Receptor tyrosine kinases modulate distinct transcriptional programs by differential usage of intracellular pathways

eLife

Volumn 4, Issue MAY, 2015, Pages

  Vasudevan, Harish N ^a   Mazot, Pierre ^a   He, Fenglei ^a   Soriano, Philippe ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLOGICAL FUNCTIONS; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; CRANIOFACIAL DEVELOPMENT; ENZYME SPECIFICITY; GENE EXPRESSION; GENE INTERACTION; GENETIC REGULATION; GENETIC TRANSCRIPTION; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; MESENCHYME CELL; MOUSE; MUTATION; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; TRANSCRIPTIONAL RESPONSE; WESTERN BLOTTING; ANIMAL; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MAMMALIAN EMBRYO; MESENCHYMAL STROMA CELL; METABOLISM; OSTEOBLAST; PALATE; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; EMBRYO, MAMMALIAN; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MESENCHYMAL STROMAL CELLS; MICE; OSTEOBLASTS; OSTEOGENESIS; PALATE; PHOSPHATIDYLINOSITOL 3-KINASES; PLATELET-DERIVED GROWTH FACTOR; PRIMARY CELL CULTURE; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84930619544     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.07186     Document Type: Article

References (69)

1. Amit I, Citri A, Shay T, Lu Y, Katz M, Zhang F, Tarcic G, Siwak D, Lahad J, Jacob-Hirsch J, Amariglio N, Vaisman N, Segal E, Rechavi G, Alon U, Mills GB, Domany E, Yarden Y. 2007. A module of negative feedback regulators defines growth factor signaling. Nature Genetics 39:503-512. doi: 10.1038/ng1987.
2. Avraham R, Yarden Y. 2011. Feedback regulation of EGFR signalling: decision making by early and delayed loops. Nature Reviews. Molecular Cell Biology 12:104-117. doi: 10.1038/nrm3048.
3. Bentires-Alj M, Kontaridis MI, Neel BG. 2006. Stops along the RAS pathway in human genetic disease. Nature Medicine 12:283-285. doi: 10.1038/nm0306-283.
4. Berger SI, Posner JM, Ma'ayan A. 2007. Genes2Networks: connecting lists of gene symbols using mammalian protein interactions databases. BMC Bioinformatics 8:372. doi: 10.1186/1471-2105-8-372.
5. Bhalla US, Ram PT, Iyengar R. 2002. MAP kinase phosphatase as a locus of flexibility in a mitogen-activated protein kinase signaling network. Science 297:1018-1023. doi: 10.1126/science.1068873.
6. Bush JO, Jiang R. 2012. Palatogenesis: morphogenetic and molecular mechanisms of secondary palate development. Development 139:828-828. doi: 10.1242/dev.079152.
7. Bush JO, Soriano P. 2010. Ephrin-B1 forward signaling regulates craniofacial morphogenesis by controlling cell proliferation across Eph-ephrin boundaries. Genes & Development 24:2068-2080. doi: 10.1101/gad. 1963210.
8. Caloca MJ, Zugaza JL, Matallanas D, Crespo P, Bustelo XR. 2003. Vav mediates Ras stimulation by direct activation of the GDP/GTP exchange factor Ras GRP1. EMBO Journal 22:3326-3336. doi: 10.1093/emboj/ cdg316.
9. Chen EY, Tan CM, Kou Y, Duan Q, Wang Z, Meirelles GV, Clark NR, Ma'ayan A. 2013. Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics 14:128. doi: 10.1186/1471- 2105-14-128.
10. Chen EY, Xu H, Gordonov S, Lim MP, Perkins MH, Ma'ayan A. 2012. Expression2Kinases: mRNA profiling linked to multiple upstream regulatory layers. Bioinformatics 28:105-111. doi: 10.1093/bioinformatics/btr625.
11. Choi SJ, Marazita ML, Hart PS, Sulima PP, Field LL, McHenry TG, Govil M, Cooper ME, Letra A, Menezes R Narayanan S, Mansilla MA, Granjeiro JM, Vieira AR, Lidral AC, Murray JC, Hart TC. 2009. The PDGF-C regulatory region SNP rs28999109 decreases promoter transcriptional activity and is associated with CL/P. European Journal of Human Genetics: EJHG 17:774-784. doi: 10.1038/ejhg.2008.245.
12. Cochran BH, Reffel AC, Stiles CD. 1983. Molecular cloning of gene sequences regulated by platelet-derived growth factor. Cell 33:939-947. doi: 10.1016/0092-8674(83)90037-5.
13. Corson LB, Yamanaka Y, Lai KM, Rossant J. 2003. Spatial and temporal patterns of ERK signaling during mouse embryogenesis. Development 130:4527-4537. doi: 10.1242/dev.00669.
14. Danielian PS, Muccino D, Rowitch DH, Michael SK, McMahon AP. 1998. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Current biology 8:1323-1326. doi: 10.1016/ S0960-9822(07)00562-3.
15. Ding H, Wu X, Boström H, Kim I, Wong N, Tsoi B, O'Rourke M, Koh GY, Soriano P, Betsholtz C, Hart TC, Marazita ML, Field LL, Tam PP, Nagy A. 2004. A specific requirement for PDGF-C in palate formation and PDGFR-alpha signaling. Nature Genetics 36:1111-1116. doi: 10.1038/ng1415.
16. Fambrough D, McClure K, Kazlauskas A, Lander ES. 1999. Diverse signaling pathways activated by growth factor receptors induce broadly overlapping, rather than independent, sets of genes. Cell 97:727-741. doi: 10.1016/ S0092-8674(00)80785-0.
17. Fantauzzo KA, Soriano P. 2014. PI3K-mediated PDGFRα signaling regulates survival and proliferation in skeletal development through p53-dependent intracellular pathways. Genes & Development 28:1005-1017. doi: 10. 1101/gad.238709.114.
18. Fantauzzo KA, Soriano P. 2015. Receptor tyrosine kinase signaling: regulating neural crest development one phosphate at a time. Current Topics in Developmental Biology 111:135-182. doi: 10.1016/bs.ctdb.2014.11.005.
19. Francavilla C, Rigbolt KT, Emdal KB, Carraro G, Vernet E, Bekker-Jensen DB, Streicher W,Wikström M, SundströmM Bellusci S, Cavallaro U, Blagoev B, Olsen JV. 2013. Functional proteomics defines the molecular switch underlying FGF receptor trafficking and cellular outputs. Molecular Cell 51:707-722. doi: 10.1016/j.molcel.2013.08.002.
20. Gotoh T, Cai D, Tian X, Feig L, Lerner A. 2000. p130(Cas) regulates the activity of AND-34, a novel Ral, Rap1, and R-Ras guanine nucleotide exchange factor. Journal of Biological Chemistry 275:30118-30123. doi: 10.1074/jbc. M003074200.
21. Hamilton TG, Klinghoffer RA, Corrin PD, Soriano P. 2003. Evolutionary divergence of platelet-derived growth factor alpha receptor signaling mechanisms. Molecular and Cellular Biology 23:4013-4025. doi: 10.1128/MCB. 23.11.4013-4025.2003.
22. He F, Soriano P. 2013. A critical role for PDGFRα signaling in medial nasal process development. Plos Genetics 9: e1003851. doi: 10.1371/journal.pgen.1003851.
23. Hoch RV, Soriano P. 2006. Context-specific requirements for Fgfr1 signaling through Frs2 and Frs3 during mouse development. Development 133:663-673. doi: 10.1242/dev.02242.
24. Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols 4:44-57. doi: 10.1038/nprot.2008.211.
25. Hunter T. 2000. Signaling-2000 and beyond. Cell 100:113-127. doi: 10.1016/S0092-8674(00)81688-8.
26. Iwata J, Hacia JG, Suzuki A, Sanchez-Lara PA, Urata M, Chai Y. 2012. Modulation of noncanonical TGF- β signaling prevents cleft palate in Tgfbr2 mutant mice. The Journal of Clinical Investigation 122:873-885. doi: 10.1172/ JCI61498.
27. Kee Y, Bronner-Fraser M. 2005. To proliferate or to die: role of Id3 in cell cycle progression and survival of neural crest progenitors. Genes & Development 19:744-755. doi: 10.1101/gad.1257405.
28. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biology 14:R36. doi: 10.1186/ gb-2013-14-4-r36.
29. Kiss-Toth E, Bagstaff SM, Sung HY, Jozsa V, Dempsey C, Caunt JC, Oxley KM, Wyllie DH, Polgar T, Harte M O'Neill LA, Qwarnstrom EE, Dower SK. 2004. Human tribbles, a protein family controlling mitogenactivated protein kinase cascades. Journal of Biological Chemistry 279:42703-42708. doi: 10.1074/jbc. M407732200.
30. Klinghoffer RA, Hamilton TG, Hoch R, Soriano P. 2002. An allelic series at the PDGFαR locus indicates unequal contributions of distinct signaling pathways during development. Developmental Cell 2:103-113. doi: 10.1016/ S1534-5807(01)00103-4.
31. Lanner F, Rossant J. 2010. The role of FGF/Erk signaling in pluripotent cells. Development 137:3351-3360. doi: 10. 1242/dev.050146.
32. Lau LF, Nathans D. 1987. Expression of a set of growth-related immediate early genes in BALB/c 3T3 cells: coordinate regulation with c-fos or c-myc. Proceedings of the National Academy of Sciences of USA 84: 1182-1186. doi: 10.1073/pnas.84.5.1182.
33. Lemmon MA, Schlessinger J. 2010. Cell signaling by receptor tyrosine kinases. Cell 141:1117-1134. doi: 10.1016/j. cell.2010.06.011.
34. Li C, Scott DA, Hatch E, Tian X, Mansour SL. 2007. Dusp6 (Mkp3) is a negative feedback regulator of FGFstimulated ERK signaling during mouse development. Development 134:167-176. doi: 10.1242/dev.02701.
35. Li L, Sun L, Gao F, Jiang J, Yang Y, Li C, Gu J, Wei Z, Yang A, Lu R, Ma Y, Tang F, Won Kwon W, Zhao Y, Li J, Jin Y. 2010. Stk40 links the pluripotency factor Oct4 to the Erk/MAPK pathway and controls extraembryonic endoderm differentiation. Proceedings of the National Academy of Sciences of USA 107:1402-1407. doi: 10.1073/pnas. 0905657107.
36. Lopez-Bergami P, Huang C, Goydos JS, Yip D, Bar-Eli M, Herlyn M, Smalley KS, Mahale A, Eroshkin A, Aaronson S Ronai Z. 2007. Rewired ERK-JNK signaling pathways in melanoma. Cancer Cell 11:447-460. doi: 10.1016/j.ccr. 2007.03.009.
37. Maeda Y, Tsuji K, Nifuji A, Noda M. 2004. Inhibitory helix-loop-helix transcription factors Id1/Id3 promote bone formation in vivo. Journal of Cellular Biochemistry 93:337-344. doi: 10.1002/jcb.20154.
38. Mansukhani A, Ambrosetti D, Holmes G, Cornivelli L, Basilico C. 2005. Sox2 induction by FGF and FGFR2 activating mutations inhibits Wnt signaling and osteoblast differentiation. The Journal of Cell Biology 168: 1065-1076. doi: 10.1083/jcb.200409182.
39. Marshall CJ. 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signalregulated kinase activation. Cell 2:179-185. doi: 10.1016/0092-8674(95)90401-8.
40. Mendoza MC, Er EE, Blenis J. 2011. The Ras-ERK and PI3K-mTOR pathways: cross-talk and compensation. Trends in Biochemical Sciences 36:320-328. doi: 10.1016/j.tibs.2011.03.006.
41. Miraoui H, Ringe J, Häupl T, Marie PJ. 2010. Increased EFG- and PDGFalpha-receptor signaling by mutant FGFreceptor 2 contributes to osteoblast dysfunction in Apert craniosynostosis. Human Molecular Genetics 19: 1678-1689. doi: 10.1093/hmg/ddq045.
42. Miraoui H, Marie PJ. 2010. Fibroblast growth factor receptor signaling crosstalk in skeletogenesis. Science Signaling 3:re9. doi: 10.1126/scisignal.3146re9.
43. Murphy LO, Smith S, Chen RH, Fingar DC, Blenis J. 2002. Molecular interpretation of ERK signal duration by immediate early gene products. Nature Cell Biology 4:556-564. doi: 10.1038/ncb822.
44. Nakakuki T, Birtwistle MR, Saeki Y, Yumoto N, Ide K, Nagashima T, Brusch L, Ogunnaike BA, Okada-Hatakeyama M, Kholodenko BN. 2010. Ligand-specific c-fos expression emerges from the spatiotemporal control of ErbB network dynamics. Cell 141:884-896. doi: 10.1016/j.cell.2010.03.054.
45. Newbern J, Zhong J, Wickramasinghe RS, Li X, Wu Y, Samuels I, Cherosky N, Karlo JC, O'Loughlin B, Wikenheiser J, Gargesha M, Doughman YQ, Charron J, Ginty DD, Watanabe M, Saitta SC, Snider WD Landreth GE. 2008. Mouse and human phenotypes indicate a critical conserved role for ERK2 signaling in neural crest development. Proceedings of the National Academy of Sciences of USA 105:17115-17120. doi: 10.1073/pnas.0805239105.
46. Ornitz D, Marie P. 2002. FGF signaling pathways in endochondral and intramembranous bone development and human genetic disease. Genes & Development 16:1446-1465. doi: 10.1101/gad.990702.
47. Owens DM, Keyse SM. 2007. Differential regulation of MAP kinase signalling by dual-specificity protein phosphatases. Oncogene 26:3203-3213. doi: 10.1038/sj.onc.1210412.
48. Pawson T. 2004. Specificity in signal transduction: from phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 116:191-203. doi: 10.1016/S0092-8674(03)01077-8.
49. Rattanasopha S, Tongkobpetch S, Srichomthong C, Siriwan P, Suphapeetiporn K, Shotelersuk V. 2012. PDGFRa mutations in humans with isolated cleft palate. European Journal of Human Genetics: EJHG 20:1058-1062. doi: 10.1038/ejhg.2012.55.
50. Raucci A, Bellosta P, Grassi R, Basilico C, Mansukhani A. 2008. Osteoblast proliferation or differentiation is regulated by relative strengths of opposing signaling pathways. Journal of Cellular Physiology 215:442-451. doi: 10.1002/jcp.21323.
51. Santos SD, Verveer PJ, Bastiaens PI. 2007. Growth factor-induced MAPK network topology shapes Erk response determining PC-12 cell fate. Nature Cell Biology 9:324-330. doi: 10.1038/ncb1543.
52. Schmahl J, Raymond CS, Soriano P. 2007. PDGF signaling specificity is mediated through multiple immediate early genes. Nature Genetics 39:52-60. doi: 10.1038/ng1922.
53. Simon MA. 2000. Receptor tyrosine kinases: specific outcomes from general signals. Cell 103:13-15. doi: 10.1016/ S0092-8674(00)00100-8.
54. Soriano P. 1997. The PDGF α receptor is required for neural crest cell development and for normal patterning of the somites. Development 124:2691-2700.
55. Sun C, Bernards R. 2014. Feedback and redundancy in receptor tyrosine kinase signaling: relevance to cancer therapies. Trends in Biochemical Sciences 39:465-474. doi: 10.1016/j.tibs.2014.08.010.
56. Tallquist MD, French WJ, Soriano P. 2003. Additive effects of PDGF receptor β signaling pathways in vascular smooth muscle cell development. Plos Biology 1:288-299. doi: 10.1371/journal.pbio.0000052.
57. Tallquist MD, Soriano P. 2003. Cell autonomous requirement for PDGFRalpha in populations of cranial and cardiac neural crest cells. Development 130:507-518. doi: 10.1242/dev.00241.
58. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology 28:511-515. doi: 10.1038/nbt.1621.
59. Traverse S, Seedorf K, Paterson H, Marshall CJ, Cohen P, Ullrich A. 1994. EGF triggers neuronal differentiation of PC12 cells that overexpress the EGF receptor. Current biology 4:694-701. doi: 10.1016/S0960-9822(00) 00154-8.
60. Trokovic N, Trokovic R, Mai P, Partanen J. 2003. Fgfr1 regulates patterning of the pharyngeal region. Genes & Development 17:141-153. doi: 10.1101/gad.250703.
61. Vasudevan HN, Soriano P. 2014. Article SRF regulates craniofacial development through selective recruitment of MRTF cofactors by PDGF signaling. Developmental Cell 31:332-344. doi: 10.1016/j.devcel. 2014.10.005.
62. Verzi MP, Agarwal P, Brown C, McCulley DJ, Schwarz JJ, Black BL. 2007. The transcription factor MEF2C is required for craniofacial development. Developmental Cell 12:645-652. doi: 10.1016/j.devcel. 2007.03.007.
63. Volinsky N, Kholodenko BN. 2013. Complexity of receptor tyrosine kinase signal processing. Cold Spring Harbor Perspectives in Biology 5:a009043. doi: 10.1101/cshperspect.a009043.
64. Wang C, Chang JY, Yang C, Huang Y, Liu J, You P, McKeehan WL, Wang F, Li X. 2013. Type 1 fibroblast growth factor receptor in cranial neural crest cell-derived mesenchyme is required for palatogenesis. The Journal of Biological Chemistry 288:22174-22183. doi: 10.1074/jbc.M113.463620.
65. Won M, Park KA, Byun HS, Kim YR, Choi BL, Hong JH, Park J, Seok JH, Lee YH, Cho CH, Song IS, Kim YK, Shen HM, Hur GM. 2009. Protein kinase SGK1 enhances MEK/ERK complex formation through the phosphorylation of ERK2: Implication for the positive regulatory role of SGK1 on the ERK function during liver regeneration. Journal of Hepatology 51:67-76. doi: 10.1016/j.jhep.2009.02.027.
66. Wu M, Li J, Engleka KA, Zhou B, Lu MM, Plotkin JB, Epstein JA. 2008. Persistent expression of Pax3 in the neural crest causes cleft palate and defective osteogenesis in mice. The Journal of Clinical Investigation 118:2076-2087. doi: 10.1172/JCI33715.
67. Xian L, Wu X, Pang L, Lou M, Rosen CJ, Qiu T, Crane J, Frassica F, Zhang L, Rodriguez JP, Xiaofeng Jia, Shoshana Yakar, Shouhong Xuan, Argiris Efstratiadis, Mei Wan, Xu Cao. 2012. Matrix IGF-1 maintains bone mass by activation of mTOR in mesenchymal stem cells. Nature Medicine 18:1095-1101. doi: 10.1038/nm.2793.
68. Yamamoto T, Ebisuya M, Ashida F, Okamoto K, Yonehara S, Nishida E. 2006. Continuous ERK activation downregulates antiproliferative genes throughout G1 phase to allow cell-cycle progression. Current Biology 16: 1171-1182. doi: 10.1016/j.cub.2006.04.044.
69. Ying Q-L, Wray J, Nichols J, Batlle-Morera L, Doble B, Woodgett J, Cohen P, Smith A. 2008. The ground state of embryonic stem cell self-renewal. Nature 453:519-523. doi: 10.1038/nature06968.