Osteopetrosis mutation R444L causes endoplasmic reticulum retention and misprocessing of vacuolar H+-ATPase a3 subunit

Journal of Biological Chemistry

Volumn 287, Issue 32, 2012, Pages 26829-26839

  Bhargava, Ajay ^a   Voronov, Irina ^a   Wang, Yongqiang ^a   Glogauer, Michael ^a   Kartner, Norbert ^a   Manolson, Morris F ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BONE DENSITY; BONE DISEASE; ENDOPLASMIC RETICULUM; GREEN FLUORESCENT PROTEIN; LIMITED PROTEOLYSIS; MUTANT PROTEINS; MUTATION RESULTS; OSTEOCLAST DIFFERENTIATION; OSTEOCLASTOGENESIS; OSTEOPETROSIS; PROTEIN CONFORMATION; RETICULUM-ASSOCIATED DEGRADATION PATHWAYS; RETROVIRAL VECTORS; STEADY-STATE EXPRESSION; V-ATPASE; WILD TYPES;

BONE; CELL MEMBRANES; GLYCOPROTEINS; MAMMALS; PEDIATRICS; PROTEIN FOLDING;

PROTEINS;

ADENOSINE TRIPHOSPHATASE; ARGININE; GREEN FLUORESCENT PROTEIN; LEUCINE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE A3; RETROVIRUS VECTOR; UNCLASSIFIED DRUG;

ALBERS SCHOENBERG DISEASE; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; LYSOSOME; MALE; MISSENSE MUTATION; MOUSE; MUTANT; NONHUMAN; OSTEOCLAST; OSTEOCLASTOGENESIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; STEADY STATE; WILD TYPE;

ANIMALS; BASE SEQUENCE; CELL LINE; DNA PRIMERS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDOPLASMIC RETICULUM; GREEN FLUORESCENT PROTEINS; MACROPHAGES; MALE; MICE; MICE, INBRED C3H; MICROSCOPY, CONFOCAL; MUTATION; OSTEOCLASTS; OSTEOPETROSIS; PROTEIN FOLDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84864531105     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.345702     Document Type: Article

References (55)

1. 0). Bioessays 30, 1096-1109
2. Cipriano, D. J., Wang, Y., Bond, S., Hinton, A., Jefferies, K. C., Qi, J., and Forgac, M. (2008) Structure and regulation of the vacuolar ATPases. Biochim. Biophys. Acta 1777, 599-604
3. Saroussi, S., and Nelson, N. (2009) The little we know on the structure and machinery of V-ATPase. J. Exp. Biol. 212, 1604-1610
4. +-ATPases. An enzyme for all seasons. Pfluegers Arch./Eur. J. Physiol. 457, 581-587
5. Toei, M., Saum, R., and Forgac, M. (2010) Regulation and isoform function of the V-ATPases. Biochemistry 49, 4715-4723
6. Nordström, T., Rotstein, O. D., Romanek, R., Asotra, S., Heersche, J. N., Manolson, M. F., Brisseau, G. F., and Grinstein, S. (1995) Regulation of cytoplasmic pH in osteoclasts. Contribution of proton pumps and a proton-selective conductance. J. Biol. Chem. 270, 2203-2212
7. Wagner, C. A., Devuyst, O., Bourgeois, S., and Mohebbi, N. (2009) Regulated acid-base transport in the collecting duct. Pfluegers Arch./Eur. J. Physiol. 458, 137-156
8. Brown, D., Smith, P. J., and Breton, S. (1997) Role of V-ATPase-rich cells in acidification of the male reproductive tract. J. Exp. Biol. 200, 257-262 (Pubitemid 27126456)
9. Manolson, M. F., Yu, H., Chen, W., Yao, Y., Li, K., Lees, R. L., and Heersche, J. N. (2003) The a3 isoform of the 100-kDa V-ATPase subunit is highly but differentially expressed in large (≥10 nuclei) and small (≤5 nuclei) osteoclasts. J. Biol. Chem. 278, 49271-49278
10. Zhang, Z., Zheng, Y., Mazon, H., Milgrom, E., Kitagawa, N., Kish-Trier, E., Heck, A. J., Kane, P. M., and Wilkens, S. (2008) Structure of the yeast vacuolar ATPase. J. Biol. Chem. 283, 35983-35995
11. +-ATPase subunit Vph1p. J. Biol. Chem. 269, 14064-14074
12. +-ATPase. J. Biol. Chem. 267, 14294-14303
13. +-ATPase subunit a. J. Biol. Chem. 276, 40050-40054
14. +-ATPase subunit defective in an inherited form of distal renal tubular acidosis. J. Am. Soc. Nephrol. 14, 3027-3038
15. +-ATPase with the a3 isoform during osteoclast differentiation. J. Biol. Chem. 278, 22023-22030
16. Li, Y. P., Chen, W., Liang, Y., Li, E., and Stashenko, P. (1999) Atp6i-deficient mice exhibit severe osteopetrosis due to loss of osteoclast-mediated extracellular acidification. Nat. Genet. 23, 447-451
17. Scimeca, J. C., Franchi, A., Trojani, C., Parrinello, H., Grosgeorge, J., Robert, C., Jaillon, O., Poirier, C., Gaudray, P., and Carle, G. F. (2000) 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 26, 207-213 (Pubitemid 30101642)
18. Ochotny, N., Flenniken, A. M., Owen, C., Voronov, I., Zirngibl, R. A., Osborne, L. R., Henderson, J. E., Adamson, S. L., Rossant, J., Manolson, M. F., and Aubin, J. E. (2011) The V-ATPase a3 subunit mutation R740S is dominant-negative and results in osteopetrosis in mice. J. Bone Miner. Res. 26, 1484-1493
19. Nyman, J. K., and Väänänen, H. K. (2010) A rationale for osteoclast selectivity of inhibiting the lysosomal V-ATPase a3 isoform. Calcif. Tissue Int. 87, 273-283
20. Del Fattore, A., Cappariello, A., and Teti, A. (2008) Genetics, pathogenesis, and complications of osteopetrosis. Bone 42, 19-29
21. Phadke, S. R., Fischer, B., Gupta, N., Ranganath, P., Kabra, M., and Kornak, U. (2010) Novel mutations in Indian patients with autosomal recessive infantile malignant osteopetrosis. Indian J. Med. Res. 131, 508-514
22. Driessen, G. J., Gerritsen, E. J., Fischer, A., Fasth, A., Hop, W. C., Veys, P., Porta, F., Cant, A., Steward, C. G., Vossen, J. M., Uckan, D., and Friedrich, W. (2003) Long-term outcome of haematopoietic stem cell transplantation in autosomal recessive osteopetrosis. An EBMT report. Bone Marrow Transplant. 32, 657-663 (Pubitemid 37258621)
23. Fasth, A., and Porras, O. (1999) Human malignant osteopetrosis. Pathophysiology, management and the role of bone marrow transplantation. Pediatr. Transplant. 3, 102-107
24. Sobacchi, C., Frattini, A., Orchard, P., Porras, O., Tezcan, I., Andolina, M., Babul-Hirji, R., Baric, I., Canham, N., Chitayat, D., Dupuis-Girod, S., Ellis, I., Etzioni, A., Fasth, A., Fisher, A., Gerritsen, B., Gulino, V., Horwitz, E., Klamroth, V., Lanino, E., Mirolo, M., Musio, A., Matthijs, G., Nonomaya, S., Notarangelo, L. D., Ochs, H. D., Superti Furga, A., Valiaho, J., van Hove, J. L., Vihinen, M., Vujic, D., Vezzoni, P., and Villa, A. (2001) The mutational spectrum of human malignant autosomal recessive osteopetrosis. Hum. Mol. Genet. 10, 1767-1773 (Pubitemid 32899094)
25. Stover, E. H., Borthwick, K. J., Bavalia, C., Eady, N., Fritz, D. M., Rungroj, N., Giersch, A. B., Morton, C. C., Axon, P. R., Akil, I., Al-Sabban, E. A., Baguley, D. M., Bianca, S., Bakkaloglu, A., Bircan, Z., Chauveau, D., Clermont, M. J., Guala, A., Hulton, S. A., Kroes, H., Li Volti, G., Mir, S., Mocan, H., Nayir, A., Ozen, S., Rodriguez Soriano, J., Sanjad, S. A., Tasic, V., Taylor, C. M., Topaloglu, R., Smith, A. N., and Karet, F. E. (2002) Novel ATP6V1B1 and ATP6V0A4 mutations in autosomal recessive distal renal tubular acidosis with new evidence for hearing loss. J. Med. Genet. 39, 796-803 (Pubitemid 35346947)
26. Zou, K. H., Tuncali, K., and Silverman, S. G. (2003) Correlation and simple linear regression. Radiology 227, 617-622 (Pubitemid 36583011)
27. Collin-Osdoby, P., Yu, X., Zheng, H., and Osdoby, P. (2003) RANKL-mediated osteoclast formation from murine RAW 264.7 cells. Methods Mol. Med. 80, 153-166
28. Lee, J. H., Yu, W. H., Kumar, A., Lee, S., Mohan, P. S., Peterhoff, C. M., Wolfe, D. M., Martinez-Vicente, M., Massey, A. C., Sovak, G., Uchiyama, Y., Westaway, D., Cuervo, A. M., and Nixon, R. A. (2010) Lysosomal proteolysis and autophagy require presinilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 141, 1146-1158
29. Shin, J., Dunbrack, R. L., Jr., Lee, S., and Strominger, J. L. (1991) Signals for retention of transmembrane proteins in the endoplasmic reticulum studied with CD4 truncation mutants. Proc. Natl. Acad. Sci. U.S.A. 88, 1918-1922 (Pubitemid 21916338)
30. Cheung, J. C., and Reithmeier, R. A. (2007) Scanning N-glycosylation mutagenesis of membrane proteins. Methods 41, 451-459 (Pubitemid 46400528)
31. Zhang, F., Kartner, N., and Lukacs, G. L. (1998) Limited proteolysis as a probe for arrested conformational maturation of ΔF508 CFTR. Nat. Struct. Biol. 5, 180-183 (Pubitemid 28113747)
32. Toei, M., Toei, S., and Forgac, M. (2011) Definition of membrane topology and identification of residues important for transport in subunit a of the vacuolar ATPase. J. Biol. Chem. 286, 35176-35186
33. Cheng, S. H., Gregory, R. J., Marshall, J., Paul, S., Souza, D. W., White, G. A., O'Riordan, C. R., and Smith, A. E. (1990) Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 63, 827-834 (Pubitemid 120035055)
34. Sato, S., Ward, C. L., Krouse, M. E., Wine, J. J., and Kopito, R. R. (1996) Glycerol reverses the misfolding phenotype of the most common cystic fibrosis mutation. J. Biol. Chem. 271, 635-638 (Pubitemid 26034907)
35. +-ATPase from lysosomes for phagosomal acidification. J. Cell Sci. 122, 2504-2513
36. +-ATPase in the contractile vacuole complex and the endosomal pathway of Dictyostelium cells. J. Cell Sci. 115, 2893-2905
37. Blair, H. C., Teitelbaum, S. L., Ghiselli, R., and Gluck, S. (1989) Osteoclastic bone resorption by a polarized vacuolar proton pump. Science 245, 855-857 (Pubitemid 19223662)
38. +-ATPase type in the ruffled borders of osteoclasts. J. Cell Biol. 111, 1305-1311
39. Malhotra, J. D., and Kaufman, R. J. (2007) The endoplasmic reticulum and the unfolded protein response. Semin. Cell Dev. Biol. 18, 716-731 (Pubitemid 350138453)
40. +-ATPase from oat seedlings. Plant Cell 10, 119-130
41. Hill, K., and Cooper, A. A. (2000) Degradation of unassembled Vph1p reveals novel aspects of the yeast ER quality control system. EMBO J. 19, 550-561 (Pubitemid 30093728)
42. Hebert, D. N., and Molinari, M. (2007) In and out of the ER. Protein folding, quality control, degradation, and related human diseases. Physiol. Rev. 87, 1377-1408 (Pubitemid 350041473)
43. Chakrabarti, A., Chen, A. W., and Varner, J. D. (2011) A review of the mammalian unfolded protein response. Biotechnol. Bioeng. 108, 2777-2793
44. Ochotny, N., Van Vliet, A., Chan, N., Yao, Y., Morel, M., Kartner, N., von Schroeder, H. P., Heersche, J. N., and Manolson, M. F. (2006) Effects of human a3 and a4 mutations that result in osteopetrosis and distal renal tubular acidosis on yeast V-ATPase expression and activity. J. Biol. Chem. 281, 26102-26111 (Pubitemid 44401816)
45. Kawasaki-Nishi, S., Nishi, T., and Forgac, M. (2001) Arg-735 of the 100-kDa subunit a of the yeast V-ATPase is essential for proton translocation. Proc. Natl. Acad. Sci. U.S.A. 98, 12397-12402 (Pubitemid 33019957)
46. Partridge, A. W., Therien, A. G., and Deber, C. M. (2004) Missense mutations in transmembrane domains of proteins. Phenotypic propensity of polar residues for human disease. Proteins Struct. Funct. Bioinformat. 54, 648-656 (Pubitemid 38298784)
47. von Heijne, G. (1992) Membrane protein structure prediction. Hydrophobicity analysis and the positive inside rule. J. Mol. Biol. 225, 487-494
48. Lerch-Bader, M., Lundin, C., Kim, H., Nilsson, I., and von Heijne, G. (2008) Contribution of positively charged flanking residues to the insertion of transmembrane helices into the endoplasmic reticulum. Proc. Natl.Acad. Sci. U.S.A. 105, 4127-4132 (Pubitemid 351754346)
49. Vostrikov, V. V., Daily, A. E., Greathouse, D. V., and Koeppe, R. E. (2010) Charged or aromatic anchor residue dependence of transmembrane peptide tilt. J. Biol. Chem. 285, 31723-31730
50. Oǧur, G., Oǧur, E., Celasun, B., Basȩr, Ï., Ïmïrzalioǧlu, N., Öztürk, T., and Alemdaroǧlu, A. (1995) Prenatal diagnosis of autosomal recessive osteopetrosis, infantile type, by x-ray evaluation. Prenatal Diagn. 15, 477-481
51. Nakamura, I., Takahashi, N., Udagawa, N., Moriyama, Y., Kurokawa, T., Jimi, E., Sasaki, T., and Suda, T. (1997) Lack of vacuolar proton ATPase association with the cytoskeleton in osteoclasts of osteosclerotic (oc/oc) mice. FEBS Lett. 401, 207-212 (Pubitemid 27056117)
52. Dalemans, W., Barbry, P., Champigny, G., Jallat, S., Dott, K., Dreyer, D., Crystal, R. G., Pavirani, A., Lecocq, J. P., and Lazdunski, M. (1991) Altered chloride ion channel kinetics associated with the ΔF508 cystic fibrosis mutation. Nature 354, 526-528 (Pubitemid 21896832)
53. deCarvalho, A. C., Ndi, C. P., Tsopmo, A., Tane, P., Ayafor, J., Connolly, J. D., and Teem, J. L. (2002) A novel natural product compound enhances cAMP-regulated chloride conductance of cells expressing CFTRΔF508. Mol. Med. 8, 75-87 (Pubitemid 35013575)
54. Welch, W. J. (2004) Role in quality control pathways in human diseases involving protein misfolding. Semin. Cell Dev. Biol. 15, 31-38
55. Zhang, X., Garbett, K., Veeraraghavalu, K., Wilburn, B., Gilmore, R., Mirnics, K., and Sisodia, S. S. (2012) A role for presenilins in autophagy revisited: Normal acidification of lysosomes in cells lacking PSEN1 and PSEN2. J. Neurosci. 32, 8633-8648