Hippocampal dysfunctions in tumor-bearing mice

Brain, Behavior, and Immunity

Volumn 36, Issue , 2014, Pages 147-155

  Yang, Miyoung ^a,e   Kim, Juhwan ^a   Kim, Joong Sun ^b   Kim, Sung Ho ^a   Kim, Jong Choon ^a   Kang, Man Jong ^a   Jung, Uhee ^c   Shin, Taekyun ^d   Wang, Hongbing ^e   Moon, Changjong ^a  

^a Chonnam National University   (South Korea)

^b Dongnam Institute of Radiological and Medical Science   (South Korea)

^c Jeongeup Campus of Korea Atomic Energy Research Institute (KAERI)   (South Korea)

^d Jeju National University   (South Korea)

^e MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Cognition; Depression; Hippocampus; Inflammatory cytokines; Peripheral tumor; Stress hormone

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOSTERONE; CYCLOOXYGENASE 2; DOUBLECORTIN; INTERLEUKIN 6; KI 67 ANTIGEN; MESSENGER RNA; STRESS HORMONE; TUMOR NECROSIS FACTOR ALPHA;

ADRENAL GLAND; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLON CARCINOMA; CONTROLLED STUDY; DEPRESSION; FEMALE; HIPPOCAMPUS; MALE; MEMORY; MEMORY DISORDER; MOUSE; NEOPLASM; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL LINE, TUMOR; CORTICOSTERONE; CYCLOOXYGENASE 2; CYTOKINES; DEPRESSION; FEMALE; HIPPOCAMPUS; INFLAMMATION; MICE; MICE, INBRED BALB C; NEOPLASMS, EXPERIMENTAL; NEUROGENESIS; RECOGNITION (PSYCHOLOGY); STRESS, PHYSIOLOGICAL;

EID: 84891826884     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2013.10.022     Document Type: Article

References (68)

1. Barrientos R.M., Sprunger D.B., Campeau S., Watkins L.R., Rudy J.W., Maier S.F. BDNF mRNA expression in rat hippocampus following contextual learning is blocked by intrahippocampal IL-1β administration. J. Neuroimmunol. 2004, 155:119-126.
2. Baune B.T., Konrad C., Grotegerd D., Suslow T., Birosova E., Ohrmann P., Bauer J., Arolt V., Heindel W., Domschke K., Schoning S., Rauch A.V., Uhlmann C., Kugel H., Dannlowski U. Interleukin-6 gene (IL-6): a possible role in brain morphology in the healthy adult brain. J. Neuroinflamm. 2012, 9:125.
3. Ben-Baruch A. Host microenvironment in breast cancer development: inflammatory cells, cytokines and chemokines in breast cancer progression: reciprocal tumor-microenvironment interactions. Breast Cancer Res. 2003, 5:31-36.
4. Bower J.E. Behavioral symptoms in patients with breast cancer and survivors. J. Clin. Oncol. 2008, 26:768-777.
5. Brattsand R., Linden M. Cytokine modulation by glucocorticoids: mechanisms and actions in cellular studies. Aliment. Pharmacol. Ther. 1996, 10:81.
6. Braun I.M., Rao S.R., Pirl W.F. Comparison of self-reported cognitive difficulties in a national sample of long-term cancer survivors and cancer-naive controls. Psychosomatics 2012, 53:68-74.
7. Brown K.W., Levy A.R., Rosberger Z., Edgar L. Psychological distress and cancer survival: a follow-up 10years after diagnosis. Psychosom. Med. 2003, 65:636-643.
8. Bruera E. Clinical management of anorexia and cachexia in patients with advanced cancer. Oncology 1992, 49(Suppl. 2):35-42.
9. Chrousos G.P. The hypothalamic-pituitary-adrenal axis and immune-mediated inflammation. N. Engl. J. Med. 1995, 332:1531.
10. Corwin E.J. Understanding cytokines part I: physiology and mechanism of action. Biol. Res. Nurs. 2000, 2:30-40.
11. Coussens L.M., Werb Z. Inflammation and cancer. Nature 2002, 420:860-867.
12. Culig Z. Cytokine disbalance in common human cancers. Biochim. Biophys. Acta 2011, 1813:308-314.
13. Dantzer R., Aubert A., Bluthe R.-M., Gheusi G., Cremona S., Laye S., Konsman J.-P., Parnet P., Kelley K.W. Mechanisms of the Behavioural Effects of Cytokines. Cytokines, Stress and Depression 1999, Springer, pp. 83-105.
14. Das U.N. Clinical laboratory tools to diagnose inflammation. Adv. Clin. Chem. 2006, 41:189-229.
15. Dinel A.-L., André C., Aubert A., Ferreira G., Layé S., Castanon N. Cognitive and emotional alterations are related to hippocampal inflammation in a mouse model of metabolic syndrome. PLoS One 2011, 6:e24325.
16. Gilbert C.A., Slingerland J.M. Cytokines, obesity and cancer: new insights on mechanisms linking obesity to cancer risk and progression. Annu. Rev. Med. 2013, 64:45-57.
17. Goshen I., Yirmiya R. Interleukin-1 (IL-1): a central regulator of stress responses. Front. Neuroendocrinol. 2009, 30:30-45.
18. Gould E., Tanapat P. Stress and hippocampal neurogenesis. Biol. Psychiatry 1999, 46:1472-1479.
19. Iosif R.E., Ekdahl C.T., Ahlenius H., Pronk C.J., Bonde S., Kokaia Z., Jacobsen S.-E.W., Lindvall O. Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. J. Neurosci. 2006, 26:9703-9712.
20. Jang S., Kelley K.W., Johnson R.W. Luteolin reduces IL-6 production in microglia by inhibiting JNK phosphorylation and activation of AP-1. Proc. Natl. Acad. Sci. 2008, 105:7534-7539.
21. Kempermann G., Kuhn H.G., Gage F.H. Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc. Natl. Acad. Sci. USA 1997, 94:10409-10414.
22. Kempermann G., Gast D., Gage F.H. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann. Neurol. 2002, 52:135-143.
23. Kim J.S., Lee H.J., Kim J.C., Kang S.S., Bae C.S., Shin T., Jin J.K., Kim S.H., Wang H., Moon C. Transient impairment of hippocampus-dependent learning and memory in relatively low-dose of acute radiation syndrome is associated with inhibition of hippocampal neurogenesis. J. Radiat. Res. 2008, 49:517-526.
24. Kim J.S., Jung J., Lee H.J., Kim J.C., Wang H., Kim S.H., Shin T., Moon C. Differences in immunoreactivities of Ki-67 and doublecortin in the adult hippocampus in three strains of mice. Acta Histochem. 2009, 111:150-156.
25. Kohman R.A., Rhodes J.S. Neurogenesis, inflammation and behavior. Brain Behav. Immun. 2012, 27:22-32.
26. Korte M., Carroll P., Wolf E., Brem G., Thoenen H., Bonhoeffer T. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. 1995, 92:8856-8860.
27. Li Y., Luikart B.W., Birnbaum S., Chen J., Kwon C.-H., Kernie S.G., Bassel-Duby R., Parada L.F. TrkB regulates hippocampal neurogenesis and governs sensitivity to antidepressive treatment. Neuron 2008, 59:399-412.
28. Linnarsson S., Björklund A., Ernfors P. Learning deficit in BDNF mutant mice. Eur. J. Neurosci. 2006, 9:2581-2587.
29. -δδCT method. Methods 2001, 25:402-408.
30. Lucas S.M., Rothwell N.J., Gibson R.M. The role of inflammation in CNS injury and disease. Br. J. Pharmacol. 2006, 147:S232-S240.
31. Lupien S.J., McEwen B.S. The acute effects of corticosteroids on cognition: integration of animal and human model studies. Brain Res. Rev. 1997, 24:1-27.
32. Maes M. Evidence for an immune response in major depression: a review and hypothesis. Prog. Neuropsychopharmacol. Biol. Psychiatry 1995, 19:11-38.
33. Mantovani G., Madeddu C., Maccio A., Gramignano G., Lusso M.R., Massa E., Astara G., Serpe R. Cancer-related anorexia/cachexia syndrome and oxidative stress: an innovative approach beyond current treatment. Cancer Epidemiol. Biomarkers Prev. 2004, 13:1651-1659.
34. Marmigère F., Givalois L., Rage F., Arancibia S., Tapia-Arancibia L. Rapid induction of BDNF expression in the hippocampus during immobilization stress challenge in adult rats. Hippocampus 2003, 13:646-655.
35. Marsland A.L., Gianaros P.J., Abramowitch S.M., Manuck S.B., Hariri A.R. Interleukin-6 covaries inversely with hippocampal grey matter volume in middle-aged adults. Biol. Psychiatry 2008, 64:484-490.
36. Martinowich K., Manji H., Lu B. New insights into BDNF function in depression and anxiety. Nat. Neurosci. 2007, 10:1089-1093.
37. McAfoose J., Baune B.T. Evidence for a cytokine model of cognitive function. Neurosci. Biobehav. Rev. 2009, 33:355-366.
38. McEwen B., De Kloet E., Rostene W. Adrenal steroid receptors and actions in the nervous system. Physiol. Rev. 1986, 66:1121-1188.
39. McEwen B.S., Cameron H., Chao H.M., Gould E., Magarinos A.M., Watanabe Y., Woolley C.S. Adrenal steroids and plasticity of hippocampal neurons: toward an understanding of underlying cellular and molecular mechanisms. Cell. Mol. Neurobiol. 1993, 13:457-482.
40. Minghetti L. Cyclooxygenase-2 (COX-2) in inflammatory and degenerative brain diseases. J. Neuropathol. Exp. Neurol. 2004, 63:901-910.
41. Monje M.L., Toda H., Palmer T.D. Inflammatory blockade restores adult hippocampal neurogenesis. Sci. Signal. 2003, 302:1760.
42. Morales I., Farias G., Maccioni R.B. Neuroimmunomodulation in the pathogenesis of Alzheimer's disease. NeuroImmunoModulation 2010, 17:202-204.
43. Nelson T., Olde Engberink A., Hernandez R., Puro A., Huitron-Resendiz S., Hao C., De Graan P., Gruol D. Altered synaptic transmission in the hippocampus of transgenic mice with enhanced central nervous systems expression of interleukin-6. Brain Behav. Immun. 2012, 26:959-971.
44. Peng Y.-P., Qiu Y.-H., Lu J.-H., Wang J.-J. Interleukin-6 protects cultured cerebellar granule neurons against glutamate-induced neurotoxicity. Neurosci. Lett. 2005, 374:192-196.
45. Pistell P.J., Morrison C.D., Gupta S., Knight A.G., Keller J.N., Ingram D.K., Bruce-Keller A.J. Cognitive impairment following high fat diet consumption is associated with brain inflammation. J. Neuroimmunol. 2010, 219:25-32.
46. Pyter L.M., Pineros V., Galang J.A., McClintock M.K., Prendergast B.J. Peripheral tumors induce depressive-like behaviors and cytokine production and alter hypothalamic-pituitary-adrenal axis regulation. Proc. Natl. Acad. Sci. USA 2009, 106:9069-9074.
47. Pyter L.M., Cochrane S.F., Ouwenga R.L., Patel P.N., Pineros V., Prendergast B.J. Mammary tumors induce select cognitive impairments. Brain Behav. Immun. 2010, 24:903-907.
48. Raison C.L., Capuron L., Miller A.H. Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends Immunol. 2006, 27:24-31.
49. Rall J.M., Mach S.A., Dash P.K. Intrahippocampal infusion of a cyclooxygenase-2 inhibitor attenuates memory acquisition in rats. Brain Res. 2003, 968:273-276.
50. Ramos E.J., Suzuki S., Marks D., Inui A., Asakawa A., Meguid M.M. Cancer anorexia-cachexia syndrome: cytokines and neuropeptides. Curr. Opin. Clin. Nutr. Metab. Care 2004, 7:427-434.
51. Schagen S.B., Muller M.J., Boogerd W., Mellenbergh G.J., van Dam F.S. Change in cognitive function after chemotherapy: a prospective longitudinal study in breast cancer patients. J. Natl Cancer Inst. 2006, 98:1742-1745.
52. Scharfman H., Goodman J., Macleod A., Phani S., Antonelli C., Croll S. Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp. Neurol. 2005, 192:348-356.
53. Seo H.S., Yang M., Song M.S., Kim J.S., Kim S.H., Kim J.C., Kim H., Shin T., Wang H., Moon C. Toluene inhibits hippocampal neurogenesis in adult mice. Pharmacol. Biochem. Behav. 2010, 94:588-594.
54. Shaw K.N., Commins S., O'Mara S.M. Deficits in spatial learning and synaptic plasticity induced by the rapid and competitive broad-spectrum cyclooxygenase inhibitor ibuprofen are reversed by increasing endogenous brain-derived neurotrophic factor. Eur. J. Neurosci. 2003, 17:2438-2446.
55. Steru L., Chermat R., Thierry B., Simon P. The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology 1985, 85:367-370.
56. Tanaka Y., Eda H., Tanaka T., Udagawa T., Ishikawa T., Horii I., Ishitsuka H., Kataoka T., Taguchi T. Experimental cancer cachexia induced by transplantable colon 26 adenocarcinoma in mice. Cancer Res. 1990, 50:2290-2295.
57. Tao X., Finkbeiner S., Arnold D.B., Shaywitz A.J., Greenberg M.E. Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 1998, 20:709-726.
58. Teather L.A., Packard M.G., Bazan N.G. Post-training cyclooxygenase-2 (COX-2) inhibition impairs memory consolidation. Learn. Mem. 2002, 9:41-47.
59. Tong L., Balazs R., Soiampornkul R., Thangnipon W., Cotman C.W. Interleukin-1β impairs brain derived neurotrophic factor-induced signal transduction. Neurobiol. Aging 2008, 29:1380-1393.
60. Watkins L.R., Nguyen K.T., Lee J.E., Maier S.F. Dynamic Regulation of Proinflammatory Cytokines. Cytokines, Stress, and Depression 1999, Springer, pp. 153-178.
61. Wefel J.S., Lenzi R., Theriault R., Buzdar A.U., Cruickshank S., Meyers C.A. 'Chemobrain' in breast carcinoma? a prologue. Cancer 2004, 101:466-475.
62. Wefel J.S., Lenzi R., Theriault R.L., Davis R.N., Meyers C.A. The cognitive sequelae of standard-dose adjuvant chemotherapy in women with breast carcinoma. Cancer 2004, 100:2292-2299.
63. Wefel J.S., Witgert M.E., Meyers C.A. Neuropsychological sequelae of non-central nervous system cancer and cancer therapy. Neuropsychol. Rev. 2008, 18:121-131.
64. Winocur G., Henkelman M., Wojtowicz J.M., Zhang H., Binns M.A., Tannock I.F. The effects of chemotherapy on cognitive function in a mouse model: a prospective study. Clin. Cancer Res. 2012, 18:3112-3121.
65. Yamagata K., Andreasson K.I., Kaufmann W.E., Barnes C.A., Worley P.F. Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids. Neuron 1993, 11:371-386.
66. Yang M., Kim J.S., Song M.S., Kim S.H., Kang S.S., Bae C.S., Kim J.C., Wang H., Shin T., Moon C. Cyclophosphamide impairs hippocampus-dependent learning and memory in adult mice: possible involvement of hippocampal neurogenesis in chemotherapy-induced memory deficits. Neurobiol. Learn. Mem. 2010, 93:487-494.
67. Yang M., Kim J.S., Kim J., Kim S.H., Kim J.C., Kim J., Wang H., Shin T., Moon C. Neurotoxicity of methotrexate to hippocampal cells in vivo and in vitro. Biochem. Pharmacol. 2011, 82:72-80.
68. Yang M., Kim J.S., Kim J., Jang S., Kim S.H., Kim J.C., Shin T., Wang H., Moon C. Acute treatment with methotrexate induces hippocampal dysfunction in a mouse model of breast cancer. Brain Res. Bull. 2012, 89:50-56.