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Involvement in Endoreduplication (Cell Cycle/Repa/Wheat Dwarf Virus) GIDEON GRAFI*T#, RONALD J

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Involvement in Endoreduplication (Cell Cycle/Repa/Wheat Dwarf Virus) GIDEON GRAFI*T#, RONALD J Proc. Natl. Acad. Sci. USA Vol. 93, pp. 8962-8967, August 1996 Cell Biology A maize cDNA encoding a member of the retinoblastoma protein family: Involvement in endoreduplication (cell cycle/RepA/wheat dwarf virus) GIDEON GRAFI*t#, RONALD J. BURNETTr*, TIM HELENTJARIS*, BRIAN A. LARKINS*§, JAMES A. DECAPRIOt, WILLIAM R. SELLERSt, AND WILLIAM G. KAELIN, JR.t *Department of Plant Sciences, University of Arizona, Tucson AZ 85721; and tDana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02115 Contributed by Brian A. Larkins, May 14, 1996 ABSTRACT Retinoblastoma (RB-1) is a tumor suppres- We identified a partial maize cDNA (ZmRB) that is pre- sor gene that encodes a 105-kDa nuclear phosphoprotein. To dicted to encode a protein with homology to members of the date, RB genes have been isolated only from metazoans. We pocket protein (Rb) family. Here we provide evidence that have isolated a cDNA from maize endosperm whose predicted ZmRb is a member of the retinoblastoma protein family and protein product (ZmRb) shows homology to the "pocket" A demonstrate its ability to bind the replication-associated pro- and B domains of the Rb protein family. We found ZmRb tein WDV RepA and its involvement in the process of DNA behaves as a pocket protein based on its ability to specifically endoreduplication during maize endosperm development. interact with oncoproteins encoded by DNA tumor viruses (E7, T-Ag, E1A). ZmRb can interact in vitro and in vivo with MATERIALS AND METHODS the replication-associated protein, RepA, encoded by the wheat dwarf virus. The maize Rb-related protein undergoes Plant Materials and Chemicals. Maize (Zea mays L.) ker- changes in level and phosphorylation state concomitant with nels from various developmental stages of an inbred developed endoreduplication, and it is phosphorylated in vitro by an from pool 33 QPM were obtained from plants grown at the S-phase kinase from endoreduplicating endosperm cells. To- University of Arizona. DNA and protein-modifying enzymes gether, our results suggest that ZmRb is a representative ofthe were purchased from BRL, New England Biolabs, or Boehr- pocket protein family and may play a role in cell cycle inger Mannheim, unless otherwise indicated. progression. Moreover, certain plant monopartite geminivi- cDNA Library and Plasmids. An endosperm (18 days after ruses may operate similarly to mammalian DNA viruses, by pollination) cDNA library in A-ZAPII was screened with the targeting and inactivating the retinoblastoma protein, which Rb-related clone 6C02C02 (14) to isolate ZmRB. ZmRB, otherwise induces G1 arrest. which encodes the pocket region of the maize protein (1-458, see Fig. 1A), was amplified by PCR with a sense primer Retinoblastoma (RB-1) is a tumor suppressor gene that en- containing a BamHI site and in frame ATG start codon codes a nuclear phosphoprotein with a molecular mass of (5'-GCCGGATCCCATATGCCGTGGGCAGAAGCCAG-3') about 105 kDa (1, 2). Inactivation of the RB-1 gene contributes and an antisense primer containing an EcoRI site (5'- to both familial and sporadic forms of cancer (3). Retinoblas- GGAATTCGCCTTCACCAATGCATGC-3') using Pfu toma and its related p107 and p130 proteins are among the DNA polymerase (Stratagene). The amplified DNA fragment negative regulators of the cell cycle (4, 5). While hypophos- was subcloned into the BamHI/EcoRI sites of either pBlue- phorylated, the Rb protein exerts a growth suppressive effect script SKI (Stratagene), pGEX-2TK (Pharmacia; ref. 15), or and arrests cells in G1 phase. pSG5 (Invitrogen) modified by Ralph Scully (Dana-Farber Hyperphosphorylation of Rb, or its interaction with viral Cancer Institute) to contain the hemagglutinin epitope with oncoproteins, prevents Rb from performing its normal func- Ncol, HindIII, SmaI, and Sall upstream and BamHI, EcoRI, tions at G1 phase and enables cells to begin DNA synthesis (6). EcoRV, andXhol restriction sites downstream. Introduction of One function of Rb appears to be an interaction with and a C to G mutation to generate ZmRB706G was performed inactivation of transcriptional factors, such as the E2F protein with a mutagenic primer (CGATCAACTTATCCTTgGCTG- family, that are required for the expression of genes involved TCTTTATGGTGTTGC) using a Transformer Site Directed in G1-S transition (7). The product of the RB gene, pRb, as Mutagenesis Kit (Clontech) and confirmed by DNA sequenc- well as its related p107 and p130 proteins, contains a "pocket" ing. HuZmRB is a hybrid molecule containing the human Rb region required for binding with cellular proteins, as well as A domain (379-602) and the maize Rb B domain (251-458; with oncoproteins encoded by DNA tumor viruses (8, 9). The see Fig. 1A). To generate the hybrid molecule, the human RB pocket region contains two functional domains, A and B, with cDNA corresponding to the large pocket region (379-928) in an intervening spacer. Certain cellular proteins, as well as viral pBluescript SKI was cleaved with BglII and EcoRI to remove oncoproteins, interact with Rb through a domain containing the B domain and C-terminal region. The ZmRB B domain the core sequence LxCxE (10). This binding motif is found in was amplified by PCR using 5'-AGGGCCGGATCCATGG- plant D-type cyclins (B-cyclins; refs. 11 and 12) and in several AGTCCACATTTGCAAG-3' as the sense BamHI primer and replication-associated proteins encoded by single-stranded the above antisense EcoRI primer. The PCR product was DNA monopartite geminiviruses (13). Among them is the digested with BamHI and EcoRI and subcloned into the RepA protein encoded by wheat dwarf virus (WDV), which BglII/EcoRI site of pBluescript carrying the human Rb A has recently been shown to interact with the Rb-related p130 protein. The LxCxE motif in RepA was found to be required Abbreviations: WDV, wheat dwarf virus; GST, glutathione-S- for efficient replication of the virus (13). transferase; CDK, cyclin-dependent kinase; DAP, day after pollination. Data deposition: The sequence reported in this paper has been deposited in the GenBank data base (accession no. U52099). The publication costs of this article were defrayed in part by page charge VPresent address: Department of Plant Genetics, The Weizmann payment. This article must therefore be hereby marked "advertisement" in Institute of Science, Rehovot 76100, Israel. accordance with 18 U.S.C. §1734 solely to indicate this fact. §To whom reprint requests should be addressed. 8962 Downloaded by guest on September 27, 2021 Cell Biology: Grafi et al. Proc. Natl. Acad. Sci. USA 93 (1996) 8963 domain. To generate pGEM-RepA, an NcoI-NdeI fragment and B domains (Fig. 1B). Furthermore, four conserved amino containing the WDV RepA coding region and part of the acid residues in ZmRb are also sites of naturally occurring pRb N-terminal region of the WDV RepB protein was excised from mutations (arrowheads Fig. 1B, Ala-562, Ser-567, Arg-661, and pWI-II (kindly provided by J. Messing; ref. 16) and inserted Cys-706; refs. 22-25). Therefore, it appeared that ZmRB might into the NcoI-NdeI sites of the pGEM-5Zf vector (Promega) also encode a pocket protein. The ZmRB gene maps to the long and used as a template in a coupled transcription/translation arm of chromosome 2, and its simple hybridization pattem reaction (TNT; Promega). To produce glutathione-S-transferase suggests that there is only one gene (data not shown). (GST)-RepA protein, the RepA DNA fragment was also inserted ZmRb Specifically Interacts with Oncoproteins Encoded by into BamHI-SmaI sites of pGEX-2TK. The human RB small Mammalian DNA Tumor Viruses. A diagnostic feature of pocket (379-792; HuRBsp) and human RB point mutant (C706 pocket proteins is their ability to interact with viral oncopro- to F, HuRB706F) were previously described (8). teins via a short motif with the core sequence LxCxE (10). We Antibodies, Immunodetection and Immunoprecipitation. A investigated whether ZmRb has properties of a pocket protein monoclonal antibody (mAb) was raised against bacterially by testing its ability to interact with the E7 oncoprotein produced GST-ZmRb by standard procedures (17). Superna- encoded by papillomavirus. Various plasmids were con- tants from growing hybridoma cell cultures were the source for structed (Fig. 2A): pZmRB contains the wild-type sequence ZmRb mAb (2E5) and that for the hemagglutinin epitope and pZmRB706G is a mutated form in which the cysteine at (12CA5) (18). Kernels were homogenized with NETN (20 mM the position corresponding to residue 706 of human Rb was Tris HCl, pH 8.0/100 mM NaCl/1 mM EDTA/0.5% Nonidet converted to glycine. A naturally occurring mutation at this P-40) buffer containing 87 mM NaF, 2 mM sodium orthovana- position renders human Rb incapable of interacting with date, 5 ,tg of aprotinin per ml, and 5 ,ug of leupeptin per ml. oncoproteins (23). pHuZmRB is a hybrid molecule containing Samples were cleared by centrifugation, aliquotted and stored the human Rb A domain and ZmRb B domain which was at -80°C. The various RB and RepA constructs were used as constructed to address the question of evolutionary conser- templates in the TNT system and proteins were labeled with vation between plant and animal pocket proteins. As a positive [35S]methionine. Two microliters of each TNT reaction, or control we used the pocket region of human Rb (HuRBsp) total protein extract (1 mg), was mixed with 50 ,ul of protein which is known to interact with E7, and as a negative control A-Sepharose (50% slurry) and 100 gl (tissue culture super- we used the mutant HuRB706F (Cys-706 -> Phe; ref. 23). natant) of the indicated mAb and incubated in NETN buffer at Plasmids were used as templates in a coupled transcription/ 4°C for 2-12 h with gentle shaking. The Sepharose was washed translation system to produce the various 35S-labeled proteins five times with NETN buffer, and bound proteins were either (Fig.
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