RhoA controls retinoid signaling by ROCK dependent regulation of retinol metabolism

Small GTPases

Volumn 9, Issue 5, 2018, Pages 433-444

  García Mariscal, Alberto ^a   Peyrollier, Karine ^a   Basse, Astrid ^a   Pedersen, Esben ^a   Rühl, Ralph ^b   van Hengel, Jolanda ^c   Brakebusch, Cord ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

retinoic acid; RhoA; ROCK; skin; stem cells

Indexed keywords

GUANOSINE TRIPHOSPHATASE; RETINOIC ACID; RETINOID DERIVATIVE; RETINOL; RHO KINASE INHIBITOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; LIGAND; RETINOID; RHO KINASE;

ANIMAL CELL; ARTICLE; CLONOGENESIS; CLONOGENIC ASSAY; CONTROLLED STUDY; CRISPR CAS SYSTEM; CYTOSKELETON; DNA MICROARRAY; EMBRYO DEVELOPMENT; FLUORESCENCE ACTIVATED CELL SORTING; GENE CONTROL; GENE EXPRESSION; GENE ONTOLOGY; KERATINOCYTE; KNOCKOUT GENE; LUCIFERASE ASSAY; MOUSE; NONHUMAN; PHENOTYPE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ANIMAL; CELL SIZE; CYTOLOGY; GENE EXPRESSION REGULATION; METABOLISM; SKIN; STEM CELL;

ANIMALS; CELL SIZE; GENE EXPRESSION REGULATION; KERATINOCYTES; LIGANDS; MICE; RETINOIDS; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; SKIN; STEM CELLS; VITAMIN A;

EID: 84995459710     PISSN: 21541248     EISSN: 21541256     Source Type: Journal    
DOI: 10.1080/21541248.2016.1248272     Document Type: Article

References (40)

1. Jaffe AB, Hall A. Rho GTPases: Biochemistry and biology. Annu Rev Cell Dev Bi 2005; 21:247-69; https://doi.org/10.1146/annurev.cellbio.21.020604.150721
2. Pedersen E, Brakebusch C. Rho GTPase function in development: how in vivo models change our view. Exp Cell Res 2012; 318:1779-87; PMID:22659168; https://doi.org/10.1016/j.yexcr.2012.05.004
3. Bustelo XR, Sauzeau V, Berenjeno IM. GTP-binding proteins of the Rho/Rac family: regulation, effectors and functions in vivo. BioEssays 2007; 29:356-70; PMID:17373658; https://doi.org/10.1002/bies.20558
4. Lawrence MS, Stojanov P, Mermel CH, Robinson JT, Garraway LA, Golub TR, Meyerson M, Gabriel SB, Lander ES, Getz G. Discovery and saturation analysis of cancer genes across 21 tumour types. Nature 2014; 505:495-501; PMID:24390350; https://doi.org/10.1038/nature12912
5. Wang K, Yuen ST, Xu J, Lee SP, Yan HH, Shi ST, Siu HC, Deng S, Chu KM, Law S, et al. Whole-genome sequencing and comprehensive molecular profiling identify new driver mutations in gastric cancer. Nat Genet 2014; 46:573-82; PMID:24816253; https://doi.org/10.1038/ng.2983
6. Posern G, Treisman R. Actin' together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol 2006; 16:588-96; PMID:17035020; https://doi.org/10.1016/j.tcb.2006.09.008
7. Busche S, Descot A, Julien S, Genth H, Posern G. Epithelial cell-cell contacts regulate SRF-mediated transcription via Rac-actin-MAL signalling. J Cell Sci 2008; 121:1025-35; PMID:18334560; https://doi.org/10.1242/jcs.014456
8. Sebe A, Erdei Z, Varga K, Bodor C, Mucsi I, Rosivall L. Cdc42 regulates myocardin-related transcription factor nuclear shuttling and alpha-smooth muscle actin promoter activity during renal tubular epithelial-mesenchymal transition. Nephron Exp Nephrol 2010; 114:E117-25; PMID:20016221; https://doi.org/10.1159/000265550
9. Marinissen MT, Chiariello M, Gutkind JS. Regulation of gene expression by the small GTPase Rho through the ERK6 (p38 gamma) MAP kinase pathway. Genes Dev 2001; 15:535-53; PMID:11238375; https://doi.org/10.1101/gad.855801
10. Charron F, Tsimiklis G, Arcand M, Robitaille L, Liang Q, Molkentin JD, Meloche S, Nemer M. Tissue-specific GATA factors are transcriptional effectors of the small GTPase RhoA. Genes Dev 2001; 15:2702-19; PMID:11641276; https://doi.org/10.1101/gad.915701
11. Jackson B, Peyrollier K, Pedersen E, Basse A, Karlsson R, Wang Z, Lefever T, Ochsenbein AM, Schmidt G, Aktories K, et al. RhoA is dispensable for skin development, but crucial for contraction and directed migration of keratinocytes. Mol Biol Cell 2011; 22:593-605; PMID:21209320; https://doi.org/10.1091/mbc.E09-10-0859
12. Kikuchi K, Tagami K, Hibi S, Yoshimura H, Tokuhara N, Tai K, Hida T, Yamauchi T, Nagai M. Syntheses and evaluation of quinoline derivatives as novel retinoic acid receptor alpha antagonists. Bioorg Med Chem Lett 2001; 11:1215-8; PMID:11354380; https://doi.org/10.1016/S0960-894X(01)00177-9
13. Lee SA, Belyaeva OV, Wu L, Kedishvili NY. Retinol dehydrogenase 10 but not retinol/sterol dehydrogenase(s) regulates the expression of retinoic acid-responsive genes in human transgenic skin raft culture. J Biol Chem 2011; 286:13550-60; PMID:21345790; https://doi.org/10.1074/jbc.M110.181065
14. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4:44-57; PMID:19131956; https://doi.org/10.1038/nprot.2008.211
15. Bernard FX, Pedretti N, Rosdy M, Deguercy A. Comparison of gene expression profiles in human keratinocyte mono-layer cultures, reconstituted epidermis and normal human skin; transcriptional effects of retinoid treatments in reconstituted human epidermis. Exp Dermatol 2002; 11:59-74; PMID:11952828; https://doi.org/10.1034/j.1600-0625.2002.110107.x
16. Lee DD, Stojadinovic O, Krzyzanowska A, Vouthounis C, Blumenberg M, Tomic-Canic M. Retinoid-Responsive Transcriptional Changes in Epidermal Keratinocytes. J Cell Physiol 2009; 220:427-39; PMID:19388012; https://doi.org/10.1002/jcp.21784
17. Torma H. Regulation of keratin expression by retinoids. Dermato-endocrinology 2011; 3:136-40; PMID:22110773; https://doi.org/10.4161/derm.15026
18. Duester G. Retinoid signaling in control of progenitor cell differentiation during mouse development. Semin Cell Dev Biol 2013; 24:694-700; PMID:23973941; https://doi.org/10.1016/j.semcdb.2013.08.001
19. Gudas LJ. Retinoids induce stem cell differentiation via epigenetic changes. Semin Cell Dev Biol 2013; 24:701-5; PMID:23973942; https://doi.org/10.1016/j.semcdb.2013.08.002
20. Osei-Sarfo K, Gudas LJ. Retinoic acid suppresses the canonical Wnt signaling pathway in embryonic stem cells and activates the noncanonical Wnt signaling pathway. Stem Cells 2014; 32:2061-71; PMID:24648413; https://doi.org/10.1002/stem.1706
21. Lim YC, Kang HJ, Kim YS, Choi EC. All-trans-retinoic acid inhibits growth of head and neck cancer stem cells by suppression of Wnt/beta-catenin pathway. Eur J Cancer 2012; 48:3310-8; PMID:22640830; https://doi.org/10.1016/j.ejca.2012.04.013
22. Collins CA, Watt FM. Dynamic regulation of retinoic acid-binding proteins in developing, adult and neoplastic skin reveals roles for beta-catenin and Notch signalling. Dev Biol 2008; 324:55-67; PMID:18805411; https://doi.org/10.1016/j.ydbio.2008.08.034
23. Rhinn M, Dolle P. Retinoic acid signalling during development. Development 2012; 139:843-58; PMID:22318625; https://doi.org/10.1242/dev.065938
24. Tang XH, Gudas LJ. Retinoids, retinoic acid receptors, and cancer. Annu Rev Pathol 2011; 6:345-64; PMID:21073338; https://doi.org/10.1146/annurev-pathol-011110-130303
25. Kumar S, Sandell LL, Trainor PA, Koentgen F, Duester G. Alcohol and aldehyde dehydrogenases: Retinoid metabolic effects in mouse knockout models. Bba-Mol Cell Biol L 2012; 1821:198-205.
26. Kang S, Duell EA, Fisher GJ, Datta SC, Wang ZQ, Reddy AP, Tavakkol A, Yi JY, Griffiths CE, Elder JT, et al. Application of retinol to human skin in vivo induces epidermal hyperplasia and cellular retinoid binding proteins characteristic of retinoic acid but without measurable retinoic acid levels or irritation. J Invest Dermatol 1995; 105:549-56; PMID:7561157; https://doi.org/10.1111/1523-1747.ep12323445
27. Kedishvili NY. Enzymology of retinoic acid biosynthesis and degradation. J Lipid Res 2013; 54:1744-60; PMID:23630397; https://doi.org/10.1194/jlr.R037028
28. Kamijo H, Matsumura Y, Thumkeo D, Koike S, Masu M, Shimizu Y, Ishizaki T, Narumiya S. Impaired vascular remodeling in the yolk sac of embryos deficient in ROCK-I and ROCK-II. Genes Cells 2011; 16:1012-21; PMID:21895889; https://doi.org/10.1111/j.1365-2443.2011.01546.x
29. Bohnsack BL, Lai L, Dolle P, Hirschi KK. Signaling hierarchy downstream of retinoic acid that independently regulates vascular remodeling and endothelial cell proliferation. Gene Dev 2004; 18:1345-58; PMID:15175265; https://doi.org/10.1101/gad.1184904
30. Terunuma A, Limgala RP, Park CJ, Choudhary I, Vogel JC. Efficient procurement of epithelial stem cells from human tissue specimens using a Rho-associated protein kinase inhibitor Y-27632. Tissue Eng Part A 2010; 16:1363-8; PMID:19912046; https://doi.org/10.1089/ten.tea.2009.0339
31. Chapman S, McDermott DH, Shen K, Jang MK, McBride AA. The effect of Rho kinase inhibition on long-term keratinocyte proliferation is rapid and conditional. Stem Cell Res Ther 2014; 5:60; PMID:24774536; https://doi.org/10.1186/scrt449
32. Singh SR. Stem cell niche in tissue homeostasis, aging and cancer. Curr Med Chem 2012; 19:5965-74; PMID:22963571; https://doi.org/10.2174/0929867311209065965
33. Pincelli C, Marconi A. Keratinocyte stem cells: friends and foes. J Cell Physiol 2010; 225:310-5; PMID:20568222; https://doi.org/10.1002/jcp.22275
34. Shalinsky DR, Bischoff ED, Gregory ML, Gottardis MM, Hayes JS, Lamph WW, Heyman RA, Shirley MA, Cooke TA, Davies PJ, et al. Retinoid-induced suppression of squamous cell differentiation in human oral squamous cell carcinoma xenografts (line 1483) in athymic nude mice. Cancer Res 1995; 55:3183-91; PMID:7541715
35. Low BC, Pan CQ, Shivashankar GV, Bershadsky A, Sudol M, Sheetz M. YAP/TAZ as mechanosensors and mechanotransducers in regulating organ size and tumor growth. FEBS Lett 2014; 588:2663-70; PMID:24747426; https://doi.org/10.1016/j.febslet.2014.04.012
36. Dai J, Brooks Y, Lefort K, Getsios S, Dotto GP. The retinoid-related orphan receptor RORalpha promotes keratinocyte differentiation via FOXN1. PLoS One 2013; 8:e70392; PMID:23922987; https://doi.org/10.1371/journal.pone.0070392
37. Pedersen E, Basse A, Lefever T, Peyrollier K, Brakebusch C. Rho GTPase knockout induction in primary keratinocytes from adult mice. Methods Mol Biol 2012; 827:157-66; PMID:22144274; https://doi.org/10.1007/978-1-61779-442-1_11
38. Ehrhardt Christina, Schmolke Mirco, Matzke Andreas, Knoblauch Alexander, Will Carola, Wixler Viktor, Ludwig S. Polyethylenimine, a cost-effective transfection reagent. Signal Transduction 2006; 6:179-84; https://doi.org/10.1002/sita.200500073
39. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002; 30:207-10; PMID:11752295; https://doi.org/10.1093/nar/30.1.207
40. Jensen KB, Driskell RR, Watt FM. Assaying proliferation and differentiation capacity of stem cells using disaggregated adult mouse epidermis. Nat Protoc 2010; 5:898-911; PMID:20431535; https://doi.org/10.1038/nprot.2010.39