Stoichiometric modeling of oxygen transportation through the surface of isolated perfused rat liver

K. V. Shadrin ; V. G. Pakhomova ; A. P. Rupenko ; O. V. Kryukova ; R. G. Khlebopros

Matematičeskaâ biologiâ i bioinformatika, Tome 11 (2016) no. 2, pp. 263-277.

Résumé

Stoichiometric modeling allows analyzing the features of metabolism both the cell populations and the holistic isolated organs. In this paper, one of the stoichiometric modeling methods, Flux Balance Analysis, was used to investigate the mechanisms of oxygen transportation through the surface of the isolated perfused rat liver at various oxygenation conditions. It is shown that the oxygen intake through the surface of the isolated perfused liver is associated with energy consumption.

Bibliographie

[1] Drozdov-Tikhomirov L. N., Serganova V. V., Skurida G. I., “Vnutrennie statsionarnye metabolicheskie potoki v multifermentnykh sistemakh: Sintez lizina iz atsetata produtsentom Corynobacterium glutamicum”, Biotekhnologiya, 2:8 (1986), 28–37

[2] Ivanov K. P., Kislyakov Yu. Ya., Energeticheskie potrebnosti i kislorodnoe obespechenie golovnogo mozga, Nauka, L., 1979, 212 pp.

[3] Inzhevatkin E. V., Nefedov V. P., Savchenko A. A., “Neirosetevaya prediktsiya potrebleniya kisloroda perfuziruemoi pechenyu krys po aktivnosti oksidoreduktaz v dinamike vosstanovitelnogo perioda posle gipertermicheskogo vozdeistviya”, Vestnik novykh meditsinskikh tekhnologii, 2000, no. 1, 25–28

[4] Kamiya N., Dvizhenie protoplazmy, IL, M., 1962, 306 pp.

[5] Lukyanova L. D., Balmukhanov B. S., Ugolev A. T., Kislorodzavisimye protsessy v kletke i ee funktsionalnoe sostoyanie, Nauka, M., 1981

[6] Nazipova N. N., Elkin Yu. E., Panyukov V. V., Drozdov-Tikhomirov L. N., “Raschet skorostei metabolicheskikh reaktsii v zhivoi kletke metodom balansa statsionarnykh metabolicheskikh potokov (metod BSMP)”, Matematicheskaya biologiya i bioinformatika, 2 (2007), 98–119 | DOI

[7] Nefedov V. P., Rupenko A. P., Valuk V. A., Panov A. V., Vavilin V. A., “Modifikatsiya deistviya adrenalina na metabolizm tkanei izolirovannoi pecheni krys pri perfuzii sredami razlichnogo sostava”, Uspekhi gepatologii, XV (1991), 335–352

[8] Nyuskholm E., Start K., Regulyatsiya metabolizma, Mir, M., 1977, 407 pp.

[9] Remmel N. N., Kratasyuk V. A., Maznyak O. M., Inzhevatkin E. V., Nefedov V. P., “Biolyuminestsentnyi kontrol intensivnosti patologicheskikh okislitelnykh protsessov v kletkakh perfuziruemoi pecheni krys posle gipertermicheskogo vozdeistviya”, Byulleten eksperimentalnoi biologii i meditsiny, 135:1 (2003), 52–54

[10] Rupenko A. P., Kruglik O. V., Morgulis I. I., “Snabzhenie pecheni kislorodom v usloviyakh izolirovannoi perfuzii”, Doklady Akademii nauk, 418:1 (2008), 128–130

[11] Ugolev A. M., Evolyutsiya pischevareniya i printsipy evolyutsii funktsii. Elementy sovremennogo funktsionalizma, Nauka, L., 1985

[12] Arai K., Lee K., Berthiaume F., Tompkins R. G., Yarmush M. L., “Intrahepatic amino acid and glucose metabolism in a D-galactosamine-induced rat liver failure model”, Hepatology, 34 (2001), 360–371 | DOI

[13] Banta S., Vemula M., Yokoyama T., Jayaraman A., Berthiaume F., Yarmush M. L., “Contribution of gene expression to metabolic fluxes in hypermetabolic livers induced through burn injury and cecal ligation and puncture in rats”, Biotechnol. Bioeng., 97 (2007), 118–137 | DOI

[14] Banta S., Yokoyama T., Berthiaume F., Yarmush M. L., “Effects of dehydroepiandrosterone administration on rat hepatic metabolism following thermal injury”, J. Surg. Res., 127 (2005), 93–105 | DOI

[15] Calvetti D., Kuceyeski A., Somersalo E., “Sampling-based analysis of a spatially distributed model for liver metabolism at steady state”, Multiscale Modeling Simulation, 7:1 (2008), 407–431 | DOI | MR | Zbl

[16] Chalhoub E., Hanson R. W., Belovich J. M., “A computer model of gluconeogenesis and lipid metabolism in the perfused liver”, Am. J. Physiol. Endocrinol. Metab., 293 (2007), E1676–E1686 | DOI

[17] Chalhoub E., Xie L., Balasubramanian V., Kim J., Belovich J., “A distributed model of carbohydrate transport and metabolism in the liver during rest and high-intensity exercise”, Ann. Biomed. Eng., 35 (2007), 474–491 | DOI

[18] Coulter N. A., “Filtration coefficient of capillaries of the brain”, American Journal of Physiology, 195 (1958), 459–464

[19] Kauffman K. J., Prakash P., Edwards J. S., “Advances in flux balance analysis”, Current Opinion in Biotechnology, 14:5 (2003), 491–496 | DOI

[20] Lee K., Berthiaume F., Stephanopoulos G. N., Yarmush D. M., Yarmush M. L., “Metabolic flux analysis of postburn hepatic hypermetabolism”, Metab. Eng., 2 (2000), 312–327 | DOI

[21] Metallo C. M., Walther J. L., Stephanopoulos G., “Evaluation of $^{13}$C isotopic tracers for metabolic flux analysis in mammalian cells”, J. Biotechnol., 144:3 (2009), 167–174 | DOI

[22] Orman M. A., Androulakis I. P., Berthiaume F., Ierapetritou M. G., “Metabolic network analysis of perfused livers under fed and fasted states: Incorporating thermodynamic and futile-cycle associated regulatory constraints”, Journal of Theoretical Biology, 293 (2012), 101–110 | DOI | Zbl

[23] Orman M. A., Arai K., Yarmush M. L., Androulakis I. P., Berthiaume F., Ierapetritou M. G., “Metabolic flux determination in perfused livers by mass balance analysis: Effect of fasting”, Biotechnol. Bioeng., 107 (2010), 825–835 | DOI

[24] Orman M. A., Berthiaume F., Androulakis I. P., Ierapetritou M. G., “Pathway analysis of liver metabolism under stressed condition”, Journal of Theoretical Biology, 272:1 (2011), 131–140 | DOI | MR

[25] Orman M. A., Ierapetritou M. G., Androulakis I. P., Berthiaume F., “Metabolic response of perfused livers to various oxygenation conditions”, Biotechnol. Bioeng., 108 (2011), 2947–2957 | DOI

[26] Ramakrishna R., Edwards J. S., McCulloch A., Palsson B. O., “Flux balance analysis of mitochondrial energy metabolism: consequences of systemic stoichiometric constraints”, American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 280 (2001), R695–R704

[27] Raman K., Chandra N., “Flux balance analysis of biological systems: applications and challenges”, Briefings in Bioinformatics, 10:4 (2009), 435–449 | DOI

[28] Salem J. E., Saidel G. M., Stanley W. C., Cabrera M. E., “Mechanistic Model of Myocardial Energy Metabolism under Normal and Ischemic Conditions”, Annals of Biomedical Engineering, 30:2 (2002), 202–216 | DOI

[29] Sengupta N., Rose S. T., Morgan J. A., “Metabolic flux analysis of CHO cell metabolism in the late non-growth phase”, Biotechnol. Bioeng., 108:1 (2011), 82–92 | DOI

[30] Sharma N. S., Ierapetritou M. G., Yarmush M. L., “Novel quantitative tools for engineering analysis of hepatocyte cultures in bioartificial liver systems”, Biotechnol. Bioeng., 92 (2005), 321–335 | DOI

[31] Stokes A. N., Rapid oxygen entry into unperfused tissue slices: an experimental artefact?, Journal of Theoretical Biology, 60:2 (1976), 473–475 | DOI

[32] Tekir S. D., Cakir T., Ulgen K. O., “Analysis of enzymopathies in the human red blood cells by constraint-based stoichiometric modeling approaches”, Comp. Biol. Chem., 30:5 (2006), 327–338 | DOI | MR | Zbl

[33] Uygun K., Matthew H. W. T., Huang Y., “Investigation of metabolic objectives in cultured hepatocytes”, Biotechnol. Bioeng., 97 (2007), 622–637 | DOI

[34] Varma A., Boesch B. W., Palsson B. O., “Biochemical production capabilities of Escherichia coli”, Biotechnology and Bioengineering, 42:1 (1993), 59–73 | DOI

[35] Yamaguchi Y., Yu Y. M., Zupke C., Yarmush D. M., Berthiaume F., Tompkins R. G., Yarmush M. L., “Effect of burn injury on glucose and nitrogen metabolism in the liver: Preliminary studies in a perfused liver system”, Surgery, 121 (1997), 295–303 | DOI

[36] Yokoyama T., Banta S., Berthiaume F., Nagrath D., Tompkins R. G., Yarmush M. L., “Evolution of intrahepatic carbon, nitrogen, and energy metabolism in a D-galactosamine-induced rat liver failure model”, Metab. Eng., 7 (2005), 88–103 | DOI