Mesenchymal stem cells shape microglia effector functions through the release of CX3CL1

Stem Cells

Volumn 30, Issue 9, 2012, Pages 2044-2053

  Giunti, Debora ^a   Parodi, Benedetta ^a   Usai, Cesare ^a   Vergani, Laura ^b   Casazza, Simona ^a   Bruzzone, Santina ^b   Mancardi, Gianluigi ^a,b   Uccelli, Antonio ^a,b,c  

^a CNR   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c Advanced Biotechnology Center ABC   (Italy)

Author keywords

Chemokines; Immunomodulation; Mesenchymal stem cells; Microglia; Neuroprotection

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSE; CALCIUM ION; CD200 RECEPTOR; CHEMOKINE RECEPTOR CX3CR1; FRACTALKINE; GAMMA INTERFERON; HEME OXYGENASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; MESSENGER RNA; METALLOTHIONEIN I; METALLOTHIONEIN II; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NITRATE; NITRITE; NUCLEAR RECEPTOR RELATED FACTOR 1; PROSTAGLANDIN E RECEPTOR 2; PROSTAGLANDIN E RECEPTOR 4; SOMATOMEDIN C; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL ACTIVATION; CELL PROLIFERATION; CELL SHAPE; CONTROLLED STUDY; CYTOKINE RELEASE; IN VITRO STUDY; INFLAMMATION; INNATE IMMUNITY; MESENCHYMAL STEM CELL; MICROGLIA; MOUSE; NEUROPROTECTION; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; CELL COMMUNICATION; CELL GROWTH PROCESSES; CHEMOKINE CX3CL1; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; MICROGLIA; PHAGOCYTOSIS;

EID: 84865312296     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1174     Document Type: Article

References (52)

1. Javazon EH, Beggs KJ, Flake AW. Mesenchymal stem cells: Paradoxes of passaging. Exp Hematol 2004;32:414-425.
2. Pittenger MF, Mackay AM, Beck SC et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-147.
3. Lee RH, Pulin AA, Seo MJ et al. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 2009;5:54-63.
4. Gerdoni E, Gallo B, Casazza S et al. Mesenchymal stem cells effectively modulate pathogenic immune response in experimental autoimmune encephalomyelitis. Ann Neurol 2007;61:219-227.
5. Phinney DG, Prockop DJ. Concise review: Mesenchymal stem/multipotent stromal cells: The state of transdifferentiation and modes of tissue repair - Current views. Stem Cells 2007;25:2896-2902.
6. Uccelli A, Pistoia V, Moretta L. Mesenchymal stem cells: A new strategy for immunosuppression? Trends Immunol 2007;28:219-226.
7. Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol 2008;8:726-736.
8. Zappia E, Casazza S, Pedemonte E et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T cell anergy. Blood 2005;106:1755-1761.
9. Zhang J, Li Y, Lu M et al. Bone marrow stromal cells reduce axonal loss in experimental autoimmune encephalomyelitis mice. J Neurosci Res 2006;84:587-595.
10. Kassis I, Grigoriadis N, Gowda-Kurkalli B et al. Neuroprotection and immunomodulation with mesenchymal stem cells in chronic experimental autoimmune encephalomyelitis. Arch Neurol 2008;65:753-761.
11. Crigler L, Robey RC, Asawachaicharn A et al. Human mesenchymal stem cell subpopulations express a variety of neuro-regulatory molecules and promote neuronal cell survival and neuritogenesis. Exp Neurol 2006;198:54-64.
12. Lanza C, Morando S, Voci A et al. Neuroprotective mesenchymal stem cells are endowed with a potent antioxidant effect in vivo. J Neurochem 2009;110:1674-1684.
13. Munoz JR, Stoutenger BR, Robinson AP et al. Human stem/progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. Proc Natl Acad Sci USA 2005;102:18171-18176.
14. Akiyama Y, Radtke C, Kocsis J. Remyelination of the rat spinal cord by transplantation of identified bone marrow stromal cells. J Neurosci 2002;22:6623-6630.
15. Rivera FJ, Couillard-Despres S, Pedre X et al. Mesenchymal stem cells instruct oligodendrogenic fate decision on adult neural stem cells. Stem Cells 2006;24:2209-2219.
16. Bai L, Lennon DP, Eaton V et al. Human bone marrow-derived mesenchymal stem cells induce Th2-polarized immune response and promote endogenous repair in animal models of multiple sclerosis. Glia 2009;57:1192-1203.
17. Li Y, Chen J, Chen XG et al. Human marrow stromal cell therapy for stroke in rat: Neurotrophins and functional recovery. Neurology 2002;59:514-523.
18. Nimmerjahn A, Kirchhoff F, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005;308:1314-1318.
19. Rivest S. Regulation of innate immune responses in the brain. Nat Rev Immunol 009;9:429-439.
20. Jack C, Ruffini F, Bar-Or A, Antel JP. Microglia and multiple sclerosis. J Neurosci Res 2005;81:363-373.
21. Ransohoff RM, Perry VH. Microglial physiology: Unique stimuli, specialized responses. Annu Rev Immunol 2009;27:119-145.
22. Saijo K, Glass CK. Microglial cell origin and phenotypes in health and disease. Nat Rev Immunol 2011;11:775-787.
23. Schwartz M, Butovsky O, Bruck W et al. Microglial phenotype: Is the commitment reversible? Trends Neurosci 2006;29:68-74.
24. Cardona AE, Pioro EP, Sasse ME et al. Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 2006;9:917-924.
25. Saijo K, Winner B, Carson CT et al. A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell 2009;137:47-59.
26. Righi M, Mori L, De Libero G et al. Monokine production by microglial cell clones. Eur J Immunol 1989;19:1443-1448.
27. Jarrossay D, Napolitani G, Colonna M et al. Specialization and complementarity in microbial molecule recognition by human myeloid and plasmacytoid dendritic cells. Eur J Immunol 2001;31:3388-3393.
28. Graeff R, Lee HC. A novel cycling assay for cellular cADP-ribose with nanomolar sensitivity. Biochem J 2002;361(pt 2):379-384.
29. Zocchi E, Daga A, Usai C et al. Expression of CD38 increases intracellular calcium concentration and reduces doubling time in HeLa and 3T3 cells. J Biol Chem 1998;273:8017-8024.
30. Takahashi K, Rochford CD, Neumann H. Clearance of apoptotic neurons without inflammation by microglial triggering receptor expressed on myeloid cells-2. J Exp Med 2005;201:647-657.
31. Jiang J, Ganesh T, Du Y et al. Neuroprotection by selective allosteric potentiators of the EP2 prostaglandin receptor. Proc Natl Acad Sci USA 2010;107:2307-2312.
32. Liu D, Wu L, Breyer R et al. Neuroprotection by the PGE2 EP2 receptor in permanent focal cerebral ischemia. Ann Neurol 2005;57:758-761.
33. Chan A, Magnus T, Gold R. Phagocytosis of apoptotic inflammatory cells by microglia and modulation by different cytokines: Mechanism for removal of apoptotic cells in the inflamed nervous system. Glia 2001;33:87-95.
34. Butchi NB, Du M, Peterson KE. Interactions between TLR7 and TLR9 agonists and receptors regulate innate immune responses by astrocytes and microglia. Glia 2010;58:650-664.
35. Franco L, Bodrato N, Moreschi I et al. Cyclic ADP-ribose is a second messenger in the lipopolysaccharide-stimulated activation of murine N9 microglial cell line. J Neurochem 2006;99:165-176.
36. Harrison JK, Jiang Y, Chen S et al. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc Natl Acad Sci USA 1998;95:10896-10901.
37. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A. Physiology of microglia. Physiol Rev 2011;91:461-553.
38. Jenmalm MC, Cherwinski H, Bowman EP et al. Regulation of myeloid cell function through the CD200 receptor. J Immunol 2006;176:191-199.
39. Fan J, Wojnar MM, Theodorakis M et al. Regulation of insulin-like growth factor (IGF)-I mRNA and peptide and IGF-binding proteins by interleukin-1. Am J Physiol 1996;270(3 pt 2):R621-629.
40. Mason JL, Suzuki K, Chaplin DD et al. Interleukin-1beta promotes repair of the CNS. J Neurosci 2001;21:7046-7052.
41. Krampera M, Cosmi L, Angeli R et al. Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells 2006;24:386-398.
42. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005;105:1815-1822.
43. Noda M, Doi Y, Liang J et al. Fractalkine attenuates excito-neurotoxicity via microglial clearance of damaged neurons and antioxidant enzyme heme oxygenase-1 expression. J Biol Chem 2011;286:2308-2319.
44. Hughes MM, Field RH, Perry VH et al. Microglia in the degenerating brain are capable of phagocytosis of beads and of apoptotic cells, but do not efficiently remove PrPSc, even upon LPS stimulation. Glia 2010;58:2017-2030.
45. Chiesa S, Morbelli S, Morando S et al. Mesenchymal stem cells impair in vivo T-cell priming by dendritic cells. Proc Natl Acad Sci USA 2011;108:17384-17389.
46. Kim J, Hematti P. Mesenchymal stem cell-educated macrophages: A novel type of alternatively activated macrophages. Exp Hematol 2009;37:1445-1453.
47. Shechter R, London A, Varol C et al. Infiltrating blood-derived macrophages are vital cells playing an anti-inflammatory role in recovery from spinal cord injury in mice. PLoS Med 2009;6:e1000113.
48. Zhou C, Zhang C, Chi S et al. Effects of human marrow stromal cells on activation of microglial cells and production of inflammatory factors induced by lipopolysaccharide. Brain Res 2009;1269:23-30.
49. Kim YJ, Park HJ, Lee G et al. Neuroprotective effects of human mesenchymal stem cells on dopaminergic neurons through anti-inflammatory action. Glia 2009;57:13-23.
50. Lee JK, Schuchman EH, Jin HK et al. Soluble CCL5 derived from bone marrow-derived mesenchymal stem cells and activated by amyloid-beta ameliorates Alzheimer's disease in mice by recruiting bone marrow-induced microglia immune responses. Stem Cells 2012;30:1544-1555.
51. Uccelli A, Mancardi G. Stem cell transplantation in multiple sclerosis. Curr Opin Neurol 2010;23:218-225.
52. Uccelli A, Laroni A, Freedman MS. Mesenchymal stem cells for the treatment of multiple sclerosis and other neurological diseases. Lancet Neurol 2011;10:649-656.