The high costs of low-grade inflammation: Persistent fatigue as a consequence of reduced cellular-energy availability and non-adaptive energy expenditure

Frontiers in Behavioral Neuroscience

Volumn 12, Issue , 2018, Pages

  Lacourt, Tamara E ^a   Vichaya, Elisabeth G ^a   Chiu, Gabriel S ^a   Dantzer, Robert ^a   Heijnen, Cobi J ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Cancer related fatigue; Chronic fatigue syndrome; Cytokines; Effort; Energy balance; Metabolism; Motivation

Indexed keywords

ADENOSINE TRIPHOSPHATE; APOLIPOPROTEIN A1; APOLIPOPROTEIN E; REACTIVE OXYGEN METABOLITE; UBIDECARENONE;

AEROBIC GLYCOLYSIS; CELL ENERGY; CHRONIC FATIGUE SYNDROME; CIRCADIAN RHYTHM; DIET SUPPLEMENTATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGY BALANCE; ENERGY EXPENDITURE; ENERGY METABOLISM; HUMAN; INFLAMMATION; INSULIN SENSITIVITY; LIPID METABOLISM; METABOLOMICS; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PROTEIN METABOLISM; REVIEW; SLEEP DISORDER; SLEEP QUALITY;

EID: 85046680745     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2018.00078     Document Type: Review

References (143)

1. Abrahams, H. J., Gielissen, M. F., Schmits, I. C., Verhagen, C. A., Rovers, M. M., and Knoop, H. (2016). Risk factors, prevalence, and course of severe fatigue after breast cancer treatment: a meta-analysis involving 12 327 breast cancer survivors. Ann. Oncol. 27, 965-974. doi: 10.1093/annonc/mdw099
2. Afari, N., and Buchwald, D. (2003). Chronic fatigue syndrome: a review. Am. J. Psychiatry 160, 221-236. doi: 10.1176/appi.ajp.160.2.221
3. Ancoli-Israel, S., Liu, L., Rissling, M., Natarajan, L., Neikrug, A. B., Palmer, B. W., et al. (2014). Sleep, fatigue, depression, and circadian activity rhythms in women with breast cancer before and after treatment: a 1-year longitudinal study. Support. Care Cancer 22, 2535-2545. doi: 10.1007/s00520-014-2204-5
4. Ancoli-Israel, S., Rissling, M., Neikrug, A., Trofimenko, V., Natarajan, L., Parker, B. A., et al. (2012). Light treatment prevents fatigue in women undergoing chemotherapy for breast cancer. Support. Care Cancer 20, 1211-1219. doi: 10.1007/s00520-011-1203-z
5. Anderson, S. T., O’Callaghan, E. K., Commins, S., and Coogan, A. N. (2015). Does prior sepsis alter subsequent circadian and sickness behaviour response to lipopolysaccharide treatment in mice? J. Neural Transm. 122(Suppl. 1), S63-S73. doi: 10.1007/s00702-013-1124-8
6. Asanuma, M., Miyazaki, I., and Ogawa, N. (2003). Dopamine- or L-DOPA-induced neurotoxicity: the role of dopamine quinone formation and tyrosinase in a model of Parkinson’s disease. Neurotox. Res. 5, 165-176. doi: 10.1007/BF03033137
7. Asghar, A., and Sheikh, N. (2017). Role of immune cells in obesity induced low grade inflammation and insulin resistance. Cell. Immunol. 315, 18-26. doi: 10.1016/j.cellimm.2017.03.001
8. Bergamini, C., Moruzzi, N., Sblendido, A., Lenaz, G., and Fato, R. (2012). A water soluble CoQ(10) formulation improves intracellular distribution and promotes mitochondrial respiration in cultured cells. PLoS ONE 7:e33712. doi: 10.1371/journal.pone.0033712
9. Blázquez, E., Velázquez, E., Hurtado-Carneiro, V., and Ruiz-Albusac, J. M. (2014). Insulin in the brain: its pathophysiological implications for States related with central insulin resistance, type 2 diabetes and Alzheimer’s disease. Front. Endocrinol. 5:161. doi: 10.3389/fendo.2014.00161
10. Blesa, J., Trigo-Damas, I., Quiroga-Varela, A., and Jackson-Lewis, V. R. (2015). Oxidative stress and Parkinson’s disease. Front. Neuroanat. 9:91. doi: 10.3389/fnana.2015.00091
11. Bonsall, D. R., Kim, H., Tocci, C., Ndiaye, A., Petronzio, A., McKay-Corkum, G., et al. (2015). Suppression of locomotor activity in female C57Bl/6J mice treated with interleukin-1beta: investigating a method for the study of fatigue in laboratory animals. PLoS ONE10:e0140678. doi: 10.1371/journal.pone.0140678
12. Boomsma, M. F., Garssen, B., Slot, E., Berbee, M., Berkhof, J., Meezenbroek Ede, J., et al. (2010). Breast cancer surgery-induced immunomodulation. J. Surg. Oncol. 102, 640-648. doi: 10.1002/jso.21662
13. Bower, J. E. (2007). Cancer-related fatigue: links with inflammation in cancer patients and survivors. Brain Behav. Immun. 21, 863-871. doi: 10.1016/j.bbi.2007.03.013
14. Bower, J. E. (2014). Cancer-related fatigue-mechanisms, risk factors, and treatments. Nat. Rev. Clin. Oncol. 11, 597-609. doi: 10.1038/nrclinonc.2014.127
15. Bower, J. E., and Lamkin, D. M. (2013). Inflammation and cancer-related fatigue: mechanisms, contributing factors, and treatment implications. Brain Behav. Immun. 30(Suppl.), S48-S57. doi: 10.1016/j.bbi.2012.06.011
16. Brown, A. E., Jones, D. E., Walker, M., and Newton, J. L. (2015). Abnormalities of AMPK activation and glucose uptake in cultured skeletal muscle cells from individuals with chronic fatigue syndrome. PLoS ONE 10:e0122982. doi: 10.1371/journal.pone.0122982
17. Brown, M., Khorana, N., and Jason, L. A. (2011). The role of changes in activity as a function of perceived available and expended energy in nonpharmacological treatment outcomes for ME/CFS. J. Clin. Psychol. 67, 253-260. doi: 10.1002/jclp.20744
18. Caron, A. M., and Stephenson, R. (2010). Energy expenditure is affected by rate of accumulation of sleep deficit in rats. Sleep 33, 1226-1235. doi: 10.1093/sleep/33.9.1226
19. Castro-Marrero, J., Cordero, M. D., Segundo, M. J., Sáez-Francàs, N., Calvo, N., Román-Malo, L., et al. (2014). Does oral coenzyme Q10 plus NADH supplementation improve fatigue and biochemical parameters in chronic fatigue syndrome? Antioxid. Redox Signal. 22, 679-685. doi: 10.1089/ars.2014.6181
20. Chiu, G. S., Maj, M. A., Rizvi, S., Dantzer, R., Vichaya, E. G., Laumet, G., et al. (2016). Pifithrin-micro prevents cisplatin-induced chemobrain by preserving neuronal mitochondrial function. Cancer Res. 77, 742-752. doi: 10.1158/0008-5472.CAN-16-1817
21. Choy, E. H. S., and Calabrese, L. H. (2017). Neuroendocrine and neurophysiological effects of interleukin 6 in rheumatoid arthritis. Rheumatology. doi: 10.1093/rheumatology/kex391. [Epub ahead of print].
22. Ciregia, F., Kollipara, L., Giusti, L., Zahedi, R. P., Giacomelli, C., Mazzoni, M. R., et al. (2016). Bottom-up proteomics suggests anassociationbetweendifferential expression of mitochondrial proteins and chronic fatigue syndrome. Transl. Psychiatry 6:e904. doi: 10.1038/tp.2016.184
23. Dantzer, R., Heijnen, C. J., Kavelaars, A., Laye, S., and Capuron, L. (2014). The neuroimmune basis of fatigue. Trends Neurosci. 37, 39-46. doi: 10.1016/j.tins.2013.10.003
24. Davis, J. M., Murphy, E. A., Carmichael, M. D., and Davis, B. (2009). Quercetin increases brain and muscle mitochondrial biogenesis and exercise tolerance. Am. J. Physiol. Regul. Integr. Comp. Physiol. 296, R1071-R1077. doi: 10.1152/ajpregu.90925.2008
25. de Pablos, R. M., Herrera, A. J., Espinosa-Oliva, A. M., Sarmiento, M., Muñoz, M. F., Machado, A., et al. (2014). Chronic stress enhances microglia activation and exacerbates death of nigral dopaminergic neurons under conditions of inflammation. J. Neuroinflammation 11:34. doi: 10.1186/1742-2094-11-34
26. Depner, C. M., Stothard, E. R., and Wright, K. P. Jr. (2014). Metabolic consequences of sleep and circadian disorders. Curr. Diab. Rep. 14:507. doi: 10.1007/s11892-014-0507-z
27. Draper, A., Koch, R. M., van der Meer, J. W., Apps, M., Pickkers, P., Husain, M., et al. (2017). Effort but not reward sensitivity is altered by acute sickness induced by experimental endotoxemia in humans. Neuropsychopharmacology 43, 1107-1118. doi: 10.1038/npp.2017.231
28. Drivsholm, T., de Fine Olivarius, N., Nielsen, A. B. S., and Siersma, V. (2005). Symptoms, signs and complications innewly diagnosed type 2 diabetic patients, and their relationship to glycaemia, blood pressure and weight. Diabetologia 48, 210-214. doi: 10.1007/s00125-004-1625-y
29. Dumas, J. F., Goupille, C., Julienne, C. M., Pinault, M., Chevalier, S., Bougnoux, P., et al. (2011). Efficiency of oxidative phosphorylation in liver mitochondria is decreased in a rat model of peritoneal carcinosis. J. Hepatol. 54, 320-327. doi: 10.1016/j.jhep.2010.08.012
30. Engler, H., Benson, S., Wegner, A., Spreitzer, I., Schedlowski, M., andElsenbruch, S. (2016). Men and women differ in inflammatory and neuroendocrine responses to endotoxin but not in the severity of sickness symptoms. Brain Behav. Immun. 52, 18-26. doi: 10.1016/j.bbi.2015.08.013
31. Felger, J. C., Mun, J., Kimmel, H. L., Nye, J. A., Drake, D. F., Hernandez, C. R., et al. (2013). Chronic interferon-alpha decreases dopamine 2 receptor binding and striatal dopamine release in association with anhedonia-like behavior in nonhuman primates. Neuropsychopharmacology 38, 2179-2187. doi: 10.1038/npp.2013.115
32. Filler, K., Lyon, D., Bennett, J., McCain, N., Elswick, R., Lukkahatai, N., et al. (2014). Association of mitochondrial dysfunction and fatigue: a review of the literature. BBA Clin. 1, 12-23. doi: 10.1016/j.bbacli.2014.04.001
33. Filler, K., Lyon, D., McCain, N., Bennett, J. Jr., Fernández-Martínez, J. L., deAndrés-Galiana, E. J., et al. (2016). Relationship of mitochondrial enzymes to fatigue intensity in men with prostate cancer receiving external beamradiation therapy. Biol. Res. Nurs. 18, 274-280. doi: 10.1177/1099800415617848
34. Fitzpatrick, F. A., and Wheeler, R. (2003). The immunopharmacology of paclitaxel (Taxol R®), docetaxel (Taxotere R®), and related agents. Int. Immunopharmacol. 3, 1699-1714. doi: 10.1016/j.intimp.2003.08.007
35. Fluge, Ø, Mella, O., Bruland, O., Risa, K., Dyrstad, S. E., Alme, K., et al. (2016). Metabolic profiling indicates impaired pyruvate dehydrogenase function in myalgic encephalopathy/chronic fatigue syndrome. JCI Insight 1:e89376. doi: 10.1172/jci.insight.89376
36. Fu, X., Ji, R., and Dam, J. (2010). Antifatigue effect of coenzyme Q10 in mice. J. Med. Food 13, 211-215. doi: 10.1089/jmf.2009.0049
37. Fukuda, K., Straus, S. E., Hickie, I., Sharpe, M. C., Dobbins, J. G., and Komaroff, A. (1994). The chronic fatigue syndrome: a comprehensive approach to its definition and study. international chronic fatigue syndrome study group. Ann. Intern. Med. 121, 953-959. doi: 10.7326/0003-4819-121-12-199412150-00009
38. Genova, M. L., Pich, M. M., Biondi, A., Bernacchia, A., Falasca, A., Bovina, C., et al. (2003). Mitochondrial production of oxygen radical species and the role of Coenzyme Q as an antioxidant. Exp. Biol. Med. 228, 506-513. doi: 10.1177/15353702-0322805-14
39. Gilliam, L. A., Lark, D. S., Reese, L. R., Torres, M. J., Ryan, T. E., Lin, C. T., et al. (2016). Targeted overexpression of mitochondrial catalase protects against cancer chemotherapy-induced skeletal muscle dysfunction. Am. J. Physiol. Endocrinol. Metab. 311, E293-E301. doi: 10.1152/ajpendo.00540.2015
40. Goedendorp, M. M., Gielissen, M. F., Verhagen, C. A., and Bleijenberg, G. (2013). Development of fatigue in cancer survivors: a prospective follow-up study from diagnosis into the year after treatment. J. Pain Symptom Manage. 45, 213-222. doi: 10.1016/j.jpainsymman.2012.02.009
41. Gorman, G. S., Elson, J. L., Newman, J., Payne, B., McFarland, R., Newton, J. L., et al. (2015). Perceived fatigue is highly prevalent and debilitating in patients with mitochondrial disease. Neuromuscul. Disord. 25, 563-566. doi: 10.1016/j.nmd.2015.03.001
42. Gouspillou, G., Scheede-Bergdahl, C., Spendiff, S., Vuda, M., Meehan, B., Mlynarski, H., et al. (2015). Anthracycline-containing chemotherapy causes long-term impairment of mitochondrial respiration and increased reactive oxygen species release in skeletal muscle. Sci. Rep. 5:8717. doi: 10.1038/srep08717
43. Guilleminault, C., Poyares, D., Rosa, A., Kirisoglu, C., Almeida, T., and Lopes, M. C. (2006). Chronic fatigue, unrefreshing sleepandnocturnal polysomnography. Sleep Med. 7, 513-520. doi: 10.1016/j.sleep.2006.03.016
44. Hall, C. N., Klein-Flugge, M. C., Howarth, C., and Attwell, D. (2012). Oxidative phosphorylation, not glycolysis, powers presynaptic and postsynaptic mechanisms underlying brain information processing. J. Neurosci. 32, 8940-8951. doi: 10.1523/JNEUROSCI.0026-12.2012
45. Hamilos, D. L., Nutter, D., Gershtenson, J., Ikle, D., Hamilos, S. S., Redmond, D. P., et al. (2001). Circadian rhythm of core body temperature in subjects with chronic fatigue syndrome. Clin. Physiol. 21, 184-195. doi: 10.1046/j.1365-2281.2001.00321.x
46. Haspel, J. A., Chettimada, S., Shaik, R. S., Chu, J. H., Raby, B. A., Cernadas, M., et al. (2014). Circadian rhythmreprogramming during lung inflammation. Nat. Commun. 5:4753. doi: 10.1038/ncomms5753
47. Hornig, M., Gottschalk, G., Peterson, D. L., Knox, K. K., Schultz, A. F., Eddy, M. L., et al. (2016). Cytokine network analysis of cerebrospinal fluid in myalgic encephalomyelitis/chronic fatigue syndrome. Mol. Psychiatry 21, 261-269. doi: 10.1038/mp.2015.29
48. Hsiao, C. P., Wang, D., Kaushal, A., Chen, M. K., andSaligan, L. (2014). Differential expression of genes related to mitochondrial biogenesis and bioenergetics in fatigued prostate cancer men receiving external beamradiation therapy. J. Pain SymptomManage. 48, 1080-1090. doi: 10.1016/j.jpainsymman.2014.03.010
49. Hsiao, C. P., Wang, D., Kaushal, A., and Saligan, L. (2013). Mitochondria-related gene expression changes are associated with fatigue in patients with nonmetastatic prostate cancer receiving external beam radiation therapy. Cancer Nurs. 36, 189-197. doi: 10.1097/NCC.0b013e318263f514
50. Huang, C. T., Chiang, R. P., Chen, C. L., and Tsai, Y. J. (2014). Sleep deprivation aggravates median nerve injury-induced neuropathic pain and enhances microglial activation by suppressing melatonin secretion. Sleep 37, 1513-1523. doi: 10.5665/sleep.4002
51. Induruwa, I., Constantinescu, C. S., and Gran, B. (2012). Fatigue in multiple sclerosis — a brief review. J. Neurol. Sci. 323, 9-15. doi: 10.1016/j.jns.2012.08.007
52. Iwase, S., Kawaguchi, T., Yotsumoto, D., Doi, T., Miyara, K., Odagiri, H., et al. (2016). Efficacy and safety of an amino acid jelly containing coenzyme Q10 and L-carnitine in controlling fatigue in breast cancer patients receiving chemotherapy: a multi-institutional, randomized, exploratory trial (JORTC-CAM01). Support. Care Cancer 24, 637-646. doi: 10.1007/s00520-015-2824-4
53. Jason, L., Benton, M., Torres-Harding, S., and Muldowney, K. (2009). The impact of energy modulation on physical functioning and fatigue severity among patients with ME/CFS. Patient Educ. Couns. 77, 237-241. doi: 10.1016/j.pec.2009.02.015
54. Jiménez-Santos, M. A., Juárez-Rojop, I. E., Tovilla-Zárate, C. A., Espinosa-García, M. T., Juárez-Oropeza, M. A., Ramón-Frías, T., et al. (2014). Coenzyme Q(10) supplementation improves metabolic parameters, liver function and mitochondrial respiration in rats with high doses of atorvastatin and a cholesterol-rich diet. Lipids Health Dis. 13:22. doi: 10.1186/1476-511X-13-22
55. Johnson, J. A., Garland, S. N., Carlson, L. E., Savard, J., Simpson, J. S. A., Ancoli-Israel, S., et al. (2017). Bright light therapy improves cancer-related fatigue in cancer survivors: a randomized controlled trial. J. Cancer Surviv. 12, 206-215. doi: 10.1007/s11764-017-0659-3
56. Karshikoff, B., Sundelin, T., and Lasselin, J. (2017). Role of inflammation in human fatigue: relevance of multidimensional assessments and potential neuronal mechanisms. Front. Immunol. 8:21. doi: 10.3389/fimmu.2017. 00021
57. Kelly, B., and O’Neill, L. A. (2015). Metabolic reprogramming in macrophages and dentritic cells in innate immunity. Cell Res. 25, 771-784. doi: 10.1038/cr.2015.68
58. Keyser, R. E. (2010). Peripheral fatigue: high-energy phosphates and hydrogen ions. PMR 2, 347-358. doi: 10.1016/j.pmrj.2010.04.009
59. Kim, J. Y., Lee, Y. D., Kim, B. J., Kim, S. P., Kim, D. H., Jo, K. J., et al. (2012). Melatonin improves inflammatory cytokine profiles in lung inflammation associated with sleep deprivation. Mol. Med. Rep. 5, 1281-1284. doi: 10.3892/mmr.2012.814
60. Knook, L., Kavelaars, A., Sinnema, G., Kuis, W., and Heijnen, C. J. (2000). High nocturnal melatonin in adolescents with chronic fatigue syndrome. J. Clin. Endocrinol. Metab. 85, 3690-3692. doi: 10.1210/jc.85.10.3690
61. Kominsky, D. J., Campbell, E. L., and Colgan, S. P. (2010). Metabolic shifts in immunity and inflammation. J. Immunol. 184, 4062-4068. doi: 10.4049/jimmunol.0903002
62. Krzyszton, C. P., Sparkman, N. L., Grant, R. W., Buchanan, J. B., Broussard, S. R., Woods, J., et al. (2008). Exacerbated fatigue and motor deficits in interleukin-10-deficient mice after peripheral immune stimulation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R1109-R1114. doi: 10.1152/ajpregu.90302.2008
63. Lacourt, T. E., and Heijnen, C. J. (2017). Mechanisms of neurotoxic symptoms as a result of breast cancer and its treatment: considerations on the contribution of stress, inflammation, and cellular bioenergetics. Curr. Breast Cancer Rep. 9, 70-81. doi: 10.1007/s12609-017-0245-8
64. Larson, S. J., Romanoff, R. L., Dunn, A. J., and Glowa, J. R. (2002). Effects of interleukin-1beta on food-maintained behavior in the mouse. Brain Behav. Immun. 16, 398-410. doi: 10.1006/brbi.2001.0634
65. Lasselin, J., Layé, S., Dexpert, S., Aubert, A., Gonzalez, C., Gin, H., et al. (2012). Fatigue symptoms relate to systemic inflammation in patients with type 2 diabetes. Brain Behav. Immun. 26, 1211-1219. doi: 10.1016/j.bbi.2012.03.003
66. Lasselin, J., Treadway, M. T., Lacourt, T. E., Soop, A., Olsson, M. J., Karshikoff, B., et al. (2017). Lipopolysaccharide alters motivated behavior in a monetary reward task: a randomized trial. Neuropsychopharmacology 42, 801-810. doi: 10.1038/npp.2016.191
67. Le Floc’h, N., Melchior, D., and Obled, C. (2004). Modifications of protein and amino acid metabolism during inflammation and immune system activation. Livest. Sci. 87, 37-45. doi: 10.1016/j.livprodsci.2003.09.005
68. Leproult, R., Holmbäck, U., and Van Cauter, E. (2014). Circadian misalignment augments markers of insulin resistance and inflammation, independently of sleep loss. Diabetes 63, 1860-1869. doi: 10.2337/db13-1546
69. Lesser, G. J., Case, D., Stark, N., Williford, S., Giguere, J., Garino, L. A., et al. (2013). Arandomized, double-blind, placebo-controlled study of oral coenzyme Q10 to relieve self-reported treatment-related fatigue in newly diagnosed patients with breast cancer. J. Support. Oncol. 11, 31-42. doi: 10.1016/j.suponc.2012.03.003
70. Liu, L., Mills, P. J., Rissling, M., Fiorentino, L., Natarajan, L., Dimsdale, J. E., et al. (2012a). Fatigue and sleep quality are associated with changes in inflammatory markers in breast cancer patients undergoing chemotherapy. Brain Behav. Immun. 26, 706-713. doi: 10.1016/j.bbi.2012.02.001
71. Liu, L., Rissling, M., Natarajan, L., Fiorentino, L., Mills, P. J., Dimsdale, J. E., et al. (2012b). The longitudinal relationship between fatigue and sleep in breast cancer patients undergoing chemotherapy. Sleep 35, 237-245. doi: 10.5665/sleep.1630
72. Liu, T. F., Vachharajani, V. T., Yoza, B. K., and McCall, C. E. (2012c). NAD+ dependent Sirtuin 1 and 6 proteins coordinate a switch from glucose to fatty acid oxidation during the acute inflammatory response. J. Biol. Chem. 287, 25758-25769. doi: 10.1074/jbc.M112.362343
73. Lukkahatai, N., Patel, S., Gucek, M., Hsiao, C. P., and Saligan, L. N. (2014). Proteomic serum profile of fatigued men receiving localized external beam radiation therapy for non-metastatic prostate cancer. J. Pain SymptomManage. 47, 748.e4-756.e4. doi: 10.1016/j.jpainsymman.2013.05.016
74. Luo, Y., Yoneda, J., Ohmori, H., Sasaki, T., Shimbo, K., Eto, S., et al. (2014). Cancer usurps skeletal muscle as an energy repository. Cancer Res. 74, 330-340. doi: 10.1158/0008-5472.CAN-13-1052
75. Ma, C., Hu, L., Tao, G., Lv, W., and Wang, H. (2015). An UPLC-MS-based metabolomics investigation on the anti-fatigue effect of salidroside in mice. J. Pharm. Biomed. Anal. 105, 84-90. doi: 10.1016/j.jpba.2014.11.036
76. MacCiò, A., Madeddu, C., Gramignano, G., Mulas, C., Floris, C., Sanna, E., et al. (2012). A randomized phase III clinical trial of a combined treatment for cachexia in patients with gynecological cancers: evaluating the impact on metabolic and inflammatory profiles and quality of life. Gynecol. Oncol. 124, 417-425. doi: 10.1016/j.ygyno.2011.12.435
77. Mahoney, S. E., Davis, J. M., Murphy, E. A., McClellan, J. L., Gordon, B., and Pena, M. M. (2013). Effects of 5-fluorouracil chemotherapy on fatigue: role of MCP-1. Brain Behav. Immun. 27, 155-161. doi: 10.1016/j.bbi.2012.10.012
78. Maitra, U., Deng, H., Glaros, T., Baker, B., Capelluto, D. G., Li, Z., et al. (2012). Molecular mechanisms responsible for the selective and low-grade induction of proinflammatory mediators in murine macrophages by lipopolysaccharide. J. Immunol. 189, 1014-1023. doi: 10.4049/jimmunol.1200857
79. Malekzadeh, A., Van de Geer-Peeters, W., De Groot, V., Teunissen, C. E., and Beckerman, H. (2015). Fatigue in patients with multiple sclerosis: is it related to pro- and anti-inflammatory cytokines? Dis. Markers 2015:758314. doi: 10.1155/2015/758314
80. Markwald, R. R., Melanson, E. L., Smith, M. R., Higgins, J., Perreault, L., Eckel, R. H., et al. (2013). Impact of insufficient sleep on total daily energy expenditure, food intake, and weight gain. Proc. Natl. Acad. Sci. U.S.A. 110, 5695-5700. doi: 10.1073/pnas.1216951110
81. Masri, S., Patel, V. R., Eckel-Mahan, K. L., Peleg, S., Forne, I., Ladurner, A. G., et al. (2013). Circadian acetylome reveals regulation of mitochondrial metabolic pathways. Proc. Natl. Acad. Sci. U.S.A. 110, 3339-3344. doi: 10.1073/pnas.1217632110
82. McGettrick, A. F., and O’Neill, L. A. (2013). How metabolism generates signals during innate immunity and inflammation. J. Biol. Chem. 288, 22893-22898. doi: 10.1074/jbc.R113.486464
83. McHill, A. W., and Wright, K. P. Jr. (2017). Role of sleep and circadian disruption on energy expenditure and in metabolic predisposition to human obesity and metabolic disease. Obes. Rev. 18(Suppl. 1), 15-24. doi: 10.1111/obr.12503
84. Miaskowski, C., Lee, K., Dunn, L., Dodd, M., Aouizerat, B. E., West, C., et al. (2011). Sleep-wake circadian activity rhythm parameters and fatigue in oncology patients before the initiation of radiation therapy. Cancer Nurs. 34, 255-268. doi: 10.1097/NCC.0b013e3181f65d9b
85. Milrad, S. F., Hall, D. L., Jutagir, D. R., Lattie, E. G., Ironson, G. H., Wohlgemuth, W., et al. (2017). Poor sleep quality is associated with greater circulating pro-inflammatory cytokines and severity and frequency of chronic fatigue syndrome/myalgic encephalomyelitis (CFS/ME) symptoms in women. J. Neuroimmunol. 303, 43-50. doi: 10.1016/j.jneuroim.2016.12.008
86. Mirmiran, M., and Pévet, P. (1986). Effects of melatonin and 5-methoxytryptamine on sleep-wake patterns in the male rat. J. Pineal Res. 3, 135-141. doi: 10.1111/j.1600-079X.1986.tb00736.x
87. Montoya, J. G., Holmes, T. H., Anderson, J. N., Maecker, H. T., Rosenberg-Hasson, Y., Valencia, I. J., et al. (2017). Cytokine signature associated with disease severity in chronic fatigue syndrome patients. Proc. Natl. Acad. Sci. U.S.A. 114, E7150-E7158. doi: 10.1073/pnas.1710519114
88. Mortimer, J. E., Waliany, S., Dieli-Conwright, C. M., Patel, S. K., Hurria, A., Chao, J., et al. (2017). Objective physical and mental markers of self-reported fatigue in women undergoing (neo)adjuvant chemotherapy for early-stage breast cancer. Cancer 123, 1810-1816. doi: 10.1002/cncr.30426
89. Moss-Morris, R., Deary, V., and Castell, B. (2013). Chronic fatigue syndrome. Handb. Clin. Neurol. 110, 303-314. doi: 10.1016/b978-0-444-52901-5.00025-3
90. Naviaux, R. K., Naviaux, J. C., Li, K., Bright, A. T., Alaynick, W. A., Wang, L., et al. (2016). Metabolic features of chronic fatigue syndrome. Proc. Natl. Acad. Sci. U.S.A. 113, E5472-E5480. doi: 10.1073/pnas.1607571113
91. Neikrug, A. B., Rissling, M., Trofimenko, V., Liu, L., Natarajan, L., Lawton, S., et al. (2012). Bright light therapy protects women from circadian rhythm desynchronization during chemotherapy for breast cancer. Behav. Sleep Med. 10, 202-216. doi: 10.1080/15402002.2011.634940
92. Neufeld-Cohen, A., Robles, M. S., Aviram, R., Manella, G., Adamovich, Y., Ladeuix, B., et al. (2016). Circadian control of oscillations in mitochondrial rate-limiting enzymes and nutrient utilization by PERIOD proteins. Proc. Natl. Acad. Sci. U.S.A. 113, E1673-E1682. doi: 10.1073/pnas.1519650113
93. Niranjan, R. (2014). The role of inflammatory and oxidative stress mechanisms in the pathogenesis of Parkinson’s disease: focus on astrocytes. Mol. Neurobiol. 49, 28-38. doi: 10.1007/s12035-013-8483-x
94. Norden, D. M., McCarthy, D. O., Bicer, S., Devine, R. D., Reiser, P. J., Godbout, J. P., et al. (2015). Ibuprofen ameliorates fatigue- and depressive-like behavior in tumor-bearing mice. Life Sci. 143, 65-70. doi: 10.1016/j.lfs.2015.10.020
95. Nunes, E. J., Randall, P. A., Estrada, A., Epling, B., Hart, E. E., Lee, C. A., et al. (2014). Effort-related motivational effects of the pro-inflammatory cytokine interleukin 1-beta: studies with the concurrent fixed ratio 5/ chow feeding choice task. Psychopharmacology 231, 727-736. doi: 10.1007/s00213-013-3285-4
96. Pacelli, C., Giguère, N., Bourque, M.-J., Lévesque, M., Slack, Ruth, S., and Trudeau, L.-É. (2015). Elevated mitochondrial bioenergetics and axonal arborization size are key contributors to the vulnerability of dopamine neurons. Curr. Biol. 25, 2349-2360. doi: 10.1016/j.cub.2015.07.050
97. Papadopoulos, A. S., and Clear, A. J. (2011). Hypothalamic-pituitary-adrenal axis dysfunction in chronic fatigue syndrome. Nat. Rev. Endocrinol. 8, 22-32. doi: 10.1038/nrendo.2011.153
98. Park, J. H., Park, Y. S., and Koh, H. C. (2016). Progressive loss of nigrostriatal dopaminergic neurons induced by inflammatory responses to fipronil. Toxicol. Lett. 258, 36-45. doi: 10.1016/j.toxlet.2016.06.011
99. Patejdl, R., Penner, I. K., Noack, T. K., and Zettl, U. K. (2016). Multiple sclerosis and fatigue: a review on the contribution of inflammation and immune-mediated neurodegeneration. Autoimmun. Rev. 15, 210-220. doi: 10.1016/j.autrev.2015.11.005
100. Payne, J. K. (2011). Alteredcircadianrhythms andcancer-relatedfatigue outcomes. Integr. Cancer Ther. 10, 221-233. doi: 10.1177/1534735410392581
101. Peek, C. B., Affinati, A. H., Ramsey, K. M., Kuo, H. Y., Yu, W., Sena, L. A., et al. (2013). Circadian clock NAD+ cycle drives mitochondrial oxidative metabolismin mice. Science 342:1243417. doi: 10.1126/science.1243417
102. Persengiev, S., Kanchev, L., and Vezenkova, G. (1991). Circadian patterns of melatonin, corticosterone, and progesterone in male rats subjected to chronic stress: effect of constant illumination. J. Pineal Res. 11, 57-62. doi: 10.1111/j.1600-079X.1991.tb00456.x
103. Pollmächer, T., Schuld, A., Kraus, T., Haack, M., Hinze-Selch, D., and Mullington, J. (2000). Experimental immunomodulation, sleep, and sleepiness in humans. Ann. N. Y. Acad. Sci. 917, 488-499. doi: 10.1111/j.1749-6632.2000.tb05413.x
104. Porter, C., Constantin-Teodosiu, D., Constantin, D., Leighton, B., Poucher, S. M., and Greenhaff, P. L. (2017). Muscle carnitine availability plays a central role in regulating fuel metabolism in the rodent. J. Physiol. 595, 5765-5780. doi: 10.1113/JP274415
105. Potter, G. D., Skene, D. J., Arendt, J., Cade, J. E., Grant, P. J., andHardie, L. J. (2016). Circadian rhythm and sleep disruption: causes, metabolic consequences, and countermeasures. Endocr. Rev. 37, 584-608. doi: 10.1210/er.2016-1083
106. Rahman, K., Burton, A., Galbraith, S., Lloyd, A., and Vollmer-Conna, U. (2011). Sleep-wake behavior in chronic fatigue syndrome. Sleep 34, 671-678. doi: 10.1093/sleep/34.5.671
107. Rahman, S. A., Castanon-Cervantes, O., Scheer, F. A., Shea, S. A., Czeisler, C. A., Davidson, A. J., et al. (2015). Endogenous circadian regulation of pro-inflammatory cytokines and chemokines in the presence of bacterial lipopolysaccharide in humans. Brain Behav. Immun. 47, 4-13. doi: 10.1016/j.bbi.2014.11.003
108. Ramis, M. R., Esteban, S., Miralles, A., Tan, D. X., and Reiter, R. J. (2015). Protective effects of melatonin and mitochondria-targeted antioxidants against oxidative stress: a review. Curr. Med. Chem. 22, 2690-2711. doi: 10.2174/0929867322666150619104143
109. Redd, W. H., Valdimarsdottir, H., Wu, L. M., Winkel, G., Byrne, E. E., Beltre, M. A., et al. (2014). Systematic light exposure in the treatment of cancer-related fatigue: a preliminary study. Psychooncology 23, 1431-1434. doi: 10.1002/pon.3553
110. Reed, R. G., Weihs, K. L., Sbarra, D. A., Breen, E. C., Irwin, M. R., and Butler, E. A. (2016). Emotional acceptance, inflammation, and sickness symptoms across the first two years following breast cancer diagnosis. Brain Behav. Immun. 56, 165-174. doi: 10.1016/j.bbi.2016.02.018
111. Roerink, M. E., Bronkhorst, E. M., and Van der Meer, J. W. (2017). Metabolom of chronic fatigue syndrome. Proc. Natl. Acad. Sci. U.S.A. 114:E910. doi: 10.1073/pnas.1618447114
112. Russell, C., Wearden, A. J., Fairclough, G., Emsley, R. A., and Kyle, S. D. (2016). Subjective but not actigraphy-defined sleep predicts next-day fatigue in chronic fatigue syndrome: a prospective daily diary study. Sleep 39, 937-944. doi: 10.5665/sleep.5658
113. Sanoobar, M., Eghtesadi, S., Azimi, A., Khalili, M., Khodadadi, B., Jazayeri, S., et al. (2015). Coenzyme Q10 supplementation ameliorates inflammatory markers in patients with multiple sclerosis: a double blind, placebo, controlled randomized clinical trial. Nutr. Neurosci. 18, 169-176. doi: 10.1179/1476830513Y.0000000106
114. Servaes, P., Verhagen, C., and Bleijenberg, G. (2002). Fatigue in cancer patients during and after treatment: prevalence, correlates and interventions. Eur. J. Cancer 38, 27-43. doi: 10.1016/S0959-8049(01)00332-X
115. Shoelson, S. E., Lee, J., and Goldfine, A. B. (2006). Inflammation and insulin resistance. J. Clin. Invest. 116, 1793-1801. doi: 10.1172/JCI29069
116. Silverman, M. N., Heim, C. M., Nater, U. M., Marques, A. H., and Sternberg, E. M. (2010). Neuroendocrine and immune contributors to fatigue. PMR2, 338-346. doi: 10.1016/j.pmrj.2010.04.008
117. Singh, A., Garg, V., Gupta, S., and Kulkarni, S. K. (2002a). Role of antioxidants in chronic fatigue syndrome in mice. Indian J. Exp. Biol. 40, 1240-1244. Available online at: http://nopr.niscair.res.in/bitstream/123456789/23570/1/IJEB%2040 %2811%29%201240-1244.pdf
118. Singh, A., Naidu, P. S., Gupta, S., and Kulkarni, S. K. (2002b). Effect of natural and synthetic antioxidants in a mouse model of chronic fatigue syndrome. J. Med. Food 5, 211-220. doi: 10.1089/109662002763003366
119. Sinha, K., Das, J., Pal, P. B., and Sil, P. C. (2013). Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis. Arch. Toxicol. 87, 1157-1180. doi: 10.1007/s00204-013-1034-4
120. Snell, C. R., Stevens, S. R., Davenport, T. E., and Van Ness, J. M. (2013). Discriminative validity of metabolic and workload measurements for identifying people with chronic fatigue syndrome. Phys. Ther. 93, 1484-1492. doi: 10.2522/ptj.20110368
121. Sridharan, V., Tripathi, P., Aykin-Burns, N., Krager, K. J., Sharma, S. K., Moros, E. G., et al. (2015). Atocotrienol-enriched formulation protects against radiation-induced changes in cardiac mitochondria without modifying late cardiac function or structure. Radiat. Res. 183, 357-366. doi: 10.1667/RR13915.1
122. Straub, R. H. (2017). The brain and immune system prompt energy shortage in chronic inflammation and ageing. Nat. Rev. Rheumatol. 13, 743-751. doi: 10.1038/nrrheum.2017.172
123. Surapaneni, D. K., Adapa, S. R., Preeti, K., Teja, G. R., Veeraragavan, M., and Krishnamurthy, S. (2012). Shilajit attenuates behavioral symptoms of chronic fatigue syndrome by modulating the hypothalamic-pituitary-adrenal axis and mitochondrial bioenergetics in rats. J. Ethnopharmacol. 143, 91-99. doi: 10.1016/j.jep.2012.06.002
124. Tabassum, H., Waseem, M., Parvez, S., and Qureshi, M. I. (2015). Oxaliplatin-induced oxidative stress provokes toxicity in isolated rat liver mitochondria. Arch. Med. Res. 46, 597-603. doi: 10.1016/j.arcmed.2015.10.002
125. Tomas, C., Brown, A., Strassheim, V., Elson, J., Newton, J., and Manning, P. (2017). Cellular bioenergetics is impaired in patients with chronic fatigue syndrome. PLoS ONE 12:e0186802. doi: 10.1371/journal.pone.0186802
126. Tzika, A. A., Fontes-Oliveira, C. C., Shestov, A. A., Constantinou, C., Psychogios, N., Righi, V., et al. (2013). Skeletal muscle mitochondrial uncoupling in a murine cancer cachexia model. Int. J. Oncol. 43, 886-894. doi: 10.3892/ijo.2013.1998
127. van Heukelom, R. O., Prins, J. B., Smits, M. G., and Bleijenberg, G. (2006). Influence of melatonin on fatigue severity in patients with chronic fatigue syndrome and late melatonin secretion. Eur. J. Neurol. 13, 55-60. doi: 10.1111/j.1468-1331.2006.01132.x
128. Vichaya, E. G., Hunt, S. C., and Dantzer, R. (2014). Lipopolysaccharide reduces incentive motivation while boosting preference for high reward in mice. Neuropsychopharmacology 39, 2884-2890. doi: 10.1038/npp.2014.141
129. Vichaya, E. G., Molkentine, J. M., Vermeer, D. W., Walker, A. K., Feng, R., Holder, G., et al. (2016). Sickness behavior induced by cisplatin chemotherapy and radiotherapy in a murine head and neck cancer model is associated with altered mitochondrial gene expression. Behav. Brain Res. 297, 241-250. doi: 10.1016/j.bbr.2015.10.024
130. Vichaya, E. G., Vermeer, D. W., Christian, D. L., Molkentine, J. M., Mason, K. A., Lee, J. H., et al. (2017). Neuroimmune mechanisms of behavioral alterations in a syngeneic murine model of human papilloma virus-related head and neck cancer. Psychoneuroendocrinology 79, 59-66. doi: 10.1016/j.psyneuen.2017.02.006
131. Wang, J., Sun, C., Zheng, Y., Pan, H., Zhou, Y., and Fan, Y. (2014). The effective mechanism of the polysaccharides from Panax ginseng on chronic fatigue syndrome. Arch. Pharm. Res. 37, 530-538. doi: 10.1007/s12272-013-0235-y
132. Wang, L., Chen, Q., Qi, H., Wang, C., Wang, C., Zhang, J., et al. (2016). Doxorubicin-induced systemic inflammation is driven by upregulation of toll-like receptor TLR4 and endotoxin leakage. Cancer Res. 76, 6631-6642. doi: 10.1158/0008-5472.CAN-15-3034
133. Williams, G., Pirmohamed, J., Minors, D., Waterhouse, J., Buchan, I., Arendt, J., et al. (1996). Dissociation of body-temperature and melatonin secretion circadian rhythms in patients with chronic fatigue syndrome. Clin. Physiol. 16, 327-337. doi: 10.1111/j.1475-097X.1996.tb00722.x
134. Williams, G., Waterhouse, J., Mugarza, J., Minors, D., and Hayden, K. (2002). Therapy of circadian rhythm disorders in chronic fatigue syndrome: no symptomatic improvement withmelatoninor phototherapy. Eur. J. Clin. Invest. 32, 831-837. doi: 10.1046/j.1365-2362.2002.01058.x
135. Wolfe, F., Hawley, D. J., and Wilson, K. (1996). The prevalence and meaning of fatigue in rheumatic disease. J. Rheumatol. 23, 1407-1417.
136. Wright, K. P., Drake, A. L., Frey, D. J., Fleshner, M., Desouza, C. A., Gronfier, C., et al. (2015). Influence of sleep deprivation and circadian misalignment on cortisol, inflammatory markers, and cytokine balance. Brain Behav. Immun. 47, 24-34. doi: 10.1016/j.bbi.2015.01.004
137. Yamano, E., Sugimoto, M., Hirayama, A., Kume, S., Yamato, M., Jin, G., et al. (2016). Index markers of chronic fatigue syndrome with dysfunction of TCA and urea cycles. Sci. Rep. 6:34990. doi: 10.1038/srep34990
138. Yan, M. H., Wang, X., and Zhu, X. (2013). Mitochondrial defects and oxidative stress in Alzheimer disease and Parkinson disease. Free Radic. Biol. Med. 62(Suppl. C), 90-101. doi: 10.1016/j.freeradbiomed.2012.11.014
139. Yohn, S. E., Arif, Y., Haley, A., Tripodi, G., Baqi, Y., Müller, C. E., et al. (2016). Effort-related motivational effects of the pro-inflammatory cytokine interleukin-6: pharmacological and neurochemical characterization. Psychopharmacology 233, 3575-3586. doi: 10.1007/s00213-016-4392-9
140. Young, K. E., and White, C. A. (2006). The prevalence and moderators of fatigue in people who have been successfully treated for cancer. J. Psychosom. Res. 60, 29-38. doi: 10.1016/j.jpsychores.2005.03.011
141. Zhang, L., Zhang, H. Q., Liang, X. Y., Zhang, H. F., Zhang, T., and Liu, F. E. (2013). Melatonin ameliorates cognitive impairment induced by sleep deprivation in rats: role of oxidative stress, BDNF and CaMKII. Behav. Brain Res. 256, 72-81. doi: 10.1016/j.bbr.2013.07.051
142. Zhang, Z. T., Du, X. M., Ma, X. J., Zong, Y., Chen, J. K., Yu, C. L., et al. (2016). Activation of the NLRP3 inflammasome in lipopolysaccharide-induced mouse fatigue and its relevance to chronic fatigue syndrome. J. Neuroinflammation 13:71. doi: 10.1186/s12974-016-0539-1
143. Zhuang, C. L., Mao, X. Y., Liu, S., Chen, W. Z., Huang, D. D., Zhang, C. J., et al. (2014). Ginsenoside Rb1 improves postoperative fatigue syndrome by reducing skeletal muscle oxidative stress through activation of the PI3K/Akt/Nrf2 pathway in aged rats. Eur. J. Pharmacol. 740, 480-487. doi: 10.1016/j.ejphar.2014.06.040