Early neuropsychological characteristics of progranulin mutation carriers

Journal of the International Neuropsychological Society

Volumn 20, Issue 7, 2014, Pages 694-703

  Hallam, Bradley J ^a   Jacova, Claudia ^a   Hsiung, Ging Yuek R ^a   Wittenberg, Dana ^a   Sengdy, Pheth ^a   Bouchard Kerr, Phoenix ^a   Slack, Penny ^a   Rademakers, Rosa ^b   Baker, Matthew ^b   Chow, Tiffany W ^c   Levine, Brian ^d   Feldman, Howard H ^a   Mackenzie, Ian R ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b MAYO GRADUATE SCHOOL   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d BAYCREST CENTRE FOR GERIATRIC CARE   (Canada)

Author keywords

Cognitive symptom; FTLD with TDP 43 Pathology; Granulin; Hereditary neurodegenerative disease; Neuropsychology; Ubiquitin positive frontotemporal dementia

Indexed keywords

GRN PROTEIN, HUMAN; SIGNAL PEPTIDE;

ADULT; AGED; ATTENTION; COGNITION DISORDERS; COMPLICATION; FEMALE; FRONTOTEMPORAL DEMENTIA; GENETICS; HUMAN; LANGUAGE; LEARNING; MALE; MEMORY; MIDDLE AGED; MUTATION; NEUROPSYCHOLOGICAL TEST; NONPARAMETRIC TEST; NUCLEOTIDE SEQUENCE; RECEIVER OPERATING CHARACTERISTIC;

ADULT; AGED; ATTENTION; COGNITION DISORDERS; DNA MUTATIONAL ANALYSIS; FEMALE; FRONTOTEMPORAL DEMENTIA; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LANGUAGE; MALE; MEMORY; MIDDLE AGED; MUTATION; NEUROPSYCHOLOGICAL TESTS; ROC CURVE; STATISTICS, NONPARAMETRIC; VERBAL LEARNING;

EID: 84919587433     PISSN: 13556177     EISSN: 14697661     Source Type: Journal    
DOI: 10.1017/S1355617714000551     Document Type: Article

References (55)

1. Arai, T., Hasegawa, M., Akiyama, H., Ikeda, K., Nonaka, T., Mori, H.,⋯Oda, T. (2006). TDP-43 is a component of ubiquitinpositive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochemical and Biophysical Research Communications, 351(3), 602-611. doi:10.1016/j.bbrc.2006.10.093
2. Baker, M., Mackenzie, I.R., Pickering-Brown, S.M., Gass, J., Rademakers, R., Lindholm, C., ⋯ Hutton, M. (2006). Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature, 442(7105), 916-919. doi:10.1038/ nature05016
3. Barandiaran, M., Estanga, A., Moreno, F., Indakoetxea, B., Alzualde, A., Balluerka, N., ⋯ de Munain, A.L. (2012). Neuropsychological features of asymptomatic c.709-1G - A progranulin mutation carriers. Journal of the International Neuropsychological Society, 18(6), 1086-1090. doi:10.1017/ S1355617712000823; 10.1017/S1355617712000823
4. Beck, J., Rohrer, J.D., Campbell, T., Isaacs, A., Morrison, K.E., Goodall, E.F., ⋯ Mead, S. (2008). A distinct clinical, neuropsychological and radiological phenotype is associated with progranulin gene mutations in a large UK series. Brain, 131(Pt 3), 706-720. doi:10.1093/brain/awm320
5. Behrens, M.I., Mukherjee, O., Tu, P.H., Liscic, R.M., Grinberg, L.T., Carter, D.,⋯Cairns, N.J. (2007). Neuropathologic heterogeneity in HDDD1: A familial frontotemporal lobar degeneration with ubiquitin-positive inclusions and progranulin mutation. Alzheimer Disease and Associated Disorders, 21(1), 1-7. doi:10.1097/WAD.0b013e31803083f2
6. Benussi, L., Ghidoni, R., Pegoiani, E., Moretti, D.V., Zanetti, O., & Binetti, G. (2009). Progranulin Leu271LeufsX10 is one of the most common FTLD and CBS associated mutations worldwide. Neurobiology of Disease, 33(3), 379-385. doi:10.1016/j. nbd.2008.11.008
7. Borroni, B., Alberici, A., Cercignani, M., Premi, E., Serra, L., Cerini, C.,⋯Bozzali, M. (2012). Granulin mutation drives brain damage and reorganization from preclinical to symptomatic FTLD. Neurobiology of Aging, 33(10), 2506-2520. doi:10.1016/j. neurobiolaging.2011.10.031; 10.1016/j.neurobiolaging.2011.10.031
8. Borroni, B., Alberici, A., Premi, E., Archetti, S., Garibotto, V., Agosti, C., ⋯ Padovani, A. (2008). Brain magnetic resonance imaging structural changes in a pedigree of asymptomatic progranulin mutation carriers. Rejuvenation Research, 11(3), 585-595.
9. Brooks, B.L., Holdnack, J.A., & Iverson, G.L. (2011). Advanced clinical interpretation of the WAIS-IV and WMS-IV: Prevalence of low scores varies by level of intelligence and years of education. Assessment 18(2), 156-167. doi:10.1177/ 1073191110385316; 10.1177/1073191110385316
10. Brooks, B.L., Iverson, G.L., & White, T. (2007). Substantial risk of "accidental MCI" in healthy older adults: Base rates of low memory scores in neuropsychological assessment. Journal of the International Neuropsychological Society, 13(3), 490-500. doi:10.1017/S1355617707070531
11. Brooks, B.L., Iverson, G.L., & White, T. (2009). Advanced interpretation of the neuropsychological assessment battery with older adults: Base rate analyses, discrepancy scores, and interpreting change. Archives of Clinical Neuropsychology, 24(7), 647-657. doi:10.1093/arclin/acp061; 10.1093/arclin/acp061
12. Bruni, A.C., Momeni, P., Bernardi, L., Tomaino, C., Frangipane, F., Elder, J., ⋯ Rogaeva, E. (2007). Heterogeneity within a large kindred with frontotemporal dementia: A novel progranulin mutation. Neurology, 69(2), 140-147. doi:10.1212/01. wnl.0000265220.64396.b4
13. Chen-Plotkin, A.S., Martinez-Lage, M., Sleiman, P.M., Hu, W., Greene, R., Wood, E.M., ⋯ Van Deerlin, V.M. (2011). Genetic and clinical features of progranulin-associated frontotemporal lobar degeneration. Archives of Neurology, 68(4), 488-497. doi:10.1001/archneurol.2011.53; 10.1001/archneurol.2011.53
14. Chow, T.W., Miller, B.L., Hayashi, V.N., & Geschwind, D.H. (1999). Inheritance of frontotemporal dementia. Archives of Neurology, 56(7), 817-822.
15. Cruts, M., Gijselinck, I., van der Zee, J., Engelborghs, S., Wils, H., Pirici, D., ⋯ Van Broeckhoven, C. (2006). Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature, 442(7105), 920-924. doi:10.1038/nature05017
16. Delis, D., Kramer, J., Kaplan, E., & Ober, B. (2000). California verbal learning test - Adult short form version. (2nd ed.). San Antonio, TX: The Psychological Corporation.
17. Folstein, M.F., Folstein, S.E., McHugh, P.R., & Fanjiang, G. (2001). Mini-mental state examination: User's guide. Odessa, FL: Psychological Assessment Resources, Inc.
18. Gass, J., Cannon, A., Mackenzie, I.R., Boeve, B., Baker, M., Adamson, J., ⋯ Rademakers, R. (2006). Mutations in progranulin are a major cause of ubiquitin-positive frontotemporal lobar degeneration. Human Molecular Genetics, 15(20), 2988-3001. doi:10.1093/hmg/ddl241
19. Gijselinck, I., Van Broeckhoven, C., & Cruts, M. (2008). Granulin mutations associated with frontotemporal lobar degeneration and related disorders: An update. HumanMutation, 29(12), 1373-1386. doi:10.1002/humu.20785; 10.1002/humu.20785
20. Gorno-Tempini, M.L., Hillis, A.E., Weintraub, S., Kertesz, A., Mendez, M., Cappa, S.F.,⋯Grossman, M. (2011). Classification of primary progressive aphasia and its variants. Neurology, 76(11), 1006-1014.
21. Heaton, R.K., Chelune, G.J., Talley, J.L., Kay, G.G., & Curtiss, G. (1993). Wisconsin card sorting test manual, revised and expanded. Odessa, FL: Psychological Assessment Resources, Inc.
22. Hsiung, G.Y.R., & Feldman, H.H. (1993). GRN-related frontotemporal dementia. In R.A. Pagon, M.P. Adam, T.D. Bird, C.R. Dolan, C.T. Fong, & K. Stephens (Eds.), Genereviews. Seattle, WA: University of Washington.
23. Jacova, C., Hsiung, G.Y., Tawankanjanachot, I., Dinelle, K., McCormick, S., Gonzalez, M., ⋯ Mackenzie, I.R. (2013). Anterior brain glucose hypometabolism predates dementia in progranulin mutation carriers. Neurology, 81(15), 1322-1331. doi:10.1212/WNL.0b013e3182a8237e; 10.1212/ WNL.0b013e3182a8237e
24. Josephs, K.A., Ahmed, Z., Katsuse, O., Parisi, J.F., Boeve, B.F., Knopman, D.S., ⋯ Dickson, D.W. (2007). Neuropathologic features of frontotemporal lobar degeneration with ubiquitinpositive inclusions with progranulin gene (PGRN) mutations. Journal of Neuropathology and Experimental Neurology, 66(2), 142-151. doi:10.1097/nen.0b013e31803020cf
25. Kelley, B.J., Haidar, W., Boeve, B.F., Baker, M., Shiung, M., Knopman, D.S., & Petersen, R.C. (2010). Alzheimer disease-like phenotype associated with the c.154delA mutation in progranulin. Archives of Neurology, 67(2), 171-177. doi:10.1001/archneurol.2010.113; 10.1001/archneurol.2010.113.
26. Kramer, J.H., Jurik, J., Sha, S.J., Rankin, K.P., Rosen, H.J., Johnson, J.K., & Miller, B.L. (2003). Distinctive neuropsychological patterns in frontotemporal dementia, semantic dementia, and alzheimer disease. Cognitive and Behavioral Neurology, 16(4), 211-218.
27. Le Ber, I., Camuzat, A., Hannequin, D., Pasquier, F., Guedj, E., Rovelet-Lecrux, A., ⋯ French research network on FTD/FTDMND. (2008). Phenotype variability in progranulin mutation carriers: A clinical, neuropsychological, imaging and genetic study. Brain, 131(Pt 3), 732-746. doi:10.1093/brain/awn012
28. Lezak, M.D., Howieson, D.B., & Loring, D.W. (2004). Neuropsychological assessment (4th ed.).New York, NY: Oxford University Press.
29. Lopez de Munain, A., Alzualde, A., Gorostidi, A., Otaegui, D., Ruiz-Martinez, J., Indakoetxea, B., ⋯ Marti Masso, J.F. (2008). Mutations in progranulin gene: Clinical, pathological, and ribonucleic acid expression findings. Biological Psychiatry, 63(10), 946-952. doi:10.1016/j.biopsych.2007.08.015
30. Mackenzie, I.R., Baker, M., Pickering-Brown, S., Hsiung, G.Y., Lindholm, C., Dwosh, E., ⋯ Feldman, H.H. (2006). The neuropathology of frontotemporal lobar degeneration caused by mutations in the progranulin gene. Brain, 129(Pt 11), 3081-3090. doi:10.1093/brain/awl271
31. Mackenzie, I.R.,Neumann,M., Bigio, E.H., Cairns, N.J., Alafuzoff, I., Kril, J., ⋯ Mann, D.M. (2009). Nomenclature for neuropathologic subtypes of frontotemporal lobar degeneration: Consensus recommendations. Acta Neuropathologica, 117(1), 15-18. doi:10.1007/s00401-008-0460-5
32. Masellis, M., Momeni, P., Meschino, W., Heffner, R., Jr, Elder, J., Sato, C., ⋯ Rogaeva, E. (2006). Novel splicing mutation in the progranulin gene causing familial corticobasal syndrome. Brain, 129(Pt 11), 3115-3123. doi:10.1093/brain/awl276
33. McKhann, G.M., Albert, M.S., Grossman, M.,Miller, B., Dickson, D., Trojanowski, J.Q., ⋯ Work Group on Frontotemporal Dementia and Pick's Disease (2001). Clinical and pathological diagnosis of frontotemporal dementia: Report of the work group on frontotemporal dementia and pick's disease. Archives of Neurology, 58(11), 1803-1809.
34. Mesulam, M., Johnson, N., Krefft, T.A., Gass, J.M., Cannon, A.D., Adamson, J.L.,⋯Graff-Radford, N.R. (2007). Progranulin mutations in primary progressive aphasia: The PPA1 and PPA3 families. Archives of Neurology, 64(1), 43-47. doi:10.1001/archneur.64.1.43
35. Mitrushina, M., Boone, K.B., Razani, J., & D'Elia, L.F. (2005). Handbook of normative data for neuropsychological assessment (2nd ed.). New York, NY: Oxford University Press.
36. Moreno, F., Indakoetxea, B., Barandiaran, M., Alzualde, A., Gabilondo, A., Estanga, A., ⋯ Lopez de Munain, A. (2009). "Frontotemporoparietal" dementia: Clinical phenotype associated with the c.709-1GA PGRN mutation. Neurology, 73(17), 1367-1374. doi:10.1212/WNL.0b013e3181bd82a7; 10.1212/ WNL.0b013e3181bd82a7
37. Mukherjee, O., Pastor, P., Cairns, N.J., Chakraverty, S., Kauwe, J.S., Shears, S., ⋯ Goate, A.M. (2006). HDDD2 is a familial frontotemporal lobar degeneration with ubiquitin-positive, taunegative inclusions caused by a missense mutation in the signal peptide of progranulin. Annals of Neurology, 60(3), 314-322. doi:10.1002/ana.20963
38. Neary, D., Snowden, J.S., Gustafson, L., Passant, U., Stuss, D., Black, S., ⋯ Benson, D.F. (1998). Frontotemporal lobar degeneration: A consensus on clinical diagnostic criteria. Neurology, 51(6), 1546-1554.
39. Neumann, M., Sampathu, D.M., Kwong, L.K., Truax, A.C., Micsenyi, M.C., Chou, T.T.,⋯ Lee, V.M. (2006). Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science, 314(5796), 130-133. doi:10.1126/ science.1134108
40. Petersen, R.C. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256(3), 183-194. doi:10.1111/j.1365-2796.2004.01388.x
41. Premi, E., Grassi, M., Gazzina, S., Paghera, B., Pepe, D., Archetti, S., ⋯ Borroni, B. (2013). The neuroimaging signature of frontotemporal lobar degeneration associated with granulin mutations: An effective connectivity study. Journal of Nuclear Medicine, 54(7), 1066-1071. doi:10.2967/jnumed.112.111773; 10.2967/jnumed.112.111773
42. Rabinovici, G.D., & Miller, B.L. (2010). Frontotemporal lobar degeneration: Epidemiology, pathophysiology, diagnosis and management. CNS Drugs, 24(5), 375-398. doi:10.2165/ 11533100-000000000-00000; 10.2165/11533100-000000000-00000
43. Rademakers, R., Baker, M., Gass, J., Adamson, J., Huey, E.D., Momeni, P., ⋯ Hutton, M. (2007). Phenotypic variability associated with progranulin haploinsufficiency in patients with the common 1477C->T (Arg493X) mutation: An international initiative. Lancet Neurology, 6(10), 857-868. doi:10.1016/ S1474-4422(07)70221-1
44. Rascovsky, K., Hodges, J.R., Knopman, D., Mendez, M.F., Kramer, J.H., Neuhaus, J., ⋯ Miller, B.L. (2011). Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain, 134(Pt 9), 2456-2477. doi:10.1093/brain/awr179
45. Rohrer, J.D., Ridgway, G.R., Modat, M., Ourselin, S., Mead, S., Fox, N.C., ⋯ Warren, J.D. (2010). Distinct profiles of brain atrophy in frontotemporal lobar degeneration caused by progranulin and tau mutations. Neuroimage, 53(3), 1070-1076. doi:10.1016/j. neuroimage.2009.12.088
46. Rohrer, J.D.,Warren, J.D., Barnes, J.,Mead, S., Beck, J., Pepple, T.,⋯ Fox, N.C. (2008). Mapping the progression of progranulinassociated frontotemporal lobar degeneration. Nature Clinical Practice. Neurology, 4(8), 455-460. doi:10.1038/ncpneuro0869
47. Rohrer, J.D., Warren, J.D., Omar, R.,Mead, S., Beck, J., Revesz, T.,⋯ Rossor, M.N. (2008). Parietal lobe deficits in frontotemporal lobar degeneration caused by a mutation in the progranulin gene. Archives of Neurology, 65(4), 506-513. doi:10.1001/ archneur.65.4.506
48. Ruff, R.M., Light, R.H., Parker, S.B.,⋯Levin, H.S. (1996). Benton controlled oral word association test: Reliability and updated norms. Archives of Clinical Neuropsychology, 11(4), 329-338.
49. Spina, S., Murrell, J.R., Huey, E.D., Wassermann, E.M., Pietrini, P., Baraibar, M.A., ⋯ Grafman, J. (2007). Clinicopathologic features of frontotemporal dementia with progranulin sequence variation. Neurology, 68(11), 820-827. doi:10.1212/01. wnl.0000254460.31273.2d
50. Stevens, M., van Duijn, C.M., Kamphorst, W., de Knijff, P., Heutink, P., van Gool, W.A., ⋯ van Swieten, J.C. (1998). Familial aggregation in frontotemporal dementia. Neurology, 50(6), 1541-1545.
51. van Swieten, J.C., & Heutink, P. (2008). Mutations in progranulin (GRN) within the spectrum of clinical and pathological phenotypes of frontotemporal dementia. Lancet Neurology, 7(10), 965-974. doi:10.1016/S1474-4422(08)70194-7; 10.1016/ S1474-4422(08)70194-7
52. Wechsler, D. (1997a). Wechsler adult intelligence scale (3rd ed.). San Antonio, TX: The Psychological Corporation.
53. Wechsler, D. (1997b). Wechsler memory scale (3rd ed.). San Antonio, TX: The Psychology Corporation.
54. Whitwell, J.L., Xu, J., Mandrekar, J., Boeve, B.F., Knopman, D.S., Parisi, J.E., ⋯ Josephs, K.A. (2013). Frontal asymmetry in behavioral variant frontotemporal dementia: Clinicoimaging and pathogenetic correlates. Neurobiology of Aging 34(2), 636-639. doi:10.1016/j.neurobiolaging.2012.03.009; 10.1016/j. neurobiolaging.2012.03.009
55. Yu, C.E., Bird, T.D., Bekris, L.M., Montine, T.J., Leverenz, J.B., Steinbart, E., ⋯ Van Deerlin, V.M. (2010). The spectrum of mutations in progranulin: A collaborative study screening 545 cases of neurodegeneration. Archives of Neurology, 67(2), 161-170. doi:10.1001/archneurol.2009.328