NKp44 and NKp30 splice variant profiles in decidua and tumor tissues: A comparative viewpoint

Oncotarget

Volumn 7, Issue 43, 2016, Pages 70912-70923

  Shemesh, Avishai ^a   Kugel, Aleksandra ^a   Steiner, Naama ^b   Yezersky, Michal ^b   Tirosh, Dan ^b   Edri, Avishay ^a   Teltsh, Omri ^a   Rosental, Benyamin ^c   Sheiner, Eyal ^b   Rubin, Eitan ^a   Campbell, Kerry S ^d   Porgador, Angel ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d FOX CHASE CANCER CENTER   (United States)

Author keywords

Decidua; Microenvironment; NKp30; NKp44; Tumor

Indexed keywords

NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 2; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; IL15 PROTEIN, HUMAN; INTERLEUKIN 15; INTERLEUKIN 18; INTERLEUKIN 18 PROTEIN, HUMAN; NCR2 PROTEIN, HUMAN; NCR3 PROTEIN, HUMAN; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; CANCER TISSUE; CONTROLLED STUDY; DECIDUA; HUMAN; HUMAN TISSUE; PREECLAMPSIA; PREGNANCY; PROTEIN EXPRESSION; SPONTANEOUS ABORTION; TISSUE SPECIFICITY; COMPARATIVE STUDY; FEMALE; FLOW CYTOMETRY; GENETICS; IMMUNE PRIVILEGE; IMMUNOLOGY; METABOLISM; NATURAL KILLER CELL; NEOPLASM; PATHOLOGY; RNA SPLICING; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT;

ABORTION, SPONTANEOUS; DECIDUA; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNE PRIVILEGE; INTERLEUKIN-15; INTERLEUKIN-18; KILLER CELLS, NATURAL; LYMPHOCYTES, TUMOR-INFILTRATING; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 2; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; NEOPLASMS; PRE-ECLAMPSIA; PREGNANCY; RNA SPLICING; TRANSFORMING GROWTH FACTOR BETA; TUMOR MICROENVIRONMENT;

EID: 84994344526     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.12292     Document Type: Article

References (43)

1. Hudspeth K, Silva-Santos B, Mavilio D. Natural cytotoxicity receptors: broader expression patterns and functions in innate and adaptive immune cells. Frontiers in immunology. 2013; 4: 69.
2. Kruse PH, Matta J, Ugolini S, Vivier E. Natural cytotoxicity receptors and their ligands. Immunology and cell biology. 2014; 92: 221-229.
3. Huret J, Senon S. Atlas of genetics and cytogenetics in oncology and haematology. 2006.
4. Shemesh A, Brusilovsky M, Hadad U, Teltsh O, Edri A, Rubin E, Campbell KS, Rosental B, Porgador A. Survival in acute myeloid leukemia is associated with NKp44 splice variants. Oncotarget. 2016; 7: 32933-32945. doi: 10.18632/oncotarget.8782.
5. Rosental B, Brusilovsky M, Hadad U, Oz D, Appel MY, Afergan F, Yossef R, Rosenberg LA, Aharoni A, Cerwenka A, Campbell KS, Braiman A, Porgador A. Proliferating cell nuclear antigen is a novel inhibitory ligand for the natural cytotoxicity receptor NKp44. Journal of immunology (Baltimore, Md.: 1950). 2011; 187: 5693-5702.
6. Kopcow HD, Allan DS, Chen X, Rybalov B, Andzelm MM, Ge B, Strominger JL. Human decidual NK cells form immature activating synapses and are not cytotoxic. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102: 15563-15568.
7. Marlin R, Duriez M, Berkane N, de Truchis C, Madec Y, Rey-Cuille M, Cummings J, Cannou C, Quillay H, Barré-Sinoussi F. Dynamic shift from CD85j/ILT-2 to NKG2D NK receptor expression pattern on human decidual NK during the first trimester of pregnancy. PLoS One. 2012; 7: e30017.
8. Delahaye NF, Rusakiewicz S, Martins I, Ménard C, Roux S, Lyonnet L, Paul P, Sarabi M, Chaput N, Semeraro M. Alternatively spliced NKp30 isoforms affect the prognosis of gastrointestinal stromal tumors. Nature medicine. 2011; 17: 700-707.
9. Messaoudene M, Fregni G, Enot D, Jacquelot N, Neves E, Germaud N, Garchon HJ, Boukouaci W, Tamouza R, Chanal J. NKp30 isoforms and NKp46 transcripts in metastatic melanoma patients: unique NKp30 pattern in rare melanoma patients with favorable evolution. OncoImmunology. 2016: 00-00.
10. Mantovani S, Mele D, Oliviero B, Barbarini G, Varchetta S, Mondelli MU. NKp30 isoforms in patients with chronic hepatitis C virus infection. Immunology. 2015; 146: 234-242.
11. Prada N, Antoni G, Commo F, Rusakiewicz S, Semeraro M, Boufassa F, Lambotte O, Meyer L, Gougeon M, Zitvogel L. Analysis of NKp30/NCR3 isoforms in untreated HIV-1-infected patients from the ANRS SEROCO cohort. Oncoimmunology. 2013; 2: e23472.
12. Shemesh A, Tirosh D, Sheiner E, Tirosh NB, Brusilovsky M, Segev R, Rosental B, Porgador A. First Trimester Pregnancy Loss and the Expression of Alternatively Spliced NKp30 Isoforms in Maternal Blood and Placental Tissue. Frontiers in immunology. 2015; 6: 189.
13. Mochizuki M, Maruo T, Matsuo H, Samoto T, Ishihara N. Biology of human trophoblast. International Journal of Gynecology & Obstetrics. 1998; 60: S21-S28.
14. Stuart-Harris R, Caldas C, Pinder S, Pharoah P. Proliferation markers and survival in early breast cancer: a systematic review and meta-analysis of 85 studies in 32,825 patients. The Breast. 2008; 17: 323-334.
15. Holtan SG, Creedon DJ, Haluska P, Markovic SN. Cancer and pregnancy: parallels in growth, invasion, and immune modulation and implications for cancer therapeutic agents. 2009; 84: 985-1000.
16. Levi I, Amsalem H, Nissan A, Darash-Yahana M, Peretz T, Mandelboim O, Rachmilewitz J. Characterization of tumor infiltrating natural killer cell subset. Oncotarget. 2015; 6: 13835-13843. doi: 10.18632/oncotarget.3453.
17. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, Prus D, Cohen-Daniel L, Arnon TI, Manaster I et al. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nature medicine. 2006; 12: 1065-1074.
18. Cerdeira AS, Rajakumar A, Royle CM, Lo A, Husain Z, Thadhani RI, Sukhatme VP, Karumanchi SA, Kopcow HD. Conversion of peripheral blood NK cells to a decidual NK-like phenotype by a cocktail of defined factors. Journal of immunology (Baltimore, Md.: 1950). 2013; 190: 3939-3948.
19. Keskin DB, Allan DS, Rybalov B, Andzelm MM, Stern JN, Kopcow HD, Koopman LA, Strominger JL. TGFbeta promotes conversion of CD16+ peripheral blood NK cells into CD16-NK cells with similarities to decidual NK cells. Proceedings of the National Academy of Sciences of the United States of America. 2007; 104: 3378-3383.
20. Hasmim M, Messai Y, Ziani L, Thiery J, Bouhris J, Noman MZ, Chouaib S. Critical role of tumor microenvironment in shaping NK cell functions: implication of hypoxic stress. Frontiers in immunology. 2015; 6.
21. Hershkovitz O, Jivov S, Bloushtain N, Zilka A, Landau G, Bar-Ilan A, Lichtenstein RG, Campbell KS, van Kuppevelt TH, Porgador A. Characterization of the recognition of tumor cells by the natural cytotoxicity receptor, NKp44. Biochemistry. 2007; 46: 7426-7436.
22. Hershkovitz O, Jarahian M, Zilka A, Bar-Ilan A, Landau G, Jivov S, Tekoah Y, Glicklis R, Gallagher JT, Hoffmann SC, Zer H, Mandelboim O, Watzl C, et al. Altered glycosylation of recombinant NKp30 hampers binding to heparan sulfate: a lesson for the use of recombinant immunoreceptors as an immunological tool. Glycobiology. 2008; 18: 28-41.
23. Rosental B, Hadad U, Brusilovsky M, Campbell KS, Porgador A. A novel mechanism for cancer cells to evade immune attack by NK cells: The interaction between NKp44 and proliferating cell nuclear antigen. Oncoimmunology. 2012; 1: 572-574.
24. Rajagopalan S, Long EO. Found: a cellular activating ligand for NKp44. Blood. 2013; 122: 2921-2922.
25. Brandt CS, Baratin M, Yi EC, Kennedy J, Gao Z, Fox B, Haldeman B, Ostrander CD, Kaifu T, Chabannon C, Moretta A, West R, Xu W, et al. The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer cell receptor NKp30 in humans. The Journal of experimental medicine. 2009; 206: 1495-1503.
26. Siewiera J, Gouilly J, Hocine H, Cartron G, Levy C, Al-Daccak R, Jabrane-Ferrat N. Natural cytotoxicity receptor splice variants orchestrate the distinct functions of human natural killer cell subtypes. Nature communications. 2015; 6.
27. Fraser R, Whitley GSJ, Thilaganathan B, Cartwright JE. Decidual natural killer cells regulate vessel stability: implications for impaired spiral artery remodelling. Journal of reproductive immunology. 2015; 110: 54-60.
28. Kanzaki H. Uterine Endometrial Function. Springer. 2016.
29. Rosinsky C, Antony PA. A role for pre-mNK cells in tumor progression. Journal for immunotherapy of cancer. 2016; 4: 1.
30. Carrega P, Morandi B, Costa R, Frumento G, Forte G, Altavilla G, Ratto GB, Mingari MC, Moretta L, Ferlazzo G. Natural killer cells infiltrating human nonsmall-cell lung cancer are enriched in CD56brightCD16-cells and display an impaired capability to kill tumor cells. Cancer. 2008; 112: 863-875.
31. Mamessier E, Sylvain A, Thibult ML, Houvenaeghel G, Jacquemier J, Castellano R, Goncalves A, Andre P, Romagne F, Thibault G, Viens P, Birnbaum D, Bertucci F, et al. Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. The Journal of clinical investigation. 2011; 121: 3609-3622.
32. Gillard-Bocquet M, Caer C, Cagnard N, Crozet L, Perez M, Fridman WH, Sautès-Fridman C, Cremer I. Lung tumor microenvironment induces specific gene expression signature in intratumoral NK cells. Frontiers in immunology. 2013; 4: 19.
33. Takayama T, Kamada N, Chinen H, Okamoto S, Kitazume MT, Chang J, Matuzaki Y, Suzuki S, Sugita A, Koganei K. Imbalance of NKp44 NKp46-and NKp44-NKp46 natural killer cells in the intestinal mucosa of patients with Crohn's disease. Gastroenterology. 2010; 139: 882-892. e3.
34. Reeves RK, Rajakumar PA, Evans TI, Connole M, Gillis J, Wong FE, Kuzmichev YV, Carville A, Johnson RP. Gut inflammation and indoleamine deoxygenase inhibit IL-17 production and promote cytotoxic potential in NKp44+ mucosal NK cells during SIV infection. Blood. 2011; 118: 3321-3330.
35. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC bioinformatics. 2011; 12: 1.
36. Platonova S, Cherfils-Vicini J, Damotte D, Crozet L, Vieillard V, Validire P, Andre P, Dieu-Nosjean MC, Alifano M, Regnard JF, Fridman WH, Sautes-Fridman C, Cremer I. Profound coordinated alterations of intratumoral NK cell phenotype and function in lung carcinoma. Cancer research. 2011; 71: 5412-5422.
37. Horton NC, Mathew SO, Mathew PA. Novel interaction between proliferating cell nuclear antigen and HLA I on the surface of tumor cells inhibits NK cell function through NKp44. PloS one. 2013; 8: e59552.
38. Fuchs A, Cella M, Kondo T, Colonna M. Paradoxic inhibition of human natural interferon-producing cells by the activating receptor NKp44. Blood. 2005; 106: 2076-2082.
39. Bashiri A, Shemesh A, Porgador A, Holcberg G, Kabessa M. New Frontiers in RPL Research and Treatment In: Anonymous Recurrent Pregnancy Loss. Springer. 2016: 185-202.
40. Candido EB, Silva LM, Carvalho AT, Lamaita RM, Filho RM, Cota BD, da Silva-Filho AL. Immune response evaluation through determination of type 1, type 2, and type 17 patterns in patients with epithelial ovarian cancer. Reproductive sciences (Thousand Oaks, Calif.). 2013; 20: 828-837.
41. De Simone V, Franze E, Ronchetti G, Colantoni A, Fantini M, Di Fusco D, Sica G, Sileri P, MacDonald T, Pallone F. Th17-type cytokines, IL-6 and TNF-α synergistically activate STAT3 and NF-kB to promote colorectal cancer cell growth. Oncogene. 2015; 34: 3493-3503.
42. Seruga B, Zhang H, Bernstein LJ, Tannock IF. Cytokines and their relationship to the symptoms and outcome of cancer. Nature Reviews Cancer. 2008; 8: 887-899.
43. Garzetti GG, Ciavattini A, Goteri G, Tranquilli AL, Muzzioli M, Fabris N, De Nictolis M, Romanini C. Natural killer cell activity in stage I endometrial carcinoma: correlation with nuclear grading, myometrial invasion, and immunoreactivity of proliferating cell nuclear antigen. Gynecologic oncology. 1994; 55: 111-114.