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Cisplatin‑resistant germ cell tumor models: An exploration of the epithelial‑mesenchymal transition regulator SLUG

  • Authors:
    • Ingridy Izabella Vieira Cardoso
    • Marcela Nunes Rosa
    • Daniel Antunes Moreno
    • Letícia Maria Barbosa Tufi
    • Lorrayne Pereira Ramos
    • Larissa Alessandra Bourdeth Pereira
    • Lenilson Silva
    • Janaina Mello Soares Galvão
    • Isabela Cristiane Tosi
    • André Van Helvoort Lengert
    • Marcelo Cavalcanti Da Cruz
    • Silvia Aparecida Teixeira
    • Rui Manuel Reis
    • Luiz Fernando Lopes
    • Mariana Tomazini Pinto
  • View Affiliations / Copyright

    Affiliations: Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos, São Paulo 14784400, Brazil, Department of Pathology, Barretos Cancer Hospital, Barretos, São Paulo 14784400, Brazil, Barretos Children's Cancer Hospital, Hospital de Amor, Barretos, São Paulo 14784400, Brazil
    Copyright: © Vieira Cardoso et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Article Number: 228
    |
    Published online on: October 4, 2024
       https://doi.org/10.3892/mmr.2024.13352
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Abstract

Germ cell tumors (GCTs) constitute diverse neoplasms arising in the gonads or extragonadal locations. Testicular GCTs (TGCTs) are the predominant solid tumors in adolescents and young men. Despite cisplatin serving as the primary therapeutic intervention for TGCTs, 10‑20% of patients with advanced disease demonstrate resistance to cisplatin‑based chemotherapy, and epithelial‑mesenchymal transition (EMT) is a potential contributor to this resistance. EMT is regulated by various factors, including the snail family transcriptional repressor 2 (SLUG) transcriptional factor, and, to the best of our knowledge, remains unexplored within TGCTs. Therefore, the present study investigated the EMT transcription factor SLUG in TGCTs. In silico analyses were performed to investigate the expression of EMT markers in TGCTs. In addition, a cisplatin‑resistant model for TGCTs was developed using the NTERA‑2 cell line, and a mouse model was also established. Subsequently, EMT was assessed both in vitro and in vivo within the cisplatin‑resistant models using quantitative PCR and western blot analyses. The results of the in silico analysis showed that the different histologies exhibited distinct expression profiles for EMT markers. Seminomas exhibited a lower expression of EMT markers, whereas embryonal carcinomas and mixed GCT demonstrated high expression. Notably, patients with lower SLUG expression had longer median progression‑free survival (46.4 months vs. 28.0 months, P=0.022). In the in vitro analysis, EMT‑associated genes [fibronectin; vimentin (VIM); actin, α2, smooth muscle; collagen type I α1; transforming growth factor‑β1; and SLUG] were upregulated in the cisplatin‑resistant NTERA‑2 (NTERA‑2R) cell line after 72 h of cisplatin treatment. Consistent with this finding, the NTERA‑2R mouse model demonstrated a significant upregulation in the expression levels of VIM and SLUG. In conclusion, the present findings suggested that SLUG may serve a crucial role in connecting EMT with the development of cisplatin resistance, and targeting SLUG may be a putative therapeutic strategy to mitigate cisplatin resistance.
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View References

1 

Kalluri R and Weinberg R: The basics of epithelial-mesenchymal transition. J Clin Invest. 119:1420–1428. 2009. View Article : Google Scholar : PubMed/NCBI

2 

Thiery JP, Acloque H, Huang RYJ and Nieto MA: Epithelial-mesenchymal transitions in development and disease. Cell. 139:871–890. 2009. View Article : Google Scholar : PubMed/NCBI

3 

Yang J and Weinberg RA: Epithelial-mesenchymal transition: At the crossroads of development and tumor metastasis. Dev Cell. 14:818–829. 2008. View Article : Google Scholar : PubMed/NCBI

4 

Ye X and Weinberg RA: Epithelial-mesenchymal plasticity: A central regulator of cancer progression. Trends Cell Biol. 25:675–686. 2015. View Article : Google Scholar : PubMed/NCBI

5 

Kaufhold S and Bonavida B: Central role of Snail1 in the regulation of EMT and resistance in cancer: A target for therapeutic intervention. J Exp Clin Cancer Res. 33:622014. View Article : Google Scholar : PubMed/NCBI

6 

Grasset EM, Dunworth M, Sharma G, Loth M, Tandurella J, Cimino-Mathews A, Gentz M, Bracht S, Haynes M, Fertig EJ and Ewald AJ: Triple-negative breast cancer metastasis involves complex epithelial-mesenchymal transition dynamics and requires vimentin. Sci Transl Med. 14:eabn75712022. View Article : Google Scholar : PubMed/NCBI

7 

Tsoukalas N, Aravantinou-Fatorou E, Tolia M, Giaginis C, Galanopoulos M, Kiakou M, Kostakis ID, Dana E, Vamvakaris I, Korogiannos A, et al: Epithelial-mesenchymal transition in non small-cell lung cancer. Anticancer Res. 37:1773–1778. 2017. View Article : Google Scholar : PubMed/NCBI

8 

Palamaris K, Felekouras E and Sakellariou S: Epithelial to mesenchymal transition: Key regulator of pancreatic ductal adenocarcinoma progression and chemoresistance. Cancers (Basel). 13:55322021. View Article : Google Scholar : PubMed/NCBI

9 

Sessa C, Schneider DT, Planchamp F, Baust K, Braicu EI, Concin N, Godzinski J, McCluggage WG, Orbach D, Pautier P, et al: ESGO-SIOPE guidelines for the management of adolescents and young adults with non-epithelial ovarian cancers. Lancet Oncol. 21:e360–e368. 2020. View Article : Google Scholar : PubMed/NCBI

10 

Ghazarian AA, Kelly SP, Altekruse SF, Rosenberg PS and McGlynn KA: Future of testicular germ cell tumor incidence in the United States: Forecast through 2026. Cancer. 123:2320–2328. 2017. View Article : Google Scholar : PubMed/NCBI

11 

Pierce JL, Frazier AL and Amatruda JF: Pediatric germ cell tumors: A developmental perspective. Adv Urol. 2018:90593822018. View Article : Google Scholar : PubMed/NCBI

12 

Culine S, Kramar A, Théodore C, Geoffrois L, Chevreau C, Biron P, Nguyen BB, Héron JF, Kerbrat P, Caty A, et al: Randomized trial comparing bleomycin/etoposide/cisplatin with alternating cisplatin/cyclophosphamide/doxorubicin and vinblastine/bleomycin regimens of chemotherapy for patients with intermediate- and poor-risk metastatic nonseminomatous germ cell tumors: Genito-Urinary Group Of The French Federation Of Cancer Centers Trial T93MP. J Clin Oncol. 26:421–427. 2008. View Article : Google Scholar : PubMed/NCBI

13 

Pinto MT, Cárcano FM, Vieira AGS, Cabral ERM and Lopes LF: Molecular biology of pediatric and adult male germ cell tumors. Cancers (Basel). 13:23492021. View Article : Google Scholar : PubMed/NCBI

14 

de Vries G, Rosas-Plaza X, van Vugt MATM, Gietema JA and de Jong S: Testicular cancer: Determinants of cisplatin sensitivity and novel therapeutic opportunities. Cancer Treat Rev. 88:1020542020. View Article : Google Scholar : PubMed/NCBI

15 

Vega S, Morales AV, Ocaña OH, Valdés F, Fabregat I and Nieto MA: Snail blocks the cell cycle and confers resistance to cell death. Genes Dev. 18:1131–1143. 2004. View Article : Google Scholar : PubMed/NCBI

16 

Saxena M, Stephens MA, Pathak H and Rangarajan A: Transcription factors that mediate epithelial-mesenchymal transition lead to multidrug resistance by upregulating ABC transporters. Cell Death Dis. 2:e1792011. View Article : Google Scholar : PubMed/NCBI

17 

Wu K and Bonavida B: The activated NF-κB-Snail-RKIP circuitry in cancer regulates both the metastatic cascade and resistance to apoptosis by cytotoxic drugs. Crit Rev Immunol. 29:241–254. 2009. View Article : Google Scholar : PubMed/NCBI

18 

Lee HH, Lee SH, Song KY, Na SJ, O JH, Park JM, Jung ES, Choi MG and Park CH: Evaluation of Slug expression is useful for predicting lymph node metastasis and survival in patients with gastric cancer. BMC Cancer. 17:6702017. View Article : Google Scholar : PubMed/NCBI

19 

Gu A, Jie Y, Yao Q, Zhang Y and Mingyan E: Slug is associated with tumor metastasis and angiogenesis in ovarian cancer. Reprod Sci. 24:291–299. 2017. View Article : Google Scholar : PubMed/NCBI

20 

Bhat-Nakshatri P, Appaiah H, Ballas C, Pick-Franke P, Goulet R Jr, Badve S, Srour EF and Nakshatri H: SLUG/SNAI2 and tumor necrosis factor generate breast cells with CD44+/CD24-phenotype. BMC Cancer. 10:4112010. View Article : Google Scholar : PubMed/NCBI

21 

Shen H, Shih J, Hollern DP, Wang L, Bowlby R, Tickoo SK, Thorsson V, Mungall AJ, Newton Y, Hegde AM, et al: Integrated molecular characterization of testicular germ cell tumors. Cell Rep. 23:3392–3406. 2018. View Article : Google Scholar : PubMed/NCBI

22 

Gu Z, Eils R and Schlesner M: Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics. 32:2847–2849. 2016. View Article : Google Scholar : PubMed/NCBI

23 

Lengert AVH, Pereira LDNB, Cabral ERM, Gomes INF, Jesus LM, Gonçalves MFS, Rocha AOD, Tassinari TA, Silva LSD, Laus AC, et al: Potential new therapeutic approaches for cisplatin-resistant testicular germ cell tumors. Front Biosci (Landmark Ed). 27:2452022. View Article : Google Scholar : PubMed/NCBI

24 

Silva-Oliveira RJ, Silva VAO, Martinho O, Cruvinel-Carloni A, Melendez ME, Rosa MN, de Paula FE, de Souza Viana L, Carvalho AL and Reis RM: Cytotoxicity of allitinib, an irreversible anti-EGFR agent, in a large panel of human cancer-derived cell lines: KRAS mutation status as a predictive biomarker. Cell Oncol (Dordr). 39:253–263. 2016. View Article : Google Scholar : PubMed/NCBI

25 

Pfaffl MW: A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e452001. View Article : Google Scholar : PubMed/NCBI

26 

Teixeira SA, Luzzi MC, Martin ACBM, Duarte TT, Leal MO, Teixeira GR, Reis MT, Junior CRA, Santos K, Melendez ME, et al: The barretos cancer hospital animal facility: Implementation and results of a dedicated platform for preclinical oncology models. Vet Sci. 9:6362022. View Article : Google Scholar : PubMed/NCBI

27 

Mikami S, Katsube KI, Oya M, Ishida M, Kosaka T, Mizuno R, Mukai M and Okada Y: Expression of Snail and Slug in renal cell carcinoma: E-cadherin repressor Snail is associated with cancer invasion and prognosis. Lab Invest. 91:1443–1458. 2011. View Article : Google Scholar : PubMed/NCBI

28 

Gerwing M, Jacobsen C, Dyshlovoy S, Hauschild J, Rohlfing T, Oing C, Venz S, Oldenburg J, Oechsle K, Bokemeyer C, et al: Cabazitaxel overcomes cisplatin resistance in germ cell tumour cells. J Cancer Res Clin Oncol. 142:1979–1994. 2016. View Article : Google Scholar : PubMed/NCBI

29 

Wang J, Wei Q, Wang X, Tang S, Liu H, Zhang F, Mohammed MK, Huang J, Guo D, Lu M, et al: Transition to resistance: An unexpected role of the EMT in cancer chemoresistance. Genes Dis. 3:3–6. 2016. View Article : Google Scholar : PubMed/NCBI

30 

Smith B and Bhowmick N: Role of EMT in metastasis and therapy resistance. J Clin Med. 5:172016. View Article : Google Scholar : PubMed/NCBI

31 

Tang LH, Gonen M, Hedvat C, Modlin IM and Klimstra DS: Objective quantification of the Ki67 proliferative index in neuroendocrine tumors of the gastroenteropancreatic system: A comparison of digital image analysis with manual methods. Am J Surg Pathol. 36:1761–1770. 2012. View Article : Google Scholar : PubMed/NCBI

32 

Klimowicz AC, Bose P, Petrillo SK, Magliocco AM, Dort JC and Brockton NT: The prognostic impact of a combined carbonic anhydrase IX and Ki67 signature in oral squamous cell carcinoma. Br J Cancer. 109:1859–1866. 2013. View Article : Google Scholar : PubMed/NCBI

33 

Fukawa T and Kanayama H: Current knowledge of risk factors for testicular germ cell tumors. Int J Urol. 25:337–344. 2018. View Article : Google Scholar : PubMed/NCBI

34 

Rocha CRR, Silva MM, Quinet A, Cabral-Neto JB and Menck CFM: DNA repair pathways and cisplatin resistance: An intimate relationship. Clinics (Sao Paulo). 73 (Suppl 1):e478s2018. View Article : Google Scholar : PubMed/NCBI

35 

Brasseur K, Gévry N and Asselin E: Chemoresistance and targeted therapies in ovarian and endometrial cancers. Oncotarget. 8:4008–4042. 2017. View Article : Google Scholar : PubMed/NCBI

36 

Antony J, Thiery JP and Huang RYJ: Epithelial-to-mesenchymal transition: Lessons from development, insights into cancer and the potential of EMT-subtype based therapeutic intervention. Phys Biol. 16:0410042019. View Article : Google Scholar : PubMed/NCBI

37 

Wakileh GA, Bierholz P, Kotthoff M, Skowron MA, Bremmer F, Stephan A, Anbuhl SM, Heukers R, Smit MJ, Ströbel P and Nettersheim D: Molecular characterization of the CXCR4/CXCR7 axis in germ cell tumors and its targetability using nanobody-drug-conjugates. Exp Hematol Oncol. 12:962023. View Article : Google Scholar : PubMed/NCBI

38 

Bremmer F, Schallenberg S, Jarry H, Küffer S, Kaulfuss S, Burfeind P, Strauß A, Thelen P, Radzun HJ, Ströbel P, et al: Role of N-cadherin in proliferation, migration, and invasion of germ cell tumours. Oncotarget. 6:33426–33437. 2015. View Article : Google Scholar : PubMed/NCBI

39 

Classen J, Souchon R, Hehr T and Bamberg M: Treatment of early stage testicular seminoma. J Cancer Res Clin Oncol. 127:475–481. 2001. View Article : Google Scholar : PubMed/NCBI

40 

De Las Rivas J, Brozovic A, Izraely S, Casas-Pais A, Witz IP and Figueroa A: Cancer drug resistance induced by EMT: Novel therapeutic strategies. Arch Toxicol. 95:2279–2297. 2021. View Article : Google Scholar : PubMed/NCBI

41 

Lu W and Kang Y: Epithelial-mesenchymal plasticity in cancer progression and metastasis. Dev Cell. 49:361–374. 2019. View Article : Google Scholar : PubMed/NCBI

42 

Singh A and Settleman J: EMT, Cancer stem cells and drug resistance: An emerging axis of evil in the war on cancer. Oncogene. 29:4741–4751. 2010. View Article : Google Scholar : PubMed/NCBI

43 

Singh D and Siddique HR: Epithelial-to-mesenchymal transition in cancer progression: Unraveling the immunosuppressive module driving therapy resistance. Cancer Metastasis Rev. 43:155–173. 2024. View Article : Google Scholar : PubMed/NCBI

44 

Solheim O, Førsund M, Tropé CG, Kraggerud SM, Nesland JM and Davidson B: Epithelial-mesenchymal transition markers in malignant ovarian germ cell tumors. APMIS. 125:781–786. 2017. View Article : Google Scholar : PubMed/NCBI

45 

Schinke H, Pan M, Akyol M, Zhou J, Shi E, Kranz G, Libl D, Quadt T, Simon F, Canis M, et al: SLUG-related partial epithelial-to-mesenchymal transition is a transcriptomic prognosticator of head and neck cancer survival. Mol Oncol. 16:347–367. 2022. View Article : Google Scholar : PubMed/NCBI

46 

Kim H, Lee SB, Myung JK, Park JH, Park E, Il Kim D, Lee C, Kim Y, Park CM, Kim MB, et al: SLUG is a key regulator of Epithelial-Mesenchymal transition in pleomorphic adenoma. Lab Invest. 102:631–640. 2022. View Article : Google Scholar : PubMed/NCBI

47 

Noguchi S, Hirano K, Tanimoto N, Shimada T and Akiyoshi H: SLUG is upregulated and induces epithelial mesenchymal transition in canine oral squamous cell carcinoma. Vet Comp Oncol. 20:134–141. 2022. View Article : Google Scholar : PubMed/NCBI

48 

Önder E, Çil N, Seçme M and Mete GA: Effect of alpha lipoic acid on epithelial mesenchymal transition in SKOV-3 cells. Gene. 892:1478802024. View Article : Google Scholar : PubMed/NCBI

49 

Alves CC, Carneiro F, Hoefler H and Becker KF: Role of the epithelial-mesenchymal transition regulator Slug in primary human cancers. Front Biosci (Landmark Ed). 14:3035–3050. 2009. View Article : Google Scholar : PubMed/NCBI

50 

Shih JY and Yang PC: The EMT regulator slug and lung carcinogenesis. Carcinogenesis. 32:1299–1304. 2011. View Article : Google Scholar : PubMed/NCBI

51 

Shih JY, Tsai MF, Chang TH, Chang YL, Yuan A, Yu CJ, Lin SB, Liou GY, Lee ML, Chen JJ, et al: Transcription repressor slug promotes carcinoma invasion and predicts outcome of patients with lung adenocarcinoma. Clin Cancer Res. 11:8070–8078. 2005. View Article : Google Scholar : PubMed/NCBI

52 

Martin TA, Goyal A, Watkins G and Jiang WG: Expression of the transcription factors snail, slug, and twist and their clinical significance in human breast cancer. Ann Surg Oncol. 12:488–496. 2005. View Article : Google Scholar : PubMed/NCBI

53 

Zivotic M, Kovacevic S, Nikolic G, Mioljevic A, Filipovic I, Djordjevic M, Jovicic V, Topalovic N, Ilic K, Radojevic Skodric S, et al: SLUG and SNAIL as potential immunohistochemical biomarkers for renal cancer staging and survival. Int J Mol Sci. 24:122452023. View Article : Google Scholar : PubMed/NCBI

54 

Haslehurst AM, Koti M, Dharsee M, Nuin P, Evans K, Geraci J, Childs T, Chen J, Li J, Weberpals J, et al: EMT transcription factors snail and slug directly contribute to cisplatin resistance in ovarian cancer. BMC Cancer. 12:912012. View Article : Google Scholar : PubMed/NCBI

55 

Liang F, Ren C, Wang J, Wang S, Yang L, Han X, Chen Y, Tong G and Yang G: The crosstalk between STAT3 and p53/RAS signaling controls cancer cell metastasis and cisplatin resistance via the Slug/MAPK/PI3K/AKT-mediated regulation of EMT and autophagy. Oncogenesis. 8:592019. View Article : Google Scholar : PubMed/NCBI

56 

Oh SJ, Ahn EJ, Kim O, Kim D, Jung TY, Jung S, Lee JH, Kim KK, Kim H, Kim EH, et al: The role played by SLUG, an Epithelial-Mesenchymal transition factor, in invasion and therapeutic resistance of malignant glioma. Cell Mol Neurobiol. 39:769–782. 2019. View Article : Google Scholar : PubMed/NCBI

57 

Shen CJ, Kuo YL, Chen CC, Chen MJ and Cheng YM: MMP1 expression is activated by Slug and enhances multi-drug resistance (MDR) in breast cancer. PLoS One. 12:e01744872017. View Article : Google Scholar : PubMed/NCBI

58 

Chang L, Hu Y, Fu Y, Zhou T, You J, Du J, Zheng L, Cao J, Ying M, Dai X, et al: Targeting slug-mediated non-canonical activation of c-Met to overcome chemo-resistance in metastatic ovarian cancer cells. Acta Pharm Sin B. 9:484–495. 2019. View Article : Google Scholar : PubMed/NCBI

59 

Mancini M, Petta S, Iacobucci I, Salvestrini V, Barbieri E and Santucci MA: Zinc-finger transcription factor slug contributes to the survival advantage of chronic myeloid leukemia cells. Cell Signal. 22:1247–1253. 2010. View Article : Google Scholar : PubMed/NCBI

60 

Vitali R, Mancini C, Cesi V, Tanno B, Mancuso M, Bossi G, Zhang Y, Martinez RV, Calabretta B, Dominici C and Raschellà G: Slug (SNAI2) Down-Regulation by RNA interference facilitates apoptosis and inhibits invasive growth in neuroblastoma preclinical models. Clin Cancer Res. 14:4622–4630. 2008. View Article : Google Scholar : PubMed/NCBI

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Vieira Cardoso II, Nunes Rosa M, Antunes Moreno D, Barbosa Tufi LM, Pereira Ramos L, Bourdeth Pereira LA, Silva L, Soares Galvão JM, Tosi IC, Van Helvoort Lengert A, Van Helvoort Lengert A, et al: Cisplatin‑resistant germ cell tumor models: An exploration of the epithelial‑mesenchymal transition regulator <em>SLUG</em>. Mol Med Rep 30: 228, 2024.
APA
Vieira Cardoso, I.I., Nunes Rosa, M., Antunes Moreno, D., Barbosa Tufi, L.M., Pereira Ramos, L., Bourdeth Pereira, L.A. ... Tomazini Pinto, M. (2024). Cisplatin‑resistant germ cell tumor models: An exploration of the epithelial‑mesenchymal transition regulator <em>SLUG</em>. Molecular Medicine Reports, 30, 228. https://doi.org/10.3892/mmr.2024.13352
MLA
Vieira Cardoso, I. I., Nunes Rosa, M., Antunes Moreno, D., Barbosa Tufi, L. M., Pereira Ramos, L., Bourdeth Pereira, L. A., Silva, L., Soares Galvão, J. M., Tosi, I. C., Van Helvoort Lengert, A., Cavalcanti Da Cruz, M., Teixeira, S. A., Reis, R. M., Lopes, L. F., Tomazini Pinto, M."Cisplatin‑resistant germ cell tumor models: An exploration of the epithelial‑mesenchymal transition regulator <em>SLUG</em>". Molecular Medicine Reports 30.6 (2024): 228.
Chicago
Vieira Cardoso, I. I., Nunes Rosa, M., Antunes Moreno, D., Barbosa Tufi, L. M., Pereira Ramos, L., Bourdeth Pereira, L. A., Silva, L., Soares Galvão, J. M., Tosi, I. C., Van Helvoort Lengert, A., Cavalcanti Da Cruz, M., Teixeira, S. A., Reis, R. M., Lopes, L. F., Tomazini Pinto, M."Cisplatin‑resistant germ cell tumor models: An exploration of the epithelial‑mesenchymal transition regulator <em>SLUG</em>". Molecular Medicine Reports 30, no. 6 (2024): 228. https://doi.org/10.3892/mmr.2024.13352
Copy and paste a formatted citation
x
Spandidos Publications style
Vieira Cardoso II, Nunes Rosa M, Antunes Moreno D, Barbosa Tufi LM, Pereira Ramos L, Bourdeth Pereira LA, Silva L, Soares Galvão JM, Tosi IC, Van Helvoort Lengert A, Van Helvoort Lengert A, et al: Cisplatin‑resistant germ cell tumor models: An exploration of the epithelial‑mesenchymal transition regulator <em>SLUG</em>. Mol Med Rep 30: 228, 2024.
APA
Vieira Cardoso, I.I., Nunes Rosa, M., Antunes Moreno, D., Barbosa Tufi, L.M., Pereira Ramos, L., Bourdeth Pereira, L.A. ... Tomazini Pinto, M. (2024). Cisplatin‑resistant germ cell tumor models: An exploration of the epithelial‑mesenchymal transition regulator <em>SLUG</em>. Molecular Medicine Reports, 30, 228. https://doi.org/10.3892/mmr.2024.13352
MLA
Vieira Cardoso, I. I., Nunes Rosa, M., Antunes Moreno, D., Barbosa Tufi, L. M., Pereira Ramos, L., Bourdeth Pereira, L. A., Silva, L., Soares Galvão, J. M., Tosi, I. C., Van Helvoort Lengert, A., Cavalcanti Da Cruz, M., Teixeira, S. A., Reis, R. M., Lopes, L. F., Tomazini Pinto, M."Cisplatin‑resistant germ cell tumor models: An exploration of the epithelial‑mesenchymal transition regulator <em>SLUG</em>". Molecular Medicine Reports 30.6 (2024): 228.
Chicago
Vieira Cardoso, I. I., Nunes Rosa, M., Antunes Moreno, D., Barbosa Tufi, L. M., Pereira Ramos, L., Bourdeth Pereira, L. A., Silva, L., Soares Galvão, J. M., Tosi, I. C., Van Helvoort Lengert, A., Cavalcanti Da Cruz, M., Teixeira, S. A., Reis, R. M., Lopes, L. F., Tomazini Pinto, M."Cisplatin‑resistant germ cell tumor models: An exploration of the epithelial‑mesenchymal transition regulator <em>SLUG</em>". Molecular Medicine Reports 30, no. 6 (2024): 228. https://doi.org/10.3892/mmr.2024.13352
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