Fine-tuning cell organelle dynamics during mitosis by small GTPases
Zijian Zhang1, Wei Zhang2, Quentin Liu1,3()
1. Sun Yat-sen University Cancer Center; State Key Laboratory of Oncology in South China; Collaborative Innovation Center for Cancer Medicine, Guangzhou 510060, China 2. Department of Clinical Immunology, The Third Affiliated Hospital, Sun Yat-sen University, Guangzhou 510630, China 3. Institute of Cancer Stem Cell, Dalian Medical University, Dalian 116044, China
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.
RanGTP recruits essential centrosome and kinetochore components and releases and activates spindle assembly factors to nucleate, bind, and organize nascent spindle microtubules
[13,36–41]
Cdc42
Bi-orientation and stabilization of spindle microtubule attachment to kinetochores, spindle assembly, and spindle orientation
[42,43]
RhoA
Maintenance of spindle orientation
[42]
Rab5
Regulation of the astral microtubule size and spindle alignment
[45]
Rab11
Bringing microtubule-nucleating factors and spindle pole proteins to spindle poles
[44,46,47]
Arl8A, Arl8B
Centrosome maturation and chromosome segregation
[48,49]
RalA
Regulation of the kinetochore–microtubule interaction in early mitosis
[50]
Plasma membrane
Rap1
Focal adhesion assembly–disassembly
[25,71,72]
RhoA
Actomyosin cortex organization beneath the plasma membrane during mitosis
[73,76,77]
Ran
Polar cortex relaxation and ingression furrow position
Rac1
Repolarization of the actomyosin cortex
[69,80]
ER & nuclear envelope
Rab5
ER membrane remodeling and NEBD. Rab5 depletion inhibits nuclear envelope disassembly
[108]
Ran
Ran activities regulate microtubule dynamics and the mechanical rupture of nuclear envelope during NEBD. After division, Ran promotes the assembly of NPCs and vesicle fusion
[114,118–123]
Cd42
Nuclear envelope sealing and ER remodeling
[126]
Golgi apparatus
Arf1
Participation in the Golgi cycle through the regulation of vesicle transportation
[96,133,134]
Sar1
Participation in the Golgi cycle through the regulation of vesicle transportation
Promotion of mitochondrial fission during mitotic entry
[21]
Arf1
Recruitment of PI(4)P-containing vesicles at ER-mitochondria contact site and promotion of mitochondrial fission
[152]
Miro
Miro1 and Miro2 bind CENP-F and associate with microtubule-growing tips. Miro loss decreases the spreading of the mitochondrial network and causes cytokinesis-specific defects
[154]
Midbody
RhoA
Position of ingression furrow and membrane ingression and abscission
[161,169–172,175,176]
Rac1
Membrane ingression. The overexpression of constitutively active Rac1 causes multinucleation and cytokinesis failure
[42,187,192]
Rab1
Rab1 facilitates new membrane supplementation along the ingressing cleavage furrow
[191]
Rab11
Through en dosome transport to facilitate furrow ingression and F-actin elimination for final abscission
[192,194,198,200,201]
Rab35
Through endosome transport to facilitate F-actin elimination for final abscission
[194,200–202]
Arf1
Golgi organization and Golgi output for ingression furrow function
[193]
Arf6
Bridge stability and abscission
[65,204]
RalA & RalB
RalA and RalB control the exocyst localization at the furrow and midbody, respectively. Their collaboration is required for abscission completion
[205,206]
Autophagosome
Rabs & Sec4
Autophagosome formation. Role in mitosis is unknown
[212–215]
Rab7, Rab8B & Rab24
Autophagosome maturation. Role in mitosis is unknown
[213,214,216–219]
Arfs & Sar1
Autophagosome biogenesis and cellular localization. Role in mitosis is unknown
[213,220]
Peroxisomes
Rho, Rab, Arf & Miro
In the interphase, small GTPases regulate peroxisome distribution and biogenesis. The disruption of spindle pole localization of peroxisomes impairs spindle orientation. The direct role in mitosis is unclear
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