Isolation of mineralizing Nestin+ Nkx6.1+ vascular muscular cells from the adult human spinal cord

BMC Neuroscience

Volumn 12, Issue , 2011, Pages

  Mamaeva, Daria ^a   Ripoll, Chantal ^b   Bony, Claire ^b   Teigell, Marisa ^b   Perrin, Florence E ^c,d   Rothhut, Bernard ^b   Bieche, Ivan ^e   Lidereau, Rosette ^e   Privat, Alain ^b   Rigau, Valérie ^f   Guillon, Hélène ^b   Vachiery Lahaye, Florence ^f   Noel, Daniele ^b   Bauchet, Luc ^f   Hugnot, Jean Philippe ^b,g  

^a INSTITUTE OF HUMAN GENETICS   (France)

^b HÔPITAL SAINT ELOI   (France)

^c BASQUE FOUNDATION FOR SCIENCE   (Spain)

^d UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^e INSTITUT CURIE   (France)

^f MONTPELLIER UNIVERSITY HOSPITAL   (France)

^g UNIV MONTPELLIER   (France)

Author keywords

Calcification; Human central nervous system; Nkx6.1; Osteogenesis; Spinal cord; Stem cells; Vascular muscle cells

Indexed keywords

BIOLOGICAL MARKER; CALPONIN; GLIAL FIBRILLARY ACIDIC PROTEIN; NESTIN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; SMOOTH MUSCLE ACTIN; TRANSCRIPTION FACTOR NKX6.1; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR TWIST; HOMEODOMAIN PROTEIN; INTERMEDIATE FILAMENT PROTEIN; NERVE PROTEIN; NKX6 1 PROTEIN, HUMAN; NKX6-1 PROTEIN, HUMAN;

ADIPOCYTE; ARTICLE; BONE DEVELOPMENT; CALCIFICATION; CARTILAGE CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL ISOLATION; CELL POPULATION; CONTROLLED STUDY; GLIA CELL; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE; MESENCHYME CELL; MINERALIZATION; MUSCLE CELL; NERVE CELL; OSTEOBLAST; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; SPINAL CORD; VASCULAR SMOOTH MUSCLE; ADULT; BLOOD; BONE MINERALIZATION; CELL ADHESION; CELL SEPARATION; CYTOLOGY; METABOLISM; METHODOLOGY; PHYSIOLOGY; PRIMARY CELL CULTURE; SMOOTH MUSCLE FIBER; VASCULARIZATION;

ADULT; CALCIFICATION, PHYSIOLOGIC; CELL ADHESION; CELL SEPARATION; HOMEODOMAIN PROTEINS; HUMANS; INTERMEDIATE FILAMENT PROTEINS; MYOCYTES, SMOOTH MUSCLE; NERVE TISSUE PROTEINS; PRIMARY CELL CULTURE; SPINAL CORD;

EID: 80053616259     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-12-99     Document Type: Article

References (39)

1. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992, 255(5052):1707-1710. 10.1126/science.1553558, 1553558.
2. Arsenijevic Y, Villemure JG, Brunet JF, Bloch JJ, Deglon N, Kostic C, Zurn A, Aebischer P. Isolation of multipotent neural precursors residing in the cortex of the adult human brain. Exp Neurol 2001, 170(1):48-62. 10.1006/exnr.2001.7691, 11421583.
3. Roy NS, Wang S, Jiang L, Kang J, Benraiss A, Harrison-Restelli C, Fraser RA, Couldwell WT, Kawaguchi A, Okano H, Nedergaard M, Goldman SA. In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus. Nat Med 2000, 6(3):271-277. 10.1038/73119, 10700228.
4. Nunes MC, Roy NS, Keyoung HM, Goodman RR, McKhann G, Jiang L, Kang J, Nedergaard M, Goldman SA. Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat Med 2003, 9(4):439-447. 10.1038/nm837, 12627226.
5. Kukekov VG, Laywell ED, Suslov O, Davies K, Scheffler B, Thomas LB, O'Brien TF, Kusakabe M, Steindler DA. Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of adult human brain. Exp Neurol 1999, 156(2):333-344. 10.1006/exnr.1999.7028, 10328940.
6. Pagano SF, Impagnatiello F, Girelli M, Cova L, Grioni E, Onofri M, Cavallaro M, Etteri S, Vitello F, Giombini S, Solero CL, Parati EA. Isolation and characterization of neural stem cells from the adult human olfactory bulb. Stem Cells 2000, 18(4):295-300. 10.1634/stemcells.18-4-295, 10924096.
7. Scolding NJ, Rayner PJ, Compston DA. Identification of A2B5-positive putative oligodendrocyte progenitor cells and A2B5-positive astrocytes in adult human white matter. Neuroscience 1999, 89(1):1-4. 10.1016/S0306-4522(98)00548-X, 10051212.
8. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-Garcia Verdugo J, Berger MS, Alvarez-Buylla A. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 2004, 427(6976):740-744. 10.1038/nature02301, 14973487.
9. Akiyama Y, Honmou O, Kato T, Uede T, Hashi K, Kocsis JD. Transplantation of clonal neural precursor cells derived from adult human brain establishes functional peripheral myelin in the rat spinal cord. Exp Neurol 2001, 167(1):27-39. 10.1006/exnr.2000.7539, 11161590.
10. Walton NM, Sutter BM, Chen HX, Chang LJ, Roper SN, Scheffler B, Steindler DA. Derivation and large-scale expansion of multipotent astroglial neural progenitors from adult human brain. Development 2006, 133(18):3671-3681. 10.1242/dev.02541, 16914491.
11. Jiang Y, Vaessen B, Lenvik T, Blackstad M, Reyes M, Verfaillie CM. Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Exp Hematol 2002, 30(8):896-904. 10.1016/S0301-472X(02)00869-X, 12160841.
12. Hugnot JP, Franzen R. The spinal cord ependymal region: A neural stem cell niche in the caudal central nervous system. Front Biosci 2011, 16:1044-1059. 10.2741/3734, 21196217.
13. Dromard C, Guillon H, Rigau V, Ripoll C, Sabourin JC, Perrin FE, Scamps F, Bozza S, Sabatier P, Lonjon N, Duffau H, Vachiery-Lahaye F, Prieto M, Tran Van Ba C, Deleyrolle L, Boularan A, Langley K, Gaviria M, Privat A, Hugnot JP, Bauchet L. Adult human spinal cord harbors neural precursor cells that generate neurons and glial cells in vitro. J Neurosci Res 2008, 86(9):1916-1926. 10.1002/jnr.21646, 18335522.
14. Alliot F, Rutin J, Leenen PJ, Pessac B. Pericytes and periendothelial cells of brain parenchyma vessels co-express aminopeptidase N, aminopeptidase A, and nestin. J Neurosci Res 1999, 58(3):367-378. 10.1002/(SICI)1097-4547(19991101)58:3<367::AID-JNR2>3.0.CO;2-T, 10518110.
15. Williams LT, Tremble P, Antoniades HN. Platelet-derived growth factor binds specifically to receptors on vascular smooth muscle cells and the binding becomes nondissociable. Proc Natl Acad Sci USA 1982, 79(19):5867-5870. 10.1073/pnas.79.19.5867, 347011, 6310551.
16. Sander M, Sussel L, Conners J, Scheel D, Kalamaras J, Dela Cruz F, Schwitzgebel V, Hayes-Jordan A, German M. Homeobox gene Nkx6.1 lies downstream of Nkx2.2 in the major pathway of beta-cell formation in the pancreas. Development 2000, 127(24):5533-5540.
17. Liu R, Cai J, Hu X, Tan M, Qi Y, German M, Rubenstein J, Sander M, Qiu M. Region-specific and stage-dependent regulation of Olig gene expression and oligodendrogenesis by Nkx6.1 homeodomain transcription factor. Development 2003, 130(25):6221-6231. 10.1242/dev.00868, 14602683.
18. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L, Norotte C, Teng PN, Traas J, Schugar R, Deasy BM, Badylak S, Buhring HJ, Giacobino JP, Lazzari L, Huard J, Peault B. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008, 3(3):301-313. 10.1016/j.stem.2008.07.003, 18786417.
19. Karussis D, Kassis I. The potential use of stem cells in multiple sclerosis: an overview of the preclinical experience. Clin Neurol Neurosurg 2008, 110(9):889-896. 10.1016/j.clineuro.2008.02.008, 18375051.
20. Dore-Duffy P, Katychev A, Wang X, Van Buren E. CNS microvascular pericytes exhibit multipotential stem cell activity. J Cereb Blood Flow Metab 2006, 26(5):613-624. 10.1038/sj.jcbfm.9600272, 16421511.
21. Franco Lambert AP, Fraga Zandonai A, Bonatto D, Cantarelli Machado D, Pegas Henriques JA. Differentiation of human adipose-derived adult stem cells into neuronal tissue: does it work?. Differentiation 2009, 77(3):221-228. 10.1016/j.diff.2008.10.016, 19272520.
22. D'Alessandro JS, Yetz-Aldape J, Wang EA. Bone morphogenetic proteins induce differentiation in astrocyte lineage cells. Growth Factors 1994, 11(1):53-69. 10.3109/08977199409015051, 7530466.
23. Whittemore SR, Morassutti DJ, Walters WM, Liu RH, Magnuson DS. Mitogen and substrate differentially affect the lineage restriction of adult rat subventricular zone neural precursor cell populations. Exp Cell Res 1999, 252(1):75-95. 10.1006/excr.1999.4621, 10502401.
24. Murray K, Dubois-Dalcq M. Emergence of oligodendrocytes from human neural spheres. J Neurosci Res 1997, 50(2):146-156. 10.1002/(SICI)1097-4547(19971015)50:2<146::AID-JNR4>3.0.CO;2-F, 9373025.
25. Compston A. From the archive "The cerebral blood-vessels in health and disease" by Pr H. Obersteiner. Brain 2007, 130:3057-3059.
26. Obersteiner H. The cerebral blood-vessels in health and disease. Brain 1884, 7:289-389.
27. Makariou E, Patsalides AD. Intracranial calcifications. Appl Radiol 2009, 38(11):48-50.
28. Wegiel J, Kuchna I, Wisniewski T, de Leon MJ, Reisberg B, Pirttila T, Kivimaki T, Lehtimaki T. Vascular fibrosis and calcification in the hippocampus in aging, Alzheimer disease, and Down syndrome. Acta Neuropathol 2002, 103(4):333-343. 10.1007/s00401-001-0471-y, 11904752.
29. Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 2000, 425(4):479-494. 10.1002/1096-9861(20001002)425:4<479::AID-CNE2>3.0.CO;2-3, 10975875.
30. Kuhn HG, Dickinson-Anson H, Gage FH. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 1996, 16(6):2027-2033.
31. Goritz C, Dias DO, Tomilin N, Barbacid M, Shupliakov O, Frisen J. A pericyte origin of spinal cord scar tissue. Science 2011, 333(6039):238-242. 10.1126/science.1203165, 21737741.
32. McMahon AP. Neural patterning: the role of Nkx genes in the ventral spinal cord. Genes Dev 2000, 14(18):2261-2264. 10.1101/gad.840800, 10995382.
33. Cai J, Xu X, Yin H, Wu R, Modderman G, Chen Y, Jensen J, Hui CC, Qiu M. Evidence for the differential regulation of Nkx-6.1 expression in the ventral spinal cord and foregut by Shh-dependent and -independent mechanisms. Genesis 2000, 27(1):6-11. 10.1002/1526-968X(200005)27:1<6::AID-GENE20>3.0.CO;2-O, 10862150.
34. Schisler JC, Fueger PT, Babu DA, Hohmeier HE, Tessem JS, Lu D, Becker TC, Naziruddin B, Levy M, Mirmira RG, Newgard CB. Stimulation of human and rat islet beta-cell proliferation with retention of function by the homeodomain transcription factor Nkx6.1. Mol Cell Biol 2008, 28(10):3465-3476. 10.1128/MCB.01791-07, 2423154, 18347054.
35. Bouffi C, Thomas O, Bony C, Giteau A, Venier-Julienne MC, Jorgensen C, Montero-Menei C, Noel D. The role of pharmacologically active microcarriers releasing TGF-beta3 in cartilage formation in vivo by mesenchymal stem cells. Biomaterials 2010, 31(25):6485-6493. 10.1016/j.biomaterials.2010.05.013, 20570347.
36. Gordeladze JO, Noel D, Bony C, Apparailly F, Louis-Plence P, Jorgensen C. Transient down-regulation of cbfa1/Runx2 by RNA interference in murine C3H10T1/2 mesenchymal stromal cells delays in vitro and in vivo osteogenesis, but does not overtly affect chondrogenesis. Exp Cell Res 2008, 314(7):1495-1506. 10.1016/j.yexcr.2007.12.023, 18313048.
37. Deleyrolle L, Marchal-Victorion S, Dromard C, Fritz V, Saunier M, Sabourin JC, Tran Van Ba C, Privat A, Hugnot JP. Exogenous and fibroblast growth factor 2/epidermal growth factor-regulated endogenous cytokines regulate neural precursor cell growth and differentiation. Stem cells (Dayton, Ohio) 2006, 24(3):748-762.
38. Bieche I, Parfait B, Le Doussal V, Olivi M, Rio MC, Lidereau R, Vidaud M. Identification of CGA as a novel estrogen receptor-responsive gene in breast cancer: an outstanding candidate marker to predict the response to endocrine therapy. Cancer Res 2001, 61(4):1652-1658.
39. Marchal-Victorion S, Deleyrolle L, De Weille J, Saunier M, Dromard C, Sandillon F, Privat A, Hugnot JP. The human NTERA2 neural cell line generates neurons on growth under neural stem cell conditions and exhibits characteristics of radial glial cells. Mol Cell Neurosci 2003, 24(1):198-213. 10.1016/S1044-7431(03)00161-1, 14550780.