Extracellular fetal hemoglobin induces increases in glomerular permeability: Inhibition with α1 -microglobulin and tempol

American Journal of Physiology - Renal Physiology

Volumn 306, Issue 4, 2014, Pages

  Sverrisson, Kristinn ^a   Axelsson, Josefin ^a   Rippe, Anna ^a   Gram, Magnus ^a   Åkerström, Bo ^a   Hansson, Stefan R ^a   Rippe, Bengt ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Adult haemoglobin; Capillary permeability; Ficoll; Glomerular sieving coefficient; Preeclampsia

Indexed keywords

ALPHA 1 MICROGLOBULIN; EDETIC ACID; FICOLL; HEMOGLOBIN A; HEMOGLOBIN F; INULIN; REACTIVE OXYGEN METABOLITE; TEMPOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; GEL PERMEATION CHROMATOGRAPHY; GLOMERULUS FILTRATION; IN VIVO STUDY; MALE; NONHUMAN; PREECLAMPSIA; PRIORITY JOURNAL; RAT; URINALYSIS;

ADULT HEMOGLOBIN; CAPILLARY PERMEABILITY; FICOLL; GLOMERULAR SIEVING COEFFICIENT; PREECLAMPSIA;

ALPHA-GLOBULINS; ANIMALS; ANTIOXIDANTS; CYCLIC N-OXIDES; FETAL HEMOGLOBIN; GLOMERULAR FILTRATION RATE; KIDNEY GLOMERULUS; MALE; PERMEABILITY; RATS; RATS, WISTAR; SPIN LABELS;

EID: 84894033202     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00502.2013     Document Type: Article

References (52)

1. AdamsonRH, ZengM, AdamsonGN, LenzJF, CurryFE. PAF- and bradykinin-induced hyperpermeability of rat venules is independent of actin-myosin contraction.Am J Physiol Heart Circ Physiol285:H406-H417,2003.
2. AkerstromB, MaghzalGJ, WinterbournCC, KettleAJ. The lipocalin α1-microglobulin has radical scavenging activity.J Biol Chem282:31493-31503,2007.
3. AllhornM, BerggardT, NordbergJ, OlssonML, AkerstromB. Processing of the lipocalin α1-microglobulin by hemoglobin induces heme-binding and heme-degradation properties.Blood99:1894-1901,2002.
4. AllhornM, KlapytaA, AkerstromB. Redox properties of the lipocalin α1-microglobulin: reduction of cytochromec, hemoglobin, and free iron.Free Radic Biol Med38:557-567,2005.
5. AndersonUD, OlssonMG, RutardottirS, CentlowM, KristensenKH, IsbergPE, ThilaganathanB, AkerstromB, HanssonSR. Fetal hemoglobin and α1-microglobulin as first- and early second-trimester predictive biomarkers for preeclampsia.Am J Obstet Gynecol204:520e521-525,2011.
6. AsgeirssonD, VenturoliD, RippeB, RippeC. Increased glomerular permeability to negatively charged Ficoll relative to neutral Ficoll in rats.Am J Physiol Renal Physiol291:F1083-F1089,2006.
7. AxelssonJ, MahmutovicI, RippeA, RippeB. Loss of size selectivity of the glomerular filtration barrier in rats following laparotomy and muscle trauma.Am J Physiol Renal Physiol297:F577-F582,2009.
8. AxelssonJ, RippeA, ObergCM, RippeB. Rapid, dynamic changes in glomerular permeability to macromolecules during systemic angiotensin II (ANG II) infusion in rats.Am J Physiol Renal Physiol303:F790-F799,2012.
9. AxelssonJ, RippeA, RippeB. Acute hyperglycemia induces rapid, reversible increases in glomerular permeability in nondiabetic rats.Am J Physiol Renal Physiol298:F1306-F1312,2010.
10. AxelssonJ, RippeA, RippeB. Transient and sustained increases in glomerular permeability following ANP infusion in rats.Am J Physiol Renal Physiol300:F24-30,2011.
11. AxelssonJ, RippeA, VenturoliD, SwardP, RippeB. Effects of early endotoxemia and dextran-induced anaphylaxis on the size selectivity of the glomerular filtration barrier in rats.Am J Physiol Renal Physiol296:F242-F248,2009.
12. BallaG, JacobHS, BallaJ, RosenbergM, NathK, AppleF, EatonJW, VercellottiGM. Ferritin: a cytoprotective antioxidant strategem of endothelium.J Biol Chem267:18148-18153,1992.
13. BerggardT, ThelinN, FalkenbergC, EnghildJJ, AkerstromB. Prothrombin, albumin and immunoglobulin A form covalent complexes with α1-microglobulin in human plasma.Eur J Biochem245:676-683,1997.
14. BuehlerPW, D'AgnilloF. Toxicological consequences of extracellular hemoglobin: biochemical and physiological perspectives.Antioxid Redox Signal12:275-291,2010.
15. BunnHFL, ForgetBG. Hemoglobin: Molecular, Genetic and Clinical Aspects.Philadelphia, PA:Saunders,1986.
16. CentlowM, CarninciP, NemethK, MezeyE, BrownsteinM, HanssonSR. Placental expression profiling in preeclampsia: local overproduction of hemoglobin may drive pathological changes.Fertil Steril90:1834-1843,2008.
17. EreminaV, SoodM, HaighJ, NagyA, LajoieG, FerraraN, GerberHP, KikkawaY, MinerJH, QuagginSE. Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases.J Clin Invest111:707-716,2003.
18. EverseJ, HsiaN. The toxicities of native and modified hemoglobins.Free Radic Biol Med22:1075-1099,1997.
19. GoswamiD, TannettaDS, MageeLA, FuchisawaA, RedmanCW, SargentIL, von DadelszenP. Excess syncytiotrophoblast microparticle shedding is a feature of early-onset pre-eclampsia, but not normotensive intrauterine growth restriction.Placenta27:56-61,2006.
20. HaraldssonB, NystromJ, DeenWM. Properties of the glomerular barrier and mechanisms of proteinuria.Physiol Rev88:451-487,2008.
21. HaraldssonB, ZackrissonU, RippeB. Calcium dependence of histamine-induced increases in capillary permeability in isolated perfused rat hindquarters.Acta Physiol Scand128:247-258,1986.
22. HenaoDE, AriasLF, MathiesonPW, NiL, WelshGI, BuenoJC, AgudeloB, CadavidAP, SaleemMA. Preeclamptic sera directly induce slit-diaphragm protein redistribution and alter podocyte barrier-forming capacity.Nephron Exp Nephrol110:e73-81,2008.
23. HvidbergV, ManieckiMB, JacobsenC, HojrupP, MollerHJ, MoestrupSK. Identification of the receptor scavenging hemopexin-heme complexes.Blood106:2572-2579,2005.
24. KubesP, GrangerDN. Nitric oxide modulates microvascular permeability.Am J Physiol Heart Circ Physiol262:H611-H615,1992.
25. KumarS, BandyopadhyayU. Free heme toxicity and its detoxification systems in human.Toxicol Lett157:175-188,2005.
26. KwasekA, OsmarkP, AllhornM, LindqvistA, AkerstromB, WasylewskiZ. Production of recombinant human α1-microglobulin and mutant forms involved in chromophore formation.Protein Expr Purif53:145-152,2007.
27. LarssonJ, AllhornM, KerstromB. The lipocalin α1-microglobulin binds heme in different species.Arch Biochem Biophys432:196-204,2004.
28. LiF, HagamanJR, KimHS, MaedaN, JennetteJC, FaberJE, KarumanchiSA, SmithiesO, TakahashiN. eNOS deficiency acts through endothelin to aggravate sFlt-1-induced pre-eclampsia-like phenotype.J Am Soc Nephrol23:652-660,2012.
29. LumH, MalikAB. Mechanisms of increased endothelial permeability.Can J Physiol Pharmacol74:787-800,1996.
30. LundU, RippeA, VenturoliD, TenstadO, GrubbA, RippeB. Glomerular filtration rate dependence of sieving of albumin and some neutral proteins in rat kidneys.Am J Physiol Renal Physiol284:F1226-F1234,2003.
31. MayK, RosenlofL, OlssonMG, CentlowM, MorgelinM, LarssonI, CederlundM, RutardottirS, SiegmundW, SchneiderH, AkerstromB, HanssonSR. Perfusion of human placenta with hemoglobin introduces preeclampsia-like injuries that are prevented by α1-microglobulin.Placenta32:323-332,2011.
32. MaynardSE, KarumanchiSA. Angiogenic factors and preeclampsia.Semin Nephrol31:33-46,2011.
33. MehtaD, MalikAB. Signaling mechanisms regulating endothelial permeability.Physiol Rev86:279-367,2006.
34. NathKA, BallaG, VercellottiGM, BallaJ, JacobHS, LevittMD, RosenbergME. Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat.J Clin Invest90:267-270,1992.
35. OhlsonM, SorenssonJ, LindstromK, BlomAM, FriesE, HaraldssonB. Effects of filtration rate on the glomerular barrier and clearance of four differently shaped molecules.Am J Physiol Renal Physiol281:F103-F113,2001.
36. OlssonMG, AllhornM, BulowL, HanssonSR, LeyD, OlssonML, SchmidtchenA, AkerstromB. Pathological conditions involving extracellular hemoglobin: molecular mechanisms, clinical significance, and novel therapeutic opportunities for α1-microglobulin.Antioxid Redox Signal17:813-846,2012.
37. OlssonMG, AllhornM, LarssonJ, CederlundM, LundqvistK, SchmidtchenA, SorensenOE, MorgelinM, AkerstromB. Up-regulation of A1M/α1-microglobulin in skin by heme and reactive oxygen species gives protection from oxidative damage.PLos One6:e27505,2011.
38. OlssonMG, AllhornM, OlofssonT, AkerstromB. Up-regulation of α1-microglobulin by hemoglobin and reactive oxygen species in hepatoma and blood cell lines.Free Radic Biol Med42:842-851,2007.
39. OlssonMG, CentlowM, RutardottirS, StenforsI, LarssonJ, Hosseini-MaafB, OlssonML, HanssonSR, AkerstromB. Increased levels of cell-free hemoglobin, oxidation markers, and the antioxidative heme scavenger α1-microglobulin in preeclampsia.Free Radic Biol Med48:284-291,2010.
40. OlssonMG, OlofssonT, TapperH, AkerstromB. The lipocalin α1-microglobulin protects erythroid K562 cells against oxidative damage induced by heme and reactive oxygen species.Free Radic Res42:725-736,2008.
41. RedmanCW, SargentIL. Circulating microparticles in normal pregnancy and pre-eclampsia.Placenta29,Suppl A:S73-S77,2008.
42. RippeB, HaraldssonB. Transport of macromolecules across microvascular walls: the two-pore theory.Physiol Rev74:163-219,1994.
43. RippeC, RippeA, LarssonA, AsgeirssonD, RippeB. Nature of glomerular capillary permeability changes following acute renal ischemia-reperfusion injury in rats.Am J Physiol Renal Physiol291:F1362-F1368,2006.
44. RippeC, RippeA, TorffvitO, RippeB. Size and charge selectivity of the glomerular filter in early experimental diabetes in rats.Am J Physiol Renal Physiol293:F1533-F1538,2007.
45. RochetteJ, CraigJE, TheinSL. Fetal hemoglobin levels in adults.Blood Rev8:213-224,1994.
46. RotherRP, BellL, HillmenP, GladwinMT. The clinical sequelae of intravascular hemolysis and extracellular plasma hemoglobin: a novel mechanism of human disease.JAMA293:1653-1662,2005.
47. StillmanIE, KarumanchiSA. The glomerular injury of preeclampsia.J Am Soc Nephrol18:2281-2284,2007.
48. WallukatG, HomuthV, FischerT, LindschauC, HorstkampB, JupnerA, BaurE, NissenE, VetterK, NeichelD, DudenhausenJW, HallerH, LuftFC. Patients with preeclampsia develop agonistic autoantibodies against the angiotensin AT1receptor.J Clin Invest103:945-952,1999.
49. WilcoxCS, PearlmanA. Chemistry and antihypertensive effects of tempol and other nitroxides.Pharmacol Rev60:418-469,2008.
50. WinterbournCC. Oxidative reactions of hemoglobin.Methods Enzymol186:265-272,1990.
51. WoodWG. Increased HbF in adult life.Baillieres Clin Haematol6:177-213,1993.
52. WuNZ, BaldwinAL. Transient venular permeability increase and endothelial gap formation induced by histamine.Am J Physiol Heart Circ Physiol262:H1238-H1247,1992.