Maternal protein restriction alters VEGF signaling and decreases pulmonary alveolar in fetal rats

International Journal of Clinical and Experimental Pathology

Volumn 7, Issue 6, 2014, Pages 3101-3111

  Liu, Xiaomei ^a   Lin, Yan ^a   Tian, Baoling ^a   Miao, Jianing ^a   Xi, Chunyan ^a   Liu, Caixia ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

Author keywords

IUGR; miRNA; Placenta; Pulmonary; VEGF

Indexed keywords

VASCULAR ENDOTHELIAL GROWTH FACTOR A, RAT; VASCULOTROPIN A;

ANIMAL; DISEASE MODEL; EMBRYOLOGY; FEMALE; FETAL MALNUTRITION; FETUS; IMMUNOBLOTTING; INTRAUTERINE GROWTH RETARDATION; LUNG; LUNG ALVEOLUS; METABOLISM; PATHOLOGY; PREGNANCY; PRENATAL EXPOSURE; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VASCULARIZATION; WISTAR RAT;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; FETAL GROWTH RETARDATION; FETAL NUTRITION DISORDERS; FETUS; IMMUNOBLOTTING; LUNG; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PULMONARY ALVEOLI; RATS; RATS, WISTAR; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84904291687     PISSN: None     EISSN: 19362625     Source Type: Journal    
DOI: None     Document Type: Article

References (62)

1. Gagnon R. Placental insufficiency and its consequences. Eur J Obstet Gynecol Reprod Biol 2003; 110 Suppl 1: S99-107.
2. Pryor J. The identification and long term effects of fetal growth restriction. Br J Obstet Gynaecol 1997; 104: 1116-1122.
3. Barker D, Eriksson J, Forsn T and Osmond C. Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol 2002; 31: 1235-1239.
4. Londhe VA, Maisonet TM, Lopez B, Shin BC, Huynh J and Devaskar SU. Retinoic acid rescues alveolar hypoplasia in the calorie-restrict ed developing rat lung. Am J Respir Cell Mol Biol 2013; 48: 179-187.
5. Aucott SW, Donohue PK and Northington FJ. Increased morbidity in severe early intrauterine growth restriction. J Perinatol 2004; 24: 435-440.
6. Bose C, Van Marter LJ, Laughon M, O'Shea TM, Allred EN, Karna P, Ehrenkranz RA, Boggess K and Leviton A. Fetal growth restriction and chronic lung disease among infants born before the 28th week of gestation. Pediatrics 2009; 124: e450-458.
7. Dezateux C, Lum S, Hoo AF, Hawdon J, Costeloe K and Stocks J. Low birth weight for gestation and airway function in infancy: exploring the fetal origins hypothesis. Thorax 2004; 59: 60-66.
8. Gortner L, Misselwitz B, Milligan D, Zeitlin J, Kollee L, Boerch K, Agostino R, Van Reempts P, Chabernaud JL, Breart G, Papiernik E, Jarreau PH, Carrapato M, Gadzinowski J and Draper E. Rates of bronchopulmonary dysplasia in very preterm neonates in Europe: results from the MOSAIC cohort. Neonatology 2011; 99: 112-117.
9. Lal MK, Manktelow BN, Draper ES and Field DJ. Chronic lung disease of prematurity and intrauterine growth retardation: a population-based study. Pediatrics 2003; 111: 483-487.
10. McIntire DD, Bloom SL, Casey BM and Leveno KJ. Birth Weight in Relation to Morbidity and Mortality among Newborn Infants. New Engl J Med 1999; 340: 1234-1238.
11. Minior VK and Divon MY. Fetal growth restriction at term: myth or reality? Obstet Gynecol 1998; 92: 57-60.
12. Kotecha SJ, Watkins WJ, Heron J, Henderson J, Dunstan FD and Kotecha S. Spirometric lung function in school-age children: effect of intrauterine growth retardation and catch-up growth. Am J Respir Crit Care Med 2010; 181: 969-974.
13. Burri PH. Structural aspects of postnatal lung development-alveolar formation and growth. Biol Neonate 2006; 89: 313-322.
14. Chen CM, Wang LF and Su B. Effects of maternal undernutrition during late gestation on the lung surfactant system and morphometry in rats. Pediatr Res 2004; 56: 329-335.
15. Cock ML, Albuquerque CA, Joyce BJ, Hooper SB and Harding R. Effects of intrauterine growth restriction on lung liquid dynamics and lung development in fetal sheep. Am J Obstet Gynecol 2001; 184: 209-216.
16. Lin Y and Lechner AJ. Surfactant content and type II cell development in fetal guinea pig lungs during prenatal starvation. Pediatr Res 1991; 29: 288-291.
17. Maritz GS, Cock ML, Louey S, Suzuki K and Harding R. Fetal growth restriction has long-term effects on postnatal lung structure in sheep. Pediatr Res 2004; 55: 287-295.
18. Rozance PJ, Seedorf GJ, Brown A, Roe G, O'Meara MC, Gien J, Tang JR and Abman SH. Intrauterine growth restriction decreases pulmonary alveolar and vessel growth and causes pulmonary artery endothelial cell dysfunction in vitro in fetal sheep. Am J Physiol Lung Cell Mol Physiol 2011; 301: L860-871.
19. Shima DT, Kuroki M, Deutsch U, Ng YS, Adamis AP and D'Amore PA. The mouse gene for vascular endothelial growth factor. Genomic structure, definition of the transcriptional unit, and characterization of transcriptional and post-transcriptional regulatory sequences. J Biol Chem 1996; 271: 3877-3883.
20. Keyt BA, Berleau LT, Nguyen HV, Chen H, Heinsohn H, Vandlen R and Ferrara N. The carboxyl-terminal domain (111-165) of vascular endothelial growth factor is critical for its mitogenic potency. J Biol Chem 1996; 271: 7788-7795.
21. Voelkel NF, Vandivier RW and Tuder RM. Vascular endothelial growth factor in the lung. Am J Physiol Lung Cell Mol Physiol 2006; 290: L209-221.
22. Compernolle V, Brusselmans K, Acker T, Hoet P, Tjwa M, Beck H, Plaisance S, Dor Y, Keshet E, Lupu F, Nemery B, Dewerchin M, Van Veldhoven P, Plate K, Moons L, Collen D and Carmeliet P. Loss of HIF-2alpha and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat Med 2002; 8: 702-710.
23. Fong GH, Rossant J, Gertsenstein M and Breitman ML. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 1995; 376: 66-70.
24. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML and Schuh AC. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 1995; 376: 62-66.
25. Kasahara Y, Tuder RM, Taraseviciene-Stewart L, Le Cras TD, Abman S, Hirth PK, Waltenberger J and Voelkel NF. Inhibition of VEGF receptors causes lung cell apoptosis and emphysema. J Clin Invest 2000; 106: 1311-1319.
26. Le Cras TD, Markham NE, Tuder RM, Voelkel NF and Abman SH. Treatment of newborn rats with a VEGF receptor inhibitor causes pulmonary hypertension and abnormal lung structure. Am J Physiol Lung Cell Mol Physiol 2002; 283: L555-562.
27. Raoul W, Chailley-Heu B, Barlier-Mur AM, Delacourt C, Maitre B and Bourbon JR. Effects of vascular endothelial growth factor on isolated fetal alveolar type II cells. Am J Physiol Lung Cell Mol Physiol 2004; 286: L1293-1301.
28. Inui M, Martello G and Piccolo S. MicroRNA control of signal transduction. Nat Rev Mol Cell Biol 2010; 11: 252-263.
29. Small EM, O'Rourke JR, Moresi V, Sutherland LB, McAnally J, Gerard RD, Richardson JA and Olson EN. Regulation of PI3-kinase/Akt signaling by muscle-enriched microRNA-486. Proc Natl Acad Sci U S A 2010; 107: 4218-4223.
30. Wurdinger T, Tannous BA, Saydam O, Skog J, Grau S, Soutschek J, Weissleder R, Breakefield XO and Krichevsky AM. miR-296 regulates growth factor receptor overexpression in angiogenic endothelial cells. Cancer Cell 2008; 14: 382-393.
31. Alvarez-Garcia I and Miska EA. MicroRNA functions in animal development and human disease. Development 2005; 132: 4653-4662.
32. Dong J, Jiang G, Asmann YW, Tomaszek S, Jen J, Kislinger T and Wigle DA. MicroRNA networks in mouse lung organogenesis. PLoS One 2010; 5: e10854.
33. Mujahid S, Logvinenko T, Volpe MV and Nielsen HC. miRNA regulated pathways in late stage murine lung development. BMC Dev Biol 2013; 13: 13.
34. Zhu X, Li H, Long L, Hui L, Chen H, Wang X, Shen H and Xu W. miR-126 enhances the sensitivity of non-small cell lung cancer cells to anticancer agents by targeting vascular endothelial growth factor A. Acta Biochim Biophys Sin (Shanghai) 2012; 44: 519-526.
35. Chamorro-Jorganes A, Araldi E, Penalva LO, Sandhu D, Fernandez-Hernando C and Suarez Y. MicroRNA-16 and microRNA-424 regulate cell-autonomous angiogenic functions in endothelial cells via targeting vascular endothelial growth factor receptor-2 and fibroblast growth factor receptor-1. Arterioscler Thromb Vasc Biol 2011; 31: 2595-2606.
36. Goyal R, Leitzke A, Goyal D, Gheorghe CP and Longo LD. Antenatal maternal hypoxic stress: adaptations in fetal lung Renin-Angiotensin system. Reprod Sci 2011; 18: 180-189.
37. Hromadnikova I, Kotlabova K, Doucha J, Dlouha K and Krofta L. Absolute and relative quantification of placenta-specific micrornas in maternal circulation with placental insuffici- ency-related complications. J Mol Diagn 2012; 14: 160-167.
38. Liu X, Qi Y, Gao H, Jiao Y, Gu H, Miao J and Yuan Z. Maternal protein restriction induces alterations in insulin signaling and ATP sensitive potassium channel protein in hypothalami of intrauterine growth restriction fetal rats. J Clin Biochem Nutr 2013; 52: 43-48.
39. Livak KJ and Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-??Ct method. Methods 2001; 25: 402-408.
40. Bhaskaran M, Wang Y, Zhang H, Weng T, Baviskar P, Guo Y, Gou D and Liu L. MicroRNA-127 modulates fetal lung development. Physiol Genomics 2009; 37: 268-278.
41. Burri PH. Fetal and postnatal development of the lung. Annu Rev Physiol 1984; 46: 617-628.
42. Zoetis T and Hurtt ME. Species comparison of lung development. Birth Defects Res B Dev Reprod Toxicol 2003; 68: 121-124.
43. Weng T, Chen Z, Jin N, Gao L and Liu L. Gene expression profiling identifies regulatory pathways involved in the late stage of rat fetal lung development. Am J Physiol Lung Cell Mol Physiol 2006; 291: L1027-1037.
44. Leung DW, Cachianes G, Kuang WJ, Goeddel DV and Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 1989; 246: 1306-1309.
45. Yoshida A, Anand-Apte B and Zetter BR. Differential endothelial migration and proliferation to basic fibroblast growth factor and vascular endothelial growth factor. Growth Factors 1996; 13: 57-64.
46. Gille H, Kowalski J, Li B, LeCouter J, Moffat B, Zioncheck TF, Pelletier N and Ferrara N. Analysis of biological effects and signaling properties of Flt-1 (VEGFR-1) and KDR (VEGFR-2) A reassessment using novel receptor-specific vascular endothelial growth factor mutants. J Biol Chem 2001; 276: 3222-3230.
47. Gerber HP, Hillan KJ, Ryan AM, Kowalski J, Keller GA, Rangell L, Wright BD, Radtke F, Aguet M and Ferrara N. VEGF is required for growth and survival in neonatal mice. Development 1999; 126: 1149-1159.
48. Grover TR, Parker TA and Abman SH. Vascular endothelial growth factor improves pulmonary vascular reactivity and structure in an experimental model of chronic pulmonary hypertension in fetal sheep. Chest 2005; 128: 614S.
49. Jakkula M, Le Cras TD, Gebb S, Hirth KP, Tuder RM, Voelkel NF and Abman SH. Inhibition of angiogenesis decreases alveolarization in the developing rat lung. Am J Physiol Lung Cell Mol Physiol 2000; 279: L600-607.
50. Del Moral PM, Sala FG, Tefft D, Shi W, Keshet E, Bellusci S and Warburton D. VEGF-A signaling through Flk-1 is a critical facilitator of early embryonic lung epithelial to endothelial crosstalk and branching morphogenesis. Dev Biol 2006; 290: 177-188.
51. Lai EC. Micro RNAs are complementary to 3' UTR sequence motifs that mediate negative post-transcriptional regulation. Nat Genet 2002; 30: 363-364.
52. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR and Ruvkun G. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000; 403: 901-906.
53. Xiao C, Calado DP, Galler G, Thai TH, Patterson HC, Wang J, Rajewsky N, Bender TP and Rajewsky K. MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell 2007; 131: 146-159.
54. Cheng AM, Byrom MW, Shelton J and Ford LP. Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res 2005; 33: 1290-1297.
55. Ambros V. The functions of animal microRNAs. Nature 2004; 431: 350-355.
56. Harris KS, Zhang Z, McManus MT, Harfe BD and Sun X. Dicer function is essential for lung epithelium morphogenesis. Proc Natl Acad Sci U S A 2006; 103: 2208-2213.
57. Hua Z, Lv Q, Ye W, Wong CK, Cai G, Gu D, Ji Y, Zhao C, Wang J, Yang BB and Zhang Y. MiRNA-directed regulation of VEGF and other angiogenic factors under hypoxia. PLoS One 2006; 1: e116.
58. Khaliq A, Dunk C, Jiang J, Shams M, Li XF, Acevedo C, Weich H, Whittle M and Ahmed A. Hypoxia down-regulates placenta growth factor, whereas fetal growth restriction up-regulates placenta growth factor expression: molecular evidence for "placental hyperoxia" in intrauterine growth restriction. Lab Invest 1999; 79: 151-170.
59. Kingdom JC and Kaufmann P. Oxygen and placental villous development: origins of fetal hypoxia. Placenta 1997; 18: 613-621; discussion 623-616.
60. Kumazaki K, Nakayama M, Suehara N and Wada Y. Expression of vascular endothelial growth factor, placental growth factor, and their receptors Flt-1 and KDR in human placenta under pathologic conditions. Hum Pathol 2002; 33: 1069-1077.
61. Szentpéteri I, Rab A, Kornya L, Kovács P, Joó JG. Gene expression patterns of vascular endothelial growth factor (VEGF-A) in human placenta from pregnancies with intrauterine growth restriction. J Maternal-Fetal Neonatal Med 2013; 26: 984-989.
62. Regnault TR, de Vrijer B, Galan HL, Davidsen ML, Trembler KA, Battaglia FC, Wilkening RB and Anthony RV. The relationship between transplacental O2 diffusion and placental expression of PlGF, VEGF and their receptors in a placental insufficiency model of fetal growth restriction. J Physiol 2003; 550: 641-656.