Skip to main content

Plasmodium Sporozoite Passage across the Sinusoidal Cell Layer

  • Chapter
Molecular Mechanisms of Parasite Invasion

Part of the book series: Subcellular Biochemistry ((SCBI,volume 47))

Abstract

Malaria sporozoites must cross at least two cell barriers to reach their initial site of replication in the mammalian host. After transmission into the skin by an infected mosquito, they migrate towards small dermal capillaries, traverse the vascular endothelial layer,1,2 and rapidly home to the liver. To infect hepatocytes, the parasites must cross the sinusoidal cell layer, composed of specialized highly fenestrated sinusoidal endothelia and Kupffer cells, the resident macrophages of the liver (Fig. 1). The exact route Plasmodium sporozoites take to hepatocytes has been subject of controversial discussions for many years. Recent cell biological, microscopic, and genetic approaches have considerably enhanced our understanding of the initial events leading to the establishment of a malaria infection in the liver (for recent reviews see refs. 38).

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Vanderberg JP, Frevert U. Intravital microscopy demonstrating antibody-mediated immobilization of Plasmodium berghei sporozoites injected into skin by mosquitoes. Int J Parasitol 2004; 34:991–996.

    Article  PubMed  Google Scholar 

  2. Amino R, Thiberge S, Martin B et al. Quantitative imaging of Plasmodium transmission from mosquito to mammal. Nat Med 2006; 12:220–224.

    Article  PubMed  CAS  Google Scholar 

  3. Frevert U. Sneaking in through the back entrance: The biology of malaria liver stages. Trends Parasitol 2004; 20:417–424.

    Article  PubMed  CAS  Google Scholar 

  4. Yuda M, Ishino T. Liver invasion by malarial parasites—how do malarial parasites break through the host barrier? Cell Microbiol 2004; 6:1119–1125.

    Article  PubMed  CAS  Google Scholar 

  5. Amino R, Menard R, Frischknecht F. In vivo imaging of malaria parasites—recent advances and future directions. Curr Opin Microbiol 2005; 8:407–414.

    Article  PubMed  CAS  Google Scholar 

  6. Silvie O, Franetich JF, Renia L et al. Malaria sporozoite: Migrating for a living. Trends Mol Med 2004; 10:97–100.

    Article  PubMed  Google Scholar 

  7. Mota MM, Rodriguez A. Migration through host cells: The first steps of Plasmodium sporozoites in the mammalian host. Cell Microbiol 2004; 6:1113–1118.

    Article  PubMed  CAS  Google Scholar 

  8. Frevert U, Usynin I, Baer K et al. Nomadic or sessile: Can Kupffer cells function as portals for malaria sporozoites to the liver? Cell Microbiol 2006; 8:1537–1546.

    Article  PubMed  CAS  Google Scholar 

  9. Pradel G, Garapaty S, Frevert U. Proteoglycans mediate malaria sporozoite targeting to the liver. Mol Microbiol 2002; 45:637–651.

    Article  PubMed  CAS  Google Scholar 

  10. Robson KJH, Frevert U, Reckmann I et al. Thrombospondin related adhesive protein (TRAP) of Plasmodium falciparum: Expression during sporozoite ontogeny and binding to human hepatocytes. EMBO J 1995; 14:3883–3894.

    PubMed  CAS  Google Scholar 

  11. Pradel G, Garapaty S, Frevert U. Kupffer and stellate cell proteoglycans mediate malaria sporozoite targeting to the liver. Comp Hepatol 2004; 3(Suppl 1):S47.

    Article  PubMed  Google Scholar 

  12. Gressner AM, Schäfer S. Comparison of sulphated glycosaminoglycan and hyaluronate synthesis and secretion in cultured hepatocytes, fat storing cells, and Kupffer cells. J Clin Chem Clin Biochem 1989; 27:141–149.

    PubMed  CAS  Google Scholar 

  13. Cerami C, Frevert U, Sinnis P et al. The basolateral domain of the hepatocyte plasma membrane bears receptors for the circumsporozoite protein of Plasmodium falciparum sporozoites. Cell 1992; 70:1021–1033.

    Article  PubMed  CAS  Google Scholar 

  14. Frevert U, Sinnis P, Cerami C et al. Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. J Exp Med 1993; 177:1287–1298.

    Article  PubMed  CAS  Google Scholar 

  15. Lyon M, Denkin JA, Gallagher JT. Liver heparan sulfate structure. A novel molecular design. J Biol Chem 1994; 269:11208–11215.

    PubMed  CAS  Google Scholar 

  16. Frevert U, Engelmann S, Zougbédé S et al. Intravital observation of Plasmodium berghei sporozoite infection of the liver. PLoS Biol 2005; 3:e192.

    Article  PubMed  CAS  Google Scholar 

  17. Pinzon-Ortiz C, Friedman J, Esko J et al. The binding of the circumsporozoite protein to cell surface heparan sulfate proteoglycans is required for Plasmodium sporozoite attachment to target cells. J Biol Chem 2001; 276:26784–26791.

    Article  PubMed  CAS  Google Scholar 

  18. Ying P, Shakibaei M, Patankar MS et al. The malaria circumsporozoite protein: Interaction of the conserved regions I and II-plus with heparin-like oligosaccharides in heparan sulfate. Exp Parasitol 1997; 85:168–182.

    Article  PubMed  CAS  Google Scholar 

  19. Ancsin JB, Kisilevsky R. A binding site for highly sulfated heparan sulfate is identified in the amino-terminus of the circumsporozoite protein: Significance for malarial sporozoite attachment to hepatocytes. J Biol Chem 2004; 279:21824–21832.

    Article  PubMed  CAS  Google Scholar 

  20. Rathore D, Kumar S, Lanar DE et al. Disruption of disulfide linkages of the Plasmodium falciparum circumsporozoite protein: Effects on cytotoxic and antibody responses in mice. Mol Biochem Parasitol 2001; 118:75–82.

    Article  PubMed  CAS  Google Scholar 

  21. Rathore D, McCutchan TF. Heparin can regulate the binding of Plasmodium falciparum circumsporozoite protein. Mol Biochem Parasitol 2000; 108:253–256.

    Article  PubMed  CAS  Google Scholar 

  22. Rathore D, McCutchan TF, Garboczi DN et al. Direct measurement of the interactions of glycosaminoglycans and a heparin decasaccharide with the malaria circumsporozoite protein. Biochemistry 2001; 40:11518–11524.

    Article  PubMed  CAS  Google Scholar 

  23. Shakibaei M, Frevert U. Dual interaction of the malaria circumsporozoite protein with the low density lipoprotein receptor-related protein (LRP) and cell surface heparan sulfate. J Exp Med 1996; 184:1699–1711.

    Article  PubMed  CAS  Google Scholar 

  24. Strickland DK, Kounnas MZ, Argraves WS. LDL receptor-related protein: A multiligand receptor for lipoprotein and proteinase catabolism. FASEB J 1995; 9:890–897.

    PubMed  CAS  Google Scholar 

  25. Strickland DK, Kounnas MZ, Williams SE et al. LDL receptor-related protein (LRP): A multiligand receptor. Fibrinolysis 1994; 8(Suppl):204–215.

    Article  CAS  Google Scholar 

  26. Herz J. The LDL-receptor-related protein—portrait of a multifunctional receptor. Curr Opin Lipidol 1993; 4:107–113.

    Article  CAS  Google Scholar 

  27. Rohlmann A, Gotthardt M, Hammer RE et al. Inducible inactivation of hepatic LRP gene by cre-mediated recombination confirms role of LRP in clearance of chylomicron remnants. J Clin Invest 1998; 101:689–695.

    Article  PubMed  CAS  Google Scholar 

  28. Rohlmann A, Gotthardt M, Willnow TE et al. Sustained somatic gene inactivation by viral transfer of Cre recombinase. Nat Biotechnol 1996; 14:1562–1565.

    Article  PubMed  CAS  Google Scholar 

  29. Herz J, Gerard RD. Adenovirus-mediated transfer of low density lipoprotein receptor gene acutely accelerates cholesterol clearance in normal mice. Proc Natl Acad Sci USA 1993; 90:2812–2816.

    Article  PubMed  CAS  Google Scholar 

  30. Shayakhmetov DM, Li ZY, Ni S et al. Analysis of adenovirus sequestration in the liver, transduction of hepatic cells, and innate toxicity after injection of fiber-modified vectors. J Virol 2004; 78:5368–5381.

    Article  PubMed  CAS  Google Scholar 

  31. Marshall P, Rohlmann A, Nussenzweig V et al. Plasmodium sporozoites invade cells with targeted deletions in the LDL receptor related protein. Mol Biochem Parasitol 2000; 106:293–298.

    Article  PubMed  CAS  Google Scholar 

  32. Usynin I, Klotz C, Frevert U. Malaria circumsporozoite protein inhibits the respiratory burst in Kupffer cells. Submitted.

    Google Scholar 

  33. Moestrup SK, Gliemann J, Pallesen G. Distribution of the a2-macroglobulin receptor / low density lipoprotein receptor-related protein in human tissues. Cell Tissue Res 1992; 269:375–382.

    Article  PubMed  CAS  Google Scholar 

  34. Mazier D, Collins WE, Mellouk S et al. Plasmodium ovale: In vitro development of hepatic stages. Exp Parasitol 1987; 64:393–400.

    Article  PubMed  CAS  Google Scholar 

  35. Millet P, Collins WE, Fisk TL et al. In vitro cultivation of exoerythrocytic stages of the human malaria parasite Plasmodium malariae. Am J Trop Med Hyg 1988; 38:470–473.

    PubMed  CAS  Google Scholar 

  36. Millet P, Fisk TL, Collins WE et al. Cultivation of exoerythrocytic stages of Plasmodium cynomolgi, P. knowlesi, P. coatneyi, and P. inui in Macaca mulatta hepatocytes. Am J Trop Med Hyg 1988; 39:529–534.

    PubMed  CAS  Google Scholar 

  37. Karnasuta C, Pavanand K, Chantakulkij S et al. Complete development of the liver stage of Plasmodium falciparum in a human hepatoma cell line. Am J Trop Med Hyg 1995; 53:607–611.

    PubMed  CAS  Google Scholar 

  38. Karnasuta C, Watt G. Enhanced detection of Plasmodium vivax liver stages by cytocentrifugation. Parasitol Today 1996; 12:451–453.

    Article  PubMed  CAS  Google Scholar 

  39. Sinden RE, Suhrbier A, Davies CS et al. The development and routine application of high-density exoerythrocytic-stage culture of Plasmodium berghei. WHO Bulletin 1990; 68(Suppl):115–125.

    Google Scholar 

  40. Calvo-Calle JM, Moreno A, Eling WMC et al. In vitro development of infectious liver stages of P. yoelii and P. berghei malaria in human cell lines. Exp Parasitol 1994; 79:362–373.

    Article  PubMed  CAS  Google Scholar 

  41. Mota MM, Rodríguez A. Invasion of mammalian host cells by Plasmodium sporozoites. BioEssays 2002; 24:149–156.

    Article  PubMed  Google Scholar 

  42. Hollingdale MR. Biology and immunology of sporozoite invasion of liver cells and exoerythrocytic development of malaria parasites. Prog Allergy 1988; 41:15–48.

    PubMed  CAS  Google Scholar 

  43. Hollingdale MR. Malaria and the liver. Hepatology 1985; 5:327–335.

    Article  PubMed  CAS  Google Scholar 

  44. Pradel G, Frevert U. Plasmodium sporozoites actively enter and pass through Kupffer cells prior to hepatocyte invasion. Hepatology 2001; 33:1154–1165.

    Article  PubMed  CAS  Google Scholar 

  45. Meis JFGM, Verhave JP, Brouwer A et al. Electron microscopic studies on the interaction of rat Kupffer cells and Plasmodium berghei sporozoites. Z Parasitenkd 1985; 71:473–483.

    Article  PubMed  CAS  Google Scholar 

  46. Meis JFGM, Verhave JP, Jap PHK et al. An ultrastructural study on the role of Kupffer cells in the process of infection by Plasmodium berghei sporozoites in rats. Parasitology 1983; 86:231–242.

    Article  PubMed  Google Scholar 

  47. Ishino T, Chinzei H, Yuda M. 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 2005; 7:199–208.

    Article  PubMed  CAS  Google Scholar 

  48. Ishino T, Yano K, Chinzei Y et al. Cell-passage activity is required for the malarial parasite to cross the liver sinusoidal cell layer. PLoS Biol 2004; 2:E4.

    Article  PubMed  CAS  Google Scholar 

  49. Sinden RE, Smith JE. 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. ActaTrop 1982; 39:11–27.

    Google Scholar 

  50. Verhave JP, Meuwissen JHET, Golenser J. The dual role of macrophages in the sporozoite-induced malaria infection. A hypothesis. Int J nucl Med Biol 1980; 7:149–156.

    Article  PubMed  CAS  Google Scholar 

  51. Vreden SGS, Sauerwein RW, Verhave JP et al. Kupffer cell elimination enhances development of liver schizonts of Plasmodium berghei in rats. Infect Immun 1993; 61:1936–1939.

    PubMed  CAS  Google Scholar 

  52. Gosset P, Lassalle P, Vanhée D et al. Production of tumor necrosis factor-α and interleukin-6 by human alveolar macrophages exposed in vitro to coal mine dust. Am J Resp Cell Mol Biol 1991; 5:431–436.

    CAS  Google Scholar 

  53. Braverman IM. Ultrastructure and organization of the cutaneous microvasculature in normal and pathologic states. J Invest Dermatol 1989; 93:2S–9S.

    Article  PubMed  CAS  Google Scholar 

  54. Perlmutter LS, Chui HC. Microangiopathy, the vascular basement membrane and Alzheimer’s disease: A review. Brain Res Bull 1990; 24:677–686.

    Article  PubMed  CAS  Google Scholar 

  55. Nerlich AG, Schleicher E. Identification of lymph and blood capillaries by immunohistochemical staining for various basement membrane components. Histochemistry 1991; 96:449–453.

    Article  PubMed  CAS  Google Scholar 

  56. Erhard H, Rietveld FJ, Brocker EB et al. Phenotype of normal cutaneous microvasculature. Immunoelectron microscopic observations with emphasis on the differences between blood vessels and lymphatics. J Invest Dermatol 1996; 106:135–140.

    Article  PubMed  CAS  Google Scholar 

  57. Tilton RG. Capillary pericytes: Perspectives and future trends. J Electron Microsc Tech 1991; 19:327–344.

    Article  PubMed  CAS  Google Scholar 

  58. Sims DE. Diversity within pericytes. Clin Exp Pharmacol Physiol 2000; 27:842–846.

    Article  PubMed  CAS  Google Scholar 

  59. Gerhardt H, Betsholtz C. Endothelial-pericyte interactions in angiogenesis. Cell Tissue Res 2003; 314:15–23.

    Article  PubMed  Google Scholar 

  60. Schmid-Schönbein GW. Microlymphatics and lymph flow. Physiol Rev 1990; 70:987–1028.

    PubMed  Google Scholar 

  61. Jeltsch M, Tammela T, Alitalo K et al. Genesis and pathogenesis of lymphatic vessels. Cell Tissue Res 2003; 314:69–84.

    Article  PubMed  CAS  Google Scholar 

  62. Zöltzer H. Initial lymphatics—morphology and function of the endothelial cells. Lymphology 2003; 36:7–25.

    PubMed  Google Scholar 

  63. Wisse E, Zanger RB, Charels K et al. The liver sieve: Considerations concerning the structure and function of endothelial fenestrae, the sinusoidal wall and the space of Disse. Hepatology 1985; 5:683–692.

    Article  PubMed  CAS  Google Scholar 

  64. Gumucio JJ, Bilir BM, Moseley RH et al. The biology of the liver cell plate. In: Arias IM, Boyer JL, Fausto N, Jakoby WB, Schachter DA, Shafritz DA, eds. The Liver: Biology and Pathobiology. New York: Raven Press, 1994:1143–1163.

    Google Scholar 

  65. Kuiper J, Brouwer A, Knook DL et al. Kupffer and sinusoidal endothelial cells. In: Arias IM, Boyer JL, Fausto N, Jakoby WB, Schachter DA, Shafritz DA, eds. The Liver: Biology and Pathobiology. New York: Raven Press, Ltd., 1994:791–818.

    Google Scholar 

  66. Wake K, Decker K, Kirn A et al. Cell biology and kinetics of Kupffer cells in the liver. Int Rev Cytol 1989; 118:173–229.

    Article  PubMed  CAS  Google Scholar 

  67. Lee SH, Starkey PM, Gordon S. Quantitative analysis of total macrophage content in adult mouse tissues. Immunochemical studies with monoclonal antibody F4/80. J Exp Med 1985; 161:475–489.

    Article  PubMed  CAS  Google Scholar 

  68. Naito M, Hayashi S, Yoshida H et al. Abnormal differentiation of tissue macrophage populations in ‘osteopetrosis’ (op) mice defective in the production of macrophage colony-stimulating factor. Am J Pathol 1991; 139:657–667.

    PubMed  CAS  Google Scholar 

  69. Witmer-Pack MD, Hughes DA, Schuler G et al. Identification of macrophages and dendritic cells in hte osteopetrotic (op/op) mouse. J Cell Sci 1993; 104:1021–1029.

    PubMed  Google Scholar 

  70. Cecchini MG, Dominguez MG, Mocci S et al. Role of colony stimulating factor-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse. Development 1994; 120:1357–1372.

    PubMed  CAS  Google Scholar 

  71. Verhave JP, Meis JFGM, Boo TMd et al. The delivery of exoerythrocytic parasites of Plasmodium berghei: A hormone controlled process. Ann Soc Beige Med Trop 1985; 65:35–44.

    Google Scholar 

  72. Sleyster EC, Knook DL. Relation between localization and function of rat liver Kupffer cells. Lab Invest 1982; 47:484–490.

    PubMed  CAS  Google Scholar 

  73. Motta PM. The three-dimensional microanatomy of the liver. Arch Histol Jpn 1984; 47:1–30.

    Article  PubMed  CAS  Google Scholar 

  74. Motta PM, Muto M, Fujita T. The vascular system. In: Motta PM, Muto M, Fujita T, eds. The Liver: An Atlas of Electron Microscopy. Tokyo: Igaku-Shoin, 1978:83–118.

    Google Scholar 

  75. Arii S, Imamura M. Physiological role of sinusoidal endothelial cells and Kupffer cells and their implication in the pathogenesis of liver injury. J Hepatobiliary Pancreat Surg 2000; 7:40–48.

    Article  PubMed  CAS  Google Scholar 

  76. McCuskey RS, Reilly FD. Hepatic microvasculature: Dynamic structure and its regulation. Semin Liver Dis 1993; 13:1–12.

    Article  PubMed  CAS  Google Scholar 

  77. Bouwens L, Wisse E. The origin of Kupffer cells and their relationship to hepatocytes. In: Billiar TR, Curran RD, eds. Hepatocyte and Kupffer Cell Interactions. Boca Raton: CRC Press, 1992:3–21.

    Google Scholar 

  78. Wisse E. Observations on the fine structure and peroxidase cytochemistry of normal rat liver Kupffer cells. J Ultrastruct Res 1974; 46:393–426.

    Article  PubMed  CAS  Google Scholar 

  79. Wisse E. Ultrastructure and function of Kupffer cells and other sinusoidal cells in the liver. In: Wisse E, Knook DL, eds. Kupffer Cells and other Liver Sinusoidal Cells. Amsterdam: Elsevier/North Holland Biomedical Press, 1977:33–60.

    Google Scholar 

  80. Wisse E, Braet F, Luo D et al. Structure and function of sinusoidal lining cells in the liver. Toxicol Pathol 1996; 24:100–111.

    Article  PubMed  CAS  Google Scholar 

  81. Mackay IR. Hepatoimmunology: A perspective. Immunol Cell Biol 2002; 80:36–44.

    Article  PubMed  Google Scholar 

  82. Bertolino P, McCaughan GW, Bowen DG. Role of primary intrahepatic T-cell activation in the ‘liver tolerance effect’. Immunol Cell Biol 2002; 80:84–92.

    Article  PubMed  Google Scholar 

  83. MacSween RNM, Desmet VJ, Roskams T et al. Developmental anatomy and normal structure. In: MacSween RNM, Burt AD, Portmann BC, Ishak K, Scheuer GPJ, Anthony PP, eds. Pathology of the Liver. New York: Churchill Livingstone, 2002:1–66.

    Google Scholar 

  84. Markiewski MM, DeAngelis RA, Lambris JD. Liver inflammation and regeneration: Two distinct biological phenomena or parallel pathophysiologic processes? Mol Immunol 2006; 43:45–56.

    Article  PubMed  CAS  Google Scholar 

  85. MacPhee PJ, Schmidt EE, Groom AC. Evidence for Kupffer cell migration along liver sinusoids, from high-resolution in vivo microscopy. Am J Physiol 1992; 263:G17–23.

    PubMed  CAS  Google Scholar 

  86. Faust N, Varas F, Kelly LM et al. Insertion of green fluorescent protein into the lysozyme gene creates mice with green fluorescent granulocytes and macrophages. Blood 2000; 96:719–726.

    PubMed  CAS  Google Scholar 

  87. Baer K, Roosevelt M, Van Rooijen N et al. Kupffer cells are obligatory for Plasmodium sporozoite infection of the liver. Cell Microbiol 2006; 8:online early.

    Google Scholar 

  88. McCuskey RS. Morphological mechanism for regulating blood flow through hepatic sinusoids. Liver 2000; 20:3–7.

    Article  PubMed  CAS  Google Scholar 

  89. McCuskey RS. The hepatic microvascular system. In: Arias IM, Boyer JL, Fausto N, Jakoby WB, Schachter DA, Shafritz DA, eds. The Liver: Biology and Pathobiology. New York: Raven Press, 1994:1089–1106.

    Google Scholar 

  90. Bouwens L, Baekeland M, De Zanger R et al. Quantitation, tissue distribution and proliferation kinetics of Kupffer cells in normal rat liver. Hepatology 1986; 6:718–722.

    Article  PubMed  CAS  Google Scholar 

  91. Crofton RW, Diesselhoff-den Dulk MM, van Furth R. The origin, kinetics, and characteristics of the Kupffer cells in the normal steady state. J Exp Med 1978; 148:1–17.

    Article  PubMed  CAS  Google Scholar 

  92. Diesselhoff-den Dulk MM, Crofton RW, van Furth R. Origin and kinetics of Kupffer cells during an acute inflammatory response. Immunology 1979; 37:7–14.

    PubMed  CAS  Google Scholar 

  93. van Furth R. [Characteristics of mononuclear phagocytes in their normal state and in inflammation]. Folia Haematol Int Mag Klin Morphol Blutforsch 1984; 111:131–140.

    PubMed  Google Scholar 

  94. Hardonk MJ, Dijkhuis FW, Grond J et al. Evidence for a migratory capability of rat Kupffer cells to portal tracts and hepatic lymph nodes. Virchows Arch B Cell Pathol Incl Mol Pathol 1986; 51:429–442.

    Article  PubMed  CAS  Google Scholar 

  95. McCuskey RS. Hepatic and splanchnic microvascular responses to inflammation and shock. Hepatogastroenterology 1999; 46(Suppl 2):1464–1467.

    PubMed  Google Scholar 

  96. Lawson JA, Farhood A, Hopper RD et al. The hepatic inflammatory response after acetaminophen overdose: Role of neutrophils. Toxicol Sci 2000; 54:509–516.

    Article  PubMed  CAS  Google Scholar 

  97. Wiktor-Jedrzejczak W, Gordon S. Cytokine regulation of the macrophage (Mτ) system studied using the colony stimulating factor-1-deficient op/op mouse. Physiol Rev 1996; 76:927–947.

    PubMed  CAS  Google Scholar 

  98. Nishioji K, Okanoue T, Mori T et al. Experimental liver injury induced by Propionibacterium acnes and lipopolysaccharide in macrophage colony stimulating factor-deficient osteopetrotic (op/op) mice. Dig Dis Sci 1999; 44:1975–1984.

    Article  PubMed  CAS  Google Scholar 

  99. Szperl M, Ansari AA, Urbanowska E et al. Increased resistance of CSF-1-deficient, macrophage-deficient, TNF alpha-deficient, and IL-1 alpha-deficient op/op mice to endotoxin. Ann NYAcad Sci 1995; 762:499–501.

    Article  CAS  Google Scholar 

  100. Shultz LD, Sidman CL. Genetically determined murine models of immunodeficiency. Annu Rev Immunol 1987; 5:367–403.

    Article  PubMed  CAS  Google Scholar 

  101. Knight TR, Jaeschke H. Peroxynitrite formation and sinusoidal endothelial cell injury during acetaminophen-induced hepatotoxicity in mice. Comp Hepatol 2004; 3(Suppl 1):S46.

    Article  PubMed  Google Scholar 

  102. Yee SB, Hanumegowda UM, Copple M BL et al. Endothelial cell injury and coagulation system activation during synergistic hepatotoxicity from monocrotaline and bacterial lipopolysaccharide coexposure. Toxicol Sci 2003; 74:203–214.

    Article  PubMed  CAS  Google Scholar 

  103. DeLeve LD, Ito Y, Bethea NW et al. Embolization by sinusoidal lining cells obstructs the micro-circulation in rat sinusoidal obstruction syndrome. Am J Physiol Gastrointest Liver Physiol 2003; 284:G1045–1052.

    PubMed  CAS  Google Scholar 

  104. Naito M, Hasegawa G, Takahashi K. Development, differentiation, and maturation of Kupffer cells. Microsc Res Tech 1997; 39:350–364.

    Article  PubMed  CAS  Google Scholar 

  105. Mota MM, Pradel G, Vanderberg JP et al. Migration of Plasmodium sporozoites through cells before infection. Science 2001; 291:141–144.

    Article  PubMed  CAS  Google Scholar 

  106. Silvie O, Greco C, Franetich JF et al. Expression of human CD81 differently affects host cell susceptibility to malaria sporozoites depending on the Plasmodium species. Cell Microbiol 2006; 8:1134–1146.

    Article  PubMed  CAS  Google Scholar 

  107. Silvie O, Rubinstein E, Franetich JF et al. Hepatocyte CD81 is required for Plasmodium falciparum and Plasmodium yoelii sporozoite infectivity. Nature Med 2002; 9:93–96.

    PubMed  Google Scholar 

  108. Mota MM, Hafalla JC, Rodriguez A. Migration through host cells activates Plasmodium sporozoi-tes for infection. Nat Med 2002; 8:1318–1322.

    Article  PubMed  CAS  Google Scholar 

  109. Ishino T, Chinzei Y, Yuda M. Two proteins with 6-cys motifs are required for malarial parasites to commit to infection of the hepatocyte. Mol Microbiol 2005; 58:1264–1275.

    Article  PubMed  CAS  Google Scholar 

  110. Bhanot P, Schauer K, Coppens I et al. A surface phospholipase is involved in the migration of Plasmodium sporozoites through cells. J Biol Chem 2005; 280:6752–6760.

    Article  PubMed  CAS  Google Scholar 

  111. Stewart MJ, Schulman S, Vanderberg JP. Rhoptry secretion of membrane whorls by Plasmodium berghei sporozoites. J Protozool 1985; 32:280–283.

    PubMed  CAS  Google Scholar 

  112. Silvie O, Charrin S, Billard M et al. Cholesterol contributes to the organization of tetraspanin-enriched microdomains and to CD81-dependent infection by malaria sporozoites. J Cell Sci 2006; 119:1992–2002.

    Article  PubMed  CAS  Google Scholar 

  113. Kaiser K, Camargo N, Kappe SH. Transformation of sporozoites into early exoerythrocytic malaria parasites does not require host cells. J Exp Med 2003; 197:1045–1050.

    Article  PubMed  CAS  Google Scholar 

  114. Rathore D, Sacci JB, de la Vega P et al. Binding and invasion of liver cells by Plasmodium falciparum sporozoites. J Biol Chem 2002; 277:7092–7098.

    Article  PubMed  CAS  Google Scholar 

  115. Sinnis P, Clavijo P, Fenyö D et al. Structural and functional properties of region-II plus of the malaria circumsporozoite protein. J Exp Med 1994; 180:297–306.

    Article  PubMed  CAS  Google Scholar 

  116. Tewari R, Spaccapelo R, Bistoni F et al. Function of region I and II adhesive motifs of Plasmodium falciparum circumsporozoite protein in sporozoite motility and infectivity. J Biol Chem 2002; 277:47613–47618.

    Article  PubMed  CAS  Google Scholar 

  117. Coppi A, Pinzon-Ortiz C, Hutter C et al. The Plasmodium circumsporozoite protein is proteolyti-cally processed during cell invasion. J Exp Med 2005; 201:27–33.

    Article  PubMed  CAS  Google Scholar 

  118. Persson C, Oliveira GA, Sultan AA et al. Cutting edge: A new tool to evaluate human preerythrocytic malaria vaccines: rodent parasites bearing a hybrid Plasmodium falciparum circumsporozoite protein. J Immunol 2002; 169:6681–6685.

    PubMed  CAS  Google Scholar 

  119. Tewari R, Rathore D, Crisanti A. Motility and infectivity of Plasmodium berghei sporozoites expressing avian Plasmodium gallinaceum circumsporozoite protein. Cell Microbiol 2005; 7:699–707.

    Article  PubMed  CAS  Google Scholar 

  120. Huff CG. Exoerythrocytic stages of avian and reptilian malarial parasites. Exp Parasitol 1969; 24:383–421.

    Article  PubMed  CAS  Google Scholar 

  121. Frevert U, Bennett B, Spaeth G et al. Exoerythrocytic development of Plasmodium gallinaceum in the domestic chicken. In preparation.

    Google Scholar 

  122. McCutchan TF, Kissinger JC, Touray MG et al. Comparison of circumsporozoite proteins from avian and mammalian malarias: Biological and phylogenetic implications. Proc Natl Acad Sci USA 1996; 93:11889–11894.

    Article  PubMed  CAS  Google Scholar 

  123. Sultan AA, Thathy V, Frevert U et al. TRAP is necessary for gliding motility and infectivity of Plasmodium sporozoites. Cell 1997; 90:511–522.

    Article  PubMed  CAS  Google Scholar 

  124. Gantt SM, Clavijo P, Bai X et al. Cell adhesion to a motif shared by the malaria circumsporozoite protein and thrombospondin is mediated by its glycosaminoglycan-binding region and not by CSVTCG. J Biol Chem 1997; 272:19205–19213.

    Article  PubMed  CAS  Google Scholar 

  125. Matuschewski K, Nunes AC, Nussenzweig V et al. Plasmodium sporozoite invasion into insect and mammalian cells is directed by the same dual binding system. EMBO J. 2002; 21:1–10.

    Article  Google Scholar 

  126. Sultan AA, Briones MRS, Gerwin N et al. Sporozoites of Plasmodium yoelii infect mice with targeted deletions in ICAM-1 and ICAM-2 or complement components C3 and C4. Mol Biochem Parasitol 1997; 88:263–266.

    Article  PubMed  CAS  Google Scholar 

  127. Wengelnik K, Spaccapelo R, Robson KJH et al. The A-domain and the thrombospondin-related motif of Plasmodium falciparum TRAP are implicated in the invasion process of mosquito salivary glands. EMBO J 1999; 18:5195–5204.

    Article  PubMed  CAS  Google Scholar 

  128. Sibley LD. Intracellular parasite invasion strategies. Science 2004; 304:248–253.

    Article  PubMed  CAS  Google Scholar 

  129. Jethwaney D, Lepore T, Hassan S et al. Fetuin-A, a hepatocyte-specific protein that binds Plasmodium berghei thrombospondin-related adhesive protein: A potential role in infectivity. Infect Immun 2005; 73:5883–5891.

    Article  PubMed  CAS  Google Scholar 

  130. Silvie O, Franetich JF, Charrin S et al. A role for apical membrane antigen 1 during invasion of hepatocytes by Plasmodium falciparum sporozoites. J Biol Chem 2004; 279:9490–9496.

    Article  PubMed  CAS  Google Scholar 

  131. Barragan A, Brossier F, Sibley LD. Transepithelial migration of Toxoplasma gondii involves an interaction of intercellular adhesion molecule 1 (ICAM-1) with the parasite adhesin MIC2. Cell Microbiol 2005; 7:561–568.

    Article  PubMed  CAS  Google Scholar 

  132. Lalor PF, Shields P, Grant A et al. Recruitment of lymphocytes to the human liver. Immunol Cell Biol 2002; 80:52–64.

    Article  PubMed  CAS  Google Scholar 

  133. Smedsrod B, De Bleser PJ, Braet F et al. Cell biology of liver endothelial and Kupffer cells. Gut 1994; 35:1509–1516.

    Article  PubMed  CAS  Google Scholar 

  134. Wang HH, Nance DM, Orr FW. Murine hepatic microvascular adhesion molecule expression is inducible and has a zonal distribution. Clin Exp Metastasis 1999; 17:149–155.

    Article  PubMed  CAS  Google Scholar 

  135. van Dijk MR, Douradinha B, Franke-Fayard B et al. Genetically attenuated, P36p-deficient malarial sporozoites induce protective immunity and apoptosis of infected liver cells. Proc Natl Acad Sci USA 2005; 102:12194–12199.

    Article  PubMed  CAS  Google Scholar 

  136. Nussenzweig V, Nussenzweig RS. Rationale for the development of an engineered sporozoite malaria vaccine. Adv Immunol 1989; 45:283–334.

    Article  PubMed  CAS  Google Scholar 

  137. Mueller AK, Labaied M, Kappe SH et al. Genetically modified Plasmodium parasites as a protective experimental malaria vaccine. Nature 2005; 433:164–167.

    Article  PubMed  CAS  Google Scholar 

  138. Mueller AK, Camargo N, Kaiser K et al. Plasmodium liver stage developmental arrest by depletion of a protein at the parasite-host interface. Proc Natl Acad Sci USA 2005; 102:3022–3027.

    Article  PubMed  CAS  Google Scholar 

  139. Carrolo M, Giordano S, Cabrita-Santos L et al. Hepatocyte growth factor and its receptor are required for malaria infection. Nature Med 2003; 9:1363–1369.

    Article  PubMed  CAS  Google Scholar 

  140. Fausto N. Liver regeneration. J Hepatol 2000; 32:19–31.

    Article  PubMed  CAS  Google Scholar 

  141. Rosario M, Birchmeier W. How to make tubes: Signaling by the Met receptor tyrosine kinase. Trends Cell Biol 2003; 13:328–335.

    Article  PubMed  CAS  Google Scholar 

  142. Zarnegar R, DeFrances MC, Michalopoulos GK. Hepatocyte growth factor. In: Arias IM, Boyer JL, Fausto N, Jakoby WB, Schachter DA, Shafritz DA, eds. The Liver: Biology and Pathobiology. New York: Raven Press, 1994:1047–1057.

    Google Scholar 

  143. Fausto N, Campbell JS. The role of hepatocytes and oval cells in liver regeneration and repopulation. Mech Dev 2003; 120:117–130.

    Article  PubMed  CAS  Google Scholar 

  144. Knolle PA, Gerken G. Local control of the immune response in the liver. Immunol Rev 2000; 174:21–34.

    Article  PubMed  CAS  Google Scholar 

  145. Danforth HD, Aikawa M, Cochrane AH et al. Sporozoites of mammalian malaria: Attachment to, interiorization and fate within macrophages. J Protozool 1980; 27:193–202.

    PubMed  CAS  Google Scholar 

  146. Vanderberg JP, Chew S, Stewart MJ. Plasmodium sporozoite interactions with macrophages in vitro: A videomicroscopic analysis. J Protozool 1990; 37:528–536.

    PubMed  CAS  Google Scholar 

  147. Vanderberg JP, Stewart MJ. Plasmodium-sporozoite-host cell interactions during sporozoite invasion. WHO Bulletin 1990; 68(Suppl.): 74–79.

    Google Scholar 

  148. Smith JE, Alexander J. Evasion of macrophage microbicidal mechanisms by mature sporozoites of Plasmodium yoelii yoelii. Parasitology 1986; 93:33–38.

    Article  PubMed  Google Scholar 

  149. Steers N, Schwenk R, Bacon DJ et al. The immune status of Kupffer cells profoundly influences their responses to infectious Plasmodium berghei sporozoites. Eur J Immunol 2005; 35:2335–2346.

    Article  PubMed  CAS  Google Scholar 

  150. Tarun AS, Baer K, Dumpit RF et al. Quantitative isolation and in vivo imaging of malaria parasite liver stages. Int J Parasitol 2006; 36:1283–1293.

    Article  PubMed  CAS  Google Scholar 

  151. Sturm A, Amino R, van de Sand C et al. Manipulaation of host hepatocytes by the malaria parasite for delivery into liver sinusoids. Science 2006; 313:1287–1290.

    Article  PubMed  CAS  Google Scholar 

  152. Bray RS. Studies on the exo-erythrocytic cycle in the genus Plasmodium. Mem London School Hyg trop Med 1957; 12:1–92.

    Google Scholar 

  153. Cantor HM, Dumont AE. Hepatic suppression of sensitization to antigen absorbed into the portal system. Nature 1967; 215:744–745.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ute Frevert .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Landes Bioscience and Springer Science+Business Media

About this chapter

Cite this chapter

Frevert, U., Usynin, I., Baer, K., Klotz, C. (2008). Plasmodium Sporozoite Passage across the Sinusoidal Cell Layer. In: Burleigh, B.A., Soldati-Favre, D. (eds) Molecular Mechanisms of Parasite Invasion. Subcellular Biochemistry, vol 47. Springer, New York, NY. https://doi.org/10.1007/978-0-387-78267-6_15

Download citation

Publish with us

Policies and ethics