Cardiac up-regulation of apolipoprotein D in a rat model of hypo- and hyperthyroidism

authors:

avatar Marziyeh Salami , avatar Roghayeh Pakdel , avatar Hamidreza Sameni ORCID , avatar Abbas Pakdel , * , avatar Abbas Ali Vafaei


how to cite: Salami M, Pakdel R , Sameni H, Pakdel A, Vafaei A A. Cardiac up-regulation of apolipoprotein D in a rat model of hypo- and hyperthyroidism. koomesh. 2021;23(3):e149961. 

Abstract

Introduction: Cardiac tissue is one of the organs affected by thyroid hormones imbalances. Apolipoprotein D is a multifunctional glycoprotein that is expressed in various tissues including heart tissue. The aim of this study was to evaluate the effect of both hypothyroidism and hyperthyroidism on the level of apolipoprotein D protein in the heart tissue. Materials and Methods: In order to induce hypothyroidism and hyperthyroidism in white mice, propylthiouracil (PTU, 100 ppm) and levothyroxine (L-T4, 8 ppm) dissolved in water  and were used for 6 weeks, respectively. ELISA method was used to measure the total T3 hormone in rat serum. After confirming the model, the mice were anesthetized and the heart tissue was removed and the ventricle and apex of the heart were used for histological examination. Immunohistochemistry was used to evaluate the expression level of apolipoprotein D. Results: We showed for the first time that the expression of apolipoprotein D in the hearts of hypothyroid (P

References

  • 1.

    [1] Vargas-Uricoechea H, Bonelo-Perdomo A, Sierra-Torres CH. Effects of thyroid hormones on the heart. Clin Investig Arterioscler 2014; 26: 296-309.

  • 2.

    https://doi.org/10.1016/j.arteri.2014.07.003.

  • 3.

    PMid:25438971.

  • 4.

    [2] De K, Ghosh G, Datta M, Konar A, Bandyopadhyay J, Bandyopadhyay D, Bhattacharya S, Bandyopadhyay A. Analysis of differentially expressed genes in hyperthyroid-induced hypertrophied heart by cDNA microarray. J Endocrinol 2004; 182: 303-314.

  • 5.

    https://doi.org/10.1677/joe.0.1820303.

  • 6.

    PMid:15283691.

  • 7.

    [3] Klein I, Danzi S. Thyroid disease and the heart. Circulation 2007; 116: 1725-1735.

  • 8.

    https://doi.org/10.1161/CIRCULATIONAHA.106.678326.

  • 9.

    PMid:17923583.

  • 10.

    [4] Stanciu AE, ZamfirChiruAnton A, Stanciu MM, Gheorghe DC. Impact of thyroid disease on heart failure. the role of the clinical cardiac electrophysiologist in the management of congestive heart failure 2017; 141.

  • 11.

    https://doi.org/10.5772/66283.

  • 12.

    [5] Elnakish MT, Ahmed AA, Mohler PJ, Janssen PM. Role of oxidative stress in thyroid hormone-induced cardiomyocyte hypertrophy and associated cardiac dysfunction: an undisclosed story. Oxid Med Cell Longev 2015; 2015: 854265.

  • 13.

    https://doi.org/10.1155/2015/854265.

  • 14.

    PMid:26146529 PMCid:PMC4471379.

  • 15.

    [6] Sabih DE, Inayatullah M. Managing thyroid dysfunction in selected special situations. Thyroid Res 2013; 6: 2.

  • 16.

    https://doi.org/10.1186/1756-6614-6-2.

  • 17.

    PMid:23379325 PMCid:PMC3626556.

  • 18.

    [7] Triggiani V, Iacoviello M, Monzani F, Puzzovivo A, Guida P, Forleo C, et al. Incidence and prevalence of hypothyroidism in patients affected by chronic heart failure: role of amiodarone. Endocr Metab Immune Disord Drug Targets 2012; 12: 86-94.

  • 19.

    https://doi.org/10.2174/187153012799278947.

  • 20.

    PMid:22214334.

  • 21.

    [8] Mishra P, Samanta L. Oxidative stress and heart failure in altered thyroid states. ScientificWorldJournal 2012; 2012: 741861.

  • 22.

    https://doi.org/10.1100/2012/741861.

  • 23.

    PMid:22649319 PMCid:PMC3354657.

  • 24.

    [9] Mancini A, Di Segni C, Raimondo S, Olivieri G, Silvestrini A, Meucci E, Curr D. Thyroid hormones, oxidative stress, and inflammation. Mediators Inflamm 2016; 2016: 6757154.

  • 25.

    https://doi.org/10.1155/2016/6757154.

  • 26.

    PMid:27051079 PMCid:PMC4802023.

  • 27.

    [10] Fernandes R, Dreher G, Schenkel P, Fernandes T, Ribeiro M, Araujo A, BellKlein A. Redox status and prosurvival/proapoptotic protein expression in the early cardiac hypertrophy induced by experimental hyperthyroidism. Cell Biochem Funct 2011; 29: 617-623.

  • 28.

    https://doi.org/10.1002/cbf.1796.

  • 29.

    PMid:21989893.

  • 30.

    [11] Bergh JJ, Lin H-Y, Lansing L, Mohamed SN, Davis FB, Mousa S, Davis PJ. Integrin V3 contains a cell surface receptor site for thyroid hormone that is linked to activation of mitogen-activated protein kinase and induction of angiogenesis. Endocrinology 2005; 146: 2864-2871.

  • 31.

    https://doi.org/10.1210/en.2005-0102.

  • 32.

    PMid:15802494.

  • 33.

    [12] Crespo-Sanjun J, Zamora-Gonzalez N, Calvo-Nieves MD, Andres-Ledesma C. Apolipoprotein D. Advances in Lipoprotein Research 2017: 25.

  • 34.

    https://doi.org/10.5772/66626.

  • 35.

    [13] Dassati S, Waldner A, Schweigreiter R. Apolipoprotein D takes center stage in the stress response of the aging and degenerative brain. Neurobiol Aging 2014; 35: 1632-1642.

  • 36.

    https://doi.org/10.1016/j.neurobiolaging.2014.01.148.

  • 37.

    PMid:24612673 PMCid:PMC3988949.

  • 38.

    [14] Martnez-Pinilla E, Navarro A, Ordez C, del Valle E, Tolivia J. Apolipoprotein D subcellular distribution pattern in neuronal cells during oxidative stress. Acta Histochemica 2015; 117: 536-544.

  • 39.

    https://doi.org/10.1016/j.acthis.2015.04.003.

  • 40.

    PMid:25953740.

  • 41.

    [15] Zhou Y, Wang L, Li R, Liu M, Li X, Su H, et al. Secreted glycoprotein BmApoD1 plays a critical role in anti-oxidation and anti-apoptosis in Bombyx mori. Biochem Biophys Res Commun 2018; 495: 839-845.

  • 42.

    https://doi.org/10.1016/j.bbrc.2017.11.044.

  • 43.

    PMid:29128356.

  • 44.

    [16] Bhatia S, Knoch B, Wong J, Kim WS, Else PL, Oakley AJ, Garner B. Selective reduction of hydroperoxyeicosatetraenoic acids to their hydroxy derivatives by apolipoprotein D: implications for lipid antioxidant activity and Alzheimer's disease. Biochem J 2012; 442: 713-721.

  • 45.

    https://doi.org/10.1042/BJ20111166.

  • 46.

    PMid:22150111.

  • 47.

    [17] Leung WC, Lawrie A, Demaries S, Massaeli H, Burry A, Yablonsky S, et al. Apolipoprotein D and platelet-derived growth factor-BB synergism mediates vascular smooth muscle cell migration. Circ Res 2004; 95: 179-186.

  • 48.

    https://doi.org/10.1161/01.RES.0000135482.74178.14.

  • 49.

    PMid:15192024.

  • 50.

    [18] Tsukamoto K, Mani D, Shi J, Zhang S, Haagensen DE, Otsuka F, et al. Identification of apolipoprotein D as a cardioprotective gene using a mouse model of lethal atherosclerotic coronary artery disease. Proc Natl Acad Sci U S A 2013; 110: 17023-17028.

  • 51.

    https://doi.org/10.1073/pnas.1315986110.

  • 52.

    PMid:24082102 PMCid:PMC3801016.

  • 53.

    [19] Salami M, Bandegi AR, Sameni HR, Vafaei AA, Pakdel A. Hippocampal up-regulation of apolipoprotein D in a rat model of maternal hypo-and hyperthyroidism: implication of oxidative stress. Neurochem Res 2019; 44: 2190-2201.

  • 54.

    https://doi.org/10.1007/s11064-019-02859-5.

  • 55.

    PMid:31414343.

  • 56.

    [20] Martnez E, Navarro A, Ordnez C, del Valle E, Tolivia J. Oxidative stress induces apolipoprotein D overexpression in hippocampus during aging and Alzheimer's disease. J Alzheimers Dis 2013; 36: 129-144.

  • 57.

    https://doi.org/10.3233/JAD-130215.

  • 58.

    PMid:23568103.

  • 59.

    [21] Pascua Maestro R, Gonzlez E, Lillo C, Ganfornina MD, Falcon-Perez JM, Sanchez D. Extracellular vesicles secreted by astroglial cells transport Apolipoprotein D to neurons and mediate neuronal survival upon oxidative stress. Front Cell Neurosci 2018; 12: 526.

  • 60.

    https://doi.org/10.3389/fncel.2018.00526.

  • 61.

    PMid:30687015 PMCid:PMC6335244.

  • 62.

    [22] Messarah M, Saoudi M, Boumendjel A, Boulakoud MS, El Feki A. Oxidative stress induced by thyroid dysfunction in rat erythrocytes and heart. Environ Toxicol Pharmacol 2011; 31: 33-41.

  • 63.

    https://doi.org/10.1016/j.etap.2010.09.003.

  • 64.

    PMid:21787667.

  • 65.

    [23] Oakley AJ, Bhatia S, Ecroyd H, Garner B. Molecular dynamics analysis of apolipoprotein-D-lipid hydroperoxide interactions: mechanism for selective oxidation of Met-93. PloS One 2012; 7: e34057.

  • 66.

    https://doi.org/10.1371/journal.pone.0034057.

  • 67.

    PMid:22479522 PMCid:PMC3316614.

  • 68.

    [24] Yao X, Sa R, Ye C, Zhang D, Zhang S, Xia H, et al. Effects of thyroid hormone status on metabolic pathways of arachidonic acid in mice and humans: a targeted metabolomic approach. Prostaglandins Other Lipid Mediat 2015; 118: 11-18.

  • 69.

    https://doi.org/10.1016/j.prostaglandins.2015.03.005.

  • 70.

    PMid:25841349.

  • 71.

    [25] Do Carmo S, Levros Jr L-C, Rassart E. Modulation of apolipoprotein D expression and translocation under specific stress conditions. Biochim Biophys Acta 2007; 1773: 954-969.

  • 72.

    https://doi.org/10.1016/j.bbamcr.2007.03.007.

  • 73.

    PMid:17477983.

  • 74.

    [26] Do Carmo S, Sguin D, Milne R, Rassart E. Modulation of apolipoprotein D and apolipoprotein E mRNA expression by growth arrest and identification of key elements in the promoter. J Biol Chem 2002; 277: 5514-5523.

  • 75.

    https://doi.org/10.1074/jbc.M105057200.

  • 76.

    PMid:11711530.

  • 77.

    [1] Vargas-Uricoechea H, Bonelo-Perdomo A, Sierra-Torres CH. Effects of thyroid hormones on the heart. Clin Investig Arterioscler 2014; 26: 296-309.

  • 78.

    https://doi.org/10.1016/j.arteri.2014.07.003.

  • 79.

    PMid:25438971.

  • 80.

    [2] De K, Ghosh G, Datta M, Konar A, Bandyopadhyay J, Bandyopadhyay D, Bhattacharya S, Bandyopadhyay A. Analysis of differentially expressed genes in hyperthyroid-induced hypertrophied heart by cDNA microarray. J Endocrinol 2004; 182: 303-314.

  • 81.

    https://doi.org/10.1677/joe.0.1820303.

  • 82.

    PMid:15283691.

  • 83.

    [3] Klein I, Danzi S. Thyroid disease and the heart. Circulation 2007; 116: 1725-1735.

  • 84.

    https://doi.org/10.1161/CIRCULATIONAHA.106.678326.

  • 85.

    PMid:17923583.

  • 86.

    [4] Stanciu AE, ZamfirChiruAnton A, Stanciu MM, Gheorghe DC. Impact of thyroid disease on heart failure. the role of the clinical cardiac electrophysiologist in the management of congestive heart failure 2017; 141.

  • 87.

    https://doi.org/10.5772/66283.

  • 88.

    [5] Elnakish MT, Ahmed AA, Mohler PJ, Janssen PM. Role of oxidative stress in thyroid hormone-induced cardiomyocyte hypertrophy and associated cardiac dysfunction: an undisclosed story. Oxid Med Cell Longev 2015; 2015: 854265.

  • 89.

    https://doi.org/10.1155/2015/854265.

  • 90.

    PMid:26146529 PMCid:PMC4471379.

  • 91.

    [6] Sabih DE, Inayatullah M. Managing thyroid dysfunction in selected special situations. Thyroid Res 2013; 6: 2.

  • 92.

    https://doi.org/10.1186/1756-6614-6-2.

  • 93.

    PMid:23379325 PMCid:PMC3626556.

  • 94.

    [7] Triggiani V, Iacoviello M, Monzani F, Puzzovivo A, Guida P, Forleo C, et al. Incidence and prevalence of hypothyroidism in patients affected by chronic heart failure: role of amiodarone. Endocr Metab Immune Disord Drug Targets 2012; 12: 86-94.

  • 95.

    https://doi.org/10.2174/187153012799278947.

  • 96.

    PMid:22214334.

  • 97.

    [8] Mishra P, Samanta L. Oxidative stress and heart failure in altered thyroid states. ScientificWorldJournal 2012; 2012: 741861.

  • 98.

    https://doi.org/10.1100/2012/741861.

  • 99.

    PMid:22649319 PMCid:PMC3354657.

  • 100.

    [9] Mancini A, Di Segni C, Raimondo S, Olivieri G, Silvestrini A, Meucci E, Curr D. Thyroid hormones, oxidative stress, and inflammation. Mediators Inflamm 2016; 2016: 6757154.

  • 101.

    https://doi.org/10.1155/2016/6757154.

  • 102.

    PMid:27051079 PMCid:PMC4802023.

  • 103.

    [10] Fernandes R, Dreher G, Schenkel P, Fernandes T, Ribeiro M, Araujo A, BellKlein A. Redox status and prosurvival/proapoptotic protein expression in the early cardiac hypertrophy induced by experimental hyperthyroidism. Cell Biochem Funct 2011; 29: 617-623.

  • 104.

    https://doi.org/10.1002/cbf.1796.

  • 105.

    PMid:21989893.

  • 106.

    [11] Bergh JJ, Lin H-Y, Lansing L, Mohamed SN, Davis FB, Mousa S, Davis PJ. Integrin V3 contains a cell surface receptor site for thyroid hormone that is linked to activation of mitogen-activated protein kinase and induction of angiogenesis. Endocrinology 2005; 146: 2864-2871.

  • 107.

    https://doi.org/10.1210/en.2005-0102.

  • 108.

    PMid:15802494.

  • 109.

    [12] Crespo-Sanjun J, Zamora-Gonzalez N, Calvo-Nieves MD, Andres-Ledesma C. Apolipoprotein D. Advances in Lipoprotein Research 2017: 25.

  • 110.

    https://doi.org/10.5772/66626.

  • 111.

    [13] Dassati S, Waldner A, Schweigreiter R. Apolipoprotein D takes center stage in the stress response of the aging and degenerative brain. Neurobiol Aging 2014; 35: 1632-1642.

  • 112.

    https://doi.org/10.1016/j.neurobiolaging.2014.01.148.

  • 113.

    PMid:24612673 PMCid:PMC3988949.

  • 114.

    [14] Martnez-Pinilla E, Navarro A, Ordez C, del Valle E, Tolivia J. Apolipoprotein D subcellular distribution pattern in neuronal cells during oxidative stress. Acta Histochemica 2015; 117: 536-544.

  • 115.

    https://doi.org/10.1016/j.acthis.2015.04.003.

  • 116.

    PMid:25953740.

  • 117.

    [15] Zhou Y, Wang L, Li R, Liu M, Li X, Su H, et al. Secreted glycoprotein BmApoD1 plays a critical role in anti-oxidation and anti-apoptosis in Bombyx mori. Biochem Biophys Res Commun 2018; 495: 839-845.

  • 118.

    https://doi.org/10.1016/j.bbrc.2017.11.044.

  • 119.

    PMid:29128356.

  • 120.

    [16] Bhatia S, Knoch B, Wong J, Kim WS, Else PL, Oakley AJ, Garner B. Selective reduction of hydroperoxyeicosatetraenoic acids to their hydroxy derivatives by apolipoprotein D: implications for lipid antioxidant activity and Alzheimer's disease. Biochem J 2012; 442: 713-721.

  • 121.

    https://doi.org/10.1042/BJ20111166.

  • 122.

    PMid:22150111.

  • 123.

    [17] Leung WC, Lawrie A, Demaries S, Massaeli H, Burry A, Yablonsky S, et al. Apolipoprotein D and platelet-derived growth factor-BB synergism mediates vascular smooth muscle cell migration. Circ Res 2004; 95: 179-186.

  • 124.

    https://doi.org/10.1161/01.RES.0000135482.74178.14.

  • 125.

    PMid:15192024.

  • 126.

    [18] Tsukamoto K, Mani D, Shi J, Zhang S, Haagensen DE, Otsuka F, et al. Identification of apolipoprotein D as a cardioprotective gene using a mouse model of lethal atherosclerotic coronary artery disease. Proc Natl Acad Sci U S A 2013; 110: 17023-17028.

  • 127.

    https://doi.org/10.1073/pnas.1315986110.

  • 128.

    PMid:24082102 PMCid:PMC3801016.

  • 129.

    [19] Salami M, Bandegi AR, Sameni HR, Vafaei AA, Pakdel A. Hippocampal up-regulation of apolipoprotein D in a rat model of maternal hypo-and hyperthyroidism: implication of oxidative stress. Neurochem Res 2019; 44: 2190-2201.

  • 130.

    https://doi.org/10.1007/s11064-019-02859-5.

  • 131.

    PMid:31414343.

  • 132.

    [20] Martnez E, Navarro A, Ordnez C, del Valle E, Tolivia J. Oxidative stress induces apolipoprotein D overexpression in hippocampus during aging and Alzheimer's disease. J Alzheimers Dis 2013; 36: 129-144.

  • 133.

    https://doi.org/10.3233/JAD-130215.

  • 134.

    PMid:23568103.

  • 135.

    [21] Pascua Maestro R, Gonzlez E, Lillo C, Ganfornina MD, Falcon-Perez JM, Sanchez D. Extracellular vesicles secreted by astroglial cells transport Apolipoprotein D to neurons and mediate neuronal survival upon oxidative stress. Front Cell Neurosci 2018; 12: 526.

  • 136.

    https://doi.org/10.3389/fncel.2018.00526.

  • 137.

    PMid:30687015 PMCid:PMC6335244.

  • 138.

    [22] Messarah M, Saoudi M, Boumendjel A, Boulakoud MS, El Feki A. Oxidative stress induced by thyroid dysfunction in rat erythrocytes and heart. Environ Toxicol Pharmacol 2011; 31: 33-41.

  • 139.

    https://doi.org/10.1016/j.etap.2010.09.003.

  • 140.

    PMid:21787667.

  • 141.

    [23] Oakley AJ, Bhatia S, Ecroyd H, Garner B. Molecular dynamics analysis of apolipoprotein-D-lipid hydroperoxide interactions: mechanism for selective oxidation of Met-93. PloS One 2012; 7: e34057.

  • 142.

    https://doi.org/10.1371/journal.pone.0034057.

  • 143.

    PMid:22479522 PMCid:PMC3316614.

  • 144.

    [24] Yao X, Sa R, Ye C, Zhang D, Zhang S, Xia H, et al. Effects of thyroid hormone status on metabolic pathways of arachidonic acid in mice and humans: a targeted metabolomic approach. Prostaglandins Other Lipid Mediat 2015; 118: 11-18.

  • 145.

    https://doi.org/10.1016/j.prostaglandins.2015.03.005.

  • 146.

    PMid:25841349.

  • 147.

    [25] Do Carmo S, Levros Jr L-C, Rassart E. Modulation of apolipoprotein D expression and translocation under specific stress conditions. Biochim Biophys Acta 2007; 1773: 954-969.

  • 148.

    https://doi.org/10.1016/j.bbamcr.2007.03.007.

  • 149.

    PMid:17477983.

  • 150.

    [26] Do Carmo S, Sguin D, Milne R, Rassart E. Modulation of apolipoprotein D and apolipoprotein E mRNA expression by growth arrest and identification of key elements in the promoter. J Biol Chem 2002; 277: 5514-5523.

  • 151.

    https://doi.org/10.1074/jbc.M105057200.

  • 152.

    PMid:11711530.