The role of the leech in medical therapeutics

Blood Reviews

Volumn 10, Issue 4, 1996, Pages 201-209

  Eldor, A ^a,c   Orevi, M ^b   Rigbi, M ^b  

^a TEL AVIV UNIVERSITY   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c TEL AVIV SOURASKY MEDICAL CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADRENALIN; ANTISTASIN; ANTITHROMBOCYTIC AGENT; APYRASE; ARACHIDONIC ACID; BLOOD CLOTTING FACTOR 10A INHIBITOR; BLOOD CLOTTING INHIBITOR; COLLAGEN; DESTABILASE; GHILANTEN; HEMADIN; HEMENTERIN; HEMENTIN; HIRUDIN; HIRUSTASIN; THEROMIN; THROMBIN; THROMBIN INHIBITOR; THROMBOCYTE ACTIVATING FACTOR; THROMBOCYTE ACTIVATING FACTOR ANTAGONIST; UNCLASSIFIED DRUG;

BLOOD CLOTTING; DRUG ISOLATION; ENZYME PURIFICATION; HEMOSTASIS; HUMAN; LEECH; NONHUMAN; PHLEBITIS; PLASTIC SURGERY; PRIORITY JOURNAL; REVIEW; SALIVA; THROMBOCYTE AGGREGATION;

EID: 0030478750     PISSN: 0268960X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0268-960X(96)90000-4     Document Type: Article

References (109)

1. Adams SI. The medicinal leech. A page from the annelids of internal medicine. Ann Int Med 1988; 109: 399-405.
2. Shipley AE. Historical preface. In: Harding WA, Moore JP, eds. The Fauna of British India: Hirudinea. London: Taylor and Francis, 1927: 5-32.
3. Nass K. Physicians and leeches and traces in words. Tidsskr Nor Laegeforen 1991; 111: 3667-3669 (Norwegian).
4. Conniff R. The little suckers have made a comeback. Discover 1987; 8: 85-94.
5. Baskova IP, Khalil S, Nartikova VF, Pashkina TS. Inhibition of plasma kallikrein, kininase and kinin-like activities from preparations of medicinal leeches. Thromb Res 1992; 67: 3721-3730.
6. Rigbi M, Levy H, Eldor A et al. The saliva of the medicinal leech Hirudo medicinalis. II. Inhibition of platelet aggregation and of leukocyte activity and examination of reputed anaesthetic effects. Comp Biochem Physiol [C] 1987; 88: 95-98.
7. Lent CM. Serotonergic modulation of the feeding behaviour of the medicinal leech. Brain Res Bull 1985; 14: 643-654.
8. Drapeau P, Kristan WB, Shankland MS, guest eds. Neurobiology and development of the leech. J Neurobiol 1995; 27: 267-445 (special issue).
9. Lent CM, Dickinson MH. The neurobiology of feeding in leeches. Sci Am 1988; 256: 98-103.
10. El-Shimy N. Distribution of the medicinal leech Hirudo medicinalis in the Middle East. Zool Middle East 1986; 1: 154-155.
11. Bromley H. The freshwater leeches (Annelida, Hirudinea) of Israel and adjacent areas. Israel J Zool 1994; 40: 1-24.
12. Babylonian Talmud. Tractate Avodah Zarah, folio 12b.
13. Markwardt F. Hirudin as an inhibitor of thrombin. In: Perlmann GE, Lorand L, eds. Methods Enzymol 1970; XIX: 924-932.
14. Chang JY. The functional domain of hirudin, a thrombin-specific inhibitor. FEBS Lett 1983; 264: 307-313.
15. Dodt J, Müller H-P, Seemüller U, Chang JY The complete amino acid sequence of hirudin, a thrombin specific inhibitor. FEBS Lett 1984; 165: 180-184.
16. Rydel TL, Ravichandran KG, Tulinsky A, et al. The structure of a complex of recombinant hirudin and human athrombin. Science 1990; 249: 277-280.
17. Markwardt F, Nowak G, Sturzebecher J, Griessbach U, Walsmann P, Vogel G. Pharmacokinetics and anticoagulant effect of hirudin in man. Thromb Haemostas 1984; 52: 160-163.
18. First International Symposium on Hirudin. Frankfurt A.M., 23-24 June 1989. Angio Archiv (Munich) 1989; 18: 1-104 (abstracts).
19. Stone SR, Maraganore JM. Hirudin and hirudin-based peptides. In: Lorand L, Mann KC, eds. Methods Enzymol 1993; 223: 312-336.
20. Märki EW, Wallis RB. The anticoagulant and antithrombotic properties of hirudins. Thromb Haemostas 1990; 64: 344-348.
21. Fritz H, Bichler J. Hirudin, a new therapeutic tool? Ann Haematol 1991; 63: 67-76.
22. Harvey RP, Degryse E, Stefani L et al. Cloning and expression of cDNA coding for the anticoagulant hirudin from the blood-sucking leech Hirudo medicinalis. Proc Natl Acad Sci USA 1986; 83: 1084-1088.
23. Bergmann C, Dodt J, Kohler S, Fink E, Ciassen HG. Chemical synthesis and expression of a gene coding for hirudin, the thrombin-specific inhibitor from the leech Hirudo medicinalis. Biol Chem Hoppe-Seyler 1986; 367: 731-740.
24. Dodt J, Shmitz T, Schafer T, Bergmann C. Expression, secretion and processing of hirudin in E. coli using the alkaline phosphatase signal sequence. FEBS Lett 1986; 202:373-377.
25. Rigbi M, Levy H, Iraqi F et al. The saliva of the medicinal leech Hirudo medicinalis. I. Biochemical characterization of the high molecular weight fraction. Comp Biochem Physiol [B] 1987; 87:567-573.
26. Strube KH, Kröger B, Bialojan S, Otte M, Dodt J. Isolation, sequence analysis and cloning of haemadin. J Biol Chem 1993; 268: 8590-8595.
27. Hemberger J, Guessow D, Lottspeich F, Wolf S, Dodt J. Isolation and characterization of theromin, a new thrombin-inhibitor from the leech Theromyzon tessulatum. XVth Congress of the International Society on Thrombosis and Haemostasis, Jerusalem, Israel, June 11-16, 1995 Abstr. No. 1557).
28. Electricwala A, Sawyer RT, Jones CP, Atkinson T. Isolation of a thrombin inhibitor from the leech Hirudinaria manillensis. Blood Coag Fibrinolysis 1991; 2: 83-89.
29. Steiner V, Knecht R, Bornsen KO et al. Primary structure and function of novel O-glycosylated hirudins from the leech Hirudinaria manillensis. Biochemistry 1992; 31: 2294-2298.
30. Scacheri E, Nitti G, Valsasina B et al. Novel hirudin variants from the leech Hirudinaria manillensis. Amino acid sequence, cDNA cloning and genomic organization. Eur J Biochem 1993; 214: 295-304.
31. Electricwala A, Hartwell R, Scawen MD, Atkinson T. The complete amino acid sequence of a hirudin variant from the leech Hirudinaria manillensis. J Protein Chem 1993; 12: 365-370.
32. Baskova IP, Nikonov GI. Destabilase, the novel ε-(γGlu)-Lys isopeptidase with thrombolytic activity. Blood Coag Fibrinolysis 1992; 2: 167-172.
33. Zavalova LL, Kuzina EV, Levina LB, Baskova IP. Monomerization of fraction DD by destabilase from the medicinal leech does not alter the N-terminal sequence of the γ-chain. Thromb Res 1994; 71: 241-244.
34. Tuszynski GP, Gasic TB, Gasic GJ. Isolation and characterization of antistasin. J Biol Chem 1987; 262: 9718-9723.
35. Dunwiddie C, Thornberry NA, Bull HG et al. Antistasin, a leech-derived inhibitor of Factor Xa. Kinetic analysis of enzyme inhibition and identification of the reactive site. J Biol Chem 1989; 264: 16694-16699.
36. Hofmann KJ, Nutt EM, Dunwiddie CT. Site-directed mutagenesis of the leech derived factor Xa inhibitor antistasin. Probing the reactive site. Biochem J 1992; 287: 943-949.
37. Manley GD, Owen TJ, Krstenansky JL, Brankamp RG, Cardin AD. Heparin binding properties of the carboxyl terminal domain of [A 103, 106, 108] antistasin 93-119. Adv Exp Med Biol 1992; 313: 135-140.
38. Schreuder H, Arkema A, de Boer B et al. Crystallization and preliminary crystallographic analysis of antistasin, a leechderived inhibitor of blood coagulation factor Xa. J Mol Biol 1993; 231: 1137-1138.
39. Dunwiddie CT, Waxman L, Vlasuk GP, Friedman PA. Purification and characterization of blood coagulation factor Xa from hematophagous organisms. In: Lorand L, Mann KC, eds. Methods Enzymol 1993; 223: 291-312.
40. Ohta N, Brush M, Jacobs JW. Interaction of antistasin-related peptides with factor Xa: identification of a core inhibitory sequence. Thromb Haemost 1994; 72: 825-830.
41. Theunissen HJ, Dijkema R, Swinkels JC, de-Poorter TL, Vink PM, van-Dinther TG. Mutational analysis of antistasin, an inhibitor of blood coagulation factor Xa derived from the Mexican leech Haementeria officinalis. Thromb Res 1994; 75: 41-50.
42. Rigbi M, Jackson CM, Latallo ZS. A specific inhibitor of bovine factor Xa in the saliva of the medicinal leech Hirudo medicinalis. 14th International Congress of Biochemistry. Prague, Czechoslovakia, 1988, Abstr. No. FR 037.
43. Rigbi M, Jackson CM, Atamna H et al. F.Xa inhibitor from the saliva of the leech Hirudo medicinalis. XVth Congress of the International Society on Thrombosis and Haemostasis. Jerusalem, Israel, 1995, Abstr. No. 1558).
44. Werber MM, Zeelon E, Levanon A et al. Yagin, a leech-derived FXa inhibitor expressed in and recovered from E. coli: Anti-thrombotic potency in vitro and in vivo. XVth Congress of the International Society on Thrombosis and Haemostasis. Jerusalem, Israel, 1995, Abstr. No. 1582.
45. Hanson SR, Harker LA, Levanon A, Panet A, Werber MM. Inhibition of Factor Xa in baboon thrombosis models. XVth Congress of the International Society on Thrombosis and Haemostasis. Jerusalem, Israel, 1995, Abstr. No. 1578.
46. Kornowski R, Eldor A, Werber M et al. Enhancement of rTPA thrombolysis with a selective factor Xa inhibitor derived from the leech: comparison to heparin and hirudin in a rabbit thrombosis model. XVth Congress of the International Society on Thrombosis and Haemostasis, Jerusalem,Israel, 1995, Abstr. No 1600.
47. Mellott MJ, Holahan MA, Lynch JJ, Vlasuk GP, Dunwiddie CT. Acceleration of recombinant tissue-type plasminogen activator-induced reperfusion and prevention of reocclusion by recombinant antistasin, a selective factor Xa inhibitor, in a canine model of femoral arterial thrombosis. Circ Res 1992; 70: 1152-1160.
48. Condra C, Nutt EM, Petroski CJ, Simpson E, Friedman PA, Jacobs JW. Isolation and structural characterization of a potent inhibitor of coagulation Factor Xa from the leech Haementeria ghilianii. Thromb Haemost 1989; 61: 437-441.
49. 48a.Brankamp, RG, Manley CG, Blankenship, DT, Bowlin TL, Cardin AD. Studies on the anticoagulant, antimetastatic and heparin-binding properties of ghilanten-related inhibitors. Blood Coagul Fibrinolysis 1991; 2: 161-167.
50. Budzynski AZ, Olexa SA, Brizuela BS, Sawyer RT, Stent GS. Anticoagulant and antifibrinolytic properties of salivary proteins from the leech Haementeria ghilianii. Proc Soc Exp Biol Med 1981; 168: 266-275.
51. Budzynski AZ. Interaction of hementin with fibrinogen and fibrin. Blood Coag Fibrinolysis 1991; 2: 149-152.
52. Sawyer RT, Jones CP, Munro RT. The biological formation of hementin in the proboscis of the leech Haementeria ghilianii. Blood Coag Fibrinolysis 1991; 2: 153-159.
53. Gasic GJ, Viner ED, Budzynski, AZ, Gasic GP. Inhibition of lung tumor colonization by leech salivary gland extracts from Haementeria ghilianii. Cancer Res 1983; 43: 1633-1635.
54. Söllner C, Mentele B, Eckerskorn C, Fritz, H, Sommerhoff CP. Isolation and characterization of hirustasin, an antistasin-type serine proteinase inhibitor from the medical leech Hirudo medicinalis. Eur J Biochem 1994; 219: 937-943.
55. Kelen EMA, Rosenfeld G. Fibrinogenolytic substance (hementerin) of Brazilian blood-sucking leeches (Haementeria lutzi Pinto [1920]) Haemostasis 1975; 4: 51-64.
56. Waxman L, Smith DE, Arcuri KE, Vlasuk GP. The tick anticoagulant peptide (TAP) is a novel inhibitor of factor Xa. Science 1990; 248: 593-596.
57. Jordan SP, Waxman L, Smith DE, Vlasuk GP. Tick anticoagulant peptide: kinetic analysis of recombinant inhibitor with blood coagulation factor Xa. Biochemistry 1990; 29: 11095-11100.
58. Fioravanti C, Burkholder D, Francis B, Siegel PK, Gibson RE. Antithrombotic activity of recombinant tick anticoagulant peptide and heparin in a rabbit model of venous thrombosis. Thromb Res 1993; 71: 317-324.
59. Jacobs JW, Cupp EW, Sardana M, Friedman PA. Isolation and characterization of a coagulation factor Xa inhibitor from black fly salivary glands. Thromb Haemostas 1990; 64: 235-238.
60. Parker KR, Mant MJ. Effect of tsetse salivary gland homogenate on coagulation and fibrinolysis. Thromb Haemostas 1979; 42: 723-751.
61. Mumcuoglu KK, Galun R, Kaminchik V, Panet A, Levanon A. Antihemostatic activity of the human body louse Pediculus humanus humanus (Anoplura: Pediculidae). J Insect Physiol (in press).
62. Gordon JR, Allen JR. Factors V and VII anticoagulant activities in the salivary glands of feeding Dermacentor andersoni ticks. J Parasitol 1991; 77: 167-170.
63. Hellman K, Hawkins R. Prolixin-S and prolixin-G: two anticoagulants from Rhodnius prolixus Stahl. Nature 1965; 207: 265-267.
64. Cappelo M, Clyne LP, McPhedran P, Hotez PJ. The Ancylostoma factor Xa inhibitor: Partial purification and its identification as a major hookworm-derived anticoagulant in vitro. J Infect Dis 1993; 167: 1474-1477.
65. Gardell SJ, Friedman PA. Vampire bat salivary plasminogen activator. In: Lorand L, Mann KC, eds. Methods Enzymol 1993; 223: 233-249.
66. Seymour JL, Lindquist RN, Dennis MS et al. Ecotin is a potent anticoagulant and reversible tight binding inhibitor of Factor Xa. Biochemistry 1994; 33: 3949-3958.
67. Galun R. The role of host blood in the feeding behaviour of ectoparasites. In: Zuckerman A, ed. Dynamic Aspects of Host-Parasite Relationships, Vol. II. New York: Wiley Jerusalem: Israel Universities Press, 1975: 132-162.
68. Orevi M, Rigbi M, Hy-Am E, Matzner Y, Eldor A. A potent inhibitor of platelet activating factor from the saliva of the leech Hirudo medicinalis. Prostaglandins 1992; 43: 483-495.
69. Orevi M, Rigbi M, Horovitz A, Eldor A. Platelet aggregation inhibitors in Hirudo medicinalis leech saliva. Partial purification and characterization by their effect on different platelet agonists. Blood 1987; 70(Suppl. 1) 357a (Abstr.).
70. Baskova IP, Misselwitz F, Nikonov GI, Novikov ID, Leitin VL, Repin VS. Salivary gland secretion of the leech Hirudo medicinalis inhibits ADP induced human platelet adhesion on a collagen coated surface. Biul Eksp Biol Med 1984; 97: 696-699 (Russian; English translation).
71. Baskova IP, Nikonov GI, Mazurov AV, et al. Mechanisms of the inhibition of vascular-platelet hemostasis by salivary gland secretion of the medicinal leech Hirudo medicinalis. Biochemistry (Biokhimiya) 1987; 52: 1261-1267 (Russian; English translation).
72. Baskova IP, Nikonov GI. Detection of prostaglandins in preparations from the medicinal leech (Hirudo medicinalis). Proc Acad Sci USSR 1987; 292: 1492-1493 (Russian).
73. Law JH, Ribeiro JMC, Wells MA. Biochemical insights derived from insect diversity. Ann Rev Biochem 1992; 67: 87-111.
74. Munro R, Jones CP, Sawyer RT. Calin - a platelet adhesion inhibitor from the saliva of the medicinal leech. Blood Coagul Fibrinolysis 1991; 2: 179-184.
75. Deckmyn H, Stassen JM, Vreys I, Van-Houtte E, Sawyer RT, Vermylen J. Calin from Hirudo medicinalis, an inhibitor of platelet adhesion to collagen, prevents platelet-rich thrombosis in hamsters. Blood 1995; 85: 712-719.
76. Harsfalvi J, Stassen JM, Hoylaerts MF et al. Calin from Hirudo medicinalis, an inhibitor of von Willebrand factor binding to collagen under static and flow conditions. Blood 1995; 85: 705-711.
77. Keller PM, Schultz LD, Condra C, Karczewski J, Connolly TM. An inhibitor of collagen-stimulated platelet activation from the salivary glands of the Haementeria officinalis leech. II. Cloning of the cDNA and expression. J Biol Chem 1992; 267: 6899-6904.
78. Connolly TM, Jacobs JW, Condra C. An inhibitor of collagen-stimulated platelet activation from the salivary glands of the Haementeria officinalis leech. I. Identification, isolation and characterization. J Biol Chem 1992; 267: 6893-6898.
79. van-Zanten GH, Connolly TM, Schiphorst ME, de Graaf S, Slootweg PJ, Sixma JJ. Recombinant leech antiplatelet protein specifically blocks platelet deposition on collagen surfaces under flow conditions. Arterioscler Thromb Vasc Biol 1995; 15: 1424-1431.
80. Ribeiro JMC, Garcia ES. Platelet antiaggregating activity in the salivary secretion of the blood-sucking bug Rhodnius prolixus. Experientia 1981; 37: 384-386.
81. Waxman L, Connolly TM. Isolation of an inhibitor selective for collagen-stimulated platelet adhesion from the soft tick Ornithodorus moubata. J Biol Chem 1993; 268: 5445-5449.
82. Keller PM, Waxman L, Arnold BA, Schulz LD, Condra C, Connolly TM. Cloning of the cDNA and expression of moubatin, an inhibitor of platelet aggregation. J Biol Chem 1993; 268: 5450-5456.
83. Noeske-Jungblut C, Krätzchmar J, Haendler B et al. Collagen-induced platelet aggregation is specifically inhibited by a salivary protein of the assassin bug (Triatoma pallipidensis). Thromb Haemost 1993; 69: 783 (Abstr.).
84. Smith JB, Dangelmaier C, Selak M. Identification of 50 kDa snake venom proteins which specifically inhibit platelet adhesion to collagen. FEBS Lett 1991; 283: 307-310.
85. Linker A, Meyer K, Hoffman P. The production of hyaluronate oligosaccharides by leech hyaluronidase and alkali. J Biol Chem 1960; 235: 924-927.
86. Yuki H, Fishman WH. Purification and characterization of leech hyaluronic acid-endo-β-glucuronidase. J Biol Chem 1963; 238: 1877-1879.
87. Damas D. Étude histologique et histochimique des glandes salivaires de la sangsue médicinale Hirudo medicinalis (Hirudinée, Gnathobdelle). Arch Zool Exp Gen 1974; 115: 279-292.
88. Seemüller U, Dodt J, Fink E, Fritz H. Proteinase inhibitors of the leech Hirudo medicinalis (hirudins, bdellins, eglins). In: Barrett AJ, Salvesen G eds. Proteinase Inhibitors. Amsterdam: Elsevier, 1986: 337-352.
89. Seemüller U, Meier M, Ohlsson K, Müller HP, Fritz H. Isolation and characterization of a low molecular inhibitor (of chymotrypsin and human granulocyte elastase and cathepsin G) from leeches. Hoppe-Seyler's Z Physiol Chem 1977; 358: 1105-1117.
90. Hanahan DJ. Platelet activating factor. A biologically active phosphoglyceride. Ann Rev Biochem 1986; 55: 435-510.
91. Braquet P, Touqi L, Shen TY, Vargaftig BB. Perspectives in platelet activating factor research. Pharmacol Rev 1987; 39: 97-145.
92. Seymour JL, Henzel WJ, Nevins B, Strels JT, Lazarus RA. Decorsin: a potent glycoprotein IIb-IIIa antagonist and platelet aggregation inhibitor from the leech Macrobdella decora. J Biol Chem 1990; 266: 10143-10147.
93. Mazur P, Henzel WJ, Seymour JL, Lazarus RA. Ornatins: potent glycoprotein IIb-IIIa antagonists and platelet aggregation inhibitors from the leech Placobdella ornata. Eur J Biochem 1991; 202: 1073-1082.
94. Mazur P, Dennis MS, Seymour JL, Lazarus RA. Expression, purification, and characterization of recombinant ornatin E, a potent glycoprotein IIb-IIIa antagonist. Protein Expr Purif 1993; 4: 282-289.
95. Denis MS, Henzel WJ, Pitti RM et al. Platelet glycoprotein IIb-IIIa protein antagonists from snake venoms. Evidence for a family of platelet aggregation inhibitors. Proc Natl Acad Sci USA 1990; 87: 2471-2475.
96. Krezel AM, Wagner G, Seymour-Ulmer J, Lazarus RA. Structure of the RGD protein decorsin: conserved motif and distinct function in leech proteins that affect blood clotting. Science 1994; 264: 1944-1947.
97. Munro R, Hechtel FOP, Sawyer RT. Sustained bleeding after a leech bite in the apparent absence of hirudin. Thromb Haemostas 1989; 61: 366-369.
98. Magnus W Der Blutegelgebiss und seine Wirkung auf menschliche Gefässe. Zentralbl Chir 1928; 55:2355-2357 (German).
99. Lindemann B. Das Verhalten der Kapillaren in der Umgebung des Blutegelgebisses. Archiv Exp Path Pharmak 1939; 193: 490-502.
100. Henderson HP, Matti B, Laing AG, Morelli S, Sully L. Avulsion of the scalp treated by microvascular repair. The use of leeches for post operative decongestion. Br J Plast Surg 1983; 36: 235-239.
101. Whitlock MR, O'Hare PM, Sanders R, Morrow NC. The medicinal leech and its use in plastic surgery. A possible cause for infection. Br J Plast Surg 1983; 36: 240-244.
102. Mutimer KL, Banis JC, Upton J. Microsurgical reattachment of totally amputated ears. Plast Reconstruct Surg 1987; 79: 535-540.
103. Lineaweaver WC, O'Hara M, Stridde B, Valauri FA, Buncke HJ. Clinical leech use in a microsugical unit: the San Francisco experience. Blood Coagul Fibrinolysis 1991; 2: 189-192.
104. Valauri FA. The use of medicinal leeches in microsurgery. Blood Coagul Fibrinolysis 1991; 2: 185-187.
105. Wells MD, Manktelow RT, Boyd JB, Bowen V. The medical leech: an old treatment revisited. Microsurgery 1993; 14: 183-186.
106. Adams JF, Lassen LF. Leech therapy for venous congestion following myocutaneous pectoralis flap reconstruction. ORL Head Neck Nurs 1995; 13: 12-14.
107. Rigbi M, Orevi M, Eldor A. Platelet aggregation and coagulation inhibitors in leech saliva and their roles in leech therapy. Sem Thrombos Hemostas 1996; 22: 273-278.
108. Brody GA, Mahoney WJ, Hentz VR. Digit replantation applying the leech Hirudo medicinalis. Clin Orthop 1989; 133: 245-249.
109. Lineaweaver WC, Hill MK, Buncke GM et al. Aeromonas hydrophila infections following use of medicinal leeches in replantation and flap surgery. Ann Plast Surg 1992; 29: 238-244.