Enhanced cellular responses and distinct gene profiles in human fetoplacental artery endothelial cells under chronic low oxygen

Biology of Reproduction

Volumn 89, Issue 6, 2013, Pages

  Jiang, Yi Zhou ^a   Wang, Kai ^a,b   Li, Yan ^a   Dai, Cai Feng ^a,d   Wang, Ping ^a   Kendziorski, Christina ^a   Chen, Dong Bao ^c   Zheng, Jing ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b Shanghai First Maternity and Infant Health Hospital   (China)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d SHANDONG UNIVERSITY   (China)

Author keywords

Angiogenesis; Artery endothelial cells; Growth factors; Physiological chronic low oxygen; Transcriptome

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 3; FIBROBLAST GROWTH FACTOR RECEPTOR 4; HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1; OXYGEN; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

AMBIENT AIR; ARTICLE; CELL CULTURE; CELL FUNCTION; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; DOWN REGULATION; ENHANCED CELLULAR RESPONSE; ENZYME MECHANISM; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENETIC ANALYSIS; HUMAN; HUMAN CELL; HUMAN UMBILICAL ARTERY ENDOTHELIAL CELL; IN VIVO STUDY; MICROARRAY ANALYSIS; MICROVASCULAR ENDOTHELIAL CELL; PRIORITY JOURNAL; UMBILICAL ARTERY; UPREGULATION;

ANGIOGENESIS; ARTERY ENDOTHELIAL CELLS; GROWTH FACTORS; PHYSIOLOGICAL CHRONIC LOW OXYGEN; TRANSCRIPTOME;

CELL HYPOXIA; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL CELLS; FEMALE; HUMANS; MICROARRAY ANALYSIS; OXYGEN; PLACENTAL CIRCULATION; PREGNANCY; STRESS, PHYSIOLOGICAL; TIME FACTORS; TRANSCRIPTOME; UMBILICAL ARTERIES;

EID: 84897942378     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.110551     Document Type: Article

References (55)

1. Reynolds LP, Redmer DA. Angiogenesis in the placenta. Biol Reprod 2001; 64:1033-1040.
2. Benirschke K, Kaufmann P, Baergen BN. Anatomy and pathology of the umbilical cord. In: Benirschke K, Kaufmann P, Baergen BN (eds.), Pathology of the Human Placenta. 5th ed. New York: Springer; 2006:380-451.
3. Magness RR, Zheng J. Circulatory changes during gestation. In: Gluckman PD, Heymann MA (eds.), Pediatric and Perinatal Medicine: The Scientific Basis. London: Edward Arnold Publishers; 1996:762-772.
4. Osol G, Mandala M. Maternal uterine vascular remodeling during pregnancy. Physiology (Bethesda) 2009; 24:58-71.
5. Wang K, Zheng J. Signaling regulation of fetoplacental angiogenesis. J Endo 2012; 212:243-255.
6. Rodesch F, Simon P, Donner C, Jauniaux E. Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet Gynecol 1992; 80:283-285.
7. Wareing M, Greenwood SL, Baker PN. Reactivity of human placental chorionic plate vessels is modified by level of oxygenation: differences between arteries and veins. Placenta 2006; 27:42-48.
8. Zamudio S. High-altitude hypoxia and preeclampsia. Front Biosci 2007; 12:2967-2977.
9. Mayhew TM. Changes in fetal capillaries during preplacental hypoxia: growth, shape remodelling and villous capillarization in placentae from high-altitude pregnancies. Placenta 2003; 24:191-198.
10. Pugh CW, Ratcliffe PJ. Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 2003; 9:677-684.
11. Semenza GL. Hypoxia-inducible factors in physiology and medicine. Cell 2012; 148:399-408.
12. Burton GJ, Reshetnikova OS, Milovanov AP, Teleshova OV. Stereological evaluation of vascular adaptations in human placental villi to differing forms of hypoxic stress. Placenta 1996; 17:49-55.
13. Savransky V, Nanayakkara A, Li J, Bevans S, Smith PL, Rodriguez A, Polotsky VY. Chronic intermittent hypoxia induces atherosclerosis. Am J Respir Crit Care Med 2007; 175:1290-1297.
14. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003; 9:669-676.
15. Podar K, Anderson KC. The pathophysiologic role of VEGF in hematologic malignancies: therapeutic implications. Blood 2005; 105: 1383-1395.
16. Turner N, Grose R. Fibroblast growth factor signaling: from development to cancer. Nat Rev Cancer 2010; 10:116-129.
17. Humar R, Kiefer FN, Berns H, Resink TJ, Battegay EJ. Hypoxia enhances vascular cell proliferation and angiogenesis in vitro via rapamycin (mTOR)-dependent signaling. FASEB J 2002; 16:771-780.
18. Meininger CJ, Schelling ME, Granger HJ. Adenosine and hypoxia stimulate proliferation and migration of endothelial cells. Am J Physiol 1988; 255:H554-H562.
19. Phillips PG, Birnby LM, Narendran A. Hypoxia induces capillary network formation in cultured bovine pulmonary microvessel endothelial cells. Am J Physiol 1995; 268:L789-L800.
20. Wang K, Jiang YZ, Chen DB, Zheng J. Hypoxia enhances FGF2- and VEGFA-stimulated human placental artery endothelial cell proliferation: roles of MEK1/2/ERK1/2 and PI3K/AKT pathways. Placenta 2009; 30: 1045-1051.
21. Jiang YZ, Wang K, Li Y, Dai CF, Wang P, Kendziorski C, Chen DB, Zheng J. Transcriptional and functional adaptations of endothelial cells to physiological chronic low oxygen. Biol Reprod 2013; 88:114.
22. Chi JT, Chang HY, Haraldsen G, Jahnsen FL, Troyanskaya OG, Chang DS, Wang Z, Rockson SG, van de Rijn M, Botstein D, Brown PO. Endothelial cell diversity revealed by global expression profiling. Proc Natl Acad Sci U S A 2003; 100:10623-10628.
23. Aitsebaomo J, Portbury AL, Schisler JC, Patterson C. Brothers and sisters: molecular insights into arterial-venous heterogeneity. Circ Res 2008; 103: 929-939.
24. Rocha SF, Adams RH. Molecular differentiation and specialization of vascular beds. Angiogenesis 2009; 12:139-147.
25. Lang I, Pabst MA, Hiden U, Blaschitz A, Dohr G, Hahn T, Desoye G. Heterogeneity of microvascular endothelial cells isolated from human term placenta and macrovascular umbilical vein endothelial cells. Eur J Cell Biol 2003; 82:163-173.
26. Min J, Jin YM, Moon JS, Sung MS, Jo SA, Jo I. Hypoxia-induced endothelial NO synthase gene transcriptional activation is mediated through the tax-responsive element in endothelial cells. Hypertension 2006; 47:1189-1196.
27. Olszewska-Pazdrak B, Hein TW, Olszewska P, Carney DH. Chronic hypoxia attenuates VEGF signaling and angiogenic responses by downregulation of KDR in human endothelial cells. Am J Physiol Cell Physiol 2009; 296:C1162-C1170.
28. Matsuo K, Malinow AM, Harman CR, Baschat AA. Decreased placental oxygenation capacity in pre-eclampsia: clinical application of a novel index of placental function preformed at the time of delivery. J Perinat Med 2009; 37:657-661.
29. Jobe SO, Ramadoss J, Koch JM, Jiang YZ, Zheng J, Magness RR. Estradiol-17b and its cytochrome P450- and catechol-O-methyltransferase- derived metabolites stimulate proliferation in uterine artery endothelial cells: role of estrogen receptor-alpha versus estrogen receptor-beta. Hypertension 2010; 55:1005-1011.
30. Dai DF, Jiang YZ, Li Y, Wang K, Liu PS, Patankar MS, Zheng J. Expression and roles of the Slit/Robo in human ovarian cancer. Histochem Cell Biol 2011; 135:475-485.
31. Hill DJ, Tevaarwerk GJ, Arany E, Kilkenny D, Gregory M, Langford KS, Miell J. Fibroblast growth factor-2 (FGF-2) is present in maternal and cord serum, and in the mother is associated with a binding protein immunologically related to the FGF receptor-1. J Clin Endocrinol Metab 1995; 80:1822-1831.
32. Baker PN, Krasnow J, Roberts JM, Yeo KT. Elevated serum levels of vascular endothelial growth factor in patients with preeclampsia. Obstet Gynecol 1995; 86:815-821.
33. Galazios G, Papazoglou D, Giagloglou K, Vassaras G, Koutlaki N, Maltezos E. Umbilical cord serum vascular endothelial growth factor (VEGF) levels in normal pregnancies and in pregnancies complicated by preterm delivery or pre-eclampsia. Int J Gynaecol Obstet 2004; 85:6-11.
34. Wallner W, Sengenberger R, Strick R, Strissel PL, Meurer B, Beckmann MW, Schlembach D. Angiogenic growth factors in maternal and fetal serum in pregnancies complicated by intrauterine growth restriction. Clin Sci (Lond) 2007; 112:51-57.
35. Jelkmann W. Pitfalls in the measurement of circulating vascular endothelial growth factor. Clin Chem 2001; 47:617-623.
36. Chung JY, Song Y, Wang Y, Magness RR, Zheng J. Differential expression of vascular endothelial growth factor (VEGF), endocrine gland derived-VEGF, and VEGF receptors in human placentas from normal and preeclamptic pregnancies. J Clin Endocrinol Metab 2004; 89:2484-2490.
37. Newton MA, Kendziorski CM. Parametric empirical Bayes methods for microarrays. In: Parmigiani G, Garrett ES, Irizarry R, Zeger SL (eds.), The Analysis of Gene Expression Data: Methods and Software. New York: Springer Verlag; 2003:254-271.
38. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J. TM4 microarray software suite. Methods Enzymol 2006; 411:134-193.
39. Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol Lett 2004; 26:509-515.
40. Pfaffl MW, HorganGW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002; 30:e36.
41. de Sousa Abreu R, Penalva LO, Marcotte EM, Vogel C. Global signatures of protein and mRNA expression levels. Mol Biosyst 2009; 5:1512-1526.
42. Rajakumar A, Conrad KP. Expression, ontogeny, and regulation of hypoxia-inducible transcription factors in the human placenta. Biol Reprod 2000; 63:559-569.
43. Rajakumar A, Whitelock KA, Weissfeld LA, Daftary AR, Markovic N, Conrad KP. Selective overexpression of the hypoxia-inducible transcription factor, HIF-2a, in placentas from women with preeclampsia. Biol Reprod 2001; 64:499-506.
44. Rajakumar A, Whitelock KA, Weissfeld LA, Daftary AR, Markovic N, Conrad KP. Selective overexpression of the hypoxia-inducible transcription factors in placentas from women with preeclampsia [Erratum]. Biol Reprod 2001; 64:1019-1020.
45. Atkuri KR, Herzenberg LA, Herzenberg LA. Culturing at atmospheric oxygen levels impacts lymphocyte function. Proc Natl Acad Sci U S A 2005; 102:3756-3759.
46. Atkuri KR, Herzenberg LA, Niemi AK, Cowan T, Herzenberg LA. Importance of culturing primary lymphocytes at physiological oxygen levels. Proc Natl Acad Sci U S A 2007; 104:4547-4552.
47. Lengner CJ, Gimelbrant AA, Erwin JA, Cheng AW, Guenther MG, Welstead GG, Alagappan R, Frampton GM, Xu P, Muffat J, Santagata S, Powers D, et al. Derivation of pre-X inactivation human embryonic stem cells under physiological oxygen concentrations. Cell 2010; 141:872-883.
48. Li TS, Cheng K, Malliaras K, Matsushita N, Sun B, Marbán L, Zhang Y, Marbán E. Expansion of human cardiac stem cells in physiological oxygen improves cell production efficiency and potency for myocardial repair. Cardiovas Res 2011; 89:157-165.
49. Hatipoglu OF, Hirohata S, Cilek MZ, Ogawa H, Miyoshi T, Obika M, Demircan K, Shinohata R, Kusachi S, Ninomiya Y. ADAMTS1 is a unique hypoxic early response gene expressed by endothelial cells. J Biol Chem 2009; 284:16325-16333.
50. Liu ZJ, Xiao M, Balint K, Soma A, Pinnix CC, Capobianco AJ, Velazquez OC, Herlyn M. Inhibition of endothelial cell proliferation by Notch1 signaling is mediated by repressing MAPK and PI3K/Akt pathways and requires MAML1. FASEB J 2006; 20:1009-1011.
51. Manalo DJ, Rowan A, Lavoie T, Natarajan L, Kelly BD, Ye SQ, Garcia JG, Semenza GL. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 2005; 105:659-669.
52. Webb JD, Coleman ML, Pugh CW. Hypoxia, hypoxia-inducible factors (HIF), HIF hydroxylases and oxygen sensing. Cell Mol Life Sci 2009; 66: 3539-3554.
53. Mense SM, Sengupta A, Zhou M, Lan C, Bentsman G, Volsky DJ, Zhang L. Gene expression profiling reveals the profound upregulation of hypoxia-responsive genes in primary human astrocytes. Physiol Genomics 2006; 25:435-449.
54. Fish JE, Yan MS, Matouk CC, St Bernard R, Ho JJ, Gavryushova A, Srivastava D, Marsden PA. Hypoxic repression of endothelial nitric-oxide synthase transcription is coupled with eviction of promoter histones. J Biol Chem 2010; 285:810-826.
55. Crosby ME, Devlin CM, Glazer PM, Calin GA, Ivan M. Emerging roles of microRNAs in the molecular responses to hypoxia. Curr Pharm Des 2009; 15:3861-3866.