Heparanase enhances nerve-growth-factor-induced PC12 cell neuritogenesis via the p38 MAPK pathway

[en] Heparanase is involved in the cleavage of the HS (heparan sulfate) chain of HSPGs (HS proteoglycans) and hence participates in remodelling of the ECM (extracellularmatrix) and BM(basement membrane). In the present study we have shown that NGF (nerve growth factor) promoted nuclear enrichment of EGR1 (early growth response 1), a transcription factor for heparanase, and markedly induced heparanase expression in rat adrenal pheochromocytoma (PC12) cells. K252a, an antagonist of the NGF receptor TrkA (tyrosine kinase receptor A), decreased heparanase protein expression induced by NGF in PC12 cells. Suramin, a heparanase inhibitor, decreased heparanase in PC12 cells and blocked NGF-induced PC12 neuritogenesis. Stable overexpression of heparanase activated p38 MAPK (mitogenactivated protein kinase) by phosphorylation and enhanced the neurite outgrowth induced by NGF, whereas knock down of heparanase impaired this process. However, overexpression of latent pro-heparanase with a Y156A mutation still led to enhanced NGF-induced neurite outgrowth and increased p38 MAPK phosphorylation. Inhibition of p38 MAPK by SB203580 suppressed the promotion of NGF-induced neuritogenesis by the wild-type and mutant heparanase. The impaired differentiation by knock down of heparanase could be restored by transfection of wild-type or mutant heparanase in PC12 cells. The results of the present study suggest that heparanase, at least in the nonenzymatic form, may promote NGF-induced neuritogenesis via the p38 MAPK pathway.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

CUI, Hengxiang

SHAO, Chenghao

LIU, Qin

YU, Wenjie

FANG, Jianping

YU, Weishi

Ali, Amjad ; Université de Liège > Département de pharmacie > Chimie médicale

DING, Kan

Language :

English

Title :

Heparanase enhances nerve-growth-factor-induced PC12 cell neuritogenesis via the p38 MAPK pathway

Publication date :

2011

Journal title :

Biochemical Journal

ISSN :

0264-6021

eISSN :

1470-8728

Publisher :

Portland Press, London, United Kingdom

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 01 June 2015

Statistics

Number of views

48 (5 by ULiège)

Number of downloads

1 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Akita, K., Toda, M., Hosoki, Y., Inoue, M., Fushiki, S., Oohira, A., Okayama, M., Yamashina, I. and Nakada, H. (2004) Heparan sulphate proteoglycans interact with neurocan and promote neurite outgrowth from cerebellar granule cells. Biochem. J. 383, 129-138 (Pubitemid 39389458)
Bishop, J. R., Schuksz, M. and Esko, J. D. (2007) Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446, 1030-1037 (Pubitemid 46676065)
Hacker, U., Nybakken, K. and Perrimon, N. (2005) Heparan sulphate proteoglycans: the sweet side of development. Nat. Rev. 6, 530-541 (Pubitemid 40943044)
Qiu, H., Yang, B., Pei, Z. C., Zhang, Z. and Ding, K. (2010) WSS25 inhibits growth of xenografted hepatocellular cancer cells in nude mice by disrupting angiogenesis via blocking BMP/SMAD/ID1 signaling. J. Biol. Chem. 285, 32638-32646
Ding, K., Sanchez-Duran, J. A., Korc, M. and Lander, A. D. (2005) Growth factor-induced shedding of syndecan-1 confers glypican-1 dependence on mitogenic responses of cancer cells. J. Cell Biol. 171, 729-738 (Pubitemid 41668731)
Bertolesi, G. E., Michaiel, G. and McFarlane, S. (2008) Two heparanase splicing variants with distinct properties are necessary in early Xenopus development. J. Biol. Chem. 283, 16004-16016
Zcharia, E., Jia, J., Zhang, X., Baraz, L., Lindahl, U., Peretz, T., Vlodavsky, I. and Li, J. P. (2009) Newly generated heparanase knock-out mice unravel co-regulation of heparanase and matrix metalloproteinases. PLoS ONE 4, e5181
Baker, A. B., Groothuis, A., Jonas, M., Ettenson, D. S., Shazly, T., Zcharia, E., Vlodavsky, I., Seifert, P. and Edelman, E. R. (2009) Heparanase alters arterial structure, mechanics, and repair following endovascular stenting in mice. Circ. Res. 104, 380-387
Sandwall, E., Bodevin, S., Nasser, N. J., Nevo, E., Avivi, A., Vlodavsky, I. and Li, J. P. (2009) Molecular structure of heparan sulfate from Spalax. Implications of heparanase and hypoxia. J. Biol. Chem. 284, 3814-3822
Klipper, E., Tatz, E., Kisliouk, T., Vlodavsky, I., Moallem, U., Schams, D., Lavon, Y., Wolfenson, D. and Meidan, R. (2009) Induction of heparanase in bovine granulosa cells by luteinizing hormone: possible role during the ovulatory process. Endocrinology 150, 413-421
Nakajima, M., Irimura, T., DiFerrante, D., DiFerrante, N. and Nicolson, G. L. (1983) Heparan sulfate degradation: relation to tumor invasive and metastatic properties of mouse B16 melanoma sublines. Science 220, 611-613 (Pubitemid 13130144)
Sasaki, N., Higashi, N., Taka, T., Nakajima, M. and Irimura, T. (2004) Cell surface localization of heparanase on macrophages regulates degradation of extracellular matrix heparan sulfate. J. Immunol. 172, 3830-3835 (Pubitemid 38337969)
Vlodavsky, I., Fuks, Z., Bar-Ner, M., Ariav, Y. and Schirrmacher, V. (1983) Lymphoma cell-mediated degradation of sulfated proteoglycans in the subendothelial extracellular matrix: relationship to tumor cell metastasis. Cancer Res. 43, 2704-2711 (Pubitemid 13100536)
Parish, C. R., Freeman, C., Hulett, M. D. and Freeman, C. (2001) Heparanase: a key enzyme involved in cell invasion. Biochim. Biophys. Acta 1471, M99-M108 (Pubitemid 32206686)
Goldshmidt, O., Zcharia, E., Abramovitch, R., Metzger, S., Aingorn, H., Friedmann, Y., Schirrmacher, V., Mitrani, E. and Vlodavsky, I. (2002) Cell surface expression and secretion of heparanase markedly promote tumor angiogenesis and metastasis. Proc. Natl. Acad. Sci. U.S.A 99, 10031-10036 (Pubitemid 34831167)
Matzner, Y., Vlodavsky, I., Bar-Ner, M., Ishai-Michaeli, R. and Tauber, A. (1992) Subcellular localization of heparanase in human neutrophils. J. Leukocyte Biol. 51, 519-524
Bitan, M., Weiss, L., Zeira, M., Zcharia, E., Slavin, S., Nagler, A. and Vlodavsky, I. (2010) Heparanase promotes engraftment and prevents graft versus host disease in stem cell transplantation. PLoS ONE 5, e10135
Marchetti, D., Li, J. and Shen, R. (2000) Astrocytes contribute to the brain-metastatic specificity of melanoma cells by producing heparanase. Cancer Res. 60, 4767-4770
Goldshmidt, O., Zcharia, E., Cohen, M., Aingorn, H., Cohen, I., Nadav, L., Katz, B. Z., Geiger, B. and Vlodavsky, I. (2003) Heparanase mediates cell adhesion independent of its enzymatic activity. FASEB J. 17, 1015-1025 (Pubitemid 36676388)
Levy-Adam, F., Feld, S., Suss-Toby, E., Vlodavsky, I. and Ilan, N. (2008) Heparanase facilitates cell adhesion and spreading by clustering of cell surface heparan sulfate proteoglycans. PLoS ONE 3, e2319
Zhang, Y., Yeung, M. N., Liu, J., Chau, C. H., Chan, Y. S. and Shum, D. K. (2006) Mapping heparanase expression in the spinal cord of adult rats. J. Comp. Neurol. 494, 345-357 (Pubitemid 41798091)
Sandwall, E., Bodevin, S., Nasser, N. J., Nevo, E., Avivi, A., Vlodavsky, I. and Li, J. P. (2009) Molecular structure of heparan sulfate from Spalax. Implications of heparanase and hypoxia. J. Biol. Chem. 284, 3814-3822
Greene, L. A. and Tischler, A. S. (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. U.S.A. 73, 2424-2428
Navarro, F. P., Fares, R. P., Sanchez, P. E., Nadam, J., Georges, B., Moulin, C., Morales, A., Pequignot, J. M. and Bezin, L. (2008) Brain heparanase expression is up-regulated during postnatal development and hypoxia-induced neovascularization in adult rats. J. Neurochem. 105, 34-45 (Pubitemid 351441630)
Abboud-Jarrous, G., Rangini-Guetta, Z., Aingorn, H., Atzmon, R., Elgavish, S., Peretz, T. and Vlodavsky, I. (2005) Site-directed mutagenesis, proteolytic cleavage, and activation of human proheparanase. J. Biol. Chem. 280, 13568-13575 (Pubitemid 40517249)
Li, D., Niu, Z., Yu, W., Qian, Y., Wang, Q., Li, Q., Yi, Z., Luo, J., Wu, X., Wang, Y. et al. (2009) SMYD1, the myogenic activator, is a direct target of serum response factor and myogenin. Nucleic Acids Res. 37, 7059-7071
Koh, D. C., Armugam, A. and Jeyaseelan, K. (2004) Sputa nerve growth factor forms a preferable substitute to mouse 7S-β nerve growth factor. Biochem. J. 383, 149-158 (Pubitemid 39389460)
Davidson, B., Vintman, L., Zcharia, E., Bedrossian, C., Berner, A., Nielsen, S., Ilan, N., Vlodavsky, I. and Reich, R. (2004) Heparanase and basic fibroblast growth factor are co-expressed in malignant mesothelioma. Clin. Exp. Metastasis 21, 469-476
Perrone, L., Paladino, S., Mazzone, M., Nitsch, L., Gulisano, M. and Zurzolo, C. (2005) Functional interaction between p75 NTR and TrkA: the endocytic trafficking of p75 NTR is driven by TrkA and regulates TrkA-mediated signalling. Biochem. J. 385, 233-241
Zhang, J., Yan, W. and Chen, X. (2006) p53 is required for nerve growth factor-mediated differentiation of PC12 cells via regulation of TrkA levels. Cell Death Differ. 13, 2118-2128 (Pubitemid 44742695)
de Mestre, A. M., Khachigian, L. M., Santiago, F. S., Staykova, M. A. and Hulett, M. D. (2003) Regulation of inducible heparanase gene transcription in activated T cells by early growth response 1. J. Biol. Chem. 278, 50377-50385 (Pubitemid 37548881)
de Mestre, A. M., Rao, S., Hornby, J. R., Soe-Htwe, T., Khachigian, L. M. and Hulett, M. D. (2005) Early growth response gene 1 (EGR1) regulates heparanase gene transcription in tumor cells. J. Biol. Chem. 280, 35136-35147 (Pubitemid 41532700)
Tai, T. C., Wong-Faull, D. C., Claycomb, R. and Wong, D. L. (2006) Nerve growth factor regulates adrenergic expression. Mol. Pharmacol. 70, 1792-1801
Vlodavsky, I., Goldshmidt, O., Zcharia, E., Metzger, S., Chajek-Shaul, T., Atzmon, R., Guatta-Rangini, Z. and Friedmann, Y. (2001) Molecular properties and involvement of heparanase in cancer progression and normal development. Biochimie 83, 831-839 (Pubitemid 32821249)
Sotnikov, I., Hershkoviz, R., Grabovsky, V., Ilan, N., Cahalon, L., Vlodavsky, I., Alon, R. and Lider, O. (2004) Enzymatically quiescent heparanase augments T cell interactions with VCAM-1 and extracellular matrix components under versatile dynamic contexts. J. Immunol. 172, 5185-5193 (Pubitemid 38542014)
Zetser, A., Bashenko, Y., Miao, H. Q., Vlodavsky, I. and Ilan, N. (2003) Heparanase affects adhesive and tumorigenic potential of human glioma cells. Cancer Res. 63, 7733-7741 (Pubitemid 37466704)
Zetser, A., Bashenko, Y., Edovitsky, E., Levy-Adam, F., Vlodavsky, I. and Ilan, N. (2006) Heparanase induces vascular endothelial growth factor expression: correlation with p38 phosphorylation levels and Src activation. Cancer Res. 66, 1455-1463 (Pubitemid 43259926)
Nadir, Y., Brenner, B., Zetser, A., Ilan, N., Shafat, I., Zcharia, E., Goldshmidt, O. and Vlodavsky, I. (2006) Heparanase induces tissue factor expression in vascular endothelial and cancer cells. J. Thromb. Haemost. 4, 2443-2451 (Pubitemid 44575440)
Goldshmidt, O., Zcharia, E., Aingorn, H., Guatta-Rangini, Z., Atzmon, R., Michal, I., Pecker, I., Mitrani, E. and Vlodavsky, I (2001) Expression pattern and secretion of human and chicken heparanase are determined by their signal peptide sequence. J. Biol. Chem. 276, 29178-29187
Moretti, M., Sinnappah-Kang, N. D., Toller, M., Curcio, F. and Marchetti, D. (2006) HPSE-1 expression and functionality in differentiating neural cells. J. Neurosci. Res. 83, 694-701 (Pubitemid 43384862)
Ethell, I. M., Irie, F., Kalo, M. S., Couchman, J. R., Pasquale, E. B. and Yamaguchi, Y. (2001) EphB/syndecan-2 signaling in dendritic spine morphogenesis. Neuron 31, 1001-1013 (Pubitemid 32925285)
Guizzetti, M., Moore, N. H., Giordano, G. and Costa, L. G. (2008) Modulation of neuritogenesis by astrocyte muscarinic receptors. J. Biol. Chem. 283, 31884-31897
Kiryushko, D., Kofoed, T., Skladchikova, G., Holm, A., Berezin, V. and Bock, E. (2003) A synthetic peptide ligand of neural cell adhesion molecule (NCAM), C3d, promotes neuritogenesis and synaptogenesis and modulates presynaptic function in primary cultures of rat hippocampal neurons. J. Biol. Chem. 278, 12325-12334 (Pubitemid 36800216)
Riehl, R., Johnson, K., Bradley, R., Grunwald, G. B., Cornel, E., Lilienbaum, A. and Holt, C. E. (1996) Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo. Neuron 17, 837-848 (Pubitemid 26424012)
Leventhal, P. S. and Feldman, E. L. (1996) Tyrosine phosphorylation and enhanced expression of paxillin during neuronal differentiation in vitro. J. Biol. Chem. 271, 5957-5960 (Pubitemid 26095391)
Gorio, A., Lesma, E., Vergani, L. and Di Giulio, A. M. (1997) Glycosaminoglycan supplementation promotes nerve regeneration and muscle reinnervation. Eur. J. Neurosci. 303, 21-26
Lesma, E., Di Giulio, A. M., Ferro, L., Prino, G. and Gorio, A. (1996) Glycosaminoglycans in nerve injury: 1. Low doses of glycosaminoglycans promote neurite formation. J. Neurosci. Res. 46, 565-571 (Pubitemid 26404649)
Fukuda, M., Gotoh, Y., Tachibana, T., Dell, K., Hattori, S., Yoneda, Y. and Nishida, E. (1995) Induction of neurite outgrowth by MAP kinase in PC12 cells. Oncogene 11, 239-244
Cowley, S., Paterson, H., Kemp, P. and Marshall, C. J. (1994) Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells. Cell 77, 841-852 (Pubitemid 24187682)
Morooka, T. and Nishida, E. (1998) Requirement of p38 mitogen-activated protein kinase for neuronal differentiation in PC12 cells. J. Biol. Chem. 273, 24285-24288 (Pubitemid 28454911)