The cannabinoid delta-9-tetrahydrocannabinol mediates inhibition of macrophage chemotaxis to RANTES/CCL5: Linkage to the CB2 receptor

Journal of NeuroImmune Pharmacology

Volumn 3, Issue 2, 2008, Pages 117-129

  Raborn, Erinn S ^a   Marciano Cabral, Francine ^a   Buckley, Nancy E ^b   Martin, Billy R ^a   Cabral, Guy A ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b CALIFORNIA STATE POLYTECHNIC UNIVERSITY   (United States)

Author keywords

Cannabinoid; Cannabinoid receptor; CB2; CCL5; Chemokine; Chemokine receptor; Chemotaxis; Cross deactivation; Delta 9 tetrahydrocannabinol; Macrophages; Marijuana; RANTES; THC

Indexed keywords

1 (4 (1,1 DIMETHYLHEPTYL) 2,6 DIMETHOXYPHENYL) 3 METHYLCYCLOHEXANOL; 1-(4-(1,1-DIMETHYLHEPTYL)-2,6-DIMETHOXYPHENYL)-3-METHYLCYCLOHEXANOL; 3 (2 HYDROXY 4 (1,1 DIMETHYLHEPTYL)PHENYL) 4 (3 HYDROXYPROPYL)CYCLOHEXANOL; 3-(2-HYDROXY-4-(1,1-DIMETHYLHEPTYL)PHENYL)-4-(3-HYDROXYPROPYL)CYCLOHEXANOL; 5 (4 CHLORO 3 METHYLPHENYL) 1 (4 METHYLBENZYL) N (1,3,3 TRIMETHYLBICYCLO[2.2.1]HEPTAN 2 YL) 3 PYRAZOLECARBOXAMIDE; ARACHIDONIC ACID DERIVATIVE; ARACHIDONYL 2 CHLOROETHYLAMIDE; ARACHIDONYL-2-CHLOROETHYLAMIDE; BORNANE DERIVATIVE; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CCR1 PROTEIN, MOUSE; CHEMOKINE RECEPTOR CCR1; CHEMOKINE RECEPTOR CCR5; CYCLOHEXANOL DERIVATIVE; G PROTEIN COUPLED RECEPTOR; MESSENGER RNA; PIPERIDINE DERIVATIVE; PYRAZOLE DERIVATIVE; RANTES; RIMONABANT; TETRAHYDROCANNABINOL;

ANIMAL; ARTICLE; BIOSYNTHESIS; C57BL MOUSE; CHEMOTAXIS; DRUG ANTAGONISM; DRUG EFFECT; FEMALE; GENETICS; MOUSE; MOUSE MUTANT; PERITONEUM MACROPHAGE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ARACHIDONIC ACIDS; BORNANES; CHEMOKINE CCL5; CHEMOTAXIS; CYCLOHEXANOLS; FEMALE; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PIPERIDINES; PYRAZOLES; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2; RECEPTORS, CCR1; RECEPTORS, CCR5; RECEPTORS, G-PROTEIN-COUPLED; RNA, MESSENGER; SIGNAL TRANSDUCTION; TETRAHYDROCANNABINOL;

EID: 43449130045     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-007-9077-z     Document Type: Article

References (74)

1. Bajetto A, Bonavia R, Barbero S, Schettini G (2002) Characterization of chemokines and their receptors in the central nervous system: physiopathological implications. J Neurochem 82:1311-1329
2. Baggiolini M, Dewald B, Moser B (1994) Interleukin-8 and related chemotactic cytokines CXC and CC chemokines. Adv Immunol 55:97-179
3. Baggiolini M, Dewald B, Moser B (1997) Human chemokines: an update. Annu Rev Immunol 15:675-705
4. Becker EL (1977) Stimulated neutrophil locomotion: chemokinesis and chemotaxis. Arch Pathol Lab Med 101:509-513
5. Berdyshev EV, Schmid PC, Krebsbach RJ, Hillard CJ, Huang C, Chen N, Dong Z, Schmid HH (2001) Cannabinoid-receptor-independent cell signaling by N-acylethanolamines. Biochem J 360:67-75
6. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
7. Buckley NE, McCoy KL, Mezey E, Bonner T, Zimmer A, Felder CC, Glass M, Zimmer A (2000) Immunomodulation by cannabinoids is absent in mice deficient for the cannabinoid CB(2) receptor. Eur J Pharmacol 396:141-149
8. Cabral GA, Dove Pettit DA (1998) Drugs and immunity: cannabinoids and their role in decreased resistance to infectious disease. J Neuroimmunol 83:116-123
9. Cabral GA, Staab A (2005) Effects on the immune system. In: Pertwee R (ed) Handbook on experimental pharmacology: cannabinoids. Springer, Berlin, pp 385-423
10. Cabral GA, Toney DM, Fischer-Stenger K, Harrison MP, Marciano-Cabral FM (1995) Anandamide inhibits macrophage-mediated killing of tumor necrosis-sensitive cells. Life Sci 56:2065-2072
11. 1-tetrahydrocannabinol on red blood cell membranes and alveolar macrophages. In: Nahas GG (ed) Marihuana: Chemistry, biochemistry, and cellular effects. Springer, New York, pp 273-281
12. Charo IF, Ransohoff RM (2006) Mechanisms of disease: The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med 354:610-621
13. Chuchawankul S, Shima M, Buckley NE, Hartmann CB, McCoy KL (2004) Role of cannabinoid receptors in inhibiting macrophage costimulatory activity. Int Immunopharmacol 4:265-278
14. Daaka Y, Friedman H, Klein TW (1996) Cannabinoid receptor proteins are increased in Jurkat, human T-cell line after mitogen activation. J Pharmacol Exp Ther 276:776-783
15. Drath DB, Shorey JM, Price L, Huber GL (1979) Metabolic and functional characteristics of alveolar macrophages recovered from rats exposed to marijuana smoke. Infect Immun 25:268-272
16. Ehrhart J, Obregon D, Mori T, Hou H, Sun N, Bai Y, Klein T, Fernandez F, Tan J, Shytle RD (2005) Stimulation of cannabinoid receptor 2 (CB2) suppresses microglial activation. J Neuroinflammation 2:29-41
17. Felder CC, Veluz JS, Williams HL, Briley EM, Matsuda LA (1992) Cannabinoid agonists stimulate both receptor- and non-receptor-mediated signal transduction pathways in cells transfected with and expressing cannabinoid receptor clones. Mol Pharmacol 42:838-845
18. Friedman M, Cepero ML, Klein T, Friedman H (1986) Suppressive effect of delta 9-tetrahydrocannabinol in vitro on phagocytosis by murine macrophages. Proc Soc Exp Biol Med 182:225-228
19. Galiegue S, Mary S, Marchand J, Dussossoy D, Carriere D, Carayon P, Bouaboula M, Shire D, Le Fur G, Casellas P (1995) Expression of central and peripheral cannabinoid receptors in human immune tissues and leukocyte subpopulations. Eur J Biochem 232:54-61
20. Gerard C, Gerard NP (1994) C5A anaphylatoxin and its seven transmembrane-segment receptor. Annu Rev Immunol 12:775-808
21. 2 modulates the CXCL12/CXCR4-mediated chemotaxis of T lymphocytes. Mol Immunol 43:2169-2179
22. Goldman DW, Goetzl EJ (1982) Specific binding of leukotriene B4 to receptors on human polymorphonuclear leukocytes. J Immunol 129:1600-1604
23. Grimm MC, Ben-Baruch A, Taub DD, Howard OM, Resau JH, Wang JM, Ali H, Richardson R, Snyderman R, Oppenheim JJ (1998) Opiates transactivate chemokine receptors: delta and mu opiate receptor-mediated heterologous desensitization. J Exp Med 188:317-325
24. Hanahan DJ (1986) Platelet activating factor: a biologically active phosphoglyceride. Annu Rev Biochem 55:483-509
25. Harris H (1953) Chemotaxis of monocytes. Br J Exp Pathol 34:276-279
26. Harris H (1954) Role of chemotaxis in inflammation. Physiol Rev 34:529-562
27. Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, Rice KC (1991) Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 11:563-583
28. Huber GL, Pochay VE, Shea JW, Hinds WC, Weker RR, First MW, Sornberger GC (1978) An experimental animal model for quantifying the biologic effects of marijuana on the defense system of the lung. Adv Biosci 22-23:301-328
29. Huber GL, Simmons GA, McCarthy CR, Cutting MB, Laguarda R, Pereira W (1975) Depressant effect of marihuana smoke on antibactericidal activity of pulmonary alveolar macrophages. Chest 68:769-773
30. Jin T, Hereld D (2006) Moving toward understanding eukaryotic chemotaxis. Eur J Cell Biol 85:905-913
31. Jordá MA, Verbakel SE, Valk PJ, Vankan-Berkhoudt YV, Maccarrone M, Finazzi-Agró A, Löwenberg B, Delwel (2002) Hematopoietic cells expression the peripheral cannabinoid receptor migrate in response to the endocannabinoid 2-arachidonoylglycerol. Blood 99:2786-2793
32. Kehrl JH (2006) Chemoattractant receptor signaling and the control of lymphocyte migration. Immunol Res 34:211-227
33. Keller HU, Wissler JH, Hess MW, Cottier H (1978) Distinct chemokinetic and chemotactic responses in neutrophil granulocytes. Eur J Immunol 8:1-7
34. Kim CH (2004) Chemokine chemokine-receptor network in immune cell trafficking. Curr Drug Targets Immune Endocr Metabol Disord 4:343-361
35. Kishimoto S, Muramatsu M, Gokoh M, Oka S, Waku K, Sugiura T (2005) Endogenous cannabinoid receptor ligand induces the migration of human natural killer cells. J Biochem 137:217-223
36. Klein TW, Friedman H, Specter S (1998) Marijuana, immunity and infection. J Neuroimmunol 83:102-115
37. Klein TW, Newton CA, Widen R, Friedman H (1985) The effect of delta-9-tetrahydrocannabinol and 11-hydroxy-delta-9-tetrahydrocannabinol on T-lymphocyte and B-lymphocyte mitogen responses. J Immunopharmacol 7:451-466
38. Lauffenburger DA, Horwitz AF (1996) Cell migration: a physically integrated molecular process. Cell 84:359-369
39. Le Y, Zhou Y, Iribarren P, Wang J (2004) Chemokines and chemokine receptors: their manifold roles in homeostasis and disease. Cell Mol Immunol 1:95-104
40. Lopez-Cepero M, Friedman M, Klein T, Friedman H (1986) Tetrahydrocannabinol-induced suppression of macrophage spreading and phagocytic activity in vitro. J Leukoc Biol 39:679-686
41. Makriyannis A, Yang DP, Griffin RG, Das Gupta SK (1990) The perturbation of model membranes by (-)-delta 9-tetrahydrocannabinol. Studies using solid-state 2H- and 13C-NMR. Biochim Biophys Acta 1028:31-42
42. Mann PE, Cohen AB, Finley TN, Ladman AJ (1971) Alveolar macrophages. Structural and functional differences between non-smokers and smokers of marijuana and tobacco. Lab Invest 25:111-120
43. Martin BR (1986) Cellular effects of cannabinoids. Pharmacol Rev 38:45-74
44. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346:561-564
45. McCarthy CR, Cutting MB, Simmons GA, Pereira W, Laguarda R, Huber GL (1976) The effect of marihuana on the in vitro function of pulmonary alveolar macrophages. In: Braude MC, Szara S (eds) Pharmacology of marihuana, Vol. 1. Raven, New York, pp 211-216
46. McCoy K, Gainey D, Cabral G (1995) Delta-9-tetrahydrocannabinol modulates antigen processing by macrophages. J Pharmacol Exp Ther 273:1216-1223
47. McCoy KL, Matveyeva M, Carlisle SJ, Cabral GA (1999) Cannabinoid inhibition of the processing of intact lysozyme by macrophages: evidence for CB2 receptor participation. J Pharmacol Exp Ther 289:1620-1625
48. Mitchison TJ, Cramer LP (1996) Actin-based cell motility and cell locomotion. Cell 84:371-379
49. Munro S, Thomas KL, Abu-Shaar M (1993) Molecular characterization of a peripheral receptor for cannabinoids. Nature 365:61-65
50. Murdoch C, Finn A (2000) Chemokine receptors and their role in inflammation and infectious disease. Blood 95:3032-3043
51. Murphy PM (2002) International Union of Pharmacology. XXX. Update on Chemokine Receptor Nomenclature. Pharmacol Rev 54:227-229
52. Price TJ, Patwardhan A, Akopian AN, Hargreaves KM, Flores CM (2004) Cannabinoid receptor-independent actions of the aminoalkylindole WIN 55,212-2 on trigeminal sensory neurons. Br J Pharmacol 142:257-266
53. Puffenbarger R, Boothe C, Cabral G (2000) Cannabinoids inhibit LPS-inducible cytokine mRNA expression in rat microglial cells. Glia 29:58-69
54. Raz A, Goldman R (1976) Effect of hashish compounds on mouse peritoneal macrophages. Lab Invest 34:69-76
55. Rios CD, Gomes I, Devi LA (2006) Mu opioid and CB1 cannabinoid receptor interactions: reciprocal inhibition of receptor signaling and neuritogenesis. Br J Pharmacol 148:387-395
56. Rios CD, Jordan BA, Gomes I, Devi LA (2001) G-protein-coupled receptor dimerization: modulation of receptor function. Pharmacol Ther 92:71-87
57. Rogers TJ, Steele AD, Howard OMZ, Oppenheim JJ (2000) Bidirectional heterologous desensitization of opioid and chemokine receptors. Ann N Y Acad Sci 917:19-28
58. Sacerdote P, Martucci C, Vaccani A, Bariselli F, Panerai AE, Colombo A, Parolaro D, Massi P (2005) The nonpsychoactive component of marijuana cannabidiol modulates chemotaxis and IL-10 and IL-12 production of murine macrophages both in vivo and in vitro J Neuroimmunol 159:97-105
59. Sacerdote P, Massi P, Panerai AE, Parolaro D (2000) In vivo and in vitro treatment with the synthetic cannabinoid CP55, 940 decreases the in vitro migration of macrophages in the rat: involvement of both CB1 and CB2 receptors. J Neuroimmunol 109:155-163
60. Schiffmann E, Corcoran BA, Wahl SM (1975) N-formyl-methionyl peptides as chemoattractants for leucocytes. Proc Natl Acad Sci U S A 72:1059-1062
61. Specter SC, Klein TW, Newton C, Mondragon M, Widen R, Friedman H (1986) Marijuana effects on immunity: suppression of human natural killer cell activity of delta-9-tetrahydrocannabinol. Int J Immunopharmacol 8:741-745
62. Specter S, Lancz G, Goodfellow D (1991) Suppression of human macrophage function in vitro by delta-9-tetrahydrocannabinol. J Leukocyte Biol 50:423-426
63. Stefano GB, Salzet M, Rialas CM, Mattocks D, Fimiani C, Bilfinger TV (1998) Macrophage behavior associated with acute and chronic exposure to HIV GP120, morphine and anandamide: endothelial implications. Int J Cardiol 64(Suppl 1):S3-S13
64. Suzuki S, Chuang L, Yau P, Doi R, Chuang R (2002) Interactions of opioid and chemokine receptors: oligomerization of mu, kappa, and delta with CCR5 on immune cells. Exp Cell Res 280:192-200
65. Szabo I, Rogers TJ (2001) Crosstalk between chemokine and opioid receptors results in downmodulation of cell migration. Adv Exp Med Biol 493:75-79
66. Szabo I, Wetzel M, McCarthy L, Steele A, Henderson E, Howard OMZ, Oppenheim JJ, Rogers TJ (2001) Interactions of opioid receptors, chemokines and chemokine receptors. Adv Exp Med Biol 493:69-74
67. Szabo I, Chen XH, Xin L, Adler MW, Howard OMZ, Oppenheim JJ, Rogers TJ (2002) Heterologous desensitization of opioid receptors by chemokines inhibits chemotaxis and enhances the perception of pain. Proc Natl Acad Sci U S A 99:10276-10281
68. Tang JL, Lancz G, Specter S, Bullock H (1992) Marijuana and immunity: tetrahydrocannabinol-mediated inhibition of growth and phagocyte activity of the murine macrophage cell line, P388D1. Int J Immunopharmacol 14:253-262
69. Waksman Y, Olson JM, Carlisle SJ, Cabral GA (1999) The central cannabinoid receptor (CB1) mediates inhibition of nitric oxide production by rat microglial cells. J Pharmacol Exp Ther 288:1357-1366
70. Walter L, Franklin A, Witting A, Wade C, Xie Y, Kunos G, Mackie K, Stella N (2003) Nonpsychotropic cannabinoid receptors regulate microglial cell migration. J Neurosci 23:1398-1405
71. Watzl B, Scuderi P, Watson RR (1991) Marijuana components stimulate human peripheral blood mononuclear cell secretion of interferon-gamma and suppresses interleukin-1 alpha in vitro. Int J Immunopharmacol 13:1091-1097
72. 2+- independent protein kinase Cs mediate heterologous desensitization of leukocyte chemokine receptors by opioid receptors. J Biol Chem 278:12729-12736
73. Zheng ZM, Specter S, Friedman H (1992) Inhibition by delta-9- tetrahydrocannabinol of tumor necrosis factor alpha production by mouse and human macrophages. Int J Immunopharmacol 14:1445-1452
74. Zimmerman S, Zimmerman AM, Cameron IL, Laurence HL (1977) Delta1-tetrahydrocannabinol, cannabidiol and cannabinol effects on the immune response of mice. Pharmacology 15:10-23