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Original Article

Pharmacokinetics and mechanisms of plasma removal of hemoglobin-based oxygen carriers

Pages 203-215 | Received 26 Apr 2015, Accepted 29 Apr 2015, Published online: 29 May 2015

References

  • Aird WC. 2007. Phenotypic heterogeneity of the endothelium I. Structure, function, and mechanisms. Circ Res. 100:158–173.
  • Alayash AI, Summers AG, Wood F, Jia Y. 2001. Effects of glutaraldehyde polymerization on oxygen transport and redox properties of bovine hemoglobin. Arch Biochem Biophys. 391:225–234.
  • Ames BN, Cathcart R, Schwiers E, Hochstein P. 1981. Uric acid provides an antioxidant defense in humans against oxidant- and radical-caused aging and cancer: A hypothesis. Proc Natl Acad Sci USA. 78:6858–6862.
  • Andersen JT, Pehrson R, Tolmachev V, Daba MB, Abrahmsén L, Ekblad C. 2011. Extending half-life by indirect targeting of the neonatal Fc receptor (FcRn) using a minimal albumin binding domain. J Biol Chem. 286:5234–5241.
  • Andersen JT, Sandlie I. 2009. The versatile MHC class I-related FcRn protects IgG and albumin from degradation: implications for development of new diagnostics and therapeutics. Drug Metab Pharmacokinet. 24:318–332.
  • Anderson PJ, Ning J, Biro GP. 1993. Clearance of differentially labelled infused hemoglobin and polymerized hemoglobin from dog plasma and accumulation in urine and selected tissues. In: Chang TMS, Ed. Blood substitutes and oxygen carriers. New York: Marcel Dekker, pp. 557–563.
  • Baek JH, Zhou Y, Harris DR, Schaer DJ, Palmer AF, Buehler PW. 2012. Down selection of polymerized bovine hemoglobins for use as oxygen releasing therapeutics in a guinea pig model. Toxicol Sci. 127:567–581.
  • Baker SL, Dodds EC. 1925. Obstruction of the renal tubules during the excretion of haemoglobin. Brit J Exp Path. 6:247–260.
  • Bakker JC, Berbers GA, Bleeker WK, den Boer PJ, Biessels PT. 1993. Preparation and characterization of crosslinked and polymerized hemoglobin solutions. In: Chang TMS, Ed. Blood substitutes and oxygen carriers. New York: Marcel Dekker, pp. 67–75.
  • Bakker JC, Bleeker WK, van der Plas J. 1986. Properties of hemoglobin interdimerically cross-linked with NFPLP. Prog Clin Biol. 211:49–55.
  • Benesch RE, Ikeda S, Benesch R. 1976. Reaction of haptoglobin with hemoglobin covalently cross-linked between the αβ dimers. J Biol Chem. 251:465–470.
  • Berbers GA, Bleeker WK, Stekkinger P, Agterberg J, Rigter G, Bakker JC. 1991. Biophysical characteristics of hemoglobin intramolecularly cross-linked and polymerized. J Lab Clin Med. 117:157–165.
  • Bissell DM, Hammaker L, Schmid R. 1972. Hemoglobin and erythrocyte catabolism in rat liver: The separate roles of parenchymal and sinusoidal cells. Blood. 40:812–822.
  • Bleeker WK, Berbers GAM, den Boer PJ, Agterberg J, Rigter G, Bakker JC. 1992. Effect of polymerization on clearance and degradation of free hemoglobin. Biomat Art Cells Immob Biotech. 20:747–750.
  • Bleeker WK, van der Plas J, Agterberg J, Rigter G, Bakker JC. 1986. Prolonged vascular retention of a hemoglobin solution modified by cross-linking with 2-nor-2-formylpyridoxal 5’-phosphate. J Lab Clin Med. 108:448–455.
  • Bleeker WK, van der Plas J, Feitsma RIJ, Agterberg J, Rigter G, De Vries-van Rossen A, et al. 1989. In vivo distribution and elimination of hemoglobin modified by intramolecular cross-linking with 2-nor-2-formylpyridoxal 5’-phosphate. J Lab Clin Med. 113:151–161.
  • Bleeker WK, Zappeij LM, den Boer PJ, Agterberg JA, Rigter GM, Bakker JC. 1995. Evaluation of the immunogenicity of polymerized hemoglobin solutions in a rabbit model. Artif Cells Blood Substit Immobil Biotechnol. 23:461–468.
  • Bonegio RG, Fuhro R, Ragno G, Valeri CR, Lieberthal W. 2006. A comparison of the acute hemodynamic and delayed effects of 50% exchange transfusion with two different cross-linked hemoglobin based oxygen carrying solutions and pentastarch. Artif Cells Blood Substit Immobil Biotechnol. 34:145–157.
  • Bonhard K, Boysen U. 1982. Preparation of coupled hemoglobin molecules. US Patent. 4336248.
  • Boretti FS, Baek JH, Palmer AF, Schaer DJ, Buehler PW. 2014. Modeling hemoglobin and hemoglobin:haptoglobin complex clearance in a non-rodent species-pharmacokinetic and therapeutic implications. Front Physiol. 5:385. Doi 10.3389/fphys.2014.00385. eCollection 2014.
  • Borvak J, Richardson J, Medesan C, Antohe F, Radu C, Simionescu M, et al. 1998. Functional expression of the MHC class I-related receptor, FcRn, in endothelial cells of mice. Int Immunol. 10:1289–1298.
  • Bouma JM. 1982. Some aspects of plasma protein metabolism as compared with intracellular protein breakdown. Acta Biol Med Ger. 41:53–60.
  • Brooks J. 1932. The oxidation of haemoglobin to methaemoglobin by oxygen. Proc R Soc London B. 109:35–50.
  • Brooks J. 1935. The oxidation of haemoglobin to methaemoglobin by oxygen II-the relation between the rate of oxidation and the partial pressure of oxygen. Proc R Soc London B. 118:560–577.
  • Bucci E, Razynska A, Kwansa H, Matheson-Urbaitis B, O’Hearne M, Ulatowski JA, Koehler RC. 1996. Production and characteristics of an infusible oxygen-carrying fluid based on hemoglobin intramolecularly cross-linked with sebacic acid. J Lab Clin Med. 128:146–153.
  • Buehler PW, D’Agnillo F, Hoffman V, Alayash AI. 2007. Effects of endogenous ascorbate on oxidation, oxygenation, and toxicokinetics of cell-free modified hemoglobin after exchange transfusion in rat and guinea pig. J Pharmacol Exp Ther. 323:49–60.
  • Buehler PW, Vallelian F, Mikolajczyk MG, Schoedon G, Schweizer T, Alayash AI, Schaer DJ. 2008. Structural stabilization in tetrameric or polymeric hemoglobin determines its interaction with endogenous antioxidant pathways. Antioxid Redox Signal. 10:1449–1462.
  • Buehler PW, Zhou Y, Cabrales P, Jia Y, Sun G, Harris DR, et al. 2010. Synthesis, biophysical properties and pharmacokinetics of ultrahigh molecular weight tense and relaxed state polymerized bovine hemoglobins. Biomaterials. 31:3723–3735.
  • Bunn HF, Esham WT, Bull RW. 1969. The renal handling of hemoglobin I. Glomerular filtration. J Exp Med. 129:909–924.
  • Bunn HF. 1967. Effect of sulfhydryl reagents on the binding of human hemoglobin to haptoglobin. J Lab Clin Med. 70:606–618.
  • Bunn HF. 1972. Erythrocyte destruction and hemoglobin catabolism. Semin Hematol. 9:3–17.
  • Burhop KE, Doyle MP. 2002. The development and preclinical testing of a second-generation recombinant hemoglobin solution, rHb2.0 for injection. In: Messmer K, Burhop KE, Hutter J, Eds. Microcirculatory effects of hemoglobin solutions. Basel: Karger, pp. 48–64.
  • Bush S, Marshall T, Spicuzza J, Nelson D. 1994. Diaspirin crosslinked hemoglobin (DCLHb): Bioanalytical studies in swine. Art Cells Blood Subs Immob Biotech. 22:917–922.
  • Carmichael FJL, Ali ACY, Campbell JA, Langlois SF, Biro GP, Willan AR, et al. 2000. A phase I study of oxidized raffinose cross-linked human hemoglobin. Crit Care Med. 28:2283–2292.
  • Caron A, Mayer JC, Menu P, Alayash A, Marie PY, Vigneron C. 2001. Measurement of blood volume after haemodilution with haemoglobin-based oxygen carriers by a radiolabelled-albumin method. Transfus Med. 11:433–442.
  • Caron A, Menu P, Faivre-Fiorina B, Labrude P, Alayash A, Vigneron C. 2000. Systemic and renal hemodynamics after moderate hemodilution with HBOCs in anesthetized rabbits. Am J Physiol Heart Circ Physiol. 278:H1974–1983.
  • Cassoly R, Gibson Q. 1975. Conformation, co-operativity and ligand binding in human hemoglobin. J Mol Biol. 91:301–313.
  • Chaudhury C, Mehnaz S, Robinson JM, Hayton WL, Pearl DK, Roopenian DC, Anderson CL. 2003. The major histocompatibility complex-related Fc receptor for IgG (FcRn) binds albumin and prolongs its lifespan. J Exp Med. 197:315–322.
  • Chernoff AI. 1953. Immunologic studies of hemoglobins I. The production of antihemoglobin sera and their immunologic characteristics. Blood. 8:399–412.
  • Chow ECY, Liu Lichuan, Ship N, Kluger RH, Pang KS. 2008. Role of haptoglobin on the uptake of native and β-chain [trimesoly-(lys82)β-(lys82)β] cross-linked human hemoglobins in isolated perfused rat livers. Drug Metabol Dis. 36:937–945.
  • Comper WD, Russo LM. 2009. The glomerular filter: an imperfect barrier is required for perfect renal function. Curr Opin Nephrol Hypertens. 18:336–342.
  • Conhaim RL, Cooler SC, McGrath AM, DeAngeles DA, Myers GA, Harms BA. 1998. Filtration of diaspirin crosslinked hemoglobin into lung and soft tissue lymph. Am J Respir Crit Care Med. 158: 1204–1212.
  • Conover CD, Gilbert CW, Shum KL, Shorr RGL. 1997a. The impact of polyethylene glycol conjugation on bovine hemoglobin's circulatory half-life and renal effects in a rabbit top-loaded transfusion model. Artif Organs. 21:907–915.
  • Conover CD, Linberg R, Gilbert CW, Shum KL, Shorr RG. 1997b. Effect of polyethylene glycol conjugated bovine hemoglobin in both top-load and exchange transfusion rat models. Artif Organs. 21: 1066–1075.
  • Conover CD, Linberg R, Shum KL, Shorr RG. 1999. The ability of polyethylene glycol conjugated bovine hemoglobin (PEG-Hb) to adequately deliver oxygen in both exchange transfusion and top-loaded rat models. Art Cells Blood Subs Immob Biotech. 27: 93–107.
  • Cunnington PG, Jenkins SN, Tam SC, Wong JTF. 1981. Oxygen-binding and immunological properties of complexes between dextran and animal haemoglobins. Biochem J. 193:261–266.
  • Dall’Acqua WF, Kiener PA, Wu H. 2006. Properties of Human IgG1s engineered for enhanced binding to the neonatal Fc receptor (FcRn). J Biol Chem. 281:23514–23524.
  • den Boer PJ, Bleeker WK, Rigter G, Agterberg J, Stekkinger P, Kannegieter LM, et al. 1992. Intravascular reduction of methemoglobin in plasma of the rat in vivo. Biomater Artif Cells Immobilization Biotechnol. 20:647–650.
  • DeVenuto F, Zegna A. 1983. Preparation and evaluation of pyridoxylated-polymerized human hemoglobin. J Surg Res. 34:205–212.
  • DeVenuto F. 1983. Modified hemoglobin solution as a resuscitation fluid. Vox Sang. 44:129–142.
  • DeVenuto F. 1978. Stability of hemoglobin solution during extended storage. J Lab Clin Med. 92:946–954.
  • Dittmer J, Ichikura T, Pivacek LE, Giorgio A, Prusty W, Valeri CR. 1992. Intravascular circulation and distribution of human 51Cr-DBBF stroma-free hemoglobin. Biomat Art Cells Immob Biotech. 20:751–755.
  • Dorman SC, Kenny CF, Miller L, Hirsch RE, Harrington JP. 2002. Role of redox potential of hemoglobin-based oxygen carriers on methemoglobin reduction by plasma components. Artif Cells Blood Substit Immobil Biotechnol. 30:39–51.
  • Doyle MP, Hoekstra JW. 1981. Oxidation of nitrogen oxides by bound dioxygen in hemoproteins. J Inorg Biochem. 14:351–358.
  • Dunne J, Caron A, Menu P, Alayash AI, Buehler PW, Wilson MT, et al. 2006. Ascorbate removes key precursors to oxidative damage by cell-free haemoglobin in vitro and in vivo. Biochem J. 399:513–524.
  • Ehrenreich BA, Cohn ZA. 1968. Fate of hemoglobin pinocytosed by macrophages in vitro. J Cell Biol. 38:244–248.
  • Elmer J, Palmer AF, Cabrales P. 2012. Oxygen delivery during extreme anemia with ultra-pure earthworm hemoglobin. Life Sci. 91:852–859.
  • El-Sayed M, Kiani MF, Naimark MD, Hikal AH, Ghandehari H. 2001. Extravasation of poly(amidoamine) (PAMAM) dendrimers across microvascular network endothelium. Pharm Res. 18:23–28.
  • Ericsson JL. 1965a. Transport and digestion of hemoglobin in the proximal tubule I. Light microscopy and cytochemistry of acid phosphatase. Lab Invest. 14:1–15.
  • Ericsson JL. 1965b. Transport and digestion of hemoglobin in the proximal tubule II. Electron microscopy. Lab Invest. 14:16–39.
  • Estep TN, Gonder J, Bornstein I, Aono F. 1992. Immunogenicity of diaspirin cross-linked human hemoglobin solutions. Biomater Artif Cells Immobilization Biotechnol. 20:603–609.
  • Etzerodt A, Kjolby M, Nielsen MJ, Maniecki M, Svendsen P, Moestrup SK. 2013. Plasma clearance of hemoglobin and haptoglobin in mice and effect of CD163 gene targeting disruption. Antiox Redox Signal. 18:2254–2263.
  • Faivre B, Menu P, Labrude P, Grandgeorge M, Vigneron C. 1994. Methemoglobin formation after administration of hemoglobin conjugated to carboxylate dextran in guinea pigs. Attempts to prevent the oxidation of hemoglobin. Artif Cells Blood Substit Immobil Biotechnol. 22:551–558.
  • Faivre-Fiorina B, Caron A, Fassot C, Fries I, Menu P, Labrude P, Vigneron C. 1999. Presence of hemoglobin inside aortic endothelial cells after cell-free hemoglobin administration in guinea pigs. Am J Physiol. 276:H766–770.
  • Faivre-Fiorina B, Caron A, Labrude P, Vigneron C. 1998. Les hémoglobines érythrocytaires, plasmatiques et substitutives face aux agents oxydants et réducteurs physiologiques. Ann Biol Clin. 56:545–556.
  • Fischer SR, Burnet M, Traber DL, Prough DS, Kramer GC. 1999. Plasma volume expansion with solutions of hemoglobin, albumin, and Ringer lactate in sheep. Am J Physiol (Heart Circ Physiol). 276:H2194–2203.
  • Fleck A. 1985. Computer models for metabolic studies on plasma proteins. Ann Clin Biochem. 22:33–49.
  • Frei B, England L, Ames BN. 1989. Ascorbate is an outstanding antioxidant in human blood plasma. Proc Natl Acad Sci. 86:6377–6381.
  • Friedman HI, DeVenuto F, Lollini L, Mellick P, Zuck TF. 1978. Morphologic effects following massive exchange transfusions with a stroma-free hemoglobin solution I. Liver . Lab Invest. 39:167–177.
  • Friedman HI, DeVenuto F. 1982. Morphological effects of transfusion with hemoglobin solutions. Crit Care Med. 10:288–293.
  • Gandhi RR, Bell DR. 1992. Importance of charge on transvascular albumin transport in skin and skeletal muscle. Am J Physiol. 262: H999–1008.
  • Gburek J, Osada J. 2000. Hemoglobin binding sites on renal brush-border membranes. Biochimie. 82:1135–1142.
  • Gburek J, Verroust PJ, Willnow TE, Fyfe JC, Nowacki W, Jacobsen C, et al. 2002. Megalin and cubulin are endocytic receptors involved in renal clearance of hemoglobin. J Am Soc Nephrol. 13:423–430.
  • Ghetie V, Hubbard JG, Kim JK, Tsen MF, Lee Y, Ward ES. 1996. Abnormally short serum half-lives of IgG in β2-microglobulin-deficient mice. Eur J Immunol. 26:690–696.
  • Ghitescu L, Desjardins M, Bendayan M. 1992. Immunocytochemical study of glomerular permeability to anionic, neutral and cationic albumins. Kidney Int. 42:25–32.
  • Gilbert C, Nho K, Johnson M, Linberg R, Shorr R. 1994. Hemoglobinuria in rats: a sensitive test of renal filtering and absorption of PEG-hemoglobin, a red blood cell substitute. Artif Cells Blood Substit Immobil Biotechnol. 22:535–541.
  • Goldfischer S, Novikoff AB, Albala A, Biempica L. 1970. Hemoglobin uptake by rat hepatocytes and its breakdown within lysosomes. J Cell Biol. 44:513–529.
  • Graversen JH, Madsen M, Moestrup SK. 2002. CD163: a signal receptor scavenging haptoglobin-hemoglobin complexes from plasma. Int J Biochem Cell Biol. 34:309–314.
  • Greenburg AG, Maffuid PW. 1983. Modification of hemoglobin – ring opened dials. In: Bolin RB, Geyer RP, Nemo GJ, Eds. Advances in blood substitute research. New York: Alan R Liss. pp. 9–17.
  • Greenburg AG, Schooley M, Peskin GW. 1977. Improved retention of stroma-free hemoglobin solution by chemical modification. J Trauma. 17:501–504.
  • Greenburg AG. 1983. The effects of hemoglobin on reticulo-endothelial function. In: Bolin RB, Geyer RP, Nemo GJ, Eds. Advances in blood substitute research. New York: Alan R Liss. pp. 127–137.
  • Gros G, Rollema HS, Jelkmann W, Gros H, Bauer C, Moll W. 1978. Net charge and oxygen affinity of human hemoglobin are independent of hemoglobin concentration. J Gen Physiol. 72:765–773.
  • Guyton AC. 1976. Textbook of medical physiology. 5th ed. Philadelphia: WB Saunders.
  • Hamilton RG, Kelly N, Gawryl MS, Rentko VT. 2001. Absence of immunopathology associated with repeated IV administration of bovine Hb-based oxygen carrier in dogs. Transfusion. 41:219–225.
  • Hamilton RG, Kickler TS. 2007. Bovine hemoglobin (glutamer-250, Hemopure)-specific immunoglobulin G antibody cross-reacts with human hemoglobin but does not lyse red blood cells in vitro. Transfusion. 47:723–728.
  • Haraldsson B, Nyström J, Deen WM. 2008. Properties of the glomerular barrier and mechanisms of proteinuria. Physiol Rev. 88: 451–487.
  • Harrington JP, Gonzalez Y, Hirsch RE. 2000. Redox concerns in the use of acellular hemoglobin-based therapeutic oxygen carriers of plasma components. Artif Cells Blood Sustit Immobil Biotechnol. 28:477–492.
  • Harvey JW, Kaneko JJ. 1976. Oxidation of human and animal haemoglobin with ascorbate, acetylphenylhydrazine, nitrite, and hydrogen peroxide. Br J Haematol. 32:193–203.
  • Heller P, Yakulis VJ, Josephson AM. 1962. Immunologic studies of human hemoglobins. J Lab Clin Med. 59:401–411.
  • Hershko C, Cook JD, Finch CA. 1972. Storage iron kinetics. II. The uptake of hemoglobin by hepatic parenchymal cells. J Lab Clin Med. 80:624–634.
  • Hertzman CM, Keipert PE, Chang TM. 1986. Serum antibody titers in rats receiving repeated small subcutaneous injections of hemoglobin or polyhemoglobin: a preliminary report. Int J Artif Organs. 9:179–182.
  • Hess JR, Fadare SO, Tolentino LSL, Bangal NR, Winslow RM. 1989. The intravascular persistence of crosslinked human hemoglobin. In: Brewer GJ, Ed. The red cell: seventh Ann Arbor conference. New York: Alan R. Liss. pp. 351–360.
  • Hsia JC, Song DL, Er SS, Wong LTL, Keipert PE, Gomez CL, et al. 1993. Pharmacokinetic studies in the rat on a o-raffinose polymerized human hemoglobin. In: Chang TMS, Ed. Blood substitutes and oxygen carriers. New York: Marcel Dekker. pp. 383–391.
  • Hughes GS, Antal EJ, Locker PK, Francom SF, Adams WJ, Jacobs EE. 1996. Physiology and pharmacokinetics of a novel hemoglobin-based oxygen carrier in humans. Crit Care Med. 24:756–764.
  • Hughes GS, Francom SF, Antal EJ, Adams WJ, Locker PK, Yancey EP, Jacobs EE. 1995. Hematologic effects of a novel hemoglobin-based oxygen carrier in normal male and female subjects. J Lab Clin Med. 126:444–451.
  • Israel EJ, Wilsker DF, Hayes KC, Schoenfeld D, Simister NE. 1996. Increased clearance of IgG in mice that lack β2-microglobulin: possible protective role of FcRn. Immunology. 89:573–578.
  • Jarnum S. 1975. Turnover of plasma proteins. J Clin Pathol Suppl (Assoc Clin Pathol). 6:13–21.
  • Jia Y, Wood F, Buehler PW, Alayash AI. 2013. Haptoglobin preferentially binds β but not α subunits cross-linked hemoglobin tetramers with minimal effects on ligand and redox reactions. PloS One. 8:e59841. Doi:10.1371/journal.pone.0059841.
  • Junghans RP, Anderson CL. 1996. The protection receptor for IgG catabolism is the β2-microglobulin-containing neonatal intestinal transport receptor. Proc Natl Acad Sci USA. 93:5512–5516.
  • Keene WR, Jandl CH. 1965. The sites of hemoglobin catabolism. Blood. 26:705–719.
  • Keipert PE, Adeniran AJ, Kwong S, Benesch RE. 1989a. Functional properties of a new crosslinked hemoglobin designed for use as a red cell substitute. Transfusion. 29:768–773.
  • Keipert PE, Chang TM. 1987. Effects of partial and total isovolemic exchange transfusion in fully conscious rats using pyridoxylated polyhemoglobin solution as a colloid oxygen-delivering replacement fluid. Vox Sang. 53:7–14.
  • Keipert PE, Chang TM. 1983. In vivo assessment of pyridoxylated crosslinked polyhemoglobin as an artificial red cell substitute in rats. Trans Am Soc Artif Intern Organs. 29:329–333.
  • Keipert PE, Gomez CL, Gonzales A, MacDonald VW, Hess JR, Winslow RM. 1994. Diaspirin cross-linked hemoglobin: Tissue distribution and long-term excretion after exchange transfusion. J Lab Clin Med. 123:701–711.
  • Keipert PE, Gomez CL, Gonzales A, MacDonald VW, Winslow RM. 1992. The role of the kidneys in the excretion of chemically modified hemoglobins. Biomater Artif Cells, Immob Biotech. 20:737–745.
  • Keipert PE, Gonzales A, Gomez CL, Macdonald VW, Hess JR, Winslow RM. 1993. Acute changes in systemic blood pressure and urine output of conscious rats following exchange transfusion with diaspirin-crosslinked hemoglobin solution. Transfusion. 33:701–708.
  • Keipert PE, Triner L. 1989. Catabolism and excretion of crosslinked hemoglobin. In: Brewer GJ, Ed. The red cell: seventh Ann Arbor conference. New York: Alan R Liss. pp. 383–405.
  • Keipert PE, Verosky M, Triner L. 1989b. Plasma retention and metabolic fate of hemoglobin modified with an interdimeric covalent cross link. ASAIO Transactions. 35:153–159.
  • Keipert PE. 1992. Properties of chemically cross-linked hemoglobin solutions designed as temporary oxygen carriers. Adv Exp Med Biol. 317:453–464.
  • Kikugawa K, Sasahara T, Sasaki T, Kurechi T. 1981. Factors influencing the autoxidation of hemoglobin A. Chem Pharm Bull. 29:1382–1389.
  • Kim HW, Clancy T, Chen F, Greenburg AG. 1993. Hepatic reticuloendothelial function following resuscitation with hemoglobin solutions. In: Chang TMS, Ed. Blood substitutes and oxygen carriers New York: Marcel Dekker Inc. pp. 564–566.
  • Kim HW, Greenburg AG, Eds. 2013. Hemoglobin-based oxygen carriers as red cell substitutes and oxygen therapeutics. Heidelberg: Springer.
  • Kino K, Mizumoto K, Watanabe J, Tsunoo H. 1987. Immunohistochemical studies on hemoglobin-haptoglobin and hemoglobin catabolism sites. J Histochem Cytochem. 35:381–386.
  • Kino K, Tsunoo H, Higa Y. 1980. Takami M, Hamaguchi H, Nakajima H. Hemoglobin-haptoglobin receptor in rat liver plasma membrane . J Biol Chem. 255:9616–9620.
  • Kramlova M, Pristoupil TI, Ulrych S, Hrkal Z. 1976. Stroma-free haemoglobin solution for infusion: changes during storage. Haematologia. 10:365–371.
  • Kristiansen M, Graversen JH, Jacobsen JC, Sonne O, Hoffman HJ, Law SK, Moestrup SK. 2001. Identification of the haemoglobin scavenger receptor. Nature. 409:198–201.
  • Kumari S, Swetha MG, Mayor S. 2010. Endocytosis unplugged: multiple ways to enter the cell. Cell Res. 20:256–275.
  • LaMuraglia GM, O’Hara PJ, Baker WH, Naslund TC, Norris EJ, Li J, Vandermeersch E. 2000. The reduction of the allogenic transfusion requirement in aortic surgery with a hemoglobin-based solution. J Vasc Surg. 31:299–308.
  • Lathem W, Davis BB, Zweig PH, Dew R. 1960. The demonstration and localization of renal tubular reabsorption of hemoglobin by stop flow analysis. J Clin Invest. 39:840–845.
  • Laurell CB, Nyman M. 1957. Studies on the serum haptoglobin level in hemoglobinemia and its influence on renal excretion of hemoglobin. Blood. 12:493–506.
  • Lee R, Neya K, Svizzero TA, Vlahakes GJ. 1995. Limitations of the efficacy of hemoglobin-based oxygen-carrying solutions. J Appl Physiol. 79:236–242.
  • Lenz G, Junger H, Schneider M, Kothe N, Lissner R, Prince AM. 1991. Elimination of pyridoxated polyhemoglobin after partial exchange transfusion in chimpanzees. Biomat Art Cells Immob Biotech. 19:699–707.
  • Lim SK, Kim H, Lim SK, bin Ali A, Lim YK, Wang Y, et al. 1998. Increased susceptibility in HP knockout mice during acute hemolysis. Blood. 92:1870–1877.
  • Lin JH. 2009. Pharmacokinetics of biotech drugs: peptides, proteins and monoclonal antibodies. Curr Drug Metab. 10:661–691.
  • Lockhart WL, Smith DB. 1975. Cross-linking of hemoglobin, haptoglobin, and hemoglobin-haptoglobin complex with bifunctional imidoesters. Can J Biochem. 53:861–867.
  • Malik AB, Lynch JJ, Cooper JA. 1989. Endothelial barrier function. J Invest Dermatol. 93:62S–67S.
  • Maniecki MB, Hasle H, Friis-Hansen L, Lausen B, Nielsen OJ, Bendix K, et al. 2008. Impaired CD163-mediated hemoglobin-scavenging and severe toxic symptoms in patients treated with gemtuzumab ozogamicin. Blood. 112:1510–1514.
  • Mansouri A, Winterhalter KH. 1973. Nonequivalence of chains in hemoglobin oxidation. Biochemistry. 12:4946–4949.
  • Marks DH, Brown DR, Ottinger WE, Atassi MZ. 1987. Antibody response to transfusion with pyridoxalated polymerized hemoglobin solution. Mil Med. 152:473–477.
  • Matheson B, Razynska A, Kwansa H, Bucci E. 2000. Appearance of dissociable and cross-linked hemoglobins in the renal hilar lymph. J Lab Clin Med. 135:459–464.
  • McGown EL, Lyons MF, Marini MA, Zegna A. 1990. Reduction of extracellular methemoglobin by erythrocytes. Biochim Biophys Acta. 1036:202–206.
  • Menaka S, Wang Y, Hack BK, Chang A, Jensen M, Bao L, Quigg RJ. 2009. Renal FcRn reclaims albumin but facilitates elimination of IgG. J Am Soc Nephrol. 20:1941–1952.
  • Mendiratta S, Qu ZC, May JM. 1998. Erythrocyte ascorbate recycling: antioxidant effects in blood. Free Radic Biol Med. 24:789–797.
  • Menu P, Faivre B, Labrude P, Riffard P, Grandgeorge M, Vigneron C. 1994. Human hemoglobin conjugated to carboxylate dextran as a potential red blood cell substitute-II−pharmacotoxicological evaluation. Artif Cells Blood Substit Immobil Biotechnol. 22:543–549.
  • Migita R, Gonzales A, Gonzales ML, Vandegriff KD, Winslow RM. 1997. Blood volume and cardiac index in rats after exchange transfusion with hemoglobin-based oxygen carriers. J Appl Physiol. 82:1995–2002.
  • Miller F. 1960. Hemoglobin absorption by the cells of the proximal convoluted tubule in the mouse kidney. J Biophys Biochem Cytol. 8:689–718.
  • Moestrup SK, Møller HJ. 2004. CD163: a regulated hemoglobin scavenger receptor with a role in the anti-inflammatory response. Ann Med. 36:347–354.
  • Mok W, Chen DE, Mazur A. 1975. Cross-linked hemoglobins as potential plasma protein extenders. Fed Proc. 34:1458–1460.
  • Morell A, Terry WD, Waldman TA. 1970. Metabolic properties of IgG subclasses in man. J Clin Invest. 49:673–680.
  • Mozzarelli A, Ronda L, Faggiano S, Bettati S, Bruno S. 2010. Haemoglobin-based oxygen carriers: research and reality towards an alternative to blood transfusion. Blood Transfus. 8 Suppl 3:s59–68.
  • Murray RK, Connell GE, Pert JH. 1961. The role of haptoglobin in the clearance and distribution of extracorpuscular hemoglobin. Blood. 17:45–53.
  • Nagel RL, Gibson QH. 1971. The binding of hemoglobin to haptoglobin and its relation to subunit dissociation of hemoglobin. J Biol Chem. 246:69–73.
  • O’Hara JF, Colburn WA, Tetzlaff JE, Novick AC, Angermeier KW, Schubert A. 2001. Hemoglobin and methemoglobin concentrations after large-dose infusions of diaspirin cross-linked hemoglobin. Anesth Analg. 92:44–48.
  • Olofsson C, Ahl T, Johansson T, Larsson S, Nellgård P, Ponzer S, et al. 2006. A multicenter clinical study of the safety and activity of maleimide-polyethylene glycol-modified hemoglobin (Hemospan) in patients undergoing major orthopedic surgery. Anesthesiology. 105:1153–1163.
  • Panter SS, Vandegriff KD, Yan PO, Regan RF. 1994. Assessment of hemoglobin-dependent neurotoxicity: Alpha-alpha crosslinked hemoglobin. Artif Cells Blood Substit Immobil Biotechnol. 22:399–413.
  • Patel MJ, Webb EJ, Shelbourn TE, Mattia-Goldberg C, George AJT, Zhang F, et al. 1998. Absence of immunogenicity of diaspirin cross-linked hemoglobin in humans. Blood. 91:710–716.
  • Pearce LB, Rentko VT, Moon-Massat PF, Gawryl MS. 2003. Comparative pharmacokinetics of a hemoglobin-based oxygen carrier. Acad Emerg Med. 10:557–558.
  • Peppard JV, Orlans E. 1980. The biological half-lives of four rat immunoglobulin isotypes. Immunology. 40:683–686.
  • Pitts RF. 1968. Physiology of the kidney and body fluids. 2nd ed. Chicago: Year Book Medical Publishers.
  • Polfliet MM, Fabriek BO, Daniëls WP, Dijkstra CD, van den Berg TK. 2006. The rat macrophage scavenger receptor CD163: expression, regulation and role in inflammatory mediator production. Immunobiology. 211:419–425.
  • Porter S. 2001. Human immune response to recombinant human proteins. J Pharm Sci. 90:1–11.
  • Przybelski RJ, Daily EK, Kisicki JC, Mattia-Goldbery C, Bounds MJ, Colburn WA. 1996. Phase I study of the safety and pharmacologic effects of diaspirin cross-linked hemoglobin solution. Crit Care Med. 24:1993–2000.
  • Rachmilewitz EA, Izak G, Nelken D. 1963. Studies on hemoglobin I. Antigenic properties of human, canine and rabbit hemoglobin solutions . Blood. 22:566–579.
  • Schaer DJ, Alayash AI, Buehler PW. 2007. Gating the radical hemoglobin to macrophages: the anti-inflammatory role of CD163, a scavenger receptor. Antiox Redox Signal. 9:991–999.
  • Schaer DJ, Schaer CA, Buehler PW, Boykins RA, Schoedon G, Alayash AI, Schaffner A. 2006. CD163 is the macrophage scavenger receptor for native and chemically modified hemoglobins in the absence of haptoglobin. Blood. 107:373–380.
  • Schnitzer JE, Oh P, Pinney E, Allard J. 1994. Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J Cell Biol. 127:1217–1232.
  • Schubert A, O’Hara JF, Przybelski RJ, Tetzlaff JE, Marks KE, Mascha E, Novick AC. 2002. Effect of diaspirin crosslinked hemoglobin (DCLHb HemAssist™) during high blood loss surgery on selected indices of organ function. Artif Cells Blood Substit Immobil Biotechnol. 30:259–283.
  • Sehgal LR, Gould SA, Rosen AL, Sehgal HL, Moss GS. 1984. Polymerized pyridoxylated hemoglobin: A red cell substitute with normal oxygen capacity. Surgery. 95:433–438.
  • Sehgal LR, Sehgal HL, Rosen AL, Gould SA, Rice CL, Moss GS. 1981. Control of methemoglobin formation in stroma-free hemoglobin solutions. J Surg Res. 31:13–17.
  • Shargel L, Wu-Pong S, Andrew Y. 2012. Applied biopharmaceutics & pharmacokinetics. 6th ed. New York: McGraw-Hill.
  • Ship NJ, Toprak A, Lai RP, Tseng E, Klugar R, Pang KS. 2005. Binding of acellular, native and cross-linked human hemoglobins to haptoglobin: enhanced distribution and clearance in the rat. Am J Physiol Gastointest Liver Physiol. 288:1301–1309.
  • Simionescu M, Gafencu A, Antohe F. 2002. Transcytosis of plasma macromolecules in endothelial cells: a cell biological survey. Microsc Res Tech. 1:269–288.
  • Smith DC, Schuschereba ST, Hess JR, McKinney L, Bunch D, Bowman PD. 1990. Liver and kidney injury after administration of hemoglobin cross-linked with bis(3,5-dibromosalicyl) fumarate. Biomater Artif Cells Artif Org. 18:251–261.
  • Snyder SR, Welty EV, Walder RY, Williams LA, Walder JA. 1987. HbXL99α: A hemoglobin derivative that is cross-linked between the α subunits is useful as a blood substitute. Proc Natl Acad Sci USA. 84:7280–7284.
  • Sprung J, Kindscher JD, Wahr JA, Levy JH, Monk TG, Moritz MW, O’Hara PJ. 2002. The use of bovine hemoglobin glutamer-250 (Hemopure®) in surgical patients: results of a multicenter, randomized, single-blinded trial. Anesth Analg. 94:799–808.
  • Standl T, Burmeister MA, Horn EP, Wilhelm S, Knoefel T, Schulte am Esch J. 1998. Bovine haemoglobin-based oxygen carrier for patients undergoing haemodilution before liver recession. Br J Anaesth. 80:189–194.
  • Swan SK, Halstenson CE, Collins AJ, Colburn WA, Blue J, Przybelski RJ. 1995. Pharmacologic profile of diaspirin cross-linked hemoglobin in hemodialysis patients. Am J Kidney Dis. 26:918–923.
  • Szabó G, Magyar Z. 1982. Extravascular circulation of plasma proteins. Acta Physiol Acad Sci Hung. 60:65–74.
  • Taguchi K, Maruyama T, Otagiri M. 2011. Pharmacokinetic properties of hemoglobin vesicles as a substitute for red blood cells. Drug Metab Rev. 43:362–373.
  • Takakura Y, Mahato RI, Hashida M. 1998. Extravasation of macromolecules. Adv Drug Deliv Rev. 34:93–108.
  • Tam SC, Blumenstein J, Wong JTF. 1978. Blood replacement in dogs by dextran-hemoglobin. Can J Biochem. 56:981–984.
  • Tenten V, Menzel S, Kunter U, Sicking EM, van Roeyen CR, Sanden SK, et al. 2013. Albumin is recycled from the primary urine by tubular transcytosis. J am Soc Nehprol. 24:1966–1980.
  • Thomas M, Matheson-Urbaitis B, Kwansa H, Bucci E, Fronticelli C. 1997. Introduction of negative charges to a crosslinked hemoglobin: lack of effect on plasma half life. Artif Cells Blood Substit Immobil Biotechnol. 25:309–314.
  • Tojo A, Kinugasa S. 2012. Mechanisms of glomerular albumin filtration and tubular reabsorption. Int J Nephrol. 2012:481520. Doi: 10.1155/2012/481520.
  • Tomoda A, Matsukawa S, Takeshita M, Yoneyama Y. 1976. Effect of organic phosphates on methemoglobin reduction by ascorbic acid. J Biol Chem. 251:7494–7498.
  • Urbaitis BK, Razynska A, Corteza Q, Fronticelli C, Bucci E. 1991. Intravascular retention and renal handling of purified natural and intramolecularly cross-linked hemoglobins. J Lab Clin Med. 117: 115–121.
  • Vandegriff KD, Malavalli A, Minn C, Jiang E, Lohman J, Young MA, et al. 2006. Oxidation and haem loss kinetics of poly(ethylene glycol)-conjugated haemoglobin (MP4): dissociation between in vitro and in vivo oxidation rates. Biochem J. 399:463–471.
  • Vandegriff KD, Malavalli A, Woodridge J, Lohman J, Winslow RM. 2003. MP4, a new nonvasoactive PEG-Hb conjugate. Transfusion. 43:509–516.
  • Vandegriff KD, McCarthy M, Rohlfs RJ, Winslow RM. 1997. Colloid osmotic properties of modified hemoglobins: chemically cross-linked versus polyethylene glycol surface-conjugated. Biophys Chem. 69:23–30.
  • Velky TS, Lee ES, Maffuid PW, Robinson GT, Yang JC, Greenburg AG. 1987. Peritoneal accumulation of infused stroma-free hemoglobin. Potential toxicity of an oxygen-carrying substitute. Arch Surg. 122:355–357.
  • Venkatachalam MA, Rennke HG. 1978. The structural and molecular basis of glomerular filtration. Circ Res. 43:337–347.
  • Viele MK, Weiskopf RB, Fisher D. 1997. Recombinant human hemoglobin does not affect renal function in humans: Analysis of safety and pharmacokinetics. Anesthesiology. 86:848–858.
  • Wada T, Oara H, Watanabe K, Kinoshita H, Yachi A. 1970. Autoradiographic study on the site of uptake of the haptoglobin-hemoglobin complex. J Reticuloendothel Soc. 8:185–193.
  • Weinstein MB, Segal HL. 1984. Uptake of free hemoglobin by rat liver parenchymal cells. Biochem Biophys Res Commun. 123:489–496.
  • Wicks D, Wong LT, Sandhu R, Stewart RK, Biro GP. 2003. The intravascular persistence and methemoglobin formation of hemolink (hemoglobin raffimer) in dogs. Artif Cells Blood Substit Biotechnol. 31:1–17.
  • Winslow RM. 1993. Potential clinical applications for blood substitutes. In: Chang TMS, Ed. Blood substitutes and oxygen carriers, New York: Marcel Dekker. pp. 44–56.
  • Zhang L, Levy A, Rifkind JM. 1991. Autoxidation of hemoglobin enhanced by dissociation into dimers. J Biol Chem. 266: 24698–24701.
  • Zuwała-Jagiełło J, Osada J. 1998. Internalization study using EDTA-prepared hepatocytes for receptor-mediated endocytosis of haemoglobin-haptoglobin complex. Int J Biochem Cell Biol. 30: 923–931.

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