Cholesterol-dependent anaplasma phagocytophilum exploits the low-density lipoprotein uptake pathway

PLoS Pathogens

Volumn 5, Issue 3, 2009, Pages

  Xiong, Qingming ^a   Lin, Mingqun ^a   Rikihisa, Yasuko ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; STEROL REGULATORY ELEMENT BINDING PROTEIN; CHOLESTEROL; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE;

3' UNTRANSLATED REGION; ANAPLASMA PHAGOCYTOPHILUM; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN GRANULOCYTIC ANAPLASMOSIS; LYSOSOME MEMBRANE; PROMYELOCYTIC LEUKEMIA; PROTEIN EXPRESSION; PROTEIN TRANSPORT; RNA STABILITY; UPREGULATION; CELL STRAIN HL 60; EHRLICHIOSIS; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANAPLASMA PHAGOCYTOPHILUM; BACTERIA (MICROORGANISMS); EUKARYOTA;

ANAPLASMA PHAGOCYTOPHILUM; BLOTTING, WESTERN; CHOLESTEROL; EHRLICHIOSIS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLUORESCENT ANTIBODY TECHNIQUE; HL-60 CELLS; HUMANS; LIPOPROTEINS, LDL; MAP KINASE KINASE KINASES; RECEPTORS, LDL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 63549109967     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000329     Document Type: Article

References (69)

1. Maxfield FR, Tabas I (2005) Role of cholesterol and lipid organization in disease. Nature 438: 612-621.
2. Ikonen E (2008) Cellular cholesterol trafficking and compartmentalization. Nat Rev Mol Cell Biol 9: 125-138.
3. Brown MS, Goldstein JL (1997) The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89:331-340.
4. Brown MS, Goldstein JL (1999) A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood. Proc Natl Acad Sci USA 96: 11041-11048.
5. Goluszko P, Nowicki B (2005) Membrane cholesterol: a crucial molecule affecting interactions of microbial pathogens with mammalian cells. Infect Immun 73: 7791-7796.
6. Watarai M, Makino S, Michikawa M, Yanagisawa K, Murakami S, et al. (2002) Macrophage plasma membrane cholesterol contributes to Brucella abortus infection of mice. Infect Immun 70: 4818-4825.
7. Howe D, Heinzen RA (2006) Coxiella burnetii inhabits a cholesterol-rich vacuole and influences cellular cholesterol metabolism. Cell Microbiol 8:496-507.
8. Garner MJ, Hayward RD, Koronakis V (2002) The Salmonella pathogenicity island 1 secretion system directs cellular cholesterol redistribution during mammalian cell entry and intracellular trafficking. Cell Microbiol 4: 153-165.
9. Dumler JS, Barbet AF, Bekker CP, Dasch GA, Palmer GH, et al. (2001) Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and 'HGE agent' as subjective synonyms of Ehrlichia phagocytophila. Int J Syst Evol Microbiol 51:2145-2165.
10. Herron MJ, Ericson ME, Kurtti TJ, Munderloh UG (2005) The interactions of Anaplasma phagocytophilum, endothelial cells, and human neutrophils. Ann N Y Acad Sci 1063: 374-382.
11. Munderloh UG, Lynch MJ, Herron MJ, Palmer AT, Kurtti TJ, et al. (2004) Infection of endothelial cells with Anaplasma marginale and A. phagocytophilum. Vet Microbiol 101: 53-64.
12. Bakken JS, Dumler JS (2000) Human granulocytic ehrlichiosis. Clin Infect Dis 31: 554-560.
13. Lin M, Rikihisa Y (2003) Ehrlichia chaffeensis and Anaplasma phagocytophilum lack genes for lipid A biosynthesis and incorporate cholesterol for their survival. Infect Immun 71: 5324-5331.
14. Xiong Q, Wang X, Rikihisa Y (2007) High-cholesterol diet facilitates Anaplasma phagocytophilum infection and up-regulates macrophage inflammatory protein- 2 and CXCR2 expression in apolipoprotein E-deficient mice. J Infect Dis 195:1497-1503.
15. Lin M, Rikihisa Y (2003) Obligatory intracellular parasitism by Ehrlichia chaffeensis and Anaplasma phagocytophilum involves caveolae and glycosylphosphatidylinositol-anchored proteins. Cell Microbiol 5: 809-820.
16. Lange Y (1991) Disposition of intracellular cholesterol in human fibroblasts. J Lipid Res 32: 329-339.
17. Tabas I (2002) Consequences of cellular cholesterol accumulation: basic concepts and physiological implications. J Clin Invest 110: 905-911.
18. Severs NJ (1997) Cholesterol cytochemistry in cell biology and disease. Subcell Biochem 28: 477-505.
19. Hao M, Lin SX, Karylowski OJ, Wustner D, McGraw TE, et al. (2002) Vesicular and non-vesicular sterol transport in living cells. The endocytic recycling compartment is a major sterol storage organelle. J Biol Chem 277:609-617.
20. Hybiske K, Stephens RS (2007) Mechanisms of host cell exit by the intracellular bacterium Chlamydia. Proc Natl Acad Sci U S A 104: 11430-11435.
21. Brown MS, Goldstein JL (1986) A receptor-mediated pathway for cholesterol homeostasis. Science 232: 34-47.
22. Chang TY, Chang CC, Ohgami N, Yamauchi Y (2006) Cholesterol sensing,
23. trafficking, and esterification. Annu Rev Cell Dev Biol 22: 129-157.
24. Jouni ZE, McNamara DJ (1991) Lipoprotein receptors of HL-60 macrophages. Effect of differentiation with tetramyristic phorbol acetate and 1,25-dihydroxyvitamin D3. Arterioscler Thromb 11: 995-1006.
25. Lange Y, Ye J, Chin J (1997) The fate of cholesterol exiting lysosomes. J Biol Chem 272: 17018-17022.
26. Liscum L, Faust JR (1989) The intracellular transport of low density lipoprotein- derived cholesterol is inhibited in Chinese hamster ovary cells cultured with 3- beta-[2-(diethylamino)ethoxy]androst-5-en-17-one. J Biol Chem 264:11796-11806.
27. Alberts AW, Chen J, Kuron G, Hunt V, HuffJ, et al. (1980) Mevinolin: a highly potent competitive inhibitor of hydroxymethylglutaryl-coenzyme A reductase and a cholesterol-lowering agent. Proc Natl Acad Sci U S A 77: 3957-3961.
28. Lange Y, Steck TL (1994) Cholesterol homeostasis. Modulation by amphiphiles. J Biol Chem 269: 29371-29374.
29. Stephan ZF, Yurachek EC (1993) Rapid fluorometric assay of LDL receptor activity by DiI-labeled LDL. JLipid Res 34: 325-330.
30. Mott J, Barnewall RE, Rikihisa Y (1999) Human granulocytic ehrlichiosis agent and Ehrlichia chaffeensis reside in different cytoplasmic compartments in HL-60 cells. Infect Immun 67: 1368-1378.
31. Castoreno AB, Wang Y, Stockinger W, Jarzylo LA, Du H, et al. (2005) Transcriptional regulation of phagocytosis-induced membrane biogenesis by sterol regulatory element binding proteins. Proc Natl Acad Sci U S A 102:13129-13134.
32. Shimano H (2001) Sterol regulatory element-binding proteins (SREBPs): transcriptional regulators oflipid synthetic genes. Prog Lipid Res 40: 439-452.
33. Horton JD, Goldstein JL, Brown MS (2002) SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 109:1125-1131.
34. Wang X, Zelenski NG, Yang J, Sakai J, Brown MS, et al. (1996) Cleavage of sterol regulatory element binding proteins (SREBPs) by CPP32 during apoptosis. Embo J15: 1012-1020.
35. Kong WJ, Liu J, Jiang JD (2006) Human low-density lipoprotein receptor gene and its regulation. J Mol Med 84: 29-36.
36. Yamamoto T, Davis CG, Brown MS, Schneider WJ, Casey ML, et al. (1984) The human LDL receptor: a cysteine-rich protein with multiple Alu sequences in its mRNA. Cell 39: 27-38.
37. Wilson GM, Vasa MZ, Deeley RG (1998) Stabilization and cytoskeletal-association of LDL receptor mRNA are mediated by distinct domains in its 3′ untranslated region. J Lipid Res 39: 1025-1032.
38. Kong W, Wei J, Abidi P, Lin M, Inaba S, et al. (2004) Berberine is a novel cholesterol-lowering drug working through a unique mechanism distinct from statins. Nat Med 10: 1344-1351.
39. Mehta KD (2002) Role ofmitogen-activated protein kinases and protein kinase C in regulating low-density lipoprotein receptor expression. Gene Expr 10:153-164.
40. Catron DM, Lange Y, Borensztajn J, Sylvester MD, Jones BD, et al. (2004) Salmonella enterica serovar Typhimurium requires nonsterol precursors of the cholesterol biosynthetic pathway for intracellular proliferation. Infect Immun 72:1036-1042.
41. Catron DM, Sylvester MD, Lange Y, Kadekoppala M, Jones BD, et al. (2002) The Salmonella-containing vacuole is a major site of intracellular cholesterol accumulation and recruits the GPI-anchored protein CD55. Cell Microbiol 4:315-328.
42. Carabeo RA, Mead DJ, Hackstadt T (2003) Golgi-dependent transport of cholesterol to the Chlamydia trachomatis inclusion. Proc Natl Acad Sci U S A 100: 6771-6776.
43. Beatty WL (2006) Trafficking from CD63-positive late endocytic multivesicular bodies is essential for intracellular development of Chlamydia trachomatis. J Cell Sci 119: 350-359.
44. Cocchiaro JL, Kumar Y, Fischer ER, Hackstadt T, Valdivia RH (2008) Cytoplasmic lipid droplets are translocated into the lumen of the Chlamydia trachomatis parasitophorous vacuole. Proc Natl Acad Sci U S A 105:9379-9384.
45. Coppens I, Sinai AP, Joiner KA (2000) Toxoplasma gondii exploits host low- density lipoprotein receptor-mediated endocytosis for cholesterol acquisition. J Cell Biol 149: 167-180.
46. Coppens I, Dunn JD, Romano JD, Pypaert M, Zhang H, et al. (2006) Toxoplasma gondii sequesters lysosomes from mammalian hosts in the vacuolar space. Cell 125: 261-274.
47. Mordue DG, Hakansson S, Niesman I, Sibley LD (1999) Toxoplasma gondii resides in a vacuole that avoids fusion with host cell endocytic and exocytic vesicular trafficking pathways. Exp Parasitol 92: 87-99.
48. Murata M, Peranen J, Schreiner R, Wieland F, Kurzchalia TV, et al. (1995) VIP21/caveolin is a cholesterol-binding protein. Proc Natl Acad Sci USA 92: 10339-10343.
49. Ikonen E, Parton RG (2000) Caveolins and cellular cholesterol balance. Traffic 1: 212-217.
50. Borregaard N, Sorensen OE, Theilgaard-Monch K (2007) Neutrophil granules: a library of innate immunity proteins. Trends Immunol 28: 340-345.
51. Manzano-Roman R, Almazan C, Naranjo V, Blouin EF, Kocan KM, et al. (2008) Expression of perilipin in human promyelocytic cells in response to Anaplasma phagocytophilum infection results in modified lipid metabolism. J Med Microbiol 57: 159-163.
52. Goto D, Okimoto T, Ono M, Shimotsu H, Abe K, et al. (1997) Upregulation of low density lipoprotein receptor by gemfibrozil, a hypolipidemic agent, in human hepatoma cells through stabilization of mRNA transcripts. Arterioscler Thromb Vasc Biol 17: 2707-2712.
53. Abidi P, Zhou Y, Jiang JD, Liu J (2005) Extracellular signal-regulated kinase- dependent stabilization of hepatic low-density lipoprotein receptor mRNA by herbal medicine berberine. Arterioscler Thromb Vasc Biol 25: 2170-2176.
54. Lee HC, Kioi M, Han J, Puri RK, Goodman JL (2008) Anaplasma phagocytophilum-induced gene expression in both human neutrophils and HL-60 cells. Genomics.
55. Tapinos N, Rambukkana A (2005) Insights into regulation of human Schwann cell proliferation by Erk1/2 via a MEK-independent and p56Lck-dependent pathway from leprosy bacilli. Proc Natl Acad Sci U S A 102: 9188-9193.
56. Su H, McClarty G, Dong F, Hatch GM, Pan ZK, et al. (2004) Activation of Raf/MEK/ERK/cPLA2 signaling pathway is essential for chlamydial acquisition of host glycerophospholipids. J Biol Chem 279: 9409-9416.
57. Krause BR, Princen HM (1998) Lack of predictability of classical animal models for hypolipidemic activity: a good time for mice? Atherosclerosis 140: 15-24.
58. Kim HY, Rikihisa Y (1998) Characterization of monoclonal antibodies to the 44-kilodalton major outer membrane protein of the human granulocytic ehrlichiosis agent. J Clin Microbiol 36: 3278-3284.
59. Radding CM, Steinberg D (1960) Studies on the synthesis and secretion of serum lipoproteins by rat liver slices. J Clin Invest 39: 1560-1569.
60. Brown MS, Goldstein JL (1974) Suppression of 3-hydroxy-3-methylglutaryl coenzyme A reductase activity and inhibition of growth of human fibroblasts by 7-ketocholesterol. J Biol Chem 249: 7306-7314.
61. Rikihisa Y, Zhi N, Wormser GP, Wen B, Horowitz HW, et al. (1997) Ultrastructural and antigenic characterization of a granulocytic ehrlichiosis agent directly isolated and stably cultivated from a patient in New York state.
62. J Infect Dis 175: 210-213.
63. Rikihisa Y, Zhang Y, Park J (1995) Role of Ca2+ and calmodulin in ehrlichial infection in macrophages. Infect Immun 63: 2310-2316.
64. Teupser D, Thiery J, Walli AK, Seidel D (1996) Determination of LDL- and scavenger-receptor activity in adherent and non-adherent cultured cells with a new single-step fluorometric assay. Biochim Biophys Acta 1303: 193-198.
65. Millard EE, Srivastava K, Traub LM, Schaffer JE, Ory DS (2000) Niemann-pick type C1 (NPC1) overexpression alters cellular cholesterol homeostasis. J Biol Chem 275: 38445-38451.
66. Holla OL, Cameron J, Berge KE, Ranheim T, Leren TP (2007) Degradation of the LDL receptors by PCSK9 is not mediated by a secreted protein acted upon by PCSK9 extracellularly. BMC Cell Biol 8: 9.
67. Beisiegel U, Schneider WJ, Brown MS, Goldstein JL (1982) Immunoblot analysis of low density lipoprotein receptors in fibroblasts from subjects with familial hypercholesterolemia. J Biol Chem 257: 13150-13156.
68. Zhang K, Shan L, Rahman MS, Unruh H, Halayko AJ, et al. (2007) Constitutive and inducible thymic stromal lymphopoietin expression in human airway smooth muscle cells: role in chronic obstructive pulmonary disease. Am J Physiol Lung Cell Mol Physiol 293: L375-382.
69. Lin M, den Dulk-Ras A, Hooykaas PJ, Rikihisa Y (2007) Anaplasma phagocytophilum AnkA secreted by type IV secretion system is tyrosine phosphorylated by Abl-1 to facilitate infection. Cell Microbiol 9: 2644-2657.