Lamin A/C Mechanotransduction in Laminopathies
Abstract
:1. Introduction
2. Lamins
PDB Code | Segment | X-ray Resolution | a.a. | Chain |
---|---|---|---|---|
1X8Y [94] | Coil 2B | 2.2 Å | 305–389 | Single chain (A) |
3V5B [95] | Coil 2B | 3 Å | 313–386 | Single chain (A) |
1IFR [54] | Globular domain | 1.4 Å | 436–552 | Single chain (A) |
2XV5 [96] | Coil 2B | 2.4 Å | 328–398 | Dimer (A + B) |
6SNZ [86] | Coil 1B | 2.6 Å | 65–222 | Tetramer (A + B + C + D) |
6JLB [23] | Head-coil 2 | 3.2 Å | 1–300 | Tetramer (A + B + C + D) |
PDB Code | Segment | X-ray Resolution | a.a. | Chain |
---|---|---|---|---|
3UMN [97] | Globular domain | 2 Å | 428–550 | Trimer (A + B + C) |
3TYY [97] | Coil 2B | 2.4 Å | 311–388 | Dimer (A + B) |
3. Lamin Binding Partners
4. Lamin A/C Roles in Cell Mechanotransduction
5. Lamin A/C Mechanotransduction in Laminopathies
6. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
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Binding Partner | Description | A-Type Lamin Binding Region | Reference |
---|---|---|---|
Lamin B | Despite their distinct assembly pathways, “the stage is set” for the assembly of A-type lamins. | ND * | [36] |
Nuclear Actin | Essential for the integrity of the nuclear envelope, it mediates chromatin movement during transcription and mitosis. Failure of this binding impairs the role of nuclear actin, as happens in Hutchinson-Gilford Progeria Syndrome (see details in Section 5). | 461–536 and 564–608 | [103,104] |
Emerin | Protein of the LEM-domain family; it is relatively immobile in the INM and it anchors the lamina. It also binds directly to the barrier-to-autointegration factor (BAF), retaining chromatin close to the nuclear envelope during cell interphase and acts on gene expression inhibition. Loss of emerin causes Emery-Dreifuss muscular dystrophy (see details in Section 5). | 384–566 | [105,106,107] |
LAP1 | Integral membrane protein that binds both A- and B-type lamins. Its role has not been characterized yet, but it is involved in Primary dystonia, a central nervous system laminopathy caused by a mutation in torsin A. | ND * | [108] |
LAP2α | The most-studied architectural partner for A-type lamins. It is located inside the nucleus and is necessary to maintain lamin A/C in a soluble and low-assembly state. Its binding to transcriptional regulators suggests its influence in gene regulation either directly, or indirectly through the lamins. Mutations in LAP2α which disrupt the binding to the A lamin are known to cause dilated cardiomyopathy. | 319–566 | [101,109,110,111] |
Nesprin 1α | Nuclear membrane protein that directly binds A-type lamins and emerin and anchors them at the nuclear envelope. Human fibroblasts lacking A-type lamins present mis-localized nesprin 1α and emerin (which are located at the endoplasmic reticulum level) inducing an impaired nuclear geometry and peripheral chromatin loss as occurs in Emery-Dreifuss muscular dystrophy. | ND * | [112,113] |
SUN1/2 | Essential during cell mitosis. Its important role has been recently suggested in anchoring and opening the nuclear pore complex, and therefore, regulating the nuclear influx of transcription factors. | 389–664 | [6,7,114,115] |
SREBP1 a/c | Known to activate genes required for cholesterol biosynthesis and adipocyte differentiation. They bind the Ig-fold domain of A-type lamins. Deregulation of this binding is involved in lipodystrophies. | 389–664 | [116,117] |
MAN1 | LEM-domain protein; it binds BAF directly, but also DNA. It is involved in TGF-β-signaling, important for bone development. | 394–664 | [118,119] |
PKCα | Serine/threonine kinase, activated by many signal pathways and involved in lamin phosphorylation. Once activated, it translocates to the nucleus and binds to the A-type lamin tail to trigger post translational modifications. | 500–664 | [120] |
12(S)-LOX | Lamin binding enzyme 12(S)-lipoxygenase converts arachidonic acid (AA) to 12(S)-hydroxy eicosatetraenoic acid [12(S)-HETE] and is involved in the lipid signaling pathway. It also activates PKCα mediating prostate tumor cell metastasis. | 463–664 | [121,122] |
cFos | Early response transcription factor sequestrated at the nuclear envelope by A-type lamins. During MAP kinase signaling, this binding is released and c-Fos can facilitate cell proliferation. | 81–219, 243–388 and 453–571 | [123,124] |
Rb | Transcriptional regulator that has a central role in cell-cycle control and in apoptosis mechanisms. It directly binds to A-type lamins and to LAP2α. It appears that Rb tumor suppressor activity depends on its attachment to both proteins. | 247–355 | [125,126] |
MOK2 | DNA-binding transcriptional repressor that modulates gene expression activated by the cone-rod homeobox protein (Crx), by competing binding to the same binding sites. It also seems to influence RNA processing. | 243–387 | [127,128] |
IMPORTIN α | Nuclear import receptor. It is supposed to prevent lamins from assembling in the nucleoplasm. | ND * | [129] |
BAF | Non-specific double-stranded DNA-binding protein. It can bridge DNA and interacts with histones. It also binds several transcription activators including Crx, with an analogous function to MOK2. Alterations in BAF expression lead to impaired chromatin structure, nuclear envelope defects and altered gene expression. | 432–544 | [105,107,130,131] |
LAD | Lamina-associated domains containing lowly transcribed genes. They are dynamic structures involved in chromosomes organization, gene repression, and cell differentiation. LAD disruptions have been correlated to diseases such as Hutchinson Gilford progeria syndrome (see details in Section 4 and Section 5). | ND * | [109,132,133] |
Core histones | Their interaction with A-type lamins affects chromatin localization and gene expression. | 396–430 | [100,102] |
PCNA | Necessary to activate the DNA replication machinery, it binds to the Ig-fold domain. | 436–552 | [134] |
DNA | The lamin-DNA interaction occurs directly, but non-specifically, by contacting the minor groove. The DNA-binding region is identical in both lamin A and lamin C. Some lamin A mutations drastically reduce the DNA affinity, leading to gene regulation problems. | 411–553 | [135,136] |
Group | Pathology | OMIM Code | Gene Involved | Reference |
---|---|---|---|---|
1 | Emery-Dreifuss muscular dystrophy, autosomal dominant (EDMD2) | 181350 | LMNA | [171,174,183,184,185] |
1 | Emery-Dreifuss muscular dystrophy, autosomal recessive (EDMD3) | 616516 | LMNA | [174,184,185] |
1 | Limb-girdle muscular dystrophy, type 1B (LGMD1B) | 159001 | LMNA | [171,174] |
1 | Congenital muscular dystrophy (CMD) | 613205 | LMNA | [172] |
1 | Autosomal dominant spinal muscular atrophy (AD-SMA) | 182980 | LMNA | [173] |
1 | Dilated cardiomyopathy 1A (CMD1A) | 115200 | LMNA | [175,184,186] |
1 | Dilated cardiomyopathy with conduction system defects (DCM-CD) | n/a | LMNA | [187,188] |
2 | Dunnigan-type familial partial lipodystrophy (FPLD2) | 151660 | LMNA | [171,177,184,189] |
2 | Metabolic syndrome (MS) | n/a | LMNA | [176] |
2 | Barraquer-Simons syndrome (acquired partial lipodystrophy -APL) | 608709 | LMNB2 | [44] |
3 | Charcot-Marie-Tooth disease, type 2B1 (CMT2B1) | 605588 | LMNA | [178] |
3 | Autosomal dominant leukodystrophy (ADLD) | 169500 | LMNB1: present an extra copy of the gene | [45] |
4 | Hutchinson-Gilford progeria syndrome (HGPS) | 176670 | LMNA: LaminA-Δ50 permanently farnesylated | [171,184,190,191,192] |
4 | Atypical Werner syndrome (WRN) | 277700 | LMNA | [171,180,187] |
4 | Restrictive dermopathy (RD) | 275210 | LMNA | [193] |
4 | Mandibuloacral dysplasia with type A lipodystrophy (MADA) | 248370 | LMNA | [171,181,184,194,195] |
4 | Heart-hand syndrome, Slovenian type (HHS) | 610140 | LMNA | [196] |
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Donnaloja, F.; Carnevali, F.; Jacchetti, E.; Raimondi, M.T. Lamin A/C Mechanotransduction in Laminopathies. Cells 2020, 9, 1306. https://doi.org/10.3390/cells9051306
Donnaloja F, Carnevali F, Jacchetti E, Raimondi MT. Lamin A/C Mechanotransduction in Laminopathies. Cells. 2020; 9(5):1306. https://doi.org/10.3390/cells9051306
Chicago/Turabian StyleDonnaloja, Francesca, Federica Carnevali, Emanuela Jacchetti, and Manuela Teresa Raimondi. 2020. "Lamin A/C Mechanotransduction in Laminopathies" Cells 9, no. 5: 1306. https://doi.org/10.3390/cells9051306