Wikipedia

ANKRD1

Ankyrin repeat domain-containing protein 1, or Cardiac ankyrin repeat protein is a protein that in humans is encoded by the ANKRD1 gene also known as CARP.[4][5][6] CARP is highly expressed in cardiac and skeletal muscle, and is a transcription factor involved in development and under conditions of stress. CARP has been implicated in several diseases, including dilated cardiomyopathy, hypertrophic cardiomyopathy, and several skeletal muscle myopathies.

ANKRD1
Identifiers
AliasesANKRD1, ALRP, C-193, CARP, CVARP, MCARP, bA320F15.2, ankyrin repeat domain 1
External IDsOMIM: 609599; MGI: 1097717; HomoloGene: 8289; GeneCards: ANKRD1; OMA:ANKRD1 - orthologs
Orthologs
SpeciesHumanMouse
Entrez

27063

107765

Ensembl

ENSG00000148677

ENSMUSG00000024803

UniProt

Q15327

Q9CR42

RefSeq (mRNA)

NM_014391

NM_013468

RefSeq (protein)

NP_055206

NP_038496

Location (UCSC)Chr 10: 90.91 – 90.92 Mbn/a
PubMed search[2][3]
Wikidata
View/Edit HumanView/Edit Mouse

Structure

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Human cardiac ankyrin repeat protein is a 36.2kDa protein composed of 319 amino acids.,[7] though in cardiomyocytes, CARP can exist as multiple alternatively spliced forms.[8] CARP contains five tandem ankyrin repeats. Studies have shown that CARP can homodimerize.[9] Studies have also shown that CARP is N-terminally, post-translationally cleaved by calpain-3 in skeletal muscle, suggesting alternate bioactive forms of CARP exist.[10] CARP has been localized to nuclei and Z-discs in animal and human muscle cells, and at intercalated discs in human cardiac muscle cells. [11]

Function

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CARP was originally identified as a YB-1-associating, cardiac-restricted transcription co-repressor in the homeobox NKX2-5 pathway that is involved in cardiac ventricular chamber specification, maturation and morphogenesis,[12][13][14] and whose mRNA levels are exquisitely sensitive to Doxorubicin, mediated through a hydrogen peroxide/ERK/p38MAP kinase-dependent[15][16] as well as M-CAT cis-element-dependent[17] mechanism. Subsequent studies showed that CARP expression in cardiomyocytes is regulated by alpha-adrenergic signaling, in part via the transcription factor GATA4.[18][19] An additional study showed that beta-adrenergic signaling via protein kinase A and CaM kinase induces the expression of CARP, and that CARP may have a negative effect on contractile function.[20] CARP has also been identified as a transcriptional co-activator of tumor suppressor protein p53 for stimulating gene expression in muscle; p53 was found to be an upstream effector of CARP via upregulation of the proximal ANKRD1 promoter.[21] CARP has a relatively short half-life being longer in cardiomyocytes than endothelial cells; and CARP is degraded by the 26S proteasome via a PEST degron.[22][23]

In animal models of disease and injury, CARP has been characterized to be a stress-inducible myofibrillar protein. CARP has been shown to play a role in skeletal muscle structure[24] remodeling,[25] and repair, being expressed in skeletal muscle near myotendinous junctions,[26] and in vascular smooth muscle cells, as a downstream target of TGF-beta/Smad sigmaling in response to balloon injury[27] and atherosclerotic plaques.[28] Further studies have identified a role for CARP in initiation and regulation of arteriogenesis.[29][30][31] Decreased expression of CARP in cardiac cells within the ischemic region was detected in a rat model of ischemic injury, and was thought to be linked to the induction of GADD153, an apoptosis-related gene.[32] In cardiomyocytes treated with doxorubicin, a model of anthracycline-induced cardiomyopathy, CARP mRNA and protein levels were depleted, myofilament gene transcription was attenuated and sarcomeres showed significant disarray.[33]

In a transgenic mouse model of cardiac-specific overexpression of CARP, mice exhibited normal physiology at baseline, but were protected against pathological cardiac hypertrophy induced via pressure-overload or isoproterenol, which could be attributed to the downregulation of the ERK1/2, MEK and TGFbeta-1 pathways.[34] Another study demonstrated that adenoviral overexpression of CARP in cardiomyocytes enhances cardiac hypertrophy induced by Angiotensin II or pressure-overload[35] and promotes cardiomyocyte apoptosis via p53 activation and mitochondrial dysfunction.[36] However, transgenic knockout models of either CARP alone or CARP in combination with the other muscle ankyrin repeat proteins (MARPs), ANKRD2 and ANKRD23 demonstrated a lack of cardiac phenotype; mice displayed normal cardiac function at baseline and in response to pressure overload-induced cardiac hypertrophy, suggesting that these proteins are not essential.[37]

Interactions between CARP and the sarcomeric proteins myopalladin and titin suggest that it may also be involved in the myofibrillar stretch-sensor system. Passive stretch in fetal cardiomyocytes induced differential CARP distribution at nuclei and I-band titin N2A regions.[38] In a mouse model of muscular dystrophy with myositis (mdm) caused by a small deletion in titin, CARP mRNA expression was shown to be 30-fold elevated in skeletal muscle tissue.[39]

Clinical significance

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A wide spectrum of clinical features have been associated with ANKRD1/CARP. Mutations in ANKRD1 have been associated with dilated cardiomyopathy, two of which result in altered binding with TLN1 and FHL2.[40][41] Mutations in ANKRD1 have also been associated with hypertrophic cardiomyopathy, and have shown to increase binding of CARP to Titin and MYPN.[42] Examination of the functional effects of CARP hypertrophic cardiomyopathy mutations in engineered heart tissue demonstrated that Thr123Met was a gain-of-function mutation exhibiting augmented contractile properties; whereas Pro52Ala and Ile280Val were unstable and failed to incorporate into sarcomeres, an effect that was remedied upon proteasome inhibition via epoxomicin.[43]

A missense mutation in ANKRD1 was shown to be associated with the congenital heart defect, Anomalous pulmonary venous connection.[44] CARP has been found as a sensitive and specific biomarker for the differential diagnosis of rhabdomyosarcoma.[45] ANKRD1 mRNA levels correlate with patient platinum sensitivity, thus ANKRD1 associates with platinum-based chemotherapy treatment outcome in ovarian adenocarcinoma patients.[46]

CARP and mRNA expression has been shown to be upregulated in left ventricles of heart failure patients.[47][48][49][50] Studies in patients with amyotrophic lateral sclerosis,[51] spinal muscular atrophy, and congenital myopathy,[52] also found altered expression of CARP in skeletal muscle fibers. Another study in congenital muscular dystrophy and Duchenne muscular dystrophy patients showed elevated expression of CARP.[53] CARP expression is also elevated in patients with lupus nephritis, and associates with proteinuria severity, suggesting that it may have biomarker potential.[54]

Interactions

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ANKRD1 has been shown to interact with:

References

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  1. ^ a b c GRCh38: Ensembl release 89: ENSG00000148677 – Ensembl, May 2017
  2. ^ "Human PubMed Reference:". National Center for Biotechnology Information, U.S. National Library of Medicine.
  3. ^ "Mouse PubMed Reference:". National Center for Biotechnology Information, U.S. National Library of Medicine.
  4. ^ "UniProt". beta.uniprot.org. Retrieved 7 March 2022.
  5. ^ Chu W, Burns DK, Swerlick RA, Presky DH (June 1995). "Identification and characterization of a novel cytokine-inducible nuclear protein from human endothelial cells". J. Biol. Chem. 270 (17): 10236–45. doi:10.1074/jbc.270.17.10236. PMID 7730328.
  6. ^ "Entrez Gene: ANKRD1 ankyrin repeat domain 1 (cardiac muscle)".
  7. ^ "Protein sequence of human ANKRD1 (Uniprot ID: Q15327)". Cardiac Organellar Protein Atlas Knowledgebase. Archived from the original on 23 June 2015. Retrieved 23 June 2015.
  8. ^ Torrado M, Iglesias R, Nespereira B, Centeno A, López E, Mikhailov AT (Jul 2009). "Intron retention generates ANKRD1 splice variants that are co-regulated with the main transcript in normal and failing myocardium". Gene. 440 (1–2): 28–41. doi:10.1016/j.gene.2009.03.017. hdl:2183/20009. PMID 19341785.
  9. ^ a b Witt SH, Labeit D, Granzier H, Labeit S, Witt CC (2005). "Dimerization of the cardiac ankyrin protein CARP: implications for MARP titin-based signaling". Journal of Muscle Research and Cell Motility. 26 (6–8): 401–8. doi:10.1007/s10974-005-9022-9. PMID 16450059. S2CID 22939053.
  10. ^ Laure L, Danièle N, Suel L, Marchand S, Aubert S, Bourg N, Roudaut C, Duguez S, Bartoli M, Richard I (Oct 2010). "A new pathway encompassing calpain 3 and its newly identified substrate cardiac ankyrin repeat protein is involved in the regulation of the nuclear factor-κB pathway in skeletal muscle". The FEBS Journal. 277 (20): 4322–37. doi:10.1111/j.1742-4658.2010.07820.x. PMID 20860623. S2CID 21285950.
  11. ^ Jasnic-Savovic J, Nestorovic A, Savic S, Karasek S, Vitulo N, Valle G, Faulkner G, Radojkovic D, Kojic S (Jun 2015). "Profiling of skeletal muscle Ankrd2 protein in human cardiac tissue and neonatal rat cardiomyocytes". Histochemistry and Cell Biology. 143 (6): 583–97. doi:10.1007/s00418-015-1307-5. PMID 25585647. S2CID 5174178.
  12. ^ a b Zou Y, Evans S, Chen J, Kuo HC, Harvey RP, Chien KR (Feb 1997). "CARP, a cardiac ankyrin repeat protein, is downstream in the Nkx2-5 homeobox gene pathway". Development. 124 (4): 793–804. doi:10.1242/dev.124.4.793. PMID 9043061.
  13. ^ Kuo H, Chen J, Ruiz-Lozano P, Zou Y, Nemer M, Chien KR (Oct 1999). "Control of segmental expression of the cardiac-restricted ankyrin repeat protein gene by distinct regulatory pathways in murine cardiogenesis". Development. 126 (19): 4223–34. doi:10.1242/dev.126.19.4223. PMID 10477291.
  14. ^ Takimoto E, Mizuno T, Terasaki F, Shimoyama M, Honda H, Shiojima I, Hiroi Y, Oka T, Hayashi D, Hirai H, Kudoh S, Toko H, Kawamura K, Nagai R, Yazaki Y, Komuro I (Apr 2000). "Up-regulation of natriuretic peptides in the ventricle of Csx/Nkx2-5 transgenic mice". Biochemical and Biophysical Research Communications. 270 (3): 1074–9. doi:10.1006/bbrc.2000.2561. PMID 10772952.
  15. ^ Jeyaseelan R, Poizat C, Baker RK, Abdishoo S, Isterabadi LB, Lyons GE, Kedes L (Sep 1997). "A novel cardiac-restricted target for doxorubicin. CARP, a nuclear modulator of gene expression in cardiac progenitor cells and cardiomyocytes". The Journal of Biological Chemistry. 272 (36): 22800–8. doi:10.1074/jbc.272.36.22800. PMID 9278441.
  16. ^ Aihara Y, Kurabayashi M, Tanaka T, Takeda SI, Tomaru K, Sekiguchi KI, Ohyama Y, Nagai R (Aug 2000). "Doxorubicin represses CARP gene transcription through the generation of oxidative stress in neonatal rat cardiac myocytes: possible role of serine/threonine kinase-dependent pathways". Journal of Molecular and Cellular Cardiology. 32 (8): 1401–14. doi:10.1006/jmcc.2000.1173. PMID 10900167.
  17. ^ Aihara Y, Kurabayashi M, Saito Y, Ohyama Y, Tanaka T, Takeda S, Tomaru K, Sekiguchi K, Arai M, Nakamura T, Nagai R (Jul 2000). "Cardiac ankyrin repeat protein is a novel marker of cardiac hypertrophy: role of M-CAT element within the promoter". Hypertension. 36 (1): 48–53. doi:10.1161/01.hyp.36.1.48. PMID 10904011.
  18. ^ Maeda T, Sepulveda J, Chen HH, Stewart AF (Sep 2002). "Alpha(1)-adrenergic activation of the cardiac ankyrin repeat protein gene in cardiac myocytes". Gene. 297 (1–2): 1–9. doi:10.1016/s0378-1119(02)00924-1. PMID 12384280.
  19. ^ Zhong L, Chiusa M, Cadar AG, Lin A, Samaras S, Davidson JM, Lim CC (May 2015). "Targeted inhibition of ANKRD1 disrupts sarcomeric ERK-GATA4 signal transduction and abrogates phenylephrine-induced cardiomyocyte hypertrophy". Cardiovascular Research. 106 (2): 261–71. doi:10.1093/cvr/cvv108. PMC 4481572. PMID 25770146.
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  30. ^ Shi Y, Reitmaier B, Regenbogen J, Slowey RM, Opalenik SR, Wolf E, Goppelt A, Davidson JM (Jan 2005). "CARP, a cardiac ankyrin repeat protein, is up-regulated during wound healing and induces angiogenesis in experimental granulation tissue". The American Journal of Pathology. 166 (1): 303–12. doi:10.1016/S0002-9440(10)62254-7. PMC 1602297. PMID 15632022.
  31. ^ Samaras SE, Shi Y, Davidson JM (Sep 2006). "CARP: fishing for novel mechanisms of neovascularization". The Journal of Investigative Dermatology. Symposium Proceedings. 11 (1): 124–31. doi:10.1038/sj.jidsymp.5650014. PMID 17069020.
  32. ^ Lee MJ, Kwak YK, You KR, Lee BH, Kim DG (Apr 2009). "Involvement of GADD153 and cardiac ankyrin repeat protein in cardiac ischemia-reperfusion injury". Experimental & Molecular Medicine. 41 (4): 243–52. doi:10.3858/emm.2009.41.4.027. PMC 2679233. PMID 19299913.
  33. ^ Chen B, Zhong L, Roush SF, Pentassuglia L, Peng X, Samaras S, Davidson JM, Sawyer DB, Lim CC (2012). "Disruption of a GATA4/Ankrd1 signaling axis in cardiomyocytes leads to sarcomere disarray: implications for anthracycline cardiomyopathy". PLOS ONE. 7 (4): e35743. Bibcode:2012PLoSO...735743C. doi:10.1371/journal.pone.0035743. PMC 3332030. PMID 22532871.
  34. ^ Song Y, Xu J, Li Y, Jia C, Ma X, Zhang L, Xie X, Zhang Y, Gao X, Zhang Y, Zhu D (2012). "Cardiac ankyrin repeat protein attenuates cardiac hypertrophy by inhibition of ERK1/2 and TGF-β signaling pathways". PLOS ONE. 7 (12): e50436. Bibcode:2012PLoSO...750436S. doi:10.1371/journal.pone.0050436. PMC 3515619. PMID 23227174.
  35. ^ Chen C, Shen L, Cao S, Li X, Xuan W, Zhang J, Huang X, Bin J, Xu D, Li G, Kitakaze M, Liao Y (2014). "Cytosolic CARP promotes angiotensin II- or pressure overload-induced cardiomyocyte hypertrophy through calcineurin accumulation". PLOS ONE. 9 (8): e104040. Bibcode:2014PLoSO...9j4040C. doi:10.1371/journal.pone.0104040. PMC 4121294. PMID 25089522.
  36. ^ Shen L, Chen C, Wei X, Li X, Luo G, Zhang J, Bin J, Huang X, Cao S, Li G, Liao Y (May 2015). "Overexpression of ankyrin repeat domain 1 enhances cardiomyocyte apoptosis by promoting p53 activation and mitochondrial dysfunction in rodents". Clinical Science. 128 (10): 665–78. doi:10.1042/CS20140586. PMID 25511237.
  37. ^ Bang ML, Gu Y, Dalton ND, Peterson KL, Chien KR, Chen J (2014). "The muscle ankyrin repeat proteins CARP, Ankrd2, and DARP are not essential for normal cardiac development and function at basal conditions and in response to pressure overload". PLOS ONE. 9 (4): e93638. Bibcode:2014PLoSO...993638B. doi:10.1371/journal.pone.0093638. PMC 3988038. PMID 24736439.
  38. ^ Miller MK, Bang ML, Witt CC, Labeit D, Trombitas C, Watanabe K, Granzier H, McElhinny AS, Gregorio CC, Labeit S (Nov 2003). "The muscle ankyrin repeat proteins: CARP, ankrd2/Arpp and DARP as a family of titin filament-based stress response molecules". Journal of Molecular Biology. 333 (5): 951–64. doi:10.1016/j.jmb.2003.09.012. PMID 14583192.
  39. ^ Witt CC, Ono Y, Puschmann E, McNabb M, Wu Y, Gotthardt M, Witt SH, Haak M, Labeit D, Gregorio CC, Sorimachi H, Granzier H, Labeit S (Feb 2004). "Induction and myofibrillar targeting of CARP, and suppression of the Nkx2.5 pathway in the MDM mouse with impaired titin-based signaling". Journal of Molecular Biology. 336 (1): 145–54. doi:10.1016/j.jmb.2003.12.021. PMID 14741210.
  40. ^ a b c Moulik M, Vatta M, Witt SH, Arola AM, Murphy RT, McKenna WJ, Boriek AM, Oka K, Labeit S, Bowles NE, Arimura T, Kimura A, Towbin JA (Jul 2009). "ANKRD1, the gene encoding cardiac ankyrin repeat protein, is a novel dilated cardiomyopathy gene". Journal of the American College of Cardiology. 54 (4): 325–33. doi:10.1016/j.jacc.2009.02.076. PMC 2915893. PMID 19608030.
  41. ^ Duboscq-Bidot L, Charron P, Ruppert V, Fauchier L, Richter A, Tavazzi L, Arbustini E, Wichter T, Maisch B, Komajda M, Isnard R, Villard E (Sep 2009). "Mutations in the ANKRD1 gene encoding CARP are responsible for human dilated cardiomyopathy". European Heart Journal. 30 (17): 2128–36. doi:10.1093/eurheartj/ehp225. PMID 19525294.
  42. ^ Arimura T, Bos JM, Sato A, Kubo T, Okamoto H, Nishi H, Harada H, Koga Y, Moulik M, Doi YL, Towbin JA, Ackerman MJ, Kimura A (Jul 2009). "Cardiac ankyrin repeat protein gene (ANKRD1) mutations in hypertrophic cardiomyopathy". Journal of the American College of Cardiology. 54 (4): 334–42. doi:10.1016/j.jacc.2008.12.082. PMID 19608031. S2CID 39348417.
  43. ^ Crocini C, Arimura T, Reischmann S, Eder A, Braren I, Hansen A, Eschenhagen T, Kimura A, Carrier L (May 2013). "Impact of ANKRD1 mutations associated with hypertrophic cardiomyopathy on contraction parameters of engineered heart tissue". Basic Research in Cardiology. 108 (3): 349. doi:10.1007/s00395-013-0349-x. PMID 23572067. S2CID 986109.
  44. ^ Cinquetti R, Badi I, Campione M, Bortoletto E, Chiesa G, Parolini C, Camesasca C, Russo A, Taramelli R, Acquati F (Apr 2008). "Transcriptional deregulation and a missense mutation define ANKRD1 as a candidate gene for total anomalous pulmonary venous return". Human Mutation. 29 (4): 468–74. doi:10.1002/humu.20711. PMID 18273862. S2CID 26121041.
  45. ^ Ishiguro N, Motoi T, Araki N, Ito H, Moriyama M, Yoshida H (Nov 2008). "Expression of cardiac ankyrin repeat protein, CARP, in malignant tumors: diagnostic use of CARP protein immunostaining in rhabdomyosarcoma". Human Pathology. 39 (11): 1673–9. doi:10.1016/j.humpath.2008.04.009. PMID 18656235.
  46. ^ Scurr LL, Guminski AD, Chiew YE, Balleine RL, Sharma R, Lei Y, Pryor K, Wain GV, Brand A, Byth K, Kennedy C, Rizos H, Harnett PR, deFazio A (Nov 2008). "Ankyrin repeat domain 1, ANKRD1, a novel determinant of cisplatin sensitivity expressed in ovarian cancer". Clinical Cancer Research. 14 (21): 6924–32. doi:10.1158/1078-0432.CCR-07-5189. PMID 18980987.
  47. ^ Bogomolovas J, Brohm K, Čelutkienė J, Balčiūnaitė G, Bironaitė D, Bukelskienė V, Daunoravičus D, Witt CC, Fielitz J, Grabauskienė V, Labeit S (2015). "Induction of ankrd1 in dilated cardiomyopathy correlates with the heart failure progression". BioMed Research International. 2015: 273936. doi:10.1155/2015/273936. PMC 4415747. PMID 25961010.
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  51. ^ Nakamura K, Nakada C, Takeuchi K, Osaki M, Shomori K, Kato S, Ohama E, Sato K, Fukayama M, Mori S, Ito H, Moriyama M (Apr 2003). "Altered expression of cardiac ankyrin repeat protein and its homologue, ankyrin repeat protein with PEST and proline-rich region, in atrophic muscles in amyotrophic lateral sclerosis". Pathobiology. 70 (4): 197–203. doi:10.1159/000069329. PMID 12679596. S2CID 37199318.
  52. ^ Nakada C, Oka A, Nonaka I, Sato K, Mori S, Ito H, Moriyama M (Oct 2003). "Cardiac ankyrin repeat protein is preferentially induced in atrophic myofibers of congenital myopathy and spinal muscular atrophy". Pathology International. 53 (10): 653–8. doi:10.1046/j.1440-1827.2003.01541.x. PMID 14516314. S2CID 23238020.
  53. ^ Nakada C, Tsukamoto Y, Oka A, Nonaka I, Takeda S, Sato K, Mori S, Ito H, Moriyama M (May 2003). "Cardiac-restricted ankyrin-repeated protein is differentially induced in duchenne and congenital muscular dystrophy". Laboratory Investigation. 83 (5): 711–9. doi:10.1097/01.lab.0000067484.35298.1a. PMID 12746480.
  54. ^ Matsuura K, Uesugi N, Hijiya N, Uchida T, Moriyama M (Mar 2007). "Upregulated expression of cardiac ankyrin-repeated protein in renal podocytes is associated with proteinuria severity in lupus nephritis". Human Pathology. 38 (3): 410–9. doi:10.1016/j.humpath.2006.09.006. PMID 17239933.
  55. ^ a b Miller MK, Bang ML, Witt CC, Labeit D, Trombitas C, Watanabe K, Granzier H, McElhinny AS, Gregorio CC, Labeit S (November 2003). "The muscle ankyrin repeat proteins: CARP, ankrd2/Arpp and DARP as a family of titin filament-based stress response molecules". J. Mol. Biol. 333 (5): 951–64. doi:10.1016/j.jmb.2003.09.012. PMID 14583192.
  56. ^ Bang ML, Mudry RE, McElhinny AS, Trombitás K, Geach AJ, Yamasaki R, Sorimachi H, Granzier H, Gregorio CC, Labeit S (April 2001). "Myopalladin, a novel 145-kilodalton sarcomeric protein with multiple roles in Z-disc and I-band protein assemblies". J. Cell Biol. 153 (2): 413–27. doi:10.1083/jcb.153.2.413. PMC 2169455. PMID 11309420.
  57. ^ Torrado M, Nespereira B, López E, Centeno A, Castro-Beiras A, Mikhailov AT (Feb 2005). "ANKRD1 specifically binds CASQ2 in heart extracts and both proteins are co-enriched in piglet cardiac Purkinje cells". Journal of Molecular and Cellular Cardiology. 38 (2): 353–65. doi:10.1016/j.yjmcc.2004.11.034. PMID 15698842.
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Further reading

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