Kupffer cells are obligatory for Plasmodium yoelii sporozoite infection of the liver

Cellular Microbiology

Volumn 9, Issue 2, 2007, Pages 397-412

  Baer, Kerstin ^a   Roosevelt, Michael ^a,d   Clarkson Jr , Allen B ^a   Van Rooijen, Nico ^b   Schnieder, Thomas ^c   Frevert, Ute ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^d REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON COLLOID; CLODRONIC ACID; COLONY STIMULATING FACTOR 1; RNA 18S;

ALBERS SCHOENBERG DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENCAPSULATION; HEPATITIS; HETEROZYGOSITY; HOMOZYGOSITY; KUPFFER CELL; LIVER CELL; LIVER CLEARANCE; LIVER PARENCHYMA; LIVER SINUSOID; MALARIA; MOUSE; MOUSE STRAIN; NONHUMAN; PHENOTYPE; PLASMODIUM YOELII; POINT MUTATION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPOROZOITE;

ANIMALS; KUPFFER CELLS; LIVER; MICE; PLASMODIUM YOELII; PROTOZOAN PROTEINS; SPOROZOITES;

MUS; PLASMODIUM YOELII;

EID: 33846264629     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2006.00798.x     Document Type: Article

References (119)

1. Amino, R., Thiberge, S., Martin, B., Celli, S., Shorte, S., Frischknecht, F., and Menard, R. (2006) Quanlitative imaging of Plasmodium transmission from mosquito to mammal. Nat Med 12: 220-224.
2. Biewenga, J., van der Ende, M.B., Krist, L.F., Borst, A., Ghufron, M., and van Rooijen, N. (1995) Macrophage depletion in the rat after intraperitoneal administration of liposome-encapsulated clodronate: depletion kinetics and accelerated repopulation of peritoneal and omental macrophages by administration of Freund's adjuvant. Cell Tissue Res 280: 189-196.
3. Bogers, W.M., Stad, R.K., Janssen, D.J., Prins, F.A., van Rooijen, N., van Es, L.A., and Daha, M.R. (1991) Kupffer cell depletion in vivo results in clearance of large-sized IgA aggregates in rats by liver endothelial cells. Clin Exp Immunol 85: 128-136.
4. Bouwens, L., and Wisse, E. (1992) The origin of Kupffer cells and their relationship to hepatocytes. In Hepatocyte and Kupffer Cell Interactions. Billiar, T.R., and Curran, R.D. (eds). Boca Raton, FL: CRC Press, pp. 3-21.
5. Bouwens, L., Baekeland, M., De Zanger, R., and Wisse, E. (1986) Quantitation, tissue distribution and proliferation kinetics of Kupffer cells in normal rat liver. Hepatology 6: 718-722.
6. Bray, R.S. (1957) Studies on the exo-erythrocytic cycle in the genus Plasmodium. London School Hyg & Trop Med Memoir 12: 1-192.
7. Briones, M.R.S., Tsuji, M., and Nussenzweig, V. (1996) The large difference in infectivity for mice of Plasmodium berghei and Plasmodium yoelii sporozoites cannot be correlated with their ability to enter hepatocytes. Mol Biochem Parasitol 77: 7-17.
8. Bruccoleri, A., and Harry, G.J. (2000) Chemical-induced hippocampal neurodegeneration and elevations in TNFalpha, TNFbeta, IL-1alpha, IP-10, and MCP-1 mRNA in osteopetrotic (op/op) mice. J Neurosci Res 62: 146-155.
9. Bruna-Romero, O., Hafalla, J.C.R., Gonzalez-Aseguinolaza, G., Sano, G., Suji, M., and Zavala, F. (2001) Detection of malaria liver-stages in mice infected through the bite of a single Anopheles mosquito using a highly sensitive real-time PCR. Int J Parasitol 31: 1499-1502.
10. Calvo-Calle, J.M., Moreno, A., Eling, W.M.C., and Nardin, E.H. (1994) In vitro development of infectious liver stages of P. yoelii and P. berghei malaria in human cell lines. Exp Parasitol 79: 362-373.
11. Cecchini, M.G., Dominguez, M.G., Mocci, S., Wetterwald, A., Felix, R., Fleisch, H., et.al. (1994) Role of colony stimulating factor-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse. Development 120: 1357-1372.
12. Crofton, R.W., Diesselhoff-den Dulk, M.M., and van Furth, R. (1978) The origin, kinetics, and characteristics of the Kupffer cells in the normal steady state. J Exp Med 148: 1-17.
13. Desser, S.S., Weller, I., and Yoeli, M. (1972) An ultrastructural study of the pre-erythrocytic development of Plasmodium berghei in the tree rat, Thamnomys surdaster. Can J Zool 50: 821-825.
14. Diesselhoff-den Dulk, M.M., Crofton, R.W., and van Furth, R. (1979) Origin and kinetics of Kupffer cells during an acute inflammatory response. Immunology 37: 7-14.
15. Doolan, D.L., and Hoffman, S.L. (2000) The complexity of protective immunity against liver-stage malaria. J Immunol 165: 1453-1492.
16. Doolan, D.L., and Martinez-Alier, N. (2006) Immune response to pre-erythrocytic stages of malaria parasites. Curr Mol Med 6: 169-185.
17. Faust, N., Varas, F., Kelly, L.M., Heck, S., and Graf, T. (2000) Insertion of green fluorescent protein into the lysozyme gene creates mice with green fluorescent granulocytes and macrophages. Blood 96: 719-726.
18. Felix, R., Cecchini, M.G., and Fleisch, H. (1990a) Macrophage colony stimulating factor restores in vivo bone resorption in the op/op osteopetrotic mouse. Endocrinology 127: 2592-2594.
19. Felix, R., Cecchini, M.G., Hofstetter, W., Elford, P.R., Stutzer, A., and Fleisch, H. (1990b) Impairment of macrophage colony-stimulating factor production and lack of resident bone marrow macrophages in the osteopetrotic op/op mouse. J Bone Miner Res 5: 781-789.
20. Frevert, U. (2004) Sneaking in through the back entrance: The biology of malaria liver stages. Trends Parasitol 20: 417-424.
21. Frevert, U., Engelmann, S., Zougbédé, S., Stange, J., Ng, B., Matuschewski, K., et.al. (2005) Intravital observation of Plasmodium berghei sporozoite infection of the liver. PLoS Biol 3: E192.
22. van Furth, R. (1984) [Characteristics of mononuclear phagocytes in their normal state and in inflammation]. Folia Haematol Int Mag Klin Morphol Blutforsch 111: 131-140.
23. Gosset, P., Lassalle, P., Vanhée, D., Wallaert, B., Aerts, C., Voisin, C., and Tonnel, A.-B. (1991) Production of tumor necrosis factor-α and interleukin-6 by human alveolar macrophages exposed in vitro to coal mine dust. Am J Respir Cell Mol Biol 5: 431-436.
24. Gressner, A.M., and Schäfer, S. (1989) Comparison of sulphated glycosaminoglycan and hyaluronate synthesis and secretion in cultured hepatocytes, fat storing cells, and Kupffer cells. J Clin Chem Clin Biochem 27: 141-149.
25. Gressner, A.M., Haarmann, R., Schäfer, S., and Zerbe, O. (1989) The role of fat storing cells in matrix proteoglycan and hyaloronate production in relation to Kupffer cells and hepatocytes. In Cells of the Hepatic Sinusoid, Vol. 2. Wisse, E., Knook, D.L., and Decker, K. (eds). Rijswijk: Kupffer Cell Foundation, pp. 64-68.
26. Guleria, I., and Pollard, J.W. (2001) Aberrant macrophage and neutrophil population dynamics and impaired Th1 response to Listeria monocytogenes in colony-stimulating factor 1-deficient mice. Infect Immun 69: 1795-1807.
27. Gumucio, J.J., Bilir, B.M., Moseley, R.H., and Berkowitz, C.M. (1994) The biology of the liver cell plate. In The Liver: Biology and Pathobiology. Arias, I.M., Boyer, J.L., Fausto, N., Jakoby, W.B., Schachter, D.A., and Shafritz, D.A. (eds). New York: Raven Press, pp. 1143-1163.
28. Hardonk, M.J., Dijkhuis, F.W., Grond, J., Koudstaal, J., and Poppema, S. (1986) Evidence for a migratory capability of rat Kupffer cells to portal tracts and hepatic lymph nodes. Virchows Arch B Cell Pathol Incl Mol Pathol 51: 429-442.
29. Hoffman, S.L., Franke, E.D., Hollingdale, M.R., and Druilhe, P. (1996) Attacking the infected hepatocyte. In Malaria Vaccine Development. Hoffman, S.L. (ed.). Washington, DC: American Society for Microbiology, pp. 35-75.
30. Hollingdale, M.R. (1985) Malaria and the liver. Hepatology 5: 327-335.
31. Hollingdale, M.R. (1988) Biology and immunology of sporozoite invasion of liver cells and exoerythrocytic development of malaria parasites. Prog Allergy 41: 15-48.
32. Hollingdale, M., and Krzych, U. (2002) Immune responses to liver-stage parasites: Implications for vaccine development. In Malaria Immunology. Perlman, P., and Troye-Blomberg, M. (eds). Basel: Karger, pp. 97-124.
33. Huff, C.G. (1969) Exoerythrocytic stages of avian and reptilian malarial parasites. Exp Parasitol 24: 383-421.
34. Hügel, F.-U., Pradel, G., and Frevert, U. (1996) Release of malaria circumsporozoite protein into the host cell cytoplasm and interaction with ribosomes. Mol Biochem Parasitol 81: 151-170.
35. Ishino, T., Yano, K., Chinzei, Y., and Yuda, M. (2004) Cell-passage activity is required for the malarial parasite to cross the liver sinusoidal cell layer. PLoS Biol 2: E4.
36. Ishino, T., Chinzei, H., and Yuda, M. (2005) A Plasmodium sporozoite protein with a membrane attack complex domain is required for breaching the liver sinusoidal cell layer prior to hepatocyte infection. Cell Microbiol 2: E4.
37. Jahiel, R.I., Vilcek, J., Nussenzweig, R., and Vanderberg, J. (1968a) Interferon inducers protect mice against Plasmodium berghei malaria. Science 161: 802-804.
38. Jahiel, R.I., Nussenzweig, R.S., Vanderberg, J., and Vilcek, J. (1968b) Anti-malarial effect of interferon inducers at different stages of development of Plasmodium berghei in the mouse. Nature 220: 710-711.
39. Jahiel, R.I., Nussenzweig, R.S., Vilcek, J., and Vanderberg, J. (1969) Protective effect of interferon inducers on Plasmodium berghei malaria. Am J Trop Med Hyg 18: 823-835.
40. Jahiel, R.I., Vilcek, J., and Nussenzweig, R.S. (1970) Exogenous interferon protects mice against Plasmodium berghei malaria. Nature 227: 1350-1351.
41. Jiang, S., Naito, M., Kaizu, C., Kuwata, K., Hasegawa, G., Mukaida, N., and Shultz, L.D. (2000) Lipopolysaccharide-induced cytokine and receptor expression and neutrophil infiltration in the liver of osteopetrosis (op/ op) mutant mice. Liver 20: 465-474.
42. Jin, Y., Dons, L., Kristensson, K., and Rottenberg, M.E. (2002) Colony-stimulating factor 1-dependent cells protect against systemic infection with Listeria monocytogenes but facilitate neuroinvasion. Infect Immun 70: 4682-4686.
43. Karnasuta, C., and Watt, G. (1996) Enhanced detection of Plasmodium vivax liver stages by cytocentrifugation. Parasitol Today 12: 451-453.
44. Karnasuta, C., Pavanand, K., Chantakulkij, S., Luttiwongsakorn, N., Rassamesoraj, M., Laohathai, K., et.al. (1995) Complete development of the liver stage of Plasmodium falciparum in a human hepatoma cell line. Am J Trop Med Hyg 53: 607-611.
45. Krzych, U., and Schwenk, J. (2005) The dissection of CD8 T cells during liver-stage infection. Curr Top Microbiol Immunol 297: 1-24.
46. Kuiper, J., Brouwer, A., Knook, D.L., and Berkel, T.J.C.V. (1994) Kupffer and sinusoidal endothelial cells. In The Liver: Biology and Pathobiology. Arias, I.M., Boyer, J.L., Fausto, N., Jakoby, W.B., Schachter, D.A., and Shafritz, D.A. (eds). New York: Raven Press, pp. 791-818.
47. Laskin, D.L. (1997) Role of hepatic macrophages in inflammation and tissue injury. In Functional Heterogeneity of Liver Tissue. Vidal-Vanaclocha, F. (ed.). Austin: R.G. Landes Company, pp. 161-176.
48. Lawson, J.A., Farhood, A., Hopper, R.D., Bajt, M.L., and Jaeschke, H. (2000) The hepatic inflammatory response after acetaminophen overdose: role of neutrophils. Toxicol Sci 54: 509-516.
49. Lee, S.H., Starkey, P.M., and 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.
50. Lieschke, G.J., Grail, D., Hodgson, G., Metcalf, D., Stanley, E., Cheers, C., et.al. (1994) Mice lacking granulocyte colony-stimulating factor have chronic neutropenia, granulocyte and macrophage progenitor cell deficiency, and impaired neutrophil mobilization. Blood 84: 1737-1746.
51. Lievens, J., Snoeys, J., Vekemans, K., Van Linthout, S., de Zanger, R., Collen, D., et.al. (2004) The size of sinusoidal fenestrae is a critical determinant of hepatocyte transduction after adenoviral gene transfer. Gene Ther 11: 1523-1531.
52. Luke, T.C., and Hoffman, S.L. (2003) Rationale and plans for developing a non-replicating, metabolically active, radiation-attenuated Plasmodium falciparum sporozoite vaccine. J Exp Biol 206: 3803-3808.
53. McCuskey, R.S. (1994) The hepatic microvascular system. In The Liver: Biology and Pathobiology. Arias, I.M., Boyer, J.L., Fausto, N., Jakoby, W.B., Schachter, D.A., and Shafritz, D.A. (eds). New York: Raven Press, pp. 1089-1106.
54. McCuskey, R.S. (2000) Morphological mechanism for regulating blood flow through hepatic sinusoids. Liver 20: 3-7.
55. McCuskey, R.S., and Reilly, F.D. (1993) Hepatic microvasculature: dynamic structure and its regulation. Semin Liver Dis 13: 1-12.
56. MacPhee, P.J., Schmidt, E.E., and Groom, A.C. (1992) Evidence for Kupffer cell migration along liver sinusoids, from high-resolution in vivo microscopy. Am J Physiol 263: G17-G23.
57. Mangold, K.A., Manson, R.U., Koay, E.S., Stephens, L., Regner, M., Thomson, R.B., Jr, et.al. (2005) Real-time PCR for detection and identification of Plasmodium spp. J Clin Microbiol 43: 2435-2440.
58. Mazier, D., Collins, W.E., Mellouk, S., Procell, P.M., Berbiguier, N., Campbell, G.H., et.al. (1987) Plasmodium ovale: In vitro development of hepatic stages. Exp Parasitol 64: 393-400.
59. Medica, D.L., and Sinnis, P. (2005) Quantitative dynamics of Plasmodium yoelii sporozoite transmission by infected anopheline mosquitoes. Infect Immun 73: 4363-4369.
60. Meis, J.F.G.M., Verhave, J.P., Jap, P.H.K., and Meuwissen, J.H.E.T. (1983) An ultrastructural study on the role of Kupffer cells in the process of infection by Plasmodium berghei sporozoites in rats. Parasitology 86: 231-242.
61. Meis, J.F.G.M., Verhave, J.P., Brouwer, A., and Meuwissen, J.H.E.T. (1985) Electron microscopic studies on the interaction of rat Kupffer cells and Plasmodium berghei sporozoites. Z Parasitenkd 71: 473-483.
62. Millet, P., Collins, W.E., Fisk, T.L., and Nguyen-Dinh, P. (1988a) In vitro cultivation of exoerythrocytic stages of the human malaria parasite Plasmodium malariae. Am J Trop Med Hyg 38: 470-473.
63. Millet, P., Fisk, T.L., Collins, W.E., Broderson, J.R., and Nguyen-Dinh, P. (1988b) Cultivation of exoerythrocytic stages of Plasmodium cynomolgi, P. knowlesi, P. coatneyi, and P. inui in Macaca mulatta hepatocytes. Am J Trop Med Hyg 39: 529-534.
64. Morrot, A., and Zavala, F. (2004) Effector and memory CD+ T cells as seen in immunity to malaria. Immunol Rev 201: 291-303.
65. Mota, M.M., and Rodríguez, A. (2002) Invasion of mammalian host cells by Plasmodium sporozoites. Bioessays 24: 149-156.
66. Motoike, T., Loughna, S., Perens, E., Roman, B.L., Liao, W., Chau, T.C., et.al. (2000) Universal GFP reporter for the study of vascular development. Genesis 28: 75-81.
67. Motta, P.M. (1984) The three-dimensional microanatomy of the liver. Arch Histol Jpn 47: 1-30.
68. Motta, P.M., Muto, M., and Fujita, T. (1978) The vascular system. In The Liver. An Atlas of Electron Microscopy. Motta, P.M., Muto, M., and Fujita, T. (eds). Tokyo: Igaku-Shoin, pp. 83-118.
69. Naito, M., Nagai, H., Kawano, S., Umezu, H., Zhu, H., Moriyama, H., et.al. (1996) Liposome-encapsulated dichloromethylene diphosphonate induces macrophage apoptosis in vivo and in vitro. J Leukoc Biol 60: 337-344.
70. Naito, M., Hasegawa, G., and Takahashi, K. (1997) Development, differentiation, and maturation of Kupffer cells. Microsc Res Tech 39: 350-364.
71. Naito, M., Hasegawa, G., Ebe, Y., and Yamamoto, T. (2004) Differentiation and function of Kupffer cells. Med Electron Microsc 37: 16-28.
72. Nanji, A.A. (2002) Role of Kupffer cells in alcoholic hepatitis. Alcohol 27: 13-15.
73. Nardin, E.H., and Nussenzweig, R.S. (1993) T cell responses to pre-erythrocytic stages of malaria: Role in protection and vaccine development against pre-erythrocytic stages. Annu Rev Immunol 11: 687-727.
74. Nishioji, K., Okanoue, T., Mori, T., Sakamoto, S., and Itoh, Y. (1999) Experimental liver injury induced by Propionibacterium acnes and lipopolysaccharide in macrophage colony stimulating factor-deficient osteopetrotic (op/op) mice. Dig Dis Sci 44: 1975-1984.
75. Pinzon-Ortiz, C., Friedman, J., Esko, J., and Sinnis, P. (2001) The binding of the circumsporozoite protein to cell surface heparan sulfate proteoglycans is required for Plasmodium sporozoite attachment to target cells. J Biol Chem 276: 26784-26791.
76. Pollard, J.W. (1997) Role of colony-stimulating factor-1 in reproduction and development. Mol Reprod Dev 46: 54-60; discussion 60-51.
77. Pradel, G., and Frevert, U. (2001) Plasmodium sporozoites actively enter and pass through Kupffer cells prior to hepatocyte invasion. Hepatology 33: 1154-1165.
78. Pradel, G., Garapaty, S., and Frevert, U. (2002) Proteoglycans mediate malaria sporozoite targeting to the liver. Mol Microbiol 45: 637-651.
79. Pradel, G., Garapaty, S., and Frevert, U. (2004) Kupffer and stellate cell proteoglycans mediate malaria sporozoite targeting to the liver. Comp Hepatol 3 (Suppl. 1): S47.
80. van Rooijen, N., and van Kesteren-Hendrikx, E. (2002) Clodronate liposomes: Perspectives in research and therapeutics. J Liposome Res 12: 81-94.
81. van Rooijen, N., and van Nieuwmegen, R. (1984) Elimination of phagocytic cells in the spleen after intravenous injection of liposome-encapsulated dichloromethylene diphosphonate. An enzyme-histochemical study. Cell Tissue Res 238: 355-358.
82. 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.
83. van Rooijen, N., and Sanders, A. (1996) Kupffer cell depletion by liposome-delivered drugs: Comparative activity of intracellular clodronate, propamidine, and ethylenediaminetetraacetic acid. Hepatology 23: 1239-1243.
84. van Rooijen, N., Kors, N., vd Ende, M., and 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.
85. van Rooijen, N., Sanders, A., and van den Berg, T.K. (1996) Apoptosis of macrophages induced by liposome-mediated intracellular delivery of clodronate and propamidine. J Immunol Methods 193: 93-99.
86. Sakamoto, T., Mabuchi, A., Kuriya, S., Sudo, T., Aida, T., Asano, G., et.al. (1990) Production of granulocyte-macrophage colony-stimulating factor by adult murine parenchymal liver cells (hepatocytes). Reg Immunol 3: 260-267.
87. Schmidt-Weber, C.B., Rittig, M., Buchner, E., Hauser, I., Schmidt, I., Palombo-Kinne, E., et.al. (1996) Apoptotic cell death in activated monocytes following incorporation of clodronate-liposomes. J Leukoc Biol 60: 230-244.
88. Schönlau, F., Schlesiger, C., Ehrchen, J., Grabbe, S., Sorg, C., and Sunderkotter, C. (2003) Monocyte and macrophage functions in M-CSF-deficient op/op mice during experimental leishmaniasis. J Leukoc Biol 73: 564-573.
89. Schümann, J., Wolf, D., Pahl, A., Brune, K., Papadopoulos, T., van Rooijen, N., and Tiegs, G. (2000) Importance of Kupffer cells for T-cell-dependent liver injury in mice. Am J Pathol 157: 1671-1683.
90. Shibuya, H., Ohkohchi, N., Tsukamoto, S., and Satomi, S. (1997) Tumor necrosis factor-induced, superoxide-mediated neutrophil accumulation in cold ischemic/reperfused rat liver. Hepatology 26: 113-120.
91. Shultz, L.D., and Sidman, C.L. (1987) Genetically determined murine models of immunodeficiency. Annu Rev Immunol 5: 367-403.
92. Sidjanski, S., and Vanderberg, J.P. (1997) Delayed migration of Plasmodium sporozoites from the mosquito bite site to the blood. Am J Trop Med Hyg 57: 426-429.
93. Sinden, R.E., and Smith, J.E. (1982) The role of the Kupffer cell in the infection of rodents by sporozoites of Plasmodium: Uptake of sporozoites by perfused liver and the establishment of infection in vivo. Acta Trop 39: 11-27.
94. Sinden, R.E., Suhrbier, A., Davies, C.S., Fleck, S.L., Hodivala, K., and Nicholas, J.C. (1990) The development and routine application of high-density exoerythrocytic-stage culture of Plasmodium berghei. WHO Bull 68 (Suppl.): 115-125.
95. Sinnis, P., Willnow, T.E., Briones, M.R.S., Herz, J., and Nussenzweig, V. (1996) Remnant lipoproteins inhibit malaria sporozoite invasion of hepatocytes. J Exp Med 184: 945-954.
96. Szperl, M., Ansari, A.A., Urbanowska, E., Szwech, P., Kalinski, P., and Wiktor-Jedrzejczak, W. (1995) Increased resistance of CSF-1-deficient, macrophage-deficient, TNF alpha-deficient, and IL-1 alpha-deficient op/ op mice to endotoxin. Ann NY Acad Sci 762: 499-501.
97. Tsuji, M., Rodrigues, E.G., and Nussenzweig, R.S. (2001) Progress toward a malaria vaccine: Efficient induction of protective anti-malaria immunity. Biol Chem 382: 553-570.
98. Tsukui, T., Kikuchi, K., Mabuchi, A., Sudo, T., Sakamoto, T., Sato, N., et.al. (1992) Production of macrophage colony-stimulating factor by adult murine parenchymal liver cells (hepatocytes). J Leukoc Biol 52: 383-389.
99. Van Furth, R., Diesselhoff-den Dulk, M.M.C., Sluiter, W., and van Dissel, J.T. (1985) New perspectives on the kinetics of mononuclear macrophages. In Mononuclear Phagocytes: Characteristics, Physiology, and Function. Van Furth, R. (ed.). Dordrecht: Martinus-Nijhoff, pp. 201-208.
100. Vanderberg, J.P., and Frevert, U. (2004) Intravital microscopy demonstrating antibody-mediated immobilization of Plasmodium berghei sporozoites injected into skin by mosquitoes. Int J Parasitol 34: 991-996.
101. Vanderberg, J.P., and Gwadz, R. (1980) The transmission by mosquitoes of Plasmodia in the laboratory. In Malaria: Pathology, Vector Studies and Culture. Kreier, J. (ed.). New York: New York Academic Press, pp. 154-218.
102. Verhave, J.P., Meuwissen, J.H.E.T., and Golenser, J. (1980) The dual role of macrophages in the sporozoite-induced malaria infection. A hypothesis. Int J Nucl Med Biol 7: 149-156.
103. Vigario, A.M., Belnoue, E., Cumano, A., Marussig, M., Miltgen, F., Landau, I., et.al. (2001) Inhibition of Plasmodium yoelii blood-stage malaria by interferon alpha through the inhibition of the production of its target cell, the reticulocyte. Blood 97: 3966-3971.
104. Vreden, S.G.S. (1994) The role of Kupffer cells in the clearance of malaria sporozoites from the circulation. ParasitolToday 10: 304-308.
105. Vreden, S.G.S., Sauerwein, R.W., Verhave, J.P., Van Rooijen, N., Meuwissen, J.H.E.T., and Broek, M.F. (1993) Kupffer cell elimination enhances development of liver schizonts of Plasmodium berghei in rats. Infect Immun 61: 1936-1939.
106. Wake, K. (1980) Perisinusoidal stellate cells (fat-storing cells, interstitial cells, lipocytes), their related structure in and around the liver sinusoids, and vitamin A-storing cells in extrahepatic organs. Int Rev Cytol 66: 303-353.
107. Wake, K., Decker, K., Kirn, A., Knook, D.L., McCuskey, R.S., Bouwens, L., and Wisse, E. (1989) Cell biology and kinetics of Kupffer cells in the liver. Int Rev Cytol 118: 173-229.
108. Widmann, J.-J., Cotran, R.S., and Fahimi, H.D. (1972) Mononuclear phagocytes (Kupffer cells) and endothelial cells. Identification of two functional cell types in rat liver sinusoids by endogenous peroxidase activity. J Cell Biol 52: 159-170.
109. Wiktor-Jedrzejczak, W. (1993) In vivo role of macrophage growth factors as delineated using CSF-1 deficient op/op mouse. Leukemia 7 (Suppl. 2): S117-S121.
110. Wiktor-Jedrzejczak, W., and Gordon, S. (1996) Cytokine regulation of the macrophage (Mθ) system studied using the colony stimulating factor-1-deficient op/op mouse. Physiol Rev 76: 927-947.
111. Wiktor-Jedrzejczak, W., Urbanowska, E., Aukerman, S.L., Pollard, J.W., Stanley, E.R., Ralph, P., et.al. (1991) Correction by CSF-1 of defects in the osteopetrotic op/op mouse suggests local, developmental, and humoral requirements for this growth factor. Exp Hematol 19: 1049-1054.
112. Wiktor-Jedrzejczak, W., Ansari, A.A., Szperl, M., and Urbanowska, E. (1992) Distinct in vivo functions of two macrophage subpopulations as evidenced by studies using macrophage-deficient op/op mouse. Eur J Immunol 22: 1951-1954.
113. Wisse, E. (1974) Observations on the fine structure and peroxidase cytochemistry of normal rat liver Kupffer cells. J Ultrastruct Res 46: 393-426.
114. Wisse, E. (1977) Ultrastructure and function of Kupffer cells and other sinusoidal cells in the liver. In Kupffer Cells and Other Liver Sinusoidal Cells. Wisse, E., and Knook, D.L. (eds). Amsterdam: Elsevier/ North Holland Biomedical Press, pp. 33-60.
115. Wisse, E., Zanger, R.B., Charels, K., Smissen, P., and McCuskey, R.S. (1985) The liver sieve: Considerations concerning the structure and function of endothelial fenestrae, the sinusoidal wall and the space of Disse. Hepatology 5: 683-692.
116. Witmer-Pack, M.D., Hughes, D.A., Schuler, G., Lawson, L., McWilliam, A., Inaba, K., et.al. (1993) Identification of macrophages and dendritic cells in the osteopetrotic (op/op) mouse. J Cell Sci 104: 1021-1029.
117. Witney, A.A., Doolan, D.L., Anthony, R.M., Weiss, W.R., Hoffman, S.L., and Carucci, D.J. (2001) Determining liver stage parasites burden by real time quantitative PCR as a method for evalutaing pre-erythrocytic malaria vaccine. Mol Biochem Parasitol 118: 233-245.
118. Yamamoto, T., Naito, M., Moriyama, H., Umezu, H., Matsuo, H., Kiwada, H., and Arakawa, M. (1996) Repopulation of murine Kupffer cells after intravenous administration of liposome-encapsulated dichloromethylene diphosphonate. Am J Pathol 149: 1271-1286.
119. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406-3415.