Vascular progenitors from cord blood-derived induced pluripotent stem cells possess augmented capacity for regenerating ischemic retinal vasculature

Circulation

Volumn 129, Issue 3, 2014, Pages 359-372

  Park, Tea Soon ^a   Bhutto, Imran ^b   Zimmerlin, Ludovic ^a   Huo, Jeffrey S ^a   Nagaria, Pratik ^c   Miller, Diana ^c   Rufaihah, Abdul Jalil ^d,e   Talbot, Connie ^f   Aguilar, Jack ^a   Grebe, Rhonda ^b   Merges, Carol ^b   Reijo Pera, Renee ^e   Feldman, Ricardo A ^c   Rassool, Feyruz ^c   Cooke, John ^d,e   Lutty, Gerard ^b   Zambidis, Elias T ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d STANFORD UNIVERSITY   (United States)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

Author keywords

Blood supply; Diabetic retinopathy; Embryonic stem cells; Induced pluripotent stem cells; Reperfusion injury; Stem cells; Transplantation

Indexed keywords

CD146 ANTIGEN; CD31 ANTIGEN; DNA; LUCIFERASE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DNA DAMAGE; EMBRYONIC STEM CELL; ENGRAFTMENT; FIBROBLAST; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PURIFICATION; REPERFUSION INJURY; RETINA BLOOD VESSEL; RETINA CAPILLARY; RETINA ISCHEMIA; SENESCENCE; STEM CELL; TRANSGENE; UMBILICAL CORD BLOOD; VASCULAR PROGENITOR; VITREOUS BODY;

BLOOD SUPPLY; DIABETIC RETINOPATHY; EMBRYONIC STEM CELLS; INDUCED PLURIPOTENT STEM CELLS; REPERFUSION INJURY; STEM CELLS; TRANSPLANTATION;

ANIMALS; CAPILLARIES; CELL AGING; DISEASE MODELS, ANIMAL; DNA DAMAGE; EMBRYONIC STEM CELLS; FETAL BLOOD; FIBROBLASTS; GRAFT SURVIVAL; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; PLURIPOTENT STEM CELLS; REGENERATION; REPERFUSION INJURY; RETINAL DISEASES; STEM CELL TRANSPLANTATION; TRANSCRIPTOME;

EID: 84893704122     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.113.003000     Document Type: Article

References (45)

1. Paxhia MJ, Ting TD, Fekrat S. Ischemic central retinal vein occlusion and retinitis pigmentosa: lower risk of neovascularization' Retina. 2001;21:179-180.
2. Awdeh RM, Elsing SH, Deramo VA, Stinnett S, Lee PP, Fekrat S. Vision-related quality of life in persons with unilateral branch retinal vein occlusion using the 25-item National Eye Institute Visual Function Questionnaire. Br J Ophthalmol. 2010;94:319-323.
3. Cao J, McLeod S, Merges CA, Lutty GA. Choriocapillaris degeneration and related pathologic changes in human diabetic eyes. Arch Ophthalmol. 1998;116:589-597.
4. Zheng L, Gong B, Hatala DA, Kern TS. Retinal ischemia and reperfusion causes capillary degeneration: similarities to diabetes. Invest Ophthalmol Vis Sci. 2007;48:361-367.
5. Kim SY, Johnson MA, McLeod DS, Alexander T, Otsuji T, Steidl SM, Hansen BC, Lutty GA. Retinopathy in monkeys with spontaneous type 2 diabetes. Invest Ophthalmol Vis Sci. 2004;45:4543-4553.
6. Joussen AM, Poulaki V, Le ML, Koizumi K, Esser C, Janicki H, Schraermeyer U, Kociok N, Fauser S, Kirchhof B, Kern TS, Adamis AP. A central role for inflammation in the pathogenesis of diabetic retinopathy. FASEB J. 2004;18:1450-1452.
7. Kim SY, Johnson MA, McLeod DS, Alexander T, Hansen BC, Lutty GA. Neutrophils are associated with capillary closure in spontaneously diabetic monkey retinas. Diabetes. 2005;54:1534-1542.
8. Joussen AM, Murata T, Tsujikawa A, Kirchhof B, Bursell SE, Adamis AP. Leukocyte-mediated endothelial cell injury and death in the diabetic retina. Am J Pathol. 2001;158:147-152.
9. D'Amore PA. Mechanisms of retinal and choroidal neovascularization. Invest Ophthalmol Vis Sci. 1994;35:3974-3979.
10. Glaser BM, D'Amore PA, Michels RG, Patz A, Fenselau A. Demonstration of vasoproliferative activity from mammalian retina. J Cell Biol. 1980;84:298-304.
11. Grant MB, Caballero S, Brown GA, Guthrie SM, Mames RN, Vaught T, Scott EW. The contribution of adult hematopoietic stem cells to retinal neovascularization. Adv Exp Med Biol. 2003;522:37-45.
12. Sengupta N, Caballero S, Mames RN, Butler JM, Scott EW, Grant MB. The role of adult bone marrow-derived stem cells in choroidal neovascularization. Invest Ophthalmol Vis Sci. 2003;44:4908-4913.
13. Sengupta N, Afzal A, Caballero S, Chang KH, Shaw LC, Pang JJ, Bond VC, Bhutto I, Baba T, Lutty GA, Grant MB. Paracrine modulation of CXCR4 by IGF-1 and VEGF: implications for choroidal neovascularization. Invest Ophthalmol Vis Sci. 2010;51:2697-2704.
14. Lu SJ, Feng Q, Caballero S, Chen Y, Moore MA, Grant MB, Lanza R. Generation of functional hemangioblasts from human embryonic stem cells. Nat Methods. 2007;4:501-509.
15. Friedlander M, Dorrell MI, Ritter MR, Marchetti V, Moreno SK, El-Kalay M, Bird AC, Banin E, Aguilar E. Progenitor cells and retinal angiogenesis. Angiogenesis. 2007;10:89-101.
16. 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.
17. Brunner S, Hoellerl F, Schmid-Kubista KE, Zeiler F, Schernthaner G, Binder S, Schernthaner GH. Circulating angiopoietic cells and diabetic retinopathy in type 2 diabetes mellitus, with or without macrovascular disease. Invest Ophthalmol Vis Sci. 2011;52:4655-4662.
18. 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.
19. Ferreira LS, Gerecht S, Shieh HF, Watson N, Rupnick MA, Dallabrida SM, Vunjak-Novakovic G, Langer R. Vascular progenitor cells isolated from human embryonic stem cells give rise to endothelial and smooth muscle like cells and form vascular networks in vivo. Circ Res. 2007;101:286-294.
20. Li Z, Wu JC, Sheikh AY, Kraft D, Cao F, Xie X, Patel M, Gambhir SS, Robbins RC, Cooke JP, Wu JC. Differentiation, survival, and function of embryonic stem cell derived endothelial cells for ischemic heart disease. Circulation. 2007;116(11 suppl):I46-I54.
21. Rufaihah AJ, Huang NF, Jamé S, Lee JC, Nguyen HN, Byers B, De A, Okogbaa J, Rollins M, Reijo-Pera R, Gambhir SS, Cooke JP. Endothelial cells derived from human iPSCS increase capillary density and improve perfusion in a mouse model of peripheral arterial disease. Arterioscler Thromb Vasc Biol. 2011;31:e72-e79.
22. Dar A, Domev H, Ben-Yosef O, Tzukerman M, Zeevi-Levin N, Novak A, Germanguz I, Amit M, Itskovitz-Eldor J. Multipotent vasculogenic pericytes from human pluripotent stem cells promote recovery of murine ischemic limb. Circulation. 2012;125:87-99.
23. Park TS, Zambidis ET, Lucitti JL, Logar A, Keller BB, Péault B. Human embryonic stem cell-derived hematoendothelial progenitors engraft chicken embryos. Exp Hematol. 2009;37:31-41.
24. Zambidis ET, Park TS, Yu W, Tam A, Levine M, Yuan X, Pryzhkova M, Péault B. Expression of angiotensin-converting enzyme (CD143) identifies and regulates primitive hemangioblasts derived from human pluripotent stem cells. Blood. 2008;112:3601-3614.
25. Grant MB, May WS, Caballero S, Brown GA, Guthrie SM, Mames RN, Byrne BJ, Vaught T, Spoerri PE, Peck AB, Scott EW. Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization. Nat Med. 2002;8:607-612.
26. Peters A, Burridge PW, Pryzhkova MV, Levine MA, Park TS, Roxbury C, Yuan X, Péault B, Zambidis ET. Challenges and strategies for generating therapeutic patient-specific hemangioblasts and hematopoietic stem cells from human pluripotent stem cells. Int J Dev Biol. 2010;54:965-990.
27. Ramos-Mejía V, Montes R, Bueno C, Ayllón V, Real PJ, Rodríguez R, Menendez P. Residual expression of the reprogramming factors prevents differentiation of iPSC generated from human fibroblasts and cord blood CD34+ progenitors. PLoS One. 2012;7:e35824.
28. Miura K, Okada Y, Aoi T, Okada A, Takahashi K, Okita K, Nakagawa M, Koyanagi M, Tanabe K, Ohnuki M, Ogawa D, Ikeda E, Okano H, Yamanaka S. Variation in the safety of induced pluripotent stem cell lines. Nat Biotechnol. 2009;27:743-745.
29. Feng Q, Lu SJ, Klimanskaya I, Gomes I, Kim D, Chung Y, Honig GR, Kim KS, Lanza R. Hemangioblastic derivatives from human induced pluripotent stem cells exhibit limited expansion and early senescence. Stem Cells. 2010;28:704-712.
30. Yu J, Hu K, Smuga-Otto K, Tian S, Stewart R, Slukvin II, Thomson JA. Human induced pluripotent stem cells free of vector and transgene sequences. Science. 2009;324:797-801.
31. Burridge PW, Thompson S, Millrod MA, Weinberg S, Yuan X, Peters A, Mahairaki V, Koliatsos VE, Tung L, Zambidis ET. A universal system for highly efficient cardiac differentiation of human induced pluripotent stem cells that eliminates interline variability. PLoS One. 2011;6:e18293.
32. Park TS, Huo JS, Peters A, Talbot CC Jr, Verma K, Zimmerlin L, Kaplan IM, Zambidis ET. Growth factor-activated stem cell circuits and stromal signals cooperatively accelerate non-integrated iPSC reprogramming of human myeloid progenitors. PLoS One. 2012;7:e42838.
33. Park TS, Zimmerlin L, Zambidis ET. Efficient and simultaneous generation of hematopoietic and vascular progenitors from human induced pluripotent stem cells. Cytometry A. 2013;83:114-126.
34. Park TS, Burridge P, Zambidis ET. 24: Generation of multipotent CD34+CD45+ hematopoietic progenitors from human induced pluripotent stem cells. In: Human embryonic and induced pluripotent stem cells: Lineage Specific Differentiation Protocols. Secaucus, NJ: Springer Science & Business Media, Springer Protocols Handbooks; 2012:337-350.
35. Zambidis ET, Peault B, Park TS, Bunz F, Civin CI. Hematopoietic differentiation of human embryonic stem cells progresses through sequential hematoendothelial, primitive, and definitive stages resembling human yolk sac development. Blood. 2005;106:860-870.
36. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L, Norotte C, Teng PN, Traas J, Schugar R, Deasy BM, Badylak S, Buhring HJ, Giacobino JP, Lazzari L, Huard J, Péault B. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008;3:301-313.
37. Park TS, Gavina M, Chen CW, Sun B, Teng PN, Huard J, Deasy BM, Zimmerlin L, Péault B. Placental perivascular cells for human muscle regeneration. Stem Cells Dev. 2011;20:451-463.
38. Rehman J, Li J, Orschell CM, March KL. Peripheral blood "endothelial progenitor cells" are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation. 2003;107:1164-1169.
39. Choi KD, Vodyanik MA, Togarrati PP, Suknuntha K, Kumar A, Samarjeet F, Probasco MD, Tian S, Stewart R, Thomson JA, Slukvin II. Identification of the hemogenic endothelial progenitor and its direct precursor in human pluripotent stem cell differentiation cultures. Cell Rep. 2012;2:553-567.
40. Gupta SK, Lysko PG, Pillarisetti K, Ohlstein E, Stadel JM. Chemokine receptors in human endothelial cells. Functional expression of CXCR4 and its transcriptional regulation by inflammatory cytokines. J Biol Chem. 1998;273:4282-4287.
41. Okita K, Yamakawa T, Matsumura Y, Sato Y, Amano N, Watanabe A, Goshima N, Yamanaka S. An efficient nonviral method to generate integration-free human-induced pluripotent cells from cord blood and peripheral blood cells. Stem Cells. 2013;31:458-466.
42. Taylor CJ, Bolton EM, Pocock S, Sharples LD, Pedersen RA, Bradley JA. Banking on human embryonic stem cells: estimating the number of donor cell lines needed for HLA matching. Lancet. 2005;366:2019-2025.
43. de Lima M, McNiece I, Robinson SN, Munsell M, Eapen M, Horowitz M, Alousi A, Saliba R, McMannis JD, Kaur I, Kebriaei P, Parmar S, Popat U, Hosing C, Champlin R, Bollard C, Molldrem JJ, Jones RB, Nieto Y, Andersson BS, Shah N, Oran B, Cooper LJ, Worth L, Qazilbash MH, Korbling M, Rondon G, Ciurea S, Bosque D, Maewal I, Simmons PJ, Shpall EJ. Cord-blood engraftment with ex vivo mesenchymal-cell coculture. N Engl J Med. 2012;367:2305-2315.
44. Hasegawa T, McLeod DS, Prow T, Merges C, Grebe R, Lutty GA. Vascular precursors in developing human retina. Invest Ophthalmol Vis Sci. 2008;49:2178-2192.
45. McLeod DS, Hasegawa T, Prow T, Merges C, Lutty G. The initial fetal human retinal vasculature develops by vasculogenesis. Dev Dyn. 2006;235:3336-3347.