Developmental cues and persistent neurogenic potential within an in vitro neural niche

BMC Developmental Biology
Chris Pierret1, Jason A. Morrison1, Peter Rath1, Rachel E. Zigler1, Laura A. Engel1, Corinne L. Fairchild1, Huidong Shi2, J.A. Maruniak1, Mark D. Kirk3
1Division of Biological Sciences, University of Missouri, Columbia, MO 65211 (USA)
2Department of Pathology and Anatomical Sciences, University of Missouri School of Medicine, Columbia, MO 65212, USA
3Division of Biological Sciences, University of Missouri, Columbia, MO 65211, USA

Tóm tắt

Abstract Background Neurogenesis, the production of neural cell-types from neural stem cells (NSCs), occurs during development as well as within select regions of the adult brain. NSCs in the adult subependymal zone (SEZ) exist in a well-categorized niche microenvironment established by surrounding cells and their molecular products. The components of this niche maintain the NSCs and their definitive properties, including the ability to self-renew and multipotency (neuronal and glial differentiation). Results We describe a model in vitro NSC niche, derived from embryonic stem cells, that produces many of the cells and products of the developing subventricular zone (SVZ) and adult SEZ NSC niche. We demonstrate a possible role for apoptosis and for components of the extracellular matrix in the maintenance of the NSC population within our niche cultures. We characterize expression of genes relevant to NSC self-renewal and the process of neurogenesis and compare these findings to gene expression produced by an established neural-induction protocol employing retinoic acid. Conclusions The in vitro NSC niche shows an identity that is distinct from the neurally induced embryonic cells that were used to derive it. Molecular and cellular components found in our in vitro NSC niche include NSCs, neural progeny, and ECM components and their receptors. Establishment of the in vitro NSC niche occurs in conjunction with apoptosis. Applications of this culture system range from studies of signaling events fundamental to niche formation and maintenance as well as development of unique NSC transplant platforms to treat disease or injury.

Từ khóa


Tài liệu tham khảo

Alvarez-Buylla A, Lim DA: For the long run: maintaining germinal niches in the adult brain. Neuron. 2004, 41: 683-686. 10.1016/S0896-6273(04)00111-4.

Casper KB, McCarthy KD: GFAP-positive progenitor cells produce neurons and oligodendrocytes throughout the CNS. Mol Cell Neurosci. 2006, 31: 676-684. 10.1016/j.mcn.2005.12.006.

Conover JC, Notti RQ: The neural stem cell niche. Cell Tissue Res. 2008, 331: 211-224. 10.1007/s00441-007-0503-6.

Doetsch F: A niche for adult neural stem cells. Curr Opin Genet Dev. 2003, 13: 543-550. 10.1016/j.gde.2003.08.012.

Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A: Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 1999, 97: 703-716. 10.1016/S0092-8674(00)80783-7.

Jackson EL, Garcia-Verdugo JM, Gil-Perotin S, Roy M, Quinones-Hinojosa A, VandenBerg S, Alvarez-Buylla A: PDGFRalpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron. 2006, 51: 187-199. 10.1016/j.neuron.2006.06.012.

Menn B, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A: Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci. 2006, 26: 7907-7918. 10.1523/JNEUROSCI.1299-06.2006.

Nait-Oumesmar B, Decker L, Lachapelle F, Avellana-Adalid V, Bachelin C, Van Evercooren AB: Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur J Neurosci. 1999, 11: 4357-4366. 10.1046/j.1460-9568.1999.00873.x.

Pierret C, Spears K, Morrison JA, Maruniak JA, Katz ML, Kirk MD: Elements of a neural stem cell niche derived from embryonic stem cells. Stem Cells Dev. 2007, 16: 1017-1026. 10.1089/scd.2007.0012.

Fuchs E, Tumbar T, Guasch G: Socializing with the neighbors: stem cells and their niche. Cell. 2004, 116: 769-778. 10.1016/S0092-8674(04)00255-7.

Ramirez-Castillejo C, Sanchez-Sanchez F, Andreu-Agullo C, Ferron SR, Aroca-Aguilar JD, Sanchez P, Mira H, Escribano J, Farinas I: Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat Neurosci. 2006, 9: 331-339. 10.1038/nn1657.

Mirzadeh Z, Merkle FT, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A: Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell. 2008, 3: 265-278. 10.1016/j.stem.2008.07.004.

Shen Q, Wang Y, Kokovay E, Lin G, Chuang SM, Goderie SK, Roysam B, Temple S: Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell. 2008, 3: 289-300. 10.1016/j.stem.2008.07.026.

Tavazoie M, Veken Van der L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B, Garcia-Verdugo JM, Doetsch F: A specialized vascular niche for adult neural stem cells. Cell Stem Cell. 2008, 3: 279-288. 10.1016/j.stem.2008.07.025.

Javaherian A, Kriegstein A: A stem cell niche for intermediate progenitor cells of the embryonic cortex. Cereb Cortex. 2009, 19 (Suppl 1): i70-77. 10.1093/cercor/bhp029.

Kriegstein A, Alvarez-Buylla A: The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci. 2009, 32: 149-184. 10.1146/annurev.neuro.051508.135600.

Lathia JD, Patton B, Eckley DM, Magnus T, Mughal MR, Sasaki T, Caldwell MA, Rao MS, Mattson MP, ffrench-Constant C: Patterns of laminins and integrins in the embryonic ventricular zone of the CNS. J Comp Neurol. 2007, 505: 630-643. 10.1002/cne.21520.

Lathia JD, Rao MS, Mattson MP, Ffrench-Constant C: The microenvironment of the embryonic neural stem cell: lessons from adult niches?. Dev Dyn. 2007, 236: 3267-3282. 10.1002/dvdy.21319.

Goetz AK, Scheffler B, Chen HX, Wang S, Suslov O, Xiang H, Brustle O, Roper SN, Steindler DA: Temporally restricted substrate interactions direct fate and specification of neural precursors derived from embryonic stem cells. Proc Natl Acad Sci USA. 2006, 103: 11063-11068. 10.1073/pnas.0510926103.

Karpowicz P, Inoue T, Runciman S, Deveale B, Seaberg R, Gertsenstein M, Byers L, Yamanaka Y, Tondat S, Slevin J, et al: Adhesion is prerequisite, but alone insufficient, to elicit stem cell pluripotency. J Neurosci. 2007, 27: 5437-5447. 10.1523/JNEUROSCI.0300-07.2007.

Esposito MS, Piatti VC, Laplagne DA, Morgenstern NA, Ferrari CC, Pitossi FJ, Schinder AF: Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci. 2005, 25: 10074-10086. 10.1523/JNEUROSCI.3114-05.2005.

Hevner RF, Hodge RD, Daza RA, Englund C: Transcription factors in glutamatergic neurogenesis: conserved programs in neocortex, cerebellum, and adult hippocampus. Neurosci Res. 2006, 55: 223-233. 10.1016/j.neures.2006.03.004.

Englund C, Fink A, Lau C, Pham D, Daza RA, Bulfone A, Kowalczyk T, Hevner RF: Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci. 2005, 25: 247-251. 10.1523/JNEUROSCI.2899-04.2005.

Kalinichenko SG, Matveeva NY: Morphological characteristics of apoptosis and its significance in neurogenesis. Neurosci Behav Physiol. 2008, 38: 333-344. 10.1007/s11055-008-0046-7.

Rakic S, Zecevic N: Programmed cell death in the developing human telencephalon. Eur J Neurosci. 2000, 12: 2721-2734. 10.1046/j.1460-9568.2000.00153.x.

Meier P, Finch A, Evan G: Apoptosis in development. Nature. 2000, 407: 796-801. 10.1038/35037734.

Conti L, Pollard SM, Gorba T, Reitano E, Toselli M, Biella G, Sun Y, Sanzone S, Ying QL, Cattaneo E, Smith A: Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol. 2005, 3: e283-10.1371/journal.pbio.0030283.

Lee SH, Lumelsky N, Studer L, Auerbach JM, McKay RD: Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat Biotechnol. 2000, 18: 675-679. 10.1038/76536.

Lenka N, Lu ZJ, Sasse P, Hescheler J, Fleischmann BK: 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.

Lenka N, Ramasamy SK: Neural induction from ES cells portrays default commitment but instructive maturation. PLoS ONE. 2007, 2: e1349-10.1371/journal.pone.0001349.

Okabe S, Forsberg-Nilsson K, Spiro AC, Segal M, McKay RD: Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech Dev. 1996, 59: 89-102. 10.1016/0925-4773(96)00572-2.

Tropepe V, Hitoshi S, Sirard C, Mak TW, Rossant J, Kooy vander D: Direct neural fate specification from embryonic stem cells: a primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron. 2001, 30: 65-78. 10.1016/S0896-6273(01)00263-X.

Yamazoe H, Kobori M, Murakami Y, Yano K, Satoh M, Mizuseki K, Sasai Y, Iwata H: One-step induction of neurons from mouse embryonic stem cells in serum-free media containing vitamin B12 and heparin. Cell Transplant. 2006, 15: 135-145. 10.3727/000000006783982061.

Bain G, Kitchens D, Yao M, Huettner JE, Gottlieb DI: Embryonic stem cells express neuronal properties in vitro. Dev Biol. 1995, 168: 342-357. 10.1006/dbio.1995.1085.

Meyer JS, Katz ML, Maruniak JA, Kirk MD: Neural differentiation of mouse embryonic stem cells in vitro and after transplantation into eyes of mutant mice with rapid retinal degeneration. Brain Res. 2004, 1014: 131-144. 10.1016/j.brainres.2004.04.019.

Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A: Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci. 1997, 17: 5046-5061.

Batista CM, Kippin TE, Willaime-Morawek S, Shimabukuro MK, Akamatsu W, Kooy van der D: A progressive and cell non-autonomous increase in striatal neural stem cells in the Huntington's disease R6/2 mouse. J Neurosci. 2006, 26: 10452-10460. 10.1523/JNEUROSCI.2850-06.2006.

Corti S, Nizzardo M, Nardini M, Donadoni C, Locatelli F, Papadimitriou D, Salani S, Del Bo R, Ghezzi S, Strazzer S, et al: Isolation and characterization of murine neural stem/progenitor cells based on Prominin-1 expression. Exp Neurol. 2007, 205: 547-562. 10.1016/j.expneurol.2007.03.021.

Cohen GM: Caspases: the executioners of apoptosis. Biochem J. 1997, 326 (Pt 1): 1-16.

Su D, Gudas LJ: Retinoic acid receptor gamma activates receptor tyrosine kinase Tie1 gene transcription through transcription factor GATA4 in F9 stem cells. Exp Hematol. 2008, 36: 624-641. 10.1016/j.exphem.2007.12.016.

Ruberte E, Friederich V, Chambon P, Morriss-Kay G: Retinoic acid receptors and cellular retinoid binding proteins. III. Their differential transcript distribution during mouse nervous system development. Development. 1993, 118: 267-282.

Chiaruttini C, Sonego M, Baj G, Simonato M, Tongiorgi E: BDNF mRNA splice variants display activity-dependent targeting to distinct hippocampal laminae. Mol Cell Neurosci. 2008, 37: 11-19. 10.1016/j.mcn.2007.08.011.

Brazel CY, Limke TL, Osborne JK, Miura T, Cai J, Pevny L, Rao MS: Sox2 expression defines a heterogeneous population of neurosphere-forming cells in the adult murine brain. Aging Cell. 2005, 4: 197-207. 10.1111/j.1474-9726.2005.00158.x.

Miura K, Law SW, Nishi S, Tamaoki T: Isolation of alpha-fetoprotein messenger RNA from mouse yolk sac. J Biol Chem. 1979, 254: 5515-5521.

Robson P, Stein P, Zhou B, Schultz RM, Baldwin HS: Inner cell mass-specific expression of a cell adhesion molecule (PECAM-1/CD31) in the mouse blastocyst. Dev Biol. 2001, 234: 317-329. 10.1006/dbio.2001.0274.

Bader BL, Smyth N, Nedbal S, Miosge N, Baranowsky A, Mokkapati S, Murshed M, Nischt R: Compound genetic ablation of nidogen 1 and 2 causes basement membrane defects and perinatal lethality in mice. Mol Cell Biol. 2005, 25: 6846-6856. 10.1128/MCB.25.15.6846-6856.2005.

Miosge N, Sasaki T, Timpl R: Evidence of nidogen-2 compensation for nidogen-1 deficiency in transgenic mice. Matrix Biol. 2002, 21: 611-621. 10.1016/S0945-053X(02)00070-7.

Murshed M, Smyth N, Miosge N, Karolat J, Krieg T, Paulsson M, Nischt R: The absence of nidogen 1 does not affect murine basement membrane formation. Mol Cell Biol. 2000, 20: 7007-7012. 10.1128/MCB.20.18.7007-7012.2000.

Salmivirta K, Talts JF, Olsson M, Sasaki T, Timpl R, Ekblom P: Binding of mouse nidogen-2 to basement membrane components and cells and its expression in embryonic and adult tissues suggest complementary functions of the two nidogens. Exp Cell Res. 2002, 279: 188-201. 10.1006/excr.2002.5611.

Bonaguidi MA, McGuire T, Hu M, Kan L, Samanta J, Kessler JA: LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells. Development. 2005, 132: 5503-5514. 10.1242/dev.02166.

Pfenninger CV, Roschupkina T, Hertwig F, Kottwitz D, Englund E, Bengzon J, Jacobsen SE, Nuber UA: CD133 is not present on neurogenic astrocytes in the adult subventricular zone, but on embryonic neural stem cells, ependymal cells, and glioblastoma cells. Cancer Res. 2007, 67: 5727-5736. 10.1158/0008-5472.CAN-07-0183.

Martinez-Agosto JA, Mikkola HK, Hartenstein V, Banerjee U: The hematopoietic stem cell and its niche: a comparative view. Genes Dev. 2007, 21: 3044-3060. 10.1101/gad.1602607.

Winkler S, Stahl RC, Carey DJ, Bansal R: Syndecan-3 and perlecan are differentially expressed by progenitors and mature oligodendrocytes and accumulate in the extracellular matrix. J Neurosci Res. 2002, 69: 477-487. 10.1002/jnr.10311.

Nusse R: Wnt signaling and stem cell control. Cell Res. 2008, 18: 523-527. 10.1038/cr.2008.47.

Jacques TS, Relvas JB, Nishimura S, Pytela R, Edwards GM, Streuli CH, ffrench-Constant C: Neural precursor cell chain migration and division are regulated through different beta1 integrins. Development. 1998, 125: 3167-3177.

Pettmann B, Henderson CE: Neuronal cell death. Neuron. 1998, 20: 633-647. 10.1016/S0896-6273(00)81004-1.

Horky M, Kotala V, Anton M, Wesierska-Gadek J: Nucleolus and apoptosis. Ann N Y Acad Sci. 2002, 973: 258-264. 10.1111/j.1749-6632.2002.tb04645.x.

Meyer JS, Katz ML, Maruniak JA, Kirk MD: Embryonic stem cell-derived neural progenitors incorporate into degenerating retina and enhance survival of host photoreceptors. Stem Cells. 2006, 24: 274-283. 10.1634/stemcells.2005-0059.

Conti L, Cattaneo E: Novel and immortalization-based protocols for the generation of neural CNS stem cell lines for gene therapy approaches. Methods Mol Biol. 2008, 438: 319-332. full_text.

Bibel M, Richter J, Schrenk K, Tucker KL, Staiger V, Korte M, Goetz M, Barde YA: Differentiation of mouse embryonic stem cells into a defined neuronal lineage. Nat Neurosci. 2004, 7: 1003-1009. 10.1038/nn1301.

Reynolds BA, Weiss S: Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 1992, 255: 1707-1710. 10.1126/science.1553558.

Garcion E, Halilagic A, Faissner A, ffrench-Constant C: Generation of an environmental niche for neural stem cell development by the extracellular matrix molecule tenascin C. Development. 2004, 131: 3423-3432. 10.1242/dev.01202.

Piao JH, Odeberg J, Samuelsson EB, Kjaeldgaard A, Falci S, Seiger A, Sundstrom E, Akesson E: Cellular composition of long-term human spinal cord- and forebrain-derived neurosphere cultures. J Neurosci Res. 2006, 84: 471-482. 10.1002/jnr.20955.

Giachino C, Basak O, Taylor V: Isolation and manipulation of mammalian neural stem cells in vitro. Methods Mol Biol. 2009, 482: 143-158. full_text.

Serban MA, Prestwich GD: Modular extracellular matrices: Solutions for the puzzle. Methods. 2008, 45: 93-98. 10.1016/j.ymeth.2008.01.010.

Milner R: A novel three-dimensional system to study interactions between endothelial cells and neural cells of the developing central nervous system. BMC Neurosci. 2007, 8: 3-10.1186/1471-2202-8-3.

Kullenberg J, Rosatini F, Vozzi G, Bianchi F, Ahluwalia A, Domenici C: Optimization of PAM Scaffolds for Neural Tissue Engineering: Preliminary Study on an SH-SY5Y Cell Line. Tissue Eng Part A. 2008, 14 (6): 1017-23. 10.1089/ten.tea.2007.0163.

Horii A, Wang X, Gelain F, Zhang S: Biological designer self-assembling Peptide nanofiber scaffolds significantly enhance osteoblast proliferation, differentiation and 3-D migration. PLoS ONE. 2007, 2: e190-10.1371/journal.pone.0000190.

Holmes TC, de Lacalle S, Su X, Liu G, Rich A, Zhang S: Extensive neurite outgrowth and active synapse formation on self-assembling peptide scaffolds. Proc Natl Acad Sci USA. 2000, 97: 6728-6733. 10.1073/pnas.97.12.6728.

Gelain F, Horii A, Zhang S: Designer self-assembling peptide scaffolds for 3-d tissue cell cultures and regenerative medicine. Macromol Biosci. 2007, 7: 544-551. 10.1002/mabi.200700033.

Wendt KD, Jensen CA, Tindall R, Katz ML: Comparison of conventional and microwave-assisted processing of mouse retinas for transmission electron microscopy. J Microsc. 2004, 214: 80-88. 10.1111/j.0022-2720.2004.01310.x.

Sato T: A modified method for lead staining of thin sections. J Electron Microsc (Tokyo). 1968, 17: 158-159.

Benninger F, Beck H, Wernig M, Tucker KL, Brustle O, Scheffler B: Functional integration of embryonic stem cell-derived neurons in hippocampal slice cultures. J Neurosci. 2003, 23: 7075-7083.

Meyer JS, Tullis G, Pierret C, Spears KM, Morrison JA, Kirk MD: Detection of Calcium Transients in Embryonic Stem Cells and Their Differentiated Progeny. Cell Mol Neurobiol. 2009

Stoppini L, Buchs PA, Muller D: A simple method for organotypic cultures of nervous tissue. J Neurosci Methods. 1991, 37: 173-182. 10.1016/0165-0270(91)90128-M.

Thông tin
Thông tin xuất bản

BMC Developmental Biology

Thông tin tác giả