The Mucin MUC16 (CA125) Binds to NK Cells and Monocytes from Peripheral Blood of Women with Healthy Pregnancy and Preeclampsia

American Journal of Reproductive Immunology

Volumn 68, Issue 1, 2012, Pages 28-37

  Tyler, Chanel ^a   Kapur, Arvinder ^a   Felder, Mildred ^a   Belisle, Jennifer A ^a   Trautman, Christine ^a   Gubbels, Jennifer A A ^b   Connor, Joseph P ^a   Patankar, Manish S ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b AUGUSTANA COLLEGE   (United States)

Author keywords

Biomarker; CA125; Immune cell subsets; MUC16; Siglec 9

Indexed keywords

CA 125 ANTIGEN; GALECTIN 1; GLYCOPROTEIN; MUCIN MUC16; PROTEIN; SIALIC ACID DERIVATIVE; SIGLEC 9 PROTEIN; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BLOOD; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; MONOCYTE; NATURAL KILLER CELL; PREECLAMPSIA; PREGNANCY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION;

ADULT; ANTIGENS, CD; BIOLOGICAL MARKERS; CA-125 ANTIGEN; COHORT STUDIES; FEMALE; FLOW CYTOMETRY; HUMANS; KILLER CELLS, NATURAL; LECTINS; MEMBRANE PROTEINS; MONOCYTES; PRE-ECLAMPSIA; PREGNANCY; PROTEIN BINDING;

EID: 84861939403     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2012.01113.x     Document Type: Article

References (51)

1. Bast RC Jr, Feeney M, Lazarus H, Nadler LM, Colvin RB, Knapp RC: Reactivity of a monoclonal antibody with human ovarian carcinoma. J Clin Invest 1981; 68:1331-1337.
2. Bast RC Jr, Klug TL, St John E, Jenison E, Niloff JM, Lazarus H, Berkowitz RS, Leavitt T, Griffiths CT, Parker L, Zurawski VR Jr, Knapp RC: A radioimmunoassay using a monoclonal antibody to monitor the course of epithelial ovarian cancer. N Engl J Med 1983; 309:883-887.
3. Rustin GJ: Use of CA-125 to assess response to new agents in ovarian cancer trials. J Clin Oncol 2003; 21:187s-193s.
4. Yin BW, Dnistrian A, Lloyd KO: Ovarian cancer antigen CA125 is encoded by the MUC16 mucin gene. Int J Cancer 2002; 98:737-740.
5. Yin BW, Lloyd KO: Molecular cloning of the ca125 ovarian cancer antigen. Identification as a new mucin, muc16. J Biol Chem 2001; 276:27371-27375.
6. O'Brien TJ, Beard JB, Underwood LJ, Dennis RA, Santin AD, York L: The CA 125 gene: an extracellular superstructure dominated by repeat sequences. Tumour Biol 2001; 22:348-366.
7. Gubbels JA, Felder M, Horibata S, Belisle JA, Kapur A, Holden H, Petrie S, Migneault M, Rancourt C, Connor JP, Patankar MS: MUC16 provides immune protection by inhibiting synapse formation between NK and ovarian tumor cells. Mol Cancer 2010; 9:11.
8. Patankar MS, Yu J, Morrison JC, Belisle JA, Lattanzio FA, Deng Y, Wong NK, Morris HR, Dell A, Clark GF: Potent suppression of natural killer cell response mediated by the ovarian tumor marker CA125. Gynecol Oncol 2005; 99:704-713.
9. O'Brien TJ, Beard JB, Underwood LJ, Shigemasa K: The CA 125 gene: a newly discovered extension of the glycosylated N-terminal domain doubles the size of this extracellular superstructure. Tumour Biol 2002; 23:154-169.
10. Hattrup CL, Gendler SJ: Structure and function of the cell surface (tethered) mucins. Annu Rev Physiol 2007; 70:431-457.
11. Belisle JA, Horibata S, Gubbels JA, Petrie S, Kapur A, Andre S, Gabius HJ, Rancourt C, Connor J, Paulson JC, Patankar MS: Identification of Siglec-9 as the receptor for MUC16 on human NK cells, B cells, and monocytes. Mol Cancer 2010; 9:118.
12. Belisle JA, Gubbels JA, Raphael CA, Migneault M, Rancourt C, Connor JP, Patankar MS: Peritoneal natural killer cells from epithelial ovarian cancer patients show an altered phenotype and bind to the tumour marker MUC16 (CA125). Immunology 2007; 122:418-429.
13. Angata T, Varki A: Cloning, characterization and phylogenetic analysis of Siglec-9, a new member of the CD33-related group of Siglecs. Evidence for co-evolution with sialic acid synthesis pathways. J Biol Chem 2000; 275:22127-22135.
14. Yamaji T, Teranishi T, Alphey MS, Crocker PR, Hashimoto Y: A small region of the natural killer cell receptor, Siglec-7, is responsible for its preferred binding to alpha2, 8-disialyl and branched alpha2, 6-sialyl residues: a comparison with Siglec-9. J Biol Chem 2001; 10:6324-6332.
15. Zhang JQ, Nicoll G, Jones C, Crocker PR: Siglec-9, a novel sialic acid binding member of the immunoglobulin superfamily expressed broadly on human blood leukocytes. J Biol Chem 2000; 275:22121-22126.
16. Avril T, Floyd H, Lopez F, Vivier E, Crocker PR: The membrane-proximal immunoreceptor tyrosine-based inhibitory motif is critical for the inhibitory signaling mediated by Siglecs-7 and -9, CD33-related Siglecs expressed on human monocytes and NK cells. J Immunol 2004; 173:6841-6849.
17. Ikehara Y, Ikehara SK, Paulson JC: Negative regulation of T cell receptor signaling by Siglec-7 (p70/AIRM) and Siglec-9. J Biol Chem 2004; 279:43117-43125.
18. O'Brien TJ, Hardin JW, Bannon GA, Norris JS, Quirk JG Jr: CA 125 antigen in human amniotic fluid and fetal membranes. Am J Obstet Gynecol 1986; 155:50-55.
19. Quirk JG Jr, Brunson GL, Long CA, Bannon GA, Sanders MM, O'Brien TJ: CA 125 in tissues and amniotic fluid during pregnancy. Am J Obstet Gynecol 1988; 159:644-649.
20. Hardardottir H, Parmley TH 2nd, Quirk JG Jr, Sanders MM, Miller FC, O'Brien TJ: Distribution of CA 125 in embryonic tissues and adult derivatives of the fetal periderm. Am J Obstet Gynecol 1990; 163:1925-1931.
21. Niloff JM, Knapp RC, Schaetzl E, Reynolds C, Bast RC Jr: CA125 antigen levels in obstetric and gynecologic patients. Obstet Gynecol 1984; 64:703-707.
22. Bon GG, Kenemans P, Verstraeten AA, Go S, Philipi PA, van Kamp GJ, van Geijn HP, van Vugt JM: Maternal serum Ca125 and Ca15-3 antigen levels in normal and pathological pregnancy. Fetal Diagn Ther 2001; 16:166-172.
23. Sibai B, Dekker G, Kupferminc M: Pre-eclampsia. Lancet 2005; 365:785-799.
24. Goodell CAR, Belisle JA, Gubbels JAA, Migneault M, Rancourt C, Connor JP, Kunnimalaiyaan M, Kravitz R, Tucker W, Zwick M, Patankar MS: Characterization of the tumor marker Muc16 (CA125) expressed by murine ovarian tumor cell lines and identification of a panel of cross-reactive monoclonal antibodies. J Ovar Res 2009; 2:8.
25. Seki K, Kikuchi Y, Uesato T, Kato K: Increased serum CA 125 levels during the first trimester of pregnancy. Acta Obstet Gynecol Scand 1986; 65:583-585.
26. Seelenmeyer C, Wegehingel S, Lechner J, Nickel W: The cancer antigen CA125 represents a novel counter receptor for galectin-1. J Cell Sci 2003; 116:1305-1318.
27. Ahn H, Park J, Gilman-Sachs A, Kwak-Kim J: Immunologic characteristics of preeclampsia, a comprehensive review. Am J Reprod Immunol 2011; 65:377-394.
28. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, Prus D, Cohen-Daniel L, Arnon TI, Manaster I, Gazit R, Yutkin V, Benharroch D, Porgador A, Keshet E, Yagel S, Mandelboim O: Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 2006; 12:1065-1074.
29. Schrocksnadel H, Daxenbichler G, Artner E, Steckel-Berger G, Dapunt O: Tumor markers in hypertensive disorders of pregnancy. Gynecol Obstet Invest 1993; 35:204-208.
30. de Groot CJ, O'Brien TJ, Taylor RN: Biochemical evidence of impaired trophoblastic invasion of decidual stroma in women destined to have preeclampsia. Am J Obstet Gynecol 1996; 175:24-29.
31. Hollingsworth MA, Swanson BJ: Mucins in cancer: protection and control of the cell surface. Nat Rev Cancer 2004; 4:45-60.
32. Bafna S, Kaur S, Batra SK: Membrane-bound mucins: the mechanistic basis for alterations in the growth and survival of cancer cells. Oncogene 2010; 29:2893-2904.
33. Swanson BJ, McDermott KM, Singh PK, Eggers JP, Crocker PR, Hollingsworth MA: MUC1 is a counter-receptor for myelin-associated glycoprotein (Siglec-4a) and their interaction contributes to adhesion in pancreatic cancer perineural invasion. Cancer Res 2007; 67:10222-10229.
34. Iida S, Yamamoto K, Irimura T: Interaction of human macrophage C-type lectin with O-linked N- acetylgalactosamine residues on mucin glycopeptides. J Biol Chem 1999; 274:10697-10705.
35. Patankar M, Gubbels JAA, Felder M, Connor JP: Immunomodulatory properties of glycoproteins in ovarian cancer. Front Biosci 2012; 4:631-650.
36. Blalock TD, Spurr-Michaud SJ, Tisdale AS, Heimer SR, Gilmore MS, Ramesh V, Gipson IK: Functions of MUC16 in corneal epithelial cells. Invest Ophthalmol Vis Sci 2007; 48:4509-4518.
37. Gubbels JA, Belisle J, Onda M, Rancourt C, Migneault M, Ho M, Bera TK, Connor J, Sathyanarayana BK, Lee B, Pastan I, Patankar MS: Mesothelin-MUC16 binding is a high affinity, N-glycan dependent interaction that facilitates peritoneal metastasis of ovarian tumors. Mol Cancer 2006; 5:50.
38. Rump A, Morikawa Y, Tanaka M, Minami S, Umesaki N, Takeuchi M, Miyajima A: Binding of ovarian cancer antigen CA125/MUC16 to mesothelin mediates cell adhesion. J Biol Chem 2004; 279:9190-9198.
39. Chang K, Pastan I: Molecular cloning of mesothelin, a differentiation antigen present on mesothelium, mesotheliomas, and ovarian cancers. Proc Natl Acad Sci U S A 1996; 93:136-140.
40. Boivin M, Lane D, Piche A, Rancourt C: CA125 (MUC16) tumor antigen selectively modulates the sensitivity of ovarian cancer cells to genotoxic drug-induced apoptosis. Gynecol Oncol 2009; 115:407-413.
41. Reinartz S, Failer S, Schuell T, Wagner U: CA125 (MUC16) gene silencing suppresses growth properties of ovarian and breast cancer cells. Eur J Cancer 2011; (Epub ahead of print).
42. Lakshmanan I, Ponnusamy MP, Das S, Chakraborty S, Haridas D, Mukhopadhyay P, Lele SM, Batra SK: MUC16 induced rapid G2/M transition via interactions with JAK2 for increased proliferation and anti-apoptosis in breast cancer cells. Oncogene 2011; 31:805-811.
43. Gipson IK, Blalock T, Tisdale A, Spurr-Michaud S, Allcorn S, Stavreus-Evers A, Gemzell K: MUC16 is lost from the uterodome (pinopode) surface of the receptive human endometrium: in vitro evidence that MUC16 is a barrier to trophoblast adherence. Biol Reprod 2007; 78:134-142.
44. Farag SS, Caligiuri MA: Human natural killer cell development and biology. Blood Rev 2006; 20:123-137.
45. Ando M, Tu W, Nishijima K, Iijima S: Siglec-9 enhances IL-10 production in macrophages via tyrosine-based motifs. Biochem Biophys Res Commun 2008; 369:878-883.
46. Sankaralingam S, Arenas IA, Lalu MM, Davidge ST: Preeclampsia: current understanding of the molecular basis of vascular dysfunction. Expert Rev Mol Med 2006; 8:1-20.
47. Kuc S, Wortelboer EJ, van Rijn BB, Franx A, Visser GH, Schielen PC: Evaluation of 7 serum biomarkers and uterine artery Doppler ultrasound for first-trimester prediction of preeclampsia: a systematic review. Obstet Gynecol Surv 2011; 66:225-239.
48. Cuckle HS: Screening for pre-eclampsia-lessons from aneuploidy screening. Placenta 2011; 1(32 Suppl):S42-S48.
49. Romero R, Kusanovic JP, Than NG, Erez O, Gotsch F, Espinoza J, Edwin S, Chefetz I, Gomez R, Nien JK, Sammar M, Pineles B, Hassan SS, Meiri H, Tal Y, Kuhnreich I, Papp Z, Cuckle HS: First-trimester maternal serum PP13 in the risk assessment for preeclampsia. Am J Obstet Gynecol 2008; 199:122-e121.
50. Wahrenbrock MG, Varki A: Multiple hepatic receptors cooperate to eliminate secretory mucins aberrantly entering the bloodstream: are circulating cancer mucins the 'tip of the iceberg'? Cancer Res 2006; 66:2433-2441.
51. Lloyd KO, Yin BW, Kudryashov V: Isolation and characterization of ovarian cancer antigen CA 125 using a new monoclonal antibody (VK-8): identification as a mucin-type molecule. Int J Cancer 1997; 71:842-850.