BMPR1a signaling determines numbers of oligodendrocytes and calbindin-expressing interneurons in the cortex

Journal of Neuroscience

Volumn 27, Issue 28, 2007, Pages 7397-7407

  Samanta, Jayshree ^a   Burke, Gordon M ^a   McGuire, Tammy ^a   Pisarek, Anna J ^a   Mukhopadhyay, Abhishek ^a   Mishina, Yuji ^b   Kessler, John A ^a,c  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^c NONE   (United States)

Author keywords

BMPR1a; Calbindin; Knock out mice; Olig1; Oligodendrocyte; Stem cell

Indexed keywords

BONE MORPHOGENETIC PROTEIN RECEPTOR 1; CALBINDIN; CALRETININ; CRE RECOMBINASE; PARVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; CELL CYCLE; CELL LINEAGE; CELL MATURATION; CONTROLLED STUDY; HYPOTHALAMUS NUCLEUS; INTERNEURON; LOXP SITE; MOUSE; MUTANT; NONHUMAN; OLIGODENDROGLIA; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STEM CELL; SUBVENTRICULAR ZONE; WILD TYPE;

AGING; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEINS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELL AGING; CELL COUNT; CELL CYCLE; CELL LINEAGE; CEREBRAL CORTEX; DEATH; GAMMA-AMINOBUTYRIC ACID; INTERNEURONS; MICE; MICE, INBRED C57BL; MUTATION; NEURONS; OLIGODENDROGLIA; SIGNAL TRANSDUCTION; SMAD PROTEINS; STEM CELLS;

EID: 34447503745     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1434-07.2007     Document Type: Article

References (86)

1. Ahn K, Mishina Y, Hanks MC, Behringer RR, Crenshaw III EB (2001) BMPR-IA signaling is required for the formation of the apical ectodermal ridge and dorsal-ventral patterning of the limb. Development 128:4449-4461.
2. Alcantara S, Ferrer I, Soriano E (1993) Postnatal development of parvalbumin and calbindin D28K immunoreactivities in the cerebral cortex of the rat. Anat Embryol (Berl) 188:63-73.
3. Alcantara S, de Lecea L, Del Rio JA, Ferrer I, Soriano E (1996) Transient colocalization of parvalbumin and calbindin D28k in the postnatal cerebral cortex: evidence for a phenotypic shift in developing nonpyramidal neurons. Eur J Neurosci 8:1329-1339.
4. Anderson SA, Qiu M, Bulfone A, Eisenstat DD, Meneses J, Pedersen R, Rubenstein JL (1997) Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron 19:27-37.
5. Anderson SA, Marin O, Horn C, Jennings K, Rubenstein JL (2001) Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128:353-363.
6. Andl T, Ahn K, Kairo A, Chu EY, Wine-Lee L, Reddy ST, Croft NJ, Cebra-Thomas JA, Metzger D, Chambon P, Lyons KM, Mishina Y, Seykora JT, Crenshaw III EB, Millar SE (2004) Epithelial Bmpr1a regulates differentiation and proliferation in postnatal hair follicles and is essential for tooth development. Development 131:2257-2268.
7. Ang Jr ES, Haydar TF, Gluncic V, Rakic P (2003) Four-dimensional migratory coordinates of GABAergic interneurons in the developing mouse cortex. J Neurosci 23:5805-5815.
8. Bansal R, Lakhina V, Remedios R, Tole S (2003) Expression of FGF receptors 1, 2, 3 in the embryonic and postnatal mouse brain compared with Pdgfralpha, Olig2 and Plp/dm20: implications for oligodendrocyte development. Dev Neurosci 25:83-95.
9. Bonaguidi MA, McGuire T, Hu M, Kan L, Samanta J, Kessler JA (2005) LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells. Development 132:5503-5514.
10. Brederlau A, Faigle R, Elmi M, Zarebski A, Sjoberg S, Fujii M, Miyazono K, Funa K (2004) The bone morphogenetic protein type Ib receptor is a major mediator of glial differentiation and cell survival in adult hippocampal progenitor cell culture. Mol Biol Cell 15:3863-3875.
11. Chenn A, Walsh CA (2002) Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297:365-369.
12. Cohen GM (1997) Caspases: the executioners of apoptosis. Biochem J 326:1-16.
13. Corbin JG, Rutlin M, Gaiano N, Fishell G (2003) Combinatorial function of the homeodomain proteins Nkx2.1 and Gsh2 in ventral telencephalic patterning. Development 130:4895-4906.
14. Davis S, Miura S, Hill C, Mishina Y, Klingensmith J (2004) BMP receptor IA is required in the mammalian embryo for endodermal morphogenesis and ectodermal patterning. Dev Biol 270:47- 63.
15. DeFelipe J (1997) Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J Chem Neuroanat 14:1-19.
16. Dewulf N, Verschueren K, Lonnoy O, Moren A, Grimsby S, Vande Spiegle K, Miyazono K, Huylebroeck D, Ten Dijke P (1995) Distinct spatial and temporal expression patterns of two type I receptors for bone morphogenetic proteins during mouse embryogenesis. Endocrinology 136:2652-2663.
17. Earnshaw WC, Martins LM, Kaufmann SH (1999) Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 68:383- 424.
18. Eriksson C, Bjorklund A, Wictorin K (2003) Neuronal differentiation following transplantation of expanded mouse neurosphere cultures derived from different embryonic forebrain regions. Exp Neurol 184:615-635.
19. Furuta Y, Piston DW, Hogan BL (1997) Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124:2203-2212.
20. Gao FB, Durand B, Raff M (1997) Oligodendrocyte precursor cells count time but not cell divisions before differentiation. Curr Biol 7:152-155.
21. Gaussin V, Morley GE, Cox L, Zwijsen A, Vance KM, Emile L, Tian Y, Liu J, Hong C, Myers D, Conway SJ, Depre C, Mishina Y, Behringer RR, Hanks MC, Schneider MD, Huylebroeck D, Fishman GI, Burch JB, Vatner SF (2005) Alk3/Bmpr1a receptor is required for development of the atrioventricular canal into valves and annulus fibrosus. Circ Res 97:219-226.
22. Gratacos E, Checa N, Perez-Navarro E, Alberch J (2001) Brain-derived neurotrophic factor (BDNF) mediates bone morphogenetic protein-2 (BMP-2) effects on cultured striatal neurones. J Neurochem 79:747-755.
23. Gratacos E, Gavalda N, Alberch J (2002) Bone morphogenetic protein-6 is a neurotrophic factor for calbindin-positive striatal neurons. J Neurosci Res 70:638-644.
24. Grinspan JB, Edell E, Carpio DF, Beesley JS, Lavy L, Pleasure D, Golden JA (2000) Stage-specific effects of bone morphogenetic proteins on the oligodendrocyte lineage. J Neurobiol 43:1-17.
25. Gritti I, Manns ID, Mainville L, Jones BE (2003) Parvalbumin, calbindin, or calretinin in cortically projecting and GABAergic, cholinergic, or glutamatergic basal forebrain neurons of the rat. J Comp Neurol 458:11-31.
26. Gross RE, Mehler MF, Mabie PC, Zang Z, Santschi L, Kessler JA (1996) Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17:595-606.
27. Grove EA, Tole S, Limon J, Yip L, Ragsdale CW (1998) The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development 125:2315-2325.
28. Gulacsi A, Lillien L (2003) Sonic hedgehog and bone morphogenetic protein regulate interneuron development from dorsal telencephalic progenitors in vitro. J Neurosci 23:9862-9872.
29. He W, Ingraham C, Rising L, Goderie S, Temple S (2001) Multipotent stem cells from the mouse basal forebrain contribute GABAergic neurons and oligodendrocytes to the cerebral cortex during embryogenesis. J Neurosci 21:8854-8862.
30. Hebert JM, Mishina Y, McConnell SK (2002) BMP signaling is required locally to pattern the dorsal telencephalic midline. Neuron 35:1029-1041.
31. Hof PR, Glezer II, Conde F, Flagg RA, Rubin MB, Nimchinsky EA, Vogt Weisenhorn DM (1999) Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns. J Chem Neuroanat 16:77-116.
32. Jakovcevski I, Zecevic N (2005) Olig transcription factors are expressed in oligodendrocyte and neuronal cells in human fetal CNS. J Neurosci 25:10064-10073.
33. Kee N, Sivalingam S, Boonstra R, Wojtowicz JM (2002) The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Methods 115:97-105.
34. Kessaris N, Fogarty M, Iannarelli P, Grist M, Wegner M, Richardson WD (2006) Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat Neurosci 9:173-179.
35. Kisielewska J, Lu P, Whitaker M (2005) GFP-PCNA as an S-phase marker in embryos during the first and subsequent cell cycles. Biol Cell 97:221-229.
36. Koenig BB, Cook JS, Wolsing DH, Ting J, Tiesman JP, Correa PE, Olson CA, Pecquet AL, Ventura F, Grant RA, et al (1994) Characterization and cloning of a receptor for BMP-2 and BMP-4 from NIH 3T3 cells. Mol Cell Biol 14:5961-5974.
37. Lavdas AA, Grigoriou M, Pachnis V, Parnavelas JG (1999) The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J Neurosci 19:7881-7888.
38. Levison SW, Goldman JE (1997) Multipotential and lineage restricted precursors coexist in the mammalian perinatal subventricular zone. J Neurosci Res 48:83-94.
39. Li W, Cogswell CA, LoTurco JJ (1998) Neuronal differentiation of precursors in the neocortical ventricular zone is triggered by BMP. J Neurosci 18:8853-8862.
40. Lu QR, Yuk D, Alberta JA, Zhu Z, Pawlitzky I, Chan J, McMahon AP, Stiles CD, Rowitch DH (2000) Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25:317-329.
41. Lu QR, Sun T, Zhu Z, Ma N, Garcia M, Stiles CD, Rowitch DH (2002) Commondevelopmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109:75-86.
42. Mabie PC, Mehler MF, Marmur R, Papavasiliou A, Song Q, Kessler JA (1997) Bone morphogenetic proteins induce astroglial differentiation of oligodendroglial-astroglial progenitor cells. J Neurosci 17:4112-4120.
43. Mabie PC, Mehler MF, Kessler JA (1999) Multiple roles of bone morphogenetic protein signaling in the regulation of cortical cell number and phenotype. J Neurosci 19:7077-7088.
44. Maga G, Hubscher U (2003) Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J Cell Sci 116:3051-3060.
45. Massague J (2004) G1 cell-cycle control and cancer. Nature 432:298-306.
46. Mehler MF, Marmur R, Gross R, Mabie PC, Zang Z, Papavasiliou A, Kessler JA (1995) Cytokines regulate the cellular phenotype of developing neural lineage species. Int J Dev Neurosci 13:213-240.
47. Mehler MF, Mabie PC, Zhang D, Kessler JA (1997) Bone morphogenetic proteins in the nervous system. Trends Neurosci 20:309-317.
48. 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.
49. Ming Kwan K, Li AG, Wang XJ, Wurst W, Behringer RR (2004) Essential roles of BMPR-IA signaling in differentiation and growth of hair follicles and in skin tumorigenesis. Genesis 39:10-25.
50. Mishina Y, Suzuki A, Ueno N, Behringer RR (1995) Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev 9:3027-3037.
51. Mishina Y, Hanks MC, Miura S, Tallquist MD, Behringer RR (2002) Generation of Bmpr/Alk3 conditional knockout mice. Genesis 32:69-72.
52. Mishina Y, Starbuck MW, Gentile MA, Fukuda T, Kasparcova V, Seedor JG, Hanks MC, Amling M, Pinero GJ, Harada S, Behringer RR (2004) Bone morphogenetic protein type IA receptor signaling regulates postnatal osteoblast function and bone remodeling. J Biol Chem 279:27560-27566.
53. Nadarajah B, Alifragis P, Wong RO, Parnavelas JG (2003) Neuronal migration in the developing cerebral cortex: observations based on real-time imaging. Cereb Cortex 13:607-611.
54. Nishiyama A, Lin XH, Giese N, Heldin CH, Stallcup WB (1996) Colocalization of NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells in the developing rat brain. J Neurosci Res 43:299-314.
55. Panchision DM, Pickel JM, Studer L, Lee SH, Turner PA, Hazel TG, McKay RD (2001) Sequential actions of BMP receptors control neural precursor cell production and fate. Genes Dev 15:2094-2110.
56. Poncet C, Soula C, Trousse F, Kan P, Hirsinger E, Pourquie O, Duprat AM, Cochard P (1996) Induction of oligodendrocyte progenitors in the trunk neural tube by ventralizing signals: effects of notochord and floor plate grafts, and of sonic hedgehog. Mech Dev 60:13-32.
57. Pringle NP, Yu WP, Guthrie S, Roelink H, Lumsden A, Peterson AC, Richardson WD (1996) Determination of neuroepithelial cell fate: induction of the oligodendrocyte lineage by ventral midline cells and sonic hedgehog. Dev Biol 177:30-42.
58. Qian X, Shen Q, Goderie SK, He W, Capela A, Davis AA, Temple S (2000) Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron 28:69-80.
59. Raff MC, Durand B, Gao FB (1998) Cell number control and timing in animal development: the oligodendrocyte cell lineage. Int J Dev Biol 42:263-267.
60. Samanta J, Kessler JA (2004) Interactions between ID and OLIG proteins mediate the inhibitory effects of BMP4 on oligodendroglial differentiation. Development 131:4131-4142.
61. Scholzen T, Gerdes J (2000) The Ki-67 protein: from the known and the unknown. J Cell Physiol 182:311-322.
62. 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.
63. See J, Mamontov P, Ahn K, Wine-Lee L, Crenshaw III EB, Grinspan JB (2007) BMP signaling mutant mice exhibit glial cell maturation defects. Mol Cell Neurosci 35:171-182.
64. Shibuya H, Iwata H, Masuyama N, Gotoh Y, Yamaguchi K, Irie K, Matsumoto K, Nishida E, Ueno N (1998) Role of TAK1 and TAB1 in BMP signaling in early Xenopus development. EMBO J 17:1019-1028.
65. Stottmann RW, Choi M, Mishina Y, Meyers EN, Klingensmith J (2004) BMP receptor IA is required in mammalian neural crest cells for development of the cardiac outflow tract and ventricular myocardium. Development 131:2205-2218.
66. Stuhmer T, Puelles L, Ekker M, Rubenstein JL (2002) Expression from a Dlx gene enhancer marks adult mouse cortical GABAergic neurons. Cereb Cortex 12:75-85.
67. Szucsik JC, Witte DP, Li H, Pixley SK, Small KM, Potter SS (1997) Altered forebrain and hindbrain development in mice mutant for the Gsh-2 homeobox gene. Dev Biol 191:230-242.
68. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T (2003) Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467:60-79.
69. Tekki-Kessaris N, Woodruff R, Hall AC, Gaffield W, Kimura S, Stiles CD, Rowitch DH, Richardson WD (2001) Hedgehog-dependent oligodendrocyte lineage specification in the telencephalon. Development 128:2545-2554.
70. Temple S, Raff MC (1986) Clonal analysis of oligodendrocyte development in culture: evidence for a developmental clock that counts cell divisions. Cell 44:773-779.
71. ten Dijke P, Korchynskyi O, Valdimarsdottir G, Goumans MJ (2003) Controlling cell fate by bone morphogenetic protein receptors. Mol Cell Endocrinol 211:105-113.
72. Thomaidou D, Mione MC, Cavanagh JF, Parnavelas JG (1997) Apoptosis and its relation to the cell cycle in the developing cerebral cortex. J Neurosci 17:1075-1085.
73. Toresson H, Campbell K (2001) A role for Gsh1 in the developing striatum and olfactory bulb of Gsh2 mutant mice. Development 128:4769-4780.
74. Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A (2001) In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128:3759-3771.
75. Williams BP, Read J, Price J (1991) The generation of neurons and oligodendrocytes from a common precursor cell. Neuron 7:685-693.
76. Wine-Lee L, Ahn KJ, Richardson RD, Mishina Y, Lyons KM, Crenshaw III EB (2004) Signaling through BMP type 1 receptors is required for development of interneuron cell types in the dorsal spinal cord. Development 131:5393-5403.
77. Xu Q, Cobos I, De La Cruz E, Rubenstein JL, Anderson SA (2004) Origins of cortical interneuron subtypes. J Neurosci 24:2612-2622.
78. Xu Q, Wonders CP, Anderson SA (2005) Sonic hedgehog maintains the identity of cortical interneuron progenitors in the ventral telencephalon. Development 132:4987-4998.
79. Yi SE, Daluiski A, Pederson R, Rosen V, Lyons KM (2000) The type I BMP receptor BMPRIB is required for chondrogenesis in the mouse limb. Development 127:621-630.
80. Yuhki M, Yamada M, Kawano M, Iwasato T, Itohara S, Yoshida H, Ogawa M, Mishina Y (2004) BMPR1A signaling is necessary for hair follicle cycling and hair shaft differentiation in mice. Development 131:1825-1833.
81. Yung SY, Gokhan S, Jurcsak J, Molero AE, Abrajano JJ, Mehler MF (2002) Differential modulation of BMP signaling promotes the elaboration of cerebral cortical GABAergic neurons or oligodendrocytes from a common sonic hedgehog-responsive ventral forebrain progenitor species. Proc Natl Acad Sci USA 99:16273-16278.
82. Zhang D, Mehler MF, Song Q, Kessler JA (1998) Development of bone morphogenetic protein receptors in the nervous system and possible roles in regulating trkC expression. J Neurosci 18:3314-3326.
83. Zhang J, Li L (2005) BMP signaling and stem cell regulation. Dev Biol 284:1-11.
84. Zhou Q, Anderson DJ (2002) The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109:61-73.
85. Zhou Q, Wang S, Anderson DJ (2000) Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 25:331-343.
86. Zhu G, Mehler MF, Mabie PC, Kessler JA (1999) Developmental changes in progenitor cell responsiveness to cytokines. J Neurosci Res 56:131-145.