Skip to main content Accessibility help
×
Home

Effects of obesity and weight loss on mitochondrial structure and function and implications for colorectal cancer risk

  • S. P. Breininger (a1) (a2) (a3) (a4), F. C. Malcomson (a1) (a2) (a4), S. Afshar (a1) (a5), D. M. Turnbull (a3) (a4), L. Greaves (a3) (a4) and J. C. Mathers (a1) (a2) (a3) (a4)...

Abstract

Colorectal cancer (CRC) is the third most common cancer globally. CRC risk is increased by obesity, and by its lifestyle determinants notably physical inactivity and poor nutrition. Obesity results in increased inflammation and oxidative stress which cause genomic damage and contribute to mitochondrial dysregulation and CRC risk. The mitochondrial dysfunction associated with obesity includes abnormal mitochondrial size, morphology and reduced autophagy, mitochondrial biogenesis and expression of key mitochondrial regulators. Although there is strong evidence that increased adiposity increases CRC risk, evidence for the effects of intentional weight loss on CRC risk is much more limited. In model systems, energy depletion leads to enhanced mitochondrial integrity, capacity, function and biogenesis but the effects of obesity and weight loss on mitochondria in the human colon are not known. We are using weight loss following bariatric surgery to investigate the effects of altered adiposity on mitochondrial structure and function in human colonocytes. In summary, there is strong and consistent evidence in model systems and more limited evidence in human subjects that over-feeding and/or obesity result in mitochondrial dysfunction and that weight loss might mitigate or reverse some of these effects.

Copyright

Corresponding author

*Corresponding author: S. P. Breininger, email s.p.breininger@ncl.ac.uk

References

Hide All
1.Ferlay, J, Soerjomataram, I, Dikshit, R, et al. (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136, E359E386.
2.Arnold, M, Sierra, MS, Laversanne, M et al. (2016) Global patterns and trends in colorectal cancer incidence and mortality. Gut 66, 683691.
3.Ning, Y, Wang, L & Giovannucci, EL (2010) A quantitative analysis of body mass index and colorectal cancer: findings from 56 observational studies. Obes Rev 11, 1930.
4.Omata, F, Deshpande, GA, Ohde, S, et al. (2013) The association between obesity and colorectal adenoma: systematic review and meta-analysis. Scand J Gastroenterol 48, 136146.
5.Mathers, JC (2018) Obesity and bowel cancer: from molecular mechanisms to interventions. Nutr Res (New York, NY) [Epublication ahead of print version].
6.Ma, Y, Yang, Y, Wang, F, et al. (2013) Obesity and risk of colorectal cancer: a systematic review of prospective studies. PloS One 8, e53916.
7.Keum, N, Lee, DH, Kim, R, et al. (2015) Visceral adiposity and colorectal adenomas: dose-response meta-analysis of observational studies. Ann Oncology: Official J Euro Soc Medical Oncology/ESMO 26, 11011109.
8.Mundade, R, Imperiale, TF, Prabhu, L, et al. (2014) Genetic pathways, prevention, and treatment of sporadic colorectal cancer. Oncoscience 1, 400406.
9.Fearon, ER (2011) Molecular genetics of colorectal cancer. Annu Rev Pathol 6, 479507.
10.Humphries, A & Wright, NA. (2008) Colonic crypt organization and tumorigenesis. Nat Rev Cancer 8, 415424.
11.Lao, VV & Grady, WM (2011) Epigenetics and colorectal cancer. Nat Rev Gastroenterol & Hepatol 8, 686700.
12.Vogelstein, B, Fearon, ER, Hamilton, SR et al. (1988) Genetic alterations during colorectal-tumor development. N Engl J Med 319, 525532.
13.Vazquez, A, Bond, EE, Levine, AJ et al. (2008) The genetics of the p53 pathway, apoptosis and cancer therapy. Nat Rev Drug Discov 7, 979987.
14.Hanahan, D & Weinberg, RA (2011) Hallmarks of cancer: the next generation. Cell 144, 646674.
15.Grady, WM, Rajput, A, Myeroff, L et al. (1998) Mutation of the type II transforming growth factor-beta receptor is coincident with the transformation of human colon adenomas to malignant carcinomas. Cancer Res 58, 31013104.
16.Bellam, N & Pasche, B (2010) Tgf-beta signaling alterations and colon cancer. Cancer Treat Res 155, 85103.
17.Sjoblom, T, Jones, S, Wood, LD et al. (2006) The consensus coding sequences of human breast and colorectal cancers. Science (New York, NY) 314, 268274.
18.Eppert, K, Scherer, SW, Ozcelik, H et al. (1996) MADR2 maps to 18q21 and encodes a TGFbeta-regulated MAD-related protein that is functionally mutated in colorectal carcinoma. Cell 86, 543552.
19.Takaku, K, Oshima, M, Miyoshi, H et al. (1998) Intestinal tumorigenesis in compound mutant mice of both Dpc4 (Smad4) and Apc genes. Cell 92, 645656.
20.Wood, LD, Parsons, DW, Jones, S et al. (2007) The genomic landscapes of human breast and colorectal cancers. Science (New York, NY) 318, 11081113.
21.Grady, WM & Carethers, JM (2008) Genomic and epigenetic instability in colorectal cancer pathogenesis. Gastroenterology 135, 10791099.
22.Colussi, D, Brandi, G, Bazzoli, F et al. (2013) Molecular pathways involved in colorectal cancer: implications for disease behavior and prevention. Int J Mol Sci 14, 1636516385.
23.World Cancer Research Fund/American Institute for Cancer Research. (2007) Food, Nutrition, Physical Activity, and the Prevention of Cancer: a Global Perspective. Washington, DC American Institute for cancer research.
24.World Cancer Research Fund (2018) Diet, Nutrition, Physical Activity and Cancer: a Global Perspective. Continuous Update Project Expert Report 2018. Available at dietandcancerreport.org
25.Edwards, RA, Witherspoon, M, Wang, K et al. (2009) Epigenetic repression of DNA mismatch repair by inflammation and hypoxia in inflammatory bowel disease-associated colorectal cancer. Cancer Res 69, 64236429.
26.Kiraly, O, Gong, G, Olipitz, W et al. (2015) Inflammation-induced cell proliferation potentiates DNA damage-induced mutations in vivo. PLoS Genet 11, e1004901.
27.Tuo, D, Christopher, JL, Stephen, B et al. (2016) Obesity, inflammation, and cancer. Annu Rev of Pathol: Mech Dis 11, 421449.
28.Wei, EK, Ma, J, Pollak, MN et al. (2005) A prospective study of C-peptide, insulin-like growth factor-I, insulin-like growth factor binding protein-1, and the risk of colorectal cancer in women. Cancer Epidemiol Biomarkers Prev 14, 850855.
29.Gunter, MJ, Stolzenberg-Solomon, R, Cross, AJ et al. (2006) A prospective study of serum C-reactive protein and colorectal cancer risk in men. Cancer Res 66, 24832487.
30.Otani, T, Iwasaki, M, Sasazuki, S et al. (2006) Plasma C-reactive protein and risk of colorectal cancer in a nested case-control study: Japan Public Health Center-based prospective study. Cancer Epidemiol Biomarkers Prev 15, 690695.
31.Erlinger, TP, Platz, EA, Rifai, N et al. (2004) C-reactive protein and the risk of incident colorectal cancer. JAMA 291, 585590.
32.Poullis, A, Foster, R, Shetty, A et al. (2004) Bowel inflammation as measured by fecal calprotectin: a link between lifestyle factors and colorectal cancer risk. Cancer Epidemiol Biomarkers Prev 13, 279284.
33.John, BJ, Irukulla, S, Abulafi, AM et al. (2006) Systematic review: adipose tissue, obesity and gastrointestinal diseases. Aliment Pharmacol Ther 23, 15111523.
34.Karin, M, Cao, Y, Greten, FR et al. (2002) NF-kappaB in cancer: from innocent bystander to major culprit. Nat Rev Cancer 2, 301310.
35.Karahalios, A, English, DR & Simpson, JA (2015) Weight change and risk of colorectal cancer: a systematic review and meta-analysis. Am J Epidemiol 181, 832845.
36.Beeken, RJ, Croker, H, Heinrich, M et al. (2017) The Impact of Diet-Induced Weight Loss on Biomarkers for Colorectal Cancer: An Exploratory Study (INTERCEPT). Obesity (Silver Spring, MD) 25, Suppl. 2, S95s101.
37.Nicklas, BJ, Ambrosius, W, Messier, SP et al. (2004) Diet-induced weight loss, exercise, and chronic inflammation in older, obese adults: a randomized controlled clinical trial. Am J Clin Nutr 79, 544551.
38.Lakhdar, N, Denguezli, M, Zaouali, M et al. (2013) Diet and diet combined with chronic aerobic exercise decreases body fat mass and alters plasma and adipose tissue inflammatory markers in obese women. Inflammation 36, 12391247.
39.Pendyala, S, Neff, LM, Suárez-Fariñas, M et al. (2011) Diet-induced weight loss reduces colorectal inflammation: implications for colorectal carcinogenesis. Am J Clin Nutr 93, 234242.
40.Kant, P, Fazakerley, R & Hull, MA (2013) Faecal calprotectin levels before and after weight loss in obese and overweight subjects. Int J Obes (2005) 37, 317319.
41.Afshar, S, Kelly, SB, Seymour, K et al. (2014) The effects of bariatric surgery on colorectal cancer risk: systematic review and meta-analysis. Obes Sur 24, 17931799.
42.Aravani, A, Downing, A, Thomas, JD et al. (2018) Obesity surgery and risk of colorectal and other obesity-related cancers: An English population-based cohort study. Cancer Epidemiol 53, 99104.
43.Afshar, S, Malcomson, F, Kelly, SB et al. (2018) Biomarkers of colorectal cancer risk decrease 6 months after Roux-en-Y gastric bypass surgery. Obes Sur 28, 945954.
44.Sainsbury, A, Goodlad, RA, Perry, SL et al. (2008) Increased colorectal epithelial cell proliferation and crypt fission associated with obesity and roux-en-Y gastric bypass. Cancer Epidemiol Biomarkers Prev 17, 14011410.
45.Kant, P, Sainsbury, A, Reed, KR et al. (2011) Rectal epithelial cell mitosis and expression of macrophage migration inhibitory factor are increased 3 years after Roux-en-Y gastric bypass (RYGB) for morbid obesity: implications for long-term neoplastic risk following RYGB. Gut 60, 893901.
46.Fernandez-Silva, P, Enriquez, JA & Montoya, J (2003) Replication and transcription of mammalian mitochondrial DNA. Exp Physiol 88, 4156.
47.Stewart, JB & Chinnery, PF (2015) The dynamics of mitochondrial DNA heteroplasmy: implications for human health and disease. Nat Rev Genet 16, 530542.
48.Case, JT & Wallace, DC (1981) Maternal inheritance of mitochondrial DNA polymorphisms in cultured human fibroblasts. Somatic cell Genetics 7, 103108.
49.Carling, PJ, Cree, LM & Chinnery, PF (2011) The implications of mitochondrial DNA copy number regulation during embryogenesis. Mitochondrion 11, 686692.
50.Gilkerson, R, Bravo, L, Garcia, I et al. (2013) The mitochondrial nucleoid: integrating mitochondrial DNA into cellular homeostasis. Cold Spring Harbor Perspectives Biol 5, a011080.
51.Sousa, JS, D'Imprima, E & Vonck, J (2018) Mitochondrial respiratory chain complexes. Subcell Biochem 87, 167227.
52.Anderson, S, Bankier, AT, Barrell, BG et al. (1981) Sequence and organization of the human mitochondrial genome. Nature 290, 457.
53.Shadel, GS & Clayton, DA (1993) Mitochondrial transcription initiation. Variation and conservation. J Biol Chem 268(22), 16083–6.
54.Larsson, NG & Clayton, DA (1995) Molecular genetic aspects of human mitochondrial disorders. Annu Rev Genet 29, 151178.
55.Johns, DR (1995) Seminars in medicine of the Beth Israel Hospital, Boston. Mitochondrial DNA and disease. N Engl J Med 333(10), 638644.
56.Gorman, GS, Chinnery, PF, DiMauro, S et al. (2016) Mitochondrial diseases. Nature Revi Disease Primers 2, 16080.
57.Machado, AM, Figueiredo, C, Seruca, R et al. (2010) Helicobacter pylori infection generates genetic instability in gastric cells. Biochim Biophys Acta 1806(1), 5865.
58.Birch-Machin, MA & Swalwell, H (2010) How mitochondria record the effects of UV exposure and oxidative stress using human skin as a model tissue. Mutagenesis 25(2), 101107.
59.Prior, SL, Griffiths, AP, Baxter, JM et al. (2006) Mitochondrial DNA mutations in oral squamous cell carcinoma. Carcinogenesis 27(5), 945950.
60.Tan, D, Goerlitz, DS, Dumitrescu, RG et al. (2008) Associations between cigarette smoking and mitochondrial DNA abnormalities in buccal cells. Carcinogenesis 02/14 10/11/received 01/22/revised 01/28/accepted;29(6), 11701177.
61.King, MP & Attardi, G (1989) Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science (New York, NY) 246(4929), 500503.
62.Boulet, L, Karpati, G & Shoubridge, EA (1992) Distribution and threshold expression of the tRNA(Lys) mutation in skeletal muscle of patients with myoclonic epilepsy and ragged-red fibers (MERRF). Am J Hum Genet 51(6), 11871200.
63.Chen, Q, Vazquez, EJ, Moghaddas, S et al. (2003) Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem 278(38), 3602736031.
64.Gao, CL, Zhu, C, Zhao, YP et al. (2010) Mitochondrial dysfunction is induced by high levels of glucose and free fatty acids in 3T3-L1 adipocytes. Mol Cell Endocrinol 320(1–2), 2533.
65.Zinovkina, LA (2018) Mechanisms of mitochondrial DNA repair in mammals. Biochemistry Biokhimiia 83(3), 233249.
66.Allen, JA & Coombs, MM (1980) Covalent binding of polycyclic aromatic compounds to mitochondrial and nuclear DNA. Nature 287(5779), 244245.
67.Cakir, Y, Yang, Z, Knight, CA et al. (2007) Effect of alcohol and tobacco smoke on mtDNA damage and atherogenesis. Free Radic Biol Med 43(9), 12791288.
68.Warburg, O (1956)On respiratory impairment in cancer cells. Science (New York, NY) 124(3215), 269270.
69.Liberti, MV & Locasale, JW (2016) The warburg effect: how does it benefit cancer cells? Trends Biochem Sci 41(3), 211218.
70.Shidara, Y, Yamagata, K, Kanamori, T et al. (2005) Positive contribution of pathogenic mutations in the mitochondrial genome to the promotion of cancer by prevention from apoptosis. Cancer Res 65(5), 16551663.
71.Ishikawa, K, Takenaga, K, Akimoto, M et al. (2008) ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis. Science (New York, NY) 320(5876), 661664.
72.Polyak, K, Li, Y, Zhu, H et al. (1998) Somatic mutations of the mitochondrial genome in human colorectal tumours. Nat Genet 20(3), 291293.
73.He, Y, Wu, J, Dressman, DC et al. (2010) Heteroplasmic mitochondrial DNA mutations in normal and tumour cells. Nature 464(7288), 610614.
74.Greaves, LC, Nooteboom, M, Elson, JL et al. (2014) Clonal expansion of early to mid-life mitochondrial DNA point mutations drives mitochondrial dysfunction during human ageing. PLoS Genet 10(9), e1004620.
75.Greaves, LC, Barron, MJ, Plusa, S et al. (2010) Defects in multiple complexes of the respiratory chain are present in ageing human colonic crypts. Exp Gerontol 45(7–8), 573579.
76.Brookheart, RT, Swearingen, AR, Collins, CA et al. (2017) High-sucrose-induced maternal obesity disrupts ovarian function and decreases fertility in Drosophila melanogaster. Biochim Biophys Acta 1863, 12551263.
77.Sparks, LM, Xie, H, Koza, RA et al. (2005) A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 54(7), 19261933.
78.Stewart, LK, Wang, Z, Ribnicky, D et al. (2009) Failure of dietary quercetin to alter the temporal progression of insulin resistance among tissues of C57BL/6J mice during the development of diet-induced obesity. Diabetologia 52(3), 514523.
79.Devarshi, PP, McNabney, SM & Henagan, TM (2017) Skeletal muscle nucleo-mitochondrial crosstalk in obesity and type 2 diabetes. Int J Mol Sci 18, 831.
80.Das, N, Mandala, A, Bhattacharjee, S et al. (2017) Dietary fat proportionately enhances oxidative stress and glucose intolerance followed by impaired expression of the genes associated with mitochondrial biogenesis. Food & Function 8(4), 15771586.
81.Putti, R, Sica, R, Migliaccio, V et al. (2015) Diet impact on mitochondrial bioenergetics and dynamics. Front Physiol 6, 109.
82.Valerio, A, Cardile, A, Cozzi, V et al. (2006) TNF-alpha downregulates eNOS expression and mitochondrial biogenesis in fat and muscle of obese rodents. J Clin Invest 116(10), 27912798.
83.Sutherland, LN, Capozzi, LC, Turchinsky, NJ et al. (2008) Time course of high-fat diet-induced reductions in adipose tissue mitochondrial proteins: Potential mechanisms and the relationship to glucose intolerance. Am J Physiol Endocrinol Metab 295(5), E1076E1E83.
84.Nishida, K & Otsu, K (2017) Inflammation and metabolic cardiomyopathy. Cardiovasc Res 113(4), 389398.
85.Guo, CA & Guo, S (2017) Insulin receptor substrate signaling controls cardiac energy metabolism and heart failure. J Endocrinol 233, R131R143.
86.Choo, HJ, Kim, JH, Kwon, OB et al. (2006) Mitochondria are impaired in the adipocytes of type 2 diabetic mice. Diabetologia 49(4), 784791.
87.Liu, R, Jin, P, Liqun, Y et al. (2014) Impaired mitochondrial dynamics and bioenergetics in diabetic skeletal muscle. PloS One 9(3), e92810.
88.Semple, RK, Crowley, VC, Sewter, CP et al. (2004) Expression of the thermogenic nuclear hormone receptor coactivator PGC-1alpha is reduced in the adipose tissue of morbidly obese subjects. Int J Obes Relat Metab Disord 28(1), 176179.
89.Yin, X, Lanza, IR, Swain, JM et al. (2014) Adipocyte mitochondrial function is reduced in human obesity independent of fat cell size. J Clin Endocrinol Metab 11/25 08/02/received 11/12/accepted;99(2), E209EE16.
90.Heinonen, S, Buzkova, J, Muniandy, M et al. (2015) Impaired mitochondrial biogenesis in adipose tissue in acquired obesity. Diabetes 64(9), 31353145.
91.Ejarque, M, Ceperuelo-Mallafré, V, Serena, C et al. (2018) Adipose tissue mitochondrial dysfunction in human obesity is linked to a specific DNA methylation signature in adipose-derived stem cells. Int J Obes [Epublication 27 September 2018].
92.Kras, KA, Langlais, PR, Hoffman, N et al. (2018) Obesity modifies the stoichiometry of mitochondrial proteins in a way that is distinct to the subcellular localization of the mitochondria in skeletal muscle. Metabolism 89, 1826.
93.Bournat, JC & Brown, CW (2010) Mitochondrial dysfunction in obesity. Curr opin Endocrinol, Diabetes Obes 17(5), 446452.
94.Rogge, MM (2009) The role of impaired mitochondrial lipid oxidation in obesity. Biol Res Nurs 10(4), 356373.
95.de Mello, AH, Costa, AB, Engel, JDG et al. (2018) Mitochondrial dysfunction in obesity. Life Sci 2018/01/01/;192, 2632.
96.Zid, BM, Rogers, AN, Katewa, SD et al. (2009) 4E-BP extends lifespan upon dietary restriction by enhancing mitochondrial activity in Drosophila. Cell 139(1), 149160.
97.Nisoli, E, Tonello, C, Cardile, A et al. (2005) Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science (New York, NY) 310(5746), 314317.
98.Raffaello, A & Rizzuto, R (2011) Mitochondrial longevity pathways. Biochim Biophys Acta 1813(1), 260268.
99.Reznick, RM, Zong, H, Li, J et al. (2007) Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis. Cell Metabolism 5(2), 151156.
100.Burnett, C, Valentini, S, Cabreiro, F et al. (2011) Absence of effects of Sir2 overexpression on lifespan in C. elegans and Drosophila. Nature 477(7365), 482485.
101.Martin-Montalvo, A & de Cabo, R (2013) Mitochondrial metabolic reprogramming induced by calorie restriction. Antioxid Redox Signal 19(3), 310320.
102.Wai, T & Langer, T (2016) Mitochondrial dynamics and metabolic regulation. Trends Endocrinol Metab 2016/02/01/;27(2), 105117.
103.Rambold, AS, Kostelecky, B, Elia, N et al. (2011) Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc Natl Acad Sci U S A 108(25), 10190–5.
104.Lee, JY, Kapur, M, Li, M et al. (2014) MFN1 deacetylation activates adaptive mitochondrial fusion and protects metabolically challenged mitochondria. J Cell Sci 127(Pt 22), 49544963.
105.McKiernan, SH, Colman, RJ, Lopez, M et al. (2011) Caloric restriction delays aging-induced cellular phenotypes in rhesus monkey skeletal muscle. Exp Gerontol 46(1), 2329.
106.Bach, D, Naon, D, Pich, S et al. (2005) Expression of Mfn2, the Charcot-Marie-Tooth neuropathy type 2A gene, in human skeletal muscle: effects of type 2 diabetes, obesity, weight loss, and the regulatory role of tumor necrosis factor alpha and interleukin-6. Diabetes 54(9), 26852693.
107.Civitarese, AE, Carling, S, Heilbronn, LK et al. (2007) Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLoS Medicine 4(3), e76.
108.Toledo, FG, Menshikova, EV, Azuma, K et al. (2008) Mitochondrial capacity in skeletal muscle is not stimulated by weight loss despite increases in insulin action and decreases in intramyocellular lipid content. Diabetes 57(4), 987994.
109.Coen, PM, Menshikova, EV, Distefano, G et al. (2015) Exercise and weight loss improve muscle mitochondrial respiration, lipid partitioning, and insulin sensitivity after gastric bypass surgery. Diabetes 64(11), 37373750.
110.Jahansouz, C, Serrot, FJ, Frohnert, BI et al. (2015) Roux-en-Y gastric bypass acutely decreases protein carbonylation and increases expression of mitochondrial biogenesis genes in subcutaneous adipose tissue. Obes Sur 25(12), 23762385.
111.Moreno-Castellanos, N, Guzman-Ruiz, R, Cano, DA et al. (2016) The effects of bariatric surgery-induced weight loss on adipose tissue in morbidly obese women depends on the initial metabolic status. Obes Sur 26(8), 17571767.
112.Fernstrom, M, Bakkman, L, Loogna, P et al. (2016) Improved muscle mitochondrial capacity following gastric bypass surgery in obese subjects. Obes Sur 26(7), 13911397.
113.Camastra, S, Vitali, A, Anselmino, M et al. (2017) Muscle and adipose tissue morphology, insulin sensitivity and beta-cell function in diabetic and nondiabetic obese patients: effects of bariatric surgery. Scientific Rep 2017/08/21;7(1), 9007.
114.Martinez de la Escalera, L, Kyrou, I, Vrbikova, J et al. (2017) Impact of gut hormone FGF-19 on type-2 diabetes and mitochondrial recovery in a prospective study of obese diabetic women undergoing bariatric surgery. BMC Medicine 15(1), 34.
115.Handschin, C & Spiegelman, BM (2006) Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr Rev 27(7), 728735.
116.Cheng, Z & Almeida, FA (2014) Mitochondrial alteration in type 2 diabetes and obesity: An epigenetic link. Cell Cycle 02/12 11/20/received 01/13/revised 02/11/accepted;13(6), 890897.
117.Padidar, S, Farquharson, AJ, Rucklidge, GJ et al. (2008) Influence of increased adiposity on mitochondrial-associated proteins of the rat colon: A proteomic and transcriptomic analysis. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease 2008/09/01/;1782(9), 532541.
118.Nimri, L, Saadi, J, Peri, I et al. (2015) Mechanisms linking obesity to altered metabolism in mice colon carcinogenesis. Oncotarget 6(35), 3819538209.
119.Yehuda-Shnaidman, E, Nimri, L, Tarnovscki, T et al. (2013) Secreted human adipose leptin decreases mitochondrial respiration in HCT116 colon cancer cells. PloS One 8(9), e74843-e.

Keywords

Effects of obesity and weight loss on mitochondrial structure and function and implications for colorectal cancer risk

  • S. P. Breininger (a1) (a2) (a3) (a4), F. C. Malcomson (a1) (a2) (a4), S. Afshar (a1) (a5), D. M. Turnbull (a3) (a4), L. Greaves (a3) (a4) and J. C. Mathers (a1) (a2) (a3) (a4)...

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed