Abstract
From a survival perspective, it is hypothesized that leech saliva exhibits certain physiological effects to ensure fast blood-feeding, including analgesia, anesthesia, and anti-inflammation to stay undetected by the host and vasodilatation and anti-hemostasis to ensure a steady, rapid, and sustained blood flow to the feeding site. Many anti-hemostatic compounds have been identified in leech saliva, such as hirudin, calin, and bdellin A. However, no specific substance with direct vasodilatory and anti-inflammatory function has been reported from forest leech saliva. Herein, using activity-guided analysis, prostaglandin E1 (PGE1) was identified for the first time as an efficient molecular tool for forest leech blood sucking. The structure of PGE1 was analyzed by nuclear magnetic resonance spectroscopy and high-resolution electrospray ionization mass spectroscopy. PGE1 was found to be primarily distributed in the leech salivary gland (1228.36 ng/g body weight). We also analyzed how forest leech PGE1 affects platelet aggregation, skin vascular permeability, bleeding time, and pain. Results indicated that PGE1 efficiently inhibited platelet aggregation induced by adenosine diphosphate (ADP) (5 μM) with an IC50 of 21.81 ± 2.24 nM. At doses of 10, 100 nM, and 1 μM, PGE1 increased vascular permeability by 1.18, 5.8, and 9.2 times. It also prolonged bleeding time in a concentration-independent manner. In the formalin-induced mouse paw pain model, PGE1 suppressed acute pain. To the best of our knowledge, this is the first report on PGE1 in invertebrates. The functions of PGE1, such as vasodilation, platelet aggregation inhibition, anti-inflammation, and pain alleviation, may facilitate the ingestion of host blood by leeches.
Highlights
IntroductionAs exclusively blood-sucking ectoparasites, leeches must penetrate the body surface of their host and suppress host reactions to injury, swelling, pain, and inflammation in order to remain undetected and successfully obtain a blood meal
Animal venom facilitates survival by antagonizing prey and predators [1]
We identified a major component showing platelet aggregation inhibition in the leech salivary gland, which accounted for ∼60% of the activity (Figure 1)
Summary
As exclusively blood-sucking ectoparasites, leeches must penetrate the body surface of their host and suppress host reactions to injury, swelling, pain, and inflammation in order to remain undetected and successfully obtain a blood meal. Leeches counteract these reactions by injecting saliva into their hosts. This suggests that analgesic or anesthetic agents may be delivered to the host during the blood-sucking process. Blood-sucking leeches have been used for medical purposes in humans for more than two thousand years and are approved as medicinal agents in many countries [4]. Increasing attention has been paid to medicinal leech therapy in pain syndromes [6] as its analgesic effects appear to be rapid, effective, and long-lasting in various conditions [7]
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