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Centro de Investigaciones Regionales Dr. Hideyo Noguchi, Universidad Autónoma de Yucatán

2023, Número 2

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Rev Biomed 2023; 34 (2)


Papel de Par-4 en tumores de cáncer de mama en etapas tardías y recurrentes

Zapata-Benavides P, Arellano-Rodríguez NC, Rodríguez-Padilla MC

Idioma: Español
Referencias bibliográficas: 73
Paginas: 224-234
Archivo PDF: 383.43 Kb.


RESUMEN

Las muertes en los pacientes con cáncer de mama ocurren principalmente por la recurrencia y metástasis y no por el tumor primario. La agresividad del tumor se asocia al estatus hormonal; tumores receptores de estrógeno o triple negativos son neoplasias de mal pronóstico que tienen la capacidad de inducir metástasis o recurrencia. La baja expresión de la proteína Par-4 se asocia a un mal pronóstico, por esa razón analizamos la participación de la proteína de respuesta de apoptosis protática (Par-4) en la recurrencia tumoral. Se realizó una búsqueda de artículos relacionados con cáncer de mama, recurrencia y Par-4 en el PubMed y en otros bancos de datos, con la finalidad de comprender la relación de Par-4 como gen supresor de tumor con el proceso carcinogénico y recurrencia de cáncer de mama. La baja expresión de Par-4 está asociado con tumores receptor de estrógeno negativo o con alto grado de transformación. La expresión de Par-4 disminuye o es bloqueada en las células remantes después de la quimioterapia y durante el proceso de la transición epitelian a mesenquimal (EMT, por sus siglas en inglés) en la recurrencia del tumor, observándose que Par-4 es necesaria y esencial para la recurrencia del cáncer de mama. El entendimiento de la biología del Par-4 en el cáncer de mama abre la posibilidad de ser empleado como una estrategia terapéutica para que coadyuve con la eliminación de los tumores resistentes o recurrentes de cáncer de mama.


REFERENCIAS (EN ESTE ARTÍCULO)

  1. Giaquinto AN, Miller KD, Tossas KY, Winn RA,Jemal A, Siegel RL. Cancer statistics for AfricanAmerican/Black people 2022. CA Cancer J Clin. 2022Feb;72(3):202–29. http://dx.doi.org/10.3322/caac.21718

  2. Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancerstatistics, 2022. CA Cancer J Clin. 2022 Jan;72(1):7–33.http://dx.doi.org/10.3322/caac.21708

  3. Alcaide-Lucena M, Rodríguez-González CJ, de Reyes-Lartategui S, Gallart-Aragón R, Sánchez-Barrón MT,García-Rubio J, et al. Molecular classification of breastcancer. Treatment and prognosis implications. Cir Andal.2021 May;32(2):155–9. doi: 10.37351/2021322.9

  4. Marchiò C, Annaratone L, Marques A, Casorzo L, BerrinoE, Sapino A. Evolving concepts in HER2 evaluation inbreast cancer: Heterogeneity, HER2-low carcinomasand beyond. Semin Cancer Biol. 2021 Jul; 72: 123–135.https://doi.org/10.1016/j.semcancer.2020.02.016

  5. Sakach E, O´Regan R, Meisel J, Li X. MolecularClassification of Triple Negative Breast Cancer and theEmergence of Targeted Therapies. Clin Breast Cancer.2021 Sep;21(6): 509–520. https://doi.org/10.1016/j.clbc.2021.09.003

  6. DeSantis CE, Ma J, Goding-Sauer A, Newman LA,Jemal A. Breast cancer statistics, 2017, racial disparityin mortality by state: Breast Cancer Statistics, 2017. CACancer J Clin. 2017 Oct;67(6):439–48. http://dx.doi.org/10.3322/caac.21412

  7. Scully OJ, Bay BH, Yip G, Yu Y. Breast cancer metastasis.Cancer genomics & proteomics. 2012 Oct; 9(5): 311-320. https://cgp.iiarjournals.org/content/9/5/311.long

  8. He XM, Zou DH. The association of young age withlocal recurrence in women with early-stage breast cancerafter breast-conserving therapy: a meta-analysis. SciRep. 2017 Sep;7(1):11058. http://dx.doi.org/10.1038/s41598-017-10729-9

  9. Fragomeni SM, Sciallis A, Jeruss JS. Molecular subtypesand local-regional control of breast cancer. Surg OncolClin N Am. 2018 Jan; 27(1): 95-120. doi: 10.1016/j.soc.2017.08.005

  10. Jin L, Han B, Siegel E, Cui Y, Giuliano A, Cui X.Breast cancer lung metastasis: Molecular biology andtherapeutic implications. Cancer Biol. Ther. 2018 Mar;19(10): 858-868. doi: 10.1080/15384047.2018.1456599

  11. Belkacemi Y, Hanna NE, Besnard C, Majdoul S,Gligorov J. Local and regional breast cancer recurrences:Salvage therapy options in the new era of molecularsubtypes. Front Oncol. 2018 Apr; 8: 112. doi: 10.3389/fonc.2018.00112

  12. O’Reilly D, Al Sendi M, Kelly CM. Overview of recentadvances in metastatic triple negative breast cancer.World J Clin Oncol. 2021 Mar; 12(3): 164. doi: 10.5306/wjco.v12.i3.164

  13. Lee K, Kruper L, Dieli-Conwright CM, Mortimer JE.The impact of obesity on breast cancer diagnosis andtreatment. Curr Oncol Rep. 2019 Mar;21(5):41. http://dx.doi.org/10.1007/s11912-019-0787-1

  14. Ecker BL, Lee JY, Sterner CJ, Solomon AC, PantDK, Shen, F, et al. Impact of obesity on breast cancerrecurrence and minimal residual disease. Breast CancerRes. 2019 Mar; 21(1): 1-16. doi: 10.1186/s13058-018-1087-7

  15. Kothari C, Diorio C, Durocher F. The Importance ofBreast Adipose Tissue in Breast Cancer. Int J MolSci. 2020 Aug; 21(16): 5760. https://doi.org/10.3390/ijms21165760

  16. Jiralerspong S, Goodwin PJ. Obesity and Breast CancerPrognosis: Evidence, Challenges, and Opportunities. JClin Oncol: official journal of the American Society ofClinical Oncology. 2016 Dec; 34(35): 4203–4216. doi:10.1200/JCO.2016.68.4480

  17. Araujo N, Sledziona J, Noothi SK, Burikhanov R,Hebbar N, Ganguly S, et al. Tumor Suppressor Par-4Regulates Complement Factor C3 and Obesity. FrontOncol. 2022 Mar; 12: 860446. https://doi.org/10.3389/fonc.2022.860446

  18. Mabe NW, Fox DB, Lupo R, Decker AE, Phelps SN,Thompson JW, et al. Epigenetic silencing of tumorsuppressor Par-4 promotes chemoresistance in recurrentbreast cancer. J Clin Invest. 2018 Aug;128(10):4413–28.http://dx.doi.org/10.1172/JCI99481

  19. Sells SF, Wood DP Jr, Joshi-Barve SS, MuthukumarS, Jacob RJ, Crist SA, et al. Commonality of the geneprograms induced by effectors of apoptosis in androgendependentand -independent prostate cells. Cell GrowthDiffer. 1994 Apr;5(4):457–66. https://pubmed.ncbi.nlm.nih.gov/8043520/

  20. Cheratta AR, Thayyullathil F, Pallichankandy S,Subburayan K, Alakkal A, Galadari S. Prostate apoptosisresponse-4 and tumor suppression: it’s not just aboutapoptosis anymore. Cell Death Dis. 2021 Jan;12(1):47.http://dx.doi.org/10.1038/s41419-020-03292-1

  21. Tiruttani Subhramanyam UK, Kubicek J, Eidhoff UB,Labahn J. Structural basis for the regulatory interactionsof proapoptotic Par-4. Cell Death Diffe. 2017 Jun; 24(9):1540-1547. https://doi.org/10.1038/cdd.2017.76

  22. Ghosalkar J, Sonawane V, Pisal T, Achrekar S, PujariR, Chugh A. Prostate Apoptosis Response-4 (Par-4):A Novel Target in Pyronaridine-Induced Apoptosis inGlioblastoma (GBM) Cells. Cancers. 2022 Jun; 14(13):3198. https://doi.org/10.3390/cancers14133198

  23. Zhang J, Sun A, Dong Y, Wei D. Recombinant productionand characterization of SAC, the core domain of par-4,by SUMO fusion system. Appl Biochem Biotechnol.2018 Oct;184(4):1155–67. http://dx.doi.org/10.1007/s12010-017-2599-9

  24. Santiago SA, Pablo ZB, Edgar MG, Karina CA, MarielaAR, Cristina RP. Truncated WT1 Protein IsoformExpression Is Increased in MCF-7 Cells with Long-Term Estrogen Depletion. Int J Breast Cancer. 2021Nov; 2021:6282514. doi: 10.1155/2021/6282514.

  25. Cheema SK, Mishra SK, Rangnekar VM, Tari A M,Kumar R, Lopez-Berestein G. Par-4 transcriptionallyregulates Bcl-2 through a WT1-binding site on the bcl-2 promoter. J Biol Chem. 2003 May;278(22): 19995–20005. https://doi.org/10.1074/jbc.M205865200

  26. Satherley LK, Sun PH, Ji KE, Mason M, Hargest R,Jiang WG, et al. Prostate Apoptosis Response-4 (PAR4)Suppresses Growth and Invasion of Breast Cancer Cellsand Is Positively Associated with Patient Survival.Anticancer Res. 2016 Mar; 36(3): 1227–1235. https://ar.iiarjournals.org/content/36/3/1227

  27. de Bessa Garcia SA, Pavanelli AC, Cruz E Melo N, NagaiMA. Prostate apoptosis response 4 (PAR4) expressionmodulates WNT signaling pathways in MCF7 breastcancer cells: A possible mechanism underlying PAR4-mediated docetaxel chemosensitivity. Int J Mol Med.2017 Feb; 39(4): 809–818. https://doi.org/10.3892/ijmm.2017.2900

  28. Burikhanov R, Zhao Y, Goswami A, Qiu S, SchwarzeSR, Rangnekar VM. The tumor suppressor Par-4activates an extrinsic pathway for apoptosis. Cell.2009 Jul;138(2):377–88. http://dx.doi.org/10.1016/j.cell.2009.05.022

  29. Shrestha-Bhattarai T, Rangnekar VM. Cancer-selectiveapoptotic effects of extracellular and intracellular Par-4. Oncogene. 2010 May;29(27):3873–80. http://dx.doi.org/10.1038/onc.2010.141

  30. Guo H, Treude F, Krämer OH, Lüscher B, Hartkamp J.PAR-4 overcomes chemo-resistance in breast cancer cellsby antagonizing cIAP1. Sci Rep. 2019 Jun;9(1):8755.http://dx.doi.org/10.1038/s41598-019-45209-9

  31. Yao X, Liu H, Zhang X, Zhang L, Li X, Wang C,et al. Cell surface GRP78 accelerated breast cancercell proliferation and migration by activating STAT3.PLoS One. 2015 May;10(5):e0125634. http://dx.doi.org/10.1371/journal.pone.0125634

  32. Cohen M, Ribaux P, Epiney M, Irion O. Role of prostateapoptosis response 4 in translocation of GRP78 from theendoplasmic reticulum to the cell surface of trophoblasticcells. PLoS One. 2013 Nov;8(11):e80231. http://dx.doi.org/10.1371/journal.pone.0080231

  33. Burikhanov R, Shrestha-Bhattarai T, Hebbar N, Qiu S,Zhao Y, Zambetti GP, et al. Paracrine apoptotic effectof p53 mediated by tumor suppressor par-4. Cell Rep.2014 Jan;6(2):271–7. http://dx.doi.org/10.1016/j.celrep.2013.12.020

  34. Nagai MA, Gerhard R, Salaorni S, Fregnani JHTG,Nonogaki S, Netto MM, et al. Down-regulation of thecandidate tumor suppressor gene PAR-4 is associatedwith poor prognosis in breast cancer. Int J Oncol. 2010Jul;37(1):41–9. http://dx.doi.org/10.3892/ijo_00000651

  35. Ahmed MM, Sheldon D, Fruitwala MA, VenkatasubbaraoK, Lee EY, Gupta S, et al. Downregulation of PAR-4, apro-apoptotic gene, in pancreatic tumors harboring K-rasmutation. Int J Cancer. 2008 Jan;122(1):63–70. http://dx.doi.org/10.1002/ijc.23019

  36. Cook J, Krishnan S, Ananth S, Sells SF, Shi Y, WaltherMM, et al. Decreased expression of the pro-apoptoticprotein Par-4 in renal cell carcinoma. Oncogene.1999 Feb;18(5):1205–8. http://dx.doi.org/10.1038/sj.onc.1202416

  37. Brasseur K, Gévry N, Asselin E. Chemoresistance andtargeted therapies in ovarian and endometrial cancers.Oncotarget. 2017 Dec; 8(3): 4008–4042. https://doi.org/10.18632/oncotarget.14021

  38. Alvarez JV, Pan T-C, Ruth J, Feng Y, Zhou A, PantD, et al. Par-4 downregulation promotes breast cancerrecurrence by preventing multinucleation followingtargeted therapy. Cancer Cell. 2013 Jun;24(1):30–44.http://dx.doi.org/10.1016/j.ccr.2013.05.007

  39. Méndez-López LF, Zapata-Benavides P, Zavala-PompaA, Aguado-Barrera ME, Pacheco-Calleros J, Rodríguez-Padilla C, et al. Immunohistochemical analysis ofprostate apoptosis response-4 (Par-4) in Mexican womenwith breast cancer: a preliminary study. Arch Med Res.2010 May;41(4):261–8. http://dx.doi.org/10.1016/j.arcmed.2010.05.005

  40. Zapata-Benavides P, Méndez-Vázquez JL, González-Rocha TR, Zamora-Avila DE, Franco-Molina MA,Garza-Garza R, et al. Expression of prostate apoptosisresponse (Par-4) is associated with progesterone receptorin breast cancer. Arch Med Res. 2009 Oct;40(7):595–9.http://dx.doi.org/10.1016/j.arcmed.2009.08.007

  41. Goswami A, Burikhanov R, de Thonel A, Fujita N,Goswami M, Zhao Y, et al. Binding and phosphorylationof par-4 by akt is essential for cancer cell survival. MolCell. 2005 Oct;20(1):33–44. http://dx.doi.org/10.1016/j.molcel.2005.08.016

  42. Gurumurthy S, Goswami A, Vasudevan KM, RangnekarVM. Phosphorylation of Par-4 by protein kinase A iscritical for apoptosis. Mol Cell Biol. 2005 Feb;25(3):1146-1161. DOI: 10.1128/MCB.25.3.1146-1161.2005

  43. de Thonel A, Hazoume A, Kochin V, Isoniemi K, JegoG, Fourmaux E, et al. Regulation of the proapoptoticfunctions of prostate apoptosis response-4 (Par-4) bycasein kinase 2 in prostate cancer cells. Cell Death Dis.2014 Jan;5(1):e1016-e1016. https://doi.org/10.1038/cddis.2013.532

  44. Ganguly S, Burikhanov R, Qiu S, Rangnekar VM.Discovery and Overview of Par-4. In: Rangnekar, V.M.(eds) Tumor Suppressor Par-4. Springer, Cham. 2022Jan. https://doi.org/10.1007/978-3-030-73572-2_1

  45. Du B, Shim JS. Targeting Epithelial-MesenchymalTransition (EMT) to Overcome Drug Resistance in Cancer.Molecules (Basel, Switzerland). 2016 Jul;21(7):965.https://doi.org/10.3390/molecules21070965

  46. Baulida J. Epithelial-to-mesenchymal transitiontranscription factors in cancer-associated fibroblasts.Mol Oncol. 2017 May;11(7): 847–859. https://doi.org/10.1002/1878-0261.12080

  47. Georgakopoulos Soares I, Chartoumpekis DV,Kyriazopoulou V, Zaravinos A. EMT Factors andMetabolic Pathways in Cancer. Front Oncol. 2020 Apr;10: 499. https://doi.org/10.3389/fonc.2020.00499

  48. Oghbaei F, Zarezadeh R, Jafari-Gharabaghlou D, RanjbarM, Nouri M, Fattahi A, et al. Epithelial-mesenchymaltransition process during embryo implantation. CellTissue Res. 2022 Jan; 388(1): 1–17. https://doi.org/10.1007/s00441-021-03574-w

  49. Francesco EM, Maggiolini M, Musti AM. Crosstalkbetween Notch, HIF-1α and GPER in Breast CancerEMT. Int J Mol Sci. 2018 Jul;19(7): 2011. https://doi.org/10.3390/ijms19072011

  50. Xu X, Zhang L, He X, Zhang P, Sun C, Xu X, et al.TGF-β plays a vital role in triple-negative breast cancer(TNBC) drug-resistance through regulating stemness,EMT and apoptosis. Biochem Biophys Res Commun.2018 Jul;502(1):160–5. http://dx.doi.org/10.1016/j.bbrc.2018.05.139

  51. Yoshimatsu Y, Wakabayashi I, Kimuro S, TakahashiN, Takahashi K, Kobayashi M, et al. TNF-α enhancesTGF-β-induced endothelial-to-mesenchymal transitionvia TGF-β signal augmentation. Cancer science. 2020May;111(7): 2385–2399. https://doi.org/10.1111/cas.14455

  52. Takatani-Nakase T, Matsui C, Hosotani M, Omura M,Takahashi K, Nakase I. Hypoxia enhances motilityand EMT through the Na+/H+ exchanger NHE-1in MDA-MB-231 breast cancer cells. Exp Cell Res.2022 Mar;412(1):113006. http://dx.doi.org/10.1016/j.yexcr.2021.113006

  53. Xu Y, Qin L, Sun T, Wu H, He T, Yang Z, et al.Twist1 promotes breast cancer invasion and metastasisby silencing Foxa1 expression. Oncogene. 2017Feb;36(8):1157–66. http://dx.doi.org/10.1038/onc.2016.286

  54. Mohammadi-Ghahhari N, Sznurkowska MK, Hulo N,Bernasconi L, Aceto N, Picard D. Cooperative interactionbetween ERα and the EMT-inducer ZEB1 reprogramsbreast cancer cells for bone metastasis. Nat Commun.2022 Apr;13(1):2104. http://dx.doi.org/10.1038/s41467-022-29723-5

  55. Karamanou K, Franchi M, Vynios D, Brézillon S.Epithelial-to-mesenchymal transition and invadopodiamarkers in breast cancer: Lumican a key regulator.Semin Cancer Biol. 2020 May; 62: 125–133. https://doi.org/10.1016/j.semcancer.2019.08.003

  56. Na TY, Schecterson L, Mendonsa AM, Gumbiner BM.The functional activity of E-cadherin controls tumor cellmetastasis at multiple steps. Proc Natl Acad Sci U S A.2020 Mar;117(11):5931–7. http://dx.doi.org/10.1073/pnas.1918167117

  57. Naderi R, Aziz SGG, Haghigi Asl AS. Evaluating theeffect of Alantolactone on the expression of N-cadherinand Vimentin genes effective in epithelial-mesenchymaltransition (EMT) in breast cancer cell line (MDAMB-231). Ann Med Surg. 2022 Jan; 73: 103240. https://doi.org/10.1016/j.amsu.2021.103240

  58. Katoch A, Suklabaidya S, Chakraborty S, NayakD, Rasool RU, Sharma D, et al. Dual role of Par-4 inabrogation of EMT and switching on Mesenchymal toEpithelial Transition (MET) in metastatic pancreaticcancer cells. Mol Carcinog. 2018 Apr;57(9):1102–1115.https://doi.org/10.1002/mc.22828

  59. Wang H, Guo S, Kim SJ, Shao F, Ho JWK, Wong KU,et al. Cisplatin prevents breast cancer metastasis throughblocking early EMT and retards cancer growth togetherwithpaclitaxel. Theranostics. 2021 Jan;11(5):2442–59.http://dx.doi.org/10.7150/thno.46460

  60. Wang J, Li Y, Ma F, Zhou H, Ding R, Lu B,et al. Inhibitory effect of Par-4 combined withcisplatin on human Wilms’ tumor cells. TumourBiol. 2017 Jul;39(7):1010428317716689. DOI:10.1177/1010428317716689

  61. Arellano-Rodríguez NC, Alvarez-Quezada OA,Benavides PZ, Vargas-Alanís G, Franco-Molina M,Zamora-Ávila D, et al. Curcumin Sensitizes 4T1Murine Breast Cancer Cells to Cisplatin Through PAR4Secretion. In vivo (Athens, Greece). 2022 Nov;36(6):2767–2773. https://doi.org/10.21873/invivo.13013

  62. Tan J, You Y, Xu T, Yu P, Wu D, Deng H, et al. Par-4downregulation confers cisplatin resistance in pancreaticcancer cells via PI3K/Akt pathway-dependent EMT.Toxicol Lett. 2014 Jan;224(1):7–15. http://dx.doi.org/10.1016/j.toxlet.2013.10.008

  63. Thayyullathil F, Pallichankandy S, Rahman A,Kizhakkayil J, Chathoth S, Patel M, et al. Caspase-3mediated release of SAC domain containing fragmentfrom Par-4 is necessary for the sphingosine-inducedapoptosis in Jurkat cells. J Mol Signal. 2013 Feb; 8(1):2. DOI: 10.1186/1750-2187-8-2

  64. Chaudhry P, Singh M, Parent S, Asselin E. Prostateapoptosis response 4 (Par-4), a novel substrate ofcaspase-3 during apoptosis activation. Mol Cell Biol.2012 Jan;32(4):826–39. http://dx.doi.org/10.1128/MCB.06321-11

  65. Clark AM, Ponniah K, Warden MS, Raitt EM, SmithBG, Pascal SM. Tetramer formation by the caspaseactivatedfragment of the Par-4 tumor suppressor. TheFEBS journal. 2019 Jun; 286(20): 4060–4073. https://doi.org/10.1111/febs.14955

  66. Burikhanov R, Hebbar N, Noothi SK, Shukla N,Sledziona J, Araujo N, et al. Chloroquine-induciblepar-4 secretion is essential for tumor cell apoptosis andinhibition of metastasis. Cell Rep. 2017 Jan;18(2):508–19. http://dx.doi.org/10.1016/j.celrep.2016.12.051

  67. Damrauer JS, Phelps SN, Amuchastegui K, Lupo R,Mabe NW, Walens A, et al. Foxo-dependent Par-4Upregulation Prevents Long-term Survival of ResidualCells Following PI3K–Akt InhibitionFoxo-Driven Par-4Expression Limits Residual Cell Survival. Mol CancerRes. 2018 Apr;16(4): 599-609. DOI: 10.1158/1541-7786.MCR-17-0492

  68. Ahmad SM, Nayak D, Mir KB, Faheem MM, Nawaz S,Yadav G, et al. Par-4 activation restrains EMT-inducedchemoresistance in PDAC by attenuating MDM-2. Pancreatology. 2020 Oct;20(8): 1698-1710. DOI:10.1016/j.pan.2020.09.021

  69. McKenna MK, Noothi SK, Alhakeem SS, ObenKZ, Greene JT, Mani R et al. Novel role of prostateapoptosis response-4 tumor suppressor in B-cell chroniclymphocytic leukemia. Blood. 2018 Jun; 131(26): 2943–2954. https://doi.org/10.1182/blood-2017-10-813931

  70. Santos RVC, de Sena WLB, Dos Santos FA, da SilvaFilho AF, da Rocha Pitta MG, da Rocha Pitta MG.Potential Therapeutic Agents Against Par-4 Target forCancer Treatment: Where Are We Going?. Curr. DrugTargets. 2019; 20(6): 635–654. https://doi.org/10.2174/1389450120666181126122440

  71. Zhang J, Dong W, Ren Y, Wei D. SAC-TRAIL, a novelanticancer fusion protein: expression, purification, andfunctional characterization. Appl Microbiol Biotechnol.2022 Feb; 106(4): 1511–1520. https://doi.org/10.1007/s00253-022-11807-3

  72. Kim K, Araujo P, Hebbar N, Zhou Z, Zheng X, Zheng Fetal. Development of a novel prostate apoptosis response-4(Par-4) protein entity with an extended duration of actionfor therapeutic treatment of cancer. Protein engineering,design & selection: PEDS. 2019 Nov; 32(3): 159–166.https://doi.org/10.1093/protein/gzz034

  73. Chen YT, Tseng TT, Tsai HP, Huang MY. Arylquin 1(Potent Par-4 Secretagogue) Inhibits Tumor Progressionand Induces Apoptosis in Colon Cancer Cells. Int J MolSci. 2022 May;23(10): 5645. https://doi.org/10.3390/ijms23105645




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