TULA-2, a novel histidine phosphatase, regulates bone remodeling by modulating osteoclast function

Cellular and Molecular Life Sciences

Volumn 70, Issue 7, 2013, Pages 1269-1284

  Back, Steven H ^a   Adapala, Naga Suresh ^c   Barbe, Mary F ^a   Carpino, Nick C ^b   Tsygankov, Alexander Y ^a   Sanjay, Archana ^a,c  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Fc receptor; ITAM; PLC ; Syk; Tyrosine kinase

Indexed keywords

PHOSPHOLIPASE C GAMMA2; PROTEIN KINASE SYK; REGULATOR PROTEIN; T CELL UBIQUITIN LIGAND 2 PROTEIN; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MASS; BONE REMODELING; CELL COUNT; CELL DIFFERENTIATION; CELL FUNCTION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION REGULATION; HEMATOPOIETIC STEM CELL; IMMUNORECEPTOR TYROSINE BASED ACTIVATION MOTIF; IN VITRO STUDY; LONG BONE; MALE; MOUSE; NONHUMAN; OSTEOCLAST; OSTEOLYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATOR GENE; SIGNAL TRANSDUCTION; T CELL UBIQUITIN LIGAND 2 GENE;

ANIMALS; BONE DENSITY; BONE MARROW CELLS; BONE REMODELING; CELLS, CULTURED; HISTIDINE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OSTEOCLASTS; PHOSPHOPROTEIN PHOSPHATASES; PROTEIN TYROSINE PHOSPHATASES; RECEPTORS, ANTIGEN, T-CELL; STEM CELLS;

MUS;

EID: 84876688173     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-012-1203-2     Document Type: Article

References (49)

1. Teitelbaum SL, Ross FP (2003) Genetic regulation of osteoclast development and function. Nat Rev Genet 4:638-649 (Pubitemid 36917505)
2. Hunter T (1995) Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 80:225-236
3. Gil-Henn H, Destaing O, Sims NA, Aoki K, Alles N, Neff L, Sanjay A, Bruzzaniti A, De Camilli P, Baron R, Schlessinger J (2007) Defective microtubule-dependent podosome organization in osteoclasts leads to increased bone density in Pyk2(-/-) mice. J Cell Biol 178:1053-1064 (Pubitemid 47443326)
4. Soriano P, Montgomery C, Geske R, Bradley A (1991) Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64:693-702 (Pubitemid 121001157)
5. Granot-Attas S, Elson A (2008) Protein tyrosine phosphatases in osteoclast differentiation, adhesion, and bone resorption. Eur J Cell Biol 87:479-490
6. v mutant mice. Bone 25:261-267 (Pubitemid 29406051)
7. Chellaiah MA, Kuppuswamy D, Lasky L, Linder S (2007) Phosphorylation of a Wiskott-Aldrich syndrome protein-associated signal complex is critical in osteoclast bone resorption. J Biol Chem 282:10104-10116 (Pubitemid 47104634)
8. Chiusaroli R, Knobler H, Luxenburg C, Sanjay A, Granot-Attas S, Tiran Z, Miyazaki T, Harmelin A, Baron R, Elson A (2004) Tyrosine phosphatase epsilon is a positive regulator of osteoclast function in vitro and in vivo. Mol Biol Cell 15:234-244 (Pubitemid 38044959)
9. Carpino N, Kobayashi R, Zang H, Takahashi Y, Jou ST, Feng J, Nakajima H, Ihle JN (2002) Identification, cDNA cloning, and targeted deletion of p70, a novel, ubiquitously expressed SH3 domain-containing protein. Mol Cell Biol 22:7491-7500
10. Carpino N, Turner S, Mekala D, Takahashi Y, Zang H, Geiger TL, Doherty P, Ihle JN (2004) Regulation of ZAP-70 activation and TCR signaling by two related proteins, Sts-1 and Sts-2. Immunity 20:37-46 (Pubitemid 38134292)
11. Feshchenko EA, Smirnova EV, Swaminathan G, Teckchandani AM, Agrawal R, Band H, Zhang X, Annan RS, Carr SA, Tsygankov AY (2004) TULA: an SH3- and UBA-containing protein that binds to c-Cbl and ubiquitin. Oncogene 23:4690-4706 (Pubitemid 38859458)
12. Wattenhofer M, Shibuya K, Kudoh J, Lyle R, Michaud J, Rossier C, Kawasaki K, Asakawa S, Minoshima S, Berry A, Bonne-Tamir B, Shimizu N, Antonarakis SE, Scott HS (2001) Isolation and characterization of the UBASH3A gene on 21q22.3 encoding a potential nuclear protein with a novel combination of domains. Hum Genet 108:140-147 (Pubitemid 32215374)
13. Rigden DJ (2008) The histidine phosphatase superfamily: structure and function. Biochem J 409:333-348 (Pubitemid 351184952)
14. Tsygankov AY (2008) Multidomain STS/TULA proteins are novel cellular regulators. IUBMB Life 60:224-231
15. Tsygankov AY (2009) TULA-family proteins: an odd couple. Cell Mol Life Sci 66:2949-2952
16. Tsygankov AY (2012) TULA-family proteins: a new class of cellular regulators. J Cell Physiol 228(1):43-49
17. de Castro RO, Zhang J, Groves JR, Barbu EA, Siraganian RP (2012) Once phosphorylated, tyrosines in carboxyl terminus of protein-tyrosine kinase Syk interact with signaling proteins, including TULA-2, a negative regulator of mast cell degranulation. J Biol Chem 287:8194-8204
18. Agrawal R, Carpino N, Tsygankov A (2008) TULA proteins regulate activity of the protein tyrosine kinase Syk. J Cell Biochem 104(3):953-964 (Pubitemid 351830843)
19. Chen X, Ren L, Kim S, Carpino N, Daniel JL, Kunapuli SP, Tsygankov AY, Pei D (2010) Determination of the substrate specificity of protein-tyrosine phosphatase TULA-2 and identification of Syk as a TULA-2 substrate. J Biol Chem 285:31268-31276
20. Mikhailik A, Ford B, Keller J, Chen Y, Nassar N, Carpino N (2007) A phosphatase activity of Sts-1 contributes to the suppression of TCR signaling. Mol Cell 27:486-497 (Pubitemid 47161133)
21. Smirnova EV, Collingwood TS, Bisbal C, Tsygankova OM, Bogush M, Meinkoth JL, Henderson EE, Annan RS, Tsygankov AY (2008) TULA proteins bind to ABCE-1, a host factor of HIV-1 assembly, and inhibit HIV-1 biogenesis in a UBA-dependent fashion. Virology 372:10-23 (Pubitemid 351215458)
22. Collingwood TS, Smirnova EV, Bogush M, Carpino N, Annan RS, Tsygankov AY (2007) T-cell ubiquitin ligand affects cell death through a functional interaction with apoptosis-inducing factor, a key factor of caspase-independent apoptosis. J Biol Chem 282:30920-30928 (Pubitemid 350035216)
23. Thomas DH, Getz TM, Newman TN, Dangelmaier CA, Carpino N, Kunapuli SP, Tsygankov AY, Daniel JL (2010) A novel histidine tyrosine phosphatase, TULA-2, associates with Syk and negatively regulates GPVI signaling in platelets. Blood 116:2570-2578
24. Brennan T, Adapala NS, Barbe MF, Yingling V, Sanjay A (2011) Abrogation of Cbl-PI3K interaction increases bone formation and osteoblast proliferation. Calcif Tissue Int 89:396-410
25. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2:595-610
26. Miyazaki T, Takayanagi H, Isshiki M, Takahashi T, Okada M, Fukui Y, Oda H, Nakamura K, Hirai H, Kurokawa T, Tanaka S (2000) In vitro and in vivo suppression of osteoclast function by adenovirus vector-induced csk gene. J Bone Miner Res 15:41-51 (Pubitemid 30026931)
27. Miyazaki T, Katagiri H, Kanegae Y, Takayanagi H, Sawada Y, Yamamoto A, Pando MP, Asano T, Verma IM, Oda H, Nakamura K, Tanaka S (2000) Reciprocal role of ERK and NF-κB pathways in survival and activation of osteoclasts. J Cell Biol 148:333-342 (Pubitemid 30078245)
28. Menaa C, Kurihara N, Roodman GD (2000) CFU-GM-derived cells form osteoclasts at a very high efficiency. Biochem Biophys Res Commun 267:943-946 (Pubitemid 30099428)
29. Miyazaki T, Sanjay A, Neff L, Tanaka S, Horne WC, Baron R (2004) Src kinase activity is essential for osteoclast function. J Biol Chem 279:17660-17666 (Pubitemid 38560531)
30. Sanjay A, Miyazaki T, Itzstein C, Purev E, Horne WC, Baron R (2006) Identification and functional characterization of an Src homology domain 3 domain-binding site on Cbl. FEBS J 273:5442-5456 (Pubitemid 44772400)
31. Adapala NS, Barbe MF, Langdon WY, Nakamura MC, Tsygankov AY, Sanjay A (2010) The loss of Cbl-phosphatidylinositol 3-kinase interaction perturbs RANKL-mediated signaling, inhibiting bone resorption and promoting osteoclast survival. J Biol Chem 285:36745-36758
32. Arai F, Miyamoto T, Ohneda O, Inada T, Sudo T, Brasel K, Miyata T, Anderson DM, 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)
33. Jacquin C, Gran DE, Lee SK, Lorenzo JA, Aguila HL (2006) Identification of multiple osteoclast precursor populations in murine bone marrow. J Bone Miner Res (the official J Am Soc Bone Miner Res) 21:67-77 (Pubitemid 43023228)
34. Mocsai A, Ruland J, Tybulewicz VL (2010) The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat Rev Immunol 10:387-402
35. Faccio R, Zou W, Colaianni G, Teitelbaum SL, Ross FP (2003) High dose M-CSF partially rescues the Dap12-/- osteoclast phenotype. J Cell Biochem 90:871-883 (Pubitemid 37467103)
36. Mocsai A, Humphrey MB, Van Ziffle JA, Hu Y, Burghardt A, Spusta SC, Majumdar S, Lanier LL, Lowell CA, Nakamura MC (2004) The immunomodulatory adapter proteins DAP12 and Fc receptor gamma-chain (FcRgamma) regulate development of functional osteoclasts through the Syk tyrosine kinase. Proc Natl Acad Sci USA 101:6158-6163 (Pubitemid 38520544)
37. Zou W, Kitaura H, Reeve J, Long F, Tybulewicz VL, Shattil SJ, Ginsberg MH, Ross FP, Teitelbaum SL (2007) Syk, c-Src, the alphavbeta3 integrin, and ITAM immunoreceptors, in concert, regulate osteoclastic bone resorption. J Cell Biol 176:877-888 (Pubitemid 46425547)
38. Lupher ML, Rao N, Lill NL, Andoniou CE, Miyake S, Clark EA, Druker B, Band H (1998) Cbl-mediated negative regulation of the Syk tyrosine kinase. A critical role for Cbl phosphotyrosine-binding domain binding to Syk phosphotyrosine 323. J Biol Chem 273:35273-35281 (Pubitemid 29028235)
39. Rao N, Ghosh AK, Ota S, Zhou P, Reddi AL, Hakezi K, Druker BK, Wu J, Band H (2001) The non-receptor tyrosine kinase Syk is a target of Cbl-mediated ubiquitylation upon B-cell receptor stimulation. EMBO J 20:7085-7095 (Pubitemid 34062300)
40. Epple H, Cremasco V, Zhang K, Mao D, Longmore GD, Faccio R (2008) Phospholipase C gamma 2 modulates integrin signaling in the osteoclast by affecting the localization and activation of Src kinase. Mol Cell Biol 28:3610-3622 (Pubitemid 351732899)
41. Mocsai A, Zhou M, Meng F, Tybulewicz VL, Lowell CA (2002) Syk is required for integrin signaling in neutrophils. Immunity 16:547-558 (Pubitemid 34442579)
42. Koga T, Inui M, Inoue K, Kim S, Suematsu A, Kobayashi E, Iwata T, Ohnishi H, Matozaki T, Kodama T, Taniguchi T, Takayanagi H, Takai T (2004) Costimulatory signals mediated by the ITAM motif cooperate with RANKL for bone homeostasis. Nature 428:758-763 (Pubitemid 38508286)
43. Lacey DL, Timms E, Tan H-L, Kelley MJ, Dunstan CR, Burgess T, Elliott R, Colombero A, Elliott G, Scully S, Hsu H, Sullivan J, Hawkins N, Davy E, Capparelli C, Eli A, Qian Y-X, Kaufman S, Sarosi I, Shalhoub V, Senaldi G, Guo J, Delaney J, Boyle WJ (1998) Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93:165-176 (Pubitemid 28180851)
44. Simonet WS, Lacey DL, Dunstan CR, Kelley M, Chang M-S, Luthy R, Nguyen HQ, Wooden S, Bennett L, Boone T, Shimamoto G, DeRose M, Elliott R, Colombero A, Tan H-L, Trail G, Sullivan J, Davy E, Bucay N, Renshaw-Gegg L, Hughes TM, Hill D, Pattison W, Campbell P, Sander S, Van G, Tarpley J, Derby P, Lee R, Boyle WJ (1997) Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell 89:309-319 (Pubitemid 27199902)
45. Teitelbaum SL (2000) Bone resorption by osteoclasts. Science 289:1504-1508
46. Karsdal MA, Martin TJ, Bollerslev J, Christiansen C, Henriksen K (2007) Are nonresorbing osteoclasts sources of bone anabolic activity? J Bone Miner Res 22:487-494 (Pubitemid 47457424)
47. Kollet O, Dar A, Shivtiel S, Kalinkovich A, Lapid K, Sztainberg Y, Tesio M, Samstein RM, Goichberg P, Spiegel A, Elson A, Lapidot T (2006) Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med 12:657-664 (Pubitemid 43865234)
48. Kim HJ, Zhang K, Zhang L, Ross FP, Teitelbaum SL, Faccio R (2009) The Src family kinase, Lyn, suppresses osteoclastogenesis in vitro and in vivo. Proc Natl Acad Sci USA 106:2325-2330
49. Kim HJ, Warren JT, Kim SY, Chappel JC, DeSelm CJ, Ross FP, Zou W, Teitelbaum SL (2010) Fyn promotes proliferation, differentiation, survival and function of osteoclast lineage cells. J Cell Biochem 111:1107-1113