JAM-A and ALCAM are therapeutic targets to inhibit diapedesis across the BBB of CD14+CD16+ monocytes in HIV-infected individuals

Journal of Leukocyte Biology

Volumn 97, Issue 2, 2015, Pages 401-412

  Williams, Dionna W ^a   Anastos, Kathryn ^a   Morgello, Susan ^b   Berman, Joan W ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

AIDS; Junctional proteins; Transmigration

Indexed keywords

ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; CD14 ANTIGEN; CD16 ANTIGEN; CD31 ANTIGEN; CD99 ANTIGEN; COLONY STIMULATING FACTOR 1; JUNCTIONAL ADHESION MOLECULE A; MEMBRANE PROTEIN; ALCAM PROTEIN, HUMAN; CELL ADHESION MOLECULE; CELL SURFACE RECEPTOR; F11R PROTEIN, HUMAN; FC RECEPTOR; FCGR3B PROTEIN, HUMAN; FETOPROTEIN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; LEUKOCYTE ANTIGEN; NERVE CELL ADHESION MOLECULE;

ADULT; ARTICLE; BLOOD BRAIN BARRIER; CD4 LYMPHOCYTE COUNT; CELL POPULATION; CELL SURFACE; CENTRAL NERVOUS SYSTEM; COHORT ANALYSIS; CONTROLLED STUDY; DIAPEDESIS; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VITRO STUDY; LIMIT OF DETECTION; MAJOR CLINICAL STUDY; MALE; MONOCYTE; NEUROPATHOLOGY; NEUTROPHIL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN TARGETING; VIRUS LOAD; CLINICAL TRIAL; GENE EXPRESSION REGULATION; HIV INFECTIONS; IMMUNOLOGY; INFLAMMATION; MIDDLE AGED; PATHOLOGY; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

ADULT; ANTIGENS, CD; ANTIGENS, CD14; BLOOD-BRAIN BARRIER; CELL ADHESION MOLECULES; CELL ADHESION MOLECULES, NEURONAL; COHORT STUDIES; FEMALE; FETAL PROTEINS; GENE EXPRESSION REGULATION; GPI-LINKED PROTEINS; HIV INFECTIONS; HUMANS; INFLAMMATION; MALE; MIDDLE AGED; MONOCYTES; RECEPTORS, CELL SURFACE; RECEPTORS, IGG; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 84929224686     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.5A0714-347R     Document Type: Article

References (56)

1. Antinori, A., Arendt, G., Becker, J. T., Brew, B. J., Byrd, D. A., Cherner, M., Clifford, D. B., Cinque, P., Epstein, L. G., Goodkin, K., Gisslen, M., Grant, I., Heaton, R. K., Joseph, J., Marder, K., Marra, C. M., McArthur, J. C., Nunn, M., Price, R. W., Pulliam, L., Robertson, K. R., Sacktor, N., Valcour, V., Wojna, V. E. (2007) Updated research nosology for HIVassociated neurocognitive disorders. Neurology 69, 1789–1799.
2. Peluso, M. J., Meyerhoff, D. J., Price, R. W., Peterson, J., Lee, E., Young, A. C., Walter, R., Fuchs, D., Brew, B. J., Cinque, P., Robertson, K., Hagberg, L., Zetterberg, H., Gisslén, M., Spudich, S. (2013) Cerebrospinal fluid and neuroimaging biomarker abnormalities suggest early neurological injury in a subset of individuals during primary HIV infection. J. Infect. Dis. 207, 1703–1712.
3. Valcour, V., Chalermchai, T., Sailasuta, N., Marovich, M., Lerdlum, S., Suttichom, D., Suwanwela, N. C., Jagodzinski, L., Michael, N., Spudich, S., van Griensven, F., de Souza, M., Kim, J., Ananworanich, J.; RV254/SEARCH 010 Study Group. (2012) Central nervous system viral invasion and inflammation during acute HIV infection. J. Infect. Dis. 206, 275–282.
4. Pulliam, L., Sun, B., Rempel, H. (2004) Invasive chronic inflammatory monocyte phenotype in subjects with high HIV-1 viral load. J. Neuroimmunol. 157, 93–98.
5. Anthony, I. C., Ramage, S. N., Carnie, F. W., Simmonds, P., Bell, J. E. (2005) Influence of HAART on HIV-related CNS disease and neuroinflammation. J. Neuropathol. Exp. Neurol. 64, 529–536.
6. Harezlak, J., Buchthal, S., Taylor, M., Schifitto, G., Zhong, J., Daar, E., Alger, J., Singer, E., Campbell, T., Yiannoutsos, C., Cohen, R., Navia, B.; HIV Neuroimaging Consortium. (2011) Persistence of HIV-associated cognitive impairment, inflammation, and neuronal injury in era of highly active antiretroviral treatment. AIDS 25, 625–633.
7. Fischer-Smith, T., Croul, S., Sverstiuk, A. E., Capini, C., L’Heureux, D., Régulier, E. G., Richardson, M. W., Amini, S., Morgello, S., Khalili, K., Rappaport, J. (2001) CNS invasion by CD14+/CD16+ peripheral blood-derived monocytes in HIV dementia: perivascular accumulation and reservoir of HIV infection. J. Neurovirol. 7, 528–541.
8. Ellery, P. J., Tippett, E., Chiu, Y. L., Paukovics, G., Cameron, P.U., Solomon, A., Lewin, S. R., Gorry, P.R., Jaworowski, A., Greene, W.C., Sonza, S., Crowe, S. M. (2007) The CD16+ monocyte subset is more permissive to infection and preferentially harbors HIV-1 in vivo. J. Immunol. 178, 6581–6589.
9. Williams, D. W., Eugenin, E. A., Calderon, T. M., Berman, J. W. (2012) Monocyte maturation, HIV susceptibility, and transmigration across the blood brain barrier are critical in HIV neuropathogenesis. J. Leukoc. Biol. 91, 401–415.
10. Ziegler-Heitbrock, L., Ancuta, P., Crowe, S., Dalod, M., Grau, V., Hart, D. N., Leenen, P. J. M., Liu, Y.-J., MacPherson, G., Randolph, G. J., Scherberich, J., Schmitz, J., Shortman, K., Sozzani, S., Strobl, H., Zembala, M., Austyn, J. M., Lutz, M. B. (2010) Nomenclature of monocytes and dendritic cells in blood. Blood 116, e74–e80.
11. Kusao, I., Shiramizu, B., Liang, C. Y., Grove, J., Agsalda, M., Troelstrup, D., Velasco, V. N., Marshall, A., Whitenack, N., Shikuma, C., Valcour, V. (2012) Cognitive performance related to HIV-1-infected monocytes. J. Neuropsychiatry Clin. Neurosci. 24, 71–80.
12. Shiramizu, B., Ananworanich, J., Chalermchai, T., Siangphoe, U., Troelstrup, D., Shikuma, C., De Grutolla, V., Sithinamsuwan, P., Praihirunkit, P., Rattanamanee, S., Valcour, V.; SEARCH 001.1 Study Group. (2012) Failure to clear intra-monocyte HIV infection linked to persistent neuropsychological testing impairment after first-line combined antiretroviral therapy. J. Neurovirol. 18, 69–73.
13. Pulliam, L., Gascon, R., Stubblebine, M., McGuire, D., McGrath, M. S. (1997) Unique monocyte subset in patients with AIDS dementia. Lancet 349, 692–695.
14. Han, J., Wang, B., Han, N., Zhao, Y., Song, C., Feng, X., Mao, Y., Zhang, F., Zhao, H., Zeng, H. (2009) CD14(high)CD16(+) rather than CD14(low)CD16(+) monocytes correlate with disease progression in chronic HIV-infected patients. J. Acquir. Immune Defic. Syndr. 52, 553–559.
15. Buckner, C. M., Calderon, T. M., Willams, D. W., Belbin, T. J., Berman, J. W. (2011) Characterization of monocyte maturation/differentiation that facilitates their transmigration across the blood-brain barrier and infection by HIV: implications for NeuroAIDS. Cell. Immunol. 267, 109–123.
16. Williams, D. W., Calderon, T. M., Lopez, L., Carvallo-Torres, L., Gaskill, P. J., Eugenin, E. A., Morgello, S., Berman, J. W. (2013) Mechanisms of HIV entry into the CNS: increased sensitivity of HIV infected CD14 +CD16+ monocytes to CCL2 and key roles of CCR2, JAM-A, and ALCAM in diapedesis. PLoS ONE 8, e69270.
17. Hemkens, L. G., Bucher, H. C. (2014) HIV infection and cardiovascular disease. Eur. Heart J. 35, 1373–1381.
18. Eugenin, E. A., Berman, J. W. (2003) Chemokine-dependent mechanisms of leukocyte trafficking across a model of the blood-brain barrier. Methods 29, 351–361.
19. Weiss, J. M., Berman, J. W. (1998) Astrocyte expression of monocyte chemoattractant protein-1 is differentially regulated by transforming growth factor beta. J. Neuroimmunol. 91, 190–197.
20. Hume, D. A., MacDonald, K. P. A. (2012) Therapeutic applications of macrophage colony-stimulating factor-1 (CSF-1) and antagonists of CSF-1 receptor (CSF-1R) signaling. Blood 119, 1810–1820.
21. Li, M., Ransohoff, R. M. (2008) Multiple roles of chemokine CXCL12 in the central nervous system: a migration from immunology to neurobiology. Prog. Neurobiol. 84, 116–131.
22. Hearps, A. C., Martin, G. E., Angelovich, T. A., Cheng, W.-J., Maisa, A., Landay, A. L., Jaworowski, A., Crowe, S. M. (2012) Aging is associated with chronic innate immune activation and dysregulation of monocyte phenotype and function. Aging Cell 11, 867–875.
23. Wrigley, B. J., Shantsila, E., Tapp, L. D., Lip, G. Y. H. (2013) CD14++CD16+ monocytes in patients with acute ischaemic heart failure. Eur. J. Clin. Invest. 43, 121–130.
24. Hearps, A. C., Martin, G. E., Rajasuriar, R., Crowe, S. M. (2014) Inflammatory co-morbidities in HIV+ individuals: learning lessons from healthy ageing. Curr. HIV/AIDS Rep. 11, 20–34.
25. Baker, J. V., Hullsiek, K. H., Singh, A., Wilson, E., Henry, K., Lichtenstein, K., Onen, N., Kojic, E., Patel, P., Brooks, J. T., Hodis, H. N., Budoff, M., Sereti, I.; CDC SUN Study Investigators. (2014) Immunologic predictors of coronary artery calcium progression in a contemporary HIV cohort. AIDS 28, 831–840.
26. Thienemann, F., Sliwa, K., Rockstroh, J. K. (2013) HIV and the heart: the impact of antiretroviral therapy: a global perspective. Eur. Heart J. 34, 3538–3546.
27. Fischer-Smith, T., Tedaldi, E. M., Rappaport, J. (2008) CD163/CD16 coexpression by circulating monocytes/macrophages in HIV: potential biomarkers for HIV infection and AIDS progression. AIDS Res. Hum. Retroviruses 24, 417–421.
28. Burdo, T. H., Weiffenbach, A., Woods, S. P., Letendre, S., Ellis, R. J., Williams, K. C. (2013) Elevated sCD163 in plasma but not cerebrospinal fluid is a marker of neurocognitive impairment in HIV infection. AIDS 27, 1387–1395.
29. Krishnan, S., Wilson, E. M. P., Sheikh, V., Rupert, A., Mendoza, D., Yang, J., Lempicki, R., Migueles, S. A., Sereti, I. (2014) Evidence for innate immune system activation in HIV type 1-infected elite controllers. J. Infect. Dis. 209, 931–939.
30. Giri, M. S., Nebozyhn, M., Raymond, A., Gekonge, B., Hancock, A., Creer, S., Nicols, C., Yousef, M., Foulkes, A. S., Mounzer, K., Shull, J., Silvestri, G., Kostman, J., Collman, R. G., Showe, L., Montaner, L. J. (2009) Circulating monocytes in HIV-1-infected viremic subjects exhibit an antiapoptosis gene signature and virus- and host-mediated apoptosis resistance. J. Immunol. 182, 4459–4470.
31. Greenwood, J., Heasman, S. J., Alvarez, J. I., Prat, A., Lyck, R., Engelhardt, B. (2011) Review: leucocyte-endothelial cell crosstalk at the blood-brain barrier: a prerequisite for successful immune cell entry to the brain. Neuropathol. Appl. Neurobiol. 37, 24–39.
32. Ballabh, P., Braun, A., Nedergaard, M. (2004) The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol. Dis. 16, 1–13.
33. Abbott, N. J., Rönnbäck, L., Hansson, E. (2006) Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7, 41–53.
34. Ikeda, K., Quertermous, T. (2004) Molecular isolation and characterization of a soluble isoform of activated leukocyte cell adhesion molecule that modulates endothelial cell function. J. Biol. Chem. 279, 55315–55323.
35. Bazzoni, G. (2003) The JAM family of junctional adhesion molecules. Curr. Opin. Cell Biol. 15, 525–530.
36. Koenen, R. R., Pruessmeyer, J., Soehnlein, O., Fraemohs, L., Zernecke, A., Schwarz, N., Reiss, K., Sarabi, A., Lindbom, L., Hackeng, T. M., Weber, C., Ludwig, A. (2009) Regulated release and functional modulation of junctional adhesion molecule A by disintegrin metalloproteinases. Blood 113, 4799–4809.
37. Ostermann, G., Fraemohs, L., Baltus, T., Schober, A., Lietz, M., Zernecke, A., Liehn, E. A., Weber, C. (2005) Involvement of JAM-A in mononuclear cell recruitment on inflamed or atherosclerotic endothelium: inhibition by soluble JAM-A. Arterioscler. Thromb. Vasc. Biol. 25, 729–735.
38. Masedunskas, A., King, J. A., Tan, F., Cochran, R., Stevens, T., Sviridov, D., Ofori-Acquah, S. F. (2006) Activated leukocyte cell adhesion molecule is a component of the endothelial junction involved in transendothelial monocyte migration. FEBS Lett. 580, 2637–2645.
39. Gimferrer, I., Calvo, M., Mittelbrunn, M., Farnós, M., Sarrias, M. R., Enrich, C., Vives, J., Sánchez-Madrid, F., Lozano, F. (2004) Relevance of CD6-mediated interactions in T cell activation and proliferation. J. Immunol. 173, 2262–2270.
40. Zimmerman, A. W., Joosten, B., Torensma, R., Parnes, J. R., van Leeuwen, F. N., Figdor, C. G. (2006) Long-term engagement of CD6 and ALCAM is essential for T-cell proliferation induced by dendritic cells. Blood 107, 3212–3220.
41. Pinto, M., Carmo, A. M. (2013) CD6 as a therapeutic target in autoimmune diseases: successes and challenges. BioDrugs 27, 191–202.
42. Tada, H., Rappaport, J., Lashgari, M., Amini, S., Wong-Staal, F., Khalili, K. (1990) Trans-activation of the JC virus late promoter by the tat protein of type 1 human immunodeficiency virus in glial cells. Proc. Natl. Acad. Sci. USA 87, 3479–3483.
43. Dubois, V., Dutronc, H., Lafon, M. E., Poinsot, V., Pellegrin, J. L., Ragnaud, J. M., Ferrer, A. M., Fleury, H. J. (1997) Latency and reactivation of JC virus in peripheral blood of human immunodeficiency virus type 1-infected patients. J. Clin. Microbiol. 35, 2288–2292.
44. Chen, Y., Bord, E., Tompkins, T., Miller, J., Tan, C. S., Kinkel, R. P., Stein, M. C., Viscidi, R. P., Ngo, L. H., Koralnik, I. J. (2009) Asymptomatic reactivation of JC virus in patients treated with natalizumab. N. Engl. J. Med. 361, 1067–1074.
45. Jilek, S., Mathias, A., Canales, M., Lysandropoulos, A., Pantaleo, G., Schluep, M., Du Pasquier, R. A. (2013) Natalizumab treatment alters the expression of T-cell trafficking marker LFA-1 a-chain (CD11a) in MS patients. Mult. Scler. 20, 837–842.
46. Ransohoff, R. M. (2007) Natalizumab for multiple sclerosis. N. Engl. J. Med. 356, 2622–2629.
47. Bowen, M. A., Patel, D. D., Li, X., Modrell, B., Malacko, A. R., Wang, W. C., Marquardt, H., Neubauer, M., Pesando, J. M., Francke, U., Haynes, B. F., Aruffo, A. (1995) Cloning, mapping, and characterization of activated leukocyte-cell adhesion molecule (ALCAM), a CD6 ligand. J. Exp. Med. 181, 2213–2220.
48. Fessler, M. B., Malcolm, K. C., Duncan, M. W., Worthen, G. S. (2002) A genomic and proteomic analysis of activation of the human neutrophil by lipopolysaccharide and its mediation by p38 mitogen-activated protein kinase. J. Biol. Chem. 277, 31291–31302.
49. Hosking, M. P., Liu, L., Ransohoff, R. M., Lane, T. E. (2009) A protective role for ELR+ chemokines during acute viral encephalomyelitis. PLoS Pathog. 5, e1000648.
50. Yan, X. T., Tumpey, T. M., Kunkel, S. L., Oakes, J. E., Lausch, R. N. (1998) Role of MIP-2 in neutrophil migration and tissue injury in the herpes simplex virus-1-infected cornea. Invest. Ophthalmol. Vis. Sci. 39, 1854–1862.
51. Gorina, R., Lyck, R., Vestweber, D., Engelhardt, B. (2014) b2 Integrinmediated crawling on endothelial ICAM-1 and ICAM-2 is a prerequisite for transcellular neutrophil diapedesis across the inflamed blood-brain barrier. J. Immunol. 192, 324–337.
52. Allen, C., Thornton, P., Denes, A., McColl, B. W., Pierozynski, A., Monestier, M., Pinteaux, E., Rothwell, N. J., Allan, S. M. (2012) Neutrophil cerebrovascular transmigration triggers rapid neurotoxicity through release of proteases associated with decondensed DNA. J. Immunol. 189, 381–392.
53. Wojkowska, D. W., Szpakowski, P., Ksiazek-Winiarek, D., Leszczynski, M., Glabinski, A. (2014) Interactions between neutrophils, Th17 cells, and chemokines during the initiation of experimental model of multiple sclerosis. Mediators Inflamm. 2014, 590409.
54. Xu, H., Oliveira-Sales, E. B., McBride, F., Liu, B., Hewinson, J., Toward, M., Hendy, E. B., Graham, D., Dominiczak, A. F., Giannotta, M., Waki, H., Ascione, R., Paton, J. F., Kasparov, S. (2012) Upregulation of junctional adhesion molecule-A is a putative prognostic marker of hypertension. Cardiovasc. Res. 96, 552–560.
55. Schmitt, M. M. N., Megens, R. T. A., Zernecke, A., Bidzhekov, K., van den Akker, N. M., Rademakers, T., van Zandvoort, M. A., Hackeng, T. M., Koenen, R. R., Weber, C. (2014) Endothelial junctional adhesion molecule-a guides monocytes into flow-dependent predilection sites of atherosclerosis. Circulation 129, 66–76.
56. Martin, G. E., Gouillou, M., Hearps, A. C., Angelovich, T. A., Cheng, A. C., Lynch, F., Cheng, W.-J., Paukovics, G., Palmer, C. S., Novak, R. M., Jaworowski, A., Landay, A. L., Crowe, S. M. (2013) Age-associated changes in monocyte and innate immune activation markers occur more rapidly in HIV infected women. PLoS One 8, e55279.