Progranulin functions as a cathepsin D chaperone to stimulate axonal outgrowth in vivo

Human Molecular Genetics

Volumn 26, Issue 15, 2017, Pages 2850-2863

  Beel, Sander ^a,b   Moisse, Matthieu ^a,b   Damme, Markus ^c   De Muynck, Louis ^a,b   Robberecht, Wim ^a,d   Van Den Bosch, Ludo ^a,b   Saftig, Paul ^c   Van Damme, Philip ^a,b,d  

^a KU LEUVEN UNIVERSITY OF LEUVEN   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c UNIVERSITY OF KIEL   (Germany)

^d UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN D; CD11B ANTIGEN; CHAPERONE; CHEMOKINE; GASTRIN RELEASING PEPTIDE; GRANULIN; HEMOGLOBIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; METAL ION; PENTOBARBITAL; PROGRANULIN; TRANSCRIPTOME; GRANULIN PRECURSOR PROTEIN; GRN PROTEIN, HUMAN; GRN PROTEIN, MOUSE; SIGNAL PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; AREA UNDER THE CURVE; ARTICLE; BICINCHONINIC ACID ASSAY; CARBOXY TERMINAL SEQUENCE; CELL VACUOLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYONIC STEM CELL; ENZYME ACTIVITY; FACIAL NERVE INJURY; FACIAL NERVE NUCLEUS; FALSE DISCOVERY RATE; FRONTOTEMPORAL DEMENTIA; GENE EXPRESSION; GENE MUTATION; GENE ONTOLOGY; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HAPLOINSUFFICIENCY; HISTOLOGY; HOMEOSTASIS; IMMUNE SYSTEM; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LEUKOCYTE ACTIVATION; LOSS OF FUNCTION MUTATION; LYMPHOCYTE ACTIVATION; LYSOSOME; MOUSE; NERVE CELL; NERVE FIBER REGENERATION; NERVE REGENERATION; NEURITE OUTGROWTH; NONHUMAN; PROTEIN DEGRADATION; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA SEQUENCING; SURGICAL TECHNIQUE; T LYMPHOCYTE ACTIVATION; UPREGULATION; WESTERN BLOTTING; ANIMAL; FACIAL NERVE; GENETICS; HUMAN; METABOLISM; MUTATION; TRANSGENIC MOUSE;

ANIMALS; CATHEPSIN D; FACIAL NERVE; FRONTOTEMPORAL DEMENTIA; HAPLOINSUFFICIENCY; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, TRANSGENIC; MOLECULAR CHAPERONES; MUTATION;

EID: 85025695352     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddx162     Document Type: Article

References (55)

1. Bateman, A. and Bennett, H.P. (1998) Granulins: the structure and function of an emerging family of growth factors. J. Endocrinol., 158, 145–151.
2. 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, 867–878.
3. De Muynck, L. and Van Damme, P. (2011) Cellular effects of progranulin in health and disease. J. Mol. Neurosci., 45, 549–560.
4. Zheng, Y., Brady, O.A., Meng, P.S., Mao, Y. and Hu, F. (2011) C-terminus of progranulin interacts with the beta-propeller region of sortilin to regulate progranulin trafficking. PLoS One, 6, e21023.
5. Petkau, T.L. and Leavitt, B.R. (2014) Progranulin in neurodegenerative disease. Trends Neurosci., 37, 388–398.
6. Petkau, T.L., Neal, S.J., Orban, P.C., MacDonald, J.L., Hill, A.M., Lu, G., Feldman, H.H., Mackenzie, I.R. and Leavitt, B.R. (2010) Progranulin expression in the developing and adult murine brain. J. Comp. Neurol., 518, 3931–3947.
7. 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, 37–41.
8. Martens, L.H., Zhang, J., Barmada, S.J., Zhou, P., Kamiya, S., Sun, B., Min, S.W., Gan, L., Finkbeiner, S., Huang, E.J. et al. (2012) Progranulin deficiency promotes neuroinflammation and neuron loss following toxin-induced injury. J. Clin. Invest., 122, 3955–3959.
9. 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, 916–919.
10. 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 ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature., 442, 920–924.
11. Finch, N., Baker, M., Crook, R., Swanson, K., Kuntz, K., Surtees, R., Bisceglio, G., Rovelet-Lecrux, A., Boeve, B., Petersen, R.C. et al. (2009) Plasma progranulin levels predict progranulin mutation status in frontotemporal dementia patients and asymptomatic family members. Brain, 132, 583–591.
12. Ghidoni, R., Benussi, L., Glionna, M., Franzoni, M. and Binetti, G. (2008) Low plasma progranulin levels predict progranulin mutations in frontotemporal lobar degeneration. Neurology, 71, 1235–1239.
13. Sleegers, K., Brouwers, N., Van Damme, P., Engelborghs, S., Gijselinck, I., van der Zee, J., Peeters, K., Mattheijssens, M., Cruts, M., Vandenberghe, R. et al. (2009) Serum biomarker for progranulin-associated frontotemporal lobar degeneration. Ann. Neurol., 65, 603–609.
14. Almeida, M.R., Macario, M.C., Ramos, L., Baldeiras, I., Ribeiro, M.H. and Santana, I. (2016) Portuguese family with the co-occurrence of frontotemporal lobar degeneration and neuronal ceroid lipofuscinosis phenotypes due to progranulin gene mutation. Neurobiol. Aging, 41, 200 e201–205.
15. Smith, K.R., Damiano, J., Franceschetti, S., Carpenter, S., Canafoglia, L., Morbin, M., Rossi, G., Pareyson, D., Mole, S.E., Staropoli, J.F. et al. (2012) Strikingly different clinicopathological phenotypes determined by progranulin-mutation dosage. Am. J. Hum. Genet., 90, 1102–1107.
16. Gotzl, J.K., Mori, K., Damme, M., Fellerer, K., Tahirovic, S., Kleinberger, G., Janssens, J., van der Zee, J., Lang, C.M., Kremmer, E. et al. (2014) Common pathobiochemical hallmarks of progranulin-associated frontotemporal lobar degeneration and neuronal ceroid lipofuscinosis. Acta Neuropathol., 127, 845–860.
17. Yin, F., Dumont, M., Banerjee, R., Ma, Y., Li, H., Lin, M.T., Beal, M.F., Nathan, C., Thomas, B. and Ding, A. (2010) Behavioral deficits and progressive neuropathology in progranulin-deficient mice: a mouse model of frontotemporal dementia. faseb J., 24, 4639–4647.
18. Philips, T., De Muynck, L., Thu, H.N., Weynants, B., Vanacker, P., Dhondt, J., Sleegers, K., Schelhaas, H.J., Verbeek, M., Vandenberghe, R. et al. (2010) Microglial upregulation of progranulin as a marker of motor neuron degeneration. J. Neuropathol. Exp. Neurol., 69, 1191–1200.
19. Lui, H., Zhang, J., Makinson, S.R., Cahill, M.K., Kelley, K.W., Huang, H.Y., Shang, Y., Oldham, M.C., Martens, L.H., Gao, F. et al. (2016) Progranulin deficiency promotes circuit-specific synaptic pruning by microglia via complement activation. Cell, 165, 921–935.
20. Tanaka, Y., Chambers, J.K., Matsuwaki, T., Yamanouchi, K. and Nishihara, M. (2014) Possible involvement of lysosomal dysfunction in pathological changes of the brain in aged progranulin-deficient mice. Acta Neuropathol. Commun., 2, 78.
21. Raitano, S., Ordovas, L., De Muynck, L., Guo, W., Espuny-Camacho, I., Geraerts, M., Khurana, S., Vanuytsel, K., Toth, B.I., Voets, T. et al. (2015) Restoration of progranulin expression rescues cortical neuron generation in an induced pluripotent stem cell model of frontotemporal dementia. Stem Cell Rep., 4, 16–24.
22. Almeida, S., Zhang, Z., Coppola, G., Mao, W., Futai, K., Karydas, A., Geschwind, M.D., Tartaglia, M.C., Gao, F., Gianni, D. et al. (2012) Induced pluripotent stem cell models of progranulin-deficient frontotemporal dementia uncover specific reversible neuronal defects. Cell Rep., 2, 789–798.
23. Minami, S.S., Min, S.W., Krabbe, G., Wang, C., Zhou, Y., Asgarov, R., Li, Y., Martens, L.H., Elia, L.P., Ward, M.E. et al. (2014) Progranulin protects against amyloid beta deposition and toxicity in Alzheimer’s disease mouse models. Nat. Med., 20, 1157–1164.
24. Laird, A.S., Van Hoecke, A., De Muynck, L., Timmers, M., Van den Bosch, L., Van Damme, P. and Robberecht, W. (2010) Progranulin is neurotrophic in vivo and protects against a mutant TDP-43 induced axonopathy. PLoS One, 5, e13368.
25. Chitramuthu, B.P., Baranowski, D.C., Kay, D.G., Bateman, A. and Bennett, H.P. (2010) Progranulin modulates zebrafish motoneuron development in vivo and rescues truncation defects associated with knockdown of Survival motor neuron 1. Mol. Neurodegener., 5, 41.
26. Jackman, K., Kahles, T., Lane, D., Garcia-Bonilla, L., Abe, T., Capone, C., Hochrainer, K., Voss, H., Zhou, P., Ding, A. et al. (2013) Progranulin deficiency promotes post-ischemic blood-brain barrier disruption. J. Neurosci., 33, 19579–19589.
27. Kanazawa, M., Kawamura, K., Takahashi, T., Miura, M., Tanaka, Y., Koyama, M., Toriyabe, M., Igarashi, H., Nakada, T., Nishihara, M. et al. (2015) Multiple therapeutic effects of progranulin on experimental acute ischaemic stroke. Brain, 138, 1932–1948.
28. Gao, X., Joselin, A.P., Wang, L., Kar, A., Ray, P., Bateman, A., Goate, A.M. and Wu, J.Y. (2010) Progranulin promotes neurite outgrowth and neuronal differentiation by regulating GSK-3beta. Protein Cell, 1, 552–562.
29. 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. et al. (2009) Progranulin is expressed within motor neurons and promotes neuronal cell survival. BMC Neurosci., 10, 130.
30. Xu, J., Xilouri, M., Bruban, J., Shioi, J., Shao, Z., Papazoglou, I., Vekrellis, K. and Robakis, N.K. (2011) Extracellular progranulin protects cortical neurons from toxic insults by activating survival signaling. Neurobiol. Aging, 32, 2326 e2325–2316.
31. De Muynck, L., Herdewyn, S., Beel, S., Scheveneels, W., Van Den Bosch, L., Robberecht, W. and Van Damme, P. (2013) The neurotrophic properties of progranulin depend on the granulin E domain but do not require sortilin binding. Neurobiol. Aging, 34, 2541–2547.
32. Gass, J., Lee, W.C., Cook, C., Finch, N., Stetler, C., Jansen-West, K., Lewis, J., Link, C.D., Rademakers, R., Nykjaer, A. et al. (2012) Progranulin regulates neuronal outgrowth independent of sortilin. Mol. Neurodegener., 7, 33.
33. Ferri, C.C., Moore, F.A. and Bisby, M.A. (1998) Effects of facial nerve injury on mouse motoneurons lacking the p75 low-affinity neurotrophin receptor. J. Neurobiol., 34, 1–9.
34. McGraw, J., McPhail, L.T., Oschipok, L.W., Horie, H., Poirier, F., Steeves, J.D., Ramer, M.S. and Tetzlaff, W. (2004) Galectin-1 in regenerating motoneurons. Eur. J. Neurosci., 20, 2872–2880.
35. Herdewyn, S., De Muynck, L., Van Den Bosch, L., Robberecht, W. and Van Damme, P. (2013) Progranulin does not affect motor neuron degeneration in mutant SOD1 mice and rats. Neurobiol. Aging, 34, 2302–2303.
36. Markmann, S., Krambeck, S., Hughes, C.J., Mirzaian, M., Aerts, J.M., Saftig, P., Schweizer, M., Vissers, J.P., Braulke, T. and Damme, M. (2017) Quantitative Proteome Analysis of Mouse Liver Lysosomes Provides Evidence for Mannose 6-phosphate-independent Targeting Mechanisms of Acid Hydrolases in Mucolipidosis II. Mol. Cell Proteomics, 16, 438–450.
37. Karwowska, A., Roszkowska-Jakimiec, W., Dabrowska, E., Gacko, M. and Chlabicz, M. (2006) The effect of temperature, acidification, and alkalization changes as well as ethanol on salivary cathepsin D activity. Adv. Med. Sci., 51 Suppl 1, 59–61.
38. Hayes, M.G., Hurley, M.J., Larsen, L.B., Heegaard, C.W., Magboul, A.A., Oliveira, J.C., McSweeney, P.L. and Kelly, A.L. (2001) Thermal inactivation kinetics of bovine cathepsin D. J. Dairy Res., 68, 267–276.
39. Zhou, X., Sun, L., Bastos de Oliveira, F., Qi, X., Brown, W.J., Smolka, M.B., Sun, Y. and Hu, F. (2015) Prosaposin facilitates sortilin-independent lysosomal trafficking of progranulin. J. Cell Biol., 210, 991–1002.
40. Tang, W., Lu, Y., Tian, Q.Y., Zhang, Y., Guo, F.J., Liu, G.Y., Syed, N.M., Lai, Y., Lin, E.A., Kong, L. et al. (2011) The growth factor progranulin binds to TNF receptors and is therapeutic against inflammatory arthritis in mice. Science, 332, 478–484.
41. Chen, X., Chang, J., Deng, Q., Xu, J., Nguyen, T.A., Martens, L.H., Cenik, B., Taylor, G., Hudson, K.F., Chung, J. et al. (2013) Progranulin does not bind tumor necrosis factor (TNF) receptors and is not a direct regulator of TNF-dependent signaling or bioactivity in immune or neuronal cells. J. Neurosci., 33, 9202–9213.
42. Altmann, C., Vasic, V., Hardt, S., Heidler, J., Haussler, A., Wittig, I., Schmidt, M.H. and Tegeder, I. (2016) Progranulin promotes peripheral nerve regeneration and reinnervation: role of notch signaling. Mol. Neurodegener., 11, 69.
43. Neill, T., Buraschi, S., Goyal, A., Sharpe, C., Natkanski, E., Schaefer, L., Morrione, A. and Iozzo, R.V. (2016) EphA2 is a functional receptor for the growth factor progranulin. J. Cell Biol., 215, 687–703.
44. Tanaka, Y., Matsuwaki, T., Yamanouchi, K. and Nishihara, M. (2013) Increased lysosomal biogenesis in activated microglia and exacerbated neuronal damage after traumatic brain injury in progranulin-deficient mice. Neuroscience, 250, 8–19.
45. Sardiello, M., Palmieri, M., di Ronza, A., Medina, D.L., Valenza, M., Gennarino, V.A., Di Malta, C., Donaudy, F., Embrione, V., Polishchuk, R.S. et al. (2009) A gene network regulating lysosomal biogenesis and function. Science, 325, 473–477.
46. Siintola, E., Partanen, S., Stromme, P., Haapanen, A., Haltia, M., Maehlen, J., Lehesjoki, A.E. and Tyynela, J. (2006) Cathepsin D deficiency underlies congenital human neuronal ceroid-lipofuscinosis. Brain, 129, 1438–1445.
47. Rossi, D.J., Londesborough, A., Korsisaari, N., Pihlak, A., Lehtonen, E., Henkemeyer, M. and Makela, T.P. (2001) Inability to enter S phase and defective RNA polymerase II CTD phosphorylation in mice lacking Mat1. embo J., 20, 2844–2856.
48. George, S.H., Gertsenstein, M., Vintersten, K., Korets-Smith, E., Murphy, J., Stevens, M.E., Haigh, J.J. and Nagy, A. (2007) Developmental and adult phenotyping directly from mutant embryonic stem cells. Proc. Natl Acad. Sci. U S A, 104, 4455–4460.
49. Buchholz, F., Angrand, P.O. and Stewart, A.F. (1998) Improved properties of FLP recombinase evolved by cycling mutagenesis. Nat. Biotechnol., 16, 657–662.
50. Lallemand, Y., Luria, V., Haffner-Krausz, R. and Lonai, P. (1998) Maternally expressed PGK-Cre transgene as a tool for early and uniform activation of the Cre site-specific recombinase. Transgenic Res., 7, 105–112.
51. Saftig, P., Hetman, M., Schmahl, W., Weber, K., Heine, L., Mossmann, H., Koster, A., Hess, B., Evers, M., von Figura, K. et al. (1995) Mice deficient for the lysosomal proteinase cathepsin D exhibit progressive atrophy of the intestinal mucosa and profound destruction of lymphoid cells. embo J., 14, 3599–3608.
52. Mesnard, N.A., Sanders, V.M. and Jones, K.J. (2011) Differential gene expression in the axotomized facial motor nucleus of presymptomatic SOD1 mice. J. Comp. Neurol., 519, 3488–3506.
53. Claussen, M., Kubler, B., Wendland, M., Neifer, K., Schmidt, B., Zapf, J. and Braulke, T. (1997) Proteolysis of insulin-like growth factors (IGF) and IGF binding proteins by cathepsin D. Endocrinology, 138, 3797–3803.
54. Zeeberg, B.R., Qin, H., Narasimhan, S., Sunshine, M., Cao, H., Kane, D.W., Reimers, M., Stephens, R.M., Bryant, D., Burt, S.K. et al. (2005) High-Throughput GoMiner, an ‘industrial-strength’ integrative gene ontology tool for interpretation of multiple-microarray experiments, with application to studies of Common Variable Immune Deficiency (CVID). BMC Bioinformatics, 6, 168.
55. Kuzis, K., Coffin, J.D. and Eckenstein, F.P. (1999) Time course and age dependence of motor neuron death following facial nerve crush injury: role of fibroblast growth factor. Exp. Neurol., 157, 77–87.