Evaluation of ameliorative effect of sodium nitrate in experimental model of streptozotocin-induced diabetic neuropathy in male rats

Adela R, Nethi SK, Bagul PK, Barui AK, Mattapally S, Kuncha M, Patra CR, Reddy PN, Banerjee SK. Hyperglycaemia enhances nitric oxide production in diabetes: a study from South Indian patients. PloS One 10, e0125270, 2015.10.1371/journal.pone.0125270Search in Google Scholar

Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: structure, function and inhibition. Biochem J 357, 593–615, 2001.10.1042/bj3570593Search in Google Scholar

Alm P, Ekstrom P, Henningsson R, Lundquist I. Morphological evidence for the existence of nitric oxide and carbon monoxide pathways in the rat islets of Langerhans: an immunocytochemical and confocal microscopical study. Diabetologia 42, 978–986, 1999.1049175810.1007/s001250051256Search in Google Scholar

Barrot M. Tests and models of nociception and pain in rodents. Neuroscience 211, 39–50, 2012.10.1016/j.neuroscience.2011.12.041Search in Google Scholar

Basbaum AI, Fields HL. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu Rev Neurosci 7, 309–338, 1984.10.1146/annurev.ne.07.030184.001521Open DOISearch in Google Scholar

Benson VS, VanLeeuwen JA, Taylor J, Somers GS, McKinney PA, Van Til L. Type 1 diabetes mellitus and components in drinking water and diet: a population-based, case-control study in Prince Edward Island, Canada. J Am Coll Nutr 29, 612–624, 2010.10.1080/07315724.2010.10719900Open DOISearch in Google Scholar

Bolcskei K, Petho G, Szolcsanyi J. Noxious heat threshold measured with slowly increasing temperatures: novel rat thermal hyperalgesia models. In Analgesia, Humana Press, Totowa, NJ 57–66, 2010.10.1007/978-1-60327-323-7_5Search in Google Scholar

Brussee V, Cunningham FA, Zochodne DW. Direct insulin signaling of neurons reverses diabetic neuropathy. Diabetes 53, 1824–1830, 2004.10.2337/diabetes.53.7.1824Search in Google Scholar

Cai S, Khoo J, Channon KM. Augmented BH4 by gene transfer restores nitric oxide synthase function in hyperglycemic human endothelial cells. Cardiovasc Res 65, 823–831, 2005.10.1016/j.cardiores.2004.10.040Search in Google Scholar

Calcutt NA, Jorge MC, Yaksh TL, Chaplan SR. Tactile allodynia and formalin hyperalgesia in streptozotocin-diabetic rats: effects of insulin, aldose reductase inhibition and lidocaine. Pain 68, 293–299, 1996.10.1016/S0304-3959(96)03201-0Open DOISearch in Google Scholar

Calcutt NA, Freshwater JD, Mizisin AP. Prevention of sensory disorders in diabetic Sprague-Dawley rats by aldose reductase inhibition or treatment with ciliary neurotrophic factor. Diabetologia 47, 718–724, 2004.10.1007/s00125-004-1354-215298349Open DOISearch in Google Scholar

California Healthcare Foundation/American Geriatrics Society Panel in Improving Care for Elders with Diabetes C. Guidelines for improving the care of the older person with diabetes mellitus. Journal of the American Geriatrics Society 51, 265–280, 2003.10.1046/j.1532-5415.51.5s.1.x12694461Search in Google Scholar

Carlstrom M, Larsen FJ, Nystrom T, Hezel M, Borniquel S, Weitzberg E, Lundberg JO. Dietary inorganic nitrate reverses features of metabolic syndrome in endothelial nitric oxide synthase-deficient mice. Proc Natl Acad Sci U S A 107, 17716–17720, 2010.10.1073/pnas.1008872107295508420876122Search in Google Scholar

Chakravarthy U, Hayes RG, Stitt AW, McAuley E, Archer DB. Constitutive nitric oxide synthase expression in retinal vascular endothelial cells is suppressed by high glucose and advanced glycation end products. Diabetes 47, 945–952, 1998.960487310.2337/diabetes.47.6.9459604873Search in Google Scholar

Cosby K, Partovi KS, Crawford JH, Patel RP, Reiter CD, Martyr S, Yang BK, Waclawiw MA, Zalos G, Xu X, Huang KT, Shields H, Kim-Shapiro DB, Schechter AN, Cannon RO 3rd, Gladwin MT. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat Med 9, 1498–1505, 2003.10.1038/nm95414595407Open DOISearch in Google Scholar

Cosentino F, Hishikawa K, Katusic ZS, Luscher TF. High glucose increases nitric oxide synthase expression and su-peroxide anion generation in human aortic endothelial cells. Circulation 96, 25–28, 1997.10.1161/01.CIR.96.1.25Open DOISearch in Google Scholar

Dobson CF, Tohyama Y, Diksic M, Hamel E. Effects of acute or chronic administration of anti-migraine drugs sumatriptan and zolmitriptan on serotonin synthesis in the rat brain. Cephalalgia 24, 2–11, 2004.1468700610.1111/j.1468-2982.2004.00647.x14687006Search in Google Scholar

Duby JJ, Campbell RK, Setter SM, Rasmussen KA. Diabetic neuropathy: an intensive review. Am J Health Syst Pharm 61, 160–173, 2004.10.1093/ajhp/61.2.16014750401Open DOISearch in Google Scholar

Duncan C, Dougall H, Johnston P, Green S, Brogan R, Leifert C, Smith L, Golden M, Benjamin N. Chemical generation of nitric oxide in the mouth from the enterosalivary circulation of dietary nitrate. Nat Med 1, 546–551, 1995.10.1038/nm0695-5467585121Search in Google Scholar

Dyck PJ, Giannini C. Pathologic alterations in the diabetic neuropathies of humans: a review. J Neuropathol Exp Neurol 55, 1181–1193, 1996.10.1097/00005072-199612000-000018957441Search in Google Scholar

Dyck PJ, Larson TS, O’Brien PC, Velosa JA. Patterns of quantitative sensation testing of hypoesthesia and hyperalgesia are predictive of diabetic polyneuropathy: a study of three cohorts. Nerve growth factor study group. Diabetes Care 23, 510–517, 2000.10.2337/diacare.23.4.510Open DOISearch in Google Scholar

Forbes JM, Cooper ME. Mechanisms of diabetic complications. Physiol Rev 93, 137–188, 2013.10.1152/physrev.00045.2011Search in Google Scholar

Fowler MJ. Microvascular and macrovascular complications of diabetes. Clinical Diabetes 26, 77–82, 2008.10.2337/diaclin.26.2.77Search in Google Scholar

Gong YH, Yu XR, Liu HL, Yang N, Zuo PP, Huang YG. Antinociceptive effects of combination of tramadol and acetaminophen on painful diabetic neuropathy in streptozotocin-induced diabetic rats Acta Anaesthesiol Taiwan 49, 16–20, 2011.10.1016/j.aat.2011.01.003Search in Google Scholar

Hoybergs YM, Meert TF. The effect of low-dose insulin on mechanical sensitivity and allodynia in type I diabetes neuropathy. Neurosci Lett 417, 149–154, 2007.10.1016/j.neulet.2007.02.087Search in Google Scholar

Jeddi S, Khalifi S, Ghanbari M, Bageripour F, Ghasemi A. Effects of nitrate intake on myocardial ischemia-reperfusion injury in diabetic rats. Arq Bras Cardiol 107, 339–347, 2016.10.5935/abc.20160137Search in Google Scholar

Jiang H, Torregrossa AC, Potts A, Pierini D, Aranke M, Garg HK, Bryan NS. Dietary nitrite improves insulin signaling through GLUT4 translocation. Free Radic Biol Med 67, 51–57, 2014.10.1016/j.freeradbiomed.2013.10.809Search in Google Scholar

Keyhanmanesh R, Hamidian G, Alipour MR, Ranjbar M, Oghbaei H. Protective effects of sodium nitrate against testicular apoptosis and spermatogenesis impairments in streptozotocin-induced diabetic male rats. Life Sci 211, 63–73, 2018.10.1016/j.lfs.2018.09.019Search in Google Scholar

Khalifi S, Rahimipour A, Jeddi S, Ghanbari M, Kazerouni F, Ghasemi A. Dietary nitrate improves glucose tolerance and lipid profile in an animal model of hyperglycemia. Nitric Oxide 44, 24–30, 2015.10.1016/j.niox.2014.11.011Open DOISearch in Google Scholar

Khan GM, Chen SR, Pan HL. Role of primary afferent nerves in allodynia caused by diabetic neuropathy in rats. Neuroscience 114, 291–299, 2002.10.1016/S0306-4522(02)00372-XSearch in Google Scholar

Kubo K, Nishikawa K, Ishizeki J, Hardy-Yamada M, Yanagawa Y, Saito S. Thermal hyperalgesia via supraspinal mechanisms in mice lacking glutamate decarboxylase 65. J Pharmacol Exp Ther 331, 162–169, 2009.10.1124/jpet.109.156034Search in Google Scholar

Lundberg JO, Feelisch M, Bjorne H, Jansson EA, Weitzberg E. Cardioprotective effects of vegetables: is nitrate the answer? Nitric Oxide 15, 359–362, 2006.1656381810.1016/j.niox.2006.01.013Search in Google Scholar

Maejima K, Nakano S, Himeno M, Tsuda SI, Makiishi H, Ito T, Nakagawa A, Kigoshi T, Ishibashi T, Nishio M, Uchida K. Increased basal levels of plasma nitric oxide in type 2 diabetic subjects: relationship to microvascular complications. J Diabetes Complications 15, 135–143, 2001.10.1016/S1056-8727(01)00144-1Search in Google Scholar

Malik RA, Tesfaye S, Newrick PG, Walker D, Rajbhandari SM, Siddique I, Sharma AK, Boulton AJ, King RH, Thomas PK, Ward JD. Sural nerve pathology in diabetic patients with minimal but progressive neuropathy. Diabetologia 48, 578–585, 2005.10.1007/s00125-004-1663-515729579Open DOISearch in Google Scholar

Mancusi G, Hutter C, Baumgartner-Parzer S, Schmidt K, Schutz W, Sexl V. High-glucose incubation of human umbilical-vein endothelial cells does not alter expression and function either of G-protein α-subunits or of endothelial NO synthase. Biochem J 315, 281–287, 1996.10.1042/bj3150281Search in Google Scholar

Meininger CJ, Marinos RS, Hatakeyama K, Martinez-Zaguilan R, Rojas JD, Kelly KA, Wu G Impaired nitric oxide production in coronary endothelial cells of the spontaneously diabetic BB rat is due to tetrahydrobiopterin deficiency. Biochem J 349, 353–356, 2000.10.1042/bj3490353Search in Google Scholar

Milsom A, Jones C, Goodfellow J, Frenneaux M, Peters J, James P. Abnormal metabolic fate of nitric oxide in Type I diabetes mellitus. Diabetologia 45, 1515–1522, 2002.1243633410.1007/s00125-002-0956-9Search in Google Scholar

Mortada Y, Khojasteh K, Zarei M, Mansouri A, Jorjani M. How nitric oxide increases in diabetic morphine tolerated male rats. Iran J Pharm Res 16, 630–639, 2017.28979316Search in Google Scholar

Nakagawa T. A new mouse model resembling human diabetic nephropathy: uncoupling of VEGF with eNOS as a novel pathogenic mechanism. Clin Nephrol 71, 103–109, 2009.10.5414/CNP71103Search in Google Scholar

Nathan C, Xie QW. Regulation of biosynthesis of nitric oxide. J Biol Chem 269, 13725–13728, 1994.10.1016/S0021-9258(17)36703-0Search in Google Scholar

Nystrom T, Ortsater H, Huang Z, Zhang F, Larsen FJ, Weitzberg E, Lundberg JO, Sjoholm A. Inorganic nitrite stimulates pancreatic islet blood flow and insulin secretion. Free Radic Biol Med 53, 1017–1023, 2012.10.1016/j.freeradbiomed.2012.06.03122750508Search in Google Scholar

Obrosova IG, Xu W, Lyzogubov VV, Ilnytska O, Mashtalir N, Vareniuk I, Pavlov IA, Zhang J, Slusher B, Drel VR. PARP inhibition or gene deficiency counteracts intraepidermal nerve fiber loss and neuropathic pain in advanced diabetic neuropathy. Free Radic Biol Med 44, 972–981, 2008.10.1016/j.freeradbiomed.2007.09.013Search in Google Scholar

Obrosova IG. Diabetes and the peripheral nerve. Biochim Biophys Acta 1792, 931–940, 2009.10.1016/j.bbadis.2008.11.005Search in Google Scholar

Oghbaei H, Asl NA, Sheikhzadeh F. Can regular moderate exercise lead to changes in miRNA-146a and its adapter proteins in the kidney of streptozotocin-induced diabetic male rats? Endocr Regul 51, 145–152, 2017.10.1515/enr-2017-0015Search in Google Scholar

Oghbaei H, Alipour MR, Hamidian G, Ahmadi M, Ghorbanzadeh V, Keyhanmanesh R. Two months sodium nitrate supplementation alleviates testicular injury in streptozotocin-induced diabetic male rats. Exp Physiol 103, 1603–1617, 2018.10.1113/EP087198Search in Google Scholar

Ohkubo Y, Kishikawa H, Araki E, Miyata T, Isami S, Motoyoshi S, Kojima Y, Furuyoshi N, Shichiri M. Intensive insulin therapy prevents the progression of diabetic microvascular complications in Japanese patients with non-insulin-dependent diabetes mellitus: a randomized prospective 6-year study. Diabetes Res Clin Pract 28, 103–117, 1995.10.1016/0168-8227(95)01064-K7587918Open DOISearch in Google Scholar

Ohtake K, Ishiyama Y, Uchida H, Muraki E, Kobayashi J. Dietary nitrite inhibits early glomerular injury in streptozotocin-induced diabetic nephropathy in rats. Nitric Oxide 17, 75–81, 2007.10.1016/j.niox.2007.06.0041768147717681477Open DOISearch in Google Scholar

Ohtake K, Nakano G, Ehara N, Sonoda K, Ito J, Uchida H, Kobayashi J. Dietary nitrite supplementation improves insulin resistance in type 2 diabetic KKAy mice. Nitric Oxide 44, 31–38, 2015.10.1016/j.niox.2014.11.0092546127125461271Open DOISearch in Google Scholar

Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87, 315–424, 2007.10.1152/physrev.00029.2006224832417237348Search in Google Scholar

Parthasarathy DK, Bryan NS. Sodium nitrite: The “cure” for nitric oxide insufficiency. Meat Sci 92, 274–279, 2012.10.1016/j.meatsci.2012.03.00122464105Open DOISearch in Google Scholar

Pirart J. Diabetes mellitus and its degenerative complications: a prospective study of 4,400 patients observed between 1947 and 1973. Diabetes Care 1, 252–263, 1978.10.2337/diacare.1.4.252Search in Google Scholar

Porta M, La Selva M, Molinatti P, Molinatti GM. Endothelial cell function in diabetic microangiopathy. Diabetologia 30, 601–619, 1987.330860210.1007/BF00277315Search in Google Scholar

Rask-Madsen C, King GL. Vascular complications of diabetes: mechanisms of injury and protective factors. Cell Metab 17, 20–33, 2013.10.1016/j.cmet.2012.11.012Search in Google Scholar

Rezabakhsh A, Ahmadi M, Khaksar M, Montaseri A, Malekinejad H, Rahbarghazi R, Garjani A. Rapamycin inhibits oxidative/nitrosative stress and enhances angiogenesis in high glucose-treated human umbilical vein endothelial cells: role of autophagy. Biomed Pharmacother 93, 885–894, 2017.10.1016/j.biopha.2017.07.04428715869Open DOISearch in Google Scholar

Sandireddy R, Yerra VG, Areti A, Komirishetty P, Kumar A. Neuroinflammation and oxidative stress in diabetic neuropathy: futuristic strategies based on these targets. Int J Endocrinol 2014, 674987, 2014.2488306110.1155/2014/674987Search in Google Scholar

Schmidt HX, Warner TD, Ishii K, Sheng H, Murad F. Insulin secretion from pancreatic B cells caused by L-arginine-derived nitrogen oxides. Science 255, 721–723, 1992.10.1126/science.1371193Search in Google Scholar

Shir Y, Seltzer ZE. A-fibers mediate mechanical hyperesthesia and allodynia and C-fibers mediate thermal hyperalgesia in a new model of causalgiform pain disorders in rats. Neurosci Lett 115, 62–67, 1990.10.1016/0304-3940(90)90518-ESearch in Google Scholar

Sjoholm A. Nitric oxide donor SIN-1 inhibits insulin release. Am J Physiol 271, C1098–C1102, 1996.10.1152/ajpcell.1996.271.4.C1098Search in Google Scholar

Smith DR, Kobrine AI, Rizzoli HV. Absence of autoregulation in peripheral nerve blood flow. J Neurol Sci 33, 347–352, 1977.10.1016/0022-510X(77)90132-0Open DOISearch in Google Scholar

Srinivasan S, Stevens M, Wiley JW. Diabetic peripheral neuropathy: evidence for apoptosis and associated mitochondrial dysfunction. Diabetes 49, 1932–1938, 2000.10.2337/diabetes.49.11.193211078462Search in Google Scholar

Tanabe M, Nagatani Y, Saitoh K, Takasu K, Ono H. Pharmacological assessments of nitric oxide synthase isoforms and downstream diversity of NO signaling in the maintenance of thermal and mechanical hypersensitivity after peripheral nerve injury in mice. Neuropharmacology 56, 702–708, 2009.10.1016/j.neuropharm.2008.12.0031911175319111753Open DOISearch in Google Scholar

Tesfaye S, Chaturvedi N, Eaton SE, Ward JD, Manes C, Ionescu-Tirgoviste C, Witte DR, Fuller JH, EURODIAB Prospective Complications Study Group. Vascular risk factors and diabetic neuropathy. N Engl J Med 352, 341–350, 2005.10.1056/NEJMoa032782Search in Google Scholar

Thrainsdottir S, Malik RA, Dahlin LB, Wiksell P, Eriksson KF, Rosen I, Petersson J, Greene DA, Sundkvist G. Endoneurial capillary abnormalities presage deterioration of glucose tolerance and accompany peripheral neuropathy in man. Diabetes 52, 2615–2622, 2003.10.2337/diabetes.52.10.261514514647Open DOISearch in Google Scholar

Vinik AI. Diabetic neuropathy: pathogenesis and therapy. Am J Med 107, 17S–26S, 1999.10.1016/S0002-9343(99)00009-1Search in Google Scholar

Vinik AI, Ziegler D. Diabetic cardiovascular autonomic neuropathy. Circulation 115, 387–397, 2007.10.1161/CIRCULATIONAHA.106.634949Search in Google Scholar

Webb AJ, Patel N, Loukogeorgakis S, Okorie M, Aboud Z, Misra S, Rashid R, Miall P, Deanfield J, Benjamin N, MacAllister R. Acute blood pressure lowering, vasoprotective, and antiplatelet properties of dietary nitrate via bioconversion to nitrite. Hypertension 51, 784–790, 2008.1825036510.1161/HYPERTENSIONAHA.107.103523Search in Google Scholar

Yagihashi S, Matsunaga M. Ultrastructural pathology of peripheral nerves in patients with diabetic neuropathy. Tohoku J Exp Med 129, 357–366, 1979.10.1620/tjem.129.357Search in Google Scholar

Yagihashi S, Mizukami H, Sugimoto K. Mechanism of diabetic neuropathy: where are we now and where to go? J Diabetes Investig 2, 18–32, 2011.10.1111/j.2040-1124.2010.00070.xSearch in Google Scholar

Yasuda H, Terada M, Maeda K, Kogawa S, Sanada M, Haneda M, Kashiwagi A, Kikkawa R. Diabetic neuropathy and nerve regeneration. Prog Neurobiol 69, 229–285, 2003.10.1016/S0301-0082(03)00034-0Search in Google Scholar

Zeng P, Li S, Zheng YH, Liu FY, Wang JL, Zhang DL, Wei J. Ghrelin receptor agonist, GHRP-2, produces antinociceptive effects at the supraspinal level via the opioid receptor in mice. Peptides 55, 103–109, 2014.10.1016/j.peptides.2014.02.01324607724Search in Google Scholar

Zhang X, Fu Y, Xu X, Li M, Du L, Han Y, Ge Y. PERK pathway are involved in NO-induced apoptosis in endothelial cells cocultured with RPE under high glucose conditions. Nitric Oxide 40, 10–16, 2014.10.1016/j.niox.2014.05.0012481339924813399Open DOISearch in Google Scholar

Zochodne DW, Levy D. Nitric oxide in damage, disease and repair of the peripheral nervous system. Cell Mol Biol (Noisy-le-grand) 51, 255–267, 2005.Search in Google Scholar