Tartrate-resistant acid phosphatase (TRAP) co-localizes with receptor activator of NF-KB ligand (RANKL) and osteoprotegerin (OPG) in lysosomal-associated membrane protein 1 (LAMP1)-positive vesicles in rat osteoblasts and osteocytes

Histochemistry and Cell Biology

Volumn 143, Issue 2, 2015, Pages 195-207

  Solberg, L B ^a   Stang, E ^a   Brorson, S H ^a   Andersson, G ^b   Reinholt, F P ^a,c  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITY OF OSLO   (Norway)

Author keywords

LAMP1; OPG; Osteoblast; Osteocyte; RANKL; TRAP

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; ACID PHOSPHATASE; ISOENZYME; TARTRATE-RESISTANT ACID PHOSPHATASE;

ANIMAL CELL; ARTICLE; CARTILAGE CELL; CELL VACUOLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; IMMUNOFLUORESCENCE; IN VITRO STUDY; NONHUMAN; OSTEOBLAST; OSTEOCYTE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; ENZYMOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; MICROBIOLOGY; PROTEIN TRANSPORT;

RATTUS;

ACID PHOSPHATASE; ANIMALS; FLUORESCENT ANTIBODY TECHNIQUE; ISOENZYMES; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; MICROSCOPY, ELECTRON, TRANSMISSION; OSTEOBLASTS; OSTEOCYTES; OSTEOPROTEGERIN; PROTEIN TRANSPORT; RANK LIGAND; RATS;

EID: 84921407934     PISSN: 09486143     EISSN: 1432119X     Source Type: Journal    
DOI: 10.1007/s00418-014-1272-4     Document Type: Article

References (54)

1. Angel NZ, Walsh N, Forwood MR, Ostrowski MC, Cassady AI, Hume DA (2000) Transgenic mice overexpressing tartrate-resistant acid phosphatase exhibit an increased rate of bone turnover. J Bone Miner Res 15:103–110
2. Aoki S, Honma M, Kariya Y, Nakamichi Y, Ninomiya T, Takahashi N, Udagawa N, Suzuki H (2010) Function of OPG as a traffic regulator for RANKL is crucial for controlled osteoclastogenesis. J Bone Miner Res 25:1907–1921
3. Baik AD, Qiu J, Hillman EM, Dong C, Guo XE (2013) Simultaneous tracking of 3D actin and microtubule strains in individual MLO-Y4 osteocytes under oscillatory flow. Biochem Biophys Res Commun 431:718–723
4. Bianco P, Ballanti P, Bonucci E (1988) Tartrate-resistant acid phosphatase activity in rat osteoblasts and osteocytes. Calcif Tissue Int 43:167–171
5. Blott EJ, Griffiths GM (2002) Secretory lysosomes. Nat Rev Mol Cell Biol 3:122–131
6. Blumer MJ, Hausott B, Schwarzer C, Hayman AR, Stempel J, Fritsch H (2012) Role of tartrate-resistant acid phosphatase (TRAP) in long bone development. Mech Dev 129:162–176
7. Bonucci E, Mocetti P, Silvestrini G, Ballanti P, Zalzal S, Fortin M, Nanci A (2001) The osteoblastic phenotype in calcium-depleted and calcium-repleted rats: a structural and histomorphometric study. J Electron Microsc (Tokyo) 50:333–347
8. Bresciani R, Von Figura K (1996) Dephosphorylation of the mannose-6-phosphate recognition marker is localized in later compartments of the endocytic route. Identification of purple acid phosphatase (uteroferrin) as the candidate phosphatase. Eur J Biochem 238:669–674
9. Ek-Rylander B, Andersson G (2010) Osteoclast migration on phosphorylated osteopontin is regulated by endogenous tartrate-resistant acid phosphatase. Exp Cell Res 316:443–451
10. Ek-Rylander B, Bill P, Norgard M, Nilsson S, Andersson G (1991) Cloning, sequence, and developmental expression of a type 5, tartrate-resistant, acid phosphatase of rat bone. J Biol Chem 266:24684–24689
11. Ek-Rylander B, Flores M, Wendel M, Heinegard D, Andersson G (1994) Dephosphorylation of osteopontin and bone sialoprotein by osteoclastic tartrate-resistant acid phosphatase. Modulation of osteoclast adhesion in vitro. J Biol Chem 269:14853–14856
12. Fagerlund KM, Ylipahkala H, Tiitinen SL, Janckila AJ, Hamilton S, Maentausta O, Vaananen HK, Halleen JM (2006) Effects of proteolysis and reduction on phosphatase and ROS-generating activity of human tartrate-resistant acid phosphatase. Arch Biochem Biophys 449:1–7
13. Fukuda M (1991) Lysosomal membrane glycoproteins. Structure, biosynthesis, and intracellular trafficking. J Biol Chem 266:21327–21330
14. Funhoff EG, Klaassen CH, Samyn B, Van Beeumen J, Averill BA (2001) The highly exposed loop region in mammalian purple acid phosphatase controls the catalytic activity. Chembiochem 2:355–363
15. Gradin P, Hollberg K, Cassady AI, Lang P, Andersson G (2012) Transgenic overexpression of tartrate-resistant acid phosphatase is associated with induction of osteoblast gene expression and increased cortical bone mineral content and density. Cells Tissues Organs 196:68–81
16. Griffiths G (1993) Fine structure immunocytochemistry. Springer, Berlin
17. Guide for the care and use of laboratory animals (2011). In Washington, DC, The National Academies Press
18. Halleen JM, Raisanen S, Salo JJ, Reddy SV, Roodman GD, Hentunen TA, Lehenkari PP, Kaija H, Vihko P, Vaananen HK (1999) Intracellular fragmentation of bone resorption products by reactive oxygen species generated by osteoclastic tartrate-resistant acid phosphatase. J Biol Chem 274:22907–22910
19. Halleen JM, Ylipahkala H, Alatalo SL, Janckila AJ, Heikkinen JE, Suominen H, Cheng S, Vaananen HK (2002) Serum tartrate-resistant acid phosphatase 5b, but not 5a, correlates with other markers of bone turnover and bone mineral density. Calcif Tissue Int 71:20–25
20. Halleen JM, Raisanen SR, Alatalo SL, Vaananen HK (2003) Potential function for the ROS-generating activity of TRACP. J Bone Miner Res 18:1908–1911
21. Hayman AR, Jones SJ, Boyde A, Foster D, Colledge WH, Carlton MB, Evans MJ, Cox TM (1996) Mice lacking tartrate-resistant acid phosphatase (Acp 5) have disrupted endochondral ossification and mild osteopetrosis. Development 122:3151–3162
22. Hessle L, Stordalen GA, Wenglen C, Petzold C, Tanner EK, Brorson SH, Baekkevold ES, Onnerfjord P, Reinholt FP, Heinegard D (2013) The skeletal phenotype of chondroadherin deficient mice. PLoS One 8:e63080
23. Hirokawa N, Takemura R (2005) Molecular motors and mechanisms of directional transport in neurons. Nat Rev Neurosci 6:201–214
24. Hollberg K, Hultenby K, Hayman A, Cox T, Andersson G (2002) Osteoclasts from mice deficient in tartrate-resistant acid phosphatase have altered ruffled borders and disturbed intracellular vesicular transport. Exp Cell Res 279:227–238
25. Holt OJ, Gallo F, Griffiths GM (2006) Regulating secretory lysosomes. J Biochem 140:7–12
26. Honma M, Ikebuchi Y, Kariya Y, Hayashi M, Hayashi N, Aoki S, Suzuki H (2013) RANKL subcellular trafficking and regulatory mechanisms in osteocytes. J Bone Miner Res 28:1936–1949
27. Ikeda T, Utsuyama M, Hirokawa K (2001) Expression profiles of receptor activator of nuclear factor kappaB ligand, receptor activator of nuclear factor kappaB, and osteoprotegerin messenger RNA in aged and ovariectomized rat bones. J Bone Miner Res 16:1416–1425
28. Kariya Y, Honma M, Aoki S, Chiba A, Suzuki H (2009) Vps33a mediates RANKL storage in secretory lysosomes in osteoblastic cells. J Bone Miner Res 24:1741–1752
29. Kariya Y, Honma M, Hanamura A, Aoki S, Ninomiya T, Nakamichi Y, Udagawa N, Suzuki H (2011) Rab27a and Rab27b are involved in stimulation-dependent RANKL release from secretory lysosomes in osteoblastic cells. J Bone Miner Res 26:689–703
30. Kartsogiannis V, Zhou H, Horwood NJ, Thomas RJ, Hards DK, Quinn JM, Niforas P, Ng KW, Martin TJ, Gillespie MT (1999) Localization of RANKL (receptor activator of NF kappa B ligand) mRNA and protein in skeletal and extraskeletal tissues. Bone 25:525–534
31. Kishimoto K, Kitazawa R, Kurosaka M, Maeda S, Kitazawa S (2006) Expression profile of genes related to osteoclastogenesis in mouse growth plate and articular cartilage. Histochem Cell Biol 125:593–602
32. Kogawa M, Wijenayaka AR, Ormsby R, Thomas GP, Anderson PH, Bonewald LF, Findlay DM, Atkins GJ (2013) Sclerostin regulates release of bone mineral by osteocytes by induction of carbonic anhydrase 2. J Bone Miner Res 28:2436–2448
33. Lang P, Andersson G (2005) Differential expression of monomeric and proteolytically processed forms of tartrate-resistant acid phosphatase in rat tissues. Cell Mol Life Sci 62:905–918
34. Lang P, van Harmelen V, Ryden M, Kaaman M, Parini P, Carneheim C, Cassady AI, Hume DA, Andersson G, Arner P (2008) Monomeric tartrate resistant acid phosphatase induces insulin sensitive obesity. PLoS One 3:e1713
35. Ljusberg J, Ek-Rylander B, Andersson G (1999) Tartrate-resistant purple acid phosphatase is synthesized as a latent proenzyme and activated by cysteine proteinases. Biochem J 1:63–69
36. Mocetti P, Ballanti P, Zalzal S, Silvestrini G, Bonucci E, Nanci A (2000) A histomorphometric, structural, and immunocytochemical study of the effects of diet-induced hypocalcemia on bone in growing rats. J Histochem Cytochem 48:1059–1078
37. Murshid SA, Kamioka H, Ishihara Y, Ando R, Sugawara Y, Takano-Yamamoto T (2007) Actin and microtubule cytoskeletons of the processes of 3D-cultured MC3T3-E1 cells and osteocytes. J Bone Miner Metab 25:151–158
38. Nakano Y, Toyosawa S, Takano Y (2004) Eccentric localization of osteocytes expressing enzymatic activities, protein, and mRNA signals for type 5 tartrate-resistant acid phosphatase (TRAP). J Histochem Cytochem 52:1475–1482
39. Nakashima T, Hayashi M, Fukunaga T, Kurata K, Oh-Hora M, Feng JQ, Bonewald LF, Kodama T, Wutz A, Wagner EF, Penninger JM, Takayanagi H (2011) Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat Med 17:1231–1234
40. Patlaka C, Norgard M, Paulie S, Nordvall-Bodell A, Lang P, Andersson G (2014) Caveolae-mediated endocytosis of the glucosaminoglycan-interacting adipokine tartrate resistant acid phosphatase 5a in adipocyte progenitor lineage cells. Biochim Biophys Acta 1843:495–507
41. Qing H, Ardeshirpour L, Pajevic PD, Dusevich V, Jahn K, Kato S, Wysolmerski J, Bonewald LF (2012) Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation. J Bone Miner Res 27:1018–1029
42. Raposo G, Stoorvogel W (2013) Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 200:373–383
43. Reinholt FP, Widholm SM, Ek-Rylander B, Andersson G (1990) Ultrastructural localization of a tartrate-resistant acid ATPase in bone. J Bone Miner Res 5:1055–1061
44. Silvestrini G, Ballanti P, Patacchioli F, Leopizzi M, Gualtieri N, Monnazzi P, Tremante E, Sardella D, Bonucci E (2005) Detection of osteoprotegerin (OPG) and its ligand (RANKL) mRNA and protein in femur and tibia of the rat. J Mol Histol 36:59–67
45. Solberg LB, Brorson SH, Stordalen GA, Baekkevold ES, Andersson G, Reinholt FP (2014) Increased tartrate-resistant acid phosphatase expression in osteoblasts and osteocytes in experimental osteoporosis in rats. Calcif Tissue Int 94:510–521
46. Sun P, Sleat DE, Lecocq M, Hayman AR, Jadot M, Lobel P (2008) Acid phosphatase 5 is responsible for removing the mannose 6-phosphate recognition marker from lysosomal proteins. Proc Natl Acad Sci USA 105:16590–16595
47. Suter A, Everts V, Boyde A, Jones SJ, Lullmann-Rauch R, Hartmann D, Hayman AR, Cox TM, Evans MJ, Meister T, von Figura K, Saftig P (2001) Overlapping functions of lysosomal acid phosphatase (LAP) and tartrate-resistant acid phosphatase (Acp5) revealed by doubly deficient mice. Development 128:4899–4910
48. Vaaraniemi J, Halleen JM, Kaarlonen K, Ylipahkala H, Alatalo SL, Andersson G, Kaija H, Vihko P, Vaananen HK (2004) Intracellular machinery for matrix degradation in bone-resorbing osteoclasts. J Bone Miner Res 19:1432–1440
49. 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
50. Xiong J, Piemontese M, Thostenson JD, Weinstein RS, Manolagas SC, O’Brien CA (2014) Osteocyte-derived RANKL is a critical mediator of the increased bone resorption caused by dietary calcium deficiency. Bone 66C:146–154
51. Yamamoto T, Nagai H (1998) Ultrastructural localization of tartrate-resistant acid phosphatase activity in rat osteoblasts. J Electron Microsc (Tokyo) 47:659–663
52. You LD, Weinbaum S, Cowin SC, Schaffler MB (2004) Ultrastructure of the osteocyte process and its pericellular matrix. Anat Rec A Discov Mol Cell Evol Biol 278:505–513
53. Zenger S, Ek-Rylander B, Andersson G (2010) Biogenesis of tartrate-resistant acid phosphatase isoforms 5a and 5b in stably transfected MDA-MB-231 breast cancer epithelial cells. Biochim Bophys Acta 1803:598–607
54. Zinchuk V, Zinchuk O, Okada T (2007) Quantitative colocalization analysis of multicolor confocal immunofluorescence microscopy images: pushing pixels to explore biological phenomena. Acta Histochem Cytochem 40:101–111