Mutation of the BiP/GRP78 gene causes axon outgrowth and fasciculation defects in the thalamocortical connections of the mammalian forebrain

Journal of Comparative Neurology

Volumn 521, Issue 3, 2013, Pages 677-696

  Favero, Carlita B ^a,c   Henshaw, Rasha N ^a   Grimsley Myers, Cynthia M ^a   Shrestha, Ayushma ^a   Beier, David R ^b   Dwyer, Noelle D ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c URSINUS COLLEGE   (United States)

Author keywords

Axon guidance; Brain development; Chaperone; Cortical lamination; Corticothalamic axons; Endoplasmic reticulum; ENU mutant; Heat shock protein; Hspa5; Mouse; Protein misfolding; UPR

Indexed keywords

GLUCOSE REGULATED PROTEIN 78;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXON OUTGROWTH DEFECT; BRAIN DEVELOPMENT; CONTROLLED STUDY; CORTICOTHALAMIC AXON; EMBRYO; FASCICULATION DEFECT; FOREBRAIN AXON TRACT; GENE; GENE FUNCTION; GENE IDENTIFICATION; GRP78 GENE; HSPA5 GENE; IN VITRO STUDY; LOSS OF FUNCTION MUTATION; MOUSE; MUTATIONAL ANALYSIS; NERVE FIBER GROWTH; NERVE GROWTH; NERVE TRACT; NERVOUS SYSTEM MALFORMATION; NEUROPATHOLOGY; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; THALAMOCORTICAL TRACT;

ANIMALS; AXONS; CELLS, CULTURED; CEREBRAL CORTEX; FEMALE; FIBROBLASTS; GENETIC TESTING; GESTATIONAL AGE; HEAT-SHOCK PROTEINS; MALE; MAMMALS; MICE; MICE, INBRED C57BL; MICE, NEUROLOGIC MUTANTS; NEURAL PATHWAYS; PREGNANCY; PROSENCEPHALON; THALAMUS;

EID: 84871457375     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23199     Document Type: Article

References (91)

1. Alcamo EA, Chirivella L, Dautzenberg M, Dobreva G, Farinas I, Grosschedl R, McConnell SK. 2008. Satb2 regulates callosal projection neuron identity in the developing cerebral cortex. Neuron 57: 364-377.
2. Aridor M, Fish KN. 2009. Selective targeting of ER exit sites supports axon development. Traffic 10: 1669-1684.
3. Arlotta P, Molyneaux BJ, Chen J, Inoue J, Kominami R, Macklis JD. 2005. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45: 207-221.
4. Asanoma K, Kubota K, Chakraborty D, Renaud SJ, Wake N, Fukushima K, Soares MJ, Rumi MA. 2012. SATB homeobox proteins regulate trophoblast stem cell renewal and differentiation. J Biol Chem 287: 2257-2268.
5. Bicknese AR, Sheppard AM, O'Leary DD, Pearlman AL. 1994. Thalamocortical axons extend along a chondroitin sulfate proteoglycan-enriched pathway coincident with the neocortical subplate and distinct from the efferent path. J Neurosci 14: 3500-3510.
6. Britanova O, Akopov S, Lukyanov S, Gruss P, Tarabykin V. 2005. Novel transcription factor Satb2 interacts with matrix attachment region DNA elements in a tissue-specific manner and demonstrates cell-type-dependent expression in the developing mouse CNS. Eur J Neurosci 21: 658-668.
7. Britanova O, de Juan Romero C, Cheung A, Kwan KY, Schwark M, Gyorgy A, Vogel T, Akopov S, Mitkovski M, Agoston D, Sestan N, Molnar Z, Tarabykin V. 2008. Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex. Neuron 57: 378-392.
8. Buttiglione M, Revest JM, Pavlou O, Karagogeos D, Furley A, Rougon G, Faivre-Sarrailh C. 1998. A functional interaction between the neuronal adhesion molecules TAG-1 and F3 modulates neurite outgrowth and fasciculation of cerebellar granule cells. J Neurosci 18: 6853-6870.
9. Chen B, Schaevitz LR, McConnell SK. 2005. Fezl regulates the differentiation and axon targeting of layer 5 subcortical projection neurons in cerebral cortex. Proc Natl Acad Sci U S A 102: 17184-17189.
10. Chen Y, Magnani D, Theil T, Pratt T, Price DJ. 2012. Evidence that descending cortical axons are essential for thalamocortical axons to cross the pallial-subpallial boundary in the embryonic forebrain. PloS One 7: e33105.
11. Chung WW, Lagenaur CF, Yan YM, Lund JS. 1991. Developmental expression of neural cell adhesion molecules in the mouse neocortex and olfactory bulb. J Comp Neurol 314: 290-305.
12. de Bergeyck V, Nakajima K, Lambert de Rouvroit C, Naerhuyzen B, Goffinet AM, Miyata T, Ogawa M, Mikoshiba K. 1997. A truncated Reelin protein is produced but not secreted in the 'Orleans' reeler mutation (Reln[rl-Orl]). Brain Res 50: 85-90.
13. De Carlos JA, O'Leary DD. 1992. Growth and targeting of subplate axons and establishment of major cortical pathways J Neurosci 12: 1194-1211.
14. Denaxa M, Chan CH, Schachner M, Parnavelas JG, Karagogeos D. 2001. The adhesion molecule TAG-1 mediates the migration of cortical interneurons from the ganglionic eminence along the corticofugal fiber system. Development 128: 4635-4644.
15. Dodd J, Morton SB, Karagogeos D, Yamamoto M, Jessell TM. 1988. Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons. Neuron 1: 105-116.
16. Dotti CG, Sullivan CA, Banker GA. 1988. The establishment of polarity by hippocampal neurons in culture. J Neurosci 8: 1454-1468.
17. Dwyer ND, Manning DK, Moran JL, Mudbhary R, Fleming MS, Favero CB, Vock VM, O'Leary DD, Walsh CA, Beier DR. 2011. A forward genetic screen with a thalamocortical axon reporter mouse yields novel neurodevelopment mutants and a distinct Emx2 mutant phenotype. Neural Dev 6: 3.
18. Felsenfeld DP, Hynes MA, Skoler KM, Furley AJ, Jessell TM. 1994. TAG-1 can mediate homophilic binding, but neurite outgrowth on TAG-1 requires an L1-like molecule and beta 1 integrins. Neuron 12: 675-690.
19. Ferland RJ, Cherry TJ, Preware PO, Morrisey EE, Walsh CA. 2003. Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain. J Comp Neurol 460: 266-279.
20. Ganz J, Kaslin J, Freudenreich D, Machate A, Geffarth M, Brand M. 2012. Subdivisions of the adult zebrafish subpallium by molecular marker analysis. J Comp Neurol 520: 633-655.
21. Ghosh A, Antonini A, McConnell SK, Shatz CJ. 1990. Requirement for subplate neurons in the formation of thalamocortical connections. Nature 347: 179-181.
22. Graner MW, Cumming RI, Bigner DD. 2007. The heat shock response and chaperones/heat shock proteins in brain tumors: surface expression, release, and possible immune consequences. J Neurosci 27: 11214-11227.
23. Grant E, Hoerder-Suabedissen A, Molnar Z. 2012. Development of the corticothalamic projections. Front Neurosci 6: 1-14.
24. Gratzner HG. 1982. Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218: 474-475.
25. Hand R, Bortone D, Mattar P, Nguyen L, Heng JI, Guerrier S, Boutt E, Peters E, Barnes AP, Parras C, Schuurmans C, Guillemot F, Polleux F. 2005. Phosphorylation of Neurogenin2 specifies the migration properties and the dendritic morphology of pyramidal neurons in the neocortex. Neuron 48: 45-62.
26. Hendershot LM. 2004. The ER function BiP is a master regulator of ER function. Mt Sinai J Med 71: 289-297.
27. Hevner RF, Shi L, Justice N, Hsueh Y, Sheng M, Smiga S, Bulfone A, Goffinet AM, Campagnoni AT, Rubenstein JL. 2001. Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29: 353-366.
28. Hevner RF, Miyashita-Lin E, Rubenstein JL. 2002. Cortical and thalamic axon pathfinding defects in Tbr1, Gbx2, and Pax6 mutant mice: evidence that cortical and thalamic axons interact and guide each other. J Comp Neurol 447: 8-17.
29. Hu H, Yang Y, Eade A, Xiong Y, Qi Y. 2007. Breaches of the pial basement membrane and disappearance of the glia limitans during development underlie the cortical lamination defect in the mouse model of muscle-eye-brain disease. J Comp Neurol 502: 168-183.
30. Huguenard JR, McCormick DA. 2007. Thalamic synchrony and dynamic regulation of global forebrain oscillations. Trends Neurosci 30: 350-356.
31. Jones EG, Rubenstein JL. 2004. Expression of regulatory genes during differentiation of thalamic nuclei in mouse and monkey. J Comp Neurol 477: 55-80.
32. Kawano H, Fukuda T, Kubo K, Horie M, Uyemura K, Takeuchi K, Osumi N, Eto K, Kawamura K. 1999. Pax-6 is required for thalamocortical pathway formation in fetal rats. J Comp Neurol 408: 147-160.
33. Khan MM, Nomura T, Chiba T, Tanaka K, Yoshida H, Mori K, Ishii S. 2004. The fusion oncoprotein PML-RARalpha induces endoplasmic reticulum (ER)-associated degradation of N-CoR and ER stress. J Biol Chem 279: 11814-11824.
34. Kim DJ, Kim JJ, Park JY, Lee SY, Kim J, Kim IY, Kim SI, Park HJ. 2008. Quantification of thalamocortical tracts in schizophrenia on probabilistic maps. Neuroreport 19: 399-403.
35. Kosik KS, Finch EA. 1987. MAP2 and tau segregate into dendritic and axonal domains after the elaboration of morphologically distinct neurites: an immunocytochemical study of cultured rat cerebrum. J Neurosci 7: 3142-3153.
36. Lee AS. 2005. The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. Methods 35: 373-381.
37. Lee AS. 2007. GRP78 induction in cancer: therapeutic and prognostic implications. Cancer Res 67: 3496-3499.
38. Li J, Lee AS. 2006. Stress induction of GRP78/BiP and its role in cancer. Curr Mol Med 6: 45-54.
39. Litterman N, Ikeuchi Y, Gallardo G, O'Connell BC, Sowa ME, Gygi SP, Harper JW, Bonni A. 2011. An OBSL1-Cul7Fbxw8 ubiquitin ligase signaling mechanism regulates Golgi morphology and dendrite patterning. PLoS Biol 9: e1001060.
40. Little GE, Lopez-Bendito G, Runker AE, Garcia N, Pinon MC, Chedotal A, Molnar Z, Mitchell KJ. 2009. Specificity and plasticity of thalamocortical connections in Sema6A mutant mice. PLoS Biol 7: e98.
41. Lopez-Bendito G, Chan CH, Mallamaci A, Parnavelas J, Molnar Z. 2002. Role of Emx2 in the development of the reciprocal connectivity between cortex and thalamus. J Comp Neurol 451: 153-169.
42. Lopez-Bendito G, Cautinat A, Sanchez JA, Bielle F, Flames N, Garratt AN, Talmage DA, Role LW, Charnay P, Marin O, Garel S. 2006. Tangential neuronal migration controls axon guidance: a role for neuregulin-1 in thalamocortical axon navigation. Cell 125: 127-142.
43. Luo B, Lee AS. 2012. The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene, doi: 10.1038/onc.2012.130.
44. Luo S, Mao C, Lee B, Lee AS. 2006. GRP78/BiP is required for cell proliferation and protecting the inner cell mass from apoptosis during early mouse embryonic development. Mol Cell Biol 26: 5688-5697.
45. Luong MX, van der Meijden CM, Xing D, Hesselton R, Monuki ES, Jones SN, Lian JB, Stein JL, Stein GS, Neufeld EJ, van Wijnen AJ. 2002. Genetic ablation of the CDP/Cux protein C terminus results in hair cycle defects and reduced male fertility. Mol Cell Biol 22: 1424-1437.
46. Ma QH, Futagawa T, Yang WL, Jiang XD, Zeng L, Takeda Y, Xu RX, Bagnard D, Schachner M, Furley AJ, Karagogeos D, Watanabe K, Dawe GS, Xiao ZC. 2008. A TAG1-APP signalling pathway through Fe65 negatively modulates neurogenesis. Nat Cell Biol 10: 283-294.
47. Mackarehtschian K, Lau CK, Caras I, McConnell SK. 1999. Regional differences in the developing cerebral cortex revealed by ephrin-A5 expression. Cereb Cortex 9: 601-610.
48. Maroof AM, Anderson SA. 2006. Off on a tangent: thalamocortical axons traverse a permissive corridor across the basal telencephalon. Neuron 50: 185-188.
49. Matus S, Glimcher LH, Hetz C. 2011. Protein folding stress in neurodegenerative diseases: a glimpse into the ER. Curr Opin Cell Biol 23: 239-252.
50. McKenna WL, Betancourt J, Larkin KA, Abrams B, Guo C, Rubenstein JL, Chen B. 2011. Tbr1 and Fezf2 regulate alternate corticofugal neuronal identities during neocortical development. J Neurosci 31: 549-564.
51. Metin C, Godement P. 1996. The ganglionic eminence may be an intermediate target for corticofugal and thalamocortical axons. J Neurosci 16: 3219-3235.
52. Miller B, Chou L, Finlay BL. 1993. The early development of thalamocortical and corticothalamic projections. J Comp Neurol 335: 16-41.
53. Mimura N, Hamada H, Kashio M, Jin H, Toyama Y, Kimura K, Iida M, Goto S, Saisho H, Toshimori K, Koseki H, Aoe T. 2007. Aberrant quality control in the endoplasmic reticulum impairs the biosynthesis of pulmonary surfactant in mice expressing mutant BiP. Cell Death Differ 14: 1475-1485.
54. Mimura N, Yuasa S, Soma M, Jin H, Kimura K, Goto S, Koseki H, Aoe T. 2008. Altered quality control in the endoplasmic reticulum causes cortical dysplasia in knock-in mice expressing a mutant BiP. Mol Cell Biol 28: 293-301.
55. Mitrofanis J, Baker GE. 1993. Development of the thalamic reticular and perireticular nuclei in rats and their relationship to the course of growing corticofugal and corticopetal axons. J Comp Neurol 338: 575-587.
56. Mizuno A, Villalobos ME, Davies MM, Dahl BC, Muller RA. 2006. Partially enhanced thalamocortical functional connectivity in autism. Brain Res 1104: 160-174.
57. Molnar Z, Blakemore C. 1991. Lack of regional specificity for connections formed between thalamus and cortex in coculture. Nature 351: 475-477.
58. Molnar Z, Cordery P. 1999. Connections between cells of the internal capsule, thalamus, and cerebral cortex in embryonic rat. J Comp Neurol 413: 1-25.
59. Molnar Z, Adams R, Blakemore C. 1998a. Mechanisms underlying the early establishment of thalamocortical connections in the rat. J Neurosci 18: 5723-5745.
60. Molnar Z, Adams R, Goffinet AM, Blakemore C. 1998b. The role of the first postmitotic cortical cells in the development of thalamocortical innervation in the reeler mouse. J Neurosci 18: 5746-5765.
61. Molnar Z, Garel S, Lopez-Bendito G, Maness P, Price DJ. 2012. Mechanisms controlling the guidance of thalamocortical axons through the embryonic forebrain. Eur J Neurosci 35: 1573-1585.
62. Nakagawa Y, O'Leary DD. 2001. Combinatorial expression patterns of LIM-homeodomain and other regulatory genes parcellate developing thalamus. J Neurosci 21: 2711-2725.
63. Ni M, Lee AS. 2007. ER chaperones in mammalian development and human diseases. FEBS Lett 581: 3641-3651.
64. Nicoletti-Carvalho JE, Nogueira TC, Gorjao R, Bromati CR, Yamanaka TS, Boschero AC, Velloso LA, Curi R, Anhe GF, Bordin S. 2010. UPR-mediated TRIB3 expression correlates with reduced AKT phosphorylation and inability of interleukin 6 to overcome palmitate-induced apoptosis in RINm5F cells. J Endocrinol 206: 183-193.
65. Nieto M, Monuki ES, Tang H, Imitola J, Haubst N, Khoury SJ, Cunningham J, Gotz M, Walsh CA. 2004. Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex. J Comp Neurol 479: 168-180.
66. Normington K, Kohno K, Kozutsumi Y, Gething MJ, Sambrook J. 1989. S. cerevisiae encodes an essential protein homologous in sequence and function to mammalian BiP. Cell 57: 1223-1236.
67. Penas C, Font-Nieves M, Fores J, Petegnief V, Planas A, Navarro X, Casas C. 2011. Autophagy, and BiP level decrease are early key events in retrograde degeneration of motoneurons. Cell Death Differ 18: 1617-1627.
68. Polleux F, Ghosh A. 2002. The slice overlay assay: a versatile tool to study the influence of extracellular signals on neuronal development. Sci STKE 136: l9.
69. Price DJ, Kennedy H, Dehay C, Zhou L, Mercier M, Jossin Y, Goffinet AM, Tissir F, Blakey D, Molnar Z. 2006. The development of cortical connections. Eur J Neurosci 23: 910-920.
70. Reddy RK, Mao C, Baumeister P, Austin RC, Kaufman RJ, Lee AS. 2003. Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors: role of ATP binding site in suppression of caspase-7 activation. J Biol Chem 278: 20915-20924.
71. Renvoise B, Blackstone C. 2010. Emerging themes of ER organization in the development and maintenance of axons. Curr Opin Neurobiol 20: 531-537.
72. Salminen A, Paananen R, Karjalainen MK, Tuohimaa A, Luukkonen A, Ojaniemi M, Jouppila P, Glasser S, Haataja R, Vuolteenaho R, Hallman M. 2009. Genetic association of SP-C with duration of preterm premature rupture of fetal membranes and expression in gestational tissues. Ann Med 41: 629-642.
73. Sasagawa Y, Yamanaka K, Ogura T. 2007. ER E3 ubiquitin ligase HRD-1 and its specific partner chaperone BiP play important roles in ERAD and developmental growth in Caenorhabditis elegans. Genes Cells 12: 1063-1073.
74. Satoh T, Furuta K, Tomokiyo K, Nakatsuka D, Tanikawa M, Nakanishi M, Miura M, Tanaka S, Koike T, Hatanaka H, Ikuta K, Suzuki M, Watanabe Y. 2000. Facilitatory roles of novel compounds designed from cyclopentenone prostaglandins on neurite outgrowth-promoting activities of nerve growth factor. J Neurochem 75: 1092-1102.
75. Schroder M, Kaufman RJ. 2005. The mammalian unfolded protein response. Ann Rev Biochem 74: 739-789.
76. Shen X, Ellis RE, Lee K, Liu CY, Yang K, Solomon A, Yoshida H, Morimoto R, Kurnit DM, Mori K, Kaufman RJ. 2001. Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107: 893-903.
77. Sheppard AM, Hamilton SK, Pearlman AL. 1991. Changes in the distribution of extracellular matrix components accompany early morphogenetic events of mammalian cortical development. J Neurosci 11: 3928-3942.
78. Simpson TI, Pratt T, Mason JO, Price DJ. 2009. Normal ventral telencephalic expression of Pax6 is required for normal development of thalamocortical axons in embryonic mice. Neural Dev 4: 19.
79. Stillman AA, Krsnik Z, Sun J, Rasin MR, State MW, Sestan N, Louvi A. 2009. Developmentally regulated and evolutionarily conserved expression of SLITRK1 in brain circuits implicated in Tourette syndrome. J Comp Neurol 513: 21-37.
80. Tuttle R, Nakagawa Y, Johnson JE, O'Leary DD. 1999. Defects in thalamocortical axon pathfinding correlate with altered cell domains in Mash-1-deficient mice. Development 126: 1903-1916.
81. Vuppalanchi D, Coleman J, Yoo S, Merianda TT, Yadhati AG, Hossain J, Blesch A, Willis DE, Twiss JL. 2010. Conserved 3′-untranslated region sequences direct subcellular localization of chaperone protein mRNAs in neurons. J Biol Chem 285: 18025-18038.
82. Wakabayashi Y, Watanabe H, Inoue J, Takeda N, Sakata J, Mishima Y, Hitomi J, Yamamoto T, Utsuyama M, Niwa O, Aizawa S, Kominami R. 2003. Bcl11b is required for differentiation and survival of alphabeta T lymphocytes. Nature Immunol 4: 533-539.
83. Wang M, Ye R, Barron E, Baumeister P, Mao C, Luo S, Fu Y, Luo B, Dubeau L, Hinton DR, Lee AS. 2010. Essential role of the unfolded protein response regulator GRP78/BiP in protection from neuronal apoptosis. Cell Death Differ 17: 488-498.
84. Welsh RC, Chen AC, Taylor SF. 2008. Low-frequency BOLD fluctuations demonstrate altered thalamocortical connectivity in schizophrenia. Schizophr Bull 36: 713-722.
85. Willis DE, van Niekerk EA, Sasaki Y, Mesngon M, Merianda TT, Williams GG, Kendall M, Smith DS, Bassell GJ, Twiss JL. 2007. Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs. J Cell Biol 178: 965-980.
86. Xu D, Perez RE, Rezaiekhaligh MH, Bourdi M, Truog WE. 2009. Knockdown of ERp57 increases BiP/GRP78 induction and protects against hyperoxia and tunicamycin-induced apoptosis. Am J Physiol 297: L44-51.
87. Ye B, Zhang Y, Song W, Younger SH, Jan LY, Jan YN. 2007. Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 130: 717-729.
88. Yuan Y, Cao P, Smith MA, Kramp K, Huang Y, Hisamoto N, Matsumoto K, Hatzoglou M, Jin H, Feng Z. 2011. Dysregulated LRRK2 signaling in response to endoplasmic reticulum stress leads to dopaminergic neuron degeneration in C. elegans. PloS One 6: e22354.
89. Zhang X, Szabo E, Michalak M, Opas M. 2007. Endoplasmic reticulum stress during the embryonic development of the central nervous system in the mouse. Int J Dev Neurosci 25: 455-463.
90. Zhao L, Longo-Guess C, Harris BS, Lee JW, Ackerman SL. 2005. Protein accumulation and neurodegeneration in the woozy mutant mouse is caused by disruption of SIL1, a cochaperone of BiP. Nat Genet 37: 974-979.
91. Zhao S, Chai X, Forster E, Frotscher M. 2004. Reelin is a positional signal for the lamination of dentate granule cells. Development 131: 5117-5125.