Carcinogenic process of canine prostate
Wnt canonical pathway and its comparative study
DOI:
https://doi.org/10.35172/rvz.2017.v24.337Keywords:
canine prostate carcinoma, compared oncology, dogs, WNT pathwayAbstract
Prostate of dogs have similar lesions to that observed in human and is the only species other
than man which frequently displays spontaneous prostatic tumors. In this way, the dog
represent an important model of studying different prostatic affections. The prostate cancer
development is multifactorial and among them, genetic and epigenetic alterations are
involved. The dog can be a natural and spontaneous model to study preneoplastic and
neoplastic lesions, with potential future studies as models for pre-clinical tests. One of
important pathway to prostate carcinogenesis is beta catenin dependent canonical WNT
pathway. In this paper, we review the role of this pathway in prostate carcinogenesis,
important in humans and dogs, besides some regulatory proteins involved in this pathway
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Environmental risk factors related to the development of canine non-Hodgkin’s
lymphoma. Cienc Rural. 2013;43(7):1302–8.
8. Keller JM, Schade GR, Ives K, Cheng X, Rosol TJ, Piert M, et al. A novel canine
model for prostate cancer. Prostate. 2013;73(9):952–9.
9. Winkler S, Escobar HM, Meyer B, Simon D, Eberle N, Baumgartner W, et al. HMGA2
expression in a canine model of prostate cancer. Cancer Genet Cytogenet.
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10. Yang G, Goltsov AA, Ren C, Kurosaka S, Edamura K, Logothetis R, et al. Caveolin-1
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12. Yu X, Wang Y, Jiang M, Bierie B, Roy-Burman P, Shen MM, et al. Activation of β-
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castration. Prostate. 2009;69(3):249–62.
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catenin caught in a loop. Int J Biochem Cell Biol. 2012;44(6):847–50.
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Signaling through inhibition of β-Catenin degradation in an intact axin1 complex. Cell.
2012;149(6):1245–56.
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17. Wang L, Liu X, Gusev E, Wang C, Fagotto F. Regulation of the phosphorylation and
nuclear import and export of β-catenin by APC and its cancer-related truncated form. J
Cell Sci. 2014;127(Pt 8):1647–59.
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2012;9(8):418–28.
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2015;100:176–81.
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R. Alterations of C-MYC, NKX3.1, and E-cadherin expression in canine prostate
carcinogenesis. Microsc Res Tech. 2013;76(12):1250–6.
22. Rodrigues MMP, Rema A, Gartner MF, Laufer-Amorim R. Role of adhesion
molecules and proliferation hyperplasic, pre neoplastic and neoplastic lesions in canine
prostate. Pak J Biol Sci. 2013;16(21):1324–9.
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treatment. Theriogenology. 2008;70:375–83.
24. L’Eplattenier HF. Studies on the pathogenesis and management of prostate carcinoma
in dogs [thesis]. Utrecht: University Utrecht; 2009.
25. Dorso L, Chanut F, Howroyd P, Burnett R. Variability in weight and histological
appearance of the prostate of beagle dogs used in toxicology studies. Toxicol Pathol.
2008;36:917–25.
26. Fonseca-Alves CE, Faleiro MBR, Amorim RL, De Moura VMBD. Avaliação
histológica da próstata de cães adultos sexualmente intactos. Arq Bras Med Vet Zootec.
2010;62(3):596–602.
27. De Marzo AM, Platz EA, Sutcliffe S, Xu J, Grönberg H, Drake CG, et al. Inflammation
in prostate carcinogenesis. Nat Rev Cancer. 2007;7(4):256–69.
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controversial relationship between benign prostatic hyperplasia and prostate cancer: the
role of inflammation. Eur Urol. 2011;60(1):106–17.
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30. Rossignol A, Villers A, Molinié V, Mazerolles C. Histologie et immunohistochimie de
la prostate du chien. Validité du modèle animal pour l’étude des lésions
précancéreuses. Rev Med Vet. 2004;1(155):21–6.
31. Galvão ALB, Ferreira GS, Léga E, Costa PF, Ondani AC, Denicol A. Principais
afecções da glândula prostática em cães. Revista Brasileira de Reprodução Animal.
2011;35(4):456–66.
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express markers of urothelial and prostatic differentiation. Vet Pathol. 2004;41(2):131–
40.
33. Matsuzaki P, Cogliati B, Sanches DS, Chaible LM, Kimura KC, Silva TC, et al.
Immunohistochemical Characterization of Canine Prostatic Intraepithelial Neoplasia. J
Comp Pathol. 2010;142(1):84–8.
34. Baetke SC, Adriaens ME, Seigneuric R, Evelo CT, Eijssen LMT. Molecular pathways
involved in prostate carcinogenesis: insights from public microarray datasets. PLoS
One . 2012;7(11):e49831.
35. Palapattu GS. Prostate carcinogenesis and inflammation: emerging insights.
Carcinogenesis. 2004;26(7):1170–81.
36. Grover PL, Martin FL. The initiation of breast and prostate cancer. Carcinogenesis.
2002;23(7):1095–102.
37. Shen MM, Abate-Shen C. Molecular genetics of prostate cancer: new prospects for old
challenges. Genes Dev. 2010;24(18):1967–2000.
38. Alshenawy HA, Ali MAE-HAE-A. Differential caveolin-1 expression in colon
carcinoma and its relation to E-cadherin–β-catenin complex. Ann Diagn Pathol.
2013;17(6):476–82.
39. Chen G, Shukeir N, Potti A, Sircar K, Aprikian A, Goltzman D, et al. Up-regulation of
Wnt-1 and beta-catenin production in patients with advanced metastatic prostate
carcinoma: potential pathogenetic and prognostic implications. Cancer.
2004;101(6):1345–56.
40. López-Knowles E, Zardawi SJ, McNeil CM, Millar EK , Crea P, Musgrove E, et al.
Cytoplasmic localization of beta-catenin is a marker of poor outcome in breast cancer
patients. Cancer Epidemiol Biomarkers Prev. 2010;19(1):301–9.
41. Morgan C, Jenkins SA, Kynaston HG, Doak SH. The role of adhesion molecules as
biomarkers for the aggressive prostate cancer phenotype. PLoS One. 2013;8(12):1–8.
42. Drivalos A, Papatsoris AG, Chrisofos M, Efstathiou E, Dimopoulos MA. The role of
the cell adhesion molecules (integrins/cadherins) in prostate cancer. Int Braz J
Urol. 2011;37(3):302–6.
43. Rodrigues MMP, Rema A, Gartner MF, Laufer-Amo R. Role of adhesion molecules
and proliferation hyperplasic, pre neoplastic and neoplastic lesions in canine prostate.
Pak J Biol Sci. 2013;16(21):1324–9.
44. Kim H, He Y, Yang I, Zeng Y, Kim Y, Seo YW, et al. δ-Catenin promotes E-cadherin
processing and activates β-catenin-mediated signaling: implications on human prostate
cancer progression. Biochim Biophys Acta. 2012;1822(4):509–21.
45. Jaggi M, Johansson SL, Baker JJ, Smith LM, Galich A, Balaji KC. Aberrant expression
of E-cadherin and beta-catenin in human prostate cancer. Urol Oncol. 2005;23(6):402–
6.
46. Faleiro-Rodrigues C, Macedo-Pinto I, Pereira D, Lopes CS. Prognostic value of Ecadherin immunoexpression in patients with primary ovarian carcinomas. Ann Oncol.
2004;15(10):1535–42.
47. Rubin MA, Mucci NR, Figurski J, Fecko A, Pienta KJ, Day ML. E-cadherin expression
in prostate cancer: a broad survey using high-density tissue microarray technology.
Hum Pathol. 2001;32(7):690–7.
48. Cervantes-Arias A, Pang LY, Argyle DJ. Epithelial-mesenchymal transition as a
fundamental mechanism underlying the cancer phenotype. Vet Comp Oncol.
2013;11(3):169–84.
49. Polakis P. The adenomatous polyposis coli (APC) tumor suppressor. Biochim Biophys
Acta. 1997;1332(3):F127–47.
50. Bruxvoort KJ, Charbonneau HM, Giambernardi TA, Goolsby JC, Qian CN, Zylstra
CR, et al. Inactivation of Apc in the mouse prostate causes prostate carcinoma. Cancer
Res. 2007;67:2490–6.
51. Watanabe M, Kakiuchi H, Kato H, Shiraishi T, Yatani R, Sugimura T, et al. APC gene
mutations in human prostate cancer. Jpn J Clin Oncol. 1996;26(2):77–81
52. Richiardi L, Fiano V, Grasso C, Zugna D, Delsedime L, Gillio-Tos A, et al.
Methylation of APC and GSTP1 in non-neoplastic tissue adjacent to prostate tumour
and mortality from prostate cancer. PloS One. 2013;8(7):e68162.
53. MacDonald BT, Tamai K, He X. Wnt/β-Catenin signaling: components, mechanisms,
and diseases. Dev Cell. 2009;17(1):9–26.
54. Valkenburg KC, Yu X, De Marzo AM, Spiering TJ, Matusik RJ, Williams BO.
Activation of Wnt/β-catenin signaling in a subpopulation of murine prostate luminal
epithelial cells induces high grade prostate intraepithelial neoplasia. Prostate.
2014;74(15):1506–20.
55. Kawano Y. Secreted antagonists of the Wnt signalling pathway. J Cell Sci.
2003;116(Pt 13):2627–34.
56. Anastas JN, Moon RT. WNT signalling pathways as therapeutic targets in cancer. Nat
Rev Cancer. 2012;13(1):11–26.
57. Clevers H, Nusse R. Wnt/β-catenin signaling and disease. Cell. 2012;149(6):1192–205.
58. Lean FZX, Kontos S, Palmieri C. Science direct expression of b -catenin and
mesenchymal markers in canine prostatic hyperplasia and carcinoma. Journal of Comp
Pathol. 2014;150(4):373–81.
59. Simons BW, Hurley PJ, Huang Z, Ross AE, Miller R, Marchionni L, et al. Wnt
signaling though beta-catenin is required for prostate lineage specification. Dev Biol.
2012;371(2):246–55.
dog. Anim Reprod Sci. 2000;60-61:405–15.
2. Toledo DC, Faleiro MBR, Rodrigues MMP, Di Santis GW, Amorim RL, Moura
VMBD. Caracterização histomorfológica da atrofia inflamatória proliferativa na
próstata canina. Cienc Rural. 2010;40(6):1372–7.
3. Teske E, Naan E, Van Dijk E, Van Garderen E, Schalken J. Canine prostate carcinoma:
epidemiological evidence of an increased risk in castrated dogs. Mol Cell Endocrinol.
2002;197(1-2):251–5.
4. Instituto Nacional de Câncer José de Alencar Gomes da Silva. Estimativa 2016:
incidência de câncer no Brasil [Internet]. Rio de Janeiro: INCA; 2016 [cited 2017 Jan
19]. Available from: http://www.inca.gov.br/estimativa/2016/.
5. LeRoy BE, Northrup N. Prostate cancer in dogs: comparative and clinical aspects. Vet
J. 2009;180(2):149–62.
6. Rowell JL, McCarthy DO, Alvarez CE. Dog models of naturally occurring cancer.
Trends Mol Med . 2011;17(7):380–8.
7. Zanini DA, Kimura KC, Nishiya AT, Ubukata R, Leandro RM, Brito CP, et al.
Environmental risk factors related to the development of canine non-Hodgkin’s
lymphoma. Cienc Rural. 2013;43(7):1302–8.
8. Keller JM, Schade GR, Ives K, Cheng X, Rosol TJ, Piert M, et al. A novel canine
model for prostate cancer. Prostate. 2013;73(9):952–9.
9. Winkler S, Escobar HM, Meyer B, Simon D, Eberle N, Baumgartner W, et al. HMGA2
expression in a canine model of prostate cancer. Cancer Genet Cytogenet.
2007;177(2):98–102.
10. Yang G, Goltsov AA, Ren C, Kurosaka S, Edamura K, Logothetis R, et al. Caveolin-1
upregulation contributes to c-Myc-Induced High-Grade prostatic intraepithelial
neoplasia and prostate cancer. Mol Cancer Res. 2012;10(2):218–29.
11. Verras M, Sun Z. Roles and regulation of Wnt signaling and beta-catenin in prostate
cancer. Cancer Lett. 2006;237(1):22–32.
12. Yu X, Wang Y, Jiang M, Bierie B, Roy-Burman P, Shen MM, et al. Activation of β-
Catenin in mouse prostate causes HGPIN and continuous prostate growth after
castration. Prostate. 2009;69(3):249–62.
13. Jamieson C, Sharma M, Henderson BR. Wnt signaling from membrane to nucleus: β-
catenin caught in a loop. Int J Biochem Cell Biol. 2012;44(6):847–50.
14. Li VSW, Ng SS, Boersema PJ, Low TY, Karthaus WR, Gerlach JP, et al. Wnt
Signaling through inhibition of β-Catenin degradation in an intact axin1 complex. Cell.
2012;149(6):1245–56.
15. Stamos JL, Weis WI. The β -Catenin destruction complex. Cold Spring Harb Perspect
Biol. 2013;5(1):a007898.
16. Richiardi L, Fiano V, Vizzini L, De Marco L, Delsedime L, Akre O, et al. Promoter
methylation in APC, RUNX3, and GSTP1 and mortality in prostate cancer patients. J
Clin Oncol. 2009;27(19):3161–8.
17. Wang L, Liu X, Gusev E, Wang C, Fagotto F. Regulation of the phosphorylation and
nuclear import and export of β-catenin by APC and its cancer-related truncated form. J
Cell Sci. 2014;127(Pt 8):1647–59.
18. Kypta RM, Waxman J. Wnt/β-catenin signalling in prostate cancer. Nat Rev Urol.
2012;9(8):418–28.
19. Fonseca-Alves CE, Kobayashi PE, Rivera-Calderón LG, Laufer-Amorim R. Evidence
of epithelial–mesenchymal transition in canine prostate cancer metastasis. Res Vet Sci.
2015;100:176–81.
20. Schmalhofer O, Brabletz S, Brabletz T. E-cadherin, β-catenin, and ZEB1 in malignant
progression of cancer. Cancer Metastasis Rev. 2009;28(1-2):151–66.
21. Fonseca-Alves CE, Rodrigues MMP, de Moura VMBD, Rogatto SR, Laufer-Amorim
R. Alterations of C-MYC, NKX3.1, and E-cadherin expression in canine prostate
carcinogenesis. Microsc Res Tech. 2013;76(12):1250–6.
22. Rodrigues MMP, Rema A, Gartner MF, Laufer-Amorim R. Role of adhesion
molecules and proliferation hyperplasic, pre neoplastic and neoplastic lesions in canine
prostate. Pak J Biol Sci. 2013;16(21):1324–9.
23. Smith J. Canine prostatic disease: a review of anatomy, pathology, diagnosis, and
treatment. Theriogenology. 2008;70:375–83.
24. L’Eplattenier HF. Studies on the pathogenesis and management of prostate carcinoma
in dogs [thesis]. Utrecht: University Utrecht; 2009.
25. Dorso L, Chanut F, Howroyd P, Burnett R. Variability in weight and histological
appearance of the prostate of beagle dogs used in toxicology studies. Toxicol Pathol.
2008;36:917–25.
26. Fonseca-Alves CE, Faleiro MBR, Amorim RL, De Moura VMBD. Avaliação
histológica da próstata de cães adultos sexualmente intactos. Arq Bras Med Vet Zootec.
2010;62(3):596–602.
27. De Marzo AM, Platz EA, Sutcliffe S, Xu J, Grönberg H, Drake CG, et al. Inflammation
in prostate carcinogenesis. Nat Rev Cancer. 2007;7(4):256–69.
28. De Nunzio C, Kramer G, Marberger M, Montironi R, Nelson W, Schröder F, et al. The
controversial relationship between benign prostatic hyperplasia and prostate cancer: the
role of inflammation. Eur Urol. 2011;60(1):106–17.
29. Omabe M, Ezeani M. Infection, inflammation and prostate carcinogenesis. Infect Genet
Evol. 2011;11(6):1195–8.
30. Rossignol A, Villers A, Molinié V, Mazerolles C. Histologie et immunohistochimie de
la prostate du chien. Validité du modèle animal pour l’étude des lésions
précancéreuses. Rev Med Vet. 2004;1(155):21–6.
31. Galvão ALB, Ferreira GS, Léga E, Costa PF, Ondani AC, Denicol A. Principais
afecções da glândula prostática em cães. Revista Brasileira de Reprodução Animal.
2011;35(4):456–66.
32. LeRoy BE, Nadella MVP, Toribio RE, Leav I, Rosol TJ. Canine prostate carcinomas
express markers of urothelial and prostatic differentiation. Vet Pathol. 2004;41(2):131–
40.
33. Matsuzaki P, Cogliati B, Sanches DS, Chaible LM, Kimura KC, Silva TC, et al.
Immunohistochemical Characterization of Canine Prostatic Intraepithelial Neoplasia. J
Comp Pathol. 2010;142(1):84–8.
34. Baetke SC, Adriaens ME, Seigneuric R, Evelo CT, Eijssen LMT. Molecular pathways
involved in prostate carcinogenesis: insights from public microarray datasets. PLoS
One . 2012;7(11):e49831.
35. Palapattu GS. Prostate carcinogenesis and inflammation: emerging insights.
Carcinogenesis. 2004;26(7):1170–81.
36. Grover PL, Martin FL. The initiation of breast and prostate cancer. Carcinogenesis.
2002;23(7):1095–102.
37. Shen MM, Abate-Shen C. Molecular genetics of prostate cancer: new prospects for old
challenges. Genes Dev. 2010;24(18):1967–2000.
38. Alshenawy HA, Ali MAE-HAE-A. Differential caveolin-1 expression in colon
carcinoma and its relation to E-cadherin–β-catenin complex. Ann Diagn Pathol.
2013;17(6):476–82.
39. Chen G, Shukeir N, Potti A, Sircar K, Aprikian A, Goltzman D, et al. Up-regulation of
Wnt-1 and beta-catenin production in patients with advanced metastatic prostate
carcinoma: potential pathogenetic and prognostic implications. Cancer.
2004;101(6):1345–56.
40. López-Knowles E, Zardawi SJ, McNeil CM, Millar EK , Crea P, Musgrove E, et al.
Cytoplasmic localization of beta-catenin is a marker of poor outcome in breast cancer
patients. Cancer Epidemiol Biomarkers Prev. 2010;19(1):301–9.
41. Morgan C, Jenkins SA, Kynaston HG, Doak SH. The role of adhesion molecules as
biomarkers for the aggressive prostate cancer phenotype. PLoS One. 2013;8(12):1–8.
42. Drivalos A, Papatsoris AG, Chrisofos M, Efstathiou E, Dimopoulos MA. The role of
the cell adhesion molecules (integrins/cadherins) in prostate cancer. Int Braz J
Urol. 2011;37(3):302–6.
43. Rodrigues MMP, Rema A, Gartner MF, Laufer-Amo R. Role of adhesion molecules
and proliferation hyperplasic, pre neoplastic and neoplastic lesions in canine prostate.
Pak J Biol Sci. 2013;16(21):1324–9.
44. Kim H, He Y, Yang I, Zeng Y, Kim Y, Seo YW, et al. δ-Catenin promotes E-cadherin
processing and activates β-catenin-mediated signaling: implications on human prostate
cancer progression. Biochim Biophys Acta. 2012;1822(4):509–21.
45. Jaggi M, Johansson SL, Baker JJ, Smith LM, Galich A, Balaji KC. Aberrant expression
of E-cadherin and beta-catenin in human prostate cancer. Urol Oncol. 2005;23(6):402–
6.
46. Faleiro-Rodrigues C, Macedo-Pinto I, Pereira D, Lopes CS. Prognostic value of Ecadherin immunoexpression in patients with primary ovarian carcinomas. Ann Oncol.
2004;15(10):1535–42.
47. Rubin MA, Mucci NR, Figurski J, Fecko A, Pienta KJ, Day ML. E-cadherin expression
in prostate cancer: a broad survey using high-density tissue microarray technology.
Hum Pathol. 2001;32(7):690–7.
48. Cervantes-Arias A, Pang LY, Argyle DJ. Epithelial-mesenchymal transition as a
fundamental mechanism underlying the cancer phenotype. Vet Comp Oncol.
2013;11(3):169–84.
49. Polakis P. The adenomatous polyposis coli (APC) tumor suppressor. Biochim Biophys
Acta. 1997;1332(3):F127–47.
50. Bruxvoort KJ, Charbonneau HM, Giambernardi TA, Goolsby JC, Qian CN, Zylstra
CR, et al. Inactivation of Apc in the mouse prostate causes prostate carcinoma. Cancer
Res. 2007;67:2490–6.
51. Watanabe M, Kakiuchi H, Kato H, Shiraishi T, Yatani R, Sugimura T, et al. APC gene
mutations in human prostate cancer. Jpn J Clin Oncol. 1996;26(2):77–81
52. Richiardi L, Fiano V, Grasso C, Zugna D, Delsedime L, Gillio-Tos A, et al.
Methylation of APC and GSTP1 in non-neoplastic tissue adjacent to prostate tumour
and mortality from prostate cancer. PloS One. 2013;8(7):e68162.
53. MacDonald BT, Tamai K, He X. Wnt/β-Catenin signaling: components, mechanisms,
and diseases. Dev Cell. 2009;17(1):9–26.
54. Valkenburg KC, Yu X, De Marzo AM, Spiering TJ, Matusik RJ, Williams BO.
Activation of Wnt/β-catenin signaling in a subpopulation of murine prostate luminal
epithelial cells induces high grade prostate intraepithelial neoplasia. Prostate.
2014;74(15):1506–20.
55. Kawano Y. Secreted antagonists of the Wnt signalling pathway. J Cell Sci.
2003;116(Pt 13):2627–34.
56. Anastas JN, Moon RT. WNT signalling pathways as therapeutic targets in cancer. Nat
Rev Cancer. 2012;13(1):11–26.
57. Clevers H, Nusse R. Wnt/β-catenin signaling and disease. Cell. 2012;149(6):1192–205.
58. Lean FZX, Kontos S, Palmieri C. Science direct expression of b -catenin and
mesenchymal markers in canine prostatic hyperplasia and carcinoma. Journal of Comp
Pathol. 2014;150(4):373–81.
59. Simons BW, Hurley PJ, Huang Z, Ross AE, Miller R, Marchionni L, et al. Wnt
signaling though beta-catenin is required for prostate lineage specification. Dev Biol.
2012;371(2):246–55.
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2017-03-31
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Emiko Kobayashi P, Fonseca-Alves CE, Rivera-Calderón LG, Laufer-Amorim R. Carcinogenic process of canine prostate: Wnt canonical pathway and its comparative study. RVZ [Internet]. 2017 Mar. 31 [cited 2024 Nov. 24];24(1):49-5. Available from: https://rvz.emnuvens.com.br/rvz/article/view/337
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