{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,17]],"date-time":"2026-03-17T18:48:17Z","timestamp":1773773297358,"version":"3.50.1"},"reference-count":50,"publisher":"Elsevier BV","issue":"11","license":[{"start":{"date-parts":[[2003,11,1]],"date-time":"2003-11-01T00:00:00Z","timestamp":1067644800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2023,2,10]],"date-time":"2023-02-10T00:00:00Z","timestamp":1675987200000},"content-version":"vor","delay-in-days":7041,"URL":"http:\/\/www.elsevier.com\/open-access\/userlicense\/1.0\/"}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["The Journal of Nutrition"],"published-print":{"date-parts":[[2003,11]]},"DOI":"10.1093\/jn\/133.11.3361","type":"journal-article","created":{"date-parts":[[2018,1,22]],"date-time":"2018-01-22T06:22:23Z","timestamp":1516602143000},"page":"3361-3368","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":22,"title":["Increased Rat Brain Cytochrome C Correlates with Degree of Perinatal Copper Deficiency Rather than Apoptosis"],"prefix":"10.1016","volume":"133","author":[{"given":"Anna A.","family":"Gybina","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Joseph R.","family":"Prohaska","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"78","reference":[{"key":"10.1093\/jn\/133.11.3361_bib1","doi-asserted-by":"crossref","first-page":"6842","DOI":"10.1073\/pnas.111058698","article-title":"Essential role for mammalian copper transporter Ctr1 in copper homeostasis and embryonic development","volume":"98","author":"Lee","year":"2001","journal-title":"Proc. Natl. Acad. Sci. U.S.A"},{"key":"10.1093\/jn\/133.11.3361_bib2","doi-asserted-by":"crossref","first-page":"6836","DOI":"10.1073\/pnas.111057298","article-title":"The copper transporter CTR1 provides an essential function in mammalian embryonic development","volume":"98","author":"Kuo","year":"2001","journal-title":"Proc. Natl. Acad. Sci. U.S.A"},{"key":"10.1093\/jn\/133.11.3361_bib3","doi-asserted-by":"crossref","first-page":"6848","DOI":"10.1073\/pnas.111058498","article-title":"The metallochaperone Atox1 plays a critical role in perinatal copper homeostasis","volume":"98","author":"Hamza","year":"2001","journal-title":"Proc. Natl. Acad. Sci. U.S.A"},{"key":"10.1093\/jn\/133.11.3361_bib4","doi-asserted-by":"crossref","first-page":"1022S","DOI":"10.1093\/ajcn\/67.5.1022S","article-title":"Menkes syndrome and animal models","volume":"67","author":"Mercer","year":"1998","journal-title":"Am. J. Clin. Nutr"},{"key":"10.1093\/jn\/133.11.3361_bib5","unstructured":"Smith, R. M. (1983) Copper and the developing brain. In: Neurobiology of the Trace Elements (Dreosti, I. E. & Smith, R. M., eds.), pp. 1\u201340. Humana Press, Clifton, New Jersey."},{"key":"10.1093\/jn\/133.11.3361_bib6","doi-asserted-by":"crossref","unstructured":"O\u2019Dell, B. L. & Prohaska, J. R. (1983) Biochemical aspects of copper deficiency in the nervous system. In: Neurobiology of the Trace Elements (Dreosti, I. E. & Smith, R. M., eds.), pp. 41\u201381. Humana Press, Clifton N J.","DOI":"10.1385\/0-89603-046-6:41"},{"key":"10.1093\/jn\/133.11.3361_bib7","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1093\/jn\/97.1.42","article-title":"Neural lesions in the offspring of female rats fed a copper-deficient diet","volume":"97","author":"Carlton","year":"1969","journal-title":"J. Nutr"},{"key":"10.1093\/jn\/133.11.3361_bib8","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1016\/0955-2863(90)90080-5","article-title":"Biochemical changes in copper deficiency","volume":"1","author":"Prohaska","year":"1990","journal-title":"J. Nutr. Biochem"},{"key":"10.1093\/jn\/133.11.3361_bib9","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1111\/j.1471-4159.1975.tb06956.x","article-title":"Copper deficiency in the developing rat brain: evidence for abnormal mitochondria","volume":"25","author":"Prohaska","year":"1975","journal-title":"J. Neurochem"},{"key":"10.1093\/jn\/133.11.3361_bib10","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1016\/S0306-4522(00)00562-5","article-title":"Neurodegeneration in the animal model of Menkes' disease involves Bcl-2-linked apoptosis","volume":"103","author":"Rossi","year":"2001","journal-title":"Neuroscience"},{"key":"10.1093\/jn\/133.11.3361_bib11","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1007\/BF00691800","article-title":"Neuronal degeneration in the brain of the brindled mouse. An ultrastructural study of the cerebral cortical neurons","volume":"45","author":"Yajima","year":"1979","journal-title":"Acta. Neuropathol"},{"key":"10.1093\/jn\/133.11.3361_bib12","doi-asserted-by":"crossref","first-page":"1031","DOI":"10.1038\/sj.cdd.4401088","article-title":"The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet","volume":"9","author":"van Loo","year":"2002","journal-title":"Cell Death Differ"},{"key":"10.1093\/jn\/133.11.3361_bib13","first-page":"2922","article-title":"The expanding role of mitochondria in apoptosis","volume":"15","author":"Wang","year":"2001","journal-title":"Genes Dev"},{"key":"10.1093\/jn\/133.11.3361_bib14","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1083\/jcb.144.2.281","article-title":"Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner","volume":"144","author":"Slee","year":"1999","journal-title":"J. Cell Biol"},{"key":"10.1093\/jn\/133.11.3361_bib15","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1038\/35048069","article-title":"Breaking the mitochondrial barrier","volume":"2","author":"Martinou","year":"2001","journal-title":"Nat. Rev. Mol. Cell. Biol"},{"key":"10.1093\/jn\/133.11.3361_bib16","doi-asserted-by":"crossref","first-page":"1340","DOI":"10.1093\/jn\/107.7.1340","article-title":"Report of the AIN Ad Hoc Committee on standards for nutritional studies","volume":"107","year":"1977","journal-title":"J. Nutr"},{"key":"10.1093\/jn\/133.11.3361_bib17","doi-asserted-by":"crossref","first-page":"1726","DOI":"10.1093\/jn\/110.8.1726","article-title":"Second report of the AIN Ad Hoc Committee on standards for nutritional studies","volume":"110","year":"1980","journal-title":"J. Nutr"},{"key":"10.1093\/jn\/133.11.3361_bib18","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1016\/0003-2697(78)90586-9","article-title":"A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples","volume":"87","author":"Markwell","year":"1978","journal-title":"Anal. Biochem"},{"key":"10.1093\/jn\/133.11.3361_bib19","doi-asserted-by":"crossref","first-page":"2048","DOI":"10.1093\/jn\/113.10.2048","article-title":"Changes in tissue growth, concentrations of copper, iron, cytochrome oxidase and superoxide dismutase subsequent to dietary or genetic copper deficiency in mice","volume":"113","author":"Prohaska","year":"1983","journal-title":"J. Nutr"},{"key":"10.1093\/jn\/133.11.3361_bib20","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1177\/153537020122600307","article-title":"Dietary copper deficiency alters protein levels of rat dopamine beta-monooxygenase and tyrosine monooxygenase","volume":"226","author":"Prohaska","year":"2001","journal-title":"Exp. Biol. Med"},{"key":"10.1093\/jn\/133.11.3361_bib21","doi-asserted-by":"crossref","first-page":"422","DOI":"10.1046\/j.1471-4159.1999.0720422.x","article-title":"The copper chaperone CCS is abundant in neurons and astrocytes in human and rodent brain","volume":"72","author":"Rothstein","year":"1999","journal-title":"J. Neurochem"},{"key":"10.1093\/jn\/133.11.3361_bib22","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1093\/jn\/133.1.28","article-title":"Copper deficiency induces the upregulation of the copper chaperone for Cu\/Zn superoxide dismutase in weanling male rats","volume":"133","author":"Bertinato","year":"2003","journal-title":"J. Nutr"},{"key":"10.1093\/jn\/133.11.3361_bib23","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1016\/S0003-9861(03)00364-3","article-title":"Metallochaperone for Cu, Zn-superoxide dismutase (CCS) protein but not mRNA is higher in organs from copper-deficient mice and rats","volume":"417","author":"Prohaska","year":"2003","journal-title":"Arch. Biochem. Biophys"},{"key":"10.1093\/jn\/133.11.3361_bib24","doi-asserted-by":"crossref","first-page":"50842","DOI":"10.1074\/jbc.M207622200","article-title":"Early mitochondrial activation and cytochrome c up-regulation during apoptosis","volume":"277","author":"Chandra","year":"2002","journal-title":"J. Biol. Chem"},{"key":"10.1093\/jn\/133.11.3361_bib25","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1093\/jn\/93.4.533","article-title":"Copper deficiency in the guinea pig","volume":"93","author":"Everson","year":"1967","journal-title":"J. Nutr"},{"key":"10.1093\/jn\/133.11.3361_bib26","doi-asserted-by":"crossref","first-page":"356","DOI":"10.1007\/s00401-001-0473-9","article-title":"Apoptosis in cerebrum of macular mutant mouse","volume":"103","author":"Ohno","year":"2002","journal-title":"Acta Neuropathol"},{"key":"10.1093\/jn\/133.11.3361_bib27","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1126\/science.8235590","article-title":"Programmed cell death and the control of cell survival: lessons from the nervous system","volume":"262","author":"Raff","year":"1993","journal-title":"Science"},{"key":"10.1093\/jn\/133.11.3361_bib28","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1111\/j.1471-4159.1974.tb06920.x","article-title":"Copper deficiency in the developing rat brain: a possible model for Menkes' steely-hair disease","volume":"23","author":"Prohaska","year":"1974","journal-title":"J. Neurochem"},{"key":"10.1093\/jn\/133.11.3361_bib29","doi-asserted-by":"crossref","unstructured":"Prohaska, J. R. (1981) Changes in Brain Enzymes Accompanying Deficiencies of the Trace Elements, Copper, Selenium, or Zinc. In: Trace Element Metabolism in Man and Animals (TEMA-4) (McC. Howell, J., Gawthorne, J. M. & White, C. L., eds.), pp. 275\u2013282. Australian Academy of Science, Canberra.","DOI":"10.1007\/978-3-642-68269-8_69"},{"key":"10.1093\/jn\/133.11.3361_bib30","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1038\/labinvest.3780078","article-title":"Metallothionein inhibits myocardial apoptosis in copper-deficient mice: role of atrial natriuretic peptide","volume":"80","author":"Kang","year":"2000","journal-title":"Lab. Invest"},{"key":"10.1093\/jn\/133.11.3361_bib31","first-page":"H2313","article-title":"Overexpression of Bcl-2 attenuates apoptosis and protects against myocardial I\/R injury in transgenic mice","volume":"280","author":"Chen","year":"2001","journal-title":"Am. J. Physiol"},{"key":"10.1093\/jn\/133.11.3361_bib32","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1038\/icb.1973.15","article-title":"Copper deficiency in the rat. Effect on the ultrastructure of hepatocytes","volume":"51","author":"Gallagher","year":"1973","journal-title":"Aust. J. Exp. Biol. Med. Sci"},{"key":"10.1093\/jn\/133.11.3361_bib33","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1203\/00006450-197005000-00003","article-title":"Cardiac hypertrophy in rats with iron and copper deficiency: quantitative contribution of mitochondrial enlargement","volume":"4","author":"Goodman","year":"1970","journal-title":"Pediatr. Res"},{"key":"10.1093\/jn\/133.11.3361_bib34","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1093\/jn\/121.6.815","article-title":"Myofibrillar, mitochondrial and valvular morphological alterations in cardiac hypertrophy among copper-deficient rats","volume":"121","author":"Medeiros","year":"1991","journal-title":"J. Nutr"},{"key":"10.1093\/jn\/133.11.3361_bib35","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1016\/0300-9629(93)90024-X","article-title":"Cardiac nucleotide levels and mitochondrial respiration in copper-deficient rats","volume":"104","author":"Chao","year":"1993","journal-title":"Comp. Biochem. Physiol"},{"key":"10.1093\/jn\/133.11.3361_bib36","doi-asserted-by":"crossref","first-page":"936","DOI":"10.1093\/jn\/115.7.936","article-title":"Adenine nucleotide and lactate levels in organs from copper-deficient mice and brindled mice","volume":"115","author":"Rusinko","year":"1985","journal-title":"J. Nutr"},{"key":"10.1093\/jn\/133.11.3361_bib37","doi-asserted-by":"crossref","first-page":"13134","DOI":"10.1074\/jbc.275.17.13134","article-title":"Sequential serum-dependent activation of CREB and NRF-1 leads to enhanced mitochondrial respiration through the induction of cytochrome c","volume":"275","author":"Herzig","year":"2000","journal-title":"J. Biol. Chem"},{"key":"10.1093\/jn\/133.11.3361_bib38","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1016\/S0891-5849(00)00303-8","article-title":"In vivo control of respiration by cytochrome c oxidase in human cells","volume":"29","author":"Villani","year":"2000","journal-title":"Free Radic. Biol. Med"},{"key":"10.1093\/jn\/133.11.3361_bib39","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1385\/BTER:83:1:57","article-title":"Nuclear respiratory factors 1 and 2 are upregulated in hearts from copper-deficient rats","volume":"83","author":"Mao","year":"2001","journal-title":"Biol. Trace Elem. Res"},{"key":"10.1093\/jn\/133.11.3361_bib40","doi-asserted-by":"crossref","first-page":"896","DOI":"10.1095\/biolreprod.102.009167","article-title":"Copper-deficient rat embryos are characterized by low superoxide dismutase activity and elevated superoxide anions","volume":"68","author":"Hawk","year":"2003","journal-title":"Biol. Reprod"},{"key":"10.1093\/jn\/133.11.3361_bib41","first-page":"134","article-title":"Effects of copper deficiency on carbon tetrachloride-induced lipid peroxidation","volume":"109","author":"Lawrence","year":"1987","journal-title":"J. Lab. Clin. Med"},{"key":"10.1093\/jn\/133.11.3361_bib42","doi-asserted-by":"crossref","first-page":"3597","DOI":"10.1523\/JNEUROSCI.23-09-03597.2003","article-title":"Sp1 and Sp3 are oxidative stress-inducible, antideath transcription factors in cortical neurons","volume":"23","author":"Ryu","year":"2003","journal-title":"J. Neurosci"},{"key":"10.1093\/jn\/133.11.3361_bib43","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/S0014-5793(98)00061-1","article-title":"Cytochrome c in the apoptotic and antioxidant cascades","volume":"423","author":"Skulachev","year":"1998","journal-title":"FEBS. Lett"},{"key":"10.1093\/jn\/133.11.3361_bib44","doi-asserted-by":"crossref","first-page":"37159","DOI":"10.1074\/jbc.M002361200","article-title":"Cytochrome c is released from mitochondria in a reactive oxygen species (ROS)-dependent fashion and can operate as a ROS scavenger and as a respiratory substrate in cerebellar neurons undergoing excitotoxic death","volume":"275","author":"Atlante","year":"2000","journal-title":"J. Biol. Chem"},{"key":"10.1093\/jn\/133.11.3361_bib45","doi-asserted-by":"crossref","first-page":"2356","DOI":"10.1074\/jbc.M209681200","article-title":"Effect of cytochrome c on the generation and elimination of O2\u2212 and H2O2 in mitochondria","volume":"278","author":"Zhao","year":"2003","journal-title":"J. Biol. Chem"},{"key":"10.1093\/jn\/133.11.3361_bib46","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/0955-2863(95)00036-Y","article-title":"Persistent neurochemical changes following perinatal copper deficiency in rats","volume":"6","author":"Prohaska","year":"1995","journal-title":"J. Nutr. Biochem"},{"key":"10.1093\/jn\/133.11.3361_bib47","doi-asserted-by":"crossref","first-page":"618","DOI":"10.1093\/jn\/126.3.618","article-title":"Auditory startle response is diminished in rats after recovery from perinatal copper deficiency","volume":"126","author":"Prohaska","year":"1996","journal-title":"J. Nutr"},{"key":"10.1093\/jn\/133.11.3361_bib48","doi-asserted-by":"crossref","first-page":"1551","DOI":"10.1046\/j.1471-4159.1994.63041551.x","article-title":"Regional specificity in alterations of rat brain copper and catecholamines following perinatal copper deficiency","volume":"63","author":"Prohaska","year":"1994","journal-title":"J. Neurochem"},{"key":"10.1093\/jn\/133.11.3361_bib49","doi-asserted-by":"crossref","first-page":"1447","DOI":"10.1093\/jn\/125.6.1447","article-title":"Copper deficiency alters rat peptidylglycine alpha-amidating monooxygenase activity","volume":"125","author":"Prohaska","year":"1995","journal-title":"J. Nutr"},{"key":"10.1093\/jn\/133.11.3361_bib50","first-page":"41","article-title":"Intact rat brain mitochondria from a single animal: Preparation and properties","volume":"2","author":"Lee","year":"1993","journal-title":"Method Toxicol"}],"container-title":["The Journal of Nutrition"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0022316622162139?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0022316622162139?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/academic.oup.com\/jn\/article-pdf\/133\/11\/3361\/24017594\/4w1103003361.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,6,29]],"date-time":"2025-06-29T23:18:37Z","timestamp":1751239117000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0022316622162139"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2003,11]]},"references-count":50,"journal-issue":{"issue":"11","published-print":{"date-parts":[[2003,11]]}},"alternative-id":["S0022316622162139"],"URL":"https:\/\/doi.org\/10.1093\/jn\/133.11.3361","relation":{},"ISSN":["0022-3166"],"issn-type":[{"value":"0022-3166","type":"print"}],"subject":[],"published":{"date-parts":[[2003,11]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Increased Rat Brain Cytochrome C Correlates with Degree of Perinatal Copper Deficiency Rather than Apoptosis","name":"articletitle","label":"Article Title"},{"value":"The Journal of Nutrition","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1093\/jn\/133.11.3361","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"Copyright \u00a9 2003 American Society for Nutrition. Published by Elsevier Inc. All rights reserved.","name":"copyright","label":"Copyright"}]}}