Hypoxia. 5. Hypoxia and hematopoiesis

American Journal of Physiology - Cell Physiology

Volumn 300, Issue 6, 2011, Pages

  Yoon, Donghoon ^a   Ponka, Prem ^b   Prchal, Josef T ^a  

^a UNIVERSITY OF UTAH   (United States)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Erythropoiesis; Hypoxia inducible factor; Oxygen delivery

Indexed keywords

ERYTHROPOIETIN; HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; MESSENGER RNA; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; TRANSCRIPTION FACTOR;

ALTITUDE DISEASE; ARTICLE; BRAIN; CHRONIC DISEASE; CHUVASH POLYCYTHEMIA; ENZYME DEFICIENCY; ERYTHROCYTE; ERYTHROPOIESIS; GENE MUTATION; HEMATOPOIESIS; HUMAN; HYPOXIA; IRON METABOLISM; LYMPHOPOIESIS; NONHUMAN; OXYGEN TENSION; POLYCYTHEMIA; PRIORITY JOURNAL; PROLINE HYDROXYLASE DEFICIENCY; REGULATORY MECHANISM; TISSUE OXYGENATION; TISSUE SPECIFICITY; VON HIPPEL LINDAU DISEASE;

ANIMALS; ANOXIA; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN; CELL HYPOXIA; CELL LINEAGE; ERYTHROPOIETIN; HEMATOPOIESIS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; IRON; KIDNEY; LIVER; OXYGEN; PLURIPOTENT STEM CELLS; PROTEIN ISOFORMS; SYNDROME;

EID: 79957649497     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00044.2011     Document Type: Article

References (91)

1. Abbrecht PH, Littell JK. Plasma erythropoietin in men and mice during acclimatization to different altitudes. J Appl Physiol 32: 54-58, 1972.
2. Adelman DM, Maltepe E, Simon MC. Multilineage embryonic hematopoiesis requires hypoxic ARNT activity. Genes Dev 13: 2478-2483, 1999.
3. Agarwal N, Gordeuk RV, Prchal JT. Genetic mechanisms underlying regulation of hemoglobin mass. Adv Exp Med Biol 618: 195-210, 2007.
4. Al-Sheikh M, Moradkhani K, Lopez M, Wajcman H, Prehu C. Disturbance in the HIF-1alpha pathway associated with erythrocytosis: further evidences brought by frameshift and nonsense mutations in the prolyl hydroxylase domain protein 2 (PHD2) gene. Blood Cells Mol Dis 40: 160-165, 2008.
5. Ang SO, Chen H, Gordeuk VR, Sergueeva AI, Polyakova LA, Miasnikova GY, Kralovics R, Stockton DW, Prchal JT. Endemic polycythemia in Russia: mutation in the VHL gene. Blood Cells Mol Dis 28: 57-62, 2002.
6. Ang SO, Chen H,ota K, Gordeuk VR, Jelinek J, Guan Y, Liu E, Sergueeva AI, Miasnikova GY, Mole D, Maxwell PH, Stockton DW, Semenza GL, Prchal JT. Disruption of oxygen homeostasis underlies congenital Chuvash polycythemia. Nat Genet 32: 614-621, 2002.
7. Bachmann S, Eckardt KU. Co-localization of erythropoietin mRNA and ecto-5'-nucleotidase immunoreactivity in peritubular cells of rat renal cortex indicates that fibroblasts produce erythropoietin. J Histochem Cytochem 41: 335-341, 1993.
8. Beall CM. Two routes to functional adaptation: Tibetan and Andean high-altitude natives. Proc Natl Acad Sci USA 104, Suppl 1: 8655-8660, 2007.
9. Beck I, Ramirez S, Weinmann R, Caro J. Enhancer element at the 3'-flanking region controls transcriptional response to hypoxia in the human erythropoietin gene. J Biol Chem 266: 15563-15566, 1991.
10. Ben-Shoshan J, Maysel-Auslender S, Mor A, Keren G, George J. Hypoxia controls CD4+CD25+ regulatory T-cell homeostasis via hypoxiainducible factor-1alpha. Eur J Immunol 38: 2412-2418, 2008.
11. Bennett CL, Christie J, Ramsdell F, Brunkow ME, Ferguson PJ, Whitesell L, Kelly TE, Saulsbury FT, Chance PF, Ochs HD. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat Genet 27: 20-21, 2001.
12. Bento MC, Chang KT, Guan Y, Liu E, Caldas G, Gatti RA, Prchal JT. Congenital polycythemia with homozygous and heterozygous mutations of von Hippel-Lindau gene: five new Caucasian patients. Haematologica 90: 128-129, 2005.
13. Bernaudin M, Bellail A, Marti HH, Yvon A, Vivien D, Duchatelle I, Mackenzie ET, Petit E. Neurons and astrocytes express EPO mRNA: oxygen-sensing mechanisms that involve the redox-state of the brain. Glia 30: 271-278, 2000.
14. Brand KA, Hermfisse U. Aerobic glycolysis by proliferating cells: a protective strategy against reactive oxygen species. FASEB J 11: 388-395, 1997.
15. Brunkow ME, Jeffery EW, Hjerrild KA, Paeper B, Clark LB, Yasayko SA, Wilkinson JE, Galas D, Ziegler SF, Ramsdell F. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat Genet 27: 68-73, 2001.
16. Burke B, Tang N, Corke KP, Tazzyman D, Ameri K, Wells M, Lewis CE. Expression of HIF-1alpha by human macrophages: implications for the use of macrophages in hypoxia-regulated cancer gene therapy. J Pathol 196: 204-212, 2002.
17. Cario H, Schwarz K, Jorch N, Kyank U, Petrides PE, Schneider DT, Uhle R, Debatin KM, Kohne E. Mutations in the von Hippel-Lindau (VHL) tumor suppressor gene and VHL-haplotype analysis in patients with presumable congenital erythrocytosis. Haematologica 90: 19-24, 2005.
18. Collins TS, Arcasoy MO. Iron overload due to X-linked sideroblastic anemia in an African American man. Am J Med 116: 501-502, 2004.
19. Cramer T, Yamanishi Y, Clausen BE, Forster I, Pawlinski R, Mackman N, Haase VH, Jaenisch R, Corr M, Nizet V, Firestein GS, Gerber HP, Ferrara N, Johnson RS. HIF-1alpha is essential for myeloid cellmediated inflammation. Cell 112: 645-657, 2003.
20. Divoky V, Liu Z, Ryan TM, Prchal JF, Townes TM, Prchal JT. Mouse model of congenital polycythemia: homologous replacement of murine gene by mutant human erythropoietin receptor gene. Proc Natl Acad Sci USA 98: 986-991, 2001.
21. Fandrey J. Oxygen-dependent and tissue-specific regulation of erythropoietin gene expression. Am J Physiol Regul Integr Comp Physiol 286: R977-R988, 2004.
22. Fischer B, Bavister BD. Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil 99: 673-679, 1993.
23. Friedrich CA. Von Hippel-Lindau syndrome. A pleomorphic condition. Cancer 86: 2478-2482, 1999.
24. Gordeuk VR, Sergueeva AI, Miasnikova GY, et al. Congenital disorder of oxygen sensing: Association of the homozygous Chuvash polycythemia VHL mutation with thrombosis and vascular abnormalities but not tumors. Blood 103: 3924, 2004.
25. Gordeuk VR, Stockton DW, Prchal JT. Congenital polycythemias/ erythrocytoses. Haematologica 90: 109-116, 2005.
26. Haase VH, Glickman JN, Socolovsky M, Jaenisch R. Vascular tumors in livers with targeted inactivation of the von Hippel-Lindau tumor suppressor. Proc Natl Acad Sci USA 98: 1583-1588, 2001.
27. Hollander AP, Corke KP, Freemont AJ, Lewis CE. Expression of hypoxia-inducible factor 1alpha by macrophages in the rheumatoid synovium: implications for targeting of therapeutic genes to the inflamed joint. Arthritis Rheum 44: 1540-1544, 2001.
28. Huang X, Pierce LJ, Chen GL, Chang KT, Spangrude GJ, Prchal JT. Erythropoietin receptor signaling regulates both erythropoiesis and megakaryopoiesis in vivo. Blood Cells Mol Dis 44: 1-6, 2010.
29. Imagawa S, Suzuki N, Ohmine K, Obara N, Mukai HY, Ozawa K, Yamamoto M, Nagasawa T. GATA suppresses erythropoietin gene expression through GATA site in mouse erythropoietin gene promoter. Int J Hematol 75: 376-381, 2002.
30. Imagawa S, Yamamoto M, Miura Y. Negative regulation of the erythropoietin gene expression by the GATA transcription factors. Blood 89: 1430-1439, 1997.
31. Iyer NV, Kotch LE, Agani F, Leung SW, Laughner E, Wenger RH, Gassmann M, Gearhart JD, Lawler AM, Yu AY, Semenza GL. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev 12: 149-162, 1998.
32. Kapitsinou PP, Liu Q, Unger TL, Rha J, Davidoff O, Keith B, Epstein JA, Moores SL, Erickson-Miller CL, Haase VH. Hepatic HIF-2 regulates erythropoietic responses to hypoxia in renal anemia. Blood 116: 3039-3048, 2010.
33. Kenneth NS, Rocha S. Regulation of gene expression by hypoxia. Biochem J 414: 19-29, 2008.
34. Khattri R, Cox T, Yasayko SA, Ramsdell F. An essential role for Scurfin in CD4+CD25+ Tregulatory cells. Nat Immunol 4: 337-342, 2003.
35. Kojima H, Gu H, Nomura S, Caldwell CC, Kobata T, Carmeliet P, Semenza GL, Sitkovsky MV. Abnormal B lymphocyte development and autoimmunity in hypoxia-inducible factor 1alpha-deficient chimeric mice. Proc Natl Acad Sci USA 99: 2170-2174, 2002.
36. Koury MJ, Ponka P. New insights into erythropoiesis: the roles of folate, vitamin B12, and iron. Annu Rev Nutr 24: 105-131, 2004.
37. Krantz SB. Erythropoietin. Blood 77: 419-434, 1991.
38. Krieg M, Marti HH, Plate KH. Coexpression of erythropoietin and vascular endothelial growth factor in nervous system tumors associated with von Hippel-Lindau tumor suppressor gene loss of function. Blood 92: 3388-3393, 1998.
39. Lee PL, Gelbart T, West C, Halloran C, Beutler E. The human Nramp2 gene: characterization of the gene structure, alternative splicing, promoter region and polymorphisms. Blood Cells Mol Dis 24: 199-215, 1998.
40. Liu E, Percy MJ, Amos CI, Guan Y, Shete S, Stockton DW, McMullin MF, Polyakova LA, Ang SO, Pastore YD, Jedlickova K, Lappin TR, Gordeuk V, Prchal JT. The worldwide distribution of the VHL 598C>T mutation indicates a single founding event. Blood 103: 1937-1940, 2004.
41. Lok CN, Ponka P. Identification of a hypoxia response element in the transferrin receptor gene. J Biol Chem 274: 24147-24152, 1999.
42. Lorenzo VFR, Simonson TS, Yang Y, Ge R, Prchal JT. A Novel PHD2 Mutation Associated with Tibetan Genetic Adaptation to High Altitude Hypoxia. ASH Annual Meeting Abstracts 116: 2602.
43. Maltepe E, Schmidt JV, Baunoch D, Bradfield CA, Simon MC. Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature 386: 403-407, 1997.
44. Manalo DJ, Rowan A, Lavoie T, Natarajan L, Kelly BD, Ye SQ, Garcia JGN, Semenza GL. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 105: 659-669, 2005.
45. Marti HH, Wenger RH, Rivas LA, Straumann U, Digicaylioglu M, Henn V, Yonekawa Y, Bauer C, Gassmann M. Erythropoietin gene expression in human, monkey and murine brain. Eur J Neurosci 8: 666-676, 1996.
46. Mastrogiannaki M, Matak P, Keith B, Simon MC, Vaulont S, Peyssonnaux C. HIF-2alpha, but not HIF-1alpha, promotes iron absorption in mice. J Clin Invest 119: 1159-1166, 2009.
47. Maxwell PH, Osmond MK, Pugh CW, Heryet A, Nicholls LG, Tan CC, Doe BG, Ferguson DJ, Johnson MH, Ratcliffe PJ. Identification of the renal erythropoietin-producing cells using transgenic mice. Kidney Int 44: 1149-1162, 1993.
48. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399: 271-275, 1999.
49. Obara N, Suzuki N, Kim K, Nagasawa T, Imagawa S, Yamamoto M. Repression via the GATA box is essential for tissue-specific erythropoietin gene expression. Blood 111: 5223-5232, 2008.
50. Pastore Y, Jedlickova K, Guan Y, Liu E, Fahner J, Hasle H, Prchal JF, Prchal JT. Mutations of von Hippel-Lindau tumor-suppressor gene and congenital polycythemia. Am J Hum Genet 73: 412-419, 2003.
51. Pastore YD, Jelinek J, Ang S, Guan Y, Liu E, Jedlickova K, Krishnamurti L, Prchal JT. Mutations in the VHL gene in sporadic apparently congenital polycythemia. Blood 101: 1591-1595, 2003.
52. Percy MJ, Beard ME, Carter C, Thein SL. Erythrocytosis and the Chuvash von Hippel-Lindau mutation. Br J Haematol 123: 371-372, 2003.
53. Percy MJ, Beer PA, Campbell G, Dekker AW, Green AR, Oscier D, Rainey MG, van Wijk R, Wood M, Lappin TR, McMullin MF, Lee FS. Novel exon 12 mutations in the HIF2A gene associated with erythrocytosis. Blood 111: 5400-5402, 2008.
54. Percy MJ, Furlow PW, Beer PA, Lappin TR, McMullin MF, Lee FS. A novel erythrocytosis-associated PHD2 mutation suggests the location of a HIF binding groove. Blood 110: 2193-2196, 2007.
55. Percy MJ, Furlow PW, Lucas GS, Li X, Lappin TR, McMullin MF, Lee FS. A gain-of-function mutation in the HIF2A gene in familial erythrocytosis. N Engl J Med 358: 162-168, 2008.
56. Percy MJ, McMullin MF, Jowitt SN, Potter M, Treacy M, Watson WH, Lappin TR. Chuvash-type congenital polycythemia in 4 families of Asian and Western European ancestry. Blood 102: 1097-1099, 2003.
57. Percy MJ, Zhao Q, Flores A, Harrison C, Lappin TR, Maxwell PH, McMullin MF, Lee FS. A family with erythrocytosis establishes a role for prolyl hydroxylase domain protein 2 in oxygen homeostasis. Proc Natl Acad Sci USA 103: 654-659, 2006.
58. Perrotta S, Cucciolla V, Ferraro M, Ronzoni L, Tramontano A, Rossi F, Scudieri AC, Borriello A, Roberti D, Nobili B, Cappellini MD, Oliva A, Amendola G, Migliaccio AR, Mancuso P, Martin-Padura I, Bertolini F, Yoon D, Prchal JT, Della Ragione F. EPO receptor gain-of-function causes hereditary polycythemia, alters CD34 cell differentiation and increases circulating endothelial precursors. PLoS One 5, 2010.
59. Perrotta S, Nobili B, Ferraro M, Migliaccio C, Borriello A, Cucciolla V, Martinelli V, Rossi F, Punzo F, Cirillo P, Parisi G, Zappia V, Rotoli B, Ragione FD. Von Hippel-Lindau-dependent polycythemia is endemic on the island of Ischia: identification of a novel cluster. Blood 107: 514-519, 2006.
60. Peyssonnaux C, Nizet V, Johnson RS. Role of the hypoxia inducible factors HIF in iron metabolism. Cell Cycle 7: 28-32, 2008.
61. Phillips PG, Birnby LM, Narendran A. Hypoxia induces capillary network formation in cultured bovine pulmonary microvessel endothelial cells. Am J Physiol Lung Cell Mol Physiol 268: L789-L800, 1995.
62. Polyakova LA. Familial erythrocytosis among inhabitants of the Chuvash ASSR. Probl Gematol 10: 30, 1974.
63. Prchal JT. Production of Erythrocytes. In: Williams Hematology (8th Ed), edited by Kaushansky K, Lichtman MA, Kipps TJ, Beutler E, Seligsohn U, Prchal JT. New York: McGraw Hill, 2010, p. 435-449.
64. Prchal JT. Secondary polycythemia (erythrocytosis). In: Williams Hematology (8th ed.), edited by Kaushansky K, Lichtman MA, Kipps TJ, Beutler E, Seligsohn U, Prchal JT. New York: McGraw Hill, 2010, p. 823-839.
65. Pugh CW, Ebert BL, Ebrahim O, Maxwell PH, Ratcliffe PJ. Analysis of cis-acting sequences required for operation of the erythropoietin 3' enhancer in different cell lines. Ann NY Acad Sci 718: 31-40, 1994.
66. Ramirez-Bergeron DL, Runge A, Dahl KD, Fehling HJ, Keller G, Simon MC. Hypoxia affects mesoderm and enhances hemangioblast specification during early development. Development 131: 4623-4634, 2004.
67. Rankin EB, Biju MP, Liu Q, Unger TL, Rha J, Johnson RS, Simon MC, Keith B, Haase VH. Hypoxia-inducible factor-2 (HIF-2) regulates hepatic erythropoietin in vivo. J Clin Invest 117: 1068-1077, 2007.
68. Rankin EB, Higgins DF, Walisser JA, Johnson RS, Bradfield CA, Haase VH. Inactivation of the arylhydrocarbon receptor nuclear translocator (Arnt) suppresses von Hippel-Lindau disease-associated vascular tumors in mice. Mol Cell Biol 25: 3163-3172, 2005.
69. Ratcliffe PJ, O'Rourke JF, Maxwell PH, Pugh CW. Oxygen sensing, hypoxia-inducible factor-1 and the regulation of mammalian gene expression. J Exp Biol 201: 1153-1162, 1998.
70. Rennie D, Frayster R, Gray G, Houston CS. Urine and plasma proteins in men at 5,400 m. J Appl Physiol 32: 369-373, 1972.
71. Richards FM. Molecular pathology of von HippelLindau disease and the VHL tumour suppressor gene. Expert Rev Mol Med 2001: 1-27, 2001.
72. Rodesch F, Simon P, Donner C, Jauniaux E. Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet Gynecol 80: 283-285, 1992.
73. Rolfs A, Kvietikova I, Gassmann M, Wenger RH. Oxygen-regulated transferrin expression is mediated by hypoxia-inducible factor-1. J Biol Chem 272: 20055-20062, 1997.
74. Sandoval H, Thiagarajan P, Dasgupta SK, Schumacher A, Prchal JT, Chen M, Wang J. Essential role for Nix in autophagic maturation of erythroid cells. Nature 454: 232-235, 2008.
75. Schuh AC, Faloon P, Hu QL, Bhimani M, Choi K. In vitro hematopoietic and endothelial potential of flk-1(-/-) embryonic stem cells and embryos. Proc Natl Acad Sci USA 96: 2159-2164, 1999.
76. Scortegagna M, Ding K, Zhang Q, Oktay Y, Bennett MJ, Bennett M, Shelton JM, Richardson JA, Moe O, Garcia JA. HIF-2alpha regulates murine hematopoietic development in an erythropoietin-dependent manner. Blood 105: 3133-3140, 2005.
77. Scortegagna M, Morris MA, Oktay Y, Bennett M, Garcia JA. The HIF family member EPAS1/HIF-2alpha is required for normal hematopoiesis in mice. Blood 102: 1634-1640, 2003.
78. Semenza GL. HIF-1 and mechanisms of hypoxia sensing. Curr Opin Cell Biol 13: 167-171, 2001.
79. Semenza GL, Dureza RC, Traystman MD, Gearhart JD, Antonarakis SE. Human erythropoietin gene expression in transgenic mice: multiple transcription initiation sites and cis-acting regulatory elements. Mol Cell Biol 10: 930-938, 1990.
80. Semenza GL, Koury ST, Nejfelt MK, Gearhart JD, Antonarakis SE. Cell-type-specific and hypoxia-inducible expression of the human erythropoietin gene in transgenic mice. Proc Natl Acad Sci USA 88: 8725-8729, 1991.
81. Semenza GL, Traystman MD, Gearhart JD, Antonarakis SE. Polycythemia in transgenic mice expressing the human erythropoietin gene. Proc Natl Acad Sci USA 86: 2301-2305, 1989.
82. Semenza GL, Wang GL. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol 12: 5447-5454, 1992.
83. Sergeyeva A, Gordeuk VR, Tokarev YN, Sokol L, Prchal JF, Prchal JT. Congenital polycythemia in Chuvashia. Blood 89: 2148-2154, 1997.
84. Simonson TS, Yang Y, Huff CD, Yun H, Qin G, Witherspoon DJ, Bai Z, Lorenzo FR, Xing J, Jorde LB, Prchal JT, Ge R. Genetic evidence for high-altitude adaptation in Tibet. Science 329: 72-75, 2010.
85. Sokol L, Luhovy M, Guan Y, Prchal JF, Semenza GL, Prchal JT. Primary familial polycythemia: a frameshift mutation in the erythropoietin receptor gene and increased sensitivity of erythroid progenitors to erythropoietin. Blood 86: 15-22, 1995.
86. Stopka T, Zivny JH, Stopkova P, Prchal JF, Prchal JT. Human hematopoietic progenitors express erythropoietin. Blood 91: 3766-3772, 1998.
87. Tacchini L, Bianchi L, Bernelli-Zazzera A, Cairo G. Transferrin receptor induction by hypoxia. HIF-1-mediated transcriptional activation and cell-specific post-transcriptional regulation. J Biol Chem 274: 24142-24146, 1999.
88. Talks KL, Turley H, Gatter KC, Maxwell PH, Pugh CW, Ratcliffe PJ, Harris AL. The expression and distribution of the hypoxia-inducible factors HIF-1alpha and HIF-2alpha in normal human tissues, cancers, and tumor-associated macrophages. Am J Pathol 157: 411-421, 2000.
89. Weidemann A, Johnson RS. Nonrenal regulation of EPO synthesis. Kidney Int 75: 682-688, 2009.
90. Weidemann A, Kerdiles YM, Knaup KX, Rafie CA, Boutin AT, Stockmann C, Takeda N, Scadeng M, Shih AY, Haase VH, Simon MC, Kleinfeld D, Johnson RS. The glial cell response is an essential component of hypoxia-induced erythropoiesis in mice. J Clin Invest 119: 3373-3383, 2009.
91. Yoon D, Pastore YD, Divoky V, Liu E, Mlodnicka AE, Rainey K, Ponka P, Semenza GL, Schumacher A, Prchal JT. Hypoxia-inducible factor-1 deficiency results in dysregulated erythropoiesis signaling and iron homeostasis in mouse development. J Biol Chem 281: 25703-25711, 2006.