Regenerating the Cardiovascular System Through Cell Reprogramming; Current Approaches and a Look Into the Future

Frontiers in Cardiovascular Medicine

Volumn 5, Issue , 2018, Pages

  Tsifaki, Marianna ^a   Kelaini, Sophia ^a   Caines, Rachel ^a   Yang, Chunbo ^a   Margariti, Andriana ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

cardiovascular system; induced pluripotent stem cells (iPS Cells); regeneration; reprogramming; vascular cells

Indexed keywords

CARDIAC MUSCLE CELL; CARDIOVASCULAR FUNCTION; CARDIOVASCULAR MORTALITY; CARDIOVASCULAR REGENERATION; CELL THERAPY; CELL TRANSDIFFERENTIATION; ENDOTHELIUM CELL; HUMAN; INDUCED PLURIPOTENT STEM CELL; NUCLEAR REPROGRAMMING; PERICYTE; REGENERATION; REVIEW; SMOOTH MUSCLE CELL;

EID: 85060591238     PISSN: None     EISSN: 2297055X     Source Type: Journal    
DOI: 10.3389/fcvm.2018.00109     Document Type: Review

References (138)

1. Mandai M, Watanabe A, Kurimoto Y, Hirami Y, Morinaga C, Daimon T, et al. Autologous induced stem-cell–derived retinal cells for macular degeneration. N Engl J Med. (2017) 376:1038–46. 10.1056/NEJMoa160836828296613
2. Yang C, Al-Aama J, Stojkovic M, Keavney B, Trafford A, Lako M, et al. Concise review: cardiac disease modeling using induced pluripotent stem cells. Stem Cells (2015) 33:2643–51. 10.1002/stem.207026033645
3. Dell'Era P, Benzoni P, Crescini E, Valle M, Xia E, Consiglio A, et al. Cardiac disease modeling using induced pluripotent stem cell-derived human cardiomyocytes. World J Stem Cells (2015) 7:329–42. 10.4252/wjsc.v7.i2.32925815118
4. Tanaka A, Yuasa S, Node K, Fukuda K. Cardiovascular disease modeling using patient-specific induced pluripotent stem cells. Int J Mol Sci. (2015) 16:18894–922. 10.3390/ijms16081889426274955
5. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature (1981) 292:154–6. 7242681
6. Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA. (1981) 78:7634–8. 6950406
7. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, et al. Embryonic stem cell lines derived from human blastocysts. Science (1998) 282:1145–7. 9804556
8. Davis RL, Weintraub H, Lassar AB. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell (1987) 51:987–1000. 3690668
9. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell (2006) 126:663–76. 10.1016/j.cell.2006.07.02416904174
10. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell (2007) 131:861–72. 10.1016/j.cell.2007.11.01918035408
11. Marson A, Foreman R, Chevalier B, Bilodeau S, Kahn M, Young RA, et al. Wnt signaling promotes reprogramming of somatic cells to pluripotency. Cell Stem Cell (2008) 3:132–5. 10.1016/j.stem.2008.06.01918682236
12. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science (2007) 318:1917–20. 10.1126/science.115152618029452
13. Zhou W, Freed CR. Adenoviral gene delivery can reprogram human fibroblasts to induced pluripotent stem cells. Stem Cells (2009) 27:2667–74. 10.1002/stem.20119697349
14. Fusaki N, Ban H, Nishiyama A, Saeki K, Hasegawa M. Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Proc Jpn Acad Ser B Phys Biol Sci. (2009) 85:348–62. 10.2183/pjab.85.348
15. Soldner F, Hockemeyer D, Beard C, Gao Q, Bell GW, Cook EG, et al. Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell (2009) 136:964–77. 10.1016/j.cell.2009.02.01319269371
16. Woltjen K, Michael IP, Mohseni P, Desai R, Mileikovsky M, Hämäläinen R, et al. piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature (2009) 458:766–70.10.1038/nature0786319252478
17. Kaji K, Norrby K, Paca A, Mileikovsky M, Mohseni P, Woltjen K. Virus-free induction of pluripotency and subsequent excision of reprogramming factors. Nature (2009) 458:771–5. 10.1038/nature0786419252477
18. Warren L, Manos PD, Ahfeldt T, Loh Y-H, Li H, Lau F, et al. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell (2010) 7:618–30. 10.1016/j.stem.2010.08.01220888316
19. Anokye-Danso F, Trivedi CM, Juhr D, Gupta M, Cui Z, Tian Y, et al. Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell (2011) 8:376–88. 10.1016/j.stem.2011.03.00121474102
20. Subramanyam D, Lamouille S, Judson RL, Liu JY, Bucay N, Derynck R, et al. Multiple targets of miR-302 and miR-372 promote reprogramming of human fibroblasts to induced pluripotent stem cells. Nat Biotechnol. (2011) 29:443–8. 10.1038/nbt.186221490602
21. Poleganov MA, Eminli S, Beissert T, Herz S, Moon J-I, Goldmann J, et al. Efficient reprogramming of human fibroblasts and blood-derived endothelial progenitor cells using nonmodified RNA for reprogramming and immune evasion. Hum Gene Ther. (2015) 26:751–66. 10.1089/hum.2015.04526381596
22. Kim D, Kim C-H, Moon J-I, Chung Y-G, Chang M-Y, Han B-S, et al. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell (2009) 4:472–6. 10.1016/j.stem.2009.05.00519481515
23. Malik N, Rao MS. A review of the methods for human iPSC derivation. Methods Mol Biol. (2013) 339:823–6. 10.1007/978-1-62703-348-0_323546745
24. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, et al. RNA-guided human genome engineering via Cas9. Science (2013) 339:823–6. 10.1126/science.123203323287722
25. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, et al. Multiplex genome engineering using CRISPR/Cas systems. Science (2013) 339:819–23. 10.1126/science.123114323287718
26. Smith C, Gore A, Yan W, Abalde-Atristain L, Li Z, He C, et al. Whole-genome sequencing analysis reveals high specificity of CRISPR/Cas9 and TALEN-based genome editing in human iPSCs. Cell Stem Cell (2014) 15:12–3.10.1016/j.stem.2014.06.01124996165
27. Hockemeyer D, Jaenisch R. Induced pluripotent stem cells meet genome editing. Cell Stem Cell (2016) 18:573–86.10.1016/j.stem.2016.04.013627152442
28. Howden SE, Maufort JP, Duffin BM, Elefanty AG, Stanley EG, Thomson JA. Simultaneous reprogramming and gene correction of patient fibroblasts. Stem Cell Rep. (2015) 5:1109–18. 10.1016/j.stemcr.2015.10.00926584543
29. Rouhani F, Kumasaka N, de Brito MC, Bradley A, Vallier L, Gaffney D. Genetic background drives transcriptional variation in human induced pluripotent stem cells. PLoS Genet. (2014) 10:e1004432. 10.1371/journal.pgen.100443224901476
30. Kyttälä A, Moraghebi R, Valensisi C, Kettunen J, Andrus C, Pasumarthy KK, et al. Genetic variability overrides the impact of parental cell type and determines iPSC differentiation potential. Stem Cell Rep. (2016) 6:200–12. 10.1016/j.stemcr.2015.12.00926777058
31. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell (2005) 122:947–56. 10.1016/j.cell.2005.08.02016153702
32. Loh Y-H, Wu Q, Chew J-L, Vega VB, Zhang W, Chen X, et al. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet. (2006) 38:431–40.10.1038/ng176016518401
33. Zhou X, Meng G, Nardini C, Mei H. Systemic evaluation of cellular reprogramming processes exploiting a novel R-tool: eegc. Bioinformatics (2017) 33:2532–8. 10.1093/bioinformatics/btx20528398503
34. Lin T, Ambasudhan R, Yuan X, Li W, Hilcove S, Abujarour R, et al. A chemical platform for improved induction of human iPSCs. Nat Methods (2009) 6:805–8. 10.1038/nmeth.139319838168
35. Huangfu D, Osafune K, Maehr R, Guo W, Eijkelenboom A, Chen S, et al. Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat Biotechnol. (2008) 26:1269–75. 10.1038/nbt.150218849973
36. Yoshida Y, Takahashi K, Okita K, Ichisaka T, Yamanaka S. Hypoxia enhances the generation of induced pluripotent stem cells. Cell Stem Cell (2009) 5:237–41. 10.1016/j.stem.2009.08.00119716359
37. Noggle S, Fung H-L, Gore A, Martinez H, Satriani KC, Prosser R, et al. Human oocytes reprogram somatic cells to a pluripotent state. Nature (2011) 478:70–5. 10.1038/nature1039721979046
38. Zhu S, Li W, Zhou H, Wei W, Ambasudhan R, Lin T, et al. Reprogramming of human primary somatic cells by OCT4 and chemical compounds. Cell Stem Cell (2010) 7:651–5.10.1016/j.stem.2010.11.01521112560
39. Ichida JK, Blanchard J, Lam K, Son EY, Chung JE, Egli D, et al. A small-molecule inhibitor of Tgf-β signaling replaces Sox2 in reprogramming by inducing Nanog. Cell Stem Cell (2009) 5:491–503. 10.1016/j.stem.2009.09.01219818703
40. Esteban MA, Wang T, Qin B, Yang J, Qin D, Cai J, et al. Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell (2010) 6:71–9. 10.1016/j.stem.2009.12.00120036631
41. Quaini F, Urbanek K, Graiani G, Lagrasta C, Maestri R, Monica M, et al. The regenerative potential of the human heart. Int J Cardiol. (2004) 95(Suppl. 1):S26–8. 10.1016/S0167-5273(04)90008-315336841
42. Hsieh PCH, Segers VFM, Davis ME, MacGillivray C, Gannon J, Molkentin JD, et al. Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nat Med. (2007) 13:970–4. 10.1038/nm161817660827
43. Toyoda Y, Guy TS, Kashem A. Present status and future perspectives of heart transplantation. Circ J. (2013) 77:1097–110. 10.1253/circj.CJ-13-029623614963
44. Chong JJH, Yang X, Don CW, Minami E, Liu Y-W, Weyers JJ, et al. Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature (2014) 510:273–7. 10.1038/nature1323324776797
45. Shiba Y, Fernandes S, Zhu W-Z, Filice D, Muskheli V, Kim J, et al. Human ES-cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts. Nature (2012) 489:322–5. 10.1038/nature1131722864415
46. Senyo SE, Steinhauser ML, Pizzimenti CL, Yang VK, Cai L, Wang M, et al. Mammalian heart renewal by pre-existing cardiomyocytes. Nature (2012) 493:433–6. 10.1038/nature1168223222518
47. Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S, et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell (2003) 114:763–76. 10.1016/S0092-8674(03)00687-114505575
48. Chiu LLY, Iyer RK, Reis LA, Nunes SS, Radisic M. Cardiac tissue engineering: current state and perspectives. Front Biosci. (2012) 17:1533–50. 10.2741/400222201819
49. Jafarkhani M, Salehi Z, Kowsari-Esfahan R, Shokrgozar MA, Rezaa Mohammadi M, Rajadas J, et al. Strategies for directing cells into building functional hearts and parts. Biomater Sci. (2018) 6:1664–90. 10.1039/c7bm01176h29767196
50. Doetschman TC, Eistetter H, Katz M, Schmidt W, Kemler R. The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol. (1985) 87:27–45. 3897439
51. Mauritz C, Schwanke K, Reppel M, Neef S, Katsirntaki K, Maier LS, et al. Generation of functional murine cardiac myocytes from induced pluripotent stem cells. Circulation (2008) 118:507–17. 10.1161/CIRCULATIONAHA.108.77879518625890
52. Schenke-Layland K, Rhodes KE, Angelis E, Butylkova Y, Heydarkhan-Hagvall S, Gekas C, et al. Reprogrammed mouse fibroblasts differentiate into cells of the cardiovascular and hematopoietic lineages. Stem Cells (2008) 26:1537–46. 10.1634/stemcells.2008-003318450826
53. Narazaki G, Uosaki H, Teranishi M, Okita K, Kim B, Matsuoka S, et al. Directed and systematic differentiation of cardiovascular cells from mouse induced pluripotent stem cells. Circulation (2008) 118:498–506. 10.1161/CIRCULATIONAHA.108.76956218625891
54. Zhang J, Wilson GF, Soerens AG, Koonce CH, Yu J, Palecek SP, et al. Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res. (2009) 104:e30–41. 10.1161/CIRCRESAHA.108.19223719213953
55. Yoshida Y, Yamanaka S. Induced pluripotent stem cells 10 years later: for cardiac applications. Circ Res. (2017) 120:1958–68. 10.1161/CIRCRESAHA.117.31108028596174
56. Kumar M, Kasala ER, Bodduluru LN, Dahiya V, Sharma D, Kumar V, et al. Animal models of myocardial infarction: mainstay in clinical translation. Regul Toxicol Pharmacol. (2016) 76:221–30. 10.1016/j.yrtph.2016.03.00526988997
57. Kawamura M, Miyagawa S, Fukushima S, Saito A, Miki K, Ito E, et al. Enhanced survival of transplanted human induced pluripotent stem cell-derived cardiomyocytes by the combination of cell sheets with the pedicled omental flap technique in a porcine heart. Circulation (2013) 128(11 Suppl. 1):S87–94. 10.1161/CIRCULATIONAHA.112.00036624030425
58. Menasché P, Vanneaux V, Fabreguettes J-R, Bel A, Tosca L, Garcia S, et al. Towards a clinical use of human embryonic stem cell-derived cardiac progenitors: a translational experience. Eur Heart J. (2015) 36:743–50. 10.1093/eurheartj/ehu19224835485
59. Menasché P, Vanneaux V, Hagège A, Bel A, Cholley B, Cacciapuoti I, et al. Human embryonic stem cell-derived cardiac progenitors for severe heart failure treatment: first clinical case report: Figure 1. Eur Heart J. (2015) 36:2011–7. 10.1093/eurheartj/ehv18925990469
60. Takeuchi JK, Bruneau BG. Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature (2009) 459:708–11. 10.1038/nature0803919396158
61. Ieda M, Fu J-D, Delgado-Olguin P, Vedantham V, Hayashi Y, Bruneau BG, et al. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell (2010) 142:375–86. 10.1016/j.cell.2010.07.00220691899
62. Qian L, Huang Y, Spencer CI, Foley A, Vedantham V, Liu L, et al. In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature (2012) 485:593–8.10.1038/nature1104422522929
63. Song K, Nam Y-J, Luo X, Qi X, Tan W, Huang GN, et al. Heart repair by reprogramming non-myocytes with cardiac transcription factors. Nature (2012) 485:599–604. 10.1038/nature1113922660318
64. Inagawa K, Miyamoto K, Yamakawa H, Muraoka N, Sadahiro T, Umei T, et al. Induction of cardiomyocyte-like cells in infarct hearts by gene transfer of Gata4, Mef2c, and Tbx5. Circ Res. (2012) 111:1147–56. 10.1161/CIRCRESAHA.112.27114822931955
65. Wang L, Liu Z, Yin C, Asfour H, Chen O, Li Y, et al. Stoichiometry of Gata4, Mef2c, and Tbx5 influences the efficiency and quality of induced cardiac myocyte reprogramming. Circ Res. (2015) 116:237–44. 10.1161/CIRCRESAHA.116.30554725416133
66. Hirai H, Katoku-Kikyo N, Keirstead SA, Kikyo N. Accelerated direct reprogramming of fibroblasts into cardiomyocyte-like cells with the MyoD transactivation domain. Cardiovasc Res. (2013) 100:105–13. 10.1093/cvr/cvt16723794713
67. Cao N, Huang Y, Zheng J, Spencer CI, Zhang Y, Fu J-D, et al. Conversion of human fibroblasts into functional cardiomyocytes by small molecules. Science (2016) 352:1216–20. 10.1126/science.aaf150227127239
68. Fu J-D, Stone NR, Liu L, Spencer CI, Qian L, Hayashi Y, et al. Direct reprogramming of human fibroblasts toward a cardiomyocyte-like state. Stem Cell Rep. (2013) 1:235–47. 10.1016/j.stemcr.2013.07.00524319660
69. Christoforou N, Chellappan M, Adler AF, Kirkton RD, Wu T, Addis RC, et al. Transcription factors MYOCD, SRF, Mesp1 and SMARCD3 enhance the cardio-inducing effect of GATA4, TBX5, and MEF2C during direct cellular reprogramming. PLoS ONE (2013)8:e63577. 10.1371/journal.pone.006357723704920
70. Nam Y-J, Song K, Luo X, Daniel E, Lambeth K, West K, et al. Reprogramming of human fibroblasts toward a cardiac fate. Proc Natl Acad Sci USA. (2013) 110:5588–93. 10.1073/pnas.130101911023487791
71. Islas JF, Liu Y, Weng K-C, Robertson MJ, Zhang S, Prejusa A, et al. Transcription factors ETS2 and MESP1 transdifferentiate human dermal fibroblasts into cardiac progenitors. Proc Natl Acad Sci USA. (2012) 109:13016–21. 10.1073/pnas.112029910922826236
72. Wang H, Cao N, Spencer CI, Nie B, Ma T, Xu T, et al. Small molecules enable cardiac reprogramming of mouse fibroblasts with a single factor. Cell Rep. (2014) 6:951–60. 10.1016/j.celrep.2014.01.03824561253
73. Muraoka N, Yamakawa H, Miyamoto K, Sadahiro T, Umei T, Isomi M, et al. MiR-133 promotes cardiac reprogramming by directly repressing Snai1 and silencing fibroblast signatures. EMBO J. (2014) 33:1565–81. 10.15252/embj.20138760524920580
74. Jayawardena TM, Egemnazarov B, Finch EA, Zhang L, Payne JA, Pandya K, et al. MicroRNA-mediated in vitro and in vivo direct reprogramming of cardiac fibroblasts to cardiomyocytes. Circ Res. (2012) 110:1465–73. 10.1161/CIRCRESAHA.112.26903522539765
75. Huang C, Tu W, Fu Y, Wang J, Xie X. Chemical-induced cardiac reprogramming in vivo. Cell Res. (2018) 28:686–9.10.1038/s41422-018-0036-429670223
76. Tousoulis D, Simopoulou C, Papageorgiou N, Oikonomou E, Hatzis G, Siasos G, et al. Endothelial dysfunction in conduit arteries and in microcirculation. novel therapeutic approaches. Pharmacol Ther. (2014) 144:253–67. 10.1016/j.pharmthera.2014.06.00324928320
77. Carmeliet P. Angiogenesis in life, disease and medicine. Nature (2005) 438:932–6.10.1038/nature0447816355210
78. Yoder MC. Differentiation of pluripotent stem cells into endothelial cells. Curr Opin Hematol. (2015) 22:252–7. 10.1097/MOH.000000000000014025767955
79. Wilson HK, Canfield SG, Shusta EV, Palecek SP. Concise review: tissue-specific microvascular endothelial cells derived from human pluripotent stem cells. Stem Cells (2014) 32:3037–45. 10.1002/stem.179725070152
80. Medina RJ, O'Neill CL, Humphreys MW, Gardiner TA, Stitt AW. Outgrowth endothelial cells: characterization and their potential for reversing ischemic retinopathy. Investig Opthalmol. Vis Sci. (2010) 51:5906. 10.1167/iovs.09-495120554606
81. Moubarik C, Guillet B, Youssef B, Codaccioni J-L, Piercecchi M-D, Sabatier F, et al. Transplanted late outgrowth endothelial progenitor cells as cell therapy product for stroke. Stem Cell Rev Rep. (2011) 7:208–20. 10.1007/s12015-010-9157-y20526754
82. Prasain N, Lee MR, Vemula S, Meador JL, Yoshimoto M, Ferkowicz MJ, et al. Differentiation of human pluripotent stem cells to cells similar to cord-blood endothelial colony–forming cells. Nat Biotechnol. (2014) 32:1151–7. 10.1038/nbt.304825306246
83. Turner RR, Beckstead JH, Warnke RA, Wood GS. Endothelial cell phenotypic diversity: in situ demonstration of immunologic and enzymatic heterogeneity that correlates with specific morphologic subtypes. Am J Clin Pathol. (1987) 87:569–75. 3554972
84. Marcelo KL, Goldie LC, Hirschi KK. Regulation of endothelial cell differentiation and specification. Circ Res. (2013) 112:1272–87. 10.1161/CIRCRESAHA.113.30050623620236
85. Adams WJ, Zhang Y, Cloutier J, Kuchimanchi P, Newton G, Sehrawat S, et al. Functional vascular endothelium derived from human induced pluripotent stem cells. Stem Cell Rep. (2013) 1:105–13. 10.1016/j.stemcr.2013.06.00724052946
86. Orlova V V, van den Hil FE, Petrus-Reurer S, Drabsch Y, ten Dijke P, Mummery CL. Generation, expansion and functional analysis of endothelial cells and pericytes derived from human pluripotent stem cells. Nat Protoc. (2014) 9:1514–31. 10.1038/nprot.2014.10224874816
87. Patsch C, Challet-Meylan L, Thoma EC, Urich E, Heckel T, O'Sullivan JF, et al. Generation of vascular endothelial and smooth muscle cells from human pluripotent stem cells. Nat Cell Biol. (2015) 17:994–1003. 10.1038/ncb320526214132
88. Harding A, Cortez-Toledo E, Magner NL, Beegle JR, Coleal-Bergum DP, Hao D, et al. Highly efficient differentiation of endothelial cells from pluripotent stem cells requires the MAPK and the PI3K pathways. Stem Cells (2017) 35:909–19. 10.1002/stem.257728248004
89. Margariti A, Winkler B, Karamariti E, Zampetaki A, Tsai T, Baban D, et al. Direct reprogramming of fibroblasts into endothelial cells capable of angiogenesis and reendothelialization in tissue-engineered vessels. Proc Natl Acad Sci USA. (2012) 109:13793–8.10.1073/pnas.120552610922869753
90. Li J, Huang NF, Zou J, Laurent TJ, Lee JC, Okogbaa J, et al. Conversion of human fibroblasts to functional endothelial cells by defined factors. Arterioscler Thromb Vasc Biol. (2013) 33:1366–75. 10.1161/ATVBAHA.112.30116723520160
91. Wong WT, Huang NF, Botham CM, Sayed N, Cooke JP. Endothelial cells derived from nuclear reprogramming. Circ Res. (2012) 111:1363–75. 10.1161/CIRCRESAHA.111.24721323104878
92. Kane NM, Howard L, Descamps B, Meloni M, McClure J, Lu R, et al. Role of microRNAs 99b, 181a, and 181b in the differentiation of human embryonic stem cells to vascular endothelial cells. Stem Cells (2012) 30:643–54. 10.1002/stem.102622232059
93. Chen T, Margariti A, Kelaini S, Cochrane A, Guha ST, Hu Y, et al. MicroRNA-199b modulates vascular cell fate during iPS cell differentiation by targeting the notch ligand Jagged1 and enhancing VEGF signaling. Stem Cells (2015) 33:1405–18. 10.1002/stem.193025535084
94. Di Bernardini E, Campagnolo P, Margariti A, Zampetaki A, Karamariti E, Hu Y, et al. Endothelial lineage differentiation from induced pluripotent stem cells is regulated by microRNA-21 and transforming growth factor β2 (TGF-β2) pathways. J Biol Chem. (2014) 289:3383–93. 10.1074/jbc.M113.49553124356956
95. Ginsberg M, Schachterle W, Shido K, Rafii S. Direct conversion of human amniotic cells into endothelial cells without transitioning through a pluripotent state. Nat Protoc. (2015) 10:1975–85. 10.1038/nprot.2015.12626540589
96. Yeh ETH, Zhang S, Wu HD, Körbling M, Willerson JT, Estrov Z. Transdifferentiation of human peripheral blood CD34+-enriched cell population into cardiomyocytes, endothelial cells, and smooth muscle cells in vivo. Circulation (2003) 108:2070–3.10.1161/01.CIR.0000099501.52718.7014568894
97. Hong X, Margariti A, Le Bras A, Jacquet L, Kong W, Hu Y, et al. Transdifferentiated human vascular smooth muscle cells are a new potential cell source for endothelial regeneration. Sci Rep. (2017) 7:5590.10.1038/s41598-017-05665-728717251
98. Bohnsack BL, Lai L, Northrop JL, Justice MJ, Hirschi KK. Visceral endoderm function is regulated byquaking and required for vascular development. Genesis (2006) 44:93–104.10.1002/gene.2018916470614
99. de Bruin RG, van der Veer EP, Prins J, Lee DH, Dane MJC, Zhang H, et al. The RNA-binding protein quaking maintains endothelial barrier function and affects VE-cadherin and β-catenin protein expression. Sci Rep. (2016) 6:21643. 10.1038/srep2164326905650
100. Cochrane A, Kelaini S, Tsifaki M, Bojdo J, Vilà-González M, Drehmer D, et al. Quaking is a key regulator of endothelial cell differentiation, neovascularization, and angiogenesis. Stem Cells (2017) 35:952–66. 10.1002/stem.259428207177
101. Tanaka T, Izawa K, Maniwa Y, Okamura M, Okada A, Yamaguchi T, et al. ETV2-TET1/TET2 complexes induce endothelial cell-specific Robo4 expression via promoter demethylation. Sci Rep. (2018) 8:5653. 10.1038/s41598-018-23937-829618782
102. Morita R, Suzuki M, Kasahara H, Shimizu N, Shichita T, Sekiya T, et al. ETS transcription factor ETV2 directly converts human fibroblasts into functional endothelial cells. Proc Natl Acad Sci USA. (2015) 112:160–5.10.1073/pnas.141323411225540418
103. Oh S-Y, Kim JY, Park C. The ETS Factor, ETV2: a master regulator for vascular endothelial cell development. Mol Cells (2015) 38:1029–36. 10.14348/molcells.2015.033126694034
104. Van Pham P, Vu NB, Nguyen HT, Huynh OT, Truong MT-H. Significant improvement of direct reprogramming efficacy of fibroblasts into progenitor endothelial cells by ETV2 and hypoxia. Stem Cell Res Ther. (2016) 7:104. 10.1186/s13287-016-0368-227488544
105. Takeda Y, Harada Y, Yoshikawa T, Dai P. Chemical compound-based direct reprogramming for future clinical applications. Biosci Rep. (2018) 38:BSR20171650. 10.1042/BSR2017165029739872
106. Paik DT, Tian L, Lee J, Sayed N, Chen IY, Rhee S, et al. Large-scale single-cell RNA-seq reveals molecular signatures of heterogeneous populations of human induced pluripotent stem cell-derived endothelial cells. Circ Res. (2018) 123:443–50. 10.1161/CIRCRESAHA.118.31291329986945
107. Ross R, Glomset JA. Atherosclerosis and the arterial smooth muscle cell: proliferation of smooth muscle is a key event in the genesis of the lesions of atherosclerosis. Science (1973) 180:1332–9. 4350926
108. Ross R, Glomset JA. The pathogenesis of atherosclerosis. N Engl J Med. (1976) 295:369–77.
109. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, et al. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med. (2002) 8:403–9.10.1038/nm0402-40311927948
110. Daniel J-M, Sedding DG. Circulating smooth muscle progenitor cells in arterial remodeling. J Mol Cell Cardiol. (2011) 50:273–9. 10.1016/j.yjmcc.2010.10.03021047514
111. Han C, Campbell GR, Campbell JH. Circulating bone marrow cells can contribute to neointimal formation. J Vasc Res. (2001) 38:113–9.10.1159/00005103811316947
112. Hillebrands JL, Klatter FA, van den Hurk BM, Popa ER, Nieuwenhuis P, Rozing J. Origin of neointimal endothelium and alpha-actin-positive smooth muscle cells in transplant arteriosclerosis. J Clin Invest. (2001) 107:1411–22. 10.1172/JCI1023311390423
113. Wang G, Jacquet L, Karamariti E, Xu Q. Origin and differentiation of vascular smooth muscle cells. J Physiol. (2015) 593:3013–30. 10.1113/JP27003325952975
114. Margariti A, Zeng L, Xu Q. Stem cells, vascular smooth muscle cells and atherosclerosis. Histol Histopathol. (2006) 21:979–85. 10.14670/HH-21.97916763948
115. Haller H, Bychkov R, Erdmann B, Lindschau C, Haase H, Morano I, et al. From totipotent embryonic stem cells to spontaneously contracting smooth muscle cells: a retinoic acid and db-cAMP in vitro differentiation model. FASEB J. (1997) 11:905–15. 9285489
116. Huang H, Zhao X, Chen L, Xu C, Yao X, Lu Y, et al. Differentiation of human embryonic stem cells into smooth muscle cells in adherent monolayer culture. Biochem Biophys Res Commun. (2006) 351:321–7.10.1016/j.bbrc.2006.09.17117069765
117. Zhang P, Li J, Tan Z, Wang C, Liu T, Chen L, et al. Short-term BMP-4 treatment initiates mesoderm induction in human embryonic stem cells. Blood (2008) 111:1933–41.10.1182/blood-2007-02-07412018042803
118. Sinha S, Hoofnagle MH, Kingston PA, McCanna ME, Owens GK. Transforming growth factor-β1 signaling contributes to development of smooth muscle cells from embryonic stem cells. Am J Physiol Physiol. (2004) 287:C1560–8.10.1152/ajpcell.00221.200415306544
119. Kurpinski K, Lam H, Chu J, Wang A, Kim A, Tsay E, et al. Transforming growth factor-β and notch signaling mediate stem cell differentiation into smooth muscle cells. Stem Cells (2010) 28:734–42. 10.1002/stem.31920146266
120. Yan Z-Q, Yao Q-P, Zhang M-L, Qi Y-X, Guo Z-Y, Shen B-R, et al. Histone deacetylases modulate vascular smooth muscle cell migration induced by cyclic mechanical strain. J Biomech. (2009) 42:945–8. 10.1016/j.jbiomech.2009.01.01219261284
121. Zhou B, Margariti A, Zeng L, Xu Q. Role of histone deacetylases in vascular cell homeostasis and arteriosclerosis. Cardiovasc Res. (2011) 90:413–20. 10.1093/cvr/cvr00321233251
122. Xu SS, Alam S, Margariti A. Epigenetics in vascular disease - therapeutic potential of new agents. Curr Vasc Pharmacol. (2014) 12:77–86. 22724461
123. Xie C-Q, Zhang J, Villacorta L, Cui T, Huang H, Chen YE. A highly efficient method to differentiate smooth muscle cells from human embryonic stem cells. Arterioscler Thromb Vasc Biol. (2007) 27:e311–2.10.1161/ATVBAHA.107.15426018029907
124. Ge X, Ren Y, Bartulos O, Lee MY, Yue Z, Kim K-Y, et al. Modeling supravalvular aortic stenosis syndrome with human induced pluripotent stem cells. Circulation (2012) 126:1695–704. 10.1161/CIRCULATIONAHA.112.11699622914687
125. Lin B, Kim J, Li Y, Pan H, Carvajal-Vergara X, Salama G, et al. High-purity enrichment of functional cardiovascular cells from human iPS cells. Cardiovasc Res. (2012) 95:327–35. 10.1093/cvr/cvs18522673369
126. Wanjare M, Kuo F, Gerecht S. Derivation and maturation of synthetic and contractile vascular smooth muscle cells from human pluripotent stem cells. Cardiovasc Res. (2013) 97:321–30. 10.1093/cvr/cvs31523060134
127. Steinbach SK, Husain M. Vascular smooth muscle cell differentiation from human stem/progenitor cells. Methods (2016) 101:85–92. 10.1016/j.ymeth.2015.12.00426678794
128. Yang L, Geng Z, Nickel T, Johnson C, Gao L, Dutton J, et al. Differentiation of human induced-pluripotent stem cells into smooth-muscle cells: two novel protocols. PLoS ONE (2016) 11:e0147155. 10.1371/journal.pone.014715526771193
129. Karamariti E, Margariti A, Winkler B, Wang X, Hong X, Baban D, et al. Smooth muscle cells differentiated from reprogrammed embryonic lung fibroblasts through DKK3 signaling are potent for tissue engineering of vascular grafts. Circ Res. (2013) 112:1433–43. 10.1161/CIRCRESAHA.111.30041523529184
130. Pallone TL, Silldorff EP. Pericyte regulation of renal medullary blood flow. Exp Nephrol. (2001) 9:165–70.10.1159/00005260811340300
131. Hellström M, Gerhardt H, Kalén M, Li X, Eriksson U, Wolburg H, et al. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol. (2001) 153:543–53. 10.1083/jcb.153.3.54311331305
132. Ahmed TA, El-Badri N. Pericytes: The role of multipotent stem cells in vascular maintenance and regenerative medicine. Adv Exp Med Biol. (2017) 7:452–64. 10.1007/5584_2017_13829282647
133. Bergers G, Song S. The role of pericytes in blood-vessel formation and maintenance. Neuro Oncol. (2005) 7:452–64.10.1215/S115285170500023216212810
134. Ferland-McCollough D, Slater S, Richard J, Reni C, Mangialardi G. Pericytes, an overlooked player in vascular pathobiology. Pharmacol Ther. (2017) 171:30–42. 10.1016/j.pharmthera.2016.11.00827916653
135. Dar A, Domev H, Ben-Yosef O, Tzukerman M, Zeevi-Levin N, Novak A, et al. Multipotent vasculogenic pericytes from human pluripotent stem cells promote recovery of murine ischemic limb. Circulation (2012) 125:87–99. 10.1161/CIRCULATIONAHA.111.04826422095829
136. Katare RG, Madeddu P. Pericytes from human veins for treatment of myocardial ischemia. Trends Cardiovasc Med. (2013) 23:66–70. 10.1016/j.tcm.2012.09.00223313330
137. Sadahiro T, Yamanaka S, Ieda M. Direct cardiac reprogramming: progress and challenges in basic biology and clinical applications. Circ Res. (2015) 116:1378–91. 10.1161/CIRCRESAHA.116.30537425858064
138. Costa-Almeida R, Granja PL, Soares R, Guerreiro SG. Cellular strategies to promote vascularisation in tissue engineering applications. Eur Cells Mater. (2014) 28:51–66. 10.22203/eCM.v028a0525050838