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1 SUPPLEMENTARY INFORMATION doi:1.138/nature1237 a b retinol retinal RA OH RDH (retinol dehydrogenase) O H Raldh2 O R/R (retinaldehyde dehydrogenase 2) RA retinal retinol Concentration (nm) 1 1 OH Cyp26 (cytochrome P45 26) Supplementary Figure 1 a, Metabolism (synthesis and degradation) of RA. b, 1
2 RESEARCH SUPPLEMENTARY INFORMATION Animal pole Head time hpf Vegetal pole Tail %-epiboly bud hindbrain r3/r4 r4/r5 r6/r7 somites 3S 6S 1S 14S 18S Supplementary Figure 2 Hindbrain posteriorization and somitogenesis of zebrafish embryos at 28 C. Anteriorly gradating RA concentrations from the raldh2-expressing paraxial mesoderm posterior to the hindbrain to the cyp26a1-expressing animal pole in the presumptive forebrain and midbrain are thought to provide positional information that specifies the locations and fates of rhombomeres during gastrulation (indicated in orange). After initiation of somite formation, the posteriorly gradating RA concentrations from the raldh2-expressing anterior presomitic mesoderm and somites to the cyp26a1-expressing tail bud are thought to control paraxial mesoderm differentiation, including somitogenesis (indicated in green). r, rhombomere; S, somite. 2
3 SUPPLEMENTARY INFORMATION RESEARCH Supplementary Figure 3 a RARβ donor acceptor R/R b donor acceptor RARγ R/R Venus Venus CFP YPet 4 cp49venus 4, 41 CyPetT65S 11 YPet 4 cp51venus CFP YPet 4 cp52venus CFP , 42 cp155ypet cp53venus CFP CFP CyPet 11 4 CFP , 41 CFP4T65S 11 4, 41 CFP4T65S 11 4, 42 cp172ypet 4, 42 cp173ypet cp174venus 4, 42 4, 42 YPet 4 GEPRA-B 4, 42, 43 (EAAAR)3cp49Venus cp17venus cp171venus cp172venus cp173venus cp174venus cp175venus cp176venus Cerulean cp174venus, 43 (EAAAR)3cp172Venus, 43 (EAAAR)3cp173Venus, 43 (EAAAR)3cp174Venus 4, 42 cp172ypet 4, 42 CyPet , 42 CFP , 42 CyPet 4 4, 42 4, 41 CFP4T65S 11 4, 42 cp195venus GEPRA-G cp229venus Supplementary Figure 3 a b). The LBD was sandwiched between various pairs of CFP and YFP mutants of Aequorea green fluorescent protein as the FRET donor and acceptor, respectively. The C-terminal truncation of CFP and the N-terminal truncation of YFP are indicated. The responses of the chimeras in HeLa cells in the presence of 1 nm RA are shown as bar graphs. 3
4 RESEARCH SUPPLEMENTARY INFORMATION 1 nm RA.65 Ratio (CFP/FRET) Time (min) Supplementary Figure 4 A typical time course of the GEPRA-B ratio (CFP/FRET) in HeLa cells after applying 1 nm RA to the medium. After application, GEPRA-B responded rapidly and the response reached a plateau in approximately 1 minutes. 4
5 SUPPLEMENTARY INFORMATION RESEARCH a.6.5 Ratio Concentration (nm) b 3S.5 1st somite S RA (GEPRA-AA) Ratio , Distance (µm, head ~ tail) Supplementary Figure 5 The low-affinity GEPRA-AA RA probe. GEPRA-AA was generated by introducing two amino-acid substitutions (R269A and S28A) in the LBD of GEPRA-B. These mutations decreased the affinity of the fusion proteins for RA 32. a, A dose-response curve for GEPRA-AA. HeLa cells expressing GEPRA-AA were imaged using a confocal microscope. Fitting with the Michaelis-Menten equation resulted in an apparant dissociation constant of 5 nm for RA. Each data point is the mean ± SD from nine experiments. b, left, A FRET ratio image (lateral view) of a 3-somite embryo transiently expressing GEPRA-AA. Scale bar, right, The FRET ratio profile (from the head to tail) of the imaged embryo. The locations of the first and newly formed (S) somites are shown. 5
6 RESEARCH SUPPLEMENTARY INFORMATION a control 3S 1 µm DEAB 3S.5 b.5 control RA (GEPRA-B) Ratio.4 DEAB 5 1, Distance (µm, head ~ tail) Supplementary Figure 6 a, FRET ratio images of a control embryo (left) and a DEAB-treated embryo (right). Embryos were first treated b, 6
7 SUPPLEMENTARY INFORMATION RESEARCH Supplementary Figure 7 a b Initial condition anterior Sink (Cyp26s) presumptive hindbrain Sink Source posterior Source (RALDH2) anterior x1 c D =.1 µm 2 /sec x2 posterior c 2 t = D c x 2 initial conditions c = (x = x1) D = 1 µm 2 /sec t =, 1, 2, 3 min boundary conditions c = (x = x1) c = 1 (x = x2) D = 1 µm 2 /sec 1 µm Supplementary Figure 7 Computer simulation of the [RA] i distribution in a gap between RA-synthesizing (source) and RA-degrading (sink) regions. The diffusion coefficient of a retinoid in the chick limb was previously determined to be 2 /s (ref. 2). a, Schematic of the presumptive hindbrain in which the simulation was modeled. b, The initial condition, which included a rectangular distribution of RA. c, Simulation results with various diffusion coefficients. Traces at min (red), 1 min (green), 2 min (blue), and 3 min (purple) are shown. 7
8 RESEARCH SUPPLEMENTARY INFORMATION a Time (hour) S 8S 12S 18S 21S 26S Phase contrast RARE - EYFP b RARE-EYFP GEPRA-B.5 raldh2 cyp26s 2S 2S 2S 2S c Supplementary Figure 8 a, A series of phase contrast (top) and fluorescence (bottom) images of an embryo from the RARE-EYFP transgenic line. Images were acquired using a confocal microscope (FV1i, Olympus) equipped with a 1 objective lens (UPlanSApo 1 /.4 air equivalent) and a 473-nm laser. The signal was detectable at later than the 18-somite stage (white double-headed arrows). b, RA signaling (left) and [RA] i imaging (right) using 2-somite embryos from the RARE-EYFP and GEPRA-B transgenic zebrafish lines. The RARE-EYFP signal is indicated by a white double-headed arrow. c, In situ hybridization results for raldh2 (left) and cyp26s (right) at the 2-somite Exogenous observation of RA signalling (RARE-EYFP) and endogenous quantitation of [RA] i (GEPRA) are different biological properties and should be discussed separately. RA-based gene expression is the result of a cascade of complex regulatory processes involving multiple RA-dependent transcription factors, which could result in nonlinear spatial profiles. This, of course, cannot be taken as evidence against a linear [RA] i gradient. Although it is not inherently fluorescent, LacZ matures more quickly than EYFP. Thus, a RARE-LacZ system may be more useful, particularly in mice 45 47, which develop more slowly than fish. 8
9 SUPPLEMENTARY INFORMATION RESEARCH RA (GEPRA-B) bud.5 otx2 / myod otx2 myod Supplementary Figure 9 The hindbrain region was identified by in situ hybridization analysis using otx2- and myod-specific probes (right) after an [RA] i 9
10 RESEARCH SUPPLEMENTARY INFORMATION Supplementary Figure 1 RA in ~3-somite stage Morphology at 36 hpf Control 1 µm DEAB 1 µm DEAB 1 nm RA 1 µm DEAB 1 nm RA Summary Ratio Distance (µm, head ~ tail) (1st somite = ) Control 1 nm RA + 1 µm DEAB 1 nm RA + 1 µm DEAB 1 µm DEAB Supplementary Figure 1 Correlation between the distribution of [RA] i at approximately the 3-somite stage (left) and overall morphology at 36 hpf (right) in DEAB and various concentrations of RA. bottom, [RA] i traces are overlaid with the first somites centered in the plot. The presumptive hindbrain region is shaded. In the transmission images, kinked heads are indicated by red 1
11 SUPPLEMENTARY INFORMATION RESEARCH a Time (hour) S 6S 8S 9S 12S 14S 16S Transmission.5 RA (GEPRA-B).6 Ratio.4 1, 2, Distance (µm, head ~ tail) b Time (hour) S 7S 1S 12S 15S Transmission c Time (hour) Transmission RA (GEPRA-G) Ratio.6.4 1, Distance (µm, head ~ tail) S 18S 2S 23S 24S 27S 28S 3S.45 RA (GEPRA-B) Ratio µm 1,5 Distance (µm, head ~ tail) Supplementary Figure 11 [RA] i gradients during somitogenesis. a, b, Early somitogenesis stages. Time-lapse [RA] i imaging in a GEPRA-B bearing embryo from the 3-somite to 16-somite stage (a) and of a GEPRA-G bearing embryo from the 5-somite to 15-somite stage (b). c, Late somitogenesis stages. Time-lapse [RA] i imaging in a GEPRA-B bearing embryo from the 16-somite to 3-somite stage. A series of transmission images (top row), [RA] i images (middle row), and ratio profiles (bottom row) are shown. The position of the somitogenesis front (S) is indicated by a red arrowhead in each image. The most anterior and most posterior points represented in the ratio profiles are indicated in the transmission images by cyan and green dots, respectively. Times (h) after the start of imaging are shown above the images. All images are lateral views. 11
12 RESEARCH SUPPLEMENTARY INFORMATION Transmission 6S RA (GEPRA-B).5 gir homozygous 6S.5 WT Supplementary Figure 12 Comparison of the [RA] i distributions in wild type (WT) and cyp26a mutant (gir) embryos that had received injections of GEPRA-B mrna. A cyp26a homozygous mutant (top, 6-somite stage) exhibited globally high signals representing [RA] i. Each embryo was lysed after imaging and genotyped as previously described
13 SUPPLEMENTARY INFORMATION RESEARCH Control MO krox2 hoxd4 r3r5 r7,r8 fgf8 MO krox2 hoxd4 r3r5 r7,r8 Supplementary Figure 13 Comparative in situ hybridization showing krox2 (r3 and r5) and hoxd4 (r7 and r8) expression at 17 hpf in 9 embryos injected with control MO (top) and in 7 embryos injected with fgf8-specific MO (bottom). A bulge in the area of the developing midbrain in each embryo injected with the fgf8-specific MO is 13
14 RESEARCH SUPPLEMENTARY INFORMATION References for Supplementary Information 38. ECFP-K27R, H164N, S175G 39. Nagai, T. et al. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nature Biotechnol. 2, 87-9 (22) 4. Nguyen, A. W. & Daugherty, P. S. Evolutionary optimization of fluorescent proteins for intracellular FRET. Nature Biotechnol. 23, (25) 41. Goedhart, J. et al. Bright cyan fluorescent protein variants identified by fluorescence lifetime screening. Nature Methods 7, (21) 42. Nagai, T., Yamada, S., Tominaga, T., Ichikawa, M. & Miyawaki, A. Expanded dynamic range of fluorescent indicators for Ca 2+ by circularly permuted yellow fluorescent proteins. Proc. Natl. Acad. Sci. USA., 11, (24) 43. Sato, M., Ueda, Y., Takagi, T. & Umezawa, Y. Production of PtdInsP 3 at endomembranes is triggered by receptor endocytosis. Nature Cell Biol. 5, (23) 44. Rizzo, M. A., Springer, G. H., Granada, B. & Piston, D. W. An improved cyan fluorescent protein variant useful for FRET. Nature Biotechnol. 22, (24) 45. Rossant, J., Zirngibl, R., Cado, D., Shago, M. & Giguére, V. Expression of a retinoic acid response element-hsplacz transgene defines specific domains of transcriptional activity during mouse embryogenesis. Genes Dev. 5, (1991) 46. Vihais-Neto, G. C. et al., Rere controls retinoic acid signaling and somite bilateral symmetry. Nature 463, (21) 47. Sirbu, I. O. & Duester, G. Retinoic-acid signaling in node ectoderm and posterior neural plate directs left-right patterning of somatic mesoderm. Nat. Cell Biol. 8, (26) 14
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