Bonner MK , Haase J , Swinderman J , Halas H , Miller Jenkins LM , Kelly AE .

             kinase activity
             kinetochore assembly

	Figure 1. Outer kinetochore assembly is completely dependent on the phosphorylation of Dsn1 by Aurora B in Xenopus egg extracts. (A) Alignment of the Dsn1 autoinhibitory basic region from indicated species showing conserved Aurora B phosphorylation sites. (B) Schematic of kinetochore assembly experiments in Xenopus egg extract. Sperm chromatin was added to WT or ΔCPC CSF extract. To express mutants, recombinant protein or mRNA was added to CSF extract at this point. Here, shown in green, mRNA was added to express the Mis12C or its variants (Mis12CDsn1EE/S77E/S84E), composed of Nsl1, Mis12, Pmf1, and Dsn1-LAP. For all figures, unless recombinant (r) protein is noted in text or figure legend, all mutants were expressed from mRNA. Calcium chloride was added to cycle extract into interphase. After 90 min, 2× volume CSF extract (WT or ΔCPC) was added to cycle the extract into metaphase in addition to drugs shown in red. After a total of 135 min, samples were taken for immunofluorescence and Western blots. (C) Representative immunofluorescence images of replicated chromosomes in WT Xenopus metaphase extracts with the Mis12C expressed from mRNA in extracts and treated with hesperadin in indicated conditions. Chromosomes were stained for Ndc80 and Dsn1. (D) Quantification of fluorescence intensity of Ndc80 on replicated chromosomes in metaphase extracts in indicated conditions shown in C, normalized to WT. n = 96 kinetochores. Error bars represent SD unless otherwise noted, and asterisks indicate a statistically significant difference (*, P < 0.001). A.U., arbitrary units. (E) Western blot for Dsn1-LAP, histone H3 phosphorylation (H3S10ph), and tubulin for samples shown in C and D.
	Figure 2. The central region of INCENP is required for kinetochore assembly. (A) Quantification of fluorescence intensity of Dsn1 and H3S10ph on replicated chromosomes in WT or CPC-depleted (ΔCPC) metaphase extracts with indicated CPC conditions, normalized to WT. Purified, preactivated, recombinant (r) Strep-INbox–His6-Aurora B was added to ΔCPC extract at 2.65 µM. Samples contained 33 µM nocodazole. n = 96 kinetochores for Dsn1, and n = 50 spindles for H3S10ph. A.U., arbitrary units. (B) Mean integrated fluorescence intensity of Dsn1 was quantified at indicated percentage mixture of CPC-depleted and mock-depleted extracts and normalized to mock-depleted levels (WT; 100% CPC). Estimated CPC concentration is indicated. Solid line represents fit to the Hill equation. n = 50 kinetochores per condition. Error bars represent SEM. (C) Western blot for INCENP, Aurora B phosphorylation (T248ph), and tubulin for samples shown in B. WT extract was mixed with CPC-depleted (ΔCPC) extract at various concentrations to determine how much CPC was necessary to enable outer kinetochore assembly. CPC-depleted extracts with >1% CPC remaining led to detectable kinetochore assembly. (D) Schematic of INCENP constructs used in this study. These constructs were expressed from mRNA in extracts, along with full-length Borealin, Survivin, and Aurora B, to reconstitute ΔCPC extracts, unless otherwise noted. To achieve full activation of Aurora B kinase when expressing mRNAs lacking the CEN domain, either beads bound with anti-INCENP antibodies or substoichiometric amounts of clustering anti-INCENP antibodies were added. Extent of Dsn1 assembly at kinetochores for each condition is indicated. (E) Quantification of fluorescence intensity of Dsn1 on replicated chromosomes in mock-depleted (WT) and ΔCPC metaphase extracts with indicated CPC conditions with anti-INCENP antibody added where specified, normalized to WT. n = 96 kinetochores. Error bars represent SD. *, P < 0.001. (F) Initial rate of chemosensor phosphorylation by indicated preactivated recombinant GST-INCENP–His6-Aurora B complexes as a function of chemosensor concentration. Solid lines represent fit by the Michaelis–Menten equation. Graphs represent data from two independent experiments. Error bars represent SEM. (G) Representative immunofluorescence images of replicated chromosomes in WT and ΔCPC metaphase extracts reconstituted with indicated CPC condition, preactivated recombinant GST-INCENP328–871–His6-Aurora B or preactivated recombinant GST-INbox–His6-Aurora B, and treated with nocodazole. Chromosomes were stained for Dsn1 or histone H3S10ph. (H) Quantification of fluorescence intensity of Dsn1 and H3S10ph on replicated chromosomes in WT or ΔCPC metaphase extracts reconstituted with indicated CPC conditions shown in G, normalized to WT. n = 50 kinetochores per condition. Error bars represent SD.
	Figure 3. The SAH domain of INCENP is critical for kinetochore assembly. (A) Representative immunofluorescence images of replicated chromosomes in WT and ΔCPC metaphase extracts reconstituted with CPC containing the indicated INCENP construct with anti-INCENP antibody added for the INCΔCEN sample to ensure kinase activation. Samples contained 33 µM nocodazole. Chromosomes were stained for Dsn1 and Ndc80. (B) Quantification of fluorescence intensity of Dsn1 on replicated chromosomes in WT or ΔCPC metaphase extracts reconstituted with indicated CPC conditions shown in A, normalized to WT. n = 96 kinetochores per condition. A.U., arbitrary units. (C) Representative IF images of replicated chromosomes in WT and ΔCPC metaphase extracts reconstituted with CPC containing the indicated INCENP construct and recombinant Mis12CDsn1EE as indicated. Chromosomes were stained for Ndc80, Dsn1, and Ndc80 phosphorylation (Ndc80S40ph). (D) Quantification of fluorescence intensity of Ndc80S40ph on replicated chromosomes in WT or ΔCPC metaphase extracts reconstituted with indicated CPC conditions shown in C, normalized to WT. n = 96 kinetochores per condition. (E) Quantification of fluorescence intensity of Ndc80 in WT and ΔCPC metaphase extracts with indicated CPC conditions and anti-INCENP antibody added to the INbox sample, treated as indicated with I-2, and normalized to WT. n = 96 kinetochores per condition. (F) Representative immunofluorescence images of replicated chromosomes in WT and ΔCPC metaphase extracts with indicated CPC conditions, treated as indicated with hesperadin. Chromosomes were stained for Ndc80 (kinetochore pairs indicated with green boxes) and FLAG (for 3XFLAG-INbox-Nsl1 construct; kinetochore pairs indicated with magenta boxes). The inset white boxes show a merged, 3X zoom image of colocalization of Ndc80 (green) and FLAG (magenta). (G) Quantification of fluorescence intensity of Ndc80 shown in F, normalized to WT. n = 96 kinetochores per condition. Error bars represent SD. *, P < 0.001.
	Figure 4. The central region promotes Dsn1 phosphorylation by Aurora B. (A) In vitro kinase assay for Dsn1 phosphorylation. Purified Xenopus recombinant (r) Mis12C was incubated with preactivated recombinant GST-INbox–His6-Aurora B kinase or recombinant GST-INC328-871–His6-Aurora B for the indicated times, and phosphorylation was assessed by Western blot (WB) using a phospho-specific antibody to Ser77 of Dsn1. (B) Quantification of kinase assay for Dsn1 phosphorylation shown in A. A.U., arbitrary units. (C) In vitro kinase assay for histone H3 phosphorylation (H3S10ph). Purified Xenopus recombinant H3–H4 was incubated with preactivated recombinant GST-INbox–His6-Aurora B kinase or recombinant GST-INC328-871–His6-Aurora B for the indicated times, and phosphorylation was assessed by Western blot using a phospho-specific antibody for H3S10ph. (D) Quantification of kinase assay for H3S10 phosphorylation shown in C. (E) Western blot for phosphorylation of Dsn1 in samples of immunoprecipitated (IP) recombinant Mis12Dsn1-LAP complex from WT and ΔCPC metaphase extracts, in indicated CPC conditions, in the presence of nocodazole, okadaic acid, and hesperadin as specified. Normalized phosphorylation levels are indicated below. (F) Western blot for phosphorylation of Dsn1 in samples of immunoprecipitated Mis12Dsn1-LAP complex expressed from mRNAs in ΔCPC metaphase extracts, in indicated CPC conditions. Recombinant GST-INbox–His6-Aurora B or recombinant GST-INC328–871–His6-Aurora B were activated with anti-INCENP beads in the presence of nocodazole and I-2. (G) Quantification of phosphorylation of Dsn1 from samples shown in C, normalized to GFP.
	Figure 5. The CPC promotes kinetochore assembly only at kinetochore-bound CENP-C. (A) Schematic of soluble Dsn1 Assay to test if Mis12C phosphorylated away from chromatin promotes kinetochore assembly (see Fig. S5 C and Materials and methods for more details). In brief, Aurora B was activated by anti-INCENP beads in CSF extract lacking chromosomes and given time to phosphorylate Mis12C. Kinase and phosphatase inhibitors were added to preserve the phosphorylation state of Mis12C, and beads were then removed. This extract, containing soluble phosphorylated Mis12C, was then added to interphase extract containing Aurora B inhibitors and chromatin to drive the reaction into metaphase. Positive and negative control reactions are indicated with blue and red, respectively. (B) Representative immunofluorescence images of replicated chromosomes from the soluble Dsn1 assay outlined in A. Chromosomes were stained for Ndc80. (C) Quantification of fluorescence intensity of Ndc80 for samples in Soluble Dsn1 assay, normalized to WT. n = 96 kinetochores per condition. A.U., arbitrary units. (D) Schematic of kinetochore assembly experiment to test whether CENP-C can be incorporated at kinetochores when added at different points in the cell cycle. CENP-C–3XFLAG from an in vitro translation reaction was added at the beginning of interphase, at the beginning of metaphase (T 90’), and at 115 min. Samples were fixed for immunofluorescence staining at 135 min. (E) Representative IF images of replicated chromosomes in WT extracts with CENP-C–3XFLAG added to extract at indicated time points. Chromosomes were stained for Ndc80 (kinetochore pairs indicated with green boxes) and FLAG (kinetochore pairs indicated with magenta boxes). The inset white boxes show a merged, 3× zoom image of colocalization of Ndc80 (green) and FLAG (magenta) for each time point. (F) Quantification of fluorescence intensity of CENP-C–3XFLAG shown in E, normalized to the T 0’ condition. n = 96 kinetochores per condition. (G) Western blot for FLAG, histone H3 phosphorylation (H3T3ph and H3S10ph), and tubulin for samples shown in E and F. Asterisk denotes CENP-C–3XFLAG band, under the background band. Error bars represent SD. *, P < 0.001.
	Figure 6. Mis12C assembly requires enrichment of Aurora B at inner kinetochores. (A) Representative immunofluorescence images of replicated chromosomes in WT and ΔCPC metaphase extracts with indicated CPC conditions, treated as indicated with I-2 and hesperadin. Chromosomes were stained for Ndc80 and FLAG (for 3XFLAG-INbox–CENP-N construct). White inset boxes show a merged, 3× zoom image of colocalization of Ndc80 (green) and 3XFLAG-INbox–CENP-N (magenta). (B) Quantification of fluorescence intensity of Ndc80 shown in A, normalized to WT. n = 96 kinetochores per condition. A.U., arbitrary units. (C) Western blot for FLAG, histone H3 phosphorylation (H3S10ph), and tubulin for samples shown in A and B. Error bars represent SD. *, P < 0.001.
	Figure 7. Autoinhibition of the Mis12C impedes the phosphorylation of Dsn1 by Aurora B. (A) In vitro kinase assay for Dsn1 phosphorylation. Purified recombinant (r) Mis12C was incubated with preactivated recombinant GST-INbox–His-Aurora B in the presence or absence of recombinant CENP-C2–55–LAP for the indicated times. Western blot shows Dsn1ph, Aurora B T248ph, and Mis12 at indicated time points of assay. (B) Quantification of Dsn1 phosphorylation data from in vitro kinase assay shown in A. A.U., arbitrary units. (C) Quantification of Dsn1 phosphorylation over time used to calculate initial rates. Purified recombinant Mis12C was incubated with preactivated recombinant GST-INbox–His6-Aurora B and indicated concentrations of recombinant CENP-C2–55–LAP. (D) Quantification of initial rates of Dsn1 phosphorylation calculated from data shown in C. Purified recombinant Mis12C was incubated with preactivated recombinant GST-INbox–His6-Aurora B and indicated concentrations of recombinant CENP-C2–55–LAP. Graph represents data from two independent experiments. Error bars represent SEM.
	Figure 8. The SAH domain is required for the SAC independently of its roles in kinetochore assembly and microtubule binding. (A) Representative immunofluorescence images of replicated chromosomes in WT and ΔCPC metaphase extracts with indicated CPC conditions, treated with 33 µM nocodazole and recombinant (r) Mis12CDsn1EE as specified. Chromosomes were stained for BubR1 or Mad2. (B and C) Quantification of fluorescence intensity of BubR1 and Mad2 shown in A normalized to WT. n = 96 kinetochores. A.U., arbitrary units. (D) Western blot for global checkpoint assay for INCENP, histone H3 phosphorylation (H3T3ph and H3S10ph), and tubulin. WT or ΔCPC metaphase extracts with indicated CPC conditions were incubated with sperm nuclei and then challenged with the addition of calcium chloride. Samples were taken at indicated time points after calcium addition, shown with representative images of chromatin morphology at the end of the assay. Error bars represent SD. *, P < 0.001.
	Figure 9. Kinetochore-localized Aurora B is required for kinetochore assembly and function. (A) Mis12C autoinhibition prevents phosphorylation by Aurora B. Away from kinetochores, the autoinhibited form of the Mis12C (orange spheres) predominates and prevents Aurora B phosphorylation of Dsn1 through burial of Dsn1S77. (B) Model for kinetochore assembly through the cooperative actions of CENP-C, the INCENP central region, and Aurora B. At the inner kinetochore, the Mis12C transiently binds to prebound CENP-C (and likely CENP-T) molecules, which relieves Mis12C autoinhibition and exposes the Dsn1 tail. In early mitosis, Aurora B is enriched at inner kinetochores by the central region of INCENP. This high local concentration of Aurora B rapidly phosphorylates the exposed Dsn1 tail to prevent dissociation of the Mis12C. Thus, the coincidence of CENP-C and the CPC at inner kinetochores stabilizes the Mis12C–CENP-C interaction to drive outer kinetochore assembly. Our data indicate that enrichment of Aurora B at the inner kinetochore is also involved in SAC signaling through the phosphorylation substrates other than Dsn1.

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