SLC4A2-mediated Cl-/HCO3- exchange activity is essential for calpain-dependent regulation of the actin cytoskeleton in osteoclasts

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 6, 2013, Pages 2163-2168

  Coury, Fabienne ^a,b,c   Zenger, Serhan ^b,c   Stewart, Andrew K ^b   Stephens, Sebastien ^b,c   Neff, Lynn ^b,c   Tsang, Kelly ^a   Shull, Gary E ^d   Alper, Seth L ^b   Baron, Roland ^b,c   Aliprantis, Antonios O ^a,b,e  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

^d UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BICARBONATE; CALPAIN; CHLORIDE; HYDROGEN POTASSIUM ADENOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; SOLUTE CARRIER FAMILY 4 ANION EXCHANGER MEMBER 2; UNCLASSIFIED DRUG;

ACID SECRETION; ACTIN FILAMENT; ALBERS SCHOENBERG DISEASE; ALKALINIZATION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANION EXCHANGE; ARTICLE; CELL FUNCTION; CELL MIGRATION; CELL PH; CELL SPREADING; CONTROLLED STUDY; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION;

ACTIN CYTOSKELETON; ANIMALS; ANION TRANSPORT PROTEINS; ANTIPORTERS; CALPAIN; CELLS, CULTURED; CHLORIDE-BICARBONATE ANTIPORTERS; HYDROGEN-ION CONCENTRATION; MICE; MICE, KNOCKOUT; MUTANT PROTEINS; OSTEOCLASTS; OSTEOPETROSIS;

EID: 84873467448     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1206392110     Document Type: Article

References (36)

1. Linder S, Aepfelbacher M (2003) Podosomes: Adhesion hot-spots of invasive cells. Trends Cell Biol 13(7):376-385.
2. Destaing O, Saltel F, Géminard JC, Jurdic P, Bard F (2003) Podosomes display actin turnover and dynamic self-organization in osteoclasts expressing actin-green fluorescent protein. Mol Biol Cell 14(2):407-416.
3. Luxenburg C, et al. (2007) The architecture of the adhesive apparatus of cultured osteoclasts: From podosome formation to sealing zone assembly. PLoS One 2(1):e179.
4. Saltel F, Chabadel A, Bonnelye E, Jurdic P (2008) Actin cytoskeletal organisation in osteoclasts: A model to decipher transmigration and matrix degradation. Eur J Cell Biol 87(8-9):459-468.
5. Destaing O, et al. (2005) A novel Rho-mDia2-HDAC6 pathway controls podosome patterning through microtubule acetylation in osteoclasts. J Cell Sci 118(Pt 13): 2901-2911.
6. Rousselle AV, Heymann D (2002) Osteoclastic acidification pathways during bone resorption. Bone 30(4):533-540.
7. Baron R, Neff L, Louvard D, Courtoy PJ (1985) Cell-mediated extracellular acidification and bone resorption: Evidence for a low pH in resorbing lacunae and localization of a 100-kD lysosomal membrane protein at the osteoclast ruffled border. J Cell Biol 101(6):2210-2222.
8. Teitelbaum SL, Ross FP (2003) Genetic regulation of osteoclast development and function. Nat Rev Genet 4(8):638-649.
9. Blair HC, Teitelbaum SL, Ghiselli R, Gluck S (1989) Osteoclastic bone resorption by a polarized vacuolar proton pump. Science 245(4920):855-857.
10. Teti A, et al. (1989) Cytoplasmic pH regulation and chloride/bicarbonate exchange in avian osteoclasts. J Clin Invest 83(1):227-233.
11. - anion exchanger SLC4A2 is required for proper osteoclast differentiation and function. Proc Natl Acad Sci USA 105(44):16934-16939.
12. Jansen ID, et al. (2009) Ae2(a, b)-deficient mice exhibit osteopetrosis of long bones but not of calvaria. FASEB J 23(10):3470-3481.
13. - exchanger Ae2 results in osteopetrosis in mice. Proc Natl Acad Sci USA 106(5):1638-1641.
14. Meyers SN, et al. (2010) A deletion mutation in bovine SLC4A2 is associated with osteopetrosis in Red Angus cattle. BMC Genomics 11:337.
15. - exchanger are achlorhydric. J Biol Chem 279(29):30531-30539.
16. Lyaruu DM, et al. (2008) The anion exchanger Ae2 is required for enamel maturation in mouse teeth. Matrix Biol 27(2):119-127.
17. + exchange activity in mineralizing osteoblasts. J Cell Physiol 226(6):1702-1712.
18. Alper SL (2009) Molecular physiology and genetics of Na+-independent SLC4 anion exchangers. J Exp Biol 212(Pt 11):1672-1683.
19. Nakamura T, et al. (2007) Estrogen prevents bone loss via estrogen receptor alpha and induction of Fas ligand in osteoclasts. Cell 130(5):811-823.
20. Stewart AK, Kurschat CE, Alper SL (2007) Role of nonconserved charged residues of the AE2 transmembrane domain in regulation of anion exchange by pH. Pflugers Arch 454(3):373-384.
21. Stewart AK, Kurschat CE, Vaughan-Jones RD, Shmukler BE, Alper SL (2007) Acute regulation of mouse AE2 anion exchanger requires isoform-specific amino acid residues from most of the transmembrane domain. J Physiol 584(Pt 1):59-73.
22. Stewart AK, Kurschat CE, Vaughan-Jones RD, Alper SL (2009) Putative re-entrant loop 1 of AE2 transmembrane domain has a major role in acute regulation of anion exchange by pH. J Biol Chem 284(10):6126-6139.
23. Zhao X, et al. (1998) pH dependency of mu-calpain and mcalpain activity assayed by casein zymography following traumatic brain injury in the rat. Neurosci Lett 247(1): 53-57.
24. Marzia M, et al. (2006) Calpain is required for normal osteoclast function and is downregulated by calcitonin. J Biol Chem 281(14):9745-9754.
25. Calle Y, Carragher NO, Thrasher AJ, Jones GE (2006) Inhibition of calpain stabilises podosomes and impairs dendritic cell motility. J Cell Sci 119(Pt 11):2375-2385.
26. Macpherson L, et al. (2012) Tyrosine phosphorylation of WASP promotes calpainmediated podosome disassembly. Haematologica 97(5):687-691.
27. Aliprantis AO, et al. (2008) NFATc1 in mice represses osteoprotegerin during osteoclastogenesis and dissociates systemic osteopenia from inflammation in cherubism. J Clin Invest 118(11):3775-3789.
28. Kühn R, Schwenk F, Aguet M, Rajewsky K (1995) Inducible gene targeting in mice. Science 269(5229):1427-1429.
29. Bronckers AL, et al. (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(4): 375-387.
30. Lakkakorpi PT, Väänänen HK (1996) Cytoskeletal changes in osteoclasts during the resorption cycle. Microsc Res Tech 33(2):171-181.
31. Gil-Henn H, et al. (2007) Defective microtubule-dependent podosome organization in osteoclasts leads to increased bone density in Pyk2(-/-) mice. J Cell Biol 178(6): 1053-1064.
32. McHugh KP, et al. (2000) Mice lacking beta3 integrins are osteosclerotic because of dysfunctional osteoclasts. J Clin Invest 105(4):433-440.
33. Soriano P, Montgomery C, Geske R, Bradley A (1991) Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64(4):693-702.
34. Ghosh S, Cox KH, Cox JV (1999) Chicken erythroid AE1 anion exchangers associate with the cytoskeleton during recycling to the Golgi. Mol Biol Cell 10(2):455-469.
35. 2+ proteases (calpain I and calpain II) purified concurrently by the same method from rat kidney. J Biol Chem 258(14):8883-8889.
36. Goll DE, Thompson VF, Li H, Wei W, Cong J (2003) The calpain system. Physiol Rev 83(3):731-801.