Human Kidney Proximal Tubule-Microvascular Model Facilitates High-Throughput Analyses of Structural and Functional Effects of Ischemia-Reperfusion Injury.
TEER
fluid shear stress
high-throughput
ischemia-reperfusion
kidney-on-a-chip
oxygen
proximal tubule
Journal
Advanced biology
ISSN: 2701-0198
Titre abrégé: Adv Biol (Weinh)
Pays: Germany
ID NLM: 101775319
Informations de publication
Date de publication:
02 Oct 2023
02 Oct 2023
Historique:
revised:
27
08
2023
received:
28
03
2023
medline:
3
10
2023
pubmed:
3
10
2023
entrez:
3
10
2023
Statut:
aheadofprint
Résumé
Kidney ischemia reperfusion injury (IRI) poses a major global healthcare burden, but effective treatments remain elusive. IRI involves a complex interplay of tissue-level structural and functional changes caused by interruptions in blood and filtrate flow and reduced oxygenation. Existing in vitro models poorly replicate the in vivo injury environment and lack means of monitoring tissue function during the injury process. Here, a high-throughput human primary kidney proximal tubule (PT)-microvascular model is described, which facilitates in-depth structural and rapid functional characterization of IRI-induced changes in the tissue barrier. The PREDICT96 (P96) microfluidic platform's user-controlled fluid flow can mimic the conditions of IR to induce pronounced changes in cell structure that resemble clinical and in vivo phenotypes. High-throughput trans-epi/endo-thelial electrical resistance (TEER) sensing is applied to non-invasively track functional changes in the PT-microvascular barrier during the two-stage injury process and over repeated episodes of injury. Notably, ischemia causes an initial increase in tissue TEER followed by a sudden increase in permeability upon reperfusion, and this biphasic response occurs only with the loss of both fluid flow and oxygenation. This study demonstrates the potential of the P96 kidney IRI model to enhance understanding of IRI and fuel therapeutic development.
Identifiants
pubmed: 37786311
doi: 10.1002/adbi.202300127
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2300127Subventions
Organisme : National Science Foundation
ID : 1804845
Organisme : National Science Foundation
ID : 1842474
Organisme : The Charles Stark Draper Laboratory Inc.
Informations de copyright
© 2023 Wiley-VCH GmbH.
Références
A. Zuk, J. V. Bonventre, Curr. Opin. Nephrol. Hypertens. 2019, 28, 397.
J. V. Bonventre, L. Yang, J. Clin. Invest. 2011, 121, 4210.
R. L. Chevalier, Am. J. Physiol. Renal. Physiol. 2016, 311, F145.
E. A. J. Hoste, J. A. Kellum, N. M. Selby, A. Zarbock, P. M. Palevsky, S. M. Bagshaw, S. L. Goldstein, J. Cerdá, L. S. Chawla, Nat. Rev. Nephrol. 2018, 14, 607.
S. J. Han, H. T. Lee, Kidney Res. Clin. Pract. 2019, 38, 427.
B. A. Molitoris, M. C. Wagner, Kidney Int. 1996, 49, 1592.
J. Feng, W. Hu, C. Feng, X. Mao, K. Jin, Y. Ye, Aging Dis. 2015, 6, 228.
B. A. Molitoris, S. A. Falk, R. H. Dahl, J. Clin. Invest. 1989, 84, 1334.
E. Verghese, S. D. Ricardo, R. Weidenfeld, J. Zhuang, P. A. Hill, R. G. Langham, J. A. Deane, J. Am. Soc. Nephrol. 2009, 20, 2147.
P. Devarajan, JASN 2006, 17, 1503.
T. A. Sutton, H. E. Mang, S. B. Campos, R. M. Sandoval, M. C. Yoder, B. A. Molitoris, Am. J. Physiol.-Renal Physiol. 2003, 285, F191.
N. Shiva, N. Sharma, Y. A. Kulkarni, S. R. Mulay, A. B. Gaikwad, Life Sci. 2020, 256, 117860.
D. J. Parekh, J. M. Weinberg, B. Ercole, K. C. Torkko, W. Hilton, M. Bennett, P. Devarajan, M. A. Venkatachalam, J. Am. Soc. Nephrol. 2013, 24, 506.
M. Essig, F. Terzi, M. Burtin, G. Friedlander, Am. J. Physiol.-Renal Physiol. 2001, 281, F751.
K.-J. Jang, A. P. Mehr, G. A. Hamilton, L. A. Mcpartlin, S. Chung, K.-Y. Suh, D. E. Ingber, Integr. Biol. 2013, 5, 1119.
T. T. G. Nieskens, M. Persson, E. J. Kelly, A.-K. Sjögren, Drug Metab. Dispos. 2020, 48, 1303.
C. M. Sakolish, B. Philip, G. J. Mahler, Biomicrofluidics 2019, 13, 014107.
J. R. Soucy, A. J. Bindas, A. N. Koppes, R. A. Koppes, iScience 2019, 21, 521.
B. Srinivasan, A. R. Kolli, M. B. Esch, H. E. Abaci, M. L. Shuler, J. J. Hickman, J. Lab. Autom. 2015, 20, 107.
K. Felix, S. Tobias, H. Jan, S. Nicolas, M. Michael, Histochem. Cell Biol. 2021, 156, 609.
L. S. Rodgers, A. S. Fanning, Cytoskeleton 2011, 68, 653.
B. C. Elias, S. Mathew, M. B. Srichai, R. Palamuttam, N. Bulus, G. Mernaugh, A. B. Singh, C. R. Sanders, R. C. Harris, A. Pozzi, R. Zent, J. Biol. Chem. 2014, 289, 8532.
P. F. Secker, N. Schlichenmaier, M. Beilmann, U. Deschl, D. R. Dietrich, Arch. Toxicol. 2019, 93, 1965.
L. Yin, G. Du, B. Zhang, H. Zhang, R. Yin, W. Zhang, S.-M. Yang, Sci. Rep. 2020, 10, 1.
A. R. Chethikkattuveli Salih, A. Asif, A. Samantasinghar, H. M. Umer Farooqi, S. Kim, K. H. Choi, ACS Biomater. Sci. Eng. 2022, 8, 3733.
H. Azizgolshani, J. R. Coppeta, E. M. Vedula, E. E. Marr, B. P. Cain, R. J. Luu, M. P. Lech, S. H. Kann, T. J. Mulhern, V. Tandon, K. Tan, N. J. Haroutunian, P. Keegan, M. Rogers, A. L. Gard, K. B. Baldwin, J. C. De Souza, B. C. Hoefler, S. S. Bale, L. B. Kratchman, A. Zorn, A. Patterson, E. S. Kim, T. A. Petrie, E. L. Wiellette, C. Williams, B. C. Isenberg, J. L. Charest, Lab Chip 2021, 21, 1454.
J. Vriend, T. T. G. Nieskens, M. K. Vormann, B. T. Van Den Berge, A. Van Den Heuvel, F. G. M. Russel, L. Suter-Dick, H. L. Lanz, P. Vulto, R. Masereeuw, M. J. Wilmer, AAPS J. 2018, 20, 87.
M. K. Vormann, J. Vriend, H. L. Lanz, L. Gijzen, A. Van Den Heuvel, S. Hutter, J. Joore, S. J. Trietsch, C. Stuut, T. T. G. Nieskens, J. G. P. Peters, D. Ramp, M. Caj, F. G. M. Russel, B. Jacobsen, A. Roth, S. Lu, J. W. Polli, A. A. Naidoo, P. Vulto, R. Masereeuw, M. J. Wilmer, L. Suter-Dick, J. Pharm. Sci. 2021, 110, 1601.
E. M. Shaughnessey, S. H. Kann, H. Azizgolshani, L. D. Black, J. L. Charest, E. M. Vedula, Sci. Rep. 2022, 12, 13182.
J. Vriend, M. K. Vormann, H. L. Lanz, J. Joore, S. J. Trietsch, F. G. M. Russel, B. Jacobsen, A. Roth, S. Lu, J. W. Polli, A. A. Naidoo, R. Masereeuw, M. J. Wilmer, L. Suter-Dick, Curr. Opin. Toxicol. 2021, 25, 42.
M. K. Vormann, L. M. Tool, M. Ohbuchi, L. Gijzen, R. van Vught, T. Hankemeier, F. Kiyonaga, T. Kawabe, T. Goto, A. Fujimori, P. Vulto, H. L. Lanz, K. Tetsuka, Kidney360 2022, 3, 217.
S. H. Kann, E. M. Shaughnessey, X. Zhang, J. L. Charest, E. M. Vedula, Analyst 2023, 148, 3204.
S. H. Kann, E. M. Shaughnessey, J. R. Coppeta, H. Azizgolshani, B. C. Isenberg, E. M. Vedula, X. Zhang, J. L. Charest, Microsyst. Nanoeng. 2022, 8, 109.
A. Eirin, S. C. Textor, L. O. Lerman, Hypertension 2018, 72, 1023.
J. N. Hansen, S. Rassmann, B. Stüven, N. Jurisch-Yaksi, D. Wachten, Eur. Phys. J. E 2021, 44, 18.
J. Pavlacky, J. Polak, Front Endocrinol. 2020, 11, 57.
J. Muñoz-Sánchez, M. E. Chánez-Cárdenas, J. Appl. Toxicol. 2019, 39, 556.
B. El Awad, B. Kreft, E.-M. Wolber, T. Hellwig-Bürgel, E. Metzen, J. Fandrey, W. Jelkmann, Kidney Int. 2000, 58, 43.
B. A. Molitoris, Am. J. Physiol.-Renal Physiol. 1993, 265, F693.
O. Kwon, G. Corrigan, B. D. Myers, R. Sibley, J. D. Scandling, D. Dafoe, E. Alfrey, W. J. Nelson, Kidney Int. 1999, 55, 963.
M. A. Venkatachalam, D. B. Bernard, J. F. Donohoe, N. G. Levinsky, Kidney Int. 1978, 14, 31.
T. Steen Olsen, H. E. Hansen, H. Steen Olsen, Virchows Archiv A 1985, 406, 91.
M. A. Venkatachalam, D. B. Jones, H. G. Rennke, D. Sandstrom, Y. Patel, Lab Invest. 1981, 45, 355.
M. Chang-Panesso, B. D. Humphreys, Nat. Rev. Nephrol. 2017, 13, 39.
E. Verghese, R. Weidenfeld, J. F. Bertram, S. D. Ricardo, J. A. Deane, Nephrol. Dial Transplant 2008, 23, 834.
O. Kwon, W. J. Nelson, R. Sibley, P. Huie, J. D. Scandling, D. Dafoe, E. Alfrey, B. D. Myers, J. Clin. Invest. 1998, 101, 2054.
T. Tsukamoto, S. K. Nigam, J. Biol. Chem. 1997, 16133, 272,.
M. Hörbelt, S.-Y. Lee, H. E. Mang, N. L. Knipe, Y. Sado, A. Kribben, T. A. Sutton, Am. J. Physiol.-Renal Physiol. 2007, 293, F688.
D. P. Basile, M. D. Anderson, T. A. Sutton, Compr. Physiol. 2012, 2, 1303.
J. F. Donohoe, M. A. Venkatachalam, D. B. Bernard, N. G. Levinsky, Kidney Int. 1978, 13, 208.
P. P. Kapitsinou, V. H. Haase, Am. J. Physiol.-Renal Physiol. 2015, 309, F821.
M. A. Turman, C. M. Bates, Renal Failure 1997, 19, 47.
E. Vandenbroucke, D. Mehta, R. Minshall, A. B. Malik, Ann. N. Y. Acad. Sci. 2008, 1123, 134.
G. Zhang, Y. Yu, M. Guo, B. Lin, L. Zhang, Sens. Actuators, B 2019, 288, 564.
M. Busche, D. Rabl, J. Fischer, C. Schmees, T. Mayr, R. Gebhardt, M. Stelzle, EXCLI J. 2022, 21, 144.
X. Wang, J. Bonventre, A. Parrish, Int. J. Mol. Sci. 2014, 15, 15358.
A. E. Carpenter, T. R. Jones, M. R. Lamprecht, C. Clarke, I. Kang, O. Friman, D. A. Guertin, J. Chang, R. A. Lindquist, J. Moffat, P. Golland, D. M. Sabatini, Genome Biol. 2006, 7, R100.
J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, A. Cardona, Nat. Methods 2012, 9, 676.
U. Schmidt, M. Weigert, C. Broaddus, G. Myers, in Medical Image Computing and Computer Assisted Intervention - MICCAI (Eds: A. F. Frangi, J. A. Schnabel, C. Davatzikos, C. Alberola-López, G. Fichtinger), vol. 11071, 2018, p. 265.
T. Wagner, M. Hiner, Xraynaud, thorstenwagner/ij-ridgedetection: Ridge Detection 1.4.0 2017.
W. McKinney, Proc. 9th Python in Science Conf. (Eds: S. van der Walt, J. Millman), vol. 445, 2010, p. 51.
M. L. Waskom, J. Open Source Softw. 2021, 6, 3021.