The centrosome in human genetic disease

The centrosome is an indispensable component of the cell-cycle machinery of eukaryotic cells, and the perturbation of core centrosomal or centrosome-associated proteins is linked to cell-cycle misregulation and cancer. Recent work has expanded our understanding of the functional complexity and importance of this organelle. The centrosomal localization of proteins that are involved in human genetic disease, and the identification of novel centrosome-associated proteins, has shown that numerous, seemingly unrelated, cellular processes can be perturbed by centrosomal dysfunction. Here, we review the mechanistic relationship between human disease phenotypes and the function of the centrosome, and describe some of the newly-appreciated functions of this organelle in animal cells.

[1]  G. Pihan,et al.  Centrosome abnormalities and chromosome instability occur together in pre-invasive carcinomas. , 2003, Cancer research.

[2]  A. Takatsuki,et al.  Possible implication of Golgi-nucleating function for the centrosome. , 2002, Biochemical and biophysical research communications.

[3]  M. Tohyama,et al.  DISC1 localizes to the centrosome by binding to kendrin. , 2004, Biochemical and biophysical research communications.

[4]  M. Slovak,et al.  Detection of NPM/MLF1 fusion in t(3;5)-positive acute myeloid leukemia and myelodysplasia. , 2003, Human pathology.

[5]  A. Ishikawa,et al.  Clinical analysis of 17 patients in 12 Japanese families with autosomal-recessive type juvenile parkinsonism , 1996, Neurology.

[6]  E. Hinchcliffe,et al.  "It takes two to tango": understanding how centrosome duplication is regulated throughout the cell cycle. , 2001, Genes & development.

[7]  P. Lansbury,et al.  NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded. , 1996, Biochemistry.

[8]  M Tohyama,et al.  Disrupted-In-Schizophrenia 1, a candidate gene for schizophrenia, participates in neurite outgrowth , 2003, Molecular Psychiatry.

[9]  G. Schatten,et al.  LIS1 association with dynactin is required for nuclear motility and genomic union in the fertilized mammalian oocyte. , 2003, Cell motility and the cytoskeleton.

[10]  L. M. May,et al.  Distribution of microtubule organizing centers in migrating sheets of endothelial cells , 1981, The Journal of cell biology.

[11]  R. Palazzo.  Centrosome and spindle pole body dynamics: A review of the EMBO/EMBL conference on centrosomes and spindle pole bodies, Heidelberg, September 13-17, 2002 , 2003 .

[12]  R. Ellis,et al.  Macromolecular crowding: an important but neglected aspect of the intracellular environment. , 2001 .

[13]  A. Merdes,et al.  Assembly of centrosomal proteins and microtubule organization depends on PCM-1 , 2002, The Journal of cell biology.

[14]  S. Baker,et al.  The intraflagellar transport protein, IFT88, is essential for vertebrate photoreceptor assembly and maintenance , 2002, The Journal of cell biology.

[15]  Naoyuki Taniguchi,et al.  Dorfin Ubiquitylates Mutant SOD1 and Prevents Mutant SOD1-mediated Neurotoxicity* , 2002, The Journal of Biological Chemistry.

[16]  A. Davies,et al.  Organization, expression and polymorphism of the human persyn gene. , 1998, Human molecular genetics.

[17]  Li-Huei Tsai,et al.  NUDEL Is a Novel Cdk5 Substrate that Associates with LIS1 and Cytoplasmic Dynein , 2000, Neuron.

[18]  J. Rosenbaum,et al.  Intraflagellar transport , 2002, Nature Reviews Molecular Cell Biology.

[19]  C. Tabin,et al.  Mechanisms of Left–Right Determination in Vertebrates , 2000, Cell.

[20]  M. Gambello,et al.  14-3-3epsilon is important for neuronal migration by binding to NUDEL: a molecular explanation for Miller-Dieker syndrome: a molecular explanation for Miller-Dieker syndrome , 2003 .

[21]  N. Katsanis.  The oligogenic properties of Bardet-Biedl syndrome. , 2004, Human molecular genetics.

[22]  C A Ross,et al.  Synphilin‐1 is present in Lewy bodies in Parkinson's disease , 2000, Annals of neurology.

[23]  E. Nigg.  Centrosomes in Development and Disease: NIGG:CENTROSOMES O-BK , 2004 .

[24]  L. Engle,et al.  Cloning, analysis, and chromosomal localization of myoxin (MYH12), the human homologue to the mouse dilute gene. , 1994, Genomics.

[25]  R. Crowther,et al.  α-Synuclein in filamentous inclusions of Lewy bodies from Parkinson’s disease and dementia with Lewy bodies , 1998 .

[26]  久保亮治.  Centriolar satellites : molecular characterization, ATP-dependent movement toward centrioles and possible involvement in ciliogenesis , 2000 .

[27]  N. Morris,et al.  Nuclear migration, nucleokinesis and lissencephaly. , 1998, Trends in cell biology.

[28]  Bethan E. Hoskins,et al.  Loss of BBS proteins causes anosmia in humans and defects in olfactory cilia structure and function in the mouse , 2004, Nature Genetics.

[29]  O. Reiner,et al.  Reduction of microtubule catastrophe events by LIS1, platelet‐activating factor acetylhydrolase subunit , 1997, The EMBO journal.

[30]  R. Fischer,et al.  Accumulation of cytoplasmic dynein and dynactin at microtubule plus ends in Aspergillus nidulans is kinesin dependent. , 2003, Molecular biology of the cell.

[31]  H. Joshi,et al.  Inhibition of microtubule nucleation at the neuronal centrosome compromises axon growth , 1994, Neuron.

[32]  C. Walsh,et al.  Genetic Malformations of the Human Cerebral Cortex , 1999, Neuron.

[33]  H. Osada,et al.  Mutations in the Plk gene lead to instability of Plk protein in human tumour cell lines , 2000, Nature Cell Biology.

[34]  G. Pazour,et al.  Intraflagellar transport and cilia-dependent diseases. , 2002, Trends in cell biology.

[35]  J. Gleeson,et al.  Cytoskeletal-associated proteins in the migration of cortical neurons. , 2004, Journal of neurobiology.

[36]  J. B. Rattner,et al.  Autoantibodies to a group of centrosomal proteins in human autoimmune sera reactive with the centrosome. , 1998, Arthritis and rheumatism.

[37]  M. Ueda,et al.  Centrosome positioning and directionality of cell movements. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[38]  S. Mcconnell,et al.  NudC Associates with Lis1 and the Dynein Motor at the Leading Pole of Neurons , 2001, The Journal of Neuroscience.

[39]  Jan-Michael Peters,et al.  The anaphase-promoting complex: proteolysis in mitosis and beyond. , 2002, Molecular cell.

[40]  Robert L. Nussbaum,et al.  Mutation in the α-Synuclein Gene Identified in Families with Parkinson's Disease , 1997 .

[41]  G. Pazour,et al.  The vertebrate primary cilium is a sensory organelle. , 2003, Current opinion in cell biology.

[42]  C. Olanow,et al.  Impairment of the ubiquitin‐proteasome system causes dopaminergic cell death and inclusion body formation in ventral mesencephalic cultures , 2002, Journal of neurochemistry.

[43]  T. Strachan,et al.  Mutations in INVS encoding inversin cause nephronophthisis type 2, linking renal cystic disease to the function of primary cilia and left-right axis determination , 2003, Nature Genetics.

[44]  S. R. Wicks,et al.  Loss of C. elegans BBS-7 and BBS-8 protein function results in cilia defects and compromised intraflagellar transport. , 2004, Genes & development.

[45]  C. Gordon.  The intracellular localization of the proteasome. , 2002, Current topics in microbiology and immunology.

[46]  Bertrand Fontaine,et al.  Spastin, a new AAA protein, is altered in the most frequent form of autosomal dominant spastic paraplegia , 1999, Nature Genetics.

[47]  D. A. Willins,et al.  Mutations in the heavy chain of cytoplasmic dynein suppress the nudF nuclear migration mutation of Aspergillus nidulans , 1997, Molecular and General Genetics MGG.

[48]  S. Tsuji,et al.  Familial juvenile parkinsonism , 1994, Neurology.

[49]  N. Craddock,et al.  Molecular genetics of bipolar disorder. , 2001, The British journal of psychiatry : the journal of mental science.

[50]  Fabrice P Cordelières,et al.  Huntingtin Controls Neurotrophic Support and Survival of Neurons by Enhancing BDNF Vesicular Transport along Microtubules , 2004, Cell.

[51]  L. Goldstein,et al.  Understanding the functions of kinesin-II. , 2000, Biochimica et biophysica acta.

[52]  C. Walsh,et al.  LIS1 Regulates CNS Lamination by Interacting with mNudE, a Central Component of the Centrosome , 2000, Neuron.

[53]  N. Copeland,et al.  Reversal of left-right asymmetry: a situs inversus mutation. , 1993, Science.

[54]  O. Reiner,et al.  Doublecortin, a stabilizer of microtubules. , 1999, Human molecular genetics.

[55]  G. Sobue,et al.  Dorfin prevents cell death by reducing mitochondrial localizing mutant superoxide dismutase 1 in a neuronal cell model of familial amyotrophic lateral sclerosis , 2004, Journal of neurochemistry.

[56]  J. Hoeijmakers,et al.  Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. , 1999, Developmental biology.

[57]  S. Mcconnell,et al.  Doublecortin Is a Developmentally Regulated, Microtubule-Associated Protein Expressed in Migrating and Differentiating Neurons , 1999, Neuron.

[58]  K. Kaibuchi,et al.  Small GTP-binding proteins. , 1992, International review of cytology.

[59]  Alexey Khodjakov,et al.  Centrosome-independent mitotic spindle formation in vertebrates , 2000, Current Biology.

[60]  S. Sorokin,et al.  CENTRIOLES AND THE FORMATION OF RUDIMENTARY CILIA BY FIBROBLASTS AND SMOOTH MUSCLE CELLS , 1962, The Journal of cell biology.

[61]  S. Wilk,et al.  Ubiquitin-mediated proteolysis centers in HeLa cells: indication from studies of an inhibitor of the chymotrypsin-like activity of the proteasome. , 1996, European journal of cell biology.

[62]  G. Eichele,et al.  The lissencephaly gene product Lis1, a protein involved in neuronal migration, interacts with a nuclear movement protein, NudC , 1998, Current Biology.

[63]  L. Tsai,et al.  Regulation of cytoplasmic dynein behaviour and microtubule organization by mammalian Lis1 , 2000, Nature Cell Biology.

[64]  Shinsei Minoshima,et al.  Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase , 2000, Nature Genetics.

[65]  E. Nigg.  Centrosomes in development and disease , 2004 .

[66]  R. Vale,et al.  Identification of katanin, an ATPase that severs and disassembles stable microtubules , 1993, Cell.

[67]  S. Doxsey,et al.  Re-evaluating centrosome function , 2001, Nature Reviews Molecular Cell Biology.

[68]  B. Kachar,et al.  Localization of myosin-V in the centrosome. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[69]  P. Thomas,et al.  Activity and Regulation of the Centrosome-associated Proteasome* , 2000, The Journal of Biological Chemistry.

[70]  M. Hatten,et al.  New Directions in Neuronal Migration , 2002, Science.

[71]  S. Pietrokovski,et al.  Doublecortin mutations cluster in evolutionarily conserved functional domains. , 2000, Human molecular genetics.

[72]  Robert E. Cohen,et al.  Proteasomes and their kin: proteases in the machine age , 2004, Nature Reviews Molecular Cell Biology.

[73]  J. Sibarita,et al.  Microtubule release from the centrosome in migrating cells , 2002, The Journal of cell biology.

[74]  S. Baker,et al.  IFT20 Links Kinesin II with a Mammalian Intraflagellar Transport Complex That Is Conserved in Motile Flagella and Sensory Cilia* , 2003, Journal of Biological Chemistry.

[75]  B. Brinkley,et al.  Supernumerary centrosomes and cancer: Boveri's hypothesis resurrected. , 1998, Cell motility and the cytoskeleton.

[76]  M. Bornens.  Centrosome composition and microtubule anchoring mechanisms. , 2002, Current opinion in cell biology.

[77]  E. Wanker,et al.  Centrosome disorganization in fibroblast cultures derived from R6/2 Huntington's disease (HD) transgenic mice and HD patients. , 2001, Human molecular genetics.

[78]  G. Woude,et al.  Abnormal Centrosome Amplification in the Absence of p53 , 1996, Science.

[79]  Jing Zhou,et al.  Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells , 2003, Nature Genetics.

[80]  Edwin M Stone,et al.  Comparative genomic analysis identifies an ADP-ribosylation factor-like gene as the cause of Bardet-Biedl syndrome (BBS3). , 2004, American journal of human genetics.

[81]  田中 輝幸.  Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration , 2005 .

[82]  M. Bornens,et al.  Microtubule minus-end anchorage at centrosomal and non-centrosomal sites: the role of ninein. , 2000, Journal of cell science.

[83]  Min Goo Lee,et al.  Dynamic Association of Proteasomal Machinery with the Centrosome , 1999, The Journal of cell biology.

[84]  Bethan E. Hoskins,et al.  The Bardet-Biedl protein BBS4 targets cargo to the pericentriolar region and is required for microtubule anchoring and cell cycle progression , 2004, Nature Genetics.

[85]  P. Worley,et al.  Huntingtin-associated protein 1 (HAP1) interacts with the p150Glued subunit of dynactin. , 1997, Human molecular genetics.

[86]  N. Berger,et al.  RET/PCM-1: a novel fusion gene in papillary thyroid carcinoma , 2000, Oncogene.

[87]  S. Minoshima,et al.  Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism , 1998, Nature.

[88]  A. Khodjakov,et al.  Requirement of a Centrosomal Activity for Cell Cycle Progression Through G1 into S Phase , 2001, Science.

[89]  H. Varmark.  Functional role of centrosomes in spindle assembly and organization , 2004, Journal of cellular biochemistry.

[90]  Tanya M. Teslovich,et al.  Basal body dysfunction is a likely cause of pleiotropic Bardet–Biedl syndrome , 2003, Nature.

[91]  P. Lansbury,et al.  Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[92]  K. Broadie,et al.  The Hereditary Spastic Paraplegia Gene, spastin, Regulates Microtubule Stability to Modulate Synaptic Structure and Function , 2004, Current Biology.

[93]  N. Hirokawa,et al.  Left-Right Asymmetry and Kinesin Superfamily Protein KIF3A: New Insights in Determination of Laterality and Mesoderm Induction by kif3A− /− Mice Analysis , 1999, The Journal of cell biology.

[94]  H. Arai,et al.  Miller-Dieker lissencephaly gene encodes a subunit of brain platelet-activating factor , 1994, Nature.

[95]  P. Baas,et al.  Microtubules released from the neuronal centrosome are transported into the axon. , 1995, Journal of cell science.

[96]  K. Münger,et al.  The human papillomavirus type 16 E6 and E7 oncoproteins cooperate to induce mitotic defects and genomic instability by uncoupling centrosome duplication from the cell division cycle. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[97]  K. Borden.  Structure/function in neuroprotection and apoptosis , 1998, Annals of neurology.

[98]  尾關 祐二.  Disrupted-in-Schizophrenia-1 (DISC-1) : mutant truncation prevents binding to NudE-like (NUDEL) and inhibits neurite outgrowth , 2004 .

[99]  C. Echeverri,et al.  Cytoplasmic Dynein and Dynactin Are Required for the Transport of Microtubules into the Axon , 1998, The Journal of cell biology.

[100]  Tanya M. Teslovich,et al.  Comparative Genomics Identifies a Flagellar and Basal Body Proteome that Includes the BBS5 Human Disease Gene , 2004, Cell.

[101]  H Knecht,et al.  Centrosome defects and genetic instability in malignant tumors. , 1998, Cancer research.

[102]  D. Glover,et al.  Polar expeditions — provisioning the centrosome for mitosis , 2003, Nature Cell Biology.

[103]  A. Wynshaw-Boris,et al.  LIS1 and dynein motor function in neuronal migration and development. , 2001, Genes & development.

[104]  E. Rugarli,et al.  Spastin interacts with the centrosomal protein NA14, and is enriched in the spindle pole, the midbody and the distal axon. , 2004, Human molecular genetics.

[105]  D. Birnbaum,et al.  FGFR1 is fused to the centrosome-associated protein CEP110 in the 8p12 stem cell myeloproliferative disorder with t(8;9)(p12;q33). , 2000, Blood.

[106]  H. Lehrach,et al.  HIP-I: a huntingtin interacting protein isolated by the yeast two-hybrid system. , 1997, Human molecular genetics.

[107]  Peter T. Lansbury,et al.  Accelerated in vitro fibril formation by a mutant α-synuclein linked to early-onset Parkinson disease , 1998, Nature Medicine.

[108]  R. Nussbaum,et al.  Alzheimer's disease and Parkinson's disease. , 2003, The New England journal of medicine.

[109]  L. Attisano,et al.  Regulation of the TGFβ signalling pathway by ubiquitin-mediated degradation , 2004, Oncogene.

[110]  R. Ellis,et al.  Macromolecular crowding: an important but neglected aspect of the intracellular environment. , 2001, Current opinion in structural biology.

[111]  N. Katsanis,et al.  MKKS/BBS6, a divergent chaperonin-like protein linked to the obesity disorder Bardet-Biedl syndrome, is a novel centrosomal component required for cytokinesis , 2005, Journal of Cell Science.

[112]  Keith A. Boroevich,et al.  Mutations in a member of the Ras superfamily of small GTP-binding proteins causes Bardet-Biedl syndrome , 2004, Nature Genetics.

[113]  A. Wynshaw-Boris,et al.  A LIS1/NUDEL/Cytoplasmic Dynein Heavy Chain Complex in the Developing and Adult Nervous System , 2000, Neuron.

[114]  Erich A. Nigg,et al.  Centrosome aberrations: cause or consequence of cancer progression? , 2002, Nature Reviews Cancer.

[115]  Y. Moriwaki,et al.  Direct evidence of autosomal recessive inheritance of Arg24 to termination codon in purine nucleoside phosphorylase gene in a family with a severe combined immunodeficiency patient , 1998, Human Genetics.

[116]  K. Kinzler,et al.  Mutations of chromosome 5q21 genes in FAP and colorectal cancer patients. , 1991, Science.

[117]  J. Thyberg,et al.  Role of microtubules in the organization of the Golgi complex. , 1999, Experimental cell research.

[118]  J. Solowska,et al.  Axonal Growth Is Sensitive to the Levels of Katanin, a Protein That Severs Microtubules , 2004, The Journal of Neuroscience.

[119]  M. López-Nevot,et al.  A poly(ADP-ribose) polymerase haplotype spanning the promoter region confers susceptibility to rheumatoid arthritis. , 2003, Arthritis and rheumatism.

[120]  J. Fink,et al.  Hereditary spastic paraplegia: spastin phenotype and function. , 2004, Archives of neurology.

[121]  L. Guay-Woodford,et al.  The polycystic kidney disease proteins, polycystin-1, polycystin-2, polaris, and cystin, are co-localized in renal cilia. , 2002, Journal of the American Society of Nephrology : JASN.

[122]  K. Münger,et al.  Centrosome abnormalities and genomic instability induced by human papillomavirus oncoproteins. , 2003, Progress in cell cycle research.

[123]  P. Sutovsky,et al.  Ubiquitination of Prohibitin in Mammalian Sperm Mitochondria: Possible Roles in the Regulation of Mitochondrial Inheritance and Sperm Quality Control1 , 2003, Biology of reproduction.

[124]  L. Tsai,et al.  Ndel1 Operates in a Common Pathway with LIS1 and Cytoplasmic Dynein to Regulate Cortical Neuronal Positioning , 2004, Neuron.

[125]  P. Lansbury,et al.  Molecular crowding accelerates fibrillization of alpha-synuclein: could an increase in the cytoplasmic protein concentration induce Parkinson's disease? , 2002, Biochemistry.

[126]  Erich E Wanker,et al.  The hunt for huntingtin function: interaction partners tell many different stories. , 2003, Trends in biochemical sciences.

[127]  S. Tsukita,et al.  Centriolar satellites: molecular characterization, ATP-dependent movement toward centrioles and possible involvement in ciliogenesis. , 1999 .

[128]  T. Strachan,et al.  Expression analyses and interaction with the anaphase promoting complex protein Apc2 suggest a role for inversin in primary cilia and involvement in the cell cycle. , 2002, Human molecular genetics.

[129]  M. L. Schmidt,et al.  α-Synuclein in Lewy bodies , 1997, Nature.

[130]  D. Ledbetter,et al.  Isolation of a Miller–Dicker lissencephaly gene containing G protein β-subunit-like repeats , 1993, Nature.

[131]  V. Wimmer,et al.  Chlamydomonas DIP13 and human NA14: a new class of proteins associated with microtubule structures is involved in cell division , 2003, Journal of Cell Science.

[132]  Y. Saijoh,et al.  The left-right determinant Inversin is a component of node monocilia and other 9+0 cilia , 2003, Development.

[133]  G. Pazour,et al.  Chlamydomonas IFT88 and Its Mouse Homologue, Polycystic Kidney Disease Gene Tg737, Are Required for Assembly of Cilia and Flagella , 2000, The Journal of cell biology.

[134]  D. Ledbetter,et al.  Refinement of a 400-kb critical region allows genotypic differentiation between isolated lissencephaly, Miller-Dieker syndrome, and other phenotypes secondary to deletions of 17p13.3. , 2003, American journal of human genetics.

[135]  Jian Feng,et al.  Parkin is recruited to the centrosome in response to inhibition of proteasomes , 2003, Journal of Cell Science.

[136]  J. Oliver,et al.  Purine nucleoside phosphorylase is associated with centrioles and basal bodies , 1981, The Journal of cell biology.

[137]  I. Kanazawa,et al.  HIP1, a human homologue of S. cerevisiae Sla2p, interacts with membrane-associated huntingtin in the brain , 1997, Nature Genetics.

[138]  M. Mann,et al.  Proteomic characterization of the human centrosome by protein correlation profiling , 2003, Nature.

[139]  O Reiner,et al.  Interaction between LIS1 and doublecortin, two lissencephaly gene products. , 2000, Human molecular genetics.

[140]  Theodor Boveri.  Ueber die Natur der Centrosomen , 2022 .

[141]  Christopher P Austin,et al.  DISC1 (Disrupted-In-Schizophrenia 1) is a centrosome-associated protein that interacts with MAP1A, MIPT3, ATF4/5 and NUDEL: regulation and loss of interaction with mutation. , 2003, Human molecular genetics.

[142]  Aaron DiAntonio,et al.  Ubiquitin-dependent regulation of the synapse. , 2004, Annual review of neuroscience.

[143]  Kiowa S. Bower,et al.  Accelerated α‐synuclein fibrillation in crowded milieu , 2002 .

[144]  E. Chan,et al.  Two major autoantigen-antibody systems of the mitotic spindle apparatus. , 1996, Arthritis and rheumatism.

[145]  V. Bohr,et al.  Central Role for the Werner Syndrome Protein/Poly(ADP-Ribose) Polymerase 1 Complex in the Poly(ADP-Ribosyl)ation Pathway after DNA Damage , 2003, Molecular and Cellular Biology.

[146]  T. Strachan,et al.  A perspective on inversin , 2004, Cell biology international.

[147]  I. Weissman,et al.  Implications for Pathogenesis and Therapy , 1996 .

[148]  X. Wang,et al.  Centrosome amplification and a defective G2-M cell cycle checkpoint induce genetic instability in BRCA1 exon 11 isoform-deficient cells. , 1999, Molecular cell.

[149]  E. Robbins,et al.  THE CENTRIOLE CYCLE IN SYNCHRONIZED HELA CELLS , 1968, The Journal of cell biology.

[150]  W. Zimmer,et al.  PCM-1, A 228-kD centrosome autoantigen with a distinct cell cycle distribution , 1994, The Journal of cell biology.

[151]  J. Rain,et al.  Disrupted in Schizophrenia 1 and Nudel form a neurodevelopmentally regulated protein complex: implications for schizophrenia and other major neurological disorders , 2004, Molecular and Cellular Neuroscience.

[152]  T. Chase,et al.  Degradation of α-Synuclein by Proteasome* , 1999, The Journal of Biological Chemistry.

[153]  M E Hatten,et al.  Motility and cytoskeletal organization of migrating cerebellar granule neurons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[154]  Michel Bornens,et al.  GMAP-210 Recruits γ-Tubulin Complexes to cis-Golgi Membranes and Is Required for Golgi Ribbon Formation , 2004, Cell.

[155]  A. Hackam,et al.  Recruitment and activation of caspase-8 by the Huntingtin-interacting protein Hip-1 and a novel partner Hippi , 2002, Nature Cell Biology.

[156]  Y. Imai,et al.  Parkin Suppresses Unfolded Protein Stress-induced Cell Death through Its E3 Ubiquitin-protein Ligase Activity* , 2000, The Journal of Biological Chemistry.