Hemoglobin variants: Biochemical properties and clinical correlates

Cold Spring Harbor Perspectives in Medicine

Volumn 3, Issue 3, 2013, Pages

  Thom, Christopher S ^a,b   Dickson, Claire F ^c   Gell, David A ^c   Weiss, Mitchell J ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c UNIVERSITY OF TASMANIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOGLOBIN; HEMOGLOBIN VARIANT; METHEMOGLOBIN; OXYGEN;

BIOSYNTHESIS; CHEMISTRY; CLASSIFICATION; GENETICS; HEMOGLOBINOPATHY; HUMAN; MUTATION; PHYSIOLOGY; REVIEW;

HEMOGLOBINOPATHIES; HEMOGLOBINS; HEMOGLOBINS, ABNORMAL; HUMANS; METHEMOGLOBIN; MUTATION; OXYGEN;

EID: 84882276985     PISSN: None     EISSN: 21571422     Source Type: Journal    
DOI: 10.1101/cshperspect.a011858     Document Type: Article

References (149)

1. Adachi K., Asakura T. 1979. The solubility of sickle and nonsickle hemoglobins in concentrated phosphate buffer. J. Biol Chem 254: 4079-4084.
2. Adachi K., Pang J, Konitzer P, Surrey S. 1996. Polymerization of recombinant hemoglobin F γE6V and hemoglobin F γE6V, γQ87Talone, and in mixtures with hemoglobin S. Blood 87: 1617-1624.
3. Adachi K., Surrey S, Nagai M. 2011. Hemoglobinopathies due to amino acid mutation/deletion: HbS and HbM. In Hemoglobin: Recent developments and topics, pp. 179-210. Research Signpost, Kerala, India.
4. Adams J., Boxer L, Baehner R, Forget B, Tsistrakis G, Steinberg M. 1979. Hemoglobin Indianapolis (β112 [G14] arginine). An unstable β-chain variant producing the phenotype of severe β-thalassemia. J Clin Invest 63: 931-938.
5. Ameri A., Fairbanks V, Yanik G, Mahdi F, Thibodeau S, McCormick D, Boxer L, McDonagh K. 1999. Identification of the molecular genetic defect of patients with methemoglobinM-Kankakee (M-Iwate), α87 (F8) His→ Tyr: Evidence for an electrostatic model of αMhemoglobin assembly. Blood 94: 1825-1826.
6. Argos P., Rossman MG, Grau UM, Zuber H, Frank G, Tratschin JD. 1979. Thermal stability and protein structure. Biochemistry 18: 5698-5703.
7. Arnone A. 1972. X-ray diffraction study of binding of 2,3-diphosphoglycerate to human deoxyhaemoglobin. Nature 237: 146-149.
8. Arous N., Braconnier F, Thillet J, Blouquit Y, Galacteros F, Chevrier M., Bordahandy C, Rosa J. 1981. Hemoglobin Saint Mandé [β102 (G4) Asn→Tyr]: A new low oxygen affinity variant. FEBS Lett 126: 114-116.
9. Asakura T., Adachi K, Shapiro M, Friedman S, Schwartz E. 1975. Mechanical precipitation of hemoglobin köln. Biochim Biophys Acta 412: 197-201.
10. Bachmann F., Marti HR. 1962. Hemoglobin Zürich. II. Physicochemical properties of the abnormal hemoglobin. Blood 20: 272-86.
11. Bare G.H., Bromberg PA, Alben JO, Brimhall B, Jones RT, Mintz S., Rother I. 1976. Altered C-terminal salt bridges in haemoglobin York cause high oxygen affinity. Nature 259: 155-156.
12. Bender J.W., Adachi K, Asakura T. 1981. Precipitation of oxyhemoglobins A and S by isopropanol. Hemoglobin 5: 463-474.
13. Blouquit Y., Bardakdjian J, Lena-Russo D, Arous N, Perrimond H., Orsini A, Rosa J, Galacteros F. 1989. Hb Bruxelles: α 2A β (2)41 or 42(C7 or CD1)Phe deleted. Hemoglobin 13: 465-474.
14. Bonaventura J., Riggs A. 1968. HemoglobinKansas, a human hemoglobin with a neutral amino acid substitution and an abnormal oxygen equilibrium. J. Biol Chem 243: 980-991.
15. Bonaventura J., Bonaventura C, Sullivan B, Ferruzzi G, McCurdy PR, Fox J, Moo-Penn WF. 1976. Hemoglobin providence. Functional consequences of two alterations of the 2,3-diphosphoglycerate binding site at position β82. J. Biol Chem 251: 7563-7571.
16. Bratu V., Lorkin PA, Lehmann H, Predescu C. 1971. Haemoglobin Buccureşti 42(CD1) Phe-Leu, a cause of unstable haemoglobin haemolytic anaemia. Biochim Biophys Acta 251: 1-6.
17. Bunn H.F., Forget BG. 1986. Hemoglobin: Molecular, genetic and clinical aspects. W.B. Saunders, Philadelphia.
18. Bunn H.F., Wohl RC, Bradley TB, Cooley M, Gibson QH. 1974. Functional properties of hemoglobin Kempsey. J Biol Chem 249: 7402-7409.
19. Bunn H.F., Schmidt GJ, Haney DN, Dluhy RG. 1975. Hemoglobin Cranston, an unstable variant having an elongated β chain due to nonhomologous crossover between two normal β chain genes. Proc Natl Acad Sci 72: 3609-3613.
20. Cao A., Kan YW. 2012. The prevention of thalassemia. Cold Spring Harb Perspect Med doi: 10.1101/cshperspect. a011775.
21. Carrell R.W., Kay R. 1972. A simple method for the detection of unstable haemoglobins. Br J Haematol 23: 615-619.
22. Charache S., Fox J, McCurdy P, Kazazian H Jr, Winslow R, Hathaway P., van Beneden R, Jessop M. 1977. Postsynthetic deamidation of hemoglobin Providence (β82 Lys replaced by Asn, Asp) and its effect on oxygen transport. J. Clin Invest 59: 652-658.
23. Clegg J.B., Weatherall DJ. 1974. Hemoglobin Constant Spring, and unusual α-chain variant involved in the etiology of hemoglobin H disease. Ann NY Acad Sci 232: 168-178.
24. Clegg J., Weatherall D, Boon W, Mustafa D. 1969. Two new haemoglobin variants involving proline substitutions. Nature 222: 379-380.
25. Clegg J.B., Weatherall DJ, Milner PF. 1971. Haemoglobin Constant Spring-A chain termination mutant? Nature 234: 337-340.
26. Coleman M.B., Steinberg MH, Adams JG 3rd. 1991. Hemoglobin Terre Haute arginine β106. A posthumous correction to the original structure of hemoglobin Indianapolis. J Biol Chem 266: 5798-5800.
27. Como P.F., Wylie BR, Trent RJ, Bruce D, Volpato F, Wilkinson T., Kronenberg H, Holland RA, Tibben EA. 1991. A new unstable and low oxygen affinity hemoglobin variant: Hb Stanmore (β111[G13]Val→Ala). Hemoglobin 15: 53-65.
28. Crowley M., Mollan T, Abdulmalik O, Butler AD, Goodwin E, Sarkar A, Stolle C, Gow A, Olson J, Weiss M. 2011. A hemoglobin variant associated with neonatal cyanosis and anemia. N Engl J Med 364: 1837-1843.
29. Dacie J.V., Shinton NK, Gaffney PJ Jr, Lehmann H. 1967. Haemoglobin Hammersmith (β-42 [CDI] Phe replaced by ser). Nature 216: 663-665.
30. Dailey H.A., Meissner PN. 2012. Erythroid heme biosynthesis and its disorders. Cold Spring Harb Perspect Med doi: 10.1101/cshperspect.a011676.
31. Derry S., Wood WG, Pippard M, Clegg JB, Weatherall DJ, Wickramasinghe S.N., Darley J, Fucharoen S, Wasi P. 1984. Hematologic and biosynthetic studies in homozygous hemoglobin Constant Spring. J. Clin Invest 73: 1673-1682.
32. Efremov G.D., Wrightstone RN, Huisman TH, Schroeder WA, Hyman C, Ortega J, Williams K. 1971. An unusual hemoglobin anomaly and its relation to α-thalassemia and hemoglobin-H disease. J. Clin Invest 50: 1628-1636.
33. Eisinger J., Flores J, Tyson JA, Shohet SB. 1985. Fluorescent cytoplasm and Heinz bodies of hemoglobin Köln erythrocytes: Evidence for intracellular heme catabolism. Blood 65: 886-893.
34. Emsley P., Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Cryst 66: 486-501.
35. Favero M.E., Costa FF. 2011. α-Hemoglobin-stabilizing protein: An erythroid molecular chaperone. Biochem Res Int 2011: 373859.
36. Forget B.G., Marotta CA, Weissman SM, Cohen-Solal M. 1975. Nucleotide sequences of the 30-terminal untranslated region of messenger RNA for human β globin chain. Proc Natl Acad Sci 72: 3614-3618.
37. Frick P.G., Hitzig WH, Betke K. 1962. Hemoglobin Zurich. I. A new hemoglobin anomaly associated with acute hemolytic episodes with inclusion bodies after sulfonamide therapy. Blood 20: 261-271.
38. Frischer H., Bowman J. 1975. Hemoglobin E, an oxidatively unstable mutation. J Lab Clin Med 85: 531-539.
39. Ganz T., Nemeth E. 2012. Iron metabolism: Interactions with normal and disordered erythropoiesis. Cold Spring Harb Perspect Med doi: 10.1101/cshperspect.a011668.
40. Garrod A. 1928. The lessons of rare maladies: Annual oration before the medical society of London. Lancet 1: 914-915.
41. Geva A., Clark JJ, Zhang Y, Popowicz A, Manning JM, Neufeld EJ. 2004. Hemoglobin Jamaica Plain-A sickling hemoglobin with reduced oxygen affinity. N Engl J Med 351: 1532-1538.
42. Giardine B., Borg J, Higgs D, Peterson K, Philipsen S, Maglott D., Singleton B, Anstee D, Basak A, Clark B, et al. 2011. Systematic documentation and analysis of human genetic variation in hemoglobinopathies using the microattribution approach. Nat Genet 43: 295-301.
43. Gibson Q.H., Riggs A, Imamura T. 1973. Kinetic and equilibrium properties of hemoglobin Kansas. J. Biol Chem 248: 5976-5986.
44. Giordano P.C., Zweegman S, Akkermans N, Arkesteijn SGJ, van Delft Peter, Versteegh FGA, Wajcman Henri, Harteveld CL. 2007. The first case of Hb Groene Hart (α119[H2]Pro→Ser, CCT→TCT [α1]) homozygosity confirms that a thalassemia phenotype is associated with this abnormal hemoglobin variant. Hemoglobin 31: 179-182.
45. Griffon N., Badens C, Lena-Russo D, Kister J, Bardakdjian J, Wajcman H., Marden MC, Poyart C. 1996. Hb Bruxelles, deletion of Pheβ42, shows a low oxygen affinity and low cooperativity of ligand binding. J. Biol Chem 271: 25916-25920.
46. Hamilton H.B., Iuchi I, Miyaji T, Shibata S. 1969. Hemoglobin Hiroshima (β143 histidine→aspartic acid): A newly identified fast moving β chain variant associated with increased oxygen affinity and compensatory erythremia. J. Clin Invest 48: 525-535.
47. Hardison R., Chui D, Giardine B, Riemer C, Patrinos G, Anagnou N., MillerW, Wajcman H. 2002. HbVar: A relational database of human hemoglobin variants and thalassemia mutations at the globin gene server. Hum Mutat 19: 225-233.
48. Harteveld C., van Delft P, Plug R, Versteegh F, Hagen B, van Rooijen I., Kok P, Wajcman H, Kister J, Giordano PC. 2002. Hb Groene Hart: A new Pro→Ser amino acid substitution at position 119 of the α1-globin chain is associated with a mild α-thalassemia phenotype. Hemoglobin 26: 255-60.
49. Hayashi A., Shimizu A, Yamamura Y, Watari H. 1966. Hemoglobins M: Identification of Iwate, Boston, and Saskatoon variants. Science 152: 207-208.
50. Hebbel R.P., Eaton JW, Kronenberg RS, Zanjani ED, Moore L.G., Berger EM. 1978. Human llamas: Adaptation to altitude in subjects with high hemoglobin oxygen affinity. J Clin Invest 62: 593-600.
51. Honig G.R., Vida LN, Rosenblum BB, Perutz MF, Fermi G. 1990. Hemoglobin Warsaw (Pheβ42(CD1)→Val), an unstable variant with decreased oxygen affinity. Characterization of its synthesis, functional properties, and structure. J. Biol Chem 265: 126-132.
52. Horlein H., Weber G. 1948. Ueber chronische familiäre methämoglobinämie und eine neue modifikation des methämoglobins. Dtsch Med Wochenschr 73: 476-478.
53. Hoyer J.D., McCormick DJ, Snow K, Kwon JH, Booth D, Duarte M., Grayson G, Kubik KS, Holmes MW, Fairbanks VF. 2002. Four new variants of the α2-globin gene without clinical or hematologic effects: Hb Park Ridge (α9[α7]Asn→Lys [α2]), Hb Norton (α72[EF1]-His→Asp [α2]), Hb Lombard (α103[G10]His→Tyr [α2]), and Hb San Antonio (A113[GH2]Leu→Arg [A2]). Hemoglobin 26: 175-179.
54. Huisman TH. 1997. Hb E and α-thalassemia; variability in the assembly of βE chain containing tetramers. Hemoglobin 21: 227-236.
55. Huisman T.H., Horton B, Bridges MT, Betke K, Hitzig WH. 1961. A new abnormal human hemoglobin-Hb: Zurich. Clin Chim Acta 6: 347-355.
56. Hunt D.M., Higgs DR, Winichagoon P, Clegg JB, Weatherall DJ. 1982. Haemoglobin Constant Spring has an unstable α chain messenger RNA. Br J Haematol 51: 405-413.
57. Ikkala E., Koskela J, Pikkarainen P, Rahiala EL, El-Hazmi MA, Nagai K, Lang A, Lehmann H. 1976. Hb Helsinki: Avariant with a high oxygen affinity and a substitution at a 2,3-DPG binding site (β82[EF6] Lys replaced by Met). Acta Haematol 56: 257-275.
58. Imai K., Hamilton HB, Miyaji T, Shibata S. 1972. Physicochemical studies of the relation between structure and function in hemoglobin Hiroshima (HC3, histidine leads to aspartate). Biochemistry 11: 114-121.
59. Jin Y., Nagai M, Nagai Y, Nagatomo S, Kitagawa T. 2004. Heme structures of five variants of hemoglobinMprobed by resonance Raman spectroscopy. Biochemistry 43: 8517-8527.
60. Keeling M.M., Ogden LL, Wrightstone RN, Wilson JB, Reynolds C.A., Kitchens JL, Huisman TH. 1971. Hemoglobin Louisville (β-42 [CD1] phe-leu): An unstable variant causing mild hemolytic anemia. J Clin Invest 50: 2395-2402.
61. Khandros E., Mollan TL, Yu X, Wang X, Yao Y, D'Souza J, Gell D.A., Olson JS, Weiss MJ. 2012. Insights into hemoglobin assembly through in vivo mutagenesis of α-hemoglobin stabilizing protein. J BiolChem287: 11325-11327.
62. King M.A., Wiltshire BG, Lehmann H, Morimoto H. 1972. An unstable haemoglobin with reduced oxygen affinity: Haemoglobin Peterborough, 3 (GI3) Valine lead to Phenylalanine, its interaction with normal haemoglobin and with haemoglobin Lepore. Br J Haematol 22: 125-134.
63. Kohne E. 2011. Hemoglobinopathies: Clinical manifestations, diagnosis, and treatment. Dtsch Ä rztebl Int 108: 532.
64. KonigsbergW, Lehmann H. 1965. The amino acid substitution in hemoglobin M-Iwate. Biochim Biophys Acta 107: 266-269.
65. Konigsberg W., Guidotti G, Hill RJ. 1961. The amino acid sequence of the α chain of human hemoglobin. J. Biol Chem 236: PC55-PC56.
66. Lacan P., Aubry M, Couprie N, Francina A. 2004. Two new α chain variants: Hb Die (α93[FG5]Val→Ala [α1]) and Hb Beziers (α99[G6]Lys→Asn [α1]). Hemoglobin 28: 59-63.
67. Lacerra G., Scarano C, Musollino G, Flagiello A, Pucci P, Carestia C. 2008. Hb Foggia or α117(GH5)Phe→Ser: A new α2 globin allele affecting the αHb-AHSP interaction. Haematologica 93: 141-142.
68. Lal A., Goldrich ML, Haines DA, Azimi M, Singer ST, Vichinsky EP. 2011. Heterogeneity of hemoglobin H disease in childhood. N. Engl J Med 364: 710-718.
69. Langdown J.V., Davidson RJ, Williamson D. 1992. A new α chain variant, Hb Turriff (α99[G6]Lys→Glu): The interference of abnormal hemoglobins in Hb A1c determination. Hemoglobin 16: 11-17.
70. Lehmann H. 1957. Haemoglobin and its abnormalities. Practitioner 178: 198-214.
71. Lettre G. 2012. The search for genetic modifiers of disease severity in the β-hemoglobinopathies. Cold Spring Harb Perspect Med doi: 10.1101/cshperspect.a015032.
72. Levitt M. 1981. Effect of proline residues on protein folding. J. Mol Biol 145: 251-263.
73. Lindstrom T.R., Baldassare JJ, Bunn HF, Ho C. 1973. Nuclear magnetic resonance and spin-label studies of hemoglobin Kempsey. Biochemistry 12: 4212-4217.
74. Little R., Roberts W. 2009. A review of variant hemoglobins interfering with hemoglobin A1c measurement. J Diabetes Sci Technol 3: 446-451.
75. Lorkin P., Stephens A, Beard M, Wrigley P, Adams L, Lehmann H. 1975. Haemoglobin Rahere (β Lys-Thr): A new high affinity haemoglobin associated with decreased 2,3-diphosphoglycerate binding and relative polycythaemia. Br Med J 4: 200-202.
76. Marinucci M., Mavilio F, Massa A, Gabbianelli M, Fontanarosa PP, Camagna A, Ignesti C, Tentori L. 1979. A new abnormal human hemoglobin: Hb Prato (α2 31 [B12] Arg leads to Ser β2). Biochim Biophys Acta 578: 534-540.
77. Martínez G, Lima F, Colombo B. 1977. Haemoglobin J Guantanamo (α 2 β 2 128 [H6] Ala replaced by Asp). A new fast unstable haemoglobin found in a Cuban family. Biochim Biophys Acta 491: 1-6.
78. McDonald MJ, Lund DP, Bleichman M, Bunn HF, De Young A., Noble RW, Foster B, Arnone A. 1980. Equilibrium, kinetic and structural properties of hemoglobin Cranston, an elongated β chain variant. J. Mol Biol 140: 357-375.
79. Milner P.F., Clegg JB, Weatherall DJ. 1971. Haemoglobin-H disease due to a unique haemoglobin variant with an elongated α-chain. Lancet 1: 729-732.
80. Molchanova T.P., Postnikov YuV, Pobedimskaya DD, Smetanina NS, Moschan AA, Kazanetz EG, Tokarev YuN, Huisman TH. 1993. Hb Alesha or α 2 β (2)67 (E11)Val→Met: A new unstable hemoglobin variant identified through sequencing of amplified DNA. Hemoglobin 17: 217-225.
81. Mollan T.L., Khandros E, Weiss MJ, Olson JS. 2012. The kinetics of α-globin binding to α hemoglobin stabilizing protein (AHSP) indicate preferential stabilization of a hemichrome folding intermediate. J Biol Chem 287: 11338-11350.
82. Moo-Penn WF, Jue DL, Bechtel KC, Johnson MH, Schmidt RM. 1976. Hemoglobin Providence. A human hemoglobin variant occurring in two forms in vivo. J. Biol Chem 251: 7557-7562.
83. Moo-Penn W, Jue D, Johnson M, Olsen K, Shih D, Jones R, Lux S., Rodgers P, Arnone A. 1988. Hemoglobin Brockton (β 138 [H16] Ala→Pro): An unstable variant near the Cterminus of the β-subunits with normal oxygen-binding properties. Biochemistry 27: 7614-7619.
84. Morales J., Russell JE, Liebhaber SA. 1997. Destabilization of human α-globin mRNA by translation anti-termination is controlled during erythroid differentiation and is paralleled by phased shortening of the poly(A) tail. J Biol Chem 272: 6607-6613.
85. Musallam K.M., Taher AT, Rachmilewitz EA. 2012. β-Thalassemia intermedia: A clinical perspective. Cold Spring Harb Perspect Med doi: 10.1101/cshperspect.a013482.
86. Nagai M., Aki M, Li R, Jin Y, Sakai H, Nagatomo S, Kitagawa T. 2000. Heme structure of hemoglobinMIwate (α87[F8]His→Tyr): A UVand visible resonance Raman study. Biochemistry 39: 13093-13105.
87. Nagel R.L., Lynfield J, Johnson J, Landau L, Bookchin RM, Harris MB. 1976. Hemoglobin Beth Israel. A mutant causing clinically apparent cyanosis. N. Engl J Med 295: 125-130.
88. Nagel R.L., Bookchin RM, Johnson J, Labie D, Wajcman H, Isaac-Sodeye WA, Honig GR, Schilirò G, Crookston JH, Matsutomo K. 1979. Structural bases of the inhibitory effects of hemoglobin F and hemoglobin A2 on the polymerization of hemoglobin S. Proc Natl Acad Sci 76: 670-672.
89. Nathan D., Orkin S, Ginsburg D, Look A, Fisher D, Lux S. 2009. Nathan and Oski's hematology of infancy and childhood, 7th ed. Saunders Elsevier, Philadelphia.
90. Ohba Y., Miyaji T, Matsuoka M, Yokoyama M, Numakura H. 1975. Hemoglobin Hirosaki (α43 [CE 1] Phe replaced by Leu), a new unstable variant. Biochim Biophys Acta 405: 155-160.
91. Olson J., Gibson Q, Nagel R, Hamilton H. 1972. The ligand-binding properties of hemoglobin Hiroshima (α2β2 146 asp). J Biol Chem 247: 7485-7493.
92. Orkin S., Kazazian HJ, Antonarakis S, Ostrer H, Goff S, Sexton J. 1982. Abnormal RNA processing due to the exon mutation of βE-globin gene. Nature 300: 768-769.
93. Paoli M., Liddington R, Tame J, Wilkinson A, Dodson G. 1996. Crystal structure of Tstate haemoglobin with oxygen bound at all four haems. J Mol Biol 256: 775-792.
94. Park S., Yokoyama T, Shibayama N, Shiro Y, Tame JR. 2006. 1.25 A resolution crystal structures of human haemoglobin in the oxy, deoxy and carbonmonoxy forms. J Mol Biol 360: 690-701.
95. Perutz M. 1960. Structure of hemoglobin. Brookhaven Symp Biol 13: 165-183.
96. Perutz M. 1970. Stereochemistry of cooperative effects in haemoglobin. Nature 228: 726-739.
97. Perutz M., Lehmann H. 1968. Molecular pathology of human haemoglobin. Nature 219: 902-909.
98. Perutz M., Rossman M, Cullis A, Muirhead H, Will G, North A. 1960. Structure of haemoglobin: Three-dimensional Fourier synthesis at 5.5-A resolution, obtained by X-ray analysis. Nature 185: 416-422.
99. Perutz M.F., Muirhead H, Mazzarella L, Crowther RA, Greer J, Kilmartin JV. 1969. Identification of residues responsible for the alkaline Bohr effect in haemoglobin. Nature 222: 1240-1243.
100. Perutz M.F., Pulsinelli P, Eyck LT, Kilmartin JV, Shibata S, Iuchi I., Miyaji T, Hamilton HB. 1971. Haemoglobin Hiroshima and the mechanism of the alkaline Bohr effect. Nat New Biol 232: 147-149.
101. Perutz M., Fermi G, Shih TB. 1984. Structure of deoxyhemoglobin Cowtown (His HC3[146] β→Leu): Origin of the alkaline Bohr effect and electrostatic interactions in hemoglobin. Proc Natl Acad Sci 81: 4781-4784.
102. Phillips S.E., Hall D, Perutz MF. 1981. Structure of deoxyhaemoglobin Zürich (HisE7[63 β]-greater than Arg). J Mol Biol 150: 137-141.
103. Poyart C., Schaad O, Kister J, Galacteros F, Edelstein SJ, Blouquit Y., Arous N. 1990. Hemoglobin Saint Mandé[β102 (G4) Asn→Tyr]. Functional studies and structural modeling reveal an altered T state. Eur J Biochem 194: 343-348.
104. Pulsinelli P.D., Perutz M, Nagel R. 1973. Structure of hemoglobinMBoston, a variant with a five-coordinated ferric heme. Proc Natl Acad Sci 70: 3870-3874.
105. Rabbitts TH. 1976. Bacterial cloning of plasmids carrying copies of rabbit globin messenger RNA. Nature 260: 221-225.
106. Reed C.S., Hampson R, Gordon S, Jones RT, Novy MJ, Brimhall B., Edwards MJ, Koler RD. 1968. Erythrocytosis secondary to increased oxygen affinity of a mutant hemoglobin, hemoglobin Kempsey. Blood 31: 623-632.
107. Rees D.C., Rochette J, Schofield C, Green B, Morris M, Parker N.E., Sasaki H, Tanaka A, Ohba Y, Clegg JB. 1996. A novel silent posttranslational mechanism converts methionine to aspartate in hemoglobin Bristol (β67[E11] Val-Met→Asp). Blood 88: 341-348.
108. Rees D.C., Clegg JB, Weatherall DJ. 1998. Is hemoglobin instability important in the interaction between hemoglobin E and β thalassemia? Blood 92: 2141-2146.
109. Reissmann K., Ruth W, Nomura T. 1961. A human hemoglobin with lowered oxygen affinity and impaired hemeheme interactions. J Clin Invest 40: 1826-1833.
110. Rieder R.F., Oski FA, Clegg JB. 1969. Hemoglobin Philly (β35 tyrosine phenylalanine): Studies in the molecular pathology of hemoglobin. J. Clin Invest 48: 1627-1642.
111. Riggs A., Gibson QH. 1973. Oxygen equilibrium and kinetics of isolated subunits from hemoglobin Kansas. Proc Natl Acad Sci 70: 1718-1720.
112. Roth EF Jr, Elbaum D, Bookchin RM, Nagel RL. 1976. The conformational requirements for the mechanical precipitation of hemoglobin S and other mutants. Blood 48: 265-271.
113. Russu I.M., Ho C. 1986. Assessment of role of β 146-histidyl and other histidyl residues in the Bohr effect of human normal adult hemoglobin. Biochemistry 25: 1706-1716.
114. Sankaran V.G., Orkin SH. 2012. The switch from fetal to adult hemoglobin. Cold Spring Harb Perspect Med doi: 10.1101/cshperspect.a011643.
115. Schneider R.G., Bremner JE, Brimhall B, Jones RT, Shih TB. 1979. Hemoglobin Cowtown (β 146 HC3 His-Leu): A mutant with high oxygen affinity and erythrocytosis. Am J Clin Pathol 72: 1028-1032.
116. Schrier S.L., Bunyaratvej A, Khuhapinant A, Fucharoen S, Aljurf M., Snyder LM, Keifer CR, Ma L, Mohandas N. 1997. The unusual pathobiology of hemoglobin constant spring red blood cells. Blood 89: 1762-1769.
117. SchroederWA, Jones RT, Shelton JR, Shelton JB, Cormick J, McCalla K. 1961. A partial sequence of the amino acid residues in the γ chain of human hemoglobin F. ProcNatl Acad Sci 47: 811-818.
118. Sciarratta G.V., Ivaldi G, Molaro GL, Sansone G, Salkie ML, Wilson J.B., Reese AL, Huisman TH. 1984. The characterization of hemoglobinManitoba or α2102(G9)Ser→Arg β2 and hemoglobin Contaldo or α2103(G10)His→Arg β2 by high performance liquid chromatography. Hemoglobin 8: 169-181.
119. Shaeffer J.R., Schmidt GJ, Kingston RE, Bunn HF. 1980. Synthesis of hemoglobin Cranston, and elongated β chain variant. J Mol Biol 140: 377-389.
120. Schechter A. 2012. Hemoglobin function. Cold Spring Harb Perspect Med doi: 10.1101/cshperspect.a011650.
121. Schechter A., Elion J. 2012. Cold Spring Harb Perspect Med (to be published).
122. Serjeant G., Rodgers G. 2012. Natural history of sickle cell disease. Cold Spring Harb Perspect Med doi: 10.1101/ cshperspect.a011783.
123. Shibata S., Tanuira A, Iuchi I. 1960. Hemoglobin M1 demonstration of a new abnormal hemoglobin in hereditary nigremia. Acta Haematol Jpn 23: 96-105.
124. Shimizu A., Tsugita A, Hayashi A, Yamamura Y. 1965. The primary structure of hemoglobin M-Iwate. Biochim Biophys Acta 107: 270-277.
125. Springer B.A., Egeberg KD, Sligar SG, Rohlfs RJ, Mathews AJ, Olson JS. 1989. Discrimination between oxygen and carbon monoxide and inhibition of autooxidation by myoglobin. Site-directed mutagenesis of the distal histidine. J Biol Chem 264: 3057-3060.
126. Stamatoyannopoulos G., Parer JT, Finch CA. 1969. Physiologic implications of a hemoglobin with decreased oxygen affinity (hemoglobin seattle). N Engl J Med 281: 916-919.
127. Stamatoyannopoulos G., Woodson R, Papayannopoulou T, Heywood D., Kurachi S. 1974. Inclusion-body β-thalassemia trait. A form of β thalassemia producing clinical manifestations in simple heterozygotes. N Engl J Med 290: 939-943.
128. Steinberg M., Forget B, Higgs D, Nagel R. 2001. Disorders of hemoglobin: Genetics, pathophysiology, and clinical management. Cambridge University Press, Cambridge.
129. Sugihara J., Imamura T, Nagafuchi S, Bonaventura J, Bonaventura C, Cashon R. 1985. Hemoglobin Rahere, a human hemoglobin variant with amino acid substitution at the 2,3-diphosphoglycerate binding site. Functional consequences of the alteration and effects of bezafibrate on the oxygen bindings. J Clin Invest 76: 1169-73.
130. Tanaka Y., Matsui K, Matsuda K, Shinohara K, Haranob K. 2005. A family with hemoglobin Hirosaki. Int J Hematol 82: 124-126.
131. Thein S.L., Hesketh C, Taylor P, Temperley IJ, Hutchinson RM, Old JM, Wood WG, Clegg JB, Weatherall DJ. 1990. Molecular basis for dominantly inherited inclusion body β-thalassemia. Proc Natl Acad Sci 87: 3924-3928.
132. Tremper K., Barker S. 1989. Pulse oximetry. Anesthesiology 70: 98-108.
133. Tucker P.W., Phillips SE, Perutz MF, Houtchens R, Caughey WS. 1978. Structure of hemoglobins Zürich (His E7[63]β replaced by Arg) and Sydney (Val E11[67]β replaced by Ala) and role of the distal residues in ligand binding. Proc Natl Acad Sci 75: 1076-1080.
134. Turbpaiboon C., Limjindaporn T, Wongwiwat W, UPratya Y, Siritanaratkul N, Yenchitsomanus P-thai, Jitrapakdee S., Wilairat P. 2006. Impaired interaction of α-haemoglobin-stabilising protein with α-globin termination mutant in a yeast two-hybrid system. Br J Haematol 132: 370-373.
135. Vasseur C., Domingues-Hamdi E, Brillet T, Marden Michael C., Baudin-Creuza V. 2009. The α-hemoglobin stabilizing protein and expression of unstable α-Hb variants. Clin Biochem 42: 1818-1823.
136. Vasseur-Godbillon C, Marden M, Giordano P, Wajcman H, Baudin-Creuza V. 2006. Impaired binding of AHSP to α chain variants: Hb Groene Hart illustrates a mechanism leading to unstable hemoglobins with α thalassemic like syndrome. Blood Cells Mol Dis 37: 173-179.
137. Verhovsek M., Henderson M, Cox G, Luo H, Steinberg M, Chui D. 2010. Unexpectedly low pulse oximetry measurements associated with variant hemoglobins: A systematic review. Am J Hematol 85: 882-885.
138. Viprakasit V., Tanphaichitr VS. 2002. Compound heterozygosity for α0-thalassemia (--THAI) and Hb constant spring causes severe Hb H disease. Hemoglobin 26: 155-162.
139. Wajcman H., Moradkhani K. 2011. Abnormal haemoglobins: Detection and characterization. Indian J Med Res 134: 538-546.
140. Wajcman H., Préhu C, Bardakdjian-Michau J, Promé D, Riou J., Godart C, Mathis M, Hurtrel D, Galactéros F. 2001. Abnormal hemoglobins: Laboratory methods. Hemoglobin 25: 169-181.
141. Wajcman H., Traeger-Synodinos J, Papassotiriou I, Giordano PC, Harteveld CL, Baudin-Creuza V, Old J. 2008. Unstable and thalassemic αchain hemoglobin variants:A cause of Hb H disease and thalassemia intermedia. Hemoglobin 32: 327-349.
142. Watson H.C., Kendrew JC. 1961. The amino-acid sequence of sperm whale myoglobin. Comparison between the amino-acid sequences of sperm whale myoglobin and of human hemoglobin. Nature 190: 670-672.
143. Watson-Williams EJ, BealeD, IrvineD, Lehmann H. 1965. A new haemoglobin, D-Ibadan (β-87 threonine-lysine), producing no sickle-cell haemoglobin D disease with haemoglobin S. Nature 205: 1273-1276.
144. Weatherall D., Clegg J. 2001. Inherited haemoglobin disorders: An increasing global health problem. Bull World Health Organ 79: 704-712.
145. Weiss I.M., Liebhaber SA. 1994. Erythroid cell-specific determinants of α-globin mRNA stability. Mol Cell Biol 14: 8123-8132.
146. Weiss M.J., Zhou S, Feng L, GellDA, Mackay JP, Shi Y, GowAJ. 2005. Role of α-hemoglobin-stabilizing protein in normal erythropoiesis and β-thalassemia. Ann NY Acad Sci 1054: 103-117.
147. Williams T.N., Weatherall DJ. 2012. World distribution, population genetics, and health burden of the hemoglobinopathies. Cold Spring Harb Perspect Med doi: 10.1101/ cshperspect.a011692.
148. Witkowska H.E., Lubin BH, Beuzard Y, Baruchel S, Esseltine D.W., Vichinsky EP, Kleman KM, Bardakdjian-Michau J., Pinkoski L, Cahn S. 1991. Sickle cell disease in a patient with sickle cell trait and compound heterozygosity for hemoglobin S and hemoglobin Quebec-Chori. N Engl J Med 325: 1150-1154.
149. Yu X., Mollan TL, Butler Andrew, Gow AJ, Olson JS, Weiss MJ. 2009. Analysis of human α globin gene mutations that impair binding to the α hemoglobin stabilizing protein. Blood 113: 5961-5969.