Sleep restriction in Wistar rats impairs epididymal postnatal development and sperm motility in association with oxidative stress
Gláucia E. M. L. Siervo A B , Fernanda M. Ogo A B , Aline D. Valério A , Thamara N. X. Silva B , Larissa Staurengo-Ferrari B , Tathiana A. Alvarenga C , Rubens Cecchini B , Waldiceu A. VerriA Department of General Biology, Biological Sciences Center, State University of Londrina – UEL, Rodovia Celso Garcia Cid, PR 445 - Km 380, Campus Universitário, 86057-970, Londrina, Paraná, Brazil.
B Department of General Pathology, Biological Sciences Center, State University of Londrina – UEL, Rodovia Celso Garcia Cid, PR 445 - Km 380, Campus Universitário, 86057-970, Londrina, Paraná, Brazil.
C Departamento de Psicobiologia, Universidade Federal de São Paulo – UNIFESP, Rua Napoleão de Barros, 925, Vila Clementino, 04024-002, São Paulo, SP, Brazil.
D Corresponding author. Email: glaura@uel.br
Reproduction, Fertility and Development 29(9) 1813-1820 https://doi.org/10.1071/RD15535
Submitted: 18 December 2015 Accepted: 27 September 2016 Published: 26 October 2016
Abstract
Good sleep quality has a direct effect on the activity of the neuroendocrine–reproductive control axis and oxidative stress. Thus, the aim of the present study was to evaluate whether sleep restriction (SR) during the peripubertal period impaired the postnatal development of the epididymis in Wistar rats. After 21 days SR (18 h per day), epididymides were collected on Postnatal Day (PND) 62 for evaluation of oxidative stress markers, inflammatory profile, sperm count and histopathological and stereological analyses; in addition, the motility of spermatozoa from the vas deferens was examined. SR significantly increased lipid peroxidation and glutathione levels in the caput and cauda epididymidis, and increased levels of total radical-trapping antioxidant potential in the caput epididymidis only. Neutrophil migration to the caput or corpus epididymidis was decreased by SR, and the size of the luminal compartment in the 2A region and the epithelial compartment in the 5A/B region was also decreased. In these regions, there was an increase in the size of the interstitial compartment. The percentage of immotile spermatozoa was higher in the SR group. In conclusion, SR affects epididymal postnatal development, as well as sperm motility, in association with increased oxidative stress and a decrease in the size of the epithelial compartment in the cauda epididymidis.
References
Aitken, R. J., Wingate, J. K., De Iuliis, G. N., Koppers, A. J., and McLaughlin, E. A. (2006). Cis-unsaturated fatty acids stimulate reactive oxygen species generation and lipid peroxidation in human spermatozoa. J. Clin. Endocrinol. Metab. 91, 4154–4163.| Cis-unsaturated fatty acids stimulate reactive oxygen species generation and lipid peroxidation in human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFSjtbvP&md5=bcda5f3c0eed1c7f954cdcd2d8fec2f0CAS | 16895947PubMed |
Alvarenga, T. A., Hirotsu, C., Mazaro-Costa, R., Tufik, S., and Andersen, M. L. (2015). Impairment of male reproductive function after sleep deprivation. Fertil. Steril. 103, 1355–1362.e1.
| Impairment of male reproductive function after sleep deprivation.Crossref | GoogleScholarGoogle Scholar | 25747127PubMed |
Alzoubi, K. H., Khabour, O. F., Rashid, B. A., Damaj, I. M., and Salah, H. A. (2012). The neuroprotective effect of vitamin E on chronic sleep deprivation-induced memory impairment: the role of oxidative stress. Behav. Brain Res. 226, 205–210.
| The neuroprotective effect of vitamin E on chronic sleep deprivation-induced memory impairment: the role of oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlertLjE&md5=6d8a9a74b17bf5c288a030558a822e1cCAS | 21944940PubMed |
Andersen, M. L., Alvarenga, T. F., Mazaro-Costa, R., Hachul, H. C., and Tufik, S. (2011). The association of testosterone, sleep, and sexual function in men and women. Brain Res. 1416, 80–104.
| The association of testosterone, sleep, and sexual function in men and women.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1agsbnP&md5=86e9c547c574d360720ce2b672457849CAS | 21890115PubMed |
Barf, R. P., Van Dijk, G., Scheurink, A. J. W., Hoffmann, K., Novati, A., Hulshof, H. J., Fuchs, E., and Meerlo, P. (2012). Metabolic consequences of chronic sleep restriction in rats: changes in body weight regulation and energy expenditure. Physiol. Behav. 107, 322–328.
| Metabolic consequences of chronic sleep restriction in rats: changes in body weight regulation and energy expenditure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslCku7fM&md5=57d43ef8e251fee41bc6e5386c58b41fCAS | 22995976PubMed |
Bradley, P. P., Priebat, D. A., Christensen, R. D., and Rothstein, G. (1982). Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J. Invest. Dermatol. 78, 206–209.
| Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XotlyitQ%3D%3D&md5=e382afc29584f2a971731d6c231a4101CAS | 6276474PubMed |
Chang, H. M., Mai, F. D., Chen, B. J., Wu, U. I., Huang, Y. L., Lan, C. T., and Ling, Y. C. (2008). Sleep deprivation predisposes liver to oxidative stress and phospholipid damage: a quantitative molecular imaging study. J. Anat. 212, 295–305.
| Sleep deprivation predisposes liver to oxidative stress and phospholipid damage: a quantitative molecular imaging study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksFWgt7Y%3D&md5=ff2bb92d47146f72f16f3e87b4f9315dCAS | 18221481PubMed |
Cornwall, G. A. (2009). New insights into epididymal biology and function. Hum. Reprod. Update 15, 213–227.
| New insights into epididymal biology and function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Ogurc%3D&md5=86111e1f62d2b208738d4cb31348aa4fCAS | 19136456PubMed |
Dacheux, J. L., and Dacheux, F. (2014). New insights into epididymal function in relation to sperm maturation. Reproduction 147, R27–R42.
| New insights into epididymal function in relation to sperm maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXisFartro%3D&md5=352f4c07673e0a0ae30f979fec4f1b12CAS | 24218627PubMed |
Dexter, D., Bijwadia, J., Schilling, D., and Applebaugh, G. (2003). Sleep, sleepiness and school start times: a preliminary study. WMJ 102, 44–46.
| 12679971PubMed |
Du Plessis, S. S., Agarwal, A., Halabi, J., and Tvrda, E. (2015). Contemporary evidence on the physiological role of reactive oxygen species in human sperm function. J. Assist. Reprod. Genet. 32, 509–520.
| Contemporary evidence on the physiological role of reactive oxygen species in human sperm function.Crossref | GoogleScholarGoogle Scholar | 25646893PubMed |
Everson, C. A., Henchen, C. J., Szabo, A., and Hogg, N. (2014). Cell injury and repair resulting from sleep loss and sleep recovery in laboratory rats. Sleep 37, 1929–1940.
| 25325492PubMed |
Favareto, A. P. A., de Toledo, F. C., and Kempinas, W. D. G. (2011). Paternal treatment with cisplatin impairs reproduction of adult male offspring in rats. Reprod. Toxicol. 32, 425–433.
| Paternal treatment with cisplatin impairs reproduction of adult male offspring in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFegtrbM&md5=1f8ff724bece24d91217bfa50c433e38CAS |
Fernandes, G. S. A., Arena, A. C., Fernandez, C. D. B., Mercadante, A., Barbisan, L. F., and Kempinas, W. G. (2007). Reproductive effects in male rats exposed to diuron. Reprod. Toxicol. 23, 106–112.
| Reproductive effects in male rats exposed to diuron.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXisValsA%3D%3D&md5=b01cbace1eae9e0038cf308461777aa5CAS |
García-Díaz, E. C., Gómez-Quiroz, L. E., Arenas-Ríos, E., Aragón-Martínez, A., Ibarra-Arias, J. A., and Retana-Márquez, M. S. I. (2015). Oxidative status in testis and epididymal sperm parameters after acute and chronic stress by cold-water immersion in the adult rat. Syst. Biol. Reprod. Med. 61, 150–160.
| 25640572PubMed |
Golub, M. S., Collman, G. W., Foster, P. M. D., Kimmel, C. A., Rajpert-De Meyts, E., Reiter, E. O., Sharpe, R. M., Skakkebaek, N. E., and Toppari, J. (2008). Public health implications of altered puberty timing. Pediatrics 121, S218–S230.
| Public health implications of altered puberty timing.Crossref | GoogleScholarGoogle Scholar | 18245514PubMed |
Gonzalez-Flecha, B., Llesuy, S., and Boveris, A. (1991). Hydroperoxide-initiated chemiluminescence: an assay for oxidative stress in biopsies of heart, liver, and muscle. Free Radic. Biol. Med. 10, 93–100.
| Hydroperoxide-initiated chemiluminescence: an assay for oxidative stress in biopsies of heart, liver, and muscle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M3gtVOisA%3D%3D&md5=a903d9d3326d34e2be45bc0a9fc216d1CAS | 1849867PubMed |
Hagenauer, M. H., and Lee, T. M. (2013). Adolescent sleep patterns in humans and laboratory animals. Horm. Behav. 64, 270–279.
| Adolescent sleep patterns in humans and laboratory animals.Crossref | GoogleScholarGoogle Scholar | 23998671PubMed |
Horinouchi, C. D. D. S., Mendes, D. A. G. B., Soley, B. D. S., Pietrovski, E. F., Facundo, V. A., Santos, A. R. S., Cabrini, D. A., and Otuki, M. F. (2013). Combretum leprosum Mart. (Combretaceae): potential as an antiproliferative and anti-inflammatory agent. J. Ethnopharmacol. 145, 311–319.
| Combretum leprosum Mart. (Combretaceae): potential as an antiproliferative and anti-inflammatory agent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhsl2jurfE&md5=e13899550e622b388afb127f7c3c4940CAS |
Hosseinzadeh Colagar, A., Karimi, F., and Jorsaraei, S. G. A. (2013). Correlation of sperm parameters with semen lipid peroxidation and total antioxidants levels in astheno- and oligoasheno-teratospermic men. Iran. Red Crescent Med. J. 15, 780–785.
| Correlation of sperm parameters with semen lipid peroxidation and total antioxidants levels in astheno- and oligoasheno-teratospermic men.Crossref | GoogleScholarGoogle Scholar | 24616785PubMed |
Jenni, O. G., and Carskadon, M. A. (2012). Sleep behavior and sleep regulation from infancy through adolescence: normative aspects. Sleep Med. Clin. 7, 529–538.
| Sleep behavior and sleep regulation from infancy through adolescence: normative aspects.Crossref | GoogleScholarGoogle Scholar |
Kumar, A., and Singh, A. (2008). Possible nitric oxide modulation in protective effect of (Curcuma longa, Zingiberaceae) against sleep deprivation-induced behavioral alterations and oxidative damage in mice. Phytomedicine 15, 577–586.
| Possible nitric oxide modulation in protective effect of (Curcuma longa, Zingiberaceae) against sleep deprivation-induced behavioral alterations and oxidative damage in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlSrs7zF&md5=61978771c6707ac47a58303a5a6aca35CAS | 18586477PubMed |
Llesuy, S. F., Milei, J., Gonzalez-Flecha, B. S., and Boveris, A. (1990). Myocardial damage induced by doxorubicins: hydroperoxide-initiated chemiluminescence and morphology. Free Radic. Biol. Med. 8, 259–264.
| Myocardial damage induced by doxorubicins: hydroperoxide-initiated chemiluminescence and morphology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXkvVCqt74%3D&md5=644c375251363e582d3251a2ef00493aCAS | 2341055PubMed |
Machado, R. B., Suchecki, D., and Tufik, S. (2005). Sleep homeostasis in rats assessed by a long-term intermittent paradoxical sleep deprivation protocol. Behav. Brain Res. 160, 356–364.
| Sleep homeostasis in rats assessed by a long-term intermittent paradoxical sleep deprivation protocol.Crossref | GoogleScholarGoogle Scholar | 15863232PubMed |
Maia, L. O., Dias, W., Carvalho, L. S., Jesus, L. R., Paiva, G. D., Araujo, P., Costa, M. F. O., Andersen, M. L., Tufik, S., and Mazaro-Costa, R. (2011). Association of methamidophos and sleep loss on reproductive toxicity of male mice. Environ. Toxicol. Pharmacol. 32, 155–161.
| 1:CAS:528:DC%2BC3MXhtVagtLzF&md5=e637d5d0578478a6b93cac125ddc8192CAS | 21843794PubMed |
Mantovani, A., and Fucic, A. (2014). Puberty dysregulation and increased risk of disease in adult life: possible modes of action. Reprod. Toxicol. 44, 15–22.
| Puberty dysregulation and increased risk of disease in adult life: possible modes of action.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVKmtr7M&md5=f73c0e9319bfc92770886a03466e447bCAS | 23791931PubMed |
McEwen, B. S. (2006). Sleep deprivation as a neurobiologic and physiologic stressor: allostasis and allostatic load. Metabolism 55, S20–S23.
| Sleep deprivation as a neurobiologic and physiologic stressor: allostasis and allostatic load.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xps1aisrw%3D&md5=4d78b5a662b4d0c6d8f5e4ce58e9c090CAS | 16979422PubMed |
Miller, R. J., and Killian, G. J. (1987). Morphometric analyses of the epididymis from normal and vasectomized rats. J. Androl. 8, 279–291.
| 1:STN:280:DyaL1c%2Fjt1KjsQ%3D%3D&md5=b9f517f25a8827727b68934c5b912b41CAS | 3667425PubMed |
Mônico-Neto, M., Antunes, H. K. M., Lee, K. S., Phillips, S. M., Giampá, S. Q. C., Souza, H. S., Dáttilo, M., Medeiros, A., Moraes, W. M., Tufik, S., and Mello, M. T. (2015). Resistance training minimizes catabolic effect induced by sleep deprivation in rats. Appl. Physiol. Nutr. Metab. 40, 1143–1150.
| Resistance training minimizes catabolic effect induced by sleep deprivation in rats.Crossref | GoogleScholarGoogle Scholar | 26513007PubMed |
National Sleep Foundation (2014). Sleep in America® poll sleep in the modern family. Available at https://sleepfoundation.org/sites/default/files/2014-NSF-Sleep-in-America-poll-summary-of-findings—FINAL-Updated-3-26-14-.pdf [verified 11 March 2015].
O’Shaughnessy, P. (2015). Testicular development. In ‘Physiology of Reproduction’. 4th edn. (Eds E. Knobil and J. D. Neill.) pp. 601–771. (Elsevier: New York.)
Oliveira, F. J., and Cecchini, R. (2000). Oxidative stress of liver in hamsters infected with Leishmania (L.) chagasi. J. Parasitol. 86, 1067–1072.
| Oxidative stress of liver in hamsters infected with Leishmania (L.) chagasi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnvVOisLk%3D&md5=085a726a2a2ac8900166c5a21284cc57CAS | 11128482PubMed |
Owens, J. (2014). Insufficient sleep in adolescents and young adults: an update on causes and consequences. Pediatrics 134, e921–e932.
| Insufficient sleep in adolescents and young adults: an update on causes and consequences.Crossref | GoogleScholarGoogle Scholar | 25157012PubMed |
Perobelli, J. E. (2014). The male peripubertal phase as a developmental window for reproductive toxicology studies. Curr. Pharm. Des. 20, 5398–5415.
| The male peripubertal phase as a developmental window for reproductive toxicology studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFCgt7nL&md5=391143bc1b28dea812cead6896b5ee2eCAS | 24502595PubMed |
Prevot, V. (2015). Puberty in mice and rats. In ‘Physiology of Reproduction’. 4th edn. (Eds E. Knobil and J. D. Neill.) pp. 1395–1439. (Elsevier: New York.)
Repetto, M., Reides, C., Gomez Carretero, M. L., Costa, M., Griemberg, G., and Llesuy, S. (1996). Oxidative stress in blood of HIV infected patients. Clin. Chim. Acta 255, 107–117.
| Oxidative stress in blood of HIV infected patients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmvFars78%3D&md5=ddcd2517f14b02cd9cbee9e01157d1f0CAS | 8937754PubMed |
Robaire, B., and Hinton, B. T. (2015). The epididymis. In ‘Physiology of Reproduction’. 4th edn. (Eds E. Knobil and J. D. Neill.) pp. 601–771. (Elsevier: New York.)
Robb, G. W., Amann, R. P., and Killian, G. J. (1978). Daily sperm production and epididymal sperm reserves of pubertal and adult rats. J. Reprod. Fertil. 54, 103–107.
| Daily sperm production and epididymal sperm reserves of pubertal and adult rats.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1M%2FltVegtg%3D%3D&md5=6695c052b6e06324fe3c7f4a55a50b9aCAS | 712697PubMed |
Rodrigues, N. C., da Cruz, N. S., de Paula Nascimento, C., da Conceição, R. R., da Silva, A. C. M., Olivares, E. L., and Marassi, M. P. (2015). Sleep deprivation alters thyroid hormone economy in rats. Exp. Physiol. 100, 193–202.
| Sleep deprivation alters thyroid hormone economy in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvV2htb8%3D&md5=3f9b135480f43e53e89b39dd7cb15ac1CAS | 25480161PubMed |
Shaw, N. D., Butler, J. P., Nemati, S., Kangarloo, T., Ghassemi, M., Malhotra, A., and Hall, J. E. (2015). Accumulated deep sleep is a powerful predictor of LH pulse onset in pubertal children. J. Clin. Endocrinol. Metab. 100, 1062–1070.
| Accumulated deep sleep is a powerful predictor of LH pulse onset in pubertal children.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXlvVGitL4%3D&md5=084c1661204cf96d55838d6cc544bbf3CAS | 25490277PubMed |
She, M., Hu, X., Su, Z., Zhang, C., Yang, S., Ding, L., Laudon, M., and Yin, W. (2014). Piromelatine, a novel melatonin receptor agonist, stabilizes metabolic profiles and ameliorates insulin resistance in chronic sleep restricted rats. Eur. J. Pharmacol. 727, 60–65.
| Piromelatine, a novel melatonin receptor agonist, stabilizes metabolic profiles and ameliorates insulin resistance in chronic sleep restricted rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXksFaisbY%3D&md5=d26fb0430be701d87f6c5b8d4b3192e9CAS | 24486392PubMed |
Siervo, G. E. M. L., Vieira, H. R., Ogo, F. M., Fernandez, C. D. B., Gonçalves, G. D., Mesquita, S. F. P., Anselmo-franci, J. A., Cecchini, R., Guarnier, F. A., and Fernandes, G. S. A. (2015). Spermatic and testicular damages in rats exposed to ethanol: influence of lipid peroxidation but not testosterone. Toxicology 330, 1–8.
| Spermatic and testicular damages in rats exposed to ethanol: influence of lipid peroxidation but not testosterone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsleqs7w%3D&md5=ef4a79b7dbe3747f68c2300f70fb8fb4CAS |
Sun, Y. (1990). Free radicals, antioxidant enzymes, and carcinogenesis. Free Radic. Biol. Med. 8, 583–599.
| Free radicals, antioxidant enzymes, and carcinogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXkvVKrsLk%3D&md5=0fafabc188638a33f41bb0743785df3eCAS | 2193855PubMed |
Sun, E. L., and Flickinger, C. J. (1979). Development of cell types and of regional differences in the postnatal rat epididymis. Am. J. Anat. 154, 27–55.
| Development of cell types and of regional differences in the postnatal rat epididymis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1M7gtFWisw%3D%3D&md5=10512e5bc2e476a4047e40a5070054cdCAS | 760488PubMed |
Tietze, F. (1969). Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem. 27, 502–522.
| Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1MXktVSlt7k%3D&md5=6cbc68257bfd5aec2d9552be8212d601CAS | 4388022PubMed |
Valério, D. A., Georgetti, S. R., Magro, D. A., Casagrande, R., Cunha, T. M., Vicentini, F. T. M. C., Vieira, S. M., Fonseca, M. J. V., Ferreira, S. H., Cunha, F. Q., and Verri, W. A. (2009). Quercetin reduces inflammatory pain: inhibition of oxidative stress and cytokine production. J. Nat. Prod. 72, 1975–1979.
| Quercetin reduces inflammatory pain: inhibition of oxidative stress and cytokine production.Crossref | GoogleScholarGoogle Scholar | 19899776PubMed |
Van den Bulck, J. (2004). Television viewing, computer game playing, and Internet use and self-reported time to bed and time out of bed in secondary-school children. Sleep 27, 101–104.
| 14998244PubMed |
Vollert, C., Zagaar, M., Hovatta, I., Taneja, M., Vu, A., Dao, A., Levine, A., Alkadhi, K., and Salim, S. (2011). Exercise prevents sleep deprivation-associated anxiety-like behavior in rats: potential role of oxidative stress mechanisms. Behav. Brain Res. 224, 233–240.
| Exercise prevents sleep deprivation-associated anxiety-like behavior in rats: potential role of oxidative stress mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVKjt7rJ&md5=9245f749a62d3007c7d47a8115f53eefCAS | 21621560PubMed |
Wallingford, J. K., Deurveilher, S., Currie, R. W., Fawcett, J. P., and Semba, K. (2014). Increases in mature brain-derived neurotrophic factor protein in the frontal cortex and basal forebrain during chronic sleep restriction in rats: possible role in initiating allostatic adaptation. Neuroscience 277, 174–183.
| Increases in mature brain-derived neurotrophic factor protein in the frontal cortex and basal forebrain during chronic sleep restriction in rats: possible role in initiating allostatic adaptation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1Oqsr7N&md5=fd30bf41088298c93d1703126b05269eCAS | 25010399PubMed |
Weibel, E. R. (1963). Principles and methods for the morphometric study of the lung and other organs. Lab. Invest. 12, 131–155.
| 1:STN:280:DyaF387ptFequw%3D%3D&md5=32961ac29d7118292464e255cfdbf87cCAS | 13999512PubMed |
Wright, J. R., Rumbaugh, R. C., Colby, H. D., and Miles, P. R. (1979). The relationship between chemiluminescence and lipid peroxidation in rat hepatic microsomes. Arch. Biochem. Biophys. 192, 344–351.
| The relationship between chemiluminescence and lipid peroxidation in rat hepatic microsomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXhsVOisL8%3D&md5=574481177be3511d9d8b8c148dafed12CAS |
Yasenkov, R., and Deboer, T. (2012). Circadian modulation of sleep in rodents. In ‘Progress in Brains Research. The Neurobiology of Circadian Timing’. (Eds A. Kalsbeek, M. Merrow, T. Roenneberg and R. G. Foster.) pp. 203–218. (Elsevier: Oxford)
Zager, A., and Andersen, M. L. (2007). Effects of acute and chronic sleep loss on immune modulation of rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R504–R509.
| 1:CAS:528:DC%2BD2sXovVygsLw%3D&md5=e80f6f0c6370b391002ceff452fe1e36CAS | 17409265PubMed |
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.
| Melatonin ameliorates cognitive impairment induced by sleep deprivation in rats: role of oxidative stress, BDNF and CaMKII.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsleis77I&md5=ad08c1a51615241883525ee641415f2dCAS | 23933144PubMed |
Zimiani, K., Guarnier, F. A., Miranda, H. C., Watanabe, M. A. E., and Cecchini, R. (2005). Nitric oxide mediated oxidative stress injury in rat skeletal muscle subjected to ischemia/reperfusion as evaluated by chemiluminescence. Nitric Oxide 13, 196–203.
| Nitric oxide mediated oxidative stress injury in rat skeletal muscle subjected to ischemia/reperfusion as evaluated by chemiluminescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFWhtLvK&md5=b9768e20ece14fedff56bb6eb706828eCAS | 16125423PubMed |