[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content

Advertisement

Springer Nature Link
Log in

Role of naringenin in protection against diabetic hyperalgesia and tactile allodynia in male Wistar rats

  • Original Paper
  • Published:
Journal of Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Hyperalgesia and allodynia are among the common manifestations of painful diabetic neuropathy. Naringenin (NA) has some biological activities, including anti-inflammatory, analgesic, and antidiabetic effects. We investigated the effects of NA administration at different doses, 20, 50, and 100 mg/kg, on streptozotocin (STZ)-induced hyperalgesia and allodynia in rats. The animals received saline or NA (20, 50, and 100 mg/kg, p.o.; once daily) for 8 weeks. Hyperalgesia was assessed by tail flick (TF) and formalin tests. Von Frey filaments were used for tactile allodynia evaluation. At the end, all rats were weighed and underwent plasma glucose and superoxide dismutase measurement. Diabetes caused significant hyperalgesia and allodynia during the above tests. NA 50 and 100 mg/kg reversed chemical and thermal hyperalgesia in diabetic rats. There were no significant differences in pain responses between NA (50 and 100 mg/kg)-treated diabetic rats and pregabalin-treated diabetic animals. Administration of NA 20 mg/kg did not alter pain-related behaviors in control and diabetic groups compared to the respective control ones. NA 50 and 100 mg/kg restored hyperglycemia as well as the decreased levels of (superoxide dismutase) SOD activity in diabetic rats. The body weight of treated diabetic rats increased significantly compared to untreated diabetics. Prolonged oral administration of NA (50 and 100 mg/kg) ameliorated some aspects of diabetic neuropathy by causing hypoglycemia and increasing the levels of antioxidant enzyme SOD. Therefore, NA makes a good candidate for treatment of diabetic neuropathy in clinical studies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Abbott FV, Franklin KB, Westbrook RF (1995) The formalin test: scoring properties of the first and second phases of the pain response in rats. Pain 60:91–102

    Article  CAS  PubMed  Google Scholar 

  2. Borradaile NM, de Dreu LE, Barrett PH, Huff MW (2002) Inhibition of hepatocyte apoB secretion by naringenin: enhanced rapid intracellular degradation independent of reduced microsomal cholesteryl esters. J Lipid Res 43:1544–1554

    Article  CAS  PubMed  Google Scholar 

  3. Borradaile NM, de Dreu LE, Barrett PH, Behrsin CD, Huff MW (2003) Hepatocyte apoB-containing lipoprotein secretion is decreased by the grapefruit flavonoid, naringenin, via inhibition of MTP mediated microsomal triglyceride accumulation. Biochemistry 42:1283–1291

    Article  CAS  PubMed  Google Scholar 

  4. Calcutt NA (2004) Experimental models of painful diabetic neuropathy. J Neurol Sci 220:137–139

    Article  PubMed  Google Scholar 

  5. Calcutt NA, Freshwater JD, Mizisin AP (2004) Prevention of sensory disorders in diabetic Sprague–Dawley rats by aldose reductase inhibition or treatment with ciliary neurotrophic factor. Diabetologia 47:718–724

    Article  CAS  PubMed  Google Scholar 

  6. Chao CL, Weng CS, Chang NC, Lin JS, Kao ST, Ho FM (2010) Naringenin more effectively inhibits inducible nitric oxide synthase and cyclooxygenase-2 expression in macrophages than in microglia. Nutr Res 30:858–64

    Article  CAS  PubMed  Google Scholar 

  7. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55–63

    Article  CAS  PubMed  Google Scholar 

  8. Cheesman KH (1993) Lipid peroxidation in biological systems. In: Halliwell B, Aruoma OI (eds) DNA and free radicals. Ellis Horwood, London, pp 12–17

    Google Scholar 

  9. Coderre TJ, Fundytus ME, McKenna JE, Dalal S, Melzack R (1993) The formalin test: a validation of the weighted-scores method of behavioural pain rating. Pain 54:43–50

    Article  CAS  PubMed  Google Scholar 

  10. Courteix C, Eschalier A, Lavarenne J (1993) Streptozotocin-induced diabetic rats: behavioral evidence for a model of chronic pain. Pain 53:81–88

    Article  CAS  PubMed  Google Scholar 

  11. Craig WJ (1999) Health-promoting properties of common herbs. Am J Clin Nutr 70:S491–S499

    Google Scholar 

  12. Dobretsov M, Hastings SL, Romanovsky D, Stimers JR, Zhang JM (2003) Mechanical hyperalgesia in rat models of systemic and local hyperglycemia. Brain Res 960:174–183

    Article  CAS  PubMed  Google Scholar 

  13. Freshwater JD, Malmberg AB, Calcutt NA (2002) Elevated spinal cyclooxygenase and prostaglandin release during hyperalgesia in diabetic rats. Diabetes 51:2249–55

    Article  CAS  PubMed  Google Scholar 

  14. Goldwasser J, Cohen PY, Yang E, Balaguer P, Yarmush ML, Nahmias Y (2010) Transcriptional regulation of human and rat hepatic lipid metabolism by the grapefruit flavonoid naringenin: role of PPARalpha, PPARgamma and LXRalpha. PLoS One 5(8):e12399

    Article  PubMed Central  PubMed  Google Scholar 

  15. Gupta M, Singh J, Sood S, Arora B (2003) Mechanism of antinociceptive effect of nimodipine in experimental diabetic neuropathic pain. Methods Find Exp Clin Pharmacol 25:49–52

    Article  CAS  PubMed  Google Scholar 

  16. Hasanein P, Soltani N (2009) Effects of the endocannabinoid transport inhibitors AM404 and UCM707 on diabetic neuropathy in rats. Clin Exp Pharmacol Physiol 36:1127–1131

    Article  CAS  PubMed  Google Scholar 

  17. Heo HJ, Kim DO, Shin SC, Kim MJ, Kim BG, Shin DH (2004) Effect of antioxidant flavanone, naringenin, from Citrus junos on neuroprotection. J Agric Food Chem 52:1520–1525

    Article  CAS  PubMed  Google Scholar 

  18. Heo HJ, Kim MJ, Lee JM, Choi SJ, Cho HY, Hong B, Kim HK, Kim E, Shin DH (2004) Naringenin from citrus junos has an inhibitory effect on acetylcholinesterase and a mitigating effect on amnesia. Dement Geriatr Cogn Disord 17:151–157

    Article  CAS  PubMed  Google Scholar 

  19. Jain V, Jaggi AS, Singh N (2009) Ameliorative potential of rosiglitazone in tibial and sural nerve transection-induced painful neuropathy in rats. Pharmacol Res 59:385–92

    Article  CAS  PubMed  Google Scholar 

  20. Kaulaskar S, Bhutada P, Rahigude A, Jain D, Harle U (2012) Effects of naringenin on allodynia and hyperalgesia in rats with chronic constriction injury-induced neuropathic pain. Zhong Xi Yi Jie He Xue Bao 10:1482–9

    Article  CAS  PubMed  Google Scholar 

  21. Kitto KF, Haley JE, Wilcox GL (1992) Involvement of nitric oxide in spinally mediated hyperalgesia in the mouse. Neurosci Lett 148:1–5

    Article  CAS  PubMed  Google Scholar 

  22. Kumar A, Meena S, Kalonia H, Gupta A, Kumar P (2011) Effect of nitric oxide in protective effect of melatonin against chronic constriction sciatic nerve injury induced neuropathic pain in rats. Indian J Exp Biol 49:664–71

    CAS  PubMed  Google Scholar 

  23. Lee JH, McCarty R (1992) Pain threshold in diabetic rats: effects of good versus poor diabetic control. Pain 50:231–236

    Article  CAS  PubMed  Google Scholar 

  24. Malcangio M, Tomlinson DR (1998) A pharmacologic analysis of mechanical hyperalgesia in streptozotocin/diabetic rats. Pain 76:151–157

    Article  CAS  PubMed  Google Scholar 

  25. Mulvihill EE, Allister EM, Sutherland BG, Telford DE, Sawyez CG, Edwards JY, Markle JM, Hegele RA, Huff MW (2009) Naringenin prevents dyslipidemia, apolipoprotein B overproduction, and hyperinsulinemia in LDL receptor-null mice with diet-induced insulin resistance. Diabetes 58:2198–2210

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. O’Connor AB, Dworkin RH (2009) Treatment of neuropathic pain: an overview of recent guidelines. Am J Med 122:S22–S32

    Article  PubMed  Google Scholar 

  27. Ortiz-Andrade RR, Sánchez-Salgado JC, Navarrete-Vázquez G, Webster SP, Binnie M, García-Jiménez S, León-Rivera I, Cigarroa-Vázquez P, Villalobos-Molina R, Estrada-Soto S (2008) Antidiabetic and toxicological evaluations of naringenin in normoglycaemic and NIDDM rat models and its implications on extra-pancreatic glucose regulation. Diabetes Obes Metab 10:1097–1104

    Article  CAS  PubMed  Google Scholar 

  28. Park J-H, Lee J-W, Paik H-D (2010) Cytotoxic effects of 7-O-butyl naringenin on human breast cancer MCF-7 cells. Food Sci Biotechnol 19:717–724

    Article  CAS  Google Scholar 

  29. Park HY, Kim GY, Choi YH (2012) Naringenin attenuates the release of pro-inflammatory mediators from lipopolysaccharide-stimulated BV2 microglia by inactivating nuclear factor-κB and inhibiting mitogen-activated protein kinases. Int J Mol Med 30:204–10

    CAS  PubMed  Google Scholar 

  30. Rahigude A, Bhutada P, Kaulaskar S, Aswar M, Otari K (2012) Participation of antioxidant and cholinergic system in protective effect of naringenin against type-2 diabetes-induced memory dysfunction in rats. Neurosci 226:62–72

    Article  CAS  Google Scholar 

  31. Rayidi S (2011) Effect of naringenin on carbohydrate metabolism in STZ-nicotinamide induced diabetic rats. Biomirror 2:1–9

    Google Scholar 

  32. Ribeiro IA, Rocha J, Sepodes B, Mota-Filipe Y, Ribeiro MH (2008) Effect of naringin enzymatic hydrolysis towards naringenin on the anti-inflammatory activity of both compounds. J Mol Catal B Enzym 52:13–18

    Article  Google Scholar 

  33. Sotnikova R, Okruhlicova L, Vlkovicova J, Navarova J, Gajdacova B, Pivackova L, Fialova S, Krenek P (2013) Rosmarinic acid administration attenuates diabetes-induced vascular dysfunction of the rat aorta. J Pharm Pharmacol 65:713–23

    Article  CAS  PubMed  Google Scholar 

  34. Tjølsen A, Berge OG, Hunskaar S, Rosland JH, Hole K (1992) The formalin test: an evaluation of the method. Pain 51:5–17

    Article  PubMed  Google Scholar 

  35. Wilcox LJ, Borradaile NM, Huff MW (1999) Antiatherogenic properties of naringenin, a citrus flavonoid. Cardiovasc Drug Rev 17:160–178

    Article  CAS  Google Scholar 

  36. Yamagishi S, Ogasawara S, Mizukami H, Yajima N, Wada R, Sugawara A, Yagihashi S (2008) Correction of protein kinase C activity and macrophage migration in peripheral nerve by pioglitazone, peroxisome proliferator activated-gamma-ligand, in insulin-deficient diabetic rats. J Neurochem 104:491–9

    CAS  PubMed  Google Scholar 

  37. Zhao DD, Yu N, Li XK, Fang X, Mu QQ, Qin PJ, Ma Y, Mo FF, Zhang DW, Gao SH (2014) Antidiabetic and antioxidative effect of jiang tang xiao ke granule in high-fat diet and low-dose streptozotocin induced diabetic rats. Evid Based Complement Alternat Med 475192

Download references

Conflict of interest

The authors state no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Biology, School of Basic Sciences, Bu-Ali Sina University, Hamedan, 6517833391, Iran

    Parisa Hasanein & Farzaneh Fazeli

Authors
  1. Parisa Hasanein
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Farzaneh Fazeli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Parisa Hasanein.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hasanein, P., Fazeli, F. Role of naringenin in protection against diabetic hyperalgesia and tactile allodynia in male Wistar rats. J Physiol Biochem 70, 997–1006 (2014). https://doi.org/10.1007/s13105-014-0369-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13105-014-0369-5

Keywords

Search

Navigation