Spermidine prolongs lifespan and prevents liver fibrosis and hepatocellular carcinoma by activating MAP1S-mediated autophagy

Cancer Research

Volumn 77, Issue 11, 2017, Pages 2938-2951

  Yue, Fei ^a   Li, Wenjiao ^a   Zou, Jing ^a   Jiang, Xianhan ^a,b   Xu, Guibin ^a,b   Huang, Hai ^a   Liu, Leyuan ^a,b,c  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^b GUANGZHOU MEDICAL UNIVERSITY   (China)

^c TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; HISTONE DEACETYLASE 4; HISTONE H2AX; HYDROXYPROLINE; LC3 PROTEIN; MARKER; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 1S; SPERMIDINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTHROPOMETRIC PARAMETERS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BODY WEIGHT; CANCER PREVENTION; CARBON TETRACHLORIDE-INDUCED LIVER FIBROSIS; CONTROLLED STUDY; HUMAN; HUMAN CELL; LIFE EXTENSION; LIVER BODY WEIGHT RATIO; LIVER CELL CARCINOMA; LIVER WEIGHT; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SURVIVAL TIME; ANIMAL; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; LIVER CIRRHOSIS; LIVER TUMOR; METABOLISM; PATHOLOGY;

ANIMALS; AUTOPHAGY; CARCINOMA, HEPATOCELLULAR; HUMANS; LIVER CIRRHOSIS; LIVER NEOPLASMS; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; SPERMIDINE;

EID: 85020832729     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-16-3462     Document Type: Article

References (50)

1. El-Serag HB. Hepatocellular carcinoma. New Engl J Med 2011;365:1118-27.
2. Zhang DY, Friedman SL. Fibrosis-dependent mechanisms of hepatocarcinogenesis. Hepatology 2012;56:769-75.
3. Singh S, Singh PP, Roberts LR, Sanchez W. Chemopreventive strategies in hepatocellular carcinoma. Nat Rev Gastroenterol Hepatol 2014;11:45-54.
4. Mizushima N, Noda T, Yoshimori T, Tanaka Y, Ishii T, George MD, et al. A protein conjugation system essential for autophagy. Nature 1998;395:395-8.
5. Fink SL, Cookson BT. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 2005;73:1907-16.
6. Suzuki T, Franchi L, Toma C, Ashida H, Ogawa M, Yoshikawa Y, et al. Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages. PLoS Pathog 2007;3:e111.
7. Doitsh G, Galloway NL, Geng X, Yang Z, Monroe KM, Zepeda O, et al. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 2014;505:509-14.
8. Wree A, Eguchi A, McGeough MD, Pena CA, Johnson CD, Canbay A, et al. NLRP3 inflammasome activation results in hepatocyte pyroptosis, liver inflammation, and fibrosis in mice. Hepatology 2014;59:898-910.
9. Liu L, Vo A, Liu G, McKeehan WL. Distinct structural domains within C19ORF5 support association with stabilized microtubules and mitochondrial aggregation and genome destruction. Cancer Res 2005;65:4191-201.
10. Liu L, Vo A, McKeehan WL. Specificity of the methylation-suppressed A isoform of candidate tumor suppressor RASSF1 for microtubule hyperstabilization is determined by cell death inducer C19ORF5. Cancer Res 2005;65:1830-8.
11. Liu L, Xie R, Yang C, McKeehan WL. Dual function microtubule- and mitochondria-associated proteins mediate mitotic cell death. Cell Oncol 2009;31:393-405.
12. Kayaba H, Hirokawa M, Watanabe A, Saitoh N, Changhao C, Yamada Y, et al. Serum markers of graft-versus-host disease after bone marrow transplantation. J Allergy Clin Immunol 2000;106:S40-4.
13. Schoenfeld TA, McKerracher L, Obar R, Vallee RB. MAP 1A and MAP 1B are structurally related microtubule associated proteins with distinct developmental patterns in the CNS. J Neurosci 1989;9:1712-30.
14. Xie R, Wang F, McKeehan WL, Liu L. Autophagy enhanced by microtubule- and mitochondrion-associated MAP1S suppresses genome instability and hepatocarcinogenesis. Cancer Res 2011;71:7537-46.
15. Liu L, McKeehan WL, Wang F, Xie R. MAP1S enhances autophagy to suppress tumorigenesis. Autophagy 2012;8:278-80.
16. Li W, Zou J, Yue F, Song K, Chen Q, McKeehan WL, et al. Defects in MAP1S-mediated autophagy cause reduction in mouse lifespans especially when fibronectin is overexpressed. Aging Cell 2016;15:370-9.
17. Jiang X, Zhong W, Huang H, He H, Jiang F, Chen Y, et al. Autophagy defects suggested by low levels of autophagy activator MAP1S and high levels of autophagy inhibitor LRPPRC predict poor prognosis of prostate cancer patients. Mol Carcinog 2015;54:1194-204.
18. Xu G, Jiang Y, Xiao Y, Liu XD, Yue F, Li W, et al. Fast clearance of lipid droplets through MAP1S-activated autophagy suppresses clear cell renal cell carcinomas and promotes patient survival. Oncotarget 2016;7:6255-65.
19. Yue F, Li W, Zou J, Chen Q, Xu G, Huang H, et al. Blocking the association of HDAC4 with MAP1S accelerates autophagy clearance of mutant Huntingtin. Aging 2015;7:839-53.
20. Eisenberg T, Knauer H, Schauer A, Buttner S, Ruckenstuhl C, Carmona-Gutierrez D, et al. Induction of autophagy by spermidine promotes longevity. Nat Cell Biol 2009;11:1305-14.
21. Morselli E, Galluzzi L, Kepp O, Criollo A, Maiuri MC, Tavernarakis N, et al. Autophagy mediates pharmacological lifespan extension by spermidine and resveratrol. Aging 2009;1:961-70.
22. Morselli E, Marino G, Bennetzen MV, Eisenberg T, Megalou E, Schroeder S, et al. Spermidine and resveratrol induce autophagy by distinct pathways converging on the acetylproteome. J Cell Biol 2011;192:615-29.
23. Eisenberg T, Abdellatif M, Schroeder S, Primessnig U, Stekovic S, Pendl T, et al. Cardioprotection and lifespan extension by the natural polyamine spermidine. Nat Med 2016;22:1428-38.
24. Pietrocola F, Pol J, Vacchelli E, Rao S, Enot DP, Baracco EE, et al. Caloric restriction mimetics enhance anticancer immunosurveillance. Cancer Cell 2016;30:147-60.
25. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 2004;15:1101-11.
26. Zou J, Yue F, Li W, Song K, Jiang X, Yi J, et al. Autophagy inhibitor LRPPRC suppresses mitophagy through interaction with mitophagy initiator Parkin. PLoS One 2014;9:e94903.
27. Xie R, Nguyen S, McKeehan K, Wang F, McKeehan WL, Liu L. Microtubule-associated protein 1S (MAP1S) bridges autophagic components with microtubules and mitochondria to affect autophagosomal biogenesis and degradation. J Biol Chem 2011;286:10367-77.
28. Glick D, Zhang W, Beaton M, Marsboom G, Gruber M, Simon MC, et al. BNip3 regulates mitochondrial function and lipid metabolism in the liver. Mol Cell Biol 2012;32:2570-84.
29. Tomita K, Teratani T, Suzuki T, Shimizu M, Sato H, Narimatsu K, et al. Acyl-CoA:cholesterol acyltransferase 1 mediates liver fibrosis by regulating free cholesterol accumulation in hepatic stellate cells. J Hepatol 2014;61:98-106.
30. Jiang X, Li X, Huang H, Jiang F, Lin Z, He H, et al. Elevated levels of mitochondrion-associated autophagy inhibitor LRPPRC are associated with poor prognosis in patients with prostate cancer. Cancer 2014;120:1228-36.
31. Grozinger CM, Schreiber SL. Regulation of histone deacetylase 4 and 5 and transcriptional activity by 14-3-3-dependent cellular localization. Proc Nat Acad Sci U S A 2000;97:7835-40.
32. Bachrach U. The early history of polyamine research. Plant Physiol Biochem 2010;48:490-5.
33. Meyskens FL Jr, McLaren CE, Pelot D, Fujikawa-Brooks S, Carpenter PM, Hawk E, et al. Difluoromethylornithine plus sulindac for the prevention of sporadic colorectal adenomas: a randomized placebo-controlled, double-blind trial. Cancer Prev Res 2008;1:32-8.
34. Russell DH. Increased polyamine concentrations in the urine of human cancer patients. Nat New Biol 1971;233:144-5.
35. Miller-Fleming L, Olin-Sandoval V, Campbell K, Ralser M. Remaining mysteries of molecular biology: the role of polyamines in the cell. J Mol Biol 2015;427:3389-406.
36. Pietrocola F, Lachkar S, Enot DP, Niso-Santano M, Bravo-San Pedro JM, Sica V, et al. Spermidine induces autophagy by inhibiting the acetyltransferase EP300. Cell Death Differ 2015;22:509-16.
37. Zhao X, Ito A, Kane CD, Liao TS, Bolger TA, Lemrow SM, et al. The modular nature of histone deacetylase HDAC4 confers phosphorylation-dependent intracellular trafficking. J Biol Chem 2001;276:35042-8.
38. Mihaylova MM, Vasquez DS, Ravnskjaer K, Denechaud PD, Yu RT, Alvarez JG, et al. Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis. Cell 2011;145:607-21.
39. Mitchell SJ, Scheibye-Knudsen M, Longo DL, de Cabo R. Animal models of aging research: implications for human aging and age-related diseases. Annu Rev Anim Biosci 2015;3:283-303.
40. McCay CM, Maynard LA, Sperling G, Barnes LL. The journal of nutrition. volume 18 July-December,1939. Pages 1-13. Retarded growth, life span, ultimate body size and age changes in the albino rat after feeding diets restricted in calories. Nutr Rev 1975;33:241-3.
41. Orentreich N, Matias JR, DeFelice A, Zimmerman JA. Low methionine ingestion by rats extends life span. J Nutr 1993;123:269-74.
42. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, et al. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 2009;460:392-5.
43. Bauer MA, Carmona-Gutierrez D, Ruckenstuhl C, Reisenbichler A, Megalou EV, Eisenberg T, et al. Spermidine promotes mating and fertilization efficiency in model organisms. Cell Cycle 2013;12:346-52.
44. Martin-Montalvo A, Mercken EM, Mitchell SJ, Palacios HH, Mote PL, Scheibye-Knudsen M, et al. Metformin improves healthspan and lifespan in mice. Nat Commun 2013;4:2192.
45. Mitchell SJ, Martin-Montalvo A, Mercken EM, Palacios HH, Ward TM, Abulwerdi G, et al. The SIRT1 activator SRT1720 extends lifespan and improves health of mice fed a standard diet. Cell Rep 2014;6:836-43.
46. Chrisam M, Pirozzi M, Castagnaro S, Blaauw B, Polishchuck R, Cecconi F, et al. Reactivation of autophagy by spermidine ameliorates the myopathic defects of collagen VI-null mice. Autophagy 2015;11:2142-52.
47. Zhang Y, Bokov A, Gelfond J, Soto V, Ikeno Y, Hubbard G, et al. Rapamycin extends life and health in C57BL/6 mice. J Gerontol 2014;69:119-30.
48. Gurpinar E, Grizzle WE, Shacka JJ, Mader BJ, Li N, Piazza NA, et al. A novel sulindac derivative inhibits lung adenocarcinoma cell growth through suppression of Akt/mTOR signaling and induction of autophagy. Mol Cancer Ther 2013;12:663-74.
49. Yin T, Wang G, Ye T, Wang Y. Sulindac, a non-steroidal anti-inflammatory drug, mediates breast cancer inhibition as an immune modulator. Sci Rep 2016;6:19534.
50. Chiou SK, Hoa N, Hodges A. Sulindac sulfide induces autophagic death in gastric epithelial cells via survivin down-regulation: a mechanism of NSAIDs-induced gastric injury. Biochem Pharmacol 2011;81:1317-23.