Meningeal leukaemic aggregates as foci of cell expansion and chemoresistance in acute lymphoblastic leukaemia metastasis

M.T. Williams, Y.M. Yousafzai, A. Elder, K. Rehe, S. Bomken, L. Frishman-Levy, S. Tavor, P. Sinclair, K. Dormon, D. Masic, T. Perry, V.J. Weston, P. Kearns, H. Blair, L.J. Russell, O. Heidenreich, J.A. Irving, S. Izraeli, J. Vormoor, G.J. Graham, C. Halsey, The ability to cross the blood-cerebrospinal fluid barrier is a generic property of acute lymphoblastic leukemia blasts. Blood. 127(16), 1998–2006 (2016). https://doi.org/10.1182/blood-2015-08-665034

Article  CAS  PubMed  Google Scholar 

R.A. Price, W.W. Johnson, The central nervous system in childhood leukemia. I. The arachnoid. Cancer. 31(3), 520–533 (1973). https://doi.org/10.1002/1097-0142(197303)31:3%3C520::aid-cncr2820310306%3E3.0.co;2-2

Y.T. Cheung, N.D. Sabin, W.E. Reddick, D. Bhojwani, W. Liu, T.M. Brinkman, J.O. Glass, S.N. Hwang, D. Srivastava, C.H. Pui, L.L. Robison, M.M. Hudson, K.R. Krull, Leukoencephalopathy and long-term neurobehavioural, neurocognitive, and brain imaging outcomes in survivors of childhood acute lymphoblastic leukaemia treated with chemotherapy: a longitudinal analysis. Lancet Haematol. 3(10), e456–e466 (2016). https://doi.org/10.1016/S2352-3026(16)30110-7

Article  PubMed  PubMed Central  Google Scholar 

N.S. Phillips, K.L. Stratton, A.M. Williams, T. Ahles, K.K. Ness, H.J. Cohen, K. Edelstein, Y. Yasui, K. Oeffinger, E.J. Chow, R.M. Howell, L.L. Robison, G.T. Armstrong, W.M. Leisenring, K.R. Krull, Late-onset cognitive impairment and modifiable risk factors in adult Childhood Cancer survivors. JAMA Netw. Open. 6(5), e2316077 (2023). https://doi.org/10.1001/jamanetworkopen.2023.16077

W.A. Mills, M.A. Coburn, U.B. Eyo, The emergence of the calvarial hematopoietic niche in health and disease. Immunol. Rev. 311(1), 26–38 (2022). https://doi.org/10.1111/imr.13120

Article  CAS  PubMed  PubMed Central  Google Scholar 

R. Pietila, F. Del Gaudio, L. He, E. Vazquez-Liebanas, M. Vanlandewijck, L. Muhl, G. Mocci, K.D. Bjornholm, C. Lindblad, A. Fletcher-Sandersjoo, M. Svensson, E.P. Thelin, J. Liu, A.J. van Voorden, M. Torres, S. Antila, L. Xin, H. Karlstrom, J. Storm-Mathisen, L.H. Bergersen, A. Moggio, E.M. Hansson, M.H. Ulvmar, P. Nilsson, T. Makinen, M. Andaloussi Mae, K. Alitalo, S.T. Proulx, B. Engelhardt, D.M. McDonald, U. Lendahl, J. Andrae, C. Betsholtz, Molecular anatomy of adult mouse leptomeninges. Neuron. 111(23), 3745–3764e3747 (2023). https://doi.org/10.1016/j.neuron.2023.09.002

Article  CAS  PubMed  Google Scholar 

K. Mollgard, F.R.M. Beinlich, P. Kusk, L.M. Miyakoshi, C. Delle, V. Pla, N.L. Hauglund, T. Esmail, M.K. Rasmussen, R.S. Gomolka, Y. Mori, M. Nedergaard, A mesothelium divides the subarachnoid space into functional compartments. Science. 379(6627), 84–88 (2023). https://doi.org/10.1126/science.adc8810

Article  CAS  PubMed  Google Scholar 

J.A. Mapunda, J. Pareja, M. Vladymyrov, E. Bouillet, P. Helie, P. Pleskac, S. Barcos, J. Andrae, D. Vestweber, D.M. McDonald, C. Betsholtz, U. Deutsch, S.T. Proulx, B. Engelhardt, VE-cadherin in arachnoid and pia mater cells serves as a suitable landmark for in vivo imaging of CNS immune surveillance and inflammation. Nat. Commun. 14(1), 5837 (2023). https://doi.org/10.1038/s41467-023-41580-4

Article  CAS  PubMed  PubMed Central  Google Scholar 

C. Niu, J. Yu, T. Zou, Y. Lu, L. Deng, H. Yun, C.Y. Si, X. Wu, H. Jiang, T. Guo, M. Wu, T. Kan, J. Feng, C. Yuan, X. Yang, Q. Cheng, J. Dong, Q. Wang, J. Zhang, Identification of hematopoietic stem cells residing in the meninges of adult mice at steady state. Cell. Rep. 41(6), 111592 (2022). https://doi.org/10.1016/j.celrep.2022.111592

Article  CAS  PubMed  Google Scholar 

S. Brioschi, W.L. Wang, V. Peng, M. Wang, I. Shchukina, Z.J. Greenberg, J.K. Bando, N. Jaeger, R.S. Czepielewski, A. Swain, D.A. Mogilenko, W.L. Beatty, P. Bayguinov, J.A.J. Fitzpatrick, L.G. Schuettpelz, C.C. Fronick, I. Smirnov, J. Kipnis, V.S. Shapiro, G.F. Wu, S. Gilfillan, M. Cella, M.N. Artyomov, S.H. Kleinstein, M. Colonna, Heterogeneity of meningeal B cells reveals a lymphopoietic niche at the CNS borders. Science. 373(6553) (2021). https://doi.org/10.1126/science.abf9277

V. Ramaglia, A. Florescu, M. Zuo, S. Sheikh-Mohamed, J.L. Gommerman, Stromal cell-mediated coordination of Immune Cell Recruitment, Retention, and function in brain-adjacent regions. J. Immunol. 206(2), 282–291 (2021). https://doi.org/10.4049/jimmunol.2000833

Article  CAS  PubMed  Google Scholar 

J. Cupovic, L. Onder, C. Gil-Cruz, E. Weiler, S. Caviezel-Firner, C. Perez-Shibayama, T. Rulicke, I. Bechmann, B. Ludewig, Central nervous system stromal cells control local CD8(+) T cell responses during Virus-Induced Neuroinflammation. Immunity. 44(3), 622–633 (2016). https://doi.org/10.1016/j.immuni.2015.12.022

Article  CAS  PubMed  PubMed Central  Google Scholar 

R. Watanabe, M. Kakizaki, Y. Ikehara, A. Togayachi, Formation of fibroblastic reticular network in the brain after infection with neurovirulent murine coronavirus. Neuropathology. 36(6), 513–526 (2016). https://doi.org/10.1111/neup.12302

Article  CAS  PubMed  PubMed Central  Google Scholar 

E.H. Wilson, T.H. Harris, P. Mrass, B. John, E.D. Tait, G.F. Wu, M. Pepper, E.J. Wherry, F. Dzierzinski, D. Roos, P.G. Haydon, T.M. Laufer, W. Weninger, C.A. Hunter, Behavior of parasite-specific effector CD8 + T cells in the brain and visualization of a kinesis-associated system of reticular fibers. Immunity. 30(2), 300–311 (2009). https://doi.org/10.1016/j.immuni.2008.12.013

Article  CAS  PubMed  PubMed Central  Google Scholar 

O.W. Howell, C.A. Reeves, R. Nicholas, D. Carassiti, B. Radotra, S.M. Gentleman, B. Serafini, F. Aloisi, F. Roncaroli, R. Magliozzi, R. Reynolds, Meningeal inflammation is widespread and linked to cortical pathology in multiple sclerosis. Brain. 134(9), 2755–2771 (2011). https://doi.org/10.1093/brain/awr182

Article  PubMed  Google Scholar 

R.J. Bevan, R. Evans, L. Griffiths, L.M. Watkins, M.I. Rees, R. Magliozzi, I. Allen, G. McDonnell, R. Kee, M. Naughton, D.C. Fitzgerald, R. Reynolds, J.W. Neal, O.W. Howell, Meningeal inflammation and cortical demyelination in acute multiple sclerosis. Ann. Neurol. 84(6), 829–842 (2018). https://doi.org/10.1002/ana.25365

Article  CAS  PubMed  Google Scholar 

L.B. Thomas, Pathology of leukemia in the brain and meninges: postmortem studies of patients with acute leukemia and of mice given inoculations of L1210 leukemia. Cancer Res. 25(9), 1555–1571 (1965)

CAS  PubMed  Google Scholar 

M. Lorger, B. Felding-Habermann, Capturing changes in the brain microenvironment during initial steps of breast cancer brain metastasis. Am. J. Pathol. 176(6), 2958–2971 (2010). https://doi.org/10.2353/ajpath.2010.090838

Article  PubMed  PubMed Central  Google Scholar 

A. Sanchez-Aguilera, S. Mendez-Ferrer, The hematopoietic stem-cell niche in health and leukemia. Cell. Mol. Life Sci. 74(4), 579–590 (2017). https://doi.org/10.1007/s00018-016-2306-y

Article  CAS  PubMed  Google Scholar 

E. Dander, C. Palmi, G. D’Amico, G. Cazzaniga, The bone Marrow Niche in B-Cell Acute Lymphoblastic Leukemia: the role of Microenvironment from Pre-leukemia to overt leukemia. Int. J. Mol. Sci. 22(9), 4426 (2021). https://doi.org/10.3390/ijms22094426

Article  CAS  PubMed  PubMed Central  Google Scholar 

S.M. Akers, S.L. Rellick, J.E. Fortney, L.F. Gibson, Cellular elements of the subarachnoid space promote ALL survival during chemotherapy. Leuk. Res. 35(6), 705–711 (2011). https://doi.org/10.1016/j.leukres.2010.12.031

Article  PubMed  PubMed Central  Google Scholar 

P. Basile, L.M. Jonart, M. Ebadi, K. Johnson, M. Kerfeld, P.M. Gordon, The meninges enhance leukaemia survival in cerebral spinal fluid. Br. J. Haematol. 189(3), 513–517 (2020). https://doi.org/10.1111/bjh.16270

Article  PubMed  PubMed Central  Google Scholar 

L.M. Jonart, M. Ebadi, P. Basile, K. Johnson, J. Makori, P.M. Gordon, Disrupting the leukemia niche in the central nervous system attenuates leukemia chemoresistance. Haematologica. 105(8), 2130–2140 (2020). https://doi.org/10.3324/haematol.2019.230334

Article  CAS  PubMed  PubMed Central  Google Scholar 

L.M. Jonart, J. Ostergaard, A. Brooks, G. Fitzpatrick, L. Chen, P.M. Gordon, CXCR4 antagonists disrupt leukaemia-meningeal cell adhesion and attenuate chemoresistance. Br. J. Haematol. 201(3), 459–469 (2023). https://doi.org/10.1111/bjh.18607

Article  CAS  PubMed  Google Scholar 

F.G.S.A. Gandarillas, N. Benito, C. Gamallo, M. Quintanilla, Induction of PA2.26, a cell-surface antigen expressed by active fibroblasts, in mouse epidermal keratinocytes during carcinogenesis. Mol. Carcinog. 20(1), 10–18 (1997). https://doi.org/10.1002/(sici)1098-2744(199709)20:1%3C10::aid-mc3%3E3.0.co;2-m

Article  CAS  PubMed  Google Scholar 

V. Pla, S. Bitsika, M.J. Giannetto, A. Ladron-de-Guevara, D. Gahn-Martinez, Y. Mori, M. Nedergaard, K. Mollgard, Structural characterization of SLYM-a 4th meningeal membrane. Fluids Barriers CNS. 20(1), 93 (2023). https://doi.org/10.1186/s12987-023-00500-w

Article  CAS  PubMed  PubMed Central  Google Scholar 

R.C. Sterner, R.M. Sterner, CAR-T cell therapy: current limitations and potential strategies. Blood Cancer J. 11(4), 69 (2021). https://doi.org/10.1038/s41408-021-00459-7

Article  PubMed 

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