Cellular ageing, increased mortality and FTLD-TDP-associated neuropathology in progranulin knockout mice

Journal of Pathology

Volumn 228, Issue 1, 2012, Pages 67-76

  Wils, Hans ^a,b   Kleinberger, Gernot ^a,b   Pereson, Sandra ^a,b   Janssens, Jonathan ^a,b   Capell, Anja ^c   Van Dam, Debby ^b   Cuijt, Ivy ^a,b   Joris, Geert ^a,b   De Deyn, Peter P ^b   Haass, Christian ^c,d   Van Broeckhoven, Christine ^a,b   Kumar Singh, Samir ^a,b  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b UNIVERSITY OF ANTWERP   (Belgium)

^c UNIVERSITY OF MUNICH   (Germany)

^d GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

ageing; FTLD; IGF 1; liver pathology; mouse model; progranulin; TDP 43

Indexed keywords

CATHEPSIN D; SOMATOMEDIN C; TAR DNA BINDING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CELL AGING; CONTROLLED STUDY; FEMALE; FRONTOTEMPORAL DEMENTIA; GENE; GLIOSIS; HIPPOCAMPUS; HISTIOCYTE; IN VIVO STUDY; LIVER DISEASE; LIVER SINUSOID; LYSOSOME; MALE; MORTALITY; NEUROPATHOLOGY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROGRANULIN GENE; PROTEIN PHOSPHORYLATION; RAT; SURVIVAL RATE; UBIQUITINATION;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CELL AGING; DNA-BINDING PROTEINS; FEMALE; FRONTOTEMPORAL LOBAR DEGENERATION; GENE EXPRESSION; GLIOSIS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER; LONGEVITY; MALE; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; SURVIVAL RATE; UBIQUITIN;

EID: 84864744790     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4043     Document Type: Article

References (42)

1. Baker M, Mackenzie IR, Pickering-Brown SM, et al., Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature 2006; 442: 916-919.
2. Cruts M, Gijselinck I, van der Zee J, et al., Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature 2006; 442: 920-924.
3. He Z, Bateman A,. Progranulin (granulin-epithelin precursor, PC-cell-derived growth factor, acrogranin) mediates tissue repair and tumorigenesis. J Mol Med 2003; 81: 600-612.
4. Van Damme P, Van Hoecke A, Lambrechts D, et al., Progranulin functions as a neurotrophic factor to regulate neurite outgrowth and enhance neuronal survival. J Cell Biol 2008; 181: 37-41.
5. Kumar-Singh S,. Progranulin and TDP-43: mechanistic links and future directions. J Mol Neurosci 2011; 45: 561-573.
6. Hu F, Padukkavidana T, Vaegter CB, et al., Sortilin-mediated endocytosis determines levels of the frontotemporal dementia protein, progranulin. Neuron 2010; 68: 654-667.
7. Tang W, Lu Y, Tian QY, et al., The growth factor progranulin binds to TNF receptors and is therapeutic against inflammatory arthritis in mice. Science 2011; 332: 478-484.
8. Neumann M, Sampathu DM, Kwong LK, et al., Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006; 314: 130-133.
9. Arai T, Hasegawa M, Akiyama H, et al., TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem Biophys Res Commun 2006; 351: 602-611.
10. Mackenzie IR, Neumann M, Bigio EH, et al., Nomenclature for neuropathologic subtypes of frontotemporal lobar degeneration: consensus recommendations. Acta Neuropathol 2009; 117: 15-18.
11. Hasegawa M, Arai T, Nonaka T, et al., Phosphorylated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Ann Neurol 2008; 64: 60-70.
12. Wils H, Kleinberger G, Janssens J, et al., TDP-43 transgenic mice develop spastic paralysis and neuronal inclusions characteristic of ALS and frontotemporal lobar degeneration. Proc Natl Acad Sci U S A 2010; 107: 3858-3863.
13. Igaz LM, Kwong LK, Xu Y, et al., Enrichment of C-terminal fragments in TAR DNA-binding protein-43 cytoplasmic inclusions in brain but not in spinal cord of frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Am J Pathol 2008; 173: 182-194.
14. Sampathu DM, Neumann M, Kwong LK, et al., Pathological heterogeneity of frontotemporal lobar degeneration with ubiquitin-positive inclusions delineated by ubiquitin immunohistochemistry and novel monoclonal antibodies. Am J Pathol 2006; 169: 1343-1352.
15. Kumar-Singh S, Pirici D, McGowan E, et al., Dense core plaques in Tg2576 and PSAPP mouse models of Alzheimer's disease are centered on vessel walls. Am J Pathol 2005; 167: 527-543.
16. Ahmed Z, Sheng H, Xu YF, et al., Accelerated lipofuscinosis and ubiquitination in granulin knockout mice suggests a role for progranulin in successful aging. Am J Pathol 2010; 177: 311-324.
17. Lehman NL,. The ubiquitin proteasome system in neuropathology. Acta Neuropathol 2009; 118: 329-347.
18. Riga D, Riga S, Halalau F, et al., Brain lipopigment accumulation in normal and pathological aging. Ann N Y Acad Sci 2006; 1067: 158-163.
19. Komatsu M, Waguri S, Koike M, et al., Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007; 131: 1149-1163.
20. Ju JS, Weihl CC,. Inclusion body myopathy, Paget's disease of the bone and fronto-temporal dementia: a disorder of autophagy. Hum Mol Genet 2010; 19: R38-R45.
21. Igaz LM, Kwong LK, Chen-Plotkin A, et al., Expression of TDP-43 C-terminal fragments in vitro recapitulates pathological features of TDP-43 proteinopathies. J Biol Chem 2009; 284: 8516-8524.
22. Rincon M, Rudin E, Barzilai N,. The insulin/IGF-1 signaling in mammals and its relevance to human longevity. Exp Gerontol 2005; 40: 873-877.
23. Xu SQ, Tang D, Chamberlain S, et al., The granulin/epithelin precursor abrogates the requirement for the insulin-like growth factor 1 receptor for growth in vitro. J Biol Chem 1998; 273: 20078-20083.
24. Kayasuga Y, Chiba S, Suzuki M, et al., Alteration of behavioural phenotype in mice by targeted disruption of the progranulin gene. Behav Brain Res 2007; 185: 110-118.
25. Ghoshal N, Dearborn JT, Wozniak DF, et al., Core features of frontotemporal dementia recapitulated in progranulin knockout mice. Neurobiol Dis 2012; 45: 395-408.
26. Yin F, Banerjee R, Thomas B, et al., Exaggerated inflammation, impaired host defense, and neuropathology in progranulin-deficient mice. J Exp Med 2009; 207: 117-128.
27. Petkau TL, Neal SJ, Milnerwood A, et al., Synaptic dysfunction in progranulin-deficient mice. Neurobiol Dis 2012; 45: 711-722.
28. Yin F, Dumont M, Banerjee R, et al., Behavioral deficits and progressive neuropathology in progranulin-deficient mice: a mouse model of frontotemporal dementia. FASEB J 2010; 24: 4639-4647.
29. Doetschman T,. Interpretation of phenotype in genetically engineered mice. Lab Anim Sci 1999; 49: 137-143.
30. Yang JT, Bader BL, Kreidberg JA, et al., Overlapping and independent functions of fibronectin receptor integrins in early mesodermal development. Dev Biol 1999; 215: 264-277.
31. Tominaga K, Matsuda J, Kido M, et al., Genetic background markedly influences vulnerability of the hippocampal neuronal organization in the 'twitcher' mouse model of globoid cell leukodystrophy. J Neurosci Res 2004; 77: 507-516.
32. Pereson S, Wils H, Kleinberger G, et al., Progranulin expression correlates with dense-core amyloid plaque burden in Alzheimer disease mouse models. J Pathol 2009; 219: 173-181.
33. Porta EA,. Pigments in aging: an overview. Ann N Y Acad Sci 2002; 959: 57-65.
34. Rubinsztein DC, Marino G, Kroemer G,. Autophagy and aging. Cell 2011; 146: 682-695.
35. Daniel R, He Z, Carmichael KP, et al., Cellular localization of gene expression for progranulin. J Histochem Cytochem 2000; 48: 999-1009.
36. Li YH, Chen MH, Gong HY, et al., Progranulin A-mediated MET signaling is essential for liver morphogenesis in zebrafish. J Biol Chem 2010; 285: 41001-41009.
37. Guerra RR, Trotta MR, Parra OM, et al., Modulation of extracellular matrix by nutritional hepatotrophic factors in thioacetamide-induced liver cirrhosis in the rat. Braz J Med Biol Res 2009; 42: 1027-1034.
38. Dormann D, Capell A, Carlson AM, et al., Proteolytic processing of TAR DNA binding protein-43 by caspases produces C-terminal fragments with disease defining properties independent of progranulin. J Neurochem 2009; 110: 1082-1094.
39. Kleinberger G, Wils H, Joris G, et al., Increased caspase activation and decreased TDP-43 solubility in progranulin knockout cortical cultures. J Neurochem 2010; 115: 735-747.
40. Spandidos A, Wang X, Wang H, et al., PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res 2010; 38: D792-D799.
41. Pirici D, van der Zee J, Vandenberghe R, et al., Characterization of ubiquitinated intraneuronal inclusions in a novel Belgian frontotemporal lobar degeneration family. J Neuropathol Exp Neurol 2006; 65: 289-301.
42. Paxinos G, Franklin KBJ,. The Mouse Brain in Stereotaxic Coordinates. Academic Press: London, 2001.