Nanodiamond-Enabled Torsion Microscopy Uncovers Multidimensional Cell-Matrix Mechanical Interactions

Abstract

Traditional cellular force-sensing techniques, such as traction force microscopy (TFM), are predominantly limited to measuring linear tractions, overlooking and technically unable to capture the nanoscale torsional forces that are critical in cell-matrix interactions. Here, we introduce a nanodiamond-enabled torsion microscopy (DTM) that integrates nitrogen-vacancy (NV) centers as orientation markers with micropillar arrays to decouple and quantify nanoscale rotational and translational motions induced by cells. This approach achieves high precision (~1.47 degree rotational accuracy and ~3.13*10-15 Nm torque sensitivity), enabling reconstruction of cellular torsional force fields and twisting energy distributions previously underestimated. Our findings reveal the widespread presence of torsional forces in cell-matrix interactions, introducing "cellular mechanical modes" where different adhesion patterns dictate the balance between traction- and torque- mediated mechanical energy transferred to the substrate. Notably, in immune cells like macrophages that generally exert low linear tractions, torque overwhelmingly dominates traction, highlighting a unique mechanical output for specific cellular functions. By uncovering these differential modes, DTM provides a versatile tool to advance biomechanical investigations, with potential applications in disease diagnostics and therapeutics.