Relation between active and passive biomechanics of small mesenteric arteries during remodeling

Small artery remodeling involves matrix reorganization, but may also encompass changed smooth muscle cell biomechanical properties. Here we study the temporal relationship between such contractile plasticity and matrix remodeling in small rat mesenteric arteries subjected to 1 or 3 days of altered flow or acute interventions on matrix structure; cross-linking by transglutaminase and matrix digestion by elastase. Diameter-tension relations were made in the passive state and upon full activation (125 mM K+ and 10−5 M norepinephrine). In low flow (LF), inward matrix remodeling occurred after 1 day, when the distended diameter at full dilation (D100) was reduced from 351±15 μm to 299±14 μm (SEM, n=8, p<0.05). The optimal diameter for force development (Dopt) was reduced after 3 days, from 291±10 μm to 247±5 μm (LF, p<0.05). As a result, a mismatch of Dopt/D100 existed after 1 day of LF, which normalized after 3 days. Dynamics of contraction were studied following quick isometric release by 0.2∙D100; tension recovery was faster in anatomically smaller vessels following normal flow. This association was partly lost after 1 day of LF, while after 3 days the vessels became not only smaller but also faster, re-establishing this association. High flow vessels demonstrated similar contractile plasticity. Active diameter-tension relations at low distension did not change following transglutaminase or elastase. However, at high distension, any alteration in passive tension coincided with an opposite change in active tension. These data demonstrate an intrinsic interaction between passive and active biomechanics that occurs instantaneously during matrix remodeling at high distensions while contractile plasticity lags matrix remodeling after flow interventions.