Enriching the housing environment for mice enhances their NK cell antitumor immunity via sympathetic nerve-dependent regulation of NKG2D and CCR5

Cancer Research

Volumn 77, Issue 7, 2017, Pages 1611-1622

  Song, Yanfang ^a   Gan, Yu ^a   Wang, Qing ^a   Meng, Zihong ^a   Li, Guohua ^a   Shen, Yuling ^a,b   Wu, Yufeng ^a   Li, Peiying ^b   Yao, Ming ^a   Gu, Jianren ^a   Tu, Hong ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; CHEMOKINE RECEPTOR CCR5; LACTATE DEHYDROGENASE; NATURAL KILLER CELL RECEPTOR NKG2D; PROPRANOLOL; VASCULOTROPIN A; CCR5 PROTEIN, MOUSE; KLRK1 PROTEIN, MOUSE; LEPTIN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K;

ADRENERGIC SYSTEM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CHEMOTAXIS; CONTROLLED STUDY; CYTOTOXICITY; EFFECTOR CELL; ENRICHMENT CULTURE; ENVIRONMENTAL EXPOSURE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LYMPHOCYTE FUNCTION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; SPLEEN CELL; SYMPATHECTOMY; SYMPATHETIC NERVE; T LYMPHOCYTE; TISSUE DISTRIBUTION; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; UPREGULATION; WESTERN BLOTTING; ANIMAL; ANIMAL HOUSING; C57BL MOUSE; ENVIRONMENT; IMMUNOLOGY; MALE; NEOPLASMS; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; ENVIRONMENT; HOUSING, ANIMAL; KILLER CELLS, NATURAL; LEPTIN; MALE; MICE; MICE, INBRED C57BL; NEOPLASMS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; RECEPTORS, CCR5; SYMPATHETIC NERVOUS SYSTEM;

EID: 85017383101     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-16-2143     Document Type: Article

References (48)

1. Cao L, Liu X, Lin EJ, Wang C, Choi EY, Riban V, et al. Environmental and genetic activation of a brain-adipocyte BDNF/leptin axis causes cancer remission and inhibition. Cell 2010;142:52-64.
2. Kempermann G, Kuhn HG, Gage FH. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997;386:493-5.
3. Birch AM, McGarry NB, Kelly AM. Short-term environmental enrichment, in the absence of exercise, improves memory, and increases NGF concentration, early neuronal survival, and synaptogenesis in the dentate gyrus in a time-dependent manner. Hippocampus 2013;23: 437-50.
4. Zhu H, Zhang J, Sun H, Zhang L, Liu H, Zeng X, et al. An enriched environment reverses the synaptic plasticity deficit induced by chronic cerebral hypoperfusion. Neurosci Lett 2011;502:71-5.
5. Novkovic T, Heumann R, Manahan-Vaughan D. Ras does not contribute to the facilitation of hippocampal synaptic plasticity enabled by environmental enrichment. Neuroscience 2015;309:214-23.
6. Artola A, von Frijtag JC, Fermont PC, Gispen WH, Schrama LH, Kamal A, et al. Long-lasting modulation of the induction of LTD and LTP in rat hippocampal CA1 by behavioural stress and environmental enrichment. Eur J Neurosci 2006;23:261-72.
7. Rampon C, Tang YP, Goodhouse J, Shimizu E, Kyin M, Tsien JZ. Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nat Neurosci 2000;3:238-44.
8. Sale A, Berardi N, Maffei L. Enrich the environment to empower the brain. Trends Neurosci 2009;32:233-9.
9. Benaroya-Milshtein N, Hollander N, Apter A, Kukulansky T, Raz N, Wilf A, et al. Environmental enrichment in mice decreases anxiety, attenuates stress responses and enhances natural killer cell activity. Eur J Neurosci 2004; 20:1341-7.
10. Baldini S, Restani L, Baroncelli L, Coltelli M, Franco R, Cenni MC, et al. Enriched early life experiences reduce adult anxiety-like behavior in rats: a role for insulin-like growth factor 1. J Neurosci 2013;33:11715-23.
11. Laviola G, Hannan AJ, Macri S, Solinas M, Jaber M. Effects of enriched environment on animal models of neurodegenerative diseases and psychiatric disorders. Neurobiol Dis 2008;31:159-68.
12. Nithianantharajah J, Hannan AJ. The neurobiology of brain and cognitive reserve: mental and physical activity as modulators of brain disorders. Prog Neurobiol 2009;89:369-82.
13. Kovesdi E, Gyorgy AB, Kwon SK, Wingo DL, Kamnaksh A, Long JB, et al. The effect of enriched environment on the outcome of traumatic brain injury; a behavioral, proteomics, and histological study. Front Neurosci 2011;5:42.
14. Nachat-Kappes R, Pinel A, Combe K, Lamas B, Farges MC, Rossary A, et al. Effects of enriched environment on COX-2, leptin and eicosanoids in a mouse model of breast cancer. PLoS One 2012;7:e51525.
15. Garofalo S, D'Alessandro G, Chece G, Brau F, Maggi L, Rosa A, et al. Enriched environment reduces glioma growth through immune and nonimmune mechanisms in mice. Nat Commun 2015;6:6623.
16. Li G, Gan Y, Fan Y, Wu Y, Lin H, Song Y, et al. Enriched environment inhibits mouse pancreatic cancer growth and down-regulates the expression of mitochondria-related genes in cancer cells. Sci Rep 2015;5:7856.
17. Arranz L, De Castro NM, Baeza I, Mate I, Viveros MP, De la Fuente M. Environmental enrichment improves age-related immune system impairment: long-term exposure since adulthood increases life span in mice. Rejuvenation Res 2010;13:415-28.
18. Arranz L, De CastroNM, Baeza I, Gimenez-Llort L, De la Fuente M. Effect of environmental enrichment on the immunoendocrine aging of male and female triple-transgenic 3xTg-AD mice for Alzheimer's disease. J Alzheimers Dis 2011;25:727-37.
19. de Sousa AA, Reis R, Bento-Torres J, Trevia N, Lins NA, Passos A, et al. Influence of enriched environment on viral encephalitis outcomes: behavioral and neuropathological changes in albino Swiss mice. PLoS One 2011;6:e15597.
20. Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ. Natural innate and adaptive immunity to cancer. Annu Rev Immunol 2011;29:235-71.
21. Vivier E, Ugolini S, Blaise D, Chabannon C, Brossay L. Targeting natural killer cells and natural killer T cells in cancer. Nat Rev Immunol 2012;12:239-52.
22. Chester C, Fritsch K, Kohrt HE. Natural killer cell immunomodulation: targeting activating, inhibitory, and co-stimulatory receptor signaling for cancer immunotherapy. Front Immunol 2015;6:601.
23. Rosi S, Pert CB, Ruff MR, McGann-Gramling K, Wenk GL. Chemokine receptor 5 antagonist D-Ala-peptide T-amide reduces microglia and astrocyte activation within the hippocampus in a neuroinflammatory rat model of Alzheimer's disease. Neuroscience 2005;134:671-6.
24. Lavergne E, Combadiere C, Iga M, Boissonnas A, Bonduelle O, Maho M, et al. Intratumoral CC chemokine ligand 5 overexpression delays tumor growth and increases tumor cell infiltration. J Immunol 2004;173: 3755-62.
25. Magnon C, Hall SJ, Lin J, Xue X, Gerber L, Freedland SJ, et al. Autonomic nerve development contributes to prostate cancer progression. Science 2013;341:1236361.
26. De la Torre JC. An improved approach to histofluorescence using the SPG method for tissue monoamines. J Neurosci Methods 1980;3:1-5.
27. Mainardi M, Scabia G, Vottari T, Santini F, Pinchera A, Maffei L, et al. A sensitive period for environmental regulation of eating behavior and leptin sensitivity. Proc Natl Acad Sci U S A 2010;107:16673-8.
28. Alter G, Malenfant JM, Altfeld M. CD107a as a functional marker for the identification of natural killer cell activity. J Immunol Methods 2004; 294:15-22.
29. Chan CJ, SmythMJ, Martinet L. Molecular mechanisms of natural killer cell activation in response to cellular stress. Cell Death Differ 2014; 21:5-14.
30. Bernardini G, Gismondi A, Santoni A. Chemokines and NK cells: regulators of development, trafficking and functions. Immunol Lett 2012;145:39-46.
31. Peng H, Tian Z. NK cell trafficking in health and autoimmunity:a comprehensive review. Clin Rev Allergy Immunol 2014;47:119-27.
32. Hwang CJ, Park MH, Hwang JY, Kim JH, Yun NY, Oh SY, et al. CCR5 deficiency accelerates lipopolysaccharide-induced astrogliosis, amyloidbeta deposit and impaired memory function. Oncotarget 2016;7: 11984-99.
33. Cao L, During MJ. What is the brain-cancer connection? Annu Rev Neurosci 2012;35:331-45.
34. Slater AM, Cao L. A protocol for housingmice in an enriched environment. J Vis Exp 2015:e52874.
35. Brown JC, Winters-Stone K, Lee A, Schmitz KH. Cancer, physical activity, and exercise. Compr Physiol 2012;2:2775-809.
36. Chida Y, Hamer M, Wardle J, Steptoe A. Do stress-related psychosocial factors contribute to cancer incidence and survival? Nat Clin Pract Oncol 2008;5:466-75.
37. Hinzey A, Gaudier-Diaz MM, Lustberg MB, DeVries AC. Breast cancer and social environment: getting by with a little help from our friends. Breast Cancer Res 2016;18:54.
38. Xiao R, Bergin SM, Huang W, Slater AM, Liu X, Judd RT, et al. Environmental and genetic activation of hypothalamic BDNF modulates T-cell immunity to exert an anticancer phenotype. Cancer Immunol Res 2016;4:488-97.
39. Iannello A, Raulet DH. Immune surveillance of unhealthy cells by natural killer cells. Cold Spring Harb Symp Quant Biol 2013;78:249-57.
40. Le Bert N, Gasser S. Advances in NKG2D ligand recognition and responses by NK cells. Immunol Cell Biol 2014;92:230-6.
41. Balistreri CR, Caruso C, Grimaldi MP, Listi F, Vasto S, Orlando V, et al. CCR5 receptor: biologic and genetic implications in age-related diseases. Ann N Y Acad Sci 2007;1100:162-72.
42. Liu C, Lou Y, Lizee G, Qin H, Liu S, Rabinovich B, et al. Plasmacytoid dendritic cells induce NK cell-dependent, tumor antigen-specific T cell cross-priming and tumor regression inmice. J Clin Invest 2008;118:1165-75.
43. Pedersen BK, Hoffman-Goetz L. Exercise and the immune system: regulation, integration, and adaptation. Physiol Rev 2000;80:1055-81.
44. Pedersen L, Idorn M, Olofsson GH, Lauenborg B, Nookaew I, Hansen RH, et al. Voluntary running suppresses tumor growth through epinephrineand IL-6-dependent NK cell mobilization and redistribution. Cell Metab 2016;23:554-62.
45. Li S, Jin M, Zhang D, Yang T, Koeglsperger T, Fu H, et al. Environmental novelty activates beta2-adrenergic signaling to prevent the impairment of hippocampal LTP by Abeta oligomers. Neuron 2013;77:929-41.
46. ThyagaRajan S, Madden KS, Teruya B, Stevens SY, Felten DL, Bellinger DL. Age-associated alterations in sympathetic noradrenergic innervation of primary and secondary lymphoid organs in female Fischer 344 rats. J Neuroimmunol 2011;233:54-64.
47. ThyagaRajan S, Tran L, Molinaro CA, Gridley DS, Felten DL, Bellinger DL. Prevention of mammary tumor development through neuroimmunomodulation in the spleen and lymph nodes of old female sprague-dawley rats by L-Deprenyl. Neuroimmunomodulation 2013;20:141-51.
48. Peng YP, Qiu YH, Jiang JL, Wang JJ. Effect of catecholamines on IL-2 production and NK cytotoxicity of rats invitro. Acta Pharmacol Sin 2004;25:1354-60.