The R740S mutation in the V-ATPase a3 subunit increases lysosomal pH, impairs NFATc1 translocation, and decreases in vitro osteoclastogenesis

Journal of Bone and Mineral Research

Volumn 28, Issue 1, 2013, Pages 108-118

  Voronov, Irina ^a   Ochotny, Noelle ^a   Jaumouillé, Valentin ^b   Owen, Celeste ^c   Manolson, Morris F ^a   Aubin, Jane E ^a,c,d  

^a UNIVERSITY OF TORONTO   (Canada)

^b HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^c MOUNT SINAI HOSPITAL   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

LYSOSOMAL pH; NFATc1; OSTEOCLAST; RCAN1; V ATPASE

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; CALCINEURIN; CATHEPSIN K; CHLOROQUINE; DENDRITIC CELL SPECIFIC TRANSMEMBRANE PROTEIN; MEMBRANE PROTEIN; OSTEOCLAST ASSOCIATED RECEPTOR; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BIOACCUMULATION; BONE MARROW CELL; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; GENOTYPE; IN VITRO STUDY; INHIBITION KINETICS; LYSOSOME; MOLECULAR DYNAMICS; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; OSTEOCLAST; OSTEOCLASTOGENESIS; PH; PROTEIN BLOOD LEVEL; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SUBUNIT; SIGNAL TRANSDUCTION; WILD TYPE;

AMINO ACID SUBSTITUTION; ANIMALS; BIOLOGICAL MARKERS; CALCINEURIN; GENE EXPRESSION REGULATION; HYDROGEN-ION CONCENTRATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYSOSOMES; MALE; MICE; MUSCLE PROTEINS; MUTATION; NFATC TRANSCRIPTION FACTORS; OSTEOCLASTS; OSTEOGENESIS; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84872856111     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.1727     Document Type: Article

References (39)

1. Boyle WJ, Simonet WS, Lacey DL,. Osteoclast differentiation and activation. Nature. 2003; 423 (6937): 337-42.
2. Takayanagi H,. The role of NFAT in osteoclast formation. Ann NY Acad Sci. 2007; 1116: 227-37.
3. Manolson MF, Yu H, Chen W, Yao Y, Li K, Lees RL, Heersche JN,. The a3 isoform of the 100-kDa V-ATPase subunit is highly but differentially expressed in large (>or = 10 nuclei) and small (
4. Toyomura T, Oka T, Yamaguchi C, Wada Y, Futai M,. Three subunit a isoforms of mouse vacuolar H(+)-ATPase. Preferential expression of the a3 isoform during osteoclast differentiation. J Biol Chem. 2000; 275 (12): 8760-5.
5. Goto T, Yamaza T, Tanaka T,. Cathepsins in the osteoclast. J Electron Microsc (Tokyo). 2003; 52 (6): 551-8.
6. Forgac M,. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat Rev Mol Cell Biol. 2007; 8 (11): 917-29.
7. Li YP, Chen W, Liang Y, Li E, Stashenko P,. Atp6i-deficient mice exhibit severe osteopetrosis due to loss of osteoclast-mediated extracellular acidification. Nat Genet. 1999; 23 (4): 447-51.
8. Toyomura T, Murata Y, Yamamoto A, Oka T, Sun-Wada GH, Wada Y, Futai M,. From lysosomes to the plasma membrane: localization of vacuolar-type H+ -ATPase with the a3 isoform during osteoclast differentiation. J Biol Chem. 2003; 278 (24): 22023-30.
9. Villa A, Guerrini MM, Cassani B, Pangrazio A, Sobacchi C,. Infantile malignant, autosomal recessive osteopetrosis: the rich and the poor. Calcif Tissue Int. 2009; 84 (1): 1-12.
10. Ochotny N, Flenniken AM, Owen C, Voronov I, Zirngibl RA, Osborne LR, Henderson JE, Adamson SL, Rossant J, Manolson MF, Aubin JE,. The V-ATPase a3 subunit mutation R740S is dominant negative and results in osteopetrosis in mice. J Bone Miner Res. 2011; 26 (7): 1484-93.
11. Scimeca JC, Franchi A, Trojani C, Parrinello H, Grosgeorge J, Robert C, Jaillon O, Poirier C, Gaudray P, Carle GF,. The gene encoding the mouse homologue of the human osteoclast-specific 116-kDa V-ATPase subunit bears a deletion in osteosclerotic (oc/oc) mutants. Bone. 2000; 26 (3): 207-13.
12. Leng XH, Manolson MF, Liu Q, Forgac M,. Site-directed mutagenesis of the 100-kDa subunit (Vph1p) of the yeast vacuolar (H+)-ATPase. J Biol Chem. 1996; 271 (37): 22487-93.
13. Steinberg BE, Huynh KK, Brodovitch A, Jabs S, Stauber T, Jentsch TJ, Grinstein S,. A cation counterflux supports lysosomal acidification. J Cell Biol. 2010; 189 (7): 1171-86.
14. Carraro-Lacroix LR, Jaumouille V, Fairn GD, Grinstein S,. A weak base-generating system suitable for selective manipulation of lysosomal pH. Traffic. 2011; 12 (11): 1490-500.
15. Komarova SV, Pereverzev A, Shum JW, Sims SM, Dixon SJ,. Convergent signaling by acidosis and receptor activator of NF-kappaB ligand (RANKL) on the calcium/calcineurin/NFAT pathway in osteoclasts. Proc Natl Acad Sci USA. 2005; 102 (7): 2643-8.
16. Ikeda F, Nishimura R, Matsubara T, Tanaka S, Inoue J, Reddy SV, Hata K, Yamashita K, Hiraga T, Watanabe T, Kukita T, Yoshioka K, Rao A, Yoneda T,. Critical roles of c-Jun signaling in regulation of NFAT family and RANKL-regulated osteoclast differentiation. J Clin Invest. 2004; 114 (4): 475-84.
17. Matsumoto M, Kogawa M, Wada S, Takayanagi H, Tsujimoto M, Katayama S, Hisatake K, Nogi Y,. Essential role of p38 mitogen-activated protein kinase in cathepsin K gene expression during osteoclastogenesis through association of NFATc1 and PU.1. J Biol Chem. 2004; 279 (44): 45969-79.
18. Kim Y, Sato K, Asagiri M, Morita I, Soma K, Takayanagi H,. Contribution of nuclear factor of activated T cells c1 to the transcriptional control of immunoreceptor osteoclast-associated receptor but not triggering receptor expressed by myeloid cells-2 during osteoclastogenesis. J Biol Chem. 2005; 280 (38): 32905-13.
19. Asagiri M, Sato K, Usami T, Ochi S, Nishina H, Yoshida H, Morita I, Wagner EF, Mak TW, Serfling E, Takayanagi H,. Autoamplification of NFATc1 expression determines its essential role in bone homeostasis. J Exp Med. 2005; 202 (9): 1261-9.
20. Hogan PG, Chen L, Nardone J, Rao A,. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 2003; 17 (18): 2205-32.
21. Sun L, Peng Y, Zaidi N, Zhu LL, Iqbal J, Yamoah K, Wang X, Liu P, Abe E, Moonga BS, Epstein S, Zaidi M,. Evidence that calcineurin is required for the genesis of bone-resorbing osteoclasts. Am J Physiol Renal Physiol. 2007; 292 (1): F285-91.
22. Arron JR, Winslow MM, Polleri A, Chang CP, Wu H, Gao X, Neilson JR, Chen L, Heit JJ, Kim SK, Yamasaki N, Miyakawa T, Francke U, Graef IA, Crabtree GR,. NFAT dysregulation by increased dosage of DSCR1 and DYRK1A on chromosome 21. Nature. 2006; 441 (7093): 595-600.
23. Egusa H, Doi M, Saeki M, Fukuyasu S, Akashi Y, Yokota Y, Yatani H, Kamisaki Y,. The small molecule harmine regulates NFATc1 and Id2 expression in osteoclast progenitor cells. Bone. 2011; 49 (2): 264-74.
24. Ishida N, Hayashi K, Hoshijima M, Ogawa T, Koga S, Miyatake Y, Kumegawa M, Kimura T, Takeya T,. Large scale gene expression analysis of osteoclastogenesis in vitro and elucidation of NFAT2 as a key regulator. J Biol Chem. 2002; 277 (43): 41147-56.
25. Lange AW, Molkentin JD, Yutzey KE,. DSCR1 gene expression is dependent on NFATc1 during cardiac valve formation and colocalizes with anomalous organ development in trisomy 16 mice. Dev Biol. 2004; 266 (2): 346-60.
26. Liu H, Wang P, Song W, Sun X,. Degradation of regulator of calcineurin 1 (RCAN1) is mediated by both chaperone-mediated autophagy and ubiquitin proteasome pathways. FASEB J. 2009; 23 (10): 3383-92.
27. Wakkach A, Mansour A, Dacquin R, Coste E, Jurdic P, Carle GF, Blin-Wakkach C,. Bone marrow microenvironment controls the in vivo differentiation of murine dendritic cells into osteoclasts. Blood. 2008; 112 (13): 5074-83.
28. Manolson MF, Wu B, Proteau D, Taillon BE, Roberts BT, Hoyt MA, Jones EW,. STV1 gene encodes functional homologue of 95-kDa yeast vacuolar H(+)-ATPase subunit Vph1p. J Biol Chem. 1994; 269 (19): 14064-74.
29. Nyman JK, Vaananen HK,. A rationale for osteoclast selectivity of inhibiting the lysosomal V-ATPase a3 isoform. Calcif Tissue Int. 2010; 87 (3): 273-83.
30. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy. 2008; 4 (2): 151-75.
31. Sobota JA, Back N, Eipper BA, Mains RE,. Inhibitors of the V0 subunit of the vacuolar H+-ATPase prevent segregation of lysosomal- and secretory-pathway proteins. J Cell Sci. 2009; 122 (Pt 19): 3542-53.
32. 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.
33. Beals CR, Sheridan CM, Turck CW, Gardner P, Crabtree GR,. Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science. 1997; 275 (5308): 1930-4.
34. Li H, Rao A, Hogan PG,. Interaction of calcineurin with substrates and targeting proteins. Trends Cell Biol. 2011; 21 (2): 91-103.
35. Crabtree GR, Schreiber SL,. SnapShot: Ca2+-calcineurin-NFAT signaling. Cell. 2009; 138 (1): 210.
36. Bhattacharyya S, Deb J, Patra AK, Thuy Pham DA, Chen W, Vaeth M, Berberich-Siebelt F, Klein-Hessling S, Lamperti ED, Reifenberg K, Jellusova J, Schweizer A, Nitschke L, Leich E, Rosenwald A, Brunner C, Engelmann S, Bommhardt U, Avots A, Muller MR, Kondo E, Serfling E,. NFATc1 affects mouse splenic B cell function by controlling the calcineurin-NFAT signaling network. J Exp Med. 2011; 208 (4): 823-839.
37. Cruciat CM, Ohkawara B, Acebron SP, Karaulanov E, Reinhard C, Ingelfinger D, Boutros M, Niehrs C,. Requirement of prorenin receptor and vacuolar H+-ATPase-mediated acidification for Wnt signaling. Science. 2010; 327 (5964): 459-63.
38. Katz SJ, Russell AS,. Re-evaluation of antimalarials in treating rheumatic diseases: re-appreciation and insights into new mechanisms of action. Curr Opin Rheumatol. 2011; 23 (3): 278-81.
39. Jang CH, Choi JH, Byun MS, Jue DM,. Chloroquine inhibits production of TNF-alpha, IL-1beta and IL-6 from lipopolysaccharide-stimulated human monocytes/macrophages by different modes. Rheumatology (Oxford). 2006; 45 (6): 703-10.