Artemisinin mimics calorie restriction to trigger mitochondrial biogenesis and compromise telomere shortening in mice

PeerJ

Volumn 2015, Issue 3, 2015, Pages

  Wang, Da Ting ^a   He, Jiang ^a   Wu, Ming ^b   Li, Si Ming ^a   Gao, Qian ^a   Zeng, Qing Ping ^a  

^a GUANGZHOU UNIVERSITY OF CHINESE MEDICINE   (China)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

Artemisinin; BRCA1; Calorie restriction; Hydrogen peroxide; Nitric oxide; Telomere

Indexed keywords

ADENOSINE TRIPHOSPHATE; ARGININE; ARTEMISININ; ARTESUNATE; CATALASE; CYTOCHROME C OXIDASE; CYTOCHROME C OXIDASE 4; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUTATHIONE; NITRIC OXIDE; NITROPRUSSIDE SODIUM; PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOGENESIS; CALORIC RESTRICTION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DNA REPAIR; DOWN REGULATION; ELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; INTRACELLULAR SIGNALING; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE STRESS; REAL TIME POLYMERASE CHAIN REACTION; RESPIRATORY CHAIN; RNA EXTRACTION; SKELETAL MUSCLE; SOUTHERN BLOTTING; TELOMERE SHORTENING; TUMOR SUPPRESSOR GENE; UBIQUITINATION; UPREGULATION; WESTERN BLOTTING;

MUS;

EID: 84926464964     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.822     Document Type: Article

References (47)

1. Anderson RM, Weindruch R. 2010. Metabolic reprogramming, caloric restriction and aging. Trends in Endocrinology and Metabolism 21:134-141 DOI 10.1016/j.tem.2009.11.005.
2. Ballal RD, Saha T, Fan S, Haddad BR, Rosen EM. 2009. BRCA1 localization to the telomere and its loss from the telomere in response to DNA damage. Journal of Biological Chemistry 284:36083-36098 DOI 10.1074/jbc. M109.025825.
3. Bao F, Wu P, Xiao N, Qiu F, Zeng QP. 2012. Nitric oxide-driven hypoxia initiates synovial angiogenesis, hyperplasia and inflammatory lesions in mice. PLoS ONE 7:e34494 DOI 10.1371/journal.pone.0034494.
4. Barros MH, Bandy B, Tahara EB, Kowaltowski AJ. 2004. Higher respiratory activity decreases mitochondrial reactive oxygen release and increases lifespan in Saccharomyces cerevisiae. Journal of Biological Chemistry 279:49883-49888 DOI 10.1074/jbc. M408918200.
5. Blagosklonny MV. 2010. Linking calorie restriction to longevity through sirtuins and autophagy: any role for TOR. Cell Death and Disease 1:e12 DOI 10.1038/cddis.2009.17.
6. Brand MD. 2000. Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Experimental Gerontology 35:811-820 DOI 10.1016/S0531-5565(00)00135-2.
7. Cai H, Davis ME, Drummond GR, Harrison DG. 2001. Induction of endothelial NO synthase by hydrogen peroxide via a Ca(2+)/calmodulin-dependent protein kinase II/janus kinase 2-dependent pathway. Arteriosclerosis, Thrombosis, and Vascular Biology 21:1571-1576 DOI 10.1161/hq1001.097028.
8. Cerqueira FM, Laurindo FRM, Kowaltowski AJ. 2011. Mild mitochondrial uncoupling and calorie restriction increase fasting eNOS, AKT and mitochondrial biogenesis. PLoS ONE 6:e18433 DOI 10.1371/journal.pone.0018433.
9. Chen ZP, Mitchelhill KI, Michell BJ, Stapleton D, Rodriguez-Crespo I, Witters LA, Power D, Oritz deMontellano PR, Kemp BE. 1999. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Letters 443:285-289 DOI 10.1016/S0014-5793(98)01705-0.
10. Chin RM, Fu X, Pai MY, Vergnes L, Hwang H, Deng G, Diep S, Lomenick B, Meli VS, Monsalve GC, Hu E, Whelan SA, Wang JX, Jung G, Solis GM, Fazlollahi F, Kaweeteerawat C, Quach A, Nili M, Krall AS, Godwin HA, Chang HR, Faull KF, Guo F, Jiang M, Trauger SA, Saghatelian A, Braas D, Christofk HR, Clarke CF, Teitell MA, Petrascheck M, Reue K, Jung ME, Frand AR, Huang J. 2014. The metabolite a-ketoglutarate extends lifespan by inhibiting ATP synthase and TOR. Nature 510:397-401 DOI 10.1038/nature13264.
11. Clark SL, Rodriguez AM, Snyder RR, Hankins GD, Boehning D. 2012. Structure-function of the tumor suppressor BRCA1. Computational and Structural Biotechnology Journal 1:e201204005 DOI 10.5936/csbj.201204005.
12. De Haes W, Frooninck XL, Van Assche R, Smolders A, Depuydet G, Billen J, Braeckman BP, Schoofs L, Temmerman L. 2014. Metformin promotes lifespan through mitohormesis via the peroxiredoxin PRDX-2. Proceedings of the National Academy of Sciences of the United States of America 111:E2501-E2509 DOI 10.1073/pnas.1321776111.
13. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. 1999. Regulation of endothelium-derived nitric oxide production by the protein kinase AKT. Nature 399:597-601 DOI 10.1038/21218.
14. Hashizume R, Fukuda M, Maeda I, Nishikawa H, Oyake D, Yabuki Y, Ogataand H, Ohta T. 2001. The RING heterodimer BRCA1-BARD1 is a ubiquitin ligase inactivated by a breast cancer-derived mutation. Journal of Biological Chemistry 276:14537-14540 DOI 10.1074/jbc. C000881200.
15. Hewitt G, Jurk D, Marques FDM, Correia-Melo C, Hardy T, Gackowska A, Anderson R, Taschuk M, Mann J, Passos JF. 2012. Telomeres are favoured targets of a persistent DNA damage response in ageing and stress-induced senescence. Nature Communications 3:Article 708 DOI 10.1038/ncomms1708.
16. Humpherey DM, Toivonen JM, Giannakou M, Partridge L, Brand MD. 2009. Expression of human uncoupling protein-3 in Drosophila insulin-producing cells increases insulin-like peptide (DILP) levels and shortens lifespan. Experimental Gerontology 44:316-327 DOI 10.1016/j.exger.2009.02.001.
17. Kamble P, Selvarajan K, Narasimhulu CA, Nandave M, Parthasarathy S. 2013. Aspirin may promote mitochondrial biogenesis via the production of hydrogen peroxide and the induction of Sirtuin1/PGC-1a genes. European Journal of Pharmacology 699:55-61 DOI 10.1016/j.ejphar.2012.11.051.
18. Korde AS, Pettigrew LC, Craddock SD, Maragos WF. 2005. The mitochondrial uncoupler 2,4-dinitrophenol attenuates tissue damage and improves mitochondrial homeostasis following transient focal cerebral ischemia. Journal of Neurochemistry 94:1676-1684 DOI 10.1111/j.1471-4159.2005.03328.x.
19. Koubova J, Guarente L. 2005. How does calorie restriction work? Genes and Development 17:313-321 DOI 10.1101/gad.1052903.
20. Lanza IR, Nair KS. 2010. Mitochondrial function as a determinant of life span. Pflügers Archiv - European Journal of Physiology 459:277-289 DOI 10.1007/s00424-009-0724-5.
21. Lee WJ, Kim M, Park H-S, Kim HS, Jeon MJ, Oh KS, Koh EH, Won JC, Kim M-S, Oh GT, Yoon M, Lee K-U, Park J-Y. 2006. AMPK activation increases fatty acid oxidation in skeletal muscle by activating PPAR alpha and PGC-1. Biochemical and Biophysical Research Communications 340:291-295 DOI 10.1016/j.bbrc.2005.12.011.
22. Lemere BD, Behrendt M, DeCorby A, Gaskova D. 2009. C. elegans longevity pathways converge to decrease mitochondrial membrane potential. Mechanisms of Ageing and Development 130:461-465 DOI 10.1016/j.mad.2009.05.001.
23. Levine YC, Li GK, Michel T. 2007. Agonist-modulated regulation of AMP-activated protein kinase in endothelial cells: evidence for an AMPK→ RAC1→ AKT→ eNOS pathway. Journal of Biological Chemistry 282:20351-20364 DOI 10.1074/jbc. M702182200.
24. Li F, Zhang L, Craddock J, Bruce-Keller AJ, Dasuri K, Nguyen A, Keller JN. 2008. Aging and dietary restriction effects on ubiquitination, sumoylation, and the proteasome in the heart. Mechanisms of Ageing and Development 129:515-521 DOI 10.1016/j.mad.2008.04.007.
25. Longo VD, Fontana L. 2010. Calorie restriction and cancer prevention: metabolic and molecular mechanisms. Trends in Pharmacological Sciences 31:89-98 DOI 10.1016/j.tips.2009.11.004.
26. López-Lluch G, Hunt N, Jones B, Zhu M, Jamieson H, Hilmer S, Cascajo MV, Allard J, Ingram DK, Navas P, de Cabo R. 2006. Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proceedings of the National Academy of Sciences of the United States of America 103:1768-1773 DOI 10.1073/pnas.0510452103.
27. Martin-Montalvo A, Mercken EM, Mitchell SJ, Palacios HH, Mote PL, Scheibye-Knudsen M, Gomes AP, Ward TM, Minor RK, Blouin MJ, Schwab M, Pollak M, Zhang Y, Yu Y, Becker KG, Bohr VA, Ingram DK, Sinclair DA, Wolf NS, Spindler SR, Bernier M, de Cabo R. 2013. Metformin improves healthspan and lifespan in mice. Nature Communications 4:Article 2192 DOI 10.1038/ncomms3192.
28. Mason MG, Nicholls P, Wilson MT, Cooper CE. 2006. Nitric oxide inhibition of respiration involves both competitive (heme) and noncompetitive (copper) binding to cytochrome c oxidase. Proceedings of the National Academy of Sciences of the United States of America 103:708-713 DOI 10.1073/pnas.0506562103.
29. 2 and superoxide dismutase activity. Proceedings of the National Academy of Sciences of the United States of America 107:15123-15128 DOI 10.1073/pnas.1004432107.
30. Nisoli E, Clementi E, Paolucci C, Cozzi V, Tonello C, Sciorati C, Bracale R, Valerio A, Francolini M, Moncada S, Moncada S, Carruba MO. 2003. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 299:896-899 DOI 10.1126/science.1079368.
31. Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L, Falcone S, Valerio A, Cantoni O, Clementi E, Carruba MO. 2005. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310:314-317 DOI 10.1126/science.1117728.
32. Ou ZJ, Wei W, Huang DD, Luo W, Luo D, Wang ZP, Zhang X, Ou JS. 2010. L-Arginine restores endothelial nitric oxide synthase-coupled activity and attenuates monocrotaline-induced pulmonary artery hypertension in rats. American Journal of Physiology, Endocrinology and Metabolism 298:E1131-E1139 DOI 10.1152/ajpendo.00107.2010.
33. Qiu X, Brown K, Hirschey MD, Verdin E, Chen D. 2010. Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metabolism 12:662-667 DOI 10.1016/j.cmet.2010.11.015.
34. Ristow M. 2014. Unraveling the truth about antioxidants: mitohormesis explains ROS-induced health benefits. Nature Medicine 20:709-711 DOI 10.1038/nm.3624.
35. Ristow M, Kim Z. 2010. How increased oxidative stress promotes longevity and metabolic health: the concept of mitochondrial hormesis (mitohormesis). Experimental Gerontology 45:410-418 DOI 10.1016/j.exger.2010.03.014.
36. Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, Puigserver P. 2005. Nutrient control of glucose homeostasis through a complex of PGC-1 alpha and SIRT1. Nature 434:113-118 DOI 10.1038/nature03354.
37. Spindler SR. 2010. Calorie restriction: from soup to nuts. Ageing Research Reviews 9:324-353 DOI 10.1016/j.arr.2009.10.003.
38. Vera E, Bernardes de Jesus B, Foronda M, Flores JM, Blasco MA. 2013. Telomerase reverse transcriptase synergizes with calorie restriction to increase health span and extend mouse longevity. PLoS ONE 8:e53760 DOI 10.1371/journal.pone.0053760.
39. Wang DT, Wu M, Li SM, Gao Q, Zeng QP. 2015. Artemisinin mimics calorie restriction to extend yeast lifespan via a dual-phase mode: a conclusion drawn from global transcriptome profiling. Science China Life Sciences 58:1-15 DOI 10.1007/s11427-014-4795-y.
40. Wang DT, Zeng QP. 2014. Modulation of yeast transporter gene expression and lipid metabolism by hormesis mimicking calorie restriction. Microbiol China 41:2012-2021 DOI 10.13344/j.microbiol.china.130928.
41. Wu P, Bao F, Zheng Q, Xiao N, Wang DT, Zeng QP. 2012. Artemisinin and rapamycin compromise nitric oxide-driven and hypoxia-triggered acute articular synovitis in mice. Scientia Sinica Vitae 42:724-738 DOI 10.1360/052012-148.
42. Xiong J, Fan S, Meng Q, Schramm L, Wang C, Bouzahza B, Zhou J, Zafonte B, Goldberg ID, Haddad BR, Pestell RG, Rosen EM. 2003. BRCA inhibition of telomerase activity in cultured cells. Molecular and Cellular Biology 23:8668-8690 DOI 10.1128/MCB.23.23.8668-8690.2003.
43. Yang W, Hekimi S. 2010. A mitochondrial superoxide signal triggers increased longevity in Caenorhabditis elegans. PLoS Biology 8:e1000556 DOI 10.1371/journal.pbio.1000556.
44. Zeng QP, Xiao N, Wu P, Yang XQ, Zeng LX, Guo XX, Zhang PZ, Qiu F. 2011. Artesunate potentiates antibiotics by inactivating bacterial heme-harbouring nitric oxide synthase and catalase. BMC Research Notes 4:223 DOI 10.1186/1756-0500-4-223.
45. Zeng QP, Zhang PZ. 2011. Artesunate mitigates proliferation of tumor cells by alkylating hemeharboring nitric oxide synthase. Nitric Oxide 24:110-112 DOI 10.1016/j.niox.2010.12.005.
46. Zhang S, Gerhard GS. 2009. Heme mediates cytotoxicity from artemisinin and serves as a general anti-proliferation target. PLoS ONE 4:e7472 DOI 10.1371/journal.pone.0007472.
47. Zhao KC, Xuan WY, Zhao Y, Song ZY. 1989. The pharmacokinetics of a transdermal preparation of artesunate in mice and rabbits. Yao Xue Xue Bao 24:813-816.