Novel stem/progenitor cells with neuronal differentiation potential reside in the leptomeningeal niche

被引:57
作者
Bifari, Francesco
Decimo, Ilaria [2 ]
Chiamulera, Christian [2 ]
Bersan, Emanuela [2 ]
Malpeli, Giorgio [3 ]
Johansson, Jan [2 ]
Lisi, Veronica
Bonetti, Bruno [4 ]
Fumagalli, Guido [2 ]
Pizzolo, Giovanni
Krampera, Mauro [1 ]
机构
[1] Univ Verona, Policlin GB Rossi, Dept Clin & Expt Med, Stem Cell Res Lab,Sect Hematol, I-37134 Verona, Italy
[2] Univ Verona, Dept Med & Publ Hlth, Pharmacol Sect, I-37134 Verona, Italy
[3] Univ Verona, Dept Pathol, Sect Pathol Anat, I-37134 Verona, Italy
[4] Univ Verona, Dept Neurol & Vis Sci, Neurol Sect, I-37134 Verona, Italy
关键词
neural stem cells; leptomeninges; stem cell niche; neuronal differentiation; NEURAL STEM-CELL; CAJAL-RETZIUS CELLS; BASEMENT-MEMBRANE; ENDOTHELIAL-CELLS; PURKINJE NEURONS; PROGENITOR; MIGRATION; NEUROGENESIS; EXPRESSION; MOUSE;
D O I
10.1111/j.1582-4934.2009.00706.x
中图分类号
Q2 [细胞生物学];
学科分类号
071013 [干细胞生物学];
摘要
Stem cells capable of generating neural differentiated cells are recognized by the expression of nestin and reside in specific regions of the brain, namely, hippocampus, subventricular zone and olfactory bulb. For other brain structures, such as leptomeninges, which contribute to the correct cortex development and functions, there is no evidence so far that they may contain stem/precursor cells. In this work, we show for the first time that nestin-positive cells are present in rat leptomeninges during development up to adulthood. The newly identified nestin-positive cells can be extracted and expanded in vitro both as neurospheres, displaying high similarity with subventricular zone-derived neural stem cells, and as homogeneous cell population with stem cell features. In vitro expanded stem cell population can differentiate with high efficiency into excitable cells with neuronal phenotype and morphology. Once injected into the adult brain, these cells survive and differentiate into neurons, thus showing that their neuronal differentiation potential is operational also in vivo. In conclusion, our data provide evidence that a specific population of immature cells endowed of neuronal differentiation potential is resident in the leptomeninges throughout the life. As leptomeninges cover the entire central nervous system, these findings could have relevant implications for studies on cortical development and for regenerative medicine applied to neurological disorders.
引用
收藏
页码:3195 / 3208
页数:14
相关论文
共 63 条
[1]
Characterization of human embryonic stem cell lines by the International Stem Cell Initiative [J].
Adewumi, Oluseun ;
Aflatoonian, Behrouz ;
Ahrlund-Richter, Lars ;
Amit, Michal ;
Andrews, Peter W. ;
Beighton, Gemma ;
Bello, Paul A. ;
Benvenisty, Nissim ;
Berry, Lorraine S. ;
Bevan, Simon ;
Blum, Barak ;
Brooking, Justin ;
Chen, Kevin G. ;
Choo, Andre B. H. ;
Churchill, Gary A. ;
Corbel, Marie ;
Damjanov, Ivan ;
Draper, Jon S. ;
Dvorak, Petr ;
Emanuelsson, Katarina ;
Fleck, Roland A. ;
Ford, Angela ;
Gertow, Karin ;
Gertsenstein, Marina ;
Gokhale, Paul J. ;
Hamilton, Rebecca S. ;
Hampl, Ales ;
Healy, Lyn E. ;
Hovatta, Outi ;
Hyllner, Johan ;
Imreh, Marta P. ;
Itskovitz-Eldor, Joseph ;
Jackson, Jamie ;
Johnson, Jacqueline L. ;
Jones, Mark ;
Kee, Kehkooi ;
King, Benjamin L. ;
Knowles, Barbara B. ;
Lako, Majlinda ;
Lebrin, Franck ;
Mallon, Barbara S. ;
Manning, Daisy ;
Mayshar, Yoav ;
Mckay, Ronald D. G. ;
Michalska, Anna E. ;
Mikkola, Milla ;
Mileikovsky, Masha ;
Minger, Stephen L. ;
Moore, Harry D. ;
Mummery, Christine L. .
NATURE BIOTECHNOLOGY, 2007, 25 (07) :803-816
[2]
Identification of neural progenitors in the adult mammalian eye [J].
Ahmad, I ;
Tang, L ;
Pham, H .
BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS, 2000, 270 (02) :517-521
[3]
Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes [J].
Alvarez-Dolado, M ;
Pardal, R ;
Garcia-Vardugo, JM ;
Fike, JR ;
Lee, HO ;
Pfeffer, K ;
Lois, C ;
Morrison, SJ ;
Alvarez-Buylla, A .
NATURE, 2003, 425 (6961) :968-973
[4]
Multipotent cell lineages in early mouse development depend on SOX2 function [J].
Avilion, AA ;
Nicolis, SK ;
Pevny, LH ;
Perez, L ;
Vivian, N ;
Lovell-Badge, R .
GENES & DEVELOPMENT, 2003, 17 (01) :126-140
[5]
FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies [J].
Beggs, HE ;
Schahin-Reed, D ;
Zang, KL ;
Goebbels, S ;
Nave, KA ;
Gorski, J ;
Jones, KR ;
Sretavan, D ;
Reichardt, LF .
NEURON, 2003, 40 (03) :501-514
[6]
Neurosphere and neurosphere-forming cells: morphological and ultrastructural characterization [J].
Bez, A ;
Corsini, E ;
Curti, D ;
Biggiogera, M ;
Colombo, A ;
Nicosia, RF ;
Pagano, SF ;
Parati, EA .
BRAIN RESEARCH, 2003, 993 (1-2) :18-29
[7]
Meninges control tangential migration of hem-derived Cajal-Retzius cells via CXCL12/CXCR4 signaling [J].
Borrell, Victor ;
Marin, Oscar .
NATURE NEUROSCIENCE, 2006, 9 (10) :1284-1293
[8]
Production of neurons, astrocytes and oligodendrocytes from mammalian CNS stem cells [J].
Chojnacki, Andrew ;
Weiss, Samuel .
NATURE PROTOCOLS, 2008, 3 (06) :935-940
[9]
Neuronal migration defects in the Dreher (Lmx1a) mutant mouse:: Role of disorders of the glial limiting membrane [J].
Costa, C ;
Harding, B ;
Copp, AJ .
CEREBRAL CORTEX, 2001, 11 (06) :498-505
[10]
A perivascular origin for mesenchymal stem cells in multiple human organs [J].
Crisan, Mihaela ;
Yap, Solomon ;
Casteilla, Louis ;
Chen, Chien-Wen ;
Corselli, Mirko ;
Park, Tea Soon ;
Andriolo, Gabriella ;
Sun, Bin ;
Zheng, Bo ;
Zhang, Li ;
Norotte, Cyrille ;
Teng, Pang-Ning ;
Traas, Jeremy ;
Schugar, Rebecca ;
Deasy, Bridget M. ;
Badylak, Stephen ;
Buehring, Hans-Joerg ;
Giacobino, Jean-Paul ;
Lazzari, Lorenza ;
Huard, Johnny ;
Peault, Bruno .
CELL STEM CELL, 2008, 3 (03) :301-313