Abstract
Human Mental Retardation (MR) is a common and highly heterogeneous pediatric disorder affecting around 3% of the general population; at least 215 X-linked MR (XLMR) conditions have been described, and mutations have been identified in 83 different genes, encoding proteins with a variety of function, such as chromatin remodeling, synaptic function, and intracellular trafficking. The small GTPases of the RAB family, which play an essential role in intracellular vesicular trafficking, have been shown to be involved in MR. We report here the identification of mutations in the small GTPase RAB39B gene in two male patients. One mutation in family X (D-23) introduced a stop codon seven amino acids after the start codon (c.21C > A; p.Y7X). A second mutation, in the MRX72 family, altered the 5' splice site (c.215+1G > A) and normal splicing. Neither instance produced a protein. Mutations segregate with the disease in the families, and in some family members intellectual disabilities were associated with autism spectrum disorder, epileptic seizures, and macrocephaly. We show that RAB39B, a novel RAB GTPase of unknown function, is a neuronal-specific protein that is localized to the Golgi compartment. Its downregulation leads to an alteration in the number and morphology of neurite growth cones and a significant reduction in presynaptic buttons, suggesting that RAB39B is required for synapse formation and maintenance. Our results demonstrate developmental and functional neuronal alteration as a consequence of downregulation of RAB39B and emphasize the critical role of vesicular trafficking in the development of neurons and human intellectual abilities.
MeSH Terms
Animals
Autistic Disorder/complications,genetics
Base Sequence
Brain/metabolism,pathology
Cell Differentiation
Craniofacial Abnormalities/complications,genetics
DNA Mutational Analysis
Down-Regulation/genetics
Epilepsy/complications,genetics
Female
Golgi Apparatus/metabolism
HeLa Cells
Humans
Male
Mental Retardation, X-Linked/complications,genetics
Mice
Molecular Sequence Data
Mutation/genetics
Neurons/metabolism,pathology
Organ Specificity/genetics
Pedigree
Protein Transport
RNA, Small Interfering/metabolism
Synapses/genetics
rab GTP-Binding Proteins/genetics
Chemicals
RNA, Small Interfering
Rab39B protein, human
rab GTP-Binding Proteins
Authors & Affiliations
23 authors, click to expand affiliations / ORCID
Giannandrea Maila
Dulbecco Telethon Institute at Division of Neuroscience, San Raffaele Scientific Institute, Milan, Italy.
Bianchi Veronica
Mignogna Maria Lidia
Sirri Alessandra
Carrabino Salvatore
D'Elia Errico
Vecellio Matteo
Russo Silvia
Cogliati Francesca
Larizza Lidia
Ropers Hans-Hilger
Tzschach Andreas
Kalscheuer Vera
Oehl-Jaschkowitz Barbara
Skinner Cindy
Schwartz Charles E
Gecz Jozef
Van Esch Hilde
Raynaud Martine
Chelly Jamel
de Brouwer Arjan P M
Toniolo Daniela
D'Adamo Patrizia
References (26)
26 references, click to expand
-
Rat hippocampal neurons in dispersed cell culture.
Brain Res. 1977 May 13;126(3):397-42
PMID: 861729
-
Mutations in GDI1 are responsible for X-linked non-specific mental retardation.
Nat Genet. 1998 Jun;19(2):134-9
PMID: 9620768
-
Formation of microtubule-based traps controls the sorting and concentration of vesicles to restricted sites of regenerating neurons after axotomy.
J Cell Biol. 2007 Feb 12;176(4):497-507
PMID: 17283182
-
Rab proteins and Rab-associated proteins: major actors in the mechanism of protein-trafficking disorders.
Eur J Pediatr. 2008 Jul;167(7):723-9
PMID: 18463892
-
Visualization of Rab9-mediated vesicle transport from endosomes to the trans-Golgi in living cells.
J Cell Biol. 2002 Feb 4;156(3):511-8
PMID: 11827983
-
Golgi-resident small GTPase Rab33B interacts with Atg16L and modulates autophagosome formation.
Mol Biol Cell. 2008 Jul;19(7):2916-25
PMID: 18448665
-
Divergent functions of neuronal Rab11b in Ca2+-regulated versus constitutive exocytosis.
J Neurosci. 2003 Nov 19;23(33):10531-9
PMID: 14627637
-
Mapping to distal Xq28 of nonspecific X-linked mental retardation MRX72: linkage analysis and clinical findings in a three-generation Sardinian family.
Am J Med Genet. 2000 Oct 23;94(5):376-82
PMID: 11050621
-
Cognitive impairment in Gdi1-deficient mice is associated with altered synaptic vesicle pools and short-term synaptic plasticity, and can be corrected by appropriate learning training.
Hum Mol Genet. 2009 Jan 1;18(1):105-17
PMID: 18829665
-
Transduction of a gene expression cassette using advanced generation lentiviral vectors.
Methods Enzymol. 2002;346:514-29
PMID: 11883088
-
Mutations of the catalytic subunit of RAB3GAP cause Warburg Micro syndrome.
Nat Genet. 2005 Mar;37(3):221-3
PMID: 15696165
-
Mutation in Rab3 GTPase-activating protein (RAB3GAP) noncatalytic subunit in a kindred with Martsolf syndrome.
Am J Hum Genet. 2006 Apr;78(4):702-7
PMID: 16532399
-
Syntaxin 16 and syntaxin 5 are required for efficient retrograde transport of several exogenous and endogenous cargo proteins.
J Cell Sci. 2007 Apr 15;120(Pt 8):1457-68
PMID: 17389686
-
The mammalian Rab family of small GTPases: definition of family and subfamily sequence motifs suggests a mechanism for functional specificity in the Ras superfamily.
J Mol Biol. 2000 Aug 25;301(4):1077-87
PMID: 10966806
-
Mutations in the small GTP-ase late endosomal protein RAB7 cause Charcot-Marie-Tooth type 2B neuropathy.
Am J Hum Genet. 2003 Mar;72(3):722-7
PMID: 12545426
-
Targeting Rab GTPases to distinct membrane compartments.
Nat Rev Mol Cell Biol. 2004 Nov;5(11):886-96
PMID: 15520808
-
A systematic, large-scale resequencing screen of X-chromosome coding exons in mental retardation.
Nat Genet. 2009 May;41(5):535-43
PMID: 19377476
-
RAB23 mutations in Carpenter syndrome imply an unexpected role for hedgehog signaling in cranial-suture development and obesity.
Am J Hum Genet. 2007 Jun;80(6):1162-70
PMID: 17503333
-
Nonspecific X-linked mental retardation I: a review with information from 24 new families.
Am J Med Genet. 1980;7(4):443-60
PMID: 7011032
-
A discussion on the measurement of growth and form; the theory of differential growth analysis.
Proc R Soc Lond B Biol Sci. 1950 Nov;137(889):470-4
PMID: 14797660
-
siRNA vs. shRNA: similarities and differences.
Adv Drug Deliv Rev. 2009 Jul 25;61(9):746-59
PMID: 19389436
-
VAMP4 cycles from the cell surface to the trans-Golgi network via sorting and recycling endosomes.
J Cell Sci. 2007 Mar 15;120(Pt 6):1028-41
PMID: 17327277
-
Deletion of the mental retardation gene Gdi1 impairs associative memory and alters social behavior in mice.
Hum Mol Genet. 2002 Oct 1;11(21):2567-80
PMID: 12354782
-
A novel RAB7 mutation associated with ulcero-mutilating neuropathy.
Ann Neurol. 2004 Oct;56(4):586-90
PMID: 15455439
-
Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells.
Mol Cell Neurosci. 2006 Jan;31(1):149-60
PMID: 16297637
-
Evolution of the Rab family of small GTP-binding proteins.
J Mol Biol. 2001 Nov 2;313(4):889-901
PMID: 11697911