Bruton tyrosine kinase–Dependent immune cell cross-talk drives pancreas cancer

Cancer Discovery

Volumn 6, Issue 3, 2016, Pages 270-285

  Gunderson, Andrew J ^a   Kaneda, Megan M ^b   Tsujikawa, Takahiro ^a,c   Nguyen, Abraham V ^b   Affara, Nesrine I ^d   Ruffell, Brian ^a   Gorjestani, Sara ^b   Liudahl, Shannon M ^a   Truit, Morgan ^d   Olson, Peter ^d   Kim, Grace ^d,e   Hanahan, Douglas ^f   Tempero, Margaret A ^d,e   Sheppard, Brett ^a,c   Irving, Bryan ^g   Chang, Betty Y ^h   Varner, Judith A ^b,i   Coussens, Lisa M ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f EPFL   (Switzerland)

^g GENENTECH INC   (United States)

^h PHARMACYCLICS INC   (United States)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BRUTON TYROSINE KINASE; CD20 ANTIGEN; FC RECEPTOR; GEMCITABINE; IBRUTINIB; IMMUNOGLOBULIN; PHOSPHATIDYLINOSITOL 3 KINASE ALPHA; PHOSPHATIDYLINOSITOL 3 KINASE GAMMA; UNCLASSIFIED DRUG; AGAMMAGLOBULINAEMIA TYROSINE KINASE; BIOLOGICAL MARKER; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CANCER INHIBITION; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXICITY; DNA MICROARRAY; ECHOGRAPHY; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; IMMUNE DEFICIENCY; IMMUNOCOMPETENT CELL; MACROPHAGE; MOUSE; NONHUMAN; PANCREAS ADENOCARCINOMA; PHENOTYPE; TH2 CELL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; WESTERN BLOTTING; ANIMAL; BONE MARROW CELL; CELL COMMUNICATION; CYTOLOGY; DISEASE COURSE; DISEASE MODEL; GENETICS; IMMUNE SYSTEM; IMMUNOLOGY; KNOCKOUT MOUSE; LEUKOCYTE; MACROPHAGE ACTIVATION; METABOLISM; PANCREAS CARCINOMA; PANCREAS TUMOR; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; B-LYMPHOCYTES; BIOMARKERS; CARCINOMA, PANCREATIC DUCTAL; CELL COMMUNICATION; CELL LINE, TUMOR; CLASS IB PHOSPHATIDYLINOSITOL 3-KINASE; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HUMANS; IMMUNE SYSTEM; LEUKOCYTES; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, KNOCKOUT; MYELOID CELLS; PANCREATIC NEOPLASMS; PROTEIN-TYROSINE KINASES; RECEPTORS, IGG; SIGNAL TRANSDUCTION;

EID: 84960124795     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-15-0827     Document Type: Article

References (51)

1. Hanahan D, Coussens LM. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 2012; 21: 309-22
2. Schmid MC, Varner JA. Myeloid cells in tumor inflammation. Vasc Cell 2012; 4: 14
3. Coussens LM, Zitvogel L, Palucka AK. Neutralizing tumor-promoting chronic inflammation: a magic bullet? Science 2013; 339: 286-91
4. SEER.cancer.gov [Internet]. Rockville: National Cancer Institute; c2015. Available from: http://seer.cancer.gov/statfacts/html/pancreas.html.
5. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012; 62: 10-29
6. Conroy T, Desseigne F, Ychou M, Bouche O, Guimbaud R, Becouarn Y, et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med 2011; 364: 1817-25
7. Von Hoff DD, Ramanathan RK, Borad MJ, Laheru DA, Smith LS, Wood TE, et al. Gemcitabine plus nab-paclitaxel is an active regimen in patients with advanced pancreatic cancer: a phase I/II trial. J Clin Oncol 2011; 29: 4548-54
8. Shibuya KC, Goel VK, Xiong W, Sham JG, Pollack SM, Leahy AM, et al. Pancreatic ductal adenocarcinoma contains an effector and regulatory immune cell infiltrate that is altered by multimodal neoadjuvant treatment. PLoS One 2014; 9: e96565
9. Affara NI, Ruffell B, Medler TR, Gunderson AJ, Johansson M, Bornstein S, et al. B cells regulate macrophage phenotype and response to chemotherapy in squamous carcinomas. Cancer Cell 2014; 25: 809-21
10. Jackson EL, Willis N, Mercer K, Bronson RT, Crowley D, Montoya R, et al. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev 2001; 15: 3243-8
11. Hingorani SR, Petricoin EF, Maitra A, Rajapakse V, King C, Jacobetz MA, et al. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 2003; 4: 437-50
12. Tuveson DA, Shaw AT, Willis NA, Silver DP, Jackson EL, Chang S, et al. Endogenous oncogenic K-ras(G12D) stimulates proliferation and widespread neoplastic and developmental defects. Cancer Cell 2004; 5: 375-87
13. Sharpless NE, Bardeesy N, Lee KH, Carrasco D, Castrillon DH, A guirre AJ, et al. Loss of p16Ink4a with retention of p19Arf predisposes mice to tumorigenesis. Nature 2001; 413: 86-91
14. Marino S, Vooijs M, van Der Gulden H, Jonkers J, Berns A. Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of Rb in the external granular layer cells of the cerebellum. Genes Dev 2000; 14: 994-1004
15. Bardeesy N, Aguirre AJ, Chu GC, Cheng KH, Lopez LV, Hezel A F, et al. Both p16(Ink4a) and the p19(Arf)-p53 pathway constrain progression of pancreatic adenocarcinoma in the mouse. Proc Natl Acad Sci U S A 2006; 103: 5947-52
16. Gu G, Dubauskaite J, Melton DA. Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 2002; 129: 2447-57
17. Chen J, Trounstine M, Alt FW, Young F, Kurahara C, Loring JF, et al. Immunoglobulin gene rearrangement in B cell deficient mice generated by targeted deletion of the JH locus. Int Immunol 1993; 5: 647-56
18. Takai T, Li M, Sylvestre D, Clynes R, Ravetch JV. FcR gamma chain deletion results in pleiotrophic effector cell defects. Cell 1994; 76: 519-29
19. Andreu P, Johansson M, Affara NI, Pucci F, Tan T, Junankar S, et al. FcRgamma activation regulates inflammation-associated squamous carcinogenesis. Cancer Cell 2010; 17: 121-34
20. Ruffell B, Chang-Strachan D, Chan V, Rosenbusch A, Ho CM, Pryer N, et al. Macrophage IL-10 blocks CD8+ T cell-dependent responses to chemotherapy by suppressing IL-12 expression in intratumoral dendritic cells. Cancer Cell 2014; 26: 623-37
21. de Gorter DJ, Beuling EA, Kersseboom R, Middendorp S, van Gils JM, Hendriks RW, et al. Bruton’s tyrosine kinase and phospholipase Cgamma2 mediate chemokine-controlled B cell migration and homing . Immunity 2007; 26: 93-104
22. Hendriks RW, Yuvaraj S, Kil LP. Targeting Bruton’s tyrosine kinase in B cell malignancies. Nat Rev Cancer 2014; 14: 219-32
23. DeNardo DG, Brennan DJ, Rexhepaj E, Ruffell B, Shiao SL, Madden SF, et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov 2011; 1: 54-67
24. Schmid MC, Franco I, Kang SW, Hirsch E, Quilliam LA, Varner JA. PI3-kinase gamma promotes Rap1a-mediated activation of myeloid cell integrin alpha4beta1, leading to tumor inflammation and growth. PLoS One 2013; 8: e60226
25. Schmid MC, Avraamides CJ, Dippold HC, Franco I, Foubert P, Ellies LG, et al. Receptor tyrosine kinases and TLR/IL1Rs unexpectedly activate myeloid cell PI3Kgamma, a single convergent point promoting tumor inflammation and progression. Cancer Cell 2011; 19: 715-27
26. Schmid MC, Avraamides CJ, Foubert P, Shaked Y, Kang SW, Kerbel RS, et al. Combined blockade of integrin-alpha4beta1 plus cytokines SDF-1alpha or IL-1beta potently inhibits tumor inflammation and growth. Cancer Res 2011; 71: 6965-75
27. Dangi-Garimella S. FDA grants accelerated approval for ibrutinib for CLL. Am J Manag Care 2014; 20: SP145
28. Palanki MS, Dneprovskaia E, Doukas J, Fine RM, Hood J, Kang X, et al. Discovery of 3,3′-(2,4-diaminopteridine-6,7-diyl)diphenol as an isozyme-selective inhibitor of PI3K for the treatment of ischemia reperfusion injury associated with myocardial infarction. J Med Chem 2007; 50: 4279-94
29. Bonecchi R, Sozzani S, Stine JT, Luini W, D’Amico G, Allavena P, et al. Divergent effects of interleukin-4 and interferon-gamma on macrophage-derived chemokine production: an amplification circuit of polarized T helper 2 responses. Blood 1998; 92: 2668-71
30. Biswas SK, Gangi L, Paul S, Schioppa T, Saccani A, Sironi M, et al. A distinct and unique transcriptional program expressed by tumorassociated macrophages (defective NF-kappaB and enhanced IRF-3/ STAT1 activation). Blood 2006; 107: 2112-22
31. Benson MJ, Rodriguez V, von Schack D, Keegan S, Cook TA, Edmonds J, et al. Modeling the clinical phenotype of BTK inhibition in the mature murine immune system. J Immunol 2014; 193: 185-97
32. Pylayeva-Gupta Y, Lee KE, Hajdu CH, Miller G, Bar-Sagi D. Oncogenic Kras-induced GM-CSF production promotes the development of pancreatic neoplasia. Cancer Cell 2012; 21: 836-47
33. Keenan BP, Saenger Y, Kafrouni MI, Leubner A, Lauer P, Maitra A, et al. A Listeria vaccine and depletion of T-regulatory cells activate immunity against early stage pancreatic intraepithelial neoplasms and prolong survival of mice. Gastroenterology 2014; 146: 1784-94 e6
34. Beatty GL, Chiorean EG, Fishman MP, Saboury B, Teitelbaum UR, Sun W, et al. CD40 agonists alter tumor stroma and show effi- cacy against pancreatic carcinoma in mice and humans. Science 2011; 331: 1612-6
35. Twyman-Saint Victor C, Rech AJ, Maity A, Rengan R, Pauken KE, Stelekati E, et al. Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature 2015; 520: 373-7
36. Sagiv-BarfiI, Kohrt HE, Czerwinski DK, Ng PP, Chang BY, Levy R. Therapeutic antitumor immunity by checkpoint blockade is enhanced by ibrutinib, an inhibitor of both BTK and ITK. Proc Natl Acad Sci U S A 2015; 112: E966-72
37. Masso-Valles D, Jauset T, Serrano E, Sodir NM, Pedersen K, Affara NI, et al. Ibrutinib exerts potent antifibrotic and antitumor activities in mouse models of pancreatic adenocarcinoma. Cancer Res 2015; 75: 1675-81
38. Schioppa T, Moore R, Thompson RG, Rosser EC, Kulbe H, Nedospasov S, et al. B regulatory cells and the tumor-promoting actions of TNF-alpha during squamous carcinogenesis. Proc Natl Acad Sci U S A 2011; 108: 10662-7
39. Wong SC, Puaux AL, Chittezhath M, Shalova I, Kajiji TS, Wang X, et al. Macrophage polarization to a unique phenotype driven by B cells. Eur J Immunol 2010; 40: 2296-307
40. Woo JR, Liss MA, Muldong MT, Palazzi K, Strasner A, Ammirante M, et al. Tumor infiltrating B-cells are increased in prostate cancer tissue. J Transl Med 2014; 12: 30
41. Ammirante M, Luo JL, Grivennikov S, Dedospasov S, Karin M. B-cellderived lymphotoxin promotes castration-resistant prostate cancer. Nature 2010; 464: 302-6
42. Shalapour S, Font-Burgada J, Di Caro G, Zhong Z, Sanchez-Lopez E, Dhar D, et al. Immunosuppressive plasma cells impede T-celldependent immunogenic chemotherapy. Nature 2015; 521: 94-8
43. Inoue S, Leitner WW, Golding B, Scott D. Inhibitory effects of B cells on antitumor immunity. Cancer Res 2006; 66: 7741-7
44. Pylayeva-Gupta Y, Das S, Handler JS, Hajdu CH, Coffre M, Koralov S, et al. IL35-producing B cells promote the development of pancreatic neoplasia. Cancer Discov 2016;6:247–55
45. Lee KE, Spata M, Bayne LJ, Buza EL, Durham AC, Allman D, et al. HIF1a deletion reveals pro-neoplastic function of B cells in pancreatic neoplasia. Cancer Discov 2016;6:256–69
46. S istigu A, Yamazaki T, Vacchelli E, Chaba K, Enot DP, Adam J, et al. Cancer cell-autonomous contribution of type I interferon signaling to the efficacy of chemotherapy. Nat Med 2014; 20: 1301-9
47. Xue J, Sharma V, Hsieh MH, Chawla A, Murali R, Pandol SJ, et al. Alternatively activated macrophages promote pancreatic fibrosis in chronic pancreatitis. Nat Commun 2015; 6: 7158
48. Lemos DR, Babaeijandaghi F, Low M, Chang CK, Lee ST, Fiore D, et al. Nilotinib reduces muscle fibrosis in chronic muscle injury by promoting TNF-mediated apoptosis of fibro/adipogenic progenitors. Nat Med 2015; 21: 786-94
49. Lin EY, Nguyen AV, Russell RG, Pollard JW. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J Exp Med 2001; 193: 727-40
50. DeNardo DG, Barreto JB, Andreu P, Vasquez L, Tawfik D, Kolhatkar N, et al. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 2009; 16: 91-102
51. Gocheva V, Wang HW, Gadea BB, Shree T, Hunter KE, Garfall A L, et al. IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Genes Dev 2010; 24: 241-55.