Induction of shock after intravenous injection of adenovirus vectors: A critical role for platelet-activating factor

Molecular Therapy

Volumn 18, Issue 3, 2010, Pages 609-616

  Xu, Zhili ^a   Smith, Jeffrey S ^a   Tian, Jie ^a   Byrnes, Andrew P ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 ETHYNYL 3 [3 FLUORO 4 [(2 METHYL 1H IMIDAZO[4,5 C]PYRIDIN 1 YL)METHYL]BENZOYL] N,N DIMETHYL 1H INDOLE 1 CARBOXAMIDE; ADENOVIRUS VECTOR; DEXAMETHASONE; THROMBOCYTE ACTIVATING FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HEMOCONCENTRATION; HYPOTENSION; IN VIVO STUDY; INNATE IMMUNITY; MALE; MOUSE; NONHUMAN; PROTEIN INDUCTION; RAT; RETICULOENDOTHELIAL SYSTEM; SAFETY; SHOCK; SPECIES DIFFERENCE; SPLENECTOMY; THROMBOCYTOPENIA; UPREGULATION; VIRAL GENE THERAPY;

ADENOVIRIDAE; MUS; RATTUS;

ADENOVIRIDAE; ANIMALS; CYTOKINES; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HUMANS; LIPIDS; MONONUCLEAR PHAGOCYTE SYSTEM; PLATELET ACTIVATING FACTOR; RATS; RATS, SPRAGUE-DAWLEY; SHOCK; SIGNAL TRANSDUCTION; THROMBOCYTOPENIA;

EID: 77649272782     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2009.279     Document Type: Article

References (50)

1. Hartman, ZC, Appledorn, DM and Amalftano, A (2008). Adenovirus vector induced innate immune responses: impact upon effcacy and toxicity in gene therapy and vaccine applications. Virus Res 132: 1-14.
2. Morrissey, RE, Horvath, C, Snyder, EA, Patrick, J and MacDonald, JS (2002). Rodent nonclinical safety evaluation studies of SCH 58500, an adenoviral vector for the p53 gene. Toxicol Sci 65: 266-275. (Pubitemid 34121119)
3. Smith, JS, Tian, J, Lozier, JN and Byrnes, AP (2004). Severe pulmonary pathology after intravenous administration of vectors in cirrhotic rats. Mol Ther 9: 932-941.
4. Smith, JS, Tian, J, Muller, J and Byrnes, AP (2004). Unexpected pulmonary uptake of adenovirus vectors in animals with chronic liver disease. Gene Ther 11: 431-438.
5. Boquet, MP, Wonganan, P, Dekker, JD and Croyle, MA (2008). Infuence of method of systemic administration of adenovirus on virus-mediated toxicity: focus on mortality, virus distribution, and drug metabolism. J Pharmacol Toxicol Methods 58: 222-232.
6. Schiedner, G, Bloch, W, Hertel, S, Johnston, M, Molojavyi, A, Dries, V et al. (2003). A hemodynamic response to intravenous adenovirus vector particles is caused by systemic Kupffer cell-mediated activation of endothelial cells. Hum Gene Ther 14: 1631-1641.
7. Machemer, T, Engler, H, Tsai, V, Lee, S, Cannon-Carlson, S, Voloch, M et al. (2005). Characterization of hemodynamic events following intravascular infusion of recombinant adenovirus reveals possible solutions for mitigating cardiovascular responses. Mol Ther 12: 254-263.
8. Pande, K, Ueda, R, Machemer, T, Sathe, M, Tsai, V, Brin, E et al. (2009). Cancer-induced expansion and activation of CD11b+ Gr-1+ cells predispose mice to adenoviral-triggered anaphylactoid-type reactions. Mol Ther 17: 508-515.
9. Reid, T, Warren, R and Kirn, D (2002). Intravascular adenoviral agents in cancer patients: lessons from clinical trials. Cancer Gene Ther 9: 979-986.
10. Munoz, J and Bergman, RK (1965). Mechanism of anaphylactic death in the mouse. Nature 205: 199-200.
11. Morrissey, RE, Horvath, C, Snyder, EA, Patrick, J, Collins, N, Evans, E et al. (2002). Porcine toxicology studies of SCH 58500, an adenoviral vector for the p53 gene. Toxicol Sci 65: 256-265. (Pubitemid 34121118)
12. Strait, RT, Morris, SC, Yang, M, Qu, XW and Finkelman, FD (2002). Pathways of anaphylaxis in the mouse. J Allergy Clin Immunol 109: 658-668.
13. Sanchez Crespo, M, Inarrea, P, Nieto, ML and Fernandez-Gallardo, S (1986). Evidence of a role for PAF-acether in the pathophysiology of the shock state. Pharmacol Res Commun 18 Suppl: 181-196.
14. Jenei, B, Lázár, G, Bartha, K and Medgyesi, GA (1991). Hypotensive action of IgG preparations containing aggregates is suppressed by PAF-receptor antagonist BN 52021 and by gadolinium chloride (an agent blocking Kupffer cell function). Agents Actions 32: 333-338.
15. Klabunde, RE and Anderson, DE (2000). Obligatory role of nitric oxide in platelet-activating factor-induced microvascular leakage. Eur J Pharmacol 404: 387-394.
16. Montrucchio, G, Alloatti, G and Camussi, G (2000). Role of platelet-activating factor in cardiovascular pathophysiology. Physiol Rev 80: 1669-1699.
17. Stafforini, DM, McIntyre, TM, Zimmerman, GA and Prescott, SM (2003). Platelet-activating factor, a pleiotrophic mediator of physiological and pathological processes. Crit Rev Clin Lab Sci 40: 643-672.
18. Vadas, P, Gold, M, Perelman, B, Liss, GM, Lack, G, Blyth, T et al. (2008). Platelet-activating factor, PAF acetylhydrolase, and severe anaphylaxis. N Engl J Med 358: 28-35.
19. Albert, DH, Magoc, TJ, Tapang, P, Luo, G, Morgan, DW, Curtin, M et al. (1997). Pharmacology of ABT-491, a highly potent platelet-activating factor receptor antagonist. Eur J Pharmacol 325: 69-80.
20. Terashita, Z, Imura, Y, Takatani, M, Tsushima, S and Nishikawa, K (1987). CV-6209, a highly potent antagonist of platelet activating factor in vitro and in vivo. J Pharmacol Exp Ther 242: 263-268.
21. Rosam, AC, Wallace, JL and Whittle, BJ (1986). Potent ulcerogenic actions of platelet-activating factor on the stomach. Nature 319: 54-56.
22. Pellón, MI, Steil, AA, Furió, V and Sánchez Crespo, M (1994). Study of the effector mechanism involved in the production of haemorrhagic necrosis of the small intestine in rat passive anaphylaxis. Br J Pharmacol 112: 1101-1108.
23. Udaka, K, Takeuchi, Y and Movat, HZ (1970). Simple method for quantitation of enhanced vascular permeability. Proc Soc Exp Biol Med 133: 1384-1387.
24. Sirois, MG, Jancar, S, Braquet, P, Plante, GE and Sirois, P (1988). PAF increases vascular permeability in selected tissues: effect of BN-52021 and L-655,240. Prostaglandins 36: 631-644.
25. Manickan, E, Smith, JS, Tian, J, Eggerman, TL, Lozier, JN, Muller, J et al. (2006). Rapid Kupffer cell death after intravenous injection of adenovirus vectors. Mol Ther 13: 108-117.
26. Chao, W, Siafaka-Kapadai, A, Olson, MS and Hanahan, DJ (1989). Biosynthesis of platelet-activating factor by cultured rat Kupffer cells stimulated with calcium ionophore A23187. Biochem J 257: 823-829.
27. Abu-Zidan, FM and Windsor, JA (2002). Lexipafant and acute pancreatitis: a critical appraisal of the clinical trials. Eur J Surg 168: 215-219.
28. Young, JM, Maloney, PJ, Jubb, SN and Clark, JS (1985). Pharmacological investigation of the mechanisms of platelet-activating factor induced mortality in the mouse. Prostaglandins 30: 545-551.
29. Wallace, JL and Whittle, BJ (1986). Effects of inhibitors of arachidonic acid metabolism on Paf-induced gastric mucosal necrosis and haemoconcentration. Br J Pharmacol 89: 415-422.
30. De Geest, B, Snoeys, J, Van Linthout, S, Lievens, J and Collen, D (2005). Elimination of innate immune responses and liver infammation by PEGylation of adenoviral vectors and methylprednisolone. Hum Gene Ther 16: 1439-1451.
31. Seregin, SS, Appledorn, DM, McBride, AJ, Schuldt, NJ, Aldhamen, YA, Voss, T et al. (2009). Transient pretreatment with glucocorticoid ablates innate toxicity of systemically delivered adenoviral vectors without reducing effcacy. Mol Ther 17: 685-696.
32. Brunetti-Pierri, N, Palmer, DJ, Beaudet, AL, Carey, KD, Finegold, M and Ng, P (2004). Acute toxicity after high-dose systemic injection of helper-dependent adenoviral vectors into nonhuman primates. Hum Gene Ther 15: 35-46.
33. Stone, D, Liu, Y, Li, ZY, Tuve, S, Strauss, R and Lieber, A (2007). Comparison of adenoviruses from species B, C, E, and F after intravenous delivery. Mol Ther 15: 2146-2153.
34. Hartman, ZC, Appledorn, DM, Serra, D, Glass, O, Mendelson, TB, Clay, TM et al. (2008). Replication-attenuated Human Adenoviral Type 4 vectors elicit capsid dependent enhanced innate immune responses that are partially dependent upon interactions with the complement system. Virology 374: 453-467.
35. Appledorn, DM, Kiang, A, McBride, A, Jiang, H, Seregin, S, Scott, JM et al. (2008). Wild-type adenoviruses from groups A-F evoke unique innate immune responses, of which HAd3 and SAd23 are partially complement dependent. Gene Ther 15: 885-901.
36. Garcia-Bañuelos, J, Siller-Lopez, F, Miranda, A, Aguilar, LK, Aguilar-Cordova, E and Armendariz-Borunda, J (2002). Cirrhotic rat livers with extensive fbrosis can be safely transduced with clinical-grade adenoviral vectors. Evidence of cirrhosis reversion. Gene Ther 9: 127-134.
37. Toietta, G, Mane, V P, Norona, WS, Finegold, MJ, Ng, P, McDonagh, AF et al. (2005). Lifelong elimination of hyperbilirubinemia in the Gunn rat with a single injection of helper-dependent adenoviral vector. Proc Natl Acad Sci USA 102: 3930-3935.
38. Billiar, TR, West, MA, Hyland, BJ and Simmons, RL (1988). Splenectomy alters Kupffer cell response to endotoxin. Arch Surg 123: 327-332.
39. Mizukami, T, Yokoyama, H, Okamura, Y, Ohgo, H, Fukuda, M, Kamegaya, Y et al. (1999). Splenectomy attenuates superoxide anion release into the hepatic sinusoids after lipopolysaccharide challenge. J Hepatol 31: 235-241. (Pubitemid 29349748)
40. Sánchez-Crespo, M, Alonso, F, Iñarrea, P, Alvarez, V and Egido, J (1982). Vascular actions of synthetic PAF-acether (a synthetic platelet-activating factor) in the rat: evidence for a platelet independent mechanism. Immunopharmacology 4: 173-185.
41. Souza, DG, Fagundes, CT, Sousa, LP, Amaral, FA, Souza, RS, Souza, AL et al. (2009). Essential role of platelet-activating factor receptor in the pathogenesis of Dengue virus infection. Proc Natl Acad Sci USA 106: 14138-14143.
42. Namm, DH, Tadepalli, AS and High, JA (1982). Species specifcity of the platelet responses to 1-0-alkyl-2-acetyl-sn-glycero-3-phosphocholine. Thromb Res 25: 341-350.
43. McManus, LM, Pinckard, RN, Fitzpatrick, FA, O'Rourke, RA, Crawford, MH and Hanahan, DJ (1981). Acetyl glyceryl ether phosphorylcholine. Intravascular alterations following intravenous infusion into the baboon. Lab Invest 45: 303-307.
44. Okamoto, M, Yoshida, K, Nishikawa, M, Kohsaka, M and Aoki, H (1986). Platelet activating factor (PAF) involvement in endotoxin-induced thrombocytopenia in rabbits: studies with FR-900452, a specifc inhibitor of PAF. Thromb Res 42: 661-671.
45. Chen, XS, Sheller, JR, Johnson, EN and Funk, CD (1994). Role of leukotrienes revealed by targeted disruption of the 5-lipoxygenase gene. Nature 372: 179-182.
46. Smith, JS, Xu, Z and Byrnes, AP (2008). A quantitative assay for measuring clearance of adenovirus vectors by Kupffer cells. J Virol Methods 147: 54-60. (Pubitemid 350250848)
47. Feng, M, Whitesall, S, Zhang, Y, Beibel, M, D'Alecy, L and DiPetrillo, K (2008). Validation of volume-pressure recording tail-cuff blood pressure measurements. Am J Hypertens 21: 1288-1291.
48. Chang, SW, Feddersen, CO, Henson, PM and Voelkel, NF (1987). Platelet-activating factor mediates hemodynamic changes and lung injury in endotoxin-treated rats. J Clin Invest 79: 1498-1509.
49. Souza, DG, Pinho, V, Soares, AC, Shimizu, T, Ishii, S and Teixeira, MM (2003). Role of PAF receptors during intestinal ischemia and reperfusion injury. A comparative study between PAF receptor-defcient mice and PAF receptor antagonist treatment. Br J Pharmacol 139: 733-740.
50. Van Rooijen, N and Sanders, A (1994). Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods 174: 83-93.