Mesenchymal stem cells from different murine tissues have differential capacity to metabolize extracellular nucleotides

Journal of Cellular Biochemistry

Volumn 115, Issue 10, 2014, Pages 1673-1682

  Iser, Isabele C ^a   Bracco, Paula A ^a   Gonçalves, Carlos E I ^b   Zanin, Rafael F ^c   Nardi, Nance B ^d   Lenz, Guido ^e   Battastini, Ana Maria O ^e   Wink, Márcia R ^a  

^a UNIVERSIDADE FEDERAL DE CIÊNCIAS DA SAÚDE DE PORTO ALEGRE   (Brazil)

^b FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^c PONTIFICAL CATHOLIC UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^d UNIVERSIDADE LUTERANA DO BRASIL   (Brazil)

^e FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

CD73; E NTPDASES; ECTONUCLEOTIDASES; MSC; PURINERGIC SIGNALING

Indexed keywords

ALKALINE PHOSPHATASE; FAT DROPLET; GLUCOSE 6 PHOSPHATE; GLYCEROL 2 PHOSPHATE; MESSENGER RNA; NUCLEOTIDE; 5' NUCLEOTIDASE; INORGANIC PYROPHOSPHATASE; NUCLEOSIDE TRIPHOSPHATE PYROPHOSPHATASE;

ADULT; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL METABOLISM; CELL POPULATION; COMPARATIVE STUDY; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVITY; GENE EXPRESSION; HYDROLYSIS; IMMUNOPHENOTYPING; INTRACELLULAR SIGNALING; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; NUCLEOTIDE METABOLISM; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; TISSUE DIFFERENTIATION; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; ENZYMOLOGY; MESENCHYMAL STROMA CELL; METABOLISM; SIGNAL TRANSDUCTION;

5'-NUCLEOTIDASE; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED BALB C; NUCLEOTIDES; PYROPHOSPHATASES; SIGNAL TRANSDUCTION;

EID: 84906090065     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24830     Document Type: Article

References (50)

1. Agresti C, Meomartini ME, Amadio S, Ambrosini E, Volonte C, Aloisi F, Visentin S,. 2005. ATP regulates oligodendrocyte progenitor migration, proliferation, and differentiation: Involvement of metabotropic P2 receptors. Brain Res Brain Res Rev 48: 157-165.
2. Beckermann BM, Kallifatidis G, Groth A, Frommhold D, Apel A, Mattern J, Salnikov AV, Moldenhauer G, Wagner W, Diehlmann A, Saffrich R, Schubert M, Ho AD, Giese N, Buchler MW, Friess H, Buchler P, Herr I,. 2008. VEGF expression by mesenchymal stem cells contributes to angiogenesis in pancreatic carcinoma. Br J Cancer 99: 622-631.
3. Bianchi G, Morandi F, Cilli M, Daga A, Bocelli-Tyndall C, Gambini C, Pistoia V, Raffaghello L,. 2012. Close interactions between mesenchymal stem cells and neuroblastoma cell lines lead to tumor growth inhibition. PloS ONE 7: e48654.
4. Biver G, Wang N, Gartland A, Orriss I, Arnett TR, Boeynaems JM, Robaye B,. 2013. Role of the P2Y receptor in the differentiation of bone marrow stromal cells into osteoblasts and adipocytes. Stem Cells.
5. Boskey AL, Doty SB, Binderman I,. 1994. Adenosine 5′-triphosphate promotes mineralization in differentiating chick limb-bud mesenchymal cell cultures. Microsc Res Tech 28: 492-504.
6. Bradford MM,. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
7. Burnstock G,. 2009. Purinergic signalling: Past, present and future. Braz J Med Biol Res 42: 3-8.
8. Cao X, Li LP, Qin XH, Li SJ, Zhang M, Wang Q, Hu HH, Fang YY, Gao YB, Li XW, Sun LR, Xiong WC, Gao TM, Zhu XH,. 2013. Astrocytic ATP release regulates the proliferation of neural stem cells in the adult hippocampus. Stem Cells.
9. Chagastelles PC, Nardi NB, Camassola M,. 2010. Biology and applications of mesenchymal stem cells. Sci Prog 93: 113-127.
10. Chamberlain G, Fox J, Ashton B, Middleton J,. 2007. Concise review: Mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 25: 2739-2749.
11. 2+ -stimulated ATPase activity. Anal Biochem 157: 375-380.
12. Chanda D, Isayeva T, Kumar S, Hensel JA, Sawant A, Ramaswamy G, Siegal GP, Beatty MS, Ponnazhagan S,. 2009. Therapeutic potential of adult bone marrow-derived mesenchymal stem cells in prostate cancer bone metastasis. Clin Cancer Res 15: 7175-7185.
13. 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: 1097-1111.
14. Coppi E, Pugliese AM, Urbani S, Melani A, Cerbai E, Mazzanti B, Bosi A, Saccardi R, Pedata F,. 2007. ATP modulates cell proliferation and elicits two different electrophysiological responses in human mesenchymal stem cells. Stem Cells 25: 1840-1849.
15. Costa MA, Barbosa A, Neto E, Sa-e-Sousa A, Freitas R, Neves JM, Magalhaes-Cardoso T, Ferreirinha F, Correia-de-Sa P,. 2011. On the role of subtype selective adenosine receptor agonists during proliferation and osteogenic differentiation of human primary bone marrow stromal cells. J Cell Physiol 226: 1353-1366.
16. da Silva Meirelles L, Caplan AI, Nardi NB,. 2008. In search of the in vivo identity of mesenchymal stem cells. Stem Cells 26: 2287-2299.
17. da Silva Meirelles L, Chagastelles PC, Nardi NB,. 2006. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 119: 2204-2213.
18. Faroni A, Rothwell SW, Grolla AA, Terenghi G, Magnaghi V, Verkhratsky A,. 2013. Differentiation of adipose-derived stem cells into Schwann cell phenotype induces expression of P2X receptors that control cell death. Cell Death Dis 4: e743.
19. Ferrari D, Gulinelli S, Salvestrini V, Lucchetti G, Zini R, Manfredini R, Caione L, Piacibello W, Ciciarello M, Rossi L, Idzko M, Ferrari S, Di Virgilio F, Lemoli RM,. 2011. Purinergic stimulation of human mesenchymal stem cells potentiates their chemotactic response to CXCL12 and increases the homing capacity and production of proinflammatory cytokines. Exp Hematol 39: 360-374, 374e361-365.
20. Friedenstein AJ, Gorskaja JF, Kulagina NN,. 1976. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 4: 267-274.
21. 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: 2112-2124.
22. Gharibi B, Abraham AA, Ham J, Evans BA,. 2012. Contrasting effects of A1 and A2b adenosine receptors on adipogenesis. Int J Obes 36: 397-406.
23. Grimm I, Ullsperger SN, Zimmermann H,. 2010. Nucleotides and epidermal growth factor induce parallel cytoskeletal rearrangements and migration in cultured adult murine neural stem cells. Acta Physiol (Oxf) 199: 181-189.
24. Jia C, Doherty JP, Crudgington S, Hegg CC,. 2009. Activation of purinergic receptors induces proliferation and neuronal differentiation in Swiss Webster mouse olfactory epithelium. Neuroscience 163: 120-128.
25. Lavoie EG, Fausther M, Kauffenstein G, Kukulski F, Kunzli BM, Friess H, Sevigny J,. 2010. Identification of the ectonucleotidases expressed in mouse, rat, and human Langerhans islets: Potential role of NTPDase3 in insulin secretion. Am J Physiol Endocrinol Metab 299: E647-E656.
26. Ledur PF, Villodre ES, Paulus R, Cruz LA, Flores DG, Lenz G,. 2012. Extracellular ATP reduces tumor sphere growth and cancer stem cell population in glioblastoma cells. Purinergic Signal 8: 39-48.
27. Lin JH, Takano T, Arcuino G, Wang X, Hu F, Darzynkiewicz Z, Nunes M, Goldman SA, Nedergaard M,. 2007. Purinergic signaling regulates neural progenitor cell expansion and neurogenesis. Dev Biol 302: 356-366.
28. Livak KJ, Schmittgen TD,. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
29. Martins I, Wang Y, Michaud M, Ma Y, Sukkurwala AQ, Shen S, Kepp O, Metivier D, Galluzzi L, Perfettini JL, Zitvogel L, Kroemer G,. 2013. 2013. Molecular mechanisms of ATP secretion during immunogenic cell death. Cell Death Differ.
30. Meirelles Lda S, Fontes AM, Covas DT, Caplan AI,. 2009. Mechanisms involved in the therapeutic properties of mesenchymal stem cells. Cytokine Growth Factor Rev 20: 419-427.
31. Michaud M, Martins I, Sukkurwala AQ, Adjemian S, Ma Y, Pellegatti P, Shen S, Kepp O, Scoazec M, Mignot G, Rello-Varona S, Tailler M, Menger L, Vacchelli E, Galluzzi L, Ghiringhelli F, di Virgilio F, Zitvogel L, Kroemer G,. 2011. Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice. Science 334: 1573-1577.
32. Millan JL,. 2006. Alkaline phosphatases: Structure, substrate specificity and functional relatedness to other members of a large superfamily of enzymes. Purinergic Signal 2: 335-341.
33. Mishra SK, Braun N, Shukla V, Fullgrabe M, Schomerus C, Korf HW, Gachet C, Ikehara Y, Sevigny J, Robson SC, Zimmermann H,. 2006. Extracellular nucleotide signaling in adult neural stem cells: Synergism with growth factor-mediated cellular proliferation. Development 133: 675-684.
34. Murrell W, Palmero E, Bianco J, Stangeland B, Joel M, Paulson L, Thiede B, Grieg Z, Ramsnes I, Skjellegrind HK, Nygard S, Brandal P, Sandberg C, Vik-Mo E, Palmero S, Langmoen IA,. 2013. Expansion of multipotent stem cells from the adult human brain. PLoS ONE 8: e71334.
35. Nakamizo A, Marini F, Amano T, Khan A, Studeny M, Gumin J, Chen J, Hentschel S, Vecil G, Dembinski J, Andreeff M, Lang FF,. 2005. Human bone marrow-derived mesenchymal stem cells in the treatment of gliomas. Cancer Res 65: 3307-3318.
36. Noel D, Caton D, Roche S, Bony C, Lehmann S, Casteilla L, Jorgensen C, Cousin B,. 2008. Cell specific differences between human adipose-derived and mesenchymal-stromal cells despite similar differentiation potentials. Exp Cell Res 314: 1575-1584.
37. Resende RR, Majumder P, Gomes KN, Britto LR, Ulrich H,. 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.
38. Roszek K, Blaszczak A, Wujak M, Komoszynski M,. 2013. Nucleotides metabolizing ectoenzymes as possible markers of mesenchymal stem cell osteogenic differentiation. Biochem Cell Biol 91: 176-181.
39. Sak K, Boeynaems JM, Everaus H,. 2003. Involvement of P2Y receptors in the differentiation of haematopoietic cells. J Leukoc Biol 73: 442-447.
40. Scheibe RJ, Kuehl H, Krautwald S, Meissner JD, Mueller WH,. 2000. Ecto-alkaline phosphatase activity identified at physiological pH range on intact P19 and HL-60 cells is induced by retinoic acid. J Cell Biochem 76: 420-436.
41. Shukla V, Zimmermann H, Wang L, Kettenmann H, Raab S, Hammer K, Sevigny J, Robson SC, Braun N,. 2005. Functional expression of the ecto-ATPase NTPDase2 and of nucleotide receptors by neuronal progenitor cells in the adult murine hippocampus. J Neurosci Res 80: 600-610.
42. Streitova D, Sefc L, Savvulidi F, Pospisil M, Hola J, Hofer M,. 2010. Adenosine A(1), A(2a), A(2b), and A(3) receptors in hematopoiesis. 1. Expression of receptor mRNA in four mouse hematopoietic precursor cells. Physiol Res 59: 133-137.
43. Sung JH, Yang HM, Park JB, Choi GS, Joh JW, Kwon CH, Chun JM, Lee SK, Kim SJ,. 2008. Isolation and characterization of mouse mesenchymal stem cells. Transplant Proc 40: 2649-2654.
44. Vegh I, Grau M, Gracia M, Grande J, de la Torre P, Flores AI,. 2013. Decidua mesenchymal stem cells migrated toward mammary tumors in vitro and in vivo affecting tumor growth and tumor development. Cancer Gene Ther 20: 8-16.
45. Wilson SM, Barsoum MJ, Wilson BW, Pappone PA,. 1999. Purine nucleotides modulate proliferation of brown fat preadipocytes. Cell Prolif 32: 131-140.
46. Wink MR, Lenz G, Rodnight R, Sarkis JJ, Battastini AM,. 2000. Identification of brain ecto-apyrase as a phosphoprotein. Mol Cell Biochem 213: 11-16.
47. Wink MR, Braganhol E, Tamajusuku AS, Casali EA, Karl J, Barreto-Chaves ML, Sarkis JJ, Battastini AM,. 2003a. Extracellular adenine nucleotides metabolism in astrocyte cultures from different brain regions. Neurochem Int 43: 621-628.
48. Wink MR, Lenz G, Braganhol E, Tamajusuku AS, Schwartsmann G, Sarkis JJ, Battastini AM,. 2003b. Altered extracellular ATP, ADP and AMP catabolism in glioma cell lines. Cancer Lett 198: 211-218.
49. Zimmermann H, Zebisch M, Strater N,. 2012. Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal 8: 437-502.
50. 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: 884-900.