Chloroquine interference with hemoglobin endocytic trafficking suppresses adaptive heme and iron homeostasis in macrophages: The paradox of an antimalarial agent

Oxidative Medicine and Cellular Longevity

Volumn , Issue , 2013, Pages

  Schaer, Christian A ^a   Laczko, Endre ^b   Schoedon, Gabriele ^a   Schaer, Dominik J ^a   Vallelian, Florence ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMALARIAL AGENT; ANTIMALARIAL DRUG; AUTOIMMUNE DISEASE; IMMUNOMODULATORY ACTIVITIES; RELATIVE QUANTIFICATION; SCAVENGER RECEPTOR; SINGLE REACTION MONITORING; TRANSFERRIN RECEPTORS;

BLOOD; DETOXIFICATION; ENZYME ACTIVITY; HEMOGLOBIN; MACROPHAGES; PEPTIDES; PHYSIOLOGY; PORPHYRINS;

IRON;

CD163 ANTIGEN; CHLOROQUINE; FERROPORTIN; HEME; HEME OXYGENASE 1; HEMOGLOBIN; HEMOGLOBIN ALPHA CHAIN; HEMOGLOBIN BETA CHAIN; IRON; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MESSENGER RNA; TRANSFERRIN; ANTIMALARIAL AGENT; CELL SURFACE RECEPTOR; DIFFERENTIATION ANTIGEN; HAPTOGLOBIN; LEUKOCYTE ANTIGEN; PEPTIDE;

ARTICLE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DETOXIFICATION; ENDOCYTOSIS; HEMOLYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; MACROPHAGE; MASS SPECTROMETRY; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; AMINO ACID SEQUENCE; CHEMISTRY; DRUG EFFECT; HEK293 CELL LINE; HOMEOSTASIS; INTRACELLULAR SPACE; METABOLISM; MOLECULAR GENETICS; PROTEIN TRANSPORT;

AMINO ACID SEQUENCE; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; ANTIMALARIALS; CHLOROQUINE; ENDOCYTOSIS; HAPTOGLOBINS; HEK293 CELLS; HEME; HEME OXYGENASE-1; HEMOGLOBINS; HOMEOSTASIS; HUMANS; INTRACELLULAR SPACE; IRON; MACROPHAGES; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN TRANSPORT; RECEPTORS, CELL SURFACE;

EID: 84880161320     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2013/870472     Document Type: Article

References (35)

1. Schaer D. J., Buehler P. W., Alayash A. I., Belcher J. D., Vercellotti G. M., Hemolysis and free hemoglobin revisited: exploring hemoglobin and hemin scavengers as a novel class of therapeutic proteins. Blood 2013 121 8 1276 1284
2. Buehler P. W., D'Agnillo F., Schaer D. J., Hemoglobin-based oxygen carriers: from mechanisms of toxicity and clearance to rational drug design. Trends in Molecular Medicine 2010 16 10 447 457 2-s2.0-77957331298 10.1016/j.molmed.2010.07.006
3. Schaer D. J., Alayash A. I., Clearance and control mechanisms of hemoglobin from cradle to grave. Antioxidants and Redox Signaling 2010 12 2 181 184 2-s2.0-77949507206 10.1089/ars.2009.2923
4. Kristiansen M., Graversen J. H., Jacobsen C., Sonne O., Hoffman H. J., Law S. K. A., Moestrup S. K., Identification of the haemoglobin scavenger receptor. Nature 2001 409 6817 198 201 2-s2.0-0035843134 10.1038/35051594
5. Schaer D. J., Schaer C. A., Buehler P. W., Boykins R. A., Schoedon G., Alayash A. I., Schaffner A., CD163 is the macrophage scavenger receptor for native and chemically modified hemoglobins in the absence of haptoglobin. Blood 2006 107 1 373 380 2-s2.0-30144435054 10.1182/blood-2005-03-1014
6. Schaer C. A., Vallelian F., Imhof A., Schoedon G., Schaer D. J., CD163-expressing monocytes constitute an endotoxin-sensitive Hb clearance compartment within the vascular system. Journal of Leukocyte Biology 2007 82 1 106 110 2-s2.0-34347400629 10.1189/jlb.0706453
7. Schaer C. A., Schoedon G., Imhof A., Kurrer M. O., Schaer D. J., Constitutive endocytosis of CD163 mediates hemoglobin-heme uptake and determines the noninflammatory and protective transcriptional response of macrophages to hemoglobin. Circulation Research 2006 99 9 943 950 2-s2.0-33750451990 10.1161/01.RES.0000247067.34173.1b
8. Vallelian F., Schaer C. A., Kaempfer T., Gehrig P., Duerst E., Schoedon G., Schaer D. J., Glucocorticoid treatment skews human monocyte differentiation into a hemoglobin-clearance phenotype with enhanced heme-iron recycling and antioxidant capacity. Blood 2010 116 24 5347 5356 2-s2.0-78149250096 10.1182/blood-2010-04-277319
9. Maniecki M. B., Hasle H., Friis-Hansen L., Lausen B., Nielsen O. J., Bendix K., Moestrup S. K., Møller H. J., Impaired CD163-mediated hemoglobin-scavenging and severe toxic symptoms in patients treated with gemtuzumab ozogamicin. Blood 2008 112 4 1510 1514 2-s2.0-51649119906 10.1182/blood-2007-09-114165
10. Yachie A., Niida Y., Wada T., Igarashi N., Kaneda H., Toma T., Ohta K., Kasahara Y., Koizumi S., Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. Journal of Clinical Investigation 1999 103 1 129 135 2-s2.0-0032893958
11. Wattiaux R., Laurent N., Wattiaux-De Coninck S., Jadot M., Endosomes, lysosomes: their implication in gene transfer. Advanced Drug Delivery Reviews 2000 41 2 201 208 2-s2.0-0343067072 10.1016/S0169-409X(99)00066-6
12. Chapman R. E., Munro S., Retrieval of TGN proteins from the cell surface requires endosomal acidification. EMBO Journal 1994 13 10 2305 2312 2-s2.0-0028283375
13. Mallman I., Fuchs R., Helenius A., Acidification of the endocytic and exocytic pathways. Annual Review of Biochemistry 1986 55 663 700 2-s2.0-0022555867
14. Hempelmann E., Hemozoin biocrystallization in Plasmodium falciparum and the antimalarial activity of crystallization inhibitors. Parasitology Research 2007 100 4 671 676 2-s2.0-33846649572 10.1007/s00436-006-0313-x
15. Pamplona A., Ferreira A., Balla J., Jeney V., Balla G., Epiphanio S., Rodrigues C. D., Gregoire I. P., Cunha-Rodrigues M., Portugal S., Soares M. P., Mota M. M., Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nature Medicine 2007 13 6 703 710 2-s2.0-34250008488 10.1038/nm1586
16. Murphy S. C., Breman J. G., GAPS in the childhood malaria burden in Africa: cerebral malaria, neurological sequelae, anemia, respiratory distress, hypoglycemia, and complications of pregnancy. American Journal of Tropical Medicine and Hygiene 2001 64 1-2 57 67 2-s2.0-0034977311
17. Zucker J. R., Lackritz E. M., Ruebush T. K., Hightower A. W., Adungosi J. E., Were J. B. O., Metchock B., Patrick E., Campbell C. C., Childhood mortality during and after hospitalization in western Kenya: effect of malaria treatment regimens. American Journal of Tropical Medicine and Hygiene 1996 55 6 655 660 2-s2.0-0030511993
18. Lackritz E. M., Campbell C. C., Ruebush T. K., Hightower A. W., Wakube W., Steketee R. W., Were J. B. O., Effect of blood transfusion on survival among children in a Kenyan hospital. The Lancet 1992 340 8818 524 528 2-s2.0-0026803111 10.1016/0140-6736(92)91719-O
19. Shah N. K., Dhillon G. P. S., Dash A. P., Arora U., Meshnick S. R., Valecha N., Antimalarial drug resistance of Plasmodium falciparum in India: changes over time and space. The Lancet Infectious Diseases 2011 11 1 57 64 2-s2.0-78650233941 10.1016/S1473-3099(10)70214-0
20. Eastman R. T., Fidock D. A., Artemisinin-based combination therapies: a vital tool in efforts to eliminate malaria. Nature Reviews Microbiology 2009 7 12 864 874 2-s2.0-70449732094 10.1038/nrmicro2239
21. Ruiz-Irastorza G., Ramos-Casals M., Brito-Zeron P., Khamashta M. A., Clinical efficacy and side effects of antimalarials in systemic lupus erythematosus: a systematic review. Annals of the Rheumatic Diseases 2010 69 1 20 28 2-s2.0-73449120372 10.1136/ard.2008.101766
22. Lee S. J., Silverman E., Bargman J. M., The role of antimalarial agents in the treatment of SLE and lupus nephritis. Nature Reviews Nephrology 2011 7 12 718 729
23. Abraham N. G., Kappas A., Pharmacological and clinical aspects of heme oxygenase. Pharmacological Reviews 2008 60 1 79 127 2-s2.0-46949108047
24. Balla J., Vercellotti G. M., Jeney V., Yachie A., Varga Z., Jacob H. S., Eaton J. W., Balla G., Heme, heme oxygenase, and ferritin: how the vascular endothelium survives (and dies) in an iron-rich environment. Antioxidants and Redox Signaling 2007 9 12 2119 2137 2-s2.0-35848957274 10.1089/ars.2007.1787
25. Krieger J. R., Taylor P., Gajadhar A. S., Guha A., Moran M. F., McGlade C. J., Identification and selected reaction monitoring (SRM) quantification of endocytosis factors associated with Numb. Molecular and Cellular Proteomics 2013 12 2 499 514 10.1074/mcp.M112.020768
26. Agard N. J., Mahrus S., Trinidad J. C., Lynn A., Burlingame A. L., Wells J. A., Global kinetic analysis of proteolysis via quantitative targeted proteomics. Proceedings of the National Academy of Sciences of the United States of America 2012 109 6 1913 1918 10.1073/pnas.1117158109
27. Khalil I. F., Alifrangis M., Recke C., Hoegberg L. C., Ronn A., Bygbjerg I. C., Koch C., Development of ELISA-based methods to measure the anti-malarial drug chloroquine in plasma and in pharmaceutical formulations. Malaria Journal 2011 10, article 249 10.1186/1475-2875-10-249
28. Lim H. S., Im J. S., Cho J. Y., Bae K. S., Klein T. A., Yeom J. S., Kim T. S., Choi J. S., Jang I. J., Park J. W., Pharmacokinetics of hydroxychloroquine and its clinical implications in chemoprophylaxis against malaria caused by plasmodium vivax. Antimicrobial Agents and Chemotherapy 2009 53 4 1468 1475 2-s2.0-65649150048 10.1128/AAC.00339-08
29. Buehler P. W., Vallelian F., Mikolajczyk M. G., Schoedon G., Schweizer T., Alayash A. I., Schaer D. J., Structural stabilization in tetrameric or polymeric hemoglobin determines its interaction with endogenous antioxidant scavenger pathways. Antioxidants and Redox Signaling 2008 10 8 1449 1462 2-s2.0-51749109815 10.1089/ars.2008.2028
30. Orimadegun A. E., Amodu O. K., Olumese P. E., Omotade O. O., Early home treatment of childhood fevers with ineffective antimalarials is deleterious in the outcome of severe malaria. Malaria Journal 2008 7, article 143 2-s2.0-49249125052 10.1186/1475-2875-7-143
31. Ganz T., Nemeth E., Iron metabolism: interactions with normal and disordered erythropoiesis. Cold Spring Harbor Perspectives in Medicine 2012 2 5 011668
32. Schaer D. J., Boretti F. S., Schoedon G., Schaffner A., Induction of the CD163-dependent haemoglobin uptake by macrophages as a novel anti-inflammatory action of glucocorticoids. British Journal of Haematology 2002 119 1 239 243 2-s2.0-0036400441 10.1046/j.1365-2141.2002.03790.x
33. Picotti P., Aebersold R., Selected reaction monitoring-based proteomics: workflows, potential, pitfalls and future directions. Nature Methods 2012 9 6 555 566
34. Maiolica A., Junger M. A., Ezkurdia I., Aebersold R., Targeted proteome investigation via selected reaction monitoring mass spectrometry. Journal of Proteomics 2012 75 12 3495 3513
35. Picotti P., Rinner O., Stallmach R., Dautel F., Farrah T., Domon B., Wenschuh H., Aebersold R., High-throughput generation of selected reaction-monitoring assays for proteins and proteomes. Nature Methods 2010 7 1 43 46 2-s2.0-74049131716 10.1038/nmeth.1408