Protective effects of geraniol (a monoterpene) in a diabetic neuropathy rat model: Attenuation of behavioral impairments and biochemical perturbations

Journal of Neuroscience Research

Volumn 92, Issue 9, 2014, Pages 1205-1216

  Prasad, Sathya N ^a   Muralidhara, Murali ^a  

^a Central Food Technological Research Institute (CFTRI)   (India)

Author keywords

Behavioral tests; Brain regions; Diabetic rat; Mitochondria; Oxidative stress; Sciatic nerve

Indexed keywords

ACETYLCHOLINESTERASE; CALCIUM; CARBONYL DERIVATIVE; CITRATE SYNTHASE; DOPAMINE; GERANIOL; HYDROPEROXIDE; MALONALDEHYDE; NITRITE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROSE OIL; STREPTOZOCIN; SUCCINATE DEHYDROGENASE; SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE; ANTIDIABETIC AGENT; HYDROGEN PEROXIDE; OXIDOREDUCTASE; TERPENE;

ADULT; ANIMAL EXPERIMENT; ARTICLE; ATTENUATION; BEHAVIOR DISORDER; BODY WEIGHT; BRAIN CORTEX; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; CYTOSOL; DIABETIC NEUROPATHY; DIET SUPPLEMENTATION; DRUG EFFICACY; ENZYME ACTIVITY; LATENT PERIOD; LEMON; MALE; MITOCHONDRION; MOTOR PERFORMANCE; NEUROPROTECTION; NITROSATIVE STRESS; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SCIATIC NERVE; SENSORY SYSTEM; SPICE; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; TAIL FLICK TEST; ANIMAL; BRAIN; COMPLICATION; DIABETIC NEUROPATHIES; DISEASE MODEL; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; HYPERALGESIA; LIPID PEROXIDATION; METABOLISM; ORAL DRUG ADMINISTRATION; PATHOLOGY; PSYCHOMOTOR DISORDERS; WISTAR RAT;

ADMINISTRATION, ORAL; ANIMALS; BODY WEIGHT; BRAIN; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEUROPATHIES; DISEASE MODELS, ANIMAL; HYDROGEN PEROXIDE; HYPERALGESIA; HYPOGLYCEMIC AGENTS; LIPID PEROXIDATION; MALE; MALONDIALDEHYDE; OXIDOREDUCTASES; PSYCHOMOTOR DISORDERS; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; SCIATIC NERVE; TERPENES;

EID: 84904287402     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23393     Document Type: Article

References (69)

1. Aebi H. 1984. Catalase in vitro. Methods Enzymol 105:121-126.
2. Ahmad ST, Arjuman W, Seth A, Nafees S, Rashid S, Ali N, Sultana S. 2011. Preclinical renal cancer chemopreventive efficacy of geraniol by modulation of multiple molecular pathways. Toxicology 290:69-81.
3. Andersen H. 2012. Motor dysfunctions in diabetes. Diabetes Metab Res Rev 28:89-92.
4. Attal N, Jazat F, Kayser V, Guilbaud G. 1990. Further evidence for pain related behaviors in model of unilateral peripheral mononeuropathy. Pain 41:235-251.
5. Berridge MV, Tans AS. 1993. Characterization of the cellular reduction of 3-(4, 5-dimethyl thiazol-2-yl)-2, 5-diphenyltetrazoliumbromide (MTT): subcellular localization, substrate dependence and involvement of mitochondrial electron transport in MTT reduction. Arch Biochem Biophys 303:474-482.
6. Cardozo MT, de Conti S, Ong TP, Scolastici C, Purgatto E, Horst MA, Bassoli BK, Moreno FS. 2011. Chemopreventive effects of β-ionone and geraniol during rat hepatocarcinogenesis promotion: distinct actions on cell proliferation, apoptosis, HMGCoA reductase and RhoA. J Nutr Biochem 22:130-135.
7. Carlberg I, Mannervick FT, Dryle DD. 1985. Glutathione reductase. Methods Enzymol 113:489-490.
8. Ceriello A. 2006. Controlling oxidative stress as a novel molecular approach to protecting the vascular wall in diabetes. Curr Opin Lipidol 17:510-518.
9. Chandrashekar KN, Muralidhara. 2008. Oxidative alternations induced by D-aspartic acid in prepubertal rat testis in vitro: a mechanistic study. Theriogenology 70:97-104.
10. Chen W, Viljoen AM. 2010. Geraniol-a review of a commercially important fragrance material. S Afr J Bot 76:643-651.
11. Chowdhury SKR, Smith DR, Fernyhough P. 2013. The role of aberrant mitochondrial bioenergetics in diabetic neuropathy. Neurobiol Dis 51:56-65.
12. Dalpiaz A, Filosa K, de Caprariis P, Conte G, Bortolotti F, Biondi C, Scatturin A, Prasad PD, Pawan B. 2007. Molecular mechanism involved in the transport of a prodrug dopamine glycosyl conjugate. Int J Pharmacol 336:133-139.
13. Dang YH, Zhao Y, Xing B, Zhao XJ, Huo FQ, Tang JS, Qu CL, Chen T. 2010. Pain mechanisms and sensory neuroscience: the role of dopamine receptors in ventrolateral orbital cortex-evoked anti-nociception in a rat model of neuropathic pain. Neuroscience 169:1872-1880.
14. de Arriba SG, Krugel U, Regenthal R, Vissiennon Z, Verdaguer E, Lewerenz A, Garcia-Jorda E, Pallas M, Camins A, Munch G, Nieber K, Allgaier C. 2006. Carbonyl stress and NMDA receptor activation contribute to methylglyoxal neurotoxicity. Free Radic Biol Med 40:779-790.
15. Dumont MF, Beal M. 2011. Neuroprotective strategies involving ROS in Alzheimer disease. Free Radic Biol Med 51:1014-26.
16. Edwards JL, Vincent AM, Cheng HT, Feldman EL. 2008. Diabetic neuropathy: mechanisms to management. Pharmacol Ther 120:1-34.
17. Ellmann GE, Courtney KD, Anderson V, Featherstone RM. 1961. A new colorimetric etermination of acetyl cholinesterase activity. Biochem Pharmacol 7:88-95.
18. Fernyhough P, Chowdhury SKR, Schmidt RE. 2010. Mitochondrial stress and pathogenesis of diabetic neuropathy. Expert Rev Endocrinol Metab 5:39-49.
19. Gul H, Yildiz O, Dogrul A, Yesilyurt O, Isimer A. 2000. The interaction between IL-1beta and morphine: possible mechanism of the deficiency of morphine-induced analgesia in diabetic mice. Pain 89:39-45.
20. Guthenberg C, Alin P, Mannervik B. 1985. Glutothione transferase from rat testis. Methods Enzymol 113:507-510.
21. Howes MJ, Houghton PJ. 2003. Plants used in Chinese and Indian traditional medicine for improvement of memory and cognitive function. Pharmacol Biochem Behav 75:513-527.
22. Jin QH, He HY, Shi YF, Lu H, Zhang X-J. 2004. Overexpression of acetylcholinesterase inhibited cell proliferation and promoted apoptosis in NRK cells. Acta Pharmacol Sin 25:1013-1021.
23. Kamboj SS, Sandhir R. 2011. Protective effect of N-acetylcysteine supplementation on mitochondrial oxidative stress and mitochondrial enzymes in cerebral cortex of streptozotocin- treated rats. Mitochondrion 11:214-222.
24. Kamei J, Zushida K, Morita K, Sasaki M, Tanaka S. 2001. Role of vanilloid VR1 receptor in thermal allodynia and hyperalgesia in diabetic mice. Eur J Pharmacol 422:83-86.
25. Kanan SA, Sarcde NE, Haddad JJ, Abdelnoor AM, Atweh SF, Jabbur SJ, Safieh-Garabedian B. 1996. Endotoxin induced local inflammation and hyperalgesia in rats and mice: a new model of inflammatory pain. Pain 66:373-379.
26. Katsukawa M, Nakata R, Koeji S, Hori K, Takahashi S, Inoue, H. 2011. Citronellol and geraniol, components of rose oil activate peroxisome proliferator-activated receptor α and γ and suppress cyclooxygenase-2 expression. Biosci Biotechnol Biochem 75:1010-1012.
27. Kostyuk VA, Potapovich AI. 1989. Superoxide driven oxidation of quercetin and a simple sensitive assay for determination of superoxide dismutase. Biochem Int 19:1117-1124.
28. Kuhad A, Chopra K. 2008. Effect of sesamol on diabetes-associated cognitive decline in rats. Exp Brain Res 185:411-420.
29. Kumar A, Negi G, Sharma SS. 2012. Suppression of NFkB and NFkB regulated oxidative stress and neuroinflammation by BAY11-7082 (IκB phosphorylation inhibitor) in experimental diabetic neuropathy. Biochimie 94:1158-65.
30. Lapczynski A, Bhatia SP, Foxenberg RJ, Letizia CS, Api AM. 2008. Fragrance material, review on geraniol. Food Chem Toxicol 46:S160-S170.
31. Latham JR, Pathirathna S, Jagodic MM, Choe WJ, Levin ME, Nelson MT, Lee WY, Krishnan K, Covey D, Todorovic SM, Jevtovic-Todorovic V. 2009. Selective T-type calcium channel blockade alleviates hyperalgesia in ob/ob mice. Diabetes 58:2656-2665.
32. Levine RL, Garland D, Oliver C, Amici A, Climent I, Lenz A. 1990. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464-478.
33. Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ. 1951. Protein measurements using folin-phenol reagent. J Biol Chem 193:265-275.
34. Luthman M, Holmgern A. 1982. Rat liver thioredoxin and thioredoxin reductase: purification and characterization. Biochemistry 21:6628-6633.
35. Madankumar A, Jayakumar S, Gokuldhas K, Rajan B, Raghunandhakumar S, Asokkumar, Devaki T. 2013. Geraniol modulates tongue and hepatic phase I and phase II conjugation activities and may contribute directly to the chemopreventive activity against experimental oral carcinogenesis. Eur J Pharmacol 705:148-155.
36. Manoharan S, Selvan MV. 2012. Chemopreventive potential of geraniol in 7, 12-dimethylbenz(a)anthracene (DMBA) induced skin carcinogenesis in Swiss albino mice. J Environ Biol 33:255-260.
37. Mokrasch LC, Teschke EJ. 1984. Glutathione content of cultured cells and rodent brain regions: a specific fluorimetric assay. Anal Biochem 140:506-509.
38. Moreadith RW, Fiskum J. 1984. Isolation of mitochondria from ascites tumor cells permeabilized with digitonin. Anal Biochem 137:360-367.
39. Muthuraman A, Jaggi AS, Singh N, Singh D. 2008. Ameliorative effects of ocimim sanctum in sciatic nerve transection induced neuropathy in rats. Eur J Pharmacol 587:104-111.
40. Navarro A, Gomez C, Lopez-Cepero JM, Boveris A. 2004. Beneficial effects of moderate exercise on mice aging: survival, behaviour; oxidative stress and mitochondrial electron transfer. Am J Physiol Regul Integr Comp Physiol 286:505-511.
41. Naziroglu M. 2011. TRPM2 Cation channels, oxidative stress and neurological diseases: where are we now? Neurochem Res 36:355-366.
42. 2+ signaling on molecular pathways of neuropathic pain in diabetes: focus on TRP channels. Neurochem Res 37:2065-2075.
43. Negi G, Kumar A, Joshi RP, Sharma SS. 2011. Oxidative stress and Nrf2 in the pathology of diabetic neuropathy: old perspective with a new angle. Biochem Biophys Res Commun 408:1-5.
44. Obrosova IG. 2009. Diabetes and the peripheral nerve. Biochim Biophys Acta 10:931-940.
45. Ohkawa H, Ohnishi N, Yagi K. 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 9:351-358.
46. Ong TP, Cardozo MT, de Conti A, Moreno FS. 2012. Chemoprevention of hepatocarcinogenesis with dietary isoprenic derivatives: cellular and molecular aspects. Curr Cancer Drug Targets 12:1173-1190.
47. 3 supplementation. Pharmacol Biochem Behav 95:216-222.
48. Pennington R. 1961. Biochemistry of dystrophic muscle: mitochondrial succinate tetrazolium reductase and adenosine triphosphatase. Biochem J 80:649-654.
49. Perry NSL, Bollen C, Perry EK, Ballard C. 2003. Salvia for dementia therapy: review of pharmacological activity and pilot tolerability and clinical test. Pharmacol Biochem Behav 75:651-659.
50. Pradat PF, Kennel P, Naimi-Sadaqui S, Finiels F, Orsini C, Revah F, Delaere P, Mallet J. 2001. Continuous delivery of neurotrophin 3by gene therapy has a neuroprotective effect in experimental models of diabetic and acrylamide neuropathies. Hum Gene Ther 12:2237-2249.
51. Prasad SN, Muralidhara. 2013. Neuroprotective efficacy of eugenol and isoeugenol in acrylamide induced neuropathy in rats: behavioral and biochemical evidence. Neurochem Res 38:330-345.
52. Prasad SN, Muralidhara. 2014. Neuroprotective effect of geraniol and curcumin in an acrylamide model of neurotoxicity in Drosophila melanogaster: relevance to neuropathy. J Insect Physiol 60:7-14.
53. Rekha KR, Selvakumar GP, Santha K, Sivakamasundari RI. 2013. Geraniol attenuates a-synuclein expression and neuromuscular impairment through increase dopamine content in MPTP intoxicated mice by dose dependent manner. Biochem Biophys Res Comm 440:664-670.
54. Safaepour M, Shahverdi AR, Shahverdi HR, Khorramizadeh MR, Gohari AR. 2009. Green synthesis of small silver nanoparticles using geraniol and its cytotoxicity against fibrosarcoma-Wehi 164. Avicenna J Med Biotech 1:111-115.
55. Schmatz R, Mazzanti CM, Spanevello R, Stefanello N, Gutierres J, Correa M, de Rosa MM, Rubin MA, Schetinger MRC, Morsch VM. 2009. Resveratrol prevents memory deficits and the increase in acetylcholinesterase activity in streptozotocin-induced diabetic rats. Eur J Pharmacol 610:42-48.
56. Shanmugam KR, Mallikarjuna K, Kesireddy N, Reddy KS. 2011. Neuroprotective effect of ginger on antioxidant enzymes in streptozotocin-induced diabetic rats. Food Chem Toxicol 49:893-897.
57. Shelton RJ, Velavan P, Nikitin NP, Coletta AP, Clark AL, Rigby AS, Freemantle N, Cleland JG. 2005. Clinical trials update from the American Heart Association meeting: ACORN-CSD, primary care trial of chronic disease management, PEACE, CREATE, SHIELD, A-HeFT, GEMINI, vitamin E meta-analysis, ESCAPE, CARP, and SCD-HeFT cost-effectiveness study. Eur J Heart Fail 7:127-135.
58. Singh BK, Tripathi M, Chaudhari BP, Pandey PK, Kakkar P. 2012. Natural terpenes prevent mitochondrial dysfunction, oxidative stress and release of apoptotic proteins during nimesulide-hepatotoxicity in rats. Plos One 7:e34200.
59. Srere PA. 1969. Citrate synthase. Methods Enzymol 13:3-26.
60. Tiwari M, Kakkar P. 2009. Plant derived antioxidants GE and camphene protect rat alveolar macrophages against t-BHP induced oxidative stress. Toxicol In Vitro 23:295-301.
61. Urban MJ, Pan P, Farmer KL, Zhao H, Blagg BSJ, Dobrowsky RT. 2012. Modulating molecular chaperones improves sensory fibre recovery and mitochondrial function in diabetic peripheral neuropathy. Exp Neurol 235:388-396.
62. 2 mitochondrial release. Int J Biochem Cell Biol 39:1731-1742.
63. Vincent AM, Russell JW, Low P, Feldman EL. 2004. Oxidative stress in the pathogenesis of diabetic neuropathy. Endocr Rev 25:612-628.
64. Vincent AM, Edwards JL, McLean LL, Hong Y, Cerri F, Lopez L, Quattrini A, Feldman EL. 2010. Mitochondrial biogenesis and fission in axons in cell culture and animal models of diabetic neuropathy. Acta Neuropathol 120:477-489.
65. Wolff SP. 1994. Ferrous ion oxidation in presence of ferric ion indicator xylenol orange for measurement of hydroperoxides. Methods Enzymol 233:182-189.
66. Yasmina BM, Gonzalo H, Laura E. 2011. Uncovering new pharmacological targets to treat neuropathic pain by understanding how the organism reacts to nerve injury. Curr Pharm Des 17:434-448.
67. Yorek MA. 2011. Treatment of diabetic neuropathy with baicalein: intervention at multiple sites. Exp Neurol 232:105-109.
68. 2+-ATPase: modulation by L-cysteine. Metab Brain Dis 24:337-348.
69. Zochodne DW, Ramji N, Toth C. 2008. Neuronal targeting in diabetes mellitus: a story sensory neurons and motor neurons. Neuroscientist 14:311-318.