Sickle Cell Disease at the Dawn of the Molecular Era

REFERENCES

• Herrick JB. Peculiar elongated and sickle-shaped red blood corpuscules in a case of severe anemia. Arch Int Med. 1910;6:517–521.
   Google Scholar
• Herrick JB. Abstract of discussion. J Am Med Assoc. 1924;83:16.
   Google Scholar
• Sydenstricker VP. Further observations on sickle cell anemia. J Am Med Assoc. 1924;83:12–15.
   Google Scholar
• Hanh EV, Gillespie EB. Sickle cell anemia. Arch Int Med. 1927;39:233.
   Google Scholar
• Scriver JR, Waugh TR. Studies on a case of sickle cell anemia. Can Med Assoc J. 1930;23:375–380.
   Google Scholar
• Pauling L. Molecular disease and evolution. Bull N Y Acad Med. 1964;40:334–342.
   PubMedGoogle Scholar
• Pauling L, Itano HA, Singer SJ, Wells IC. Sickle cell anemia, a molecular disease. Science. 1949;110:543–548.
   PubMed Web of Science ®Google Scholar
• Neel JV. The inheritance of sickle cell anemia. Science. 1949;110:64–66.
   PubMed Web of Science ®Google Scholar
• Watson J, Stahman AW, Bilello FP. The significance of the paucity of sickle cells in newborn Negro infants. Am J Med Sci. 1948;215:419–423.
   PubMed Web of Science ®Google Scholar
• Ingram VM. Abnormal human haemoglobins. I. The comparison of normal human and sickle-cell haemoglobins by fingerprinting. Biochim Biophys Acta. 1958;28:539–545.
   PubMed Web of Science ®Google Scholar
• Ferrone FA. Polymerization and sickle cell disease: a molecular view. Microcirculation. 2004;11:115–128.
   PubMed Web of Science ®Google Scholar
• Stamatoyannopoulos G. Control of globin gene expression during development and erythroid differentiation. Exp Hematol. 2005;33:259–271.
   PubMed Web of Science ®Google Scholar
• Bank A. Regulation of human fetal hemoglobin: new players, new complexities. Blood. 2006;107:435–443.
   PubMed Web of Science ®Google Scholar
• Platt OS, Brambilla DJ, Rosse WF, et al. Mortality in sickle cell disease. Life expectancy and risk factors for early death. N Engl J Med. 1994;330:1639–1644.
   PubMed Web of Science ®Google Scholar
• Serjeant GR, Sommereux AM, Stevenson M, Mason K, Serjeant BE. Comparison of sickle cell-beta0 thalassaemia with homozygous sickle cell disease. Br J Haematol. 1979;41:83–93.
   PubMed Web of Science ®Google Scholar
• Serjeant GR, Ashcroft MT, Serjeant BE, Milner PF. The clinical features of sickle-cell-thalassaemia in Jamaica. Br J Haematol. 1973;24:19–30.
   PubMed Web of Science ®Google Scholar
• Reiter CD, Wang X, Tanus-Santos JE, et al. Cell-free hemoglobin limits nitric oxide bioavailability in sickle-cell disease. Nat Med. 2002;8:1383–1389.
   PubMed Web of Science ®Google Scholar
• Gladwin MT, Kato GJ. Cardiopulmonary complications of sickle cell disease: role of nitric oxide and hemolytic anemia. Hematology Am Soc Hematol Educ Program. 2005; 51–57.
   PubMedGoogle Scholar
• Hebbel RP. Auto-oxidation and a membrane-associated ‘Fenton reagent’: a possible explanation for development of membrane lesions in sickle erythrocytes. Clin Haematol. 1985;14:129–140.
   PubMedGoogle Scholar
• Schnog JB, Teerlink T, van der Dijs FP, Duits AJ, Muskiet FA. Plasma levels of asymmetric dimethylarginine (ADMA), an endogenous nitric oxide synthase inhibitor, are elevated in sickle cell disease. Ann Hematol. 2005;84:282–286.
   PubMed Web of Science ®Google Scholar
• Landburg PP, Teerlink T, Muskiet FA, Duits AJ, Schnog JJ, CURAMA Study Group. Plasma concentrations of asymmetric dimethylarginine, an endogenous nitric oxide synthase inhibitor, are elevated in sickle cell patients but do not increase further during painful crisis. Am J Hematol. 2008;83:577–579.
   Google Scholar
• Gladwin MT, Sachdev V, Jison ML, et al. Pulmonary hypertension as a risk factor for death in patients with sickle cell disease. N Engl J Med. 2004;350:886–895.
   PubMed Web of Science ®Google Scholar
• Ataga KI, Sood N, De GG, et al. Pulmonary hypertension in sickle cell disease. Am J Med. 2004;117:665–669.
   PubMed Web of Science ®Google Scholar
• De Castro LM, Jonassaint JC, Graham FL, Ashley-Koch A, Telen MJ. Pulmonary hypertension associated with sickle cell disease: clinical and laboratory endpoints and disease outcomes. Am J Hematol. 2008;83:19–25.
   PubMed Web of Science ®Google Scholar
• Ataga KI, Moore CG, Jones S, et al. Pulmonary hypertension in patients with sickle cell disease: a longitudinal study. Br J Haematol. 2006;134:109–115.
   PubMed Web of Science ®Google Scholar
• Sachdev V, Machado RF, Shizukuda Y, et al. Diastolic dysfunction is an independent risk factor for death in patients with sickle cell disease. J Am Coll Cardiol. 2007;49:472–479.
   PubMed Web of Science ®Google Scholar
• Machado RF, Anthi A, Steinberg MH, et al. N-terminal pro-brain natriuretic peptide levels and risk of death in sickle cell disease. J Am Med Assoc. 2006;296:310–318.
   PubMed Web of Science ®Google Scholar
• Kato GJ, Gladwin MT. Evolution of novel small-molecule therapeutics targeting sickle cell vasculopathy. J Am Med Assoc. 2008;300:2638–2646.
   PubMed Web of Science ®Google Scholar
• Champion HC, Bivalacqua TJ, Takimoto E, Kass DA, Burnett AL. Phosphodiesterase-5A dysregulation in penile erectile tissue is a mechanism of priapism. Proc Natl Acad Sci U S A. 2005;102:1661–1666.
   PubMed Web of Science ®Google Scholar
• Bialecki ES, Bridges KR. Sildenafil relieves priapism in patients with sickle cell disease. Am J Med. 2002;113:252.
   PubMed Web of Science ®Google Scholar
• Burnett AL, Bivalacqua TJ, Champion HC, Musicki B. Long-term oral phosphodiesterase 5 inhibitor therapy alleviates recurrent priapism. Urology. 2006;67:1043–1048.
   PubMed Web of Science ®Google Scholar
• Ohene-Frempong K, Weiner SJ, Sleeper LA, et al. Cerebrovascular accidents in sickle cell disease: rates and risk factors. Blood. 1998;91:288–294.
   PubMed Web of Science ®Google Scholar
• Lezcano NE, Odo N, Kutlar A, Brambilla D, Adams RJ. Regular transfusion lowers plasma free hemoglobin in children with sickle-cell disease at risk for stroke. Stroke. 2006;37:1424–1426.
   PubMed Web of Science ®Google Scholar
• Adams RJ, McKie VC, Hsu L, et al. Prevention of a first stroke by transfusions in children with sickle cell anemia and abnormal results on transcranial Doppler ultrasonography. N Engl J Med. 1998;339:5–11.
   PubMed Web of Science ®Google Scholar
• Kinney TR, Sleeper LA, Wang WC, et al. Silent cerebral infarcts in sickle cell anemia: a risk factor analysis. The cooperative study of sickle cell disease. Pediatrics. 1999;103:640–645.
   PubMed Web of Science ®Google Scholar
• Morris CR, Kato GJ, Poljakovic M, et al. Dysregulated arginine metabolism, hemolysis-associated pulmonary hypertension and mortality in sickle cell disease. J Am Med Assoc. 2005;294:81–90.
   PubMed Web of Science ®Google Scholar
• Kato GJ, McGowan VR, Machado RF, et al. Lactate dehydrogenase as a biomarker of hemolysis-associated nitric oxide resistance, priapism, leg ulceration, pulmonary hypertension and death in patients with sickle cell disease. Blood. 2006;107:2279–2285.
   PubMed Web of Science ®Google Scholar
• Nolan VG, Adewoye A, Baldwin C, et al. Sickel cell leg ulcers: associations with haemolysis and SNPs in Klotho, TEK and genes of the TGF-beta/BMP pathway. Br J Haematol. 2006;133:570–578.
   PubMed Web of Science ®Google Scholar
• de Jong K, Larkin SK, Styles LA, Bookchin RM, Kuypers FA. Characterization of the phosphatidylserine-exposing subpopulation of sickle cells. Blood. 2001;98:860–867.
   PubMed Web of Science ®Google Scholar
• Yasin Z, Witting S, Palascak MB, Joiner CH, Rucknagel DL, Franco RS. Phosphatidylserine externalization in sickle red blood cells: associations with cell age, density, and hemoglobin F. Blood. 2003;102:365–370.
   PubMedGoogle Scholar
• Chiu D, Lubin B, Roelofsen B, van Deenen LL. Sickled erythrocytes accelerate clotting in vitro: an effect of abnormal membrane lipid asymmetry. Blood. 1981;58:398–401.
   PubMed Web of Science ®Google Scholar
• Atichartakarn V, Angchaisuksiri P, Aryurachai K, et al. Relationship between hypercoagulable state and erythrocyte phosphatidylserine exposure in splenectomized haemoglobin E/beta-thalassaemic patients. Br J Haematol. 2002;118:893–898.
   PubMed Web of Science ®Google Scholar
• Atichartakarn V, Angchaisuksiri P, Aryurachai K, Chuncharunee S, Thakkinstian A. In vivo platelet activation and hyperaggregation in hemoglobin E/beta-thalassemia: a consequence of splenectomy. Int J Hematol. 2003;77:299–303.
   PubMed Web of Science ®Google Scholar
• Chou R, DeLoughery TG. Recurrent thromboembolic disease following splenectomy for pyruvate kinase deficiency. Am J Hematol. 2001;67:197–199.
   PubMed Web of Science ®Google Scholar
• Hayag-Barin JE, Smith RE, Tucker FC Jr.. Hereditary spherocytosis, thrombocytosis, and chronic pulmonary emboli: a case report and review of the literature. Am J Hematol. 1998;57:82–84.
   PubMed Web of Science ®Google Scholar
• Aessopos A, Farmakis D, Deftereos S, Tsironi M, Polonifi A, Moyssakis I. Cardiovascular effects of splenomegaly and splenectomy in beta-thalassemia. Ann Hematol. 2005;84:353–357.
   PubMed Web of Science ®Google Scholar
• Stewart GW, Amess JA, Eber SW, et al. Thrombo-embolic disease after splenectomy for hereditary stomatocytosis. Br J Haematol. 1996;93:303–310.
   PubMed Web of Science ®Google Scholar
• Setty BN, Kulkarni S, Stuart MJ. Role of erythrocyte phosphatidylserine in sickle red cell-endothelial adhesion. Blood. 2002;99:1564–1571.
   PubMed Web of Science ®Google Scholar
• Setty BN, Rao AK, Stuart MJ. Thrombophilia in sickle cell disease: the red cell connection. Blood. 2001;98:3228–3233.
   Google Scholar
• Stuart MJ, Setty BN. Hemostatic alterations in sickle cell disease: relationships to disease pathophysiology. Pediatr Pathol Mol Med. 2001;20:27–46.
   PubMed Web of Science ®Google Scholar
• Kuypers FJ, de Jong K. The role of phosphatidylserine in recognition and removal of erythrocytes. Cell Mol Biol. 2004;50:147–158.
   PubMed Web of Science ®Google Scholar
• Hawker H, Neilson H, Hayes RJ, Serjeant GR. Haematological factors associated with avascular necrosis of the femoral head in homozygous sickle cell disease. Br J Haematol. 1982;50:29–34.
   PubMed Web of Science ®Google Scholar
• Castro O, Brambilla DJ, Thorington B, et al. The acute chest syndrome in sickle cell disease: incidence and risk factors. The cooperative study of sickle cell disease. Blood. 1994;84:643–649.
   PubMed Web of Science ®Google Scholar
• Bailey K, Morris JS, Thomas P, Serjeant GR. Fetal haemoglobin and early manifestations of homozygous sickle cell disease. Arch Dis Child. 1992;67:517–520.
   PubMed Web of Science ®Google Scholar
• Steinberg MH. Predicting clinical severity in sickle cell anaemia. Br J Haematol. 2005;129:465–481.
   PubMed Web of Science ®Google Scholar
• Nolan VG, Wyszynski DF, Farrer LA, Steinberg MH. Hemolysis-associated priapism in sickle cell disease. Blood. 2005;106:3264–3267.
   PubMed Web of Science ®Google Scholar
• Franco RS, Yasin Z, Palascak MB, Ciraolo P, Joiner CH, Rucknagel DL. The effect of fetal hemoglobin on the survival characteristics of sickle cells. Blood. 2006;108:1073–1076.
   PubMed Web of Science ®Google Scholar
• Sebastiani P, Ramoni MF, Nolan V, Baldwin CT, Steinberg MH. Genetic dissection and prognostic modeling of overt stroke in sickle cell anemia. Nat Genet. 2005;37:435–440.
   PubMed Web of Science ®Google Scholar
• De Ceulaer K, Higgs DR, Weatherall DJ, Hayes RJ, Serjeant BE, Serjeant GR. Alpha thalassemia reduces the hemolytic rate in homozygous sickle-cell disease. N Engl J Med. 1983;309:189–190.
   PubMed Web of Science ®Google Scholar
• Embury SH, Dozy AM, Miller J, et al. Concurrent sickle-cell anemia and alpha-thalassemia: effect on severity of anemia. N Engl J Med. 1982;306:270–274.
   PubMed Web of Science ®Google Scholar
• Steinberg MH, Rosenstock W, Coleman MB, et al. Effects of thalassemia and microcytosis on the hematologic and vasoocclusive severity of sickle cell anemia. Blood. 1984;63:1353–1360.
   PubMed Web of Science ®Google Scholar
• Koshy M, Entsuah R, Koranda A, et al. Leg ulcers in patients with sickle cell disease. Blood. 1989;74:1403–1408.
   PubMed Web of Science ®Google Scholar
• Higgs DR, Aldridge BE, Lamb J, et al. The interaction of alpha-thalassemia and homozygous sickle-cell disease. N Engl J Med. 1982;306:1441–1446.
   PubMed Web of Science ®Google Scholar
• Adams RJ, Kutlar A, McKie V, et al. Alpha thalassemia and stroke risk in sickle cell anemia. Am J Hematol. 1994;45:279–282.
   PubMed Web of Science ®Google Scholar
• Hsu LL, Miller ST, Wright E, et al. Alpha thalassemia is associated with decreased risk of abnormal transcranial Doppler ultrasonography in children with sickle cell anemia. J Pediatr Hematol Oncol. 2003;25:622–628.
   PubMed Web of Science ®Google Scholar
• Neonato MG, Guilloud-Bataille M, Beauvais P, et al. Acute clinical events in 299 homozygous sickle cell patients living in France. French study group on sickle cell disease. Eur J Haematol. 2000;65:155–164.
   PubMed Web of Science ®Google Scholar
• Gill FM, Sleeper LA, Weiner SJ, et al. Clinical events in the first decade in a cohort of infants with sickle cell disease. Cooperative study of sickle cell disease. Blood. 1995;86:776–783.
   PubMed Web of Science ®Google Scholar
• Billett HH, Nagel RL, Fabry ME. Paradoxical increase of painful crises in sickle cell patients with alpha-thalassemia. Blood. 1995;86:4382.
   PubMed Web of Science ®Google Scholar
• Billett HH, Kim K, Fabry ME, Nagel RL. The percentage of dense red cells does not predict incidence of sickle cell painful crisis. Blood. 1986;68:301–303.
   PubMed Web of Science ®Google Scholar
• Bailey S, Higgs DR, Morris J, Serjeant GR. Is the painful crisis of sickle-cell disease due to sickling?. Lancet 1991;337:735.
   Google Scholar
• Milner PF, Kraus AP, Sebes JI, et al. Sickle cell disease as a cause of osteonecrosis of the femoral head. N Engl J Med. 1991;325:1476–1481.
   PubMed Web of Science ®Google Scholar
• Ballas SK, Talacki CA, Rao VM, Steiner RM. The prevalence of avascular necrosis in sickle cell anemia: correlation with alpha-thalassemia. Hemoglobin. 1989;13:649–655.
   PubMed Web of Science ®Google Scholar
• Frenette PS, Atweh GF. Sickle cell disease: old discoveries, new concepts, and future promise. J Clin Invest. 2007;117:850–858.
   PubMed Web of Science ®Google Scholar
• Kato GJ, Martyr S, Blackwelder WC, et al. Levels of soluble endothelium-derived adhesion molecules in patients with sickle cell disease are associated with pulmonary hypertension, organ dysfunction, and mortality. Br J Haematol. 2005;130:943–953.
   PubMed Web of Science ®Google Scholar
• Klings ES, Anton Bland D, Rosenman D, et al. Pulmonary arterial hypertension and left-sided heart disease in sickle cell disease: clinical characteristics and association with soluble adhesion molecule expression. Am J Hematol. 2008;83:547–553.
   PubMed Web of Science ®Google Scholar
• Belcher JD, Mahaseth H, Welch TE, Otterbein LE, Hebbel RP, Vercellotti GM. Heme oxygenase-1 is a modulator of inflammation and vaso-occlusion in transgenic sickle mice. J Clin Invest. 2006;116:808–816.
   PubMed Web of Science ®Google Scholar
• Rother RP, Bell L, Hillmen P, Gladwin MT. The clinical sequelae of intravascular hemolysis and extracellular plasma hemoglobin: a novel mechanism of human disease. J Am Med Assoc. 2005;293:1653–1662.
   PubMed Web of Science ®Google Scholar
• Nagel RL, Gibson QH. The binding of hemoglobin to haptoglobin and its relation to subunit dissociation of hemoglobin. J Biol Chem. 1971;246:69–73.
   PubMed Web of Science ®Google Scholar
• Kristiansen M, Graversen JH, Jacobsen C, et al. Identification of the haemoglobin scavenger receptor. Nature. 2001;409:198–201.
   PubMed Web of Science ®Google Scholar
• Ryter SW, Otterbein LE, Morse D, Choi AM. Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance. Mol Cell Biochem. 2002; 234–235249–263.
   Google Scholar
• Baranano DE, Rao M, Ferris CD, Snyder SH. Biliverdin reductase: a major physiologic cytoprotectant. Proc Natl Acad Sci U S A. 2002;99:16093–16098.
   PubMed Web of Science ®Google Scholar
• Otterbein LE, Bach FH, Alam J, et al. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med. 2000;6:422–428.
   PubMed Web of Science ®Google Scholar
• Melamed-Frank M, Lache O, Enav BI, et al. Structure-function analysis of the antioxidant properties of haptoglobin. Blood. 2001;98:3693–3698.
   PubMed Web of Science ®Google Scholar
• Okpala I. Leukocyte adhesion and the pathophysiology of sickle cell disease. Curr Opin Hematol. 2006;13:40–44.
   PubMed Web of Science ®Google Scholar
• Frenette PS. Sickle cell vasoocclusion: heterotypic, multicellular aggregations driven by leukocyte adhesion. Microcirculation. 2004;11:167–177.
   PubMed Web of Science ®Google Scholar
• Schmid-Schonbein GW. The damaging potential of leukocyte activation in the microcirculation. Angiology. 1993;44:45–56.
   Google Scholar
• House SD, Lipowsky HH. Leukocyte-endothelium adhesion: microhemodynamics in mesentery of the cat. Microvasc Res. 1987;34:363–379.
   PubMed Web of Science ®Google Scholar
• Turhan A, Weiss LA, Mohandas N, Coller BS, Frenette PS. Primary role for adherent leukocytes in sickle cell vascular occlusion: a new paradigm. Proc Natl Acad Sci U S A. 2002;99:3047–3051.
   PubMed Web of Science ®Google Scholar
• Frenette PS, Mayadas TN, Rayburn H, Hynes RO, Wagner DD. Susceptibility to infection and altered hematopoiesis in mice deficient in both P- and E-selectins. Cell. 1996;84:563–574.
   PubMed Web of Science ®Google Scholar
• Hofstra TC, Kalra VK, Meiselman HJ, Coates TD. Sickle erythrocytes adhere to polymorphonuclear neutrophils and activate the neutrophil respiratory burst. Blood. 1996;87:4440–4447.
   PubMed Web of Science ®Google Scholar
• Chiang EY, Hidalgo A, Chang J, Frenette PS. Imaging receptor microdomains on leukocyte subsets in live mice. Nat Methods. 2007;4:219–222.
   PubMedGoogle Scholar
• Balkaran B, Char G, Morris JS, Thomas PW, Serjeant BE, Serjeant GR. Stroke in a cohort of patients with homozygous sickle cell disease. J Pediatr. 1992;120:360–366.
   PubMed Web of Science ®Google Scholar
• Miller ST, Sleeper LA, Pegelow CH, et al. Prediction of adverse outcomes in children with sickle cell disease. N Engl J Med. 2000;342:83–89.
   PubMed Web of Science ®Google Scholar
• Sasaki J, Waterman MR, Buchanan GR, Cottam GL. Plasma and erythrocyte lipids in sickle cell anaemia. Clin Lab Haematol. 1983;5:35–44.
   PubMedGoogle Scholar