Chondroitin sulfate proteoglycans regulate the growth, differentiation and migration of multipotent neural precursor cells through the integrin signaling pathway
Open accessAbstract
Background: Neural precursor cells (NPCs) are defined by their ability to proliferate, self-renew, and retain the potential to differentiate into neurons and glia. Deciphering the factors that regulate their behaviors will greatly aid in their use as potential therapeutic agents or targets. Chondroitin sulfate proteoglycans (CSPGs) are prominent components of the extracellular matrix (ECM) in the central nervous system (CNS) and are assumed to play important roles in controlling neuronal differentiation and development. Results: In the present study, we demonstrated that CSPGs were constitutively expressed on the NPCs isolated from the E16 rat embryonic brain. When chondroitinase ABC was used to abolish the function of endogenous CSPGs on NPCs, it induced a series of biological responses including the proliferation, differentiation and migration of NPCs, indicating that CSPGs may play a critical role in NPC development and differentiation. Finally, we provided evidence suggesting that integrin signaling pathway may be involved in the effects of CSPGs on NPCs. Conclusion: The present study investigating the influence and mechanisms of CSPGs on the differentiation and migration of NPCs should help us to understand the basic biology of NPCs during CNS development and provide new insights into developing new strategies for the treatment of the neurological disorders in the CNS.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Aggrecan and CS-6 expression in glial cells are involved in regulation of astrocyte maturation, which has a key role in PNN formation and maintenance.
“Furthermore, aggrecan and CS-6 expression in glial cells are involved in the regulation of astrocyte maturation, which, in turn, has a key role in PNN formation and maintenance.35, 49”
From Aggrecan and chondroitin-6-sulfate abnormalities in schizophrenia and bipolar disorder: a postmortem study on the amygdala (2015) · cites this paper as [49]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Regeneration beyond the glial scar
Silver, J., & Miller, J. H. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1326 · Cited by 3,090 · see citing works
Mechanotransduction Across the Cell Surface and Through the Cytoskeleton
Wang, N., Butler, J. P., & Ingber, D. E. (1993) · Science · doi:10.1126/science.7684161 · Cited by 3,007 · see citing works
Integrins and Signal Transduction Pathways: the Road Taken
Clark, E. A., & Brugge, J. S. (1995) · Science · doi:10.1126/science.7716514 · Cited by 2,983 · see citing works
Chondroitinase ABC promotes functional recovery after spinal cord injury
Bradbury, E. J., Moon, L. D. F., Popat, R. J., King, V. R., Bennett, G. S., Patel, P. N., Fawcett, J. W., & McMahon, S. B. (2002) · Nature · doi:10.1038/416636a · Cited by 2,357 · see citing works
Signal transduction from the extracellular matrix.
Juliano, R. L., & Haskill, S. (1993) · The Journal of cell biology · doi:10.1083/jcb.120.3.577 · Cited by 1,683 · see citing works
Reactivation of Ocular Dominance Plasticity in the Adult Visual Cortex
Pizzorusso, T., Medini, P., Berardi, N., Chierzi, S., Fawcett, J. W., & Maffei, L. (2002) · Science · doi:10.1126/science.1072699 · Cited by 1,679 · see citing works
Álvarez-Buylla, A., & Lim, D. A. (2004) · Neuron · doi:10.1016/s0896-6273(04)00111-4 · Cited by 1,320 · see citing works
Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton
Ingber, D. E. (1993) · Journal of Cell Science · doi:10.1242/jcs.104.3.613 · Cited by 1,155 · see citing works
Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain.
Gage, F. H., Coates, P. W., Palmer, T. D., Kuhn, H. G., Fisher, L. J., Suhonen, J., Peterson, D. A., Suhr, S. T., & Ray, J. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.25.11879 · Cited by 1,020 · see citing works
Cell replacement therapies for central nervous system disorders
Björklund, A., & Lindvall, O. (2000) · Nature Neuroscience · doi:10.1038/75705 · Cited by 940 · see citing works
Lu, P., Jones, L. L., Snyder, E. Y., & Tuszynski, M. H. (2003) · Experimental Neurology · doi:10.1016/s0014-4886(03)00037-2 · Cited by 869 · see citing works
Self-citationMoon, L. D. F., Asher, R. A., Rhodes, K. E., & Fawcett, J. W. (2001) · Nature Neuroscience · doi:10.1038/87415 · Cited by 563 · see citing works
Ogawa, Y., Sawamoto, K., Miyata, T., Miyao, S., Watanabe, M., Nakamura, M., Bregman, B. S., Koike, M., Uchiyama, Y., Toyama, Y., et al. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10341 · Cited by 544 · see citing works
Fouad, K., Schnell, L., Bunge, M. B., Schwab, M. E., Liebscher, T., & Pearse, D. D. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3562-04.2005 · Cited by 473 · see citing works
Chondroitinase ABC Promotes Sprouting of Intact and Injured Spinal Systems after Spinal Cord Injury
Barritt, A. W., Davies, M., Marchand, F., Hartley, R., Grist, J., Yip, P., McMahon, S. B., & Bradbury, E. J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2980-06.2006 · Cited by 413 · see citing works
Monnier, P. P., Sierra, A., Schwab, J. M., Henke‐Fahle, S., & Mueller, B. K. (2003) · Molecular and Cellular Neuroscience · doi:10.1016/s1044-7431(02)00035-0 · Cited by 400 · see citing works
Anatomy of the brain neurogenic zones revisited: Fractones and the fibroblast/macrophage network
Mercier, F., Kitasako, J. T., & Hatton, G. I. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10342 · Cited by 384 · see citing works
Anton, E. S., Kreidberg, J. A., & RAKIC, P. T. (1999) · Neuron · doi:10.1016/s0896-6273(00)81089-2 · Cited by 351 · see citing works
Campos, L. S., Leone, D. P., Relvas, J. B., Brakebusch, C., Fässler, R., Suter, U., & ffrench‐Constant, C. (2004) · Development · doi:10.1242/dev.01199 · Cited by 313 · see citing works
Essential role of α6 integrins in cortical and retinal lamination
Georges‐Labouesse, E., Mark, M. P., Messaddeq, N., & Gansmüller, A. (1998) · Current Biology · doi:10.1016/s0960-9822(98)70402-6 · Cited by 304 · see citing works
Extracellular matrix and the brain: components and function
Novak, U., & Kaye, A. H. (2000) · Journal of Clinical Neuroscience · doi:10.1054/jocn.1999.0212 · Cited by 279 · see citing works
Gates, M. A., Thomas, L. B., Howard, E. M., Laywell, E. D., Sajin, B., Faissner, A., Götz, B., Silver, J., & Steindler, D. A. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903610205 · Cited by 268 · see citing works
Neural precursor cell chain migration and division are regulated through different β1 integrins
Jacques, T. S., Relvas, J. B., Nishimura, S. L., Pytela, R., Edwards, G. M., Streuli, C. H., & ffrench‐Constant, C. (1998) · Development · doi:10.1242/dev.125.16.3167 · Cited by 265 · see citing works
Brakebusch, C., Seidenbecher, C. I., Asztely, F., Rauch, U., Matthies, H., Meyer, H., Krug, M., Böckers, T. M., Zhou, X., Kreutz, M. R., et al. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.21.7417-7427.2002 · Cited by 264 · see citing works
Landolt, R., Vaughan, L., Winterhalter, K. H., & Zimmermann, D. R. (1995) · Development · doi:10.1242/dev.121.8.2303 · Cited by 260 · see citing works
Liang, X., Draghi, N. A., & Resh, M. D. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5319-03.2004 · Cited by 255 · see citing works
Niederöst, B. P., Zimmermann, D. R., Schwab, M. E., & Bandtlow, C. E. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-20-08979.1999 · Cited by 249 · see citing works
Murase, S., & Horwitz, A. F. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03568.2002 · Cited by 245 · see citing works
Regulation of human neural precursor cells by laminin and integrins
Flanagan, L. A., Rebaza, L. M., Derzic, S., Schwartz, P. H., & Monuki, E. S. (2006) · Journal of Neuroscience Research · doi:10.1002/jnr.20778 · Cited by 243 · see citing works
Human neural stem cell transplants improve motor function in a rat model of Huntington's disease
McBride, J. L., Behrstock, S. P., Chen, E., Jakel, R. J., Siegel, I. M., Svendsen, C. N., & Kordower, J. H. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20176 · Cited by 243 · see citing works
Mooney, D. J., Langer, R., & Ingber, D. E. (1995) · Journal of Cell Science · doi:10.1242/jcs.108.6.2311 · Cited by 240 · see citing works
Milner, R., & ffrench‐Constant, C. (1994) · Development · doi:10.1242/dev.120.12.3497 · Cited by 210 · see citing works
Lladó, J., Haenggeli, C., Maragakis, N. J., Snyder, E. Y., & Rothstein, J. D. (2004) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2004.07.010 · Cited by 208 · see citing works
Chau, C., Shum, D. K., Li, H., Pei, J., Lui, Y., Wirthlin, L., Chan, Y., & Xu, X. (2003) · The FASEB Journal · doi:10.1096/fj.03-0196fje · Cited by 198 · see citing works
Self-citationSirko, S., von Holst, A., Wizenmann, A., Götz, M., & Faissner, A. (2007) · Development · doi:10.1242/dev.02871 · Cited by 193 · see citing works
Importance of Intrinsic Mechanisms in Cell Fate Decisions in the Developing Rat Retina
Cayouette, M., Barres, B. A., & RAFF, M. C. (2003) · Neuron · doi:10.1016/s0896-6273(03)00756-6 · Cited by 180 · see citing works
Neurotrophic factors, gene therapy, and neural stem cells for spinal cord repair.
Blesch, A., Lu, P., & Tuszynski, M. (2002) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00774-2 · Cited by 172 · see citing works
Self-citationMultiple Regions of the NG2 Proteoglycan Inhibit Neurite Growth and Induce Growth Cone Collapse
Ughrin, Y., Chen, Z. J., & Levine, J. M. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-01-00175.2003 · Cited by 165 · see citing works
Ikegami, T., Nakamura, M., Yamane, J., Katoh, H., Okada, S., Iwanami, A., Watanabe, K., Ishii, K., Kato, F., Fujita, H., et al. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04492.x · Cited by 165 · see citing works
Regulation of neural progenitor proliferation and survival by β1 integrins
Leone, D. P., Relvas, J. B., Campos, L. S., Hemmi, S., Brakebusch, C., Fässler, R., ffrench‐Constant, C., & Suter, U. (2005) · Journal of Cell Science · doi:10.1242/jcs.02396 · Cited by 163 · see citing works
Miller, G. (2005) · Science · doi:10.1126/science.308.5723.778 · Cited by 153 · see citing works
von Holst, A., Sirko, S., & Faissner, A. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0422-06.2006 · Cited by 124 · see citing works
Relvas, J., Setzu, A., Baron, W., Buttery, P., LaFlamme, S., Franklin, R., & ffrench-Constant, C. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00292-5 · Cited by 118 · see citing works
Tate, M. C., Garcı́a, A. J., Keselowsky, B. G., Schumm, M. A., Archer, D. R., & LaPlaca, M. C. (2004) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2004.05.001 · Cited by 113 · see citing works
From barriers to bridges: chondroitin sulfate proteoglycans in neuropathology
Viapiano, M. S., & Matthews, R. T. (2006) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2006.08.007 · Cited by 101 · see citing works
Extracellular matrix effects on neurosphere cell motility
Kearns, S. (2003) · Experimental Neurology · doi:10.1016/s0014-4886(03)00124-9 · Cited by 101 · see citing works
Integrins mediate a neuronal survival signal for oligodendrocytes
Frost, E. E., Buttery, P. C., Milner, R., & ffrench‐Constant, C. (1999) · Current Biology · doi:10.1016/s0960-9822(99)80506-5 · Cited by 99 · see citing works
Repair of spinal cord injuries: where are we, where are we going?
Fawcett, J. W. (2002) · Spinal Cord · doi:10.1038/sj.sc.3101328 · Cited by 91 · see citing works
Mercado, M. L. T., Nur‐E‐Kamal, A., Liu, H., Gross, S. R., Movahed, R., & Meiners, S. A. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4519-03.2004 · Cited by 82 · see citing works
Drago, J., Nurcombe, V., & Bartlett, P. F. (1991) · Experimental Cell Research · doi:10.1016/0014-4827(91)90184-v · Cited by 78 · see citing works
Neural precursors express multiple chondroitin sulfate proteoglycans, including the lectican family
Kabos, P., Matundan, H. H., Zandian, M., Bertolotto, C., Robinson, M. L., Davy, B. E., Yu, J. S., & Krueger, R. C. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.04.114 · Cited by 58 · see citing works
Hu, J., Fu, S., Zhang, K., Li, Y., Yin, L., Lu, P., & Xu, X. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20317 · Cited by 56 · see citing works
Self-citationLiesi, P., Fried, G., & Stewart, R. R. (2001) · Journal of Neuroscience Research · doi:10.1002/jnr.1061 · Cited by 52 · see citing works
Zhang, Z., & Galileo, D. S. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-17-06928.1998 · Cited by 43 · see citing works
Expression and regulation of versican in neural precursor cells and their lineages
Gu, W.-L., Fu, S., Wang, Y.-X., Li, Y., Wang, X., Xu, X., & Lu, P. (2007) · Acta Pharmacologica Sinica · doi:10.1111/j.1745-7254.2007.00659.x · Cited by 23 · see citing works
Self-citationJordan, C. L. (1996) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199609)31:1 · Cited by 14 · see citing works
Flagged first, then by citations
1 of the 57 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Extracellular Matrix: Functions in the Nervous System
Barros, C. S., Franco, S. J., & Muller, U. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005108 · Cited by 506 · see citing works
How the extracellular matrix shapes neural development
Long, K. R., & Huttner, W. Β. (2019) · Open Biology · doi:10.1098/rsob.180216 · Cited by 263 · see citing works
Functional polarization of neuroglia: Implications in neuroinflammation and neurological disorders
Jha, M. K., Lee, W., & Suk, K. (2015) · Biochemical Pharmacology · doi:10.1016/j.bcp.2015.11.003 · Cited by 260 · see citing works
Blumenthal, N. R., Hermanson, O., Heimrich, B., & Shastri, V. P. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1412740111 · Cited by 157 · see citing works
Neural stem cell niches: Roles for the hyaluronan-based extracellular matrix
Preston, M. (2011) · Frontiers in Bioscience-Scholar · doi:10.2741/218 · Cited by 160 · see citing works
Pantazopoulos, H., Markota, M., Jaquet, F., Ghosh, D., Wallin, A., Santos, A., Caterson, B., & Berretta, S. (2015) · Translational Psychiatry · doi:10.1038/tp.2014.128 · Cited by 153 · see citing works
Chondroitin sulfates and their binding molecules in the central nervous system
Djerbal, L., Lortat-Jacob, H., & Kwok, J. (2017) · Glycoconjugate Journal · doi:10.1007/s10719-017-9761-z · Cited by 144 · see citing works
Franco, S. J., & Müller, U. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20946 · Cited by 117 · see citing works
Towards microstructure-informed material models for human brain tissue
Budday, S., Sarem, M., Starck, L., Sommer, G., Pfefferle, J., Phunchago, N., Ellen Kuhl, A., Paulsen, F. P., Steinmann, P., Shastri, V. P., et al. (2019) · Acta Biomaterialia · doi:10.1016/j.actbio.2019.12.030 · Cited by 109 · see citing works
Contributions of chondroitin sulfate proteoglycans to neurodevelopment, injury, and cancer
Silver, D. J., & Silver, J. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.03.016 · Cited by 84 · see citing works
Matrix Components and Scaffolds for Sustained Islet Function
Cheng, J. Y. C., Raghunath, M., Whitelock, J. M., & Poole-Warren, L. A. (2011) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2011.0004 · Cited by 82 · see citing works
Yuan, F., Wang, H., Guan, J., Fu, J.-N., Yang, M., Zhang, J., Chen, Y., Wang, X., & Yu, J. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13091487 · Cited by 79 · see citing works
Melrose, J. (2018) · Journal of Neurochemistry · doi:10.1111/jnc.14652 · Cited by 72 · see citing works
The Role of Chondroitin Sulfate Proteoglycans in Nervous System Development
Mencio, C. P., Hussein, R. K., Yu, P., & Geller, H. M. (2020) · Journal of Histochemistry & Cytochemistry · doi:10.1369/0022155420959147 · Cited by 68 · see citing works
Amine functionalized nanodiamond promotes cellular adhesion, proliferation and neurite outgrowth
Hopper, A., Dugan, J. M., Gill, A. A., Fox, O., May, P. W., Haycock, J. W., & Claeyssens, F. (2014) · Biomedical Materials · doi:10.1088/1748-6041/9/4/045009 · Cited by 68 · see citing works
Flexible Roles for Proteoglycan Sulfation and Receptor Signaling
Yu, P., Pearson, C. S., & Geller, H. M. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2017.10.005 · Cited by 67 · see citing works
Chondroitin Sulfate Impairs Neural Stem Cell Migration Through ROCK Activation
Galindo, L. T., Mundim, M. V., Pinto, A. A. S., Chiarantin, G. M. D., de Almeida, M. E. S., Lamers, M. L., Horwitz, A. R., dos Santos, M. F., & Porcionatto, M. A. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0565-8 · Cited by 62 · see citing works
Zheng, Q., Liu, H., Yu, W., Dong, Y., Zhou, L., Deng, W., & Hua, F. (2023) · Brain and Behavior · doi:10.1002/brb3.3136 · Cited by 58 · see citing works
Tham, M., Ramasamy, S., Gan, H. T., Ramachandran, A., Poonepalli, A., Yu, Y. H., & Ahmed, S. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015341 · Cited by 59 · see citing works
The Extracellular Matrix in the Evolution of Cortical Development and Folding
Amin, S., & Borrell, V. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.604448 · Cited by 58 · see citing works
Führmann, T., Anandakumaran, P. N., Payne, S. L., Pakulska, M. M., Varga, B. V., Nagy, A., Tator, C. H., & Shoichet, M. S. (2017) · Biomedical Materials · doi:10.1088/1748-605x/aa96dc · Cited by 60 · see citing works
Adak, A., Das, G., Khan, J., Mukherjee, N., Gupta, V., Mallesh, R., & Ghosh, S. (2020) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.9b01829 · Cited by 54 · see citing works
Hayes, A. J., Sugahara, K., Farrugia, B. L., Whitelock, J. M., Caterson, B., & Melrose, J. (2018) · Biochemical Journal · doi:10.1042/bcj20170820 · Cited by 52 · see citing works
Kim, Y., Kang, H., Powathil, G., Kim, H., Trucu, D., Lee, W., Lawler, S. E., & Chaplain, M. A. J. (2018) · PLoS ONE · doi:10.1371/journal.pone.0204865 · Cited by 50 · see citing works
Galactosaminoglycans: Medical Applications and Drawbacks
Pomin, V. H., Vignovich, W. P., Gonzales, A. V., Vasconcelos, A. A., & Mulloy, B. (2019) · Molecules · doi:10.3390/molecules24152803 · Cited by 49 · see citing works
Chondroitin Sulfate in Solution: Effects of Mono- and Divalent Salts
Horkay, F., Basser, P. J., Hecht, A., & Geissler, E. (2012) · Macromolecules · doi:10.1021/ma202693s · Cited by 48 · see citing works
Xu, J.-C., Xiao, M.-F., Jakovčevski, I., Sivukhina, E. V., Hargus, G., Cui, Y.-F., Irintchev, A., Schachner, M., & Bernreuther, C. (2013) · Journal of Cell Science · doi:10.1242/jcs.137612 · Cited by 47 · see citing works
Sarveazad, A., Babahajian, A., Bakhtiari, M., Soleimani, M., Behnam, B., Yari, A., Akbari, A., Yousefifard, M., Janzadeh, A., Amini, N., et al. (2016) · Neuropeptides · doi:10.1016/j.npep.2016.07.004 · Cited by 45 · see citing works
Bian, S., Akyüz, N., Bernreuther, C., Loers, G., Laczynska, E., Jakovčevski, I., & Schachner, M. (2011) · Journal of Cell Science · doi:10.1242/jcs.088120 · Cited by 43 · see citing works
Regulation of oligodendrocyte precursor maintenance by chondroitin sulphate glycosaminoglycans
Karus, M., Ulc, A., Ehrlich, M., Czopka, T., Hennen, E., Fischer, J., Mizhorova, M., Qamar, N., Brüstle, O., & Faissner, A. (2015) · Glia · doi:10.1002/glia.22928 · Cited by 42 · see citing works
Kim, Y., Lee, H. G., Dmitrieva, N., Kim, J., Kaur, B., & Friedman, A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0102499 · Cited by 41 · see citing works
Chondroitin sulfate-based biomaterials for tissue engineering
Kwon, H. J., & Han, Y. (2016) · TURKISH JOURNAL OF BIOLOGY · doi:10.3906/biy-1507-16 · Cited by 40 · see citing works
Regulation of adult neural precursor cell migration
Leong, S. Y., & Turnley, A. M. (2011) · Neurochemistry International · doi:10.1016/j.neuint.2010.12.024 · Cited by 37 · see citing works
Role of Region-Specific Brain Decellularized Extracellular Matrix on In Vitro Neuronal Maturation
Reginensi, D., Ortiz, D. A., Pravia, A., Burillo, A., Morales, F. L., Morgan, C., Jimenez, L., Dave, K. R., Pérez‐Pinzón, M. A., & Gittens, R. A. (2020) · Tissue Engineering Part A · doi:10.1089/ten.tea.2019.0277 · Cited by 34 · see citing works
Vallen, M. J. E., van der Steen, S. C. H. A., van Tilborg, A. A. G., Massuger, L. F. A. G., & Kuppevelt, T. H. V. (2014) · Gynecologic Oncology · doi:10.1016/j.ygyno.2014.08.023 · Cited by 33 · see citing works
Wang, S., Ji, X., Chen, S., Zhang, C., Wang, Y., Lin, H., & Zhao, L. (2021) · European Polymer Journal · doi:10.1016/j.eurpolymj.2021.110875 · Cited by 32 · see citing works
Self-citationNeuronal TIMP2 regulates hippocampus-dependent plasticity and extracellular matrix complexity
Ferreira, A. C., Hemmer, B. M., Philippi, S. M., Grau-Perales, A. B., Rosenstadt, J. L., Liu, H., Zhu, J. D., Kareva, T., Ahfeldt, T., Varghese, M., et al. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02296-5 · Cited by 30 · see citing works
The Gain-of-Function Integrin β3 Pro33 Variant Alters the Serotonin System in the Mouse Brain
Dohn, M. R., Kooker, C. G., Bastarache, L. A., Jessen, T. N., Rinaldi, C., Varney, S., Mazalouskas, M. D., Pan, H., Oliver, K. H., Edwards, D. R. V., et al. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1482-17.2017 · Cited by 29 · see citing works
Pietrucha, K. (2015) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2015.07.005 · Cited by 29 · see citing works
Sun, Y., Deng, Y., Xiao, M., Hu, L., Li, Z., & Chen, C. (2017) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2017.3153 · Cited by 28 · see citing works
Xu, J., Xiao, M., Jakovčevski, I., Sivukhina, E. V., Hargus, G., Cui, Y., Irintchev, A., Schachner, M., & Bernreuther, C. (2014) · Development · doi:10.1242/dev.108605 · Cited by 27 · see citing works
HENSON, F. M. D., Getgood, A. M. J., Caborn, D. N. M., McIlwraith, C. W., & Rushton, N. (2012) · American Journal of Veterinary Research · doi:10.2460/ajvr.73.2.306 · Cited by 26 · see citing works
Chemistry and Function of Glycosaminoglycans in the Nervous System
Schwartz, N. B., & Domowicz, M. S. (2014) · Advances in Neurobiology · doi:10.1007/978-1-4939-1154-7_5 · Cited by 25 · see citing works
Normal sulfation levels regulate spinal cord neural precursor cell proliferation and differentiation
Karus, M., Samtleben, S., Busse, C., Tsai, T., Dietzel, I. D., Faissner, A., & Wiese, S. (2012) · Neural Development · doi:10.1186/1749-8104-7-20 · Cited by 25 · see citing works
Zhang, L., Yang, J., Ding, C., Sun, S., Zhang, S., Ding, Q., Zhao, T., & Liu, W. (2024) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2024.122585 · Cited by 22 · see citing works
Acute Implantation of Aligned Hydrogel Tubes Supports Delayed Spinal Progenitor Implantation
Ciciriello, A. J., Smith, D. R., Munsell, M. K., Boyd, S. J., Shea, L. D., & Dumont, C. M. (2020) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.0c00844 · Cited by 21 · see citing works
Tee, J. Y., Sutharsan, R., Fan, Y., & Mackay‐Sim, A. (2017) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2017.03.005 · Cited by 19 · see citing works
Vinukonda, G., Zia, M., Bhimavarapu, B. B. R., Hu, F., Feinberg, M. L., Bokhari, A., Ungvari, Z. I., Fried, V. A., & Ballabh, P. (2013) · Experimental Neurology · doi:10.1016/j.expneurol.2013.02.018 · Cited by 20 · see citing works
Spinal Progenitor-Laden Bridges Support Earlier Axon Regeneration Following Spinal Cord Injury
Dumont, C. M., Munsell, M. K., Carlson, M. A., Cummings, B. J., Anderson, A. J., & Shea, L. D. (2018) · Tissue Engineering Part A · doi:10.1089/ten.tea.2018.0053 · Cited by 18 · see citing works
Single-Cell mRNA Profiling Identifies Progenitor Subclasses in Neurospheres
Narayanan, G., Poonepalli, A., Chen, J., Sankaran, S., Hariharan, S., Yu, Y. H., Robson, P., Yang, H. H., & Ahmed, S. (2012) · Stem Cells and Development · doi:10.1089/scd.2012.0232 · Cited by 17 · see citing works
Chondroitin Sulfate as a Potential Modulator of the Stem Cell Niche in Cornea
Ashworth, S., Harrington, J., Hammond, G. M., Bains, K. K., Koudouna, E., Hayes, A. J., Ralphs, J. R., Regini, J. W., Young, R. D., Hayashi, R., et al. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.567358 · Cited by 17 · see citing works
Chemistry and Function of Glycosaminoglycans in the Nervous System
Schwartz, N. B., & Domowicz, M. S. (2022) · Advances in neurobiology · doi:10.1007/978-3-031-12390-0_5 · Cited by 16 · see citing works
Human t-DARPP is induced during striatal development
Straccia, M., Carrere-Molina, J., Rosser, A., & Canals, J. M. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.07.022 · Cited by 15 · see citing works
Adhikari, B., Stinson, B. S., Osmond, M. J., Pantcheva, M. B., & Krebs, M. D. (2021) · Industrial & Engineering Chemistry Research · doi:10.1021/acs.iecr.1c02828 · Cited by 12 · see citing works
Photochemically modified diamond-like carbon surfaces for neural interfaces
Hopper, A., Dugan, J. M., Gill, A. A., Regan, E. M., Haycock, J. W., Kelly, S., May, P. W., & Claeyssens, F. (2015) · Materials Science and Engineering C · doi:10.1016/j.msec.2015.09.013 · Cited by 11 · see citing works
Xu, C., Wang, J., & Jin, W. (2015) · Journal of Molecular Neuroscience · doi:10.1007/s12031-015-0538-1 · Cited by 11 · see citing works
Pai, V. C., Lo, I., Huang, Y., Tsai, I.-C., Cheng, H.-P., Shi, G., Wu, H., & Jiang, M. J. (2018) · Journal of Biomedical Science · doi:10.1186/s12929-018-0415-7 · Cited by 11 · see citing works
Chronic Inflammation in the Epidermis: A Mathematical Model
Nakaoka, S., Kuwahara, S., Lee, C. H., Jeon, H., Lee, J.-H., Takeuchi, Y., & Kim, Y. (2016) · Applied Sciences · doi:10.3390/app6090252 · Cited by 11 · see citing works
Hodgkinson, G. N., Tresco, P. A., & Hlady, V. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.02.046 · Cited by 9 · see citing works
Lu, X., Zhong, Q., Liu, J., Yang, F., Lu, C., Xiong, H., Li, S., Zhu, Y., & Wu, L. (2019) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2019.11.215 · Cited by 9 · see citing works
Degradation of proteoglycans affects astrocytes and neurite formation in organotypic tissue cultures
Hashemian, S., Marschinke, F., af Bjerkén, S., & Strömberg, I. (2014) · Brain Research · doi:10.1016/j.brainres.2014.03.043 · Cited by 8 · see citing works
Yamauchi, S., Kurosu, A., Hitosugi, M., Nagai, T., Oohira, A., & Tokudome, S. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2011.02.019 · Cited by 8 · see citing works
Bernstock, J. D., Verheyen, J., Huang, B. Y., Hallenbeck, J. M., & Pluchino, S. (2014) · InTech eBooks · doi:10.5772/58599 · Cited by 8 · see citing works
Comparison of various types of collagenous scaffolds applied for embryonic nerve cell culture
Drobnik, J., Pietrucha, K., Kudzin, M. H., Mader, K., Szymański, J., & Szczepanowska, A. (2017) · Biologicals · doi:10.1016/j.biologicals.2017.01.001 · Cited by 8 · see citing works
Innervation in corneal bioengineering
Maher, C. B., Chen, Z. X., Zhou, Y. X., You, J., Sutton, G. L., & Wallace, G. G. (2024) · Acta Biomaterialia · doi:10.1016/j.actbio.2024.10.009 · Cited by 7 · see citing works
Wang, S., Wang, L., Bu, Q., Wei, Q., Jiang, L., Dai, Y., Zhang, N., Kuang, W., Zhao, Y., & Cen, X. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1242109 · Cited by 7 · see citing works
Kim, M. H., Park, S. R., & Choi, B. H. (2020) · Tissue Engineering and Regenerative Medicine · doi:10.1007/s13770-020-00295-z · Cited by 7 · see citing works
Kukreja, B., Jeon, S. T., Cao, W., Rusu, B., Harrison, C. F., Ghazisaeidi, S., Tahmasian, N., Feng, M. Y., Chan, R., Loan, A., et al. (2026) · Nature Neuroscience · doi:10.1038/s41593-025-02162-3 · Cited by 7 · see citing works
Activation of Astrocytes in Vitro by Macrophages Polarized with Keratin Biomaterial Treatment
Fearing, B. V., & Dyke, M. E. V. (2016) · Open Journal of Regenerative Medicine · doi:10.4236/ojrm.2016.51001 · Cited by 6 · see citing works
The Behavior of Embryonic Neural Cells within the 3D Micro-structured Collagen-Based Scaffolds
Pietrucha, K., Szymański, J., & Drobnik, J. (2014) · World Congress on Medical Physics and Biomedical Engineering, September 7 - 12, 2009, Munich, Germany · doi:10.1007/978-3-319-11128-5_137 · Cited by 6 · see citing works
Lee, H. G., & Kim, Y. (2015) · Japan Journal of Industrial and Applied Mathematics · doi:10.1007/s13160-015-0188-2 · Cited by 6 · see citing works
Komatsuya, K., Iguchi, T., Fukuyama, M., Kawashima, I., Ogura, K., Kikuchi, N., Shimoda, Y., Takeda, Y., Shimonaka, M., Yamamoto, N., et al. (2022) · Journal of Neurochemistry · doi:10.1111/jnc.15709 · Cited by 5 · see citing works
Hutchings, C., Nuriel, Y., Lazar, D., Kohl, A., Muir, E. M., Genin, O., Cinnamon, Y., Benyamini, H., Nevo, Y., & Sela‐Donenfeld, D. (2024) · Development · doi:10.1242/dev.201934 · Cited by 5 · see citing works
Potential involvement of chondroitin sulfate A in the pathogenesis of ameloblastoma
Li, X., Kurita, H., Xiao, T., Iijima, K., Kurashina, K., & Nakayama, J. (2017) · Acta Histochemica · doi:10.1016/j.acthis.2017.04.001 · Cited by 5 · see citing works
Cell adhesion properties of neural stem cells in the chick embryo
Canning, D. R., & Cunningham, R. L. (2014) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/s11626-014-9851-1 · Cited by 3 · see citing works
Hopper, A. (2015) · White Rose eTheses Online (University of Leeds, The University of Sheffield, University of York)
Direct cell differentiation towards neural specific phenotypes
Ritchie, M. F. (2012) · University of Minnesota Digital Conservancy (University of Minnesota)
MODIFYING CHONDROITIN SULFATION ENHANCES RETINAL GANGLION CELL AXON REGENERATION
Pearson, C. S. (2018) · Apollo (University of Cambridge) · doi:10.17863/cam.32374
La régénération du système nerveux périphérique et central par la voie RSK-RPS6
Decourt, C. (2023) · theses.fr (ABES) · doi:10.70675/03404a46z2d34z458bzb422z41a80f2bdac6
Extracellular matrix and perineuronal nets in neural plasticity, memory, and epileptogenesis
Zhu, H., Li, Q., Li, Y., & Wang, W. (2026) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2026.1945520
Self-citation
- Authors
- Gu, W.-L., Fu, S.-L., Wang, Y.-X., Li, Y., Lü, H.-Z., Xu, X.-M., & Lu, P.-H.
- Affiliations
- Shanghai Jiao Tong University (CN)
- Corresponding author
- Xu, Xiao-Ming
- Lu, Pei-Hua
- Venue
- BMC Neuroscience
- Published
- 2009-10-21
- Volume
- 10
- Issue
- 1
- Pages
- 128-128
- ISSN
- 1471-2202 (ISSN-L)
- PMC
- PMC2773784
- OpenAlex
- W1965593502
- Cited by
- 80
- References
- 57
- Citations by year
- 2026: 2 · 2024: 3 · 2023: 4 · 2022: 2 · 2021: 4 · 2020: 6 · 2019: 4 · 2018: 6 · 2017: 9 · 2016: 5 · 2015: 8 · 2014: 11 · 2013: 2 · 2012: 6
- FWCI
- 1.46
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- BMC Neuroscience (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- IUScholarWorks (Indiana University) (submittedVersion, cc-by)
- Purdue University Indianapolis (Indiana University) (submittedVersion, cc-by)
- Publisher
- Funders
- Shanghai Jiao Tong University
- Major State Basic Research Development Program of China (2003CB515302)
- National Institutes of Health
- School of Medicine, Shanghai Jiao Tong University
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- chondroitin sulfate proteoglycans, neural progenitor cells, integrin signaling, cell proliferation, neuronal differentiation, cell migration, chondroitinase ABC, extracellular matrix, embryonic brain, central nervous system development, neurological disorders
- MeSH terms
- Animals, Astrocytes, Cell Differentiation, Cell Movement, Cells, Cultured, Flow Cytometry, Fluorescent Antibody Technique, Neurons, Oligodendroglia, Peptides, Platelet Aggregation Inhibitors, Chondroitin Sulfate Proteoglycans, Blotting, Western, Integrins, Rats, Sprague-Dawley, Chondroitin ABC Lyase, Intercellular Signaling Peptides and Proteins, Multipotent Stem Cells, Cell Shape, Cell Proliferation, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review