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Critical Reviews™ in Eukaryotic Gene Expression
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ISSN En Línea: 2162-6502

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Critical Reviews™ in Eukaryotic Gene Expression

DOI: 10.1615/CritRevEukaryotGeneExpr.2020029243
pages 153-168

The Identification of Key Gene Expression Signature in Prostate Cancer

Yu Huang
Department of Urology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
Qi Cao
Department of Urology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
Zhengshuai Song
Department of Urology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
Hailong Ruan
Department of Urology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
Keshan Wang
Department of Urology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
Ke Chen
Department of Urology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
Xiaoping Zhang
Department of Urology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China

SINOPSIS

Prostate cancer (PCa) is one of the most common malignancies affecting men's health worldwide. The aim of this study is to identify key genes and their regulatory networks and evaluate the usefulness of these genes on diagnosis of and prognosis for prostate cancer. The gene expression microarray dataset GSE55945 was downloaded for analysis. The differentially expressed genes (DEGs) were accessed with RStudio. Gene ontology (GO) and the Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses were performed using the database for annotation, visualization and integrated discovery (DAVID) database. A protein-protein interaction network was carried out using STRING. The survival and diagnostic analysis of hub genes were conducted using the cancer genome atlas (TCGA) data. Finally, we identified 387 DEGs. GO and KEGG analyses reveled that the DEGs in PCa were mainly enriched in the bone morphogenetic protein (BMP) signaling pathway and cytochrome P450. Among 15 hub genes, we found that only a different expression level of MYH11 affected patient survival. And further gene set enrichment analysis (GSEA) showed that low expression of MYH11 was associated with the cell cycle, DNA replication, TGF-P1 signal pathway, and PCa. In conclusion, we identified 387 DEGs that may be involved in core pathways such as the BMP pathway and cytochrome P450, which may contribute to the progression of PCa. In addition, hub gene MYH11 has the potential to be a novel biomarker for diagnosing and determining the prognosis for PCa.

PALABRAS CLAVE: MYH11, biomarker, survival

REFERENCIAS

  1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin. 2018;68(1):7-30.

  2. Wang T, Song W, Chen Y, Chen R, Liu Z, Wu L, Li M, Yang J, Wang L, Liu J, Ye Z, Wang C, Chen K. Flightless I homolog represses prostate cancer progression through targeting androgen receptor signaling. Clin Cancer Res. 2016;22(6):1531-44.

  3. Al Olama AA, Kote-Jarai Z, Berndt SI, Conti DV, Schumacher F, Han Y, Benlloch S, Hazelett DJ, Wang Z, Saunders E, Leongamornlert D, Lindstrom S, Jugurnauth-Little S, Dadaev T, Tymrakiewicz M, Stram DO, Rand K, Wan P, Stram A, Sheng X, Pooler LC, Park K, Xia L, Tyrer J, Kolonel LN, Le Marchand L, Hoover RN, Machiela MJ, Yeager M, Burdette L, Chung CC, Hutchinson A, Yu K, Goh C, Ahmed M, Govindasami K, Guy M, Tammela TL, Auvinen A, Wahlfors T, Schleutker J, Visakorpi T, Leinonen, KA, Xu J, Aly M, Donovan J, Travis RC, Key TJ, Siddiq A, Canzian F, Khaw KT, Takahashi A, Kubo M, Pharoah P, Pashayan N, Weischer M, Nordestgaard BG, Nielsen SF, Klarskov P, Roder MA, Iversen P, Thibodeau SN, McDonnell SK, Schaid DJ, Stanford JL, Kolb S, Holt S, Knudsen B, Coll AH, Gapstur SM, Diver WR, Stevens VL, Maier C, Luedeke M, Herkommer K, Rinckleb AE, Strom SS, Pettaway C, Yeboah ED, Tettey Y, Biritwum RB, Adjei AA, Tay E, Truelove A, Niwa S, Chokkalingam AP, Cannon-Albright L, Cybulski C, Wokolorczyk D, Kluzniak W, Park J, Sellers T, Lin HY, Isaacs WB, Partin AW, Brenner H, Dieffenbach AK, Stegmaier C, Chen C, Giovannucci EL, Ma J, Stampfer M, Penney KL, Mucci L, John EM, Ingles SA, Kittles RA, Murphy AB, Pandha H, Michael A, Kierzek AM, Blot W, Signorello LB, Zheng W, Albanes D, Virtamo J, Weinstein S, Nemesure B, Carpten J, Leske C, Wu SY, Hennis A, Kibel AS, Rybicki BA, Neslund-Dudas C, Hsing AW, Chu L, Goodman PJ, Klein EA, Zheng SL, Batra J, Clements J, Spurdle A, Teixeira MR, Paulo P, Maia S, Slavov C, Kaneva R, Mitev V, Witte JS, Casey G, Gillanders EM, Seminara D, Riboli E, Hamdy FC, Coetzee GA, Li Q, Freedman ML, Hunter DJ, Muir K, Gronberg H, Neal DE, Southey M, Giles GG, Severi G, Cook MB, Nakagawa H, Wiklund F, Kraft P, Chanock SJ, Henderson BE, Easton DF, Eeles RA, Haiman CA. A meta-analysis of 87,040 individuals identifies 23 new susceptibility loci for prostate cancer. Nat Genet. 2014;46(10):1103-9.

  4. Penney KL, Stampfer MJ, Jahn JL, Sinnott JA, Flavin R, Rider JR, Finn S, Giovannucci E, Sesso HD, Loda M, Mucci LA, Fiorentino M. Gleason grade progression is uncommon. Cancer Res. 2013;73(16):5163-8.

  5. D'Amico AV, Whittington R, Malkowicz SB, Schultz D, Blank K, Broderick GA, Tomaszewski JE, Renshaw AA, Kaplan I, Beard CJ, Wein A. Biochemical outcome after radical prostatectomy, external beam radiation therapy, or interstitial radiation therapy for clinically localized prostate cancer. JAMA. 1998;280(11):969-74.

  6. Cooperberg MR, Broering JM, Carroll PR. Risk assessment for prostate cancer metastasis and mortality at the time of diagnosis. J Natl Cancer Inst. 2009;101(12):878-87.

  7. Cucchiara V, Cooperberg MR, Dall'Era M, Lin DW, Montorsi F, Schalken JA, Evans CP. Genomic markers in prostate cancer decision making. Eur Urol. 2018;73(4):572-82.

  8. Robinson D, Van Allen EM, Wu YM, Schultz N, Lonigro RJ, Mosquera JM, Montgomery B, Taplin ME, Pritchard CC, Attard G, Beltran H, Abida W, Bradley RK, Vinson J, Cao X, Vats P, Kunju LP, Hussain M, Feng FY, Tom- lins SA, Cooney KA, Smith DC, Brennan C, Siddiqui J, Mehra R, Chen Y, Rathkopf DE, Morris MJ, Solomon SB, Durack JC, Reuter VE, Gopalan A, Gao J, Loda M, Lis RT, Bowden M, Balk SP, Gaviola G, Sougnez C, Gupta M, Yu EY, Mostaghel EA, Cheng HH, Mulcahy H, True LD, Plymate SR, Dvinge H, Ferraldeschi R, Flohr P, Miranda S, Zafeiriou Z, Tunariu N, Mateo J, Perez-Lopez R, Demi- chelis F, Robinson BD, Schiffman M, Nanus DM, Tagawa ST, Sigaras A, Eng KW, Elemento O, Sboner A, Heath EI, Scher HI, Pienta KJ, Kantoff P, de Bono JS, Rubin MA, Nelson PS, Garraway LA, Sawyers CL, Chinnaiyan AM. Integrative clinical genomics of advanced prostate cancer. Cell. 2015;161(5):1215-28.

  9. Affolter VK. Dermatopathology - the link between ancillary techniques and clinical lesions. Vet Dermatol. 2017;28(1):134-e28.

  10. Abeshouse A, Ahn J, Akbani R, Ally A, Amin S, Andry CD, Annala M, Aprikian A, Armenia J, Arora A, Auman JT. The molecular taxonomy of primary prostate cancer. Cell. 2015;163(4):1011-25.

  11. Massague J. How cells read TGF-P signals. Nat Rev Mol Cell Biol. 2000;1(3):169-78.

  12. Huminiecki L, Goldovsky L, Freilich S, Moustakas A, Ouzounis C, Heldin CH. Emergence, development and diversification of the TGF-P signalling pathway within the animal kingdom. BMC Evol Biol. 2009;9:28.

  13. Gratchev A. TGF-P signalling in tumour associated macrophages. Immunobiology. 2017;222(1):75-81.

  14. Carreira AC, Lojudice FH, Halcsik E, Navarro RD, Sogayar MC, Granjeiro JM. Bone morphogenetic proteins: Facts, challenges, and future perspectives. J Dent Res. 2014;93(4):335-45.

  15. Lissenberg-Thunnissen SN, de Gorter DJ, Sier CF, Schipper IB. Use and efficacy of bone morphogenetic proteins in fracture healing. Int Orthop. 2011;35(9):1271-80.

  16. Lowery JW, de Caestecker MP. BMP signaling in vascular development and disease. Cytokine Growth Factor Rev. 2010;21(4):287-98.

  17. Wang S, Chen YG. BMP signaling in homeostasis, transformation and inflammatory response of intestinal epithelium. Sci China Life Sci. 2018;61(7):800-7.

  18. Zhang YE. Non-Smad pathways in TGF-beta signaling. Cell Res. 2009;19(1):128-39.

  19. Tang Y, Xie H, Chen J, Geng L, Chen H, Li X, Hou Y, Lu L, Shi S, Zeng X, Sun L. Activated NF-KB in bone marrow mesenchymal stem cells from systemic lupus erythematosus patients inhibits osteogenic differentiation through downregulating Smad signaling. Stem Cells Dev. 2013;22(4):668-78.

  20. Moustakas A, Heldin CH. Non-Smad TGF-P signals. J Cell Sci. 2005;118(Pt 16):3573-84.

  21. Zhang L, Ye Y, Long X, Xiao P, Ren X, Yu J. BMP signaling and its paradoxical effects in tumorigenesis and dissemination. Oncotarget. 2016;7(47):78206-18.

  22. Maegdefrau U, Bosserhoff AK. BMP activated Smad signaling strongly promotes migration and invasion of hepatocellular carcinoma cells. Exp Mol Pathol. 2012;92(1):74-81.

  23. Fei ZH, Yao CY, Yang XL, Huang XE, Ma SL. Serum BMP-2 up-regulation as an indicator of poor survival in advanced non-small cell lung cancer patients. Asian Pac J Cancer Prev. 2013;14(9):5293-9.

  24. Motoyama K, Tanaka F, Kosaka Y, Mimori K, Uetake H, Inoue H, Sugihara K, Mori M. Clinical significance of BMP7 in human colorectal cancer. Ann Surg Oncol. 2008;15(5):1530-7.

  25. Chen J, Ye L, Xie F, Yang Y, Zhang L, Jiang WG. Expression of bone morphogenetic protein 7 in lung cancer and its biological impact on lung cancer cells. Anticancer Res. 2010;30(4):1113-20.

  26. Basic-Jukic N, Hudolin T, Radic-Antolic M, Coric M, Zadro R, Kastelan Z, Pasini J, Bandic-Pavlovic D, Kes P. Bone morphogenetic protein-7 expression is down-regulated in human clear cell renal carcinoma. J Nephrol. 2011;24(1):91-7.

  27. Megumi K, Ishigami S, Uchikado Y, Kita Y, Okumura H, Matsumoto M, Uenosono Y, Arigami T, Kijima Y, Kitazono M, Shinchi H, Ueno S, Natsugoe S. Clinicopathological significance of BMP7 expression in esophageal squamous cell carcinoma. Ann Surg Oncol. 2012;19(6): 2066-71.

  28. Herrera B, Garcia-Alvaro M, Cruz S, Walsh P, Fernandez M, Roncero C, Fabregat I, Sanchez A, Inman GJ. BMP9 is a proliferative and survival factor for human hepatocellular carcinoma cells. PLoS One. 2013;8(7):e69535.

  29. Chen JC, Yang ST, Lin CY, Hsu CJ, Tsai CH, Su JL,Tang CH. BMP-7 enhances cell migration and avp3 integrin expression via a c-Src-dependent pathway in human chondrosarcoma cells. PLoS One. 2014;9(11):e112636.

  30. Peng J, Yoshioka Y, Mandai M, Matsumura N, Baba T, Yamaguchi K, Hamanishi J, Kharma B, Murakami R, Abiko K, Murphy SK, Konishi I. The BMP signaling pathway leads to enhanced proliferation in serous ovarian cancer-a potential therapeutic target. Mol Carcinog. 2016;55(4):335-45.

  31. Holtzhausen A, Golzio C, How T, Lee YH, Schiemann WP, Katsanis N, Blobe GC. Novel bone morphogenetic protein signaling through Smad2 and Smad3 to regulate cancer progression and development. FASEB J. 2014;28(3):1248-67.

  32. Zheng Y, Wang X, Wang H, Yan W, Zhang Q, Chang X. Bone morphogenetic protein 2 inhibits hepatocellular carcinoma growth and migration through down-regulation of the PI3K/AKT pathway. Tumour Biol. 2014;35(6):5189-98.

  33. Yeh LC. In vitro and in vivo studies on the effects of bone morphogenetic protein-7 on human kidney and lung tumor cells. Int J Biomed Sci. 2010;6(3):176-81.

  34. Tsuchida R, Osawa T, Wang F, Nishii R, Das B, Tsuchida S, Muramatsu M, Takahashi T, Inoue T, Wada Y, Minami T, Yuasa Y, Shibuya M. BMP4/Thrombospondin-1 loop paracrinically inhibits tumor angiogenesis and suppresses the growth of solid tumors. Oncogene. 2014;33(29):3803-11.

  35. Barnes J, Anthony CT, Wall N, Steiner MS. Bone morphogenetic protein-6 expression in normal and malignant prostate. World J Urol. 1995;13(6):337-43.

  36. Ye L, Lewis-Russell JM, Kynaston H, Jiang WG. Endogenous bone morphogenetic protein-7 controls the motility of prostate cancer cells through regulation of bone morphogenetic protein antagonists. J Urol. 2007;178(3 Pt 1):1086-91.

  37. Kobayashi A, Okuda H, Xing F, Pandey PR, Watabe M, Hirota S, Pai SK, Liu W, Fukuda K, Chambers C, Wilber A, Watabe K. Bone morphogenetic protein 7 in dormancy and metastasis of prostate cancer stem-like cells in bone. J Exp Med. 2011;208(13):2641-55.

  38. Lim M, Chuong CM, Roy-Burman P. PI3K, Erk signaling in BMP7-induced epithelial-mesenchymal transition (EMT) of PC-3 prostate cancer cells in 2- and 3-dimensional cultures. Horm Cancer. 2011;2(5):298-309.

  39. Dai J, Kitagawa Y, Zhang J, Yao Z, Mizokami A, Cheng S, Nor J, McCauley LK, Taichman RS, Keller ET. Vascular endothelial growth factor contributes to the prostate cancer-induced osteoblast differentiation mediated by bone morphogenetic protein. Cancer Res. 2004;64(3):994-9.

  40. Ye L, Kynaston H, Jiang WG. Bone morphogenetic protein-9 induces apoptosis in prostate cancer cells, the role of prostate apoptosis response-4. Mol Cancer Res. 2008;6(10):1594-606.

  41. Le Beau MM, Larson RA, Bitter MA, Vardiman JW, Golomb HM, Rowley JD. Association of an inversion of chromosome 16 with abnormal marrow eosinophils in acute myelomonocytic leukemia-a unique cytogenetic-clinicopathological association. N Engl J Med. 1983;309(11):630-6.

  42. Albano F, Anelli L, Zagaria A, Coccaro N, Tota G, Impera L, Minervini CF, Cellamare A, Delia M, Minervini A, Casieri P, Specchia G. Acute myeloid leukemia with t(16;16) (p13;q22) showing a new CBFB-MYH11 fusion transcript associated with an atypical leukemic blasts morphology. Hum Pathol. 2014;45(3):643-7.

  43. Hyde RK, Zhao L, Alemu L, Liu PP. Runx1 is required for hematopoietic defects and leukemogenesis in Cb-fb-MYH11 knock-in mice. Leukemia. 2015;29(8):1771-8.

  44. Douet-Guilbert N, Chauveau A, Gueganic N, Guillerm G, Tous C, Le Bris MJ, Basinko A, Morel F, Ugo V, De Braekeleer M. Acute myeloid leukaemia (FAB AML- M4Eo) with cryptic insertion of cbfb resulting in cb-fb-Myh11 fusion. Hematol Oncol. 2017;35(3):385-9.

  45. Jo YS, Kim MS, Yoo NJ, Lee SH. Somatic mutations and intratumoral heterogeneity of MYH11 gene in gastric and colorectal cancers. Appl Immunohistochem Mol Morphol. 2018;26(8):562-6.

  46. Wang RJ, Wu P, Cai GX, Wang ZM, Xu Y, Peng JJ, Sheng WQ, Lu HF, Cai SJ. Down-regulated MYH11 expression correlates with poor prognosis in stage II and III colorectal cancer. Asian Pac J Cancer Prev. 2014;15(17):7223-8.

  47. Alhopuro P, Karhu A, Winqvist R, Waltering K, Visakorpi T, Aaltonen LA. Somatic mutation analysis of MYH11 in breast and prostate cancer. BMC Cancer. 2008;8:263.

  48. Popova AP, Bozyk PD, Goldsmith AM, Linn MJ, Lei J, Bentley JK, Hershenson MB. Autocrine production of TGF-P1 promotes myofibroblasts differentiation of neo-natal lung mesenchymal stem cells. Am J Physiol Lung Cell Mol Physiol. 2010;298(6):L735-43.

  49. Jiao J, Xiong W, Wang L, Yang J, Qiu P, Hirai H, Shao L, Milewicz D, Chen YE, Yang B. Differentiation defect in neural crest-derived smooth muscle cells in patients with aortopathy associated with bicuspid aortic valves. EBio-Medicine. 2016;10:282-90.

  50. Renard M, Callewaert B, Baetens M, Campens L, Mac-Dermot K, Fryns JP, Bonduelle M, Dietz HC, Gaspar IM, Cavaco D, Stattin EL, Schrander-Stumpel C, Coucke P, Loeys B, De Paepe A, De Backer J. Novel MYH11 and ACTA2 mutations reveal a role for enhanced TGFp signaling in FTAAD. Int J Cardiol. 2013;165(2):314-21.

  51. Herring BP, Hoggatt AM, Griffith SL, McClintick JN, Gallagher PJ. Inflammation and vascular smooth muscle cell dedifferentiation following carotid artery ligation. Physiol Genomics. 2017;49(3):115-26.

  52. Rais-Bahrami S, Siddiqui MM, Vourganti S, Turkbey B, Rastinehad AR, Stamatakis L, Truong H, Walton-Diaz A, Hoang AN, Nix JW, Merino MJ, Wood BJ, Simon RM, Choyke PL, Pinto PA. Diagnostic value of bipara-metric magnetic resonance imaging (MRI) as an adjunct to prostate-specific antigen (PSA)-based detection of prostate cancer in men without prior biopsies. BJU Int. 2015;115(3):381-8.

  53. Chen R, Xie L, Cai X, Huang Y, Zhou L, Ma L, Gao X, Xu C, Ren S, Shao P, Xu D, Xu K, Ye Z, Liu C, Ye D, Lu L, Fu Q, Hou J, Yuan J, He D, Zhou T, Wang F, He B, Sun Y. Percent free prostate-specific antigen for prostate cancer diagnosis in Chinese men with a PSA of 4.0-10.0 ng/mL: Results from the Chinese Prostate Cancer Consortium. Asian J Urol. 2015;2(2):107-13.

  54. Chistiakov DA, Myasoedova VA, Grechko AV, Melnichenko AA, Orekhov AN. New biomarkers for diagnosis and prognosis of localized prostate cancer. Semin Cancer Biol. 2018;52(Pt 1):9-16.

  55. Pepe P, Fraggetta F, Galia A, Skonieczny G, Aragona F. PCA3 score and prostate cancer diagnosis at repeated saturation biopsy. Which cut-off: 20 or 35? Int Braz J Urol. 2012;38(4):489-95.

  56. Tomlins SA, Day JR, Lonigro RJ, Hovelson DH, Siddiqui J, Kunju LP, Dunn, RL, Meyer S, Hodge P, Groskopf J, Wei JT, Chinnaiyan AM. Urine TMPRSS2:ERG plus PCA3 for individualized prostate cancer risk assessment. Eur Urol. 2016;70(1):45-53.

  57. Kanwal R, Shukla S, Walker E, Gupta S. Acquisition of tumorigenic potential and therapeutic resistance in CD133+ subpopulation of prostate cancer cells exhibiting stem-cell like characteristics. Cancer Lett. 2018;430:25-33.

  58. Torrealba N, Rodriguez-Berriguete G, Fraile B, Olmedilla G, Martinez-Onsurbe P, Sanchez-Chapado M, Paniagua R, Royuela M. PI3K pathway and Bcl-2 family. Clinicopathological features in prostate cancer. Aging Male. 2018;21(3):211-22.

  59. Gao S, Zhao Z, Wu R, Wu L, Tian X, Zhang Z. MiR-146b inhibits autophagy in prostate cancer by targeting the PTEN/Akt/mTOR signaling pathway. Aging. 2018;10(8):2113-21.


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