Mesenchymal stem cell secreted platelet derived growth factor exerts a pro-migratory effect on resident Cardiac Atrial appendage Stem Cells

Journal of Molecular and Cellular Cardiology

Volumn 66, Issue , 2014, Pages 177-188

  Windmolders, Severina ^a,b   De Boeck, Astrid ^c   Koninckx, Remco ^a,b   Daniëls, Annick ^a   De Wever, Olivier ^c   Bracke, Marc ^c   Hendrikx, Marc ^a,b   Hensen, Karen ^a,b   Rummens, Jean Luc ^a,b  

^a JESSA HOSPITAL   (Belgium)

^b HASSELT UNIVERSITY   (Belgium)

^c GHENT UNIVERSITY HOSPITAL   (Belgium)

Author keywords

Cardiac stem cells; Conditioned medium; Mesenchymal stem cells; Migration; Myocardial infarction; Platelet derived growth factor

Indexed keywords

ALDEHYDE DEHYDROGENASE; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR AA; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN TYROSINE KINASE;

ARTICLE; CARDIAC ATRIAL APPENDAGE STEM CELL; CELL DIFFERENTIATION; CELL EXPANSION; CELL ISOLATION; CELL MIGRATION; CULTURE MEDIUM; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HEART ATRIUM APPENDAGE; HEART MUSCLE INJURY; HEART VENTRICLE REMODELING; HUMAN; HUMAN CELL; HUMAN TISSUE; MESENCHYMAL STEM CELL; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

3D; ALDEHYDE DEHYDROGENASE; ALDH; ANNEALING TEMPERATURE; AT; AXL RECEPTOR; AXLR; BM-SCS; BONE MARROW STEM CELLS; CARDIAC ATRIAL APPENDAGE STEM CELLS; CARDIAC STEM CELLS; CARDIAC TROPONIN; CASCS; CFU-FS; COLONY-FORMING-UNIT FIBROBLASTS; CONDITIONED MEDIUM; CSCS; CTN; DEAB; DIETHYLAMINO-BENZALDEHYDE; EGFR; ELISA; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPIDERMAL GROWTH FACTOR RECEPTOR; FAK; FCS; FETAL CALF SERUM; FGFR; FIBROBLAST GROWTH FACTOR RECEPTOR; FLUORESCENCE MINUS ONE; FMO; FOCAL ADHESION KINASE; GFP; GREEN FLUORESCENT PROTEIN; IHD; INSR; INSULIN RECEPTOR; ISCHEMIC HEART DISEASE; LG-DMEM; LOW-GLUCOSE DULBECCO'S MODIFIED EAGLE MEDIUM; MATRIX METALLOPROTEINASES; MESENCHYMAL STEM CELL CONDITIONED MEDIUM; MESENCHYMAL STEM CELLS; MI; MIGRATION; MMPS; MSC-CM; MSCS; MYOCARDIAL INFARCTION; NEONATAL RAT CARDIOMYOCYTES; NRCMS; P/S; PDGF; PDGFR; PENICILLIN/STREPTOMYCIN; PHOSPHO-INOSITIDE-3 KINASE; PHOSPHOLIPASE C-Γ; PI3K; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PLC-Γ; RALDH2; RECEPTOR TYROSINE KINASE; RETINALDEHYDE DEHYDROGENASE 2; REVERSE TRANSCRIPTASE PCR; RT-PCR; RTK; T-BOX 18; TBX18; TGF-Β; THREE-DIMENSIONAL; THYMOSIN Β4; TRANSFORMING GROWTH FACTOR-Β; TΒ4; VASCULAR ENDOTHELIAL GROWTH FACTOR; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR; VEGF; VEGFR; WILM'S TUMOR 1; WT1;

ADULT STEM CELLS; ANIMALS; BIOLOGICAL MARKERS; CELL COUNT; CELL DIFFERENTIATION; CELL MOVEMENT; CULTURE MEDIA, CONDITIONED; GENE EXPRESSION; HEART ATRIA; HOMEODOMAIN PROTEINS; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MESENCHYMAL STROMAL CELLS; MYOCYTES, CARDIAC; OCTAMER TRANSCRIPTION FACTOR-3; PLATELET-DERIVED GROWTH FACTOR; PRIMARY CELL CULTURE; PROTO-ONCOGENE PROTEINS C-MYC; RATS;

EID: 84891700345     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.11.016     Document Type: Article

References (48)

1. Orlic D., Kajstura J., Chimenti S., Jakoniuk I., Anderson S.M., Li B., et al. Bone marrow cells regenerate infarcted myocardium. Nature 2001, 410(6829):701-705.
2. Kinnaird T., Stabile E., Burnett M.S., Shou M., Lee C.W., Barr S., et al. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation 2004, 109(12):1543-1549.
3. Leri A., Kajstura J., Anversa P. Role of cardiac stem cells in cardiac pathophysiology: a paradigm shift in human myocardial biology. Circ Res 2011, 109(8):941-961.
4. Koninckx R., Daniels A., Windmolders S., Mees U., Macianskiene R., Mubagwa K., et al. The cardiac atrial appendage stem cell: a new and promising candidate for myocardial repair. Cardiovasc Res 2012, 97(3):413-423.
5. Bolli R., Chugh A.R., D'Amario D., Loughran J.H., Stoddard M.F., Ikram S., et al. Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet 2011, 378(9806):1847-1857.
6. Makkar R.R., Smith R.R., Cheng K., Malliaras K., Thomson L.E., Berman D., et al. Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet 2012, 379(9819):895-904.
7. Smith R.R., Barile L., Cho H.C., Leppo M.K., Hare J.M., Messina E., et al. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 2007, 115(7):896-908.
8. Amado L.C., Saliaris A.P., Schuleri K.H., St John M., Xie J.S., Cattaneo S., et al. Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction. Proc Natl Acad Sci U S A 2005, 102(32):11474-11479.
9. Schachinger V., Erbs S., Elsasser A., Haberbosch W., Hambrecht R., Holschermann H., et al. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N Engl J Med 2006, 355(12):1210-1221.
10. Abdel-Latif A., Bolli R., Tleyjeh I.M., Montori V.M., Perin E.C., Hornung C.A., et al. Adult bone marrow-derived cells for cardiac repair: a systematic review and meta-analysis. Arch Intern Med 2007, 167(10):989-997.
11. Kinnaird T., Stabile E., Burnett M.S., Lee C.W., Barr S., Fuchs S., et al. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res 2004, 94(5):678-685.
12. Timmers L., Lim S.K., Hoefer I.E., Arslan F., Lai R.C., van Oorschot A.A., et al. Human mesenchymal stem cell-conditioned medium improves cardiac function following myocardial infarction. Stem Cell Res 2011, 6(3):206-214.
13. Gnecchi M., He H., Liang O.D., Melo L.G., Morello F., Mu H., et al. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 2005, 11(4):367-368.
14. Kamihata H., Matsubara H., Nishiue T., Fujiyama S., Tsutsumi Y., Ozono R., et al. Implantation of bone marrow mononuclear cells into ischemic myocardium enhances collateral perfusion and regional function via side supply of angioblasts, angiogenic ligands, and cytokines. Circulation 2001, 104(9):1046-1052.
15. Benzhi C., Limei Z., Ning W., Jiaqi L., Songling Z., Fanyu M., et al. Bone marrow mesenchymal stem cells upregulate transient outward potassium currents in postnatal rat ventricular myocytes. J Mol Cell Cardiol 2009, 47(1):41-48.
16. Mias C., Lairez O., Trouche E., Roncalli J., Calise D., Seguelas M.H., et al. Mesenchymal stem cells promote matrix metalloproteinase secretion by cardiac fibroblasts and reduce cardiac ventricular fibrosis after myocardial infarction. Stem Cells 2009, 27(11):2734-2743.
17. Lee R.H., Pulin A.A., Seo M.J., Kota D.J., Ylostalo J., Larson B.L., 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(1):54-63.
18. Koninckx R., Hensen K., Daniels A., Moreels M., Lambrichts I., Jongen H., et al. Human bone marrow stem cells co-cultured with neonatal rat cardiomyocytes display limited cardiomyogenic plasticity. Cytotherapy 2009, 11(6):778-792.
19. De Wever O., Nguyen Q.D., Van Hoorde L., Bracke M., Bruyneel E., Gespach C., et al. Tenascin-C and SF/HGF produced by myofibroblasts in vitro provide convergent pro-invasive signals to human colon cancer cells through RhoA and Rac. FASEB J 2004, 18(9):1016-1018.
20. De Wever O., Hendrix A., De Boeck A., Westbroek W., Braems G., Emami S., et al. Modeling and quantification of cancer cell invasion through collagen type I matrices. Int J Dev Biol 2010, 54(5):887-896.
21. Ball S.G., Shuttleworth C.A., Kielty C.M. Vascular endothelial growth factor can signal through platelet-derived growth factor receptors. J Cell Biol 2007, 177(3):489-500.
22. Chong J.J., Chandrakanthan V., Xaymardan M., Asli N.S., Li J., Ahmed I., et al. Adult cardiac-resident MSC-like stem cells with a proepicardial origin. Cell Stem Cell 2011, 9(6):527-540.
23. Park S.H., Kim K.W., Chun Y.S., Kim J.C. Human mesenchymal stem cells differentiate into keratocyte-like cells in keratocyte-conditioned medium. Exp Eye Res 2012, 101:16-26.
24. Koninckx R. Unpublished results. 2011.
25. Andrae J., Gallini R., Betsholtz C. Role of platelet-derived growth factors in physiology and medicine. Genes Dev 2008, 22(10):1276-1312.
26. Salazar K.D., Lankford S.M., Brody A.R. Mesenchymal stem cells produce Wnt isoforms and TGF-beta1 that mediate proliferation and procollagen expression by lung fibroblasts. Am J Physiol Lung Cell Mol Physiol 2009, 297(5):L1002-L1011.
27. De Boeck A., Hendrix A., Maynard D., Van Bockstal M., Daniels A., Pauwels P., et al. Differential secretome analysis of cancer-associated fibroblasts and bone marrow-derived precursors to identify microenvironmental regulators of colon cancer progression. Proteomics 2012, 13(2):379-388.
28. Tate M.C., Garcia A.J., Keselowsky B.G., Schumm M.A., Archer D.R., LaPlaca M.C. Specific beta1 integrins mediate adhesion, migration, and differentiation of neural progenitors derived from the embryonic striatum. Mol Cell Neurosci 2004, 27(1):22-31.
29. Thankamony S.P., Sackstein R. Enforced hematopoietic cell E- and L-selectin ligand (HCELL) expression primes transendothelial migration of human mesenchymal stem cells. Proc Natl Acad Sci U S A 2011, 108(6):2258-2263.
30. Buhring H.J., Battula V.L., Treml S., Schewe B., Kanz L., Vogel W. Novel markers for the prospective isolation of human MSC. Ann N Y Acad Sci 2007, 1106:262-271.
31. Koninckx R., Daniels A., Windmolders S., Carlotti F., Mees U., Steels P., et al. Mesenchymal stem cells or cardiac progenitors for cardiac repairα A comparative study. Cell Mol Life Sci 2011, 68(12):2141-2156.
32. Moreb J.S., Ucar D., Han S., Amory J.K., Goldstein A.S., Ostmark B., et al. The enzymatic activity of human aldehyde dehydrogenases 1A2 and 2 (ALDH1A2 and ALDH2) is detected by Aldefluor, inhibited by diethylaminobenzaldehyde and has significant effects on cell proliferation and drug resistance. Chem Biol Interact 2012, 195(1):52-60.
33. Smart N., Bollini S., Dube K.N., Vieira J.M., Zhou B., Davidson S., et al. De novo cardiomyocytes from within the activated adult heart after injury. Nature 2011, 474(7353):640-644.
34. Limana F., Bertolami C., Mangoni A., Di Carlo A., Avitabile D., Mocini D., et al. Myocardial infarction induces embryonic reprogramming of epicardial c-kit(+) cells: role of the pericardial fluid. J Mol Cell Cardiol 2010, 48(4):609-618.
35. Hatzistergos K.E., Quevedo H., Oskouei B.N., Hu Q., Feigenbaum G.S., Margitich I.S., et al. Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ Res 2010, 107(7):913-922.
36. Nakanishi C., Yamagishi M., Yamahara K., Hagino I., Mori H., Sawa Y., et al. Activation of cardiac progenitor cells through paracrine effects of mesenchymal stem cells. Biochem Biophys Res Commun 2008, 374(1):11-16.
37. Wang H., Yin Y., Li W., Zhao X., Yu Y., Zhu J., et al. Over-expression of PDGFR-beta promotes PDGF-induced proliferation, migration, and angiogenesis of EPCs through PI3K/Akt signaling pathway. PLoS ONE 2012, 7(2):e30503.
38. Ozaki Y., Nishimura M., Sekiya K., Suehiro F., Kanawa M., Nikawa H., et al. Comprehensive analysis of chemotactic factors for bone marrow mesenchymal stem cells. Stem Cells Dev 2007, 16(1):119-129.
39. Anand-Apte B., Zetter B. Signaling mechanisms in growth factor-stimulated cell motility. Stem Cells 1997, 15(4):259-267.
40. Zisa D., Shabbir A., Mastri M., Suzuki G., Lee T. Intramuscular VEGF repairs the failing heart: role of host-derived growth factors and mobilization of progenitor cells. Am J Physiol Regul Integr Comp Physiol 2009, 297(5):R1503-R1515.
41. Tang J., Wang J., Kong X., Yang J., Guo L., Zheng F., et al. Vascular endothelial growth factor promotes cardiac stem cell migration via the PI3K/Akt pathway. Exp Cell Res 2009, 315(20):3521-3531.
42. Bujak M., Frangogiannis N.G. The role of TGF-beta signaling in myocardial infarction and cardiac remodeling. Cardiovasc Res 2007, 74(2):184-195.
43. Dobaczewski M., Chen W., Frangogiannis N.G. Transforming growth factor (TGF)-beta signaling in cardiac remodeling. J Mol Cell Cardiol 2011, 51(4):600-606.
44. Brenmoehl J., Miller S.N., Hofmann C., Vogl D., Falk W., Scholmerich J., et al. Transforming growth factor-beta 1 induces intestinal myofibroblast differentiation and modulates their migration. World J Gastroenterol 2009, 15(12):1431-1442.
45. Liu Y.R., Ye W.L., Zeng X.M., Ren W.H., Zhang Y.Q., Mei Y.A. K+ channels and the cAMP-PKA pathway modulate TGF-beta1-induced migration of rat vascular myofibroblasts. J Cell Physiol 2008, 216(3):835-843.
46. Howard C., Murray P.E., Namerow K.N. Dental pulp stem cell migration. J Endod 2010, 36(12):1963-1966.
47. Wan M., Li C., Zhen G., Jiao K., He W., Jia X., et al. Injury-activated transforming growth factor beta controls mobilization of mesenchymal stem cells for tissue remodeling. Stem Cells 2012, 30(11):2498-2511.
48. Sun X., Gao X., Zhou L., Sun L., Lu C. PDGF-BB-induced MT1-MMP expression regulates proliferation and invasion of mesenchymal stem cells in 3-dimensional collagen via MEK/ERK1/2 and PI3K/AKT signaling. Cell Signal 2013, 25(5):1279-1287.