Mechanism of metformin: Inhibition of DNA damage and proliferative activity in Drosophila midgut stem cell

Mechanisms of Ageing and Development

Volumn 134, Issue 9, 2013, Pages 381-390

  Na, Hyun Jin ^a   Park, Joung Sun ^a   Pyo, Jung Hoon ^a   Lee, Shin Hae ^a   Jeon, Ho Jun ^a   Kim, Young Shin ^a   Yoo, Mi Ae ^a  

^a Pusan National University   (South Korea)

Author keywords

Aging; DNA damage; Drosophila; Intestinal stem cells; Metformin

Indexed keywords

METFORMIN; PROTEIN KINASE B;

AGE; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; DROSOPHILA; DRUG MECHANISM; ENZYME ACTIVITY; GENE EXPRESSION; GENOMIC INSTABILITY; IMMUNOCHEMISTRY; MIDGUT; MIDGUT STEM CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; STEM CELL; TRANSGENE;

AGING; DNA DAMAGE; DROSOPHILA; INTESTINAL STEM CELLS; METFORMIN;

AGING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BROMODEOXYURIDINE; CELL AGING; CELL PROLIFERATION; DNA DAMAGE; DROSOPHILA; FEMALE; GREEN FLUORESCENT PROTEINS; HYPOGLYCEMIC AGENTS; INTESTINES; MALE; METFORMIN; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; STEM CELLS; TEMPERATURE;

EID: 84885861971     PISSN: 00476374     EISSN: 18726216     Source Type: Journal    
DOI: 10.1016/j.mad.2013.07.003     Document Type: Article

References (57)

1. Algire C., Amrein L., Zakikhani M., Panasci L., Pollak M. Metformin blocks the stimulative effect of a high-energy diet on colon carcinoma growth in vivo and is associated with reduced expression of fatty acid synthase. Endocrine-Related Cancer 2010, 17:351-360.
2. Algire C., Moiseeva O., Deschenes-Simard X., Amrein L., Petruccelli L., Birman E., Viollet B., Ferbeyre G., Pollak M.N. Metformin reduces endogenous reactive oxygen species and associated DNA damage. Cancer Prevention Research 2012, 5:536-543.
3. Aljada A., Mousa S.A. Metformin and neoplasia: implications and indications. Pharmacology and Therapeutics 2011, 133:108-115.
4. Amcheslavsky A., Jiang J., Ip Y.T. Tissue damage-induced intestinal stem cell division in Drosophila. Cell Stem Cell 2009, 4:49-61.
5. Apidianakis Y., Rahme L.G. Drosophila melanogaster as a model for human intestinal infection and pathology. Disease Models and Mechanisms 2011, 4:21-30.
6. Baur D.M., Klotsche J., Hamnvik O.P., Sievers C., Pieper L., Wittchen H.U., Stalla G.K., Schmid R.M., Kales S.N., Mantzoros C.S. Type 2 diabetes mellitus and medications for type 2 diabetes mellitus are associated with risk for and mortality from cancer in a German primary care cohort. Metabolism: Clinical and Experimental 2010, 60:1363-1371.
7. Bellacosa A., Kumar C.C., Di Cristofano A., Testa J.R. Activation of AKT kinases in cancer: implications for therapeutic targeting. Advances in Cancer Research 2005, 94:29-86.
8. Biteau B., Hochmuth C.E., Jasper H. JNK activity in somatic stem cells causes loss of tissue homeostasis in the aging Drosophila gut. Cell Stem Cell 2008, 3:442-455.
9. Biteau B., Hochmuth C.E., Jasper H. Maintaining tissue homeostasis: dynamic control of somatic stem cell activity. Cell Stem Cell 2011, 9:402-411.
10. Biteau B., Jasper H. EGF signaling regulates the proliferation of intestinal stem cells in Drosophila. Development 2011, 138:1045-1055.
11. Biteau B., Karpac J., Supoyo S., Degennaro M., Lehmann R., Jasper H. Lifespan extension by preserving proliferative homeostasis in Drosophila. PLoS Genetics 2010, 6:e1001159.
12. Blagosklonny M.V. Aging: ROS or TOR. Cell Cycle 2008, 7:3344-3354.
13. Bond D., Foley E. Autocrine platelet-derived growth factor-vascular endothelial growth factor receptor-related (Pvr) pathway activity controls intestinal stem cell proliferation in the adult Drosophila midgut. Journal of Biological Chemistry 2012, 287:27359-27370.
14. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118:401-415.
15. Broedbaek K., Weimann A., Stovgaard E.S., Poulsen H.E. Urinary 8-oxo-7,8-dihydro-2'-deoxyguanosine as a biomarker in type 2 diabetes. Free Radical Biology and Medicine 2011, 51:1473-1479.
16. Buchon N., Broderick N.A., Kuraishi T., Lemaitre B. Drosophila EGFR pathway coordinates stem cell proliferation and gut remodeling following infection. BMC Biology 2010, 8:152.
17. Choi N.H., Kim J.G., Yang D.J., Kim Y.S., Yoo M.A. Age-related changes in Drosophila midgut are associated with PVF2, a PDGF/VEGF-like growth factor. Aging Cell 2008, 7:318-334.
18. Choi N.H., Lucchetta E., Ohlstein B. Nonautonomous regulation of Drosophila midgut stem cell proliferation by the insulin-signaling pathway. Proceedings of the National Academy of Sciences 2011, 108:18702-18707.
19. Cordero J.B., Stefanatos R.K., Scopelliti A., Vidal M., Sansom O.J. Inducible progenitor-derived Wingless regulates adult midgut regeneration in Drosophila. EMBO Journal 2012, 31:3901-3917.
20. Cui Y., Andersen D.K. Diabetes and pancreatic cancer. Endocrine-Related Cancer 2012, 19:F9-F26.
21. Graham G.G., Punt J., Arora M., Day R.O., Doogue M.P., Duong J.K., Furlong T.J., Greenfield J.R., Greenup L.C., Kirkpatrick C.M., Ray J.E., Timmins P., Williams K.M. Clinical pharmacokinetics of metformin. Clinical Pharmacokinetics 2011, 50:81-98.
22. Habib S.L., Bhandari B.K., Sadek N., Abboud-Werner S.L., Abboud H.E. Novel mechanism of regulation of the DNA repair enzyme OGG1 in tuberin-deficient cells. Carcinogenesis 2010, 31:2022-2030.
23. Habib S.L., Riley D.J., Mahimainathan L., Bhandari B., Choudhury G.G., Abboud H.E. Tuberin regulates the DNA repair enzyme OGG1. Renal Physiology: American Journal of Physiology 2008, 294:F281-F290.
24. Halicka H.D., Zhao H., Li J., Lee Y.S., Hsieh T.C., Wu J.M., Darzynkiewicz Z. Potential anti-aging agents suppress the level of constitutive mTOR- and DNA damage-signaling. Aging (Albany, NY) 2012, 952-965.
25. Halicka H.D., Zhao H., Li J., Traganos F., Zhang S., Lee M., Darzynkiewicz Z. Genome protective effect of metformin as revealed by reduced level of constitutive DNA damage signaling. Aging (Albany, NY) 2011, 3:1028-1038.
26. Hasson P., Egoz N., Winkler C., Volohonsky G., Jia S., Dinur T., Volk T., Courey A.J., Paroush Z. EGFR signaling attenuates Groucho-dependent repression to antagonize Notch transcriptional output. Nature Genetics 2005, 37:101-105.
27. Hinokio Y., Suzuki S., Hirai M., Chiba M., Hirai A., Toyota T. Oxidative DNA damage in diabetes mellitus: its association with diabetic complications. Diabetologia 1999, 42:995-998.
28. Jiang H., Edgar B.A. EGFR signaling regulates the proliferation of Drosophila adult midgut progenitors. Development 2009, 136:483-493.
29. Jiang H., Edgar B.A. Intestinal stem cells in the adult Drosophila midgut. Experimental Cell Research 2011, 317:2780-2788.
30. Jiang H., Grenley M.O., Bravo M.J., Blumhagen R.Z., Edgar B.A. EGFR/Ras/MAPK signaling mediates adult midgut epithelial homeostasis and regeneration in Drosophila. Cell Stem Cell 2011, 8:84-95.
31. Jiang H., Patel P.H., Kohlmaier A., Grenley M.O., McEwen D.G., Edgar B.A. Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 2009, 137:1343-1355.
32. Jones D.L., Rando T.A. Emerging models and paradigms for stem cell ageing. Nature Cell Biology 2011, 13:506-512.
33. Jung J.W., Park S.B., Lee S.J., Seo M.S., Trosko J.E., Kang K.S. Metformin represses self-renewal of the human breast carcinoma stem cells via inhibition of estrogen receptor-mediated OCT4 expression. PLoS ONE 2011, 6:e28068.
34. Karpowicz P., Perez J., Perrimon N. The Hippo tumor suppressor pathway regulates intestinal stem cell regeneration. Development 2010, 137:4135-4145.
35. Landman G.W., Kleefstra N., van Hateren K.J., Groenier K.H., Gans R.O., Bilo H.J. Metformin associated with lower cancer mortality in type 2 diabetes: ZODIAC-16. Diabetes care 2009, 33:322-326.
36. Lin G., Xi R. Intestinal stem cell, muscular niche and Wingless signaling. Fly 2008, 2:310-312.
37. Lin G., Xu N., Xi R. Paracrine Wingless signalling controls self-renewal of Drosophila intestinal stem cells. Nature 2008, 455:1119-1123.
38. Liu W., Singh S.R., Hou S.X. JAK-STAT is restrained by Notch to control cell proliferation of the Drosophila intestinal stem cells. Journal of Cellular Biochemistry 2010, 109:992-999.
39. Massie C., Mills I.G. The developing role of receptors and adaptors. Nature Reviews Cancer 2006, 6:403-409.
40. McGuire S.E., Roman G., Davis R.L. Gene expression systems in Drosophila: a synthesis of time and space. Trends in Biochemical Sciences 2004, 20:384-391.
41. Micchelli C.A., Perrimon N. Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 2006, 439:475-479.
42. O'Brien L.E., Soliman S.S., Li X., Bilder D. Altered modes of stem cell division drive adaptive intestinal growth. Cell 2011, 147:603-614.
43. Ohlstein B., Spradling A. The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 2006, 439:470-474.
44. Ohlstein B., Spradling A. Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential notch signaling. Science 2007, 315:988-992.
45. Owen M.R., Doran E., Halestrap A.P. Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain. Biochemical Journal 2000, 348(Pt 3):607-614.
46. Park J.S., Kim Y.S., Yoo M.A. The role of p38b MAPK in age-related modulation of intestinal stem cell proliferation and differentiation in Drosophila. Aging (Albany, NY) 2009, 1:637-651.
47. Park J.S., Lee S.H., Na H.J., Pyo J.H., Kim Y.S., Yoo M.A. Age- and oxidative stress-induced DNA damage in Drosophila intestinal stem cells as marked by Gamma-H2AX. Experimental Gerontology 2012, 47:401-405.
48. Phelps C.B., Brand A.H. Ectopic gene expression in Drosophila using GAL4 system. Methods 1998, 14:367-379.
49. Rando T.A. Stem cells, ageing and the quest for immortality. Nature 2006, 441:1080-1086.
50. Ren F., Wang B., Yue T., Yun E.Y., Ip Y.T., Jiang J. Hippo signaling regulates Drosophila intestine stem cell proliferation through multiple pathways. Proceedings of the National Academy of Sciences 2010, 107:21064-21069.
51. Simone S., Gorin Y., Velagapudi C., Abboud H.E., Habib S.L. Mechanism of oxidative DNA damage in diabetes: tuberin inactivation and downregulation of DNA repair enzyme 8-oxo-7,8-dihydro-2'-deoxyguanosine-DNA glycosylase. Diabetes 2008, 57:2626-2636.
52. Surucu B., Bozulic L., Hynx D., Parcellier A., Hemmings B.A. In vivo analysis of protein kinase B (PKB)/Akt regulation in DNA-PKcs-null mice reveals a role for PKB/Akt in DNA damage response and tumorigenesis. Journal of Biological Chemistry 2008, 283:30025-30033.
53. Toker A. Achieving specificity in Akt signaling in cancer. Advances in Biological Regulation 2012, 52:78-87.
54. Winter J.N., Jefferson L.S., Kimball S.R. ERK and Akt signaling pathways function through parallel mechanisms to promote mTORC1 signaling. American Journal of Physiology: Cell Physiology 2011, 300:C1172-C1180.
55. Xu N., Wang S.Q., Tan D., Gao Y., Lin G., Xi R. EGFR, Wingless and JAK/STAT signaling cooperatively maintain Drosophila intestinal stem cells. Developmental Biology 2011, 354:31-43.
56. Yang Z., Ming X.F. mTOR signalling: the molecular interface connecting metabolic stress, aging and cardiovascular diseases. Obesity Reviews 2012, 13(Suppl. 2):58-68.
57. Zhang X., Rielland M., Yalcin S., Ghaffari S. Regulation and function of FoxO transcription factors in normal and cancer stem cells: what have we learned?. Current Drug Targets 2011, 12:1267-1283.