Ae2a,b-deficient mice exhibit osteopetrosis of long bones but not of calvaria

FASEB Journal

Volumn 23, Issue 10, 2009, Pages 3470-3481

  Jansen, Ineke D C ^a   Mardones, Pablo ^b   Lecanda, Fernando ^c   De Vries, Teun J ^a   Recalde, Sergio ^c   Hoeben, Kees A ^b   Schoenmaker, Ton ^a   Ravesloot, Jan Hindrik ^b   Van Borren, Marcel M G J ^b   Van Eijden, Theo M ^a   Bronckers, Antonius L J J ^a   Kellokumpu, Sakari ^d   Medina, Juan F ^c   Everts, Vincent ^a   Oude Elferink, Ronald P J ^b  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UNIVERSITY OF NAVARRA   (Spain)

^d UNIVERSITY OF OULU   (Finland)

Author keywords

Osteoclast; Osteoclastogenesis; Skull; Solute carriers; Tibia

Indexed keywords

ANTIPORTER; CALCIUM; CARRIER PROTEIN; COLLAGEN TYPE 1; MESSENGER RNA; PHOSPHATE; SLC4A4 PROTEIN; SODIUM INDEPENDENT CHLORIDE BICARBONATE ANION EXCHANGE PROTEIN 2; SODIUM INDEPENDENT CHLORIDE BICARBONATE ANION EXCHANGE PROTEIN 2A; SODIUM INDEPENDENT CHLORIDE BICARBONATE ANION EXCHANGE PROTEIN 2B1; SODIUM INDEPENDENT CHLORIDE BICARBONATE ANION EXCHANGE PROTEIN 2B2; UNCLASSIFIED DRUG;

ALBERS SCHOENBERG DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANION EXCHANGE; ARTICLE; BONE DEVELOPMENT; BONE MARROW CELL; BONE MARROW CULTURE; BONE STRENGTH; CALVARIA; CELL COUNT; CELL MEMBRANE; CELL PH; CELL STRUCTURE; CONTROLLED STUDY; FEMALE; GROWTH RETARDATION; IN VITRO STUDY; LONG BONE; MALE; MOUSE; MULTINUCLEAR CELL; NONHUMAN; OSTEOCLAST; OSTEOLYSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SKULL; WEIGHT REDUCTION;

ANIMALS; ANION TRANSPORT PROTEINS; ANTIPORTERS; BONE AND BONES; HYDROGEN-ION CONCENTRATION; MICE; MICE, KNOCKOUT; OSTEOCLASTS; OSTEOPETROSIS; SKULL;

MUS;

EID: 70349666550     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-122598     Document Type: Article

References (48)

1. Teitelbaum, S. L. (2000) Bone resorption by osteoclasts. Science 289, 1504-1508
2. Tolar, J., Teitelbaum, S. L., and Orchard, P. J. (2004) Osteopetrosis. N. Engl. J. Med. 351, 2839-2849
3. Teti, A., Blair, H. C., Teitelbaum, S. L., Kahn, A. J., Koziol, C., Konsek, J., Zambonin-Zallone, A., and Schlesinger, P. H. (1989) Cytoplasmic pH regulation and chloride/bicarbonate exchange in avian osteoclasts. J. Clin. Invest. 83, 227-233 (Pubitemid 19048428)
4. +-ATPase cause infantile malignant osteopetrosis. Hum. Mol. Genet. 9, 2059-2063
5. Kornak, U., Kasper, D., Bosl, M. R., Kaiser, E., Schweizer, M., Schulz, A., Friedrich, W., Delling, G., and Jentsch, T. J. (2001) Loss of the ClC-7 chloride channel leads to osteopetrosis in mice and man. Cell 104, 205-215 (Pubitemid 32174837)
6. - transporters. Pflügers Arch. 447, 495-509
7. - anion exchanger AE1. Biochemistry 39, 5527-5533
8. - exchanger binds carbonic anhydrase IV. J. Biol. Chem. 277, 25239-25246
9. Medina, J. F., Acin, A., and Prieto, J. (1997) Molecular cloning and characterization of the human AE2 anion exchanger (SLC4A2) gene. Genomics 39, 74-85 (Pubitemid 27057274)
10. Medina, J. F., Lecanda, J., Acin, A., Ciesielczyk, P., and Prieto, J. (2000) Tissue-specific N-terminal isoforms from overlapping alternate promoters of the human AE2 anion exchanger gene. Biochem. Biophys. Res. Commun. 267, 228-235 (Pubitemid 30072535)
11. Aranda, V., Martinez, I., Melero, S., Lecanda, J., Banales, J. M., Prieto, J., and Medina, J. F. (2004) Shared apical sorting of anion exchanger isoforms AE2a, AE2b1, and AE2b2 in primary hepatocytes. Biochem. Biophys. Res. Commun. 319, 1040-1046 (Pubitemid 38739424)
12. Lecanda, J., Urtasun, R., and Medina, J. F. (2000) Molecular cloning and genomic organization of the mouse AE2 anion exchanger gene. Biochem. Biophys. Res. Commun. 276, 117-124
13. - exchanger are encoded by mRNAs transcribed from alternative promoters. J. Biol. Chem. 271, 7835-7843
14. o sensitivity of AE2c1-mediated anion exchange reveals novel regulatory determinants in the AE2 N-terminal cytoplasmic domain. J. Biol. Chem. 281, 1885-1896
15. -/- mice. Am. J. Pathol. 169, 165-176
16. Medina, J. F., Recalde, S., Prieto, J., Lecanda, J., Saez, E., Funk, C. D., Vecino, P., van Roon, M. A., Ottenhoff, R., Bosma, P. J., Bakker, C. T., and Elferink, R. P. (2003) Anion exchanger 2 is essential for spermiogenesis in mice. Proc. Natl. Acad. Sci. U. S. A. 100, 15847-15852 (Pubitemid 38021078)
17. El Zohairy, A. A., De Gee, A. J., Mohsen, M. M., and Feilzer, A. J. (2003) Microtensile bond strength testing of luting cements to prefabricated CAD/CAM ceramic and composite blocks. Dent. Mater. 19, 575-583
18. Creemers, L. B., Jansen, D. C., van Veen-Reurings, A., van den Bos, T., and Everts, V. (1997) Microassay for the assessment of low levels of hydroxyproline. BioTechniques 22, 656-658
19. Hess, H. H., and Derr, J. E. (1975) Assay of inorganic and organic phosphorus in the 0.1-5 nanomole range. Anal. Biochem. 63, 607-613
20. Holappa, K., Suokas, M., Soininen, P., and Kellokumpu, S. (2001) Identification of the full-length AE2 (AE2a) isoform as the Golgi-associated anion exchanger in fibroblasts. J. Histochem. Cytochem. 49, 259-269 (Pubitemid 32113388)
21. De Bruijn, M. F., Slieker, W. A., van der Loo, J. C., Voerman, J. S., van Ewijk, W., and Leenen, P. J. (1994) Distinct mouse bone marrow macrophage precursors identified by differential expression of ER-MP12 and ER-MP20 antigens. Eur. J. Immunol. 24, 2279-2284
22. De Vries, T. J., Schoenmaker, T., Beertsen, W., van der Neut, R., and Everts, V. (2005) Effect of CD44 deficiency on in vitro and in vivo osteoclast formation. J. Cell. Biochem. 94, 954-966 (Pubitemid 41420256)
23. + pumps in intracellular pH regulation in neonatal rat osteoclasts. J. Gen. Physiol. 105, 177-208
24. Salo, J., Lehenkari, P., Mulari, M., Metsikko, K., and Vaananen, H. K. (1997) Removal of osteoclast bone resorption products by transcytosis. Science 276, 270-273 (Pubitemid 27172688)
25. 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
26. Lyaruu, D. M., Bronckers, A. L., Mulder, L., Mardones, P., Medina, J. F., Kellokumpu, S., Oude Elferink, R. P., and Everts, V. (2008) The anion exchanger Ae2 is required for enamel maturation in mouse teeth. Matrix Biol. 27, 119-127 (Pubitemid 351227380)
27. Bronckers, A. L., Lyaruu, D. M., Jansen, I. D., Medina, J. F., Kellokumpu, S., Hoeben, K. A., Gawenis, L. R., Oude-Elferink, R. P., and Everts, V. (2009) Localization and function of the anion exchanger Ae2 in developing teeth and orofacial bone in rodents. J. Exp. Zoolog. B Mol. Dev. Evol. 312B, 375-387
28. Arai, F., Miyamoto, T., Ohneda, O., Inada, T., Sudo, T., Brasel, K., Miyata, T., Anderson, D. M., and Suda, T. (1999) Commitment and differentiation of osteoclast precursor cells by the sequential expression of c-Fms and receptor activator of nuclear factor kappaB (RANK) receptors. J. Exp. Med. 190, 1741-1754 (Pubitemid 30013841)
29. Yamane, T., Kunisada, T., Yamazaki, H., Era, T., Nakano, T., and Hayashi, S. I. (1997) Development of osteoclasts from embryonic stem cells through a pathway that is c-fms but not c-kit dependent. Blood 90, 3516-3523 (Pubitemid 27473421)
30. Helfrich, M. H. (2003) Osteoclast diseases. Microsc. Res. Tech. 61, 514-532
31. Tondravi, M. M., McKercher, S. R., Anderson, K., Erdmann, J. M., Quiroz, M., Maki, R., and Teitelbaum, S. L. (1997) Osteopetrosis in mice lacking haematopoietic transcription factor PU.1. Nature 386, 81-84 (Pubitemid 27130924)
32. Kong, Y. Y., Yoshida, H., Sarosi, I., Tan, H. L., Timms, E., Capparelli, C., Morony, S., Oliveira-dos-Santos, A. J., Van, G., Itie, A., Khoo, W., Wakeham, A., Dunstan, C. R., Lacey, D. L., Mak, T. W., Boyle, W. J., and Penninger, J. M. (1999) OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 397, 315-323 (Pubitemid 29061638)
33. Thesingh, C. W., and Scherft, J. P. (1985) Fusion disability of embryonic osteoclast precursor cells and macrophages in the microphthalmic osteopetrotic mouse. Bone 6, 43-52
34. Soriano, P., Montgomery, C., Geske, R., and Bradley, A. (1991) Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64, 693-702 (Pubitemid 121001157)
35. Lomaga, M. A., Yeh, W. C., Sarosi, I., Duncan, G. S., Furlonger, C., Ho, A., Morony, S., Capparelli, C., Van, G., Kaufman, S., van der Heiden, A., Itie, A., Wakeham, A., Khoo, W., Sasaki, T., Cao, Z., Penninger, J. M., Paige, C. J., Lacey, D. L., Dunstan, C. R., Boyle, W. J., Goeddel, D. V., and Mak, T. W. (1999) TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev. 13, 1015-1024 (Pubitemid 29200984)
36. Borthwick, K. J., Kandemir, N., Topaloglu, R., Kornak, U., Bakkaloglu, A., Yordam, N., Ozen, S., Mocan, H., Shah, G. N., Sly, W. S., and Karet, F. E. (2003) A phenocopy of CAII deficiency: a novel genetic explanation for inherited infantile osteopetrosis with distal renal tubular acidosis. J. Med. Genet. 40, 115-121 (Pubitemid 36232816)
37. Sly, W. S., Hewett-Emmett, D., Whyte, M. P., Yu, Y. S., and Tashian, R. E. (1983) Carbonic anhydrase II deficiency identified as the primary defect in the autosomal recessive syndrome of osteopetrosis with renal tubular acidosis and cerebral calcification. Proc. Natl. Acad. Sci. U. S. A. 80, 2752-2756
38. Taranta, A., Migliaccio, S., Recchia, I., Caniglia, M., Luciani, M., De Rossi, G., Dionisi-Vici, C., Pinto, R. M., Francalanci, P., Boldrini, R., Lanino, E., Dini, G., Morreale, G., Ralston, S. H., Villa, A., Vezzoni, P., Del Principe, D., Cassiani, F., Palumbo, G., and Teti, A. (2003) Genotype-phenotype relationship in human ATP6i-dependent autosomal recessive osteopetrosis. Am. J. Pathol. 162, 57-68 (Pubitemid 36050039)
39. - exchangers in migrating renal epithelial cells. J. Gen. Physiol. 115, 599-608
40. Denker, S. P., and Barber, D. L. (2002) Ion transport proteins anchor and regulate the cytoskeleton. Curr. Opin. Cell Biol. 14, 214-220
41. Everts, V., Korper, W., Jansen, D. C., Steinfort, J., Lammerse, I., Heera, S., Docherty, A. J., and Beertsen, W. (1999) Functional heterogeneity of osteoclasts: matrix metalloproteinases participate in osteoclastic resorption of calvarial bone but not in resorption of long bone. FASEB J. 13, 1219-1230 (Pubitemid 29300367)
42. Perez-Amodio, S., Jansen, D. C., Schoenmaker, T., Vogels, I. M., Reinheckel, T., Hayman, A. R., Cox, T. M., Saftig, P., Beertsen, W., and Everts, V. (2006) Calvarial osteoclasts express a higher level of tartrate-resistant acid phosphatase than long bone osteoclasts and activation does not depend on cathepsin K or L activity. Calcif. Tissue. Int. 79, 245-254 (Pubitemid 44673718)
43. 2+ concentration. Pflügers Arch. 442, 718-728
44. - exchanger Ae2 results in osteopetrosis in mice. Proc. Natl. Acad. Sci. U. S. A. 106, 1638-1641
45. - anion exchanger SLC4A2 is required for proper osteoclast differentiation and function. Proc. Natl. Acad. Sci. U. S. A. 105, 16934-16939
46. - exchanger are achlorhydric. J. Biol. Chem. 279, 30531-30539
47. Samuelson, L. C., and Hinkle, K. L. (2003) Insights into the regulation of gastric acid secretion through analysis of genetically engineered mice. Annu. Rev. Physiol. 65, 383-400
48. a,b-deficient mice develop antimitochondrial antibodies and other features resembling primary biliary cirrhosis. Gastroenterology 134, 1482-1493