Evidence of endoplasmic reticulum stress and protein synthesis inhibition in the placenta of non-native women at high altitude

FASEB Journal

Volumn 26, Issue 5, 2012, Pages 1970-1981

  Yung, Hong Wa ^a   Cox, Mathew ^a   Van Patot, Martha Tissot ^a   Burton, Graham J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

AKT mTOR signaling; Birth weight; Hypoxia; Pregnancy

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; INITIATION FACTOR 2ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE B; SALUBRINAL;

ADULT; ALTITUDE; ARTICLE; BIRTH WEIGHT; CANCER CELL CULTURE; CELL PROLIFERATION; CHORIOCARCINOMA; CHORION VILLUS; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENZYME PHOSPHORYLATION; FEMALE; FETOPLACENTAL UNIT; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; IMMUNOHISTOCHEMISTRY; LOW BIRTH WEIGHT; PLACENTA; PREGNANCY; PREGNANT WOMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TROPHOBLAST;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ALTITUDE; BLOTTING, WESTERN; CELL LINE, TUMOR; ENDOPLASMIC RETICULUM; EUKARYOTIC INITIATION FACTOR-2; FEMALE; HUMANS; OXIDATIVE STRESS; PHOSPHOPROTEINS; PHOSPHORYLATION; PLACENTA; PREGNANCY; PROTEIN BIOSYNTHESIS; PROTO-ONCOGENE PROTEINS C-AKT; REAL-TIME POLYMERASE CHAIN REACTION;

EUKARYOTA;

EID: 84860909945     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-190082     Document Type: Article

References (58)

1. Moore, L. G., Niermeyer, S., and Zamudio, S. (1998) Human adaptation to high altitude: regional and life-cycle perspectives. Am. J. Physiol. Anthropol. Suppl. 27, 25-64
2. Giussani, D. A., Phillips, P. S., Anstee, S., and Barker, D. J. (2001) Effects of altitude versus economic status on birth weight and body shape at birth. Pediatr. Res. 49, 490-494 (Pubitemid 32274961)
3. Keyes, L. E., Armaza, J. F., Niermeyer, S., Vargas, E., Young, D. A., and Moore, L. G. (2003) Intrauterine growth restriction, preeclampsia, and intrauterine mortality at high altitude in Bolivia. Pediatr. Res. 54, 20-25 (Pubitemid 36736800)
4. Moore, L. G., Young, D., McCullough, R. E., Droma, T., and Zamudio, S. (2001) Tibetan protection from intrauterine growth restriction (IUGR) and reproductive loss at high altitude. Am. J. Hum. Biol. 13, 635-644 (Pubitemid 32771407)
5. Julian, C. G., Vargas, E., Armaza, J. F., Wilson, M. J., Niermeyer, S., 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 (Pubitemid 47436223)
6. Giussani, D. A., Salinas, C. E., Villena, M., and Blanco, C. E. (2007) The role of oxygen in prenatal growth: studies in the chick embryo. J. Physiol. 585, 911-917 (Pubitemid 350278724)
7. Krampl, E., Lees, C., Bland, J. M., Espinoza Dorado, J., Moscoso, G., and Campbell, S. (2000) Fetal biometry at 4300 m compared to sea level in Peru. Ultrasound Obstet. Gynecol. 16, 9-18 (Pubitemid 33108680)
8. Postigo, L., Heredia, G., Illsley, N. P., Torricos, T., Dolan, C., Echalar, L., Tellez, W., Maldonado, I., Brimacombe, M., Balanza, E., Vargas, E., and Zamudio, S. (2009) Where the O2 goes to: preservation of human fetal oxygen delivery and consumption at high altitude. J. Physiol. 587, 693-708
9. 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. Regul. Integr. Comp. Physiol. 296, R1564-R1575
10. Moore, L. G., Zamudio, S., Zhuang, J., Sun, S., and Droma, T. (2001) Oxygen transport in Tibetan women during pregnancy at 3,658 m. Am. J. Physiol. Anthropol. 114, 42-53 (Pubitemid 32047317)
11. Wouters, B. G., and Koritzinsky, M. (2008) Hypoxia signalling through mTOR and the unfolded protein response in cancer. Nat. Rev. Cancer 8, 851-864
12. Carter, A. M. (2000) Placental oxygen consumption. Part I: in vivo studies-a review. Placenta 21(Suppl. A), S31-S37
13. Jackson, M. R., Mayhew, T. M., and Haas, J. D. (1987) The volumetric composition of human term placentae: altitudinal, ethnic and sex differences in Bolivia. J. Anat. 152, 173-187 (Pubitemid 17121533)
14. Jackson, M. R., Mayhew, T. M., and Haas, J. D. (1987) Morphometric studies on villi in human term placentae and the effects of altitude, ethnic grouping and sex of newborn. Placenta 8, 487-495 (Pubitemid 17159583)
15. Koritzinsky, M., Magagnin, M. G., van den Beucken, T., Seigneuric, R., Savelkouls, K., Dostie, J., Pyronnet, S., Kaufman, R. J., Weppler, S. A., Voncken, J. W., Lambin, P., Koumenis, C., Sonenberg, N., and Wouters, B. G. (2006) Gene expression during acute and prolonged hypoxia is regulated by distinct mechanisms of translational control. EMBO J. 25, 1114 -1125
16. Wek, R. C., Jiang, H. Y., and Anthony, T. G. (2006) Coping with stress: eIF2 kinases and translational control. Biochem. Soc. Trans. 34, 7-11 (Pubitemid 43235522)
17. Bi, M., Naczki, C., Koritzinsky, M., Fels, D., Blais, J., Hu, N., Harding, H., Novoa, I., Varia, M., Raleigh, J., Scheuner, D., Kaufman, R. J., Bell, J., Ron, D., Wouters, B. G., and Koumenis, C. (2005) ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J. 24, 3470-3481 (Pubitemid 41486784)
18. Liu, L., Wise, D. R., Diehl, J. A., and Simon, M. C. (2008) Hypoxic reactive oxygen species regulate the integrated stress response and cell survival. J. Biol. Chem. 283, 31153-31162
19. Koromilas, A. E., Roy, S., Barber, G. N., Katze, M. G., and Sonenberg, N. (1992) Malignant transformation by a mutant of the IFN-inducible dsRNA-dependent protein kinase. Science 257, 1685-1689
20. Scheuner, D., Song, B., McEwen, E., Liu, C., Laybutt, R., Gillespie, P., Saunders, T., Bonner-Weir, S., and Kaufman, R. J. (2001) Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7, 1165-1176 (Pubitemid 32607351)
21. Yamaguchi, S., Ishihara, H., Yamada, T., Tamura, A., Usui, M., Tominaga, R., Munakata, Y., Satake, C., Katagiri, H., Tashiro, F., Aburatani, H., Tsukiyama-Kohara, K., Miyazaki, J., Sonenberg, N., and Oka, Y. (2008) ATF4-mediated induction of 4E-BP1 contributes to pancreatic beta cell survival under endoplasmic reticulum stress. Cell Metab. 7, 269-276 (Pubitemid 351285529)
22. Alessi, D. R., Andjelkovic, M., Caudwell, B., Cron, P., Morrice, N., Cohen, P., and Hemmings, B. A. (1996) Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15, 6541-6551 (Pubitemid 26413787)
23. Sarbassov, D. D., Guertin, D. A., Ali, S. M., and Sabatini, D. M. (2005) Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307, 1098-1101 (Pubitemid 40262113)
24. Nave, B. T., Ouwens, M., Withers, D. J., Alessi, D. R., and Shepherd, P. R. (1999) Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochem. J. 344, 427-431 (Pubitemid 30011599)
25. Inoki, K., Li, Y., Zhu, T., Wu, J., and Guan, K. L. (2002) TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat. Cell Biol. 4, 648-657 (Pubitemid 34993700)
26. Gingras, A. C., Gygi, S. P., Raught, B., Polakiewicz, R. D., Abraham, R. T., Hoekstra, M. F., Aebersold, R., and Sonenberg, N. (1999) Regulation of 4E-BP1 phosphorylation: a novel twostep mechanism. Genes Dev. 13, 1422-1437 (Pubitemid 29270247)
27. Brown, E. J., Beal, P. A., Keith, C. T., Chen, J., Shin, T. B., and Schreiber, S. L. (1995) Control of p70 s6 kinase by kinase activity of FRAP in vivo. Nature 377, 441-446
28. Yung, H. W., Korolchuk, S., Tolkovsky, A. M., Charnock-Jones, D. S., and Burton, G. J. (2007) Endoplasmic reticulum stress exacerbates ischemia-reperfusion-induced apoptosis through attenuation of Akt protein synthesis in human choriocarcinoma cells. FASEB J. 21, 872-884 (Pubitemid 46348260)
29. Yung, H. W., Charnock-Jones, D. S., and Burton, G. J. (2011) Regulation of AKT phosphorylation at Ser473 and Thr308 by endoplasmic reticulum stress modulates substrate specificity in a severity dependent manner. PLoS One 6, e17894
30. Van Patot, M. C., Valdez, M., Becky, V., Cindrova-Davies, T., Johns, J., Zwerdling, L., Jauniaux, E., and Burton, G. J. (2009) Impact of pregnancy at high altitude on placental morphology in non-native women with and without preeclampsia. Placenta 30, 523-528
31. Tissot van Patot, M. C., Murray, A. J., Beckey, V., Cindrova-Davies, T., Johns, J., Zwerdlinger, L., Jauniaux, E., Burton, G. J., and Serkova, N. J. (2010) Human placental metabolic adaptation to chronic hypoxia, high altitude: hypoxic preconditioning. Am. J. Physiol. Regul. Integr Comp. Physiol. 298, R166-R172
32. Cindrova-Davies, T., Yung, H. W., Johns, J., Spasic-Boskovic, O., Korolchuk, S., Jauniaux, E., Burton, G. J., and Charnock-Jones, D. S. (2007) Oxidative stress, gene expression, and protein changes induced in the human placenta during labor. Am. J. Pathol. 171, 1168-1179 (Pubitemid 47582891)
33. Malhotra, J. D., and Kaufman, R. J. (2007) Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid. Redox Signal. 9, 2277-2293 (Pubitemid 350059010)
34. Cindrova-Davies, T., Spasic-Boskovic, O., Jauniaux, E., Charnock-Jones, D. S., and Burton, G. J. (2007) Nuclear factor-κB, p38, and stress-activated protein kinase mitogen-activated protein kinase signaling pathways regulate proinflammatory cytokines and apoptosis in human placental explants in response to oxidative stress: effects of antioxidant vitamins. Am. J. Pathol. 170, 1511-1520 (Pubitemid 47339297)
35. Karim, M. M., Hughes, J. M., Warwicker, J., Scheper, G. C., Proud, C. G., and McCarthy, J. E. (2001) A quantitative molecular model for modulation of mammalian translation by the eIF4E-binding protein 1. J. Biol. Chem. 276, 20750-20757
36. Jacinto, E., Facchinetti, V., Liu, D., Soto, N., Wei, S., Jung, S. Y., Huang, Q., Qin, J., and Su, B. (2006) SIN1/MIP1 maintains rictor-mTOR complex integrity and regulates Akt phosphorylation and substrate specificity. Cell 127, 125-137 (Pubitemid 44466632)
37. Zetterberg, A., Larsson, O., and Wiman, K. G. (1995) What is the restriction point? Curr. Opin. Cell Biol. 7, 835-842
38. Boyce, M., Bryant, K. F., Jousse, C., Long, K., Harding, H. P., Scheuner, D., Kaufman, R. J., Ma, D., Coen, D. M., Ron, D., and Yuan, J. (2005) A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 307, 935-939 (Pubitemid 40229232)
39. Yung, H. W., Calabrese, S., Hynx, D., Hemmings, B. A., Cetin, I., Charnock-Jones, D. S., and Burton, G. J. (2008) Evidence of placental translation inhibition and endoplasmic reticulum stress in the etiology of human intrauterine growth restriction. Am. J. Pathol. 173, 451-462
40. Yang, Z. Z., Tschopp, O., Hemmings-Mieszczak, M., Feng, J., Brodbeck, D., Perentes, E., and Hemmings, B. A. (2003) Protein kinase B alpha/Akt1 regulates placental development and fetal growth. J. Biol. Chem. 278, 32124-32131 (Pubitemid 37048402)
41. Soma, H., Hata, T., Oguro, T., Fujita, K., Kudo, M., and Vaidya, U. (2005) Characteristics of histopathological and ultrastructural features of placental villi in pregnant Nepalese women. Med. Mol. Morphol. 38, 92-103 (Pubitemid 351543878)
42. Siems, W. G., Schmidt, H., Gruner, S., and Jakstadt, M. (1992) Balancing of energy-consuming processes of K 562 cells. Cell Biochem. Funct. 10, 61-66
43. Illsley, N. P., Caniggia, I., and Zamudio, S. (2010) Placental metabolic reprogramming: do changes in the mix of energygenerating substrates modulate fetal growth? Int. J. Dev. Biol. 54, 409-419
44. Colleoni, F., Yung, H. W., Padmanabhan, N., Cetin, I., Tissot van Patot, M. C., Burton, G. J., and Murray, A. J. (2011) Hypoxia induces electron transport chain dysfunction in human placental mitochondria. Placenta 32, A46
45. Walsh, B., Tonkonogi, M., Soderlund, K., Hultman, E., Saks, V., and Sahlin, K. (2001) The role of phosphorylcreatine and creatine in the regulation of mitochondrial respiration in human skeletal muscle. J. Physiol. 537, 971-978 (Pubitemid 34026622)
46. Raman, L., Tkac, I., Ennis, K., Georgieff, M. K., Gruetter, R., and Rao, R. (2005) In vivo effect of chronic hypoxia on the neurochemical profile of the developing rat hippocampus. Brain Res. Dev. Brain Res. 156, 202-209 (Pubitemid 41132130)
47. Pestova, T. V., Kolupaeva, V. G., Lomakin, I. B., Pilipenko, E. V., Shatsky, I. N., Agol, V. I., and Hellen, C. U. (2001) Molecular mechanisms of translation initiation in eukaryotes. Proc. Natl. Acad. Sci. U. S. A. 98, 7029-7036 (Pubitemid 32567898)
48. Jan, E., Thompson, S. R., Wilson, J. E., Pestova, T. V., Hellen, C. U., and Sarnow, P. (2001) Initiator Met-tRNA-independent translation mediated by an internal ribosome entry site element in cricket paralysis virus-like insect viruses. Cold Spring Harb. Symp. Quant. Biol. 66, 285-292 (Pubitemid 36097935)
49. Lu, P. D., Harding, H. P., and Ron, D. (2004) Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J. Cell Biol. 167, 27-33 (Pubitemid 39363411)
50. Kim, Y. K., and Jang, S. K. (2002) Continuous heat shock enhances translational initiation directed by internal ribosomal entry site. Biochem. Biophys. Res. Commun. 297, 224-231 (Pubitemid 35216158)
51. Choi, S. J., Oh, S. Y., Kim, J. H., Sadovsky, Y., and Roh, C. R. (2007) Increased expression of N-myc downstream-regulated gene 1 (NDRG1) in placentas from pregnancies complicated by intrauterine growth restriction or preeclampsia. Am. J. Obstet. Gynecol. 196, 45 e41-e47
52. Bastide, A., Karaa, Z., Bornes, S., Hieblot, C., Lacazette, E., Prats, H., and Touriol, C. (2008) An upstream open reading frame within an IRES controls expression of a specific VEGF-A isoform. Nucleic Acids Res. 36, 2434-2445 (Pubitemid 351567014)
53. Gingras, A. C., Raught, B., and Sonenberg, N. (1999) eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68, 913-963 (Pubitemid 29449212)
54. Gingras, A. C., Raught, B., Gygi, S. P., Niedzwiecka, A., Miron, M., Burley, S. K., Polakiewicz, R. D., Wyslouch-Cieszynska, A., Aebersold, R., and Sonenberg, N. (2001) Hierarchical phosphorylation of the translation inhibitor 4E-BP1. Genes Dev. 15, 2852-2864 (Pubitemid 33042055)
55. Reshetnikova, O. S., Burton, G. J., and Milovanov, A. P. (1994) Effects of hypobaric hypoxia on the fetoplacental unit: the morphometric diffusing capacity of the villous membrane at high altitude. Am. J. Obstet. Gynecol. 171, 1560-1565
56. Espinoza, J., Sebire, N. J., McAuliffe, F., Krampl, E., and Nicolaides, K. H. (2001) Placental villus morphology in relation to maternal hypoxia at high altitude. Placenta 22, 606 - 608
57. Drogat, B., Auguste, P., Nguyen, D. T., Bouchecareilh, M., Pineau, R., Nalbantoglu, J., Kaufman, R. J., Chevet, E., Bikfalvi, A., and Moenner, M. (2007) IRE1 signaling is essential for ischemia-induced vascular endothelial growth factor-A expression and contributes to angiogenesis and tumor growth in vivo. Cancer Res. 67, 6700-6707 (Pubitemid 47105516)
58. Iwawaki, T., Akai, R., Yamanaka, S., and Kohno, K. (2009) Function of IRE1 alpha in the placenta is essential for placental development and embryonic viability. Proc. Natl. Acad. Sci. U. S. A. 106, 16657-16662