Optimizing the lyophilization of Lumbricus terrestris erythrocruorin

References

• Cannon JW. Hemorrhagic shock. N Engl J Med. 2018;378(4):370–379. doi:10.1056/NEJMra1705649.
   PubMed Web of Science ®Google Scholar
• Burgess FW, Sborov MJ, Calcagni DR. Hemorrhage, shock, and fluid resuscitation. In: Zajtchuk R, Grande CM, editors. Anesthesia and perioperative care of the combat casualty. 1st ed. Washington, D.C.: Office of the Surgen General at TMM Publications Borden Institute; 1995. p. 81–100.
   Google Scholar
• Gurney JM, Le TD, Becker TE, et al. Epidemiology if hemorrhagic shock. In: Pascual JL, Cannon JW, editors. Hemorrhagic shock. 1st ed. New York, NY: Nova Science Publishers, Inc.; 2017. p. 1–17.
   Google Scholar
• Kim-Shapiro DB, Lee J, Gladwin MT. Storage lesion: role of red blood cell breakdown. Transfusion (Paris). 2011;51(4):844–851. doi:10.1111/j.1537-2995.2011.03100.x.
   PubMed Web of Science ®Google Scholar
• Malsby RF, Quesada J, Powell-Dunford N, et al. Prehospital blood product transfusion by U.S. Army MEDEVAC during combat operations in Afghanistan: a process improvement initiative. Mil Med. 2013;178(7):785–791. doi:10.7205/MILMED-D-13-00047.
   PubMed Web of Science ®Google Scholar
• Spinella PC, Dunne J, Beilman GJ, et al. Constant challenges and evolution of US military transfusion medicine and blood operations in combat. Transfusion (Paris). 2012;52(5):1146–1153. doi:10.1111/j.1537-2995.2012.03594.x.
   Web of Science ®Google Scholar
• Pusateri AE, Given MB, Schreiber MA, et al. Dried plasma: state of the science and recent developments. Transfusion (Paris). 2016;56(Suppl 2):S128–S139. doi:10.1111/trf.13580.
   Google Scholar
• Bowersox JC, Hess JR. Trauma and military applications of blood substitutes. Artif Cells Blood Substit Immobil Biotechnol. 1994;22(2):145–157. doi:10.3109/10731199409117410.
   PubMed Web of Science ®Google Scholar
• Matsuhira T, Sakai H. Artificial oxygen carriers, from nanometer- to micrometer-sized particles, made of hemoglobin composites substituting for red blood cells. Particuology. 2021;64:43–55. doi:10.1016/j.partic.2021.08.010.
   Web of Science ®Google Scholar
• Elmer J, Palmer AF. Biophysical properties of Lumbricus terrestris erythrocruorin and its potential use as a red blood cell substitute. J Funct Biomater. 2012;3(1):49–60. doi:10.3390/jfb3010049.
   PubMedGoogle Scholar
• Muzzelo C, Neely C, Shah P, et al. Prolonging the shelf life of Lumbricus terrestris erythrocruorin for use as a novel blood substitute. Artif Cells Nanomed Biotechnol. 2018;46(1):39–46. doi:10.1080/21691401.2017.1290645.
   PubMed Web of Science ®Google Scholar
• Elmer J, Harris D, Palmer AF. Purification of hemoglobin from red blood cells using tangential flow filtration and immobilized metal ion affinity chromatography. J Chromatogr B Analyt Technol Biomed Life Sci. 2011;879(2):131–138. doi:10.1016/j.jchromb.2010.11.021.
   PubMed Web of Science ®Google Scholar
• Elmer J, Palmer AF, Cabrales P. Oxygen delivery during extreme anemia with ultra-pure earthworm hemoglobin. Life Sci. 2012;91(17–18):852–859. doi:10.1016/j.lfs.2012.08.036.
   PubMed Web of Science ®Google Scholar
• Elmer J, Zorc K, Rameez S, et al. Hypervolemic infusion of Lumbricus terrestris erythrocruorin purified by tangential-flow filtration. Transfusion (Paris). 2012;52(8):1729–1740. doi:10.1111/j.1537-2995.2011.03523.x.
   Web of Science ®Google Scholar
• Fernandez-Moure J, Maisha N, Lavik EB, et al. The chemistry of lyophilized blood products. Bioconjug Chem. 2018;29(7):2150–2160. doi:10.1021/acs.bioconjchem.8b00271.
   PubMed Web of Science ®Google Scholar
• Maher P, Utarnachitt R, Louzon MJ, et al. Logistical concerns for prehospital blood product use by air medical services. Air Med J. 2017;36(5):263–267. doi:10.1016/j.amj.2017.05.003.
   PubMedGoogle Scholar
• Goodrich RP, Sowemimo-Coker SO, Zerez CR, et al. Preservation of metabolic activity in lyophilized human erythrocytes. Proc Natl Acad Sci U S A. 1992;89(3):967–971. doi:10.1073/pnas.89.3.967.
   PubMed Web of Science ®Google Scholar
• Butreddy A, Janga KY, Ajjarapu S, et al. Instability of therapeutic proteins—an overview of stresses, stabilization mechanisms and analytical techniques involved in lyophilized proteins. Int J Biol Macromol. 2021;167:309–325. doi:10.1016/j.ijbiomac.2020.11.188.
   PubMed Web of Science ®Google Scholar
• Franks F. Freeze-drying of bioproducts: putting principles into practice. Eur J Pharm Biopharm. 1998;45(3):221–229. doi:10.1016/s0939-6411(98)00004-6.
   PubMed Web of Science ®Google Scholar
• Sailliol A, Martinaud C, Cap AP, et al. The evolving role of lyophilized plasma in remote damage control resuscitation in the French armed forces health service. Transfusion (Paris). 2013;53(Suppl 1):65S–71S. doi:10.1111/trf.12038.
   Google Scholar
• Iijima T. Thermal analysis of cryoprotective solutions for red blood cells. Cryobiology. 1998;36(3):165–173. doi:10.1006/cryo.1998.2075.
   PubMed Web of Science ®Google Scholar
• Chao H, Davies PL, Carpenter JF. Effects of antifreeze proteins on red blood cell survival during cryopreservation. J Exp Biol. 1996;199(Pt 9):2071–2076. doi:10.1242/jeb.199.9.2071.
   PubMed Web of Science ®Google Scholar
• Mazur P. Freezing of living cells: mechanisms and implications. Am J Physiol. 1984;247(3 Pt 1):C125–C142. doi:10.1152/ajpcell.1984.247.3.C125.
   PubMed Web of Science ®Google Scholar
• Meryman HT. Freezing injury and its prevention in living cells. Annu Rev Biophys Bioeng. 1974;3(0):341–363. doi:10.1146/annurev.bb.03.060174.002013.
   PubMedGoogle Scholar
• Lovelock JE. The mechanism of the protective action of glycerol against haemolysis by freezing and thawing. Biochim Biophys Acta. 1953;11(1):28–36. doi:10.1016/0006-3002(53)90005-5.
   PubMedGoogle Scholar
• Zal F, Rousselot M. Annelid haemoglobin lyophilisation process. USA: US Patent & Trademark Office; 2020.
   Google Scholar
• Chintala R, Bhambhani A. HPV vaccine formulations comprising aluminum adjuvant and methods of producing same [internet]. US Patent App. 14/126,992. USA: US Patent & Trademark Office; 2020. Available from: http://www.google.com/patents/US20140127260.
   Google Scholar
• McAleer WJ, Markus HZ. Lyophilization process for live viral compositions [internet]. USA: US Patent & Trademark Office; 1981. Available from: https://patents.google.com/patent/US4273762A/en.
   Google Scholar
• Akers MJ, Vasudevan V, Stickelmeyer M. Formulation development of protein dosage forms. Pharm Biotechnol. 2002;14:47–127. doi:10.1007/978-1-4615-0549-5_2.
   PubMedGoogle Scholar
• Patapoff TW, Overcashier DE. The importance of freezing on lyophilization cycle development. BioPharm. 2002;15:16–21 + 72.
   Google Scholar
• Zal F, Rousselot M. Annelid haemoglobin lyophilisation process. European Union: European Patent Office; 2018.
   Google Scholar
• Savla C, Palmer AF. Lyophilized annelid mega-hemoglobin retains its’ quaternary structure and oxygen equilibrium properties after room temperature storage for over 6 months. PLoS One. 2022;17(2):e0263996. doi:10.1371/journal.pone.0263996.
   PubMed Web of Science ®Google Scholar
• Zimmerman D, Dienes J, Abdulmalik O, et al. Purification of diverse hemoglobins by metal salt precipitation. Protein Expr Purif. 2015;125:74–82. doi:10.1016/j.pep.2015.09.006.
   PubMed Web of Science ®Google Scholar
• Timm B, Elmer J. Enhancing the stability of Lumbricus terrestris erythrocruorin (LtEc) for use as a blood substitute. International Symposium for Blood Substitutes 2017 Review; 2019. p. 3093.
   Google Scholar
• Schwegman JJ, Hardwick LM, Akers MJ. Practical formulation and process development of Freeze-Dried products. Pharm Dev Technol. 2005;10(2):151–173. doi:10.1081/pdt-56308.
   PubMed Web of Science ®Google Scholar
• Heller MC, Carpenter JF, Randolph TW. Protein formulation and lyophilization cycle design: prevention of damage due to freeze-concentration induced phase separation. Biotechnol Bioeng. 1999;63(2):166–174. doi:10.1002/(SICI)1097-0290(19990420)63:2<166::AID-BIT5>3.0.CO;2-H.
   PubMed Web of Science ®Google Scholar
• Koike Y, Tomono Y, Tanaka H, et al. The possible effects of the aggregation of the molecules of hemoglobin on its dissociation curves. J Physiol. 1910;40:iv–vii. Available from: https://cir.nii.ac.jp/crid/1571980074887256960.
   Google Scholar
• Rajesh A, Zimmerman D, Spivack K, et al. Glutaraldehyde cross-linking increases the stability of Lumbricus terrestris erythrocruorin. Biotechnol Prog. 2018;34(2):521–528. doi:10.1002/btpr.2593.
   PubMed Web of Science ®Google Scholar
• Spivack K, Tucker M, Zimmerman D, et al. Increasing the stability of lumbricus terrestris erythrocruorin via poly(acrylic acid) conjugation. Artif Cells Nanomed Biotechnol. 2018;46(sup2):1137–1144. doi:10.1080/21691401.2018.1480491.
   PubMed Web of Science ®Google Scholar
• Zimmerman D, DiIusto M, Dienes J, et al. Direct comparison of oligochaete erythrocruorins as potential blood substitutes. Bioeng Transl Med. 2017;2(2):212–221. doi:10.1002/btm2.10067.
   PubMed Web of Science ®Google Scholar
• Edelstein SJ. Cooperative interactions of hemoglobin. Annu Rev Biochem. 1975;44(1):209–232. doi:10.1146/annurev.bi.44.070175.001233.
   PubMedGoogle Scholar
• Carver TE, Brantley RE, Singleton EW, et al. A novel site-directed mutant of myoglobin with an unusually high O2 affinity and low autooxidation rate. J Biol Chem. 1992;267(20):14443–14450. doi:10.1016/S0021-9258(19)49732-9.
   PubMed Web of Science ®Google Scholar
• Bitensky MW, Yoshida T. Blood storage device and method for oxygen removal. USA: USPTO; 2000.
   Google Scholar
• Zolla L, D’Alessandro A. An efficient apparatus for rapid deoxygenation of erythrocyte concentrates for alternative banking strategies. J Blood Transfus. 2013;2013:896537–896538. doi:10.1155/2013/896537.
   PubMedGoogle Scholar
• Panjwani D, Li MLJ. Methemoglobinemi. In: Mattu A, Chanmugam AS, Swadron SP, et al., editors. Avoiding common errors in the emergency department. 2nd ed. Waltham, MA: Wolters Kluwer; 2017. p. 827–829.
   Google Scholar
• Wright RO, Lewander WJ, Woolf AD. Methemoglobinemia: etiology, pharmacology, and clinical management. Ann Emerg Med. 1999;34(5):646–656. doi:10.1016/s0196-0644(99)70167-8.
   PubMed Web of Science ®Google Scholar
• Costello JF, Plass C. Methylation matters. J Med Genet. 2001;38(5):285–303. Available from: www.jmedgenet.com. doi:10.1136/jmg.38.5.285.
   PubMed Web of Science ®Google Scholar
• Tomoda A, Takeshita M, Yoneyama Y. Characterization of intermediate hemoglobin produced during methemoglobin reduction by ascorbic acid; 1978.
   Google Scholar
• Dela Cruz M, Glick J, Merker SH, et al. Survival after severe methemoglobinemia secondary to sodium nitrate ingestion. Toxicol Commun. 2018;2(1):21–23. doi:10.1080/24734306.2018.1467532.
   Google Scholar
• Ludlow JT, Wilkerson RG, Nappe TM. Methemoglobinemia. StatPearls. Treasure Island, FL: StatPearls Publishing LLC; 2023.
   Google Scholar
• Institute of Medicine F and NB. Vitamin C. In: Institute of Medicine F and NB. editor. Dietary reference intakes for vitamin C, vitamin E, selenium, and carotenoids [internet]. Washington, DC: National Academy Press; 2000. p. 95–186. Available from: https://www.ebsco.com/terms-of-use.
   Google Scholar
• Sulaiman S, Heis Z, Jahangir A. Drug-Nutrient Interactions in the Elderly. In: Malavolta M, Mocchegiani E, eds. Molecular Basis of Nutrition and Aging. 1st ed. San Diego, CA: Academic Press; 2016:73–107.
   Google Scholar
• Bianchi J, Rose RC. Dehydroascorbic acid and cell membranes: possible disruptive effects. Toxicology. 1986;40(1):75–82. doi:10.1016/0300-483x(86)90047-8.
   PubMed Web of Science ®Google Scholar
• ThermoFisher Scientific. Ascorbic Acid Safety Data Sheet. 2021.
   Google Scholar
• Cayman Chemicals. Dehydroascorbic Acid Safety Data Sheet. 2019.
   Google Scholar
• Woodson LC, Sherwood ER, Aarsland A, et al. Anesthesia for burned patients. In: Herndon DN, editor. Total burn care: expert consult. 4th ed. Philadelphia, PA: Elsevier, Inc.; 2012. p. 194.
   Google Scholar
• Manjula BN, Acharya SA. Hemoglobin disorders molecular methods and protocols. In: Nagel RL, editor. Hemoglobin disorders: molecular methods and protocols. Totowa, NJ: Humana Press; 2003. p. 31–47.
   Google Scholar
• Nguyen TQ. Interactions of human hemoglobin with high‐molecular‐weight dextran sulfate and diethylaminoethyl dextran. Makromol Chem. 1986;187(11):2567–2578. doi:10.1002/macp.1986.021871106.
   Web of Science ®Google Scholar
• Ardin S, Störmer M, Radojska S, et al. Comparison of three noninvasive methods for hemoglobin screening of blood donors. Transfusion (Paris). 2015;55(2):379–387. doi:10.1111/trf.12819.
   PubMed Web of Science ®Google Scholar
• Hospira. Mannitol injection, for intravenous use [Internet]. 2020. Available from: www.fda.gov/medwatch.
   Google Scholar
• Cayman Chemical. Mannitol Safety Data Sheet. 2022.
   Google Scholar
• VWR Canada. Sucrose Safety Data Sheet. 2009.
   Google Scholar
• Song BK, Nugent WH, Moon-Massat PF, et al. Effects of a hemoglobin-based oxygen carrier (HBOC-201) and derivatives with altered oxygen affinity and viscosity on systemic and microcirculatory variables in a top-load rat model. Microvasc Res. 2014;95:124–130. doi:10.1016/j.mvr.2014.07.005.
   PubMed Web of Science ®Google Scholar