Cloning and in vivo expression of vascular endothelial growth factor receptor 2 (Flk1) in the naturally hypoxia-tolerant subterranean mole rat

FASEB Journal

Volumn 22, Issue 1, 2008, Pages 105-112

  Band, Mark ^a   Shams, Imad ^b   Joel, Alma ^b   Avivi, Aaron ^b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF HAIFA   (Israel)

Author keywords

Spalax ehrenbergi; VEGF R2

Indexed keywords

AMINO ACID; NUCLEIC ACID; VASCULOTROPIN RECEPTOR 2; COMPLEMENTARY DNA; MESSENGER RNA; PRIMER DNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLINDNESS; BRAIN REGION; CONTROLLED STUDY; HYPOXIA; IN VIVO STUDY; MOLE RAT; MOLECULAR CLONING; MUSCLE; NONHUMAN; ORTHOLOGY; OXYGEN SUPPLY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ADAPTATION; ANIMAL; ANOXIA; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; OPEN READING FRAME;

ANIMALIA; MAMMALIA; NANNOSPALAX EHRENBERGI; RATTUS; SPALAX;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANOXIA; BASE SEQUENCE; CLONING, MOLECULAR; DNA PRIMERS; DNA, COMPLEMENTARY; MOLE RATS; OPEN READING FRAMES; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 38049188324     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.07-8892com     Document Type: Article

References (52)

1. Arieli, R., Ar, A., and Skolnik, A. (1977) Metabolic responses of a fossorial rodent (Spalax ehrenbergi) to stimulated burrow conditions. Physiol. Zool. 50, 61-75
2. Ar, A., Arieli, R., and Shkolnik, A. (1977) Blood-gas properties and function in the fossorial mole rat under normal and hypoxic-hypercapnic atmospheric conditions. Respir. Physiol. 30, 201-219
3. Nevo, E. (1961) Observations on Israeli populations of the mole rat, Spalax ehrenbergi (Nehring, 1898). Mammalia 25, 127-144
4. Nevo, E. (1999) Mosaic Evolution of Subterranean Mammals: Regression, Progression and Global Convergence, Oxford Univ. Press, Oxford
5. Nevo, E., Ivanitskaya, E., and Beiles, A. (2001) Adaptive Radiation of Blind Subterranean Mole Rats, Backhuys, Leiden
6. Burlington, R. F., and Maher, J. T. (1968) Effect of anoxia on mechanical performance of isolated atria from ground squirrels and rats acclimatized to altitude. Nature 219, 1370-1371
7. Kerem, D., Hammond, D. D., and Elsner, R. (1973) Tissue glycogen levels in the Weddell seal, Leptonychotes weddelli: a possible adaptation to asphyxial hypoxia. Comp. Biochem. Physiol. A. 45, 731-736
8. Arieli, R., Heth, G., Nevo, E., Zamir, Y., and Neutra, O. (1986) Adaptive heart and breathing frequencies in 4 ecologically differentiating chromosomal species of mole rats in Israel. Experientia 42, 131-133
9. Arieli, R., Heth, G., Nevo, E., and Hoch, D. (1986) Hematocrit and hemoglobin concentration in four chromosomal species and some isolated populations of actively speciating subterranean mole rats in Israel. Experientia 42, 441-443
10. Arieli, R., Arieli, M., Heth, G., and Nevo, E. (1984) Adaptive respiratory variation in 4 chromosomal species of mole rats. Experientia. 40, 512-514
11. Arieli, R., and Nevo, E. (1991) Hypoxic survival differs between two mole rat species (Spalax ehrenbergi) of humid and arid habitats. Comp. Biochem. Physiol. A. 100, 543-545
12. Avivi, A., Resnick, M. B., Nevo, E., Joel, A., and Levy, A. P. (1999) Adaptive hypoxic tolerance in the subterranean mole rat Spalax ehrenbergi: the role of vascular endothelial growth factor. FEBS Lett. 452, 133-140
13. Shams, I., Avivi, A., and Nevo, E. (2005) Oxygen and carbon dioxide fluctuations in burrows of subterranean blind mole rats indicate tolerance to hypoxic-hypercapnic stresses. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 142, 376-382
14. Nevo, E., Ben-Shlomo, R., and Maeda, N. (1989) Haptoglobin DNA polymorphism in subterranean mole rats of the Spalax ehrenbergi superspecies in Israel. Heredity 62 (Pt 1), 85-90
15. Kleinschmidt, T., Nevo, E., and Braunitzer, G. (1984) The primary structure of the hemoglobin of the mole rat (Spalax ehrenbergi, rodentia, chromosome species 60). Hoppe. Seylers. Z. Physiol. Chem. 365, 531-537
16. Hankeln, T., Ebner, B., Fuchs, C., Gerlach, F., Haberkamp, M., Laufs, T. L., Roesner, A., Schmidt, M., Weich, B., Wystub, S., et al. (2005) Neuroglobin and cytoglobin in search of their role in the vertebrate globin family. J. Inorg. Biochem. 99, 110-119
17. Gurnett, A. M., O'Connell, J., Harris, D. E., Lehmann, H., Joysey, K. A. and Nevo, E. (1984) The myoglobin of rodents: Lagostomus maximus (viscacha) and Spalax ehrenbergi (mole rat). J. Protein. Chem. 3, 445-454
18. Shams, I., Avivi, A., and Nevo, E. (2004) Hypoxic stress tolerance of the blind subterranean mole rat: expression of erythropoietin and hypoxia-inducible factor 1 alpha. Proc. Natl. Acad. Sci. U. S. A. 101, 9698-9703
19. Shams, I., Nevo, E., and Avivi, A. (2005) Ontogenetic expression of erythropoietin and hypoxia-inducible factor-1 alpha genes in subterranean blind mole rats. FASEB J. 19, 307-309
20. Shams, I., Nevo, E., and Avivi, A. (2005) Erythropoietin receptor spliced forms differentially expressed in blind subterranean mole rats. FASEB J. 19, 1749-1751
21. Ashur-Fabian, O., Avivi, A., Trakhtenbrot, L., Adamsky, K., Cohen, M., Kajakaro, G., Joel, A., Amariglio, N., Nevo, E., and Rechavi, G. (2004) Evolution of p53 in hypoxia-stressed Spalax mimics human tumor mutation. Proc. Natl. Acad. Sci. U. S. A. 101, 12236-12241
22. Avivi, A., Ashur-Fabian, O., Joel, A., Trakhtenbrot, L., Adamsky, K., Goldstein, I., Amariglio, N., Rechavi, G., and Nevo, E. (2006) P53 in blind subterranean mole rats - loss-of-function versus gain-of-function activities on newly cloned Spalax target genes. Oncogene 26, 2507-2512
23. Shweiki, D., Itin, A., Soffer, D., and Keshet, E. (1992) Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359, 843-845
24. Wiener, C. M., Booth, G., and Semenza, G. L. (1996) In vivo expression of mRNAs encoding hypoxia-inducible factor 1. Biochem. Biophys. Res. Commun. 225, 485-488
25. Levy, N. S., Chung, S., Furneaux, H., and Levy, A. P. (1998) Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J. Biol. Chem. 273, 6417-6423
26. Avivi, A., Shams, I., Joel, A., Lache, O., Levy, A. P., and Nevo, E. (2005) Increased blood vessel density provides the mole rat physiological tolerance to its hypoxic subterranean habitat. FASEB J. 19, 1314-1316
27. Ferrara, N., Gerber, H. P., and LeCouter, J. (2003) The biology of VEGF and its receptors. Nat. Med. 9, 669-676
28. Yang, S., Xin, X., Zlot, C., Ingle, G., Fuh, G., Li, B., Moffat, B., de Vos, A. M., and Gerritsen, M. E. (2001) Vascular endothelial cell growth factor-driven endothelial tube formation is mediated by vascular endothelial cell growth factor receptor-2, a kinase insert domain-containing receptor. Arterioscler. Thromb. Vasc. Biol. 21, 1934-1940
29. Shalaby, F., Rossant, J., Yamaguchi, T. P., Gertsenstein, M., Wu, X. F., Breitman, M. L., and Schuh, A. C. (1995) Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376, 62-66
30. Avivi, A., Brodsky, L., Nevo, E., and Band, M. R. (2006) Differential expression profiling of the blind subterranean mole rat Spalax ehrenbergi superspecies: bioprospecting for hypoxia tolerance. Physiol. Genomics 27, 54-64
31. Widmer, H. R., Hoppeler, H., Nevo, E., Taylor, C. R., and Weibel, E. R. (1997) Working underground: respiratory adaptations in the blind mole rat. Proc. Natl. Acad. Sci. U. S. A. 94, 2062-2067
32. Bustin, S. A. (2002) Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): trends and problems. J. Mol. Endocrinol. 29, 23-39
33. Wang, Y., Jin, K., Mao, X. O., Xie, L., Banwait, S., Marti, H. H., and Greenberg, D. A. (2007) VEGF-overexpressing transgenic mice show enhanced post-ischemic neurogenesis and neuromigration. J. Neurosci. Res. 85, 740-747
34. Shiote, M., Nagano, I., Ilieva, H., Murakami, T., Narai, H., Ohta, Y., Nagata, T., Shoji, M., and Abe, K. (2005) Reduction of a vascular endothelial growth factor receptor, fetal liver kinase-1, by antisense oligonucleotides induces motor neuron death in rat spinal cord exposed to hypoxia. Neuroscience 132, 175-182
35. Laudenbach, V., Fontaine, R. H., Medja, F., Carmeliet, P., Hicklin, D. J., Gallego, J., Leroux, P., Marret, S., and Gressens, P. (2007) Neonatal hypoxic preconditioning involves vascular endothelial growth factor. Neurobiol. Dis. 26, 243-252
36. Xiao, Z., Kong, Y., Yang, S., Li, M., Wen, J., and Li, L. (2007) Upregulation of Flk-1 by bFGF via the ERK pathway is essential for VEGF-mediated promotion of neural stem cell proliferation. Cell Res. 17, 73-79
37. Zeller, K., Vogel, J., and Kuschinsky, W. (1996) Postnatal distribution of Glut1 glucose transporter and relative capillary density in blood-brain barrier structures and circumventricular organs during development. Brain Res. Dev. Brain Res. 91, 200-208
38. Kremer, C., Breier, G., Risau, W., and Plate, K. H. (1997) Up-regulation of flk-1/vascular endothelial growth factor receptor 2 by its ligand in a cerebral slice culture system. Cancer Res. 57, 3852-3859
39. Hare, G. M. (2004) Anaemia and the brain. Curr. Opin. Anaesthesiol. 17, 363-369
40. Harik, N., Harik, S. I., Kuo, N. T., Sakai, K., Przybylski, R. J., and LaManna, J. C. (1996) Time-course and reversibility of the hypoxia-induced alterations in cerebral vascularity and cerebral capillary glucose transporter density. Brain Res. 737, 335-338
41. Jensen, A., Garnier, Y., and Berger, R. (1999) Dynamics of fetal circulatory responses to hypoxia and asphyxia. Eur. J. Obstet. Gynecol. Reprod. Biol. 84, 155-172
42. Lou, H. C., Edvinsson, L., and MacKenzie, E. T. (1987) The concept of coupling blood flow to brain function: revision required? Ann. Neurol. 22, 289-297
43. Andresen, J., Shafi, N. I., and Bryan, R. M., Jr. (2006) Endothelial influences on cerebrovascular tone. J. Appl. Physiol. 100, 318-327
44. Gilbert, R. D., Pearce, W. J., and Longo, L. D. (2003) Fetal cardiac and cerebrovascular acclimatization responses to high altitude, long-term hypoxia. High Alt. Med. Biol. 4, 203-213
45. Soderstrom, V., Renshaw, G. M., and Nilsson, G. E. (1999) Brain blood flow and blood pressure during hypoxia in the epaulette shark Hemiscyllium ocellatum, a hypoxia-tolerant elasmo-branch. J. Exp. Biol. 202, 829-835
46. Soderstrom, V., Nilsson, G. E., Renshaw, G. M., and Franklin, C. E. (1999) Hypoxia stimulates cerebral blood flow in the estuarine crocodile (Crocodylus porosus). Neurosci. Lett. 267, 1-4
47. Rissanen, T. T., Vajanto, I., Hiltunen, M. O., Rutanen, J., Kettunen, M. I., Niemi, M., Leppanen, P., Turunen, M. P., Markkanen, J. E., Arve, K., et al. (2002) Expression of vascular endothelial growth factor and vascular endothelial growth factor receptor-2 (KDR/Flk-1) in ischemic skeletal muscle and its regeneration. Am. J. Pathol. 160, 1393-1403
48. Kappel, A., Schlaeger, T. M., Flamme, I., Orkin, S. H., Risau, W., and Breier, G. (2000) Role of SCL/Tal-1, GATA, and ets transcription factor binding sites for the regulation of flk-1 expression during murine vascular development. Blood 96, 3078-3085
49. Gerber, H. P., Condorelli, F., Park, J., and Ferrara, N. (1997) Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. Flt-1, but not Flk-1/KDR, is up-regulated by hypoxia. J. Biol. Chem. 272, 23659-23667
50. Elvert, G., Kappel, A., Heidenreich, R., Englmeier, U., Lanz, S., Acker, T., Rauter, M., Plate, K., Sieweke, M., Breier, G., and Flamme, I. (2003) Cooperative interaction of hypoxia-inducible factor-2alpha (HIF-2alpha) and Ets-1 in the transcriptional activation of vascular endothelial growth factor receptor-2 (Flk-1). J. Biol. Chem. 278, 7520-7530
51. Choi, J., Dong, L., Ahn, J., Dao, D., Hammerschmidt, M., and Chen, J. N. (2007) FoxH1 negatively modulates flk1 gene expression and vascular formation in zebrafish. Dev. Biol. 304, 735-744
52. Shen, B. Q., Lee, D. Y., Gerber, H. P., Keyt, B. A., Ferrara, N., and Zioncheck, T. F. (1998) Homologous up-regulation of KDR/Flk-1 receptor expression by vascular endothelial growth factor in vitro. J. Biol. Chem. 273, 29979-29985