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Histochemistry

, Volume 100, Issue 2, pp 101–108 | Cite as

Increased synthesis and specific localization of a major lysosomal membrane sialoglycoprotein (LGP107) at the ruffled border membrane of active osteoclasts

  • Akifumi Akamine
  • Takayuki Tsukuba
  • Ryusei Kimura
  • Katsumasa Maeda
  • Yoshitaka Tanaka
  • Keitaro Kato
  • Kenji Yamamoto
Article

Abstract

The immunocytochemical localization was investigated of a major lysosomal membrane sialoglycoprotein with a molecular mass of 107 kDa, which was designated as LGP107. The study utilized rat osteoclasts with different bone resorbing activity and osteoclast precursors at various stages of differentiation and maturation together with monospecific antibodies to this protein. Despite its localization primarily in lysosomes and endosomes in the other cell types examined, LGP107 was exclusively confined to the apical plasma membrane at the ruffled border of the active osteoclast, where the osteoclast is in contact with the bone surface. The protein was also concentrated in a number of endocytic vacuoles in the vicinity of the ruffled border membrane. However the labeling was not found in the basolateral membranes of the active osteoclast. The ruffled border membrane detached from the bone surface showed a marked decrease in the extent of the immunolabeling. The post-and/or resting osteoclasts, which were located away from the bone surface, were totally devoid of the membraneous localization of LGP107. No definite immunolabeling was found in the immature preosteoclasts. These results indicate that the protein is largely synthesized in the active osteoclast and rapidly translocated to the ruffled border membrane by vectorial vesicle transport. LGP107 is suggested to contribute to the formation and maintenance of the specialized acidic environment for bone resorption.

Keywords

Plasma Membrane Molecular Mass Bone Resorbing Specific Localization Marked Decrease 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Akasaki K, Yamaguchi Y, Ohta M, Matsuura F, Furuno K, Tsuji H (1990) Purification and characterization of a major glycoprotein in rat liver lysosomal membrane. Chem Pharm Bull 38:2766–2770Google Scholar
  2. Akisaka T, Gay GV (1986) Ultrastructural evidence for a proton pump adenosine triphosphatase (Ca++-ATPase) in chick tiba. Cell Tissue Res 245:507–517Google Scholar
  3. Anderson RE, Woodbury DM, Jee WSS (1986) Humoral and ionic regulation of osteoclast activity. Calcif Tissue Int 39:252–258Google Scholar
  4. Barnicot NA (1948) The local activation of the parathyroid and other tissue on bone in intracerebral grafts. J Anat 82:233–248Google Scholar
  5. Baron R, Neff L, Louvard DL, Courtoy PJ (1985) Cell-mediated extracellular acidification and bone resorption: evidence for a low pH in resorbing lacunae and localization of a 100-kDa lysosomal membrane protein at the osteoclast ruffled border. J Cell Biol 101:2210–2222Google Scholar
  6. Baron R, Neff L, Brown W, Courtoy PJ, Louvard D, Farquhr MG (1988) Polarized secretion of lysosomal enzymes: co-distribution of cation independent mannose 6-phosphate receptors and lysosomal enzymes in the osteoclast exocytic pathway. J Cell Biol 106:1863–1872Google Scholar
  7. Blair HC, Kahn AJ, Crouch EC, Jeffrey JL, Teitelbaum SL (1986) Isolated osteoclasts resorb the organic and inorganic components of bone. J Cell Biol 102:1164–1172Google Scholar
  8. Blair HC, Teitelbaum SL, Ghiselli R, Gluck S (1989) Osteoclastic bone resorption by a polarized vacuolar proton pump. Science 245:855–858Google Scholar
  9. Delaisse JM, Eeckhout Y, Vaes G (1984) In vitro and in vivo evidence for the involvement of cysteine proteases in bone resorption. Biochem Biophys Res Commun 125:441–447Google Scholar
  10. Eeckhout Y (1990) Possible role and mechanism of action of dissolved calcium in the degradation of bone collagen by lysosomal cathepsins and collagenase. Biochem J 272:529–532Google Scholar
  11. Ejiri S (1983) The preosteoclast and its cytodifferential into the osteoclast: ultrastructural and histochemical studies of rat fetal parietal bone. Arch Histol Jpn 46:533–557Google Scholar
  12. Everts V, Dellaisse J-M, Korper W, Niehof A, Vaes G, Beertsen W (1992) Degradation of collagen in the bone-resorbing component underlying the osteoclasts involves both cysteine-proteases and matrix metalloproteases. J Cell Physiol 150:221–231Google Scholar
  13. Furuno K, Ishikawa T, Akasaki K, Yano S, Tanaka Y, Yamaguchi Y, Tsuji H, Himeno M, Kato K (1989a) Morphological localization of a major membrane glycoprotein in the endocytic membrane system. J Biochem 106:708–716Google Scholar
  14. Furuno K, Ishikawa T, Akasaki K, Yano S, Tanaka Y, Yamaguchi Y, Tsuji H, Himeno M, Kato K (1989b) Biochemical analysis of the movement of a major lysosomal membrane glycoprotein in the endocytic membrane system. J Biochem 106:717–722Google Scholar
  15. Goto T, Tsukuba T, Ayasaka N, Yamamoto K, Tanaka T (1992) Immunocytochemical localization of cathepsin D in the rat osteoclasts. Histochemistry 97:13–18Google Scholar
  16. Goto T, Tsukuba T, Kiyoshima T, Nishimura Y, Kato K, Yamamoto K, Tanaka T (1993) Immunohistochemical localization of cathepsins B, D and L in the rat osteoclasts. Histochemistry 99:411–414Google Scholar
  17. Granger BL, Gleen SA, Gabel CA, Howe CL, Mellman I, Helenius A (1990) Characterization of cloning of lgp 110 a lysosomal membrane glycoprotein from mouse and rat cells. J Biol Chem 265:12036–12043Google Scholar
  18. Himeno M, Noguchi Y, Sasaki H, Tanaka Y, Furuno K, Kono A, Sakaki Y, Kato K (1989) Isolation and sequencing of a cDNA clone encoding 107-kDa sialoglycoprotein in rat liver lysosomal membranes. FEBS Lett 244:351–356Google Scholar
  19. Howe CL, Granger BL, Hull M, Green SA, Gabel CA, Helenius A, Mellman I (1988) Derived protein sequence, oligosaccharides, and membrane insertion the 120-kDa lysosomal membrane glycoprotein (lgp120): identification of a highly conserved family of lysosomal membrane glycoproteins. Proc Natl Acad Sci USA 85:7577–7581Google Scholar
  20. Laferte S, Dennis JW (1988) Glycosylation-dependent collagen-binding activities of two membrane glycoproteins in MDAY-D2 tumor cells. Cancer Res 48:4743–4748Google Scholar
  21. Luk SC, Napajaroonsri C, Simon GT (1974) The ultrastructure of endostem: A topographic study in young adult rabbit. J Ultrastruct Res 46:165–183Google Scholar
  22. Moriyama Y, Maeda M, Futai M (1992) Involvement of a non-proton pump factor (possibly Donnan-type equilibrium) in maintenance of an acidic pH in lysosomes. FEBS Lett 302:18–20Google Scholar
  23. Njus D, Kelly PM, Harnadek GJ (1986) Bioenergetics of secretory vesicles. Biochim Biophys Acta 853:237–265Google Scholar
  24. Ohsumi Y, Ishikawa T, Kato K (1983) A rapid and simplified method for the preparation of lysosomal membranes from rat liver. J Biochem 93:547–556Google Scholar
  25. Reeves JP (1984). The mechanism of lysosomal acidification. In: Dingle JT, Dean RT, Sly W (eds) Lysosomes in biology and pathology, vol 7. Elsevier/North-Holland, Amsterdam, pp 175–199Google Scholar
  26. Rifkin BR, Brand JS, Cushing JE, Coleman SJ, Sanavi F (1980) Fine structure of fetal rat calvarium: provisional identification of preosteoclasts. Calcif Tissue Int 31:21–28Google Scholar
  27. Rifkin BR, Vernillo AT, Kleckner AP, Auszmann JM, Rosenberg LR, Zimmerman M (1991) Cathepsin B and L activities in isolated osteoclasts. Biochem Biophys Res Commun 179:63–69Google Scholar
  28. Yamamoto K, Ikehara Y, Kawamoto S, Kato K (1980) Characterization of enzymes and glycoproteins in rat liver lysosomal membranes. J Biochem 87:237–248Google Scholar
  29. Väänänen HK, Karhukorpi E-K, Sundquist K, Wallmark Broininen I, Hentunen T, Tuukkanen J, Lakkakorpi P (1990) Evidence for the presence of a proton pump of the vacuolar H+-ATPase type in the ruffled borders of osteoclasts. J Cell Biol 111:1305–1311Google Scholar
  30. Yokota S, Tsuji H, Kato K (1986) Immunocytochemical localization of cathepsin B in rat kidney. II. Electron microscopic study using the protein A-gold technique. J Histochem Cytochem 34:899–907Google Scholar
  31. Yokota S, Nishimura Y, Kawabata T, Kato K (1990) Immunoenzyme localization of cathepsins in the Golgi region of rat hepatocytes and renal tubule cells. Histochemistry 94:629–635Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • Akifumi Akamine
    • 1
  • Takayuki Tsukuba
    • 2
  • Ryusei Kimura
    • 1
  • Katsumasa Maeda
    • 1
  • Yoshitaka Tanaka
    • 3
  • Keitaro Kato
    • 3
  • Kenji Yamamoto
    • 2
  1. 1.Department of Conservative Dentistry I, Faculty of DentistryKyushu UniversityFukuokaJapan
  2. 2.Department of Pharmacology, Faculty of DentistryKyushu UniversityFukuokaJapan
  3. 3.Department of Physiological Chemistry, Faculty of Pharmaceutical SciencesKyushu UniversityFukuokaJapan

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