The effect of abscisic acid chronic treatment on neuroinflammatory markers and memory in a rat model of high-fat diet induced neuroinflammation

Nutrition and Metabolism

Volumn 13, Issue 1, 2016, Pages 1-11

  Sánchez Sarasúa, Sandra ^a   Moustafa, Salma ^a   García Avilés, Álvaro ^a   López Climent, María Fernanda ^a   Gómez Cadenas, Aurelio ^a   Olucha Bordonau, Francisco E ^a   Sánchez Pérez, Ana M ^a  

^a UNIVERSITAT JAUME I   (Spain)

Author keywords

Microglia; Obesity; Phytohormones; Working memory

Indexed keywords

ABSCISIC ACID; GLUCOSE; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL PROLIFERATION; CONTROLLED STUDY; DIETARY SUPPLEMENT; DRUG BLOOD LEVEL; DRUG EFFECT; DRUG TISSUE LEVEL; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; INSULIN RESISTANCE; LIPID DIET; LONG TERM CARE; MALE; MAZE TEST; MEMORY; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; RAT; T MAZE TEST; TNFA GENE; TREATMENT DURATION;

EID: 84995483148     PISSN: None     EISSN: 17437075     Source Type: Journal    
DOI: 10.1186/s12986-016-0137-3     Document Type: Article

References (60)

1. Miller AA, Spencer SJ. Obesity and neuroinflammation: a pathway to cognitive impairment. Brain Behav Immun. 2014;42:10-21.
2. Della-Morte D, Palmirotta R, Rehni AK, Pastore D, Capuani B, Pacifici F, De Marchis ML, Dave KR, Bellia A, Fogliame G, Ferroni P, Donadel G, Cacciatore F, Abete P, Dong C, Pileggi A, Roselli M, Ricordi C, Sbraccia P, Guadagni F, Rundek T, Lauro D. Pharmacogenomics and pharmacogenetics of thiazolidinediones: role in diabetes and cardiovascular risk factors. Pharmacogenomics. 2014;15:2063-82.
3. Panicker GK, Karnad DR, Salvi V, Kothari S. Cardiovascular risk of oral antidiabetic drugs: current evidence and regulatory requirements for new drugs. J Assoc Physicians India. 2012;60:56-61.
4. Nissen SE, Wolski K. Effect of rosiglitazone on the risk of myocardial infarction and death from cardiovascular causes. N Engl J Med. 2007;356:2457-71.
5. Le Page-Degivry MT, Bidard JN, Rouvier E, Bulard C, Lazdunski M. Presence of abscisic acid, a phytohormone, in the mammalian brain. Proc Natl Acad Sci U S A. 1986;83:1155-8.
6. Minorsky PV. Abscisic acid: a universal signalling factor? Plant Physiol. 2002;128:788-9.
7. Gomez-Cadenas A, Vives V, Zandalinas SI, Manzi M, Sanchez-Perez AM, Perez-Clemente RM, Arbona V. Abscisic acid: a versatile phytohormone in plant signaling and beyond. Curr Protein Pept Sci. 2015;16:413-34.
8. Magnone M, Ameri P, Salis A, Andraghetti G, Emionite L, Murialdo G, De Flora A, Zocchi E. Microgram amounts of abscisic acid in fruit extracts improve glucose tolerance and reduce insulinemia in rats and in humans. FASEB J. 2015;29:4783-93.
9. Puce S, Basile G, Bavestrello G, Bruzzone S, Cerrano C, Giovine M, Arillo A, Zocchi E. Abscisic acid signaling through cyclic ADP-ribose in hydroid regeneration. J Biol Chem. 2004;279:39783-8.
10. Bassaganya-Riera J, Skoneczka J, Kingston DGJ, Krishnan A, Misyak SA, Guri AJ, Pereira A, Carter AB, Minorsky P, Tumarkin R, Hontecillas R. Mechanisms of action and medicinal applications of abscisic Acid. Curr Med Chem. 2010;17:467-78.
11. Bruzzone S, Bodrato N, Usai C, Guida L, Moreschi I, Nano R, Antonioli B, Fruscione F, Magnone M, Scarfì S, De Flora A, Zocchi E. Abscisic acid is an endogenous stimulator of insulin release from human pancreatic islets with cyclic ADP ribose as second messenger. J Biol Chem. 2008;283:32188-97.
12. Guri AJ, Evans NP, Hontecillas R, Bassaganya-Riera J. T cell PPARγ is required for the anti-inflammatory efficacy of abscisic acid against experimental IBD. J Nutr Biochem. 2011;22:812-9.
13. Sturla L, Fresia C, Guida L, Bruzzone S, Scarfì S, Usai C, Fruscione F, Magnone M, Millo E, Basile G, Grozio A, Jacchetti E, Allegretti M, De Flora A, Zocchi E. LANCL2 is necessary for abscisic acid binding and signaling in human granulocytes and in rat insulinoma cells. J Biol Chem. 2009;284:28045-57.
14. Lu P, Hontecillas R, Philipson CW, Bassaganya-Riera J. Lanthionine synthetase component C-like protein 2: a new drug target for inflammatory diseases and diabetes. Curr Drug Targets. 2014;15:565-72.
15. Bremner JD, Shearer KD, McCaffery PJ. Retinoic acid and affective disorders: the evidence for an association. J Clin Psychiatry. 2012;73:37-50.
16. Qi C-C, Zhang Z, Fang H, Liu J, Zhou N, Ge J-F, Chen F-H, Xiang C-B, Zhou J-N. Antidepressant effects of abscisic acid mediated by the downregulation of corticotrophin-releasing hormone gene expression in rats. Int J Neuropsychopharmacol. 2014;(1-9). doi:10.1093/ijnp/pyu006.
17. Qi C-C, Ge J-F, Zhou J-N. Preliminary evidence that abscisic acid improves spatial memory in rats. Physiol Behav. 2015;139:231-9.
18. Gao Y, Ottaway N, Schriever SC, Legutko B, García-Cáceres C, de la Fuente E, Mergen C, Bour S, Thaler JP, Seeley RJ, Filosa J, Stern JE, Perez-Tilve D, Schwartz MW, Tschöp MH, Yi C-X. Hormones and diet, but not body weight, control hypothalamic microglial activity. Glia. 2014;62:17-25.
19. Spielman LJ, Little JP, Klegeris A. Inflammation and insulin/IGF-1 resistance as the possible link between obesity and neurodegeneration. J Neuroimmunol. 2014;273:8-21.
20. Sobesky JL, Barrientos RM, De May HS, Thompson BM, Weber MD, Watkins LR, Maier SF. High-fat diet consumption disrupts memory and primes elevations in hippocampal IL-1β, an effect that can be prevented with dietary reversal or IL-1 receptor antagonism. Brain Behav Immun. 2014;42:22-32.
21. Guri AJ, Hontecillas R, Si H, Liu D, Bassaganya-Riera J. Dietary abscisic acid ameliorates glucose tolerance and obesity-related inflammation in db/db mice fed high-fat diets. Clin Nutr. 2007;26:107-16.
22. Ropelle ER, Flores MB, Cintra DE, Rocha GZ, Pauli JR, Morari J, de Souza CT, Moraes JC, Prada PO, Guadagnini D, Marin RM, Oliveira AG, Augusto TM, Carvalho HF, Velloso LA, Saad MJA, Carvalheira JBC. IL-6 and IL-10 anti-inflammatory activity links exercise to hypothalamic insulin and leptin sensitivity through IKKbeta and ER stress inhibition. PLoS Biol. 2010;8(8). doi:10.1371/journal.pbio.1000465.
23. Gaskin S, Tardif M, Cole E, Piterkin P, Kayello L, Mumby DG. Object familiarization and novel-object preference in rats. Behav Processes. 2010;83:61-71.
24. André C, Dinel A-L, Ferreira G, Layé S, Castanon N. Diet-induced obesity progressively alters cognition, anxiety-like behavior and lipopolysaccharide-induced depressive-like behavior: focus on brain indoleamine 2,3-dioxygenase activation. Brain Behav Immun. 2014;41:10-21.
25. Durgbanshi A, Arbona V, Pozo O, Miersch O, Sancho JV, Gómez-Cadenas A. Simultaneous determination of multiple phytohormones in plant extracts by liquid chromatography-electrospray tandem mass spectrometry. J Agric Food Chem. 2005;53:8437-42.
26. Cui Y, Shu Y, Zhu Y, Shi Y, Le G. High-fat diets impair spatial learning of mice in the Y-maze paradigm: ameliorative potential of α-lipoic acid. J Med Food. 2012;15:713-7.
27. Edwards LM, Murray AJ, Holloway CJ, Carter EE, Kemp GJ, Codreanu I, Brooker H, Tyler DJ, Robbins PA, Clarke K. Short-term consumption of a high-fat diet impairs whole-body efficiency and cognitive function in sedentary men. FASEB J. 2011;25:1088-96.
28. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, Kohsaka S. Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res. 1998;57:1-9.
29. De Souza CT, Araujo EP, Bordin S, Ashimine R, Zollner RL, Boschero AC, Saad MJA, Velloso LA. Consumption of a fat-rich diet activates a proinflammatory response and induces insulin resistance in the hypothalamus. Endocrinology. 2005;146:4192-9.
30. Wang X, Ge A, Cheng M, Guo F, Zhao M, Zhou X, Liu L, Yang N. Increased hypothalamic inflammation associated with the susceptibility to obesity in rats exposed to high-fat diet. Exp Diabetes Res. 2012;2012:847246.
31. Velloso LA, Schwartz MW. Altered hypothalamic function in diet-induced obesity. Int J Obes (Lond). 2011;35:1455-65.
32. Liu Z, Patil IY, Jiang T, Sancheti H, Walsh JP, Stiles BL, Yin F, Cadenas E. High-fat diet induces hepatic insulin resistance and impairment of synaptic plasticity. PLoS One. 2015;10:e0128274.
33. Petrov D, Pedrós I, Artiach G, Sureda FX, Barroso E, Pallàs M, Casadesús G, Beas-Zarate C, Carro E, Ferrer I, Vazquez-Carrera M, Folch J, Camins A. High-fat diet-induced deregulation of hippocampal insulin signaling and mitochondrial homeostasis deficiences contribute to Alzheimer disease pathology in rodents. Biochim Biophys Acta. 1852;2015:1687-99.
34. Magnusson KR, Hauck L, Jeffrey BM, Elias V, Humphrey A, Nath R, Perrone A, Bermudez LE. Relationships between diet-related changes in the gut microbiome and cognitive flexibility. Neuroscience. 2015;300:128-40.
35. Guri AJ, Hontecillas R, Ferrer G, Casagran O, Wankhade U, Noble AM, Eizirik DL, Ortis F, Cnop M, Liu D, Si H, Bassaganya-Riera J. Loss of PPAR gamma in immune cells impairs the ability of abscisic acid to improve insulin sensitivity by suppressing monocyte chemoattractant protein-1 expression and macrophage infiltration into white adipose tissue. J Nutr Biochem. 2008;19:216-28.
36. Kamara K, Eskay R, Castonguay T. High-fat diets and stress responsivity. Physiol Behav. 1998;64:1-6.
37. Cruces J, Venero C, Pereda-Pérez I, De la Fuente M. A higher anxiety state in old rats after social isolation is associated to an impairment of the immune response. J Neuroimmunol. 2014;277:18-25.
38. Turner PV, Pekow C, Vasbinder MA, Brabb T. Administration of substances to laboratory animals: equipment considerations, vehicle selection, and solute preparation. J Am Assoc Lab Anim Sci. 2011;50:614-27.
39. McNeilly AD, Williamson R, Sutherland C, Balfour DJK, Stewart CA. High fat feeding promotes simultaneous decline in insulin sensitivity and cognitive performance in a delayed matching and non-matching to position task. Behav Brain Res. 2011;217:134-41.
40. McNay EC, Ong CT, McCrimmon RJ, Cresswell J, Bogan JS, Sherwin RS. Hippocampal memory processes are modulated by insulin and high-fat-induced insulin resistance. Neurobiol Learn Mem. 2010;93:546-53.
41. Valladolid-Acebes I, Stucchi P, Cano V, Fernández-Alfonso MS, Merino B, Gil-Ortega M, Fole A, Morales L, Ruiz-Gayo M, Del Olmo N. High-fat diets impair spatial learning in the radial-arm maze in mice. Neurobiol Learn Mem. 2011;95:80-5.
42. Bassaganya-Riera J, Guri AJ, Lu P, Climent M, Carbo A, Sobral BW, Horne WT, Lewis SN, Bevan DR, Hontecillas R. Abscisic acid regulates inflammation via ligand-binding domain-independent activation of peroxisome proliferator-activated receptor gamma. J Biol Chem. 2011;286:2504-16.
43. Bassaganya-Riera J, Guri AJ, Hontecillas R. Treatment of obesity-related complications with novel classes of naturally occurring PPAR agonists. J Obes. 2011;2011:897894.
44. Kariharan T, Nanayakkara G, Parameshwaran K, Bagasrawala I, Ahuja M, Abdel-Rahman E, Amin AT, Dhanasekaran M, Suppiramaniam V, Amin RH. Central activation of PPAR-gamma ameliorates diabetes induced cognitive dysfunction and improves BDNF expression. Neurobiol Aging. 2015;36:1451-61.
45. Nenov MN, Tempia F, Denner L, Dineley KT, Laezza F. Impaired firing properties of dentate granule neurons in an Alzheimer's disease animal model are rescued by PPARγ agonism. J Neurophysiol. 2015;113:1712-26.
46. Olton D, Markowska A, Voytko ML, Givens B, Gorman L, Wenk G. Basal forebrain cholinergic system: a functional analysis. Adv Exp Med Biol. 1991;295:353-72.
47. DEMBER WN, FOWLER H. Spontaneous alternation behavior. Psychol Bull. 1958;55:412-28.
48. Bodrato N, Franco L, Fresia C, Guida L, Usai C, Salis A, Moreschi I, Ferraris C, Verderio C, Basile G, Bruzzone S, Scarfì S, De Flora A, Zocchi E. Abscisic acid activates the murine microglial cell line N9 through the second messenger cyclic ADP-ribose. J Biol Chem. 2009;284:14777-87.
49. Jiang SX, Benson CL, Zaharia LI, Abrams SR, Hou ST. Abscisic acid does not evoke calcium influx in murine primary microglia and immortalised murine microglial BV-2 and N9 cells. Biochem Biophys Res Commun. 2010;401:435-9.
50. Neumann H, Kotter MR, Franklin RJM. Debris clearance by microglia: an essential link between degeneration and regeneration. Brain. 2009;132(Pt 2):288-95.
51. Smith JA, Das A, Ray SK, Banik NL. Role of pro-inflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res Bull. 2012;87:10-20.
52. Thaler JP, Yi C-X, Schur EA, Guyenet SJ, Hwang BH, Dietrich MO, Zhao X, Sarruf DA, Izgur V, Maravilla KR, Nguyen HT, Fischer JD, Matsen ME, Wisse BE, Morton GJ, Horvath TL, Baskin DG, Tschöp MH, Schwartz MW. Obesity is associated with hypothalamic injury in rodents and humans. J Clin Invest. 2012;122:153-62.
53. Lozano D, Gonzales-Portillo GS, Acosta S, de la Pena I, Tajiri N, Kaneko Y, Borlongan CV. Neuroinflammatory responses to traumatic brain injury: etiology, clinical consequences, and therapeutic opportunities. Neuropsychiatr Dis Treat. 2015;11:97-106.
54. Madinier A, Bertrand N, Mossiat C, Prigent-Tessier A, Beley A, Marie C, Garnier P. Microglial involvement in neuroplastic changes following focal brain ischemia in rats. PLoS One. 2009;4:e8101.
55. Bouvier DS, Murai KK. Synergistic actions of microglia and astrocytes in the progression of Alzheimer's disease. J Alzheimers Dis. 2015;45:1001-14.
56. Perry VH, Holmes C. Microglial priming in neurodegenerative disease. Nat Rev Neurol. 2014;10:217-24.
57. Riazi K, Galic M a, Kuzmiski JB, Ho W, Sharkey K a, Pittman QJ. Microglial activation and TNFalpha production mediate altered CNS excitability following peripheral inflammation. Proc Natl Acad Sci U S A. 2008;105:17151-6.
58. Najjar S, Pearlman DM. Neuroinflammation and white matter pathology in schizophrenia: systematic review. Schizophr Res. 2015;161:102-12.
59. Rial D, Lemos C, Pinheiro H, Duarte JM, Gonçalves FQ, Real JI, Prediger RD, Gonçalves N, Gomes CA, Canas PM, Agostinho P, Cunha RA. Depression as a glial-based synaptic dysfunction. Front Cell Neurosci. 2015;9:521.
60. McLarnon JG. Microglial chemotactic signaling factors in Alzheimer's disease. Am J Neurodegener Dis. 2012;1:199-204.