Inhibition of peroxisome proliferator-activated receptor γ: A potential link between chronic maternal hypoxia and impaired fetal growth

FASEB Journal

Volumn 28, Issue 3, 2014, Pages 1268-1279

  Julian, Colleen G ^a   Yang, Ivana V ^b   Browne, Vaughn A ^c   Vargas, Enrique ^d   Rodriguez, Carmelo ^e   Pedersen, Brent S ^b   Moore, Lorna G ^b   Schwartz, David A ^b  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^d Bolivian Institute of High Altitude Biology   (Bolivia)

^e Clinica Sirani   (Bolivia)

Author keywords

Intrauterine growth restriction; PPAR

Indexed keywords

GLUCOSE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA;

ADULT; ALTITUDE; ARTICLE; BIRTH WEIGHT; CHRONIC MATERNAL HYPOXIA; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DELIVERY; FEMALE; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; HEAD CIRCUMFERENCE; HUMAN; HUMAN CELL; HYPOXIA; IMPAIRED FETAL GROWTH; INTRAUTERINE GROWTH RETARDATION; LONG TERM EXPOSURE; MOLECULAR PATHOLOGY; PERIPHERAL BLOOD MONONUCLEAR CELL; PREGNANCY; PRIORITY JOURNAL; RESIDENT; SEA LEVEL; ANOXIA; CHRONIC DISEASE; DRUG ANTAGONISM; INTRAUTERINE GROWTH RESTRICTION; NEWBORN; PATHOPHYSIOLOGY; PPARΓ; PREGNANCY COMPLICATION; VALIDATION STUDY; YOUNG ADULT;

INTRAUTERINE GROWTH RESTRICTION; PPARΓ;

ADULT; ANOXIA; CHRONIC DISEASE; FEMALE; FETAL GROWTH RETARDATION; HUMANS; INFANT, NEWBORN; PPAR GAMMA; PREGNANCY; PREGNANCY COMPLICATIONS; YOUNG ADULT;

EID: 84899572589     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-239749     Document Type: Article

References (59)

1. Julian, C. G., Vargas, E., Armaza, J. F., Wilson, M. J., Niermeyer, S., Villena, M., and Moore, L. G. (2007) High-Altitude ancestry protects against hypoxia-Associated reductions in fetal growth. Arch. Dis. Child Fetal Neonatal Ed. 92, F372-F377
2. Palmer, S. K., Moore, L. G., Young, D. A., Cregger, B., Berman, J. C., and Zamudio, S. (1999) Altered blood pressure course during normal pregnancy and increased preeclampsia at high altitude (3100 meters) in Colorado. Am. J. Obstet. Gynecol. 180, 1161-1168
3. Krampl, E., Espinoza-Dorado, J., Lees, C. C., Moscoso, G., and Bland, J. M. (2001) Maternal uterine artery Doppler studies at high altitude and sea level. Ultrasound Obstet. Gynecol. 18, 578-582
4. Krampl, E., Lees, C., Bland, J. M., Dorado, J. E., Gonzalo, M., and Campbell, S. (2000) Fetal biometry at 4300 m compared with sea level in Peru. Ultrasound Obstet. Gynecol. 16, 9-18
5. Moore, L., Shriver, M., Bemis, L., Hickler, B., Wilson, M., Brutsaert, T., Parra, E., and Vargas, E. (2004) Maternal adaptation to high-Altitude pregnancy: an experiment of nature. Placenta 25(Suppl.), S60-S71
6. Keyes, L. E., Armaza, J. F., Niermeyer, S., Vargas, E., Young, D., Villena, M., and Moore, L. G. (2003) Intrauterine growth restriction, preeclampsia and intrauterine mortality at high altitude in Bolivia. Pediatr. Res. 54, 20-25
7. Villar, K., Say, L., G? ulmenzoglu, A. M., Merialdi, M., Lindheimer, M. D., Betran, A. P., and Piaggio, G. (2003) Eclampsia and pre-eclampsia: a health problem for 2000 years. In Preeclampsia (Critchley, H. M. A., Poston, L., and Walker, J. J., eds) pp. 189-207, RCOG Press, London, UK
8. Walker, J. J. (2000) Pre-eclampsia. Lancet 356, 1260-1265
9. Gilbert, W., and Danielsen, B. (2003) Pregnancy outcomes associated with intrauterine growth restriction. Am. J. Obstet. Gynecol. 188, 1596-1599; discussion 1599-1601
10. Caniggia, I., and Winter, J. L. (2002) Hypoxia inducible factor-1: oxygen regulation of trophoblast differentiation in normal and pre-eclamptic pregnancies-A review. Placenta 23, S47-S57
11. Wheaton, W. W., and Chandel, N. S. (2011) Hypoxia. 2. Hypoxia regulates cellular metabolism. Am. J. Physiol. Cell Physiol. 300, C385-C393
12. Semenza, G. L. (2007) Life with oxygen. Science 318, 62-64
13. Arngrimsson, R., Hayward, C., Nadaud, S., Baldursdottir, A., Walker, J. J., Liston, W. A., Bjarnadottir, R. I., Brock, D. J. H., Geirsson, R. T., Connor, J. M., and Soubrier, F. (1997) Evidence for a familial pregnancy-induced hypertension locus in the eNOS-gene region. Am. J. Hum. Genet. 61, 354-362
14. Savvidou, M. D., Valance, P. J. T., Nicolaides, K. H., and Hingorani, A. D. (2001) Endothelial nitric oxide synthase gene polymorphism and maternal vascular adaptation to pregnancy. Hypertension 38, 1289-1293
15. Davila, R. D., Julian, C. G., Wilson, M. J., Browne, V. A., Rodriguez, C., Bigham, A. W., Shriver, M. D., Vargas, E., and Moore, L. G. (2010) Do cytokines contribute to the Andeanassociated protection from reduced fetal growth at high altitude? Reprod. Sci. 18, 79-87
16. Davila, R. D., Julian, C. G., Wilson, M. J., Browne, V. A., Rodriguez, C., Bigham, A. W., Shriver, M. D., Vargas, E., and Moore, L. G. (2010) Do anti-Angiogenic or angiogenic factors contribute to the protection of birth weight at high altitude afforded by Andean ancestry? Reprod. Sci. 17, 861-870
17. Julian, C. G., Galan, H. L., Wilson, M. J., Desilva, W., Cioffi-Ragan, D., Schwartz, J., and Moore, L. G. (2008) Lower uterine artery blood flow and higher endothelin relative to nitric oxide metabolite levels are associated with reductions in birth weight at high altitude. Am. J. Physiol. 295, R906-R915
18. Zamudio, S., Baumann, M. U., and Illsley, N. P. (2006) Effects of chronic hypoxia in vivo on the expression of human placental glucose transporters. Placenta 27, 49-55
19. Zamudio, S., Wu, Y., Ietta, F., Rolfo, A., Cross, A., Wheeler, T., Post, M., Illsley, N. P., and Caniggia, I. (2007) Human placental hypoxia-inducible factor-1alpha expression correlates with clinical outcomes in chronic hypoxia in vivo. Am. J. Pathol. 170, 2171-2179
20. Baumann, M. U., Zamudio, S., and Illsley, N. P. (2007) Hypoxic upregulation of glucose transporters in BeWo choriocarcinoma cells is mediated by hypoxia-inducible factor-1. Am. J. Physiol. Cell Physiol. 293, C477-C485
21. Bigham, A. W., Wilson, M. J., Browne, V. A., Julian, C. G., Vargas, E., Rodriquez, C., Shriver, M. D., and Moore, L. G. (2012) Maternal genetic variation near PRKAA1 and EDNRA is associated with birth weight among residents of high altitude. Abstract 3290, American Society of Human Genetics Annual Meeting, San Francisco, CA, USA
22. Escher, P., and Wahli, W. (2000) Peroxisome proliferatoractivated receptors: insight into multiple cellular functions. Mutat. Res. 448, 121-138
23. McCarthy, F. P., Delany, A. C., Kenny, L. C., and Walsh, S. K. (2013) PPAR-gamma-A possible drug target for complicated pregnancies. Br. J. Pharmacol. 168, 1074-1085
24. Bigham, A., Bauchet, M., Pinto, D., Mao, X., Akey, J. M., Mei, R., Scherer, S. W., Julian, C. G., Wilson, M. J., Lopez Herraez, D., Brutsaert, T., Parra, E. J., Moore, L. G., and Shriver, M. D. (2010) Identifying signatures of natural selection in tibetan and andean populations using dense genome scan data. PLoS Genet. 6
25. Julian, C. G., Wilson, M. J., Lopez, M., Yamashiro, H., Tellez, W., Rodriguez, A., Bigham, A. W., Shriver, M. D., Rodriguez, C., Vargas, E., and Moore, L. G. (2009) Augmented uterine artery blood flow and oxygen delivery protect Andeans from altitudeassociated reductions in fetal growth. Am. J. Physiol. 296, R1564-1575
26. Shriver, M. D., Mei, R., Parra, E. J., Sonpar, V., Halder, I., Tishkoff, S. A., Schurr, T. G., Zhadanov, S. I., Osipova, L. P., Brutsaert, T. D., Friedlaender, J., Jorde, L. B., Watkins, G., Fernandez, J. R., Akey, J. M., and Jones, K. W. (2005) Large-scale SNP analysis reveals clustered and continuous patterns of human genetic variation. Hum. Genomics 2, 81-89
27. Witter, F. R., and Luke, B. (1991) The effect of maternal height on birth weight and birth length. Early Hum. Dev. 25, 181-186
28. Oken, E., Kleinman, K. P., Rich-Edwards, J., and Gillman, M. W. (2003) A nearly continuous measure of birth weight for gestational age using a United States national reference. BMC Pediatrics 3, 6
29. Irizarry, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U., and Speed, T. P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264
30. Leek, J. T., Johnson, W. E., Parker, H. S., Jaffe, A. E., and Storey, J. D. (2012) The sva package for removing batch effects and other unwanted variation in high-Throughput experiments. Bioinformatics 28, 882-883
31. Smyth, G. K. (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article 3
32. Benjamini, Y., and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Royal Stat. Soc. Series B 57, 289-300
33. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-Time quantitative PCR and the 2[-delta delta C(T)] method. Methods 25, 402-408
34. Weix, J., Forger, F., Haupl, T., Surbek, D., Ostensen, M., and Villiger, P. M. (2012) Influence of pregnancy on the adipocytokine and peroxisome proliferator-Activated receptor pathways in peripheral blood mononuclear cells from healthy donors and rheumatoid arthritis patients. Arthritis Rheum. 64, 2095-2103
35. Bull, T. M., Coldren, C. D., Geraci, M. W., and Voelkel, N. F. (2007) Gene expression profiling in pulmonary hypertension. Proc. Am. Thorac. Soc. 4, 117-120
36. Capeless, E., and Clapp, J. (1991) When do cardiovascular parameters return to their preconception values? Am. J. Obstet. Gynecol. 165, 883-886
37. Parast, M. M., Yu, H., Ciric, A., Salata, M. W., Davis, V., and Milstone, D. S. (2009) PPARgamma regulates trophoblast proliferation and promotes labyrinthine trilineage differentiation. PLoS One 4, e8055
38. Ricote, M., Li, A. C., Willson, T. M., Kelly, C. J., and Glass, C. K. (1998) The peroxisome proliferator-Activated receptor-gamma is a negative regulator of macrophage activation. Nature 391, 79-82
39. Jozkowicz, A., Dulak, J., Piatkowska, E., Placha, W., and Dembinska-Kiec, A. (2000) Ligands of peroxisome proliferatoractivated receptor-gamma increase the generation of vascular endothelial growth factor in vascular smooth muscle cells and in macrophages. Acta Biochim. Pol. 47, 1147-1157
40. Li, X., Kimura, H., Hirota, K., Sugimoto, H., Kimura, N., Takahashi, N., Fujii, H., and Yoshida, H. (2007) Hypoxia reduces the expression and anti-inflammatory effects of peroxisome proliferator-Activated receptor-gamma in human proximal renal tubular cells. Nephrol. Dial. Transplant. 22, 1041-1051
41. McCarthy, F. P., Drewlo, S., English, F. A., Kingdom, J., Johns, E. J., Kenny, L. C., and Walsh, S. K. (2011) Evidence implicating peroxisome proliferator-Activated receptor-gamma in the pathogenesis of preeclampsia. Hypertension 58, 882-887
42. McCarthy, F. P., Drewlo, S., Kingdom, J., Johns, E. J., Walsh, S. K., and Kenny, L. C. (2011) Peroxisome proliferator-Activated receptor-gamma as a potential therapeutic target in the treatment of preeclampsia. Hypertension 58, 280-286
43. Diaz, M., Bassols, J., Lopez-Bermejo, A., Gomez-Roig, M. D., de Zegher, F., and Ibanez, L. (2012) Placental expression of peroxisome proliferator-Activated receptor gamma (PPARgamma): relation to placental and fetal growth. J. Clin. Endocrinol. Metab. 97, E1468-1472
44. Waite, L. L., Louie, R. E., and Taylor, R. N. (2005) Circulating activators of peroxisome proliferator-Activated receptors are reduced in preeclamptic pregnancy. J. Clin. Endocrinol. Metab. 90, 620-626
45. Rodie, V. A., Young, A., Jordan, F., Sattar, N., Greer, I. A., and Freeman, D. J. (2005) Human placental peroxisome proliferator-Activated receptor delta and gamma expression in healthy pregnancy and in preeclampsia and intrauterine growth restriction. J. Soc. Gynecol. Investig. 12, 320-329
46. Holdsworth-Carson, S. J., Lim, R., Mitton, A., Whitehead, C., Rice, G. E., Permezel, M., and Lappas, M. (2010) Peroxisome proliferator-Activated receptors are altered in pathologies of the human placenta: gestational diabetes mellitus, intrauterine growth restriction and preeclampsia. Placenta 31, 222-229
47. Schaiff, W. T., Carlson, M. G., Smith, S. D., Levy, R., Nelson, D. M., and Sadovsky, Y. (2000) Peroxisome proliferator-Activated receptor-gamma modulates differentiation of human trophoblast in a ligand-specific manner. J. Clin. Endocrinol. Metab. 85, 3874-3881
48. Pijnenborg, R., Dixon, G., Robertson, W. B., and Brosens, I. (1980) Trophoblastic invasion of human decidua from 8 to 18 weeks of pregnancy. Placenta 1, 3-19
49. Khong, T. Y., De Wolf, F., Robertson, W. B., and Brosens, I. (1986) Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-forgestational age infants. Br. J. Obstet. Gynaecol. 93, 1049-1059
50. Tissot Van Patot, M., Grilli, A., Chapman, P., Broad, E., Tyson, W., Heller, D. S., Zwerdlinger, L., and Zamudio, S. (2003) Remodeling of uteroplacental arteries is decreased in high altitude placentae. Placenta 24, 326-335
51. Jiang, C., Ting, A. T., and Seed, B. (1998) PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines. Nature 391, 82-86
52. Guo, Y., Xiao, P., Lei, S., Deng, F., Xiao, G. G., Liu, Y., Chen, X., Li, L., Wu, S., Chen, Y., Jiang, H., Tan, L., Xie, J., Zhu, X., Liang, S., and Deng, H. (2008) How is mRNA expression predictive for protein expression? A correlation study on human circulating monocytes. Acta Biochim. Biophys. Sinica 40, 426-436
53. Zamudio, S., Torricos, T., Fik, E., Oyala, M., Echalar, L., Pullockaran, J., Tutino, E., Martin, B., Belliappa, S., Balanza, E., and Illsley, N. P. (2010) Hypoglycemia and the origin of hypoxia-induced reduction in human fetal growth. PLoS One 5, e8551
54. Towler, M. C., and Hardie, D. G. (2007) AMP-Activated protein kinase in metabolic control and insulin signaling. Circ. Res. 100, 328-341
55. Zhang, B. B., Zhou, G., and Li, C. (2009) AMPK: an emerging drug target for diabetes and the metabolic syndrome. Cell Metab. 9, 407-416
56. Bugianesi, E., McCullough, A. J., and Marchesini, G. (2005) Insulin resistance: a metabolic pathway to chronic liver disease. Hepatology 42, 987-1000
57. Sozio, M. S., Lu, C., Zeng, Y., Liangpunsakul, S., and Crabb, D. W. (2011) Activated AMPK inhibits PPAR-And PPAR-α transcriptional activity in hepatoma cells. Am. J. Physiol. Gastrointest. Liver Physiol. 301, G739-G747
58. Krampl, E., Kametas, N. A., Cacho-Zegarra, A. M., Roden, M., and Nicolaides, K. H. (2001) Maternal plasma glucose at high altitude. Br. J. Obstet. Gynaecol. 108, 254-257
59. Barker, D. J. (1999) Fetal origins of cardiovascular disease. Ann. Med. 31 3-6