Secreted Human Adipose Leptin Decreases Mitochondrial Respiration in HCT116 Colon Cancer Cells

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Yehuda Shnaidman, Einav ^a   Nimri, Lili ^a   Tarnovscki, Tanya ^b   Kirshtein, Boris ^c   Rudich, Assaf ^b   Schwartz, Betty ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^c BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOOXYGENASE 2; CYTOCHROME C; LACTIC ACID; LEPTIN; MITOCHONDRIAL PROTEIN; PROTEIN BAX;

ADIPOSE TISSUE; ADULT; ARTICLE; CANCER CELL CULTURE; CELL METABOLISM; CELL VIABILITY; COLON CANCER; CONTROLLED STUDY; COX GENE; COX5 GENE; CYTC GENE; EXTRACELLULAR ACIDIFICATION RATE; GENE EXPRESSION; GLYCOLYSIS; HORMONE RELEASE; HUMAN; HUMAN CELL; HUMAN TISSUE; METABOLIC PARAMETERS; MITOCHONDRIAL GENE; MITOCHONDRIAL RESPIRATION; ND1 GENE; NDUFA13 GENE; OBESITY; OXYGEN CONSUMPTION RATE; PROTEIN EXPRESSION; SDHD GENE;

ADIPOSE TISSUE; ADULT; BLOTTING, WESTERN; CELL RESPIRATION; CELL SURVIVAL; COLONIC NEOPLASMS; CULTURE MEDIA, CONDITIONED; GLYCOLYSIS; HUMANS; LEPTIN; MIDDLE AGED; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; OBESITY; OXYGEN CONSUMPTION; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 84884475734     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074843     Document Type: Article

References (49)

1. Braun S, Bitton-Worms K, LeRoith D, (2011) The link between the metabolic syndrome and cancer. Int J Biol Sci 7: 1003-1015. PubMed: 21912508.
2. Pais R, Silaghi H, Silaghi AC, Rusu ML, Dumitrascu DL, (2009) Metabolic syndrome and risk of subsequent colorectal cancer. World J Gastroenterol 15: 5141-5148. doi:10.3748/wjg.15.5141. PubMed: 19891012.
3. Ronti T, Lupattelli G, Mannarino E, (2006) The endocrine function of adipose tissue: an update. Clin Endocrinol (Oxf) 64: 355-365. PubMed: 16584505.
4. Park J, Euhus DM, Scherer PE, (2011) Paracrine and endocrine effects of adipose tissue on cancer development and progression. Endocr Rev 32: 550-570. doi:10.1210/er.2010-0030. PubMed: 21642230.
5. Collins S, (2012) Can having fun protect you from obesity and its cancer risk? Pigment Cell. Melanoma Res 25: 2-3.
6. Anubhuti, Arora S, (2008) Leptin and its metabolic interactions: an update. Diabetes Obes Metab 10: 973-993. doi:10.1111/j.1463-1326.2008.00852.x. PubMed: 18284436.
7. Jaffe T, Schwartz B, (2008) Leptin promotes motility and invasiveness in human colon cancer cells by activating multiple signal-transduction pathways. Int J Cancer 123: 2543-2556. doi:10.1002/ijc.23821. PubMed: 18767036.
8. Bensinger SJ, Christofk HR, (2012) New aspects of the Warburg effect in cancer cell biology. Semin Cell Dev Biol 23: 352-361. doi:10.1016/j.semcdb.2012.02.003. PubMed: 22406683.
9. Robey IF, Lien AD, Welsh SJ, Baggett BK, Gillies RJ, (2005) Hypoxia-inducible factor-1alpha and the glycolytic phenotype in tumors. Neoplasia 7: 324-330. doi:10.1593/neo.04430. PubMed: 15967109.
10. Kovsan J, Blüher M, Tarnovscki T, Klöting N, Kirshtein B, et al. (2011) Altered autophagy in human adipose tissues in obesity. J Clin Endocrinol Metab 96: E268-E277. doi:10.1210/jc.2010-1681. PubMed: 21047928.
11. Kuan SF, Byrd JC, Basbaum CB, Kim YS, (1987) Characterization of quantitative mucin variants from a human colon cancer cell line. Cancer Res 47: 5715-5724. PubMed: 3664476.
12. Bresalier RS, Schwartz B, Kim YS, Duh QY, Kleinman HK, et al. (1995) The laminin alpha 1 chain Ile-Lys-Val-Ala-Val (IKVAV)-containing peptide promotes liver colonization by human colon cancer cells. Cancer Res 55: 2476-2480. PubMed: 7758002.
13. Schwartz B, Bresalier RS, Kim YS, (1992) The role of mucin in colon-cancer metastasis. Int J Cancer 52: 60-65. doi:10.1002/ijc.2910520113. PubMed: 1323540.
14. Collins S, Yehuda-Shnaidman E, Wang H, (2010) Positive and negative control of Ucp1 gene transcription and the role of beta-adrenergic signaling networks. Int J Obes (Lond) 34 (Suppl 1):: S28-S33. doi:10.1038/ijo.2010.180.
15. Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, et al. (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203-218. doi:10.1038/nature06341. PubMed: 17994087.
16. Lavi I, Levinson D, Peri I, Tekoah Y, Hadar Y, et al. (2010) Chemical characterization, antiproliferative and antiadhesive properties of polysaccharides extracted from Pleurotus pulmonarius mycelium and fruiting bodies. Appl Microbiol Biotechnol 85: 1977-1990. doi:10.1007/s00253-009-2296-x. PubMed: 19830415.
17. Gonzalez RR, Cherfils S, Escobar M, Yoo JH, Carino C, et al. (2006) Leptin signaling promotes the growth of mammary tumors and increases the expression of vascular endothelial growth factor (VEGF) and its receptor type two (VEGF-R2). J Biol Chem 281: 26320-26328. doi:10.1074/jbc.M601991200. PubMed: 16825198.
18. Cirillo D, Rachiglio AM, la Montagna R, Giordano A, Normanno N, (2008) Leptin signaling in breast cancer: an overview. J Cell Biochem 105: 956-964. doi:10.1002/jcb.21911. PubMed: 18821585.
19. Bayley JP, Devilee P, (2012) The Warburg effect in 2012. Curr Opin Oncol 24: 62-67. doi:10.1097/CCO.0b013e32834deb9e. PubMed: 22123234.
20. Moreno-Sánchez R, Rodríguez-Enríquez S, Marín-Hernández A, Saavedra E, (2007) Energy metabolism in tumor cells. FEBS J 274: 1393-1418. doi:10.1111/j.1742-4658.2007.05686.x. PubMed: 17302740.
21. Christofk HR, Vander Heiden MG, Harris MH, Ramanathan A, Gerszten RE, et al. (2008) The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452: 230-233. doi:10.1038/nature06734. PubMed: 18337823.
22. Huysentruyt LC, Shelton LM, Seyfried TN, (2010) Influence of methotrexate and cisplatin on tumor progression and survival in the VM mouse model of systemic metastatic cancer. Int J Cancer 126: 65-72. doi:10.1002/ijc.24649. PubMed: 19536778.
23. Wolf A, Agnihotri S, Micallef J, Mukherjee J, Sabha N, et al. (2011) Hexokinase 2 is a key mediator of aerobic glycolysis and promotes tumor growth in human glioblastoma multiforme. J Exp Med 208: 313-326. doi:10.1084/jem.20101470. PubMed: 21242296.
24. Chandra D, Singh KK, (2011) Genetic insights into OXPHOS defect and its role in cancer. Biochim Biophys Acta 1807: 620-625. doi:10.1016/j.bbabio.2010.10.023. PubMed: 21074512.
25. Cook CC, Higuchi M, (2012) The awakening of an advanced malignant cancer: An insult to the mitochondrial genome. Biochim Biophys Acta 1820: 652-662. doi:10.1016/j.bbagen.2011.08.017. PubMed: 21920409.
26. Vander Heiden MG, Cantley LC, Thompson CB, (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324: 1029-1033. doi:10.1126/science.1160809. PubMed: 19460998.
27. Ward PS, Thompson CB, (2012) Signaling in control of cell growth and metabolism. Cold Spring Harb Perspect Biol 4: a006783. doi:10.1101/cshperspect.a006783. PubMed: 22687276.
28. Gross A, McDonnell JM, Korsmeyer SJ, (1999) BCL-2 family members and the mitochondria in apoptosis. Genes Dev 13: 1899-1911. doi:10.1101/gad.13.15.1899. PubMed: 10444588.
29. Schnäbele K, Roser S, Rechkemmer G, Hauner H, Skurk T, (2009) Effects of adipocyte-secreted factors on cell cycle progression in HT29 cells. Eur J Nutr 48: 154-161. doi:10.1007/s00394-009-0775-6. PubMed: 19169726.
30. Gertler A, (2006) Development of leptin antagonists and their potential use in experimental biology and medicine. Trends Endocrinol Metab 17: 372-378. doi:10.1016/j.tem.2006.09.006. PubMed: 17010639.
31. Collins S, Pi J, Yehuda-Shnaidman E, Uncoupling and reactive oxygen species (ROS) - A double-edged sword for β-cell function?. Moderation All Things. Best Practice & Research Clinical Endocrinology & Metabolism.
32. Sung MK, Yeon JY, Park SY, Park JH, Choi MS, (2011) Obesity-induced metabolic stresses in breast and colon cancer. Ann N Y Acad Sci 1229: 61-68. doi:10.1111/j.1749-6632.2011.06094.x. PubMed: 21793840.
33. Smolková K, Plecitá-Hlavatá L, Bellance N, Benard G, Rossignol R, et al. (2011) Waves of gene regulation suppress and then restore oxidative phosphorylation in cancer cells. Int J Biochem Cell Biol 43: 950-968. doi:10.1016/j.biocel.2010.05.003. PubMed: 20460169.
34. Marín-Hernández A, Gallardo-Pérez JC, Rodríguez-Enríquez S, Encalada R, Moreno-Sánchez R, et al. (2011) Modeling cancer glycolysis. Biochim Biophys Acta 1807: 755-767. doi:10.1016/j.bbabio.2010.11.006. PubMed: 21110941.
35. Zu XL, Guppy M, (2004) Cancer metabolism: facts, fantasy, and fiction. Biochem Biophys Res Commun 313: 459-465. doi:10.1016/j.bbrc.2003.11.136. PubMed: 14697210.
36. Bluemlein K, Grüning NM, Feichtinger RG, Lehrach H, Kofler B, et al. (2011) No evidence for a shift in pyruvate kinase PKM1 to PKM2 expression during tumorigenesis. Oncotarget 2: 393-400. PubMed: 21789790.
37. Schmidt H, Siems W, Müller M, Dumdey R, Rapoport SM, (1991) ATP-producing and consuming processes of Ehrlich mouse ascites tumor cells in proliferating and resting phases. Exp Cell Res 194: 122-127. doi:10.1016/0014-4827(91)90140-P. PubMed: 1707821.
38. Friedman JM, (1998) Leptin, leptin receptors, and the control of body weight. Nutr Rev 56: s38-s46; discussion s54-75. PubMed: 9564176.
39. Margetic S, Gazzola C, Pegg GG, Hill RA, (2002) Leptin: a review of its peripheral actions and interactions. Int J Obes Relat Metab Disord 26: 1407-1433. doi:10.1038/sj.ijo.0802142. PubMed: 12439643.
40. Endo H, Hosono K, Uchiyama T, Sakai E, Sugiyama M, et al. (2011) Leptin acts as a growth factor for colorectal tumours at stages subsequent to tumour initiation in murine colon carcinogenesis. Gut 60: 1363-1371. doi:10.1136/gut.2010.235754. PubMed: 21406387.
41. Zheng Q, Dunlap SM, Zhu J, Downs-Kelly E, Rich J, et al. (2011) Leptin deficiency suppresses MMTV-Wnt-1 mammary tumor growth in obese mice and abrogates tumor initiating cell survival. Endocr Relat Cancer 18: 491-503. doi:10.1530/ERC-11-0102. PubMed: 21636700.
42. Park J, Kusminski CM, Chua SC, Scherer PE, (2010) Leptin receptor signaling supports cancer cell metabolism through suppression of mitochondrial respiration in vivo. Am J Pathol 177: 3133-3144. doi:10.2353/ajpath.2010.100595. PubMed: 21056997.
43. Garofalo C, Koda M, Cascio S, Sulkowska M, Kanczuga-Koda L, et al. (2006) Increased expression of leptin and the leptin receptor as a marker of breast cancer progression: possible role of obesity-related stimuli. Clin Cancer Res 12: 1447-1453. doi:10.1158/1078-0432.CCR-05-1913. PubMed: 16533767.
44. Toyoshima Y, Gavrilova O, Yakar S, Jou W, Pack S, et al. (2005) Leptin improves insulin resistance and hyperglycemia in a mouse model of type 2 diabetes. Endocrinology 146: 4024-4035. doi:10.1210/en.2005-0087. PubMed: 15947005.
45. Heather LC, Clarke K, (2011) Metabolism, hypoxia and the diabetic heart. J Mol Cell Cardiol 50: 598-605. doi:10.1016/j.yjmcc.2011.01.007. PubMed: 21262230.
46. Kalakonda S, Nallar SC, Lindner DJ, Hu J, Reddy SP, et al. (2007) Tumor-suppressive activity of the cell death activator GRIM-19 on a constitutively active signal transducer and activator of transcription 3. Cancer Res 67: 6212-6220. doi:10.1158/0008-5472.CAN-07-0031. PubMed: 17616678.
47. Kaaman M, Sparks LM, van Harmelen V, Smith SR, Sjölin E, et al. (2007) Strong association between mitochondrial DNA copy number and lipogenesis in human white adipose tissue. Diabetologia 50: 2526-2533. doi:10.1007/s00125-007-0818-6. PubMed: 17879081.
48. Penta JS, Johnson FM, Wachsman JT, Copeland WC, (2001) Mitochondrial DNA in human malignancy. Mutat Res 488: 119-133. doi:10.1016/S1383-5742(01)00053-9. PubMed: 11344040.
49. Amemori S, Ootani A, Aoki S, Fujise T, Shimoda R, et al. (2007) Adipocytes and preadipocytes promote the proliferation of colon cancer cells in vitro. Am J Physiol Gastrointest Liver Physiol 292: G923-G929. PubMed: 17170030.