Complement activation-related cardiac anaphylaxis in pigs: Role of C5a anaphylatoxin and adenosine in liposome-induced abnormalities in ECG and heart function

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 290, Issue 3, 2006, Pages

  Szebeni, János ^a,d   Baranyi, Lajos ^b   Sávay, Sándor ^b   Bodó, Michael ^b   Milosevits, János ^b   Alving, Carl R ^a   Bünger, Rolf ^c  

^a Department of Vaccine Production and Delivery   (United States)

^b WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^c UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^d US Military HIV Research Program   (United States)

Author keywords

Adenosine receptors; Allergy; Anaphylactoid reactions; Bezold jarisch reflex; Cyclopentyl xanthine; Electrocardiography; Hemodynamic changes; Hypersensitivity reactions; Pseudoallergy

Indexed keywords

ADENOSINE; ADENOSINE RECEPTOR; ADENOSINE RECEPTOR BLOCKING AGENT; ANAPHYLATOXIN; ANTIBODY; COMPLEMENT COMPONENT C3B RECEPTOR; COMPLEMENT COMPONENT C5A; COMPLEMENT COMPONENT C5A ANTIBODY; DOXORUBICIN; LIPOSOME; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; ZM 24135; ZYMOSAN; COMPLEMENT COMPONENT C5A RECEPTOR;

ANAPHYLAXIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRADYCARDIA; COMPLEMENT ACTIVATION; CONTROLLED STUDY; DRUG INHIBITION; ECG ABNORMALITY; HEART ARREST; HEART ARRHYTHMIA; HEART FUNCTION; HEART STRESS; HEART VENTRICLE FIBRILLATION; HEMODYNAMICS; HYPOTENSION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; SWINE; SYMPTOM; TACHYCARDIA; ANIMAL; CHEMICALLY INDUCED DISORDER; DISEASE MODEL; DRUG EFFECT; ELECTROCARDIOGRAPHY; HEART LEFT VENTRICLE FUNCTION; IMMUNOLOGY;

ADENOSINE; ANAPHYLAXIS; ANIMALS; ARRHYTHMIA; COMPLEMENT ACTIVATION; DISEASE MODELS, ANIMAL; ELECTROCARDIOGRAPHY; LIPOSOMES; RECEPTOR, ANAPHYLATOXIN C5A; RECEPTORS, PURINERGIC P1; SWINE; VENTRICULAR DYSFUNCTION, LEFT;

EID: 33645739682     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00622.2005     Document Type: Article

References (53)

1. Aguado JM, Hidalgo M, Moya I, Alcazar JM, Jimenez MJ, and Noriega AR. Ventricular arrhythmias with conventional and liposomal amphotericin. Lancet 342: 1239, 1993.
2. ALZA. Pharmaceuticals Doxil Package Insert. Mountain View, CA: ALZA, 2000.
3. Aviado DM and Aviado GD. The Bezold-Jarisch reflex. A historical perspective of cardiopulmonary reflexes. Ann NY Acad Sci 940: 48-58, 2001.
4. Bellardinelli L, Linden J, and Berne RM. The cardiac effects of adenosine. Prog Cardiovasc Dis 32: 73-97, 1987.
5. Ciesielski-Carlucci C, Leong P, and Jacobs C. Case report of anaphylaxis from cisplatin/paclitaxel and a review of their hypersensitivity reaction profiles. Am J Clin Oncol 20: 373-375, 1997.
6. De Luca L, Cinque C, Chiummariello S, and Berni Canani R. Cardiac involvement in food allergy study of cardiac activity by Holter monitoring in 12 allergic children during food challenge. Pediatr Med Chir 12: 139-145, 1990.
7. Del Balzo U, Polley MJ, and Levi R. Cardiac anaphylaxis. Complement activation as an amplification system. Circ Res 65: 847-857, 1989.
8. Del Balzo U, Sakuma I, and Levi R. Cardiac dysfunction caused by recombinant human C5A anaphylatoxin: mediation by histamine, adenosine and cyclooxygenase arachidonate metabolites. J Pharmacol Exp Ther 253: 171-179, 1990.
9. Demetriades D, Chan LS, Bhasin P, Berne TV, Ramicone E, Huicochea F, Velmahos G, Cornwell EE, Belzberg H, Murray J, and Asensio JA. Relative bradycardia in patients with traumatic hypotension. J Trauma 45: 534-539, 1998.
10. Fossa SD, Aass N, and Paro G. A phase II study of DaunoXome in advanced urothelial transitional cell carcinoma. Eur J Cancer 34: 1131-1132, 1998.
11. Fredholm BB, Izerman AP, Jacobson KA, Klotz KN, and Linden J. International union of pharmacology. XXV nomenclature and classification of adenosine receptors. Pharmacol Rev 53: 527-552, 2001.
12. Grossman J. The occurrence of arrhythmias in hospitalized asthmatic patients. J Allergy Clin Immunol 57: 310-317, 1976.
13. Homeister JW, Satoh P, and Lucchesi BR. Effects of complement activation in the isolated heart. Role of the terminal complement components. Circ Res 71: 303-319, 1992.
14. Hopken U, Mohr M, Struber A, Montz H, Burchardi H, Gotze O, and Oppermann M. Inhibition of interleukin-6 synthesis in an animal model of septic shock by anti-C5a monoclonal antibodies. Eur J Immunol 26: 1103-1109, 1996.
15. Hugli TE. Structure and function of anaphylatoxins. Springer Semin Immunopathol 7: 193-219, 1984.
16. Ilschner S, Nolte C, and Kettenmann H. Complement factor C5a and epidermal growth factor trigger the activation of outward potassium currents in cultured murine microglia. Neuroscience 73: 1109-1120, 1996.
17. Ito BR and Del Balzo U. Effect of platelet depletion and inhibition of platelet cyclooxygenase on C5a-mediated myocardial ischemia. Am J Physiol Heart Circ Physiol 267: H1288-H1294, 1994.
18. Ito BR, Engler RL, and Del Balzo U. Role of cardiac mast cells in complement C5a-induced myocardial ischemia. Am J Physiol Heart Circ Physiol 264: H1346-H1354, 1993.
19. Laher S and Karp SJ. Acute myocardial infarction following paclitaxel administration for ovarian carcinoma. Clin Oncol (R Coll Radiol) 9: 124-126, 1997.
20. Marceau F, Lundberg C, and Hugli TE. Effects of anaphylatoxins on circulation. Immunopharmacology 14: 67-84, 1987.
21. Markman M, Kennedy A, Webster K, Kulp B, Peterson G, and Belinson J. Paclitaxel administration to gynecologic cancer patients with major cardiac risk factors. J Clin Oncol 16: 3483-3485, 1998.
22. Marone G, Bova M, Detoraki A, Onorati AM, Rossi FW, and Spadaro G. The human heart as a shock organ in anaphylaxis. Novartis Found Symp 257: 133-149, 2004.
23. Marone G, de Crescenzo G, Adt M, Patella V, Arbustini E, and Genovese A. Immunological characterization and functional importance of human heart mast cells. Immunopharmacology 31: 1-18, 1995.
24. Marone G, Patella V, de Crescenzo G, Genovese A, and Adt M. Human heart mast cells in anaphylaxis and cardiovascular disease. Int Arch Allergy Immunol 107: 72-75, 1995.
25. Martin SE, Chenoweth DE, Engler RL, Roth DM, and Longhurst JC. C5a decreases regional coronary blood flow and myocardial function in pigs: implications for a granulocyte mechanism. Circ Res 63: 483-491, 1988.
26. 1 receptor system. Cardiovasc Res 27: 28-35, 1993.
27. Patella V, de Crescenzo G, Ciccarelli A, Marin I, Adt M, and Marone G. Human heart mast cells: a definitive case of mast cell heterogeneity. Int Arch Allergy Immunol 106: 386-393, 1995.
28. Patella V, Marino I, Lamparter B, Arbustini E, Adt M, and Marone G. Human heart mast cells. Isolation, purification, ultrastructure, and immunologic characterization. J Immunol 154: 2855-2865, 1995.
29. Prakash ES and Madanmohan. When the heart is stopped for good: hypotension-bradycardia paradox revisited. Adv Physiol Educ 29: 15-20, 2005.
30. Pumphrey RS. Lessons for management of anaphylaxis from a study of fatal reactions. Clin Exp Allergy 30: 1144-1150, 2000.
31. Rothermel E, Gotze O, Zahn S, and Schlaf G. Analysis of the tissue distribution of the rat C5a receptor and inhibition of C5a-mediated effects through the use of two MoAbs. Scand J Immunol 52: 401-410, 2000.
32. Rowinsky EK, Eisenhauer EA, Chaudhry V, Arbuck SG, and Donehower RC. Clinical toxicities encountered with paclitaxel (Taxol). Semin Oncol 20: 1-15, 1993.
33. Rowinsky EK, McGuire WP, and Guarnieri T. Cardiac disturbances during the administration of Taxol. J Clin Oncol 9: 1704-1712, 1991.
34. Rubin LE and Levi R. Protective role of bradykinin in cardiac anaphylaxis. Coronary-vasodilating and antiarrhythmic activities mediated by autocrine/paracrine mechanisms. Circ Res 76: 434-440, 1995.
35. 2 in cardiovascular response to intracoronary C5a. Circ Res 66: 1103-1111, 1990.
36. Stahl GL, Behroozi F, and Morrissey M. Monoclonal antibody, GS1, functionally inhibits porcine C5a induced neutrophil activation, but not C5b-9 formation (Abstract). FASEB J 11: A331, 1997.
37. Stahl GL, Reenstra WR, and Frendl G. Complement-mediated loss of endothelium-dependent relaxation of porcine coronary arteries. Role of terminal membrane attack complex. Circ Res 76: 575-583, 1995.
38. Szebeni J. Complement activation-related pseudoallergy caused by liposomes, micellar carriers of intravenous drugs and radiocontrast agents. Crit Rev Ther Drug Carrier Syst 18: 567-606, 2001.
39. Szebeni J. Complement activation-related pseudoallergy: a new class of drug-induced acute immune toxicity. Toxicology 216: 106-121, 2005.
40. Szebeni J. Complement activation-related pseudoallergy: mechanism of anaphylactoid reactions to drug carriers and radiocontrast agents. In: The Complement System: Novel Roles in Health and Disease, edited by Szebeni J. Boston, MA: Kluwer, 2004, p. 399-440.
41. Szebeni J. The interaction of liposomes with the complement system. Crit Rev Ther Drug Carrier Syst 15: 57-88, 1998.
42. Szebeni J, Alving CR, Savay S, Barenholz Y, Priev A, Danino D, and Talmon Y. Formation of complement-activating particles in aqueous solutions of Taxol: possible role in hypersensitivity reactions. Int Immunopharmacol 1: 721-735, 2001.
43. Szebeni J, Baranyi B, Savay S, Bodo M, Morse DS, Basta M, Stahl GL, Bünger R, and Alving CR. Liposome-induced pulmonary hypertension: properties and mechanism of a complement-mediated pseudoallergic reaction. Am J Physiol Heart Circ Physiol 279: H1319-H1328, 2000.
44. Szebeni J, Baranyi B, Savay S, Lutz LU, Jelezarova E, Bünger R, and Alving CR. The role of complement activation in hypersensitivity to pegylated liposomal doxorubicin (Doxil). J Liposome Res 10: 347-361, 2000.
45. Szebeni J, Baranyi L, Götze O, Alving CR, Bünger R, and Mongan PD. Complement activation during hemorrhagic shock and resuscitation in swine. Shock 20: 347-355, 2003.
46. Szebeni J, Baranyi L, Savay S, Milosevits J, Bodo M, Bünger R, and Alving CR. The interaction of liposomes with the complement system: in vitro and in vivo assays. Methods Enzymol 373: 136-154, 2003.
47. Szebeni J, Fontana JL, Wassef NM, Mongan PD, Morse DS, Dobbins DE, Stahl GL, Bünger R, and Alving CR. Hemodynamic changes induced by liposomes and liposome-encapsulated hemoglobin in pigs: a model for pseudo-allergic cardiopulmonary reactions to liposomes. Role of complement and inhibition by soluble CR1 and anti-C5a antibody. Circulation 99: 2302-2309, 1999.
48. Szebeni J, Muggia FM, and Alving CR. Complement activation by Cremophor EL as a possible contributor to hypersensitivity to paclitaxel: an in vitro study. J Natl Cancer Inst 90: 300-306, 1998.
49. Tibotec Therapeutics. Doxil Product Information. Raritan, NJ: Tibotec, 2005 [http://www.doxil.com/common/prescribing_information/DOXIL/ PDF/DOXIL_PI_Booklet.pdf (25 September 2005)].
50. Tsavaris NB and Kosmas C. Risk of severe acute hypersensitivity reactions after rapid paclitaxel infusion of less than 1-h duration. Cancer Chemother Pharmacol 42: 509-511, 1998.
51. Tuchinda M, Podhipleux P, Vichitbanda P, and Habanananda S. Electrocardiographic study in asthmatic children. Ann Allergy 44: 95-99, 1980.
52. Varga L, Farkas H, and Füst G. Role of complement in allergy. In: The Complement System: Novel Roles in Health and Disease, edited by Szebeni J. Boston, MA: Kluwer, 2004, p. 399-440.
53. Wang D, Shryock JC, and Belardinelli L. Cellular basis for the negative dromotropic effect of adenosine on rabbit single atrioventricular nodal cells. Circ Res 78: 697-706, 1996.