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Published in: Comparative Clinical Pathology 2/2015

01-03-2015 | Original Article

Effect of adipose tissue-derived mesenchymal stem cell treatment on oxidative stress and inflammatory response following Escherichia coli lipopolysaccharide

Authors: Omar M. E. Abdel-Salam, Eman R. Youness, Enayat A. Omara, Amany A. Sleem

Published in: Comparative Clinical Pathology | Issue 2/2015

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Abstract

Stem cells are the focus of extensive experimental and clinical research with the aim of replacing lost or damaged tissues. This paper studies the effect of systemic stem cell injections on the redox status of the brain and liver in a model of systemic inflammatory illness. Mice were treated with intraperitoneal (i.p.) injection of adipose tissue-derived mesenchymal stem cell (AT-MSCs) suspension, or saline at time of lipopolysaccharide (LPS; 200 mg/kg, i.p.) administration and euthanized 4 h later. Results show that the administration of LPS increased the oxidative stress in the brain and liver tissues. Malondialdehyde (MDA) increased by 53 and 68.9 %, reduced glutathione (GSH) decreased by 44.4 and 50.6 %, and nitric oxide increased by 47.7 and 87.2 % in the brain and liver, respectively. Total antioxidant capacity (TAC) decreased by 37.8 and 76.2 %, catalase activity decreased by 58.2 and 29.2 %, and paraoxonase 1 (PON1) activity decreased by 53.1 and 22.5 % in the brain and liver, respectively. In addition, nuclear factor kappa B (NF-κB) and the monocyte chemoattractant protein-1 (MCP-1) increased in the brain and liver, respectively, after endotoxin injection. Mice treated with AT-MSCs showed unchanged MDA, increased brain GSH (45.5 %), TAC (171.1 %), catalase activity (58.4 %), and PON1 activity (110.4 %). In the liver, MDA and catalase activity were unchanged, but TAC decreased by −36.7 % and PON1 activity decreased by −22.8 %. NF-κB decreased in the liver, while MCP-1 decreased in the brain and liver by AT-MSCs treatment. AT-MSCs reduced inflammatory cell infiltration and necrotic damage in the liver and markedly decreased the number of degenerated neurons in the cortex and striatum in LPS-treated mice. Stem cell treatment was associated with lower tumor necrosis factor-alpha (TNF-α), inducible nitric oxide synthase (iNOS), and caspase-3 immunoreactivity in the brain (cortex and striatum) and liver tissues compared to that in the LPS control group. Thus, the systemic administration of AT-MSCs suspension in a model of mild systemic illness modulates the cellular oxidative response and exerts anti-inflammatory effect. AT-MSCs prevent tissue injury via decreased nitric oxide generation due to iNOS expression and decreased activation of caspase-3, TNF-α, and MCP-1.
Literature
go back to reference Akahane K, Okamoto K, Kikuchi M, Todoroki H, Higure A, Ohuchida T, Kitahara K, Takeda S, Itoh H, Ohsato K (2001) Inhibition of factor Xa suppresses the expression of tissue factor in human monocytes and lipopolysaccharide-induced endotoxemia in rats. Surgery 130:809–818CrossRefPubMed Akahane K, Okamoto K, Kikuchi M, Todoroki H, Higure A, Ohuchida T, Kitahara K, Takeda S, Itoh H, Ohsato K (2001) Inhibition of factor Xa suppresses the expression of tissue factor in human monocytes and lipopolysaccharide-induced endotoxemia in rats. Surgery 130:809–818CrossRefPubMed
go back to reference Aleksandrova MA, Poltavtseva RA, Revishchin AV, Korochkin LI, Sukhikh GT (2004) Development of neural stem/progenitor cells from human brain by transplantation into the brains of adult rats. Neurosci Behav Physiol 34:659–662CrossRefPubMed Aleksandrova MA, Poltavtseva RA, Revishchin AV, Korochkin LI, Sukhikh GT (2004) Development of neural stem/progenitor cells from human brain by transplantation into the brains of adult rats. Neurosci Behav Physiol 34:659–662CrossRefPubMed
go back to reference Andjelkovic AV, Kerkovich D, Pachter JS (2000) Monocyte:astrocyte interactions regulate MCP-1 expression in both cell types. J Leukoc Biol 68:545–552PubMed Andjelkovic AV, Kerkovich D, Pachter JS (2000) Monocyte:astrocyte interactions regulate MCP-1 expression in both cell types. J Leukoc Biol 68:545–552PubMed
go back to reference Andrews EM, Tsai SY, Johnson SC, Farrer JR, Wagner JP, Kopen GC, Kartje GL (2008) Human adult bone marrow-derived somatic cell therapy results in functional recovery and axonal plasticity following stroke in the rat. Exp Neurol 211:588–592CrossRefPubMedCentralPubMed Andrews EM, Tsai SY, Johnson SC, Farrer JR, Wagner JP, Kopen GC, Kartje GL (2008) Human adult bone marrow-derived somatic cell therapy results in functional recovery and axonal plasticity following stroke in the rat. Exp Neurol 211:588–592CrossRefPubMedCentralPubMed
go back to reference Bacigaluppi M, Pluchino S, Jametti LP, Kilic E, Kilic U, Salani G, Brambilla E, West MJ, Comi G, Martino G, Hermann DM (2009) Delayed post-ischaemic neuroprotection following systemic neural stem cell transplantation involves multiple mechanisms. Brain 132:2239–2251CrossRefPubMed Bacigaluppi M, Pluchino S, Jametti LP, Kilic E, Kilic U, Salani G, Brambilla E, West MJ, Comi G, Martino G, Hermann DM (2009) Delayed post-ischaemic neuroprotection following systemic neural stem cell transplantation involves multiple mechanisms. Brain 132:2239–2251CrossRefPubMed
go back to reference Bal-Price A, Brown GC (2000) Nitric-oxide-induced necrosis and apoptosis in PC12 cells mediated by mitochondria. J Neurochem 75:1455–1464CrossRefPubMed Bal-Price A, Brown GC (2000) Nitric-oxide-induced necrosis and apoptosis in PC12 cells mediated by mitochondria. J Neurochem 75:1455–1464CrossRefPubMed
go back to reference Bantel H, Lügering A, Poremba C, Lügering N, Held J, Domschke W, Schulze-Osthoff K (2001) Caspase activation correlates with the degree of inflammatory liver injury in chronic hepatitis C virus infection. Hepatology 34(4 Pt 1):758–767CrossRefPubMed Bantel H, Lügering A, Poremba C, Lügering N, Held J, Domschke W, Schulze-Osthoff K (2001) Caspase activation correlates with the degree of inflammatory liver injury in chronic hepatitis C virus infection. Hepatology 34(4 Pt 1):758–767CrossRefPubMed
go back to reference Beurel E, Jope RS (2009) Lipopolysaccharide-induced interleukin-6 production is controlled by glycogen synthase kinase-3 and STAT3 in the brain. J Neuroinflammation 6:9CrossRefPubMedCentralPubMed Beurel E, Jope RS (2009) Lipopolysaccharide-induced interleukin-6 production is controlled by glycogen synthase kinase-3 and STAT3 in the brain. J Neuroinflammation 6:9CrossRefPubMedCentralPubMed
go back to reference Blackwell TS, Christman JW (1997) The role of nuclear factor-kappa B in cytokine gene regulation. Am J Respir Cell Mol Biol 17:3–9CrossRefPubMed Blackwell TS, Christman JW (1997) The role of nuclear factor-kappa B in cytokine gene regulation. Am J Respir Cell Mol Biol 17:3–9CrossRefPubMed
go back to reference Blau HM, Brazelton TR, Weimann JM (2001) The evolving concept of a stem cell: entity or function? Cell 105:829–841CrossRefPubMed Blau HM, Brazelton TR, Weimann JM (2001) The evolving concept of a stem cell: entity or function? Cell 105:829–841CrossRefPubMed
go back to reference Buja LM, Vela D (2010) Immunologic and inflammatory reactions to exogenous stem cells implications for experimental studies and clinical trials for myocardial repair. J Am Coll Cardiol 56:1693–1700CrossRefPubMed Buja LM, Vela D (2010) Immunologic and inflammatory reactions to exogenous stem cells implications for experimental studies and clinical trials for myocardial repair. J Am Coll Cardiol 56:1693–1700CrossRefPubMed
go back to reference Cao C, Matsumura K, Yamagata K, Watanabe Y (1995) Induction by lipopolysaccharide of cyclooxygenase-2 mRNA in rat brain; its possible role in the febrile response. Brain Res 697:187–196CrossRefPubMed Cao C, Matsumura K, Yamagata K, Watanabe Y (1995) Induction by lipopolysaccharide of cyclooxygenase-2 mRNA in rat brain; its possible role in the febrile response. Brain Res 697:187–196CrossRefPubMed
go back to reference Chen F, Castranova V, Shi X, Demers LM (1999) New insights into the role of nuclear factor-kappaB, a ubiquitous transcription factor in the initiation of diseases. Clin Chem 45:7–17PubMed Chen F, Castranova V, Shi X, Demers LM (1999) New insights into the role of nuclear factor-kappaB, a ubiquitous transcription factor in the initiation of diseases. Clin Chem 45:7–17PubMed
go back to reference Crowley LV (1967) The Reitman-Frankel colorimetric transaminase procedure in suspected myocardial infarction. Clin Chem 13:482–487PubMed Crowley LV (1967) The Reitman-Frankel colorimetric transaminase procedure in suspected myocardial infarction. Clin Chem 13:482–487PubMed
go back to reference Czaja MJ, Geerts A, Xu J, Schmiedeberg P, Ju Y (1994) Monocyte chemoattractant protein 1 (MCP-1) expression occurs in toxic rat liver injury and human liver disease. J Leukoc Biol 55:120–126PubMed Czaja MJ, Geerts A, Xu J, Schmiedeberg P, Ju Y (1994) Monocyte chemoattractant protein 1 (MCP-1) expression occurs in toxic rat liver injury and human liver disease. J Leukoc Biol 55:120–126PubMed
go back to reference Czapski GA, Cakala M, Chalimoniuk M, Gajkowska B, Strosznajder JB (2007) Role of nitric oxide in the brain during lipopolysaccharide-evoked systemic inflammation. J Neurosci Res 85:1694–1703CrossRefPubMed Czapski GA, Cakala M, Chalimoniuk M, Gajkowska B, Strosznajder JB (2007) Role of nitric oxide in the brain during lipopolysaccharide-evoked systemic inflammation. J Neurosci Res 85:1694–1703CrossRefPubMed
go back to reference Dawson TM, Dawson VL (2002) Neuroprotective and neurorestorative strategies for Parkinson’s disease. Nat Neurosci 5(Suppl):1058–1061CrossRefPubMed Dawson TM, Dawson VL (2002) Neuroprotective and neurorestorative strategies for Parkinson’s disease. Nat Neurosci 5(Suppl):1058–1061CrossRefPubMed
go back to reference de Wert G, Mummery C (2003) Human embryonic stem cells: research, ethics and policy. Hum Reprod 18:672–682CrossRefPubMed de Wert G, Mummery C (2003) Human embryonic stem cells: research, ethics and policy. Hum Reprod 18:672–682CrossRefPubMed
go back to reference Einstein O, Fainstein N, Vaknin I, Mizrachi-Kol R, Reihartz E, Grigoriadis N, Lavon I, Baniyash M, Lassmann H, Ben-Hur T (2007) Neural precursors attenuate autoimmune encephalomyelitis by peripheral immunosuppression. Ann Neurol 61:209–218CrossRefPubMed Einstein O, Fainstein N, Vaknin I, Mizrachi-Kol R, Reihartz E, Grigoriadis N, Lavon I, Baniyash M, Lassmann H, Ben-Hur T (2007) Neural precursors attenuate autoimmune encephalomyelitis by peripheral immunosuppression. Ann Neurol 61:209–218CrossRefPubMed
go back to reference Furlong CE, Suzuki SM, Stevens RC, Marsillach J, Richter RJ, Jarvik GP, Checkoway H, Samii A, Costa LG, Griffith A, Roberts JW, Yearout D, Zabetian CP (2010) Human PON1, a biomarker of risk of disease and exposure. Chem Biol Interact 187:355–361CrossRefPubMedCentralPubMed Furlong CE, Suzuki SM, Stevens RC, Marsillach J, Richter RJ, Jarvik GP, Checkoway H, Samii A, Costa LG, Griffith A, Roberts JW, Yearout D, Zabetian CP (2010) Human PON1, a biomarker of risk of disease and exposure. Chem Biol Interact 187:355–361CrossRefPubMedCentralPubMed
go back to reference Gill R, Soriano M, Blomgren K, Hagberg H, Wybrecht R, Miss MT, Hoefer S, Adam G, Niederhauser O, Kemp JA, Loetscher H (2002) Role of caspase-3 activation in cerebral ischemia-induced neurodegeneration in adult and neonatal brain. J Cereb Blood Flow Metab 22:420–430CrossRefPubMed Gill R, Soriano M, Blomgren K, Hagberg H, Wybrecht R, Miss MT, Hoefer S, Adam G, Niederhauser O, Kemp JA, Loetscher H (2002) Role of caspase-3 activation in cerebral ischemia-induced neurodegeneration in adult and neonatal brain. J Cereb Blood Flow Metab 22:420–430CrossRefPubMed
go back to reference Glabinski AR, Balasingam V, Tani M, Kunkel SL, Strieter RM, Wee Yong V, Ransohoff RM (1996) Chemokine monocyte chemoattractant protein-1 is expressed by astrocytes after mechanical injury to the brain. J Immunol 156:4363–4368PubMed Glabinski AR, Balasingam V, Tani M, Kunkel SL, Strieter RM, Wee Yong V, Ransohoff RM (1996) Chemokine monocyte chemoattractant protein-1 is expressed by astrocytes after mechanical injury to the brain. J Immunol 156:4363–4368PubMed
go back to reference Grisham MB, Jourd’Heuil D, Wink DA (1999) Nitric oxide. I. Physiological chemistry of nitric oxide and its metabolites: implications in inflammation. Am J Physiol 276:G315–G321PubMed Grisham MB, Jourd’Heuil D, Wink DA (1999) Nitric oxide. I. Physiological chemistry of nitric oxide and its metabolites: implications in inflammation. Am J Physiol 276:G315–G321PubMed
go back to reference Gutteridge JMC (1995) Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clin Chem 41:1819–1828PubMed Gutteridge JMC (1995) Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clin Chem 41:1819–1828PubMed
go back to reference Guzman R, Uchida N, Bliss TM, He D, Christopherson KK, Stellwagen D, Capela A, Greve J, Malenka RC, Moseley ME, Palmer TD, Steinberg GK (2007) Long-term monitoring of transplanted human neural stem cells in developmental and pathological contexts with MRI. Proc Natl Acad Sci U S A 104:10211–10216CrossRefPubMedCentralPubMed Guzman R, Uchida N, Bliss TM, He D, Christopherson KK, Stellwagen D, Capela A, Greve J, Malenka RC, Moseley ME, Palmer TD, Steinberg GK (2007) Long-term monitoring of transplanted human neural stem cells in developmental and pathological contexts with MRI. Proc Natl Acad Sci U S A 104:10211–10216CrossRefPubMedCentralPubMed
go back to reference Heng BC, Cao T, Haider HK, Wang DZ, Sim EK, Ng SC (2004) An overview and synopsis of techniques for directing stem cell differentiation in vitro. Cell Tissue Res 315:291–303CrossRefPubMed Heng BC, Cao T, Haider HK, Wang DZ, Sim EK, Ng SC (2004) An overview and synopsis of techniques for directing stem cell differentiation in vitro. Cell Tissue Res 315:291–303CrossRefPubMed
go back to reference Higashino K, Takahashi Y, Yamamura Y (1972) Release of phenyl acetate esterase from liver microsomes by carbon tetrachloride. Clin Chim Acta 41:313–320CrossRefPubMed Higashino K, Takahashi Y, Yamamura Y (1972) Release of phenyl acetate esterase from liver microsomes by carbon tetrachloride. Clin Chim Acta 41:313–320CrossRefPubMed
go back to reference Hollis JH, Lemus M, Evetts MJ, Oldfield BJ (2010) Central interleukin-10 attenuates lipopolysaccharide-induced changes in food intake, energy expenditure and hypothalamic Fos expression. Neuropharmacology 58:730–738CrossRefPubMed Hollis JH, Lemus M, Evetts MJ, Oldfield BJ (2010) Central interleukin-10 attenuates lipopolysaccharide-induced changes in food intake, energy expenditure and hypothalamic Fos expression. Neuropharmacology 58:730–738CrossRefPubMed
go back to reference Hua XY, Chen P, Fox A, Myers RR (1996) Involvement of cytokines in lipopolysaccharide-induced facilitation of CGRP release from capsaicin-sensitive nerves in the trachea: studies with interleukin-1beta and tumor necrosis factor-alpha. J Neurosci 16:4742–4748PubMed Hua XY, Chen P, Fox A, Myers RR (1996) Involvement of cytokines in lipopolysaccharide-induced facilitation of CGRP release from capsaicin-sensitive nerves in the trachea: studies with interleukin-1beta and tumor necrosis factor-alpha. J Neurosci 16:4742–4748PubMed
go back to reference Huang DR, Wang J, Kivisakk P, Rollins BJ, Ransohoff RM (2001) Absence of monocyte chemoattractant protein-1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J Exp Med 193:713–726CrossRefPubMedCentralPubMed Huang DR, Wang J, Kivisakk P, Rollins BJ, Ransohoff RM (2001) Absence of monocyte chemoattractant protein-1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J Exp Med 193:713–726CrossRefPubMedCentralPubMed
go back to reference Irons H, Lind JG, Wakade CG, Yu G, Hadman M, Carroll J, Hess DC, Borlongan CV (2004) Intracerebral xenotransplantation of GFP mouse bone marrow stromal cells in intact and stroke rat brain: graft survival and immunologic response. Cell Transplant 13:283–294CrossRefPubMed Irons H, Lind JG, Wakade CG, Yu G, Hadman M, Carroll J, Hess DC, Borlongan CV (2004) Intracerebral xenotransplantation of GFP mouse bone marrow stromal cells in intact and stroke rat brain: graft survival and immunologic response. Cell Transplant 13:283–294CrossRefPubMed
go back to reference Jacewicz M, Czapski GA, Katkowska I, Strosznajder RP (2009) Systemic administration of lipopolysaccharide impairs glutathione redox state and object recognition in male mice. The effect of PARP-1 inhibitor. Folia Neuropathol 47:321–328PubMed Jacewicz M, Czapski GA, Katkowska I, Strosznajder RP (2009) Systemic administration of lipopolysaccharide impairs glutathione redox state and object recognition in male mice. The effect of PARP-1 inhibitor. Folia Neuropathol 47:321–328PubMed
go back to reference Jayakumar AR, Bethea JR, Tong XY, Gomez J, Norenberg MD (2011) NF-κB in the mechanism of brain edema in acute liver failure: studies in transgenic mice. Neurobiol Dis 41:498–507CrossRefPubMedCentralPubMed Jayakumar AR, Bethea JR, Tong XY, Gomez J, Norenberg MD (2011) NF-κB in the mechanism of brain edema in acute liver failure: studies in transgenic mice. Neurobiol Dis 41:498–507CrossRefPubMedCentralPubMed
go back to reference Jeong H-K, Jou I, Joe EH (2010) Systemic LPS administration induces brain inflammation but not dopaminergic neuronal death in the substantia nigra. Exp Mol Med 42:823–832CrossRefPubMedCentralPubMed Jeong H-K, Jou I, Joe EH (2010) Systemic LPS administration induces brain inflammation but not dopaminergic neuronal death in the substantia nigra. Exp Mol Med 42:823–832CrossRefPubMedCentralPubMed
go back to reference Karin M, Delhase M (2000) The I kappaB kinase (IKK) and NF-kappaB: key elements of proinflammatory signaling. Semin Immunol 12:85–98CrossRefPubMed Karin M, Delhase M (2000) The I kappaB kinase (IKK) and NF-kappaB: key elements of proinflammatory signaling. Semin Immunol 12:85–98CrossRefPubMed
go back to reference Kilroy GE, Foster SJ, Wu X, Ruiz J, Sherwood S, Heifetz A, Ludlow JW, Stricker DM, Potiny S, Green P, Halvorsen YD, Cheatham B, Storms RW, Gimble JM (2007) Cytokine profile of human adipose-derived stem cells: expression of angiogenic, hematopoietic, and pro-inflammatory factors. J Cell Physiol 212:702–709CrossRefPubMed Kilroy GE, Foster SJ, Wu X, Ruiz J, Sherwood S, Heifetz A, Ludlow JW, Stricker DM, Potiny S, Green P, Halvorsen YD, Cheatham B, Storms RW, Gimble JM (2007) Cytokine profile of human adipose-derived stem cells: expression of angiogenic, hematopoietic, and pro-inflammatory factors. J Cell Physiol 212:702–709CrossRefPubMed
go back to reference Kim JS, Gautam SC, Chopp M, Zaloga C, Jones ML, Ward PA, Welch KM (1995) Expression of monocyte chemoattractant protein-1 and macrophage inflammatory protein-1 after focal cerebral ischemia in the rat. J Neuroimmunol 56:127–134CrossRefPubMed Kim JS, Gautam SC, Chopp M, Zaloga C, Jones ML, Ward PA, Welch KM (1995) Expression of monocyte chemoattractant protein-1 and macrophage inflammatory protein-1 after focal cerebral ischemia in the rat. J Neuroimmunol 56:127–134CrossRefPubMed
go back to reference Kolios G, Valatas V, Manousou P, Xidakis C, Notas G, Kouroumalis E (2008) Nitric oxide and MCP-1 regulation in LPS activated rat Kupffer cells. Mol Cell Biochem 319:91–98CrossRefPubMed Kolios G, Valatas V, Manousou P, Xidakis C, Notas G, Kouroumalis E (2008) Nitric oxide and MCP-1 regulation in LPS activated rat Kupffer cells. Mol Cell Biochem 319:91–98CrossRefPubMed
go back to reference Koo JW, Russo SJ, Ferguson D, Nestler EJ, Duman RS (2010) Nuclear factor-kappaB is a critical mediator of stress-impaired neurogenesis and depressive behavior. Proc Natl Acad Sci U S A 107:2669–2674CrossRefPubMedCentralPubMed Koo JW, Russo SJ, Ferguson D, Nestler EJ, Duman RS (2010) Nuclear factor-kappaB is a critical mediator of stress-impaired neurogenesis and depressive behavior. Proc Natl Acad Sci U S A 107:2669–2674CrossRefPubMedCentralPubMed
go back to reference Kratsovnik E, Bromberg Y, Sperling O, Zoref-Shani E (2005) Oxidative stress activates transcription factor NF-kB-mediated protective signaling in primary rat neuronal cultures. J Mol Neurosci 26:27–32CrossRefPubMed Kratsovnik E, Bromberg Y, Sperling O, Zoref-Shani E (2005) Oxidative stress activates transcription factor NF-kB-mediated protective signaling in primary rat neuronal cultures. J Mol Neurosci 26:27–32CrossRefPubMed
go back to reference Lee ST, Chu K, Park JE, Lee K, Kang L, Kim SU, Kim M (2005) Intravenous administration of human neural stem cells induces functional recovery in Huntington’s disease rat model. Neurosci Res 52:243–249CrossRefPubMed Lee ST, Chu K, Park JE, Lee K, Kang L, Kim SU, Kim M (2005) Intravenous administration of human neural stem cells induces functional recovery in Huntington’s disease rat model. Neurosci Res 52:243–249CrossRefPubMed
go back to reference Lee HJ, Kim KS, Kim EJ, Choi HB, Lee KH, Park IH, Ko Y, Jeong SW, Kim SU (2007) Brain transplantation of immortalized human neural stem cells promotes functional recovery in mouse intracerebral hemorrhage stroke model. Stem Cells 25:1204–1212CrossRefPubMed Lee HJ, Kim KS, Kim EJ, Choi HB, Lee KH, Park IH, Ko Y, Jeong SW, Kim SU (2007) Brain transplantation of immortalized human neural stem cells promotes functional recovery in mouse intracerebral hemorrhage stroke model. Stem Cells 25:1204–1212CrossRefPubMed
go back to reference Lee ST, Chu K, Jung KH, Kim SJ, Kim DH, Kang KM, Hong NH, Kim JH, Ban JJ, Park HK, Kim SU, Park CG, Lee SK, Kim M, Roh JK (2008) Anti-inflammatory mechanism of intravascular neural stem cell transplantation in haemorrhagic stroke. Brain 131:616–629CrossRefPubMed Lee ST, Chu K, Jung KH, Kim SJ, Kim DH, Kang KM, Hong NH, Kim JH, Ban JJ, Park HK, Kim SU, Park CG, Lee SK, Kim M, Roh JK (2008) Anti-inflammatory mechanism of intravascular neural stem cell transplantation in haemorrhagic stroke. Brain 131:616–629CrossRefPubMed
go back to reference Li N, Karin M (1999) Is NF-kB the sensor of oxidative stress? FASEB J 13:1137–1143PubMed Li N, Karin M (1999) Is NF-kB the sensor of oxidative stress? FASEB J 13:1137–1143PubMed
go back to reference Luedde T, Beraza N, Trautwein C (2006) Evaluation of the role of nuclear factor-kappaB signaling in liver injury using genetic animal models. J Gastroenterol Hepatol 21(Suppl 3):S43–S46CrossRefPubMed Luedde T, Beraza N, Trautwein C (2006) Evaluation of the role of nuclear factor-kappaB signaling in liver injury using genetic animal models. J Gastroenterol Hepatol 21(Suppl 3):S43–S46CrossRefPubMed
go back to reference Mackness B, Quarck R, Verreth W, Mackness M, Holvoet P (2006) Human paraoxonase-1 overexpression inhibits atherosclerosis in a mouse model of metabolic syndrome. Arterioscler Thromb Vasc Biol 26:1545–1550CrossRefPubMed Mackness B, Quarck R, Verreth W, Mackness M, Holvoet P (2006) Human paraoxonase-1 overexpression inhibits atherosclerosis in a mouse model of metabolic syndrome. Arterioscler Thromb Vasc Biol 26:1545–1550CrossRefPubMed
go back to reference Mahmood A, Lu D, Chopp M (2004) Intravenous administration of marrow stromal cells (MSCs) increases the expression of growth factors in rat brain after traumatic brain injury. J Neurotrauma 21:33–39CrossRefPubMed Mahmood A, Lu D, Chopp M (2004) Intravenous administration of marrow stromal cells (MSCs) increases the expression of growth factors in rat brain after traumatic brain injury. J Neurotrauma 21:33–39CrossRefPubMed
go back to reference Mandrekar P, Ambade A, Lim A, Szabo G, Catalano D (2011) An essential role for monocyte chemoattractant protein-1 in alcoholic liver injury: regulation of proinflammatory cytokines and hepatic steatosis in mice. Hepatology 54:2185–2197CrossRefPubMedCentralPubMed Mandrekar P, Ambade A, Lim A, Szabo G, Catalano D (2011) An essential role for monocyte chemoattractant protein-1 in alcoholic liver injury: regulation of proinflammatory cytokines and hepatic steatosis in mice. Hepatology 54:2185–2197CrossRefPubMedCentralPubMed
go back to reference Martin-Sanz P, Hortelano S, Callejas NA, Goren N, Casado M, Zeini N, Boscá L (2002) Nitric oxide in liver inflammation and regeneration. Metab Brain Dis 17(4):325–334CrossRefPubMed Martin-Sanz P, Hortelano S, Callejas NA, Goren N, Casado M, Zeini N, Boscá L (2002) Nitric oxide in liver inflammation and regeneration. Metab Brain Dis 17(4):325–334CrossRefPubMed
go back to reference Mei SH, Haitsma JJ, Dos Santos CC, Deng Y, Lai PF, Slutsky AS, Liles WC, Stewart DJ (2010) Mesenchymal stem cells reduce inflammation while enhancing bacterial clearance and improving survival in sepsis. Am J Respir Crit Care Med 182:1047–1057CrossRefPubMed Mei SH, Haitsma JJ, Dos Santos CC, Deng Y, Lai PF, Slutsky AS, Liles WC, Stewart DJ (2010) Mesenchymal stem cells reduce inflammation while enhancing bacterial clearance and improving survival in sepsis. Am J Respir Crit Care Med 182:1047–1057CrossRefPubMed
go back to reference Miller MD, Krangel MS (1992) Biology and biochemistry of the chemokines: a family of chemotactic and inflammatory cytokines. Crit Rev Immunol 12:17–46PubMed Miller MD, Krangel MS (1992) Biology and biochemistry of the chemokines: a family of chemotactic and inflammatory cytokines. Crit Rev Immunol 12:17–46PubMed
go back to reference Moshage H, Kok B, Huizenga JR (1995) Nitrite and nitrate determination in plasma: a critical evaluation. Clin Chem 41:892–896PubMed Moshage H, Kok B, Huizenga JR (1995) Nitrite and nitrate determination in plasma: a critical evaluation. Clin Chem 41:892–896PubMed
go back to reference Németh K, Leelahavanichkul A, Yuen PS, Mayer B, Parmelee A, Doi K, Robey PG, Leelahavanichkul K, Koller BH, Brown JM, Hu X, Jelinek I, Star RA, Mezey E (2009) Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med 15:42–49CrossRefPubMedCentralPubMed Németh K, Leelahavanichkul A, Yuen PS, Mayer B, Parmelee A, Doi K, Robey PG, Leelahavanichkul K, Koller BH, Brown JM, Hu X, Jelinek I, Star RA, Mezey E (2009) Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med 15:42–49CrossRefPubMedCentralPubMed
go back to reference Noble F, Rubira E, Boulanouar M, Palmier B, Plotkine M, Warnet JM, Marchand-Leroux C, Massicot F (2007) Acute systemic inflammation induces central mitochondrial damage and amnesic deficit in adult Swiss mice. Neurosci Lett 424:106–110CrossRefPubMed Noble F, Rubira E, Boulanouar M, Palmier B, Plotkine M, Warnet JM, Marchand-Leroux C, Massicot F (2007) Acute systemic inflammation induces central mitochondrial damage and amnesic deficit in adult Swiss mice. Neurosci Lett 424:106–110CrossRefPubMed
go back to reference Peterson KE, Errett JS, Wei T, Dimcheff DE, Ransohoff R, Kuziel WA, Evans L, Chesebro B (2004) MCP-1 and CCR2 contribute to non-lymphocyte-mediated brain disease induced by Fr98 polytropic retrovirus infection in mice: role for astrocytes in retroviral neuropathogenesis. J Virol 78:6449–6458CrossRefPubMedCentralPubMed Peterson KE, Errett JS, Wei T, Dimcheff DE, Ransohoff R, Kuziel WA, Evans L, Chesebro B (2004) MCP-1 and CCR2 contribute to non-lymphocyte-mediated brain disease induced by Fr98 polytropic retrovirus infection in mice: role for astrocytes in retroviral neuropathogenesis. J Virol 78:6449–6458CrossRefPubMedCentralPubMed
go back to reference Porter AG, Jänicke RU (1999) Emerging roles of caspase-3 in apoptosis. Cell Death Differ 6:99–104CrossRefPubMed Porter AG, Jänicke RU (1999) Emerging roles of caspase-3 in apoptosis. Cell Death Differ 6:99–104CrossRefPubMed
go back to reference Primo-Parmo SL, Sorenson RC, Teiber J, La Du BN (1996) The human serum paraoxonase/arylesterase gene (PON1) is one member of a multigene family. Genomics 33:498–507CrossRefPubMed Primo-Parmo SL, Sorenson RC, Teiber J, La Du BN (1996) The human serum paraoxonase/arylesterase gene (PON1) is one member of a multigene family. Genomics 33:498–507CrossRefPubMed
go back to reference Qin L, Wu X, Block ML, Liu Y, Breese GR, Hong JS, Knapp DJ, Crews FT (2007) Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55:453–462CrossRefPubMedCentralPubMed Qin L, Wu X, Block ML, Liu Y, Breese GR, Hong JS, Knapp DJ, Crews FT (2007) Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55:453–462CrossRefPubMedCentralPubMed
go back to reference Ramsay MAE (2002) Will stem cells transform medicine? Proc (Bayl Univ Med Cent) 15:135–137 Ramsay MAE (2002) Will stem cells transform medicine? Proc (Bayl Univ Med Cent) 15:135–137
go back to reference Ruiz-Larrea MB, Leal AM, Liza M, Lacort M, de Groot H (1994) Antioxidant effects of estradiol and 2-hydroxyestradiol on iron-induced lipid peroxidation of rat liver microsomes. Steroids 59:383–388CrossRefPubMed Ruiz-Larrea MB, Leal AM, Liza M, Lacort M, de Groot H (1994) Antioxidant effects of estradiol and 2-hydroxyestradiol on iron-induced lipid peroxidation of rat liver microsomes. Steroids 59:383–388CrossRefPubMed
go back to reference Sass G, Heinlein S, Agli A, Bang R, Schümann J, Tiegs G (2002) Cytokine expression in three mouse models of experimental hepatitis. Cytokine 19:115–120CrossRefPubMed Sass G, Heinlein S, Agli A, Bang R, Schümann J, Tiegs G (2002) Cytokine expression in three mouse models of experimental hepatitis. Cytokine 19:115–120CrossRefPubMed
go back to reference Schwabe RF, Brenner DA (2006) Mechanisms of liver injury. I. TNF-alpha-induced liver injury: role of IKK, JNK, and ROS pathways. Am J Physiol Gastrointest Liver Physiol 290:G583–G589CrossRefPubMed Schwabe RF, Brenner DA (2006) Mechanisms of liver injury. I. TNF-alpha-induced liver injury: role of IKK, JNK, and ROS pathways. Am J Physiol Gastrointest Liver Physiol 290:G583–G589CrossRefPubMed
go back to reference Semple BD, Bye N, Rancan M, Ziebell JM, Morganti-Kossmann MC (2010) Role of CCL2 (MCP-1) in traumatic brain injury (TBI): evidence from severe TBI patients and CCL2−/− mice. J Cereb Blood Flow Metab 30:769–782CrossRefPubMedCentralPubMed Semple BD, Bye N, Rancan M, Ziebell JM, Morganti-Kossmann MC (2010) Role of CCL2 (MCP-1) in traumatic brain injury (TBI): evidence from severe TBI patients and CCL2−/− mice. J Cereb Blood Flow Metab 30:769–782CrossRefPubMedCentralPubMed
go back to reference Suetsugu H, Iimuro Y, Uehara T, Nishio T, Harada N, Yoshida M, Hatano E, Son G, Fujimoto J, Yamaoka Y (2005) Nuclear factor κB inactivation in the rat liver ameliorates short term total warm ischaemia/reperfusion injury. Gut 54:835–842CrossRefPubMedCentralPubMed Suetsugu H, Iimuro Y, Uehara T, Nishio T, Harada N, Yoshida M, Hatano E, Son G, Fujimoto J, Yamaoka Y (2005) Nuclear factor κB inactivation in the rat liver ameliorates short term total warm ischaemia/reperfusion injury. Gut 54:835–842CrossRefPubMedCentralPubMed
go back to reference Sun CK, Yen CH, Lin YC, Tsai TH, Chang LT, Kao YH, Chua S, Fu M, Ko SF, Leu S, Yip HK (2011) Autologous transplantation of adipose-derived mesenchymal stem cells markedly reduced acute ischemia-reperfusion lung injury in a rodent model. J Transl Med 9:118CrossRefPubMedCentralPubMed Sun CK, Yen CH, Lin YC, Tsai TH, Chang LT, Kao YH, Chua S, Fu M, Ko SF, Leu S, Yip HK (2011) Autologous transplantation of adipose-derived mesenchymal stem cells markedly reduced acute ischemia-reperfusion lung injury in a rodent model. J Transl Med 9:118CrossRefPubMedCentralPubMed
go back to reference Takeuchi H, Natsume A, Wakabayashi T, Aoshima C, Shimato S, Ito M, Ishii J, Maeda Y, Hara M, Kim SU, Yoshida J (2007) Intravenously transplanted human neural stem cells migrate to the injured spinal cord in adult mice in an SDF-1- and HGF-dependent manner. Neurosci Lett 426:69–74CrossRefPubMed Takeuchi H, Natsume A, Wakabayashi T, Aoshima C, Shimato S, Ito M, Ishii J, Maeda Y, Hara M, Kim SU, Yoshida J (2007) Intravenously transplanted human neural stem cells migrate to the injured spinal cord in adult mice in an SDF-1- and HGF-dependent manner. Neurosci Lett 426:69–74CrossRefPubMed
go back to reference Thompson WL, Karpus WJ, Van Eldik LJ (2008) MCP-1-deficient mice show reduced neuroinflammatory responses and increased peripheral inflammatory responses to peripheral endotoxin insult. J Neuroinflammation 5:35CrossRefPubMedCentralPubMed Thompson WL, Karpus WJ, Van Eldik LJ (2008) MCP-1-deficient mice show reduced neuroinflammatory responses and increased peripheral inflammatory responses to peripheral endotoxin insult. J Neuroinflammation 5:35CrossRefPubMedCentralPubMed
go back to reference Tomiyama K, Murase N, Stolz DB, Toyokawa H, O’Donnell DR, Smith DM, Dudas JR, Rubin JP, Marra KG (2008) Characterization of transplanted GFP+ bone marrow cells into adipose tissue. Stem Cells 26:330–338CrossRefPubMedCentralPubMed Tomiyama K, Murase N, Stolz DB, Toyokawa H, O’Donnell DR, Smith DM, Dudas JR, Rubin JP, Marra KG (2008) Characterization of transplanted GFP+ bone marrow cells into adipose tissue. Stem Cells 26:330–338CrossRefPubMedCentralPubMed
go back to reference Tuaillon N, Shen DF, Berger RB, Lu B, Rollins BJ, Chan CC (2002) MCP-1 expression in endotoxin-induced uveitis. Invest Ophthalmol Vis Sci 43:1493–1498PubMed Tuaillon N, Shen DF, Berger RB, Lu B, Rollins BJ, Chan CC (2002) MCP-1 expression in endotoxin-induced uveitis. Invest Ophthalmol Vis Sci 43:1493–1498PubMed
go back to reference Turrin NP, Gayle D, Ilyin SE, Flynn MC, Langhans W, Schwartz GJ, Plata-Salamán CR (2001) Pro-inflammatory and anti-inflammatory cytokine mRNA induction in the periphery and brain following intraperitoneal administration of bacterial lipopolysaccharide. Brain Res Bull 54:443–453CrossRefPubMed Turrin NP, Gayle D, Ilyin SE, Flynn MC, Langhans W, Schwartz GJ, Plata-Salamán CR (2001) Pro-inflammatory and anti-inflammatory cytokine mRNA induction in the periphery and brain following intraperitoneal administration of bacterial lipopolysaccharide. Brain Res Bull 54:443–453CrossRefPubMed
go back to reference Tweedie D, Sambamurti K, Greig NH (2007) Review TNF-alpha inhibition as a treatment strategy for neurodegenerative disorders: new drug candidates and targets. Curr Alzheimer Res 4:378–385CrossRefPubMed Tweedie D, Sambamurti K, Greig NH (2007) Review TNF-alpha inhibition as a treatment strategy for neurodegenerative disorders: new drug candidates and targets. Curr Alzheimer Res 4:378–385CrossRefPubMed
go back to reference Uccelli A, Milanese M, Principato MC, Morando S, Bonifacino T, Vergani L, Giunti D, Voci A, Carminati E, Giribaldi F, Caponnetto C, Bonanno G (2012) Intravenous mesenchymal stem cells improve survival and motor function in experimental amyotrophic lateral sclerosis. Mol Med 18:794–804CrossRefPubMedCentralPubMed Uccelli A, Milanese M, Principato MC, Morando S, Bonifacino T, Vergani L, Giunti D, Voci A, Carminati E, Giribaldi F, Caponnetto C, Bonanno G (2012) Intravenous mesenchymal stem cells improve survival and motor function in experimental amyotrophic lateral sclerosis. Mol Med 18:794–804CrossRefPubMedCentralPubMed
go back to reference Valatas V, Kolios G, Manousou P, Notas G, Xidakis C, Diamantis I, Kouroumalis E (2004) Octreotide regulates CC but not CXC LPS-induced chemokine secretion in rat Kupffer cells. Br J Pharmacol 141:477–487CrossRefPubMedCentralPubMed Valatas V, Kolios G, Manousou P, Notas G, Xidakis C, Diamantis I, Kouroumalis E (2004) Octreotide regulates CC but not CXC LPS-induced chemokine secretion in rat Kupffer cells. Br J Pharmacol 141:477–487CrossRefPubMedCentralPubMed
go back to reference Wang X, Quinn PJ (2010) Endotoxins: lipopolysaccharides of gram-negative bacteria. Subcell Biochem 53:3–25CrossRefPubMed Wang X, Quinn PJ (2010) Endotoxins: lipopolysaccharides of gram-negative bacteria. Subcell Biochem 53:3–25CrossRefPubMed
go back to reference Wang L, Li Y, Chen X, Chen J, Gautam SC, Xu Y, Chopp M (2002) MCP-1, MIP-1, IL-8 and ischemic cerebral tissue enhance human bone marrow stromal cell migration in interface culture. Hematology 7:113–7 Wang L, Li Y, Chen X, Chen J, Gautam SC, Xu Y, Chopp M (2002) MCP-1, MIP-1, IL-8 and ischemic cerebral tissue enhance human bone marrow stromal cell migration in interface culture. Hematology 7:113–7
go back to reference Wang H, Wu YB, Du XH (2005) Effect of dexamethasone on nitric oxide synthase and caspase-3 gene expressions in endotoxemia in neonate rat brain. Biomed Environ Sci 18:181–186PubMed Wang H, Wu YB, Du XH (2005) Effect of dexamethasone on nitric oxide synthase and caspase-3 gene expressions in endotoxemia in neonate rat brain. Biomed Environ Sci 18:181–186PubMed
go back to reference Wang Q, Matsumoto Y, Shindo T, Miyake K, Shindo A, Kawanishi M, Kawai N, Tamiya T, Nagao S (2006) Neural stem cells transplantation in cortex in a mouse model of Alzheimer’s disease. J Med Investig 53:61–69CrossRef Wang Q, Matsumoto Y, Shindo T, Miyake K, Shindo A, Kawanishi M, Kawai N, Tamiya T, Nagao S (2006) Neural stem cells transplantation in cortex in a mouse model of Alzheimer’s disease. J Med Investig 53:61–69CrossRef
go back to reference Wang F, Yasuhara T, Shingo T, Kameda M, Tajiri N, Yuan WJ, Kondo A, Kadota T, Baba T, Tayra JT, Kikuchi Y, Miyoshi Y, Date I (2010) Intravenous administration of mesenchymal stem cells exerts therapeutic effects on parkinsonian model of rats: focusing on neuroprotective effects of stromal cell-derived factor-1alpha. BMC Neurosci 11:52CrossRefPubMedCentralPubMed Wang F, Yasuhara T, Shingo T, Kameda M, Tajiri N, Yuan WJ, Kondo A, Kadota T, Baba T, Tayra JT, Kikuchi Y, Miyoshi Y, Date I (2010) Intravenous administration of mesenchymal stem cells exerts therapeutic effects on parkinsonian model of rats: focusing on neuroprotective effects of stromal cell-derived factor-1alpha. BMC Neurosci 11:52CrossRefPubMedCentralPubMed
go back to reference Wang B, Wu SM, Wang T, Liu K, Zhang G, Zhang XQ, Yu JH, Liu CZ, Fang CC (2012) Pre-treatment with bone marrow-derived mesenchymal stem cells inhibits systemic intravascular coagulation and attenuates organ dysfunction in lipopolysaccharide-induced disseminated intravascular coagulation rat model. Chin Med J (Engl) 125:1753–1759 Wang B, Wu SM, Wang T, Liu K, Zhang G, Zhang XQ, Yu JH, Liu CZ, Fang CC (2012) Pre-treatment with bone marrow-derived mesenchymal stem cells inhibits systemic intravascular coagulation and attenuates organ dysfunction in lipopolysaccharide-induced disseminated intravascular coagulation rat model. Chin Med J (Engl) 125:1753–1759
go back to reference Watson AD, Berliner JA, Hama SY, La Du BN, Faull KF, Fogelman AM, Navab M (1995) Protective effect of high density lipoprotein associated paraoxonase. Inhibition of the biological activity of minimally oxidized low density lipoprotein. J Clin Invest 96:2882–2891CrossRefPubMedCentralPubMed Watson AD, Berliner JA, Hama SY, La Du BN, Faull KF, Fogelman AM, Navab M (1995) Protective effect of high density lipoprotein associated paraoxonase. Inhibition of the biological activity of minimally oxidized low density lipoprotein. J Clin Invest 96:2882–2891CrossRefPubMedCentralPubMed
go back to reference Weil BR, Herrmann JL, Abarbanell AM, Manukyan MC, Poynter JA, Meldrum DR (2011) Intravenous infusion of mesenchymal stem cells is associated with improved myocardial function during endotoxemia. Shock 36:235–241CrossRefPubMed Weil BR, Herrmann JL, Abarbanell AM, Manukyan MC, Poynter JA, Meldrum DR (2011) Intravenous infusion of mesenchymal stem cells is associated with improved myocardial function during endotoxemia. Shock 36:235–241CrossRefPubMed
go back to reference Wen-Hui J, Ai-Qun MA, Yan-Min Z, Ke H, Yu L, Zeng-Tie Z, Ting-Zhong W, Xin H, Xiao-Pu Z (2005) Migration of intravenously grafted mesenchymal stem cells to injured heart in rats. Acta Physiol Sin 57:566–572 Wen-Hui J, Ai-Qun MA, Yan-Min Z, Ke H, Yu L, Zeng-Tie Z, Ting-Zhong W, Xin H, Xiao-Pu Z (2005) Migration of intravenously grafted mesenchymal stem cells to injured heart in rats. Acta Physiol Sin 57:566–572
go back to reference Yagi H, Soto-Gutierrez A, Navarro-Alvarez N, Nahmias Y, Goldwasser Y, Kitagawa Y, Tilles AW, Tompkins RG, Parekkadan B, Yarmush ML (2010) Reactive bone marrow stromal cells attenuate systemic inflammation via sTNFR1. Mol Ther 18:1857–1864CrossRefPubMedCentralPubMed Yagi H, Soto-Gutierrez A, Navarro-Alvarez N, Nahmias Y, Goldwasser Y, Kitagawa Y, Tilles AW, Tompkins RG, Parekkadan B, Yarmush ML (2010) Reactive bone marrow stromal cells attenuate systemic inflammation via sTNFR1. Mol Ther 18:1857–1864CrossRefPubMedCentralPubMed
go back to reference Zhang H, Fang J, Su H, Yang M, Lai W, Mai Y, Wu Y (2012) Bone marrow mesenchymal stem cells attenuate lung inflammation of hyperoxic newborn rats. Pediatr Transplant 16:589–598CrossRefPubMed Zhang H, Fang J, Su H, Yang M, Lai W, Mai Y, Wu Y (2012) Bone marrow mesenchymal stem cells attenuate lung inflammation of hyperoxic newborn rats. Pediatr Transplant 16:589–598CrossRefPubMed
Metadata
Title
Effect of adipose tissue-derived mesenchymal stem cell treatment on oxidative stress and inflammatory response following Escherichia coli lipopolysaccharide
Authors
Omar M. E. Abdel-Salam
Eman R. Youness
Enayat A. Omara
Amany A. Sleem
Publication date
01-03-2015
Publisher
Springer London
Published in
Comparative Clinical Pathology / Issue 2/2015
Print ISSN: 1618-5641
Electronic ISSN: 1618-565X
DOI
https://doi.org/10.1007/s00580-014-1906-x

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