Up-regulated fractalkine (FKN) and its receptor CX3CR1 are involved in fructose-induced neuroinflammation: Suppression by curcumin

Brain, Behavior, and Immunity

Volumn 58, Issue , 2016, Pages 69-81

  Xu, Min Xuan ^a   Yu, Rong ^a   Shao, Li Fei ^a   Zhang, Yan Xiu ^a   Ge, Chen Xu ^a   Liu, Xin Meng ^a   Wu, Wen Yuan ^a   Li, Jian Mei ^a   Kong, Ling Dong ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

Curcumin; FKN CX3CR1 signaling; Fructose; Neuroinflammation; Neuronal damage

Indexed keywords

CHEMOKINE RECEPTOR CX3CR1; CURCUMIN; CYTOKINE; FRACTALKINE; FRUCTOSE; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PIOGLITAZONE; TOLL LIKE RECEPTOR 4; CX3CL1 PROTEIN, MOUSE; CX3CR1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DENTATE GYRUS; DRUG MECHANISM; GENE EXPRESSION; HIPPOCAMPUS; IN VITRO STUDY; MALE; MICROGLIA; MOUSE; NERVE CELL LESION; NERVE CELL NETWORK; NERVOUS SYSTEM INFLAMMATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; UPREGULATION; ANIMAL; CELL PROLIFERATION; CHEMICALLY INDUCED; DRUG EFFECTS; ENCEPHALITIS; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; ASTROCYTES; CELL PROLIFERATION; CHEMOKINE CX3CL1; CURCUMIN; CX3C CHEMOKINE RECEPTOR 1; ENCEPHALITIS; FRUCTOSE; HIPPOCAMPUS; MALE; MICE, INBRED ICR; MICROGLIA; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84953791558     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2016.01.001     Document Type: Article

References (57)

1. Andrikopoulos, S., Blair, A.R., Deluca, N., Fam, B.C., Proietto, J., Evaluating the glucose tolerance test in mice. Am. J. Physiol. Endocrinol. Metab. 295 (2008), E1323–E1332.
2. Arindkar, S., Bhattacharjee, J., Kumar, J.M., Das, B., Upadhyay, P., Asif, S., Juyal, R.C., Majumdar, S.S., Perumal, N., Antigen peptide transporter 1 is involved in the development of fructose-induced hepatic steatosis in mice. J. Gastroenterol. Hepatol. 28 (2013), 1403–1409.
3. Bachstetter, A.D., Morganti, J.M., Jernberg, J., Schlunk, A., Mitchell, S.H., Brewster, K.W., Hudson, C.E., Cole, M.J., Harrison, J.K., Bickford, P.C., Gemma, C., Fractalkine and CX3CR1 regulate hippocampal neurogenesis in adult and aged rats. Neurobiol. Aging 32 (2011), 2030–2044.
4. Bertollini, C., Ragozzino, D., Gross, C., Limatola, C., Eusebi, F., Fractalkine/CX3CL1 depresses central synaptic transmission in mouse hippocampal slices. Neuropharmacology 51 (2006), 816–821.
5. Cameron, H.A., McKay, R.D., Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol. 435 (2001), 406–417.
6. Cardona, A.E., Pioro, E.P., Sasse, M.E., Kostenko, V., Cardona, S.M., Dijkstra, I.M., Huang, D., Kidd, G., Dombrowski, S., Dutta, R., Lee, J.C., Cook, D.N., Jung, S., Lira, S.A., Littman, D.R., Ransohoff, R.M., Control of microglial neurotoxicity by the fractalkine receptor. Nat. Neurosci. 9 (2006), 917–924.
7. Chandrasekar, B., Mummidi, S., Perla, R.P., Bysani, S., Dulin, N.O., Liu, F., Melby, P.C., Fractalkine (CX3CL1) stimulated by nuclear factor kappaB (NF-kappaB)-dependent inflammatory signals induces aortic smooth muscle cell proliferation through an autocrine pathway. Biochem. J. 373 (2003), 547–558.
8. Cipriani, R., Villa, P., Chece, G., Lauro, C., Paladini, A., Micotti, E., Perego, C., De Simoni, M.G., Fredholm, B.B., Eusebi, F., Limatola, C., CX3CL1 is neuroprotective in permanent focal cerebral ischemia in rodents. J. Neurosci. 31 (2011), 16327–16335.
9. Couillard-Despres, S., Winner, B., Schaubeck, S., Aigner, R., Vroemen, M., Weidner, N., Bogdahn, U., Winkler, J., Kuhn, H.G., Aigner, L., Doublecortin expression levels in adult brain reflect neurogenesis. Eur. J. Neurosci. 21 (2005), 1–14.
10. Doggui, S., Belkacemi, A., Paka, G.D., Perrotte, M., Pi, R., Ramassamy, C., Curcumin protects neuronal-like cells against acrolein by restoring Akt and redox signaling pathways. Mol. Nutr. Food Res. 57 (2013), 1660–1670.
11. Escartin, C., Bonvento, G., Targeted activation of astrocytes: a potential neuroprotective strategy. Mol. Neurobiol. 38 (2008), 231–241.
12. Fuhrmann, M., Bittner, T., Jung, C.K., Burgold, S., Page, R.M., Mitteregger, G., Haass, C., LaFerla, F.M., Kretzschmar, H., Herms, J., Microglial Cx3cr1 knockout prevents neuron loss in a mouse model of Alzheimer's disease. Nat. Neurosci. 13 (2010), 411–413.
13. Gabel, S., Koncina, E., Dorban, G., Heurtaux, T., Birck, C., Glaab, E., Michelucci, A., Heuschling, P., Grandbarbe, L., Inflammation promotes a conversion of astrocytes into neural progenitor cells via NF-κB activation. Mol. Neurobiol., 2015 [Epub ahead of print].
14. Gray, E., Ginty, M., Kemp, K., Scolding, N., Wilkins, A., The PPAR-gamma agonist pioglitazone protects cortical neurons from inflammatory mediators via improvement in peroxisomal function. J. Neuroinflammation, 9, 2012, 63.
15. Haydon, P.G., GLIA: listening and talking to the synapse. Nat. Rev. Neurosci. 2 (2001), 185–193.
16. Hsu, T.M., Konanur, V.R., Taing, L., Usui, R., Kayser, B.D., Goran, M.I., Kanoski, S.E., Effects of sucrose and high fructose corn syrup consumption on spatial memory function and hippocampal neuroinflammation in adolescent rats. Hippocampus 25 (2015), 227–239.
17. Hwang, I.K., Kim, I.Y., Kim, D.W., Yoo, K.Y., Kim, Y.N., Yi, S.S., Won, M.H., Lee, I.S., Yoon, Y.S., Seong, J.K., Strain-specific differences in cell proliferation and differentiation in the dentate gyrus of C57BL/6N and C3H/HeN mice fed a high fat diet. Brain Res. 1241 (2008), 1–6.
18. Hwang, I.K., Yi, S.S., Song, W., Won, M.H., Yoon, Y.S., Seong, J.K., Effects of age and treadmill exercise in chronic diabetic stages on neuroblast differentiation in a rat model of type 2 diabetes. Brain Res. 1341 (2010), 63–71.
19. Lang, B.T., Yan, Y., Dempsey, R.J., Vemuganti, R., Impaired neurogenesis in adult type-2 diabetic rats. Brain Res. 1258 (2009), 25–33.
20. Le, M.T., Frye, R.F., Rivard, C.J., Cheng, J., McFann, K.K., Segal, M.S., Johnson, R.J., Johnson, J.A., Effects of high-fructose corn syrup and sucrose on the pharmacokinetics of fructose and acute metabolic and hemodynamic responses in healthy subjects. Metabolism 61 (2012), 641–651.
21. Lee, J.K., Seo, E.M., Lee, S.S., Park, S.H., Sim, Y.B., Jung, J.S., Kim, S.M., Suh, H.W., Activation of PPARalpha attenuates IFNgamma and IL-1beta-induced cell proliferation in astrocytes: involvement of IL-6 independent pathway. Korean J. Physiol. Pharmacol. 14 (2010), 185–189.
22. Lee, S., Varvel, N.H., Konerth, M.E., Xu, G., Cardona, A.E., Ransohoff, R.M., Lamb, B.T., CX3CR1 deficiency alters microglial activation and reduces beta-amyloid deposition in two Alzheimer's disease mouse models. Am. J. Pathol. 177 (2010), 2549–2562.
23. Li, J.M., Ge, C.X., Xu, M.X., Wang, W., Yu, R., Fan, C.Y., Kong, L.D., Betaine recovers hypothalamic neural injury by inhibiting astrogliosis and inflammation in fructose-fed rats. Mol. Nutr. Food Res. 59 (2015), 189–202.
24. Lyssiotis, C.A., Cantley, L.C., Metabolic syndrome: F stands for fructose and fat. Nature 502 (2013), 181–182.
25. Maciejewski-Lenoir, D., Chen, S., Feng, L., Maki, R., Bacon, K.B., Characterization of fractalkine in rat brain cells: migratory and activation signals for CX3CR-1-expressing microglia. J. Immunol. 163 (1999), 1628–1635.
26. Miller, A.A., Spencer, S.J., Obesity and neuroinflammation: a pathway to cognitive impairment. Brain Behav. Immun. 42 (2014), 10–21.
27. Mizuno, T., Kawanokuchi, J., Numata, K., Suzumura, A., Production and neuroprotective functions of fractalkine in the central nervous system. Brain Res. 979 (2003), 65–70.
28. Morari, J., Anhe, G.F., Nascimento, L.F., de Moura, R.F., Razolli, D., Solon, C., Guadagnini, D., Souza, G., Mattos, A.H., Tobar, N., Ramos, C.D., Pascoal, V.D., Saad, M.J., Lopes-Cendes, I., Moraes, J.C., Velloso, L.A., Fractalkine (CX3CL1) is involved in the early activation of hypothalamic inflammation in experimental obesity. Diabetes 63 (2014), 3770–3784.
29. Nash, K.R., Moran, P., Finneran, D.J., Hudson, C., Robinson, J., Morgan, D., Bickford, P.C., Fractalkine over expression suppresses alpha-synuclein-mediated neurodegeneration. Mol. Ther. 23 (2015), 17–23.
30. Orre, M., Kamphuis, W., Osborn, L.M., Melief, J., Kooijman, L., Huitinga, I., Klooster, J., Bossers, K., Hol, E.M., Acute isolation and transcriptome characterization of cortical astrocytes and microglia from young and aged mice. Neurobiol. Aging 35 (2014), 1–14.
31. Pabon, M.M., Bachstetter, A.D., Hudson, C.E., Gemma, C., Bickford, P.C., CX3CL1 reduces neurotoxicity and microglial activation in a rat model of Parkinson's disease. J. Neuroinflammation, 8, 2011, 9.
32. Paolicelli, R.C., Bisht, K., Tremblay, M.E., Fractalkine regulation of microglial physiology and consequences on the brain and behavior. Front. Cell. Neurosci., 8, 2014, 129.
33. Papadopoulos, P., Rosa-Neto, P., Rochford, J., Hamel, E., Pioglitazone improves reversal learning and exerts mixed cerebrovascular effects in a mouse model of Alzheimer's disease with combined amyloid-beta and cerebrovascular pathology. PLoS One, 8, 2013, e68612.
34. Pascual, O., Ben Achour, S., Rostaing, P., Triller, A., Bessis, A., Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc. Natl. Acad. Sci. USA 109 (2012), E197–E205.
35. Pehar, M., Cassina, P., Vargas, M.R., Castellanos, R., Viera, L., Beckman, J.S., Estevez, A.G., Barbeito, L., Astrocytic production of nerve growth factor in motor neuron apoptosis: implications for amyotrophic lateral sclerosis. J. Neurochem. 89 (2004), 464–473.
36. Piccinin, S., Di Angelantonio, S., Piccioni, A., Volpini, R., Cristalli, G., Fredholm, B.B., Limatola, C., Eusebi, F., Ragozzino, D., CX3CL1-induced modulation at CA1 synapses reveals multiple mechanisms of EPSC modulation involving adenosine receptor subtypes. J. Neuroimmunol. 224 (2010), 85–92.
37. Polyak, A., Ferenczi, S., Denes, A., Winkler, Z., Kriszt, R., Pinter-Kubler, B., Kovacs, K.J., The fractalkine/Cx3CR1 system is implicated in the development of metabolic visceral adipose tissue inflammation in obesity. Brain Behav. Immun. 38 (2014), 25–35.
38. Raspe, C., Hocherl, K., Rath, S., Sauvant, C., Bucher, M., NF-kappaB-mediated inverse regulation of fractalkine and CX3CR1 during CLP-induced sepsis. Cytokine 61 (2013), 97–103.
39. Ray, K., Obesity: metabolic effects of fructose. Nat. Rev. Endocrinol., 9, 2013, 627.
40. Schutz, B., Reimann, J., Dumitrescu-Ozimek, L., Kappes-Horn, K., Landreth, G.E., Schurmann, B., Zimmer, A., Heneka, M.T., The oral antidiabetic pioglitazone protects from neurodegeneration and amyotrophic lateral sclerosis-like symptoms in superoxide dismutase-G93A transgenic mice. J. Neurosci. 25 (2005), 7805–7812.
41. Shah, R., O'Neill, S.M., Hinkle, C., Caughey, J., Stephan, S., Lynch, E., Bermingham, K., Lynch, G., Ahima, R.S., Reilly, M.P., Metabolic effects of CX3CR1 deficiency in diet-induced obese mice. PLoS One, 10, 2015, e0138317.
42. Shehzad, A., Rehman, G., Lee, Y.S., Curcumin in inflammatory diseases. BioFactors 39 (2013), 69–77.
43. Sheridan, G.K., Murphy, K.J., Neuron-glia crosstalk in health and disease: fractalkine and CX3CR1 take centre stage. Open Biol., 3, 2013, 130181.
44. Sobesky, J.L., Barrientos, R.M., De May, H.S., Thompson, B.M., Weber, M.D., Watkins, L.R., Maier, S.F., High-fat diet consumption disrupts memory and primes elevations in hippocampal IL-1beta, an effect that can be prevented with dietary reversal or IL-1 receptor antagonism. Brain Behav. Immun. 42 (2014), 22–32.
45. Tamashiro, T.T., Dalgard, C.L., Byrnes, K.R., Primary microglia isolation from mixed glial cell cultures of neonatal rat brain tissue. J. Visualized Exp., 2012, e3814.
46. Tappy, L., Le, K.A., Metabolic effects of fructose and the worldwide increase in obesity. Physiol. Rev. 90 (2010), 23–46.
47. Thaler, J.P., Yi, C.X., Schur, E.A., Guyenet, S.J., Hwang, B.H., Dietrich, M.O., Zhao, X., Sarruf, D.A., Izgur, V., Maravilla, K.R., Nguyen, H.T., Fischer, J.D., Matsen, M.E., Wisse, B.E., Morton, G.J., Horvath, T.L., Baskin, D.G., Tschop, M.H., Schwartz, M.W., Obesity is associated with hypothalamic injury in rodents and humans. J. Clin. Invest. 122 (2012), 153–162.
48. Tizabi, Y., Hurley, L.L., Qualls, Z., Akinfiresoye, L., Relevance of the anti-inflammatory properties of curcumin in neurodegenerative diseases and depression. Molecules 19 (2014), 20864–20879.
49. Tu, X.K., Yang, W.Z., Chen, J.P., Chen, Y., Ouyang, L.Q., Xu, Y.C., Shi, S.S., Curcumin inhibits TLR2/4-NF-kappaB signaling pathway and attenuates brain damage in permanent focal cerebral ischemia in rats. Inflammation 37 (2014), 1544–1551.
50. Utreras, E., Hamada, R., Prochazkova, M., Terse, A., Takahashi, S., Ohshima, T., Kulkarni, A.B., Suppression of neuroinflammation in forebrain-specific Cdk5 conditional knockout mice by PPARgamma agonist improves neuronal loss and early lethality. J. Neuroinflammation, 11, 2014, 28.
51. Vargas, M.R., Johnson, D.A., Sirkis, D.W., Messing, A., Johnson, J.A., Nrf2 activation in astrocytes protects against neurodegeneration in mouse models of familial amyotrophic lateral sclerosis. J. Neurosci. 28 (2008), 13574–13581.
52. Viscogliosi, G., Andreozzi, P., Chiriac, I.M., Cipriani, E., Servello, A., Marigliano, B., Ettorre, E., Marigliano, V., Depressive symptoms in older people with metabolic syndrome: is there a relationship with inflammation?. Int. J. Geriatric Psychiatry 28 (2013), 242–247.
53. von Bernhardi, R., Eugenin, J., Microglial reactivity to beta-amyloid is modulated by astrocytes and proinflammatory factors. Brain Res. 1025 (2004), 186–193.
54. Wang, W., Ding, X.Q., Gu, T.T., Song, L., Li, J.M., Xue, Q.C., Kong, L.D., Pterostilbene and allopurinol reduce fructose-induced podocyte oxidative stress and inflammation via microRNA-377. Free Radic. Biol. Med. 83 (2015), 214–226.
55. Yang, Z., Zhao, T., Zou, Y., Zhang, J.H., Feng, H., Curcumin inhibits microglia inflammation and confers neuroprotection in intracerebral hemorrhage. Immunol. Lett. 160 (2014), 89–95.
56. Zhang, X., Zhang, J.H., Chen, X.Y., Hu, Q.H., Wang, M.X., Jin, R., Zhang, Q.Y., Wang, W., Wang, R., Kang, L.L., Li, J.S., Li, M., Pan, Y., Huang, J.J., Kong, L.D., Reactive oxygen species-induced TXNIP drives fructose-mediated hepatic inflammation and lipid accumulation through NLRP3 inflammasome activation. Antioxid. Redox Signal. 22 (2015), 848–870.
57. Zhu, H.T., Bian, C., Yuan, J.C., Chu, W.H., Xiang, X., Chen, F., Wang, C.S., Feng, H., Lin, J.K., Curcumin attenuates acute inflammatory injury by inhibiting the TLR4/MyD88/NF-kappaB signaling pathway in experimental traumatic brain injury. J. Neuroinflammation, 11, 2014, 59.