High glucose enhances HIV entry into T cells through upregulation of CXCR4

Journal of Leukocyte Biology

Volumn 94, Issue 4, 2013, Pages 769-777

  Lan, Xiqian ^a   Cheng, Kang ^a   Chandel, Nirupama ^a   Lederman, Rivka ^a   Jhaveri, Aakash ^a   Husain, Mohammad ^a   Malhotra, Ashwani ^a   Singhal, Pravin C ^a  

^a DONALD AND BARBARA ZUCKER SCHOOL OF MEDICINE AT HOFSTRA NORTHWELL   (United States)

Author keywords

Antioxidants; Enzymes; HIF 1 ; Jurkat cells; LTR; Receptors; ROS

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; GLUCOSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; REACTIVE OXYGEN METABOLITE;

ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HYPERGLYCEMIA; LEUKEMIA CELL LINE; MOLECULAR MECHANICS; OXIDATIVE STRESS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; UPREGULATION; VIRUS ENTRY; VIRUS ENVELOPE;

ANTIOXIDANTS; ENZYMES; HIF-1Α; JURKAT CELLS; LTR; RECEPTORS; ROS;

CELL MEMBRANE; GENE SILENCING; GLUCOSE; HUMANS; HYDROGEN PEROXIDE; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; JURKAT CELLS; MODELS, BIOLOGICAL; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RECEPTORS, CXCR4; RNA, MESSENGER; T-LYMPHOCYTES; UP-REGULATION; VIRUS INTERNALIZATION;

EID: 84884886803     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0313142     Document Type: Article

References (61)

1. Joint United Nations Programme on HIV/AIDS (UNAIDS). (2012) Global report: UNAIDS report on the global AIDS epidemic 2012. UNAIDS, Geneva, Switzerland. Retrieved from http://www.unaids.org/en/ media/unaids/contentassets/documents/epidemiology/2012/gr2012/ 20121120_UNAIDS_Global_Report_2012_with_annexes_en.pdf/.
2. Centers for Disease Control. (2012) Estimated HIV incidence among adults and adolescents in the United States, 2007-2010. CDC, Atlanta, GA, USA. Retrieved from http://www.cdc.gov/hiv/statistics/pdf_hssr_ vol_17_no_4.pdf/.
3. Kaul, K., Tarr, J. M., Ahmad, S. I., Kohner, E. M., Chibber, R. (2012) Introduction to diabetes mellitus. Adv. Exp. Med. Biol. 771, 1-11.
4. Wild, S., Roglic, G., Green, A., Sicree, R., King, H. (2004) Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care. 27, 1047-1053.
5. Tzur, F., Chowers, M., Mekori, Y., Hershko, A. (2012) Prevalence of diabetes mellitus among Ethiopian-born HIV patients in Israel. J. Int. AIDS Soc. 15, 18158.
6. Rodriguez-Penney, A. T., Iudicello, J. E., Riggs, P. K., Doyle, K., Ellis, R. J., Letendre, S. L., Grant, I., Woods, S. P., and The HIV Neurobehavioral Research Program Hnrp Group. (2013) Co-morbidities in persons infected with HIV: increased burden with older age and negative effects on health-related quality of life. AIDS Patient Care STDS. 27, 5-16.
7. Dave, J. A., Lambert, E. V., Badri, M., West, S., Maartens, G., Levitt, N. S. (2011) Effect of nonnucleoside reverse transcriptase inhibitorbased antiretroviral therapy on dysglycemia and insulin sensitivity in South African HIV-infected patients. J. Acquir. Immune. Defic. Syndr. 57, 284-289.
8. Nasreddine, N., Borde, C., Gozlan, J., Bélec, L., Maréchal, V., Hocini, H. (2011) Advanced glycation end products inhibit both infection and transmission in trans of HIV-1 from monocyte-derived dendritic cells to autologous T cells. J. Immunol. 186, 5687-5695.
9. Rasmussen, L. D., Mathiesen, E. R., Kronborg, G., Pedersen, C., Gerstoft, J., Obel, N. (2012) Risk of diabetes mellitus in persons with and without HIV: a Danish nationwide population-based cohort study. PLoS One 7, e44575.
10. Tien, P. C., Schneider, M. F., Cole, S. R., Levine, A. M., Cohen, M., De-Hovitz, J., Young, M., Justman, J. E. (2008) Antiretroviral therapy exposure and insulin resistance in the Women's Interagency HIV study. J Acquir. Immune Defic Syndr. 49, 369-376.
11. Cuzin, L., Allavena, C., Morlat, P., Dellamonica, P. (2008) Boosted protease inhibitor-based or nonnucleoside reverse transcriptase-based HAART: is there a best choice for antiretroviral-naive HIV-1 infected patients? AIDS Rev. 10, 205-211.
12. Calza, L., Manfredi, R., Pocaterra, D., Chiodo, F. (2008) Risk of premature atherosclerosis and ischemic heart disease associated with HIV infection and antiretroviral therapy. J. Infect. 57, 16-32.
13. Tien, P. C., Schneider, M. F., Cole, S. R., Levine, A. M., Cohen, M., De-Hovitz, J., Young, M., Justman, J. E. (2007) Antiretroviral therapy exposure and incidence of diabetes mellitus in the Women's Interagency HIV Study. AIDS 21, 1739-17345.
14. Loisel-Meyer, S., Swainson, L., Craveiro, M., Oburoglu, L., Mongellaz, C., Costa, C., Martinez, M., Cosset, F. L., Battini, J. L., Herzenberg, L. A., Atkuri, K. R., Sitbon, M., Kinet, S., Verhoeyen, E., Taylor, N. (2012) Glut1-mediated glucose transport regulates HIV infection. Proc. Natl. Acad. Sci. U. S. A. 109, 2549-2554.
15. Tilton, J. C., and Doms, R. W. (2010) Entry inhibitors in the treatment of HIV-1 infection. Antiviral Res. 85, 91-100.
16. Henrich, T. J., Kuritzkes, D. R. (2013) HIV-1 entry inhibitors: recent development and clinical use. Curr. Opin. Virol. 3, 51-57.
17. Harrigan, P. R., Swenson, L., McGovern, R. A., Pollock, G. J. (2009) The determinants and consequences of HIV coreceptor switching. HIV Medical Update 4, Retrieved from http://www.cfenet.ubc.ca/publications/ determinants-and-consequences-hiv-coreceptor-switching/ Accessed Jan 21, 2013.
18. Poveda, E., Briz, V., Quiñones, M. M., Soriano, V. (2006) HIV tropism: diagnostic tools and implications for disease progression and treatment with entry inhibitors. AIDS. 20, 1359-1367.
19. Kamiyama, H., Kakoki, K., Shigematsu, S., Izumida, M., Yashima, Y., Tanaka, Y., Hayashi, H., Matsuyama, T., Sato, H., Yamamoto, N., Sano, T., Shidoji, Y., Kubo, Y. (2013) CXCR4-tropic, but not CCR5-tropic, human immunodeficiency virus infection is inhibited by the lipid raft-associated factors, acyclic retinoid analogs, and cholera toxin B subunit. AIDS Res. Hum. Retroviruses 29, 279-288.
20. By, Y., Durand-Gorde, J. M., Condo, J., Lejeune, P. J., Fenouillet, E., Guieu, R., Ruf, J. (2010) Monoclonal antibody-assisted stimulation of adenosine A2A receptors induces simultaneous downregulation of CXCR4 and CCR5 on CD4+ T-cells. Hum. Immunol. 71, 1073-1076.
21. + T cells through TLR2 activation. J. Immunol. 184, 2814-2824.
22. Juffermans, N. P., Paxton, W. A., Dekkers, P. E., Verbon, A., de Jonge, E., Speelman, P., van Deventer, S. J., van der Poll, T. (2000) Upregulation of HIV coreceptors CXCR4 and CCR5 on CD4(+) T cells during human endotoxemia and after stimulation with (myco) bacterial antigens: the role of cytokines. Blood 96, 2649-2654.
23. Sozzani, S., Ghezzi, S., Iannolo, G., Luini, W., Borsatti, A., Polentarutti, N., Sica, A., Locati, M., Mackay, C., Wells, T. N., Biswas, P., Vicenzi, E., Poli, G., Mantovani, A. (1998) Interleukin 10 increases CCR5 expression and HIV infection in human monocytes. J. Exp. Med. 187, 439-444.
24. Zella, D., Barabitskaja, O., Burns, J. M., Romerio, F., Dunn, D. E., Revello, M. G., Gerna, G., Reitz, M. S. Jr., Gallo, R. C., Weichold, F. F. (1998) Interferon-gamma increases expression of chemokine receptors CCR1, CCR3, and CCR5, but not in monocytoid U937 cells. Blood 91, 4444-4450.
25. Dolei, A., Biolchini, A., Serra, C., Curreli, S., Gomes, E., Dianzani, F. (1998) Increased replication of T-cell-tropic HIV strains and CXCchemokine receptor-4 induction in T cells treated with macrophage inflammatory protein (MIP)-1alpha, MIP-1beta and RANTES beta-chemokines. AIDS 12, 183-190.
26. Wahl, S. M., Greenwell-Wild, T., Peng, G., Hale-Donze, H., Doherty, T. M., Mizel, D., Orenstein, J. M. (1998) Mycobacterium avium complex augments macrophage HIV-1 production and increases CCR5 expression. Proc. Natl. Acad. Sci. U. S. A. 95, 12574-12579.
27. Wu, L., Paxton, W. A., Kassam, N., Ruffing, N., Rottman, J. B., Sullivan, N., Choe, H., Sodroski, J., Newman, W., Koup, R. A., Mackay, C. R. (1997) CCR5 levels and expression pattern correlate with infectability by macrophage-tropic HIV-1, in vitro. J. Exp. Med. 185, 1681-1691.
28. Planesas, J. M., Pérez-Nueno, V. I., Borrell, J. I., Teixidó, J. (2012) Impact of the CXCR4 structure on docking-based virtual screening of HIV entry inhibitors. J. Mol. Graph. Model. 38, 123-136.
29. Pan, J., Mestas, J., Burdick, M. D., Phillips, R. J., Thomas, G. V., Reckamp, K., Belperio, J. A., Strieter, R. M. (2006) Stromal derived factor-1 (SDF-1/CXCL12) and CXCR4 in renal cell carcinoma metastasis. Mol. Cancer 5, 56.
30. Ishikawa, T., Nakashiro, K., Klosek, S. K., Goda, H., Hara, S., Uchida, D., Hamakawa, H. (2009) Hypoxia enhances CXCR4 expression by activating HIF-1 in oral squamous cell carcinoma. Oncol. Rep. 21, 707-712.
31. Melchionna, R., Romani, M., Ambrosino, V., D'Arcangelo, D., Cencioni, C., Porcelli, D., Toietta, G., Truffa, S., Gaetano, C., Mangoni, A., Pozzoli, O., Cappuzzello, C., Capogrossi, M. C., Napolitano, M. (2010) Role of HIF-1αlpha in proton-mediated CXCR4 down-regulation in endothelial cells. Cardiovasc. Res. 86, 293-301.
32. Moriuchi, M., Moriuchi, H., Turner, W., Fauci, A. S. (1997) Cloning and analysis of the promoter region of CXCR4, a coreceptor for HIV-1 entry. J. Immunol. 159, 4322-4329.
33. Chetram, M. A., Hinton, C. V. (2012) ROS-mediated regulation of CXCR4 in Cancer Front. Biol.: doi10.1007/s11515-012-1204-4 [Epub ahead of print].
34. Jie, W., Wang, X., Zhang, Y., Guo, J., Kuang, D., Zhu, P., Wang, G., Ao, Q. (2010) SDF-1α/CXCR4 axis is involved in glucose-potentiated proliferation and chemotaxis in rat vascular smooth muscle cells. Int. J. Exp. Pathol. 91, 436-444.
35. Li, J., Zhao, S. Z., Wang, P. P., Yu, S. P., Zheng, Z., Xu, X. (2012) Calcium mediates high glucose-induced HIF-1α and VEGF expression in cultured rat retinal Müller cells through CaMKII-CREB pathway. Acta Pharmacol. Sin. 33, 1030-1036.
36. Zhang, H., Zhang, G., Gonzalez, F. J., Park, S. M., Cai, D. (2011) Hypoxiainducible factor directs POMC gene to mediate hypothalamic glucose sensing and energy balance regulation. PLoS Biol. 9, e1001112.
37. Yan, J., Zhang, Z., Shi, H. (2012) HIF-1 is involved in high glucose-induced paracellular permeability of brain endothelial cells. Cell. Mol. Life. Sci. 69, 115-128.
38. Isoe, T., Makino, Y., Mizumoto, K., Sakagami, H., Fujita, Y., Honjo, J., Takiyama, Y., Itoh, H., Haneda, M. (2010) High glucose activates HIF-1-mediated signal transduction in glomerular mesangial cells through a carbohydrate response element binding protein. Kidney Int. 78, 48-59.
39. Li, J., Wang, J. J., Yu, Q., Chen, K., Mahadev, K., Zhang, S. X. (2010) Inhibition of reactive oxygen species by Lovastatin downregulates vascular endothelial growth factor expression and ameliorates blood-retinal barrier breakdown in db/db mice: role of NADPH oxidase 4. Diabetes 59, 1528-1538.
40. Guo, S., Bragina, O., Xu, Y., Cao, Z., Chen, H., Zhou, B., Morgan, M., Lin, Y., Jiang, B. H., Liu, K. J., Shi, H. (2008) Glucose up-regulates HIF-1 alpha expression in primary cortical neurons in response to hypoxia through maintaining cellular redox status. J. Neurochem. 105, 1849-1860.
41. Rehman, S., Chandel, N., Salhan, D., Rai, P., Sharma, B., Singh, T., Husain, M., Malhotra, A.,. Singhal, P. C. (2013) Ethanol and vitamin D receptor in T cell apoptosis. J. Neuroimmune Pharmacol. 8, 251-261.
42. Chandel, N., Husain, M., Goel, H., Salhan, D., Lan, X., Malhotra, A., McGowan, J., and Singhal, P. (2013) VDR hypermethylation and HIVinduced T cell loss. J. Leuk. Bio. 93, 623-631.
43. Lan, X., Rai, P., Chandel, N., Cheng, K., Lederman, R., Saleem, M. A., Mathieson, P. W., Husain, M., Crosson, J. T., Gupta, K., Malhotra, A., Singhal, P. C. (2013) Morphine induces albuminuria by compromising podocyte integrity. PloS One 8, e55748.
44. Lan, X., Xu, J., Kiyota, T., Peng, H., Zheng, J. C., Ikezu, T. (2011) HIV-1 reduces Aβ-degrading enzymatic activities in primary human mononuclear phagocytes. J. Immunol. 186, 6925-6932.
45. Bonello, S., Zähringer, C., BelAiba, R. S., Djordjevic, T., Hess, J., Michiels, C., Kietzmann, T., Görlach, A. (2007) Reactive oxygen species activate the HIF-1αlpha promoter via a functional NFkappaB site. Arterioscler. Thromb. Vasc. Biol. 27, 755-761.
46. Edeas, M., Attaf, D., Mailfert, A. S., Nasu, M., Joubet, R. (2010) Maillard reaction, mitochondria and oxidative stress: potential role of antioxidants. Pathol. Biol. (Paris) 58, 220-225.
47. Yao, K., Ge, J. B., Sun, A. J., Hong, X. W., Shi, H. Y., Huang, R. C., Jia, Q. Z., Wang, K. Q., Zhong, C. P., Cao, X. T., Zou, Y. Z. (2006) Effects and mechanism of hyperglycemia on development and maturation and immune function of human monocyte derived dendritic cells [in Chinese]. Zhonghua Xin Xue Guan Bing Za Zhi 34, 60-64.
48. Quan, Y., Jiang, C. T., Xue, B., Zhu, S. G., Wang, X. (2011) High glucose stimulates TNF-α and MCP-1 expression in rat microglia via ROS and NF-κB pathways. Acta Pharmacol. Sin. 32, 188-193.
49. Wu, C. H., Wu, C. F., Huang, H. W., Jao, Y. C., Yen, G. C. (2009) Naturally occurring flavonoids attenuate high glucose-induced expression of proinflammatory cytokines in human monocytic THP-1 cells. Mol. Nutr. Food Res. 53, 984-995.
50. Ma, T., Zhu, J., Chen, X., Zha, D., Singhal, P. C., Ding, G. (2013) High glucose induces autophagy in podocytes. Exp. Cell Res. 319, 779-789.
51. Shah, A., Xia, L., Goldberg, H., Lee, K. W., Quaggin, S. E., Fantus, I. G. (2013) Thioredoxin-interacting protein mediates high glucoseinduced reactive oxygen species (ROS) generation by mitochondria and the NADPH oxidase, Nox4, in mesangial cells. J. Biol. Chem. 288, 6835-6848.
52. Li, Y., Jia, Y., Zhou, J., Huang, K. (2013) Effect of methionine sulfoxide reductase B1 silencing on high-glucose-induced apoptosis of human lens epithelial cells. Life Sci. 92, 193-201.
53. Valko, M., Leibfritz, D., Moncol, J., Cronin, M. T., Mazur, M., Telser, J. (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39, 44-84.
54. Bolin, A. P., Guerra, B. A., Nascimento, S. J., Otton, R. (2012) Changes in lymphocyte oxidant/antioxidant parameters after carbonyl and antioxidant exposure. Int. Immunopharmacol. 14, 690-697.
55. Hamed, S., Brenner, B., Abassi, Z., Aharon, A., Daoud, D., Roguin, A. (2010) Hyperglycemia and oxidized-LDL exert a deleterious effect on endothelial progenitor cell migration in type 2 diabetes mellitus. Thromb. Res. 126, 166-174.
56. Ceradini, D. J., Yao, D., Grogan, R. H., Callaghan, M. J., Edelstein, D., Brownlee, M., Gurtner, G. C. (2008) Decreasing intracellular superoxide corrects defective ischemia-induced new vessel formation in diabetic mice. J. Biol. Chem. 283, 10930-10938.
57. Dehne, N., Hintereder, G., Brüne, B. (2010) High glucose concentrations attenuate hypoxia-inducible factor-1alpha expression and signaling in non-tumor cells. Exp. Cell Res. 316, 1179-1189.
58. Ostrowski, M. A., Justement, S. J., Catanzaro, A., Hallahan, C. A., Ehler, L. A., Mizell, S. B., Kumar, P. N., Mican, J. A., Chun, T. W., Fauci, A. S. (1998) Expression of chemokine receptors CXCR4 and CCR5 in HIV-1-infected and uninfected individuals. J. Immunol. 161, 3195-3201.
59. Shanmugam, N., Reddy, M. A., Guha, M., Natarajan, R. (2003) High glucose-induced expression of proinflammatory cytokine and chemokine genes in monocytic cells. Diabetes 52, 1256-1264.
60. Granowitz, E. V., Saget, B. M., Wang, M. Z., Dinarello, C. A., Skolnik, P. R. (1995) Interleukin 1 induces HIV-1 expression in chronically infected U1 cells: blockade by interleukin 1 receptor antagonist and tumor necrosis factor binding protein type 1. Mol. Med. 1, 667-677.
61. Fakruddin, J. M., Laurence, J. (2004) Interactions among human immunodeficiency virus (HIV)-1, interferon-γ and receptor of activated NF-κ B ligand (RANKL): implications for HIV pathogenesis. Clin. Exp. Immunol. 137, 538-545, 2004 September.