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Erschienen in: Journal of Diabetes & Metabolic Disorders 2/2018

16.08.2018 | Research Article

Imbalanced oxidative stress and pro-inflammatory markers differentiate the development of diabetic neuropathy variants in streptozotocin-induced diabetic rats

verfasst von: Che Aishah Nazariah Ismail, Che Badariah Abd Aziz, Rapeah Suppian, Idris Long

Erschienen in: Journal of Diabetes & Metabolic Disorders | Ausgabe 2/2018

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Abstract

Purpose

Diabetic neuropathy is a prolonged symptom of diabetes mellitus that affect a number of diabetes mellitus patients. So far, the variants of diabetic neuropathy, either painful (PDN) or non-painful (or painless, non-PDN) response have distinctive clinical entities. This study aims to determine the effects of oxidative stress parameters and pro-inflammatory factors at spinal cord level of streptozotocin-induced diabetic neuropathy rat model.

Methods

Thirty Sprague-Dawley rats were randomly assigned to control (non-diabetic), PDN and non-PDN groups (n = 10). The rats were induced with diabetes by streptozotocin injection (60 mg/kg). Tactile allodynia and thermal hyperalgesia were assessed on day 0, 14 (week 2) and 21 (week 3) in the rats. The rats were sacrificed and the spinal cord tissue was collected for the measurement of oxidative stress (malondialdehyde (MDA), superoxide dismutase (SOD) and catalase) and pro-inflammatory markers (interleukin-1β (IL-1β) and tumour necrosis factor-α (TNF-α)).

Results

PDN rats demonstrated a marked tactile allodynia with no thermal hyperalgesia whilst non-PDN rats exhibited a prominent hypo-responsiveness towards non-noxious stimuli and hypoalgesia towards thermal input. The MDA level and pro-inflammatory TNF-α was significantly increased in PDN rats whilst catalase was reduced in these rats. Meanwhile, non-PDN rats demonstrated reduced SOD enzyme activity and TNF-α level and increased MDA and catalase activity.

Conclusion

The changes in oxidative stress parameters and pro-inflammatory factors may contribute to the changes in behavioural responses in both PDN and non-PDN rats.
Literatur
1.
Zurück zum Zitat Besson JM, Chaouch A. Peripheral and spinal mechanisms of nociception. Physiol Rev. 1987;67:67–186.CrossRefPubMed Besson JM, Chaouch A. Peripheral and spinal mechanisms of nociception. Physiol Rev. 1987;67:67–186.CrossRefPubMed
2.
Zurück zum Zitat Britland ST, Young RJ, Sharma AK, Clarke BF. Association of painful and painless diabetic polyneuropathy with different patterns of nerve fiber degeneration and regeneration. Diabetes. 1990;39:898–908.CrossRefPubMed Britland ST, Young RJ, Sharma AK, Clarke BF. Association of painful and painless diabetic polyneuropathy with different patterns of nerve fiber degeneration and regeneration. Diabetes. 1990;39:898–908.CrossRefPubMed
3.
Zurück zum Zitat Calcutt NA. Potential mechanisms of neuropathic pain in diabetes. Int Rev Neurobiol. 2002;50:205–28.CrossRefPubMed Calcutt NA. Potential mechanisms of neuropathic pain in diabetes. Int Rev Neurobiol. 2002;50:205–28.CrossRefPubMed
4.
Zurück zum Zitat Courteix C, Eschalier A, Lavarenne J. Streptozocin-induced diabetic rats: behavioural evidence for a model of chronic pain. Pain. 1993;53:81–8.CrossRefPubMed Courteix C, Eschalier A, Lavarenne J. Streptozocin-induced diabetic rats: behavioural evidence for a model of chronic pain. Pain. 1993;53:81–8.CrossRefPubMed
5.
Zurück zum Zitat Cui XP, Li BY, Gao HQ, Wei N, Wang WL, Lu M. Effects of grape seed proanthocyanidin extracts on peripheral nerves in streptozocin-induced diabetic rats. J Nutr Sci Vitaminol. 2008;54:321–8.CrossRefPubMed Cui XP, Li BY, Gao HQ, Wei N, Wang WL, Lu M. Effects of grape seed proanthocyanidin extracts on peripheral nerves in streptozocin-induced diabetic rats. J Nutr Sci Vitaminol. 2008;54:321–8.CrossRefPubMed
6.
Zurück zum Zitat Daulhac L, Maffre V, Mallet C, Etienne M, Privat A, Kowalski-Chavuvel A, et al. Phosphorylation of spinal N-methyl-D-aspartate receptor NR1 subunits by extracellular signal-regulated kinase in dorsal horn neurons and microglia contributes to diabetes-induced paiful neuropathy. Eur J Pain. 2011;15:169. e1-12PubMed Daulhac L, Maffre V, Mallet C, Etienne M, Privat A, Kowalski-Chavuvel A, et al. Phosphorylation of spinal N-methyl-D-aspartate receptor NR1 subunits by extracellular signal-regulated kinase in dorsal horn neurons and microglia contributes to diabetes-induced paiful neuropathy. Eur J Pain. 2011;15:169. e1-12PubMed
7.
Zurück zum Zitat El-Khatib AS, Moustafa AM, Abdel-Aziz AAH, Al-Shabanah OA, El-Kashef HA. Effects of aminoguanidine and desferrioxamine on some vascular and biochemical changes associated with streptozotocin-induced hyperglycaemia in rats. Pharmacol Res. 2001;43:233–40.CrossRefPubMed El-Khatib AS, Moustafa AM, Abdel-Aziz AAH, Al-Shabanah OA, El-Kashef HA. Effects of aminoguanidine and desferrioxamine on some vascular and biochemical changes associated with streptozotocin-induced hyperglycaemia in rats. Pharmacol Res. 2001;43:233–40.CrossRefPubMed
8.
Zurück zum Zitat Fishbain DA, Cole B, Lewis JE, Gao J. What is the evidence for chronic pain being etiologically associated with the DSM-IV category of sleep disorder due to a general medical condition? A structured evidence-based review. Pain Med. 2010;11:158–79.CrossRefPubMed Fishbain DA, Cole B, Lewis JE, Gao J. What is the evidence for chronic pain being etiologically associated with the DSM-IV category of sleep disorder due to a general medical condition? A structured evidence-based review. Pain Med. 2010;11:158–79.CrossRefPubMed
9.
Zurück zum Zitat Fröde T, Medeiros Y. Animal models to test drugs with potential antidiabetic activity. J Ethnopharmacol. 2008;115:173–83.CrossRefPubMed Fröde T, Medeiros Y. Animal models to test drugs with potential antidiabetic activity. J Ethnopharmacol. 2008;115:173–83.CrossRefPubMed
10.
Zurück zum Zitat Hunskaar S, Berge OG, Hole K. A modified hot-plate test sensitive to mild analgesics. Behav Brain Res. 1986;21:101–8.CrossRefPubMed Hunskaar S, Berge OG, Hole K. A modified hot-plate test sensitive to mild analgesics. Behav Brain Res. 1986;21:101–8.CrossRefPubMed
11.
Zurück zum Zitat Jirmanova I. Giant axonopathy in streptozotocin diabetes of rats. Acta Neuropathol. 1993;86:42–8.CrossRefPubMed Jirmanova I. Giant axonopathy in streptozotocin diabetes of rats. Acta Neuropathol. 1993;86:42–8.CrossRefPubMed
12.
Zurück zum Zitat Kȩdziora-Kornatowska KZ, Luciak M, Błaszczyk J, Pawlak W. Effect of Aminoguanidine on Erythrocyte Lipid Peroxiclation and Activities of Antioxidant Enzymes in Experimental Diabetes. Clin Chem Lab Med. 1998;36:771–5.PubMedCrossRef Kȩdziora-Kornatowska KZ, Luciak M, Błaszczyk J, Pawlak W. Effect of Aminoguanidine on Erythrocyte Lipid Peroxiclation and Activities of Antioxidant Enzymes in Experimental Diabetes. Clin Chem Lab Med. 1998;36:771–5.PubMedCrossRef
13.
Zurück zum Zitat Kline KM, Caroll DG, Malnar KF. Painful diabetic peripheral neuropathy relieved with use of oral topiramate. South Med J. 2003;96 Kline KM, Caroll DG, Malnar KF. Painful diabetic peripheral neuropathy relieved with use of oral topiramate. South Med J. 2003;96
14.
Zurück zum Zitat Krämer HH, Rolke R, Bickel A, Birklein F. Thermal thresholds predict painfulness of diabetic neuropathies. Diabetes Care. 2004;27:2386–91.CrossRefPubMed Krämer HH, Rolke R, Bickel A, Birklein F. Thermal thresholds predict painfulness of diabetic neuropathies. Diabetes Care. 2004;27:2386–91.CrossRefPubMed
15.
Zurück zum Zitat Malcangio M, Tomlinson DR. A pharmacologic analysis of mechanical hyperalgesia in streptozotocin-diabetic rats. Pain. 1998;76:151–7.CrossRefPubMed Malcangio M, Tomlinson DR. A pharmacologic analysis of mechanical hyperalgesia in streptozotocin-diabetic rats. Pain. 1998;76:151–7.CrossRefPubMed
16.
Zurück zum Zitat Martinov T, Mack M, Sykes A, Chatterjea D. Measuring changes in tactile sensitivity in the Hind paw of mice using an electronic von Frey apparatus. J Vis Exp. 2013;82:5212. Martinov T, Mack M, Sykes A, Chatterjea D. Measuring changes in tactile sensitivity in the Hind paw of mice using an electronic von Frey apparatus. J Vis Exp. 2013;82:5212.
17.
Zurück zum Zitat Obrosova IG. Diabetes and the peripheral nerve. Biochim Biophys Acta. 1792;2009:931–40. Obrosova IG. Diabetes and the peripheral nerve. Biochim Biophys Acta. 1792;2009:931–40.
19.
Zurück zum Zitat Obrosova IG, Fathallah L, Greene D. Early changes in lipid peroxidation and antioxidative defense in diabetic rat retina: effect of DL-α-lipoic acid. Eur J Pharmacol. 2000;398:139–46.CrossRefPubMed Obrosova IG, Fathallah L, Greene D. Early changes in lipid peroxidation and antioxidative defense in diabetic rat retina: effect of DL-α-lipoic acid. Eur J Pharmacol. 2000;398:139–46.CrossRefPubMed
20.
Zurück zum Zitat Pabreja K, Dua K, Sharma S, Padi SS, Kulkarni SK. Minocycline attenuates the development of diabetic neuropathic pain: possible anti-inflammatory and anti-oxidant mechanisms. Eur J Pharmacol. 2011;661:15–21.CrossRefPubMed Pabreja K, Dua K, Sharma S, Padi SS, Kulkarni SK. Minocycline attenuates the development of diabetic neuropathic pain: possible anti-inflammatory and anti-oxidant mechanisms. Eur J Pharmacol. 2011;661:15–21.CrossRefPubMed
21.
Zurück zum Zitat Perovic A, Vuckovic T, Cvijic G, Djordjevic J, Davidovic V. Involvement of nitric oxide in noradrenaline-induced changes in the activity of antioxidant enzymes and lipid peroxidation in rat brown adipose tissue and heart. Physiol Res. 2008;57:95.PubMed Perovic A, Vuckovic T, Cvijic G, Djordjevic J, Davidovic V. Involvement of nitric oxide in noradrenaline-induced changes in the activity of antioxidant enzymes and lipid peroxidation in rat brown adipose tissue and heart. Physiol Res. 2008;57:95.PubMed
22.
Zurück zum Zitat Sadosky A, McDermott AM, Brandenburg NA, Strauss M. A review of the epidemiology of painful diabetic peripheral neuropathy, postherpetic neuralgia, and less commonly studied neuropathic pain conditions. Pain Pract. 2008;8:45–56.CrossRefPubMed Sadosky A, McDermott AM, Brandenburg NA, Strauss M. A review of the epidemiology of painful diabetic peripheral neuropathy, postherpetic neuralgia, and less commonly studied neuropathic pain conditions. Pain Pract. 2008;8:45–56.CrossRefPubMed
23.
Zurück zum Zitat Spallone V, Greco C. Painful and painless diabetic neuropathy: one disease or two? Current Diabetes Report. 2013;13:533–49.CrossRef Spallone V, Greco C. Painful and painless diabetic neuropathy: one disease or two? Current Diabetes Report. 2013;13:533–49.CrossRef
24.
Zurück zum Zitat Tanenberg R. Painless diabetic peripheral neuropathy: the forgotten complication. Journal of Diabetes, Metabolic Disorders & Control. 2016;3:1–2. Tanenberg R. Painless diabetic peripheral neuropathy: the forgotten complication. Journal of Diabetes, Metabolic Disorders & Control. 2016;3:1–2.
25.
Zurück zum Zitat Tanenberg RJ. Diabetic peripheral neuropathy: painful or painless. Hospital Physician. 2009;45:1–8. Tanenberg RJ. Diabetic peripheral neuropathy: painful or painless. Hospital Physician. 2009;45:1–8.
26.
Zurück zum Zitat Tesfaye S, Boulton AJ, Dyck PJ, Freeman R, Horowitz M, Kempler P, et al. Diabetic neuropathies: update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care. 2010;33:2285–93.CrossRefPubMedPubMedCentral Tesfaye S, Boulton AJ, Dyck PJ, Freeman R, Horowitz M, Kempler P, et al. Diabetic neuropathies: update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care. 2010;33:2285–93.CrossRefPubMedPubMedCentral
27.
Zurück zum Zitat Tsigos C, White A, Young R. Discrimination between painful and painless diabetic neuropathy based on testing of large somatic nerve and sympathetic nerve function. Diabet Med. 1992;9:359–65.CrossRefPubMed Tsigos C, White A, Young R. Discrimination between painful and painless diabetic neuropathy based on testing of large somatic nerve and sympathetic nerve function. Diabet Med. 1992;9:359–65.CrossRefPubMed
28.
Zurück zum Zitat Tsuda M, Ueno H, Kataoka A, Tozaki-Saitoh H, Inoue K. Activation of dorsal horn microglia contributes to diabetes-induced tactile allodynia via extracellular signal-regulated protein kinase signaling. Glia. 2008;56:378–86.CrossRefPubMed Tsuda M, Ueno H, Kataoka A, Tozaki-Saitoh H, Inoue K. Activation of dorsal horn microglia contributes to diabetes-induced tactile allodynia via extracellular signal-regulated protein kinase signaling. Glia. 2008;56:378–86.CrossRefPubMed
29.
Zurück zum Zitat Van Dam PS, Van Asbeck BS, Bravenboer B, Van Oirschot JF, Gispen WH, Marx JJ. Nerve function and oxidative stress in diabetic and vitamin E-deficient rats. Free Radic Biol Med. 1998;24:18–26.CrossRefPubMed Van Dam PS, Van Asbeck BS, Bravenboer B, Van Oirschot JF, Gispen WH, Marx JJ. Nerve function and oxidative stress in diabetic and vitamin E-deficient rats. Free Radic Biol Med. 1998;24:18–26.CrossRefPubMed
30.
Zurück zum Zitat Vincent AM, Russel JW, Low P, Feldman EL. Oxidative stress in the pathogenesis of diabetic neuropathy. Endocr Rev. 2004;25:612–28.CrossRefPubMed Vincent AM, Russel JW, Low P, Feldman EL. Oxidative stress in the pathogenesis of diabetic neuropathy. Endocr Rev. 2004;25:612–28.CrossRefPubMed
31.
Zurück zum Zitat Vinik AI. Advances in diabetes for the millennium: new treatments for diabetic neuropathies. Medscape Gen Med. 2004;6:13. Vinik AI. Advances in diabetes for the millennium: new treatments for diabetic neuropathies. Medscape Gen Med. 2004;6:13.
32.
Zurück zum Zitat Zulazmi NA, Gopalsamy B, Farouk AAO, Sulaiman MR, Bharatham BH, Perimal EK. Antiallodynic and antihyperalgesic effects of zerumbone on a mouse model of chronic constriction injury-induced neuropathic pain. Fitoterapia. 2015;105:215–21.CrossRefPubMed Zulazmi NA, Gopalsamy B, Farouk AAO, Sulaiman MR, Bharatham BH, Perimal EK. Antiallodynic and antihyperalgesic effects of zerumbone on a mouse model of chronic constriction injury-induced neuropathic pain. Fitoterapia. 2015;105:215–21.CrossRefPubMed
Metadaten
Titel
Imbalanced oxidative stress and pro-inflammatory markers differentiate the development of diabetic neuropathy variants in streptozotocin-induced diabetic rats
verfasst von
Che Aishah Nazariah Ismail
Che Badariah Abd Aziz
Rapeah Suppian
Idris Long
Publikationsdatum
16.08.2018
Verlag
Springer International Publishing
Erschienen in
Journal of Diabetes & Metabolic Disorders / Ausgabe 2/2018
Elektronische ISSN: 2251-6581
DOI
https://doi.org/10.1007/s40200-018-0350-x

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