The rate of oxygen utilization by cells

Free Radical Biology and Medicine

Volumn 51, Issue 3, 2011, Pages 700-712

  Wagner, Brett A ^a   Venkataraman, Sujatha ^a   Buettner, Garry R ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Cell culture; Cell volume; Free radicals; Oxygen uptake

Indexed keywords

CELL PROTEIN; OXYGEN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ALLOMETRY; ANIMAL CELL; ARTICLE; CANCER CELL; CELL CULTURE; CELL FUNCTION; CELL VOLUME; COMBUSTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; OSMOLARITY; OXIDATION REDUCTION REACTION; OXYGEN CONSUMPTION; OXYGEN TISSUE LEVEL; OXYGENATION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT;

ANIMALS; CELL CULTURE TECHNIQUES; CELL GROWTH PROCESSES; CELL SIZE; ELECTROPHYSIOLOGY; ENERGY METABOLISM; HUMANS; NEOPLASMS; OXIDATION-REDUCTION; OXYGEN CONSUMPTION; PROTEIN BIOSYNTHESIS; REACTIVE OXYGEN SPECIES; REFERENCE VALUES; U937 CELLS;

MAMMALIA;

EID: 79959942853     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.05.024     Document Type: Article

References (107)

1. R.C. Weast CRC Handbook of Chemistry and Physics 1987 CRC Press Boca Raton
2. D.J. Wilkinson The contributions of Lavoisier, Scheele and Priestley to the early understanding of respiratory physiology in the eighteenth century Resuscitation 61 2004 249 255 (Pubitemid 38686880)
3. J.W. Severinghaus Fire-air and dephlogistication: revisionisms of oxygen's discovery Adv. Exp. Med. Biol. 543 2003 7 19 (Pubitemid 38183713)
4. C. Djerassi, and R. Hoffmann Oxygen: A Play in Two Acts 2001 Wiley-VCH Weinheim/New York
5. FAO/WHO/UNU Human energy requirements: report of a Joint FAO/WHO/UNU Expert Consultation FAO Food and Nutrition Technical Report Series 1 2004 United Nations University/World Health Organization/Food and Agriculture Organization of the United Nations Rome URL: http://www.fao.org/docrep/007/y5686e/y5686e00. htm#Contents Accessed 2011.06.08.
6. C. Allard, G. De Lamirande, and A. Cantero Mitochondrial population of mammalian cells. II. Variation in the mitochondrial population of the average rat liver cell during regeneration; use of the mitochondrion as a unit of measurement Cancer Res. 12 1952 580 583
7. M.P. Murphy How mitochondria produce reactive oxygen species Biochem. J. 417 2009 1 13
8. J. St-Pierre, J.A. Buckingham, S.J. Roebuck, and M. Brand Topology of superoxide production from different sites in the mitochondrial electron transport chain J. Biol. Chem. 277 2002 44784 44790 (Pubitemid 36159072)
9. A. Boveris, N. Oshino, and B. Chance The cellular production of hydrogen peroxide Biochem. J. 128 1972 617 630
10. J.F. Turrens, and A. Boveris Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria Biochem. J. 191 1980 421 427
11. A. Boveris, E. Cadenas, and A.O. Stoppani Role of ubiquinone in the mitochondrial generation of hydrogen peroxide Biochem. J. 156 1976 435 444
12. E. Cadenas, A. Boveris, C.I. Ragan, and A.O. Stoppani Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria Arch. Biochem. Biophys. 180 1977 248 257 (Pubitemid 8115490)
13. A. Boveris Mitochondrial production of superoxide radical and hydrogen peroxide Adv. Exp. Med. Biol. 78 1977 67 82
14. J.F. Turrens, A. Alexandre, and A.L. Lehninger Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria Arch. Biochem. Biophys. 237 1985 408 414 (Pubitemid 15144894)
15. A.M. James, R.A. Smith, and M.P. Murphy Antioxidant and prooxidant properties of mitochondrial coenzyme Q Arch. Biochem. Biophys. 423 2004 47 56 (Pubitemid 38198212)
16. J.F. Turrens Mitochondrial formation of reactive oxygen species J. Physiol. 552 2003 335 344 (Pubitemid 37321833)
17. J.M. McCord, and I. Fridovich Superoxide dismutase: an enzymic function for erythrocuprein (hemocuprein) J. Biol. Chem. 244 1969 6049 6055
18. S.G. Rhee Redox signaling: hydrogen peroxide as intracellular messenger Exp. Mol. Med. 31 1999 53 59 (Pubitemid 29326708)
19. L.W. Oberley, T.D. Oberley, and G.R. Buettner Cell division in normal and transformed cells: the possible role of superoxide dismutase and hydrogen peroxide Med. Hypotheses 7 1981 21 42 (Pubitemid 11127866)
20. T.S. Gechev, and J. Hille Hydrogen peroxide as a signal controlling plant programmed cell death J. Cell Biol. 168 2005 17 20 (Pubitemid 40111052)
21. R.P. Patel, D. Moellering, J. Murphy-Ullrich, H. Jo, J.S. Beckman, and V.M. Darley-Usmar Cell signaling by reactive nitrogen and oxygen species in atherosclerosis Free Radic. Biol. Med. 28 2000 1780 1794 (Pubitemid 30628665)
22. F.Q. Schafer, and G.R. Buettner Redox state of the cell as viewed through the glutathione disulfide/glutathione couple Free Radic. Biol. Med. 30 2001 1191 1212 (Pubitemid 32463931)
23. R.G. Allen, R.K. Newton, R.S. Sohal, G.L. Shipley, and C. Nations Alterations in superoxide dismutase, glutathione, and peroxides in the plasmodial slime mold Physarum polycephalum during differentiation J. Cell. Physiol. 125 1985 413 419 (Pubitemid 16200936)
24. S.S. Iyer, C.J. Accardi, T.R. Ziegler, R.A. Blanco, J.D. Ritzenthaler, M. Rojas, J. Roman, and D.P. Jones Cysteine redox potential determines pro-inflammatory IL-1beta levels PLoS One 4 2009 e5017
25. D.P. Jones Disruption of mitochondrial redox circuitry in oxidative stress Chem. Biol. Interact. 163 2006 38 53 (Pubitemid 44572221)
26. G.R. Buettner Superoxide dismutase in redox biology: the roles of superoxide and hydrogen peroxide Anticancer Agents Med. Chem. 11 2011 341 346
27. L.W. Oberley, and G.R. Buettner Role of superoxide dismutase in cancer: a review Cancer Res. 39 1979 1141 1149 (Pubitemid 9183825)
28. C.J. Weydert, T.A. Waugh, J.M. Ritchie, K.S. Lyer, J.L. Smith, L. Li, D.R. Spitz, and L.W. Oberley Overexpression of manganese or copper-zinc superoxide dismutase inhibits breast cancer growth Free Radic. Biol. Med. 41 2006 226 237 (Pubitemid 43928496)
29. M.E. Tome, D.B. Johnson, L.M. Rimsza, R.A. Roberts, T.M. Grogan, T.P. Miller, L.W. Oberley, and M.M. Briehl A redox signature score identifies diffuse large B-cell lymphoma patients with a poor prognosis Blood 106 2005 3594 3601 (Pubitemid 41609198)
30. L.W. Oberley Mechanism of the tumor suppressive effect of MnSOD overexpression Biomed. Pharmacother. 59 2005 143 148 (Pubitemid 40603325)
31. Y.S. Ho, M.S. Dey, and J.D. Crapo Antioxidant enzyme expression in rat lungs during hyperoxia Am. J. Physiol. 270 1996 L810 L818
32. D.A. Ferrick, A. Neilson, and C. Beeson Advances in measuring cellular bioenergetics using extracellular flux Drug Discov. Today 13 2008 268 274
33. A.A. Gerencser, A. Neilson, S.W. Choi, U. Edman, N. Yadava, R.J. Oh, D.A. Ferrick, D.G. Nicholls, and M.D. Brand Quantitative microplate-based respirometry with correction for oxygen diffusion Anal. Chem. 81 2009 6868 6878
34. D.G. Nicholls, V.M. Darley-Usmar, M. Wu, P.B. Jensen, G.W. Rogers, and D.A. Ferrick Bioenergetic profile experiment using C2C12 myoblast cells J. Vis. Exp. 46 2010 2511
35. M.B. Lees, and S. Paxman Modification of the Lowry procedure for the analysis of proteolipid protein Anal. Biochem. 47 1972 184 192
36. M. Wang, J.S. Kirk, S. Venkataraman, F.E. Domann, H.J. Zhang, F.Q. Schafer, S.W. Flanagan, C.J. Weydert, D.R. Spitz, G.R. Buettner, and L.W. Oberley Manganese superoxide dismutase suppresses hypoxic induction of hypoxia inducible factor-1α and vascular endothelial growth factor Oncogene 24 2005 8154 8166 (Pubitemid 41759814)
37. 2 in cells and thereby their biological state Free Radic. Biol. Med. 41 2006 1338 1350 (Pubitemid 44479829)
38. E.H. Sarsour, S. Venkataraman, A.L. Kalen, L.W. Oberley, and P.C. Goswami Manganese superoxide dismutase activity regulates transitions between quiescent and proliferative growth Aging Cell 7 2008 405 417 (Pubitemid 351663909)
39. E.H. Sarsour, M.G. Kumar, L. Chaudhuri, A.L. Kalen, and P.C. Goswami Redox control of the cell cycle in health and disease Antioxid. Redox Signal. 11 2009 2985 3011
40. S. Miriyala, A.K. Holley, and D.K. St Clair Mitochondrial superoxide dismutase-signals of distinction Anticancer Agents Med. Chem. 11 2011 181 190
41. N. Hempel, P.M. Carrico, and J.A. Melendez Manganese superoxide dismutase (Sod2) and redox-control of signaling events that drive metastasis Anticancer Agents Med. Chem. 11 2011 191 201
42. A.K. Holley, S.K. Dhar, and D.K. St Clair Manganese superoxide dismutase versus p53: the mitochondrial center Ann. N. Y. Acad. Sci. 1201 2010 72 78
43. G. Froese The respiration of ascites tumour cells at low oxygen concentrations Biochim. Biophys. Acta 57 1962 509 519
44. D.F. Wilson, M. Erecińska, C. Drown, and I.A. Silver The oxygen dependence of cellular energy metabolism Arch. Biochem. Biophys. 195 1979 485 493 (Pubitemid 9235081)
45. J.W. Boag Cell respiration as a function of oxygen tension Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 18 1970 475 478
46. I.S. Longmuir Respiration rate of rat-liver cells at low oxygen concentrations Biochem. J. 65 1957 378 382
47. 2 uptake by Chinese hamster ovary cells during the cell cycle Proc. Natl. Acad. Sci. USA 79 1982 1166 1170 (Pubitemid 12105568)
48. R.J. Fleischaker, and A.J. Sinskey Oxygen demand and supply in cell culture Eur. J. Appl. Microbiol. Biotechnol. 12 1981 193 197 (Pubitemid 11025442)
49. m for oxygen of cytochrome oxidase with turnover under de-energized and energized conditions Biochem. Soc. Trans. 24 1996 464s (Pubitemid 26306459)
50. U.J. Balis, K. Behnia, and B. Dwarakanath Oxygen consumption characteristics of porcine hepatocytes Metab. Eng. 1 1999 49 62 (Pubitemid 129499371)
51. B. Foy, A. Rotem, M. Toner, R.G. Tompkins, and M.L. Yarmush A device to measure the oxygen uptake rates of attached cells: importance in bioartificial organ design Cell Transplant. 3 1994 515 527 (Pubitemid 24372212)
52. B.G. Hill, B.P. Dranka, L. Zou, J.C. Chatham, and V.M. Darley-Usmar Importance of the bioenergetic reserve capacity in response to cardiomyocyte stress induced by 4-hydroxynonenal Biochem. J. 424 2009 99 107
53. J.G. Corasanti, D. Gleeson, and J.L. Boyer Effects of osmotic stresses on isolated rat hepatocytes. I. Ionic mechanisms of cell volume regulation Am. J. Physiol. 258 Gastrointest. Liver Physiol. 21 1990 G290 G298
54. A. Bredel-Geissler, U. Karbach, S. Walenta, L. Vollrath, and W. Mueller-Klieser Proliferation-associated oxygen consumption and morphology of tumor cells in monolayer and spheroid culture J. Cell. Physiol. 153 1992 44 52
55. H.E. Kubitschek, and J.A. Friske Determination of bacterial cell volume with the Coulter counter J. Bacteriol. 168 1986 1466 1467 (Pubitemid 17226844)
56. H.E. Kubitschek Cell volume increase in Escherichia coli after shifts to richer media J. Bacteriol. 172 1990 94 101 (Pubitemid 20016819)
57. C.B. Tyson, P.G. Lord, and A.E. Wheals Dependency of size of Saccharomyces cerevisiae cells on growth rate J. Bacteriol. 138 1979 92 98 (Pubitemid 9165543)
58. J.A. Child, J. King, T.H. Newman, and R.L. Waterfield A diffraction method for measuring the average volumes and shapes of red blood cells Br. J. Haematol. 13 1967 364 375
59. H.P. Ting-Beall, D. Needham, and R.M. Hochmuth Volume and osmotic properties of human neutrophils Blood 81 1993 2774 2780 (Pubitemid 23147586)
60. M.P. Gamcsik, K.K. Millis, and O.M. Colvin Noninvasive detection of elevated glutathione levels in MCF-7 cells resistant to 4- hydroperoxycyclophosphamide Cancer Res. 55 1995 2012 2016
61. 2 gradients across biomembranes FEBS Lett. 475 2000 121 126 (Pubitemid 30365063)
62. J.B. Leikin, and F.P. Paloucek Poisoning and Toxicology Handbook 2007 Informa Healthcare London 1049
63. C. Hwang, and A. Sinskey The role of oxidation-reduction potential in monitoring growth of cultured mammalian cells R.E. Spire, J.B. Griffiths, B. Meignier, Production of Biologicals from Animal Cells in Culture 1991 Butterworth-Heinemann Oxford 548 569
64. C.R. Jonas, T.R. Ziegler, L.H. Gu, and D.P. Jones Extracellular thiol/disulfide redox state affects proliferation rate in a human colon carcinoma (Caco2) cell line Free Radic. Biol. Med. 33 2002 1499 1506 (Pubitemid 35351593)
65. C.L. Anderson, S.S. Iyer, T.R. Ziegler, and D.P. Jones Control of extracellular cysteine/cystine redox state by HT-29 cells is independent of cellular glutathione Am. J. Physiol. Regul. Integr. Comp. Physiol. 293 2007 R1069 R1075
66. K. Bedard, and K.H. Krause The Nox family of ROS-generating NADPH oxidases: physiology and pathophysiology Physiol. Rev. 87 2007 245 313 (Pubitemid 46209993)
67. J.H. Carpenter New measurements of oxygen solubility in pure and natural water Limnol. Oceanogr. 11 1966 264 277
68. C.N. Murray, and J.P. Riley The solubility of gases in distilled water and sea water-II. Oxygen Deep Sea Res. Oceanogr. Abstr. 16 1969 311 320
69. J. Robinson, and J.M. Cooper Method of determining oxygen concentrations in biological media suitable for calibration of the oxygen electrode Anal. Biochem. 33 1970 390 939
70. W.H. Koppenol, and J. Butler Energetics of interconversion reactions of oxyradicals Adv. Free Radic. Biol. Med. 1 1985 91 131 (Pubitemid 16122935)
71. R.D. Guarino, L.E. Dike, T.A. Haq, J.A. Rowley, J.B. Pitner, and M.R. Timmins Method for determining oxygen consumption rates of static cultures from microplate measurements of pericellular dissolved oxygen concentration Biotechnol. Bioeng. 86 2004 775 787 [Erratum in Biotechnol. Bioeng. 91:392; 2005] (Pubitemid 38745695)
72. P.M. Herst, and M.V. Berridge Cell surface oxygen consumption: a major contributor to cellular oxygen consumption in glycolytic cancer cell lines Biochim. Biophys. Acta 1767 2007 170 177 (Pubitemid 46282606)
73. P. Jorjani, and S.S. Ozturk Effects of cell density and temperature on oxygen consumption rate for different mammalian cell lines Biotechnol. Bioeng. 64 1999 349 356 (Pubitemid 29297388)
74. Y. Zhang, H.M. Zhang, Y. Shi, M. Lustgarten, Y. Li, W. Qi, B.X. Zhang, and H. Van Remmen Loss of manganese superoxide dismutase leads to abnormal growth and signal transduction in mouse embryonic fibroblasts Free Radic. Biol. Med. 49 2010 1255 1262
75. A.J. de Groof, M.M. te Lindert, M.M. van Dommelen, M. Wu, M. Willemse, A.L. Smift, M. Winer, F. Oerlemans, H. Pluk, J.A. Fransen, and B. Wieringa Increased OXPHOS activity precedes rise in glycolytic rate in H-RasV12/E1A transformed fibroblasts that develop a Warburg phenotype Mol. Cancer 8 2009 54
76. 2 respiration, reduced ATP utilization, and inducible fumarate respiration Am. J. Physiol. Cell Physiol. 295 2008 C29 C37
77. T. Delgado, P.A. Carroll, A.S. Punjabi, D. Margineantu, D.M. Hockenbery, and M. Lagunoff Induction of the Warburg effect by Kaposi's sarcoma herpesvirus is required for the maintenance of latently infected endothelial cells Proc. Natl. Acad. Sci. USA 107 2010 10696 10701
78. Y. Abe, T. Sakairi, H. Kajiyama, S. Shrivastav, C. Beeson, and J.B. Kopp Bioenergetic characterization of mouse podocytes Am. J. Physiol. Cell Physiol. 299 2010 C464 C476
79. J.A. Graves, K. Rothermund, T. Wang, W. Qian, B. Van Houten, and E.V. Prochownik Point mutations in c-Myc uncouple neoplastic transformation from multiple other phenotypes in rat fibroblasts PLoS One 5 2010 e13717
80. J.E. Telford, S.M. Kilbride, and G.P. Davey Complex I is rate-limiting for oxygen consumption in the nerve terminal J. Biol. Chem. 284 2009 9109 9114
81. B.S. Danes, M.M. Broadfoot, and J. Paul A comparative study of respiratory metabolism in cultured mammalian cell strains Exp. Cell Res. 30 1963 369 378
82. H.J. Phillips, and R.V. Andrews Instability of metabolic quotients obtained from tissue cultures Proc. Soc. Exp. Biol. Med. 103 1960 160 163
83. C. Giulivi, P. Hochstein, and K.J. Davies Hydrogen peroxide production by red blood cells Free Radic. Biol. Med. 16 1994 123 129
84. J.A. Santolucito, and E. Whitcomb Effect of paraoxon on erythrocyte metabolism as measured by oxygen uptake in vitro Br. J. Pharmacol. 42 1971 298 302
85. H.W. Katinger, W. Scheirer, and E. Kroemer Der Blasens iulenfermenter ftir die Massensus pensionskultur tierischer Zellen Chem. Ing. Tech. 50 1978 193 197
86. P.E. James, S.K. Jackson, O.Y. Grinberg, and H.M. Swartz The effects of endotoxin on oxygen consumption of various cell types in vitro: an EPR oximetry study Free Radic. Biol. Med. 18 1995 641 647
87. R.R. Deshpande, and E. Heinzle On-line oxygen uptake rate and culture viability measurement of animal cell culture using microplates with integrated oxygen sensors Biotechnol. Lett. 26 2004 763 767 (Pubitemid 38982883)
88. R. Motterlini, H. Kerger, C.J. Green, R.M. Winslow, and M. Intaglietta Depression of endothelial and smooth muscle cell oxygen consumption by endotoxin Am. J. Physiol. Heart Circ. Physiol. 275 1998 H776 H782
89. T. Yamada, J.J. Yang, N.V. Ricchiuti, and M.W. Seraydarian Oxygen consumption of mammalian myocardial cells in culture: measurements in beating cells attached to the substrate of the culture dish Anal. Biochem. 145 1985 302 307 (Pubitemid 15100959)
90. M. Wu, A. Neilson, A.L. Swift, R. Moran, J. Tamagnine, D. Parslow, S. Armistead, K. Lemire, J. Orrell, J. Teich, S. Chomicz, and D.A. Ferrick Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells Am. J. Physiol. Cell Physiol. 292 2007 C125 C136
91. A.H. Burns, and W.J. Reddy Amino acid stimulation of oxygen and substrate utilization by cardiac myocytes Am. J. Physiol. Endocrinol. Metab. 235 1978 E461 E466
92. 2 consumption in monolayer cell cultures Respir. Physiol. 100 1995 101 106
93. C.M. Chi, L.N. Frautschy, F.B. Cerra, and W.S. Hu A sensitive measurement of oxygen uptake rate using an optochemical sensor Biotechnol. Tech. 7 1993 99 104
94. D. von Heimburg, K. Hemmrich, S. Zachariah, H. Staiger, and N. Pallua Oxygen consumption in undifferentiated versus differentiated adipogenic mesenchymal precursor cells Respir. Physiol. Neurobiol. 146 2005 107 111
95. J. Reyes, L. Borriero, N. Tanphaichitr, A.R. Bellve, and D.J. Benos Energy metabolism of cultured TM4 cells and the action of gossypol Biol. Reprod. 34 1986 809 819 (Pubitemid 17190597)
96. M. Pignatelli, J. Sanchez-Rodriguez, A. Santos, and A. Perez-Castillo 15-Deoxy-delta-12,14-prostaglandin J2 induces programmed cell death of breast cancer cells by a pleiotropic mechanism Carcinogenesis 26 2005 81 92 (Pubitemid 40207702)
97. J. Shen, N. Khan, L.D. Lewis, R. Armand, O. Grinberg, E. Demidenko, and H. Swartz Oxygen consumption rates and oxygen concentration in Molt-4 cells and their mtDNA depleted mutants Biophys. J. 84 2003 1291 1298 (Pubitemid 36133450)
98. H.K. Kim, W.S. Park, S.H. Kang, M. Warda, N. Kim, J.H. Ko, Ael-B. Prince, and J. Han Mitochondrial alterations in human gastric carcinoma cell line Am. J. Physiol. Cell Physiol. 293 2007 C761 C771
99. C.A. Peng, and B.O. Palsson Determination of specific oxygen uptake rates in human hematopoietic cultures and implications for bioreactor design Ann. Biomed. Eng. 24 1996 373 381
100. N.I. zur Nieden, J.T. Cormier, D.E. Rancourt, and M.S. Kallos Embryonic stem cells remain highly pluripotent following long term expansion as aggregates in suspension bioreactors J. Biotechnol. 129 2007 421 432 (Pubitemid 46560150)
101. M.S. Kallos, and L.A. Behie Inoculation and growth conditions for high-cell density expansion of mammalian neural stem cells in suspension bioreactors Biotechnol. Bioeng. 63 1999 473 483 (Pubitemid 29157051)
102. A. Tanabe, Y. Kobayashi, and T. Usui Enhancement of human neutrophil oxygen consumption by chemotactic factors Experientia 39 1983 604 606 (Pubitemid 13053551)
103. R.A. Proctor Endotoxin in vitro interactions with human neutrophils: depression of chemiluminescence, oxygen consumption, superoxide production, and killing Infect. Immun. 25 1979 912 921 (Pubitemid 9251894)
104. T.C. Pithon Curi, M. Pires de Melo, R. Bentes de Azevedo, T.M.T. Zorn, and R. Curi Glutamine utilization by rat neutrophils: presence of phosphate-dependent glutaminase Am. J. Physiol. 273 1997 C1124 C1129
105. J.P. Freyer, E. Tustanoff, A.J. Franko, and R.M. Sutherland In situ oxygen consumption rates of cells in V-79 multicellular spheroids during growth J. Cell. Physiol. 118 1984 53 61 (Pubitemid 14184343)
106. F. Kallinowski, G. Tyler, W. Mueller-Klieser, and P. Vau-pel Growth-related changes of oxygen consumption rates of tumor cells grown in vitro and in vivo J. Cell. Physiol. 138 1989 183 191 (Pubitemid 19038686)
107. R.L. Buck New equations for computing vapor pressure and enhancement factor J. Appl. Meteorol. 20 1981 1527 1532