Three-Dimensional Vascular Network Assembly from Diabetic Patient-Derived Induced Pluripotent Stem Cells

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 35, Issue 12, 2015, Pages 2677-2685

  Chan, Xin Yi ^a   Black, Rebecca ^a   Dickerman, Kayla ^a   Federico, Joseph ^a   Levesque, Mathieu ^c   Mumm, Jeff ^c   Gerecht, Sharon ^a,b  

^a Institute for NanoBioTechnology   (United States)

^b Johns Hopkins University   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Diabetes mellitus; endothelial cells; hydrogels; induced pluripotent stem cells; vascular networks

Indexed keywords

ACETYL LOW DENSITY LIPOPROTEIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYALURONIC ACID; INTERCELLULAR ADHESION MOLECULE 1; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; RHO KINASE INHIBITOR; TUMOR NECROSIS FACTOR ALPHA; VASCULAR ENDOTHELIAL CADHERIN; VON WILLEBRAND FACTOR; ACETYL-LDL; CADHERIN; GREEN FLUORESCENT PROTEIN; HYDROGEL; LEUKOCYTE ANTIGEN; LOW DENSITY LIPOPROTEIN; NOS3 PROTEIN, HUMAN; TUMOR NECROSIS FACTOR;

ADHERENT CELL; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ADHESION; CELL DENSITY; CELL DIFFERENTIATION; CELL JUNCTION; CELL MATURATION; CELL SURVIVAL; COMPARATIVE STUDY; CONTROLLED STUDY; DIABETIC PATIENT; ENDOCRINE CELL; ENDOTHELIAL PROGENITOR CELL; FIBROBLAST; HUMAN; HUMAN CELL; HYDROGEL; IMMUNOFLUORESCENCE; INSULIN DEPENDENT DIABETES MELLITUS; LECTIN BINDING; MORPHOGENESIS; NERVE CELL NETWORK; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; THREE DIMENSIONAL VASCULAR NETWORK; ANIMAL; BIOSYNTHESIS; BLOOD; CASE CONTROL STUDY; CELL HYPOXIA; CELL LINE; CELL SEPARATION; CELL SHAPE; CHEMISTRY; DRUG EFFECTS; GENETICS; INDUCED PLURIPOTENT STEM CELL; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PHENOTYPE; TRANSGENIC ANIMAL; TRANSPLANTATION; XENOGRAFT; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIGENS, CD; CADHERINS; CASE-CONTROL STUDIES; CELL DIFFERENTIATION; CELL HYPOXIA; CELL LINE; CELL SEPARATION; CELL SHAPE; DIABETES MELLITUS, TYPE 1; ENDOTHELIAL PROGENITOR CELLS; GREEN FLUORESCENT PROTEINS; HETEROGRAFTS; HUMANS; HYALURONIC ACID; HYDROGELS; INDUCED PLURIPOTENT STEM CELLS; LIPOPROTEINS, LDL; NEOVASCULARIZATION, PATHOLOGIC; NITRIC OXIDE SYNTHASE TYPE III; PHENOTYPE; TUMOR NECROSIS FACTOR-ALPHA; VON WILLEBRAND FACTOR; ZEBRAFISH;

EID: 84948114253     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.115.306362     Document Type: Article

References (53)

1. Murphy SL, Xu J, Kochanek KD. Deaths: final data for 2010. Natl Vital Stat Rep. 2013;61:1-117.
2. Resnick HE, Howard BV. Diabetes and cardiovascular disease. Annu Rev Med. 2002;53:245-267. doi: 10.1146/annurev.med.53.082901.103904.
3. Wilson PW. Diabetes mellitus and coronary heart disease. Am J Kidney Dis. 1998;32(5 suppl 3):S89-S100.
4. Kota SK, Meher LK, Jammula S, Kota SK, Krishna SV, Modi KD. Aberrant angiogenesis: the gateway to diabetic complications. Indian J Endocrinol Metab. 2012;16:918-930. doi: 10.4103/2230-8210.102992.
5. Simons M. Angiogenesis, arteriogenesis, and diabetes: paradigm reassessed J Am Coll Cardiol. 2005;46:835-837. doi: 10.1016/j.jacc.2005.06.008.
6. Bento CF, Pereira P. Regulation of hypoxia-inducible factor 1 and the loss of the cellular response to hypoxia in diabetes. Diabetologia. 2011;54:1946-1956. doi: 10.1007/s00125-011-2191-8.
7. Caballero S, Sengupta N, Afzal A, Chang KH, Li Calzi S, Guberski DL, Kern TS, Grant MB. Ischemic vascular damage can be repaired by healthy, but not diabetic, endothelial progenitor cells. Diabetes. 2007;56:960-967. doi: 10.2337/db06-1254.
8. Kusuma S, Shen YI, Hanjaya-Putra D, Mali P, Cheng L, Gerecht S. Selforganized vascular networks from human pluripotent stem cells in a synthetic matrix. Proc Natl Acad Sci USA. 2013;110:12601-12606. doi: 10.1073/pnas.1306562110.
9. Seifu DG, Purnama A, Mequanint K, Mantovani D. Small-diameter vascular tissue engineering. Nat Rev Cardiol. 2013;10:410-421. doi: 10.1038/nrcardio.2013.77.
10. Sun G, Gerecht S. Vascular regeneration: engineering the stem cell microenvironment. Regen Med. 2009;4:435-447. doi: 10.2217/rme.09.1.
11. Leeper NJ, Hunter AL, Cooke JP. Stem cell therapy for vascular regeneration: adult, embryonic, and induced pluripotent stem cells. Circulation. 2010;122:517-526. doi: 10.1161/CIRCULATIONAHA.109.881441.
12. Cho SW, Moon SH, Lee SH, Kang SW, Kim J, Lim JM, Kim HS, Kim BS, Chung HM. Improvement of postnatal neovascularization by human embryonic stem cell derived endothelial-like cell transplantation in a mouse model of hindlimb ischemia. Circulation. 2007;116:2409-2419. doi: 10.1161/CIRCULATIONAHA.106.687038.
13. Huang NF, Niiyama H, Peter C, De A, Natkunam Y, Fleissner F, Li Z, Rollins MD, Wu JC, Gambhir SS, Cooke JP. Embryonic stem cell-derived endothelial cells engraft into the ischemic hindlimb and restore perfusion. Arterioscler Thromb Vasc Biol. 2010;30:984-991. doi: 10.1161/ATVBAHA.110.202796.
14. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275:964-967.
15. Li Z, Wilson KD, Smith B, Kraft DL, Jia F, Huang M, Xie X, Robbins RC, Gambhir SS, Weissman IL, Wu JC. Functional and transcriptional characterization of human embryonic stem cell-derived endothelial cells for treatment of myocardial infarction. PLoS One. 2009;4:e8443. doi: 10.1371/journal.pone.0008443.
16. Loomans CJ, van Haperen R, Duijs JM, Verseyden C, de Crom R, Leenen PJ, Drexhage HA, de Boer HC, de Koning EJ, Rabelink TJ, Staal FJ, van Zonneveld AJ. Differentiation of bone marrow-derived endothelial progenitor cells is shifted into a proinflammatory phenotype by hyperglycemia. Mol Med. 2009;15:152-159. doi: 10.2119/molmed.2009.00032.
17. Menegazzo L, Albiero M, Avogaro A, Fadini GP. Endothelial progenitor cells in diabetes mellitus. Biofactors. 2012;38:194-202. doi: 10.1002/biof.1016.
18. Tepper OM, Galiano RD, Capla JM, Kalka C, Gagne PJ, Jacobowitz GR, Levine JP, Gurtner GC. Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation. 2002;106:2781-2786.
19. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007;318:1917-1920. doi: 10.1126/science.1151526.
20. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131:861-872. doi: 10.1016/j.cell.2007.11.019.
21. Mattout A, Biran A, Meshorer E. Global epigenetic changes during somatic cell reprogramming to iPS cells. J Mol Cell Biol. 2011;3:341-350. doi: 10.1093/jmcb/mjr028.
22. Kusuma S, Peijnenburg E, Patel P, Gerecht S. Low oxygen tension enhances endothelial fate of human pluripotent stem cells. Arterioscler Thromb Vasc Biol. 2014;34:913-920. doi: 10.1161/ATVBAHA.114.303274.
23. Kusuma S, Facklam A, Gerecht S. Characterizing human pluripotentstem-cell-derived vascular cells for tissue engineering applications. Stem Cells Dev. 2015;24:451-458. doi: 10.1089/scd.2014.0377.
24. Armulik A, Genové G, Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell. 2011;21:193-215. doi: 10.1016/j.devcel.2011.07.001.
25. Chou BK, Mali P, Huang X, Ye Z, Dowey SN, Resar LM, Zou C, Zhang YA, Tong J, Cheng L. Efficient human iPS cell derivation by a non-integrating plasmid from blood cells with unique epigenetic and gene expression signatures. Cell Res. 2011;21:518-529. doi: 10.1038/cr.2011.12.
26. Cheng L, Hansen NF, Zhao L, Du Y, Zou C, Donovan FX, Chou BK, Zhou G, Li S, Dowey SN, Ye Z, Chandrasekharappa SC, Yang H, Mullikin JC, Liu PP; NISC Comparative Sequencing Program. Low incidence of DNA sequence variation in human induced pluripotent stem cells generated by nonintegrating plasmid expression. Cell Stem Cell. 2012;10:337-344. doi: 10.1016/j.stem.2012.01.005.
27. Watanabe K, Ueno M, Kamiya D, Nishiyama A, Matsumura M, Wataya T, Takahashi JB, Nishikawa S, Nishikawa S, Muguruma K, Sasai Y. A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat Biotechnol. 2007;25:681-686. doi: 10.1038/nbt1310.
28. Gage BK, Webber TD, Kieffer TJ. Initial cell seeding density influences pancreatic endocrine development during in vitro differentiation of human embryonic stem cells. PLoS One. 2013;8:e82076. doi: 10.1371/journal. pone.0082076.
29. Johannesson B, Sagi I, Gore A, et al. Comparable frequencies of coding mutations and loss of imprinting in human pluripotent cells derived by nuclear transfer and defined factors. Cell Stem Cell. 2014;15:634-642. doi: 10.1016/j.stem.2014.10.002.
30. Maehr R, Chen S, Snitow M, Ludwig T, Yagasaki L, Goland R, Leibel RL, Melton DA. Generation of pluripotent stem cells from patients with type 1 diabetes. Proc Natl Acad Sci USA. 2009;106:15768-15773. doi: 10.1073/pnas.0906894106.
31. Kusuma S, Macklin B, Gerecht S. Derivation and network formation of vascular cells from human pluripotent stem cells. Methods Mol Biol. 2014;1202:1-9. doi: 10.1007/7651-2013-39.
32. Hanjaya-Putra D, Bose V, Shen YI, Yee J, Khetan S, Fox-Talbot K, Steenbergen C, Burdick JA, Gerecht S. Controlled activation of morphogenesis to generate a functional human microvasculature in a synthetic matrix. Blood. 2011;118:804-815. doi: 10.1182/blood-2010-12-327338.
33. Davis GE, Stratman AN, Sacharidou A, Koh W. Molecular basis for endothelial lumen formation and tubulogenesis during vasculogenesis and angiogenic sprouting. Int Rev Cell Mol Biol. 2011;288:101-165. doi: 10.1016/B978-0-12-386041-5.00003-0.
34. Capla JM, Grogan RH, Callaghan MJ, Galiano RD, Tepper OM, Ceradini DJ, Gurtner GC. Diabetes impairs endothelial progenitor cell-mediated blood vessel formation in response to hypoxia. Plast Reconstr Surg. 2007;119:59-70. doi: 10.1097/01.prs.0000244830.16906.3f.
35. Park KM, Gerecht S. Hypoxia-inducible hydrogels. Nat Commun. 2014;5:4075. doi: 10.1038/ncomms5075.
36. Orlova VV, 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;9:1514-1531. doi: 10.1038/nprot.2014.102.
37. Au P, Daheron LM, Duda DG, Cohen KS, Tyrrell JA, Lanning RM, Fukumura D, Scadden DT, Jain RK. Differential in vivo potential of endothelial progenitor cells from human umbilical cord blood and adult peripheral blood to form functional long-lasting vessels. Blood. 2008;111:1302-1305. doi: 10.1182/blood-2007-06-094318.
38. Au P, Tam J, Fukumura D, Jain RK. Bone marrow-derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood. 2008;111:4551-4558. doi: 10.1182/blood-2007-10-118273.
39. Koike N, Fukumura D, Gralla O, Au P, Schechner JS, Jain RK. Tissue engineering: creation of long-lasting blood vessels. Nature. 2004;428:138-139. doi: 10.1038/428138a.
40. Wang ZZ, Au P, Chen T, Shao Y, Daheron LM, Bai H, Arzigian M, Fukumura D, Jain RK, Scadden DT. Endothelial cells derived from human embryonic stem cells form durable blood vessels in vivo. Nat Biotechnol. 2007;25:317-318. doi: 10.1038/nbt1287.
41. Holy CE, Shoichet MS, Davies JE. Engineering three-dimensional bone tissue in vitro using biodegradable scaffolds: investigating initial cell-seeding density and culture period. J Biomed Mater Res. 2000;51:376-382.
42. Ghosh S, Dean A, Walter M, Bao Y, Hu Y, Ruan J, Li R. Cell densitydependent transcriptional activation of endocrine-related genes in human adipose tissue-derived stem cells. Exp Cell Res. 2010;316:2087-2098. doi: 10.1016/j.yexcr.2010.04.015.
43. Chen G, Hou Z, Gulbranson DR, Thomson JA. Actin-myosin contractility is responsible for the reduced viability of dissociated human embryonic stem cells. Cell Stem Cell. 2010;7:240-248. doi: 10.1016/j.stem.2010.06.017.
44. Joo HJ, Choi DK, Lim JS, Park JS, Lee SH, Song S, Shin JH, Lim DS, Kim I, Hwang KC, Koh GY. ROCK suppression promotes differentiation and expansion of endothelial cells from embryonic stem cell-derived Flk1(+) mesodermal precursor cells. Blood. 2012;120:2733-2744. doi: 10.1182/blood-2012-04-421610.
45. Li Z, Dong X, Dong X, Wang Z, Liu W, Deng N, Ding Y, Tang L, Hla T, Zeng R, Li L, Wu D. Regulation of PTEN by Rho small GTPases. Nat Cell Biol. 2005;7:399-404. doi: 10.1038/ncb1236.
46. Yang S, Kim HM. The RhoA-ROCK-PTEN pathway as a molecular switch for anchorage dependent cell behavior. Biomaterials. 2012;33:2902-2915. doi: 10.1016/j.biomaterials.2011.12.051.
47. Song MS, Salmena L, Pandolfi PP. The functions and regulation of the PTEN tumour suppressor. Nat Rev Mol Cell Biol. 2012;13:283-296. doi: 10.1038/nrm3330.
48. Shiojima I, Walsh K. Role of Akt signaling in vascular homeostasis and angiogenesis. Circ Res. 2002;90:1243-1250.
49. Castellani L, Salvati E, Alemà S, Falcone G. Fine regulation of RhoA and Rock is required for skeletal muscle differentiation. J Biol Chem. 2006;281:15249-15257. doi: 10.1074/jbc.M601390200.
50. Pagiatakis C, Gordon JW, Ehyai S, McDermott JC. A novel RhoA/ROCKCPI-17-MEF2C signaling pathway regulates vascular smooth muscle cell gene expression. J Biol Chem. 2012;287:8361-8370. doi: 10.1074/jbc. M111.286203.
51. Liu ZJ, Velazquez OC. Hyperoxia, endothelial progenitor cell mobilization, and diabetic wound healing. Antioxid Redox Signal. 2008;10:1869-1882. doi: 10.1089/ars.2008.2121.
52. Loomans CJ, de Koning EJ, Staal FJ, Rookmaaker MB, Verseyden C, de Boer HC, Verhaar MC, Braam B, Rabelink TJ, van Zonneveld AJ. Endothelial progenitor cell dysfunction: a novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes. 2004;53:195-199.
53. Steed DL, Attinger C, Colaizzi T, Crossland M, Franz M, Harkless L, Johnson A, Moosa H, Robson M, Serena T, Sheehan P, Veves A, Wiersma-Bryant L. Guidelines for the treatment of diabetic ulcers. Wound Repair Regen. 2006;14:680-692. doi: 10.1111/j.1524-475X.2006.00176.x.