Progranulin promotes neurite outgrowth and neuronal differentiation by regulating GSK-3β
详细信息 查看全文
- 作者：Xue Gao (1)
Alvin P. Joselin (1)
Lei Wang (1)
Amar Kar (1)
Payal Ray (1)
Andrew Bateman (2)
Alison M. Goate (3)
Jane Y. Wu (1) - 关键词：progranulin ; frontotemporal lobar degeneration ; glycogen synthase kinase 3 beta (GSK ; 3β) ; neurite outgrowth
- 刊名：Protein & Cell
- 出版年：2010
- 出版时间：June 2010
- 年：2010
- 卷：1
- 期：6
- 页码：552-562
- 全文大小：348KB
- 参考文献：1. Amador-Ortiz, C., Lin, W.L., Ahmed, Z., Personett, D., Davies, P., Duara, R., Graff-Radford, N.R., Hutton, M.L., and Dickson, D.W. (2007). TDP-43 immunoreactivity in hippocampal sclerosis and Alzheimer’s disease. Ann Neurol 61, 435-45. CrossRef
2. Arai, T., Hasegawa, M., Akiyama, H., Ikeda, K., Nonaka, T., Mori, H., Mann, D., Tsuchiya, K., Yoshida, M., Hashizume, Y., / et al. (2006). TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem Biophys Res Commun 351, 602-11. CrossRef
3. Armstrong, R.A., Ellis, W., Hamilton, R.L., Mackenzie, I.R., Hedreen, J., Gearing, M., Montine, T., Vonsattel, J.P., Head, E., Lieberman, A.P., / et al. (2010). Neuropathological heterogeneity in frontotemporal lobar degeneration with TDP-43 proteinopathy: a quantitative study of 94 cases using principal components analysis. J Neural Transm 117, 227-39. CrossRef
4. Baba, T., Hoff, H.B. 3rd, Nemoto, H., Lee, H., Orth, J., Arai, Y., and Gerton, G.L. (1993). Acrogranin, an acrosomal cysteine-rich glycoprotein, is the precursor of the growth-modulating peptides, granulins, and epithelins, and is expressed in somatic as well as male germ cells. Mol Reprod Dev 34, 233-43. CrossRef
5. Baker, M., Mackenzie, I.R., Pickering-Brown, S.M., Gass, J., Rademakers, R., Lindholm, C., Snowden, J., Adamson, J., Sadovnick, A.D., Rollinson, S., / et al. (2006). Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature 442, 916-19. CrossRef
6. Bateman, A., Belcourt, D., Bennett, H., Lazure, C., and Solomon, S. (1990). Granulins, a novel class of peptide from leukocytes. Biochem Biophys Res Commun 173, 1161-168. CrossRef
7. Beurel, E., and Jope, R.S. (2006). The paradoxical pro- and antiapoptotic actions of GSK3 in the intrinsic and extrinsic apoptosis signaling pathways. Prog Neurobiol 79, 173-89. CrossRef
8. Bhandari, V., Palfree, R.G., and Bateman, A. (1992). Isolation and sequence of the granulin precursor cDNA from human bone marrow reveals tandem cysteine-rich granulin domains. Proc Natl Acad Sci U S A 89, 1715-719. CrossRef
9. Brouwers, N., Nuytemans, K., van der Zee, J., Gijselinck, I., Engelborghs, S., Theuns, J., Kumar-Singh, S., Pickut, B.A., Pals, P., Dermaut, B., / et al. (2007). Alzheimer and Parkinson diagnoses in progranulin null mutation carriers in an extended founder family. Arch Neurol 64, 1436-446. CrossRef
10. Cairns, N.J., Bigio, E.H., Mackenzie, I.R., Neumann, M., Lee, V.M., Hatanpaa, K.J., White, C.L. 3rd, Schneider, J.A., Grinberg, L.T., Halliday, G., / et al, and the Consortium for Frontotemporal Lobar Degeneration. (2007a). Neuropathologic diagnostic and nosologic criteria for frontotemporal lobar degeneration: consensus of the Consortium for Frontotemporal Lobar Degeneration. Acta Neuropathol 114, 5-2. CrossRef
11. Cotman, C.W., Poon, W.W., Rissman, R.A., and Blurton-Jones, M. (2005). The role of caspase cleavage of tau in Alzheimer disease neuropathology. J Neuropathol Exp Neurol 64, 104-12.
12. Cross, D.A., Alessi, D.R., Cohen, P., Andjelkovich, M., and Hemmings, B.A. (1995). Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785-89. CrossRef
13. Cruts, M., Gijselinck, I., van der Zee, J., Engelborghs, S., Wils, H., Pirici, D., Rademakers, R., Vandenberghe, R., Dermaut, B., Martin, J.J., / et al. (2006). Null mutations in progranulin cause ubiquitinpositive frontotemporal dementia linked to chromosome 17q21. Nature 442, 920-24. CrossRef
14. Daniel, R., Daniels, E., He, Z., and Bateman, A. (2003). Progranulin (acrogranin/PC cell-derived growth factor/granulin-epithelin precursor) is expressed in the placenta, epidermis, microvasculature, and brain during murine development. Dev Dyn 227, 593-99. CrossRef
15. Daniel, R., He, Z., Carmichael, K.P., Halper, J., and Bateman, A. (2000). Cellular localization of gene expression for progranulin. J Histochem Cytochem 48, 999-009.
16. Delehedde, M., Sergeant, N., Lyon, M., Rudland, P.S., and Fernig, D. G. (2001). Hepatocyte growth factor/scatter factor stimulates migration of rat mammary fibroblasts through both mitogen-activated protein kinase and phosphatidylinositol 3-kinase/Akt pathways. Eur J Biochem 268, 4423-429. CrossRef
17. Dill, J., Wang, H., Zhou, F., and Li, S. (2008). Inactivation of glycogen synthase kinase 3 promotes axonal growth and recovery in the CNS. J Neurosci 28, 8914-928. CrossRef
18. Eickholt, B.J., Walsh, F.S., and Doherty, P. (2002). An inactive pool of GSK-3 at the leading edge of growth cones is implicated in Semaphorin 3A signaling. J Cell Biol, 157, 211-17. CrossRef
19. Encinas, M., Iglesias, M., Liu, Y., Wang, H., Muhaisen, A., Ce?a, V., Gallego, C., and Comella, J.X. (2000). Sequential treatment of SHSY5Y cells with retinoic acid and brain-derived neurotrophic factor gives rise to fully differentiated, neurotrophic factor-dependent, human neuron-like cells. J Neurochem 75, 991-003. CrossRef
20. Ferrer, I., Gomez-Isla, T., Puig, B., Freixes, M., Ribé, E., Dalfó, E., and Avila, J. (2005). Current advances on different kinases involved in tau phosphorylation, and implications in Alzheimer’s disease and tauopathies. Curr Alzheimer Res 2, 3-8. CrossRef
21. Fuentealba, R.A., Farias, G., Scheu, J., Bronfman, M., Marzolo, M.P., and Inestrosa, N.C. (2004). Signal transduction during amyloidbeta-peptide neurotoxicity: role in Alzheimer disease. Brain Res Brain Res Rev 47, 275-89. CrossRef
22. Gass, J., Cannon, A., Mackenzie, I.R., Boeve, B., Baker, M., Adamson, J., Crook, R., Melquist, S., Kuntz, K., Petersen, R., / et al. (2006). Mutations in progranulin are a major cause of ubiquitin-positive frontotemporal lobar degeneration. Hum Mol Genet 15, 2988-001. CrossRef
23. Gervais, F.G., Xu, D., Robertson, G.S., Vaillancourt, J.P., Zhu, Y., Huang, J., LeBlanc, A., Smith, D., Rigby, M., Shearman, M.S., / et al. (1999). Involvement of caspases in proteolytic cleavage of Alzheimer’s amyloid-beta precursor protein and amyloidogenic A beta peptide formation. Cell 97, 395-06. CrossRef
24. Gijselinck, I., Van Broeckhoven, C., and Cruts, M. (2008). Granulin mutations associated with frontotemporal lobar degeneration and related disorders: An update. Hum Mutat 29, 1373-386. CrossRef
25. Guyant-Maréchal, L., Laquerrière, A., Duyckaerts, C., Dumanchin, C., Bou, J., Dugny, F., Le Ber, I., Frébourg, T., Hannequin, D., and Campion, D. (2006). Valosin-containing protein gene mutations: clinical and neuropathologic features. Neurology 67, 644-51. CrossRef
26. He, Z., and Bateman, A. (1999). Progranulin gene expression regulates epithelial cell growth and promotes tumor growth in vivo. Cancer Res 59, 3222-229.
27. He, Z., Ong, C.H., Halper, J., and Bateman, A. (2003). Progranulin is a mediator of the wound response. Nat Med 9, 225-29. CrossRef
28. J?ms?, A., Hasslund, K., Cowburn, R.F., B?ckstr?m, A., and Vas?nge, M. (2004). The retinoic acid and brain-derived neurotrophic factor differentiated SH-SY5Y cell line as a model for Alzheimer’s disease-like tau phosphorylation. Biochem Biophys Res Commun 319, 993-000. CrossRef
29. Jiang, H., Guo, W., Liang, X., and Rao, Y. (2005). Both the establishment and the maintenance of neuronal polarity require active mechanisms: critical roles of GSK-3beta and its upstream regulators. Cell 120, 123-35.
30. Kim, W.Y., Zhou, F.Q., Zhou, J., Yokota, Y., Wang, Y.M., Yoshimura, T., Kaibuchi, K., Woodgett, J.R., Anton, E.S., and Snider, W.D. (2006). Essential roles for GSK-3s and GSK-3-primed substrates in neurotrophin-induced and hippocampal axon growth. Neuron 52, 981-96. CrossRef
31. King, T.D., Bijur, G.N., and Jope, R.S. (2001). Caspase-3 activation induced by inhibition of mitochondrial complex I is facilitated by glycogen synthase kinase-3beta and attenuated by lithium. Brain Res 919, 106-14. CrossRef
32. Koh, S.H., Lee, Y.B., Kim, K.S., Kim, H.J., Kim, M., Lee, Y.J., Kim, J., Lee, K.W., and Kim, S.H. (2005). Role of GSK-3beta activity in motor neuronal cell death induced by G93A or A4V mutant hSOD1 gene. Eur J Neurosci 22, 301-09. CrossRef
33. Liu, G., Beggs, H., Jürgensen, C., Park, H.T., Tang, H., Gorski, J., Jones, K.R., Reichardt, L.F., Wu, J., and Rao, Y. (2004). Netrin requires focal adhesion kinase and Src family kinases for axon outgrowth and attraction. Nat Neurosci 7, 1222-232. CrossRef
34. Mackenzie, I.R., and Rademakers, R. (2007). The molecular genetics and neuropathology of frontotemporal lobar degeneration: recent developments. Neurogenetics 8, 237-48. CrossRef
35. Mann, D.M. (1998). Dementia of frontal type and dementias with subcortical gliosis. Brain Pathol 8, 325-38.
36. Mukherjee, O., Wang, J., Gitcho, M., Chakraverty, S., Taylor-Reinwald, L., Shears, S., Kauwe, J.S., Norton, J., Levitch, D., Bigio, E.H., / et al. (2008). Molecular characterization of novel progranulin (GRN) mutations in frontotemporal dementia. Hum Mutat 29, 512-21. CrossRef
37. Nakashima-Yasuda, H., Uryu, K., Robinson, J., Xie, S.X., Hurtig, H., Duda, J.E., Arnold, S.E., Siderowf, A., Grossman, M., Leverenz, J. B., / et al. (2007). Co-morbidity of TDP-43 proteinopathy in Lewy body related diseases. Acta Neuropathol 114, 221-29. CrossRef
38. Neary, D., Snowden, J.S., Northen, B., and Goulding, P. (1988). Dementia of frontal lobe type. J Neurol Neurosurg Psychiatry 51, 353-61. CrossRef
39. Neumann, M., Sampathu, D.M., Kwong, L.K., Truax, A.C., Micsenyi, M.C., Chou, T.T., Bruce, J., Schuck, T., Grossman, M., Clark, C.M., / et al. (2006). Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314, 130-33. CrossRef
40. Neumann, M. (2007). TDP-43 proteinopathies: a new class of proteinopathies. Future Neurol 2, 549-57. CrossRef
41. Ong, C.H., He, Z., Kriazhev, L., Shan, X., Palfree, R.G., and Bateman, A. (2006). Regulation of progranulin expression in myeloid cells. Am J Physiol Regul Integr Comp Physiol 291, 1602-612.
42. Phiel, C., Wilson, C., Lee, V., and Klein, P. (2003). GSK-3α regulates production of Alzheimer’s disease amyloid-? peptides. Nature 423, 435-39. CrossRef
43. Pickering-Brown, S.M., Baker, M., Gass, J., Boeve, B.F., Loy, C.T., Brooks, W.S., Mackenzie, I.R., Martins, R.N., Kwok, J.B., Halliday, G.M., / et al. (2006). Mutations in progranulin explain atypical phenotypes with variants in MAPT. Brain 129, 3124-126. CrossRef
44. Plowman, G.D., Green, J.M., Neubauer, M.G., Buckley, S.D., McDonald, V.L., Todaro, G.J., and Shoyab, M. (1992). The epithelin precursor encodes two proteins with opposing activities on epithelial cell growth. J Biol Chem 267, 13073-3078.
45. Rohn, T.T., Head, E., Nesse, W.H., Cotman, C.W., and Cribbs, D.H. (2001). Activation of caspase-8 in the Alzheimer’s disease brain. Neurobiol Dis 8, 1006-016. CrossRef
46. Rohn, T.T., Rissman, R.A., Davis, M.C., Kim, Y.E., Cotman, C.W., and Head, E. (2002). Caspase-9 activation and caspase cleavage of tau in the Alzheimer’s disease brain. Neurobiol Dis 11, 341-54. CrossRef
47. Shankaran, S.S., Capell, A., Hruscha, A.T., Fellerer, K., Neumann, M., Schmid, B., and Haass, C. (2008). Missense mutations in the progranulin gene linked to frontotemporal lobar degeneration with ubiquitin-immunoreactive inclusions reduce progranulin production and secretion. J Biol Chem 283, 1744-753. CrossRef
48. Skibinski, G., Parkinson, N.J., Brown, J.M., Chakrabarti, L., Lloyd, S. L., Hummerich, H., Nielsen, J.E., Hodges, J.R., Spillantini, M.G., Thusgaard, T., / et al. (2005). Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in frontotemporal dementia. Nat Genet 37, 806-08. CrossRef
49. Sleegers, K., Brouwers, N., Maurer-Stroh, S., van Es, M.A., Van Damme, P., van Vught, P.W., van der Zee, J., Serneels, S., De Pooter, T., Van den Broeck, M., / et al. (2008). Progranulin genetic variability contributes to amyotrophic lateral sclerosis. Neurology 71, 253-59. CrossRef
50. Sleegers, K., Cruts, M., Van Broeckhoven, C. (2010). Molecular pathways of frontotemporal lobar degeneration. Annu Rev Neurosci 33, 71-8. CrossRef
51. Smith, C.J., Anderton, B.H., Davis, D.R., and Gallo, J.M. (1995). Tau isoform expression and phosphorylation state during differentiation of cultured neuronal cells. FEBS Lett 375, 243-48. CrossRef
52. Takashima, A., Noguchi, K., Sato, K., Hoshino, T., and Imahori, K. (1993). Tau protein kinase I is essential for amyloid beta-proteininduced neurotoxicity. Proc Natl Acad Sci U S A 90, 7789-793. CrossRef
53. Van Damme, P., Van Hoecke, A., Lambrechts, D., Vanacker, P., Bogaert, E., van Swieten, J., Carmeliet, P., Van Den Bosch, L., and Robberecht, W. (2008). Progranulin functions as a neurotrophic factor to regulate neurite outgrowth and enhance neuronal survival. J Cell Biol 181, 37-1. CrossRef
54. van Swieten, J.C., and Heutink, P. (2008). Mutations in progranulin (GRN) within the spectrum of clinical and pathological phenotypes of frontotemporal dementia. Lancet Neurol 7, 965-74. CrossRef
55. Verret, L., Jankowsky, J.L., Xu, G.M., Borchelt, D.R., and Rampon, C. (2007). Alzheimer’s-type amyloidosis in transgenic mice impairs survival of newborn neurons derived from adult hippocampal neurogenesis. J Neurosci 27, 6771-780. CrossRef
56. Winner, B., Rockenstein, E., Lie, D.C., Aigner, R., Mante, M., Bogdahn, U., Couillard-Despres, S., Masliah, E., and Winkler, J. (2008). Mutant alpha-synuclein exacerbates age-related decrease of neurogenesis. Neurobiol Aging 29, 913-25. CrossRef
57. Yang, F., Sun, X., Beech, W., Teter, B., Wu, S., Sigel, J., Vinters, H.V., Frautschy, S.A., and Cole, G.M. (1998). Antibody to caspase-cleaved actin detects apoptosis in differentiated neuroblastoma and plaqueassociated neurons and microglia in Alzheimer’s disease. Am J Pathol 152, 379-89.
58. Yoshimura, T., Kawano, Y., Arimura, N., Kawabata, S., Kikuchi, A., and Kaibuchi, K. (2005). GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120, 137-49. CrossRef
59. Yu, J.Y., Taylor, J., DeRuiter, S.L., Vojtek, A.B., and Turner, D.L. (2003). Simultaneous inhibition of GSK3alpha and GSK3beta using hairpin siRNA expression vectors. Mol Ther 7, 228-36. CrossRef
60. Zanocco-Marani, T., Bateman, A., Romano, G., Valentinis, B., He, Z. H., and Baserga, R. (1999). Biological activities and signaling pathways of the granulin/epithelin precursor. Cancer Res 59, 5331-340.
61. Zhang, Y.J., Xu, Y.F., Dickey, C.A., Buratti, E., Baralle, F., Bailey, R., Pickering-Brown, S., Dickson, D., and Petrucelli, L. (2007). Progranulin mediates caspase-dependent cleavage of TAR DNA binding protein-43. J Neurosci 27, 10530-0534. CrossRef
62. Zhou, J., Gao, G., Crabb, J.W., and Serrero, G. (1993). Purification of an autocrine growth factor homologous with mouse epithelin precursor from a highly tumorigenic cell line. J Biol Chem 268, 10863-0869.
63. Zhu, J., Nathan, C., Jin, W., Sim, D., Ashcroft, G.S., Wahl, S.M., Lacomis, L., Erdjument-Bromage, H., Tempst, P., Wright, C.D., / et al. (2002). Conversion of proepithelin to epithelins: roles of SLPI and elastase in host defense and wound repair. Cell 111, 867-78. CrossRef - 作者单位：Xue Gao (1)
Alvin P. Joselin (1)
Lei Wang (1)
Amar Kar (1)
Payal Ray (1)
Andrew Bateman (2)
Alison M. Goate (3)
Jane Y. Wu (1)
1. Department of Neurology, Lurie Cancer Center, Center for Genetic Medicine Northwestern University Feinberg School of Medicine, Chicago, IL, 60611, USA
2. Division of Experimental Medicine, McGill University, and Endocrine Research Laboratory, Royal Victoria Hospital, Montréal, Québec, Canada
3. Department of Psychiatry, Washington University School of Medicine, St. Louis, MO, 63110, USA
文摘
Progranulin (PGRN) has recently emerged as a key player in a subset of frontotemporal dementias (FTD). Numerous mutations in the progranulin gene have been identified in patients with familial or sporadic frontotemporal lobar degeneration (FTLD). In order to understand the molecular mechanisms by which PGRN deficiency leads to FTLD, we examined activity of PGRN in mouse cortical and hippocampal neurons and in human neuroblastoma SH-SY5Y cells. Treatment of mouse neurons with PGRN protein resulted in an increase in neurite outgrowth, supporting the role of PGRN as a neurotrophic factor. PGRN treatment stimulated phosphorylation of glycogen synthase kinase-3 beta (GSK-3β) in cultured neurons. Knockdown of PGRN in SH-SY5Y cells impaired retinoic acid induced differentiation and reduced the level of phosphorylated GSK-3β. PGRN knockdown cells were also more sensitized to staurosporine-induced apoptosis. These results reveal an important role of PGRN in neurite outgrowth and involvement of GSK-3β in mediating PGRN activity. Identification of GSK-3β activation as a downstream event for PGRN signaling provides a mechanistic explanation for PGRN activity in the nervous system. Our work also suggest that loss of axonal growth stimulation during neural injury repair or deficits in axonal repair may contribute to neuronal damage or axonal loss in FTLD associated with PGRN mutations. Finally, our study suggests that modulating GSK-3β or similar signaling events may provide therapeutic benefits for FTLD cases associated with PGRN mutations.