Clodronate inhibits the secretion of proinflammatory cytokines and NO by isolated microglial cells and reduces the number of proliferating glial cells in excitotoxically injured organotypic hippocampal slice cultures

Experimental Neurology

Volumn 189, Issue 2, 2004, Pages 241-251

  Dehghani, Faramarz ^a   Conrad, Ariane ^a,b   Kohl, Angelika ^a,b   Korf, Horst Werner ^a   Hailer, Nils P ^c  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Clodronate; Microglial cell; Neuron

Indexed keywords

BROXURIDINE; CLODRONIC ACID; COLONY STIMULATING FACTOR 1; CYTOKINE; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; LECTIN; LIPOPOLYSACCHARIDE; N METHYL DEXTRO ASPARTIC ACID; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN INJURY; BRAIN SLICE; CELL ACTIVATION; CELL INTERACTION; CELL ISOLATION; CELL LABELING; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; DRUG EFFECT; GRIFFONIA; HIPPOCAMPUS; MICROGLIA; MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; RAT; STATISTICAL SIGNIFICANCE; TISSUE CULTURE;

ANIMALS; ANIMALS, NEWBORN; ANTIMETABOLITES; ASTROCYTES; CELL COUNT; CELL DIVISION; CLODRONIC ACID; CYTOKINES; DOWN-REGULATION; GLIOSIS; HIPPOCAMPUS; INFLAMMATION MEDIATORS; INTERLEUKIN-1; MICROGLIA; N-METHYLASPARTATE; NEUROTOXINS; NITRIC OXIDE; RATS; RATS, WISTAR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 4544382302     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.expneurol.2004.06.010     Document Type: Article

References (49)

1. Bal-Price A., Brown G.C. Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity. J. Neurosci. 21:2001;6480-6491
2. Bartholdi D., Schwab M.E. Expression of pro-inflammatory cytokine and chemokine mRNA upon experimental spinal cord injury in mouse: an in situ hybridization study. Eur. J. Neurosci. 9:1997;1422-1438
3. Benford H.L., McGowan N.W., Helfrich M.H., Nuttall M.E., Rogers M.J. Visualization of bisphosphonate-induced caspase-3 activity in apoptotic osteoclasts in vitro. Bone. 28:2001;465-473
4. Bethea J.R., Nagashima H., Acosta M.C., Briceno C., Gomez F., Marcillo A.E., Loor K., Green J., Dietrich W.D. Systemically administered interleukin-10 reduces tumor necrosis factor-alpha production and significantly improves functional recovery following traumatic spinal cord injury in rats. J. Neurotrauma. 16:1999;851-863
5. Beyer M., Gimsa U., Eyupoglu I.Y., Hailer N.P., Nitsch R. Phagocytosis of neuronal or glial debris by microglial cells: upregulation of MHC class II expression and multinuclear giant cell formation in vitro. Glia. 31:2000;262-266
6. Chen C.C., Wang J.K. p38 but not p44/42 mitogen-activated protein kinase is required for nitric oxide synthase induction mediated by lipopolysaccharide in RAW 264.7 macrophages. Mol. Pharmacol. 55:1999;481-488
7. Dehghani F., Hischebeth G.T., Wirjatijasa F., Kohl A., Korf H.W., Hailer N.P. The immunosuppressant mycophenolate mofetil attenuates neuronal damage after excitotoxic injury in hippocampal slice cultures. Eur. J. Neurosci. 18:2003;1061-1072
8. Dusart I., Schwab M.E. Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur. J. Neurosci. 6:1994;712-724
9. Elkabes S., DiCicco-Bloom E.M., Black I.B. Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function. J. Neurosci. 16:1996;2508-2521
10. Fleisch H. Bisphosphonates: a new class of drugs in diseases of bone and calcium metabolism. Recent Results Cancer Res. 116:1989;1-28
11. Fleisch H. Bisphosphonates. Pharmacology and use in the treatment of tumour-induced hypercalcaemic and metastatic bone disease. Drugs. 42:1991;919-944
12. Frith J.C., Monkkonen J., Blackburn G.M., Russell R.G., Rogers M.J. Clodronate and liposome-encapsulated clodronate are metabolized to a toxic ATP analog, adenosine 5′-(beta, gamma-dichloromethylene) triphosphate, by mammalian cells in vitro. J. Bone Miner. Res. 12:1997;1358-1367
13. Frith J.C., Monkkonen J., Auriola S., Monkkonen H., Rogers M.J. The molecular mechanism of action of the antiresorptive and antiinflammatory drug clodronate: evidence for the formation in vivo of a metabolite that inhibits bone resorption and causes osteoclast and macrophage apoptosis. Arthritis Rheum. 44:2001;2201-2210
14. Galiano M., Liu Z.Q., Kalla R., Bohatschek M., Koppius A., Gschwendtner A., Xu S., Werner A., Kloss C.U., Jones L.L., Bluethmann H., Raivich G. Interleukin-6 (IL6) and cellular response to facial nerve injury: effects on lymphocyte recruitment, early microglial activation and axonal outgrowth in IL6-deficient mice. Eur. J. Neurosci. 14:2001;327-341
15. Ganter S., Northoff H., Mannel D., Gebicke-Harter P.J. Growth control of cultured microglia. J. Neurosci. Res. 33:1992;218-230
16. Giulian D., Baker T.J., Shih L.C., Lachman L.B. Interleukin 1 of the central nervous system is produced by ameboid microglia. J. Exp. Med. 164:1986;594-604
17. Guo H., Tong N., Turner T., Epstein L.G., McDermott M.P., Kilgannon P., Gelbard H.A. Release of the neuronal glycoprotein ICAM-5 in serum after hypoxic-ischemic injury. Ann. Neurol. 48:2000;590-602
18. Hailer N.P., Bechmann I., Heizmann S., Nitsch R. Adhesion molecule expression on phagocytic microglial cells following anterograde degeneration of perforant path axons. Hippocampus. 7:1997;341-349
19. Hailer N.P., Heppner F.L., Haas D., Nitsch R. Astrocytic factors deactivate antigen presenting cells that invade the central nervous system. Brain Pathol. 8:1998;459-474
20. Heppner F.L., Roth K., Nitsch R., Hailer N.P. Vitamin E induces ramification and down-regulation of adhesion molecules in cultured microglial cells. Glia. 22:1998;180-188
21. Hoffmann La Roche Ltd., 1998. Ostac product monograph. Mississauga, Ontario.
22. Hurst M., Noble S. Clodronate: a review of its use in breast cancer. Drugs Aging. 15:1999;143-167
23. Kloss C.U., Kreutzberg G.W., Raivich G. Proliferation of ramified microglia on an astrocyte monolayer: characterization of stimulatory and inhibitory cytokines. J. Neurosci. Res. 49:1997;248-254
24. Kohl A., Dehghani F., Korf H., Hailer N.P. The bisphosphonate clodronate depletes microglial cells in excitotoxically injured organotypic hippocampal slice cultures. Exp. Neurol. 181:2003;1-11
25. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19:1996;312-318
26. Lee S.C., Liu W., Roth P., Dickson D.W., Berman J.W., Brosnan C.F. Macrophage colony-stimulating factor in human fetal astrocytes and microglia. Differential regulation by cytokines and lipopolysaccharide, and modulation of class II MHC on microglia. J. Immunol. 150:1993;594-604
27. Lee S.C., Liu W., Brosnan C.F., Dickson D.W. GM-CSF promotes proliferation of human fetal and adult microglia in primary cultures. Glia. 12:1994;309-318
28. Liu W., Brosnan C.F., Dickson D.W., Lee S.C. Macrophage colony-stimulating factor mediates astrocyte-induced microglial ramification in human fetal central nervous system culture. Am. J. Pathol. 145:1994;48-53
29. Liu Y., Qin L., Li G., Zhang W., An L., Liu B., Hong J.S. Dextromethorphan protects dopaminergic neurons against inflammation-mediated degeneration through inhibition of microglial activation. J. Pharmacol. Exp. Ther. 305:2003;212-218
30. Makkonen N., Hirvonen M.R., Teravainen T., Savolainen K., Monkkonen J. Different effects of three bisphosphonates on nitric oxide production by RAW 264 macrophage-like cells in vitro. J. Pharmacol. Exp. Ther. 277:1996;1097-1102
31. Makkonen N., Salminen A., Rogers M.J., Frith J.C., Urtti A., Azhayeva E., Monkkonen J. Contrasting effects of alendronate and clodronate on RAW 264 macrophages: the role of a bisphosphonate metabolite. Eur. J. Pharm. Sci. 8:1999;109-118
32. Minghetti L., Levi G. Microglia as effector cells in brain damage and repair: focus on prostanoids and nitric oxide. Prog. Neurobiol. 54:1998;99-125
33. Murphy G.M. Jr., Yang L., Cordell B. Macrophage colony-stimulating factor augments beta-amyloid-induced interleukin-1, interleukin-6, and nitric oxide production by microglial cells. J. Biol. Chem. 273:1998;20967-20971
34. Nicholas R.S., Compston A., Brown D.R. Inhibition of tumour necrosis factor-alpha (TNFalpha)-induced NF-kappaB p52 converts the metabolic effects of microglial-derived TNFalpha on mouse cerebellar neurones to neurotoxicity. J. Neurochem. 76:2001;1431-1438
35. Oudega M., Vargas C.G., Weber A.B., Kleitman N., Bunge M.B. Long-term effects of methylprednisolone following transection of adult rat spinal cord. Eur. J. Neurosci. 11:1999;2453-2464
36. Polfliet M.M., Goede P.H., Kesteren-Hendrikx E.M., van Rooijen N., Dijkstra C.D., van den Berg T.K. A method for the selective depletion of perivascular and meningeal macrophages in the central nervous system. J. Neuroimmunol. 116:2001;188-195
37. Raivich G., Moreno-Flores M.T., Moller J.C., Kreutzberg G.W. Inhibition of posttraumatic microglial proliferation in a genetic model of macrophage colony-stimulating factor deficiency in the mouse. Eur. J. Neurosci. 6:1994;1615-1618
38. Raivich G., Haas S., Werner A., Klein M.A., Kloss C., Kreutzberg G.W. Regulation of MCSF receptors on microglia in the normal and injured mouse central nervous system: a quantitative immunofluorescence study using confocal laser microscopy. J. Comp. Neurol. 395:1998;342-358
39. Rogers M.J., Chilton K.M., Coxon F.P., Lawry J., Smith M.O., Suri S., Russell R.G. Bisphosphonates induce apoptosis in mouse macrophage-like cells in vitro by a nitric oxide-independent mechanism. J. Bone Miner. Res. 11:1996;1482-1491
40. Russell R.G., Rogers M.J. Bisphosphonates: from the laboratory to the clinic and back again. Bone. 25:1999;97-106
41. Saccani S., Pantano S., Natoli G. p38-Dependent marking of inflammatory genes for increased NF-kappa B recruitment. Nat. Immunol. 3:2002;69-75
42. Sauty A., Pecherstorfer M., Zimmer-Roth I., Fioroni P., Juillerat L., Markert M., Ludwig H., Leuenberger P., Burckhardt P., Thiebaud D. Interleukin-6 and tumor necrosis factor alpha levels after bisphosphonates treatment in vitro and in patients with malignancy. Bone. 18:1996;133-139
43. Schmitt A.B., Buss A., Breuer S., Brook G.A., Pech K., Martin D., Schoenen J., Noth J., Love S., Schroder J.M., Kreutzberg G.W., Nacimiento W. Major histocompatibility complex class II expression by activated microglia caudal to lesions of descending tracts in the human spinal cord is not associated with a T cell response. Acta Neuropathol. (Berl). 100:2000;528-536
44. Takeuchi A., Miyaishi O., Kiuchi K., Isobe K. Macrophage colony-stimulating factor is expressed in neuron and microglia after focal brain injury. J. Neurosci. Res. 65:2001;38-44
45. Thery C., Dobbertin A., Mallat M. Downregulation of in vitro neurotoxicity of brain macrophages by prostaglandin E2 and a beta-adrenergic agonist. Glia. 11:1994;383-386
46. van Rooijen N., Sanders A., van den Berg T.K. Apoptosis of macrophages induced by liposome-mediated intracellular delivery of clodronate and propamidine. J. Immunol. Methods. 193:1996;93-99
47. Vincent V.A.M., Tilders F.J.H., Van Dam A.-M. Inhibition of endotoxin-induced nitric oxide synthase production in microglial cells by the presence of astroglial cells: a role for transforming growth factor beta. Glia. 19:1997;190-198
48. Vincent V.A., Selwood S.P., Murphy G.M. Jr. Proinflammatory effects of M-CSF and A beta in hippocampal organotypic cultures. Neurobiol. Aging. 23:2002;349-362
49. Wilms H., Hartmann D., Sievers J. Ramification of microglia, monocytes and macrophages in vitro: influences of various epithelial and mesenchymal cells and their conditioned media. Cell Tissue Res. 287:1997;447-458