Chemical dampening of Ly6Chi monocytes in the periphery produces anti-depressant effects in mice

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Zheng, Xiao ^a,b   Ma, Sijing ^a,c   Kang, An ^d   Wu, Mengqiu ^a   Wang, Lin ^a   Wang, Qiong ^b   Wang, Guangji ^a   Hao, Haiping ^a  

^a CHINA PHARMACEUTICAL UNIVERSITY   (China)

^b NANJING UNIVERSITY   (China)

^c Hunan Research Academy of Environmental Science   (China)

^d NANJING UNIVERSITY OF CHINESE MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIDEPRESSANT AGENT; GINSENOSIDE; GINSENOSIDE RG 1; LY ANTIGEN; LY-6C ANTIGEN, MOUSE; MONOCYTE CHEMOTACTIC PROTEIN 1;

ANIMAL; ANIMAL BEHAVIOR; BRAIN; DEPRESSION; DRUG EFFECTS; INFLAMMATION; MALE; METABOLISM; MONOCYTE; MOUSE; PATHOLOGY; PHENOTYPE; PHYSIOLOGICAL STRESS; SECRETION (PROCESS); SIGNAL TRANSDUCTION;

ANIMALS; ANTIDEPRESSIVE AGENTS; ANTIGENS, LY; BEHAVIOR, ANIMAL; BRAIN; CHEMOKINE CCL2; DEPRESSION; GINSENOSIDES; INFLAMMATION; MALE; MICE; MONOCYTES; PHENOTYPE; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84955262021     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep19406     Document Type: Article

References (45)

1. Haroon, E., Raison, C. L. & Miller, A. H. Psychoneuroimmunology meets neuropsychopharmacology: translational implications of the impact of inflammation on behavior. Neuropsychopharmacology 37, 137-162 (2012).
2. Hsiao, E. Y., McBride, S. W., Chow, J., Mazmanian, S. K. & Patterson, P. H. Modeling an autism risk factor in mice leads to permanent immune dysregulation. Proc. Natl. Acad. Sci. USA 109, 12776-12781 (2012).
3. Kornhuber, J., Muller, C. P., Becker, K. A., Reichel, M. & Gulbins, E. The ceramide system as a novel antidepressant target. Trends Pharmacol. Sci. 35, 293-304 (2014).
4. Zheng, X., Zhang, X., Wang, G. & Hao, H. Treat the brain and treat the periphery: toward a holistic approach to major depressive disorder. Drug Discov. Today 20, 562-568 (2015).
5. Heidt, T. et al. Chronic variable stress activates hematopoietic stem cells. Nat. Med. 20, 754-758 (2014).
6. Alcocer-Gomez, E. et al. NLRP3 inflammasome is activated in mononuclear blood cells from patients with major depressive disorder. Brain Behav. Immun. 36, 111-117 (2014).
7. Hodes, G. E. et al. Individual differences in the peripheral immune system promote resilience versus susceptibility to social stress. Proc. Natl. Acad. Sci. USA 111, 16136-16141 (2014).
8. Agudelo, L. Z. et al. Skeletal Muscle PGC-1alpha1 Modulates Kynurenine Metabolism and Mediates Resilience to Stress-Induced Depression. Cell 159, 33-45 (2014).
9. McKim, D. B. et al. Sympathetic Release of Splenic Monocytes Promotes Recurring Anxiety Following Repeated Social Defeat. Biol. Psychiatry (2015) doi: 10.1016/j.biopsych.2015.07.010.
10. Town, T. et al. Blocking TGF-beta-Smad2/3 innate immune signaling mitigates Alzheimer-like pathology. Nat. Med. 14, 681-687 (2008).
11. Zwilling, D. et al. Kynurenine 3-monooxygenase inhibition in blood ameliorates neurodegeneration. Cell 145, 863-874 (2011).
12. King, I. L., Dickendesher, T. L. & Segal, B. M. Circulating Ly-6C+ myeloid precursors migrate to the CNS and play a pathogenic role during autoimmune demyelinating disease. Blood 113, 3190-3197 (2009).
13. Kleinschnitz, C. et al. Regulatory T cells are strong promoters of acute ischemic stroke in mice by inducing dysfunction of the cerebral microvasculature. Blood 121, 679-691 (2013).
14. Liesz, A. et al. Regulatory T cells are key cerebroprotective immunomodulators in acute experimental stroke. Nat. Med. 15, 192-199 (2009).
15. Shechter, R. et al. Recruitment of beneficial M2 macrophages to injured spinal cord is orchestrated by remote brain choroid plexus. Immunity 38, 555-569 (2013).
16. Hao, H., Zheng, X. & Wang, G. Insights into drug discovery from natural medicines using reverse pharmacokinetics. Trends Pharmacol. Sci. 35, 168-177 (2014).
17. Long, F., Yang, H., Xu, Y., Hao, H. & Li, P. A strategy for the identification of combinatorial bioactive compounds contributing to the holistic effect of herbal medicines. Sci. Rep. 5, 12361 (2015).
18. Kang, A. et al. Peripheral anti-inflammatory effects explain the ginsenosides paradox between poor brain distribution and antidepression efficacy. J. Neuroinflammation 8, 100 (2011).
19. Zheng, X. et al. Peripheral immunomodulation with ginsenoside Rg1 ameliorates neuroinflammation-induced behavioral deficits in rats. Neuroscience 256, 210-222 (2014).
20. Fu, X. et al. Central administration of lipopolysaccharide induces depressive-like behavior in vivo and activates brain indoleamine 2,3 dioxygenase in murine organotypic hippocampal slice cultures. J. Neuroinflammation 7, 43 (2010).
21. Pan, Y. et al. The effects of central pro-and anti-inflammatory immune challenges on depressive-like behavior induced by chronic forced swim stress in rats. Behav. Brain Res. 247, 232-240 (2013).
22. Wu, J. et al. Ginsenoside Rg1 protection against beta-amyloid peptide-induced neuronal apoptosis via estrogen receptor alpha and glucocorticoid receptor-dependent anti-protein nitration pathway. Neuropharmacology 63, 349-361 (2012).
23. Zong, Y. et al. Ginsenoside Rg1 attenuates lipopolysaccharide-induced inflammatory responses via the phospholipase C-gamma1 signaling pathway in murine BV-2 microglial cells. Curr. Med. Chem. 19, 770-779 (2012).
24. Hettinger, J. et al. Origin of monocytes and macrophages in a committed progenitor. Nat. Immunol. 14, 821-830 (2013).
25. Hucke, S. et al. Licensing of myeloid cells promotes central nervous system autoimmunity and is controlled by peroxisome proliferator-activated receptor gamma. Brain 135, 1586-1605 (2012).
26. Moreno, M. et al. Conditional ablation of astroglial CCL2 suppresses CNS accumulation of M1 macrophages and preserves axons in mice with MOG peptide EAE. J. Neurosci. 34, 8175-8185 (2014).
27. Giraud, S. N., Caron, C. M., Pham-Dinh, D., Kitabgi, P. & Nicot, A. B. Estradiol inhibits ongoing autoimmune neuroinflammation and NFkappaB-dependent CCL2 expression in reactive astrocytes. Proc. Natl. Acad. Sci. USA 107, 8416-8421 (2010).
28. Getts, D. R. et al. Ly6c+ "inflammatory monocytes" are microglial precursors recruited in a pathogenic manner in West Nile virus encephalitis. J. Exp. Med. 205, 2319-2337 (2008).
29. Mildner, A. et al. Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat. Neurosci. 10, 1544-1553 (2007).
30. Kim, H. S., Ullevig, S. L., Zamora, D., Lee, C. F. & Asmis, R. Redox regulation of MAPK phosphatase 1 controls monocyte migration and macrophage recruitment. Proc. Natl. Acad. Sci. USA 109, E2803-2812 (2012).
31. Butovsky, O. et al. Modulating inflammatory monocytes with a unique microRNA gene signature ameliorates murine ALS. J. Clin. Invest. 122, 3063-3087 (2012).
32. Weber, M. D., Frank, M. G., Sobesky, J. L., Watkins, L. R. & Maier, S. F. Blocking toll-like receptor 2 and 4 signaling during a stressor prevents stress-induced priming of neuroinflammatory responses to a subsequent immune challenge. Brain Behav. Immun. 32, 112-121 (2013).
33. Hafner, S. et al. Association between social isolation and inflammatory markers in depressed and non-depressed individuals: results from the MONICA/KORA study. Brain Behav. Immun. 25, 1701-1707 (2011).
34. Wohleb, E. S. et al. Knockdown of interleukin-1 receptor type-1 on endothelial cells attenuated stress-induced neuroinflammation and prevented anxiety-like behavior. J. Neurosci. 34, 2583-2591 (2014).
35. Choi, Y. J., Yoon, J. H., Cha, S. W. & Lee, S. G. Ginsenoside Rh1 inhibits the invasion and migration of THP-1 acute monocytic leukemia cells via inactivation of the MAPK signaling pathway. Fitoterapia 82, 911-919 (2011).
36. Ajami, B., Bennett, J. L., Krieger, C., McNagny, K. M. & Rossi, F. M. Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat. Neurosci. 14, 1142-1149 (2011).
37. Swirski, F. K. et al. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 325, 612-616 (2009).
38. Wohleb, E. S., Powell, N. D., Godbout, J. P. & Sheridan, J. F. Stress-induced recruitment of bone marrow-derived monocytes to the brain promotes anxiety-like behavior. J. Neurosci. 33, 13820-13833 (2013).
39. Brachman, R. A., Lehmann, M. L., Maric, D. & Herkenham, M. Lymphocytes from chronically stressed mice confer antidepressantlike effects to naive mice. J. Neurosci. 35, 1530-1538 (2015).
40. Cecchelli, R. et al. Modelling of the blood-brain barrier in drug discovery and development. Nat. Rev. Drug Discov. 6, 650-661 (2007).
41. Clapper, J. R. et al. Anandamide suppresses pain initiation through a peripheral endocannabinoid mechanism. Nat. Neurosci. 13, 1265-1270 (2010).
42. Tully, T., Bourtchouladze, R., Scott, R. & Tallman, J. Targeting the CREB pathway for memory enhancers. Nat. Rev. Drug Discov. 2, 267-277 (2003).
43. Aid, S. et al. Cyclooxygenase-1 and-2 differentially modulate lipopolysaccharide-induced blood-brain barrier disruption through matrix metalloproteinase activity. J. Cereb. Blood Flow Metab. 30, 370-380 (2010).
44. Choi, S. H., Langenbach, R. & Bosetti, F. Genetic deletion or pharmacological inhibition of cyclooxygenase-1 attenuate lipopolysaccharide-induced inflammatory response and brain injury. FASEB J. 22, 1491-1501 (2008).
45. Berton, O. et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311, 864-868 (2006