Bridging epigenetics and metabolism: Role of non-essential amino acids

Epigenetics

Volumn 8, Issue 3, 2013, Pages 231-236

  Phang, James M ^a   Liu, Wei ^a   Hancock, Chad ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Epigenetics; Metabolism and cancer; Non essential amino acids; Proline metabolism; Reactive oxygen species; Redox regulation

Indexed keywords

2 OXOGLUTARIC ACID; ACETYL COENZYME A; ADENOSINE TRIPHOSPHATE; ALANINE; GLUTAMINASE; GLUTAMINE; MICRORNA; NICOTINAMIDE ADENINE DINUCLEOTIDE; NONESSENTIAL AMINO ACID; PROLINE; PYRROLINE 5 CARBOXYLATE REDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; S ADENOSYLMETHIONINE;

AMINO ACID SYNTHESIS; ARTICLE; BIOSYNTHESIS; CITRIC ACID CYCLE; CRYPTOSPORIDIUM; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION; HISTONE ACETYLATION; HUMAN; METABOLISM; METABOLOMICS; NONHUMAN; ONCOGENE C MYC; PROTEIN DEGRADATION; REGULATORY MECHANISM; TUMOR MICROENVIRONMENT; UPREGULATION;

EID: 84875709775     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.24042     Document Type: Article

References (71)

1. Knudson AG Jr. Mutation and cancer: statistical study of retinoblastoma. Proc Natl Acad Sci U S A 1971; 68:820-3. PMID:5279523; http://dx.doi.org/10.1073/pnas.68.4.820.
2. Vogelstein B, Kinzler KW. The multistep nature of cancer. Trends Genet 1993; 9:138-41. PMID:8516849; http://dx.doi.org/10.1016/0168-9525(93)90209-Z.
3. Vogelstein B, Kinzler KW. Cancer genes and the pathways they control. Nat Med 2004; 10:789-99. PMID:15286780; http://dx.doi.org/10.1038/nm1087.
4. Esteller M. Epigenetics in cancer. N Engl J Med 2008; 358:1148-59. PMID:18337604; http://dx.doi.org/10.1056/NEJMra072067.
5. Baylin SB, Jones PA. A decade of exploring the cancer epigenome - biological and translational implications. Nat Rev Cancer 2011; 11:726-34. PMID:21941284; http://dx.doi.org/10.1038/nrc3130.
6. Dawson MA, Kouzarides T. Cancer epigenetics: from mechanism to therapy. Cell 2012; 150:12-27. PMID:22770212; http://dx.doi.org/10.1016/j.cell.2012.06.013.
7. Robertson KD. DNA methylation and human disease. Nat Rev Genet 2005; 6:597-610. PMID:16136652; http://dx.doi.org/10.1038/nrg1655.
8. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 2009; 459:108-12. PMID:19295514; http://dx.doi.org/10.1038/nature07829.
9. Yun J, Johnson JL, Hanigan CL, Locasale JW. Interactions between epigenetics and metabolism in cancers. Front Oncol 2012; 2:163. PMID:23162793; http://dx.doi.org/10.3389/fonc.2012.00163.
10. Lu C, Thompson CB. Metabolic regulation of epigenetics. Cell Metab 2012; 16:9-17. PMID:22768835; http://dx.doi.org/10.1016/j.cmet.2012.06.001.
11. Cai L, Sutter BM, Li B, Tu BP. Acetyl-CoA induces cell growth and proliferation by promoting the acetylation of histones at growth genes. Mol Cell 2011; 42:426-37. PMID:21596309; http://dx.doi.org/10.1016/j.molcel.2011.05.004.
12. Lin SJ, Defossez PA, Guarente L. Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae. Science 2000; 289:2126-8. PMID:11000115; http://dx.doi.org/10.1126/science.289.5487.2126.
13. DeBerardinis RJ, Lum JJ, Hatzivassiliou G, Thompson CB. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab 2008; 7:11-20. PMID:18177721; http://dx.doi.org/10.1016/j.cmet.2007.10.002.
14. Kroemer G, Pouyssegur J.Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell 2008; 13:472-82. PMID:18538731; http://dx.doi.org/10.1016/j.ccr.2008.05.005.
15. Warburg O. On the origin of cancer cells. Science 1956; 123:309-14. PMID:13298683; http://dx.doi.org/10.1126/science.123.3191.309.
16. Cardaci S, Ciriolo MR. TCA Cycle Defects and Cancer: When Metabolism Tunes Redox State. Int J Cell Biol 2012; 2012:161837. PMID:22888353; http://dx.doi.org/10.1155/2012/161837.
17. Vousden KH, Ryan KM. p53 and metabolism. Nat Rev Cancer 2009; 9:691-700. PMID:19759539; http://dx.doi.org/10.1038/nrc2715.
18. Dang CV. MYC, microRNAs and glutamine addiction in cancers. Cell Cycle 2009; 8:3243-5. PMID:19806017; http://dx.doi.org/10.4161/cc.8.20.9522.
19. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009; 324:1029-33. PMID:19460998; http://dx.doi.org/10.1126/science.1160809.
20. Locasale JW, Cantley LC. Metabolic flux and the regulation of mammalian cell growth. Cell Metab 2011; 14:443-51. PMID:21982705; http://dx.doi.org/10.1016/j.cmet.2011.07.014.
21. Meier U, Gressner AM. Endocrine regulation of energy metabolism: review of pathobiochemical and clinical chemical aspects of leptin, ghrelin, adiponectin, and resistin. Clin Chem 2004; 50:1511-25. PMID:15265818; http://dx.doi.org/10.1373/clinchem.2004.032482.
22. Gillies RJ, Robey I, Gatenby RA. Causes and consequences of increased glucose metabolism of cancers. J Nucl Med 2008; 49(Suppl 2):24S-42S. PMID:18523064; http://dx.doi.org/10.2967/jnumed.107.047258.
23. Phang JM, Liu W, Hancock C, Christian KJ.The proline regulatory axis and cancer. Front Oncol 2012; 2:60. PMID:22737668; http://dx.doi.org/10.3389/fonc.2012.00060.
24. Payne SH, Loomis WF. Retention and loss of amino acid biosynthetic pathways based on analysis of whole-genome sequences. Eukaryot Cell 2006; 5:272-6. PMID:16467468; http://dx.doi.org/10.1128/EC.5.2.272-276.2006.
25. Possemato R, Marks KM, Shaul YD, Pacold ME, Kim D, Birsoy K, et al. Functional genomics reveal that the serine synthesis pathway is essential in breast cancer. Nature 2011; 476:346-50. PMID:21760589; http://dx.doi.org/10.1038/nature10350.
26. Le A, Lane AN, Hamaker M, Bose S, Gouw A, Barbi J, et al. Glucose-independent glutamine metabolism via TCA cycling for proliferation and survival in B cells. Cell Metab 2012; 15:110-21. PMID:22225880; http://dx.doi.org/10.1016/j.cmet.2011.12.009.
27. Darmaun D, Matthews DE, Bier DM. Physiological hypercortisolemia increases proteolysis, glutamine, and alanine production. Am J Physiol 1988; 255:E366-73. PMID:3048115.
28. Chiang PK, Gordon RK, Tal J, Zeng GC, Doctor BP, Pardhasaradhi K, et al. S-Adenosylmethionine and methylation. FASEB J 1996; 10:471-80. PMID:8647346.
29. Barron JT, Gu L, Parrillo JE. Malate-aspartate shuttle, cytoplasmic NADH redox potential, and energetics in vascular smooth muscle. J Mol Cell Cardiol 1998; 30:1571-9. PMID:9737943; http://dx.doi.org/10.1006/jmcc.1998.0722.
30. Takamura Y, Nomura G. Changes in the intracellular concentration of acetyl-CoA and malonyl-CoA in relation to the carbon and energy metabolism of Escherichia coli K12. J Gen Microbiol 1988; 134:2249-53. PMID:3075658.
31. Vander Heiden MG, Lunt SY, Dayton TL, Fiske BP, Israelsen WJ, Mattaini KR, et al. Metabolic Pathway Alterations that Support Cell Proliferation. Cold Spring Harb Symp Quant Biol 2012.
32. Phang JM, Donald SP, Pandhare J, Liu Y. The metabolism of proline, a stress substrate, modulates carcinogenic pathways. Amino Acids 2008; 35:681-90. PMID:18401543; http://dx.doi.org/10.1007/s00726-008-0063-4.
33. Phang JM, Liu W. Proline metabolism and cancer. Front Biosci 2012; 17:1835-45. PMID:22201839; http://dx.doi.org/10.2741/4022.
34. Adams E, Frank L. Metabolism of proline and the hydroxyprolines. Annu Rev Biochem 1980; 49:1005-61. PMID:6250440; http://dx.doi.org/10.1146/annurev.bi.49.070180.005041.
35. Polyak K, Xia Y, Zweier JL, Kinzler KW, Vogelstein B. A model for p53-induced apoptosis. Nature 1997; 389:300-5. PMID:9305847; http://dx.doi.org/10.1038/38525.
36. Donald SP, Sun XY, Hu CA, Yu J, Mei JM, Valle D, et al. Proline oxidase, encoded by p53-induced gene-6, catalyzes the generation of proline-dependent reactive oxygen species. Cancer Res 2001; 61:1810-5. PMID:11280728.
37. Maxwell SA, Rivera A. Proline oxidase induces apoptosis in tumor cells, and its expression is frequently absent or reduced in renal carcinomas. J Biol Chem 2003; 278:9784-9. PMID:12514185; http://dx.doi.org/10.1074/jbc.M210012200.
38. Pandhare J, Cooper SK, Phang JM. Proline oxidase, a proapoptotic gene, is induced by troglitazone: evidence for both peroxisome proliferator-activated receptor gamma-dependent and -independent mechanisms. J Biol Chem 2006; 281:2044-52. PMID:16303758; http://dx.doi.org/10.1074/jbc. M507867200.
39. Liu Y, Borchert GL, Surazynski A, Hu CA, Phang JM. Proline oxidase activates both intrinsic and extrinsic pathways for apoptosis: the role of ROS/superoxides, NFAT and MEK/ERK signaling. Oncogene 2006; 25:5640-7. PMID:16619034; http://dx.doi.org/10.1038/sj.onc.1209564.
40. Liu Y, Borchert GL, Donald SP, Surazynski A, Hu CA, Weydert CJ, et al. MnSOD inhibits proline oxidase-induced apoptosis in colorectal cancer cells. Carcinogenesis 2005; 26:1335-42. PMID:15817612; http://dx.doi.org/10.1093/carcin/bgi083.
41. Liu Y, Borchert GL, Donald SP, Diwan BA, Anver M, Phang JM. Proline oxidase functions as a mitochondrial tumor suppressor in human cancers. Cancer Res 2009; 69:6414-22. PMID:19654292; http://dx.doi.org/10.1158/0008-5472.CAN-09-1223.
42. Hu CA, Donald SP, Yu J, Lin WW, Liu Z, Steel G, et al. Overexpression of proline oxidase induces proline-dependent and mitochondria-mediated apoptosis. Mol Cell Biochem 2007; 295:85-92. PMID:16874462; http://dx.doi.org/10.1007/s11010-006-9276-6.
43. Liu W, Glunde K, Bhujwalla ZM, Raman V, Sharma A, Phang JM. Proline oxidase promotes tumor cell survival in hypoxic tumor microenvironments. Cancer Res 2012; 72:3677-86. PMID:22609800; http://dx.doi.org/10.1158/0008-5472.CAN-12-0080.
44. Pandhare J, Donald SP, Cooper SK, Phang JM. Regulation and function of proline oxidase under nutrient stress. J Cell Biochem 2009; 107:759-68. PMID:19415679; http://dx.doi.org/10.1002/jcb.22174.
45. Liu W, Zabirnyk O, Wang H, Shiao YH, Nickerson ML, Khalil S, et al. miR-23b targets proline oxidase, a novel tumor suppressor protein in renal cancer. Oncogene 2010; 29:4914-24. PMID:20562915; http://dx.doi.org/10.1038/onc.2010.237.
46. Liu W, Le A, Hancock C, Lane AN, Dang CV, Fan TW, et al. Reprogramming of proline and glutamine metabolism contributes to the proliferative and metabolic responses regulated by oncogenic transcription factor c-MYC. Proc Natl Acad Sci U S A 2012; 109:8983-8. PMID:22615405; http://dx.doi.org/10.1073/pnas.1203244109.
47. Wanduragala S, Sanyal N, Liang X, Becker DF. Purification and characterization of Put1p from Saccharomyces cerevisiae. Arch Biochem Biophys 2010; 498:136-42. PMID:20450881; http://dx.doi.org/10.1016/j.abb.2010.04.020.
48. Chandel NS. Mitochondrial complex III: an essential component of universal oxygen sensing machinery? Respir Physiol Neurobiol 2010; 174:175-81. PMID:20708106; http://dx.doi.org/10.1016/j.resp.2010.08.004.
49. Adams E. Metabolism of proline and of hydroxyproline. Int Rev Connect Tissue Res 1970; 5:1-91. PMID:5500436.
50. Phang JM. The regulatory functions of proline and pyrroline-5-carboxylic acid. Curr Top Cell Regul 1985; 25:91-132. PMID:2410198.
51. Willis A, Bender HU, Steel G, Valle D. PRODH variants and risk for schizophrenia. Amino Acids 2008; 35:673-9. PMID:18528746; http://dx.doi.org/10.1007/s00726-008-0111-0.
52. Cooper SK, Pandhare J, Donald SP, Phang JM. A novel function for hydroxyproline oxidase in apoptosis through generation of reactive oxygen species. J Biol Chem 2008; 283:10485-92. PMID:18287100; http://dx.doi.org/10.1074/jbc.M702181200.
53. Wang R, Dillon CP, Shi LZ, Milasta S, Carter R, Finkelstein D, et al. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity 2011; 35:871-82. PMID:22195744; http://dx.doi.org/10.1016/j.immuni.2011.09.021.
54. Stoner GD, Merchant DJ.Amino acid utilization by L-M strain mouse cells in a chemically defined medium. In Vitro 1972; 7:330-43. PMID:5064338.
55. Windmueller HG, Spaeth AE. Uptake and metabolism of plasma glutamine by the small intestine. J Biol Chem 1974; 249:5070-9. PMID:4605420.
56. Reversade B, Escande-Beillard N, Dimopoulou A, Fischer B, Chng SC, Li Y, et al. Mutations in PYCR1 cause cutis laxa with progeroid features. Nat Genet 2009; 41:1016-21. PMID:19648921; http://dx.doi.org/10.1038/ng.413.
57. Meng Z, Lou Z, Liu Z, Li M, Zhao X, Bartlam M, et al. Crystal structure of human pyrroline-5-carboxylate reductase. J Mol Biol 2006; 359:1364-77. PMID:16730026; http://dx.doi.org/10.1016/j.jmb.2006.04.053.
58. De Ingeniis J, Ratnikov B, Richardson AD, Scott DA, Aza-Blanc P, De SK, et al. Functional specialization in proline biosynthesis of melanoma. PLoS One 2012; 7:e45190. PMID:23024808; http://dx.doi.org/10.1371/journal.pone.0045190.
59. Baumgartner MR, Hu CA, Almashanu S, Steel G, Obie C, Aral B, et al. Hyperammonemia with reduced ornithine, citrulline, arginine and proline: a new inborn error caused by a mutation in the gene encoding delta(1)-pyrroline-5-carboxylate synthase. Hum Mol Genet 2000; 9:2853-8. PMID:11092761; http://dx.doi.org/10.1093/hmg/9.19.2853.
60. Provenzano PP, Inman DR, Eliceiri KW, Keely PJ.Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene 2009; 28:4326-43. PMID:19826415; http://dx.doi.org/10.1038/onc.2009.299.
61. Fujimoto WY, Subak-Sharpe JH, Seegmiller JE. Hypoxanthine-guanine phosphoribosyltransferase deficiency: chemical agents selective for mutant or normal cultured fibroblasts in mixed and heterozygote cultures. Proc Natl Acad Sci U S A 1971; 68:1516-9. PMID:5283941; http://dx.doi.org/10.1073/pnas.68.7.1516.
62. Fiaschi T, Marini A, Giannoni E, Taddei ML, Gandellini P, De Donatis A, et al. Reciprocal metabolic reprogramming through lactate shuttle coordinately influences tumor-stroma interplay. Cancer Res 2012; 72:5130-40. PMID:22850421; http://dx.doi.org/10.1158/0008-5472.CAN-12-1949.
63. Phang JM, Yeh GC, Hagedorn CH. The inter-cellular proline cycle. Life Sci 1981; 28:53-8. PMID:6894321; http://dx.doi.org/10.1016/0024-3205(81)90365-9.
64. Hagedorn CH, Yeh GC, Phang JM. Transfer of 1-pyrroline-5-carboxylate as oxidizing potential from hepatocytes to erythrocytes. Biochem J 1982; 202:31-9. PMID:7082315.
65. Phang JM, Downing SJ, Yeh GC, Smith RJ, Williams JA, Hagedorn CH. Stimulation of the hexosemono-phosphate-pentose pathway by pyrroline-5-carboxylate in cultured cells. J Cell Physiol 1982; 110:255-61. PMID:6896335; http://dx.doi.org/10.1002/jcp.1041100306.
66. Cyr AR, Domann FE. The redox basis of epigenetic modifications: from mechanisms to functional consequences. Antioxid Redox Signal 2011; 15:551-89. PMID:20919933; http://dx.doi.org/10.1089/ars.2010.3492.
67. Lim SO, Gu JM, Kim MS, Kim HS, Park YN, Park CK, et al. Epigenetic changes induced by reactive oxygen species in hepatocellular carcinoma: methylation of the E-cadherin promoter. Gastroenterology 2008; 135:2128-40, 2140, e1-8. PMID:18801366; http://dx.doi.org/10.1053/j.gastro.2008.07.027.
68. Washington JM, Rathjen J, Felquer F, Lonic A, Bettess MD, Hamra N, et al. L-Proline induces differentiation of ES cells: a novel role for an amino acid in the regulation of pluripotent cells in culture. Am J Physiol Cell Physiol 2010; 298:C982-92. PMID:20164384; http://dx.doi.org/10.1152/ajp-cell.00498.2009.
69. Casalino L, Comes S, Lambazzi G, De Stefano B, Filosa S, De Falco S, et al. Control of embryonic stem cell metastability by L-proline catabolism. J Mol Cell Biol 2011; 3:108-22. PMID:21307025; http://dx.doi.org/10.1093/jmcb/mjr001.
70. Zarse K, Schmeisser S, Groth M, Priebe S, Beuster G, Kuhlow D, et al. Impaired insulin/IGF1 signaling extends life span by promoting mitochondrial L-proline catabolism to induce a transient ROS signal. Cell Metab 2012; 15:451-65. PMID:22482728; http://dx.doi.org/10.1016/j.cmet.2012.02.013.
71. Schroeder EA, Shadel GS. Alternative mitochondrial fuel extends life span. Cell Metab 2012; 15:417-8. PMID:22482723; http://dx.doi.org/10.1016/j.cmet.2012.03.011.