Decreased bone formation and increased osteoclastogenesis cause bone loss in mucolipidosis II

EMBO Molecular Medicine

Volumn 5, Issue 12, 2013, Pages 1871-1886

  Kollmann, Katrin ^a   Pestka, Jan Malte ^a   Kühn, Sonja Christin ^a   Schöne, Elisabeth ^a   Schweizer, Michaela ^a   Karkmann, Kathrin ^a   Otomo, Takanobu ^a   Catala Lehnen, Philip ^a   Failla, Antonio Virgilio ^a   Marshall, Robert Percy ^a   Krause, Matthias ^a   Santer, Rene ^a   Amling, Michael ^a   Braulke, Thomas ^a   Schinke, Thorsten ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Alendronate; Interleukin 6; Mannose 6 phosphate; Mucolipidosis II; Osteoclastogenesis

Indexed keywords

ACID HYDROLASE; INTERLEUKIN 6;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MASS; CARTILAGE CELL; CELL DIFFERENTIATION; CHILD; CONTROLLED STUDY; FEMALE; GROWTH PLATE; HUMAN; HUMAN TISSUE; LYSOSOME STORAGE DISEASE; MORPHOMETRICS; MOUSE; MUCOLIPIDOSIS TYPE 2; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCLAST; OSTEOCLAST ACTIVITY; OSTEOCLASTOGENESIS; OSTEOLYSIS; PHENOTYPE; PRESCHOOL CHILD; PRIORITY JOURNAL; STORAGE DISEASE; TRABECULAR BONE;

ALENDRONATE; INTERLEUKIN-6; MANNOSE 6-PHOSPHATE; MUCOLIPIDOSIS II; OSTEOCLASTOGENESIS;

ANIMALS; BONE AND BONES; BONE DENSITY CONSERVATION AGENTS; BONE DEVELOPMENT; CELLS, CULTURED; CHILD, PRESCHOOL; CHONDROCYTES; DIPHOSPHONATES; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; INTERLEUKIN-6; MICE; MICE, INBRED C57BL; MUCOLIPIDOSES; OSTEOCLASTS; OSTEOGENESIS; RANK LIGAND; TRANSFERASES (OTHER SUBSTITUTED PHOSPHATE GROUPS);

EID: 84896988103     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201302979     Document Type: Article

References (58)

1. Amling M, Priemel M, Holzmann T, Chapin K, Rueger JM, Baron R, Demay MB (1999) Rescue of the skeletal phenotype of vitamin D receptor-ablated mice in the setting of normal mineral ion homeostasis: Formal histomorphometric and biomechanical analyses. Endocrinology 140: 4982-4987
2. Bao M, Booth JL, Elmendorf BJ, Canfield WM (1996) Bovine UDP-N-acetylglucosamine:lysosomal-enzyme N-acetylglucosamine-1-phosphotransferase. I. Purification and subunit structure. J Biol Chem 271: 31437-31445
3. Bargal R, Zeigler M, Abu-Libdeh B, Zuri V, Mandel H, Ben Neriah Z, Stewart F, Elcioglu N, Hindi T, Le Merrer M, et al (2006) When mucolipidosis III meets mucolipidosis II: GNPTA gene mutations in 24 patients. Mol Genet Metab 88: 359-363
4. Baron R, Neff L, Brown W, Courtoy PJ, Louvard D, Farquhar MG (1988) Polarized secretion of lysosomal enzymes: Co-distribution of cation-independent mannose-6-phosphate receptors and lysosomal enzymes along the osteoclast exocytic pathway. J Cell Biol 106: 1863-1872
5. Boonen M, van Meel E, Oorschot V, Klumperman J, Kornfeld S (2011) Vacuolization of mucolipidosis type II mouse exocrine gland cells represents accumulation of autolysosomes. Mol Biol Cell 22: 1135-1147
6. Boyle WJ, Simonet WS, Lacey DL (2003) Osteoclast differentiation and activation. Nature 423: 337-342
7. Braulke T, Bonifacino JS (2009) Sorting of lysosomal proteins. Biochim Biophys Acta 1793: 605-614
8. Braulke T, Gartung C, Hasilik A, von Figura K (1987) Is movement of mannose 6-phosphate-specific receptor triggered by binding of lysosomal enzymes? J Cell Biol 104: 1735-1742
9. Braulke T, Raas-Rothschild A, Kornfeld S, (2013) I-cell disease and pseudo-Hurler polydystrophy: Disorders of lysosomal enzyme phosphorylation and localization. In The Online Metabolic and Molecular Bases of Inherited Disease, Valle D, Beaudet A, Vogelstein B, Kinzler K, Antonarakis S, Ballabio A, Scriver C, Sly W, Childs B, Bunz F, et al (eds). New York City, NY: McGraw Hill
10. Cathey S. S, Kudo M, Tiede S, Raas-Rothschild A, Braulke T, Beck M, Taylor HA, Canfield WM, Leroy JG, Neufeld EF, et al (2008) Molecular order in mucolipidosis II and III nomenclature. Am J Med Genet A 146A: 512-513
11. Cathey SS, Leroy JG, Wood T, Eaves K, Simensen RJ, Kudo M, Stevenson RE, Friez MJ (2010) Phenotype and genotype in mucolipidoses II and III alpha/beta: A study of 61 probands. J Med Genet 47: 38-48
12. Cenedella RJ (2009) Cholesterol synthesis inhibitor U18666A and the role of sterol metabolism and trafficking in numerous pathophysiological processes. Lipids 44: 477-487
13. Cioffi M, Corradino M, Gazzerro P, Vietri MT, Di Macchia C, Contursi A, Colicigno R, Catalano T, Molinari AM (2000) Serum concentrations of intact parathyroid hormone in healthy children. Clin Chem 46: 863-864
14. Claussen M, Kübler B, Wendland M, Neifer K, Schmidt B, Zapf J, Braulke T (1997) Proteolysis of insulin-like growth factors (IGF) and IGF binding proteins by cathepsin D. Endocrinology 138: 3797-3803
15. Cox TM, Aerts JM, Belmatoug N, Cappellini MD, vom Dahl S, Goldblatt J, Grabowski GA, Hollak CE, Hwu P, Maas M, et al (2008) Management of non-neuronopathic Gaucher disease with special reference to pregnancy, splenectomy, bisphosphonate therapy, use of biomarkers and bone disease monitoring. J Inherit Metab Dis 31: 319-336
16. Coxon FP, Taylor A (2008) Vesicular trafficking in osteoclasts. Semin Cell Dev Biol 19: 424-433
17. David-Vizcarra G, Briody J, Ault J, Fietz M, Fletcher J, Savarirayan R, Wilson M, McGill J, Edwards M, Munns C, et al (2010) The natural history and osteodystrophy of mucolipidosis types II and III. J Paediatr Child Health 46: 316-322
18. De Benedetti F, Rucci N, Del Fattore A, Peruzzi B, Paro R, Longo M, Vivarelli M, Muratori F, Berni S, Ballanti P, et al (2006) Impaired skeletal development in interleukin-6-transgenic mice: A model for the impact of chronic inflammation on the growing skeletal system. Arthritis Rheum 54: 3551-3563
19. Doty SB, Schofield BH (1972) Electron microscopic localization of hydrolytic enzymes in osteoclasts. Histochem J 4: 245-258
20. Ducy P, Starbuck M, Priemel M, Shen J, Pinero G, Geoffroy V, Amling M, Karsenty G (1999) A Cbfa1-dependent genetic pathway controls bone formation beyond embryonic development. Genes Dev 13: 1025-1036
21. Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210
22. Edwards JR, Mundy GR (2011) Advances in osteoclast biology: Old findings and new insights from mouse models. Nat Rev Rheumatol 7: 235-243
23. Glickman JN, Kornfeld S (1993) Mannose 6-phosphate-independent targeting of lysosomal enzymes in I-cell disease B lymphoblasts. J Cell Biol 123: 99-108
24. Glorieux FH, Travers R, Taylor A, Bowen JR, Rauch F, Norman M, Parfitt AM (2000) Normative data for iliac bone histomorphometry in growing children. Bone 26: 103-109
25. Henriksen K, Karsdal MA, John Martin T (2013) Osteoclast-derived coupling factors in bone remodeling. Calcif Tissue Int, DOI 10.1007/s00223-013-9741-7
26. Huebner AK, Schinke T, Priemel M, Schilling S, Schilling AF, Emeson RB, Rueger JM, Amling M (2006) Calcitonin deficiency in mice progressively results in high bone turnover. J Bone Miner Res 21: 1924-1934
27. Husain SM, Mughal Z, Williams G, Ward K, Smith CS, Dutton J, Fraser WD (1999) Urinary excretion of pyridinium crosslinks in healthy 4-10 year olds. Arch Dis Child 80: 370-373
28. Ishimi Y, Miyaura C, Jin CH, Akatsu T, Abe E, Nakamura Y, Yamaguchi A, Yoshiki S, Matsuda T, Hirano T, et al (1990) IL-6 is produced by osteoblasts and induces bone resorption. J Immunol 145: 3297-3303
29. Kollmann K, Damme M, Markmann S, Morelle W, Schweizer M, Hermans-Borgmeyer I, Röchert AK, Pohl S, Lübke T, Michalski JC, et al (2012) Lysosomal dysfunction causes neurodegeneration in mucolipidosis II 'knock-in' mice. Brain 135: 2661-2675
30. Kollmann K, Pohl S, Marschner K, Encarnacao M, Sakwa I, Tiede S, Poorthuis BJ, Lübke T, Müller-Loennies S, Storch S, et al (2010) Mannose phosphorylation in health and disease. Eur J Cell Biol 89: 117-123
31. Kong YY, Feige U, Sarosi I, Bolon B, Tafuri A, Morony S, Capparelli C, Li J, Elliott R, McCabe S, et al (1999) Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 402: 304-309
32. Kudo M, Bao M, D'Souza A, Ying F, Pan H, Roe BA, Canfield WM (2005) The alpha- and beta-subunits of the human UDP-N-acetylglucosamine:lysosomal enzyme N-acetylglucosamine-1-phosphotransferase [corrected] are encoded by a single cDNA. J Biol Chem 280: 36141-36149
33. Kudo O, Sabokbar A, Pocock A, Itonaga I, Fujikawa Y, Athanasou NA (2003) Interleukin-6 and interleukin-11 support human osteoclast formation by a RANKL-independent mechanism. Bone 32: 1-7
34. Lucht U (1971) Acid phosphatase of osteoclasts demonstrated by electron microscopic histochemistry. Histochemie 28: 103-117
35. Marschner K, Kollmann K, Schweizer M, Braulke T, Pohl S (2011) A key enzyme in the biogenesis of lysosomes is a protease that regulates cholesterol metabolism. Science 333: 87-90
36. McLeod MJ (1980) Differential staining of cartilage and bone in whole mouse fetuses by alcian blue and alizarin red S. Teratology 22: 299-301
37. Nakashima T, Hayashi M, Fukunaga T, Kurata K, Oh-Hora M, Feng JQ, Bonewald LF, Kodama T, Wutz A, Wagner EF, et al (2011) Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat Med 17: 1231-1234
38. Otomo T, Yamamoto T, Fujikawa Y, Shimotsuji T, Ozono K (2011) Elevated bone turnover in an infantile patient with mucolipidosis II; no association with hyperparathyroidism. Clin Pediatr Endocrinol 20: 7-12
39. Owada M, Neufeld EF (1982) Is there a mechanism for introducing acid hydrolases into liver lysosomes that is independent of mannose 6-phosphate recognition? Evidence from I-cell disease. Biochem Biophys Res Commun 105: 814-820
40. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR (1987) Bone histomorphometry: Standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2: 595-610
41. Parisien M, Silverberg SJ, Shane E, Dempster DW, Bilezikian JP (1990) Bone disease in primary hyperparathyroidism. Endocrinol Metab Clin North Am 19: 19-34
42. Poli V, Balena R, Fattori E, Markatos A, Yamamoto M, Tanaka H, Ciliberto G, Rodan GA, Costantini F (1994) Interleukin-6 deficient mice are protected from bone loss caused by estrogen depletion. EMBO J 13: 1189-1196
43. Raas-Rothschild A, Cormier-Daire V, Bao M, Genin E, Salomon R, Brewer K, Zeigler M, Mandel H, Toth S, Roe B, et al (2000) Molecular basis of variant pseudo-hurler polydystrophy (mucolipidosis IIIC). J Clin Invest 105: 673-681
44. Raggatt LJ, Partridge NC (2010) Cellular and molecular mechanisms of bone remodeling. J Biol Chem 285: 25103-25108
45. Robinson C, Baker N, Noble J, King A, David G, Sillence D, Hofman P, Cundy T (2002) The osteodystrophy of mucolipidosis type III and the effects of intravenous pamidronate treatment. J Inherit Metab Dis 25: 681-693
46. Russell RG (2011) Bisphosphonates: The first 40 years. Bone 49: 2-19
47. Schenk RK, Spiro D, Wiener J (1967) Cartilage resorption in the tibial epiphyseal plate of growing rats. J Cell Biol 34: 275-291
48. Schmidt K, Schinke T, Haberland M, Priemel M, Schilling AF, Mueldner C, Rueger JM, Sock E, Wegner M, Amling M (2005) The high mobility group transcription factor Sox8 is a negative regulator of osteoblast differentiation. J Cell Biol 168: 899-910
49. Scott BL (1967) The occurrence of specific cytoplasmic granules in the osteoclast. J Ultrastruct Res 19: 417-431
50. Silverman SL (2011) Bisphosphonate use in conditions other than osteoporosis. Ann N Y Acad Sci 1218: 33-37
51. Spranger JW, Wiedemann HR (1970) The genetic mucolipidoses. Diagnosis and differential diagnosis. Humangenetik 9: 113-139
52. Suzuki M, Sugimoto Y, Ohsaki Y, Ueno M, Kato S, Kitamura Y, Hosokawa H, Davies JP, Ioannou YA, Vanier MT, et al (2007) Endosomal accumulation of Toll-like receptor 4 causes constitutive secretion of cytokines and activation of signal transducers and activators of transcription in Niemann-Pick disease type C (NPC) fibroblasts: A potential basis for glial cell activation in the NPC brain. J Neurosci 27: 1879-1891
53. Teitelbaum SL, Ross FP (2003) Genetic regulation of osteoclast development and function. Nat Rev Genet 4: 638-649
54. Tiede S, Storch S, Lübke T, Henrissat B, Bargal R, Raas-Rothschild A, Braulke T (2005) Mucolipidosis II is caused by mutations in GNPTA encoding the alpha/beta GlcNAc-1-phosphotransferase. Nat Med 11: 1109-1112
55. Unger S, Paul DA, Nino MC, McKay CP, Miller S, Sochett E, Braverman N, Clarke JT, Cole DE, Superti-Furga A (2005) Mucolipidosis II presenting as severe neonatal hyperparathyroidism. Eur J Pediatr 164: 236-243
56. van Meel E, Boonen M, Zhao H, Oorschot V, Ross FP, Kornfeld S, Klumperman J (2011) Disruption of the Man-6-P targeting pathway in mice impairs osteoclast secretory lysosome biogenesis. Traffic 12: 912-924
57. Weinert S, Jabs S, Supanchart C, Schweizer M, Gimber N, Richter M, Rademann J, Stauber T, Kornak U, Jentsch TJ (2010) Lysosomal pathology and osteopetrosis upon loss of H+-driven lysosomal Cl- accumulation. Science 328: 1401-1403
58. Xiong J, Onal M, Jilka RL, Weinstein RS, Manolagas SC, O'Brien CA (2011) Matrix-embedded cells control osteoclast formation. Nat Med 17: 1235-1241