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Published in: Clinical and Translational Medicine 1/2014

Open Access 01-12-2014 | Review

Pluripotent muse cells derived from human adipose tissue: a new perspective on regenerative medicine and cell therapy

Authors: Ariel A Simerman, Daniel A Dumesic, Gregorio D Chazenbalk

Published in: Clinical and Translational Medicine | Issue 1/2014

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Abstract

In 2010, Multilineage Differentiating Stress Enduring (Muse) cells were introduced to the scientific community, offering potential resolution to the issue of teratoma formation that plagues both embryonic stem (ES) and induced pluripotent (iPS) stem cells. Isolated from human bone marrow, dermal fibroblasts, adipose tissue and commercially available adipose stem cells (ASCs) under severe cellular stress conditions, Muse cells self-renew in a controlled manner and do not form teratomas when injected into immune-deficient mice. Furthermore, Muse cells express classic pluripotency markers and differentiate into cells from the three embryonic germ layers both spontaneously and under media-specific induction. When transplanted in vivo, Muse cells contribute to tissue generation and repair. This review delves into the aspects of Muse cells that set them apart from ES, iPS, and various reported adult pluripotent stem cell lines, with specific emphasis on Muse cells derived from adipose tissue (Muse-AT), and their potential to revolutionize the field of regenerative medicine and stem cell therapy.
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Literature
1.
go back to reference Evans MJ, Kaufman MH: Establishment in culture of pluripotential cells from mouse embryos. Nature 1981, 292(5819):154–156. 10.1038/292154a0CrossRefPubMed Evans MJ, Kaufman MH: Establishment in culture of pluripotential cells from mouse embryos. Nature 1981, 292(5819):154–156. 10.1038/292154a0CrossRefPubMed
2.
go back to reference Martin GR: Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A 1981, 78(12):7634–7638. 10.1073/pnas.78.12.7634PubMedCentralCrossRefPubMed Martin GR: Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A 1981, 78(12):7634–7638. 10.1073/pnas.78.12.7634PubMedCentralCrossRefPubMed
3.
go back to reference Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM: Embryonic stem cell lines derived from human blastocysts. Science 1998, 282(5391):1145–1147.CrossRefPubMed Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM: Embryonic stem cell lines derived from human blastocysts. Science 1998, 282(5391):1145–1147.CrossRefPubMed
4.
go back to reference Przyborski SA: Differentiation of human embryonic stem cells after transplantation in immune-deficient mice. Stem Cells 2005, 23(9):1242–1250. 10.1634/stemcells.2005-0014CrossRefPubMed Przyborski SA: Differentiation of human embryonic stem cells after transplantation in immune-deficient mice. Stem Cells 2005, 23(9):1242–1250. 10.1634/stemcells.2005-0014CrossRefPubMed
5.
go back to reference Maherali N, Sridharan R, Xie W, Utikal J, Eminli S, Arnold K, Stadtfeld M, Yachechko R, Tchieu J, Jaenisch R, Plath K, Hochedlinger K: Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell 2007, 1(1):55–70. 10.1016/j.stem.2007.05.014CrossRefPubMed Maherali N, Sridharan R, Xie W, Utikal J, Eminli S, Arnold K, Stadtfeld M, Yachechko R, Tchieu J, Jaenisch R, Plath K, Hochedlinger K: Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell 2007, 1(1):55–70. 10.1016/j.stem.2007.05.014CrossRefPubMed
6.
go back to reference Takahashi K, Yamanaka S: Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126(4):663–676. 10.1016/j.cell.2006.07.024CrossRefPubMed Takahashi K, Yamanaka S: Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126(4):663–676. 10.1016/j.cell.2006.07.024CrossRefPubMed
7.
8.
go back to reference Power C, Rasko JE: Promises and challenges of stem cell research for regenerative medicine. Ann Intern Med 2011, 155(10):706–713. W217 W217 10.7326/0003-4819-155-10-201111150-00010CrossRefPubMed Power C, Rasko JE: Promises and challenges of stem cell research for regenerative medicine. Ann Intern Med 2011, 155(10):706–713. W217 W217 10.7326/0003-4819-155-10-201111150-00010CrossRefPubMed
9.
10.
go back to reference Fong CY, Gauthaman K, Bongso A: Teratomas from pluripotent stem cells: A clinical hurdle. J Cell Biochem 2010, 111(4):769–781. 10.1002/jcb.22775CrossRefPubMed Fong CY, Gauthaman K, Bongso A: Teratomas from pluripotent stem cells: A clinical hurdle. J Cell Biochem 2010, 111(4):769–781. 10.1002/jcb.22775CrossRefPubMed
11.
go back to reference Geng YJ: Molecular mechanisms for cardiovascular stem cell apoptosis and growth in the hearts with atherosclerotic coronary disease and ischemic heart failure. Ann N Y Acad Sci 2003, 1010: 687–697. 10.1196/annals.1299.126CrossRefPubMed Geng YJ: Molecular mechanisms for cardiovascular stem cell apoptosis and growth in the hearts with atherosclerotic coronary disease and ischemic heart failure. Ann N Y Acad Sci 2003, 1010: 687–697. 10.1196/annals.1299.126CrossRefPubMed
12.
go back to reference Hanna J, Saha K, Pando B, van Zon J, Lengner CJ, Creyghton MP, van Oudenaarden A, Jaenisch R: Direct cell reprogramming is a stochastic process amenable to acceleration. Nature 2009, 462(7273):595–601. 10.1038/nature08592PubMedCentralCrossRefPubMed Hanna J, Saha K, Pando B, van Zon J, Lengner CJ, Creyghton MP, van Oudenaarden A, Jaenisch R: Direct cell reprogramming is a stochastic process amenable to acceleration. Nature 2009, 462(7273):595–601. 10.1038/nature08592PubMedCentralCrossRefPubMed
13.
go back to reference Kim J, Woo AJ, Chu J, Snow JW, Fujiwara Y, Kim CG, Cantor AB, Orkin SH: A Myc network accounts for similarities between embryonic stem and cancer cell transcription programs. Cell 2010, 143(2):313–324. 10.1016/j.cell.2010.09.010PubMedCentralCrossRefPubMed Kim J, Woo AJ, Chu J, Snow JW, Fujiwara Y, Kim CG, Cantor AB, Orkin SH: A Myc network accounts for similarities between embryonic stem and cancer cell transcription programs. Cell 2010, 143(2):313–324. 10.1016/j.cell.2010.09.010PubMedCentralCrossRefPubMed
14.
go back to reference Smith ZD, Nachman I, Regev A, Meissner A: Dynamic single-cell imaging of direct reprogramming reveals an early specifying event. Nat Biotechnol 2010, 28(5):521–526. 10.1038/nbt.1632PubMedCentralCrossRefPubMed Smith ZD, Nachman I, Regev A, Meissner A: Dynamic single-cell imaging of direct reprogramming reveals an early specifying event. Nat Biotechnol 2010, 28(5):521–526. 10.1038/nbt.1632PubMedCentralCrossRefPubMed
15.
go back to reference Kim D, Kim CH, Moon JI, Chung YG, Chang MY, Han BS, Ko S, Yang E, Cha KY, Lanza R, Kim KS: Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 2009, 4(6):472–476. 10.1016/j.stem.2009.05.005PubMedCentralCrossRefPubMed Kim D, Kim CH, Moon JI, Chung YG, Chang MY, Han BS, Ko S, Yang E, Cha KY, Lanza R, Kim KS: Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 2009, 4(6):472–476. 10.1016/j.stem.2009.05.005PubMedCentralCrossRefPubMed
16.
go back to reference 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(5928):797–801. 10.1126/science.1172482PubMedCentralCrossRefPubMed 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(5928):797–801. 10.1126/science.1172482PubMedCentralCrossRefPubMed
17.
go back to reference Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du J, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM: Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002, 418(6893):41–49. 10.1038/nature00870CrossRefPubMed Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du J, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM: Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002, 418(6893):41–49. 10.1038/nature00870CrossRefPubMed
18.
go back to reference Dimomeletis I, Deindl E, Zaruba M, Groebner M, Zahler S, Laslo SM, David R, Kostin S, Deutsch MA, Assmann G, Mueller-Hoecker J, Feuring-Buske M, Franz WM: Assessment of human MAPCs for stem cell transplantation and cardiac regeneration after myocardial infarction in SCID mice. Exp Hematol 2010, 38(11):1105–1114. 10.1016/j.exphem.2010.06.013CrossRefPubMed Dimomeletis I, Deindl E, Zaruba M, Groebner M, Zahler S, Laslo SM, David R, Kostin S, Deutsch MA, Assmann G, Mueller-Hoecker J, Feuring-Buske M, Franz WM: Assessment of human MAPCs for stem cell transplantation and cardiac regeneration after myocardial infarction in SCID mice. Exp Hematol 2010, 38(11):1105–1114. 10.1016/j.exphem.2010.06.013CrossRefPubMed
19.
go back to reference Kucia M, Zuba-Surma EK, Wysoczynski M, Wu W, Ratajczak J, Machalinski B, Ratajczak MZ: Adult marrow-derived very small embryonic-like stem cells and tissue engineering. Expert Opin Biol Ther 2007, 7(10):1499–1514. 10.1517/14712598.7.10.1499CrossRefPubMed Kucia M, Zuba-Surma EK, Wysoczynski M, Wu W, Ratajczak J, Machalinski B, Ratajczak MZ: Adult marrow-derived very small embryonic-like stem cells and tissue engineering. Expert Opin Biol Ther 2007, 7(10):1499–1514. 10.1517/14712598.7.10.1499CrossRefPubMed
20.
go back to reference Santourlidis S, Wernet P, Ghanjati F, Graffmann N, Springer J, Kriegs C, Zhao X, Brands J, Arauzo-Bravo MJ, Neves R, Koegler G, Uhrberg M: Unrestricted somatic stem cells (USSC) from human umbilical cord blood display uncommitted epigenetic signatures of the major stem cell pluripotency genes. Stem Cell Res 2011, 6(1):60–69. 10.1016/j.scr.2010.08.003CrossRefPubMed Santourlidis S, Wernet P, Ghanjati F, Graffmann N, Springer J, Kriegs C, Zhao X, Brands J, Arauzo-Bravo MJ, Neves R, Koegler G, Uhrberg M: Unrestricted somatic stem cells (USSC) from human umbilical cord blood display uncommitted epigenetic signatures of the major stem cell pluripotency genes. Stem Cell Res 2011, 6(1):60–69. 10.1016/j.scr.2010.08.003CrossRefPubMed
21.
go back to reference Miyanishi M, Mori Y, Seita J, Chen JY, Karten S, Chan CK, Nakauchi H, Weissman IL: Do pluripotent stem cells exist in adult mice as very small embryonic stem cells? Stem Cell Reports 2013, 1(2):198–208. 10.1016/j.stemcr.2013.07.001PubMedCentralCrossRefPubMed Miyanishi M, Mori Y, Seita J, Chen JY, Karten S, Chan CK, Nakauchi H, Weissman IL: Do pluripotent stem cells exist in adult mice as very small embryonic stem cells? Stem Cell Reports 2013, 1(2):198–208. 10.1016/j.stemcr.2013.07.001PubMedCentralCrossRefPubMed
22.
go back to reference Prockop DJ: Repair of tissues by adult stem/progenitor cells (MSCs): controversies, myths, and changing paradigms. Mol Ther 2009, 17(6):939–946. 10.1038/mt.2009.62PubMedCentralCrossRefPubMed Prockop DJ: Repair of tissues by adult stem/progenitor cells (MSCs): controversies, myths, and changing paradigms. Mol Ther 2009, 17(6):939–946. 10.1038/mt.2009.62PubMedCentralCrossRefPubMed
23.
go back to reference Obokata H, Wakayama T, Sasai Y, Kojima K, Vacanti MP, Niwa H, Yamato M, Vacanti CA: Stimulus-triggered fate conversion of somatic cells into pluripotency. Nature 2014, 505(7485):641–647. 10.1038/nature12968CrossRefPubMed Obokata H, Wakayama T, Sasai Y, Kojima K, Vacanti MP, Niwa H, Yamato M, Vacanti CA: Stimulus-triggered fate conversion of somatic cells into pluripotency. Nature 2014, 505(7485):641–647. 10.1038/nature12968CrossRefPubMed
24.
go back to reference 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, Nabeshima Y, Fujiyoshi Y, Dezawa M: Unique multipotent cells in adult human mesenchymal cell populations. Proc Natl Acad Sci U S A 2010, 107(19):8639–8643. 10.1073/pnas.0911647107PubMedCentralCrossRefPubMed 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, Nabeshima Y, Fujiyoshi Y, Dezawa M: Unique multipotent cells in adult human mesenchymal cell populations. Proc Natl Acad Sci U S A 2010, 107(19):8639–8643. 10.1073/pnas.0911647107PubMedCentralCrossRefPubMed
25.
go back to reference 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(24):9875–9880. 10.1073/pnas.1100816108PubMedCentralCrossRefPubMed 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(24):9875–9880. 10.1073/pnas.1100816108PubMedCentralCrossRefPubMed
26.
go back to reference Heneidi S, Simerman AA, Keller E, Singh P, Li X, Dumesic DA, Chazenbalk G: Awakened by cellular stress: isolation and characterization of a novel population of pluripotent stem cells derived from human adipose tissue. PLoS One 2013, 8(6):e64752. 10.1371/journal.pone.0064752PubMedCentralCrossRefPubMed Heneidi S, Simerman AA, Keller E, Singh P, Li X, Dumesic DA, Chazenbalk G: Awakened by cellular stress: isolation and characterization of a novel population of pluripotent stem cells derived from human adipose tissue. PLoS One 2013, 8(6):e64752. 10.1371/journal.pone.0064752PubMedCentralCrossRefPubMed
27.
go back to reference Ogura F, Wakao S, Kuroda Y, Tsuchiyama K, Bagheri M, Heneidi S, Chazenbalk G, Aiba S, Dezawa M: Human adipose tissue possesses a unique population of pluripotent stem cells with non-tumorigenic and low telomerase activities: potential implications in regenerative medicine. Stem Cells Dev 2013, 23(7):717.CrossRef Ogura F, Wakao S, Kuroda Y, Tsuchiyama K, Bagheri M, Heneidi S, Chazenbalk G, Aiba S, Dezawa M: Human adipose tissue possesses a unique population of pluripotent stem cells with non-tumorigenic and low telomerase activities: potential implications in regenerative medicine. Stem Cells Dev 2013, 23(7):717.CrossRef
28.
go back to reference Tsuchiyama K, Wakao S, Kuroda Y, Ogura F, Nojima M, Sawaya N, Yamasaki K, Aiba S, Dezawa M: Functional melanocytes are readily reprogrammable from multilineage-differentiating stress-enduring (muse) cells, distinct stem cells in human fibroblasts. J Invest Dermatol 2013, 133(10):2425–2435. 10.1038/jid.2013.172CrossRefPubMed Tsuchiyama K, Wakao S, Kuroda Y, Ogura F, Nojima M, Sawaya N, Yamasaki K, Aiba S, Dezawa M: Functional melanocytes are readily reprogrammable from multilineage-differentiating stress-enduring (muse) cells, distinct stem cells in human fibroblasts. J Invest Dermatol 2013, 133(10):2425–2435. 10.1038/jid.2013.172CrossRefPubMed
29.
go back to reference Wesselschmidt RL: The teratoma assay: an in vivo assessment of pluripotency. Methods Mol Biol 2011, 767: 231–241. 10.1007/978-1-61779-201-4_17CrossRefPubMed Wesselschmidt RL: The teratoma assay: an in vivo assessment of pluripotency. Methods Mol Biol 2011, 767: 231–241. 10.1007/978-1-61779-201-4_17CrossRefPubMed
30.
go back to reference Ben-David U, Benvenisty N: The tumorigenicity of human embryonic and induced pluripotent stem cells. Nat Rev Cancer 2011, 11(4):268–277. 10.1038/nrc3034CrossRefPubMed Ben-David U, Benvenisty N: The tumorigenicity of human embryonic and induced pluripotent stem cells. Nat Rev Cancer 2011, 11(4):268–277. 10.1038/nrc3034CrossRefPubMed
31.
go back to reference Gutierrez-Aranda I, Ramos-Mejia V, Bueno C, Munoz-Lopez M, Real PJ, Macia A, Sanchez L, Ligero G, Garcia-Parez JL, Menendez P: Human induced pluripotent stem cells develop teratoma more efficiently and faster than human embryonic stem cells regardless the site of injection. Stem Cells 2010, 28(9):1568–1570. 10.1002/stem.471PubMedCentralCrossRefPubMed Gutierrez-Aranda I, Ramos-Mejia V, Bueno C, Munoz-Lopez M, Real PJ, Macia A, Sanchez L, Ligero G, Garcia-Parez JL, Menendez P: Human induced pluripotent stem cells develop teratoma more efficiently and faster than human embryonic stem cells regardless the site of injection. Stem Cells 2010, 28(9):1568–1570. 10.1002/stem.471PubMedCentralCrossRefPubMed
32.
go back to reference Lee AS, Tang C, Rao MS, Weissman IL, Wu JC: Tumorigenicity as a clinical hurdle for pluripotent stem cell therapies. Nat Med 2013, 19(8):998–1004. 10.1038/nm.3267PubMedCentralCrossRefPubMed Lee AS, Tang C, Rao MS, Weissman IL, Wu JC: Tumorigenicity as a clinical hurdle for pluripotent stem cell therapies. Nat Med 2013, 19(8):998–1004. 10.1038/nm.3267PubMedCentralCrossRefPubMed
33.
go back to reference Ohm JE, Mali P, Van Neste L, Berman DM, Liang L, Pandiyan K, Briggs KJ, Zhang W, Argani P, Simons B, Yu W, Matsui W, Van Criekinge W, Rassool FV, Zambidis E, Schuebel KE, Cope L, Yen J, Mohammad HP, Cheng L, Baylin SB: Cancer-related epigenome changes associated with reprogramming to induced pluripotent stem cells. Cancer Res 2010, 70(19):7662–7673. 10.1158/0008-5472.CAN-10-1361PubMedCentralCrossRefPubMed Ohm JE, Mali P, Van Neste L, Berman DM, Liang L, Pandiyan K, Briggs KJ, Zhang W, Argani P, Simons B, Yu W, Matsui W, Van Criekinge W, Rassool FV, Zambidis E, Schuebel KE, Cope L, Yen J, Mohammad HP, Cheng L, Baylin SB: Cancer-related epigenome changes associated with reprogramming to induced pluripotent stem cells. Cancer Res 2010, 70(19):7662–7673. 10.1158/0008-5472.CAN-10-1361PubMedCentralCrossRefPubMed
34.
go back to reference Gentile L, Cebria F, Bartscherer K: The planarian flatworm: an in vivo model for stem cell biology and nervous system regeneration. Dis Model Mech 2011, 4(1):12–19. 10.1242/dmm.006692PubMedCentralCrossRefPubMed Gentile L, Cebria F, Bartscherer K: The planarian flatworm: an in vivo model for stem cell biology and nervous system regeneration. Dis Model Mech 2011, 4(1):12–19. 10.1242/dmm.006692PubMedCentralCrossRefPubMed
36.
go back to reference Marson A, Levine SS, Cole MF, Frampton GM, Brambrink T, Johnstone S, Guenther MG, Johnston WK, Wernig M, Newman J, Calabrese JM, Dennis LM, Volkert TL, Gupta S, Love J, Hannett N, Sharp PA, Bartel DP, Jaenisch R, Young RA: Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 2008, 134(3):521–533. 10.1016/j.cell.2008.07.020PubMedCentralCrossRefPubMed Marson A, Levine SS, Cole MF, Frampton GM, Brambrink T, Johnstone S, Guenther MG, Johnston WK, Wernig M, Newman J, Calabrese JM, Dennis LM, Volkert TL, Gupta S, Love J, Hannett N, Sharp PA, Bartel DP, Jaenisch R, Young RA: Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 2008, 134(3):521–533. 10.1016/j.cell.2008.07.020PubMedCentralCrossRefPubMed
37.
38.
go back to reference Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH: Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001, 7(2):211–228. 10.1089/107632701300062859CrossRefPubMed Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH: Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001, 7(2):211–228. 10.1089/107632701300062859CrossRefPubMed
39.
go back to reference Chazenbalk G, Bertolotto C, Heneidi S, Jumabay M, Trivax B, Aronowitz J, Yoshimura K, Simmons CF, Dumesic DA, Azziz R: Novel pathway of adipogenesis through cross-talk between adipose tissue macrophages, adipose stem cells and adipocytes: evidence of cell plasticity. PLoS One 2011, 6(3):e17834. 10.1371/journal.pone.0017834PubMedCentralCrossRefPubMed Chazenbalk G, Bertolotto C, Heneidi S, Jumabay M, Trivax B, Aronowitz J, Yoshimura K, Simmons CF, Dumesic DA, Azziz R: Novel pathway of adipogenesis through cross-talk between adipose tissue macrophages, adipose stem cells and adipocytes: evidence of cell plasticity. PLoS One 2011, 6(3):e17834. 10.1371/journal.pone.0017834PubMedCentralCrossRefPubMed
40.
go back to reference Kultz D: Molecular and evolutionary basis of the cellular stress response. Annu Rev Physiol 2005, 67: 225–257. 10.1146/annurev.physiol.67.040403.103635CrossRefPubMed Kultz D: Molecular and evolutionary basis of the cellular stress response. Annu Rev Physiol 2005, 67: 225–257. 10.1146/annurev.physiol.67.040403.103635CrossRefPubMed
41.
go back to reference Meier P, Finch A, Evan G: Apoptosis in development. Nature 2000, 407(6805):796–801. 10.1038/35037734CrossRefPubMed Meier P, Finch A, Evan G: Apoptosis in development. Nature 2000, 407(6805):796–801. 10.1038/35037734CrossRefPubMed
42.
go back to reference Blanpain C, Lowry WE, 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(5):635–648. 10.1016/j.cell.2004.08.012CrossRefPubMed Blanpain C, Lowry WE, 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(5):635–648. 10.1016/j.cell.2004.08.012CrossRefPubMed
44.
go back to reference Huang J, Zhang Z, Guo J, Ni A, Deb A, Zhang L, Mirotsou M, Pratt RE, Dzau VJ: Genetic modification of mesenchymal stem cells overexpressing CCR1 increases cell viability, migration, engraftment, and capillary density in the injured myocardium. Circ Res 2010, 106(11):1753–1762. 10.1161/CIRCRESAHA.109.196030PubMedCentralCrossRefPubMed Huang J, Zhang Z, Guo J, Ni A, Deb A, Zhang L, Mirotsou M, Pratt RE, Dzau VJ: Genetic modification of mesenchymal stem cells overexpressing CCR1 increases cell viability, migration, engraftment, and capillary density in the injured myocardium. Circ Res 2010, 106(11):1753–1762. 10.1161/CIRCRESAHA.109.196030PubMedCentralCrossRefPubMed
45.
go back to reference Vasiliou V, Nebert DW: Analysis and update of the human aldehyde dehydrogenase (ALDH) gene family. Hum Genomics 2005, 2(2):138–143.PubMedCentralPubMed Vasiliou V, Nebert DW: Analysis and update of the human aldehyde dehydrogenase (ALDH) gene family. Hum Genomics 2005, 2(2):138–143.PubMedCentralPubMed
46.
go back to reference Dayem AA, Choi HY, Kim JH, Cho SG: Role of oxidative stress in stem, cancer, and cancer stem cells. Cancers (Basel) 2010, 2(2):859–884. 10.3390/cancers2020859CrossRef Dayem AA, Choi HY, Kim JH, Cho SG: Role of oxidative stress in stem, cancer, and cancer stem cells. Cancers (Basel) 2010, 2(2):859–884. 10.3390/cancers2020859CrossRef
47.
go back to reference Hodgetts SI, Beilharz MW, Scalzo AA, Grounds MD: Why do cultured transplanted myoblasts die in vivo? DNA quantification shows enhanced survival of donor male myoblasts in host mice depleted of CD4+ and CD8+ cells or Nk1.1+ cells. Cell Transplant 2000, 9(4):489–502.PubMed Hodgetts SI, Beilharz MW, Scalzo AA, Grounds MD: Why do cultured transplanted myoblasts die in vivo? DNA quantification shows enhanced survival of donor male myoblasts in host mice depleted of CD4+ and CD8+ cells or Nk1.1+ cells. Cell Transplant 2000, 9(4):489–502.PubMed
48.
go back to reference Hofmann M, Wollert KC, Meyer GP, Menke A, Arseniev L, Hertenstein B, Ganser A, Knapp WH, Drexler H: Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation 2005, 111(17):2198–2202. 10.1161/01.CIR.0000163546.27639.AACrossRefPubMed Hofmann M, Wollert KC, Meyer GP, Menke A, Arseniev L, Hertenstein B, Ganser A, Knapp WH, Drexler H: Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation 2005, 111(17):2198–2202. 10.1161/01.CIR.0000163546.27639.AACrossRefPubMed
50.
go back to reference Oh JS, Kim KN, An SS, Pennant WA, Kim HJ, Gwak SJ, Yoon Do H, Lim MH, Choi BH, Ha Y: Cotransplantation of mouse neural stem cells (mNSCs) with adipose tissue-derived mesenchymal stem cells improves mNSC survival in a rat spinal cord injury model. Cell Transplant 2010, 20(6):837–849.CrossRefPubMed Oh JS, Kim KN, An SS, Pennant WA, Kim HJ, Gwak SJ, Yoon Do H, Lim MH, Choi BH, Ha Y: Cotransplantation of mouse neural stem cells (mNSCs) with adipose tissue-derived mesenchymal stem cells improves mNSC survival in a rat spinal cord injury model. Cell Transplant 2010, 20(6):837–849.CrossRefPubMed
51.
go back to reference Abdollahi H, Harris LJ, Zhang P, McIlhenny S, Srinivas V, Tulenko T, DiMuzio PJ: The role of hypoxia in stem cell differentiation and therapeutics. J Surg Res 2009, 165(1):112–117.PubMedCentralCrossRefPubMed Abdollahi H, Harris LJ, Zhang P, McIlhenny S, Srinivas V, Tulenko T, DiMuzio PJ: The role of hypoxia in stem cell differentiation and therapeutics. J Surg Res 2009, 165(1):112–117.PubMedCentralCrossRefPubMed
52.
go back to reference Chacko SM, Ahmed S, Selvendiran K, Kuppusamy ML, Khan M, Kuppusamy P: Hypoxic preconditioning induces the expression of prosurvival and proangiogenic markers in mesenchymal stem cells. Am J Physiol Cell Physiol 2010, 299(6):C1562-C1570. 10.1152/ajpcell.00221.2010PubMedCentralCrossRefPubMed Chacko SM, Ahmed S, Selvendiran K, Kuppusamy ML, Khan M, Kuppusamy P: Hypoxic preconditioning induces the expression of prosurvival and proangiogenic markers in mesenchymal stem cells. Am J Physiol Cell Physiol 2010, 299(6):C1562-C1570. 10.1152/ajpcell.00221.2010PubMedCentralCrossRefPubMed
53.
go back to reference Eliasson P, Rehn M, Hammar P, Larsson P, Sirenko O, Flippin LA, Cammenga J, Jonsson JI: Hypoxia mediates low cell-cycle activity and increases the proportion of long-term-reconstituting hematopoietic stem cells during in vitro culture. Exp Hematol 2010, 38(4):301–310. e2 e2 10.1016/j.exphem.2010.01.005CrossRefPubMed Eliasson P, Rehn M, Hammar P, Larsson P, Sirenko O, Flippin LA, Cammenga J, Jonsson JI: Hypoxia mediates low cell-cycle activity and increases the proportion of long-term-reconstituting hematopoietic stem cells during in vitro culture. Exp Hematol 2010, 38(4):301–310. e2 e2 10.1016/j.exphem.2010.01.005CrossRefPubMed
Metadata
Title
Pluripotent muse cells derived from human adipose tissue: a new perspective on regenerative medicine and cell therapy
Authors
Ariel A Simerman
Daniel A Dumesic
Gregorio D Chazenbalk
Publication date
01-12-2014
Publisher
Springer Berlin Heidelberg
Published in
Clinical and Translational Medicine / Issue 1/2014
Electronic ISSN: 2001-1326
DOI
https://doi.org/10.1186/2001-1326-3-12

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