Protein kinase C-delta deficiency perturbs bone homeostasis by selective uncoupling of cathepsin K secretion and ruffled border formation in osteoclasts

Journal of Bone and Mineral Research

Volumn 27, Issue 12, 2012, Pages 2452-2463

  Cremasco, Viviana ^a   Decker, Corinne E ^a   Stumpo, Deborah ^b   Blackshear, Perry J ^b   Nakayama, Keiichi I ^c   Nakayama, Keiko ^d   Lupu, Traian S ^a   Graham, Daniel B ^a   Novack, Deborah V ^a   Faccio, Roberta ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^c KYUSHU UNIVERSITY   (Japan)

^d TOHOKU UNIVERSITY   (Japan)

Author keywords

BONE RESORPTION; LYSOSOMAL SECRETION; OSTEOCLASTS; PKC

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ALANINE; CATHEPSIN K; PROTEIN KINASE C DELTA; UNCLASSIFIED DRUG; VACUOLAR ADENOSINE TRIPHOSPHATASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MASS; CELL VACUOLE; CONTROLLED STUDY; ENZYME SUBSTRATE; EXOCYTOSIS; FEMALE; HOMEOSTASIS; IN VIVO STUDY; LYSOSOME; MOUSE; MYRISTYLATION; NONHUMAN; OSTEOCLAST; OSTEOLYSIS; POSTMENOPAUSE OSTEOPOROSIS; PROTEIN FUNCTION; PROTEIN SECRETION;

ANIMALS; BONE AND BONES; BONE RESORPTION; CATHEPSIN K; CELL MEMBRANE; EXOCYTOSIS; HOMEOSTASIS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYSOSOMES; MEMBRANE PROTEINS; MICE; OSTEOCLASTS; PROTEIN KINASE C-DELTA; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84869480738     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.1701     Document Type: Article

References (44)

1. Blott EJ, Griffiths GM., Secretory lysosomes. Nat Rev Mol Cell Biol. 2002; 3 (2): 122-31.
2. Novack DV, Teitelbaum SL., The osteoclast: friend or foe?. Annu Rev Pathol. 2008; 3: 457-84.
3. Zaidi M., Skeletal remodeling in health and disease. Nat Med. 2007; 13 (7): 791-801.
4. Teitelbaum SL, Ross FP., Genetic regulation of osteoclast development and function. Nat Rev Genet. 2003; 4: 638-49.
5. Collin O, Tracqui P, Stephanou A, Usson Y, Clement-Lacroix J, Planus E., Spatiotemporal dynamics of actin-rich adhesion microdomains: influence of substrate flexibility. J Cell Sci. 2006; 119 (Pt 9): 1914-25.
6. Teti A, Grano M, Carano A, Colucci S, Zambonin Zallone A., Immunolocalization of beta 3 subunit of integrins in osteoclast membrane. Boll Soc Ital Biol Sper. 1989; 65 (11): 1031-7.
7. Vaananen HK, Horton M., The osteoclast clear zone is a specialized cell-extracellular matrix adhesion structure. J Cell Sci. 1995; 108: 2729-32.
8. Nakamura I, Pilkington MF, Lakkakorpi PT, Lipfert L, Sims SM, Dixon SJ, Rodan GA, Duong LT., Role of avb3 integrin in osteoclast migration and formation of the sealing zone. J Cell Sci. 1999; 112: 3985-93.
9. Baron R, Neff L, Brown W, Courtoy PJ, Louvard D, Farquhar M., 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. 1988; 106: 1863-72.
10. Palokangas H, Mulari M, Vaananen HK., Endocytic pathway from the basal plasma membrane to the ruffled border membrane in bone-resorbing osteoclasts. J Cell Sci. 1997; 110 (Pt 15): 1767-80.
11. Vaananen HK, Karhukorpi EK, Sundquist K, Wallmark B, Roininen I, Hentunen T, Tuukkanen J, Lakkakorpi P., Evidence for the presence of a proton pump of the vacuolar H(+)-ATPase type in the ruffled borders of osteoclasts. J Cell Biol. 1990; 111 (3): 1305-11.
12. Baron R, Neff L, Louvard D, Courtoy PJ., Cell-mediated extracellular acidification and bone resorption: evidence for a low pH in resorbing lacunae and localization of a 100-kD lysosomal membrane protein at the osteoclast ruffled border. J Cell Biol. 1985; 101 (6): 2210-22.
13. Gowen M, Lazner F, Dodds R, Kapadia R, Feild J, Tavaria M, Bertoncello I, Drake F, Zavarselk S, Tellis I, Hertzog P, Debouck C, Kola I., Cathepsin K knockout mice develop osteopetrosis due to a deficit in matrix degradation but not demineralization. J Bone Miner Res. 1999; 14 (10): 1654-63.
14. Drake FH, Dodds RA, James IE, Connor JR, Debouck C, Richardson S, Leerykaczewski E, Coleman L, Rieman D, Barthlow R, Hastings G, Gowen M., Cathepsin K, but not Cathepsins B, L, or S, is abundantly expressed in human osteoclasts. J Biol Chem. 1996; 271: 12511-6.
15. Johnson MR, Polymeropoulos MH, Vos HL, Ortiz deLuna RI, Francomano CA., A nonsense mutation in the cathepsin K gene observed in a family with pycnodysostosis. Genome Res. 1996; 6 (11): 1050-5.
16. Gelb BD, Shi GP, Chapman HA, Desnick RJ., Pycnodysostosis, a lysosomal disease caused by cathepsin K deficiency. Science. 1996; 273: 1236-8.
17. Stenbeck G., Formation and function of the ruffled border in osteoclasts. Semin Cell Dev Biol. 2002; 13 (4): 285-92.
18. Zhao H, Ettala O, Vaananen HK., Intracellular membrane trafficking pathways in bone-resorbing osteoclasts revealed by cloning and subcellular localization studies of small GTP-binding rab proteins. Biochem Biophys Res Commun. 2002; 293: 1060-5.
19. Zhao H, Laitala-Leinonen T, Parikka V, Vaananen HK., Downregulation of small GTPase Rab7 impairs osteoclast polarization and bone resorption. J Biol Chem. 2001; 276 (42): 39295-302.
20. Zhao H, Ito Y, Chappel J, Andrews NW, Teitelbaum SL, Ross FP., Synaptotagmin VII regulates bone remodeling by modulating osteoclast and osteoblast secretion. Dev Cell. 2008; 14 (6): 914-25.
21. Dumas F, Byrne RD, Vincent B, Hobday TM, Poccia DL, Larijani B., Spatial regulation of membrane fusion controlled by modification of phosphoinositides. PLoS One. 2010; 5 (8): e12208.
22. Epple H, Cremasco V, Zhang K, Mao D, Longmore GD, Faccio R., Phospholipase Cgamma2 modulates integrin signaling in the osteoclast by affecting the localization and activation of Src kinase. Mol Cell Biol. 2008; 28 (11): 3610-22.
23. Stumpo DJ, Bock CB, Tuttle JS, Blackshear PJ., MARCKS deficiency in mice leads to abnormal brain development and perinatal death. Proc Natl Acad Sci U S A. 1995; 92 (4): 944-8.
24. Miyamoto A, Nakayama K, Imaki H, Hirose S, Jiang Y, Abe M, Tsukiyama T, Nagahama H, Ohno S, Hatakeyama S, Nakayama KI., Increased proliferation of B cells and auto-immunity in mice lacking protein kinase Cdelta. Nature. 2002; 416 (6883): 865-9.
25. Ito Y, Teitelbaum SL, Zou W, Zheng Y, Johnson JF, Chappel J, Ross FP, Zhao H., Cdc42 regulates bone modeling and remodeling in mice by modulating RANKL/M-CSF signaling and osteoclast polarization. J Clin Invest. 2010; 120 (6): 1981-93.
26. Faccio R, Novack DV, Zallone A, Ross FP, Teitelbaum SL., Dynamic changes in the osteoclast cytoskeleton in response to growth factors and cell attachment are controlled by beta3 integrin. J Cell Biol. 2003; 162 (3): 499-509.
27. Mulari MT, Zhao H, Lakkakorpi PT, Vaananen HK., Osteoclast ruffled border has distinct subdomains for secretion and degraded matrix uptake. Traffic. 2003; 4 (2): 113-25.
28. Blackshear PJ., The MARCKS family of cellular protein kinase C substrates. J Biol Chem. 1993; 268 (3): 1501-4.
29. Coue M, Brenner SL, Spector I, Korn ED., Inhibition of actin polymerization by latrunculin A. FEBS Lett. 1987; 213 (2): 316-8.
30. Hartwig JH, Thelen M, Rosen A, Janmey PA, Nairn AC, Aderem A., MARCKS is an actin filament crosslinking protein regulated by protein kinase C and calcium-calmodulin. Nature. 1992; 356 (6370): 618-22.
31. van Meel E, Boonen M, Zhao H, Oorschot V, Ross FP, Kornfeld S, Klumperman J., Disruption of the Man-6-P targeting pathway in mice impairs osteoclast secretory lysosome biogenesis. Traffic. 2011; 12 (7): 912-24.
32. Tu X, Joeng KS, Nakayama KI, Nakayama K, Rajagopal J, Carroll TJ, McMahon AP, Long F., Noncanonical Wnt signaling through G protein-linked PKCdelta activation promotes bone formation. Dev Cell. 2007; 12 (1): 113-27.
33. Moonga BS, Stein LS, Kilb JM, Dempster DW., Effect of diacylglycerols on osteoclastic bone resorption. Calcif Tissue Int. 1996; 59 (2): 105-8.
34. Trifaro JM, Gasman S, Gutierrez LM., Cytoskeletal control of vesicle transport and exocytosis in chromaffin cells. Acta Physiol (Oxf). 2008; 192 (2): 165-72.
35. Pigeau GM, Kolic J, Ball BJ, Hoppa MB, Wang YW, Ruckle T, Woo M, Manning Fox JE, MacDonald PE., Insulin granule recruitment and exocytosis is dependent on p110gamma in insulinoma and human beta-cells. Diabetes. 2009; 58 (9): 2084-92.
36. Kim J, Shishido T, Jiang X, Aderem A, McLaughlin S., Phosphorylation, high ionic strength, and calmodulin reverse the binding of MARCKS to phospholipid vesicles. J Biol Chem. 1994; 269 (45): 28214-9.
37. Taniguchi H, Manenti S., Interaction of myristoylated alanine-rich protein kinase C substrate (MARCKS) with membrane phospholipids. J Biol Chem. 1993; 268 (14): 9960-3.
38. Thelen M, Rosen A, Nairn AC, Aderem A., Regulation by phosphorylation of reversible association of a myristoylated protein kinase C substrate with the plasma membrane. Nature. 1991; 351 (6324): 320-2.
39. Cuchillo-Ibanez I, Lejen T, Albillos A, Rose SD, Olivares R, Villarroya M, Garcia AG, Trifaro JM., Mitochondrial calcium sequestration and protein kinase C cooperate in the regulation of cortical F-actin disassembly and secretion in bovine chromaffin cells. J Physiol. 2004; 560 (Pt 1): 63-76.
40. Doreian BW, Fulop TG, Meklemburg RL, Smith CB., Cortical F-actin, the exocytic mode, and neuropeptide release in mouse chromaffin cells is regulated by myristoylated alanine-rich C-kinase substrate and myosin II. Mol Biol Cell. 2009; 20 (13): 3142-54.
41. Vitale ML, Seward EP, Trifaro JM., Chromaffin cell cortical actin network dynamics control the size of the release-ready vesicle pool and the initial rate of exocytosis. Neuron. 1995; 14 (2): 353-63.
42. Rose SD, Lejen T, Zhang L, Trifaro JM., Chromaffin cell F-actin disassembly and potentiation of catecholamine release in response to protein kinase C activation by phorbol esters is mediated through myristoylated alanine-rich C kinase substrate phosphorylation. J Biol Chem. 2001; 276 (39): 36757-63.
43. Burgoyne RD, Morgan A., Secretory granule exocytosis. Physiol Rev. 2003; 83 (2): 581-632.
44. Brown AC, Oddos S, Dobbie IM, Alakoskela JM, Parton RM, Eissmann P, Neil MA, Dunsby C, French PM, Davis I, Davis DM., Remodelling of cortical actin where lytic granules dock at natural killer cell immune synapses revealed by super-resolution microscopy. PLoS Biol. 2011; 9 (9): e1001152.