Mechanisms of PECAM-1-mediated cytoprotection and implications for cancer cell survival

Leukemia and Lymphoma

Volumn 46, Issue 10, 2005, Pages 1409-1421

  Bergom, Carmen ^a   Gao, Cunji ^a   Newman, Peter J ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Apoptosis; Cancer; Leukemia; PECAM 1; SHP 2

Indexed keywords

ANTINEOPLASTIC AGENT; CD31 ANTIGEN; PROTEIN TYROSINE PHOSPHATASE SHP 2;

APOPTOSIS; CANCER CELL; CANCER RESISTANCE; CARCINOGENESIS; CELL ADHESION; CELL PROTECTION; CELL SURVIVAL; DRUG MECHANISM; HEMATOLOGIC MALIGNANCY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; LEUKEMIA; LYMPHOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SOLID TUMOR;

ANIMALS; ANTIGENS, CD31; CELL SURVIVAL; CYTOPROTECTION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; NEOPLASMS; PROTEIN-TYROSINE-PHOSPHATASE; SIGNAL TRANSDUCTION;

EID: 26944440907     PISSN: 10428194     EISSN: None     Source Type: Journal    
DOI: 10.1080/10428190500126091     Document Type: Review

References (126)

1. Johnstone RW, Ruefli AA, Lowe SW. Apoptosis: a link between cancer genetics and chemotherapy. Cell 2002;108: 153-164.
2. Kitada S, Pedersen IM, Schimmer AD, Reed JC. Dysregulation of apoptosis genes in hematopoietic malignancies. Oncogene 2002;21:3459-3474.
3. Schimmer AD, Pedersen IM, Kitada S, Eksioglu-Demiralp E, Minden MD, Pinto R, et al. Functional blocks in caspase activation pathways are common in leukemia and predict patient response to induction chemotherapy. Cancer Res 2003;63:1242-1248.
4. Schimmer AD, Munk-Pedersen I, Minden MD, Reed JC. Bcl-2 and apoptosis in chronic lymphocytic leukemia. Curr Treat Options Oncol 2003;4:211-218.
5. Frisch SM, Ruoslahti E. Integrins and anoikis. Curr Opin Cell Biol 1997;9:701-706.
6. Watt SM, Williamson J, Genevier H, Fawcett J, Simmons DL, Hatzfeld A, et al. The heparin binding PECAM-1 adhesion molecule is expressed by CD34+ hematopoietic precursor cells with early myeloid and B-lymphoid cell phenotypes. Blood 1993;82:2649-2663.
7. Jackson DE, Gully LM, Henshall TL, Mardell CE, Macardle PJ. Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31) is associated with a naive B-cell phenotype in human tonsils. Tissue Antigens 2000;56:105-116.
8. Mazurov AV, Vinogradov DV, Kabaeva NV, Antonova GN, Romanov YA, Vlasik TN, et al. A monoclonal antibody, VM64, reacts with a 130 kDa glycoprotein common to platelets and endothelial cells: heterogeneity in antibody binding to human aortic endothelial cells. Thromb Haemost 1991;66:494-499.
9. Metzelaar MJ, Korteweg J, Sixma JJ, Nieuwenhuis HK. Biochemical characterization of PECAM-1 (CD31 antigen) on human platelets. Thromb Haemost 1991;66(6):700-707.
10. Newman PJ. The role of PECAM-1 in vascular cell biology. Ann N Y Acad Sci 1994;714:165-174.
11. Tanaka Y, Albelda SM, Horgan KJ, van Seventer GA, Shimizu Y, Newman W et al. CD31 expressed on distinctive T cell subsets is a preferential amplifier of beta 1 integrin-mediated adhesion. J Exp Med 1992;176:245-253.
12. Torimoto Y, Rothstein DM, Dang NH, Schlossman SF, Morimoto C. CD31, a novel cell surface marker for CD4 cells of suppressor lineage, unaltered by state of activation. J Immunol 1992;148:388-396.
13. Zehnder JL, Hirai K, Shatsky M, McGregor JL, Levin LJ, Leung LL. The cell adhesion molecule CD31 is phosphorylated after cell activation. Down-regulation of CD31 in activated T lymphocytes. J Biol Chem 1992;267:5243-5249.
14. Muller WA, Ratti CM, McDonnell SL, Cohn ZA. A human endothelial cell-restricted, externally disposed plasmalemmal protein enriched in intercellular junctions. J Exp Med 1989;170:399-414.
15. Albelda SM, Oliver PD, Romer LH, Buck CA. EndoCAM: a novel endothelial cell-cell adhesion molecule. J Cell Biol 1990;110:1227-1237.
16. Newman PJ, Berndt MC, Gorski J, White GC, Lyman S, Paddock C, Muller WA. PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily. Science 1990;247:1219-1222.
17. Sun J, Williams J, Yan HC, Amin KM, Albelda SM, DeLisser HM. Platelet endothelial cell adhesion molecule-1 (PECAM-1) homophilic adhesion is mediated by immunoglobulin-like domains 1 and 2 and depends on the cytoplasmic domain and the level of surface expression. J Biol Chem 1996;271:18561-18570.
18. Sun QH, DeLisser HM, Zukowski MM, Paddock C, Albelda SM, Newman PJ. Individually distinct Ig homology domains in PECAM-1 regulate homophilic binding and modulate receptor affinity. J Biol Chem 1996;271:11090-11098.
19. DeLisser HM, Christofidou-Solomidou M, Strieter RM, Burdick MD, Robinson CS, Wexler RS et al. Involvement of endothelial PECAM-1/CD31 in angiogenesis. Am J Pathol 1997;151:671-677.
20. Zhou Z, Christofidou-Solomidou M, Garlanda C, DeLisser HM. Antibody against murine PECAM-1 inhibits tumor angiogenesis in mice. Angiogenesis 1999;3:181-188.
21. Cao G, O'Brien CD, Zhou Z, Sanders SM, Greenbaum JN, Makrigiannakis A, DeLisser HM. Involvement of human PECAM-1 in angiogenesis and in vitro endothelial cell migration. Am J Physiol Cell Physiol 2002;282:C1181-C1190.
22. Muller WA, Weigl SA, Deng X, Phillips DM. PECAM-1 is required for transendothelial migration of leukocytes. J Exp Med 1993;178:449-460.
23. Vaporciyan AA, DeLisser HM, Yan HC, Mendiguren II, Thom SR, Jones ML, et al. Involvement of platelet-endothelial cell adhesion molecule-1 in neutrophil recruitment in vivo. Science 1993;262:1580-1582.
24. Jackson DE, Ward CM, Wang R, Newman PJ. The protein-tyrosine phosphatase SHP-2 binds platelet/endothelial cell adhesion molecule-1 (PECAM-1) and forms a distinct signaling complex during platelet aggregation. Evidence for a mechanistic link between PECAM-1- and integrin-mediated cellular signaling. J Biol Chem 1997;272:6986-6993.
25. Masuda M, Osawa M, Shigematsu H, Harada N, Fujiwara K. Platelet endothelial cell adhesion molecule-1 is a major SH-PTP2 binding protein in vascular endothelial cells. FEBS Lett 1997;408:331-336.
26. Jackson DE, Kupcho KR, Newman PJ. Characterization of phosphotyrosine binding motifs in the cytoplasmic domain of platelet/endothelial cell adhesion molecule-1 (PECAM-1) that are required for the cellular association and activation of the protein-tyrosine phosphatase, SHP-2. J Biol Chem 1997;272:24868-24875.
27. Sagawa K, Kimura T, Swieter M, Siraganian RP. The protein-tyrosine phosphatase SHP-2 associates with tyrosine-phosphorylated adhesion molecule PECAM-1 (CD31). J Biol Chem 1997;272:31086-31091.
28. Cao MY, Huber M, Beauchemin N, Famiglietti J, Albelda SM, Veillette A. Regulation of mouse PECAM-1 tyrosine phosphorylation by the Src and Csk families of protein-tyrosine kinases. J Biol Chem 1998;273:15765-15772.
29. Hua CT, Gamble Jr, Vadas MA, Jackson DE. Recruitment and activation of SHP-1 protein-tyrosine phosphatase by human platelet endothelial cell adhesion molecule-1 (PECAM-1). Identification of immunoreceptor tyrosine-based inhibitory motif-like binding motifs and substrates. J Biol Chem 1998;273:28332-28340.
30. Pumphrey NJ, Taylor V, Freeman S, Douglas MR, Bradfield PF, Young SP, et al. Differential association of cytoplasmic signalling molecules SHP-1, SHP-2, SHIP and phospholipase C-gamma1 with PECAM-1/CD31. FEBS Lett 1999;450:77-83.
31. Newton-Nash DK, Newman PJ. A new role for platelet-endothelial cell adhesion molecule-1 (CD31): inhibition of TCR-mediated signal transduction. J Immunol 1999; 163:682-688.
32. Henshall TL, Jones KL, Wilkinson R, Jackson DE. Src homology 2 domain-containing protein-tyrosine phosphatases, SHP-1 and SHP-2, are required for platelet endothelial cell adhesion molecule-1/CD31-mediated inhibitory signaling. J Immunol 2001;166:3098-3106.
33. Osawa M, Masuda M, Kusano K, Fujiwara K. Evidence for a role of platelet endothelial cell adhesion molecule-1 in endothelial cell mechanosignal transduction: is it a mechanoresponsive molecule? J Cell Biol 2002;158:773-785.
34. Newman PJ. Switched at birth: a new family for PECAM-1. J Clin Invest 1999;103:5-9.
35. Patil S, Newman DK, Newman PJ. Platelet endothelial cell adhesion molecule-1 serves as an inhibitory receptor that modulates platelet responses to collagen. Blood 2001; 97:1727-1732.
36. Jones KL, Hughan SC, Dopheide SM, Farndale RW, Jackson SP, Jackson DE. Platelet endothelial cell adhesion molecule-1 is a negative regulator of platelet-collagen interactions. Blood 2001;98:1456-1463.
37. Wilkinson R, Lyons AB, Roberts D, Wong MX, Bartley PA, Jackson DE. Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31) acts as a regulator of B-cell development, B-cell antigen receptor (BCR)-mediated activation, and autoimmune disease. Blood 2002;100:184-193.
38. Piali L, Albelda SM, Baldwin HS, Hammel P, Gisler RH, Imhof BA. Murine platelet endothelial cell adhesion molecule (PECAM-1)/CD31 modulates beta 2 integrins on lymphokine-activated killer cells. Eur J Immunol 1993; 23:2464-2471.
39. Leavesley DI, Oliver JM, Swart BW, Berndt MC, Haylock DN, Simmons PJ. Signals from platelet/endothelial cell adhesion molecule enhance the adhesive activity of the very late antigen-4 integrin of human CD34+ hemopoietic progenitor cells. J Immunol 1994;153:4673-4683.
40. Berman ME, Muller WA. Ligation of platelet/endothelial cell adhesion molecule 1 (PECAM-1/CD31) on monocytes and neutrophils increases binding capacity of leukocyte CR3 (CD11b/CD18). J Immunol 1995;154:299-307.
41. Berman ME, Xie Y, Muller WA. Roles of platelet/endothelial cell adhesion molecule-1 (PECAM-1, CD31) in natural killer cell transendothelial migration and beta 2 integrin activation. J Immunol 1996;156:1515-1524.
42. Varon D, Jackson DE, Shenkman B, Dardik R, Tamarin I, Savion N, Newman PJ. Platelet/endothelial cell adhesion molecule-1 serves as a costimulatory agonist receptor that modulates integrin-dependent adhesion and aggregation of human platelets. Blood 1998;91:500-507.
43. Chiba R, Nakagawa N, Kurasawa K, Tanaka Y, Saito Y, Iwamoto I. Ligation of CD31 (PECAM-1) on endothelial cells increases adhesive function of alphavbeta3 integrin and enhances beta1 integrin-mediated adhesion of eosinophils to endothelial cells. Blood 1999;94:1319-1329.
44. Zhao T, Newman PJ. Integrin activation by regulated dimerization and oligomerization of platelet endothelial cell adhesion molecule (PECAM)-1 from within the cell. J Cell Biol 2001;152:65-73.
45. Maas M, Stapleton M, Bergom C, Mattson DL, Newman DK, Newman PJ. Endothelial cell PECAM-1 confers protection against endotoxic shock. Am J Physiol Heart Circ Physiol 2005;288:H159-H164.
46. Carrithers M, Tandon S, Canosa S, Michaud M, Graesser D, Madri JA. Enhanced susceptibility to endotoxic: shock and impaired STAT3 signaling in CD31-deficient mice. Am J Pathol 2005;166:185-196.
47. Noble KE, Wickremasinghe RG, DeCornet C, Panayiotidis P, Yong KL. Monocytes stimulate expression of the Bcl-2 family member, A1, in endothelial cells and confer protection against apoptosis. J Immunol 1999;162:1376-1383.
48. Bird IN, Taylor V, Newton JP, Spragg JH, Simmons DL, Salmon M, Buckley CD. Homophilic PECAM-1(CD31) interactions prevent endothelial cell apoptosis but do not support cell spreading or migration. J Cell Sci 1999;112(Pt 12):1989-1997.
49. Evans PC, Taylor ER, Kilshaw PJ. Signaling through CD31 protects endothelial cells from apoptosis. Transplantation 2001;71:457-460.
50. Ferrero E, Belloni D, Contini P, Foglieni C, Ferrero ME, Fabbri M, et al. Transendothelial migration leads to protection from starvation-induced apoptosis in CD34+CD14+ circulating precursors: evidence for PECAM-1 involvement through Akt/PKB activation. Blood 2003;101:186-193.
51. Gao C, Sun W, Christofidou-Solomidou M, Sawada M, Newman DK, Bergom C et al. PECAM-1 functions as a specific and potent inhibitor of mitochondrial-dependent apoptosis. Blood 2003;102:169-179.
52. Limaye VS, Li X, Hahn C, Xia P, Berndt MC, Vadas MA, Gamble JR. Sphingosine kinase-1 enhances endothelial cell survival through a PECAM-1-dependent activation of PI-3K/Akt and regulation of Bcl-2 family members. Blood 2005; 105:3169-3177.
53. Hengartner MO. The biochemistry of apoptosis. Nature 2000;407:770-776.
54. Newman PJ, Newman DK. Signal transduction pathways mediated by PECAM-1: new roles for an old molecule in platelet and vascular cell biology. Arterioscler Thromb Vasc Biol 2003;23:953-964.
55. Pellegatta F, Chierchia SL, Zocchi MR. Functional association of platelet endothelial cell adhesion molecule-1 and phosphoinositide 3-kinase in human neutrophils. J Biol Chem 1998;273:27768-27771.
56. Matsumura T, Wolff K, Petzelbauer P. Endothelial cell tube fonnation depends on cadherin 5 and CD31 interactions with filamentous actin. J Immunol. 1997;158:3408-3416.
57. Ilan N, Mahooti S, Rimm DL, Madri JA. PECAM-1 (CD31) functions as a reservoir for and a modulator of tyrosine-phosphorylated beta-catenin. J Cell Sci 1999;112 (Pt 18): 3005-3014.
58. Ilan N, Cheung L, Pinter E, Madri JA. Platelet-endothelial cell adhesion molecule-1 (CD31), a scaffolding molecule for selected catenin family members whose binding is mediated by different tyrosine and serine/threonine phosphorylation. J Biol Chem 2000;275:21435-21443.
59. Fukuda Y, Aoyama Y, Wada A, Igarashi Y. Identification of PECAM-1 association with sphingosine kinase 1 and its regulation by agonist-induced phosphorylation. Biochim Biophys Acta 2004;1636:12-21.
60. Ilan N, Cheung L, Miller S, Mohsenin A, Tucker A, Madri JA. Pecam-1 is a modulator of star family member phosphorylation and localization: lessons from a transgenic mouse. Dev Biol 2001;232:219-232.
61. O'Brien CD, Ji G, Wang YX, Sun J, Krymskaya VP, Ruberg FL, et al. PECAM-1 (CD31) engagement activates a phosphoinositide-independent, nonspecific cation channel in endothelial cells. FASEB J 2001;15:1257-1260.
62. Ji G, O'Brien CD, Feldman M, Manevich Y, Lim P, Sun J, et al. PECAM-1 (CD31) regulates a hydrogen peroxide-activated nonselective cation channel in endothelial cells. J Cell Biol 2002;157:173-184.
63. Wong MX, Harbour SN, Wee JL, Lau LM, Andrews RK, Jackson DE. Proteolytic cleavage of platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31) is regulated by a calmodulin-binding motif. FEBS Lett 2004;568(1-3):70-78.
64. Deaglio S, Morra M, Mallone R, Ausiello CM, Prager E, Garbarino G, et al. Human CD38 (ADP-ribosyl cyclase) is a counter-receptor of CD31, an Ig superfamily member. J Immunol 1998;160:395-402.
65. Oakes SA, Opferman JT, Pozzan T, Korsmeyer SJ, Scorrano L. Regulation of endoplasmic reticulum Ca2+ dynamics by proapoptotic BCL-2 family members. Biochem Pharmacol 2003;66:1335-1340.
66. Neel BG, Gu H, Pao L. The 'Shp'ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends Biochem Sci 2003;28:284-293.
67. Tartaglia M, Mehler EL, Goldberg R, Zampino G, Brunner HG, Kremer H et al. Mutations in PTPN11, encoding the protein tyrosine phosphatase SHP-2, cause Noonan syndrome. Nat Genet 2001;29:465-468.
68. Tartaglia M, Kalidas K, Shaw A, Song X, Musat DL, Van DBI, et al. PTPN11 mutations in Noonan syndrome: molecular spectrum, genotype-phenotype correlation, and phenotypic heterogeneity. Am J Hum Genet 2002;70:1555-1563.
69. Kosaki K, Suzuki T, Muroya K, Hasegawa T, Sato S, Matsuo N, et al. PTPN11 (protein-tyrosine phosphatase, nonreceptor-type 11) mutations in seven Japanese patients with Noonan syndrome. J Clin Endocrinol Metab 2002;87:3529-3533.
70. Yoshida R, Hasegawa T, Hasegawa Y, Nagai T, Kinoshita E, Tanaka Y, et al. Protein-tyrosine phosphatase, nonreceptor type 11 mutation analysis and clinical assessment in 45 patients with Noonan syndrome. J Clin Endocrinol Metab 2004;89:3359-3364.
71. Tartaglia M, Niemeyer CM, Fragale A, Song X, Buechner J, Jung A, et al. Somatic mutations in PTPN11 in juvenile myelomonocytic leukemia, myelodysplastic syndromes and acute myeloid leukemia. Nat Genet 2003;34:148-150.
72. Loh ML, Vattikuti S, Schubbert S, Reynolds MG, Carlson E, Lieuw KH, et al. Mutations in PTPN11 implicate the SHP-2 phosphatase in leukemogenesis. Blood 2004;103:2325-2331.
73. Loh ML, Reynolds MG, Vattikuti S, Gerbing RB, Alonzo TA, Carlson E, et al. PTPN11 mutations in pediatric patients with acute myeloid leukemia: results from the Children's Cancer Group. Leukemia 2004;18:1831-1834.
74. Tartaglia M, Martinelli S, Cazzaniga G, Cordeddu V, Iavarone I, Spinelli M, et al. Genetic evidence for lineage-related and differentiation stage-related contribution of somatic PTPN11 mutations to leukemogenesis in childhood acute leukemia. Blood 2004;104:307-313.
75. Bentires-Alj M, Paez JG, David FS, Keilhack H, Halmos B, Naold K, et al. Activating mutations of the noonan syndrome-associated SHP2/PTPN11 gene in human solid tumors and adult acute myelogenous leukemia. Cancer Res 2004;64:8816-8820.
76. Tartaglia M, Niemeyer CM, Shannon KM, Loh ML. SHP-2 and myeloid malignancies. Curr Opin Hematol 2004;11:44-50.
77. Zhang SQ, Yang W, Kontaridis MI, Bivona TG, Wen G, Araki T, et al. Shp2 regulates SRC family kinase activity and Ras/Erk activation by controlling Csk recruitment. Mol Cell 2004;13:341-355.
78. Yuan L, Yu WM, Yuan Z, Haudenschild CC, Qu CK. Role of SHP-2 tyrosine phosphatase in the DNA damage-induced cell death response. J Biol Chem 2003;278:15208-15216.
79. Ivins ZC, Kontaridis MI, Fornaro M, Feng GS, Bennett AM. SHP-2 regulates the phosphatidylinositide 3′-kinase/Akt pathway and suppresses caspase 3-mediated apoptosis. J Cell Physiol 2004;199:227-236.
80. Wu CJ, O'Rourke DM, Feng GS, Johnson GR, Wang Q, Greene MI. The tyrosine phosphatase SHP-2 is required for mediating phosphatidylinositol 3-kinase/Akt activation by growth factors. Oncogene 2001;20:6018-6025.
81. Zhang SQ, Tsiaras WG, Araki T, Wen G, Minichiello L, Klein R, Neel BG. Receptor-specific regulation of phosphatidylinositol 3′-kinase activation by the protein tyrosine phosphatase Shp2. Mol Cell Biol 2002;22:4062-4072.
82. Irby RB, Yeatman TJ. Role of Src expression and activation in human cancer. Oncogene 2000;19:5636-5642.
83. De Young BR, Swanson PE, Argenyi ZB, Ritter JH, Fitzgibbon JF, Stahl DJ, et al. CD31 immunoreactivity in mesenchymal neoplasms of the skin and subcutis: report of 145 cases and review of putative immunohistologic markers of endothelial differentiation. J Cutan Pathol 1995;22:215-222.
84. De Young BR, Frierson HF, Jr., Ly MN, Smith D, Swanson PE. CD31 immunoreactivity in carcinomas and mesotheliomas. Am J Clin Pathol 1998;110:374-377.
85. Nicholson SA, McDermott MB, DeYoung BR, Swanson PE. CD31 immunoreactivity in small round cell tumors. Appl Immunohistochem Mol Morphol 2000;8:19-24.
86. Parums DV, Cordell JL, Micklem K, Heryet AR, Gatter KC, Mason DY. JC70: a new monoclonal antibody that detects vascular endothelium associated antigen on routinely processed tissue sections. J Clin Pathol 1990;43:752-757.
87. Tang DG, Chen YQ, Newman PJ, Shi L, Gao X, Diglio CA, Honn KV. Identification of PECAM-1 in solid tumor cells and its potential involvement in tumor cell adhesion to endothelium. J Biol Chem 1993;268:22883-22894.
88. Miettinen M, Lindenmayer AE, Chaubal A. Endothelial cell markers CD31, CD34, and BNH9 antibody to H- and Y-antigens - evaluation of their specificity and sensitivity in the diagnosis of vascular tumors and comparison with von Willebrand factor. Mod Pathol 1994;7:82-90.
89. Martin-Padura I, De CC, Uccini S, Pilozzi E, Natali PG, Nicotra MR, et al. Expression of VE (vascular endothelial)-cadherin and other endothelial-specific markers in haemangiomas. J Pathol 1995;175:51-57.
90. Ohsawa M, Naka N, Tomita Y, Kawamori D, Kanno H, Aozasa K. Use of immunohistochemical procedures in diagnosing angiosarcoma. Evaluation of 98 cases. Cancer 1995;75:2867-2874.
91. Russell Jr, Orchard G, Zelger B, Wilson JE. Immunostaining for CD31 and CD34 in Kaposi sarcoma. J Clin Pathol 1995;48:1011-1016.
92. Poblet E, Gonzalez-Palacios F, Jimenez FJ. Different immunoreactivity of endothelial markers in well and poorly differentiated areas of angiosarcomas. Virchows Arch 1996;428:217-221.
93. Lin BT, Colby T, Gown AM, Hammar SP, Mertens RB, Churg A, Battifora H. Malignant vascular tumors of the serous membranes mimicking mesothelioma. A report of 14 cases. Am J Surg Pathol 1996;20:1431-1439.
94. Klementsen B, Jorgensen L. Distribution of adhesion molecules on HeLa cells, platelets and endothelium in an in vitro model mimicking the early phase of metastasis. An immunogold electron microscopic study. APMIS 1997; 105:546-558.
95. Davidson B, Goldberg I, Gotlieb WE, Lerner-Geva L, Ben Baruch G, Kopolovic J. Ulex Europaeus lectin and anti-CD31 staining in squamous cell carcinoma of the uterine cervix: potential prognostic markers. Int J Gynecol Pathol 1998;17:205-210.
96. Breiteneder-Geleff S, Soleiman A, Kowalski H, Horvat R, Amann G, Kriehuber E et al. Angiosarcomas express mixed endothelial phenotypes of blood and lymphatic capillaries: podoplanin as a specific marker for lymphatic endothelium. Am J Pathol 1999;154:385-394.
97. Aroca F, Renaud W, Bartoli C, Bouvier-Labit C, Figarella-Branger D. Expression of PECAM-1/CD31 isoforms in human brain gliomas. J Neurooncol 1999;43:19-25.
98. Tan ST, Velickovic M, Ruger BM, Davis PF. Cellular and extracellular markers of hemangioma. Plast Reconstr Surg 2000;106:529-538.
99. Sapino A, Bongiovanni M, Cassoni P, Righi L, Arisio R, Deaglio S, Malavasi F. Expression of CD31 by cells of extensive ductal in situ and invasive carcinomas of the breast. J Pathol 2001;194:254-261.
100. Perschbacher K, Jackson-Boeters L, Daley T. The adhesion molecules NCAM, HCAM, PECAM-1 and ICAM-1 in normal salivary gland tissues and salivary gland malignancies. J Oral Pathol Med 2004;33:230-236.
101. Xie Y, Muller WA. Assignment of PECAM1 to human chromosome bands 17q22- > q23 by in situ hybridization. Cytogenet Cell Genet 1996;74:156.
102. Kallioniemi A, Kallioniemi OP, Piper J, Tanner M, Stokke T, Chen L, et al. Detection and mapping of amplified DNA sequences in breast cancer by comparative genomic hybridization. Proc Natl Acad Sci USA 1994;91:2156-2160.
103. Righi L, Deaglio S, Pecchioni C, Gregorini A, Horenstein AL, Bussolati G, et al. Role of CD31/platelet endothelial cell adhesion molecule-1 expression in in vitro and in vivo growth and differentiation of human breast cancer cells. Am J Pathol 2003;162:1163-1174.
104. Stacchini A, Chiarle R, Antinoro V, Demurtas A, Novero D, Palestro G. Expression of the CD31 antigen in normal B-cells and non Hodgkin's lymphomas. J Biol Regul Homeost Agents 2003;17:308-315.
105. Garcia-Barros M, Paris F, Cordon-Cardo C, Lyden D, Rafii S, Haimovitz-Friedman A, et al. Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science 2003;300:1155-1159.
106. Ohto H, Maeda H, Shibata Y, Chen RF, Ozaki Y, Higashihara M, et al. A novel leukocyte differentiation antigen: two monoclonal antibodies TM2 and TM3 define a 120-kd molecule present on neutrophils, monocytes, platelets, and activated lymphoblasts. Blood 1985;66:873-881.
107. Goyert SM, Ferrero EM, Seremetis SV, Winchester RJ, Silver J, Mattison AC. Biochemistry and expression of myelomonocytic antigens. J Immunol 1986;137:3909-3914.
108. Ashman LK, Aylett GW, Cambareri AC, Cole SR. Different epitopes of the CD31 antigen identified by monoclonal antibodies: cell type-specific patterns of expression. Tissue Antigens 1991;38:199-207.
109. Kuzu I, Bicknell R, Harris AL, Jones M, Gatter KC, Mason DY. Heterogeneity of vascular endothelial cells with relevance to diagnosis of vascular tumours. J Clin Pathol 1992;45:143-148.
110. Tassone P, Bonelli P, Tuccillo F, Turco MC, De RG, Morrone G, et al. Analysis of peripheral blood normal and malignant cells with the novel murine monoclonal antibody UN2. Immunol Lett 1994;42:55-62.
111. Goldberger A, Middleton KA, Newman PJ. Changes in expression of the cell adhesion molecule PECAM-1 (CD31) during differentiation of human leukemic cell lines. Tissue Antigens 1994;44:285-293.
112. El-Marsafy S, Carosella ED, Agrawal SG, Gluckman E, Mansur IG, Elhabazi A, et al. Functional role of PECAM-1/CD31 molecule expressed on human cord blood progenitors. Leukemia 1996;10:1340-1346.
113. Govender D, Harilal P, Dada M, Chetty R. CD31 (JC70) expression in plasma cells: an immunohistochemical analysis of reactive and neoplastic plasma cells. J Clin Pathol 1997;50:490-493.
114. Sembries S, Pahl H, Stilgenbauer S, Dohner H, Schriever F. Reduced expression of adhesion molecules and cell signaling receptors by chronic lymphocytic leukemia cells with 11q deletion. Blood 1999;93:624-631.
115. De WM, Renmans W, Jochmans K, Schots R, Lacor P, Trullemans F, et al. Different expression of adhesion molecules on CD34+ cells in AML and B-lineage ALL and their normal bone marrow counterparts. Eur J Haematol 1999;63:192-201.
116. Vallario A, Chilosi M, Adami F, Montagna L, Deaglio S, Malavasi F, Caligaris-Cappio F. Human myeloma cells express the CD38 ligand CD31. Br J Haematol 1999;105:441-444.
117. Brouwer RE, Hoefnagel J, Borger van Der BB, Jedema I, Zwinderman YH, Starrenburg IC, et al. Expression of costimulatory and adhesion molecules and chemokine or apoptosis receptors on acute myeloid leukaemia: high CD40 and CD11a expression correlates with poor prognosis. Br J Haematol 2001;115:298-308.
118. Lee ST, Jang JH, Min YH, Hahn JS, Ko YW. AC133 antigen as a prognostic factor in acute leukemia. Leuk Res 2001;25:757-767.
119. Ibrahim S, Jilani I, O'Brien S, Rogers A, Manshouri T, Giles F, et al. Clinical relevance of the expression of the CD31 ligand for CD38 in patients with B-cell chronic lymphocytic leukemia. Cancer 2003;97:1914-1919.
120. Wang Y, Su X, Sorenson CM, Sheibani N. Modulation of PECAM-1 expression and alternative splicing during differentiation and activation of hematopoietic cells. J Cell Biochem 2003;88:1012-1024.
121. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D, et al. ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 2004;6:1-6.
122. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D, et al. Large-scale meta-analysis of cancer microarray data identifies common transcriptional profiles of neoplastic transformation and progression. Proc Natl Acad Sci USA 2004;101:9309-9314.
123. Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS, Rosenwald A, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 2000;403:503-511.
124. Rosenwald A, Wright G, Chan WC, Connors JM, Campo E, Fisher RI, et al. The use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma. N Engl J Med 2002;346:1937-1947.
125. Oncomine Cancer Microarray Database. 2005. Ref Type: Electronic Citation
126. Yeoh EJ, Ross ME, Shurtleff SA, Williams WK, Patel D, Mahfouz R, et al. Classification, subtype discovery, and prediction of outcome in pediatric acute lymphoblastic leukemia by gene expression profiling. Cancer Cell 2002;1:133-143.