Abstract
Malign melanom, melanositlerden kaynaklanan agresif bir cilt kanseridir. Melanom hem genetik hem de çevresel faktörlerden kaynaklanan karmaşık bir hastalıktır. Melanomda, kanser kök hücreleri (CSC'ler), kendini yenileme ve farklılaşma yetenekleri nedeniyle tümör ilerlemesinde, terapötik dirençte ve nüksde önemli bir rol oynar. Sonic Hedgehog (SHH) sinyal yolağı CSC'lerin önemli bir düzenleyicisidir ve hücre farklılaşması ve çoğalması için gereklidir. Embriyonik gelişimdeki ve kanserlerdeki rolü bilindiğinden, SHH yolağı malign melanomda CSC davranışını önemli ölçüde etkileyerek tümörijenisiteyi, metastazı ve tedavilere direnci teşvik eder. Bu yolak, Gli transkripsiyon faktörlerini içeren kanonik mekanizmaları ve hücre göçünü ve hücre iskeleti organizasyonunu etkileyen kanonik olmayan mekanizmaları koordine eder. SHH yolağının hedeflenmesi, Smoothened (Smo) ve Gli proteinleri gibi bileşenlere odaklanan inhibitörlerle umut verici bir terapötik strateji olarak ortaya çıkmıştır. Bununla birlikte, bu inhibitörlere karşı direnç, yeni terapötik kombinasyonların daha fazla araştırılmasını gerektirmektedir. Mevcut araştırmalar, daha etkili ve uzun süreli yanıtlar için SHH inhibitörlerini immünoterapilerle birleştirmeye odaklanmaktadır. SHH süreçlerini bozan hedefe yönelik ilaçlar, karsinogenezin temel nedenlerini ortadan kaldırmaya ve melanom hastalarının hayatta kalma oranlarını artırmaya çalışmaktadır.
Keywords
Malign Melanom Kanser Kök Hücreleri (CSC) Sonic Hedgehog (SHH) Sinyal Yolağı Terapötik Direnç Metastaz
Ethical Statement
Derleme çalışmasıdır. Etik kurul belgesine ihtiyaç yoktur.
Supporting Institution
Ege Üniversitesi Bilimsel Araştırma Projeleri Koordinasyon Birimi
Project Number
20785
Thanks
Ege Üniversitesi Bilimsel Araştırma Projeleri Koordinasyon Birimi
References
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- Pfeifer GP. Correction to: Mechanisms of UV-induced mutations and skin cancer. Genome Instab Dis [Internet]. 2021;2(4):262. Available at: https://doi.org/10.1007/s42764-021-00037-y
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- Wouters J, Stas M, Gremeaux L, Govaere O, Van den Broeck A, Maes H, vd. The human melanoma side population displays molecular and functional characteristics of enriched chemoresistance and tumorigenesis. PLoS One. 2013;8(10):e76550.
- Kozovska Z, Gabrisova V, Kucerova L. Malignant melanoma: diagnosis, treatment and cancer stem cells. Neoplasma. 2016;63(4):510–7.
- Murphy GF, Wilson BJ, Girouard SD, Frank NY, Frank MH. Stem cells and targeted approaches to melanoma cure. Mol Aspects Med. Ekim 2014;39:33–49.
- Zeng Z, Fu M, Hu Y, Wei Y, Wei X, Luo M. Regulation and signaling pathways in cancer stem cells: implications for targeted therapy for cancer. Mol Cancer [Internet]. 2023;22(1):172. Available at: https://doi.org/10.1186/s12943-023-01877-w
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- Al Hmada Y, Brodell RT, Kharouf N, Flanagan TW, Alamodi AA, Hassan S-Y, vd. Mechanisms of Melanoma Progression and Treatment Resistance: Role of Cancer Stem-like Cells. C. 16, Cancers. 2024.
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- Schatton T, Frank MH. Cancer stem cells and human malignant melanoma. Pigment Cell Melanoma Res. Şubat 2008;21(1):39–55.
- Giuntini G, Coppola F, Falsini A, Filippi I, Monaci S, Naldini A, vd. Role of the Hedgehog Pathway and CAXII in Controlling Melanoma Cell Migration and Invasion in Hypoxia. C. 14, Cancers. 2022.
- Stecca B, Mas C, Clement V, Zbinden M, Correa R, Piguet V, vd. Melanomas require HEDGEHOG-GLI signaling regulated by interactions between GLI1 and the RAS-MEK/AKT pathways. Proc Natl Acad Sci [Internet]. 03 Nisan 2007;104(14):5895–900. Available at: https://doi.org/10.1073/pnas.0700776104
- Dunjic M, Lukic N, Djordjevic B, Uzelac B, Ostojic N, Supic G. GLI-1 polymorphisms of Hedgehog pathway as novel risk and prognostic biomarkers in melanoma patients. Melanoma Res [Internet]. 2022;32(1). Available at: https://journals.lww.com/melanomaresearch/Fulltext/2022/02000/GLI_1_polymorphisms_of_Hedgehog_pathway_as_novel.2.aspx
- Sabbatino F, Wang Y, Wang X, Flaherty KT, Yu L, Pepin D, vd. PDGFRα up-regulation mediated by Sonic Hedgehog pathway activation leads to BRAF inhibitor resistance in melanoma cells with BRAF mutation. Oncotarget; Vol 5, No 7 [Internet]. 2014; Available at: https://www.oncotarget.com/article/1878/text/
- Li X, Li Y, Li S, Li H, Yang C, Lin J. The role of Shh signalling pathway in central nervous system development and related diseases. Cell Biochem Funct. Mart 2021;39(2):180–9.
- Carballo GB, Honorato JR, De Lopes GPF, Spohr TCLDSE. A highlight on Sonic hedgehog pathway. C. 16, Cell Communication and Signaling. 2018.
- Yang Z, Zhang C, Qi W, Cui Y, Xuan Y. GLI1 promotes cancer stemness through intracellular signaling pathway PI3K/Akt/NFκB in colorectal adenocarcinoma. Exp Cell Res. Aralık 2018;373(1–2):145–54.
- Shi Y, He G, Lee W-C, McKenzie JA, Silva MJ, Long F. Gli1 identifies osteogenic progenitors for bone formation and fracture repair. Nat Commun [Internet]. 2017;8(1):2043. Available at: https://doi.org/10.1038/s41467-017-02171-2
- Kwon Y-J, Hurst DR, Steg AD, Yuan K, Vaidya KS, Welch DR, vd. Gli1 enhances migration and invasion via up-regulation of MMP-11 and promotes metastasis in ERα negative breast cancer cell lines. Clin Exp Metastasis. Haziran 2011;28(5):437–49.
- Lin Y, Guo L. GLI1 is involved in HIF-1α-induced migration, invasion, and epithelial-mesenchymal transition in glioma cells. Folia Histochem Cytobiol. 2022;60(2):156–66.
- Lin Y, Wu Z. Hypoxia-inducible factor 1α (HIF-1α)-activated Gli1 induces invasion and EMT by H3K4 methylation in glioma cells. Oncologie. 2023;25(1):71–9.
- Ozdil B, Avci CB, Kocaturk DC, Gorgulu V, Uysal A, Guler G, vd. Modulating cancer stem cell characteristics in CD133+ melanoma cells through HIF1α, KLF4, and SHH silencing. 2024; Available at: https://www.researchsquare.com/article/rs-4808028/v1
- Rimkus TK, Carpenter RL, Qasem S, Chan M, Lo HW. Targeting the sonic hedgehog signaling pathway: Review of smoothened and GLI inhibitors. C. 8, Cancers. 2016.
- Cerchia C, Lavecchia A. Small Molecule Drugs and Targeted Therapy for Melanoma: Current Strategies and Future Directions. Curr Med Chem. 2017;24(21):2312–44.
- Holland JD, Klaus A, Garratt AN, Birchmeier W. Wnt signaling in stem and cancer stem cells. Curr Opin Cell Biol. 2013;25(2):254–64.
- Wend P, Holland JD, Ziebold U, Birchmeier W. Wnt signaling in stem and cancer stem cells. Içinde: Seminars in cell & developmental biology. Elsevier; 2010. s. 855–63.
- Kumar D, Kumar S, Gorain M, Tomar D, Patil HS, Radharani NN V, vd. Notch1-MAPK Signaling Axis Regulates CD133(+) Cancer Stem Cell-Mediated Melanoma Growth and Angiogenesis. J Invest Dermatol. Aralık 2016;136(12):2462–74.
- Du Y, Shao H, Moller M, Prokupets R, Tse YT, Liu Z-J. Intracellular Notch1 Signaling in Cancer-Associated Fibroblasts Dictates the Plasticity and Stemness of Melanoma Stem/Initiating Cells. Stem Cells [Internet]. 01 Temmuz 2019;37(7):865–75. Available at: https://doi.org/10.1002/stem.3013
- Venkatesh V, Nataraj R, Thangaraj GS, Karthikeyan M, Gnanasekaran A, Kaginelli SB, vd. Targeting Notch signalling pathway of cancer stem cells. Stem cell Investig [Internet]. Mart 2018;5:5. Available at: https://pubmed.ncbi.nlm.nih.gov/29682512
- Moreno-Londoño AP, Robles-Flores M. Functional Roles of CD133: More than Stemness Associated Factor Regulated by the Microenvironment. Stem cell Rev reports. Ocak 2024;20(1):25–51.
- Zhao J, Li R, Li J, Chen Z, Lin Z, Zhang B, vd. CAFs-derived SCUBE1 promotes malignancy and stemness through the Shh/Gli1 pathway in hepatocellular carcinoma. J Transl Med [Internet]. 2022;20(1):520. Available at: https://doi.org/10.1186/s12967-022-03689-w
- Lospinoso Severini L, Ghirga F, Bufalieri F, Quaglio D, Infante P, Di Marcotullio L. The SHH/GLI signaling Volume 64 Issue 2, June 2025 / Cilt 64 Sayı 2, Haziran 2025 423 pathway: a therapeutic target for medulloblastoma. Expert Opin Ther Targets. Kasım 2020;24(11):1159–81.
- Najem A, Krayem M, Perdix A, Kerger J, Awada A, Journe F, vd. New Drug Combination Strategies in Melanoma: Current Status and Future Directions. Anticancer Res [Internet]. 01 Kasım 2017;37(11):5941 LP – 5953. Available at: http://ar.iiarjournals.org/content/37/11/5941.abstract
- Lear JT, Morris LM, Ness DB, Lewis LD. Pharmacokinetics and pharmacodynamics of Hedgehog pathway inhibitors used in the treatment of advanced or treatment-refractory basal cell carcinoma. Expert Rev Clin Pharmacol. 2023;16(12):1211–20.
Abstract
Malignant melanoma is an aggressive skin cancer arising from melanocytes. Melanoma is a complex disease both sourced from genetics and environmental factors. Within melanoma, cancer stem cells (CSCs) play a crucial role in tumor progression, therapeutic resistance, and recurrence due to their capabilities for self-renewal and differentiation. The Sonic Hedgehog (SHH) signaling pathway is an important regulator of CSCs and is essential for cell differentiation and proliferation. Due to it is known role in embryonic development and involvement in cancers, SHH pathway significantly affects CSC behavior in malignant melanoma, promoting tumorigenicity, metastasis, and resistance to therapies. This pathway coordinates canonical mechanisms involving Gli transcription factors and non-canonical mechanisms affecting cell migration and cytoskeletal organization. Targeting the SHH pathway has emerged as a promising therapeutic strategy, with inhibitors focusing on components like Smoothened (Smo) and Gli proteins. However, resistance to these inhibitors necessitates further exploration of novel therapeutic combinations. Current research focuses on combining SHH inhibitors with immunotherapies for more effective, long-lasting responses. Targeted medicines, which disrupt SHH processes, attempt to eliminate the fundamental causes of carcinogenesis and increase melanoma patient survival rates.
Keywords
Malignant Melanoma Cancer Stem Cells (CSC) Sonic Hedgehog (SHH) Signaling Pathway Therapeutic Resistance Metastasis
Ethical Statement
It is a review study. There is no need for an ethics committee document.
Supporting Institution
Scientific Research Projects Coordination Unit at Ege University
Project Number
20785
Thanks
Scientific Research Projects Coordination Unit at Ege University
References
- Pandiani C, Béranger GE, Leclerc J, Ballotti R, Bertolotto C. Focus on cutaneous and uveal melanoma specificities. Genes Dev. Nisan 2017;31(8):724–43.
- Hessler M, Jalilian E, Xu Q, Reddy S, Horton L, Elkin K, vd. Melanoma biomarkers and their potential application for in vivo diagnostic imaging modalities. Int J Mol Sci. 2020;21(24):9583.
- Moran B, Silva R, Perry AS, Gallagher WM. Epigenetics of malignant melanoma. Semin Cancer Biol [Internet]. 2018;51:80–8. Available at: https://www.sciencedirect.com/science/article/pii/S1044579X1730130X
- Apalla Z, Lallas A, Sotiriou E, Lazaridou E, Ioannides D. Epidemiological trends in skin cancer. Dermatol Pract Concept [Internet]. 30 Nisan 2017;7(2):1–6. Available at: https://pubmed.ncbi.nlm.nih.gov/28515985
- Liu Z, Wang H, Sun C, He Y, Xia T, Wang J, vd. ZWZ-3, a Fluorescent Probe Targeting Mitochondria for Melanoma Imaging and Therapy [Internet]. C. 13, Frontiers in Pharmacology . 2022. Available at: https://www.frontiersin.org/article/10.3389/fphar.2022.829684
- Jin S-G, Padron F, Pfeifer GP. UVA Radiation, DNA Damage, and Melanoma. ACS omega. Eylül 2022;7(37):32936–48.
- Pfeifer GP. Correction to: Mechanisms of UV-induced mutations and skin cancer. Genome Instab Dis [Internet]. 2021;2(4):262. Available at: https://doi.org/10.1007/s42764-021-00037-y
- Chu X, Tian W, Ning J, Xiao G, Zhou Y, Wang Z, vd. Cancer stem cells: advances in knowledge and implications for cancer therapy. Signal Transduct Target Ther [Internet]. 2024;9(1):170. Available at: https://doi.org/10.1038/s41392-024-01851-y
- Perego M, Tortoreto M, Tragni G, Mariani L, Deho P, Carbone A, vd. Heterogeneous Phenotype of Human Melanoma Cells with In Vitro and In Vivo Features of Tumor-Initiating Cells. J Invest Dermatol. 2010;130(7):1877–86.
- Wouters J, Stas M, Gremeaux L, Govaere O, Van den Broeck A, Maes H, vd. The human melanoma side population displays molecular and functional characteristics of enriched chemoresistance and tumorigenesis. PLoS One. 2013;8(10):e76550.
- Kozovska Z, Gabrisova V, Kucerova L. Malignant melanoma: diagnosis, treatment and cancer stem cells. Neoplasma. 2016;63(4):510–7.
- Murphy GF, Wilson BJ, Girouard SD, Frank NY, Frank MH. Stem cells and targeted approaches to melanoma cure. Mol Aspects Med. Ekim 2014;39:33–49.
- Zeng Z, Fu M, Hu Y, Wei Y, Wei X, Luo M. Regulation and signaling pathways in cancer stem cells: implications for targeted therapy for cancer. Mol Cancer [Internet]. 2023;22(1):172. Available at: https://doi.org/10.1186/s12943-023-01877-w
- Marzagalli M, Raimondi M, Fontana F, Montagnani Marelli M, Moretti RM, Limonta P. Cellular and molecular biology of cancer stem cells in melanoma: Possible therapeutic implications. Semin Cancer Biol. Aralık 2019;59:221–35.
- Al Hmada Y, Brodell RT, Kharouf N, Flanagan TW, Alamodi AA, Hassan S-Y, vd. Mechanisms of Melanoma Progression and Treatment Resistance: Role of Cancer Stem-like Cells. C. 16, Cancers. 2024.
- Parmiani G. Melanoma Cancer Stem Cells: Markers and Functions. Cancers (Basel). Mart 2016;8(3).
- Schatton T, Frank MH. Cancer stem cells and human malignant melanoma. Pigment Cell Melanoma Res. Şubat 2008;21(1):39–55.
- Giuntini G, Coppola F, Falsini A, Filippi I, Monaci S, Naldini A, vd. Role of the Hedgehog Pathway and CAXII in Controlling Melanoma Cell Migration and Invasion in Hypoxia. C. 14, Cancers. 2022.
- Stecca B, Mas C, Clement V, Zbinden M, Correa R, Piguet V, vd. Melanomas require HEDGEHOG-GLI signaling regulated by interactions between GLI1 and the RAS-MEK/AKT pathways. Proc Natl Acad Sci [Internet]. 03 Nisan 2007;104(14):5895–900. Available at: https://doi.org/10.1073/pnas.0700776104
- Dunjic M, Lukic N, Djordjevic B, Uzelac B, Ostojic N, Supic G. GLI-1 polymorphisms of Hedgehog pathway as novel risk and prognostic biomarkers in melanoma patients. Melanoma Res [Internet]. 2022;32(1). Available at: https://journals.lww.com/melanomaresearch/Fulltext/2022/02000/GLI_1_polymorphisms_of_Hedgehog_pathway_as_novel.2.aspx
- Sabbatino F, Wang Y, Wang X, Flaherty KT, Yu L, Pepin D, vd. PDGFRα up-regulation mediated by Sonic Hedgehog pathway activation leads to BRAF inhibitor resistance in melanoma cells with BRAF mutation. Oncotarget; Vol 5, No 7 [Internet]. 2014; Available at: https://www.oncotarget.com/article/1878/text/
- Li X, Li Y, Li S, Li H, Yang C, Lin J. The role of Shh signalling pathway in central nervous system development and related diseases. Cell Biochem Funct. Mart 2021;39(2):180–9.
- Carballo GB, Honorato JR, De Lopes GPF, Spohr TCLDSE. A highlight on Sonic hedgehog pathway. C. 16, Cell Communication and Signaling. 2018.
- Yang Z, Zhang C, Qi W, Cui Y, Xuan Y. GLI1 promotes cancer stemness through intracellular signaling pathway PI3K/Akt/NFκB in colorectal adenocarcinoma. Exp Cell Res. Aralık 2018;373(1–2):145–54.
- Shi Y, He G, Lee W-C, McKenzie JA, Silva MJ, Long F. Gli1 identifies osteogenic progenitors for bone formation and fracture repair. Nat Commun [Internet]. 2017;8(1):2043. Available at: https://doi.org/10.1038/s41467-017-02171-2
- Kwon Y-J, Hurst DR, Steg AD, Yuan K, Vaidya KS, Welch DR, vd. Gli1 enhances migration and invasion via up-regulation of MMP-11 and promotes metastasis in ERα negative breast cancer cell lines. Clin Exp Metastasis. Haziran 2011;28(5):437–49.
- Lin Y, Guo L. GLI1 is involved in HIF-1α-induced migration, invasion, and epithelial-mesenchymal transition in glioma cells. Folia Histochem Cytobiol. 2022;60(2):156–66.
- Lin Y, Wu Z. Hypoxia-inducible factor 1α (HIF-1α)-activated Gli1 induces invasion and EMT by H3K4 methylation in glioma cells. Oncologie. 2023;25(1):71–9.
- Ozdil B, Avci CB, Kocaturk DC, Gorgulu V, Uysal A, Guler G, vd. Modulating cancer stem cell characteristics in CD133+ melanoma cells through HIF1α, KLF4, and SHH silencing. 2024; Available at: https://www.researchsquare.com/article/rs-4808028/v1
- Rimkus TK, Carpenter RL, Qasem S, Chan M, Lo HW. Targeting the sonic hedgehog signaling pathway: Review of smoothened and GLI inhibitors. C. 8, Cancers. 2016.
- Cerchia C, Lavecchia A. Small Molecule Drugs and Targeted Therapy for Melanoma: Current Strategies and Future Directions. Curr Med Chem. 2017;24(21):2312–44.
- Holland JD, Klaus A, Garratt AN, Birchmeier W. Wnt signaling in stem and cancer stem cells. Curr Opin Cell Biol. 2013;25(2):254–64.
- Wend P, Holland JD, Ziebold U, Birchmeier W. Wnt signaling in stem and cancer stem cells. Içinde: Seminars in cell & developmental biology. Elsevier; 2010. s. 855–63.
- Kumar D, Kumar S, Gorain M, Tomar D, Patil HS, Radharani NN V, vd. Notch1-MAPK Signaling Axis Regulates CD133(+) Cancer Stem Cell-Mediated Melanoma Growth and Angiogenesis. J Invest Dermatol. Aralık 2016;136(12):2462–74.
- Du Y, Shao H, Moller M, Prokupets R, Tse YT, Liu Z-J. Intracellular Notch1 Signaling in Cancer-Associated Fibroblasts Dictates the Plasticity and Stemness of Melanoma Stem/Initiating Cells. Stem Cells [Internet]. 01 Temmuz 2019;37(7):865–75. Available at: https://doi.org/10.1002/stem.3013
- Venkatesh V, Nataraj R, Thangaraj GS, Karthikeyan M, Gnanasekaran A, Kaginelli SB, vd. Targeting Notch signalling pathway of cancer stem cells. Stem cell Investig [Internet]. Mart 2018;5:5. Available at: https://pubmed.ncbi.nlm.nih.gov/29682512
- Moreno-Londoño AP, Robles-Flores M. Functional Roles of CD133: More than Stemness Associated Factor Regulated by the Microenvironment. Stem cell Rev reports. Ocak 2024;20(1):25–51.
- Zhao J, Li R, Li J, Chen Z, Lin Z, Zhang B, vd. CAFs-derived SCUBE1 promotes malignancy and stemness through the Shh/Gli1 pathway in hepatocellular carcinoma. J Transl Med [Internet]. 2022;20(1):520. Available at: https://doi.org/10.1186/s12967-022-03689-w
- Lospinoso Severini L, Ghirga F, Bufalieri F, Quaglio D, Infante P, Di Marcotullio L. The SHH/GLI signaling Volume 64 Issue 2, June 2025 / Cilt 64 Sayı 2, Haziran 2025 423 pathway: a therapeutic target for medulloblastoma. Expert Opin Ther Targets. Kasım 2020;24(11):1159–81.
- Najem A, Krayem M, Perdix A, Kerger J, Awada A, Journe F, vd. New Drug Combination Strategies in Melanoma: Current Status and Future Directions. Anticancer Res [Internet]. 01 Kasım 2017;37(11):5941 LP – 5953. Available at: http://ar.iiarjournals.org/content/37/11/5941.abstract
- Lear JT, Morris LM, Ness DB, Lewis LD. Pharmacokinetics and pharmacodynamics of Hedgehog pathway inhibitors used in the treatment of advanced or treatment-refractory basal cell carcinoma. Expert Rev Clin Pharmacol. 2023;16(12):1211–20.
Details
| Primary Language | English |
|---|---|
| Subjects | Cancer Cell Biology |
| Journal Section | Reviews |
| Authors | |
| Project Number | 20785 |
| Publication Date | June 10, 2025 |
| Submission Date | September 24, 2024 |
| Acceptance Date | January 27, 2025 |
| Published in Issue | Year 2025 Volume: 64 Issue: 2 |
