Awakened by Cellular Stress: Isolation and Characterization of a Novel Population of Pluripotent Stem Cells Derived from Human Adipose Tissue

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Heneidi, Saleh ^a   Simerman, Ariel A ^b   Keller, Erica ^b   Singh, Prapti ^b   Li, Xinmin ^b   Dumesic, Daniel A ^b   Chazenbalk, Gregorio ^b  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGENASE; CYTOKERATIN 7; NESTIN; NUCLEIC ACID BINDING PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN TR 1 60; STAGE SPECIFIC EMBRYO ANTIGEN 3; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR REX1; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; DIFFERENTIATION ANTIGEN; TRANSCRIPTOME;

ADIPOSE DERIVED STEM CELL; ADIPOSE TISSUE; ARTICLE; CARCINOGENICITY; CELL CYCLE REGULATION; CELL DEATH; CELL DIFFERENTIATION; CELL HOMING; CELL HYPOXIA; CELL ISOLATION; CELL LINEAGE; CELL POPULATION; CELL PROLIFERATION; CELL RENEWAL; CELL SELECTION; CELL STRESS; CELL SURVIVAL; DNA REPAIR; DNA REPLICATION; DOWN REGULATION; EMBRYO DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; LONG TERM EXPOSURE; LOW TEMPERATURE; MICROARRAY ANALYSIS; MULTILINEAGE DIFFERENTIATING STRESS ENDURING CELL; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; REGENERATIVE MEDICINE; STEM CELL TRANSPLANTATION; UPREGULATION; ABDOMINAL SUBCUTANEOUS FAT; CELL CULTURE; CELL SHAPE; CULTURE TECHNIQUE; CYTOLOGY; DNA MICROARRAY; ECTODERM; ENDODERM; GENETICS; LIVER CELL; MESODERM; METABOLISM; NERVE CELL; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SMOOTH MUSCLE FIBER;

ANTIGENS, DIFFERENTIATION; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL SHAPE; CELLS, CULTURED; ECTODERM; ENDODERM; FEMALE; HEPATOCYTES; HUMANS; MESODERM; MYOCYTES, SMOOTH MUSCLE; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLURIPOTENT STEM CELLS; REGENERATIVE MEDICINE; STRESS, PHYSIOLOGICAL; SUBCUTANEOUS FAT, ABDOMINAL; TRANSCRIPTOME; UP-REGULATION;

EID: 84878752151     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064752     Document Type: Article

References (67)

1. Dayen AA, Choi H, Kim J, Cho S, (2010) Role of Oxidate Stress in Stem, Cancer, and Cancer Stem Cells. Cancers 2: 859-884.
2. Fulda S, Gorman AM, Hori O, Samali A (2009) Cellular Stress Responses: Cell Survival and Cell Death. International Journal of Cell Biology 2010.
3. Hodgetts SI, Beilharz MW, Scalzo AA, Grounds MD, (2000) 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 9: 489-502.
4. Oh JS, Kim KN, An SS, Pennant WA, Kim HJ, et al. (2010) 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 20: 837-849.
5. Mingliang R, Bo Z, Zhengguo W, (2011) Stem cells for cardiac repair: status, mechanisms, and new strategies. Stem Cells Int 2011: 310928.
6. Hofmann M, Wollert KC, Meyer GP, Menke A, Arseniev L, et al. (2005) Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation 111: 2198-2202.
7. Kultz D, (2005) Molecular and evolutionary basis of the cellular stress response. Annu Rev Physiol 67: 225-257.
8. Chacko SM, Ahmed S, Selvendiran K, Kuppusamy ML, Khan M, et al. (2010) Hypoxic preconditioning induces the expression of prosurvival and proangiogenic markers in mesenchymal stem cells. Am J Physiol Cell Physiol 299: C1562-1570.
9. Csete M, (2005) Oxygen in the cultivation of stem cells. Ann N Y Acad Sci 1049: 1-8.
10. Grayson WL, Zhao F, Bunnell B, Ma T, (2007) Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophys Res Commun 358: 948-953.
11. Abdollahi H, Harris LJ, Zhang P, McIlhenny S, Srinivas V, et al. (2009) The role of hypoxia in stem cell differentiation and therapeutics. J Surg Res 165: 112-117.
12. Eliasson P, Rehn M, Hammar P, Larsson P, Sirenko O, et al. (2010) Hypoxia mediates low cell-cycle activity and increases the proportion of long-term-reconstituting hematopoietic stem cells during in vitro culture. Exp Hematol 38: 301-310 e302.
13. Kuroda Y, Kitada M, Wakao S, Nishikawa K, Tanimura Y, et al. (2010) Unique multipotent cells in adult human mesenchymal cell populations. Proc Natl Acad Sci U S A 107: 8639-8643.
14. Wakao S, Kitada M, Kuroda Y, Shigemoto T, Matsuse D, et al. (2011) 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 108: 9875-9880.
15. Gimble JM, Katz AJ, Bunnell BA, (2007) Adipose-derived stem cells for regenerative medicine. Circ Res 100: 1249-1260.
16. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, et al. (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13: 4279-4295.
17. Hristov M, Zernecke A, Bidzhekov K, Liehn EA, Shagdarsuren E, et al. (2007) Importance of CXC chemokine receptor 2 in the homing of human peripheral blood endothelial progenitor cells to sites of arterial injury. Circ Res 100: 590-597.
18. Oyagi S, Hirose M, Kojima M, Okuyama M, Kawase M, et al. (2006) Therapeutic effect of transplanting HGF-treated bone marrow mesenchymal cells into CCl4-injured rats. J Hepatol 44: 742-748.
19. Hermann A, Gastl R, Liebau S, Popa MO, Fiedler J, et al. (2004) Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells. J Cell Sci 117: 4411-4422.
20. Di Rocco G, Iachininoto MG, Tritarelli A, Straino S, Zacheo A, et al. (2006) Myogenic potential of adipose-tissue-derived cells. J Cell Sci 119: 2945-2952.
21. Chazenbalk G, Bertolotto C, Heneidi S, Jumabay M, Trivax B, et al. (2011) Novel pathway of adipogenesis through cross-talk between adipose tissue macrophages, adipose stem cells and adipocytes: evidence of cell plasticity. PLoS One 6: e17834.
22. Listenberger LL, Brown DA (2007) Fluorescent detection of lipid droplets and associated proteins. Curr Protoc Cell Biol Chapter 24: Unit 24 22.
23. Sarugaser R, Hanoun L, Keating A, Stanford WL, Davies JE, (2009) Human mesenchymal stem cells self-renew and differentiate according to a deterministic hierarchy. PLoS One 4: e6498.
24. Beier JP, Bitto FF, Lange C, Klumpp D, Arkudas A, et al. (2011) Myogenic differentiation of mesenchymal stem cells co-cultured with primary myoblasts. Cell Biol Int 35: 397-406.
25. Fink T, Zachar V, (2011) Adipogenic differentiation of human mesenchymal stem cells. Methods Mol Biol 698: 243-251.
26. Bunnell BA, Flaat M, Gagliardi C, Patel B, Ripoll C, (2008) Adipose-derived stem cells: isolation, expansion and differentiation Methods. 45: 115-120.
27. Kuhlmann WD, Peschke P, (2006) Hepatic progenitor cells, stem cells, and AFP expression in models of liver injury. Int J Exp Pathol 87: 343-359.
28. Carlini P, Ferranti P, Polizio F, Ciriolo MR, Rotilio G, (2007) Purification and characterization of Alpha-Fetoprotein from the human hepatoblastoma HepG2 cell line in serum-free medium. Biometals 20: 869-878.
29. Si-Tayeb K, Noto FK, Nagaoka M, Li J, Battle MA, et al. (2010) Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology 51: 297-305.
30. Teramoto K, Asahina K, Kumashiro Y, Kakinuma S, Chinzei R, et al. (2005) Hepatocyte differentiation from embryonic stem cells and umbilical cord blood cells. J Hepatobiliary Pancreat Surg 12: 196-202.
31. Levy YS, Merims D, Panet H, Barhum Y, Melamed E, et al. (2003) Induction of neuron-specific enolase promoter and neuronal markers in differentiated mouse bone marrow stromal cells. J Mol Neurosci 21: 121-132.
32. Yuan SH, Martin J, Elia J, Flippin J, Paramban RI, et al. (2011) Cell-surface marker signatures for the isolation of neural stem cells, glia and neurons derived from human pluripotent stem cells. PLoS One 6: e17540.
33. MacPherson PA, Jones S, Pawson PA, Marshall KC, McBurney MW, (1997) P19 cells differentiate into glutamatergic and glutamate-responsive neurons in vitro. Neuroscience 80: 487-499.
34. Molnar E, Baude A, Richmond SA, Patel PB, Somogyi P, et al. (1993) Biochemical and immunocytochemical characterization of antipeptide antibodies to a cloned GluR1 glutamate receptor subunit: cellular and subcellular distribution in the rat forebrain. Neuroscience 53: 307-326.
35. Woodbury D, Reynolds K, Black IB, (2002) Adult bone marrow stromal stem cells express germline, ectodermal, endodermal, and mesodermal genes prior to neurogenesis. J Neurosci Res 69: 908-917.
36. Kuwabara T, Hsieh J, Muotri A, Yeo G, Warashina M, et al. (2009) Wnt-mediated activation of NeuroD1 and retro-elements during adult neurogenesis. Nat Neurosci 12: 1097-1105.
37. Gottlieb DI, Huettner JE, (1999) An in vitro pathway from embryonic stem cells to neurons and glia. Cells Tissues Organs 165: 165-172.
38. Karumbayaram S, Novitch BG, Patterson M, Umbach JA, Richter L, et al. (2009) Directed differentiation of human-induced pluripotent stem cells generates active motor neurons. Stem Cells 27: 806-811.
39. Li M, Pevny L, Lovell-Badge R, Smith A, (1998) Generation of purified neural precursors from embryonic stem cells by lineage selection. Curr Biol 8: 971-974.
40. Reubinoff BE, Itsykson P, Turetsky T, Pera MF, Reinhartz E, et al. (2001) Neural progenitors from human embryonic stem cells. Nat Biotechnol 19: 1134-1140.
41. Zhang SC, Wernig M, Duncan ID, Brustle O, Thomson JA, (2001) In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 19: 1129-1133.
42. Suzuki S, Namiki J, Shibata S, Mastuzaki Y, Okano H, (2010) The neural stem/progenitor cell marker nestin is expressed in proliferative endothelial cells, but not in mature vasculature. J Histochem Cytochem 58: 721-730.
43. Kuznetsov SA, Rodionov VI, Gelfand VI, Rosenblat VA, (1981) Purification of high-Mr microtubule proteins MAP1 and MAP2. FEBS Lett 135: 237-240.
44. del Castillo FJ, Cohen-Salmon M, Charollais A, Caille D, Lampe PD, et al. (2010) Consortin, a trans-Golgi network cargo receptor for the plasma membrane targeting and recycling of connexins. Hum Mol Genet 19: 262-275.
45. Liu L, Wise DR, Diehl JA, Simon MC, (2008) Hypoxic reactive oxygen species regulate the integrated stress response and cell survival. J Biol Chem 283: 31153-31162.
46. Hollenbeck ST, Senghaas A, Komatsu I, Zhang Y, Erdmann D, et al. (2012) Tissue engraftment of hypoxic-preconditioned adipose-derived stem cells improves flap viability. Wound Repair Regen 20: 872-878.
47. Blanpain C, Lowry WE, Geoghegan A, Polak L, Fuchs E, (2004) Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118: 635-648.
48. Li L, Bhatia R, (2011) Stem cell quiescence. Clin Cancer Res 17: 4936-4941.
49. Medici D, Shore EM, Lounev VY, Kaplan FS, Kalluri R, et al. (2010) Conversion of vascular endothelial cells into multipotent stem-like cells. Nat Med 16: 1400-1406.
50. Xiao N, Jani K, Morgan K, Okabe R, Cullen DE, et al. (2012) Hematopoietic stem cells lacking Ott1 display aspects associated with aging and are unable to maintain quiescence during proliferative stress. Blood 119: 4898-4907.
51. Acharyya S, Oskarsson T, Vanharanta S, Malladi S, Kim J, et al. (2012) A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell 150: 165-178.
52. Huang J, Zhang Z, Guo J, Ni A, Deb A, et al. (2010) Genetic modification of mesenchymal stem cells overexpressing CCR1 increases cell viability, migration, engraftment, and capillary density in the injured myocardium. Circ Res 106: 1753-1762.
53. Plath K, Lowry WE, (2011) Progress in understanding reprogramming to the induced pluripotent state. Nat Rev Genet 12: 253-265.
54. Couture JP, Daviau A, Fradette J, Blouin R, (2009) The mixed-lineage kinase DLK is a key regulator of 3T3-L1 adipocyte differentiation. PLoS One 4: e4743.
55. Thompson SA, Copeland CR, Reich DH, Tung L, (2011) Mechanical coupling between myofibroblasts and cardiomyocytes slows electric conduction in fibrotic cell monolayers. Circulation 123: 2083-2093.
56. Banas A, Teratani T, Yamamoto Y, Tokuhara M, Takeshita F, et al. (2007) Adipose tissue-derived mesenchymal stem cells as a source of human hepatocytes. Hepatology 46: 219-228.
57. Behbahan IS, Duan Y, Lam A, Khoobyari S, Ma X, et al. (2011) New approaches in the differentiation of human embryonic stem cells and induced pluripotent stem cells toward hepatocytes. Stem Cell Rev 7: 748-759.
58. Hamazaki T, Iiboshi Y, Oka M, Papst PJ, Meacham AM, et al. (2001) Hepatic maturation in differentiating embryonic stem cells in vitro. FEBS Lett 497: 15-19.
59. Hu AB, Cai JY, Zheng QC, He XQ, Shan Y, et al. (2004) High-ratio differentiation of embryonic stem cells into hepatocytes in vitro. Liver Int 24: 237-245.
60. Zamule SM, Coslo DM, Chen F, Omiecinski CJ, (2011) Differentiation of human embryonic stem cells along a hepatic lineage. Chem Biol Interact 190: 62-72.
61. Mizuno H, Tobita M, Uysal AC, (2012) Concise review: Adipose-derived stem cells as a novel tool for future regenerative medicine. Stem Cells 30: 804-810.
62. Mignone JL, Kukekov V, Chiang AS, Steindler D, Enikolopov G, (2004) Neural stem and progenitor cells in nestin-GFP transgenic mice. J Comp Neurol 469: 311-324.
63. Kang KS, Trosko JE, (2011) Stem cells in toxicology: fundamental biology and practical considerations. Toxicol Sci 120Suppl 1: S269-289.
64. Vasiliou V, Nebert DW, (2005) Analysis and update of the human aldehyde dehydrogenase (ALDH) gene family. Hum Genomics 2: 138-143.
65. Trosko JE, Chang CC, Wilson MR, Upham B, Hayashi T, et al. (2000) Gap junctions and the regulation of cellular functions of stem cells during development and differentiation. Methods 20: 245-264.
66. Loven J, Orlando DA, Sigova AA, Lin CY, Rahl PB, et al. (2012) Revisiting global gene expression analysis. Cell 151: 476-482.
67. Meier P, Finch A, Evan G, (2000) Apoptosis in development. Nature 407: 796-801.