RhoA determines lineage fate of mesenchymal stem cells by modulating CTGF-VEGF complex in extracellular matrix

Nature Communications

Volumn 7, Issue , 2016, Pages

  Li, Changjun ^a,c   Zhen, Gehua ^a   Chai, Yu ^a   Xie, Liang ^a   Crane, Janet L ^a   Farber, Emily ^b   Farber, Charles R ^b   Luo, Xianghang ^c   Gao, Peisong ^d   Cao, Xu ^a   Wan, Mei ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c CENTRAL SOUTH UNIVERSITY   (China)

^d JOHNS HOPKINS ASTHMA AND ALLERGY CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; 4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ALPHA SMOOTH MUSCLE ACTIN; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CD31 ANTIGEN; COLLAGEN TYPE 1; CONNECTIVE TISSUE GROWTH FACTOR; FASUDIL; FIBRONECTIN; LEPTIN RECEPTOR; MESSENGER RNA; MULTIPROTEIN COMPLEX; NESTIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; STROMELYSIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN; CTGF PROTEIN, MOUSE; MMP3 PROTEIN, MOUSE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO KINASE; RHOA PROTEIN, MOUSE; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

CELLS AND CELL COMPONENTS; DIFFERENTIATION; GROWTH; PATHOLOGY; PHYSIOLOGICAL RESPONSE; PROTEIN;

ADIPOGENESIS; ADVENTITIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA; ARTERY INJURY; ARTICLE; BLOOD SAMPLING; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL FATE; CELL INTERACTION; CELL LINEAGE; CELL SPECIFICITY; CHONDROGENESIS; COMPLEX FORMATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME INACTIVATION; EXTRACELLULAR MATRIX; FEMORAL ARTERY; INTIMA; INTRACELLULAR SIGNALING; MALE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; MYOFIBROBLAST; NEOINTIMA; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; RAT; STEM CELL EXPANSION; TISSUE REPAIR; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; INJURIES; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; REGENERATION; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; TRANSGENIC MOUSE; WOUND HEALING;

ANIMALS; CELL DIFFERENTIATION; CONNECTIVE TISSUE GROWTH FACTOR; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; FEMORAL ARTERY; GENE EXPRESSION REGULATION; MALE; MATRIX METALLOPROTEINASE 3; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYOFIBROBLASTS; RATS; RATS, SPRAGUE-DAWLEY; REGENERATION; RHO GTP-BINDING PROTEINS; RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WOUND HEALING;

EID: 84964614331     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11455     Document Type: Article

References (70)

1. Bianco, P., Riminucci, M., Gronthos, S. & Robey, P. G. Bone marrow stromal stem cells: Nature, biology, and potential applications. Stem Cells 19, 180-192 (2001).
2. Discher, D. E., Mooney, D. J. & Zandstra, P. W. Growth factors, matrices, and forces combine and control stem cells. Science 324, 1673-1677 (2009).
3. Guilak,, F. et al. Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 5, 17-26 (2009).
4. Humphrey, J. D., Dufresne, E. R. & Schwartz, M. A. Mechanotransduction and extracellular matrix homeostasis. Nat. Rev. Mol. Cell Biol. 15, 802-812 (2014).
5. Dingal, P. C. & Discher, D. E. Combining insoluble and soluble factors to steer stem cell fate. Nat. Mater. 13, 532-537 (2014).
6. Tenney, R. M. & Discher, D. E. Stem cells, microenvironment mechanics, and growth factor activation. Curr. Opin. Cell Biol. 21, 630-635 (2009).
7. Newby, A. C. & Zaltsman, A. B. Molecular mechanisms in intimal hyperplasia. J. Pathol. 190, 300-309 (2000).
8. Zalewski, A. & Shi, Y. Vascular myofibroblasts: lessons from coronary repair and remodeling. Arterioscler. Thromb.Vasc. Biol. 17, 417-422 (1997).
9. Forte, A., Della Corte, A., De Feo, M., Cerasuolo, F. & Cipollaro, M. Role of myofibroblasts in vascular remodelling: focus on restenosis and aneurysm. Cardiovasc. Res. 88, 395-405 (2010).
10. Goel, S. A., Guo, L. W., Liu, B. & Kent, K. C. Mechanisms of post-intervention arterial remodelling. Cardiovasc. Res. 96, 363-371 (2012).
11. Mendez-Ferrer, S. et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466, 829-834 (2010).
12. Klein, D. et al. Nestin(+) tissue-resident multipotent stem cells contribute to tumor progression by differentiating into pericytes and smooth muscle cells resulting in blood vessel remodeling. Front. Oncol. 4, 169 (2014).
13. Wan, M. et al. Injury-activated transforming growth factor beta controls mobilization of mesenchymal stem cells for tissue remodeling. Stem Cells 30, 2498-2511 (2012).
14. Wang, W. et al. Mesenchymal stem cells recruited by active TGFbeta contribute to osteogenic vascular calcification. Stem Cells Dev. 23, 1392-1404 (2014).
15. Kipshidze, N. et al. Role of the endothelium in modulating neointimal formation: vasculoprotective approaches to attenuate restenosis after percutaneous coronary interventions. J. Am. Coll. Cardiol. 44, 733-739 (2004).
16. Kong, D. et al. Enhanced inhibition of neointimal hyperplasia by genetically engineered endothelial progenitor cells. Circulation 109, 1769-1775 (2004).
17. Xing, D. et al. Endothelial cells overexpressing interleukin-8 receptors reduce inflammatory and neointimal responses to arterial injury. Circulation 125, 1533-1541 (2012).
18. Creighton, W. M. et al. Regional variability in the time course of TGF-β1 expression, cellular proliferation and extracellular matrix expansion following arterial injury. Growth Factors 14, 297-306 (1997).
19. Ryan, S. T., Koteliansky, V. E., Gotwals, P. J. & Lindner, V. Transforming growth factor-beta-dependent events in vascular remodeling following arterial injury. J. Vasc. Res. 40, 37-46 (2003).
20. Duffield, J. S., Lupher, M., Thannickal, V. J. & Wynn, T. A. Host responses in tissue repair and fibrosis. Annu. Rev. Pathol. 8, 241-276 (2013).
21. Weber, K. T., Sun, Y., Bhattacharya, S. K., Ahokas, R. A. & Gerling, I. C. Myofibroblast-mediated mechanisms of pathological remodelling of the heart. Nat. Rev. Cardiol. 10, 15-26 (2013).
22. Derynck, R. TGF-beta-receptor-mediated signaling. Trends BiochemSci. 19, 548-553 (1994).
23. Lee, M. K. et al. TGF-beta activates Erk MAP kinase signalling through direct phosphorylation of ShcA. EMBO J. 26, 3957-3967 (2007).
24. Yamashita, M. et al. TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-beta. Mol. Cell 31, 918-924 (2008).
25. Guo, X., Stice, S. L., Boyd, N. L. & Chen, S. Y. A novel in vitro model system for smooth muscle differentiation from human embryonic stem cell-derived mesenchymal cells. Am. J. Physiol. Cell Physiol. 304, C289-C298 (2013).
26. Kakudo, N. et al. Effects of transforming growth factor-beta1 on cell motility, collagen gel contraction, myofibroblastic differentiation, and extracellular matrix expression of human adipose-derived stem cell. Hum. Cell 25, 87-95 (2012).
27. Mignone, J. L., Kukekov, V., Chiang, A. S., Steindler, D. & Enikolopov, G. Neural stem and progenitor cells in nestin-GFP transgenic mice. J. Comp. Neurol. 469, 311-324 (2004).
28. Zhou, B. o. O., Yue, R., Murphy Malea, M., Peyer, J. G. & Morrison Sean, J. Leptin-receptor-expressing mesenchymal stromal cells represent the main source of bone formed by adult bone marrow. Cell Stem Cell 15, 154-168 (2014).
29. Mizoguchi, T. et al. Osterix marks distinct waves of primitive and definitive stromal progenitors during bone marrow development. Dev. Cell 29, 340-349 (2014).
30. Tang, Y. et al. TGF-beta1-induced migration of bone mesenchymal stem cells couples bone resorption with formation. Nature Med. 15, 757-765 (2009).
31. Page-McCaw, A., Ewald, A. J. & Werb, Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 8, 221-233 (2007).
32. de Winter, P., Leoni, P. & Abraham, D. Connective tissue growth factor: structure-function relationships of a mosaic, multifunctional protein. Growth Factors 26, 80-91 (2008).
33. Inoki, I. et al. Connective tissue growth factor binds vascular endothelial growth factor (VEGF) and inhibits VEGF-induced angiogenesis. FASEB J. 15, 219-221 (2001).
34. Ponticos, M. Connective tissue growth factor (CCN2) in blood vessels. Vasc. Pharmacol. 58, 189-193 (2013).
35. Wu, J. M. F. et al. Circulating cells contribute to cardiomyocyte regeneration after injury. Circ. Res. 116, 633-641 (2015).
36. Loffredo Francesco, S. et al. Growth differentiation factor 11 is a circulating factor that reverses age-related cardiac hypertrophy. Cell 153, 828-839 (2013).
37. Herring, B. P., Hoggatt, A. M., Burlak, C. & Offermanns, S. Previously differentiated medial vascular smooth muscle cells contribute to neointima formation following vascular injury. Vasc. Cell 6, 21-21 (2014).
38. Tanaka, K., Sata, M., Hirata, Y. & Nagai, R. Diverse contribution of bone marrow cells to neointimal hyperplasia after mechanical vascular injuries. Circ. Res. 93, 783-790 (2003).
39. Vardouli, L., Moustakas, A. & Stournaras, C. LIM-kinase 2 and cofilin phosphorylation mediate actin cytoskeleton reorganization induced by transforming growth factor-β. J. Biol. Chem. 280, 11448-11457 (2005).
40. Vardouli, L., Vasilaki, E., Papadimitriou, E., Kardassis, D. & Stournaras, C. A novel mechanism of TGFβ-induced actin reorganization mediated by Smad proteins and Rho GTPases. FEBS J. 275, 4074-4087 (2008).
41. Papadimitriou, E., Kardassis, D., Moustakas, A. & Stournaras, C. TGF β-induced Early Activation of the Small GTPase RhoA is Smad2/3-independent and Involves Src and the Guanine Nucleotide Exchange Factor Vav2. Cell. Physiol. Biochem. 28, 229-238 (2011).
42. Muslin, A. J. MAPK signalling in cardiovascular health and disease: molecular mechanisms and therapeutic targets. Clin. Sci. 115, 203-218 (2008).
43. Wang, C. H. et al. Late-outgrowth endothelial cells attenuate intimal hyperplasia contributed by mesenchymal stem cells after vascular injury. Arterioscler. Thromb.Vasc. Biol. 28, 54-60 (2008).
44. Ainsworth, C. Cell biology: Stretching the imagination. Nature 456, 696-699 (2008).
45. Engler, A. J., Sen, S., Sweeney, H. L. & Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689 (2006).
46. McBeath, R., Pirone, D. M., Nelson, C. M., Bhadriraju, K. & Chen, C. S. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6, 483-495 (2004).
47. Sordella, R., Jiang, W., Chen, G. C., Curto, M. & Settleman, J. Modulation of rho GTPase signaling regulates a switch between adipogenesis and myogenesis. Cell 113, 147-158 (2003).
48. Kshitiz, A. J., Kim, D. H. & Levchenko, A. Concise review: mechanotransduction via p190RhoGAP regulates a switch between cardiomyogenic and endothelial lineages in adult cardiac progenitors. Stem Cells 32, 1999-2007 (2014).
49. van Nieuw Amerongen, G. P. Involvement of RhoA/Rho Kinase Signaling in VEGF-Induced Endothelial Cell Migration and Angiogenesis in vitro. Arterioscler. Thromb.Vasc. Biol. 23, 211-217 (2002).
50. Yin, L. et al. Fasudil inhibits vascular endothelial growth factor-induced angiogenesis in vitro and in vivo. Mol. Cancer Ther. 6, 1517-1525 (2007).
51. Borikova, A. L. et al. Rho kinase inhibition rescues the endothelial cell cerebral cavernous malformation phenotype. J. Biol. Chem. 285, 11760-11764 (2010).
52. Mavria, G. et al. ERK-MAPK signaling opposes Rho-kinase to promote endothelial cell survival and sprouting during angiogenesis. Cancer Cell 9, 33-44 (2006).
53. Nohria, A. et al. Rho kinase inhibition improves endothelial function in human subjects with coronary artery disease. Circ. Res. 99, 1426-1432 (2006).
54. Richardson, B. T., Dibble, C. F., Borikova, A. L. & Johnson, G. L. Cerebral cavernous malformation is a vascular disease associated with activated RhoA signaling. Biol. Chem. 394, 35-42 (2013).
55. Lambert, V. et al. MMP-2 and MMP-9 synergize in promoting choroidal neovascularization. FASEB J. 17, 2290 (2003).
56. Vu, T. H. et al. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93, 411-422 (1998).
57. Bergers, G. et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat. Cell Biol. 2, 737-744 (2000).
58. Margariti, A. et al. Direct reprogramming of fibroblasts into endothelial cells capable of angiogenesis and reendothelialization in tissue-engineered vessels. Proc. Natl Acad. Sci. USA 109, 13793-13798 (2012).
59. Li, J. et al. Conversion of human fibroblasts to functional endothelial cells by defined factors. Arterioscler Thromb Vasc Biol. 33, 1366 (2013).
60. Hu, E. & Lee, D. Rho kinase as potential therapeutic target for cardiovascular diseases: opportunities and challenges. Expert Opin. Ther. Targets 9, 715-736 (2005).
61. Sata, M. et al. A mouse model of vascular injury that induces rapid onset of medial cell apoptosis followed by reproducible neointimal hyperplasia. J. Mol. Cell. Cardiol. 32, 2097-2104 (2000).
62. Sata, M., Fukuda, D., Tanaka, K., Kaneda, Y., Yashiro, H. & Shirakawa, I. The role of circulating precursors in vascular repair and lesion formation. J. Cell Mol. Med. 9, 557-568 (2005).
63. Tanaka, K. et al. Circulating progenitor cells contribute to neointimal formation in nonirradiated chimeric mice. FASEB J. 22, 428-436 (2008).
64. Wan, M. et al. LRP6 mediates cAMP generation by g protein-coupled receptors through regulating the membrane targeting of G alpha(s). Sci. Signal. 4, 12 (2011).
65. Wan, M. et al. Parathyroid hormone signaling through low-density lipoprotein-related protein 6. Genes Dev. 22, 2968-2979 (2008).
66. Kimura, M. et al. Impaired acetylcholine-induced release of nitric oxide in the aorta of male aromatase-knockout mice: regulation of nitric oxide production by endogenous sex hormones in males. Circ. Res. 93, 1267-1271 (2003).
67. Du, P., Kibbe, W. A. & Lin, S. M. lumi: a pipeline for processing Illumina microarray. Bioinformatics 24, 1547-1548 (2008).
68. Hsueh, H. M., Chen, J. J. & Kodell, R. L. Comparison of methods for estimating the number of true null hypotheses in multiplicity testing. J. Biopharm. Stat. 13, 675-689 (2003).
69. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408 (2001).
70. Pflieger, D. et al. Comparative proteomic analysis of extracellular matrix proteins secreted by two types of skin fibroblasts. Proteomics 6, 5868-5879 (2006).