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Gene expression in prolactinomas: a systematic review

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Abstract

Introduction

Prolactinomas are the most common functional pituitary adenomas. Current classification systems rely on phenotypic elements and have few molecular markers for complementary classification. Treatment protocols for prolactinomas are also devoid of molecular targets, leaving those refractory to standard treatments without many options.

Methods

A systematic literature review was performed utilizing the PRISMA guidelines. We aimed to summarize prior research exploring gene and protein expression in prolactinomas in order to highlight molecular variations associated with tumor development, growth, and prolactin secretion. A PubMed search of select MeSH terms was performed to identify all studies reporting gene and protein expression findings in prolactinomas from 1990 to 2014.

Results

1392 abstracts were screened and 51 manuscripts were included in the analysis, yielding 54 upregulated and 95 downregulated genes measured by various direct and indirect analytical methods. Of the many genes identified, three upregulated (HMGA2, HST, SNAP25), and three downregulated (UGT2B7, Let7, miR-493) genes were selected for further analysis based on our subjective identification of strong potential targets.

Conclusions

Many significant genes have been identified and validated in prolactinomas and most have not been fully analyzed for therapeutic and diagnostic potential. These genes could become candidate molecular targets for biomarker development and precision drug targeting as well as catalyze deeper research efforts utilizing next generation profiling/sequencing techniques, particularly genome scale expression and epigenomic analyses.

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References

  1. Ezzat S, Asa SL, Couldwell WT, Barr CE, Dodge WE, Vance ML, McCutcheon IE (2004) The prevalence of pituitary adenomas. Cancer 101(3):613–619

    Article  PubMed  Google Scholar 

  2. Daly AF, Rixhon M, Adam C, Dempegioti A, Tichomirowa MA, Beckers A (2006) High prevalence of pituitary adenomas: a cross-sectional study in the province of Liege, Belgium. J Clin Endocrinol Metab 91(12):4769–4775

    Article  PubMed  CAS  Google Scholar 

  3. Fernandez A, Karavitaki N, Wass JA (2010) Prevalence of pituitary adenomas: a community-based, cross-sectional study in Banbury (Oxfordshire, UK). Clin Endocrinol (Oxf) 72(3):377–382

    Article  Google Scholar 

  4. Melmed S (2011) Pathogenesis of pituitary tumors. Nat Rev Endocrinol 7(5):257–266

    Article  PubMed  CAS  Google Scholar 

  5. Mindermann T, Wilson CB (1994) Age-related and gender-related occurrence of pituitary adenomas. Clin Endocrinol (Oxf) 41(3):359–364

    Article  CAS  Google Scholar 

  6. Raappana A, Koivukangas J, Ebeling T, Pirilä T (2010) Incidence of pituitary adenomas in Northern Finland in 1992–2007. J Clin Endocrinol Metab 95(9):4268–4275

    Article  PubMed  CAS  Google Scholar 

  7. Ciccarelli A, Daly AF, Beckers A (2005) The epidemiology of prolactinomas. Pituitary 8(1):3–6

    Article  PubMed  Google Scholar 

  8. Arafah BM, Nasrallah MP (2001) Pituitary tumors: pathophysiology, clinical manifestations and management. Endocr Relat Cancer 8(4):287–305

    Article  PubMed  CAS  Google Scholar 

  9. Davis JR, Farrell WE, Clayton RN (2001) Pituitary tumours. Reproduction 121(3):363–371

    Article  PubMed  CAS  Google Scholar 

  10. Knosp E, Steiner E, Kitz K, Matula C (1993) Pituitary adenomas with invasion of the cavernous sinus space. Neurosurgery 33(4):610–617

    Article  PubMed  CAS  Google Scholar 

  11. Barnes L (2005) Pathology and genetics of head and neck tumours. IARC Press, Lyon

    Google Scholar 

  12. Zada G, Woodmansee WW, Ramkissoon S, Amadio J, Nose V, Laws ER Jr (2011) Atypical pituitary adenomas: incidence, clinical characteristics, and implications. J Neurosurg 114(2):336–344

    Article  PubMed  Google Scholar 

  13. Smith MV, Laws ER Jr (1994) Magnetic resonance imaging measurements of pituitary stalk compression and deviation in patients with nonprolactin-secreting intrasellar and parasellar tumors: lack of correlation with serum prolactin levels. Neurosurgery 34(5):834–839

    Article  PubMed  CAS  Google Scholar 

  14. Korevaar T, Wass JA, Grossman AB, Karavitaki N (2012) Disconnection hyperprolactinaemia in nonadenomatous sellar/parasellar lesions practically never exceeds 2000 mU/l. Clin Endocrinol (Oxf) 76(4):602–603

    Article  CAS  Google Scholar 

  15. Di Sarno A, Landi ML, Cappabianca P, Di Salle F, Rossi FW, Pivonello R, Di Somma C, Faggiano A, Lombardi G, Colao A (2001) Resistance to cabergoline as compared with bromocriptine in hyperprolactinemia: prevalence, clinical definition, and therapeutic strategy. J Clin Endocrinol Metab 86(11):5256–5261

    Article  PubMed  Google Scholar 

  16. Gillam MP, Molitch ME, Lombardi G, Colao A (2006) Advances in the treatment of prolactinomas. Endocr Rev 27(5):485–534

    Article  PubMed  CAS  Google Scholar 

  17. Moher D, Liberati A, Tetzlaff J, Altman DG (2010) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 8(5):336–341

    Article  PubMed  Google Scholar 

  18. Yoshida S, Kato T, Higuchi M, Yako H, Chen M, Kanno N, Ueharu H, Kato Y (2013) Rapid transition of NESTIN-expressing dividing cells from PROP1-positive to PIT1-positive advances prenatal pituitary development. J Neuroendocrinol 25(9):779–791

    Article  PubMed  CAS  Google Scholar 

  19. 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(3):431–441

    Article  PubMed  CAS  Google Scholar 

  20. Scott AF, Jabs EW, Hamosh A, Bocchini CA, Hartz PA (2014) High mobility group AT-Hook 2; HMGA2. http://omim.org/entry/600698?search=HMGA2&highlight=hmga2. Accessed 30 Dec 2014

  21. Palmieri D, D’Angelo D, Valentino T, De Martino I, Ferraro A, Wierinckx A, Fedele M, Trouillas J, Fusco A (2012) Downregulation of HMGA-targeting microRNAs has a critical role in human pituitary tumorigenesis. Oncogene 31(34):3857–3865

    Article  PubMed  CAS  Google Scholar 

  22. Fedele M, Palmieri D, Fusco A (2010) HMGA2: a pituitary tumour subtype-specific oncogene? Mol Cell Endocrinol 326(1–2):19–24

    Article  PubMed  CAS  Google Scholar 

  23. Fedele M, Battista S, Kenyon L, Baldassarre G, Fidanza V, Klein-Szanto AJ, Parlow AF, Visone R, Pierantoni GM, Outwater E, Santoro M, Croce CM, Fusco A (2002) Overexpression of the HMGA2 gene in transgenic mice leads to the onset of pituitary adenomas. Oncogene 21(20):3190–3198

    Article  PubMed  CAS  Google Scholar 

  24. Fedele M, Visone R, De Martino I, Troncone G, Palmieri D, Battista S, Ciarmiello A, Pallante P, Arra C, Melillo RM, Helin K, Croce CM, Fusco A (2006) HMGA2 induces pituitary tumorigenesis by enhancing E2F1 activity. Cancer Cell 9(6):459–471

    Article  PubMed  CAS  Google Scholar 

  25. De Martino I, Visone R, Wierinckx A, Palmieri D, Ferraro A, Cappabianca P, Chiappetta G, Forzati F, Lombardi G, Colao A, Trouillas J, Fedele M, Fusco A (2009) HMGA proteins up-regulate CCNB2 gene in mouse and human pituitary adenomas. Cancer Res 69(5):1844–1850

    Article  PubMed  CAS  Google Scholar 

  26. 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(1–2):1–7

    Article  PubMed  CAS  Google Scholar 

  27. 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(7):E1128–E1138

    Article  PubMed  CAS  Google Scholar 

  28. Hamosh A, Watkins-Chow D (2011) Fibroblast growth factor 4; FGF4. http://www.omim.org/entry/164980. Accessed 30 Dec 2014

  29. Sakamoto H, Mori M, Taira M, Yoshida T, Matsukawa S, Shimizu K, Sekiguchi M, Terada M, Sugimura T (1986) Transforming gene from human stomach cancers and a noncancerous portion of stomach mucosa. Proc Natl Acad Sci USA 83(11):3997–4001

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Yoshida T, Tsutsumi M, Sakamoto H, Miyagawa K, Teshima S, Sugimura T, Terada M (1988) Expression of the HST1 oncogene in human germ cell tumors. Biochem Biophys Res Commun 155(3):1324–1329

    Article  PubMed  CAS  Google Scholar 

  31. Huebner K, Ferrari AC, Delli BP, Croce CM, Basilico C (1988) The FGF-related oncogene, K-FGF, maps to human chromosome region 11q13, possibly near int-2. Oncogene Res 3(3):263–270

    PubMed  CAS  Google Scholar 

  32. Shimon I, Melmed S (1997) Genetic basis of endocrine disease: pituitary tumor pathogenesis. J Clin Endocrinol Metab 82(6):1675–1681

    PubMed  CAS  Google Scholar 

  33. Shimon I, Hinton DR, Weiss MH, Melmed S (1998) Prolactinomas express human heparin-binding secretory transforming gene (hst) protein product: marker of tumour invasiveness. Clin Endocrinol (Oxf) 48(1):23–29

    Article  CAS  Google Scholar 

  34. Shimon I, Hüttner A, Said J, Spirina OM, Melmed S (1996) Heparin-binding secretory transforming gene (hst) facilitates rat lactotrope cell tumorigenesis and induces prolactin gene transcription. J Clin Invest 97(1):187–195

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Hurko O, Hamosh A, Hartz PA, Black JL, Tiller GE (2012) Synaptosomal-associated protein, 25-KD; SNAP25. http://www.omim.org/entry/600322. Accessed 30 Dec 2014

  36. Bark IC, Hahn KM, Ryabinin AE, Wilson MC (1995) Differential expression of SNAP-25 protein isoforms during divergent vesicle fusion events of neural development. Proc Natl Acad Sci USA 92(5):1510–1514

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Aguado F, Majó G, Ruiz-Montasell B, Canals JM, Casanova A, Marsal J, Blasi J (1996) Expression of synaptosomal-associated protein SNAP-25 in endocrine anterior pituitary cells. Eur J Cell Biol 69(4):351–359

    PubMed  CAS  Google Scholar 

  38. Majó G, Ferrer I, Marsal J, Blasi J, Aguado F (1997) Immunocytochemical analysis of the synaptic proteins SNAP-25 and Rab3A in human pituitary adenomas. Overexpression of SNAP-25 in the mammmosomatotroph lineages. J Pathol 183(4):440–446

    Article  PubMed  Google Scholar 

  39. Rotondo F, Kovacs K, Scheithauer BW, Horvath E, Bell CD, Lloyd RV, Cusimano M (2008) Immunohistochemical expression of SNAP-25 protein in adenomas of the human pituitary. Appl Immunohistochem Mol Morphol 16(5):477–481

    Article  PubMed  CAS  Google Scholar 

  40. Arsenault J, Ferrari E, Niranjan D, Cuijpers SA, Gu C, Vallis Y, O’Brien J, Davletov B (2013) Stapling of the botulinum type A protease to growth factors and neuropeptides allows selective targeting of neuroendocrine cells. J Neurochem 126(2):223–233

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Converse PJ, Hartz PA, Phillips JA (2008) Uridine diphosphate glycosyltransferase 2 family, member B7; UGT2B7. http://omim.org/entry/600068. Accessed 30 Dec 2014

  42. Ouzzine M, Gulberti S, Ramalanjaona N, Magdalou J, Fournel-Gigleux S (2014) The UDP-glucuronosyltransferases of the blood-brain barrier: their role in drug metabolism and detoxication. Front Cell Neurosci 8:349

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Jiang Z, Gui S, Zhang Y (2011) Analysis of differential gene expression using fiber-optic bead array and pathway analyses in pituitary adenomas. J Clin Neurosci 18(10):1386–1391

    Article  PubMed  CAS  Google Scholar 

  44. Heaney AP, Horwitz GA, Wang Z, Singson R, Melmed S (1999) Early involvement of estrogen-induced pituitary tumor transforming gene and fibroblast growth factor expression in prolactinoma pathogenesis. Nat Med 5(11):1317–1321

    Article  PubMed  CAS  Google Scholar 

  45. Garcia MM, Kapcala LP (1995) Growth of a microprolactinoma to a macroprolactinoma during estrogen therapy. J Endocrinol Invest 18(6):450–455

    Article  PubMed  CAS  Google Scholar 

  46. Michaelis KA, Knox AJ, Xu M, Kiseljak-Vassiliades K, Edwards MG, Geraci M, Kleinschmidt-DeMasters BK, Lillehei KO, Wierman ME (2011) Identification of growth arrest and DNA-damage-inducible gene beta (GADD45beta) as a novel tumor suppressor in pituitary gonadotrope tumors. Endocrinology 152(10):3603–3613

    Article  PubMed  CAS  Google Scholar 

  47. Li XH, Wang EL, Zhou HM, Yoshimoto K, Qian ZR (2014) MicroRNAs in human pituitary adenomas. Int J Endocrinol 2014:435171

    PubMed  PubMed Central  Google Scholar 

  48. Chapman CG, Pekow J (2015) The emerging role of miRNAs in inflammatory bowel disease: a review. Therap Adv Gastroeneterol 8(1):4–22

    Article  CAS  Google Scholar 

  49. Babashah S (2014) MicroRNAs: key regulators of oncogenesis. Springer International Publishing, New York

    Book  Google Scholar 

  50. Hamosh A, Antonarakis SE, McKusick VA, Hartz PA, Converse PJ (2014) Micro RNA LET7A1; MIRLET7A1. http://www.omim.org/entry/605386. Accessed 30 Dec 2014

  51. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T (2001) Identification of novel genes coding for small expressed RNAs. Science 294(5543):853–858

    Article  PubMed  CAS  Google Scholar 

  52. 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(2):370–377

    Article  PubMed  CAS  Google Scholar 

  53. Righi A, Morandi L, Leonardi E, Farnedi A, Marucci G, Sisto A, Frank G, Faustini-Fustini M, Zoli M, Mazzatenta D, Agati R, Foschini MP (2013) Galectin-3 expression in pituitary adenomas as a marker of aggressive behavior. Hum Pathol 44(11):2400–2409

    Article  PubMed  CAS  Google Scholar 

  54. Dai D, Li Y, Lu Q, Yu L, Min W, Wang L, Cao Y, Yue Z (2014) GAL3 protein expression is related to clinical features of prolactin-secreting pituitary microadenoma and predicts its recurrence after surgical treatment. Cell Physiol Biochem 33(4):1026–1035

    Article  PubMed  CAS  Google Scholar 

  55. Akinci H, Kapucu A, Dar KA, Celik O, Tutunculer B, Sirin G, Oz B, Gazioglu N, Ince H, Aliustaoglu S, Kadioglu P (2013) Aromatase cytochrome P450 enzyme expression in prolactinomas and its relationship to tumor behavior. Pituitary 16(3):386–392

    Article  PubMed  CAS  Google Scholar 

  56. Aletsee-Ufrecht MC, Langley K, Gratzl O, Gratzl M (1990) Differential expression of the neural cell adhesion molecule NCAM 140 in human pituitary tumors. FEBS Lett 272(1–2):45–49

    Article  PubMed  CAS  Google Scholar 

  57. Asa SL, Puy LA, Lew AM, Sundmark VC, Elsholtz HP (1993) Cell type-specific expression of the pituitary transcription activator pit-1 in the human pituitary and pituitary adenomas. J Clin Endocrinol Metab 77(5):1275–1280

    PubMed  CAS  Google Scholar 

  58. 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(1):280–285

    Article  PubMed  CAS  Google Scholar 

  59. Chile T, Corrêa-Giannella ML, Fortes MA, Bronstein MD, Cunha-Neto MB, Giannella-Neto D, Giorgi RR (2011) Expression of CRABP1, GRP, and RERG mRNA in clinically non-functioning and functioning pituitary adenomas. J Endocrinol Invest 34(8):e214–e218

    PubMed  CAS  Google Scholar 

  60. Delhase M, Vergani P, Malur A, Velkeniers B, Teugels E, Trouillas J, Hooghe-Peters EL (1993) Pit-1/GHF-1 expression in pituitary adenomas: further analogy between human adenomas and rat SMtTW tumours. J Mol Endocrinol 11(2):129–139

    Article  PubMed  CAS  Google Scholar 

  61. Evans CO, Yao C, Laborde D, Oyesiku NM (2008) Folate receptor expression in pituitary adenomas cellular and molecular analysis. Vitam Horm 79:235–266

    Article  PubMed  CAS  Google Scholar 

  62. Fratticci A, Grieco FA, Spilioti C, Giangaspero F, Ventura L, Esposito V, Piccirilli M, Santoro A, Gulino A, Cantore G, Alesse E, Jaffrain-Rea ML (2007) Differential expression of neurogenins and NeuroD1 in human pituitary tumours. J Endocrinol 194(3):475–484

    Article  PubMed  CAS  Google Scholar 

  63. Friend KE, Chiou YK, Laws ER Jr, Lopes MB, Shupnik MA (1993) Pit-1 messenger ribonucleic acid is differentially expressed in human pituitary adenomas. J Clin Endocrinol Metab 77(5):1281–1286

    PubMed  CAS  Google Scholar 

  64. Friend KE, Chiou YK, Laws ER Jr, Lopes MB, Shupnik MA (1994) Estrogen receptor expression in human pituitary: correlation with immunohistochemistry in normal tissue, and immunohistochemistry and morphology in macroadenomas. J Clin Endocrinol Metab 78(6):1497–1504

    PubMed  CAS  Google Scholar 

  65. Giorgi RR, Chile T, Bello AR, Reyes R, Fortes MA, Machado MC, Cescato VA, Musolino NR, Bronstein MD, Giannella-Neto D, Corrêa-Giannella ML (2008) Expression of neurotensin and its receptors in pituitary adenomas. J Neuroendocrinol 20(9):1052–1057

    Article  PubMed  CAS  Google Scholar 

  66. Hossain MG, Iwata T, Mizusawa N, Qian ZR, Shima SW, Okutsu T, Yamada S, Sano T, Yoshimoto K (2009) Expression of p18(INK4C) is down-regulated in human pituitary adenomas. Endocr Pathol 20(2):114–121

    Article  PubMed  CAS  Google Scholar 

  67. Jiang Z, Gui S, Zhang Y (2010) Analysis of differential gene expression by fiber-optic BeadArray and pathway in prolactinomas. Endocrine 38(3):360–368

    Article  PubMed  CAS  Google Scholar 

  68. La Rosa S, Uccella S, Dainese L, Marchet S, Placidi C, Vigetti D, Capella C (2008) Characterization of c-kit (CD117) expression in human normal pituitary cells and pituitary adenomas. Endocr Pathol 19(2):104–111

    Article  PubMed  CAS  Google Scholar 

  69. La Rosa S, Vigetti D, Placidi C, Finzi G, Uccella S, Clerici M, Bartolini B, Carnevali I, Losa M, Capella C (2010) Localization of carboxyl ester lipase in human pituitary gland and pituitary adenomas. J Histochem Cytochem 58(10):881–889

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Lange M, Pagotto U, Hopfner U, Ehrenreich H, Oeckler R, Sinowatz F, Stalla GK (1994) Endothelin expression in normal human anterior pituitaries and pituitary adenomas. J Clin Endocrinol Metab 79(6):1864–1870

    PubMed  CAS  Google Scholar 

  71. Lloyd RV, Jin L, Chandler WF, Horvath E, Stefaneanu L, Kovacs K (1993) Pituitary specific transcription factor messenger ribonucleic expression in adenomatous and nontumorous human pituitary tissues. Lab Invest 69(5):570–575

    PubMed  CAS  Google Scholar 

  72. Lloyd RV, Jin L, Qian X, Scheithauer BW, Young WF Jr, Davis DH (1995) Analysis of the chromogranin A post-translational cleavage product pancreastatin and the prohormone convertases PC2 and PC3 in normal and neoplastic human pituitaries. Am J Pathol 146(5):1188–1198

    PubMed  PubMed Central  CAS  Google Scholar 

  73. Martínez-Fuentes AJ, Molina M, Vázquez-Martínez R, Gahete MD, Jiménez-Reina L, Moreno-Fernández J, Benito-López P, Quintero A, de la Riva A, Diéguez C, Soto A, Leal-Cerro A, Resmini E, Webb SM, Zatelli MC, degli Uberti EC, Malagón MM, Luque RM, Castaño JP (2011) Expression of functional KISS1 and KISS1R system is altered in human pituitary adenomas: evidence for apoptotic action of kisspeptin-10. Eur J Endocrinol 164(3):355–362

    Article  PubMed  CAS  Google Scholar 

  74. Miyakoshi T, Takei M, Kajiya H, Egashira N, Takekoshi S, Teramoto A, Osamura RY (2008) Expression of Wnt4 in human pituitary adenomas regulates activation of the beta-catenin-independent pathway. Endocr Pathol 19(4):261–273

    Article  PubMed  CAS  Google Scholar 

  75. Morris DG, Musat M, Czirják S, Hanzély Z, Lillington DM, Korbonits M, Grossman AB (2005) Differential gene expression in pituitary adenomas by oligonucleotide array analysis. Eur J Endocrinol 153(1):143–151

    Article  PubMed  CAS  Google Scholar 

  76. Musat M, Korbonits M, Kola B, Borboli N, Hanson MR, Nanzer AM, Grigson J, Jordan S, Morris DG, Gueorguiev M, Coculescu M, Basu S, Grossman AB (2005) Enhanced protein kinase B/Akt signalling in pituitary tumours. Endocr Relat Cancer 12(2):423–433

    Article  PubMed  CAS  Google Scholar 

  77. Occhi G, Albiger N, Berlucchi S, Gardiman M, Scanarini M, Scienza R, Fassina A, Mantero F, Scaroni C (2007) Peroxisome proliferator-activated receptor gamma in the human pituitary gland: expression and splicing pattern in adenomas versus normal pituitary. J Neuroendocrinol 19(7):552–559

    Article  PubMed  CAS  Google Scholar 

  78. Pellegrini I, Barlier A, Gunz G, Figarella-Branger D, Enjalbert A, Grisoli F, Jaquet P (1994) Pit-1 gene expression in the human pituitary and pituitary adenomas. J Clin Endocrinol Metab 79(1):189–196

    PubMed  CAS  Google Scholar 

  79. Pellegrini-Bouiller I, Manrique C, Gunz G, Grino M, Zamora AJ, Figarella-Branger D, Grisoli F, Jaquet P, Enjalbert A (1999) Expression of the members of the Ptx family of transcription factors in human pituitary adenomas. J Clin Endocrinol Metab 84(6):2212–2220

    PubMed  CAS  Google Scholar 

  80. Perez-Millan MI, Berner SI, Luque GM, De Bonis C, Sevlever G, Becu-Villalobos D, Cristina C (2013) Enhanced nestin expression and small blood vessels in human pituitary adenomas. Pituitary 16(3):303–310

    Article  PubMed  CAS  Google Scholar 

  81. Rabbitt EH, Ayuk J, Boelaert K, Sheppard MC, Hewison M, Stewart PM, Gittoes NJ (2003) Abnormal expression of 11 beta-hydroxysteroid dehydrogenase type 2 in human pituitary adenomas: a prereceptor determinant of pituitary cell proliferation. Oncogene 22(11):1663–1667

    Article  PubMed  CAS  Google Scholar 

  82. Raica M, Coculescu M, Cimpean AM, Ribatti D (2010) Endocrine gland derived-VEGF is down-regulated in human pituitary adenoma. Anticancer Res 30(10):3981–3986

    PubMed  Google Scholar 

  83. Revill K, Dudley KJ, Clayton RN, McNicol AM, Farrell WE (2009) Loss of neuronatin expression is associated with promoter hypermethylation in pituitary adenoma. Endocr Relat Cancer 16(2):537–548

    Article  PubMed  CAS  Google Scholar 

  84. Rezai AR, Rezai A, Martínez-Maza O, Vander-Meyden M, Weiss MH (1994) Interleukin-6 and interleukin-6 receptor gene expression in pituitary tumors. J Neurooncol 19(2):131–135

    Article  PubMed  CAS  Google Scholar 

  85. Righi A, Zhang S, Jin L, Scheithauer BW, Kovacs K, Kovacs G, Goth MI, Korbonits M, Lloyd RV (2010) Analysis of IMP3 expression in normal and neoplastic human pituitary tissues. Endocr Pathol 21(1):25–31

    Article  PubMed  CAS  Google Scholar 

  86. Riss D, Jin L, Qian X, Bayliss J, Scheithauer BW, Young WF Jr, Vidal S, Kovacs K, Raz A, Lloyd RV (2003) Differential expression of galectin-3 in pituitary tumors. Cancer Res 63(9):2251–2255

    PubMed  CAS  Google Scholar 

  87. Sanno N, Jin L, Qian X, Osamura RY, Scheithauer BW, Kovacs K, Lloyd RV (1997) Gonadotropin-releasing hormone and gonadotropin-releasing hormone receptor messenger ribonucleic acids expression in nontumorous and neoplastic pituitaries. J Clin Endocrinol Metab 82(6):1974–1982

    PubMed  CAS  Google Scholar 

  88. Stilling G, Sun Z, Zhang S, Jin L, Righi A, Kovācs G, Korbonits M, Scheithauer BW, Kovacs K, Lloyd RV (2010) MicroRNA expression in ACTH-producing pituitary tumors: up-regulation of microRNA-122 and -493 in pituitary carcinomas. Endocrine 38(1):67–75

    Article  PubMed  CAS  Google Scholar 

  89. Tampanaru-Sarmesiu A, Stefaneanu L, Thapar K, Kontogeorgos G, Sumi T, Kovacs K (1998) Transferrin and transferrin receptor in human hypophysis and pituitary adenomas. Am J Pathol 152(2):413–422

    PubMed  PubMed Central  CAS  Google Scholar 

  90. Tannahill LA, Visser TJ, McCabe CJ, Kachilele S, Boelaert K, Sheppard MC, Franklyn JA, Gittoes NJ (2002) Dysregulation of iodothyronine deiodinase enzyme expression and function in human pituitary tumours. Clin Endocrinol (Oxf) 56(6):735–743

    Article  CAS  Google Scholar 

  91. Theodoropoulou M, Cavallari I, Barzon L, D’Agostino DM, Ferro T, Arzberger T, Grübler Y, Schaaf L, Losa M, Fallo F, Ciminale V, Stalla GK, Pagotto U (2004) Differential expression of menin in sporadic pituitary adenomas. Endocr Relat Cancer 11(2):333–344

    Article  PubMed  CAS  Google Scholar 

  92. Turner HE, Nagy Z, Sullivan N, Esiri MM, Wass JA (2000) Expression analysis of cyclins in pituitary adenomas and the normal pituitary gland. Clin Endocrin (Oxf) 53(3):337–344

    Article  CAS  Google Scholar 

  93. Wang DG, Johnston CF, Atkinson AB, Heaney AP, Mirakhur M, Buchanan KD (1996) Expression of bcl-2 oncoprotein in pituitary tumours: comparison with c-myc. J Clin Pathol 49(10):795–797

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  94. Wasko R, Jaskula M, Kotwicka M, Andrusiewicz M, Jankowska A, Liebert W, Sowinski J (2008) The expression of ghrelin in somatotroph and other types of pituitary adenomas. Neuro Endocrinol Lett 29(6):929–938

    PubMed  CAS  Google Scholar 

  95. Xu Y, Wang Y, Ma G, Wang Q, Wei G (2014) CUL4A is overexpressed in human pituitary adenomas and regulates pituitary tumor cell proliferation. J Neuroncol 116(3):625–632

    Article  CAS  Google Scholar 

  96. Yuan Y, Qian ZR, Sano T, Asa SL, Yamada S, Kagawa N, Kudo E (2008) Reduction of GSTP1 expression by DNA methylation correlates with clinicopathological features in pituitary adenomas. Mod Pathol 21(7):856–865

    Article  PubMed  CAS  Google Scholar 

  97. Zhang X, Horwitz GA, Heaney AP, Nakashima M, Prezant TR, Bronstein MD, Melmed S (1999) Pituitary tumor transforming gene (PTTG) expression in pituitary adenomas. J Clin Endocrinol Metab 84(2):761–767

    Article  PubMed  CAS  Google Scholar 

  98. Zhang X, Sun H, Danila DC, Johnson SR, Zhou Y, Swearingen B, Klibanski A (2002) Loss of expression of GADD45 gamma, a growth inhibitory gene, in human pituitary adenomas: implications for tumorigenesis. J Clin Endocrinol Metab 87(3):1262–1267

    PubMed  CAS  Google Scholar 

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Acknowledgments

Dr. Carmichael has served as a consultant for Novartis and has received non-study-related clinical or research support from Novartis.

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Correspondence to Justin Seltzer.

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The other authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

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Seltzer, J., Scotton, T.C., Kang, K. et al. Gene expression in prolactinomas: a systematic review. Pituitary 19, 93–104 (2016). https://doi.org/10.1007/s11102-015-0674-1

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