Attenuation of HIV-1 replication in macrophages by cannabinoid receptor 2 agonists

Journal of Leukocyte Biology

Volumn 93, Issue 5, 2013, Pages 801-810

  Ramirez, Servio H ^a   Reichenbach, Nancy L ^a   Fan, Shongshan ^a   Rom, Slava ^a   Merkel, Steven F ^a   Wang, Xu ^a   Ho, Wen Zhe ^a   Persidsky, Yuri ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CB2; CCR5; CXCR4; Encephalitis; JWH133; Neuroinflammation

Indexed keywords

1 DEOXY 3 (1,1 DIMETHYLBUTYL) DELTA8 TETRAHYDROCANNABINOL; 5 (4 CHLORO 3 METHYLPHENYL) 1 (4 METHYLBENZYL) N (1,3,3 TRIMETHYLBICYCLO[2.2.1]HEPTAN 2 YL) 3 PYRAZOLECARBOXAMIDE; CANNABINOID 2 RECEPTOR; CANNABINOID 2 RECEPTOR AGONIST; IMMUNOMODULATING AGENT; RESORCINOL;

ARTICLE; CELL DIFFERENTIATION; CELL VIABILITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; IMMUNOREACTIVITY; IN VITRO STUDY; MACROPHAGE; MONOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS ENTRY; VIRUS INHIBITION; VIRUS REPLICATION;

ANISOLES; CANNABINOID RECEPTOR AGONISTS; CANNABINOIDS; CELLS, CULTURED; HIV LONG TERMINAL REPEAT; HIV-1; HUMANS; INDENES; MACROPHAGES; PYRAZOLES; RECEPTOR, CANNABINOID, CB2; RECEPTORS, CCR5; RECEPTORS, CXCR4; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84877065224     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.1012523     Document Type: Article

References (37)

1. Ellis, R. J., Badiee, J., Vaida, F., Letendre, S., Heaton, R. K., Clifford, D., Collier, A. C., Gelman, B., McArthur, J., Morgello, S., McCutchan, J. A., Grant, I. (2011) CD4 nadir is a predictor of HIV neurocognitive impairment in the era of combination antiretroviral therapy. AIDS 25, 1747-1751.
2. Kraft-Terry, S. D., Buch, S. J., Fox, H. S., Gendelman, H. E. (2009) A coat of many colors: neuroimmune crosstalk in human immunodeficiency virus infection. Neuron 64, 133-145.
3. Thompson, K. A., Cherry, C. L., Bell, J. E., McLean, C. A. (2011) Brain cell reservoirs of latent virus in presymptomatic HIV-infected individuals. Am. J. Pathol. 179, 1623-1629.
4. Miller, A. M., Stella, N. (2008) CB2 receptor-mediated migration of immune cells: it can go either way. Br. J. Pharmacol. 153, 299-308.
5. Molina, P. E., Amedee, A., LeCapitaine, N. J., Zabaleta, J., Mohan, M., Winsauer, P., Vande Stouwe, C. (2011) Cannabinoid neuroimmune modulation of SIV disease. J. Neuroimmune Pharmacol. 6, 516-527.
6. Ellis, R. J., Toperoff, W., Vaida, F., van den Brande, G., Gonzales, J., Gouaux, B., Bentley, H., Atkinson, J. H. (2009) Smoked medicinal cannabis for neuropathic pain in HIV: a randomized, crossover clinical trial. Neuropsychopharmacology 34, 672-680.
7. Persidsky, Y., Ho, W., Ramirez, S. H., Potula, R., Abood, M. E., Unterwald, E., Tuma, R. (2011) HIV-1 infection and alcohol abuse: neurocognitive impairment, mechanisms of neurodegeneration and therapeutic interventions. Brain Behav. Immun. 25 (Suppl. 1), S61-S70.
8. Cosenza-Nashat, M. A., Bauman, A., Zhao, M. L., Morgello, S., Suh, H. S., Lee, S. C. (2011) Cannabinoid receptor expression in HIV encephalitis and HIV-associated neuropathologic comorbidities. Neuropathol. Appl. Neurobiol. 37, 464-483.
9. Rock, R. B., Gekker, G., Hu, S., Sheng, W. S., Cabral, G. A., Martin, B. R., Peterson, P. K. (2007) WIN55,212-2-mediated inhibition of HIV-1 expression in microglial cells: involvement of cannabinoid receptors. J. Neuroimmune Pharmacol. 2, 178-183.
10. Fraga, D., Raborn, E. S., Ferreira, G. A., Cabral, G. A. (2011) Cannabinoids inhibit migration of microglial-like cells to the HIV protein Tat. J. Neuroimmune Pharmacol. 6, 566-577.
11. Lu, T. S., Avraham, H. K., Seng, S., Tachado, S. D., Koziel, H., Makriyannis, A., Avraham, S. (2008) Cannabinoids inhibit HIV-1 Gp120-mediated insults in brain microvascular endothelial cells. J. Immunol. 181, 6406-6416.
12. Hu, S., Sheng, W. S., Rock, R. B. (2011) Immunomodulatory properties of κ opioids and synthetic cannabinoids in HIV-1 neuropathogenesis. J. Neuroimmune Pharmacol. 6, 528-539.
13. Gorantla, S., Makarov, E., Roy, D., Finke-Dwyer, J., Murrin, L. C., Gendelman, H. E., Poluektova, L. (2010) Immunoregulation of a CB2 receptor agonist in a murine model of neuroAIDS. J. Neuroimmune Pharmacol. 5, 456-468.
14. Wiley, J. L., Beletskaya, I. D., Ng, E. W., Dai, Z., Crocker, P. J., Mahadevan, A., Razdan, R. K., Martin, B. R. (2002) Resorcinol derivatives: a novel template for the development of cannabinoid CB(1)/CB(2) and CB(2)-selective agonists. J. Pharmacol. Exp. Ther. 301, 679-689.
15. Wahl, L. M., Katona, I. M., Wilder, R. L., Winter, C. C., Haraoui, B., Scher, I., Wahl, S. M. (1984) Isolation of human mononuclear cell subsets by counterflow centrifugal elutriation (CCE). I. Characterization of B-lymphocyte-, T-lymphocyte-, and monocyte-enriched fractions by flow cytometric analysis. Cell Immunol. 85, 373-383.
16. Ramirez, S. H., Fan, S., Dykstra, H., Reichenbach, N., Del Valle, L., Potula, R., Phipps, R. P., Maggirwar, S. B., Persidsky, Y. (2010) Dyad of CD40/CD40 ligand fosters neuroinflammation at the blood-brain barrier and is regulated via JNK signaling: implications for HIV-1 encephalitis. J. Neurosci. 30, 9454-9464.
17. Ghorpade, A., Nukuna, A., Che, M., Haggerty, S., Persidsky, Y., Carter, E., Carhart, L., Shafer, L., Gendelman, H. E. (1998) Human immunodeficiency virus neurotropism: an analysis of viral replication and cytopathicity for divergent strains in monocytes and microglia. J. Virol. 72, 3340-3350.
18. Guo, C. J., Li, Y., Tian, S., Wang, X., Douglas, S. D., Ho, W. Z. (2002) Morphine enhances HIV infection of human blood mononuclear phagocytes through modulation of β-chemokines and CCR5 receptor. J. Investig. Med. 50, 435-442.
19. Ramirez, S. H., Hasko, J., Skuba, A., Fan, S., Dykstra, H., McCormick, R., Reichenbach, N., Krizbai, I., Mahadevan, A., Zhang, M., Tuma, R., Son, Y. J., Persidsky, Y. (2012) Activation of cannabinoid receptor 2 attenuates leukocyte-endothelial cell interactions and blood-brain barrier dysfunction under inflammatory conditions. J. Neurosci. 32, 4004-4016.
20. Huffman, J. W., Liddle, J., Yu, S., Aung, M. M., Abood, M. E., Wiley, J. L., Martin, B. R. (1999) 3-(1′,1′-dimethylbutyl)-1-deoxy-Δ8-THC and related compounds: synthesis of selective ligands for the CB2 receptor. Bioorg. Med. Chem. 7, 2905-2914.
21. Murineddu, G., Lazzari, P., Ruiu, S., Sanna, A., Loriga, G., Manca, I., Falzoi, M., Dessi, C., Curzu, M. M., Chelucci, G., Pani, L., Pinna, G. A. (2006) Tricyclic pyrazoles. 4. Synthesis and biological evaluation of analogues of the robust and selective CB2 cannabinoid ligand 1-(2′,4′-dichlorophenyl)-6-methyl-N-piperidin-1-yl-1,4-dihydroindeno[1,2-c]pyrazo le-3-carboxamide. J. Med. Chem. 49, 7502-7512.
22. Montecucco, F., Burger, F., Mach, F., Steffens, S. (2008) CB2 cannabinoid receptor agonist JWH-015 modulates human monocyte migration through defined intracellular signaling pathways. Am. J. Physiol. Heart Circ. Physiol. 294, H1145-H1155.
23. Preet, A., Qamri, Z., Nasser, M. W., Prasad, A., Shilo, K., Zou, X., Groopman, J. E., Ganju, R. K. (2011) Cannabinoid receptors, CB1 and CB2, as novel targets for inhibition of non-small cell lung cancer growth and metastasis. Cancer Prev. Res. (Phila). 4, 65-75.
24. Pini, A., Mannaioni, G., Pellegrini-Giampietro, D., Passani, M. B., Mastroianni, R., Bani, D., Masini, E. (2012) The role of cannabinoids in inflammatory modulation of allergic respiratory disorders, inflammatory pain and ischemic stroke. Curr. Drug Targets 13, 984-993.
25. Roberts, T. K., Buckner, C. M., Berman, J. W. (2010) Leukocyte transmigration across the blood-brain barrier: perspectives on neuroAIDS. Front. Biosci. 15, 478-536.
26. Persidsky, Y., Ramirez, S. H., Haorah, J., Kanmogne, G. D. (2006) Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J. Neuroimmune Pharmacol. 1, 223-236.
27. Benito, C., Kim, W. K., Chavarria, I., Hillard, C. J., Mackie, K., Tolon, R. M., Williams, K., Romero, J. (2005) A glial endogenous cannabinoid system is upregulated in the brains of macaques with simian immunodeficiency virus-induced encephalitis. J. Neurosci. 25, 2530-2536.
28. Miller, L. K., Devi, L. A. (2011) The highs and lows of cannabinoid receptor expression in disease: mechanisms and their therapeutic implications. Pharmacol. Rev. 63, 461-470.
29. Benito, C., Tolon, R. M., Pazos, M. R., Nunez, E., Castillo, A. I., Romero, J. (2008) Cannabinoid CB2 receptors in human brain inflammation. Br. J. Pharmacol. 153, 277-285.
30. Cabral, G. A., Marciano-Cabral, F. (2005) Cannabinoid receptors in microglia of the central nervous system: immune functional relevance. J. Leukoc. Biol. 78, 1192-1197.
31. Raborn, E. S., Cabral, G. A. (2010) Cannabinoid inhibition of macrophage migration to the trans-activating (Tat) protein of HIV-1 is linked to the CB(2) cannabinoid receptor. J. Pharmacol. Exp. Ther. 333, 319-327.
32. Costantino, C. M., Gupta, A., Yewdall, A. W., Dale, B. M., Devi, L. A., Chen, B. K. (2012) Cannabinoid receptor 2-mediated attenuation of CXCR4-tropic HIV infection in primary CD4 T cells. PLoS One 7, e33961.
33. Peterson, P. K., Gekker, G., Hu, S., Cabral, G., Lokensgard, J. R. (2004) Cannabinoids and morphine differentially affect HIV-1 expression in CD4() lymphocyte and microglial cell cultures. J. Neuroimmunol. 147, 123-126.
34. Jeon, Y. J., Yang, K. H., Pulaski, J. T., Kaminski, N. E. (1996) Attenuation of inducible nitric oxide synthase gene expression by Δ 9-tetrahydrocannabinol is mediated through the inhibition of nuclear factor-κ B/Rel activation. Mol. Pharmacol. 50, 334-341.
35. Borner, C., Smida, M., Hollt, V., Schraven, B., Kraus, J. (2009) Cannabinoid receptor type 1-and 2-mediated increase in cyclic AMP inhibits T cell receptor-triggered signaling. J. Biol. Chem. 284, 35450-35460.
36. Abrams, D. I., Hilton, J. F., Leiser, R. J., Shade, S. B., Elbeik, T. A., Aweeka, F. T., Benowitz, N. L., Bredt, B. M., Kosel, B., Aberg, J. A., Deeks, S. G., Mitchell, T. F., Mulligan, K., Bacchetti, P., McCune, J. M., Schambelan, M. (2003) Short-term effects of cannabinoids in patients with HIV-1 infection: a randomized, placebo-controlled clinical trial. Ann. Intern. Med. 139, 258-266.
37. Soldan, S. S., Jacobson, S. (2010) Viral infections of the central nervous system: pathogenesis to therapeutics. J. Neuroimmune. Pharmacol. 5, 267-270.