Fen Hu, Yali Zhao, Zhenhai Hui, Fulin Xing, Jianyu Yang, Imshik Lee, Xinzheng Zhang, Leiting Pan, Jingjun Xu. Regulation of intracellular Ca2+/CaMKII signaling by TRPV4 membrane translocation during osteoblastic differentiation[J]. Biophysics Reports, 2019, 5(5-6): 254-263. doi: 10.1007/s41048-019-00100-y
Citation: Fen Hu, Yali Zhao, Zhenhai Hui, Fulin Xing, Jianyu Yang, Imshik Lee, Xinzheng Zhang, Leiting Pan, Jingjun Xu. Regulation of intracellular Ca2+/CaMKII signaling by TRPV4 membrane translocation during osteoblastic differentiation[J]. Biophysics Reports, 2019, 5(5-6): 254-263. doi: 10.1007/s41048-019-00100-y

Regulation of intracellular Ca2+/CaMKII signaling by TRPV4 membrane translocation during osteoblastic differentiation

doi: 10.1007/s41048-019-00100-y
Funds:  Leiting Pan
  • Received Date: 10 June 2019
  • Publish Date: 31 December 2019
  • Bone constantly remodels between resorption by osteoclasts and formation by osteoblasts; therefore the functions of osteoblasts are pivotal for maintaining homeostasis of bone mass. Transient receptor potential vanilloid 4 (TRPV4), a type of mechanosensitive channel, has been reported to be a key regulator in bone remodeling. However, the relationship between TRPV4 and osteoblast function remains largely elusive. Only little is known about the spatial distribution change of TRPV4 during osteoblastic differentiation and related signal events. Based on three-dimensional super-resolution microscopy, our results clearly showed a different distribution of TRPV4 in undifferentiated and differentiated osteoblasts, which reflected the plasma membrane translocation of TRPV4 along with prolonged differentiation. GSK1016790A (GSK101), the most potent agonist of TRPV4, triggered rapid calcium entry and calmodulin-dependent protein kinase II (CaMKII) phosphorylation via TRPV4 activation in a differentiation-dependent manner, indicating that the abundance of TRPV4 at the cell surface resulting from differentiation may be related to the modulation of Ca2+ response and CaMKII activity. These data provide compelling evidences for the plasma membrane translocation of TRPV4 during osteoblastic differentiation as well as demonstrate the regulation of downstream Ca2+/CaMKII signaling.
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  • Abed E, Labelle D, Martineau C, Loghin A, Moreau R (2009)Expression of transient receptor potential (TRP) channels in human and murine osteoblast-like cells. Mol Membr Biol 26:146-158
    AbuZineh K, Joudeh LI, Al Alwan B, Hamdan SM, Merzaban JS, Habuchi S (2018) Microfluidics-based super-resolution microscopy enables nanoscopic characterization of blood stem cell rolling. Sci Adv 4:5304
    Blair HC, Larrouture QC, Li Y, Lin H, Beer-Stoltz D, Liu L, Tuan RS, Robinson LJ, Schlesinger PH, Nelson DJ (2017) Osteoblast differentiation and bone matrix formation in vivo and in vitro.Tissue Eng Part B 23:268-280
    Christensen AP, Corey DP (2007) TRP channels in mechanosensation:direct or indirect activation? Nat Rev Neurosci 8:510-521
    Crockett JC, Rogers MJ, Coxon FP, Hocking LJ, Helfrich MH (2011)Bone remodelling at a glance. J Cell Sci 124:991-998
    Cuajungco MP, Grimm C, Oshima K, D'hoedt D, Nilius B, Mensenkamp AR, Bindels RJ, Plomann M, Heller S (2006)PACSINs bind to the TRPV4 cation channel. PACSIN 3 modulates the subcellular localization of TRPV4. J Biol Chem 281:18753-18762
    Darby WG, Grace MS, Baratchi S, McIntyre P (2016) Modulation of TRPV4 by diverse mechanisms. Int J Biochem Cell Biol 78:217-228
    Echeverry S, Rodriguez MJ, Torres YP (2016) Transient receptor potential channels in microglia:roles in physiology and disease. Neurotox Res 30:467-478
    Ehrlich PJ, Lanyon LE (2002) Mechanical strain and bone cell function:a review. Osteoporos Int 13:688-700
    Ferrandiz-Huertas C, Mathivanan S, Wolf CJ, Devesa I, FerrerMontiel A (2014) Trafficking of ThermoTRP Channels.Membranes (Basel) 4:525-564
    Flockerzi V, Nilius B (2014) TRPs:truly remarkable proteins.Handb Exp Pharmacol 222:1-12
    Garcia-Elias A, Mrkonjić S, Jung C, Pardo-Pastor C, Vicente R, Valverde MA (2014) The TRPV4 channel. Handb Exp Pharmacol 222:293-319
    Guilak F, Leddy HA, Liedtke W (2010) Transient receptor potential vanilloid 4:the sixth sense of the musculoskeletal system? Ann N Y Acad Sci 1192:404-409
    Gundberg CM (2000) Biochemical markers of bone formation. Clin Lab Med 20:489-501
    Hu F, Pan L, Zhang K, Xing F, Wang X, Lee I, Zhang X, Xu J (2014)Elevation of extracellular Ca2+ induces store-operated calcium entry via calcium-sensing receptors:a pathway contributes to the proliferation of osteoblasts. PLoS One 9:e107217
    Huang B, Wang W, Bates M, Zhuang X (2008) Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319:810-813
    Kang SS, Shin SH, Auh CK, Chun J (2012) Human skeletal dysplasia caused by a constitutive activated transient receptor potential vanilloid 4 (TRPV4) cation channel mutation. Exp Mol Med 44:707-722
    Kassem M, Abdallah BM, Saeed H (2008) Osteoblastic cells:differentiation and trans-differentiation. Arch Biochem Biophys 473:183-187
    Katagiri T, Takahashi N (2002) Regulatory mechanisms of osteoblast and osteoclast differentiation. Oral Dis 8:147-159
    Leddy HA, McNulty AL, Guilak F, Liedtke W (2014) Unraveling the mechanism by which TRPV4 mutations cause skeletal dysplasias. Rare Dis 2:e962971
    Lieben L, Carmeliet G (2012) The involvement of TRP channels in bone homeostasis. Front Endocrinol (Lausanne) 20:99
    Long F (2011) Building strong bones:molecular regulation of the osteoblast lineage. Nat Rev Mol Cell Biol 13:27-38
    Loukin SH, Teng J, Kung C (2015) A channelopathy mechanism revealed by direct calmodulin activation of TrpV4. Proc Natl Acad Sci USA 112:9400-9405
    Marie PJ (2008) Transcription factors controlling osteoblastogenesis. Arch Biochem Biophys 473:98-105
    Masuyama R, Vriens J, Voets T, Karashima Y, Owsianik G, Vennekens R, Lieben L, Torrekens S, Moermans K, Vanden Bosch A, Bouillon R, Nilius B, Carmeliet G (2008) TRPV4-mediated calcium influx regulates terminal differentiation of osteoclasts. Cell Metab 8:257-265
    Masuyama R, Mizuno A, Komori H, Kajiya H, Uekawa A, Kitaura H, Okabe K, Ohyama K, Komori T (2012) Calcium/calmodulinsignaling supports TRPV4 activation in osteoclasts and regulates bone mass. J Bone Miner Res 27:1708-1721
    Maycas M, Esbrit P, Gortázar AR (2017) Molecular mechanisms in bone mechanotransduction. Histol Histopathol 32:751-760
    Meng G, Li C, Sun H, Lee I (2018) Multiple calcium patterns of rat osteoblasts under fluidic shear stress. J Orthop Res 36:2039-2051
    Nilius B, Vriens J, Prenen J, Droogmans G, Voets T (2004) TRPV4 calcium entry channel:a paradigm for gating diversity. Am J Physiol Cell Physiol 286:C195-C205
    O'Conor CJ, Griffin TM, Liedtke W, Guilak F (2013) Increased susceptibility of Trpv4-deficient mice to obesity and obesityinduced osteoarthritis with very high-fat diet. Ann Rheum Dis 72:300-304
    O'Conor CJ, Leddy HA, Benefield HC, Liedtke WB, Guilak F (2014) TRPV4-mediated mechanotransduction regulates the metabolic response of chondrocytes to dynamic loading. Proc Natl Acad Sci USA 111:1316-1321
    Pan L, Yan R, Li W, Xu K (2018) Super-resolution microscopy reveals the native ultrastructure of the erythrocyte cytoskeleton. Cell Rep 22:1151-1158
    Panupinthu N, Rogers JT, Zhao L, Solano-Flores LP, Possmayer F, Sims SM, Dixon SJ (2008) P2X7 receptors on osteoblasts couple to production of lysophosphatidic acid:a signaling axis promoting osteogenesis. J Cell Biol 181:859-871
    Raggatt LJ, Partridge NC (2010) Cellular and molecular mechanisms of bone remodeling. J Biol Chem 285:25103-25108
    Roh KH, Lillemeier BF, Wang F, Davis MM (2015) The coreceptor CD4 is expressed in distinct nanoclusters and does not colocalize with T-cell receptor and active protein tyrosine kinase p56lck. Proc Natl Acad Sci USA 112:E1604-E1613
    Suzuki T, Notomi T, Miyajima D, Mizoguchi F, Hayata T, Nakamoto T, Hanyu R, Kamolratanakul P, Mizuno A, Suzuki M, Ezura Y, Izumi Y, Noda M (2013) Osteoblastic differentiation enhances expression of TRPV4 that is required for calcium oscillation induced by mechanical force. Bone 54:172-178
    van der Eerden BC, Oei L, Roschger P, Fratzl-Zelman N, Hoenderop JG, van Schoor NM, Pettersson-Kymmer U, SchreudersKoedam M, Uitterlinden AG, Hofman A, Suzuki M, Klaushofer K, Ohlsson C, Lips PJ, Rivadeneira F, Bindels RJ, van Leeuwen JP (2013) TRPV4 deficiency causes sexual dimorphism in bone metabolism and osteoporotic fracture risk. Bone 57:443-454
    White JP, Cibelli M, Urban L, Nilius B, McGeown JG, Nagy I (2016)TRPV4:molecular conductor of a diverse orchestra. Physiol Rev 96:911-973
    Winslow MM, Pan M, Starbuck M, Gallo EM, Deng L, Karsenty G, Crabtree GR (2006) Calcineurin/NFAT signaling in osteoblasts regulates bone mass. Dev Cell 10:771-782
    Xu H, Fu Y, Tian W, Cohen DM (2006) Glycosylation of the osmoresponsive transient receptor potential channel TRPV4 on Asn-651 influences membrane trafficking. Am J Physiol Renal Physiol 290:F1103-F1109
    Yan Q, Lu Y, Zhou L, Chen J, Xu H, Cai M, Shi Y, Jiang J, Xiong W, Gao J, Wang H (2018) Mechanistic insights into GLUT1 activation and clustering revealed by super-resolution imaging. Proc Natl Acad Sci USA 115:7033-7038
    Zaidi M (2007) Skeletal remodeling in health and disease. Nat Med 13:791-801
    Zayzafoon M (2006) Calcium/calmodulin signaling controls osteoblast growth and differentiation. J Cell Biochem 97:56-70
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