Literature DB >> 26216878

Divergent roles of CAAX motif-signaled posttranslational modifications in the regulation and subcellular localization of Ral GTPases.

Leanna R Gentry1, Akiyuki Nishimura2, Adrienne D Cox3, Timothy D Martin1, Denis Tsygankov1, Motohiro Nishida2, Timothy C Elston1, Channing J Der4.   

Abstract

The Ras-like small GTPases RalA and RalB are well validated effectors of RAS oncogene-driven human cancer growth, and pharmacologic inhibitors of Ral function may provide an effective anti-Ras therapeutic strategy. Intriguingly, although RalA and RalB share strong overall amino acid sequence identity, exhibit essentially identical structural and biochemical properties, and can utilize the same downstream effectors, they also exhibit divergent and sometimes opposing roles in the tumorigenic and metastatic growth of different cancer types. These distinct biological functions have been attributed largely to sequence divergence in their carboxyl-terminal hypervariable regions. However, the role of posttranslational modifications signaled by the hypervariable region carboxyl-terminal tetrapeptide CAAX motif (C = cysteine, A = aliphatic amino acid, X = terminal residue) in Ral isoform-selective functions has not been addressed. We determined that these modifications have distinct roles and consequences. Both RalA and RalB require Ras converting CAAX endopeptidase 1 (RCE1) for association with the plasma membrane, albeit not with endomembranes, and loss of RCE1 caused mislocalization as well as sustained activation of both RalA and RalB. In contrast, isoprenylcysteine carboxylmethyltransferase (ICMT) deficiency disrupted plasma membrane localization only of RalB, whereas RalA depended on ICMT for efficient endosomal localization. Furthermore, the absence of ICMT increased stability of RalB but not RalA protein. Finally, palmitoylation was critical for subcellular localization of RalB but not RalA. In summary, we have identified striking isoform-specific consequences of distinct CAAX-signaled posttranslational modifications that contribute to the divergent subcellular localization and activity of RalA and RalB.
© 2015 by The American Society for Biochemistry and Molecular Biology, Inc.

Entities:  

Keywords:  ICMT; RCE1; Ras protein; intracellular trafficking; plasma membrane; protein isoprenylation; protein palmitoylation; proteolytic enzyme; signal transduction; small GTPase

Mesh:

Substances:

Year:  2015        PMID: 26216878      PMCID: PMC4566255          DOI: 10.1074/jbc.M115.656710

Source DB:  PubMed          Journal:  J Biol Chem        ISSN: 0021-9258            Impact factor:   5.157


  53 in total

1.  Posttranslational lipid modification of Rho family small GTPases.

Authors:  Natalia Mitin; Patrick J Roberts; Emily J Chenette; Channing J Der
Journal:  Methods Mol Biol       Date:  2012

2.  Crystallographic analysis of CaaX prenyltransferases complexed with substrates defines rules of protein substrate selectivity.

Authors:  T Scott Reid; Kimberly L Terry; Patrick J Casey; Lorena S Beese
Journal:  J Mol Biol       Date:  2004-10-15       Impact factor: 5.469

3.  RalA-exocyst-dependent recycling endosome trafficking is required for the completion of cytokinesis.

Authors:  Xiao-Wei Chen; Mayumi Inoue; Shu C Hsu; Alan R Saltiel
Journal:  J Biol Chem       Date:  2006-10-06       Impact factor: 5.157

4.  Geranylgeranyltransferase I inhibitors target RalB to inhibit anchorage-dependent growth and induce apoptosis and RalA to inhibit anchorage-independent growth.

Authors:  Samuel C Falsetti; De-an Wang; Hairuo Peng; Dora Carrico; Adrienne D Cox; Channing J Der; Andrew D Hamilton; Saïd M Sebti
Journal:  Mol Cell Biol       Date:  2007-09-17       Impact factor: 4.272

Review 5.  Drugging the undruggable RAS: Mission possible?

Authors:  Adrienne D Cox; Stephen W Fesik; Alec C Kimmelman; Ji Luo; Channing J Der
Journal:  Nat Rev Drug Discov       Date:  2014-10-17       Impact factor: 84.694

6.  Functional significance of beta gamma-subunit carboxymethylation for the activation of phospholipase C and phosphoinositide 3-kinase.

Authors:  C A Parish; A V Smrcka; R R Rando
Journal:  Biochemistry       Date:  1995-06-13       Impact factor: 3.162

Review 7.  Post-prenylation-processing enzymes as new targets in oncogenesis.

Authors:  Ann M Winter-Vann; Patrick J Casey
Journal:  Nat Rev Cancer       Date:  2005-05       Impact factor: 60.716

8.  Disruption of the mouse Rce1 gene results in defective Ras processing and mislocalization of Ras within cells.

Authors:  E Kim; P Ambroziak; J C Otto; B Taylor; M Ashby; K Shannon; P J Casey; S G Young
Journal:  J Biol Chem       Date:  1999-03-26       Impact factor: 5.157

9.  Activation and involvement of Ral GTPases in colorectal cancer.

Authors:  Timothy D Martin; Jonathan C Samuel; Elizabeth D Routh; Channing J Der; Jen Jen Yeh
Journal:  Cancer Res       Date:  2011-01-01       Impact factor: 12.701

10.  Isoprenylcysteine carboxylmethyltransferase deficiency exacerbates KRAS-driven pancreatic neoplasia via Notch suppression.

Authors:  Helen Court; Marc Amoyel; Michael Hackman; Kyoung Eun Lee; Ruliang Xu; George Miller; Dafna Bar-Sagi; Erika A Bach; Martin O Bergö; Mark R Philips
Journal:  J Clin Invest       Date:  2013-11       Impact factor: 14.808

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  18 in total

Review 1.  Oncogenic Ras Isoforms Signaling Specificity at the Membrane.

Authors:  Ruth Nussinov; Chung-Jung Tsai; Hyunbum Jang
Journal:  Cancer Res       Date:  2017-12-22       Impact factor: 12.701

Review 2.  Focus on the glycerophosphocholine pathway in choline phospholipid metabolism of cancer.

Authors:  Kanchan Sonkar; Vinay Ayyappan; Caitlin M Tressler; Oluwatobi Adelaja; Ruoqing Cai; Menglin Cheng; Kristine Glunde
Journal:  NMR Biomed       Date:  2019-06-11       Impact factor: 4.044

3.  Isoprenylcysteine carboxy methyltransferase (ICMT) is associated with tumor aggressiveness and its expression is controlled by the p53 tumor suppressor.

Authors:  Carla Borini Etichetti; Carolina Di Benedetto; Carolina Rossi; María Virginia Baglioni; Silvio Bicciato; Giannino Del Sal; Mauricio Menacho-Marquez; Javier Girardini
Journal:  J Biol Chem       Date:  2019-01-17       Impact factor: 5.157

4.  Plasma membrane phosphatidylinositol 4-phosphate and 4,5-bisphosphate determine the distribution and function of K-Ras4B but not H-Ras proteins.

Authors:  Gergő Gulyás; Glória Radvánszki; Rita Matuska; András Balla; László Hunyady; Tamas Balla; Péter Várnai
Journal:  J Biol Chem       Date:  2017-09-22       Impact factor: 5.157

Review 5.  Small change, big effect: Taking RAS by the tail through suppression of post-prenylation carboxylmethylation.

Authors:  Hiu Yeung Lau; Mei Wang
Journal:  Small GTPases       Date:  2018-01-25

6.  SIRT2 and Lysine Fatty Acylation Regulate the Activity of RalB and Cell Migration.

Authors:  Nicole A Spiegelman; Xiaoyu Zhang; Hui Jing; Ji Cao; Ilana B Kotliar; Pornpun Aramsangtienchai; Miao Wang; Zhen Tong; Kelly M Rosch; Hening Lin
Journal:  ACS Chem Biol       Date:  2019-09-03       Impact factor: 5.100

Review 7.  A New View of Ras Isoforms in Cancers.

Authors:  Ruth Nussinov; Chung-Jung Tsai; Mayukh Chakrabarti; Hyunbum Jang
Journal:  Cancer Res       Date:  2015-12-10       Impact factor: 12.701

8.  GTP Binding and Oncogenic Mutations May Attenuate Hypervariable Region (HVR)-Catalytic Domain Interactions in Small GTPase K-Ras4B, Exposing the Effector Binding Site.

Authors:  Shaoyong Lu; Avik Banerjee; Hyunbum Jang; Jian Zhang; Vadim Gaponenko; Ruth Nussinov
Journal:  J Biol Chem       Date:  2015-10-09       Impact factor: 5.157

Review 9.  RAL GTPases: Biology and Potential as Therapeutic Targets in Cancer.

Authors:  Chao Yan; Dan Theodorescu
Journal:  Pharmacol Rev       Date:  2018-01       Impact factor: 25.468

10.  Ral GTPase is essential for actin dynamics and Golgi apparatus distribution in mouse oocyte maturation.

Authors:  Ming-Hong Sun; Lin-Lin Hu; Chao-Ying Zhao; Xiang Lu; Yan-Ping Ren; Jun-Li Wang; Xiang-Shun Cui; Shao-Chen Sun
Journal:  Cell Div       Date:  2021-06-10       Impact factor: 5.130

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