Modulation of endothelial cell migration by ER stress and insulin resistance: A role during maternal obesity?

Frontiers in Pharmacology

Volumn 5 AUG, Issue , 2014, Pages

  Sáez, Pablo J ^a   Villalobos Labra, Roberto ^a   Westermeier, Francisco ^a,b,c   Sobrevia, Luis ^a,d,e   Farías Jofré, Marcelo ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b UNIVERSIDAD SAN SEBASTIÁN   (Chile)

^c UNIVERSITY OF CHILE   (Chile)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Akt; Cytoskeleton; Mesenchymal migration; Polarization; RhoA; Scrib; Unfolded protein response

Indexed keywords

PROTEIN KINASE B; RHO KINASE;

ANGIOGENESIS; CALCIUM SIGNALING; CELL MIGRATION; CELL POLARITY; CELL STRESS; CENTROSOME; CHEMOTAXIS; DIMERIZATION; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIUM CELL; GOLGI COMPLEX; HUMAN; INSULIN RESISTANCE; MATERNAL OBESITY; MICROTUBULE; NONHUMAN; PROGENY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN UNFOLDING; REVIEW; UPREGULATION;

EID: 84906499785     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2014.00189     Document Type: Review

References (113)

1. Aepfelbacher, M., Essler, M., Huber, E., Sugai, M., and Weber, P. C. (1997). Bacterial toxins block endothelial wound repair. Evidence that Rho GTPases control cytoskeletal rearrangements in migrating endothelial cells. Arterioscler. Thromb. Vasc. Biol. 17, 1623-1629. doi: 10.1161/01.ATV.17.9.1623
2. American College of Obstetricians and Gynecologists [ACOG]. (2005). ACOG committee opinion number 315, September 2005. Obesity in pregnancy. Obstet. Gynecol. 106, 671-675.
3. Amin, A., Choi, S. K., Galan, M., Kassan, M., Partyka, M., Kadowitz, P.,et al. (2012). Chronic inhibition of endoplasmic reticulum stress and inflammation prevents ischaemia-induced vascular pathology in type II diabetic mice. J. Pathol. 227, 165-174. doi: 10.1002/path.3960
4. Appenzeller-Herzog, C., and Hall, M. N. (2012). Bidirectional crosstalk between endoplasmic reticulum stress and mTOR signaling. Trends Cell Biol. 22, 274-282. doi: 10.1016/j.tcb.2012.02.006
5. Aranda, E., and Owen, G. I. (2009). A semi-quantitative assay to screen for angiogenic compounds and compounds with angiogenic potential using the EA.hy 926 endothelial cell line. Biol. Res. 42, 377-389. doi: 10.4067/S0716-97602009000300012
6. Banerjee, A., Lang, J. Y., Hung, M. C., Sengupta, K., Banerjee, S. K., Baksi, K.,et al. (2011). Unfolded protein response is required in nu/nu mice microvasculature for treating breast tumor with tunicamycin. J. Biol. Chem. 286, 29127-29138. doi: 10.1074/jbc.M110.169771
7. Basha, B., Samuel, S. M., Triggle, C. R., and Ding, H. (2012). Endothelial dysfunction in diabetes mellitus: possible involvement of endoplasmic reticulum stress? Exp. Diabetes Res. 2012, 481840. doi: 10.1155/2012/481840
8. Berridge, M. J., Bootman, M. D., and Roderick, H. L. (2003). Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4, 517-529. doi: 10.1038/nrm1155
9. Boddu, N. J., Theus, S., Luo, S., Wei, J. Y., and Ranganathan, G. (2014). Is the lack of adiponectin associated with increased ER/SR stress and inflammation in the heart? Adipocyte 3, 10-18. doi: 10.4161/adip.26684
10. Boden, G., Cheung, P., Salehi, S., Homko, C., Loveland-Jones, C., Jayarajan, S.,et al. (2014). Insulin regulates the unfolded protein response in human adipose tissue. Diabetes 63, 912-922. doi: 10.2337/db13-0906
11. Brozinick, J. T. Jr., Roberts, B. R., and Dohm, G. L. (2003). Defective signaling through Akt-2 and -3 but not Akt-1 in insulin-resistant human skeletal muscle: potential role in insulin resistance. Diabetes 52, 935-941. doi: 10.2337/diabetes.52.4.935
12. Bruyndonckx, L., Hoymans, V. Y., Van Craenenbroeck, A. H., Vissers, D. K., Vrints, C. J., Ramet, J.,et al. (2013). Assessment of endothelial dysfunction in childhood obesity and clinical use. Oxid. Med. Cell Longev. 2013, 174782. doi: 10.1155/2013/174782
13. 2+, leading to induction of endoplasmic reticulum stress in pancreatic Β-cells. Diabetes 54, 452-461. doi: 10.2337/diabetes.54.2.452
14. Catalano, P. M., Presley, L., Minium, J., and Hauguel-De Mouzon, S. (2009). Fetuses of obese mothers develop insulin resistance in utero. Diabetes Care 32, 1076-1080. doi: 10.2337/dc08-2077
15. Cnop, M., Foufelle, F., and Velloso, L. A. (2012). Endoplasmic reticulum stress, obesity and diabetes. Trends Mol. Med. 18, 59-68. doi: 10.1016/j.molmed.2011.07.010
16. Cheng, X., Chapple, S. J., Patel, B., Puszyk, W., Sugden, D., Yin, X.,et al. (2013). Gestational diabetes mellitus impairs Nrf2-mediated adaptive antioxidant defenses and redox signaling in fetal endothelial cells in utero. Diabetes 62, 4088-4097. doi: 10.2337/db13-0169
17. Christiaens, V., and Lijnen, H. R. (2010). Angiogenesis and development of adipose tissue. Mol. Cell. Endocrinol. 318, 2-9. doi: 10.1016/j.mce.2009.08.006
18. 2+entry to ATP and mitochondrial potential. Biochem. Biophys. Res. Commun. 381, 176-180. doi: 10.1016/j.bbrc.2009.02.006
19. da Silva, A. F., Mariotti, F. R., Maximo, V., and Campello, S. (2014). Mitochondria dynamism: of shape, transport and cell migration. Cell. Mol. Life Sci. 71, 2313-2324. doi: 10.1007/s00018-014-1557-8
20. Dejeans, N., Pluquet, O., Lhomond, S., Grise, F., Bouchecareilh, M., Juin, A.,et al. (2012). Autocrine control of glioma cells adhesion and migration through IRE1alpha-mediated cleavage of SPARC mRNA. J. Cell Sci. 125, 4278-4287. doi: 10.1242/jcs.099291
21. Dinarello, C. A. (2007). Historical insights into cytokines. Eur. J. Immunol. 37(Suppl. 1), S34-S45. doi: 10.1002/eji.200737772
22. Dong, D., Ni, M., Li, J., Xiong, S., Ye, W., Virrey, J. J.,et al. (2008). Critical role of the stress chaperone GRP78/BiP in tumor proliferation, survival, and tumor angiogenesis in transgene-induced mammary tumor development. Cancer Res. 68, 498-505. doi: 10.1158/0008-5472.CAN-07-2950
23. Dorscheid, D. R., Wojcik, K. R., Yule, K., and White, S. R. (2001). Role of cell surface glycosylation in mediating repair of human airway epithelial cell monolayers. Am. J. Physiol. Lung. Cell. Mol. Physiol. 281, L982-L992.
24. Dubois, V., Delort, L., Billard, H., Vasson, M. P., and Caldefie-Chezet, F. (2013). Breast cancer and obesity: in vitro interferences between adipokines and proangiogenic features and/or antitumor therapies? PLoS ONE 8:e58541. doi: 10.1371/journal.pone.0058541
25. Dubova, E. A., Pavlov, K. A., Borovkova, E. I., Bayramova, M. A., Makarov, I. O., and Shchegolev, A. I. (2011). Vascular endothelial growth factor and its receptors in the placenta of pregnant women with obesity. Bull. Exp. Biol. Med. 151, 253-258. doi: 10.1007/s10517-011-1302-3
26. Duksin, D., and Bornstein, P. (1977). Changes in surface properties of normal and transformed cells caused by tunicamycin, an inhibitor of protein glycosylation. Proc. Natl. Acad. Sci. U.S.A. 74, 3433-3437. doi: 10.1073/pnas.74.8.3433
27. Etienne-Manneville, S. (2013). Microtubules in cell migration. Annu. Rev. Cell Dev. Biol. 29, 471-499. doi: 10.1146/annurev-cellbio-101011-155711
28. Farías, M., Puebla, C., Westermeier, F., Jo, M. J., Pastor-Anglada, M., Casanello, P.,et al. (2010). Nitric oxide reduces SLC29A1 promoter activity and adenosine transport involving transcription factor complex hCHOP-C/EBPalpha in human umbilical vein endothelial cells from gestational diabetes. Cardiovasc. Res. 86, 45-54. doi: 10.1093/cvr/cvp410
29. Farías, M., San Martin, R., Puebla, C., Pearson, J. D., Casado, J. F., Pastor-Anglada, M.,et al. (2006). Nitric oxide reduces adenosine transporter ENT1 gene (SLC29A1) promoter activity in human fetal endothelium from gestational diabetes. J. Cell. Physiol. 208, 451-460. doi: 10.1002/jcp.20680
30. Flamment, M., Hajduch, E., Ferre, P., and Foufelle, F. (2012). New insights into ER stress-induced insulin resistance. Trends Endocrinol. Metab. 23, 381-390. doi: 10.1016/j.tem.2012.06.003
31. Flenady, V., Koopmans, L., Middleton, P., Froen, J. F., Smith, G. C., Gibbons, K.,et al. (2011). Major risk factors for stillbirth in high-income countries: a systematic review and meta-analysis. Lancet 377, 1331-1340. doi: 10.1016/S0140-6736(10)62233-7
32. Friedl, P., Wolf, K., and Lammerding, J. (2011). Nuclear mechanics during cell migration. Curr. Opin. Cell Biol. 23, 55-64. doi: 10.1016/j.ceb.2010.10.015
33. Fu, S., Watkins, S. M., and Hotamisligil, G. S. (2012). The role of endoplasmic reticulum in hepatic lipid homeostasis and stress signaling. Cell Metab. 15, 623-634. doi: 10.1016/j.cmet.2012.03.007
34. Galan, M., Kassan, M., Kadowitz, P. J., Trebak, M., Belmadani, S., and Matrougui, K. (2014). Mechanism of endoplasmic reticulum stress-induced vascular endothelial dysfunction. Biochim. Biophys. Acta 1843, 1063-1075. doi: 10.1016/j.bbamcr.2014.02.009
35. Garg, A. D., Kaczmarek, A., Krysko, O., Vandenabeele, P., Krysko, D. V., and Agostinis, P. (2012). ER stress-induced inflammation: does it aid or impede disease progression? Trends Mol. Med. 18, 589-598. doi: 10.1016/j.molmed.2012.06.010
36. Ghosh, R., Lipson, K. L., Sargent, K. E., Mercurio, A. M., Hunt, J. S., Ron, D.,et al. (2010). Transcriptional regulation of VEGF-A by the unfolded protein response pathway. PLoS ONE 5:e9575. doi: 10.1371/journal.pone.0009575
37. Gipson, I. K., Kiorpes, T. C., and Brennan, S. J. (1984). Epithelial sheet movement: effects of tunicamycin on migration and glycoprotein synthesis. Dev. Biol. 101, 212-220. doi: 10.1016/0012-1606(84)90131-3
38. Goetze, S., Bungenstock, A., Czupalla, C., Eilers, F., Stawowy, P., Kintscher, U.,et al. (2002). Leptin induces endothelial cell migration through Akt, which is inhibited by PPARgamma-ligands. Hypertension 40, 748-754. doi: 10.1161/01.HYP.0000035522.63647.D3
39. Gotlieb, A. I., May, L. M., Subrahmanyan, L., and Kalnins, V. I. (1981). Distribution of microtubule organizing centers in migrating sheets of endothelial cells. J. Cell Biol. 91, 589-594. doi: 10.1083/jcb.91.2.589
40. Gregor, M. F., Yang, L., Fabbrini, E., Mohammed, B. S., Eagon, J. C., Hotamisligil, G. S.,et al. (2009). Endoplasmic reticulum stress is reduced in tissues of obese subjects after weight loss. Diabetes 58, 693-700. doi: 10.2337/db08-1220
41. Guo, S. (2014). Insulin signaling, resistance, and the metabolic syndrome: insights from mouse models into disease mechanisms. J. Endocrinol. 220, T1-T23. doi: 10.1530/JOE-13-0327
42. Haberzettl, P., Vladykovskaya, E., Srivastava, S., and Bhatnagar, A. (2009). Role of endoplasmic reticulum stress in acrolein-induced endothelial activation. Toxicol. Appl. Pharmacol. 234, 14-24. doi: 10.1016/j.taap.2008.09.019
43. Hetz, C., Chevet, E., and Harding, H. P. (2013). Targeting the unfolded protein response in disease. Nat. Rev. Drug Discov. 12, 703-719. doi: 10.1038/nrd3976
44. Hosoi, T., Sasaki, M., Miyahara, T., Hashimoto, C., Matsuo, S., Yoshii, M.,et al. (2008). Endoplasmic reticulum stress induces leptin resistance. Mol. Pharmacol. 74, 1610-1619. doi: 10.1124/mol.108.050070
45. Hotamisligil, G. S. (2010). Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140, 900-917. doi: 10.1016/j.cell.2010.02.034
46. Hotchkiss, K. A., Ashton, A. W., Mahmood, R., Russell, R. G., Sparano, J. A., and Schwartz, E. L. (2002). Inhibition of endothelial cell function in vitro and angiogenesis in vivo by docetaxel (Taxotere): association with impaired repositioning of the microtubule organizing center. Mol. Cancer Ther. 1, 1191-1200.
47. Huang, Y., Zheng, L., Yang, H., Chen, J., Wang, Y., Li, H.,et al. (2013). Calcium mobilization in HeLa cells induced by nitric oxide. Scanning doi: 10.1002/sca.21098 [Epub ahead of print].
48. Indra, M. R., Karyono, S., Ratnawati, R., and Malik, S. G. (2013). Quercetin suppresses inflammation by reducing ERK1/2 phosphorylation and NF kappa B activation in leptin-induced human umbilical vein endothelial cells (HUVECs). BMC Res. Notes 6:275. doi: 10.1186/1756-0500-6-275
49. 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. doi: 10.1073/pnas.0903775106
50. Jaffe, A. B., and Hall, A. (2005). Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269. doi: 10.1146/annurev.cellbio.21.020604.150721
51. Jung, D. Y., Chalasani, U., Pan, N., Friedline, R. H., Prosdocimo, D. A., Nam, M.,et al. (2013). KLF15 is a molecular link between endoplasmic reticulum stress and insulin resistance. PLoS ONE 8:e77851. doi: 10.1371/journal.pone.0077851
52. Kamath, K., Smiyun, G., Wilson, L., and Jordan, M. A. (2014). Mechanisms of inhibition of endothelial cell migration by taxanes. Cytoskeleton (Hoboken) 71, 46-60. doi: 10.1002/cm.21153
53. Kanda, T., Wakino, S., Homma, K., Yoshioka, K., Tatematsu, S., Hasegawa, K.,et al. (2006). Rho-kinase as a molecular target for insulin resistance and hypertension. FASEB J. 20, 169-171. doi: 10.1096/fj.05-4197fje
54. Kaplon, R. E., Chung, E., Reese, L., Cox-York, K., Seals, D. R., and Gentile, C. L. (2013). Activation of the unfolded protein response in vascular endothelial cells of nondiabetic obese adults. J. Clin. Endocrinol. Metab. 98, E1505-E1509. doi: 10.1210/jc.2013-1841
55. Karali, E., Bellou, S., Stellas, D., Klinakis, A., Murphy, C., and Fotsis, T. (2014). VEGF signals through ATF6 and PERK to promote endothelial cell survival and angiogenesis in the absence of ER stress. Mol. Cell. 54, 559-572. doi: 10.1016/j.molcel.2014.03.022
56. Kozutsumi, Y., Segal, M., Normington, K., Gething, M. J., and Sambrook, J. (1988). The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature 332, 462-464. doi: 10.1038/332462a0
57. Krause, B. J., Costello, P. M., Munoz-Urrutia, E., Lillycrop, K. A., Hanson, M. A., and Casanello, P. (2013). Role of DNA methyltransferase 1 on the altered eNOS expression in human umbilical endothelium from intrauterine growth restricted fetuses. Epigenetics 8, 944-952. doi: 10.4161/epi.25579
58. Lamalice, L., Le Boeuf, F., and Huot, J. (2007). Endothelial cell migration during angiogenesis. Circ. Res. 100, 782-794. doi: 10.1161/01.RES.0000259593.07661.1e
59. Lange, S., Gonzalez, I., Pinto, M. P., Arce, M., Valenzuela, R., Aranda, E.,et al. (2014). Independent anti-angiogenic capacities of coagulation factors X and Xa. J. Cell Physiol. doi: 10.1002/jcp.24612 [Epub ahead of print].
60. Lee, P. C., Salyapongse, A. N., Bragdon, G. A., Shears, L. L. II, Watkins, S. C., Edington, H. D.,et al. (1999). Impaired wound healing and angiogenesis in eNOS-deficient mice. Am. J. Physiol. 277, H1600-H1608.
61. Leiva, A., Pardo, F., Ramírez, M. A., Farías, M., Casanello, P., and Sobrevia, L. (2011). Fetoplacental vascular endothelial dysfunction as an early phenomenon in the programming of human adult diseases in subjects born from gestational diabetes mellitus or obesity in pregnancy. Exp. Diabetes Res. 2011, 349286. doi: 10.1155/2011/349286
62. Li, C., Wang, L., Huang, K., and Zheng, L. (2012). Endoplasmic reticulum stress in retinal vascular degeneration: protective role of resveratrol. Invest. Ophthalmol. Vis. Sci. 53, 3241-3249. doi: 10.1167/iovs.11-8406
63. Li, J., Wang, J. J., Yu, Q., Wang, M., and Zhang, S. X. (2009). Endoplasmic reticulum stress is implicated in retinal inflammation and diabetic retinopathy. FEBS Lett. 583, 1521-1527. doi: 10.1016/j.febslet.2009.04.007
64. Loinard, C., Zouggari, Y., Rueda, P., Ramkhelawon, B., Cochain, C., Vilar, J.,et al. (2012). C/EBP homologous protein-10 (CHOP-10) limits postnatal neovascularization through control of endothelial nitric oxide synthase gene expression. Circulation 125, 1014-1026. doi: 10.1161/CIRCULATIONAHA.111.041830
65. Lu, J. W., Liao, C. Y., Yang, W. Y., Lin, Y. M., Jin, S. L., Wang, H. D.,et al. (2014). Overexpression of endothelin 1 triggers hepatocarcinogenesis in zebrafish and promotes cell proliferation and migration through the AKT pathway. PLoS ONE 9:e85318. doi: 10.1371/journal.pone.0085318
66. Mansouri, K., Khodarahmi, R., and Ghadami, S. A. (2013). An in vitro model for spontaneous angiogenesis using rat mesenteric endothelial cells: possible therapeutic perspective for obesity and related disorders. Pharm. Biol. 51, 974-980. doi: 10.3109/13880209.2013.773452
67. McMillen, I. C., and Robinson, J. S. (2005). Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol. Rev. 85, 571-633. doi: 10.1152/physrev.00053.2003
68. Melo, A. M., Benatti, R. O., Ignacio-Souza, L. M., Okino, C., Torsoni, A. S., Milanski, M.,et al. (2014). Hypothalamic endoplasmic reticulum stress and insulin resistance in offspring of mice dams fed high-fat diet during pregnancy and lactation. Metabolism 63, 682-692. doi: 10.1016/j.metabol.2014.02.002
69. Merchan, J. R., Kovacs, K., Railsback, J. W., Kurtoglu, M., Jing, Y., Pina, Y.,et al. (2010). Antiangiogenic activity of 2-deoxy-D-glucose. PLoS ONE 5:e13699. doi: 10.1371/journal.pone.0013699
70. Michaelis, U. R., Chavakis, E., Kruse, C., Jungblut, B., Kaluza, D., Wandzioch, K.,et al. (2013). The polarity protein Scrib is essential for directed endothelial cell migration. Circ. Res. 112, 924-934. doi: 10.1161/CIRCRESAHA.112.300592
71. Minamino, T., and Kitakaze, M. (2010). ER stress in cardiovascular disease. J. Mol. Cell Cardiol. 48, 1105-1110. doi: 10.1016/j.yjmcc.2009.10.026
72. Murohara, T., Witzenbichler, B., Spyridopoulos, I., Asahara, T., Ding, B., Sullivan, A.,et al. (1999). Role of endothelial nitric oxide synthase in endothelial cell migration. Arterioscler. Thromb. Vasc. Biol. 19, 1156-1161. doi: 10.1161/01.ATV.19.5.1156
73. Nunes, K. P., Rigsby, C. S., and Webb, R. C. (2010). RhoA/Rho-kinase and vascular diseases: what is the link? Cell Mol. Life Sci. 67, 3823-3836. doi: 10.1007/s00018-010-0460-1
74. Omelchenko, T., Vasiliev, J. M., Gelfand, I. M., Feder, H. H., and Bonder, E. M. (2003). Rho-imdependent formation of epithelial "leader" cells during wound healing. Proc. Natl. Acad. Sci. U.S.A. 100, 10788-10793. doi: 10.1073/pnas.1834401100
75. O'Toole, T. E., Abplanalp, W., Li, X., Cooper, N., Conklin, D. J., Haberzettl, P.,et al. (2014). Acrolein decreases endothelial cell migration and insulin sensitivity through induction of Let-7a. Toxicol. Sci. doi: 10.1093/toxsci/kfu087 [Epub ahead of print].
76. Ozcan, L., Ergin, A. S., Lu, A., Chung, J., Sarkar, S., Nie, D.,et al. (2009). Endoplasmic reticulum stress plays a central role in development of leptin resistance. Cell Metab. 9, 35-51. doi: 10.1016/j.cmet.2008.12.004
77. Paridaens, A., Laukens, D., Vandewynckel, Y. P., Coulon, S., Van Vlierberghe, H., Geerts, A.,et al. (2014). Endoplasmic reticulum stress and angiogenesis: is there an interaction between them? Liver Int. 34, e10-e18. doi: 10.1111/liv.12457
78. Pereira, E. R., Liao, N., Neale, G. A., and Hendershot, L. M. (2010). Transcriptional and post-transcriptional regulation of proangiogenic factors by the unfolded protein response. PLoS ONE 5:e12521. doi: 10.1371/journal.pone.0012521
79. Polec, A., Fedorcsak, P., Eskild, A., and Tanbo, T. G. (2014). The interplay of human chorionic gonadotropin (hCG) with basic fibroblast growth factor and adipokines on angiogenesis in vitro. Placenta 35, 249-253. doi: 10.1016/j.placenta.2014.02.002
80. Povero, D., Eguchi, A., Niesman, I. R., Andronikou, N., De Mollerat Du Jeu, X., Mulya, A.,et al. (2013). Lipid-induced toxicity stimulates hepatocytes to release angiogenic microparticles that require Vanin-1 for uptake by endothelial cells. Sci. Signal. 6, ra88. doi: 10.1126/scisignal.2004512
81. Reffay, M., Parrini, M. C., Cochet-Escartin, O., Ladoux, B., Buguin, A., Coscoy, S.,et al. (2014). Interplay of RhoA and mechanical forces in collective cell migration driven by leader cells. Nat. Cell Biol. 16, 217-223. doi: 10.1038/ncb2917
82. Rorth, P. (2009). Collective cell migration. Annu. Rev. Cell Dev. Biol. 25, 407-429. doi: 10.1146/annurev.cellbio.042308.113231
83. Roy, A., and Kolattukudy, P. E. (2012). Monocyte chemotactic protein-induced protein (MCPIP) promotes inflammatory angiogenesis via sequential induction of oxidative stress, endoplasmic reticulum stress and autophagy. Cell. Signal. 24, 2123-2131. doi: 10.1016/j.cellsig.2012.07.014
84. Saben, J., Lindsey, F., Zhong, Y., Thakali, K., Badger, T. M., Andres, A.,et al. (2014). Maternal obesity is associated with a lipotoxic placental environment. Placenta 35, 171-177. doi: 10.1016/j.placenta.2014.01.003
85. Salminen, A., Kauppinen, A., Hyttinen, J. M., Toropainen, E., and Kaarniranta, K. (2010). Endoplasmic reticulum stress in age-related macular degeneration: trigger for neovascularization. Mol. Med. 16, 535-542. doi: 10.2119/molmed.2010.00070
86. Schroder, M., and Kaufman, R. J. (2005). The mammalian unfolded protein response. Annu. Rev. Biochem. 74, 739-789. doi: 10.1146/annurev.biochem.73.011303.074134
87. Shiojima, I., and Walsh, K. (2002). Role of Akt signaling in vascular homeostasis and angiogenesis. Circ. Res. 90, 1243-1250. doi: 10.1161/01.RES.0000022200.71892.9F
88. Snyder-Cappione, J. E., and Nikolajczyk, B. S. (2013). When diet and exercise are not enough, think immunomodulation. Mol. Aspects Med. 34, 30-38. doi: 10.1016/j.mam.2012.10.003
89. Somanath, P. R., Razorenova, O. V., Chen, J., and Byzova, T. V. (2006). Akt1 in endothelial cell and angiogenesis. Cell Cycle 5, 512-518. doi: 10.4161/cc.5.5.2538
90. Song, J. W., Daubriac, J., Tse, J. M., Bazou, D., and Munn, L. L. (2012). RhoA mediates flow-induced endothelial sprouting in a 3-D tissue analogue of angiogenesis. Lab Chip 12, 5000-5006. doi: 10.1039/c2lc40389g
91. Suganya, N., Bhakkiyalakshmi, E., Suriyanarayanan, S., Paulmurugan, R., and Ramkumar, K. M. (2014). Quercetin ameliorates tunicamycin-induced endoplasmic reticulum stress in endothelial cells. Cell Prolif. 47, 231-240. doi: 10.1111/cpr.12102
92. Tabata, Y., Takano, K., Ito, T., Iinuma, M., Yoshimoto, T., Miura, H.,et al. (2007). Vaticanol B, a resveratrol tetramer, regulates endoplasmic reticulum stress and inflammation. Am. J. Physiol. Cell Physiol. 293, C411-C418. doi: 10.1152/ajpcell.00095.2007
93. Takatsuki, A., Arima, K., and Tamura, G. (1971). Tunicamycin, a new antibiotic. I. Isolation and characterization of tunicamycin. J. Antibiot. (Tokyo) 24, 215-223. doi: 10.7164/antibiotics.24.215
94. Triunfo, S., and Lanzone, A. (2014). Impact of overweight and obesity on obstetric outcomes. J. Endocrinol. Invest. doi: 10.1007/s40618-014-0058-9 [Epub ahead of print].
95. 2+pulses control local cycles of lamellipodia retraction and adhesion along the front of migrating cells. Curr. Biol. 22, 837-842. doi: 10.1016/j.cub.2012.03.037
96. 2+, diacylglycerol and STIM1 signalling system regulates directed cell migration. Nat. Cell Biol. 16, 133-144. doi: 10.1038/ncb2906
97. van Nieuw Amerongen, G. P., Koolwijk, P., Versteilen, A., and Van Hinsbergh, V. W. (2003). Involvement of RhoA/Rho kinase signaling in VEGF-induced endothelial cell migration and angiogenesis in vitro. Arterioscler. Thromb. Vasc. Biol. 23, 211-217. doi: 10.1161/01.ATV.0000054198.68894.88
98. Vitorino, P., and Meyer, T. (2008). Modular control of endothelial sheet migration. Genes Dev. 22, 3268-3281. doi: 10.1101/gad.1725808
99. Wang, S., Park, J. K., and Duh, E. J. (2012). Novel targets against retinal angiogenesis in diabetic retinopathy. Curr. Diab. Rep. 12, 355-363. doi: 10.1007/s11892-012-0289-0
100. Wei, C., Wang, X., Chen, M., Ouyang, K., Song, L. S., and Cheng, H. (2009). Calcium flickers steer cell migration. Nature 457, 901-905. doi: 10.1038/nature07577
101. Wei, C., Wang, X., Zheng, M., and Cheng, H. (2012). Calcium gradients underlying cell migration. Curr. Opin. Cell Biol. 24, 254-261. doi: 10.1016/j.ceb.2011.12.002
102. Westermeier, F., Sáez, P. J., Villalobos-Labra, R., Sobrevia, L., and Farías-Jofré, M. (2014). Programming of fetal insulin resistance in pregnancies with maternal obesity by ER stress and inflammation. BioMed Res. Int. 2014:917672. doi: 10.1155/2014/917672
103. Westermeier, F., Salomón, C., Gonzalez, M., Puebla, C., Guzmán-Gutierrez, E., Cifuentes, F.,et al. (2011). Insulin restores gestational diabetes mellitus-reduced adenosine transport involving differential expression of insulin receptor isoforms in human umbilical vein endothelium. Diabetes 60, 1677-1687. doi: 10.2337/db11-0155
104. World Health Organ [WHO]. (2003). Diet, nutrition and the prevention of chronic diseases. World Health Organ Tech. Rep. Ser. 916(i-viii), 1-149.
105. Wu, J., Rutkowski, D. T., Dubois, M., Swathirajan, J., Saunders, T., Wang, J.,et al. (2007). ATF6alpha optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev. Cell 13, 351-364. doi: 10.1016/j.devcel.2007.07.005
106. Wu, Z., Zhao, J., Xu, H., Lyv, Y., Feng, X., Fang, Y.,et al. (2014). Maternal quercetin administration during gestation and lactation decrease endoplasmic reticulum stress and related inflammation in the adult offspring of obese female rats. Eur. J. Nutr. doi: 10.1007/s00394-014-0673i4 [Epub ahead of print].
107. Yao, R., Du, Y., Zhang, R., Lin, F., and Luan, J. (2013). A biomimetic physiological model for human adipose tissue by adipocytes and endothelial cell cocultures with spatially controlled distribution. Biomed. Mater. 8, 045005. doi: 10.1088/1748-6041/8/4/045005
108. Yi, N., Chen, S. Y., Ma, A., Chen, P. S., Yao, B., Liang, T. M.,et al. (2012). Tunicamycin inhibits PDGF-BB-induced proliferation and migration of vascular smooth muscle cells through induction of HO-1. Anat. Rec. (Hoboken) 295, 1462-1472. doi: 10.1002/ar.22539
109. Yoon, J. S., Kim, H. M., Yadunandam, A. K., Kim, N. H., Jung, H. A., Choi, J. S.,et al. (2013). Neferine isolated from Nelumbo nucifera enhances anti-cancer activities in Hep3B cells: molecular mechanisms of cell cycle arrest, ER stress induced apoptosis and anti-angiogenic response. Phytomedicine 20, 1013-1022. doi: 10.1016/j.phymed.2013.03.024
110. 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. doi: 10.1371/journal.pone.0017894
111. Zeng, L., Xiao, Q., Chen, M., Margariti, A., Martin, D., Ivetic, A.,et al. (2013). Vascular endothelial cell growth-activated XBP1 splicing in endothelial cells is crucial for angiogenesis. Circulation 127, 1712-1722. doi: 10.1161/CIRCULATIONAHA.112.001337
112. Zera, C. A., Seely, E. W., Wilkins-Haug, L. E., Lim, K. H., Parry, S. I., and Mcelrath, T. F. (2014). The association of body mass index with serum angiogenic markers in normal and abnormal pregnancies. Am. J. Obstet. Gynecol. doi: 10.1016/j.ajog.2014.03.020 [Epub ahead of print].
113. Zhang, K., and Kaufman, R. J. (2008). From endoplasmic-reticulum stress to the inflammatory response. Nature 454, 455-462. doi: 10.1038/nature07203