Role of adenosine signalling and metabolism in β-cell regeneration

Experimental Cell Research

Volumn 321, Issue 1, 2014, Pages 3-10

  Andersson, Olov ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Adenosine; ATP; Diabetes; Insulin; Proliferation; Regeneration; Cell

Indexed keywords

ADENOSINE; ADENOSINE DIPHOSPHATE; ADENOSINE RECEPTOR; ADENOSINE TRIPHOSPHATE; C PEPTIDE; CALCIUM; CYCLIC AMP; GLUCOSE; PHOSPHODIESTERASE III; PROINSULIN; TEPLIZUMAB;

CD8+ T LYMPHOCYTE; CELL DEATH; CELL HOMEOSTASIS; CELL PROLIFERATION; CELL REGENERATION; CELL SURVIVAL; CELL TRANSDIFFERENTIATION; ENDOPLASMIC RETICULUM STRESS; GLUCOSE HOMEOSTASIS; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RELEASE; INTRACELLULAR SIGNALING; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; REVIEW;

ADENOSINE; ATP; DIABETES; INSULIN; PROLIFERATION; REGENERATION; Β CELL;

ADENOSINE; ANIMALS; DIABETES MELLITUS; HUMANS; INSULIN-SECRETING CELLS; REGENERATION; SIGNAL TRANSDUCTION;

EID: 84892513484     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.11.019     Document Type: Review

References (53)

1. Ackermann A.M., Gannon M. Molecular regulation of pancreatic beta-cell mass development, maintenance, and expansion. J. Mol. Endocrinol. 2007, 38:193-206.
2. Al-Hasani K., Pfeifer A., Courtney M., Ben-Othman N., Gjernes E., Vieira A., Druelle N., Avolio F., Ravassard P., Leuckx G., Lacas-Gervais S., Ambrosetti D., Benizri E., Hecksher-Sorensen J., Gounon P., Ferrer J., Gradwohl G., Heimberg H., Mansouri A., Collombat P. Adult duct-lining cells can reprogram into beta-like cells able to counter repeated cycles of toxin-induced diabetes. Dev. Cell 2013, 26:86-100.
3. Andersson O., Adams B.A., Yoo D., Ellis G.C., Gut P., Anderson R.M., German M.S., Stainier D.Y. Adenosine signaling promotes regeneration of pancreatic beta cells in vivo. Cell Metab. 2012, 15:885-894.
4. Annes J.P., Ryu J.H., Lam K., Carolan P.J., Utz K., Hollister-Lock J., Arvanites A.C., Rubin L.L., Weir G., Melton D.A. Adenosine kinase inhibition selectively promotes rodent and porcine islet beta-cell replication. Proc. Nat. Acad. Sci. U.S.A. 2012, 109:3915-3920.
5. Arda H.E., Benitez C.M., Kim S.K. Gene regulatory networks governing pancreas development. Dev. Cell 2013, 25:5-13.
6. Assmann A., Ueki K., Winnay J.N., Kadowaki T., Kulkarni R.N. Glucose effects on beta-cell growth and survival require activation of insulin receptors and insulin receptor substrate 2. Mol. Cell. Biol. 2009, 29:3219-3228.
7. Augusto E., Matos M., Sevigny J., El-Tayeb A., Bynoe M.S., Muller C.E., Cunha R.A., Chen J.F. Ecto-5'-nucleotidase (CD73)-mediated formation of adenosine is critical for the striatal adenosine A2A receptor functions. J. Neurosci.the official journal of the Society for Neuroscience 2013, 33:11390-11399.
8. Balasubramanian R., Ruiz de Azua I., Wess J., Jacobson K.A. Activation of distinct P2Y receptor subtypes stimulates insulin secretion in MIN6 mouse pancreatic beta cells. Biochem. Pharmacol. 2010, 79:1317-1326.
9. Bjursell M.K., Blom H.J., Cayuela J.A., Engvall M.L., Lesko N., Balasubramaniam S., Brandberg G., Halldin M., Falkenberg M., Jakobs C., Smith D., Struys E., von Dobeln U., Gustafsson C.M., Lundeberg J., Wedell A. Adenosine kinase deficiency disrupts the methionine cycle and causes hypermethioninemia, encephalopathy, and abnormal liver function. Am. J. Hum. Genet. 2011, 89:507-515.
10. Bonner-Weir S., Li W.C., Ouziel-Yahalom L., Guo L., Weir G.C., Sharma A. Beta-cell growth and regeneration: replication is only part of the story. Diabetes 2010, 59:2340-2348.
11. Burnstock G., Novak I. Purinergic signalling and diabetes. Purinergic Signal. 2013.
12. Butler A.E., Janson J., Bonner-Weir S., Ritzel R., Rizza R.A., Butler P.C. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 2003, 52:102-110.
13. Chen D., Errey J.C., Heitman L.H., Marshall F.H., Ijzerman A.P., Siegal G. Fragment screening of GPCRs using biophysical methods: identification of ligands of the adenosine A(2A) receptor with novel biological activity. ACS Chem. Biol. 2012, 7:2064-2073.
14. Chen J.F., Eltzschig H.K., Fredholm B.B. Adenosine receptors as drug targets-what are the challenges?. Nat. Rev. Drug Discovery 2013, 12:265-286.
15. Chhabra, P., Wang, K., Zeng, Q., Jecmenica, M., Langman, L., Linden, J., Ketchum, R.J., Brayman, K.L. Adenosine A(2A) agonist administration improves islet transplant outcome: evidence for the role of innate immunity in islet graft rejection. Cell Transplant. 19, 597-612.
16. Chia J.S., McRae J.L., Thomas H.E., Fynch S., Elkerbout L., Hill P., Murray-Segal L., Robson S.C., Chen J.F., d'Apice A.J., Cowan P.J., Dwyer K.M. The protective effects of CD39 overexpression in multiple low-dose streptozotocin-induced diabetes in mice. Diabetes 2013, 62:2026-2035.
17. Choi Y.H., Park S., Hockman S., Zmuda-Trzebiatowska E., Svennelid F., Haluzik M., Gavrilova O., Ahmad F., Pepin L., Napolitano M., Taira M., Sundler F., Stenson Holst L., Degerman E., Manganiello V.C. Alterations in regulation of energy homeostasis in cyclic nucleotide phosphodiesterase 3B-null mice. J. Clin. Invest. 2006, 116:3240-3251.
18. Cui X.A., Singh B., Park J., Gupta R.S. Subcellular localization of adenosine kinase in mammalian cells: the long isoform of AdK is localized in the nucleus. Biochem. Biophys. Res. Commun. 2009, 388:46-50.
19. Dor Y., Brown J., Martinez O.I., Melton D.A. Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 2004, 429:41-46.
20. Dunwiddie T.V., Diao L. Extracellular adenosine concentrations in hippocampal brain slices and the tonic inhibitory modulation of evoked excitatory responses. J. Pharmacol. Exp. Ther. 1994, 268:537-545.
21. Eliasson L., Ma X., Renstrom E., Barg S., Berggren P.O., Galvanovskis J., Gromada J., Jing X., Lundquist I., Salehi A., Sewing S., Rorsman P. SUR1 regulates PKA-independent cAMP-induced granule priming in mouse pancreatic B-cells. J. Gen. Physiol. 2003, 121:181-197.
22. Figler, R.A., Wang, G., Srinivasan, S., Jung, D.Y., Zhang, Z., Pankow, J.S., Ravid, K., Fredholm, B., Hedrick, C.C., Rich, S.S., Kim, J.K., LaNoue, K.F., Linden, J. Links between insulin resistance, adenosine A2B receptors, and inflammatory markers in mice and humans. Diabetes 60, 669-679.
23. Fitz J.G. Regulation of cellular ATP release. Trans. Am. Clin. Climatol. Assoc. 2007, 118:199-208.
24. Glas R., Sauter N.S., Schulthess F.T., Shu L., Oberholzer J., Maedler K. Purinergic P2×7 receptors regulate secretion of interleukin-1 receptor antagonist and beta cell function and survival. Diabetologia 2009, 52:1579-1588.
25. Hanley S.C., Austin E., Assouline-Thomas B., Kapeluto J., Blaichman J., Moosavi M., Petropavlovskaia M., Rosenberg L. {beta}-Cell mass dynamics and islet cell plasticity in human type 2 diabetes. Endocrinology 2010, 151:1462-1472.
26. Hazama A., Hayashi S., Okada Y. Cell surface measurements of ATP release from single pancreatic beta cells using a novel biosensor technique. Pflugers Arch., Eur. J. Physiol. 1998, 437:31-35.
27. Heit J.J., Apelqvist A.A., Gu X., Winslow M.M., Neilson J.R., Crabtree G.R., Kim S.K. Calcineurin/NFAT signalling regulates pancreatic beta-cell growth and function. Nature 2006, 443:345-349.
28. Herold K.C., Gitelman S.E., Ehlers M.R., Gottlieb P.A., Greenbaum C.J., Hagopian W., Boyle K.D., Keyes-Elstein L., Aggarwal S., Phippard D., Sayre P.H., McNamara J., Bluestone J.A. Teplizumab (anti-CD3 mAb) treatment preserves C-peptide responses in patients with new-onset type 1 diabetes in a randomized controlled trial: metabolic and immunologic features at baseline identify a subgroup of responders. Diabetes 2013, 62:3766-3774.
29. Hussain M.A., Porras D.L., Rowe M.H., West J.R., Song W.J., Schreiber W.E., Wondisford F.E. Increased pancreatic beta-cell proliferation mediated by CREB binding protein gene activation. Mol. Cell. Biol. 2006, 26:7747-7759.
30. Imai Y., Dobrian A.D., Morris M.A., Nadler J.L. Islet inflammation: a unifying target for diabetes treatment?. Trends Endocrinol. Metab. 2013, 24:351-360.
31. Jacques-Silva M.C., Correa-Medina M., Cabrera O., Rodriguez-Diaz R., Makeeva N., Fachado A., Diez J., Berman D.M., Kenyon N.S., Ricordi C., Pileggi A., Molano R.D., Berggren P.O., Caicedo A. ATP-gated P2×3 receptors constitute a positive autocrine signal for insulin release in the human pancreatic beta cell. Proc. Nat. Acad. Sci. U.S.A. 2010, 107:6465-6470.
32. Kassem S., Bhandari S., Rodriguez-Bada P., Motaghedi R., Heyman M., Garcia-Gimeno M.A., Cobo-Vuilleumier N., Sanz P., Maclaren N.K., Rahier J., Glaser B., Cuesta-Munoz A.L. Large islets, beta-cell proliferation, and a glucokinase mutation. N. Engl. J. Med. 2010, 362:1348-1350.
33. Koupenova M., Ravid K. Adenosine, adenosine receptors and their role in glucose homeostasis and lipid metabolism. J. Cell. Physiol. 2013.
34. Levitt H.E., Cyphert T.J., Pascoe J.L., Hollern D.A., Abraham N., Lundell R.J., Rosa T., Romano L.C., Zou B., O'Donnell C.P., Stewart A.F., Garcia-Ocana A., Alonso L.C. Glucose stimulates human beta cell replication in vivo in islets transplanted into NOD-severe combined immunodeficiency (SCID) mice. Diabetologia 2011, 54:572-582.
35. Liu B., Barbosa-Sampaio H., Jones P.M., Persaud S.J., Muller D.S. The CaMK4/CREB/IRS-2 cascade stimulates proliferation and inhibits apoptosis of beta-cells. PLoS One 2012, 7:e45711.
36. Metukuri M.R., Zhang P., Basantani M.K., Chin C., Stamateris R.E., Alonso L.C., Takane K.K., Gramignoli R., Strom S.C., O'Doherty R.M., Stewart A.F., Vasavada R.C., Garcia-Ocana A., Scott D.K. ChREBP mediates glucose-stimulated pancreatic beta-cell proliferation. Diabetes 2012, 61:2004-2015.
37. Mondal B.C., Mukherjee T., Mandal L., Evans C.J., Sinenko S.A., Martinez-Agosto J.A., Banerjee U. Interaction between differentiating cell- and niche-derived signals in hematopoietic progenitor maintenance. Cell 2011, 147:1589-1600.
38. Nakamura A., Terauchi Y., Ohyama S., Kubota J., Shimazaki H., Nambu T., Takamoto I., Kubota N., Eiki J., Yoshioka N., Kadowaki T., Koike T. Impact of small-molecule glucokinase activator on glucose metabolism and beta-cell mass. Endocrinology 2009, 150:1147-1154.
39. Nemeth Z.H., Bleich D., Csoka B., Pacher P., Mabley J.G., Himer L., Vizi E.S., Deitch E.A., Szabo C., Cronstein B.N., Hasko G. Adenosine receptor activation ameliorates type 1 diabetes. FASEB J. 2007, 21:2379-2388.
40. Nitta T., Itoh T., Matsuoka N., Mera T., Kojima D., Nakano M., Yamashita Y., Yasunami Y. Prevention of early loss of transplanted islets in the liver of mice by adenosine. Transplantation 2009, 88:49-56.
41. Pan F.C., Wright C. Pancreas organogenesis: from bud to plexus to gland. Dev. Dyn. 2011, 240:530-565.
42. Porat S., Weinberg-Corem N., Tornovsky-Babaey S., Schyr-Ben-Haroush R., Hija A., Stolovich-Rain M., Dadon D., Granot Z., Ben-Hur V., White P., Girard C.A., Karni R., Kaestner K.H., Ashcroft F.M., Magnuson M.A., Saada A., Grimsby J., Glaser B., Dor Y. Control of pancreatic beta cell regeneration by glucose metabolism. Cell Metab. 2011, 13:440-449.
43. Rahier J., Guiot Y., Goebbels R.M., Sempoux C., Henquin J.C. Pancreatic beta-cell mass in European subjects with type 2 diabetes. Diabetes Obes. Metab. 2008, 10(Suppl. 4):32-42.
44. Ravassard P., Hazhouz Y., Pechberty S., Bricout-Neveu E., Armanet M., Czernichow P., Scharfmann R. A genetically engineered human pancreatic beta cell line exhibiting glucose-inducible insulin secretion. J. Clin. Invest. 2011, 121:3589-3597.
45. Roep B.O., Solvason N., Gottlieb P.A., Abreu J.R., Harrison L.C., Eisenbarth G.S., Yu L., Leviten M., Hagopian W.A., Buse J.B., von Herrath M., Quan J., King R.S., Robinson W.H., Utz P.J., Garren H., Steinman L. Plasmid-encoded proinsulin preserves C-peptide while specifically reducing proinsulin-specific CD8+T cells in type 1 diabetes. Sci. Transl. Med. 2013, 5. (191ra182).
46. Salpeter S.J., Klein A.M., Huangfu D., Grimsby J., Dor Y. Glucose and aging control the quiescence period that follows pancreatic beta cell replication. Development 2010, 137:3205-3213.
47. Stanger B.Z., Hebrok M. Control of cell identity in pancreas development and regeneration. Gastroenterology 2013, 144:1170-1179.
48. Thorel F., Nepote V., Avril I., Kohno K., Desgraz R., Chera S., Herrera P.L. Conversion of adult pancreatic alpha-cells to beta-cells after extreme beta-cell loss. Nature 2010, 464:1149-1154.
49. Weir G.C., Bonner-Weir S. Islet beta cell mass in diabetes and how it relates to function, birth, and death. Ann. N. Y. Acad. Sci. 2013, 1281:92-105.
50. Williams-Karnesky R.L., Sandau U.S., Lusardi T.A., Lytle N.K., Farrell J.M., Pritchard E.M., Kaplan D.L., Boison D. Epigenetic changes induced by adenosine augmentation therapy prevent epileptogenesis. J. Clin. Invest. 2013.
51. Xu F., Wu H., Katritch V., Han G.W., Jacobson K.A., Gao Z.G., Cherezov V., Stevens R.C. Structure of an agonist-bound human A2A adenosine receptor. Science 2011, 332:322-327.
52. Yan L., Burbiel J.C., Maass A., Muller C.E. Adenosine receptor agonists: from basic medicinal chemistry to clinical development. Expert Opin. Emerg. Drugs 2003, 8:537-576.
53. Ziv O., Glaser B., Dor Y. The plastic pancreas. Dev. Cell 2013, 26:3-7.