Mary M. Zutter, M.D.

Professor

mary.zutter@vanderbilt.edu
Faculty Appointments
Assistant Vice-Chancellor for Integrative Diagnostics at Vanderbilt University Medical Center Professor of Pathology, Microbiology and Immunology Louise B. McGavock ChairProfessor of Cancer Biology
Education
M.D., Medicine, Tulane University, New Orleans, LouisianaB.S., Biochemistry, Newcomb College of Tulane University, New Orleans, Louisiana
Office Address
T 3218A MCN (2561)
Nashville, TN 2651
Research Description
Cancer progression involves fundamental alterations of cell-cell and cell-matrix interactions and the cues derived from them that contribute to the invasive and metastatic phenotype. As important mediators of cell adhesive behavior, integrins play a critical role in tumor progression and metastasis. Their role in mediating adhesion to either components of the extracellular matrix or to other cells is now well established.

Our laboratory focuses on the molecular basis of cell adhesion to collagen with a focus on the α2β1 integrin. The α2β1 integrin, a receptor for collagens, laminins, decorin, E-cadherin, as well as other ligands, has been implicated in normal developmental, inflammatory, and oncogenic processes. We use cell and molecular biology, mouse models of cancer, and organotypic model systems to address questions in cancer biology, immunology, and hemostasis.

1. The α2β1 integrin: a regulator of breast cancer metastasis.

The α2β1 integrin is expressed at high levels by most normal epithelial cells. In many epithelial malignancies α2β1 integrin expression is diminished or lost in a manner that correlates with the loss of epithelial differentiation and tumor progression. To characterize the role of the α2β1 integrin in tumor biology we utilized genetically engineered mice (GEM) in which expression of the α2β1 integrin is completely eliminated. Early studies provided the initial correlative suggestion that loss of α2β1 integrin expression might play an important role in cancer progression. Alternatively, loss of α2β1 integrin expression may simply be a consequence of malignant progression. In other studies, however, using cell lines either in vivo or in vitro suggest that the α2β1 integrin may serve to enhance metastasis to different organs.
The results of in vitro and in vivo studies of various designs may be subject to conflicting interpretation. Therefore, we have explored the role of the α2β1 integrin in cancer initiation and progression using a clinically-relevant, spontaneous mouse model, the MMTV-Neu model of breast cancer progression and metastasis. Furthermore, we have validated and extended the conclusions of our model system with a detailed analysis of α2 integrin gene expression and its significance in human breast and prostate cancer. We demonstrate that the α2β1 integrin is a metastasis suppressor of breast cancer and we identify key mechanistic steps in the metastatic cascade enhanced by loss of α2β1 integrin expression.
Although, the contribution of α2β1 integrin expression to metastasis suppression is clear, these data raise important questions which are the focus of ongoing work in the laboratory to dissect the molecular mechanisms by which α2β1 integrin suppresses the metastatic phenotype. Studies are ongoing to define the role of the integrin expression or lack thereof on the tumor cells alone, on cells within the host microenvironment alone, or the contribution on both the tumor cells and within the host microenvironment in tumor metastasis.

2. The α2β1 integrin and the innate immune response

The α2β1 integrin is expressed on activated T lymphocytes, natural killer cells, other inflammatory cells, and mast cells. We have recently discovered that the α2β1 integrin is a novel receptor for multiple collectins and the C1q complement protein and is required for the innate immune response. The α2β1 integrin provides a co-stimulatory signal required for mast cell activation, cytokine secretion and initiation of innate immunity. We recently demonstrated that crosstalk between c-met/hepatocyte growth factor receptor and the α2β1 integrin contributes to mast-cell activation. Ongoing projects are directed toward understanding the role that the α2β1 integrin plays in immune modulation in the tumor microenvironment.

Research Keywords
Integrin, cell adhesion, tumor biology, tumor-host interactions, endothelial and epithelial morphogenesis, innate immunity, mast cells, angiogenesis, metastasis
Clinical Research Keywords
Hematopathology, Leukemia, Lymphoma
Publications
McCall-Culbreath KD, Li Z, Zutter MM. Crosstalk between the alpha2beta1 integrin and c-met/HGF-R regulates innate immunity. Blood [print-electronic]. 2008 Apr 4/1/2008; 111(7): 3562-70. PMID: 18198349, PMCID: PMC2275022, PII: blood-2007-08-107664, DOI: 10.1182/blood-2007-08-107664, ISSN: 0006-4971.

Zhang Z, Ramirez NE, Yankeelov TE, Li Z, Ford LE, Qi Y, Pozzi A, Zutter MM. Alpha2beta1 integrin expression in the tumor microenvironment enhances tumor angiogenesis in a tumor cell-specific manner. Blood [print-electronic]. 2008 Feb 2/15/2008; 111(4): 1980-8. PMID: 18042800, PMCID: PMC2234046, PII: blood-2007-06-094680, DOI: 10.1182/blood-2007-06-094680, ISSN: 0006-4971.

McCall-Culbreath KD, Zutter MM. Collagen receptor integrins: rising to the challenge. Curr Drug Targets. 2008 Feb; 9(2): 139-49. PMID: 18288965, ISSN: 1873-5592.

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.

Zutter MM. Integrin-mediated adhesion: tipping the balance between chemosensitivity and chemoresistance. Adv. Exp. Med. Biol. 2007; 608: 87-100. PMID: 17993234, ISSN: 0065-2598.

Zutter MM, Edelson BT. The alpha2beta1 integrin: a novel collectin/C1q receptor. Immunobiology [print-electronic]. 2007; 212(4-5): 343-53. PMID: 17544819, PII: S0171-2985(06)00148-3, DOI: 10.1016/j.imbio.2006.11.013, ISSN: 0171-2985.

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.

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. 2006; 107: 143-56.

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.

DeClerck YA, Mercurio AM, Stack MS, Chapman HA, Zutter MM, Muschel RJ, Raz A, Matrisian LM, Sloane BF, Noel A, Hendrix MJ, Coussens L, Padarathsingh M. Proteases, extracellular matrix, and cancer: a workshop of the path B study section. Am. J. Pathol. 2004 Apr; 164(4): 1131-9. PMID: 15039201, PMCID: PMC1615345, PII: S0002-9440(10)63200-2, DOI: 10.1016/S0002-9440(10)63200-2, ISSN: 0002-9440.

Edelson BT, Li Z, Pappan LK, Zutter MM. Mast cell-mediated inflammatory responses require the alpha 2 beta 1 integrin. Blood [print-electronic]. 2004 Mar 3/15/2004; 103(6): 2214-20. PMID: 14645004, PII: 2003-08-2978, DOI: 10.1182/blood-2003-08-2978, ISSN: 0006-4971.

Zutter, MM, Santoro, SA. Widespread histologic distribution of the a2b1 integin cell surface collagan receptor. Am J Pathol. 2004; 137: 113-20.

Edelson, BT, Li, Z, Pappan, LK, Zutter, MM. Mast cell-mediated inflammatory responses require the a2b1 integrin. Blood. 2004; 103: 2214-20.

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.

Grenache, DG, Coleman, T, Semenkovich, CF, santoro, SA, Zutter, MM. A2b1 integrin and development of atheroscierosis in a mouse model: Assessment of risk. Arteriosclerosis, Thombois, and Vascular Biology. 2003; 23: 2104-9.

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.

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.

Kaleem Z, White G, Zutter MM. Aberrant expression of T-cell-associated antigens on B-cell non-Hodgkin lymphomas. Am. J. Clin. Pathol. 2001 Mar; 115(3): 396-403. PMID: 11242796, DOI: 10.1309/EHMY-7WU1-UYE7-EE99, ISSN: 0002-9173.

Klekotka, PA, Santoro, SA, Zutter, MM. A2 integrin subunit cytoplasmic domain dependent cellular migration requiresp38 MAPK. J Biol Chem. 2001; 276: 9503-11.

O'Sullivan MJ, Kaleem Z, Bolger MJ, Swanson PE, Zutter MM. Composite prolymphocytoid and hodgkin transformation of chronic lymphocytic leukemia. Arch. Pathol. Lab. Med. 2000 Jun; 124(6): 907-9. PMID: 10835534, DOI: 10.1043/0003-9985(2000)124<0907:CPAHTO>2.0.CO;2, ISSN: 0003-9985.

Kaleem Z, Zehnbauer BA, White G, Zutter MM. Lack of expression of surface immunoglobulin light chains in B-cell non-Hodgkin lymphomas. Am. J. Clin. Pathol. 2000 Mar; 113(3): 399-405. PMID: 10705821, DOI: 10.1309/28ED-MM0T-DT3B-MT4P, ISSN: 0002-9173.

Kaleem Z, Shuster JJ, Carroll AJ, Borowitz MJ, Pullen DJ, Camitta BM, Zutter MM, Watson MS. Acute lymphoblastic leukemia with an unusual t(8;14)(q11.2;q32): a Pediatric Oncology Group Study. Leukemia. 2000 Feb; 14(2): 238-40. PMID: 10673739, ISSN: 0887-6924.

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.

Wang, H, Gai, Q, Yang, X, Li, Z, Linders, B, Santoro, S, Zutter, M. Role of the a1 and a2 integrin cytoplasmic domains in cell morphology, motility and responsiveness to stimulation by the protein kinase C pathway. Cell Adhesion and Communication. 2000; 74: 281-97.

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.

Kaleem Z, Watson MS, Zutter MM, Blinder MA, Hess JL. Acute promyelocytic leukemia with additional chromosomal abnormalities and absence of Auer rods. Am. J. Clin. Pathol. 1999 Jul; 112(1): 113-8. PMID: 10396293, ISSN: 0002-9173.

Zutter MM, Painter AD, Yang X. The Megakaryocyte/Platelet-specific enhancer of the alpha2beta1 integrin gene: two tandem AP1 sites and the mitogen-activated protein kinase signaling cascade. Blood. 1999 Mar 3/1/1999; 93(5): 1600-11. PMID: 10029589, ISSN: 0006-4971.

Zutter, MM, Painter, AD, Yang, X. The megakaryocyte/platelet-specific enhancer of the a2b1 integrin gene: Two tandem AP1 sites and the mitogen activated protein kinase signaling cascade. Blood. 1999; 93: 1600-11.

Zutter, MM, Santoro, SA, Wu, JE, Wakatsuki, T, Dickeson, SK, Elson, E. Collagen receptor control of epithelial morphogenesis and cell cycle progression. Am J Path. 1999; 155: 927-40.

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. Gastrointestinal carcinoma antigen GA733: target for immunodestruction and potential modifier of invasiveness and chemoresponsiveness [editorial]. J. Natl. Cancer Inst. 1998 May 5/6/1998; 90(9): 642-4. PMID: 9586655, ISSN: 0027-8874.

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.

Zutter MM, Hess JL. Guidelines for the diagnosis of leukemia or lymphoma in children. Am. J. Clin. Pathol. 1998 Apr; 109(4 Suppl 1): S9-22. PMID: 9533745, ISSN: 0002-9173.

Naughton MJ, Hess JL, Zutter MM, Bartlett NL. Bone marrow staging in patients with non-Hodgkin's lymphoma: is flow cytometry a useful test?. Cancer. 1998 Mar 3/15/1998; 82(6): 1154-9. PMID: 9506363, PII: 10.1002/(SICI)1097-0142(19980315)82:6<1154::AID-CNCR21>3.0.CO;2-4, ISSN: 0008-543X.

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.

Zutter, MM, Sun, H, Santoro, SA. Altered integrin expression and the malignant phenotype: the contribution of multiple integrated integrin-derived influences. J Mam Gland Biol and Neo. 1998; 3(2): 191-200.

Xu, J, Zutter, MM, Santoro, SA, Clark, RAF. A three dimensional collagen lattice ctivates NF-kB in human fibroblasts: role in integrin a2 gene expression and tissue remodeling. J Cell Biol. 1998; 140: 709-19.

Hong, S, Santoro, SA, Zutter, MM. Down-stream events in mammary gland morphogenesis mediated by re-expression of the a2b1 integrin: the role of the a6 and b4 integrin subunits. Cancer Research. 1998; 58: 2224-33.

Tachibana I, Bodorova J, Berditchevski F, Zutter MM, Hemler ME. NAG-2, a novel transmembrane-4 superfamily (TM4SF) protein that complexes with integrins and other TM4SF proteins. J. Biol. Chem. 1997 Nov 11/14/1997; 272(46): 29181-9. PMID: 9360996, ISSN: 0021-9258.

Zutter MM, Ryan EE, Painter AD. Binding of phosphorylated Sp1 protein to tandem Sp1 binding sites regulates alpha2 integrin gene core promoter activity. Blood. 1997 Jul 7/15/1997; 90(2): 678-89. PMID: 9226168, ISSN: 0006-4971.

Zutter, MM, Ryan, EE, Painter, AD. Binding of phosphorylated Sp1 protein to tandem Sp1 binding sites regulates a2 integrin gene core promoter activity. Blood. 1997; 90: 678-89.

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.

Clatch RJ, Walloch JL, Zutter MM, Kamentsky LA. Immunophenotypic analysis of hematologic malignancy by laser scanning cytometry. Am. J. Clin. Pathol. 1996 Jun; 105(6): 744-55. PMID: 8659450, ISSN: 0002-9173.

Berditchevski F, Zutter MM, Hemler ME. Characterization of novel complexes on the cell surface between integrins and proteins with 4 transmembrane domains (TM4 proteins). Mol. Biol. Cell. 1996 Feb; 7(2): 193-207. PMID: 8688552, PMCID: PMC275873, ISSN: 1059-1524.

Hess JL, Zutter MM, Castleberry RP, Emanuel PD. Juvenile chronic myelogenous leukemia. Am. J. Clin. Pathol. 1996 Feb; 105(2): 238-48. PMID: 8607451, ISSN: 0002-9173.

Zutter MM, Painter AA, Staatz WD, Tsung YL. Regulation of alpha 2 integrin gene expression in cells with megakaryocytic features: a common theme of three necessary elements. Blood. 1995 Oct 10/15/1995; 86(8): 3006-14. PMID: 7579393, ISSN: 0006-4971.

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.

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.

Grossman, WJ, Kimata, JT, Wong, FH, Zutter, MM, Ley, T, Ratner, L. Development of leukemia in mice transgenic for the Tax gene of human T-cell leukemia virus Type 1. Proc Natl Acad Sci USA. 1995; 92: 1057-61.

Zutter, MM, Santoro, SA, Staatz, WD, Tsung, YL. Re-expression of the a2b1 integrin abrogates the malignant phenotype of breast carcinoma cells. Proc Natl Acad Sci USA. 1995; 92: 7411-5.

Keely, PJ, Fong, AM, Zutter, MM, Santoro, SA. Alteration of collagen-dependent adhesion, motility, and morphogenesis by the expression of antisense a2 integrin mRNA in mammary cells. J Cell Science. 1995; 108: 595-607.

Santoro, SA, Zutter, MM. A collagen receptor on platelets and other cells. Thromb Haemostas. 1995; 74: 813-21.

Zutter, MM, Painter, AD, Staatz, WD, Tsung, YL. Regulation of a2 integrin gene espression during megakaryocte differentiation: A common theme of three necessary elements for megakaryocyte-specific, developmentally regulated gene expression. Blood. 1995; 86: 3006-14.

Clatch RJ, Krigman HR, Peters MG, Zutter MM. Dysplastic haemopoiesis following orthotopic liver transplantation: comparison with similar changes in HIV infection and primary myelodysplasia. Br. J. Haematol. 1994 Dec; 88(4): 685-92. PMID: 7819094, ISSN: 0007-1048.

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.

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.

Zutter, MM, Santoro, SA, Painter, AS, Tsung, YL, Gafford, A. Identification of positive and negative regulatory elements important in cell-type and developmentally-restricted gene expression. J Biol Chem. 1994; 269: 463-9.

Kaufman BA, Jones L, Zutter MM, Park TS. Megakaryoblastic leukemia presenting as a temporal bone granulocytic sarcoma. Case report. J. Neurosurg. 1993 Jul; 79(1): 128-31. PMID: 8315452, DOI: 10.3171/jns.1993.79.1.0128, ISSN: 0022-3085.

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.

Lentz SR, Krewson L, Zutter MM. Recurrent neuroendocrine (Merkel cell) carcinoma of the skin presenting as marrow failure in a man with systemic lupus erythematosus. Med. Pediatr. Oncol. 1993; 21(2): 137-41. PMID: 8433681, ISSN: 0098-1532.

Zutter, MM, Krigman, HR, Santoro, SA. Altered integrin expression in adenocarcinoma of the breast: Analysis by in situ hybridization. Am J Pathol. 1993; 142: 1439-48.

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.

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.

Zutter, MM, Fong, AF, Krigman, HR, Santoro, SA. Differential regulation of the a(2)b(1) and a(IIb)b(3) integrin genes during megakaryocytic differentiation of pluripotent K562 leukemia cells. J Biol Chem. 1992; 267: 20233-8.

Zutter MM. Immunolocalization of integrin receptors in normal lymphoid tissues. Blood. 1991 May 5/15/1991; 77(10): 2231-6. PMID: 2029582, ISSN: 0006-4971.

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.

Gratama JW, Zutter MM, Minarovits J, Oosterveer MA, Thomas ED, Klein G, Ernberg I. Expression of Epstein-Barr virus-encoded growth-transformation-associated proteins in lymphoproliferations of bone-marrow transplant recipients. Int. J. Cancer. 1991 Jan 1/21/1991; 47(2): 188-92. PMID: 1846349, ISSN: 0020-7136.

Zutter, MM. The immunolocalization of integrin receptors in normal lymphoid tissues. Blood. 1991; 77: 2231-6.

Hockenbery, D, Zutter, MM, Hickey, W., Nahm, M., Korsmeyer, SJ. Bcl-2 protein expression is topographically restricted in tissue characterized by apoptotic cell death. Proc Natl Acad Sci USA. 1991; 88: 6961-5.

Zutter MM, Durnam DM, Hackman RC, Loughran TP, Kidd PG, Ashley RL, Petersdorf EW, Martin PJ, Thomas ED. Secondary T-cell lymphoproliferation after marrow transplantation. Am. J. Clin. Pathol. 1990 Dec; 94(6): 714-21. PMID: 2173884, ISSN: 0002-9173.

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.

Zutter MM, Gersell DJ. Acute lymphoblastic leukemia. An unusual case of primary relapse in the uterine cervix. Cancer. 1990 Sep 9/1/1990; 66(5): 1002-4. PMID: 2386910, ISSN: 0008-543X.

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.

Atlas AB, Manthei U, Zutter MM, Polmar SH. Necrotizing granulomatosis of the spleen in chronic granulomatous disease. Am. J. Dis. Child. 1990 Jan; 144(1): 14-5. PMID: 2403745, ISSN: 0002-922X.

Zutter MM, Martin PJ, Hanke D, Kidd PG. CD7+ acute non-lymphocytic leukemia: evidence for an early multipotential progenitor. Leuk. Res. 1990; 14(1): 23-6. PMID: 1689436, PII: 0145-2126(90)90142-V, ISSN: 0145-2126.

Zutter, MM, Mazoujian, G., Santoro, SA. Decreased expression of integrin adhesive protein receptors in adenocarcinoma of the breast. Am J Pathol. 1990; 137: 863-70.

Zutter MM, Martin PJ, Sale GE, Shulman HM, Fisher L, Thomas ED, Durnam DM. Epstein-Barr virus lymphoproliferation after bone marrow transplantation. Blood. 1988 Aug; 72(2): 520-9. PMID: 2840986, ISSN: 0006-4971.