Members of the high mobility group B protein family are dynamically expressed in embryonic neural stem cells

Proteome Science

Volumn 11, Issue 1, 2013, Pages

  Abraham, Ariel B ^a,d   Bronstein, Robert ^a   Chen, Emily I ^a   Koller, Antonius ^a   Ronfani, Lorenza ^b   Maletic Savatic, Mirjana ^c   Tsirka, Stella E ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d STONY BROOK UNIVERSITY   (United States)

Author keywords

HMGB; Mice; Shotgun proteomics; Subventricular zone

Indexed keywords

CASPASE 3; GLIAL FIBRILLARY ACIDIC PROTEIN; HETEROCHROMATIN PROTEIN 1; HIGH MOBILITY GROUP B PROTEIN; HIGH MOBILITY GROUP B1 PROTEIN; HIGH MOBILITY GROUP B2 PROTEIN; HIGH MOBILITY GROUP B3 PROTEIN; HIGH MOBILITY GROUP B4 PROTEIN; MARCKS PROTEIN; MESSENGER RNA; NESTIN; UNCLASSIFIED DRUG; VIMENTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CELL RENEWAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORRELATION ANALYSIS; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; FOREBRAIN; IMMUNOBLOTTING; MOUSE; NEURAL STEM CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEOMICS; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM;

MAMMALIA; MUS;

EID: 84876679496     PISSN: None     EISSN: 14775956     Source Type: Journal    
DOI: 10.1186/1477-5956-11-18     Document Type: Article

References (49)

1. Kriegstein A, Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 2009, 32:149-184. 10.1146/annurev.neuro.051508.135600, 3086722, 19555289.
2. Gage FH. Mammalian neural stem cells. Science 2000, 287(5457):1433-1438. 10.1126/science.287.5457.1433, 10688783.
3. Ming GL, Song H. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 2005, 28:223-250. 10.1146/annurev.neuro.28.051804.101459, 16022595.
4. Reynolds BA, Tetzlaff W, Weiss S. A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci 1992, 12(11):4565-4574.
5. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992, 255(5052):1707-1710. 10.1126/science.1553558, 1553558.
6. Reynolds BA, Weiss S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol 1996, 175(1):1-13. 10.1006/dbio.1996.0090, 8608856.
7. Gritti A, Frolichsthal-Schoeller P, Galli R, Parati EA, Cova L, Pagano SF, Bjornson CR, Vescovi AL. Epidermal and fibroblast growth factors behave as mitogenic regulators for a single multipotent stem cell-like population from the subventricular region of the adult mouse forebrain. J Neurosci 1999, 19(9):3287-3297.
8. Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 2002, 36(6):1021-1034. 10.1016/S0896-6273(02)01133-9, 12495619.
9. Maslov AY, Barone TA, Plunkett RJ, Pruitt SC. Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice. J Neurosci 2004, 24(7):1726-1733. 10.1523/JNEUROSCI.4608-03.2004, 14973255.
10. Molofsky AV, Slutsky SG, Joseph NM, He S, Pardal R, Krishnamurthy J, Sharpless NE, Morrison SJ. Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature 2006, 443(7110):448-452. 10.1038/nature05091, 2586960, 16957738.
11. Nishino J, Kim I, Chada K, Morrison SJ. Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4a and p19Arf Expression. Cell 2008, 135(2):227-239. 10.1016/j.cell.2008.09.017, 2582221, 18957199.
12. Bustin M. Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol Cell Biol 1999, 19(8):5237-5246. 84367, 10409715.
13. Thomas JO. HMG1 and 2: architectural DNA-binding proteins. Biochem Soc Trans 2001, 29(Pt 4):395-401.
14. Hock R, Furusawa T, Ueda T, Bustin M. HMG chromosomal proteins in development and disease. Trends Cell Biol 2007, 17(2):72-79. 10.1016/j.tcb.2006.12.001, 2442274, 17169561.
15. Lee YS, Dutta A. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev 2007, 21(9):1025-1030. 10.1101/gad.1540407, 1855228, 17437991.
16. Levi BP, Morrison SJ. Stem cells use distinct self-renewal programs at different ages. Cold Spring Harb Symp Quant Biol 2008, 73:539-553. 10.1101/sqb.2008.73.049, 19150957.
17. Bustin M. Chromatin unfolding and activation by HMGN(*) chromosomal proteins. Trends Biochem Sci 2001, 26(7):431-437. 10.1016/S0968-0004(01)01855-2, 11440855.
18. Bianchi ME, Agresti A. HMG proteins: dynamic players in gene regulation and differentiation. Curr Opin Genet Dev 2005, 15(5):496-506. 10.1016/j.gde.2005.08.007, 16102963.
19. Kishi Y, Fujii Y, Hirabayashi Y, Gotoh Y. HMGA regulates the global chromatin state and neurogenic potential in neocortical precursor cells. Nature Neurosci 2012, 15(8):1127-1133. 10.1038/nn.3165, 22797695.
20. Chaerkady R, Letzen B, Renuse S, Sahasrabuddhe NA, Kumar P, All AH, Thakor NV, Delanghe B, Gearhart JD, Pandey A, et al. Quantitative temporal proteomic analysis of human embryonic stem cell differentiation into oligodendrocyte progenitor cells. Proteomics 2011, 11(20):4007-4020. 10.1002/pmic.201100107, 21770034.
21. Fortunel NO, Otu HH, Ng HH, Chen J, Mu X, Chevassut T, Li X, Joseph M, Bailey C, Hatzfeld JA, et al. Comment on " 'Stemness': transcriptional profiling of embryonic and adult stem cells" and "a stem cell molecular signature". Science 2003, 302(5644):393. author reply 393.
22. Zhao X, Kuja-Panula J, Rouhiainen A, Chen Y-C, Panula P, Rauvala H. High mobility group box-1 (HMGB1; amphoterin) is required for zebrafish brain development. J Biol Chem 2011, 286(26):23200-23213. 10.1074/jbc.M111.223834, 3123087, 21527633.
23. Lim DA, Suarez-Farinas M, Naef F, Hacker CR, Menn B, Takebayashi H, Magnasco M, Patil N, Alvarez-Buylla A. In vivo transcriptional profile analysis reveals RNA splicing and chromatin remodeling as prominent processes for adult neurogenesis. Mol Cell Neurosci 2006, 31(1):131-148. 10.1016/j.mcn.2005.10.005, 16330219.
24. Tanner S, Shu H, Frank A, Wang LC, Zandi E, Mumby M, Pevzner PA, Bafna V. InsPecT: identification of posttranslationally modified peptides from tandem mass spectra. Anal Chem 2005, 77(14):4626-4639. 10.1021/ac050102d, 16013882.
25. Theiler K. The house mouse: atlas of embryonic development 1989, New York: Springer-Verlag.
26. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008, 3(6):1101-1108. 10.1038/nprot.2008.73, 18546601.
27. Parmar M, Skogh C, Bjorklund A, Campbell K. Regional Specification of Neurosphere Cultures Derived from Subregions of the Embryonic Telencephalon. Mol Cell Neurosci 2002, 21:645-656. 10.1006/mcne.2002.1204, 12504597.
28. Pfenninger CV, Roschupkina T, Hertwig F, Kottwitz D, Englund E, Bengzon J, Jacobsen SE, Nuber UA. CD133 is not present on neurogenic astrocytes in the adult subventricular zone, but on embryonic neural stem cells, ependymal cells, and glioblastoma cells. Cancer Res 2007, 67(12):5727-5736. 10.1158/0008-5472.CAN-07-0183, 17575139.
29. Liao L, McClatchy DB, Yates JR. Shotgun proteomics in neuroscience. Neuron 2009, 63(1):12-26. 10.1016/j.neuron.2009.06.011, 2746002, 19607789.
30. Blackshear PJ. The MARCKS family of cellular protein kinase C substrates. J Biol Chem 1993, 268(3):1501-1504.
31. Weimer JM, Yokota Y, Stanco A, Stumpo DJ, Blackshear PJ, Anton ES. MARCKS modulates radial progenitor placement, proliferation and organization in the developing cerebral cortex. Development 2009, 136(17):2965-2975. 10.1242/dev.036616, 2723068, 19666823.
32. Aucott R, Bullwinkel J, Yu Y, Shi W, Billur M, Brown JP, Menzel U, Kioussis D, Wang G, Reisert I, et al. HP1-beta is required for development of the cerebral neocortex and neuromuscular junctions. J Cell Biol 2008, 183(4):597-606. 10.1083/jcb.200804041, 2582898, 19015315.
33. Mignone JL, Kukekov V, Chiang AS, Steindler D, Enikolopov G. Neural stem and progenitor cells in nestin-GFP transgenic mice. J Comp Neurol 2004, 469(3):311-324. 10.1002/cne.10964, 14730584.
34. Gupta A, Tsai L-H, Wynshaw-Boris A. Life is a journey: a genetic look at neocortical development. Nature Rev Gen 2002, 3:342-355.
35. Ronfani L, Ferraguti M, Croci L, Ovitt CE, Scholer HR, Consalez GG, Bianchi ME. Reduced fertility and spermatogenesis defects in mice lacking chromosomal protein Hmgb2. Development 2001, 128(8):1265-1273.
36. Taniguchi N, Carames B, Kawakami Y, Amendt BA, Komiya S, Lotz M. Chromatin protein HMGB2 regulates articular cartilage surface maintenance via beta-catenin pathway. Proc Natl Acad Sci USA 2009, 106(39):16817-16822. 10.1073/pnas.0904414106, 2757822, 19805379.
37. Lei C, Lin S, Zhang C, Tao W, Dong W, Hao Z, Liu M, Wu B. Effects of high-mobility group box1 on cerebral angiogenesis and neurogenesis after intracerebral hemorrhage. Neuroscience 2013, 229:12-19.
38. Taniguchi N, Carames B, Hsu E, Cherqui S, Kawakami Y, Lotz M. Expression patterns and function of chromatin protein HMGB2 during mesenchymal stem cell differentiation. J Biol Chem 2011, 286(48):41489-41498. 10.1074/jbc.M111.236984, 3308860, 21890638.
39. Giraldez AJ, Cinalli RM, Glasner ME, Enright AJ, Thomson JM, Baskerville S, Hammond SM, Bartel DP, Schier AF. MicroRNAs regulate brain morphogenesis in zebrafish. Science 2005, 308(5723):833-838. 10.1126/science.1109020, 15774722.
40. Shi Y, Zhao X, Hsieh J, Wichterle H, Impey S, Banerjee S, Neveu P, Kosik KS. MicroRNA regulation of neural stem cells and neurogenesis. J Neurosci 2010, 30(45):14931-14936. 10.1523/JNEUROSCI.4280-10.2010, 3071711, 21068294.
41. Lang MF, Shi Y. Dynamic Roles of microRNAs in Neurogenesis. Front neuroscience 2012, 6:71.
42. Griffiths-Jones S. miRBase: the microRNA sequence database. Methods Mol Biol 2006, 342:129-138.
43. Griffiths-Jones S, Saini HK, Van Dongen S, Enright AJ, Griffiths-Jones S, Saini HK, Van Dongen S, Enright AJ. miRBase: tools for microRNA genomics. Nucleic Acids Res 2008, 36(Database issue):D154-158. 2238936, 17991681.
44. Cheli S, Francois S, Bodega B, Ferrari F, Tenedini E, Roncaglia E, Ferrari S, Ginelli E, Meneveri R. Expression profiling of FSHD-1 and FSHD-2 cells during myogenic differentiation evidences common and distinctive gene dysregulation patterns. PLoS One 2011, 6(6):e20966. 10.1371/journal.pone.0020966, 3113851, 21695143.
45. Dahlhaus M, Schult C, Lange S, Freund M, Junghanss C. MicroRNA 181a Influences the Expression of HMGB1 and CD4 in Acute Leukemias. Anticancer Res 2013, 33(2):445-452.
46. Maciotta S, Meregalli M, Cassinelli L, Parolini D, Farini A, Fraro GD, Gandolfi F, Forcato M, Ferrari S, Gabellini D, et al. Hmgb3 is regulated by microrna-206 during muscle regeneration. PLoS One 2012, 7(8):e43464. 10.1371/journal.pone.0043464, 3422271, 22912879.
47. Kippin TE, Martens DJ, van der Kooy D. p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferation capacity. Genes Dev 2005, 19(6):756-767. 10.1101/gad.1272305, 1065728, 15769947.
48. Franklin S, Chen H, Mitchell-Jordan S, Ren S, Wang Y, Vondriska TM. Quantitative analysis of the chromatin proteome in disease reveals remodeling principles and identifies high mobility group protein B2 as a regulator of hypertrophic growth. Mol Cell Proteomics 2012, 11(6):M111-014258. 3394943, 22493179.
49. Taniguchi N, Carames B, Ronfani L, Ulmer U, Komiya S, Bianchi ME, Lotz M. Aging-related loss of the chromatin protein HMGB2 in articular cartilage is linked to reduced cellularity and osteoarthritis. Proc Natl Acad Sci USA 2009, 106(4):1181-1186. 10.1073/pnas.0806062106, 2633567, 19139395.