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Endocrine, Metabolic & Immune Disorders - Drug Targets

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ISSN (Online): 2212-3873

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Review Article

Chronic Tobacco Exposure by Smoking Develops Insulin Resistance

Author(s): Suchismita Mukharjee, Sarbashri Bank and Smarajit Maiti*

Volume 20, Issue 6, 2020

Page: [869 - 877] Pages: 9

DOI: 10.2174/1871530320666200217123901

Price: $65

Abstract

Background and Objectives: The present review critically discusses the high occurrence rate, insulin resistance and type-2 diabetes in tobacco exposed individuals. Tobacco extracts and smoke contain a large number of toxic materials and a significant number of those are metabolic disintegrators.

Discussion: Glucose and lipid homeostasis is severely impaired by this compound. Tobacco exposure contributes to adverse effects by impairing the physical, biochemical and molecular mechanisms in the tissues. The immunological components are damaged by tobacco with high production of proinflammatory cytokines (IL-6, TNF-∞) and augmentation of inflammatory responses. These events result in damages to cytoskeletal structures of different tissues. Degradation of matrix structure (by activation of different types of MMPs) results in the permanent damages to the tissues and their metabolic functions. Cellular antioxidant defense system mostly cannot or hardly nullify CS-induced ROS production that activates polymorphonuclear neutrophils (PMNs), which are a major source of cytokines and chemokines (TNFα, IL6, IL8, INFγ). Additive effects of these immediately promote the low energy-metabolism as well as inflammation. Oxidative stress, mitochondrial dysfunction, and inflammation contribute to the direct nicotine toxicity via nAChRs in diabetes. The investigator identified that skeletal muscle insulin-resistance occurs in smokers due to phosphorylation of insulin receptor substrate1 (IRS1) at Ser-636 position.

Conclusion: Tobacco exposure initiates free radical related immunological impairment, DNA damage, and inflammation. So, the present analysis is of importance to figure out the mechanistic layout of tobacco-induced tissue damage and its possible therapeutic interventions.

Keywords: Tobacco consumption, reactive oxygen species, antioxidant systems, inflammatory responses, TNFα /INFγ, pancreatic beta-cell damage, insulin resistance.

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[1]
Heidrich, J.; Wellmann, J.; Heuschmann, P.U.; Kraywinkel, K.; Keil, U. Mortality and morbidity from coronary heart disease attributable to passive smoking. Eur. Heart J., 2007, 28(20), 2498-2502.
[http://dx.doi.org/10.1093/eurheartj/ehm151] [PMID: 17507368]
[2]
Samet, J.M.; Wipfli, H.L. Globe still in grip of addiction. Nature, 2010, 463(7284), 1020-1021.
[http://dx.doi.org/10.1038/4631020a] [PMID: 20182492]
[3]
Houston, T.K.; Person, S.D.; Pletcher, M.J.; Liu, K.; Iribarren, C.; Kiefe, C.I. Active and passive smoking and development of glucose intolerance among young adults in a prospective cohort: CARDIA study. BMJ, 2006, 332(7549), 1064-1069.
[http://dx.doi.org/10.1136/bmj.38779.584028.55] [PMID: 16603565]
[4]
Eliasson, B.; Mero, N.; Taskinen, M.R.; Smith, U. The insulin resistance syndrome and postprandial lipid intolerance in smokers. Atherosclerosis, 1997, 129(1), 79-88.
[http://dx.doi.org/10.1016/S0021-9150(96)06028-5] [PMID: 9069521]
[5]
Attvall, S.; Fowelin, J.; Lager, I.; Von Schenck, H.; Smith, U. Smoking induces insulin resistance--a potential link with the insulin resistance syndrome. J. Intern. Med., 1993, 233(4), 327-332.
[http://dx.doi.org/10.1111/j.1365-2796.1993.tb00680.x] [PMID: 8463765]
[6]
Seet, R.C.S.; Loke, W.M.; Khoo, C.M.; Chew, S.E.; Chong, W.L.; Quek, A.M.; Lim, E.C.; Halliwell, B. Acute effects of cigarette smoking on insulin resistance and arterial stiffness in young adults. Atherosclerosis, 2012, 224(1), 195-200.
[http://dx.doi.org/10.1016/j.atherosclerosis.2012.06.060] [PMID: 22840427]
[7]
Napierala, M.; Merritt, T.A.; Mazela, J.; Jablecka, K.; Miechowicz, I.; Marszalek, A.; Florek, E. The effect of tobacco smoke on oxytocin concentrations and selected oxidative stress parameters in plasma during pregnancy and post-partum - an experimental model. Hum. Exp. Toxicol., 2017, 36(2), 135-145.
[http://dx.doi.org/10.1177/0960327116639363] [PMID: 27009111]
[8]
Śliwińska-Mossoń, M.; Milnerowicz, H. The impact of smoking on the development of diabetes and its complications. Diab. Vasc. Dis. Res., 2017, 265-276.
[9]
Axelsson, T.; Jansson, P.A.; Smith, U.; Eliasson, B. Nicotine infusion acutely impairs insulin sensitivity in type 2 diabetic patients but not in healthy subjects. J. Intern. Med., 2001, 249(6), 539-544.
[http://dx.doi.org/10.1046/j.1365-2796.2001.00840.x] [PMID: 11422660]
[10]
Rönnemaa, T.; Rönnemaa, E.M.; Puukka, P.; Pyörälä, K.; Laakso, M. Smoking is independently associated with high plasma insulin levels in nondiabetic men. Diabetes Care, 1996, 19(11), 1229-1232.
[http://dx.doi.org/10.2337/diacare.19.11.1229] [PMID: 8908385]
[11]
Wang, H.; Liu, X.; Umino, T.; Sköld, C.M.; Zhu, Y.; Kohyama, T.; Spurzem, J.R.; Romberger, D.J.; Rennard, S.I. Cigarette smoke inhibits human bronchial epithelial cell repair processes. Am. J. Respir. Cell Mol. Biol., 2001, 25(6), 772-779.
[http://dx.doi.org/10.1165/ajrcmb.25.6.4458] [PMID: 11726404]
[12]
Bhalla, D.K.; Hirata, F.; Rishi, A.K.; Gairola, C.G. Cigarette smoke, inflammation, and lung injury: a mechanistic perspective. J. Toxicol. Environ. Health B Crit. Rev., 2009, 12(1), 45-64.
[http://dx.doi.org/10.1080/10937400802545094] [PMID: 19117209]
[13]
Bouloukaki, I.; Tsoumakidou, M.; Vardavas, C.I.; Mitrouska, I.; Koutala, E.; Siafakas, N.M.; Schiza, S.E.; Tzanakis, N. Maintained smoking cessation for 6 months equilibrates the percentage of sputum CD8+ lymphocyte cells with that of nonsmokers. Mediators Inflamm., 2009, 2009812102
[http://dx.doi.org/10.1155/2009/812102] [PMID: 20182552]
[14]
Chang, S.A. Smoking and type 2 diabetes mellitus. Diabetes Metab. J., 2012, 36(6), 399-403. [PubMed: 23275932].
[http://dx.doi.org/10.4093/dmj.2012.36.6.399] [PMID: 23275932]
[15]
Cruz, B.; Flores, R.J.; Uribe, K.P.; Espinoza, E.J.; Spencer, C.T.; Serafine, K.M.; Nazarian, A.; O’Dell, L.E. Insulin modulates the strong reinforcing effects of nicotine and changes in insulin biomarkers in a rodent model of diabetes. Neuropsychopharmacology, 2019, 44(6), 1141-1151.
[http://dx.doi.org/10.1038/s41386-018-0306-3] [PMID: 30647447]
[16]
Pipkin, J.A.; Cruz, B.; Flores, R.J.; Hinojosa, C.A.; Carcoba, L.M.; Ibarra, M.; Francis, W.; Nazarian, A.; O’Dell, L.E. Both nicotine reward and withdrawal are enhanced in a rodent model of diabetes. Psychopharmacology (Berl.), 2017, 234(9-10), 1615-1622.
[http://dx.doi.org/10.1007/s00213-017-4592-y] [PMID: 28342091]
[17]
Stämpfli, M.R.; Anderson, G.P. How cigarette smoke skews immune responses to promote infection, lung disease and cancer. Nat. Rev. Immunol., 2009, 9(5), 377-384.
[http://dx.doi.org/10.1038/nri2530] [PMID: 19330016]
[18]
Roisin, RR; Vestbro, J Global initiative for chronic obstructive lung disease., 2011, 1-74.
[19]
Youlden, D.R.; Cramb, S.M.; Baade, P.D. The International Epidemiology of Lung Cancer: geographical distribution and secular trends. J. Thorac. Oncol., 2008, 3(8), 819-831.
[http://dx.doi.org/10.1097/JTO.0b013e31818020eb] [PMID: 18670299]
[20]
Śliwińska-Mossoń, M.; Milnerowicz, S.; Nabzdyk, S.; Kokot, I.; Nowak, M.; Milnerowicz, H. The effect of smoking on endothelin-1 in patients with chronic pancreatitis. Appl. Immunohistochem. Mol. Morphol., 2015, 23(4), 288-296.
[http://dx.doi.org/10.1097/PAI.0000000000000077] [PMID: 25203431]
[21]
Sliwińska-Mossoń, M.; Milnerowicz, H.; Jabłonowska, M.; Milnerowicz, S.; Nabzdyk, S.; Rabczyński, J. The effect of smoking on expression of IL-6 and antioxidants in pancreatic fluids and tissues in patients with chronic pancreatitis. Pancreatology, 2012, 12(4), 295-304.
[http://dx.doi.org/10.1016/j.pan.2012.04.007] [PMID: 22898629]
[22]
Qin, R.; Chen, T.; Lou, Q.; Yu, D. Excess risk of mortality and cardiovascular events associated with smoking among patients with diabetes: meta-analysis of observational prospective studies. Int. J. Cardiol., 2013, 167(2), 342-350.
[http://dx.doi.org/10.1016/j.ijcard.2011.12.100] [PMID: 22251416]
[23]
Jung, K.J.; Yun, Y.D.; Baek, S.J.; Jee, S.H.; Kim, I.S. Smoking-attributable mortality among Korean adults, 2012. J. Korea Soc. Health Inform. Stat., 2013, 38, 36-48.
[24]
Baker, R.R.; Bishop, L.J. The pyrolysis of tobacco ingredients. J. Anal. Appl. Pyrolysis, 2004, 71, 223-331.
[http://dx.doi.org/10.1016/S0165-2370(03)00090-1]
[25]
Mallock, N.; Pieper, E.; Hutzler, C.; Henkler-Stephani, F.; Luch, A. Heated Tobacco Products: A Review of Current Knowledge and Initial Assessments. Front. Public Health, 2019, 7, 287.
[http://dx.doi.org/10.3389/fpubh.2019.00287] [PMID: 31649912]
[26]
Holt, P.G.; Keast, D. Environmentally induced changes in immunological function: Acute and chronic effects of inhalation of tobacco smoke and other atmospheric contaminants in man and experimental animals. Bacteriol. Rev., 1977, 41(1), 205-216.
[PMID: 405003]
[27]
Sopori, M. Effects of cigarette smoke on the immune system. Nat. Rev. Immunol., 2002, 2(5), 372-377.
[http://dx.doi.org/10.1038/nri803] [PMID: 12033743]
[28]
Singh, S.P.; Kalra, R.; Puttfarcken, P.; Kozak, A.; Tesfaigzi, J.; Sopori, M.L. Acute and chronic nicotine exposures modulate the immune system through different pathways. Toxicol. Appl. Pharmacol., 2000, 164(1), 65-72.
[http://dx.doi.org/10.1006/taap.2000.8897] [PMID: 10739745]
[29]
Arcavi, L.; Benowitz, N.L. Cigarette smoking and infection. Arch. Intern. Med., 2004, 164(20), 2206-2216.
[http://dx.doi.org/10.1001/archinte.164.20.2206] [PMID: 15534156]
[30]
Amin, K.; Ekberg-Jansson, A.; Löfdahl, C.G.; Venge, P. Relationship between inflammatory cells and structural changes in the lungs of asymptomatic and never smokers: a biopsy study. Thorax, 2003, 58(2), 135-142.
[http://dx.doi.org/10.1136/thorax.58.2.135] [PMID: 12554896]
[31]
Chrysofakis, G.; Tzanakis, N.; Kyriakoy, D.; Tsoumakidou, M.; Tsiligianni, I.; Klimathianaki, M.; Siafakas, N.M. Perforin expression and cytotoxic activity of sputum CD8+ lymphocytes in patients with COPD. Chest, 2004, 125(1), 71-76.
[http://dx.doi.org/10.1378/chest.125.1.71] [PMID: 14718423]
[32]
Wirtz, P.H.; von Känel, R.; Kunz-Ebrecht, S.; Ehlert, U.; Fischer, J.E. Enhanced glucocorticoid sensitivity of cytokine release from circulating leukocytes stimulated with lipopolysaccharide in healthy male smokers. Brain Behav. Immun., 2004, 18(6), 536-543.
[http://dx.doi.org/10.1016/j.bbi.2004.01.002] [PMID: 15331124]
[33]
Arnson, Y.; Shoenfeld, Y.; Amital, H. Effects of tobacco smoke on immunity, inflammation and autoimmunity. J. Autoimmun., 2010, 34(3), J258-J265.
[http://dx.doi.org/10.1016/j.jaut.2009.12.003] [PMID: 20042314]
[34]
Hoser, G.; Domagała-Kulawik, J.; Droszcz, P.; Droszcz, W.; Kawiak, J. Lymphocyte subsets differences in smokers and nonsmokers with primary lung cancer: A flow cytometry analysis of bronchoalveolar lavage fluid cells. Med. Sci. Monit., 2003, 9(8), BR310-BR315.
[PMID: 12942027]
[35]
Madani, A.; Alack, K.; Richter, M.J.; Krüger, K. Immune-regulating effects of exercise on cigarette smoke-induced inflammation. J. Inflamm. Res., 2018, 11, 155-167.
[http://dx.doi.org/10.2147/JIR.S141149] [PMID: 29731655]
[36]
Gadgil, A.; Duncan, S.R. Role of T-lymphocytes and pro-inflammatory mediators in the pathogenesis of chronic obstructive pulmonary disease. Int. J. Chron. Obstruct. Pulmon. Dis., 2008, 3(4), 531-541.
[PMID: 19281072]
[37]
Lams, B.E.; Sousa, A.R.; Rees, P.J.; Lee, T.H. Subepithelial immunopathology of the large airways in smokers with and without chronic obstructive pulmonary disease. Eur. Respir. J., 2000, 15(3), 512-516.
[http://dx.doi.org/10.1034/j.1399-3003.2000.15.14.x] [PMID: 10759445]
[38]
Churg, A.; Cosio, M.; Wright, J.L. Mechanisms of cigarette smoke-induced COPD: insights from animal models. Am. J. Physiol. Lung Cell. Mol. Physiol., 2008, 294(4), L612-L631.
[http://dx.doi.org/10.1152/ajplung.00390.2007] [PMID: 18223159]
[39]
Crotty Alexander, L.E.; Shin, S.; Hwang, J.H. Inflammatory diseases of the lung induced by conventional cigarette smoke: A review. Chest, 2015, 148(5), 1307-1322.
[http://dx.doi.org/10.1378/chest.15-0409] [PMID: 26135024]
[40]
Ribeiro, F.; Alves, A.J.; Duarte, J.A.; Oliveira, J. Is exercise training an effective therapy targeting endothelial dysfunction and vascular wall inflammation? Int. J. Cardiol., 2010, 141(3), 214-221.
[http://dx.doi.org/10.1016/j.ijcard.2009.09.548] [PMID: 19896741]
[41]
Wijnhoven, H.J.; Heunks, L.M.; Geraedts, M.C.; Hafmans, T.; Viña, J.R.; Dekhuijzen, P.N. Oxidative and nitrosative stress in the diaphragm of patients with COPD. Int. J. Chron. Obstruct. Pulmon. Dis., 2006, 1(2), 173-179.
[http://dx.doi.org/10.2147/copd.2006.1.2.173] [PMID: 18046894]
[42]
Ansarin, K.; Chatkin, J.M.; Ferreira, I.M.; Gutierrez, C.A.; Zamel, N.; Chapman, K.R. Exhaled nitric oxide in chronic obstructive pulmonary disease: relationship to pulmonary function. Eur. Respir. J., 2001, 17(5), 934-938.
[http://dx.doi.org/10.1183/09031936.01.17509340] [PMID: 11488329]
[43]
MacNee, W. Pulmonary and systemic oxidant/antioxidant imbalance in chronic obstructive pulmonary disease. Proc. Am. Thorac. Soc., 2005, 2(1), 50-60.
[http://dx.doi.org/10.1513/pats.200411-056SF] [PMID: 16113469]
[44]
Bruin, J.; Gerstein, H.; Morrison, K.; Holloway, A. Increased pancreatic beta cell apoptosis following fetal and noenatal exposure to nicotine is mediated via the mitochondria. Toxicol. Sci., in press
[45]
Fischer, R.; Maier, O. Interrelation of oxidative stress and inflammation in neurodegenerative disease: role of TNF. Oxid. Med. Cell. Longev., 2015, 2015610813
[http://dx.doi.org/10.1155/2015/610813] [PMID: 25834699]
[46]
Aravamudan, B.; Kiel, A.; Freeman, M.; Delmotte, P.; Thompson, M.; Vassallo, R.; Sieck, G.C.; Pabelick, C.M.; Prakash, Y.S. Cigarette smoke-induced mitochondrial fragmentation and dysfunction in human airway smooth muscle. Am. J. Physiol. Lung Cell. Mol. Physiol., 2014, 306(9), L840-L854.
[http://dx.doi.org/10.1152/ajplung.00155.2013] [PMID: 24610934]
[47]
Fetterman, J.L.; Sammy, M.J.; Ballinger, S.W. Mitochondrial toxicity of tobacco smoke and air pollution. Toxicology, 2017, 391, 18-33.
[http://dx.doi.org/10.1016/j.tox.2017.08.002] [PMID: 28838641]
[48]
Ashcroft, F.M.; Rorsman, P. ATP-sensitive K+ channels: a link between B-cell metabolism and insulin secretion. Biochem. Soc. Trans., 1990, 18(1), 109-111.
[http://dx.doi.org/10.1042/bst0180109] [PMID: 2185070]
[49]
Pravenec, M. Direct linkage of mitochondrial genome variation to risk factors for type 2 diabetes in conplastic strains. Genome Res., 2007, 17(9), 1319-26.
[50]
Glossop, J.R.; Dawes, P.T.; Mattey, D.L. Association between cigarette smoking and release of tumour necrosis factor alpha and its soluble receptors by peripheral blood mononuclear cells in patients with rheumatoid arthritis. Rheumatology (Oxford), 2006, 45(10), 1223-1229.
[http://dx.doi.org/10.1093/rheumatology/kel094] [PMID: 16585133]
[51]
Churg, A.; Zhou, S.; Wang, X.; Wang, R.; Wright, J.L. The role of interleukin-1beta in murine cigarette smoke-induced emphysema and small airway remodeling. Am. J. Respir. Cell Mol. Biol., 2009, 40(4), 482-490.
[http://dx.doi.org/10.1165/rcmb.2008-0038OC] [PMID: 18931327]
[52]
Southworth, T.; Metryka, A.; Lea, S.; Farrow, S.; Plumb, J.; Singh, D. IFN-gamma synergistically enhances LPS signalling in alveolar macrophages from COPD patients and controls by corticosteroid-resistant STAT1 activation. Br. J. Pharmacol., 2012, 166(7), 2070-2083.
[53]
Wang, X.; Bao, W.; Liu, J.; Ouyang, Y.Y.; Wang, D.; Rong, S.; Xiao, X.; Shan, Z.L.; Zhang, Y.; Yao, P.; Liu, L.G. Inflammatory markers and risk of type 2 diabetes: a systematic review and meta-analysis. Diabetes Care, 2013, 36(1), 166-175.
[http://dx.doi.org/10.2337/dc12-0702] [PMID: 23264288]
[54]
Harju, T.; Kaarteenaho-Wiik, R.; Sirviö, R.; Pääkkö, P.; Crapo, J.D.; Oury, T.D.; Soini, Y.; Kinnula, V.L. Manganese superoxide dismutase is increased in the airways of smokers’ lungs. Eur. Respir. J., 2004, 24(5), 765-771.
[http://dx.doi.org/10.1183/09031936.04.00121203] [PMID: 15516670]
[55]
MacNee, W. Oxidants and COPD. Curr. Drug Targets Inflamm. Allergy, 2005, 4(6), 627-641.
[http://dx.doi.org/10.2174/156801005774912815] [PMID: 17305519]
[56]
Zuo, L.; Clanton, T.L. Reactive oxygen species formation in the transition to hypoxia in skeletal muscle. Am. J. Physiol. Cell Physiol., 2005, 289(1), C207-C216.
[http://dx.doi.org/10.1152/ajpcell.00449.2004] [PMID: 15788484]
[57]
Yoshikawa, H.; Hellström-Lindahl, E.; Grill, V. Evidence for functional nicotinic receptors on pancreatic beta cells. Metabolism, 2005, 54(2), 247-254.
[http://dx.doi.org/10.1016/j.metabol.2004.08.020] [PMID: 15690320]
[58]
Bruin, J.E.; Gerstein, H.C.; Holloway, A.C. Long-term consequences of fetal and neonatal nicotine exposure: a critical review. Toxicol. Sci., 2010, 116(2), 364-374.
[http://dx.doi.org/10.1093/toxsci/kfq103] [PMID: 20363831]
[59]
Bruin, J.E.; Petre, M.A.; Lehman, M.A.; Raha, S.; Gerstein, H.C.; Morrison, K.M.; Holloway, A.C. Maternal nicotine exposure increases oxidative stress in the offspring. Free Radic. Biol. Med., 2008, 44(11), 1919-1925.
[http://dx.doi.org/10.1016/j.freeradbiomed.2008.02.010] [PMID: 18343235]
[60]
Bergman, B.C.; Perreault, L.; Hunerdosse, D.; Kerege, A.; Playdon, M.; Samek, A.M.; Eckel, R.H. Novel and reversible mechanisms of smoking-induced insulin resistance in humans. Diabetes, 2012, 61(12), 3156-3166.
[http://dx.doi.org/10.2337/db12-0418] [PMID: 22966072]
[61]
Asthana, A.; Johnson, H.M.; Piper, M.E.; Fiore, M.C.; Baker, T.B.; Stein, J.H. Effects of smoking intensity and cessation on inflammatory markers in a large cohort of active smokers. Am. Heart J., 2010, 160(3), 458-463.
[http://dx.doi.org/10.1016/j.ahj.2010.06.006] [PMID: 20826253]
[62]
Pradhan, A.D.; Manson, J.E.; Rifai, N.; Buring, J.E.; Ridker, P.M. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA, 2001, 286(3), 327-334.
[http://dx.doi.org/10.1001/jama.286.3.327] [PMID: 11466099]
[63]
Grassi, G.; Seravalle, G.; Calhoun, D.A.; Bolla, G.B.; Giannattasio, C.; Marabini, M.; Del Bo, A.; Mancia, G. Mechanisms responsible for sympathetic activation by cigarette smoking in humans. Circulation, 1994, 90(1), 248-253.
[http://dx.doi.org/10.1161/01.CIR.90.1.248] [PMID: 8026005]
[64]
Hellerstein, M.K.; Benowitz, N.L.; Neese, R.A.; Schwartz, J.M.; Hoh, R.; Jacob, P., III; Hsieh, J.; Faix, D. Effects of cigarette smoking and its cessation on lipid metabolism and energy expenditure in heavy smokers. J. Clin. Invest., 1994, 93(1), 265-272.
[http://dx.doi.org/10.1172/JCI116955] [PMID: : 8282797]
[65]
Borowitz, J.L.; Isom, G.E. Nicotine and type 2 diabetes. Toxicol. Sci., 2008, 103(2), 225-227.
[http://dx.doi.org/10.1093/toxsci/kfn050] [PMID: 18353801]
[66]
Leff, T.; Mathews, S.T.; Camp, H.S. Review: peroxisome proliferator-activated receptor-gamma and its role in the development and treatment of diabetes. Exp. Diabesity Res., 2004, 5(2), 99-109.
[http://dx.doi.org/10.1080/15438600490451668] [PMID: 15203881]
[67]
Holloway, A.C.; Lim, G.E.; Petrik, J.J.; Foster, W.G.; Morrison, K.M.; Gerstein, H.C. Fetal and neonatal exposure to nicotine in Wistar rats results in increased beta cell apoptosis at birth and postnatal endocrine and metabolic changes associated with type 2 diabetes. Diabetologia, 2005, 48(12), 2661-2666.
[http://dx.doi.org/10.1007/s00125-005-0022-5] [PMID: 16270195]
[68]
An, D.; Rodrigues, B. Role of changes in cardiac metabolism in development of diabetic cardiomyopathy. Am. J. Physiol. Heart Circ. Physiol., 2006, 291(4), H1489-H1506.
[http://dx.doi.org/10.1152/ajpheart.00278.2006] [PMID: 16751293]
[69]
Gudz, T.I.; Tserng, K.Y.; Hoppel, C.L. Direct inhibition of mitochondrial respiratory chain complex III by cell-permeable ceramide. J. Biol. Chem., 1997, 272(39), 24154-24158.
[http://dx.doi.org/10.1074/jbc.272.39.24154] [PMID: 9305864]
[70]
Yang, Y.M.; Liu, G.T. Damaging effect of cigarette smoke extract on primary cultured human umbilical vein endothelial cells and its mechanism. Biomed. Environ. Sci., 2004, 17(2), 121-134.
[PMID: 15386938]
[71]
Dabkowski, E.R.; Baseler, W.A.; Williamson, C.L.; Powell, M.; Razunguzwa, T.T.; Frisbee, J.C.; Hollander, J.M. Mitochondrial dysfunction in the type 2 diabetic heart is associated with alterations in spatially distinct mitochondrial proteomes. Am. J. Physiol. Heart Circ. Physiol., 2010, 299(2), H529-H540.
[http://dx.doi.org/10.1152/ajpheart.00267.2010] [PMID: 20543078]

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