The neurotrophic properties of progranulin depend on the granulin E domain but do not require sortilin binding

Neurobiology of Aging

Volumn 34, Issue 11, 2013, Pages 2541-2547

  De Muynck, Louis ^a,b   Herdewyn, Sarah ^a,b,c   Beel, Sander ^a,b   Scheveneels, Wendy ^a,b   Van Den Bosch, Ludo ^a,b   Robberecht, Wim ^a,b,c   Van Damme, Philip ^a,b,c  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

Blocking antibody; Frontotemporal lobar degeneration; Granulin E; Progranulin; Sortilin; Zebrafish

Indexed keywords

GRANULIN E; NEUROPEPTIDE; PROGRANULIN; SORTILIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; GENE DELETION; GENE SILENCING; IN VITRO STUDY; IN VIVO STUDY; NEUROPROTECTION; NEUROTROPISM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; ZEBRA FISH;

BLOCKING ANTIBODY; FRONTOTEMPORAL LOBAR DEGENERATION; GRANULIN E; PROGRANULIN; SORTILIN; ZEBRAFISH;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; ANIMALS, NEWBORN; ANTIBODIES; BINDING SITES; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; CYCLIC S-OXIDES; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; ENDOCYTOSIS; ENZYME INHIBITORS; IMMUNOPRECIPITATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MORPHOLINES; MOTOR NEURONS; NERVE GROWTH FACTORS; NEURITES; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, WISTAR; THIAZOLES; ZEBRAFISH;

EID: 84881553329     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.04.022     Document Type: Article

References (41)

1. Baker M., Mackenzie I.R., Pickering-Brown S.M., Gass J., Rademakers R., Lindholm C., Snowden J., Adamson J., Sadovnick A.D., Rollinson S., Cannon A., Dwosh E., Neary D., Melquist S., Richardson A., Dickson D., Berger Z., Eriksen J., Robinson T., Zehr C., Dickey C.A., Crook R., McGowan E., Mann D., Boeve B., Feldman H., Hutton M. Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature 2006, 442:916-919.
2. Beraud-Dufour S., Coppola T., Massa F., Mazella J. Neurotensin receptor-2 and -3 are crucial for the anti-apoptotic effect of neurotensin on pancreatic beta-TC3 cells. Int. J. Biochem. Cell Biol. 2009, 41:2398-2402.
3. Butler G.S., Dean R.A., Tam E.M., Overall C.M. Pharmacoproteomics of a metalloproteinase hydroxamate inhibitor in breast cancer cells: dynamics of membrane type 1 matrix metalloproteinase-mediated membrane protein shedding. Mol. Cell. Biol. 2008, 28:4896-4914.
4. Carrasquillo M.M., Nicholson A.M., Finch N., Gibbs J.R., Baker M., Rutherford N.J., Hunter T.A., DeJesus-Hernandez M., Bisceglio G.D., Mackenzie I.R., Singleton A., Cookson M.R., Crook J.E., Dillman A., Hernandez D., Petersen R.C., Graff-Radford N.R., Younkin S.G., Rademakers R. Genome-wide screen identifies rs646776 near sortilin as a regulator of progranulin levels in human plasma. Am. J. Hum. Genet. 2010, 87:890-897.
5. Chitramuthu B.P., Baranowski D.C., Kay D.G., Bateman A., Bennett H.P. Progranulin modulates zebrafish motoneuron development invivo and rescues truncation defects associated with knockdown of Survival motor neuron 1. Mol. Neurodegener. 2010, 5:41.
6. Coppola G., Karydas A., Rademakers R., Wang Q., Baker M., Hutton M., Miller B.L., Geschwind D.H. Gene expression study on peripheral blood identifies progranulin mutations. Ann. Neurol. 2008, 64:92-96.
7. Cruts M., Gijselinck I., van der Zee J., Engelborghs S., Wils H., Pirici D., Rademakers R., Vandenberghe R., Dermaut B., Martin J.J., van Duijn C., Peeters K., Sciot R., Santens P., De Pooter T., Mattheijssens M., Van den Broeck M., Cuijt I., Vennekens K., De Deyn P.P., Kumar-Singh S., Van Broeckhoven C. Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature 2006, 442:920-924.
8. De Muynck L., Van Damme P. Cellular effects of progranulin in health and disease. J.Mol. Neurosci. 2011, 45:549-560.
9. DeJesus-Hernandez M., Mackenzie I.R., Boeve B.F., Boxer A.L., Baker M., Rutherford N.J., Nicholson A.M., Finch N.A., Flynn H., Adamson J., Kouri N., Wojtas A., Sengdy P., Hsiung G.Y., Karydas A., Seeley W.W., Josephs K.A., Coppola G., Geschwind D.H., Wszolek Z.K., Feldman H., Knopman D.S., Petersen R.C., Miller B.L., Dickson D.W., Boylan K.B., Graff-Radford N.R., Rademakers R. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 2011, 72:245-256.
10. Evans S.F., Irmady K., Ostrow K., Kim T., Nykjaer A., Saftig P., Blobel C., Hempstead B.L. Neuronal brain-derived neurotrophic factor is synthesized in excess, with levels regulated by sortilin-mediated trafficking and lysosomal degradation. J.Biol. Chem. 2011, 286:29556-29567.
11. Finch N., Baker M., Crook R., Swanson K., Kuntz K., Surtees R., Bisceglio G., Rovelet-Lecrux A., Boeve B., Petersen R.C., Dickson D.W., Younkin S.G., Deramecourt V., Crook J., Graff-Radford N.R., Rademakers R. Plasma progranulin levels predict progranulin mutation status in frontotemporal dementia patients and asymptomatic family members. Brain 2009, 132(Pt 3):583-591.
12. Gao X., Joselin A.P., Wang L., Kar A., Ray P., Bateman A., Goate A.M., Wu J.Y. Progranulin promotes neurite outgrowth and neuronal differentiation by regulating GSK-3beta. Protein Cell 2010, 1:552-562.
13. Gass J., Lee W.C., Cook C., Finch N., Stetler C., Jansen-West K., Lewis J., Link C.D., Rademakers R., Nykjaer A., Petrucelli L. Progranulin regulates neuronal outgrowth independent of sortilin. Mol. Neurodegener. 2012, 7:33.
14. Ghidoni R., Benussi L., Glionna M., Franzoni M., Binetti G. Low plasma progranulin levels predict progranulin mutations in frontotemporal lobar degeneration. Neurology 2008, 71:1235-1239.
15. Gijselinck I., Van Langenhove T., van der Zee J., Sleegers K., Philtjens S., Kleinberger G., Janssens J., Bettens K., Van Cauwenberghe C., Pereson S., Engelborghs S., Sieben A., De Jonghe P., Vandenberghe R., Santens P., De Bleecker J., Maes G., Baumer V., Dillen L., Joris G., Cuijt I., Corsmit E., Elinck E., Van Dongen J., Vermeulen S., Van den Broeck M., Vaerenberg C., Mattheijssens M., Peeters K., Robberecht W., Cras P., Martin J.J., De Deyn P.P., Cruts M., Van Broeckhoven C. AC9orf72 promoter repeat expansion in a Flanders-Belgian cohort with disorders of the frontotemporal lobar degeneration-amyotrophic lateral sclerosis spectrum: a gene identification study. Lancet Neurol. 2012, 11:54-65.
16. He Z., Bateman A. Progranulin gene expression regulates epithelial cell growth and promotes tumor growth invivo. Cancer Res. 1999, 59:3222-3229.
17. Hu F., Padukkavidana T., Vaegter C.B., Brady O.A., Zheng Y., Mackenzie I.R., Feldman H.H., Nykjaer A., Strittmatter S.M. Sortilin-mediated endocytosis determines levels of the frontotemporal dementia protein, progranulin. Neuron 2010, 68:654-667.
18. Kessenbrock K., Frohlich L., Sixt M., Lammermann T., Pfister H., Bateman A., Belaaouaj A., Ring J., Ollert M., Fassler R., Jenne D.E. Proteinase 3 and neutrophil elastase enhance inflammation in mice by inactivating antiinflammatory progranulin. J.Clin. Invest. 2008, 118:2438-2447.
19. Kwon S., Christian J.L. Sortilin associates with transforming growth factor-beta family proteins to enhance lysosome-mediated degradation. J.Biol. Chem. 2011, 286:21876-21885.
20. Laird A.S., Van Hoecke A., De Muynck L., Timmers M., Van Den Bosch L., Van Damme P., Robberecht W. Progranulin is neurotrophic invivo and protects against a mutant TDP-43 induced axonopathy. PLoS One 2010, 5:e13368.
21. Lemmens R., Van Hoecke A., Hersmus N., Geelen V., D'Hollander I., Thijs V., Van Den Bosch L., Carmeliet P., Robberecht W. Overexpression of mutant superoxide dismutase 1 causes a motor axonopathy in the zebrafish. Hum. Mol. Genet. 2007, 16:2359-2365.
22. Mazella J., Zsurger N., Navarro V., Chabry J., Kaghad M., Caput D., Ferrara P., Vita N., Gully D., Maffrand J.P., Vincent J.P. The 100-kDa neurotensin receptor is gp95/sortilin, a non-G-protein-coupled receptor. J.Biol. Chem. 1998, 273:26273-26276.
23. McWhorter M.L., Monani U.R., Burghes A.H., Beattie C.E. Knockdown of the survival motor neuron (Smn) protein in zebrafish causes defects in motor axon outgrowth and pathfinding. J.Cell Biol. 2003, 162:919-931.
24. Navarro V., Vincent J.P., Mazella J. Shedding of the luminal domain of the neurotensin receptor-3/sortilin in the HT29 cell line. Biochem. Biophys. Res. Commun. 2002, 298:760-764.
25. Neary D., Snowden J., Mann D. Frontotemporal dementia. Lancet Neurol. 2005, 4:771-780.
26. 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., McCluskey L.F., Miller B.L., Masliah E., Mackenzie I.R., Feldman H., Feiden W., Kretzschmar H.A., Trojanowski J.Q., Lee V.M. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006, 314:130-133.
27. Nyborg A.C., Ladd T.B., Zwizinski C.W., Lah J.J., Golde T.E. Sortilin, SorCS1b, and SorLA Vps10p sorting receptors, are novel gamma-secretase substrates. Mol. Neurodegener. 2006, 1:3.
28. Nykjaer A., Lee R., Teng K.K., Jansen P., Madsen P., Nielsen M.S., Jacobsen C., Kliemannel M., Schwarz E., Willnow T.E., Hempstead B.L., Petersen C.M. Sortilin is essential for proNGF-induced neuronal cell death. Nature 2004, 427:843-848.
29. Quistgaard E.M., Madsen P., Groftehauge M.K., Nissen P., Petersen C.M., Thirup S.S. Ligands bind to Sortilin in the tunnel of a ten-bladed beta-propeller domain. Nat. Struct. Mol. Biol. 2009, 16:96-98.
30. Renton A.E., Majounie E., Waite A., Simon-Sanchez J., Rollinson S., Gibbs J.R., Schymick J.C., Laaksovirta H., van Swieten J.C., Myllykangas L., Kalimo H., Paetau A., Abramzon Y., Remes A.M., Kaganovich A., Scholz S.W., Duckworth J., Ding J., Harmer D.W., Hernandez D.G., Johnson J.O., Mok K., Ryten M., Trabzuni D., Guerreiro R.J., Orrell R.W., Neal J., Murray A., Pearson J., Jansen I.E., Sondervan D., Seelaar H., Blake D., Young K., Halliwell N., Callister J.B., Toulson G., Richardson A., Gerhard A., Snowden J., Mann D., Neary D., Nalls M.A., Peuralinna T., Jansson L., Isoviita V.M., Kaivorinne A.L., Holtta-Vuori M., Ikonen E., Sulkava R., Benatar M., Wuu J., Chio A., Restagno G., Borghero G., Sabatelli M., Heckerman D., Rogaeva E., Zinman L., Rothstein J.D., Sendtner M., Drepper C., Eichler E.E., Alkan C., Abdullaev Z., Pack S.D., Dutra A., Pak E., Hardy J., Singleton A., Williams N.M., Heutink P., Pickering-Brown S., Morris H.R., Tienari P.J., Traynor B.J. Ahexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 2011, 72:257-268.
31. Ryan C.L., Baranowski D.C., Chitramuthu B.P., Malik S., Li Z., Cao M., Minotti S., Durham H.D., Kay D.G., Shaw C.A., Bennett H.P., Bateman A. Progranulin is expressed within motor neurons and promotes neuronal cell survival. BMC Neurosci. 2009, 10:130.
32. Simpson C.L., Lemmens R., Miskiewicz K., Broom W.J., Hansen V.K., van Vught P.W., Landers J.E., Sapp P., Van Den Bosch L., Knight J., Neale B.M., Turner M.R., Veldink J.H., Ophoff R.A., Tripathi V.B., Beleza A., Shah M.N., Proitsi P., Van Hoecke A., Carmeliet P., Horvitz H.R., Leigh P.N., Shaw C.E., van den Berg L.H., Sham P.C., Powell J.F., Verstreken P., Brown R.H., Robberecht W., Al-Chalabi A. Variants of the elongator protein 3 (ELP3) gene are associated with motor neuron degeneration. Hum. Mol. Genet. 2009, 18:472-481.
33. Sleegers K., Brouwers N., Van Damme P., Engelborghs S., Gijselinck I., van der Zee J., Peeters K., Mattheijssens M., Cruts M., Vandenberghe R., De Deyn P.P., Robberecht W., Van Broeckhoven C. Serum biomarker for progranulin-associated frontotemporal lobar degeneration. Ann. Neurol. 2009, 65:603-609.
34. Van Damme P., Bogaert E., Dewil M., Hersmus N., Kiraly D., Scheveneels W., Bockx I., Braeken D., Verpoorten N., Verhoeven K., Timmerman V., Herijgers P., Callewaert G., Carmeliet P., Van Den Bosch L., Robberecht W. Astrocytes regulate GluR2 expression in motor neurons and their vulnerability to excitotoxicity. Proc. Natl. Acad. Sci. U.S.A 2007, 104:14825-14830.
35. 2+-dependent AMPA receptor-mediated motoneuron death. J.Neurosci. 2003, 23:4942-4950.
36. Van Damme P., Van Hoecke A., Lambrechts D., Vanacker P., Bogaert E., van Swieten J., Carmeliet P., Van Den Bosch L., Robberecht W. Progranulin functions as a neurotrophic factor to regulate neurite outgrowth and enhance neuronal survival. J.Cell Biol. 2008, 181:37-41.
37. Van Den Bosch L., Storkebaum E., Vleminckx V., Moons L., Vanopdenbosch L., Scheveneels W., Carmeliet P., Robberecht W. Effects of vascular endothelial growth factor (VEGF) on motor neuron degeneration. Neurobiol. Dis. 2004, 17:21-28.
38. Willnow T.E., Petersen C.M., Nykjaer A. VPS10P-domain receptors - regulators of neuronal viability and function. Nat. Rev. Neurosci. 2008, 9:899-909.
39. Xu J., Xilouri M., Bruban J., Shioi J., Shao Z., Papazoglou I., Vekrellis K., Robakis N.K. Extracellular progranulin protects cortical neurons from toxic insults by activating survival signaling. Neurobiol. Aging 2011, 32:2326.e5-2326.e16.
40. Zheng Y., Brady O.A., Meng P.S., Mao Y., Hu F. C-terminus of progranulin interacts with the beta-propeller region of sortilin to regulate progranulin trafficking. PLoS One 2011, 6:e21023.
41. Zhu J., Nathan C., Jin W., Sim D., Ashcroft G.S., Wahl S.M., Lacomis L., Erdjument-Bromage H., Tempst P., Wright C.D., Ding A. Conversion of proepithelin to epithelins: roles of SLPI and elastase in host defense and wound repair. Cell 2002, 111:867-878.