Di-isodityrosine, a novel tetrametric derivative of tyrosine in plant cell wall proteins: a new potential cross-link

Brady, Jeffrey D.; Sadler, Ian H.; Fry, Stephen C.

doi:10.1042/bj3150323

Cited by 104 publications

(92 citation statements)

References 33 publications

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“…An ether link connecting two Tyr residues, identical to that observed in trHbO, has been reported as an oxidative modification of the plant cell wall extensins, where formation of isodityrosine may support insolubilization of these structural proteins (34,35). Moreover, it has long been known that in H 2 O 2 -treated Mb the Fe-heme triggers formation of Tyr-phenoxyl radicals, whose reactivity can affect residues distantly located within the protein scaffold (38)(39)(40).…”

Section: Discussionmentioning

confidence: 99%

A TyrCD1/TrpG8 hydrogen bond network and a TyrB10—TyrCD1 covalent link shape the heme distal site of Mycobacterium tuberculosis hemoglobin O

Milani

Savard

Ouellet

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

109

158

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Truncated hemoglobins (Hbs) are small hemoproteins, identified in microorganisms and in some plants, forming a separate cluster within the Hb superfamily. Two distantly related truncated Hbs, trHbN and trHbO, are expressed at different developmental stages in Mycobacterium tuberculosis. Sequence analysis shows that the two proteins share 18% amino acid identities and belong to different groups within the truncated Hb cluster. Although a specific defense role against nitrosative stress has been ascribed to trHbN (expressed during the Mycobacterium stationary phase), no clear functions have been recognized for trHbO, which is expressed throughout the Mycobacterium growth phase. The 2.1-Å crystal structure of M. tuberculosis cyano-met trHbO shows that the protein assembles in a compact dodecamer. Six of the dodecamer subunits are characterized by a double conformation for their CD regions and, most notably, by a covalent bond linking the phenolic O atom of TyrB10 to the aromatic ring of TyrCD1, in the heme distal cavity. All 12 subunits display a cyanide ion bound to the heme Fe atom, stabilized by a tight hydrogen-bonded network based on the (globin very rare) TyrCD1 and TrpG8 residues. The small apolar AlaE7 residue leaves room for ligand access to the heme distal site through the conventional ''E7 path,'' as proposed for myoglobin. Different from trHbN, where a 20-Å protein matrix tunnel is held to sustain ligand diffusion to an otherwise inaccessible heme distal site, the topologically related region in trHbO hosts two protein matrix cavities.T runcated hemoglobins (trHbs) are a class of small oxygenbinding hemoproteins, dispersed in eubacteria, cyanobacteria, protozoa, and plants, recently recognized as a separate cluster within the hemoglobin (Hb) superfamily. On the basis of amino acid sequence analysis, three phylogenetic groups (groups I, II, and III) have been identified within the trHb family; some organisms contain genes from more than one group, suggesting different functions for trHbs belonging to the diverse groups (1). Crystal structures of three group I trHbs (2, 3) revealed that trHbs are clearly not just another variation on the motif of vertebrate myoglobin (Mb) and Hb. Neither are they similar to nonvertebrate Hbs, including the heme-containing domain of flavohemoglobins, nor to the plant symbiotic and nonsymbiotic Hbs (4-10). Major structural differences associated with known trHbs are an unprecedented 2-on-2 ␣-helical sandwich fold, resulting from striking editing of the classical 3-on-3 globin ␣-helical sandwich, and an extended hydrophobic tunnel͞cavity network linking the solvent space and the distal heme pocket (1-3). Much smaller and topologically unrelated cavities, known by their ability to incorporate Xe atoms, have been found in Mb and interpreted as temporary ligand-docking sites (11,12). In trHbs, the positioning and size of the hydrophobic tunnel suggest important roles in controlling ligand access to the heme, in ligand storage, and͞or accumulation (1-3).An additional major diffe...

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Section: Discussionmentioning

confidence: 99%

A TyrCD1/TrpG8 hydrogen bond network and a TyrB10—TyrCD1 covalent link shape the heme distal site of Mycobacterium tuberculosis hemoglobin O

Milani

Savard

Ouellet

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

109

158

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“…1). The tetra-Tyr derivative, di-Idt, can be formed from two Idt residues in neighboring molecules, while the tri-Tyr derivative, pulcherosine, can be formed from Idt and Tyr (Fry, 1982;Brady et al, 1996;Brady and Fry, 1997). The apparent absence of Idt motifs in the P1 peptides isolated earlier (Smith et al, 1986) may reflect the restriction of Idt to the C-terminal YVYSSPPPPYHY (SGN-U315189).…”

Section: The Extensin Superfamily Over 5 Decadesmentioning

confidence: 99%

“…However, discovery of the cross-linked Tyr derivatives di-isodityrosine (di-Idt) and pulcherosine (Brady et al, 1996) resolves the issue (Fig. 1).…”

Section: The Extensin Superfamily Over 5 Decadesmentioning

confidence: 99%

Role of the Extensin Superfamily in Primary Cell Wall Architecture

et al. 2011

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“…Such differences may imply functionally distinct roles for IDT-rich and IDT-poor extensins, suggested earlier (15) and exemplified by the recent isolation of the lethal RSH mutant (4) corresponding to the loss of a putatively IDT-rich extensin with an essential role in cross-wall formation. Thus self-assembly of these extensin networks in muro may indeed involve self-recognition mediated by the inherent hydrophobicity of the putative cross-linking sites (21,48) aided by concurrent alignment of the highly regular and hydrophilic Ser-(Hyp) 4 glycomodules (1,21).…”

Section: Figmentioning

confidence: 99%

“…More recently, Fry and co-workers (21,22) identified the tetrameric tyrosine derivative, di-isodityrosine (di-IDT), and the trimeric tyrosine derivative, pulcherosine, in wall hydrolysates. They speculated that IDT-containing extensins could be insolubilized into the cell wall network through intermolecular cross-linking of IDT and Tyr residues to form di-IDT and pulcherosine.…”

mentioning

confidence: 99%

Di-isodityrosine Is the Intermolecular Cross-link of Isodityrosine-rich Extensin Analogs Cross-linked in Vitro

Held

Li²,

Kamyab³

et al. 2004

Journal of Biological Chemistry

107

129

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Extensins are cell wall hydroxyproline-rich glycoproteins that form covalent networks putatively involving tyrosyl and lysyl residues in cross-links catalyzed by one or more extensin peroxidases. The precise cross-links remain to be chemically identified both as network components in muro and as enzymic products generated in vitro with native extensin monomers as substrates. However, some extensin monomers contain variations within their putative cross-linking motifs that complicate cross-link identification. Other simpler extensins are recalcitrant to isolation including the ubiquitous P3-type extensin whose major repetitive motif, Ser-(Hyp) 4 -Ser-Hyp-Ser-(Hyp) 4 -Tyr-Tyr-Tyr-Lys, is of particular interest, not least because its Tyr-Tyr-Tyr intramolecular isodityrosine cross-link motifs are also putative candidates for further intermolecular cross-linking to form di-isodityrosine. Therefore, we designed a set of extensin analogs encoding tandem repeats of the P3 motif, including Tyr 3 Phe and Lys 3 Leu variations. Expression of these P3 analogs in Nicotiana tabacum cells yielded glycoproteins with virtually all Pro residues hydroxylated and subsequently arabinosylated and with likely galactosylated Ser residues. This was consistent with earlier analyses of P3 glycopeptides isolated from cell wall digests and the predictions of the Hyp contiguity hypothesis. The tyrosine-rich P3 analogs also contained isodityrosine, formed in vivo. Significantly, these isodityrosine-containing analogs were further crosslinked in vitro by an extensin peroxidase to form the tetra-tyrosine intermolecular cross-link amino acid diisodityrosine. This is the first identification of an intermolecular cross-link amino acid in an extensin module and corroborates earlier suggestions that di-isodityrosine represents one mechanism for cross-linking extensins in muro.Hydroxyproline-rich glycoproteins (HRGPs), 1 which include the extensins, proline-rich proteins, and arabinogalactan proteins (AGPs), contribute to extracellular matrix architecture throughout the plant kingdom and the chlorophycean green algae (1-3). HRGPs are involved in all aspects of plant growth and development, including wall assembly during embryogenesis (4), and responses to biotic and abiotic stress that include mechanical stress (5), physical wounding (6), pathogenesis (7), and symbiosis (8 -10).HRGPs are extended macromolecules consisting of small repetitive peptide and glycopeptide motifs that form peptide modules and glycomodules of functional significance, as in "mix-and-match" mode they define the molecular properties of the overall macromolecule. The glycomodules result from a combination of post-translational modifications unique to plants, namely proline hydroxylation (11) and its subsequent glycosylation (12) that leads either to short arabino-oligosaccharide or larger arabinogalactan polysaccharide addition to the Hyp residues. A sequence-dependent O-Hyp glycosylation code directs the addition of oligosaccharide and polysaccharides (13), and it is likely that...

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Di-isodityrosine, a novel tetrametric derivative of tyrosine in plant cell wall proteins: a new potential cross-link

Cited by 104 publications

References 33 publications

A TyrCD1/TrpG8 hydrogen bond network and a TyrB10—TyrCD1 covalent link shape the heme distal site of Mycobacterium tuberculosis hemoglobin O

A TyrCD1/TrpG8 hydrogen bond network and a TyrB10—TyrCD1 covalent link shape the heme distal site of Mycobacterium tuberculosis hemoglobin O

Role of the Extensin Superfamily in Primary Cell Wall Architecture

Di-isodityrosine Is the Intermolecular Cross-link of Isodityrosine-rich Extensin Analogs Cross-linked in Vitro

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