MicroRNA-1 enhances the angiogenic differentiation of human cardiomyocyte progenitor cells

Journal of Molecular Medicine

Volumn 91, Issue 8, 2013, Pages 1001-1012

  Van Mil, Alain ^a,b   Vrijsen, Krijn R ^a   Goumans, Marie José ^c   Metz, Corina H ^a   Doevendans, Pieter A ^a,b   Sluijter, Joost P ^a,b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b ROYAL NETHERLANDS ACADEMY OF ARTS AND SCIENCES   (Netherlands)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Angiogenesis; Cardiac progenitor cell; Differentiation; microRNA 1; Spred1

Indexed keywords

COLLAGEN; MICRORNA 1; PROTEIN; SPROUTY RELATED EVH1 DOMAIN CONTAINING PROTEIN 1; UNCLASSIFIED DRUG;

ANGIOGENESIS; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; ENDOTHELIUM CELL; FETUS; HEART MUSCLE CELL; HUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SPHEROID CELL; SYSTEMS BIOLOGY; UPREGULATION;

CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICRORNAS; MYOCYTES, CARDIAC; NEOVASCULARIZATION, PHYSIOLOGIC; STEM CELLS;

EID: 84881261064     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-013-1017-1     Document Type: Article

References (35)

1. Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S, Kasahara H, Rota M, Musso E, Urbanek K et al (2003) Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114:763-776 (Pubitemid 37186770)
2. Oh H, Bradfute SB, Gallardo TD, Nakamura T, Gaussin V, Mishina Y, Pocius J, Michael LH, Behringer RR, Garry DJ et al (2003) Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci U S A 100:12313-12318 (Pubitemid 37271557)
3. Messina E, De Angelis L, Frati G, Morrone S, Chimenti S, Fiordaliso F, Salio M, Battaglia M, Latronico MV, Coletta M et al (2004) Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res 95:911-921 (Pubitemid 39435006)
4. Laugwitz KL, Moretti A, Lam J, Gruber P, Chen Y, Woodard S, Lin LZ, Cai CL, Lu MM, Reth M et al (2005) Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433:647-653 (Pubitemid 40282999)
5. Goumans MJ, de Boer TP, Smits AM, van Laake LW, van Vliet P, Metz CH, Korfage TH, Kats KP, Hochstenbach R, Pasterkamp G et al (2007) TGF-beta1 induces efficient differentiation of human cardiomyocyte progenitor cells into functional cardiomyocytes in vitro. Stem Cell Res 1:138-149
6. Bearzi C, Rota M, Hosoda T, Tillmanns J, Nascimbene A, De Angelis A, Yasuzawa-Amano S, Trofimova I, Siggins RW, Lecapitaine N et al (2007) Human cardiac stem cells. Proc Natl Acad Sci U S A 104:14068-14073 (Pubitemid 350003336)
7. Vrijsen KR, Chamuleau SA, Noort WA, Doevendans PA, Sluijter JP (2009) Stem cell therapy for end-stage heart failure: indispensable role for the cell? Curr Opin Organ Transplant 14:560-565
8. Tang XL, Rokosh DG, Guo Y, Bolli R (2010) Cardiac progenitor cells and bone marrow-derived very small embryonic-like stem cells for cardiac repair after myocardial infarction. Circ J 74:390-404
9. Ptaszek LM, Mansour M, Ruskin JN, Chien KR (2012) Towards regenerative therapy for cardiac disease. Lancet 379:933-942
10. Smits AM, van Laake LW, den Ouden K, Schreurs C, Szuhai K, van Echteld CJ, Mummery CL, Doevendans PA, Goumans MJ (2009) Human cardiomyocyte progenitor cell transplantation preserves long-term function of the infarcted mouse myocardium. Cardiovasc Res 83:527-535
11. den Haan MC, Grauss RW, Smits AM, Winter EM, van Tuyn J, Pijnappels DA, Steendijk P, Gittenberger-De Groot AC, van der Laarse A, Fibbe WE et al (2012) Cardiomyogenic differentiation-independent improvement of cardiac function by human cardiomyocyte progenitor cell injection in ischemic mouse hearts. Journal of Cellular and Molecular Medicine 16:1508-1521
12. Sluijter JP, van Mil A, van Vliet P, Metz CH, Liu J, Doevendans PA, Goumans MJ (2010) MicroRNA-1 and -499 regulate differentiation and proliferation in human-derived cardiomyocyte progenitor cells. Arterioscler Thromb Vasc Biol 30:859-868
13. Ivey KN, Muth A, Arnold J, King FW, Yeh RF, Fish JE, Hsiao EC, Schwartz RJ, Conklin BR, Bernstein HS et al (2008) MicroRNA regulation of cell lineages in mouse and human embryonic stem cells. Cell Stem Cell 2:219-229 (Pubitemid 351298595)
14. Wilson KD, Hu S, Venkatasubrahmanyam S, Fu JD, Sun N, Abilez OJ, Baugh JJ, Jia F, Ghosh Z, Li RA et al (2010) Dynamic microRNA expression programs during cardiac differentiation of human embryonic stem cells: role for miR-499. Circ Cardiovasc Genet 3:426-435
15. Howard L, Kane NM, Milligan G, Baker AH (2011) MicroRNAs regulating cell pluripotency and vascular differentiation. Vasc Pharmacol 55:69-78
16. Ohtani K, Dimmeler S (2011) Control of cardiovascular differentiation by microRNAs. Basic Res Cardiol 106:5-11
17. Jakob P, Landmesser U (2012) Role of microRNAs in stem/progenitor cells and cardiovascular repair. Cardiovasc Res 93:614-622
18. Wakioka T, Sasaki A, Kato R, Shouda T, Matsumoto A, Miyoshi K, Tsuneoka M, Komiya S, Baron R, Yoshimura A (2001) Spred is a Sprouty-related suppressor of Ras signalling. Nature 412:647-651 (Pubitemid 32772277)
19. Taniguchi K, Kohno R, Ayada T, Kato R, Ichiyama K, Morisada T, Oike Y, Yonemitsu Y, Maehara Y, Yoshimura A (2007) Spreds are essential for embryonic lymphangiogenesis by regulating vascular endothelial growth factor receptor 3 signaling. Mol Cell Biol 27:4541-4550 (Pubitemid 46906575)
20. Smits AM, van Vliet P, Metz CH, Korfage T, Sluijter JP, Doevendans PA, Goumans MJ (2009) Human cardiomyocyte progenitor cells differentiate into functional mature cardiomyocytes: an in vitro model for studying human cardiac physiology and pathophysiology. Nat Protoc 4:232-243
21. Smits AM, van Oorschot AA, Goumans MJ (2012) Isolation and differentiation of human cardiomyocyte progenitor cells into cardiomyocytes. Methods Mol Biol 879:339-349
22. van Mil A, Grundmann S, Goumans MJ, Lei Z, Oerlemans MI, Jaksani S, Doevendans PA, Sluijter JP (2012) MicroRNA-214 inhibits angiogenesis by targeting Quaking and reducing angiogenic growth factor release. Cardiovasc Res 93:655-665
23. Niemisto A, Dunmire V, Yli-Harja O, Zhang W, Shmulevich I (2005) Robust quantification of in vitro angiogenesis through image analysis. IEEE Trans Med Imaging 24:549-553 (Pubitemid 40538211)
24. Wang S, Aurora AB, Johnson BA, Qi X, McAnally J, Hill JA, Richardson JA, Bassel-Duby R, Olson EN (2008) The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell 15:261-271
25. Fish JE, Santoro MM, Morton SU, Yu S, Yeh RF, Wythe JD, Ivey KN, Bruneau BG, Stainier DY, Srivastava D (2008) miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell 15:272-284
26. Xie C, Huang H, Sun X, Guo Y, Hamblin M, Ritchie RP, Garcia-Barrio MT, Zhang J, Chen YE (2011) MicroRNA-1 regulates smooth muscle cell differentiation by repressing Kruppel-like factor 4. Stem Cells Dev 20:205-210
27. Chen J, Yin H, Jiang Y, Radhakrishnan SK, Huang ZP, Li J, Shi Z, Kilsdonk EP, Gui Y, Wang DZ et al (2011) Induction of microRNA-1 by myocardin in smooth muscle cells inhibits cell proliferation. Arterioscler Thromb Vasc Biol 31:368-375
28. Miyoshi K, Wakioka T, Nishinakamura H, Kamio M, Yang L, Inoue M, Hasegawa M, Yonemitsu Y, Komiya S, Yoshimura A (2004) The Sprouty-related protein, Spred, inhibits cell motility, metastasis, and Rho-mediated actin reorganization. Oncogene 23:5567-5576 (Pubitemid 39093034)
29. Yoshida T, Hisamoto T, Akiba J, Koga H, Nakamura K, Tokunaga Y, Hanada S, Kumemura H, Maeyama M, Harada M et al (2006) Spreds, inhibitors of the Ras/ERK signal transduction, are dysregulated in human hepatocellular carcinoma and linked to the malignant phenotype of tumors. Oncogene 25:6056-6066 (Pubitemid 44562404)
30. Zhao Y, Samal E, Srivastava D (2005) Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature 436:214-220 (Pubitemid 41021266)
31. Chen JF (2006) The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 38:228-233 (Pubitemid 43177239)
32. Bastian I, Tam Tam S, Zhou XF, Kazenwadel J, Van der Hoek M, Michael MZ, Gibbins I, Haberberger RV (2011) Differential expression of microRNA-1 in dorsal root ganglion neurons. Histochem Cell Biol 135:37-45
33. Carmeliet P, Tessier-Lavigne M (2005) Common mechanisms of nerve and blood vessel wiring. Nature 436:193-200 (Pubitemid 41021263)
34. di Bari MG, Lutsiak ME, Takai S, Mostbock S, Farsaci B, Semnani RT, Wakefield LM, Schlom J, Sabzevari H (2009) TGF-beta modulates the functionality of tumor-infiltrating CD8+ T cells through effects on TCR signaling and Spred1 expression. Cancer Immunol Immunother 58:1809-1818
35. Nakajima N, Takahashi T, Kitamura R, Isodono K, Asada S, Ueyama T, Matsubara H, Oh H (2006) MicroRNA-1 facilitates skeletal myogenic differentiation without affecting osteoblastic and adipogenic differentiation. Biochem Biophys Res Commun 350:1006-1012 (Pubitemid 44584193)