Fluorescence imaging analysis of the glioma microenvironment

Xuwen Peng; Yuzhou Chen; Yuke Wang; Shuhong Qi

doi:10.1142/S1793545822450055

[1] M. Weller, W. Wick, K. Aldape, M. Brada, M. Berger, S. M. Pfister, R. Nishikawa, M. Rosenthal, P. Y. Wen, R. Stupp, G. Reifenberger. Glioma. Nat. Rev. Dis. Prim., 1, 15017(2015).

[2] D. N. Louis, A. Perry, P. Wesseling, D. J. Brat, I. A. Cree, D. Figarella-Branger, C. Hawkins, H. K. Ng, S. M. Pfister, G. Reifenberger, R. Soffietti, A. von Deimling, D. W. Ellison. The 2021 WHO Classification of Gliomas of the Central Nervous System: A summary. Neuro Oncol., 23, 1231-1251(2021).

[3] A. Abdurashitov, V. Tuchin, O. Semyachkina-Glushkovskaya. Photodynamic therapy of brain tumors and novel optical coherence tomography strategies for in vivo monitoring of cerebral fluid dynamics. J. Innov. Opt. Health Sci., 13, 2030004(2020).

[4] D. F. Quail, J. A. Joyce. The microenvironmental landscape of brain tumors. Cancer Cell, 31, 326-341(2017).

[5] A. Gieryng, D. Pszczolkowska, K. A. Walentynowicz, W. D. Rajan, B. Kaminska. Immune microenvironment of gliomas. Lab Invest, 97, 498-518(2017).

[6] B. M. Andersen, C. Faust Akl, M. A. Wheeler, E. A. Chiocca, D. A. Reardon, F. J. Quintana. Glial and myeloid heterogeneity in the brain tumour microenvironment. Nat. Rev. Cancer, 21, 786-802(2021).

[7] A. Vollmann-Zwerenz, V. Leidgens, G. Feliciello, C. A. Klein, P. Hau. Tumor cell invasion in glioblastoma. Int. J. Mol. Sci., 21, 1932(2020).

[8] S. Tamai, T. Ichinose, T. Tsutsui, S. Tanaka, F. Garaeva, H. Sabit, M. Nakada. Tumor microenvironment in glioma invasion. Brain Sci., 12, 505(2022).

[9] H. S. Venkatesh, W. Morishita, A. C. Geraghty, D. Silverbush, S. M. Gillespie, M. Arzt, L. T. Tam, C. Espenel, A. Ponnuswami, L. J. Ni, P. J. Woo, K. R. Taylor, A. Agarwal, A. Regev, D. Brang, H. Vogel, S. Hervey-Jumper, D. E. Bergles, M. L. Suva, R. C. Malenka, M. Monje. Electrical and synaptic integration of glioma into neural circuits. Nature, 573, 539-545(2019).

[10] H. S. Venkatesh, T. B. Johung, V. Caretti, A. Noll, Y. J. Tang, S. Nagaraja, E. M. Gibson, C. W. Mount, J. Polepalli, S. S. Mitra, P. J. Woo, R. C. Malenka, H. Vogel, M. Bredel, P. Mallick, M. Monje. Neuronal activity promotes glioma growth through neuroligin-3 secretion. Cell, 161, 803-816(2015).

[11] G. Sprugnoli, A. J. Golby, E. Santarnecchi. Newly discovered neuron-to-glioma communication: New noninvasive therapeutic opportunities on the horizon?. Neurooncol. Adv., 3, vdab018(2021).

[12] H. S. Venkatesh, L. T. Tam, P. J. Woo, J. Lennon, S. Nagaraja, S. M. Gillespie, J. Ni, D. Y. Duveau, P. J. Morris, J. J. Zhao, C. J. Thomas, M. Monje. Targeting neuronal activity-regulated neuroligin-3 dependency in high-grade glioma. Nature, 549, 533-547(2017).

[13] S. C. Buckingham, S. L. Campbell, B. R. Haas, V. Montana, S. Robel, T. Ogunrinu, H. Sontheimer. Glutamate release by primary brain tumors induces epileptic activity. Nat. Med., 17, 1269-1299(2011).

[14] S. L. Campbell, S. C. Buckingham, H. Sontheimer. Human glioma cells induce hyperexcitability in cortical networks. Epilepsia, 53, 1360-1370(2012).

[15] C. C. J. Lin, K. Yu, A. Hatcher, T. W. Huang, H. K. Lee, J. Carlson, M. C. Weston, F. J. Chen, Y. Q. Zhang, W. Y. Zhu, C. A. Mohila, N. Ahnied, A. J. Patel, B. R. Arenkiel, J. L. Noebels, C. J. Creighton, B. Deneen. Identification of diverse astrocyte populations and their malignant analogs. Nat. Neurosci., 20, 396-405(2017).

[16] S. L. Campbell, S. Robel, V. A. Cuddapah, S. Robert, S. C. Buckingham, K. T. Kahle, H. Sontheimer. GABAergic disinhibition and impaired KCC2 cotransporter activity underlie tumor-associated epilepsy. Glia, 63, 23-36(2015).

[17] T. Takano, J. H. C. Lin, G. Arcuino, Q. Gao, J. Yang, M. Nedergaard. Glutamate release promotes growth of malignant gliomas. Nat. Med., 7, 1010-1015(2001).

[18] Y. J. Lin, C. Y. J. Wu, J. Y. Wu, M. Lim. The role of myeloid cells in GBM immunosuppression. Front Immunol., 13, 887781(2022).

[19] C. D. Russo, N. Cappoli. Glioma associated microglia/macrophages, a potential pharmacological target to promote antitumor inflammatory immune response in the treatment of glioblastoma. Neuroimmunolo. Neuroinflamm., 5, 36(2018).

[20] C. Y. J. Wu, C. H. Chen, C. Y. Lin, L. Y. Feng, Y. C. Lin, K. C. Wei, C. Y. Huang, J. Y. Fang, P. Y. Chen. CCL5 of glioma-associated microglia/macrophages regulates glioma migration and invasion via calcium-dependent matrix metalloproteinase 2. Neuro Oncol., 22, 253-266(2020).

[21] S. F. Hussain, D. Yang, D. Suki, K. Aldape, E. Grimm, A. B. Heimberger. The role of human glioma-infiltrating microglia/macrophages in mediating antitumor immune responses. Neuro Oncol., 8, 261-279(2006).

[22] X. Z. Ye, S. L. Xu, Y. H. Xin, S. C. Yu, Y. F. Ping, L. Chen, H. L. Xiao, B. Wang, L. Yi, Q. L. Wang, X. F. Jiang, L. Yang, P. Zhang, C. Qian, Y. H. Cui, X. Zhang, X. W. Bian. Tumor-associated microglia/macrophages enhance the invasion of glioma stem-like cells via TGF-beta1 signaling pathway. J. Immunol., 189, 444-453(2012).

[23] S. Qi, H. Li, L. Lu, Z. Qi, L. Liu, L. Chen, G. Shen, L. Fu, Q. Luo, Z. Zhang. Long-term intravital imaging of the multicolor-coded tumor microenvironment during combination immunotherapy. Elife, 5, e14756(2016).

[24] V. Di Nunno, E. Franceschi, A. Tosoni, L. Gatto, S. Bartolini, A. A. Brandes. Tumor-associated microenvironment of adult gliomas: A review. Front. Oncol., 12, 891543(2022).

[25] S. Qi, L. Lu, F. Zhou, Y. Chen, M. Xu, L. Chen, X. Yu, W. R. Chen, Z. Zhang. Neutrophil infiltration and whole-cell vaccine elicited by N-dihydrogalactochitosan combined with NIR phototherapy to enhance antitumor immune response and T cell immune memory. Theranostics, 10, 1814-1832(2020).

[26] S. Han, C. Zhang, Q. Li, J. Dong, Y. Liu, Y. Huang, T. Jiang, A. Wu. Tumour-infiltrating CD4(+) and CD8(+) lymphocytes as predictors of clinical outcome in glioma. Br. J. Cancer, 110, 2560-2568(2014).

[27] V. Haage, M. Semtner, R. O. Vidal, D. P. Hernandez, W. W. Pong, Zh. Chen, D. Hambardzumyan, V. Magrini, A. Ly, J. Walker, E. Mardis, P. Mertins, S. Sauer, H. Kettenmann, D. H. Gutmann. Comprehensive gene expression meta-analysis identifies signature genes that distinguish microglia from peripheral monocytes/macrophages in health and glioma. Acta Neuropathol. Commun., 7, 20(2019).

[28] R. L. Bowman, F. Klemm, L. Akkari, S. M. Pyonteck, L. Sevenich, D. F. Quail, S. Dhara, K. Simpson, E. E. Gardner, C. A. Iacobuzio-Donahue, C. W. Brennan, V. Tabar, P. H. Gutin, J. A. Joyce. Macrophage ontogeny underlies differences in glioma-specific education in brain malignancies. Cell. Rep., 17, 2445-2459(2016).

[29] Z. Chen, J. L. Ross, D. Hambardzumyan. Intravital 2-photon imaging reveals distinct morphology and infiltrative properties of glioblastoma-associated macrophages. Proc. Natl. Acad. Sci. USA, 116, 14254-14259(2019).

[30] S. Hernandez, F. Rojas, C. Laberiano, R. Lazcano, I. Wistuba, E. R. Parra. Multiplex immunofluorescence tyramide signal amplification for immune cell profiling of paraffin-embedded tumor tissues. Front Mol. Biosci., 8, 667067(2021).

[31] E. R. Parra. Novel platforms of multiplexed immunofluorescence for study of paraffin tumor tissues. J. Cancer Treat., 2, 43-53(2018).

[32] F. S. Varn, K. C. Johnson, J. Martinek, J. T. Huse, M. P. Nasrallah, P. Wesseling, L. A. D. Cooper, T. M. Malta, T. E. Wade, T. S. Sabedot, D. Brat, P. V. Gould, A. Woehrer, K. Aldape, A. Ismail, S. K. Sivajothi, F. P. Barthel, H. Kim, E. Kocakavuk, N. Ahmed, K. White, I. Datta, H. E. Moon, S. Pollock, C. Goldfarb, G. H. Lee, L. Garofano, K. J. Anderson, D. Nehar-Belaid, J. S. Barnholtz-Sloan, S. Bakas, A. T. Byrne, F. D’Angelo, H. K. Gan, M. Khasraw, S. Migliozzi, D. R. Ormond, S. H. Paek, E. G. Van Meir, A. M. E. Walenkamp, C. Watts, T. Weiss, M. Weller, K. Palucka, L. F. Stead, L. M. Poisson, H. Noushmehr, A. Iavarone, R. G. W. Verhaak, G. Consortium. Glioma progression is shaped by genetic evolution and microenvironment interactions. Cell, 185, 2184-2199(2022).

[33] B. M. Verhoeven, S. Mei, T. K. Olsen, K. Gustafsson, A. Valind, A. Lindstrom, D. Gisselsson, S. S. Fard, C. Hagerling, P. V. Kharchenko, P. Kogner, J. I. Johnsen, N. Baryawno. The immune cell atlas of human neuroblastoma. Cell. Rep. Med., 3, 100657(2022).

[34] S. Long, Y. Zhao, Y. Xu, H. Li, H. Zhao, D. Chen, J. Zeng, H. Qiu, X. Li, Y. Gu. Immune response induced by hematoporphyrin derivatives mediated photodynamic therapy: Immunogenic cell death and elevated costimulatory molecules. J. Innov. Opt. Health Sci., 15, 2240002(2022).

[35] H. W. Ai, K. L. Hazelwood, M. W. Davidson, R. E. Campbell. Fluorescent protein FRET pairs for ratiometric imaging of dual biosensors. Nat. Met., 5, 401-403(2008).

[36] J. F. Araneda, W. E. Piers, B. Heyne, M. Parvez, R. McDonald. High Stokes shift anilido-pyridine boron difluoride dyes. Angew. Chem. Int. Ed. Engl., 50, 12214-12217(2011).

[37] E. Beurel, M. Toups, C. B. Nemeroff. The bidirectional relationship of depression and inflammation: Double trouble. Neuron, 107, 234-256(2020).

[38] T. Kitabayashi, Y. Dong, T. Furuta, H. Sabit, S. Jiapaer, J. K. Zhang, G. T. Zhang, Y. Hayashi, M. Kobayashi, T. Domoto, T. Minamoto, A. Hirao, M. Nakada. Identification of GSK3 beta inhibitor kenpaullone as a temozolomide enhancer against glioblastoma. Sci. Rep., 9, 10049(2019).

[39] G. T. Zhang, S. Tanaka, S. Jiapaer, H. Sabit, S. Tamai, M. Kinoshita, M. Nakada. RBPJ contributes to the malignancy of glioblastoma and induction of proneural-mesenchymal transition via IL-6-STAT3 pathway. Cancer Sci., 111, 4166-4176(2020).