3,809
Views
51
CrossRef citations to date
0
Altmetric
Research Paper

Adipose tissue lipolysis and energy metabolism in early cancer cachexia in mice

, , , , &
Pages 886-897 | Received 08 Aug 2014, Accepted 09 Nov 2014, Published online: 22 May 2015

References

  • Tisdale M. Mechanisms of cancer cachexia. Physiol Rev 2009; 89:381-410; PMID:19342610; http://dx.doi.org/10.1152/physrev.00016.2008
  • Tan BH, Fearon KC. Cachexia: prevalence and impact in medicine. Curr Opin Clin Nutr Metab Care 2008; 11:400-7; PMID:18541999; http://dx.doi.org/10.1097/MCO.0b013e328300ecc1
  • Fearon K, Strasser F, Anker SD, Bosaeus I, Bruera E, Fainsinger RL, Jatoi A, Loprinzi C, MacDonald N, Mantovani G, et al. Definition and classification of cancer cachexia: an international consensus. Lancet Oncol 2011; 12:489-95; PMID:21296615; http://dx.doi.org/10.1016/S1470-2045(10)70218-7
  • Zhou X, Wang JL, Lu J, Song Y, Kwak KS, Jiao Q, Rosenfeld R, Chen Q, Boone T, Simonet WS, et al. Reversal of cancer cachexia and muscle wasting by ActRIIB antagonism leads to prolonged survival. Cell 2010; 142:531-43; PMID:20723755; http://dx.doi.org/10.1016/j.cell.2010.07.011
  • Byerley LO, Lee SH, Redmann S, Culberson C, Clemens M, Lively MO. Evidence for a novel serum factor distinct from zinc α-2 glycoprotein that promotes body fat loss early in the development of cachexia. Nutr Cancer 2010; 62:484-94; PMID:20432169; http://dx.doi.org/10.1080/01635580903441220
  • Murphy RA, Wilke MS, Perrine M, Pawlowicz M, Mourtzakis M, Lieffers JR, Maneshgar M, Bruera E, Clandinin MT, Baracos VE, et al. Loss of adipose tissue and plasma phospholipids: relationship to survival in advanced cancer patients. Clin Nutr 2010; 29:482-7; PMID:19959263; http://dx.doi.org/10.1016/j.clnu.2009.11.006
  • Dalal S, Hui D, Bidaut L, Lem K, Del Fabbro E, Crane C, Reyes-Gibby CC, Bedi D, Bruera E. Relationships among body mass index, longitudinal body composition alterations, and survival in patients with locally advanced pancreatic cancer receiving chemoradiation: a pilot study. J Pain Symptom Manage 2012; 44:181-91; PMID:22695045; http://dx.doi.org/10.1016/j.jpainsymman.2011.09.010
  • Di Sebastiano KM, Yang L, Zbuk K, Wong RK, Chow T, Koff D, Moran GR, Mourtzakis M. Accelerated muscle and adipose tissue loss may predict survival in pancreatic cancer patients: the relationship with diabetes and anaemia. Br J Nutr 2013; 109:302-12; PMID:23021109; http://dx.doi.org/10.1017/S0007114512001067
  • Das SK, Eder S, Schauer S, Diwoky C, Temmel H, Guertl B, Gorkiewicz G, Tamilarasan KP, Kumari P, Trauner M, et al. Adipose triglyceride lipase contributes to cancer-associated cachexia. Science 2011; 333:233-8; PMID:21680814; http://dx.doi.org/10.1126/science.1198973
  • Shaw JH, Wolfe RR. Fatty acid and glycerol kinetics in septic patients and in patients with gastrointestinal cancer. The response to glucose infusion and parenteral feeding. Ann Surg 1987; 205:368-76; PMID:3105476; http://dx.doi.org/10.1097/00000658-198704000-00005
  • Klein S, Wolfe RR. Whole-body lipolysis and triglyceride-fatty acid cycling in cachectic patients with esophageal cancer. J Clin Invest 1990; 86:1403-8; PMID:2243120; http://dx.doi.org/10.1172/JCI114854
  • Zuijdgeest-van Leeuwen SD, van den Berg JW, Wattimena JL, van der Gaast A, Swart GR, Wilson JH, Dagnelie PC. Lipolysis and lipid oxidation in weight-losing cancer patients and healthy subjects. Metabolism 2000; 49:931-6; PMID:10910006; http://dx.doi.org/10.1053/meta.2000.6740
  • Agustsson T, Ryden M, Hoffstedt J, van Harmelen V, Dicker A, Laurencikiene J, Isaksson B, Permert J, Arner P. Mechanism of increased lipolysis in cancer cachexia. Cancer Res 2007; 67:5531-7; PMID:17545636; http://dx.doi.org/10.1158/0008-5472.CAN-06-4585
  • Ryden M, Agustsson T, Laurencikiene J, Britton T, Sjolin E, Isaksson B, Permert J, Arner P. Lipolysis-not inflammation, cell death, or lipogenesis-is involved in adipose tissue loss in cancer cachexia. Cancer 2008; 113:1695-704; PMID:18704987; http://dx.doi.org/10.1002/cncr.23802
  • Thompson MP, Koons JE, Tan ET, Grigor MR. Modified lipoprotein lipase activities, rates of lipogenesis, and lipolysis as factors leading to lipid depletion in C57BL mice bearing the preputial gland tumor, ESR-586. Cancer Res 1981; 41:3228-32; PMID:7248977
  • Islam-Ali B, Khan S, Price SA, Tisdale MJ. Modulation of adipocyte G-protein expression in cancer cachexia by a lipid-mobilizing factor (LMF). Br J Cancer 2001; 85:758-63; PMID:11531264; http://dx.doi.org/10.1054/bjoc.2001.1992
  • Korber J, Pricelius S, Heidrich M, Muller MJ. Increased lipid utilization in weight losing and weight stable cancer patients with normal body weight. Eur J Clin Nutr 1999; 53:740-5; PMID:10509772; http://dx.doi.org/10.1038/sj.ejcn.1600843
  • Dahlman I, Mejhert N, Linder K, Agustsson T, Mutch DM, Kulyte A, Isaksson B, Permert J, Petrovic N, Nedergaard J, et al. Adipose tissue pathways involved in weight loss of cancer cachexia. Br J Cancer 2010; 102:1541-8; PMID:20407445; http://dx.doi.org/10.1038/sj.bjc.6605665
  • Arruda AP, Milanski M, Romanatto T, Solon C, Coope A, Alberici LC, Festuccia WT, Hirabara SM, Ropelle E, Curi R, et al. Hypothalamic actions of tumor necrosis factor α provide the thermogenic core for the wastage syndrome in cachexia. Endocrinology 2010; 151:683-94; PMID:19996183; http://dx.doi.org/10.1210/en.2009-0865
  • Tsoli M, Moore M, Burg D, Painter A, Taylor R, Lockie SH, Turner N, Warren A, Cooney G, Oldfield B, et al. Activation of thermogenesis in brown adipose tissue and dysregulated lipid metabolism associated with cancer cachexia in mice. Cancer Res 2012; 72:4372-82; PMID:22719069; http://dx.doi.org/10.1158/0008-5472.CAN-11-3536
  • Jaworski K, Ahmadian M, Duncan RE, Sarkadi-Nagy E, Varady KA, Hellerstein MK, Lee HY, Samuel VT, Shulman GI, Kim KH, et al. AdPLA ablation increases lipolysis and prevents obesity induced by high-fat feeding or leptin deficiency. Nat Med 2009; 15:159-68; PMID:19136964; http://dx.doi.org/10.1038/nm.1904
  • Ahmadian M, Duncan RE, Varady KA, Frasson D, Hellerstein MK, Birkenfeld AL, Samuel VT, Shulman GI, Wang Y, Kang C, et al. Adipose overexpression of desnutrin promotes fatty acid use and attenuates diet-induced obesity. Diabetes 2009; 58:855-66; PMID:19136649; http://dx.doi.org/10.2337/db08-1644
  • Bordicchia M, Liu D, Amri EZ, Ailhaud G, Dessi-Fulgheri P, Zhang C, Takahashi N, Sarzani R, Collins S. Cardiac natriuretic peptides act via p38 MAPK to induce the brown fat thermogenic program in mouse and human adipocytes. J Clin Invest 2012; 122:1022-36; PMID:22307324; http://dx.doi.org/10.1172/JCI59701
  • Yehuda-Shnaidman E, Buehrer B, Pi J, Kumar N, Collins S. Acute stimulation of white adipocyte respiration by PKA-induced lipolysis. Diabetes 2010; 59:2474-83; PMID:20682684; http://dx.doi.org/10.2337/db10-0245
  • Kazantzis M, Seelaender MC. Cancer cachexia modifies the zonal distribution of lipid metabolism-related proteins in rat liver. Cell Tissue Res 2005; 321:419-27; PMID:16021474; http://dx.doi.org/10.1007/s00441-005-1138-0
  • Silverio R, Laviano A, Rossi Fanelli F, Seelaender M. L-Carnitine induces recovery of liver lipid metabolism in cancer cachexia. Amino Acids 2012; 42:1783-92; PMID:21465256; http://dx.doi.org/10.1007/s00726-011-0898-y
  • Siddiqui RA, Williams JF. The regulation of fatty acid and branched-chain amino acid oxidation in cancer cachectic rats: a proposed role for a cytokine, eicosanoid, and hormone trilogy. Biochem Med Metab Biol 1989; 42:71-86; PMID:2775564; http://dx.doi.org/10.1016/0885-4505(89)90043-1
  • Julienne CM, Dumas JF, Goupille C, Pinault M, Berri C, Collin A, Tesseraud S, Couet C, Servais S. Cancer cachexia is associated with a decrease in skeletal muscle mitochondrial oxidative capacities without alteration of ATP production efficiency. J Cachexia Sarcopenia Muscle 2012; 3:265-75; PMID:22648737; http://dx.doi.org/10.1007/s13539-012-0071-9
  • Weber MA, Krakowski-Roosen H, Schroder L, Kinscherf R, Krix M, Kopp-Schneider A, Essig M, Bachert P, Kauczor HU, Hildebrandt W. Morphology, metabolism, microcirculation, and strength of skeletal muscles in cancer-related cachexia. Acta Oncol 2009; 48:116-24; PMID:18607877; http://dx.doi.org/10.1080/02841860802130001
  • Seelaender MC, Nascimento CM, Curi R, Williams JF. Studies on the lipid metabolism of Walker 256 tumour-bearing rats during the development of cancer cachexia. Biochem Mol Biol Int 1996; 39:1037-47; PMID:8866022
  • Asp ML, Tian M, Kliewer KL, Belury MA. Rosiglitazone delayed weight loss and anorexia while attenuating adipose depletion in mice with cancer cachexia. Cancer Biol Ther 2011; 12:957-65; PMID:22104958; http://dx.doi.org/10.4161/cbt.12.11.18134
  • Tian M, Kliewer KL, Asp ML, Stout MB, Belury MA. c9t11-Conjugated linoleic acid-rich oil fails to attenuate wasting in colon-26 tumor-induced late-stage cancer cachexia in male CD2F1 mice. Mol Nutr Food Res 2011; 55:268-77; PMID:20827675; http://dx.doi.org/10.1002/mnfr.201000176
  • Bing C. Lipid mobilization in cachexia: mechanisms and mediators. Curr Opin Support Palliat Care 2011; 5:356-60; PMID:21934502; http://dx.doi.org/10.1097/SPC.0b013e32834bde0e
  • Festuccia WT, Guerra-Sa R, Kawashita NH, Garofalo MA, Evangelista EA, Rodrigues V, Kettelhut IC, Migliorini RH. Expression of glycerokinase in brown adipose tissue is stimulated by the sympathetic nervous system. Am J Physiol Regul Integr Comp Physiol 2003; 284:R1536-41; PMID:12736183
  • Bing C, Brown M, King P, Collins P, Tisdale MJ, Williams G. Increased gene expression of brown fat uncoupling protein (UCP)1 and skeletal muscle UCP2 and UCP3 in MAC16-induced cancer cachexia. Cancer Res 2000; 60:2405-10; PMID:10811117
  • Wu P, Inskeep K, Bowker-Kinley MM, Popov KM, Harris RA. Mechanism responsible for inactivation of skeletal muscle pyruvate dehydrogenase complex in starvation and diabetes. Diabetes 1999; 48:1593-9; PMID:10426378; http://dx.doi.org/10.2337/diabetes.48.8.1593
  • Bing C, Russell S, Becket E, Pope M, Tisdale MJ, Trayhurn P, Jenkins JR. Adipose atrophy in cancer cachexia: morphologic and molecular analysis of adipose tissue in tumour-bearing mice. Br J Cancer 2006; 95:1028-37; PMID:17047651; http://dx.doi.org/10.1038/sj.bjc.6603360
  • Tsoli M, Schweiger M, Vanniasinghe AS, Painter A, Zechner R, Clarke S, Robertson G. Depletion of white adipose tissue in cancer cachexia syndrome is associated with inflammatory signaling and disrupted circadian regulation. PLoS One 2014; 9:e92966; PMID:24667661; http://dx.doi.org/10.1371/journal.pone.0092966
  • Stephens NA, Skipworth RJ, Macdonald AJ, Greig CA, Ross JA, Fearon KC. Intramyocellular lipid droplets increase with progression of cachexia in cancer patients. J Cachexia Sarcopenia Muscle 2011; 2:111-7; PMID:21766057; http://dx.doi.org/10.1007/s13539-011-0030-x
  • Blum D, Stene GB, Solheim TS, Fayers P, Hjermstad MJ, Baracos VE, Fearon K, Strasser F, Kaasa S. Validation of the consensus-definition for cancer cachexia and evaluation of a classification model-a study based on data from an international multicentre project (EPCRC-CSA). Ann Oncol 2014; 25:1635-42; PMID:24562443; http://dx.doi.org/10.1093/annonc/mdu086
  • Kir S, White JP, Kleiner S, Kazak L, Cohen P, Baracos VE, Spiegelman BM. Tumour-derived PTH-related protein triggers adipose tissue browning and cancer cachexia. Nature 2014; 513:100-4; PMID:25043053; http://dx.doi.org/10.1038/nature13528
  • Maclean PS, Bergouignan A, Cornier MA, Jackman MR. Biology's response to dieting: the impetus for weight regain. Am J Physiol Regul Integr Comp Physiol 2011; 301:R581-600; PMID:21677272; http://dx.doi.org/10.1152/ajpregu.00755.2010
  • Hambly C, Simpson CA, McIntosh S, Duncan JS, Dalgleish GD, Speakman JR. Calorie-restricted mice that gorge show less ability to compensate for reduced energy intake. Physiol Behav 2007; 92:985-92; PMID:17706730; http://dx.doi.org/10.1016/j.physbeh.2007.07.005
  • Hambly C, Speakman JR. Contribution of different mechanisms to compensation for energy restriction in the mouse. Obes Res 2005; 13:1548-57; PMID:16222057; http://dx.doi.org/10.1038/oby.2005.190
  • Li X, Cope MB, Johnson MS, Smith DL, Jr., Nagy TR. Mild calorie restriction induces fat accumulation in female C57BL/6J mice. Obesity (Silver Spring) 2010; 18:456-62; PMID:19798071; http://dx.doi.org/10.1038/oby.2009.312
  • Goldsmith R, Joanisse DR, Gallagher D, Pavlovich K, Shamoon E, Leibel RL, Rosenbaum M. Effects of experimental weight perturbation on skeletal muscle work efficiency, fuel utilization, and biochemistry in human subjects. Am J Physiol Regul Integr Comp Physiol 2010; 298:R79-88; PMID:19889869; http://dx.doi.org/10.1152/ajpregu.00053.2009
  • Rosenbaum M, Vandenborne K, Goldsmith R, Simoneau JA, Heymsfield S, Joanisse DR, Hirsch J, Murphy E, Matthews D, Segal KR, et al. Effects of experimental weight perturbation on skeletal muscle work efficiency in human subjects. Am J Physiol Regul Integr Comp Physiol 2003; 285:R183-92; PMID:12609816
  • Hyltander A, Daneryd P, Sandstrom R, Korner U, Lundholm K. Beta-adrenoceptor activity and resting energy metabolism in weight losing cancer patients. Eur J Cancer 2000; 36:330-4; PMID:10708933; http://dx.doi.org/10.1016/S0959-8049(99)00273-7
  • Falconer JS, Fearon KC, Plester CE, Ross JA, Carter DC. Cytokines, the acute-phase response, and resting energy expenditure in cachectic patients with pancreatic cancer. Ann Surg 1994; 219:325-31; PMID:7512810; http://dx.doi.org/10.1097/00000658-199404000-00001
  • Fearon KC, Glass DJ, Guttridge DC. Cancer cachexia: mediators, signaling, and metabolic pathways. Cell Metab 2012; 16:153-66; PMID:22795476; http://dx.doi.org/10.1016/j.cmet.2012.06.011
  • Cray C, Zaias J, Altman NH. Acute phase response in animals: a review. Comp Med 2009; 59:517-26; PMID:20034426
  • Stephens NA, Skipworth RJ, Fearon KC. Cachexia, survival and the acute phase response. Curr Opin Support Palliat Care 2008; 2:267-74; PMID:19060563; http://dx.doi.org/10.1097/SPC.0b013e3283186be2
  • Falconer JS, Fearon KC, Ross JA, Elton R, Wigmore SJ, Garden OJ, Carter DC. Acute-phase protein response and survival duration of patients with pancreatic cancer. Cancer 1995; 75:2077-82; PMID:7535184; http://dx.doi.org/10.1002/1097-0142(19950415)75:8%3c2077::AID-CNCR2820750808%3e3.0.CO;2-9
  • Wigmore SJ, Falconer JS, Plester CE, Ross JA, Maingay JP, Carter DC, Fearon KC. Ibuprofen reduces energy expenditure and acute-phase protein production compared with placebo in pancreatic cancer patients. Br J Cancer 1995; 72:185-8; PMID:7541236; http://dx.doi.org/10.1038/bjc.1995.300
  • Bartelt A, Heeren J. Adipose tissue browning and metabolic health. Nat Rev Endocrinol 2014; 10:24-36; PMID:24146030; http://dx.doi.org/10.1038/nrendo.2013.204
  • Petruzzelli M, Schweiger M, Schreiber R, Campos-Olivas R, Tsoli M, Allen J, Swarbrick M, Rose-John S, Rincon M, Robertson G, et al. A Switch from White to Brown Fat Increases Energy Expenditure in Cancer-Associated Cachexia. Cell Metab 2014; 20:433-47; PMID:25043816; http://dx.doi.org/10.1016/j.cmet.2014.06.011
  • Klein S, Young VR, Blackburn GL, Bistrian BR, Wolfe RR. The impact of body composition on the regulation of lipolysis during short-term fasting. J Am Coll Nutr 1988; 7:77-84; PMID:3343478; http://dx.doi.org/10.1080/07315724.1988.10720223
  • Mittendorfer B, Magkos F, Fabbrini E, Mohammed BS, Klein S. Relationship between body fat mass and free fatty acid kinetics in men and women. Obesity (Silver Spring) 2009; 17:1872-7; PMID:19629053; http://dx.doi.org/10.1038/oby.2009.224
  • Seelaender MC, Curi R, Colquhoun A, Williams JF, Zammitt VA. Carnitine palmitoyltransferase II activity is decreased in liver mitochondria of cachectic rats bearing the Walker 256 carcinosarcoma: effect of indomethacin treatment. Biochem Mol Biol Int 1998; 44:185-93; PMID:9503162
  • Nachiappan V, Curtiss D, Corkey BE, Kilpatrick L. Cytokines inhibit fatty acid oxidation in isolated rat hepatocytes: synergy among TNF, IL-6, and IL-1. Shock 1994; 1:123-9; PMID:7749930; http://dx.doi.org/10.1097/00024382-199402000-00007
  • Rebeca R, Bracht L, Noleto GR, Martinez GR, Cadena SM, Carnieri EG, Rocha ME, de Oliveira MB. Production of cachexia mediators by Walker 256 cells from ascitic tumors. Cell Biochem Funct 2008; 26:731-8; PMID:18646274; http://dx.doi.org/10.1002/cbf.1497
  • Yasumoto K, Mukaida N, Harada A, Kuno K, Akiyama M, Nakashima E, Fujioka N, Mai M, Kasahara T, Fujimoto-Ouchi K, et al. Molecular analysis of the cytokine network involved in cachexia in colon 26 adenocarcinoma-bearing mice. Cancer Res 1995; 55:921-7; PMID:7850809
  • Tanaka Y, Eda H, Tanaka T, Udagawa T, Ishikawa T, Horii I, Ishitsuka H, Kataoka T, Taguchi T. Experimental cancer cachexia induced by transplantable colon 26 adenocarcinoma in mice. Cancer Res 1990; 50:2290-5; PMID:2317817
  • Talbert EE, Metzger GA, He WA, Guttridge DC. Modeling human cancer cachexia in colon 26 tumor-bearing adult mice. J Cachexia Sarcopenia Muscle 2014; PMID:24668658
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25:402-8; PMID:11846609; http://dx.doi.org/10.1006/meth.2001.1262
  • Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957; 226:497-509; PMID:13428781
  • McLean J, Tobin G. Animal and Human Calorimetry. Cambridge UK: Cambridge University Press, 1987
  • Tschop MH, Speakman JR, Arch JR, Auwerx J, Bruning JC, Chan L, Eckel RH, Farese RV, Jr., Galgani JE, Hambly C, et al. A guide to analysis of mouse energy metabolism. Nat Methods 2012; 9:57-63; PMID:22205519; http://dx.doi.org/10.1038/nmeth.1806

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.