Protein BTG2

Last updated
BTG2
Protein BTG2 PDB 3DJU.png
Available structures
PDB Ortholog search: PDBe RCSB
Identifiers
Aliases BTG2 , PC3, TIS21, BTG family member 2, BTG anti-proliferation factor 2, APRO1
External IDs OMIM: 601597 MGI: 108384 HomoloGene: 31406 GeneCards: BTG2
Orthologs
SpeciesHumanMouse
Entrez

7832

12227

Ensembl

ENSG00000159388

ENSMUSG00000020423

UniProt

P78543

Q04211

RefSeq (mRNA)

NM_006763

NM_007570

RefSeq (protein)

NP_006754

NP_031596

Location (UCSC) Chr 1: 203.31 – 203.31 Mb Chr 1: 134 – 134.01 Mb
PubMed search [3] [4]
Wikidata
View/Edit Human View/Edit Mouse

Protein BTG2 also known as BTG family member 2 or NGF-inducible anti-proliferative protein PC3 or NGF-inducible protein TIS21, is a protein that in humans is encoded by the BTG2 gene (B-cell translocation gene 2) [5] and in other mammals by the homologous Btg2 gene. [6] [7] This protein controls cell cycle progression and proneural genes expression by acting as a transcription coregulator that enhances or inhibits the activity of transcription factors.

Contents

The protein BTG2 is the human homolog of the PC3 (pheochromocytoma cell 3) protein in rat and of the Tis21 (tetradecanoyl phorbol acetate-inducible sequence 21) protein in mouse. [8] [9] Tis21 had been originally isolated as a sequence induced by TPA in mouse fibroblasts, [7] whereas PC3 was originally isolated as sequence induced at the beginning of neuron differentiation; [6] BTG2 was then isolated in human cells as sequence induced by p53 and DNA damage. [5] [10]

The protein encoded by the gene BTG2 (which is the official name assigned to the gene PC3/Tis21/BTG2) is a member of the BTG/Tob family (that comprises six proteins BTG1, BTG2/PC3/Tis21, BTG3/ANA, BTG4/PC3B, Tob1/Tob and Tob2). [8] [9] [11] This family has structurally related proteins that appear to have antiproliferative properties. In particular, the BTG2 protein has been shown to negatively control a cell cycle checkpoint at the G1 to S phase transition in fibroblasts and neuronal cells by direct inhibition of the activity of cyclin D1 promoter. [12] [13] [14]

Regulator of neuron differentiation

A number of studies in vivo have shown that BTG2 expression is associated with the neurogenic asymmetric division in neural progenitor cells. [15] [16] [17] [18] [19] Tis21-GFP has been used as a neurogenic marker because it is not expressed until neurogenesis begins, is present in almost all early-born neurons, and interacts with neuron producing intermediate progenitor cells. [20] Moreover, when directly overexpressed in vivo in neural progenitor cells, BTG2 induces their differentiation. [21] [22] In fact, in the neuronal PC12 cell line BTG2 is not able to trigger differentiation by itself, but only to synergize with NGF, [23] [24] while in vivo BTG2 is fully able to induce differentiation of progenitor cells, i.e., during embryonic development in the neuroblast of the neural tube and in granule precursors of cerebellum, as well in adult progenitor cells of the dentate gyrus and of the subventricular zone. [21] [22] Notably, it has recently been shown that BTG2 is essential for the differentiation of new neurons, using a BTG2 knock out mouse. [25] BTG2 is thus a pan-neural gene required for the development of the new neurons generated during adulthood, in the two neurogenic regions of adult brain, i.e., the hippocampus and the subventricular zone. [25] Such requirement of BTG2 in neuron maturation is consistent with the fact that during brain development BTG2 is expressed in the proliferating neuroblasts of the ventricular zone of the neural tube, and to a lower extent in the differentiating neuroblasts of the mantle zone; postnatally it is expressed in cerebellar precursors mainly in the proliferating regions of the neuropithelium (i.e., in the external granular layer), and in the hippocampus in proliferating and differentiating progenitor cells. [15] [21] [22] The pro-differentiative action of BTG2 appears to be consequent not only to inhibition of cell cycle progression but also to a BTG2-dependent activation of proneural genes in neural progenitor cells. [21] [25] In fact, BTG2 activates proneural genes by associating with the promoter of Id3, a key inhibitor of proneural gene activity, and by negatively regulating its activity. [25]

BTG2 is a transcriptional cofactor, given that it has been shown to associate with, and regulate the promoters not only of Id3 but also of cyclin D1 and RAR-β, being part of transcriptional complexes. [14] [26] [27] It has been shown that when the differentiation of new neurons of the hippocampus - a brain region important for learning and memory - is either accelerated or delayed by means of overexpression or deletion of BTG2, respectively, spatial and contextual memory is heavily altered. [22] [25] This suggests that the time the young neurons spend in different states of neuronal differentiation is critical for their ultimate function in learning and memory, and that BTG2 may play a role in the timing of recruitment of the new neuron into memory circuits. [22] [25]

In conclusion, the main action of Btg2 on neural progenitor cells of the dentate gyrus and subventricular zone during adult neurogenesis is the positive control of their terminal differentiation (see for review: [28] ). During the early postnatal development of the cerebellum, Btg2 is mainly required to control the migration and differentiation of the precursor cells of cerebellar granule neurons. [29] In contrast, BTG1, the closest homolog to Btg2, appears to negatively regulate the proliferation of adult stem cells in the dentate gyrus and subventricular zone, maintaining in quiescence the stem cells pool and preserving it from depletion. [30] [31] BTG1 is also necessary to limit the proliferative expansion of cerebellar precursor cells, as without BTG1 the adult cerebellum is larger and unable to coordinate motor activity. [32]

Medulloblastoma suppressor

BTG2 has been shown to inhibit medulloblastoma, the very aggressive tumor of cerebellum, by inhibiting the proliferation and triggering the differentiation of the precursors of cerebellar granule neurons. This demonstration was obtained by overexpressing BTG2 in a mouse model of medulloblastoma, presenting activation of the sonic hedgehog pathway (heterozygous for the gene Patched1). [14] More recently, it has been shown that the ablation of BTG2 greatly enhances the medulloblastoma frequency by inhibiting the migration of cerebellar granule neuron precursors. This impairment of migration of the precursors of cerebellar granule neurons forces them to remain at the surface of the cerebellum, where they continue to proliferate, becoming target of transforming insults. [33] The impairment of migration of the precursors of cerebellar granule neurons (GCPs) depends on the inhibition of expression of the chemokine CXCL3 consequent to ablation of BTG2. In fact, the transcription of CXCL3 is directly regulated by BTG2, and CXCL3 is able to induce cell-autonomously the migration of cerebellar granule precursors. Treatment with CXCL3 prevents the growth of medulloblastoma lesions in a Shh-type mouse model of medulloblastoma. [34] Thus, CXCL3 is a target for medulloblastoma therapy. [33] [34]

Interactions

BTG2 has been shown to interact with PRMT1, [27] HOXB9, [35] [36] CNOT8 [37] and HDAC1 HDAC4 and HDAC9. [38] [14] It has also been studied with Pax6 and Tbr2 when observing the role of Tis21 in neurogenic divisions. [20]

Related Research Articles

<span class="mw-page-title-main">Cellular differentiation</span> Developmental biology

Cellular differentiation is the process in which a stem cell changes from one type to a differentiated one. Usually, the cell changes to a more specialized type. Differentiation happens multiple times during the development of a multicellular organism as it changes from a simple zygote to a complex system of tissues and cell types. Differentiation continues in adulthood as adult stem cells divide and create fully differentiated daughter cells during tissue repair and during normal cell turnover. Some differentiation occurs in response to antigen exposure. Differentiation dramatically changes a cell's size, shape, membrane potential, metabolic activity, and responsiveness to signals. These changes are largely due to highly controlled modifications in gene expression and are the study of epigenetics. With a few exceptions, cellular differentiation almost never involves a change in the DNA sequence itself. However, metabolic composition does get altered quite dramatically where stem cells are characterized by abundant metabolites with highly unsaturated structures whose levels decrease upon differentiation. Thus, different cells can have very different physical characteristics despite having the same genome.

<span class="mw-page-title-main">MyoD</span> Mammalian protein found in Homo sapiens

MyoD, also known as myoblast determination protein 1, is a protein in animals that plays a major role in regulating muscle differentiation. MyoD, which was discovered in the laboratory of Harold M. Weintraub, belongs to a family of proteins known as myogenic regulatory factors (MRFs). These bHLH transcription factors act sequentially in myogenic differentiation. Vertebrate MRF family members include MyoD1, Myf5, myogenin, and MRF4 (Myf6). In non-vertebrate animals, a single MyoD protein is typically found.

<span class="mw-page-title-main">Medulloblastoma</span> Most common type of primary brain cancer in children

Medulloblastoma is a common type of primary brain cancer in children. It originates in the part of the brain that is towards the back and the bottom, on the floor of the skull, in the cerebellum, or posterior fossa.

<span class="mw-page-title-main">Bone morphogenetic protein 4</span> Human protein and coding gene

Bone morphogenetic protein 4 is a protein that in humans is encoded by BMP4 gene. BMP4 is found on chromosome 14q22-q23.

<span class="mw-page-title-main">CXCL3</span> Mammalian protein found in Homo sapiens

Chemokine ligand 3 (CXCL3) is a small cytokine belonging to the CXC chemokine family that is also known as GRO3 oncogene (GRO3), GRO protein gamma (GROg) and macrophage inflammatory protein-2-beta (MIP2b). CXCL3 controls migration and adhesion of monocytes and mediates its effects on its target cell by interacting with a cell surface chemokine receptor called CXCR2. More recently, it has been shown that Cxcl3 regulates cell autonomously the migration of the precursors of cerebellar granule neurons toward the internal layers of cerebellum, during the morphogenesis of cerebellum. Moreover, if the expression of Cxcl3 is reduced in cerebellar granule neuron precursors, this highly enhances the frequency of the medulloblastoma, the tumor of cerebellum. In fact, the reduced expression of Cxcl3 forces the cerebellar granule neuron precursors to remain at the surface of the cerebellum, where they highly proliferate under the stimulus of Sonic hedgehog, becoming target of transforming insults. Remarkably, the treatment with CXCL3 completely prevents the growth of medulloblastoma lesions in a Shh-type mouse model of medulloblastoma. Thus, CXCL3 is a target for medulloblastoma therapy. Cxcl3 is directly regulated transcriptionally by BTG2

<span class="mw-page-title-main">HDAC1</span> Protein-coding gene in the species Homo sapiens

Histone deacetylase 1 (HDAC1) is an enzyme that in humans is encoded by the HDAC1 gene.

<span class="mw-page-title-main">HDAC4</span>

Histone deacetylase 4, also known as HDAC4, is a protein that in humans is encoded by the HDAC4 gene.

<span class="mw-page-title-main">ID3 (gene)</span> Protein-coding gene in the species Homo sapiens

DNA-binding protein inhibitor ID-3 is a protein that in humans is encoded by the ID3 gene.

<span class="mw-page-title-main">HDAC9</span> Protein-coding gene in the species Homo sapiens

Histone deacetylase 9 is an enzyme that in humans is encoded by the HDAC9 gene.

<span class="mw-page-title-main">HES1</span> Protein-coding gene in the species Homo sapiens

Transcription factor HES1 is a protein that is encoded by the Hes1 gene, and is the mammalian homolog of the hairy gene in Drosophila. HES1 is one of the seven members of the Hes gene family (HES1-7). Hes genes code nuclear proteins that suppress transcription.

<span class="mw-page-title-main">HOXB9</span> Protein-coding gene in humans

Homeobox protein Hox-B9 is a protein that in humans is encoded by the HOXB9 gene.

<span class="mw-page-title-main">IFRD1</span> Protein-coding gene in the species Homo sapiens

Interferon-related developmental regulator 1 is a protein that in humans is encoded by the IFRD1 gene. The gene is expressed mostly in neutrophils, skeletal and cardiac muscle, the brain, and the pancreas. The rat and the mouse homolog genes of interferon-related developmental regulator 1 gene are also known with the name PC4 and Tis21, respectively. IFRD1 is member of a gene family that comprises a second gene, IFRD2, also known as SKmc15.

<span class="mw-page-title-main">CNOT7</span> Protein-coding gene in the species Homo sapiens

CCR4-NOT transcription complex subunit 7 is a protein that in humans is encoded by the CNOT7 gene. It is a subunit of the CCR4-Not deadenylase complex.

<span class="mw-page-title-main">Protein BTG1</span> Protein-coding gene in humans

Protein BTG1 is a protein that in humans is encoded by the BTG1 gene.

Neurogenins, often abbreviated as Ngn, are a family of bHLH transcription factors involved in specifying neuronal differentiation. The family consisting of Neurogenin-1, Neurogenin-2, and Neurogenin-3, plays a fundamental role in specifying neural precursor cells and regulating the differentiation of neurons during embryonic development. It is one of many gene families related to the atonal gene in Drosophila. Other positive regulators of neuronal differentiation also expressed during early neural development include NeuroD and ASCL1.

<span class="mw-page-title-main">ZNF238</span> Protein-coding gene in humans

Zinc finger protein 238 is a zinc finger containing transcription factor that in humans is encoded by the ZNF238 gene.

<span class="mw-page-title-main">Protein BTG3</span> Protein-coding gene in the species Homo sapiens

Protein BTG3 is a protein that in humans is encoded by the BTG3 gene.

<span class="mw-page-title-main">Cerebellar granule cell</span> Thick granular layer of the cerebellar cortex

Cerebellar granule cells form the thick granular layer of the cerebellar cortex and are among the smallest neurons in the brain. Cerebellar granule cells are also the most numerous neurons in the brain: in humans, estimates of their total number average around 50 billion, which means that they constitute about 3/4 of the brain's neurons.

<span class="mw-page-title-main">Protein BTG4</span> Protein-coding gene in the species Homo sapiens

Protein BTG4 also known as BTG family member 4 is a protein that in humans is encoded by the BTG4 gene (B-cell translocation gene 4). BTG4 has anti-proliferative properties and can induce G1 cell cycle arrest.

<span class="mw-page-title-main">Eomesodermin</span> Protein-coding gene in the species Homo sapiens

Eomesodermin also known as T-box brain protein 2 (Tbr2) is a protein that in humans is encoded by the EOMES gene.

References

  1. 1 2 3 GRCh38: Ensembl release 89: ENSG00000159388 - Ensembl, May 2017
  2. 1 2 3 GRCm38: Ensembl release 89: ENSMUSG00000020423 - Ensembl, May 2017
  3. ↑ "Human PubMed Reference:". National Center for Biotechnology Information, U.S. National Library of Medicine.
  4. ↑ "Mouse PubMed Reference:". National Center for Biotechnology Information, U.S. National Library of Medicine.
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  29. ↑ Ceccarelli M, Micheli L, D'Andrea G, De Bardi M, Scheijen B, Ciotti M, Leonardi L, Luvisetto S, Tirone F (December 2015). "Altered cerebellum development and impaired motor coordination in mice lacking the Btg1 gene: Involvement of cyclin D1" (PDF). Developmental Biology. 408 (1): 109–25. doi: 10.1016/j.ydbio.2015.10.007 . PMID   26524254.
  30. ↑ Farioli-Vecchioli S, Micheli L, Saraulli D, Ceccarelli M, Cannas S, Scardigli R, Leonardi L, Cinà I, Costanzi M, Ciotti MT, Moreira P, Rouault JP, Cestari V, Tirone F (2012). "Btg1 is Required to Maintain the Pool of Stem and Progenitor Cells of the Dentate Gyrus and Subventricular Zone". Frontiers in Neuroscience. 6: 124. doi: 10.3389/fnins.2012.00124 . PMC   3431174 . PMID   22969701.
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  32. ↑ Ceccarelli M, Micheli L, D'Andrea G, De Bardi M, Scheijen B, Ciotti M, Leonardi L, Luvisetto S, Tirone F (December 2015). "Altered cerebellum development and impaired motor coordination in mice lacking the Btg1 gene: Involvement of cyclin D1". Developmental Biology. 408 (1): 109–25. doi: 10.1016/j.ydbio.2015.10.007 . PMID   26524254. http://www.inmm.cnr.it/tirone/pdfs/Dev%20Biol%202015.pdf
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  34. 1 2 Ceccarelli M, Micheli L, Tirone F (2016). "Suppression of Medulloblastoma Lesions by Forced Migration of Preneoplastic Precursor Cells with Intracerebellar Administration of the Chemokine Cxcl3". Frontiers in Pharmacology. 7: 484. doi: 10.3389/fphar.2016.00484 . PMC   5159413 . PMID   28018222.
  35. ↑ Prévôt D, Voeltzel T, Birot AM, Morel AP, Rostan MC, Magaud JP, Corbo L (January 2000). "The leukemia-associated protein Btg1 and the p53-regulated protein Btg2 interact with the homeoprotein Hoxb9 and enhance its transcriptional activation". The Journal of Biological Chemistry. 275 (1): 147–53. doi: 10.1074/jbc.275.1.147 . PMID   10617598.
  36. ↑ Berthet C, Guéhenneux F, Revol V, Samarut C, Lukaszewicz A, Dehay C, Dumontet C, Magaud JP, Rouault JP (January 2002). "Interaction of PRMT1 with BTG/TOB proteins in cell signalling: molecular analysis and functional aspects". Genes to Cells. 7 (1): 29–39. doi: 10.1046/j.1356-9597.2001.00497.x . PMID   11856371.
  37. ↑ Prévôt D, Morel AP, Voeltzel T, Rostan MC, Rimokh R, Magaud JP, Corbo L (March 2001). "Relationships of the antiproliferative proteins BTG1 and BTG2 with CAF1, the human homolog of a component of the yeast CCR4 transcriptional complex: involvement in estrogen receptor alpha signaling pathway". The Journal of Biological Chemistry. 276 (13): 9640–8. doi: 10.1074/jbc.M008201200 . PMID   11136725.
  38. ↑ Micheli L, D'Andrea G, Leonardi L, Tirone F (2017). "HDAC1, HDAC4, and HDAC9 Bind to PC3/Tis21/Btg2 and Are Required for Its Inhibition of Cell Cycle Progression and Cyclin D1 Expression" (PDF). Journal of Cellular Physiology. 232 (7): 1696–1707. doi:10.1002/jcp.25467. PMID   27333946. S2CID   4070837.

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