Physical activity and breast cancer survival: An epigenetic link through reduced methylation of a tumor suppressor gene L3MBTL1

Breast Cancer Research and Treatment

Volumn 133, Issue 1, 2012, Pages 127-135

  Zeng, Hongmei ^a,b   Irwin, Melinda L ^a   Lu, Lingeng ^a   Risch, Harvey ^a   Mayne, Susan ^a   Mu, Lina ^c   Deng, Qian ^a   Scarampi, Luca ^d   Mitidieri, Marco ^d   Katsaros, Dionyssios ^d   Yu, Herbert ^a  

^a YALE CANCER CENTER   (United States)

^b PEKING UNIVERSITY CANCER HOSPITAL AND INSTITUTE   (China)

^c UNIVERSITY AT BUFFALO   (United States)

^d UNIVERSITY OF TURIN   (Italy)

Author keywords

DNA methylation; L3MBTL1; Physical activity; Survival; Tumor suppressor gene

Indexed keywords

GENOMIC DNA; HORMONE RECEPTOR;

AEROBIC EXERCISE; ANALYTIC METHOD; ARTICLE; BLOOD ANALYSIS; BREAST CANCER; BREAST TUMOR; CANCER GRADING; CANCER MORTALITY; CANCER PATIENT; CANCER RECURRENCE; CANCER SURVIVAL; CHROMATIN; CONTROLLED STUDY; DNA METHYLATION; DNA MICROARRAY; EPIGENETICS; FEMALE; GENE EXPRESSION REGULATION; GENE FUNCTION; GERM LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; L3MBTL1 GENE; LEUKOCYTE; MAJOR CLINICAL STUDY; METHYLATION SPECIFIC POLYMERASE CHAIN REACTION; OVERALL SURVIVAL; PHYSICAL ACTIVITY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL; SURVIVAL PREDICTION; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE;

BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CARCINOMA, LOBULAR; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; HUMANS; KAPLAN-MEIER ESTIMATE; MOTOR ACTIVITY;

EID: 84860318482     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-011-1716-7     Document Type: Article

References (34)

1. CN Holick PA Newcomb A Trentham-Dietz L Titus-Ernstoff AJ Bersch MJ Stampfer JA Baron KM Egan WC Willett 2008 Physical activity and survival after diagnosis of invasive breast cancer Cancer Epidemiol Biomarkers Prev 17 2 379 386 18250341 10.1158/1055-9965.EPI-07-0771 (Pubitemid 351272790)
2. MD Holmes WY Chen D Feskanich CH Kroenke GA Colditz 2005 Physical activity and survival after breast cancer diagnosis JAMA 293 20 2479 2486 15914748 10.1001/jama.293.20.2479 1:CAS:528:DC%2BD2MXksFWksbk%3D (Pubitemid 40705729)
3. ML Irwin AW Smith A McTiernan R Ballard-Barbash K Cronin FD Gilliland RN Baumgartner KB Baumgartner L Bernstein 2008 Influence of pre- and postdiagnosis physical activity on mortality in breast cancer survivors: the health, eating, activity, and lifestyle study J Clin Oncol 26 24 3958 3964 18711185 10.1200/JCO.2007.15.9822
4. A McTiernan SS Tworoger KB Rajan Y Yasui B Sorenson CM Ulrich J Chubak FZ Stanczyk D Bowen ML Irwin, et al. 2004 Effect of exercise on serum androgens in postmenopausal women: a 12-month randomized clinical trial Cancer Epidemiol Biomarkers Prev 13 7 1099 1105 15247119 1:CAS:528:DC%2BD2cXlsFeksr8%3D (Pubitemid 38917897)
5. A McTiernan SS Tworoger CM Ulrich Y Yasui ML Irwin KB Rajan B Sorensen RE Rudolph D Bowen FZ Stanczyk, et al. 2004 Effect of exercise on serum estrogens in postmenopausal women: a 12-month randomized clinical trial Cancer Res 64 8 2923 2928 15087413 10.1158/0008-5472.CAN-03-3393 1:CAS:528:DC%2BD2cXjtV2lurk%3D (Pubitemid 38500634)
6. PJ Goodwin M Ennis KI Pritchard ME Trudeau J Koo Y Madarnas W Hartwick B Hoffman N Hood 2002 Fasting insulin and outcome in early-stage breast cancer: results of a prospective cohort study J Clin Oncol 20 1 42 51 11773152 10.1200/JCO.20.1.42 1:CAS:528:DC%2BD38XnsFekug%3D%3D (Pubitemid 34032594)
7. HK Neilson CM Friedenreich NT Brockton RC Millikan 2009 Physical activity and postmenopausal breast cancer: proposed biologic mechanisms and areas for future research Cancer Epidemiol Biomarkers Prev 18 1 11 27 19124476 10.1158/1055-9965.EPI-08-0756 1:CAS:528:DC%2BD1MXhvFektQ%3D%3D
8. JA Ligibel N Campbell A Partridge WY Chen T Salinardi H Chen K Adloff A Keshaviah EP Winer 2008 Impact of a mixed strength and endurance exercise intervention on insulin levels in breast cancer survivors J Clin Oncol 26 6 907 912 18281663 10.1200/JCO.2007.12.7357 1:CAS:528:DC%2BD1cXjtFeltro%3D (Pubitemid 351398083)
9. PJ Goodwin M Ennis KI Pritchard ME Trudeau J Koo W Hartwick B Hoffma N Hood 2002 Insulin-like growth factor binding proteins 1 and 3 and breast cancer outcomes Breast Cancer Res Treat 74 1 65 76 12150454 10.1023/A:1016075709022 1:CAS:528:DC%2BD38XkslKltL0%3D (Pubitemid 34734598)
10. ML Irwin K Varma M Alvarez-Reeves L Cadmus A Wiley GG Chung L Dipietro ST Mayne H Yu 2009 Randomized controlled trial of aerobic exercise on insulin and insulin-like growth factors in breast cancer survivors: the Yale Exercise and Survivorship study Cancer Epidemiol Biomarkers Prev 18 1 306 313 19124513 10.1158/1055-9965.EPI-08-0531 1:CAS:528:DC%2BD1MXhvFCjsg%3D%3D
11. KH Schmitz RL Ahmed PJ Hannan D Yee 2005 Safety and efficacy of weight training in recent breast cancer survivors to alter body composition, insulin, and insulin-like growth factor axis proteins Cancer Epidemiol Biomarkers Prev 14 7 1672 1680 16030100 10.1158/1055-9965.EPI-04-0736 1:CAS:528: DC%2BD2MXmt1Grsb8%3D (Pubitemid 40995078)
12. AS Fairey KS Courneya CJ Field GJ Bell LW Jones JR Mackey 2003 Effects of exercise training on fasting insulin, insulin resistance, insulin-like growth factors, and insulin-like growth factor binding proteins in postmenopausal breast cancer survivors: a randomized controlled trial Cancer Epidemiol Biomarkers Prev 12 8 721 727 12917202 1:CAS:528:DC%2BD3sXmt1elsrg%3D (Pubitemid 36993161)
13. YM Coyle XJ Xie CM Lewis D Bu S Milchgrub DM Euhus 2007 Role of physical activity in modulating breast cancer risk as defined by APC and RASSF1A promoter hypermethylation in nonmalignant breast tissue Cancer Epidemiol Biomarkers Prev 16 2 192 196 17301249 10.1158/1055-9965.EPI-06-0700 1:CAS:528: DC%2BD2sXhs1yls7w%3D (Pubitemid 46383333)
14. Y Yuasa H Nagasaki Y Akiyama Y Hashimoto T Takizawa K Kojima T Kawano K Sugihara K Imai K Nakachi 2009 DNA methylation status is inversely correlated with green tea intake and physical activity in gastric cancer patients Int J Cancer 124 11 2677 2682 19170207 10.1002/ijc.24231 1:CAS:528: DC%2BD1MXltlegurs%3D
15. ML Irwin L Cadmus M Alvarez-Reeves M O'Neil E Mierzejewski R Latka H Yu L Dipietro B Jones MT Knobf, et al. 2008 Recruiting and retaining breast cancer survivors into a randomized controlled exercise trial: the Yale Exercise and Survivorship Study Cancer 112 11 Suppl 2593 2606 18428192 10.1002/cncr.23446
16. L Mu D Katsaros L Lu M Preti A Durando R Arisio H Yu 2008 TGF-beta1 genotype and phenotype in breast cancer and their associations with IGFs and patient survival Br J Cancer 99 8 1357 1363 18827819 10.1038/sj.bjc.6604689 1:CAS:528:DC%2BD1cXht1Cmtr%2FN
17. BE Ainsworth WL Haskell MC Whitt ML Irwin AM Swartz SJ Strath WL O'Brien DR Bassett Jr KH Schmitz PO Emplaincourt, et al. 2000 Compendium of physical activities: an update of activity codes and MET intensities Med Sci Sports Exerc 32 9 Suppl S498 S504 10993420 1:STN:280:DC%2BD3cvktlegsg%3D%3D
18. L Lu D Katsaros IA de la Longrais O Sochirca H Yu 2007 Hypermethylation of let-7a-3 in epithelial ovarian cancer is associated with low insulin-like growth factor-II expression and favorable prognosis Cancer Res 67 21 10117 10122 17974952 10.1158/0008-5472.CAN-07-2544 1:CAS:528:DC%2BD2sXht1erur7M (Pubitemid 350070782)
19. A Plaitakis I Zaganas 2001 Regulation of human glutamate dehydrogenases: implications for glutamate, ammonia and energy metabolism in brain J Neurosci Res 66 5 899 908 11746417 10.1002/jnr.10054 1:CAS:528:DC%2BD3MXpt1Sgt7k%3D (Pubitemid 33126392)
20. R Bonasio E Lecona D Reinberg 2010 MBT domain proteins in development and disease Semin Cell Dev Biol 21 2 221 223 19778625 10.1016/j.semcdb.2009.09.010 1:CAS:528:DC%2BC3cXisFGrt7k%3D
21. K Satoh E Ginsburg BK Vonderhaar 2004 Msx-1 and Msx-2 in mammary gland development J Mammary Gland Biol Neoplasia 9 2 195 205 15300013 10.1023/B:JOMG.0000037162.84758.b5 (Pubitemid 39177503)
22. K Nakajima M Takeoka M Mori S Hashimoto A Sakurai H Nose K Higuchi N Itano M Shiohara T Oh, et al. 2010 Exercise effects on methylation of ASC gene Int J Sports Med 31 9 671 675 20200803 10.1055/s-0029-1246140 1:CAS:528:DC%2BC3cXhtlemsrbK
23. DG DeNardo LM Coussens 2007 Inflammation and breast cancer. Balancing immune response: crosstalk between adaptive and innate immune cells during breast cancer progression Breast Cancer Res 9 4 212 17705880 10.1186/bcr1746
24. P Allavena A Sica G Solinas C Porta A Mantovani 2008 The inflammatory micro-environment in tumor progression: the role of tumor-associated macrophages Crit Rev Oncol Hematol 66 1 1 9 17913510 10.1016/j.critrevonc.2007.07.004 (Pubitemid 351324128)
25. P Boccuni D MacGrogan JM Scandura SD Nimer 2003 The human L(3)MBT polycomb group protein is a transcriptional repressor and interacts physically and functionally with TEL (ETV6) J Biol Chem 278 17 15412 15420 12588862 10.1074/jbc.M300592200 1:CAS:528:DC%2BD3sXjtVClt7s%3D (Pubitemid 36799881)
26. AJ Bench J Li BJ Huntly E Delabesse N Fourouclas AR Hunt P Deloukas AR Green 2004 Characterization of the imprinted polycomb gene L3MBTL, a candidate 20q tumour suppressor gene, in patients with myeloid malignancies Br J Haematol 127 5 509 518 15566354 10.1111/j.1365-2141.2004.05278.x 1:CAS:528: DC%2BD2MXjslGjsQ%3D%3D (Pubitemid 39627175)
27. PA Northcott Y Nakahara X Wu L Feuk DW Ellison S Croul S Mack PN Kongkham J Peacock A Dubuc, et al. 2009 Multiple recurrent genetic events converge on control of histone lysine methylation in medulloblastoma Nat Genet 41 4 465 472 19270706 10.1038/ng.336 1:CAS:528:DC%2BD1MXivVKntro%3D
28. L Addou-Klouche J Adelaide P Finetti N Cervera A Ferrari I Bekhouche F Sircoulomb C Sotiriou P Viens S Moulessehoul, et al. 2010 Loss, mutation and deregulation of L3MBTL4 in breast cancers Mol Cancer 9 213 20698951 10.1186/1476-4598-9-213
29. A Janic L Mendizabal S Llamazares D Rossell C Gonzalez 2010 Ectopic expression of germline genes drives malignant brain tumor growth in Drosophila Science 330 6012 1824 1827 21205669 10.1126/science.1195481 1:CAS:528: DC%2BC3cXhsF2jtbvE
30. K Buehlmeyer F Doering H Daniel B Kindermann T Schulz H Michna 2008 Alteration of gene expression in rat colon mucosa after exercise Ann Anat 190 1 71 80 18342145 10.1016/j.aanat.2007.04.002 1:CAS:528:DC%2BD1cXkvVaktbY%3D (Pubitemid 351168655)
31. AD Luster SC Jhanwar RS Chaganti JH Kersey JV Ravetch 1987 Interferon-inducible gene maps to a chromosomal band associated with a (4;11) translocation in acute leukemia cells Proc Natl Acad Sci USA 84 9 2868 2871 2437586 10.1073/pnas.84.9.2868 1:CAS:528:DyaL2sXktVWruro%3D (Pubitemid 17064740)
32. N O'Donovan M Galvin JG Morgan 1999 Physical mapping of the CXC chemokine locus on human chromosome 4 Cytogenet Cell Genet 84 1-2 39 42 10343098 10.1159/000015209 (Pubitemid 29218923)
33. K Ueda DP Clark CJ Chen IB Roninson MM Gottesman I Pastan 1987 The human multidrug resistance (mdr1) gene. cDNA cloning and transcription initiation J Biol Chem 262 2 505 508 3027054 1:CAS:528:DyaL2sXnvFKitw%3D%3D (Pubitemid 17005205)
34. WT Wong MH Kraus F Carlomagno A Zelano T Druck CM Croce K Huebner PP Di Fiore 1994 The human eps15 gene, encoding a tyrosine kinase substrate, is conserved in evolution and maps to 1p31-p32 Oncogene 9 6 1591 1597 8183552 1:CAS:528:DyaK2cXlt1Kmtrg%3D