The microtubule-associated C-I subfamily of TRIM proteins and the regulation of polarized cell responses

Advances in Experimental Medicine and Biology

Volumn 770, Issue , 2012, Pages 105-118

  Cox, Timothy C ^a,b,c  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^c MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA4 PROTEIN; BINDING PROTEIN; CELL PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN MID1; PROTEIN MID2; PROTEIN MIG12; PROTEIN TNL; PROTEIN TRIM; PROTEIN TRIM36; PROTEIN TRIM9; REGULATOR PROTEIN; TRIFIC PROTEIN; UNCLASSIFIED DRUG; PROTEIN;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; COMPLEX FORMATION; GENE; HUMAN; MICROTUBULE; MID1 GENE; MID2 GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; ANIMAL; CELL POLARITY; CHEMISTRY; METABOLISM; PROTEIN BINDING; PROTEIN MOTIF; REVIEW;

AMINO ACID MOTIFS; ANIMALS; CELL POLARITY; HUMANS; MICROTUBULES; PROTEIN BINDING; PROTEINS;

MLCS; MLOWN;

EID: 84878902455     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4614-5398-7_8     Document Type: Article

References (78)

1. I. Meroni G, Diez-Roux G. TRIM/RBCC, a novel class of ' single protein RING finger' E3 ubiquitin ligases. Bioessays 2005; 27 (11):1147-1 157.
2. Reymond A, Meron i G, Fantozz i A, et al. The tripartite motiffamily identifies cell compartments . EMBO J 2001 ; 20(9):2140-21 51.
3. Short KM, Cox TC. Subclassification of the RBCC/TRIM superfamily reveals a novel motif necessary for microtubule binding. J Bioi Che rn 2006 ; 281(13):8970-8980.
4. Lerner M, Corcoran M, Cepeda D, et al. The RBCC gene RFP2 (Leu5) encodes a novel transmembrane E3 ubiquitin ligase involved in ERAD. Mol BioI Cell 2007; 18(5):1670-1682.
5. Palmer S, Perry J, Kipling D, et al. A gene spans the pseudoautosomal boundary in mice. Proe Natl Acad Sci USA 1997; 94(22):12 030-12035 .
6. Quaderi NA, Schweiger S, Gaude nz K, et al. Opitz G/BBB syndrome, a defect of midline develo pment, is due to mutations in a new RING finger gene on Xp22. Nat Genet 1997; 17(3):285-29 1.
7. De Falco F, Cainarea S, Andolfi G, et al. X-linke d Opitz syndrome:novel mutations in the MIDI gene and redefinition of the clinical spectrum. Am J Med Genet A 2003; 120A(2):222-228.
8. So J, Suckow V, Kijas Z, et al. Mild phenotypes in a series of patients with Opitz GBBB syndrome with MIDI mutations. Am J Med Genet A 2005; 132A(I):1-7.
9. Cox TC, Allen LR, Cox LL, et al. New mutations in MIDI provi de support for loss offunetion as the cause of X-Iinked Opitz syndrome. Hum Mol Genet 2000; 9 (17):2553-2562.
10. Liu J, Prickett TD, Elliott E, et al. Phosphorylation and micro tubule associa tion of the Opitz syndrome protein mid-I is regulated by protein phosphatase 2A via binding to the regulatory subunit alpha 4. Proc Natl Acad Sci USA 200 I; 98(12) :6650-6655
11. ShortKM,Hopwood B,YiZ, et al.MIDI andMID2 homo-andheterodimerise to tether the rapamycin-sensitive PP2A regulatory subunit, alpha 4, to micro tubules:implieations for the clinical variability of X-linked Opitz GBBB syndrome and other developme ntal disorders. BMC Cell Bioi 2002 ; 3(1) :1.
12. Trockenbacher A, Suckow V, Foerster J, et al. MID I, mutated in Opitz syndrome, encodes an ubiquitin ligase that targets phosphatase 2A for degradation. Nat Genet 2001; 29(3):287-294.
13. Landry JR, Rouhi A, Medstrand P, et al. The opitz syndrome gene midI is transcribed from a human endogenous retroviral promoter. Mol BioI Evol 2002; 19 (II) :1934-1942.
14. Dal Zotto L, Quaderi NA, Elliott R, et al. The mouse Midigene: implieations for the pathogenesis of Opitz syndro me and the evolution of the mammalian pseudoautosomal region. Hum Mol Genet 1998; 7(3): 489-499.
15. Pinson L, Auge J, Audollent S, et al. Embryonic expressio n of the human MIDI gene and its mutations in Opitz syndrome. J Med Genet 2004; 41(5):38 1-386.
16. Richman JM, Fu KK, Cox LL, et al. Isolation and characterisation of the chick ortholog ue of the Opitz syndro me gene, Mid I, supports a conse rved role in vertebrate deve lopment. Int J Dev Bioi 2002; 46(4) : 441-448.
17. Suzuki M, 1·lara Y, Takagi C, et al. MIDI and MID2 are req uired for Xenopus neural tube closure through the regulation of microtubule organization. Develo pment 2010; 137(14):2329-2339.
18. Granata A, Quaderi NA. The Opitz syndrome gene MID I is essential for establish ing asymme tric gene expression in Hensen's node. Dev BioI 2003; 258(2):397-405.
19. Granata A, Savery D, Hazan J, et al. Evidence offunetional redundancy betweenMID proteins:implications for the presentation ofOpitz syndro me. Dev Bioi 2005; 277(2):417-424.
20. Buchner G, Montini E, Andolfi G, et al. MID2, a homologue of the Opitz syndrome gene MID I:similarities in subcellular localization and differences in expression during development. Hum Mol Genet 1999; 8(8):1397-1407.
21. Perry J, Short KM, Romer JTet al. FXY2/MID 2, a gene related to the X-linked Opitz syndrome gene FXYI MID I, maps to Xq22 and encodes a FNIII domain-conta ining protein that assoc iates with micro tubules. Genomics 1999; 62(3):385-394.
22. Cox TC. unpublished data.
23. Lancioni A, Pizzo M, Fontanella B, et al. Lack of Mid I, the mouse ortho log of the Opitz syndrome gene, causes abnormal deve lopment ofthe anterior cerebellar vermis. J Neurosci 2010; 30(8) :2880-2887.
24. Berti C, Fonta nella B, Ferrenti no Ret al. Mig l2, a novelOpitz syndrome gene product partner, is expressed in the embryonic ventral midline and co-operates with Mid I to bundle and sta bilize miero tubules. BMC Cell BioI 2004; 5:9.
25. Conway G. A nove l gene expressed during zebrafis h gastrulation identified by differential RNA display. Mech Dev 1995; 52(2-3):383-391.
26. Il ayes JM, Kim SK, Abitua PB, et al. Identification of nove l eiliogenes is factors using a new in vivo model for mucociliary epithelial development. Dev BioI 2007; 312(1): 115-130.
27. Aipoalani DL, O'Callaghan BL, et al. Overlap ping roles of the glucose-responsive genes, S I4 and SI4R, in hepatic lipogenesis, Endocrinology 2010; 151(5):2071 -2077.
28. Inoue J, Yamasaki K, Ikeuchi E, et al. Identification of MIG 12 as a mediator for stimulation of lipogenesis by LXR activation. Mol Endocri nol2011; 25(6) :995-1005 .
29. Kim CW, Moon YA, Park SW, et al. Induced polymerization of mammalian acetyl-CoA carboxylase by MIG 12 provides a tertiary level of regulation offatty acid synthesis. Proc Nat! Acad Sci USA 2010; 107(21):9626 -963 1.
30. Kong M, Ditswort h 0, Lindsten T, et al. Alpha4 is an essential regulator of PP2A phosphatase activity. Mol Cell 2009; 36(1):51-60
31. Murata K, Wu J, Brautigan DL. B cell receptor-associated protein alpha 4 displays rapamycin-scns itive bindi ng directly to the catalytic subunit of protein phosphatase 2A. PNAS 1997; 94(20):106 24-10629.
32. Nana hoshi M, Tsuj ishita Y, Tokunaga C, et al. Alpha4 protein as a common regulator of type 2A-related serine/threonine protein phosphatases. FEBS Lett 1999; 446(1):108-112.
33. Virshup OM, Shenol ikar S. From promiscuity to precis ion:protein phosphatases get a makeover. Mol Cell 2009; 33(5):537-545.
34. Prickett TO, Brautigan DL. The alpha4 regulatory subunit exerts opposing allosteric effects on protein phosphatases LL6 and PP2A. J BioI Chern 2006; 28 1(41):30503-305 11.
35. McConnell JI., Watkins GR, Soss SE, et al. Alpha4 is a ubiquitin-binding protein that regulates protein serine/threonine phosphatase 2A ubiquitination. Biochemistry 2010; 49(8):1713-1718.
36. LeNoue -Newton M, Watkins GR, Zou I, et al. The E3 ubiquitin ligase-and protein phosphatase 2A (PP2A)-binding domains ofthe Alpha4 protein are both required for Alpha4 to inhibit PP2A degradation. J BioI Chern 201 1; 286(20) :17665-17671 .
37. Han X, Du H, Massiah MA. Detection and characterization of the in vitro e3 ligase activity of the human MID I protein. J Mol BioI 20 I I; 407(4) :505-520.
38. Liu E, Knutzen CA, Krauss S, et al. Control ofmTORC 1 signaling by the Opitz syndrome protein MIDI. Proc Natl Acad Sci USA 20 11; 108(2 1):8680-8685.
39. Zonc u R, Efeyan A, Sabatini OM. mTOR:from growth signal integration to cancer, diabetes and ageing . Nat Rev Mol Cell BioI 201 I ; 12(1):21-35.
40. Gayle SS, Arnold SL,O'R egan RM, et al. Pharmacologic inhibition ofmTOR improves lapatinib sensitivity in HER2-ove rexpress ing breast cancer cells with primary trastuzumab resistance. Anticancer Agents Med Chern 20 12; 12(2):151-162
41. Hussein O., Tiedemann K, Murshe d Met al. Rapamycin inhibits osteo lysis and improves surv ival in a model of experimental bone metastases. Cancer Lett 20 12; 314(2): 176-184.
42. Trapc AI', Katayama ML, Roela RA et al. Gene express ion profile in response to doxorubicin-rapa mycin combined treatment of HER-2-overexpressing human mammary epithelial cell lines. Mol Cancer Ther 2012; 11(2):464-474 .
43. Dowling RJ, Topisirovic I, Fonseca BD, et al. Dissecti ng the role ofmTOR:lessons from mTOR inhibitors . Biochim Biophys Acta 2010; 1804(3):433-439.
44. Jiang Y, Broach Jr. Tor proteins and protein phosphatase 2A reciprocally regulate Tap42 in controlling cell growth in yeas t. EMBO J 1999; 18(10):2782-2792.
45. YanG, Shen X, Jiang Y. Rapamycin activat es Tap42-asso ciated phosphatase s by abrogati ng their associatio n with Tor complex 1.EMBO J 2006; 25(15) :3546-3555.
46. Jacinto E, Hall MN. Tor signalling in bugs, brain and brawn. Nat Rev Mol Cell Bioi 2003; 4(2):117-126 .
47. Yamashita T, Inui S, Maeda K, et al. The heterodimer ofalpha4 and PP2Ac is assoc iated with S6 kinase I in B cells. Biochem Biophys Res Commun 2005; 330(2):439 -445.
48. McDonald WJ, Sangster SM, Moffat LD, et al. alpha4 phosphoprotein interacts with EDD E3 ubiquitin ligase and poly(A)-b inding protein. J Cell Biochem 20 10; 110(5):1123-1129.
49. Aranda-Orgilles B, Trockenbacher A, Winter Jet al. The Opitz syndrome gene prod uct MIDI assemb les a microtubule-associated ribonucleoprotein complex. Hum Genet 2008; 123(2):163-176.
50. Aranda-Orgilles B, Rutschow 0, Zeller R, et al. Protein phosphatase 2A (PP2A) -spccific ubiquitin ligase MIDI isa sequence-dependent regulator oftranslationefficiency controlling3-phosphoinositide-dependent protein kinase-I (PDPK-I). J BioI Chern 201 1; 286(46) :39945-39957 .
51. Lewis TS, Shapiro PS, Ahn NG. Signal transduction through MAP kinase cascades. Adv Cancer Res 1998; 74:49-139.
52. Sutherland C. What Are the bona fide GSK3 Substrates? Int J Alzheimers Dis 2011; 2011:505607.
53. Aranda-Orgilles B, Aigner J, Kunath M, et al. Active transport of the ubiquitin ligase MID I along the microtub ules is regulated by protein phosphatase 2A. PIoS One 2008; 3(10):e3507 .
54. LiY, Chin I.S, Weige lC, et al. Spring, anovcl RING fingcrprotcin thatrcgulates synapticvesiclc exocytosis. J Bioi Chern 2001; 276(44):4082 4-40833.
55. Chen YA, Scheller RH. SNAR E-mediated membrane fusion. Nat Rev Mol Cell Bioi 200 I; 2(2):98 -106.
56. Cah ill AL, Herri ng BE, Fox AP. Stable silencing ofSNAP-25 in PCI 2 cells by RNA interference. BMC Neurosci 2006; 7:9.
57. Tao-Cheng JH, Du J, McBain CJ. Snap-25 is polarized to axons and abundant along the axolemma:an immunogold study of intact neurons. J Neurocytol2000; 29(1):67-77.
58. Dhingra V, Li X, Liu Y, et al. Proteomic profiling reveals that rabies virus infection results in di fferential expression of host proteins involved in ion homeostasis and synaptic physiology in the centra l nervous system. J Neurovirol 2007 ; 13(2):I07-117.
59. Tanji K, Kamitani T, Mori F, et al. TRIM9, a novel brain-specific E3 ubiquitin ligase, is repressed in the brain of Parkinson's disease and dementia with Lewy bod ies. Neuro biol Dis 20 10; 38(2) :210-218.
60. Schlossmac her MG, Frosch MP, Gai WP, et al. Parkin localizes to the Lewy bodies of Parkinson disease and dementia with Lewy bodies. AM J Patho12002 ; 160(5): 1655-1667
61. Spillantini MG, Schmidt ML, Lee VM, et al. Alpha-synucle in in Lewy bodies. Nature 1997; 388(6645): 839-840.
62. Fanelli M, Fantozzi A, De Luca P, et al. The coiled-coi l domain is the structura l determinant for mammalian homologues of Drosophila Sina-mediated degradation of promyelocytic leukemia protein and other tripartite motif proteins by the proteasome. J Bioi Chern 2004; 279(7) :5374-5379 .
63. Alexander M, Selman G, Seetharaman A, et al. MADD-2, a homolog ofthe Opitz syndrome protein MIDI, regulates guidance tothemidIine through UNC-40 inCaenorhabditiselegans. DevCell2010; 18(6):96 1-972.
64. Hao JC, Adler CE, Mebane L, et al. The tripartite motif protein MADD-2 functio ns with the receptor UNC-40 (DCC) in Netrin-mediated axon attraction and branching. Dev Cell 20 10; 18(6): 950-960.
65. Song S, Ge Q, Wang J, et al. TRIM-9 functions in the UNC-6/UNC -40 pathway to regula te ventral guidance. J Genet Genomics 2011; 38(1):1-11.
66. Sun KLW, CorreiaJP, Kennedy TE.Netrins:versatileextrace llularc ueswith diverse functions. Development 2011; 138(1 1):2 153-2169 .
67. Chang C, Adler CE, Krause M, et al. MIG-IO/lamellipodin and AGE-I/P13K promote axon guidance and outgrowt h in response to slit and netrin. Curr BioI 2006; 16(9):854-862.
68. Quinn CC, Pfeil OS, Chen E, et al. UNC-6/netrin and SLT-l/sl it guidance cues orient axon outgrowth mediated by MIG-IO/RIAM/lamellipodin. Curr BioI 2006; 16(9):845-853.
69. Quinn CC, Wadsworth WG. Axon guidance:asymmetric signaling orients polarized outgrowth. Trends Cell BioI 2008; 18(12):597-603.
70. Tcherkezian J, Brittis PA, Thomas F, et al. Transmembrane receptor DCC assoc iates with protein synthes is machinery and regulates translation. Cell 20 10; 141(4):632-644.
71. Kitamura K, Tanaka H, Nishimune Y. Haprin, a novel haploid germ cell-speci fic RING finger protein involved in the acroso me reaction. J BioI Chern 2003 ; 278(45):444 17-44423.
72. Kierszen baum AL. Fusion of membranes during the acrosome reaction: A tale of two SNAREs. Mol Reprod Dev 2000; 57(4):309-310.
73. Kitamura K, Tanaka H, Nishimune Y.The RING-finger protein haprin:domains and function inth e acrosome react ion.Curr Protein Pept Sci 2005 ; 6(6) :567-57 4.
74. Cuy kendall TN, Houston OW. Vegetally localized Xenopus trim36 regula tes cortical rotation and dorsal axis formation . Develo pment 2009; 136(18) :3057-3065.
75. Yoshigai E, Kawamura S, Kuhara S, et al. Trim36/llaprin plays a critica l role in the arrange ment of somites during Xeno pus embryogenesis. Biochem Biophys Res Commun 2009; 378(3) :428-432.
76. Kong M, Bui TV, Ditswo rth Det al. The PP2A-associated protein alpha4 plays acritica l role in the regulation of cell spreading and migration . J BioI Chern 2007; 282(40) :29712-29720 .
77. Miyajima N, Maruyama S, Nonomura K, et al. TRIM36 interacts with the kinetochore protein CENP-H and delays cell cycle progression. Biochem Biophys Res Commun 2009; 381(3):383-387.
78. Sakamoto T, Uezu A, Kawauchi S, et al. Mass spectrometric analys is of microtubule cosed imented proteins from rat brain. Genes Cells 2008; 13(4):295-3 12.