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New insights regarding the regulation of chemotaxis by nucleotides, adenosine, and their receptors

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Abstract

The directional movement of cells can be regulated by ATP, certain other nucleotides (e.g., ADP, UTP), and adenosine. Such regulation occurs for cells that are “professional phagocytes” (e.g., neutrophils, macrophages, certain lymphocytes, and microglia) and that undergo directional migration and subsequent phagocytosis. Numerous other cell types (e.g., fibroblasts, endothelial cells, neurons, and keratinocytes) also change motility and migration in response to ATP, other nucleotides, and adenosine. In this article, we review how nucleotides and adenosine modulate chemotaxis and motility and highlight the importance of nucleotide- and adenosine-regulated cell migration in several cell types: neutrophils, microglia, endothelial cells, and cancer cells. We also discuss difficulties in conducting experiments and drawing conclusions regarding the ability of nucleotides and adenosine to modulate the migration of professional and non-professional phagocytes.

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References

  1. Flannagan RS, Cosio G, Grinstein S (2009) Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat Rev Microbiol 7(5):355–366. doi:10.1038/nrmicro2128

    PubMed  CAS  Google Scholar 

  2. Krause KH (2000) Professional phagocytes: predators and prey of microorganisms. Schweiz Med Wochenschr 130(4):97–100

    PubMed  CAS  Google Scholar 

  3. Brown EJ (1995) Phagocytosis. Bioessays 17(2):109–117. doi:10.1002/bies.950170206

    PubMed  CAS  Google Scholar 

  4. Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, Walk SF, Park D, Woodson RI, Ostankovich M, Sharma P, Lysiak JJ, Harden TK, Leitinger N, Ravichandran KS (2009) Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 461(7261):282–286

    PubMed  CAS  Google Scholar 

  5. Ravichandran KS (2010) Find-me and eat-me signals in apoptotic cell clearance: progress and conundrums. J Exp Med 207(9):1807–1817. doi:10.1084/jem.20101157

    PubMed  CAS  Google Scholar 

  6. Junger WG (2011) Immune cell regulation by autocrine purinergic signalling. Nat Rev Immunol 11(3):201–212. doi:10.1038/nri2938

    PubMed  CAS  Google Scholar 

  7. Linden J (2011) Regulation of leukocyte function by adenosine receptors. Adv Pharmacol 61:95–114. doi:10.1016/B978-0-12-385526-8.00004-7

    PubMed  CAS  Google Scholar 

  8. Iglesias PA, Devreotes PN (2008) Navigating through models of chemotaxis. Curr Opin Cell Biol 20(1):35–40

    PubMed  CAS  Google Scholar 

  9. Patlak C (1953) Random walk with persistence and external bias. Bull Math Biol 15(3):311–338. doi:10.1007/bf02476407

    CAS  Google Scholar 

  10. Bosgraaf L, Van Haastert PJM (2009) The ordered extension of pseudopodia by amoeboid cells in the absence of external cues. PLoS One 4(4):e5253

    PubMed  Google Scholar 

  11. Petrie RJ, Doyle AD, Yamada KM (2009) Random versus directionally persistent cell migration. Nat Rev Mol Cell Biol 10(8):538–549

    PubMed  CAS  Google Scholar 

  12. Lazarowski E (2012) Vesicular and conductive mechanisms of nucleotide release. Purinergic Signalling. doi:10.1007/s11302-012-9304-9

  13. McDonald B, Pittman K, Menezes GB, Hirota SA, Slaba I, Waterhouse CCM, Beck PL, Muruve DA, Kubes P (2010) Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 330 (6002):362–366. doi:10.1126/science.1195491

    Google Scholar 

  14. Isfort K, Ebert F, Bornhorst J, Sargin S, Kardakaris R, Pasparakis M, Baehler M, Schwerdtle T, Schwab A, Hanley PJ (2011) Real-time imaging reveals that P2Y2 and P2Y12 receptor agonists are not chemoattractants and macrophage chemotaxis to C5a is PI3K- and p38 MAPK-independent. J Biol Chem. doi:10.1074/jbc.M111.289793

  15. Surprenant A, North RA (2009) Signaling at purinergic P2X receptors. Annu Rev Physiol 71(1):333–359. doi:10.1146/annurev.physiol.70.113006.100630

    PubMed  CAS  Google Scholar 

  16. von Kugelgen I, Harden TK (2011) Molecular pharmacology, physiology, and structure of the P2Y receptors. Adv Pharmacol 61:373–415. doi:10.1016/B978-0-12-385526-8.00012-6

    Google Scholar 

  17. Zimmermann H (2000) Extracellular metabolism of ATP and other nucleotides. Naunyn Schmiedebergs Arch Pharmacol 362(4–5):299–309

    PubMed  CAS  Google Scholar 

  18. Fredholm BB, Ijzerman AP, Jacobson KA, Linden J, Muller CE (2011) International union of basic and clinical pharmacology. LXXXI. Nomenclature and classification of adenosine receptors—an update. Pharmacol Rev 63(1):1–34. doi:10.1124/pr.110.003285

    PubMed  CAS  Google Scholar 

  19. Young JD, Yao SY, Sun L, Cass CE, Baldwin SA (2008) Human equilibrative nucleoside transporter (ENT) family of nucleoside and nucleobase transporter proteins. Xenobiotica 38(7–8):995–1021. doi:10.1080/00498250801927427

    PubMed  CAS  Google Scholar 

  20. Sager G, Ravna AW (2009) Cellular efflux of cAMP and cGMP—a question about selectivity. Mini Rev Med Chem 9(8):1009–1013

    PubMed  CAS  Google Scholar 

  21. Bader S, Kortholt A, Van Haastert PJM (2007) Seven dictyostelium discoideum phosphodiesterases degrade three pools of cAMP and cGMP. Biochem J 402(1):153–161. doi:10.1042/bj20061153

    PubMed  CAS  Google Scholar 

  22. Rosenberg PA, Dichter MA (1989) Extracellular cAMP accumulation and degradation in rat cerebral cortex in dissociated cell culture. J Neurosci 9(8):2654–2663

    PubMed  CAS  Google Scholar 

  23. Jackson EK, Mi Z, Dubey RK (2007) The extracellular cAMP-adenosine pathway significantly contributes to the in vivo production of adenosine. J Pharmacol Exp Ther 320(1):117–123. doi:10.1124/jpet.106.112748

    PubMed  CAS  Google Scholar 

  24. Di Virgilio F (2007) Liaisons dangereuses: P2X(7) and the inflammasome. Trends Pharmacol Sci 28(9):465–472. doi:10.1016/j.tips.2007.07.002

    PubMed  Google Scholar 

  25. Martinon F, Gaide O, Pétrilli V, Mayor A, Tschopp J (2007) NALP inflammasomes: a central role in innate immunity. Semin Immunopathol 29(3):213–229. doi:10.1007/s00281-007-0079-y

    PubMed  CAS  Google Scholar 

  26. Jandl JH (1996) Blood: textbook of hematology. Boston, Little Brown and Co.

  27. Bagorda A, Parent CA (2008) Eukaryotic chemotaxis at a glance. J Cell Sci 121(16):2621–2624. doi:10.1242/jcs.018077

    PubMed  CAS  Google Scholar 

  28. Zigmond SH (1977) Ability of polymorphonuclear leukocytes to orient in gradients of chemotactic factors. J Cell Biol 75(2 Pt 1):606–616

    PubMed  CAS  Google Scholar 

  29. Chen Y, Corriden R, Inoue Y, Yip L, Hashiguchi N, Zinkernagel A, Nizet V, Insel PA, Junger WG (2006) ATP release guides neutrophil chemotaxis via P2Y2 and A3 receptors. Science 314(5806):1792–1795. doi:10.1126/science.1132559

    PubMed  CAS  Google Scholar 

  30. Lecut C, Frederix K, Johnson DM, Deroanne C, Thiry M, Cl F, Maree Rl, Evans RJ, Volders PGA, Bours V, Oury Cc (2009) P2X1 ion channels promote neutrophil chemotaxis through rho kinase activation. J Immunol 183(4):2801–2809. doi:10.4049/jimmunol.0804007

    PubMed  CAS  Google Scholar 

  31. He R, Tan L, Browning DD, Wang JM, Ye RD (2000) The synthetic peptide Trp-Lys-Tyr-Met-Val-D-Met is a potent chemotactic agonist for mouse formyl peptide receptor. J Immunol 165(8):4598–4605

    PubMed  CAS  Google Scholar 

  32. Kronlage M, Song J, Sorokin L, Isfort K, Schwerdtle T, Leipziger J, Robaye B, Conley PB, Kim H-C, Sargin S, Schon P, Schwab A, Hanley PJ (2010) Autocrine purinergic receptor signaling is essential for macrophage chemotaxis. Sci Signal 3(132):ra55. doi:10.1126/scisignal.2000588

    PubMed  Google Scholar 

  33. Jr R, Vollmer I, Stark S, Wagner R, Ngamsri K-C, Eltzschig HK (2009) Adenosine and inflammation: CD39 and CD73 are critical mediators in LPS-induced PMN trafficking into the lungs. FASEB J 23(2):473–482. doi:10.1096/fj.08-119701

    Google Scholar 

  34. Corriden R, Insel PA, Junger WG (2007) A novel method using fluorescence microscopy for real-time assessment of ATP release from individual cells. Am J Physiol Cell Physiol 293(4):C1420–C1425. doi:10.1152/ajpcell.00271.2007

    PubMed  CAS  Google Scholar 

  35. Inoue Y, Chen Y, Hirsh MI, Yip L, Junger WG (2008) A3 and P2Y2 receptors control the recruitment of neutrophils to the lungs in a mouse model of sepsis. Shock 30(2):173–177. doi:10.1097/shk.0b013e318160dad4

    PubMed  Google Scholar 

  36. Chen Y, Yao Y, Sumi Y, Li A, To UK, Elkhal A, Inoue Y, Woehrle T, Zhang Q, Hauser C, Junger WG (2010) Purinergic signaling: a fundamental mechanism in neutrophil activation. Sci Signal 3 (125):ra45-. doi:10.1126/scisignal.2000549

  37. Kukulski F, Ben Yebdri F, Lecka J, Kauffenstein G, Levesque SA, Martín-Satué M, Sévigny J (2009) Extracellular ATP and P2 receptors are required for IL-8 to induce neutrophil migration. Cytokine 46(2):166–170

    PubMed  CAS  Google Scholar 

  38. Fredholm BB, IJzerman AP, Jacobson KA, Klotz KN, Linden J (2001) International union of pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol Rev 53(4):527–552

    PubMed  CAS  Google Scholar 

  39. Koizumi S, Odashima M, Otaka M, Jin M, Linden J, Watanabe S, Ohnishi H (2009) Attenuation of gastric mucosal inflammation induced by indomethacin through activation of the A2A adenosine receptor in rats. J Gastroenterol 44(5):419–425. doi:10.1007/s00535-009-0028-8

    PubMed  CAS  Google Scholar 

  40. Wang H, Zhang W, Tang R, Zhu C, Bucher C, Blazar BR, Geng JG, Zhang C, Linden J, Wu C, Huo Y (2010) Adenosine receptor A2A deficiency in leukocytes increases arterial neointima formation in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 30(5):915–922. doi:10.1161/ATVBAHA.109.202572

    PubMed  CAS  Google Scholar 

  41. Neely CF, Jin J, Keith IM (1997) A1-adenosine receptor antagonists block endotoxin-induced lung injury. Am J Physiol 272(2 Pt 1):L353–L361

    PubMed  CAS  Google Scholar 

  42. Cronstein BN, Levin RI, Philips M, Hirschhorn R, Abramson SB, Weissmann G (1992) Neutrophil adherence to endothelium is enhanced via adenosine A1 receptors and inhibited via adenosine A2 receptors. J Immunol 148(7):2201–2206

    PubMed  CAS  Google Scholar 

  43. Ngamsri KC, Wagner R, Vollmer I, Stark S, Reutershan J (2010) Adenosine receptor A1 regulates polymorphonuclear cell trafficking and microvascular permeability in lipopolysaccharide-induced lung injury. J Immunol 185(7):4374–4384. doi:10.4049/jimmunol.1000433

    PubMed  CAS  Google Scholar 

  44. van der Hoeven D, Wan TC, Auchampach JA (2008) Activation of the A(3) adenosine receptor suppresses superoxide production and chemotaxis of mouse bone marrow neutrophils. Mol Pharmacol 74(3):685–696. doi:10.1124/mol.108.048066

    PubMed  Google Scholar 

  45. Wagner R, Ngamsri K-C, Stark S, Vollmer I, Jr R (2010) Adenosine receptor A3 is a critical mediator in LPS-induced pulmonary inflammation. Am J Physiol Lung Cell Mol Physiol 299(4):L502–L512. doi:10.1152/ajplung.00083.2010

    PubMed  CAS  Google Scholar 

  46. van der Hoeven D, Gizewski ET, Auchampach JA (2010) Activation of the A(3) adenosine receptor inhibits fMLP-induced Rac activation in mouse bone marrow neutrophils. Biochem Pharmacol 79(11):1667–1673. doi:10.1016/j.bcp.2010.02.002

    PubMed  Google Scholar 

  47. Corriden R, Chen Y, Inoue Y, Beldi G, Robson SC, Insel PA, Junger WG (2008) Ecto-nucleoside triphosphate diphosphohydrolase 1 (E-NTPDase1/CD39) regulates neutrophil chemotaxis by hydrolyzing released ATP to adenosine. J Biol Chem 283(42):28480–28486. doi:10.1074/jbc.M800039200

    PubMed  CAS  Google Scholar 

  48. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A (2011) Physiology of microglia. Physiol Rev 91(2):461–553. doi:10.1152/physrev.00011.2010

    PubMed  CAS  Google Scholar 

  49. Neary JT, Baker L, Jorgensen SL, Norenberg MD (1994) Extracellular ATP induces stellation and increases glial fibrillary acidic protein content and DNA synthesis in primary astrocyte cultures. Acta Neuropathol 87(1):8–13

    PubMed  CAS  Google Scholar 

  50. Honda S, Sasaki Y, Ohsawa K, Imai Y, Nakamura Y, Inoue K, Kohsaka S (2001) Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J Neurosci 21(6):1975–1982

    PubMed  CAS  Google Scholar 

  51. Kurpius D, Nolley EP, Dailey ME (2007) Purines induce directed migration and rapid homing of microglia to injured pyramidal neurons in developing hippocampus. Glia 55(8):873–884. doi:10.1002/glia.20509

    PubMed  Google Scholar 

  52. Duan Y, Sahley CL, Muller KJ (2009) ATP and NO dually control migration of microglia to nerve lesions. Dev Neurobiol 69(1):60–72. doi:10.1002/dneu.20689

    PubMed  CAS  Google Scholar 

  53. Miller AM, Stella N (2009) Microglial cell migration stimulated by ATP and C5a involve distinct molecular mechanisms: quantification of migration by a novel near-infrared method. Glia 57(8):875–883. doi:10.1002/glia.20813

    PubMed  Google Scholar 

  54. Choi M, Cho K, Shin S, Ko H, Kwon K, Shin C, Ko K (2010) ATP induced microglial cell migration through non-transcriptional activation of matrix metalloproteinase-9. Arch Pharm Res 33(2):257–265. doi:10.1007/s12272-010-0211-8

    PubMed  Google Scholar 

  55. Lambert C, Ase AR, Seguela P, Antel JP (2010) Distinct migratory and cytokine responses of human microglia and macrophages to ATP. Brain Behav Immun 24(8):1241–1248. doi:10.1016/j.bbi.2010.02.010

    PubMed  CAS  Google Scholar 

  56. Samuels SE, Lipitz JB, Dahl G, Muller KJ (2010) Neuroglial ATP release through innexin channels controls microglial cell movement to a nerve injury. J Gen Physiol 136(4):425–442. doi:10.1085/jgp.201010476

    PubMed  CAS  Google Scholar 

  57. Haynes SE, Hollopeter G, Yang G, Kurpius D, Dailey ME, Gan WB, Julius D (2006) The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat Neurosci 9(12):1512–1519. doi:10.1038/nn1805

    PubMed  CAS  Google Scholar 

  58. De Simone R, Niturad CE, De Nuccio C, Ajmone-Cat MA, Visentin S, Minghetti L (2010) TGF-β and LPS modulate ADP-induced migration of microglial cells through P2Y1 and P2Y12 receptor expression. J Neurochem 115(2):450–459. doi:10.1111/j.1471-4159.2010.06937.x

    PubMed  Google Scholar 

  59. Horvath RJ, DeLeo JA (2009) Morphine enhances microglial migration through modulation of P2X4 receptor signaling. J Neurosci 29(4):998–1005. doi:10.1523/jneurosci.4595-08.2009

    PubMed  CAS  Google Scholar 

  60. Ifuku M, Farber K, Okuno Y, Yamakawa Y, Miyamoto T, Nolte C, Merrino VF, Kita S, Iwamoto T, Komuro I, Wang B, Cheung G, Ishikawa E, Ooboshi H, Bader M, Wada K, Kettenmann H, Noda M (2007) Bradykinin-induced microglial migration mediated by B1-bradykinin receptors depends on Ca2+ influx via reverse-mode activity of the Na+/Ca2+ exchanger. J Neurosci 27(48):13065–13073. doi:10.1523/JNEUROSCI.3467-07.2007

    PubMed  CAS  Google Scholar 

  61. Cudaback E, Li X, Montine KS, Montine TJ, Keene CD (2011) Apolipoprotein E isoform-dependent microglia migration. FASEB J 25(6):2082–2091. doi:10.1096/fj.10-176891

    PubMed  CAS  Google Scholar 

  62. Orr AG, Orr AL, Li XJ, Gross RE, Traynelis SF (2009) Adenosine A(2A) receptor mediates microglial process retraction. Nat Neurosci 12(7):872–878. doi:10.1038/nn.2341

    PubMed  CAS  Google Scholar 

  63. van der Putten C, Zuiderwijk-Sick EA, van Straalen L, de Geus ED, Boven LA, Kondova I, Ijzerman AP, Bajramovic JJ (2009) Differential expression of adenosine A3 receptors controls adenosine A2A receptor-mediated inhibition of TLR responses in microglia. J Immunol 182(12):7603–7612. doi:10.4049/jimmunol.0803383

    PubMed  Google Scholar 

  64. Bernascone S, Erriquez J, Ferraro M, Genazzani AA, Distasi C (2010) Novel adenosine and cAMP signalling pathways in migrating glial cells. Cell Calcium 48 (1):83–90

    Google Scholar 

  65. Choi I-Y, Lee J-C, Ju C, Hwang S, Cho G-S, Lee HW, Choi WJ, Jeong LS, Kim W-K (2011) A3 adenosine receptor agonist reduces brain ischemic injury and inhibits inflammatory cell migration in rats. Am J Pathol 179 (4):2042–2052

    Google Scholar 

  66. Braun N, Sevigny J, Robson SC, Enjyoji K, Guckelberger O, Hammer K, Di Virgilio F, Zimmermann H (2000) Assignment of ecto-nucleoside triphosphate diphosphohydrolase-1/cd39 expression to microglia and vasculature of the brain. Eur J Neurosci 12(12):4357–4366

    PubMed  CAS  Google Scholar 

  67. Nedeljkovic N, Bjelobaba I, Subasic S, Lavrnja I, Pekovic S, Stojkov D, Vjestica A, Rakic L, Stojiljkovic M (2006) Up-regulation of ectonucleotidase activity after cortical stab injury in rats. Cell Biol Int 30(6):541–546. doi:10.1016/j.cellbi.2006.03.001

    PubMed  CAS  Google Scholar 

  68. Farber K, Markworth S, Pannasch U, Nolte C, Prinz V, Kronenberg G, Gertz K, Endres M, Bechmann I, Enjyoji K, Robson SC, Kettenmann H (2008) The ectonucleotidase cd39/ENTPDase1 modulates purinergic-mediated microglial migration. Glia 56(3):331–341. doi:10.1002/glia.20606

    PubMed  Google Scholar 

  69. Avignone E, Ulmann L, Levavasseur F, Rassendren F, Audinat E (2008) Status epilepticus induces a particular microglial activation state characterized by enhanced purinergic signaling. J Neurosci 28(37):9133–9144. doi:10.1523/JNEUROSCI.1820-08.2008

    PubMed  CAS  Google Scholar 

  70. Folkman J (2006) Angiogenesis. Annu Rev Med 57(1):1–18. doi:10.1146/annurev.med.57.121304.131306

    PubMed  CAS  Google Scholar 

  71. Shen J, DiCorleto PE (2008) ADP stimulates human endothelial cell migration via P2Y1 nucleotide receptor-mediated mitogen-activated protein kinase pathways. Circ Res 102(4):448–456. doi:10.1161/CIRCRESAHA.107.165795

    PubMed  CAS  Google Scholar 

  72. Yokdang N, Tellez JD, Tian H, Norvell J, Barsky SH, Valencik M, Buxton IL (2011) A role for nucleotides in support of breast cancer angiogenesis: heterologous receptor signalling. Br J Cancer 104(10):1628–1640. doi:10.1038/bjc.2011.134

    PubMed  CAS  Google Scholar 

  73. Gerasimovskaya E, Woodward H, Tucker D, Stenmark K (2008) Extracellular ATP is a pro-angiogenic factor for pulmonary artery vasa vasorum endothelial cells. Angiogenesis 11(2):169–182. doi:10.1007/s10456-007-9087-8

    PubMed  CAS  Google Scholar 

  74. Roedersheimer M, Nijmeh H, Burns N, Sidiakova AA, Stenmark KR, Gerasimovskaya EV (2011) Complementary effects of extracellular nucleotides and platelet-derived extracts on angiogenesis of vasa vasorum endothelial cells in vitro and subcutaneous Matrigel plugs in vivo. Vasc Cell 3(1):4. doi:10.1186/2045-824X-3-4

    PubMed  CAS  Google Scholar 

  75. Koyama T, Kimura C, Hayashi M, Watanabe M, Karashima Y, Oike M (2009) Hypergravity induces ATP release and actin reorganization via tyrosine phosphorylation and RhoA activation in bovine endothelial cells. Pflugers Arch 457(4):711–719. doi:10.1007/s00424-008-0544-z

    PubMed  CAS  Google Scholar 

  76. Kaczmarek E, Erb L, Koziak K, Jarzyna R, Wink MR, Guckelberger O, Blusztajn JK, Trinkaus-Randall V, Weisman GA, Robson SC (2005) Modulation of endothelial cell migration by extracellular nucleotides: involvement of focal adhesion kinase and phosphatidylinositol 3-kinase-mediated pathways. Thromb Haemost 93(4):735–742. doi:10.1267/THRO05040735

    PubMed  CAS  Google Scholar 

  77. Woodward HN, Anwar A, Riddle S, Taraseviciene-Stewart L, Fragoso M, Stenmark KR, Gerasimovskaya EV (2009) PI3K, Rho, and ROCK play a key role in hypoxia-induced ATP release and ATP-stimulated angiogenic responses in pulmonary artery vasa vasorum endothelial cells. Am J Physiol Lung Cell Mol Physiol 297(5):L954–L964. doi:10.1152/ajplung.00038.2009

    PubMed  CAS  Google Scholar 

  78. Quillen EE, Haslam GC, Samra HS, Amani-Taleshi D, Knight JA, Wyatt DE, Bishop SC, Colvert KK, Richter ML, Kitos PA (2006) Ectoadenylate kinase and plasma membrane ATP synthase activities of human vascular endothelial cells. J Biol Chem 281(30):20728–20737. doi:10.1074/jbc.M513042200

    PubMed  CAS  Google Scholar 

  79. Zhang X, Gao F, L-l Yu, Peng Y, H-h L, J-y L, Yin M, Ni J (2008) Dual functions of a monoclonal antibody against cell surface F1F0 ATP synthase on both HUVEC and tumor cells1. Acta Pharmacol Sin 29(8):942–950. doi:10.1111/j.1745-7254.2008.00830.x

    PubMed  CAS  Google Scholar 

  80. Notari L, Arakaki N, Mueller D, Meier S, Amaral J, Becerra SP (2010) Pigment epithelium-derived factor binds to cell-surface F(1)-ATP synthase. FEBS J 277(9):2192–2205. doi:10.1111/j.1742-4658.2010.07641.x

    PubMed  CAS  Google Scholar 

  81. Freeman KW, Bowman BR, Zetter BR (2011) Regenerative protein thymosin Œ ≤ −4 is a novel regulator of purinergic signaling. FASEB J 25(3):907–915. doi:10.1096/fj.10-169417

    PubMed  CAS  Google Scholar 

  82. Moser TL, Stack MS, Asplin I, Enghild JJ, Hojrup P, Everitt L, Hubchak S, Schnaper HW, Pizzo SV (1999) Angiostatin binds ATP synthase on the surface of human endothelial cells. Proc Natl Acad Sci USA 96(6):2811–2816

    PubMed  CAS  Google Scholar 

  83. Muller T, Robaye B, Vieira RP, Ferrari D, Grimm M, Jakob T, Martin SF, Di Virgilio F, Boeynaems JM, Virchow JC, Idzko M (2010) The purinergic receptor P2Y2 receptor mediates chemotaxis of dendritic cells and eosinophils in allergic lung inflammation. Allergy 65(12):1545–1553. doi:10.1111/j.1398-9995.2010.02426.x

    PubMed  CAS  Google Scholar 

  84. Slater M, Danieletto S, Pooley M, Cheng Teh L, Gidley-Baird A, Barden JA (2004) Differentiation between cancerous and normal hyperplastic lobules in breast lesions. Breast Cancer Res Treat 83(1):1–10. doi:10.1023/B:BREA.0000010670.85915.0f

    PubMed  Google Scholar 

  85. Slater M, Danieletto S, Gidley-Baird A, Teh LC, Barden JA (2004) Early prostate cancer detected using expression of non-functional cytolytic P2X7 receptors. Histopathology 44(3):206–215. doi:10.1111/j.0309-0167.2004.01798.x

    PubMed  CAS  Google Scholar 

  86. Adinolfi E, Melchiorri L, Falzoni S, Chiozzi P, Morelli A, Tieghi A, Cuneo A, Castoldi G, Di Virgilio F, Baricordi OR (2002) P2X7 receptor expression in evolutive and indolent forms of chronic B lymphocytic leukemia. Blood 99(2):706–708

    PubMed  CAS  Google Scholar 

  87. Solini A, Cuccato S, Ferrari D, Santini E, Gulinelli S, Callegari MG, Dardano A, Faviana P, Madec S, Di Virgilio F, Monzani F (2008) Increased P2X7 receptor expression and function in thyroid papillary cancer: a new potential marker of the disease? Endocrinology 149(1):389–396. doi:10.1210/en.2007-1223

    PubMed  CAS  Google Scholar 

  88. Wei W, Ryu JK, Choi HB, McLarnon JG (2008) Expression and function of the P2X(7) receptor in rat C6 glioma cells. Cancer Lett 260(1–2):79–87. doi:10.1016/j.canlet.2007.10.025

    PubMed  CAS  Google Scholar 

  89. Jelassi B, Chantome A, Alcaraz-Perez F, Baroja-Mazo A, Cayuela ML, Pelegrin P, Surprenant A, Roger S (2011) P2X(7) receptor activation enhances SK3 channels- and cystein cathepsin-dependent cancer cells invasiveness. Oncogene 30(18):2108–2122. doi:10.1038/onc.2010.593

    PubMed  CAS  Google Scholar 

  90. Miki K, Tanaka H, Nagai Y, Kimura C, Oike M (2010) Transforming growth factor β1 alters calcium mobilizing properties and endogenous ATP release in A549 cells: possible implications for cell migration. J Pharmacol Sci: 1007220420. doi:10.1254/jphs.10124FP

  91. Chi SL, Wahl ML, Mowery YM, Shan S, Mukhopadhyay S, Hilderbrand SC, Kenan DJ, Lipes BD, Johnson CE, Marusich MF, Capaldi RA, Dewhirst MW, Pizzo SV (2007) Angiostatin-like activity of a monoclonal antibody to the catalytic subunit of F1F0 ATP synthase. Cancer Res 67(10):4716–4724. doi:10.1158/0008-5472.CAN-06-1094

    PubMed  CAS  Google Scholar 

  92. Wang L, Zhou X, Zhou T, Ma D, Chen S, Zhi X, Yin L, Shao Z, Ou Z, Zhou P (2008) Ecto-5′-nucleotidase promotes invasion, migration and adhesion of human breast cancer cells. J Cancer Res Clin Oncol 134(3):365–372. doi:10.1007/s00432-007-0292-z

    PubMed  CAS  Google Scholar 

  93. Stagg J, Divisekera U, McLaughlin N, Sharkey J, Pommey S, Denoyer D, Dwyer KM, Smyth MJ (2010) Anti-CD73 antibody therapy inhibits breast tumor growth and metastasis. Proc Natl Acad Sci U S A 107(4):1547–1552. doi:10.1073/pnas.0908801107

    PubMed  CAS  Google Scholar 

  94. Richard CL, Tan EY, Blay J (2006) Adenosine upregulates CXCR4 and enhances the proliferative and migratory responses of human carcinoma cells to CXCL12/SDF-1α. Int J Cancer 119(9):2044–2053. doi:10.1002/ijc.22084

    PubMed  CAS  Google Scholar 

  95. Stracke ML, Krutzsch HC, Unsworth EJ, Arestad A, Cioce V, Schiffmann E, Liotta LA (1992) Identification, purification, and partial sequence analysis of autotaxin, a novel motility-stimulating protein. J Biol Chem 267(4):2524–2529

    PubMed  CAS  Google Scholar 

  96. Ptaszynska MM, Pendrak ML, Stracke ML, Roberts DD (2010) Autotaxin signaling via lysophosphatidic acid receptors contributes to vascular endothelial growth factor-induced endothelial cell migration. Mol Cancer Res 8(3):309–321. doi:10.1158/1541-7786.MCR-09-0288

    PubMed  CAS  Google Scholar 

  97. Panupinthu N, Lee HY, Mills GB (2010) Lysophosphatidic acid production and action: critical new players in breast cancer initiation and progression. Br J Cancer 102(6):941–946. doi:10.1038/sj.bjc.6605588

    PubMed  CAS  Google Scholar 

  98. Hirakawa M, Oike M, Karashima Y, Ito Y (2004) Sequential activation of RhoA and FAK/paxillin leads to ATP release and actin reorganization in human endothelium. J Physiol 558(Pt 2):479–488. doi:10.1113/jphysiol.2004.065334jphysiol.2004.065334

    PubMed  CAS  Google Scholar 

  99. Roussos ET, Condeelis JS, Patsialou A (2011) Chemotaxis in cancer. Nat Rev Cancer 11 (8):573–587

    Google Scholar 

  100. Quezada SA, Peggs KS, Simpson TR, Allison JP (2011) Shifting the equilibrium in cancer immunoediting: from tumor tolerance to eradication. Immunol Rev 241 (1):104–118. doi:10.1111/j.1600-065X.2011.01007.x

    Google Scholar 

  101. Schuster M, Nechansky A, Kircheis R (2006) Cancer immunotherapy. Biotechnol J 1(2):138–147. doi:10.1002/biot.200500044

    PubMed  CAS  Google Scholar 

  102. Barreiro O, Martin P, Gonzalez-Amaro R, Sanchez-Madrid F (2010) Molecular cues guiding inflammatory responses. Cardiovasc Res 86(2):174–182. doi:10.1093/cvr/cvq001

    PubMed  CAS  Google Scholar 

  103. Birmingham JM, Busik JV, Hansen-Smith FM, Fenton JI (2009) Novel mechanism for obesity-induced colon cancer progression. Carcinogenesis 30(4):690–697. doi:10.1093/carcin/bgp041

    PubMed  CAS  Google Scholar 

  104. Velnar T, Bailey T, Smrkolj V (2009) The wound healing process: an overview of the cellular and molecular mechanisms. J Int Med Res 37(5):1528–1542

    PubMed  CAS  Google Scholar 

  105. Aman A, Piotrowski T (2010) Cell migration during morphogenesis. Dev Biol 341(1):20–33

    PubMed  CAS  Google Scholar 

  106. Chung WC, Kermode JC (2005) Suramin disrupts receptor-G protein coupling by blocking association of G protein alpha and betagamma subunits. J Pharmacol Exp Ther 313(1):191–198. doi:10.1124/jpet.104.078311

    PubMed  CAS  Google Scholar 

  107. Feng Y, Li M, Wang B, Zheng YG (2010) Discovery and mechanistic study of a class of protein arginine methylation inhibitors. J Med Chem 53(16):6028–6039. doi:10.1021/jm100416n

    PubMed  CAS  Google Scholar 

  108. Zengel P, Nguyen-Hoang A, Schildhammer C, Zantl R, Kahl V, Horn E (2011) mu-Slide chemotaxis: a new chamber for long-term chemotaxis studies. BMC Cell Biol 12(1):21. doi:10.1186/1471-2121-12-21

    PubMed  Google Scholar 

  109. Zigmond SH, Foxman EF, Segall JE (2001) Chemotaxis assays for eukaryotic cells. In: Current protocols in cell biology. John Wiley & Sons, Inc. doi:10.1002/0471143030.cb1201s00

  110. Seror C, Melki MT, Subra F, Raza SQ, Bras M, Saidi H, Nardacci R, Voisin L, Paoletti A, Law F, Martins I, Amendola A, Abdul-Sater AA, Ciccosanti F, Delelis O, Niedergang F, Thierry S, Said-Sadier N, Lamaze C, Metivier D, Estaquier J, Fimia GM, Falasca L, Casetti R, Modjtahedi N, Kanellopoulos J, Mouscadet JF, Ojcius DM, Piacentini M, Gougeon ML, Kroemer G, Perfettini JL (2011) Extracellular ATP acts on P2Y2 purinergic receptors to facilitate HIV-1 infection. J Exp Med 208(9):1823–1834. doi:10.1084/jem.20101805

    PubMed  CAS  Google Scholar 

  111. Tanneur V, Duranton C, Brand VB, Sandu CD, Akkaya C, Kasinathan RS, Gachet C, Sluyter R, Barden JA, Wiley JS, Lang F, Huber SM (2006) Purinoceptors are involved in the induction of an osmolyte permeability in malaria-infected and oxidized human erythrocytes. FASEB J 20(1):133–135. doi:10.1096/fj.04-3371fje

    PubMed  CAS  Google Scholar 

  112. Mackay CR (2008) Moving targets: cell migration inhibitors as new anti-inflammatory therapies. Nat Immunol 9(9):988–998

    PubMed  CAS  Google Scholar 

  113. Striedinger K, Meda P, Scemes E (2007) Exocytosis of ATP from astrocyte progenitors modulates spontaneous Ca2+ oscillations and cell migration. Glia 55(6):652–662. doi:10.1002/glia.20494

    PubMed  Google Scholar 

  114. Braun OO, Lu D, Aroonsakool N, Insel PA (2010) Uridine triphosphate (UTP) induces profibrotic responses in cardiac fibroblasts by activation of P2Y2 receptors. J Mol Cell Cardiol 49(3):362–369. doi:10.1016/j.yjmcc.2010.05.001

    PubMed  CAS  Google Scholar 

  115. Mayo C, Ren R, Rich C, Stepp MA, Trinkaus-Randall V (2008) Regulation by P2X7: epithelial migration and stromal organization in the cornea. Invest Ophthalmol Vis Sci 49(10):4384–4391. doi:10.1167/iovs.08-1688

    PubMed  Google Scholar 

  116. Crooke A, Mediero A, Guzman-Aranguez A, Pintor J (2009) Silencing of P2Y2 receptor delays Ap4A-corneal re-epithelialization process. Mol Vis 15:1169–1178

    PubMed  CAS  Google Scholar 

  117. Boucher I, Rich C, Lee A, Marcincin M, Trinkaus-Randall V (2010) The P2Y2 receptor mediates the epithelial injury response and cell migration. Am J Physiol Cell Physiol 299(2):C411–C421. doi:10.1152/ajpcell.00100.2009

    PubMed  CAS  Google Scholar 

  118. Vanderstocken G, Bondue B, Horckmans M, Di Pietrantonio L, Robaye B, Boeynaems JM, Communi D (2010) P2Y2 receptor regulates VCAM-1 membrane and soluble forms and eosinophil accumulation during lung inflammation. J Immunol 185(6):3702–3707. doi:10.4049/jimmunol.0903908

    PubMed  CAS  Google Scholar 

  119. Kobayashi T, Kouzaki H, Kita H (2010) Human eosinophils recognize endogenous danger signal crystalline uric acid and produce proinflammatory cytokines mediated by autocrine ATP. J Immunol 184(11):6350–6358. doi:10.4049/jimmunol.0902673

    PubMed  CAS  Google Scholar 

  120. Hess CN, Kou R, Johnson RP, Li GK, Michel T (2009) ADP signaling in vascular endothelial cells. J Biol Chem 284(47):32209–32224. doi:10.1074/jbc.M109.032656

    PubMed  CAS  Google Scholar 

  121. Tagami M, Kusuhara S, Imai H, Uemura A, Honda S, Tsukahara Y, Negi A (2010) MRP4 knockdown enhances migration, suppresses apoptosis, and produces aggregated morphology in human retinal vascular endothelial cells. Biochem Biophys Res Commun 400(4):593–598. doi:10.1016/j.bbrc.2010.08.109

    PubMed  CAS  Google Scholar 

  122. Rossi L, Manfredini R, Bertolini F, Ferrari D, Fogli M, Zini R, Salati S, Salvestrini V, Gulinelli S, Adinolfi E, Ferrari S, Di Virgilio F, Baccarani M, Lemoli RM (2007) The extracellular nucleotide UTP is a potent inducer of hematopoietic stem cell migration. Blood 109(2):533–542. doi:10.1182/blood-2006-01-035634

    PubMed  CAS  Google Scholar 

  123. Hashmi AZ, Hakim W, Kruglov EA, Watanabe A, Watkins W, Dranoff JA, Mehal WZ (2007) Adenosine inhibits cytosolic calcium signals and chemotaxis in hepatic stellate cells. Am J Physiol Gastrointest Liver Physiol 292(1):G395–G401. doi:10.1152/ajpgi.00208.2006

    PubMed  CAS  Google Scholar 

  124. Andrade CM, Lopez PL, Noronha BT, Wink MR, Borojevic R, Margis R, Lenz G, Battastini AM, Guma FC (2011) Ecto-5′-nucleotidase/CD73 knockdown increases cell migration and mRNA level of collagen I in a hepatic stellate cell line. Cell Tissue Res 344(2):279–286. doi:10.1007/s00441-011-1140-7

    PubMed  CAS  Google Scholar 

  125. Giltaire S, Lambert S, Poumay Y (2011) HB-EGF synthesis and release induced by cholesterol depletion of human epidermal keratinocytes is controlled by extracellular atp and involves both p38 and ERK1/2 signaling pathways. J Cell Physiol 226(6):1651–1659. doi:10.1002/jcp.22496

    PubMed  CAS  Google Scholar 

  126. Taboubi S, Milanini J, Delamarre E, Parat F, Garrouste F, Pommier G, Takasaki J, Hubaud JC, Kovacic H, Lehmann M (2007) G alpha(q/11)-coupled P2Y2 nucleotide receptor inhibits human keratinocyte spreading and migration. FASEB J 21(14):4047–4058. doi:10.1096/fj.06-7476com

    PubMed  CAS  Google Scholar 

  127. Taboubi S, Garrouste F, Parat F, Pommier G, Faure E, Monferran S, Kovacic H, Lehmann M (2010) Gq-coupled purinergic receptors inhibit insulin-like growth factor-I/phosphoinositide 3-kinase pathway-dependent keratinocyte migration. Mol Biol Cell 21(6):946–955. doi:10.1091/mbc.E09-06-0497

    PubMed  CAS  Google Scholar 

  128. Lin C, Ren S, Zhang L, Jin H, Sun J, Zuo Y (2011) Extracellular ATP induces CD44 shedding from macrophage-like P388D1 cells via the P2X7 receptor. Hematol Oncol. doi:10.1002/hon.1008

  129. Martins JP, Silva RB, Coutinho-Silva R, Takiya CM, Battastini AM, Morrone FB, Campos MM (2011) P2X7 purinergic receptor and its role in inflammatory and nociceptive alterations associated to cyclophosphamide-induced hemorrhagic cystitis in mice. Br J Pharmacol. doi:10.1111/j.1476-5381.2011.01535.x

  130. Koroskenyi K, Duro E, Pallai A, Sarang Z, Kloor D, Ucker DS, Beceiro S, Castrillo A, Chawla A, Ledent CA, Fesus L, Szondy Z (2011) Involvement of adenosine A2A receptors in engulfment-dependent apoptotic cell suppression of inflammation. J Immunol 186(12):7144–7155. doi:10.4049/jimmunol.1002284

    PubMed  CAS  Google Scholar 

  131. Williams AJ, Cronstein BN (2011) The Effect of A(2A) adenosine receptor activation on C-C chemokine receptor 7 expression in human THP1 macrophages during inflammation. Inflammation. doi:10.1007/s10753-011-9353-1

  132. Ode A, Kopf J, Kurtz A, Schmidt-Bleek K, Schrade P, Kolar P, Buttgereit F, Lehmann K, Hutmacher DW, Duda GN, Kasper G (2011) CD73 and CD29 concurrently mediate the mechanically induced decrease of migratory capacity of mesenchymal stromal cells. Eur Cell Mater 22:26–42

    PubMed  CAS  Google Scholar 

  133. Ohsawa K, Irino Y, Nakamura Y, Akazawa C, Inoue K, Kohsaka S (2007) Involvement of P2X4 and P2Y12 receptors in ATP-induced microglial chemotaxis. Glia 55(6):604–616. doi:10.1002/glia.20489

    PubMed  Google Scholar 

  134. Ben Yebdri F, Kukulski F, Tremblay A, Sévigny J (2009) Concomitant activation of P2Y2 and P2Y6 receptors on monocytes is required for TLR1/2-induced neutrophil migration by regulating IL-8 secretion. Eur J Immunol 39(10):2885–2894. doi:10.1002/eji.200939347

    PubMed  CAS  Google Scholar 

  135. Gorini S, Callegari G, Romagnoli G, Mammi C, Mavilio D, Rosano G, Fini M, Di Virgilio F, Gulinelli S, Falzoni S, Cavani A, Ferrari D, la Sala A (2010) ATP secreted by endothelial cells blocks CXCL 1-elicited natural killer cell chemotaxis and cytotoxicity via P2Y receptor activation. Blood 116(22):4492–4500. doi:10.1182/blood-2009-12-260828

    PubMed  CAS  Google Scholar 

  136. Liu X, Hashimoto-Torii K, Torii M, Haydar TF, Rakic P (2008) The role of ATP signaling in the migration of intermediate neuronal progenitors to the neocortical subventricular zone. Proc Natl Acad Sci USA 105(33):11802–11807. doi:10.1073/pnas.0805180105

    PubMed  CAS  Google Scholar 

  137. 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(2):181–189. doi:10.1111/j.1748-1716.2010.02092.x

    CAS  Google Scholar 

  138. Kukulski F, Ben Yebdri F, Bahrami F, Levesque SA, Martin-Satue M, Sevigny J (2010) The P2 receptor antagonist PPADS abrogates LPS-induced neutrophil migration in the murine air pouch via inhibition of MIP-2 and KC production. Mol Immunol 47(4):833–839. doi:10.1016/j.molimm.2009.09.037

    PubMed  CAS  Google Scholar 

  139. Hyman MC, Petrovic-Djergovic D, Visovatti SH, Liao H, Yanamadala S, Bouis D, Su EJ, Lawrence DA, Broekman MJ, Marcus AJ, Pinsky DJ (2009) Self-regulation of inflammatory cell trafficking in mice by the leukocyte surface apyrase CD39. J Clin Invest 119(5):1136–1149. doi:10.1172/JCI36433

    PubMed  CAS  Google Scholar 

  140. Reutershan J, Cagnina RE, Chang D, Linden J, Ley K (2007) Therapeutic anti-inflammatory effects of myeloid cell adenosine receptor A2a stimulation in lipopolysaccharide-induced lung injury. J Immunol 179(2):1254–1263

    PubMed  CAS  Google Scholar 

  141. Ando K, Obara Y, Sugama J, Kotani A, Koike N, Ohkubo S, Nakahata N (2010) P2Y2 receptor-Gq/11 signaling at lipid rafts is required for UTP-induced cell migration in NG 108–15 cells. J Pharmacol Exp Ther. doi:10.1124/jpet.110.167528

  142. Agresti C, Meomartini ME, Amadio S, Ambrosini E, Serafini B, Franchini L, Volonte C, Aloisi F, Visentin S (2005) Metabotropic P2 receptor activation regulates oligodendrocyte progenitor migration and development. Glia 50(2):132–144. doi:10.1002/glia.20160

    PubMed  CAS  Google Scholar 

  143. Omatsu-Kanbe M, Inoue K, Fujii Y, Yamamoto T, Isono T, Fujita N, Matsuura H (2006) Effect of ATP on preadipocyte migration and adipocyte differentiation by activating P2Y receptors in 3T3-L1 cells. Biochem J 393(Pt 1):171–180. doi:10.1042/BJ20051037

    PubMed  CAS  Google Scholar 

  144. Klawitter S, Hofmann LP, Pfeilschifter J, Huwiler A (2007) Extracellular nucleotides induce migration of renal mesangial cells by upregulating sphingosine kinase-1 expression and activity. Br J Pharmacol 150(3):271–280. doi:10.1038/sj.bjp.0706983

    PubMed  CAS  Google Scholar 

  145. Lin CC, Lin WN, Cheng SE, Tung WH, Wang HH, Yang CM (2011) Transactivation of EGFR/PI3K/Akt involved in ATP-induced inflammatory protein expression and cell motility. J Cell Physiol. doi:10.1002/jcp.22880

  146. Yu N, Erb L, Shivaji R, Weisman GA, Seye CI (2008) Binding of the P2Y2 nucleotide receptor to filamin A regulates migration of vascular smooth muscle cells. Circ Res 102(5):581–588. doi:10.1161/CIRCRESAHA.107.162271

    PubMed  CAS  Google Scholar 

  147. Harada K, Matsumoto Y, Umemura K (2011) Adenosine diphosphate receptor P2Y12-mediated migration of host smooth muscle-like cells and leukocytes in the development of transplant arteriosclerosis. Transplantation 92(2):148–154. doi:10.1097/TP.0b013e318221d407

    PubMed  CAS  Google Scholar 

  148. Behdad A, Sun X, Khalpey Z, Enjyoji K, Wink M, Wu Y, Usheva A, Robson S (2009) Vascular smooth muscle cell expression of ectonucleotidase CD39 (ENTPD1) is required for neointimal formation in mice. Purinergic Signalling 5(3):335–342. doi:10.1007/s11302-009-9158-y

    PubMed  CAS  Google Scholar 

  149. Burnett LA, Blais EM, Unadkat JD, Hille B, Tilley SL, Babcock DF (2010) Testicular expression of Adora3i2 in Adora3 knockout mice reveals a role of mouse A3Ri2 and human A3Ri3 adenosine receptors in sperm. J Biol Chem 285(44):33662–33670. doi:10.1074/jbc.M110.156075

    PubMed  CAS  Google Scholar 

  150. Rodriguez-Miranda E, Buffone MG, Edwards SE, Ord TS, Lin K, Sammel MD, Gerton GL, Moss SB, Williams CJ (2008) Extracellular adenosine 5′-triphosphate alters motility and improves the fertilizing capability of mouse sperm. Biol Reprod 79(1):164–171. doi:10.1095/biolreprod.107.065565

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Cell Signalling, University of Nottingham, Nottingham, UK

    Ross Corriden

  2. Departments of Pharmacology and Medicine, University of California, San Diego, CA, USA

    Paul A. Insel

  3. Department of Pharmacology, University of California San Diego, 9500 Gilman Drive, Mail code 0636, La Jolla, CA, 92093, USA

    Paul A. Insel

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  1. Ross Corriden
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Correspondence to Paul A. Insel.

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Work in the authors’ laboratories is supported by grants from the NIH and the MRC.

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Corriden, R., Insel, P.A. New insights regarding the regulation of chemotaxis by nucleotides, adenosine, and their receptors. Purinergic Signalling 8, 587–598 (2012). https://doi.org/10.1007/s11302-012-9311-x

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