Advancing Radiobiology: Investigating the Effects of Photon, Proton, and Carbon-Ion Irradiation on PANC-1 Cells in 2D and 3D Tumor Models

<b>Introduction:</b> Pancreatic cancer (PC) is one of the most aggressive and lethal malignancies, calling for enhanced research. Pancreatic ductal adenocarcinoma (PDAC) represents 70–80% of all cases and is known for its resistance to conventional therapies. Carbon-ion radiotherapy (CIR...

Full description

Saved in:
Bibliographic Details
Main Authors: Alexandra Charalampopoulou, Amelia Barcellini, Giuseppe Magro, Anna Bellini, Sara Sevan Borgna, Giorgia Fulgini, Giovanni Battista Ivaldi, Alessio Mereghetti, Ester Orlandi, Marco Giuseppe Pullia, Simone Savazzi, Paola Tabarelli De Fatis, Gaia Volpi, Angelica Facoetti
Format: Article
Language:English
Published: MDPI AG 2025-01-01
Series:Current Oncology
Subjects:
Online Access:https://www.mdpi.com/1718-7729/32/1/49
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1832588693073821696
author Alexandra Charalampopoulou
Amelia Barcellini
Giuseppe Magro
Anna Bellini
Sara Sevan Borgna
Giorgia Fulgini
Giovanni Battista Ivaldi
Alessio Mereghetti
Ester Orlandi
Marco Giuseppe Pullia
Simone Savazzi
Paola Tabarelli De Fatis
Gaia Volpi
Angelica Facoetti
author_facet Alexandra Charalampopoulou
Amelia Barcellini
Giuseppe Magro
Anna Bellini
Sara Sevan Borgna
Giorgia Fulgini
Giovanni Battista Ivaldi
Alessio Mereghetti
Ester Orlandi
Marco Giuseppe Pullia
Simone Savazzi
Paola Tabarelli De Fatis
Gaia Volpi
Angelica Facoetti
author_sort Alexandra Charalampopoulou
collection DOAJ
description <b>Introduction:</b> Pancreatic cancer (PC) is one of the most aggressive and lethal malignancies, calling for enhanced research. Pancreatic ductal adenocarcinoma (PDAC) represents 70–80% of all cases and is known for its resistance to conventional therapies. Carbon-ion radiotherapy (CIRT) has emerged as a promising approach due to its ability to deliver highly localized doses and unique radiobiological properties compared to X-rays. In vitro radiobiology has relied on two-dimensional (2D) cell culture models so far; however, these are not sufficient to replicate the complexity of the in vivo tumor architecture. Three-dimensional (3D) models become a paradigm shift, surpassing the constraints of traditional models by accurately re-creating morphological, histological, and genetic characteristics as well as the interaction of tumour cells with the microenvironment. <b>Materials and Methods:</b> This study investigates the survival of pancreatic cancer cells in both 2D and spheroids, a 3D model, following photon, proton, and carbon-ion irradiation by means of clonogenic, MTT, spheroid growth, and vitality assays. <b>Results:</b> Our results demonstrate that carbon ions are more efficient in reducing cancer cell survival compared to photons and protons. In 2D cultures, carbon-ion irradiation reduced cell survival to approximately 15%, compared to 45% with photons and 30% with protons. In the 3D culture model, spheroid growth was similarly inhibited by carbon-ion irradiation; however, the overall survival rates were higher across all irradiation modalities compared to the 2D cultures. Carbon ions consistently showed the highest efficacy in reducing cell viability in both models. <b>Conclusions:</b> Our research highlights the pivotal role of 3D models in unraveling the complexities of pancreatic cancer radiobiology, offering new avenues for designing more effective and precise treatment protocols.
format Article
id doaj-art-45e06e3d6f544a4db4f4a2b8f45e1109
institution Kabale University
issn 1198-0052
1718-7729
language English
publishDate 2025-01-01
publisher MDPI AG
record_format Article
series Current Oncology
spelling doaj-art-45e06e3d6f544a4db4f4a2b8f45e11092025-01-24T13:28:29ZengMDPI AGCurrent Oncology1198-00521718-77292025-01-013214910.3390/curroncol32010049Advancing Radiobiology: Investigating the Effects of Photon, Proton, and Carbon-Ion Irradiation on PANC-1 Cells in 2D and 3D Tumor ModelsAlexandra Charalampopoulou0Amelia Barcellini1Giuseppe Magro2Anna Bellini3Sara Sevan Borgna4Giorgia Fulgini5Giovanni Battista Ivaldi6Alessio Mereghetti7Ester Orlandi8Marco Giuseppe Pullia9Simone Savazzi10Paola Tabarelli De Fatis11Gaia Volpi12Angelica Facoetti13Radiobiology Unit, Research and Development Department, CNAO National Center for Oncological Hadrontherapy, 27100 Pavia, ItalyRadiation Oncology Unit, Clinical Department, CNAO National Center for Oncological Hadrontherapy, 27100 Pavia, ItalyMedical Physics Unit, Clinical Department, CNAO National Center for Oncological Hadrontherapy, 27100 Pavia, ItalyRadiobiology Unit, Research and Development Department, CNAO National Center for Oncological Hadrontherapy, 27100 Pavia, ItalyRadiobiology Unit, Research and Development Department, CNAO National Center for Oncological Hadrontherapy, 27100 Pavia, ItalyRadiobiology Unit, Research and Development Department, CNAO National Center for Oncological Hadrontherapy, 27100 Pavia, ItalyRadiation Oncology Department, Clinical Scientific Institutes Maugeri IRCCS, 27100 Pavia, ItalyResearch and Development Department, CNAO National Center for Oncological Hadrontherapy, 27100 Pavia, ItalyRadiation Oncology Unit, Clinical Department, CNAO National Center for Oncological Hadrontherapy, 27100 Pavia, ItalyResearch and Development Department, CNAO National Center for Oncological Hadrontherapy, 27100 Pavia, ItalyResearch and Development Department, CNAO National Center for Oncological Hadrontherapy, 27100 Pavia, ItalyMedical Physics Unit, Clinical Scientific Institutes Maugeri IRCCS, 27100 Pavia, ItalyRadiobiology Unit, Research and Development Department, CNAO National Center for Oncological Hadrontherapy, 27100 Pavia, ItalyRadiobiology Unit, Research and Development Department, CNAO National Center for Oncological Hadrontherapy, 27100 Pavia, Italy<b>Introduction:</b> Pancreatic cancer (PC) is one of the most aggressive and lethal malignancies, calling for enhanced research. Pancreatic ductal adenocarcinoma (PDAC) represents 70–80% of all cases and is known for its resistance to conventional therapies. Carbon-ion radiotherapy (CIRT) has emerged as a promising approach due to its ability to deliver highly localized doses and unique radiobiological properties compared to X-rays. In vitro radiobiology has relied on two-dimensional (2D) cell culture models so far; however, these are not sufficient to replicate the complexity of the in vivo tumor architecture. Three-dimensional (3D) models become a paradigm shift, surpassing the constraints of traditional models by accurately re-creating morphological, histological, and genetic characteristics as well as the interaction of tumour cells with the microenvironment. <b>Materials and Methods:</b> This study investigates the survival of pancreatic cancer cells in both 2D and spheroids, a 3D model, following photon, proton, and carbon-ion irradiation by means of clonogenic, MTT, spheroid growth, and vitality assays. <b>Results:</b> Our results demonstrate that carbon ions are more efficient in reducing cancer cell survival compared to photons and protons. In 2D cultures, carbon-ion irradiation reduced cell survival to approximately 15%, compared to 45% with photons and 30% with protons. In the 3D culture model, spheroid growth was similarly inhibited by carbon-ion irradiation; however, the overall survival rates were higher across all irradiation modalities compared to the 2D cultures. Carbon ions consistently showed the highest efficacy in reducing cell viability in both models. <b>Conclusions:</b> Our research highlights the pivotal role of 3D models in unraveling the complexities of pancreatic cancer radiobiology, offering new avenues for designing more effective and precise treatment protocols.https://www.mdpi.com/1718-7729/32/1/492D cell cultures3D cell culture modelsconventional radiotherapyhadrontherapypancreatic cancerradiobiology
spellingShingle Alexandra Charalampopoulou
Amelia Barcellini
Giuseppe Magro
Anna Bellini
Sara Sevan Borgna
Giorgia Fulgini
Giovanni Battista Ivaldi
Alessio Mereghetti
Ester Orlandi
Marco Giuseppe Pullia
Simone Savazzi
Paola Tabarelli De Fatis
Gaia Volpi
Angelica Facoetti
Advancing Radiobiology: Investigating the Effects of Photon, Proton, and Carbon-Ion Irradiation on PANC-1 Cells in 2D and 3D Tumor Models
Current Oncology
2D cell cultures
3D cell culture models
conventional radiotherapy
hadrontherapy
pancreatic cancer
radiobiology
title Advancing Radiobiology: Investigating the Effects of Photon, Proton, and Carbon-Ion Irradiation on PANC-1 Cells in 2D and 3D Tumor Models
title_full Advancing Radiobiology: Investigating the Effects of Photon, Proton, and Carbon-Ion Irradiation on PANC-1 Cells in 2D and 3D Tumor Models
title_fullStr Advancing Radiobiology: Investigating the Effects of Photon, Proton, and Carbon-Ion Irradiation on PANC-1 Cells in 2D and 3D Tumor Models
title_full_unstemmed Advancing Radiobiology: Investigating the Effects of Photon, Proton, and Carbon-Ion Irradiation on PANC-1 Cells in 2D and 3D Tumor Models
title_short Advancing Radiobiology: Investigating the Effects of Photon, Proton, and Carbon-Ion Irradiation on PANC-1 Cells in 2D and 3D Tumor Models
title_sort advancing radiobiology investigating the effects of photon proton and carbon ion irradiation on panc 1 cells in 2d and 3d tumor models
topic 2D cell cultures
3D cell culture models
conventional radiotherapy
hadrontherapy
pancreatic cancer
radiobiology
url https://www.mdpi.com/1718-7729/32/1/49
work_keys_str_mv AT alexandracharalampopoulou advancingradiobiologyinvestigatingtheeffectsofphotonprotonandcarbonionirradiationonpanc1cellsin2dand3dtumormodels
AT ameliabarcellini advancingradiobiologyinvestigatingtheeffectsofphotonprotonandcarbonionirradiationonpanc1cellsin2dand3dtumormodels
AT giuseppemagro advancingradiobiologyinvestigatingtheeffectsofphotonprotonandcarbonionirradiationonpanc1cellsin2dand3dtumormodels
AT annabellini advancingradiobiologyinvestigatingtheeffectsofphotonprotonandcarbonionirradiationonpanc1cellsin2dand3dtumormodels
AT sarasevanborgna advancingradiobiologyinvestigatingtheeffectsofphotonprotonandcarbonionirradiationonpanc1cellsin2dand3dtumormodels
AT giorgiafulgini advancingradiobiologyinvestigatingtheeffectsofphotonprotonandcarbonionirradiationonpanc1cellsin2dand3dtumormodels
AT giovannibattistaivaldi advancingradiobiologyinvestigatingtheeffectsofphotonprotonandcarbonionirradiationonpanc1cellsin2dand3dtumormodels
AT alessiomereghetti advancingradiobiologyinvestigatingtheeffectsofphotonprotonandcarbonionirradiationonpanc1cellsin2dand3dtumormodels
AT esterorlandi advancingradiobiologyinvestigatingtheeffectsofphotonprotonandcarbonionirradiationonpanc1cellsin2dand3dtumormodels
AT marcogiuseppepullia advancingradiobiologyinvestigatingtheeffectsofphotonprotonandcarbonionirradiationonpanc1cellsin2dand3dtumormodels
AT simonesavazzi advancingradiobiologyinvestigatingtheeffectsofphotonprotonandcarbonionirradiationonpanc1cellsin2dand3dtumormodels
AT paolatabarellidefatis advancingradiobiologyinvestigatingtheeffectsofphotonprotonandcarbonionirradiationonpanc1cellsin2dand3dtumormodels
AT gaiavolpi advancingradiobiologyinvestigatingtheeffectsofphotonprotonandcarbonionirradiationonpanc1cellsin2dand3dtumormodels
AT angelicafacoetti advancingradiobiologyinvestigatingtheeffectsofphotonprotonandcarbonionirradiationonpanc1cellsin2dand3dtumormodels