Placenta-Derived Adherent Stromal Cells Improve Diabetes Mellitus-Associated Left Ventricular Diastolic Performance

Stem Cells Translational Medicine

Volumn 6, Issue 12, 2017, Pages 2135-2145

  Van Linthout, Sophie ^a,b   Hamdani, Nazha ^c   Miteva, Kapka ^a   Koschel, Annika ^a   Müller, Irene ^a,b   Pinzur, Lena ^d   Aberman, Zami ^d   Pappritz, Kathleen ^a,b   Linke, Wolfgang Albrecht ^c   Tschöpe, Carsten ^a,b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^c RUHR UNIVERSITY BOCHUM   (Germany)

^d PLURISTEM THERAPEUTICS INC   (Israel)

Author keywords

Diabetes mellitus; Diastole; Passive force; Placenta expanded cell; Titin

Indexed keywords

ANTIFIBROTIC AGENT; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CASPASE; CONNECTIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP DEPENDENT PROTEIN KINASE; GAMMA INTERFERON; GLUCOSE; NITRIC OXIDE; TRANSFORMING GROWTH FACTOR BETA1; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ADHESION ASSAY; CELL THERAPY; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC CARDIOMYOPATHY; FIBROBLAST; FLOW CYTOMETRY; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN CELL; IMMUNOHISTOLOGY; INFLAMMATION; LEFT VENTRICULAR DIASTOLIC DYSFUNCTION; MALE; MESENCHYMAL STROMA CELL; MOUSE; MRNA EXPRESSION ASSAY; NONHUMAN; PHOSPHORYLATION; PLACENTA DERIVED ADHERENT STROMAL CELL; REGULATORY T LYMPHOCYTE; SPLEEN CELL; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE CELL; CELL CULTURE; CYTOLOGY; DIASTOLE; EXPERIMENTAL DIABETES MELLITUS; FEMALE; HEART VENTRICLE FUNCTION; MESENCHYMAL STEM CELL TRANSPLANTATION; METABOLISM; PLACENTA; PREGNANCY; PROCEDURES; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC CARDIOMYOPATHIES; DIASTOLE; FEMALE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MICE; MICE, INBRED C57BL; MYOCYTES, CARDIAC; PLACENTA; PREGNANCY; VENTRICULAR FUNCTION;

EID: 85031089674     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.1002/sctm.17-0130     Document Type: Article

References (53)

1. Van Linthout S, Spillmann F, Riad A et al. Human apolipoprotein A-I gene transfer reduces the development of experimental diabetic cardiomyopathy. Circulation 2008;117:1563–1573.
2. Tschope C, Walther T, Königer J et al. Prevention of cardiac fibrosis and left ventricular dysfunction in diabetic cardiomyopathy in rats by transgenic expression of the human tissue kallikrein gene. FASEB J 2004;18:828–835.
3. Chen JX, Zeng H, Reese J et al. Overexpression of angiopoietin-2 impairs myocardial angiogenesis and exacerbates cardiac fibrosis in the diabetic db/db mouse model. Am J Physiol Heart Circ Physiol 2012;302:H1003–H1012.
4. Farhangkhoee H, Khan ZA, Kaur H et al. Vascular endothelial dysfunction in diabetic cardiomyopathy: Pathogenesis and potential treatment targets. Pharmacol Ther 2006;111:384–399.
5. Kruger M, Babicz K, von Frieling-Salewsky M et al. Insulin signaling regulates cardiac titin properties in heart development and diabetic cardiomyopathy. J Mol Cell Cardiol 2010;48:910–916.
6. Raev DC. Which left ventricular function is impaired earlier in the evolution of diabetic cardiomyopathy? An echocardiographic study of young type I diabetic patients. Diabetes Care 1994;17:633–639.
7. Cosson S, Kevorkian JP. Left ventricular diastolic dysfunction: An early sign of diabetic cardiomyopathy?. Diabetes Metab 2003;29:455–466.
8. Stone PH, Muller JE, Hartwell T et al. The effect of diabetes mellitus on prognosis and serial left ventricular function after acute myocardial infarction: Contribution of both coronary disease and diastolic left ventricular dysfunction to the adverse prognosis. The MILIS Study Group. J Am Coll Cardiol 1989;14:49–57.
9. MacDonald MR, Petrie MC, Varyani F et al. Impact of diabetes on outcomes in patients with low and preserved ejection fraction heart failure: An analysis of the Candesartan in Heart failure: Assessment of Reduction in Mortality and morbidity (CHARM) programme. Eur Heart J 2008;29:1377–1385.
10. Falcao-Pires I, Hamdani N, Borbély A et al. Diabetes mellitus worsens diastolic left ventricular dysfunction in aortic stenosis through altered myocardial structure and cardiomyocyte stiffness. Circulation 2011;124:1151–1159.
11. Westermann D, Lindner D, Kasner M et al. Cardiac inflammation contributes to changes in the extracellular matrix in patients with heart failure and normal ejection fraction. Circ Heart Fail 2011;4:44–52.
12. Tschope C, Van Linthout S. New insights in (inter)cellular mechanisms by heart failure with preserved ejection fraction. Curr Heart Fail Rep 2014;11:436–444.
13. Hamdani N, Franssen C, Lourenço A et al. Myocardial titin hypophosphorylation importantly contributes to heart failure with preserved ejection fraction in a rat metabolic risk model. Circ Heart Fail 2013;6:1239–1249.
14. Hamdani N, Paulus WJ. Myocardial titin and collagen in cardiac diastolic dysfunction: Partners in crime. Circulation 2013;128:5–8.
15. Chung CS, Hutchinson KR, Methawasin M et al. Shortening of the elastic tandem immunoglobulin segment of titin leads to diastolic dysfunction. Circulation 2013;128:19–28.
16. Tschope C, Bock CT, Kasner M et al. High prevalence of cardiac parvovirus B19 infection in patients with isolated left ventricular diastolic dysfunction. Circulation 2005;111:879–886.
17. Mohammed SF, Hussain S, Mirzoyev SA et al. Coronary microvascular rarefaction and myocardial fibrosis in heart failure with preserved ejection fraction. Circulation 2015;131:550–559.
18. Van Linthout S, Tschope C. Inflammation—Cause or consequence of heart failure or both? Curr Heart Fail Rep 2017;14:251–265.
19. Franssen C, Chen S, Unger A et al. Myocardial microvascular inflammatory endothelial activation in heart failure with preserved ejection fraction. JACC Heart Fail 2016;4:312–324.
20. Van Linthout S, Savvatis K, Miteva K et al. Mesenchymal stem cells improve murine acute coxsackievirus B3-induced myocarditis. Eur Heart J 2011;32:2168–2178.
21. Savvatis K, van Linthout S, Miteva K et al. Mesenchymal stromal cells but not cardiac fibroblasts exert beneficial systemic immunomodulatory effects in experimental myocarditis. PLoS One 2012;7:e41047.
22. Miteva K, Pappritz K, El-Shafeey M et al. Mesenchymal stromal cells modulate monocytes trafficking in Coxsackievirus B3-induced myocarditis. Stem Cells Translational Medicine 2017;6:1249–1261.
23. Roy R, Brodarac A, Kukucka M et al. Cardioprotection by placenta-derived stromal cells in a murine myocardial infarction model. J Surg Res 2013;185:70–83.
24. Prather WR, Toren A, Meiron M et al. The role of placental-derived adherent stromal cell (PLX-PAD) in the treatment of critical limb ischemia. Cytotherapy 2009;11:427–434.
25. Hare JM, Traverse JH, Henry TD et al. A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. J Am Coll Cardiol 2009;54:2277–2286.
26. Zhang N, Li J, Luo R et al. Bone marrow mesenchymal stem cells induce angiogenesis and attenuate the remodeling of diabetic cardiomyopathy. Exp Clin Endocrinol Diabetes 2008;116:104–111.
27. Li Q, Turdi S, Thomas DP et al. Intra-myocardial delivery of mesenchymal stem cells ameliorates left ventricular and cardiomyocyte contractile dysfunction following myocardial infarction. Toxicol Lett 2008;195:119–126.
28. Ramot Y, Meiron M, Toren A et al. Safety and biodistribution profile of placental-derived mesenchymal stromal cells (PLX-PAD) following intramuscular delivery. Toxicol Pathol 2009;37:606–616.
29. McBride C, Gaupp D, Phinney DG. Quantifying levels of transpolanted murine and human mesenchymal stem cells in vivo via real-time PCR. Cytotherapy 2003;5:7–18.
30. Miteva K, Haag M, Peng J et al. Human cardiac-derived adherent proliferating cells reduce murine acute Coxsackievirus B3-induced myocarditis. PLoS One 2011;6:e28513.
31. Van Linthout S, Lusky M, Collen D et al. Persistent hepatic expression of human apo A-I after transfer with a helper-virus independent adenoviral vector. Gene Ther 2002;9:1520–1528.
32. Spillmann F, Miteva K, Pieske B et al. High-density lipoproteins reduce endothelial-to-mesenchymal transition. Arterioscler Thromb Vasc Biol 2015;35:1774–1777.
33. Spillmann F, Van Linthout S, Miteva K et al. LXR agonism improves TNF-alpha-induced endothelial dysfunction in the absence of its cholesterol-modulating effects. Atherosclerosis 2014;232:1–9.
34. Miteva K, Van Linthout S, Pappritz K et al. Human endomyocardial biopsy specimen-derived stromal cells modulate angiotensin II-induced cardiac remodeling. Stem Cells Translational Medicine 2016;5:1707–1718.
35. Hamdani N, Bishu KG, von Frieling-Salewsky M et al. Deranged myofilament phosphorylation and function in experimental heart failure with preserved ejection fraction. Cardiovasc Res 2013;97:464–471.
36. Hamdani N, Krysiak J, Kreusser MM et al. Crucial role for Ca2(+)/calmodulin-dependent protein kinase-II in regulating diastolic stress of normal and failing hearts via titin phosphorylation. Circ Res 2013;112:664–674.
37. Ren G, Zhang L, Zhao X et al. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2008;2:141–150.
38. Tschope C, Walther T, Escher F et al. Transgenic activation of the kallikrein-kinin system inhibits intramyocardial inflammation, endothelial dysfunction and oxidative stress in experimental diabetic cardiomyopathy. FASEB J 2005;19:2057–2059.
39. Van Linthout S, Miteva K, Tschope C. Crosstalk between fibroblasts and inflammatory cells. Cardiovasc Res 2014;102:258–269.
40. Ismahil MA, Hamid T, Bansal SS et al. Remodeling of the mononuclear phagocyte network underlies chronic inflammation and disease progression in heart failure: Critical importance of the cardiosplenic axis. Circ Res 2014;114:266–282.
41. Paulus WJ, Tschope C. A novel paradigm for heart failure with preserved ejection fraction: Comorbidities drive myocardial dysfunction and remodeling through coronary microvascular endothelial inflammation. J Am Coll Cardiol 2013;62:263–271.
42. Riad A et al. Reduced cardiac performance after differential pharmacological stress in streptozotocin-induced diabetic rats. J Clinic Experiment Cardiol 2010;1:108.
43. van Dijk CG, Oosterhuis NR, Xu YJ et al. Distinct endothelial cell responses in the heart and kidney microvasculature characterize the progression of heart failure with preserved ejection fraction in the obese ZSF1 rat with cardiorenal metabolic syndrome. Circ Heart Fail 2016;9:e002760.
44. Kasal DA, Barhoumi T, Li MW et al. T regulatory lymphocytes prevent aldosterone-induced vascular injury. Hypertension 2012;59:324–330.
45. Mian MO, Barhoumi T, Briet M et al. Deficiency of T-regulatory cells exaggerates angiotensin II-induced microvascular injury by enhancing immune responses. J Hypertens 2016;34:97–108.
46. Cao Y, Xu W, Xiong S. Adoptive transfer of regulatory T cells protects against Coxsackievirus B3-induced cardiac fibrosis. PLoS One 2013;8:e74955.
47. Spillmann F, De Geest B, Muthuramu I et al. Apolipoprotein A-I gene transfer exerts immunomodulatory effects and reduces vascular inflammation and fibrosis in ob/ob mice. J Inflamm (Lond) 2016;13:25.
48. Van Linthout S, Spillmann F, Lorenz M et al. Vascular-protective effects of high-density lipoprotein include the downregulation of the angiotensin II type 1 receptor. Hypertension 2009;53:682–687.
49. van Heerebeek L, Hamdani N, Falcão-Pires I et al. Low myocardial protein kinase G activity in heart failure with preserved ejection fraction. Circulation 2012;126:830–839.
50. Yamasaki R, Wu Y, McNabb M et al. Protein kinase A phosphorylates titin's cardiac-specific N2B domain and reduces passive tension in rat cardiac myocytes. Circ Res 2002;90:1181–1188.
51. Hidalgo C, Hudson B, Bogomolovas J et al. PKC phosphorylation of titin's PEVK element: A novel and conserved pathway for modulating myocardial stiffness. Circ Res 2009;105:631–638, 617 p following 638.
52. Linthout SV, Spillmann F, Schultheiss HP et al. Effects of mesenchymal stromal cells on diabetic cardiomyopathy. Curr Pharm Des 2011;17:3341–3347.
53. Lee RH, Pulin AA, Seo MJ et al. Intravenous hmscs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein tsg-6. Cell Stem Cell 2009;5:54–63.