Fine-tuning cell organelle dynamics during mitosis by small GTPases

Abstract

During mitosis, the allocation of genetic material concurs with organelle transformation and distribution. The coordination of genetic material inheritance with organelle dynamics directs accurate mitotic progression, cell fate determination, and organismal homeostasis. Small GTPases belonging to the Ras superfamily regulate various cell organelles during division. Being the key regulators of membrane dynamics, the dysregulation of small GTPases is widely associated with cell organelle disruption in neoplastic and non-neoplastic diseases, such as cancer and Alzheimer’s disease. Recent discoveries shed light on the molecular properties of small GTPases as sophisticated modulators of a remarkably complex and perfect adaptors for rapid structure reformation. This review collects current knowledge on small GTPases in the regulation of cell organelles during mitosis and highlights the mediator role of small GTPase in transducing cell cycle signaling to organelle dynamics during mitosis.

Keywords

small GTPase / cell organelle / mitosis

References

[1] Champion L, Linder MI, Kutay U. Cellular reorganization during mitotic entry. Trends Cell Biol 2017; 27( 1): 26– 41

[2] Carlton JG, Jones H, Eggert US. Membrane and organelle dynamics during cell division. Nat Rev Mol Cell Biol 2020; 21( 3): 151– 166

[3] Jongsma MLM, Berlin I, Neefjes J. On the move: organelle dynamics during mitosis. Trends Cell Biol 2015; 25( 3): 112– 124

[4] Song S, Cong W, Zhou S, Shi Y, Dai W, Zhang H, Wang X, He B, Zhang Q. Small GTPases: structure, biological function and its interaction with nanoparticles. Asian J Pharm Sci 2019; 14( 1): 30– 39

[5] Vetter IR. The structure of the G domain of the Ras superfamily. In: Wittinghofer A. Ras Superfamily Small G Proteins: Biology and Mechanisms 1. Springer Vienna, 2014: 25- 50 doi:10.1007/978-3-7091-1806-1_2

[6] Wennerberg K, Rossman KL, Der CJ. The Ras superfamily at a glance. J Cell Sci 2005; 118( 5): 843– 846

[7] Hodge RG, Schaefer A, Howard SV, Der CJ. RAS and RHO family GTPase mutations in cancer: twin sons of different mothers? Crit Rev Biochem Mol Biol 2020; 55(4): 386–407

[8] Rojas AM, Fuentes G, Rausell A, Valencia A. The Ras protein superfamily: evolutionary tree and role of conserved amino acids. J Cell Biol. 2012; 196 : 189– 201

[9] Cherfils J, Zeghouf M. Regulation of small GTPases by GEFs, GAPs, and GDIs. Physiol Rev 2013; 93( 1): 269– 309

[10] Bos J Rehmann H Wittinghofer A. GEFs and GAPs: critical elements in the control of small G proteins. Cell 2007; 129(5): 865–877 Erratum in: Cell 2007; 130(2): 385

[11] Cherfils J. GEFs and GAPs: mechanisms and structures. In: Wittinghofer A. Ras Superfamily Small G Proteins: Biology and Mechanisms 1. Springer Vienna; 2014: 51- 63

[12] Mishra AK, Lambright DG. Small GTPases and their GAPs. Biopolymers 2016; 105( 8): 431– 448

[13] Clarke PR, Zhang C. Spatial and temporal coordination of mitosis by Ran GTPase. Nat Rev Mol Cell Biol 2008; 9( 6): 464– 477

[14] Jackson CL, Bouvet S. Arfs at a glance. J Cell Sci 2014; 127( 19): 4103– 4109

[15] Schwartz SL, Cao C, Pylypenko O, Rak A, Wandinger-Ness A. Rab GTPases at a glance. J Cell Sci 2007; 120( 22): 3905– 3910

[16] D’Souza-Schorey C, Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 2006; 7( 5): 347– 358

[17] Kjos I, Vestre K, Guadagno NA, Borg Distefano M, Progida C. Rab and Arf proteins at the crossroad between membrane transport and cytoskeleton dynamics. Biochim Biophys Acta Mol Cell Res 2018; 1865( 10): 1397– 1409

[18] Bannykh SI, Plutner H, Matteson J, Balch WE. The role of ARF1 and rab GTPases in polarization of the Golgi stack. Traffic 2005; 6( 9): 803– 819

[19] Yahara N, Ueda T, Sato K, Nakano A. Multiple roles of Arf1 GTPase in the yeast exocytic and endocytic pathways. Mol Biol Cell 2001; 12( 1): 221– 238

[20] Donaldson JG, Honda A, Weigert R. Multiple activities for Arf1 at the Golgi complex. Biochim Biophys Acta 2005; 1744( 3): 364– 373

[21] Kashatus DF, Lim KH, Brady DC, Pershing NLKK, Cox AD, Counter CM. RALA and RALBP1 regulate mitochondrial fission at mitosis. Nat Cell Biol 2011; 13( 9): 1108– 1115

[22] Shinde SR, Maddika S. Post translational modifications of Rab GTPases. Small GTPases 2018; 9( 1-2): 49– 56

[23] Hodge RG, Ridley AJ. Regulating Rho GTPases and their regulators. Nat Rev Mol Cell Biol 2016; 17( 8): 496– 510

[24] Nigg EA. Mitotic kinases as regulators of cell division and its checkpoints. Nat Rev Mol Cell Biol 2001; 2( 1): 21– 32

[25] Dao VT, Dupuy AG, Gavet O, Caron E, de Gunzburg J. Dynamic changes in Rap1 activity are required for cell retraction and spreading during mitosis. J Cell Sci 2009; 122( 16): 2996– 3004

[26] Glotzer M, Murray AW, Kirschner MW. Cyclin is degraded by the ubiquitin pathway. Nature 1991; 349( 6305): 132– 138

[27] Lei Z, Wang J, Zhang L, Liu CH. Ubiquitination-dependent regulation of small GTPases in membrane trafficking: from cell biology to human diseases. Front Cell Dev Biol 2021; 9 : 688352

[28] de la Vega M, Burrows JF, Johnston JA. Ubiquitination: added complexity in Ras and Rho family GTPase function. Small GTPases 2011; 2( 4): 192– 201

[29] Ding F, Yin Z, Wang HR. Ubiquitination in Rho signaling. Curr Top Med Chem 2011; 11( 23): 2879– 2887

[30] Song P, Trajkovic K, Tsunemi T, Krainc D. Parkin modulates endosomal organization and function of the endo-lysosomal pathway. J Neurosci 2016; 36( 8): 2425– 2437

[31] Wang H-R, Zhang Y, Ozdamar B, Ogunjimi AA, Alexandrova E, Thomsen GH, Wrana JL. Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 2003; 302( 5651): 1775– 1779

[32] Seabra MC, Goldstein JL, Südhof TC, Brown MS. Rab geranylgeranyl transferase. A multisubunit enzyme that prenylates GTP-binding proteins terminating in Cys-X-Cys or Cys-Cys. J Biol Chem 1992; 267( 20): 14497– 14503

[33] Leung KF, Baron R, Ali BR, Magee AI, Seabra MC. Rab GTPases containing a CAAX motif are processed post-geranylgeranylation by proteolysis and methylation. J Biol Chem 2007; 282( 2): 1487– 1497

[34] Heald R, Khodjakov A. Thirty years of search and capture: the complex simplicity of mitotic spindle assembly. J Cell Biol 2015; 211( 6): 1103– 1111

[35] O’Connell CB, Khodjakov AL. Cooperative mechanisms of mitotic spindle formation. J Cell Sci 2007; 120( 10): 1717– 1722

[36] Lavia P. The GTPase RAN regulates multiple steps of the centrosome life cycle. Chromosome Res 2016; 24( 1): 53– 65

[37] Feng Y, Yuan JH, Maloid SC, Fisher R, Copeland TD, Longo DL, Conrads TP, Veenstra TD, Ferris A, Hughes S, Dimitrov DS, Ferris DK. Polo-like kinase 1-mediated phosphorylation of the GTP-binding protein Ran is important for bipolar spindle formation. Biochem Biophys Res Commun 2006; 349( 1): 144– 152

[38] Bompard G, Rabeharivelo G, Frank M, Cau J, Delsert C, Morin N. Subgroup II PAK-mediated phosphorylation regulates Ran activity during mitosis. J Cell Biol 2010; 190( 5): 807– 822

[39] Tedeschi A, Ciciarello M, Mangiacasale R, Roscioli E, Rensen WM, Lavia P. RANBP1 localizes a subset of mitotic regulatory factors on spindle microtubules and regulates chromosome segregation in human cells. J Cell Sci 2007; 120( 21): 3748– 3761

[40] Sit ST, Manser E. Rho GTPases and their role in organizing the actin cytoskeleton. J Cell Sci 2011; 124( 5): 679– 683

[41] Müller PM, Rademacher J, Bagshaw RD, Wortmann C, Barth C, van Unen J, Alp KM, Giudice G, Eccles RL, Heinrich LE, Pascual-Vargas P, Sanchez-Castro M, Brandenburg L, Mbamalu G, Tucholska M, Spatt L, Czajkowski MT, Welke RW, Zhang S, Nguyen V, Rrustemi T, Trnka P, Freitag K, Larsen B, Popp O, Mertins P, Gingras AC, Roth FP, Colwill K, Bakal C, Pertz O, Pawson T, Petsalaki E, Rocks O. Systems analysis of RhoGEF and RhoGAP regulatory proteins reveals spatially organized RAC1 signalling from integrin adhesions. Nat Cell Biol 2020; 22( 4): 498– 511

[42] Chircop M. Rho GTPases as regulators of mitosis and cytokinesis in mammalian cells. Small GTPases 2014; 5( 2): e29770

[43] Yasuda S, Taniguchi H, Oceguera-Yanez F, Ando Y, Watanabe S, Monypenny J, Narumiya S. An essential role of Cdc42-like GTPases in mitosis of HeLa cells. FEBS Lett 2006; 580( 14): 3375– 3380

[44] Miserey-Lenkei S, Colombo MI. Small RAB GTPases regulate multiple steps of mitosis. Front Cell Dev Biol 2016; 4 : 2

[45] Lanzetti L. A novel function of Rab5 in mitosis. Small GTPases 2012; 3( 3): 168– 172

[46] Hehnly H, Doxsey S. Rab11 endosomes contribute to mitotic spindle organization and orientation. Dev Cell 2014; 28( 5): 497– 507

[47] Hobdy-Henderson KC, Hales CM, Lapierre LA, Cheney RE, Goldenring JR. Dynamics of the apical plasma membrane recycling system during cell division. Traffic 2003; 4( 10): 681– 693

[48] Zhou C, Cunningham L, Marcus AI, Li Y, Kahn RA. Arl2 and Arl3 regulate different microtubule-dependent processes. Mol Biol Cell 2006; 17( 5): 2476– 2487

[49] Okai T, Araki Y, Tada M, Tateno T, Kontani K, Katada T. Novel small GTPase subfamily capable of associating with tubulin is required for chromosome segregation. J Cell Sci 2004; 117( 20): 4705– 4715

[50] Papini D, Langemeyer L, Abad MA, Kerr A, Samejima I, Eyers PA, Jeyaprakash AA, Higgins JMG, Barr FA, Earnshaw WC. TD-60 links RalA GTPase function to the CPC in mitosis. Nat Commun 2015; 6( 1): 7678

[51] Boeynaems S, Alberti S, Fawzi NL, Mittag T, Polymenidou M, Rousseau F, Schymkowitz J, Shorter J, Wolozin B, Van Den Bosch L, Tompa P, Fuxreiter M. Protein phase separation: a new phase in cell biology. Trends Cell Biol 2018; 28( 6): 420– 435

[52] Zhang C, Rabouille C. Membrane-bound meet membraneless in health and disease. Cells 2019; 8( 9): 1000

[53] Nott TJ, Petsalaki E, Farber P, Jervis D, Fussner E, Plochowietz A, Craggs TD, Bazett-Jones DP, Pawson T, Forman-Kay JD, Baldwin AJ. Phase transition of a disordered nuage protein generates environmentally responsive membraneless organelles. Mol Cell 2015; 57( 5): 936– 947

[54] Gomes E, Shorter J. The molecular language of membraneless organelles. J Biol Chem 2019; 294( 18): 7115– 7127

[55] Rai AK, Chen JXX, Selbach M, Pelkmans L. Kinase-controlled phase transition of membraneless organelles in mitosis. Nature 2018; 559( 7713): 211– 216

[56] Jiang H, Wang S, Huang Y, He X, Cui H, Zhu X, Zheng Y. Phase transition of spindle-associated protein regulate spindle apparatus assembly. Cell 2015; 163( 1): 108– 122

[57] Woodruff JB, Ferreira Gomes B, Widlund PO, Mahamid J, Honigmann A, Hyman AA. The centrosome is a selective condensate that nucleates microtubules by concentrating tubulin. Cell 2017; 169( 6): 1066– 1077.e10

[58] Keryer G, Witczak O, Delouvée A, Kemmner WA, Rouillard D, Taskén K, Bornens M. Dissociating the centrosomal matrix protein AKAP450 from centrioles impairs centriole duplication and cell cycle progression. Mol Biol Cell 2003; 14( 6): 2436– 2446

[59] Keryer G, Di Fiore B, Celati C, Lechtreck KF, Mogensen M, Delouvée A, Lavia P, Bornens M, Tassin AM. Part of Ran is associated with AKAP450 at the centrosome: involvement in microtubule-organizing activity. Mol Biol Cell 2003; 14( 10): 4260– 4271

[60] Bompard G, Rabeharivelo G, Cau J, Abrieu A, Delsert C, Morin N. P21-activated kinase 4 (PAK4) is required for metaphase spindle positioning and anchoring. Oncogene 2013; 32( 7): 910– 919

[61] Kilchert C, Weidner J, Prescianotto-Baschong C, Spang A. Defects in the secretory pathway and high Ca²⁺ induce multiple P-bodies. Mol Biol Cell 2010; 21( 15): 2624– 2638

[62] Serio G, Margaria V, Jensen S, Oldani A, Bartek J, Bussolino F, Lanzetti L. Small GTPase Rab5 participates in chromosome congression and regulates localization of the centromere-associated protein CENP-F to kinetochores. Proc Natl Acad Sci USA 2011; 108( 42): 17337– 17342

[63] Zhang X, Hagen J, Muniz VP, Smith T, Coombs GS, Eischen CM, Mackie DI, Roman DL, Van Rheeden R, Darbro B, Tompkins VS, Quelle DE. RABL6A, a novel RAB-like protein, controls centrosome amplification and chromosome instability in primary fibroblasts. PLoS One 2013; 8( 11): e80228

[64] Hehnly H, Chen CTT, Powers CM, Liu HLL, Doxsey S. The centrosome regulates the Rab11-dependent recycling endosome pathway at appendages of the mother centriole. Curr Biol 2012; 22( 20): 1944– 1950

[65] Takahashi S, Takei T, Koga H, Takatsu H, Shin HW, Nakayama K. Distinct roles of Rab11 and Arf6 in the regulation of Rab11-FIP3/arfophilin-1 localization in mitotic cells. Genes Cells 2011; 16( 9): 938– 950

[66] Champion L, Linder MI, Kutay U. Cellular reorganization during mitotic entry. Trends Cell Biol 2017; 27( 1): 26– 41

[67] Ramkumar N, Baum B. Coupling changes in cell shape to chromosome segregation. Nat Rev Mol Cell Biol 2016; 17( 8): 511– 521

[68] Atilla-Gokcumen GE, Muro E, Relat-Goberna J, Sasse S, Bedigian A, Coughlin ML, Garcia-Manyes S, Eggert US. Dividing cells regulate their lipid composition and localization. Cell 2014; 156( 3): 428– 439

[69] Storck EM, Özbalci C, Eggert US. Lipid cell biology: a focus on lipids in cell division. Annu Rev Biochem 2018; 87( 1): 839– 869

[70] Théry M, Bornens M. Get round and stiff for mitosis. HFSP J 2008; 2( 2): 65– 71

[71] Lee HS, Lim CJ, Puzon-McLaughlin W, Shattil SJ, Ginsberg MH. RIAM activates integrins by linking talin to ras GTPase membrane-targeting sequences. J Biol Chem 2009; 284( 8): 5119– 5127

[72] Lafuente EM, van Puijenbroek AAFL, Krause M, Carman CV, Freeman GJ, Berezovskaya A, Constantine E, Springer TA, Gertler FB, Boussiotis VA. RIAM, an Ena/VASP and Profilin ligand, interacts with Rap1-GTP and mediates Rap1-induced adhesion. Dev Cell 2004; 7( 4): 585– 595

[73] Marchesi S, Montani F, Deflorian G, D’Antuono R, Cuomo A, Bologna S, Mazzoccoli C, Bonaldi T, Di Fiore PP, Nicassio F. DEPDC1B coordinates de-adhesion events and cell-cycle progression at mitosis. Dev Cell 2014; 31( 4): 420– 433

[74] Lancaster OM, Le Berre M, Dimitracopoulos A, Bonazzi D, Zlotek-Zlotkiewicz E, Picone R, Duke T, Piel M, Baum B. Mitotic rounding alters cell geometry to ensure efficient bipolar spindle formation. Dev Cell 2013; 25( 3): 270– 283

[75] Chugh P, Paluch EK. The actin cortex at a glance. J Cell Sci 2018; 131( 14): jcs186254

[76] Arnold TR, Stephenson RE, Miller AL. Rho GTPases and actomyosin: partners in regulating epithelial cell-cell junction structure and function. Exp Cell Res 2017; 358( 1): 20– 30

[77] Rosa A, Vlassaks E, Pichaud F, Baum B. Ect2/Pbl acts via Rho and polarity proteins to direct the assembly of an isotropic actomyosin cortex upon mitotic entry. Dev Cell 2015; 32( 5): 604– 616

[78] Mierzwa B, Gerlich DW. Cytokinetic abscission: molecular mechanisms and temporal control. Dev Cell 2014; 31( 5): 525– 538

[79] Pollard TD, O’Shaughnessy B. Molecular mechanism of cytokinesis. Annu Rev Biochem 2019; 88( 1): 661– 689

[80] Neto H, Collins LL, Gould GW. Vesicle trafficking and membrane remodelling in cytokinesis. Biochem J 2011; 437( 1): 13– 24

[81] Kiyomitsu T, Cheeseman IM. Cortical dynein and asymmetric membrane elongation coordinately position the spindle in anaphase. Cell 2013; 154( 2): 391– 402

[82] Kiyomitsu T, Cheeseman IM. Chromosome- and spindle-pole-derived signals generate an intrinsic code for spindle position and orientation. Nat Cell Biol 2012; 14( 3): 311– 317

[83] Bird SL, Heald R, Weis K. RanGTP and CLASP1 cooperate to position the mitotic spindle. Mol Biol Cell 2013; 24( 16): 2506– 2514

[84] Queralt E, Uhlmann F. Cdk-counteracting phosphatases unlock mitotic exit. Curr Opin Cell Biol 2008; 20( 6): 661– 668

[85] Baumann O, Walz B. Endoplasmic reticulum of animal cells and its organization into structural and functional domains. Int Rev Cytol 2001; 205 : 149– 214

[86] Friedman JR, Voeltz GK. The ER in 3D: a multifunctional dynamic membrane network. Trends Cell Biol 2011; 21( 12): 709– 717

[87] Westrate LM, Lee JE, Prinz WA, Voeltz GK. Form follows function: the importance of endoplasmic reticulum shape. Annu Rev Biochem 2015; 84( 1): 791– 811

[88] Schwarz DS, Blower MD. The endoplasmic reticulum: structure, function and response to cellular signaling. Cell Mol Life Sci 2016; 73( 1): 79– 94

[89] English AR, Voeltz GK. Endoplasmic reticulum structure and interconnections with other organelles. Cold Spring Harb Perspect Biol 2013; 5( 4): a013227

[90] Merta H, Carrasquillo Rodríguez JW, Anjur-Dietrich MI, Vitale T, Granade ME, Harris TE, Needleman DJ, Bahmanyar S. Cell cycle regulation of ER membrane biogenesis protects against chromosome missegregation. Dev Cell 2021; 56( 24): 3364– 3379.e10

[91] Oertle T, Klinger M, Stuermer CAO, Schwab ME. A reticular rhapsody: phylogenic evolution and nomenclature of the RTN/Nogo gene family. FASEB J 2003; 17( 10): 1238– 1247

[92] Di Sano F, Bernardoni P, Piacentini M. The reticulons: guardians of the structure and function of the endoplasmic reticulum. Exp Cell Res 2012; 318( 11): 1201– 1207

[93] Voeltz GK, Prinz WA, Shibata Y, Rist JM, Rapoport TA. A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 2006; 124( 3): 573– 586

[94] Gerondopoulos A, Bastos RN, Yoshimura S, Anderson R, Carpanini S, Aligianis I, Handley MT, Barr FA. Rab18 and a Rab18 GEF complex are required for normal ER structure. J Cell Biol 2014; 205( 5): 707– 720

[95] English AR, Voeltz GK. Rab10 GTPase regulates ER dynamics and morphology. Nat Cell Biol 2013; 15( 2): 169– 178

[96] Morohashi Y, Balklava Z, Ball M, Hughes H, Lowe M. Phosphorylation and membrane dissociation of the ARF exchange factor GBF1 in mitosis. Biochem J 2010; 427( 3): 401– 412

[97] Kumar D, Golchoubian B, Belevich I, Jokitalo E, Schlaitz ALL. REEP3 and REEP4 determine the tubular morphology of the endoplasmic reticulum during mitosis. Mol Biol Cell 2019; 30( 12): 1377– 1389

[98] Schlaitz AL, Thompson J, Wong CCLL, Yates JR 3rd, Heald R. REEP3/4 ensure endoplasmic reticulum clearance from metaphase chromatin and proper nuclear envelope architecture. Dev Cell 2013; 26( 3): 315– 323

[99] Arnone JT, Walters AD, Cohen-Fix O. The dynamic nature of the nuclear envelope: lessons from closed mitosis. Nucleus 2013; 4( 4): 261– 266

[100] LaJoie D, Ullman KS. Coordinated events of nuclear assembly. Curr Opin Cell Biol 2017; 46 : 39– 45

[101] Vietri M, Stenmark H, Campsteijn C. Closing a gap in the nuclear envelope. Curr Opin Cell Biol 2016; 40 : 90– 97

[102] Hetzer MW. The nuclear envelope. Cold Spring Harb Perspect Biol 2010; 2( 3): a000539

[103] Prunuske AJ, Ullman KS. The nuclear envelope: form and reformation. Curr Opin Cell Biol 2006; 18( 1): 108– 116

[104] Peter M, Nakagawa J, Dorée M, Labbé JC, Nigg EA. Identification of major nucleolar proteins as candidate mitotic substrates of cdc2 kinase. Cell 1990; 60( 5): 791– 801

[105] Heald R, McKeon F. Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 1990; 61( 4): 579– 589

[106] Torvaldson E, Kochin V, Eriksson JE. Phosphorylation of lamins determine their structural properties and signaling functions. Nucleus 2015; 6( 3): 166– 171

[107] Martinez de Ilarduya O, Vicente-Carbajosa J, Sanchez de la Hoz P, Carbonero P. Sucrose synthase genes in barley. cDNA cloning of the Ss2 type and tissue-specific expression of Ss1 and Ss2. FEBS Lett 1993; 320( 2): 177– 181

[108] Audhya A, Desai A, Oegema K. A role for Rab5 in structuring the endoplasmic reticulum. J Cell Biol 2007; 178( 1): 43– 56

[109] Nielsen E, Severin F, Backer JM, Hyman AA, Zerial M. Rab5 regulates motility of early endosomes on microtubules. Nat Cell Biol 1999; 1( 6): 376– 382

[110] Bucci C, Parton RG, Mather IH, Stunnenberg H, Simons K, Hoflack B, Zerial M. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 1992; 70( 5): 715– 728

[111] Cavazza T, Vernos I. The RanGTP pathway: from nucleo-cytoplasmic transport to spindle assembly and beyond. Front Cell Dev Biol 2016; 3 : 82

[112] Wesolowska N, Avilov I, Machado P, Geiss C, Kondo H, Mori M, Lénárt P. Actin assembly ruptures the nuclear envelope by prying the lamina away from nuclear pores and nuclear membranes in starfish oocytes. eLife 2020; 9 : e49774

[113] Penfield L, Wysolmerski B, Mauro M, Farhadifar R, Martinez MA, Biggs R, Wu HY, Broberg C, Needleman D, Bahmanyar S. Dynein pulling forces counteract lamin-mediated nuclear stability during nuclear envelope repair. Mol Biol Cell 2018; 29( 7): 852– 868

[114] Mühlhäusser P, Kutay U. An in vitro nuclear disassembly system reveals a role for the RanGTPase system and microtubule-dependent steps in nuclear envelope breakdown. J Cell Biol 2007; 178( 4): 595– 610

[115] Beaudouin J, Gerlich D, Daigle N, Eils R, Ellenberg J. Nuclear envelope breakdown proceeds by microtubule-induced tearing of the lamina. Cell 2002; 108( 1): 83– 96

[116] Salina D, Bodoor K, Eckley DMM, Schroer TA, Rattner JBB, Burke B. Cytoplasmic dynein as a facilitator of nuclear envelope breakdown. Cell 2002; 108( 1): 97– 107

[117] Sullivan M, Morgan DO. Finishing mitosis, one step at a time. Nat Rev Mol Cell Biol 2007; 8( 11): 894– 903

[118] Zhang C, Clarke PR. Chromatin-independent nuclear envelope assembly induced by Ran GTPase in Xenopus egg extracts. Science 2000; 288( 5470): 1429– 1432

[119] Hetzer M, Gruss OJ, Mattaj IW. The Ran GTPase as a marker of chromosome position in spindle formation and nuclear envelope assembly. Nat Cell Biol 2002; 4( 7): E177– E184

[120] Bamba C, Bobinnec Y, Fukuda M, Nishida E. The GTPase Ran regulates chromosome positioning and nuclear envelope assembly in vivo. Curr Biol 2002; 12( 6): 503– 507

[121] Hetzer M, Bilbao-Cortés D, Walther TC, Gruss OJ, Mattaj IW. GTP hydrolysis by Ran is required for nuclear envelope assembly. Mol Cell 2000; 5( 6): 1013– 1024

[122] Schellhaus AK De Magistris P Antonin W. Nuclear reformation at the end of mitosis. J Mol Biol 2016; 428(10Pt A): 1962–1985 doi:10.1016/j.jmb.2015.09.016

[123] Matchett KB, McFarlane S, Hamilton SE, Eltuhamy YSA, Davidson MA, Murray JT, Faheem AM, El-Tanani M. Ran GTPase in Nuclear Envelope Formation and Cancer Metastasis. Adv Exp Med Biol 2014; 773 : 323– 351

[124] Townley AK, Feng Y, Schmidt K, Carter DA, Porter R, Verkade P, Stephens DJ. Efficient coupling of Sec23-Sec24 to Sec13-Sec31 drives COPII-dependent collagen secretion and is essential for normal craniofacial development. J Cell Sci 2008; 121( 18): 3025– 3034

[125] Siniossoglou S, Lutzmann M, Santos-Rosa H, Leonard K, Mueller S, Aebi U, Hurt E. Structure and assembly of the Nup84p complex. J Cell Biol 2000; 149( 1): 41– 54

[126] Lu MS, Drubin DG. Cdc42 GTPase regulates ESCRTs in nuclear envelope sealing and ER remodeling. J Cell Biol 2020; 219( 8): e201910119

[127] Chen X, Simon ES, Xiang Y, Kachman M, Andrews PC, Wang Y. Quantitative proteomics analysis of cell cycle-regulated Golgi disassembly and reassembly. J Biol Chem 2010; 285( 10): 7197– 7207

[128] Klumperman J. Architecture of the mammalian Golgi. Cold Spring Harb Perspect Biol 2011; 3( 7): a005181

[129] Xiang Y, Wang Y. GRASP55 and GRASP65 play complementary and essential roles in Golgi cisternal stacking. J Cell Biol 2010; 188( 2): 237– 251

[130] Colanzi A, Corda D. Mitosis controls the Golgi and the Golgi controls mitosis. Curr Opin Cell Biol 2007; 19( 4): 386– 393

[131] Tang D, Wang Y. Cell cycle regulation of Golgi membrane dynamics. Trends Cell Biol 2013; 23( 6): 296– 304

[132] Valente C, Colanzi A. Mechanisms and regulation of the mitotic inheritance of the Golgi complex. Front Cell Dev Biol 2015; 3 : 79

[133] Mao L Li N Guo Y Xu X Gao L Xu Y Zhou L Liu W. AMPK phosphorylates GBF1 for mitotic Golgi disassembly. J Cell Sci 2013; 126(Pt 6): 1498–1505 doi:10.1242/jcs.121954

[134] Yadav S, Puthenveedu MA, Linstedt AD. Golgin160 recruits the dynein motor to position the Golgi apparatus. Dev Cell 2012; 23( 1): 153– 165

[135] Kano F, Tanaka AR, Yamauchi S, Kondo H, Murata M. Cdc2 kinase-dependent disassembly of endoplasmic reticulum (ER) exit sites inhibits ER-to-Golgi vesicular transport during mitosis. Mol Biol Cell 2004; 15( 9): 4289– 4298

[136] Prescott AR, Farmaki T, Thomson C, James J, Paccaud JP, Tang BL, Hong W, Quinn M, Ponnambalam S, Lucocq J. Evidence for prebudding arrest of ER export in animal cell mitosis and its role in generating Golgi partitioning intermediates. Traffic 2001; 2( 5): 321– 335

[137] Stroud WJ, Jiang S, Jack G, Storrie B. Persistence of Golgi matrix distribution exhibits the same dependence on Sar1p activity as a Golgi glycosyltransferase. Traffic 2003; 4( 9): 631– 641

[138] Ward TH, Polishchuk RS, Caplan S, Hirschberg K, Lippincott-Schwartz J. Maintenance of Golgi structure and function depends on the integrity of ER export. J Cell Biol 2001; 155( 4): 557– 570

[139] Miles S, McManus H, Forsten KE, Storrie B. Evidence that the entire Golgi apparatus cycles in interphase HeLa cells: sensitivity of Golgi matrix proteins to an ER exit block. J Cell Biol 2001; 155( 4): 543– 556

[140] Corda D, Barretta ML, Cervigni RI, Colanzi A. Golgi complex fragmentation in G2/M transition: an organelle-based cell-cycle checkpoint. IUBMB Life 2012; 64( 8): 661– 670

[141] Persico A, Cervigni RI, Barretta ML, Corda D, Colanzi A. Golgi partitioning controls mitotic entry through Aurora-A kinase. Mol Biol Cell 2010; 21( 21): 3708– 3721

[142] Altan-Bonnet N, Sougrat R, Lippincott-Schwartz J. Molecular basis for Golgi maintenance and biogenesis. Curr Opin Cell Biol 2004; 16( 4): 364– 372

[143] Altan-Bonnet N, Sougrat R, Liu W, Snapp EL, Ward T, Lippincott-Schwartz J. Golgi inheritance in mammalian cells is mediated through endoplasmic reticulum export activities. Mol Biol Cell 2006; 17( 2): 990– 1005

[144] Magliozzi R, Carrero ZI, Low TY, Yuniati L, Valdes-Quezada C, Kruiswijk F, van Wijk K, Heck AJR, Jackson CL, Guardavaccaro D. Inheritance of the Golgi apparatus and cytokinesis are controlled by degradation of GBF1. Cell Rep 2018; 23( 11): 3381– 3391.e4

[145] Miserey-Lenkei S, Couëdel-Courteille A, Del Nery E, Bardin S, Piel M, Racine V, Sibarita JB, Perez F, Bornens M, Goud B. A role for the Rab6A′ GTPase in the inactivation of the Mad2-spindle checkpoint. EMBO J 2006; 25( 2): 278– 289

[146] Mishra P, Chan DC. Mitochondrial dynamics and inheritance during cell division, development and disease. Nat Rev Mol Cell Biol 2014; 15( 10): 634– 646

[147] Giacomello M, Pyakurel A, Glytsou C, Scorrano L. The cell biology of mitochondrial membrane dynamics. Nat Rev Mol Cell Biol 2020; 21( 4): 204– 224

[148] Kashatus DF, Lim KH, Brady DC, Pershing NLK, Cox AD, Counter CM. RALA and RALBP1 regulate mitochondrial fission at mitosis. Nat Cell Biol 2011; 13( 9): 1108– 1115

[149] Kanfer G, Kornmann B. Dynamics of the mitochondrial network during mitosis. Biochem Soc Trans 2016; 44( 2): 510– 516

[150] Benard G, Bellance N, James D, Parrone P, Fernandez H, Letellier T, Rossignol R. Mitochondrial bioenergetics and structural network organization. J Cell Sci 2007; 120( 5): 838– 848

[151] Parone PA, Da Cruz S, Tondera D, Mattenberger Y, James DI, Maechler P, Barja F, Martinou JC. Preventing mitochondrial fission impairs mitochondrial function and leads to loss of mitochondrial DNA. PLoS One 2008; 3( 9): e3257

[152] Nagashima S, Tábara LC, Tilokani L, Paupe V, Anand H, Pogson JH, Zunino R, McBride HM, Prudent J. Golgi-derived PI(4)P-containing vesicles drive late steps of mitochondrial division. Science 2020; 367( 6484): 1366– 1371

[153] Horbay R, Bilyy R. Mitochondrial dynamics during cell cycling. Apoptosis 2016; 21( 12): 1327– 1335

[154] Kanfer G, Courthéoux T, Peterka M, Meier S, Soste M, Melnik A, Reis K, Aspenström P, Peter M, Picotti P, Kornmann B. Mitotic redistribution of the mitochondrial network by Miro and Cenp-F. Nat Commun 2015; 6( 1): 8015

[155] Walch L, Pellier E, Leng W, Lakisic G, Gautreau A, Contremoulins V, Verbavatz JM, Jackson CL. GBF1 and Arf1 interact with Miro and regulate mitochondrial positioning within cells. Sci Rep 2018; 8( 1): 17121

[156] Frederick RL, Shaw JM. Moving mitochondria: establishing distribution of an essential organelle. Traffic 2007; 8( 12): 1668– 1675

[157] Kettenbach AN, Schweppe DK, Faherty BK, Pechenick D, Pletnev AA, Gerber SA. Quantitative phosphoproteomics identifies substrates and functional modules of Aurora and Polo-like kinase activities in mitotic cells. Sci Signal 2011; 4( 179): rs5

[158] Dephoure N, Zhou C, Villén J, Beausoleil SA, Bakalarski CE, Elledge SJ, Gygi SP. A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci USA 2008; 105( 31): 10762– 10767

[159] Malik R, Lenobel R, Santamaria A, Ries A, Nigg EA, Körner R. Quantitative analysis of the human spindle phosphoproteome at distinct mitotic stages. J Proteome Res 2009; 8( 10): 4553– 4563

[160] D’Avino PP, Giansanti MG, Petronczki M. Cytokinesis in animal cells. Cold Spring Harb Perspect Biol 2015; 7( 4): a015834

[161] Kechad A, Jananji S, Ruella Y, Hickson GRX. Anillin acts as a bifunctional linker coordinating midbody ring biogenesis during cytokinesis. Curr Biol 2012; 22( 3): 197– 203

[162] Steigemann P, Gerlich DW. Cytokinetic abscission: cellular dynamics at the midbody. Trends Cell Biol 2009; 19( 11): 606– 616

[163] Hu CK, Coughlin M, Mitchison TJ. Midbody assembly and its regulation during cytokinesis. Mol Biol Cell 2012; 23( 6): 1024– 1034

[164] Wadsworth P. Cytokinesis: Rho marks the spot. Curr Biol 2005; 15 : R871– R874

[165] Piekny A, Werner M, Glotzer M. Cytokinesis: welcome to the Rho zone. Trends Cell Biol 2005; 15( 12): 651– 658

[166] Jordan SN, Canman JC. Rho GTPases in animal cell cytokinesis: an occupation by the one percent. Cytoskeleton (Hoboken) 2012; 69( 11): 919– 930

[167] Narumiya S, Yasuda S. Rho GTPases in animal cell mitosis. Curr Opin Cell Biol 2006; 18( 2): 199– 205

[168] Fraschini R. Cytokinesis in eukaryotic cells: the furrow complexity at a glance. Cells 2020; 9( 2): 271

[169] Bement WM, Benink HAHA, von Dassow G. A microtubule-dependent zone of active RhoA during cleavage plane specification. J Cell Biol 2005; 170( 1): 91– 101

[170] Yüce O, Piekny A, Glotzer M. An ECT2-centralspindlin complex regulates the localization and function of RhoA. J Cell Biol 2005; 170( 4): 571– 582

[171] Yoshizaki H, Ohba Y, Kurokawa K, Itoh RE, Nakamura T, Mochizuki N, Nagashima K, Matsuda M. Activity of Rho-family GTPases during cell division as visualized with FRET-based probes. J Cell Biol 2003; 162( 2): 223– 232

[172] Kotýnková K, Su KC, West SC, Petronczki M. Plasma membrane association but not midzone recruitment of RhoGEF ECT2 is essential for cytokinesis. Cell Rep 2016; 17( 10): 2672– 2686

[173] Schroeder TE. The contractile ring. I. Fine structure of dividing mammalian (HeLa) cells and the effects of cytochalasin B. Z Zellforsch Mikrosk Anat 1970; 109( 4): 431– 449

[174] Schroeder TE. Actin in dividing cells: contractile ring filaments bind heavy meromyosin. Proc Natl Acad Sci USA 1973; 70( 6): 1688– 1692

[175] Otomo T, Otomo C, Tomchick DR, Machius M, Rosen MK. Structural basis of Rho GTPase-mediated activation of the formin mDia1. Mol Cell 2005; 18( 3): 273– 281

[176] Rose R, Weyand M, Lammers M, Ishizaki T, Ahmadian MR, Wittinghofer A. Structural and mechanistic insights into the interaction between Rho and mammalian Dia. Nature 2005; 435( 7041): 513– 518

[177] Castrillon DH, Wasserman SA. Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. Development 1994; 120( 12): 3367– 3377

[178] Evangelista M, Pruyne D, Amberg DC, Boone C, Bretscher A. Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat Cell Biol 2002; 4( 3): 260– 269

[179] Sagot I, Rodal AA, Moseley J, Goode BL, Pellman D. An actin nucleation mechanism mediated by Bni1 and profilin. Nat Cell Biol 2002; 4( 8): 626– 631

[180] Watanabe N, Madaule P, Reid T, Ishizaki T, Watanabe G, Kakizuka A, Saito Y, Nakao K, Jockusch BM, Narumiya S. p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J 1997; 16( 11): 3044– 3056

[181] Kawano Y, Fukata Y, Oshiro N, Amano M, Nakamura T, Ito M, Matsumura F, Inagaki M, Kaibuchi K. Phosphorylation of myosin-binding subunit (MBS) of myosin phosphatase by Rho-kinase in vivo. J Cell Biol 1999; 147( 5): 1023– 1038

[182] Kosako H, Yoshida T, Matsumura F, Ishizaki T, Narumiya S, Inagaki M. Rho-kinase/ROCK is involved in cytokinesis through the phosphorylation of myosin light chain and not ezrin/radixin/moesin proteins at the cleavage furrow. Oncogene 2000; 19( 52): 6059– 6064

[183] Yokoyama T, Goto H, Izawa I, Mizutani H, Inagaki M. Aurora-B and Rho-kinase/ROCK, the two cleavage furrow kinases, independently regulate the progression of cytokinesis: possible existence of a novel cleavage furrow kinase phosphorylates ezrin/radixin/moesin (ERM). Genes Cells 2005; 10( 2): 127– 137

[184] Khasnis M, Nakatomi A, Gumpper K, Eto M. Reconstituted human myosin light chain phosphatase reveals distinct roles of two inhibitory phosphorylation sites of the regulatory subunit, MYPT1. Biochemistry 2014; 53( 16): 2701– 2709

[185] Gai M, Camera P, Dema A, Bianchi F, Berto G, Scarpa E, Germena G, Di Cunto F. Citron kinase controls abscission through RhoA and anillin. Mol Biol Cell 2011; 22( 20): 3768– 3778

[186] D’Avino PP. Citron kinase—renaissance of a neglected mitotic kinase. J Cell Sci 2017; 130( 10): 1701– 1708

[187] Canman JC, Lewellyn L, Laband K, Smerdon SJ, Desai A, Bowerman B, Oegema K. Inhibition of Rac by the GAP activity of centralspindlin is essential for cytokinesis. Science 2008; 322( 5907): 1543– 1546

[188] Boucrot E, Kirchhausen T. Endosomal recycling controls plasma membrane area during mitosis. Proc Natl Acad Sci USA 2007; 104( 19): 7939– 7944

[189] Ai E, Skop AR. Endosomal recycling regulation during cytokinesis. Commun Integr Biol 2009; 2( 5): 444– 447

[190] Schiel JA, Prekeris R. Membrane dynamics during cytokinesis. Curr Opin Cell Biol 2013; 25( 1): 92– 98

[191] Sechi S, Frappaolo A, Fraschini R, Capalbo L, Gottardo M, Belloni G, Glover DM, Wainman A, Giansanti MG. Rab1 interacts with GOLPH3 and controls Golgi structure and contractile ring constriction during cytokinesis in Drosophila melanogaster. Open Biol 2017; 7( 1): 160257

[192] Cao J, Albertson R, Riggs B, Field CM, Sullivan W. Nuf, a Rab11 effector, maintains cytokinetic furrow integrity by promoting local actin polymerization. J Cell Biol 2008; 182( 2): 301– 313

[193] Rodrigues FF, Shao W, Harris TJC. The Arf GAP Asap promotes Arf1 function at the Golgi for cleavage furrow biosynthesis in Drosophila. Mol Biol Cell 2016; 27( 20): 3143– 3155

[194] Frémont S, Echard A. Membrane traffic in the late steps of cytokinesis. Curr Biol 2018; 28( 8): R458– R470

[195] Albertson R, Riggs B, Sullivan W. Membrane traffic: a driving force in cytokinesis. Trends Cell Biol 2005; 15( 2): 92– 101

[196] Montagnac G, Echard A, Chavrier P. Endocytic traffic in animal cell cytokinesis. Curr Opin Cell Biol 2008; 20( 4): 454– 461

[197] Schiel JA, Childs C, Prekeris R. Endocytic transport and cytokinesis: from regulation of the cytoskeleton to midbody inheritance. Trends Cell Biol 2013; 23( 7): 319– 327

[198] Schiel JA, Simon GC, Zaharris C, Weisz J, Castle D, Wu CC, Prekeris R. FIP3-endosome-dependent formation of the secondary ingression mediates ESCRT-III recruitment during cytokinesis. Nat Cell Biol 2012; 14( 10): 1068– 1078

[199] Minoshima Y, Kawashima T, Hirose K, Tonozuka Y, Kawajiri A, Bao YC, Deng X, Tatsuka M, Narumiya S, May WS Jr, Nosaka T, Semba K, Inoue T, Satoh T, Inagaki M, Kitamura T. Phosphorylation by aurora B converts MgcRacGAP to a RhoGAP during cytokinesis. Dev Cell 2003; 4( 4): 549– 560

[200] Yu X, Prekeris R, Gould GW. Role of endosomal Rab GTPases in cytokinesis. Eur J Cell Biol 2007; 86( 1): 25– 35

[201] Hanai A, Ohgi M, Yagi C, Ueda T, Shin HW, Nakayama K. Class I Arfs (Arf1 and Arf3) and Arf6 are localized to the Flemming body and play important roles in cytokinesis. J Biochem 2016; 159( 2): 201– 208

[202] Dambournet D, Machicoane M, Chesneau L, Sachse M, Rocancourt M, El Marjou A, Formstecher E, Salomon R, Goud B, Echard A. Rab35 GTPase and OCRL phosphatase remodel lipids and F-actin for successful cytokinesis. Nat Cell Biol 2011; 13( 8): 981– 988

[203] Frémont S, Hammich H, Bai J, Wioland H, Klinkert K, Rocancourt M, Kikuti C, Stroebel D, Romet-Lemonne G, Pylypenko O, Houdusse A, Echard A. Oxidation of F-actin controls the terminal steps of cytokinesis. Nat Commun 2017; 8( 1): 14528

[204] Montagnac G, Sibarita JB, Loubéry S, Daviet L, Romao M, Raposo G, Chavrier P. ARF6 interacts with JIP4 to control a motor switch mechanism regulating endosome traffic in cytokinesis. Curr Biol 2009; 19( 3): 184– 195

[205] Cascone I, Selimoglu R, Ozdemir C, Del Nery E, Yeaman C, White M, Camonis J. Distinct roles of RalA and RalB in the progression of cytokinesis are supported by distinct RalGEFs. EMBO J 2008; 27( 18): 2375– 2387

[206] Chen XW, Inoue M, Hsu SC, Saltiel AR. RalA-exocyst-dependent recycling endosome trafficking is required for the completion of cytokinesis. J Biol Chem 2006; 281( 50): 38609– 38616

[207] Neumann B, Walter T, Hériché JKK, Bulkescher J, Erfle H, Conrad C, Rogers P, Poser I, Held M, Liebel U, Cetin C, Sieckmann F, Pau G, Kabbe R, Wünsche A, Satagopam V, Schmitz MH, Chapuis C, Gerlich DW, Schneider R, Eils R, Huber W, Peters JM, Hyman AA, Durbin R, Pepperkok R, Ellenberg J. Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes. Nature 2010; 464( 7289): 721– 727

[208] Yang PL, Hsu TH, Wang CW, Chen RH. Lipid droplets maintain lipid homeostasis during anaphase for efficient cell separation in budding yeast. Mol Biol Cell 2016; 27( 15): 2368– 2380

[209] Brill JA, Wong R, Wilde A. Phosphoinositide function in cytokinesis. Curr Biol 2011; 21( 22): R930– R934

[210] Ben El Kadhi K, Roubinet C, Solinet S, Emery G, Carréno S. The inositol 5-phosphatase dOCRL controls PI(4,5)P2 homeostasis and is necessary for cytokinesis. Curr Biol 2011; 21( 12): 1074– 1079

[211] Field SJ, Madson N, Kerr ML, Galbraith KAA, Kennedy CE, Tahiliani M, Wilkins A, Cantley LC. PtdIns(4,5)P2 functions at the cleavage furrow during cytokinesis. Curr Biol 2005; 15( 15): 1407– 1412

[212] Zoppino FCM, Militello RD, Slavin I, Álvarez C, Colombo MI. Autophagosome formation depends on the small GTPase Rab1 and functional ER exit sites. Traffic 2010; 11( 9): 1246– 1261

[213] Ao X, Zou L, Wu Y. Regulation of autophagy by the Rab GTPase network. Cell Death Differ 2014; 21( 3): 348– 358

[214] Chua CEL, Gan BQ, Tang BL. Involvement of members of the Rab family and related small GTPases in autophagosome formation and maturation. Cell Mol Life Sci 2011; 68( 20): 3349– 3358

[215] Hutagalung AH, Novick PJ. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 2011; 91( 1): 119– 149

[216] Ganley IG, Wong PM, Gammoh N, Jiang X. Distinct autophagosomal-lysosomal fusion mechanism revealed by thapsigargin-induced autophagy arrest. Mol Cell 2011; 42( 6): 731– 743

[217] Pilli M, Arko-Mensah J, Ponpuak M, Roberts E, Master S, Mandell MA, Dupont N, Ornatowski W, Jiang S, Bradfute SB, Bruun JA, Hansen TE, Johansen T, Deretic V. TBK-1 promotes autophagy-mediated antimicrobial defense by controlling autophagosome maturation. Immunity 2012; 37( 2): 223– 234

[218] Munafó DB, Colombo MI. Induction of autophagy causes dramatic changes in the subcellular distribution of GFP-Rab24. Traffic 2002; 3( 7): 472– 482

[219] Sakurai A, Maruyama F, Funao J, Nozawa T, Aikawa C, Okahashi N, Shintani S, Hamada S, Ooshima T, Nakagawa I. Specific behavior of intracellular Streptococcus pyogenes that has undergone autophagic degradation is associated with bacterial streptolysin O and host small G proteins Rab5 and Rab7. J Biol Chem 2010; 285( 29): 22666– 22675

[220] Bento CF, Puri C, Moreau K, Rubinsztein DC. The role of membrane-trafficking small GTPases in the regulation of autophagy. J Cell Sci 2013; 126( 5): 1059– 1069

[221] Bodemann BO, Orvedahl A, Cheng T, Ram RR, Ou YH, Formstecher E, Maiti M, Hazelett CC, Wauson EM, Balakireva M, Camonis JH, Yeaman C, Levine B, White MA. RalB and the exocyst mediate the cellular starvation response by direct activation of autophagosome assembly. Cell 2011; 144( 2): 253– 267

[222] Nakashima N, Noguchi E, Nishimoto T. Saccharomyces cerevisiae putative G protein, Gtr1p, which forms complexes with itself and a novel protein designated as Gtr2p, negatively regulates the Ran/Gsp1p G protein cycle through Gtr2p. Genetics 1999; 152( 3): 853– 867

[223] Sekiguchi T, Hirose E, Nakashima N, Ii M, Nishimoto T. Novel G proteins, Rag C and Rag D, interact with GTP-binding proteins, Rag A and Rag B. J Biol Chem 2001; 276( 10): 7246– 7257

[224] Sancak Y, Bar-Peled L, Zoncu R, Markhard AL, Nada S, Sabatini DM. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 2010; 141( 2): 290– 303

[225] Sancak Y, Peterson TR, Shaul YD, Lindquist RA, Thoreen CC, Bar-Peled L, Sabatini DM. The rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 2008; 320( 5882): 1496– 1501

[226] Odle RI, Walker SA, Oxley D, Kidger AM, Balmanno K, Gilley R, Okkenhaug H, Florey O, Ktistakis NT, Cook SJ. An mTORC1-to-CDK1 switch maintains autophagy suppression during mitosis. Mol Cell 2020; 77( 2): 228– 240.e7

[227] Thiam AR, Farese RV Jr, Walther TC. The biophysics and cell biology of lipid droplets. Nat Rev Mol Cell Biol 2013; 14( 12): 775– 786

[228] Walther TC, Farese RV Jr. Lipid droplets and cellular lipid metabolism. Annu Rev Biochem 2012; 81( 1): 687– 714

[229] Martin S, Parton RG. Lipid droplets: a unified view of a dynamic organelle. Nat Rev Mol Cell Biol 2006; 7( 5): 373– 378

[230] Hashemi HF, Goodman JM. The life cycle of lipid droplets. Curr Opin Cell Biol 2015; 33 : 119– 124

[231] Cruz ALS, Carrossini N, Teixeira LK, Ribeiro-Pinto LF, Bozza PT, Viola JPB. Cell cycle progression regulates biogenesis and cellular localization of lipid droplets. Mol Cell Biol 2019; 39( 9): e00374– 18

[232] Tan R, Wang W, Wang S, Wang Z, Sun L, He W, Fan R, Zhou Y, Xu X, Hong W, Wang T. Small GTPase Rab40c associates with lipid droplets and modulates the biogenesis of lipid droplets. PLoS One 2013; 8( 4): e63213

[233] Ozeki S, Cheng J, Tauchi-Sato K, Hatano N, Taniguchi H, Fujimoto T. Rab18 localizes to lipid droplets and induces their close apposition to the endoplasmic reticulum-derived membrane. J Cell Sci 2005; 118( 12): 2601– 2611

[234] Schroeder B, Schulze RJ, Weller SG, Sletten AC, Casey CA, McNiven MA. The small GTPase Rab7 as a central regulator of hepatocellular lipophagy. Hepatology 2015; 61( 6): 1896– 1907

[235] Gabaldón T. Peroxisome diversity and evolution. Philos Trans R Soc Lond B Biol Sci 2010; 365( 1541): 765– 773

[236] Knoblach B, Rachubinski RA. How peroxisomes partition between cells. A story of yeast, mammals and filamentous fungi. Curr Opin Cell Biol 2016; 41 : 73– 80

[237] Nguyen T, Bjorkman J, Paton BC, Crane DI. Failure of microtubule-mediated peroxisome division and trafficking in disorders with reduced peroxisome abundance. J Cell Sci 2006; 119( 4): 636– 645

[238] Asare A, Levorse J, Fuchs E. Coupling organelle inheritance with mitosis to balance growth and differentiation. Science 2017; 355( 6342): eaah4701

[239] Heasman SJ, Ridley AJ. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 2008; 9( 9): 690– 701

[240] Castro IG, Richards DM, Metz J, Costello JL, Passmore JB, Schrader TA, Gouveia A, Ribeiro D, Schrader M. A role for mitochondrial Rho GTPase 1 (MIRO1) in motility and membrane dynamics of peroxisomes. Traffic 2018; 19( 3): 229– 242

[241] Schollenberger L, Gronemeyer T, Huber CM, Lay D, Wiese S, Meyer HE, Warscheid B, Saffrich R, Peränen J, Gorgas K, Just WW. RhoA regulates peroxisome association to microtubules and the actin cytoskeleton. PLoS One 2010; 5( 11): e13886

[242] Just WW, Peränen J. Small GTPases in peroxisome dynamics. Biochim Biophys Acta 2016; 1863( 5): 1006– 1013

[243] Gronemeyer T, Wiese S, Grinhagens S, Schollenberger L, Satyagraha A, Huber LA, Meyer HE, Warscheid B, Just WW. Localization of Rab proteins to peroxisomes: a proteomics and immunofluorescence study. FEBS Lett 2013; 587( 4): 328– 338

[244] Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001; 2( 2): 107– 117

[245] Cussac D, Leblanc P, L’Heritier A, Bertoglio J, Lang P, Kordon C, Enjalbert A, Saltarelli D. Rho proteins are localized with different membrane compartments involved in vesicular trafficking in anterior pituitary cells. Mol Cell Endocrinol 1996; 119( 2): 195– 206

[246] Croisé P, Estay-Ahumada C, Gasman S, Ory S. Rho GTPases, phosphoinositides, and actin: a tripartite framework for efficient vesicular trafficking. Small GTPases 2014; 5( 2): e29469

[247] Wittinghofer A. Ras Superfamily Small G Proteins: Biology and Mechanisms 1: general features, signaling. Springer Vienna, 2014

[248] Zhou B Cox AD. Posttranslational modifications of small G proteins. In: Wittinghofer A. Ras Superfamily Small G Proteins: Biology and Mechanisms 1. Springer Vienna, 2014: 99– 131

[249] Barr F, Lambright DG. Rab GEFs and GAPs. Curr Opin Cell Biol 2010; 22( 4): 461– 470

[250] Eathiraj S, Pan X, Ritacco C, Lambright DG. Structural basis of family-wide Rab GTPase recognition by rabenosyn-5. Nature 2005; 436( 7049): 415– 419

[251] Spang A, Saw JH, Jørgensen SL, Zaremba-Niedzwiedzka K, Martijn J, Lind AE, van Eijk R, Schleper C, Guy L, Ettema TJG. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 2015; 521( 7551): 173– 179

Acknowledgements

We would like to thank Mr. Christopher M. Lavender and Dr. Yuchen Zhang for critically reading our manuscript, and members of the Liu Q laboratory for scientific advice. Space constraints limited the number of citations. We apologize to those whose work we are unable to cite. This research work is supported by the National Key R&D Program of China (Nos. 2019YFA0110300 and 2017YFA0505600-04), the National Natural Science Foundation of China (Nos. 81820108024 and 81630005), the Innovative Research Team in University of Ministry of Education of China (No. IRT-17R15), and the Natural Science Foundation of Guangdong (Nos. 2016A030311038 and 2017A030313608).

Compliance with ethics guidelines

Zijian Zhang, Wei Zhang, and Quentin Liu declare no competing interest. This manuscript is a review article and does not involve a research protocol requiring approval by the relevant institutional review board or ethics committee.

RIGHTS & PERMISSIONS

2022 Higher Education Press