Anti-Diabetic Countermeasures Against Tobacco Smoke-Dependent Cerebrovascular Toxicity: Use and Effect of Rosiglitazone

Tobacco smoking (TS) is one of the most addictive habit sand a main public health hazards, impacting the vascular endothelium through oxidative stress (OS) stimuli, exposure to nicotine, and smoking-induced inflammation in a dose-dependent manner. Increasing evidence also suggested that TS increases glucose intolerance and the risk factor of developing type-2 diabetes mellitus (2DM), which, along with TS, is connected to blood–brain barrier (BBB) injuries, and heightens the risk of cerebrovascular disorders. Although the exact mechanism of rosiglitazone (RSG) is unknown, our previous in vitro work showed how RSG, an oral anti-diabetic drug belonging to the family of thiazolidinedione class, can protect BBB integrity through enhancement of nuclear factor erythroid 2-related factor (Nrf2) activity. Herein, we have validated the protective role of rosiglitazone against TS-induced BBB impairment in vivo. Our results revealed that RSG as a peroxisome proliferator-activated receptor gamma (PPARγ), activates counteractive mechanisms primarily associated with the upregulation of Nrf2 and PPARγ pathways which reduce TS-dependent toxicity at the cerebrovascular level. In line with these findings, our results show that RSG reduces inflammation and protects BBB integrity. In conclusion, RSG offers a novel and promising therapeutic application to reduce TS-induced cerebrovascular dysfunction through activation of the PPARγ-dependent and/or PPARγ-independent Nrf2 pathway.

[1]  Farzane Sivandzade,et al.  Cerebrovascular and Neurological Disorders: Protective Role of NRF2 , 2019, International journal of molecular sciences.

[2]  Farzane Sivandzade,et al.  Assessing the protective effect of rosiglitazone against electronic cigarette/tobacco smoke-induced blood–brain barrier impairment , 2019, BMC Neuroscience.

[3]  Farzane Sivandzade,et al.  NRF2 and NF-қB interplay in cerebrovascular and neurodegenerative disorders: Molecular mechanisms and possible therapeutic approaches , 2018, Redox biology.

[4]  Farzane Sivandzade,et al.  Conventional and electronic cigarettes dysregulate the expression of iron transporters and detoxifying enzymes at the brain vascular endothelium: In vivo evidence of a gender-specific cellular response to chronic cigarette smoke exposure , 2018, Neuroscience Letters.

[5]  Farzane Sivandzade,et al.  In-vitro blood–brain barrier modeling: A review of modern and fast-advancing technologies , 2018, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[6]  P. Moreira,et al.  Oxidative Stress: A Major Player in Cerebrovascular Alterations Associated to Neurodegenerative Events , 2018, Front. Physiol..

[7]  J. Duarte,et al.  The Role of Nrf2 Signaling in PPARβ/δ-Mediated Vascular Protection against Hyperglycemia-Induced Oxidative Stress , 2018, Oxidative medicine and cellular longevity.

[8]  L. Cucullo,et al.  A convenient UHPLC-MS/MS method for routine monitoring of plasma and brain levels of nicotine and cotinine as a tool to validate newly developed preclinical smoking model in mouse , 2017, BMC Neuroscience.

[9]  T. Abbruscato,et al.  Offsetting the impact of smoking and e-cigarette vaping on the cerebrovascular system and stroke injury: Is Metformin a viable countermeasure? , 2017, Redox biology.

[10]  Leena Kadam,et al.  Rosiglitazone Regulates TLR4 and Rescues HO-1 and NRF2 Expression in Myometrial and Decidual Macrophages in Inflammation-Induced Preterm Birth , 2017, Reproductive Sciences.

[11]  T. Abbruscato,et al.  Role of Nrf2 and protective effects of Metformin against tobacco smoke-induced cerebrovascular toxicity , 2017, Redox biology.

[12]  I. Samudio,et al.  DMSO Represses Inflammatory Cytokine Production from Human Blood Cells and Reduces Autoimmune Arthritis , 2016, PloS one.

[13]  Shafiqur Rahman,et al.  Drugs of abuse and blood-brain barrier endothelial dysfunction: A focus on the role of oxidative stress , 2016, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[14]  L. Cucullo,et al.  Impact of cigarette smoke extract and hyperglycemic conditions on blood–brain barrier endothelial cells , 2015, Fluids and Barriers of the CNS.

[15]  L. Cucullo,et al.  Effect of full flavor and denicotinized cigarettes exposure on the brain microvascular endothelium: a microarray-based gene expression study using a human immortalized BBB endothelial cell line , 2015, BMC Neuroscience.

[16]  L. Cucullo,et al.  Altered Nrf2 Signaling Mediates Hypoglycemia-Induced Blood–Brain Barrier Endothelial Dysfunction In Vitro , 2015, PloS one.

[17]  L. Cucullo,et al.  Differential Cerebrovascular Toxicity of Various Tobacco Products: A Regulatory Perspective , 2015, Journal of pharmacovigilance.

[18]  H. Koh,et al.  Rosiglitazone inhibits chlorpyrifos-induced apoptosis via modulation of the oxidative stress and inflammatory response in SH-SY5Y cells. , 2014, Toxicology and applied pharmacology.

[19]  Neel M. Fofaria,et al.  Oxidative and pro-inflammatory impact of regular and denicotinized cigarettes on blood brain barrier endothelial cells: is smoking reduced or nicotine-free products really safe? , 2014, BMC Neuroscience.

[20]  S. Weber,et al.  NRF2-regulation in brain health and disease: Implication of cerebral inflammation , 2014, Neuropharmacology.

[21]  E. Heiss,et al.  Glucose availability is a decisive factor for Nrf2-mediated gene expression☆ , 2013, Redox biology.

[22]  V. Sapira,et al.  Evaluation of oxidative stress in patients with acute ischemic stroke. , 2013, Romanian journal of internal medicine = Revue roumaine de medecine interne.

[23]  B. Popescu,et al.  Triggers and Effectors of Oxidative Stress at Blood-Brain Barrier Level: Relevance for Brain Ageing and Neurodegeneration , 2013, Oxidative medicine and cellular longevity.

[24]  A. Kakita,et al.  Keap1 Is Localized in Neuronal and Glial Cytoplasmic Inclusions in Various Neurodegenerative Diseases , 2013, Journal of neuropathology and experimental neurology.

[25]  Q. Ma,et al.  Molecular Basis of Electrophilic and Oxidative Defense: Promises and Perils of Nrf2 , 2012, Pharmacological Reviews.

[26]  E. Jakubowska-Dogru,et al.  Rosiglitazone treatment reduces hippocampal neuronal damage possibly through alleviating oxidative stress in chronic cerebral hypoperfusion , 2012, Neurochemistry International.

[27]  Jeffrey N Keller,et al.  Oxidative stress and cerebral endothelial cells: regulation of the blood-brain-barrier and antioxidant based interventions. , 2012, Biochimica et biophysica acta.

[28]  H. Soininen,et al.  Emerging role of p62/sequestosome-1 in the pathogenesis of Alzheimer's disease , 2012, Progress in Neurobiology.

[29]  M. Modo,et al.  Targeting the Nrf2–Keap1 antioxidant defence pathway for neurovascular protection in stroke , 2011, The Journal of physiology.

[30]  S. Liebner,et al.  Current concepts of blood-brain barrier development. , 2011, The International journal of developmental biology.

[31]  T. Ichiki Collaboration between smokers and tobacco in endothelial dysfunction. , 2011, Cardiovascular research.

[32]  Wen Li,et al.  Double antioxidant activities of rosiglitazone against high glucose-induced oxidative stress in hepatocyte. , 2011, Toxicology in vitro : an international journal published in association with BIBRA.

[33]  P. Grammas,et al.  Cerebral microvascular endothelium and the pathogenesis of neurodegenerative diseases , 2011, Expert Reviews in Molecular Medicine.

[34]  K. Tufekci,et al.  The Nrf2/ARE Pathway: A Promising Target to Counteract Mitochondrial Dysfunction in Parkinson's Disease , 2011, Parkinson's disease.

[35]  P. Mazzone,et al.  Pathophysiological Impact of Cigarette Smoke Exposure on the Cerebrovascular System with a Focus on the Blood-brain Barrier: Expanding the Awareness of Smoking Toxicity in an Underappreciated Area , 2010, International journal of environmental research and public health.

[36]  Ferdinando Giacco,et al.  Oxidative stress and diabetic complications. , 2010, Circulation research.

[37]  S. Reddy,et al.  Nrf2-regulated PPAR{gamma} expression is critical to protection against acute lung injury in mice. , 2010, American journal of respiratory and critical care medicine.

[38]  T. Standiford,et al.  Nrf2 and PPAR{gamma}: PPARtnering against oxidant-induced lung injury. , 2010, American journal of respiratory and critical care medicine.

[39]  Y. Shoenfeld,et al.  Effects of tobacco smoke on immunity, inflammation and autoimmunity. , 2010, Journal of autoimmunity.

[40]  C. Klaassen,et al.  Nuclear Factor Erythroid 2-Related Factor 2 Deletion Impairs Glucose Tolerance and Exacerbates Hyperglycemia in Type 1 Diabetic Mice , 2010, Journal of Pharmacology and Experimental Therapeutics.

[41]  T. Davis,et al.  Oxidative Stress Increases Blood–Brain Barrier Permeability and Induces Alterations in Occludin during Hypoxia–Reoxygenation , 2010, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[42]  C. Lin,et al.  Oxidative damage to RNA: mechanisms, consequences, and diseases , 2010, Cellular and Molecular Life Sciences.

[43]  C. J. Van der Schyf,et al.  Nicotine Exacerbates Brain Edema during In Vitro and In Vivo Focal Ischemic Conditions , 2010, Journal of Pharmacology and Experimental Therapeutics.

[44]  David J. Begley,et al.  Structure and function of the blood–brain barrier , 2010, Neurobiology of Disease.

[45]  L. Leybaert,et al.  Peroxisome Proliferator-Activated Receptor γ Activation Alleviates Postoperative Ileus in Mice by Inhibition of Egr-1 Expression and Its Downstream Target Genes , 2009, Journal of Pharmacology and Experimental Therapeutics.

[46]  L. Franco,et al.  Rosiglitazone Reduces Glucose-Induced Oxidative Stress Mediated by NAD(P)H Oxidase via AMPK-Dependent Mechanism , 2007, Arteriosclerosis, thrombosis, and vascular biology.

[47]  S. Reddy,et al.  Gene expression profiling of NRF2-mediated protection against oxidative injury. , 2005, Free radical biology & medicine.

[48]  S. Bolesta,et al.  Rosiglitazone in the treatment of type 2 diabetes mellitus: a critical review. , 2000, Clinical therapeutics.

[49]  S. Dohi,et al.  Mechanisms underlying cerebrovascular effects of cigarette smoking in rats in vivo. , 1998, Stroke.

[50]  Mark Payne,et al.  Health and Human Services , 2020, Congress and the Nation 2013-2016, Volume XIV: Politics and Policy in the 113th and 114th Congresses.

[51]  C. Sobey,et al.  Oxidative stress and endothelial dysfunction in cerebrovascular disease. , 2011, Frontiers in bioscience.

[52]  S. Glantz,et al.  Cigarette smoking is a risk factor for Alzheimer's Disease: an analysis controlling for tobacco industry affiliation. , 2010, Journal of Alzheimer's disease : JAD.