Signals from embryonic fibroblasts induce adult intestinal epithelial cells to form nestin-positive cells with proliferation and multilineage differentiation capacity in vitro

Stem Cells

Volumn 24, Issue 9, 2006, Pages 2085-2097

  Wiese, Cornelia ^a   Rolletschek, Alexandra ^a   Kania, Gabriela ^a   Navarrete Santos, Anne ^b   Anisimov, Sergey V ^c   Steinfarz, Barbara ^d   Tarasov, Kirill V ^c   Brugh, Sheryl A ^c   Zahanich, Ihor ^e   Rüschenschmidt, Christiane ^d   Beck, Heinz ^d   Blyszczuk, Przemyslaw ^a   Czyz, Jaroslaw ^a   Heubach, Jürgen F ^e   Ravens, Ursula ^e   Horstmann, Olaf ^g   St Onge, Luc ^h   Braun, Thomas ^f   Brüstle, Oliver ^d   Boheler, Kenneth R ^c   Wobus, Anna M ^a   more..

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^c NATIONAL INSTITUTE ON AGING   (United States)

^d UNIVERSITY OF BONN   (Germany)

^e DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^f MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

^g UNIVERSITY OF GÖTTINGEN   (Germany)

^h DeveloGen AG   (Germany)

Author keywords

Embryonic fibroblasts; In vitro differentiation; Intestinal epithelium; Mouse; Nestin; Wnt Bone morphogenetic protein

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 4; LYMPHOID ENHANCER FACTOR 1; NESTIN; UNCLASSIFIED DRUG; WNT PROTEIN; WNT4 PROTEIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHIMERA; FIBROBLAST; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTESTINE EPITHELIUM CELL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CELLS, CULTURED; ECTODERM; ENDODERM; ENTEROCYTES; FIBROBLASTS; GENE EXPRESSION PROFILING; HUMANS; INTERMEDIATE FILAMENT PROTEINS; MICE; NERVE TISSUE PROTEINS; POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; UP-REGULATION; WNT PROTEINS;

EID: 33749165460     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2006-0008     Document Type: Article

References (65)

1. Leedham SJ, Brittan M, McDonald SA et al. Intestinal stem cells. J Cell Mol Med 2005;9:11-24.
2. Potten CS, Loeffler M. Stem cells: Attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 1990;110:1001-1020.
3. Winton DJ. Stem cells in the epithelium of the small intestine and colon. In: Marshak DR, Gardner RL, Gottlieb D, eds. Stem Cell Biology. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 2001:515-536.
4. Dignass AU, Sturm A. Peptide growth factors in the intestine. Eur J Gastroenterol Hepatol 2001;13:763-770.
5. Clatworthy JP, Subramanian V. Stem cells and the regulation of proliferation, differentiation and patterning in the intestinal epithelium: Emerging insights from gene expression patterns, transgenic and gene ablation studies. Mech Dev 101:3-9, 2001.
6. He XC, Zhang J, Tong WG et al. BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-beta-catenin signaling. Nat Genet 2004;36:1117-1121.
7. Fre S, Huyghe M, Mourikis P et al. Notch signals control the fate of immature progenitor cells in the intestine. Nature 2005;435:964-968.
8. Kayahara T, Sawada M, Takaishi S et al. Candidate markers for stem and early progenitor cells, Musashi-1 and Hes1, are expressed in crypt base columnar cells of mouse small intestine. FEBS Lett 535:131-135, 2003.
9. Subramanian T, Marchionini D, Potter EM et al. Striatal xenotransplantation of human retinal pigment epithelial cells attached to microcarriers in hemiparkinsonian rats ameliorates behavioral deficits without provoking a host immune response. Cell Transplant 2002;11:207-214.
10. Korinek V, Barker N, Moerer P et al. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet 1998;19:379-383.
11. Bach SP, Renehan AG, Potten CS. Stem cells: The intestinal stem cell as a paradigm. Carcinogenesis 2000;21:469-476.
12. Lendahl U, Zimmerman LB, McKay RD. CNS stem cells express a new class of intermediate filament protein. Cell 1990;60:585-595.
13. Wiese C, Rolletschek A, Kania G et al. Nestin expression: A property of multi-lineage progenitor cells? Cell Mol Life Sci 61:2510-2522, 2004.
14. Kania G, Corbeil D, Fuchs J et al. Somatic stem cell marker prominin-1/CD133 is expressed in embryonic stem cell-derived progenitors. STEM CELLS 2005;23:791-804.
15. Wobus AM, Guan K, Yang HT et al. Embryonic stem cells as a model to study cardiac, skeletal muscle, and vascular smooth muscle cell differentiation. Methods Mol Biol 2002;185:127-156.
16. Li M, Sendtner M, Smith A. Essential function of LIF receptor in motor neurons. Nature 1995;378:724-727.
17. Gritti A, Cova L, Parati EA et al. Basic fibroblast growth factor supports the proliferation of epidermal growth factor-generated neuronal precursor cells of the adult mouse CNS. Neurosci Lett 1995;185:151-154.
18. Okabe S, Forsberg-Nilsson K, Spiro AC et al. Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech Dev 1996;59:89-102.
19. Branton RL, Love RM, Clarke DJ. cAMP included during cell suspension preparation improves survival of dopaminergic neurons in vitro. Neuroreport 1998;9:3223-3227.
20. Rolletschek A, Chang H, Guan K et al. Differentiation of embryonic stem cell-derived dopaminergic neurons is enhanced by survival-promoting factors. Mech Dev 105:93-104, 2001.
21. Blyszczuk P, Czyz J, Kania G et al. Expression of Pax4 in embryonic stem cells promotes differentiation of nestin-positive progenitor and insulin-producing cells. Proc Natl Acad Sci U S A 2003;100:998-1003.
22. Kania G, Blyszczuk P, Czyz J et al. Differentiation of mouse embryonic stem cells into pancreatic and hepatic cells. Methods Enzymol 2003;365:287-303.
23. Anisimov SV, Tarasov KV, Tweedie D et al. SAGE identification of gene transcripts with profiles unique to pluripotent mouse R1 embryonic stem cells. Genomics 2002;79:169-176.
24. Meyer BI, Gruss P. Mouse Cdx-1 expression during gastrulation. Development 1993;117:191-203.
25. Toma JG, Akhavan M, Fernandes KJ et al. Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 2001;3:778-784.
26. Zhao X, Das AV, Thoreson WB et al. Adult corneal limbal epithelium: A model for studying neural potential of non-neural stem cells/progenitors. Dev Biol 2002;250:317-331.
27. Yang Q, Bermingham NA, Finegold MJ et al. Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science 2001;294:2155-2158.
28. Legay C, Faudon M, Hery F et al. 5-Ht Metabolism in the intestinal wall of the rat. 1. The Mucosa. Neurochem Int 1983;5:721-727.
29. Lenka N, Lu ZJ, Sasse P et al. Quantitation and functional characterization of neural cells derived from ES cells using nestin enhancer-mediated targeting in vitro. J Cell Sci 2002;115:1471-1485.
30. Batlle E, Henderson JT, Beghtel H et al. Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 2002;111:251-263.
31. Wong MH, Huelsken J, Birchmeier W et al. Selection of multipotent stem cells during morphogenesis of small intestinal crypts of Lieberkuhn is perturbed by stimulation of Lef-1/beta-catenin signaling. J Biol Chem 2002;277:15843-15850.
32. Zulewski H, Abraham EJ, Gerlach MJ et al. Multipotential nestin-positive stem cells isolated from adult pancreatic islets differentiate ex vivo into pancreatic endocrine, exocrine, and hepatic phenotypes. Diabetes 2001;50:521-533.
33. Seaberg RM, Smukler SR, Kieffer TJ et al. Clonal identification of multipotent precursors from adult mouse pancreas that generate neural and pancreatic lineages. Nat Biotechnol 2004;22:1115-1124.
34. Niki T, Pekny M, Hellemans K et al. Class VI intermediate filament protein nestin is induced during activation of rat hepatic stellate cells. Hepatology 1999;29:520-527.
35. Evans GS, Flint N, Somers AS et al. The development of a method for the preparation of a rat intestinal epithelial cell primary cultures. J Cell Sci 1992;101:219-231.
36. Fukamachi H. Proliferation and differentiation of fetal rat intestinal epithelial cells in primary serum-free culture. J Cell Sci 1992;103:511-519.
37. Tsujimura T, Makiishi-Shimobayashi C, Lundkvist J et al. Expression of the intermediate filament nestin in gastrointestinal stromal tumors and interstitial cells of Cajal. Am J Pathol 2001;158:817-823.
38. Kruger GM, Mosher JT, Bixby S et al. Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness. Neuron 2002;35:657-669.
39. Brault V, Moore R, Kutsch S et al. Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 2001;128:1253-1264.
40. Lo L, Sommer L, Anderson DJ. MASH1 maintains competence for BMP2-induced neuronal differentiation in post-migratory neural crest cells. Curr Biol 1997;7:440-450.
41. Kleber M, Sommer L. Wnt signaling and the regulation of stem cell function. Curr Opin Cell Biol 2004;16:681-687.
42. Jönsson M, Smith K, Harris AL. Regulation of Wnt5a expression in human mammary cells by protein kinase C activity and the cytoskeleton. Br J Cancer 1998;78:430-438.
43. Parr BA, Shea MJ, Vassileva G et al. Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development 1993;119:247-261.
44. Wroblewski J, Engstrom M, Edwall-Arvidsson C et al. Distribution of nestin in the developing mouse limb bud in vivo and in micro-mass cultures of cells isolated from limb buds. Differentiation 1997;61:151-159.
45. Chimal-Monroy J, Montero JA, Ganan Y et al. Comparative analysis of the expression and regulation of Wnt5a, Fz4, and Frzb1 during digit formation and in micromass cultures. Dev Dyn 2002;224:314-320.
46. Lickert H, Domon C, Huls G et al. Wnt/(beta)-catenin signaling regulates the expression of the homeobox gene Cdx1 in embryonic intestine. Development 2000;127:3805-3813.
47. Pizette S, Abate-Shen C, Niswander L. BMP controls proximodistal outgrowth, via induction of the apical ectodermal ridge, and dorsoventral patterning in the vertebrate limb. Development 2001;128:4463-4474.
48. Bartholin L, Maguer-Satta V, Hayette S et al. Transcription activation of FLRG and follistatin by activin A, through Smad proteins, participates in a negative feedback loop to modulate activin A function. Oncogene 2002;21:2227-2235.
49. Theil T, Aydin S, Koch S et al. Wnt and Bmp signalling cooperatively regulate graded Emx2 expression in the dorsal telencephalon. Development 2002;129:3045-3054.
50. Fainsod A, Deissler K, Yelin R et al. The dorsalizing and neural inducing gene follistatin is an antagonist of BMP-4. Mech Dev 1997;63:39-50.
51. Seaberg RM, van der Kooy D. Adult rodent neurogenic regions: The ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. J Neurosci 2002;22:1784-1793.
52. Hack MA, Sugimori M, Lundberg C et al. Regionalization and fate specification in neurospheres: The role of Olig2 and Pax6. Mol Cell Neurosci 2004;25:664-678.
53. Kabos P, Ehtesham M, Kabosova A et al. Generation of neural progenitor cells from whole adult bone marrow. Exp Neurol 2002;178:288-293.
54. Wislet-Gendebien S, Leprince P, Moonen G et al. Regulation of neural markers nestin and GFAP expression by cultivated bone marrow stromal cells. J Cell Sci 2003;116:3295-3302.
55. Buzanska L, Machaj EK, Zablocka B et al. Human cord blood-derived cells attain neuronal and glial features in vitro. J Cell Sci 2002;115:2131-2138.
56. Li H, Liu H, Heller S. Pluripotent stem cells from the adult mouse inner ear. Nat Med 2003;9:1293-1299.
57. Seigel GM, Sun W, Salvi R et al. Human corneal stem cells display functional neuronal properties. Mol Vis 2003;9:159-163.
58. Maria-Engler SS, Correa-Giannella ML, Labriola L et al. Co-localization of nestin and insulin and expression of islet cell markers in long-term human pancreatic nestin-positive cell cultures. J Endocrinol 2004;183:455-467.
59. Vaittinen S, Lukka R, Sahlgren C et al. The expression of intermediate filament protein nestin as related to vimentin and desmin in regenerating skeletal muscle. J Neuropathol Exp Neurol 2001;60:588-597.
60. Lin RC, Matesic DF, Marvin M et al. Re-expression of the intermediate filament nestin in reactive astrocytes. Neurobiol Dis 1995;2:79-85.
61. Sejersen T, Lendahl U. Transient expression of the intermediate filament nestin during skeletal muscle development. J Cell Sci 1993;106:1291-1300.
62. Potten CS, Li YQ, O'Connor PJ et al. A possible explanation for the differential cancer incidence in the intestine, based on distribution of the cytotoxic effects of carcinogens in the murine large bowel. Carcinogenesis 1992;13:2305-2312.
63. Ishikawa R, Nishikori K, Furukawa S. Appearance of nerve growth factor and acidic fibroblast growth factor with different time courses in the cavity-lesioned cortex of the rat brain. Neurosci Lett 1991;127:70-72.
64. About I, Laurent-Maquin D, Lendahl U et al. Nestin expression in embryonic and adult human teeth under normal and pathological conditions. Am J Pathol 2000;157:287-295.
65. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992;255:1707-1710.