Identification and characterization of infiltrating macrophages in acetaminophen-induced liver injury

Journal of Leukocyte Biology

Volumn 84, Issue 6, 2008, Pages 1410-1421

  Holt, Michael P ^a   Cheng, Linling ^a   Ju, Cynthia ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Apoptosis; Inflammation; Monocyte; Neutrophil; Phagocytosis

Indexed keywords

PARACETAMOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INFILTRATION; CELL ISOLATION; CELL POPULATION; CELL SURFACE; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; IN VITRO STUDY; LIVER INJURY; MACROPHAGE; MALE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL;

ACETAMINOPHEN; ANALGESICS, NON-NARCOTIC; ANIMALS; APOPTOSIS; BONE MARROW; FEMALE; FLOW CYTOMETRY; HUMANS; JURKAT CELLS; LIVER; MACROPHAGES; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; NECROSIS; PHAGOCYTOSIS; PHENOTYPE; RECEPTORS, CCR2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

MUS;

EID: 57149108312     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0308173     Document Type: Article

References (98)

1. Hartleb, M., Biernat, L., Kochel, A. (2002) Drug-induced liver damage - a three-year study of patients from one gastroenterological department. Med. Sci. Monit. 8, CR292-CR296.
2. Lazarou, J., Pomeranz, B. H., Corey, P. N. (1998) Incidence of adverse drug reactions in hospitalized patients: a meta-analysis of prospective studies. JAMA 279, 1200-1205.
3. Lazerow, S. K., Abdi, M. S., Lewis, J. H. (2005) Drug-induced liver disease 2004. Curr. Opin. Gastroenterol. 21, 283-292.
4. Lee, W. M., Senior, J. R. (2005) Recognizing drug-induced liver injury: current problems, possible solutions. Toxicol. Pathol. 33, 155-164.
5. Lee, W. M. (2003) Drug-induced hepatotoxicity. N. Engl. J. Med. 349, 474-485.
6. Larson, A. M., Polson, J., Fontana, R. J., Davern, T. J., Lalani, E., Hynan, L. S., Reisch, J. S., Schiodt, F. V., Ostapowicz, G., Shakil, A. O., Lee, W. M., Acute Liver Failure Study Group (2005) Acetaminophen-induced acute liver failure: results of a United States multicenter, prospective study. Hepatology 42, 1364-1372.
7. Nelson, S. D. (1995) Mechanisms of the formation and disposition of reactive metabolites that can cause acute liver injury. Drug Metab. Rev. 27, 147-177.
8. Pumford, N. R., Halmes, N. C., Hinson, J. A. (1997) Covalent binding of xenobiotics to specific proteins in the liver. Drug Metab. Rev. 29, 39-57.
9. Lee, S. S., Buters, J. T., Pineau, T., Fernandez-Salguero, P., Gonzalez, F. J. (1996) Role of CYP2E1 in the hepatotoxicity of acetaminophen. J. Biol. Chem. 271, 12063-12067.
10. Liu, Z. X., Govindarajan, S., Kaplowitz, N. (2004) Innate immune system plays a critical role in determining the progression and severity of acetaminophen hepatotoxicity. Gastroenterology 127, 1760-1774.
11. Liu, Z. X., Han, D., Gunawan, B., Kaplowitz, N. (2006) Neutrophil depletion protects against murine acetaminophen hepatotoxicity. Hepatology 43, 1220-1230.
12. Liu, Z. X., Kaplowitz, N. (2002) Immune-mediated drug-induced liver disease. Clin. Liver Dis. 6, 755-774.
13. Ishida, Y., Kondo, T., Kimura, A., Tsuneyama, K., Takayasu, T., Mukaida, N. (2006) Opposite roles of neutrophils and macrophages in the pathogenesis of acetaminophen-induced acute liver injury. Eur. J. Immunol. 36, 1028-1038.
14. Michael, S. L., Pumford, N. R., Mayeux, P. R., Niesman, M. R., Hinson, J. A. (1999) Pretreatment of mice with macrophage inactivators decreases acetaminophen hepatotoxicity and the formation of reactive oxygen and nitrogen species. Hepatology 30, 186-195.
15. Laskin, D. L., Gardner, C. R., Price, V. F., Jollow, D. J. (1995) Modulation of macrophage functioning abrogates the acute hepatotoxicity of acetaminophen. Hepatology 21, 1045-1050.
16. Ju, C., Reilly, T. P., Bourdi, M., Radonovich, M. F., Brady, J. N., George, J. W., Pohl, L. R. (2002) Protective role of Kupffer cells in acetaminophen-induced hepatic injury in mice. Chem. Res. Toxicol. 15, 1504-1513.
17. Geissmann, F., Jung, S., Littman, D. R. (2003) Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19, 71-82.
18. Stout, R. D., Suttles, J. (1997) T cell signaling of macrophage function in inflammatory disease. Front. Biosci. 2, d197-d206.
19. Gordon, S. (2003) Alternative activation of macrophages. Nat. Rev. Immunol. 3, 23-35.
20. Stout, R. D., Suttles, J. (1995) T cell signaling of macrophage activation. In Cell Contact-Dependent and Cytokine Signals (R. G. Landes, ed.), Austin, TX, USA, Springer-Verlag.
21. Goerdt, S., Politz, O., Schledzewski, K., Birk, R., Gratchev, A., Guillot, P., Hakiy, N., Klemke, C. D., Dippel, E., Kodelja, V., Orfanos, C. E. (1999) Alternative versus classical activation of macrophages. Pathobiology 67, 222-226.
22. Stein, M., Keshav, S., Harris, N., Gordon, S. (1992) Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J. Exp. Med. 176, 287-292.
23. Duffield, J. S. (2003) The inflammatory macrophage: a story of Jekyll and Hyde. Clin. Sci. (Lond.) 104, 27-38.
24. Erwig, L. P., Kluth, D. C., Walsh, G. M., Rees, A. J. (1998) Initial cytokine exposure determines function of macrophages and renders them unresponsive to other cytokines. J. Immunol. 161, 1983-1988.
25. Goerdt, S., Orfanos, C. E. (1999) Other functions, other genes: alternative activation of antigen-presenting cells. Immunity 10, 137-142.
26. Fadok, V. A., Bratton, D. L., Konowal, A., Freed, P. W., Westcott, J. Y., Henson, P. M. (1998) Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-β, PGE2, and PAF. J. Clin. Invest. 101, 890-898.
27. Bartolone, J. B., Sparks, K., Cohen, S. D., Khairallah, E. A. (1987) Immunochemical detection of acetaminophen-bound liver proteins. Biochem. Pharmacol. 36, 1193-1196.
28. Fennekohl, A., Sugimoto, Y., Segi, E., Maruyama, T., Ichikawa, A., Puschel, G. P. (2002) Contribution of the two Gs-coupled PGE2-receptors EP2-receptor and EP4-receptor to the inhibition by PGE2 of the LPS-induced TNFα-formation in Kupffer cells from EP2- or EP4-receptor-deficient mice. Pivotal role for the EP4-receptor in wild type Kupffer cells. J. Hepatol. 36, 328-334.
29. Smedsrod, B., Pertoft, H. (1985) Preparation of pure hepatocytes and reticuloendothelial cells in high yield from a single rat liver by means of Percoll centrifugation and selective adherence. J. Leukoc. Biol. 38, 213-230.
30. Ju, C., Pohl, L. R. (2001) Immunohistochemical detection of protein adducts of 2,4-dinitrochlorobenzene in antigen presenting cells and lymphocytes after oral administration to mice: lack of a role of Kupffer cells in oral tolerance. Chem. Res. Toxicol. 14, 1209-1217.
31. Meijer, C., Wiezer, M. J., Diehl, A. M., Schouten, H. J., Schouten, H. J., Meijer, S., van Rooijen, N., van Lambalgen, A. A., Dijkstra, C. D., van Leeuwen, P. A. (2000) Kupffer cell depletion by CI2MDP-liposomes alters hepatic cytokine expression and delays liver regeneration after partial hepatectomy. Liver 20, 66-77.
32. Van Rooijen, N., Kors, N., vd Ende, M., Dijkstra, C. D. (1990) Depletion and repopulation of macrophages in spleen and liver of rat after intravenous treatment with liposome-encapsulated dichloromethylene diphosphonate. Cell Tissue Res. 260, 215-222.
33. Yamamoto, T., Naito, M., Moriyama, H., Umezu, H., Matsuo, H., Kiwada, H., Arakawa, M. (1996) Repopulation of murine Kupffer cells after intravenous administration of liposome-encapsulated dichloromethylene diphosphonate. Am. J. Pathol. 149, 1271-1286.
34. Lee, S. H., Starkey, P. M., Gordon, S. (1985) Quantitative analysis of total macrophage content in adult mouse tissues. Immunochemical studies with monoclonal antibody F4/80. J. Exp. Med. 161, 475-489.
35. Leenen, P. J., de Bruijn, M. F., Voerman, J. S., Campbell, P. A., van Ewijk, W. (1994) Markers of mouse macrophage development detected by monoclonal antibodies. J. Immunol. Methods 174, 5-19.
36. Goda, S., Imai, T., Yoshie, O., Yoneda, O., Inoue, H., Nagano, Y., Okazaki, T., Imai, H., Bloom, E. T., Domae, N., Umehara, H. (2000) CX3C-chemokine, fractalkine-enhanced adhesion of THP-1 cells to endothelial cells through integrin-dependent and -independent mechanisms. J. Immunol. 164, 4313-4320.
37. Fong, A. M., Robinson, L. A., Steeber, D. A., Tedder, T. F., Yoshie, O., Imai, T., Patel, D. D. (1998) Fractalkine and CX3CR1 mediate a novel mechanism of leukocyte capture, firm adhesion, and activation under physiologic flow. J. Exp. Med. 188, 1413-1419.
38. Haskell, C. A., Cleary, M. D., Charo, I. F. (2000) Unique role of the chemokine domain of fractalkine in cell capture. Kinetics of receptor dissociation correlate with cell adhesion. J. Biol. Chem. 275, 34183-34189.
39. Kuziel, W. A., Morgan, S. J., Dawson, T. C., Griffin, S., Smithies, O., Ley, K., Maeda, N. (1997) Severe reduction in leukocyte adhesion and monocyte extravasation in mice deficient in CC chemokine receptor 2. Proc. Natl. Acad. Sci. USA 94, 12053-12058.
40. Chang, N. C., Hung, S. I., Hwa, K. Y., Kato, I., Chen, J. E., Liu, C. H., Chang, A. C. (2001) A macrophage protein, Ym1, transiently expressed during inflammation is a novel mammalian lectin. J. Biol. Chem. 276, 17497-17506.
41. Raes, G., De Baetselier, P., Noel, W., Beschin, A., Brombacher, F., Hassanzadeh, G. G. (2002) Differential expression of FIZZ1 and Ym1 in alternatively versus classically activated macrophages. J. Leukoc. Biol. 71, 597-602.
42. Holcomb, I. N., Kabakoff, R. C., Chan, B., Baker, T. W., Gurney, A., Henzel, W., Nelson, C., Lowman, H. B., Wright, B. D., Skelton, N. J., Frantz, G. D., Tumas, D. B., Peale Jr., F. V., Shelton, D. L., Hébert, C. C. (2000) FIZZ1, a novel cysteine-rich secreted protein associated with pulmonary inflammation, defines a new gene family. EMBO J. 19, 4046-4055.
43. Munder, M., Eichmann, K., Modolell, M. (1998) Alternative metabolic states in murine macrophages reflected by the nitric oxide synthase/arginase balance: competitive regulation by CD4+ T cells correlates with Th1/Th2 phenotype. J. Immunol. 160, 5347-5354.
44. Zheng, T., Zhu, Z., Wang, Z., Homer, R. J., Ma, B., Riese Jr., R. J., Chapman Jr., H. A., Shapiro, S. D., Elias, J. A. (2000) Inducible targeting of IL-13 to the adult lung causes matrix metalloproteinase- and cathepsin-dependent emphysema. J. Clin. Invest. 106, 1081-1093.
45. De Noncourt, P., Robledo, O., Alain, T., Kossakowska, A. E., Urbanski, S. J., Potworowski, E. F., St Pierre, Y. (2001) Leukocyte elastase in murine and human non-Hodgkin lymphomas. J. Leukoc. Biol. 70, 585-591.
46. Lee, C. G., Homer, R. J., Zhu, Z., Lanone, S., Wang, X., Koteliansky, V., Shipley, J. M., Gotwals, P., Noble, P., Chen, Q., Senior R. M., Elias, J. A. (2001) Interleukin-13 induces tissue fibrosis by selectively stimulating and activating transforming growth factor β(1). J. Exp. Med. 194, 809-821.
47. Raes, G., Brys, L., Dahal, B. K., Brandt, J., Grooten, J., Brombacher, F., Vanham, G., Noel, W., Bogaert, P., Boonefaes, T., Kindt, A., Van den Bergh, R., Leenen, P. J., De Baetselier, P., Ghassabeh, G. H. (2005) Macrophage galactose-type C-type lectins as novel markers for alternatively activated macrophages elicited by parasitic infections and allergic airway inflammation. J. Leukoc. Biol. 77, 321-327.
48. Gill, S. E., Parks, W. C. (2008) Metalloproteinases and their inhibitors: regulators of wound healing. Int. J. Biochem. Cell Biol. 40, 1334-1347.
49. Curran, J. N., Winter, D. C., Bouchier-Hayes, D. (2006) Biological fate and clinical implications of arginine metabolism in tissue healing. Wound Repair Regen. 14, 376-386.
50. Sturge, J., Todd, S. K., Kogianni, G., McCarthy, A., Isacke, C. M. (2007) Mannose receptor regulation of macrophage cell migration. J. Leukoc. Biol. 82, 585-593.
51. Sato, K., Imai, Y., Higashi, N., Kumamoto, Y., Onami, T. M., Hedrick, S. M., Irimura, T. (2005) Lack of antigen-specific tissue remodeling in mice deficient in the macrophage galactose-type calcium-type lectin 1/CD301a. Blood 106, 207-215.
52. Dini, L., Pagliara, P., Carla, E. C. (2002) Phagocytosis of apoptotic cells by liver: a morphological study. Microsc. Res. Tech. 57, 530-540.
53. Bijl, M., Reefman, E., Horst, G., Limburg, P. C., Kallenberg, C. G. (2006) Reduced uptake of apoptotic cells by macrophages in systemic lupus erythematosus: correlates with decreased serum levels of complement. Ann. Rheum. Dis. 65, 57-63.
54. Gardai, S. J., McPhillips, K. A., Frasch, S. C., Janssen, W. J., Starefeldt, A., Murphy-Ullrich, J. E., Bratton, D. L., Oldenborg, P. A., Michalak, M., Henson, P. M. (2005) Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123, 321-334.
55. Serbina, N. V., Pamer, E. G. (2006) Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat. Immunol. 7, 311-317.
56. Xu, H., Manivannan, A., Dawson, R., Crane, I. J., Mack, M., Sharp, P., Liversidge, J. (2005) Differentiation to the CCR2+ inflammatory phenotype in vivo is a constitutive, time-limited property of blood monocytes and is independent of local inflammatory mediators. J. Immunol. 175, 6915-6923.
57. Brown, S. B., Savill, J. (1999) Phagocytosis triggers macrophage release of Fas ligand and induces apoptosis of bystander leukocytes. J. Immunol. 162, 480-485.
58. Kettritz, R., Xu, Y. X., Kerren, T., Quass, P., Klein, J. B., Luft, F. C., Haller, H. (1999) Extracellular matrix regulates apoptosis in human neutrophils. Kidney Int. 55, 562-571.
59. Lang, R. A., Bishop, J. M. (1993) Macrophages are required for cell death and tissue remodeling in the developing mouse eye. Cell 74, 453-462.
60. Murray, J., Barbara, J. A., Dunkley, S. A., Lopez, A. F., Van Ostade, X., Condliffe, A. M., Dransfield, I., Haslett, C., Chilvers, E. R. (1997) Regulation of neutrophil apoptosis by tumor necrosis factor-α: requirement for TNFR55 and TNFR75 for induction of apoptosis in vitro. Blood 90, 2772-2783.
61. Tsuchida, H., Takeda, Y., Takei, H., Shinzawa, H., Takahashi, T., Sendo, F. (1995) In vivo regulation of rat neutrophil apoptosis occurring spontaneously or induced with TNF-α or cycloheximide. J. Immunol. 154, 2403-2412.
62. Meszaros, A. J., Reichner, J. S., Albina, J. E. (2000) Macrophage-induced neutrophil apoptosis. J. Immunol. 165, 435-441.
63. Allenbach, C., Zufferey, C., Perez, C., Launois, P., Mueller, C., Tacchini-Cottier, F. (2006) Macrophages induce neutrophil apoptosis through membrane TNF, a process amplified by Leishmania major. J. Immunol. 176, 6656-6664.
64. Dambach, D. M., Watson, L. M., Gray, K. R., Durham, S. K., Laskin, D. L. (2002) Role of CCR2 in macrophage migration into the liver during acetaminophen-induced hepatotoxicity in the mouse. Hepatology 35, 1093-1103.
65. Kurushima, H., Ramprasad, M., Kondratenko, N., Foster, D. M., Quehenberger, O., Steinberg, D. (2000) Surface expression and rapid internalization of macrosialin (mouse CD68) on elicited mouse peritoneal macrophages. J. Leukoc. Biol. 67, 104-108.
66. Rabinowitz, S. S., Gordon, S. (1991) Macrosialin, a macrophage-restricted membrane sialoprotein differentially glycosylated in response to inflammatory stimuli. J. Exp. Med. 174, 827-836.
67. Arnold, L., Henry, A., Poron, F., Baba-Am, Y., van Rooijen, N., Plonquet, A., Gherardi, R. K., Chazaud, B. (2007) Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J. Exp. Med. 204, 1057-1069.
68. McDonald, P. P., Fadok, V. A., Bratton, D., Henson, P. M. (1999) Transcriptional and translational regulation of inflammatory mediator production by endogenous TGF-β in macrophages that have ingested apoptotic cells. J. Immunol. 163, 6164-6172.
69. Huynh, M. L., Fadok, V. A., Henson, P. M. (2002) Phosphatidylserine- dependent ingestion of apoptotic cells promotes TGF-β1 secretion and the resolution of inflammation. J. Clin. Invest. 109, 41-50.
70. Odaka, C., Mizuochi, T., Yang, J., Ding, A. (2003) Murine macrophages produce secretory leukocyte protease inhibitor during clearance of apoptotic cells: implications for resolution of the inflammatory response. J. Immunol. 171, 1507-1514.
71. Crowe, M. J., Doetschman, T., Greenhalgh, D. G. (2000) Delayed wound healing in immunodeficient TGF-β 1 knockout mice. J. Invest. Dermatol. 115, 3-11.
72. Ashcroft, G. S., Lei, K., Jin, W., Longenecker, G., Kulkarni, A. B., Greenwell-Wild, T., Hale-Donze, H., McGrady, G., Song, X. Y., Wahl, S. M. (2000) Secretory leukocyte protease inhibitor mediates non-redundant functions necessary for normal wound healing. Nat. Med. 6, 1147-1153.
73. Ishida, Y., Kondo, T., Ohshima, T., Fujiwara, H., Iwakura, Y., Mukaida, N. (2002) A pivotal involvement of IFN-γ in the pathogenesis of acetaminophen-induced acute liver injury. FASEB J. 16, 1227-1236.
74. Lawson, J. A., Farhood, A., Hopper, R. D., Bajt, M. L., Jaeschke, H. (2000) The hepatic inflammatory response after acetaminophen overdose: role of neutrophils. Toxicol. Sci. 54, 509-516.
75. Smith, G. S., Nadig, D. E., Kokoska, E. R., Solomon, H., Tiniakos, D. G., Miller, T. A. (1998) Role of neutrophils in hepatotoxicity induced by oral acetaminophen administration in rats. J. Surg. Res. 80, 252-258.
76. Newman, S. L., Henson, J. E., Henson, P. M. (1982) Phagocytosis of senescent neutrophils by human monocyte-derived macrophages and rabbit inflammatory macrophages. J. Exp. Med. 156, 430-442.
77. Malech, H. L. (2008) Phagocytic cells: egress from marrow and diapedesis. In Inflammation: Basic Principles and Clinical Correlates (J. I. Gallin, M. Goldstein, R. Snyderman, eds.), New York, NY, USA, Raven.
78. Weiss, S. J. (1989) Tissue destruction by neutrophils. N. Engl. J. Med. 320, 365-376.
79. Savill, J. (1997) Apoptosis in resolution of inflammation. J. Leukoc. Biol. 61, 375-380.
80. Hogaboam, C. M., Bone-Larson, C. L., Steinhauser, M. L., Matsukawa, A., Gosling, J., Boring, L., Charo, I. F., Simpson, K. J., Lukacs, N. W., Kunkel, S. L. (2000) Exaggerated hepatic injury due to acetaminophen challenge in mice lacking C-C chemokine receptor 2. Am. J. Pathol. 156, 1245-1252.
81. Linehan, S. A., Martinez-Pomares, L., Stahl, P. D., Gordon, S. (1999) Mannose receptor and its putative ligands in normal murine lymphoid and nonlymphoid organs: in situ expression of mannose receptor by selected macrophages, endothelial cells, perivascular microglia, and mesangial cells, but not dendritic cells. J. Exp. Med. 189, 1961-1972.
82. Mizuochi, S., Akimoto, Y., Imai, Y., Hirano, H., Irimura, T. (1997) Unique tissue distribution of a mouse macrophage C-type lectin. Glycobiology 7, 137-146.
83. Nair, M. G., Cochrane, D. W., Allen, J. E. (2003) Macrophages in chronic type 2 inflammation have a novel phenotype characterized by the abundant expression of Ym1 and Fizz1 that can be partly replicated in vitro. Immunol. Lett. 85, 173-180.
84. Nair, M. G., Gallagher, I. J., Taylor, M. D., Loke, P., Coulson, P. S., Wilson, R. A., Maizels, R. M., Allen, J. E. (2005) Chitinase and Fizz family members are a generalized feature of nematode infection with selective upregulation of Ym1 and Fizz1 by antigen-presenting cells. Infect. Immun. 73, 385-394.
85. Ward, J. M., Yoon, M., Anver, M. R., Haines, D. C., Kudo, G., Gonzalez, F. J., Kimura, S. (2001) Hyalinosis and Ym1/Ym2 gene expression in the stomach and respiratory tract of 129S4/SvJae and wild-type and CYP1A2-null B6, 129 mice. Am. J. Pathol. 158, 323-332.
86. Biswas, S. K., Gangi, L., Paul, S., Schioppa, T., Saccani, A., Sironi, M., Bottazzi, B., Doni, A., Vincenzo, B., Pasqualini, F., Vago, L., Nebuloni, M., Mantovani, A., Sica, A. (2006) A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-κB and enhanced IRF-3/STAT1 activation). Blood 107, 2112-2122.
87. Ito, Y., Bethea, N. W., Abril, E. R., McCuskey, R. S. (2003) Early hepatic microvascular injury in response to acetaminophen toxicity. Microcirculation 10, 391-400.
88. Ito, Y., Machen, N. W., Abril, E. R., McCuskey, R. S. (2004) Effects of acetaminophen on hepatic microcirculation in mice. Comp. Hepatol. 3 (Suppl. 1), S33.
89. Mantovani, A., Sica, A., Sozzani, S., Allavena, P., Vecchi, A., Locati, M. (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25, 677-686.
90. Kampfer, H., Pfeilschifter, J., Frank, S. (2003) Expression and activity of arginase isoenzymes during normal and diabetes-impaired skin repair. J. Invest. Dermatol. 121, 1544-1551.
91. Teng, X., Li, D., Champion, H. C., Johns, R. A. (2003) FIZZ1/RELMα, a novel hypoxia-induced mitogenic factor in lung with vasoconstrictive and angiogenic properties. Circ. Res. 92, 1065-1067.
92. Bergers, G., Brekken, R., McMahon, G., Vu, T. H., Itoh, T., Tamaki, K., Tanzawa, K., Thorpe, P., Itohara, S., Werb, Z., Hanahan, D. (2000) Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat. Cell Biol. 2, 737-744.
93. Coussens, L. M., Tinkle, C. L., Hanahan, D., Werb, Z. (2000) MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 103, 481-490.
94. Masson, V., de la Ballina, L. R., Munaut, C., Wielockx, B., Jost, M., Maillard, C., Blacher, S., Bajou, K., Itoh, T., Itohara, S., Werb, Z., Libert, C., Foidart, J. M., Noël, A. (2005) Contribution of host MMP-2 and MMP-9 to promote tumor vascularization and invasion of malignant keratinocytes. FASEB J. 19, 234-236.
95. Yang, L., DeBusk, L. M., Fukuda, K., Fingleton, B., Green-Jarvis, B., Shyr, Y., Matrisian, L. M., Carbone, D. P., Lin, P. C. (2004) Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 6, 409-421.
96. Ito, Y., Bethea, N. W., Abril, E. R., McCuskey, R. S. (2003) Early hepatic microvascular injury in response to acetaminophen toxicity. Microcirculation 10, 391-400.
97. Williams, A. M., Langley, P. G., Osei-Hwediah, J., Wendon, J. A., Hughes, R. D. (2003) Hyaluronic acid and endothelial damage due to paracetamol-induced hepatotoxicity. Liver Int. 23, 110-115.
98. McCuskey, R. S., Bethea, N. W., Wong, J., McCuskey, M. K., Abril, E. R., Wang, X., Ito, Y., DeLeve, L. D. (2005) Ethanol binging exacerbates sinusoidal endothelial and parenchymal injury elicited by acetaminophen. J. Hepatol. 42, 371-377.