Purinergic receptors influence the differentiation of human mesenchymal stem cells

Stem Cells and Development

Volumn 21, Issue 6, 2012, Pages 884-900

  Zippel, Nina ^a   Limbach, Christian Andreas ^a   Ratajski, Nadine ^a   Urban, Christian ^b   Luparello, Claudio ^c   Pansky, Andreas ^a   Kassack, Matthias Ullrich ^b   Tobiasch, Edda ^a  

^a BONN RHEIN SIEG UNIVERSITY OF APPLIED SCIENCES   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UNIVERSITY OF PALERMO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

PURINERGIC P2 RECEPTOR; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2X2 RECEPTOR; PURINERGIC P2X3 RECEPTOR; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X5 RECEPTOR; PURINERGIC P2X6 RECEPTOR; PURINERGIC P2X7 RECEPTOR; PURINERGIC P2Y1 RECEPTOR; PURINERGIC P2Y11 RECEPTOR; PURINERGIC P2Y12 RECEPTOR; PURINERGIC P2Y13 RECEPTOR; PURINERGIC P2Y2 RECEPTOR; PURINERGIC P2Y4 RECEPTOR; PURINERGIC P2Y6 RECEPTOR;

ADIPOGENESIS; ADIPOSE DERIVED STEM CELL; ADULT; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL FATE; DOWN REGULATION; FEMALE; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADULT STEM CELLS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; HUMANS; MESENCHYMAL STEM CELLS; RECEPTORS, PURINERGIC; RECEPTORS, PURINERGIC P2;

EID: 84859401064     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2010.0576     Document Type: Article

References (91)

1. Caplan AI. (1991). Mesenchymal stem cells. J Orthop Res 9:641-650.
2. Pittenger MF, AM Mackay, SC Beck, RK Jaiswal, R Douglas, JD Mosca, MA Moorman, DW Simonetti, S Craig and DR Marshak. (1999). Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147.
3. Jiang Y, BN Jahagirdar, RL Reinhardt, RE Schwartz, CD Keene, XR Ortiz-Gonzalez, M Reyes, T Lenvik, T Lund, et al. (2002). Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41-49.
4. Barry FP and JM Murphy. (2004). Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol 36:568-584.
5. Wagner W, F Wein, A Seckinger, M Frankhauser, U Wirkner, U Krause, J Blake, C Schwager, V Eckstein, et al. (2005). Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 33:1402-1416.
6. Kern S, H Eichler, J Stoeve, H Kluter and K Bieback. (2006). Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24:1294-1301.
7. Lee RH, B Kim, I Choi, H Kim, HS Choi, K Suh, YC Bae and JS Jung. (2004). Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell Physiol Biochem 14:311-324.
8. De Ugarte DA, K Morizono, A Elbarbary, Z Alfonso, PA Zuk, M Zhu, JL Dragoo, P Ashjian, B Thomas, et al. (2003). Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 174:101-109.
9. Morsczeck C, TE Reichert, F Vollner, T Gerlach and O Driemel. (2007). The state of the art in human dental stem cell research. Mund Kiefer Gesichtschir 11:259-266.
10. Haddouti E-M, M Skroch, N Zippel, C Müller, B Birova, A Pansky, C Kleinfeld, M Winter and E Tobiasch. (2009). Human dental follicle precursor cells of wisdom teeth: isolation and differentiation towards osteoblasts for implants with and without scaffolds. Mater Sci Eng Tech 40: 732-737.
11. Abbracchio MP, G Burnstock, J-M Boeynaems, EA Barnard, JL Boyer, C Kennedy, GE Knight, M Fumagalli, C Gachet, KA Jacobson and GA Weisman. (2006). International Union of Pharmacology LVIII: update on the p2y g proteincoupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol Rev 58: 281-341.
12. Ralevic V and G Burnstock. (1998). Receptors for purines and pyrimidines. Pharmacol Rev 50:413-492.
13. Abbracchio MP and G Burnstock (1994). Purinoceptors: are there families of P2X and P2Y purinoceptors? Pharmacol Ther 64:445-475.
14. Khakh BS, G Burnstock, C Kennedy, BF King, RA North, P Seguela, M Voigt and PPA Humphrey. (2001). International Union of Pharmacology. XXIV. Current status of the nomenclature and properties of P2X receptors and their subunits. Pharmacol Rev 53:107-118.
15. Burnstock G. (2006). Purinergic signalling. Br J Pharmacol 147:S172-S181.
16. von Kügelgen I and A Wetter. (2000). Molecular pharmacology of P2Y-receptors. Naunyn Schmiedebergs Arch Pharmacol 362:310-323.
17. Burnstock G and G Knight. (2004). Cellular distribution and functions of P2 receptor subtypes in different systems. Int Rev Cytol 240:31-304.
18. Burnstock G. (2006). Pathophysiology and therapeutic potential of purinergic signaling. Pharmacol Rev 58:58-86.
19. Halperin ML, ML Mak and WM Taylor. (1978). Control of glucose transport in adipose tissue of the rat: role of insulin, ATP and intracellular metabolites. Can J Biochem 56:708-712.
20. Schmidt M and G Lõffler. (1998). Induction of aromatase activity in human adipose tissue stromal cells by extracellular nucleotides. Eur J Biochem 252:147-154.
21. Lee H, D-J Jun, B-C Suh, B-H Choi, J-H Lee, M-S Do, B-S Suh, H Ha and K-T Kim. (2005). Dual roles of P2 purinergic receptors in insulin-stimulated leptin production and lipolysis in differentiated rat white adipocytes. J Biol Chem 280:28556-28563.
22. Hashimoto N, FW Robinson, Y Shibata, JE Flanagan and T Kono. (1987). Diversity in the effects of extracellular ATP and adenosine on the cellular processing and physiologic actions of insulin in rat adipocytes. J Biol Chem 262:15026-15032.
23. Tamura S, RE Dubler and J Larner. (1983). Stimulation of maximal intracellular insulin action on glycogen synthase by preincubation of adipocytes with adenosine 5¢-triphosphate. J Biol Chem 258:719-724.
24. Burnstock G and TR Arnett. (2007). Nucleotides and Regulation of Bone Cell Function. Taylor & Francis Group, Boca Raton, FL.
25. Hoebertz A, A Townsend-Nicholson, R Glass, G Burnstock and TR Arnett. (2000). Expression of P2 receptors in bone and cultured bone cells. Bone 27:503-510.
26. Ke HZ, H Qi, AF Weidema, Q Zhang, N Panupinthu, DT Crawford, WA Grasser, VM Paralkar, M Li, et al. (2003). Deletion of the P2X7 nucleotide receptor reveals its regulatory roles in bone formation and resorption. Mol Endocrinol 17:1356-1367.
27. Li J, D Liu, HZ Ke, RL Duncan and CH Turner. (2005). The P2X7 nucleotide receptor mediates skeletal mechanotransduction. J Biol Chem 280:42952-42959.
28. Hoebertz A, S Mahendran, G Burnstock and TR Arnett. (2002). ATP and UTP at low concentrations strongly inhibit bone formation by osteoblasts: a novel role for the P2Y1 and 2 receptor in bone remodeling. J Cell Biochem 86: 413-419.
29. Heo JS and HJ Han. (2006). ATP stimulates mouse embryonic stem cell proliferation via protein kinase C, phosphatidylinositol 3-kinase/Akt, and mitogen-activated protein kinase signaling pathways. Stem Cells 24:2637-2648.
30. Kawano S, K Otsu, A Kuruma, S Shoji, E Yanagida, Y Muto, F Yoshikawa, Y Hirayama, K Mikoshiba and T Furuichi. (2006). ATP autocrine/paracrine signaling induces calcium oscillations and NFAT activation in human mesenchymal stem cells. Cell Calcium 39:313-324.
31. Wang L, SE Jacobsen, A Bengtsson and D Erlinge. (2004). P2 receptor mRNA expression profiles in human lymphocytes, monocytes and CD34 + stem and progenitor cells. BMC Immunol 5:16.
32. Sak K, J-M Boeynaems and H Everaus. (2003). Involvement of P2Y receptors in the differentiation of haematopoietic cells. J Leukoc Biol 73:442-447.
33. Lemoli RM, D Ferrari,MFogli, L Rossi, C Pizzirani, S Forchap, P Chiozzi, D Vaselli, F Bertolini, et al. (2004). Extracellular nucleotides are potent stimulators of human hematopoietic stem cells in vitro and in vivo. Blood 104:1662-1670.
34. Rossi L, R Manfredini, F Bertolini, D Ferrari, M Fogli, R Zini, S Salati, V Salvestrini, S Gulinelli, et al. (2007). The extracellular nucleotide UTP is a potent inducer of hematopoietic stem cell migration. Blood 109:533-542.
35. Ryu JK, HB Choi, K Hatori, RL Heisel, SL Pelech, JG McLarnon and SU Kim. (2003). Adenosine triphosphate induces proliferation of human neural stem cells: role of calcium and p70 ribosomal protein S6 kinase. J Neurosci Res 72:352-362.
36. Arthur DB, K Akassoglou and PA Insel. (2005). P2Y2 receptor activates nerve growth factor/TrkA signaling to enhance neuronal differentiation. Proc Natl Acad Sci U S A 102:19138-19143.
37. Mishra SK, N Braun and V Shukla. (2006). Extracellular nucleotide signalling in adult neural stem cells: synergism with growth factor-mediated cellular proliferation. Development 133:675-684.
38. Lin JHC, T Takano, G Arcuino, X Wang, F Hu, Z Darzynkiewicz, M Nunes, SA Goldman and M Nedergaard. (2007). Purinergic signaling regulates neural progenitor cell expansion and neurogenesis. Dev Biol 302:356-366.
39. Omatsu-Kanbe M, K Inoue, Y Fujii, T Yamamoto, T Isono, N Fujita and H Matsuura. (2006). Effect of ATP on preadipocyte migration and adipocyte differentiation by activating P2Y receptors in 3T3-L1 cells. Biochem J 393:171-180.
40. Coppi E, AM Pugliese, S Urbani, A Melani, E Cerbai, B Mazzanti, A Bosi, R Saccardi and F Pedata. (2007). ATP modulates cell proliferation and elicits two different electrophysiological responses in human mesenchymal stem cells. Stem Cells 25:1840-1849.
41. Harden TK, JL Boyer and RA Nicholas. (1995). P2-purinergic receptors: subtype-associated signaling responses and structure. Annu Rev Pharmacol Toxicol 35:541-579.
42. Zuk PA, M Zhu, H Mizuno, J Huang, JW Futrell, AJ Katz, P Benhaim, HP Lorenz and MH Hedrick. (2001). Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7:211-228.
43. Zuk PA, M Zhu, P Ashjian, DA De Ugarte, JI Huang, H Mizuno, ZC Alfonso, JK Fraser, P Benhaim and MH Hedrick. (2002). Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279-4295.
44. Kassack MU, B Hofgen, J Lehmann, N Eckstein, JM Quillan and W Sadee. (2002). Functional screening of G protein- coupled receptors by measuring intracellular calcium with a fluorescence microplate reader. J Biomol Screen 7:233-246.
45. Dunn PM and AGH Blakeley. (1988). Suramin: a reversible P2-purinoceptor antagonist in the mouse vas deferens. Br J Pharmacol 93:243-245.
46. Sun B, J Li, K Okahara and J Kambayashi. (1998). P2X1 purinoceptor in human platelets -molecular cloning and functional characterization after heterologous expression. J Biol Chem 273:11544-11547.
47. Watanabe S, M Ikekita and H Nakata. (2005). Identification of specific [3H]adenine-binding sites in rat brain membranes. J Biochem 137:323-329.
48. Müller C. (2002). P2-pyrimidinergic receptors and their ligands. Curr Pharm Des 8:2353-2369.
49. Yoshimura K, T Shimegi, D Matsumoto, T Sato, Y Takaki, E Aiba-Kojima, K Sato, K Inoue, T Nagase, I Koshima and K Gonda. (2006). Characterization of freshly isolated and cultured cells derived from the fatty and fluid portions of liposuction aspirates. J Cell Physiol 208:64-76.
50. Dominici M, K Le Blanc, I Mueller, I Slaper-Cortenbach, F Marini, D Krause, R Deans, A Keating, D Prockop and E Horwitz. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315-317.
51. Bonewald L, S Harris, J Rosser, M Dallas, S Dallas, N Camacho, B Boyan and A Boskey. (2003). von Kossa staining alone is not sufficient to confirm that mineralization in vitro represents bone formation. Calcif Tissue Int 72:537-547.
52. Orriss I, J Utting, A Brandao-Burch, K Colston, B Grubb, G Burnstock and T Arnett. (2007). Extracellular nucleotides block bone mineralization in vitro: evidence for dual inhibitory mechanisms involving both P2Y2 receptors and pyrophosphate. Endocrinology 148:4208-4216.
53. Karp J, L Ferreira, A Khademhosseini, A Kwon, J Yeh and R Langer. (2006). Cultivation of human embryonic stem cells without the embryoid body step enhances osteogenesis in vitro. Stem Cells Dev 24:835-843.
54. Haddouti E-M, M Scroch, N Zippel, C Müller, B Birova, A Pansky, C Kleinfeld, M Winter and E Tobiasch. (2009). Human dental follicle precursor cells of wisdom teeth: isolation and differentiation towards osteocytes for implants with and without scaffolds. Mat Sci Eng Tech 40:732-737.
55. Kémoun P, S Laurencin-Dalicieux, J Rue, JC Farges, I Gennero, F Conte-Auriol, F Briand-Mesange, M Gadelorge, H Arzate, et al. (2007). Human dental follicle cells acquire cementoblast features under stimulation by BMP-2/-7 and enamel matrix derivatives (EMD) in vitro. Cell Tissue Res 329:283-294.
56. Slootweg PJ. (2009). Lesions of the jaws. Histopathology 54:401-418.
57. Chung UI, H Kawaguchi, T Takato and K Nakamura. (2004). Distinct osteogenic mechanisms of bones of distinct origins. J Orthop Sci 9:410-414.
58. Luan X, S Dangaria, Y Ito, C Walker, T Jin, M Schmidt, M Galang and R Druzinsky. (2009). Neural crest lineage segregation: a blueprint for periodontal regeneration. J Dent Res 88:781-791.
59. Depew M, C Simpson, M Morasso and J Rubenstein. (2005). Reassessing the Dlx code: the genetic regulation of branchial arch skeletal pattern and development. J Anat 207:501-561.
60. Dangaria SJ, Y Ito, X Luan and TGH Diekwisch. (2011). Differentiation of neural-crest-derived intermediate pluripotent progenitors into committed periodontal populations involves unique molecular signature changes, cohort shifts, and epigenetic modifications. Stem Cells Dev 20:39-52.
61. Sengupta A and JA Cancelas. (2010). Cancer stem cells: a stride towards cancer cure? J Cell Physiol 225:7-14.
62. Milosevic J, A Brandt, U Roemuss, A Arnold, F Wegner, SC Schwarz, A Storch H Zimmermann and J Schwarz. (2006). Uracil nucleotides stimulate human neural precursor cell proliferation and dopaminergic differentiation: involvement of MEK/ERK signalling. J Neurochem 99:913-923.
63. Orriss IR, GE Knight, S Ranasinghe, G Burnstock and TR Arnett. (2006). Osteoblast responses to nucleotides increase during differentiation. Bone 39:300-309.
64. Nishii N, N Nejime, C Yamauchi, N Yanai, K Shinozuka and T Nakabayashi. (2009). Effects of ATP on the intracellular calcium level in the osteoblastic TBR31-2 cell line. Biol Pharm Bull 32:18-32.
65. Orriss I, G Burnstock and T Arnett. (2010). Purinergic signalling and bone remodelling. Curr Opin Pharmacol 10:322-330.
66. Hsu HH and HC Anderson. (1977). A simple and defined method to study calcification by isolated matrix vesicles. Effect of ATP and vesicle phosphatase. Biochim Biophys Acta 500:162-172.
67. Nakamura EI, Y Uezono, KI Narusawa, I Shibuya, Y Oishi, M Tanaka, N Yanagihara, T Nakamura and F Izumi. (2000). ATP activates DNA synthesis by acting on P2X receptors in human osteoblast-like MG-63 cells. Am J Physiol Cell Physiol 279:C510-C519.
68. Gartland A, RA Hipskind, JA Gallagher and WB Bowler. (2001). Expression of a P2X7 receptor by a subpopulation of human osteoblasts. J Bone Miner Res 16:846-856.
69. Grol MW, N Panupinthu, J Korcok, SM Sims and SJ Dixon. (2009). Expression, signaling, and function of P2X7 receptors in bone. Purinergic Signal 5:205-221.
70. Panupinthu N, L Zhao, F Possmayer, HZ Ke, SM Sims and SJ Dixon. (2007). P2X7 nucleotide receptors mediate blebbing in osteoblasts through a pathway involving lysophosphatidic acid. J Biol Chem 282:3403-3412.
71. Panupinthu N, JT Rogers, L Zhao, LP Solano-Flores, F Possmayer, SM Sims and SJ Dixon. (2008). P2X7 receptors on osteoblasts couple to production of lysophosphatidic acid: a signaling axis promoting osteogenesis. J Cell Biol 181:859-871.
72. Gavala M, L Hill, L Lenertz, M Karta and P Bertics. (2010). Activation of the transcription factor FosB/activating protein-1 (AP-1) is a prominent downstream signal of the extracellular nucleotide receptor P2RX7 in monocytic and osteoblastic cells. J Biol Chem 285:34288-34298.
73. Liu D, D Genetos, Y Shao, D Geist, J Li, H Ke, C Turner and R Duncan. (2008). Activation of extracellular-signal regulated kinase (ERK1/2) by fluid shear is Ca2 + - and ATPdependent in MC3T3-E1 osteoblasts. Bone 42:644-652.
74. Kaplan AD, WJ Reimer, RD Feldman and SJ Dixon. (1995). Extracellular nucleotides potentiate the cytosolic Ca2 + , but not cyclic adenosine 3¢, 5¢-monophosphate response to parathyroid hormone in rat osteoblastic cells. Endocrinology 136:1674-1685.
75. Sistare FD, BA Rosenzweig and JG Contrera. (1995). P2 purinergic receptors potentiate parathyroid hormone receptormediated increases in intracellular calcium and inositol trisphosphate in UMR-106 rat osteoblasts. Endocrinology 136:4489-4497.
76. Bowler WB, KA Buckley, A Gartland, RA Hipskind, G Bilbe and JA Gallagher. (2001). Extracellular nucleotide signaling: a mechanism for integrating local and systemic responses in the activation of bone remodeling. Bone 28:507-512.
77. Buckley KA, RA Hipskind, A Gartland, WB Bowler and JA Gallagher. (2002). Adenosine triphosphate stimulates human osteoclast activity via upregulation of osteoblast-expressed receptor activator of nuclear factor-[kappa]B ligand. Bone 31:582-590.
78. Jones SJ, C Gray, A Boyde and G Burnstock. (1997). Purinergic transmitters inhibit bone formation by cultured osteoblasts. Bone 21:393-399.
79. Shimegi S. (1996). ATP and adenosine act as a mitogen for osteoblast-like cells (MC3T3-E1). Calcif Tissue Int 58:109-113.
80. Erb L, Z Liao, C Seye and G Weisman. (2006). P2 receptors: intracellular signaling. Pflugers Arch Eur J Physiol 452:552-562.
81. Gallagher JA. (2004). ATP P2 receptors and regulation of bone effector cells. J Musculoskelet Neuronal Interact 4:125-127.
82. Jorgensen NR, ST Geist, R Civitelli and TH Steinberg. (1997). ATP- and Gap junction-dependent intercellular calcium signaling in osteoblastic cells. J Cell Biol 139:497-506.
83. Henriksen Z, JF Hiken, TH Steinberg and NR Jørgensen. (2006). The predominant mechanism of intercellular calcium wave propagation changes during long-term culture of human osteoblast-like cells. Cell Calcium 39:435-444.
84. Orriss I, G Knight, J Utting, S Taylor, G Burnstock and T Arnett. (2009). Hypoxia stimulates vesicular ATP release from rat osteoblasts. J Cell Physiol 220:155-162.
85. Cavaliere F, V Nestola, S Amadio, N D'Ambrosi, D Angelini, G Sancesario, G Bernardi and C Volonté. (2005). The metabotropic P2Y4 receptor participates in the commitment to differentiation and cell death of human neuroblastoma SHSY5Y cells. Neurobiol Dis 18:100-109.
86. Resende RR, P Majumder, KN Gomes, LRG Britto and H Ulrich. (2007). P19 embryonal carcinoma cells as in vitro model for studying purinergic receptor expression and modulation of N-methyl-d-aspartate-glutamate and acetylcholine receptors during neuronal differentiation. Neuroscience 146:1169-1181.
87. Burrell HE, WB Bowler, JA Gallagher and GR Sharpe. (2003). Human keratinocytes express multiple P2Y-receptors: evidence for functional P2Y1, P2Y2, and P2Y4 receptors. J Invest Dermatol 120:440-447.
88. Abbracchio MP, J-M Boeynaems, EA Barnard, JL Boyer, C Kennedy, MT Miras-Portugal, BF King, C Gachet, KA Jacobson, GA Weisman and G Burnstock. (2003). Characterization of the UDP-glucose receptor (re-named here the P2Y14 receptor) adds diversity to the P2Y receptor family. Trends Pharmacol Sci 24:52-55.
89. Chambers JK, LE Macdonald, HM Sarau, RS Ames, K Freeman, JJ Foley, Y Zhu, MM McLaughlin, P Murdock, et al. (2000). A G protein-coupled receptor for UDP-glucose. J Biol Chem 275:10767-10771.
90. Choi S-Y and K-T Kim. (1997). Extracellular ATP-stimulated increase of cytosolic cAMP in HL-60 cells. Biochem Pharmacol 53:429-432.
91. Yang D-C, H-J Tsay, S-Y Lin, S-H Chiou, M-J Li, T-J Chang and S-C Hung. (2008). cAMP/PKA regulates osteogenesis, adipogenesis and ratio of RANKL/OPG mRNA expression in mesenchymal stem cells by suppressing leptin. PLoS ONE 3:e1540.