Purinergic signalling is required for calcium oscillations in migratory chondrogenic progenitor cells

Pflugers Archiv European Journal of Physiology

Volumn 467, Issue 2, 2015, Pages 429-442

  Matta, Csaba ^a   Fodor, János ^a   Miosge, Nicolai ^b   Takács, Roland ^a   Juhász, Tamás ^a   Rybaltovszki, Henrik ^a   Tóth, Adrienn ^a   Csernoch, László ^a   Zákány, Róza ^a  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Calcium oscillation; Chondrogenesis; Mesenchymal stem cell; Osteoarthritis; SOCE

Indexed keywords

CALCIUM CHANNEL; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; MEMBRANE PROTEIN; ORAI1 PROTEIN, HUMAN; PURINERGIC RECEPTOR; RYANODINE RECEPTOR; STIM1 PROTEIN, HUMAN; TUMOR PROTEIN;

ADULT STEM CELL; AGED; CALCIUM SIGNALING; CARTILAGE; CELL CULTURE; CYTOLOGY; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM;

ADULT STEM CELLS; AGED; CALCIUM CHANNELS; CALCIUM SIGNALING; CARTILAGE; CELLS, CULTURED; HEK293 CELLS; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; MEMBRANE PROTEINS; NEOPLASM PROTEINS; RECEPTORS, PURINERGIC; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 84922927078     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1529-8     Document Type: Article

References (55)

1. Bird GS, Hwang SY, Smyth JT, Fukushima M, Boyles RR, Putney JW Jr (2009) STIM1 is a calcium sensor specialized for digital signaling. Curr Biol 19(20):1724–1729. doi:10.1016/j.cub.2009.08.022
2. + release. FASEB J 16(10):1145–1150. doi:10.1096/fj.02-0037rev
3. Burnstock G (2007) Purine and pyrimidine receptors. Cell Mol Life Sci 64(12):1471–1483. doi:10.1007/s00018-007-6497-0
4. Bygrave FL, Benedetti A (1996) What is the concentration of calcium ions in the endoplasmic reticulum? Cell Calcium 19(6):547–551
5. Carroll SH, Ravid K (2013) Differentiation of mesenchymal stem cells to osteoblasts and chondrocytes: a focus on adenosine receptors. Expert Rev Mol Med 15:e1. doi:10.1017/erm.2013.2
6. Ciciarello M, Zini R, Rossi L, Salvestrini V, Ferrari D, Manfredini R, Lemoli RM (2013) Extracellular purines promote the differentiation of human bone marrow-derived mesenchymal stem cells to the osteogenic and adipogenic lineages. Stem Cells Dev 22(7):1097–1111. doi:10.1089/scd.2012.0432
7. D’Alimonte I, Nargi E, Lannutti A, Marchisio M, Pierdomenico L, Costanzo G, Iorio PD, Ballerini P, Giuliani P, Caciagli F, Ciccarelli R (2013) Adenosine A1 receptor stimulation enhances osteogenic differentiation of human dental pulp-derived mesenchymal stem cells via WNT signaling. Stem Cell Res 11(1):611–624. doi:10.1016/j.scr.2013.04.002
8. + response amplitude and duration. Nature 386(6627):855–858. doi:10.1038/386855a0
9. Ferrero ME (2009) A new approach to the inflammatory/autoimmune diseases. Recent Pat Antiinfect Drug Discov 4(2):108–113
10. Fodor J, Matta C, Juhasz T, Olah T, Gonczi M, Szijgyarto Z, Gergely P, Csernoch L, Zakany R (2009) Ionotropic purinergic receptor P2X4 is involved in the regulation of chondrogenesis in chicken micromass cell cultures. Cell Calcium 45(5):421–430. doi:10.1016/j.ceca.2009.02.004
11. Fodor J, Matta C, Olah T, Juhasz T, Takacs R, Toth A, Dienes B, Csernoch L, Zakany R (2013) Store-operated calcium entry and calcium influx via voltage-operated calcium channels regulate intracellular calcium oscillations in chondrogenic cells. Cell Calcium 54(1):1–16. doi:10.1016/j.ceca.2013.03.003
12. Gharibi B, Abraham AA, Ham J, Evans BA (2011) Adenosine receptor subtype expression and activation influence the differentiation of mesenchymal stem cells to osteoblasts and adipocytes. J Bone Miner Res 26(9):2112–2124. doi:10.1002/jbmr.424
13. i transients and oscillations in mouse fibroblasts are mediated by endogenously released ATP. J Biol Chem 270(9):4451–4456
14. + indicators with greatly improved fluorescence properties. J Biol Chem 260(6):3440–3450
15. Harper MT, Poole AW (2011) Store-operated calcium entry and non-capacitative calcium entry have distinct roles in thrombin-induced calcium signalling in human platelets. Cell Calcium 50(4):351–358. doi:10.1016/j.ceca.2011.06.005
16. Hoth M, Niemeyer BA (2013) The neglected CRAC proteins: Orai2, Orai3, and STIM2. Curr Top Membr 71:237–271. doi:10.1016/B978-0-12-407870-3.00010-X
17. Hu J, Qin K, Zhang Y, Gong J, Li N, Lv D, Xiang R, Tan X (2011) Downregulation of transcription factor Oct4 induces an epithelial-to-mesenchymal transition via enhancement of Ca2+ influx in breast cancer cells. Biochem Biophys Res Commun 411(4):786–791. doi:10.1016/j.bbrc.2011.07.025
18. Jacobson KA, Ivanov AA, de Castro S, Harden TK, Ko H (2009) Development of selective agonists and antagonists of P2Y receptors. Purinergic Signal 5(1):75–89. doi:10.1007/s11302-008-9106-2
19. Kapur N, Mignery GA, Banach K (2007) Cell cycle-dependent calcium oscillations in mouse embryonic stem cells. Am J Physiol Cell Physiol 292(4):C1510–C1518. doi:10.1152/ajpcell.00181.2006
20. Karlsson C, Dehne T, Lindahl A, Brittberg M, Pruss A, Sittinger M, Ringe J (2010) Genome-wide expression profiling reveals new candidate genes associated with osteoarthritis. Osteoarthritis Cartilage 18(4):581–592. doi:10.1016/j.joca.2009.12.002
21. Katebi M, Soleimani M, Cronstein BN (2009) Adenosine A2A receptors play an active role in mouse bone marrow-derived mesenchymal stem cell development. J Leukoc Biol 85(3):438–444. doi:10.1189/jlb.0908520
22. Kawano S, Otsu K, Kuruma A, Shoji S, Yanagida E, Muto Y, Yoshikawa F, Hirayama Y, Mikoshiba K, Furuichi T (2006) ATP autocrine/paracrine signaling induces calcium oscillations and NFAT activation in human mesenchymal stem cells. Cell Calcium 39(4):313–324. doi:10.1016/j.ceca.2005.11.008
23. +) exchanger and plasma membrane Ca(2+) pump induce fluctuations of membrane currents and potentials in human mesenchymal stem cells. Cell Calcium 34(2):145–156
24. +) signaling pathways in human mesenchymal stem cells. Cell Calcium 32(4):165–174
25. Koelling S, Kruegel J, Irmer M, Path JR, Sadowski B, Miro X, Miosge N (2009) Migratory chondrogenic progenitor cells from repair tissue during the later stages of human osteoarthritis. Cell Stem Cell 4(4):324–335. doi:10.1016/j.stem.2009.01.015
26. Kupzig S, Walker SA, Cullen PJ (2005) The frequencies of calcium oscillations are optimized for efficient calcium-mediated activation of Ras and the ERK/MAPK cascade. Proc Natl Acad Sci U S A 102(21):7577–7582. doi:10.1073/pnas.0409611102
27. + entry into mouse skeletal muscle fibres. J Physiol 533(1):185–199
28. Kwon HJ (2012) Extracellular ATP signaling via P2X(4) receptor and cAMP/PKA signaling mediate ATP oscillations essential for prechondrogenic condensation. J Endocrinol 214(3):337–348. doi:10.1530/JOE-12-0131
29. Loredo GA, Benton HP (1998) ATP and UTP activate calcium-mobilizing P2U-like receptors and act synergistically with interleukin-1 to stimulate prostaglandin E2 release from human rheumatoid synovial cells. Arthritis Rheum 41(2):246–255. doi:10.1002/1529-0131(199802)41:2<246::AID-ART8>3.0.CO;2-I
30. Lorenzo P, Bayliss MT, Heinegard D (2004) Altered patterns and synthesis of extracellular matrix macromolecules in early osteoarthritis. Matrix Biol 23(6):381–391. doi:10.1016/j.matbio.2004.07.007
31. Mankin HJ, Lippiello L (1970) Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. J Bone Joint Surg Am 52(3):424–434
32. Martel-Pelletier J, Boileau C, Pelletier JP, Roughley PJ (2008) Cartilage in normal and osteoarthritis conditions. Best Pract Res Clin Rheumatol 22(2):351–384. doi:10.1016/j.berh.2008.02.001
33. + concentration exhibits a characteristic temporal pattern during in vitro cartilage differentiation: a possible regulatory role of calcineurin in Ca-signalling of chondrogenic cells. Cell Calcium 44(3):310–323. doi:10.1016/j.ceca.2007.12.010
34. Matta C, Mobasheri A (2014) Regulation of chondrogenesis by protein kinase C: emerging new roles in calcium signalling. Cell Signal. doi:10.1016/j.cellsig.2014.01.011
35. Matta C, Zakany R (2013) Calcium signalling in chondrogenesis: implications for cartilage repair. Front Biosci 5:305–324, Schol Ed
36. Mignen O, Thompson JL, Shuttleworth TJ (2009) The molecular architecture of the arachidonate-regulated Ca2 + -selective ARC channel is a pentameric assembly of Orai1 and Orai3 subunits. J Physiol 587(17):4181–4197. doi:10.1113/jphysiol.2009.174193
37. + signals by differential expression of IP3 receptor subtypes. EMBO J 18(5):1303–1308. doi:10.1093/emboj/18.5.1303
38. Mobasheri A, Henrotin Y (2010) Identification, validation and qualification of biomarkers for osteoarthritis in humans and companion animals: mission for the next decade. Vet J 185(2):95–97. doi:10.1016/j.tvjl.2010.05.026
39. Muramatsu S, Wakabayashi M, Ohno T, Amano K, Ooishi R, Sugahara T, Shiojiri S, Tashiro K, Suzuki Y, Nishimura R, Kuhara S, Sugano S, Yoneda T, Matsuda A (2007) Functional gene screening system identified TRPV4 as a regulator of chondrogenic differentiation. J Biol Chem 282(44):32158–32167. doi:10.1074/jbc.M706158200
40. Nguyen C, Lieberherr M, Bordat C, Velard F, Come D, Liote F, Ea HK (2012) Intracellular calcium oscillations in articular chondrocytes induced by basic calcium phosphate crystals lead to cartilage degradation. Osteoarthritis Cartilage 20(11):1399–1408. doi:10.1016/j.joca.2012.07.017
41. Picher M, Graff RD, Lee GM (2003) Extracellular nucleotide metabolism and signaling in the pathophysiology of articular cartilage. Arthritis Rheum 48(10):2722–2736. doi:10.1002/art.11289
42. Piirainen H, Ashok Y, Nanekar RT, Jaakola VP (2011) Structural features of adenosine receptors: from crystal to function. Biochim Biophys Acta 1808(5):1233–1244. doi:10.1016/j.bbamem.2010.05.021
43. Ralevic V, Burnstock G (1998) Receptors for purines and pyrimidines. Pharmacol Rev 50(3):413–492
44. Ramage L, Martel MA, Hardingham GE, Salter DM (2008) NMDA receptor expression and activity in osteoarthritic human articular chondrocytes. Osteoarthritis Cartilage 16(12):1576–1584. doi:10.1016/j.joca.2008.04.023
45. Rosenthal AK, Hempel D, Kurup IV, Masuda I, Ryan LM (2011) Purine receptors modulate chondrocyte extracellular inorganic pyrophosphate production. Osteoarthritis Cartilage 18(11):1496–1501. doi:10.1016/j.joca.2010.08.004
46. Ryzhov S, Goldstein AE, Novitskiy SV, Blackburn MR, Biaggioni I, Feoktistov I (2012) Role of A2B adenosine receptors in regulation of paracrine functions of stem cell antigen 1-positive cardiac stromal cells. J Pharmacol Exp Ther 341(3):764–774. doi:10.1124/jpet.111.190835
47. Sauer H, Hofmann C, Wartenberg M, Wobus AM, Hescheler J (1998) Spontaneous calcium oscillations in embryonic stem cell-derived primitive endodermal cells. Exp Cell Res 238(1):13–22. doi:10.1006/excr.1997.3809
48. Shih YR, Hwang Y, Phadke A, Kang H, Hwang NS, Caro EJ, Nguyen S, Siu M, Theodorakis EA, Gianneschi NC, Vecchio KS, Chien S, Lee OK, Varghese S (2014) Calcium phosphate-bearing matrices induce osteogenic differentiation of stem cells through adenosine signaling. Proc Natl Acad Sci U S A 111(3):990–995. doi:10.1073/pnas.1321717111
49. Stout CE, Costantin JL, Naus CC, Charles AC (2002) Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 277(12):10482–10488. doi:10.1074/jbc.M109902200
50. + oscillations in human bone marrow mesenchymal stem cells. J Cell Mol Med 15(12):2684–2696. doi:10.1111/j.1582-4934.2011.01263.x
51. Tian M, Duan Y, Duan X (2010) Chloride channels regulate chondrogenesis in chicken mandibular mesenchymal cells. Arch Oral Biol 55(12):938–945. doi:10.1016/j.archoralbio.2010.08.005
52. Varani K, De Mattei M, Vincenzi F, Tosi A, Targa M, Masieri FF, Pellati A, Massari L, Borea PA (2010) P2X(1) and P2X(3) purinergic receptors differentially modulate the inflammatory response in human osteoarthritic synovial fibroblasts. Cell Physiol Biochem 25(2-3):325–336. doi:10.1159/000276565
53. Varga Z, Juhasz T, Matta C, Fodor J, Katona E, Bartok A, Olah T, Sebe A, Csernoch L, Panyi G, Zakany R (2011) Switch of voltage-gated K + channel expression in the plasma membrane of chondrogenic cells affects cytosolic Ca2 + -oscillations and cartilage formation. PLoS One 6(11):e27957. doi:10.1371/journal.pone.0027957
54. Zhang S, Fritz N, Ibarra C, Uhlen P (2011) Inositol 1,4,5-trisphosphate receptor subtype-specific regulation of calcium oscillations. Neurochem Res 36(7):1175–1185. doi:10.1007/s11064-011-0457-7
55. Zippel N, Limbach CA, Ratajski N, Urban C, Luparello C, Pansky A, Kassack MU, Tobiasch E (2012) Purinergic receptors influence the differentiation of human mesenchymal stem cells. Stem Cells Dev 21(6):884–900. doi:10.1089/scd.2010.0576