The discovery of berberine erythrocyte-hemoglobin self-assembly delivery system: a neglected carrier underlying its pharmacokinetics

References

• Allen TM, Cullis PR. (2004). Drug delivery systems: Entering the mainstream. Science 303:1818–22.
   PubMed Web of Science ®Google Scholar
• Atkins CG, Buckley K, Blades MW, et al. (2017). Raman Spectroscopy of blood and blood components. Appl Spectrosc 71:767–93.
   PubMed Web of Science ®Google Scholar
• Bao X, Zhu Z, Li NQ, et al. (2001). Electrochemical studies of rutin interacting with hemoglobin and determination of hemoglobin. Talanta 54:591–6.
   PubMed Web of Science ®Google Scholar
• Basu A, Suresh Kumar G. (2015). Binding of carmoisine, a food colorant, with hemoglobin: spectroscopic and calorimetric studies. Food Res Int 72:54–61.
   Web of Science ®Google Scholar
• Berikkhanova K, Omarbaev R, Gulyayev A, et al. (2016). Red blood cell ghosts as promising drug carriers to target wound infections. Med Eng Phys 38:877–84.
   PubMed Web of Science ®Google Scholar
• Borkar RM, Bhandi MM, Dubey AP, et al. (2015). Plasma protein binding, pharmacokinetics, tissue distribution and CYP450 biotransformation studies of fidarestat by ultra high performance liquid chromatography-high resolution mass spectrometry. J Pharm Biomed Anal 102:386–99.
   PubMed Web of Science ®Google Scholar
• Cai Z, Wang C, Yang W. (2016). Role of berberine in Alzheimer's disease. Neuropsychiatr Dis Treat 12:2509–20.
   PubMed Web of Science ®Google Scholar
• Chen HB, Luo CD, Ai GX, et al. (2021). A comparative investigation of the interaction and pharmacokinetics of hemoglobin with berberine and its oxymetabolite. J Pharm Biomed Anal 199:114032.
   PubMed Web of Science ®Google Scholar
• Chen W, Miao YQ, Fan DJ, et al. (2011). Bioavailability study of berberine and the enhancing effects of TPGS on intestinal absorption in rats. Aaps Pharmscitech 12:705–11.
   PubMed Web of Science ®Google Scholar
• Cicero AF, Baggioni A. (2016). Berberine and its role in chronic disease. Adv Exp Med Biol 928:27–45.
   PubMed Web of Science ®Google Scholar
• Dou Y, Huang R, Li Q, et al. (2021). Oxyberberine, an absorbed metabolite of berberine, possess superior hypoglycemic effect via regulating the PI3K/Akt and Nrf2 signaling pathways. Biomed Pharmacother 137:111312.
   PubMed Web of Science ®Google Scholar
• Dybas J, Chiura T, Marzec KM, Mak PJ. (2021). Probing heme active sites of hemoglobin in functional red blood cells using resonance Raman Spectroscopy. J Phys Chem B 125:3556–65.
   PubMed Web of Science ®Google Scholar
• Fan NC, Cheng FY, Ho JA, et al. (2012a). Photocontrolled targeted drug delivery: photocaged biologically active folic acid as a light-responsive tumor-targeting molecule. Angew Chem Int Ed Engl 51:8806–10.
   PubMed Web of Science ®Google Scholar
• Fan W, Yan W, Xu Z, et al. (2012b). Erythrocytes load of low molecular weight chitosan nanoparticles as a potential vascular drug delivery system. Colloids Surf B Biointerfaces 95:258–65.
   PubMed Web of Science ®Google Scholar
• Feng X, Sureda A, Jafari S, et al. (2019). Berberine in cardiovascular and metabolic diseases: from mechanisms to therapeutics. Theranostics 9:1923–51.
   PubMed Web of Science ®Google Scholar
• Fernandes HP, Cesar CL, Barjas-Castro Mde L. (2011). Electrical properties of the red blood cell membrane and immunohematological investigation. Rev Bras Hematol Hemoter 33:297–301.
   PubMedGoogle Scholar
• Fontes A, Fernandes HP, de Thomaz AA, et al. (2008). Measuring electrical and mechanical properties of red blood cells with double optical tweezers. J Biomed Opt 13:014001.
   PubMed Web of Science ®Google Scholar
• Fu K, Wang Z, Cao R. (2021). Berberine attenuates the inflammatory response by activating the Keap1/Nrf2 signaling pathway in bovine endometrial epithelial cells. Int Immunopharmacol 96:107738.
   PubMed Web of Science ®Google Scholar
• Gong Z, Chen Y, Zhang R, et al. (2014). Pharmacokinetic comparison of berberine in rat plasma after oral administration of berberine hydrochloride in normal and post inflammation irritable bowel syndrome rats. Int J Mol Sci 15:456–67.
   PubMed Web of Science ®Google Scholar
• Gu S, Song X, Xie R, et al. (2020). Berberine inhibits cancer cells growth by suppressing fatty acid synthesis and biogenesis of extracellular vesicles. Life Sci 257:118122.
   PubMed Web of Science ®Google Scholar
• Hamidi M, Zarrin A, Foroozesh M, et al. (2007). Applications of carrier erythrocytes in delivery of biopharmaceuticals. J Control Release 118:145–60.
   PubMed Web of Science ®Google Scholar
• Harisa G. E-d I, Ibrahim MF, Alanazi FK. (2011). Characterization of human erythrocytes as potential carrier for pravastatin: an in vitro study. Int J Med Sci 8:222–30.
   PubMed Web of Science ®Google Scholar
• Hazra S, Hossain M, Suresh Kumar G. (2013). Binding of isoquinoline alkaloids berberine, palmatine and coralyne to hemoglobin: structural and thermodynamic characterization studies. Mol Biosyst 9:143–53.
   PubMedGoogle Scholar
• Hou Q, He W-J, Wu Y-S, et al. (2020). Berberine: a traditional natural product with novel biological activities. Altern Ther Health Med 26:20–7.
   PubMed Web of Science ®Google Scholar
• Hua W, Ding L, Chen Y, et al. (2007). Determination of berberine in human plasma by liquid chromatography-electrospray ionization-mass spectrometry. J Pharm Biomed Anal 44:931–7.
   PubMed Web of Science ®Google Scholar
• JBF L. (1971). Synchronized excitation of fluorescence emission spectra. Cell Rep Phys Sci 231:64–5.
   Google Scholar
• Keene WR, Jandl JH. (1965). The sites of hemoglobin catabolism. Blood 26:705–19.
   PubMed Web of Science ®Google Scholar
• Khan AY, Hossain M, Kumar GS. (2013). Binding of plant alkaloids berberine and palmatine to serum albumins: a thermodynamic investigation. Mol Biol Rep 40:553–66.
   PubMed Web of Science ®Google Scholar
• Khan AY, Kumar GS. (2016). Probing the binding of anticancer drug topotecan with human hemoglobin: structural and thermodynamic studies. J Photochem Photobiol B 163:185–93.
   PubMed Web of Science ®Google Scholar
• Klajnert B, Bryszewska M. (2002). Fluorescence studies on PAMAM dendrimers interactions with bovine serum albumin. Bioelectrochemistry 55:33–5.
   PubMed Web of Science ®Google Scholar
• Klatt S, Roberts A, Lothian A, et al. (2020). Optimizing red blood cell protein extraction for biomarker quantitation with mass spectrometry. Anal Bioanal Chem 412:1879–92.
   PubMed Web of Science ®Google Scholar
• Klei TR, Meinderts SM, van den Berg TK, et al. (2017). From the cradle to the grave: the role of macrophages in erythropoiesis and erythrophagocytosis. Front Immunol 8.
   PubMed Web of Science ®Google Scholar
• Koleva L, Bovt E, Ataullakhanov F, et al. (2020). Erythrocytes as carriers: from drug delivery to biosensors. Pharmaceutics 12:276.
   PubMed Web of Science ®Google Scholar
• Kostjukova LO, Kostjukov VV. (2021). The electronic states and vibronic absorption spectrum of berberine in aqueous solution. Int J Quantum Chem 121:e26537.
   Web of Science ®Google Scholar
• Lau CW, Yao XQ, Chen ZY, et al. (2001). Cardiovascular actions of berberine. Cardiovasc Drug Rev 19:234–44.
   PubMed Web of Science ®Google Scholar
• Lee SJ, Park SY, Jung MY, et al. (2011). Mechanism for phosphatidylserine-dependent erythrophagocytosis in mouse liver. Blood 117:5215–23.
   PubMed Web of Science ®Google Scholar
• Lemler P, Premasiri WR, DelMonaco A, et al. (2014). NIR Raman spectra of whole human blood: effects of laser-induced and in vitro hemoglobin denaturation. Anal Bioanal Chem 406:193–200.
   PubMed Web of Science ®Google Scholar
• Li C, Ai G, Wang Y, et al. (2020). Oxyberberine, a novel gut microbiota-mediated metabolite of berberine, possesses superior anti-colitis effect: Impact on intestinal epithelial barrier, gut microbiota profile and TLR4-MyD88-NF-κB pathway. Pharmacol Res 152:104603.
   PubMed Web of Science ®Google Scholar
• Li CL, Tan LH, Wang YF, et al. (2019). Comparison of anti-inflammatory effects of berberine, and its natural oxidative and reduced derivatives from Rhizoma Coptidis in vitro and in vivo. Phytomedicine 52:272–83.
   PubMed Web of Science ®Google Scholar
• Li QP, Dou YX, Huang ZW, et al. (2021). Therapeutic effect of oxyberberine on obese non-alcoholic fatty liver disease rats. Phytomedicine 85:153550.
   PubMed Web of Science ®Google Scholar
• Li Y, Liu XG, Wang HY, et al. (2016). Pharmacokinetic studies of phellodendrine in rat plasma and tissues after intravenous administration using ultra-high performance liquid chromatography-tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 1029-1030:95–101.
   PubMed Web of Science ®Google Scholar
• Liu CS, Zheng YR, Zhang YF, et al. (2016). Research progress on berberine with a special focus on its oral bioavailability. Fitoterapia 109:274–82.
   PubMed Web of Science ®Google Scholar
• Liu YT, Hao HP, Xie HG, et al. (2010). Extensive intestinal first-pass elimination and predominant hepatic distribution of berberine explain its low plasma levels in rats. Drug Metab Dispos 38:1779–84.
   PubMed Web of Science ®Google Scholar
• Li XY, Roman S, Czernuszewicz , et. Al. (1990). Consistent porphyrin force field. 2. Nickel octaethylporphyrin skeletal and substituent mode assignments from 15N, meso-d4, and methylene-d16 Raman and infrared isotope shifts. J Phys Chem 94: 1.
   Web of Science ®Google Scholar
• Lu JQ, Jin F, Sun TQ, et al. (2007). Multi-spectroscopic study on interaction of bovine serum albumin with lomefloxacin-copper(II) complex. Int J Biol Macromol 40:299–304.
   PubMed Web of Science ®Google Scholar
• Nagai M, Mizusawa N, Kitagawa T, et al. (2018). A role of heme side-chains of human hemoglobin in its function revealed by circular dichroism and resonance Raman spectroscopy. Biophys Rev 10:271–84.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Ortiz LM, Lombardi P, Tillhon M, et al. (2014). Berberine, an epiphany against cancer. Molecules 19:12349–67.
   PubMed Web of Science ®Google Scholar
• Patel P. (2021). A bird's eye view on a therapeutically ‘wonder molecule’: berberine. Phytomed Plus 1:100070.
   Google Scholar
• Patil S, Sandberg A, Heckert E, et al. (2007). Protein adsorption and cellular uptake of cerium oxide nanoparticles as a function of zeta potential. Biomaterials 28:4600–7.
   PubMed Web of Science ®Google Scholar
• Pierigè F, Bigini N, Rossi L, et al. (2017). Reengineering red blood cells for cellular therapeutics and diagnostics. Wires 9:e1454.
   Google Scholar
• Romański M, Zacharzewska A, Teżyk A, et al. (2018). In vivo red blood cells/plasma partition coefficient of treosulfan and its active monoepoxide in rats. Eur J Drug Metab Pharmacokinet 43:565–71.
   PubMed Web of Science ®Google Scholar
• Ross PD, Subramanian S. (1981). Thermodynamics of protein association reactions: forces contributing to stability. Biochemistry 20:3096–102.
   PubMed Web of Science ®Google Scholar
• Scarlett G, Siligardi G, Kneale GG. (2015). Circular dichroism for the analysis of protein-DNA interactions. Methods Mol Biol 1334:299–312.
   PubMedGoogle Scholar
• Schmidt S, Gonzalez D, Derendorf H. (2010). Significance of protein binding in pharmacokinetics and pharmacodynamics. J Pharm Sci 99:1107–22.
   PubMed Web of Science ®Google Scholar
• Shen XC, Liou XY, Ye PL, et al. (2007). Spectroscopic studies on the interaction between human hemoglobin and CdS quantum dots. J Colloid Interface Sci 311:400–6.
   PubMed Web of Science ®Google Scholar
• Ship NJ, Toprak A, Lai RP, et al. (2005). Binding of acellular, native and cross-linked human hemoglobins to haptoglobin: enhanced distribution and clearance in the rat. Am J Physiol Gastrointest Liver Physiol 288:G1301–G1309.
   PubMed Web of Science ®Google Scholar
• Shobini J, Mishra AK, Sandhya K, et al. (2001). Interaction of coumarin derivatives with human serum albumin: investigation by fluorescence spectroscopic technique and modeling studies. Spectrochim Acta A Mol Biomol Spectrosc 57:1133–47.
   Web of Science ®Google Scholar
• Singhal R, Chawla S, Rathore DK, et al. (2017). Development of pro-inflammatory phenotype in monocytes after engulfing Hb-activated platelets in hemolytic disorders. Clin Immunol 175:133–42.
   PubMed Web of Science ®Google Scholar
• Sousa T, Paterson R, Moore V, et al. (2008). The gastrointestinal microbiota as a site for the biotransformation of drugs. Int J Pharm 363:1–25.
   PubMed Web of Science ®Google Scholar
• Spiro TG. (1985). Resonance Raman spectroscopy as a probe of heme protein structure and dynamics. Adv Protein Chem 37:111–59.
   PubMedGoogle Scholar
• Sun Y, Wang W, Tong Y. (2019). Berberine inhibits proliferative ability of breast cancer cells by reducing metadherin. Med Sci Monit 25:9058–66.
   PubMed Web of Science ®Google Scholar
• Szumiło M. (2013). Erythrocytes - the new application in medicine. Pol Merkur Lekarski 34:5–8.
   PubMedGoogle Scholar
• Tan XS, Ma JY, Feng R, et al. (2013). Tissue distribution of berberine and its metabolites after oral administration in rats. PLOS One 8:e77969.
   PubMed Web of Science ®Google Scholar
• Theurl I, Hilgendorf I, Nairz M, et al. (2016). On-demand erythrocyte disposal and iron recycling requires transient macrophages in the liver. Nat Med 22:945–51.
   PubMed Web of Science ®Google Scholar
• Venkatesh B, Ramasamy S, Mylrajan M, et al. (1999). Fourier transform Raman approach to structural correlation in hemoglobin derivatives. S Spectrochim Acta A Mol Biomol Spectrosc 55:1691–7.
   Web of Science ®Google Scholar
• Vos FE, Schollum JB, Coulter CV, et al. (2011). Red blood cell survival in long-term dialysis patients. Am J Kidney Dis 58:591–8.
   PubMed Web of Science ®Google Scholar
• Wang C, Perumalla SR, Lu J, et al. (2016). Sweet berberine. Crystal Growth & Design 16:933–9.
   Web of Science ®Google Scholar
• Wang YQ, Zhang HM, Zhang GC, et al. (2007). Studies of the interaction between paraquat and bovine hemoglobin. Int J Biol Macromol 41:243–50.
   PubMed Web of Science ®Google Scholar
• Wood BR, Caspers P, Puppels GJ, et al. (2007). Resonance Raman spectroscopy of red blood cells using near-infrared laser excitation. Anal Bioanal Chem 387:1691–703.
   PubMed Web of Science ®Google Scholar
• Woody RW. (1995). Circular-dichroism. In: K. Sauer, editor, Biochemical spectroscopy. Methods enzymol 246:34–71.
   Google Scholar
• Wu T, Wu Q, Guan S, et al. (2007). Binding of the environmental pollutant naphthol to bovine serum albumin. Biomacromolecules 8:1899–906.
   PubMed Web of Science ®Google Scholar
• Xu L, Lin G, Yu Q, et al. (2021). Anti-hyperuricemic and nephroprotective effects of dihydroberberine in potassium oxonate- and hypoxanthine-induced hyperuricemic mice. Front Pharmacol 12:645879.
   PubMed Web of Science ®Google Scholar
• Yan QN, Zhang S, Zhang ZQ. (2009). Study on the tissue distribution of berberine from Rhizoma Coptidis and compatibility with Rhizoma Coptidis and Cortex Cinnamomi in rats. Zhong Yao Cai 32:575–8.
   PubMedGoogle Scholar
• Yang Q, Liang J, Han H. (2009). Probing the interaction of magnetic iron oxide nanoparticles with bovine serum albumin by spectroscopic techniques. J Phys Chem B 113:10454–8.
   PubMed Web of Science ®Google Scholar
• Yin WY, Yuan J, Zhang ZM, et al. (2021). 18F-fluorodeoxyglucose positron emission tomography-computed tomography for assessing organ distribution of stressed red blood cells in mice. Sci Rep 11:2505.
   PubMed Web of Science ®Google Scholar
• Yu F, Ao M, Zheng X, et al. (2017). PEG-lipid-PLGA hybrid nanoparticles loaded with berberine-phospholipid complex to facilitate the oral delivery efficiency. Drug Deliv 24:825–33.
   PubMed Web of Science ®Google Scholar
• Zhang K, Mao L, Cai R. (2000). Stopped-flow spectrophotometric determination of hydrogen peroxide with hemoglobin as catalyst. Talanta 51:179–86.
   PubMed Web of Science ®Google Scholar
• Zhang N, Palmer AF. (2011). Development of a dichloroacetic acid-hemoglobin conjugate as a potential targeted anti-cancer therapeutic. Biotechnol Bioeng 108:1413–20.
   PubMed Web of Science ®Google Scholar
• Zou K, Li Z, Zhang Y, et al. (2017). Advances in the study of berberine and its derivatives: a focus on anti-inflammatory and anti-tumor effects in the digestive system. Acta Pharmacol Sin 38:157–67.
   PubMed Web of Science ®Google Scholar
• Zuo F, Nakamura N, Akao T, et al. (2006). Pharmacokinetics of berberine and its main metabolites in conventional and pseudo germ-free rats determined by liquid chromatography/ion trap mass spectrometry. Drug Metab Dispos 34:2064–72.
   PubMed Web of Science ®Google Scholar