The DOI matches its Crossref record; 63 of the 63 references it cites were found in a registry or an index.
Recruitment of Progenitor Cells by an Extracellular Matrix Cryptic Peptide in a Mouse Model of Digit Amputation
Open accessAbstract
Biologic scaffolds composed of extracellular matrix (ECM) have been used successfully in preclinical models and humans for constructive remodeling of functional, site-appropriate tissue after injury. The mechanisms underlying ECM-mediated constructive remodeling are not completely understood, but scaffold degradation and site-directed recruitment of both differentiated and progenitor cells are thought to play critical roles. Previous studies have shown that degradation products of ECM scaffolds can recruit a population of progenitor cells both in vitro and in vivo. The present study identified a single cryptic peptide derived from the α subunit of the collagen III molecule that is chemotactic for a well-characterized perivascular stem cell in vitro and causes the site-directed accumulation of progenitor cells in vivo. The oligopeptide was additionally chemotactic for human cortical neural stem cells, rat adipocyte stem cells, C2C12 myoblast cells, and rat Schwann cells in vitro. In an adult murine model of digit amputation, treatment with this peptide after mid-second phalanx amputation resulted in a greater number of Sox2+ and Sca1+,Lin- cells at the site of injury compared to controls. Since progenitor cell activation and recruitment are key prerequisites for epimorphic regeneration in adult mammalian tissues, endogenous site-directed recruitment of such cells has the potential to alter the default wound healing response from scar tissue toward regeneration.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
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?
In the citing paper
“Following implantation, these natural ECM scaffolds undergo a degree of degradation, releasing matricryptic peptides and growth factors. This process triggers a shift in macrophage polarization from pro-inflammatory (M1) phenotype to an anti-inflammatory regenerative phenotype (M2 macrophages), promoting angiogenesis and recruiting stem/progenitor cell toward the implanted tissue for constructive”
From Liver tissue engineering using decellularized scaffolds: Current progress, challenges, and opportunities (2024) · cites this paper as [57]
Citations
Cites
Identification of stem cells in small intestine and colon by marker gene Lgr5
Barker, N., van Es, J. H., Kuipers, J., Kujala, P., van den Born, M., Cozijnsen, M., Haegebarth, A., Korving, J., Begthel, H., Peters, P. J., et al. (2007) · Nature · doi:10.1038/nature06196 · Cited by 5,687
Endostatin: an endogenous inhibitor of angiogenesis and tumor growth
O'Reilly, M. S., Boehm, T., Shing, Y., Fukai, N., Vasios, G., Lane, W. S., Flynn, E., Birkhead, J. R., Olsen, B. R., & Folkman, J. (1997) · Cell · doi:10.1016/s0092-8674(00)81848-6 · Cited by 4,486
A perivascular origin for mesenchymal stem cells in multiple human organs
Crisan, M., Yap, S., Casteilla, L., Chen, C.-W., Corselli, M., Park, T. S., Andriolo, G., Sun, B., Zheng, B., Zhang, L., et al. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2008.07.003 · Cited by 3,991 · cited 1×
“Bruno Peault, and these cells were isolated and prepared as previously described.(30) Perivascular stem cells were cultured in high-glucose Dulbecco’s modified Eagle’s medium (DMEM; Invitrogen) containing 20% fetal bovine serum (FBS; Thermo), 100 U/mL penicillin, and 100 mg/mL streptomycin (Sigma) at 37 C in 5% CO2.”
MethodSelf-citationAn 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
Self-citationDefensins: antimicrobial peptides of innate immunity
Ganz, T. (2003) · Nature Reviews Immunology · doi:10.1038/nri1180 · Cited by 3,066
Perfusion-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
Purified hematopoietic stem cells can differentiate into hepatocytes in vivo
Lagasse, E., Connors, H., Al-Dhalimy, M., Reitsma, M., Dohse, M., Osborne, L., Wang, X., Finegold, M., Weissman, I. L., & Grompe, M. (2000) · Nature Medicine · doi:10.1038/81326 · Cited by 2,314
Uygun, B. E., Soto-Gutierrez, A., Yagi, H., Izamis, M.-L., Guzzardi, M. A., Shulman, C., Milwid, J., Kobayashi, N., Tilles, A., Berthiaume, F., et al. (2010) · Nature Medicine · doi:10.1038/nm.2170 · Cited by 1,370
Regeneration 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
Cells keep a memory of their tissue origin during axolotl limb regeneration
Kragl, M., Knapp, D., Nacu, E., Khattak, S., Maden, M., Epperlein, H. H., & Tanaka, E. M. (2009) · Nature · doi:10.1038/nature08152 · Cited by 854
The extracellular matrix as a scaffold for tissue reconstruction
Badylak, S. F. (2002) · Seminars in Cell and Developmental Biology · doi:10.1016/s1084952102000940 · Cited by 826
Self-citationLee, C. H., Cook, J. L., Mendelson, A., Moioli, E. K., Yao, H., & Mao, J. J. (2010) · The Lancet · doi:10.1016/s0140-6736(10)60668-x · Cited by 614
Small intestinal submucosa as a large diameter vascular graft in the dog
Badylak, S. F., Lantz, G. C., Coffey, A. C., & Geddes, L. A. (1989) · Journal of Surgical Research · doi:10.1016/0022-4804(89)90050-4 · Cited by 613
Self-citationHistone H3 phosphorylation and cell division
Hans, F., & Dimitrov, S. I. (2001) · Oncogene · doi:10.1038/sj.onc.1204326 · Cited by 519
Molecular Basis for the Nerve Dependence of Limb Regeneration in an Adult Vertebrate
Kumar, A., Godwin, J. W., Gates, P. B., Garza-Garcı́a, A., & Brockes, J. P. (2007) · Science · doi:10.1126/science.1147710 · Cited by 487
Davis, G. E., Bayless, K. J., Davis, M. J., & Meininger, G. A. (2000) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65020-1 · Cited by 463
Anti-angiogenic cues from vascular basement membrane collagen.
Colorado, P. C., Torre, A., Kamphaus, G. D., Maeshima, Y., Hopfer, H., Takahashi, K., Volk, R., Zamborsky, E. D., Herman, S., Sarkar, P. K., et al. (2000) · PubMed · Cited by 421
EXTRACELLULAR MATRIX BIOSCAFFOLDS FOR ORTHOPAEDIC APPLICATIONS
Valentin, J. E., Badylak, J. S., McCabe, G. P., & Badylak, S. F. (2006) · Journal of Bone and Joint Surgery · doi:10.2106/jbjs.e.01008 · Cited by 410
Self-citationDegradation 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
Self-citationRegeneration of Dental-Pulp-like Tissue by Chemotaxis-Induced Cell Homing
Kim, J. Y., Xin, X., Moioli, E. K., Chung, J., Lee, C., Chen, M., Fu, S. Y., Koch, P. D., & Mao, J. J. (2010) · Tissue Engineering Part A · doi:10.1089/ten.tea.2010.0181 · Cited by 363
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
Self-citationMicroarray and cDNA sequence analysis of transcription during nerve-dependent limb regeneration
Monaghan, J. R., EPP, L. G., Putta, S., Page, R. B., Walker, J. A., Beachy, C. K., Zhu, W. Z., Pao, G. M., Verma, I. M., Hunter, T. R., et al. (2009) · BMC Biology · doi:10.1186/1741-7007-7-1 · Cited by 309
Mase, V. J., Hsu, J. R., Wolf, S. E., Wenke, J. C., Baer, D. G., Owens, J. G., Badylak, S. F., & Walters, J. (2010) · Orthopedics · doi:10.3928/01477447-20100526-24 · Cited by 291
Self-citationEsophageal Reconstruction with ECM and Muscle Tissue in a Dog Model
Badylak, S. F., Vorp, D. A., Spievack, A. R., Simmons-Byrd, A., Hanke, J., Freytes, D. O., Thapa, A., Gilbert, T. W., & Nieponice, A. (2005) · Journal of Surgical Research · doi:10.1016/j.jss.2005.03.002 · Cited by 291
Self-citationAntiangiogenic Activity of Restin, NC10 Domain of Human Collagen XV: Comparison to Endostatin
Ramchandran, R., Dhanabal, M., Volk, R., Waterman, M. J. F., Segal, M. S., Lu, H. A. J., Knebelmann, B., & Sukhatme, V. P. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.0248 · Cited by 290
Resorbable bioscaffold for esophageal repair in a dog model
Badylak, S. F., Meurling, S., Chen, M., Spievack, A. R., & Simmons-Byrd, A. (2000) · Journal of Pediatric Surgery · doi:10.1053/jpsu.2000.7834 · Cited by 277
Self-citationBiaxial strength of multilaminated extracellular matrix scaffolds
Freytes, D. O., Badylak, S. F., Webster, T. J., Geddes, L. A., & Rundell, A. E. (2003) · Biomaterials · doi:10.1016/j.biomaterials.2003.09.015 · Cited by 235
Self-citationChemoattraction of Progenitor Cells by Remodeling Extracellular Matrix Scaffolds
Beattie, A. J., Gilbert, T. W., Guyot, J. P., Yates, A. J., & Badylak, S. F. (2008) · Tissue Engineering Part A · doi:10.1089/ten.tea.2008.0162 · Cited by 218
Self-citationSellaro, T. L., Ravindra, A. K., Stolz, D. B., & Badylak, S. F. (2007) · Tissue Engineering · doi:10.1089/ten.2006.0437 · Cited by 214
Self-citationSmall Intestinal Submucosa as a Small-Diameter Arterial Graft in the Dog
Lantz, G. C., Badylak, S. F., Coffey, A. C., Geddes, L. A., & Blevins, W. E. (1990) · Journal of Investigative Surgery · doi:10.3109/08941939009140351 · Cited by 210
Self-citationAntimicrobial activity of cecropins
Moore, A., Beazley, W. D., Bibby, M. C., & DeVine, D. (1996) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/37.6.1077 · Cited by 206
Extracellular matrix scaffold devices for rotator cuff repair
Derwin, K. A., Badylak, S. F., Steinmann, S. P., & Iannotti, J. P. (2010) · Journal of Shoulder and Elbow Surgery · doi:10.1016/j.jse.2009.10.020 · Cited by 205
Self-citationLi, F., Li, W., Johnson, S. A., Ingram, D. A., Yöder, M. C., & Badylak, S. F. (2004) · Endothelium · doi:10.1080/10623320490512390 · Cited by 197
Self-citationAksu, A. E., Rubin, J. P., Dudas, J. R., & Marra, K. G. (2008) · Annals of Plastic Surgery · doi:10.1097/sap.0b013e3180621ff0 · Cited by 196
Zantop, T., Gilbert, T. W., Yöder, M. C., & Badylak, S. F. (2006) · Journal of Orthopaedic Research® · doi:10.1002/jor.20071 · Cited by 186
Self-citationMarrow-derived cells populate scaffolds composed of xenogeneic extracellular matrix
Badylak, S. F., Park, K., Peppas, N. A., McCabe, G. P., & Yöder, M. C. (2001) · Experimental Hematology · doi:10.1016/s0301-472x(01)00729-9 · Cited by 176
Self-citationBone Metabolism Markers in Sports Medicine
Banfi, G., Lombardi, G., Colombini, A., & Lippi, G. (2010) · Sports Medicine · doi:10.2165/11533090-000000000-00000 · Cited by 175
An extracellular matrix scaffold for esophageal stricture prevention after circumferential EMR
Nieponice, A., McGrath, K., Qureshi, I. R., Beckman, E. J., Luketich, J. D., Gilbert, T. W., & Badylak, S. F. (2008) · Gastrointestinal Endoscopy · doi:10.1016/j.gie.2008.04.022 · Cited by 171
Self-citationKochupura, P. V., Azeloglu, E. U., Kelly, D. J., Doronin, S. V., Badylak, S. F., Krukenkamp, I. B., Cohen, I. S., & Gaudette, G. R. (2005) · Circulation · doi:10.1161/circulationaha.104.524355 · Cited by 168
Self-citationPreliminary experimental anticancer activity of cecropins.
Moore, A., Devine, D., & Bibby, M. C. (1994) · PubMed · Cited by 165
Epimorphic regeneration approach to tissue replacement in adult mammals
Agrawal, V., Johnson, S. A., Reing, J. E., Zhang, L., Tottey, S., Wang, G., Hirschi, K. K., Braunhut, S. J., Gudas, L. J., & Badylak, S. F. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0905851106 · Cited by 162
Self-citationLewis, J. P., & Trobaugh, F. E. (1964) · Nature · doi:10.1038/204589a0 · Cited by 161
Melman, L. M., Jenkins, E. D., Hamilton, N. A., Bender, L. C., Brodt, M. D., Deeken, C. R., Greco, S., Frisella, M. M., & Matthews, B. D. (2011) · Hernia · doi:10.1007/s10029-010-0770-0 · Cited by 127
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
Self-citationHistology after dural grafting with small intestinal submucosa
Cobb, M. A., Badylak, S. F., Janas, W., & Boop, F. A. (1996) · Surgical Neurology · doi:10.1016/s0090-3019(96)00202-9 · Cited by 119
Self-citationZalavras, C. G., Gardocki, R., Huang, E. Y., Stevanovic, M. V., Hedman, T., & Tibone, J. E. (2006) · Journal of Shoulder and Elbow Surgery · doi:10.1016/j.jse.2005.06.007 · Cited by 106
Surgical technique for xenograft (SIS) augmentation of rotator-cuff repairs
Metcalf, M. H., Savoie, F. H. “., & Kellum, B. (2002) · Operative Techniques in Orthopaedics · doi:10.1053/otor.2002.36298 · Cited by 102
Magainins: A new family of membrane-active host defense peptides
Berkowitz, B. A., Bevins, C. L., & ZASLOFF, M. A. (1990) · Biochemical Pharmacology · doi:10.1016/0006-2952(90)90138-b · Cited by 102
Tottey, S., Corselli, M., Jeffries, E. M., Londoño, R., Péault, B., & Badylak, S. F. (2010) · Tissue Engineering Part A · doi:10.1089/ten.tea.2010.0188 · Cited by 101
Self-citationAgrawal, V., Brown, B. N., Beattie, A. J., Gilbert, T. W., & Badylak, S. F. (2009) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.200 · Cited by 99
Self-citationReinforcement of Esophageal Anastomoses With an Extracellular Matrix Scaffold in a Canine Model
Nieponice, A., Gilbert, T. W., & Badylak, S. F. (2006) · The Annals of Thoracic Surgery · doi:10.1016/j.athoracsur.2006.06.036 · Cited by 95
Self-citationMorphologic Assessment of Extracellular Matrix Scaffolds for Patch Tracheoplasty in a Canine Model
Gilbert, T. W., Gilbert, S., Madden, M., Reynolds, S. D., & Badylak, S. F. (2008) · The Annals of Thoracic Surgery · doi:10.1016/j.athoracsur.2008.04.071 · Cited by 80
Self-citationHodde, J. P., Badylak, S. F., & Shelbourne, K. D. (1997) · Tissue Engineering · doi:10.1089/ten.1997.3.27 · Cited by 78
Self-citationRepair of the tympanic membrane with urinary bladder matrix
Parekh, A., Mantle, B. A., Banks, J. M., Swarts, J. D., Badylak, S. F., Dohar, J. E., & Hebda, P. A. (2009) · The Laryngoscope · doi:10.1002/lary.20233 · Cited by 76
Self-citationBoruch, A. V., Nieponice, A., Qureshi, I. R., Gilbert, T. W., & Badylak, S. F. (2009) · Journal of Surgical Research · doi:10.1016/j.jss.2009.02.014 · Cited by 74
Self-citationBarth, D., Kyrieleis, O. J. P., Frank, S., Renner, C., & Moroder, L. (2003) · Chemistry - A European Journal · doi:10.1002/chem.200304918 · Cited by 71
KANOUPAKIS, E. M., Manios, E. G., Kallergis, E. M., Mavrakis, H. E., Goudis, C. A., Saloustros, I. G., Milathianaki, M. E., CHLOUVERAKIS, G. I., & Vardas, P. E. (2010) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2010.02.040 · Cited by 63
In vivo bladder regeneration using small intestinal submucosa: experimental study
Caione, P., Capozza, N., Zavaglia, D., Palombaro, G., & Boldrini, R. (2006) · Pediatric Surgery International · doi:10.1007/s00383-006-1705-9 · Cited by 60
Kelly, D. J., Rosen, A. B., Schuldt, A. J. T., Kochupura, P. V., Doronin, S. V., Potapova, I. A., Azeloglu, E. U., Badylak, S. F., Brink, P. R., Cohen, I. S., et al. (2009) · Tissue Engineering Part A · doi:10.1089/ten.tea.2008.0430 · Cited by 51
Self-citationKitahara, T., Takeishi, Y., Arimoto, T., Niizeki, T., Koyama, Y., Sasaki, T., Suzuki, S., Nozaki, N., Hirono, O., Nitobe, J., et al. (2007) · Circulation Journal · doi:10.1253/circj.71.929 · Cited by 36
WOUND HEALING PROCESSES IN AMPUTATED MOUSE DIGITS
Schotté, O. E., & Smith, C. B. (1959) · Biological Bulletin · doi:10.2307/1538866 · Cited by 35
Davis, N. F., Callanan, A., McGuire, B. B., Mooney, R., Flood, H. D., & McGloughlin, T. M. (2010) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2010.11.005 · Cited by 23
Witteman, B. P. L., Foxwell, T. J., Monsheimer, S., Gelrud, A., Eid, G. M., Nieponice, A., O’Rourke, R. W., Hoppo, T., Bouvy, N. D., Badylak, S. F., et al. (2009) · Journal of Gastrointestinal Surgery · doi:10.1007/s11605-009-1053-x · Cited by 22
Self-citation
Flagged first, then by citations
Research works printed but not linked: 4
- Mase V.J., 2010, Orthopedics, 33, 511
- Moore A.J., 1994, Pept Res, 7, 265
- Colorado P.C., 2000, Cancer Res, 60, 2520
- 10.1016/j.jjs.2010.08.035 · DOI
Cited by
Sorted by citations
Extracellular matrix-based materials for regenerative medicine
Hussey, G. S., Dziki, J. L., & Badylak, S. F. (2018) · Nature Reviews Materials · doi:10.1038/s41578-018-0023-x · Cited by 844
Self-citationExtracellular matrix hydrogels from decellularized tissues: Structure and function
Saldin, L. T., Cramer, M. C., Velankar, S., White, L. J., & Badylak, S. F. (2016) · Acta Biomaterialia · doi:10.1016/j.actbio.2016.11.068 · Cited by 841
Self-citationZhang, X., Chen, X., Hong, H., Hu, R., Liu, J., & Liu, C. (2022) · Bioactive Materials · doi:10.1016/j.bioactmat.2021.09.014 · Cited by 680
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 532
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 498
Self-citation
Metadata
- Authors
- Agrawal, V., Tottey, S., Johnson, S. A., Freund, J. M., Siu, B. F., & Badylak, S. F.
- Affiliations
- University of Pittsburgh (US)
- Corresponding author
- Badylak, Stephen F.
- Venue
- Tissue Engineering Part A
- Publisher
- SAGE Publications
- Published
- 2011-10
- Volume
- 17
- Issue
- 19-20
- Pages
- 2435-2443
- ISSN
- 1937-3341 (ISSN-L)
- 1937-335X
- PMC
- PMC3179613
- OpenAlex
- W2169478984
- Cited by
- 180
- References
- 63
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 9 · 2023: 12 · 2022: 3 · 2021: 12 · 2020: 16 · 2019: 7 · 2018: 16 · 2017: 20 · 2016: 18 · 2015: 17 · 2014: 14 · 2013: 10 · 2012: 13
- FWCI
- 13.11
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Tissue Engineering Part A (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (W81XWH, W81XWH-08-2-0032)
- National Heart, Lung, and Blood Institute (1F30-HL102990, F30HL102990)
- Topics
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Health Sciences › Medicine › Surgery › Wound Healing and Treatments
- Physical Sciences › Engineering › Biomedical Engineering › Bone Tissue Engineering Materials
- Keywords
- extracellular matrix, cryptic peptides, type III collagen, progenitor cell recruitment, chemotaxis, digit amputation, epimorphic regeneration, perivascular stem cells, neural stem cells, Schwann cells, myoblasts, scaffold degradation, wound healing, scar tissue, tissue engineering scaffolds
- MeSH terms
- Amputation, Surgical, Animals, Cell Count, Cell Separation, Chemotaxis, Disease Models, Animal, Extracellular Matrix, Forelimb, Humans, Peptides, Stem Cells, Toes, Reproducibility of Results, Sus scrofa, Cell Proliferation, Mice, Rats, SOXB1 Transcription Factors
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