Migration of oligodendrocyte progenitor cells is controlled by transforming growth factor β family proteins during corticogenesis

Journal of Neuroscience

Volumn 34, Issue 45, 2014, Pages 14973-14983

  Choe, Youngshik ^a,c   Huynh, Trung ^a   Pleasure, Samuel J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Korea Brain Research Institute (KBRI)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

6 [4 (1 PIPERAZINYL) PHENYL] 3 (4 QUINOLINYL) PYRAZOLO [1, 5 A] PYRIMIDINE; BONE MORPHOGENETIC PROTEIN 4; GREEN FLUORESCENT PROTEIN; KI 67 ANTIGEN; MESSENGER RNA; NOGGIN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; OSTEOGENIC PROTEIN 1; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; SMAD1 PROTEIN; SMAD4 PROTEIN; TRANSCRIPTION FACTOR FOXC1; TRANSCRIPTION FACTOR SOX10; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; WNT1 PROTEIN; BMP4 PROTEIN, MOUSE; BMP7 PROTEIN, MOUSE; SMAD4 PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BOYDEN CHAMBER ASSAY; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN PERICYTE; CELL ACTIVATION; CELL INVASION ASSAY; CELL MIGRATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CORTICOGENESIS; ELECTROPORATION; EMBRYO DEVELOPMENT; FEMALE; FOREBRAIN; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTRACELLULAR SIGNALING; MALE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; TRANSCELLULAR CELL MIGRATION; ANIMAL; CELL MOTION; CYTOLOGY; EMBRYOLOGY; GENETICS; MENINX; MESENCHYMAL STROMA CELL; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; OLIGODENDROGLIA; PERICYTE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 7; CELL MOVEMENT; CEREBRAL CORTEX; MENINGES; MESENCHYMAL STROMAL CELLS; MICE; NEURAL STEM CELLS; NEUROGENESIS; OLIGODENDROGLIA; PERICYTES; SIGNAL TRANSDUCTION; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84908529632     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1156-14.2014     Document Type: Article

References (53)

1. Ara J, See J, Mamontov P, Hahn A, Bannerman P, Pleasure D, Grinspan JB (2008) Bone morphogenetic proteins 4, 6, and 7 are up-regulated in mouse spinal cord during experimental autoimmune encephalomyelitis. J Neurosci Res 86:125-135. CrossRef Medline
2. Bagri A, Gurney T, He X, Zou YR, Littman DR, Tessier-Lavigne M, Pleasure SJ (2002) The chemokine SDF1 regulates migration of dentate granule cells. Development 129:4249-4260.Medline
3. Bardeesy N, Cheng KH, Berger JH, Chu GC, Pahler J, Olson P, Hezel AF, Horner J, Lauwers GY, Hanahan D, DePinho RA (2006) Smad4 is dispensable for normal pancreas development yet critical in progression and tumor biology of pancreas cancer. Genes Dev 20:3130-3146. CrossRef Medline
4. Bribián A, Esteban PF, Clemente D, Soussi-Yanicostas N, Thomas JL, Zalc B, de Castro F (2008) A novel role for anosmin-1 in the adhesion and migration of oligodendrocyte precursors. Dev Neurobiol 68:1503-1516. CrossRef Medline
5. Chang W, Lin Z, Kulessa H, Hebert J, Hogan BL, Wu DK (2008) Bmp4 is essential for the formation of the vestibular apparatus that detects angular head movements. PLoS Genet 4:e1000050. CrossRef Medline
6. Choe Y, Siegenthaler JA, Pleasure SJ (2012) A cascade of morphogenic signaling initiated by the meninges controls corpus callosum formation. Neuron 73:698-712. CrossRef Medline
7. Choe Y, Kozlova A, Graf D, Pleasure SJ (2013) Bone morphogenic protein signaling is a major determinant of dentate development. J Neurosci 33: 6766-6775. CrossRef Medline
8. Cuny GD, Yu PB, Laha JK, Xing X, Liu JF, Lai CS, Deng DY, Sachidanandan C, Bloch KD, Peterson RT (2008) Structure-activity relationship study of bone morphogenetic protein (BMP) signaling inhibitors. Bioorg Med Chem Lett 18:4388-4392. CrossRef Medline
9. Danielian PS, Muccino D, Rowitch DH, Michael SK, McMahon AP (1998) Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr Biol 8:1323-1326. CrossRef Medline
10. Dizon ML, Maa T, Kessler JA (2011) The bone morphogenetic protein antagonist noggin protects white matter after perinatal hypoxia-ischemia. Neurobiol Dis 42:318-326. CrossRef Medline
11. Dudas M, Sridurongrit S, Nagy A, Okazaki K, Kaartinen V (2004) Craniofacial defects in mice lackingBMPtype I receptor Alk2 in neural crest cells. Mech Dev 121:173-182. CrossRef Medline
12. Dummula K, Vinukonda G, Chu P, Xing Y, Hu F, Mailk S, Csiszar A, Chua C, Mouton P, Kayton RJ, Brumberg JC, Bansal R, Ballabh P (2011) Bone morphogenetic protein inhibition promotes neurological recovery after intraventricular hemorrhage. J Neurosci 31:12068-12082. CrossRef Medline
13. Foo SS, Turner CJ, Adams S, Compagni A, Aubyn D, Kogata N, Lindblom P, Shani M, Zicha D, Adams RH (2006) Ephrin-B2 controls cell motility and adhesion during blood-vessel-wall assembly. Cell 124:161-173. CrossRef Medline
14. Foppiano S, Hu D, Marcucio RS (2007) Signaling by bone morphogenetic proteins directs formation of an ectodermal signaling center that regulates craniofacial development. Dev Biol 312:103-114. CrossRef Medline
15. Fuller ML, DeChant AK, Rothstein B, Caprariello A, Wang R, Hall AK, Miller RH (2007) Bone morphogenetic proteins promote gliosis in demyelinating spinal cord lesions. Ann Neurol 62:288-300. CrossRef Medline
16. Furuta Y, Piston DW, Hogan BL (1997) Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124: 2203-2212.Medline
17. Goldstein AM, Brewer KC, Doyle AM, Nagy N, Roberts DJ (2005) BMPsignaling is necessary for neural crest cell migration and ganglion formation in the enteric nervous system. Mech Dev 122:821-833. CrossRef Medline
18. Gomes WA, Mehler MF, Kessler JA (2003) Transgenic overexpression of BMP4 increases astroglial and decreases oligodendroglial lineage commitment. Dev Biol 255:164-177. CrossRef Medline
19. Gross RE, Mehler MF, Mabie PC, Zang Z, Santschi L, Kessler JA (1996) Bone morphogeneticproteinspromoteastrogliallineagecommitmentbymammaliansubventricular zone progenitor cells. Neuron 17:595-606. CrossRef Medline
20. Hayashi H, Kume T (2008) Forkhead transcription factors regulate expression of the chemokine receptor CXCR4 in endothelial cells and CXCL12-induced cell migration. Biochem Biophys ResCommun367:584-589. CrossRef Medline
21. Hogan BL (1996) Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev 10:1580-1594. CrossRef Medline
22. Hughes EG, Kang SH, Fukaya M, Bergles DE (2013) Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain. Nat Neurosci 16:668-676. CrossRef Medline
23. Jablonska B, Aguirre A, Raymond M, Szabo G, Kitabatake Y, Sailor KA, Ming GL, Song H, Gallo V (2010) Chordin-induced lineage plasticity of adult SVZ neuroblasts after demyelination. Nat Neurosci 13:541-550. CrossRef Medline
24. Keller B, Yang T, Chen Y, Munivez E, Bertin T, Zabel B, Lee B (2011) Interaction of TGFbeta and BMP signaling pathways during chondrogenesis. PLoS One 6:e16421. CrossRef Medline
25. Kessaris N, Fogarty M, Iannarelli P, Grist M, Wegner M, Richardson WD (2006) Competingwaves of oligodendrocytes in the forebrainandpostnatal elimination of an embryonic lineage. Nat Neurosci 9:173-179. CrossRef Medline
26. Klämbt C (2009) Modes and regulation of glial migration in vertebrates and invertebrates. Nat Rev Neurosci 10:769-779. CrossRef Medline
27. Kondo T, Raff MC (2004) A role for Noggin in the development of oligodendrocyte precursor cells. Dev Biol 267:242-251. CrossRef Medline
28. Langseth AJ, Munji RN, Choe Y, Huynh T, Pozniak CD, Pleasure SJ (2010) Wnts influence the timing and efficiency of oligodendrocyte precursor cell generation in the telencephalon. J Neurosci 30:13367-13372. CrossRef Medline
29. Lim DA, Tramontin AD, Trevejo JM, Herrera DG, García-Verdugo JM, Alvarez-Buylla A (2000) Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28:713-726. CrossRef Medline
30. Lind M, Eriksen EF, Bünger C (1996) Bone morphogenetic protein-2 but not bone morphogenetic protein-4 and-6 stimulates chemotactic migration of human osteoblasts, human marrow osteoblasts, and U2-OS cells. Bone 18:53-57. CrossRef Medline
31. Matsuoka T, Ahlberg PE, Kessaris N, Iannarelli P, Dennehy U, Richardson WD, McMahon AP, Koentges G (2005) Neural crest origins of the neck and shoulder. Nature 436:347-355. CrossRef Medline
32. McKinnon RD, Piras G, Ida JA Jr, Dubois-Dalcq M (1993) A role for TGFbeta in oligodendrocyte differentiation. J Cell Biol 121:1397-1407. CrossRef Medline
33. Mekki-Dauriac S, Agius E, Kan P, Cochard P (2002) Bone morphogenetic proteins negatively control oligodendrocyte precursor specification in the chick spinal cord. Development 129:5117-5130.Medline
34. Miller RH, Dinsio K, Wang R, Geertman R, Maier CE, Hall AK (2004) Patterning of spinal cord oligodendrocyte development by dorsally derived BMP4. J Neurosci Res 76:9-19. CrossRef Medline
35. Nakahira E, Kagawa T, Shimizu T, Goulding MD, Ikenaka K (2006) Direct evidence that ventral forebrain cells migrate to the cortex and contribute to the generation of cortical myelinating oligodendrocytes. Dev Biol 291: 123-131. CrossRef Medline
36. Nomura M, Li E (1998) Smad2 role in mesoderm formation, left-right patterning and craniofacial development. Nature 393:786-790. CrossRef Medline
37. Piaton G, Aigrot MS, Williams A, Moyon S, Tepavcevic V, Moutkine I, Gras J, Matho KS, Schmitt A, Soellner H, Huber AB, Ravassard P, Lubetzki C (2011) Class 3 semaphorins influence oligodendrocyte precursor recruitment and remyelination in adult central nervous system. Brain 134: 1156-1167. CrossRef Medline
38. Prestoz L, Chatzopoulou E, Lemkine G, Spassky N, Lebras B, Kagawa T, Ikenaka K, Zalc B, Thomas JL (2004) Control of axonophilic migration of oligodendrocyte precursor cells by Eph-ephrin interaction. Neuron Glia Biol 1:73-83. CrossRef Medline
39. Rowitch DH (2004) Glial specification in the vertebrate neural tube. Nat Rev Neurosci 5:409-419. CrossRef Medline
40. Sabo JK, Aumann TD, Merlo D, Kilpatrick TJ, Cate HS (2011) Remyelination is altered by bone morphogenic protein signaling in demyelinated lesions. J Neurosci 31:4504-4510. CrossRef Medline
41. Samanta J, Burke GM, McGuire T, Pisarek AJ, Mukhopadhyay A, Mishina Y, Kessler JA (2007) BMPR1a signaling determines numbers of oligodendrocytes and calbindin-expressing interneurons in the cortex. J Neurosci 27:7397-7407. CrossRef Medline
42. See J, Zhang X, Eraydin N, Mun SB, Mamontov P, Golden JA, Grinspan JB (2004) Oligodendrocyte maturation is inhibited by bone morphogenetic protein. Mol Cell Neurosci 26:481-492. CrossRef Medline
43. See J, Mamontov P, Ahn K, Wine-Lee L, Crenshaw EB III, Grinspan JB (2007) BMP signaling mutant mice exhibit glial cell maturation defects. Mol Cell Neurosci 35:171-182. CrossRef Medline
44. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, Allen R, Sidman C, Proetzel G, Calvin D (1992) Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 359:693-699. CrossRef Medline
45. Sotobori T, Ueda T, Myoui A, Yoshioka K, Nakasaki M, Yoshikawa H, Itoh K (2006) Bone morphogenetic protein-2 promotes the haptotactic migration of murine osteoblastic and osteosarcoma cells by enhancing incorporation of integrin beta1 into lipid rafts. Exp Cell Res 312:3927-3938. CrossRef Medline
46. Spinella-Jaegle S, Roman-Roman S, Faucheu C, Dunn FW, Kawai S, Galléa S, Stiot V, Blanchet AM, Courtois B, Baron R, Rawadi G (2001) Opposite effects of bone morphogenetic protein-2 and transforming growth factorbeta1 on osteoblast differentiation. Bone 29:323-330. CrossRef Medline
47. Tsai HH, Macklin WB, Miller RH (2006) Netrin-1 is required for the normal development of spinal cord oligodendrocytes. J Neurosci 26:1913-1922. CrossRef Medline
48. Wang Y, Cheng X, He Q, Zheng Y, Kim DH, Whittemore SR, Cao QL (2011) Astrocytes from the contused spinal cord inhibit oligodendrocyte differentiation of adult oligodendrocyte precursor cells by increasing the expression of bone morphogenetic proteins. J Neurosci 31:6053-6058. CrossRef Medline
49. Yeh HJ, Ruit KG, Wang YX, Parks WC, Snider WD, Deuel TF (1991) PDGF A-chain gene is expressed by mammalian neurons during development and in maturity. Cell 64:209-216. CrossRef Medline
50. Zhang Y, Zhang J, Navrazhina K, Argaw AT, Zameer A, Gurfein BT, Brosnan CF, John GR (2010) TGFbeta1 induces Jagged1 expression in astrocytes via ALK5 and Smad3 and regulates the balance between oligodendrocyte progenitor proliferation and differentiation. Glia 58:964-974. CrossRef Medline
51. Zhou Y, Liu HX, Mistretta CM (2006) Bone morphogenetic proteins and noggin: inhibiting and inducing fungiform taste papilla development. Dev Biol 297:198-213. CrossRef Medline
52. Zhu G, Mehler MF, Mabie PC, Kessler JA (1999) Developmental changes in progenitor cell responsiveness to cytokines. J Neurosci Res 56:131-145. CrossRef Medline
53. Zouvelou V, Passa O, Segklia K, Tsalavos S, Valenzuela DM, Economides AN, Graf D (2009) Generation and functional characterization of mice with a conditional BMP7 allele. Int J Dev Biol 53:597-603. CrossRef Medline