Influence of pH on Extracellular Matrix Preservation During Lung Decellularization
Open accessAbstract
The creation of decellularized organs for use in regenerative medicine requires the preservation of the organ extracellular matrix (ECM) as a means to provide critical cues for differentiation and migration of cells that are seeded onto the organ scaffold. The purpose of this study was to assess the influence of varying pH levels on the preservation of key ECM components during the decellularization of rat lungs. Herein, we show that the pH of the 3-[(3-cholamidopropyl)dimethylammonio]-1-propanesulfonate (CHAPS)-based decellularization solution influences ECM retention, cell removal, and also the potential for host response upon implantation of acellular lung tissue. The preservation of ECM components, including elastin, fibronectin, and laminin, were better retained in the lower pH conditions that were tested (pH ranges tested: 8, 10, 12); glycosaminoglycans were preserved to a higher extent in the lower pH groups as well. The DNA content following decellularization of the rat lung was inversely correlated with the pH of the decellularization solution. Despite detectible levels of cyotoskeletal proteins and significant residual DNA, tissues decellularized at pH 8 demonstrated the greatest tissue architecture maintenance and the least induction of host response of all acellular conditions. These results highlight the effect of pH on the results obtained by organ decellularization and suggest that altering the pH of the solutions used for decellularization may influence the ability of cells to properly differentiate and home to appropriate locations within the scaffold, based on the preservation of key ECM components and implantation results.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
More aggressive protocols designed for decellularization at higher pH diminish fibronectin, laminin, elastin, and GAGs' content and integrity, which interferes with subsequent cell adhesion and proliferation.
“Notably, more aggressive protocols designed for decellularization in higher pH diminish fibronectin, laminin, elastin, and GAGs’ content and integrity, which in turn interfere with subsequent cell adhesion and proliferation [82].”
From Immunogenicity of decellularized extracellular matrix scaffolds: a bottleneck in tissue engineering and regenerative medicine (2023) · cites this paper as [82]
Higher pH shatters ECM and produces particles that elicit more severe immune reactions.
“Presumably, higher pH shatters ECM and produces particles that elicit more severe immune reactions [81, 82].”
From Immunogenicity of decellularized extracellular matrix scaffolds: a bottleneck in tissue engineering and regenerative medicine (2023) · cites this paper as [82]
Alkalines such as NaOH separate DNA strands at pH>11 and extract cell components, but decellularization at higher pH provokes a more robust immune response than in neutral conditions.
“Alkalines such as NaOH separate DNA strands at pH>11 and extract cell components, but decellularization at higher pH provokes a more robust immune response than in neutral conditions.”
From Immunogenicity of decellularized extracellular matrix scaffolds: a bottleneck in tissue engineering and regenerative medicine (2023) · cites this paper as [82]
CHAPS deplete elastin and GAGs content of ECM.
“Of note, they have been demonstrated to deplete the elastin and GAGs content of ECM [51, 75, 82].”
From Immunogenicity of decellularized extracellular matrix scaffolds: a bottleneck in tissue engineering and regenerative medicine (2023) · cites this paper as [82]
Cites
1 retracted
RETRACTED: Clinical transplantation of a tissue-engineered airway
Macchiarini, P., Jungebluth, P., Go, T., Asnaghi, M. A., Rees, L., Cogan, T. A., Dodson, A., Martorell, J., Bellini, S., Parnigotto, P. P., et al. (2008) · The Lancet · doi:10.1016/s0140-6736(08)61598-6 · Cited by 1,431 · see citing works
RetractedPerfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart
Ott, H. C., Matthiesen, T. S., Goh, S.-K., Black, L. D., Kren, S. M., Netoff, T. I., & Taylor, D. A. (2008) · Nature Medicine · doi:10.1038/nm1684 · Cited by 2,650 · see citing works
Decellularization of tissues and organs
Gilbert, T. W., Sellaro, T. L., & Badylak, S. F. (2006) · Biomaterials · doi:10.1016/j.biomaterials.2006.02.014 · Cited by 2,222 · see citing works
Tissue-Engineered Lungs for in Vivo Implantation
Petersen, T. H., Calle, E. A., Zhao, L., Lee, E. J., Gui, L., Raredon, M. S. B., Gavrilov, K., Yi, T., Zhuang, Z. W., Breuer, C. K., et al. (2010) · Science · doi:10.1126/science.1189345 · Cited by 1,177 · see citing works
Self-citationRegeneration and orthotopic transplantation of a bioartificial lung
Ott, H. C., Clippinger, B., Conrad, C., Schuetz, C., Pomerantseva, I., Ikonomou, L., Kotton, D., & Vacanti, J. P. (2010) · Nature Medicine · doi:10.1038/nm.2193 · Cited by 1,090 · see citing works
Badylak, S. F., Taylor, D., & Uygun, K. (2011) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-071910-124743 · Cited by 1,041 · see citing works
Kielty, C. M., Sherratt, M. J., & Shuttleworth, C. A. (2002) · Journal of Cell Science · doi:10.1242/jcs.115.14.2817 · Cited by 841 · see citing works
Regeneration and experimental orthotopic transplantation of a bioengineered kidney
Song, J. J., Guyette, J. P., Gilpin, S. E., Gonzalez, G., Vacanti, J. P., & Ott, H. C. (2013) · Nature Medicine · doi:10.1038/nm.3154 · Cited by 793 · see citing works
Acellular vascular tissues: natural biomaterials for tissue repair and tissue engineering
Schmidt, C. E., & Baier, J. M. (2000) · Biomaterials · doi:10.1016/s0142-9612(00)00148-4 · Cited by 762 · see citing works
LAMININ FUNCTIONS IN TISSUE MORPHOGENESIS
Miner, J. H., & Yurchenco, P. D. (2004) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.20.010403.094555 · Cited by 756 · see citing works
Xenogeneic extracellular matrix as a scaffold for tissue reconstruction
Badylak, S. F. (2004) · Transplant Immunology · doi:10.1016/j.trim.2003.12.016 · Cited by 747 · see citing works
The Basement Membrane Component of Biologic Scaffolds Derived from Extracellular Matrix
Brown, B. N., Lindberg, K., Reing, J. E., Stolz, D. B., & Badylak, S. F. (2006) · Tissue Engineering · doi:10.1089/ten.2006.12.519 · Cited by 436 · see citing works
Cortiella, J., Niles, J. A., Cantu, A., Brettler, A. C., Pham, A. N., Vargas, G., Winston, S., Wang, J. P., Walls, S., & Nichols, J. E. (2010) · Tissue Engineering Part A · doi:10.1089/ten.tea.2009.0730 · Cited by 381 · see citing works
Badylak, S. F. (2014) · Annals of Biomedical Engineering · doi:10.1007/s10439-013-0963-7 · Cited by 307 · see citing works
Decellularized matrices for tissue engineering
Hoshiba, T., Lu, H., Kawazoe, N., & Chen, G. (2010) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2010.534079 · Cited by 295 · see citing works
Cavalcante, F. S. Á., Ito, S., Brewer, K. K., Sakai, H., Alencar, A. M., de Almeida, M. P., Andrade, J. S., Majumdar, A., Ingenito, E. P., & Suki, B. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00619.2004 · Cited by 262 · see citing works
Development of Decellularized Human Umbilical Arteries as Small-Diameter Vascular Grafts
Gui, L., Muto, A., Chan, S. A., Breuer, C. K., & Niklason, L. E. (2009) · Tissue Engineering Part A · doi:10.1089/ten.tea.2008.0526 · Cited by 256 · see citing works
Self-citationMatrix Composition and Mechanics of Decellularized Lung Scaffolds
Petersen, T. H., Calle, E. A., Colehour, M. B., & Niklason, L. E. (2011) · Cells Tissues Organs · doi:10.1159/000324896 · Cited by 229 · see citing works
Self-citationExtracellular matrix biology in the lung
Dunsmore, S. E., & Rannels, D. E. (1996) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.1996.270.1.l3 · Cited by 214 · see citing works
Estimation of hydroxyproline by the AutoAnalyser
Grant, R. A. (1964) · Journal of Clinical Pathology · doi:10.1136/jcp.17.6.685 · Cited by 200 · see citing works
Mendoza‐Novelo, B., Ávila, E. E., Cauich‐Rodríguez, J. V., Jorge‐Herrero, E., Rojo, F. J., Guinea, G. V., & Mata‐Mata, J. L. (2010) · Acta Biomaterialia · doi:10.1016/j.actbio.2010.11.017 · Cited by 197 · see citing works
Wallis, J. M., Borg, Z. D., Daly, A. B., Deng, B., Ballif, B. A., Allen, G. B., Jaworski, D. M., & Weiss, D. J. (2011) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2011.0567 · Cited by 187 · see citing works
Enhanced In Vivo Function of Bioartificial Lungs in Rats
Song, J. J., Kim, S. S., Liu, Z., Madsen, J. C., Mathisen, D. J., Vacanti, J. P., & Ott, H. C. (2011) · The Annals of Thoracic Surgery · doi:10.1016/j.athoracsur.2011.05.018 · Cited by 182 · see citing works
Effects of collagenase and elastase on the mechanical properties of lung tissue strips
Yuan, H., Kononov, S., Cavalcante, F. S. Á., Lutchen, K. R., Ingenito, E. P., & Suki, B. (2000) · Journal of Applied Physiology · doi:10.1152/jappl.2000.89.1.3 · Cited by 161 · see citing works
Laminin isoforms and lung development: All isoforms are not equal
Nguyen, N. M., & Senior, R. M. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.03.032 · Cited by 127 · see citing works
Falke, G. F., Yoo, J. J., Kwon, T. G., Moreland, R. B., & Atala, A. (2003) · Tissue Engineering · doi:10.1089/107632703322495529 · Cited by 113 · see citing works
Isenburg, J. C., Simionescu, D. T., & Vyavahare, N. R. (2004) · Biomaterials · doi:10.1016/j.biomaterials.2004.04.034 · Cited by 111 · see citing works
Novel Utilization of Serum in Tissue Decellularization
Gui, L., Chan, S. A., Breuer, C. K., & Niklason, L. E. (2010) · Tissue Engineering Part C: Methods · doi:10.1089/ten.tec.2009.0120 · Cited by 109 · see citing works
Self-citationEstimation of hydroxyproline by the AutoAnalyzer.
Grant, R. A. (1965) · Journal of Clinical Pathology · doi:10.1136/jcp.18.5.686 · Cited by 72 · see citing works
The Alkaline Denaturation of Deoxyribose Nucleic Acid
Ehrlich, P., & Doty, P. M. (1958) · Journal of the American Chemical Society · doi:10.1021/ja01549a033 · Cited by 67 · see citing works
Utility and Control of Proteoglycans in Tissue Engineering
Ferdous, Z., & Grande-Allen, K. J. (2007) · Tissue Engineering · doi:10.1089/ten.2006.0056 · Cited by 43 · see citing works
Filová, E., Brynda, E., Riedel, T., Chlupáč, J., Vandrovcová, M., Švindrych, Z., Lisá, V., Houška, M., Pirk, J., & Bačáková, L. (2013) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.34733 · Cited by 38 · see citing works
Kligys, K. R., Wu, Y., Hamill, K. J., Lewandowski, K. T., Hopkinson, S. B., Budinger, G. R. S., & Jones, J. (2013) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2012-0509oc · Cited by 23 · see citing works
Kikuchi, W., Arai, H., Ishida, A., Takahashi, Y., & Takada, G. (2003) · Experimental Lung Research · doi:10.1080/01902140303774 · Cited by 7 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Advancing biomaterials of human origin for tissue engineering
Chen, F.-M., & Liu, X. (2016) · Progress in Polymer Science · doi:10.1016/j.progpolymsci.2015.02.004 · Cited by 1,158 · see citing works
Methods of tissue decellularization used for preparation of biologic scaffolds and in vivo relevance
Keane, T. J., Swinehart, I. T., & Badylak, S. F. (2015) · Methods · doi:10.1016/j.ymeth.2015.03.005 · Cited by 670 · see citing works
Kasravi, M., Ahmadi, A., Babajani, A., Mazloomnejad, R., Hatamnejad, M. R., Shariatzadeh, S., Bahrami, S., & Niknejad, H. (2023) · Biomaterials Research · doi:10.1186/s40824-023-00348-z · Cited by 316 · see citing works
Extracellular matrix-derived biomaterials in engineering cell function
Xing, H., Lee, H., Luo, L., & Kyriakides, T. R. (2020) · Biotechnology Advances · doi:10.1016/j.biotechadv.2019.107421 · Cited by 302 · see citing works
Extracellular matrix in lung development, homeostasis and disease
Zhou, Y., Horowitz, J. C., Naba, A., Ambalavanan, N., Atabai, K., Balestrini, J. L., Bitterman, P. B., CORLEY, R. A., Ding, B., Engler, A. J., et al. (2018) · Matrix Biology · doi:10.1016/j.matbio.2018.03.005 · Cited by 285 · see citing works
Self-citationNeishabouri, A., Soltani Khaboushan, A., Daghigh, F., Kajbafzadeh, A.-M., & Majidi Zolbin, M. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.805299 · Cited by 281 · see citing works
Biomimetic scaffolds for regeneration of volumetric muscle loss in skeletal muscle injuries
Grasman, J. M., Zayas, M. J., Page, R. L., & Pins, G. D. (2015) · Acta Biomaterialia · doi:10.1016/j.actbio.2015.07.038 · Cited by 245 · see citing works
Decellularization for the retention of tissue niches
Moffat, D., Ye, K., & Jin, S. (2022) · Journal of Tissue Engineering · doi:10.1177/20417314221101151 · Cited by 152 · see citing works
Decellularization systems and devices: State-of-the-art
Choudhury, D., Yee, M., Sheng, Z. L. J., Amirul, A., & Naing, M. W. (2020) · Acta Biomaterialia · doi:10.1016/j.actbio.2020.07.060 · Cited by 137 · see citing works
Naba, A., Clauser, K. R., & Hynes, R. O. (2015) · Journal of Visualized Experiments · doi:10.3791/53057 · Cited by 135 · see citing works
Calle, E. A., Hill, R. C., Leiby, K. L., Le, A. V., Gard, A. L., Madri, J. A., Hansen, K. C., & Niklason, L. E. (2016) · Acta Biomaterialia · doi:10.1016/j.actbio.2016.09.043 · Cited by 113 · see citing works
Self-citationNovoseletskaya, E., Grigorieva, O., Nimiritsky, P., Basalova, N., Eremichev, R., Milovskaya, I., Kulebyakin, K., Kulebyakina, M., Rodionov, S., Omelyanenko, N., et al. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.555378 · Cited by 106 · see citing works
Functional vascularized lung grafts for lung bioengineering
Dorrello, N. V., Guenthart, B. A., O’Neill, J. D., Kim, J.-H., Cunningham, K. M., Chen, Y., Biscotti, M., Swayne, T. C., Wobma, H., Huang, S. X. L., et al. (2017) · Science Advances · doi:10.1126/sciadv.1700521 · Cited by 96 · see citing works
Extracellular Matrix as a Driver for Lung Regeneration
Balestrini, J. L., & Niklason, L. E. (2014) · Annals of Biomedical Engineering · doi:10.1007/s10439-014-1167-5 · Cited by 86 · see citing works
Self-citationBalestrini, J. L., Gard, A. L., Gerhold, K. A., Wilcox, E. C., Liu, A., Schwan, J., Le, A. V., Baevova, P., Dimitrievska, S., Zhao, L., et al. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.06.025 · Cited by 86 · see citing works
Self-citationZvarova, B., Uhl, F. E., Uriarte, J. J., Borg, Z. D., Coffey, A. L., Bonenfant, N. R., Weiss, D. J., & Wagner, D. E. (2016) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2015.0439 · Cited by 87 · see citing works
The impact of decellularization agents on renal tissue extracellular matrix
Poornejad, N., Schaumann, L. B., Buckmiller, E. M., Momtahan, N., Gassman, J. R., Ma, H. H., Roeder, B. L., Reynolds, P. R., & Cook, A. D. (2016) · Journal of Biomaterials Applications · doi:10.1177/0885328216656099 · Cited by 78 · see citing works
Production of decellularized porcine lung scaffolds for use in tissue engineering
Balestrini, J. L., Gard, A. L., Liu, A., Leiby, K. L., Schwan, J., Kunkemoeller, B. H., Calle, E. A., Sivarapatna, A., Lin, T., Dimitrievska, S., et al. (2015) · Integrative Biology · doi:10.1039/c5ib00063g · Cited by 74 · see citing works
Self-citationRapid release of growth factors regenerates force output in volumetric muscle loss injuries
Grasman, J. M., Duc, M., Page, R. L., & Pins, G. D. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2015.08.047 · Cited by 73 · see citing works
Doi, R., Tsuchiya, T., Mitsutake, N., Nishimura, S., Matsuu‐Matsuyama, M., Nakazawa, Y., Ogi, T., Akita, S., Yukawa, H., Baba, Y., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-09115-2 · Cited by 70 · see citing works
Self-citationChio, J. C. T., Punjani, N., Hejrati, N., Zavvarian, M.-M., Hong, J., & Fehlings, M. G. (2021) · Antioxidants and Redox Signaling · doi:10.1089/ars.2021.0120 · Cited by 67 · see citing works
How to build a lung: latest advances and emerging themes in lung bioengineering
Santis, M. M. D., Bölükbas, D. A., Lindstedt, S., & Wagner, D. E. (2018) · European Respiratory Journal · doi:10.1183/13993003.01355-2016 · Cited by 61 · see citing works
Sterilization of Lung Matrices by Supercritical Carbon Dioxide
Balestrini, J. L., Liu, A., Gard, A. L., Huie, J. L., Blatt, K. M. S., Schwan, J., Zhao, L., Broekelmann, T. J., Mecham, R. P., Wilcox, E. C., et al. (2015) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2015.0449 · Cited by 61 · see citing works
Self-citationRevascularization of decellularized lung scaffolds: principles and progress
Stabler, C. T., Lecht, S., Mondrinos, M. J., Goulart, E., Lazarovici, P., & Lelkes, P. I. (2015) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00237.2015 · Cited by 59 · see citing works
Human-scale lung regeneration based on decellularized matrix scaffolds as a biologic platform
Ohata, K., & Ott, H. C. (2020) · Surgery Today · doi:10.1007/s00595-020-02000-y · Cited by 57 · see citing works
Lung Microvascular Niche, Repair, and Engineering
Tsuchiya, T., Doi, R., Obata, T., Hatachi, G., & Nagayasu, T. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.00105 · Cited by 49 · see citing works
Self-citationBruyneel, A. A. N., & Carr, C. A. (2016) · Artificial Organs · doi:10.1111/aor.12838 · Cited by 47 · see citing works
Mazloomnejad, R., Babajani, A., Kasravi, M., Ahmadi, A., Shariatzadeh, S., Bahrami, S., & Niknejad, H. (2023) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2023.1103727 · Cited by 46 · see citing works
Development of novel apoptosis-assisted lung tissue decellularization methods
Song, Y. H., Maynes, M. A., Hlavac, N., Visosevic, D., Daramola, K. O., Porvasnik, S. L., & Schmidt, C. E. (2021) · Biomaterials Science · doi:10.1039/d1bm00032b · Cited by 33 · see citing works
Development potential of extracellular matrix hydrogels as hemostatic materials
Cai, D., & Weng, W. (2023) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2023.1187474 · Cited by 35 · see citing works
Comprehensive characterization of the human pancreatic proteome for bioengineering applications
Asthana, A., Tamburrini, R., Chaimov, D., Gazia, C., Walker, S. J., Van Dyke, M., Tomei, A., Lablanche, S., Robertson, J., Opara, E. C., et al. (2021) · Biomaterials · doi:10.1016/j.biomaterials.2020.120613 · Cited by 33 · see citing works
Sodium hydroxide based non-detergent decellularizing solution for rat lung
Sengyoku, H., Tsuchiya, T., Obata, T., Doi, R., Hashimoto, Y., Ishii, M., Sakai, H., Matsuo, N., Taniguchi, D., Suematsu, T., et al. (2018) · Organogenesis · doi:10.1080/15476278.2018.1462432 · Cited by 31 · see citing works
Self-citationYuan, Y., Engler, A. J., Raredon, M. S. B., Le, A. V., Baevova, P., Yöder, M. C., & Niklason, L. E. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2019.02.005 · Cited by 29 · see citing works
Self-citationDecellularization and Their Significance for Tissue Regeneration in the Era of 3D Bioprinting
Gadre, M. A., Kasturi, M., Agarwal, P., & Vasanthan, K. S. (2024) · ACS Omega · doi:10.1021/acsomega.3c08930 · Cited by 31 · see citing works
Hussein, K. H., Ahmadzada, B., Correa, J. C., Sultan, A., Wilken, S., Amiot, B., & Nyberg, S. L. (2024) · Bioactive Materials · doi:10.1016/j.bioactmat.2024.06.001 · Cited by 28 · see citing works
“These alkaline agents can separate DNA strands at pH levels higher than 11, extract cell components, and considered cytocompatible for the subsequent recellularization process [102,109].”
BackgroundUtilization of Natural Detergent Potassium Laurate for Decellularization in Lung Bioengineering
Obata, T., Tsuchiya, T., Akita, S., Kawahara, T., Matsumoto, K., Miyazaki, T., Masumoto, H., Kobayashi, E., Niklason, L. E., & Nagayasu, T. (2019) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2019.0016 · Cited by 27 · see citing works
Self-citationDecellularized extracellular matrix as a drug delivery carrier
Kolliopoulos, V., & Mikos, A. G. (2025) · Journal of Controlled Release · doi:10.1016/j.jconrel.2025.113661 · Cited by 25 · see citing works
Decellularized Rat Lung Scaffolds Using Sodium Lauryl Ether Sulfate for Tissue Engineering
Ma, J., Ju, Z., Yu, J., Qiao, Y., Hou, C., Wang, C., & Hei, F. (2017) · ASAIO Journal · doi:10.1097/mat.0000000000000654 · Cited by 25 · see citing works
The future perspectives of natural materials for pulmonary drug delivery and lung tissue engineering
Kim, S. Y., Wong, A. H. M., Neel, E. A. A., Chrzanowski, W., & Chan, H. (2014) · Expert Opinion on Drug Delivery · doi:10.1517/17425247.2015.993314 · Cited by 22 · see citing works
Kidney bioengineering in regenerative medicine: An emerging therapy for kidney disease
Lin, Y.-Q., Wang, L., Pan, L., Wang, H., Zhu, G., Liu, W., Wang, J., Braddock, M., & Zheng, M. (2015) · Cytotherapy · doi:10.1016/j.jcyt.2015.10.004 · Cited by 21 · see citing works
Decellularization of various tissues and organs through chemical methods
Tabatabai, T. S., Salehi, M., Rezakhani, L., Arabpour, Z., Djalilian, A. R., & Alizadeh, M. (2024) · Tissue and Cell · doi:10.1016/j.tice.2024.102573 · Cited by 20 · see citing works
Bioengineered Lungs: A Challenge and An Opportunity
Farré, R., Otero, J., Almendros, I., & Navajas, D. (2017) · Archivos de Bronconeumología · doi:10.1016/j.arbr.2017.09.010 · Cited by 20 · see citing works
Shevchuk, O. I., Korcheva, V., Moskalenko, N. S., Kyryk, V. M., Kot, K., & Krasnienkov, D. S. (2025) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2025.1621641 · Cited by 18 · see citing works
Seshadri, D. R., & Ramamurthi, A. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00759 · Cited by 16 · see citing works
Hashimoto, Y., Tsuchiya, T., Doi, R., Matsumoto, K., Higami, Y., Kobayashi, E., & Nagayasu, T. (2019) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.2923 · Cited by 15 · see citing works
Self-citationDecellularization techniques: unveiling the blueprint for tracheal tissue engineering
Gomes, K. T., Prasad, P. R., Sandhu, J. S., Kumar, A., Kumar, N. A. N., Shridhar, N., Bisht, B., & Paul, M. K. (2025) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2025.1518905 · Cited by 15 · see citing works
Soltanmohammadi, F., Gharehbaba, A. M., & Javadzadeh, Y. (2025) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2025.118200 · Cited by 12 · see citing works
Ex vivo organ engineering using decellularized tissue scaffolds
Saleh, T., Caciolli, L., Giobbe, G. G., & Coppi, P. D. (2025) · Nature Reviews Bioengineering · doi:10.1038/s44222-025-00322-5 · Cited by 11 · see citing works
Use of High-Rate Ventilation Results in Enhanced Recellularization of Bioengineered Lung Scaffolds
Ahmadipour, M., Taniguchi, D., Duchesneau, P., Aoki, F. G., Phillips, G., Sinderby, C. A., Waddell, T. K., & Karoubi, G. (2021) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2021.0182 · Cited by 11 · see citing works
Zhao, J., Chao, T., Zhou, M., Yue, K., Xu, F., Wang, H., Guo, J., & Gao, Z. (2024) · Regenerative medicine reports . · doi:10.4103/regenmed.regenmed-d-24-00016 · Cited by 11 · see citing works
Tavares, D. F., Mano, J. F., & Oliveira, M. B. (2025) · Materials Today Bio · doi:10.1016/j.mtbio.2025.101735 · Cited by 11 · see citing works
Development of Brain-Derived Bioscaffolds for Neural Progenitor Cell Culture
Terek, J. C., Hebb, M. O., & Flynn, L. E. (2023) · ACS Pharmacology & Translational Science · doi:10.1021/acsptsci.2c00232 · Cited by 9 · see citing works
Comprehensive Matrisome Profiling of Human Adipose Tissue for Soft Tissue Reconstruction
Major, G. S., Simcock, J., Kumar, A., Kleffmann, T., Woodfield, T. B. F., & Lim, K. S. (2023) · Advanced Biology · doi:10.1002/adbi.202300448 · Cited by 9 · see citing works
Current status and future prospects of decellularized kidney tissue
Nishimura, Y. (2022) · Journal of Artificial Organs · doi:10.1007/s10047-022-01366-9 · Cited by 9 · see citing works
Development of 2-D and 3-D culture platforms derived from decellularized nucleus pulposus
Quijano, M. A. H., Sharma, N., Martin, P. M., Séguin, C. A., & Flynn, L. E. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.937239 · Cited by 9 · see citing works
Generation of a Close-to-Native In Vitro System to Study Lung Cells–Extracellular Matrix Crosstalk
Garlíková, Z., Silva, A. C., Rabata, A., Potěšil, D., Ihnatová, I., Dumková, J., Koledova, Z. S., Zdráhal, Z., Vinarský, V., Hampl, A., et al. (2017) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2017.0283 · Cited by 9 · see citing works
New advances in liver decellularization and recellularization: innovative and critical technologies
Lin, Y.-Q., Wang, L., Wang, J., Pan, L., Zhu, G., Liu, W., Braddock, M., & Zheng, M. (2015) · Expert Review of Gastroenterology & Hepatology · doi:10.1586/17474124.2015.1058155 · Cited by 8 · see citing works
Dalgliesh, A. J., Liu, Z. Z., & Griffiths, L. G. (2017) · Tissue Engineering Part A · doi:10.1089/ten.tea.2016.0405 · Cited by 7 · see citing works
The Research of Acellular Pancreatic Bioscaffold as a Natural 3-Dimensional Platform In Vitro
Wang, X., Li, Y.-G., Du, Y. J., Zhu, J., & Zhao, L. (2018) · Pancreas · doi:10.1097/mpa.0000000000001123 · Cited by 7 · see citing works
Self-citationThe effect of decellularization processes on the immune response and compatibility of tissues
Nochalabadi, A., Khazaei, M., Zamani, S., & Rezakhani, L. (2025) · Tissue and Cell · doi:10.1016/j.tice.2025.103135 · Cited by 6 · see citing works
Hisanaga, M., Tsuchiya, T., Watanabe, H., Shimoyama, K., Iwatake, M., Tanoue, Y., Maruyama, K., Yukawa, H., Sato, K., Kato, Y., et al. (2023) · Organogenesis · doi:10.1080/15476278.2023.2212582 · Cited by 6 · see citing works
Self-citationHarmsen, M. C., Getova, V. E., Zhang, M., Zhao, F., van Dongen, J. A., Martinez-Garcia, F. D., Nizamoglu, M., & Burgess, J. K. (2023) · Springer eBooks · doi:10.1007/978-3-030-92090-6_43-1 · Cited by 5 · see citing works
Engineered Whole Lungs for Tissue BiologyPreprint
Greaney, A. M., Raredon, M. S. B., Obata, T., Wang, J., Adams, T. S., Schupp, J. C., Mizoguchi, S., Edelstein, S. E., Yuan, Y., Baevova, P., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.10.02.616240 · Cited by 5 · see citing works
Self-citationEvaluation methods for decellularized tissues: A focus on human amniotic membrane
García, M. G. S., Díaz, N. F., López, G. G., Álvarez-Maya, I., Jimenez, C. H., Maldonado, Y. R., Aguayo, D. J. M., & Diaz-Martinez, N. E. (2024) · Journal of Bioscience and Bioengineering · doi:10.1016/j.jbiosc.2024.10.009 · Cited by 4 · see citing works
Decellularizing Bone Tissue: Various Protocols
Emami, A., & Izadi, E. (2024) · Regenerative Engineering and Translational Medicine · doi:10.1007/s40883-024-00375-9 · Cited by 4 · see citing works
Mendoza‐Novelo, B., Castellano, L. E., Delgado, J., Quintero‐Ortega, I. A., Vargas‐Mancilla, J., & Vega‐González, A. (2015) · Materials Letters · doi:10.1016/j.matlet.2015.11.048 · Cited by 4 · see citing works
Can, S. S., Tuncer, S., Bilgiç, H. A., İmrak, G., Günal, G., Damadoğlu, E., Aydın, H. M., & Karaaslan, Ç. (2024) · Journal of Biomaterials Science Polymer Edition · doi:10.1080/09205063.2024.2392356 · Cited by 3 · see citing works
Scaffolds for tendon tissue engineering
Capella‐Monsonís, H., Guillaumin, S., Ribeiro, S., Korntner, S. H., Bayon, Y., & Zeugolis, D. I. (2019) · Elsevier eBooks · doi:10.1016/b978-0-08-102563-5.00013-7 · Cited by 3 · see citing works
Engineering Bioartificial Lungs for Transplantation
Wu, T., Economopoulos, K. P., & Ott, H. C. (2017) · Current Stem Cell Reports · doi:10.1007/s40778-017-0082-8 · Cited by 3 · see citing works
Detecting Collagen VI in Bethlem Myopathy
Sabatelli, P., Gualandi, F., Bonaldo, P., & Merlini, L. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.l115.639088 · Cited by 3 · see citing works
Decellularized Extracellular Matrix for Stem Cell Culture
Hoshiba, T. (2021) · Springer eBooks · doi:10.1007/978-981-16-4420-7_17 · Cited by 2 · see citing works
Wu, Z., Liu, Y., Tang, Z., Jiang, Z., Song, M., & Liang, Y. (2025) · Springer eBooks · doi:10.1007/978-3-031-81743-4_11 · Cited by 1 · see citing works
Enhancing peripheral nerve regeneration through NaOH ‐based decellularization of human nerve tissue
Kim, S., Park, S., Mun, J., Jung, S. W., Lee, W. J., Lee, D. W., & Lee, K. (2025) · Bioengineering & Translational Medicine · doi:10.1002/btm2.70072 · Cited by 1 · see citing works
Development of a 3D tumor model based on decellularized matrix using high-throughput approaches
Siahmansouri, H., Fenoglio, D., Filaci, G., & Mastrogiacomo, M. (2026) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2025.1690844 · Cited by 1 · see citing works
Acellular Lung Scaffolds in Lung Bioengineering
Wagner, D. E., Uhl, F. E., & Weiss, D. J. (2015) · Stem cell biology and regenerative medicine · doi:10.1007/978-3-319-21082-7_18 · Cited by 1 · see citing works
Raredon, M. S. B., Yuan, Y., & Niklason, L. E. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-818422-6.00070-8 · Cited by 1 · see citing works
Self-citationClinical Translation of Engineered Pulmonary Vascular Models
Yuan, Y. (2023) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-26625-6_14 · Cited by 1 · see citing works
Decellularized Matrix Hydrogels for In Vitro Disease Modeling
Ferreira, L. P., Monteiro, M. V., Gaspar, V. M., & Mano, J. F. (2021) · Royal Society of Chemistry eBooks · doi:10.1039/9781839161124-00626 · Cited by 1 · see citing works
Biomimetic Micropatterning of Electrospun Scaffolds for Tissue Engineering
Jeffries, E. M. (2015) · D-Scholarship@Pitt (University of Pittsburgh)
Regenerating the Respiratory Tract
Lim, M. L., Firsova, A. B., Feliu, N., Kuevda, E. V., Jungebluth, P., & Macchiarini, P. (2015) · Stem cell biology and regenerative medicine · doi:10.1007/978-3-319-21082-7_17
Zhao, L., Du, Y. J., & Wang, X. (2022) · Pancreas · doi:10.1097/mpa.0000000000002184
Self-citationHarmsen, M. C., Getova, V. E., Zhang, M., Zhao, F., van Dongen, J. A., Martinez-Garcia, F. D., Nizamoglu, M., & Burgess, J. K. (2024) · Springer eBooks · doi:10.1007/978-3-031-56363-8_43
Lokesh, B. V. S., Nair, R. S., Hashim, N. M., & Sim, M. S. (2025) · Journal of Biomaterials Science Polymer Edition · doi:10.1080/09205063.2025.2574939
A pilot study for decellularizing porcine cornea for future use in corneal regeneration
Josifovska, N., Niemi, E. M., Ramalingam, M., Manivasagam, G., Scholz, H., & Petrovski, G. (2025) · PLoS ONE · doi:10.1371/journal.pone.0339462
Niemi, E. M., Nyman, T. A., Attramadal, H., Hoel, H., Antonio, R., Hisdal, J., & Scholz, H. (2026) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2026.1773372
Scaffold degradation and tissue integration
Chinnappan, B. A., Santhini, E., Bal, T., Sharif, F., Smrithi, N. S., Misra, N., & Pillai, P. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-36767-0.00006-7
Lost cells, retained structure: proteomic mapping of decellularized lung matrisome across species
Čimborová, K., Pelková, V., Bernatík, O., Potěšil, D., Pustka, V., Vaškovicová, N., Kotasová, H., Mitáš, L., Vaňhara, P., Sedláková, V., et al. (2026) · Materials & Design · doi:10.1016/j.matdes.2026.116823
- Authors
- Tsuchiya, T., Balestrini, J. L., Mendez, J., Calle, E. A., Zhao, L., & Niklason, L. E.
- Affiliations
- Yale University (US)
- Corresponding author
- Niklason, Laura E.
- Venue
- Tissue Engineering Part C: Methods
- Publisher
- SAGE Publications
- Published
- 2014-12
- Volume
- 20
- Issue
- 12
- Pages
- 1028-1036
- ISSN
- 1937-3384 (ISSN-L)
- 1937-3392
- PMC
- PMC4241865
- OpenAlex
- W2084112522
- Cited by
- 89
- References
- 34
- Citations by year
- 2026: 4 · 2025: 11 · 2024: 10 · 2023: 8 · 2022: 5 · 2021: 5 · 2020: 6 · 2019: 5 · 2018: 5 · 2017: 7 · 2016: 6 · 2015: 15 · 2014: 2
- FWCI
- 9.92
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Tissue Engineering Part C Methods (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Institutional Repositories DataBase (IRDB) (submittedVersion, cc-by-nc-nd)
- Nagasaki University's Academic Output SITE (Nagasaki University) (submittedVersion, cc-by-nc-nd)
- Funders
- National Heart, Lung, and Blood Institute (R01HL098220, U01HL111016)
- National Institute of General Medical Sciences (T32GM086287)
- Topics
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Hydrogels: synthesis, properties, applications
- Keywords
- extracellular matrix preservation, pH, CHAPS, elastin, fibronectin, laminin, glycosaminoglycans, residual DNA, host response, tissue structure, rat lung, regenerative medicine
- MeSH terms
- Animals, Cholic Acids, Collagen, Elastin, Extracellular Matrix, Fibronectins, Glycosaminoglycans, Hydrogen-Ion Concentration, Laminin, Lung, Male, Rats, Sprague-Dawley, Implants, Experimental, Tissue Engineering, Subcutaneous Tissue
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review