CXCR1/2 ligands induce p38 MAPK-dependent translocation and release of opioid peptides from primary granules in vitro and in vivo

Brain, Behavior, and Immunity

Volumn 21, Issue 8, 2007, Pages 1021-1032

  Rittner, Heike L ^a   Labuz, Dominika ^a   Richter, Jan F ^a   Brack, Alexander ^a   Schäfer, Michael ^a   Stein, Christoph ^a   Mousa, Shaaban A ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Endorphin; Antinociception; Chemokine; Inflammatory pain; Met enkephalin; Neutrophil; Signalling

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; BETA ENDORPHIN; CD63 ANTIGEN; CHEMOKINE RECEPTOR CXCR1; CHEMOKINE RECEPTOR CXCR2; CYTOCHALASIN; FREUND ADJUVANT; METENKEPHALIN; MITOGEN ACTIVATED PROTEIN KINASE P38; MYELOPEROXIDASE; OPIATE PEPTIDE;

ANALYSIS OF VARIANCE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; NEUTROPHIL; PRIORITY JOURNAL;

ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD; BETA-ENDORPHIN; CYTOPLASMIC GRANULES; ENKEPHALIN, METHIONINE; EXOCYTOSIS; HUMANS; LIGANDS; MALE; NEUTROPHILS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PEROXIDASE; PLATELET MEMBRANE GLYCOPROTEINS; PROTEIN TRANSPORT; RATS; RATS, WISTAR; RECEPTORS, INTERLEUKIN-8A; RECEPTORS, INTERLEUKIN-8B; REFERENCE VALUES; SIGNAL TRANSDUCTION; STATISTICS, NONPARAMETRIC;

EID: 34748848626     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2007.05.002     Document Type: Article

References (66)

1. Abdel-Latif D., Steward M., Macdonald D.L., Francis G.A., Dinauer M.C., and Lacy P. Rac2 is critical for neutrophil primary granule exocytosis. Blood 104 (2004) 832-839
2. Antonijevic I., Mousa S.A., Schäfer M., and Stein C. Perineurial defect and peripheral opioid analgesia in inflammation. J. Neurosci. 15 (1995) 165-172
3. Bach J.P., Borta H., Ackermann W., Faust F., Borchers O., and Schrader M. The secretory granule protein syncollin localizes to HL-60 cells and neutrophils. J. Histochem. Cytochem. 54 (2006) 877-888
4. Bentwood B.J., and Henson P.M. The sequential release of granule constituents from human neutrophils. J. Immunol. 124 (1980) 855-862
5. Borregaard N. The human neutrophil. Function and dysfunction. Eur. J. Haematol. 41 (1988) 401-413
6. Borregaard N., and Cowland J.B. Granules of the human neutrophilic polymorphonuclear leukocyte. Blood 89 (1997) 3503-3521
7. Borregaard N., Lollike K., Kjeldsen L., Sengelov H., Bastholm L., Nielsen M.H., and Bainton D.F. Human neutrophil granules and secretory vesicles. Eur. J. Haematol. 51 (1993) 187-198
8. Brack A., Labuz D., Schlitz A., Rittner H.L., Machelska H., Schäfer M., Rezka R., and Stein C. Tissue monocytes/macrophages in inflammation: hyperalgesia versus opioid-mediated peripheral antinociception. Anesthesiology 101 (2004) 204-211
9. Brack A., Rittner H.L., Machelska H., Leder K., Mousa S.A., Schäfer M., and Stein C. Control of inflammatory pain by chemokine-mediated recruitment of opioid-containing polymorphonuclear cells. Pain 112 (2004) 229-238
10. Brack A., Rittner H.L., Machelska H., Shaqura M., Mousa S.A., Labuz D., Zöllner C., Schäfer M., and Stein C. Endogenous peripheral antinociception in early inflammation is not limited by the number of opioid-containing leukocytes but by opioid receptor expression. Pain 108 (2004) 67-75
11. Cabot P.J., Carter L., Gaiddon C., Zhang Q., Schäfer M., Loeffler J.P., and Stein C. Immune cell-derived beta-endorphin. Production, release, and control of inflammatory pain in rats. J. Clin. Invest. 100 (1997) 142-148
12. Cabot P.J., Carter L., Schäfer M., and Stein C. Methionine-enkephalin and Dynorphin A-release from immune cells and control of inflammatory pain. Pain 93 (2001) 207-212
13. Chakrabarti S., and Patel K.D. Regulation of matrix metalloproteinase-9 release from IL-8-stimulated human neutrophils. J. Leukoc. Biol. 78 (2005) 279-288
14. Cieutat A.M., Lobel P., August J.T., Kjeldsen L., Sengelov H., Borregaard N., and Bainton D.F. Azurophilic granules of human neutrophilic leukocytes are deficient in lysosome-associated membrane proteins but retain the mannose 6-phosphate recognition marker. Blood 91 (1998) 1044-1058
15. Daniels R.H., Elmore M.A., Hill M.E., Shimizu Y., Lackie J.M., and Finnen M.J. Priming of the oxidative burst in human neutrophils by physiological agonists or cytochalasin B results from the recruitment of previously non-responsive cells. Immunology 82 (1994) 465-472
16. Faurschou M., and Borregaard N. Neutrophil granules and secretory vesicles in inflammation. Microbes Infect. 5 (2003) 1317-1327
17. Fryer R.M., Hsu A.K., and Gross G.J. ERK and p38 MAP kinase activation are components of opioid-induced delayed cardioprotection. Basic Res. Cardiol. 96 (2001) 136-142
18. Fuhler G.M., Knol G.J., Drayer A.L., and Vellenga E. Impaired interleukin-8- and GROalpha-induced phosphorylation of extracellular signal-regulated kinase result in decreased migration of neutrophils from patients with myelodysplasia. J. Leukoc. Biol. 77 (2005) 257-266
19. Ganju P., Davis A., Patel S., Nunez X., and Fox A. p38 stress-activated protein kinase inhibitor reverses bradykinin B(1) receptor-mediated component of inflammatory hyperalgesia. Eur. J. Pharmacol. 421 (2001) 191-199
20. Gullberg U., Andersson E., Garwicz D., Lindmark A., and Olsson I. Biosynthesis, processing and sorting of neutrophil proteins: insight into neutrophil granule development. Eur. J. Haematol. 58 (1997) 137-153
21. Itou T., Collins L.V., Thoren F.B., Dahlgren C., and Karlsson A. Changes in activation states of murine polymorphonuclear leukocytes (PMN) during inflammation: a comparison of bone marrow and peritoneal exudate PMN. Clin. Vaccine Immunol. 13 (2006) 575-583
22. Iwase M., Takaoka S., Uchida M., Kondo G., Watanabe H., Ohashi M., and Nagumo M. Accelerative effect of a selective cyclooxygenase-2 inhibitor on Fas-mediated apoptosis in human neutrophils. Int. Immunopharmacol. 6 (2006) 334-341
23. Ji R.R. Peripheral and central mechanisms of inflammatory pain, with emphasis on MAP kinases. Curr. Drug Targets Inflamm. Allergy 3 (2004) 299-303
24. Ji R.R., Kawasaki Y., Zhuang Z.Y., Wen Y.R., and Zhang Y.Q. Protein kinases as potential targets for the treatment of pathological pain. Handb. Exp. Pharmacol. (2007) 359-389
25. Ji R.R., Samad T.A., Jin S.X., Schmoll R., and Woolf C.J. p38 Mapk activation by Ngf in primary sensory neurons after inflammation increases Trpv1 levels and maintains heat hyperalgesia. Neuron 36 (2002) 57-68
26. Jog N.R., Rane M.J., Lominadze G., Luerman G.C., Ward R.A., and McLeish K.R. The actin cytoskeleton regulates exocytosis of all neutrophil granule subsets. Am. J. Physiol. Cell Physiol. (2007)
27. Kasper B., Brandt E., Bulfone-Paus S., and Petersen F. Platelet factor 4 (PF-4)-induced neutrophil adhesion is controlled by src-kinases, whereas PF-4-mediated exocytosis requires the additional activation of p38 MAP kinase and phosphatidylinositol 3-kinase. Blood 103 (2004) 1602-1610
28. Kimura T., Iwase M., Kondo G., Watanabe H., Ohashi M., Ito D., and Nagumo M. Suppressive effect of selective cyclooxygenase-2 inhibitor on cytokine release in human neutrophils. Int. Immunopharmacol. 3 (2003) 1519-1528
29. Machelska H., Mousa S.A., Brack A., Schopohl J.K., Rittner H.L., Schäfer M., and Stein C. Opioid control of inflammatory pain regulated by intercellular adhesion molecule-1. J. Neurosci. 22 (2002) 5588-5596
30. Machelska H., Schopohl J.K., Mousa S.A., Labuz D., Schäfer M., and Stein C. Different mechanisms of intrinsic pain inhibition in early and late inflammation. J. Neuroimmunol. 141 (2003) 30-39
31. Maloney C.G., Kutchera W.A., Albertine K.H., McIntyre T.M., Prescott S.M., and Zimmerman G.A. Inflammatory agonists induce cyclooxygenase type 2 expression by human neutrophils. J. Immunol. 160 (1998) 1402-1410
32. Martin-Martin B., Nabokina S.M., Blasi J., Lazo P.A., and Mollinedo F. Involvement of SNAP-23 and syntaxin 6 in human neutrophil exocytosis. Blood 96 (2000) 2574-2583
33. Mocsai A., Jakus Z., Vantus T., Berton G., Lowell C.A., and Ligeti E. Kinase pathways in chemoattractant-induced degranulation of neutrophils: the role of p38 mitogen-activated protein kinase activated by Src family kinases. J. Immunol. 164 (2000) 4321-4331
34. Mollinedo F., Calafat J., Janssen H., Martin-Martin B., Canchado J., Nabokina S.M., and Gajate C. Combinatorial SNARE complexes modulate the secretion of cytoplasmic granules in human neutrophils. J. Immunol. 177 (2006) 2831-2841
35. Mollinedo F., Martin-Martin B., Calafat J., Nabokina S.M., and Lazo P.A. Role of vesicle-associated membrane protein-2, through Q-soluble N-ethylmaleimide-sensitive factor attachment protein receptor/R-soluble N-ethylmaleimide-sensitive factor attachment protein receptor interaction, in the exocytosis of specific and tertiary granules of human neutrophils. J. Immunol. 170 (2003) 1034-1042
36. Mollinedo F., Nakajima M., Llorens A., Barbosa E., Callejo S., Gajate C., and Fabra A. Major co-localization of the extracellular-matrix degradative enzymes heparanase and gelatinase in tertiary granules of human neutrophils. Biochem. J. 327 (1997) 917-923
37. Mollinedo F., Pulido R., Lacal P.M., and Sanchez-Madrid F. Mobilization of gelatinase-rich granules as a regulatory mechanism of early functional responses in human neutrophils. Scand. J. Immunol. 34 (1991) 33-43
38. Motta E.M., Calixto J.B., and Rae G.A. Mechanical hyperalgesia induced by endothelin-1 in rats is mediated via phospholipase C, protein kinase C, and MAP kinases. Exp. Biol. Med. 231 (2006) 1141-1145
39. Mousa S.A., Bopaiah C.P., Stein C., and Schäfer M. Involvement of corticotropin-releasing hormone receptor subtypes 1 and 2 in peripheral opioid-mediated inhibition of inflammatory pain. Pain 106 (2003) 297-307
40. Mousa S.A., Machelska H., Schäfer M., and Stein C. Immunohistochemical localization of endomorphin-1 and endomorphin-2 in immune cells and spinal cord in a model of inflammatory pain. J. Neuroimmunol. 126 (2002) 5-15
41. Mousa S.A., Shakibaei M., Sitte N., Schäfer M., and Stein C. Subcellular pathways of beta-endorphin synthesis, processing, and release from immunocytes in inflammatory pain. Endocrinology 145 (2004) 1331-1341
42. 2+ induced exocytosis in individual human neutrophils: high- and low-affinity granule populations and submaximal responses. EMBO J. 17 (1998) 1279-1288
43. Ozaki S., Narita M., Narita M., Ozaki M., Khotib J., and Suzuki T. Role of extracellular signal-regulated kinase in the ventral tegmental area in the suppression of the morphine-induced rewarding effect in mice with sciatic nerve ligation. J. Neurochem. 88 (2004) 1389-1397
44. Przewlocki R., Hassan A.H., Lason W., Epplen C., Herz A., and Stein C. Gene expression and localization of opioid peptides in immune cells of inflamed tissue: functional role in antinociception. Neuroscience 48 (1992) 491-500
45. Rittner H.L., Brack A., Machelska H., Mousa S.A., Bauer M., Schäfer M., and Stein C. Opioid peptide expressing leukocytes-Identification, recruitment and simultaneously increasing inhibition of inflammatory pain. Anesthesiology 95 (2001) 500-508
46. 2+-regulated release of opioid peptides from polymorphonuclear cells. FASEB J. 20 (2006) 2627-2629
47. Rittner H.L., Mousa S.A., Labuz D., Beschmann K., Schäfer M., Stein C., and Brack A. Selective local PMN recruitment by CXCL1 or CXCL2/3 injection does not cause inflammatory pain. J. Leukoc. Biol. 79 (2006) 1022-1032
48. Schäfer M., Carter L., and Stein C. Interleukin 1 beta and corticotropin-releasing factor inhibit pain by releasing opioids from immune cells in inflamed tissue. Proc. Natl. Acad. Sci. USA 91 (1994) 4219-4223
49. Schroder A.K., von der Ohe M., Kolling U., Altstaedt J., Uciechowski P., Fleischer D., Dalhoff K., Ju X., Zenke M., Heussen N., and Rink L. Polymorphonuclear leucocytes selectively produce anti-inflammatory interleukin-1 receptor antagonist and chemokines, but fail to produce pro-inflammatory mediators. Immunology 119 (2006) 317-327
50. Sengelov H., Kjeldsen L., and Borregaard N. Control of exocytosis in early neutrophil activation. J. Immunol. 150 (1993) 1535-1543
51. Sharp B., and Linner K. What do we know about the expression of proopiomelanocortin transcripts and related peptides in lymphoid tissue?. Endocrinology 133 (1993) 1921A-1921B [editorial; comment]
52. Sibinga N.E., and Goldstein A. Opioid peptides and opioid receptors in cells of the immune system. Annu. Rev. Immunol. 6 (1988) 219-249
53. Sitte N., Busch M., Mousa S.A., Labuz D., Rittner H., Gore C., Krause H., Stein C., and Schäfer M. Lymphocytes upregulate signal sequence-encoding proopiomelanocortin mRNA and beta-endorphin during painful inflammation in vivo. J. Neuroimmunol. 183 (2007) 133-145
54. Stein C., Hassan A.H., Przewlocki R., Gramsch C., Peter K., and Herz A. Opioids from immunocytes interact with receptors on sensory nerves to inhibit nociception in inflammation. Proc. Natl. Acad. Sci. USA 87 (1990) 5935-5939
55. Stein C., Millan M.J., and Herz A. Unilateral inflammation of the hindpaw in rats as a model of prolonged noxious stimulation: alterations in behavior and nociceptive thresholds. Pharmacol. Biochem. Behav. 31 (1988) 451-455
56. Stein C., Schäfer M., and Machelska H. Attacking pain at its source: new perspectives on opioids. Nat. Med. 9 (2003) 1003-1008
57. 2+ regulated exocytosis and SNARE function. Trends Endocrinol. Metab. 16 (2005) 81-83
58. Takafuji S., Ishida A., Miyakuni Y., and Nakagawa T. Matrix metalloproteinase-9 release from human leukocytes. J. Investig. Allergol. Clin. Immunol. 13 (2003) 50-55
59. Takami M., Terry V., and Petruzzelli L. Signaling pathways involved in IL-8-dependent activation of adhesion through Mac-1. J. Immunol. 168 (2002) 4559-4566
60. Takashi S., Park J., Fang S., Koyama S., Parikh I., and Adler K.B. A peptide against the N-terminus of myristoylated alanine-rich C kinase substrate inhibits degranulation of human leukocytes in vitro. Am. J. Respir. Cell Mol. Biol. 34 (2006) 647-652
61. Tuluc F., Garcia A., Bredetean O., Meshki J., and Kunapuli S.P. Primary granule release from human neutrophils is potentiated by soluble fibrinogen through a mechanism depending on multiple intracellular signaling pathways. Am. J. Physiol. Cell Physiol. 287 (2004) C1264-C1272
62. Vindrola O., Padros M.R., Sterin-Prync A., Ase A., Finkielman S., and Nahmod V. Proenkephalin system in human polymorphonuclear cells. Production and release of a novel 1.0-kDa peptide derived from synenkephalin. J. Clin. Invest. 86 (1990) 531-537
63. Walling E.A., Krafft G.A., and Ware B.R. Actin assembly activity of cytochalasins and cytochalasin analogs assayed using fluorescence photobleaching recovery. Arch. Biochem. Biophys. 264 (1988) 321-332
64. Ward R.A., Nakamura M., and McLeish K.R. Priming of the neutrophil respiratory burst involves p38 mitogen-activated protein kinase-dependent exocytosis of flavocytochrome b558-containing granules. J. Biol. Chem. 275 (2000) 36713-36719
65. Zhang Z., Xin S.M., Wu G.X., Zhang W.B., Ma L., and Pei G. Endogenous delta-opioid and ORL1 receptors couple to phosphorylation and activation of p38 MAPK in NG108-15 cells and this is regulated by protein kinase A and protein kinase C. J. Neurochem. 73 (1999) 1502-1509
66. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16 (1983) 109-110