Protease nexin 1 and its receptor LRP modulate SHH signalling during cerebellar development

Development

Volumn 134, Issue 9, 2007, Pages 1745-1754

  Vaillant, Catherine ^a   Michos, Odyssé ^b   Orlicki, Slobodanka ^a   Brellier, Florence ^a   Taieb, Sabrina ^a   Moreno, Eliza ^a   Te, Hélène ^a   Zeller, Rolf ^b   Monard, Denis ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Cerebellum; Low density lipoprotein; Mouse; Proliferation; Protease nexin 1; Receptor related protein (LRP); Sonic hedgehog

Indexed keywords

CYCLIN D1; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; PROTEASE NEXIN I; SONIC HEDGEHOG PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL CYCLE ARREST; CELL ISOLATION; CELL PROLIFERATION; CEREBELLUM; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE TARGETING; IN VIVO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEFICIENCY; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CELLS, CULTURED; CEREBELLUM; FEMALE; HEDGEHOG PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, CELL SURFACE; RECEPTORS, LDL; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

ERINACEIDAE; MUS;

EID: 34248996368     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02840     Document Type: Article

References (47)

1. Baker, J. B., Low, D. A., Simmer, R. L. and Cunningham, D. D. (1980). Protease-nexin: a cellular component that links thrombin and plasminogen activator and mediates their binding to cells. Cell 21, 37-45.
2. Ben Arie, N., Bellen, H. J., Armstrong, D. L., McCall, A. E., Gordadze, P. R., Guo, Q., Matzuk, M. M. and Zoghbl, H. Y. (1997). Math1 is essential for genesis of cerebellar granule neurons. Nature 390, 169-172.
3. Corrales, J. D., Rocco, G. L., Blaess, S., Guo, Q. and Joyner, A. L. (2004). Spatial pattern of sonic hedgehog signaling through Gli genes during cerebellum development. Development 131, 5581-5590.
4. Corrales, J. D., Blaess, S., Mahoney, E. M. and Joyner, A. L. (2006). The level of sonic hedgehog signaling regulates the complexity of cerebellar foliation. Development 133, 1811-1821.
5. Crisp, R. J., Knauer, D. J. and Knauer, M. F. (2000). Roles of the helparin and low density lipid receptor-related protein-binding sites of protease nexin 1 (PN1) in urokinase-PN1 complex catabolism. The PN1 heparin-binding site mediates complex retention and degradation but not cell surface binding or internalization. J. Biol. Chem. 275, 19628-19637.
6. Croy, J. E., Shin, W. D., Knauer, M. F., Knauer, D. J. and Komives, E. A. (2003). All three LDL receptor homology regions of the LDL receptor-related protein bind multiple ligands. Biochemistry 42, 13049-13057.
7. Dahmane, N. and Altaba, A. (1999). Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126, 3089-3100.
8. Dai, P., Akimaru, H., Tanaka, Y., Maekawa, T., Nakafuku, M. and Ishii, S. (1999). Sonic Hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. J. Biom. Chem. 274, 8143-8152.
9. Easwaran, V., Lee, S. H., Inge, L., Guo, L., Goldbeck, C., Garrett, E., Wiesmann, M., Garcia, P. D., Fuller, J. H., Chan, V. et al. (2003). beta-Catenin regulates vascular endothelial growth factor expression in colon cancer. Cancer Res. 63, 3145-3153.
10. Gleeson, J. G., Lin, P. T., Flanagan, L. A. and Walsh, C. A. (1999). Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23, 257-271.
11. Glinka, A., Wu, W., Delius, H., Monaghan, A. P., Blumenstock, C. and Niehours, C. (1998). Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 391, 357-362.
12. Gloor, S., Odink, K., Guenther, J., Nick, H. and Monard, D. (1986). A glia-derived neurite promoting factor with protease inhibitory activity belongs to the protease nexins. Cell 47, 687-693.
13. Goodrich, L. V. and Scott, M. P. (1998). Hedgehog and patched in neural development and disease. Neuron 21, 1243-1257.
14. Hatten, M. E. (1985). Neuronal regulation of astroglial morphology and proliferation in vitro. J. Cell Biol. 100, 384-396.
15. Hatten, M. E., Lynch, M., Rydel, R. E., Sanchez, J., Joseph-Silverstein, J., Moscatelli, D. and Rifkin, D. B. (1988). In vitro neurite extension by granule neurons is dependent upon astroglial-derived fibroblast growth factor. Dev. Biol. 125, 280-289.
16. Herz, J., Goldstein, J. L., Strickland, D. K., Ho, Y. K. and Brown, M. S. (1991). 39-kDa protein modulates binding of ligands to low density lipoprotein receptor-related protein/alpha 2-macroglobulin receptor. J. Biol. Chem. 266, 21232-21238.
17. Ho, K. S. and Scott, M. P. (2002). Sonic hedgehog in the nervous system: functions, modifications and mechanisms. Curr. Opin. Neurobiol. 12, 57-63.
18. Ingham, P. W. and McMahon, A. P. (2001). Hedgehog signaling in animal development: paradigms and principles. Genes Dev 15, 3059-3087.
19. Kenney, A. M. and Rowitch, D. H. (2000). Sonic hedgehog promotes G(1) cyclin expression and sustained cell cycle progression in mammalian neuronal precursors. Mol. Cell. Biol. 20, 9055-9067.
20. Klein R. S., Rubin, J. B., Gibson, H. D., DeHaan, E. N., Alvarez-Hernandez, X., Segal, R. A. and Luster, A. D. (2001). SDF-1 alpha induces chemotaxis and enhances Sonic hedgehog-induced proliferation of cerebellar granule cells. Development 128, 1971-1981.
21. Knauer, D. J., Majumdar, D., Fong, P. C. and Knauer, M. F. (2000). SERPIN regulation of factor XIa. The novel observation that protease nexin 1 in the presence of helparin is a more potent inhibitor of factor XIa than C1 inhibitor. J. Biol. Chem. 275, 37340-37346.
22. Knauer, M. F., Hawley, S. B. and Knauer, D. J. (1997a). Identification of a binding site in protease nexin I (PN1) required for the receptor mediated internalization of PN1-thrombin complexes. J. Biol. Chem. 272, 12261-12264.
23. Knauer, M. F., Kridel, S. J., Hawley, S. B. and Knauer, D. J. (1997b). The efficient catabolism of thrombin-protease nexin 1 complexes is a synergistic mechanism that requires both the LDL receptor-related protein and cell surface heparins. J. Biol. Chem. 272, 29039-29045.
24. Kury, P., Schaeren-Wiemers, N. and Monard, D. (1997). Protease nexin-1 is expressed at the mouse met-/mesencephalic junction and FGF signaling regulates its promoter activity in primary met-/mesencephalic cells. Development 124, 1251-1262.
25. Kvajo. M., Albrecht, H., Meins, M., Hengst, U., Troncoso, E., Lefort, S., Kiss, J. Z., Petersen, C. C. and Monard, D. (2004). Regulation of brain proteolytic activity is necessary for the in vivo function of NMDA receptors. J. Neurosci. 24, 9734-9743.
26. Lee, A., Kessler, J. D., Read, T. A., Kaiser, C., Corbell, D., Huttner, W. B., Johnson, J. E. and Wechsler-Reya, R. J. (2005). Isolation of neural stem cells from the postnatal cerebellum. Nat. Neurosci. 8, 723-729.
27. Lee, J., Platt, K. A., Censullo, P. and Altaba, A. (1997). Gli1 is a target of Sonic hedgehog that induces ventral neural tube development. Development 124, 2537-2552.
28. Lewis, P. M., Gritli-Linde, A., Smeyne, R., Kottmann, A. and McMahon, A. P. (2004). Sonic hedgehog signaling is required for expansion of granule neuron precursors and patterning of the mouse cerebellum. Dev. Biol. 270, 393-410.
29. Luthi, A., Van der Putten, H., Botteri, F. M., Mansuy, I. M., Meins, M., Frey, U., Sansig, G., Portet, C., Schmutz, M., Schroder, M. et al. (1997). Endogenous serine protease inhibitor modulates epileptic activity and hippocampal long-term potentiation. J. Neurosci. 17, 4688-4699.
30. Mansuy, I. M., Van der Putten, H., Schmid, P., Meins, M., Botteri, F. M. and Monard, D. (1993). Variable and multiple expression of Protease Nexin-1 during mouse organogenesis and nervous system development. Development 119, 1119-1134.
31. McCarthy, R. A., Barth, J. L., Chintalapudi, M. R., Knaak, C. and Argraves, W. S. (2002). Megalin functions as an endocytic sonic hedgehog receptor. J. Biol. Chem. 277, 25660-25667.
32. Meier, R., Spreyer, R, Ortmann, R., Harel, A. and Monard, D. (1989). Induction of glia-derived nexin after lesion of a peripheral nerve. Nature 342, 548-550.
33. Michos, O., Panman, L., Vintersten, K., Beier, K., Zeller, R. and Zuniga, A. (2004). Gremlin-mediated BMP antagonism induces the epithelial-mesenchymal feedback signaling controlling metanephric kidney and limb organogenesis. Development 131, 3401-3410.
34. Miyazawa, K., Himi, T., Garcia, V., Yamagishi, H., Sato, S. and Ishizaki, Y. (2000). A role for p27/Kip1 in the control of cerebellar granule cell precursor proliferation. J. Neurosci. 20, 5756-5763.
35. Nicot A., Lelievre, V., Tam, J., Waschek, J. A. and DiCicco-Bloom, E. (2002). Pituitary adenylate cyclase-activating polypeptide and sonic hedgehog interact to control cerebellar granule precursor cell proliferation. J. Neurosci. 22, 9244-9254.
36. Nybakken, K. and Perrimon, N. (2002). Hedgehog signal transduction: recent findings. Curr. Opin. Genet Dev 12, 503-511.
37. Pons, S., Trejo, J. L., Martinez-Morales, J. R. and Marti, E. (2001). Vitronectin regulates Sonic hedgehog activity during cerebellum development through CREB phosphorylation. Development 128, 1481-1492.
38. Rios, I., Alvarez-Rodriguez, R., Marti, E. and Pons, S. (2004). Bmp2 antagonizes sonic hedgehog-mediated proliferation of cerebellar granule neurones through Smad5 signalling. Development 131, 3159-3168.
39. Rubin, J. B., Choi, Y. and Segal, R. A. (2002). Cerebellar proteoglycans regulate sonic hedgehog responses during development. Development 129, 2223-2232.
40. Schneider, W. J. and Nimpf, J. (2003). LDL receptor relatives at the crossroad of endocytosis and signaling. Cell Mol. Life Sci. 60, 892-903.
41. Sommer, J., Meyhack, B., Rovelli, G., Buergi, R. and Monard, D. (1989). Synthesis of glia-derived nexin in yeast. Gene 85, 453-459.
42. Spoelgen, R., Hammes, A., Anzenberger, U., Zechner, D., Andersen, O. M., Jerchow, B. and Willnow, T. E. (2005). LRP2/megalin is required for patterning of the ventral telencephalon. Development 132, 405-414.
43. Strickland, D. K. and Ranganathan, S. (2003). Diverse role of LDL receptor-related protein in the clearance of proteases and in signaling. J. Thromb. Haemost 1, 1663-1670.
44. Wallace, V. A. (1999). Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr. Biol. 9, 445-448.
45. Wechsler-Reya, R. J. and Scott, M. P. (1999). Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22, 103-114.
46. Yao, S., Lum, L. and Beachy, P. (2006). The ihog cell-surface proteins bind Hedgehog and mediate pathway activation. Cell 125, 343-357.
47. Zeller, R. (2004). It takes time to make a pinky: unexpected insights into how SHH patterns vertebrate digits. Sci. STKE 2004, e53.