Immunomodulatory effects in the spleen-injured mice following exposure to titanium dioxide nanoparticles

Journal of Biomedical Materials Research - Part A

Volumn 102, Issue 10, 2014, Pages 3562-3572

  Sang, Xuezi ^a   Fei, Min ^a   Sheng, Lei ^a   Zhao, Xiaoyang ^a   Yu, Xiaohong ^a   Hong, Jie ^a   Ze, Yuguan ^a   Gui, Suxin ^a   Sun, Qingqing ^a   Ze, Xiao ^a   Wang, Ling ^a   Hong, Fashui ^a,b,c  

^a MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

^b SOOCHOW UNIVERSITY   (China)

^c State Key Laboratory of Stem Cell and Biomaterials Ministry of Science and Technology   (China)

Author keywords

immunomodulation; immunotoxicity; mice; spleen injury; titanium dioxide nanoparticles

Indexed keywords

AMINO ACIDS; ANTIBIOTICS; CELL DEATH; GLYCOPROTEINS; MACROPHAGES; MAMMALS; NANOPARTICLES; OXIDES; PROTEINS;

IMMUNO MODULATIONS; IMMUNOTOXICITY; MICE; SPLEEN INJURY; TITANIUM DIOXIDE NANOPARTICLES;

TITANIUM DIOXIDE;

CD69 ANTIGEN; EOTAXIN; FAS LIGAND; FIBROBLAST GROWTH FACTOR 2; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANZYME B; INTERLEUKIN 13; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 2; MIGRATION INHIBITION FACTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL KILLER CELL RECEPTOR; NATURAL KILLER CELL RECEPTOR 2B4; NATURAL KILLER CELL RECEPTOR NKG2D; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE 1; PROTEIN TYROSINE PHOSPHATASE; TITANIUM DIOXIDE NANOPARTICLE; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; AUTACOID; CHEMOKINE; IMMUNOLOGIC FACTOR; MESSENGER RNA; NANOPARTICLE; TITANIUM; TITANIUM DIOXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; FEMALE; HISTOPATHOLOGY; IMMUNE INJURY; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOTOXICITY; LYMPHOCYTIC INFILTRATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SPLEEN; SPLEEN CELL; SPLEEN INJURY; THYMUS; ANIMAL; ANTIBODY SPECIFICITY; BODY WEIGHT; CHEMISTRY; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INJURIES; METABOLISM; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; APOPTOSIS; BODY WEIGHT; CHEMOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION REGULATION; IMMUNOLOGIC FACTORS; INFLAMMATION MEDIATORS; MICE; NANOPARTICLES; ORGAN SPECIFICITY; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPLEEN; TITANIUM;

EID: 84906783859     PISSN: 15493296     EISSN: 15524965     Source Type: Journal    
DOI: 10.1002/jbm.a.35034     Document Type: Article

References (84)

1. Moghimi SM, Hunter AC, Murray JC,. Nanomedicine: Current status and future prospects. J FASEB 2005; 19: 311-330.
2. Chen XB, Mao SS,. Titanium dioxide nanomaterials: Synthesis, properties, modifications, and applications. Chem Rev 2007; 107: 2891-2959.
3. Zhang XT, Jin M, Liu ZY, Tryk DA, Nishimoto S, Murakami T, Fujishima A,. Superhydrophobic TiO2 surfaces: Preparation, photocatalytic wettability conversion, and superhydrophobic-superhydrophilic patterning. J Phys Chem C 2007; 111: 14521-14529.
4. Ashkarran AA, Mohammadizadeh MR,. Superhydrophilicity of TiO2 thin films using TiCl4 as a precursor. Mater Res Bull 2008; 43: 522-530.
5. EPA US. Nanomaterial Case Studies: Nanoscale Titanium Dioxide in Water Treatment and in Topical Sunscreen (Final). Washington, DC: U.S. Environmental Protection Agency, EPA/600/R-09/057F, 2010.
6. Lee DJ, Senseman SA, Sciumbato AS, Jung SC, Krutz LJ,. The Effect of titanium dioxide alumina beads on the photocatalytic degradation of picloram in water. J Agric Food Chem 2003; 51: 2659-2664.
7. Chan, EPH, Mhawi, A, Clode, P, Saunders, M, Filgueira, L,. Effects of titanium (iv) ions on human monocyte-derived dendritic cells. Metallomics 2009; 1: 166-174.
8. Prombutara P, Kulwatthanasal Y, Supaka N, Sramala I, Chareonpornwattana S,. Production of nisin-loaded solid lipid nanoparticles for sustained antimicrobial activity. Food Control 2012; 24: 184-190.
9. Ortlieb, M,. White giant or white dwarf? Particle size distribution measurements of TiO2. GIT Lab J Eur 2010; 14: 42-43.
10. Sanvicens N, Marco MP,. Multifunctional nanoparticles-properties and prospects for their use in human medicine. J Trends Biotechnol 2008; 26: 425-433.
11. Luft, JR, Furlani, NM, NeMoyer, RE, Penna, EJ, Wolfley, JR, Snell, ME, Potter, SA, Snell, EH,. Crystal cookery-using high-throughput technologies and the grocery store as a teaching tool. J Appl Crystallog 2010; 43: 1189-1207.
12. Sadrieh N, Wokovich AM, Gopee NV, Zheng J, Haines D, Parmiter D, Siitonen PH, Cozart CR, Patri AK, McNeil SE, Howard PC, Doub WH, Buhse LF,. Lack of significant dermal penetration of titanium dioxide from sunscreen formulations containing nano- and submicron-size TiO2 particles. Toxicol Sci 2010; 115: 156-66.
13. Jovanovic̈ B, Palic̈ D,. Immunotoxicology of non-functionalized engineered nanoparticles in aquatic organisms with special emphasis on fish-Review of current knowledge, gap identification, and call for further research. Aquatic Toxicol 2012; 118-119: 141-151.
14. Iavicoli I, Leso V, Bergamaschi A,. Toxicological effects of titanium dioxide nanoparticles: A review of in vivo studies. J Nanomaterials 2012; 1-36.
15. Zhou L, Yang WX,. Nanoparticles and spermatogenesis: How do nanoparticles affect spermatogenesis and penetrate the blood-testis barrier. Nanomedicine 2012; 7: 579-596.
16. Shi HB, Magaye RT, Castranova V, Zhao JS,. Titanium dioxide nanoparticles: A review of current toxicological data. Part Fibre Toxicol 2013; 10: 15.
17. Gui SX, Sang XZ, Zheng L, Ze YG, Zhao XY, Sheng L, Sun QQ, Cheng Z, Cheng J, Hu RP, Wang L, Hong FS, Tang M,. Intragastric exposure to titanium dioxide nanoparticles induced nephrotoxicity in mice, assessed by physiological and gene expression modifications. Part Fibre Toxicol 2013; 10: 4.
18. Gui SX, Li BY, Zhao XY, Sheng L, Hong J, Yu XH, Sang XZ, Sun QQ, Ze YG, Wang L, Hong FS,. Renal injury and Nrf2 modulation in mouse kidney following exposure to titanium dioxide nanoparticles. J Agric Food Chem, dx.doi.org/10.1021/jf402387e.
19. Li B, Ze YG, Sun QQ, Zhang T, Sang XZ, Cui YL, Wang XC, Gui SX, Tan DL, Zhu M, Zhao XY, Sheng L, Wang L, Hong FS, Tang M,. Molecular mechanisms of nanosized titanium dioxide-induced pulmonary injury in mice. Plos One 2013; 8: e55563.
20. Gao GD, Ze YG, Li B, Zhao XY, Zhang T, Sheng L, Hu RP, Gui SX, Sang XZ, Sun QQ, Cheng J, Cheng Z, Wang L, Tang M, Hong FS,. Ovarian dysfunction and gene-expressed characteristics of female mice caused by long-term exposure to titanium dioxide nanoparticles. J Hazard Mater 2012; 243: 19-27.
21. Zhao XY, Ze YG, Li B, Zhang T, Gui SX, Sang XZ, Sheng L, Sun QQ, Wang L, Tang M, Hong FS,. Nanosized TiO2-induced reproductive system dysfunction and its mechanism in female mice. Plos One 2013; 8: 59378.
22. Gao GD, Ze YG, Zhao XY, Sang XZ, Zheng L, Ze X, Gui SX, Sheng L, Sun QQ, Hong J, Yu XH, Wang L, Hong FS, Zhang XG,. Titanium dioxide nanoparticle-induced testicular damage, spermatogenesis suppression, and gene expression alterations in male mice. J Hazard Mater 2013; 258-259: 133-143.
23. Ze YG, Zheng L, Zhao XY, Gui SX, Sang XZ, Su JJ, Guan N, Zhu LY, Sheng L, Hu RP, Cheng J, Cheng Z, Sun QQ, Wang L, Hong FS,. Molecular mechanism of titanium dioxide nanoparticles-induced oxidative injury in the brain of mice. Chemosphere 2013; 92: 1183-1189.
24. Wluka A, Olszewski WL,. Innate and adaptive processes in the spleen. Ann Transplant 2006; 11: 22-29.
25. Chen JY, Dong X, Zhao J, Tang GP,. In vivo acute toxicity of titanium dioxide nanoparticles to mice after intraperitoneal injection. Appl Toxicol 2009; 29: 330-337.
26. Wang J, Li N, Zheng L, Wang Y, Duan YM, Wang SS, Zhao XY, Cui YL, Zhou M, Cai JW, Gong SJ, Wang H, Hong FS,. P38-Nrf-2 signaling pathway of oxidative stress in mice caused by nanoparticulate TiO2. Biol Trace Elem Res 2011; 140: 186-197.
27. Li N, Duan YM, Hong MM, Zheng L, Fei M, Zhao XY, Wang Y, Cui YL, Liu HT, Cai JW, Gong SJ, Wang H, Hong FS,. Spleen injury and apoptotic pathway in mice caused bytitanium dioxide nanoparticules. Toxicol Lett 2010; 195: 161-168.
28. Sang XZ, Zheng L, Sun QQ, Li N, Cui YL, Hu RP, Gao GD, Cheng Z, Cheng J, Gui SX, Liu HT, Zhang ZL, Hong FS,. The chronic spleen injury of mice following long-period exposure to titanium dioxide nanoparticles. J Biomed Mater Res A 2012; 100A: 894-902.
29. Sang XZ, Li B, Ze YG, H J, Ze, X, Gui, SX, Sun, QQ, Liu, HT, Zhao, XY, Sheng, L, Liu, D, Yu, XH, Wang, L, Hong, FS,. Toxicological mechanisms of nanosized titanium dioxide-induced spleen injury in mice after repeated peroral application. J Agric Food Chem 2013; 61: 5590-5599.
30. Yang P, Lu C, Hua N, Du Y,. Titanium dioxide nanoparticles co-doped with Fe3+ and Eu3+ ions for photocatalysis. Mater Lett 2002; 57: 794-801.
31. Hu RP, Zheng L, Zhang T, Cui YL, Gao GD, Cheng Z, Chen J, Tang M, Hong FS,. Molecular mechanism of hippocampal apoptosis of mice following exposure to titanium dioxide nanoparticles. J Hazard Mater 2011; 191: 32-40.
32. Zhang WF, He YL, Zhang MS, Yin Z, Chen Q,. Raman scattering study on anatase TiO2 nanocrystals. J Phys D: Appl Phys 2000; 33: 912-91.
33. Ke LD, Chen Z,. A reliability test of standard-based quantitative PCR: Exogenous vs endogenous standards. Mol Cell Probes 2000; 4: 127-135.
34. Liu WH, Saint DA,. Validation of a quantitative method for real time PCR kinetics. Biochem Biophys Res Commun 2002; 294: 347-353.
35. Livak KJ, Schmittgen TD,. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001; 25: 402-408.
36. Zou LP, Pelidou SH, Abbas N, Deretzi G, Mix E, Schaltzbeerg M, Winblad B, Zhu J,. Dynamics of production of MIP-1a, MCP-1 and MIP-2 and potential role of neutralization of these chemokines in the regulation of immune responses during experimental autoimmune neuritis in Lewis rats. J Neuroimmunol 1999; 98: 168-175.
37. Lentzsch S, Gries M, Janz M, Bargou R, Dörken B, Mapara MY,. Macrophage inflammatory protein 1-alpha (MIP-1α) triggers migration and signaling cascades mediating survival and proliferation in multiple myeloma (MM) cells. Blood 2003; 101: 9:3568-3573.
38. Fuller K, Owens JM, Chambers TJ,. Macrophage inflammatory protein-1 alpha and IL-8 stimulate the motility but suppress the resorption of isolated rat osteoclasts. J Immunol 1995; 154: 6065-6072.
39. Schall TJ, Bacon K, Camp RD, Kaspari JW., and, Goeddel DV., Human macrophage inflammatory protein alpha(MIP-1 alpha)and MIP-1 betachemokines attract distinct populations of lymphocytes. J Exp Med 1993; 177: 1821-1826.
40. Kim C, Pelus M, White J, Appelbaum E, Johanson K, and, Broxmeyer H,. CKβ-11/Macrophage inflammatory protein-3β/EBI1-ligand chemokine is an efficacious chemoattractant for T and B Cells. J Immunol 1998; 160: 2418-2424.
41. Lei X, Hossain M, M., Qadri S, Liu L,. Different microvascular permeability responses elicited by the CXC chemokines MIP-2 and KC during leukocyte recruitment: Role of LSP1. Biochem Biophys Res Commun 2012; 423: 484-489.
42. Griffiths-Johnson DA, Collins PD, Rossi AG, Jose PJ, Williams TJ,. The chemokine, eotaxin, activates guinea-pig eosinophils in vitro, and causes their accumulation into the lung in vivo. Biochem Biophys Res Commun 1993; 197: 1167-1172.
43. Jose PJ, Griffiths-Johnson DA, Collins PD, Walsh DT, Moqbel R, Totty NF, Truong O, Hsuan JJ, Williams TJ,. Eotaxin: A potent eosinophil chemoattractant cytokine detected in a guinea-pig model of allergic airways inflammation. J Exp Med 1994; 179: 881-887.
44. Charo IF, Taubman MB,. Chemokines in the pathogenesis of vascular disease. Circ Res 2004; 95: 858-66.
45. Qi Yf, Liang J, She ZG, Cai Y, Wang J, Lei TH, Stallcup WB, Fu MG,. MCP-induced protein 1 suppresses TNF-α-induced VCAM-1 expression in human endothelial cells. FEBS Lett 2010; 584: 3065-3072.
46. Liu K, Chi DS, Li CF, Kenton Hall H, Milhorn DM, Krishnaswamy G,. HIV-1 Tat protein-induced VCAM-1 expression in human pulmonary artery endothelial cells and its signaling. Am J Physiol Lung Cell Mol Physiol 2005; 289: L252-L260.
47. Rankin SM, Conroy DM, Williams TJ,. Eotaxin and eosinophil recruitment: Implications for human disease. Mol Med Today 2000; 6: 20-27.
48. Doucet C, Brouty-Boye D, Pottin-Clemenceau C, Canonica GW, Jasmin C, Azzarone B,. Interleukin (IL) 4 and IL-13 act on human lung fibroblasts. Implication in asthma. J Clin Invest 1998; 101: 2129-39.
49. Ono SJ, Nakamura T, Miyazaki D, Ohbayashi M, Dawson M, Toda M,. Chemokines. roles in leukocyte development, trafficking, and effector function. J Allergy Clin Immunol 2003; 111: 1185-1199.
50. David M, Jonathan B, David R, Ivan R,. Immunology, 8th ed, Amsterdam: Elsevier; 2012, p 1-488.
51. Cabrera-Vera TM, Vanhauwe J, Thomas TO, Medkova M, Preininger A, Mazzoni MR,. Insights into G protein structure, function, and regulation. Endocr Rev 2003; 24: 765-781.
52. Liu M, Guo S, Hibbert JM, Jain V, Singh N, Wilson NO, Stiles JK,. CXCL10/IP-10 in infectious diseases pathogenesis and potential therapeutic implications. Cytokine Growth Factor Rev 2011; 22: 121-130.
53. Rowe T, Leõn AJ, Crevar CJ, Carter DM, Xu L, Ran L, Fang Y, Cameron CM, Cameron MJ, Banner D, Ng DC, Ran R, Weirback HK, Wiley CA, Kelvin DJ, Ross TM,. Modeling host responses in ferrets during A/California/07/2009 influenza infection. J Virol 2010; 401: 257-65.
54. Cameron MJ, Ran L, Xu L, Danesh A, Bermejo-Martin JF, Cameron CM, Muller MP, Gold WL, Richardson SE, Poutanen SM, Willey BM, DeVries ME, Fang Y, Seneviratne C, Bosinger SE, Persad D, Wilkinson P, Greller LD, Somogyi R, Humar A, Keshavjee S, Louie M, Loeb MB, Brunton J, McGeer AJ,; Canadian SARS Research Network, Kelvin DJ,. Interferon-mediated immunopathological events are associated with atypical innate and adaptive immune responses in patients with severe acute respiratory syndrome. J Virol 2007; 81: 8692-706.
55. Bosinger SE, Hosiawa KA, Cameron MJ, Persad D, Ran L, Xu L, Boulassel MR, Parenteau M, Fournier J, Rud EW, Kelvin DJ,. Gene expression profiling of host response in models of acute HIV infection. J Immunol 2004; 173: 6858-63.
56. Lolis E,. Glucocorticoid counter regulation: Macrophage migration inhibitory factor as a target for drug discovery. Curr Opin Pharmacol 2001; 1: 662-66.
57. T, Roger, T,. Macrophage migration inhibitory factor: A regulator of innate immunity. Nat Rev Immunol 2003; 3: 791-800.
58. Lue H, Kleemann R, Calandra T, Roger T, Bernhagen J,. Macrophage migration inhibitory factor (MIF): Mechanisms of action andm role in disease. Microb Infect 2002; 4: 449-460.
59. Morand EF, Leech M, Bernhagen J,. MIF: A new cytokine link between rheumatoid arthritis and atherosclerosis. Nat Rev Drug Discov 2006; 5: 399-410.
60. Zernecke A, Bernhagen J, Weber C,. Macrophage migration inhibitory factor in cardiovascular disease. Circulation 2008; 117: 1594-1602.
61. Morgan CD, Greene JF, Measel JW,. Induction of surface antigen CD69 expression in T- lymphocytes following exposure to actinomycin D. Int J Immunopharmacol 1999; 21: 689-703.
62. Ishizaki S, Kasuya Y, Kuroda F, Tanaka K, Tsuyusaki J, Yamauchi K, Matsunaga H, Iwamura C, Nakayama T, Tatsumi K,. Role of CD69 in acute lung injury. Life Sci 2012; 90: 657-665.
63. Ishikawa C, Kawakami H, Uchihara JN, Senba M, Mori N,. CD69 overexpression by human T-cell leukemia virus type 1 Tax transactivation. Biochim Biophys Acta 2013; 1833: 1542-1552.
64. Holling TM, Schooten E, van Den Elsen PJ,. Function and Regulation of MHC Class II Molecules in T-Lymphocytes: Of Mice and Men. J Hum Immunol 2004; 65: 282-290.
65. Maenaka K, Jones EY,. MHC superfamily structure and the immune system. Curr Opin Struct Biol 1999; 9: 745-53.
66. Grossmann ME, Wood M, Celis E,. Expression, specificity and immunotherapy potential of prostate-associated genes in murine cell lines. World J Urol 2001; 19: 365-70.
67. Di Santo JP,. Natural killer cell developmental pathways: A question of balance. Annu Rev Immunol 2006; 24: 257-286.
68. Pegram HJ, Andrews DM, Smyth MJ, Darcy PK, Kershaw MH,. Activating and inhibitory receptors of natural killer cells. Immunol Cell Biol 2011; 89: 216-24.
69. Watzl C,. The NKG2D receptor and its ligands-recognition beyond the "missing self"? Microbes Infect 2003; 5: 31-7.
70. Obeidy P, Sharland AF,. The NKG2D and its ligands. Int J Biochem Cell Biol 2009; 41: 2364-2367.
71. Bottino C, Biassoni R, Millo R, Moretta L, Moretta A,. The human natural cytotoxicity receptors (NCR) that induce HLA class I independent NK cell triggering. Hum Immunol 2000; 61: 1-6.
72. Mandelboim O, Lieberman N, Lev M, Paul L, Arnon TI, Bushkin Y, Davis DM, Strominger JL, Yewdell JW, Porgador A,. Sialic acid-based binding of NKp46 to viral hemagglutinins activates lysis by human natural killer cells. Nature 2001; 409: 1055-1060.
73. Vaidya SV, Stepp SE, McNerney ME, Lee JK, Bennett M, Lee KM, Stewart CL, Kumar V, Mathew PA,. Targeted disruption of the 2B4 gene in mice reveals an in vivo role of 2B4 (CD244) in the rejection of B16 melanoma cells. J Immunol 2005; 174: 800-807.
74. Lee KM, McNerney ME, Stepp SE, Mathew PA, Schatzle JD, Bennett M, Kumar V,. 2B4 acts as a non-major histocompatibility complex binding inhibitory receptor on mouse natural killer cells. J Exp Med 2004; 199: 1245-1254.
75. Tibbles LA, Ing YL, Kiefer F, Chan J, Iscove N, Woodgett JR, Lassam NJ,. MLK-3 activates the SAPK/JNK and p38/RK pathways via SEK1 and MKK3/6. J EMBO 1996; 15: 7026-35.
76. Andersen JN, Mortensen OH,. Structural and evolutionary relationships among protein tyrosine phosphatase domains. J Mol Cell Biol 2001; 21: 711727136.
77. Tiganis T, Bennett AM,. Protein tyrosine phosphatase function: The substrate perspective. J Biochem 2007; 402: 1-15.
78. Wang, X, Lin, G, Martins-Taylor, K, Zeng, H, Xu, RH, Inhibition of caspase-mediated anoikis is critical for basic fibroblast growth factor-sustained culture of human pluripotent stem cells. J Biol Chem 2009; 284: 34054-34064.
79. House SL, Bolte C, Zhou M, Doetschman T, Klevitsky R, Newman G, Schultz Jel J,. Cardiac-specific overexpression of fibroblast growth factor-2 protects against myocardial dysfunction and infarction in a murine model of low-flow ischemia. Circulation 2003; 108: 3140-3148.
80. Barrientos S, Stojadinovic O, Golinko MS, Brem H, TomicCanic M,. Growth factors and cytokines in wound healing. Wound Repair Regen 2008; 16: 585-601.
81. Kerr JF, Wyllie AH, Currie AR,. Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972; 26: 239-57.
82. Russell JH, Ley TJ,. Lymphocyte-mediated cytotoxicity. Annu Rev Immunol 2002; 20: 323-70.
83. Goping IS, Barry M, Liston P, Sawchuk T, Constantinescu G, Michalak KM, Shostak I, Roberts DL, Hunter AM, Korneluk R, and, Bleackley RC,. Granzyme B-induced apoptosis requires both direct caspase activation and relief of caspase inhibition. Immunity 2003; 18: 355-365.
84. Pardo J, Bosque A, Brehm R, Wallich R, Naval J, Müllbacher A, Anel A, Simon MM,. Apoptotic pathways are selectively activated by granzyme A and/or granzyme B in CTL-mediated target cell lysis. J Cell Biol 2004; 167: 457-68.