A point mutation in the ubiquitin-associated domain of SQSMT1 is sufficient to cause a Paget's disease-like disorder in mice

Human Molecular Genetics

Volumn 20, Issue 14, 2011, Pages 2734-2744

  Daroszewska, Anna ^a   van 't Hof, Robert J ^a   Rojas, Javier A ^a   Layfield, Robert ^b   Landao Basonga, Euphemie ^a   Rose, Lorraine ^a   Rose, Ken ^a   Ralston, Stuart H ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGY PROTEIN 5; BAFILOMYCIN; PROLINE; SQSTM1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BONE LESION; BONE STRUCTURE; BONE TURNOVER; CELL NUCLEUS INCLUSION BODY; CONTROLLED STUDY; FEMALE; GENE MUTATION; HETEROZYGOTE; HOMOZYGOTE; LIGHT CHAIN; MOUSE; NONHUMAN; OSSIFICATION; OSTEOCLAST; OSTEOLYSIS; PAGET BONE DISEASE; POINT MUTATION; PRIORITY JOURNAL; WILD TYPE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SUBSTITUTION; ANIMALS; AUTOPHAGY; BONE RESORPTION; DISEASE MODELS, ANIMAL; HEAT-SHOCK PROTEINS; HUMANS; MICE; MICE, MUTANT STRAINS; MICROTUBULE-ASSOCIATED PROTEINS; OSTEITIS DEFORMANS; OSTEOCLASTS; OSTEOGENESIS; POINT MUTATION; RANK LIGAND;

MUS;

EID: 79959810997     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr172     Document Type: Article

References (43)

1. Ralston, S.H., Langston, A.L. and Reid, I.R. (2008) Pathogenesis and management of Paget's disease of bone. Lancet, 372, 155-163.
2. Laurin, N., Brown, J.P., Morissette, J. and Raymond, V. (2002) Recurrent mutation of the gene encoding sequestosome 1 (SQSTM1/p62) in Paget disease of bone. Am. J. Hum. Genet., 70, 1582-1588.
3. Hocking, L.J., Lucas, G.J.A., Daroszewska, A., Mangion, J., Olavesen, M., Nicholson, G.C., Ward, L., Bennett, S.T., Wuyts, W., Van Hul, W. et al. (2002) Domain specific mutations in Sequestosome 1 (SQSTM1) cause familial and sporadic Paget's disease. Hum. Mol. Genet., 11, 2735-2739.
4. Albagha, O.M., Visconti, M.R., Alonso, N., Langston, A.L., Cundy, T., Dargie, R., Dunlop, M.G., Fraser, W.D., Hooper, M.J., Isaia, G. et al. (2010) Genome-wide association study identifies variants at CSF1, OPTN and TNFRSF11A as genetic risk factors for Paget's disease of bone. Nat. Genet., 42, 520-524.
5. Moscat, J. and Diaz-Meco, M.T. (2009) p62 at the crossroads of autophagy, apoptosis, and cancer. Cell, 137, 1001-1004.
6. Hocking, L.J., Lucas, G.J.A., Daroszewska, A., Cundy, T., Nicholson, G.C., Donath, J., Walsh, J.P., Finlayson, C., Cavey, J.R., Ciani, B. et al. (2004) Novel UBA domain mutations of SQSTM1 in Paget's disease of bone: genotype phenotype correlation, functional analysis and structural consequences. J. Bone Miner. Res., 19, 1122-1127.
7. Falchetti, A., Di Stefano, M., Marini, F., Ortolani, S., Ulivieri, M.F., Bergui, S., Masi, L., Cepollaro, C., Benucci, M., Di, M.O. et al. (2009) Genetic epidemiology of Paget's disease of bone in Italy: sequestosome1/ p62 gene mutational test and haplotype analysis at 5q35 in a large representative series of sporadic and familial Italian cases of Paget's disease of bone. Calcif. Tissue Int., 84, 20-37.
8. Rea, S.L., Walsh, J.P., Ward, L., Magno, A.L., Ward, B.K., Shaw, B., Layfield, R., Kent, G.N., Xu, J. and Ratajczak, T. (2009) Sequestosome 1 mutations in Paget's disease of bone in Australia: prevalence, genotype/phenotype correlation and a novel non-UBA domain mutation (P364S) associated with increased NF-kappaB signaling without loss of ubiquitin-binding. J. Bone Miner. Res., 24, 1216-1223.
9. Johnson-Pais, T.L., Wisdom, J.H., Weldon, K.S., Cody, J.D., Hansen, M.F., Singer, F.R. and Leach, R.J. (2003) Three novel mutations in SQSTM1 identified in familial Paget's disease of bone. J. Bone Miner. Res., 18, 1748-1753.
10. Cavey, J.R., Ralston, S.H., Sheppard, P.W., Ciani, B., Gallagher, T.R., Long, J.E., Searle, M.S. and Layfield, R. (2006) Loss of ubiquitin binding is a unifying mechanism by which mutations of SQSTM1 cause Paget's disease of bone. Calcif. Tissue Int., 78, 271-277.
11. Yip, K.H., Feng, H., Pavlos, N.J., Zheng, M.H. and Xu, J. (2006) p62 ubiquitin binding-associated domain mediated the receptor activator of nuclear factor-kappaB ligand-induced osteoclast formation: a new insight into the pathogenesis of Paget's disease of bone. Am. J. Pathol., 169, 503-514.
12. Rea, S.L., Walsh, J.P., Ward, L., Yip, K., Ward, B.K., Kent, G.N., Steer, J.H., Xu, J. and Ratajczak, T. (2006) A novel mutation (K378X) in the sequestosome 1 gene associated with increased NF-kappaB signaling and Paget's disease of bone with a severe phenotype. J. Bone Miner. Res., 21, 1136-1145.
13. Chamoux, E., Couture, J., Bisson, M., Morissette, J., Brown, J.P. and Roux, S. (2009) The p62 P392L mutation linked to Paget's disease induces activation of human osteoclasts. Mol. Endocrinol., 23, 1668-1680.
14. Morissette, J., Laurin, N. and Brown, J.P. (2006) Sequestosome 1: mutation frequencies, haplotypes, and phenotypes in familial Paget's disease of bone. J. Bone Miner. Res., 21(Suppl. 2), 38-44.
15. Bolland, M.J., Tong, P.C., Naot, D., Callon, K.E., Wattie, D.J., Gamble, G.D. and Cundy, T. (2007) Delayed development of Paget's disease in offspring inheriting SQSTM1 mutations. J. Bone Miner. Res., 22, 411-415.
16. Cundy, H.R., Gamble, G., Wattie, D., Rutland, M. and Cundy, T. (2004) Paget's disease of bone in New Zealand: continued decline in disease severity. Calcif. Tissue Int., 75, 358-364.
17. Cooper, C., Schafheutle, K., Dennison, E., Kellingray, S., Guyer, P. and Barker, D. (1999) The epidemiology of Paget's disease in Britain: is the prevalence decreasing?. J. Bone Miner. Res., 14, 192-197.
18. Roodman, G.D. and Windle, J.J. (2005) Paget disease of bone. J. Clin. Invest., 115, 200-208.
19. Rebel, A., Malkani, K., Basle, M., Bregeon, C., Patezour, A. and Filmon, R. (1974) Ultrastructural characteristics of osteoclasts in Paget's disease. Rev. Rhum. Mal. Osteoartic., 41, 767-771.
20. Mills, B.G. and Singer, F.R. (1976) Nuclear inclusions in Paget's disease of bone. Science, 194, 201-202.
21. Harvey, L., Gray, T., Beneton, M.N.C., Douglas, D.L., Kanis, J.A. and Russell, R.G.G. (1982) Ultrastructural features of the osteoclasts from Paget's disease of bone in relation to a viral aetiology. J. Clin. Path., 35, 771-779.
22. Eekhoff, E.W., Karperien, M., Houtsma, D., Zwinderman, A.H., Dragoiescu, C., Kneppers, A.L. and Papapoulos, S.E. (2004) Familial Paget's disease in The Netherlands: occurrence, identification of new mutations in the sequestosome 1 gene, and their clinical associations. Arth. Rheum., 50, 1650-1654.
23. Helfrich, M.H., Hobson, R.P., Grabowski, P.S., Zurbriggen, A., Cosby, S.L., Dickson, G.R., Fraser, W.D., Ooi, C.G., Selby, P.L., Crisp, A.J. et al. (2000) A negative search for a paramyxoviral etiology of Paget's disease of bone: molecular, immunological, and ultrastructural studies in UK patients. J. Bone Miner. Res., 15, 2315-2329.
24. Garg, R.K. (2002) Subacute sclerosing panencephalitis. Postgrad. Med. J., 78, 63-70.
25. Layfield, R., Cavey, J.R., Najat, D., Long, J., Sheppard, P.W., Ralston, S.H. and Searle, M.S. (2006) p62 mutations, ubiquitin recognition and Paget's disease of bone. Biochem. Soc. Trans., 34, 735-737.
26. Aguado, C., Sarkar, S., Korolchuk, V.I., Criado, O., Vernia, S., Boya, P., Sanz, P., de, C. Sr, Knecht, E. and Rubinsztein, D.C. (2010) Laforin, the most common protein mutated in Lafora disease, regulates autophagy. Hum. Mol. Genet., 19, 2867-2876.
27. Komatsu, M., Waguri, S., Chiba, T., Murata, S., Iwata, J., Tanida, I., Ueno, T., Koike, M., Uchiyama, Y., Kominami, E. et al. (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature, 441, 880-884.
28. Prescott, N.J., Fisher, S.A., Franke, A., Hampe, J., Onnie, C.M., Soars, D., Bagnall, R., Mirza, M.M., Sanderson, J., Forbes, A. et al. (2007) A nonsynonymous SNP in ATG16L1 predisposes to ileal Crohn's disease and is independent of CARD15 and IBD5. Gastroenterology, 132, 1665-1671.
29. Ravikumar, B., Sarkar, S., Davies, J.E., Futter, M., Garcia-Arencibia, M., Green-Thompson, Z.W., Jimenez-Sanchez, M., Korolchuk, V.I., Lichtenberg, M., Luo, S. et al. (2010) Regulation of mammalian autophagy in physiology and pathophysiology. Physiol. Rev., 90, 1383-1435.
30. Ravikumar, B., Futter, M., Jahreiss, L., Korolchuk, V.I., Lichtenberg, M., Luo, S., Massey, D.C., Menzies, F.M., Narayanan, U., Renna, M. et al. (2009) Mammalian macroautophagy at a glance. J. Cell Sci., 122, 1707-1711.
31. Langston, A.L., Campbell, M.K., Fraser, W.D., MacLennan, G.S., Selby, P.L. and Ralston, S.H. (2010) Randomised trial of intensive bisphosphonate treatment versus symptomatic management in Paget's disease of bone. J. Bone Miner. Res., 25, 20-31.
32. Collet, C., Michou, L., Audran, M., Chasseigneaux, S., Hilliquin, P., Bardin, T., Lemaire, I., Cornelis, F., Launay, J.M., Orcel, P. et al. (2007) Paget's disease of bone in the French population: novel SQSTM1 mutations, functional analysis, and genotype-phenotype correlations. J. Bone Miner. Res., 22, 310-317.
33. Solomon, L.R. (1979) Billiard-player's fingers: an unusual case of Paget's disease of bone. Br. Med. J., 1, 931.
34. Gasper, T.M. (1979) Paget's disease in a treadle machine operator [letter]. Br. Med. J., 1, 1217-1218.
35. Rosol, T.J., Tannehill-Gregg, S.H., LeRoy, B.E., Mandl, S. and Contag, C.H. (2003) Animal models of bone metastasis. Cancer, 97, 748-757.
36. Merchant, A., Smielewska, M., Patel, N., Akunowicz, J.D., Saria, E.A., Delaney, J.D., Leach, R.J., Seton, M. and Hansen, M.F. (2009) Somatic mutations in SQSTM1 detected in affected tissues from patients with sporadic Paget's disease of bone. J. Bone Miner. Res., 24, 484-494.
37. Matthews, B.G., Naot, D., Bava, U., Callon, K.E., Pitto, R.P., McCowan, S.A., Wattie, D., Cundy, T., Cornish, J. and Reid, I.R. (2009) Absence of somatic SQSTM1 mutations in Paget's disease of bone. J. Clin. Endocrinol. Metab., 94, 691-694.
38. Merlotti, D., Gennari, L., Galli, B., Martini, G., Calabro, A., De Paola, V, Ceccarelli, E., Nardi, P., Avanzati, A. and Nuti, R. (2005) Characteristics and familial aggregation of Paget's disease of bone in Italy. J. Bone Miner. Res., 20, 1356-1364.
39. Duran, A., Serrano, M., Leitges, M., Flores, J.M., Picard, S., Brown, J.P., Moscat, J. and Diaz-Meco, M.T. (2004) The atypical PKC-interacting protein p62 is an important mediator of RANK-activated osteoclastogenesis. Dev. Cell, 6, 303-309.
40. Kurihara, N., Hiruma, Y., Zhou, H., Subler, M.A., Dempster, D.W., Singer, F.R., Reddy, S.V., Gruber, H.E., Windle, J.J. and Roodman, G.D. (2007) Mutation of the sequestosome 1 (p62) gene increases osteoclastogenesis but does not induce Paget disease. J. Clin. Invest., 117, 133-142.
41. Hiruma, Y., Kurihara, N., Subler, M.A., Zhou, H., Boykin, C.S., Zhang, H., Ishizuka, S., Dempster, D.W., Roodman, G.D. and Windle, J.J. (2008) A SQSTM1/p62 mutation linked to Paget's disease increases the osteoclastogenic potential of the bone microenvironment. Hum. Mol. Genet., 17, 3708-3719.
42. Idris, A.I., Sophocleous, A., Landao-Bassonga, E., van't Hof, R.J. and Ralston, S.H. (2008) Regulation of bone mass, osteoclast function and ovariectomy-induced bone loss by the type 2 cannabinoid receptor. Endocrinology, 149, 5619-5626.
43. Idris, A.I., Rojas, J., Greig, I.R., van't Hof, R.J. and Ralston, S.H. (2008) Aminobisphosphonates cause osteoblast apoptosis and inhibit bone nodule formation in vitro. Calcif. Tissue Int., 82, 191-201.