Mechanisms of cancer cell dormancy-another hallmark of cancer?

Cancer Research

Volumn 75, Issue 23, 2015, Pages 5014-5022

  Yeh, Albert C ^a,b   Ramaswamy, Sridhar ^a,b,c,d,e  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d HARVARD STEM CELL INSTITUTE   (United States)

^e HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; COLONY STIMULATING FACTOR 1; CYCLIN D; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLIN DEPENDENT KINASE INHIBITOR 1C; CYCLIN DEPENDENT KINASE INHIBITOR 2A; GLYCOGEN SYNTHASE KINASE 3BETA; GRANULOCYTE COLONY STIMULATING FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RAS PROTEIN; SOMATOMEDIN C; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR FOXO;

ACUTE MYELOBLASTIC LEUKEMIA; BREAST CANCER; CANCER ADJUVANT THERAPY; CANCER CELL; CANCER CELL DORMANCY; CANCER GROWTH; CANCER RECURRENCE; CANCER STEM CELL; CANCER SURVIVAL; CARCINOGENESIS; CELL CYCLE ARREST; CELL FUNCTION; CELL MOTILITY; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CIRCULATING TUMOR CELL; COLON CANCER; DOWN REGULATION; EXTRACELLULAR MATRIX; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; ANIMAL; NEOPLASM; PATHOLOGY;

ANIMALS; HUMANS; NEOPLASMS;

EID: 84955441840     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-1370     Document Type: Review

References (87)

1. Friedl W, Herfarth C. [The long-term prognosis of breast cancer. Retrospective study of 973 patients]. Langenbecks Arch Chir 1992;377:168-73.
2. Leman JA, Mac Kie RM. Late (> 10 years) recurrence of melanoma: the Scottish experience. Br J Dermatol 2003;148:372-3.
3. Goss PE, Chambers AF. Does tumour dormancy offer a therapeutic target? Nat Rev Cancer 2010;10:871-7.
4. Aguirre-Ghiso JA. Models, mechanisms and clinical evidence for cancer dormancy. Nat Rev Cancer 2007;7:834-46.
5. Giancotti FG. Mechanisms governing metastatic dormancy and reactivation. Cell 2013;155:750-64.
6. Sosa MS, Bragado P, Aguirre-Ghiso JA. Mechanisms of disseminated cancer cell dormancy: an awakening field. Nat Rev Cancer 2014;14:611-22.
7. Celsus AC, Spencer WG. De medicina. London: W. Heinemann ltd.; 1935.
8. Willis RA. The spread of tumours in the human body. London: J. & A. Churchill; 1934.
9. Hadfield G. The dormant cancer cell. Br Med J 1954;2:607-10.
10. Crowley NJ, Seigler HF. Late recurrence of malignant melanoma. Analysis of 168 patients. Ann Surg 1990;212:173-7.
11. Hansel G, Schonlebe J, Haroske G, Wollina U. Late recurrence (10 years or more) of malignant melanoma in south-east Germany (Saxony). A singlecentre analysis of 1881 patients with a follow-up of 10 years or more. J Eur Acad Dermatol Venereol 2010;24:833-6.
12. Schmid-Wendtner MH, Baumert J, Schmidt M, Konz B, Holzel D, Plewig G, et al. Late metastases of cutaneous melanoma: an analysis of 31 patients. J Am Acad Dermatol 2000;43:605-9.
13. Tsao H, Cosimi AB, Sober AJ. Ultra-late recurrence (15 years or longer) of cutaneous melanoma. Cancer 1997;79:2361-70.
14. Karrison TG, Ferguson DJ, Meier P. Dormancy of mammary carcinoma after mastectomy. J Natl Cancer Inst 1999;91:80-5.
15. Meng S, Tripathy D, Frenkel EP, Shete S, Naftalis EZ, Huth JF, et al. Circulating tumor cells in patients with breast cancer dormancy. Clin Cancer Res 2004;10:8152-62.
16. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, et al. Molecular portraits of human breast tumours. Nature 2000;406:747-52.
17. Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res 2007;13(15 Pt 1):4429-34.
18. Pantel K, Brakenhoff RH. Dissecting the metastatic cascade. Nat Rev Cancer 2004;4:448-56.
19. Klein CA, Holzel D. Systemic cancer progression and tumor dormancy: mathematical models meet single cell genomics. Cell Cycle 2006;5: 1788-98.
20. Ramaswamy S, Ross KN, Lander ES, Golub TR. A molecular signature of metastasis in primary solid tumors. Nat Genet 2003;33:49-54.
21. Demicheli R, Terenziani M, Bonadonna G. Estimate of tumor growth time for breast cancer local recurrences: rapid growth after wake-up? Breast Cancer Res Treat 1998;51:133-7.
22. Willis L, Graham TA, Alarcon T, Alison MR, Tomlinson IP, Page KM. What can be learnt about disease progression in breast cancer dormancy from relapse data? PLoS ONE 2013;8:e62320.
23. Loddo M, Kingsbury SR, Rashid M, Proctor I, Holt C, Young J, et al. Cell-cycle-phase progression analysis identifies unique phenotypes of major prognostic and predictive significance in breast cancer. Br J Cancer 2009;100:959-70.
24. Yerushalmi R, Woods R, Ravdin PM, Hayes MM, Gelmon KA. Ki67 in breast cancer: prognostic and predictive potential. Lancet Oncol 2010;11: 174-83.
25. Lambert G, Estevez-Salmeron L, Oh S, Liao D, Emerson BM, Tlsty TD, et al. An analogy between the evolution of drug resistance in bacterial communities and malignant tissues. Nat Rev Cancer 2011;11:375-82.
26. Roesch A, Fukunaga-Kalabis M, Schmidt EC, Zabierowski SE, Brafford PA, Vultur A, et al. A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 2010;141: 583-94.
27. Sharma SV, Lee DY, Li B, Quinlan MP, Takahashi F, Maheswaran S, et al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 2010;141:69-80.
28. Borst P. Cancer drug pan-resistance: pumps, cancer stem cells, quiescence, epithelial to mesenchymal transition, blocked cell death pathways, persisters or what? Open Biol 2012;2:120066.
29. Folkman J. Role of angiogenesis in tumor growth and metastasis. Semin Oncol 2002;29(6 Suppl 16):15-8.
30. Holmgren L, O'Reilly MS, Folkman J. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat Med 1995;1:149-53.
31. Naumov GN, Bender E, Zurakowski D, Kang SY, Sampson D, Flynn E, et al. A model of human tumor dormancy: an angiogenic switch from the nonangiogenic phenotype. J Natl Cancer Inst 2006;98:316-25.
32. Uhr JW, Pantel K. Controversies in clinical cancer dormancy. Proc Natl Acad Sci U S A 2011;108:12396-400.
33. Weinhold KJ, Goldstein LT, Wheelock EF. The tumor dormant state. Quantitation of L5178Y cells and host immune responses during the establishment and course of dormancy in syngeneic DBA/2 mice. J Exp Med 1979;149:732-44.
34. Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 2005;5:263-74.
35. Massague J. G1 cell-cycle control and cancer. Nature 2004;432:298-306.
36. Townson JL, Chambers AF. Dormancy of solitary metastatic cells. Cell Cycle 2006;5:1744-50.
37. Folkman J. Tumor angiogenesis. Adv Cancer Res 1985;43:175-203.
38. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003; 3:721-32.
39. Folkman J, Kalluri R. Cancer without disease. Nature 2004;427:787.
40. Giuriato S, Ryeom S, Fan AC, Bachireddy P, Lynch RC, Rioth MJ, et al. Sustained regression of tumors upon MYC inactivation requires p53 or thrombospondin-1 to reverse the angiogenic switch. Proc Natl Acad Sci U S A 2006;103:16266-71.
41. Indraccolo S, Stievano L, Minuzzo S, Tosello V, Esposito G, Piovan E, et al. Interruption of tumor dormancy by a transient angiogenic burst within the tumor microenvironment. Proc Natl Acad Sci U S A 2006; 103:4216-21.
42. Al-Mehdi AB, Tozawa K, Fisher AB, Shientag L, Lee A, Muschel RJ. Intra-vascular origin of metastasis from the proliferation of endothelium-attached tumor cells: a new model for metastasis. Nat Med 2000;6:100-2.
43. Burnet FM. The concept of immunological surveillance. Prog Exp Tumor Res 1970;13:1-27.
44. Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immuno-surveillance and immunoediting. Immunity 2004;21:137-48.
45. Koebel CM, Vermi W, Swann JB, Zerafa N, Rodig SJ, Old LJ, et al. Adaptive immunity maintains occult cancer in an equilibrium state. Nature 2007;450:903-7.
46. Teng MW, Swann JB, Koebel CM, Schreiber RD, Smyth MJ. Immunemediated dormancy: an equilibrium with cancer. J Leukoc Biol 2008; 84:988-93.
47. Farrar JD, Katz KH, Windsor J, Thrush G, Scheuermann RH, Uhr JW, et al. Cancer dormancy. VII. A regulatory role for CD8+ T cells and IFN-gamma in establishing and maintaining the tumor-dormant state. J Immunol 1999;162:2842-9.
48. Matsuzawa A, Takeda Y, Narita M, Ozawa H. Survival of leukemic cells in a dormant state following cyclophosphamide-induced cure of strongly immunogenic mouse leukemia (DL811). Int J Cancer 1991;49: 303-9.
49. MacKie RM, Reid R, Junor B. Fatal melanoma transferred in a donated kidney 16 years after melanoma surgery. N Engl J Med 2003;348: 567-8.
50. Elder GJ, Hersey P, Branley P. Remission of transplanted melanoma-clinical course and tumour cell characterisation. Clin Transplant 1997; 11:565-8.
51. Penn I. Malignant melanoma in organ allograft recipients. Transplantation 1996;61:274-8.
52. Suranyi MG, Hogan PG, Falk MC, Axelsen RA, Rigby R, Hawley C, et al. Advanced donor-origin melanoma in a renal transplant recipient: immunotherapy, cure, and retransplantation. Transplantation 1998;66:655-61.
53. Montagna D, Maccario R, Locatelli F, Montini E, Pagani S, Bonetti F, et al. Emergence of antitumor cytolytic T cells is associated with maintenance of hematologic remission in children with acute myeloid leukemia. Blood 2006;108:3843-50.
54. Penn I. Post-transplant malignancy: the role of immunosuppression. Drug Saf 2000;23:101-13.
55. Vajdic CM, McDonald SP, McCredie MR, van Leeuwen MT, Stewart JH, Law M, et al. Cancer incidence before and after kidney transplantation. JAMA 2006;296:2823-31.
56. Shiao SL, Ganesan AP, Rugo HS, Coussens LM. Immune microenvironments in solid tumors: new targets for therapy. Genes Dev 2011;25: 2559-72.
57. Naumov GN, MacDonald IC, Weinmeister PM, Kerkvliet N, Nadkarni KV, Wilson SM, et al. Persistence of solitary mammary carcinoma cells in a secondary site: a possible contributor to dormancy. Cancer Res 2002; 62:2162-8.
58. Dey-Guha I, Wolfer A, Yeh AC, J GA, Darp R, Leon E, et al. Asymmetric cancer cell division regulated by AKT. Proc Natl Acad Sci U S A 2011;108: 12845-50.
59. Muller V, Stahmann N, Riethdorf S, Rau T, Zabel T, Goetz A, et al. Circulating tumor cells in breast cancer: correlation to bone marrow micrometastases, heterogeneous response to systemic therapy and low proliferative activity. Clin Cancer Res 2005;11:3678-85.
60. Pantel K, Brakenhoff RH, Brandt B. Detection, clinical relevance and specific biological properties of disseminating tumour cells. Nat Rev Cancer 2008;8:329-40.
61. Solakoglu O, Maierhofer C, Lahr G, Breit E, Scheunemann P, Heumos I, et al. Heterogeneous proliferative potential of occult metastatic cells in bone marrow of patients with solid epithelial tumors. Proc Natl Acad Sci U S A 2002;99:2246-51.
62. Sherr CJ, Roberts JM. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 1999;13:1501-12.
63. Lu Z, Luo RZ, Lu Y, Zhang X, Yu Q, Khare S, et al. The tumor suppressor gene ARHI regulates autophagy and tumor dormancy in human ovarian cancer cells. J Clin Invest 2008;118:3917-29.
64. Weaver VM, Petersen OW, Wang F, Larabell CA, Briand P, Damsky C, et al. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol 1997;137:231-45.
65. White DE, Kurpios NA, Zuo D, Hassell JA, Blaess S, Mueller U, et al. Targeted disruption of beta1-integrin in a transgenic mouse model of human breast cancer reveals an essential role in mammary tumor induction. Cancer Cell 2004;6:159-70.
66. Endo H, Okuyama H, Ohue M, Inoue M. Dormancy of cancer cells with suppression of AKT activity contributes to survival in chronic hypoxia. PLoS ONE 2014;9:e98858.
67. Dey-Guha I, Alves CP, Yeh AC, Salony, Sole X, Darp R, et al. A mechanism for asymmetric cell division resulting in proliferative asynchronicity. Mol Cancer Res 2015;13:223-30.
68. Aguirre-Ghiso JA, Ossowski L, Rosenbaum SK. Green fluorescent protein tagging of extracellular signal-regulated kinase and p38 pathways reveals novel dynamics of pathway activation during primary and metastatic growth. Cancer Res 2004;64:7336-45.
69. Barkan D, Kleinman H, Simmons JL, Asmussen H, Kamaraju AK, Hoenorhoff MJ, et al. Inhibition of metastatic outgrowth from single dormant tumor cells by targeting the cytoskeleton. Cancer Res 2008;68:6241-50.
70. Shibue T, Weinberg RA. Integrin beta1-focal adhesion kinase signaling directsthe proliferation of metastatic cancer cells disseminatedinthe lungs. Proc Natl Acad Sci U S A 2009;106:10290-5.
71. Barkan D, El Touny LH, Michalowski AM, Smith JA, Chu I, Davis AS, et al. Metastatic growth from dormant cells induced by a col-I-enriched fibrotic environment. Cancer Res 2010;70:5706-16.
72. Ghajar CM, Peinado H, Mori H, Matei IR, Evason KJ, Brazier H, et al. The perivascular niche regulates breast tumour dormancy. Nat Cell Biol 2013;15:807-17.
73. Boyerinas B, Zafrir M, Yesilkanal AE, Price TT, Hyjek EM, Sipkins DA. Adhesion to osteopontin in the bone marrow niche regulates lymphoblastic leukemia cell dormancy. Blood 2013;121:4821-31.
74. Marlow R, Honeth G, Lombardi S, Cariati M, Hessey S, Pipili A, et al. A novel model of dormancy for bone metastatic breast cancer cells. Cancer Res 2013;73:6886-99.
75. Barkan D, Chambers AF. beta1-integrin: a potential therapeutic target in the battle against cancer recurrence. Clin Cancer Res 2011;17:7219-23.
76. Ranganathan AC, Zhang L, Adam AP, Aguirre-Ghiso JA. Functional coupling of p38-induced up-regulation of BiP and activation of RNA-dependent protein kinase-like endoplasmic reticulum kinase todrug resistance of dormant carcinoma cells. Cancer Res 2006;66:1702-11.
77. Amaravadi RK. Autophagy-induced tumor dormancy in ovarian cancer. J Clin Invest 2008;118:3837-40.
78. Aguirre-Ghiso JA, Estrada Y, Liu D, Ossowski L. ERK(MAPK) activity as a determinant of tumor growth and dormancy; regulation by p38(SAPK). Cancer Res 2003;63:1684-95.
79. Aguirre-Ghiso JA, Liu D, Mignatti A, Kovalski K, Ossowski L. Urokinase receptor and fibronectin regulate the ERK(MAPK) to p38(MAPK) activity ratios that determine carcinoma cell proliferation or dormancy in vivo. Mol Biol Cell 2001;12:863-79.
80. Gupta PB, Fillmore CM, Jiang G, Shapira SD, Tao K, Kuperwasser C, et al. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 2011;146:633-44.
81. Shachaf CM, Kopelman AM, Arvanitis C, Karlsson A, Beer S, Mandl S, et al. MYC inactivation uncovers pluripotent differentiation and tumour dormancy in hepatocellular cancer. Nature 2004;431:1112-7.
82. Gao X, Cui Y, Levenson RM, Chung LW, Nie S. In vivo cancer targeting and imaging with semiconductor quantum dots. Nat Biotechnol 2004; 22:969-76.
83. Voura EB, Jaiswal JK, Mattoussi H, Simon SM. Tracking metastatic tumor cell extravasation with quantum dot nanocrystals and fluorescence emission-scanning microscopy. Nat Med 2004;10:993-8.
84. Murrell DH, Foster PJ, Chambers AF. Brain metastases from breast cancer: lessons from experimental magnetic resonance imaging studies and clinical implications. J Mol Med 2014;92:5-12.
85. Moody SE, Sarkisian CJ, Hahn KT, Gunther EJ, Pickup S, Dugan KD, et al. Conditional activation of Neu in the mammary epithelium of transgenic mice results in reversible pulmonary metastasis. Cancer Cell 2002;2: 451-61.
86. Naumov GN, Townson JL, MacDonald IC, Wilson SM, Bramwell VH, Groom AC, et al. Ineffectiveness of doxorubicin treatment on solitary dormant mammary carcinoma cells or late-developing metastases. Breast Cancer Res Treat 2003;82:199-206.
87. Essers MA, Trumpp A. Targeting leukemic stem cells by breaking their dormancy. Mol Oncol 2010;4:443-50.