Tumor cells disseminate early, but immunosurveillance limits metastatic outgrowth, in a mouse model of melanoma

Journal of Clinical Investigation

Volumn 120, Issue 6, 2010, Pages 2030-2039

  Eyles, Jo ^a   Puaux, Anne Laure ^a   Wang, Xiaojie ^a   Toh, Benjamin ^a   Prakash, Celine ^a   Hong, Michelle ^a   Tan, Tze Guan ^a   Zheng, Lin ^b   Ong, Lai Chun ^b   Jin, Yi ^b   Kato, Masashi ^c   Prévost Blondel, Armelle ^d,e   Chow, Pierce ^b,f   Yang, Henry ^a   Abastado, Jean Pierre ^a  

^a AGENCY FOR SCIENCE   (Singapore)

^b SINGAPORE GENERAL HOSPITAL   (Singapore)

^c CHUBU UNIVERSITY   (Japan)

^d INSTITUT COCHIN   (France)

^e INSERM   (France)

^f DUKE NUS MEDICAL SCHOOL   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORODEOXYGLUCOSE F 18;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER GROWTH; CELL PROLIFERATION; DISSEMINATED CANCER; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IMMUNOSURVEILLANCE; MELANOMA; METASTASIS; MOUSE; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PRIMARY TUMOR; PRIORITY JOURNAL;

ANIMALS; CELLULAR STRUCTURES; HUMANS; MELANOMA; MICE; MICE, TRANSGENIC; MONITORING, IMMUNOLOGIC; T-LYMPHOCYTES;

EID: 77953225810     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI42002     Document Type: Article

References (72)

1. Jemal A, et al. Cancer statistics, 2008. CA Cancer J Clin. 2008;58(2):71-96.
2. Pazdur R, Wagman L, Camphausen K, Hoskins W. Cancer management: a multidisciplinary approach. Huntington, New York: PRR; 2008.
3. Nguyen DX, Bos PD, Massague J. Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer. 2009;9(4):274-284.
4. Fidler IJ, Kripke ML. Metastasis results from preexisting variant cells within a malignant tumor. Science. 1977;197(4306):893-895.
5. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell. 1990;61(5):759-767.
6. Fidler IJ, Hart IR. Biological diversity in metastatic neoplasms: origins and implications. Science. 1982;217(4564):998-1003. (Pubitemid 12059094)
7. Ramaswamy S, Ross KN, Lander ES, Golub TR. A molecular signature of metastasis in primary solid tumors. Nat Genet. 2003;33(1):49-54. (Pubitemid 36068681)
8. van't Veer LJ, et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature. 2002;415(6871):530-536.
9. Sotiriou C, Piccart MJ. Taking gene-expression profiling to the clinic: when will molecular signatures become relevant to patient care? Nat Rev Cancer. 2007;7(7):545-553. (Pubitemid 46985399)
10. Desmedt C, Ruiz-Garcia E, Andre F. Gene expression predictors in breast cancer: current status, limitations and perspectives. Eur J Cancer. 2008; 44(18):2714-2720.
11. Bernards R, Weinberg RA. A progression puzzle. Nature. 2002;418(6900):823.
12. Pantel K, Brakenhoff RH. Dissecting the metastatic cascade. Nat Rev Cancer. 2004;4(6):448-456.
13. Wikman H, Vessella R, Pantel K. Cancer micrometastasis and tumour dormancy. Apmis. 2008; 116(7-8):754-770.
14. Husemann Y, et al. Systemic spread is an early step in breast cancer. Cancer Cell. 2008;13(1):58-68. (Pubitemid 350309740)
15. Dunn GP, Old LJ, Schreiber RD. The three Es of cancer immunoediting. Annu Rev Immunol. 2004;22:329-360.
16. Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Nat Med. 2004;10(9):909-915. (Pubitemid 39273730)
17. Lengagne R, et al. Distinct role for CD8 T cells toward cutaneous tumors and visceral metastases. J Immunol. 2008;180(1):130-137.
18. Iwamoto T, et al. Aberrant melanogenesis and melanocytic tumour development in transgenic mice that carry a metallothionein/ret fusion gene. EMBO J. 1991;10(11):3167-3175. (Pubitemid 21905339)
19. Dragani TA, et al. Mapping of melanoma modifier loci in RET transgenic mice. Jpn J Cancer Res. 2000;91(11):1142-1147.
20. Minn AJ, et al. Lung metastasis genes couple breast tumor size and metastatic spread. Proc Natl Acad Sci U S A. 2007;104(16):6740-6745.
21. North JH, Pack MS. Malignant tumors of the small intestine: a review of 144 cases. Am Surg. 2000;66(1):46-51.
22. Macak J. Melanoma of the stomach: reality or fiction? Pathologica. 1998;90(4):388-390. (Pubitemid 128566368)
23. Chalkiadakis G, Wihlm JM, Morand G, Weill-Bousson M, Witz JP. Primary malignant melanoma of the esophagus. Ann Thorac Surg. 1985;39(5):472-475.
24. Christova S, Meinhard K, Mihailov I, Alexiev B. Three cases of primary malignant melanoma of the alimentary tract. Gen Diagn Pathol. 1996;142(1):63-67. (Pubitemid 26167143)
25. Sachs DL, Lowe L, Chang AE, Carson E, Johnson TM. Do primary small intestinal melanomas exist? Report of a case. J Am Acad Dermatol. 1999; 41(6):1042-1044.
26. Kadivar TF, Vanek VW, Krishnan EU. Primary malignant melanoma of the small bowel: a case study. Am Surg. 1992;58(7):418-422.
27. Stranks GJ, Mathai JT, Rowe-Jones DC. Primary malignant melanoma of the oesophagus: case report and review of surgical pathology. Gut. 1991;32(7):828-830.
28. Tarantino L, et al. Primary small-bowel melanoma: color Doppler ultrasonographic, computed tomographic, and radiologic findings with pathologic correlations. J Ultrasound Med. 2007;26(1):121-127. (Pubitemid 46080085)
29. Klein CA. Parallel progression of primary tumours and metastases. Nat Rev Cancer. 2009;9(4):302-312.
30. Chin L, Garraway LA, Fisher DE. Malignant mela noma: genetics and therapeutics in the genomic era. Genes Dev. 2006;20(16):2149-2182. (Pubitemid 44244518)
31. Ulmer A, et al. Visualization of circulating melanoma cells in peripheral blood of patients with primary uveal melanoma. Clin Cancer Res. 2008;14(14):4469-4474.
32. Schuster R, et al. Circulating tumor cells as prognostic factor for distant metastases and survival in patients with primary uveal melanoma. Clin Cancer Res. 2007;13(4):1171-1178. (Pubitemid 46424057)
33. Callejo SA, Antecka E, Blanco PL, Edelstein C, Burnier MN Jr. Identification of circulating malignant cells and its correlation with prognostic factors and treatment in uveal melanoma. A prospective longitudinal study. Eye (Lond). 2007;21(6):752-759. (Pubitemid 46909176)
34. Ossowski L, Aguirre-Ghiso JA. Dormancy of metastatic melanoma. Pigment Cell Melanoma Res. 2009;23(1):41-56.
35. Mocellin S, Hoon D, Ambrosi A, Nitti D, Rossi CR. The prognostic value of circulating tumor cells in patients with melanoma: a systematic review and meta-analysis. Clin Cancer Res. 2006;12(15):4605-4613. (Pubitemid 44297811)
36. Palmieri G, et al. Prognostic value of circulating melanoma cells detected by reverse transcriptasepolymerase chain reaction. J Clin Oncol. 2003;21(5):767-773. (Pubitemid 46606433)
37. Allard WJ, et al. Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin Cancer Res. 2004;10(20):6897-6904.
38. Braun S, et al. Cytokeratin-positive cells in the bone marrow and survival of patients with stage I, II, or III breast cancer. N Engl J Med. 2000;342(8):525-533. (Pubitemid 30117892)
39. Bidard FC, et al. Disseminated tumor cells of breast cancer patients: a strong prognostic factor for distant and local relapse. Clin Cancer Res. 2008;14(11):3306-3311.
40. Meng S, et al. Circulating tumor cells in patients with breast cancer dormancy. Clin Cancer Res. 2004;10(24):8152-8162. (Pubitemid 40053373)
41. Schlimok G, et al. Micrometastatic cancer cells in bone marrow: in vitro detection with anti-cytokeratin and in vivo labeling with anti-17-1A monoclonal antibodies. Proc Natl Acad Sci U S A. 1987;84(23):8672-8676.
42. Vinokurova S, et al. Clonal history of papillomavirus-induced dysplasia in the female lower genital tract. J Natl Cancer Inst. 2005;97(24):1816-1821. (Pubitemid 43033902)
43. Buell JF, et al. Donor transmitted malignancies. Ann Transplant. 2004;9(1):53-56.
44. Milton CA, Barbara J, Cooper J, Rao M, Russell C, Russ G. The transmission of donor-derived malignant melanoma to a renal allograft recipient. Clin Transplant. 2006;20(5):547-550. (Pubitemid 44383399)
45. MacKie RM, Reid R, Junor B. Fatal melanoma transferred in a donated kidney 16 years after melanoma surgery. N Engl J Med. 2003;348(6):567-568. (Pubitemid 36159900)
46. Mihm MC Jr, Clemente CG, Cascinelli N. Tumor infiltrating lymphocytes in lymph node melanoma metastases: a histopathologic prognostic indicator and an expression of local immune response. Lab Invest. 1996;74(1):43-47. (Pubitemid 26041007)
47. Piras F, et al. The predictive value of CD8, CD4, CD68, and human leukocyte antigen-D-related cells in the prognosis of cutaneous malignant melanoma with vertical growth phase. Cancer. 2005; 104(6):1246-1254. (Pubitemid 41278960)
48. Mullins IM, et al. CXC chemokine receptor 3 expression by activated CD8+ T cells is associated with survival in melanoma patients with stage III disease. Cancer Res. 2004;64(21):7697-7701.
49. Harlin H, et al. Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res. 2009;69(7):3077-3085.
50. Hillen F, et al. Leukocyte infiltration and tumor cell plasticity are parameters of aggressiveness in primary cutaneous melanoma. Cancer Immunol Immunother. 2008;57(1):97-106. (Pubitemid 350043652)
51. Dworacki G, et al. Decreased zeta chain expression and apoptosis in CD3+ peripheral blood T lymphocytes of patients with melanoma. Clin Cancer Res. 2001;7(3 suppl):947s-957s. (Pubitemid 33600950)
52. Staibano S, et al. Tumor infiltrating lymphocytes in uveal melanoma: a link with clinical behavior? Int J Immunopathol Pharmacol. 2006;19(1):171-179.
53. Gatenby RA, Gillies RJ. A microenvironmental model of carcinogenesis. Nat Rev Cancer. 2008;8(1):56-61.
54. Norton L, Massague J. Is cancer a disease of selfseeding? Nat Med. 2006;12(8):875-878.
55. Norton L. Conceptual and practical implications of breast tissue geometry: toward a more effective, less toxic therapy. Oncologist. 2005;10(6):370-381. (Pubitemid 40993565)
56. Wall L, Burke F, Smyth JF, Balkwill F. The anti-proliferative activity of interferon-gamma on ovarian cancer: in vitro and in vivo. Gynecol Oncol. 2003;88(1 pt 2):S149-S151.
57. Chin YE, Kitagawa M, Su WC, You ZH, Iwamoto Y, Fu XY. Cell growth arrest and induction of cyclindependent kinase inhibitor p21 WAF1/CIP1 mediated by STAT1. Science. 1996;272(5262):719-722.
58. Ikeda H, Old LJ, Schreiber RD. The roles of IFN gamma in protection against tumor development and cancer immunoediting. Cytokine Growth Factor Rev. 2002;13(2):95-109. (Pubitemid 34229385)
59. Muller-Hermelink N, et al. TNFR1 signaling and IFN-gamma signaling determine whether T cells induce tumor dormancy or promote multistage carcinogenesis. Cancer Cell. 2008;13(6):507-518. (Pubitemid 351763899)
60. Koebel CM, et al. Adaptive immunity maintains occult cancer in an equilibrium state. Nature. 2007;450(7171):903-907.
61. Weir L, Speers C, D'Yachkova Y, Olivotto IA. Prognostic significance of the number of axillary lymph nodes removed in patients with node-negative breast cancer. J Clin Oncol. 2002;20(7):1793-1799. (Pubitemid 34273268)
62. Morrow M. A survival benefit from axillary dissection: was Halsted correct? Ann Surg Oncol. 1999;6(1):17-18. (Pubitemid 29077483)
63. Veronesi U, Marubini E, Mariani L, Valagussa P, Zucali R. The dissection of internal mammary nodes does not improve the survival of breast cancer patients. 30-year results of a randomised trial. Eur J Cancer. 1999;35(9):1320-1325. (Pubitemid 29397430)
64. Braun S, et al. Lack of effect of adjuvant chemotherapy on the elimination of single dormant tumor cells in bone marrow of high-risk breast cancer patients. J Clin Oncol. 2000;18(1):80-86. (Pubitemid 30036339)
65. Old LJ. Cancer vaccines: an overview. Cancer Immun. 2008;8(suppl 1):1.
66. Kato M, et al. Transgenic mouse model for skin malignant melanoma. Oncogene. 1998;17(14):1885-1888. (Pubitemid 28482792)
67. Moorhead M, et al. Optimal genotype determination in highly multiplexed SNP data. Eur J Hum Genet. 2006;14(2):207-215. (Pubitemid 43135864)
68. Olshen AB, Venkatraman ES, Lucito R, Wigler M. Circular binary segmentation for the analysis of array-based DNA copy number data. Biostatistics. 2004;5(4):557-572. (Pubitemid 41180205)
69. Venkatraman ES, Olshen AB. A faster circular binary segmentation algorithm for the analysis of array CGH data. Bioinformatics. 2007;23(6):657-663. (Pubitemid 46554715)
70. Waldman FM, DeVries S, Chew KL, Moore DH 2nd, Kerlikowske K, Ljung BM. Chromosomal alterations in ductal carcinomas in situ and their in situ recurrences. J Natl Cancer Inst. 2000;92(4):313-320. (Pubitemid 30117734)
71. Choi JH, Jung HY, Kim HS, Cho HG. PhyloDraw: a phylogenetic tree drawing system. Bioinformatics. 2000;16(11):1056-1058.
72. Felsenstein J. An alternating least squares approach to inferring phylogenies from pairwise distances. Syst Biol. 1997;46(1):101-111. (Pubitemid 127365610)