Human immunodeficiency virus-1 uses the mannose-6-phosphate receptor to cross the blood-brain barrier

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Dohgu, Shinya ^a   Ryerse, Jan S ^b   Robinson, Sandra M ^b   Banks, William A ^c,d  

^a FUKUOKA UNIVERSITY   (Japan)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CATION; CYCLIC AMP; MANNAN; MANNOSE; MANNOSE 6 PHOSPHATE; MANNOSE OLIGOSACCHARIDE; PLANT LECTIN; PROTAMINE SULFATE; SOMATOMEDIN B RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN REGION; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; VIRUS MORPHOLOGY; VIRUS TRANSMISSION;

ANIMALS; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BRAIN; CALCIUM; CYCLIC AMP; ENDOTHELIAL CELLS; HIV-1; MALE; MICE; RECEPTOR, IGF TYPE 2; SIGNAL TRANSDUCTION; TRANSCYTOSIS; WHEAT GERM AGGLUTININS;

EID: 84862639014     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039565     Document Type: Article

References (49)

1. Marcus CD, Taylor-Robinson SD, Sargentoni J, Ainsworth JG, Frize G, et al. (1998) 1H MR spectroscopy of the brain in HIV-1-seropositive subjects: evidence for diffuse metabolic abnormalities. Metabolic Brain Disease 13: 123-136.
2. Nottet HS, Persidsky Y, Sasseville VG, Nukuna AN, Bock P, et al. (1996) Mechanisms for the transendothelial migration of HIV-1-infected monocytes into brain. The Journal of Immunology 156: 1284-1295.
3. Persidsky Y, Stins M, Way D, Witte MH, Weinand M, et al. (1997) A model for monocyte migration through the blood-brain barrier during HIV-1 encephalitis. The Journal of Immunology 158: 3499-3510.
4. Banks WA, Freed EO, Wolf KM, Robinson SM, Franko M, et al. (2001) Transport of human immunodeficiency virus type 1 pseudoviruses across the blood-brain barrier: role of envelope proteins and adsorptive endocytosis. Journal of Virology 75: 4681-4691.
5. Moses AV, Bloom FE, Pauza CD, Nelson JA, (1993) Human immunodeficiency virus infection of human brain capillary endothelial cells occurs via a CD4/galactosylceramide-independent mechanism. Proceedings of the National Academy of Sciences USA 90: 10474-10478.
6. Banks WA, Kastin AJ, Akerstrom V, (1997) HIV-1 protein gp120 crosses the blood-brain barrier: role of adsorptive endocytosis. Life Sciences 61: L119-L125.
7. Banks WA, Kastin AJ, (1998) Characterization of lectin-mediated brain uptake of HIV-1 gp120. Journal of Neuroscience Research 54: 522-529.
8. Banks WA, Robinson SM, Wolf KM, Bess JW Jr, Arthur LO, (2004) Binding, internalization, and membrane incorporation of human immunodeficiency virus-1 at the blood-brain barrier is differentially regulated. Neuroscience 128: 143-153.
9. Bobardt MD, Salmon P, Wang L, Esko JD, Gabuzda D, et al. (2004) Contribution of proteoglycans to human immunodeficiency virus type 1 brain invasion. J Virol 78: 6567-6584.
10. Hansen JE, Nielsen CM, Nielsen C, Heegaard P, Mathiesen LR, et al. (1989) Correlation between carbohydrate structures on the envelope glycoprotein gp120 of HIV-1 and HIV-2 and syncytium inhibition with lectins. AIDS 3: 635-641.
11. Larkin M, Childs RA, Matthews TJ, Thiel S, Mizuochi T, et al. (1989) Oligosaccharide-mediated interactions of the envelope glycoprotein gp120 of HIV-1 that are independent of CD4 recognition. AIDS 3: 793-798.
12. Robinson WE, Montefiori DC, MItchell WM, (1987) Evidence that mannosyl residues are involved in human immunodeficiency virus type I (HIV-1) pathogenesis. AIDS Res Hum Retroviruses 3: 265-282.
13. Dezutter-Dambuyant C, Schmitt DA, Dusserre N, Hanau D, Kolbe HVJ, et al. (1991) Interaction of human epidermal Langerhans cells with HIV-1 viral envelope proteins (gp120 and gp160s) involves a receptor-mediated endocytosis independent of the CD4 T4A epitope. The Journal of Dermatology 18: 377-392.
14. Bourinbaiar AS, Phillips DM, (1991) Transmission of human immunodeficiency virus from monocytes to epithelia. Journal of Acquired Immune Deficiency Syndromes 4: 56-63.
15. Mbemba E, Gluckman JC, Gattegno L, (1994) Interactions of HIV-1 and HIV-2 envelope glycoproteins with sulphated polysachharides and mannose-6-phosphate. Glycobiology 4: 13-21.
16. Suh HS, Cosenza-Nashat M, Choi N, Zhao ML, Li JF, et al. (2010) Insulin-like growth factor 2 receptor is a IFNfamma-inducible microglial protein that facilitates intracellular HIV replicaton: implications for HIV-induced neurocognitive disorders. Am J Path 177: 2446-2458.
17. Hambleton S, (2005) Chickenpox. Curr Opin Infect Dis 18: 235-240.
18. Urayama A, Grubb JH, Banks WA, Sly WS, (2007) Epinephrine enhances lysosomal enzyme delivery across the blood-brain barrier by up-regulation of the mannose 6-phosphate receptor. Proceedings of the National Academy of Sciences USA 31: 12873-12878.
19. Urayama A, Grubb JH, Sly WS, Banks WA, (2004) Developmentally regulated mannose 6-phosphate receptor-mediated transport of a lysosomal enzyme across the blood-brain barrier. Proceedings of the National Academy of Sciences USA 101: 12658-12663.
20. Urayama A, Grubb JH, Sly WS, Banks WA, (2008) Mannose 6-phosphate receptor mediated transport of sulfamidase across the blood-brain barrier in the newborn mouse. Molecular Therapy 16: 1261-1266.
21. Arthur LO, Bess JW Jr, Chertova EN, Rossio JL, Esser MT, et al. (1998) Chemical inactivation of retroviral infectivity by targeting nucleocapsid protein zinc fingers: A candidate SIV vaccine. AIDS Research and Human Retroviruses 14: 311.
22. Rossio JL, Esser MT, Suryanarayana K, Schneider DK, Bess JW Jr, et al. (1998) Inactivation of human immunodeficiency virus type 1 infectivity with preservation of conformational and functional integrity of virion surface proteins. Journal of Virology 72: 7992-8001.
23. Ott DE, Nigida SM Jr, Henderson LE, Arthur LO, (1995) The majority of cells are superinfected in a cloned cell line that produces high levels of human immunodeficiency virus type 1 strain MN. Journal of Virology 69: 2443-2450.
24. Frost EH, (1977) Radioactive labelling of viruses: an iodination preserving biological properties. JGenVirol 35: 181-185.
25. Montelaro RC, Rueckert RR, (1975) On the use of chloramine-T to iodinate specifically the surface proteins of intact enveloped viruses. JGenVirol 29: 127-131.
26. Banks WA, Clever CM, Farrell CL, (2000) Partial saturation and regional variation in the blood to brain transport of leptin in normal weight mice. American Journal of Physiology 278: E1158-E1165.
27. Glowinski J, Iversen LL, (1966) Regional studies of catecholamines in the rat brain. I. The disposition of [3H]norepinephrine, [3H]dopamine and [3H]dopa in various regions of the brain. Journal of Neurochemistry 13: 655-669.
28. Ryerse JS, Colombini M, Hagerty T, Nagel BA, Liu TT, (1997) Isolation and characterization of the mitochondrial channel, VDAC, from the insect Heliothis virescens. Biochim et Biophys ACTA 1327: 193-203.
29. Ryerse JS, Hoffman J, Mohmood S, Nagel B, DeMello D, (2001) Immunolocalization of CC10 in Clara cells in mouse and human lung. Histochem anc Cell Biol 115: 325-332.
30. Szabo CA, Deli MA, Ngo TKD, Joo F, (1997) Production of pure primary rat cerebral endothelial cell culture: a comparison of different methods. Neurobiology 5: 1-16.
31. Nakagawa S, Deli MA, Nakao S, Honda M, Hayashi K, et al. (2007) Pericytes from brain microvessels strengthen the barrier integrity in primary cultures of rat brain endothelial cells. Cell Mol Neurobiol 27: 687-694.
32. Dehouck MP, Jolliet-Riant P, Bree F, Fruchart JC, Cecchelli R, et al. (1992) Drug transfer across the blood-brain barrier: Correlation between in vitro and in vivo models. J Neurochem 58: 1790-1797.
33. Hall NC, Dempsey RJ, Carney JM, Donaldson DL, Butterfield DA, (1995) Structural alterations in synaptosomal membrane-associated proteins and lipids by transient middle cerebral artery occlusion in the cat. Neurochemical Research 20: 1161-1169.
34. Gelderblom HR, (1997) Fie structure of HIV and SIV: A note to the HIV sequence database. Available:http:wwwhivlanlgov/content/sequence/HIV/COMPENDIUM/1997/partIII/Gelderblompdf.
35. Banks WA, Kumar VB, Franko MW, Bess JW Jr, Arthur LO, (2005) Evidence that the species barrier of human immunodeficiency virus-1 does not extend to uptake by the blood-brain barrier: Comparison of mouse and human brain microvessels. Life Sciences 77: 2361-2368.
36. Hawkes C, Kar S, (2003) Insulin-like growth factor-II/mannose-6-phosphate receptor: widespread distribution in neurons of the central nervous system including those expressing cholinergic phenotype. J Comp Neurol 458: 113-127.
37. Zhu P, Chertova E, Bess JJ, Lifson JD, Arthur LO, et al. (2003) Electron tomography analysis of envelope glycoprotein tirmers on HIV and simian immunodeficiency virus virions. Proc Natl Acad Sci USA 100: 15812-15817.
38. Zhang LQ, Simmonds P, Ludlam CA, Brown AJL, (1991) Detection, quantification and sequencing of HIV-1 from the plasma of seropositive individuals and from factor VIII concentrates. AIDS 5: 675-681.
39. Saag MS, Crain MJ, Decker WD, Campbell-Hill S, Robinson S, et al. (1991) High-level viremia in adults and children infected with human immunodeficiencty virus: relation to disease stage and CD4+ lymphocyte levels. J Infect Dis 164: 72-80.
40. Brown RC, Davis TP, (2002) Calcium modulation of adherens tight junction function: a potential mechanism for blood-brain barrier disruption after stroke. Stroke 33: 1706-1711.
41. Johnson RT, (1994) The virology of demyelinating diseases. Ann Neurol 36: S54-60.
42. Kimura-Kuroda J, Nagashima K, Yasui K, (1994) Inhibition of formation by HIV-1 gp120 in rat cerebral cortex culture. Archives of Virology 137: 81-99.
43. Liuzzi GM, Mastroianni CM, Fanelli M, Massetti AP, Vullo V, et al. (1994) Mylein degrading activity in the CSF of HIV-1 infected patients with neurological diseases. Neuroreport 6: 157-160.
44. Deli MA, Abraham CR, Kataoka Y, Niwa M, (2005) Permeability studies on in vitro blood-brain barrier models: physiology, pathology, and pharmacology. Cellular and Molecular Neurobiology 25: 59-127.
45. Banks WA, Akerstrom V, Kastin AJ, (1998) Adsorptive endocytosis mediates the passage of HIV-1 across the blood-brain barrier: evidence for a post-internalization coreceptor. Journal of Cell Science 111: 533-540.
46. Hoflack B, Kornfeld S, (1985) Lysosomal enzyme binding to mouse P388D1 macrophage membranes lacking the 214-kDa mannose 6-phosphate receptor: evidence for the existence of a second mannose 6-phosphate receptor. Proc Natl Acad Sci 82: 4428-4432.
47. Kim JJ, Olson LJ, Dahms NM, (2009) Carbohydrate recognition by the mannose-6-phosphate receptors. Curr Opin Struct Biol 19: 534-542.
48. Yu ZW, Wickman A, Eriksson JW, (1996) Cryptic receptors for insulin-like growth factor II in the plasma membrane of rat adipocytes - a possible link to cellular insulin resistance. Biochim Biophys ACTA 1282: 57-62.
49. McKinnon T, Chakraborty C, Gleeson LM, Chidiac P, Lala PK, (2001) Stimulation of human extravillouis trophoblast migration by IGF-II is mediated by IGF type 2 receptor involving inhibitory G protein(s) and phosphorylation of MAPK. J Clin Endocrinol Metab 86: 3665-3674.