Login Register Cart 0
Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe Translate in Chinese
Review Article

Translational Research of Hemoglobin Vesicles as a Transfusion Alternative

Author(s): Hiromi Sakai*, Naoko Kobayashi, Tomoko Kure and Chie Okuda

Volume 29, Issue 3, 2022

Published on: 12 April, 2021

Page: [591 - 606] Pages: 16

DOI: 10.2174/0929867328666210412130035

Price: $65

Abstract

Clinical situations arise in which blood for transfusion becomes scarce or unavailable. Considerable demand for a transfusion alternative persists because of various difficulties posed by blood donation and transfusion systems. Hemoglobin-vesicles (Hb- V) are artificial oxygen carriers being developed for use as a transfusion alternative. Just as biomembranes of red blood cells (RBCs) do, phospholipid vesicles (liposomes) for Hb encapsulation can protect the human body from the toxic effects of molecular Hb. The main HbV component, Hb, is obtained from discarded human donated blood. Therefore, HbV can be categorized as a biologic agent targeting oxygen for peripheral tissues. The purification procedure strictly eliminates the possibility of viral contamination. It also removes all concomitant unstable enzymes present in RBC for utmost safety from infection. The deoxygenated HbVs, which are storable for over the years at ambient temperature, can function as an alternative to blood transfusion for resuscitation from hemorrhagic shock and O2 therapeutics. Moreover, a recent study clarified beneficial effects for anti- oxidation and anti-inflammation by carbon monoxide (CO)-bound HbVs. Autoxidation of HbV (HbO2 → metHb + O2 -.) is unavoidable after intravenous administration. Co-injection of methylene blue can extract the intraerythrocytic glycolytic electron energy effectively and reduce metHb. Other phenothiazine dyes can also function as electron mediators to improve the functional life span of HbV. This review paper summarizes recent progress of the research and development of HbV, aimed at clinical applications.

Keywords: Artificial blood, blood substitutes, carbon monoxide, electron mediator, glycolytic electron energy, hemoglobin-based oxygen carriers, liposomes, NAD(P)H.

« Previous
[1]
Garraud, O.; Schneider, T. International collaboration for blood safety: The French-African experience. Transfus. Clin. Biol, 2021, 28, 154-157.
[2]
Mili, F.D.; Teng, Y.; Shiraishi, R.W.; Yu, J.; Bock, N.; Drammeh, B.; Watts, D.H.; Benech, I. New HIV infections from blood transfusions averted in 28 countries supported by PEPFAR blood safety programs, 2004-2015. Transfusion, 2021, 61, 851-861.
[http://dx.doi.org/10.1111/trf.16256] [PMID: 33506960]
[3]
Ticehurst, J.R.; Pisanic, N.; Forman, M.S.; Ordak, C.; Heaney, C.D.; Ong, E.; Linnen, J.M.; Ness, P.M.; Guo, N.; Shan, H.; Nelson, K.E. Probable transmission of hepatitis E virus (HEV) via transfusion in the United States. Transfusion, 2019, 59(3), 1024-1034.
[http://dx.doi.org/10.1111/trf.15140] [PMID: 30702157]
[4]
Brecher, M.E.; Hay, S.N. Bacterial contamination of blood components. Clin. Microbiol. Rev., 2005, 18(1), 195-204.
[http://dx.doi.org/10.1128/CMR.18.1.195-204.2005] [PMID: 15653826]
[5]
Ngoma, A.M.; Goto, A.; Nollet, K.E.; Sawamura, Y.; Ohto, H.; Yasumura, S. Blood Donor Deferral among Students in Northern Japan: Challenges Ahead. Transfus. Med. Hemother., 2014, 41(4), 251-256.
[http://dx.doi.org/10.1159/000365406] [PMID: 25254020]
[6]
Stanworth, S.J.; New, H.V.; Apelseth, T.O.; Brunskill, S.; Cardigan, R.; Doree, C.; Germain, M.; Goldman, M.; Massey, E.; Prati, D.; Shehata, N.; So-Osman, C.; Thachil, J. Effects of the COVID-19 pandemic on supply and use of blood for transfusion. Lancet Haematol., 2020, 7(10), e756-e764.
[http://dx.doi.org/10.1016/S2352-3026(20)30186-1] [PMID: 32628911]
[7]
Al Mahmasani, L.; Hodroj, M.H.; Finianos, A.; Taher, A. COVID-19 pandemic and transfusion medicine: the worldwide challenge and its implications. Ann. Hematol., 2021, 1, 1-8.
[PMID: 33527161]
[8]
Bunn, H.F.; Forget, B.G. Hemoglobin: Molecular, Genetic and Clinical Aspects; W.B. Sanders Company: Philadelphia, 1986.
[9]
Winslow, R.M. Hemoglobin-based Red Cell Substitutes; The Johns Hopkins University Press: Baltimore, USA, 1992.
[10]
Griffon, N.; Baudin, V.; Dieryck, W.; Dumoulin, A.; Pagnier, J.; Poyart, C.; Marden, M.C. Tetramer-dimer equilibrium of oxyhemoglobin mutants determined from auto-oxidation rates. Protein Sci., 1998, 7(3), 673-680.
[http://dx.doi.org/10.1002/pro.5560070316] [PMID: 9541399]
[11]
Sakai, H.; Sato, A.; Masuda, K.; Takeoka, S.; Tsuchida, E. Encapsulation of concentrated hemoglobin solution in phospholipid vesicles retards the reaction with NO, but not CO, by intracellular diffusion barrier. J. Biol. Chem., 2008, 283(3), 1508-1517.
[http://dx.doi.org/10.1074/jbc.M707660200] [PMID: 18003613]
[12]
Goda, N.; Suzuki, K.; Naito, M.; Takeoka, S.; Tsuchida, E.; Ishimura, Y.; Tamatani, T.; Suematsu, M. Distribution of heme oxygenase isoforms in rat liver. Topographic basis for carbon monoxide-mediated microvascular relaxation. J. Clin. Invest., 1998, 101(3), 604-612.
[http://dx.doi.org/10.1172/JCI1324] [PMID: 9449694]
[13]
Regan, R.F.; Rogers, B. Delayed treatment of hemoglobin neurotoxicity. J. Neurotrauma, 2003, 20(1), 111-120.
[http://dx.doi.org/10.1089/08977150360517236] [PMID: 12614593]
[14]
Murray, J.A.; Ledlow, A.; Launspach, J.; Evans, D.; Loveday, M.; Conklin, J.L. The effects of recombinant human hemoglobin on esophageal motor functions in humans. Gastroenterology, 1995, 109(4), 1241-1248.
[http://dx.doi.org/10.1016/0016-5085(95)90584-7] [PMID: 7557091]
[15]
Burhop, K.; Gordon, D.; Estep, T. Review of hemoglobin-induced myocardial lesions. Artif. Cells Blood Substit. Immobil. Biotechnol., 2004, 32(3), 353-374.
[http://dx.doi.org/10.1081/BIO-200027429] [PMID: 15508274]
[16]
Blood Substitutes; Winslow, R.M., Ed.;Elsevier: Amsterdam, The Netherlands, 2005..
[17]
Chemistry and Biochemistry of Oxygen Therapeutics From Transfusion to Artificial Blood.Mozzarelli, A.; Bettati, S.,; John Wiley & Sons Ltd: Chichester, United Kingdom, 2011.
[http://dx.doi.org/10.1002/9781119975427]
[18]
Hemoglobin-based oxygen carriers as red cell substitutes and oxygen therapeutics.Kim, H.W.; Greenburg, A.G., Eds.;; Springer-Verlag: Berlin Heidelberg, Germany, 2013.
[http://dx.doi.org/10.1007/978-3-642-40717-8]
[19]
Selected topics in nanomedicine.Chang, T.M.S., Ed.;; World Scientific: Singapore, 2014.
[20]
Jahr, J.S.; Guinn, N.R.; Lowery, D.R.; Shore-Lesserson, L.; Shander, A. Blood Substitutes and Oxygen Therapeutics: A Review. Anesth. Analg., 2021, 132(1), 119-129.
[http://dx.doi.org/10.1213/ANE.0000000000003957] [PMID: 30925560]
[21]
Holzner, M.L.; DeMaria, S.; Haydel, B.; Smith, N.; Flaherty, D.; Florman, S. Pegylated Bovine Carboxyhemoglobin (SANGUINATE) in a Jehovah’s Witness Undergoing Liver Transplant: A Case Report. Transplant. Proc., 2018, 50(10), 4012-4014.
[http://dx.doi.org/10.1016/j.transproceed.2018.09.006] [PMID: 30577305]
[22]
Alayash, A.I. Mechanisms of Toxicity and Modulation of Hemoglobin-based Oxygen Carriers. Shock, 2019, 52(1S Suppl 1), 41-49.
[http://dx.doi.org/10.1097/SHK.0000000000001044]
[23]
Zumberg, M.; Gorlin, J.; Griffiths, E.A.; Schwartz, G.; Fletcher, B.S.; Walsh, K.; Dao, K.H.; Vansandt, A.; Lynn, M.; Shander, A. A case study of 10 patients administered HBOC-201 in high doses over a prolonged period: outcomes during severe anemia when transfusion is not an option. Transfusion, 2020, 60(5), 932-939.
[http://dx.doi.org/10.1111/trf.15778] [PMID: 32358832]
[24]
Natanson, C.; Kern, S.J.; Lurie, P.; Banks, S.M.; Wolfe, S.M. Cell-free hemoglobin-based blood substitutes and risk of myocardial infarction and death: a meta-analysis. JAMA, 2008, 299(19), 2304-2312.
[http://dx.doi.org/10.1001/jama.299.19.jrv80007] [PMID: 18443023]
[25]
Benitez Cardenas, A.S.; Samuel, P.P.; Olson, J.S. Current Challenges in the Development of Acellular Hemoglobin Oxygen Carriers by Protein Engineering. Shock, 2019, 52(1S Suppl 1), 28-40.
[http://dx.doi.org/10.1097/SHK.0000000000001053]
[26]
Marrazzo, F.; Larson, G.; Sherpa Lama, T.T.; Teggia Droghi, M.; Joyce, M.; Ichinose, F.; Watkins, M.T.; Stowell, C.; Crowley, J.; Berra, L. Inhaled nitric oxide prevents systemic and pulmonary vasoconstriction due to hemoglobin-based oxygen carrier infusion: A case report. J. Crit. Care, 2019, 51, 213-216.
[http://dx.doi.org/10.1016/j.jcrc.2018.04.008] [PMID: 30709560]
[27]
Kim, J.; Jeong, S.; Korneev, R.; Shin, K.; Kim, K.T. Cross-Linked Polymersomes with Reversible Deformability and Oxygen Transportability. Biomacromolecules, 2019, 20(6), 2430-2439.
[http://dx.doi.org/10.1021/acs.biomac.9b00485] [PMID: 31059234]
[28]
Kao, I.; Xiong, Y.; Steffen, A.; Smuda, K.; Zhao, L.; Georgieva, R.; Pruss, A.; Bäumler, H. Preclinical In Vitro Safety Investigations of Submicron Sized Hemoglobin Based Oxygen Carrier HbMP-700. Artif. Organs, 2018, 42(5), 549-559.
[http://dx.doi.org/10.1111/aor.13071] [PMID: 29508415]
[29]
Gu, X.; Bolden-Rush, C.; Cuddington, C.T.; Belcher, D.A.; Savla, C.; Pires, I.S.; Palmer, A.F. Comprehensive characterization of tense and relaxed quaternary state glutaraldehyde polymerized bovine hemoglobin as a function of cross-link density. Biotechnol. Bioeng., 2020, 117(8), 2362-2376.
[http://dx.doi.org/10.1002/bit.27382] [PMID: 32472694]
[30]
Paciello, A.; Amalfitano, G.; Garziano, A.; Urciuolo, F.; Netti, P.A. Hemoglobin-Conjugated Gelatin Microsphere as a Smart Oxygen Releasing Biomaterial. Adv. Healthc. Mater., 2016, 5(20), 2655-2666.
[http://dx.doi.org/10.1002/adhm.201600559] [PMID: 27594116]
[31]
Coll-Satue, C.; Bishnoi, S.; Chen, J.; Hosta-Rigau, L. Stepping stones to the future of haemoglobin-based blood products: clinical, preclinical and innovative examples. Biomater. Sci, 2020, 1135-1152.
[http://dx.doi.org/10.1039/d0bm01767a] [PMID: 33350411]
[32]
Jansman, M.M.T.; Liu, X.; Kempen, P.; Clergeaud, G.; Andresen, T.L.; Thulstrup, P.W.; Hosta-Rigau, L. Hemoglobin-Based Oxygen Carriers Incorporating Nanozymes for the Depletion of Reactive Oxygen Species. ACS Appl. Mater. Interfaces, 2020, 12(45), 50275-50286.
[http://dx.doi.org/10.1021/acsami.0c14822] [PMID: 33124811]
[33]
Timm, B.; Abdulmalik, O.; Chakrabarti, A.; Elmer, J. Purification of Lumbricus terrestris erythrocruorin (LtEc) with anion exchange chromatography. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 2020, 1150, 122162.
[http://dx.doi.org/10.1016/j.jchromb.2020.122162] [PMID: 32505113]
[34]
Schakowski, K.M.; Linders, J.; Ferenz, K.B.; Kirsch, M. Synthesis and characterisation of aqueous haemoglobin-based microcapsules coated by genipin-cross-linked albumin. J. Microencapsul., 2020, 37(3), 193-204.
[http://dx.doi.org/10.1080/02652048.2020.1715498] [PMID: 31950867]
[35]
Liu, X.; Jansman, M.M.T.; Thulstrup, P.W.; Mendes, A.C.; Chronakis, I.S.; Hosta-Rigau, L. Low-Fouling Electrosprayed Hemoglobin Nanoparticles with Antioxidant Protection as Promising Oxygen Carriers. Macromol. Biosci., 2020, 20(2), e1900293.
[http://dx.doi.org/10.1002/mabi.201900293] [PMID: 31846219]
[36]
Zhang, K.; Xiao, X.; Li, L.; Fan, Y.; Cai, Q.; Lee, I.S.; Li, X. Development of novel oxygen carriers by coupling hemoglobin to functionalized multiwall carbon nanotubes. J. Mater. Chem. B Mater. Biol. Med., 2019, 7(31), 4821-4832.
[http://dx.doi.org/10.1039/C9TB00894B] [PMID: 31389959]
[37]
Roamcharern, N.; Payoungkiattikun, W.; Anwised, P.; Mahong, B.; Jangpromma, N.; Daduang, S.; Klaynongsruang, S. Physicochemical properties and oxygen affinity of glutaraldehyde polymerized crocodile hemoglobin: the new alternative hemoglobin source for hemoglobin-based oxygen carriers. Artif. Cells Nanomed. Biotechnol., 2019, 47(1), 852-861.
[http://dx.doi.org/10.1080/21691401.2019.1579733] [PMID: 30873884]
[38]
Cooper, C.E.; Silkstone, G.G.A.; Simons, M.; Gretton, S.; Rajagopal, B.S.; Allen-Baume, V.; Syrett, N.; Shaik, T.; Popa, G.; Sheng, X.; Bird, M.; Choi, J.W.; Piano, R.; Ronda, L.; Bettati, S.; Paredi, G.; Mozzarelli, A.; Reeder, B.J. Engineering hemoglobin to enable homogenous PEGylation without modifying protein functionality. Biomater. Sci., 2020, 8(14), 3896-3906.
[http://dx.doi.org/10.1039/C9BM01773A] [PMID: 32539053]
[39]
Natarajan, C.; Signore, A.V.; Kumar, V.; Storz, J.F. Synthesis of Recombinant Human Hemoglobin With NH2 -Terminal Acetylation in Escherichia coli. Curr. Protoc. Protein Sci., 2020, 101(1), e112.
[http://dx.doi.org/10.1002/cpps.112] [PMID: 32687676]
[40]
Funaki, R.; Okamoto, W.; Endo, C.; Morita, Y.; Kihira, K.; Komatsu, T. Genetically engineered haemoglobin wrapped covalently with human serum albumins as an artificial O2 carrier. J. Mater. Chem. B Mater. Biol. Med., 2020, 8(6), 1139-1145.
[http://dx.doi.org/10.1039/C9TB02184A] [PMID: 31840728]
[41]
Ishchuk, O.P.; Martínez, J.L.; Petranovic, D. Improving the Production of Cofactor-Containing Proteins: Production of Human Hemoglobin in Yeast. Methods Mol. Biol., 2019, 1923, 243-264.
[http://dx.doi.org/10.1007/978-1-4939-9024-5_11] [PMID: 30737744]
[42]
Alayash, A.I. βCysteine 93 in human hemoglobin: a gateway to oxidative stability in health and disease. Lab. Invest., 2021, 101(1), 4-11.
[http://dx.doi.org/10.1038/s41374-020-00492-3] [PMID: 32980855]
[43]
Chang, T.M. Semipermeable microcapsules. Science, 1964, 146(3643), 524-525.
[http://dx.doi.org/10.1126/science.146.3643.524] [PMID: 14190240]
[44]
Bangham, A.D.; Horne, R.W. Negative staining of phospholipids and their structure modification by surface-active agents as observed in the electron microscope. J. Mol. Biol., 1964, 8, 660-668.
[http://dx.doi.org/10.1016/S0022-2836(64)80115-7] [PMID: 14187392]
[45]
Filipczak, N.; Pan, J.; Yalamarty, S.S.K.; Torchilin, V.P. Recent advancements in liposome technology. Adv. Drug Deliv. Rev., 2020, 156, 4-22.
[http://dx.doi.org/10.1016/j.addr.2020.06.022] [PMID: 32593642]
[46]
Goswami, R.; O’Hagan, D.T.; Adamo, R.; Baudner, B.C. Conjugation of Mannans to Enhance the Potency of Liposome Nanoparticles for the Delivery of RNA Vaccines. Pharmaceutics, 2021, 13(2), 240.
[http://dx.doi.org/10.3390/pharmaceutics13020240] [PMID: 33572332]
[47]
Djordjevich, L.; Miller, I.F. Lipid encapsulated hemoglobin as a synthetic erythrocyte. Fed. Proc., 1977, 36, 567.
[48]
Djordjevich, L.; Miller, I.F. Synthetic erythrocytes from lipid encapsulated hemoglobin. Exp. Hematol., 1980, 8(5), 584-592.
[PMID: 7461058]
[49]
Sakai, H.; Sou, K.; Tsuchida, E. Hemoglobin-vesicles as an artificial oxygen carrier. Methods Enzymol., 2009, 465, 363-384.
[http://dx.doi.org/10.1016/S0076-6879(09)65019-9] [PMID: 19913177]
[50]
Hunt, C.A.; Burnette, R.R.; MacGregor, R.D.; Strubbe, A.E.; Lau, D.T.; Taylor, N.; Kiwada, H. Synthesis and evaluation of a prototypal artificial red cell. Science, 1985, 230(4730), 1165-1168.
[http://dx.doi.org/10.1126/science.4071041] [PMID: 4071041]
[51]
Kato, A.; Arakawa, M.; Kondo, T. Preparation and stability of liposome-type artificial red blood cells stabilized with carboxymethylchitin. J. Microencapsul., 1984, 1(2), 105-112.
[http://dx.doi.org/10.3109/02652048409038514] [PMID: 6336519]
[52]
Farmer, M.C.; Rudolph, A.S.; Vandegriff, K.D.; Hayre, M.D.; Bayne, S.A.; Johnson, S.A. Liposome-encapsulated hemoglobin: oxygen binding properties and respiratory function. Biomater. Artif. Cells Artif. Organs, 1988, 16(1-3), 289-299.
[http://dx.doi.org/10.3109/10731198809132578] [PMID: 3179470]
[53]
Phillips, W.T.; Klipper, R.W.; Awasthi, V.D.; Rudolph, A.S.; Cliff, R.; Kwasiborski, V.; Goins, B.A. Polyethylene glycol-modified liposome-encapsulated hemoglobin: a long circulating red cell substitute. J. Pharmacol. Exp. Ther., 1999, 288(2), 665-670.
[PMID: 9918573]
[54]
Phillips, W.T.; Lemen, L.; Goins, B.; Rudolph, A.S.; Klipper, R.; Fresne, D.; Jerabek, P.A.; Emch, M.E.; Martin, C.; Fox, P.T.; McMahan, C.A. Use of oxygen-15 to measure oxygen-carrying capacity of blood substitutes in vivo. Am. J. Physiol., 1997, 272(5 Pt 2), H2492-H2499.
[PMID: 9176321]
[55]
Szebeni, J.; Fontana, J.L.; Wassef, N.M.; Mongan, P.D.; Morse, D.S.; Dobbins, D.E.; Stahl, G.L.; Bünger, R.; Alving, C.R. Hemodynamic changes induced by liposomes and liposome-encapsulated hemoglobin in pigs: a model for pseudoallergic cardiopulmonary reactions to liposomes. Role of complement and inhibition by soluble CR1 and anti-C5a antibody. Circulation, 1999, 99(17), 2302-2309.
[http://dx.doi.org/10.1161/01.CIR.99.17.2302] [PMID: 10226097]
[56]
Usuba, A.; Motoki, R.; Miyauchi, Y.; Suzuki, K.; Takahashi, A. Effect of neo red cells on the canine hemorrhagic shock model. Int. J. Artif. Organs, 1991, 14(11), 739-744.
[http://dx.doi.org/10.1177/039139889101401111] [PMID: 1757162]
[57]
Kawaguchi, F.; Kawaguchi, A.T.; Murayama, C.; Kamijo, A.; Haida, M. Liposome-Encapsulated Hemoglobin Improves Tumor Oxygenation as Detected by Near-Infrared Spectroscopy in Colon Carcinoma in Mice. Artif. Organs, 2017, 41(4), 327-335.
[http://dx.doi.org/10.1111/aor.12825] [PMID: 27873328]
[58]
Kawaguchi, A.T.; Tamaki, T. Artificial oxygen carrier improves fatigue resistance in slow muscle but not in fast muscle in a rat in situ model. Artif. Organs, 2020, 44(1), 72-80.
[http://dx.doi.org/10.1111/aor.13535] [PMID: 31291698]
[59]
Satoh, T.; Kobayashi, K.; Sekiguchi, S.; Tsuchida, E. Characteristics of artificial red cells. Hemoglobin encapsulated in poly-lipid vesicles. ASAIO J., 1992, 38(3), M580-M584.
[http://dx.doi.org/10.1097/00002480-199207000-00102] [PMID: 1457926]
[60]
Akama, K.; Awai, K.; Yano, Y.; Tokuyama, S.; Nakano, Y. In vitro and in vivo stability of polymerized mixed liposomes composed of 2,4-octadecadienoyl groups of phospholipids. Polym. Adv. Technol., 2000, 11(6), 280-287.
[http://dx.doi.org/10.1002/1099-1581(200006)11:6<280::AID-PAT942>3.0.CO;2-C]
[61]
Pape, A.; Kertscho, H.; Meier, J.; Horn, O.; Laout, M.; Steche, M.; Lossen, M.; Theisen, A.; Zwissler, B.; Habler, O. Improved short-term survival with polyethylene glycol modified hemoglobin liposomes in critical normovolemic anemia. Intensive Care Med., 2008, 34(8), 1534-1543.
[http://dx.doi.org/10.1007/s00134-008-1082-z] [PMID: 18385978]
[62]
Sakai, H.; Sou, K.; Horinouchi, H.; Kobayashi, K.; Tsuchida, E. Haemoglobin-vesicles as artificial oxygen carriers: present situation and future visions. J. Intern. Med., 2008, 263(1), 4-15.
[PMID: 18042220]
[63]
Rao, G.; Yadav, V.R.; Awasthi, S.; Roberts, P.R.; Awasthi, V. Effect of liposome-encapsulated hemoglobin resuscitation on proteostasis in small intestinal epithelium after hemorrhagic shock. Am. J. Physiol. Gastrointest. Liver Physiol., 2016, 311(1), G180-G191.
[http://dx.doi.org/10.1152/ajpgi.00157.2016] [PMID: 27288424]
[64]
Yadav, V.R.; Rao, G.; Houson, H.; Hedrick, A.; Awasthi, S.; Roberts, P.R.; Awasthi, V. Nanovesicular liposome-encapsulated hemoglobin (LEH) prevents multi-organ injuries in a rat model of hemorrhagic shock. Eur. J. Pharm. Sci., 2016, 93, 97-106.
[http://dx.doi.org/10.1016/j.ejps.2016.08.010] [PMID: 27503458]
[65]
Rameez, S.; Guzman, N.; Banerjee, U.; Fontes, J.; Paulaitis, M.E.; Palmer, A.F.; Patel, R.P.; Honavar, J. Encapsulation of hemoglobin inside liposomes surface conjugated with poly(ethylene glycol) attenuates their reactions with gaseous ligands and regulates nitric oxide dependent vasodilation. Biotechnol. Prog., 2012, 28(3), 636-645.
[http://dx.doi.org/10.1002/btpr.1532] [PMID: 22467599]
[66]
Zhu, C.; Guo, X.; Luo, L.; Wu, Z.; Luo, Z.; Jiang, M.; Zhang, J.; Qin, B.; Shi, Y.; Lou, Y.; Qiu, Y.; You, J. Extremely Effective Chemoradiotherapy by Inducing Immunogenic Cell Death and Radio-Triggered Drug Release under Hypoxia Alleviation. ACS Appl. Mater. Interfaces, 2019, 11(50), 46536-46547.
[http://dx.doi.org/10.1021/acsami.9b16837] [PMID: 31751119]
[67]
Sen Gupta, A. Hemoglobin-based oxygen carriers: current state-of-the-art and novel molecules. Shock, 2019, 52(1S)(Suppl. 1), 70-83.
[http://dx.doi.org/10.1097/SHK.0000000000001009] [PMID: 31513123]
[68]
Rameez, S.; Banerjee, U.; Fontes, J.; Roth, A.; Palmer, A.F. The Reactivity of Polymersome Encapsulated Hemoglobin with Physiologically Important Gaseous Ligands: Oxygen, Carbon Monoxide and Nitric Oxide. Macromolecules, 2012, 45(5), 2385-2389.
[http://dx.doi.org/10.1021/ma202739f] [PMID: 22865934]
[69]
Cherwin, A.; Namen, S.; Rapacz, J.; Kusik, G.; Anderson, A.; Wang, Y.; Kaltchev, M.; Schroeder, R.; O’Connell, K.; Stephens, S.; Chen, J.; Zhang, W. Design of a Novel Oxygen Therapeutic Using Polymeric Hydrogel Microcapsules Mimicking Red Blood Cells. Pharmaceutics, 2019, 11(11), 583.
[http://dx.doi.org/10.3390/pharmaceutics11110583] [PMID: 31703298]
[70]
Peng, S.; Liu, J.; Qin, Y.; Wang, H.; Cao, B.; Lu, L.; Yu, X. Metal-Organic Framework Encapsulating Hemoglobin as a High-Stable and Long-Circulating Oxygen Carriers to Treat Hemorrhagic Shock. ACS Appl. Mater. Interfaces, 2019, 11(39), 35604-35612.
[http://dx.doi.org/10.1021/acsami.9b15037] [PMID: 31495166]
[71]
Blocher McTigue, W.C.; Perry, S.L. Design rules for encapsulating proteins into complex coacervates. Soft Matter, 2019, 15(15), 3089-3103.
[http://dx.doi.org/10.1039/C9SM00372J] [PMID: 30916112]
[72]
Tu, J.; Bussmann, J.; Du, G.; Gao, Y.; Bouwstra, J.A.; Kros, A. Lipid bilayer-coated mesoporous silica nanoparticles carrying bovine hemoglobin towards an erythrocyte mimic. Int. J. Pharm., 2018, 543(1-2), 169-178.
[http://dx.doi.org/10.1016/j.ijpharm.2018.03.037] [PMID: 29567198]
[73]
Sen Gupta, A.; Doctor, A. Oxygen Carriers. In: Damage Control Resuscitation; Spinella, P.C., Ed.; Springer Nature: Switzerland, 2020; Chapter 11, pp. 197-222.
[http://dx.doi.org/10.1007/978-3-030-20820-2_11]
[74]
Ogata, Y.; Goto, H.; Kimura, T.; Fukui, H. Development of neo red cells (NRC) with the enzymatic reduction system of methemoglobin. Artif. Cells Blood Substit. Immobil. Biotechnol., 1997, 25(4), 417-427.
[http://dx.doi.org/10.3109/10731199709118931] [PMID: 9242936]
[75]
Iwashita, Y.; Yabuki, A.; Yamaji, K.; Iwasaki, K.; Okami, T.; Hirata, C.; Kosaka, K. A new resuscitation fluid “stabilized hemoglobin” preparation and characteristics. Biomater. Artif. Cells Artif. Organs, 1988, 16(1-3), 271-280.
[http://dx.doi.org/10.3109/10731198809132576] [PMID: 3179469]
[76]
Sakai, H.; Masada, Y.; Takeoka, S.; Tsuchida, E. Characteristics of bovine hemoglobin as a potential source of hemoglobin-vesicles for an artificial oxygen carrier. J. Biochem., 2002, 131(4), 611-617.
[http://dx.doi.org/10.1093/oxfordjournals.jbchem.a003141] [PMID: 11927000]
[77]
Wang, Q.; Hu, T.; Sun, L.; Ji, S.; Zhao, D.; Liu, J.; Ma, G.; Su, Z. CO binding improves the structural, functional, physical and anti-oxidation properties of the PEGylated hemoglobin. Artif. Cells Nanomed. Biotechnol., 2015, 43(1), 18-25.
[http://dx.doi.org/10.3109/21691401.2014.885444] [PMID: 24641771]
[78]
Sou, K.; Naito, Y.; Endo, T.; Takeoka, S.; Tsuchida, E. Effective encapsulation of proteins into size-controlled phospholipid vesicles using freeze-thawing and extrusion. Biotechnol. Prog., 2003, 19(5), 1547-1552.
[http://dx.doi.org/10.1021/bp0201004] [PMID: 14524718]
[79]
Sakai, H.; Tomiyama, K.I.; Sou, K.; Takeoka, S.; Tsuchida, E. Poly(ethylene glycol)-conjugation and deoxygenation enable long-term preservation of hemoglobin-vesicles as oxygen carriers in a liquid state. Bioconjug. Chem., 2000, 11(3), 425-432.
[http://dx.doi.org/10.1021/bc990173h] [PMID: 10821660]
[80]
Kure, T.; Sakai, H. Transmembrane difference in colloid osmotic pressure affects the lipid membrane fluidity of liposomes encapsulating a concentrated hemoglobin solution. Langmuir, 2017, 33(6), 1533-1540.
[http://dx.doi.org/10.1021/acs.langmuir.6b04643] [PMID: 28106401]
[81]
Cable, C.A.; Razavi, S.A.; Roback, J.D.; Murphy, D.J. RBC Transfusion Strategies in the ICU: A Concise Review. Crit. Care Med., 2019, 47(11), 1637-1644.
[http://dx.doi.org/10.1097/CCM.0000000000003985] [PMID: 31449062]
[82]
Sakai, H.; Sato, A.; Takeoka, S.; Tsuchida, E. Rheological properties of hemoglobin vesicles (artificial oxygen carriers) suspended in a series of plasma-substitute solutions. Langmuir, 2007, 23(15), 8121-8128.
[http://dx.doi.org/10.1021/la7004503] [PMID: 17567054]
[83]
Takeoka, S.; Ohgushi, T.; Terase, K.; Ohmori, T.; Tsuchida, E. Layer-controlled hemoglobin vesicles by interaction of hemoglobin with a phospholipid assembly. Langmuir, 1996, 12, 1755-1759.
[http://dx.doi.org/10.1021/la940936j]
[84]
Sou, K.; Tsuchida, E. Electrostatic interactions and complement activation on the surface of phospholipid vesicle containing acidic lipids: effect of the structure of acidic groups. Biochim. Biophys. Acta, 2008, 1778(4), 1035-1041.
[http://dx.doi.org/10.1016/j.bbamem.2008.01.006] [PMID: 18242163]
[85]
Takeoka, S.; Teramura, Y.; Atoji, T.; Tsuchida, E. Effect of Hb-encapsulation with vesicles on H2O2 reaction and lipid peroxidation. Bioconjug. Chem., 2002, 13(6), 1302-1308.
[http://dx.doi.org/10.1021/bc025546k] [PMID: 12440866]
[86]
Abe, H.; Azuma, H.; Yamaguchi, M.; Fujihara, M.; Ikeda, H.; Sakai, H.; Takeoka, S.; Tsuchida, E. Effects of hemoglobin vesicles, a liposomal artificial oxygen carrier, on hematological responses, complement and anaphylactic reactions in rats. Artif. Cells Blood Substit. Immobil. Biotechnol., 2007, 35(2), 157-172.
[http://dx.doi.org/10.1080/10731190601188224] [PMID: 17453702]
[87]
Sakai, H.; Suzuki, Y.; Sou, K.; Kano, M. Cardiopulmonary hemodynamic responses to the small injection of hemoglobin vesicles (artificial oxygen carriers) in miniature pigs. J. Biomed. Mater. Res. A, 2012, 100(10), 2668-2677.
[http://dx.doi.org/10.1002/jbm.a.34208] [PMID: 22615268]
[88]
Benesch, R.E.; Yung, S.; Suzuki, T.; Bauer, C.; Benesch, R. Pyridoxal compounds as specific reagents for the alpha and beta N-termini of hemoglobin. Proc. Natl. Acad. Sci. USA, 1973, 70(9), 2595-2599.
[http://dx.doi.org/10.1073/pnas.70.9.2595] [PMID: 4517674]
[89]
Tsai, A.G.; Vandegriff, K.D.; Intaglietta, M.; Winslow, R.M. Targeted O2 delivery by low-P50 hemoglobin: a new basis for O2 therapeutics. Am. J. Physiol. Heart Circ. Physiol., 2003, 285(4), H1411-H1419.
[http://dx.doi.org/10.1152/ajpheart.00307.2003] [PMID: 12805024]
[90]
Yamamoto, M.; Horinouchi, H.; Kobayashi, K.; Seishi, Y.; Sato, N.; Itoh, M.; Sakai, H. Fluid resuscitation of hemorrhagic shock with hemoglobin vesicles in Beagle dogs: pilot study. Artif. Cells Blood Substit. Immobil. Biotechnol., 2012, 40(1-2), 179-195.
[http://dx.doi.org/10.3109/10731199.2011.637929] [PMID: 22288842]
[91]
Sakai, H.; Masada, Y.; Horinouchi, H.; Yamamoto, M.; Ikeda, E.; Takeoka, S.; Kobayashi, K.; Tsuchida, E. Hemoglobin-vesicles suspended in recombinant human serum albumin for resuscitation from hemorrhagic shock in anesthetized rats. Crit. Care Med., 2004, 32(2), 539-545.
[http://dx.doi.org/10.1097/01.CCM.0000109774.99665.22] [PMID: 14758176]
[92]
Terajima, K.; Tsueshita, T.; Sakamoto, A.; Ogawa, R. Fluid resuscitation with hemoglobin vesicles in a rabbit model of acute hemorrhagic shock. Shock, 2006, 25(2), 184-189.
[http://dx.doi.org/10.1097/01.shk.0000192118.68295.5d] [PMID: 16525358]
[93]
Sakai, H.; Seishi, Y.; Obata, Y.; Takeoka, S.; Horinouichi, H.; Tsuchida, E.; Kobayashi, K. Fluid resuscitation with artificial oxygen carriers in hemorrhaged rats: profiles of hemoglobin-vesicle degradation and hematopoiesis for 14 days. Shock, 2009, 31(2), 192-200.
[http://dx.doi.org/10.1097/SHK.0b013e31817d4066] [PMID: 18520699]
[94]
Tokuno, M.; Taguchi, K.; Yamasaki, K.; Sakai, H.; Otagiri, M. Long-term stored hemoglobin-vesicles, a cellular type of hemoglobin-based oxygen carrier, has resuscitative effects comparable to that for fresh red blood cells in a rat model with massive hemorrhage without post-transfusion lung injury. PLoS One, 2016, 11(10), e0165557.
[http://dx.doi.org/10.1371/journal.pone.0165557] [PMID: 27798697]
[95]
Seishi, Y.; Horinouchi, H.; Sakai, H.; Kobayashi, K. Effect of the cellular-type artificial oxygen carrier hemoglobin vesicle as a resuscitative fluid for prehospital treatment: experiments in a rat uncontrolled hemorrhagic shock model. Shock, 2012, 38(2), 153-158.
[http://dx.doi.org/10.1097/SHK.0b013e31825ad7cf] [PMID: 22777109]
[96]
Hagisawa, K.; Kinoshita, M.; Miyawaki, H.; Sato, S.; Miyazaki, H.; Takeoka, S.; Suzuki, H.; Iwaya, K.; Seki, S.; Shono, S.; Saitoh, D.; Nishida, Y.; Handa, M. Fibrinogen γ-Chain Peptide-Coated Adenosine 5′ Diphosphate-Encapsulated Liposomes Rescue Mice From Lethal Blast Lung Injury via Adenosine Signaling. Crit. Care Med., 2016, 44(9), e827-e837.
[http://dx.doi.org/10.1097/CCM.0000000000001707] [PMID: 27054893]
[97]
Hagisawa, K.; Kinoshita, M.; Takase, B.; Hashimoto, K.; Saitoh, D.; Seki, S.; Nishida, Y.; Sakai, H. Efficacy of Resuscitative Transfusion With Hemoglobin Vesicles in the Treatment of Massive Hemorrhage in Rabbits With Thrombocytopenic Coagulopathy and Its Effect on Hemostasis by Platelet Transfusion. Shock, 2018, 50(3), 324-330.
[http://dx.doi.org/10.1097/SHK.0000000000001042] [PMID: 30106387]
[98]
Hagisawa, K.; Kinoshita, M.; Takikawa, M.; Takeoka, S.; Saitoh, D.; Seki, S.; Sakai, H. Combination therapy using fibrinogen γ-chain peptide-coated, ADP-encapsulated liposomes and hemoglobin vesicles for trauma-induced massive hemorrhage in thrombocytopenic rabbits. Transfusion, 2019, 59(10), 3186-3196.
[http://dx.doi.org/10.1111/trf.15427] [PMID: 31257633]
[99]
Hagisawa, K.; Kinoshita, M.; Saitoh, D.; Morimoto, Y.; Sakai, H. Intraosseous transfusion of hemoglobin vesicles in the treatment of hemorrhagic shock with collapsed vessels in a rabbit model. Transfusion, 2020, 60(7), 1400-1409.
[http://dx.doi.org/10.1111/trf.15915] [PMID: 32579275]
[100]
Yuki, Y.; Hagisawa, K.; Kinoshita, M.; Ishibashi, H.; Ishida, O.; Saitoh, D.; Sakai, H.; Terui, K. Efficacy of Resuscitative Transfusion with Hemoglobin Vesicles in the Management of Massive Obstetric Hemorrhage. Am. J. Obstet. Gynecol., 2021, 224(4), 398.e1-398.e11.
[http://dx.doi.org/10.1016/j.ajog.2020.09.010] [PMID: 32926859]
[101]
Adachi, T.; Hori, S.; Miyazaki, K.; Nakagawa, M.; Inoue, S.; Ohnishi, Y.; Nakazawa, H.; Aikawa, N.; Ogawa, S. Inhibition of nitric oxide synthesis aggravates myocardial ischemia in hemorrhagic shock in constant pressure model. Shock, 1998, 9(3), 204-209.
[http://dx.doi.org/10.1097/00024382-199803000-00008] [PMID: 9525328]
[102]
Thacker, S.A.; Robinson, P.; Abel, A.; Tweardy, D.J. Modulation of the unfolded protein response during hepatocyte and cardiomyocyte apoptosis in trauma/hemorrhagic shock. Sci. Rep., 2013, 3, 1187.
[http://dx.doi.org/10.1038/srep01187] [PMID: 23378918]
[103]
Kreimeier, U.; Messmer, K. Perioperative hemodilution. Transfus. Apheresis Sci., 2002, 27(1), 59-72.
[http://dx.doi.org/10.1016/S1473-0502(02)00027-7] [PMID: 12201472]
[104]
Takase, B.; Higashimura, Y.; Hashimoto, K.; Asahina, H.; Ishihara, M.; Sakai, H. Myocardial Electrical Remodeling and the Arrhythmogenic Substrate in Hemorrhagic Shock-Induced Heart: Anti-Arrhythmogenic Effect of Liposome-Encapsulated Hemoglobin (HbV) on the Myocardium. Shock, 2019, 52(3), 378-386.
[http://dx.doi.org/10.1097/SHK.0000000000001262] [PMID: 30239419]
[105]
Motterlini, R.; Foresti, R. Biological signaling by carbon monoxide and carbon monoxide-releasing molecules. Am. J. Physiol. Cell Physiol., 2017, 312(3), C302-C313.
[http://dx.doi.org/10.1152/ajpcell.00360.2016] [PMID: 28077358]
[106]
El Ali, Z.; Ollivier, A.; Manin, S.; Rivard, M.; Motterlini, R.; Foresti, R. Therapeutic effects of CO-releaser/Nrf2 activator hybrids (HYCOs) in the treatment of skin wound, psoriasis and multiple sclerosis. Redox Biol., 2020, 34, 101521.
[http://dx.doi.org/10.1016/j.redox.2020.101521] [PMID: 32335359]
[107]
Berrino, E.; Carradori, S.; Angeli, A.; Carta, F.; Supuran, C.T.; Guglielmi, P.; Coletti, C.; Paciotti, R.; Schweikl, H.; Maestrelli, F.; Cerbai, E.; Gallorini, M. Dual Carbonic Anhydrase IX/XII Inhibitors and Carbon Monoxide Releasing Molecules Modulate LPS-Mediated Inflammation in Mouse Macrophages. Antioxidants, 2021, 10(1), 56.
[http://dx.doi.org/10.3390/antiox10010056] [PMID: 33466457]
[108]
Opoku-Damoah, Y.; Zhang, R.; Ta, H.T.; Amilan Jose, D.; Sakla, R.; Xu, Z.P. Lipid-encapsulated upconversion nanoparticle for near-infrared light-mediated carbon monoxide release for cancer gas therapy. Eur. J. Pharm. Biopharm., 2021, 158, 211-221.
[http://dx.doi.org/10.1016/j.ejpb.2020.11.014] [PMID: 33276086]
[109]
Lazarus, L.S.; Benninghoff, A.D.; Berreau, L.M. Development of Triggerable, Trackable, and Targetable Carbon Monoxide Releasing Molecules. Acc. Chem. Res., 2020, 53(10), 2273-2285.
[http://dx.doi.org/10.1021/acs.accounts.0c00402] [PMID: 32929957]
[110]
Sakai, H.; Horinouchi, H.; Tsuchida, E.; Kobayashi, K. Hemoglobin vesicles and red blood cells as carriers of carbon monoxide prior to oxygen for resuscitation after hemorrhagic shock in a rat model. Shock, 2009, 31(5), 507-514.
[http://dx.doi.org/10.1097/SHK.0b013e318188f83d] [PMID: 18827742]
[111]
Nagao, S.; Taguchi, K.; Miyazaki, Y.; Wakayama, T.; Chuang, V.T.; Yamasaki, K.; Watanabe, H.; Sakai, H.; Otagiri, M.; Maruyama, T. Evaluation of a new type of nano-sized carbon monoxide donor on treating mice with experimentally induced colitis. J. Control. Release, 2016, 234, 49-58.
[http://dx.doi.org/10.1016/j.jconrel.2016.05.016] [PMID: 27173944]
[112]
Nagao, S.; Taguchi, K.; Sakai, H.; Tanaka, R.; Horinouchi, H.; Watanabe, H.; Kobayashi, K.; Otagiri, M.; Maruyama, T. Carbon monoxide-bound hemoglobin-vesicles for the treatment of bleomycin-induced pulmonary fibrosis. Biomaterials, 2014, 35(24), 6553-6562.
[http://dx.doi.org/10.1016/j.biomaterials.2014.04.049] [PMID: 24811261]
[113]
Taguchi, K.; Nagao, S.; Maeda, H.; Yanagisawa, H.; Sakai, H.; Yamasaki, K.; Wakayama, T.; Watanabe, H.; Otagiri, M.; Maruyama, T. Biomimetic carbon monoxide delivery based on hemoglobin vesicles ameliorates acute pancreatitis in mice via the regulation of macrophage and neutrophil activity. Drug Deliv., 2018, 25(1), 1266-1274.
[http://dx.doi.org/10.1080/10717544.2018.1477860] [PMID: 29847178]
[114]
Taguchi, K.; Ogaki, S.; Nagasaki, T.; Yanagisawa, H.; Nishida, K.; Maeda, H.; Enoki, Y.; Matsumoto, K.; Sekijima, H.; Ooi, K.; Ishima, Y.; Watanabe, H.; Fukagawa, M.; Otagiri, M.; Maruyama, T. Carbon Monoxide Rescues the Developmental Lethality of Experimental Rat Models of Rhabdomyolysis-Induced Acute Kidney Injury. J. Pharmacol. Exp. Ther., 2020, 372(3), 355-365.
[http://dx.doi.org/10.1124/jpet.119.262485] [PMID: 31924689]
[115]
Cabrales, P.; Tsai, A.G.; Intaglietta, M. Hemorrhagic shock resuscitation with carbon monoxide saturated blood. Resuscitation, 2007, 72(2), 306-318.
[http://dx.doi.org/10.1016/j.resuscitation.2006.06.021] [PMID: 17092627]
[116]
Shikama, K. The Molecular Mechanism of Autoxidation for Myoglobin and Hemoglobin: A Venerable Puzzle. Chem. Rev., 1998, 98(4), 1357-1374.
[http://dx.doi.org/10.1021/cr970042e] [PMID: 11848936]
[117]
Sakai, H.; Li, B.; Lim, W.L.; Iga, Y. Red blood cells donate electrons to methylene blue mediated chemical reduction of methemoglobin compartmentalized in liposomes in blood. Bioconjug. Chem., 2014, 25(7), 1301-1310.
[http://dx.doi.org/10.1021/bc500153x] [PMID: 24877769]
[118]
Nagai, M.; Yubisui, T.; Yoneyama, Y. Enzymatic reduction of hemoglobins M Milwaukee-1 and M Saskatoon by NADH-cytochrome b5 reductase and NADPH-flavin reductase purified from human erythrocytes. J. Biol. Chem., 1980, 255(10), 4599-4602.
[http://dx.doi.org/10.1016/S0021-9258(19)85536-9] [PMID: 7372598]
[119]
Bradberry, S.M. Occupational methaemoglobinaemia. Mechanisms of production, features, diagnosis and management including the use of methylene blue. Toxicol. Rev., 2003, 22(1), 13-27.
[http://dx.doi.org/10.2165/00139709-200322010-00003] [PMID: 14579544]
[120]
Katabami, K.; Hayakawa, M.; Gando, S. Severe Methemoglobinemia due to Sodium Nitrite Poisoning. Case Rep. Emerg. Med., 2016, 2016, 9013816.
[http://dx.doi.org/10.1155/2016/9013816] [PMID: 27563472]
[121]
Sakai, H.; Leong, C. Prolonged functional life span of artificial red cells in blood circulation by repeated methylene blue injections. Artif. Cells Nanomed. Biotechnol., 2019, 47(1), 3123-3128.
[http://dx.doi.org/10.1080/21691401.2019.1645157] [PMID: 31352837]
[122]
Paul, P.; Mati, S.S.; Bhattacharya, S.C.; Kumar, G.S. Exploring the interaction of phenothiazinium dyes methylene blue, new methylene blue, azure A and azure B with tRNAPhe: spectroscopic, thermodynamic, voltammetric and molecular modeling approach. Phys. Chem. Chem. Phys., 2017, 19(9), 6636-6653.
[http://dx.doi.org/10.1039/C6CP07888E] [PMID: 28210726]
[123]
Kettisen, K.; Bülow, L.; Sakai, H. Potential electron mediators to extract electron energies of RBC glycolysis for prolonged in vivo functional lifetime of hemoglobin vesicles. Bioconjug. Chem., 2015, 26(4), 746-754.
[http://dx.doi.org/10.1021/acs.bioconjchem.5b00076] [PMID: 25734688]
[124]
Ghirmai, S.; Bülow, L.; Sakai, H. In vivo evaluation of electron mediators for the reduction of methemoglobin encapsulated in liposomes using electron energies produced by red blood cell glycolysis. Artif. Cells Nanomed. Biotechnol., 2018, 46(7), 1364-1372.
[http://dx.doi.org/10.1080/21691401.2017.1397003] [PMID: 29103319]
[125]
Fultz, M.L.; Durst, R.A. Mediator compounds for the electrochemical study of biological redox systems: a compilation. Anal. Chim. Acta, 1982, 140, 1-18.
[http://dx.doi.org/10.1016/S0003-2670(01)95447-9]
[126]
Sakai, H.; Masada, Y.; Horinouchi, H.; Ikeda, E.; Sou, K.; Takeoka, S.; Suematsu, M.; Takaori, M.; Kobayashi, K.; Tsuchida, E. Physiological capacity of the reticuloendothelial system for the degradation of hemoglobin vesicles (artificial oxygen carriers) after massive intravenous doses by daily repeated infusions for 14 days. J. Pharmacol. Exp. Ther., 2004, 311(3), 874-884.
[http://dx.doi.org/10.1124/jpet.104.073049] [PMID: 15297471]
[127]
Taguchi, K.; Watanabe, H.; Sakai, H.; Horinouchi, H.; Kobayashi, K.; Maruyama, T.; Otagiri, M. A fourteen-day observation and pharmacokinetic evaluation after a massive intravenous infusion of hemoglobin-vesicles (artificial oxygen carriers) in cynomolgus monkeys. J. Drug Metab. Toxicol., 2012, 3, 128.
[http://dx.doi.org/10.4172/2157-7609.1000128]
[128]
Taguchi, K.; Urata, Y.; Anraku, M.; Watanabe, H.; Kadowaki, D.; Sakai, H.; Horinouchi, H.; Kobayashi, K.; Tsuchida, E.; Maruyama, T.; Otagiri, M. Hemoglobin vesicles, polyethylene glycol (PEG)ylated liposomes developed as a red blood cell substitute, do not induce the accelerated blood clearance phenomenon in mice. Drug Metab. Dispos., 2009, 37(11), 2197-2203.
[http://dx.doi.org/10.1124/dmd.109.028852] [PMID: 19679674]
[129]
Cooper, C.E.; Silkstone, G.G.A.; Simons, M.; Rajagopal, B.; Syrett, N.; Shaik, T.; Gretton, S.; Welbourn, E.; Bülow, L.; Eriksson, N.L.; Ronda, L.; Mozzarelli, A.; Eke, A.; Mathe, D.; Reeder, B.J. Engineering tyrosine residues into hemoglobin enhances heme reduction, decreases oxidative stress and increases vascular retention of a hemoglobin based blood substitute. Free Radic. Biol. Med., 2019, 134, 106-118.
[http://dx.doi.org/10.1016/j.freeradbiomed.2018.12.030] [PMID: 30594736]
[130]
Cooper, C.E.; Silaghi-Dumitrescu, R.; Rukengwa, M.; Alayash, A.I.; Buehler, P.W. Peroxidase activity of hemoglobin towards ascorbate and urate: a synergistic protective strategy against toxicity of Hemoglobin-Based Oxygen Carriers (HBOC). Biochim. Biophys. Acta, 2008, 1784(10), 1415-1420.
[http://dx.doi.org/10.1016/j.bbapap.2008.03.019] [PMID: 18457681]
[131]
Yan, W.; Shen, L.; Yu, W.; Wang, Y.; Wang, Q.; You, G.; Zhao, L.; Zhou, H.; Hu, T. A triply modified human adult hemoglobin with low oxygen affinity, rapid autoxidation and high tetramer stability. Int. J. Biol. Macromol., 2020, 159, 236-242.
[http://dx.doi.org/10.1016/j.ijbiomac.2020.05.007] [PMID: 32387364]
[132]
Jani, V.P.; Jelvani, A.; Moges, S.; Nacharaju, P.; Roche, C.; Dantsker, D.; Palmer, A.; Friedman, J.M.; Cabrales, P. Polyethylene Glycol Camouflaged Earthworm Hemoglobin. PLoS One, 2017, 12(1), e0170041.
[http://dx.doi.org/10.1371/journal.pone.0170041] [PMID: 28099525]
[133]
Araki, J.; Sakai, H.; Takeuchi, D.; Kagaya, Y.; Tashiro, K.; Naito, M.; Mihara, M.; Narushima, M.; Iida, T.; Koshima, I. Normothermic preservation of the rat hind limb with artificial oxygen-carrying hemoglobin vesicles. Transplantation, 2015, 99(4), 687-692.
[http://dx.doi.org/10.1097/TP.0000000000000528] [PMID: 25606798]
[134]
Shonaka, T.; Matsuno, N.; Obara, H.; Yoshikawa, R.; Nishikawa, Y.; Ishihara, Y.; Bochimoto, H.; Gochi, M.; Otani, M.; Kanazawa, H.; Azuma, H.; Sakai, H.; Furukawa, H. Impact of human-derived hemoglobin based oxygen vesicles as a machine perfusion solution for liver donation after cardiac death in a pig model. PLoS One, 2019, 14(12), e0226183.
[http://dx.doi.org/10.1371/journal.pone.0226183] [PMID: 31825976]
[135]
Rikihisa, N.; Tominaga, M.; Watanabe, S.; Mitsukawa, N.; Saito, Y.; Sakai, H. Intravenous injection of artificial red cells and subsequent dye laser irradiation causes deep vessel impairment in an animal model of port-wine stain. Lasers Med. Sci., 2018, 33(6), 1287-1293.
[http://dx.doi.org/10.1007/s10103-018-2480-2] [PMID: 29546617]
[136]
Kobayashi, M.; Mori, T.; Kiyono, Y.; Tiwari, V.N.; Maruyama, R.; Kawai, K.; Okazawa, H. Cerebral oxygen metabolism of rats using injectable (15)O-oxygen with a steady-state method. J. Cereb. Blood Flow Metab., 2012, 32(1), 33-40.
[http://dx.doi.org/10.1038/jcbfm.2011.125] [PMID: 21863038]
[137]
Nakajima, J.; Bessho, M.; Adachi, T.; Yamagishi, T.; Tokuno, S.; Horinouchi, H.; Ohsuzu, F. Hemoglobin vesicle improves recovery of cardiac function after ischemia-reperfusion by attenuating oxidative stress in isolated rat hearts. J. Cardiovasc. Pharmacol., 2011, 58(5), 528-534.
[http://dx.doi.org/10.1097/FJC.0b013e31822de06e] [PMID: 21795989]
[138]
Komatsu, H.; Furuya, T.; Sato, N.; Ohta, K.; Matsuura, A.; Ohmura, T.; Takagi, S.; Matsuura, M.; Yamashita, M.; Itoda, M.; Itoh, J.; Horinouchi, H.; Kobayashi, K. Effect of hemoglobin vesicle, a cellular-type artificial oxygen carrier, on middle cerebral artery occlusion- and arachidonic acid-induced stroke models in rats. Neurosci. Lett., 2007, 421(2), 121-125.
[http://dx.doi.org/10.1016/j.neulet.2007.04.080] [PMID: 17566655]
[139]
Li, H.; Ohta, H.; Tahara, Y.; Nakamura, S.; Taguchi, K.; Nakagawa, M.; Oishi, Y.; Goto, Y.; Wada, K.; Kaga, M.; Inagaki, M.; Otagiri, M.; Yokota, H.; Shibata, S.; Sakai, H.; Okamura, K.; Yaegashi, N. Artificial oxygen carriers rescue placental hypoxia and improve fetal development in the rat pre-eclampsia model. Sci. Rep., 2015, 5, 15271.
[http://dx.doi.org/10.1038/srep15271] [PMID: 26471339]
[140]
Yamamoto, M.; Izumi, Y.; Horinouchi, H.; Teramura, Y.; Sakai, H.; Kohno, M.; Watanabe, M.; Kawamura, M.; Adachi, T.; Ikeda, E.; Takeoka, S.; Tsuchida, E.; Kobayashi, K. Systemic administration of hemoglobin vesicle elevates tumor tissue oxygen tension and modifies tumor response to irradiation. J. Surg. Res., 2009, 151(1), 48-54.
[http://dx.doi.org/10.1016/j.jss.2007.12.770] [PMID: 18262559]
[141]
Stucki, D.; Stahl, W. Carbon monoxide - beyond toxicity? Toxicol. Lett., 2020, 333, 251-260.
[http://dx.doi.org/10.1016/j.toxlet.2020.08.010] [PMID: 32860873]
[142]
Jang, D.H.; Piel, S.; Greenwood, J.C.; Kelly, M.; Mazandi, V.M.; Ranganathan, A.; Lin, Y.; Starr, J.; Hallowell, T.; Shofer, F.S.; Baker, W.B.; Lafontant, A.; Andersen, K.; Ehinger, J.K.; Kilbaugh, T.J. Alterations in cerebral and cardiac mitochondrial function in a porcine model of acute carbon monoxide poisoning. Clin. Toxicol. (Phila.), 2021, 2, 1-14.
[http://dx.doi.org/10.1080/15563650.2020.1870691] [PMID: 33529085]

Rights & Permissions Print Cite
Article Metrics
22
2
© 2024 Bentham Science Publishers | Privacy Policy