Deficiencies in lamin B1 and lamin B2 cause neurodevelopmental defects and distinct nuclear shape abnormalities in neurons

Molecular Biology of the Cell

Volumn 22, Issue 23, 2011, Pages 4683-4693

  Coffinier, Catherine ^a   Jung, Hea Jin ^a   Nobumori, Chika ^a   Chang, Sandy ^a   Tu, Yiping ^a   Barnes II, Richard H ^a   Yoshinaga, Yuko ^b   De Jong, Pieter J ^b   Vergnes, Laurent ^c   Reue, Karen ^c   Fong, Loren G ^a   Young, Stephen G ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LAMIN B; LAMIN B1; LAMIN B2; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN ATROPHY; BRAIN CELL; BRAIN DEVELOPMENT; CELL MIGRATION; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; EMBRYO; FOREBRAIN; KNOCKOUT MOUSE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEUROLOGIC DISEASE; NONHUMAN; NUCLEAR SHAPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ANIMALS; BRAIN; LAMIN TYPE B; MICE; MICE, KNOCKOUT; NEURONS; NUCLEAR LAMINA; PROSENCEPHALON;

EID: 82655181488     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-06-0504     Document Type: Article

References (41)

1. Ayala R, Shu T, Tsai LH (2007). Trekking across the brain: the journey of neuronal migration. Cell 128, 29-43. (Pubitemid 46055273)
2. Coffinier C, Chang SY, Nobumori C, Tu Y, Farber EA, Toth JI, Fong LG, Young SG (2010a). Abnormal development of the cerebral cortex and cerebellum in the setting of lamin B2 deficiency. Proc Natl Acad Sci USA 107, 5076-5081.
3. Coffinier C et al. (2010b). Direct synthesis of lamin A, bypassing prelamin A processing, causes misshapen nuclei in fibroblasts but no detectable pathology in mice. J Biol Chem 285, 20818-20826.
4. Dechat T, Adam SA, Goldman RD (2009). Nuclear lamins and chromatin: when structure meets function. Adv Enzyme Regul 49, 157-166.
5. Dechat T, Pfleghaar K, Sengupta K, Shimi T, Shumaker DK, Solimando L, Goldman RD (2008). Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev 22, 832-853. (Pubitemid 351482836)
6. Dehay C, Kennedy H (2007). Cell-cycle control and cortical development. Nat Rev Neurosci 8, 438-450. (Pubitemid 46789227)
7. Deutsch SI, Burket JA, Katz E (2010). Does subtle disturbance of neuronal migration contribute to schizophrenia and other neurodevelopmental disorders? Potential genetic mechanisms with possible treatment implications. Eur Neuropsychopharmacol 20, 281-287.
8. Feng Y, Walsh CA (2004). Mitotic spindle regulation by Nde1 controls cerebral cortical size. Neuron 44, 279-293. (Pubitemid 39346252)
9. Folker ES, Ostlund C, Luxton GW, Worman HJ, Gundersen GG (2011). Lamin A variants that cause striated muscle disease are defective in anchoring transmembrane actin-associated nuclear lines for nuclear movement. Proc Natl Acad Sci USA 108, 131-136.
10. Fridkin A, Penkner A, Jantsch V, Gruenbaum Y (2009). SUN-domain and KASH-domain proteins during development, meiosis and disease. Cell Mol Life Sci 66, 1518-1533.
11. Gorski JA, Talley T, Qiu M, Puelles L, Rubenstein JL, Jones KR (2002). Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J Neurosci 22, 6309-6314. (Pubitemid 35386383)
12. Gupta A, Tsai LH, Wynshaw-Boris A (2002). Life is a journey: a genetic look at neocortical development. Nat Rev Genet 3, 342-355. (Pubitemid 34506716)
13. Hutchison CJ (2002). Lamins: building blocks or regulators of gene expression?. Nat Rev Mol Cell Biol 3, 848-858.
14. Ji JY, Lee RT, Vergnes L, Fong LG, Stewart CL, Reue K, Young SG, Zhang Q, Shanahan CM, Lammerding J (2007). Cell nuclei spin in the absence of lamin B1. J Biol Chem 282, 20015-20026. (Pubitemid 47100106)
15. Kahler AK et al. (2008). Association analysis of schizophrenia on 18 genes involved in neuronal migration: MDGA1 as a new susceptibility gene. Am J Med Genet B Neuropsychiatr Genet 147B, 1089-1100.
16. Li BS, Zhang L, Takahashi S, Ma W, Jaffe H, Kulkarni AB, Pant HC (2002). Cyclin-dependent kinase 5 prevents neuronal apoptosis by negative regulation of c-Jun N-terminal kinase 3. EMBO J 21, 324-333. (Pubitemid 34137294)
17. Lopez-Soler RI, Moir RD, Spann TP, Stick R, Goldman RD (2001). A role for nuclear lamins in nuclear envelope assembly. J Cell Biol 154, 61-70. (Pubitemid 34289278)
18. Méjat A, Misteli T (2010). LINC complexes in health and disease. Nucleus 1, 40-52.
19. Moir RD, Spann TP, Lopez-Soler RI, Yoon M, Goldman AE, Khuon S, Goldman RD (2000). Review: the dynamics of the nuclear lamins during the cell cycle - relationship between structure and function. J Struct Biol 129, 324-334. (Pubitemid 30481374)
20. Muchir A et al. (2004). Nuclear envelope alterations in fibroblasts from patients with muscular dystrophy, cardiomyopathy, and partial lipodystrophy carrying lamin A/C gene mutations. Muscle Nerve 30, 444-450. (Pubitemid 39288147)
21. Nagy A, Gertsenstein M, Vintersten K, Behringer R (2003). Manipulating the Mouse Embryo: A Laboratory Manual, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
22. Pawlisz AS, Mutch C, Wynshaw-Boris A, Chenn A, Walsh CA, Feng Y (2008). Lis1-Nde1-dependent neuronal fate control determines cerebral cortical size and lamination. Hum Mol Genet 17, 2441-2455.
23. Rice DS, Curran T (2001). Role of the reelin signaling pathway in central nervous system development. Annu Rev Neurosci 24, 1005-1039. (Pubitemid 32695252)
24. Rober RA, Weber K, Osborn M (1989). Differential timing of nuclear lamin A/C expression in the various organs of the mouse embryo and the young animal: a developmental study. Development 105, 365-378. (Pubitemid 19053283)
25. Sasaki S et al. (2005). Complete loss of Ndel1 results in neuronal migration defects and early embryonic lethality. Mol Cell Biol 25, 7812-7827. (Pubitemid 41170141)
26. Shimi T et al. (2008). The A- and B-type nuclear lamin networks: microdomains involved in chromatin organization and transcription. Genes Dev 22, 3409-3421.
27. Solecki DJ, Govek EE, Tomoda T, Hatten ME (2006). Neuronal polarity in CNS development. Genes Dev 20, 2639-2647. (Pubitemid 44498374)
28. Soriano P (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21, 70-71.
29. Sullivan T, Escalante-Alcalde D, Bhatt H, Anver M, Bhat N, Nagashima K, Stewart CL, Burke B (1999). Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J Cell Biol 147, 913-919.
30. Tanaka T, Serneo FF, Higgins C, Gambello MJ, Wynshaw-Boris A, Gleeson JG (2004). Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J Cell Biol 165, 709-721. (Pubitemid 38765772)
31. Tsai JW, Bremner KH, Vallee RB (2007). Dual subcellular roles for LIS1 and dynein in radial neuronal migration in live brain tissue. Nat Neurosci 10, 970-979. (Pubitemid 47185202)
32. Tsai MY, Wang S, Heidinger JM, Shumaker DK, Adam SA, Goldman RD, Zheng Y (2006). A mitotic lamin B matrix induced by RanGTP required for spindle assembly. Science 311, 1887-1893.
33. Vallee RB, Tsai JW (2006). The cellular roles of the lissencephaly gene LIS1, and what they tell us about brain development. Genes Dev 20, 1384-1393. (Pubitemid 43830646)
34. Vergnes L, Peterfy M, Bergo MO, Young SG, Reue K (2004). Lamin B1 is required for mouse development and nuclear integrity. Proc Natl Acad Sci USA 101, 10428-10433. (Pubitemid 38924942)
35. Wegiel J et al. (2010). The neuropathology of autism: defects of neurogenesis and neuronal migration, and dysplastic changes. Acta Neuropathol 119, 755-770.
36. Worman HJ, Fong LG, Muchir A, Young SG (2009). Laminopathies and the long strange trip from basic cell biology to therapy. J Clin Invest 119, 1825-1836.
37. Wynshaw-Boris A (2007). Lissencephaly and LIS1: insights into the molecular mechanisms of neuronal migration and development. Clin Genet 72, 296-304.
38. Wynshaw-Boris A, Gambello MJ (2001). LIS1 and dynein motor function in neuronal migration and development. Genes Dev 15, 639-651. (Pubitemid 32244894)
39. Yang SH, Chang SY, Yin L, Tu Y, Hu Y, Yoshinaga Y, Jong PJ, Fong LG, Young SG (2011). An absence of both lamin B1 and lamin B2 in keratinocytes has no effect on cell proliferation or the development of the skin and hair. Hum Mol Genet 20, 3537-3544.
40. Yingling J, Youn YH, Darling D, Toyo-Oka K, Pramparo T, Hirotsune S, Wynshaw-Boris A (2008). Neuroepithelial stem cell proliferation requires LIS1 for precise spindle orientation and symmetric division. Cell 132, 474-486. (Pubitemid 351192005)
41. Zhang X, Lei K, Yuan X, Wu X, Zhuang Y, Xu T, Xu R, Han M (2009). SUN1/2 and Syne/Nesprin-1/2 complexes connect centrosome to the nucleus during neurogenesis and neuronal migration in mice. Neuron 64, 173-187.