Mechanism of drug sensitivity and resistance in melanoma

Current Cancer Drug Targets

Volumn 9, Issue 3, 2009, Pages 391-397

  La Porta, Caterina A M ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ABC TRANSPORTER A1; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; BEVACIZUMAB; BREAST CANCER RESISTANCE PROTEIN; CAMPTOTHECIN; CISPLATIN; DACARBAZINE; DOXORUBICIN; FLUOROURACIL; FOTEMUSTINE; HISTONE DEACETYLASE INHIBITOR; MELANIN; MITOXANTRONE; MULTIDRUG RESISTANCE PROTEIN 1; PHORBOL ESTER DERIVATIVE; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; TEMOZOLOMIDE; TRICOSTATIN A; UNCLASSIFIED DRUG; VINDESINE; X LINKED INHIBITOR OF APOPTOSIS;

ANGIOGENESIS; APOPTOSIS; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CANCER STEM CELL; CARCINOGENIC ACTIVITY; DRUG EFFICACY; DRUG SENSITIVITY; DRUG TREATMENT FAILURE; GLIOMA; HUMAN; MELANOGENESIS; MELANOMA; METASTASIS; MULTIDRUG RESISTANCE; NONHUMAN; PROTEIN EXPRESSION; REVIEW; TISSUE DIFFERENTIATION; TUMOR GROWTH;

ANTINEOPLASTIC AGENTS; CELL DIFFERENTIATION; DISEASE PROGRESSION; DRUG RESISTANCE, NEOPLASM; HUMANS; MELANOMA; NEOPLASM METASTASIS; NEOPLASTIC STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC;

EID: 65649107620     PISSN: 15680096     EISSN: None     Source Type: Journal    
DOI: 10.2174/156800909788166574     Document Type: Review

References (124)

1. Clark, Jr. W. H.; Elder, D. E.; Guerry, D.; Epstein, M. N.; Greene, M. H.; Van Horn, M. A study of tumor progression: the precursor lesions of superficial spreading and nodular melanoma. Hum. Pathol. 1984, 15, 1147-1165. (Pubitemid 15128121)
2. Bishop, J. A.; Wachsmuth, R. C.; Harland, M.; Bataille, V.; Pinney, E.; MacK, P.; Baglietto, L.; Cuzick, J.; Bishop, D. T. Genotype/ phenotype and penetrance studies in melanoma families with germline CDKN2A mutations. J. Invest. Dermatol. 2000, 114, 28-33. (Pubitemid 30195968)
3. Koh, H. K. Cutaneous melanoma. N. Engl. J. Med. 1991, 325, 171-182.
4. Fidler, I. J. Tumor heterogeneity and the biology of cancer invasion and metastasis. Cancer Res. 1978, 38, 2651-2660. (Pubitemid 9001502)
5. Folkman, J. How is blood vessel growth regulated in normal and neoplastic tissue? G.H.A. Clowes memorial Award lecture. Cancer Res. 1986, 46, 467-473.
6. Folkman, J. Angiogenesis: an organizing principle for drug discovery? Nat. Rev. Drug Discov. 2007, 6, 273-286.
7. Piepkorn, M. W.; Barnhill, R. L.; Cannon-Albright, A. L.; Elden, D. E.; Golgar, D. E.; Lewis, C. M.; Maize, J. C.; Meyer, L. J.; Rabkin, M. S.; Sagebile, R. W.; Skonick, M. H.; Zone, J. J. A multiobserver, population-based analysis of histologic dysplasia in melanocytic nevi. J. Am. Acad. Dermatol. 1994, 30, 707-714. (Pubitemid 24157110)
8. Helm, K. F.; Marks, J. G. Differential diagnosis in dermathology; New York, Churchill Livingston, 1997.
9. Farmer, E. R.; Gonin, R.; Hanna, N. P. Discordance in the histopathologic diagnosis of melanoma and melanocytic nevi between expert pathologists. Hum. Pathol. 1996, 27, 528-531. (Pubitemid 26187274)
10. Korner, A.; Pawelek, J. Activation of melanoma tyrosinase by a cyclic AMP-dependent protein kinase in a cell-free system. Nature 1977, 267, 444-447. (Pubitemid 8105529)
11. La Porta, C. A. M.; Comolli, R. Activation of protein kinase C-alpha isoform in murine melanoma cells with high metastatic potential. Clin. Exp. Metatstasis 1997, 15, 568-579. (Pubitemid 27435738)
12. Gruber, J. R.; Ohno, S.; Niles, R. M. Increased expression of protein kinase C alpha plays a key role in retinoic acid-induced melanoma differentiation. J. Biol. Chem. 1992, 267, 13356-13360.
13. La Porta, C. A. M.; Di Dio, A.; Porro, D.; Comolli, R. Overexpression of novel protein kinase C delta in BL6 murine melanoma cells inhibits the proliferative capacity in vitro but enhances the metastatic potential in vivo. Melanoma Res. 2000, 10, 93-102. (Pubitemid 30256871)
14. Englaro, W.; Rezzonico, R.; Durand-Clement, M.; Lallemand, D.; Ortonne, J. P.; Ballotti, R. Mitogen-activated protein kinase pathway and AP-1 are activated during cAMP-induced melanogenesis in B-16 melanoma cells. J. Biol. Chem. 1995, 270, 24315-24320.
15. Oka, M.; Nagai, H.; Ando, H.; Fukunaga, M.; Mastsumura, M.; Araki, K.; Ogawa, W.; Miki, T.; Sakaue, M.; Tsukamoto, K.; Konishi, H.; Kikkawa, U.; Ichihashi, M. Regulation of melanogenesis through phosphatidylinositol 3-kinase-Akt pathway in human G361 melanoma cells. J. Invest. Dermatol. 2000, 115, 699-703.
16. Prezioso, J. A.; Wang, N.; Duty, L.; Bloomer, W. D.; Gorelik, E. Enhancement of pulmonary metastasis formation and gamma-glutamyltranspeptidase activity in B16 melanoma induced by differentiation in vitro. Clin. Exp. Metastasis 1993, 11, 263-274. (Pubitemid 23138525)
17. Elstad, C. A.; Meadows, G. G. Modulation of B16-BL6 murine melanoma metastatic phenotype by tyrosine and phenylalanine restriction in the absence of host selection pressures. Anticancer Res. 1993, 13, 523-528. (Pubitemid 23196797)
18. Pierson, H. F.; Meadows, G. G. Sodium ascorbate enhancement of carbidopa-levodopa methyl ester antitumor activity against pigmented B16 melanoma. Cancer Res. 1983, 43, 2047-2051.
19. Bennet, D. C.; Dexter, T. J.; Ormerod, E. J.; Hart, I. R. Increased experimental metastatic capacity of a murine melanoma following induction of differentiation. Cancer Res. 1986, 46, 3239-13144
20. La Porta, C. A. M.; Porro, D.; Comolli, R. Higher levels of melanin and inhibition of cdk2 activity in primary human melanoma cells WM115 over expressing nPKCdelta. Melanoma Res. 2002, 12, 297-307.
21. La Porta, C. A. M.; Comolli, R. Different levels of TGFbeta, IL-10 and gelatinase A occur in experimental white and black metastases induced by bryostatin 1 or by phorbol-ester treated BL6T murine melanoma cells. Clin. Exp. Metastasis 2001, 18, 361-369.
22. La Porta, C. A. M. Perspectives in melanoma treatment with signal transduction. Curr. Med. Chem. Anticancer Agents 2002, 3, 371-385.
23. Barndhill, R. L.; Fandrey, K.; Levy, M. A.; Mihm, M. C. Jr.; Hyman, B. Angiogenesis and tumor progression of melanoma. Quantification of vascularity in melanocytic nevi and cutaneous malignant melanoma. Lab. Invest. 1992, 67, 331-337.
24. Liotta, L. A.; Steeg, P. S.; Stetler-Stevenson, W. G. Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell 1991, 64, 327-336. (Pubitemid 121001258)
25. Folkman, J. Tumor angiogenesis. Adv. Cancer Res. 1985, 43, 175-203.
26. La Porta, C. A. M.; Porro, D.; Comolli, R. Opposite effects of TPA on G1/S transition and on cell size in the low metastatic B16F1 with respect to high metastatic BL6 murine melanoma cells. Cancer Lett. 1998, 132, 159-164. (Pubitemid 28535199)
27. Kingsley, D. The TGF-beta superfamily: new members, new receptors, and new genetic tests of function in different organisms. Gene Dev. 1994, 8, 133-146.
28. Laiho, M.; Keski-Oja, J. Transforming growth factors-beta as regulators of cellular growth and phenotype. Crit. Rev. Oncol. 1992, 3, 1-26.
29. Krasagakis, K.; Tholke, D.; Farthmann, B.; Eberle, J.; Mannsmann, U.; Orfanos, C. E. Elevated plasma levels of transforming growth factor (TGF)-beta1 and TGF-beta2 in patients with disseminated malignant melanoma. Br. J. Cancer 1998, 77, 1492-1494. (Pubitemid 28190751)
30. La Porta, C. A. M.; Di Dio, A.; Porro, D.; Comolli, R. Overexpression of nPKCdelta in BL6 murine melanoma cells enhances TGFbeta1 release into the plasma of metastasised animals. Melanoma Res. 2000, 10, 527-534. (Pubitemid 32011974)
31. Bodey, B.; Bodey, B.; Siegel, S. E.; Keiser, H. E. Immunocytochemical detection of endoglin is indicative of angiogenesis in malignant melanoma. Anticancer Res. 1998, 18, 2701-2710. (Pubitemid 28386569)
32. Jemal, A.; Devesa, S. S.; Hartge, P.; Tucker, M. A. Recent trends in cutaneous melanoma incidence among whites in the United States. J. Natl. Cancer Inst. 2001, 93, 678-683. (Pubitemid 32492808)
33. Florez, A.; Cruces, M. Melanoma epidemic: true or false? Int. J. Dermatol. 2004, 43, 405-407.
34. Welch, H. G.; Woloshin, S.; Schwartz, L. M. Skin biopsy rates and incidence of melanoma: population based ecological study. BMJ 2005, 331, 481.
35. Douglas, J. G.; Margolin, K. The treatment of brain metastases from malignant melanoma. Semin. Oncol. 2002, 29, 518-524. (Pubitemid 35178291)
36. Sertoli, M. R.; Queirolo, P.; Bajetta, E.; Del Vecchio, M.; Comella, G.; Barduagni, L.; Bernengo, M. G.; Vecchio, S.; Criscuolo, D.; Bufalino, R.; Morabito, A.; Cascinelli, N. Multi-institutional phase II randomized trial of integrated therapy with cisplatin, dacarbazine, vindesine, subcutaneous interleukin-2, interferon alpha2a and tamoxifen in metastatic melanoma. BREMIM (Biological Response Modifiers in Melanoma). Melanoma Res. 1999, 9, 503-509. (Pubitemid 29494116)
37. Helmbach, H.; Rossmann, E.; Kern, M. A.; Schadendorf, D. Drug-resistance in human melanoma. Int. J. Cancer 2001, 93, 617-622.
38. Serrone, L.; Zeuli, M.; Sega, F. M.; Cognetti, F. Dacarbazine-based chemotherapy for metastatic melanoma: thirty-year experience overview. J. Exp. Clin. Cancer Res. 2000, 19, 21-34.
39. Lens, M. B.; Eisen, T. G. Systemic chemotherapy in the treatment of malignant melanoma. Expert Opin. Pharmacother. 2003, 4, 2205-2211. (Pubitemid 37541234)
40. Lawson, D. H. Update on the systemic treatment of malignant melanoma. Semin. Oncol. 2004, 31, 33-37. (Pubitemid 38609791)
41. Gottesman, M. M.; Fojo, T.; Bates, S. E. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat. Rev. Cancer 2002, 2, 48-58. (Pubitemid 37328807)
42. Higgins, C. F. ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 1992, 8, 67-113.
43. Dean, M.; Rzhetsky, A.; Allikmets, R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res. 2001, 11, 1156-1166. (Pubitemid 32677289)
44. Ambudkar, S. V.; Kimchi-Sarfaty, C.; Sauna, Z. E.; Gottesman, M. M. P-glycoprotein: from genomics to mechanism. Oncogene 2003, 22, 7468-7485.
45. Goldstein, L. J.; Galski, H.; Fojo, A.; Willingham, M.; Lai, S. L.; Gazdar, A.; Pirker, R.; Green, A.; Crist, W.; Brodeur, G. M.; et al. Expression of a multidrug resistance gene in human cancers. J. Natl. Cancer Inst. 1989, 81, 116-124.
46. Gros, P.; Ben Neriah, Y. B.; Croop, J. M.; Housman, D. E. Isolation and expression of a complementary DNA that confers multidrug resistance. Nature 1986, 323, 728-731. (Pubitemid 17172974)
47. Riordan, J. R.; Deuchars, K.; Kartner, N.; Alon, N.; Trent, J.; Ling, V. Amplification of P-glycoprotein genes in multidrug-resistant mammalian cell lines. Nature 1985, 316, 817-819. (Pubitemid 15003740)
48. Roninson, I. B.; Chin, J. E.; Choi, K. G.; Gros, P.; Housman, D. E.; Fojo, A.; Shen, D. W.; Gottesman, M. M.; Pastan, I. Isolation of human mdr DNA sequences amplified in multidrug-resistant KB carcinoma cells. Proc. Natl. Acad. Sci. USA 1986, 83, 4538-4542. (Pubitemid 16057084)
49. Ueda, K.; Cornwell, M. M.; Gottesman, M. M.; Pastan, I.; Roninson, I. B.; Ling, V.; Riordan, J. R. The mdr1 gene, responsible for multidrug-resistance, codes for P-glycoprotein. Biochem. Biophys. Res. Commun. 1986, 141, 956-962. (Pubitemid 17006141)
50. Van der Bliek, A. M.; Baas, F.; Ten Houte de Lange, T.; Kooiman, P. M.; Van der Velde-Koerts, T.; Borst, P. The human mdr3 gene encodes a novel P-glycoprotein homologue and gives rise to alternatively spliced mRNAs in liver. EMBO J. 1987, 6, 3325-3331.
51. Frank, N. Y.; Margaryan, A.; Huang, Y.; Schatton, T.; Waaga- Gasser, A. M.; Gasser, M.; Sayegh, M. H.; Sadee, W.; Frank, M. H. ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma. Cancer Res. 2005, 65, 4320-4333. (Pubitemid 40775671)
52. Chen, K. G.; Szakacs, G.; Annereau, J. P.; Rouzaud, F.; Liang, X. J.; Valencia, J. C.; Nagineni, C. N.; Hooks, J. J.; Hearing, V. J.; Gottesman, M. M. Principal expression of two mRNA isoforms (ABCB 5alpha and ABCB 5beta ) of the ATP-binding cassette transporter gene ABCB 5 in melanoma cells and melanocytes. Pigment Cell Res. 2005, 18, 102-112.
53. Huang, Y.; Anderle, P.; Bussey, K. J.; Barbacioru, C.; Shankavaram, U.; Dai, Z.; Reinhold, W. C.; Papp, A.; Weinstein, J. N.; Sadée, W. Membrane transporters and channels: role of the transportome in cancer chemosensitivity and chemoresistance. Cancer Res. 2004, 64, 4294-4301.
54. Allikmets, R.; Schriml, L. M.; Hutchinson, A.; Romano-Spica, V.; Dean, M. A human placenta-specific ATP-binding cassette gene (ABCP) on chromosome 4q22 that is involved in multidrug resistance. Cancer Res. 1998, 58, 5337-5339.
55. Miyake, K.; Mickley, L.; Litman, T.; Zhan, Z.; Robey, R.; Cristensen, B.; Brangi, M.; reenberger, L.; Dean, M.; Fojo, T.; Bates, S. E. Molecular cloning of cDNAs which are highly overexpressed in mitoxantrone-resistant cells: demonstration of homology to ABC transport genes. Cancer Res. 1999, 59, 8-13.
56. Doyle, L. A.; Yang, W.; Abruzzo, L. V. ; Krogmann, T.; Gao, Y.; Rishi, A. K.; Ross, D. D. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc. Natl. Acad. Sci. USA 1998, 95, 15665-15670. (Pubitemid 29018757)
57. Abbott, B. L. ABCG2 (BCRP) expression in normal and malignant hematopoietic cells. Hematol. Oncol. 2003, 21, 115-130. (Pubitemid 37305331)
58. Schinkel, A. H.; Jonker, J. W. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv. Drug. Deliv. Rev. 2003, 55, 3-29. (Pubitemid 36078452)
59. Monzani, E.; Facchetti, F.; Galmozzi, E.; Corsini, E.; Benetti, A.; Cavazzin, C.; Gritti, A.; Piccinini, A.; Porro, D.; Santinami, M.; Invernici, G.; Parati, E.; Alessandri, G.; La Porta, C. A. M. Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. Eur. J. Cancer 2007, 43, 935-946.
60. Liedert, B.; Materna, V.; Schadendorf, D.; Thomale, J.; Lage, H. Overexpression of cMOAT (MRP2/ABCC2) is associated with decreased formation of platinum-DNA adducts and decreased G2- arrest in melanoma cells resistant to cisplatin. J. Invest. Dermatol. 2003, 121, 172-176. (Pubitemid 36900469)
61. Igney, F. H.; Krammer, P. H. Death and anti-death: tumour resistance to apoptosis. Nat. Rev. Cancer 2002, 2, 277-288. (Pubitemid 37328781)
62. Soengas, M. S.; Alarcon, R. M.; Yoshida, H.; Giaccia, A. J.; Hakem, R.; Mak, T. W.; Lowe, S. W. Apaf-1 and caspase-9 in p53- dependent apoptosis and tumor inhibition. Science 1999, 284, 156-159. (Pubitemid 29282071)
63. Li, F.; Ambrosini, G.; Chu, E. Y.; Plescia, J.; Tognin, S.; Marchisio, P. C.; Altieri, D. C. Control of apoptosis and mitotic spindle checkpoint by survivin. Nature 1998, 396, 580-584. (Pubitemid 28563719)
64. Albino, A. P.; Vidal, M. J.; McNutt, N. S.; Shea, C. R.; Prieto, V. G.; Nanus, D. M.; Palmer, J. M.; Hayward, N. K. Mutation and expression of the p53 gene in human malignant melanoma. Melanoma Res. 1994, 4, 35-45.
65. Soengas, M. S.; Capodieci, P.; Polsky, D.; Mora, J.; Esteller, M.; Opitz-Araya, X.; McCombie, R.; Herman, J. G.; Gerald, W. L.; Lazebnik, Y. A.; Cordon-Cardo, C.; Lowe, S. W. Inactivation of the apoptosis effector Apaf-1 in malignant melanoma. Nature 2001, 409, 207-211. (Pubitemid 32144287)
66. Bird, A. P.; Wolffe, A. P. Methylation-induced repression--belts, braces, and chromatin. Cell 1999, 99, 451-454.
67. Baldi, A.; Santini, D.; Russo, P.; Catricala, C.; Amantea, A.; Picardo, M.; Tatangelo, F.; Botti, G.; Dragonetti, E.; Murace, R.; Tonini, G.; Natali, P. G.; Baldi, F.; Paggi, M. G. Analysis of APAF-1 expression in human cutaneous melanoma progression. Exp. Dermatol. 2004, 13, 93-97. (Pubitemid 38247867)
68. Zanon, M.; Piris, A.; Bersani, I.; Vegetti, C.; Molla, A.; Scarito, A.; Anichini, A. Apoptosis protease activator protein-1 expression is dispensable for response of human melanoma cells to distinct proapoptotic agents. Cancer Res. 2004, 64, 7386-7394.
69. Dai, D. L.; Martinka, M.; Bush, J. A.; Li, G. Reduced Apaf-1 expression in human cutaneous melanomas. Br. J. Cancer 2004, 91, 1089-1095.
70. Fujimoto, A.; Takeuchi, H.; Taback, B.; Hsueh, E. C.; Elashoff, D.; Morton, D. L.; Hoon, D. S. Allelic imbalance of 12q22-23 associated with APAF-1 locus correlates with poor disease outcome in cutaneous melanoma. Cancer Res. 2004, 64, 2245-2250.
71. Mustika, R.; Budiyanto, A.; Nishigori, C.; Ichihashi, M.; Ueda, M. Decreased expression of Apaf-1 with progression of melanoma. Pigment Cell Res. 2005, 18, 59-62.
72. Soengas, M. S.; Lowe, S. W. Apoptosis and melanoma chemoresistance. Oncogene 2003, 22, 3138-3151. (Pubitemid 36713766)
73. Irmler, M.; Thome, M.; Hahne, M.; Schneider, P.; Hofmann, K.; Steiner, V.; Bodmer, J. L.; Schroter, M.; Burns, K.; Mattmann, C.; Rimoldi, D.; French, L. E.; Tschopp, J. Inhibition of death receptor signals by cellular FLIP. Nature 1997, 388, 190-195. (Pubitemid 27297457)
74. Grossman, D.; Altieri, D. C. Drug resistance in melanoma: mechanisms, apoptosis, and new potential therapeutic targets. Cancer Metastasis Rev. 2001, 20, 3-11.
75. Facchetti, F.; Previdi, S.; Ballarini, M.; Minucci, S.; Perego, P.; La Porta, C. A. Modulation of pro- and anti-apoptotic factors in human melanoma cells exposed to histone deacetylase inhibitors. Apoptosis 2004, 9, 573-582. (Pubitemid 39158633)
76. Chin, L.; Merlino, G.; DePinho, R. A. Malignant melanoma: modern black plague and genetic black box. Genes Dev. 1998, 12, 3467-3481.
77. Serrone, L.; Hersey, P. The chemoresistance of human malignant melanoma: an update. Melanoma Res. 1999, 9, 51-58. (Pubitemid 29169989)
78. Karst, A. M.; Dai, L. D.; Martinka, M.; Li, G. PUMA expression is significantly reduced in human cutaneous melanomas. Oncogene 2005, 24, 1111-1116. (Pubitemid 40313889)
79. Salvesen, G. S.; Duckett, C. S. IAP proteins: blocking the road to death's door. Nat. Rev. Mol. Cell Biol. 2002, 3, 401-410. (Pubitemid 34685698)
80. Liston, P.; Fong, W. G.; Korneluk, R. G. The inhibitors of apoptosis: there is more to life than Bcl2. Oncogene 2003, 22, 8568-8580. (Pubitemid 38019194)
81. Deveraux, Q. L.; Takahashi, R.; Salvesen, G. S.; Reed, J. C. X-linked IAP is a direct inhibitor of cell-death proteases. Nature 1997, 388, 300-304. (Pubitemid 27317977)
82. Roy, N.; Deveraux, Q. L.; Takahashi, R.; Salvesen, G. S.; Reed, J. C. The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases. EMBO J. 1997, 16, 6914-6925.
83. Kasof, G. M.; Gomes, B. C. Livin, a novel inhibitor of apoptosis protein family member. J. Biol. Chem. 2001, 276, 3238-3246.
84. Shin, S.; Sung, B. J.; Cho, Y. S.; Kim, H. J.; Ha, N. C.; Hwang, J. I.; Chung, C. W.; Jung, Y. K.; Oh, B. H. An anti-apoptotic protein human survivin is a direct inhibitor of caspase-3 and -7. Biochemistry 2001, 40, 1117-1123. (Pubitemid 32108606)
85. Maier, J. K.; Lahoua, Z.; Gendron, N. H.; Fetni, R.; Johnston, A.; Davoodi, J.; Rasper, D.; Roy, S.; Slack, R. S.; Nicholson, D. W.; MacKenzie, A. E. The neuronal apoptosis inhibitory protein is a direct inhibitor of caspases 3 and 7. J. Neurosci. 2002, 22, 2035-2043.
86. Du, C.; Fang, M.; Li, Y.; Li, L.; Wang, X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000, 102, 33-42.
87. Suzuki, Y.; Imai, Y.; Nakayama, H.; Takahashi, K.; Takio, K.; Takahashi, R. A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol. Cell. 2001, 8, 613-621.
88. Hegde, R.; Srinivasula, S. M.; Zhang, Z.; Wassell, R.; Mukattash, R.; Cilenti, L.; DuBois, G.; Lazebnik, Y.; Zervos, A. S.; Fernandes- Alnemri, T.; Alnemri, E. S. Identification of Omi/HtrA2 as a mitochondrial apoptotic serine protease that disrupts inhibitor of apoptosis protein-caspase interaction. J. Biol. Chem. 2002, 277, 432-438.
89. Martins, M. L.; Iaccarino, I.; Tenev, T.; Gschmeissner, S.; Totty, N. F.; Lemoine, N. R.; Savopoulos, J.; Gray, C. W.; Creasy, C. L.; Dingwall, C.; Downward, J. The serine protease Omi/HtrA2 regulates apoptosis by binding XIAP through a reaper-like motif. J. Biol. Chem. 2002, 277, 439-444.
90. Verhagen, A. M.; Silke, J.; Ekert, P. G.; Pakusch, M.; Kaufmann, H.; Connolly, L. M.; Day, C. L.; Tikoo, A.; Burke, R.; Wrobel, C.; Moritz, R. L.; Simpson, R. J.; Vaux, D. L. HtrA2 promotes cell death through its serine protease activity and its ability to antagonize inhibitor of apoptosis proteins. J. Biol. Chem. 2002, 277, 445-454.
91. Liston, P.; Fong, W. G.; Kelly, N. L.; Toji, S.; Miyazaki, T.; Conte, D.; Tamai, K.; Craig, C. G.; McBurney, M. W.; Korneluk, R. G. Identification of XAF1 as an antagonist of XIAP anti-Caspase activity. Nat. Cell Biol. 2001, 3, 128-133. (Pubitemid 32118365)
92. Ng. K. G.; Campos, E. I.; Martinka, M.; Li, G. XAF1 expression is significantly reduced in human melanoma. J. Invest. Dermatol. 2004, 123, 1127-1134. (Pubitemid 39586836)
93. Goodell, M. A.; Brose, K.; Paradis, G.; Conner, A. S.; Mulligan, R. C. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J. Exp. Med. 1996, 183, 1797-1806. (Pubitemid 26134320)
94. Schatton, T.; Murphy, G. F.; Frank, N. Y.; Yamaura, K.; Waaga- Gasser, A. M.; Gasser, M.; Zhan, Q.; Jordan, S.; Duncan, L. M.; Weishaupt, C.; Fuhlbrigge, R. C.; Kupper, T. S.; Sayegh, M. H.; Frank, M. H. Identification of cells initiating human melanomas. Nature 2008, 451, 345-349.
95. Dean, M.; Fojo, T.; Bates, S. Tumour stem cells and drug resistance. Nat. Rev. Cancer 2005, 5, 275-284. (Pubitemid 40488633)
96. Mimeault, M.; Batra, S. K. Concise review: recent advances on the significance of stem cells in tissue regeneration and cancer therapies. Stem Cell 2006, 24, 2319-2345. (Pubitemid 44679695)
97. Mimeault, M.; Hauke, R.; Batra, S. K. Stem cells: a revolution in therapeutics-recent advances in stem cell biology and their therapeutic applications in regenerative medicine and cancer therapies. Clin. Pharmnacol. Ther. 2007, 82, 252-264.
98. Rosell, R.; Cecere, F.; Cognetti, F.; Cuello, M.; Sanchez, J. M.; Taron, M.; Reguart, N.; Jablons, D.; Future directions in the second- line treatment of non-small cell lung cancer. Semin. Oncol. 2006, 33, S45-S51. (Pubitemid 43201987)
99. Sato, M.; Shemes, D. S.; Gazdar, A. F.; Minna, J. D. A translational view of the molecular pathogenesis of lung cancer. J. Thorac. Oncol. 2007, 2, 327-343. (Pubitemid 47181718)
100. Baker, N.; Clevers, H. Mining the Wnt pathway for cancer therapeutics. Nat. Rev. Drug Discov. 2006, 5, 997-1014.
101. Rubin, L. L.; de Sauvage, F. J. Targeting the Hedgehog pathway in cancer. Nat. Rev. Drug Discov. 2006, 5, 1026-1033.
102. Mimeault, M.; Batra, S. Interplay of distinct growth factors during epithelial mesenchymal transition of cancer progenitor cells and molecular targeting as novel cancer therapies. Ann. Oncol. 2007, 18, 1605-1619. (Pubitemid 47506246)
103. Mimeault, M.; Batra, S. K. Functions of tumorigenic and migrating cancer progenitor cells in cancer progression and metastasis and their therapeutic implications. Cancer Metastasis Rev. 2007, 26, 203-214.
104. Nicolis, S. K. Cancer stem cells and "stemness" genes in neurooncology. Neurobiol. Dis. 2007, 25, 217-229.
105. Fodde, R.; Brabletz, T. Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr. Opin. Cell Biol. 2007, 19, 150-158.
106. de Jonge-Peeters, S. D.; Kuipers, F.; de Vries, E. G.; Vellenga, E. ABC transporter expression in hematopoietic stem cells and the role in AML drug resistance. Crit. Rev. Oncol. Hematol., 2007, 62, 214-226. (Pubitemid 46679286)
107. Hirschmann-Jax, C.; Foster, A. E.; Wulf, G. G.; Goodell, M. A.; Brenner, M. K. A distinct "side population" of cells in human tumor cells: implications for tumor biology and therapy. Cell Cycle 2005, 4, 203-205.
108. Reya, T.; Clevers, H. Wnt signalling in stem cells and cancer. Nature 2005, 434, 843-850. (Pubitemid 40558990)
109. Woodward, W. A.; Chen, M. S.; Behbod, F.; Rosen, J. M. On mammary stem cells. J. Cell Sci. 2005, 118, 3585-3594.
110. Galmozzi, E.; Facchetti, F.; La Porta, C. A. M. Cancer stem cells and therapeutic perspectives. Curr. Med. Chem. 2006, 13, 603-607.
111. Rizo, A.; Vallenga, E.; de Haan, G.; Schuringa, J. J. Signaling pathways in self-renewing hematopoietic and leukemic stem cells: do all stem cells need a niche? Hum. Mol. Genet. 2006, 15, R210-R219. (Pubitemid 44446796)
112. Wicha, M. S.; Liu, S.; Dontu, G. Cancer stem cells: an old idea - a paradigm shift. Cancer Res. 2006, 66, 1883-1890.
113. Liu, S.; Dontu, G.; Mantle, I. D.; Patel, S.; Ahn, N. S.; Jackson, K. W.; Suri, P.; Wicha, M. S. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 2006, 66, 6063-6071.
114. Villanueva, A.; Newell, P.; Chiang, D. Y.; Friendman, S. L.; Llovet, J. M. Genomics and signaling pathways in hepatocellular carcinoma. Semin. Liver Dis. 2007, 27, 55-76. (Pubitemid 46269805)
115. Lowenberg, B.; Griffin, J. D.; Tallman, M. S. Acute myeloid leukemia and acute promyelocytic leukemia. Hematol. Am. Soc. Hematol. Educational Prog. 2003, 82-101.
116. Gray-Schopfer, V.; Wellbrock, C.; Marais, R. Melanoma biology and new targeted therapy. Nature 2007, 445, 851-857. (Pubitemid 46309849)
117. Sorscher, S. M. Biological therapy update in colorectal cancer. Expert. Opin. Biol. Ther. 2007, 7, 509-519. (Pubitemid 46524675)
118. Milas, L.; Raju, U.; Liao, Z.; Ajani, J. Targeting molecular determinants of tumor chemo-radioresistance. Semin. Oncol. 2005, 32, S78-S81. (Pubitemid 43080922)
119. Lou, H.; Dean, M. Targeted therapy for cancer stem cells: the patched pathway and ABC transporters. Oncogene 2007, 26, 1357-1360. (Pubitemid 46328461)
120. Zhang, Q.; Chen, G.; Liu, X.; Qian, Q. Monoclonal antibodies as therapeutic agents in oncology and antibody gene therapy. Cell Res. 2007, 17, 89-99.
121. Calabrese, C.; Poppleton, H.; Kocak, M.; Hogg, T. L.; Fuller, C.; Hamner, B.; Oh, E. Y.; Gaber, M. W.; Finklestein, D.; Allen, M.; Frank, A.; Bayazitov, I. T.; Zakherenko, S. S.; Gajjar, A.; Davidoff, A.; Gilbertson, R. J. A perivascular niche for brain tumor stem cells. Cancer Cell 2007, 11, 69-82. (Pubitemid 46054518)
122. Monzani, E.; La Porta, C. A. M. Targeting cancer stem cells to modulate alternative vascularization mechanisms. Stem Cell Rev. 2008, 4, 51-56.
123. Sozzani, S.; Rusnati, M.; Riboldi, E.; Mitola, S.; Presta, M. Dendritic cell-endothelial cell cross-talk in angiogenesis. Trends Immunol. 2007, 28, 385-392.
124. Scavelli, C.; Nico, B.; Cirulli, T.; Ria, R.; Di Pietro, G.; Mangieri, D.; Bacigalupo, A.; Mangialardi, G.; Coluccia, A. M.; Caravita, T.; Molica, S.; Ribatti, D.; Dammacco, F.; Vacca, A. Vasculogenic mimicry by bone marrow macrophages in patients with multiple myeloma. Oncogene 2008, 27, 663-674.