Abstract
Pheochromocytoma (PCC) is a neuroendocrine tumor that produces and secretes catecholamine from either the adrenal medulla or extra-adrenal locations. MicroRNAs (miRNAs, miR) can be used as biomarkers to detect cancer or the return of a previously treated disease. Blood-borne miRNAs might be envisioned as noninvasive markers of malignancy or prognosis, and new studies demonstrate that microRNAs are released in body fluids as well as tissues. MiRNAs have the potential to be therapeutic targets, which would greatly increase the restricted therapy options for adrenal tumors. This article aims to consolidate and synthesize the most recent studies on miRNAs in PCC, discussing their potential clinical utility as diagnostic and prognostic biomarkers while also addressing their limitations.
Similar content being viewed by others
Data availability
Not applicable.
References
Abd El Fattah YK, Abulsoud AI, AbdelHamid SG, Hamdy NM (2022) Interactome battling of lncRNA CCDC144NL-AS1: its role in the emergence and ferocity of cancer and beyond. Int J Biol Macromol 222:1676–1687
Abdel Mageed SS, Doghish AS, Ismail A, El-Husseiny AA, Fawzi SF, Mahmoud AMA, El-Mahdy HA (2023) The role of miRNAs in insulin resistance and diabetic macrovascular complications – a review. Int J Biol Macromol 230:123189
Abdelmaksoud NM, Abulsoud AI, Abdelghany TM, Elshaer SS, Rizk SM, Senousy MA (2023) Mitochondrial remodeling in colorectal cancer initiation, progression, metastasis, and therapy: a review. Pathol Res Pract 246:154509
Abulsoud AI, El-Husseiny HM, El-Husseiny AA, El-Mahdy HA, Ismail A, Elkhawaga SY, Khidr EG, Fathi D, Mady EA, Najda A, Algahtani M, Theyab A, Alsharif KF, Albrakati A, Bayram R, Abdel-Daim MM, Doghish AS (2023) Mutations in SARS-CoV-2: insights on structure, variants, vaccines, and biomedical interventions. Biomed Pharmacother 157:113977
Al-Noshokaty TM, Elballal MS, Helal GK, Abulsoud AI, Elshaer SS, El-Husseiny AA, Fathi D, Abdelmaksoud NM, Abdel Mageed SS, Midan HM, Zaki MB, Abd-Elmawla MA, Rizk NI, Elrebehy MA, Zewail MB, Mohammed OA, Doghish AS (2023) miRNAs driving diagnosis, prognosis and progression in Merkel cell carcinoma. Pathol Res Pract 249:154763
Al-Noshokaty TM, Mesbah NM, Abo-Elmatty DM, Abulsoud AI, Abdel-Hamed AR (2022) Selenium nanoparticles overcomes sorafenib resistance in thioacetamide induced hepatocellular carcinoma in rats by modulation of mTOR, NF-κB pathways and LncRNA-AF085935/GPC3 axis. J Life Sci 303:120675
Alrezk R, Suarez A, Tena I, Pacak K (2018) Update of pheochromocytoma syndromes: genetics, biochemical evaluation, and imaging. Front Endocrinol 9:515
Amit M, Takahashi H, Dragomir MP, Lindemann A, Gleber-Netto FO, Pickering CR, Anfossi S, Osman AA, Cai Y, Wang R, Knutsen E, Shimizu M, Ivan C, Rao X, Wang J, Silverman DA, Tam S, Zhao M, Caulin C, Zinger A, Tasciotti E, Dougherty PM, El-Naggar A, Calin GA, Myers JN (2020) Loss of p53 drives neuron reprogramming in head and neck cancer. Nature 578:449–454
Assié G, Letouzé E, Fassnacht M, Jouinot A, Luscap W, Barreau O, Omeiri H, Rodriguez S, Perlemoine K, René-Corail F, Elarouci N, Sbiera S, Kroiss M, Allolio B, Waldmann J, Quinkler M, Mannelli M, Mantero F, Papathomas T, De Krijger R, Tabarin A, Kerlan V, Baudin E, Tissier F, Dousset B, Groussin L, Amar L, Clauser E, Bertagna X, Ragazzon B, Beuschlein F, Libé R, de Reyniès A, Bertherat J (2014) Integrated genomic characterization of adrenocortical carcinoma. Nat Genet 46:607–612
Babiarz JE, Ruby JG, Wang Y, Bartel DP, Blelloch R (2008) Mouse ES cells express endogenous shRNAs, siRNAs, and other microprocessor-independent, dicer-dependent small RNAs. Genes Dev 22:2773–2785
Babin PJ, Gibbons GF (2009) The evolution of plasma cholesterol: direct utility or a “spandrel” of hepatic lipid metabolism? Prog Lipid Res 48:73–91
Bakr M, Abd-Elmawla MA, Elimam H, Gamal El-Din H, Fawzy A, Abulsoud AI, Rizk SM (2023) Telomerase RNA component lncRNA as potential diagnostic biomarker promotes CRC cellular migration and apoptosis evasion via modulation of β-catenin protein level. Non-Coding RNA Research 8:302–314
Bakr Zaki M, Abulsoud AI, Elsisi AM, Doghish AS, Mansour OAE, Amin AI, Elrebehy MA, Mohamed MY, Goda MA (2019) Potential role of circulating microRNAs (486–5p, 497, 509–5p and 605) in metabolic syndrome Egyptian male patients. Diabetes Metab Syndr Obes 12:601–611
Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297
Beard CM, Sheps SG, Kurland LT, Carney JA, Lie JT (1983) Occurrence of pheochromocytoma in Rochester, Minnesota, 1950 through 1979, 58(12):802–804
Callis TE, Pandya K, Seok HY, Tang R-H, Tatsuguchi M, Huang Z-P, Chen J-F, Deng Z, Gunn B, Shumate J (2009) MicroRNA-208a is a regulator of cardiac hypertrophy and conduction in mice. J Clin Investig 119:2772–2786
Calsina B, Castro-Vega LJ, Torres-Pérez R, Inglada-Pérez L, Currás-Freixes M, Roldán-Romero JM, Mancikova V, Letón R, Remacha L, Santos M, Burnichon N, Lussey-Lepoutre C, Rapizzi E, Graña O, Álvarez-Escolá C, de Cubas AA, Lanillos J, Cordero-Barreal A, Martínez-Montes ÁM, Bellucci A, Amar L, Fernandes-Rosa FL, Calatayud M, Aller J, Lamas C, Sastre-Marcos J, Canu L, Korpershoek E, Timmers HJ, Lenders JW, Beuschlein F, Fassnacht-Capeller M, Eisenhofer G, Mannelli M, Al-Shahrour F, Favier J, Rodríguez-Antona C, Cascón A, Montero-Conde C, Gimenez-Roqueplo AP, Robledo M (2019) Integrative multi-omics analysis identifies a prognostic miRNA signature and a targetable miR-21-3p/TSC2/mTOR axis in metastatic pheochromocytoma/paraganglioma. Theranostics 9:4946–4958
Castro-Vega LJ, Calsina B, Burnichon N, Drossart T, Martínez-Montes ÁM, Verkarre V, Amar L, Bertherat J, Rodríguez-Antona C, Favier J, Robledo M, Gimenez-Roqueplo AP (2020) Overexpression of miR-483-5p is confined to metastases and linked to high circulating levels in patients with metastatic pheochromocytoma/paraganglioma. Clin Transl Med 10(8):e260
Chabre O, Libé R, Assie G, Barreau O, Bertherat J, Bertagna X, Feige JJ, Cherradi N (2013) Serum miR-483-5p and miR-195 are predictive of recurrence risk in adrenocortical cancer patients. Endocr Relat Cancer 20:579–594
Chen CZ (2005) MicroRNAs as oncogenes and tumor suppressors. N Engl J Med 353:1768–1771
Colpaert RM, Calore M (2019) MicroRNAs in cardiac diseases. Cells 8:737
Crona J, Taïeb D, Pacak K (2017) New perspectives on pheochromocytoma and paraganglioma: toward a molecular classification. Endocr Rev 38:489–515
Cui M, Wang H, Yao X, Zhang D, **e Y, Cui R, Zhang X (2019) Circulating MicroRNAs in cancer: potential and challenge. Front Genet 10:626
Dahia PLM (2014) Pheochromocytoma and paraganglioma pathogenesis: learning from genetic heterogeneity. Nat Rev Cancer 14:108–119
de Cubas AA, Leandro-García LJ, Schiavi F, Mancikova V, Comino-Méndez I, Inglada-Pérez L, Perez-Martinez M, Ibarz N, **ménez-Embún P, López-Jiménez E, Maliszewska A, Letón R, Gómez Graña A, Bernal C, Alvarez-Escolá C, Rodríguez-Antona C, Opocher G, Muñoz J, Megias D, Cascón A, Robledo M (2013) Integrative analysis of miRNA and mRNA expression profiles in pheochromocytoma and paraganglioma identifies genotype-specific markers and potentially regulated pathways. Endocr Relat Cancer 20:477–493
Denli AM, Tops BB, Plasterk RH, Ketting RF, Hannon GJ (2004) Processing of primary microRNAs by the microprocessor complex. Nature 432:231–235
Doghish AS, Bassyouni AA, Mahfouz MH, Abd El-Aziz HG, Zakaria RY (2019) Plasma endoglin in type2 diabetic patients with nephropathy. Diabetes Metab Syndr 13:764–768
Doghish AS, Elkhatib WF, Hassan EA, Elkhateeb AF, Mahmoud EE, Ahmed MI, Khalil MA (2021a) Clinical characteristics of egyptian male patients with COVID-19 acute respiratory distress syndrome. PLoS ONE 16:e0249346
Doghish AS, Elsisi AM, Amin AI, Abulsoud AI (2021b) Circulating miR-148a-5p and miR-21-5p as novel diagnostic biomarkers in adult egyptian male patients with metabolic syndrome. Can J Diabetes 45:614–618
Doghish AS, Ismail A, El-Mahdy HA, Elkady MA, Elrebehy MA, Sallam AM (2022) A review of the biological role of miRNAs in prostate cancer suppression and progression. Int J Biol Macromol 197:141–156
Doghish AS, Ali MA, Elrebehy MA, Mohamed HH, Mansour R, Ghanem A, Hassan A, Elballal MS, Elazazy O, Elesawy AE, Abdel Mageed SS, Nassar YA, Mohammed OA, Abulsoud AI (2023a) The interplay between toxoplasmosis and host miRNAs: mechanisms and consequences. Pathol Res Pract 250:154790
Doghish AS, Elballal MS, Elazazy O, Elesawy AE, Elrebehy MA, Shahin RK, Midan HM, Sallam A-AM (2023b) The role of miRNAs in liver diseases: potential therapeutic and clinical applications. Pathol Res Pract 243:154375
Doghish AS, Elballal MS, Elazazy O, Elesawy AE, Shahin RK, Midan HM, Sallam A-AM, Elbadry AMM, Mohamed AKI, Ishak NW, Hassan KA, Ayoub AM, Shalaby RE, Elrebehy MA (2023c) miRNAs as potential game-changers in bone diseases: future medicinal and clinical Uses. Pathol Res Pract 245:154440
Doghish AS, Ismail A, El-Mahdy HA, Elkhawaga SY, Elsakka EGE, Mady EA, Elrebehy MA, Khalil MAF, El-Husseiny HM (2023d) miRNAs insights into rheumatoid arthritis: favorable and detrimental aspects of key performers. Life Sci 314:121321
Dragomir MP, Knutsen E, Calin GA (2022) Classical and noncanonical functions of miRNAs in cancers. Trends Genet 38:379–394
Duregon E, Rapa I, Votta A, Giorcelli J, Daffara F, Terzolo M, Scagliotti GV, Volante M, Papotti M (2014) MicroRNA expression patterns in adrenocortical carcinoma variants and clinical pathologic correlations. Hum Pathol 45:1555–1562
Ebert MS, Neilson JR, Sharp PA (2007) MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods 4:721–726
Eisenhofer G, Huynh T, Pacak K, Brouwers F, Walther M, Linehan W, Munson P, Mannelli M, Goldstein D, Elkahloun A (2004) Distinct gene expression profiles in norepinephrine-and epinephrine-producing hereditary and sporadic pheochromocytomas: activation of hypoxia-driven angiogenic pathways in von hippel-Lindau syndrome. Endocr Relat Cancer 11:897–911
Eissa KI, Kamel MM, Mohamed LW, Doghish AS, Alnajjar R, Al-Karmalawy AA, Kassab AE (2023) Design, synthesis, and biological evaluation of thienopyrimidine derivatives as multifunctional agents against Alzheimer's disease. Drug Dev Res 84(5):937–961
Elazazy O, Midan HM, Shahin RK, Elesawy AE, Elballal MS, Sallam A-AM, Elbadry AMM, Elrebehy MA, Bhnsawy A, Doghish AS (2023) Long non-coding RNAs and rheumatoid arthritis: pathogenesis and clinical implications. Pathol Res Pract 246:154512
El-Dakroury WA, Midan HM, Abulsoud AI, Elshaer SS, El-Husseiny AA, Fathi D, Abdelmaksoud NM, Mageed SSA, Elballal MS, Zaki MB (2023a) miRNAs orchestration of adrenocortical carcinoma-particular emphasis on diagnosis, progression and drug resistance. Pathol Res Pract 248:154665
El-Dakroury WA, Zewail MB, Amin MM (2023b) Design, optimization, and in-vivo performance of glipizide-loaded O-carboxymethyl chitosan nanoparticles in insulin resistant/type 2 diabetic rat model. J Drug Deliv Sci Technol 79:104040
Elesawy AE, Abulsoud AI, Moustafa HAM, Elballal MS, Sallam A-AM, Elazazy O, El-Dakroury WA, Mageed SSA, Abdelmaksoud NM, Midan HM (2023) miRNAs orchestration of testicular germ cell tumors-particular emphasis on diagnosis, progression and drug resistance. Pathol Res Pract 248:54612
Elkady MA, Doghish AS, Elshafei A, Elshafey MM (2021) MicroRNA-567 inhibits cell proliferation and induces cell apoptosis in A549 NSCLC cells by regulating cyclin-dependent kinase 8. Saudi J Biol Sci 28:2581–2590
Elkady MA, Yehia AM, Elsakka EGE, Abulsoud AI, Abdelmaksoud NM, Elshafei A, Elkhawaga SY, Ismail A, Mokhtar MM, El-Mahdy HA, Hegazy M, Elballal MS, Mohammed OA, El-Husseiny HM, Midan HM, El-Dakroury WA, Zewail MB, Abdel Mageed SS, Doghish AS (2023) miRNAs driving diagnosis, progression, and drug resistance in multiple myeloma. Pathol Res Pract 248:154704
Elkhawaga SY, Ismail A, Elsakka EGE, Doghish AS, Elkady MA, El-Mahdy HA (2023) miRNAs as cornerstones in adipogenesis and obesity. Life Sci 315:121382
Elsakka EGE, Abulsoud AI, El-Mahdy HA, Ismail A, Elballal MS, Mageed SSA, Khidr EG, Mohammed OA, Sarhan OM, Elkhawaga SY, El-Husseiny AA, Abdelmaksoud NM, El-Demerdash AA, Shahin RK, Midan HM, Elrebehy MA, Doghish AA, Doghish AS (2023) miRNAs orchestration of cardiovascular diseases – particular emphasis on diagnosis, and progression. Pathol Res Pract 248:154613
El-Sheikh NM, Abulsoud AI, Wasfey EF, Hamdy NM (2022) Insights on the potential oncogenic impact of long non-coding RNA nicotinamide nucleotide transhydrogenase antisense RNA 1 in different cancer types; integrating pathway(s) and clinical outcome(s) association. Pathol Res Pract 240:154183
El-Sheikh NM, Abulsoud AI, Fawzy A, Wasfey EF, Hamdy NM (2023) LncRNA NNT-AS1/hsa-miR-485–5p/HSP90 axis in-silico and clinical prospect correlated-to histologic grades-based CRC stratification: a step toward ncRNA precision. Pathol Res Pract 247:154570
Ergin K, Çetinkaya R (2022) Regulation of microRNAs. miRNomics. Springer, 2257:1–32
Erturk E, Onur OE, Akgun O, Tuna GP, Yildiz Y, Ari F (2022) Mitochondrial miRNAs (MitomiRs): their potential roles in breast and other cancers. Mitochondrion 66:74–81
Faria AM, Sbiera S, Ribeiro TC, Soares IC, Mariani BM, Freire DS, de Sousa GR, Lerario AM, Ronchi CL, Deutschbein T, Wakamatsu A, Alves VA, Zerbini MC, Mendonca BB, Fragoso MC, Latronico AC, Fassnacht M, Almeida MQ (2015) Expression of LIN28 and its regulatory microRNAs in adult adrenocortical cancer. Clin Endocrinol 82:481–488
Feinmesser M, Benbassat C, Meiri E, Benjamin H, Lebanony D, Lebenthal Y, de Vries L, Drozd T, Spector Y (2015) Specific microRNAs differentiate adrenocortical adenomas from carcinomas and correlate with Weiss histopathologic system. Appl Immunohistochem Mol Morphol 23:522–531
Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, Garcia JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037
Hamada N, Fujita Y, Kojima T, Kitamoto A, Akao Y, Nozawa Y, Ito M (2012) MicroRNA expression profiling of NGF-treated PC12 cells revealed a critical role for miR-221 in neuronal differentiation. Neurochem Int 60:743–750
Hermeking H (2007) p53 enters the microRNA world. Cancer Cell 12:414–418
Hunter MP, Ismail N, Zhang X, Aguda BD, Lee EJ, Yu L, **ao T, Schafer J, Lee M-LT, Schmittgen TD (2008) Detection of microRNA expression in human peripheral blood microvesicles. PLoS ONE 3:e3694
Ismail A, Abulsoud AI, Mansour OA, Fawzy A (2019) Diagnostic significance of miR-639 and miR-10b in βreast cancer patients. Meta Gene 19:155–159
Ismail A, Doghish AS, Elkhatib WF, Magdy AM, Mahmoud EE, Ahmed MI, Khalil MA (2022) Clinical and chest computed tomography features of patients suffering from mild and severe COVID-19 at Fayoum University Hospital in Egypt. PLoS ONE 17:e0271271
Ismail A, El-Mahdy HA, Eldeib MG, Doghish AS (2023) miRNAs as cornerstones in diabetic microvascular complications. Mol Genet Metab 138:106978
Jaiswal R, Gong J, Sambasivam S, Combes V, Mathys JM, Davey R, Grau GE, Bebawy M (2012) Microparticle-associated nucleic acids mediate trait dominance in cancer. FASEB J 26:420–429
Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080
Khidr EG, Abulsoud AI, Doghish AA, El-Mahdy HA, Ismail A, Elballal MS, Sarhan OM, Abdel Mageed SS, Elsakka EGE, Elkhawaga SY, El-Husseiny AA, Abdelmaksoud NM, El-Demerdash AA, Shahin RK, Midan HM, Elrebehy MA, Mohammed OA, Abulsoud LA, Doghish AS (2023) The potential role of miRNAs in the pathogenesis of cardiovascular diseases – a focus on signaling pathways interplay. Pathol Res Pract 248:154624
Kim SI, Shin D, Choi TH, Lee JC, Cheon G-J, Kim K-Y, Park M, Kim M (2007) Systemic and specific delivery of small interfering RNAs to the liver mediated by apolipoprotein AI. Mol Ther 15:1145–1152
Lee H, Kim SI, Shin D, Yoon Y, Choi TH, Cheon G-J, Kim M (2009) Hepatic siRNA delivery using recombinant human apolipoprotein AI in mice. Biochem Biophys Res Commun 378:192–196
Lee Y, El Andaloussi S, Wood MJ (2012) Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy. Hum Mol Genet 21:R125–R134
Li C, Dou P, Wang T, Lu X, Xu G, Lin X (2022) Defining disease-related modules based on weighted miRNA synergistic network. Comput Biol Med 152:106382
Liang Y-C, Wu Y-P, Chen D-N, Chen S-H, Li X-D, Sun X-L, Wei Y, Ning X, Xue X-Y (2018) Building a competing endogenous RNA network to find potential long non-coding RNA biomarkers for pheochromocytoma. Cell Physiol Biochem 51:2916–2924
Liu C, **e Y, Li X, Yao X, Wang X, Wang M, Li Z, Cao F (2021) Folic acid/peptides modified PLGA–PEI–PEG polymeric vectors as efficient gene delivery vehicles: synthesis, characterization and their biological performance. Mol Biotechnol 63:63–79
Liu S, Fan M, Zheng Q, Hao S, Yang L, **a Q, Qi C, Ge J (2022) MicroRNAs in Alzheimer’s disease: potential diagnostic markers and therapeutic targets. Biomed Pharmacother 148:112681
Lowery AJ, Walsh S, McDermott EW, Prichard RS (2013) Molecular and therapeutic advances in the diagnosis and management of malignant pheochromocytomas and paragangliomas. Oncologist 18:391–407
Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, Downing JR, Jacks T, Horvitz HR, Golub TR (2005) MicroRNA expression profiles classify human cancers. Nature 435:834–838
Ma W, Gehret PM, Hoff RE, Kelly LP, Suh WH (2019) The investigation into the toxic potential of iron oxide nanoparticles utilizing rat pheochromocytoma and human neural stem cells. Nanomaterials 9:453
Malhotra N, Lee J-S, Liman RAD, Ruallo JMS, Villaflores OB, Ger T-R, Hsiao C-D (2020) Potential toxicity of iron oxide magnetic nanoparticles: a review. Molecules 25:3159
Malumbres M (2013) miRNAs and cancer: an epigenetics view. Mol Aspects Med 34:863–874
Manso J, Bertazza L, Barollo S, Mondin A, Censi S, Carducci S, Ferrara AM, Boschin IM, Zovato S, Schiavi F, Gregianin M, Pennelli G, Iacobone M, Mian C (2022) Overexpression of miR-375 and L-type amino acid transporter 1 in pheochromocytoma and their molecular and functional implications 23(5):2413
Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10:155–159
Meyer-Rochow GY, Jackson NE, Conaglen JV, Whittle DE, Kunnimalaiyaan M, Chen H, Westin G, Sandgren J, Stålberg P, Khanafshar E, Shibru D, Duh QY, Clark OH, Kebebew E, Gill AJ, Clifton-Bligh R, Robinson BG, Benn DE, Sidhu SB (2010) MicroRNA profiling of benign and malignant pheochromocytomas identifies novel diagnostic and therapeutic targets. Endocr Relat Cancer 17:835–846
Midan HM, Helal GK, Abulsoud AI, Elshaer SS, El-Husseiny AA, Fathi D, Abdelmaksoud NM, Abdel Mageed SS, Elballal MS, Zaki MB, Abd-Elmawla MA, Al-Noshokaty TM, Rizk NI, Elrebehy MA, El-Dakroury WA, Hashem AH, Doghish AS (2023) The potential role of miRNAs in the pathogenesis of adrenocortical carcinoma – a focus on signaling pathways interplay. Pathol Res Pract 248:154690
Mocellin S, Pasquali S, Pilati P (2009) Oncomirs: from tumor biology to molecularly targeted anticancer strategies. Mini Rev Med Chem 9:70–80
Mohammed OA, Abdel-Reheim MA, Saleh LA, Alamri MMS, Alfaifi J, Adam MIE, Farrag AA, AlQahtani AAJ, BinAfif WF, Hashish AA, Abdel-Ghany S, Elmorsy EA, El-wakeel HS, Doghish AS, Hamad RS, Saber S (2023) Alvespimycin exhibits potential anti-TGF-β signaling in the setting of a proteasome activator in rats with bleomycin-induced pulmonary fibrosis: a promising novel approach. Pharmaceuticals 16:1123
Newman MA, Hammond SM (2010) Emerging paradigms of regulated microRNA processing. Genes Dev 24:1086–1092
Nomier YA, Alshahrani S, Elsabahy M, Asaad GF, Hassan A, El-Dakroury WA (2022) Ameliorative effect of chitosan nanoparticles against carbon tetrachloride-induced nephrotoxicity in Wistar rats. Pharm Biol 60:2134–2144
Oreglia M, Sbiera S, Fassnacht M, Guyon L, Denis J, Cristante J, Chabre O, Cherradi N (2020) Early postoperative circulating miR-483–5p is a prognosis marker for adrenocortical cancer. Cancers 12(3):724
Özata DM, Caramuta S, Velázquez-Fernández D, Akçakaya P, **e H, Höög A, Zedenius J, Bäckdahl M, Larsson C, Lui WO (2011) The role of microRNA deregulation in the pathogenesis of adrenocortical carcinoma. Endocr Relat Cancer 18:643–655
Patterson E, Webb R, Weisbrod A, Bian B, He M, Zhang L, Holloway AK, Krishna R, Nilubol N, Pacak K, Kebebew E (2012) The microRNA expression changes associated with malignancy and SDHB mutation in pheochromocytoma. Endocr Relat Cancer 19:157–166
Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans ES, Lindenberg JL, de Gruijl TD, Würdinger T, Middeldorp JM (2010) Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci 107:6328–6333
Peng Y, Croce CM (2016) The role of MicroRNAs in human cancer. Signal Transduct Target Ther 1:15004
Peters LJ, Biessen EA, Hohl M, Weber C, Van der Vorst EP, Santovito D (2020) Small things matter: relevance of microRNAs in cardiovascular disease. Front Physiol 11:793
Pillai S, Lo CY, Liew V, Lalloz M, Smith RA, Gopalan V, Lam AK-Y (2017) MicroRNA 183 family profiles in pheochromocytomas are related to clinical parameters and SDHB expression. Hum Pathol 64:91–97
Rechavi O, Erlich Y, Amram H, Flomenblit L, Karginov FV, Goldstein I, Hannon GJ, Kloog Y (2009) Cell contact-dependent acquisition of cellular and viral nonautonomously encoded small RNAs. Genes Dev 23:1971
Reisch N, Peczkowska M, Januszewicz A, Neumann HPH (2006) Pheochromocytoma: presentation, diagnosis and treatment. J Hypertens 24(12):2331–2339
Rizk NI, Abulsoud AI, Kamal MM, Kassem DH, Hamdy NM (2022) Exosomal-long non-coding RNAs journey in colorectal cancer: evil and goodness faces of key players. Life Sci 292:120325
Ruby JG, Jan CH, Bartel DP (2007) Intronic microRNA precursors that bypass Drosha processing. Nature 448:83–86
Sallam A-AM, Darwish SF, El-Dakroury WA, Radwan E (2021) Olmesartan niosomes ameliorates the indomethacin-induced gastric ulcer in rats: insights on MAPK and Nrf2/HO-1 signaling pathway. Pharm Res 38:1821–1838
Salman IT, Abulsoud AI, Abo-Elmatty DM, Fawzy A, Mesbah NM, Saleh SM (2023) The long non-coding RNA ZFAS1 promotes colorectal cancer progression via miR200b/ZEB1 axis. Pathol Res Pract 247:154567
Salvianti F, Canu L, Poli G, Armignacco R, Scatena C, Cantini G, Di Franco A, Gelmini S, Ercolino T, Pazzagli M, Nesi G, Mannelli M, Pinzani P, Luconi M (2017) New insights in the clinical and translational relevance of miR483-5p in adrenocortical cancer. Oncotarget 8:65525–65533
Shahin RK, Elkady MA, Abulsoud AI, Abdelmaksoud NM, Abdel Mageed SS, El-Dakroury WA, Zewail MB, Elazazy M, Sobhy MH, Nomier Y, Elazazy O, Elballal MS, Mohammed OA, Midan HM, Elrebehy MA, Ziada BO, Doghish AS (2023) miRNAs orchestration of gallbladder cancer - particular emphasis on diagnosis, progression and drug resistance. Pathol Res Pract 248:154684
Shantsila E, Kamphuisen P, Lip G (2010) Circulating microparticles in cardiovascular disease: implications for atherogenesis and atherothrombosis. J Thromb Haemost 8:2358–2368
Shehabeldine AM, Doghish AS, El-Dakroury WA, Hassanin MM, Al-Askar AA, AbdElgawad H, Hashem AH (2023) Antimicrobial, antibiofilm, and anticancer activities of syzygium aromaticum essential oil nanoemulsion. Molecules 28:5812
Sohel MH (2016) Extracellular/circulating microRNAs: release mechanisms, functions and challenges. Achiev Life Sci 10:175–186
Soon PS, Tacon LJ, Gill AJ, Bambach CP, Sywak MS, Campbell PR, Yeh MW, Wong SG, Clifton-Bligh RJ, Robinson BG, Sidhu SB (2009) miR-195 and miR-483-5p identified as predictors of poor prognosis in adrenocortical cancer. Clin Cancer Res 15:7684–7692
Steer CJ, Subramanian S (2012) Circulating microRNAs as biomarkers: a new frontier in diagnostics. Liver Transplant 18(3):265–269
Tömböl Z, Éder K, Kovács A, Szabó PM, Kulka J, Likó I, Zalatnai A, Rácz G, Tóth M, Patócs A, Falus A, Rácz K, Igaz P (2010) MicroRNA expression profiling in benign (sporadic and hereditary) and recurring adrenal pheochromocytomas. Mod Pathol 23:1583–1595
Turchinovich A, Weiz L, Langheinz A, Burwinkel B (2011) Characterization of extracellular circulating microRNA. Nucleic Acids Res 39:7223–7233
Turiák L, Misják P, Szabó TG, Aradi B, Pálóczi K, Ozohanics O, Drahos L, Kittel Á, Falus A, Buzás EI (2011) Proteomic characterization of thymocyte-derived microvesicles and apoptotic bodies in BALB/c mice. J Proteomics 74:2025–2033
Ullmann P, Nurmik M, Begaj R, Haan S, Letellier E (2019) Hypoxia- and microRNA-induced metabolic reprogramming of tumor-initiating cells. Cells 8:528
Urbé S, Sachse M, Row PE, Preisinger C, Barr FA, Strous G, Klumperman J, Clague MJ (2003) The UIM domain of Hrs couples receptor sorting to vesicle formation. J Cell Sci 116:4169–4179
Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9:654–659
Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT (2011) MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 13:423–433
Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, Lanza G, Scarpa A, Vecchione A, Negrini M, Harris CC, Croce CM (2006) A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A 103:2257–2261
von Lersner A, Droesen L, Zijlstra A (2019) Modulation of cell adhesion and migration through regulation of the immunoglobulin superfamily member ALCAM/CD166. Clin Exp Metas 36:87–95
Wang Z, Li Y, Zhong Y, Wang Y, Peng M (2020) Comprehensive analysis of aberrantly expressed competitive endogenous RNA network and identification of prognostic biomarkers in pheochromocytoma and paraganglioma. Onco Targets Ther 13:11377–11395
Weber JA, Baxter DH, Zhang S, Huang DY, How Huang K, Jen Lee M, Galas DJ, Wang K (2010) The microRNA spectrum in 12 body fluids. Clin Chem 56:1733–1741
Wei X, Ke H, Wen A, Gao B, Shi J, Feng Y (2021) Structural basis of microRNA processing by Dicer-like 1. Nat Plants 7:1389–1396
Wu KJ (2020) The role of miRNA biogenesis and DDX17 in tumorigenesis and cancer stemness. Biomed J 43:107–114
Wu TP, Wang T, Seetin MG, Lai Y, Zhu S, Lin K, Liu Y, Byrum SD, Mackintosh SG, Zhong M (2016) DNA methylation on N 6-adenine in mammalian embryonic stem cells. Nature 532:329–333
Wu J, Sun J (2010) Effect of iron oxide nanoparticles on PC12 cells by MTS and p53. 2010 3rd International Nanoelectronics Conference (INEC). IEEE, pp. 842–843
Xue Q, Sun K, Deng HJ, Lei ST, Dong JQ, Li GX (2014) MicroRNA-338-3p inhibits colorectal carcinoma cell invasion and migration by targeting smoothened. Jpn J Clin Oncol 44:13–21
Yang M, Liu R, Sheng J, Liao J, Wang Y, Pan E, Guo W, Pu Y, Yin L (2013) Differential expression profiles of microRNAs as potential biomarkers for the early diagnosis of esophageal squamous cell carcinoma. Oncol Rep 29:169–176
Yang N, Ekanem NR, Sakyi CA, Ray SD (2015) Hepatocellular carcinoma and microRNA: new perspectives on therapeutics and diagnostics. Adv Drug Deliv Rev 81:62–74
Yehia AM, Elsakka EGE, Abulsoud AI, Abdelmaksoud NM, Elshafei A, Elkhawaga SY, Ismail A, Mokhtar MM, El-Mahdy HA, Hegazy M, Elballal MS, Mohammed OA, El-Husseiny HM, Midan HM, El-Dakroury WA, Zewail MB, Abdel Mageed SS, Moustafa YM, Mostafa RM, Elkady MA, Doghish AS (2023) Decoding the role of miRNAs in multiple myeloma pathogenesis: a focus on signaling pathways. Pathol Res Pract 248:154715
Ying H, Ebrahimi M, Keivan M, Khoshnam SE, Salahi S, Farzaneh M (2021) miRNAs; a novel strategy for the treatment of COVID-19. Cell Biol Int 45:2045–2053
Zemach A, McDaniel IE, Silva P, Zilberman D (2010) Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328:916–919
Zernecke A, Bidzhekov K, Noels H, Shagdarsuren E, Gan L, Denecke B, Hristov M, Köppel T, Jahantigh MN, Lutgens E (2009) Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Science signaling 2:ra81–ra81
Zewail MB, El-Gizawy SA, Asaad GF, Shabana ME, El-Dakroury WA (2023) Chitosan coated clove oil-based nanoemulsion: an attractive option for oral delivery of leflunomide in rheumatoid arthritis. Int J Pharm 643:123224
Zhang Q-H, Sun H-M, Zheng R-Z, Li Y-C, Zhang Q, Cheng P, Tang Z-H, Huang F (2013) Meta-analysis of microRNA-183 family expression in human cancer studies comparing cancer tissues with noncancerous tissues. Gene 527:26–32
Zhao N, Su N, Wang G, Fu D, Gao F, Zhang Y (2021) microRNA-184 enhances the sensitivity of pheochromocytoma-12 cells to doxorubicin by targeting ADAM22. Mol Cell Toxicol 17:123–132
Zong L, Meng L, Shi R (2015) Role of miR-101 in pheochromocytoma patients with SDHD mutation. Int J Clin Exp Pathol 8:1545–1554
Acknowledgements
The authors are thankful to the Deanship of Scientific Research at University of Bisha for supporting this work through the Fast-Track Research Support Program. The authors would like to thank the Deanship of Scientific Research at Shaqra University for supporting this work.
Author information
Authors and Affiliations
Contributions
HAE, O.A.M., A.I., M.A.A., A.I.A., Mo.A.E., N.M.A., S.Y.E., A.E., and A.S.D.: conceptualization, methodology, supervision, writing — original draft, review and editing. E.G.E.E., M.M.M., M.S.E., R.K.S., W.A.E, S.S.A., and M.H.: investigation, writing — original draft, data curation, methodology. Ma.A.E., A.I., A.M.Y., M.H., and H.A.E.: formal analysis, resources, visualization, writing — original draft, writing — review and editing.The authors confirm that no paper mill and artificial intelligence was used.
Corresponding authors
Ethics declarations
Ethical approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Elsakka, E.G.E., Elshafei, A., Elkady, M.A. et al. From diagnosis to resistance: a symphony of miRNAs in pheochromocytoma progression and treatment response. Naunyn-Schmiedeberg's Arch Pharmacol 397, 1957–1969 (2024). https://doi.org/10.1007/s00210-023-02759-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00210-023-02759-0