Concise review: Mechanotransduction via p190RhoGAP regulates a switch between cardiomyogenic and endothelial lineages in adult cardiac progenitors

Stem Cells

Volumn 32, Issue 8, 2014, Pages 1999-2007

  Kshitiz, ^a,b   Afzal, Junaid ^c   Kim, Deok Ho ^a,b   Levchenko, Andre ^d  

^a University of Washington   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c DEPARTMENT OF PATHOLOGY   (United States)

^d Yale University   (United States)

Author keywords

Adult stem cells; Angiogenesis; Cardiac differentiation; Cell signaling; Endothelial differentiation; Stem cell microenvironment interactions; Tissue regeneration; Tissue specific stem cells

Indexed keywords

ANGIOGENESIS; CELL LINEAGE; CELL POPULATION; CELL SUBPOPULATION; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; GENETIC MANIPULATION; HEART MUSCLE; HUMAN; MECHANOTRANSDUCTION; MULTIPOTENT STEM CELL; MUSCLE RIGIDITY; NONHUMAN; PHASE 2 CLINICAL TRIAL (TOPIC); REVIEW; TISSUE DIFFERENTIATION; TISSUE REGENERATION; ADULT STEM CELL; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; HEART MUSCLE CELL; METABOLISM; PHYSIOLOGY;

ARHGAP35 PROTEIN, HUMAN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; REPRESSOR PROTEIN;

ADULT STEM CELLS; ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; ENDOTHELIAL CELLS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MYOCYTES, CARDIAC; REPRESSOR PROTEINS;

EID: 84904428711     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1700     Document Type: Review

References (83)

1. Gupta K, Kim DH, Ellison D, et al. Lab-on-a-chip devices as an emerging platform for stem cell biology. Lab Chip 2010; 10: 2019-2031.
2. Kajstura J, Rota M, Cappetta D, et al. Cardiomyogenesis in the aging and failing human heart. Circulation 2012; 126: 1869-1881.
3. Levenstein ME, Berggren WT, Lee JE, et al. Secreted proteoglycans directly mediate human embryonic stem cell-basic fibroblast growth factor 2 interactions critical for proliferation. Stem Cells 2008; 26: 3099-3107.
4. Wu D, Pang Y, Ke Y, et al. A conserved mechanism for control of human and mouse embryonic stem cell pluripotency and differentiation by shp2 tyrosine phosphatase. PLoS One 2009; 4: e4914.
5. Hosoda T, Zheng H, Cabral-da-Silva M, et al. Human cardiac stem cell differentiation is regulated by a mircrine mechanism. Circulation 2011; 123: 1287-1296.
6. Mammoto A, Connor KM, Mammoto T, et al. A mechanosensitive transcriptional mechanism that controls angiogenesis. Nature 2009; 457: 1103-1108.
7. Howard B, Ashworth A,. Signalling pathways implicated in early mammary gland morphogenesis and breast cancer. PLoS Genet 2006; 2: e112.
8. Engler AJ, Sen S, Sweeney HL, et al. Matrix elasticity directs stem cell lineage specification. Cell 2006; 126: 677-689.
9. Gilbert PM, Havenstrite KL, Magnusson KE, et al. Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 2010; 329: 1078-1081.
10. Ingber DE,. Mechanical signaling and the cellular response to extracellular matrix in angiogenesis and cardiovascular physiology. Circ Res 2002; 91: 877-887.
11. Kim DH, Provenzano PP, Smith CL, et al. Matrix nanotopography as a regulator of cell function. J Cell Biol 2012; 197: 351-360.
12. Saez A, Ghibaudo M, Buguin A, et al. Rigidity-driven growth and migration of epithelial cells on microstructured anisotropic substrates. Proc Natl Acad Sci USA 2007; 104: 8281-8286.
13. Kim DH, Kshitiz, Smith RR, et al. Nanopatterned cardiac cell patches promote stem cell niche formation and myocardial regeneration. Integr Biol 2012; 4: 1019-1033.
14. Kshitiz, Hubbi ME, Ahn EH, et al. Matrix rigidity controls endothelial differentiation and morphogenesis of cardiac precursors. Sci Signal 2012; 5: ra41.
15. Bergmann O, Bhardwaj RD, Bernard S, et al. Evidence for cardiomyocyte renewal in humans. Science 2009; 324: 98-102.
16. Senyo SE, Steinhauser ML, Pizzimenti CL, et al. Mammalian heart renewal by pre-existing cardiomyocytes. Nature 2013; 493: 433-436.
17. Mollova M, Bersell K, Walsh S, et al. Cardiomyocyte proliferation contributes to heart growth in young humans. Proc Natl Acad Sci USA 2013; 110: 1446-1451.
18. Beltrami AP, Barlucchi L, Torella D, et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 2003; 114: 763-776.
19. Oh H, Bradfute SB, Gallardo TD, et al. Cardiac progenitor cells from adult myocardium: Homing, differentiation, and fusion after infarction. Proc Natl Acad Sci USA 2003; 100: 12313-12318.
20. Smith RR, Barile L, Cho HC, et al. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 2007; 115: 896-908.
21. Ellison GM, Vicinanza C, Smith AJ, et al. Adult c-kit(pos) cardiac stem cells are necessary and sufficient for functional cardiac regeneration and repair. Cell 2013; 154: 827-842.
22. Passier R, van Laake LW, Mummery CL,. Stem-cell-based therapy and lessons from the heart. Nature 2008; 453: 322-329.
23. Waldo KL, Hutson MR, Ward CC, et al. Secondary heart field contributes myocardium and smooth muscle to the arterial pole of the developing heart. Dev Biol 2005; 281: 78-90.
24. Lafontant PJ, Behzad AR, Brown E, et al. Cardiac myocyte diversity and a fibroblast network in the junctional region of the zebrafish heart revealed by transmission and serial block-face scanning electron microscopy. PLoS One 2013; 8: e72388.
25. Castaldo C, Di Meglio F, Miraglia R, et al. Cardiac fibroblast-derived extracellular matrix (biomatrix) as a model for the studies of cardiac primitive cell biological properties in normal and pathological adult human heart. BioMed Res Int 2013; 2013: 352370.
26. Ruiz-Villalba A, Ziogas A, Ehrbar M, et al. Characterization of epicardial-derived cardiac interstitial cells: Differentiation and mobilization of heart fibroblast progenitors. PLoS One 2013; 8: e53694.
27. Makkar RR, Smith RR, Cheng K, et al. Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): A prospective, randomised phase 1 trial. Lancet 2012; 379: 895-904.
28. Kim HN, Jiao A, Hwang NS, et al. Nanotopography-guided tissue engineering and regenerative medicine. Adv Drug Deliv Rev 2013; 65: 536-558.
29. Bearzi C, Rota M, Hosoda T, et al. Human cardiac stem cells. Proc Natl Acad Sci USA 2007; 104: 14068-14073.
30. Ponik SM, Trier SM, Wozniak MA, et al. RhoA is down-regulated at cell-cell contacts via p190RhoGAP-B in response to tensional homeostasis. Mol Biol Cell 2013; 24: 1688-1699, S1681-1683.
31. Zebda N, Tian Y, Tian X, et al. Interaction of p190RhoGAP with C-terminal domain of p120-catenin modulates endothelial cytoskeleton and permeability. J Biol Chem 2013; 288: 18290-18299.
32. Mammoto A, Mammoto T, Ingber DE,. Rho signaling and mechanical control of vascular development. Curr Opin Hematol 2008; 15: 228-234.
33. Nimnual AS, Taylor LJ, Bar-Sagi D,. Redox-dependent downregulation of Rho by Rac. Nat Cell Biol 2003; 5: 236-241.
34. Falconnet D, Csucs G, Grandin HM, et al. Surface engineering approaches to micropattern surfaces for cell-based assays. Biomaterials 2006; 27: 3044-3063.
35. Deutsch J, Motiagh D, Russell B, et al. Fabrication of microtextured membranes for cardiac myocyte attachment and orientation. J Biomed Mater Res 2000; 53: 267-275.
36. Agarwal A, Farouz Y, Nesmith AP, et al. Micropatterning alginate substrates for in vitro cardiovascular muscle on a chip. Adv Funct Mater 2013; 23: 3738-3746.
37. Annabi N, Tsang K, Mithieux SM, et al. Highly elastic micropatterned hydrogel for engineering functional cardiac tissue. Adv Funct Mater 2013; 23: 4950-4959.
38. Isenberg BC, Tsuda Y, Williams C, et al. A thermoresponsive, microtextured substrate for cell sheet engineering with defined structural organization. Biomaterials 2008; 29: 2565-2572.
39. Noren NK, Arthur WT, Burridge K,. Cadherin engagement inhibits RhoA via p190RhoGAP. J Biol Chem 2003; 278: 13615-13618.
40. Tomar A, Lim ST, Lim Y, et al. A FAK-p120RasGAP-p190RhoGAP complex regulates polarity in migrating cells. J Cell Sci 2009; 122: 1852-1862.
41. Wildenberg GA, Dohn MR, Carnahan RH, et al. p120-catenin and p190RhoGAP regulate cell-cell adhesion by coordinating antagonism between Rac and Rho. Cell 2006; 127: 1027-1039.
42. Su L, Agati JM, Parsons SJ,. p190RhoGAP is cell cycle regulated and affects cytokinesis. J Cell Biol 2003; 163: 571-582.
43. Troller U, Raghunath A, Larsson C,. A possible role for p190RhoGAP in PKCepsilon-induced morphological effects. Cell Signal 2004; 16: 245-252.
44. Jeon CY, Kim HJ, Morii H, et al. Neurite outgrowth from PC12 cells by basic fibroblast growth factor (bFGF) is mediated by RhoA inactivation through p190RhoGAP and ARAP3. J Cell Physiol 2010; 224: 786-794.
45. Molina-Ortiz I, Bartolome RA, Hernandez-Varas P, et al. Overexpression of E-cadherin on melanoma cells inhibits chemokine-promoted invasion involving p190RhoGAP/p120ctn-dependent inactivation of RhoA. J Biol Chem 2009; 284: 15147-15157.
46. Siddiqui MR, Komarova YA, Vogel SM, et al. Caveolin-1-eNOS signaling promotes p190RhoGAP-A nitration and endothelial permeability. J Cell Biol 2011; 193: 841-850.
47. Sharma SV,. Rapid recruitment of p120RasGAP and its associated protein, p190RhoGAP, to the cytoskeleton during integrin mediated cell-substrate interaction. Oncogene 1998; 17: 271-281.
48. Settleman J, Narasimhan V, Foster LC, et al. Molecular cloning of cDNAs encoding the GAP-associated protein p190: Implications for a signaling pathway from ras to the nucleus. Cell 1992; 69: 539-549.
49. Burbelo PD, Miyamoto S, Utani A, et al. p190-B, a new member of the Rho GAP family, and Rho are induced to cluster after integrin cross-linking. J Biol Chem 1995; 270: 30919-30926.
50. Sordella R, Jiang W, Chen GC, et al. Modulation of Rho GTPase signaling regulates a switch between adipogenesis and myogenesis. Cell 2003; 113: 147-158.
51. Sordella R, Classon M, Hu KQ, et al. Modulation of CREB activity by the Rho GTPase regulates cell and organism size during mouse embryonic development. Dev Cell 2002; 2: 553-565.
52. Chakravarty G, Hadsell D, Buitrago W, et al. p190-B RhoGAP regulates mammary ductal morphogenesis. Mol Endocrinol 2003; 17: 1054-1065.
53. Brouns MR, Matheson SF, Hu KQ, et al. The adhesion signaling molecule p190 RhoGAP is required for morphogenetic processes in neural development. Development 2000; 127: 4891-4903.
54. Wolf RM, Draghi N, Liang X, et al. p190RhoGAP can act to inhibit PDGF-induced gliomas in mice: A putative tumor suppressor encoded on human chromosome 19q13.3. Genes Dev 2003; 17: 476-487.
55. Ludwig K, Parsons SJ,. The tumor suppressor, p190RhoGAP, differentially initiates apoptosis and confers docetaxel sensitivity to breast cancer cells. Genes Cancer 2011; 2: 20-30.
56. Grinnell KL, Harrington EO,. Interplay between FAK, PKCdelta, and p190RhoGAP in the regulation of endothelial barrier function. Microvasc Res 2012; 83: 12-21.
57. Chava KR, Tauseef M, Sharma T, et al. Cyclic AMP response element-binding protein prevents endothelial permeability increase through transcriptional controlling p190RhoGAP expression. Blood 2012; 119: 308-319.
58. Park HJ, Ward SM, Desgrosellier JS, et al. Transforming growth factor beta regulates the expression of the M2 muscarinic receptor in atrial myocytes via an effect on RhoA and p190RhoGAP. J Biol Chem 2006; 281: 19995-20002.
59. Todorovic B, Nichols AC, Chitilian JM, et al. The human papillomavirus E7 proteins associate with and alter p190RhoGAP function. J Virol 2014; 88: 3653-3663.
60. Arthur WT, Burridge K,. RhoA inactivation by p190RhoGAP regulates cell spreading and migration by promoting membrane protrusion and polarity. Mol Biol Cell 2001; 12: 2711-2720.
61. Brouns MR, Matheson SF, Settleman J,. p190 RhoGAP is the principal Src substrate in brain and regulates axon outgrowth, guidance and fasciculation. Nat Cell Biol 2001; 3: 361-367.
62. Brandt D, Gimona M, Hillmann M, et al. Protein kinase C induces actin reorganization via a Src- and Rho-dependent pathway. J Biol Chem 2002; 277: 20903-20910.
63. Levay M, Bartos B, Ligeti E,. p190RhoGAP has cellular RacGAP activity regulated by a polybasic region. Cell Signal 2013; 25: 1388-1394.
64. Bustos RI, Forget MA, Settleman JE, et al. Coordination of Rho and Rac GTPase function via p190B RhoGAP. Curr Biol 2008; 18: 1606-1611.
65. Bradley WD, Hernandez SE, Settleman J, et al. Integrin signaling through Arg activates p190RhoGAP by promoting its binding to p120RasGAP and recruitment to the membrane. Mol Biol Cell 2006; 17: 4827-4836.
66. Schober M, Raghavan S, Nikolova M, et al. Focal adhesion kinase modulates tension signaling to control actin and focal adhesion dynamics. J Cell Biol 2007; 176: 667-680.
67. Wennerberg K, Forget MA, Ellerbroek SM, et al. Rnd proteins function as RhoA antagonists by activating p190 RhoGAP. Curr Biol 2003; 13: 1106-1115.
68. Oinuma I, Kawada K, Tsukagoshi K, et al. Rnd1 and Rnd3 targeting to lipid raft is required for p190 RhoGAP activation. Mol Biol Cell 2012; 23: 1593-1604.
69. Barberis D, Casazza A, Sordella R, et al. p190 Rho-GTPase activating protein associates with plexins and it is required for semaphorin signalling. J Cell Sci 2005; 118: 4689-4700.
70. Asnaghi L, Vass WC, Quadri R, et al. E-cadherin negatively regulates neoplastic growth in non-small cell lung cancer: Role of Rho GTPases. Oncogene 2010; 29: 2760-2771.
71. Ratheesh A, Gomez GA, Priya R, et al. Central spindlin and alpha-catenin regulate Rho signalling at the epithelial zonula adherens. Nat Cell Biol 2012; 14: 818-828.
72. Birukova AA, Zebda N, Cokic I, et al. p190RhoGAP mediates protective effects of oxidized phospholipids in the models of ventilator-induced lung injury. Exp Cell Res 2011; 317: 859-872.
73. Kshitiz, Park J, Kim P, et al. Control of stem cell fate and function by engineering physical microenvironments. Integr Biol 2012; 4: 1008-1018.
74. Gupta K, Kim DH, Ellison D, et al. Using lab-on-a-chip technologies for stem cell biology. In:, Appasani K, Appasani RK, eds. Stem Cell Biology and Regenerative Medicine. Humana Press, Springer, 2011: 483-498.
75. Stergachis AB, Neph S, Reynolds A, et al. Developmental fate and cellular maturity encoded in human regulatory DNA landscapes. Cell 2013; 154: 888-903.
76. Weyers JJ, Schwartz SM, Minami E, et al. Effects of cell grafting on coronary remodeling after myocardial infarction. J Am Heart Assoc 2013; 2.
77. Takashima S, Tempel D, Duckers HJ,. Current outlook of cardiac stem cell therapy towards a clinical application. Heart 2013; 99: 1772-1784.
78. Wright S, Lakin R, Esfandiari S,. Getting at the heart of the issue: Advanced imaging and stem cell-based therapy offer a novel approach to cardiac resynchronization. J Physiol-London 2013; 591: 5271-5272.
79. Kishore R, Verma SK, Mackie AR, et al. Bone marrow progenitor cell therapy-mediated paracrine regulation of cardiac miRNA-155 modulates fibrotic response in diabetic hearts. PLoS One 2013; 8.
80. Lundy SD, Zhu WZ, Regnier M, et al. Structural and functional maturation of cardiomyocytes derived from human pluripotent stem cells. Stem Cells Dev 2013; 22: 1991-2002.
81. Andersen DC, Andersen P, Schneider M, et al. Murine " cardiospheres" are not a source of stem cells with cardiomyogenic potential. Stem Cells 2009; 27: 1571-1581.
82. Ahn EH, Kim YH, Kshitiz, et al. Spatial control of adult stem cell fate using nanotopographic cues. Biomaterials 2014; 35: 2401-2410.
83. Kshitiz, Kim DH, Beebe DJ, et al. Micro- and nanoengineering for stem cell biology: The promise with a caution. Trends Biotechnol 2011; 29: 399-408.