J Vet Sci.  2018 Mar;19(2):162-171. 10.4142/jvs.2018.19.2.162.

Comparative aspects of microRNA expression in canine and human cancers

• Sahabi K
• Selvarajah GT
• Abdullah R
• Cheah YK
• Tan GC

• KMID: 2407615
• DOI: http://doi.org/10.4142/jvs.2018.19.2.162

Abstract

MicroRNAs (miRNAs) have important roles in all biological pathways in multicellular organisms. Over 1,400 human miRNAs have been identified, and many are conserved among vertebrates and invertebrates. Regulation of miRNA is the most common mode of post-transcriptional gene regulation. The miRNAs that are involved in the initiation and progression of cancers are termed oncomiRs and several of them have been identified in canine and human cancers. Similarly, several miRNAs have been reported to be down-regulated in cancers of the two species. In this review, current information on the expression and roles of miRNAs in oncogenesis and progression of human and canine cancers, as well the roles miRNAs have in cancer stem cell biology, are highlighted. The potential for the use of miRNAs as therapeutic targets in personalized cancer therapy in domestic dogs and their possible application in human cancer counterparts are also discussed.

Keyword

dogs; gene expression; microRNAs; neoplasms; stem cells

MeSH Terms

Animals
Biology
Carcinogenesis
Dogs
Gene Expression
Humans*
Invertebrates
MicroRNAs*
Neoplastic Stem Cells
Stem Cells
Vertebrates
MicroRNAs

Reference

1. Acunzo M, Romano G, Wernicke D, Croce CM. MicroRNA and cancer--a brief overview. Adv Biol Regul. 2015; 57:1–9.

2. Albonico F, Mortarino M, Avallone G, Gioia G, Comazzi S, Roccabianca P. The expression ratio of miR-17-5p and miR-155 correlates with grading in canine splenic lymphoma. Vet Immunol Immunopathol. 2013; 155:117–123.

3. Ambros V. A hierarchy of regulatory genes controls a larva-to-adult developmental switch in C. elegans. Cell. 1989; 57:49–57.

4. Bao B, Ahmad A, Azmi AS, Ali S, Sarkar FH. Overview of cancer stem cells (CSCs) and mechanisms of their regulation: implications for cancer therapy. Curr Protoc Pharmacol. 2013; Chapter 14:Unit 14.25.

5. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009; 136:215–233.

6. Bertoli G, Cava C, Castiglioni I. MicroRNAs: new biomarkers for diagnosis, prognosis, therapy prediction and therapeutic tools for breast cancer. Theranostics. 2015; 5:1122–1143.

7. Bhaskaran M, Mohan M. MicroRNAs: history, biogenesis, and their evolving role in animal development and disease. Vet Pathol. 2014; 51:759–774.

8. Boggs RM, Wright ZM, Stickney MJ, Porter WW, Murphy KE. MicroRNA expression in canine mammary cancer. Mamm Genome. 2008; 19:561–569.

9. Borge KS, Nord S, Van Loo P, Lingjærde OC, Gunnes G, Alnæs GI, Solvang HK, Lüders T, Kristensen VN, Børresen-Dale AL, Lingaas F. Canine mammary tumours are affected by frequent copy number aberrations, including amplification of MYC and loss of PTEN. PLoS One. 2015; 10:e0126371.

10. Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, Shannon MF, Goodall GJ. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res. 2008; 68:7846–7854.

11. Breen M, Modiano JF. Evolutionarily conserved cytogenetic changes in hematological malignancies of dogs and humans-man and his best friend share more than companionship. Chromosome Res. 2008; 16:145–154.

12. Bueno MJ, Pérez de Castro I, Gómez de Cedrón M, Santos J, Calin GA, Cigudosa JC, Croce CM, Fernández-Piqueras J, Malumbres M. Genetic and epigenetic silencing of microRNA-203 enhances ABL1 and BCR-ABL1 oncogene expression. Cancer Cell. 2008; 13:496–506.

13. Calin GA, Cimmino A, Fabbri M, Ferracin M, Wojcik SE, Shimizu M, Taccioli C, Zanesi N, Garzon R, Aqeilan RI, Alder H, Volinia S, Rassenti L, Liu X, Liu CG, Kipps TJ, Negrini M, Croce CM. MiR-15a and miR-16-1 cluster functions in human leukemia. Proc Natl Acad Sci U S A. 2008; 105:5166–5171.

14. Chen SC, Stern P, Guo Z, Chen J. Expression of multiple artificial microRNAs from a chicken miRNA126-based lentiviral vector. PLoS One. 2011; 6:e22437.

15. Chira P, Vareli K, Sainis I, Papandreou C, Briasoulis E. Alterations of microRNAs in solid cancers and their prognostic value. Cancers (Basel). 2010; 2:1328–1353.

16. Chou J, Lin JH, Brenot A, Kim JW, Provot S, Werb Z. GATA3 suppresses metastasis and modulates the tumour microenvironment by regulating microRNA-29b expression. Nat Cell Biol. 2013; 15:201–213.

17. Cocola C, Anastasi P, Astigiano S, Piscitelli E, Pelucchi P, Vilardo L, Bertoli G, Beccaglia M, Veronesi MC, Sanzone S, Barbieri O, Reinbold RA, Luvoni GC, Zucchi I. Isolation of canine mammary cells with stem cell properties and tumour-initiating potential. Reprod Domest Anim. 2009; 44:Suppl 2. 214–217.

18. Croce CM. Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet. 2009; 10:704–714.

19. Cui Y, Huang T, Zhang X. RNA editing of microRNA prevents RNA-induced silencing complex recognition of target mRNA. Open Biol. 2015; 5:150126.

20. Díaz-Martín J, Díaz-López A, Moreno-Bueno G, Castilla MÁ, Rosa-Rosa JM, Cano A, Palacios J. A core microRNA signature associated with inducers of the epithelial-to-mesenchymal transition. J Pathol. 2014; 232:319–329.

21. Egeland NG, Lunde S, Jonsdottir K, Lende TH, Cronin-Fenton D, Gilje B, Janssen EA, Søiland H. The role of microRNAs as predictors of response to tamoxifen treatment in breast cancer patients. Int J Mol Sci. 2015; 16:24243–24275.

22. Fabian MR, Sonenberg N. The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat Struct Mol Biol. 2012; 19:586–593.

23. Faraoni I, Antonetti FR, Cardone J, Bonmassar E. miR-155 gene: a typical multifunctional microRNA. Biochim Biophys Acta. 2009; 1792:497–505.

24. Fedorko M, Stanik M, Iliev R, Redova-Lojova M, Machackova T, Svoboda M, Pacik D, Dolezel J, Slaby O. Combination of miR-378 and miR-210 serum levels enables sensitive detection of renal cell carcinoma. Int J Mol Sci. 2015; 16:23382–23389.

25. Fenger JM, Bear MD, Volinia S, Lin TY, Harrington BK, London CA, Kisseberth WC. Overexpression of miR-9 in mast cells is associated with invasive behavior and spontaneous metastasis. BMC Cancer. 2014; 14:84.

26. Fenger JM, Roberts RD, Iwenofu OH, Bear MD, Zhang X, Couto JI, Modiano JF, Kisseberth WC, London CA. MiR-9 is overexpressed in spontaneous canine osteosarcoma and promotes a metastatic phenotype including invasion and migration in osteoblasts and osteosarcoma cell lines. BMC Cancer. 2016; 16:784.

27. Finver SN, Nishikura K, Finger LR, Haluska FG, Finan J, Nowell PC, Croce CM. Sequence analysis of the MYC oncogene involved in the t(8;14)(q24;q11) chromosome translocation in a human leukemia T-cell line indicates that putative regulatory regions are not altered. Proc Natl Acad Sci U S A. 1988; 85:3052–3056.

28. Frankel LB, Christoffersen NR, Jacobsen A, Lindow M, Krogh A, Lund AH. Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J Biol Chem. 2008; 283:1026–1033.

29. Gioia G, Mortarino M, Gelain ME, Albonico F, Ciusani E, Forno I, Marconato L, Martini V, Comazzi S. Immunophenotype-related microRNA expression in canine chronic lymphocytic leukemia. Vet Immunol Immunopathol. 2011; 142:228–235.

30. Gregory PA, Bracken CP, Smith E, Bert AG, Wright JA, Roslan S, Morris M, Wyatt L, Farshid G, Lim YY, Lindeman GJ, Shannon MF, Drew PA, Khew-Goodall Y, Goodall GJ. An autocrine TGF-beta/ZEB/miR-200 signaling network regulates establishment and maintenance of epithelial-mesenchymal transition. Mol Biol Cell. 2011; 22:1686–1698.

31. Griffiths-Jones S. miRBase: microRNA sequences and annotation. Curr Protoc Bioinformatics. 2010; Chapter 12:Unit 12.9.1–Unit 12.9.10.

32. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000; 100:57–70.

33. Heishima K, Mori T, Sakai H, Sugito N, Murakami M, Yamada N, Akao Y, Maruo K. MicroRNA-214 promotes apoptosis in canine hemangiosarcoma by targeting the COP1-p53 axis. PLoS One. 2015; 10:e0137361.

34. Hossain A, Kuo MT, Saunders GF. Mir-17-5p regulates breast cancer cell proliferation by inhibiting translation of AIB1 mRNA. Mol Cell Biol. 2006; 26:8191–8201.

35. Jansson MD, Lund AH. MicroRNA and cancer. Mol Oncol. 2012; 6:590–610.

36. Kang L, Mao J, Tao Y, Song B, Ma W, Lu Y, Zhao L, Li J, Yang B, Li L. MicroRNA-34a suppresses the breast cancer stem cell-like characteristics by downregulating Notch1 pathway. Cancer Sci. 2015; 106:700–708.

37. Kobayashi M, Saito A, Tanaka Y, Michishita M, Kobayashi M, Irimajiri M, Kaneda T, Ochiai K, Bonkobara M, Takahashi K, Hori T, Kawakami E. MicroRNA expression profiling in canine prostate cancer. J Vet Med Sci. 2017; 79:719–725.

38. Li L, Yuan L, Luo J, Gao J, Guo J, Xie X. MiR-34a inhibits proliferation and migration of breast cancer through down-regulation of Bcl-2 and SIRT1. Clin Exp Med. 2013; 13:109–117.

39. Liu T, Hu K, Zhao Z, Chen G, Ou X, Zhang H, Zhang X, Wei X, Wang D, Cui M, Liu C. MicroRNA-1 down-regulates proliferation and migration of breast cancer stem cells by inhibiting the Wnt/b-catenin pathway. Oncotarget. 2015; 6:41638–41649.

40. Liu X, Liu X, Wu Y, Wu Q, Wang Q, Yang Z, Li L. MicroRNAs in biofluids are novel tools for bladder cancer screening. Oncotarget. 2017; 8:32370–32379.

41. Longo DL, Fauci AS, Kasper DL, Hauser SL, Jameson JL. Less common hematologic malignancies. In : Wiener C, Fauci AS, Braunwald E, Kasper DL, Hauser S, Longo D, Jameson JL, Loscalzo J, Brown C, editors. Harrison's Principles of Internal Medicine Self-Assessment and Board Review. 18th ed. New York: McGraw-Hill Professional;2012. p. 1–14.

42. Louie E, Nik S, Chen JS, Schmidt M, Song B, Pacson C, Chen XF, Park S, Ju J, Chen EI. Identification of a stem-like cell population by exposing metastatic breast cancer cell lines to repetitive cycles of hypoxia and reoxygenation. Breast Cancer Res. 2010; 12:R94.

43. Lujambio A, Ropero S, Ballestar E, Fraga MF, Cerrato C, Setién F, Casado S, Suarez-Gauthier A, Sanchez-Cespedes M, Git A, Spiteri I, Das PP, Caldas C, Miska E, Esteller M. Genetic unmasking of an epigenetically silenced microRNA in human cancer cells. Cancer Res. 2007; 67:1424–1429.

44. Lutful Kabir FM, DeInnocentes P, Bird RC. Altered microRNA expression profiles and regulation of INK4A/CDKN2A tumor suppressor genes in canine breast cancer models. J Cell Biochem. 2015; 116:2956–2969.

45. Ma L, Reinhardt F, Pan E, Soutschek J, Bhat B, Marcusson EG, Teruya-Feldstein J, Bell GW, Weinberg RA. Therapeutic silencing of miR-10b inhibits metastasis in a mouse mammary tumor model. Nat Biotechnol. 2010; 28:341–347.

46. Ma L, Young J, Prabhala H, Pan E, Mestdagh P, Muth D, Teruya-Feldstein J, Reinhardt F, Onder TT, Valastyan S, Westermann F, Speleman F, Vandesompele J, Weinberg RA. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol. 2010; 12:247–256.

47. Morris JS. Genomic and proteomic profiling for cancer diagnosis in dogs. Vet J. 2016; 215:101–109.

48. Mortarino M, Gioia G, Gelain ME, Albonico F, Roccabianca P, Ferri E, Comazzi S. Identification of suitable endogenous controls and differentially expressed microRNAs in canine fresh-frozen and FFPE lymphoma samples. Leuk Res. 2010; 34:1070–1077.

49. Mulder KM. Role of Ras and Mapks in TGFbeta signaling. Cytokine Growth Factor Rev. 2000; 11:23–35.

50. Noguchi S, Mori T, Hoshino Y, Yamada N, Maruo K, Akao Y. MicroRNAs as tumour suppressors in canine and human melanoma cells and as a prognostic factor in canine melanomas. Vet Comp Oncol. 2013; 11:113–123.

51. Noguchi S, Mori T, Hoshino Y, Yamada N, Nakagawa T, Sasaki N, Akao Y, Maruo K. Comparative study of anti-oncogenic microRNA-145 in canine and human malignant melanoma. J Vet Med Sci. 2012; 74:1–8.

52. Novosad CA. Principles of treatment for mammary gland tumors. Clin Tech Small Anim Pract. 2003; 18:107–109.

53. Ouzounova M, Vuong T, Ancey PB, Ferrand M, Durand G, Le-Calvez Kelm F, Croce C, Matar C, Herceg Z, Hernandez-Vargas H. MicroRNA miR-30 family regulates non-attachment growth of breast cancer cells. BMC Genomics. 2013; 14:139.

54. Pan H, Gu L, Liu B, Li Y, Wang Y, Bai X, Li L, Wang B, Peng Q, Yao Z, Tang Z. Tropomyosin-1 acts as a potential tumor suppressor in human oral squamous cell carcinoma. PLoS One. 2017; 12:e0168900.

55. Pazzaglia L, Leonardi L, Conti A, Novello C, Quattrini I, Montanini L, Roperto F, Del Piero F, Di Guardo G, Piro F, Picci P, Benassi MS. miR-196a expression in human and canine osteosarcomas: a comparative study. Res Vet Sci. 2015; 99:112–119.

56. Pekarsky Y, Balatti V, Palamarchuk A, Rizzotto L, Veneziano D, Nigita G, Rassenti LZ, Pass HI, Kipps TJ, Liu CG, Croce CM. Dysregulation of a family of short noncoding RNAs, tsRNAs, in human cancer. Proc Natl Acad Sci U S A. 2016; 113:5071–5076.

57. Piva R, Spandidos DA, Gambari R. From microRNA functions to microRNA therapeutics: novel targets and novel drugs in breast cancer research and treatment (Review). Int J Oncol. 2013; 43:985–994.

58. Qi L, Zhang B, Zhang S, Ci X, Wu Q, Ma G, Luo A, Fu L, King JL, Nahta R, Dong JT. ERRF sensitizes ERBB2-positive breast cancer cells to lapatinib treatment likely by attenuating MCL1 and ERBB2 expression. Oncotarget. 2017; 8:36054–36066.

59. Qin W, Ren Q, Liu T, Huang Y, Wang J. MicroRNA-155 is a novel suppressor of ovarian cancer-initiating cells that targets CLDN1. FEBS Lett. 2013; 587:1434–1439.

60. Qiu C, Lin D, Wang J, Wang L. Expression and significance of PTEN in canine mammary gland tumours. Res Vet Sci. 2008; 85:383–388.

61. Radojicic J, Zaravinos A, Vrekoussis T, Kafousi M, Spandidos DA, Stathopoulos EN. MicroRNA expression analysis in triple-negative (ER, PR and Her2/neu) breast cancer. Cell Cycle. 2011; 10:507–517.

62. Rothschild SI. microRNA therapies in cancer. Mol Cell Ther. 2014; 2:7.

63. Rybicka A, Mucha J, Majchrzak K, Taciak B, Hellmen E, Motyl T, Krol M. Analysis of microRNA expression in canine mammary cancer stem-like cells indicates epigenetic regulation of transforming growth factor-beta signaling. J Physiol Pharmacol. 2015; 66:29–37.

64. Salzman DW, Shubert-Coleman J, Furneaux H. P68 RNA helicase unwinds the human let-7 microRNA precursor duplex and is required for let-7-directed silencing of gene expression. J Biol Chem. 2007; 282:32773–32779.

65. Sarver AL, Thayanithy V, Scott MC, Cleton-Jansen AM, Hogendoorn PC, Modiano JF, Subramanian S. MicroRNAs at the human 14q32 locus have prognostic significance in osteosarcoma. Orphanet J Rare Dis. 2013; 8:7.

66. Sassen S, Miska EA, Caldas C. MicroRNA: implications for cancer. Virchows Arch. 2008; 452:1–10.

67. Schultz NA, Dehlendorff C, Jensen BV, Bjerregaard JK, Nielsen KR, Bojesen SE, Calatayud D, Nielsen SE, Yilmaz M, Holländer NH, Andersen KK, Johansen JS. MicroRNA biomarkers in whole blood for detection of pancreatic cancer. JAMA. 2014; 311:392–404.

68. Selvarajah GT, Kirpensteijn J, van Wolferen ME, Rao NA, Fieten H, Mol JA. Gene expression profiling of canine osteosarcoma reveals genes associated with short and long survival times. Mol Cancer. 2009; 8:72.

69. Shalaby T, Grotzer MA. MYC as therapeutic target for embryonal tumors: potential and challenges. Curr Cancer Drug Targets. 2016; 16:2–21.

70. Shi SB, Wang M, Tian J, Li R, Chang CX, Qi JL. MicroRNA 25, microRNA 145, and microRNA 210 as biomarkers for predicting the efficacy of maintenance treatment with pemetrexed in lung adenocarcinoma patients who are negative for epidermal growth factor receptor mutations or anaplastic lymphoma kinase translocations. Transl Res. 2016; 170:1–7.

71. Song SJ, Poliseno L, Song MS, Ala U, Webster K, Ng C, Beringer G, Brikbak NJ, Yuan X, Cantley LC, Richardson AL, Pandolfi PP. MicroRNA-antagonism regulates breast cancer stemness and metastasis via TET-family-dependent chromatin remodeling. Cell. 2013; 154:311–324.

72. Tan GC, Chan E, Molnar A, Sarkar R, Alexieva D, Isa IM, Robinson S, Zhang S, Ellis P, Langford CF, Guillot PV, Chandrashekran A, Fisk NM, Castellano L, Meister G, Winston RM, Cui W, Baulcombe D, Dibb NJ. 5′ isomiR variation is of functional and evolutionary importance. Nucleic Acids Res. 2014; 42:9424–9435.

73. Tang J, Ahmad A, Sarkar FH. The role of microRNAs in breast cancer migration, invasion and metastasis. Int J Mol Sci. 2012; 13:13414–13437.

74. Tang R, Yang C, Ma X, Wang Y, Luo D, Huang C, Xu Z, Liu P, Yang L. MiR-let-7a inhibits cell proliferation, migration, and invasion by down-regulating PKM2 in gastric cancer. Oncotarget. 2016; 7:5972–5984.

75. Thayanithy V, Park C, Sarver AL, Kartha RV, Korpela DM, Graef AJ, Steer CJ, Modiano JF, Subramanian S. Combinatorial treatment of DNA and chromatin-modifying drugs cause cell death in human and canine osteosarcoma cell lines. PLoS One. 2012; 7:e43720.

76. Thayanithy V, Sarver AL, Kartha RV, Li L, Angstadt AY, Breen M, Steer CJ, Modiano JF, Subramanian S. Perturbation of 14q32 miRNAs-cMYC gene network in osteosarcoma. Bone. 2012; 50:171–181.

77. Uhl E, Krimer P, Schliekelman P, Tompkins SM, Suter S. Identification of altered MicroRNA expression in canine lymphoid cell lines and cases of B- and T-Cell lymphomas. Genes Chromosomes Cancer. 2011; 50:950–967.

78. Vinall RL, Kent MS, deVere White RW. Expression of microRNAs in urinary bladder samples obtained from dogs with grossly normal bladders, inflammatory bladder disease, or transitional cell carcinoma. Am J Vet Res. 2012; 73:1626–1633.

79. von Deetzen MC, Schmeck B, Gruber AD, Klopfleisch R. Molecular quantification of canine specific microRNA species. Res Vet Sci. 2013; 95:562–568.

80. von Deetzen MC, Schmeck BT, Gruber AD, Klopfleisch R. Malignancy associated MicroRNA expression changes in canine mammary cancer of different malignancies. ISRN Vet Sci. 2014; 2014:148597.

81. Wiggins JF, Ruffino L, Kelnar K, Omotola M, Patrawala L, Brown D, Bader AG. Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res. 2010; 70:5923–5930.

82. Wood LD, Parsons DW, Jones S, Lin J, Sjöblom T, Leary RJ, Shen D, Boca SM, Barber T, Ptak J, Silliman N, Szabo S, Dezso Z, Ustyanksky V, Nikolskaya T, Nikolsky Y, Karchin R, Wilson PA, Kaminker JS, Zhang Z, Croshaw R, Willis J, Dawson D, Shipitsin M, Willson JK, Sukumar S, Polyak K, Park BH, Pethiyagoda CL, Pant PV, Ballinger DG, Sparks AB, Hartigan J, Smith DR, Suh E, Papadopoulos N, Buckhaults P, Markowitz SD, Parmigiani G, Kinzler KW, Velculescu VE, Vogelstein B. The genomic landscapes of human breast and colorectal cancers. Science. 2007; 318:1108–1113.

83. Xu X, Zhu Y, Liang Z, Li S, Xu X, Wang X, Wu J, Hu Z, Meng S, Liu B, Qin J, Xie L, Zheng X. c-Met and CREB1 are involved in miR-433-mediated inhibition of the epithelial-mesenchymal transition in bladder cancer by regulating Akt/GSK-3b/Snail signaling. Cell Death Dis. 2016; 7:e2088.

84. Yun SJ, Jeong P, Kim WT, Kim TH, Lee YS, Song PH, Choi YH, Kim IY, Moon SK, Kim WJ. Cell-free microRNAs in urine as diagnostic and prognostic biomarkers of bladder cancer. Int J Oncol. 2012; 41:1871–1878.

85. Zadran S, Remacle F, Levine R. miRNA and mRNA cancer signatures determined by analysis of expression levels in large cohorts of patients. Proc Natl Acad Sci U S A. 2013; 110:19160–19165.

86. Zhang B, Zhao R, He Y, Fu X, Fu L, Zhu Z, Fu L, Dong JT. MicroRNA 100 sensitizes luminal A breast cancer cells to paclitaxel treatment in part by targeting mTOR. Oncotarget. 2016; 7:5702–5714.

87. Zhou X, Zhu W, Li H, Wen W, Cheng W, Wang F, Wu Y, Qi L, Fan Y, Chen Y, Ding Y, Xu J, Qian J, Huang Z, Wang T, Zhu D, Shu Y, Liu P. Diagnostic value of a plasma microRNA signature in gastric cancer: a microRNA expression analysis. Sci Rep. 2015; 5:11251.