Activation of the pluripotency factor OCT4 in smooth muscle cells is atheroprotective

Nature Medicine

Volumn 22, Issue 6, 2016, Pages 657-665

  Cherepanova, Olga A ^a   Gomez, Delphine ^a   Shankman, Laura S ^a   Swiatlowska, Pamela ^a,b   Williams, Jason ^c   Sarmento, Olga F ^d   Alencar, Gabriel F ^e   Hess, Daniel L ^a   Bevard, Melissa H ^a   Greene, Elizabeth S ^a   Murgai, Meera ^a   Turner, Stephen D ^a   Geng, Yong Jian ^a   Bekiranov, Stefan ^c   Connelly, Jessica J ^a   Tomilin, Alexey ^a   Owens, Gary K ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF GDA SK   (Poland)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^d MAYO CLINIC   (United States)

^e INSTITUTE OF CYTOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; KRUPPEL LIKE FACTOR 4; OCTAMER TRANSCRIPTION FACTOR 4; APOLIPOPROTEIN E; HIF1A PROTEIN, MOUSE; KRUPPEL LIKE FACTOR; POU5F1 PROTEIN, HUMAN; POU5F1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CELL ACTIVATION; CELL MIGRATION; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HEART PROTECTION; HUMAN; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SMOOTH MUSCLE CELL; ANIMAL; AORTA; CELL LINEAGE; CELL MOTION; CELL SURVIVAL; CHROMATIN IMMUNOPRECIPITATION; CORONARY ARTERY DISEASE; CYTOLOGY; GENETICS; MALE; METABOLISM; MIDDLE AGED; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SITE DIRECTED MUTAGENESIS; WESTERN BLOTTING; WESTERN DIET;

ANIMALS; AORTA; APOLIPOPROTEINS E; ATHEROSCLEROSIS; BLOTTING, WESTERN; CELL LINEAGE; CELL MOVEMENT; CELL SURVIVAL; CHROMATIN IMMUNOPRECIPITATION; CORONARY ARTERY DISEASE; DIET, WESTERN; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MALE; MICE; MICE, KNOCKOUT; MIDDLE AGED; MUTAGENESIS, SITE-DIRECTED; MYOCYTES, SMOOTH MUSCLE; OCTAMER TRANSCRIPTION FACTOR-3; PLAQUE, ATHEROSCLEROTIC; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84968625044     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.4109     Document Type: Article

References (47)

1. Schöler, H.R., Ruppert, S., Suzuki, N., Chowdhury, K. & Gruss, P. New type of POU domain in germ line-specific protein Oct-4. Nature 344, 435-439 (1990).
2. Lengner, C.J., Welstead, G.G. & Jaenisch, R. The pluripotency regulator Oct4: A role in somatic stem cells? Cell Cycle 7, 725-728 (2008).
3. Firth, A.L., Yao, W., Remillard, C.V., Ogawa, A. & Yuan, J.X. Upregulation of Oct-4 isoforms in pulmonary artery smooth muscle cells from patients with pulmonary arterial hypertension. Am. J. Physiol. Lung Cell. Mol. Physiol. 298, L548-L557 (2010).
4. He, W., Li, K., Wang, F., Qin, Y.R. & Fan, Q.X. Expression of OCT4 in human esophageal squamous cell carcinoma is significantly associated with poorer prognosis. World J. Gastroenterol. 18, 712-719 (2012).
5. Holmberg, J. et al. Activation of neural and pluripotent stem cell signatures correlates with increased malignancy in human glioma. PLoS One 6, e18454 (2011).
6. Lengner, C.J. et al. Oct4 expression is not required for mouse somatic stem cell self-renewal. Cell Stem Cell 1, 403-415 (2007).
7. Atlasi, Y., Mowla, S.J., Ziaee, S.A., Gokhale, P.J. & Andrews, P.W. OCT4 spliced variants are differentially expressed in human pluripotent and nonpluripotent cells. Stem Cells 26, 3068-3074 (2008).
8. Takeda, J., Seino, S. & Bell, G.I. Human Oct3 gene family: cDNA sequences, alternative splicing, gene organization, chromosomal location, and expression at low levels in adult tissues. Nucleic Acids Res. 20, 4613-4620 (1992).
9. Cantz, T. et al. Absence of OCT4 expression in somatic tumor cell lines. Stem Cells 26, 692-697 (2008).
10. Jez, M. et al. Expression and differentiation between OCT4A and its pseudogenes in human ESCs and differentiated adult somatic cells. PLoS One 9, e89546 (2014).
11. Takahashi, K. & Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676 (2006).
12. Buganim, Y. et al. Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase. Cell 150, 1209-1222 (2012).
13. Shu, J. et al. Induction of pluripotency in mouse somatic cells with lineage specifiers. Cell 153, 963-975 (2013).
14. Gao, Y. et al. Replacement of Oct4 by Tet1 during iPSC induction reveals an important role of DNA methylation and hydroxymethylation in reprogramming. Cell Stem Cell 12, 453-469 (2013).
15. Owens, G.K., Kumar, M.S. & Wamhoff, B.R. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 84, 767-801 (2004).
16. Alexander, M.R. & Owens, G.K. Epigenetic control of smooth muscle cell differentiation and phenotypic switching in vascular development and disease. Annu. Rev. Physiol. 74, 13-40 (2012).
17. Libby, P. Inflammation in atherosclerosis. Nature 420, 868-874 (2002).
18. Shankman, L.S.S. et al. KLF4-dependent phenotypic modulation of smooth muscle cells has a key role in atherosclerotic plaque pathogenesis. Nat. Med. 21, 628-637 (2015).
19. Piedrahita, J.A., Zhang, S.H., Hagaman, J.R., Oliver, P.M. & Maeda, N. Generation of mice carrying a mutant apolipoprotein E gene inactivated by gene targeting in embryonic stem cells. Proc. Natl. Acad. Sci. USA 89, 4471-4475 (1992).
20. Liedtke, S., Stephan, M. & Kögler, G. Oct4 expression revisited: potential pitfalls for data misinterpretation in stem cell research. Biol. Chem. 389, 845-850 (2008).
21. Kehler, J. et al. Oct4 is required for primordial germ cell survival. EMBO Rep. 5, 1078-1083 (2004).
22. Wirth, A. et al. G12-G13-LARG-mediated signaling in vascular smooth muscle is required for salt-induced hypertension. Nat. Med. 14, 64-68 (2008).
23. Gomez, D., Shankman, L.S., Nguyen, A.T. & Owens, G.K. Detection of histone modifications at specific gene loci in single cells in histological sections. Nat. Methods 10, 171-177 (2013).
24. Nishimura, R.A. et al. 2014 AHA/ACC guideline for the management of patients with valvular heart disease: A report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. J. Thorac. Cardiovasc. Surg. 148, e1-e132 (2014).
25. Clausen, B.E., Burkhardt, C., Reith, W., Renkawitz, R. & Förster, I. Conditional gene targeting in macrophages and granulocytes using LysM-cre mice. Transgenic Res. 8, 265-277 (1999).
26. Cherepanova, O.A. et al. Oxidized phospholipids induce type VIII collagen expression and vascular smooth muscle cell migration. Circ. Res. 104, 609-618 (2009).
27. Pidkovka, N.A. et al. Oxidized phospholipids induce phenotypic switching of vascular smooth muscle cells in vivo and in vitro. Circ. Res. 101, 792-801 (2007).
28. Botquin, V. et al. New POU dimer configuration mediates antagonistic control of an osteopontin preimplantation enhancer by Oct-4 and Sox-2. Genes Dev. 12, 2073-2090 (1998).
29. Alexander, M.R. et al. Genetic inactivation of IL-1 signaling enhances atherosclerotic plaque instability and reduces outward vessel remodeling in advanced atherosclerosis in mice. J. Clin. Invest. 122, 70-79 (2012).
30. Yang, S.W., Lim, L., Ju, S., Choi, D.H. & Song, H. Effects of matrix metalloproteinase 13 on vascular smooth muscle cells migration via Akt-ERK dependent pathway. Tissue Cell 47, 115-121 (2015).
31. Mathieu, J. et al. HIF induces human embryonic stem cell markers in cancer cells. Cancer Res. 71, 4640-4652 (2011).
32. Marsch, E., Sluimer, J.C. & Daemen, M.J. Hypoxia in atherosclerosis and inflammation. Curr. Opin. Lipidol. 24, 393-400 (2013).
33. Athanasiadou, R. et al. Targeting of de novo DNA methylation throughout the Oct-4 gene regulatory region in differentiating embryonic stem cells. PLoS One 5, e9937 (2010).
34. Feldman, N. et al. G9a-mediated irreversible epigenetic inactivation of Oct-3/4 during early embryogenesis. Nat. Cell Biol. 8, 188-194 (2006).
35. Manabe, I. & Owens, G.K. Recruitment of serum response factor and hyperacetylation of histones at smooth muscle-specific regulatory regions during differentiation of a novel P19-derived in vitro smooth muscle differentiation system. Circ. Res. 88, 1127-1134 (2001).
36. Cole, J.E. et al. Unexpected protective role for toll-like receptor 3 in the arterial wall. Proc. Natl. Acad. Sci. USA 108, 2372-2377 (2011).
37. Edfeldt, K., Swedenborg, J., Hansson, G.K. & Yan, Z.-Q. Expression of toll-like receptors in human atherosclerotic lesions: A possible pathway for plaque activation. Circulation 105, 1158-1161 (2002).
38. Lee, J. et al. Activation of innate immunity is required for efficient nuclear reprogramming. Cell 151, 547-558 (2012).
39. Lambert, C.M., Roy, M., Robitaille, G.A., Richard, D.E. & Bonnet, S. HIF-1 inhibition decreases systemic vascular remodelling diseases by promoting apoptosis through a hexokinase 2-dependent mechanism. Cardiovasc. Res. 88, 196-204 (2010).
40. Yoshida, T., Kaestner, K.H. & Owens, G.K. Conditional deletion of Kröppel-like factor 4 delays downregulation of smooth muscle cell differentiation markers but accelerates neointimal formation following vascular injury. Circ. Res. 102, 1548-1557 (2008).
41. Shatrov, V.A., Sumbayev, V.V., Zhou, J. & Brone, B. Oxidized low-density lipoprotein (oxLDL) triggers hypoxia-inducible factor-1alpha (HIF-1α) accumulation via redox-dependent mechanisms. Blood 101, 4847-4849 (2003).
42. Nakagawa, M. et al. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat. Biotechnol. 26, 101-106 (2008).
43. Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15-21 (2013).
44. Liao, Y., Smyth, G.K. & Shi, W. featureCounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923-930 (2014).
45. Love, M.I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
46. Huang, W., Sherman, B.T. & Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).
47. Wiznerowicz, M. & Trono, D. Conditional suppression of cellular genes: lentivirus vector-mediated drug-inducible RNA interference. J. Virol. 77, 8957-8961 (2003).