Distinct post-transcriptional regulation of Igfbp1 gene by hypoxia in lowland mouse and Qinghai-Tibet plateau root vole Microtus oeconomus

Molecular and Cellular Endocrinology

Volumn 376, Issue 1-2, 2013, Pages 33-42

  Zhang, Shengting ^a   Zhao, Yang ^a,b   Hu, Xiaofeng ^a   Liu, Zongyun ^a,b   Chen, Xiaocheng ^c   Chen, Xuequn ^a,b   Du, Jizeng ^a,b  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c NORTHWEST INSTITUTE OF PLATEAU BIOLOGY   (China)

Author keywords

Hypoxia; Insulin like growth factor; Microtus oeconomus; Mouse; MRNA stability; U rich element

Indexed keywords

MESSENGER RNA; SOMATOMEDIN BINDING PROTEIN 1; SOMATOMEDIN C;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ARTICLE; CHINA; CONTROLLED STUDY; GENE; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; HYPOXIA; IGFBP1 GENE; MALE; MOLECULAR CLONING; MOLECULAR EVOLUTION; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA STABILITY; SEQUENCE ANALYSIS; UPREGULATION;

HYPOXIA; INSULIN-LIKE GROWTH FACTOR; MICROTUS OECONOMUS; MOUSE; MRNA STABILITY; U-RICH ELEMENT;

ADAPTATION, BIOLOGICAL; AMINO ACID SEQUENCE; ANIMALS; ANOXIA; ARVICOLINAE; BIOLOGICAL EVOLUTION; CELL LINE; GENE EXPRESSION REGULATION; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 1; INSULIN-LIKE GROWTH FACTOR I; LIVER; MALE; MICE; MICE, INBRED ICR; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA STABILITY; RNA, MESSENGER; SEQUENCE ALIGNMENT; TIBET;

EID: 84879531283     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2013.05.025     Document Type: Article

References (60)

1. Abbas A., Grant P.J., Kearney M.T. Role of IGF-1 in glucose regulation and cardiovascular disease. Expert Rev. Cardiovasc. Ther. 2008, 6:1135-1149.
2. Annunziata M., Granata R., Ghigo E. The IGF system. Acta Diabetol. 2011, 48:1-9.
3. Baxter R.C. Insulin-like growth factor (IGF)-binding proteins: interactions with IGFs and intrinsic bioactivities. Am. J. Physiol. Endocrinol Metab. 2000, 278. E967-76.
4. Bonefeld K., Moller S. Insulin-like growth factor-I and the liver. Liver Int. 2011, 31:911-919.
5. Brunhoff C., Galbreath K.E., Fedorov V.B., Cook J.A., Jaarola M. Holarctic phylogeography of the root vole (Microtus oeconomus): implications for late Quaternary biogeography of high latitudes. Mol. Ecol. 2003, 12:957-968.
6. Bunn R.C., Fowlkes J.L. Insulin-like growth factor binding protein proteolysis. Trends Endocrinol. Metab. 2003, 14:176-181.
7. Cao Y.B., Chen X.Q., Wang S., Wang Y.X., Du J.Z. Evolution and regulation of the downstream gene of hypoxia-inducible factor-1alpha in naked carp (Gymnocypris przewalskii) from Lake Qinghai, China. J. Mol. Evol. 2008, 67:570-580.
8. Cao Y.B., Chen X.Q., Wang S., Chen X.C., Wang Y.X., Chang J.P., Du J.Z. Growth hormone and insulin-like growth factor of naked carp (Gymnocypris przewalskii) in Lake Qinghai: expression in different water environments. Gen. Comp. Endocrinol. 2009, 161:400-406.
9. Chen Z., Du J.Z. Hypoxia effects on hypothalamic corticotropin-releasing hormone and anterior pituitary cAMP. Zhongguo Yao Li Xue Bao. 1996, 17:489-492.
10. Chen X.Q., Xu N.Y., Du J.Z., Wang Y., Duan C. Corticotropin-releasing factor receptor subtype 1 and somatostatin modulating hypoxia-caused downregulated mRNA of pituitary growth hormone and upregulated mRNA of hepatic insulin-like growth factor-I of rats. Mol. Cell. Endocrinol. 2005, 242:50-58.
11. Chen X.Q., Wang S.J., Du J.Z., Chen X.C. Diversities in hepatic HIF-1, IGF-I/IGFBP-1, LDH/ICD, and their mRNA expressions induced by CoCl(2) in Qinghai-Tibetan plateau mammals and sea level mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292. R516-26.
12. Daughaday W.H., Parker K.A., Borowsky S., Trivedi B., Kapadia M. Measurement of somatomedin-related peptides in fetal, neonatal, and maternal rat serum by insulin-like growth factor (IGF) I radioimmunoassay, IGF-II radioreceptor assay (RRA), and multiplication-stimulating activity RRA after acid-ethanol extraction. Endocrinology 1982, 110:575-581.
13. Dormoy-Raclet V., Menard I., Clair E., Kurban G., Mazroui R., Di Marco S., von Roretz C., Pause A., Gallouzi I.E. The RNA-binding protein HuR promotes cell migration and cell invasion by stabilizing the beta-actin mRNA in a U-rich-element-dependent manner. Mol. Cell. Biol. 2007, 27:5365-5380.
14. Duan C., Xu Q. Roles of insulin-like growth factor (IGF) binding proteins in regulating IGF actions. Gen. Comp. Endocrinol. 2005, 142:44-52.
15. El-Desoky A.E., Seifalian A.M., Davidson B.R. Effect of graded hypoxia on hepatic tissue oxygenation measured by near infrared spectroscopy. J. Hepatol. 1999, 31:71-76.
16. Eliasz S., Liang S., Chen Y., De Marco M.A., Machek O., Skucha S., Miele L., Bocchetta M. Notch-1 stimulates survival of lung adenocarcinoma cells during hypoxia by activating the IGF-1R pathway. Oncogene 2010, 29:2488-2498.
17. Ezzat V.A., Duncan E.R., Wheatcroft S.B., Kearney M.T. The role of IGF-I and its binding proteins in the development of type 2 diabetes and cardiovascular disease. Diabetes Obes. Metab. 2008, 10:198-211.
18. Fukuda R., Hirota K., Fan F., Jung Y.D., Ellis L.M., Semenza G.L. Insulin-like growth factor 1 induces hypoxia-inducible factor 1-mediated vascular endothelial growth factor expression, which is dependent on MAP kinase and phosphatidylinositol 3-kinase signaling in colon cancer cells. J. Biol. Chem. 2002, 277:38205-38211.
19. Gay E., Babajko S. AUUUA sequences compromise human insulin-like growth factor binding protein-1 mRNA stability. Biochem. Biophys. Res. Commun. 2000, 267:509-515.
20. Gehmert S., Sadat S., Song Y.H., Yan Y., Alt E. The anti-apoptotic effect of IGF-1 on tissue resident stem cells is mediated via PI3-kinase dependent secreted frizzled related protein 2 (Sfrp2) release. Biochem. Biophys. Res. Commun. 2008, 371:752-755.
21. Gibson J.M., Aplin J.D., White A., Westwood M. Regulation of IGF bioavailability in pregnancy. Mol. Hum. Reprod. 2001, 7:79-87.
22. Goldstein S., Phillips L.S. Extraction and nutritional/hormonal regulation of tissue insulin-like growth factor 1 activity. J. Biol. Chem. 1991, 266:14725-14731.
23. Harrison T.M., Copeland P., Kidd W.S., Yin A. Raising tibet. Science 1992, 255:1663-1670.
24. Hwa V., Oh Y., Rosenfeld R.G. The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocr. Rev. 1999, 20:761-787.
25. Jansson M., Uhlen M., Nilsson B. Structural changes in insulin-like growth factor (IGF) I mutant proteins affecting binding kinetic rates to IGF binding protein 1 and IGF-I receptor. Biochemistry 1997, 36:4108-4117.
26. Jansson M., Andersson G., Uhlen M., Nilsson B., Kordel J. The insulin-like growth factor (IGF) binding protein 1 binding epitope on IGF-I probed by heteronuclear NMR spectroscopy and mutational analysis. J. Biol. Chem. 1998, 273:24701-24707.
27. Jones J.I., Gockerman A., Busby W.H., Wright G., Clemmons D.R. Insulin-like growth factor binding protein 1 stimulates cell migration and binds to the alpha 5 beta 1 integrin by means of its Arg-Gly-Asp sequence. Proc. Natl. Acad. Sci. USA 1993, 90:10553-10557.
28. Jungermann K., Kietzmann T. Oxygen: modulator of metabolic zonation and disease of the liver. Hepatology 2000, 31:255-260.
29. Kajimura S., Aida K., Duan C. Insulin-like growth factor-binding protein-1 (IGFBP-1) mediates hypoxia-induced embryonic growth and developmental retardation. Proc. Natl. Acad. Sci. USA 2005, 102:1240-1245.
30. Kajimura S., Aida K., Duan C. Understanding hypoxia-induced gene expression in early development: in vitro and in vivo analysis of hypoxia-inducible factor 1-regulated zebra fish insulin-like growth factor binding protein 1 gene expression. Mol. Cell. Biol. 2006, 26:1142-1155.
31. Khabar K.S. Post-transcriptional control during chronic inflammation and cancer: a focus on AU-rich elements. Cell. Mol. Life Sci. 2010, 67:2937-2955.
32. Lee P.D., Giudice L.C., Conover C.A., Powell D.R. Insulin-like growth factor binding protein-1: recent findings and new directions. Proc. Soc. Exp. Biol. Med. 1997, 216:319-357.
33. Lee C., Raffaghello L., Longo V.D. Starvation, detoxification, and multidrug resistance in cancer therapy. Drug Resist. Update 2012, 15:114-122.
34. Levy N.S., Chung S., Furneaux H., Levy A.P. Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J. Biol. Chem. 1998, 273:6417-6423.
35. Liu W., D'Ercole J.A., Ye P. Blunting type 1 insulin-like growth factor receptor expression exacerbates neuronal apoptosis following hypoxic/ischemic injury. BMC Neurosci. 2011, 12:64.
36. Magne L., Blanc E., Marchand A., Fafournoux P., Barouki R., Rouach H., Garlatti M. Stabilization of IGFBP-1 mRNA by ethanol in hepatoma cells involves the JNK pathway. J. Hepatol. 2007, 47:691-698.
37. McGary E.C., Rondon I.J., Beckman B.S. Post-transcriptional regulation of erythropoietin mRNA stability by erythropoietin mRNA-binding protein. J. Biol. Chem. 1997, 272:8628-8634.
38. Mehrhof F.B., Muller F.U., Bergmann M.W., Li P., Wang Y., Schmitz W., Dietz R., von Harsdorf R. In cardiomyocyte hypoxia, insulin-like growth factor-I-induced antiapoptotic signaling requires phosphatidylinositol-3-OH-kinase-dependent and mitogen-activated protein kinase-dependent activation of the transcription factor cAMP response element-binding protein. Circulation 2001, 104:2088-2094.
39. Murphy L.J. Overexpression of insulin-like growth factor binding protein-1 in transgenic mice. Pediatr. Nephrol. 2000, 14:567-571.
40. Ohlsson C., Mohan S., Sjogren K., Tivesten A., Isgaard J., Isaksson O., Jansson J.O., Svensson J. The role of liver-derived insulin-like growth factor-I. Endocr. Rev. 2009, 30:494-535.
41. Ohtsuki T., Otsuki M., Murakami Y., Maekawa T., Yamamoto T., Akasaka K., Takeuchi S., Takahashi S. Organ-specific and age-dependent expression of insulin-like growth factor-I (IGF-I) mRNA variants: IGF-IA and IB mRNAs in the mouse. Zool. Sci. 2005, 22:1011-1021.
42. Powell D.R., Allander S.V., Scheimann A.O., Wasserman R.M., Durham S.K., Suwanichkul A. Multiple proteins bind the insulin response element in the human IGFBP-1 promoter. Prog. Growth Factor Res. 1995, 6:93-101.
43. Qiu Q., Zhang G., Ma T., Qian W., Wang J., Ye Z., Cao C., Hu Q., Kim J., Larkin D.M., Auvil L., Capitanu B., Ma J., Lewin H.A., Qian X., Lang Y., Zhou R., Wang L., Wang K., Xia J., Liao S., Pan S., Lu X., Hou H., Wang Y., Zang X., Yin Y., Ma H., Zhang J., Wang Z., Zhang Y., Zhang D., Yonezawa T., Hasegawa M., Zhong Y., Liu W., Huang Z., Zhang S., Long R., Yang H., Lenstra J.A., Cooper D.N., Wu Y., Shi P., Liu J. The yak genome and adaptation to life at high altitude. Nat. Genet. 2012, 44:946-949.
44. Rajpathak S.N., Gunter M.J., Wylie-Rosett J., Ho G.Y., Kaplan R.C., Muzumdar R., Rohan T.E., Strickler H.D. The role of insulin-like growth factor-I and its binding proteins in glucose homeostasis and type 2 diabetes. Diabetes Metab. Res. Rev. 2009, 25:3-12.
45. Ream M., Ray A.M., Chandra R., Chikaraishi D.M. Early fetal hypoxia leads to growth restriction and myocardial thinning. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 295. R583-95.
46. Sala A., Capaldi S., Campagnoli M., Faggion B., Labo S., Perduca M., Romano A., Carrizo M.E., Valli M., Visai L., Minchiotti L., Galliano M., Monaco H.L. Structure and properties of the C-terminal domain of insulin-like growth factor-binding protein-1 isolated from human amniotic fluid. J. Biol. Chem. 2005, 280:29812-29819.
47. Scharf J.G., Unterman T.G., Kietzmann T. Oxygen-dependent modulation of insulin-like growth factor binding protein biosynthesis in primary cultures of rat hepatocytes. Endocrinology 2005, 146:5433-5443.
48. Seferovic M.D., Ali R., Kamei H., Liu S., Khosravi J.M., Nazarian S., Han V.K., Duan C., Gupta M.B. Hypoxia and leucine deprivation induce human insulin-like growth factor binding protein-1 hyperphosphorylation and increase its biological activity. Endocrinology 2009, 150:220-231.
49. Seifalian A.M., El-Desoky H., Delpy D.T., Davidson B.R. Effect of graded hypoxia on the rat hepatic tissue oxygenation and energy metabolism monitored by near-infrared and 31P nuclear magnetic resonance spectroscopy. FASEB J. 2001, 15:2642-2648.
50. Smith T.J. Insulin-like growth factor-I regulation of immune function: a potential therapeutic target in autoimmune diseases?. Pharmacol. Rev. 2010, 62:199-236.
51. Sugawara J., Tazuke S.I., Suen L.F., Powell D.R., Kaper F., Giaccia A.J., Giudice L.C. Regulation of insulin-like growth factor-binding protein 1 by hypoxia and 3',5'-cyclic adenosine monophosphate is additive in HepG2 cells. J. Clin. Endocrinol. Metab. 2000, 85:3821-3827.
52. Sun C.F., Tao Y., Jiang X.Y., Zou S.M. IGF binding protein 1 is correlated with hypoxia-induced growth reduce and developmental defects in grass carp (Ctenopharyngodon idellus) embryos. Gen. Comp. Endocrinol. 2011, 172:409-415.
53. Sutton K.M., Hayat S., Chau N.M., Cook S., Pouyssegur J., Ahmed A., Perusinghe N., Le Floch R., Yang J., Ashcroft M. Selective inhibition of MEK1/2 reveals a differential requirement for ERK1/2 signalling in the regulation of HIF-1 in response to hypoxia and IGF-1. Oncogene 2007, 26:3920-3929.
54. Tapanainen P.J., Bang P., Wilson K., Unterman T.G., Vreman H.J., Rosenfeld R.G. Maternal hypoxia as a model for intrauterine growth retardation: effects on insulin-like growth factors and their binding proteins. Pediatr. Res. 1994, 36:152-158.
55. Tazuke S.I., Mazure N.M., Sugawara J., Carland G., Faessen G.H., Suen L.F., Irwin J.C., Powell D.R., Giaccia A.J., Giudice L.C. Hypoxia stimulates insulin-like growth factor binding protein 1 (IGFBP-1) gene expression in HepG2 cells: a possible model for IGFBP-1 expression in fetal hypoxia. Proc. Natl. Acad. Sci. USA 1998, 95:10188-10193.
56. Wei D.B., Wei L., Zhang J.M., Yu H.Y. Blood-gas properties of plateau zokor (Myospalax baileyi). Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2006, 145:372-375.
57. Wheatcroft S.B., Kearney M.T. IGF-dependent and IGF-independent actions of IGF-binding protein-1 and -2: implications for metabolic homeostasis. Trends Endocrinol. Metab. 2009, 20:153-162.
58. Yamada N., Yanai R., Nakamura M., Inui M., Nishida T. Role of the C domain of IGFs in synergistic promotion, with a substance P-derived peptide, of rabbit corneal epithelial wound healing. Invest. Ophthalmol. Vis. Sci. 2004, 45:1125-1131.
59. Zhao Y., Wang M.Y., Hao K., Chen X.Q., Du J.Z. CRHR1 mediates p53 transcription induced by high altitude hypoxia through ERK 1/2 signaling in rat hepatic cells. Peptides 2013.
60. Zhou S., Gu L., He J., Zhang H., Zhou M. MDM2 regulates vascular endothelial growth factor mRNA stabilization in hypoxia. Mol. Cell. Biol. 2011, 31:4928-4937.