Degradation of extracellular matrix proteins by hemorrhagic metalloproteinases

Baramova, Eugenia N.; Shannon, John D.; Bjarnason, Jón B.; Fox, Jay W.

doi:10.1016/0003-9861(89)90350-0

Cited by 215 publications

(111 citation statements)

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“…Since the early descriptions of SVMPs and SVMPinduced hemorrhage, it has been postulated that a key step in the pathogenesis of microvascular damage is the enzymatic hydrolysis of BM components [10,28]. However, these observations were based primarily on in vitro degradation studies.…”

Section: Discussionmentioning

confidence: 99%

“…Enzymatic hydrolysis of basement membrane (BM) components has been proposed as a key event in the onset of capillary vessel disruption [5,8]. In vitro, SVMPs are able to digest the BM preparation Matrigel [9], as well as puriWed BM components [9][10][11][12][13][14]. Most of these analyses have been performed by observing the patterns of hydrolysis in SDS-PAGE.…”

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confidence: 99%

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Novel insights into capillary vessel basement membrane damage by snake venom hemorrhagic metalloproteinases: A biochemical and immunohistochemical study

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Shannon

Moura-da-Silva

et al. 2006

Archives of Biochemistry and Biophysics

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The hemorrhagic activity characteristic of viperid snake envenomations is due to the action of venom metalloproteinases (SVMPs) on the capillary vessel basement membrane (BM). This study compared the action of two SVMPs on BM in vitro (degradation of Matrigel) and in vivo (immunohistochemical assessment of BM markers in mouse gastrocnemius muscle). SVMPs BaP1 (belonging to the P-I class) and jararhagin (of the P-III class) had a similar proteolytic activity on azocasein and degraded Matrigel with a slightly diVerent cleavage pattern, since BaP1 exerted a limited proteolysis of both laminin and nidogen, whereas jararhagin predominantly degraded nidogen. In contrast with this pattern of limited proteolysis of BM proteins observed in vitro, immunohistochemical analysis of laminin, nidogen and type IV collagen, as well as of the endothelial cell marker VEGFR-2, in the hemorrhagic areas in the muscle, revealed a pronounced reduction in the immunostaining of these three BM components, associated with a loss of the endothelial cell marker. BM of muscle Wbers was aVected to a lesser extent. In conclusion, in vitro results demonstrated that SVMPs induce a pattern of limited proteolysis on BM components. The drastic loss of these antigens in aVected capillaries in vivo is likely to depend on the combination of limited proteolysis of BM and the action of hemodynamic biophysical forces, previously shown to play a role in SVMP-induced capillary damage, which may cause a mechanical disruption of BM structure.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Novel insights into capillary vessel basement membrane damage by snake venom hemorrhagic metalloproteinases: A biochemical and immunohistochemical study

Escalante

Shannon

Moura-da-Silva

et al. 2006

Archives of Biochemistry and Biophysics

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101

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“…However, their target are not interstitial collagens of type 1, 111, or V, but rather type IV collagen, nidogen, fibronectin, laminin, and gelatin. In this regard, they are more similar to stromelysin (Baramova et al, 1989). The snake venom proteinases show a preference for medium-sized hydrophobic residues in the Pi and P; position and uncharged residues in P, (Kurecki et al, 1978;Fox et al, 1986).…”

Section: Substrate Specificitymentioning

confidence: 99%

The metzincins — Topological and sequential relations between the astacins, adamalysins, serralysins, and matrixins (collagenases) define a super family of zinc‐peptidases

et al. 1995

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The three-dimensional structures of the zinc endopeptidases human neutrophil collagenase, adamalysin I1 from rattle snake venom, alkaline proteinase from Pseudomonas aeruginosa, and astacin from crayfish are topologically similar, with respect to a five-stranded 0-sheet and three a-helices arranged in typical sequential order. The four proteins exhibit the characteristic consensus motif HEXXHXXGXXH, whose three histidine residues are involved in binding of the catalytically essential zinc ion. Moreover, they all share a conserved methionine residue beneath the active site metal as part of a superimposable "Met-turn.'' This structural relationship is supported by a sequence alignment performed on the basis of topological equivalence showing faint but distinct sequential similarity. The alkaline proteinase is about equally distant (26% sequence identity) to both human neutrophil collagenase and astacin and a little further away from adamalysin I1 (17% identity). The pairs astacin/adamalysin 11, astacidhuman neutrophil collagenase, and adamalysin Whuman neutrophil collagenase exhibit sequence identities of 16%, 14%, and 13%, respectively. Therefore, the corresponding four distinct families of zinc peptidases, the astacins, the matrix metalloproteinases (matrixins, collagenases), the adamalysins/reprolysins (snake venom proteinases/reproductive tract proteins), and the serralysins (large bacterial proteases from Serratia, Erwinia, and Pseudomonas) appear to have originated by divergent evolution from a common ancestor and form a superfamily of proteolytic enzymes for which the designation "metzincins" has been proposed. There is also a faint but significant structural relationship of the metzincins to the thermolysin-like enzymes, which share the truncated zincbinding motif HEXXH and, moreover, similar topologies in their N-terminal domains.Keywords: crystal structure; metalloproteinase; molecular evolution; protein family; sequence alignment; topology is involved in metal binding (McKerrow, 1987;

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“…Of the SVMPs, the PIII class is distinguished by being comprised of proproteinase, proteinase, disintegrin-like, and cysteine-rich domains (4). The proteinase domain of all the SVMP hemorrhagic toxins is believed to function to degrade capillary basement membranes, endothelial cell surfaces, and stromal matrix ultimately causing extravasation of capillary contents into the surround stroma (5,6). Interestingly the PIII class of SVMPs is typically much more potent in causing hemorrhage compared with the PI and PII classes that lack the cysteine-rich domain found in the PIII class (4) suggesting a role for this domain in the pathophysiology of the PIII hemorrhagic toxins.…”

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confidence: 99%

“…Indeed the disintegrin-like/cysteine-rich domains of certain hemorrhagic toxins have been shown to be potent inhibitors of collagen-induced platelet aggregation as a result of interaction of the cysteine-rich domain with the ␣2␤1 integrin on platelets (7,8). Proteolytic degradation of capillary basement membrane structures and inhibition of platelet aggregation have been considered to be the key features underlying the hemorrhagic potency of PIII SVMP hemorrhagic toxins (5,9). Similarly recent studies from our laboratory demonstrated the ability of natural disintegrinlike/cysteine-rich domains processed from PIII SVMPs, as well as a recombinant cysteine-rich domain based on the structure from the PIII SVMP atrolysin A proteinase from Crotalus atrox venom, to support the interaction of the PIII SVMPs with von Willebrand factor (10).…”

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confidence: 99%

The Cysteine-rich Domain of Snake Venom Metalloproteinases Is a Ligand for von Willebrand Factor A Domains

Serrano

Kim

Wang

et al. 2006

Journal of Biological Chemistry

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Snake venom metalloproteinases (SVMPs) are members of the Reprolysin family of metalloproteinases to which the ADAM (a disintegrin and metalloproteinase) proteins also belong. The disintegrin-like/cysteine-rich domains of the ADAMs have been implicated in their function. In the case of the SVMPs, we hypothesized that these domains could function to target the metalloproteinases to key extracellular matrix proteins or cell surface proteins. Initially we detected interaction of collagen XIV, a fibril-associated collagen with interrupted triple helices containing von Willebrand factor A (VWA) domains, with the PIII SVMP catrocollastatin. Next we investigated whether other VWA domain-containing matrix proteins could support the binding of PIII SVMPs. Using surface plasmon resonance, the PIII SVMP jararhagin and a recombinant cysteine-rich domain from a PIII SVMP were demonstrated to bind to collagen XIV, collagen XII, and matrilins 1, 3, and 4. Jararhagin was shown to cleave these proteins predominantly at sites localized at or near the VWA domains suggesting that it is the VWA domains to which the PIII SVMPs are binding via their cysteine-rich domain. In light of the fact that these extracellular matrix proteins function to stabilize matrix, targeting the SVMPs to these proteins followed by their specific cleavage could promote the destabilization of extracellular matrix and cell-matrix interactions and in the case of capillaries could contribute to their disruption and hemorrhage. Although there is only limited structural homology shared by the cysteine-rich domains of the PIII SVMPs and the ADAMs our results suggest an analogous function for the cysteine-rich domains in certain members of the expanded ADAM family of proteins to target them to VWA domain-containing proteins.One of the hallmarks of viperid envenoming is local hemorrhage caused by the snake venom metalloproteinases (SVMPs) 2 (1, 2). SVMPs are members of the Reprolysin subfamily of the M12 family of metalloproteinases (3). Of the SVMPs, the PIII class is distinguished by being comprised of proproteinase, proteinase, disintegrin-like, and cysteine-rich domains (4). The proteinase domain of all the SVMP hemorrhagic toxins is believed to function to degrade capillary basement membranes, endothelial cell surfaces, and stromal matrix ultimately causing extravasation of capillary contents into the surround stroma (5, 6). Interestingly the PIII class of SVMPs is typically much more potent in causing hemorrhage compared with the PI and PII classes that lack the cysteine-rich domain found in the PIII class (4) suggesting a role for this domain in the pathophysiology of the PIII hemorrhagic toxins. Indeed the disintegrin-like/cysteine-rich domains of certain hemorrhagic toxins have been shown to be potent inhibitors of collagen-induced platelet aggregation as a result of interaction of the cysteine-rich domain with the ␣2␤1 integrin on platelets (7,8). Proteolytic degradation of capillary basement membrane structures and inhibition of platelet aggregation have...

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Degradation of extracellular matrix proteins by hemorrhagic metalloproteinases

Cited by 215 publications

References 40 publications

Novel insights into capillary vessel basement membrane damage by snake venom hemorrhagic metalloproteinases: A biochemical and immunohistochemical study

Novel insights into capillary vessel basement membrane damage by snake venom hemorrhagic metalloproteinases: A biochemical and immunohistochemical study

The metzincins — Topological and sequential relations between the astacins, adamalysins, serralysins, and matrixins (collagenases) define a super family of zinc‐peptidases

The Cysteine-rich Domain of Snake Venom Metalloproteinases Is a Ligand for von Willebrand Factor A Domains

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