Momordica charantia (bitter melon) attenuates high-fat diet-associated oxidative stress and neuroinflammation

Journal of Neuroinflammation

Volumn 8, Issue , 2011, Pages

  Nerurkar, Pratibha V ^a   Johns, Lisa M ^a   Buesa, Lance M ^a   Kipyakwai, Gideon ^a   Volper, Esther ^a   Sato, Ryuei ^a   Shah, Pranjal ^a   Feher, Domonkos ^b   Williams, Philip G ^b   Nerurkar, Vivek R ^a  

^a UNIVERSITY OF HAWAII   (United States)

^b John A Burns School of Medicine University of Hawaii at Manoa ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; CD11B ANTIGEN; CELL PROTEIN; EVANS BLUE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTATHIONE; GLUTATHIONE PEROXIDASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 16; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 22; IONIZED CALCIUM BINDING ADAPTER MOLECULE 1; MESSENGER RNA; NUCLEAR FACTOR KAPPA B1; PHOSPHATE BUFFERED SALINE; PROTEIN S100B; SIRTUIN 1; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG; ANTIOXIDANT; BIOLOGICAL MARKER; FORKHEAD TRANSCRIPTION FACTOR; FOXO1 PROTEIN, MOUSE; NEUROPROTECTIVE AGENT; PHENOL DERIVATIVE; PLANT EXTRACT; SIRT1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN PERFUSION; BRAIN TISSUE; CONTROLLED STUDY; CYTOKINE RELEASE; DIET SUPPLEMENTATION; ENDOPLASMIC RETICULUM STRESS; ENZYMATIC ASSAY; FEMALE; FUNCTIONAL FOOD; GENE EXPRESSION REGULATION; GLIA CELL; IMMUNOASSAY; LIPID DIET; MICROARRAY ANALYSIS; MOMORDICA CHARANTIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OBESITY; OXIDATIVE STRESS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TREATMENT DURATION; WESTERN BLOTTING; ANIMAL; BRAIN; C57BL MOUSE; CHEMISTRY; DEGENERATIVE DISEASE; DRUG EFFECT; ENCEPHALITIS; FAT INTAKE; METABOLISM; PATHOPHYSIOLOGY; RANDOMIZATION;

ANIMALS; ANTIOXIDANTS; BIOLOGICAL MARKERS; BLOOD-BRAIN BARRIER; BRAIN; CATALASE; DIETARY FATS; DIETARY SUPPLEMENTS; ENCEPHALITIS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GLUTATHIONE PEROXIDASE; MICE; MICE, INBRED C57BL; MICROARRAY ANALYSIS; MOMORDICA CHARANTIA; NEURODEGENERATIVE DISEASES; NEUROPROTECTIVE AGENTS; OBESITY; OXIDATIVE STRESS; PHENOLS; PLANT EXTRACTS; RANDOM ALLOCATION; SIRTUIN 1; SUPEROXIDE DISMUTASE;

EID: 79957807811     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-8-64     Document Type: Article

References (72)

1. Bruce-Keller AJ, Keller JN, Morrison CD. Obesity and vulnerability of the CNS. Biochim Biophys Acta 2008,
2. Oh-I S, Thaler JP, Ogimoto K, Wisse BE, Morton GJ, Schwartz MW. Central administration of interleukin-4 exacerbates hypothalamic inflammation and weight gain during high-fat feeding. Am J Physiol Endocrinol Metab 2010, 299:E47-E53. 10.1152/ajpendo.00026.2010, 20371733.
3. De Souza CT, Araujo EP, Bordin S, Ashimine R, Zollner RL, Boschero AC, Saad MJ, Velloso LA. Consumption of a fat-rich diet activates a proinflammatory response and induces insulin resistance in the hypothalamus. Endocrinology 2005, 146:4192-4199. 10.1210/en.2004-1520, 16002529.
4. Volkow ND, Wang GJ, Telang F, Fowler JS, Goldstein RZ, Alia-Klein N, Logan J, Wong C, Thanos PK, Ma Y, Pradhan K. Inverse Association Between BMI and Prefrontal Metabolic Activity in Healthy Adults. Obesity (Silver Spring) 2009, 17:60-65.
5. Ward MA, Carlsson CM, Trivedi MA, Sager MA, Johnson SC. The effect of body mass index on global brain volume in middle-aged adults: a cross sectional study. BMC Neurol 2005, 5:23-31. 10.1186/1471-2377-5-23, 1325254, 16321166.
6. Gustafson D, Steen B, Skoog I. Body mass index and white matter lesions in elderly women. An 18-year longitudinal study. Int J Psychogeriatr 2004, 16:327-336.
7. Gustafson D, Lissner L, Bengtsson C, Björkelund C, Skoog I. A 24-year follow-up of body mass index and cerebral atrophy. Neurology 2004, 63:1876-1881.
8. Mrak RE. Alzheimer-type neuropathological changes in morbidly obese elderly individuals. Clinical Neuropathology 2009, 28:40-45.
9. Jurdak N, Lichtenstein AH, Kanarek RB. Diet-induced obesity and spatial cognition in young male rats. Nutr Neurosci 2008, 11:48-54. 10.1179/147683008X301333, 18510803.
10. Wu A, Molteni R, Ying Z, Gomez-Pinilla F. A saturated-fat diet aggravates the outcome of traumatic brain injury on hippocampal plasticity and cognitive function by reducing brain-derived neurotrophic factor. Neuroscience 2003, 119:365-375. 10.1016/S0306-4522(03)00154-4, 12770552.
11. Studzinski C, Li F, Bruce-Keller A, Fernandez-Kim S, Zhang L, Weidner A, Markesbery W, Murphy M, Keller J. Effects of shrot-term Western diet on cerebral oxidative stress and diabetes related factors in APP X PS1 knock-in mice. J Neurochem 2009, 108:860-866. 10.1111/j.1471-4159.2008.05798.x, 2748316, 19046405.
12. Wu A, Ying Z, Gomez-Pinilla F. Oxidative stress modulates Sir2alpha in rat hippocampus and cerebral cortex. Eur J Neurosci 2006, 23:2573-2580. 10.1111/j.1460-9568.2006.04807.x, 16817860.
13. Yehuda S, Rabinovitzi S, Mostofsky D. Mediation of cognitive function by high fat diet following stress and inflammation. Nutritional Neuroscience 2005, 309:309-315.
14. Willcox BJ, Willcox DC, Ferrucci L. Secrets of healthy aging and longevity from exceptional survivors around the globe: lessons from octogenarians to supercentenarians. J Gerontol A Biol Sci Med Sci 2008, 63:1181-1185.
15. Willcox DC, Willcox BJ, Shimajiri S, Kurechi S, Suzuki M. Aging gracefully: a retrospective analysis of functional status in Okinawan centenarians. Am J Geriatr Psychiatry 2007, 15:252-256. 10.1097/JGP.0b013e31803190cc, 17322136.
16. Abascal K, Yarnell E. Using bitter melon to treat diabetes. Alternative and Complemetary Medicine 2005, 179-184.
17. Chen Q, Chan LL, Li ET. Bitter melon (Momordica charantia) reduces adiposity, lowers serum insulin and normalizes glucose tolerance in rats fed a high fat diet. J Nutr 2003, 133:1088-1093.
18. Shih CC, Lin CH, Lin WL. Effects of Momordica charantia on insulin resistance and visceral obesity in mice on high-fat diet. Diabetes Res Clin Pract 2008, 81:134-143. 10.1016/j.diabres.2008.04.023, 18550200.
19. Nerurkar PV, Lee YK, Motosue M, Adeli K, Nerurkar VR. Momordica charantia (bitter melon) reduces plasma apolipoprotein B-100 and increases hepatic insulin receptor substrate and phosphoinositide-3 kinase interactions. Br J Nutr 2008, 100:751-759.
20. Raza H, Ahmed I, John A, Sharma AK. Modulation of xenobiotic metabolism and oxidative stress in chronic streptozotocin-induced diabetic rats fed with Momordica charantia fruit extract. J Biochem Mol Toxicol 2000, 14:131-139. 10.1002/(SICI)1099-0461(2000)14:3<131::AID-JBT2>3.0.CO;2-Q, 10711628.
21. Lin J-Y, Tang C-Y. Strawberry, loquat, mulberry, and bitter melon juices exhibit prophylactic effects on LPS-induced inflammation using murine peritoneal macrophages. Food Chemistry 2008, 107:1587-1596.
22. Yao Y, Tsirka SE. Truncation of monocyte chemoattractant protein 1 by plasmin promotes blood-brain barrier disruption. Journal of Cell Science 2011, 124:1486-1495. 10.1242/jcs.082834, 21486949.
23. Man S-M, Ma Y-R, Shang D-S, Zhao W-D, Li B, Guo D-W, Fang W-G, Zhu L, Chen Y-H. Peripheral T cells overexpress MIP-1α to enhance its transendothelial migration in Alzheimer's disease. Neurobiology of Aging 2007, 28:485-496. 10.1016/j.neurobiolaging.2006.02.013, 16600437.
24. Louboutin J-P, Chekmasova A, Marusich E, Agrawal L, Strayer DS. Role of CCR5 and its ligands in the control of vascular inflammation and leukocyte recruitment required for acute excitotoxic seizure induction and neural damage. The FASEB Journal 2011, 25:737-753. 10.1096/fj.10-161851, 20940264.
25. Uyama O, Okamura N, Yanase M, Narita M, Kawabata K, Sugita M. Quantitative evaluation of vascular permeability in the gerbil brain after transient ischemia using Evans blue fluorescence. J Cereb Blood Flow Metab 1988, 8:282-284. 10.1038/jcbfm.1988.59, 3343300.
26. Chen X, Ghribi O, Geiger JD. Caffeine protects against disruptions of the blood-brain barrier in animal models of Alzheimer's and Parkinson's diseases. J Alzheimers Dis 2010, 20(Suppl 1):127-141.
27. Verma S, Ziegler K, Ananthula P, Co JK, Frisque RJ, Yanagihara R, Nerurkar VR. JC virus induces altered patterns of cellular gene expression: interferon-inducible genes as major transcriptional targets. Virology 2006, 345:457-467. 10.1016/j.virol.2005.10.012, 16297951.
28. Hissin PJ, Hilf R. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal Biochem 1976, 74:214-226. 10.1016/0003-2697(76)90326-2, 962076.
29. Lim ST, Dragull K, Tang CS, Bittenbender HC, Efird JT, Nerurkar PV. Effects of kava alkaloid, pipermethystine, and kavalactones on oxidative stress and cytochrome P450 in F-344 rats. Toxicol Sci 2007, 97:214-221. 10.1093/toxsci/kfm035, 17329236.
30. Liebrich M, Guo L-H, Schluesener HJ, Schwab JM, Dietz K, Will BE, Meyermann R. Expression of interleukin-16 by tumor-associated macrophages/activated microglia in high-grade astrocytic brain tumors. Arch Immunol Ther Exp 2007, 55:41-47.
31. Kebir H, Kreymborg K, Ifergan I, Dodelet-Devillers A, Cayrol R, Bernard M, Giuliani F, Arbour N, Becher B, Prat A. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nature Med 2007, 13:1173-1175. 10.1038/nm1651, 17828272.
32. Takechi R, Galloway S, Pallebage-Gamarallage MMS, Lam V, Mamo JCL. Dietary fats, cerebrovasculature integrity and Alzheimer's disease risk. Progress in Lipid Res 2010, 49:159-170.
33. Velloso LA. The brain is the conductor: diet-induced inflammation overlapping physiological control of body mass and metabolism. Arq Bras Endocrinol Metab 2009, 53/2:151-158.
34. Baran S, Cambell A, Kleen J, Foltz C, Wright R, Diamond D, Conrad C. Combination of high fat diet and chronic stress retracts hippocampal dendrites. Neuroreport 2005, 16:39-43. 10.1097/00001756-200501190-00010, 1363787, 15618887.
35. Lindqvist A, Mohapel P, Bouter B, Frielingsdorf H, Pizzo D, Brundin P, Erlanson-Albertsson C. High-fat diet impairs hippocampal neurogenesis in male rats. Eur J Neurol 2006, 13:1385-1388. 10.1111/j.1468-1331.2006.01500.x, 17116226.
36. Zhang X, Zhang G, Zhang H, Karin M, Bai H, Cai D. Hypothalamic IKKbeta/NF-kappaB and ER stress link overnutrition to energy imbalance and obesity. Cell 2008, 135:61-73. 10.1016/j.cell.2008.07.043, 2586330, 18854155.
37. Granholma A-C, Bimonte-Nelsonb HA, Moorea AB, Nelsona ME, Freemana LR, Sambamurtia K. Effects of a Saturated Fat and High Cholesterol Diet on Memory and Hippocampal Morphology in the Middle-Aged Rat. J Alzheimers Dis 2008, 14:133-145. 2670571, 18560126.
38. Thaler JP, Schwartz MW. Inflammation and obesity pathogenesis: The hypothalamus heats up. Endocrinology 2010,
39. Krause DL, M̈uller N. Neuroinflammation, Microglia and Implications for Anti-Inflammatory Treatment in Alzheimer's Disease. International Journal of Alzheimer's Disease 2010,
40. Greenwood CE, Winocur G. High-fat diets, insulin resistance and declining cognitive function. Neurobiol Aging 2005, 26:42-45. 10.1016/j.neurobiolaging.2005.08.017, 16257476.
41. Laye S. Polyunsaturated fatty acids, neuroinflammation and well being. Prostaglandins, LeukotrienesandEssentialFattyAcids 2010, 82:295-303.
42. Stolp HB, Dziegielewska KM. Review: Role of developmental inflammation and blood-brain barrier dysfunction in neurodevelopmental and neurodegenerative diseases. Neuropathology and Applied Neurobiology 2009, 35:132-146. 10.1111/j.1365-2990.2008.01005.x, 19077110.
43. Krause DL, Miller N. Neuroinflammation, Microglia and Implications for Anti-Inflammatory Treatment in Alzheimer's Disease. International Journal of Alzheimer's Disease 2010,
44. Schwab JM, Nguyen TD, Meyermann R, Schluesener HJ. Human focal cerebral infarctions induce differential lesional interleukin-16 (IL-16) expression confined to infiltrating granulocytes, 1 CD8 T-lymphocytes and activated microglia / macrophages. Journal of Neuroimmunology 2001, 114:232-241. 10.1016/S0165-5728(00)00433-1, 11240037.
45. Malik ZA, Singh M, Sharma PL. Neuroprotective effect of Momordica charantia in global cerebral ischemia and reperfusion induced neuronal damage in diabetic mice. J Ethnopharmacol 2010,
46. Shin JH, Shin DW, Noh M. Interleukin-17A inhibits adipocyte differentiation in human mesenchymal stem cells and regulates pro-inflammatory responses in adipocytes. Biochemical Pharmacology 2009, 77:1835-1844. 10.1016/j.bcp.2009.03.008, 19428338.
47. Fabry Z, Schreiber HA, Harris MG, Sandor M. Sensing the microenvironment of the central nervous system: immune cells in the central nervous system and their pharmacological manipulation. Curr Opin Pharmacol 2008, 8:496-507. 10.1016/j.coph.2008.07.009, 2614337, 18691672.
48. Liu L, Yang P, He H, Lin X, Jiang L, Chi W. Leptin increases in Vogt-Koyanagi-Harada (VKH) disease and promotes cell proliferation and inflammatory cytokine secretion. Br J Ophthalmol 2008, 92:557-561. 10.1136/bjo.2007.128769, 18245271.
49. Murphy AC, Lalor SJ, Lynch MA, Mills KHG. Infiltration of Th1 and Th17 cells and activation of microglia in the CNS during the course of experimental autoimmune encephalomyelitis. Brain, Behavior, and Immunity 2010, 24:641-651. 10.1016/j.bbi.2010.01.014, 20138983.
50. Peron JPS, Yang K, Chen M-L, Brandao WN, Basso AS, Commondaro AG, Weiner HL, Rozzo LV. Oral tolerance reduces Th17 cells as well as the overall inflammation in the central nervous system of EAE mice. J Neuroimmunology 2010,
51. Wekerle H, Sun D, Oropeza-Wekerle RL, Meyermann R. Immune reactivity in the nervous system: modulation of T-lymphocyte activation by glial cells. J Exp Biol 1987, 132:43-57.
52. Winer S, Palster G, Chan Y, Tsui H, Engleman E, Winer D, Dosch H-M. Obesity predisposes to Th17 bias. Eur J Immunol 2009, 39:2629-2635. 10.1002/eji.200838893, 19662632.
53. Miller AM, Asquith DL, Hueber AJ, Anderson LA, Holmes WM, McKenzie AN, Xu D, Sattar N, McInnes IB, Liew FY. Interleukin-33 induces protective effects in adipose tissue inflammation during obesity in mice. Circ Res 2010, 107:650-658. 10.1161/CIRCRESAHA.110.218867, 20634488.
54. Laske C, Stransky E, Hoffmann N, Maetzler W, Straten G, Eschweiler GW, Leyhe T. Macrophage colony-stimulating factor (M-CSF) in plasma and CSF of patients with mild cognitive impairment and Alzheimer's disease. Curr Alzheimer Res 2010, 7:409-414. 10.2174/156720510791383813, 20455868.
55. Engelhardt B. Molecular mechanisms involved in T cell migration across the blood-brain barrier. J Neural transm 2006, 113:477-485. 10.1007/s00702-005-0409-y, 16550326.
56. Wang D, Zhao Y, Wang G, Sun B, Kong Q, Zhao K, Zhang Y, Wang J, Liu Y, Mu L, et al. IL-17 potentiates neuronal injury induced by oxygen-glucose deprivation and affects neuronal IL-17 receptor expression. Journal of Neuroimmunology 2009, 212:17-25. 10.1016/j.jneuroim.2009.04.007, 19457561.
57. Delgado M, Varela N, Gonzalez-Rey E. Vasoactive intestinal peptide protects against beta-amyloid-induced neurodegeneration by inhibiting microglia activation at multiple levels. Glia 2008, 56:1091-1103. 10.1002/glia.20681, 18442091.
58. Wu A, Ying Z, Gomez-Pinilla F. The interplay between oxidative stress and brain-derived neurotrophic factor modulates the outcome of a saturated fat diet on synaptic plasticity and cognition. Euro J Neurosci 2004, 19:1699-1707.
59. Ray SD, Lam TS, Rotollo JA, Phadke S, Patel C, Dontabhaktuni A, Mohammad S, Lee H, Strika S, Dobrogowska A, et al. Oxidative stress is the master operator of drug and chemically-induced programmed and unprogrammed cell death: Implications of natural antioxidants in vivo. Biofactors 2004, 21:223-232. 10.1002/biof.552210144, 15630201.
60. Sathishsekar D, Subramanian S. Antioxidant properties of Momordica Charantia (bitter gourd) seeds on Streptozotocin induced diabetic rats. Asia Pac J Clin Nutr 2005, 14:153-158.
61. Hatayama T, Yamagishi N, Moinobe E, Sakai K. Role of hsp105 in Protection against Stress-Induced Apoptosis in Neuronal PC12 Cells. Biochem Biophys Res Commun 2001, 288:528-534. 10.1006/bbrc.2001.5802, 11676475.
62. Ohtsuka K, Siuzuki T. Roles of molecular chaperones in the nervous system. Brain Research Bulletin 2000, 53:141-146. 10.1016/S0361-9230(00)00325-7, 11044589.
63. Salminen A, Ojala J, Huuskonen J, Kauppinen A, Suuronen T, Kaarniranta K. Interaction of aging-associated signaling cascades: inhibition of NF-kappaB signaling by longevity factors FoxOs and SIRT1. Cell Mol Life Sci 2008, 65:1049-1058. 10.1007/s00018-008-7461-3, 18193389.
64. Gan L, Mucke L. Paths of convergence: sirtuins in aging and neurodegeneration. Neuron 2008, 58:10-14. 10.1016/j.neuron.2008.03.015, 18400158.
65. Chen D, Steele AD, Hutter G, Bruno J, Govindarajan A, Easlon E, Lin SJ, Aguzzi A, Lindquist S, Guarente L. The role of calorie restriction and SIRT1 in prion-mediated neurodegeneration. Exp Gerontol 2008, 43:1086-1093. 10.1016/j.exger.2008.08.050, 2735260, 18799131.
66. Yang Y, Hubbard BP, Sinclair DA, Tong Q. Characterization of murine SIRT3 transcript variants and corresponding protein products. J Cell Biochem 2010,
67. Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y, Tran H, Ross SE, Mostoslavsky R, Cohen HY, et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 2004, 303:2011-2015. 10.1126/science.1094637, 14976264.
68. Kobayashi Y, Furukawa-Hibi Y, Chen C, Horio Y, Isobe K, Ikeda K, Motoyama N. SIRT1 is critical regulator of FOXO-mediated transcription in response to oxidative stress. Int J Mol Med 2005, 16:237-243.
69. Zheng WH, Kar S, Quirion R. Insulin-like growth factor-1-induced phosphorylation of transcription factor FKHRL1 is mediated by phosphatidylinositol 3-kinase/Akt kinase and role of this pathway in insulin-like growth factor-1-induced survival of cultured hippocampal neurons. Mol Pharmacol 2002, 62:225-233. 10.1124/mol.62.2.225, 12130673.
70. Maiese K, Chong ZZ, Shang YC. "Sly as a FOXO": new paths with Forkhead signaling in the brain. Curr Neurovasc Res 2007, 4:295-302. 10.2174/156720207782446306, 2570708, 18045156.
71. Manabe M, Takenaka R, Nakasa T, Okinaka O. Induction of anti-inflammatory responses by dietary Momordica charantia L. (bitter gourd). Biosci Biotechnol Biochem 2003, 67:2512-2517. 10.1271/bbb.67.2512, 14730127.
72. Horax R, Hettiarachchy N, Chen P. Extraction, quantification, and antioxidant activities of phenolics from pericarp and seeds of bitter melons (Momordica charantia) harvested at three maturity stages (Immature, mature, and ripe). J Agri Food Chem 2010, 58:4428-4433.