Effect of source animal age upon macrophage response to extracellular matrix biomaterials
Open accessAbstract
Extracellular matrix biomaterials have been shown to promote constructive remodeling in many preclinical and clinical applications. This response has been associated with the promotion of a timely switch from pro-inflammatory (M1) to anti-inflammatory (M2) macrophages. A previous study has shown that this beneficial response is lost when these biomaterials are derived from aged animals. This study examined the impact of small intestine submucosa (SIS) derived from 12, 26 and 52 week old pigs on the phenotype and function of bone marrow macrophages derived either from 2 or 18 month old mice. Results showed that 52 week old SIS promoted less iNOS in 2 month macrophages and Fizz1 expression in 2 and 18 month compared to 12 week SIS. Pro-inflammatory cytokine exposure to 52 week SIS-treated macrophages resulted in higher iNOS in 18 month macrophages and reduced MHC-II expression in 2 month macrophages, as well as reduced nitric oxide production in comparison to 12 week SIS. These results indicate that ECM derived from aged animals promotes an altered macrophage phenotype compared to young controls. This suggests that sourcing of ECM from young donors is important to preserve constructive remodeling outcomes of ECM biomaterials. Alteration of macrophage phenotype by aged ECM also raises the hypothesis that alterations in aged ECM may play a role in immune dysfunction in aged individuals.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
SIS obtained from 52-week-old pigs elicited diminished iNOS production in 2-month macrophages and suppressed Fizz 1 expression in both 2 and 18-month macrophages compared to 12-week SIS, suggesting that ECM derived from aged animals results in a distinct macrophage phenotype compared to younger controls.
“According to the findings, SIS obtained from 52-week-old pigs elicited diminished iNOS production in 2-month macrophages and suppressed Fizz 1 expression in both 2 and 18-month macrophages in comparison to 12-week SIS. The study suggested that ECM derived from aged animals results in a distinct macrophage phenotype compared to younger controls, emphasizing the importance of sourcing ECM from young”
From Liver tissue engineering using decellularized scaffolds: Current progress, challenges, and opportunities (2024) · cites this paper as [82]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Chronic Inflammation (Inflammaging) and Its Potential Contribution to Age-Associated Diseases
Franceschi, C., & Campisi, J. (2014) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/glu057 · Cited by 3,891 · see citing works
Of Mice and Not Men: Differences between Mouse and Human Immunology
Mestas, J., & Hughes, C. C. W. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.5.2731 · Cited by 3,822 · see citing works
An overview of tissue and whole organ decellularization processes
Crapo, P. M., Gilbert, T. W., & Badylak, S. F. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.01.057 · Cited by 3,591 · see citing works
Mechanisms of phagocytosis in macrophages
Aderem, A., & Underhill, D. M. (1999) · Annual Review of Immunology · doi:10.1146/annurev.immunol.17.1.593 · Cited by 2,854 · see citing works
Franceschi, C., Capri, M., Monti, D., Giunta, S., Olivieri, F., Sevini, F., Panourgia, M. P., Invidia, L., Celani, L., Scurti, M., et al. (2007) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2006.11.016 · Cited by 2,087 · see citing works
The intersection between aging and cardiovascular disease
North, B. J., & Sinclair, D. A. (2012) · Circulation Research · doi:10.1161/circresaha.111.246876 · Cited by 1,585 · see citing works
Regulatory interactions between muscle and the immune system during muscle regeneration
Tidball, J. G., & Villalta, S. A. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00735.2009 · Cited by 1,105 · see citing works
Brown, B. N., Valentin, J. E., Stewart-Akers, A. M., McCabe, G. P., & Badylak, S. F. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2008.11.040 · Cited by 896 · see citing works
Self-citationImmunosenescence: emerging challenges for an ageing population
Aw, D., Silva, A. B., & Palmer, D. B. (2007) · Immunology · doi:10.1111/j.1365-2567.2007.02555.x · Cited by 880 · see citing works
Folkman, J., Klagsbrun, M., Sasse, J., Wadzinski, M., Ingber, D. E., & Vlodavsky, I. (1988) · PubMed Central · Cited by 875 · see citing works
Anti-inflammatory M2, but not pro-inflammatory M1 macrophages promote angiogenesis in vivo
Jetten, N., Verbruggen, S. E. L., Gijbels, M. J., Post, M. J., de Winther, M. P. J., & Donners, M. M. P. C. (2013) · Angiogenesis · doi:10.1007/s10456-013-9381-6 · Cited by 841 · see citing works
Brown, B. N., Londono, R., Tottey, S., Zhang, L., Kukla, K. A., Wolf, M. T., Daly, K. A., Reing, J. E., & Badylak, S. F. (2012) · Acta Biomaterialia · doi:10.1016/j.actbio.2011.11.031 · Cited by 745 · see citing works
Self-citationConsequences of ineffective decellularization of biologic scaffolds on the host response
Keane, T. J., Londono, R., Turner, N. J., & Badylak, S. F. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2011.10.054 · Cited by 613 · see citing works
CCR2 recruits an inflammatory macrophage subpopulation critical for angiogenesis in tissue repair
Willenborg, S., Lucas, T., van Loo, G., Knipper, J. A., Krieg, T., Haase, I., Brachvogel, B., Hammerschmidt, M., Nagy, A., Ferrara, N., et al. (2012) · Blood · doi:10.1182/blood-2012-01-403386 · Cited by 534 · see citing works
Extracellular matrix as an inductive scaffold for functional tissue reconstruction
Brown, B. N., & Badylak, S. F. (2013) · Translational research · doi:10.1016/j.trsl.2013.11.003 · Cited by 518 · see citing works
Self-citationSicari, B. M., Rubin, J. P., Dearth, C. L., Wolf, M. T., Ambrosio, F., Boninger, M. L., Turner, N. J., Weber, D. J., Simpson, T. W., Wyse, A. J., et al. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3008085 · Cited by 490 · see citing works
Bingisser, R. M., Tilbrook, P. A., Holt, P. G., & Kees, U. R. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.160.12.5729 · Cited by 480 · see citing works
Reing, J. E., Brown, B. N., Daly, K. A., Freund, J. M., Gilbert, T. W., Hsiong, S. X., Huber, A., Kullas, K. E., Tottey, S., Wolf, M. T., et al. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.07.083 · Cited by 475 · see citing works
Self-citationThe central role of muscle stem cells in regenerative failure with aging
Blau, H. M., Cosgrove, B. D., & Ho, A. T. V. (2015) · Nature Medicine · doi:10.1038/nm.3918 · Cited by 437 · 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
Self-citationAge-Related Alterations in the Inflammatory Response to Dermal Injury
Swift, M. E., Burns, A. L., Gray, K. L., & DiPietro, L. A. (2001) · Journal of Investigative Dermatology · doi:10.1046/j.0022-202x.2001.01539.x · Cited by 398 · see citing works
Degradation Products of Extracellular Matrix Affect Cell Migration and Proliferation
Reing, J. E., Zhang, L., Myers-Irvin, J., Cordero, K. E., Freytes, D. O., Heber-Katz, E., Bedelbaeva, K., McIntosh, D., Dewilde, A., Braunhut, S. J., et al. (2009) · Tissue Engineering Part A · doi:10.1089/ten.tea.2007.0425 · Cited by 387 · see citing works
Matrix-bound nanovesicles within ECM bioscaffolds
Huleihel, L., Hussey, G. S., Naranjo, J. D., Zhang, L., Dziki, J. L., Turner, N. J., Stolz, D. B., & Badylak, S. F. (2016) · Science Advances · doi:10.1126/sciadv.1600502 · Cited by 387 · see citing works
Macrophage Participation in the Degradation and Remodeling of Extracellular Matrix Scaffolds
Valentin, J. E., Stewart-Akers, A. M., Gilbert, T. W., & Badylak, S. F. (2009) · Tissue Engineering Part A · doi:10.1089/ten.tea.2008.0419 · Cited by 356 · see citing works
(1999) · PubMed · Cited by 354 · see citing works
Morphologic Study of Small Intestinal Submucosa as a Body Wall Repair Device
Badylak, S. F., Kokini, K., Tullius, B., Simmons-Byrd, A., & Morff, R. J. (2002) · Journal of Surgical Research · doi:10.1006/jsre.2001.6349 · Cited by 310 · see citing works
Ashcroft, G. S., Mills, S. J., & Ashworth, J. J. (2002) · Biogerontology · doi:10.1023/a:1021399228395 · Cited by 309 · see citing works
Miller, K. J., Thaloor, D., Matteson, S., & Pavlath, G. K. (2000) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2000.278.1.c174 · Cited by 274 · see citing works
The promotion of a constructive macrophage phenotype by solubilized extracellular matrix
Sicari, B. M., Dziki, J. L., Siu, B. F., Medberry, C. J., Dearth, C. L., & Badylak, S. F. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.06.060 · Cited by 255 · see citing works
Lateral transmission of force is impaired in skeletal muscles of dystrophic mice and very old rats
Ramaswamy, K., Palmer, M. L., van der Meulen, J. H., Renoux, A. J., Kostrominova, T. Y., Michele, D. E., & Faulkner, J. A. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2010.201921 · Cited by 235 · see citing works
Vorotnikova, E., McIntosh, D., Dewilde, A. H., Zhang, J., Reing, J. E., Zhang, L., Cordero, K. E., Bedelbaeva, K., Gourevitch, D. L., Heber‐Katz, E., et al. (2010) · Matrix Biology · doi:10.1016/j.matbio.2010.08.007 · Cited by 231 · see citing works
Badylak, S. F., Hoppo, T., Nieponice, A., Gilbert, T. W., Davison, J. M., & Jobe, B. A. (2011) · Tissue Engineering Part A · doi:10.1089/ten.tea.2010.0739 · Cited by 222 · see citing works
Advanced Age Impairs Macrophage Polarization
Mahbub, S., Deburghgraeve, C. R., & Kovacs, E. J. (2012) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.2011.0058 · Cited by 222 · see citing works
Wang, Y., Wehling‐Henricks, M., Samengo, G., & Tidball, J. G. (2015) · Aging Cell · doi:10.1111/acel.12350 · Cited by 205 · see citing works
(1998) · PubMed · Cited by 203 · see citing works
The effects of aging on satellite cells in skeletal muscles of mice and rats
Snow, M. H. (1977) · Cell and Tissue Research · doi:10.1007/bf00220299 · Cited by 201 · see citing works
Dziki, J. L., Wang, D. S., Pineda, C., Sicari, B. M., Rausch, T., & Badylak, S. F. (2017) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.35894 · Cited by 201 · see citing works
ECM hydrogel coating mitigates the chronic inflammatory response to polypropylene mesh
Faulk, D. M., Londono, R., Wolf, M. T., Ranallo, C. A., Carruthers, C. A., Wildemann, J. D., Dearth, C. L., & Badylak, S. F. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.06.057 · Cited by 183 · see citing works
Agrawal, V., Tottey, S., Johnson, S. A., Freund, J. M., Siu, B. F., & Badylak, S. F. (2011) · Tissue Engineering Part A · doi:10.1089/ten.tea.2011.0036 · Cited by 180 · see citing works
Aging impairs peritoneal but not bone marrow‐derived macrophage phagocytosis
Linehan, E., Dombrowski, Y., Snoddy, R., Fallon, P. G., Kissenpfennig, A., & Fitzgerald, D. C. (2014) · Aging Cell · doi:10.1111/acel.12223 · Cited by 169 · see citing works
Macrophage phenotype in response to ECM bioscaffolds
Huleihel, L., Dziki, J. L., Bartolacci, J. G., Rausch, T., Scarritt, M. E., Cramer, M. C., Vorobyov, T., LoPresti, S. T., Swineheart, I. T., White, L. J., et al. (2017) · Seminars in Immunology · doi:10.1016/j.smim.2017.04.004 · Cited by 169 · see citing works
Self-citationThe ins and outs of muscle stem cell aging
Brack, A. S., & Muñoz-Cánoves, P. (2015) · Skeletal Muscle · doi:10.1186/s13395-016-0072-z · Cited by 166 · see citing works
Increased Stiffness in Aged Skeletal Muscle Impairs Muscle Progenitor Cell Proliferative Activity
Lacraz, G., Rouleau, A.-J., Couture, V., Söllrald, T., Drouin, G., Veillette, N., Grandbois, M., & Grenier, G. (2015) · PLoS ONE · doi:10.1371/journal.pone.0136217 · Cited by 156 · see citing works
Zhang, J., Hu, Z. Q., Turner, N. J., Teng, S. F., Cheng, W. Y., Zhou, H. Y., Zhang, L., Hu, H. W., Wang, Q., & Badylak, S. F. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.02.040 · Cited by 141 · see citing works
Sicari, B. M., Johnson, S. A., Siu, B. F., Crapo, P. M., Daly, K. A., Jiang, H., Medberry, C. J., Tottey, S., Turner, N. J., & Badylak, S. F. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.04.017 · Cited by 139 · see citing works
Schlie-Wolter, S., Ngezahayo, A., & Chichkov, B. N. (2013) · Experimental Cell Research · doi:10.1016/j.yexcr.2013.03.016 · Cited by 139 · see citing works
Immunosenescence of macrophages: reduced MHC class II gene expression
Herrero, C., Sebastián, C., Marqués, L., Comalada, M., Xaus, J., Valledor, A. F., Lloberas, J., & Celada, A. (2002) · Experimental Gerontology · doi:10.1016/s0531-5565(01)00205-4 · Cited by 139 · see citing works
The effect of source animal age upon extracellular matrix scaffold properties
Tottey, S., Johnson, S. A., Crapo, P. M., Reing, J. E., Zhang, L., Jiang, H., Medberry, C. J., Reines, B., & Badylak, S. F. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2010.09.006 · Cited by 138 · see citing works
Costa, A., Naranjo, J. D., Londono, R., & Badylak, S. F. (2017) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a025676 · Cited by 135 · see citing works
Zhang, B., Bailey, W. M., Braun, K. J., & Gensel, J. C. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.08.001 · Cited by 125 · see citing works
Brennan-Pierce, E. P., Tang, X., Stewart‐Akers, A. M., Gudas, L. J., & Badylak, S. F. (2008) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.123 · Cited by 125 · see citing works
Hepatocyte Growth Factor Is a Regulator of Monocyte-Macrophage Function
Galimi, F., Cottone, E., Vigna, E., Arena, N., Boccaccio, C., Giordano, S., Naldini, L., & Comoglio, P. M. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.2.1241 · Cited by 124 · see citing works
Matrix-bound nanovesicles recapitulate extracellular matrix effects on macrophage phenotype
Huleihel, L., Bartolacci, J. G., Dziki, J. L., Vorobyov, T., Arnold, B., Scarritt, M. E., Pineda Molina, C., LoPresti, S. T., Brown, B. N., Naranjo, J. D., et al. (2017) · Tissue Engineering Part A · doi:10.1089/ten.tea.2017.0102 · Cited by 116 · see citing works
Self-citationFibronectin peptides mediate HMEC adhesion to porcine-derived extracellular matrix
Hodde, J. P., Record, R. D., Tullius, R. S., & Badylak, S. F. (2002) · Biomaterials · doi:10.1016/s0142-9612(01)00310-6 · Cited by 115 · see citing works
Chemokine receptor CX3CR1 contributes to macrophage survival in tumor metastasis
Zheng, J., Yang, M. H., Shao, J., Miao, Y.-J., Han, J., & Du, J. (2013) · Molecular Cancer · doi:10.1186/1476-4598-12-141 · Cited by 115 · see citing works
Lung Collagens Perpetuate Pulmonary Fibrosis via CD204 and M2 Macrophage Activation
Stahl, M., Schupp, J. C., Jäger, B., Schmid, M., Zissel, G., Müller–Quernheim, J., & Prasse, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0081382 · Cited by 108 · see citing works
Vestergaard, C., Just, H., Nielsen, J. B., Thestrup‐Pedersen, K., & Deleuran, M. S. (2004) · Acta Dermato Venereologica · doi:10.1080/00015550410034444 · Cited by 103 · see citing works
Keane, T. J., Dziki, J. L., Sobieski, E., Smoulder, A. L., Castleton, A. A., Turner, N. J., White, L. J., & Badylak, S. F. (2016) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjw149 · Cited by 99 · see citing works
Gilbert, T. W., Stewart‐Akers, A. M., Sydeski, J., Nguyen, T. D., Badylak, S. F., & Woo, S. L. (2007) · Tissue Engineering · doi:10.1089/ten.2006.0318 · Cited by 88 · see citing works
Increased Plasma HB-EGF Associated with Obesity and Coronary Artery Disease
Matsumoto, S., Kishida, K., Shimomura, I., Maeda, N., Nagaretani, H., Matsuda, M., Nishizawa, H., Kihara, S., Funahashi, T., & Matsuzawa, Y. (2002) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2002.6720 · Cited by 86 · see citing works
Hindle, A. G., Horning, M., Mellish, J. E., & Lawler, J. M. (2009) · Journal of Experimental Biology · doi:10.1242/jeb.025387 · Cited by 85 · see citing works
Yamaji-Kegan, K., Su, Q., Angelini, D. J., Myers, A. C., Cheadle, C., & Johns, R. A. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0904021 · Cited by 82 · see citing works
Agrawal, V., Kelly, J., Tottey, S., Daly, K. A., Johnson, S. A., Siu, B. F., Reing, J. E., & Badylak, S. F. (2011) · Tissue Engineering Part A · doi:10.1089/ten.tea.2011.0257 · Cited by 81 · see citing works
Preparation and characterization of a biologic scaffold from esophageal mucosa
Keane, T. J., Londoño, R., Carey, R. M., Carruthers, C. A., Reing, J. E., Dearth, C. L., D’Amore, A., Medberry, C. J., & Badylak, S. F. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.05.052 · Cited by 76 · see citing works
Kovanen, V., Suominen, H., Risteli, J., & Risteli, L. (1988) · Collagen and Related Research · doi:10.1016/s0174-173x(88)80026-8 · Cited by 74 · see citing works
Wu, Y., Wang, J., Shi, Y., Pu, H., Leak, R. K., Liou, A. K. F., Badylak, S. F., Liu, Z., Zhang, J., Chen, J., et al. (2017) · Cell Transplantation · doi:10.1177/0963689717714090 · Cited by 74 · see citing works
The Role of Basic Fibroblast Growth Factor in Skeletal Muscle Regeneration
Guthridge, M. A., Wilson, M., Cowling, J., Bertolini, J., & Hearn, M. T. W. (1992) · Growth Factors · doi:10.3109/08977199209008871 · Cited by 72 · see citing works
Gryder, R., Lamon, M., & Adams, E. (1975) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)41624-4 · Cited by 68 · see citing works
Edwards, J. P., Zhang, X., & Mosser, D. M. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0802703 · Cited by 55 · see citing works
Epidermal Growth Factor Receptor Down-Regulation Triggers Human Myoblast Differentiation
Leroy, M. C., Perroud, J., Darbellay, B., Bernheim, L., & König, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071770 · Cited by 54 · see citing works
Effects of aging upon the host response to implants
Hachim, D., Wang, N., Lopresti, S. T., Stahl, E. C., Umeda, Y. U., Rege, R. D., Carey, S. T., Mani, D., & Brown, B. N. (2017) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.36013 · Cited by 52 · see citing works
Self-citationPreparation and characterization of a biologic scaffold and hydrogel derived from colonic mucosa
Keane, T. J., Dziki, J. L., Castelton, A., Faulk, D. M., Messerschmidt, V. L., Londoño, R., Reing, J. E., Velankar, S., & Badylak, S. F. (2015) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.33556 · Cited by 51 · see citing works
Diabetes, aging, and their tissue complications
Bucala, R. (2014) · Journal of Clinical Investigation · doi:10.1172/jci75224 · Cited by 50 · see citing works
The Host Response to Endotoxin-Contaminated Dermal Matrix
Daly, K. A., Liu, S., Agrawal, V., Brown, B. N., Huber, A., Johnson, S. A., Reing, J., Sicari, B., Wolf, M., Zhang, X., et al. (2012) · Tissue Engineering Part A · doi:10.1089/ten.tea.2011.0597 · Cited by 46 · see citing works
Self-citationAge-dependent remodeling of connective tissue: role of fibronectin and laminin
Labat‐Robert, J. (2003) · Pathologie Biologie · doi:10.1016/j.patbio.2003.09.006 · Cited by 46 · see citing works
Senescence and quiescence induced compromised function in cultured macrophages
Holt, D. J., & Grainger, D. W. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.06.099 · Cited by 43 · see citing works
Rodriguez-Menocal, L., Faridi, M. H., Martinez, L., Shehadeh, L. A., Duque, J. C., Wei, Y., Mesa, A., Pena, A., Gupta, V., Pham, S. M., et al. (2014) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00641.2013 · Cited by 41 · see citing works
The Expression of MHC Class II Genes in Macrophages Is Cell Cycle Dependent
Xaus, J., Comalada, M., Barrachina, M., Herrero, C., Goñalons, E., Soler, C., Lloberas, J., & Celada, A. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.165.11.6364 · Cited by 40 · see citing works
Obesity in the Context of Aging: Quality of Life Considerations
Corica, F., Bianchi, G. P., Corsonello, A., Mazzella, N., Lattanzio, F., & Marchesini, G. (2014) · PharmacoEconomics · doi:10.1007/s40273-014-0237-8 · Cited by 39 · see citing works
Ostuni, M. A., Guellec, J., Hermand, P., Durand-Smet, P., Combadière, C., Pincet, F., & Déterre, P. (2014) · Biology Open · doi:10.1242/bio.20149845 · Cited by 36 · see citing works
Aging affects the responsiveness of rat peritoneal macrophages to GM-CSF and IL-4
Dimitrijević, M., Stanojević, S., Blagojević, V., Ćuruvija, I., Vujnović, I., Petrović, R., Arsenović-Ranin, N., Vujić, V., & Leposavić, G. (2015) · Biogerontology · doi:10.1007/s10522-015-9620-x · Cited by 31 · see citing works
Longevity and aging. Mechanisms and perspectives
Labat‐Robert, J., & Robert, L. (2015) · Pathologie Biologie · doi:10.1016/j.patbio.2015.08.001 · Cited by 27 · see citing works
Effect of aging on nitric oxide production by rat alveolar macrophages
Koike, E., Kobayashi, T., Mochitate, K., & Murakami, M. (1999) · Experimental Gerontology · doi:10.1016/s0531-5565(99)00061-3 · Cited by 25 · see citing works
Age-related alterations in the strength and collagen content of left colon in rats
Christensen, H. K., Andreassen, T. T., & Oxlund, H. (1992) · International Journal of Colorectal Disease · doi:10.1007/bf00341292 · Cited by 18 · see citing works
Reed, M. J., Karres, N., Eyman, D., Vernon, R. B., & Edelberg, J. M. (2006) · PubMed · Cited by 17 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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-Based Biomaterials and Their Influence Upon Cell Behavior
Cramer, M. C., & Badylak, S. F. (2020) · Annals of Biomedical Engineering · doi:10.1007/s10439-019-02408-9 · Cited by 196 · see citing works
Extracellular Matrix‐Based Strategies for Immunomodulatory Biomaterials Engineering
Rowley, A. T., Nagalla, R. R., Wang, S., & Liu, W. F. (2019) · Advanced Healthcare Materials · doi:10.1002/adhm.201801578 · Cited by 193 · see citing works
Preparation and Use of Decellularized Extracellular Matrix for Tissue Engineering
McInnes, A. D., Moser, M., & Chen, D. (2022) · Journal of Functional Biomaterials · doi:10.3390/jfb13040240 · Cited by 141 · see citing works
Increased immunosuppression impairs tissue homeostasis with aging and age-related diseases
Salminen, A. (2020) · Journal of Molecular Medicine · doi:10.1007/s00109-020-01988-7 · Cited by 110 · see citing works
Duan, Y.-Y., Zheng, H.-H., Li, Z., Yao, Y., Ding, J., Wang, X., Nakkala, J. R., Zhang, D., Wang, Z., Zuo, X., et al. (2020) · Biomaterials · doi:10.1016/j.biomaterials.2020.120012 · Cited by 77 · see citing works
Abdollahiyan, P., Oroojalian, F., Hejazi, M., de la Guárdia, M., & Mokhtarzadeh, A. (2021) · Journal of Controlled Release · doi:10.1016/j.jconrel.2021.04.003 · Cited by 71 · see citing works
Innovative approaches to wound healing: insights into interactive dressings and future directions
Yadav, R., Kumar, R., Kathpalia, M., Ahmed, B., Dua, K., Gulati, M., Singh, S. K., Singh, P. J., Kumar, S., Shah, R., et al. (2024) · Journal of Materials Chemistry B · doi:10.1039/d3tb02912c · Cited by 72 · see citing works
Extracellular matrix scaffold-immune microenvironment modulates tissue regeneration
Yu, Y., Zhang, W., Liu, X., Wang, H., Shen, J., Xiao, H., Mei, J., Chai, Y., & Wen, G. (2021) · Composites Part B Engineering · doi:10.1016/j.compositesb.2021.109524 · Cited by 63 · see citing works
Bioscaffold-Induced Brain Tissue Regeneration
Modo, M. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01156 · Cited by 63 · see citing works
Decellularized Extracellular Matrix for Tissue Engineering (Review)
Isaeva, E. V., Beketov, E. E., Arguchinskaya, N. V., Иванов, С. А., Шегай, П. В., & Каприн, А. Д. (2022) · Современные технологии в медицине · doi:10.17691/stm2022.14.3.07 · Cited by 42 · see citing works
Koch, S. E., de Kort, B. J., Holshuijsen, N., Brouwer, H. F. M., van der Valk, D. C., Dankers, P. Y. W., van Luijk, J. A. K. R., Hooijmans, C. R., de Vries, R. B. M., Bouten, C. V. C., et al. (2022) · npj Regenerative Medicine · doi:10.1038/s41536-022-00211-0 · Cited by 33 · see citing works
Modo, M., & Badylak, S. F. (2019) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2019.05.013 · Cited by 33 · see citing works
Xie, X., Wang, W., Cheng, J. Q., Liang, H., Lin, Z., Zhang, T., Lu, Y., & Li, Q. (2020) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2020.110903 · Cited by 32 · see citing works
Effect of different aged cartilage ECM on chondrogenesis of BMSCs in vitro and in vivo
Wang, X., Lu, Y., Wang, W., Wang, Q., Liang, J., Fan, Y., & Zhang, X. (2020) · Regenerative Biomaterials · doi:10.1093/rb/rbaa028 · Cited by 30 · 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
“For instance, LoPresti and Brown investigated the influence of age using decellularized small intestine submucosa (SIS) derived from pigs of different ages (12, 26, and 52 weeks) on the phenotype and function of bone marrow macrophages obtained from mice aged 2 or 18 months [82].”
BackgroundLoPresti, S. T., Popovic, B., Kulkarni, M., Skillen, C. D., & Brown, B. N. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2019.119376 · Cited by 24 · see citing works
Self-citationHachim, D., LoPresti, S. T., Rege, R. D., Umeda, Y. U., Iftikhar, A., Nolfi, A. L., Skillen, C. D., & Brown, B. N. (2020) · Biomaterials Science · doi:10.1039/d0bm00568a · Cited by 23 · see citing works
Self-citationHachim, D., Iftikhar, A., LoPresti, S. T., Nolfi, A. L., Ravichandar, S., Skillen, C. D., & Brown, B. N. (2019) · Journal of Controlled Release · doi:10.1016/j.jconrel.2019.05.020 · Cited by 22 · see citing works
Self-citationHogan, K. J., Smoak, M. M., Koons, G. L., Perez, M. R., Bedell, M. L., Jiang, E. Y., Young, S. W., & Mikos, A. G. (2022) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.37355 · Cited by 19 · see citing works
Ghuman, H., Hitchens, T. K., & Modo, M. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.116090 · Cited by 18 · see citing works
Zhang, C., Xia, D., Li, J., Zheng, Y., Weng, B., Mao, H., Mei, J., Wu, T., Li, M., & Zhao, J. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.818191 · Cited by 13 · see citing works
Characterizing the Macrophage Response to Immunomodulatory Biomaterials Through Gene Set Analyses
Blatt, S. E., Lurier, E. B., Risser, G. E., & Spiller, K. L. (2020) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2019.0309 · Cited by 13 · see citing works
Kulkarni, M. M., Popovic, B., Nolfi, A. L., Skillen, C. D., & Brown, B. N. (2025) · Biomaterials · doi:10.1016/j.biomaterials.2025.123204 · Cited by 12 · see citing works
Self-citationCramer, M. C., Borrelli, M., Mathews, L. R., Dewey, M. J., Schwarzmann, W. E., Soman, V., Sembrat, J., Rojas, M. M., McTiernan, C., Chandran, U. R., et al. (2024) · International Journal of Cardiology · doi:10.1016/j.ijcard.2024.132892 · Cited by 7 · see citing works
Beyond polarization: macrophage senescence in immunoregulation and cancer therapy
Mei, S., Zhang, L., Dai, X., Ji, S., Shen, J., & He, W. (2025) · International Journal of Biological Sciences · doi:10.7150/ijbs.115921 · Cited by 7 · see citing works
Bioengineering liver tissue by repopulation of decellularised scaffolds
Afzal, Z., & Huguet, E. (2023) · World Journal of Hepatology · doi:10.4254/wjh.v15.i2.151 · Cited by 6 · see citing works
Decellularized Scaffolds for Tissue Regeneration: Techniques and Applications
Biazar, E. (2024) · Biomedical engineering · doi:10.5772/intechopen.1007748 · Cited by 4 · see citing works
de Santis, J. O., de Sousa, G. R., Queiróz, R. G. D. P., Cândido, M. F., Almeida, F. B. D. R., Rezende, C. P., Ruy, P. D. C., Arini, G. S., Coyle, B., Wade, P., et al. (2025) · Human Cell · doi:10.1007/s13577-025-01181-3 · Cited by 4 · see citing works
Bhattacharya, T., Bej, A., Das, A., Bartwal, S. S., & Nandi, A. (2025) · Regenerative Engineering and Translational Medicine · doi:10.1007/s40883-025-00499-6 · Cited by 2 · see citing works
Matrix bound nanovesicles: A great promise for TERM in less than a decade of research
Francesco, D. D., Mantovani, D., Hussey, G. S., & Boccafoschi, F. (2025) · Matrix Biology · doi:10.1016/j.matbio.2025.10.001 · Cited by 3 · see citing works
Extracellular Matrices In Gynecological Surgery – Literature Review
Banacu, M., Socea, B., Pelinaru, A., & Lascăr, I. (2020) · Archives of the Balkan Medical Union · doi:10.31688/abmu.2020.55.2.14 · Cited by 2 · see citing works
Insights into decellularized matrix-based therapeutic delivery systems in myocardial infarction
Bhattacharya, T., Kundu, M., Patil, P. D., Bhattacharya, I., Sibi, N. P., Sahu, A., Sarkar, S., Sreedhar, R., & Arumugam, S. (2025) · Journal of Drug Delivery Science and Technology · doi:10.1016/j.jddst.2025.107618
- Authors
- LoPresti, S. T., & Brown, B. N.
- Affiliations
- University of Pittsburgh (US)
- Corresponding author
- Brown, Bryan N.
- Venue
- Journal of Immunology and Regenerative Medicine
- Publisher
- Elsevier BV
- Published
- 2018-03
- Volume
- 1
- Pages
- 57-66
- ISSN
- 2468-4988 (ISSN-L)
- PMC
- PMC6082641
- OpenAlex
- W2799621257
- Cited by
- 33
- References
- 85
- Citations by year
- 2025: 6 · 2024: 4 · 2023: 2 · 2022: 5 · 2021: 2 · 2020: 7 · 2019: 7
- FWCI
- 4.16
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Journal of Immunology and Regenerative Medicine (acceptedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (K12HD043441, R03AG043606, R01AG055564, T32EB001026)
- Topics
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Health Sciences › Medicine › Rehabilitation › Wound Healing and Treatments
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Keywords
- extracellular matrix biomaterials, donor age, macrophage phenotype, macrophage polarization, small intestinal submucosa, bone marrow-derived macrophages, inducible nitric oxide synthase, Fizz1, nitric oxide, MHC class II, tissue remodeling, aging
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