The Role of Molecular Microtubule Motors and the Microtubule Cytoskeleton in Stress Granule Dynamics

Table 1

Cytoskeletal-associated proteins that participate in SG dynamics. All proteins in this table localize to SGs. Assembly factors are shown in (a), disassembly factors are shown in (b), and proteins associated with SGs but with additional functions in SG dynamics are shown in (c). Cytoskeletal-associated proteins that functioned in SG coalescence were not identified, but publications demonstrating the importance of microtubule function in SG coalescence are suggestive of molecular motors aiding in this process.

(a) Assembly factors/phenotypes

Protein	Function	Cytoskeletal-association
CPEB	Translational regulator; OX induces SG formation; binding partners: RCK, eIF4E, FXR1P [32]	MT-associated [42]
DIC1/DHC1	Required for SG formation; transport [43–45]	MT-associated molecular motor [46]
DIS1	May function as a translational regulator; OX promotes assembly of SGs; binding partner eIF3h [47]	MT-associated [48]
eIF4A	An RNA helicase required for ribosome recruitment; inhibition induces SG formation [35]	Cytoskeletal-associated [49]
FMRP	Functions in mRNA transport or translation; OX induces SG formation; binding partners Ago2, RISC [28]	Cytoskeletal-associated [50, 51]
Grb7	Translational regulator; K/D inhibits SG formation; stimulates SG formation by stabilizing TIA-1 aggregates and enhancing SG or RNP integrity [52]	Cytoskeletal-associated [53]
Pumilio 2	Translational inhibitor; OX induces SGs; K/D interferes with SG formation [54]	MT-associated [54]
Smaug1	Translational repressor; OX induces SG formation [55]	Cortical cytoskeletal-associated [55]
Staufen	mRNA binding, transport, and decay; OX impairs SG formation; depletion facilitates SG assembly [56]	MT-associated [56, 57]
SMN	Assembly of small mRNP complexes; OX induces SG [33]	Role in actin dynamics [58]
TDP-43	OX induces SG; K/D has no effect on formation [59]	Role in microtubule organization [60]

(b) Disassembly factors/phenotypes

Protein	Function	Cytoskeletal-association
FAK	K/D impairs SG disassembly; FAK activity causes Grb7 phosphorylation and SG disassembly in recovering cells [52]	Role in actin assembly/microtubule organization [61, 62]
KHC/KLC	Required for SG dissolution; K/D inhibits SG disassembly; transport [44]	MT-associated molecular motor [63]
Dynein	Inhibition affects dissolution; transport [43–45]	MT-associated molecular motor [46]

(c) Factors with additional roles in SG dynamics

Protein	Function	Cytoskeletal-association
eIF2B	Guanine nucleotide exchange factor for eIF2 [27]	Cytokeletal-associated [64]
eIF3	Recruited to SGs during disassembly [5, 27]	MT-associated [49]
eIF4E	mRNA 5′ cap binding protein [65]	Cytoskeletal-associated [66]
eIF4G	Early translation initiation factor [67]	Roles in F-actin localization/microtubule organization [68]
FXR1P	FRMP-associated protein [28]	MT-associated [50]
FXR2P	FMRP-associated protein [28]	MT-associated [50]
Hsp27	Granzyme-associated molecular chaperone [69]	Cytoskeletal-associated [70, 71]
HuD	ELAV/Hu family of RNA-binding proteins, mRNA localization [72]	MT-associated [73]
NAT1/p97	Related to eIF4G, translational repressor activated in apoptosis [74]	MT-associated [75]
PABP-1	Initiation factor binds poly(A) tail [38]	Binds mRNA to MT [76]
PMR1	mRNA decay endonuclease forms a complex with TIA-1 [77]	Cytoskeletal-associated through binding partners [78]
RACK1	Allows survival of stressed cells [1, 79]	Required for astral MT length [80]
Sam68	Nuclear RNA-binding protein [81]	Roles in cytoskeleton organization [82]
TRAF2	Allows survival of stressed cells [1, 83]	Regulates actin cytoskeleton [84]
Xrn1	5′-3′ exoribonuclease I [31, 85]	MT-associated [86]
YB1	SG stability [87, 88]	Binds mRNA to microtubules [76]
ZBP1	RNA-binding protein important for localized translation [89]	MT-associated [90]