Abstract
Blood clotting at wound sites is critical for preventing blood loss and invasion by microorganisms in multicellular animals, especially small insects vulnerable to dehydration. The mechanistic reaction of the clot is the first step in providing scaffolding for the formation of new epithelial and cuticular tissue. The clot, therefore, requires special materials properties. We have developed and used nano-rheological magnetic rotational spectroscopy with nanorods to quantitatively study nucleation of cell aggregates that occurs within fractions of a second. Using larvae of Manduca sexta, we discovered that clot nucleation is a two-step process whereby cell aggregation is the time-limiting step followed by rigidification of the aggregate. Clot nucleation and transformation of viscous blood into a visco-elastic aggregate happens in a few minutes, which is hundreds of times faster than wound plugging and scab formation. This discovery sets a time scale for insect clotting phenomena, establishing a materials metric for the kinetics of biochemical reaction cascades. Combined with biochemical and biomolecular studies, these discoveries can help design fast-working thickeners for vertebrate blood, including human blood, based on clotting principles of insect blood.
Highlights
Living in an environment surrounded by natural enemies and microbial pathogens, insects have evolved distinct strategies to deal with wounding and potential infection[1,2,3,4,5,6,7]
The most detailed analysis and classification of physical phenomena and patterns of cell aggregation associated with blood coagulation and clotting in insects was described in the last century[1,15,16,17]
Recent progress in understanding wound healing has been achieved with advances in microscopy and genetics, revealing that the cellular responses are coordinated by multiple signals from the wound[4,7,9,18,19]
Summary
Living in an environment surrounded by natural enemies and microbial pathogens, insects have evolved distinct strategies to deal with wounding and potential infection[1,2,3,4,5,6,7]. Catalysis of phenoloxidase results in formation of a variety of immune defense molecules, high molecular weight macromolecular complexes, and pigments of the melanin group[11,12] These molecules and macromolecular complexes trigger an orchestrated action of physico-chemical phenomena at different temporal and spatial scales to form a fibrous biopolymer gel with entrapped cells. The most detailed analysis and classification of physical phenomena and patterns of cell aggregation associated with blood coagulation and clotting in insects was described in the last century[1,15,16,17]. Our primary goal was to identify the pattern of cell aggregation and quantify its kinetics at short time scales (minutes). We show that cell aggregation occurs in two steps within several minutes: 1) the cells first gather into an aggregate, followed by 2) densification and rigidification of the aggregate, leading to formation of an elastic clot
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