both of which have fairly small capsids; in these viruses, the architecture of the assembled capsid orients the axis of the jelly roll parallel or "horizontally" relative to the capsid surface. A large-scale analysis of viral capsid components suggested that the single horizontal jelly roll is the most common fold among capsid proteins, accounting for about 28% of known examples. Another group of viruses uses single jelly roll proteins in their capsids, but in the vertical rather than horizontal orientation. These viruses are evolutionarily related to the large group of double jelly-roll viruses known as the
PRD1 ''Tectiviridae'' is a family of viruses with 10 species in five genera. Bacteria serve as natural hosts. Tectiviruses have no head-tail structure, but are capable of producing tail-like tubes of ~ 60×10 nm upon adsorption or after chlorofo ...
-
adenovirus Adenoviruses (members of the family ''Adenoviridae'') are medium-sized (90–100 nm), nonenveloped (without an outer lipid bilayer) viruses with an icosahedral nucleocapsid containing a double-stranded DNA genome. Their name derives from the ...
viral lineage, with similar capsid architecture realized through assembly of two distinct single jelly-roll major capsid proteins expressed from distinct genes. These single vertical jelly-roll viruses comprise the taxon
Helvetiavirae ''Alphasphaerolipovirus'' is a genus of double stranded DNA viruses that infect haloarchaea. The genus contains four species. Taxonomy The genus contains the following species: * '' Haloarcula hispanica icosahedral virus 2'' * '' Haloarcula his ...
. Known viruses with vertical single jelly roll capsids infect
extremophilic An extremophile (from Latin ' meaning "extreme" and Greek ' () meaning "love") is an organism that is able to live (or in some cases thrive) in extreme environments, i.e. environments that make survival challenging such as due to extreme tempe ...
prokaryote A prokaryote () is a single-celled organism that lacks a nucleus and other membrane-bound organelles. The word ''prokaryote'' comes from the Greek πρό (, 'before') and κάρυον (, 'nut' or 'kernel').Campbell, N. "Biology:Concepts & Connec ...
s.


Double jelly roll proteins

Double jelly roll capsid proteins consist of two single jelly roll folds connected by a short linker region. They are found in both
double-stranded DNA virus A DNA virus is a virus that has a genome made of deoxyribonucleic acid (DNA) that is replicated by a DNA polymerase. They can be divided between those that have two strands of DNA in their genome, called double-stranded DNA (dsDNA) viruses, and ...
es and
single-stranded DNA viruses A DNA virus is a virus that has a genome made of deoxyribonucleic acid (DNA) that is replicated by a DNA polymerase. They can be divided between those that have two strands of DNA in their genome, called double-stranded DNA (dsDNA) viruses, and ...
of at least ten different viral families, including viruses that infect all
domains of life In Biology, biological Taxonomy (biology), taxonomy, a domain ( or ) (Latin: ''regio''), also dominion, superkingdom, realm, or empire, is the highest taxonomic rank of all organisms taken together. It was introduced in the three-domain system of ...
, and spanning a large capsid size range. In the double jelly roll capsid architecture, the jelly roll axis is oriented perpendicular or "vertically" relative to the capsid surface. Double jelly roll proteins are believed to have evolved from single jelly roll proteins by
gene duplication Gene duplication (or chromosomal duplication or gene amplification) is a major mechanism through which new genetic material is generated during molecular evolution. It can be defined as any duplication of a region of DNA that contains a gene. ...
. It is likely that vertical single jelly roll viruses represent a transitional form, and that the vertical and horizontal jelly roll capsid proteins have independent evolutionary origins from ancestral cellular proteins. The degree of structural similarity among double-jelly-roll virus capsids has led to the conclusion that these viruses likely have a common evolutionary origin despite their diversity in size and in host range; this has become known as the
PRD1 ''Tectiviridae'' is a family of viruses with 10 species in five genera. Bacteria serve as natural hosts. Tectiviruses have no head-tail structure, but are capable of producing tail-like tubes of ~ 60×10 nm upon adsorption or after chlorofo ...
-
adenovirus Adenoviruses (members of the family ''Adenoviridae'') are medium-sized (90–100 nm), nonenveloped (without an outer lipid bilayer) viruses with an icosahedral nucleocapsid containing a double-stranded DNA genome. Their name derives from the ...
lineage (
Bamfordvirae ''Bamfordvirae'' is a kingdom of viruses. This kingdom is recognized for its use of double jelly roll major capsid proteins. It was formerly known as the PRD1-adenovirus lineage. The kingdom is named after Dennis H. Bamford who first promoted ...
). Many members of this group have been identified through
metagenomics Metagenomics is the study of genetic material recovered directly from environmental or clinical samples by a method called sequencing. The broad field may also be referred to as environmental genomics, ecogenomics, community genomics or microb ...
and in some cases have few to no other viral genes in common. Although most members of this group have
icosahedral In geometry, an icosahedron ( or ) is a polyhedron with 20 faces. The name comes and . The plural can be either "icosahedra" () or "icosahedrons". There are infinitely many non- similar shapes of icosahedra, some of them being more symmetrica ...
capsid geometry, a few families such as the ''
Poxviridae ''Poxviridae'' is a family of double-stranded DNA viruses. Vertebrates and arthropods serve as natural hosts. There are currently 83 species in this family, divided among 22 genera, which are divided into two subfamilies. Diseases associated wit ...
'' and ''
Ascoviridae ''Ascoviridae'' is a family of double strand DNA viruses that infect primarily invertebrates, mainly noctuids and spodoptera species; it contains two genera, ''Ascovirus'', which contains three species, and ''Toursvirus'' with a single species ' ...
'' have oval or brick-shaped mature virions; poxviruses such as ''
Vaccinia ''Vaccinia virus'' (VACV or VV) is a large, complex, enveloped virus belonging to the poxvirus family. It has a linear, double-stranded DNA genome approximately 190 kbp in length, which encodes approximately 250 genes. The dimensions of the ...
'' undergo dramatic conformational changes mediated by highly derived double jelly roll proteins during maturation and likely derive from an icosahedral ancestor. Shared double-jelly-roll capsid proteins, along with other homologous proteins, have also been cited in support of the proposed order ''
Megavirales ''Nucleocytoviricota'' is a phylum of viruses. Members of the phylum are also known as the nucleocytoplasmic large DNA viruses (NCLDV), which serves as the basis of the name of the phylum with the suffix - for virus phylum. These viruses are refe ...
'' containing the
nucleocytoplasmic large DNA virus ''Nucleocytoviricota'' is a phylum of viruses. Members of the phylum are also known as the nucleocytoplasmic large DNA viruses (NCLDV), which serves as the basis of the name of the phylum with the suffix - for virus phylum. These viruses are refe ...
es (NCLDV). Initially, it was believed that double jelly roll proteins are unique to viruses, because they were not observed in cellular proteins. However, in 2022, comparison of protein structures revealed several families of bona fide cellular proteins with the double jelly roll fold


Non-capsid proteins

Single jelly rolls also occur in non-capsid viral proteins, including minor components of the assembled
virion A virus is a submicroscopic infectious agent that replicates only inside the living cells of an organism. Viruses infect all life forms, from animals and plants to microorganisms, including bacteria and archaea. Since Dmitri Ivanovsky's 1 ...
as well as non-virion proteins such as polyhedrin.


Cellular proteins

Both single and double jelly roll folds are found in proteins of cellular origin. One class of cellular proteins with single jelly roll fold is the
nucleoplasmin Nucleoplasmin, the first identified molecular chaperone is a thermostable acidic protein with a pentameric structure. The protein was first isolated from Xenopus species Functions The pentameric protein participates in various significant cellula ...
s, which serve as
molecular chaperone In molecular biology, molecular chaperones are proteins that assist the conformational folding or unfolding of large proteins or macromolecular protein complexes. There are a number of classes of molecular chaperones, all of which function to assi ...
proteins for
histone In biology, histones are highly basic proteins abundant in lysine and arginine residues that are found in eukaryotic cell nuclei. They act as spools around which DNA winds to create structural units called nucleosomes. Nucleosomes in turn are wr ...
assembly into
nucleosome A nucleosome is the basic structural unit of DNA packaging in eukaryotes. The structure of a nucleosome consists of a segment of DNA wound around eight histone proteins and resembles thread wrapped around a spool. The nucleosome is the fundamen ...
s. The
N-terminal The N-terminus (also known as the amino-terminus, NH2-terminus, N-terminal end or amine-terminus) is the start of a protein or polypeptide, referring to the free amine group (-NH2) located at the end of a polypeptide. Within a peptide, the ami ...
domain Domain may refer to: Mathematics *Domain of a function, the set of input values for which the (total) function is defined **Domain of definition of a partial function **Natural domain of a partial function **Domain of holomorphy of a function * Do ...
of nucleoplasmins possesses a single jelly roll fold and assembled into a pentamer. Similar structures have since been reported in additional groups of
chromatin Chromatin is a complex of DNA and protein found in eukaryotic cells. The primary function is to package long DNA molecules into more compact, denser structures. This prevents the strands from becoming tangled and also plays important roles in r ...
remodeling proteins. Jelly roll motifs with identical beta-sheet connectivity are also found in
tumor necrosis factor Tumor necrosis factor (TNF, cachexin, or cachectin; formerly known as tumor necrosis factor alpha or TNF-α) is an adipokine and a cytokine. TNF is a member of the TNF superfamily, which consists of various transmembrane proteins with a homolog ...
ligands and proteins from the bacterium ''
Yersinia pseudotuberculosis ''Yersinia pseudotuberculosis'' is a Gram-negative bacterium that causes Far East scarlet-like fever in humans, who occasionally get infected zoonotically, most often through the food-borne route. Animals are also infected by ''Y. pseudotuberc ...
'' that belong to a class of viral and bacterial proteins known as superantigens. More broadly, the members of the extremely diverse
cupin superfamily The cupin superfamily is a diverse superfamily of proteins named after its conserved barrel domain (''cupa'' being the Latin term for a small barrel). The superfamily includes a wide variety of enzymes as well as non-enzymatic seed storage p ...
are also often described as jelly rolls; though the common core of the cupin domain structure contains only six beta strands, many cupins have eight. Examples include the non-
heme Heme, or haem (pronounced / hi:m/ ), is a precursor to hemoglobin, which is necessary to bind oxygen in the bloodstream. Heme is biosynthesized in both the bone marrow and the liver. In biochemical terms, heme is a coordination complex "consisti ...
dioxygenase Dioxygenases are oxidoreductase enzymes. Aerobic life, from simple single-celled bacteria species to complex eukaryotic organisms, has evolved to depend on the oxidizing power of dioxygen in various metabolic pathways. From energetic adenosine tri ...
enzymes and JmjC-family histone demethylases. Cellular proteins with the double jelly roll fold include glycoside hydrolases of the DUF2961 family, peptide:N-glycosidase F (PNGases F) and
peptidylglycine alpha-amidating monooxygenase Peptidyl-glycine alpha-amidating monooxygenase is an enzyme that catalyzes the conversion of glycine amides to amides and glyoxylate. The enzyme is involved in the biosynthesis of many signaling peptides and some fatty acid amides. In humans, t ...
. A notable difference between PNGases F and the other double jelly roll proteins is the absence of the α-helices, which follow the F and F' strands in capsid proteins and DUF2961. The equivalent regions are variable in the PNGases F and contain either long loops or insertions. By contrast, jelly-roll domains of DUF2961 proteins contain an insertion of short β-hairpins upstream of the G and G' strands of the double jelly roll fold. Importantly, DUF2961 family proteins form trimers resembling viral capsomers.


Evolution

Comparative studies of proteins classified as jelly roll and Greek key structures suggest that the Greek key proteins evolved significantly earlier than their more topologically complex jelly roll counterparts. Structural bioinformatics studies comparing virus capsid jelly-roll proteins to other proteins of known structure indicates that the capsid proteins form a well-separated cluster, suggesting that they are subject to a distinctive set of evolutionary constraints. One of the most notable features of viral capsid jelly roll proteins is their ability to form oligomers in a repeated tiling pattern to produce a closed protein shell; the cellular proteins that are most similar in fold and topology are mostly also oligomers. It has been proposed that viral jelly-roll capsid proteins have evolved from cellular jelly-roll proteins, potentially on several independent occasions, at the earliest stages of cellular evolution.


History and nomenclature

The name "jelly roll" was first used for the structure composed of an elaboration on the Greek key motif by
Jane S. Richardson Jane Shelby Richardson (born January 25, 1941) is an American biophysicist best known for developing the Richardson diagram, or ribbon diagram, a method of representing the 3D structure of proteins. Ribbon diagrams have become a standard repr ...
in 1981 and was intended to reflect the structure's resemblance to a jelly or
Swiss roll A Swiss roll, jelly roll (United States), roll cake, cream roll, roulade or Swiss log is a type of rolled sponge cake filled with whipped cream, jam, or icing. The origins of the term are unclear; in spite of the name "Swiss roll", the cake i ...
cake. The structure has been given a variety of descriptive names, including a wedge, beta barrel, and beta roll. The edges of the two sheets do not meet to form regular
hydrogen bond In chemistry, a hydrogen bond (or H-bond) is a primarily electrostatic force of attraction between a hydrogen (H) atom which is covalently bound to a more electronegative "donor" atom or group (Dn), and another electronegative atom bearing a ...
ing patterns, and so it is often not considered to be a true
beta barrel In protein structures, a beta barrel is a beta sheet composed of tandem repeats that twists and coils to form a closed toroidal structure in which the first strand is bonded to the last strand (hydrogen bond). Beta-strands in many beta-barrels are ...
, though the term is in common use in describing viral capsid architecture. Cellular proteins containing jelly roll-like structures may be described as a cupin fold, a JmjC fold, or a double-stranded beta helix.


References

{{reflist, 30em


External links


Antiparallel β Domains
a section from ''Anatomy and Taxonomy of Protein Structure'' by Jane S. Richardson

by Jacqueline Humphries at ''Small Things Considered'', a blog sponsored by the
American Society for Microbiology The American Society for Microbiology (ASM), originally the Society of American Bacteriologists, is a professional organization for scientists who study viruses, bacteria, fungi, algae, and protozoa as well as other aspects of microbiology. It ...
Protein folds