Rab13 Is Upregulated During Osteoclast Differentiation and Associates with Small Vesicles Revealing Polarized Distribution in Resorbing Cells

Journal of Histochemistry and Cytochemistry

Volumn 60, Issue 7, 2012, Pages 537-549

  Hirvonen, Mirkka J ^a   Mulari, Mika T K ^a   Büki, Kálmán G ^a   Vihko, Pirkko ^b   Härkönen, Pirkko L ^a   Väänänen, H Kalervo ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

bone resorption; osteoclast; Rab; Rab13; vesicle traffic

Indexed keywords

GLUCOSE TRANSPORTER; GLUTATHIONE TRANSFERASE; RAB PROTEIN; RAB13 PROTEIN; RAB32 PROTEIN; RAB7 PROTEIN; UNCLASSIFIED DRUG; RAB13 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEFECT; CELL FUNCTION; CELL MIGRATION; CELL POLARITY; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; GENETIC REGULATION; HUMAN; HUMAN CELL; IMMUNOLOCALIZATION; MONOCYTE; NONHUMAN; OSTEOCLASTOGENESIS; OSTEOLYSIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; TRANS GOLGI NETWORK; TRANSCYTOSIS; UPREGULATION; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; OSTEOCLAST; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; CELL DIFFERENTIATION; CELL POLARITY; CELLS, CULTURED; HUMANS; IMMUNOHISTOCHEMISTRY; OSTEOCLASTS; RAB GTP-BINDING PROTEINS; RATS; REAL-TIME POLYMERASE CHAIN REACTION; UP-REGULATION;

EID: 84865842066     PISSN: 00221554     EISSN: None     Source Type: Journal    
DOI: 10.1369/0022155412448069     Document Type: Article

References (49)

1. Abu-Amer Y,Teitelbaum SL,Chappel JC,Schlesinger P,Ross FP.Expression and regulation of RAB3 proteins in osteoclasts and their precursors.J Bone Miner Res. 1999;14:1855-1860.
2. Alatalo SL,Halleen JM,Hentunen TA,Monkkonen J,Vaananen HK.Rapid screening method for osteoclast differentiation in vitro that measures tartrate-resistant acid phosphatase 5b activity secreted into the culture medium.Clin Chem. 2000;46:1751-1754.
3. Alto NM,Soderling J,Scott JD.Rab32 is an A-kinase anchoring protein and participates in mitochondrial dynamics.J Cell Biol. 2002;158:659-668.
4. Bahadoran P,Aberdam E,Mantoux F,Busca R,Bille K,Yalman N,de Saint-Basile G,Casaroli-Marano R,Ortonne JP,Ballotti R.Rab27a: A key to melanosome transport in human melanocytes.J Cell Biol. 2001;152:843-850.
5. Baron R,Neff L,Brown W,Courtoy PJ,Louvard D,Farquhar MG.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;106:1863-1872.
6. Bielli A,Thornqvist PO,Hendrick AG,Finn R,Fitzgerald K,McCaffrey MW.The small GTPase Rab4A interacts with the central region of cytoplasmic dynein light intermediate chain-1.Biochem Biophys Res Commun. 2001;281:1141-1153.
7. Coxon FP,Ebetino FH,Mules EH,Seabra MC,McKenna CE,Rogers MJ.Phosphonocarboxylate inhibitors of Rab geranylgeranyl transferase disrupt the prenylation and membrane localization of Rab proteins in osteoclasts in vitro and in vivo.Bone. 2005;37:349-358.
8. Coxon FP,Helfrich MH,Larijani B,Muzylak M,Dunford JE,Marshall D,McKinnon AD,Nesbitt SA,Horton MA,Seabra MC,Ebetino FH,Rogers MJ.Identification of a novel phosphonocarboxylate inhibitor of Rab geranylgeranyl transferase that specifically prevents Rab prenylation in osteoclasts and macrophages.J Biol Chem. 2001;276:48213-48222.
9. Di Giovanni S,De Biase A,Yakovlev A,Finn T,Beers J,Hoffman EP,Faden AI.In vivo and in vitro characterization of novel neuronal plasticity factors identified following spinal cord injury.J Biol Chem. 2005;280:2084-2091.
10. Doege H,Bocianski A,Joost HG,Schürmann A.Activity and genomic organization of human glucose transporter 9 (GLUT9), a novel member of the family of sugar-transport facilitators predominantly expressed in brain and leucocytes.Biochem J. 2000;350 (Pt 3): 771-776.
11. Fukushima O,Bekker PJ,Gay CV.Ultrastructural localization of tartrate-resistant acid phosphatase (purple acid phosphatase) activity in chicken cartilage and bone.Am J Anat. 1991;191:228-236.
12. Grosshans BL,Ortiz D,Novick P.Rabs and their effectors: achieving specificity in membrane traffic.Proc Natl Acad Sci U S A. 2006;103:11821-11827.
13. Halleen JM,Raisanen S,Salo JJ,Reddy SV,Roodman GD,Hentunen TA,Lehenkari PP,Kaija H,Vihko P,Vaananen HK.Intracellular fragmentation of bone resorption products by reactive oxygen species generated by osteoclastic tartrate-resistant acid phosphatase.J Biol Chem. 1999;274:22907-22910.
14. Husheem M,Nyman JK,Vaaraniemi J,Vaananen HK,Hentunen TA.Characterization of circulating human osteoclast progenitors: development of in vitro resorption assay.Calcif Tissue Int. 2005;76:222-230.
15. Hutagalung AH,Novick PJ.Role of Rab GTPases in membrane traffic and cell physiology.Physiol Rev. 2011;91:119-149.
16. Kaija H,Jia J,Lindqvist Y,Andersson G,Vihko P.Tartrate-resistant bone acid phosphatase: large-scale production and purification of the recombinant enzyme, characterization, and crystallization.J Bone Miner Res. 1999;14:424-430.
17. Kim J-M,Jeong D,Kang HK,Jung SY,Kang SS,Min B-M.Osteoclast precursors display dynamic metabolic shifts toward accelerated glucose metabolism at an early stage of RANKL-stimulated osteoclast differentiation.Cell Physiol Biochem. 2007;20:935-946.
18. Knowles HJ,Athanasou NA.Hypoxia-inducible factor is expressed in giant cell tumour of bone and mediates paracrine effects of hypoxia on monocyte-osteoclast differentiation via induction of VEGF.J Pathol. 2008;215:56-66.
19. Kohler K,Louvard D,Zahraoui A.Rab13 regulates PKA signaling during tight junction assembly.J Cell Biol. 2004;165:175-180.
20. Lakkakorpi P,Tuukkanen J,Hentunen T,Jarvelin K,Vaananen K.Organization of osteoclast microfilaments during the attachment to bone surface in vitro.J Bone Miner Res. 1989;4:817-825.
21. Lakkakorpi PT,Vaananen HK.Kinetics of the osteoclast cytoskeleton during the resorption cycle in vitro.J Bone Miner Res. 1991;6:817-826.
22. Livak KJ,Schmittgen TD.Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method.Methods. 2001;25:402-408.
23. Marzesco AM,Dunia I,Pandjaitan R,Recouvreur M,Dauzonne D,Benedetti EL,Louvard D,Zahraoui A.The small GTPase Rab13 regulates assembly of functional tight junctions in epithelial cells.Mol Biol Cell. 2002;13:1819-1831.
24. Morimoto R,Uehara S,Yatsushiro S,Juge N,Hua Z,Senoh S,Echigo N,Hayashi M,Mizoguchi T,Ninomiya T,Udagawa N,Omote H,Yamamoto A,Edwards RH,Moriyama Y.Secretion of L-glutamate from osteoclasts through transcytosis.EMBO J. 2006;25:4175-4186.
25. Morimoto S,Nishimura N,Terai T,Manabe S,Yamamoto Y,Shinahara W,Miyake H,Tashiro S,Shimada M,Sasaki T.Rab13 mediates the continuous endocytic recycling of occludin to the cell surface.J Biol Chem. 2005;280:2220-2228.
26. Mulari MT,Zhao H,Lakkakorpi PT,Vaananen HK.Osteoclast ruffled border has distinct subdomains for secretion and degraded matrix uptake.Traffic. 2003;4:113-125.
27. Nesbitt SA,Horton M.Traffiking of matrix collagens through bone-resorbing osteoclasts.Science. 1997;276:266-269.
28. Nokes RL,Fields IC,Collins RN,Fölsch H.Rab13 regulates membrane trafficking between TGN and recycling endosomes in polarized epithelial cells.J Cell Biol. 2008;182:845-853.
29. 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.110(Pt 15):. 1997;:1767-1780.
30. Pavlos NJ,Xu J,Riedel D,Yeoh JS,Teitelbaum SL,Papadimitriou JM,Jahn R,Ross FP,Zheng MH.Rab3D regulates a novel vesicular trafficking pathway that is required for osteoclastic bone resorption.Mol Cell Biol. 2005;25:5253-5269.
31. Reinholt FP,Widholm SM,Ek-Rylander B,Andersson G.Ultrastructural localization of a tartrate-resistant acid ATPase in bone.J Bone Miner Res. 1990;5:1055-1061.
32. Salo J,Lehenkari P,Mulari M,Metsikko K,Vaananen HK.Removal of osteoclast bone resorption products by transcytosis.Science. 1997;276:270-273.
33. Salo J,Metsikko K,Palokangas H,Lehenkari P,Vaananen HK.Bone-resorbing osteoclasts reveal a dynamic division of basal plasma membrane into two different domains. J Cell Sci.109(Pt 2):. 1996;:301-307.
34. Seabra MC,Mules EH,Hume AN.Rab GTPases, intracellular traffic and disease.Trends Mol Med. 2002;8:23-30.
35. Stenmark H.Rab GTPases as coordinators of vesicle traffic.Nat Rev Mol Cell Biol. 2009;10:513-525.
36. Sun Y,Bilan PJ,Liu Z,Klip A.Rab8A and Rab13 are activated by insulin and regulate GLUT4 translocation in muscle cells.Proc Natl Acad Sci U S A. 2010;107:19909-19914.
37. Sun Y,Buki KG,Ettala O,Vaaraniemi JP,Vaananen HK.Possible role of direct Rac1-Rab7 interaction in ruffled border formation of osteoclasts.J Biol Chem. 2005;280:32356-32361.
38. Taylor A,Rogers MJ,Tosh D,Coxon FP.A novel method for efficient generation of transfected human osteoclasts.Calcif Tissue Int. 2007;80:132-136.
39. Vaananen HK,Horton M.The osteoclast clear zone is a specialized cell-extracellular matrix adhesion structure.J Cell Sci. 1995;108 (Pt 8): 2729-2732.
40. 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;111:1305-1311.
41. Vaaraniemi J,Halleen JM,Kaarlonen K,Ylipahkala H,Alatalo SL,Andersson G,Kaija H,Vihko P,Vaananen HK.Intracellular machinery for matrix degradation in bone-resorbing osteoclasts.J Bone Miner Res. 2004;19:1432-1440.
42. Wasmeier C,Romao M,Plowright L,Bennett DC,Raposo G,Seabra MC.Rab38 and Rab32 control post-Golgi trafficking of melanogenic enzymes.J Cell Biol. 2006;175:271-281.
43. Williams JP,Blair HC,McDonald JM,McKenna MA,Jordan SE,Williford J,Hardy RW.Regulation of osteoclastic bone resorption by glucose.Biochem Biophys Res Commun. 1997;235:646-651.
44. Wixler V,Wixler L,Altenfeld A,Ludwig S,Goody RS,Itzen A.Identification and characterisation of novel Mss4-binding Rab GTPases.Biol Chem. 2011;392:239-248.
45. Wu X,Rao K,Bowers MB,Copeland NG,Jenkins NA,Hammer JA.Rab27a enables myosin Va-dependent melanosome capture by recruiting the myosin to the organelle.J Cell Sci. 2001;114:1091-1100.
46. Yamamoto Y,Nishimura N,Morimoto S,Kitamura H,Manabe S,Kanayama HO,Kagawa S,Sasaki T.Distinct roles of Rab3B and Rab13 in the polarized transport of apical, basolateral, and tight junctional membrane proteins to the plasma membrane.Biochem Biophys Res Commun. 2003;308:270-275.
47. Zahraoui A,Joberty G,Arpin M,Fontaine JJ,Hellio R,Tavitian A,Louvard D.A small rab GTPase is distributed in cytoplasmic vesicles in non polarized cells but colocalizes with the tight junction marker ZO-1 in polarized epithelial cells.J Cell Biol. 1994;124:101-115.
48. 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;293:1060-1065.
49. Zhao H,Laitala-Leinonen T,Parikka V,Vaananen HK.Downregulation of small GTPase Rab7 impairs osteoclast polarization and bone resorption.J Biol Chem. 2001;276:39295-39302.