Minocycline reduces engraftment and activation of bone marrow-derived cells but sustains their phagocytic activity in a mouse model of alzheimer's disease

GLIA

Volumn 56, Issue 16, 2008, Pages 1767-1779

  Malm, Tarja M ^a   Magga, Johanna ^a   Kuh, Georges Ful ^a   Vatanen, Tero ^c   Koistinaho, Milla ^a,b   Koistinaho, Jari ^a,c  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b Medeia Therapeutics Ltd   (Finland)

^c KUOPIO UNIVERSITY HOSPITAL   (Finland)

Author keywords

amyloid; Alzheimer's disease; Bone marrow; Inflammation; Microglia; Transplantation

Indexed keywords

AMYLOID BETA PROTEIN; ANTIINFECTIVE AGENT; AUTACOID; BIOLOGICAL MARKER; MINOCYCLINE;

ALZHEIMER DISEASE; ANIMAL; ARTICLE; BONE MARROW TRANSPLANTATION; C57BL MOUSE; CYTOLOGY; DISEASE MODEL; DRUG EFFECT; ENCEPHALITIS; FEMALE; GRAFT SURVIVAL; HUMAN; METABOLISM; METHODOLOGY; MICROGLIA; MONOCYTE; MOUSE; PATHOPHYSIOLOGY; PHAGOCYTOSIS; PHYSIOLOGY; TRANSGENIC MOUSE; TRANSPLANTATION;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; ANTI-BACTERIAL AGENTS; BIOLOGICAL MARKERS; BONE MARROW TRANSPLANTATION; DISEASE MODELS, ANIMAL; ENCEPHALITIS; FEMALE; GRAFT SURVIVAL; HUMANS; INFLAMMATION MEDIATORS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; MINOCYCLINE; MONOCYTES; PHAGOCYTOSIS;

EID: 62149143767     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20726     Document Type: Article

References (60)

1. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, Fiebich BL, Finch CE, Frautschy S, Griffin WS, Hampel H, Hull M, Landreth G, Lue L, Mrak R, Mackenzie IR, McGeer PL, O'Banion MK, Pachter J, Pasinetti G, Plata-Salaman C, Rogers J, Rydel R, Shen Y, Streit W, Strohmeyer R, Tooyoma I, Van Muiswinkel FL, Veerhuis R, Walker D, Webster S, Wegrzyniak B, Wenk G, Wyss-Coray T. 2000. Inflammation and Alzheimer's disease. Neurobiol Aging 21:383-421.
2. Bard F, Cannon C, Barbour R, Burke RL, Games D, Grajeda H, Guido T, Hu K, Huang J, Johnson-Wood K, Khan K, Kholodenko D, Lee M, Lieberburg I, Motter R, Nguyen M, Soriano F, Vasquez N, Weiss K, Welch B, Seubert P, Schenk D, Yednock T. 2000. Peripherally administered antibodies against amyloid beta-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat Med 6:916-919.
3. Bettany JT, Wolowacz RG. 1998. Tetracycline derivatives induce apoptosis selectively in cultured monocytes and macrophages but not in mesenchymal cells. Adv Dent Res 12:136-143.
4. Blais V, Turrin NP, Rivest S. 2005. Cyclooxygenase 2 (COX-2) inhibition increases the inflammatory response in the brain during systemic immune stimuli. J Neurochem 95:1563-1574.
5. Borchelt DR, Ratovitski T, van Lare J, Lee MK, Gonzales V, Jenkins NA, Copeland NG, Price DL, Sisodia SS. 1997. Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron 19:939-945.
6. Brundula V, Rewcastle NB, Metz LM, Bernard CC, Yong VW. 2002. Targeting leukocyte MMPs and transmigration: Minocycline as a potential therapy for multiple sclerosis. Brain 125(PART 6):1297- 1308.
7. Chen M, Ona VO, Li M, Ferrante RJ, Fink KB, Zhu S, Bian J, Guo L, Farrell LA, Hersch SM, Hobbs W, Vonsattel JP, Cha JH, Friedlander RM. 2000. Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease. Nat Med 6:797-801.
8. Cuadros MA, Navascues J. 1998. The origin and differentiation of microglial cells during development. Prog Neurobiol 56:173-189.
9. da Silva RP, Gordon S. 1999. Phagocytosis stimulates alternative glycosylation of macrosialin (mouse CD68), a macrophage-specific endosomal protein. Biochem J 338(PART 3):687-694.
10. DiCarlo G, Wilcock D, Henderson D, Gordon M, Morgan D. 2001. Intrahippocampal LPS injections reduce Abeta load in APP1PS1 transgenic mice. Neurobiol Aging 22:1007-1012.
11. Du Y, Ma Z, Lin S, Dodel RC, Gao F, Bales KR, Triarhou LC, Chernet E, Perry KW, Nelson DL, Luecke S, Phebus LA, Bymaster FP, Paul SM. 2001. Minocycline prevents nigrostriatal dopaminergic neurodegeneration in the MPTP model of Parkinson's disease. Proc Natl Acad Sci USA 98:14669-14674.
12. Eglitis MA, Mezey E. 1997. Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc Natl Acad Sci USA 94:4080-4085.
13. Familian A, Boshuizen RS, Eikelenboom P, Veerhuis R. 2006. Inhibitory effect of minocycline on amyloid beta fibril formation and human microglial activation. Glia 53:233-240.
14. Familian A, Eikelenboom P, Veerhuis R. 2007. Minocycline does not affect amyloid beta phagocytosis by human microglial cells. Neurosci Lett 416:87-91.
15. Fan LW, Pang Y, Lin S, Rhodes PG, Cai Z. 2005a. Minocycline attenuates lipopolysaccharide-induced white matter injury in the neonatal rat brain. Neuroscience 133:159-168.
16. Fan LW, Pang Y, Lin S, Tien LT, Ma T, Rhodes PG, Cai Z. 2005b. Minocycline reduces lipopolysaccharide-induced neurological dysfunction and brain injury in the neonatal rat. J Neurosci Res 82:71-82.
17. Fan R, Xu F, Previti ML, Davis J, Grande AM, Robinson JK, Van Nostrand WE. 2007. Minocycline reduces microglial activation and improves behavioral deficits in a transgenic model of cerebral microvascular amyloid. J Neurosci 27:3057-3063.
18. Fendrick SE, Miller KR, Streit WJ. 2005. Minocycline does not inhibit microglia proliferation or neuronal regeneration in the facial nucleus following crush injury. Neurosci Lett 385:220-223.
19. Frautschy SA, Hu W, Kim P, Miller SA, Chu T, Harris-White ME, Cole GM. 2001. Phenolic anti-inflammatory antioxidant reversal of Abetainduced cognitive deficits and neuropathology. Neurobiol Aging 22:993-1005.
20. Giuliani F, Hader W, Yong VW. 2005. Minocycline attenuates T cell and microglia activity to impair cytokine production in T cell-microglia interaction. J Leukoc Biol 78:135-143.
21. Henderson AS, Jorm AF, Christensen H, Jacomb PA, Korten AE. 1997. Aspirin, anti-inflammatory drugs and risk of dementia. Int J Geriatr Psychiatry 12:926-930.
22. Herber DL, Roth LM, Wilson D, Wilson N, Mason JE, Morgan D, Gordon MN. 2004. Time-dependent reduction in Abeta levels after intracranial LPS administration in APP transgenic mice. Exp Neurol 190:245-253.
23. Itagaki S, McGeer PL, Akiyama H. 1988. Presence of T-cytotoxic suppressor and leucocyte common antigen positive cells in Alzheimer's disease brain tissue. Neurosci Lett 91:259-264.
24. Kalaria RN. 2000. The role of cerebral ischemia in Alzheimer's disease. Neurobiol Aging 21:321-330.
25. Koenigsknecht-Talboo J, Landreth GE. 2005. Microglial phagocytosis induced by fibrillar beta-amyloid and IgGs are differentially regulated by proinflammatory cytokines. J Neurosci 25:8240-8249.
26. Koistinaho M, Lin S, Wu X, Esterman M, Koger D, Hanson J, Higgs R, Liu F, Malkani S, Bales KR, Paul SM. 2004. Apolipoprotein E promotes astrocyte colocalization and degradation of deposited amyloidbeta peptides. Nat Med 10:719-726.
27. Kreutzberg GW. 1996. Microglia: A sensor for pathological events in the CNS. Trends Neurosci 19:312-318.
28. Lai AY, Todd KG. 2006. Hypoxia-activated microglial mediators of neuronal survival are differentially regulated by tetracyclines. Glia 53:809-816.
29. Lee SM, Yune TY, Kim SJ, Kim YC, Oh YJ, Markelonis GJ, Oh TH. 2004. Minocycline inhibits apoptotic cell death via attenuation of TNF-alpha expression following iNOS/NO induction by lipopolysaccharide in neuron/glia co-cultures. J Neurochem 91:568-578.
30. Lim GP, Chu T, Yang F, Beech W, Frautschy SA, Cole GM. 2001. The curry spice curcumin reduces oxidative damage and amyloid pathology in an Alzheimer transgenic mouse. J Neurosci 21:8370-8377.
31. Malm TM, Koistinaho M, Parepalo M, Vatanen T, Ooka A, Karlsson S, Koistinaho J. 2005. Bone-marrow-derived cells contribute to the recruitment of microglial cells in response to beta-amyloid deposition in APP/PS1 double transgenic Alzheimer mice. Neurobiol Dis 18:134- 142.
32. McGeer PL, Schulzer M, McGeer EG. 1996. Arthritis and anti-inflammatory agents as possible protective factors for Alzheimer's disease: A review of 17 epidemiologic studies. Neurology 47:425-432.
33. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y. 1997. 'Green mice' as a source of ubiquitous green cells. FEBS Lett 407: 313-319.
34. Power C, Henry S, Del Bigio MR, Larsen PH, Corbett D, Imai Y, Yong VW, Peeling J. 2003. Intracerebral hemorrhage induces macrophage activation and matrix metalloproteinases. Ann Neurol 53: 731-742.
35. Priller J, Flugel A, Wehner T, Boentert M, Haas CA, Prinz M, Fernandez-Klett F, Prass K, Bechmann I, de Boer BA, Frotscher M, Kreutzberg GW, Persons DA, Dirnagl U. 2001. Targeting gene-modified hematopoietic cells to the central nervous system: Use of green fluorescent protein uncovers microglial engraftment. Nat Med 7:1356-1361.
36. Rabinowitz S, Gordon S. 1989. Differential expression of membrane sialoglycoproteins in exudate and resident mouse peritoneal macrophages. J Cell Sci 93 (PART 4):623-630.
37. Rabinowitz SS, Gordon S. 1991. Macrosialin, a macrophage-restricted membrane sialoprotein differentially glycosylated in response to inflammatory stimuli. J Exp Med 174:827-836.
38. Rogers J, Lue LF. 2001. Microglial chemotaxis, activation, and phagocytosis of amyloid beta-peptide as linked phenomena in Alzheimer's disease. Neurochem Int 39(5/6):333-340.
39. Ryu JK, McLarnon JG. 2006. Minocycline or iNOS inhibition block 3-nitrotyrosine increases and blood-brain barrier leakiness in amyloid beta-peptide-injected rat hippocampus. Exp Neurol 198:552-557.
40. Sanchez Mejia RO, Ona VO, Li M, Friedlander RM. 2001. Minocycline reduces traumatic brain injury-mediated caspase-1 activation, tissue damage, and neurological dysfunction. Neurosurgery 48:1393-1399; discussion 1399-1401.
41. Schenk D, Barbour R, Dunn W, Gordon G, Grajeda H, Guido T, Hu K, Huang J, Johnson-Wood K, Khan K, Kholodenko D, Lee M, Liao Z, Lieberburg I, Motter R, Mutter L, Soriano F, Shopp G, Vasquez N, Vandevert C, Walker S, Wogulis M, Yednock T, Games D, Seubert P. 1999. Immunization with amyloid-beta attenuates Alzheimer-diseaselike pathology in the PDAPP mouse. Nature 400:173-177.
42. Seabrook TJ, Jiang L, Maier M, Lemere CA. 2006. Minocycline affects microglia activation, Abeta deposition, and behavior in APP-tg mice. Glia 53:776-782.
43. Simard AR, Rivest S. 2004. Bone marrow stem cells have the ability to populate the entire central nervous system into fully differentiated parenchymal microglia. Faseb J 18:998-1000.
44. Simard AR, Soulet D, Gowing G, Julien JP, Rivest S. 2006. Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron 49:489-502.
45. Stalder AK, Ermini F, Bondolfi L, Krenger W, Burbach GJ, Deller T, Coomaraswamy J, Staufenbiel M, Landmann R, Jucker M. 2005. Invasion of hematopoietic cells into the brain of amyloid precursor protein transgenic mice. J Neurosci 25:11125-11132.
46. Stewart WF, Kawas C, Corrada M, Metter EJ. 1997. Risk of Alzheimer's disease and duration of NSAID use. Neurology 48:626-632.
47. Tikka T, Fiebich BL, Goldsteins G, Keinanen R, Koistinaho J. 2001. Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 21:2580-2588.
48. Tikka TM, Koistinaho JE. 2001. Minocycline provides neuroprotection against N-methyl-D-aspartate neurotoxicity by inhibiting microglia. J Immunol 166:7527-7533.
49. Tikka TM, Vartiainen NE, Goldsteins G, Oja SS, Andersen PM, Marklund SL, Koistinaho J. 2002. Minocycline prevents neurotoxicity induced by cerebrospinal fluid from patients with motor neurone disease. Brain 125(PART 4):722-731.
50. Togo T, Akiyama H, Iseki E, Kondo H, Ikeda K, Kato M, Oda T, Tsuchiya K, Kosaka K. 2002. Occurrence of T cells in the brain of Alzheimer's disease and other neurological diseases. J Neuroimmunol 124(1/2):83-92.
51. Wang AL, Yu AC, Lau LT, Lee C, Wu le M, Zhu X, Tso MO. 2005. Minocycline inhibits LPS-induced retinal microglia activation. Neurochem Int 47(1/2):152-158.
52. Wilcock DM, DiCarlo G, Henderson D, Jackson J, Clarke K, Ugen KE, Gordon MN, Morgan D. 2003. Intracranially administered anti-Abeta antibodies reduce beta-amyloid deposition by mechanisms both independent of and associated with microglial activation. J Neurosci 23:3745-3751.
53. Wilcock DM, Munireddy SK, Rosenthal A, Ugen KE, Gordon MN, Morgan D. 2004. Microglial activation facilitates Abeta plaque removal following intracranial anti-Abeta antibody administration. Neurobiol Dis 15:11-20.
54. Wyss-Coray T, Lin C, Yan F, Yu GQ, Rohde M, McConlogue L, Masliah E, Mucke L. 2001. TGF-beta1 promotes microglial amyloid-beta clearance and reduces plaque burden in transgenic mice. Nat Med 7:612- 618.
55. Wyss-Coray T, Loike JD, Brionne TC, Lu E, Anankov R, Yan F, Silverstein SC, Husemann J. 2003. Adult mouse astrocytes degrade amyloid-beta in vitro and in situ. Nat Med 9:453-457.
56. Wyss-Coray T, Yan F, Lin AH, Lambris JD, Alexander JJ, Quigg RJ, Masliah E. 2002. Prominent neurodegeneration and increased plaque formation in complement-inhibited Alzheimer's mice. Proc Natl Acad Sci USA 99:10837-10842.
57. Yrjanheikki J, Keinanen R, Pellikka M, Hokfelt T, Koistinaho J. 1998. Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci USA 95:15769- 15774.
58. Yrjanheikki J, Tikka T, Keinanen R, Goldsteins G, Chan PH, Koistinaho J. 1999. A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc Natl Acad Sci USA 96:13496-13500.
59. Zhang SC, Goetz BD, Duncan ID. 2003. Suppression of activated microglia promotes survival and function of transplanted oligodendroglial progenitors. Glia 41:191-198.
60. Zhu S, Stavrovskaya IG, Drozda M, Kim BY, Ona V, Li M, Sarang S, Liu AS, Hartley DM, Wu DC, Gullans S, Ferrante RJ, Przedborski S, Kristal BS, Friedlander RM. 2002. Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 417:74-78.