Abstract
Specific, sensitive and non-invasive biomarkers are always needed in endocrine disorders. miRNAs are short, non-coding RNA molecules with well-known role in gene expression regulation. They are frequently dysregulated in metabolic and endocrine diseases. Recently it has been shown that they are secreted into biofluids by nearly all kind of cell types. As they can be taken up by other cells they may have a role in a new kind of paracrine, cell-to-cell communication. Circulating miRNAs are protected by RNA-binding proteins or microvesicles hence they can be attractive candidates as diagnostic or prognostic biomarkers. In this review, we summarize the characteristics of extracellular miRNA’s and our knowledge about their origin and potential roles in endocrine and metabolic diseases. Discussions about the technical challenges occurring during identification and measurement of extracellular miRNAs and future perspectives about their roles are also highlighted.
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References
Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T (2001) Identification of novel genes coding for small expressed RNAs. Science 294:853–858
Place RF, Li LC, Pookot D, Noonan EJ, Dahiya R (2008) MicroRNA-373 induces expression of genes with complementary promoter sequences. Proc Natl Acad Sci USA 105:1608–1613
Orom UA, Nielsen FC, Lund AH (2008) MicroRNA-10a binds the 5′UTR of ribosomal protein mRNAs and enhances their translation. Mol Cell 30:460–471
Zhang J, Guo H, Qian G, Ge S, Ji H, Hu X, Chen W (2010) MiR-145, a new regulator of the DNA fragmentation factor-45 (DFF45)-mediated apoptotic network. Mol Cancer 9:211
Chendrimada TP, Gregory RI, Kumaraswamy E, Norman J, Cooch N, Nishikura K, Shiekhattar R (2005) TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436:740–744
Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R (2005) Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 123:631–640
Chen K, Rajewsky N (2006) Natural selection on human microRNA binding sites inferred from SNP data. Nat Genet 38:1452–1456
Lewis BP, Burge CB, Bartel DP (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15–20
Mattick JS, Makunin IV (2005) Small regulatory RNAs in mammals. Hum Mol Genet. 14 Spec No 1:R121–R132
Szabó PM, Butz H, Igaz P, Rácz K, Hunyady L, Patócs A (2013) Minireview: miRomics in endocrinology: a novel approach for modeling endocrine diseases. Mol Endocrinol 27:573–585
Farazi TA, Hoell JI, Morozov P, Tuschl T (2013) MicroRNAs in human cancer. Adv Exp Med Biol 774:1–20
Rottiers V, Naar AM (2012) MicroRNAs in metabolism and metabolic disorders. Nat Rev Mol Cell Biol 13:239–250
Sivapragasam M, Rotondo F, Lloyd RV, Scheithauer BW, Cusimano M, Syro LV, Kovacs K (2011) MicroRNAs in the human pituitary. Endocr Pathol 22:134–143
Lawrie CH, Gal S, Dunlop HM, Pushkaran B, Liggins AP, Pulford K, Banham AH, Pezzella F, Boultwood J, Wainscoat JS, Hatton CS, Harris AL (2008) Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br J Haematol 141:672–675
Silva J, García V, Zaballos Á, Provencio M, Lombardía L, Almonacid L, García JM, Domínguez G, Peña C, Diaz R, Herrera M, Varela A, Bonilla F (2011) Vesicle-related microRNAs in plasma of nonsmall cell lung cancer patients and correlation with survival. Eur Respir J 37:617–623
Li X (2014) MiR-375, a microRNA related to diabetes. Gene 533:1–4
Hossain MM, Sohel MM, Schellander K, Tesfaye D (2012) Characterization and importance of microRNAs in mammalian gonadal functions. Cell Tissue Res 349:679–690
Lisse TS, Adams JS, Hewison M (2013) Vitamin D and microRNAs in bone. Crit Rev Eukaryot Gene Expr 23:195–214
Pallante P, Battista S, Pierantoni GM, Fusco A (2014) Deregulation of microRNA expression in thyroid neoplasias. Nat Rev Endocrinol 10:88–101
Leone V, D’Angelo D, Ferraro A, Pallante P, Rubio I, Santoro M, Croce CM, Fusco A (2011) A TSH-CREB1-microRNA loop is required for thyroid cell growth. Mol Endocrinol 25:1819–1830
Singh P, Soon PS, Feige JJ, Chabre O, Zhao JT, Cherradi N, Lalli E, Sidhu SB (2012) Dysregulation of microRNAs in adrenocortical tumors. Mol Cell Endocrinol 351:118–128
Gadelha MR, Kasuki L, Dénes J, Trivellin G, Korbonits M (2013) MicroRNAs: suggested role in pituitary adenoma pathogenesis. J Endocrinol Invest 36:889–895
Zhang Z, Florez S, Gutierrez-Hartmann A, Martin JF, Amendt BA (2010) MicroRNAs regulate pituitary development, and microRNA 26b specifically targets lymphoid enhancer factor 1 (Lef-1), which modulates pituitary transcription factor 1 (Pit-1) expression. J Biol Chem 285:34718–34728
Lynn FC, Skewes-Cox P, Kosaka Y, McManus MT, Harfe BD, German MS (2007) MicroRNA expression is required for pancreatic islet cell genesis in the mouse. Diabetes 56:2938–2945
Correa-Medina M, Bravo-Egana V, Rosero S, Ricordi C, Edlund H, Diez J, Pastori RL (2009) MicroRNA miR-7 is preferentially expressed in endocrine cells of the developing and adult human pancreas. Gene Expr Patterns 9:193–199
Hong X, Luense LJ, McGinnis LK, Nothnick WB, Christenson LK (2008) Dicer1 is essential for female fertility and normal development of the female reproductive system. Endocrinology 149:6207–6212
Mishra PJ, Merlino G (2009) MicroRNA reexpression as differentiation therapy in cancer. J Clin Invest 119:2119–2123
Mishra PJ, Humeniuk R, Mishra PJ, Longo-Sorbello GS, Banerjee D, Bertino JR (2007) A miR-24 microRNA binding-site polymorphism in dihydrofolate reductase gene leads to methotrexate resistance. Proc Natl Acad Sci USA 104:13513–13518
Mishra PJ, Bertino JR (2009) MicroRNA polymorphisms: the future of pharmacogenomics, molecular epidemiology and individualized medicine. Pharmacogenomics 10:399–416
Mishra PJ, Song B, Mishra PJ, Wang Y, Humeniuk R, Banerjee D, Merlino G, Ju J, Bertino JR (2009) MiR-24 tumor suppressor activity is regulated independent of p53 and through a target site polymorphism. PLoS One 4:e8445
Weber JA, Baxter DH, Zhang S, Huang DY, Huang KH, Lee MJ, Galas DJ, Wang K (2010) The microRNA spectrum in 12 body fluids. Clin Chem 56:1733–1741
Turchinovich A, Weiz L, Langheinz A, Burwinkel B (2011) Characterization of extracellular circulating microRNA. Nucleic Acids Res 39:7223–7233
Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, Mitchell PS, Bennett CF, Pogosova-Agadjanyan EL, Stirewalt DL, Tait JF, Tewari M (2011) Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 108:5003–5008
Turchinovich A, Weiz L, Burwinkel B (2012) Extracellular miRNAs: the mystery of their origin and function. Trends Biochem Sci 37:460–465
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
Krämer-Albers EM, Bretz N, Tenzer S, Winterstein C, Möbius W, Berger H, Nave KA, Schild H, Trotter J (2007) Oligodendrocytes secrete exosomes containing major myelin and stress-protective proteins: trophic support for axons? Proteomics Clin Appl 1:1446–1461
Quesenberry PJ, Aliotta JM (2008) The paradoxical dynamism of marrow stem cells: considerations of stem cells, niches, and microvesicles. Stem Cell Rev 4:137–147
Mallegol J, van NG, Heyman M (2005) Phenotypic and functional characterization of intestinal epithelial exosomes. Blood Cells Mol Dis 35:11–16
Zitvogel L, Regnault A, Lozier A, Wolfers J, Flament C, Tenza D, Ricciardi-Castagnoli P, Raposo G, Amigorena S (1998) Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med 4:594–600
Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, Geuze HJ (1996) B lymphocytes secrete antigen-presenting vesicles. J Exp Med 183:1161–1172
Thery C (2011) Exosomes: secreted vesicles and intercellular communications. F1000 Biol Rep 3:15
Thery C, Zitvogel L, Amigorena S (2002) Exosomes: composition, biogenesis and function. Nat Rev Immunol 2:569–579
Pigati L, Yaddanapudi SC, Iyengar R, Kim DJ, Hearn SA, Danforth D, Hastings ML, Duelli DM (2010) Selective release of microRNA species from normal and malignant mammary epithelial cells. PLoS One 5:e13515
Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, Schwille P, Brügger B, Simons M (2008) Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319:1244–1247
Poutsiaka DD, Schroder EW, Taylor DD, Levy EM, Black PH (1985) Membrane vesicles shed by murine melanoma cells selectively inhibit the expression of Ia antigen by macrophages. J Immunol 134:138–144
Kucharzewska P, Belting M (2013) Emerging roles of extracellular vesicles in the adaptive response of tumour cells to microenvironmental stress. J Extracell Vesicles 2:20304
Kucharzewska P, Christianson HC, Welch JE, Svensson KJ, Fredlund E, Ringnér M, Mörgelin M, Bourseau-Guilmain E, Bengzon J, Belting M (2013) Exosomes reflect the hypoxic status of glioma cells and mediate hypoxia-dependent activation of vascular cells during tumor development. Proc Natl Acad Sci USA 110:7312–7317
Peinado H, Lavotshkin S, Lyden D (2011) The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin Cancer Biol 21:139–146
Skog J, Würdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT Jr, Carter BS, Krichevsky AM, Breakefield XO (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10:1470–1476
Fabbri M, Paone A, Calore F, Galli R, Gaudio E, Santhanam R, Lovat F, Fadda P, Mao C, Nuovo GJ, Zanesi N, Crawford M, Ozer GH, Wernicke D, Alder H, Caligiuri MA, Nana-Sinkam P, Perrotti D, Croce CM (2012) MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci USA 109:E2110–E2116
Yang L, Wu X, Luo C, He Y, Zhang Y, Chen X, Zhang L, Chen L (2012) Effects of renal carcinoma cell line ACHN-derived exosomes on ACHN cell proliferation and apoptosis. Nan Fang Yi Ke Da Xue Xue Bao 32:1498–1502
Ohshima K, Inoue K, Fujiwara A, Hatakeyama K, Kanto K, Watanabe Y, Muramatsu K, Fukuda Y, Ogura S, Yamaguchi K, Mochizuki T (2010) Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS One 5:e13247
Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, Guo J, Zhang Y, Chen J, Guo X, Li Q, Li X, Wang W, Zhang Y, Wang J, Jiang X, Xiang Y, Xu C, Zheng P, Zhang J, Li R, Zhang H, Shang X, Gong T, Ning G, Wang J, Zen K, Zhang J, Zhang CY (2008) Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res 18:997–1006
Kroh EM, Parkin RK, Mitchell PS, Tewari M (2010) Analysis of circulating microRNA biomarkers in plasma and serum using quantitative reverse transcription-PCR (qRT-PCR). Methods 50:298–301
Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O’Briant KC, Allen A, Lin DW, Urban N, Drescher CW, Knudsen BS, Stirewalt DL, Gentleman R, Vessella RL, Nelson PS, Martin DB, Tewari M (2008) Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 105:10513–10518
Laterza OF, Scott MG, Garrett-Engele PW, Korenblat KM, Lockwood CM (2013) Circulating miR-122 as a potential biomarker of liver disease. Biomark Med 7:205–210
Weng H, Shen C, Hirokawa G, Ji X, Takahashi R, Shimada K, Kishimoto C, Iwai N (2011) Plasma miR-124 as a biomarker for cerebral infarction. Biomed Res 32:135–141
Corsten MF, Dennert R, Jochems S, Kuznetsova T, Devaux Y, Hofstra L, Wagner DR, Staessen JA, Heymans S, Schroen B (2010) Circulating MicroRNA-208b and MicroRNA-499 reflect myocardial damage in cardiovascular disease. Circ Cardiovasc Genet 3:499–506
Teixeira AL, Ferreira M, Silva J, Gomes M, Dias F, Santos JI, Maurício J, Lobo F, Medeiros R (2014) Higher circulating expression levels of miR-221 associated with poor overall survival in renal cell carcinoma patients. Tumour Biol 35:4057–4066
Selth LA, Townley SL, Bert AG, Stricker PD, Sutherland PD, Horvath LG, Goodall GJ, Butler LM, Tilley WD (2013) Circulating microRNAs predict biochemical recurrence in prostate cancer patients. Br J Cancer 109:641–650
Tanaka K, Miyata H, Yamasaki M, Sugimura K, Takahashi T, Kurokawa Y, Nakajima K, Takiguchi S, Mori M, Doki Y (2013) Circulating miR-200c levels significantly predict response to chemotherapy and prognosis of patients undergoing neoadjuvant chemotherapy for esophageal cancer. Ann Surg Oncol 20(Suppl 3):S607–S615
Guay C, Regazzi R (2013) Circulating microRNAs as novel biomarkers for diabetes mellitus. Nat Rev Endocrinol 9:513–521
Zampetaki A, Kiechl S, Drozdov I, Willeit P, Mayr U, Prokopi M, Mayr A, Weger S, Oberhollenzer F, Bonora E, Shah A, Willeit J, Mayr M (2010) Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circ Res 107:810–817
Kong L, Zhu J, Han W, Jiang X, Xu M, Zhao Y, Dong Q, Pang Z, Guan Q, Gao L, Zhao J, Zhao L (2011) Significance of serum microRNAs in pre-diabetes and newly diagnosed type 2 diabetes: a clinical study. Acta Diabetol 48:61–69
Karolina DS, Tavintharan S, Armugam A, Sepramaniam S, Pek SL, Wong MT, Lim SC, Sum CF, Jeyaseelan K (2012) Circulating miRNA profiles in patients with metabolic syndrome. J Clin Endocrinol Metab 97:E2271–E2276
Zhang T, Lv C, Li L, Chen S, Liu S, Wang C, Su B (2013) Plasma miR-126 is a potential biomarker for early prediction of type 2 diabetes mellitus in susceptible individuals. Biomed Res Int 2013:761617
Nielsen LB, Wang C, Sørensen K, Bang-Berthelsen CH, Hansen L, Andersen ML, Hougaard P, Juul A, Zhang CY, Pociot F, Mortensen HB (2012) Circulating levels of microRNA from children with newly diagnosed type 1 diabetes and healthy controls: evidence that miR-25 associates to residual beta-cell function and glycaemic control during disease progression. Exp Diabetes Res 2012:896362
Sebastiani G, Grieco FA, Spagnuolo I, Galleri L, Cataldo D, Dotta F (2011) Increased expression of microRNA miR-326 in type 1 diabetic patients with ongoing islet autoimmunity. Diabetes Metab Res Rev 27:862–866
Salas-Pérez F, Codner E, Valencia E, Pizarro C, Carrasco E, Pérez-Bravo F (2013) MicroRNAs miR-21a and miR-93 are down regulated in peripheral blood mononuclear cells (PBMCs) from patients with type 1 diabetes. Immunobiology 218:733–737
Erener S, Mojibian M, Fox JK, Denroche HC, Kieffer TJ (2013) Circulating miR-375 as a biomarker of beta-cell death and diabetes in mice. Endocrinology 154:603–608
Prats-Puig A, Ortega FJ, Mercader JM, Moreno-Navarrete JM, Moreno M, Bonet N, Ricart W, López-Bermejo A, Fernández-Real JM (2013) Changes in circulating microRNAs are associated with childhood obesity. J Clin Endocrinol Metab 98:E1655–E1660
Wang YC, Li Y, Wang XY, Zhang D, Zhang H, Wu Q, He YQ, Wang JY, Zhang L, Xia H, Yan J, Li X, Ying H (2013) Circulating miR-130b mediates metabolic crosstalk between fat and muscle in overweight/obesity. Diabetologia 56:2275–2285
Cermelli S, Ruggieri A, Marrero JA, Ioannou GN, Beretta L (2011) Circulating microRNAs in patients with chronic hepatitis C and non-alcoholic fatty liver disease. PLoS One 6:e23937
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
Roldo C, Missiaglia E, Hagan JP, Falconi M, Capelli P, Bersani S, Calin GA, Volinia S, Liu CG, Scarpa A, Croce CM (2006) MicroRNA expression abnormalities in pancreatic endocrine and acinar tumors are associated with distinctive pathologic features and clinical behavior. J Clin Oncol 24:4677–4684
Li SC, Essaghir A, Martijn C, Lloyd RV, Demoulin JB, Oberg K, Giandomenico V (2013) Global microRNA profiling of well-differentiated small intestinal neuroendocrine tumors. Mod Pathol 26:685–696
Li A, Yu J, Kim H, Wolfgang CL, Canto MI, Hruban RH, Goggins M (2013) MicroRNA array analysis finds elevated serum miR-1290 accurately distinguishes patients with low-stage pancreatic cancer from healthy and disease controls. Clin Cancer Res 19:3600–3610
Yu S, Liu Y, Wang J, Guo Z, Zhang Q, Yu F, Zhang Y, Huang K, Li Y, Song E, Zheng XL, Xiao H (2012) Circulating microRNA profiles as potential biomarkers for diagnosis of papillary thyroid carcinoma. J Clin Endocrinol Metab 97:2084–2092
Lee JC, Zhao JT, Clifton-Bligh RJ, Gill A, Gundara JS, Ip JC, Glover A, Sywak MS, Delbridge LW, Robinson BG, Sidhu SB (2013) MicroRNA-222 and microRNA-146b are tissue and circulating biomarkers of recurrent papillary thyroid cancer. Cancer 119:4358–4365
Lee YS, Lim YS, Lee JC, Wang SG, Park HY, Kim SY, Lee BJ (2015) Differential expression levels of plasma-derived miR-146b and miR-155 in papillary thyroid cancer. Oral Oncol 51:77–83
Cantara S, Pilli T, Sebastiani G, Cevenini G, Busonero G, Cardinale S, Dotta F, Pacini F (2014) Circulating miRNA95 and miRNA190 are sensitive markers for the differential diagnosis of thyroid nodules in a Caucasian population. J Clin Endocrinol Metab 99:4190–4198
Patel D, Boufraqech M, Jain M, Zhang L, He M, Gesuwan K, Gulati N, Nilubol N, Fojo T, Kebebew E (2013) MiR-34a and miR-483-5p are candidate serum biomarkers for adrenocortical tumors. Surgery 154:1224–1228
Szabó DR, Luconi M, Szabó PM, Tóth M, Szücs N, Horányi J, Nagy Z, Mannelli M, Patócs A, Rácz K, Igaz P (2014) Analysis of circulating microRNAs in adrenocortical tumors. Lab Invest 94:331–339
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
Palumbo T, Faucz FR, Azevedo M, Xekouki P, Iliopoulos D, Stratakis CA (2013) Functional screen analysis reveals miR-26b and miR-128 as central regulators of pituitary somatomammotrophic tumor growth through activation of the PTEN–AKT pathway. Oncogene 32:1651–1659
D’Angelo D, Palmieri D, Mussnich P, Roche M, Wierinckx A, Raverot G, Fedele M, Croce CM, Trouillas J, Fusco A (2012) Altered microRNA expression profile in human pituitary GH adenomas: down-regulation of miRNA targeting HMGA1, HMGA2, and E2F1. J Clin Endocrinol Metab 97:E1128–E1138
Butz H, Likó I, Czirják S, Igaz P, Korbonits M, Rácz K, Patócs A (2011) MicroRNA profile indicates downregulation of the TGFβ pathway in sporadic non-functioning pituitary adenomas. Pituitary 14:112–124
Gentilin E, Tagliati F, Filieri C, Molè D, Minoia M, Rosaria Ambrosio M, Degli Uberti EC, Zatelli MC (2013) miR-26a plays an important role in cell cycle regulation in ACTH-secreting pituitary adenomas by modulating protein kinase Cδ. Endocrinology 154:1690–1700
Qian ZR, Asa SL, Siomi H, Siomi MC, Yoshimoto K, Yamada S, Wang EL, Rahman MM, Inoue H, Itakura M, Kudo E, Sano T (2009) Overexpression of HMGA2 relates to reduction of the let-7 and its relationship to clinicopathological features in pituitary adenomas. Mod Pathol 22:431–441
Leone V, Langella C, D’Angelo D, Mussnich P, Wierinckx A, Terracciano L, Raverot G, Lachuer J, Rotondi S, Jaffrain-Rea ML, Trouillas J, Fusco A (2014) Mir-23b and miR-130b expression is downregulated in pituitary adenomas. Mol Cell Endocrinol 390:1–7
Butz H, Likó I, Czirják S, Igaz P, Khan MM, Zivkovic V, Bálint K, Korbonits M, Rácz K, Patócs A (2010) Down-regulation of Wee1 kinase by a specific subset of microRNA in human sporadic pituitary adenomas. J Clin Endocrinol Metab 95:E181–E191
Trivellin G, Butz H, Delhove J, Igreja S, Chahal HS, Zivkovic V, McKay T, Patócs A, Grossman AB, Korbonits M (2012) MicroRNA miR-107 is overexpressed in pituitary adenomas and inhibits the expression of aryl hydrocarbon receptor-interacting protein in vitro. Am J Physiol Endocrinol Metab 303:E708–E719
Bottoni A, Piccin D, Tagliati F, Luchin A, Zatelli MC, Degli Uberti EC (2005) miR-15a and miR-16-1 down-regulation in pituitary adenomas. J Cell Physiol 204:280–285
Amaral FC, Torres N, Saggioro F, Neder L, Machado HR, Silva WA Jr, Moreira AC, Castro M (2009) MicroRNAs differentially expressed in ACTH-secreting pituitary tumors. J Clin Endocrinol Metab 94:320–323
Bottoni A, Zatelli MC, Ferracin M, Tagliati F, Piccin D, Vignali C, Calin GA, Negrini M, Croce CM, Degli Uberti EC (2007) Identification of differentially expressed microRNAs by microarray: a possible role for microRNA genes in pituitary adenomas. J Cell Physiol 210:370–377
Mao ZG, He DS, Zhou J, Yao B, Xiao WW, Chen CH, Zhu YH, Wang HJ (2010) Differential expression of microRNAs in GH-secreting pituitary adenomas. Diagn Pathol 5:79
Wang C, Su Z, Sanai N, Xue X, Lu L, Chen Y, Wu J, Zheng W, Zhuge Q, Wu ZB (2012) microRNA expression profile and differentially-expressed genes in prolactinomas following bromocriptine treatment. Oncol Rep 27:1312–1320
Di Ieva A, Butz H, Niamah M, Rotondo F, De Rosa S, Sav A, Yousef GM, Kovacs K, Cusimano MD (2014) MicroRNAs as biomarkers in pituitary tumors. Neurosurgery. 75:181–189
Wang Q, Li P, Li A, Jiang W, Wang H, Wang J, Xie K (2012) Plasma specific miRNAs as predictive biomarkers for diagnosis and prognosis of glioma. J Exp Clin Cancer Res 31:97
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
Wang K, Yuan Y, Cho JH, McClarty S, Baxter D, Galas DJ (2012) Comparing the MicroRNA spectrum between serum and plasma. PLoS One 7:e41561
Pritchard CC, Kroh E, Wood B, Arroyo JD, Dougherty KJ, Miyaji MM, Tait JF, Tewari M (2012) Blood cell origin of circulating microRNAs: a cautionary note for cancer biomarker studies. Cancer Prev Res (Phila) 5:492–497
Redova M, Poprach A, Nekvindova J, Iliev R, Radova L, Lakomy R, Svoboda M, Vyzula R, Slaby O (2012) Circulating miR-378 and miR-451 in serum are potential biomarkers for renal cell carcinoma. J Transl Med 10:55
Sanders I, Holdenrieder S, Walgenbach-Brünagel G, von Ruecker A, Kristiansen G, Müller SC, Ellinger J (2012) Evaluation of reference genes for the analysis of serum miRNA in patients with prostate cancer, bladder cancer and renal cell carcinoma. Int J Urol 19:1017–1025
Zen K, Zhang CY (2012) Circulating microRNAs: a novel class of biomarkers to diagnose and monitor human cancers. Med Res Rev 32:326–348
Acknowledgments
This study has been funded by “Lendület” grant provided to Attila Patocs by Hungarian Academy of Sciences.
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The authors declare that there is no conflict of interest.
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All procedures performing in studies involving human participants were in accordance with the ethical standards of institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
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Informed consent of the present retrospective study was waived.
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Butz, H., Kinga, N., Racz, K. et al. Circulating miRNAs as biomarkers for endocrine disorders. J Endocrinol Invest 39, 1–10 (2016). https://doi.org/10.1007/s40618-015-0316-5
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DOI: https://doi.org/10.1007/s40618-015-0316-5