Expression profiling reveals novel hypoxic biomarkers in peripheral blood of adult mice exposed to chronic hypoxia

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Mosqueira, Matias ^a,b   Willmann, Gabriel ^a,c,d   Zeiger, Ulrike ^a,e   Khurana, Tejvir S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY OF COLOGNE   (Germany)

^d UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^e UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; OXIDOREDUCTASE; PYRROLINE 5 CARBOXYLATE REDUCTASE 1; SPECTRIN ALPHA 1; UBIQUITIN; UBIQUITIN DOMAIN FAMILY 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; DOWN REGULATION; EXPOSURE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENETIC MARKER; ISCHEMIA; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; REAL TIME POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION; UPREGULATION; WILD TYPE;

ANIMALS; ANOXIA; BIOLOGICAL MARKERS; GENE EXPRESSION PROFILING; MICE; PYRROLINE CARBOXYLATE REDUCTASES; RNA, MESSENGER; SPECTRIN; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

MUS;

EID: 84861325303     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037497     Document Type: Article

References (70)

1. Windsor JS, Rodway GW, (2007) Heights and haematology: the story of haemoglobin at altitude. Postgrad Med J 83: 148-151.
2. Kellogg RH, (1978) "La Pression barometrique": Paul Bert's hypoxia theory and its critics. Respir Physiol 34: 1-28.
3. Jelkmann W, (1986) Erythropoietin research, 80 years after the initial studies by Carnot and Deflandre. Respir Physiol 63: 257-266.
4. Ebert BL, Bunn HF, (1999) Regulation of the erythropoietin gene. Blood 94: 1864-1877.
5. Miyake T, Kung CK, Goldwasser E, (1977) Purification of human erythropoietin. J Biol Chem 252: 5558-5564.
6. Fisher JW, (2003) Erythropoietin: physiology and pharmacology update. Exp Biol Med (Maywood) 228: 1-14.
7. Wang GL, Semenza GL, (1995) Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 270: 1230-1237.
8. Wenger RH, (2000) Mammalian oxygen sensing, signalling and gene regulation. J Exp Biol 203: 1253-1263.
9. Stroka DM, Burkhardt T, Desbaillets I, Wenger RH, Neil DA, et al. (2001) HIF-1 is expressed in normoxic tissue and displays an organ-specific regulation under systemic hypoxia. Faseb J 15: 2445-2453.
10. Baze MM, Schlauch K, Hayes JP, (2010) Gene expression of the liver in response to chronic hypoxia. Physiol Genomics.
11. Benita Y, Kikuchi H, Smith AD, Zhang MQ, Chung DC, et al. (2009) An integrative genomics approach identifies Hypoxia Inducible Factor-1 (HIF-1)-target genes that form the core response to hypoxia. Nucleic Acids Res 37: 4587-4602.
12. Rogers HM, Yu X, Wen J, Smith R, Fibach E, et al. (2008) Hypoxia alters progression of the erythroid program. Exp Hematol 36: 17-27.
13. Dennis G, Jr, Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3.
14. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
15. Houwen B, (2002) Blood film preparation and staining procedures. Clin Lab Med 22: 1-14, v.
16. Gharib SA, Dayyat EA, Khalyfa A, Kim J, Clair HB, et al. (2010) Intermittent hypoxia mobilizes bone marrow-derived very small embryonic-like stem cells and activates developmental transcriptional programs in mice. Sleep 33: 1439-1446.
17. Balbir A, Lee H, Okumura M, Biswal S, Fitzgerald RS, et al. (2007) A search for genes that may confer divergent morphology and function in the carotid body between two strains of mice. Am J Physiol Lung Cell Mol Physiol 292: L704-715.
18. Gaber T, Haupl T, Sandig G, Tykwinska K, Fangradt M, et al. (2009) Adaptation of human CD4+ T cells to pathophysiological hypoxia: a transcriptome analysis. J Rheumatol 36: 2655-2669.
19. Hammond EM, Mandell DJ, Salim A, Krieg AJ, Johnson TM, et al. (2006) Genome-wide analysis of p53 under hypoxic conditions. Mol Cell Biol 26: 3492-3504.
20. Juul SE, Beyer RP, Bammler TK, McPherson RJ, Wilkerson J, et al. (2009) Microarray analysis of high-dose recombinant erythropoietin treatment of unilateral brain injury in neonatal mouse hippocampus. Pediatr Res 65: 485-492.
21. Komor M, Guller S, Baldus CD, de Vos S, Hoelzer D, et al. (2005) Transcriptional profiling of human hematopoiesis during in vitro lineage-specific differentiation. Stem Cells 23: 1154-1169.
22. Roiniotis J, Dinh H, Masendycz P, Turner A, Elsegood CL, et al. (2009) Hypoxia prolongs monocyte/macrophage survival and enhanced glycolysis is associated with their maturation under aerobic conditions. J Immunol 182: 7974-7981.
23. Gheorghe CP, Mohan S, Oberg KC, Longo LD, (2007) Gene expression patterns in the hypoxic murine placenta: a role in epigenesis? Reprod Sci 14: 223-233.
24. Lai Y, Brandhorst H, Hossain H, Bierhaus A, Chen C, et al. (2009) Activation of NFkappaB dependent apoptotic pathway in pancreatic islet cells by hypoxia. Islets 1: 19-25.
25. Pfafflin A, Brodbeck K, Heilig CW, Haring HU, Schleicher ED, et al. (2006) Increased glucose uptake and metabolism in mesangial cells overexpressing glucose transporter 1 increases interleukin-6 and vascular endothelial growth factor production: role of AP-1 and HIF-1alpha. Cell Physiol Biochem 18: 199-210.
26. Salim A, Nacamuli RP, Morgan EF, Giaccia AJ, Longaker MT, (2004) Transient changes in oxygen tension inhibit osteogenic differentiation and Runx2 expression in osteoblasts. J Biol Chem 279: 40007-40016.
27. van den Beucken T, Magagnin MG, Jutten B, Seigneuric R, Lambin P, et al. (2011) Translational control is a major contributor to hypoxia induced gene expression. Radiother Oncol 99: 379-384.
28. Pistilli EE, Bogdanovich S, Mosqueira M, Lachey J, Seehra J, et al. (2010) Pretreatment with a soluble activin type IIB receptor/Fc fusion protein improves hypoxia-induced muscle dysfunction. Am J Physiol Regul Integr Comp Physiol 298: R96-R103.
29. Dill RP, Chadan SG, Li C, Parkhouse WS, (2001) Aging and glucose transporter plasticity in response to hypobaric hypoxia. Mech Ageing Dev 122: 533-545.
30. Harik SI, Behmand RA, LaManna JC, (1994) Hypoxia increases glucose transport at blood-brain barrier in rats. J Appl Physiol 77: 896-901.
31. Savourey G, Launay JC, Besnard Y, Guinet A, Bourrilhon C, et al. (2004) Control of erythropoiesis after high altitude acclimatization. Eur J Appl Physiol 93: 47-56.
32. Xia Y, Warshaw JB, Haddad GG, (1997) Effect of chronic hypoxia on glucose transporters in heart and skeletal muscle of immature and adult rats. Am J Physiol 273: R1734-1741.
33. Forbes WH, (1936) Blood sugar and glucose tolerance at high altutides. Am J Physiol 30: 309.
34. Pison CM, Chauvin C, Fontaine E, Catelloni F, Keriel C, et al. (1995) Mechanism of gluconeogenesis inhibition in rat hepatocytes isolated after in vivo hypoxia. Am J Physiol 268: E965-973.
35. Ogawa Y, Masuzaki H, Isse N, Okazaki T, Mori K, et al. (1995) Molecular cloning of rat obese cDNA and augmented gene expression in genetically obese Zucker fatty (fa/fa) rats. J Clin Invest 96: 1647-1652.
36. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, et al. (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372: 425-432.
37. Hoggard N, Hunter L, Duncan JS, Williams LM, Trayhurn P, et al. (1997) Leptin and leptin receptor mRNA and protein expression in the murine fetus and placenta. Proc Natl Acad Sci U S A 94: 11073-11078.
38. Bado A, Levasseur S, Attoub S, Kermorgant S, Laigneau JP, et al. (1998) The stomach is a source of leptin. Nature 394: 790-793.
39. Wang J, Liu R, Hawkins M, Barzilai N, Rossetti L, (1998) A nutrient-sensing pathway regulates leptin gene expression in muscle and fat. Nature 393: 684-688.
40. Morash B, Li A, Murphy PR, Wilkinson M, Ur E, (1999) Leptin gene expression in the brain and pituitary gland. Endocrinology 140: 5995-5998.
41. Schwartz MW, Woods SC, Porte D, Jr, Seeley RJ, Baskin DG, (2000) Central nervous system control of food intake. Nature 404: 661-671.
42. Yingzhong Y, Droma Y, Rili G, Kubo K, (2006) Regulation of body weight by leptin, with special reference to hypoxia-induced regulation. Intern Med 45: 941-946.
43. Ahima RS, (2000) Leptin and the neuroendocrinology of fasting. Front Horm Res 26: 42-56.
44. Anubhuti, Arora S, (2008) Leptin and its metabolic interactions: an update. Diabetes Obes Metab 10: 973-993.
45. Friedman JM, Halaas JL, (1998) Leptin and the regulation of body weight in mammals. Nature 395: 763-770.
46. Ahima RS, Flier JS, (2000) Leptin. Annu Rev Physiol 62: 413-437.
47. Ambrosini G, Nath AK, Sierra-Honigmann MR, Flores-Riveros J, (2002) Transcriptional activation of the human leptin gene in response to hypoxia. Involvement of hypoxia-inducible factor 1. J Biol Chem 277: 34601-34609.
48. Grosfeld A, Andre J, Hauguel-De Mouzon S, Berra E, Pouyssegur J, et al. (2002) Hypoxia-inducible factor 1 transactivates the human leptin gene promoter. J Biol Chem 277: 42953-42957.
49. Ou LC, Leiter JC, (2004) Effects of exposure to a simulated altitude of 5500 m on energy metabolic pathways in rats. Respir Physiol Neurobiol 141: 59-71.
50. Ou LC, (1980) Hypoxia-induced hemoglobinemia: hypoxic threshold and pathogenic mechanism. Exp Hematol 8: 243-248.
51. Koistinen PO, Rusko H, Irjala K, Rajamaki A, Penttinen K, et al. (2000) EPO, red cells, and serum transferrin receptor in continuous and intermittent hypoxia. Med Sci Sports Exerc 32: 800-804.
52. Hill NS, Petit RD, Gagnon J, Warburton RR, Ou LC, (1993) Hematologic responses and the early development of hypoxic pulmonary hypertension in rats. Respir Physiol 91: 261-270.
53. Febbraio M, Hajjar DP, Silverstein RL, (2001) CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation, and lipid metabolism. J Clin Invest 108: 785-791.
54. Serghides L, Smith TG, Patel SN, Kain KC, (2003) CD36 and malaria: friends or foes? Trends Parasitol 19: 461-469.
55. Telen MJ, (2000) Red blood cell surface adhesion molecules: their possible roles in normal human physiology and disease. Semin Hematol 37: 130-142.
56. Telen MJ, (2005) Erythrocyte adhesion receptors: blood group antigens and related molecules. Transfus Med Rev 19: 32-44.
57. Kwapiszewska G, Wilhelm J, Wolff S, Laumanns I, Koenig IR, et al. (2005) Expression profiling of laser-microdissected intrapulmonary arteries in hypoxia-induced pulmonary hypertension. Respir Res 6: 109.
58. Mwaikambo BR, Yang C, Chemtob S, Hardy P, (2009) Hypoxia up-regulates CD36 expression and function via hypoxia-inducible factor-1- and phosphatidylinositol 3-kinase-dependent mechanisms. J Biol Chem 284: 26695-26707.
59. Gonzalez-Cinca N, Perez de la Ossa P, Carreras J, Climent F, (2004) Effects of thyroid hormone and hypoxia on 2,3-bisphosphoglycerate, bisphosphoglycerate synthase and phosphoglycerate mutase in rabbit erythroblasts and reticulocytes in vivo. Horm Res 62: 191-196.
60. Pascual J, Pfuhl M, Rivas G, Pastore A, Saraste M, (1996) The spectrin repeat folds into a three-helix bundle in solution. FEBS Lett 383: 201-207.
61. Shotton DM, Burke BE, Branton D, (1979) The molecular structure of human erythrocyte spectrin. Biophysical and electron microscopic studies. J Mol Biol 131: 303-329.
62. Speicher DW, (1984) Structural and functional features of the alpha-1 domain from human erythrocyte spectrin. Prog Clin Biol Res 165: 441-456.
63. Yan Y, Winograd E, Viel A, Cronin T, Harrison SC, et al. (1993) Crystal structure of the repetitive segments of spectrin. Science 262: 2027-2030.
64. Baines AJ, (2009) Evolution of spectrin function in cytoskeletal and membrane networks. Biochem Soc Trans 37: 796-803.
65. Chakrabarti A, Kelkar DA, Chattopadhyay A, (2006) Spectrin organization and dynamics: new insights. Biosci Rep 26: 369-386.
66. Fenner BJ, Scannell M, Prehn JH, (2009) Identification of polyubiquitin binding proteins involved in NF-kappaB signaling using protein arrays. Biochim Biophys Acta 1794: 1010-1016.
67. Kim JW, Tchernyshyov I, Semenza GL, Dang CV, (2006) HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 3: 177-185.
68. Adams E, (1970) Metabolism of proline and of hydroxyproline. Int Rev Connect Tissue Res 5: 1-91.
69. Yeh GC, Phang JM, (1980) The function of pyrroline-5-carboxylate reductase in human erythrocytes. Biochem Biophys Res Commun 94: 450-457.
70. Mense SM, Sengupta A, Zhou M, Lan C, Bentsman G, et al. (2006) Gene expression profiling reveals the profound upregulation of hypoxia-responsive genes in primary human astrocytes. Physiol Genomics 25: 435-449.