Stress as a fundamental theme in cell plasticity

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1849, Issue 4, 2015, Pages 371-377

  Shoshani, Ofer ^a   Zipori, Dov ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Cell plasticity; Dedifferentiation; Reprogramming; Stem cell; Stress; Transdifferentiation

Indexed keywords

CELL DEDIFFERENTIATION; CELL STRESS; CELL TRANSDIFFERENTIATION; IN VIVO STUDY; MAMMAL CELL; MICROENVIRONMENT; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; REVIEW; TISSUE INJURY; ANIMAL; CELL FUNCTION; HUMAN; MAMMAL; NUCLEAR REPROGRAMMING; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

MAMMALIA;

ANIMALS; CELL DEDIFFERENTIATION; CELL PHYSIOLOGICAL PHENOMENA; CELLULAR REPROGRAMMING; HUMANS; MAMMALS; STRESS, PHYSIOLOGICAL;

EID: 85028148634     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2014.07.006     Document Type: Review

References (103)

1. Aoi T., Yae K., Nakagawa M., Ichisaka T., Okita K., Takahashi K., Chiba T., Yamanaka S. Generation of pluripotent stem cells from adult mouse liver and stomach cells. Science 2008, 321:699-702.
2. Badiavas E.V., Abedi M., Butmarc J., Falanga V., Quesenberry P. Participation of bone marrow derived cells in cutaneous wound healing. J. Cell. Physiol. 2003, 196:245-250.
3. Barry E.R., Morikawa T., Butler B.L., Shrestha K., de la Rosa R., Yan K.S., Fuchs C.S., Magness S.T., Smits R., Ogino S., Kuo C.J., Camargo F.D. Restriction of intestinal stem cell expansion and the regenerative response by YAP. Nature 2013, 493:106-110.
4. Biernaskie J., Paris M., Morozova O., Fagan B.M., Marra M., Pevny L., Miller F.D. SKPs derive from hair follicle precursors and exhibit properties of adult dermal stem cells. Cell Stem Cell 2009, 5:610-623.
5. Bjornson C.R., Rietze R.L., Reynolds B.A., Magli M.C., Vescovi A.L. Turning brain into blood: a hematopoietic fate adopted by adult neural stem cells in vivo. Science 1999, 283:534-537.
6. Blanpain C., Lowry W.E., Geoghegan A., Polak L., Fuchs E. Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 2004, 118:635-648.
7. Booth B.W., Mack D.L., Androutsellis-Theotokis A., McKay R.D., Boulanger C.A., Smith G.H. The mammary microenvironment alters the differentiation repertoire of neural stem cells. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:14891-14896.
8. Boulanger C.A., Mack D.L., Booth B.W., Smith G.H. Interaction with the mammary microenvironment redirects spermatogenic cell fate in vivo. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:3871-3876.
9. Bru T., Clarke C., McGrew M.J., Sang H.M., Wilmut I., Blow J.J. Rapid induction of pluripotency genes after exposure of human somatic cells to mouse ES cell extracts. Exp. Cell Res. 2008, 314:2634-2642.
10. Buganim Y., Faddah D.A., Cheng A.W., Itskovich E., Markoulaki S., Ganz K., Klemm S.L., van Oudenaarden A., Jaenisch R. Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase. Cell 2012, 150:1209-1222.
11. Chen X., Mao Z., Liu S., Liu H., Wang X., Wu H., Wu Y., Zhao T., Fan W., Li Y., Yew D.T., Kindler P.M., Li L., He Q., Qian L., Fan M. Dedifferentiation of adult human myoblasts induced by CNTF in vitro. Mol. Biol. Cell 2005, 16:3140-3151.
12. Chong A.S., Shen J., Tao J., Yin D., Kuznetsov A., Hara M., Philipson L.H. Reversal of diabetes in non-obese diabetic mice without spleen cell-derived beta cell regeneration. Science 2006, 311(5768):1774-1775.
13. Condorelli G., Borello U., De Angelis L., Latronico M., Sirabella D., Coletta M., Galli R., Balconi G., Follenzi A., Frati G., Cusella De Angelis M.G., Gioglio L., Amuchastegui S., Adorini L., Naldini L., Vescovi A., Dejana E., Cossu G. Cardiomyocytes induce endothelial cells to trans-differentiate into cardiac muscle: implications for myocardium regeneration. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:10733-10738.
14. Conrad S., Renninger M., Hennenlotter J., Wiesner T., Just L., Bonin M., Aicher W., Buhring H.J., Mattheus U., Mack A., Wagner H.J., Minger S., Matzkies M., Reppel M., Hescheler J., Sievert K.D., Stenzl A., Skutella T. Generation of pluripotent stem cells from adult human testis. Nature 2008, 456:344-349.
15. Cumano A., Ferraz J.C., Klaine M., Di Santo J.P., Godin I. Intraembryonic, but not yolk sac hematopoietic precursors, isolated before circulation, provide long-term multilineage reconstitution. Immunity 2001, 15:477-485.
16. D'Ippolito G., Diabira S., Howard G.A., Menei P., Roos B.A., Schiller P.C. Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential. J. Cell Sci. 2004, 117:2971-2981. (Epub 2004 Jun 1).
17. Dar A., Goichberg P., Shinder V., Kalinkovich A., Kollet O., Netzer N., Margalit R., Zsak M., Nagler A., Hardan I., Resnick I., Rot A., Lapidot T. Chemokine receptor CXCR4-dependent internalization and resecretion of functional chemokine SDF-1 by bone marrow endothelial and stromal cells. Nat. Immunol. 2005, 6:1038-1046.
18. Dorrell M.I., Otani A., Aguilar E., Moreno S.K., Friedlander M. Adult bone marrow-derived stem cells use R-cadherin to target sites of neovascularization in the developing retina. Blood 2004, 103:3420-3427.
19. Efroni S., Duttagupta R., Cheng J., Dehghani H., Hoeppner D.J., Dash C., Bazett-Jones D.P., Le Grice S., McKay R.D., Buetow K.H., Gingeras T.R., Misteli T., Meshorer E. Global transcription in pluripotent embryonic stem cells. Cell Stem Cell 2008, 2:437-447.
20. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
21. Eun S.H., Shi Z., Cui K., Zhao K., Chen X. A non-cell autonomous role of E(z) to prevent germ cells from turning on a somatic cell marker. Science 2014, 343:1513-1516.
22. Faustman D.L., Tran S.D., Kodama S., Lodde B.M., Szalayova I., Key S., Toth Z.E., Mezey E. Comment on papers by Chong et al., Nishio et al., and Suri et al. on diabetes reversal in NOD mice. Science 2006, 314(5803):1243.
23. Ferrari G., Cusella-De Angelis G., Coletta M., Paolucci E., Stornaiuolo A., Cossu G., Mavilio F. Muscle regeneration by bone marrow-derived myogenic progenitors. Science 1998, 279:1528-1530.
24. Galli R., Borello U., Gritti A., Minasi M.G., Bjornson C., Coletta M., Mora M., De Angelis M.G., Fiocco R., Cossu G., Vescovi A.L. Skeletal myogenic potential of human and mouse neural stem cells. Nat. Neurosci. 2000, 3:986-991.
25. Gershengorn M.C., Hardikar A.A., Wei C., Geras-Raaka E., Marcus-Samuels B., Raaka B.M. Epithelial-to-mesenchymal transition generates proliferative human islet precursor cells. Science 2004, 306:2261-2264.
26. Guan K., Nayernia K., Maier L.S., Wagner S., Dressel R., Lee J.H., Nolte J., Wolf F., Li M., Engel W., Hasenfuss G. Pluripotency of spermatogonial stem cells from adult mouse testis. Nature 2006, 440:1199-1203.
27. Gurdon J.B., Elsdale T.R., Fischberg M. Sexually mature individuals of Xenopus laevis from the transplantation of single somatic nuclei. Nature 1958, 182:64-65.
28. Gussoni E., Soneoka Y., Strickland C.D., Buzney E.A., Khan M.K., Flint A.F., Kunkel L.M., Mulligan R.C. Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 1999, 401:390-394.
29. Hakelien A.M., Gaustad K.G., Taranger C.K., Skalhegg B.S., Kuntziger T., Collas P. Long-term in vitro, cell-type-specific genome-wide reprogramming of gene expression. Exp. Cell Res. 2005, 309:32-47.
30. Halaban R., Cheng E., Zhang Y., Moellmann G., Hanlon D., Michalak M., Setaluri V., Hebert D.N. Aberrant retention of tyrosinase in the endoplasmic reticulum mediates accelerated degradation of the enzyme and contributes to the dedifferentiated phenotype of amelanotic melanoma cells. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:6210-6215.
31. Hanley S.C., Pilotte A., Massie B., Rosenberg L. Cellular origins of adult human islet in vitro dedifferentiation. Lab. Investig. 2008, 88:761-772.
32. Hay E.D., Fischman D.A. Origin of the blastema in regenerating limbs of the newt Triturus viridescens. An autoradiographic study using tritiated thymidine to follow cell proliferation and migration. Dev. Biol. 1961, 3:26-59.
33. Hess D., Li L., Martin M., Sakano S., Hill D., Strutt B., Thyssen S., Gray D.A., Bhatia M. Bone marrow-derived stem cells initiate pancreatic regeneration. Nat. Biotechnol. 2003, 21:763-770.
34. Hochedlinger K., Jaenisch R. Monoclonal mice generated by nuclear transfer from mature B and T donor cells. Nature 2002, 415:1035-1038.
35. Humpherys D., Eggan K., Akutsu H., Friedman A., Hochedlinger K., Yanagimachi R., Lander E.S., Golub T.R., Jaenisch R. Abnormal gene expression in cloned mice derived from embryonic stem cell and cumulus cell nuclei. Proc. Natl. Acad. Sci. U. S. A. 2002, 99(20):12889-12894.
36. Hussein S.M., Batada N.N., Vuoristo S., Ching R.W., Autio R., Närvä E., Ng S., Sourour M., Hämäläinen R., Olsson C., Lundin K., Mikkola M., Trokovic R., Peitz M., Brüstle O., Bazett-Jones D.P., Alitalo K., Lahesmaa R., Nagy A., Otonkoski T. Copy number variation and selection during reprogramming to pluripotency. Nature 2011, 471(7336):58-62.
37. Iskovich S., Kaminitz A., Yafe M.P., Mizrahi K., Stein J., Yaniv I., Askenasy N. Participation of adult bone marrow-derived stem cells in pancreatic regeneration: neogenesis versus endogenesis. Curr. Stem Cell Res. Ther. 2007, 2:272-279.
38. Jiang Y., Jahagirdar B.N., Reinhardt R.L., Schwartz R.E., Keene C.D., Ortiz-Gonzalez X.R., Reyes M., Lenvik T., Lund T., Blackstad M., Du J., Aldrich S., Lisberg A., Low W.C., Largaespada D.A., Verfaillie C.M. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002, 418:41-49.
39. Kai T., Spradling A. Differentiating germ cells can revert into functional stem cells in Drosophila melanogaster ovaries. Nature 2004, 428:564-569.
40. Kim K., Doi A., Wen B., Ng K., Zhao R., Cahan P., Kim J., Aryee M.J., Ji H., Ehrlich L.I., Yabuuchi A., Takeuchi A., Cunniff K.C., Hongguang H., McKinney-Freeman S., Naveiras O., Yoon T.J., Irizarry R.A., Jung N., Seita J., Hanna J., Murakami P., Jaenisch R., Weissleder R., Orkin S.H., Weissman I.L., Feinberg A.P., Daley G.Q. Epigenetic memory in induced pluripotent stem cells. Nature 2010, 467:285-290.
41. Ko K., Tapia N., Wu G., Kim J.B., Bravo M.J., Sasse P., Glaser T., Ruau D., Han D.W., Greber B., Hausdorfer K., Sebastiano V., Stehling M., Fleischmann B.K., Brustle O., Zenke M., Scholer H.R. Induction of pluripotency in adult unipotent germline stem cells. Cell Stem Cell 2009, 5:87-96.
42. Kodama S., Kühtreiber W., Fujimura S., Dale E.A., Faustman D.L. Islet regeneration during the reversal of autoimmune diabetes in NOD mice. Science 2003, 302(5648):1223-1227.
43. Kogler G., Sensken S., Airey J.A., Trapp T., Muschen M., Feldhahn N., Liedtke S., Sorg R.V., Fischer J., Rosenbaum C., Greschat S., Knipper A., Bender J., Degistirici O., Gao J., Caplan A.I., Colletti E.J., Almeida-Porada G., Muller H.W., Zanjani E., Wernet P. A new human somatic stem cell from placental cord blood with intrinsic pluripotent differentiation potential. J. Exp. Med. 2004, 200:123-135.
44. Kondo T., Raff M. Chromatin remodeling and histone modification in the conversion of oligodendrocyte precursors to neural stem cells. Genes Dev. 2004, 18:2963-2972.
45. Kossack N., Meneses J., Shefi S., Nguyen H.N., Chavez S., Nicholas C., Gromoll J., Turek P.J., Reijo-Pera R.A. Isolation and characterization of pluripotent human spermatogonial stem cell-derived cells. Stem Cells 2008, 27:138-149.
46. Krause D.S., Theise N.D., Collector M.I., Henegariu O., Hwang S., Gardner R., Neutzel S., Sharkis S.J. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 2001, 105(3):369-377.
47. Kucia M., Reca R., Campbell F.R., Zuba-Surma E., Majka M., Ratajczak J., Ratajczak M.Z. A population of very small embryonic-like (VSEL) CXCR4(+)SSEA-1(+)Oct-4+ stem cells identified in adult bone marrow. Leukemia 2006, 20:857-869.
48. Kuroda Y., Kitada M., Wakao S., Nishikawa K., Tanimura Y., Makinoshima H., Goda M., Akashi H., Inutsuka A., Niwa A., Shigemoto T., Nabeshima Y., Nakahata T., Fujiyoshi Y., Dezawa M. Unique multipotent cells in adult human mesenchymal cell populations. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:8639-8643.
49. Kusaba T., Lalli M., Kramann R., Kobayashi A., Humphreys B.D. Differentiated kidney epithelial cells repair injured proximal tubule. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:1527-1532.
50. Landsverk H.B., Hakelien A.M., Kuntziger T., Robl J.M., Skalhegg B.S., Collas P. Reprogrammed gene expression in a somatic cell-free extract. EMBO Rep. 2002, 3:384-389.
51. Lechner A., Nolan A.L., Blacken R.A., Habener J.F. Redifferentiation of insulin-secreting cells after in vitro expansion of adult human pancreatic islet tissue. Biochem. Biophys. Res. Commun. 2005, 327:581-588.
52. Levin S., Pevsner-Fischer M., Kagan S., Lifshitz H., Weinstock A., Gataulin D., Friedlander G., Zipori D. Divergent levels of LBP and TGFbeta1 in MUrine MSCs lead to heterogenic response to TLR and proinflammatory cytokine activation. Stem Cell Rev. 2014, 10:376-388.
53. Matsumoto T., Kano K., Kondo D., Fukuda N., Iribe Y., Tanaka N., Matsubara Y., Sakuma T., Satomi A., Otaki M., Ryu J., Mugishima H. Mature adipocyte-derived dedifferentiated fat cells exhibit multilineage potential. J. Cell. Physiol. 2008, 215:210-222.
54. Mayshar Y., Ben-David U., Lavon N., Biancotti J.C., Yakir B., Clark A.T., Plath K., Lowry W.E., Benvenisty N. Identification and classification of chromosomal aberrations in human induced pluripotent stem cells. Cell Stem Cell 2010, 7(4):521-531.
55. Mazumdar J., O'Brien W.T., Johnson R.S., LaManna J.C., Chavez J.C., Klein P.S., Simon M.C. O2 regulates stem cells through Wnt/beta-catenin signalling. Nat. Cell Biol. 2010, 12:1007-1013.
56. Medici D., Shore E.M., Lounev V.Y., Kaplan F.S., Kalluri R., Olsen B.R. Conversion of vascular endothelial cells into multipotent stem-like cells. Nat. Med. 2010, 16:1400-1406.
57. Mezey E., Chandross K.J., Harta G., Maki R.A., McKercher S.R. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science 2000, 290(5497):1779-1782.
58. Nakagawa T., Nabeshima Y., Yoshida S. Functional identification of the actual and potential stem cell compartments in mouse spermatogenesis. Dev. Cell 2007, 12:195-206.
59. Nicolson G.L. Organ specificity of tumor metastasis: role of preferential adhesion, invasion and growth of malignant cells at specific secondary sites. Cancer Metastasis Rev. 1988, 7:143-188.
60. Nishio J., Gaglia J.L., Turvey S.E., Campbell C., Benoist C., Mathis D. Islet recovery and reversal of murine type 1 diabetes in the absence of any infused spleen cell contribution. Science 2006, 311(5768):1775-1778.
61. Obokata H., Sasai Y., Niwa H., Kadota M., Andrabi M., Takata N., Tokoro M., Terashita Y., Yonemura S., Vacanti C.A., Wakayama T. Retraction: Bidirectional developmental potential in reprogrammed cells with acquired pluripotency. Nature 2014, 511:112.
62. Obokata H., Wakayama T., Sasai Y., Kojima K., Vacanti M.P., Niwa H., Yamato M., Vacanti C.A. Retraction: stimulus-triggered fate conversion of somatic cells into pluripotency. Nature 2014, 511:112.
63. Peled A., Petit I., Kollet O., Magid M., Ponomaryov T., Byk T., Nagler A., Ben-Hur H., Many A., Shultz L., Lider O., Alon R., Zipori D., Lapidot T. Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 1999, 283:845-848.
64. Petersen B.E., Bowen W.C., Patrene K.D., Mars W.M., Sullivan A.K., Murase N., Boggs S.S., Greenberger J.S., Goff J.P. Bone marrow as a potential source of hepatic oval cells. Science 1999, 284:1168-1170.
65. Pevsner-Fischer M., Levin S., Zipori D. The origins of mesenchymal stromal cell heterogeneity. Stem Cell Rev. 2011, 7:560-568.
66. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., Moorman M.A., Simonetti D.W., Craig S., Marshak D.R. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147.
67. Ramskold D., Luo S., Wang Y.C., Li R., Deng Q., Faridani O.R., Daniels G.A., Khrebtukova I., Loring J.F., Laurent L.C., Schroth G.P., Sandberg R. Full-length mRNA-Seq from single-cell levels of RNA and individual circulating tumor cells. Nat. Biotechnol. 2012, 30:777-782.
68. Rando T.A. Stem cells, ageing and the quest for immortality. Nature 2006, 441:1080-1086.
69. Reyes M., Verfaillie C.M. Characterization of multipotent adult progenitor cells, a subpopulation of mesenchymal stem cells. Ann. N. Y. Acad. Sci. 2001, 938:231-233. (discussion 233-5).
70. Roobrouck V.D., Vanuytsel K., Verfaillie C.M. Concise review: culture mediated changes in fate and/or potency of stem cells. Stem Cells 2011, 29:583-589.
71. Schilling T., Noth U., Klein-Hitpass L., Jakob F., Schutze N. Plasticity in adipogenesis and osteogenesis of human mesenchymal stem cells. Mol. Cell. Endocrinol. 2007, 271:1-17.
72. Sharif A., Legendre P., Prevot V., Allet C., Romao L., Studler J.M., Chneiweiss H., Junier M.P. Transforming growth factor alpha promotes sequential conversion of mature astrocytes into neural progenitors and stem cells. Oncogene 2006, 26:2695-2706.
73. Shih C.C., Weng Y., Mamelak A., LeBon T., Hu M.C., Forman S.J. Identification of a candidate human neurohematopoietic stem-cell population. Blood 2001, 98:2412-2422.
74. Shimizu K., Sugiyama S., Aikawa M., Fukumoto Y., Rabkin E., Libby P., Mitchell R.N. Host bone-marrow cells are a source of donor intimal smooth-muscle-like cells in murine aortic transplant arteriopathy. Nat. Med. 2001, 7:738-741.
75. Shoshani O., Massalha H., Shani N., Kagan S., Ravid O., Madar S., Trakhtenbrot L., Leshkowitz D., Rechavi G., Zipori D. Polyploidization of murine mesenchymal cells is associated with suppression of the long noncoding RNA H19 and reduced tumorigenicity. Cancer Res. 2012, 72:6403-6413.
76. Shoshani O., Ravid O., Massalha H., Aharonov A., Ovadya Y., Pevsner-Fischer M., Leshkowitz D., Zipori D. Cell isolation induces fate changes of bone marrow mesenchymal cells leading to loss or alternatively to acquisition of new differentiation potentials. Stem Cells 2014, 32:2008-2020.
77. Shoshani O., Zipori D. Mammalian cell dedifferentiation as a possible outcome of stress. Stem Cell Rev. 2011, 7:488-493.
78. Shoshani O., Zipori D. Transition of endothelium to cartilage and bone. Cell Stem Cell 2011, 8:10-11.
79. Sohni A., Verfaillie C.M. Multipotent adult progenitor cells. Best Pract. Res. Clin. Haematol. 2011, 24:3-11.
80. Spencer J.A., Ferraro F., Roussakis E., Klein A., Wu J., Runnels J.M., Zaher W., Mortensen L.J., Alt C., Turcotte R., Yusuf R., Cote D., Vinogradov S.A., Scadden D.T., Lin C.P. Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature 2014, 508:269-273.
81. Stange D.E., Koo B.K., Huch M., Sibbel G., Basak O., Lyubimova A., Kujala P., Bartfeld S., Koster J., Geahlen J.H., Peters P.J., van Es J.H., van de Wetering M., Mills J.C., Clevers H. Differentiated Troy+ chief cells act as reserve stem cells to generate all lineages of the stomach epithelium. Cell 2013, 155:357-368.
82. Streets A.M., Zhang X., Cao C., Pang Y., Wu X., Xiong L., Yang L., Fu Y., Zhao L., Tang F., Huang Y. Microfluidic single-cell whole-transcriptome sequencing. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:7048-7053.
83. Sugimura R., He X.C., Venkatraman A., Arai F., Box A., Semerad C., Haug J.S., Peng L., Zhong X.B., Suda T., Li L. Noncanonical Wnt signaling maintains hematopoietic stem cells in the niche. Cell 2012, 150:351-365.
84. Suri A., Calderon B., Esparza T.J., Frederick K., Bittner P., Unanue E.R. Immunological reversal of autoimmune diabetes without hematopoietic replacement of beta cells. Science 2006, 311(5768):1778-1780.
85. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
86. Tata P.R., Mou H., Pardo-Saganta A., Zhao R., Prabhu M., Law B.M., Vinarsky V., Cho J.L., Breton S., Sahay A., Medoff B.D., Rajagopal J. Dedifferentiation of committed epithelial cells into stem cells in vivo. Nature 2013, 503:218-223.
87. Tavian M., Robin C., Coulombel L., Peault B. The human embryo, but not its yolk sac, generates lympho-myeloid stem cells: mapping multipotent hematopoietic cell fate in intraembryonic mesoderm. Immunity 2001, 15:487-495.
88. Theise N.D., Krause D.S., Sharkis S. Comment on "Little evidence for developmental plasticity of adult hematopoietic stem cells". Science 2003, 299(5611):1317.
89. Thorel F., Nepote V., Avril I., Kohno K., Desgraz R., Chera S., Herrera P.L. Conversion of adult pancreatic alpha-cells to beta-cells after extreme beta-cell loss. Nature 2010, 464:1149-1154.
90. Vassilopoulos G., Wang P.R., Russell D.W. Transplanted bone marrow regenerates liver by cell fusion. Nature 2003, 422:901-904.
91. Wagers A.J., Sherwood R.I., Christensen J.L., Weissman I.L. Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 2002, 297(5590):2256-2259. (5).
92. Wakao S., Kitada M., Kuroda Y., Shigemoto T., Matsuse D., Akashi H., Tanimura Y., Tsuchiyama K., Kikuchi T., Goda M., Nakahata T., Fujiyoshi Y., Dezawa M. Multilineage-differentiating stress-enduring (Muse) cells are a primary source of induced pluripotent stem cells in human fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:9875-9880.
93. Weigel D., Jurgens G. Stem cells that make stems. Nature 2002, 415:751-754.
94. Wilmut I., Schnieke A.E., McWhir J., Kind A.J., Campbell K.H. Viable offspring derived from fetal and adult mammalian cells. Nature 1997, 385:810-813.
95. Yamashita Y.M., Mahowald A.P., Perlin J.R., Fuller M.T. Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 2007, 315:518-521.
96. Yang L., Li S., Hatch H., Ahrens K., Cornelius J.G., Petersen B.E., Peck A.B. In vitro trans-differentiation of adult hepatic stem cells into pancreatic endocrine hormone-producing cells. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:8078-8083.
97. Zipori D. Cell interactions in the bone marrow microenvironment: role of endogenous colony-stimulating activity. J. Supramol. Struct. Cell. Biochem. 1981, 17:347-357.
98. Zipori D. Regulation of hemopoiesis by cytokines that restrict options for growth and differentiation. Cancer Cells 1990, 2:205-211.
99. Zipori D. The nature of stem cells: state rather than entity. Nat. Rev. Genet. 2004, 5:873-878.
100. Zipori D. The stem state: plasticity is essential, whereas self-renewal and hierarchy are optional. Stem Cells 2005, 23:719-726.
101. Zipori D. Biology of Stem Cells and the Molecular Basis of the Stem State 2009, Humana Press (Springer), (e-ISBN 978-1-60761-130-1).
102. Zipori D., Sasson T. Adherent cells from mouse bone marrow inhibit the formation of colony stimulating factor (CSF) induced myeloid colonies. Exp. Hematol. 1980, 8:816-817.
103. Zuba-Surma E.K., Ratajczak M.Z. Overview of very small embryonic-like stem cells (VSELs) and methodology of their identification and isolation by flow cytometric methods. Curr. Protoc. Cytom. 2010, 51. 9.29.1-15 (Chapter 9:Unit9 29).