A 3D matrix platform for the rapid generation of therapeutic anti-human carcinoma monoclonal antibodies

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 41, 2014, Pages 14882-14887

  Dudley, David T ^a   Li, Xiao Yan ^a   Hu, Casey Y ^a   Kleer, Celina G ^b   Willis, Amanda L ^a   Weiss, Stephen J ^a  

^a Life Sciences Institute   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Bone; Extracellular matrix; MDA MB 231; Metastasis; Mouse model

Indexed keywords

ALPHA2 INTEGRIN; MONOCLONAL ANTIBODY; TRANSCRIPTOME; TUMOR ANTIGEN;

ANIMAL; BONE TUMOR; BREAST TUMOR; CELL PROLIFERATION; CHICKEN; CONTRAST MEDIUM EXTRAVASATION; DRUG SCREENING; FEMALE; GENETICS; HUMAN; IMMUNOASSAY; IMMUNOLOGY; METABOLISM; NUDE MOUSE; PATHOLOGY; PROCEDURES; SECONDARY; TUMOR CELL LINE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, NEOPLASM; BONE NEOPLASMS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CHICKENS; EXTRAVASATION OF DIAGNOSTIC AND THERAPEUTIC MATERIALS; FEMALE; HUMANS; IMMUNOASSAY; INTEGRIN ALPHA2; MICE, NUDE; TRANSCRIPTOME; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84907899169     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1410996111     Document Type: Article

References (72)

1. Rowe RG, Weiss SJ (2008) Breaching the basement membrane: Who, when and how? Trends Cell Biol 18(11):560-574.
2. Rowe RG, Weiss SJ (2009) Navigating ECM barriers at the invasive front: The cancer cell-stroma interface. Annu Rev Cell Dev Biol 25:567-595.
3. Cheung KJ, Gabrielson E, Werb Z, Ewald AJ (2013) Collective invasion in breast cancer requires a conserved basal epithelial program. Cell 155(7):1639-1651.
4. Lyons TR, et al. (2011) Postpartum mammary gland involution drives progression of ductal carcinoma in situ through collagen and COX-2. Nat Med 17(9):1109-1115.
5. Nguyen-Ngoc KV, et al. (2012) ECM microenvironment regulates collective migration and local dissemination in normal and malignant mammary epithelium. Proc Natl Acad Sci USA 109(39):E2595-E2604.
6. Egeblad M, Rasch MG, Weaver VM (2010) Dynamic interplay between the collagen scaffold and tumor evolution. Curr Opin Cell Biol 22(5):697-706.
7. Lu P, Weaver VM, Werb Z (2012) The extracellular matrix: A dynamic niche in cancer progression. J Cell Biol 196(4):395-406.
8. Barkan D, et al. (2010) Metastatic growth from dormant cells induced by a col-I-enriched fibrotic environment. Cancer Res 70(14):5706-5716.
9. Cox TR, et al. (2013) LOX-mediated collagen crosslinking is responsible for fibrosis-enhanced metastasis. Cancer Res 73(6):1721-1732.
10. Salo S, et al. (2013) Human bone marrow mesenchymal stem cells induce collagen production and tongue cancer invasion. PLoS ONE 8(10):e77692.
11. Levental KR, et al. (2009) Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139(5):891-906.
12. Naba A, Clauser KR, Lamar JM, Carr SA, Hynes RO (2014) Extracellular matrix signatures of human mammary carcinoma identify novel metastasis promoters. eLife 3:e01308.
13. Swinney DC, Anthony J (2011) How were new medicines discovered? Nat Rev Drug Discov 10(7):507-519.
14. Sliwkowski MX, Mellman I (2013) Antibody therapeutics in cancer. Science 341(6151):1192-1198.
15. Rust S, et al. (2013) Combining phenotypic and proteomic approaches to identify membrane targets in a "triple negative" breast cancer cell type. Mol Cancer 12:11.
16. Sabeh F, Shimizu-Hirota R, Weiss SJ (2009) Protease-dependent versus -independent cancer cell invasion programs: Three-dimensional amoeboid movement revisited. J Cell Biol 185(1):11-19.
17. Kang Y, et al. (2003) A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3(6):537-549.
18. Bos PD, et al. (2009) Genes that mediate breast cancer metastasis to the brain. Nature 459(7249):1005-1009.
19. Minn AJ, et al. (2005) Genes that mediate breast cancer metastasis to lung. Nature 436(7050):518-524.
20. Hotary KB, et al. (2003) Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell 114(1):33-45.
21. Sabeh F, et al. (2004) Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J Cell Biol 167(4):769-781.
22. Ota I, Li XY, Hu Y, Weiss SJ (2009) Induction of a MT1-MMP - and MT2-MMP-dependent basement membrane transmigration program in cancer cells by Snail1. Proc Natl Acad Sci USA 106(48):20318-20323.
23. Koop S, et al. (1996) Independence of metastatic ability and extravasation: Metastatic ras-transformed and control fibroblasts extravasate equally well. Proc Natl Acad Sci USA 93(20):11080-11084.
24. Tang Y, et al. (2013) MT1-MMP-dependent control of skeletal stem cell commitment via a β1-integrin/YAP/TAZ signaling axis. Dev Cell 25(4):402-416.
25. Maller O, Martinson H, Schedin P (2010) Extracellular matrix composition reveals complex and dynamic stromal-epithelial interactions in the mammary gland. J Mammary Gland Biol Neoplasia 15(3):301-318.
26. Ibaragi S, et al. (2011) Induction of MMP-13 expression in bone-metastasizing cancer cells by type I collagen through integrin α1β1 and α2β1-p38 MAPK signaling. Anti-cancer Res 31(4):1307-1313.
27. Lundström A, Holmbom J, Lindqvist C, Nordström T (1998) The role of alpha2beta1 and alpha3beta1 integrin receptors in the initial anchoring of MDA-MB-231 human breast cancer cells to cortical bone matrix. Biochem Biophys Res Commun 250(3):735-740.
28. van der Pluijm, et al. (1997) Attachment characteristics and involvement of integrins in adhesion of breast cancer cell lines to extracellular bone matrix components. Lab Invest 77(6):665-675.
29. Emsley J, Knight CG, Farndale RW, Barnes MJ, Liddington RC (2000) Structural basis of collagen recognition by integrin alpha2beta1. Cell 101(1):47-56.
30. Leitinger B (2011) Transmembrane collagen receptors. Annu Rev Cell Dev Biol 27:265-290.
31. Kurosawa G, et al. (2008) Comprehensive screening for antigens overexpressed on carcinomas via isolation of human mAbs that may be therapeutic. Proc Natl Acad Sci USA 105(20):7287-7292.
32. Kurosawa G, et al. (2011) Selection and analysis of anti-cancer antibodies for cancer therapy obtained from antibody phage library. Cancer Sci 102(1):175-181.
33. Harunaga JS, Yamada KM (2011) Cell-matrix adhesions in 3D. Matrix Biol 30(7-8):363-368.
34. Willis AL, Sabeh F, Li XY, Weiss SJ (2013) Extracellular matrix determinants and the regulation of cancer cell invasion stratagems. J Microsc 251(3):250-260.
35. Gill BJ, et al. (2012) A synthetic matrix with independently tunable biochemistry and mechanical properties to study epithelial morphogenesis and EMT in a lung adenocarcinoma model. Cancer Res 72(22):6013-6023.
36. Grzesiak JJ, Vargas F, Bouvet M (2010) Divalent cations modulate alpha2beta1 integrin-mediated malignancy in a novel 3-dimensional in vitro model of pancreatic cancer. Pancreas 39(6):904-912.
37. Hall CL, Dai J, van Golen KL, Keller ET, Long MW (2006) Type I collagen receptor (alpha 2 beta 1) signaling promotes the growth of human prostate cancer cells within the bone. Cancer Res 66(17):8648-8654.
38. Hall CL, et al. (2008) Type I collagen receptor (alpha2beta1) signaling promotes prostate cancer invasion through RhoC GTPase. Neoplasia 10(8):797-803.
39. Kirkland SC (2009) Type I collagen inhibits differentiation and promotes a stem cell-like phenotype in human colorectal carcinoma cells. Br J Cancer 101(2):320-326.
40. Kirkland SC, Ying H (2008) Alpha2beta1 integrin regulates lineage commitment in multipotent human colorectal cancer cells. J Biol Chem 283(41):27612-27619.
41. Kostenuik PJ, Sanchez-Sweatman O, Orr FW, Singh G (1996) Bone cell matrix promotes the adhesion of human prostatic carcinoma cells via the alpha 2 beta 1 integrin. Clin Exp Metastasis 14(1):19-26.
42. Li X, et al. (2013) Lung cancer cells that survive ionizing radiation show increased integrin α2β1- and EGFR-dependent invasiveness. PLoS ONE 8(8):e70905.
43. Lochter A, Navre M, Werb Z, Bissell MJ (1999) alpha1 and alpha2 integrins mediate invasive activity of mouse mammary carcinoma cells through regulation of stromelysin-1 expression. Mol Biol Cell 10(2):271-282.
44. Shield K, et al. (2007) Alpha2beta1 integrin affects metastatic potential of ovarian carcinoma spheroids by supporting disaggregation and proteolysis. J Carcinog 6:11.
45. Vallés AM, Boyer B, Tarone G, Thiery JP (1996) Alpha 2 beta 1 integrin is required for the collagen- and FGF-1-induced cell dispersion in a rat bladder carcinoma cell line. Cell Adhes Commun 4(3):187-199.
46. Van Slambrouck S, Jenkins AR, Romero AE, Steelant WF (2009) Reorganization of the integrin alpha2 subunit controls cell adhesion and cancer cell invasion in prostate cancer. Int J Oncol 34(6):1717-1726.
47. Vuoriluoto K, Högnäs G, Meller P, Lehti K, Ivaska J (2011) Syndecan-1 and -4 differentially regulate oncogenic K-ras-dependent cell invasion into collagen through α2β1 integrin and MT1-MMP. Matrix Biol 30(3):207-217.
48. Yang C, et al. (2003) Integrin alpha1beta1 and alpha2beta1 are the key regulators of hepatocarcinoma cell invasion across the fibrotic matrix microenvironment. Cancer Res 63(23):8312-8317.
49. Ramirez NE, et al. (2011) The α2β1 integrin is a metastasis suppressor in mouse models and human cancer. J Clin Invest 121(1):226-237.
50. Chan BM, Matsuura N, Takada Y, Zetter BR, Hemler ME (1991) In vitro and in vivo consequences of VLA-2 expression on rhabdomyosarcoma cells. Science 251(5001):1600-1602.
51. Kato H, et al. (2012) The primacy of β1 integrin activation in the metastatic cascade. PLoS ONE 7(10):e46576.
52. Sottnik JL, et al. (2013) Integrin alpha2beta 1 (α2β1) promotes prostate cancer skeletal metastasis. Clin Exp Metastasis 30(5):569-578.
53. van der Bij GJ, et al. (2008) Blocking alpha2 integrins on rat CC531s colon carcinoma cells prevents operation-induced augmentation of liver metastases outgrowth. Hepatology 47(2):532-543.
54. Tran T, et al. (2011) Loss of the α2β1 integrin alters human papilloma virus-induced squamous carcinoma progression in vivo and in vitro. PLoS ONE 6(10):e26858.
55. Reticker-Flynn NE, et al. (2012) A combinatorial extracellular matrix platform identifies cell-extracellular matrix interactions that correlate with metastasis. Nat Commun 3:1122.
56. Vuoristo M, et al. (2007) Increased gene expression levels of collagen receptor integrins are associated with decreased survival parameters in patients with advanced melanoma. Melanoma Res 17(4):215-223.
57. Veit G, et al. (2011) Collagen XXIII, novel ligand for integrin alpha2beta1 in the epidermis. J Biol Chem 286(31):27804-27813.
58. Nieuwenhuis HK, Akkerman JW, Houdijk WP, Sixma JJ (1985) Human blood platelets showing no response to collagen fail to express surface glycoprotein Ia. Nature 318(6045):470-472.
59. Blumbach K, et al. (2012) Dwarfism in mice lacking collagen-binding integrins α2β1 and α11β1 is caused by severely diminished IGF-1 levels. J Biol Chem 287(9):6431-6440.
60. Chen J, Diacovo TG, Grenache DG, Santoro SA, Zutter MM (2002) The alpha(2) integrin subunit-deficient mouse: A multifaceted phenotype including defects of branching morphogenesis and hemostasis. Am J Pathol 161(1):337-344.
61. Holtkötter O, et al. (2002) Integrin alpha 2-deficient mice develop normally, are fertile, but display partially defective platelet interaction with collagen. J Biol Chem 277(13):10789-10794.
62. Halland N, Blum H, Buning C, Kohlmann M, Lindenschmidt A (2014) Small macrocycles as highly active integrin α2β1 antagonists. ACS Med Chem Lett 5(2):193-198.
63. Miller MW, et al. (2009) Small-molecule inhibitors of integrin alpha2beta1 that prevent pathological thrombus formation via an allosteric mechanism. Proc Natl Acad Sci USA 106(3):719-724.
64. Borza CM, et al. (2012) Inhibition of integrin α2β1 ameliorates glomerular injury. J Am Soc Nephrol 23(6):1027-1038.
65. Grenache DG, et al. (2007) Wound healing in the alpha2beta1 integrin-deficient mouse: Altered keratinocyte biology and dysregulated matrix metalloproteinase expression. J Invest Dermatol 127(2):455-466.
66. He L, et al. (2003) The contributions of the alpha 2 beta 1 integrin to vascular thrombosis in vivo. Blood 102(10):3652-3657.
67. Peters MA, et al. (2012) The loss of α2β1 integrin suppresses joint inflammation and cartilage destruction in mouse models of rheumatoid arthritis. Arthritis Rheum 64(5):1359-1368.
68. San Antonio JD, et al. (2009) A key role for the integrin alpha2beta1 in experimental and developmental angiogenesis. Am J Pathol 175(3):1338-1347.
69. Schiro JA, et al. (1991) Integrin alpha 2 beta 1 (VLA-2) mediates reorganization and contraction of collagen matrices by human cells. Cell 67(2):403-410.
70. Zweers MC, et al. (2007) Integrin alpha2beta1 is required for regulation of murine wound angiogenesis but is dispensable for reepithelialization. J Invest Dermatol 127(2):467-478.
71. Quante M, et al. (2011) Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell 19(2):257-272.
72. Naba A, et al. (2014) Extracellular matrix signatures of human primary metastatic colon cancers and their metastases to liver. BMC Cancer 14:518.