The Role of Cdk5 in Neuroendocrine Thyroid Cancer

Cancer Cell

Volumn 24, Issue 4, 2013, Pages 499-511

  Pozo, Karine ^a   Castro Rivera, Emely ^a   Tan, Chunfeng ^a   Plattner, Florian ^a   Schwach, Gert ^b   Siegl, Veronika ^b   Meyer, Douglas ^a   Guo, Ailan ^c   Gundara, Justin ^d   Mettlach, Gabriel ^a   Richer, Edmond ^e   Guevara, Jonathan A ^e   Ning, Li ^f   Gupta, Anjali ^e   Hao, Guiyang ^e   Tsai, Li Huei ^g   Sun, Xiankai ^e   Antich, Pietro ^e   Sidhu, Stanley ^d   Robinson, Bruce G ^d   Chen, Herbert ^f   Nwariaku, Fiemu E ^e,h   Pfragner, Roswitha ^b   Richardson, James A ^a,e   Bibb, James A ^a,e,h   more..

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b MEDICAL UNIVERSITY OF GRAZ   (Austria)

^c CELL SIGNALING TECHNOLOGY   (United States)

^d UNIVERSITY OF SYDNEY   (Australia)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^f UNIVERSITY OF WISCONSIN   (United States)

^g MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^h UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 5; PROTEIN P25; PROTEIN P35; RETINOBLASTOMA PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CELL HYPERPLASIA; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE OVEREXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEOMICS; THYROID MEDULLARY CARCINOMA; TUMOR GROWTH;

EID: 84885360915     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2013.08.027     Document Type: Article

References (72)

1. Agrawal N., Jiao Y., Sausen M., Leary R., Bettegowda C., Roberts N.J., Bhan S., Ho A.S., Khan Z., Bishop J., et al. Exomic sequencing of medullary thyroid cancer reveals dominant and mutually exclusive oncogenic mutations in RET and RAS. J.Clin. Endocrinol. Metab. 2013, 98:E364-E369.
2. Angelo M., Plattner F., Giese K.P. Cyclin-dependent kinase 5 in synaptic plasticity, learning and memory. J. Neurochem. 2006, 99:353-370.
3. Asai N., Jijiwa M., Enomoto A., Kawai K., Maeda K., Ichiahara M., Murakumo Y., Takahashi M. RET receptor signaling: dysfunction in thyroid cancer and Hirschsprung's disease. Pathol. Int. 2006, 56:164-172.
4. Berger C.L., de Bustros A., Roos B.A., Leong S.S., Mendelsohn G., Gesell M.S., Baylin S.B. Human medullary thyroid carcinoma in culture provides a model relating growth dynamics, endocrine cell differentiation, and tumor progression. J.Clin. Endocrinol. Metab. 1984, 59:338-343.
5. Bibb J.A., Snyder G.L., Nishi A., Yan Z., Meijer L., Fienberg A.A., Tsai L.H., Kwon Y.T., Girault J.A., Czernik A.J., et al. Phosphorylation of DARPP-32 by Cdk5 modulates dopamine signalling in neurons. Nature 1999, 402:669-671.
6. Boichard A., Croux L., Al Ghuzlan A., Broutin S., Dupuy C., Leboulleux S., Schlumberger M., Bidart J.M., Lacroix L. Somatic RAS mutations occur in a large proportion of sporadic RET-negative medullary thyroid carcinomas and extend to a previously unidentified exon. J.Clin. Endocrinol. Metab. 2012, 97:E2031-E2035.
7. Bracken A.P., Ciro M., Cocito A., Helin K. E2F target genes: unraveling the biology. Trends Biochem. Sci. 2004, 29:409-417.
8. Chellappan S.P., Hiebert S., Mudryj M., Horowitz J.M., Nevins J.R. The E2F transcription factor is a cellular target for the RB protein. Cell 1991, 65:1053-1061.
9. Chen J., Kelz M.B., Zeng G., Sakai N., Steffen C., Shockett P.E., Picciotto M.R., Duman R.S., Nestler E.J. Transgenic animals with inducible, targeted gene expression in brain. Mol. Pharmacol. 1998, 54:495-503.
10. Ciampi R., Mian C., Fugazzola L., Cosci B., Romei C., Barollo S., Cirello V., Bottici V., Marconcini G., Rosa P.M., et al. Evidence of a low prevalence of RAS mutations in a large medullary thyroid cancer series. Thyroid 2013, 23:50-57.
11. Cranston A.N., Ponder B.A. Modulation of medullary thyroid carcinoma penetrance suggests the presence of modifier genes in a RET transgenic mouse model. Cancer Res. 2003, 63:4777-4780.
12. Cruz J.C., Tseng H.C., Goldman J.A., Shih H., Tsai L.-H. Aberrant Cdk5 activation by p25 triggers pathological events leading to neurodegeneration and neurofibrillary tangles. Neuron 2003, 40:471-483.
13. Dar A.C., Das T.K., Shokat K.M., Cagan R.L. Chemical genetic discovery of targets and anti-targets for cancer polypharmacology. Nature 2012, 486:80-84.
14. DeGregori J., Leone G., Miron A., Jakoi L., Nevins J.R. Distinct roles for E2F proteins in cell growth control and apoptosis. Proc. Natl. Acad. Sci. USA 1997, 94:7245-7250.
15. Demelash A., Rudrabhatla P., Pant H.C., Wang X., Amin N.D., McWhite C.D., Naizhen X., Linnoila R.I. Achaete-scute homologue-1 (ASH1) stimulates migration of lung cancer cells through Cdk5/p35 pathway. Mol. Biol. Cell 2012, 23:2856-2866.
16. Feldmann G., Mishra A., Hong S.M., Bisht S., Strock C.J., Ball D.W., Goggins M., Maitra A., Nelkin B.D. Inhibiting the cyclin-dependent kinase CDK5 blocks pancreatic cancer formation and progression through the suppression of Ras-Ral signaling. Cancer Res. 2010, 70:4460-4469.
17. Fialkowski E.A., Moley J.F. Current approaches to medullary thyroid carcinoma, sporadic and familial. J.Surg. Oncol. 2006, 94:737-747.
18. Flicker K., Ulz P., Höger H., Zeitlhofer P., Haas O.A., Behmel A., Buchinger W., Scheuba C., Niederle B., Pfragner R., Speicher M.R. High-resolution analysis of alterations in medullary thyroid carcinoma genomes. Int. J. Cancer 2012, 131:E66-E73.
19. Futatsugi A., Utreras E., Rudrabhatla P., Jaffe H., Pant H.C., Kulkarni A.B. Cyclin-dependent kinase 5 regulates E2F transcription factor through phosphorylation of Rb protein in neurons. Cell Cycle 2012, 11:1603-1610.
20. Goodyear S., Sharma M.C. Roscovitine regulates invasive breast cancer cell (MDA-MB231) proliferation and survival through cell cycle regulatory protein cdk5. Exp. Mol. Pathol. 2007, 82:25-32.
21. Hamdane M., Bretteville A., Sambo A.V., Schindowski K., Bégard S., Delacourte A., Bertrand P., Buée L. p25/Cdk5-mediated retinoblastoma phosphorylation is an early event in neuronal cell death. J.Cell Sci. 2005, 118:1291-1298.
22. Harbour J.W., Luo R.X., Dei Santi A., Postigo A.A., Dean D.C. Cdk phosphorylation triggers sequential intramolecular interactions that progressively block Rb functions as cells move through G1. Cell 1999, 98:859-869.
23. Harrison D.J., Hooper M.L., Armstrong J.F., Clarke A.R. Effects of heterozygosity for the Rb-1t19neo allele in the mouse. Oncogene 1995, 10:1615-1620.
24. Harvey M., Vogel H., Lee E.Y., Bradley A., Donehower L.A. Mice deficient in both p53 and Rb develop tumors primarily of endocrine origin. Cancer Res. 1995, 55:1146-1151.
25. Hu M.I., Cote G.J. Medullary thyroid carcinoma: who's on first?. Thyroid 2012, 22:451-453.
26. Huang C., Rajfur Z., Yousefi N., Chen Z., Jacobson K., Ginsberg M.H. Talin phosphorylation by Cdk5 regulates Smurf1-mediated talin head ubiquitylation and cell migration. Nat. Cell Biol. 2009, 11:624-630.
27. Jiang H., Luo S., Li H. Cdk5 activator-binding protein C53 regulates apoptosis induced by genotoxic stress via modulating the G2/M DNA damage checkpoint. J.Biol. Chem. 2005, 280:20651-20659.
28. Kaczirek K., Schindl M., Weinhäusel A., Scheuba C., Passler C., Prager G., Raderer M., Hamilton G., Mittlböck M., Siegl V., et al. Cytotoxic activity of camptothecin and paclitaxel in newly established continuous human medullary thyroid carcinoma cell lines. J.Clin. Endocrinol. Metab. 2004, 89:2397-2401.
29. Karran E., Palmer A.M. Neurodegenerative disorders and their treatment. Drug News Perspect. 2007, 20:407-412.
30. Kedzia C., Lacroix L., Ameur N., Ragot T., Kelly P.A., Caillou B., Binart N. Medullary thyroid carcinoma arises in the absence of prolactin signaling. Cancer Res. 2005, 65:8497-8503.
31. Kim E., Chen F., Wang C.C., Harrison L.E. CDK5 is a novel regulatory protein in PPARgamma ligand-induced antiproliferation. Int. J. Oncol. 2006, 28:191-194.
32. Knostman K.A., Jhiang S.M., Capen C.C. Genetic alterations in thyroid cancer: the role of mouse models. Vet. Pathol. 2007, 44:1-14.
33. Knudsen K.E., Fribourg A.F., Strobeck M.W., Blanchard J.M., Knudsen E.S. Cyclin A is a functional target of retinoblastoma tumor suppressor protein-mediated cell cycle arrest. J.Biol. Chem. 1999, 274:27632-27641.
34. Kusakawa G., Saito T., Onuki R., Ishiguro K., Kishimoto T., Hisanaga S. Calpain-dependent proteolytic cleavage of the p35 cyclin-dependent kinase 5 activator to p25. J.Biol. Chem. 2000, 275:17166-17172.
35. Lagace D.C., Benavides D.R., Kansy J.W., Mapelli M., Greengard P., Bibb J.A., Eisch A.J. Cdk5 is essential for adult hippocampal neurogenesis. Proc. Natl. Acad. Sci. USA 2008, 105:18567-18571.
36. Leung S.W., Wloga E.H., Castro A.F., Nguyen T., Bronson R.T., Yamasaki L. A dynamic switch in Rb+/- mediated neuroendocrine tumorigenesis. Oncogene 2004, 23:3296-3307.
37. Lilja L., Yang S.N., Webb D.L., Juntti-Berggren L., Berggren P.O., Bark C. Cyclin-dependent kinase 5 promotes insulin exocytosis. J.Biol. Chem. 2001, 276:34199-34205.
38. Lin H., Chen M.C., Chiu C.Y., Song Y.M., Lin S.Y. Cdk5 regulates STAT3 activation and cell proliferation in medullary thyroid carcinoma cells. J.Biol. Chem. 2007, 282:2776-2784.
39. Liska J., Altanerova V., Galbavy S., Stvrtina S., Brtko J. Thyroid tumors: histological classification and genetic factors involved in the development of thyroid cancer. Endocr. Regul. 2005, 39:73-83.
40. Lopes J.P., Agostinho P. Cdk5: multitasking between physiological and pathological conditions. Prog. Neurobiol. 2011, 94:49-63.
41. Massoll N., Mazzaferri E.L. Diagnosis and management of medullary thyroid carcinoma. Clin. Lab. Med. 2004, 24:49-83.
42. Meyer D.A., Richer E., Benkovic S.A., Hayashi K., Kansy J.W., Hale C.F., Moy L.Y., Kim Y., O'Callaghan J.P., Tsai L.H., et al. Striatal dysregulation of Cdk5 alters locomotor responses to cocaine, motor learning, and dendritic morphology. Proc. Natl. Acad. Sci. USA 2008, 105:18561-18566.
43. Nevins J.R. The Rb/E2F pathway and cancer. Hum. Mol. Genet. 2001, 10:699-703.
44. Nikitin A.Y., Juárez-Pérez M.I., Li S., Huang L., Lee W.H. RB-mediated suppression of spontaneous multiple neuroendocrine neoplasia and lung metastases in Rb+/- mice. Proc. Natl. Acad. Sci. USA 1999, 96:3916-3921.
45. Pang Z.P., Südhof T.C. Cell biology of Ca2+-triggered exocytosis. Curr. Opin. Cell Biol. 2010, 22:496-505.
46. Panickar K.S., Nonner D., White M.G., Barrett J.N. Overexpression of Cdk5 or non-phosphorylatable retinoblastoma protein protects septal neurons from oxygen-glucose deprivation. Neurochem. Res. 2008, 33:1852-1858.
47. Pfragner R., Höfler H., Behmel A., Ingolic E., Walser V. Establishment and characterization of continuous cell line MTC-SK derived from a human medullary thyroid carcinoma. Cancer Res. 1990, 50:4160-4166.
48. Pfragner R., Wirnsberger G., Behmel A., Wolf G., Passath A., Ingolic E., Adamiker D., Schauenstein K. New continuous cell-line from human medullary-thyroid carcinoma - sinj - phenotypic analysis and in vivo carcinogenesis. Int. J. Oncol. 1993, 2:831-836.
49. Pfragner R., Wirnsberger G.H., Ingolic E., Niederle B. Medullary thyroid carcinomas in cell culture-models for future therapies. Wien. Klin. Wochenschr. 2002, 114:279-283.
50. Quintavalle M., Elia L., Price J.H., Heynen-Genel S., Courtneidge S.A. A cell-based high-content screening assay reveals activators and inhibitors of cancer cell invasion. Sci. Signal. 2011, 4:ra49.
51. Ruiz-Llorente S., Montero-Conde C., Milne R.L., Moya C.M., Cebrián A., Letón R., Cascón A., Mercadillo F., Landa I., Borrego S., et al. Association study of 69 genes in the ret pathway identifies low-penetrance loci in sporadic medullary thyroid carcinoma. Cancer Res. 2007, 67:9561-9567. Medullary Thyroid Carcinoma Clinical Group.
52. Rush J., Moritz A., Lee K.A., Guo A., Goss V.L., Spek E.J., Zhang H., Zha X.M., Polakiewicz R.D., Comb M.J. Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat. Biotechnol. 2005, 23:94-101.
53. Sadleir K.R., Vassar R. Cdk5 protein inhibition and Aβ42 increase BACE1 protein level in primary neurons by a post-transcriptional mechanism: implications of CDK5 as a therapeutic target for Alzheimer disease. J.Biol. Chem. 2012, 287:7224-7235.
54. Saito T., Konno T., Hosokawa T., Asada A., Ishiguro K., Hisanaga S. p25/cyclin-dependent kinase 5 promotes the progression of cell death in nucleus of endoplasmic reticulum-stressed neurons. J.Neurochem. 2007, 102:133-140.
55. Salon C., Merdzhanova G., Brambilla C., Brambilla E., Gazzeri S., Eymin B. E2F-1, Skp2 and cyclin E oncoproteins are upregulated and directly correlated in high-grade neuroendocrine lung tumors. Oncogene 2007, 26:6927-6936.
56. Schlumberger M., Carlomagno F., Baudin E., Bidart J.M., Santoro M. New therapeutic approaches to treat medullary thyroid carcinoma. Nat. Clin. Pract. Endocrinol. Metab. 2008, 4:22-32.
57. Sellers W.R., Rodgers J.W., Kaelin W.G. A potent transrepression domain in the retinoblastoma protein induces a cell cycle arrest when bound to E2F sites. Proc Natl Acad Sci U S A 1995, 92:11544-11548.
58. Sherman S.I. Lessons learned and questions unanswered from use of multitargeted kinase inhibitors in medullary thyroid cancer. Oral Oncol. 2013, 49:707-710.
59. Sippel R.S., Kunnimalaiyaan M., Chen H. Current management of medullary thyroid cancer. Oncologist 2008, 13:539-547.
60. Strock C.J., Park J.I., Nakakura E.K., Bova G.S., Isaacs J.T., Ball D.W., Nelkin B.D. Cyclin-dependent kinase 5 activity controls cell motility and metastatic potential of prostate cancer cells. Cancer Res. 2006, 66:7509-7515.
61. Takahashi M. The GDNF/RET signaling pathway and human diseases. Cytokine Growth Factor Rev. 2001, 12:361-373.
62. Takahashi C., Contreras B., Bronson R.T., Loda M., Ewen M.E. Genetic interaction between Rb and K-ras in the control of differentiation and tumor suppression. Mol. Cell. Biol. 2004, 24:10406-10415.
63. Takahashi C., Contreras B., Iwanaga T., Takegami Y., Bakker A., Bronson R.T., Noda M., Loda M., Hunt J.L., Ewen M.E. Nras loss induces metastatic conversion of Rb1-deficient neuroendocrine thyroid tumor. Nat. Genet. 2006, 38:118-123.
64. van Veelen W., Klompmaker R., Gloerich M., van Gasteren C.J., Kalkhoven E., Berger R., Lips C.J., Medema R.H., Höppener J.W., Acton D.S. P18 is a tumor suppressor gene involved in human medullary thyroid carcinoma and pheochromocytoma development. Int. J. Cancer 2009, 124:339-345.
65. Wei F.Y., Nagashima K., Ohshima T., Saheki Y., Lu Y.F., Matsushita M., Yamada Y., Mikoshiba K., Seino Y., Matsui H., Tomizawa K. Cdk5-dependent regulation of glucose-stimulated insulin secretion. Nat. Med. 2005, 11:1104-1108.
66. Weinberg R.A. The retinoblastoma protein and cell cycle control. Cell 1995, 81:323-330.
67. Wells S.A., Robinson B.G., Gagel R.F., Dralle H., Fagin J.A., Santoro M., Baudin E., Elisei R., Jarzab B., Vasselli J.R., et al. Vandetanib in patients with locally advanced or metastatic medullary thyroid cancer: a randomized, double-blind phase III trial. J.Clin. Oncol. 2012, 30:134-141.
68. Wen Y., Planel E., Herman M., Figueroa H.Y., Wang L., Liu L., Lau L.F., Yu W.H., Duff K.E. Interplay between cyclin-dependent kinase 5 and glycogen synthase kinase 3 beta mediated by neuregulin signaling leads to differential effects on tau phosphorylation and amyloid precursor protein processing. J.Neurosci. 2008, 28:2624-2632.
69. Williams B.O., Remington L., Albert D.M., Mukai S., Bronson R.T., Jacks T. Cooperative tumorigenic effects of germline mutations in Rb and p53. Nat. Genet. 1994, 7:480-484.
70. Yamasaki L., Bronson R., Williams B.O., Dyson N.J., Harlow E., Jacks T. Loss of E2F-1 reduces tumorigenesis and extends the lifespan of Rb1(+/-)mice. Nat. Genet. 1998, 18:360-364.
71. Ye L., Santarpia L., Cote G.J., El-Naggar A.K., Gagel R.F. High resolution array-comparative genomic hybridization profiling reveals deoxyribonucleic acid copy number alterations associated with medullary thyroid carcinoma. J.Clin. Endocrinol. Metab. 2008, 93:4367-4372.
72. Ziebold U., Lee E.Y., Bronson R.T., Lees J.A. E2F3 loss has opposing effects on different pRB-deficient tumors, resulting in suppression of pituitary tumors but metastasis of medullary thyroid carcinomas. Mol. Cell. Biol. 2003, 23:6542-6552.