期刊论文详细信息
Retrovirology
Sialic acid-binding Ig-like lectin-7 interacts with HIV-1 gp120 and facilitates infection of CD4pos T cells and macrophages
Domenico Mavilio4  Mario U Mondelli9  Renato Maserati8  Agostino Riva1  Mauro Malnati7  Raffaello Cimbro5  Stefania Paolucci3  Dalila Mele6  Joanna Mikulak2  Kelly Hudspeth2  Paolo Lusso5  Stefania Varchetta6 
[1] Dipartimento di Scienze Cliniche (DISC) L. Sacco Hospital-Infectious diseases and Immunopathology Section, University of Milan, Milan, Italy;Unit of Clinical and Experimental Immunology, Humanitas Clinical and Research Center, Rozzano, Milan, Italy;S. S. Virologia Molecolare, S. C. Virologia e Microbiologia, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy;Department of Medical Biotechnologies and Translational Medicine, University of Milan, Milan, Italy;Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA;Research Laboratories, Department of Infectious Diseases, Fondazione IRCCS, Policlinico San Matteo, Pavia, Italy;Unit of Human Virology Division of Immunology, Transplantation and Infectious Diseases, San Raffaele Scientific Institute, Milan, Italy;HIV Outpatient clinic, Department of Infectious Diseases, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy;Department of Internal Medicine, University of Pavia, Pavia, Italy
关键词: AIDS patients;    Macrophages;    CD4+ T cells;    Siglec-7;    HIV-1 infection;   
Others  :  805805
DOI  :  10.1186/1742-4690-10-154
 received in 2013-06-26, accepted in 2013-12-10,  发布年份 2013
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【 摘 要 】

Background

Sialic acid-binding Ig-like lectin-7 (Siglec-7) expression is strongly reduced on natural killer (NK) cells from HIV-1 infected viremic patients. To investigate the mechanism(s) underlying this phenomenon, we hypothesized that Siglec-7 could contribute to the infection of CD4pos target cells following its interaction with HIV-1 envelope (Env) glycoprotein 120 (gp120).

Results

The ability of Siglec-7 to bind gp120 Env in a sialic acid-dependent manner facilitates the infection of both T cells and monocyte-derived macrophages (MDMs). Indeed, pre-incubation of HIV-1 with soluble Siglec-7 (sSiglec-7) increases the infection rate of CD4pos T cells, which do not constitutively express Siglec-7. Conversely, selective blockade of Siglec-7 markedly reduces the degree of HIV-1 infection in Siglec-7pos MDMs. Finally, the sSiglec-7 amount is increased in the serum of AIDS patients with high levels of HIV-1 viremia and inversely correlates with CD4pos T cell counts.

Conclusions

Our results show that Siglec-7 binds HIV-1 and contributes to enhance the susceptibility to infection of CD4pos T cells and MDMs. This phenomenon plays a role in HIV-1 pathogenesis and in disease progression, as suggested by the inverse correlation between high serum level of sSiglec-7 and the low CD4pos T cell count observed in AIDS patients in the presence of chronic viral replication.

【 授权许可】

   
2013 Varchetta et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Pantophlet R, Burton DR: GP120: target for neutralizing HIV-1 antibodies. Annu Rev Immunol 2006, 24:739-769.
  • [2]Scanlan CN, Offer J, Zitzmann N, Dwek RA: Exploiting the defensive sugars of HIV-1 for drug and vaccine design. Nature 2007, 446:1038-1045.
  • [3]Wei X, Decker JM, Wang S, Hui H, Kappes JC, Wu X, Salazar-Gonzalez JF, Salazar MG, Kilby JM, Saag MS, et al.: Antibody neutralization and escape by HIV-1. Nature 2003, 422:307-312.
  • [4]Go EP, Chang Q, Liao HX, Sutherland LL, Alam SM, Haynes BF, Desaire H: Glycosylation site-specific analysis of clade C HIV-1 envelope proteins. J Proteome Res 2009, 8:4231-4242.
  • [5]Zhang M, Gaschen B, Blay W, Foley B, Haigwood N, Kuiken C, Korber B: Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin. Glycobiology 2004, 14:1229-1246.
  • [6]Schauer R: Achievements and challenges of sialic acid research. Glycoconj J 2000, 17:485-499.
  • [7]Varki A: Glycan-based interactions involving vertebrate sialic-acid-recognizing proteins. Nature 2007, 446:1023-1029.
  • [8]Yamaji T, Teranishi T, Alphey MS, Crocker PR, Hashimoto Y: A small region of the natural killer cell receptor, Siglec-7, is responsible for its preferred binding to alpha 2,8-disialyl and branched alpha 2,6-sialyl residues. A comparison with Siglec-9. J Biol Chem 2002, 277:6324-6332.
  • [9]Nicoll G, Ni J, Liu D, Klenerman P, Munday J, Dubock S, Mattei MG, Crocker PR: Identification and characterization of a novel siglec, siglec-7, expressed by human natural killer cells and monocytes. J Biol Chem 1999, 274:34089-34095.
  • [10]Crocker PR, Paulson JC, Varki A: Siglecs and their roles in the immune system. Nat Rev Immunol 2007, 7:255-266.
  • [11]von Gunten S, Bochner BS: Basic and clinical immunology of Siglecs. Ann N Y Acad Sci 2008, 1143:61-82.
  • [12]Avril T, Floyd H, Lopez F, Vivier E, Crocker PR: The membrane-proximal immunoreceptor tyrosine-based inhibitory motif is critical for the inhibitory signaling mediated by Siglecs-7 and -9, CD33-related Siglecs expressed on human monocytes and NK cells. J Immunol 2004, 173:6841-6849.
  • [13]Varchetta S, Brunetta E, Roberto A, Mikulak J, Hudspeth KL, Mondelli MU, Mavilio D: Engagement of Siglec-7 receptor induces a pro-inflammatory response selectively in monocytes. PLoS One 2012, 7:e45821.
  • [14]Avril T, Wagner ER, Willison HJ, Crocker PR: Sialic acid-binding immunoglobulin-like lectin 7 mediates selective recognition of sialylated glycans expressed on Campylobacter jejuni lipooligosaccharides. Infect Immun 2006, 74:4133-4141.
  • [15]Khatua B, Ghoshal A, Bhattacharya K, Mandal C, Saha B, Crocker PR, Mandal C: Sialic acids acquired by Pseudomonas aeruginosa are involved in reduced complement deposition and siglec mediated host-cell recognition. FEBS Lett 2010, 584:555-561.
  • [16]Khatua B, Bhattacharya K, Mandal C: Sialoglycoproteins adsorbed by Pseudomonas aeruginosa facilitate their survival by impeding neutrophil extracellular trap through siglec-9. J Leukoc Biol 2012, 91:641-655.
  • [17]Mercier S, St-Pierre C, Pelletier I, Ouellet M, Tremblay MJ, Sato S: Galectin-1 promotes HIV-1 infectivity in macrophages through stabilization of viral adsorption. Virology 2008, 371:121-129.
  • [18]Ouellet M, Mercier S, Pelletier I, Bounou S, Roy J, Hirabayashi J, Sato S, Tremblay MJ: Galectin-1 acts as a soluble host factor that promotes HIV-1 infectivity through stabilization of virus attachment to host cells. J Immunol 2005, 174:4120-4126.
  • [19]Furci L, Sironi F, Tolazzi M, Vassena L, Lusso P: Alpha-defensins block the early steps of HIV-1 infection: interference with the binding of gp120 to CD4. Blood 2007, 109:2928-2935.
  • [20]Feng Z, Dubyak GR, Lederman MM, Weinberg A: Cutting edge: human beta defensin 3–a novel antagonist of the HIV-1 coreceptor CXCR4. J Immunol 2006, 177:782-786.
  • [21]Munk C, Wei G, Yang OO, Waring AJ, Wang W, Hong T, Lehrer RI, Landau NR, Cole AM: The theta-defensin, retrocyclin, inhibits HIV-1 entry. AIDS Res Hum Retroviruses 2003, 19:875-881.
  • [22]Ezekowitz RA, Kuhlman M, Groopman JE, Byrn RA: A human serum mannose-binding protein inhibits in vitro infection by the human immunodeficiency virus. J Exp Med 1989, 169:185-196.
  • [23]de Witte L, Nabatov A, Pion M, Fluitsma D, de Jong MA, de Gruijl T, Piguet V, van Kooyk Y, Geijtenbeek TB: Langerin is a natural barrier to HIV-1 transmission by Langerhans cells. Nat Med 2007, 13:367-371.
  • [24]Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, Middel J, Cornelissen IL, Nottet HS, KewalRamani VN, Littman DR, et al.: DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 2000, 100:587-597.
  • [25]Nguyen DG, Hildreth JE: Involvement of macrophage mannose receptor in the binding and transmission of HIV by macrophages. Eur J Immunol 2003, 33:483-493.
  • [26]de Witte L, Bobardt M, Chatterji U, Degeest G, David G, Geijtenbeek TB, Gallay P: Syndecan-3 is a dendritic cell-specific attachment receptor for HIV-1. Proc Natl Acad Sci USA 2007, 104:19464-19469.
  • [27]Lambert AA, Gilbert C, Richard M, Beaulieu AD, Tremblay MJ: The C-type lectin surface receptor DCIR acts as a new attachment factor for HIV-1 in dendritic cells and contributes to trans- and cis-infection pathways. Blood 2008, 112:1299-1307.
  • [28]Rempel H, Calosing C, Sun B, Pulliam L: Sialoadhesin expressed on IFN-induced monocytes binds HIV-1 and enhances infectivity. PLoS One 2008, 3:e1967.
  • [29]Zou Z, Chastain A, Moir S, Ford J, Trandem K, Martinelli E, Cicala C, Crocker P, Arthos J, Sun PD: Siglecs facilitate HIV-1 infection of macrophages through adhesion with viral sialic acids. PLoS One 2011, 6:e24559.
  • [30]Izquierdo-Useros N, Lorizate M, Puertas MC, Rodriguez-Plata MT, Zangger N, Erikson E, Pino M, Erkizia I, Glass B, Clotet B, et al.: Siglec-1 is a novel dendritic cell receptor that mediates HIV-1 trans-infection through recognition of viral membrane gangliosides. PLoS Biol 2012, 10:e1001448.
  • [31]Brunetta E, Fogli M, Varchetta S, Bozzo L, Hudspeth KL, Marcenaro E, Moretta A, Mavilio D: The decreased expression of Siglec-7 represents an early marker of dysfunctional natural killer-cell subsets associated with high levels of HIV-1 viremia. Blood 2009, 114:3822-3830.
  • [32]Lusso P, Cocchi F, Balotta C, Markham PD, Louie A, Farci P, Pal R, Gallo RC, Reitz MS Jr: Growth of macrophage-tropic and primary human immunodeficiency virus type 1 (HIV-1) isolates in a unique CD4+ T-cell clone (PM1): failure to downregulate CD4 and to interfere with cell-line-tropic HIV-1. J Virol 1995, 69:3712-3720.
  • [33]Hudspeth K, Fogli M, Correia DV, Mikulak J, Roberto A, Della Bella S, Silva-Santos B, Mavilio D: Engagement of NKp30 on Vdelta1 T cells induces the production of CCL3, CCL4, and CCL5 and suppresses HIV-1 replication. Blood 2012, 119:4013-4016.
  • [34]Dalgleish AG, Beverley PC, Clapham PR, Crawford DH, Greaves MF, Weiss RA: The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 1984, 312:763-767.
  • [35]Klatzmann D, Champagne E, Chamaret S, Gruest J, Guetard D, Hercend T, Gluckman JC, Montagnier L: T-lymphocyte T4 molecule behaves as the receptor for human retrovirus LAV. Nature 1984, 312:767-768.
  • [36]McLain L, Dimmock NJ: A human CD4+ T-cell line expresses functional CD64 (Fc gamma RI), CD32 (Fc gamma RII), and CD16 (Fc gamma RIII) receptors but these do not enhance the infectivity of HIV-1-IgG complexes. Immunology 1997, 90:109-114.
  • [37]Lanier LL, Kipps TJ, Phillips JH: Functional properties of a unique subset of cytotoxic CD3+ T lymphocytes that express Fc receptors for IgG (CD16/Leu-11 antigen). J Exp Med 1985, 162:2089-2106.
  • [38]Kazazi F, Mathijs JM, Foley P, Cunningham AL: Variations in CD4 expression by human monocytes and macrophages and their relationships to infection with the human immunodeficiency virus. J Gen Virol 1989, 70(Pt 10):2661-2672.
  • [39]Wilen CB, Tilton JC, Doms RW: HIV: cell binding and entry. Cold Spring Harb Perspect Med 2012., 2(8) doi:pii: a006866. 10.1101/cshperspect.a006866. Review
  • [40]Jacobs T, Erdmann H, Fleischer B: Molecular interaction of Siglecs (sialic acid-binding Ig-like lectins) with sialylated ligands on Trypanosoma cruzi. Eur J Cell Biol 2010, 89:113-116.
  • [41]Erdmann H, Steeg C, Koch-Nolte F, Fleischer B, Jacobs T: Sialylated ligands on pathogenic Trypanosoma cruzi interact with Siglec-E (sialic acid-binding Ig-like lectin-E). Cell Microbiol 2009, 11:1600-1611.
  • [42]Carlin AF, Lewis AL, Varki A, Nizet V: Group B streptococcal capsular sialic acids interact with siglecs (immunoglobulin-like lectins) on human leukocytes. J Bacteriol 2007, 189:1231-1237.
  • [43]Carlin AF, Uchiyama S, Chang YC, Lewis AL, Nizet V, Varki A: Molecular mimicry of host sialylated glycans allows a bacterial pathogen to engage neutrophil Siglec-9 and dampen the innate immune response. Blood 2009, 113:3333-3336.
  • [44]Jones C, Virji M, Crocker PR: Recognition of sialylated meningococcal lipopolysaccharide by siglecs expressed on myeloid cells leads to enhanced bacterial uptake. Mol Microbiol 2003, 49:1213-1225.
  • [45]Pillai S, Netravali IA, Cariappa A, Mattoo H: Siglecs and immune regulation. Annu Rev Immunol 2012, 30:357-392.
  • [46]Cao H, Crocker PR: Evolution of CD33-related siglecs: regulating host immune functions and escaping pathogen exploitation? Immunology 2011, 132:18-26.
  • [47]Vanderheijden N, Delputte PL, Favoreel HW, Vandekerckhove J, Van Damme J, van Woensel PA, Nauwynck HJ: Involvement of sialoadhesin in entry of porcine reproductive and respiratory syndrome virus into porcine alveolar macrophages. J Virol 2003, 77:8207-8215.
  • [48]Delputte PL, Nauwynck HJ: Porcine arterivirus infection of alveolar macrophages is mediated by sialic acid on the virus. J Virol 2004, 78:8094-8101.
  • [49]Sun J, Barbeau B, Sato S, Tremblay MJ: Neuraminidase from a bacterial source enhances both HIV-1-mediated syncytium formation and the virus binding/entry process. Virology 2001, 284:26-36.
  • [50]Kwong PD, Wyatt R, Sattentau QJ, Sodroski J, Hendrickson WA: Oligomeric modeling and electrostatic analysis of the gp120 envelope glycoprotein of human immunodeficiency virus. J Virol 2000, 74:1961-1972.
  • [51]Sakaida H, Hori T, Yonezawa A, Sato A, Isaka Y, Yoshie O, Hattori T, Uchiyama T: T-tropic human immunodeficiency virus type 1 (HIV-1)-derived V3 loop peptides directly bind to CXCR-4 and inhibit T-tropic HIV-1 infection. J Virol 1998, 72:9763-9770.
  • [52]Crocker PR, Varki A: Siglecs in the immune system. Immunology 2001, 103:137-145.
  • [53]Brunetta E, Fogli M, Varchetta S, Bozzo L, Hudspeth KL, Marcenaro E, Moretta A, Mavilio D: Chronic HIV-1 viremia reverses NKG2A/NKG2C ratio on natural killer cells in patients with human cytomegalovirus co-infection. AIDS 2010, 24:27-34.
  • [54]Brunetta E, Hudspeth KL, Mavilio D: Pathologic natural killer cell subset redistribution in HIV-1 infection: new insights in pathophysiology and clinical outcomes. J Leukoc Biol 2010, 88:1119-1130.
  • [55]Lackner AA, Lederman MM, Rodriguez B: HIV pathogenesis: the host. Cold Spring Harb Perspect Med 2012, 2:a007005.
  • [56]Shacklett BL: Immune responses to HIV and SIV in mucosal tissues: 'location, location, location'. Curr Opin HIV AIDS 2010, 5:128-134.
  • [57]Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, Kazzaz Z, Bornstein E, Lambotte O, Altmann D, et al.: Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006, 12:1365-1371.
  • [58]Hudspeth K, Silva-Santos B, Mavilio D: Natural cytotoxicity receptors: broader expression patterns and functions in innate and adaptive immune cells. Front Immunol 2013, 4:69.
  • [59]Eisele E, Siliciano RF: Redefining the viral reservoirs that prevent HIV-1 eradication. Immunity 2012, 37:377-388.
  • [60]Gupta N, Arthos J, Khazanie P, Steenbeke TD, Censoplano NM, Chung EA, Cruz CC, Chaikin MA, Daucher M, Kottilil S, et al.: Targeted lysis of HIV-infected cells by natural killer cells armed and triggered by a recombinant immunoglobulin fusion protein: implications for immunotherapy. Virology 2005, 332:491-497.
  • [61]Rusmini M, Griseri P, Lantieri F, Matera I, Hudspeth KL, Roberto A, Mikulak J, Avanzini S, Rossi V, Mattioli G, et al.: Induction of RET dependent and independent pro-inflammatory programs in human peripheral blood mononuclear cells from Hirschsprung patients. PLoS One 2013, 8:e59066.
  • [62]Avettand-Fenoel V, Chaix ML, Blanche S, Burgard M, Floch C, Toure K, Allemon MC, Warszawski J, Rouzioux C: LTR real-time PCR for HIV-1 DNA quantitation in blood cells for early diagnosis in infants born to seropositive mothers treated in HAART area (ANRS CO 01). J Med Virol 2009, 81:217-223.
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