Creatine Kinase-MM/Proto-oncogene Tyrosine-Protein Kinase Receptor as a Sensitive Indicator for Duchenne Muscular Dystrophy Carriers.
Biomarker
Creatine kinase-MM
DMD carriers
RET
Journal
Molecular neurobiology
ISSN: 1559-1182
Titre abrégé: Mol Neurobiol
Pays: United States
ID NLM: 8900963
Informations de publication
Date de publication:
20 May 2024
20 May 2024
Historique:
received:
01
12
2023
accepted:
13
05
2024
medline:
20
5
2024
pubmed:
20
5
2024
entrez:
20
5
2024
Statut:
aheadofprint
Résumé
Duchenne muscular dystrophy (DMD), a lethal X-linked recessive genetic disease, is characterized by progressive muscle wasting which will lead to premature death by cardiorespiratory complications in their late twenties. And 2.5-19% DMD carriers that also suffer from skeletal muscle damage or dilated cardiomyopathy when diagnosed as soon as possible is meaningful for prenatal diagnosis and advance warning for self-health. The current DMD carrier screening mainly relies on detecting serum creatine kinase activity, covering only 50-70% DMD carriers which will cause many false negatives and require the discovery of highly effective biomarker and simple detection procedure for DMD carriers. In this article, we have compiled a comprehensive summary of all documented biomarkers associated with DMD and categorized them based on their expression patterns. We specifically pinpointed novel DMD biomarkers, previously unreported in DMD carriers, and conducted further investigations to explore their potential. Compared to creatine kinase activity alone in DMD carriers, creatine kinase-MM can improve the specificity from 73 to 81%. And our investigation revealed another promising protein: proto-oncogene tyrosine-protein kinase receptor (RET). When combined with creatine kinase-MM (creatine kinase-MM/RET ratio), it significantly enhances the specificity (from 81 to 83%) and sensitivity (from 71.4 to 93%) of detecting DMD carriers in serum. Moreover, we successfully devised an efficient method for extracting RET from dried blood spots. This breakthrough allowed us to detect both creatine kinase-MM and RET using dried blood spots without compromising the detection rate.
Identifiants
pubmed: 38767836
doi: 10.1007/s12035-024-04235-z
pii: 10.1007/s12035-024-04235-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : National Natural Science Foundation of China
ID : 82202065
Organisme : Nanjing Health Science and Technology Development Special Fund
ID : YKK21159
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Muntoni F, Torelli S, Ferlini A (2003) Dystrophin and mutations: one gene, several proteins, multiple phenotypes. Lancet Neurol 2(12):731–740. https://doi.org/10.1016/s1474-4422(03)00585-4
doi: 10.1016/s1474-4422(03)00585-4
pubmed: 14636778
DMD Care Considerations Working Group, Birnkrant DJ, Bushby K, Bann CM, Apkon SD, Blackwell A, Brumbaugh D, Case LE, Clemens PR, Hadjiyannakis S, Pandya S, Street N, Tomezsko J, Wagner KR, Ward LM, Weber DR (2018) Diagnosis and management of Duchenne muscular dystrophy, part 1: diagnosis, and neuromuscular, rehabilitation, endocrine, and gastrointestinal and nutritional management. Lancet Neurol 17(3):251–267. https://doi.org/10.1016/S1474-4422(18)30024-3
doi: 10.1016/S1474-4422(18)30024-3
Grounds MD, Terrill JR, Al-Mshhdani BA, Duong MN, Radley-Crabb HG, Arthur PG (2020) Biomarkers for Duchenne muscular dystrophy: myonecrosis, inflammation and oxidative stress. Dis Model Mech 13(2):dmm043638. https://doi.org/10.1242/dmm.043638
doi: 10.1242/dmm.043638
pubmed: 32224496
pmcid: 7063669
Mendell JR, Shilling C, Leslie ND, Flanigan KM, Al-Dahhak R, Gastier-Foster J, Kneile K, Dunn DM, Duval B, Aoyagi A, Hamil C, Mahmoud M, Roush K, Bird L, Rankin C, Lilly H, Street N, Chandrasekar R, Weiss RB (2012) Evidence-based path to newborn screening for Duchenne muscular dystrophy. Ann Neurol 71(3):304–313. https://doi.org/10.1002/ana.23528
doi: 10.1002/ana.23528
pubmed: 22451200
Moat SJ, Korpimaki T, Furu P, Hakala H, Polari H, Merio L, Makinen P, Weeks I (2017) Characterization of a blood spot creatine kinase skeletal muscle isoform immunoassay for high-throughput newborn screening of Duchenne muscular dystrophy. Clin Chem 63(4):908–914. https://doi.org/10.1373/clinchem.2016.268425
doi: 10.1373/clinchem.2016.268425
pubmed: 28209627
Falzarano MS, Scotton C, Passarelli C, Ferlini A (2015) Duchenne muscular dystrophy: from diagnosis to therapy. Molecules 20(10):18168–18184. https://doi.org/10.3390/molecules201018168
doi: 10.3390/molecules201018168
pubmed: 26457695
pmcid: 6332113
Ke Q, Zhao ZY, Griggs R, Wiley V, Connolly A, Kwon J, Qi M, Sheehan D, Ciafaloni E, Howell RR, Furu P, Sazani P, Narayana A, Gatheridge M (2017) Newborn screening for Duchenne muscular dystrophy in China: follow-up diagnosis and subsequent treatment. World J Pediatr 13(3):197–201. https://doi.org/10.1007/s12519-017-0036-3
doi: 10.1007/s12519-017-0036-3
pubmed: 28466241
Mendell JR, Goemans N, Lowes LP, Alfano LN, Berry K, Shao J, Kaye EM, Mercuri E (2016) Eteplirsen Study Group Telethon Foundation DMD Italian Network. Longitudinal effect of eteplirsen versus historical control on ambulation in Duchenne muscular dystrophy. Ann Neurol 79(2):257–271. https://doi.org/10.1002/ana.24555
doi: 10.1002/ana.24555
pubmed: 26573217
pmcid: 5064753
McCaffrey T, Guglieri M, Murphy AP, Bushby K, Johnson A, Bourke JP (2017) Cardiac involvement in female carriers of Duchenne or Becker muscular dystrophy. Muscle Nerve 55(6):810–818. https://doi.org/10.1002/mus.25445
doi: 10.1002/mus.25445
pubmed: 27761893
Ishizaki M, Kobayashi M, Adachi K, Matsumura T, Kimura E (2018) Female dystrophinopathy: review of current literature. Neuromuscul Disord 28(7):572–581. https://doi.org/10.1016/j.nmd.2018.04.005
doi: 10.1016/j.nmd.2018.04.005
pubmed: 29801751
Politano L, Nigro V, Nigro G, Petretta VR, Passamano L, Papparella S, Di Somma S, Comi LI (1996) Development of cardiomyopathy in female carriers of Duchenne and Becker muscular dystrophies. JAMA 275(17):1335–1338
doi: 10.1001/jama.1996.03530410049032
pubmed: 8614119
Schade van Westrum SM, Hoogerwaard EM, Dekker L, Standaar TS, Bakker E, Ippel PF, Oosterwijk JC, Majoor-Krakauer DF, van Essen AJ, Leschot NJ, Wilde AA, de Haan RJ, de Visser M, van der Kooi AJ (2011) Cardiac abnormalities in a follow-up study on carriers of Duchenne and Becker muscular dystrophy. Neurology 77(1):62–66. https://doi.org/10.1212/WNL.0b013e318221ad14
doi: 10.1212/WNL.0b013e318221ad14
pubmed: 21700587
Ayoglu B, Chaouch A, Lochmuller H, Politano L, Bertini E, Spitali P, Hiller M, Niks EH, Gualandi F, Ponten F, Bushby K, Aartsma-Rus A, Schwartz E, Le Priol Y, Straub V, Uhlen M, Cirak S, t Hoen PA, Muntoni F, Ferlini A, Schwenk JM, Nilsson P, Al-Khalili Szigyarto C (2014) Affinity proteomics within rare diseases: a BIO-NMD study for blood biomarkers of muscular dystrophies. EMBO Mol Med 6(7): 918–936. https://doi.org/10.15252/emmm.201303724 .
Li X, Li Y, Zhao L, Zhang D, Yao X, Zhang H, Wang YC, Wang XY, Xia H, Yan J, Ying H (2014) Circulating muscle-specific miRNAs in Duchenne muscular dystrophy patients. Mol Ther Nucleic Acids 3(7):e177. https://doi.org/10.1038/mtna.2014.29
doi: 10.1038/mtna.2014.29
pubmed: 25050825
pmcid: 4121518
Srivastava NK, Annarao S, Sinha N (2016) Metabolic status of patients with muscular dystrophy in early phase of the disease: in vitro, high resolution NMR spectroscopy based metabolomics analysis of serum. Life Sci 151:122–129. https://doi.org/10.1016/j.lfs.2016.01.032
doi: 10.1016/j.lfs.2016.01.032
pubmed: 26930370
Gatheridge MA, Kwon JM, Mendell JM, Scheuerbrandt G, Moat SJ, Eyskens F, Rockman-Greenberg C, Drousiotou A, Griggs RC (2016) Identifying non–Duchenne muscular dystrophy–positive and false negative results in prior Duchenne muscular dystrophy newborn screening programs. JAMA Neurol 73(1):111–116. https://doi.org/10.1001/jamaneurol.2015.3537
doi: 10.1001/jamaneurol.2015.3537
pubmed: 26594870
Mokuno K, Riku S, Sugimura K, Takahashi A, Kato K, Osugi S (1987) Serum creatine kinase isoenzymes in Duchenne muscular dystrophy determined by sensitive enzyme immunoassay methods. Muscle Nerve 10(5):459–463. https://doi.org/10.1002/mus.880100513
doi: 10.1002/mus.880100513
pubmed: 3302699
Timonen A, Lloyd-Puryear M, Hougaard DM, Merio L, Makinen P, Laitala V, Polonen T, Skogstrand K, Kennedy A, Airenne S, Polari H, Korpimaki TD (2019) Duchenne muscular dystrophy newborn screening: evaluation of a new GSP((R)) neonatal creatine kinase-MM kit in a US and Danish population. Int J Neonatal Screen 5(3):27. https://doi.org/10.3390/ijns5030027
doi: 10.3390/ijns5030027
pubmed: 33072986
pmcid: 7510235
Migliore BA, Zhou L, Duparc M, Robles VR, Rehder CW, Peay HL, Kucera KS (2022) Evaluation of the GSP creatine kinase-MM assay and assessment of CK-MM stability in newborn, patient, and contrived dried blood spots for newborn screening for Duchenne muscular dystrophy. Int J Neonatal Screen 8(1):12. https://doi.org/10.3390/ijns8010012
doi: 10.3390/ijns8010012
pubmed: 35225934
pmcid: 8883886
Brandsema JF, Darras BT (2015) Dystrophinopathies. Semin Neurol 35(4):369–384. https://doi.org/10.1055/s-0035-1558982
doi: 10.1055/s-0035-1558982
pubmed: 26502761
Santoro M, Melillo RM, Carlomagno F, Vecchio G, Fusco A (2004) Minireview: RET: normal and abnormal functions. Endocrinology 145(12):5448–5451. https://doi.org/10.1210/en.2004-0922
doi: 10.1210/en.2004-0922
pubmed: 15331579
Menshykau D, Michos O, Lang C, Conrad L, McMahon AP, Iber D (2019) Image-based modeling of kidney branching morphogenesis reveals GDNF-RET based Turing-type mechanism and pattern-modulating WNT11 feedback. Nat Commun 10(1):239. https://doi.org/10.1038/s41467-018-08212-8
doi: 10.1038/s41467-018-08212-8
pubmed: 30651543
pmcid: 6484223
Rhymes ER, Tosolini AP, Fellows AD, Mahy W, McDonald NQ, Schiavo G (2022) Bimodal regulation of axonal transport by the GDNF-RET signalling axis in healthy and diseased motor neurons. Cell Death Dis 13(7):584. https://doi.org/10.1038/s41419-022-05031-0
doi: 10.1038/s41419-022-05031-0
pubmed: 35798698
pmcid: 9263112
La Pietra V, Sartini S, Botta L, Antonelli A, Ferrari SM, Fallahi P, Moriconi A, Coviello V, Quattrini L, Ke YY, Hsing-Pang H, Da Settimo F, Novellino E, La Motta C, Marinelli L (2018) Challenging clinically unresponsive medullary thyroid cancer: discovery and pharmacological activity of novel RET inhibitors. Eur J Med Chem 150:491–505. https://doi.org/10.1016/j.ejmech.2018.02.080
doi: 10.1016/j.ejmech.2018.02.080
pubmed: 29549836
Yang C, Hutto D, Sah DW (2006) Distribution of GDNF family receptor alpha3 and RET in rat and human non-neural tissues. J Mol Histol 37(1–2):69–77. https://doi.org/10.1007/s10735-006-9035-8
doi: 10.1007/s10735-006-9035-8
pubmed: 16773224
Moyle LA, Blanc E, Jaka O, Prueller J, Banerji CR, Tedesco FS, Harridge SD, Knight RD, Zammit PS (2016) Ret function in muscle stem cells points to tyrosine kinase inhibitor therapy for facioscapulohumeral muscular dystrophy. Elife 5:e11405. https://doi.org/10.7554/eLife.11405
doi: 10.7554/eLife.11405
pubmed: 27841748
pmcid: 5108591
Klein R, Dardik R, Avishai E, Lalezari S, Barg AA, Levy-Mendelovich S, Budnik I, Barel O, Khavkin Y, Kenet G, Livnat T (2021) Molecular mechanisms of skewed X-chromosome inactivation in female hemophilia patients—lessons from wide genome analyses. Int J Mol Sci 22(16):9074. https://doi.org/10.3390/ijms22169074
doi: 10.3390/ijms22169074
Hathout Y, Brody E, Clemens PR, Cripe L, DeLisle RK, Furlong P, Gordish-Dressman H, Hache L, Henricson E, Hoffman EP, Kobayashi YM, Lorts A, Mah JK, McDonald C, Mehler B, Nelson S, Nikrad M, Singer B, Steele F, Sterling D, Sweeney HL, Williams S, Gold L (2016) Large-scale serum protein biomarker discovery in Duchenne muscular dystrophy. Proc Natl Acad Sci USA 112(23):7153–7158. https://doi.org/10.1073/pnas.1507719112
doi: 10.1073/pnas.1507719112
Shiba N, Yang X, Sato M, Kadota S, Suzuki Y, Agata M, Nagamine K, Izumi M, Honda Y, Koganehira T, Kobayashi H, Ichimura H, Chuma S, Nakai J, Tohyama S, Fukuda K, Miyazaki D, Nakamura A, Shiba Y (2023) Efficacy of exon-skipping therapy for DMD cardiomyopathy with mutations in actin binding domain 1. Mol Ther Nucleic Acids 34:102060. https://doi.org/10.1016/j.omtn.2023.102060
doi: 10.1016/j.omtn.2023.102060
pubmed: 38028197
pmcid: 10654596
Patterson G, Conner H, Groneman M, Blavo C, Parmar MS (2023) Duchenne muscular dystrophy: current treatment and emerging exon skipping and gene therapy approach. Eur J Pharmacol 947:175675. https://doi.org/10.1016/j.ejphar.2023.175675
doi: 10.1016/j.ejphar.2023.175675
pubmed: 36963652
Saoudi A, Fergus C, Gileadi T, Montanaro F, Morgan JE, Kelly VP, Tensorer T, Garcia L, Vaillend C, Muntoni F, Goyenvalle A (2023) Investigating the impact of delivery routes for exon skipping therapies in the CNS of DMD mouse models. Cells 12(6):908. https://doi.org/10.3390/cells12060908
doi: 10.3390/cells12060908
pubmed: 36980249
pmcid: 10047648
Sheikh O, Yokota T (2022) Pharmacology and toxicology of eteplirsen and SRP-5051 for DMD exon 51 skipping: an update. Arch Toxicol 96(1):1–9. https://doi.org/10.1007/s00204-021-03184-z
doi: 10.1007/s00204-021-03184-z
pubmed: 34797383
Lo KR, Hurst SM, Atkinson KR, Vandenbogaerde T, Beaven CM, Ingram JR (2010) Development and validation of a sensitive immunoassay for the skeletal muscle isoform of creatine kinase. J Sci Med Sport 13(1):117–119. https://doi.org/10.1016/j.jsams.2008.08.004
doi: 10.1016/j.jsams.2008.08.004
pubmed: 18976957
Subbiah V, Yang D, Velcheti V, Drilon A, Meric-Bernstam F (2020) State-of-the-art strategies for targeting RET-dependent cancers. J Clin Oncol 38(11): 1209–1221. https://doi.org/10.1200/JCO.19.02551 .
Li AY, McCusker MG, Russo A, Scilla KA, Gittens A, Arensmeyer K, Mehra R, Adamo V, Rolfo C (2019) RET fusions in solid tumors. Cancer Treat Rev 81:101911. https://doi.org/10.1016/j.ctrv.2019.101911
doi: 10.1016/j.ctrv.2019.101911
pubmed: 31715421
Li L, Rozo M, Yue S, Zheng X, Tan J, Lepper C, Fan CM (2019) Muscle stem cell renewal suppressed by Gas1 can be reversed by GDNF in mice. Nat Metab 1(10):985–995. https://doi.org/10.1038/s42255-019-0110-3
doi: 10.1038/s42255-019-0110-3
pubmed: 32021964
pmcid: 7000153
Suriben R, Chen M, Higbee J, Oeffinger J, Ventura R, Li B, Mondal K, Gao Z, Ayupova D, Taskar P, Li D, Starck SR, Chen HH, McEntee M, Katewa SD, Phung V, Wang M, Kekatpure A, Lakshminarasimhan D, White A, Olland A, Haldankar R, Solloway MJ, Hsu JY, Wang Y, Tang J, Lindhout DA, Allan BB (2020) Antibody-mediated inhibition of GDF15–GFRAL activity reverses cancer cachexia in mice. Nat Med 26(8):1264–1270. https://doi.org/10.1038/s41591-020-0945-x
doi: 10.1038/s41591-020-0945-x
pubmed: 32661391
Klein P, Muller-Rischart AK, Motori E, Schonbauer C, Schnorrer F, Winklhofer KF (2014) Ret rescues mitochondrial morphology and muscle degeneration of Drosophila Pink1 mutants. EMBO J 33(4):341–355. https://doi.org/10.1002/embj.201284290
doi: 10.1002/embj.201284290
pubmed: 24473149
pmcid: 3983680
Christensen K, Kristiansen M, Hagen-Larsen H, Skytthe A, Bathum L, Jeune B, Andersen-Ranberg K, Vaupel JW, Orstavik KH (2000) X-linked genetic factors regulate hematopoietic stem-cell kinetics in females. Blood 95(7):2449–2451. https://doi.org/10.1182/blood.V95.7.2449
doi: 10.1182/blood.V95.7.2449
pubmed: 10733522
Roberts AL, Morea A, Amar A, Zito A, El-Sayed Moustafa JS, Tomlinson M, Bowyer RCE, Zhang X, Christiansen C, Costeira R, Steves CJ, Mangino M, Bell JT, Wong CCY, Vyse TJ (2022) Age acquired skewed X chromosome inactivation is associated with adverse health outcomes in humans. Elife 11:e78263. https://doi.org/10.7554/eLife.78263
doi: 10.7554/eLife.78263
pubmed: 36412098
pmcid: 9681199
Bushby K, Muntoni F, Bourke JP (2003) 107th ENMC international workshop: the management of cardiac involvement in muscular dystrophy and myotonic dystrophy. 7th-9th June 2002, Naarden, the Netherlands. Neuromuscul Disord 13(2):166–72. https://doi.org/10.1016/s0960-8966(02)00213-4
doi: 10.1016/s0960-8966(02)00213-4
pubmed: 12565916
American Academy of Pediatrics Section on Cardiology and Cardiac Surgery (2005) Cardiovascular health supervision for individuals affected by Duchenne or Becker muscular dystrophy. Pediatrics 116(6):1569–1573. https://doi.org/10.1542/peds.2005-2448
doi: 10.1542/peds.2005-2448
Small KS, He WB, Du J, Xie PY, Zhou S, Zhang YX, Lu GX, Lin G, Li W, Tan YQ (2019) X-chromosome inactivation pattern of amniocytes predicts the risk of dystrophinopathy in fetal carriers of DMD mutations. Prenat Diagn 39(8):603–608. https://doi.org/10.1002/pd.5473
doi: 10.1002/pd.5473