CaMKK2: A novel target for shaping the androgen-regulated tumor ecosystem

Trends in Molecular Medicine

Volumn 19, Issue 2, 2013, Pages 83-88

  Racioppi, Luigi ^a,b  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Androgen receptor; CaMKK2; Cancer therapy; Inflammation; Macrophage; Prostate cancer

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR ANTAGONIST; ARN509; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE KINASE; CYCLIN D1; ENZALUTAMIDE; PROSTATE SPECIFIC ANTIGEN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ADENOCARCINOMA; BREAST CANCER; CANCER GROWTH; CARCINOGENESIS; CASTRATION RESISTANT PROSTATE CANCER; CELL ENERGY; ENERGY BALANCE; HUMAN; INTRACELLULAR SIGNALING; MACROPHAGE ACTIVATION; NEOPLASM; NONHUMAN; PROTEIN EXPRESSION; REVIEW; TUMOR MICROENVIRONMENT;

ANDROGENS; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; HUMANS; MACROPHAGE ACTIVATION; MACROPHAGES; MALE; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; SIGNAL TRANSDUCTION;

EID: 84873169147     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2012.12.004     Document Type: Review

References (72)

1. Lonergan P.E., Tindall D.J. Androgen receptor signaling in prostate cancer development and progression. J. Carcinog. 2011, 10:20.
2. Garay J.P., Park B.H. Androgen receptor as a targeted therapy for breast cancer. Am. J. Cancer Res. 2012, 2:434-445.
3. Wang Q., et al. Androgen receptor regulates a distinct transcription program in androgen-independent prostate cancer. Cell 2009, 138:245-256.
4. Wang Q., et al. A hierarchical network of transcription factors governs androgen receptor-dependent prostate cancer growth. Mol. Cell 2007, 27:380-392.
5. Ryan C.J., Tindall D.J. Androgen receptor rediscovered: the new biology and targeting the androgen receptor therapeutically. J. Clin. Oncol. 2011, 29:3651-3658.
6. Attar R.M., et al. Discovery of BMS-641988, a novel and potent inhibitor of androgen receptor signaling for the treatment of prostate cancer. Cancer Res. 2009, 69:6522-6530.
7. Attard G., et al. Selective inhibition of CYP17 with abiraterone acetate is highly active in the treatment of castration-resistant prostate cancer. J. Clin. Oncol. 2009, 27:3742-3748.
8. Tran C., et al. Development of a second-generation antiandrogen for treatment of advanced prostate cancer. Science 2009, 324:787-790.
9. Snoek R., et al. In vivo knockdown of the androgen receptor results in growth inhibition and regression of well-established, castration-resistant prostate tumors. Clin. Cancer Res. 2009, 15:39-47.
10. Berridge M.J., et al. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 2003, 4:517-529.
11. 2+/CaM-dependent kinases: from activation to function. Annu. Rev. Pharmacol. Toxicol. 2001, 41:471-505.
12. Soderling T.R. The Ca-calmodulin-dependent protein kinase cascade. Trends Biochem. Sci. 1999, 24:232-236.
13. Racioppi L., Means A.R. Calcium/calmodulin-dependent protein kinase kinase 2: roles in signaling and pathophysiology. J. Biol. Chem. 2012, 287:31658-31665.
14. Racioppi L., Means A.R. Calcium/calmodulin-dependent kinase IV in immune and inflammatory responses: novel routes for an ancient traveller. Trends Immunol. 2008, 29:600-607.
15. Hawley S.A., et al. Calmodulin-dependent protein kinase kinase-β is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab. 2005, 2:9-19.
16. 2+/calmodulin-dependent protein kinase kinase-β acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab. 2005, 2:21-33.
17. 2+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases. J. Biol. Chem. 2005, 280:29060-29066.
18. Hardie D.G., et al. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell Biol. 2012, 13:251-262.
19. Anderson K.A., et al. Hypothalamic CaMKK2 contributes to the regulation of energy balance. Cell Metab. 2008, 7:377-388.
20. Hoyer-Hansen M., et al. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-β, and Bcl-2. Mol. Cell 2007, 25:193-205.
21. Nelson P.S., et al. The program of androgen-responsive genes in neoplastic prostate epithelium. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:11890-11895.
22. Frigo D.E., et al. CaM kinase kinase β-mediated activation of the growth regulatory kinase AMPK is required for androgen-dependent migration of prostate cancer cells. Cancer Res. 2011, 71:528-537.
23. Massie C.E., et al. The androgen receptor fuels prostate cancer by regulating central metabolism and biosynthesis. EMBO J. 2011, 30:2719-2733.
24. 2+/calmodulin-dependent protein kinase kinase 2 (CaMKK2) and the androgen receptor in prostate cancer progression. J. Biol. Chem. 2012, 287:24832-24843.
25. Shima T., et al. Down-regulation of calcium/calmodulin-dependent protein kinase kinase 2 by androgen deprivation induces castration-resistant prostate cancer. Prostate 2012, 72:1789-1801.
26. 2+/calmodulin-dependent protein kinase kinase. J. Biol. Chem. 2002, 277:15813-15818.
27. Pollard J.W. Trophic macrophages in development and disease. Nat. Rev. Immunol. 2009, 9:259-270.
28. Medzhitov R. Inflammation 2010: new adventures of an old flame. Cell 2010, 140:771-776.
29. Kawai T., Akira S. TLR signaling. Semin. Immunol. 2007, 19:24-32.
30. Galgani M., et al. Cyclic AMP modulates the functional plasticity of immature dendritic cells by inhibiting Src-like kinases through protein kinase A-mediated signaling. J. Biol. Chem. 2004, 279:32507-32514.
31. Napolitani G., et al. Activation of src-family tyrosine kinases by LPS regulates cytokine production in dendritic cells by controlling AP-1 formation. Eur. J. Immunol. 2003, 33:2832-2841.
32. Galgani M., et al. Helicobacter pylori induces apoptosis of human monocytes but not monocyte-derived dendritic cells: role of the cag pathogenicity island. Infect. Immun. 2004, 72:4480-4485.
33. Zanoni I., Granucci F. Regulation of antigen uptake, migration, and lifespan of dendritic cell by Toll-like receptors. J. Mol. Med. (Berl.) 2010, 88:873-880.
34. Illario M., et al. Calmodulin-dependent kinase IV links Toll-like receptor 4 signaling with survival pathway of activated dendritic cells. Blood 2008, 111:723-731.
35. Ostuni R., et al. Deciphering the complexity of Toll-like receptor signaling. Cell. Mol. Life Sci. 2010, 67:4109-4134.
36. Kawai T., Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 2011, 34:637-650.
37. Teng E.C., et al. A cell-intrinsic role for CaMKK2 in granulocyte lineage commitment and differentiation. J. Leukoc. Biol. 2011, 90:897-909.
38. Racioppi L., et al. Calcium/calmodulin-dependent protein kinase kinase 2 regulates macrophage-mediated inflammatory responses. J. Biol. Chem. 2012, 287:11579-11591.
39. Nakaya H.I., et al. Systems biology of vaccination for seasonal influenza in humans. Nat. Immunol. 2011, 12:786-795.
40. 2+-induced regulation of ion channel and MAP kinase functions. Nature 1995, 376:737-745.
41. Okigaki M., et al. Pyk2 regulates multiple signaling events crucial for macrophage morphology and migration. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:10740-10745.
42. Stanzione R., et al. Variations of proline-rich kinase Pyk2 expression correlate with prostate cancer progression. Lab. Invest. 2001, 81:51-59.
43. Iiizumi M., et al. RhoC promotes metastasis via activation of the Pyk2 pathway in prostate cancer. Cancer Res. 2008, 68:7613-7620.
44. Zhang X., et al. Calcium/calmodulin-dependent protein kinase (CaMK) Iα mediates the macrophage inflammatory response to sepsis. J. Leukoc. Biol. 2011, 90:249-261.
45. Salminen A., et al. AMP-activated protein kinase inhibits NF-κB signaling and inflammation: impact on healthspan and lifespan. J. Mol. Med. (Berl.) 2011, 89:667-676.
46. Yang Z., et al. Macrophage α1 AMP-activated protein kinase (α1AMPK) antagonizes fatty acid-induced inflammation through SIRT1. J. Biol. Chem. 2010, 285:19051-19059.
47. Yuk J.M., et al. The orphan nuclear receptor SHP acts as a negative regulator in inflammatory signaling triggered by Toll-like receptors. Nat. Immunol. 2011, 12:742-751.
48. Sag D., et al. Adenosine 5'-monophosphate-activated protein kinase promotes macrophage polarization to an anti-inflammatory functional phenotype. J. Immunol. 2008, 181:8633-8641.
49. Zanoni I., et al. CD14 regulates the dendritic cell life cycle after LPS exposure through NFAT activation. Nature 2009, 460:264-268.
50. Ivashkiv L.B. Cross-regulation of signaling by ITAM-associated receptors. Nat. Immunol. 2009, 10:340-347.
51. Wang L., et al. 'Tuning' of type I interferon-induced Jak-STAT1 signaling by calcium-dependent kinases in macrophages. Nat. Immunol. 2008, 9:186-193.
52. Turnbull I.R., Colonna M. Activating and inhibitory functions of DAP12. Nat. Rev. Immunol. 2007, 7:155-161.
53. Green M.F., et al. Characterization of the CaMKKβ-AMPK signaling complex. Cell. Signal. 2011, 23:2005-2012.
54. Alonso-Torre S.R., Trautmann A. Calcium responses elicited by nucleotides in macrophages. Interaction between two receptor subtypes. J. Biol. Chem. 1993, 268:18640-18647.
55. Hanley P.J., et al. Transient P2X7 receptor activation triggers macrophage death independent of Toll-like receptors 2 and 4, caspase-1, and pannexin-1 proteins. J. Biol. Chem. 2012, 287:10650-10663.
56. Paredes-Gamero E.J., et al. Calcium signaling as a regulator of hematopoiesis. Front. Biosci. (Elite Ed.) 2012, 4:1375-1384.
57. Chen G.Y., Nuñez G. Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 2010, 10:826-837.
58. Balkwill F.R., Mantovani A. Cancer-related inflammation: common themes and therapeutic opportunities. Semin. Cancer Biol. 2012, 22:33-40.
59. Gabrilovich D.I., et al. Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 2012, 12:253-268.
60. Kozin S.V., et al. Recruitment of myeloid but not endothelial precursor cells facilitates tumor regrowth after local irradiation. Cancer Res. 2010, 70:5679-5685.
61. Ahn G.O., et al. Inhibition of Mac-1 (CD11b/CD18) enhances tumor response to radiation by reducing myeloid cell recruitment. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:8363-8368.
62. Meng Y., et al. Blockade of tumor necrosis factor α signaling in tumor-associated macrophages as a radiosensitizing strategy. Cancer Res. 2010, 70:1534-1543.
63. Ammirante M., et al. B-cell-derived lymphotoxin promotes castration-resistant prostate cancer. Nature 2010, 464:302-305.
64. Luo J.L., et al. Nuclear cytokine-activated IKKα controls prostate cancer metastasis by repressing Maspin. Nature 2007, 446:690-694.
65. Nonomura N., et al. Infiltration of tumour-associated macrophages in prostate biopsy specimens is predictive of disease progression after hormonal therapy for prostate cancer. BJU Int. 2011, 107:1918-1922.
66. Azevedo A., et al. IL-6/IL-6R as a potential key signaling pathway in prostate cancer development. World J. Clin. Oncol. 2011, 2:384-396.
67. Zhu P., et al. Macrophage/cancer cell interactions mediate hormone resistance by a nuclear receptor derepression pathway. Cell 2006, 124:615-629.
68. Yamaoka M., et al. Overcoming persistent dependency on androgen signaling after progression to castration-resistant prostate cancer. Clin. Cancer Res. 2010, 16:4319-4324.
69. Lai J.J., et al. Androgen receptor influences on body defense system via modulation of innate and adaptive immune systems: lessons from conditional AR knockout mice. Am. J. Pathol. 2012, 181:1504-1512.
70. Lai J.J., et al. Monocyte/macrophage androgen receptor suppresses cutaneous wound healing in mice by enhancing local TNF-α expression. J. Clin. Invest. 2009, 119:3739-3751.
71. Lu T., et al. Targeting androgen receptor to suppress macrophage-induced EMT and benign prostatic hyperplasia (BPH) development. Mol. Endocrinol. 2012, 26:1707-1715.
72. Chen Y., et al. Anti-androgens and androgen-depleting therapies in prostate cancer: new agents for an established target. Lancet Oncol. 2009, 10:981-991.