Cell injury and repair resulting from sleep loss and sleep recovery in laboratory rats

Sleep

Volumn 37, Issue 12, 2014, Pages 1929-1940

  Everson, Carol A ^a,b   Henchen, Christopher J ^a   Szabo, Aniko ^a   Hogg, Neil ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b CLEMENT J ZABLOCKI VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

8 hydroxydeoxyguanosine; Apoptosis; Cell injury; Lipid peroxidation; Oxidative stress

Indexed keywords

3 NITROTYROSINE; CASPASE 3; CATALASE; GLUTATHIONE PEROXIDASE; LIPID; ANTIOXIDANT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; CELL DAMAGE; CELL DEATH; CELL FATE; CELL PROLIFERATION; CELL REGENERATION; CELLULAR DISTRIBUTION; COMPARATIVE STUDY; CONTROLLED STUDY; DNA DAMAGE; GENERAL CONDITION DETERIORATION; HEART; INTESTINE; LIMIT OF QUANTITATION; LIPID PEROXIDATION; LIVER; LUNG; MALE; NONHUMAN; OXIDATIVE STRESS; RAT; SIGNAL TRANSDUCTION; SLEEP DEPRIVATION; SPLEEN; ANIMAL; COMPLICATION; DISEASE PREDISPOSITION; DNA REPAIR; ENZYMOLOGY; METABOLISM; PATHOLOGY; PHYSIOLOGY; SLEEP; SMALL INTESTINE;

ANIMALS; ANTIOXIDANTS; CATALASE; CELL DEATH; CELL PROLIFERATION; DISEASE SUSCEPTIBILITY; DNA DAMAGE; DNA REPAIR; GLUTATHIONE PEROXIDASE; INTESTINE, SMALL; LIVER; LUNG; MALE; ORGAN SPECIFICITY; OXIDATIVE STRESS; RATS; SIGNAL TRANSDUCTION; SLEEP; SLEEP DEPRIVATION;

EID: 84914093940     PISSN: 01618105     EISSN: 15509109     Source Type: Journal    
DOI: 10.5665/sleep.4244     Document Type: Article

References (94)

1. National Sleep Disorders Research Plan: US Department of Health and Human Services, NIH Publication No. 11-7820, 2011.
2. Altman NG, Izci-Balserak B, Schopfer E, et al. Sleep duration versus sleep insufficiency as predictors of cardiometabolic health outcomes. Sleep Med 2012;13:1261-70.
3. Foley D, Ancoli-Israel S, Britz P, Walsh J. Sleep disturbances and chronic disease in older adults: results of the 2003 National Sleep Foundation Sleep in America Survey. J Psychosom Res 2004;56:497-502.
4. von Ruesten A, Weikert C, Fietze I, Boeing H. Association of sleep duration with chronic diseases in the European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam study. PLoS ONE 2012;7(1):e30972.
5. Jackson CM. The Effects of Inanition and Malnutrition Upon Growth and Structure. Philadelphia, PA: P. Blakiston's Son and Co., 1925.
6. Morgulis S. Fasting and Undernutrition. New York: Dutton, 1923.
7. Everson CA, Laatsch CD, Hogg N. Antioxidant defense responses to sleep loss and sleep recovery. Am J Physiol Regul Integr Comp Physiol 2005;288:374-83.
8. Halliwell B, Gutteridge JMC. Free Radicals in Biology and Medicine. 3rd ed. Oxford: Oxford University Press, 1999.
9. Altemus M, Rao B, Dhabhar FS, Ding W, Granstein RD. Stress-induced changes in skin barrier function in healthy women. J Invest Dermatol 2001;117:309-17.
10. Everson CA. Clinical manifestations of prolonged sleep deprivation. In: Schwartz WJ, ed. Sleep Science: Integrating Basic Research and Clinical Practice. Basel: Karger, 1997:34-59.
11. Frey DJ, Fleshner M, Wright KP Jr. The effects of 40 hours of total sleep deprivation on inflammatory markers in healthy young adults. Brain Behav Immun 2007;21:1050-7.
12. Haack M, Sanchez E, Mullington JM. Elevated inflammatory markers in response to prolonged sleep restriction are associated with increased pain experience in healthy volunteers. Sleep 2007;30:1145-52.
13. Hu J, Chen Z, Gorczynski CP, et al. Sleep-deprived mice show altered cytokine production manifest by perturbations in serum IL-1ra, TNFa, and IL-6 levels. Brain Behav Immun 2003;17:498-504.
14. Meier-Ewert HK, Ridker PM, Rifai N, et al. Effect of sleep loss on C-reactive protein, an inflammatory marker of cardiovascular risk. JACC 2004;43:678-83.
15. Moldofsky H, Lue FA, Davidson JR, Gorczynski R. Effects of sleep deprivation on human immune functions. FASEB J 1989;3:1972-7.
16. Shearer WT, Reuben JM, Mullington JM, et al. Soluble TNF-alpha receptor 1 and IL-6 plasma levels in humans subjected to the sleep deprivation model of spaceflight. J Allergy Clin Immunol 2001;107:165-70.
17. van Leeuwen WM, Lehto M, Karisola P, et al. Sleep restriction increases the risk of developing cardiovascular diseases by augmenting proinflammatory responses through IL-17 and CRP. PLoS ONE 2009;4(2):e4589.
18. Vgontzas AN, Zoumakis E, Bixler EO, et al. Adverse effects of modest sleep restriction on sleepiness, performance, and inflammatory cytokines. J Clin Endocrinol Metab 2004;89:2119-26.
19. Chang HM, Mai FD, Chen BJ, et al. Sleep deprivation predisposes liver to oxidative stress and phospholipid damage: a quantitative molecular imaging study. J Anat 2008;212:295-305.
20. Cirelli C, Faraguna U, Tononi G. Changes in brain gene expression after long-term sleep deprivation. J Neurochem 2006;98:1632-45.
21. Everson CA, Thalacker CD, Hogg N. Phagocyte migration and cellular stress induced in liver, lung, and intestine during sleep loss and sleep recovery. Am J Physiol Regul Integr Comp Physiol 2008;295:2067-74.
22. Guo JS, Chau JF, Shen XZ, Cho CH, Luk JM, Koo MW. Over-expression of inducible heat shock protein 70 in the gastric mucosa of partially sleepdeprived rats. Scand J Gastroenterol 2004;39:510-5.
23. Naidoo N, Ferber M, Master M, Zhu Y, Pack AI. Aging impairs the unfolded protein response to sleep deprivation and leads to proapoptotic signaling. J Neurosci 2008;28:6539-48.
24. Terao A, Steininger TL, Hyder K, et al. Differential increase in the expression of heat shock protein family members during sleep deprivation and during sleep. Neuroscience 2003;116:187-200.
25. Lungato L, Marques MS, Pereira VG, et al. Sleep deprivation alters gene expression and antioxidant enzyme activity in mice splenocytes. Scand J Immunol 2013;77:195-9.
26. Ramanathan L, Gulyani S, Nienhuis R, Siegel JM. Sleep deprivation decreases superoxide dismutase activity in rat hippocampus and brainstem. Neuroreport 2002;13:1387-90.
27. Dinges DF, Douglas SD, Zaugg L, et al. Leukocytosis and natural killer cell function parallel neurobehavioral fatigue induced by 64 hours of sleep deprivation. J Clin Invest 1994;93:1930-9.
28. Kleitman N. Sleep and Wakefulness. Chicago, IL: University of Chicago Press, 1963.
29. Kuhn E, Brodan V, Brodanova M, Rysanek K. Metabolic reflection of sleep deprivation. Act Nerv Super (Praha) 1969;11:165-74.
30. Andersen ML, Ribeiro DA, Bergamaschi CT, et al. Distinct effects of acute and chronic sleep loss on DNA damage in rats. Prog Neuropsychopharmacol Biol Psychiatry 2009;33:562-7.
31. Mendelson WB, Guthrie RD, Frederick G, Wyatt R.J. The flower pot technique of rapid eye movement (REM) sleep deprivation. Pharmacol Biochem Behav 1974;2:553-6.
32. Suchecki D, Tufik S. Social stability attenuates the stress in the modified multiple platform method for paradoxical sleep deprivaiton in the rat. Physiol Behav 2000;68:309-16.
33. Everson CA. Clinical assessment of blood leukocytes, serum cytokines, and serum immunoglobulins as responses to sleep deprivation in laboratory rats. Am J Physiol Regul Integr Comp Physiol 2005;289:1054-63.
34. Everson CA. Sustained sleep deprivation impairs host defense. Am J Physiol Regul Integr Comp Physiol 1993;265:1148-54.
35. Gilliland M, Wold L, Wollmann R, Eschenbach K, Rechtschaffen A. Pathology in sleep deprived rats is not reflected in histologic abnormalities (Abstract). Sleep Res 1984;13:190.
36. National Research Council of the National Academies. Committee for the Update of the Guide for the Care and Use of Laboratory Animals. Guide for the Care and Use of Laboratory Animals. 8th ed. Washington, DC: The National Academies Press, 2011.
37. Bergmann BM, Kushida CA, Everson CA, Gilliland MA, Obermeyer W, Rechtschaffen A. Sleep deprivation in the rat: II. Methodology. Sleep 1989;12:5-12.
38. Mistlberger RE, Belcourt J, Antle MC. Circadian clock resetting by sleep deprivation without exercise in Syrian hamsters: dark pulses revisited. J Biol Rhythms 2002;17:227-37.
39. Tsai LL, Bergmann BM, Rechtschaffen A. Sleep deprivation in the rat: XVI. Effects in a light-dark cycle. Sleep 1992;15:537-44.
40. Romanovsky AA, Ivanov AI, Shimansky YP. Ambient temperature for experiments in rats: a new method for determining the zone of thermal neutrality. J Appl Physiol 2002;92:2667-79.
41. Everson CA, Wehr TA. Nutritional and metabolic adaptations to prolonged sleep deprivation in the rat. Am J Physiol Regul Integr Comp Physiol 1993;264:376-87.
42. Everson CA, Bergmann BM, Rechtschaffen A. Sleep deprivation in the rat. III. Total sleep deprivation. Sleep 1989;12:13-21.
43. Everson CA, Smith CB, Sokoloff L. Effects of prolonged sleep deprivation on local rates of cerebral energy metabolism in freely moving rats. J Neurosci 1994;14:6769-78.
44. Everson CA, Szabo A. Recurrent restriction of sleep and inadequate recuperation induce both adaptive changes and pathological outcomes. Am J Physiol Regul Integr Comp Physiol 2009;297:1430-40.
45. Everson CA, Gilliland MA, Kushida CA, et al. Sleep deprivation in the rat: IX. Recovery. Sleep 1989;12:60-7.
46. Rechtschaffen A, Bergmann BM, Gilliland MA, Bauer K. Effects of method, duration, and sleep stage on rebounds from sleep deprivation in the rat. Sleep 1999;22:11-31.
47. Milne GL, Sanchez SC, Musiek ES, Morrow JD. Quantification of F2-isoprostanes as a biomarker of oxidative stress. Nat Protoc 2007;2:221-6.
48. Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979;95:351-8.
49. Aebi H. Catalase. In: Bergmeyer HU, ed. Methods of Enzymatic Analysis. New York: Academic Press, 1974:673-84.
50. Karthikeyan K, Bai BR, Gauthaman K, Sathish KS, Devaraj SN. Cardioprotective effect of the alcoholic extract of Terminalia arjuna bark in an in vivo model of myocardial ischemic reperfusion injury. Life Sci 2003;73:2727-39.
51. Drucker DJ, Ehrlich P, Asa SL, Brubaker PL. Induction of intestinal epithelial proliferation by glucagon-like peptide 2. Proc Natl Acad Sci U S A 1996;93:7911-6.
52. Kotani J, Usami M, Nomura H, et al. Enteral nutrition prevents bacterial translocation but does not improve survival during acute pancreatitis. Arch Surg 1999:287-92.
53. Renes IB, Verburg M, Bulsing NP, et al. Protection of the Peyer's patch-associated crypt and villus epithelium against methotrexate-induced damage is based on its distinct regulation of proliferation. J Pathol 2002;198:60-8.
54. Taminiau JA, Gall DG, Hamilton JR. Response of the rat small-intestine epithelium to methotrexate. Gut 1980;21:486-92.
55. Toyoda K, Nishikawa A, Furukawa F, Kawanishi T, Hayashi Y, Takahashi M. Cell proliferation induced by laxatives and related compounds in the rat intestine. Cancer Lett 1994;83:43-9.
56. Scholzen T, Gerdes J. The Ki-67 protein: from the known and the unknown. J Cell Physiol 2000;182:311-22.
57. Hakem R. DNA-damage repair; the good, the bad, and the ugly. EMBO J 2008;27:589-605.
58. Halliwell B. Effect of diet on cancer development: is oxidative DNA damage a biomarker? Free Radic Biol Med 2002;32:968-74.
59. Valavanidis A, Vlachogianni T, Fiotakis C. 8-hydroxy-2'-deoxyguanosine (8-OHdG): a critical biomarker of oxidative stress and carcinogenesis. J Environ Sci Health Part C Environ Carcinog Ecotoxicol Rev 2009;27:120-39.
60. Chipuk JE, Green DR. Dissecting p53-dependent apoptosis. Cell Death Differ 2006;13:994-1002.
61. Loft S, Poulsen HE. Cancer risk and oxidative DNA damage in man. J Mol Med 1996;74:297-312.
62. Matsui A, Ikeda T, Enomoto K, et al. Increased formation of oxidative DNA damage, 8-hydroxy-2'-deoxyguanosine, in human breast cancer tissue and its relationship to GSTP1 and COMT genotypes. Cancer Lett 2000;151:87-95.
63. Iwai K, Adachi S, Takahashi M, et al. Early oxidative DNA damages and late development of lung cancer in diesel exhaust-exposed rats. Environ Res 2000;84:255-64.
64. Bashir S, Harris G, Denman MA, Blake DR, Winyard PG. Oxidative DNA damage and cellular sensitivity to oxidative stress in human autoimmune diseases. Ann Rheum Dis 1993;52:659-66.
65. Gray K, Bennett M. Role of DNA damage in atherosclerosis - bystander or participant? Biochem Pharmacol 2011;82:693-700.
66. Mahmoudi M, Mercer J, Bennett M. DNA damage and repair in atherosclerosis. Cardiovasc Res 2006;71:259-68.
67. Wang JC, Bennett M. Aging and atherosclerosis: mechanisms, functional consequences, and potential therapeutics for cellular senescence. Circ Res 2012;111:245-59.
68. Feng B, Ruiz MA, Chakrabarti S. Oxidative-stress-induced epigenetic changes in chronic diabetic complications. Can J Physiol Pharmacol 2013;91:213-20.
69. Kawasaki E, Abiru N, Eguchi K. Prevention of type 1 diabetes: from the view point of beta cell damage. Diabetes Res Clin Pract 2004;66:27-32.
70. Jena G, Trivedi PP, Sandala B. Oxidative stress in ulcerative colitis: an old concept but a new concern. Free Radic Res 2012;46:1339-45.
71. Okayasu I. Development of ulcerative colitis and its associated colorectal neoplasia as a model of the organ-specific chronic inflammationcarcinoma sequence. Pathol Int 2012;62:368-80.
72. Berquist BR, Wilson DM 3rd. Pathways for repairing and tolerating the spectrum of oxidative DNA lesions. Cancer Lett 2012;327:61-72.
73. Heath JP. Epithelial cell migration in the intestine. Cell Biol Int 1996;20:139-46.
74. Klein RM, McKenzie JC. The role of cell renewal in the ontogeny of the intestine. I. Cell proliferation patterns in adult, fetal, and neonatal intestine. J Pediatr Gastroenterol Nutr 1983;2:10-43.
75. Creamer B, Shorter RG, Bamforth J. The turnover and shedding of epithelial cells. I. The turnover in the gastro-intestinal tract. Gut 1961:110-8.
76. Dotan I, Mayer L. Mucosal immunity. In: Feldman M, Friedman LS, Brandt LJ, eds. Sleisenger and Fordtran's Gastrointestinal and Liver Disease. 9th ed. Philadelphia, PA: Saunders, 2010:21-30.
77. Casado J, Fernandez-Lopez JA, Esteve M, Rafecas I, Argiles JM, Alemany M. Rat splanchnic net oxygen consumption, energy implications. J Physiol (Lond) 1990;431:557-69.
78. Ferrell CL. Contribution of visceral organs to animal energy expenditures. J Anim Sci 1988;66:23-34.
79. Seril DN, Liao J, Yang GY, Yang CS. Oxidative stress and ulcerative colitis-associated carcinogenesis: studies in humans and animal models. Carcinogenesis 2003;24:353-62.
80. Rizk P, Barker N. Gut stem cells in tissue renewal and disease: methods, markers, and myths. Wiley Interdiscip Rev Syst Biol Med 2012;4:475-96.
81. Gopaul NK, Halliwell B, Anggard EE. Measurement of plasma F2-isoprostanes as an index of lipid peroxidation does not appear to be confounded by diet. Free Radic Res 2000;33:115-27.
82. Roberts LJ, Morrow JD. Measurement of F(2)-isoprostanes as an index of oxidative stress in vivo. Free Radic Biol Med 2000;28:505-13.
83. Hulbert AJ, Pamplona R, Buffenstein R, Buttemer WA. Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev 2007;87:1175-213.
84. Sanz A, Pamplona R, Barja G. Is the mitochondrial free radical theory of aging intact? Antioxid Redox Signal 2006;8:582-99.
85. Everson CA, Crowley WR. Reductions in circulating anabolic hormones induced by sustained sleep deprivation in rats. Am J Physiol Endocrinol Metab 2004;286:1060-70.
86. Everson CA, Nowak TSJ. Hypothalamic thyrotropin-releasing hormone mRNA responses to hypothyroxinemia induced by sleep deprivation. Am J Physiol Endocrinol Metab 2002;283:85-93.
87. Everson CA, Reed HL. Pituitary and peripheral thyroid hormone responses to thyrotropin-releasing hormone during sustained sleep deprivation in freely moving rats. Endocrinology 1995;136:1426-34.
88. Gulec M, Ozkol H, Selvi Y, et al. Oxidative stress in patients with primary insomnia. Prog Neuropsychopharmacol Biol Psychiatry 2012;37:247-51.
89. Gopalakrishnan A, Ji L, Cirelli C. Sleep deprivation and cellular responses to oxidative stress. Sleep 2004;27:27-35.
90. Barclay JL, Husse J, Bode B, et al. Circadian desynchrony promotes metabolic disruption in a mouse model of shiftwork. PLoS ONE 2012;7(5):e37150.
91. Moller-Levet CS, Archer SN, Bucca G, et al. Effects of insufficient sleep on circadian rhythmicity and expression amplitude of the human blood transcriptome. Proc Natl Acad Sci U S A 2013;110:E1132-41.
92. Orr WC, Stahl ML. Sleep disturbances after open heart surgery. Am J Cardiol 1977;39:196-201.
93. Soutiere SE, Shemery A, Steele CT, Quatroche A, Dyche J. Scientific rationale for the "All Hands Awake" 24-hour watchstanding schedule. Document NSMRL/50513/TR-2013, Groton, CT, 2013.
94. Luyster FS, Strollo PJ, Zee PC, Walsh JK, Boards of Directors of the American Academy of Sleep Medicine and the Sleep Research Society. Sleep: a health imperative. Sleep 2012;35:727-34.