The Dual Function of RhoGDI2 in Immunity and Cancer

[en] RhoGDI2 is a guanine nucleotide dissociation inhibitor (GDI) specific for the Rho family of small GTPases. It is highly expressed in hematopoietic cells but is also present in a large array of other cell types. RhoGDI2 has been implicated in multiple human cancers and immunity regulation, where it can display a dual role. Despite its involvement in various biological processes, we still do not have a clear understanding of its mechanistic functions. This review sheds a light on the dual opposite role of RhoGDI2 in cancer, highlights its underappreciated role in immunity and proposes ways to explain its intricate regulatory functions.

Research Center/Unit :

GIGA-LCTB - GIGA Cancer-Connective Tissue Biology - ULiège

Disciplines :

Oncology
Biochemistry, biophysics & molecular biology

Author, co-author :

Tripathi, Mudrika ; Université de Liège - ULiège > GIGA > GIGA Cancer - Connective Tissue Biology

Colige, Alain ; Université de Liège - ULiège > GIGA > GIGA Cancer - Connective Tissue Biology

Deroanne, Christophe ; Université de Liège - ULiège > GIGA > GIGA Cancer - Connective Tissue Biology

Language :

English

Title :

The Dual Function of RhoGDI2 in Immunity and Cancer

Publication date :

16 February 2023

Journal title :

International Journal of Molecular Sciences

ISSN :

1661-6596

eISSN :

1422-0067

Publisher :

MDPI AG

Special issue title :

Mechanical and Biochemical Interplay between Cells and Their Microenvironment

Volume :

Issue :

Pages :

4015

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://www.mdpi.com/1422-0067/24/4/4015/pdf

Name of the research project :

Deciphering the RhoGDI2-specific protein interaction network and dynamics to understand its dual function in cancer.

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique

Funding number :

Télévie Grant No. 7.6533.21

Data Set :

10.3390/ijms24044015

Available on ORBi :

since 20 February 2023

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Bibliography

Vega F.M. Ridley A.J. Rho GTPases in cancer cell biology FEBS Lett. 2008 582 2093 2101 10.1016/j.febslet.2008.04.039
Rodenburg W.S. van Buul J.D. Rho GTPase signalling networks in cancer cell transendothelial migration Vasc. Biol. 2021 3 R77 R95 10.1530/VB-21-0008
Magalhaes Y.T. Farias J.O. Silva L.E. Forti F.L. GTPases, genome, actin: A hidden story in DNA damage response and repair mechanisms DNA Repair 2021 100 103070 10.1016/j.dnarep.2021.103070
Mosaddeghzadeh N. Ahmadian M. The RHO Family GTPases: Mechanisms of Regulation and Signaling Cells 2021 10 1831 10.3390/cells10071831
Svensmark J.H. Brakebusch C. Rho GTPases in cancer: Friend or foe? Oncogene 2019 38 7447 7456 10.1038/s41388-019-0963-7
Kreider-Letterman G. Carr N.M. Garcia-Mata R. Fixing the GAP: The role of RhoGAPs in cancer Eur. J. Cell Biol. 2022 101 151209 10.1016/j.ejcb.2022.151209
Maldonado M.D.M. Medina J.I. Velazquez L. Dharmawardhane S. Targeting Rac and Cdc42 GEFs in Metastatic Cancer Front. Cell Dev. Biol. 2020 8 201 10.3389/fcell.2020.00201
Cho H.J. Kim J.-T. Baek K.E. Kim B.-Y. Lee H.G. Regulation of Rho GTPases by RhoGDIs in Human Cancers Cells 2019 8 1037 10.3390/cells8091037
Crosas-Molist E. Samain R. Kohlhammer L. Orgaz J.L. George S.L. Maiques O. Barcelo J. Sanz-Moreno V. Rho GTPase signaling in cancer progression and dissemination Physiol. Rev. 2022 102 455 510 10.1152/physrev.00045.2020
Kowluru A. Roles of GTP and Rho GTPases in pancreatic islet beta cell function and dysfunction Small GTPases 2020 12 323 335 10.1080/21541248.2020.1815508
Fukumoto Y. Kaibuchi K. Hori Y. Fujioka H. Araki S. Ueda T. Kikuchi A. Takai Y. Molecular cloning and characterization of a novel type of regulatory protein (GDI) for the rho proteins, ras p21-like small GTP-binding proteins Oncogene 1990 5 1321 1328
Kowluru A. Gleason N.F. Underappreciated roles for Rho GDP dissociation inhibitors (RhoGDIs) in cell function: Lessons learned from the pancreatic islet β-cell Biochem. Pharmacol. 2021 197 114886 10.1016/j.bcp.2021.114886
Lelias J.M. Adra C.N. Wulf G.M. Guillemot J.C. Khagad M. Caput D. Lim B. cDNA cloning of a human mRNA preferentially expressed in hematopoietic cells and with homology to a GDP-dissociation inhibitor for the rho GTP-binding proteins Proc. Natl. Acad. Sci. USA 1993 90 1479 1483 10.1073/pnas.90.4.1479
Scherle P. Behrens T. Staudt L.M. Ly-GDI, a GDP-dissociation inhibitor of the RhoA GTP-binding protein, is expressed preferentially in lymphocytes Proc. Natl. Acad. Sci. USA 1993 90 7568 7572 10.1073/pnas.90.16.7568
De León-Bautista M.P. Cardenas-Aguayo M.D.C. Casique-Aguirre D. Almaraz-Salinas M. Parraguirre-Martinez S. Olivo-Diaz A. Thompson-Bonilla M.D.R. Vargas M. Immunological and Functional Characterization of RhoGDI3 and Its Molecular Targets RhoG and RhoB in Human Pancreatic Cancerous and Normal Cells PLoS ONE 2016 11 e0166370 10.1371/journal.pone.0166370
Leffers H. Nielsen M.S. Andersen A.H. Honoré B. Madsen P. Vandekerckhove J. Celis J.E. Identification of Two Human Rho GDP Dissociation Inhibitor Proteins Whose Overexpression Leads to Disruption of the Actin Cytoskeleton Exp. Cell Res. 1993 209 165 174 10.1006/excr.1993.1298
Garcia-Mata R. Boulter E. Burridge K. The ‘invisible hand’: Regulation of RHO GTPases by RHOGDIs Nat. Rev. Mol. Cell Biol. 2011 12 493 504 10.1038/nrm3153
Keep N. Barnes M. Barsukov I. Badii R. Lian L.-Y. Segal A.W. Moody P.C. Roberts G.C. A modulator of rho family G proteins, rhoGDI, binds these G proteins via an immunoglobulin-like domain and a flexible N-terminal arm Structure 1997 5 623 633 10.1016/S0969-2126(97)00218-9
Mosaddeghzadeh N. Jasemi N.S.K. Majolée J. Zhang S.-C. Hordijk P.L. Dvorsky R. Ahmadian M.R. Electrostatic Forces Mediate the Specificity of RHO GTPase-GDI Interactions Int. J. Mol. Sci. 2021 22 12493 10.3390/ijms222212493
Kardol-Hoefnagel T. van Logtestijn S.A. Otten H.G. A Review on the Function and Regulation of ARHGDIB/RhoGDI2 Expression Including the Hypothetical Role of ARHGDIB/RhoGDI2 Autoantibodies in Kidney Transplantation Transplant. Direct 2020 6 e548 10.1097/txd.0000000000000993
Choi E.-K. Kim J.-G. Kim H.-J. Cho J.-Y. Jeong H. Park Y. Islam R. Cap C.K. Park J.-B. Regulation of RhoA GTPase and novel target proteins for ROCK Small GTPases 2017 11 95 102 10.1080/21541248.2017.1364831
Majolée J. Podieh F. Hordijk P.L. Kovačević I. The interplay of Rac1 activity, ubiquitination and GDI binding and its consequences for endothelial cell spreading PLoS ONE 2021 16 e0254386 10.1371/journal.pone.0254386
Chinchole A.N. Lone K.A. Tyagi S. MLL regulates actin cytoskeleton and cell migration by stabilizing Rho GTPases via the transcription of RhoGDI1 J. Cell Sci. 2022 135 jcs260042 10.1242/jcs.260042
Liu W. Wang X. Wang S. Ba X. Xu T. Wang X. Zeng X. RhoGDI2 positively regulates the Rho GTPases activation in response to the β2 outside-in signaling in T cells adhesion and migration on ICAM-1 J. Leukoc. Biol. 2019 106 431 446 10.1002/JLB.2A0718-272RR
Nagar H. Kim S. Lee I. Choi S.-J. Piao S. Jeon B.H. Shong M. Kim C.-S. CRIF1 deficiency suppresses endothelial cell migration via upregulation of RhoGDI2 PLoS ONE 2021 16 e0256646 10.1371/journal.pone.0256646
Yin L. Schwartzberg P. Scharton-Kerstenj T.M. Staudt L. Lenardo M. Immune responses in mice deficient in Ly-GDI, a lymphoid-specific regulator of Rho GTPases Mol. Immunol. 1997 34 481 491 10.1016/S0161-5890(97)00053-9
Zhu G.-F. Xu Y.-W. Li J. Niu H.-L. Ma W.-X. Xu J. Zhou P.-R. Liu X. Ye D.-L. Liu X.-R. et al. Mir20a/106a-WTX axis regulates RhoGDIa/CDC42 signaling and colon cancer progression Nat. Commun. 2019 10 112 10.1038/s41467-018-07998-x
Li X. Wang J. Zhang X. Zeng Y. Liang L. Ding Y. Overexpression of RhoGDI2 Correlates with Tumor Progression and Poor Prognosis in Colorectal Carcinoma Ann. Surg. Oncol. 2011 19 145 153 10.1245/s10434-011-1944-4
Cho H.J. Kim J.-T. Lee S.-J. Hwang Y.S. Park S.Y. Kim B.-Y. Yoo J. Hong K.S. Min J.-K. Lee C.-H. et al. Protein phosphatase 1B dephosphorylates Rho guanine nucleotide dissociation inhibitor 1 and suppresses cancer cell migration and invasion Cancer Lett. 2018 417 141 151 10.1016/j.canlet.2018.01.002
Zhang Y. Zhang B. D4-GDI, a Rho GTPase Regulator, Promotes Breast Cancer Cell Invasiveness Cancer Res 2006 66 5592 5598 10.1158/0008-5472.CAN-05-4004
Wang X. Bi X. Huang X. Wang B. Guo Q. Wu Z. Systematic investigation of biomarker-like role of ARHGDIB in breast cancer Cancer Biomark. 2020 28 101 110 10.3233/CBM-190562 32176626
Hu L. Zou H. Zhan S. Cao K. Biphasic expression of RhoGDI2 in the progression of breast cancer and its negative relation with lymph node metastasis Oncol. Rep. 2007 17 1383 1389 10.3892/or.17.6.1383 17487395
Joly M.M. Williams M.M. Hicks D.J. Jones B. Sanchez V. Young C.D. Sarbassov D.D. Muller W.J. Brantley-Sieders D. Cook R.S. Two distinct mTORC2-dependent pathways converge on Rac1 to drive breast cancer metastasis Breast Cancer Res. 2017 19 74 10.1186/s13058-017-0868-8 28666462
Liang L. Li Q. Huang L.Y. Li D.W. Wang Y.W. Li X.X. Cai S.J. Loss of ARHGDIA expression is associated with poor prognosis in HCC and promotes invasion and metastasis of HCC cells Int. J. Oncol. 2014 45 659 666 10.3892/ijo.2014.2451
Fang Y. Yi J. Lizhi L. Qiucheng C. Rho GDP Dissociation Inhibitor Beta Promotes Cell Proliferation and Invasion by Modulating the AKT Pathway in Hepatocellular Carcinoma DNA Cell Biol. 2014 33 781 786 10.1089/dna.2014.2545 25180836
Liu L. Cui J. Zhao Y. Liu X. Chen L. Xia Y. Wang Y. Chen S. Sun S. Shi B. et al. KDM6A-ARHGDIB axis blocks metastasis of bladder cancer by inhibiting Rac1 Mol. Cancer 2021 20 77 10.1186/s12943-021-01369-9 34006303
Ahmed M. Sottnik J.L. Dancik G.M. Sahu D. Hansel D.E. Theodorescu D. Schwartz M.A. An Osteopontin/CD44 Axis in RhoGDI2-Mediated Metastasis Suppression Cancer Cell 2016 30 432 443 10.1016/j.ccell.2016.08.002
Stevens E.V. Banet N. Onesto C. Plachco A. Alan J.K. Nikolaishvili-Feinberg N. Midkiff B.R. Kuan P.F. Liu J. Miller C.R. et al. RhoGDI2 antagonizes ovarian carcinoma growth, invasion and metastasis Small GTPases 2011 2 202 210 10.4161/sgtp.2.4.17795
Xia B. Wang J. Adenosine Inhibits Ovarian Cancer Growth Through Regulating RhoGDI2 Protein Expression Drug Des. Dev. Ther. 2019 13 3837 3844 10.2147/DDDT.S219028
Küppers R. Klein U. Schwering I. Distler V. Bräuninger A. Cattoretti G. Tu Y. Stolovitzky G.A. Califano A. Hansmann M.-L. et al. Identification of Hodgkin and Reed-Sternberg cell-specific genes by gene expression profiling J. Clin. Investig. 2003 111 529 537 10.1172/JCI200316624
Ma L. Xu G. Sotnikova A. Szczepanowski M. Giefing M. Krause K. Krams M. Siebert R. Jin J. Klapper W. Loss of expression of LyGDI (ARHGDIB), a rho GDP-dissociation inhibitor, in Hodgkin lymphoma Br. J. Haematol. 2007 139 217 223 10.1111/j.1365-2141.2007.06782.x 17897297
Zeng Y. Ren M. Li Y. Liu Y. Chen C. Su J. Su B. Xia H. Liu F. Jiang H. et al. Knockdown of RhoGDI2 represses human gastric cancer cell proliferation, invasion and drug resistance via the Rac1/Pak1/LIMK1 pathway Cancer Lett. 2020 492 136 146 10.1016/j.canlet.2020.07.013 32860848
Kim H.-J. Ryu K.-J. Kim M. Kim T. Kim S.-H. Han H. Kim H. Hong K.-S. Song C.Y. Choi Y. et al. RhoGDI2-Mediated Rac1 Recruitment to Filamin A Enhances Rac1 Activity and Promotes Invasive Abilities of Gastric Cancer Cells Cancers 2022 14 255 10.3390/cancers14010255 35008419
Yi B. Hu Y. Qin G. Gu W. Zhu X. He S. Zhou J. Li D. Depletion of RhoGDI2 expression inhibits the ability of invasion and migration in pancreatic carcinoma Int. J. Mol. Med. 2014 34 205 212 10.3892/ijmm.2014.1765 24788627
Zhang M. Ding G. Zhou L. Shen T. Xu X. Zhao T. Jia S. Cao L. Interferon Gamma Inhibits CXCL8-Induced Proliferation and Migration of Pancreatic Cancer BxPC-3 Cell Line via a RhoGDI2/Rac1/NF-κB Signaling Pathway J. Interferon Cytokine Res. 2018 38 413 422 10.1089/jir.2018.0070 30192158
Yi B. Hu Y. Zhu D. Yao J. Zhou J. Zhang Y. He Z. Zhang L. Zhang Z. Yang J. et al. RhoGDI2 induced malignant phenotypes of pancreatic cancer cells via regulating Snail expression Genes Genom. 2022 44 561 569 10.1007/s13258-022-01217-0
Liu Y. Wei X. Guan L. Xu S. Yuan Y. Lv D. He X. Zhan J. Kong Y. Guo J. et al. Unconventional myosin VIIA promotes melanoma progression J. Cell Sci. 2018 131 jcs209924 10.1242/jcs.209924
Niu H. Wu B. Jiang H. Li H. Zhang Y. Peng Y. He P. Mechanisms of RhoGDI2 Mediated Lung Cancer Epithelial-Mesenchymal Transition Suppression Cell. Physiol. Biochem. 2014 34 2007 2016 10.1159/000366396
Niu H. Wu B. Peng Y. Jiang H. Zhang Y. Wang J. Zhang Y. He P. RNA interference-mediated knockdown of RhoGDI2 induces the migration and invasion of human lung cancer A549 cells via activating the PI3K/Akt pathway Tumor Biol. 2014 36 409 419 10.1007/s13277-014-2671-9
Cao J. Wang Y. Dong R. Lin G. Zhang N. Wang J. Lin N. Gu Y. Ding L. Ying M. et al. Hypoxia-Induced WSB1 Promotes the Metastatic Potential of Osteosarcoma Cells Cancer Res 2015 75 4839 4851 10.1158/0008-5472.CAN-15-0711
Che J. Jin Z. Yan F. You J. Xie J. Chen B. Cheng G. Zhu H. He Q. Hu Y. et al. Discovery of 5,6-Bis(4-methoxy-3-methylphenyl)pyridin-2-amine as a WSB1 Degrader to Inhibit Cancer Cell Metastasis J. Med. Chem. 2021 64 8621 8643 10.1021/acs.jmedchem.1c00586 34060833
Nakata Y. Kondoh K. Fukushima S. Hashiguchi A. Du W. Hayashi M. Fujimoto J.-I. Hata J.-I. Yamada T. Mutated D4-guanine diphosphate–dissociation inhibitor is found in human leukemic cells and promotes leukemic cell invasion Exp. Hematol. 2008 36 37 50 10.1016/j.exphem.2007.08.023 18037226
Luo J. Wang J. Zheng H. Wang L. Rho GDP-Dissociation Inhibitor 2 Inhibits C-X-C Chemokine Receptor Type 4-Mediated Acute Lymphoblastic Leukemia Cell Migration Front. Oncol. 2020 10 1512 10.3389/fonc.2020.01512 32903764
Mokhtar A.M.B.A. Ahmed S.B.M. Darling N.J. Harris M. Mott H.R. Owen D. A Complete Survey of RhoGDI Targets Reveals Novel Interactions with Atypical Small GTPases Biochemistry 2021 60 1533 1551 10.1021/acs.biochem.1c00120 33913706
Kasper B. Tidow N. Grothues D. Welte K. Differential expression and regulation of GTPases (RhoA and Rac2) and GDIs (LyGDI and RhoGDI) in neutrophils from patients with severe congenital neutropenia Blood 2000 95 2947 2953 10.1182/blood.V95.9.2947.009k10_2947_2953 10779444
Scheffzek K. Stephan I. Jensen O.N. Illenberger D. Gierschik P. The Rac-RhoGDI complex and the structural basis for the regulation of Rho proteins by RhoGDI Nat. Struct. Biol. 2000 7 122 126 10.1038/72392 10655614
Platko J.V. Leonard A.D. Adra C.N. Shaw R.J. Cerione A.R. Lim B. A single residue can modify target-binding affinity and activity of the functional domain of the Rho-subfamily GDP dissociation inhibitors Proc. Natl. Acad. Sci. USA 1995 92 2974 2978 10.1073/pnas.92.7.2974 7708758
Togawa A. Miyoshi J. Ishizaki H. Tanaka M. Takakura A. Nishioka H. Yoshida H. Doi T. Mizoguchi A. Matsuura N. et al. Progressive impairment of kidneys and reproductive organs in mice lacking Rho GDIα Oncogene 1999 18 5373 5380 10.1038/sj.onc.1202921
Ishizaki H. Togawa A. Tanaka-Okamoto M. Hori K. Nishimura M. Hamaguchi A. Imai T. Takai Y. Miyoshi J. Defective Chemokine-Directed Lymphocyte Migration and Development in the Absence of Rho Guanosine Diphosphate-Dissociation Inhibitors α and β J. Immunol. 2006 177 8512 8521 10.4049/jimmunol.177.12.8512
Bagci H. Sriskandarajah N. Robert A. Boulais J. Elkholi I.E. Tran V. Lin Z.-Y. Thibault M.-P. Dubé N. Faubert D. et al. Mapping the proximity interaction network of the Rho-family GTPases reveals signalling pathways and regulatory mechanisms Nat. Cell Biol. 2019 22 120 134 Correction in Nat. Cell Biol. 2020, 22, 353 10.1038/s41556-019-0438-7
Liu S. Cui H. Li Q. Zhang L. Na Q. Liu C. RhoGDI2 Is Expressed in Human Trophoblasts and Involved in Their Migration by Inhibiting the Activation of RAC11 Biol. Reprod. 2014 90 88 10.1095/biolreprod.113.111153 24554735
Institute for Quality and Efficiency in Health Care (IQWiG) The Innate and Adaptive Immune Systems 2020 Available online: https://www.ncbi.nlm.nih.gov/books/NBK279396/ (accessed on 5 December 2022)
Mehta P. Wavreille A.-S. Justiniano S. Marsh R.L. Yu J. Burry R.W. Jarjoura D. Eubank T. Caligiuri M.A. Butchar J.P. et al. LyGDI, a Novel SHIP-Interacting Protein, Is a Negative Regulator of FcγR-Mediated Phagocytosis PLoS ONE 2011 6 e21175 10.1371/journal.pone.0021175 21695085
Castellano F. Chavrier P. Caron E. Actin dynamics during phagocytosis Semin. Immunol. 2001 13 347 355 10.1006/smim.2001.0331 11708890
Vitali R. Palone F. Armuzzi A. Fulci V. Negroni A. Carissimi C. Cucchiara S. Stronati L. Proteomic Analysis Identifies Three Reliable Biomarkers of Intestinal Inflammation in the Stools of Patients with Inflammatory Bowel Disease J. Crohn’s Colitis 2022 17 92 102 10.1093/ecco-jcc/jjac110
Nguyen T.B. Do D.N. Nguyen T.T.P. Nguyen T.L. Nguyen-Thanh T. Nguyen H.T. Immune–related biomarkers shared by inflammatory bowel disease and liver cancer PLoS ONE 2022 17 e0267358 10.1371/journal.pone.0267358
Wu J. Cao J. Fan Y. Li C. Hu X. Comprehensive analysis of miRNA–mRNA regulatory network and potential drugs in chronic chagasic cardiomyopathy across human and mouse BMC Med. Genom. 2021 14 283 10.1186/s12920-021-01134-3
Tabellini G. Baronio M. Patrizi O. Benevenuto A. Gazzurelli L. Plebani A. Parolini S. Lougaris V. The RAC2-PI3K axis regulates human NK cell maturation and function Clin. Immunol. 2019 208 108257 10.1016/j.clim.2019.108257
Hojjatipour T. Aslani S. Salimifard S. Mikaeili H. Hemmatzadeh M. Navashenaq J.G. Parvin E.A. Jadidi-Niaragh F. Mohammadi H. NK cells—Dr. Jekyll and Mr. Hyde in autoimmune rheumatic diseases Int. Immunopharmacol. 2022 107 108682 10.1016/j.intimp.2022.108682
Zeng X. Luo X. Mao X. Wen D. Zhang H. Wang J. Inflammatory and immune-related factor Caspase 1 contributes to the development of oral lichen planus Arch. Oral Biol. 2021 131 105244 10.1016/j.archoralbio.2021.105244
Kamburova E.G. Gruijters M.L. Kardol-Hoefnagel T. Wisse B.W. Joosten I. Allebes W.A. van der Meer A. Hilbrands L.B. Baas M.C. Spierings E. et al. Antibodies against ARHGDIB are associated with long-term kidney graft loss Am. J. Transplant. 2019 19 3335 3344 10.1111/ajt.15493
Senev A. Otten H.G. Kamburova E.G. Callemeyn J. Lerut E. Van Sandt V. Kuypers D. Emonds M.-P. Naesens M. Antibodies against ARHGDIB and ARHGDIB Gene Expression Associate with Kidney Allograft Outcome Transplantation 2020 104 1462 1471 10.1097/TP.0000000000003005 31651716
Betjes M.G. Sablik K.A. Litjens N.H. Otten H.G. de Weerd A.E. ARHGDIB and AT1R autoantibodies are differentially related to the development and presence of chronic antibody-mediated rejection and fibrosis in kidney allografts Hum. Immunol. 2021 82 89 96 10.1016/j.humimm.2020.12.003 33358038
Kardol-Hoefnagel T. Michielsen L.A. Ehlers A.M. van Zuilen A.D. Luijk B. Otten H.G. Complement component C3 and C5b-9 deposition on hypoxia reperfused endothelial cells by non-HLA antibodies against RhoGDI2: A player involved in graft failure? Hla 2022 101 103 114 10.1111/tan.14858 36266772
Gorvel J.-P. Chang T.-C. Boretto J. Azuma T. Chavrier P. Differential properties of D4/LyGDI versus RhoGDI: Phosphorylation and rho GTPase selectivity FEBS Lett. 1998 422 269 273 10.1016/S0014-5793(98)00020-9
Groysman M. Hornstein I. Alcover A. Katzav S. Vav1 and Ly-GDI Two Regulators of Rho GTPases, Function Cooperatively as Signal Transducers in T Cell Antigen Receptor-induced Pathways J. Biol. Chem. 2002 277 50121 50130 10.1074/jbc.M204299200
Ngo A.T.P. Thierheimer M.L.D. Babur Ö. Rocheleau A.D. Huang T. Pang J. Rigg R.A. Mitrugno A. Theodorescu D. Burchard J. et al. Assessment of roles for the Rho-specific guanine nucleotide dissociation inhibitor Ly-GDI in platelet function: A spatial systems approach Am. J. Physiol. Physiol. 2017 312 C527 C536 10.1152/ajpcell.00274.2016
Na S. Chuang T.-H. Cunningham A. Turi T.G. Hanke J.H. Bokoch G.M. Danley D.E. D4-GDI, a Substrate of CPP32, Is Proteolyzed during Fas-induced Apoptosis J. Biol. Chem. 1996 271 11209 11213 10.1074/jbc.271.19.11209
Krieser R.J. Eastman A. Cleavage and nuclear translocation of the caspase 3 substrate Rho GDP-dissociation inhibitor, D4-GDI, during apoptosis Cell Death Differ. 1999 6 412 419 10.1038/sj.cdd.4400515
Choi M.-R. Groot M. Drexler H.C.A. Functional implications of caspase-mediated RhoGDI2 processing during apoptosis of HL60 and K562 leukemia cells Apoptosis 2007 12 2025 2035 10.1007/s10495-007-0121-5
Kettritz R. Xu Y.X. Faass B. Klein J.B. Müller E.C. Otto A. Busjahn A. Luft F.C. Haller H. TNF-alpha-mediated neutrophil apoptosis involves Ly-GDI, a Rho GTPase regulator J. Leukoc. Biol. 2000 68 277 283 10.1189/jlb.68.2.277
Tavares L.A. Januário Y.C. Dasilva L.L.P. HIV-1 Hijacking of Host ATPases and GTPases That Control Protein Trafficking Front. Cell Dev. Biol. 2021 9 622610 10.3389/fcell.2021.622610 34307340
Watanabe T. Urano E. Miyauchi K. Ichikawa R. Hamatake M. Misawa N. Sato K. Ebina H. Koyanagi Y. Komano J. The Hematopoietic Cell-Specific Rho GTPase Inhibitor ARHGDIB/D4GDI Limits HIV Type 1 Replication AIDS Res. Hum. Retrovir. 2012 28 913 922 10.1089/aid.2011.0180 21936715
Anokhin B. Spearman P. Viral and Host Factors Regulating HIV-1 Envelope Protein Trafficking and Particle Incorporation Viruses 2022 14 1729 10.3390/v14081729 36016351
Weber K.T. Anversa P. Armstrong P.W. Brilla C.G. Burnett J.C. Cruickshank J.M. Devereux R.B. Giles T.D. Korsgaard N. Leier C.V. et al. Remodeling and reparation of the cardiovascular system J. Am. Coll. Cardiol. 1992 20 3 16 10.1016/0735-1097(92)90130-F
Kloc M. Ghobrial R.M. Chronic allograft rejection: A significant hurdle to transplant success Burn. Trauma 2014 2 3 10 10.4103/2321-3868.121646
Dai F. Qi Y. Guan W. Meng G. Liu Z. Zhang T. Yao W. RhoGDI stability is regulated by SUMOylation and ubiquitination via the AT1 receptor and participates in Ang II-induced smooth muscle proliferation and vascular remodeling Atherosclerosis 2019 288 124 136 10.1016/j.atherosclerosis.2019.07.010
Zhang J. Tang L. Dai F. Qi Y. Yang L. Liu Z. Deng L. Yao W. Qi Y. Deng W.Y.L. ROCK inhibitors alleviate myofibroblast transdifferentiation and vascular remodeling via decreasing TGFβ1-mediated RhoGDI expression Gen. Physiol. Biophys. 2019 38 271 280 10.4149/gpb_2019017
Tang L. Feng P. Qi Y. Huang L. Liang X. Chen X. TGFβ1 induces myofibroblast transdifferentiation via increasing Smad-mediated RhoGDI-RhoGTPase signaling Gen. Physiol. Biophys. 2022 41 511 521 10.4149/gpb_2022044
Nagy Á. Munkácsy G. Győrffy B. Pancancer survival analysis of cancer hallmark genes Sci. Rep. 2021 11 6047 10.1038/s41598-021-84787-5
Huang H. Jin H. Zhao H. Wang J. Li X. Yan H. Wang S. Guo X. Xue L. Li J. et al. RhoGDIβ promotes Sp1/MMP-2 expression and bladder cancer invasion through perturbing miR-200c-targeted JNK2 protein translation Mol. Oncol. 2017 11 1579 1594 10.1002/1878-0261.12132
Yu Y. Jin H. Xu J. Gu J. Li X. Xie Q. Huang H. Li J. Tian Z. Jiang G. et al. XIAP overexpression promotes bladder cancer invasion in vitro and lung metastasis in vivo via enhancing nucleolin-mediated Rho-GDIβ mRNA stability Int. J. Cancer 2017 142 2040 2055 10.1002/ijc.31223
Xu J. Hua X. Jin H. Zhu J. Li Y. Li J. Huang C. NFκB2 p52 stabilizesrhogdiβmRNA by inhibiting AUF1 protein degradation via a miR-145/Sp1/USP8-dependent axis Mol. Carcinog. 2019 58 777 793 10.1002/mc.22970 30604907
Teicher B.A. Fricker S.P. CXCL12 (SDF-1)/CXCR4 Pathway in Cancer Clin. Cancer Res. 2010 16 2927 2931 10.1158/1078-0432.CCR-09-2329 20484021
Devel L. Guedeney N. Bregant S. Chowdhury A. Jean M. Legembre P. Role of metalloproteases in the CD95 signaling pathways Front. Immunol. 2022 13 1074099 10.3389/fimmu.2022.1074099
Zhang Y. Yan C. Li Y. Mao X. Tao W. Tang Y. Lin Y. Guo Q. Duan J. Lin N. Therapeutic effects of Euphorbia Pekinensis and Glycyrrhiza glabra on Hepatocellular Carcinoma Ascites Partially Via Regulating the Frk-Arhgdib-Inpp5d-Avpr2-Aqp4 Signal Axis Sci. Rep. 2017 7 41925 10.1038/srep41925
Shi M.K. Xuan Y.L. He X.F. FHL1 Overexpression as a Inhibitor of Lung Cancer Cell Invasion via Increasing RhoGDIß mRNA Expression Cell J. Yakhteh 2022 24 239 244 10.22074/cellj.2022.8031
Dang H. Schiebel E. Emerging roles of centrosome cohesion Open Biol. 2022 12 220229 10.1098/rsob.220229
Ge R. Cao M. Chen M. Liu M. Xie S. Cytoskeletal networks in primary cilia: Current knowledge and perspectives J. Cell. Physiol. 2022 237 3975 3983 10.1002/jcp.30865 36000703
Hoffmann I. Role of Polo-like Kinases Plk1 and Plk4 in the Initiation of Centriole Duplication—Impact on Cancer Cells 2022 11 786 10.3390/cells11050786
Porter A.P. Reed H. White G.R.M. Ogg E.-L. Whalley H.J. Malliri A. The RAC1 activator Tiam1 regulates centriole duplication through controlling PLK4 levels J. Cell Sci. 2021 134 jcs252502 10.1242/jcs.252502
Epting D. Slanchev K. Boehlke C. Hoff S. Loges N.T. Yasunaga T. Indorf L. Nestel S. Lienkamp S.S. Omran H. et al. The Rac1 regulator ELMO controls basal body migration and docking in multiciliated cells through interaction with Ezrin Development 2015 142 174 184 10.1242/dev.112250 25516973
Streets A.J. Prosseda P.P. Ong A.C. Polycystin-1 regulates ARHGAP35-dependent centrosomal RhoA activation and ROCK signaling JCI Insight 2020 5 e135385 10.1172/jci.insight.135385 32663194
Jiang Y.-S. Maeda M. Okamoto M. Fujii M. Fukutomi R. Hori M. Tatsuka M. Ota T. Centrosomal localization of RhoGDIβ and its relevance to mitotic processes in cancer cells Int. J. Oncol. 2012 42 460 468 10.3892/ijo.2012.1730 23232495
Doi N. Togari H. Minagi K. Iwaoka Y. Tai A. Nakaoji K. Hamada K. Tatsuka M. 2-O-Octadecylascorbic acid represses RhoGDIβ expression and ameliorates DNA damage-induced abnormal spindle orientations J. Cell. Biochem. 2021 122 739 751 10.1002/jcb.29908 33586155