Caveolin-1 mediated uptake via langerin restricts HIV-1 infection in human Langerhans cells

Retrovirology

Volumn 11, Issue 1, 2014, Pages

  van den Berg, Linda M ^a   Ribeiro, Carla M ^a   Zijlstra Willems, Esther M ^a   de Witte, Lot ^b   Fluitsma, Donna ^c   Tigchelaar, Wikky ^a   Everts, Vincent ^a,d   Geijtenbeek, Teunis B ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^d VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

Birbeck granules; Caveolar uptake; Caveolin 1; Clathrin; HIV 1 restriction; Langerhans cells; Langerin

Indexed keywords

CAVEOLIN 1; CLATHRIN; LANGERIN; CD207 PROTEIN, HUMAN; LECTIN; LEUKOCYTE ANTIGEN; MANNOSE BINDING LECTIN;

ARTICLE; BIRBECK GRANULE; CELL GRANULE; CELL MEMBRANE; CELL VACUOLE; CONTROLLED STUDY; ENDOCYTOSIS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INTRACELLULAR SIGNALING; LANGERHANS CELL; LYSOSOME MEMBRANE; MICROBIAL DEGRADATION; NONHUMAN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; VIRUS DNA CELL DNA INTERACTION; VIRUS ENTRY; CYTOPLASM VESICLE; HUMAN IMMUNODEFICIENCY VIRUS 1; METABOLISM; PHYSIOLOGY; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ANTIGENS, CD; CAVEOLIN 1; CYTOPLASMIC VESICLES; ENDOCYTOSIS; HIV-1; HUMANS; LANGERHANS CELLS; LECTINS, C-TYPE; MANNOSE-BINDING LECTINS; VIRUS INTERNALIZATION;

EID: 84924127191     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/s12977-014-0123-7     Document Type: Article

References (34)

1. van der Vlist M, Geijtenbeek TBH: Langerin functions as an antiviral receptor on Langerhans cells. Immunol Cell Biol 2010, 88:410-415.
2. Cunningham AL, Abendroth A, Jones C, Nasr N, Turville S: Viruses and Langerhans cells. Immunol Cell Biol 2010, 88:416-423.
3. de Witte L, Nabatov A, Pion M, Fluitsma D, De Jong MAWP, de Gruijl T, Piguet V, van Kooyk Y, Geijtenbeek TBH: Langerin is a natural barrier to HIV-1 transmission by Langerhans cells. Nat Med 2007, 13:367-371.
4. Patterson BK, Landay A, Siegel JN, Flener Z, Pessis D, Chaviano A, Bailey RC: Susceptibility to human immunodeficiency virus-1 infection of human foreskin and cervical tissue grown in explant culture. Am J Pathol 2002, 161:867-873.
5. Hladik F, Sakchalathorn P, Ballweber L, Lentz G, Fialkow M, Eschenbach D, McElrath MJ: Initial events in establishing vaginal entry and infection by human immunodeficiency virus type-1. Immunity 2007, 26:257-270.
6. De Jong MAWP, de Witte L, Oudhoff MJ, Gringhuis SI, Gallay P, Geijtenbeek TBH: TNF-alpha and TLR agonists increase susceptibility to HIV-1 transmission by human Langerhans cells ex vivo. J Clin Investig 2008, 118:3440-3452.
7. Ganor Y, Zhou Z, Tudor D, Schmitt A, Vacher-Lavenu MC, Gibault L, Thiounn N, Tomasini J, Wolf JP, Bomsel M: Within 1h, HIV-1 uses viral synapses to enter efficiently the inner, but not outer, foreskin mucosa and engages Langerhans-T cell conjugates. Mucosal Immunol 2010, 3:506-522.
8. Sarrami-Forooshani R, Mesman AW, van Teijlingen NH, Sprokholt JK, van der Vlist M, Ribeiro CMS, Geijtenbeek TBH: Human immature Langerhans cells restrict CXCR4-using HIV-1 transmission. Retrovirology 2014, 11:52.
9. Valladeau J, Dezutter-Dambuyant C, Saeland S: Langerin/CD207 sheds light on formation of birbeck granules and their possible function in langerhans cells. Immunol Res 2003, 28:93-107.
10. Valladeau J, Ravel O, Dezutter-Dambuyant C, Moore K, Kleijmeer M, Liu Y, Duvert-Frances V, Vincent C, Schmitt D, Davoust J, Caux C, Lebecque S, Saeland S: Langerin, a novel C-type lectin specific to Langerhans cells, is an endocytic receptor that induces the formation of Birbeck granules. Immunity 2000, 12:71-81.
11. Thepaut M, Valladeau J, Nurisso A, Kahn R, Arnou B, Vives C, Saeland S, Ebel C, Monnier C, Dezutter-Dambuyant C, Imberty A, Fieschi F: Structural studies of Langerin and Birbeck granule: a macromolecular organization model. Biochemistry 2009, 48:2684-2698.
12. McDermott R, Bausinger H, Fricker D, Spehner D, Proamer F, Lipsker D, Cazenave JP, Goud B, De La Salle H, Salamero J, Hanau D: Reproduction of Langerin/CD207 traffic and Birbeck granule formation in a human cell line model. J Investig Dermatol 2004, 123:72-77.
13. van der Vlist M, de Witte L, de Vries RD, Litjens M, De Jong MAWP, Fluitsma D, de Swart RL, Geijtenbeek TBH: Human Langerhans cells capture measles virus through Langerin and present viral antigens to CD4(+) T cells but are incapable of cross-presentation. Eur J Immunol 2011, 41:2619-2631.
14. McDermott R, Ziylan U, Spehner D, Bausinger H, Lipsker D, Mommaas M, Cazenave JP, Raposo G, Goud B, De La Salle H, Salamero J, Hanau D: Birbeck granules are subdomains of endosomal recycling compartment in human epidermal Langerhans cells, which form where Langerin accumulates. Mol Biol Cell 2002, 13:317-335.
15. Gallusser A, Kirchhausen T: The beta 1 and beta 2 subunits of the AP complexes are the clathrin coat assembly components. EMBO J 1993, 12:5237-5244.
16. Owen DJ, Evans PR: A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 1998, 282:1327-1332.
17. Lapierre LA, Ducharme NA, Drake KR, Goldenring JR, Kenworthy AK: Coordinated regulation of caveolin-1 and Rab11a in apical recycling compartments of polarized epithelial cells. Exp Cell Res 2012, 318:103-113.
18. Polak ME, Thirdborough SM, Ung CY, Elliott T, Healy E, Freeman TC, Ardern-Jones MR: Distinct molecular signature of human skin Langerhans cells denotes critical differences in cutaneous dendritic cell immune regulation. J Investig Dermatol 2014, 134:695-703.
19. Glenney JR, Soppet D: Sequence and expression of caveolin, a protein-component of caveolae plasma-membrane domains phosphorylated on tyrosine in rous-sarcoma virus-transformed fibroblasts. Proc Natl Acad Sci U S A 1992, 89:10517-10521.
20. Kurzchalia TV, Dupree P, Parton RG, Kellner R, Virta H, Lehnert M, Simons K: Vip21, A 21-Kd membrane-protein is an integral component of Trans-Golgi-network-derived transport vesicles. J Cell Biol 1992, 118:1003-1014.
21. Fra AM, Williamson E, Simons K, Parton RG: De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc Natl Acad Sci U S A 1995, 92:8655-8659.
22. Lipardi C, Mora R, Colomer V, Paladino S, Nitsch L, Rodriguez-Boulan E, Zurzolo C: Caveolin transfection results in caveolae formation but not apical sorting of glycosylphosphatidylinositol (GPI)-anchored proteins in epithelial cells. J Cell Biol 1998, 140:617-626.
23. Hayer A, Stoeber M, Ritz D, Engel S, Meyer HH, Helenius A: Caveolin-1 is ubiquitinated and targeted to intralumenal vesicles in endolysosomes for degradation. J Cell Biol 2010, 191:615-629.
24. Yan M, Peng J, Jabbar IA, Liu X, Filgueira L, Frazer IH, Thomas R: Despite differences between dendritic cells and Langerhans cells in the mechanism of papillomavirus-like particle antigen uptake, both cells cross-prime T cells. Virology 2004, 324:297-310.
25. Smith JL, Campos SK, Ozbun MA: Human papillomavirus type 31 uses a caveolin 1- and dynamin 2-mediated entry pathway for infection of human keratinocytes. J Virol 2007, 81:9922-9931.
26. Rohde M, Muller E, Chhatwal GS, Talay SR: Host cell caveolae act as an entry-port for group A streptococci. Cell Microbiol 2003, 5:323-342.
27. Orlandi PA, Fishman PH: Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J Cell Biol 1998, 141:905-915.
28. Schnitzer JE, Oh P, Pinney E, Allard J: Filipin-sensitive caveolae-mediated transport in endothelium - reduced transcytosis, scavenger endocytosis, and capillary-permeability of select macromolecules. J Cell Biol 1994, 127:1217-1232.
29. de Jong MA, de Witte L, Santegoets SJ, Fluitsma D, Taylor ME, de Gruijl TD, Geijtenbeek TB: Mutz-3-derived Langerhans cells are a model to study HIV-1 transmission and potential inhibitors. J Leukoc Biol 2010, 87:637-643.
30. Klasse PJ: The molecular basis of HIV entry. Cell Microbiol 2012, 14:1183-1192.
31. Cavrois M, de Noronha C, Greene WC: A sensitive and specific enzyme-based assay detecting HIV-1 virion fusion in primary T lymphocytes. Nat Biotechnol 2002, 20:1151-1154.
32. Brussel A, Sonigo P: Evidence for gene expression by unintegrated human immunodeficiency virus type 1 DNA species. J Virol 2004, 78:11263-11271.
33. Uzan-Gafsou S, Bausinger H, Proamer F, Monier S, Lipsker D, Cazenave JP, Goud B, De La Salle H, Hanau D, Salamero J: Rab11A controls the biogenesis of Birbeck granules by regulating Langerin recycling and stability. Mol Biol Cell 2007, 18:3169-3179.
34. Gidon A, Bardin S, Cinquin B, Boulanger J, Waharte F, Heliot L, De La Salle H, Hanau D, Kervrann C, Goud B, Salamero J: A Rab11A/myosin Vb/Rab11-FIP2 complex frames two late recycling steps of langerin from the ERC to the plasma membrane. Traffic 2012, 13:815-833.