CoChat
Sign Up
Cited by 35Tissue Engineering and Regenerative MedicineElectrospun Nanofibers in Biomedical ApplicationsCollagen: Extraction and Characterization

Antigen removal process preserves function of small diameter venous valved conduits, whereas SDS-decellularization results in significant valvular insufficiency

Open access
Lopera Higuita, Manuela, Griffiths, Leigh G.·2020·Acta Biomaterialia
DOI 10.1016/j.actbio.2020.03.003PMC PMC7164717
Open this paper in CoChat — free account

Abstract

Chronic venous disease (CVD) is the most common reported chronic condition in the United States, affecting more than 25 million Americans. Regardless of its high occurrence, current therapeutic options are far from ideal due to their palliative nature. For best treatment outcomes, challenging cases of chronic venous insufficiency (CVI) are treated by repair or replacement of venous valves. Regrettably, the success of venous valve transplant is dependent on the availability of autologous venous valves and hindered by the possibility of donor site complications and increased patient morbidity. Therefore, the use of alternative tissue sources to provide off-the-shelf venous valve replacements has potential to be extremely beneficial to the field of CVI. This manuscript demonstrates the capability of producing off-the-shelf fully functional venous valved extracellular matrix (ECM) scaffold conduits from bovine saphenous vein (SV), using an antigen removal (AR) method. AR ECM scaffolds maintained native SV structure-function relationships and associated venous valves function. Conversely, SDS decellularization caused significant changes to the collagen and elastin macromolecular structures, resulting in collagen fibril merging, elimination of fibril crimp, amalgaming collagen fibers and fragmentation of the inner elastic lamina. ECM changes induced by SDS decellularization resulted in significant venous valve dysfunction. Venous valved conduits generated using the AR approach have potential to serve as off-the-shelf venous valve replacements for CVI. STATEMENT OF SIGNIFICANCE: Retention of the structure and composition of extracellular matrix (ECM) proteins within xenogeneic scaffolds for tissue engineering is of crucial importance, due to the undeniable effect ECM proteins can impose on repopulating cells and function of the resultant biomaterial. This manuscript demonstrates that alteration or elimination of ECM proteins via commonly utilized decellularization approach results in complete disruption of venous valve function. Conversely, retention of the delicate ECM structure and composition of native venous tissue, using an antigen removal tissue processing method, results in preservation of native venous valve function.

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.actbio.2020.03.003

Cites

6 of 6 references verified0 citation errors · 0 not checkable

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.

A few free checks a day · papers already verified open instantly · results are public

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?

  • Damage to elastin can lead to release of elastin peptides through harsh decellularization or depletion of GAGs, and liberated elastin particles can induce monocyte chemotaxis, promote T helper cell differentiation into inflammatory phenotypes, and contribute to antibody-mediated inflammatory responses.

    “Damage to elastin can lead to the release of elastin peptides, either through harsh decellularization processes or the depletion of glycosaminoglycans (GAGs). GAGs play a crucial role in protecting elastin from protease activity [[76], [77], [78]]. The liberated elastin particles could induce monocyte chemotaxis, promote T helper cell differentiation into inflammatory phenotypes (TH1 and TH17),”

    From Liver tissue engineering using decellularized scaffolds: Current progress, challenges, and opportunities (2024) · cites this paper as [76]

    Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.

    Experimental — accuracy not yet measured

  • C3b components bind their corresponding receptors on M1 macrophages and trigger release of matrix metalloproteinases (MMPs), the principal ECM degradative enzyme, mediating dECM graft failure.

    “C3b components bind their corresponding receptors on these M1 macrophages and trigger the release of matrix metalloproteinases (MMPs), the principal ECM degradative enzyme, mediating the dECM graft failure [46, 47].”

    From Immunogenicity of decellularized extracellular matrix scaffolds: a bottleneck in tissue engineering and regenerative medicine (2023) · cites this paper as [46]

    The Discussion states that activated macrophages produce matrix metalloproteinases that disrupt ECM scaffolds, potentially causing functional deficiencies. It does not describe C3b binding to receptors on M1 macrophages as the trigger, or identify MMPs as the principal ECM-degradative enzyme. No page number is available in our copy. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • During decellularization of elastin-containing tissues, elastin may be denatured leading to release of elastin particles, directly via harsh agents such as SDS and trypsin or indirectly via depletion of GAGs, which protect elastin from protease activity.

    “During the decellularization of such tissues, elastin may be denatured that leads to the release of elastin particles; directly via the impact of harsh agents such as SDS and trypsin or indirectly via the depletion of GAGs, which have a critical role in protecting elastin from protease activity [46, 106–108].”

    From Immunogenicity of decellularized extracellular matrix scaffolds: a bottleneck in tissue engineering and regenerative medicine (2023) · cites this paper as [46]

    Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.

    Experimental — accuracy not yet measured

  • Decellularization protocols differ in their ability to remove each immunogenic cell protein; a process that removes cytosolic immunogen proteins may not effectively remove immunogen cytoskeleton proteins.

    “While a decellularization process successfully removes cytosolic immunogen proteins, it might be unable to remove immunogen cytoskeleton proteins effectively [46].”

    From Immunogenicity of decellularized extracellular matrix scaffolds: a bottleneck in tissue engineering and regenerative medicine (2023) · cites this paper as [46]

    The Introduction (page unavailable) says antigens can persist in completely acellular scaffolds, supporting the general point that decellularization may leave immunogenic material behind. It does not establish the specific contrast claimed: successful removal of cytosolic immunogen proteins alongside ineffective removal of cytoskeletal immunogen proteins. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

  • The amount of remaining hydrophilic and hydrophobic antigens precisely correlates with the immunogenicity of dECM scaffolds, unlike the level of DNA retention.

    “Unlike the level of DNA retention, the amount of remaining hydrophilic and hydrophobic antigens precisely correlates with the immunogenicity of the dECM scaffolds [25, 46].”

    From Immunogenicity of decellularized extracellular matrix scaffolds: a bottleneck in tissue engineering and regenerative medicine (2023) · cites this paper as [46]

    The Introduction (page not specified) says residual antigen content correlates with in vivo adaptive immune response, whereas scaffold cellularity is poorly correlated with residual antigen content. The Results measure DNA and hydrophilic and lipophilic antigens, but the paper does not establish a precise immunogenicity correlation for each antigen fraction or directly compare that correlation with DNA retention. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

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

Flagged first, then by citations

Research works printed but not linked: 93

  1. [1]Eberhardt RT and Raffetto JD, Chronic venous insufficiency. Circulation, 2014 130(4): p. 333– 46. 25047584
  2. [2]Nicolaides AN, Cardiovascular Disease E, Research T, European S Society of Vascular, T.I.A.S.A.C. Organization, A. International Union of, and C. Union Internationale de Phlebologie at the Abbaye des Vaux de, Investigation of chronic venous insufficiency: A consensus statement (France, March 5–9, 1997). Circulation, 2000 102(20): p. E126– 63. 11076834
  3. [3]Novak CJ, Khimani N, Kaye AD, Jason Yong R, and Urman RD, Current Therapeutic Interventions in Lower Extremity Venous Insufficiency: a Comprehensive Review. Curr Pain Headache Rep, 2019 23(3): p. 16. 30830460
  4. [4]Meissner MH, Moneta G, Burnand K, Gloviczki P, Lohr JM, Lurie F, Mattos MA, McLafferty RB, Mozes G, Rutherford RB, Padberg F, and Sumner DS, The hemodynamics and diagnosis of venous disease. J Vasc Surg, 2007 46 Suppl S: p. 4S– 24S. 18068561
  5. [5]Labropoulos N, Leon M, Nicolaides AN, Giannoukas AD, Volteas N, and Chan P, Superficial venous insufficiency: correlation of anatomic extent of reflux with clinical symptoms and signs. J Vasc Surg, 1994 20(6): p. 953– 8. 7990191
  6. [6]Beebe-Dimmer JL, Pfeifer JR, Engle JS, and Schottenfeld D, The epidemiology of chronic venous insufficiency and varicose veins. Ann Epidemiol, 2005 15(3): p. 175– 84. 15723761
  7. [7]Ruckley CV, Socioeconomic impact of chronic venous insufficiency and leg ulcers. Angiology, 1997 48(1): p. 67– 9. 8995346
  8. [8]Boersma D, Kornmann VN, van Eekeren RR, Tromp E, Unlu C, Reijnen MM, and de Vries JP, Treatment Modalities for Small Saphenous Vein Insufficiency: Systematic Review and Meta-analysis. J Endovasc Ther, 2016 23(1): p. 199– 211. 26564912
  9. [9]Rautio T, Ohinmaa A, Perala J, Ohtonen P, Heikkinen T, Wiik H, Karjalainen P, Haukipuro K, and Juvonen T, Endovenous obliteration versus conventional stripping operation in the treatment of primary varicose veins: a randomized controlled trial with comparison of the costs. J Vasc Surg, 2002 35(5): p. 958– 65. 12021712
  10. [10]Rosales A, Valve reconstructions. Phlebology, 2015 30(1 Suppl): p. 50– 8. 25729068
  11. [11]Beale RJ and Gough MJ, Treatment options for primary varicose veins--a review. Eur J Vasc Endovasc Surg, 2005 30(1): p. 83– 95. 15933989
  12. [12]Darwood RJ, Theivacumar N, Dellagrammaticas D, Mavor AI, and Gough MJ, Randomized clinical trial comparing endovenous laser ablation with surgery for the treatment of primary great saphenous varicose veins. Br J Surg, 2008 95(3): p. 294– 301. 18278775
  13. [13]Merchant RF, Pichot O, and Closure Study G, Long-term outcomes of endovenous radiofrequency obliteration of saphenous reflux as a treatment for superficial venous insufficiency. J Vasc Surg, 2005 42(3): p. 502– 9; discussion 509. 16171596
  14. [14]Raju S, Neglen P, Doolittle J, and Meydrech EF, Axillary vein transfer in trabeculated postthrombotic veins. J Vasc Surg, 1999 29(6): p. 1050– 62; discussion 1062–4. 10359939
  15. [15]Bry JD, Muto PA, O’Donnell TF, and Isaacson LA, The clinical and hemodynamic results after axillary-to-popliteal vein valve transplantation. J Vasc Surg, 1995 21(1): p. 110– 9. 7823349
  16. [16]Hillis LD, Smith PK, Anderson JL, Bittl JA, Bridges CR, Byrne JG, Cigarroa JE, DiSesa VJ, Hiratzka LF, Hutter AM Jr., Jessen ME, Keeley EC, Lahey SJ, Lange RA, London MJ, Mack MJ, Patel MR, Puskas JD, Sabik JF, Selnes O, Shahian DM, Trost JC, Winniford MD, Jacobs AK, Anderson JL, Albert N, Creager MA, Ettinger SM, Guyton RA, Halperin JL, Hochman JS, Kushner FG, Ohman EM, Stevenson W, Yancy CW, and American G College of Cardiology Foundation/American Heart Association Task Force on Practice, 2011 ACCF/AHA guideline for coronary artery bypass graft surgery: executive summary: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. J Thorac Cardiovasc Surg, 2012 143(1): p. 4– 34. 22172748
  17. [17]Dalsing MC, Lalka SG, Unthank JL, Grieshop RJ, Nixon C, and Davis T, Venous valvular insufficiency: influence of a single venous valve (native and experimental). J Vasc Surg, 1991 14(5): p. 576– 87. 1942365
  18. [18]Kehl D, Weber B, and Hoerstrup SP, Bioengineered living cardiac and venous valve replacements: current status and future prospects. Cardiovasc Pathol, 2016 25(4): p. 300– 305. 27167776
  19. [19]Neglen P and Raju S, Venous reflux repair with cryopreserved vein valves. J Vasc Surg, 2003 37(3): p. 552– 7. 12618691
  20. [20]Taheri SA and Schultz RO, Experimental prosthetic vein valve. Long-term results. Angiology, 1995 46(4): p. 299– 303. 7726449
  21. [21]Reeves TR, Cezeaux JL, Sackman JE, Cassada DC, Freeman MB, Stevens SL, and Goldman MH, Mechanical characteristics of lyophilized human saphenous vein valves. J Vasc Surg, 1997 26(5): p. 823– 8. 9372821
  22. [22]Kaya M, Grogan JB, Lentz D, Tew W, and Raju S, Glutaraldehyde-preserved venous valve transplantation in the dog. J Surg Res, 1988 45(3): p. 294– 7. 3411953
  23. [23]Hill R, Schmidt S, Evancho M, Hunter T, Hillegass D, and Sharp W, Development of a prosthetic venous valve. J Biomed Mater Res, 1985 19(7): p. 827– 32. 4077898
  24. [24]Elkins RC, Dawson PE, Goldstein S, Walsh SP, and Black KS, Decellularized human valve allografts. Ann Thorac Surg, 2001 71(5 Suppl): p. S428– 32. 11388241
  25. [25]Teebken OE, Puschmann C, Aper T, Haverich A, and Mertsching H, Tissue- engineered bioprosthetic venous valve: a long-term study in sheep. Eur J Vasc Endovasc Surg, 2003 25(4): p. 305– 12. 12651167
  26. [26]Gates KV, Pereira NL, and Griffiths LG, Cardiac Non-Human Leukocyte Antigen Identification: Techniques and Troubles. Front Immunol, 2017 8: p. 1332. 29093713 PMC5651233
  27. [27]Griffiths LG, Choe LH, Reardon KF, Dow SW, and Christopher Orton E, Immunoproteomic identification of bovine pericardium xenoantigens. Biomaterials, 2008 29(26): p. 3514– 20. 18514307 PMC2518324
  28. [30]Manji RA, Hara H, and Cooper DK, Characterization of the cellular infiltrate in bioprosthetic heart valves explanted from patients with structural valve deterioration. Xenotransplantation, 2015 22(5): p. 406– 7. 26315116
  29. [31]Gates KV, Xing Q, and Griffiths LG, Immunoproteomic Identification of Noncarbohydrate Antigens Eliciting Graft-Specific Adaptive Immune Responses in Patients with Bovine Pericardial Bioprosthetic Heart Valves. Proteomics Clin Appl, 2019 13(4): p. e1800129. 30548925 PMC6565515
  30. [32]Papalamprou A and Griffiths LG, Cardiac Extracellular Matrix Scaffold Generated Using Sarcomeric Disassembly and Antigen Removal. Annals of Biomedical Engineering, 2016 44(4): p. 1047– 1060. 26215309
  31. [33]Wong ML and Griffiths LG, Immunogenicity in xenogeneic scaffold generation: antigen removal vs. decellularization. Acta Biomater, 2014 10(5): p. 1806– 16. 24486910 PMC3976714
  32. [34]Nerem RM and Seliktar D, Vascular tissue engineering. Annu Rev Biomed Eng, 2001 3: p. 225– 43. 11447063
  33. [35]Mancuso L, Gualerzi A, Boschetti F, Loy F, and Cao G, Decellularized ovine arteries as small-diameter vascular grafts. Biomed Mater, 2014 9(4): p. 045011. 25050540
  34. [36]Boer U, Hurtado-Aguilar LG, Klingenberg M, Lau S, Jockenhoevel S, Haverich A, and Wilhelmi M, Effect of Intensified Decellularization of Equine Carotid Arteries on Scaffold Biomechanics and Cytotoxicity. Ann Biomed Eng, 2015 43(11): p. 2630– 41. 25921001
  35. [37]Negishi J, Funamoto S, Kimura T, Nam K, Higami T, and Kishida A, Effect of treatment temperature on collagen structures of the decellularized carotid artery using high hydrostatic pressure. J Artif Organs, 2011 14(3): p. 223– 31. 21559816
  36. [38]Bertanha M, Moroz A, Jaldin RG, Silva RA, Rinaldi JC, Golim MA, Felisbino SL, Domingues MA, Sobreira ML, Reis PP, and Deffune E, Morphofunctional characterization of decellularized vena cava as tissue engineering scaffolds. Exp Cell Res, 2014 326(1): p. 103– 11. 24929113
  37. [39]Xiong Y, Chan WY, Chua AW, Feng J, Gopal P, Ong YS, and Song C, Decellularized porcine saphenous artery for small-diameter tissue-engineered conduit graft. Artif Organs, 2013 37(6): p. E74– 87. 23566255
  38. [40]Campbell EM, Cahill PA, and Lally C, Investigation of a small-diameter decellularised artery as a potential scaffold for vascular tissue engineering; biomechanical evaluation and preliminary cell seeding. J Mech Behav Biomed Mater, 2012 14: p. 130– 42. 23026691
  39. [41]Pellegata AF, Asnaghi MA, Stefani I, Maestroni A, Maestroni S, Dominioni T, Zonta S, Zerbini G, and Mantero S, Detergent-enzymatic decellularization of swine blood vessels: insight on mechanical properties for vascular tissue engineering. Biomed Res Int, 2013 2013: p. 918753. 23865072 PMC3705825
  40. [42]Crapo PM, Gilbert TW, and Badylak SF, An overview of tissue and whole organ decellularization processes. Biomaterials, 2011 32(12): p. 3233– 43. 21296410 PMC3084613
  41. [45]Papalamprou A and Griffiths LG, Cardiac Extracellular Matrix Scaffold Generated Using Sarcomeric Disassembly and Antigen Removal. Ann Biomed Eng, 2016 44(4): p. 1047– 60. 26215309
  42. [46]Wong ML, Leach JK, Athanasiou KA, and Griffiths LG, The role of protein solubilization in antigen removal from xenogeneic tissue for heart valve tissue engineering. Biomaterials, 2011 32(32): p. 8129– 38. 21810537
  43. [47]Perla-Kajan J, Gryszczynska A, Mielcarek S, and Jakubowski H, Cation exchange HPLC analysis of desmosines in elastin hydrolysates. Anal Bioanal Chem, 2011 401(8): p. 2473– 9. 21887606 PMC3184222
  44. [48]Hara S, Yamaguchi M, Takemori Y, Furuhata K, Ogura H, and Nakamura M, Determination of mono-O-acetylated N-acetylneuraminic acids in human and rat sera by fluorometric high-performance liquid chromatography. Anal Biochem, 1989 179(1): p. 162– 6. 2757191
  45. [49]Badylak SF, The extracellular matrix as a scaffold for tissue reconstruction. Semin Cell Dev Biol, 2002 13(5): p. 377– 83. 12324220
  46. [50]Faulk DM, Johnson SA, Zhang L, and Badylak SF, Role of the extracellular matrix in whole organ engineering. J Cell Physiol, 2014 229(8): p. 984– 9. 24347365
  47. [51]Badylak SF, Regenerative medicine and developmental biology: the role of the extracellular matrix. Anat Rec B New Anat, 2005 287(1): p. 36– 41. 16308858
  48. [53]Bonvillain RW, Danchuk S, Sullivan DE, Betancourt AM, Semon JA, Eagle ME, Mayeux JP, Gregory AN, Wang G, Townley IK, Borg ZD, Weiss DJ, and Bunnell BA, A nonhuman primate model of lung regeneration: detergent-mediated decellularization and initial in vitro recellularization with mesenchymal stem cells. Tissue Eng Part A, 2012 18(23–24): p. 2437– 52. 22764775 PMC3501118
  49. [54]Cebotari S, Tudorache I, Jaekel T, Hilfiker A, Dorfman S, Ternes W, Haverich A, and Lichtenberg A, Detergent decellularization of heart valves for tissue engineering: toxicological effects of residual detergents on human endothelial cells. Artif Organs, 2010 34(3): p. 206– 10. 20447045
  50. [55]Lichtenberg A, Tudorache I, Cebotari S, Ringes-Lichtenberg S, Sturz G, Hoeffler K, Hurscheler C, Brandes G, Hilfiker A, and Haverich A, In vitro re-endothelialization of detergent decellularized heart valves under simulated physiological dynamic conditions. Biomaterials, 2006 27(23): p. 4221– 9. 16620956
  51. [56]Wallis JM, Borg ZD, Daly AB, Deng B, Ballif BA, Allen GB, Jaworski DM, and Weiss DJ, Comparative assessment of detergent-based protocols for mouse lung de- cellularization and re-cellularization. Tissue Eng Part C Methods, 2012 18(6): p. 420– 32. 22165818 PMC3358122
  52. [57]Youngstrom DW, Barrett JG, Jose RR, and Kaplan DL, Functional characterization of detergent-decellularized equine tendon extracellular matrix for tissue engineering applications. PLoS One, 2013 8(5): p. e64151. 23724028 PMC3664617
  53. [59]Korossis SA, Booth C, Wilcox HE, Watterson KG, Kearney JN, Fisher J, and Ingham E, Tissue engineering of cardiac valve prostheses II: biomechanical characterization of decellularized porcine aortic heart valves. J Heart Valve Dis, 2002 11(4): p. 463– 71. 12150291
  54. [60]Ott HC, Matthiesen TS, Goh SK, Black LD, Kren SM, Netoff TI, and Taylor DA, Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart. Nat Med, 2008 14(2): p. 213– 21. 18193059
  55. [61]Petersen TH, Calle EA, Colehour MB, and Niklason LE, Matrix composition and mechanics of decellularized lung scaffolds. Cells Tissues Organs, 2012 195(3): p. 222– 31. 21502745 PMC3696368
  56. [62]Schaner PJ, Martin ND, Tulenko TN, Shapiro IM, Tarola NA, Leichter RF, Carabasi RA, and Dimuzio PJ, Decellularized vein as a potential scaffold for vascular tissue engineering. J Vasc Surg, 2004 40(1): p. 146– 53. 15218475
  57. [63]Uygun BE, Soto-Gutierrez A, Yagi H, Izamis ML, Guzzardi MA, Shulman C, Milwid J, Kobayashi N, Tilles A, Berthiaume F, Hertl M, Nahmias Y, Yarmush ML, and Uygun K, Organ reengineering through development of a transplantable recellularized liver graft using decellularized liver matrix. Nat Med, 2010 16(7): p. 814– 20. 20543851 PMC2930603
  58. [64]Zou Y and Zhang Y, Mechanical evaluation of decellularized porcine thoracic aorta. J Surg Res, 2012 175(2): p. 359– 68. 21571306 PMC3100660
  59. [65]Gratzer PF, Harrison RD, and Woods T, Matrix alteration and not residual sodium dodecyl sulfate cytotoxicity affects the cellular repopulation of a decellularized matrix. Tissue Eng, 2006 12(10): p. 2975– 83. 17518665
  60. [66]Faulk DM, Wildemann JD, and Badylak SF, Decellularization and cell seeding of whole liver biologic scaffolds composed of extracellular matrix. J Clin Exp Hepatol, 2015 5(1): p. 69– 80. 25941434 PMC4415199
  61. [67]Badylak SF, The extracellular matrix as a biologic scaffold material. Biomaterials, 2007 28(25): p. 3587– 93. 17524477
  62. [68]Seddon AM, Curnow P, and Booth PJ, Membrane proteins, lipids and detergents: not just a soap opera. Biochim Biophys Acta, 2004 1666(1–2): p. 105– 17. 15519311
  63. [69]Faulk DM, Carruthers CA, Warner HJ, Kramer CR, Reing JE, Zhang L, D’Amore A, and Badylak SF, The effect of detergents on the basement membrane complex of a biologic scaffold material. Acta Biomater, 2014 10(1): p. 183– 93. 24055455 PMC3857635
  64. [70]Hwang J, San BH, Turner NJ, White LJ, Faulk DM, Badylak SF, Li Y, and Yu SM, Molecular assessment of collagen denaturation in decellularized tissues using a collagen hybridizing peptide. Acta Biomater, 2017 53: p. 268– 278. 28161576 PMC5462463
  65. [71]Rabilloud T, Gianazza E, Catto N, and Righetti PG, Amidosulfobetaines, a family of detergents with improved solubilization properties: application for isoelectric focusing under denaturing conditions. Anal Biochem, 1990 185(1): p. 94– 102. 2344051
  66. [72]Rabilloud T, Solubilization of proteins in 2DE: an outline. Methods Mol Biol, 2009 519: p. 19– 30. 19381574
  67. [74]Gerhard Meisenberg WHS, The Extracellular matrix, in Principles of Medical Biochemistry. 2017, Elsevier, Inc.: Philadelphia.
  68. [75]Ferdous Z and Grande-Allen KJ, Utility and control of proteoglycans in tissue engineering. Tissue Eng, 2007 13(8): p. 1893– 904. 17518731
  69. [77]Rapraeger AC, The coordinated regulation of heparan sulfate, syndecans and cell behavior. Curr Opin Cell Biol, 1993 5(5): p. 844– 53. 8240828
  70. [78]Elfenbein A and Simons M, Auxiliary and autonomous proteoglycan signaling networks. Methods Enzymol, 2010 480: p. 3– 31. 20816202 PMC3741665
  71. [79]Joyce EM, Liao J, Schoen FJ, Mayer JE Jr., and Sacks MS, Functional collagen fiber architecture of the pulmonary heart valve cusp. Ann Thorac Surg, 2009 87(4): p. 1240– 9. 19324159 PMC2878658
  72. [80]Balguid A, Rubbens MP, Mol A, Bank RA, Bogers AJ, van Kats JP, de Mol BA, Baaijens FP, and Bouten CV, The role of collagen cross-links in biomechanical behavior of human aortic heart valve leaflets--relevance for tissue engineering. Tissue Eng, 2007 13(7): p. 1501– 11. 17518750
  73. [81]Pocock ES, Alsaigh T, Mazor R, and Schmid-Schonbein GW, Cellular and molecular basis of Venous insufficiency. Vasc Cell, 2014 6(1): p. 24. 25520775 PMC4268799
  74. [82]Licup AJ, Munster S, Sharma A, Sheinman M, Jawerth LM, Fabry B, Weitz DA, and MacKintosh FC, Stress controls the mechanics of collagen networks. Proc Natl Acad Sci U S A, 2015 112(31): p. 9573– 8. 26195769 PMC4534289
  75. [83]Allman AJ, McPherson TB, Badylak SF, Merrill LC, Kallakury B, Sheehan C, Raeder RH, and Metzger DW, Xenogeneic extracellular matrix grafts elicit a TH2-restricted immune response. Transplantation, 2001 71(11): p. 1631– 40. 11435976
  76. [84]Badylak SF, Decellularized allogeneic and xenogeneic tissue as a bioscaffold for regenerative medicine: factors that influence the host response. Ann Biomed Eng, 2014 42(7): p. 1517– 27. 24402648
  77. [85]Badylak SF, Xenogeneic extracellular matrix as a scaffold for tissue reconstruction. Transpl Immunol, 2004 12(3–4): p. 367– 77. 15157928
  78. [86]Badylak SF and Gilbert TW, Immune response to biologic scaffold materials. Semin Immunol, 2008 20(2): p. 109– 16. 18083531 PMC2605275
  79. [87]Rieder E, Steinacher-Nigisch A, and Weigel G, Human immune-cell response towards diverse xenogeneic and allogeneic decellularized biomaterials. Int J Surg, 2016 36(Pt A): p. 347– 351. 27362520
  80. [88]Ruffer A, Purbojo A, Cicha I, Glockler M, Potapov S, Dittrich S, and Cesnjevar RA, Early failure of xenogenous de-cellularised pulmonary valve conduits--a word of caution! Eur J Cardiothorac Surg, 2010 38(1): p. 78– 85. 20219384
  81. [89]Simon P, Kasimir MT, Seebacher G, Weigel G, Ullrich R, Salzer-Muhar U, Rieder E, and Wolner E, Early failure of the tissue engineered porcine heart valve SYNERGRAFT in pediatric patients. Eur J Cardiothorac Surg, 2003 23(6): p. 1002– 6; discussion 1006. 12829079
  82. [90]Van Nooten G, Somers P, Cornelissen M, Bouchez S, Gasthuys F, Cox E, Sparks L, and Narine K, Acellular porcine and kangaroo aortic valve scaffolds show more intense immune-mediated calcification than cross-linked Toronto SPV valves in the sheep model. Interact Cardiovasc Thorac Surg, 2006 5(5): p. 544– 9. 17670642
  83. [91]Rieder E, Seebacher G, Kasimir MT, Eichmair E, Winter B, Dekan B, Wolner E, Simon P, and Weigel G, Tissue engineering of heart valves: decellularized porcine and human valve scaffolds differ importantly in residual potential to attract monocytic cells. Circulation, 2005 111(21): p. 2792– 7. 15911701
  84. [92]Bailey MT, Pillarisetti S, Xiao H, and Vyavahare NR, Role of elastin in pathologic calcification of xenograft heart valves. J Biomed Mater Res A, 2003 66(1): p. 93– 102. 12833435
  85. [93]Janeway CA Jr, Travers P, Walport M, and Shlomchik MJ, Macrophage activation by armed CD4 TH1 cells, in Immunobiology: The Immune System in Health and Disease. 5th edition 2001, Garland Science.
  86. [94]Melamed D, Messika O, Glass-Marmor L, and Miller A, Modulation of matrix metalloproteinase-9 (MMP-9) secretion in B lymphopoiesis. Int Immunol, 2006 18(9): p. 1355– 62. 16844724
  87. [95]Elkington PT, Green JA, and Friedland JS, Analysis of matrix metalloproteinase secretion by macrophages. Methods Mol Biol, 2009 531: p. 253– 65. 19347322
  88. [96]Papalamprou A, Chang CW, Vapniarsky N, Clark A, Walker N, and Griffiths LG, Xenogeneic cardiac extracellular matrix scaffolds with or without seeded mesenchymal stem cells exhibit distinct in vivo immunosuppressive and regenerative properties. Acta Biomater, 2016 45: p. 155– 168. 27445086
  89. [97]Jorge-Herrero E, Fernandez P, Gutierrez M, and Castillo-Olivares JL, Study of the calcification of bovine pericardium: analysis of the implication of lipids and proteoglycans. Biomaterials, 1991 12(7): p. 683– 9. 1742413
  90. [98]Pathak CP, Adams AK, Simpson T, Phillips RE Jr., and Moore MA, Treatment of bioprosthetic heart valve tissue with long chain alcohol solution to lower calcification potential. J Biomed Mater Res A, 2004 69(1): p. 140– 4. 14999761
  91. [99]Rossi MA, Braile DM, Teixeira MD, Souza DR, and Peres LC, Lipid extraction attenuates the calcific degeneration of bovine pericardium used in cardiac valve bioprostheses. J Exp Pathol (Oxford), 1990 71(2): p. 187– 96. 2331406 PMC1998711
  92. [100]Butany J, Collins MJ, Nair V, Leask RL, Scully HE, Williams WG, and David TE, Morphological findings in explanted Toronto stentless porcine valves. Cardiovasc Pathol, 2006 15(1): p. 41– 8. 16414456
  93. [101]Jorge-Herrero E, Fernandez P, de la Torre N, Escudero C, Garcia-Paez JM, Bujan J, and Castillo-Olivares JL, Inhibition of the calcification of porcine valve tissue by selective lipid removal. Biomaterials, 1994 15(10): p. 815– 20. 7986946

Cited by

Sorted by citations

Authors
Lopera Higuita, M., & Griffiths, L. G.
Affiliations
Mayo Clinic (US)
Corresponding author
Griffiths, Leigh G.
ORCID
Griffiths, Leigh G.
Venue
Acta Biomaterialia
Publisher
Elsevier BV
Published
2020-04
Volume
107
Pages
115-128
ISSN
1742-7061 (ISSN-L)
DOI
10.1016/j.actbio.2020.03.003
PMC
PMC7164717
OpenAlex
W3009078494
Cited by
35
References
6
Citations by year
2026: 4 · 2025: 4 · 2024: 5 · 2023: 6 · 2022: 5 · 2021: 11
FWCI
5.03
Type
journal article
Language
en
Open access
Licence
Locations
  • Acta Biomaterialia (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institutes of Health (R01HL121068)
Topics
  • Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
  • Physical Sciences › Materials Science › Biomaterials › Electrospun Nanofibers in Biomedical Applications
  • Physical Sciences › Materials Science › Biomaterials › Collagen: Extraction and Characterization
Keywords
antigen removal, venous valve function, chronic venous insufficiency, extracellular matrix scaffolds, collagen fibril structure, elastic lamina
MeSH terms
Animals, Antigens, Surface, Cattle, Collagen, Elastin, Extracellular Matrix, Chemical Fractionation, Humans, Rabbits, Saphenous Vein, Sodium Dodecyl Sulfate, Extracellular Matrix Proteins, Tissue Engineering, Tissue Scaffolds, Venous Valves

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