Cited by 607Liver physiology and pathologyDrug-Induced Hepatotoxicity and ProtectionOrgan Transplantation Techniques and Outcomes

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Metabolic zonation of the liver: Regulation and implications for liver function

Gebhardt, Rolf·1992·Pharmacology & Therapeutics

DOI 10.1016/0163-7258(92)90055-5

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Abstract

Liver parenchyma shows a remarkable heterogeneity of the hepatocytes along the porto-central axis with respect to ultrastructure and enzyme activities resulting in different cellular functions within different zones of the liver lobuli. According to the concept of metabolic zonation, the spatial organization of the various metabolic pathways and functions forms the basis for the efficient adaptation of liver metabolism to the different nutritional requirements of the whole organism in different metabolic states. The present review summarizes current knowledge about this heterogeneity, its development and determination, as well as about its significance for the understanding of all aspects of liver function and pathology, especially of intermediary metabolism, biotransformation of drugs and zonal toxicity of hepatotoxins.

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Cell kinetics in the liver of rats under normal and abnormal dietary conditions
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Metabolism of cysteinyl leukotrienes in non‐recirculating rat liver perfusion
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Acinar zonation of cytosolic but not organelle-bound activities of phosphoenolpyruvate carboxykinase and aspartate aminotransferase in guinea-pig liver
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Microquantitative determination of the distribution patterns of alcohol dehydrogenase activity in the liver of rat, guinea-pig and horse
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Hepatic heme synthesis in a new model of experimental hemochromatosis: Studies in rats fed finely divided elemental iron
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Identification of G6PDH-active sinusoidal cells as Kupffer cells in the rat liver
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Histochemical and microbiochemical demonstration of reduced pyruvate kinase activity in thioacetamide-induced neoplastic nodules of rat liver
Klimek, F., Moore, M. A., Schneider, E., & Bannasch, P. (1988) · Histochemistry and Cell Biology · doi:10.1007/bf00495704 · Cited by 30
Effects of oxygen deficiency and calcium omission on carbon tetrachloride hepatotoxicity in isolated perfused livers from phenobarbital-pretreated rats
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Mechanism of the permissive action of dexamethasone on the glucagon‐dependent activation of the phosphoenolpyruvate carboxykinase gene in cultured rat hepatocytes
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Net prostaglandin release by perfused rat liver after stimulation with phorbol 12-myristate 13-acetate
Tran-Thi, T. A., Gyufko, K., Häussinger, D., & Decker, K. (1988) · Journal of Hepatology · doi:10.1016/s0168-8278(88)80026-6 · Cited by 30
Pathologic changes in the cytokeratin pericanalicular sheath in experimental cholestasis and alcoholic fatty liver.
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Intralobular heterogeneity of carbon tetrachloride-induced oxidative stress in perfused rat liver visualized by digital imaging fluorescence microscopy.
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Hormonal control of specific gene expression in the rat liver during the suckling-weaning transition
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In situ kinetic parameters of glucose-6-phosphate dehydrogenase and phosphogluconate dehydrogenase in different areas of the rat liver acinus
Jonges, G. N., & Noorden, C. J. F. V. (1989) · The Histochemical Journal · doi:10.1007/bf01753359 · Cited by 29
Immunohistochemical determination of inducibility phenotype with a monoclonal antibody to a methylcholanthrene-inducible isozyme of cytochrome P-450.
Anderson, L. M., Ward, J. M., Park, S. S., Jones, A. B., Junker, J., Gelboin, H. V., & Rice, J. M. (1987) · PubMed · Cited by 29
Urea‐Cycle Enzymes in Normal Liver and in Patients with Alcoholic Hepatitis
Maier, K., Volk, B., Hoppe-Seyler, G., & Gerok, W. (1974) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.1974.tb00391.x · Cited by 29
The oxidation of acrolein by rat liver aldehyde dehydrogenases. Relation to allyl alcohol hepatotoxicity.
Rikans, L. E. (1987) · Drug Metabolism and Disposition · doi:10.1016/s0090-9556(25)06708-x · Cited by 28
Quantitative histochemical resolution of the oxidation-reduction and phosphate potentials within the simple hepatic acinus.
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Liver Structure and Innervation
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Heterogeneous Distribution of ATP Citrate Lyase in Rat‐Liver Parenchyma
Katz, N. R., FISCHER, W., & Ick, M. (1983) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1983.tb07151.x · Cited by 28
Multiple requirements for glycogen synthesis by hepatocytes isolated from fasted rats.
Chen, K. S., & Lardy, H. A. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)38625-8 · Cited by 28
Differences in the half‐lives of some mitochondrial rat liver enzymes may derive partially from hepatocyte heterogeneity
Várgas, J. L., Roche, E., Knecht, E., & Grisolı́a, S. (1987) · FEBS Letters · doi:10.1016/0014-5793(87)80444-1 · Cited by 28
Immunohistochemical localisation of arginase in human liver using monoclonal antibodies against human liver arginase
Multhaupt, H. A. B., Fritz, P., & Schumacher, K. R. (1987) · Histochemistry and Cell Biology · doi:10.1007/bf00496818 · Cited by 28
Multihormonal control of enzyme clusters in rat liver ontogenesis I. Effects of adrenalectomy and gonadectomy
Lamers, W. H., & Mooren, P. G. (1981) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(81)90009-9 · Cited by 28
A quantitative histochemical study of 5′-nucleotidase activity in rat liver using the lead salt method and polyvinyl alcohol
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In vivo demonstration by radioautography of binding sites for insulin in liver, kidney, and calcified tissues of the rat
Martineau‐Doizé, B., McKee, M. D., Warshawsky, H., & Bergeron, J. J. M. (1986) · The Anatomical Record · doi:10.1002/ar.1092140205 · Cited by 28
A random arrangement of albumin‐containing hepatocytes seen with histo‐immunologic methods. II. Conditions that produce the artifact
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Effects of dietary lipid and phenobarbitone on the distribution and concentration of cytochrome P‐450 in the liver studied by quantitative cytochemistry
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Detection of mRNAs present at low concentrations in rat liver by in situ hybridization: application to the study of metabolic regulation and azo dye hepatocarcinogenesis.
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Liver Microsomal β-Glucuronidase and UDP-GIucuronyltransferase
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Localization of liver fatty acid-binding protein and its mRNA in the liver and jejunum of rats: an immunohistochemical and in situ hybridization study
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Induction of glutamine synthetase and transient co-expression with carbamoylphosphate synthetase in hepatocytes transplanted into fat pads of syngeneic hosts
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Hepatic Clearance of Human Growth Hormone1
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Variations in the intralobular distribution of copper in the livers of copper-loaded rats in relation to the pathogenesis of copper storage diseases
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Albumin influences sulfobromophthalein transport by hepatocytes of each acinar zone
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Long-Term Effects of Dietary Polychlorinated Biphenyl and High Level of Vitamin E on Ascorbic Acid and Lipid Metabolism in Rats
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Induction of P-450IIB genes within the rat liver acinus is not dependent on the chemical inducer or on the acinar organization
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Covalent Binding of Oxidative Biotransformation Intermediates Is Associated with Halothane Hepatotoxicity in Guinea Pigs
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Possible Growth Hormone Control of Liver Glutamine Synthetase Activity in Rats*
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Greater taurodeoxycholate biotransformation during backward perfusion of rat liver
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Correlations between hemodynamic parameters of the liver and norepinephrine release upon hepatic nerve stimulation in the dog
Yamaguchi, N., & Garceau, D. (1980) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y80-204 · Cited by 25
Zonal Signal Heterogeneity and Induction of Hepatocyte Heterogeneity
Jungermann, K. A. (1986) · Springer eBooks · doi:10.1007/978-1-4684-5041-5_16 · Cited by 25
The zonation of liver and the distribution of fructose 2,6-bisphosphate in rat liver.
Wals, P. A., Palacı́n, M., & Katz, J. J. (1988) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)68867-2 · Cited by 25
Distribution of epidermal growth factor binding sites in the adult rat liver
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The heterogeneity of hepatocytes during the postnatal development of the mouse
Kanamura, S., & Asada‐Kubota, M. (1980) · Anatomy and Embryology · doi:10.1007/bf00315902 · Cited by 25
Allyl alcohol cytotoxicity and glutathione depletion in isolated periportal and perivenous rat hepatocytes
Penttilä, K. E. (1988) · Chemico-Biological Interactions · doi:10.1016/0009-2797(88)90048-8 · Cited by 25
Ethylated fluoresceins: Assay of cytochrome P-450 activity and application to measurements in single cells by flow cytometry
Miller, A. D. (1983) · Analytical Biochemistry · doi:10.1016/0003-2697(83)90220-8 · Cited by 25
Functional hepatocellular heterogeneity determined by the hepatotoxins allyl alcohol and bromobenzene in immature and adult Fischer 344 rats
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Differential induction profile of drug-metabolizing enzymes after treatment with hypolipidaemic agents
Fournel‐Gigleux, S., Magdalou, J., Pinon, P., & Siest, G. (1987) · Xenobiotica · doi:10.3109/00498258709043951 · Cited by 25
Bile salt transport after selective damage to acinar zone 3 hepatocytes by bromobenzene in the rat
Gumucio, J. J., Katz, M. E., Miller, D. L., Balabaud, C. P., Greenfield, J. M., & Wagner, R. M. (1979) · Toxicology and Applied Pharmacology · doi:10.1016/0041-008x(79)90494-0 · Cited by 25
Characterisation of Hepatocyte Sub‐populations Generated by Centrifugal Elutriation
Sumner, I. G., Freedman, R. B., & Lodola, A. (1983) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1983.tb07600.x · Cited by 25
Heterogeneous lobular distribution of hepatocytes expressing acute-phase genes during the acute inflammatory reaction.
Bernuau, D., Legrès, L., Lamri, Y., Giuily, N., Fey, G. H., & Feldmann, G. (1989) · The Journal of Experimental Medicine · doi:10.1084/jem.170.1.349 · Cited by 25
Alteration in the Capacities as well as in the Zonal and Cellular Distributions of Pyruvate Kinase L and M2 in Regenerating Rat Liver
Chatzipanagiotou, S., Nath, A., Vogt, B., & Jungermann, K. A. (1985) · Biological Chemistry Hoppe-Seyler · doi:10.1515/bchm3.1985.366.1.271 · Cited by 25
Perinatal development of the distributions of phosphoenolpyruvate carboxykinase and succinate dehydrogenase in rat liver parenchyma.
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Zonal hepatic function: solute-hepatocyte interactions within the liver acinus.
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The diagnostic significance of periportal hepatic necrosis and inflammation
BAPTISTA, A., Bianchi, L., de Groote, J., Desmet, V. J., Ishak, K. G., Korb, G., MacSween, R. N. M., Pópper, H., Poulsen, H. H., Scheuer, P. J., et al. (1988) · Histopathology · doi:10.1111/j.1365-2559.1988.tb01982.x · Cited by 24
Sex specific regional differences in hepatic glucokinase activity
Teutsch, H. F., & Lowry, O. H. (1982) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(82)91143-3 · Cited by 24
Genetic regulation of NADPH supply in perfused mouse liver. Role of the Ah locus during induction by 3-methylcholanthrene.
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Glycogen synthesis via the indirect gluconeogenic pathway in the periportal and via the direct glucose utilizing pathway in the perivenous zone of perfused rat liver
Bartels, H., Vogt, B., & Jungermann, K. A. (1988) · Histochemistry and Cell Biology · doi:10.1007/bf00493149 · Cited by 24
Age and Gender Influence Halothane-Associated Hepatotoxicity in Strain 13 Guinea Pigs
Lind, R. C., Gandolfi, A. J., & Hall, P. D. L. Μ. (1989) · Anesthesiology · doi:10.1097/00000542-198912000-00011 · Cited by 24
Fatty acid metabolism in hepatocytes cultured with hypolipidaemic drugs. Role of carnitine
Gerondaes, P., Alberti, K. G. M. M., & Agius, L. (1988) · Biochemical Journal · doi:10.1042/bj2530161 · Cited by 24
Heterogeneous acinar localization of the asialoglycoprotein internalization system in rat hepatocytes
van der Sluijs, P., Braakman, I., Meijer, D. K. F., & Groothuis, G. M. M. (1988) · Hepatology · doi:10.1002/hep.1840080609 · Cited by 24
Selective loss of hormonal induction of glutamate transport in primary cultures of hepatocytes from rats treated with CCl4
Gebhardt, R., & Burger, H.-J. (1987) · Journal of Hepatology · doi:10.1016/s0168-8278(87)80549-4 · Cited by 24
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Quantitative immunohistochemistry: a comparison of microdensitometric analysis of unlabeled antibody peroxidase-antiperoxidase staining and of microfluorometric analysis of indirect fluorescent antibody staining for nicotinamide adenosine dinucleotide phosphate (NADPH)-cytochrome c (P-450) reductase in rat liver.
Smith, M. T., Redick, J. A., & Baron, J. (1983) · Journal of Histochemistry & Cytochemistry · doi:10.1177/31.10.6411804 · Cited by 24
Acinar redistribution and heterogeneity in transport of the organic cation rhodamine B in rat liver
Braakman, I., Groothuis, G. M., & Meijer, D. K. F. (1987) · Hepatology · doi:10.1002/hep.1840070510 · Cited by 24
Control by pH of urea synthesis in isolated rat hepatocytes
Boon, L., & Meijer, A. J. (1988) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1988.tb13911.x · Cited by 24
Distributions of monooxygenase components and epoxide hydratase within the livers of untreated male rats
Redick, A. J., Kawabata, I. T., Guengerich, F. P., Krieter, P. A., Shires, T. K., & Baron, J. (1980) · Life Sciences · doi:10.1016/0024-3205(80)90523-8 · Cited by 24
Changes in the sensitivity of lipogenesis in rat hepatocytes to hormones and precursors over the diurnal cycle and during longer-term starvation of donor animals.
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An Immunohistochemical Study on the Localization and Distribution of Epoxide Hydrolase within Livers of Untreated Rats
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Localization of halothane-induced antigen in situ by specific anti-halothane metabolite antibodies.
Hubbard, A. K., Roth, T. P., Schuman, S. S., & Gandolfi, A. J. (1989) · PubMed Central · Cited by 23
Urea synthesis from ammonia in periportal and pericentral regions of the liver lobule
Kari, F. W., Yoshihara, H., & Thurman, R. G. (1987) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1987.tb10728.x · Cited by 23
Drug metabolism by periportal and perivenous rat hepatocytes
Suolinna, E.-M., Penttilä, K. E., Winell, B.-M., Sjöholm, A.-C., & Lindros, K. O. (1989) · Biochemical Pharmacology · doi:10.1016/0006-2952(89)90340-7 · Cited by 23
PHOSPHORUS POISONING
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Gluconeogenic-glycolytic capacities and metabolic zonation in liver of rats with streptozotocin, non-ketotic as compared to alloxan, ketotic diabetes
Miethke, H., WITTIG, B., Nath, A., & Jungermann, K. A. (1986) · Histochemistry and Cell Biology · doi:10.1007/bf00508430 · Cited by 23
The application of quantitative cytochemistry to study the acinar distribution of enzymatic activities in human liver biopsy sections
Sokal, E. M., Trivedi, P., Cheeseman, P., Portmann, B. C., & Mowat, A. P. (1989) · Journal of Hepatology · doi:10.1016/0168-8278(89)90074-3 · Cited by 23
Three-dimensional structure of endothelial cells in hepatic sinusoids of the rat as revealed by the Golgi method
Wake, K., Motomatsu, K., Dan, C., & Kaneda, K. (1988) · Cell and Tissue Research · doi:10.1007/bf00219747 · Cited by 23
Bromobenzene-induced zonal necrosis in the hepatic acinus
Miller, D. L., Harasin, J. M., & Gumcio, J. J. (1978) · Experimental and Molecular Pathology · doi:10.1016/0014-4800(78)90078-3 · Cited by 23
Hepatobiliary transport of drugs: do periportal and perivenous hepatocytes perform the same job?
Groothuis, G. M. M., Hardonk, M. J., & Meijer, D. K. F. (1985) · Trends in Pharmacological Sciences · doi:10.1016/0165-6147(85)90151-8 · Cited by 23
Zonal redox changes as a cause of selective perivenular hepatotoxicity of alcohol
Baraona, E., Jauhonen, P., Miyakawa, H., & Lieber, C. S. (1983) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(83)90216-2 · Cited by 23
Transferrin Receptor Expression in Rat Liver: Immunohistochemical and Biochemical Analysis of the Effect of Age and Iron Storage
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Cytochrome p-450 gene expression in the functional units of the fetal liver
José Chianale, B., Dvorak, C., Farmer, D. L., Michaels, L., & Gumucio, J. J. (1988) · Hepatology · doi:10.1002/hep.1840080222 · Cited by 23
Diurnal rhythms of hepatic carbohydrate metabolism during development of the rat
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Acute toxicological experiment of T-2 toxin in rabbits.
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Hydrolysis of organic sulfates in periportal and pericentral regions of the liver lobule: studies with 4-methylumbelliferyl sulfate in the perfused rat liver.
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Glucuronidation of 7-hydroxycoumarin in periportal and pericentral regions of the lobule in livers from untreated and 3-methylcholanthrene-treated rats.
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Hepatic necrosis following halothane anesthesia in goats
O’Brien, T. D., Raffe, M. R., Cox, V. S., Stevens, D. L., & O'Leary, T. P. (1986) · Journal of the American Veterinary Medical Association · doi:10.2460/javma.1986.189.12.1591 · Cited by 23
Induction of phosphoenolpyruvate carboxykinase by sympathetic agents in primary cultures of adult rat hepatocytes
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New Micromethods for Studying Sublobular Structure and Function in the Isolated, Perfused Rat Liver
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Regulation of hepatic metabolism by extracellular nucleotides and eicosanoids
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Immunohistochemical localization of human liver glutathione S-transferase (GST) isozymes with special reference to polymorphic GST1
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Hepatic zonation of drug metabolizing enzymes. Studies on hepatocytes isolated from the periportal or perivenous region of the liver acinus
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Quantitative histochemical assessment of regional differences in hepatic glucose uptake and release
Teutsch, H. F. (1985) · Histochemistry and Cell Biology · doi:10.1007/bf00708200 · Cited by 22
Hepatocytes explanted in the spleen preferentially express carbamoylphosphate synthetase rather than glutamine synthetase
Lamers, W. H., Been, W., Charles, R., & Moorman, A. F. M. (1990) · Hepatology · doi:10.1002/hep.1840120414 · Cited by 22
Effect of 16,16-dimethyl prostaglandin E2 on oxygen uptake and microcirculation in the perfused rat liver
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Microquantitative analysis of the intra-acinar profiles of glutamate dehydrogenase in rat liver.
Maly, I. P., & Sasse, D. (1991) · Journal of Histochemistry & Cytochemistry · doi:10.1177/39.8.1856459 · Cited by 22
Changes in the acinar distribution of some enzymes involved in carbohydrate metabolism in rat liver parenchyma after experimentally induced cholestasis
Noorden, C. J. F. V., Frederiks, W. M., Aronson, D. C., Marx, F., Bosch, K. S., Jonges, G. N., Vogels, I. M. C., & James, J. (1986) · Virchows Archiv B Cell Pathology Including Molecular Pathology · doi:10.1007/bf02889989 · Cited by 22
Cytochrome P-450 localization in normal human adult and foetal liver by immunocytochemistry using a monoclonal antibody against human cytochrome P—450
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Authors: Gebhardt, R.
Affiliations: University of Tübingen (DE)
Corresponding author: Gebhardt, Rolf
Venue: Pharmacology & Therapeutics
Publisher: Elsevier BV
Published: 1992-01
Volume: 53
Issue: 3
Pages: 275-354
ISSN: 0163-7258 (ISSN-L)
DOI: 10.1016/0163-7258(92)90055-5
OpenAlex: W2061717797
Cited by: 607
References: 880
Citations by year: 2026: 17 · 2025: 23 · 2024: 16 · 2023: 30 · 2022: 22 · 2021: 31 · 2020: 33 · 2019: 30 · 2018: 29 · 2017: 19 · 2016: 18 · 2015: 15 · 2014: 19 · 2013: 21 · 2012: 15
FWCI: 3.78
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Pharmacology & Therapeutics (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Hepatology › Liver physiology and pathology
Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Pharmacology › Drug-Induced Hepatotoxicity and Protection
Health Sciences › Medicine › Surgery › Organ Transplantation Techniques and Outcomes
Keywords: metabolic zonation, liver lobule, hepatocyte heterogeneity, intermediary metabolism, drug metabolism, hepatotoxins, liver function, liver pathology
MeSH terms: Animals, Humans, Liver

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Metabolic zonation of the liver: Regulation and implications for liver function

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