Mehmet Dinçer BİLGİN, Hatice KESER, Muhammed MAJEED, Özlem BOZKURT GİRİT, Mahadeva NAYAK

Pterostilbene administration improves the recovery potential of extremely low-frequency magnetic field in acute renal ischemia-reperfusion injury: an FTIR spectroscopic study

Renal ischemia-reperfusion (I/R) injury, one of the drastic outcomes of renal failure and organ transplantation, tends todeteriorate over time; therefore, noninvasive therapeutic strategies will avail the progression-free survival of the patients. Magneticfield has been proposed as a noninvasive treatment strategy; however, with recent scientific advances, many controversies have arisenregarding its efficacy. Pterostilbene, a natural analog of resveratrol, was documented to be effective in treatment of I/R injuries. Thisstudy aims to assess the acute therapeutic effects of combined extremely low-frequency magnetic field (ELF-MF) and pterostilbenetreatment on renal I/R injury. After induction of renal I/R in Wistar rats, treatments of 50 Hz, 1 mT ELF-MF applied alone or incombination with pterostilbene were applied for 5 consecutive days. Kidney homogenates were analyzed by Fourier transform infraredspectroscopy. I/R injury resulted in an altered protein and lipid structure with the dominance of longer acyl chains; a slight decrease inlipid, protein, unsaturated lipid, and unsaturated/saturated lipid content; and an increase in membrane fluidity and lipid peroxidationin rat kidneys. Although ELF-MF treatment alone was not sufficient to restore all ischemia-induced alterations, the combined treatmentstrategy of pterostilbene administration in the presence of ELF-MF was successful and warrants further investigation.

PDF

___

Allred AJ, Chappell MC, Ferrario CM, Diz DI (2000). Differential actions of renal ischemic injury on the intrarenal angiotensin system. American Journal of Physiology-Renal Physiology 279 (4): F636-645. doi: 10.1152/ajprenal.2000.279.4.F636
Baker MJ, Byrne HJ, Chalmers J, Gardner P, Goodacre R et el. (2018). Clinical applications of infrared and Raman spectroscopy: state of play and future challenges. Analyst 143 (8): 1735-1757. doi: 10.1039/c7an01871a
Bozkurt O, Haman Bayari S, Severcan M, Krafft C, Popp J et al. (2012). Structural alterations in rat liver proteins due to streptozotocin-induced diabetes and the recovery effect of selenium: Fourier transform infrared microspectroscopy and neural network study. Journal of Biomedical Optics 17 (7): 076023. doi: 10.1117/1.JBO.17.7.076023
Bozkurt O, Severcan M, Severcan F (2010). Diabetes induces compositional, structural and functional alterations on rat skeletal soleus muscle revealed by FTIR spectroscopy: a comparative study with EDL muscle. Analyst 135 (12): 3110- 3119. doi: 10.1039/c0an00542h
Bułdak RJ, Polaniak R, Bułdak L, Zwirska-Korczala K, Skonieczna M et al. (2012). Short-term exposure to 50Hz ELF-EMF alters the cisplatin-induced oxidative response in AT478 murine squamous cell carcinoma cells. Bioelectromagnetics 33 (8): 641-651. doi: 10.1002/bem.21732
Cakmak G, Miller LM, Zorlu F, Severcan F (2012). Amifostine, a radioprotectant agent, protects rat brain tissue lipids against ionizing radiation induced damage: an FTIR microspectroscopic imaging study. Archives of Biochemistry and Biophysics 520 (2): 67-73. doi: 10.1016/j.abb.2012.02.012
Cakmak G, Zorlu F, Severcan M, Severcan F (2011). Screening of protective effect of amifostine on radiation-ınduced structural and functional variations in rat liver microsomal membranes by FT-IR spectroscopy. Analytical Chemistry 83 (7): 2438- 2444. doi: 10.1021/ac102043p
Callaghan MJ, Chang EI, Seiser N, Aarabi S, Ghali S et al. (2008). Pulsed electromagnetic fields accelerate normal and diabetic wound healing by increasing endogenous FGF-2 release. Plastic and Reconstructive Surgery 121 (1): 130-141. doi: 10.1097/01. prs.0000293761.27219.84
Chen ZW, Miu HF, Wang HP, Wu ZN, Wang WJ et al. (2018). Pterostilbene protects against uraemia serum-induced endothelial cell damage via activation of Keap1/Nrf2/HO-1 signaling. International Urology and Nephrology 50 (3): 559- 570. doi: 10.1007/s11255-017-1734-4
Cheng Y, Di S, Fan C, Cai L, Gao C et al. (2016). SIRT1 activation by pterostilbene attenuates the skeletal muscle oxidative stress injury and mitochondrial dysfunction induced by ischemia reperfusion injury. Apoptosis 21 (8): 905-916. doi: 10.1007/ s10495-016-1258-x
Cichoń N, Bijak M, Miller E, Saluk J (2017). Extremely low frequency electromagnetic field (ELF-EMF) reduces oxidative stress and improves functional and psychological status in ischemic stroke patients. Bioelectromagnetics 38 (5): 386-396. doi: 10.1002/bem.22055
Costa EVL, Jimenez GC, Barbosa CTF (2013). Fractal analysis of extra-embryonic vascularization in Japanese quail embryos exposed to extremely low frequency magnetic fields. Bioelectromagnetics 34: 114-121. doi: 10.1002/bem.21759
Delle Monache S, Alessandro R, Iorio R, Gualtieri G, Colonna R (2008). Extremely low frequency electromagnetic fields (ELF-EMFs) induce in vitro angiogenesis process in human endothelial cells. Bioelectromagnetics 29 (8): 640-648. doi: 10.1002/bem.20430
Delle Monache S, Angelucci A, Sanità P, Iorio R, Bennato F et al. (2013). Inhibition of angiogenesis mediated by extremely low-frequency magnetic fields (ELF-MFs). PLoS One 8 (11): e79309. doi: 10.1371/journal.pone.0079309
de Zwart LL, Meerman JHN, Commandeur JNM, Vermeulen NPE (1999). Biomarkers of free radical damage applications in experimental animals and in humans. Free Radical Biology and Medicine 26 (1-2): 202-226.
Duffield JS, Park KM, Hsiao LL, Kelley VR, Scadden DT et al. (2005). Restoration of tubular epithelial cells during repair of the postischemic kidney occurs independently of bone marrowderived stem cells. Journal of Clinical Investigation 115 (7): 1743-1755. doi: 10.1172/JCI22593
Emre M, Cetiner S, Zencir S, Unlukurt I, Kahraman I et al. (2011). Oxidative stress and apoptosis in relation to exposure to magnetic field. Cell Biochemistry and Biophysics 59 (2): 71-77. doi: 10.1007/s12013-010-9113-0
Fouad AA, Al-Mulhim AS, Jresat I, Morsy MA (2013) Protective effects of captopril in diabetic rats exposed to ischemia/reperfusion renal injury. Journal of Pharmacy and Pharmacology 65 (2): 243-252. doi: 10.1111/j.2042-7158.2012.01585.x
Frahm J, Mattsson MO, Simko M (2000). Exposure to ELF magnetic fields modulate redox related protein expression in mouse macrophages. Toxicology Letters 192 (3): 330-336. doi: 10.1016/j.toxlet.2009.11.010
Fujigaki Y (2012). Different modes of renal proximal tubule regeneration in health and disease. World Journal of Nephrology 1 (4): 92-99. doi: 10.5527/wjn.v1.i4.92
Gao D, Jing S, Zhang Q, Wu G (2018). Pterostilbene protects against acute renal ischemia reperfusion injury and inhibits oxidative stress, inducible nitric oxide synthase expression and inflammation in rats via the Toll-like receptor 4/nuclear factorκB signaling pathway. Experimental and Therapeutic Medicine 15 (1): 1029-1035. doi: 10.3892/etm.2017.5479
Gasper R, Dewelle J, Kiss R, Mijatovic T, Goormaghtigh E (2009). IR Spectroscopy as a new tool for evidencing antitumor drug signatures. Biochimica et Biophysica Acta 1788 (6): 1263-1270. doi: 10.1016/j.bbamem.2009.02.016
Glinka M, Sieroń A, Birkner E, Cieślar G (2013). Influence of extremely low-frequency magnetic field on the activity of antioxidant enzymes during skin wound healing in rats. Electromagnetic Biology and Medicine 32 (4): 463-470. doi: 10.3109/15368378.2012.743906
Grana DR, Marcos HJ, Kokubu GA (2008). Pulsed electromagnetic fields as adjuvant therapy in bone healing and peri-implant bone formation: an experimental study in rats.Acta Odontolica Latinoamericana 21 (1): 77-83.
Haris PI, Severcan F (1999). FTIR spectroscopic characterization of protein structure in aqueous and non-aqueous media. Journal of Molecular Catalysis B: Enzymatic 7: 207-221.
Hosseinabadi MB, Khanjani N, Samaei SE, Nazarkhani F (2019). Effect of long-term occupational exposure to extremely lowfrequency electromagnetic fields on proinflammatory cytokine and hematological parameters. International Journal of Radiation Biology 5: 1-8. doi: 10.1080/09553002.2019
Inal M, Altışık M, Bilgin MD (2002). The effect of quercetin on renal ischemia and reperfusion injury in the rat. Cell Biochemistry and Function 20 (4): 291-296. doi: 10.1002/cbf.953
Kapetanovic IM, Muzzio M, Huang Z, Thompson TN, McCormick DL (2011). Pharmacokinetics, oral bioavailability, and metabolic profile of resveratrol and its dimethylether analog, pterostilbene, in rats. Cancer Chemotherapy and Pharmacology 68 (3): 593-601. doi: 10.1007/s00280-010-1525-4
Khan SA, Liu X, Li H, Fan W, Shah BR et al (2015). Organ-specific antioxidant defenses and FT-IR spectroscopy of muscles in Crucian carp (Carassius auratus gibelio) exposed to environmental Pb2+. Turkish Journal of Biology 39: 427-437. doi: 10.3906/biy-1410-3
Kohen R, Nyska A (2002). Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicologic Pathology 30 (6): 620-650. doi: 10.1080/01926230290166724
Li F, Lei T, Xie K, Wu X, Tang C et al. (2016). Effects of extremely low frequency pulsed magnetic fields on diabetic nephropathy in streptozotocin-treated rats. Biomedical Engineering Online 15: 8. doi: 10.1186/s12938-015-0121-6
Li Z, Wang Y, Sun N, Liu X, Song E et al. (2019). Melatonin therapy protects against renal injury before and after release of bilateral ureteral obstruction in rats. Life Sciences 229: 104-115. doi: 10.1016/j.lfs.2019.05.034
Ma F, Li W, Li X, Tran BH, Suguro R et al. (2016). Novel protective effects of pulsed electromagnetic field ischemia/reperfusion injury rats. Bioscience Reports 36 (6): e00420. doi: 10.1042/ BSR20160082
Manikonda PK, Rajendra P, Devendranath D, Gunasekaran B, Channakeshava Aradhya SR et al. (2014). Extremely low frequency magnetic fields induce oxidative stress in rat brain. General Physiology Biophysics 33 (1): 81-90. doi: 10.4149/ gpb_2013059
Martínez-Sámano J, Torres-Durán PV, Juárez-Oropeza MA, ElíasViñas D, Verdugo-Díaz L (2010). Effects of acute electromagnetic field exposure and movement restraint on antioxidant system in liver, heart, kidney and plasma of Wistar rats: a preliminary report. International Journal of Radiation Biology 86 (12): 1088- 1094. doi: 10.3109/09553002.2010.501841
McCormack D, McFadden D (2013). A review of pterostilbene antioxidant activity and disease modification. Oxidative Medicine and Cellular Longevity 2013: 575482. doi: 10.1155/2013/575482
McKay JC, Corbacio M, Tyml K, Prato FS, Thomas AW (2010). Extremely low frequency pulsed electromagnetic field designed for antinociception does not affect microvascular responsiveness to the vasodilator acetylcholine. Bioelectromagnetics 31 (1): 64- 76. doi: 10.1002/bem.20533
Mordechai S, Shufan E, Porat Katz BS, Salman A (2017). Early diagnosis of Alzheimer’s disease using infrared spectroscopy of isolated blood samples followed by multivariate analyses. Analyst 142 (8): 1276-1284. doi: 10.1039/c6an01580h
Movasaghi Z, Rehman S, Rehman I (2008). Fourier transform infrared (FTIR) spectroscopy of biological tissues. Applied Spectroscopy Reviews 43 (2): 134-179. doi: 10.1080/05704920701829043
Nara M, Okazaki M, Kagi H (2002). Infrared study of human serum very-low-density and low-density lipoproteins. Implication of esterified lipid C=O stretching bands for characterizing lipoproteins. Chemistry and Physics of Lipids 117 (1-2): 1-6.
Nath KA, Grande JP, Croatt AJ, Frank E, Caplice NM et al. (2005). Transgenic sickle mice are markedly sensitive to renal ischemiareperfusion injury. American Journal of Pathology 166 (4): 963- 972. doi: 10.1016/S0002-9440(10)62318-8
Ozek NS, Tuna S, Erson-Bensan AE, Severcan F (2010). Characterization of microRNA-125b expression in MCF7 breast cancer cells by ATR-FTIR spectroscopy. Analyst 135 (12): 3094- 3102. doi: 10.1039/c0an00543f
Pan Y, Dong Y, Hou W, Ji Z, Zhi K et al. (2013). Effects of PEMF on microcirculation and angiogenesis in a model of acute hindlimb ischemia in diabetic rats. Bioelectromagnetics 34 (3): 180-188. doi: 10.1002/bem.21755
Pan Z, Agarwal AK, Xu T, Feng Q, Baerson SR et al. (2008). Identification of molecular pathways affected by pterostilbene, a natural dimethylether analog of resveratrol. BMC Medical Genomics 1: 7. doi: 10.1186/1755-8794-1-7
Park WS, Park MS, Kang SW, Jin SA, Jeon Y et al. (2019). Hesperidin shows protective effects on renal function in ischemia-induced acute kidney injury (Sprague-Dawley rats). Transplantation Proceedings 51 (8): 2838-2841. doi: 10.1016/j. transproceed.2019.02.055
Rauš S, Selaković V, Manojlović-Stojanoski M, Radenović L, Prolić Z et al. (2013). Response of hippocampal neurons and glial cells to alternating magnetic field in gerbils submitted to global cerebral ischemia. Neurotoxicity Research 23 (1): 79-91. doi: 10.1007/s12640-012-9333-8
Rauš Balind S, Selaković V, Radenović L, Prolić Z, Janać B (2014). Extremely low frequency magnetic field (50 Hz, 0.5 mT) reduces oxidative stress in the brain of gerbils submitted to global cerebral ischemia. PLoS One 9 (2): e88921. doi: 10.1371/ journal.pone.0088921
Rieppo L, Saarakkala S, Närhi T, Helminen HJ, Jurvelin JS et al. (2012). Application of second derivative spectroscopy for increasing molecular specificity of Fourier transform infrared spectroscopic imaging of articular cartilage. Osteoarthritis and Cartilage 20 (5): 451-459. doi: 10.1016/j.joca.2012.01.010
Sen I, Bozkurt O, Aras E, Heise S, Brockmann GA et al. (2015). Lipid profiles of adipose and muscle tissues in mouse models of juvenile onset of obesity without high fat diet induction: a Fourier transform infrared (FT-IR) spectroscopic study. Applied Spectroscopy 69 (6): 679-688. doi: 10.1366/14-07443
Severcan F, Bozkurt O, Gurbanov R, Gorgulu G (2010). FT-IR spectroscopy in diagnosis of diabetes in rat animal model. Journal of Biophotonics 3 (8-9): 621-631. doi: 10.1002/ jbio.201000016
Severcan F, Sahin I, Kazanci N (2005). Melatonin strongly interacts with zwitterionic model membranes--evidence from Fourier transform infrared spectroscopy and differential scanning calorimetry. Biochimica et Biophysica Acta 1668 (2): 215-222. doi: 10.1016/j.bbamem.2004.12.009
Szalontai B, Nishiyama Y, Gombos Z, Murata N (2000). Membrane dynamics as seen by Fourier transform infrared spectroscopy in a cyanobacterium, Synechocystis PCC 6803: the effects of lipid unsaturation and the protein-to-lipid ratio. Biochimica et Biophysica Acta 1509 (1-2): 409-419. doi: 10.1016/s0005- 2736(00)00323-0
Talari ACS, Martinez MAG, Movasaghi Z, Rehman S, Rehman IU (2017). Advances in Fourier transform infrared (FTIR) spectroscopy of biological tissues. Applied Spectroscopy Reviews 52 (5): 456-506. doi: 10.1080/05704928.2016.1230863
Umemura J, Cameron DG, Mantsch HH (1980). A Fourier transform infrared spectroscopic study of the molecular interaction of cholesterol with 1,2-dipalmitoyl-sn-glycero-3- phosphocholine. Biochimica et Biophysica Acta 602 (1): 32-44. doi: 10.1016/0005-2736(80)90287-4
Watanabe Y, Nakagawa M, Miyakoshi Y (1997). Enhancement of lipid peroxidation in the liver of mice exposed to magnetic fields. Industrial Health 35 (2): 285-290. doi: 10.2486/ indhealth.35.285
Xia Y, Chen Y, Tang L, Wang Z, Zheng Y (2018). Pterostilbene attenuates acute kidney injury in septic mice. Experimental and Therapeutic Medicine 15 (4): 3551-3555. doi: 10.3892/ etm.2018.5808
Yamanaka K, Houben P, Bruns H, Schultze D, Hatano E et al. (2015). A systematic review of pharmacological treatment options used to reduce ischemia reperfusion injury in rat liver transplantation. PLoS One 10 (4): e0122214. doi: 10.1371/ journal.pone.0122214
Yu Z, Wang S, Zhang X, Li Y, Zhao Q et al. (2017). Pterostilbene protects against myocardial ischemia/reperfusion injury via suppressing oxidative/nitrative stress and inflammatory response. International Immunopharmacology 43: 7-15. doi: 10.1016/j.intimp.2016.11.018
Zhang J, McCullough PA (2016). Lipoic acid in the prevention of acute kidney injury. Nephron 134 (3): 133-140. doi: 10.1159/000448666
Zheng Y, Cheng J, Dong L, Ma X, Kong Q (2019). Effects of exposure to extremely low frequency electromagnetic fields on hippocampal long-term potentiation in hippocampal CA1 region. Biochemical and Biophysical Research Communications 517 (3): 513-519. doi: 10.1016/j.bbrc.2019.07.085
Zhou Y, Zhang XM, Ma A, Zhang YL, Chen YY et al. (2015). Orally administrated pterostilbene attenuates acute cerebral ischemiareperfusion injury in a dose- and time-dependent manner in mice. Pharmacology, Biochemistry and Behavior 135: 199-209. doi: 10.1016/j.pbb.2015.06.009
Zou C, Hu H, Xi X, Shi Z, Wang G et al. (2013). Pioglitazone protects against renal ischemia-reperfusion injury by enhancing antioxidant capacity. Journal of Surgical Research 184 (2): 1092-1095. doi: 10.1016/j.jss.2013.03.027