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PLOS ONE  2012 

The Molecular Profiles of Neural Stem Cell Niche in the Adult Subventricular Zone

DOI: 10.1371/journal.pone.0050501

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Abstract:

Neural stem cells (NSCs) reside in a unique microenvironment called the neurogenic niche and generate functional new neurons. The neurogenic niche contains several distinct types of cells and interacts with the NSCs in the subventricular zone (SVZ) of the lateral ventricle. While several molecules produced by the niche cells have been identified to regulate adult neurogenesis, a systematic profiling of autocrine/paracrine signaling molecules in the neurogenic regions involved in maintenance, self-renewal, proliferation, and differentiation of NSCs has not been done. We took advantage of the genetic inducible fate mapping system (GIFM) and transgenic mice to isolate the SVZ niche cells including NSCs, transit-amplifying progenitors (TAPs), astrocytes, ependymal cells, and vascular endothelial cells. From the isolated cells and microdissected choroid plexus, we obtained the secretory molecule expression profiling (SMEP) of each cell type using the Signal Sequence Trap method. We identified a total of 151 genes encoding secretory or membrane proteins. In addition, we obtained the potential SMEP of NSCs using cDNA microarray technology. Through the combination of multiple screening approaches, we identified a number of candidate genes with a potential relevance for regulating the NSC behaviors, which provide new insight into the nature of neurogenic niche signals.

References

[1]  Kriegstein A, Alvarez-Buylla A (2009) The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32: 149–184.
[2]  Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28: 223–250.
[3]  Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132: 645–660.
[4]  Alvarez-Buylla A, Lim DA (2004) For the long run: maintaining germinal niches in the adult brain. Neuron 41: 683–686.
[5]  Doetsch F (2003) A niche for adult neural stem cells. Curr Opin Genet Dev 13: 543–550.
[6]  Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264: 1145–1148.
[7]  Suhonen JO, Peterson DA, Ray J, Gage FH (1996) Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature 383: 624–627.
[8]  Ihrie RA, Alvarez-Buylla A (2011) Lake-front property: a unique germinal niche by the lateral ventricles of the adult brain. Neuron 70: 674–686.
[9]  Miller FD, Gauthier-Fisher A (2009) Home at last: neural stem cell niches defined. Cell Stem Cell 4: 507–510.
[10]  Mu Y, Lee SW, Gage FH (2010) Signaling in adult neurogenesis. Curr Opin Neurobiol 20: 416–423.
[11]  Doetsch F, García-Verdugo JM, Alvarez-Buylla A (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17: 5046–5061.
[12]  Lledo PM, Merkle FT, Alvarez-Buylla A (2008) Origin and function of olfactory bulb interneuron diversity. Trends Neurosci 31: 392–400.
[13]  Smith DE, Johanson CE, Keep RF (2004) Peptide and peptide analog transport systems at the blood-CSF barrier. Adv Drug Deliv Rev 56: 1765–1791.
[14]  Mirzadeh Z, Merkle FT, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A (2008) Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3: 265–278.
[15]  Palmer TD, Willhoite AR, Gage FH (2000) Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425: 479–494.
[16]  Tavazoie M, Van der Veken L, Silva-Vargas V, Louissaint M, Colonna L, et al. (2008) A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3: 279–288.
[17]  Ramírez-Castillejo C, Sánchez-Sánchez F, Andreu-Agulló C, Ferrón SR, Aroca-Aguilar JD, et al. (2006) Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat Neurosci 9: 331–339.
[18]  Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, et al. (2004) Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304: 1338–1340.
[19]  Lim DA, Alvarez-Buylla A (1999) Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc Natl Acad Sci U S A 96: 7526–7531.
[20]  Han YG, Spassky N, Romaguera-Ros M, Garcia-Verdugo JM, Aguilar A, et al. (2008) Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat Neurosci 11: 277–284.
[21]  Singla V, Reiter JF (2006) The primary cilium as the cell’s antenna: signaling at a sensory organelle. Science 313: 629–633.
[22]  Johanson CE, Duncan JA, Klinge PM, Brinker T, Stopa EG, et al. (2008) Multiplicity of cerebrospinal fluid functions: New challenges in health and disease. Cerebrospinal Fluid Res 5: 10.
[23]  Ahn S, Joyner AL (2005) In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 437: 894–897.
[24]  Lim DA, Tramontin AD, Trevejo JM, Herrera DG, García-Verdugo JM, et al. (2000) Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28: 713–726.
[25]  Palma V, Lim DA, Dahmane N, Sánchez P, Brionne TC, et al. (2005) Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development 132: 335–344.
[26]  Qu Q, Sun G, Li W, Yang S, Ye P, et al.. (2010) Orphan nuclear receptor TLX activates Wnt/beta-catenin signalling to stimulate neural stem cell proliferation and self-renewal. Nat Cell Biol 12: 31–40; sup 1–9.
[27]  Aguirre A, Rubio ME, Gallo V (2010) Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature 467: 323–327.
[28]  Craig CG, Tropepe V, Morshead CM, Reynolds BA, Weiss S, et al. (1996) In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci 16: 2649–2658.
[29]  Garcion E, Halilagic A, Faissner A, ffrench-Constant C (2004) Generation of an environmental niche for neural stem cell development by the extracellular matrix molecule tenascin C. Development. 131: 3423–3432.
[30]  Palmer TD, Ray J, Gage FH (1995) FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol Cell Neurosci 6: 474–486.
[31]  Zigova T, Pencea V, Wiegand SJ, Luskin MB (1998) Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol Cell Neurosci 11: 234–245.
[32]  Taupin P, Ray J, Fischer WH, Suhr ST, Hakansson K, et al. (2000) FGF-2-responsive neural stem cell proliferation requires CCg, a novel autocrine/paracrine cofactor. Neuron 28: 385–397.
[33]  Tham M, Ramasamy S, Gan HT, Ramachandran A, Poonepalli A, et al. (2010) CSPG is a secreted factor that stimulates neural stem cell survival possibly by enhanced EGFR signaling. PLoS One 5: e15341.
[34]  Gómez-Gaviro MV, Scott CE, Sesay AK, Matheu A, Booth S, et al.. (2012) Betacellulin promotes cell proliferation in the neural stem cell niche and stimulates neurogenesis. Proc Natl Acad Sci U S A.
[35]  Kojima T, Kitamura T (1999) A signal sequence trap based on a constitutively active cytokine receptor. Nat Biotechnol 17: 487–490.
[36]  Matsubara A, Iwama A, Yamazaki S, Furuta C, Hirasawa R, et al. (2005) Endomucin, a CD34-like sialomucin, marks hematopoietic stem cells throughout development. J Exp Med 202: 1483–1492.
[37]  Ikeda Y, Imai Y, Kumagai H, Nosaka T, Morikawa Y, et al. (2004) Vasorin, a transforming growth factor beta-binding protein expressed in vascular smooth muscle cells, modulates the arterial response to injury in vivo. Proc Natl Acad Sci U S A 101: 10732–10737.
[38]  Isodono K, Takahashi T, Imoto H, Nakanishi N, Ogata T, et al. (2010) PARM-1 is an endoplasmic reticulum molecule involved in endoplasmic reticulum stress-induced apoptosis in rat cardiac myocytes. PLoS One 5: e9746.
[39]  Toda H, Tsuji M, Nakano I, Kobuke K, Hayashi T, et al. (2003) Stem cell-derived neural stem/progenitor cell supporting factor is an autocrine/paracrine survival factor for adult neural stem/progenitor cells. J Biol Chem 278: 35491–35500.
[40]  Vigon I, Mornon JP, Cocault L, Mitjavila MT, Tambourin P, et al. (1992) Molecular cloning and characterization of MPL, the human homolog of the v-mpl oncogene: identification of a member of the hematopoietic growth factor receptor superfamily. Proc Natl Acad Sci U S A 89: 5640–5644.
[41]  Onishi M, Mui AL, Morikawa Y, Cho L, Kinoshita S, et al. (1996) Identification of an oncogenic form of the thrombopoietin receptor MPL using retrovirus-mediated gene transfer. Blood 88: 1399–1406.
[42]  Ahn S, Joyner AL (2004) Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 118: 505–516.
[43]  Zhuo L, Sun B, Zhang CL, Fine A, Chiu SY, et al. (1997) Live astrocytes visualized by green fluorescent protein in transgenic mice. Dev Biol 187: 36–42.
[44]  Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, et al. (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13: 133–140.
[45]  Zhang Y, Huang G, Shornick LP, Roswit WT, Shipley JM, et al. (2007) A transgenic FOXJ1-Cre system for gene inactivation in ciliated epithelial cells. Am J Respir Cell Mol Biol 36: 515–519.
[46]  Motoike T, Loughna S, Perens E, Roman BL, Liao W, et al. (2000) Universal GFP reporter for the study of vascular development. Genesis 28: 75–81.
[47]  Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, et al. (1999) Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23: 99–103.
[48]  Morita S, Kojima T, Kitamura T (2000) Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther 7: 1063–1066.
[49]  Palacios R, Steinmetz M (1985) Il-3-dependent mouse clones that express B-220 surface antigen, contain Ig genes in germ-line configuration, and generate B lymphocytes in vivo. Cell 41: 727–734.
[50]  Kitamura T, Onishi M, Kinoshita S, Shibuya A, Miyajima A, et al. (1995) Efficient screening of retroviral cDNA expression libraries. Proc Natl Acad Sci U S A 92: 9146–9150.
[51]  Guo G, Huss M, Tong GQ, Wang C, Li Sun L, et al. (2010) Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev Cell 18: 675–685.
[52]  Kippin TE, Kapur S, van der Kooy D (2005) Dopamine specifically inhibits forebrain neural stem cell proliferation, suggesting a novel effect of antipsychotic drugs. J Neurosci 25: 5815–5823.
[53]  Doetsch F, Caillé I, Lim DA, García-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97: 703–716.
[54]  Ferri AL, Cavallaro M, Braida D, Di Cristofano A, Canta A, et al. (2004) Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development 131: 3805–3819.
[55]  Komitova M, Eriksson PS (2004) Sox-2 is expressed by neural progenitors and astroglia in the adult rat brain. Neurosci Lett 369: 24–27.
[56]  Jacquet BV, Salinas-Mondragon R, Liang H, Therit B, Buie JD, et al. (2009) FoxJ1-dependent gene expression is required for differentiation of radial glia into ependymal cells and a subset of astrocytes in the postnatal brain. Development 136: 4021–4031.
[57]  Parras CM, Galli R, Britz O, Soares S, Galichet C, et al. (2004) Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J 23: 4495–4505.
[58]  Calaora V, Chazal G, Nielsen PJ, Rougon G, Moreau H (1996) mCD24 expression in the developing mouse brain and in zones of secondary neurogenesis in the adult. Neuroscience 73: 581–594.
[59]  Morshead CM, Reynolds BA, Craig CG, McBurney MW, Staines WA, et al. (1994) Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13: 1071–1082.
[60]  Beckervordersandforth R, Tripathi P, Ninkovic J, Bayam E, Lepier A, et al. (2010) In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. Cell Stem Cell 7: 744–758.
[61]  Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A (2002) EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36: 1021–1034.
[62]  Pastrana E, Cheng LC, Doetsch F (2009) Simultaneous prospective purification of adult subventricular zone neural stem cells and their progeny. Proc Natl Acad Sci U S A 106: 6387–6392.
[63]  Dennis G, Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3.
[64]  Pennartz S, Belvindrah R, Tomiuk S, Zimmer C, Hofmann K, et al. (2004) Purification of neuronal precursors from the adult mouse brain: comprehensive gene expression analysis provides new insights into the control of cell migration, differentiation, and homeostasis. Mol Cell Neurosci 25: 692–706.
[65]  Corrales JD, Rocco GL, Blaess S, Guo Q, Joyner AL (2004) Spatial pattern of sonic hedgehog signaling through Gli genes during cerebellum development. Development 131: 5581–5590.
[66]  Pinto L, G?tz M (2007) Radial glial cell heterogeneity–the source of diverse progeny in the CNS. Prog Neurobiol 83: 2–23.
[67]  Scudiero DA, Shoemaker RH, Paull KD, Monks A, Tierney S, et al. (1988) Evaluation of a soluble tetrazolium/formazan assay for cell growth and drug sensitivity in culture using human and other tumor cell lines. Cancer Res 48: 4827–4833.
[68]  Stracke ML, Krutzsch HC, Unsworth EJ, Arestad A, Cioce V, et al. (1992) Identification, purification, and partial sequence analysis of autotaxin, a novel motility-stimulating protein. J Biol Chem 267: 2524–2529.
[69]  Umezu-Goto M, Kishi Y, Taira A, Hama K, Dohmae N, et al. (2002) Autotaxin has lysophospholipase D activity leading to tumor cell growth and motility by lysophosphatidic acid production. J Cell Biol 158: 227–233.
[70]  Houben AJ, Moolenaar WH (2011) Autotaxin and LPA receptor signaling in cancer. Cancer Metastasis Rev 30: 557–565.
[71]  Choi JW, Herr DR, Noguchi K, Yung YC, Lee CW, et al. (2010) LPA receptors: subtypes and biological actions. Annu Rev Pharmacol Toxicol 50: 157–186.
[72]  Svetlov SI, Ignatova TN, Wang KK, Hayes RL, English D, et al. (2004) Lysophosphatidic acid induces clonal generation of mouse neurospheres via proliferation of Sca-1- and AC133-positive neural progenitors. Stem Cells Dev 13: 685–693.
[73]  Dickson PW, Aldred AR, Menting JG, Marley PD, Sawyer WH, et al. (1987) Thyroxine transport in choroid plexus. J Biol Chem 262: 13907–13915.
[74]  Dussault JH, Ruel J (1987) Thyroid hormones and brain development. Annu Rev Physiol 49: 321–334.
[75]  Ambrogini P, Cuppini R, Ferri P, Mancini C, Ciaroni S, et al. (2005) Thyroid hormones affect neurogenesis in the dentate gyrus of adult rat. Neuroendocrinology 81: 244–253.
[76]  Lemkine GF, Raj A, Alfama G, Turque N, Hassani Z, et al. (2005) Adult neural stem cell cycling in vivo requires thyroid hormone and its alpha receptor. FASEB J 19: 863–865.
[77]  Gongidi V, Ring C, Moody M, Brekken R, Sage EH, et al. (2004) SPARC-like 1 regulates the terminal phase of radial glia-guided migration in the cerebral cortex. Neuron 41: 57–69.
[78]  Lively S, Brown IR (2008) Extracellular matrix protein SC1/hevin in the hippocampus following pilocarpine-induced status epilepticus. J Neurochem 107: 1335–1346.
[79]  Sullivan MM, Sage EH (2004) Hevin/SC1, a matricellular glycoprotein and potential tumor-suppressor of the SPARC/BM-40/Osteonectin family. Int J Biochem Cell Biol 36: 991–996.
[80]  Claeskens A, Ongenae N, Neefs JM, Cheyns P, Kaijen P, et al. (2000) Hevin is down-regulated in many cancers and is a negative regulator of cell growth and proliferation. Br J Cancer 82: 1123–1130.
[81]  Soderling JA, Reed MJ, Corsa A, Sage EH (1997) Cloning and expression of murine SC1, a gene product homologous to SPARC. J Histochem Cytochem 45: 823–835.
[82]  Whitman MC, Fan W, Rela L, Rodriguez-Gil DJ, Greer CA (2009) Blood vessels form a migratory scaffold in the rostral migratory stream. J Comp Neurol 516: 94–104.
[83]  Fricker LD (1988) Carboxypeptidase E. Annu Rev Physiol. 50: 309–321.
[84]  Cawley NX, Wetsel WC, Murthy SR, Park JJ, Pacak K, et al.. (2012) New Roles of Carboxypeptidase E in Endocrine and Neural Function and Cancer. Endocr Rev.
[85]  Cool DR, Normant E, Shen F, Chen HC, Pannell L, et al. (1997) Carboxypeptidase E is a regulated secretory pathway sorting receptor: genetic obliteration leads to endocrine disorders in Cpe(fat) mice. Cell 88: 73–83.
[86]  Lou H, Kim SK, Zaitsev E, Snell CR, Lu B, et al. (2005) Sorting and activity-dependent secretion of BDNF require interaction of a specific motif with the sorting receptor carboxypeptidase e. Neuron 45: 245–255.
[87]  H?ring E, Harter PN, Seznec J, Schittenhelm J, Bühring HJ, et al.. (2012) The “go or grow” potential of gliomas is linked to the neuropeptide processing enzyme carboxypeptidase E and mediated by metabolic stress. Acta Neuropathol.
[88]  Lee TK, Murthy SR, Cawley NX, Dhanvantari S, Hewitt SM, et al. (2011) An N-terminal truncated carboxypeptidase E splice isoform induces tumor growth and is a biomarker for predicting future metastasis in human cancers. J Clin Invest 121: 880–892.
[89]  Koshimizu H, Senatorov V, Loh YP, Gozes I (2009) Neuroprotective protein and carboxypeptidase E. J Mol Neurosci. 39: 1–8.
[90]  Carrel D, Du Y, Komlos D, Hadzimichalis NM, Kwon M, et al. (2009) NOS1AP regulates dendrite patterning of hippocampal neurons through a carboxypeptidase E-mediated pathway. J Neurosci 29: 8248–8258.
[91]  Woronowicz A, Cawley NX, Chang SY, Koshimizu H, Phillips AW, et al. (2010) Carboxypeptidase E knockout mice exhibit abnormal dendritic arborization and spine morphology in central nervous system neurons. J Neurosci Res 88: 64–72.
[92]  Barraud P, Thompson L, Kirik D, Bj?rklund A, Parmar M (2005) Isolation and characterization of neural precursor cells from the Sox1-GFP reporter mouse. Eur J Neurosci 22: 1555–1569.
[93]  Kawaguchi A, Miyata T, Sawamoto K, Takashita N, Murayama A, et al. (2001) Nestin-EGFP transgenic mice: visualization of the self-renewal and multipotency of CNS stem cells. Mol Cell Neurosci 17: 259–273.
[94]  Lim DA, Suárez-Fari?as M, Naef F, Hacker CR, Menn B, et al. (2006) In vivo transcriptional profile analysis reveals RNA splicing and chromatin remodeling as prominent processes for adult neurogenesis. Mol Cell Neurosci 31: 131–148.
[95]  Rietze RL, Valcanis H, Brooker GF, Thomas T, Voss AK, et al. (2001) Purification of a pluripotent neural stem cell from the adult mouse brain. Nature 412: 736–739.
[96]  Luo J, Shook BA, Daniels SB, Conover JC (2008) Subventricular zone-mediated ependyma repair in the adult mammalian brain. J Neurosci 28: 3804–3813.
[97]  Luo J, Daniels SB, Lennington JB, Notti RQ, Conover JC (2006) The aging neurogenic subventricular zone. Aging Cell 5: 139–152.
[98]  Urade Y, Kitahama K, Ohishi H, Kaneko T, Mizuno N, et al. (1993) Dominant expression of mRNA for prostaglandin D synthase in leptomeninges, choroid plexus, and oligodendrocytes of the adult rat brain. Proc Natl Acad Sci U S A 90: 9070–9074.
[99]  Fina L, Molgaard HV, Robertson D, Bradley NJ, Monaghan P, et al. (1990) Expression of the CD34 gene in vascular endothelial cells. Blood 75: 2417–2426.
[100]  Richardson SJ (2007) Cell and molecular biology of transthyretin and thyroid hormones. Int Rev Cytol 258: 137–193.
[101]  Palha JA, Fernandes R, de Escobar GM, Episkopou V, Gottesman M, et al. (2000) Transthyretin regulates thyroid hormone levels in the choroid plexus, but not in the brain parenchyma: study in a transthyretin-null mouse model. Endocrinology 141: 3267–3272.
[102]  Richardson SJ, Lemkine GF, Alfama G, Hassani Z, Demeneix BA (2007) Cell division and apoptosis in the adult neural stem cell niche are differentially affected in transthyretin null mice. Neurosci Lett 421: 234–238.
[103]  Bolton K, Segal D, McMillan J, Sanigorski A, Collier G, et al. (2009) Identification of secreted proteins associated with obesity and type 2 diabetes in Psammomys obesus. Int J Obes (Lond) 33: 1153–1165.
[104]  Jacobs KA, Collins-Racie LA, Colbert M, Duckett M, Golden-Fleet M, et al. (1997) A genetic selection for isolating cDNAs encoding secreted proteins. Gene 198: 289–296.
[105]  Taft RA, Denegre JM, Pendola FL, Eppig JJ (2002) Identification of genes encoding mouse oocyte secretory and transmembrane proteins by a signal sequence trap. Biol Reprod 67: 953–960.
[106]  Ruiz i Altaba A, Palma V, Dahmane N (2002) Hedgehog-Gli signalling and the growth of the brain. Nat Rev Neurosci 3: 24–33.
[107]  Inestrosa NC, Arenas E (2010) Emerging roles of Wnts in the adult nervous system. Nat Rev Neurosci 11: 77–86.
[108]  Pierfelice TJ, Schreck KC, Eberhart CG, Gaiano N (2008) Notch, neural stem cells, and brain tumors. Cold Spring Harb Symp Quant Biol 73: 367–375.
[109]  Caronia G, Wilcoxon J, Feldman P, Grove EA (2010) Bone morphogenetic protein signaling in the developing telencephalon controls formation of the hippocampal dentate gyrus and modifies fear-related behavior. J Neurosci 30: 6291–6301.
[110]  Maeda N, Ichihara-Tanaka K, Kimura T, Kadomatsu K, Muramatsu T, et al. (1999) A receptor-like protein-tyrosine phosphatase PTPzeta/RPTPbeta binds a heparin-binding growth factor midkine. Involvement of arginine 78 of midkine in the high affinity binding to PTPzeta. J Biol Chem 274: 12474–12479.
[111]  Meng K, Rodriguez-Pe?a A, Dimitrov T, Chen W, Yamin M, et al. (2000) Pleiotrophin signals increased tyrosine phosphorylation of beta beta-catenin through inactivation of the intrinsic catalytic activity of the receptor-type protein tyrosine phosphatase beta/zeta. Proc Natl Acad Sci U S A 97: 2603–2608.
[112]  Soh BS, Song CM, Vallier L, Li P, Choong C, et al. (2007) Pleiotrophin enhances clonal growth and long-term expansion of human embryonic stem cells. Stem Cells 25: 3029–3037.
[113]  Tanaka M, Maeda N, Noda M, Marunouchi T (2003) A chondroitin sulfate proteoglycan PTPzeta/RPTPbeta regulates the morphogenesis of Purkinje cell dendrites in the developing cerebellum. J Neurosci 23: 2804–2814.
[114]  Zou P, Muramatsu H, Miyata T, Muramatsu T (2006) Midkine, a heparin-binding growth factor, is expressed in neural precursor cells and promotes their growth. J Neurochem 99: 1470–1479.

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