Normal sulfation levels regulate spinal cord neural precursor cell proliferation and differentiation

Neural Development

Volumn 7, Issue 1, 2012, Pages

  Karus, Michael ^a   Samtleben, Samira ^a   Busse, Claudia ^a   Tsai, Teresa ^a   Dietzel, Irmgard D ^a   Faissner, Andreas ^a   Wiese, Stefan ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Chondroitin sulfate proteoglycans; Extracellular matrix; Neuronal differentiation; Sulfation

Indexed keywords

A73025; CHONDROITIN SULFATE; GLYCOSAMINOGLYCAN; SULFATE;

ANIMAL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECT; FEMALE; METABOLISM; MOUSE; MOUSE STRAIN; NEURAL STEM CELL; PHYSIOLOGY; PRENATAL DEVELOPMENT; PRIMARY CELL CULTURE; SPINAL CORD;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CHONDROITIN SULFATES; FEMALE; GLYCOSAMINOGLYCANS; MICE; MICE, INBRED STRAINS; NEURAL STEM CELLS; PRIMARY CELL CULTURE; SPINAL CORD; SULFATES;

EID: 84861935123     PISSN: None     EISSN: 17498104     Source Type: Journal    
DOI: 10.1186/1749-8104-7-20     Document Type: Article

References (53)

1. Kleene R, Schachner M. Glycans and neural cell interactions. Nat Rev Neurosci 2004, 5:195-208. 10.1038/nrn1349, 14976519.
2. Yanagisawa M, Yu RK. The expression and functions of glycoconjugates in neural stem cells. Glycobiology 2007, 17:57R-74R. 10.1093/glycob/cwm018, 17307762.
3. Yu RK, Yanagisawa M. Glycosignaling in neural stem cells: involvement of glycoconjugates in signal transduction modulating the neural stem cell fate. J Neurochem 2007, 103(Suppl 1):39-46.
4. Gu WL, Fu SL, Wang YX, Li Y, Lu HZ, Xu XM, Lu PH. Chondroitin sulfate proteoglycans regulate the growth, differentiation and migration of multipotent neural precursor cells through the integrin signaling pathway. BMC Neurosci 2009, 10:128. 10.1186/1471-2202-10-128, 2773784, 19845964.
5. Sirko S, von Holst A, Weber A, Wizenmann A, Theocharidis U, Gotz M, Faissner A. Chondroitin sulfates are required for fibroblast growth factor-2-dependent proliferation and maintenance in neural stem cells and for epidermal growth factor-dependent migration of their progeny. Stem Cells 2010, 28:775-787. 10.1002/stem.309, 20087964.
6. Sirko S, von Holst A, Wizenmann A, Gotz M, Faissner A. Chondroitin sulfate glycosaminoglycans control proliferation, radial glia cell differentiation and neurogenesis in neural stem/progenitor cells. Development 2007, 134:2727-2738. 10.1242/dev.02871, 17596283.
7. Tham M, Ramasamy S, Gan HT, Ramachandran A, Poonepalli A, Yu YH, Ahmed S. CSPG is a secreted factor that stimulates neural stem cell survival possibly by enhanced EGFR signaling. PLoS One 2010, 5:e15341. 10.1371/journal.pone.0015341, 3001889, 21179491.
8. Akita K, von Holst A, Furukawa Y, Mikami T, Sugahara K, Faissner A. Expression of multiple chondroitin/dermatan sulfotransferases in the neurogenic regions of the embryonic and adult central nervous system implies that complex chondroitin sulfates have a role in neural stem cell maintenance. Stem Cells 2008, 26:798-809. 10.1634/stemcells.2007-0448, 18079434.
9. Properzi F, Carulli D, Asher RA, Muir E, Camargo LM, van Kuppevelt TH, ten Dam GB, Furukawa Y, Mikami T, Sugahara K, Toida T, Geller HM, Fawcett JW. Chondroitin 6-sulphate synthesis is up-regulated in injured CNS, induced by injury-related cytokines and enhanced in axon-growth inhibitory glia. Eur J Neurosci 2005, 21:378-390. 10.1111/j.1460-9568.2005.03876.x, 15673437.
10. Silver J, Miller JH. Regeneration beyond the glial scar. Nat Rev Neurosci 2004, 5:146-156. 10.1038/nrn1326, 14735117.
11. Garcia-Alias G, Barkhuysen S, Buckle M, Fawcett JW. Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation. Nat Neurosci 2009, 12:1145-1151. 10.1038/nn.2377, 19668200.
12. Wang D, Ichiyama RM, Zhao R, Andrews MR, Fawcett JW. Chondroitinase combined with rehabilitation promotes recovery of forelimb function in rats with chronic spinal cord injury. J Neurosci 2011, 31:9332-9344. 10.1523/JNEUROSCI.0983-11.2011, 21697383.
13. Lin R, Rosahl TW, Whiting PJ, Fawcett JW, Kwok JC. 6-sulphated chondroitins have a positive influence on axonal regeneration. PLoS One 2011, 6:e21499. 10.1371/journal.pone.0021499, 3128591, 21747937.
14. Eswarakumar VP, Lax I, Schlessinger J. Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev 2005, 16:139-149. 10.1016/j.cytogfr.2005.01.001, 15863030.
15. Capela A, Temple S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 2002, 35:865-875. 10.1016/S0896-6273(02)00835-8, 12372282.
16. Capela A, Temple S. LeX is expressed by principle progenitor cells in the embryonic nervous system, is secreted into their environment and binds Wnt-1. Dev Biol 2006, 291:300-313. 10.1016/j.ydbio.2005.12.030, 16458284.
17. Hennen E, Czopka T, Faissner A. Structurally distinct LewisX glycans distinguish subpopulations of neural stem/progenitor cells. J Biol Chem 2011, 286:16321-16331. 10.1074/jbc.M110.201095, 3091238, 21385876.
18. Liedtke S, Geyer H, Wuhrer M, Geyer R, Frank G, Gerardy-Schahn R, Zahringer U, Schachner M. Characterization of N-glycans from mouse brain neural cell adhesion molecule. Glycobiology 2001, 11:373-384. 10.1093/glycob/11.5.373, 11425798.
19. Habuchi O. Diversity and functions of glycosaminoglycan sulfotransferases. Biochim Biophys Acta 2000, 1474:115-127. 10.1016/S0304-4165(00)00016-7, 10742590.
20. Kusche-Gullberg M, Kjellen L. Sulfotransferases in glycosaminoglycan biosynthesis. Curr Opin Struct Biol 2003, 13:605-611. 10.1016/j.sbi.2003.08.002, 14568616.
21. Jones KS, Petrow-Sadowski C, Bertolette DC, Huang Y, Ruscetti FW. Heparan sulfate proteoglycans mediate attachment and entry of human T-cell leukemia virus type 1 virions into CD4+ T cells. J Virol 2005, 79:12692-12702. 10.1128/JVI.79.20.12692-12702.2005, 1235841, 16188972.
22. Karus M, Denecke B, Ffrench-Constant C, Wiese S, Faissner A. The extracellular matrix molecule tenascin C modulates expression levels and territories of key patterning genes during spinal cord astrocyte specification. Development 2011, 138:5321-5331. 10.1242/dev.067413, 22071102.
23. Sirko S, Akita K, Von Holst A, Faissner A. Structural and functional analysis of chondroitin sulfate proteoglycans in the neural stem cell niche. Methods Enzymol 2010, 479:37-71.
24. Sommer I, Schachner M. Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Dev Biol 1981, 83:311-327. 10.1016/0012-1606(81)90477-2, 6786942.
25. Faissner A, Clement A, Lochter A, Streit A, Mandl C, Schachner M. Isolation of a neural chondroitin sulfate proteoglycan with neurite outgrowth promoting properties. J Cell Biol 1994, 126:783-799. 10.1083/jcb.126.3.783, 2120143, 7519189.
26. Kempf M, Clement A, Faissner A, Lee G, Brandt R. Tau binds to the distal axon early in development of polarity in a microtubule- and microfilament-dependent manner. J Neurosci 1996, 16:5583-5592.
27. Garwood J, Schnadelbach O, Clement A, Schutte K, Bach A, Faissner A. DSD-1-proteoglycan is the mouse homolog of phosphacan and displays opposing effects on neurite outgrowth dependent on neuronal lineage. J Neurosci 1999, 19:3888-3899.
28. Bossard C, Jarry A, Colombeix C, Bach-Ngohou K, Moreau A, Loussouarn D, Mosnier JF, Laboisse CL. Phosphohistone H3 labelling for histoprognostic grading of breast adenocarcinomas and computer-assisted determination of mitotic index. J Clin Pathol 2006, 59:706-710. 10.1136/jcp.2005.030452, 1860410, 16461563.
29. Conway CD, Howe KM, Nettleton NK, Price DJ, Mason JO, Pratt T. Heparan sulfate sugar modifications mediate the functions of slits and other factors needed for mouse forebrain commissure development. J Neurosci 2011, 31:1955-1970. 10.1523/JNEUROSCI.2579-10.2011, 21307234.
30. Ishii M, Maeda N. Oversulfated chondroitin sulfate plays critical roles in the neuronal migration in the cerebral cortex. J Biol Chem 2008, 283:32610-32620. 10.1074/jbc.M806331200, 18819920.
31. Ishii M, Maeda N. Spatiotemporal expression of chondroitin sulfate sulfotransferases in the postnatal developing mouse cerebellum. Glycobiology 2008, 18:602-614. 10.1093/glycob/cwn040, 18480156.
32. Ito Z, Sakamoto K, Imagama S, Matsuyama Y, Zhang H, Hirano K, Ando K, Yamashita T, Ishiguro N, Kadomatsu K. N-acetylglucosamine 6-O-sulfotransferase-1-deficient mice show better functional recovery after spinal cord injury. J Neurosci 2010, 30:5937-5947. 10.1523/JNEUROSCI.2570-09.2010, 20427653.
33. Properzi F, Lin R, Kwok J, Naidu M, van Kuppevelt TH, Ten Dam GB, Camargo LM, Raha-Chowdhury R, Furukawa Y, Mikami T, Sugahara K, Fawcett JW. Heparan sulphate proteoglycans in glia and in the normal and injured CNS: expression of sulphotransferases and changes in sulphation. Eur J Neurosci 2008, 27:593-604. 10.1111/j.1460-9568.2008.06042.x, 18279312.
34. Wilson VA, Gallagher JT, Merry CL. Heparan sulfate 2-O-sulfotransferase (Hs2st) and mouse development. Glycoconj J 2002, 19:347-354.
35. Ford-Perriss M, Turner K, Guimond S, Apedaile A, Haubeck HD, Turnbull J, Murphy M. Localisation of specific heparan sulfate proteoglycans during the proliferative phase of brain development. Dev Dyn 2003, 227:170-184. 10.1002/dvdy.10298, 12761845.
36. Kabos P, Matundan H, Zandian M, Bertolotto C, Robinson ML, Davy BE, Yu JS, Krueger RC. Neural precursors express multiple chondroitin sulfate proteoglycans, including the lectican family. Biochem Biophys Res Commun 2004, 318:955-963. 10.1016/j.bbrc.2004.04.114, 15147965.
37. von Holst A, Sirko S, Faissner A. The unique 473HD-Chondroitinsulfate epitope is expressed by radial glia and involved in neural precursor cell proliferation. J Neurosci 2006, 26:4082-4094. 10.1523/JNEUROSCI.0422-06.2006, 16611825.
38. Kerever A, Schnack J, Vellinga D, Ichikawa N, Moon C, Arikawa-Hirasawa E, Efird JT, Mercier F. Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor fibroblast growth factor 2 from the extracellular milieu. Stem Cells 2007, 25:2146-2157. 10.1634/stemcells.2007-0082, 17569787.
39. Fjeldstad K, Pedersen ME, Vuong TT, Kolset SO, Nordstrand LM, Prydz K. Sulfation in the Golgi lumen of Madin-Darby canine kidney cells is inhibited by brefeldin A and depends on a factor present in the cytoplasm and on Golgi membranes. J Biol Chem 2002, 277:36272-36279. 10.1074/jbc.M206365200, 12138122.
40. Clement AM, Nadanaka S, Masayama K, Mandl C, Sugahara K, Faissner A. The DSD-1 carbohydrate epitope depends on sulfation, correlates with chondroitin sulfate D motifs, and is sufficient to promote neurite outgrowth. J Biol Chem 1998, 273:28444-28453. 10.1074/jbc.273.43.28444, 9774473.
41. Rieder CL. Mitosis in vertebrates: the G2/M and M/A transitions and their associated checkpoints. Chromosome Res 2011, 19:291-306. 10.1007/s10577-010-9178-z, 21194009.
42. Lillien L, Raphael H. BMP and FGF regulate the development of EGF-responsive neural progenitor cells. Development 2000, 127:4993-5005.
43. Guo Y, Zhang X, Meng J, Wang ZY. An anticancer agent icaritin induces sustained activation of the extracellular signal-regulated kinase (ERK) pathway and inhibits growth of breast cancer cells. Eur J Pharmacol 2011, 658:114-122. 10.1016/j.ejphar.2011.02.005, 3071461, 21376032.
44. Wei F, Xie Y, Tao L, Tang D. Both ERK1 and ERK2 kinases promote G2/M arrest in etoposide-treated MCF7 cells by facilitating ATM activation. Cell Signal 2010, 22:1783-1789. 10.1016/j.cellsig.2010.07.007, 20637859.
45. Xu Y, Xia W, Baker D, Zhou J, Cha HC, Voorhees JJ, Fisher GJ. Receptor-type protein tyrosine phosphatase beta (RPTP-beta) directly dephosphorylates and regulates hepatocyte growth factor receptor (HGFR/Met) function. J Biol Chem 2011, 286:15980-15988. 10.1074/jbc.M110.212597, 3091207, 21454675.
46. Sasaki N, Hirano T, Ichimiya T, Wakao M, Hirano K, Kinoshita-Toyoda A, Toyoda H, Suda Y, Nishihara S. The 3′-phosphoadenosine 5′-phosphosulfate transporters, PAPST1 and 2, contribute to the maintenance and differentiation of mouse embryonic stem cells. PLoS One 2009, 4:e8262. 10.1371/journal.pone.0008262, 2788424, 20011239.
47. Busch SA, Silver J. The role of extracellular matrix in CNS regeneration. Curr Opin Neurobiol 2007, 17:120-127. 10.1016/j.conb.2006.09.004, 17223033.
48. See J, Bonner J, Neuhuber B, Fischer I. Neurite outgrowth of neural progenitors in presence of inhibitory proteoglycans. J Neurotrauma 2010, 27:951-957. 10.1089/neu.2009.1158, 20102265.
49. Klausmeyer A, Conrad R, Faissner A, Wiese S. Influence of glial-derived matrix molecules, especially chondroitin sulfates, on neurite growth and survival of cultured mouse embryonic motoneurons. J Neurosci Res 2010, 89:127-141.
50. Dietzel ID. Voltage-gated ion currents in embryogenesis. Perspect Dev Neurobiol 1995, 2:293-308.
51. Brackenbury WJ, Calhoun JD, Chen C, Miyazaki H, Nukina N, Oyama F, Ranscht B, Isom LL. Functional reciprocity between Na + channel Nav1.6 and beta1 subunits in the coordinated regulation of excitability and neurite outgrowth. Proc Natl Acad Sci U S A 2010, 107:2283-2288. 10.1073/pnas.0909434107, 2836661, 20133873.
52. Niederkinkhaus V, Marx R, Hoffmann G, Dietzel ID. Thyroid hormone (T3)-induced up-regulation of voltage-activated sodium current in cultured postnatal hippocampal neurons requires secretion of soluble factors from glial cells. Mol Endocrinol 2009, 23:1494-1504. 10.1210/me.2009-0132, 2737559, 19460859.
53. Pyka M, Wetzel C, Aguado A, Geissler M, Hatt H, Faissner A. Chondroitin sulfate proteoglycans regulate astrocyte-dependent synaptogenesis and modulate synaptic activity in primary embryonic hippocampal neurons. Eur J Neurosci 2011, 33:2187-2202. 10.1111/j.1460-9568.2011.07690.x, 21615557.