Skip to main content Accessibility help
×
Home
Hostname: page-component-5bf98f6d76-m4xc2 Total loading time: 0.287 Render date: 2021-04-20T21:10:11.640Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": false, "newCiteModal": false, "newCitedByModal": true }

Effects of vitamin A deficiency on mitochondrial function in rat liver and heart

Published online by Cambridge University Press:  09 March 2007

Ernesto Estornell
Affiliation:
Department de Bioquímica Biologia Molecular, Facultat de Farmàcia, Universitat de València, Spain
José R. Tormo
Affiliation:
Department de Bioquímica Biologia Molecular, Facultat de Farmàcia, Universitat de València, Spain
Pilar Marín
Affiliation:
Department de Bioquímica Biologia Molecular, Facultat de Farmàcia, Universitat de València, Spain
Jaime Renau-Piqueras
Affiliation:
Centro de Investigación, Hospital La Fé, València, Spain
Joaquín Timoneda
Affiliation:
Department de Bioquímica Biologia Molecular, Facultat de Farmàcia, Universitat de València, Spain
Teresa Barber
Affiliation:
Department de Bioquímica Biologia Molecular, Facultat de Farmàcia, Universitat de València, Spain
Corresponding
E-mail address:
Rights & Permissions[Opens in a new window]

Abstract

The aim of this study was to investigate comparative effects of vitamin A deficiency on respiratory activity and structural integrity in liver and heart mitochondria. Male rats were fed a liquid control diet (control rats) or a liquid vitamin A-deficient diet (vitamin A-deficient rats) for 50 days. One group of vitamin-A deficient rats was refed a control diet for 15 days (vitamin A-recovered rats). To assess the respiratory function of mitochondria the contents of coenzyme Q (ubiquinone, CoQ), cytochrome c and the activities of the whole electron transport chain and of each of its respiratory complexes were evaluated. Chronic vitamin A deficiency promoted a significant increase in the endogenous coenzyme Q content in liver and heart mitochondria when compared with control values. Vitamin A deficiency induced a decrease in the activity of complex I (NADH–CoQ reductase) and complex II (succinate–CoQ reductase) and in the levels of complex I and cytochrome c in heart mitochondria. However, NADH and succinate oxidation rates were maintained at the control levels due to an increase in the CoQ content in accordance with the kinetic behaviour of CoQ as an homogeneous pool. On the contrary, the high CoQ content did not affect the electron-transfer rate in liver mitochondria, whose integrity was preserved from the deleterious effects of the vitamin A deficiency. Ultrastuctural assessment of liver and heart showed that vitamin A deficiency did not induce appreciable alterations in the morphology of their mitochondria. After refeeding the control diet, serum retinol, liver and heart CoQ content and the activity of complex I and complex II in heart mitochondria returned to normality. However, the activities of both whole electron transfer chain and complex I in liver were increased over the control values. The interrelationships between physiological antioxidants in biological membranes and the beneficial effects of their administration in mitochondrial diseases are discussed.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2000

References

Akmal, KM, Dufour, JM, Vo, M, Higginson, S & Kim, KH (1998) Ligand dependent regulation of retinoic acid receptor alpha in rat testis:. in vivo response to depletion and repletion of vitamin A. Endocrinology 139, 12391248.CrossRefGoogle ScholarPubMed
Barber, T, Triguero, A, Martínez-López, I, Torres, L, García, C, Miralles, VJ & Viña, JR (1999) Elevated expression of liver gamma-cystathionase is required for the maintenance of lactation in rats. Journal of Nutrition 129, 928933.Google ScholarPubMed
Barua, AB & Olson, JA (1998) Reversed-phase gradient high-performance liquid chromatographic procedure for simultaneous analysis of very polar to nonpolar retinoids, carotenoids and tocopherols in animals and plant samples. Journal of Chromatography B 707, 6979.CrossRefGoogle ScholarPubMed
Burton (1994) Vitamin E: molecular and biological function. Proceedings of the Nutrition Society 53, 251262.CrossRefGoogle ScholarPubMed
Ciaccio, M, Valenza, M, Tesoriere, L, Bongiorno, A, Albiero, R & Livrea, L (1993) Vitamin A inhibits doxorubicin-induced membrane lipid peroxidation in rat tissues. in vivo. Archives of Biochemistry and Biophysics 302, 103108.CrossRefGoogle ScholarPubMed
Cooper, JM, Petty, RKH, Hayes, DJ, Morgan-Hughes, JA & Clark, JB (1988) Chronic administration of the oral hypoglycaemic agent diphenyleneiodonium to rats. An animal model of impaired oxidative phosphorylation (mitochondrial myopathy). Biochemical Pharmacology 37, 687694.CrossRefGoogle Scholar
Degli Esposti, M & Lenaz, G (1982) Kinetics of ubiquinol-1-cytochrome c reductase in bovine heart mitochondria and submitochondrial particles. Biochimica et Biophysica Acta 682, 189200.CrossRefGoogle ScholarPubMed
Estornell, E, Fato, R, Castelluccio, C, Cavazzoni, M, Parenti Castelli, G & Lenaz, G (1992) Saturation kinetics of coenzyme Q in NADH and succinate oxidation in beef heart mitochondria. FEBS Letters 311, 107109.CrossRefGoogle ScholarPubMed
Estornell, E, Fato, R, Pallotti, F & Lenaz, G (1993) Assay conditions for the mitochondrial NADH:coenzyme Q oxidoreductase. FEBS Letters 332, 127131.CrossRefGoogle ScholarPubMed
Estornell, E, Barber, T & Cabo, J (1994) Improved nitrogen metabolism in rats fed on lipid-rich liquid diets. British Journal of Nutrition 71, 361373.CrossRefGoogle ScholarPubMed
Estornell, E, Tormo, JR & Barber, T (1997) A deficiency in respiratory complex I in heart mitochondria from vitamin A-deficient rats is counteracted by an increase in coenzyme Q. Biochemical and Biophysical Research Communications 233, 451454.CrossRefGoogle ScholarPubMed
Evarts, RP, Hu, Z, Omori, N, Omori, M, Marsden, ER & Thogeirsson, SS (1995) Effect of vitamin A deficiency on the integrity of hepatocytes after partial hepatectomy. American Journal of Pathology 147, 699706.Google ScholarPubMed
Genova, ML, Castelluccio, C, Fato, R, Parenti Castelli, G, Merlo Pich, M, Formiggini, G, Bovina, C, Marchetti, M & Lenaz, G (1995) Major changes in complex I activity in mitochondria from aged rats may not be detected by direct assay of NADH:coenzyme Q reductase. Biochemical Journal 311, 105109.CrossRefGoogle Scholar
Green, DR & Reed, JC (1998) Mitochondria and apoptosis. Science 281, 13091312.CrossRefGoogle ScholarPubMed
Johnson, D & Lardy, H (1967) Isolation of liver or kidney mitochondria. Methods in Enzymology 10, 9496.CrossRefGoogle Scholar
Krahenbuhl, S & Reichen, J (1992) Adaptation of mitochondrial metabolism in liver cirrhosis. Different strategies to maintain a vital function. Scandinavian Journal of Gastroenterology 193, 9096.CrossRefGoogle ScholarPubMed
Kröger, A (1978) Determination of contents and redox states of ubiquinone and menaquinone. Methods in Enzymology 53, 579591.CrossRefGoogle ScholarPubMed
Lea, RG, Riley, SC, Antipatis, C, Hannah, L, Ashworth, CJ, Clark, DA & Critchley, HO (1999) Cytokines and the regulation of apoptosis in reproductive tissues: a review. American Journal of Reproductive Immunology 42, 100109.Google ScholarPubMed
Lenaz, G, Fato, R, Genova, ML, Formiggini, G, Parenti Castelli, G & Bovina, C (1995) Underevaluation of complex I activity by the direct assay of NADH–coenzyme Q reductase in rat liver mitochondria. FEBS Letters 366, 119121.CrossRefGoogle ScholarPubMed
Lenaz, G, Bovina, C, Castelluccio, C, Cavazzoni, M, Estornell, E, Fato, R, Huertas, JR, Merlo-Pich, M, Pallotti, F, Parenti Castelli, G & Rauchova, H (1995) Modes of coenzyme Q function in electron transfer. Protoplasma 184, 5062.CrossRefGoogle Scholar
Leo, MA, Sato, M & Lieber, CS (1983) Effect of hepatic vitamin A depletion on the liver in humans and rats. Gastroenterology 84, 562572.Google ScholarPubMed
Liu, X, Kim, CN, Yang, J, Jemmerson, R & Wang, X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86, 147157.CrossRefGoogle ScholarPubMed
Livrea, MA & Tesoriere, L (1998) Antioxidant activity of vitamin A within lipid environments. In Subcellular Biochemistry, pp. 113143 [Quinn, PJ and Kagan, VE, editors]. New York: Plenum Press.Google Scholar
Maden, M, Gale, E & Zile, M (1998) The role of vitamin A in the development of the central nervous system. Journal of Nutrition 128, 471S475S.Google ScholarPubMed
Morimoto, T, Jikkoh, A, Yokoo, N, Taki, Y, Tanaka, J, Kamiyama, Y, Ozawa, K & Tobe, T (1985) Changes in coenzyme Q level in mitochondria of cirrhotic rat liver. Life Sciences 36, 15771580.CrossRefGoogle ScholarPubMed
Morre, DM, Morre, DJ & Walter, M (1981) Vitamin A effects on hepatic Golgi apparatus architecture. European Journal of Cellular Biology 25, 2835.Google ScholarPubMed
Nicholls, P (1976) Catalytic activity of cytochromes c and c 1 in mitochondria and submitochondrial particles. Biochimica et Biophysica Acta 430, 3045.CrossRefGoogle ScholarPubMed
Packer, L & Landvik, S (1990) Vitamin E in biological systems. Advances in Experimental Medicine and Biology 264, 93103.CrossRefGoogle ScholarPubMed
Palace, VP, Khaper, N, Qin, Q & Singal, PK (1999) Antioxidant potentials of vitamin A and carotenoids and their relevance to heart disease. Free Radical Biology and Medicine 26, 746761.CrossRefGoogle ScholarPubMed
Pasatiempo, AM, Taylor, CE & Ross, AC (1991) Vitamin A status and the immune response to pneumococcal polysaccharide: effects of age and early stages of retinol deficiency in rats. Journal of Nutrition 121, 556562.Google ScholarPubMed
Reeves, PG, Nielsen, FH & Fahey, GC (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing Committee on the reformulation of the AIN-76 rodent diet. Journal of Nutrition 123, 19391953.Google Scholar
Ross, AC (1992) Vitamin A status: relationship to immunity and the antibody response. Proceedings of the Society for Experimental Biology and Medicine 200, 303320.CrossRefGoogle ScholarPubMed
Sancho-Tello, M, Renau-Piqueras, J, Báguena-Cervellera, R & Guerri, C (1987) A biochemical and stereological study of neonatal rat hepatocyte subpopulations. Effect of pre- and postnatal exposure to ethanol. Virchows Archives of Biology and Cellular Pathology 54, 170181.CrossRefGoogle Scholar
Schapira, AHV (1998) Human complex I defects in neurodegenerative diseases. Biochimica et Biophysica Acta 1364, 261270.CrossRefGoogle ScholarPubMed
Selvaraj, RJ & Susheela, TP (1970) Estimation of serum vitamin A by a microfluorometric procedure. Clinica Chimica Acta 27, 165170.CrossRefGoogle ScholarPubMed
Semba, RD (1994) Vitamin A, immunity, and infection. Clinical Infectious Diseases 19, 489499.CrossRefGoogle Scholar
Semba, RD (1999) Vitamin A and immunity to viral, bacterial and protozoan infections. Proceedings of the Nutrition Society 58, 719727.CrossRefGoogle ScholarPubMed
Shi, H, Noguchi, N & Niki, E (1999) Comparative study on dynamics of antioxidative action of alpha-tocopherol hydroquinone, ubiquinol and alpha-tocopherol against lipid peroxidation. Free Radical Biology and Medicine 27, 334346.CrossRefGoogle ScholarPubMed
Smith, AL (1967) Preparation, properties and conditions for assay of mitochondria: slaughterhouse material, small scale. Methods in Enzymology 10, 8186.CrossRefGoogle Scholar
Tesoriere, L, Ciaccio, M, Bongiorno, A, Riccio, A, Pintaudi, AM & Livrea, MA (1993) Antioxidant activity of all-trans-retinol in homogeneous solution and in phosphatidylcholine liposomes. Archives of Biochemistry and Biophysics 307, 217223.CrossRefGoogle ScholarPubMed
Thomas, PK, Cooper, JM, King, RH, Workman, JM, Schapira, AHV, Goss-Sampson, MA & Muller, DPR (1993) Myopathy in vitamin E deficient rats: muscle fibre necrosis associated with disturbances of mitochondrial function. Journal of Anatomy 183, 451461.Google ScholarPubMed
Traber, MG & Packer, L (1995) Vitamin E: beyond antioxidant function. American Journal of Clinical Nutrition 62, 1501S1509S.Google ScholarPubMed
Vanneste, VH (1966) Molecular proportion of the fixed cytochrome components of the respiratory chain of Keilin–Hartree particles and beef heart mitochondria. Biochimica et Biophysica Acta 113, 175178.CrossRefGoogle ScholarPubMed
Wallace, DC (1999) Mitochondrial diseases in man and mouse. Science 283, 14821488.CrossRefGoogle Scholar
Zile, M (1998) Vitamin A and embryonic development: an overview. Journal of Nutrition 128, 455S458S.Google ScholarPubMed

Full text views

Full text views reflects PDF downloads, PDFs sent to Google Drive, Dropbox and Kindle and HTML full text views.

Total number of HTML views: 0
Total number of PDF views: 181 *
View data table for this chart

* Views captured on Cambridge Core between September 2016 - 20th April 2021. This data will be updated every 24 hours.

You have Access

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Effects of vitamin A deficiency on mitochondrial function in rat liver and heart
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Effects of vitamin A deficiency on mitochondrial function in rat liver and heart
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Effects of vitamin A deficiency on mitochondrial function in rat liver and heart
Available formats
×
×

Reply to: Submit a response


Your details


Conflicting interests

Do you have any conflicting interests? *