Very small embryonic-like stem cells: Biology and therapeutic potential for heart repair

Antioxidants and Redox Signaling

Volumn 15, Issue 7, 2011, Pages 1821-1834

  Zuba Surma, Ewa K ^a   Wojakowski, Wojciech ^b   Ratajczak, Mariusz Z ^c   Dawn, Buddhadeb ^d  

^a JAGIELLONIAN UNIVERSITY   (Poland)

^b MEDICAL UNIVERSITY OF SILESIA   (Poland)

^c UNIVERSITY OF LOUISVILLE   (United States)

^d UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATAXIN 1; CD133 ANTIGEN;

ACUTE HEART INFARCTION; CELL DIFFERENTIATION; CELL REGENERATION; CELL TRANSPLANTATION; ECTODERM; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; HEART LEFT VENTRICLE PERFORMANCE; HEART MUSCLE CELL; HUMAN; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; VERY SMALL EMBRYONIC LIKE STEM CELL;

ANIMALS; ANTIGENS, DIFFERENTIATION; BLASTOCYST; BONE MARROW CELLS; CELL CULTURE TECHNIQUES; EPIGENESIS, GENETIC; FETAL BLOOD; GENE EXPRESSION; HEART; HEART DISEASES; HUMANS; PHENOTYPE; PLURIPOTENT STEM CELLS; REGENERATION; REGENERATIVE MEDICINE;

MUS;

EID: 80051973867     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2010.3817     Document Type: Review

References (95)

1. Abdel-Latif A, Bolli R, Tleyjeh IM, Montori VM, Perin EC, Hornung CA, Zuba-Surma EK, Al-Mallah M, and Dawn B. Adult bone marrow-derived cells for cardiac repair: a systematic review and meta-analysis. Arch Intern Med 167: 989-997, 2007. (Pubitemid 46835786)
2. Abdel-Latif A, Zuba-Surma EK, Case J, Tiwari S, Hunt G, Ranjan S, Vincent RJ, Srour EF, Bolli R, and Dawn B. TGFbeta1 enhances cardiomyogenic differentiation of skeletal muscle-derived adult primitive cells. Basic Res Cardiol 103: 514-524, 2008.
3. Abdel-Latif A, Zuba-Surma EK, Ziada KM, Kucia M, Cohen DA, Kaplan AM, Van Zant G, Selim S, Smyth SS, and Ratajczak MZ. Evidence of mobilization of pluripotent stem cells into peripheral blood of patients with myocardial ischemia. Exp Hematol 38: 1131-1142.e1, 2010.
4. Alison MR, Poulsom R, Otto WR, Vig P, Brittan M, Direkze NC, Preston SL, and Wright NA. Plastic adult stem cells: will they graduate from the school of hard knocks? J Cell Sci 116: 599-603, 2003. (Pubitemid 36231298)
5. Anjos-Afonso F and Bonnet D. Nonhematopoietic/endothelial SSEA-1 + cells define the most primitive progenitors in the adult murine bone marrow mesenchymal compartment. Blood 109: 1298-1306, 2007. (Pubitemid 46220683)
6. Basiji DA, Ortyn WE, Liang L, Venkatachalam V, and Morrissey P. Cellular image analysis and imaging by flow cytometry. Clin Lab Med 27: 653-670, viii, 2007. (Pubitemid 47068811)
7. Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S, Kasahara H, Rota M, Musso E, Urbanek K, Leri A, Kajstura J, Nadal-Ginard B, and Anversa P. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114: 763-776, 2003. (Pubitemid 37186770)
8. Beltrami AP, Cesselli D, Bergamin N, Marcon P, Rigo S, Puppato E, D'Aurizio F, Verardo R, Piazza S, Pignatelli A, Poz A, Baccarani U, Damiani D, Fanin R, Mariuzzi L, Finato N, Masolini P, Burelli S, Belluzzi O, Schneider C, and Beltrami CA. Multipotent cells can be generated in vitro from several adult human organs (heart, liver, and bone marrow). Blood 110: 3438-3446, 2007. (Pubitemid 350106340)
9. Bittira B, Shum-Tim D, Al-Khaldi A, and Chiu RC. Mobilization and homing of bone marrow stromal cells in myocardial infarction. Eur J Cardiothorac Surg 24: 393-398, 2003. (Pubitemid 37083532)
10. Broxmeyer HE, Douglas GW, Hangoc G, Cooper S, Bard J, English D, Arny M, Thomas L, and Boyse EA. Human umbilical cord blood as a potential source of transplantable hematopoietic stem/progenitor cells. Proc Natl Acad Sci USA 86: 3828-3832, 1989. (Pubitemid 19141838)
11. Buzanska L, Jurga M, and Domanska-Janik K. Neuronal differentiation of human umbilical cord blood neural stemlike cell line. Neurodegener Dis 3: 19-26, 2006. (Pubitemid 43760363)
12. Buzanska L, Machaj EK, Zablocka B, Pojda Z, and Domanska-Janik K. Human cord blood-derived cells attain neuronal and glial features in vitro. J Cell Sci 115: 213-218, 2002.
13. Castro RF, Jackson KA, Goodell MA, Robertson CS, Liu H, and Shine HD. Failure of bone marrow cells to transdifferentiate into neural cells in vivo. Science 297: 1299, 2002. (Pubitemid 34913161)
14. Chimenti I, Smith RR, Li TS, Gerstenblith G, Messina E, Giacomello A, and Marban E. Relative roles of direct regeneration versus paracrine effects of human cardiospherederived cells transplanted into infarcted mice. Circ Res 106: 971-980, 2010.
15. Chugh AR, Zuba-Surma EK, and Dawn B. Bone marrowderived mesenchymal stems cells and cardiac repair. Minerva Cardioangiol 57: 185-202, 2009.
16. Dai W and Kloner RA. Myocardial regeneration by embryonic stem cell transplantation: present and future trends. Exp Rev Cardiovasc Ther 4: 375-383, 2006. (Pubitemid 43796995)
17. Danner S, Kajahn J, Geismann C, Klink E, and Kruse C. Derivation of oocyte-like cells from a clonal pancreatic stem cell line. Mol Hum Reprod 13: 11-20, 2007. (Pubitemid 44942720)
18. Das S, Bonaguidi M, Muro K, and Kessler JA. Generation of embryonic stem cells: limitations of and alternatives to inner cell mass harvest. Neurosurg Focus 24: E4, 2008.
19. Dawn B, Abdel-Latif A, Sanganalmath SK, Flaherty MP, and Zuba-Surma EK. Cardiac repair with adult bone marrowderived cells: the clinical evidence. Antioxid Redox Signal 11: 1865-1882, 2009.
20. Dawn B, Stein AB, Urbanek K, Rota M, Whang B, Rastaldo R, Torella D, Tang XL, Rezazadeh A, Kajstura J, Leri A, Hunt G, Varma J, Prabhu SD, Anversa P, and Bolli R. Cardiac stem cells delivered intravascularly traverse the vessel barrier, regenerate infarcted myocardium, and improve cardiac function. Proc Natl Acad Sci USA 102: 3766-3771, 2005. (Pubitemid 40354686)
21. Dawn B, Tiwari S, Kucia MJ, Zuba-Surma EK, Guo Y, Sanganalmath SK, Abdel-Latif A, Hunt G, Vincent RJ, Taher H, Reed NJ, Ratajczak MZ, and Bolli R. Transplantation of bone marrow-derived very small embryonic-like stem cells attenuates left ventricular dysfunction and remodeling after myocardial infarction. Stem Cells 26: 1646-1655, 2008.
22. De Coppi P, Bartsch G, Jr., Siddiqui MM, Xu T, Santos CC, Perin L, Mostoslavsky G, Serre AC, Snyder EY, Yoo JJ, Furth ME, Soker S, and Atala A. Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol 25: 100-106, 2007. (Pubitemid 46087908)
23. Di Campli C, Piscaglia AC, Pierelli L, Rutella S, Bonanno G, Alison MR, Mariotti A, Vecchio FM, Nestola M, Monego G, Michetti F, Mancuso S, Pola P, Leone G, Gasbarrini G, and Gasbarrini A. A human umbilical cord stem cell rescue therapy in a murine model of toxic liver injury. Dig Liver Dis 36: 603-613, 2004. (Pubitemid 41122182)
24. Dyce PW, Zhu H, Craig J, and Li J. Stem cells with multilineage potential derived from porcine skin. Biochem Biophys Res Commun 316: 651-658, 2004. (Pubitemid 38368002)
25. Eggenschwiler J, Ludwig T, Fisher P, Leighton PA, Tilghman SM, and Efstratiadis A. Mouse mutant embryos overexpressing IGF-II exhibit phenotypic features of the Beckwith-Wiedemann and Simpson-Golabi-Behmel syndromes. Genes Dev 11: 3128-3142, 1997. (Pubitemid 27528054)
26. Gnecchi M, He H, Liang OD, Melo LG, Morello F, Mu H, Noiseux N, Zhang L, Pratt RE, Ingwall JS, and Dzau VJ. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 11: 367-368, 2005. (Pubitemid 40562318)
27. Hajkova P, Erhardt S, Lane N, Haaf T, El-Maarri O, Reik W, Walter J, and Surani MA. Epigenetic reprogramming in mouse primordial germ cells. Mech Dev 117: 15-23, 2002. (Pubitemid 36158711)
28. Hao Y, Crenshaw T, Moulton T, Newcomb E, and Tycko B. Tumour-suppressor activity of H19 RNA. Nature 365: 764-767, 1993. (Pubitemid 23339885)
29. Harris DT and Rogers I. Umbilical cord blood: a unique source of pluripotent stem cells for regenerative medicine. Curr Stem Cell Res Ther 2: 301-309, 2007.
30. Hatzistergos KE, Quevedo H, Oskouei BN, Hu Q, Feigenbaum GS, Margitich IS, Mazhari R, Boyle AJ, Zambrano JP, Rodriguez JE, Dulce R, Pattany PM, Valdes D, Revilla C, Heldman AW, McNiece I, and Hare JM. Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ Res 107: 819, 2010.
31. Kanatsu-Shinohara M, Inoue K, Lee J, Yoshimoto M, Ogonuki N, Miki H, Baba S, Kato T, Kazuki Y, Toyokuni S, Toyoshima M, Niwa O, Oshimura M, Heike T, Nakahata T, Ishino F, Ogura A, and Shinohara T. Generation of pluripotent stem cells from neonatal mouse testis. Cell 119: 1001-1012, 2004. (Pubitemid 40037613)
32. Kerkis I, Kerkis A, Dozortsev D, Stukart-Parsons GC, Gomes Massironi SM, Pereira LV, Caplan AI, and Cerruti HF. Isolation and characterization of a population of immature dental pulp stem cells expressing OCT-4 and other embryonic stem cell markers. Cells Tissues Organs 184: 105-116, 2006.
33. Kogler G, Sensken S, Airey JA, Trapp T, Muschen M, Feldhahn N, Liedtke S, Sorg RV, Fischer J, Rosenbaum C, Greschat S, Knipper A, Bender J, Degistirici O, Gao J, Caplan AI, Colletti EJ, Almeida-Porada G, Muller HW, Zanjani E, and Wernet P. A new human somatic stem cell from placental cord blood with intrinsic pluripotent differentiation potential. J Exp Med 200: 123-135, 2004. (Pubitemid 38982172)
34. Koso H, Ouchi Y, Tabata Y, Aoki Y, Satoh S, Arai K, and Watanabe S. SSEA-1 marks regionally restricted immature subpopulations of embryonic retinal progenitor cells that are regulated by the Wnt signaling pathway. Dev Biol 292: 265-276, 2006.
35. Kruse C, Kajahn J, Petschnik AE, Maass A, Klink E, Rapoport DH, and Wedel T. Adult pancreatic stem/progenitor cells spontaneously differentiate in vitro into multiple cell lineages and form teratoma-like structures. Ann Anat 188: 503-517, 2006. (Pubitemid 44603944)
36. Kucia M, Dawn B, Hunt G, Guo Y, Wysoczynski M, Majka M, Ratajczak J, Rezzoug F, Ildstad ST, Bolli R, and Ratajczak MZ. Cells expressing early cardiac markers reside in the bone marrow and are mobilized into the peripheral blood after myocardial infarction. Circ Res 95: 1191-1199, 2004. (Pubitemid 39648210)
37. Kucia M, Halasa M, Wysoczynski M, Baskiewicz-Masiuk M, Moldenhawer S, Zuba-Surma E, Czajka R, Wojakowski W, Machalinski B, and Ratajczak MZ. Morphological and molecular characterization of novel population of CXCR4 + SSEA-4 + Oct-4 + very small embryonic-like cells purified from human cord blood: preliminary report. Leukemia 21: 297-303, 2007. (Pubitemid 46158123)
38. Kucia M, Reca R, Campbell FR, Zuba-Surma E, Majka M, Ratajczak J, and Ratajczak MZ. A population of very small embryonic-like (VSEL) CXCR4(+)SSEA-1(+)Oct-4 + stem cells identified in adult bone marrow. Leukemia 20: 857-869, 2006.
39. Kucia M, Reca R, Jala VR, Dawn B, Ratajczak J, and Ratajczak MZ. Bone marrow as a home of heterogenous populations of nonhematopoietic stem cells. Leukemia 19: 1118-1127, 2005. (Pubitemid 40945992)
40. Kumar D, Kamp TJ, and LeWinter MM. Embryonic stem cells: differentiation into cardiomyocytes and potential for heart repair and regeneration. Coron Artery Dis 16: 111-116, 2005. (Pubitemid 40393186)
41. Lamoury FM, Croitoru-Lamoury J, and Brew BJ. Undifferentiated mouse mesenchymal stem cells spontaneously express neural and stem cell markers Oct-4 and Rex-1. Cytotherapy 8: 228-242, 2006. (Pubitemid 43947789)
42. Ling TY, Kuo MD, Li CL, Yu AL, Huang YH, Wu TJ, Lin YC, Chen SH, and Yu J. Identification of pulmonary Oct-4 + stem/progenitor cells and demonstration of their susceptibility to SARS coronavirus (SARS-CoV) infection in vitro. Proc Natl Acad Sci USA 103: 9530-9535, 2006. (Pubitemid 43955859)
43. Massa M, Rosti V, Ferrario M, Campanelli R, Ramajoli I, Rosso R, De Ferrari GM, Ferlini M, Goffredo L, Bertoletti A, Klersy C, Pecci A, Moratti R, and Tavazzi L. Increased circulating hematopoietic and endothelial progenitor cells in the early phase of acute myocardial infarction. Blood 105: 199-206, 2005. (Pubitemid 40053083)
44. Mayani H and Lansdorp PM. Biology of human umbilical cord blood-derived hematopoietic stem/progenitor cells. Stem Cells 16: 153-165, 1998. (Pubitemid 28235160)
45. Mezey E, Chandross KJ, Harta G, Maki RA, and McKercher SR. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science 290: 1779-1782, 2000. (Pubitemid 32004811)
46. Murry CE, Soonpaa MH, Reinecke H, Nakajima H, Nakajima HO, Rubart M, Pasumarthi KB, Virag JI, Bartelmez SH, Poppa V, Bradford G, Dowell JD, Williams DA, and Field LJ. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428: 664-668, 2004. (Pubitemid 38524810)
47. Newsome PN, Johannessen I, Boyle S, Dalakas E, McAulay KA, Samuel K, Rae F, Forrester L, Turner ML, Hayes PC, Harrison DJ, Bickmore WA, and Plevris JN. Human cord blood-derived cells can differentiate into hepatocytes in the mouse liver with no evidence of cellular fusion. Gastroenterology 124: 1891-1900, 2003. (Pubitemid 36666784)
48. Orkin SH and Zon LI. Hematopoiesis and stem cells: plasticity versus developmental heterogeneity. Nat Immunol 3: 323-328, 2002. (Pubitemid 34308613)
49. Ortyn WE, Hall BE, George TC, Frost K, Basiji DA, Perry DJ, Zimmerman CA, Coder D, and Morrissey PJ. Sensitivity measurement and compensation in spectral imaging. Cytometry A 69: 852-862, 2006. (Pubitemid 44469997)
50. Paczkowska E, Kucia M, Koziarska D, Halasa M, Safranow K, Masiuk M, Karbicka A, Nowik M, Nowacki P, Ratajczak MZ, and Machalinski B. Clinical evidence that very small embryonic-like stem cells are mobilized into peripheral blood in patients after stroke. Stroke 40: 1237-1244, 2009.
51. Paczkowska E, Larysz B, Rzeuski R, Karbicka A, Jalowinski R, Kornacewicz-Jach Z, Ratajczak MZ, and Machalinski B. Human hematopoietic stem/progenitor-enriched CD34(+) cells are mobilized into peripheral blood during stress related to ischemic stroke or acute myocardial infarction. Eur J Haematol 75: 461-467, 2005. (Pubitemid 41687779)
52. Pesce M, Orlandi A, Iachininoto MG, Straino S, Torella AR, Rizzuti V, Pompilio G, Bonanno G, Scambia G, and Capogrossi MC. Myoendothelial differentiation of human umbilical cord blood-derived stem cells in ischemic limb tissues. Circ Res 93: e51-e62, 2003.
53. Ratajczak MZ, Kucia M, Ratajczak J, and Zuba-Surma EK. A multi-instrumental approach to identify and purify very small embryonic like stem cells (VSELs) from adult tissues. Micron 40: 386-393, 2009.
54. Ratajczak MZ, Kucia M, Reca R, Majka M, Janowska-Wieczorek A, and Ratajczak J. Stem cell plasticity revisited: CXCR4-positive cells expressing mRNA for early muscle, liver and neural cells 'hide out' in the bone marrow. Leukemia 18: 29-40, 2004. (Pubitemid 38159436)
55. Ratajczak MZ, Machalinski B, Wojakowski W, Ratajczak J, and Kucia M. A hypothesis for an embryonic origin of pluripotent Oct-4(+) stem cells in adult bone marrow and other tissues. Leukemia 21: 860-867, 2007. (Pubitemid 46672060)
56. Ratajczak MZ, Zuba-Surma EK, Machalinski B, and Kucia M. Bone-marrow-derived stem cells: our key to longevity? J Appl Genet 48: 307-319, 2007. (Pubitemid 350219928)
57. Ratajczak MZ, Zuba-Surma EK, Machalinski B, Ratajczak J, and Kucia M. Very small embryonic-like (VSEL) stem cells: purification from adult organs, characterization, and biological significance. Stem Cell Rev 4: 89-99, 2008.
58. Ratajczak MZ, Zuba-Surma EK, Shin DM, Ratajczak J, and Kucia M. Very small embryonic-like (VSEL) stem cells in adult organs and their potential role in rejuvenation of tissues and longevity. Exp Gerontol 43: 1009-1017, 2008.
59. Ratajczak MZ, Zuba-Surma EK, Wysoczynski M, Ratajczak J, and Kucia M. Very small embryonic-like stem cells: characterization, developmental origin, and biological significance. Exp Hematol 36: 742-751, 2008. (Pubitemid 351637617)
60. Ratajczak MZ, Zuba-Surma EK, Wysoczynski M, Wan W, Ratajczak J, Wojakowski W, and Kucia M. Hunt for pluripotent stem cell: regenerative medicine search for almighty cell. J Autoimmun 30: 151-162, 2008.
61. Reik W and Walter J. Genomic imprinting: parental influence on the genome. Nat Rev Genet 2: 21-32, 2001. (Pubitemid 33674766)
62. Saito S, Liu B, and Yokoyama K. Animal embryonic stem (ES) cells: self-renewal, pluripotency, transgenesis and nuclear transfer. Hum Cell 17: 107-115, 2004.
63. Shah RV and Mitchell RN. The role of stem cells in the response to myocardial and vascular wall injury. Cardiovasc Pathol 14: 225-231, 2005. (Pubitemid 41317268)
64. Shin DM, Liu R, Klich I, Ratajczak J, Kucia M, and Ratajczak MZ. Molecular characterization of isolated from murine adult tissues very small embryonic/epiblast like stem cells (VSELs). Mol Cells 29: 533-538, 2010.
65. Shin DM, Zuba-Surma EK, Wu W, Ratajczak J, Wysoczynski M, Ratajczak MZ, and Kucia M. Novel epigenetic mechanisms that control pluripotency and quiescence of adult bone marrow-derived Oct4(+) very small embryonic-like stem cells. Leukemia 23: 2042-2051, 2009.
66. Shintani S, Murohara T, Ikeda H, Ueno T, Honma T, Katoh A, Sasaki K, Shimada T, Oike Y, and Imaizumi T. Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation 103: 2776-2779, 2001. (Pubitemid 32550062)
67. Spevack DM, Cavaleri S, Zolotarev A, Liebes L, Inghirami G, Tunick PA, and Kronzon I. Increase in circulating bone marrow progenitor cells after myocardial infarction. Coron Artery Dis 17: 345-349, 2006. (Pubitemid 44309793)
68. Tachibana M, Ueda J, Fukuda M, Takeda N, Ohta T, Iwanari H, Sakihama T, Kodama T, Hamakubo T, and Shinkai Y. Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3-K9. Genes Dev 19: 815-826, 2005.
69. Taichman RS, Wang Z, Shiozawa Y, Jung Y, Song J, Balduino A, Wang J, Patel LR, Havens AM, Kucia M, Ratajczak MZ, and Krebsbach PH. Prospective identification and skeletal localization of cells capable of multilineage differentiation in vivo. Stem Cells Dev 19: 1557-1570, 2010.
70. Tang J, Xie Q, Pan G, Wang J, and Wang M. Mesenchymal stem cells participate in angiogenesis and improve heart function in rat model of myocardial ischemia with reperfusion. Eur J Cardiothorac Surg 30: 353-361, 2006. (Pubitemid 44051890)
71. Wang Y, Haider H, Ahmad N, Zhang D, and Ashraf M. Evidence for ischemia induced host-derived bone marrow cell mobilization into cardiac allografts. J Mol Cell Cardiol 41: 478-487, 2006. (Pubitemid 44349132)
72. Weiss ML and Troyer DL. Stem cells in the umbilical cord. Stem Cell Rev 2: 155-162, 2006. (Pubitemid 46137576)
73. Wojakowski W, Tendera M, Kucia M, Zuba-Surma E, Milewski K, Wallace-Bradley D, Kazmierski M, Buszman P, Hrycek E, Cybulski W, Kaluza G, Wieczorek P, Ratajczak J, and Ratajczak MZ. Cardiomyocyte differentiation of bone marrow-derived Oct-4+CXCR4+SSEA-1+very small embryonic-like stem cells. Int J Oncol 37: 237-247, 2010.
74. Wojakowski W, Tendera M, Kucia M, Zuba-Surma E, Paczkowska E, Ciosek J, Halasa M, Krol M, Kazmierski M, Buszman P, Ochala A, Ratajczak J, Machalinski B, and Ratajczak MZ. Mobilization of bone marrow-derived Oct-4 + SSEA-4 + very small embryonic-like stem cells in patients with acute myocardial infarction. J Am Coll Cardiol 53: 1-9, 2009.
75. Wojakowski W, Tendera M, Michalowska A, Majka M, Kucia M, Maslankiewicz K, Wyderka R, Ochala A, and Ratajczak MZ. Mobilization of CD34/CXCR4+, CD34/CD117+, c-met+stem cells, and mononuclear cells expressing early cardiac, muscle, and endothelial markers into peripheral blood in patients with acute myocardial infarction. Circulation 110: 3213-3220, 2004. (Pubitemid 39525068)
76. Wojakowski W, Tendera M, Zebzda A, Michalowska A, Majka M, Kucia M, Maslankiewicz K, Wyderka R, Krol M, Ochala A, Kozakiewicz K, and Ratajczak MZ. Mobilization of CD34(+), CD117(+), CXCR4(+), c-met(+) stem cells is correlated with left ventricular ejection fraction and plasma NT-proBNP levels in patients with acute myocardial infarction. Eur Heart J 27: 283-289, 2006. (Pubitemid 43100022)
77. Wollert KC and Drexler H. Cell therapy for the treatment of coronary heart disease: a critical appraisal. Nat Rev Cardiol 7: 204-215, 2010.
78. Yoshida Y and Yamanaka S. Recent stem cell advances: induced pluripotent stem cells for disease modeling and stem cell-based regeneration. Circulation 122: 80-87, 2010.
79. Yu G, Borlongan CV, Stahl CE, Yu SJ, Bae E, Yang T, Zhou J, Li Y, Xiong W, Qin L, and Zhou B. Transplantation of human umbilical cord blood cells for the repair of myocardial infarction. Med Sci Monit 14: RA163-RA172, 2008.
80. Yu H, Fang D, Kumar SM, Li L, Nguyen TK, Acs G, Herlyn M, and Xu X. Isolation of a novel population of multipotent adult stem cells from human hair follicles. Am J Pathol 168: 1879-1888, 2006. (Pubitemid 43825308)
81. Zuba-Surma EK, Abdel-Latif A, Case J, Tiwari S, Hunt G, Kucia M, Vincent RJ, Ranjan S, Ratajczak MZ, Srour EF, Bolli R, and Dawn B. Sca-1 expression is associated with decreased cardiomyogenic differentiation potential of skeletal muscle-derived adult primitive cells. J Mol Cell Cardiol 41: 650-660, 2006. (Pubitemid 44374538)
82. Zuba-Surma EK, Guo Y, Taher H, Dawn B, Ratajczak MZ, and Bolli R. The reparative benefits of very small embryonic like (VSEL) stem cells are sustained during long-term follow-up. Circulation 112: 21-28, 2008.
83. Zuba-Surma EK, Guo Y, Taher H, Sanganalmath SK, Hunt G, Vincent RJ, Kucia M, Abdel-Latif A, Tang XL, Ratajczak MZ, Dawn B, and Bolli R. Transplantation of expanded bone marrow-derived very small embryonic-like stem cells (VSEL-SCs) improves left ventricular function and remodeling after myocardial infarction. J Cell Mol Med: [Epub ahead of print], 2010.
84. Zuba-Surma EK, Klich I, Greco N, Laughlin MJ, Ratajczak J, and Ratajczak MZ. Optimization of isolation and further characterization of umbilical-cord-blood-derived very small embryonic epiblast-like stem cells (VSELs). Eur J Haematol 84: 34-46, 2010.
85. Zuba-Surma EK, Kucia M, Abdel-Latif A, Dawn B, Hall B, Singh R, Lillard JW Jr, and Ratajczak MZ. Morphological characterization of very small embryonic-like stem cells (VSELs) by ImageStream system analysis. J Cell Mol Med 12: 292-303, 2008.
86. Zuba-Surma EK, Kucia M, Abdel-Latif A, Lillard JW Jr, Ratajczak MZ. The ImageStream System: a key step to a new era in imaging. Folia Histochem Cytobiol 45: 279-270, 2007.
87. Zuba-Surma EK, Kucia M, Dawn B, Guo Y, Ratajczak MZ, and Bolli R. Bone marrow-derived pluripotent very small embryonic-like stem cells (VSELs) are mobilized after acute myocardial infarction. J Mol Cell Cardiol 44: 865-873, 2008.
88. Zuba-Surma EK, Kucia M, Liu R, Klich I, Ratajczak MZ, and Ratajczak J. CD45-/ALDH-low/SSEA-4 +/Oct-4 +/CD133 +/CXCR4 +/Lin-very small embryonic-like (VSEL) stem cells isolated from umbilical cord blood as potential long term repopulating hematopoietic stem cells. Blood 112: 850, 2008.
89. Zuba-Surma EK, Kucia M, Ratajczak J, and Ratajczak MZ. "Small stem cells" in adult tissues: very small embryonic-like stem cells stand up! Cytometry A 75: 4-13, 2009.
90. Zuba-Surma EK, Kucia M, and Ratajczak MZ. "Decoding of dot": the ImageStream System (ISS) as a supportive tool for flow cytometric analysis. Cen Eur J Biol 3: 1-10, 2008. (Pubitemid 351659764)
91. Zuba-Surma EK, Kucia M, Rui L, Shin DM, Wojakowski W, Ratajczak J, and Ratajczak MZ. Fetal liver very small embryonic/epiblast like stem cells follow developmental migratory pathway of hematopoietic stem cells. Ann N Y Acad Sci 1176: 205-218, 2009.
92. Zuba-Surma EK, Kucia M, Wu W, Klich I, Lillard JW Jr, Ratajczak J, and Ratajczak MZ. Very small embryonic-like stem cells are present in adult murine organs: ImageStreambased morphological analysis and distribution studies. Cytometry A 73A: 1116-1127, 2008.
93. Zuba-Surma EK and Ratajczak MZ. Overview of very small embryonic-like stem cells (VSELs) and methodology of their identification and isolation by flow cytometric methods. Curr Protoc Cytom 9: 29, 2010.
94. Zuba-Surma EK, Wu W, Ratajczak J, Kucia M, and Ratajczak MZ. Very small embryonic-like stem cells in adult tissues: potential implications for aging. Mech Ageing Dev 130: 58-66, 2009.
95. Zuba-Surma EK, Yoshimoto M, Kucia M, Ratajczak J, Yoder M, and Ratajczak MZ. An evidence that CD45-Lin-Sca-1 + Oct4 + VSEL stem cells are embryonic remnants and are present in embryonic tissues during development. Human Gene Ther 20: 1493, 2009.