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Francis Swaby Markland, PhD

Title(s)Professor of Biochemistry & Molecular Medicine
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    Collapse Biography 
    Collapse Education and Training
    Penn State University, State College, PAB.S.06/1957Ag. Bio. Chem.
    Johns Hopkins University Medical School, Baltimore, MDPh.D.02/1964Physiological Chemistry
    Collapse Awards and Honors
    UCLA1968  - 1973NIH Career Development Award

    Collapse Overview 
    Collapse Overview
    DISINTEGRINS - EFFECTIVE INHIBITORS OF CANCER INVASION AND DISSEMINATION:
    We have been studying a peptide from southern copperhead snake venom that we call contortrostatin (CN). CN is a homodimer with two identical chains held together by two inter-chain disulfide bonds. The peptide possesses potent anti-tumor and anti-invasive activity. CN is a member of a family of peptides called disintegrins that are found in snake venoms. Many members of this family are distinguished by the presence of an amino acid sequence, arginine-glycine-aspartic acid (RGD), that enables them to bind to a subset of cell surface receptors called integrins found on cancer cells and newly growing (angiogenic) blood vessels supplying the tumor. Integrins mediate interactions between cells and their surroundings, and on cancer cells they play important roles in tumor invasion and dissemination. We postulated that since contortrostatin disrupts integrin interactions, it should block both cancer cell and newly growing blood vessel cell integrins and may, therefore, have significant anti-angiogenic and anti-metastatic activity. We have shown that CN acts as an effective inhibitor of breast cancer progression. Importantly, CN displays impressive inhibitory activity on the growth of new blood vessels into the breast cancer. But, there is a problem with CN and that is it is present in snake venom in very small quantities, making its translation to the clinic very difficult. However, we recently succeeded in producing a recombinant version of CN using an E. coli expression system. The recombinant protein is a monomer, called vicrostatin (VCN), purposefully designed with a slightly different amino acid sequence at its COOH-terminus to improve binding affinity to an important member of the integrin family. Using a delivery system in which VCN is encapsulated in unilamellar lipid particles (liposomes), we have shown that intravenous delivery of the liposomal formulation (LVCN) twice weekly in animal models of human, triple-negative, metastatic breast cancer, or human prostate cancer, leads to close to 80% inhibition of tumor growth and angiogenesis. More recently we have been examining the effect of VCN introduced intraperitoneally on the growth of human ovarian cancer cells in mice and have observed potent inhibition of tumor growth and dissemination. Presently we are studying human breast, prostate and ovarian cancer and glioma (a devastating brain tumor) animal models to demonstrate the anti-invasive and anti-tumor activities of VCN. We are also examining the mechanism by which VCN dramatically disrupts the actin cytoskeleton of cancer and angiogenic blood vessel cells leading to an abrupt halt to the locomotor apparatus of these cells. Finally, we are examining the diagnostic activity of VCN as an imaging agent to detect integrin positive cancer in prostate cancer mouse model studies, and then use VCN to treat the tumor.
    In separate studies we are examining another class of related proteins derived from members of the ADAM (A Disintegrin and Metalloproteinase domain) family. We are able to recombinantly produce large quantities of the disintegrin domain (DD) of the ADAM proteins using a highly engineered bacterial expression system. One of these ADAM DDs has interesting antitumor activity based on its interaction with integrins on the tumor cell surface. Since members of the ADAM family have different structures of their DDs, we are interested in characterizing the integrin binding specificities and affinities of these ADAM DDs and characterizing their biological activities with potential application to human cancer or other diseases.

    Collapse Research 
    Collapse Research Activities and Funding
    Development of a combination therapy for the treatment of prostate cancer
    NIH/NCI R41CA126001Aug 13, 2007 - Jul 31, 2009
    Role: Principal Investigator
    Liposomal Disintegrin: Novel and Effective Antitumor Agent Phase I
    NIH/NCI R41CA121452May 4, 2007 - Apr 30, 2009
    Role: Principal Investigator
    Antiidiotype mAb:an Antiangiogenic /Antimetastatic Agent
    NIH/NCI R41CA096368Mar 1, 2002 - Feb 28, 2004
    Role: Principal Investigator
    TREATMENT OF OVARIAN CANCER WITH CONTORTROSTATIN
    NIH/NCI R41CA089848Sep 11, 2001 - Aug 31, 2004
    Role: Principal Investigator
    THROMBOLYSIS BY RAPID DIRECT-ACTING FIBRINOLYTIC AGENTS
    NIH/NHLBI R01HL031389Jan 1, 1984 - Dec 31, 1987
    Role: Principal Investigator
    CHARACTERIZATION OF THE MAMMARY GLUCOCORTICOID RECEPTOR
    NIH/NCI R01CA022910Jan 1, 1979 - Dec 31, 1986
    Role: Principal Investigator

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    Collapse Required Scholarly Project Mentor

    Collapse Bibliographic 
    Collapse Publications
    Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Researchers can login to make corrections and additions, or contact us for help.
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    1. Swenson SD, Silva-Hirschberg C, Markland FS. Methods for Evaluation of a Snake Venom-Derived Disintegrin in Animal Models of Human Cancer. Methods Mol Biol. 2020; 2068:185-204. PMID: 31576529.
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    2. Swenson S, Minea RO, Tuan CD, Thein TZ, Chen TC, Markland FS. A Novel Venom-Derived Peptide for Brachytherapy of Glioblastoma: Preclinical Studies in Mice. Molecules. 2018 Nov 08; 23(11). PMID: 30413113.
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    3. Janib SM, Gustafson JA, Minea RO, Swenson SD, Liu S, Pastuszka MK, Lock LL, Cui H, Markland FS, Conti PS, Li Z, MacKay JA. Multimeric disintegrin protein polymer fusions that target tumor vasculature. Biomacromolecules. 2014 Jul 14; 15(7):2347-58. PMID: 24871936.
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    4. Levine M, Swenson S, McCormick T, Henderson SO, Thomas SH, Markland FS. Reversal of thienopyridine-induced platelet dysfunction following desmopressin administration. J Med Toxicol. 2013 Jun; 9(2):139-43. PMID: 23161280.
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    5. Lee JY, Markland FS, Lucchesi BR. Hirudin and s18886 maintain luminal patency after thrombolysis with alfimeprase. J Cardiovasc Pharmacol. 2013 Feb; 61(2):152-9. PMID: 23188127.
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    6. Markland FS, Swenson S. Snake venom metalloproteinases. Toxicon. 2013 Feb; 62:3-18. PMID: 23000249.
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    7. Hubbard S, Choudhary S, Maus E, Shukla D, Swenson S, Markland FS, Tiwari V. Contortrostatin, a homodimeric disintegrin isolated from snake venom inhibits herpes simplex virus entry and cell fusion. Antivir Ther. 2012; 17(7):1319-26. PMID: 22875654.
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    8. Minea R, Helchowski C, Rubino B, Brodmann K, Swenson S, Markland F. Development of a chimeric recombinant disintegrin as a cost-effective anti-cancer agent with promising translational potential. Toxicon. 2012 Mar 15; 59(4):472-86. PMID: 21354198.
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    9. Lin E, Wang Q, Swenson S, Jadvar H, Groshen S, Ye W, Markland FS, Pinski J. The disintegrin contortrostatin in combination with docetaxel is a potent inhibitor of prostate cancer in vitro and in vivo. Prostate. 2010 Sep 01; 70(12):1359-70. PMID: 20623636.
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    10. Minea RO, Helchowski CM, Zidovetzki SJ, Costa FK, Swenson SD, Markland FS. Vicrostatin - an anti-invasive multi-integrin targeting chimeric disintegrin with tumor anti-angiogenic and pro-apoptotic activities. PLoS One. 2010 Jun 03; 5(6):e10929. PMID: 20532165.
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    11. Markland FS, Swenson S. Fibrolase: trials and tribulations. Toxins (Basel). 2010 04; 2(4):793-808. PMID: 22069611.
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    12. Helchowski CM, Minea RO, Swenson SD, Markland FS. The use of pepsin in receptor internalization assays. Biochem Biophys Res Commun. 2009 Oct 16; 388(2):240-6. PMID: 19665997.
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    13. Moiseeva N, Bau R, Swenson SD, Markland FS, Choe JY, Liu ZJ, Allaire M. Structure of acostatin, a dimeric disintegrin from Southern copperhead (Agkistrodon contortrix contortrix), at 1.7 A resolution. Acta Crystallogr D Biol Crystallogr. 2008 Apr; 64(Pt 4):466-70. PMID: 18391413.
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    14. Swenson S, Ramu S, Markland FS. Anti-angiogenesis and RGD-containing snake venom disintegrins. Curr Pharm Des. 2007; 13(28):2860-71. PMID: 17979731.
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    15. Pyrko P, Wang W, Markland FS, Swenson SD, Schmitmeier S, Schönthal AH, Chen TC. The role of contortrostatin, a snake venom disintegrin, in the inhibition of tumor progression and prolongation of survival in a rodent glioma model. J Neurosurg. 2005 Sep; 103(3):526-37. PMID: 16235686.
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    16. Schmitmeier S, Markland FS, Schönthal AH, Chen TC. Potent mimicry of fibronectin-induced intracellular signaling in glioma cells by the homodimeric snake venom disintegrin contortrostatin. Neurosurgery. 2005 Jul; 57(1):141-53; discussion 141-53. PMID: 15987550.
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    17. Swenson S, Markland FS. Snake venom fibrin(ogen)olytic enzymes. Toxicon. 2005 Jun 15; 45(8):1021-39. PMID: 15882884.
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    18. Golubkov V, Garcia A, Markland FS. Action of fenretinide (4-HPR) on ovarian cancer and endothelial cells. Anticancer Res. 2005 Jan-Feb; 25(1A):249-53. PMID: 15816545.
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    19. Minea R, Swenson S, Costa F, Chen TC, Markland FS. Development of a novel recombinant disintegrin, contortrostatin, as an effective anti-tumor and anti-angiogenic agent. Pathophysiol Haemost Thromb. 2005; 34(4-5):177-83. PMID: 16707923.
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    20. Swenson S, Costa F, Ernst W, Fujii G, Markland FS. Contortrostatin, a snake venom disintegrin with anti-angiogenic and anti-tumor activity. Pathophysiol Haemost Thromb. 2005; 34(4-5):169-76. PMID: 16707922.
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    21. Swenson S, Toombs CF, Pena L, Johansson J, Markland FS. Alpha-fibrinogenases. Curr Drug Targets Cardiovasc Haematol Disord. 2004 Dec; 4(4):417-35. PMID: 15578961.
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    22. Swenson S, Costa F, Minea R, Sherwin RP, Ernst W, Fujii G, Yang D, Markland FS. Intravenous liposomal delivery of the snake venom disintegrin contortrostatin limits breast cancer progression. Mol Cancer Ther. 2004 Apr; 3(4):499-511. PMID: 15078994.
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    23. Schmitmeier S, Markland FS, Ritter MR, Sawcer DE, Chen TC. Functional effect of contortrostatin, a snake venom disintegrin, on human glioma cell invasion in vitro. Cell Commun Adhes. 2003 Jan-Feb; 10(1):1-16. PMID: 12881036.
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    24. Golubkov V, Hawes D, Markland FS. Anti-angiogenic activity of contortrostatin, a disintegrin from Agkistrodon contortrix contortrix snake venom. Angiogenesis. 2003; 6(3):213-24. PMID: 15041797.
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    25. Moiseeva N, Swenson SD, Markland FS, Bau R. Purification, crystallization and preliminary X-ray analysis of the disintegrin contortrostatin from Agkistrodon contortrix contortrix snake venom. Acta Crystallogr D Biol Crystallogr. 2002 Dec; 58(Pt 12):2122-4. PMID: 12454474.
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    26. de Carvalho DD, Schmitmeier S, Novello JC, Markland FS. Effect of BJcuL (a lectin from the venom of the snake Bothrops jararacussu) on adhesion and growth of tumor and endothelial cells. Toxicon. 2001 Oct; 39(10):1471-6. PMID: 11478954.
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    27. Markland FS, Shieh K, Zhou Q, Golubkov V, Sherwin RP, Richters V, Sposto R. A novel snake venom disintegrin that inhibits human ovarian cancer dissemination and angiogenesis in an orthotopic nude mouse model. Haemostasis. 2001 May-Dec; 31(3-6):183-91. PMID: 11910184.
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    28. Ritter MR, Markland FS. Differential regulation of tyrosine phosphorylation in tumor cells by contortrostatin, a homodimeric disintegrin, and monomeric disintegrins echistatin and flavoridin. Toxicon. 2001 Feb-Mar; 39(2-3):283-9. PMID: 10978746.
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    29. Ritter MR, Zhou Q, Markland FS. Contortrostatin, a homodimeric disintegrin, actively disrupts focal adhesion and cytoskeletal structure and inhibits cell motility through a novel mechanism. Cell Commun Adhes. 2001; 8(2):71-86. PMID: 11771727.
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    30. Bolger MB, Swenson S, Markland FS. Three-dimensional structure of fibrolase, the fibrinolytic enzyme from southern copperhead venom, modeled from the X-ray structure of adamalysin II and atrolysin C. AAPS PharmSci. 2001; 3(2):E16. PMID: 11741267.
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    31. Swenson S, Bush LR, Markland FS. Chimeric derivative of fibrolase, a fibrinolytic enzyme from southern copperhead venom, possesses inhibitory activity on platelet aggregation. Arch Biochem Biophys. 2000 Dec 15; 384(2):227-37. PMID: 11368309.
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    32. Schmitmeier S, Markland FS, Chen TC. Anti-invasive effect of contortrostatin, a snake venom disintegrin, and TNF-alpha on malignant glioma cells. Anticancer Res. 2000 Nov-Dec; 20(6B):4227-33. PMID: 11205252.
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    33. Estêvão-Costa MI, Diniz CR, Magalhães A, Markland FS, Sanchez EF. Action of metalloproteinases mutalysin I and II on several components of the hemostatic and fibrinolytic systems. Thromb Res. 2000 Aug 15; 99(4):363-76. PMID: 10963787.
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    34. Ritter MR, Markland FS. Contortrostatin activates ERK2 and tyrosine phosphorylation events via distinct pathways. Biochem Biophys Res Commun. 2000 Jul 21; 274(1):142-8. PMID: 10903909.
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    35. Ritter MR, Zhou Q, Markland FS. Contortrostatin, a snake venom disintegrin, induces alphavbeta3-mediated tyrosine phosphorylation of CAS and FAK in tumor cells. J Cell Biochem. 2000 Jul 19; 79(1):28-37. PMID: 10906753.
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    36. Zhou Q, Sherwin RP, Parrish C, Richters V, Groshen SG, Tsao-Wei D, Markland FS. Contortrostatin, a dimeric disintegrin from Agkistrodon contortrix contortrix, inhibits breast cancer progression. Breast Cancer Res Treat. 2000 Jun; 61(3):249-60. PMID: 10966001.
      View in: PubMed
    37. Zhou Q, Hu P, Ritter MR, Swenson SD, Argounova S, Epstein AL, Markland FS. Molecular cloning and functional expression of contortrostatin, a homodimeric disintegrin from southern copperhead snake venom. Arch Biochem Biophys. 2000 Mar 15; 375(2):278-88. PMID: 10700384.
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    38. Zhou Q, Nakada MT, Brooks PC, Swenson SD, Ritter MR, Argounova S, Arnold C, Markland FS. Contortrostatin, a homodimeric disintegrin, binds to integrin alphavbeta5. Biochem Biophys Res Commun. 2000 Jan 07; 267(1):350-5. PMID: 10623623.
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    39. Zhou Q, Nakada MT, Arnold C, Shieh KY, Markland FS. Contortrostatin, a dimeric disintegrin from Agkistrodon contortrix contortrix, inhibits angiogenesis. Angiogenesis. 1999; 3(3):259-69. PMID: 14517425.
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    40. Markland FS. Snake venoms and the hemostatic system. Toxicon. 1998 Dec; 36(12):1749-800. PMID: 9839663.
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    41. Mercer B, Markland F, Minkin C. Contortrostatin, a homodimeric snake venom disintegrin, is a potent inhibitor of osteoclast attachment. J Bone Miner Res. 1998 Mar; 13(3):409-14. PMID: 9525341.
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    42. Markland FS. Snake venom fibrinogenolytic and fibrinolytic enzymes: an updated inventory. Registry of Exogenous Hemostatic Factors of the Scientific and Standardization Committee of the International Society on Thrombosis and Haemostasis. Thromb Haemost. 1998 Mar; 79(3):668-74. PMID: 9531060.
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    43. Kamiguti AS, Markland FS, Zhou Q, Laing GD, Theakston RD, Zuzel M. Proteolytic cleavage of the beta1 subunit of platelet alpha2beta1 integrin by the metalloproteinase jararhagin compromises collagen-stimulated phosphorylation of pp72. J Biol Chem. 1997 Dec 19; 272(51):32599-605. PMID: 9405475.
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    44. Sanchez EF, Bush LR, Swenson S, Markland FS. Chimeric fibrolase: covalent attachment of an RGD-like peptide to create a potentially more effective thrombolytic agent. Thromb Res. 1997 Aug 01; 87(3):289-302. PMID: 9263396.
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    45. Markland FS. Snake venoms. Drugs. 1997; 54 Suppl 3:1-10. PMID: 9360847.
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    46. Markland FS. Fibrolase, an active thrombolytic enzyme in arterial and venous thrombosis model systems. Adv Exp Med Biol. 1996; 391:427-38. PMID: 8726081.
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    47. Loayza SL, Trikha M, Markland FS, Riquelme P, Kuo J. Resolution of isoforms of natural and recombinant fibrolase, the fibrinolytic enzyme from Agkistrodon contortrix contortrix snake venom, and comparison of their EDTA sensitivities. J Chromatogr B Biomed Appl. 1994 Dec 09; 662(2):227-43. PMID: 7719479.
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    48. Trikha M, Schmitmeier S, Markland FS. Purification and characterization of fibrolase isoforms from venom of individual southern copperhead (Agkistrodon contortrix Contortrix) snakes. Toxicon. 1994 Dec; 32(12):1521-31. PMID: 7725320.
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    49. Markland FS, Friedrichs GS, Pewitt SR, Lucchesi BR. Thrombolytic effects of recombinant fibrolase or APSAC in a canine model of carotid artery thrombosis. Circulation. 1994 Nov; 90(5):2448-56. PMID: 7955202.
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    50. Trikha M, De Clerck YA, Markland FS. Contortrostatin, a snake venom disintegrin, inhibits beta 1 integrin-mediated human metastatic melanoma cell adhesion and blocks experimental metastasis. Cancer Res. 1994 Sep 15; 54(18):4993-8. PMID: 7520832.
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    51. Clark EA, Trikha M, Markland FS, Brugge JS. Structurally distinct disintegrins contortrostatin and multisquamatin differentially regulate platelet tyrosine phosphorylation. J Biol Chem. 1994 Sep 02; 269(35):21940-3. PMID: 7520909.
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    52. Retzios AD, Markland FS. Fibrinolytic enzymes from the venoms of Agkistrodon contortrix contortrix and Crotalus basiliscus basiliscus: cleavage site specificity towards the alpha-chain of fibrin. Thromb Res. 1994 May 15; 74(4):355-67. PMID: 8085237.
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    53. Trikha M, Rote WE, Manley PJ, Lucchesi BR, Markland FS. Purification and characterization of platelet aggregation inhibitors from snake venoms. Thromb Res. 1994 Jan 01; 73(1):39-52. PMID: 8178312.
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    54. Retzios AD, Markland FS. Purification, characterization, and fibrinogen cleavage sites of three fibrinolytic enzymes from the venom of Crotalus basiliscus basiliscus. Biochemistry. 1992 May 19; 31(19):4547-57. PMID: 1581310.
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    55. Randolph A, Chamberlain SH, Chu HL, Retzios AD, Markland FS, Masiarz FR. Amino acid sequence of fibrolase, a direct-acting fibrinolytic enzyme from Agkistrodon contortrix contortrix venom. Protein Sci. 1992 May; 1(5):590-600. PMID: 1304358.
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    56. Takacs Z, Retzios AD, Markland FS. A hemorrhagic (basement membrane degrading) zinc metalloproteinase from southern copperhead venom. Matrix Suppl. 1992; 1:101-3. PMID: 1480009.
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    57. Guan AL, Retzios AD, Henderson GN, Markland FS. Purification and characterization of a fibrinolytic enzyme from venom of the southern copperhead snake (Agkistrodon contortrix contortrix). Arch Biochem Biophys. 1991 Sep; 289(2):197-207. PMID: 1898066.
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    58. Markland FS. Inventory of alpha- and beta-fibrinogenases from snake venoms. For the Subcommittee on Nomenclature of Exogenous Hemostatic Factors of the Scientific and Standardization Committee of the International Society on Thrombosis and Haemostasis. Thromb Haemost. 1991 Apr 08; 65(4):438-43. PMID: 2057928.
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    59. Chen HM, Guan AL, Markland FS. Immunological properties of the fibrinolytic enzyme (fibrolase) from southern copperhead (Agkistrodon contortrix contortrix) venom and its purification by immunoaffinity chromatography. Toxicon. 1991; 29(6):683-94. PMID: 1926169.
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    60. Retzios AD, Markland FS. HPLC-based two-step purification of fibrinolytic enzymes from the venom of Agkistrodon contortrix contortrix and Agkistrodon piscivorus conanti. Protein Expr Purif. 1990 Sep; 1(1):33-9. PMID: 2152182.
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    61. Ahmed NK, Tennant KD, Markland FS, Lacz JP. Biochemical characteristics of fibrolase, a fibrinolytic protease from snake venom. Haemostasis. 1990; 20(3):147-54. PMID: 1696922.
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    62. Hutchens TW, Hawkins EF, Markland FS. Glucocorticoid receptor from lactating goat mammary tissue comparison of native and activated forms in a cell free system. J Steroid Biochem. 1989 May; 32(5):651-68. PMID: 2739406.
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    63. Retzios AD, Markland FS. A direct-acting fibrinolytic enzyme from the venom of Agkistrodon contortrix contortrix: effects on various components of the human blood coagulation and fibrinolysis systems. Thromb Res. 1988 Dec 15; 52(6):541-52. PMID: 3232124.
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    64. Guan AL, Markland FS. Isoelectric focusing in immobilized pH gradients of a snake venom fibrinolytic enzyme. J Biochem Biophys Methods. 1988 Jun-Jul; 16(2-3):215-26. PMID: 3411084.
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    65. Egen NB, Russell FE, Sammons DW, Humphreys RC, Guan AL, Markland FS. Isolation by preparative isoelectric focusing of a direct acting fibrinolytic enzyme from the venom of Agkistrodon contortrix contortrix (southern copperhead). Toxicon. 1987; 25(11):1189-98. PMID: 2448917.
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    66. Markland FS. Antitumor action of crotalase, a defibrinogenating snake venom enzyme. Semin Thromb Hemost. 1986 Oct; 12(4):284-90. PMID: 3538422.
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    67. Markland FS, Perdon A. Comparison of two methods for proteolytic enzyme detection in snake venom. Toxicon. 1986; 24(4):385-93. PMID: 3087029.
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    68. Russell FE, Sullivan JB, Egen NB, Jeter WS, Markland FS, Wingert WA, Bar-Or D. Preparation of a new antivenin by affinity chromatography. Am J Trop Med Hyg. 1985 Jan; 34(1):141-50. PMID: 2578749.
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    69. Hutchens TW, Markland FS, Hawkins EF. RNA induced reversal of glucocorticoid receptor activation. Biochem Biophys Res Commun. 1982 Mar 15; 105(1):20-7. PMID: 6178401.
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    70. Markland FS, Kettner C, Schiffman S, Shaw E, Bajwa SS, Reddy KN, Kirakossian H, Patkos GB, Theodor I, Pirkle H. Kallikrein-like activity of crotalase, a snake venom enzyme that clots fibrinogen. Proc Natl Acad Sci U S A. 1982 Mar; 79(6):1688-92. PMID: 7043462.
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    71. Naritoku WY, Howard EB, Britt JO, Markland FS. Effect of molybdate on androgen receptor levels in canine prostate. Prostate. 1982; 3(6):611-4. PMID: 7155993.
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    72. Bajwa SS, Russell FE, Markland FS. Thrombolytic agents in snake venoms. Proc West Pharmacol Soc. 1982; 25:353-6. PMID: 7122520.
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    73. Bajwa SS, Kirakossian H, Reddy KN, Markland FS. Thrombin-like and fibrinolytic enzymes in the venoms from the Gaboon viper (Bitis gabonica), eastern cottonmouth moccasin (Agkistrodon p. piscivorus) and southern copperhead (Agkistrodon c. contortrix) snakes. Toxicon. 1982; 20(2):427-32. PMID: 7043785.
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    74. Hutchens TW, Markland FS, Hawkins EF. Physicochemical analysis of reversible molybdate effects on different molecular forms of glucocorticoid receptor. Biochem Biophys Res Commun. 1981 Nov 16; 103(1):60-7. PMID: 7317071.
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    75. Markland FS, Kettner C, Shaw E, Bajwa SS. The inhibition of crotalase, a thrombin-like snake venom enzyme, by several peptide chloromethyl ketone derivatives. Biochem Biophys Res Commun. 1981 Oct 30; 102(4):1302-9. PMID: 6797424.
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    76. Pirkle H, Markland FS, Theodor I, Baumgartner R, Bajwa SS, Kirakossian H. The primary structure of crotalase, a thrombin-like venom enzyme, exhibits closer homology to kallikrein than to other serine proteases. Biochem Biophys Res Commun. 1981 Mar 31; 99(2):715-21. PMID: 7016120.
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    77. Bajwa SS, Markland FS, Russell FE. Fibrinolytic and fibrinogen clotting enzymes present in the venoms of western diamondback rattlesnake, Crotalus atrox, eastern diamondback rattlesnake, Crotalus adamanteus, and southern Pacific rattlesnake, Crotalus viridis helleri. Toxicon. 1981; 19(1):53-9. PMID: 7222089.
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    78. Bajwa SS, Markland FS, Russell FE. Fibrinolytic enzyme(s) in western diamondback rattlesnake (Crotalus atrox) venom. Toxicon. 1980; 18(3):285-90. PMID: 7394818.
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    79. Bajwa SS, Markland FS. A new method for purification of the thrombin-like enzyme from the venom of the eastern diamondback rattlesnake. Thromb Res. 1979; 16(1-2):11-23. PMID: 505414.
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    80. Markland FS, Pirkle H. Thrombin-like enzyme from the venom of Crotalus adamanteus (eastern diamondback rattlesnake). Thromb Res. 1977 Mar; 10(3):487-94. PMID: 854881.
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    81. Bacharach AD, Markland FS, Pellino A, Weber BH. Modification of yeast 3-phosphoglycerate kinase: isolation and sequence determination of a nitrated active-site peptide and isolation of a carboxyl modified active-site peptide. Biochem Biophys Res Commun. 1977 Jan 10; 74(1):165-71. PMID: 319791.
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    82. Markland FS, Pirkle H. Characterization of a thrombin-like enzyme from Crotalus adamanteus (Eastern diamondback rattlesnake) [proceedings]. Toxicon. 1976; 14(6):412-3. PMID: 1014024.
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    83. Damus PS, Markland FS, Davidson TM, Shanley JD. A purified procoagulant enzyme from the venom of the eastern diamondback rattlesnake (Crotalus adamanteus): in vivo and in vitro studies. J Lab Clin Med. 1972 Jun; 79(6):906-23. PMID: 4623612.
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    84. Markland FS, Damus PS. Purification and properties of a thrombin-like enzyme from the venom of Crotalus adamanteus (Eastern diamondback rattlesnake). J Biol Chem. 1971 Nov; 246(21):6460-73. PMID: 5132665.
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