A Map of Human Type 1 Diabetes Progression by Imaging Mass Cytometry

Cell Metabolism

Volumn 29, Issue 3, 2019, Pages 755-768.e5

  Damond, Nicolas ^a   Engler, Stefanie ^a   Zanotelli, Vito R T ^a   Schapiro, Denis ^a   Wasserfall, Clive H ^b   Kusmartseva, Irina ^b   Nick, Harry S ^b   Thorel, Fabrizio ^c   Herrera, Pedro L ^c   Atkinson, Mark A ^b   Bodenmiller, Bernd ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

endocrine pancreas; highly multiplexed imaging; imaging mass cytometry; immune cells; in situ imaging; islet of Langerhans; pseudotime; T cell recruitment; type 1 diabetes; cell

Indexed keywords

CELL MARKER; EPITOPE; TRANSCRIPTION FACTOR NKX6.1; TRANSCRIPTION FACTOR PDX 1; BIOLOGICAL MARKER;

ARTICLE; CELL COUNT; CELL LOSS; CONTROLLED STUDY; DISEASE DURATION; DISEASE EXACERBATION; HELPER CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INSULIN DEPENDENT DIABETES MELLITUS; MASS CYTOMETRY; MOLECULAR IMAGING; MOLECULAR PATHOLOGY; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; SINGLE CELL ANALYSIS; SUPERVISED MACHINE LEARNING; IMAGE CYTOMETRY; METABOLISM; PANCREAS; PANCREAS ISLET; PATHOLOGY; PROCEDURES;

BIOMARKERS; DIABETES MELLITUS, TYPE 1; DISEASE PROGRESSION; HUMANS; IMAGE CYTOMETRY; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; PANCREAS;

EID: 85062081871     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2018.11.014     Document Type: Article

References (48)

1. Allo, B., Lou, X., Bouzekri, A., Ornatsky, O., Clickable and high-sensitivity metal-containing tags for mass cytometry. Bioconjug. Chem. 29 (2018), 2028–2038.
2. Angelo, M., Bendall, S.C., Finck, R., Hale, M.B., Hitzman, C., Borowsky, A.D., Levenson, R.M., Lowe, J.B., Liu, S.D., Zhao, S., et al. Multiplexed ion beam imaging of human breast tumors. Nat. Med. 20 (2014), 436–442.
3. Atkinson, M.A., Eisenbarth, G.S., Michels, A.W., Type 1 diabetes. Lancet 383 (2014), 69–82.
4. Bodenmiller, B., Multiplexed epitope-based tissue imaging for discovery and healthcare applications. Cell Syst. 2 (2016), 225–238.
5. Boldison, J., Wong, F.S., Immune and pancreatic β cell interactions in type 1 diabetes. Trends Endocrinol. Metab. 27 (2016), 856–867.
6. Bosco, D., Armanet, M., Morel, P., Niclauss, N., Sgroi, A., Muller, Y.D., Giovannoni, L., Parnaud, G., Berney, T., Unique arrangement of alpha- and beta-cells in human islets of Langerhans. Diabetes 59 (2010), 1202–1210.
7. Brereton, M.F., Vergari, E., Zhang, Q., Clark, A., Alpha-, delta- and PP-cells: are they the architectural cornerstones of islet structure and co-ordination?. J. Histochem. Cytochem. 63 (2015), 575–591.
8. Brissova, M., Fowler, M.J., Nicholson, W.E., Chu, A., Hirshberg, B., Harlan, D.M., Powers, A.C., Assessment of human pancreatic islet architecture and composition by laser scanning confocal microscopy. J. Histochem. Cytochem. 53 (2005), 1087–1097.
9. Cabrera, O., Berman, D.M., Kenyon, N.S., Ricordi, C., Berggren, P.-O., Caicedo, A., The unique cytoarchitecture of human pancreatic islets has implications for islet cell function. Proc. Natl. Acad. Sci. U S A 103 (2006), 2334–2339.
10. Campbell-Thompson, M., Wasserfall, C., Kaddis, J., Albanese-O'Neill, A., Staeva, T., Nierras, C., Moraski, J., Rowe, P., Gianani, R., Eisenbarth, G., et al. Network for pancreatic organ donors with diabetes (nPOD): developing a tissue biobank for type 1 diabetes. Diabetes Metab. Res. Rev. 28 (2012), 608–617.
11. Campbell-Thompson, M.L., Montgomery, E.L., Foss, R.M., Kolheffer, K.M., Phipps, G., Schneider, L., Atkinson, M.A., Collection protocol for human pancreas. J. Vis. Exp., 2012, e4039, 10.3791/4039.
12. Campbell-Thompson, M., Fu, A., Kaddis, J.S., Wasserfall, C., Schatz, D.A., Pugliese, A., Atkinson, M.A., Insulitis and β-cell mass in the natural history of type 1 diabetes. Diabetes 65 (2016), 719–731.
13. Cannoodt, R., Saelens, W., Sichien, D., Tavernier, S., Janssens, S., Guilliams, M., Lambrecht, B.N., de Preter, K., Saeys, Y., SCORPIUS improves trajectory inference and identifies novel modules in dendritic cell development. bioRxiv, 2016, 10.1101/079509.
14. Carpenter, A.E., Jones, T.R., Lamprecht, M.R., Clarke, C., Kang, I.H., Friman, O., Guertin, D.A., Chang, J.H., Lindquist, R.A., Moffat, J., et al. CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol., 7, 2006, R100.
15. Chen, K.H., Boettiger, A.N., Moffitt, J.R., Wang, S., Zhuang, X., RNA imaging. Spatially resolved, highly multiplexed RNA profiling in single cells. Science, 348, 2015, aaa6090.
16. Chen, C., Cohrs, C.M., Stertmann, J., Bozsak, R., Speier, S., Human beta cell mass and function in diabetes: Recent advances in knowledge and technologies to understand disease pathogenesis. Mol. Metab. 6 (2017), 943–957.
17. Chevrier, S., Crowell, H.L., Zanotelli, V.R.T., Engler, S., Robinson, M.D., Bodenmiller, B., Compensation of signal spillover in suspension and imaging mass cytometry. Cell Syst. 6 (2018), 612–620.e5.
18. Coppieters, K.T., Dotta, F., Amirian, N., Campbell, P.D., Kay, T.W.H., Atkinson, M.A., Roep, B.O., von Herrath, M.G., Demonstration of islet-autoreactive CD8 T cells in insulitic lesions from recent onset and long-term type 1 diabetes patients. J. Exp. Med. 209 (2012), 51–60.
19. Foulis, A.K., Stewart, J.A., The pancreas in recent-onset type 1 (insulin-dependent) diabetes mellitus: insulin content of islets, insulitis and associated changes in the exocrine acinar tissue. Diabetologia 26 (1984), 456–461.
20. Gepts, W., Pathologic anatomy of the pancreas in juvenile diabetes mellitus. Diabetes 14 (1965), 619–633.
21. Gerdes, M.J., Sevinsky, C.J., Sood, A., Adak, S., Bello, M.O., Bordwell, A., Can, A., Corwin, A., Dinn, S., Filkins, R.J., et al. Highly multiplexed single-cell analysis of formalin-fixed, paraffin-embedded cancer tissue. Proc. Natl. Acad. Sci. U S A 110 (2013), 11982–11987.
22. Gianani, R., Campbell-Thompson, M., Sarkar, S.A., Wasserfall, C., Pugliese, A., Solis, J.M., Kent, S.C., Hering, B.J., West, E., Steck, A., et al. Dimorphic histopathology of long-standing childhood-onset diabetes. Diabetologia 53 (2010), 690–698.
23. Giesen, C., Wang, H.A.O., Schapiro, D., Zivanovic, N., Jacobs, A., Hattendorf, B., Schüffler, P.J., Grolimund, D., Buhmann, J.M., Brandt, S., et al. Highly multiplexed imaging of tumor tissues with subcellular resolution by mass cytometry. Nat. Methods 11 (2014), 417–422.
24. Goltsev, Y., Samusik, N., Kennedy-Darling, J., Bhate, S., Hale, M., Vazquez, G., Black, S., Nolan, G.P., Deep profiling of mouse splenic architecture with CODEX multiplexed imaging. Cell 174 (2018), 968–981.e15.
25. Gut, G., Herrmann, M.D., Pelkmans, L., Multiplexed protein maps link subcellular organization to cellular states. Science, 361, 2018, eaar7042.
26. Kamentsky, L., Jones, T.R., Fraser, A., Bray, M.-A., Logan, D.J., Madden, K.L., Ljosa, V., Rueden, C., Eliceiri, K.W., Carpenter, A.E., Improved structure, function and compatibility for CellProfiler: modular high-throughput image analysis software. Bioinformatics 27 (2011), 1179–1180.
27. Ke, R., Mignardi, M., Pacureanu, A., Svedlund, J., Botling, J., Wählby, C., Nilsson, M., In situ sequencing for RNA analysis in preserved tissue and cells. Nat. Methods 10 (2013), 857–860.
28. Lee, J.H., Daugharthy, E.R., Scheiman, J., Kalhor, R., Yang, J.L., Ferrante, T.C., Terry, R., Jeanty, S.S.F., Li, C., Amamoto, R., et al. Highly multiplexed subcellular RNA sequencing in situ. Science 343 (2014), 1360–1363.
29. Lin, J.-R., Fallahi-Sichani, M., Sorger, P.K., Highly multiplexed imaging of single cells using a high-throughput cyclic immunofluorescence method. Nat. Commun., 6, 2015, 8390.
30. Malaisse-Lagae, F., Stefan, Y., Cox, J., Perrelet, A., Orci, L., Identification of a lobe in the adult human pancreas rich in pancreatic polypeptide. Diabetologia 17 (1979), 361–365.
31. Marchetti, P., Suleiman, M., Marselli, L., Organ donor pancreases for the study of human islet cell histology and pathophysiology: a precious and valuable resource. Diabetologia 61 (2018), 770–774.
32. Meier, J.J., Bhushan, A., Butler, A.E., Rizza, R.A., Butler, P.C., Sustained beta cell apoptosis in patients with long-standing type 1 diabetes: indirect evidence for islet regeneration?. Diabetologia 48 (2005), 2221–2228.
33. Pugliese, A., Insulitis in the pathogenesis of type 1 diabetes. Pediatr. Diabetes 17:Suppl 22 (2016), 31–36.
34. Qiu, X., Mao, Q., Tang, Y., Wang, L., Chawla, R., Pliner, H.A., Trapnell, C., Reversed graph embedding resolves complex single-cell trajectories. Nat. Methods 14 (2017), 979–982.
35. Rodriguez-Calvo, T., Suwandi, J.S., Amirian, N., Zapardiel-Gonzalo, J., Anquetil, F., Sabouri, S., von Herrath, M.G., Heterogeneity and lobularity of pancreatic pathology in type 1 diabetes during the prediabetic phase. J. Histochem. Cytochem. 63 (2015), 626–636.
36. Rodriguez-Calvo, T., Zapardiel-Gonzalo, J., Amirian, N., Castillo, E., Lajevardi, Y., Krogvold, L., Dahl-Jørgensen, K., von Herrath, M.G., Increase in pancreatic proinsulin and preservation of β-cell mass in autoantibody-positive donors prior to type 1 diabetes onset. Diabetes 66 (2017), 1334–1345.
37. Rui, J., Deng, S., Arazi, A., Perdigoto, A.L., Liu, Z., Herold, K.C., β cells that resist immunological attack develop during progression of autoimmune diabetes in NOD mice. Cell Metab. 25 (2017), 727–738.
38. Saelens, W., Cannoodt, R., Todorov, H., Saeys, Y., A comparison of single-cell trajectory inference methods. Towards more accurate and robust tools. bioRxiv, 2018, 10.1101/276907.
39. Schapiro, D., Jackson, H.W., Raghuraman, S., Fischer, J.R., Zanotelli, V.R.T., Schulz, D., Giesen, C., Catena, R., Varga, Z., Bodenmiller, B., histoCAT: analysis of cell phenotypes and interactions in multiplex image cytometry data. Nat. Methods 14 (2017), 873–876.
40. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9 (2012), 676–682.
41. Schubert, W., Bonnekoh, B., Pommer, A.J., Philipsen, L., Böckelmann, R., Malykh, Y., Gollnick, H., Friedenberger, M., Bode, M., Dress, A.W.M., Analyzing proteome topology and function by automated multidimensional fluorescence microscopy. Nat. Biotechnol. 24 (2006), 1270–1278.
42. Schulz, D., Zanotelli, V.R.T., Fischer, J.R., Schapiro, D., Engler, S., Lun, X.-K., Jackson, H.W., Bodenmiller, B., Simultaneous multiplexed imaging of mRNA and proteins with subcellular resolution in breast cancer tissue samples by mass cytometry. Cell Syst. 6 (2018), 25–36.e5.
43. Sommer, C., Straehle, C., Kothe, U., and Hamprecht, F.A. (2011). Ilastik. Interactive learning and segmentation toolkit. In 2011 8th IEEE International Symposium on Biomedical Imaging (IEEE), pp. 230–233.
44. van der Maaten, L., Hinton, G., Visualizing data using t-SNE. J. Mach. Learn. Res. 9 (2008), 2579–2605.
45. Wang, Y.J., Kaestner, K.H., Single-cell RNA-seq of the pancreatic islets—a promise not yet fulfilled?. Cell Metab, 29, 2019, 10.1016/j.cmet.2018.11.016 Published online December 20, 2019.
46. Wang, Y.J., Traum, D., Schug, J., Gao, L., Liu, C., HPAP Consortium. Atkinson, M.A., Powers, A.C., Feldman, M.D., Naji, A., et al. Multiplexed in situ imaging mass cytometry analysis of the human endocrine pancreas and immune system in type 1 diabetes. Cell Metab., 29, 2019, 10.1016/j.cmet.2019.01.003 Published online January 31, 2019.
47. Wasserfall, C., Nick, H.S., Campbell-Thompson, M., Beachy, D., Haataja, L., Kusmartseva, I., Posgai, A., Beery, M., Rhodes, C., Bonifacio, E., et al. Persistence of pancreatic insulin mRNA expression and proinsulin protein in type 1 diabetes pancreata. Cell Metab. 26 (2017), 568–575.e3.
48. Zrazhevskiy, P., Gao, X., Quantum dot imaging platform for single-cell molecular profiling. Nat. Commun., 4, 2013, 1619.