Samuel A. Santoro, M.D., Ph.D.

Faculty Appointments
Chair of the Department of Pathology, Microbiology and Immunology Professor of Pathology, Microbiology and Immunology Professor of BiochemistryDorothy Beryl and Theodore R. Austin Chair in Pathology
M.D., Medicine, Vanderbilt University, Nashville, TennesseePh.D., Biochemistry, Vanderbilt University, Nashville, TennesseeB.S., Chemistry, Emory University, Atlanta, Georgia
Office Address
C-3322 MCN
TN 2561
Research Description
The molecular mechanisms of cell-substrate adhesion and the biologic roles of cellular adhesion are the foci of our research program. Most of our studies are centered on the alpha 2/beta 1 integrin, a cell surface receptor for collagen that was originally identified and characterized in our laboratory. Current efforts are devoted to elucidation of the structural basis of ligand recognition by the integrin, the structural basis of integrin activation and the roles of the alpha 2/beta 1 and related integrins in complex biological processes such as differentiation, development, wound healing and repair, tumor cell invasion and metastasis, and hemostasis and thrombosis.

Ongoing projects include: 1) elucidation of the structural basis by which the integrin recognizes and binds both collagenous and noncollagenous ligands, 2) elucidation of the structural basis of integrin activation that permits higher affinity binding of some ligands or that is required for the binding of other ligands, 3) exploration of the role of altered integrin expression in the invasive and metastatic behavior of tumor cells, 4) definition of the structural and biologic basis of MMP-1 (matrix metalloproteinase-1) interactions with the integrin and the role of the interaction in regulating cell surface matrix metalloproteinase activity in wound repair and related events, 5) examination of the role of integrin-mediated cell-matrix interactions in the establishment and maintenance of the differentiated epithelial phenotype, and 6) and elucidation of the structural basis and pathbiologic function of the alpha 2/beta 1 integrin as a receptor for echoviruses and reoviruses. In addition, we continue to identify new ligands that implicate the alpha 2/beta 1 integrin in novel facets of biology and pathology.

Our studies combine the application of modern protein and peptide biochemistry, immunochemical and molecular genetic approaches (including knockout mice) to address the fundamental roles and mechanisms of cellular adhesion in complex cell biological processes. .
Research Keywords
Structure and biology of integrin adhesive receptors for extracellular matrix proteins
Wright S, Parham C, Lee B, Clarke D, Auckland L, Johnston J, Lawrence AL, Dickeson SK, Santoro SA, Griswold-Prenner I, Bix G. Perlecan domain V inhibits a2 integrin-mediated amyloid-ß neurotoxicity. Neurobiol. Aging [print-electronic]. 2012 Jul; 33(7): 1379-88. PMID: 21126803, PII: S0197-4580(10)00463-X, DOI: 10.1016/j.neurobiolaging.2010.10.018, ISSN: 1558-1497.

Marjoram RJ, Voss B, Pan Y, Dickeson SK, Zutter MM, Hamm HE, Santoro SA. Suboptimal activation of protease-activated receptors enhances alpha2beta1 integrin-mediated platelet adhesion to collagen. J. Biol. Chem [print-electronic]. 2009 Dec 12/11/2009; 284(50): 34640-7. PMID: 19815553, PMCID: PMC2787326, PII: M109.020990, DOI: 10.1074/jbc.M109.020990, ISSN: 1083-351X.

Zou Z, Schmaier AA, Cheng L, Mericko P, Dickeson SK, Stricker TP, Santoro SA, Kahn ML. Negative regulation of activated alpha-2 integrins during thrombopoiesis. Blood [print-electronic]. 2009 Jun 6/18/2009; 113(25): 6428-39. PMID: 19258597, PII: blood-2008-08-175356, DOI: 10.1182/blood-2008-08-175356, ISSN: 1528-0020.

Santoro SA, Mosse CA, Young PP. The MD/PhD pathway to a career in laboratory medicine. Clin. Lab. Med. 2007 Jun; 27(2): 425-34; abstract ix. PMID: 17556094, PII: S0272-2712(07)00028-5, DOI: 10.1016/j.cll.2007.03.012, ISSN: 0272-2712.

Grenache DG, Zhang Z, Wells LE, Santoro SA, Davidson JM, Zutter MM. Wound healing in the alpha2beta1 integrin-deficient mouse: altered keratinocyte biology and dysregulated matrix metalloproteinase expression. J. Invest. Dermatol [print-electronic]. 2007 Feb; 127(2): 455-66. PMID: 17068473, PII: 5700611, DOI: 10.1038/sj.jid.5700611, ISSN: 1523-1747.

Maginnis MS, Forrest JC, Kopecky-Bromberg SA, Dickeson SK, Santoro SA, Zutter MM, Nemerow GR, Bergelson JM, Dermody TS. Beta1 integrin mediates internalization of mammalian reovirus. J. Virol. 2006 Mar; 80(6): 2760-70. PMID: 16501085, PMCID: PMC1395463, PII: 80/6/2760, DOI: 10.1128/JVI.80.6.2760-2770.2006, ISSN: 0022-538X.

Edelson BT, Stricker TP, Li Z, Dickeson SK, Shepherd VL, Santoro SA, Zutter MM. Novel collectin/C1q receptor mediates mast cell activation and innate immunity. Blood [print-electronic]. 2006 Jan 1/1/2006; 107(1): 143-50. PMID: 16166590, PMCID: PMC1895357, PII: 2005-06-2218, DOI: 10.1182/blood-2005-06-2218, ISSN: 0006-4971.

Sarratt KL, Chen H, Zutter MM, Santoro SA, Hammer DA, Kahn ML. GPVI and alpha2beta1 play independent critical roles during platelet adhesion and aggregate formation to collagen under flow. Blood [print-electronic]. 2005 Aug 8/15/2005; 106(4): 1268-77. PMID: 15886326, PMCID: PMC1895202, PII: 2004-11-4434, DOI: 10.1182/blood-2004-11-4434, ISSN: 0006-4971.

Bix G, Fu J, Gonzalez EM, Macro L, Barker A, Campbell S, Zutter MM, Santoro SA, Kim JK, Höök M, Reed CC, Iozzo RV. Endorepellin causes endothelial cell disassembly of actin cytoskeleton and focal adhesions through alpha2beta1 integrin. J. Cell Biol. 2004 Jul 7/5/2004; 166(1): 97-109. PMID: 15240572, PMCID: PMC2172143, PII: jcb.200401150, DOI: 10.1083/jcb.200401150, ISSN: 0021-9525.

Wang H, Fu W, Im JH, Zhou Z, Santoro SA, Iyer V, DiPersio CM, Yu QC, Quaranta V, Al-Mehdi A, Muschel RJ. Tumor cell alpha3beta1 integrin and vascular laminin-5 mediate pulmonary arrest and metastasis. J. Cell Biol. 2004 Mar 3/15/2004; 164(6): 935-41. PMID: 15024036, PMCID: PMC2172296, PII: jcb.200309112, DOI: 10.1083/jcb.200309112, ISSN: 0021-9525.

He L, Pappan LK, Grenache DG, Li Z, Tollefsen DM, Santoro SA, Zutter MM. The contributions of the alpha 2 beta 1 integrin to vascular thrombosis in vivo. Blood [print-electronic]. 2003 Nov 11/15/2003; 102(10): 3652-7. PMID: 12893751, PII: 2003-04-1323, DOI: 10.1182/blood-2003-04-1323, ISSN: 0006-4971.

Grenache DG, Coleman T, Semenkovich CF, Santoro SA, Zutter MM. Alpha2beta1 integrin and development of atherosclerosis in a mouse model: assessment of risk. Arterioscler. Thromb. Vasc. Biol [print-electronic]. 2003 Nov 11/1/2003; 23(11): 2104-9. PMID: 14512368, PII: 01.ATV.0000097282.22923.EF, DOI: 10.1161/01.ATV.0000097282.22923.EF, ISSN: 1524-4636.

Chen J, Diacovo TG, Grenache DG, Santoro SA, Zutter MM. The alpha(2) integrin subunit-deficient mouse: a multifaceted phenotype including defects of branching morphogenesis and hemostasis. Am. J. Pathol. 2002 Jul; 161(1): 337-44. PMID: 12107118, PMCID: PMC1850700, PII: S0002-9440(10)64185-5, ISSN: 0002-9440.

Klekotka PA, Santoro SA, Ho A, Dowdy SF, Zutter MM. Mammary epithelial cell-cycle progression via the alpha(2)beta(1) integrin: unique and synergistic roles of the alpha(2) cytoplasmic domain. Am. J. Pathol. 2001 Sep; 159(3): 983-92. PMID: 11549591, PMCID: PMC1850465, PII: S0002-9440(10)61774-9, ISSN: 0002-9440.

Klekotka PA, Santoro SA, Wang H, Zutter MM. Specific residues within the alpha 2 integrin subunit cytoplasmic domain regulate migration and cell cycle progression via distinct MAPK pathways. J. Biol. Chem [print-electronic]. 2001 Aug 8/24/2001; 276(34): 32353-61. PMID: 11418614, PII: M101921200, DOI: 10.1074/jbc.M101921200, ISSN: 0021-9258.

Dumin JA, Dickeson SK, Stricker TP, Bhattacharyya-Pakrasi M, Roby JD, Santoro SA, Parks WC. Pro-collagenase-1 (matrix metalloproteinase-1) binds the alpha(2)beta(1) integrin upon release from keratinocytes migrating on type I collagen. J. Biol. Chem [print-electronic]. 2001 Aug 8/3/2001; 276(31): 29368-74. PMID: 11359786, PII: M104179200, DOI: 10.1074/jbc.M104179200, ISSN: 0021-9258.

Stricker TP, Dumin JA, Dickeson SK, Chung L, Nagase H, Parks WC, Santoro SA. Structural analysis of the alpha(2) integrin I domain/procollagenase-1 (matrix metalloproteinase-1) interaction. J. Biol. Chem [print-electronic]. 2001 Aug 8/3/2001; 276(31): 29375-81. PMID: 11359774, PII: M102217200, DOI: 10.1074/jbc.M102217200, ISSN: 0021-9258.

Ohman T, King SL, Krithivas A, Cunningham J, Dickeson SK, Santoro SA, Bergelson JM. Echoviruses 1 and 8 are closely related genetically, and bind to similar determinants within the VLA-2 I domain. Virus Res. 2001 Jul; 76(1): 1-8. PMID: 11376841, PII: S0168-1702(01)00226-X, ISSN: 0168-1702.

Klekotka PA, Santoro SA, Zutter MM. Alpha 2 integrin subunit cytoplasmic domain-dependent cellular migration requires p38 MAPK. J. Biol. Chem [print-electronic]. 2001 Mar 3/23/2001; 276(12): 9503-11. PMID: 11121402, PII: M006286200, DOI: 10.1074/jbc.M006286200, ISSN: 0021-9258.

Keene DR, San Antonio JD, Mayne R, McQuillan DJ, Sarris G, Santoro SA, Iozzo RV. Decorin binds near the C terminus of type I collagen. J. Biol. Chem. 2000 Jul 7/21/2000; 275(29): 21801-4. PMID: 10823816, PII: C000278200, DOI: 10.1074/jbc.C000278200, ISSN: 0021-9258.

Ding Q, Gladson CL, Guidry CR, Santoro SA, Dickeson SK, Shin JT, Thompson JA. Extracellular FGF-1 inhibits cytoskeletal organization and promotes fibroblast motility. Growth Factors. 2000; 18(2): 93-107. PMID: 11019781, ISSN: 0897-7194.

Wang H, Gai Q, Yang X, Li Z, Linders B, Santoro SA, Zutter MM. Role of the alpha1 and alpha2 integrin cytoplasmic domains in cell morphology, motility and responsiveness to stimulation by the protein kinase C pathway. Cell Adhes. Commun. 2000 Jan; 7(4): 281-97. PMID: 10714390, ISSN: 1061-5385.

Dickeson SK, Mathis NL, Rahman M, Bergelson JM, Santoro SA. Determinants of ligand binding specificity of the alpha(1)beta(1) and alpha(2)beta(1) integrins. J. Biol. Chem. 1999 Nov 11/5/1999; 274(45): 32182-91. PMID: 10542255, ISSN: 0021-9258.

Zutter MM, Santoro SA, Wu JE, Wakatsuki T, Dickeson SK, Elson EL. Collagen receptor control of epithelial morphogenesis and cell cycle progression. Am. J. Pathol. 1999 Sep; 155(3): 927-40. PMID: 10487850, PMCID: PMC1866884, PII: S0002-9440(10)65192-9, DOI: 10.1016/S0002-9440(10)65192-9, ISSN: 0002-9440.

Santoro SA. Platelet surface collagen receptor polymorphisms: variable receptor expression and thrombotic/hemorrhagic risk. Blood. 1999 Jun 6/1/1999; 93(11): 3575-7. PMID: 10339460, ISSN: 0006-4971.

Hamerski DA, Santoro SA. Integrins and the kidney: biology and pathobiology. Curr. Opin. Nephrol. Hypertens. 1999 Jan; 8(1): 9-14. PMID: 9914855, ISSN: 1062-4821.

Dickeson SK, Bhattacharyya-Pakrasi M, Mathis NL, Schlesinger PH, Santoro SA. Ligand binding results in divalent cation displacement from the alpha 2 beta 1 integrin I domain: evidence from terbium luminescence spectroscopy. Biochemistry. 1998 Aug 8/11/1998; 37(32): 11280-8. PMID: 9698375, PII: bi9727848, DOI: 10.1021/bi9727848, ISSN: 0006-2960.

Bhattacharyya-Pakrasi M, Dickeson SK, Santoro SA. Alpha2beta1 integrin recognition of the carboxyl-terminal propeptide of type I procollagen: integrin recognition and feed-back regulation of matrix biosynthesis are mediated by distinct sequences. Matrix Biol. 1998 Jul; 17(3): 223-32. PMID: 9707345, ISSN: 0945-053X.

Dickeson SK, Walsh JJ, Santoro SA. Binding of the alpha 2 integrin I domain to extracellular matrix ligands: structural and mechanistic differences between collagen and laminin binding. Cell Adhes. Commun. 1998 Jun; 5(4): 273-81. PMID: 9762468, ISSN: 1061-5385.

Dickeson SK, Santoro SA. Ligand recognition by the I domain-containing integrins. Cell. Mol. Life Sci. 1998 Jun; 54(6): 556-66. PMID: 9676575, ISSN: 1420-682X.

Sun H, Santoro SA, Zutter MM. Downstream events in mammary gland morphogenesis mediated by reexpression of the alpha2beta1 integrin: the role of the alpha6 and beta4 integrin subunits. Cancer Res. 1998 May 5/15/1998; 58(10): 2224-33. PMID: 9605770, ISSN: 0008-5472.

Zutter MM, Sun H, Santoro SA. Altered integrin expression and the malignant phenotype: the contribution of multiple integrated integrin receptors. J Mammary Gland Biol Neoplasia. 1998 Apr; 3(2): 191-200. PMID: 10819527, ISSN: 1083-3021.

Xu J, Zutter MM, Santoro SA, Clark RA. A three-dimensional collagen lattice activates NF-kappaB in human fibroblasts: role in integrin alpha2 gene expression and tissue remodeling. J. Cell Biol. 1998 Feb 2/9/1998; 140(3): 709-19. PMID: 9456329, PMCID: PMC2140166, ISSN: 0021-9525.

Zutter MM, Santoro SA. The ups and downs of alpha 2 beta 1-integrin expression: contributions to epithelial cell differentiation and the malignant phenotype. Curr. Top. Microbiol. Immunol. 1998; 231: 167-85. PMID: 9479866, ISSN: 0070-217X.

Staatz WD, Walsh JJ, Santoro SA. The alpha 2 beta 1 integrin binds to the CB4 peptide of the alpha 2(I) collagen chain. Biochem. Mol. Biol. Int. 1997 Jul; 42(3): 577-82. PMID: 9247715, ISSN: 1039-9712.

Despotis GJ, Ikonomakou S, Levine V, Joiner-Maier D, Santoro SA, Joist JH. Effects of platelets and white blood cells and antiplatelet agent C7E3 (Reopro) on a new test of PAF procoagulant activity of whole blood. Thromb. Res. 1997 May 5/1/1997; 86(3): 205-19. PMID: 9175242, PII: S0049384897000649, ISSN: 0049-3848.

Dieckgraefe BK, Weems DM, Santoro SA, Alpers DH. ERK and p38 MAP kinase pathways are mediators of intestinal epithelial wound-induced signal transduction. Biochem. Biophys. Res. Commun. 1997 Apr 4/17/1997; 233(2): 389-94. PMID: 9144545, PII: S0006-291X(97)96469-X, DOI: 10.1006/bbrc.1997.6469, ISSN: 0006-291X.

Windus DW, Santoro SA, Atkinson R, Royal HD. Effects of antiplatelet drugs on dialysis-associated platelet deposition in polytetrafluoroethylene grafts. Am. J. Kidney Dis. 1997 Apr; 29(4): 560-4. PMID: 9100045, PII: S0272-6386(97)90338-3, ISSN: 0272-6386.

Dickeson SK, Walsh JJ, Santoro SA. Contributions of the I and EF hand domains to the divalent cation-dependent collagen binding activity of the alpha2beta1 integrin. J. Biol. Chem. 1997 Mar 3/21/1997; 272(12): 7661-8. PMID: 9065422, ISSN: 0021-9258.

Despotis GJ, Joist JH, Goodnough LT, Santoro SA, Spitznagel E. Whole blood heparin concentration measurements by automated protamine titration agree with plasma anti-Xa measurements. J. Thorac. Cardiovasc. Surg. 1997 Mar; 113(3): 611-3. PMID: 9081112, PII: S0022-5223(97)70380-5, DOI: 10.1016/S0022-5223(97)70380-5, ISSN: 0022-5223.

Despotis GJ, Levine V, Joist H, Santoro SA, Mendeloff E. Multiple episodes of thrombosis with biventricular support devices with inadequate anticoagulation and evidence of accelerated intravascular coagulation. J. Thorac. Cardiovasc. Surg. 1997 Feb; 113(2): 419-22. PMID: 9040641, PII: S0022-5223(97)70344-1, DOI: 10.1016/S0022-5223(97)70344-1, ISSN: 0022-5223.

Despotis GJ, Joist JH, Hogue CW, Alsoufiev A, Joiner-Maier D, Santoro SA, Spitznagel E, Weitz JI, Goodnough LT. More effective suppression of hemostatic system activation in patients undergoing cardiac surgery by heparin dosing based on heparin blood concentrations rather than ACT. Thromb. Haemost. 1996 Dec; 76(6): 902-8. PMID: 8972009, ISSN: 0340-6245.

Despotis GJ, Levine V, Filos KS, Santoro SA, Joist JH, Spitznagel E, Goodnough LT. Evaluation of a new point-of-care test that measures PAF-mediated acceleration of coagulation in cardiac surgical patients. Anesthesiology. 1996 Dec; 85(6): 1311-23. PMID: 8968178, ISSN: 0003-3022.

Xu J, Zutter MM, Santoro SA, Clark RA. PDGF induction of alpha 2 integrin gene expression is mediated by protein kinase C-zeta. J. Cell Biol. 1996 Sep; 134(5): 1301-11. PMID: 8794869, PMCID: PMC2120983, ISSN: 0021-9525.

Despotis GJ, Alsoufiev A, Hogue CW, Zoys TN, Goodnough LT, Santoro SA, Kater KM, Barnes P, Lappas DG. Evaluation of complete blood count results from a new, on-site hemocytometer compared with a laboratory-based hemocytometer. Crit. Care Med. 1996 Jul; 24(7): 1163-7. PMID: 8674329, ISSN: 0090-3493.

Wu JE, Santoro SA. Differential expression of integrin alpha subunits supports distinct roles during lung branching morphogenesis. Dev. Dyn. 1996 Jun; 206(2): 169-81. PMID: 8725284, PII: 10.1002/(SICI)1097-0177(199606)206:2<169::AID-AJA6>3.0.CO;2-G, DOI: 10.1002/(SICI)1097-0177(199606)206:2<169::AID-AJA6>3.0.CO;2-G, ISSN: 1058-8388.

Windus DW, Atkinson R, Santoro S. The effects of hemodialysis on platelet activation with new and reprocessed regenerated cellulose dialyzers. Am. J. Kidney Dis. 1996 Mar; 27(3): 387-93. PMID: 8604708, PII: S0272-6386(96)90362-5, ISSN: 0272-6386.

Dieckgraefe BK, Santoro SA, Alpers DH. Immunolocalization of alpha-integrin subunits and extracellular matrix components during human colonic organogenesis. Gastroenterology. 1996 Jan; 110(1): 58-71. PMID: 8536889, PII: S0016508596000443, ISSN: 0016-5085.

Saelman EU, Keely PJ, Santoro SA. Loss of MDCK cell alpha 2 beta 1 integrin expression results in reduced cyst formation, failure of hepatocyte growth factor/scatter factor-induced branching morphogenesis, and increased apoptosis. J. Cell. Sci. 1995 Nov; 108 ( Pt 11): 3531-40. PMID: 8586664, ISSN: 0021-9533.

Despotis GJ, Hogue CW, Santoro SA, Joist JH, Barnes PW, Lappas DG. Effect of heparin on whole blood activated partial thromboplastin time using a portable, whole blood coagulation monitor. Crit. Care Med. 1995 Oct; 23(10): 1674-9. PMID: 7587232, ISSN: 0090-3493.

Windus DW, Santoro S, Royal HD. The effects of hemodialysis on platelet deposition in prosthetic graft fistulas. Am. J. Kidney Dis. 1995 Oct; 26(4): 614-21. PMID: 7573016, PII: 0272-6386(95)90598-7, ISSN: 0272-6386.

Santoro SA, Zutter MM. The alpha 2 beta 1 integrin: a collagen receptor on platelets and other cells. Thromb. Haemost. 1995 Sep; 74(3): 813-21. PMID: 8571303, ISSN: 0340-6245.

Zutter MM, Santoro SA, Staatz WD, Tsung YL. Re-expression of the alpha 2 beta 1 integrin abrogates the malignant phenotype of breast carcinoma cells. Proc. Natl. Acad. Sci. U.S.A. 1995 Aug 8/1/1995; 92(16): 7411-5. PMID: 7638207, PMCID: PMC41349, ISSN: 0027-8424.

Despotis GJ, Joist JH, Hogue CW, Alsoufiev A, Kater K, Goodnough LT, Santoro SA, Spitznagel E, Rosenblum M, Lappas DG. The impact of heparin concentration and activated clotting time monitoring on blood conservation. A prospective, randomized evaluation in patients undergoing cardiac operation. J. Thorac. Cardiovasc. Surg. 1995 Jul; 110(1): 46-54. PMID: 7609568, PII: S0022-5223(05)80008-X, DOI: 10.1016/S0022-5223(05)80008-X, ISSN: 0022-5223.

Keely PJ, Wu JE, Santoro SA. The spatial and temporal expression of the alpha 2 beta 1 integrin and its ligands, collagen I, collagen IV, and laminin, suggest important roles in mouse mammary morphogenesis. Differentiation. 1995 Jul; 59(1): 1-13. PMID: 7589890, PII: S0301-4681(09)60785-4, DOI: 10.1046/j.1432-0436.1995.5910001.x, ISSN: 0301-4681.

Keely PJ, Fong AM, Zutter MM, Santoro SA. Alteration of collagen-dependent adhesion, motility, and morphogenesis by the expression of antisense alpha 2 integrin mRNA in mammary cells. J. Cell. Sci. 1995 Feb; 108 ( Pt 2): 595-607. PMID: 7769004, ISSN: 0021-9533.

Despotis GJ, Joist JH, Joiner-Maier D, Alsoufiev AL, Triantafillou AN, Goodnough LT, Santoro SA, Lappas DG. Effect of aprotinin on activated clotting time, whole blood and plasma heparin measurements. Ann. Thorac. Surg. 1995 Jan; 59(1): 106-11. PMID: 7529483, PII: 0003-4975(94)00798-C, DOI: 10.1016/0003-4975(94)00798-C, ISSN: 0003-4975.

Despotis GJ, Summerfield AL, Joist JH, Goodnough LT, Santoro SA, Spitznagel E, Cox JL, Lappas DG. Comparison of activated coagulation time and whole blood heparin measurements with laboratory plasma anti-Xa heparin concentration in patients having cardiac operations. J. Thorac. Cardiovasc. Surg. 1994 Dec; 108(6): 1076-82. PMID: 7983877, PII: S0022522394001169, ISSN: 0022-5223.

Despotis GJ, Summerfield AL, Joist JH, Goodnough LT, Santoro SA, Zimmermann JJ, Lappas DG. In vitro reversal of heparin effect with heparinase: evaluation with whole blood prothrombin time and activated partial thromboplastin time in cardiac surgical patients. Anesth. Analg. 1994 Oct; 79(4): 670-4. PMID: 7943773, ISSN: 0003-2999.

Fong AM, Santoro SA. Transcriptional regulation of alpha IIb integrin gene expression during megakaryocytic differentiation of K562 cells. Role of a silencer element. J. Biol. Chem. 1994 Jul 7/15/1994; 269(28): 18441-7. PMID: 7518432, ISSN: 0021-9258.

Santoro SA. Antiphospholipid antibodies and thrombotic predisposition: underlying pathogenetic mechanisms [editorial]. Blood. 1994 May 5/1/1994; 83(9): 2389-91. PMID: 8167328, ISSN: 0006-4971.

Wu JE, Santoro SA. Complex patterns of expression suggest extensive roles for the alpha 2 beta 1 integrin in murine development. Dev. Dyn. 1994 Apr; 199(4): 292-314. PMID: 7521231, DOI: 10.1002/aja.1001990405, ISSN: 1058-8388.

Despotis GJ, Santoro SA, Spitznagel E, Kater KM, Barnes P, Cox JL, Lappas DG. On-site prothrombin time, activated partial thromboplastin time, and platelet count. A comparison between whole blood and laboratory assays with coagulation factor analysis in patients presenting for cardiac surgery. Anesthesiology. 1994 Feb; 80(2): 338-51. PMID: 8311316, ISSN: 0003-3022.

Zutter MM, Santoro SA, Painter AS, Tsung YL, Gafford A. The human alpha 2 integrin gene promoter. Identification of positive and negative regulatory elements important for cell-type and developmentally restricted gene expression. J. Biol. Chem. 1994 Jan 1/7/1994; 269(1): 463-9. PMID: 8276836, ISSN: 0021-9258.

Despotis GJ, Santoro SA, Spitznagel E, Kater KM, Cox JL, Barnes P, Lappas DG. Prospective evaluation and clinical utility of on-site monitoring of coagulation in patients undergoing cardiac operation. J. Thorac. Cardiovasc. Surg. 1994 Jan; 107(1): 271-9. PMID: 8283896, PII: S0022522394001996, ISSN: 0022-5223.

Santoro SA, Zutter MM, Wu JE, Staatz WD, Saelman EU, Keely PJ. Analysis of collagen receptors. Meth. Enzymol. 1994; 245: 147-83. PMID: 7760733, ISSN: 0076-6879.

Choi ET, Engel L, Callow AD, Sun S, Trachtenberg J, Santoro S, Ryan US. Inhibition of neointimal hyperplasia by blocking alpha V beta 3 integrin with a small peptide antagonist GpenGRGDSPCA. J. Vasc. Surg. 1994 Jan; 19(1): 125-34. PMID: 7508000, PII: S0741521494001989, ISSN: 0741-5214.

Zutter MM, Krigman HR, Santoro SA. Altered integrin expression in adenocarcinoma of the breast. Analysis by in situ hybridization. Am. J. Pathol. 1993 May; 142(5): 1439-48. PMID: 8388172, PMCID: PMC1886906, ISSN: 0002-9440.

Winters KJ, Walsh JJ, Rubin BG, Santoro SA. Platelet interactions with fibronectin: divalent cation-independent platelet adhesion to the gelatin-binding domain of fibronectin. Blood. 1993 Apr 4/1/1993; 81(7): 1778-86. PMID: 8461464, ISSN: 0006-4971.

Rubin BG, Santoro SA, Sicard GA. Platelet interactions with the vessel wall and prosthetic grafts. Ann Vasc Surg. 1993 Mar; 7(2): 200-7. PMID: 8518140, PII: S0890-5096(06)60592-X, DOI: 10.1007/BF02001017, ISSN: 0890-5096.

Zutter MM, Fong AM, Krigman HR, Santoro SA. Differential regulation of the alpha 2 beta 1 and alpha IIb beta 3 integrin genes during megakaryocytic differentiation of pluripotential K562 cells. J. Biol. Chem. 1992 Oct 10/5/1992; 267(28): 20233-8. PMID: 1400341, ISSN: 0021-9258.

Burger SR, Zutter MM, Sturgill-Koszycki S, Santoro SA. Induced cell surface expression of functional alpha 2 beta 1 integrin during megakaryocytic differentiation of K562 leukemic cells. Exp. Cell Res. 1992 Sep; 202(1): 28-35. PMID: 1511736, PII: 0014-4827(92)90400-3, ISSN: 0014-4827.

Rubin BG, McGraw DJ, Sicard GA, Santoro SA. New RGD analogue inhibits human platelet adhesion and aggregation and eliminates platelet deposition on canine vascular grafts. J. Vasc. Surg. 1992 Apr; 15(4): 683-91; discussion 691. PMID: 1560559, PII: 0741-5214(92)90016-2, ISSN: 0741-5214.

Hortin GL, Staatz WD, Santoro SA. Preparation of soluble peptide libraries: application to studies of platelet adhesion sequences. Biochem. Int. 1992 Mar; 26(4): 731-8. PMID: 1610377, ISSN: 0158-5231.

Pacifici R, Basilico C, Roman J, Zutter MM, Santoro SA, McCracken R. Collagen-induced release of interleukin 1 from human blood mononuclear cells. Potentiation by fibronectin binding to the alpha 5 beta 1 integrin. J. Clin. Invest. 1992 Jan; 89(1): 61-7. PMID: 1729281, PMCID: PMC442819, DOI: 10.1172/JCI115586, ISSN: 0021-9738.

Santoro SA, Walsh JJ, Staatz WD, Baranski KJ. Distinct determinants on collagen support alpha 2 beta 1 integrin-mediated platelet adhesion and platelet activation. Cell Regul. 1991 Nov; 2(11): 905-13. PMID: 1809397, PMCID: PMC361889, ISSN: 1044-2030.

Winters KJ, Santoro SA, Miletich JP, Eisenberg PR. Relative importance of thrombin compared with plasmin-mediated platelet activation in response to plasminogen activation with streptokinase. Circulation. 1991 Oct; 84(4): 1552-60. PMID: 1833087, ISSN: 0009-7322.

Staatz WD, Fok KF, Zutter MM, Adams SP, Rodriguez BA, Santoro SA. Identification of a tetrapeptide recognition sequence for the alpha 2 beta 1 integrin in collagen. J. Biol. Chem. 1991 Apr 4/25/1991; 266(12): 7363-7. PMID: 2019571, ISSN: 0021-9258.

Pacifici R, Carano A, Santoro SA, Rifas L, Jeffrey JJ, Malone JD, McCracken R, Avioli LV. Bone matrix constituents stimulate interleukin-1 release from human blood mononuclear cells. J. Clin. Invest. 1991 Jan; 87(1): 221-8. PMID: 1845868, PMCID: PMC295032, DOI: 10.1172/JCI114975, ISSN: 0021-9738.

Winters KJ, Eisenberg PR, Jaffe AS, Santoro SA. Dependence of plasmin-mediated degradation of platelet adhesive receptors on temperature and Ca2+. Blood. 1990 Oct 10/15/1990; 76(8): 1546-57. PMID: 2169924, ISSN: 0006-4971.

Zutter MM, Mazoujian G, Santoro SA. Decreased expression of integrin adhesive protein receptors in adenocarcinoma of the breast. Am. J. Pathol. 1990 Oct; 137(4): 863-70. PMID: 2221016, PMCID: PMC1877561, ISSN: 0002-9440.

Torr SR, Winters KJ, Santoro SA, Sobel BE. The nature of interactions between tissue-type plasminogen activator and platelets. Thromb. Res. 1990 Jul 7/15/1990; 59(2): 279-93. PMID: 2146766, ISSN: 0049-3848.

Zutter MM, Santoro SA. Widespread histologic distribution of the alpha 2 beta 1 integrin cell-surface collagen receptor. Am. J. Pathol. 1990 Jul; 137(1): 113-20. PMID: 2164774, PMCID: PMC1877693, ISSN: 0002-9440.

Love PE, Santoro SA. Antiphospholipid antibodies: anticardiolipin and the lupus anticoagulant in systemic lupus erythematosus (SLE) and in non-SLE disorders. Prevalence and clinical significance. Ann. Intern. Med. 1990 May 5/1/1990; 112(9): 682-98. PMID: 2110431, PII: S0022214302000896, ISSN: 0003-4819.

Staatz WD, Peters KJ, Santoro SA. Divalent cation-dependent structure in the platelet membrane glycoprotein Ia-IIa (VLA-2) complex. Biochem. Biophys. Res. Commun. 1990 Apr 4/16/1990; 168(1): 107-14. PMID: 2327992, PII: 0006-291X(90)91681-H, ISSN: 0006-291X.

Staatz WD, Walsh JJ, Pexton T, Santoro SA. The alpha 2 beta 1 integrin cell surface collagen receptor binds to the alpha 1 (I)-CB3 peptide of collagen. J. Biol. Chem. 1990 Mar 3/25/1990; 265(9): 4778-81. PMID: 2156854, ISSN: 0021-9258.

Hawrylowicz CM, Santoro SA, Platt FM, Unanue ER. Activated platelets express IL-1 activity. J. Immunol. 1989 Dec 12/15/1989; 143(12): 4015-8. PMID: 2592766, ISSN: 0022-1767.

McGoff MA, Allen BT, Der T, Sicard GA, Santoro SA. Mechanisms of vascular graft thrombosis: role of altered canine platelet sensitivity to thromboxane. Thromb. Res. 1989 Sep 9/15/1989; 55(6): 695-707. PMID: 2506670, ISSN: 0049-3848.

Staatz WD, Rajpara SM, Wayner EA, Carter WG, Santoro SA. The membrane glycoprotein Ia-IIa (VLA-2) complex mediates the Mg++-dependent adhesion of platelets to collagen. J. Cell Biol. 1989 May; 108(5): 1917-24. PMID: 2715183, PMCID: PMC2115564, ISSN: 0021-9525.

Santoro SA, Lawing WJ. Modulation of an RGDS binding site on the platelet membrane glycoprotein IIb-IIIa complex. Biochem. Biophys. Res. Commun. 1989 Apr 4/14/1989; 160(1): 189-95. PMID: 2712830, PII: 0006-291X(89)91639-2, ISSN: 0006-291X.

Santoro SA. Inhibition of platelet adhesion to fibronectin, fibrinogen, and von Willebrand factor substrates by complex gangliosides. Blood. 1989 Feb; 73(2): 484-9. PMID: 2783860, ISSN: 0006-4971.

Bourey RE, Santoro SA. Interactions of exercise, coagulation, platelets, and fibrinolysis--a brief review. Med Sci Sports Exerc. 1988 Oct; 20(5): 439-46. PMID: 3057308, ISSN: 0195-9131.

Santoro SA, Rajpara SM, Staatz WD, Woods VL. Isolation and characterization of a platelet surface collagen binding complex related to VLA-2. Biochem. Biophys. Res. Commun. 1988 May 5/31/1988; 153(1): 217-23. PMID: 2837201, PII: S0006-291X(88)81211-7, ISSN: 0006-291X.

Hortin GL, Tollefsen DM, Santoro SA. Assessment of interference by heparin cofactor II in the DuPont aca antithrombin-III assay. Am. J. Clin. Pathol. 1988 Apr; 89(4): 515-7. PMID: 3354504, ISSN: 0002-9173.

Santoro SA. Molecular basis of platelet adhesion to collagen. Prog. Clin. Biol. Res. 1988; 283: 291-314. PMID: 3062626, ISSN: 0361-7742.

Santoro SA. The dualistic mechanisms of platelet adhesion to von Willebrand factor substrates. Exp. Cell Res. 1987 Dec; 173(2): 413-24. PMID: 3500868, ISSN: 0014-4827.

Santoro SA. Thrombospondin and the adhesive behavior of platelets. Semin. Thromb. Hemost. 1987 Jul; 13(3): 290-7. PMID: 3686021, DOI: 10.1055/s-2007-1003504, ISSN: 0094-6176.

Santoro SA, Lawing WJ. Competition for related but nonidentical binding sites on the glycoprotein IIb-IIIa complex by peptides derived from platelet adhesive proteins. Cell. 1987 Mar 3/13/1987; 48(5): 867-73. PMID: 3493077, PII: 0092-8674(87)90083-3, ISSN: 0092-8674.

Santoro SA, Frazier WA. Isolation and characterization of thrombospondin. Meth. Enzymol. 1987; 144: 438-46. PMID: 3626880, PII: 0076-6879(87)44193-1, ISSN: 0076-6879.

Santoro SA. Identification of a 160,000 dalton platelet membrane protein that mediates the initial divalent cation-dependent adhesion of platelets to collagen. Cell. 1986 Sep 9/12/1986; 46(6): 913-20. PMID: 3757029, PII: 0092-8674(86)90073-5, ISSN: 0092-8674.

Santoro SA, Cowan JF. Thrombin enhanced adhesion of platelets to von Willebrand factor substrates. Thromb. Res. 1986 Jul 7/1/1986; 43(1): 57-72. PMID: 3014679, ISSN: 0049-3848.

Haverstick DM, Cowan JF, Yamada KM, Santoro SA. Inhibition of platelet adhesion to fibronectin, fibrinogen, and von Willebrand factor substrates by a synthetic tetrapeptide derived from the cell-binding domain of fibronectin. Blood. 1985 Oct; 66(4): 946-52. PMID: 3876125, ISSN: 0006-4971.

Galvin NJ, Dixit VM, O'Rourke KM, Santoro SA, Grant GA, Frazier WA. Mapping of epitopes for monoclonal antibodies against human platelet thrombospondin with electron microscopy and high sensitivity amino acid sequencing. J. Cell Biol. 1985 Oct; 101(4): 1434-41. PMID: 2413043, PMCID: PMC2113943, ISSN: 0021-9525.

Roberts DD, Haverstick DM, Dixit VM, Frazier WA, Santoro SA, Ginsburg V. The platelet glycoprotein thrombospondin binds specifically to sulfated glycolipids. J. Biol. Chem. 1985 Aug 8/5/1985; 260(16): 9405-11. PMID: 3926767, ISSN: 0021-9258.

Cornelison GS, Rollins A, Santoro SA. Duplicate coagulation assays warranted [letter]. Am. J. Clin. Pathol. 1985 Aug; 84(2): 261-2. PMID: 4025239, ISSN: 0002-9173.

Dixit VM, Haverstick DM, O'Rourke KM, Hennessy SW, Grant GA, Santoro SA, Frazier WA. Effects of anti-thrombospondin monoclonal antibodies on the agglutination of erythrocytes and fixed, activated platelets by purified thrombospondin. Biochemistry. 1985 Jul 7/30/1985; 24(16): 4270-5. PMID: 4052397, ISSN: 0006-2960.

Haverstick DM, Dixit VM, Grant GA, Frazier WA, Santoro SA. Characterization of the platelet agglutinating activity of thrombospondin. Biochemistry. 1985 Jun 6/18/1985; 24(13): 3128-34. PMID: 4027236, ISSN: 0006-2960.

Dixit VM, Haverstick DM, O'Rourke K, Hennessy SW, Broekelmann TJ, McDonald JA, Grant GA, Santoro SA, Frazier WA. Inhibition of platelet aggregation by a monoclonal antibody against human fibronectin. Proc. Natl. Acad. Sci. U.S.A. 1985 Jun; 82(11): 3844-8. PMID: 2582428, PMCID: PMC397884, ISSN: 0027-8424.

Dixit VM, Haverstick DM, O'Rourke KM, Hennessy SW, Grant GA, Santoro SA, Frazier WA. A monoclonal antibody against human thrombospondin inhibits platelet aggregation. Proc. Natl. Acad. Sci. U.S.A. 1985 May; 82(10): 3472-6. PMID: 2582413, PMCID: PMC397798, ISSN: 0027-8424.

Haverstick DM, Dixit VM, Grant GA, Frazier WA, Santoro SA. Localization of the hemagglutinating activity of platelet thrombospondin to a 140 000-dalton thermolytic fragment. Biochemistry. 1984 Nov 11/6/1984; 23(23): 5597-603. PMID: 6509039, ISSN: 0006-2960.

Dixit VM, Grant GA, Santoro SA, Frazier WA. Isolation and characterization of a heparin-binding domain from the amino terminus of platelet thrombospondin. J. Biol. Chem. 1984 Aug 8/25/1984; 259(16): 10100-5. PMID: 6236212, ISSN: 0021-9258.

Shafer KE, Santoro SA, Sobel BE, Jaffe AS. Monitoring activity of fibrinolytic agents. A therapeutic challenge. Am. J. Med. 1984 May; 76(5): 879-86. PMID: 6232847, PII: 0002-9343(84)91003-9, ISSN: 0002-9343.

Dixit VM, Grant GA, Frazier WA, Santoro SA. Isolation of the fibrinogen-binding region of platelet thrombospondin. Biochem. Biophys. Res. Commun. 1984 Mar 3/30/1984; 119(3): 1075-81. PMID: 6712666, PII: 0006-291X(84)90884-2, ISSN: 0006-291X.

Santoro SA, Cowan JF. Mechanism of inhibition by trinitrophenylation of the ristocetin cofactor activity of von Willebrand factor. Biochim. Biophys. Acta. 1984 Feb 2/14/1984; 797(2): 178-85. PMID: 6607747, ISSN: 0006-3002.

Santoro SA. Inhibition of platelet aggregation by fibronectin. Biochem. Biophys. Res. Commun. 1983 Oct 10/14/1983; 116(1): 135-40. PMID: 6416252, PII: 0006-291X(83)90391-1, ISSN: 0006-291X.

Santoro SA. Differential effects of concanavalin A and succinyl concanavalin A on the macromolecular events of platelet activation. Biochim. Biophys. Acta. 1983 May 5/4/1983; 757(1): 101-10. PMID: 6682338, ISSN: 0006-3002.

Santoro SA. Preferential binding of high molecular weight forms of von Willebrand factor to fibrillar collagen. Biochim. Biophys. Acta. 1983 Mar 3/15/1983; 756(1): 123-6. PMID: 6402037, ISSN: 0006-3002.

Santoro SA. Amino group modification inhibits ristocetin cofactor activity of human von Willebrand factor. Biochem. Biophys. Res. Commun. 1982 Sep 9/30/1982; 108(2): 479-85. PMID: 6983351, PII: 0006-291X(82)90854-3, ISSN: 0006-291X.

Santoro SA, Cunningham LW. Platelet-collagen adhesion. Meth. Enzymol. 1982; 82 Pt A: 509-13. PMID: 7078447, ISSN: 0076-6879.

Santoro SA, Cowan JF. Adsorption of von Willebrand factor by fibrillar collagen--implications concerning the adhesion of platelets to collagen. Coll. Relat. Res. 1982 Jan; 2(1): 31-43. PMID: 6809414, ISSN: 0174-173X.

Santoro SA, Cunningham LW. Platelet-collagen adhesion-membrane fluidity and the development of high affinity adhesion through multiple interacting sites. Coll. Relat. Res. 1981 Nov; 1(6): 517-26. PMID: 7346233, ISSN: 0174-173X.

Santoro SA. Adsorption of von Willebrand factor/factor VIII by the genetically distinct interstitial collagens. Thromb. Res. 1981 Mar 3/15/1981; 21(6): 689-91. PMID: 6791300, ISSN: 0049-3848.

Santoro SA, Cunningham LW. Collagen-mediated platelet aggregation: the role of multiple interactions between the platelet surface and collagen. Thromb. Haemost. 1980 Jun 6/18/1980; 43(2): 158-62. PMID: 6779394, ISSN: 0340-6245.

Santoro SA, Cunningham LW. Fibronectin and the multiple interaction model for platelet-collagen adhesion. Proc. Natl. Acad. Sci. U.S.A. 1979 Jun; 76(6): 2644-8. PMID: 288053, PMCID: PMC383664, ISSN: 0027-8424.

Cunningham LW, Santoro S, Davies H. Primary hemostasis (collagen-platelet interaction): introduction. Suppl Thromb Haemost. 1978; 63: 205-13. PMID: 262324, ISSN: 0344-7618.

Santoro SA, Cunningham LW. Collagen-mediated platelet aggregation. Evidence for multivalent interactions of intermediate specificity between collagen and platelets. J. Clin. Invest. 1977 Nov; 60(5): 1054-60. PMID: 198432, PMCID: PMC372457, DOI: 10.1172/JCI108856, ISSN: 0021-9738.