Neuro-muscular differentiation of adult porcine skin derived stem cell-like cells

PLoS ONE

Volumn 5, Issue 1, 2010, Pages

  Lermen, Dominik ^a   Gorjup, Erwin ^b   Dyce, Paul W ^c   Von Briesen, Hagen ^b   Müller, Paul ^a  

^a UNIVERSITY OF TRIER   (Germany)

^b FRAUNHOFER INSTITUTE FOR BIOMEDICAL ENGINEERING   (Germany)

^c UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA TUBULIN; BETA1 INTEGRIN; BMI1 PROTEIN; BREAST CANCER RESISTANCE PROTEIN; CD9 ANTIGEN; ENDOGLIN; GLIAL FIBRILLARY ACIDIC PROTEIN; HERMES ANTIGEN; NESTIN; OCTAMER TRANSCRIPTION FACTOR 4; STAT3 PROTEIN; TRANSCRIPTION FACTOR SOX2;

ADIPOCYTE; ANIMAL CELL; ARTICLE; ASTROCYTE; CELL DIFFERENTIATION; CELL EXPANSION; CELL ISOLATION; CELL PROLIFERATION; CELL RENEWAL; CELL STRUCTURE; COLONY FORMING UNIT; CONTROLLED STUDY; DOWN REGULATION; EMBRYONIC STEM CELL; EXPERIMENTAL PIG; FLOW CYTOMETRY; MESENCHYMAL STEM CELL; MULTIPOTENT STEM CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; SKIN; SMOOTH MUSCLE FIBER; SOMATIC CELL; UPREGULATION;

ANIMALS; ANTIGENS, CD; CELL DIFFERENTIATION; CELL PROLIFERATION; FLOW CYTOMETRY; MUSCLES; NERVOUS SYSTEM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STEM CELLS; SWINE;

SUS;

EID: 77749292076     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0008968     Document Type: Article

References (92)

1. Dick I, Scott R (1992) Pig ear skin as an in-vitro model for human skin permeability. The Journal of pharmacy and pharmacology 44: 640-5.
2. Simon G, Maibach H (2000) The Pig as an Experimental Animal Model of Percutaneous Permeation in Man: Qualitative and Quantitative Observations-An Overview. Skin Pharmacology and Applied Skin Physiology 13: 229-234.
3. Jacobi U, Kaiser M, Toll R, Mangelsdorf S, Audring H, et al. (2007) Porcine ear skin: an in vitro model for human skin. Skin Research and Technology 13: 19-24.
4. Strojek RM, Reed MA, Hoover JL, Wagner TE (1990) A method for cultivating morphologically undifferentiated embryonic stem cells from porcine blastocysts. Theriogenology 33: 901-913.
5. Piedrahita JA, Anderson GB, BonDurant RH (1990) On the isolation of embryonic stem cells: Comparative behavior of murine, porcine and ovine embryos. Theriogenology 34: 879-901.
6. Shim H, Gutierrez-Adan A, Chen LR, BonDurant RH, Behboodi E, et al. (1997) Isolation of pluripotent stem cells from cultured porcine primordial germ cells. Biol Reprod 57: 1089-1095.
7. Iohara K, Zheng L, Ito M, Tomokiyo A, Matsushita K, et al. (2006) Side Population Cells Isolated from Porcine Dental Pulp Tissue with Self-Renewal and Multipotency for Dentinogenesis, Chondrogenesis, Adipogenesis, and Neurogenesis. Stem Cells 24: 2493-2503.
8. Ringe J, Kaps C, Schmitt B, Büscher K, Bartel J, et al. (2002) Porcine mesenchymal stem cells. Cell and Tissue Research 307: 321-327.
9. Schwartz PH, Nethercott H, Kirov II, Ziaeian B, Young MJ, et al. (2005) Expression of Neurodevelopmental Markers by Cultured Porcine Neural Precursor Cells. Stem Cells 23: 1286-1294.
10. Bickenbach JR, Chism E (1998) Selection and Extended Growth of murine Epidermal Stem Cells in Culture. Experimental Cell Research 244: 184-195.
11. Lavker R, Sun T (2000) Epidermal stem cell: Properties, markers and lokation. Proceedings of the National Academy of Sciences of the United States of America 97: 13473-13475.
12. Dunnwald M, Tomanek-Chalkley A, Alexandrunas D, Fishbaugh J, Bickenbach JR (2001) Isolating a pure population of epidermal stem cells for use in tissue engineering. Experimental Dermatology 10: 45-54.
13. Liang L, Bickenbach JR (2002) Somatic Epidermal Stem Cells Can Produce Multible Cell Lineages During Development. Stem Cells 20: 21-31.
14. Cotsarelis GKP, Dhouailly D, Hengge U, Bickenbach JR (1999) Epithelial stem cells in the skin: definition, markers, lokation and function. Experimental Dermatology 8: 80-88.
15. Watt FM, Celso CL, Silva-Vargas V (2006) Epidermal stem cells: an update. Current Opinion in Genetics & Development 16: 518-524.
16. Toma J, Akhavan M, Fernandes K, Barnabé-Heider F, Sadikot A, et al. (2001) Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nature Cell Biology 3: 778-784.
17. Kajahn J, Gorjup E, Tiede S, von Briesen H, Paus R, et al. (2008) Skin-derived human adult stem cells surprisingly share many features with human pancreatic stem cells. European Journal of Cell Biology 87: 39-46.
18. Kruse C, Bodo E, Petschnik A, Danner S, Tiede S, et al. (2006) Towards the development of a pragmatic technique for isolating and differentiating nestinpositive cells from human scalp skin into neuronal and glial cell populations: generating neurons from human skin? Experimental Dermatology 15: 794-800.
19. Chunmeng S, Tianmin C (2004) Skin: a promising reservoir for adult stem cell populations. Medical Hypotheses 62: 683-688.
20. Fernandes KJL, McKenzie IA, Mill P, Smith KM, Akhavan M, et al. (2004) A dermal niche for multipotent adult skin-derived precursor cells. Nat Cell Biol 6: 1082-1093.
21. Toma JG, McKenzie IA, Bagli D, Miller FD (2005) Isolation and Characterization of Multipotent Skin-Derived Precursors from Human Skin. Stem Cells 23: 727-737.
22. Ghazizadeh S, Taichman LB (2001) Multiple classes of stem cells in cutaneous epithelium: a lineage analysis of adult mouse skin. Embo J 20: 1215-1222.
23. Reynolds AJ, Jahoda CAB (1991) Hair follicle stem cells? A distinct germinative epidermal cell population is activated in vitro by the presence of hair dermal papilla cells. Journal of Cell Science 99: 373-385.
24. Morris R, Liu Y, Marles L, Yang Z, Trempus C, et al. (2004) Capturing and profiling adult hair follicle stem cells. Nature Biotechnologie 22: 411-417.
25. Hoogduijn MJ, Gorjup E, Genever PG (2006) Comparative Characterization of Hair Follicle Dermal Stem Cells and Bone Marrow Mesenchymal Stem Cells. Stem Cells and Development 15: 49-60.
26. Lermen D, Blömeke B, Browne R, Clarke A, Dyce PW, et al. (2009) Cryobanking of viable biomaterials: implementation of new strategies for conservation purposes. Molecular Ecology 18: 1030-1033.
27. Kim MK, Jang G, Oh HJ, Yuda F, Kim HJ, et al. (2007) Endangered Wolves Cloned from Adult Somatic Cells. Cloning and Stem Cells 9: 130-137.
28. Holt WV, Pickard AR, Prather RS (2004) Wildlife conservation and reproductive cloning. Reproduction 127: 317-324.
29. Leon-Quinto T, Simon MA, Cadenas R, Jones J, Martinez-Hernandez FJ, et al. (2009) Developing biological resource banks as a supporting tool for wildlife reproduction and conservation: The Iberian lynx bank as a model for other endangered species. Animal Reproduction Science 112: 347-361.
30. Dyce PW, Zhu H, Craig J, Li J (2004) Stem cells with multilineage potential derived from porcine skin. Biochemical Biophysical Research Communication 316: 651-658.
31. Dyce PW, Wen L, Li J (2006) In vitro germline potential of stem cells derived from fetal porcine skin. Nat Cell Biol 8: 384-390.
32. Masui S, Nakatake Y, Toyooka Y, Shimosato D, Yagi R, et al. (2007) Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nat Cell Biol 9: 625-635.
33. Nakatake Y, Fukui N, Iwamatsu Y, Masui S, Takahashi K, et al. (2006) Klf4 Cooperates with Oct3/4 and Sox2 To Activate the Lefty1 Core Promoter in Embryonic Stem Cells. Mol Cell Biol 26: 7772-7782.
34. Chambers I, Colby D, Robertson M, Nichols J, Lee S, et al. (2003) Functional Expression Cloning of Nanog, a Pluripotency Sustaining Factor in Embryonic Stem Cells. Cell 113: 643-655.
35. Loh Y-H, Wu Q, Chew J-L, Vega VB, Zhang W, et al. (2006) The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 38: 431-440.
36. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, et al. (2005) Core Transcriptional Regulatory Circuitry in Human Embryonic Stem Cells. Cell 122: 947-956.
37. Zhong Z, Wen Z, Darnell JE Jr (1994) Stat3: a STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6. Science 264: 95-98.
38. Niwa H, Burdon T, Chambers I, Smith A (1998) Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev 12: 2048-2060.
39. Matsuda T, Nakamura T, Nakao K, Arai T, Katsuki M, et al. (1999) STAT3 activation is sufficient to maintain an undifferentiated state of mouse embryonic stem cells. The EMBO Journal 18: 4261-4269.
40. Toshio H, Katsuhiko I, Masahiko H (2000) Roles of STAT3 in mediating the cell growth, differentiation and survival signals relayed through the IL-6 family of cytokine receptors. Oncogene 19: 2548-2556.
41. Heinrich PC, Behrmann I, Müller-Newen G, Schaper F, Graeve L (1998) Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem J 334: 297-314.
42. Go MJ, Takenaka C, Ohgushi H (2008) Forced expression of Sox2 or Nanog in human bone marrow derived mesenchymal stem cells maintains their expansion and differentiation capabilities. Experimental Cell Research 314: 1147-1154.
43. Gorjup E, Danner S, Rotter N, Habermann J, Brassat U, et al. (2009) Glandular tissue from human pancreas and salivary gland yields similar stem cell populations. European Journal of Cell Biology 88: 409-421.
44. Chamberlain G, Fox J, Ashton B, Middleton J (2007) Concise Review: Mesenchymal Stem Cells: Their Phenotype, Differentiation Capacity, Immunological Features, and Potential for Homing. Stem Cells 25: 2739-2749.
45. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, et al. (1999) Multilineage Potential of Adult Human Mesenchymal Stem Cells. Science 284: 143-147.
46. Conget P, Minguell J (1999) Phenotypical and functional properties of human bone marrow mesenchymal progenitor cells. Journal of Cellular Physiology 181: 67-73.
47. Wiese C, Rolletschek A, Kania G, Blyszczuk P, Tarasov KV, et al. (2004) Nestin expression-a property of multi-lineage progenitor cells? Cellular and Molecular Life Sciences (CMLS) 61: 2510-2522.
48. Li L, Mignone J, Yang M, Matic M, Penman S, et al. (2003) Nestin expression in hair follicle sheath progenitor cells. Proceedings of the National Academy of Sciences 100: 9958-9961.
49. Zulewski H, Abraham EJ, Gerlach MJ, Daniel PB, Moritz W, et al. (2001) Multipotential Nestin-Positive Stem Cells Isolated From Adult Pancreatic Islets Differentiate Ex Vivo Into Pancreatic Endocrine, Exocrine, and Hepatic Phenotypes. Diabetes 50: 521-533.
50. Park I-K, Morrison SJ, Clarke MF (2004) Bmi1, stem cells, and senescence regulation. J Clin Invest 113: 175-179.
51. Iwama A, Oguro H, Negishi M, Kato Y, Morita Y, et al. (2004) Enhanced Self-Renewal of Hematopoietic Stem Cells Mediated by the Polycomb Gene Product Bmi-1. Immunity 21: 843-851.
52. Bruggeman SWM, Valk-Lingbeek ME, van der Stoop PPM, Jacobs JJL, Kieboom K, et al. (2005) Ink4a and Arf differentially affect cell proliferation and neural stem cell self-renewal in Bmi1-deficient mice. Genes Dev 19: 1438-1443.
53. Jacobs JJL, Kieboom K, Marino S, DePinho RA, van Lohuizen M (1999) The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397: 164-168.
54. Sangiorgi E, Capecchi MR (2008) Bmi1 is expressed in vivo in intestinal stem cells. Nat Genet 40: 915-920.
55. Zhou S, Morris JJ, Barnes Y, Lan L, Schuetz JD, et al. (2002) Bcrp1 gene expression is required for normal numbers of side population stem cells in mice, and confers relative protection to mitoxantrone in hematopoietic cells in vivo. Proceedings of the National Academy of Sciences 99: 12339-12344.
56. Lassalle B, Bastos H, Louis JP, Riou L, Testart J, et al. (2004) 'Side Population' cells in adult mouse testis express Bcrp1 gene and are enriched in spermatogonia and germinal stem cells. Development 131: 479-487.
57. Malcolm RA (2003) Tissue-based stem cells: ABC transporter proteins take centre stage. The Journal of Pathology 200: 547-550.
58. Kim M, Turnquist H, Jackson J, Sgagias M, Yan Y, et al. (2002) The Multidrug Resistance Transporter ABCG2 (Breast Cancer Resistance Protein 1) Effluxes Hoechst 33342 and Is Overexpressed in Hematopoietic Stem Cells. Clin Cancer Res 8: 22-28.
59. Zeng L, Rahrmann E, Hu Q, Lund T, Sandquist L, et al. (2006) Multipotent Adult Progenitor Cells from Swine Bone Marrow. Stem Cells 24: 2355-2366.
60. Lee RH, Kim B, Choi I, Kim H, Choi HS, et al. (2004) Characterisation and Expression Analysis of Mesenchymal Stem Cells from Human Bone Marrow and Adipose Tissue. Cellular Pysiology and Biochemistry 14: 311-324.
61. Tropel P, Noël D, Platet N, Legrand P, Benabid A-L, et al. (2004) Isolation and characterisation of mesenchymal stem cells from adult mouse bone marrow. Experimental Cell Research 295: 395-406.
62. Maniatopoulos C, Sodek J, Melcher AH (1988) Bone formation in vitro by stromal cells obtained from bone marrow of young adult rats. Cell and Tissue Research 254: 317-330.
63. Pittenger MF, Martin BJ (2004) Mesenchymal Stem Cells and Their Potential as Cardiac Therapeutics. Circ Res 95: 9-20.
64. Friedenstein AJ, Chailakhyan RK, Gerasimov UV (1987) Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers. Cell Proliferation 20: 263-272.
65. Wislet-Gendebien S, Hans G, Leprince P, Rigo J-M, Moonen G, et al. (2005) Plasticity of Cultured Mesenchymal Stem Cells: Switch from Nestin-Positive to Excitable Neuron-Like Phenotype. Stem Cells 23: 392-402.
66. Ying X, Qiang Z, Bing-bing J, Guo-ping H, Yu-lin X, et al. (2007) Ex vivo expansion and pluripotential differentiation of cryopreserved human bone marrow mesenchymal stem cells. Journal of Zhejiang University - Science B 8: 136-146.
67. Alexanian AR (2005) Neural stem cells induce bone-marrow-derived mesenchymal stem cells to generate neural stem-like cells via juxtacrine and paracrine interactions. Experimental Cell Research 310: 383-391.
68. Sanchez-Ramos J, Song S, Cardozo-Pelaez F, Hazzi C, Stedeford T, et al. (2000) Adult Bone Marrow Stromal Cells Differentiate into Neural Cells in Vitro. Experimental Neurology 164: 247-256.
69. Barry FP, Murphy JM (2004) Mesenchymal stem cells: clinical applications and biological characterization. The International Journal of Biochemistry & Cell Biology 36: 568-584.
70. DiGirolamo C, Stokes D, Colter D, Phinney D, Class R, et al. (1999) Propagation and senescence of human marrow stromal cells in culture: a simple colony-forming assay identifies samples with the greatest potential to propagate and differentiate. British Journal of Haematology 107: 275-281.
71. Shih DT-b, Lee D-C, Chen S-C, Tsai R-Y, Huang C-T, et al. (2005) Isolation and Characterization of Neurogenic Mesenchymal Stem Cells in Human Scalp Tissue. Stem Cells 23: 1012-1020.
72. Baddoo M, Hill K, Wilkinson R, Gaupp D, Hughes C, et al. (2003) Characterization of mesenchymal stem cells isolated from murine bone marrow by negative selection. Journal of Cellular Biochemistry 89: 1235-1249.
73. Peister A, Mellad JA, Larson BL, Hall BM, Gibson LF, et al. (2004) Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood 103: 1662-1668.
74. Wexler SA, Donaldson C, Denning-Kendall P, Rice C, Bradley B, et al. (2003) Adult bone marrow is a rich source of human mesenchymal 'stem' cells but umbilical cord and mobilized adult blood are not. British Journal of Haematology 121: 368-374.
75. Okumura-Nakanishi S, Saito M, Niwa H, Ishikawa F (2005) Oct-3/4 and Sox2 Regulate Oct-3/4 Gene in Embryonic Stem Cells. J Biol Chem 280: 5307-5317.
76. Graham V, Khudyakov J, Ellis P, Pevny L (2003) SOX2 Functions to Maintain Neural Progenitor Identity. Neuron 39: 749-765.
77. Tai M-H, Chang C-C, Olson LK, Trosko JE (2005) Oct4 expression in adult human stem cells: evidence in support of the stem cell theory of carcinogenesis. Carcinogenesis 26: 495-502.
78. Zhao M, Isom SC, Lin H, Hao Y, Zhang Y, et al. (2009) Tracing the Stemness of Porcine Skin-Derived Progenitors (pSKP) Back to Specific Marker Gene Expression. Cloning and Stem Cells 11: 111-122.
79. Takahashi K, Yamanaka S (2006) Induction of Pluripotent Stem Cells from Mouse Embryonic and Adult Fibroblast Cultures by Defined Factors. Cell 126: 663-676.
80. Okita K, Ichisaka T, Yamanaka S (2007) Generation of germline-competent induced pluripotent stem cells. Nature 448: 313-317.
81. Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, et al. (2007) In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448: 318-324.
82. Kim JB, Zaehres H, Wu G, Gentile L, Ko K, et al. (2008) Pluripotent stem cells induced from adult neural stem cells by reprogramming with two factors. Nature 454: 646-650.
83. Shi Y, Desponts C, Do JT, Hahm HS, Schöler HR, et al. (2008) Induction of Pluripotent Stem Cells from Mouse Embryonic Fibroblasts by Oct4 and Klf4 with Small-Molecule Compounds. Cell Stem Cell 3: 568-574.
84. Tondreau T, Laurence L, Marielle D, Martine M, Christine M, et al. (2004) Bone marrow-derived mesenchymal stem cells already express specific neural proteins before any differentiation. Differentiation 72: 319-326.
85. Danner S, Kajahn J, Geismann C, Klink E, Kruse C (2007) Derivation of oocyte-like cells from a clonal pancreatic stem cell line. Mol Hum Reprod 13: 11-20.
86. Kruse C, Birth M, Rohwedel J, Assmuth K, Goepel A, et al. (2004) Pluripotency of adult stem cells derived from human and rat pancreas. Applied Physics A 79: 1617-1624.
87. Lendahl U, Zimmerman LB, McKay RDG (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60: 585-595.
88. Loo DT, Althoen MC, Cotman CW (1994) Down regulation of nestin by TGF-[beta] or serum in SFME cells accompanies differentiation into astrocytes. NeuroReport 5: 1585-1588.
89. Moreels M, Vandenabeele F, Dumont D, Robben J, Lambrichts I (2008) Alphasmooth muscle actin (α-SMA) and nestin expression in reactive astrocytes in multiple sclerosis lesions: potential regulatory role of transforming growth factorbeta 1 (TGF-β 1). Neuropathology and Applied Neurobiology 34: 532-546.
90. Draberova E, Valle LD, Gordon J, Markova V, Smejkalova B, et al. (2008) Class III [beta]-Tubulin Is Constitutively Coexpressed With Glial Fibrillary Acidic Protein and Nestin in Midgestational Human Fetal Astrocytes: Implications for Phenotypic Identity. Journal of Neuropathology & Experimental Neurology 67: 341-354.
91. Ramsay TG, Yan X, Morrison C (1998) The obesity gene in swine: sequence and expression of porcine leptin. J Anim Sci 76: 484-490.
92. Misko TP, Radeke MJ, Shooter EM (1987) Nerve growth factor in neuronal development and maintenance. J Exp Biol 132: 177-190.