β1-Integrins Are Critical for Cerebellar Granule Cell Precursor Proliferation

Journal of Neuroscience

Volumn 24, Issue 13, 2004, Pages 3402-3412

  Blaess, Sandra ^a   Graus Porta, Diana ^b   Belvindrah, Richard ^c   Radakovits, Randor ^c   Pons, Sebastian ^d   Littlewood Evans, Amanda ^b   Senften, Mathias ^c   Guo, Huailian ^e   Li, Yuqing ^e   Miner, Jeffrey H ^f   Reichardt, Louis F ^g   Müller, Ulrich ^c  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NOVARTIS PHARMA AG   (Switzerland)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d INST D INVESTIGACIONS B   (Spain)

^e UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^f WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Granule cell precursor; Integrin; Laminin; Proliferation; Sonic hedgehog

Indexed keywords

BETA1 INTEGRIN; CDKN1B PROTEIN, MOUSE; CELL CYCLE PROTEIN; CRE RECOMBINASE; CYCLIN DEPENDENT KINASE INHIBITOR 1B; GROWTH PROMOTOR; INTEGRASE; LAMININ; LAMININ 1; SONIC HEDGEHOG PROTEIN; TRANSACTIVATOR PROTEIN; TUMOR SUPPRESSOR PROTEIN; VIRUS PROTEIN;

ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN SIZE; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CEREBELLUM CORTEX; CONTROLLED STUDY; EMBRYO; GRANULE CELL; HEDGEHOG; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; CELL DIVISION; CYTOLOGY; DRUG EFFECT; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENE TARGETING; GENETICS; GROWTH, DEVELOPMENT AND AGING; IN SITU HYBRIDIZATION; METABOLISM; METHODOLOGY; MOUSE MUTANT; NERVE CELL; PHYSIOLOGY; PRENATAL DEVELOPMENT; STEM CELL; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD29; CELL CYCLE PROTEINS; CELL DIVISION; CELLS, CULTURED; CEREBELLUM; CYCLIN-DEPENDENT KINASE INHIBITOR P27; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE TARGETING; GROWTH SUBSTANCES; HEDGEHOG PROTEINS; IN SITU HYBRIDIZATION; INTEGRASES; LAMININ; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURONS; SIGNAL TRANSDUCTION; STEM CELLS; TRANS-ACTIVATORS; TUMOR SUPPRESSOR PROTEINS; VIRAL PROTEINS;

EID: 1842610839     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5241-03.2004     Document Type: Article

References (47)

1. Altman J, Bayer SA (1997) Development of the cerebellar system in relation to its evolution, structure, and function. New York: CRC.
2. Baeg GH, Perrimon N (2000) Functional binding of secreted molecules to heparan sulfate proteoglycans in Drosophila. Curr Opin Cell Biol 12:575-580.
3. Barakat I, Wittendorp-Rechenmann W, Rechenmann RV, Sensenbrenner M (1981) Influence of meningeal cells on the proliferation of neuroblasts in culture. Dev Neurosci 4:363-372.
4. Bellaiche Y, The I, Perrimon N (1998) Tout-velu is a Drosophila bomologue of the putative tumour suppressor EXT-1 and is needed for Hh diffusion. Nature 394:85-88.
5. Bhatt RS, Tomoda T, Fang Y, Hatten ME (2000) Discoidin domain receptor 1 functions in axon extension of cerebellar granule neurons. Genes Dev 14:2216-2228.
6. Brakebusch C, Grose R, Quondamatteo F, Ramirez A, Jorcano JL, Pirro A, Svensson M, Herken R, Sasaki T, Timpl R, Werner S, Fassler R (2000) Skin and hair follicle integrity is crucially dependent on beta 1 integrin expression on keratinocytes. EMBO J 19:3990-4003.
7. Carroll JM, Romero MR, Watt FM (1995) Suprabasal integrin expression in the epidermis of transgenic mice results in developmental defects and a phenotype resembling psoriasis. Cell 83:957-968.
8. Colognato H, Yurchenco PD (2000) Form and function: the laminin family of heterotrimers. Dev Dyn 218:213-234.
9. Dahmane N, Ruiz-i-Altaba A (1999) Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126:3089-3100.
10. Diaz E, Ge Y, Yang YH, Loh KC, Serafini TA, Okazaki Y, Hayashizaki Y, Speed TP, Ngai J, Scheiffele P (2002) Molecular analysis of gene expression in the developing pontocerebellar projection system. Neuron 36:417-434.
11. Fang F, Orend G, Watanabe N, Hunter T, Ruoslahti E (1996) Dependence of cyclin E-CDK2 kinase activity on cell anchorage. Science 271:499-502
12. Furley AJ, Morton SB, Manalo D, Karagogeos D, Dodd J, Jessell TM (1990) The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth-promoting activity. Cell 61:157-170.
13. Gao WO, Heintz N, Hatten ME (1991) Cerebellar granule cell neurogenesis is regulated by cell-cell interactions in vitro. Neuron 6:705-715.
14. Georges-Labouesse E, Messaddeq N, Yehia G, Cadalbert L, Dierich A, Le Meur M (1996) Absence of integrin alpha 6 leads to epidermolysis bullosa and neonatal death in mice. Nat Genet 13:370-373.
15. Giancotti FG, Ruoslahti E (1999) Integrin signaling. Science 285:1028-1032.
16. Graus-Porta D, Blaess S, Senften M, Littlewood-Evans A, Damsky C, Huang Z, Orban P, Klein R, Schittny JC, Muller U (2001) Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 31:367-379.
17. Gritli-Linde A, Lewis P, McMahon AP, Linde A (2001) The whereabouts of a morphogen: direct evidence for short- and graded long-range activity of hedgehog signaling peptides. Dev Biol 236:364-386.
18. Harten ME (1985) Neuronal regulation of astroglial morphology and proliferation in vitro. J Cell Biol 100:384-396.
19. Hatten ME (1999) Central nervous system neuronal migration. Annu Rev Neurosci 22:511-539.
20. Hatten ME, Gao WQ, Morrison MA, Mason CA (1998) The cerebellum: purification and coculture of identified cell populations. In: Culturing nerve cells (Banker G, Goslin K, eds). Cambridge, Massachusetts: MIT.
21. Helms AW, Johnson JE (1998) Progenitors of dorsal commissural interneurons are defined by MATH1 expression. Development 125:919-928.
22. Hemler ME (1999) Integrins. In: Guidebook to the Extracellular Matris, Anchor and Adhesion Proteins (Kreis T, Vale R, eds), pp 196-212. New York: Oxford University Press.
23. Henry MD, Campbell KP (1999) Dystroglycan inside and out. Curr Opin Cell Biol 11:602-607.
24. Herrup K, Kuemerle B (1997) The compartmentalization of the cerebellum. Annu Rev Neurosci 20:61-90.
25. Huard JM, Forster CC, Carter ML, Sicinski P, Ross ME (1999) Cerebellar histogenesis is disturbed in mice lacking cyclin D2. Development 126:1927-1935.
26. Kenney AM, Rowitch DH (2000) Sonic hedgehog promotes G(1) cyclin expression and sustained cell cycle progression in mammalian neuronal precursors. Mol Cell Biol 20:9055-9067.
27. Klein RS, Rubin JB, Gibson HD, DeHaan EN, Alvarez-Hernandez X, Segal RA, Luster AD (2001) SDF-1 alpha induces chemotaxis and enhances Sonic hedgehog-induced proliferation of cerebellar granule cells. Development 128:1971-1981.
28. Kuhar SG, Feng L, Vidan S, Ross ME, Hatten ME, Heintz N (1993) Changing patterns of gene expression define four stages of cerebellar granule neuron differentiation. Development 117:97-104.
29. Mao X, Fujiwara Y, Orkin SH (1999) Improved reporter strain for monitoring Cre recombinase-mediated DNA excisions in mice. Proc Natl Acad Sci USA 96:5037-5042.
30. Miner J, Patton BL, Lentz SI, Gilbert DJ, Snider WD, Jenkins NA, Copeland NG, Sanes JR (1997) THe laminin alpha chains: expression, developmental transitions, and chromosomal locations of alpha 1-5, identification of heterotrimeric laminins 8-11, and cloning of a novel alpha 3 isoform. J Cell Biol 137:685-701.
31. Miyazawa K, Himi T, Garcia V, Yamagishi H, Sato S, Ishizaki Y (2000) A role for p27-Kip1 in the control of cerebellar granule cell precursor proliferation. J Neurosci 20:5756-5763.
32. Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
33. Noakes PG, Miner JH, Gautam M, Cunningham JM, Sanes JR, Merlie JP (1995) The renal glomerulus of mice lacking s-laminin/laminin beta 2: nephrosis despite molecular compensation by laminin beta 1. Nat Genet 10:400-406.
34. Pons S, Marti E (2000) Shh synergizes with the extracellular matrix protein vitronectin to induce spinal motor neuron differentiation. Development 127:333-342.
35. Pons S, Trejo JL, Martinez-Morales JR, Marti E (2001) Vitronectin regulates Sonic hedgehog activity during cerebellum development through CREB phosphorylation. Development 128:1481-1492.
36. Raghavan S, Bauer C, Mundschau G, Li Q, Fuchs E (2000) Conditional ablation of beta1 integrin in skin. Severe defects in epidermal proliferation, basement membrane formation, and hair follicle invagination. J Cell Biol 150:1149-1160.
37. Rubin JB, Choi Y, Segal RA (2002) Cerebellar proteoglycans regulate sonic hedgehog responses during development. Development 129:2223-2232.
38. Schwarzbauer J (1999) Basement membranes: Putting up the barriers. Curr Biol 9:R242-244.
39. Smeyne RJ, Chu T, Lewin A, Bian F, S SC, Kunsch C, Lira SA, Oberdick J (1995) Local control of granule cell generation by cerebellar Purkinje cells. Mol Cell Neurosci 6:230-251.
40. Stephens LE, Sutherland AE, Klimanskaya IV, Andrieux A, Meneses J, Pedersen RA, Damsky CH (1995) Deletion of beta 1 integrinsin mice results in inner cell mass failure and peri-implantation lethality. Genes Dev 9:1883-1895.
41. The I, Bellaiche Y, Perrimon N (1999) Hedgehog movement is regulated through tout velu-dependent synthesis of a heparan sulfate proteoglycan. Mol Cell 4:633-639.
42. Thompson CL, Stephenson FA (1994) GABAA receptor subtypes expressed in cerebellar granule cells: a developmental study. J Neurochem 62:2037-2044.
43. Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, Orban PC, Bock R, Klein R, Schutz G (1999) Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23:99-103.
44. Wallace VA (1999) Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr Biol 9:445-448.
45. Wechsler-Reya RJ, Scott MP (1999) Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22:103-114.
46. Zhao Q, Kho A, Kenney AM, Yuk DI, Kohane I, Rowitch DH (2002) Identification of genes expressed with temporal-spatial restriction to developing cerebellar neuron precursors by a functional genomic approach. Proc Natl Acad Sci USA 99:5704-5709.
47. Zhu X, Ohtsubo M, Bohmer RM, Roberts JM, Assoian RK (1996) Adhesion-dependent cell cycle progression linked to the expression of cyclin DI, activation of cyclin E-cdk2, and phosphorylation of the retinoblastoma protein. J Cell Biol 133:391-403.